CDA Journal - October 2020: Dentistry and COVID-19 by California Dental Association

Journa C A L I F O R N I A

D E N TA L

A S S O C I AT I O N

Mouth-COVID Connection Dental Aerosols Face Masks and Respirators Teledentistry

Dentistry and

COVID-19

O C T O B E R 2020

Vol 48 Nº 10

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d e pa r t m e n t s

475 The Editor/Masters of Splatter 476 Letter to the Editor 477

Impressions

569 RM Matters/Business Controls Reduce Employee Theft

571 Regulatory Compliance/Teledentistry and HIPAA

573 Ethics/Food for Thought 574 Tech Trends

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f e at u r e s

481 A Slice of Time An introduction to the issue. Kerry K. Carney, DDS, CDE

485 The Mouth-COVID Connection: Il-6 Levels in Periodontal Disease — Potential Role in COVID-19-Related Respiratory Complications This article discusses the importance of oral hygiene and periodontal health for respiratory conditions and how COVID-19 should not be underestimated. Shervin Molayem, DDS, and Carla Cruvinel Pontes, DDS, MsC, PhD

501 Decoding Dental Aerosols in the Age of COVID-19 This article discusses how the conflation with medical aerosols in the age of COVID-19 has created an inaccurate and potentially dangerous argument in dentistry. Anthony D. Mair, DDS, MCID; Paul H. Korne, DDS, MCID; and Mohamed-Nur Abdallah, BDS, MSc, PhD

507 Global Impact of COVID-19 on Service Delivery and Vulnerable Populations’ Access to Dental Care This paper provides an overview of the global impact of COVID-19 on dental professionals as well as highlights the barriers and challenges of global access to oral health care during the pandemic, especially among vulnerable populations. Francisco Ramos-Gomez, DDS, MS, MPH; Morenike Oluwatoyin Folayan, MBChD, MBA; Marcela Diaz-Betancourt, DDS, MIPH; Gyanendra Kumar, MDS; Thomas Gerhard Wolf, DMD; Margherita Fontana, DDS, PhD; and Guglielmo Campus, DDS, PhD C O N T I N U E S O N PAG E 4 73

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Journa C A L I F O R N I A

D E N TA L

published by the California Dental Association 1201 K St., 14th Floor Sacramento, CA 95814 800.232.7645 cda.org

CDA Officers Richard J. Nagy, DDS President president@cda.org

Volume 48 Number 10 October 2020

A S S O C I AT I O N

Management Peter A. DuBois Executive Director Carrie E. Gordon Chief Strategy Officer Kristine Allington Chief Marketing Officer

Jack F. Conley, DDS Editor Emeritus

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Journal of the California Dental Association Editorial Board

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The Journal of the California Dental Association (ISSN 1043–2256) is published monthly by the California Dental Association, 1201 K St., 14th Floor, Sacramento, CA 95814, 916.554.5950. The California Dental Association holds the copyright for all articles and artwork published herein.

Steven W. Friedrichsen, DDS, professor and dean, Western University of Health Sciences College of Dental Medicine, Pomona, Calif. Mina Habibian, DMD, MSc, PhD, associate professor of clinical dentistry, Herman Ostrow School of Dentistry of USC, Los Angeles Robert Handysides, DDS, dean and associate professor, department of endodontics, Loma Linda University School of Dentistry, Loma Linda, Calif. Bradley Henson, DDS, PhD , associate dean for research and biomedical sciences and associate professor, Western University of Health Sciences College of Dental Medicine, Pomona, Calif. Paul Krebsbach, DDS, PhD, dean and professor, section of periodontics, University of California, Los Angeles, School of Dentistry Jayanth Kumar, DDS, MPH, state dental director, Sacramento, Calif. Lucinda J. Lyon, BSDH, DDS, EdD, associate dean, oral health education, University of the Pacific, Arthur A. Dugoni School of Dentistry, San Francisco Nader A. Nadershahi, DDS, MBA, EdD, dean, University of the Pacific, Arthur A. Dugoni School of Dentistry, San Francisco Francisco Ramos-Gomez, DDS, MS, MPH, professor, section of pediatric dentistry and director, UCLA Center for Children’s Oral Health, University of California, Los Angeles, School of Dentistry Michael Reddy, DMD, DMSc, dean, University of California, San Francisco, School of Dentistry

The Journal of the California Dental Association is published under the supervision of CDA’s editorial staff. Neither the editorial staff, the editor, nor the association are responsible for any expression of opinion or statement of fact, all of which are published solely on the authority of the author whose name is indicated. The association reserves the right to illustrate, reduce, revise or reject any manuscript submitted. Articles are considered for publication on condition that they are contributed solely to the Journal of the California Dental Association. The association does not assume liability for the content of advertisements, nor do advertisements constitute endorsement or approval of advertised products or services.

Avishai Sadan, DMD, dean, Herman Ostrow School of Dentistry of USC, Los Angeles

Brian J. Swann, DDS, MPH, chief, oral health services, Cambridge Health Alliance; assistant professor, oral health policy and epidemiology, Harvard School of Dental Medicine, Boston

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Harold Slavkin, DDS, dean and professor emeritus, division of biomedical sciences, Center for Craniofacial Molecular Biology, Herman Ostrow School of Dentistry of USC, Los Angeles

Richard W. Valachovic, DMD, MPH, president emeritus, American Dental Education Association, Washington, D.C.

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517 Oral Pathology in the Context of COVID-19: Perspectives Based on a Compilation of Literature Data This literature review of the pandemic and its potential impact on dental practice makes it clear that in order to deal with COVID-19, the dental professional must stay current with its stomatological manifestations and its maxillofacial pathology. Paulo Victor Mendes Penafort, DDS; Tayná Figueiredo Maciel, DDS; Ana Paula Ferreira Souza, DDS; Tássia Caroline da Costa Mendes, DDS; Renata Gualberto Cunha, DDS, MSc; Naiza Menezes Medeiros Abrahim, DDS, MSc; Lucileide Castro Oliveira, DDS, MSc; Jeconias Câmara, DDS, MSc; Paulo Henrique Braz-Silva, DDS, PhD; and Tatiana Nayara Libório-Kimura, DDS, PhD

531 Face Masks and Respirators for the Dental Health Care Provider: A Review This article reviews the current respiratory protection devices used to minimize the risk of SARS-CoV-2 infection. Emma Bhaskar, BS

537 COVID-19: New Considerations for Respiratory Protection in Dental Practice This article discusses the use of powered air-purifying respirators (PAPRs) in dentistry now and in the post-COVID-19 future. Bruce L. Whitcher, DDS

545 Teledentistry 101: A Primer for Dental Professionals for the New Normal This article provides essential tips to launch teledentistry in your office for the new normal and the foreseeable future. Parvati Iyer, DDS; Shuba Anantha, DDS; Amy Griffith, DDS; and Casey Farrand, BS

553 Back-to-Practice Resources

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Editor

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Masters of Splatter Kerry K. Carney, DDS, CDE

asters of Splatter, if there were such a superhero title, it would belong to us. As Masters of Splatter, we harness the forces of good to combat the forces of infection that threaten our patients, our practices, our very lives. Comic books/graphic novels and superheroes allow us to think of our world in an allegorical or symbolic way. They make it easier to grapple with and analyze complex problems and interactions. What if we reinterpret how dentists reduce risk and combat infection using a superhero model? (Perhaps I have watched “Guardians of the Galaxy” too many times during the COVID-19 shutdown. But bear with me as I try to conceptualize a more symbolic image of how we reduce our risks of exposure to the virus that causes COVID-19 and the aerosols that are part of our everyday practice in dentistry.) In a superhero scenario, there should exist a supervillain. It is not much of a stretch to cast SARS-CoV-2, the virus that causes COVID-19, as that supervillain and COVID-19 as the global threat to life as we know it. Now picture the Dentist as the superhero. The Dentist is an everyday infection control warrior who may be unaware of their superpowers. It is in times of crisis, like the one we now experience, that superheroes discover and learn to master the powers they wield. Place our superhero into a version of Gotham City; we will call it the Practice. The Practice consists of four critical zones: ■ Zone 1: the oral cavity. ■ Zone 2: the 3-foot radius around the oral cavity.

The Dentist, the Master of Splatter, must endeavor to protect their patients, staff and community as well as themselves.

Zone 3: the operatory. Zone 4: the rest of the practice. These are the areas that our superhero must vigilantly protect from contamination by the virus. The Dentist has both a strategic battle plan and an arsenal of powerful weapons to deploy. Consider first the battle plan: the NIOSH Hierarchy of Hazard Control. For our purposes, the standard five-level inverted pyramid of feasible and effective control solutions will be modified into four levels. From top to bottom, these levels are: ■ Removal/substitution. ■ Engineering controls (isolating the hazard from people). ■ Administrative controls (changing the way people behave). ■ PPE (personal protective equipment, isolating people from the hazard). The inverted pyramid is a great visual aid to help us understand that the most effective controls are on the top and their impact is diminished as we progress from the top to the bottom. But back to our superhero. The Dentist, the Master of Splatter, must endeavor to protect their patients, staff and community as well as themselves. To this end, the Dentist first employs the power of removal. By designing and carrying out careful screening and temperature taking, the Dentist is trying ■ ■

to keep the villain virus from entering the Practice. If screening were 100% effective, the Dentist would not have to call on other powers of risk control. But as we know from other superhero scenarios, no superpower is 100% effective. In our case, asymptomatic virus shedding appears to be one way the virus can slip past this defense and enter the Practice undetected. Our Dentist’s next line of defense employs some of the most powerful engineering solutions. If the virus has succeeded in penetrating the Practice and resides in a patient’s oral cavity (Zone 1), then the goal must be to restrict the transmission from the oral cavity into the other zones of the Practice. To achieve this, our superhero must reduce the potential risks of aerosolizing the virus by way of rotary and ultrasonic instruments. When aerosol generation is unavoidable, the Dentist can call on tried-and-true sidekicks: the rubber dam and the powerful high-volume evacuator (HVE). The rubber dam restricts transmission by isolating the virus behind the latex shield. Every superhero could use a shield (think Captain America). The HVE acts as a powerful means of removing the potentially virus-laden aerosol at the source in that critical Zone 1. (Think Koshiro, an anime character whose superpower is vacuum forces that can draw in and rip his enemies to shreds.) OC TOBER 2 0 2 0 475

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In order to contain the potentially infectious aerosolized virus from fomite transmission, our superhero’s teammates, the Assistants, play a crucial role in cleaning and disinfecting the operatory before and after a patient procedure. Without the Assistants, the superhero guardian, the Dentist, would be doomed to failure in infection control. (Imagine here the slow-motion, synchronized, determined walk of the Dentist and the Assistants approaching the camera, Guardians-of-the-Galaxy style.) We have moved through the first and second levels of the inverted pyramid of hazard control solutions. The third level is administrative. This involves changing the way people behave. It requires everyone in the Practice to operate with common sense in following recommended protocols to reduce transmission. In some ways, this is the hardest power to deploy. Because, as in the words of that 18thcentury superhero Voltaire, “common sense is not very common.” Getting people to behave in a common-sense manner requires the superpowers of persuasion and consistency. Mandating that everyone in the practice wash their hands frequently, maintain physical distance and wear face coverings modifies behavior with the goal of reducing viral transmission. The Dentist will have to change some diagnostic and treatment behaviors as well. It will be necessary to choose nonaerosol-creating therapeutic interventions whenever possible. The use of silver diamide fluoride and minimally invasive procedures can help reduce the aerosol generation that can give COVID-19 wings. Finally, we come down to the ultimate, and least effective, weapon in our hero’s arsenal: PPE. In Marvel Comics, the last superpower 476 OC TOBER

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may not seem extraordinary at all. This pedestrian power is usually something like truth or love, but it usually overcomes evil by reinforcing humanity’s inherent goodness. In the case of the Dentist in the Practice, the last and least powerful of their risk controls is a barrier that prevents the hazard from contacting the vulnerable mucosal tissues and respiratory tract. If all the other hazard controls were 100% effective, the Dentist could provide surgical procedures in a T-shirt and shorts (or in our superhero’s case, in the Leotard of Justice). This last barrier between health and infection is critically important to stop that supervillain virus from inoculating the dental health care providers. However, PPE is not infallible. We cannot guarantee it will always protect us. To minimize risks, the Dentist must use the powers available across all levels of the inverted pyramid of hazard-control solutions. Consistent, effective teamwork in the performance of carefully designed and executed infection control plans is what protects our patients, our staff, our communities and ourselves. In the words of one of my favorite philosophers, Spiderman, “With great power comes great responsibility.” It is the Dentist who wields the power of effective hazard controls. These risk mitigations derive from years of experience and an everincreasing knowledge base rooted in the never-ending battle against infection. Who better than the Dentist, our superhero, to marshal the forces of good to combat the forces of evil? Who better than dentists to don the mantle of responsibility as infection control experts in the Practice and assume their rightful title as Masters of Splatter? We are the Masters of Splatter. n

Letter COVID-19 Pandemic: Need for Teleconsulting Module in Dental Education This letter is in response to the urgent need for incorporating a teleconsulting module in dental education during the COVID-19 pandemic. Broadly speaking, dentistry is viewed as a strict “handson” profession. But in reality, diagnostic work-up, prescription of medicines, referrals and follow-ups can be done via teleconsulting without delaying or degrading patient care. The COVID-19 pandemic has severely impacted health care practices and students in training in the educational institutions. Consequently, a surge in the use of teleconsulting to deliver patient care has been observed globally. Unfortunately, this does not hold true for most of the dental students who have been crippled in delivering patient care during the COVID-19 pandemic. This could have been prevented, in part, if students had already been introduced to teleconsulting during their education. That said, the need for integrating a teleconsulting module into the dental school curriculum is apparent and cannot be overemphasized. chitr a p. emperumal, bds, ms glenn t. clark, dds, ms

Herman Ostrow School of Dentistry of USC

Impressions

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Polymers in Water Eliminate Aerosols

Scaler using water in the dental setting: (a) initial state as the scaler initiates aerosolization of water blob in which it is submerged; (b) violent aerosolization with a stream of droplets; (c) pseudo-steady state. Scale bar: 1 mm. (Credit: Plog et al. Creative Commons license)

“It was amazing that these materials were capable of so easily and completely suppressing aerosolization by dental tools.” — ALEXANDER YARIN, DDS, PHD

The aerosol transmissibility of SARS-CoV-2 has created a high-risk situation in dentistry where the generation of aerosols is an unavoidable part of most dental therapies. But researchers from the University of Illinois at Chicago have found that forces of a vibrating tool or dentist’s drill are no match for the viscoelastic properties of food-grade polymers, such as polyacrylic acid, when the polymers are used as a small admixture to water in dental settings. The research team led by Alexander Yarin, PhD, created a two-part irrigation solution made up of water and a highmolecular weight, FDA-approved polymer that reduces or completely eliminates droplet formation by rotary and ultrasonic instruments used in dentistry. Not only did the admixture completely eliminate aerosolization, but it did so with ease, exhibiting the effectiveness of fundamental polymer physics such as coil-stretch transition, according to the study published in Physics of Fluids. Dr. Yarin and his research team tested two FDA-approved polymers. Polyacrylic acid proved more effective than xanthan gum because in addition to its high elongational viscosity (highelastic stresses in stretching), it revealed a relatively low-shear viscosity, which makes pumping it easy. “What was surprising is that the very first experiment in my lab completely proved the concept,” Dr. Yarin said. “It was amazing that these materials were capable of so easily and completely suppressing aerosolization by dental tools, with significant inertial forces involved. Nevertheless, the elastic forces generated by small polymer additives were stronger.” The study documented the violent explosion of pockets of water supplied to teeth and gums that the dental tool aerosolizes. The polymer admixture, when used to irrigate, suppresses bursts; instead, polymer macromolecules that stretch like rubber bands restrict water aerosolization. When the tip of a vibrating tool or dental drill plunges into polymer solution, the solution threads into snakelike strands, which are pulled back toward the tip of the tool, altering the usual dynamics seen with pure water in dentistry. “When droplets try to detach from a liquid body, the droplet tail is stretched. That’s where the significant elastic forces associated with the coil-stretch transition of polymer macromolecules come into play,” Dr. Yarin said. “They suppress tail elongation and pull the droplet back, completely preventing aerosolization.” The FDA-approved irrigation solutions introduced by this research reduce or completely eliminate aerosol generation, but they are not antiviral, antibacterial or intended to kill viruses or bacteria. Thus, clinical dentistry will still be required to use PPE to protect workers from natural aerosolization that occurs when breathing, speaking, coughing and sneezing. Learn more about this study in Physics of Fluids (2020); doi.org/10.1063/5.0021476.n OC TOBER 2 0 2 0 477

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Bacteria Form Biofilms Like Settlers Form Cities Ancient Teeth Hold History of Epidemics The earliest written records of tiny infectious organisms overhauling human societies stretch back as far as the Plague of Justinian in A.D. 541, which is thought to have killed up to 50 million people, or even the earlier Antonine Plague in A.D. 165, which left 5 million dead, according to an article in the Washington Post. But now, paleogenomics — a nascent field that studies DNA in remnants of ancient teeth — is rewriting the first chapter of humanity’s entanglement with diseases such as COVID-19 to thousands of years older than originally thought. Paleogenomics, which adapts highend medical tools similar to some now being used to track the coronavirus, has amounted to a “revolution” in understanding disease history, said Maria Spyrou, PhD, a microbiologist at the Max Planck Institute in Germany. “Where historical records are lacking, DNA evidence offers the possibility of filling in gaps, sometimes in surprising ways,” she said. “Until 2015, we thought that plague was maybe a 3,000-year-old disease.” Scientists and archaeologists now believe, however, that the plague bacteria, which caused the medieval Black Death that killed up to half of Europe’s population, infected humans roughly 5,000 years ago in the Stone Age. The bacteria, after it had entered the bloodstream and likely killed the host, circulated into the pulp chamber of teeth, which kept its DNA insulated from millennia of environmental wear. In the past decade, scientists have been able to extract and analyze that DNA. 478 OC TOBER

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Microbiologists have long adopted the language of human settlement to describe how bacteria live and grow: They “invade” and “colonize” and relations dwelling in close proximity are “colonies.” By pairing super-resolution imaging technology with a computational algorithm, a new study in Nature Communications confirms that this metaphor is more apt than scientists may have realized. The findings show that as individual bacteria multiply and grow into a dense and sticky biofilm, such as the community that forms dental plaque, their growth patterns and dynamics mirror those seen in the growth of cities. For the study, researchers used the microbe Streptococcus mutans. They distributed the bacteria on a tooth enamel-like material and followed hundreds of individual microbes during several hours as they divided and grew. Overall, the growth patterns were reminiscent of the formation of urban areas. Some individual “settlers” grew, expanding into small bacteria “villages.” Then, as the boundaries of the villages grew and, in some cases, met, they joined to form larger villages and eventually “cities.” Some of these cities then merged to form larger “megacities.” The researchers were surprised to find that only a subset of the bacteria grew — less than 40% — with the rest either dying off or being engulfed by the growth of other microcolonies. The authors caution that while the study is a useful analogy, it should be taken with a grain of salt. “We’re not saying these bacteria are anthropomorphic. But taking this perspective of biofilm growth gives us a multiscale, multidimensional picture of how they grow that we’ve not seen before,” they said. Learn more about this study in Nature Communications (2020); doi.org/10.1038/s41467-020-15165-4.

By tracking the growth of a biofilm with super-resolution imaging, researchers found similarities in how it formed that mimicked how urbanization occurs. (Credit: Amauri J. Paula/University of Pennsylvania)

In February, researchers at the day Russia, where archaeological evidence Massachusetts Institute of Technology has shown that humans began to abandon published evidence that types of Salmonella foraging for pastoral living. The Salmonella enterica, which sicken about a million DNA in their teeth is the first evidence people in the United States every year, that the adoption of this lifestyle in close were afflicting humans 6,500 years ago. contact with animals may have introduced Microbiologist Felix Key, PhD, identified pathogens to humans. Salmonella DNA in teeth recovered from Read more of this article in the burial sites near the Volga River in present- Washington Post.

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Periodontal Disease May Raise Cancer Risk People who have periodontal disease may have a higher risk of developing some forms of cancer, suggests a letter published in the journal Gut detailing a prospective study. Researchers found that a history of periodontal disease appeared to be associated with a raised risk of esophageal cancer and gastric cancer and this risk was also higher among people who had lost teeth previously.

The researchers from Harvard T.H. Chan School of Public Health in Boston carried out a study of data on patients over decades of follow-up. They examined the association of history of periodontal disease and tooth loss with the risk of esophageal and gastric cancer in 98,459 women from the Nurses’ Health Study (1992–2014) and 49,685

Atomic Imaging Reveals Tooth Decay A collaboration between researchers from Cornell University and Northwestern University combined complementary imaging techniques to explore the atomic structure of human enamel, exposing tiny chemical flaws in the fundamental building blocks of our teeth. The findings could help scientists prevent or possibly reverse tooth decay, according to the study. The team’s paper, “Chemical Gradients in Human Enamel Crystallites,” was published in July in the journal Nature. In recent years, Northwestern researchers imaged sensitive biological materials with atom probe tomography, a process that essentially strips atoms off a sample’s surface one at a time and reconstructs the structure of the material. At the same time, Cornell researchers have advanced a form of low-temperature electron microscopy that can image the atomic structure of radiation-sensitive samples. The technique can also safely map a sample’s chemical composition by measuring how much energy is lost when the electrons interact with the atoms. By combining their complementary techniques, the Cornell and Northwestern researchers were able to image an enamel crystallite and its hydroxylapatite atomic lattice. But all was not crystal clear: The lattice contained dark distortions caused by two nanometric layers with magnesium as well as sodium, fluoride and carbonate ion impurities near the core of the crystal. Additional modeling confirmed the irregularities are a source of strain in the crystallite. Paradoxically, these irregularities and the enamel’s core-shell architecture may also play a role in reinforcing the enamel, making it more resilient. Read more of this study in Nature (2020); doi.org/10.1038/s41586-020-2433-3. Impurities such as magnesium appeared as dark distortions (indicated by white arrows) in the atomic lattice of human enamel crystallites. (Credit: Paul Smeets/Northwestern University and Berit Goodge/Cornell University)

men from the Health Professionals Follow-Up Study (1988–2016). Dental measures, demographics, lifestyle and diet were assessed using follow-up questionnaires and selfreported cancer diagnosis was confirmed after reviewing medical records. The results showed that during 22 to 28 years of follow-up, there were 199 cases of esophageal cancer and 238 cases of gastric cancer. A history of periodontal disease was associated with a 43% and 52% increased risk of esophageal cancer and gastric cancer, respectively. Compared to people with no tooth loss, the risks of esophageal and gastric cancer for those who lost two or more teeth were also modestly higher — 42% and 33%, respectively. In addition, among individuals with a history of periodontal disease, no tooth loss and losing one or more teeth were equally associated with a 59% increased risk of esophageal cancer compared to those with no history of periodontal disease and no tooth loss. Similarly, the same group of individuals had 50% and 68% greater risk of gastric cancer, respectively. This was an observational study, so no firm conclusions can be drawn about cause and effect, and the researchers cannot rule out the possibility that some of the observed risk may be due to other unmeasured (confounding) factors. Learn more about the prospective study in Gut (2020); dx.doi.org/10.1136/ gutjnl-2020-321949. OC TOBER 2 0 2 0 479

introduction C D A J O U R N A L , V O L 4 8 , Nº 1 0

A Slice of Time Kerry K. Carney, DDS, CDE

hen you observe a fossil encased in the veneer stone of a marble wall, you are witnessing a slice of time. You may dismiss it as an ancient artifact. But it is a snapshot of the life of an organism in the context of its environment. To make the point clear, think of finding an old, yellowed photo of your grandparents at their wedding. You do not dismiss it as just a very old photo of a young couple related to you. Instead, you think of what was happening to them. What were they experiencing in that moment? You think of them in the context of their lives. This issue of the Journal of the California Dental Association is a slice of time. We are living in an interesting and rapidly changing environment. Data about the spread of the SARSCoV-2 virus and the tally of those who have succumbed to COVID-19 change daily. In this issue, we have compiled several articles detailing our current understanding of COVID-19; however, it goes without saying that figures cited in these pages will have changed by publication. Given the dynamic environment, the CDA Journal is being presented

as a slice of time. We know that in 18 months, five years or a decade from now the information we have gathered, processed and built on will be astounding. This event might even become a scientific watershed. We may categorize our knowledge of virology, epidemiology, public health and dental practice in terms of our pre-COVID-19 and post-COVID-19 understanding. This special COVID-19 issue is not only designed to update the contemporary reader but will serve as an archive for future researchers. This issue provides a context for how we reacted to this unfolding pandemic. The articles herein illustrate what we think we know at this time. Molayem et al. take a periodontal perspective in their article “The MouthCOVID Connection: Il-6 Levels in Periodontal Disease-Potential Role in COVID-19-Related Respiratory Complications.” In their review, they explore the association between periodontal therapy, serum IL-6 levels, systemic inflammatory activity and COVID-19 severity. Mair et al. in their article “Decoding Dental Aerosols in the Age of COVID-19” posit that dentistry has a strong record of effective dental aerosol mitigation and an overemphasis on dental aerosols OC TOBER 2 0 2 0 481

introduction C D A J O U R N A L , V O L 4 8 , Nº 1 0

may distract from the importance of preventing nonclinical transmission through physical distancing, face masks and optimized ventilation. The authors hypothesize that public confidence in the safety of dental office visits may be undermined as a result of the dental aerosol mitigation emphasis. “Global Impact of COVID-19 on Service Delivery and Vulnerable Populations’ Access to Dental Care” by Ramos-Gomez et al. helps us step back and see how other countries and their oral health care providers have been impacted by the pandemic. In addition, it underscores how this pandemic is making the environment even more difficult for those most at risk and reminds us that less-invasive treatment strategies may allow us to manage disease without using an aerosolproducing drill. In the article “Oral Pathology in the Context of COVID-19: Perspectives Based on a Compilation of Literature Data,” Libório-Kimura et al. provide a review of indexed articles related to SARS-CoV-2 over a six-month period. In addition, the authors review literature addressing relevant aspects that oral pathologists, stomatologists and general dentists need to be aware of in the context of the COVID-19 pandemic. Personal protective equipment has become a linchpin in this pandemic. Bhaskar has provided a review of face masks in her article entitled “Face Masks and Respirators for the Dental Health Care Provider.” The breakdown in the supply chain for acceptable, traditional masks has made our profession consider powered air-purifying respirators (PAPRs) as a potential replacement for the N95 when respiratory 482 OC TOBER

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protection is called for. In the article “COVID-19: New Considerations for Respiratory Protection in Dental Practice,” Whitcher discusses PAPRs and how they might fit into our standard PPE armamentarium in a post-COVID-19 future. Finally, Iyer et al.’s article “Teledentistry 101: A Primer for Dental Professionals for the New Normal” reviews teledentistry, a technological modification to our traditional practice. Teledentistry

Dental offices, though deemed essential, were advised to reduce the pressure on the supply of PPE by limiting patient treatment to only emergency care. can remove the risk of infection by eliminating or abbreviating some face-to-face interactions. In addition to these articles about COVID-19, we are using this issue of the CDA Journal to archive resources CDA developed and made available to members and nonmembers through this time of crisis. Early in March 2020, it became clear that SARS-CoV-2 transmission was a significant threat in America and throughout the world and authorities began recommending that health care prioritize vital services and protection of front-line health care workers. Dental offices, though deemed essential, were advised by government and public health officials to reduce the pressure on the supply of PPE by

limiting patient treatment to only emergency care. CDA turned its attention to supporting dentists and dentistry during this crisis. CDA President Richard Nagy, DDS, appointed a 15-member clinical care workgroup comprised of practicing general dentists and specialists, dental school deans and academicians and representatives from dental hygiene and dental assisting. The group was tasked with developing guidance for care during the pandemic. In particular, it was clear that heading back to practice after a prolonged break in normal operations and patient care would require significant changes. New patient- and staff-screening protocols and changes to office spaces and disinfection procedures would need to be developed, streamlined and disseminated. Co-chaired by Dr. Nagy and California State Dental Director Jayanth Kumar, DDS, MPH, this COVID-19 clinical care workgroup discussed issues of concern, sought answers to commonly asked questions, clarified areas of confusion and identified and developed helpful resources and training. Named “Back to Practice,” this special section of the CDA website continues to be updated regularly as information becomes available, but highlights of the work have been extracted from cda.org and are provided here for readers’reference. (These resources are updated frequently; the Back to Practice section in this issue was accessed Aug. 28, 2020.) n For full and free access to these Back-toPractice materials, visit cda.org/Home/ Practice/Back-to-Practice.

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periodontitis C D A J O U R N A L , V O L 4 8 , Nº 1 0

The Mouth-COVID Connection: Il-6 Levels in Periodontal Disease — Potential Role in COVID -19 -Related Respiratory Complications Shervin Molayem, DDS, and Carla Cruvinel Pontes, DDS, MsC, PhD

a b s t r a c t Researchers are combining efforts to better understand SARS-

CoV-2, and recent findings point to the importance of cytokine storms. Elevated interleukin-6 (IL-6) levels can predict COVID-19 pulmonary complications. Dental professionals play a significant role because periodontitis can increase IL-6 levels locally and systemically. Periodontal treatment has positive effects in systemic inflammation, and the importance of oral hygiene and periodontal health for respiratory conditions and COVID-19 should not be underestimated.

AUTHORS Shervin Molayem, DDS, earned his Doctor of Dental Surgery at the University of California, Los Angeles, School of Dentistry and completed a specialty program in periodontics at the Herman Ostrow School of Dentistry of USC. He is a periodontist in private practice in Los Angeles. Conflict of Interest Disclosure: None reported.

Carla Cruvinel Pontes, DDS, MsC, PhD, is a Brazilian dentist and researcher with a Master of Science degree in periodontology from the University of Sao Paulo and a doctorate in health sciences from the University of Copenhagen, Denmark. She works as an independent dental researcher and writer in Cape Town, South Africa. Conflict of Interest Disclosure: None reported.

esearchers around the world are combining efforts to increase our understanding of SARSCoV-2, and recent findings point to the potential role of cytokine storms in the severity of this viral infection. High interleukin-6 (IL-6) levels have been linked to significantly higher risk for pulmonary complications and increased need for mechanical ventilation in COVID-19 patients. As dental professionals try to establish a new normal in their practices, they play a significant role in decreasing transmission of the coronavirus and decreasing inflammation and IL-6 levels because periodontitis has been shown to increase cytokine levels locally and systemically. Periodontitis has been previously associated with increased

risk for respiratory conditions, such as chronic obstructive pulmonary disease (COPD), pneumonia and lung function, hence there is biological plausibility for a link between periodontitis, IL-6 levels and COVID-19-related pulmonary problems. The potential mechanisms behind this association include systemic inflammation, bacterial load, gut dysbiosis and endothelial function. Genetic variations in the IL-6 gene can also be a relevant risk factor for exacerbated inflammatory response. Findings from pneumonia studies showing lower rates of infection and mortality associated with plaque control suggest that dental care can have a major impact in the coronavirus disease course. Furthermore, for systemically healthy patients and those who have systemic OC TOBER 2 0 2 0 485

periodontitis C D A J O U R N A L , V O L 4 8 , Nº 1 0

conditions, periodontal treatment can decrease the burden of systemic inflammation, thus decreasing the risk for pulmonary complication due to COVID-19. Despite the lack of studies on this topic, the importance of oral hygiene and periodontal health for respiratory conditions and COVID-19 infections should not be underestimated. Dentists should promote screening, plaque control and periodontal treatment because a healthy periodontium can help decrease the severity and complications related to COVID-19.

salivary glands to function as reservoirs for COVID-19, the infectivity of saliva and occupational health issues due to the nature of dental treatments. With the reopening of dental practices during the pandemic, dental professionals are faced with challenges that range from strict infection control measures to a decrease in the number of patients willing to undergo dental treatments.6 In these extraordinary times, dental professionals might need to shift their focus to a general health and systemic inflammation approach.

Introduction

The global COVID-19 outbreak has caused a public health emergency crisis, as declared by the World Health Organization (WHO) in January 2020.1 While up to 80% of patients infected by SARS-CoV-2 recover after mild cold-like symptoms with no major complications, 20% can develop serious respiratory complications that can develop into acute respiratory distress syndrome due to the virus’ ability to infect human respiratory epithelial cells. Around 5% of COVID-19 patients require intensive care and mechanical ventilation.2 As researchers from different countries try to shed light on potential treatments and vaccines against the coronavirus, recent findings point to the potential role of cytokine storms in this viral infection, particularly IL-6.3–5 A recent study from Germany suggested that high IL-6 levels can be a powerful predictor of respiratory failure and the need for mechanical ventilation in hospitalized COVID-19 patients.4 Dental professionals have suffered the impact of COVID-19 in profound ways, which are directly related to the importance of the oral cavity as a transmission route, the potential for 486 OC TOBER

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Previous studies have linked periodontitis to respiratory conditions, with increased risk for complications and higher mortality rate in hospitalized patients. In this context, periodontitis has been linked to increased levels of proinflammatory cytokines, including IL-6, which is a recognized mediator in the periodontal destruction process.7 The ability of nonsurgical periodontal treatment to lower cytokine levels has been highlighted in the dental literature.8,9 Thus, lower IL-6 levels and inflammation resulting from periodontal treatment can potentially protect COVID-19 patients against lifethreatening respiratory complications. In fact, previous studies have linked periodontitis to respiratory conditions, with increased risk for complications and higher mortality rate in hospitalized patients.10 The impact of a connection between periodontal treatment, IL-6 levels, respiratory conditions and

COVID-19 can be powerful considering the high prevalence of periodontal disease in adults, the high transmission rate of SARS-CoV-2, the limited access to periodontal treatment during the pandemic and the shortage of health care resources related to hospitalized COVID-19 patients who require mechanical ventilation.11 The proposed biological mechanisms behind the link between periodontitis and increased risk for COVID-19 complications are presented in the FIGURE. In this review, the current state of knowledge on the scientific foundation for the connection between IL-6 levels and periodontitis, COVID-19 and respiratory diseases is presented, including the importance of this cytokine for periodontitis, viral infections and COVID-19, the effect of periodontal treatment in IL-6 levels, the biological link between periodontitis, respiratory problems and coronavirus disease. The clinical importance of this review lies in the awareness that dental professionals can have a major impact on the COVID-19 pandemic through promotion of periodontal health, considering the benefits of prevention and treatment of periodontal disease on overall health, including the prevention of complications resulting from the coronavirus.

IL-6 in Relation to Periodontitis

Periodontitis is characterized by an inflammatory process that results in destruction of the periodontium triggered by mediators derived from the adaptive and innate immune response to microorganisms in the biofilm.12 Cytokines are soluble proteins that attach to cell surfaces through specific receptors, regulating cell function and mediating complex cell interactions involved in periodontal destruction.

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Local inflammation

STRESS

Systemic inflammation

Aspiration oral bacteria

IL-6

DIRECT LINK HIGH IL-6

Bacteriemia

High blood levels inflammatory cytokines TNF-α, Il-1β, CRP

Endothelial dysfunction

COVID19 Gut dysbiosis

Changes - Lungs - Epithelium - Higher risk infection and complications

FIGURE . The link between periodontitis and increased risk for COVID-19 complications.

In periodontitis, cytokines cause (SNPs), resulting in different gene intracellular cascades and phenotypic versions or alleles. Cytokine SNPs changes that regulate the amplitude can influence risk and outcomes for and severity of the host response, with certain diseases, such as periodontitis, interleukin-1ß (IL-1ß), tumor necrosis by influencing secretion of these factor α (TNF-α) and IL-6 being the mediators, immune and inflammatory responses.15 The diversity in the most extensively investigated.13 IL-6 is a well-known proinflammatory clinical presentation of periodontitis cytokine secreted by a multitude of cells, has been partly attributed to genetic including monocytes, macrophages, nucleotide variations in the IL-6 endothelial cells, epithelial cells and gene, localized in chromosome 7.16 In B and T cells. In periodontitis, IL-6 is 2003, the first study associating an IL-6 crucial for regulation of the host response polymorphism (–174) to periodontitis to infection, injury and alveolar bone was published, and a protective effect resorption.14 The participation of IL-6 for allele C against periodontitis was in periodontal inflammation has been reported in a sample from Brazil.17 well described in the literature through The role of IL-6 polymorphisms genetic studies on IL-6 polymorphisms in the susceptibility to periodontitis and studies evaluating IL-6 expression has been explored in several other levels in serum, saliva, gingival crevicular studies, with different SNPs being fluid (GCF) and gingival tissues. Each investigated (–174, –572, –597, –373, of these categories is discussed below. –190, –1363, –6106, –1480, +874). A summary of published studies on Genetic Studies: IL-6 Polymorphisms IL-6 gene polymorphisms in patients with periodontitis is presented in and Risk for Periodontitis Polymorphisms deriving from one the TABLE . For the IL-6 gene, SNP base change in the genome are known –174 (promoter region) and –572 as single nucleotide polymorphisms (regulatory region) have been the most

investigated, and the majority of studies have found an association between these polymorphisms and the risk for periodontitis,17–28 which was confirmed in a recent meta-analysis.29 The SNP –163 was only evaluated in two studies, which reported a positive association with periodontitis.20,30 Two studies investigated IL-6 SNP –597, from which one found an association with periodontitis.31,32 The remaining IL-6 polymorphisms have been investigated to a lesser degree with varying results (TABLE) . Data on IL-6 gene variants suggest that SNP –174 allele C can protect against chronic and aggressive periodontitis, while allele G increases the risk. Likewise, for SNP –572, allele C seems to have a protective effect for chronic and aggressive periodontitis. The majority of these studies report on data from European, Asian and Brazilian participants, hence, further studies on different ethnic groups are warranted. The protective effect of the polymorphisms has been linked to lower serum IL-6 levels.32,33 The other IL-6 SNPs have been studied to a lesser degree, which is why their association to periodontitis needs to be further explored.

In Vitro Studies on IL-6 Expression in Periodontitis

High expression of IL-6 has been reported in inflamed gingival tissues, and human gingival fibroblasts are able to produce elevated IL-6 levels when exposed to polysaccharides (LPS) or IL-1.34,35 The role of IL-6 on periodontal bone destruction has been investigated through in vitro studies, which suggest that this cytokine is involved in osteoclastogenesis, a crucial process in alveolar bone destruction. IL-6 stimulates OC TOBER 2 0 2 0 487

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TABLE

Periodontal Studies on IL-6 Polymorphisms IL-6 SNPs

Association with periodontitis

Year of publication

Country

Diagnosis

Reference

–572

Yes

2019

China

Zhao et al.

–572

Yes

2017

Turkey

Toker et al.

–174, –572

Yes

2017

Brazil

Gorgun et al.

–174

Yes

2017

India

Kavitha et al.

–572

Yes

2017

China

Shi et al.

–174, –573

2016

Iran

Salman et al.

– 572

2014

China

Zhang et al.

–174

Yes

2014

Brazil

Teixeira et al.

–597

Yes

2014

India

Sharma et al.

–174

2014

India

Sharma et al.

–1363

Yes

2014

China

Zhang et al.

–572

2011

China

Zhang et al.

–174

2010

Turkey

Erciyas et al.

–572

Yes

2010

China

Jingjin et al.

–572, – 174

2009

Japan

Kobayashi et al.

–174

Yes

2009

England

AP and CP

Nibali et al.

–1480, –1363

Yes

2008

England

Nibali et al.

–6106

2008

England

Nibali et al.

–174

Yes

2007

Finland

Tervonen et al.

–174

Yes

2007

Brazil

AP and CP

Moreira et al.

–174

2006

Sweden

Jansson et al.

+874

2006

Germany

Babel et al.

–174

Yes

2006

Germany

Babel et al.

–174

2006

United States

Wohlfahrt et al.

–174

Yes

2005

England

AP and CP

Brett et al.

–373

Yes

2005

Japan

Komatsu et al.

–597, –572, –190, – 174

2005

Japan

Komatsu et al.

– 597, – 174

2004

Czech

Holla et al.

– 572

Yes

2004

Czech

Holla et al.

–174

Yes

2003

Brazil

Trevilato et al.

rs2069837

Yes

2016

Brazil

Farhat et al.

AP: aggressive periodontitis; CP: chronic periodontitis

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osteoclast formation and increases expression of receptor activator of nuclear factor-κB ligand (RANKL) in osteoblasts, being an essential mediator for osteoclast function and possibly osteoblast function.36,37 Additional in vitro studies have revealed that upregulation of matrix metalloproteinases (MMPs) is one of the mechanisms by which IL-6 causes periodontal destruction.35 IL-6 stimulates the production of MMP-1 in human gingival fibroblasts, which is a key protease in the process of tissue destruction due to its ability to degrade collagen and activate the fibrinolytic protease cascade.38 When CD4+ T-cells from gingival tissue and peripheral blood from periodontitis patients were exposed to Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans, upregulation of IL-6 levels was observed in comparison to healthy subjects.39 Similar responses were found in studies exposing monocytes or whole blood cells from periodontitis patients to LPS and/or periodontal pathogens where increased levels of IL-6 were consistently observed in cells from periodontitis patients compared to periodontally health patients. The main cellular sources for IL-6 secretion in the periodontium have been identified as macrophages, epithelial cells and T-cells.40,41 Collectively, data from in vitro studies have shown that T-cells, gingival fibroblasts, monocytes and peripheral mononuclear cells from gingiva and blood produce elevated IL-6 levels when stimulated by pathogens, LPS or other cytokines. Cells from periodontitis patients can express a different phenotype, characterized by higher IL-6 expression when compared to cells from

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periodontally healthy subjects. Once secreted, IL-6 mediates periodontal destruction through upregulation of MMPs and osteoclastogenesis.

IL-6 levels in Gingival Crevicular Fluid (GCF), Saliva, Gingival Tissues and Serum

As soluble proteins, cytokines produced in periodontal tissues can be detected in the GCF. A variety of studies have measured IL-6 levels in GCF, and despite some conflicting results, IL-6 levels seem to be higher in the GCF of periodontitis patients when compared to subjects with a healthy periodontium, according to a comprehensive meta-analysis.42 Doubled IL-6 levels have been reported in sites with refractory periodontitis when compared to stable periodontal sites.43 As another potential source for biomarkers, saliva has also been investigated for IL-6 levels, given the higher volume and easier access for sampling in comparison to GCF.44 Despite the fact that IL-6 salivary levels seem to be low in periodontal health and periodontitis, few studies have detected an increase in salivary IL-6 levels in the presence of periodontitis.45,46 In a recent clinical study by Batool and co-workers, IL-6 salivary levels increased with increasing severity of chronic periodontitis.47 However, several other studies have failed to detect differences in salivary IL-6 levels of periodontitis, suggesting that IL-6 might not be a strong biomarker for periodontitis in saliva.48,49 When compared to healthy gingival tissues, inflamed gingival tissues have shown higher IL-6 concentration through immunohistochemistry methods.50 In addition, increased IL-6

mRNA and protein expression have been observed in periodontitis patients when compared to periodontally healthy patients.51 A recent study on periodontitis patients reported gingival IL-6 levels ranging from 3 pg/ml to 13 pg/ml, with one patient presenting levels as high as 53.1 pg/ml.52 Serum levels of IL-6 in patients with periodontitis have been reported to be significantly higher than those for patients with a healthy periodontium, with values ranging from 0.25 pg/ml to 41.2 pg/ml in periodontitis.53 Similar results have been confirmed by other investigations on chronic and aggressive periodontitis.54,55 Interestingly, in a

The improvement in circulating IL-6 levels has been reported for systemically healthy patients and for patients with systemic conditions. clinical study from Almaghlouth and co-workers,56 the maximum serum IL-6 levels found in the periodontitis group was 216.3 pg/ml.

Impact of Periodontal Treatment on IL-6 Levels

D’Aiuto and co-workers (2004) investigated the effect of nonsurgical periodontal treatment in serum inflammatory markers in 94 systemically healthy participants presenting severe generalized periodontitis. A significant decrease in serum IL-6 (median decrease 0.2 ng/L) and CRP (median decrease 0.5 mg/L) was observed six months

after treatment.57 These findings were confirmed by other investigations, where serum levels of IL-6 were significantly reduced after conventional nonsurgical periodontal treatment in chronic periodontitis patients.53,58,59 Interestingly, Lobao et al. (2019) noted an average IL-6 reduction of 12 pg/ml three months after conventional periodontal treatment. In this study, even participants subjected to supragingival scaling and polishing (control group) presented significant serum IL-6 comparable to the test group, who received supra and subgingival scaling and root planing.60 In another study from D’Aiuto et al. (2006), conventional nonsurgical periodontal treatment was compared to intensive periodontal treatment in 40 systemically healthy participants. Intensive therapy, which included local antimicrobial agents, resulted in greater reductions of serum IL-6 and CRP after two and six months.61 A recent systematic review and meta-analysis evaluated the effect of periodontal therapy on IL-6 levels in patients with diabetes. When obese participants were excluded, the majority of studies reported a significant decrease in serum IL-6 levels in diabetics after periodontal treatment.62 Conventional periodontal therapy has also been shown to decrease IL-6 levels in patients with other systemic conditions, such as hypertension, metabolic syndrome, atherosclerosis and coronary heart disease.9,63,64 Altogether, these findings support a beneficial effect of periodontal therapy in serum IL-6 levels and in systemic inflammatory activity. The improvement in circulating IL-6 levels has been reported for systemically healthy patients and for patients with systemic conditions. OC TOBER 2 0 2 0 489

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Summary: IL-6 Significance for Oral Diseases and Periodontitis

There is strong evidence in the key role played by IL-6 in the immune and inflammatory response and bone resorption in periodontitis based on the following findings: ■ Genetic studies confirm that IL-6 polymorphisms can increase susceptibility to periodontitis. ■ In vitro studies confirm that IL-6 can be produced by a variety of cells in the periodontium, being a mediator for inflammation, host response and bone destruction. ■ IL-6 levels are upregulated locally in periodontal tissues, GCF and potentially in saliva in periodontitis patients with the potential to spread to the systemic circulation as confirmed by elevated serum levels of IL-6 in periodontitis patients. ■ Periodontal treatment can contribute to a decrease in local and circulating IL-6 levels in healthy individuals and in those who present systemic conditions. ■ Pulpitis and periapical lesions can be linked to increased expression of IL-6 as well as oral squamous cell carcinoma; however, these associations have been investigated to a lesser degree compared to periodontitis.

Respiratory Diseases, Pulmonary Function and Periodontitis COPD

COPD is a highly prevalent inflammatory condition affecting nearly 24 million Americans. It is among the leading causes of death in the U.S., being characterized by compromised pulmonary function, limited airflow and breathing problems.65 Observational studies have linked COPD to 490 OC TOBER

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periodontitis, and the association was supported by results from a metaanalysis by Zeng et al. (2012). In total, 14 studies and nearly 4,000 COPD patients were included, and the results showed a robust association between COPD and periodontitis with OR = 2.08 (1.48–2.91). The authors concluded that periodontitis is an independent risk factor for COPD.66 More recent data show increased prevalence of periodontitis in COPD patients who require hospitalization.67 Fewer remaining teeth, higher loss

Dental treatment to intensive care patients resulted in a dramatic reduction in the incidence of respiratory infections and ventilatorassociated pneumonia. of attachment and higher levels of inflammatory mediators in the GCF were reported in COPD patients.68

Pneumonia

Pneumonia is the infection of the pulmonary parenchyma, which can be caused by bacteria and viruses. It presents high mortality rates worldwide and often affects individuals with impaired immune systems, being usually classified as community-acquired or hospital-acquired (nosocomial).69 In a systematic review from Scannapieco et al. (2003) including nine randomized controlled trial (RCT) and 11 case-control studies, there was a significant association between nosocomial pneumonia and poor oral hygiene.70 In another systematic review, Azarpazhooh and Leake (2006) investigated

the association between oral health and respiratory diseases. Based on findings from 19 studies, the authors found good evidence to support a link between antimicrobial oral hygiene interventions and decreased incidence of pneumonia in nursing home patients.71 Data from several RCTs published since 2010 provide further evidence on the impact of poor oral hygiene and periodontitis in the incidence of nosocomial pneumonia in adults.72 In intensive care patients, oral swabbing with 0.2% chlorhexidine (CHX) decreased the rate of nosocomial infection.73 In patients scheduled for surgery for esophageal cancer, preoperative toothbrushing alone reduced the rate of postoperative pneumonia.74 In contrast, a study on nursing home patients failed to find reduction in pneumonia rates as a result of oral hygiene care interventions.75 Very interesting results were reported in one RCT, where comprehensive professional dental care provided by a dental surgeon in the intensive care unit was compared to routine oral hygiene offered by nurses. Dental treatment to intensive care patients (toothbrushing, tongue scraping, atraumatic caries treatment, removal of calculus and extractions) resulted in a dramatic reduction in the incidence of respiratory infections and ventilator-associated pneumonia. These results suggest that in hospitalized patients, intense dental therapy can help prevent respiratory infections.76

Pulmonary Function

In a case-control study from Peter et al. (2013), worse periodontal status was observed in COPD

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patients and associated with increased lung obstruction measured as forced expiratory volume in one second (FEV1).77 Another study investigated lung function in systemically healthy patients as part of the Study of Health in Pomerania, which included 1,463 subjects. Periodontal disease and number of missing teeth were positively associated with airflow limitation and reduced lung volume.78 Similar findings were reported in a recent large study based on the NHANES III data, where poorer pulmonary function was associated with increased severity of periodontitis in systemically healthy participants.79 In one interventional study on the effect of periodontal therapy on lung function, the authors compared three treatment groups (scaling and root planing, supragingival scaling and oral hygiene instructions alone) and concluded that the two therapy groups resulted in improved lung function, measured as FEV.80 A lack of correlation between pulmonary function and periodontitis has also been reported in one study.81

Asthma

Asthma is a prevalent chronic condition that can affect adults and children, characterized by alterations in the airways, bronchoconstriction and inflammation. Currently, there are contradictory results regarding a potential association of periodontitis and asthma.82 Two recent systematic reviews have addressed this association. The systematic review from Moraschini et al. (2017) included 21 studies on adults and children and the results showed increased gingival inflammation in asthmatic subjects in relation to systemically healthy individuals, which can be related to the use of inhalers, mouth breathing and decreased salivary

production.82 The other systematic review focused on adults with asthma (Ferreira et al. 2019) and, based on results from 11 studies, the authors concluded that there was increased prevalence of periodontal disease, particularly gingivitis, in adults with asthma.83 In a case-control study by SoledadeMarques and co-workers (2017), severe asthma was associated with periodontitis with adjusted OR = 3.01–3.25. Prevalence of periodontitis was higher in patients with severe asthma (46.6%) in comparison to systemically healthy controls (22.3%)

Mortality rates are higher for subjects presenting certain risk factors such as over age 70, respiratory disease, diabetes, cardiovascular disease and cancer. and periodontitis patients had a threefold increased risk of having severe asthma.84 Altogether, findings from most published studies on respiratory conditions and oral health suggest an association between periodontitis and COPD, pneumonia, worse lung function and potentially asthma. Oral hygiene interventions, dental and periodontal treatment are crucial to decrease the risk for nosocomial pneumonia and other respiratory conditions.

IL-6, Viral Infections and COVID-19

The coronavirus disease is caused by a new coronavirus, known as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), and due to high transmission rates, it has spread catastrophically in most

countries, including the U.S. The pandemic caused by the virus is unprecedented, according to the WHO, and has put a strain on primary health care systems around the world.85 Although most cases have been described as mild to moderate with self-limiting, cold-like symptoms or no symptoms, around 20% of patients can develop more severe complications that require hospitalization, of which approximately 5% need intensive care and mechanical ventilation. Mortality rates range from 0.25% to 3.0% on average, being higher for vulnerable subjects presenting certain risk factors such as age over 70, respiratory disease, diabetes, cardiovascular disease and cancer. The most frequent cause of mortality is COVID-19-related pneumonia and acute respiratory distress syndrome (ARDS), with some patients also presenting severe cardiovascular damage. In severe cases, mortality rates can be as high as 60.5%.86 The virus infects host cells through the angiotensin converting enzyme 2 (ACE2) receptor, which is highly expressed in several organs, including the salivary glands.87 Studies on the coronavirus suggest that there is a massive activation of mononuclear macrophages and T lymphocytes and release of inflammatory mediators such as IL-6. In SARS-CoV-2, IL-6 seems to bind to target cells, inducing increased cytokine production that perpetuates inflammation in the pulmonary tissues and in other organs.88 Some studies have investigated the potential role of upregulated levels of IL-6 in the exacerbation of viral diseases before the pandemic, suggesting that IL-6 has the potential to promote worsening of clinical symptoms and facilitate virus survival.3 OC TOBER 2 0 2 0 491

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Of interest, IL-6 has been suggested to contribute to viral persistence, with serum upregulation of IL-6 being linked to other viral infections in humans, including influenza virus and human immunodeficiency virus.89 During infection, together with IL-1β and TNF-α, IL-6 is a crucial mediator.90 The potential biological mechanisms for increased IL-6 production during viral infection include the potential ability of some viruses to evade the immune response and increase IL-6 levels as viral loads increase, and the presence of genetic IL-6 polymorphisms leading to overproduction of IL-6 during the infection.91 Furthermore, studies on COVID-19 suggest that higher IL-6 levels can worsen alveolar capillary blood gas exchange in the lungs and oxygen diffusion, potentially contributing to fibrosis and pulmonary failure.88 Recently, a study on IL-6 levels in hospitalized COVID-19 patients suggested an important role of this cytokine in predicting the need for mechanical ventilation.4 Forty hospitalized COVID-19 patients were included, from which 32.5% deteriorated and required mechanical ventilation. There was a strong association between the need for ventilation and IL-6 serum levels above 80 pg/ml. High IL-6 levels accurately predicted respiratory failure with 22 times higher risk for respiratory complications. The authors highlighted that the accuracy of the cutoff value needs to be further assessed due to the small sample size.4 In a recent metaanalysis, severe COVID-19 cases presented a 2.9 fold increase in IL-6 levels when compared to mild to moderate cases without complications.92 With the current shortage of health 492 OC TOBER

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care resources due to the high number of infections, identification of patients who have increased risk for respiratory complications can be crucial for resource allocation.11 The importance of IL-6 for COVID19-related pulmonary complications has been confirmed by a small study in China, where tocilizumab was given to 20 hospitalized patients who had severe COVID-19. The drug had excellent results, with 90.5% of patients recovering after an average of 13.5 days.93 Tocilizumab is a humanized IL-6 receptor

Entrance of oral pathogens into the systemic circulation is another potential mechanism that can result in upregulated production of inflammatory mediators in the body. monoclonal antibody, which has high affinity for IL-6 receptors. It binds to these receptors, preventing IL-6 from altering cellular behavior and ultimately improving inflammation. Currently, two RCTs are underway to further investigate the effect of IL-6 receptor antagonists in severe COVID-19 cases (NCT04310228 and NCT04315298).93 Further confirmation on the importance of an intense inflammatory reaction in critically ill COVID-19 patients comes from a recent report from the RECOVERY Trial. This RCT from the U.K. included 2,100 participants in the dexamethasone arm (6 mg/day for 10 days) and 4,300 participants in the standard care arm. Preliminary results show that in COVID-19 patients who were on

ventilators, dexamethasone decreased mortality by one-third. Previous studies show that dexamethasone inhibit T-cell activation and downregulates IL-6 and other proinflammatory cytokines, promoting a shift towards an anti-inflammatory direction.94 Another line of treatment currently being investigated is the use of inhaled steroids, with ongoing studies taking place in the U.S., France and England. Inhaled steroids are thought to reduce virus replication and inflammation in the airways, leading to less immunosuppression than systemic steroids.95 Findings from COVID-19 studies and the current treatment options under investigation suggest a pivotal role of cytokine storms in the mortality associated with COVID-19 complications, hence, mitigating sources of inflammation is prudent.

Biological Mechanisms Behind the Connection Between Periodontal Disease and Pulmonary Conditions, Including COVID-19-Related Respiratory Complications Systemic Inflammation

In the presence of inflammation in the periodontium, several host cells can increase production of IL-6, which can diffuse into the systemic circulation together with other cytokines. Elevated IL-6 levels have been reported in periodontal tissues, saliva, GCF and serum in periodontitis patients, as discussed previously in this review. Once in the blood, IL-6 and other mediators have the potential to affect distant organs and tissues, such as the lungs, through the activation of circulating immune cells and endothelial cells, which induces further release of inflammatory mediators and potentially

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contributes to inflammation in the respiratory tissues.10 Entrance of oral pathogens into the systemic circulation is another potential mechanism that can result in upregulated production of inflammatory mediators in the body. Endothelial cells and leukocytes respond to circulating bacterial antigens with secretion of proinflammatory mediators. Continuous systemic exposure to bacterial antigens cause formation of immune complexes that further promote production of TNF-α, IL-6 and IL-1β. Moreover, in periodontitis patients, peripheral blood neutrophils present a hyperactive profile characterized by increased production of proinflammatory cytokines and reactive oxygen species.96

Bacterial Load

Approximately 100 million bacteria are present in every cubic millimeter of oral biofilm, which can function as a reservoir for periodontal and respiratory pathogens.97 According to Scannapieco et al., there are four possible ways through which oral pathogens can contribute to respiratory diseases.98 The first is the aspiration of secretions from the oropharynx into the upper and lower airways. They can adhere to the respiratory epithelium and initiate/exacerbate infection indirectly through the release of LPS or directly through signal transduction via adhesion receptors. Second, enzymes produced in periodontal disease can alter the surface of the respiratory epithelium and facilitate adherence of respiratory pathogens. Third, hydrolytic enzymes produced in periodontal disease can deteriorate salivary proteins on bacterial surfaces, facilitating their adherence to mucosa.

Lastly, cytokines can modulate bacterial adhesion of pathogens to the pulmonary epithelium.98 Elimination of aspirated bacteria by the immune system is impaired in patients with impaired saliva production, swallowing disorders and poor cough reflex, putting these patients at higher risk for lung infections. For intensive care patients, intubation and mechanical ventilation decreases clearance of oral secretions leading to increased oral bacterial load and risk for pneumonia.99 In support of

New research suggests periodontal pathogens can contribute to gut dysbiosis, given that oral bacteria are frequently swallowed through saliva. these findings, studies have reported cultures of oral facultative and anaerobe species from infected lung fluids, such as Porphyromonas gingivalis, Eikenella corrodens, Fusobacterium nucleatum, Aggregatibacter actinomycetemcomitans and Peptostreptococci.100 Studies have suggested that bacteria and/or bacterial products of oral origin are able to induce secretion of cytokines from pulmonary epithelial cells, leading to recruitment of inflammatory cells. The inflamed respiratory epithelium can in turn become more susceptible to infection due to epithelial inflammation.98 Some oral pathogens are able to stimulate epithelial cells to produce proinflammatory cytokines to a similar degree to that observed for respiratory pathogens.101

Gut Dysbiosis

Gut dysbiosis has been suggested as a potential novel pathogenic mechanism linked to changes in immunity, systemic inflammation and development of respiratory disease.102 New research suggests that periodontal pathogens can contribute to gut dysbiosis, given that oral bacteria are frequently swallowed through saliva. Thus, periodontal pathogens can reach the intestines, alter the local microbiota, increase gut permeability and the risk for endotoxemia, which is defined as the entrance of LPS in the blood circulation and promotes systemic inflammation.103 In vitro experiments have shown that Porphyromonas gingivalis was able to successfully withstand stomach acids and colonize the colon, leading to functional changes.104 In health, oral microorganisms are poor colonizers of the gastrointestinal tract; however, when systemic conditions such as viral infections are present, higher numbers of oral bacteria have been identified in the intestines.105 Despite the early stages of research on gut dysbiosis in periodontitis patients, this can become an additional biological mechanism to explain the proinflammatory effect of periodontitis in the systemic environment and the lungs.

Endothelial Dysfunction

Endothelial dysfunction encompasses changes in endothelial physiology, representing an early step in atherosclerosis. It is mainly characterized by reduced production of nitric oxide and impaired endotheliumdependent vasodilatation. Periodontitis has been linked to endothelial dysfunction in healthy patients and in patients with hypertension.106 OC TOBER 2 0 2 0 493

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Accordingly, periodontal treatment was able to improve acetylcholineinduced vasodilation in hypertensive and normal patients, suggesting a positive effect on endothelial dysfunction irrespective of the patient’s general condition.107,108 To conclude, there are several biological pathways for the link between periodontitis and COVID-19. The oral bacterial load and systemic inflammation resulting from periodontal disease can affect the lung endothelium and the gut microbiome. Aspiration of oral bacteria is another potential mechanism through which oral pathogens can reach the respiratory tract and potentially interact with the SARS-CoV-2 virus to increase severity and mortality. In the lungs, circulating bacteria and cytokines such as IL-6 can alter the respiratory tissues, leading to decreased lung function, increased risk for infection and other complications, particularly in patients with COVID-19 (FIGURE). Changes in the lungs have been reported even in systemically healthy patients as a consequence of periodontitis, suggesting that periodontal and dental treatment are essential for both healthy subjects and for those who have lung diseases or other chronic diseases, such as hypertension, diabetes and atherosclerosis. Directly through high IL-6 levels or indirectly through alterations in the lung endothelium and gut microbiome, periodontitis can increase the risk for COVID-19 severity and complications, potentially affecting the course of the disease. Of note, chronic psychological stress has also been linked to elevated circulating IL-6 levels.109 Considering the widespread psychological and financial stress 494 OC TOBER

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brought by the pandemic, it can be a significant contributor to periodontal and systemic inflammation, further increasing IL-6 levels and the risk for COVID-19 related complications.

Periodontal Screening and Treatment as Preventive Tools Against COVID-19

Considering the potential impact of poor oral hygiene and periodontitis on respiratory infections and COVID-19, periodontal interventions are important to reduce the burden of

In nursing homes and ICUs, oral hygiene and professional oral health have been shown to reduce the rate of pneumonia and mortality.

oral bacteria and potentially decrease systemic inflammation.57,60,61 As dental offices remained closed for elective procedures during lockdown, millions of dental cleaning appointments were postponed, suggesting a possible increase in the rates of gingivitis and periodontitis, with consequent elevation of systemic inflammation. Given the high transmission rate of the virus and the 22 times higher risk for COVID-19 respiratory issues linked to high IL-6 levels,4 every attempt to decrease this inflammatory mediator should be prioritized. Furthermore, periodontitis is considered as a risk factor for cardiovascular disease, hypertension and diabetes, which are comorbidities associated with increased mortality rate for COVID-19.110

In nursing homes and ICUs, oral hygiene and professional oral health have been shown to reduce the rate of pneumonia and mortality.111 In Brazil, hospitals that have a dentist presented a reduction in aspiration pneumonia and hospital infections, decreased need for antibiotics, shorter hospitalization time, lower costs, reduced mortality and improved general well-being.112 Based on these findings, a national law was approved in 2016 requiring the presence of a dentist in private and public hospitals that have an ICU in Brazil.112 The Centers for Disease Control and Prevention (CDC) has estimated that up to 30% of COVID-19 cases in the U.S. require hospitalization. With the evidence that dental care, including topical application of CHX, can be effective in the prevention of respiratory infections, it is tempting to wonder if hospital dentistry or dental care delivered by hospital nurses could make a difference in the disease course of thousands of hospitalized COVID-19 patients. Because the throat seems to be crucial for virus replication early after infection with COVID-19, oral rinses can potentially alter the viral lipid envelope, reducing the viral load and the risk of transmission.113 Despite the lack of human studies on the effect of mouthwashes on SARS-CoV-2, the American Dental Association (ADA) recommends the following agents to help reduce transmission of the virus: 1% hydrogen peroxide and 0.2–0.5% povidone. The current recommendations for use of oral rinses include preoperative for all patients during the pandemic (ADA). Challacombe et al. (2020) suggest the use of povidone 0.5% every two to three hours (up to four times daily) for dentists and dental assistants to reduce their risk of infection.114

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Despite the fact that CHX can reduce the risk of pneumonia in hospitalized patients undergoing mechanical ventilation, few in vitro studies suggest less effectiveness against viruses when compared to povidone and hydrogen peroxide. A study from England suggests mouthwashes containing 21%–27% ethanol combined with essential oils can be effective against viruses; however, they require further clinical studies.113

IL-6 Genetic Testing

Findings from studies on the –174 IL-6 genetic polymorphism suggest that the G/G genotype increases the risk for severe periodontitis due to exacerbated inflammatory response characterized by elevated IL-6 levels.19,24 According to data from 12,000 salivary tests performed by OralDNA Labs (Eden Prairie, Minn.) for the –174 IL-6 polymorphism, 45.2% of periodontitis patients have the high-risk genotype (G/G), 41.0% have intermediate risk (C/G) and 13.8% have low risk (C/C) (unpublished data). In the study from Trevilatto et al. (2003), 71% of severe periodontitis and 50% of moderate periodontitis patients presented the G/G genotype.17 Despite the fact that periodontitis is multifactorial and associated with multiple cytokines,103 recent findings on the pivotal role of IL-6 in cytokine storms in hospitalized COVID-19 patients make it a promising choice for genetic testing. Currently, there are no studies on the role of –174 IL-6 polymorphism in coronavirus disease. In the near future, IL-6 genetic testing for COVID-19 patients could help identify those at risk for cytokine storms and guide treatment to decrease complications and mortality. It will be interesting to investigate if the high-risk G/G genotype that predisposes to severe periodontitis is also linked to the severity of coronavirus disease.

Solutions Section

Based on the scientific evidence provided in this review and on guidelines from the ADA, the following solutions are recommended for the oral team during these unprecedented times.

be enough, hence, instructions for periodontitis patients need to be customized. Early identification of patients with periodontitis is very important for timely treatment and reduction of the inflammatory response.

Promotion of Oral Hygiene To Decrease the Burden of Bacteria and Screening for Untreated Periodontitis

Professional Teeth Cleaning and Periodontal Treatment To Decrease the Burden of Inflammation

Good personal hygiene has never been so crucial, including optimal daily oral hygiene. Bacterial plaque can harbor respiratory and periodontal pathogens,

Systemic antibiotics can be considered as an adjunct to periodontal treatment for better clinical and microbiological effects.

which can reach the systemic circulation and invade host cells. Keeping the burden of oral bacteria as low as possible can reduce the risk of aspiration to the respiratory tract. Patients should be encouraged to brush their teeth twice per day for a minimum of two minutes with fluoridated toothpaste and perform interproximal cleaning. In a recent meta-analysis, interdental brushes and water-jets showed the highest reduction in gingival bleeding, while unsupervised flossing was not effective.115 For management of gingivitis, the consensus from the 11th European Workshop in Periodontology suggests that flossing should only take place when there is no space for an interdental brush. For periodontitis patients, two minutes of toothbrushing might not

Not all patients have motivation or fine motor skills to maintain optimal plaque control. The consensus from the 11th European Workshop is in support of professional plaque control as a way to improve gingival inflammation, decrease plaque and reinforce oral hygiene habits.116 As discussed previously, it is imperative for periodontitis patients to undergo comprehensive treatment to control alveolar bone loss and decrease systemic inflammation and IL-6 levels. For advanced cases, systemic antibiotics can be considered as an adjunct to periodontal treatment for better clinical and microbiological effects, taking into consideration both local and systemic health. Successful control of periodontal inflammation can be beneficial to the lungs, possibly decreasing severity and risk of COVID-19 respiratory problems.

Genetic IL-6 Testing To Provide Risk Assessment for Periodontitis

The G alleles in the IL-6 polymorphism in the –174 promoter region have been linked to increased risk for severe periodontitis.17–19 IL-6 genetic testing can be a useful tool to provide information on the risk for severe periodontitis and guide treatment, as more aggressive approaches may be required in patients who carry the G allele in order to diminish the inflammatory response. Currently, there are no studies evaluating genetic OC TOBER 2 0 2 0 495

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variations in this position of the IL-6 gene in COVID-19 patients.

Infection Control Measures To Decrease the Spread of SARS-CoV-2

The ADA COVID-19 Center and the CDC have provided comprehensive recommendations to mitigate the spread of SARSCoV-2 in dental practices regarding patient management, personnel, facility and equipment considerations, administrative and engineering controls, infection control, personal protective equipment (PPE) and hygiene.117 As mentioned previously, hydrogen peroxide has been recommended as a preprocedural rinse with the potential to decrease the transmission of SARS-CoV-2 because it is vulnerable to oxidation. Although it has not been tested in clinical trials, in vitro studies report that it can inhibit virus replication in epithelial cells. As discussed earlier, hospitalized patients are unable to maintain oral hygiene, resulting in plaque build-up that can provide a niche for respiratory pathogens and a source for aspiration of oral pathogens. This increases the risk for pneumonia and respiratory problems and can have a negative impact in COVID-19-related respiratory complications, although there are currently no studies on this topic. Based on data from pneumonia studies, it can be speculated that use of hydrogen peroxide or chlorhexidine could have a positive affect on the course of the coronavirus disease in hospitalized patients.

Virtual Dental Consultations and Monitoring and Mobile Dentistry for Patients Who Want To Avoid Leaving Their Homes

With the high transmission rate of SARS-CoV-2, it is understandable that

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patients want to avoid potential exposure to the virus, particularly those with comorbidities. Teledentistry can be a solution, as several platforms have emerged to offer dentists complete solutions to provide virtual dental consultations. Even though professional cleaning and periodontal treatment require in-office visits, triaging for dental emergencies and oral hygiene reinforcement can be done virtually. In addition, mobile dentistry can become a necessary solution in the future to offer treatment in the comfort of the patient’s home or workplace.118

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Mobile dentistry can become a necessary solution in the future to offer treatment in the comfort of the patient’s home or workplace. ■

Take-Home Message ■

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The coronavirus disease can dysregulate the host immune response and elevate IL-6 levels. High IL-6 levels increase the risk for mechanical ventilation in hospitalized patients by 22 times, being a predictor for COVID-19related respiratory complications. IL-6 receptor antagonists and dexamethasone have the potential to improve disease severity in hospitalized patients through changes in the inflammatory response; however, results from robust trials need to confirm safety and effectiveness for this treatment. Oral diseases, particularly periodontitis, can contribute to a systemic inflammatory response with

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high circulating IL-6 levels. Certain genetic variations of the IL-6 gene can increase the risk to severe periodontitis through an exacerbated IL-6 response. Genetic testing can be useful to identify patients at high risk and guide treatment. High IL-6 levels in periodontitis patients can contribute to COVID-19 respiratory complications. Oral bacteria can be aspirated and affect lung function, increasing the risk for pneumonia, COPD and potentially COVID-19-related pulmonary complications. Oral hygiene interventions, periodontal and dental treatment have the potential to decrease the oral bacterial burden and the systemic inflammatory response. Thus, is it essential to treat periodontitis and promote good plaque control for general health and decrease the risk of COVID-19 problems. Periodontal treatment is beneficial for systemically healthy patients and for those with pulmonary conditions, as it can decrease IL-6 levels and decreased inflammation. Periodontal health can help prevent severe COVID-19 respiratory complications. Prevention of COVID-19-related pulmonary complications can have a huge impact on health care systems with the potential to decrease the need for intensive care and mechanical ventilation and decrease mortality rates.

Conclusion

There are several biological reasons to consider periodontitis as a risk factor for respiratory diseases, and as such, it can contribute to the development of respiratory complications in COVID-19

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patients. Several mechanisms are proposed as possible explanations for the link between the oral environment and the lungs, including systemic inflammation, bacterial load, gut dysbiosis and endothelial function. High serum IL-6 levels can predict COVID19-related respiratory complications and the need for mechanical ventilation, hence, dentists should focus on eliminating underlying conditions that promote systemic inflammation, such as periodontitis and other oral conditions. Despite the current lack of studies on this topic, the potential of oral hygiene and periodontal interventions to decrease the burden of oral bacteria and inflammation, improve general health and protect against severe complications from coronavirus disease should not be underestimated. n ACKNOWLEDGMENT We appreciate Dr. Joan Otomo-Corgel for her valuable and constructive suggestions during the development of this research work. REFERENCES 1. Sohrabi C, et al. World Health Organization declares global emergency: A review of the 2019 novel coronavirus (COVID-19). Int J Surg 2020 Apr;76:71–76. doi: 10.1016/j. ijsu.2020.02.034. 2. Zhou F, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 2020 Mar;395(10229):P1054–1062. doi: 10.1016/S01406736(20)30566-3. 3. Velazquez-Salinas L, Verdugo-Rodriguez A, Rodriguez LL, Borca MV. The role of interleukin 6 during viral infections. Front Microbiol 2019 May;10:1057. doi: 10.3389/ fmicb.2019.01057. 4. Herold T, et al. Level of IL-6 predicts respiratory failure in hospitalized symptomatic COVID-19 patients. J Allergy Clin Immunol 2020 Jul;146(1):128–136.e4. doi: 10.1016/j. jaci.2020.05.008. 5. Mehta P, et al. COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 2020 Mar;395(10229):P1033–1034. doi:10.1016/S01406736(20)30628-0. 6. Coulthard P. Dentistry and coronavirus (COVID-19) — moral decision-making. Br Dent J 2020 Apr;228(7):503–505. doi:10.1038/s41415-020-1482-1. 7. Irwin C, Myrillas T. The role of IL-6 in the pathogenesis of periodontal disease. Oral Dis 2008 Mar;4(1):43–47. doi:10.1111/j.1601-0825.1998.tb00255.x.

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is increased across patients with neither periodontal disease nor diabetes, patients with periodontal disease alone and patients with both diseases. J Periodontal Res 2010 Oct;45(5):688–694. doi: 10.1111/j.16000765.2010.01286.x. 52. Noh MK, et al. Assessment of IL-6, IL-8 and TNF-α levels in the gingival tissue of patients with periodontitis. Exp Ther Med 2013 Sep;6(3):847–851. doi: 10.3892/ etm.2013.1222. 53. Marcaccini AM, et al. Circulating interleukin-6 and high-sensitivity c-reactive protein decrease after periodontal therapy in otherwise healthy subjects. J Periodontol 2009 Apr;80(4):594–602. doi: 10.1902/jop.2009.080561. 54. Sun XJ, et al. Elevation of C-reactive protein and interleukin-6 in plasma of patients with aggressive periodontitis. J Periodontal Res 2009 Jun;44(3):311–316. doi:1 0.1111/j.1600-0765.2008.01131.x. 55. Leira Y, et al. Periodontitis and systemic markers of neurodegeneration: A case-control study. J Clin Periodontol 2020 May;47(5). doi: 10.1111/jcpe.13267. 56. Almaghlouth AA, et al. Effect of periodontal treatment on peak serum levels of inflammatory markers. Clin Oral Investig 2014 Dec;18(9):2113–2121. doi: 10.1007/ s00784-014-1187-4. 57. D’Aiuto F, et al. Periodontitis and systemic inflammation: Control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res 2004 Feb;83(2):156–160. doi: 10.1177/154405910408300214. 58. de Moura Leite SA, et al. The effect of nonsurgical periodontal therapy on hepcidin and on inflammatory and iron marker levels. Braz Oral Res 2019 Sep;33:e055. doi: 10.1590/1807-3107bor-2019.vol33.0055. 59. Shimada Y, Komatsu Y, Ikezawa-Suzuki I, Tai H, Sugita N, Yoshie H. The effect of periodontal treatment on serum leptin, interleukin-6 and C-reactive protein. J Periodontol 2010 Aug;81(8):1118–1123. doi: 10.1902/ jop.2010.090741. 60. Lobão WJM, et al. Relationship between periodontal outcomes and serum biomarkers changes after nonsurgical periodontal therapy. An Acad Bras Cienc 2019 May;91(2):e20170652. doi: 10.1590/00013765201920170652. 61. D’Aiuto F, Parkar M, Nibali L, Suvan J, Lessem J, Tonetti MS. Periodontal infections cause changes in traditional and novel cardiovascular risk factors: Results from a randomized controlled clinical trial. Am Heart J 2006 May;151(5):977–984. doi: 10.1016/j.ahj.2005.06.018. 62. Lima R, et al. Effect of periodontal therapy on serum levels of IL-6 in Type 2 diabetics: A systematic review. Int J Periodontics Restorative Dent 2019 Jan-Feb;39(1):e1–e10. doi: 10.11607/prd.3866. 63. Montenegro MM, et al. Randomized controlled trial of the effect of periodontal treatment on cardiovascular risk biomarkers in patients with stable coronary artery disease: Preliminary findings of 3 months. J Clin Periodontol 2019 Mar;46(3):321–331. doi: 10.1111/jcpe.13085. 64. Torumtay G, Kırzıoğlu FY, Öztürk Tonguç M, Kale B, Calapoğlu M, Orhan H. Effects of periodontal treatment on inflammation and oxidative stress markers in patients with metabolic syndrome. J Periodontal Res 2016 Aug;51(4):489–498. doi: 10.1111/jre.12328. 65. Vos T, et al. Global, regional, and national incidence,

prevalence and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017 Sep 16;390(10100):1211–1259. doi: 10.1016/S0140-6736(17)32154-2. 66. Zeng XT, Tu ML, Liu DY, Zheng D, Zhang J, Leng WD. Periodontal disease and risk of chronic obstructive pulmonary disease: A meta-analysis of observational studies. PLoS One 2012;7(10). doi: 10.1371/journal. pone.0046508. 67. Shen TC, et al. Risk of periodontal diseases in patients with chronic obstructive pulmonary disease a nationwide population-based cohort study. Medicine (Baltimore) 2015 Nov;94(46):e2047. doi: 10.1097/ MD.0000000000002047. 68. Öztekin G, et al. The association between periodontal disease and chronic obstructive pulmonary disease: A case control study. COPD 2014 Aug;11(4):424–430. doi: 10.3109/15412555.2013.858316. 69. Raghavendran K, Mylotte JM, Scannapieco FA. Nursing home-associated pneumonia, hospital-acquired pneumonia and ventilator-associated pneumonia: The contribution of dental biofilms and periodontal inflammation. Periodontol 2000 2007;44(1):164–177. doi: 10.1111/j.16000757.2006.00206.x. 70. Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease. A systematic review. Ann Periodontol 2003 Dec;8:54–69. doi: 10.1902/annals.2003.8.1.54. 71. Azarpazhooh A, Leake JL. Systematic review of the association between respiratory diseases and oral health. J Periodontol 2006 Sep;77(9):1465–1482. doi: 10.1902/ jop.2006.060010. 72. Sabharwal A, Gomes-Filho IS, Stellrecht E, Scannapieco FA. Role of periodontal therapy in management of common complex systemic diseases and conditions: An update. Periodontol 2000 2018 Oct;78(1):212–226. doi: 10.1111/prd.12226. 73. Ćabov T, et al. The impact of oral health and 0.2% chlorhexidine oral gel on the prevalence of nosocomial infections in surgical intensive-care patients: A randomized placebo-controlled study. Wien Klin Wochenschr 2010 Jul;122(13–14):397–404. doi:10.1007/s00508-010-1397-y. 74. Akutsu Y, et al. Pre-operative dental brushing can reduce the risk of postoperative pneumonia in esophageal cancer patients. Surgery 2010 Apr;147(4):497–502. doi: 10.1016/j.surg.2009.10.048. 75. Hollaar VRY, Van Der Putten GJ, Van Der MaarelWierink CD, Bronkhorst EM, De Swart BJM, Creugers NHJ. The effect of a daily application of a 0.05% chlorhexidine oral rinse solution on the incidence of aspiration pneumonia in nursing home residents: A multicenter study. BMC Geriatr 2017 Jun;17(1):128. doi: 10.1186/s12877-017-0519-z. 76. Bellissimo-Rodrigues WT, et al. Effectiveness of a dental care intervention in the prevention of lower respiratory tract nosocomial infections among intensive care patients: A randomized clinical trial. Infect Control Hosp Epidemiol 2014 Nov;35(11):1342–1348. doi: 10.1086/678427. 77. Peter KP, Mute BR, Doiphode SS, Bardapurkar SJ, Borkar MS, Raje DV. Association between periodontal disease and chronic obstructive pulmonary disease: A reality or just a

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dogma? J Periodontol 2013 Dec;84(12):1717–1723. doi: 10.1902/jop.2013.120347. 78. Holtfreter B, Richter S, Kocher T, et al. Periodontitis is related to lung volumes and airflow limitation: A crosssectional study. Eur Respir J 2013 Dec;42(6):1524–1535. doi: 10.1183/09031936.00109112. 79. Lee W, et al. Association between periodontitis and pulmonary function based on the Third National Health and Nutrition Examination Survey (NHANES III). J Clin Periodontol 2020 Jul;47(7);788–795. doi: 10.1111/ jcpe.13303. 80. Zhou X, Han J, Liu Z, Song Y, Wang Z, Sun Z. Effects of periodontal treatment on lung function and exacerbation frequency in patients with chronic obstructive pulmonary disease and chronic periodontitis: A 2-year pilot randomized controlled trial. J Clin Periodontol 2014 Jun;41(6):564–572. doi: 10.1111/jcpe.12247. 81. Lee E, Lee SW. Prevalence of periodontitis and its association with reduced pulmonary function: Results from the Korean national health and nutrition examination survey. Medicine (Kaunas) 2019 Sep;55(9):581. doi: 10.3390/ medicina55090581. 82. Moraschini V, de Albuquerque Calasans-Maia J, Diuana Calasans-Maia M. Association between asthma and periodontal disease: A systematic review and metaanalysis. J Periodontol 2017;89(4):1–20. doi: 10.1902/ jop.2017.170363. 83. Ferreira MKM, et al. Is there an association between asthma and periodontal disease among adults? Systematic review and meta-analysis. Life Sci 2019 Apr;223:74–87. doi: 10.1016/j.lfs.2019.03.005. 84. Soledade-Marques KR, et al. Association between periodontitis and severe asthma in adults: A case-control study. Oral Dis 2017:1–7. doi:10.1111/odi.12737. 85. Spinelli A, Pellino G. COVID-19 pandemic: Perspectives on an unfolding crisis. Br J Surg 2020;107(7):785–787. doi: 10.1002/bjs.11627. 86. Yang X, Yu Y, Xu J, et al. Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: A single-centered, retrospective, observational study. Lancet Respir Med 2020;8(5):475– 481. doi: 10.1016/S2213-2600(20)30079-5. 87. Xu J, Li Y, Gan F, Du Y, Yao Y. Salivary glands: Potential reservoirs for COVID-19 asymptomatic infection. J Dent Res 2020 99(8):989. doi: 10.1177/0022034520918518. 88. Fu B, Xu X, Wei H. Why tocilizumab could be an effective treatment for severe COVID-19? J Transl Med 2020 Apr;18(1):164. doi: 10.1186/s12967-02002339-3. 89. Borges ÁH, O’Connor JL, Phillips AN, et al. Factors associated with plasma IL-6 levels during HIV infection. J Infect Dis 2015;212(4):585–595. doi: 10.1093/ infdis/jiv123. 90. Dienz O, Rincon M. The effects of IL-6 on CD4 T cell responses. Clin Immunol 2009;130(1):27–33. doi: 10.1016/j.clim.2008.08.018. 91. Lan T, Chang L, Wu L, Yuan Y-F. IL-6 plays a crucial role in HBV infection. J Clin Transl Hepatol 2015;3(4):271– 276. doi: 10.14218/JCTH.2015.00024. 92. Coomes EA, Haghbayan H. Interleukin-6 in COVID-19: A systematic review and meta-analysis. MedRxiv 2020:20048058. doi:10.1101/2020.03.30.20048058. 93. Xu X, et al. Effective treatment of severe COVID-19

patients with tocilizumab. Proc Natl Acad Sci U S A 2020;117(20):10970–10975. doi: 10.1073/ pnas.2005615117. 94. Ledford H. Coronavirus breakthrough: Dexamethasone is first drug shown to save lives. Nature 2020;582(7813):469. doi: 10.1038/d41586-02001824-5. 95. Armitage LC, Brettell R. Inhaled corticosteroids: A rapid review of the evidence for treatment or prevention of COVID-19. Cent Evidence-Based Med Univ Oxford 2020. 96. Dias IHK, Matthews JB, Chapple ILC, Wright HJ, Dunston CR, Griffiths HR. Activation of the neutrophil respiratory burst by plasma from periodontitis patients is mediated by proinflammatory cytokines. J Clin Periodontol 2011;38(1):1–7. doi: 10.1111/j.1600051X.2010.01628.x. 97. Thoden van Velzen SK, Abraham‐Inpijn L, Moorer WR. Plaque and systemic disease: A reappraisal of the focal infection concept. J Clin Periodontol 1984;11(4):209–220. doi: 10.1111/j.1600-051X.1984.tb02211.x. 98. Scannapieco FA. Role of oral bacteria in respiratory infection. J Periodontol 1999;70(7):793–802. doi: 10.1902/jop.1999.70.7.793. 99. Munro CL, Grap MJ, Elswick RK, McKinney J, Sessler CN, Hummel RS. Oral health status and development of ventilator-associated pneumonia: A descriptive study. Am J Crit Care 2006;15(5):453–460. doi: 10.4037/ ajcc2006.15.5.453. 100. Chen AC, Liu CC, Yao WJ, Chen CT, Wang JY. Actinobacillus actinomycetemcomitans pneumonia with chest wall and subphrenic abscess. Scand J Infect Dis 1995;27(3):289–290. doi: 10.3109/00365549509019023. 101. Scannapieco FA, Wang B, Shiau HJ. Oral bacteria and respiratory infection: Effects on respiratory pathogen adhesion and epithelial cell proinflammatory cytokine production. Ann Periodontol 2001;6(1):78–86. doi: 10.1902/annals.2001.6.1.78. 102. Budden KF, et al. Emerging pathogenic links between microbiota and the gut-lung axis. Nat Rev Microbiol 2017;15(1):55–63. doi: 10.1038/nrmicro.2016.142. 103. Hajishengallis G. Periodontitis: From microbial immune subversion to systemic inflammation. Nat Rev Immunol 2015;15(1):30—44. doi: 10.1038/nri3785. 104. Walker MY, Pratap S, Southerland JH, Farmer-Dixon CM, Lakshmyya K, Gangula PR. Role of oral and gut microbiome in nitric oxide-mediated colon motility. Nitric Oxide 2018;73:81–88. doi: 10.1016/j.niox.2017.06.003. 105. Seedorf H, Griffin NW, Ridaura VK, et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 2014;159(2):253–266. doi: 10.1016/j. cell.2014.09.008. 106. Moura MF, et al. Periodontitis and endothelial dysfunction: Periodontal clinical parameters and levels of salivary markers interleukin-1, tumor necrosis factor-, matrix metalloproteinase-2, tissue inhibitor of metalloproteinases-2 complex and nitric oxide. J Periodontol 2017;88(8):778– 787. doi: 10.1902/jop.2017.170023. 107. Orlandi M, et al. Association between periodontal disease and its treatment, flow-mediated dilatation and carotid intima-media thickness: A systematic review and meta-analysis. Atherosclerosis 2014;236(1). doi: 10.1016/j.atherosclerosis.2014.06.002.

108. Higashi Y, et al. Periodontal infection is associated with endothelial dysfunction in healthy subjects and hypertensive patients. Hypertension 2008;51:446–453. doi: 10.1161/HYPERTENSIONAHA.107.101535. 109. Rohleder N, Aringer M, Boentert M. Role of interleukin-6 in stress, sleep and fatigue. Ann N Y Acad Sci 2012;1261(1):88–96. doi: 10.1111/j.17496632.2012.06634.x. 110. Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: Summary of a report of 72,314 cases from the Chinese Center for Disease Control and Prevention. JAMA 2020;323(13):1239–1242. doi: 10.1001/jama.2020.2648. 111. Yang LC, Suen YJ, Wang YH, Lin TC, Yu HC, Chang YC. The association of periodontal treatment and decreased pneumonia: A nationwide population-based cohort study. Int J Environ Res Public Health 2020;17(1). doi: 10.3390/ ijerph17010356. 112. Santaella N, Santos P, De Souza IS, Santaella NG, Sérgio P, Santos S. The practice of hospital dentistry in Brazil: An integrative literature review. Rev Bras Odontol 2017;74(3):232–241. doi: 10.18363/rbo.v74n3.p.232. 113. O’Donnell VB, et al. Potential role of oral rinses targeting the viral lipid envelope in SARS-CoV-2 infection. Function 2020;1(1). doi: 10.1093/function/zqaa002. 114. Challacombe SJ, Kirk-Bayley J, Sunkaraneni VS, Combes J. Povidone iodine. Br Dent J 2020;228(9):656– 657. doi: 10.1038/s41415-020-1589-4. 115. Kotsakis GA, Lian Q, Ioannou AL, Michalowicz BS, John MT, Chu H. A network meta-analysis of interproximal oral hygiene methods in the reduction of clinical indices of inflammation. J Periodontol 2018;89(5):558–570. doi: 10.1002/JPER.17-0368. 116. Chapple ILC, Van Der Weijden F, Doerfer C, et al. Primary prevention of periodontitis: Managing gingivitis. J Clin Periodontol 2015;42(S16):S71–S76. doi:10.1111/ jcpe.12366. 117. CDC. Center for Disease Control. www.cdc.gov/ coronavirus/2019-ncov/cases-updates/hospitalizationsforecasts.html. Published 2020. 118. Carvajal P, Gómez M, Gomes S, et al. Prevalence, severity, and risk indicators of gingival inflammation in a multi-center study on South American adults: A cross sectional study. J Appl Oral Sci 2016;24(5):524. doi: 10.1590/1678-775720160178. THE CORRESPONDING AUTHOR, Shervin Molayem, DDS, can be reached at drmolayem@synergyspecialists.com.

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Decoding Dental Aerosols in the Age of COVID-19 Anthony D. Mair, DDS, MCID; Paul H. Korne, DDS, MCID; and Mohamed-Nur Abdallah, BDS, MSc, PhD

a b s t r a c t The conflation with medical aerosols in the age of COVID-19 has

created an inaccurate and potentially dangerous argument in dentistry.

AUTHORS Anthony D. Mair, DDS, MCID, is an adjunct professor in graduate orthodontics at Western University in London, Ontario, and a clinical associate in graduate orthodontics at the University of Toronto. He is a past president of the Ontario Association of Orthodontists. Conflict of Interest Disclosure: None reported.

Paul H. Korne, DDS, MCID, is a faculty lecturer at McGill University in Montreal. He is a past president and member of the Canadian Association of Orthodontists. Conflict of Interest Disclosure: None reported. Mohamed-Nur Abdallah, BDS, MSc, PhD, is an orthodontics and dentofacial orthopedics resident at the Faculty of Dentistry at the University of Toronto. Conflict of Interest Disclosure: None reported.

he outbreak of SARS-CoV-2 has negatively impacted society over the past few months.1 The shutting of economies and the introduction of “physical distancing” was a necessary response to reduce the rate of new infections and prevent overloading of our health care systems. As such, dental clinics, along with most other nonessential businesses, were asked to cease operations to reduce social contacts and, in turn, protect the public. In North America, dental offices are undergoing phased reopening. It is at this critical juncture that a new controversy has risen to prominence — the possible risk of dental aerosols and aerosol-generating dental procedures (AGDPs).2 In the past few months, some members of the dental community have expressed concern that AGDPs could facilitate the infective transmission of SARS-CoV-2 and endanger dental staff and patients.3

Virus Transmission Versus Disease Infection

SARS-CoV-2 is the causative virus for the resultant disease COVID-19. It is important to note that transmission is necessary for infection, but infection does not inevitably follow exposure.4,5 It is established that SARS-CoV-2 can infect a host via droplet and, to a lesser degree, contact transmission, whereas acquiring COVID-19 disease via airborne transmission remains unlikely.1,2,5–8 The viral load can be defined as the number of viral particles in a given volume of droplets. The minimal infective dose is the lowest number of viral particles that can initiate disease.4,5,9 The minimal infective dose for each virus varies with host susceptibility and immune response. Furthermore, it has been shown that the probability of getting infected as well as the severity of disease are dose-dependent.4,5,9,10 However, the OC TOBER 2 0 2 0 501

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minimal infective dose for SARSCoV-2 is not well established.5 Accordingly, it is important to protect the susceptible portals of entry. SARS-CoV-2 enters the human body through the mucus membranes: the nose, the mouth and the eyes.3,11–13 Therefore, one should shield these areas with appropriate personal protective equipment (PPE).

Aerosols: Droplet, Contact and Airborne Transmission

Many of the following terms are often used interchangeably: “aerosols,” “droplets,” “droplet nuclei,” “airborne” and “solid particulates.” This makes it more difficult to draw recommendations on how to adapt clinical practice. In general, aerosols are solid or liquid particles that are suspended in the air; while they can be visible, most often they are not.9,14,15 Aerosols can be divided into large droplets and small droplets. Researchers and clinicians tend to reserve the term aerosol only for small droplets. In this instance, they would use the term droplet for larger droplets and the term aerosols for smaller droplets. Large droplets behave ballistically and tend to be falling when they infect the recipient. This mode of transmission is known as droplet transmission.5 Large droplets may also contaminate objects and be transferred to mucous membranes by way of touch. This is called contact transmission.16 Small droplets stay suspended in the air for a variable amount of time or they evaporate and change into a solid particulate droplet nuclei that float freely. The transmission of these small droplets is known as airborne transmission.8,14,15 Examples of diseases with established airborne transmission 502 OC TOBER

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include tuberculosis and measles.17,18 There is significant controversy regarding the cut-off point between small and large droplets.4,5,14,15,19,20

inducing the patient to cough. It has been shown that coughing emits up to 1,000 times the number of droplets compared to normal breathing.19

Aerosol-Generating Procedures

Aerosol-Generating Medical Procedures

An aerosol-generating procedure (AGP) is a medical or dental intervention that has the potential of creating aerosols in addition to those that patients naturally produce during breathing, speaking, sneezing and coughing.14,20 AGPs produce both small and large droplets, and each

When the oral cavity is exposed to instruments that rotate, vibrate or expel compressed air, an aerosol of these microbes is inevitably created. AGP creates a different pattern and composition of aerosols. Therefore, the term AGP should not be used loosely, and one should not presume that all AGPs have the same risk or require the same level of PPE (i.e., an AGP does not indicate by default a high-risk procedure). The decision to categorize an AGP as a high-risk procedure should be based on evidence.14 Furthermore, it is inaccurate to conclude that generating aerosols will always cause infection. It is also inaccurate to grant equivalency between aerosolgenerating medical procedures (AGMPs) and AGDPs.. The aerosol composition differs considerably even among AGMPs. For instance, certain AGMPs generate aerosols by

Generally, AGMPs can be divided into two categories: procedures that induce the patient to produce aerosols and those that mechanically create aerosols.14 Medical procedures that agitate the airway (hereinafter referred as agitative AGMPs), such as tracheal and bronchial intubation, may induce the patient to cough forcibly, thereby releasing aerosols filled with a high viral infectious dose.14,21 Indeed, both these procedures have been associated with a high risk of SARS-CoV-1 transmission to health care workers.5,14 For example, a retrospective cohort study reported an increased risk of being infected with SARS-CoV-1 in health care staff involved with intubation procedures.22 It should be noted that while all health care workers wore N95 masks, some of them did not have eye protection.22 In contrast, AGMPs may also disperse aerosols mechanically through interventions such as ventilation, suctioning or nebulizer treatment. Despite the limited evidence, these procedures are generally considered less risky than the induction group described above.5,14,21,23 For example, a meta-analysis of three cohort studies concluded that nebulizer treatment had no significant increased risk in the transmission of SARSCoV-1 to health care workers.21 Hospitals adopted more stringent PPE protocols and airborne precautions to reduce morbidity and mortality when medical health care workers were exposed to agitative

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AGMPs.14,24,25 In medicine, not all AGMPs require this higher level of intervention.21,26 This selective approach to PPE continues now during the COVID-19 pandemic.26–30

Aerosol-Generating Dental Procedures

Dental aerosols have been studied for well over 50 years. The tissues and fluids of the oral cavity are replete with bacteria and viruses.31–34 When the oral cavity is exposed to instruments that rotate, vibrate or expel compressed air, an aerosol of these microbes is inevitably created.33,35,36 It is also well established in the literature that the attentive use of high-volume evacuation (HVE) will reduce dental aerosols by at least 90%.37–39 It is important to note here that most hospital suction units are not rated as high volume.33 The majority of dental aerosol droplets that escape HVE land innocuously on the patient’s face or body.40–42 A smaller percentage of these droplets constitute the dental aerosol that remains suspended in the air for 10–30 minutes, depending on the airflow characteristics of the operatory.31 Many studies have examined the relative infectivity of dental aerosols as well as the risk of crosscontamination in dental settings. Most of these studies were written in response to a new or resurgent disease such as TB, HIV/AIDS, hepatitis B, SARS, MERS, etc.24,43–49 Generally, these articles all contain a phrase alluding to the possible/ potential infectivity of dental aerosols generated from an infected patient. To our knowledge, there is no evidence that general dental aerosol exposure has resulted in the infection of dental health care workers or other

patients, provided that routine PPE/HVE protocols were in place.

Dental Aerosols and COVID-19

Current evidence points to droplet transmission as the primary vector of infection by SARS-CoV-2.1,2,5,6,8 Contact transmission plays a minor role.16 However, some are concerned that the virus could become aerosolized under specific conditions, thereby introducing the possibility of airborne transmission. In dentistry, this concern is particularly relevant because there

The recent closure of dental offices was about physical distancing and PPE conservation, with dental aerosols being a much lower priority. is a significant percentage of infected people who are either asymptomatic or presymptomatic.3,50–52 These individuals cannot be identified by routine screening questions or temperature checks. The concern is that treating asymptomatic/presymptomatic patients with AGDPs could endanger the health of the dental health care workers, clerical staff or other patients. Because COVID-19 is a new disease, we will not have all the facts for quite some time, but we believe there is enough current and historical data to arrive at some reasonable conclusions. Below are the points on which we have built our commentary: ■ Dental aerosol transmissions have little to no history of

infectivity when regular PPE/ HVE is being practiced.43–49 ■ Six months of patient data have clearly established that COVID-19 is spread primarily by droplet transmission.1,2,5,6,8 ■ The probability of infection from viral exposure in respiratory diseases is proportional to both dose (viral load) and time (amount of time a susceptible host is exposed to the virus).4,5 ■ The lowest rate of viral shedding occurs during nasal breathing;4 during dental procedures, patients generally do not speak, shout or sing. Therefore, the potential viral dose is already quite low. This situation is dramatically different during agitative AGMPs, such as tracheal intubation or bronchoscopy, because they may cause the patient to cough forcefully and release aerosols with a high load of infectious viral droplets.14 Contact tracing has established that asymptomatic spreaders can cause cluster infections in various settings: places of worship, cruise ships, family gatherings, nursing homes, restaurants, business conferences, meat processing plants, choir rehearsals, etc. Unquestionably, asymptomatic spreaders have also visited dentists this year. Yet there remain no documented cluster events linked to dental aerosols. We submit that this is because both dose and time are mitigated during traditional dental visits due to PPE, HVE and the brevity of social interactions.

Discussion

The dental regulatory bodies have taken a rightfully cautious approach to limit the spread of SARS-CoV-2, but in doing so, may not have considered OC TOBER 2 0 2 0 503

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historical evidence. Dentists have often (but unknowingly) generated aerosols in patients infected by pathogens. The dental aerosols of 2020 are only marginally changed from those of 2019 and before. Now they may also contain the SARS-CoV-2 virus in addition to the multitudes of previous pathogens.33,41,45,53 There is no evidence that the viral load of the 2020 dental aerosols is more hazardous than that of those previously encountered. The use of HVE and routine PPE has protected dentists, staff and patients from cluster infections. If this were not the case, there should be ample evidence to the contrary. The recent closure of dental offices, in our opinion, was about physical distancing and PPE conservation, with dental aerosols being a much lower priority. It bears noting that during the last pandemic (H1N1, 2009), neither the licensing bodies of Ontario nor Quebec mandated restriction of dental aerosols. Instead, emphasis was placed on preprocedural screening and hand hygiene. Aerosols from certain medical procedures can be extremely hazardous. Tragic infection and death of health care workers during the SARS and Ebola outbreaks crystalized this awareness.14 The use of more stringent PPE protocols and other airborne precautions is wholly appropriate for those medical interventions on infectious COVID-19 patients. In dentistry, unlike medicine, AGDPs have been labeled as hazardous in the absence of evidence. European countries such as Germany and Sweden continued dental practice during the pandemic with only minor upgrades to PPE and other precautions.54 To our knowledge, there are no incidences of cluster infections linked to dental aerosols in those regions. 504 OC TOBER

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Medically and dentally generated aerosols are not the same. In a regrettable rush to judgement, these very different interventions have been conflated.

Conclusions

We believe there are two primary concerns in the current regulatory environment: ■ The emphasis on dental aerosol mitigation distracts from the real transmission risk in a dental office — the nonclinical areas. Nonclinical areas are where higher viral doses from sustained speaking (and perhaps even coughing and sneezing) may occur, possibly without masks and certainly without the benefit of high-volume evacuation. Therefore, it is imperative to enforce protocols designed to protect staff and patients in the nonclinical spaces of dental offices, including physical distancing, use of face masks and optimized ventilation. ■ The emphasis on dental aerosol mitigation has created a false impression that visits to the dentist are dangerous. Patients are unquestionably safer in dental offices than in most other social settings. Yet if the public perceives visits to the dentist as a health risk, its dental health will inevitably suffer. Dentistry has a long history of leading the way in preventing the transmission of communicable, infectious diseases. Consequently, the profession is already well-poised to meet this new challenge. It is the authors’ opinion that minor modifications to already exemplary protocols are what are needed to keep staff and patients safe. n

Authors’ note: The original objective of this commentary was to persuade our respective provincial licensing bodies to adopt evidence-based, return-to-work protocols when dental aerosols became the flashpoint of infection control mitigation. REFERENCES 1. Wu D, Wu T, Liu Q, Yang Z. The SARS-CoV-2 outbreak: What we know. Int J Infect Dis 2020 May;94:44–48. doi: 10.1016/j.ijid.2020.03.004. Epub 2020 Mar 12. 2. Centers for Disease Control and Prevention. Guidance for Dental Settings. 2020; www.cdc.gov/ coronavirus/2019-ncov/hcp/dental-settings.html. Accessed June 16, 2020. 3. Meng L, Hua F, Bian Z. Coronavirus disease 2019 (COVID-19): Emerging and future challenges for dental and oral medicine. J Dent Res 2020 May;99(5):481–487. doi: 10.1177/0022034520914246. Epub 2020 Mar 12. 4. Tang JW, Li Y, Eames I, Chan PK, Ridgway GL. Factors involved in the aerosol transmission of infection and control of ventilation in healthcare premises. J Hosp Infect 2006 Oct;64(2):100–14. doi: 10.1016/j.jhin.2006.05.022. Epub 2006 Aug 17. 5. Wilson NM, Norton A, Young FP, Collins DW. Airborne transmission of severe acute respiratory syndrome coronavirus-2 to healthcare workers: A narrative review. Anaesthesia 2020 Aug;75(8):1086–1095. doi: 10.1111/anae.15093. Epub 2020 May 8. 6. World Health Organization (WHO). Report of the WHO-China Joint Mission on Coronavirus Disease 2019 (COVID-19) 2020. www.who.int/docs/default-source/ coronaviruse/who-china-joint-mission-on-covid-19-finalreport.pdf. Accessed June 16, 2020. 7. Rafiq D, Batool A, Bazaz MA. Three months of COVID-19: A systematic review and meta-analysis. Rev Med Virol 2020:e2113. doi.org/10.1002/rmv.2113. 8. World Health Organization (WHO). Transmission of SARS-CoV-2: Implications for infection prevention precautions. www.who.int/news-room/commentaries/ detail/transmission-of-sars-cov-2-implications-for-infectionprevention-precautions. Accessed July 31, 2020. 9. Tellier R. Aerosol transmission of influenza A virus: A review of new studies. J R Soc Interface 2009 Dec 6;6 Suppl 6(Suppl 6):S783–90. doi.org/10.1098/ rsif.2009.0302.focus. Epub 2009 Sep 22. 10. Kowalik MM, Trzonkowski P, Łasińska-Kowara M, Mital A, Smiatacz T, Jaguszewski M. COVID-19 — toward a comprehensive understanding of the disease. Cardiol J 2020;27(2):99–114. doi: 10.5603/CJ.a2020.0065. Epub 2020 May 7. 11. Zhao S, Ling K, Yan H, et al. Anesthetic management of patients with COVID 19 infections during emergency procedures. J Cardiothorac Vasc Anesth 2020 May;34(5):1125–1131. doi: 10.1053/j. jvca.2020.02.039. Epub 2020 Feb 28. 12. Lu CW, Liu XF, Jia ZF. 2019-nCoV transmission through the ocular surface must not be ignored. Lancet 020 Feb 22;395(10224):e39. doi: 10.1016/S01406736(20)30313-5. Epub 2020 Feb 6.

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13. Gengler I, Wang JC, Speth MM, Sedaghat AR. Sinonasal pathophysiology of SARS-CoV-2 and COVID-19: A systematic review of the current evidence. Laryngoscope Investig Otolaryngol April 2020. doi.org/10.1002/ lio2.384. 14. Judson SD, Munster VJ. Nosocomial transmission of emerging viruses via aerosol-generating medical procedures. Viruses 2019 Oct 12;11(10):940. doi: 10.3390/ v11100940. 15. Jones RM, Brosseau LM. Aerosol transmission of infectious disease. J Occup Environ Med 2015 May;57(5):501–8. doi: 10.1097/ JOM.0000000000000448. 16. Ferretti L, Wymant C, Kendall M, et al. Quantifying SARS-CoV-2 transmission suggests epidemic control with digital contact tracing. Science 2020 May 8;368(6491):eabb6936. doi: 10.1126/science.abb6936. Epub 2020 Mar 31. 17. Merte JL, Kroll CM, Collins AS, Melnick AL. An epidemiologic investigation of occupational transmission of Mycobacterium tuberculosis infection to dental health care personnel: Infection prevention and control implications. J Am Dent Assoc 2014;145(5):464–471. doi: 10.14219/ jada.2013.52. 18. Botelho-Nevers E, Gautret P, Biellik R, Brouqui P. Nosocomial transmission of measles: An updated review. Vaccine 2012 Jun 8;30(27):3996–4001. doi: 10.1016/j. vaccine.2012.04.023. 19. Fiegel J, Clarke R, Edwards DA. Airborne infectious disease and the suppression of pulmonary bioaerosols. Drug Discov Today 2006 Jan;11(1–2):51–57. doi. org/10.1016/S1359-6446(05)03687-1. 20. Gralton J, Tovey E, McLaws ML, Rawlinson WD. The role of particle size in aerosolised pathogen transmission: A review. J Infect 2011 Jan;62(1):1–13. doi: 10.1016/j. jinf.2010.11.010. Epub 2010 Nov 19. 21. Tran K, Cimon K, Severn M, Pessoa-Silva CL, Conly J. Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: A systematic review. PloS One 2012;7(4):e35797. doi: 10.1371/journal.pone.0035797. Epub 2012 Apr 26. 22. Fowler RA, Guest CB, Lapinsky SE, et al. Transmission of severe acute respiratory syndrome during intubation and mechanical ventilation. Am J Respir Crit Care Med 2004;169(11):1198–1202. doi: 10.1164/rccm.200305715OC. Epub 2004 Feb 27. 23. Davies A, Thomson G, Walker J, Bennett A. A review of the risks and disease transmission associated with aerosol generating medical procedures. J Infect Prev 2009;10(4):122–126. doi. org/10.1177/1757177409106456. 24. Baseer MA, Ansari SH, AlShamrani SS, Alakras AR, Mahrous R, Alenazi AM. Awareness of droplet and airborne isolation precautions among dental health professionals during the outbreak of corona virus infection in Riyadh City, Saudi Arabia. J Clin Exp Dent 2016;8(4):e379–e387. doi: 10.4317/jced.52811. eCollection 2016 Oct. 25. Raboud J, Shigayeva A, McGeer A, et al. Risk factors for SARS Transmission from patients requiring intubation: A multicentre investigation in Toronto, Canada. PloS One 2010;5(5):e10717. doi: 10.1371/journal.pone.0010717. 26. Thamboo A, Lea J, Sommer DD, et al. Clinical evidencebased review and recommendations of aerosol generating

medical procedures in otolaryngology — head and neck surgery during the COVID-19 pandemic. J Otolaryngol Head Neck Surg 2020 May 6;49(1):28. doi: 10.1186/s40463020-00425-6. 27. Mick P, Murphy R. Aerosol-generating otolaryngology procedures and the need for enhanced PPE during the COVID-19 pandemic: A literature review. J Otolaryngol Head Neck Surg 2020 May 11;49(1):29. doi: 10.1186/s40463020-00424-7. 28. Heffernan DS, Evans HL, Huston JM, et al. Surgical infection society guidance for operative and perioperative care of adult patients infected by the severe acute respiratory syndrome Coronavirus-2 (SARS-CoV-2). Surgical Infect (Larchmt) 2020 May;21(4):301–308. doi: 10.1089/ sur.2020.101. 29. Tang LY, Wang J. Anesthesia and COVID-19: What we should know and what we should do. Semin Cardiothorac Vasc Anesth 2020 Jun;24(2):127–137. doi: 10.1177/1089253220921590. Epub 2020 Apr 27. 30. Perkins GD, Morley PT, Nolan JP, et al. International Liaison Committee on Resuscitation: COVID-19 consensus on science, treatment recommendations and task force insights. Resuscitation 2020 Jun;151:145–147. doi: 10.1016/j. resuscitation.2020.04.035. Epub 2020 May 1. 31. Bennett AM, Fulford MR, Walker JT, Bradshaw DJ, Martin MV, Marsh PD. Microbial aerosols in general dental practice. Brit Dent J 2000 Dec 23;189(12):664–7. doi: 10.1038/ sj.bdj.4800859. 32. Gao L, Xu T, Huang G, Jiang S, Gu Y, Chen F. Oral microbiomes: More and more importance in oral cavity and whole body. Protein Cell 2018 May;9(5):488–500. doi: 10.1007/s13238-018-0548-1. Epub 2018 May 7. 33. Harrel SK, Molinari J. Aerosols and splatter in dentistry: A brief review of the literature and infection control implications. J Am Dent Assoc 2004 Apr;135(4):429–37. doi: 10.14219/ jada.archive.2004.0207. 34. Marui VC, Souto MLS, Rovai ES, Romito GA, Chambrone L, Pannuti CM. Efficacy of preprocedural mouth rinses in the reduction of microorganisms in aerosol: A systematic review. J Am Dent Assoc 2019 Dec;150(12):1015–1026.e1. doi: 10.1016/j.adaj.2019.06.024. 35. Szymańska J. Dental bioaerosol as an occupational hazard in a dentist’s workplace. Ann Agric Environ Med 2007;14(2):203–207. 36. Leggat PA, Kedjarune U. Bacterial aerosols in the dental clinic: A review. Int Dent J 2001 Feb;51(1):39–44. doi: 10.1002/j.1875-595x.2001.tb00816.x. 37. Micik RE, Miller RL, Mazzarella MA, Ryge G. Studies on dental aerobiology: I. Bacterial aerosols generated during dental procedures. J Dent Res Jan–Feb 1969;48(1):49–56. doi: 10.1177/00220345690480012401. 38. Harrel SK, Barnes JB, Rivera-Hidalgo F. Reduction of aerosols produced by ultrasonic scalers. J Periodontol 1996 Jan;67(1):28–32. doi: 10.1902/jop.1996.67.1.28. 39. Jacks ME. A laboratory comparison of evacuation devices on aerosol reduction. J Dent Hyg 2002;76(3):202–206. 40. Bentley CD, Burkhart NW, Crawford JJ. Evaluating spatter and aerosol contamination during dental procedures. J Am Dent Assoc 1994 May;125(5):579–584. doi: 10.14219/ jada.archive.1994.0093. 41. Zemouri C, Volgenant CMC, Buijs MJ, et al. Dental aerosols: Microbial composition and spatial distribution. J Oral Microbiol 2020 May;12(1):1762040. doi:

10.1080/20002297.2020.1762040. 42. Timmerman MF, Menso L, Steinfort J, van Winkelhoff AJ, van der Weijden GA. Atmospheric contamination during ultrasonic scaling. J Clin Periodontol 2004 Jun;31(6):458– 62. doi: 10.1111/j.1600-051X.2004.00511.x. 43. Laheij AMGA, Kistler JO, Belibasakis GN, Välimaa H, de Soet JJ, European Oral Microbiology W. Healthcareassociated viral and bacterial infections in dentistry. J Oral Microbiol 2012;4:10.3402. doi: 10.3402/jom. v4i0.17659. 44. Cleveland JL, Kent J, Gooch BF, et al. Multidrug-resistant Mycobacterium tuberculosis in an HIV dental clinic. Infect Control Hosp Epidemiol 1995 Jan;16(1):7–11. doi: 10.1086/646995. 45. Volgenant CMC, de Soet JJ. Cross-transmission in the dental office: Does this make you ill? Curr Oral Health Rep 2018;5(4):221–228. doi: 10.1007/s40496-018-0201-3. 46. Zemouri C, de Soet H, Crielaard W, Laheij A. A scoping review on bio-aerosols in healthcare and the dental environment. PloS One 2017 May 22;12(5):e0178007. doi: 10.1371/journal.pone.0178007. eCollection 2017. 47. Samaranayake LP. Re-emergence of tuberculosis and its variants: Implications for dentistry. Int Dent J 2002 Oct;52(5):330–6. doi: 10.1002/j.1875-595x.2002. tb00880.x. 48. Faecher RS, Thomas JE, Bender BS. Tuberculosis: A growing concern for dentistry? J Am Dent Assoc 1993 Jan;124(1):94–104. doi: 10.14219/jada. archive.1993.0003. 49. Samaranayake LP, Peiris M. Severe acute respiratory syndrome and dentistry: A retrospective view. J Am Dent Assoc 2004 Sep;135(9):1292–302. doi: 10.14219/jada. archive.2004.0405. 50. He X, Lau EHY, Wu P, et al. Temporal dynamics in viral shedding and transmissibility of COVID-19. Nat Med 2020;26(5):672–675. doi.org/10.1038/s41591-0200869-5. 51. Cheng H-Y, Jian S-W, Liu D-P, et al. Contact tracing assessment of COVID-19 transmission dynamics in Taiwan and risk at different exposure periods before and after symptom onset. JAMA Intern Med 2020 May 1:e202020. doi: 10.1001/jamainternmed.2020.2020. 52. Rothe C, Schunk M, Sothmann P, et al. Transmission of 2019-nCoV Infection from an asymptomatic contact in Germany. N Engl J Med 2020 Mar 5;382(10):970–971. doi: 10.1056/NEJMc2001468. Epub 2020 Jan 30. 53. Tellier R, Li Y, Cowling BJ, Tang JW. Recognition of aerosol transmission of infectious agents: A commentary. BMC Infect Dis 2019;19(1):101. doi: 10.1186/s12879019-3707-y. 54. Council of European Dentists (CED). COVID-19 — Overview of national measures affecting dentists in CED countries. www.omd.pt/content/uploads/2020/04/covid19-ced-measures.pdf. Accessed June 16, 2020. THE CORRESPONDING AUTHORS, Anthony D. Mair, DDS, MCID, and Paul H. Korne, DDS, MCID, can be reached at drmair@worldofsmiles.com and drpaulkorne@korneortho.com.

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Global Impact of COVID -19 on Service Delivery and Vulnerable Populations’ Access to Dental Care Francisco Ramos-Gomez, DDS, MS, MPH; Morenike Oluwatoyin Folayan, MBChD, MBA; Marcela Diaz-Betancourt, DDS, MIPH; Gyanendra Kumar, MDS; Thomas Gerhard Wolf, DDS, Dr med dent Priv-Doz; Margherita Fontana, DDS, PhD; and Guglielmo Campus, DDS, PhD

a b s t r a c t COVID-19 is most commonly spread through aerosol droplets and

contact with infected individuals and contaminated surfaces. The nature of how this virus is spread will affect the practice of dentistry for the foreseeable future. The aim of this paper is to provide an overview of the global impact of COVID-19 on dental professionals as well as highlight the barriers and challenges of global access to oral health care during the pandemic, especially among vulnerable populations.

AUTHORS Francisco RamosGomez, DDS, MS, MPH, is a professor in the section of pediatric dentistry and director at the UCLA Center for Children’s Oral Health at the University of California, Los Angeles, School of Dentistry.

Marcela DiazBetancourt, DDS, MIPH, is a scientific associate in the department of restorative, preventive and pediatric dentistry at the University of Bern School of Dental Medicine in Bern, Switzerland.

Morenike Oluwatoyin Folayan, MBChD, MBA, is a professor of pediatric dentistry at the Obafemi Awolowo University in Ile-Ife, Nigeria.

Gyanendra Kumar, MDS, is an associate professor of pediatric and preventive dentistry at the Maulana Azad Institute of Dental Sciences in New Delhi.

Thomas Gerhard Wolf, DDS, Dr med dent, Priv-Doz, is a senior physician in the department of periodontology and operative dentistry at the University Medical Center of the Johannes GutenbergUniversity Mainz in Mainz, Germany. He is also associate professor at the University of Bern School of Dental Medicine in Bern, Switzerland.

Margherita Fontana, DDS, PhD, is the Clifford Nelson endowed professor of dentistry in the department of cariology, restorative sciences and endodontics at the University of Michigan School of Dentistry. Guglielmo Campus, DDS, PhD, is an associate professor in the department of surgery, microsurgery and medicine sciences at the University of Sassari School of Dentistry in Sassari, Italy. Conflict of Interest Disclosure for all authors: None reported.

n December 2019, a highly infectious respiratory disease started to spread in Wuhan, China, and escalating in the lapse of three months to a pandemic.1 In January 2020, the World Health Organization (WHO) announced that this novel coronavirus, severe acute respiratory syndrome coronavirus 2 (SARSCoV-2), was the pathogen causing the COVID-19 disease1 and was a public health emergency of international concern.2 This paper provides an overview of the global perspective of COVID-19 as it relates to the following three oral healthrelated topics: the impact of COVID-19 on oral health care providers and dental practice; how COVID-19 affects access to oral health care services and unmet needs among vulnerable populations; and OC TOBER 2 0 2 0 507

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understanding the barriers and challenges to global access to oral health care during the pandemic by sharing perspectives from different regions of the world.

Impact of COVID-19 on Oral Health Care Providers and Dental Practice

The potential risk for COVID-19 infection is a major stress inducer for many oral health care workers, as they are considered high-risk health care providers.3 The lack of a preventive vaccine and effective treatment further heightens this concern, thus placing a high psychological toll on them.4 During dental appointments, avoiding close contact and adhering to social distancing guidelines creates myriad issues for dental providers. Infectious agents can be transmitted between patients and oral health workers in the dental clinic environment through infected air droplets, saliva and instruments contaminated with secretions.5 The close person-toperson contact during dental clinical care and the spatters and aerosols produced during routine dental treatments further increase the risk of transmission of pathogens from patients to dentists. This risk is heightened when managing asymptomatic carriers of disease pathogens or those in the postinfection “window period” during which antibodies cannot be detected.6,7 The long incubation period of seven to 24 days for COVID-19 and the risk of exposure to the pathogen through the respiratory system during face-to-face contact8 and through the oral cavity8,9 and gingiva fluid10 during dental procedures are of great concern to dental care providers.7 The use of instruments that create aerosol droplets generate cross-infection challenges when providing dental care.1,11 Thus, developing and implementing rigorous 508 OC TOBER

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and effective infection and management control protocols for dental practitioners and other oral health care providers is crucial, especially in nations with large numbers of COVID-19 cases.9

COVID-19 Clinical Oral Health Care Prevention Approach: The Hierarchy of Controls

In the midst of the COVID-19 pandemic, resources like the hierarchy of controls framework (FIGURE) can be especially helpful for dental providers as they navigate appropriate safety measures to adopt during clinical visits. Following the hierarchy of controls framework normally leads to the implementation of inherently safer systems with significantly reduced risk of illness or injury.12,13 The hierarchy of controls framework outlines an inverse pyramid of five levels of protective measures in order of most to least effective as follows.12 The five levels include: elimination and substitution (changes in equipment or procedures that reduce exposure to hazards); engineering controls (isolating employees from hazards connected to their work by taking measures to reduce exposures to such hazards); administrative controls (implementing changes in work policies or procedures in order to minimize exposure to hazards); and the use of personal protective equipment (face masks, face shields, gloves, goggles and respiratory protection as appropriate).

The Need for Minimally Invasive Dentistry and Teledentistry in Light of the COVID-19 Pandemic

The COVID-19 pandemic has highlighted the importance of using minimally invasive restorations and procedures within dentistry. The most recent recommendations published by the Centers for Disease Control and Prevention (CDC) urge dentists

to avoid, when possible, procedures that might produce aerosols.14 This includes avoiding the use of dental handpieces, air/water syringes and ultrasonic scalers that place dentists at a higher risk because the spray created by items such as handpieces, ultrasonic scalers and air-water syringes can contain particle droplets of water, saliva, microorganisms and other materials.14,15 While surgical masks can be used to protect an individual’s mouth and nose from droplets, they cannot be relied upon to prevent wearers from inhaling infectious agents that exist in the air.14 In circumstances that do require aerosol-generative procedures, the CDC advises dentists to minimize aerosols by using four-handed dentistry, dental dams and high-volume evacuators (HVEs).14 The standard HVE device used in dentistry has a large opening and is attached to an evacuation system that will remove a volume of air up to 100 cubic feet per minute. HVEs control the spray from aerosols and can reduce the risk of transmitting the virus. Studies have shown that HVEs can reduce 90% to 98% of aerosols regardless of the source. As there is no single solution that will provide complete protection, a combination of protective measures including PPE, preprocedural rinses, prepolishing, an advanced air filtration system and HVEs offers the most effective and practical method of reducing the overall risk of infection from viruses such as COVID-19.16 The emerging trend of teledentistry/ telehealth started before the COVID-19 pandemic, but the pandemic has put this option at the forefront as it serves as a means to avoid potential exposure to aerosolized infectious agents for those patients with nonemergent needs. Teledentistry allows for the exchange of clinical

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Most effective

information and images over remote distances for consultation, diagnosis, treatment planning, dental care and education.17,18 For example, dentists and other oral health care providers could conduct an initial oral health assessment via phone or computer. Based on the initial assessment, the provider can then rank appointment urgency remotely to arrange for in-person visits when needed.

COVID-19 and Access to Services and Unmet Needs of Vulnerable Populations

In response to the initial fear and concern about contracting COVID-19, large numbers of private and public clinics were closed and some were open only for emergency care.3 Closures also came per recommendations from the CDC in an effort to preserve PPE for frontline health care workers.14 The impact of this response is not only about the loss of revenue for the dental clinics and the dental workforce, but also the inability of individuals to access routine oral health care with significant implications for vulnerable populations. Vulnerable and special needs populations, such as medically compromised patients, the elderly, young children and individuals with disabilities, are reliant upon routine health care to prevent deterioration of their overall health, including oral health. It is estimated that 15% of the world’s population experience some form of disability and 20% of the estimated global population experience significant disabilities.19 Many persons with disabilities also have health comorbidities that compromise their health and increase their need for routine oral health care.19 The inability to access routine dental health care will have a significant negative impact

Elimination

Physically remove the hazard

Substitution

Replace the hazard

Engineering controls

Isolate people from the hazard

Administrative controls

Change the way people work

PPE

Protect the worker with personal protective equipment

Least effective • Elimination and substitution are considered the most important of the control levels but are sometimes not available to implement. These controls are the most effective at reducing hazard exposure but are also the most difficult to implement and may require major changes in equipment and procedures. Screening patients before they come into the office and not permitting patients suspected of being COVID-19 positive to come into the office would be considered one method of eliminating COVID-19 from the workplace. • Engineering controls involves isolating employees from hazards connected to their work by taking measures to reduce exposures to such hazards. With COVID-19, engineering controls may include installing high-efficiency air filters and barriers such as plastic sneeze guards, increasing ventilation in the workplace and using specialized negative-pressure ventilation for aerosol-generating procedures. • Administrative controls rely on the worker or employer to implement changes in work policies or procedures in order to minimize

exposure to hazards. Specific administrative controls related to COVID-19 could include encouraging workers to stay home if ill, utilizing teledentistry when possible, staggering shifts to reduce the number of workers on-site at one time, implementing emergency communication plans and providing appropriate COVID-19 education and training for workers in a language and at a level they can understand. Additionally, implementing minimally invasive restorative procedures reduces the risk of exposure at this level. • Personal protective equipment (PPE) includes face masks, face shields, gloves, goggles and respiratory protection as appropriate. Risk-level PPE will vary based on location, so providers should regularly check their governmental health care and occupational safety websites for updates in order to make necessary adjustments. PPE should be specific to the individual worker and must be properly fitted and refitted as needed. Workers should receive proper training on how to consistently wear, remove, clean, store and/or dispose of PPE properly. Inspection, maintenance and replacement of PPE when necessary are also important.

FIGURE . Hierarchy of controls framework.12

on the oral health and quality of life of these vulnerable populations.19 Additionally, people with special health care needs and disabilities are at increased risk of contracting COVID-19 because of multiple factors such as poor access to information, increased risk of poverty, poor housing and sanitation and social and economic exclusion.19,20

Understanding and Addressing Oral Health Disparities in the Context of Macro- and Microsystem Levels as They Relate to COVID-19

Addressing oral health disparities in vulnerable and at-risk populations requires a multifaceted approach, which includes changes at both the macro- and microsystem levels. Macro-level systems OC TOBER 2 0 2 0 509

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operate on a large scale that can affect entire communities, states and countries.21 Micro-level systems operate at the individual level.21 COVID-19 can be considered an example of a macro-level systemic factor. It affects oral health equity and social justice on a global level and can lead to the continuation of privilege for some and discrimination for others based on characteristics such as economic status, gender, age and special needs status.21 For example, at the macro level, policies and governance systems during the COVID-19 pandemic severely impacted access to markets and food, as many countries instituted a lockdown or shelter-in-place policy to restrict movement as a way to contain the pandemic. The inability of individuals to obtain food, especially vulnerable populations that are greatly affected by food insecurities, can impact the maintenance of a healthy diet, which will have implications for the oral health of affected individuals in both the short and long term.22 Scardina and Messina23 clearly outline how poor diet affects dental organogenesis, maxilla growth and skull/facial development and increases the risk of oral diseases. Mandatory shelter-in-place orders resulted in many health care institutions limiting services to emergency care in multiple countries. This has implications for a potential increase in health morbidities associated with oral health care. For example, when patients’ diabetes mellitus and kidney disease conditions deteriorate, the risk of periodontal diseases also increases.24–26 Similarly, COVID-19 is associated with increased risk of developing diabetes mellitus27 and kidney injury,28 thereby being an indirect risk factor for oral diseases. COVID-19 has also been shown to be associated with poor oral 510 OC TOBER

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health, including oral manifestations such as mucosal lesions29 in the mouth, which is unique to the disease.30,31 At an individual (micro) level, childhood difficulty with speech, attention problems in school and negative social interactions and/or lack of social relationships that result from poor oral health can have a lifelong impact.32 Addressing macro-level forces within a health equity and social justice framework can have a positive impact on microlevel systemic factors. This affects an individual’s overall health in various ways

The inability of individuals to obtain food can impact the maintenance of a healthy diet, which will have implications for the oral health of affected individuals. that include creating a culture of oral health that promotes a comprehensive approach to total health and wellness as a continuum of medical/dental integration throughout the COVID-19 pandemic and making it possible to access culturally and linguistically sensitive providers through telehealth programs to reduce the burden of disease throughout the pandemic.

Understanding the Barriers and Challenges Related to Global Access and Oral Health Care During the Pandemic: Worldview Perspectives The WHO Global Perspective on COVID-19

Recently, the WHO published guidelines on the considerations for essential oral health services during the

COVID-19 pandemic,33 confirming the recommendations produced by the U.S. Occupational Safety and Health Administration (OSHA) that divided job tasks into four risk exposure levels for COVID-19, from low to very-high risk. These risk categories affect all dental health care personnel: dentists, dental hygienists and dental assistants.34 Thousands of dentists from35 low-, middleand high-income countries expressed their concerns about the impact of the COVID-19 pandemic on their practice in one of the largest global surveys in recent history.35 The major concerns included risk of contagion, testing, transfer of dental care costs to patients due to increasing PPE expenses and how teledentistry will fit into the field of dentistry.35 The University California, Los Angeles (UCLA) School of Dentistry Section of Pediatric Dentistry Department designed and disseminated a survey in conjunction with the WHO to assess the impact COVID-19 had on dentistry at a global level. As part of this survey, UCLA included several questions to assess the financial impact of the pandemic as well as quality of life of U.S. dentists who completed the survey. Dentists reported experiencing a significant amount of financial hardship. They reported a significant reduction in the hours spent at the office, in patient visits and procedures being performed. Regarding the qualityof-life questions, responses indicated that a majority of dentists were not having trouble concentrating, were not feeling sadness or depression and were not having difficulty completing routine activities.

Access to Dental Care at the Global Level During COVID-19: A Circuitous Route

According to the WHO Department of Noncommunicable Diseases in Geneva, urgent dental care has been the second

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most disrupted service in 122 countries during the pandemic.36 This department consists of the WHO Oral Health Program along with cardiovascular diseases, chronic respiratory diseases, diabetes, cancers and mental health conditions. Despite the influence of oral infections on diabetes and cardiovascular diseases36 and the recognized need to ensure continuity of care for pain and orofacial infections and trauma, even urgent dental care has been curtailed during the pandemic. Several reports and recommendations on workflows, guidelines and hygiene protocols were issued for dentists all over the world.37,38 Webinars, virtual conferences and online lectures complemented the spectrum of measures taken in dental facilities, universities and dental hospitals to ensure timely and appropriate information management and support. However, there is still a lack of published data on nosocomial infections associated with the movement of patients seeking treatment for dental pain during the pandemic. Additionally, the evaluation of broader aspects of service provision, such as the establishment of regional urgency shifts and dental services, triage procedures, teleconsultation scope and standards, is still in its infancy. Restriction of interactions between patients and dental practitioners in offices or hospitals during lockdown is only one of the multiple aspects affecting access to oral care at the global level. Unavailability of qualified oral health professionals, distance to services, poverty, out-ofpocket expenditures,39 reimbursement fees,40 lack of universal health coverage, expensive dental material supplies and underfunded health systems continue to be barriers to care. While these barriers to care are not new, they have been exacerbated by the pandemic. In the postpandemic recovery context, there will be a need to reach out to

communities to assess their needs (especially in underserved and vulnerable populations), gather relevant data and evaluate findings to facilitate the development of projects with immediate benefit for preventive/ therapeutic intervention and to establish policy dialogue with decision-makers at the country level.

Asian Perspective: India

The first case of COVID-19 reported in India was on Jan. 30, 2020. The number of active cases continues to increase (approximately 12.4 million

The concept of teledentistry has come to the forefront, and it has become a mandate to call each patient beforehand to ascertain the level of need for the visit. cases at the time of this writing), and as a result, the dental community faces a challenge to define the “new normal” of dentistry while prioritizing quality dental care for patients. For the first time ever in India, the government has become involved in establishing guidelines for dental practices. While dentists have continued to provide treatment following the guidelines established by the government, these guidelines are subject to change and have the potential of becoming more stringent as the number of COVID-19 cases increases. The fear of contracting the disease in dental clinics has created a change in the psyche of both dentists and patients in India. Initially, more than 90% of dentists closed their clinics and struggled to determine the best way to

operate and sustain their practices under the changed conditions. Many dentists suspended all emergency treatments for their patients, and some dentists have reported increased levels of depression.2 Patients are no longer being treated on a “first-come, first-served” basis; instead, they are treated based on the emergency level of the procedure. The concept of teledentistry has come to the forefront, and it has become a mandate to call each patient beforehand to ascertain the level of need for the visit.41 Additionally, inquiring about the personal, travel and medical history of patients has become mandated among dental practices. At the structural level, precautionary measures at dental clinics in India focus on the design of the office, the need for a well-ventilated operatory with appropriate air flow and the use of negative-pressure equipment in addition to disinfection measures in order to maintain hygiene and sanitation after every patient. Before COVID-19, gloves and head caps were the only protective measures for dentists, but now PPE kits are mandatory while examining or treating patients.42 Patients have also been made aware of the hygiene measures implemented in dental clinics and the need for efficient sterilization. Currently, zones in India are categorized based upon the number of active cases: red (greatest number of cases), orange (mid-level number of cases) and green (fewest number of cases). Dentists have to modify their treatment modalities depending upon the zone to which the patient belongs; as such, where the clinic is situated will greatly impact dental practices. Since initial closures, dentists have been advised to conduct only emergency dental procedures in red zones, whereas full dental consultation is allowed in orange and green zones under all precautionary measures. OC TOBER 2 0 2 0 511

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African Perspective: Nigeria

The first case of COVID-19 in Nigeria was reported on Feb. 27, 2020, traced to an international traveler from Italy. Since then, the number of COVID-19 cases in Nigeria and the continent of Africa began to increase exponentially. As of Aug. 1, 2020, there were 926,917 COVID-19 cases in Africa. This constituted 5.3% of the 17,579,197 cases of COVID-19 reported globally at that time.43 There were also 19,645 deaths from COVID-19. Nigeria had the third highest number of cases in African countries (43,151) after South Africa (493,183) and Egypt (94,078) and the fourth highest number of deaths (879) after South Africa (8,005), Egypt (4,805) and Algeria (1,210).43 The Nigerian government responded to the pandemic by establishing a presidential task force that developed a national strategy for the COVID-19 response. It shut down schools, closed state borders and imposed lockdowns. The economic impact has been huge, with a drastic increase in food insecurity due to the pandemic’s disruption of farming, food supply chains and trade.44 The Nigerian workforce, 1.15 million people, 83.2% of whom operate in the informal sector, could not be effectively reached with cash and food distribution, especially the most vulnerable households.44 The decade-long conflicts in some parts of the country have increased the risk of COVID-19 for over 7 million Nigerians in conflict areas, approximately 2 million people in internally displaced persons camps and nearly 475,000 people in highly congested camps. These areas will be most affected by the pandemic, especially because they currently have a high prevalence of comorbidities with other diseases such as endemic cholera, malaria, Lassa fever, measles and chronic malnutrition. The country 512 OC TOBER

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has also had to deal with distrust and disbelief about the pandemic from large sections of the community, thus limiting individuals’ use of face masks in public and social distancing.44 Public hospitals were initially open to emergency cases only to enable hospitals to focus on managing patients with COVID-19 infection and reducing the risk of hospital transmission of infection to nonCOVID-19 patients. However, on April 18, 2020, the coordinator of the presidential task force issued a directive to reach out to the relevant professional associations to

The Nigerian government responded to the pandemic by establishing a presidential task force that developed a national strategy for the COVID-19 response. draft operational guidelines for resuming nonemergency patient care. The Division of Dentistry also received this directive, and the Nigerian Dental Association was charged with the responsibility of developing guidelines applicable to both public and private dental practice sectors. The guidelines stipulated the use of advice, analgesics and antimicrobials for the management of nonemergency dental care, identified what cases are considered dental emergencies and should be handled during the pandemic, how staff and patients are to be evaluated before entering the main clinic, procedural practices for patients, posttherapy instructions, waste management and management of patients with COVID-19 symptoms. Screening questions now include questions about international travel history and travel from high-epidemic

areas as part of the patient’s medical history. The use of long-sleeved scrubs, waterproof aprons, disposable gloves and face shields are part of the mandatory PPE to be worn while conducting nonaerosolgenerating procedures. When conducting aerosol-generating procedures, respirators are expected to be worn in addition to wearing full surgical gowns, waterproof aprons, full-face shields and covered shoes. While public and private clinics that shut down during the early days of the COVID-19 pandemic are gradually opening to provide services to the public, precautionary measures have been instituted. Private dental clinics are not allowed to manage patients with COVID-19 symptoms. In the public setting, symptomatic and asymptomatic patients with COVID-19 infections are expected to be referred to designated COVID-19 management centers for care in any of the 37 states in Nigeria. Finally, the populations who have limited access to oral health care and who had traditionally been reached through outreach and sponsored programs45 will be at a huge loss during this period where outreach has been suspended in order to limit close social contact. In effect, COVID-19 may have further widened the disparities in access to oral health care among these vulnerable populations in Nigeria, thereby worsening oral health inequity in the country.

European Perspective: Italy, Germany and Switzerland

Italian perspective. Italy saw a rapid increase of COVID-19 at the beginning of the pandemic. As of May 2020, Italy was still among the European countries with the highest number of COVID-19 cases. The majority of cases were concentrated in the northern part of the country (Lombardy).37 Health care workers were

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greatly impacted by the pandemic. As of May 12, 2020, the official number of COVID-19-infected health care workers was 21,981. A survey carried out during the peak of the pandemic provided some insight into the impact of COVID-19 on dental professionals, and a high percentage of the dentists reported symptoms attributable to the infection. German perspective. According to the Ministry of Health in Bavaria in southern Germany, the first confirmed case of COVID-19 in Germany was on Jan. 27, 2020. Since then, new cases have been reported continuously and several patients have been hospitalized. On Feb. 28, 2020, the Robert KochInstitute in Berlin assessed the risk of COVID-19 for Germany and initially classified it as “low to moderate” for the population.46 This was revised on March 17, 2020, to reclassify COVID-19 as a “high-level risk” for the population in Germany, and for at-risk groups the risk level was “very high.”46 This was taken as an opportunity for the Bundestag to identify an epidemic situation of national importance, and on March 27, 2020, it passed a law entitled “Law to protect the population in the event of an epidemic situation of national importance.”47 This allowed orders to be issued at the federal level in the federal health system without the consent of the Federal Council. Since then, a worldwide travel warning was issued, nonessential travel to the EU was restricted, numerous businesses were closed and an entry ban for thirdcountry nationals was implemented. Regarding dental services during the lockdown, many regions in Germany restricted dental care to emergency care only. Therefore, elective procedures were to be postponed and risk groups were to be treated with special protective measures.48 Nevertheless, dentists with a health insurance fund

license (legally insured, state-owned) were obligated to treat patients. The Swiss perspective. In early February 2020, the Swiss canton of Ticino in the south of Switzerland, bordering on northern Italy and the Lombardy region not far from Milan, identified two COVID-19-positive individuals. The increase was so rapid that on Feb. 28, 2020, the Swiss Federal Council assessed the situation as a “special situation” under the Epidemics Act and adopted the Ordinance on Measures to Combat Coronavirus (COVID-19). A campaign by the Swiss Federal Office of

A worldwide travel warning was issued, travel to the EU was restricted, numerous businesses were closed and an entry ban for third-country nationals was implemented. Public Health was launched on March 1, 2020, with hygiene recommendations for protection against COVID-19.49 The Swiss Dental Association (SSO) developed a protection clause for dental surgeries during the period of the emergency legislation passed by the Federal Office on March 16, 2020.50 Furthermore, also on March 16, 2020, the Swiss Federal Council defined the “extraordinary situation” due to the highest danger level with measures to protect the population in accordance with the Epidemics Act. As a result, all shops, restaurants, bars as well as entertainment and leisure facilities, with the exception of grocery stores and health care facilities, were closed until April 19, 2020.49 The “extraordinary situation” was later extended until April 26, 2020. However, according to the COVID-19 Ordinance, practices and

health care facilities must have a protection clause that is appropriate to the situation and operation.49 The “Smart Restart” initiative by the Swiss Dental Association (SSO) allowed for individual implementation of protective measures such as PPE and has made it possible to reopen dental practices for patient care since April 27, 2020, largely without restrictions.51

United States Perspective

On March 13, 2020, the U.S. government responded to the COVID-19 pandemic by declaring a national emergency. Following this, the CDC and the American Dental Association (ADA) recommended that dentists nationwide defer elective dental treatment and focus on emergency care. This was further reinforced by OSHA’s recommendation that dental treatment during the COVID-19 pandemic use a combination of standard contact precautions and droplet precautions, including eye protection (e.g., goggles or face shields) to protect dental professionals performing patient care that does not involve aerosol-generating procedures on individuals not suspected or confirmed to be COVID-19 positive. When performing aerosol-generating procedures, additional airborne precautions were added to protect dental professionals. While the lack of national precautionary guidance and severe PPE shortages led to the closure of many dental offices early in the pandemic, by May 2020, the ADA and several states in the U.S. issued guidance for reopening dental practices. In March 2020, the ADA Health Policy Institute initiated a nationwide biweekly poll on the economic conditions during the pandemic to quantify the magnitude of the pandemic’s impact on dental practices over time. The survey results showed that by July 27, 2020, nearly all offices were open; however, patient volume was estimated OC TOBER 2 0 2 0 513

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to be 73% of pre-COVID-19 levels. Dental offices continued to experience N95 respirator and PPE shortages and higher expenses for instituting PPE. An encouraging finding was that data from consumer polling indicated 80% of adults were very comfortable visiting the dentist now, reflecting a high level of confidence in the infection control measures being undertaken. In the U.S., COVID-19 has particularly affected certain racial and ethnic minority groups. Data show that African Americans continue to experience the highest overall COVID-19 mortality rates — about 2.3 times as high as the rate for whites and Asians.45 According to the CDC, inequities in the social determinants of health, such as living conditions, poverty, health care access and underlying medical conditions affecting these groups, increase their risks for infection and death.52 African Americans and Latinos are disproportionately represented in certain occupational settings that put them at increased risk of contracting the virus due to several factors, such as close contact with others, inability to work from home, a lack of sick days, crowded housing and the use of public transportation.

California Perspective

In California, statewide shelterin-place and “safer-at-home” orders began on March 16, 2020, and remained in place in most cities until mid-June when they were loosened. Similar to other countries, all nonemergent dental services were required to shut down. As the provision of nonemergent dental services slowly resumes in California, dental clinics and dental health care personnel are instructed to follow the recommendations and guidelines set forth by the CDC and the California Department of Public Health (CDPH) 514 OC TOBER

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and Cal/OSHA guidance for resuming deferred and preventive dental care. In addition to these guidelines, the California Dental Association (CDA) developed practice guidance that worked in conjunction with the guidelines set forth by the CDPH.53 These guidelines stipulate that dental clinics should balance the need to provide necessary services while minimizing risk to patients and staff. Before providing any care, it is important to ensure that appropriate PPE and sanitation supplies are

African Americans and Latinos are disproportionately represented in certain occupational settings that put them at increased risk of contracting the virus. available to support patient volume and that updated engineering controls, work practice protocols and infection control measures are in place.

Discussion

The COVID-19 pandemic has had a major impact on dental professionals and the delivery of dental care worldwide. Not only have dental practitioners been required to implement rigorous and effective infection and management control protocols in the dental setting for both providers and patients, they will also have to come up with solutions to ensure the most vulnerable populations are able to access needed dental care. The pandemic has also impacted the mental and social psyche of both

dental practitioners and patients. This paper presents some of the challenges currently being faced by dental professionals worldwide and discusses potential solutions to these challenges. The following is a summary of key findings. Early on in the pandemic, dental care was restricted to emergency cases in much of the world. However, as nonemergent dental care has slowly resumed, several reports and recommendations on workflows, guidelines and hygiene protocols were issued for dentists worldwide.37,38 Mandates have included the use of PPE for providers (e.g., face masks, face shields, goggles, gloves and respiratory protection) and highlighted the importance of using minimally invasive restorations and procedures to reduce the spread of infection. Structural changes have also been instituted in many clinic environments to reduce the risk of transmission (e.g., improving office ventilation with appropriate air flow, use of negativepressure equipment and disinfection measures to maintain hygiene and sanitation after every patient.) The large number of private and public clinics that were closed early in the pandemic resulted in the inability of individuals to access routine oral health care, which has significant implications for vulnerable and special needs populations who are reliant upon routine care to prevent deterioration of their overall health. To address this concern, practitioners have turned to the concept of teledentistry or “virtual dental check-ups” to help reduce the need for in-person visits and increase access to care for vulnerable and underserved populations. However, reaching the very poor or individuals who don’t have access to technology is still a gap that needs to be addressed.

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Finally, the fear of contracting COVID-19 in dental clinics has created a change in the psyche of both dentists and patients. Many dental professionals have still not determined the best way to operate and sustain their practice under the changed conditions, and some dentists have reported increased levels of depression.2 Additionally, patients in some countries continue to report hesitancy regarding going to the dentists for fear of contracting COVID-19.3 Teledentistry comes to the forefront on how to relieve some of these stressors for both providers and patients, but more research is needed to better understand the psychosocial impact of COVID-19 on dental providers and how best to address this problem.

Conclusion

The COVID-19 pandemic has created many challenges for the field of dentistry and oral health care, many of which will have lasting impacts, especially economically and financially. The oral health care system was already dealing with issues of access to care and medical/dental integration as a way of maintaining continuity of care as well as addressing oral health disparities. All of these complex issues have been exacerbated by the COVID-19 pandemic. As the pandemic draws on, and continues, it will be important for dental practitioners and other oral health care providers to continue to assess issues that arise in the field and keep finding ways and opportunities to be creative and to provide care to the most at-risk and vulnerable populations worldwide. n ACKNOWLEDGMENTS We express our sincere gratitude to all of our authors, additional contributor Jayanth Kumar, DDS, MPH, and our research assistants Helen Lindau and Janni

Nadjat-Haiem who are dedicated to advancing dentistry and oral health practices while addressing the difficulties that the COVID-19 pandemic have presented for the field. REFERENCES 1. Barabari P, Moharamzadeh K. Novel coronavirus (COVID-19) and dentistry – A comprehensive review of literature. Dent J (Basel) 2020 May 21;8(2):53. doi:10.3390/dj8020053. 2. Gambhir RS, Dhaliwal JS, Aggarwal A, Anand S, Anand V, Bhangu AK. COVID-19: A survey on knowledge, awareness and hygiene practices among dental health professionals in an Indian scenario. Rocz Panstw Zakl Hig 2020;7(2):223– 229. doi: 10.32394/rpzh.2020.0115. 3. Ahmed MA, Jouhar R, Ahmed N, et al. Fear and practice modifications among dentists to combat novel coronavirus disease (COVID-19) outbreak. Int J Environ Res Public Health 2020 Apr 19;17(8):2821. doi:10.3390/ijerph17082821. 4. Lai J, Ma S, Wang Y, et al. Factors associated with mental health outcomes among health care workers exposed to coronavirus disease 2019. JAMA Netw Open 2020 Mar;3(3):e203976. doi:10.1001/ jamanetworkopen.2020.3976. 5. Baseer MA, Rahman G, Yassin MA. Infection control practices in dental school: A patient perspective from Saudi Arabia. Dent Res J (Isfahan) 2013 Jan;10(1):25–30. doi:10.4103/1735-3327.111763. 6. Cagetti MG, Cairoli JL, Senna A, Campus G. COVID-19 outbreak in north Italy: An overview on dentistry. A questionnaire survey. Int J Environ Res Public Health 2020 May 28;17(11):3835. doi:10.3390/ijerph17113835. 7. Tada A, Watanabe M, Senpuku H. Factors influencing compliance with infection control practice in Japanese dentists. Int J Occup Environ Med 2014 Jan;5(1):24–31. PMID: 24463798. 8. Wang W-K, Chen S-Y, Liu I-J, et al. Detection of SARSassociated coronavirus in throat wash and saliva in early diagnosis. Emerg Infect Dis 2004 Jul;10(7):1213–1219. doi:10.3201/eid1007.031113. 9. Ceron JJ, Lamy E, Martinez-Subiela S, et al. Use of saliva for diagnosis and monitoring the SARS-CoV-2: A general perspective. J Clin Med 2020 May 15;9(5)1491. doi:10.3390/jcm9051491. 10. Supriya Kheur, Mohit Kheur, Archana A. Gupta, A. Thirumal Raj. Is the gingival sulcus a potential niche for SARS-Corona virus-2? Med Hypotheses 2020 May 27;143:109892. doi: 10.1016/j.mehy.2020.109892. Online ahead of print. europepmc.org/article/pmc/ pmc7255245. Accessed July 27, 2020. 11. Balaji SM. COVID-19 — Future of dentistry. Indian J Dent Res Mar–Apr 2020;31(2):167–168. doi:10.4103/ ijdr.IJDR_347_20. 12. Centers for Disease Control and Prevention/NIOSH. Hierarchy of controls. Published June 17, 2020. www.cdc. gov/niosh/topics/hierarchy/default.html. Accessed July 21, 2020. 13. Ramos-Gomez F. Evidence-based ECC prevention, intervention and management strategies. J Mich Dent Assoc published online July 2020. www.michigandental. org/Portals/pro/Journals/July%202020/html5/index. html?page=1&noflash. Accessed Aug. 27, 2020.

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for the management of dental practice. Int J Environ Res Public Health 2020 May 11;17(9):3325. doi:10.3390/ ijerph17093325. 38. FDI World Dental Federation. FDI COVID-19 resource library. Published March 31, 2020. www.fdiworlddental.org/ fdi-covid-19-resource-library. Accessed Aug. 14, 2020. 39. Medina-Solís CE, Ávila-Burgos L, Márquez-Corona M de L, et al. Out-of-pocket expenditures on dental care for schoolchildren aged 6 to 12 years: A cross-sectional estimate in a less-developed country setting. Int J Environ Res Public Health 2019; Jun 5;16(11):1997. doi: 10.3390/ ijerph16111997. 40. Ortiz-Ospina E, Roser M. Financing healthcare. Our World Data. Published online June 16, 2017. Accessed Aug. 14, 2020. ourworldindata.org/financing-healthcare. 41. Jevon P, Shamsi S. COVID-19 and medical emergencies in the dental practice. Br Dent J 2020;229(1):19–24. doi:10.1038/s41415-020-1782-5. 42. Centers for Disease Control and Prevention. Standard precautions. Published Jan. 24, 2020. www.cdc.gov/ oralhealth/infectioncontrol/summary-infection-preventionpractices/standard-precautions.html. Accessed July 27, 2020. 43. European Centre for Disease Prevention and Control. COVID-19 situation update worldwide, as of 3 August 2020. www.ecdc.europa.eu/en/geographical-distribution-2019ncov-cases. Accessed Aug. 3, 2020. 44. Chatham House. Nigeria’s political leaders need to win trust to tackle COVID-19. www.chathamhouse.org/expert/ comment/nigeria-s-political-leaders-need-win-trust-tacklecovid-19. Accessed Aug. 3, 2020. 45. APM Research Lab. COVID-19 deaths analyzed by race and ethnicity. www.apmresearchlab.org/covid/deaths-byrace. Accessed Aug. 25, 2020. 46. RKI Robert Koch Institution. COVID-19 in Germany. www.rki.de/EN/Home/homepage_node.html. Accessed Aug. 28, 2020.

47. Bundesgesetzblatt Teil I. Law to protect the population in the event of an epidemic situation of national concern. 2020;(14):587. 48. e.V. (BZÄK) B-A der DZ. Sars-CoV-2/COVID 19. Bundeszahnärztekammer — Arbeitsgemeinschaft der Deutschen Zahnärztekammern e.V. (BZÄK). www.bzaek.de/ berufsausuebung/sars-cov-2covid-19.html. Accessed Aug. 28, 2020. 49. Swiss Federal Office of Public Health FOPH. New Coronavirus: Situation in Switzerland. www.bag.admin. ch/bag/en/home/krankheiten/ausbrueche-epidemienpandemien/aktuelle-ausbrueche-epidemien/novel-cov/ situation-schweiz-und-international.html. Accessed Aug. 28, 2020. 50. Association of Cantonal Dentists of Switzerland (VKZS) and Swiss Dental Association SSO. Position paper. Covid-19 guidelines for the operation of a dental practice during the Covid-19 pandemic. www.sso.ch/fileadmin/upload_sso/5_ Newsletter/2020/Covid-19-Positionspapier_VKZS_4_D.pdf. Accessed Aug. 28, 2020. 51. Swiss Dental Association (SSO). Frequently Asked Questions about Smart Restart. COVID-19 Communication. translate.google.com/translate?hl=en&sl=de&u=https:// www.sso.ch/fileadmin/upload_sso/5_ Newsletter/2020/200424_FAQ-Smart-Restart-D. pdf&prev=search&pto=aue. Accessed Aug. 27, 2020. 52. Centers for Disease Control and Prevention. Communities, schools, workplaces and events. Published April 30, 2020. www.cdc.gov/coronavirus/2019-ncov/community/healthequity/race-ethnicity.html. Accessed Aug. 26, 2020. 53. California Dental Association. Practice Management. www.cda.org/Home/Practice/Back-to-Practice/PracticeManagement. Accessed Aug. 26, 2020. THE CORRESPONDING AUTHOR, Francisco Ramos-Gomez, DDS, MS, MPH, can be reached at frg@dentistry.ucla.edu.

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• Disposable • Inexpensive • Non-Toxic

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Dentistry in the Context of COVID-19 : Oral Pathologists’ Perspectives Based on a Compilation of Data Paulo Victor Mendes Penafort, DDS; Tayná Figueiredo Maciel, DDS; Ana Paula Ferreira Souza, DDS; Tássia Caroline da Costa Mendes, DDS; Renata Gualberto Cunha, DDS, MSc; Naiza Menezes Medeiros Abrahim, DDS, MSc; Lucileide Castro Oliveira, DDS, MSc; Jeconias Câmara, DDS, MSc; Paulo Henrique Braz-Silva, DDS, PhD; and Tatiana Nayara Libório-Kimura, DDS, PhD

a b s t r a c t A review of articles related to SARS-CoV-2 indexed in databases,

primarily PubMed, from December 2019 to August 2020 as well as historical support literature was conducted addressing relevant aspects that oral pathologists, stomatologists and general dentists need to be aware of in the context of the COVID-19 pandemic. The discussion was based on the contextualization of general aspects as a basis for understanding of the scenario dental professionals are currently facing.

AUTHORS Paulo Victor Mendes Penafort, DDS, is an oral an maxillofacial pathology resident at the Federal University of Amazonas. Tayná Figueiredo Maciel, DDS, is an oral and maxillofacial pathology resident at the Federal University of Amazonas. Ana Paula Ferreira Souza, DDS, is an oral and maxillofacial pathology resident at the Federal University of Amazonas. Tássia Caroline da Costa Mendes, DDS, is an oral and maxillofacial pathology resident at the Federal University of Amazonas.

Renata Gualberto Cunha, DDS, MSc, is an assistant professor and preceptor of the residency program of oral and maxillofacial pathology at the Federal University of Amazonas. Naiza Menezes Medeiros Abrahim, DDS, MSc, is an assistant professor and preceptor of the residency program of oral and maxillofacial pathology at the Federal University of Amazonas. Lucileide Castro Oliveira, DDS, MSc, is an assistant professor and preceptor of

the residency program of oral and maxillofacial pathology at the Federal University of Amazonas. Jeconias Câmara, DDS, MSc, is an adjunct professor and coordinator of the residency program of oral and maxillofacial pathology at the Federal University of Amazonas. Paulo Henrique Braz-Silva, DDS, PhD, is an assistant professor in the department of stomatology in the School of Dentistry and in the laboratory of virology at the Institute of Tropical Medicine of São Paulo,

School of Medicine at the University of São Paulo. Tatiana Nayara Libório-Kimura, DDS, PhD, is an associate professor in the department of pathology and legal medicine and vicecoordinator of the residency program of oral and maxillofacial pathology at the Federal University of Amazonas in Manaus, Brazil. Conflict of Interest Disclosure for all authors: None reported.

he new coronavirus pandemic has become a true challenge for health professionals around the world, significantly affecting dental practitioners in private offices, universities and research institutes.1,2 The World Health Organization (WHO) declared this pandemic on March 11, 2020,3 and according to data from June 22, 2020, there were 8,860,331 confirmed cases of COVID-19 worldwide at that time, including 465,740 deaths, as reported by the WHO.4 Despite the increasing rise in studies on COVID-19 in both medical and dental contexts, little is known about the possible general effects of the disease in view of the countless variables related to geographical OC TOBER 2 0 2 0 517

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aspects, type of affected population, individual immunity and profile of the response to the proposed treatments. In addition, a possible genetic predisposition to the disease has been recently raised that individuals with blood type O would be more protected than those with blood type A, who would be at higher risk.5,6 There is no treatment for the disease, and the therapeutic perspectives are based on existing drugs used for other diseases. Given the severity of the pandemic, the optimal design for clinical trials is faced with an unfavorable scenario due to recruitment difficulty, methodology for control group design and steps of blinding and randomization, which make it even more difficult to establish an effective treatment compatible with the majority of the population.7,8 In this sense, the most viable way in the context of dentistry is to find the pathogenic mechanisms of the disease, its local and systemic effects and how they affect oral medicine and pathology. From this, it is possible to contribute to the guidance of clinical practices, routine laboratory tests and histopathological reports in accordance with biosafety issues.2,9 It is important to know not only the disease, but also the possible treatments available (even if not proven), as they may or may not have oral repercussions requiring attention during the diagnostic process. Also, the underlying disease itself may affect oral soft tissues in which vesicular-bullous lesions, ulcerated wounds, aphthous-like ulcerations and erythematous macules are the current signs.10–17 In addition, saliva contains biomarkers that are used to diagnose several diseases, thus being a promising source in the context of COVID-19. We have provided information about the history of coronavirus in the context of pandemics, general aspects of SARS-CoV-2 and signs and symptoms 518 OC TOBER

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of the disease including extrapulmonary manifestations. Despite the scarcity of published studies on the relation between dentistry and COVID-19, especially in the field of oral pathology, we provide information on oral manifestations observed in patients with COVID-19 and on emerging potential treatments of the disease, including possible implications to oral mucosal lesions with which dentists should be familiarized. We also present aspects of dental practice related to COVID-19 and the oral pathology practice in the context of COVID-19.

In 2012, a man attended a health service and reported common cold symptoms and shortness of breath similar to those found in the 2002 SARS pandemic. History of Coronavirus in the Context of Pandemics

Since the beginning of the 21st century, viruses of the Coronaviridae family have been responsible for diseases characterized by serious damage to the respiratory system,18 causing flulike symptoms and acute respiratory distress. These viruses emerged in China in 2002, resulting in a pandemic of severe acute respiratory syndrome (SARS) caused by SARS-CoV.19 In June 2012 in Saudi Arabia, a man attended a health service and reported common cold symptoms and shortness of breath similar to those found in the 2002 SARS pandemic. The man died of acute pneumonia and renal failure. A novel coronavirus was isolated from his sputum and was named MERS-CoV and is the

virus responsible for Middle East respiratory syndrome (MERS).20,21 A study on the 2003 SARS pandemic published in 2007 drew attention to the possibility of a resurgence of SARS through genetic recombination. This might happen in southern China where there is a local culture of eating exotic mammals, such as bats, that are a major reservoir of these viruses. Thus, the need to prepare for a new pandemic should not be ignored.22 In December 2019, approximately 18 years after the first pandemic caused by a coronavirus, health officials from Wuhan City, China, reported cases of patients with pneumonia of unknown cause.23 In January 2020, using samples of bronchoalveolar lavage fluid from these patients, the genome of the novel β genus coronavirus was identified. Initially, the virus and disease were named 2019-nCoV and novel coronavirus-infected pneumonia (NCIP), respectively.24 On Feb. 11, 2020, the virus was named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) based on its genetic similarity to the coronavirus responsible for the 2003 SARS pandemic, and COVID-19 was the name assigned to the disease.25 In less than three months, this disease spread rapidly to the rest of the world, causing the WHO to declare a pandemic on March 11, 2020.3

General Aspects of SARS-CoV-2

SARS-CoV-2 belongs to the family of coronaviruses and corresponds to the seventh member of the group, presenting a genetic compatibility of 70% with SARS-CoV.1 Angiotensin-converting enzyme 2 (ACE2) is a protein that acts as a viral receptor for SARS-CoV-2.26 This receptor was found in approximately

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72 types of human tissue through realtime polymerase chain reaction (RTPCR).27 Studies show that this receptor is expressed on the surface of several cell types and is found more in alveolar epithelial cells of the lung and in small intestine enterocytes. In the nasal and oral mucosa and nasopharynx, this receptor was found in the basal layer of nonkeratinized squamous epithelium.28 The laboratory diagnosis consists of the detection of viral RNA found in respiratory tract samples collected from infected patients using RT-PCR examination.1

Virus Transmission and Signs and Symptoms of the Disease

In a study of 181 patients with COVID-19 whose period of transmission and onset of symptoms were detected, the average incubation period for the virus was 5.1 days.29 The transmission of the virus occurs from person to person through respiratory droplets that are expelled during speech or sneezing, causing a very quick spread of the disease.1 The symptoms found in patients affected by COVID-19 include fever (in most cases), coughing (the second most common symptom), myalgia or fatigue, expectoration and dyspnea. Other symptoms can be found in a minority of cases, such as headache or dizziness, diarrhea, nausea and vomiting. There is, however, the possibility that individuals can carry the virus without developing symptoms, which are asymptomatic cases, and this group presents a danger to the dynamics of virus transmission.30–32 A recently accepted publication using a smell and taste questionnaire was carried out in 12 European hospitals by Lechien et al. (2020). Of the 417 European patients with mild to moderate symptoms of the disease, 85.6% and 88.8% reported olfactory and gustatory dysfunctions, respectively.33

Although these results were criticized, the authors reinforced the previously published information and highlighted that a majority of these patients were not hospitalized and the prevalence of smell and taste loss was based on a reliable self-reported questionnaire.34 A brief communication published on April 27, 2020, draws attention to symptoms such as ageusia and anosmia, which may be the first symptoms or the only ones, especially in patients with few symptoms of COVID-19.35 A study of 72 COVID-19 patients found the presence

There is the possibility that individuals can carry the virus without developing symptoms, and this group presents a danger to the dynamics of virus transmission. of chemosensitive disorders in 73.6% of them, of which 60 patients had various degrees of hyposmia and two patients had anosmia. Taste evaluation revealed hypogeusia in 33 patients and complete ageusia in one patient.36 A case series regarding oral lesions in patients with COVID-19 drew attention to the oral cavity as a target organ for SARS-CoV-2 based on the important role of the ACE2 receptor in the virus cellular entry and therefore, the development of dysgeusia and anosmia in the course of SARSCoV-2 infection could be an early event. For this reason, these manifestations could be considered a possible disease marker by dentists working in the frontlines of the pandemic.17 With focus on the new-onset dysgeusia as a potential early marker of COVID-19

infection, a letter to the editor from Lozada-Nur et al. (2020) raised some new questions regarding dysgeusia as a prognostic marker for the severity of COVID-19, possible patients factors (including medical conditions, medications) that could modify the severity of dysgeusia and also if patients characteristics (such as age, sex, ethnicity and severity of COVID-19) could be related to dysgeusia occurrence. These questions will likely be answered in future studies.37 In parallel, these same authors37 proposed some mechanisms for the establishment of dysgeusia in patients with COVID-19. These mechanisms could be related to several aspects such as direct infection of salivary glands by SARS-CoV-2, possible neurological nature, including direct damage to cells that express ACE2 of the taste buds and peripheral neurosensory chemoreceptors of the taste, also an inflammatory mechanism and oxygen deficiency (hypoxia). Finally, the authors hypothesized that due to an immune response to SARS-CoV-2 viral replication, dysgeusia may arise based on changes in localized cellular zinc homeostasis in oral gustatory cells accompanied or not by hypozincemia. In addition, once the olfactory epithelium is affected by the virus, taste can also be altered, as it is closely linked to the sense of smell. Approximately 80% of the infected patients develop a mild form of the disease, but about 1 in 5 can progress to severe pulmonary involvement, especially the elderly and/or those with comorbidities.38

Extrapulmonary Manifestations of COVID-19

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disease leads to a systemic infection, facilitating its spread throughout the human body. Viral involvement of the central nervous system, for example, can lead to symptoms such as dizziness, headache, impaired consciousness, acute cerebrovascular disease, ataxia and seizure.39 Histopathological analysis of a liver sample taken from a patient who died of COVID-19 revealed the presence of microvesicular steatosis and mild lobular and portal activity, suggesting hepatic impairment due to both viral infection and reaction to the drugs used for treatment of the disease.40 A study of urine samples from 333 patients with COVID-19 revealed renal involvement in 75.4% of the cases (251 of 333). Proteinuria, hematuria and acute renal failure were the most common findings. Renal complications in patients with COVID-19 are associated with a high risk of mortality.41 Expression of the ACE2 receptor in the intestinal epithelium and the infection by SARS-CoV-2 have been associated with gastrointestinal manifestations of coronavirus disease. Diarrhea is the most common symptom, with an occurrence rate ranging from 2% to 50% in studies of COVID-19 patients. This symptom may even precede respiratory symptoms.42 Histopathological analysis of a heart sample taken from a patient who died of COVID-19 did not show any major damage to cardiac tissue, only a few mononuclear inflammatory infiltrates in the interstitium.40 The mechanism by which SARS-CoV-2 causes damage to the myocardium is not well established. It is known that the virus acts through ACE2 receptors and that patients with cardiovascular diseases have a worse prognosis and need special treatment.43 Hematological changes were mainly found in patients with a severe form 520 OC TOBER

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of the disease. In these patients, the lymphocyte count in adult patients may be lower than in patients with the mild form. Other findings in these patients include coagulation indices, such as prothrombin time, activated partial thromboplastin time and D-dimer, which can show higher levels.32

Oral and Skin Manifestations Found in COVID-19

Cutaneous and oral manifestations have been increasingly associated with COVID-19. There are myriad

Based on our search, only six authors had reported oral lesions suspected to be associated with COVID-19, most of them with concomitant skin lesions. studies on clinical presentations, but few attempts to standardize these lesions are observed. Recalcati (2020) was one of the pioneers in observing the concomitance of exanthematous lesions and virus infection in which 20.4% of the 88 patients developed skin lesions (i.e., erythematous rash), generalized urticaria and chicken pox-like vesicles.44 Fernandez-Nieto et al. (2020) evaluated 24 patients who tested positive for SARSCoV-2 by means of a nasopharyngeal swab and reported the appearance of lesions, such as small papules, vesicles and pustules of various sizes, classified into two patterns.45 Vesicular lesions were predominant, representing 54.5% of the 22 patients

evaluated. It is speculated that pseudochilblain and vesicular lesions may be indicators of the disease.46,47 The common microscopic findings in cutaneous biopsies of vesicularbullous lesions proved to be nonspecific, and the lesions do not appear to have pathognomonic characteristics differentiating them from other viral infections with cutaneous manifestations. Therefore, the possibility of dermatological side effects of the drugs used in patients for treatment of the disease should be considered.48 Lesios mimicking the rash pattern like those found in Steven-Johnson syndrome (SJS) have been seen on the skin of patients infected with SARSCoV-2. The oral cavity of patients with SJS is frequently affected, and according to the above-mentioned mimetic pattern, similar oral lesions may appear in patients infected by COVID-19. The use of the drug imatinib may have played a role in the appearance of this manifestation in the patient studied by Lagziel et al. (2020).49 Vesicular-bullous lesions, ulcerations, macules, aphthous-like lesions and petechiae were also reported in the oral cavity of suspected and infected patients. However, reports and reviews are brief compared to those of cutaneous manifestations. Based on our search as of August 2020, approximately eight authors had reported oral lesions suspected to be associated with COVID-19, some with concomitant skin lesions. As the inferences about the viral etiology of SARS-CoV-2 are recent, a standardization of the clinical characteristics cannot yet be established.10–17 In the oral cavity, Martín CarrerasPresas et al. (2020) described lesions in three potential COVID-19 patients; two were suspected cases based on

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TABLE

Clinical and Histopathological Findings of Skin and Mucocutaneous Lesions in Patients With SARS-CoV-2 Author(s) No. of Date of publication patients

Drugs reported in previous 2 weeks

Clinical aspect

Site

Histopathological findings

* Chaux-Bodard et al. 4/12/2020

No information

Irregular ulcer

Side of tongue

•

No information

Fernandez-Nieto et al. 4/15/2020

Hydroxychloroquine, azithromycin

Urticariform rash

Trunk and thighs

•

Perivascular infiltrate of lymphocytes, some eosinophils Upper dermal edema

Magro et al. 4/15/2020

Hydroxychloroquine, azithromycin, remdesivir

Retiform purpura

Buttocks

• • • • •

Hydroxychloroquine, enoxaparin

Dusky purpuric patches

Palms and soles bilaterally

• •

No information

Purpuric reticulated eruption

Chest, legs and arms

• • • •

Striking thrombogenic vasculopathy Extensive necrosis of the epidermis and adnexal structures including the eccrine coil Significant degree of interstitial and perivascular neutrophilia with prominent leukocytoclasia Extensive deposition of C5b-9 within the microvasculature Superficial vascular ectasia and an occlusive arterial thrombus within the deeper reticular dermis in the absence of inflammation Extensive vascular deposits of C5b-9, C3d and C4d throughout the dermis with marked deposition in an occluded artery Modest perivascular lymphocytic infiltrate in the superficial dermis Deeper seated small thrombi within rare venules of the deep dermis Absence of a clear vasculitis Significant vascular deposits of C5b-9 and C4d

Galván Casas et al.04/29/2020

375

Paracetamol, NSAIDs, chloroquine, hydroxychloroquine, lopinavir, ritonavir, tocilizumab systemic corticosteroids, azithromycin

Five major clinical patterns (and several subpatterns) Acral areas of erythema–oedema with some vesicles or pustules (pseudo-chilblain); other vesicular eruptions; urticarial lesions; other maculopapules; and livedo or necrosis Note: Dermatologists also perceived an increased number of herpes zoster cases in patients with COVID-19

Atlas of the manifestations showed the spread of cutaneous lesions all over the body. Among them, at least three patients showied oral involvment, including ulcer and petechies on the palate, lower lip and erythema in the gingiva.

No information

Ahouach et al. 4/30/2020

Paracetamol

Maculopapular lesions

Limbs and trunk

• • •

Slight spongiosis Basal cell vacuolation Mild perivascular lymphocytic infiltrate

Diaz-Guimaraens et al. 4/30/2020

None

Erythematous macules, papules and petechiae

Buttocks, popliteal fossae, proximal anterior thighs and lower abdomen

•

Superficial perivascular lymphocytic infiltrate with abundant red cell extravasation Focal papillary edema along with focal parakeratosis and isolated dyskeratotic cells No features of thrombotic vasculopathy were

• •

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C O N T I N U E D F R O M P R E V I O U S PAG E

Author(s) Date of publication

No. of patients

Reported drugs in previous 2 weeks

Clinical aspect

Site

Histopathological findings

Gianotti et al. 4/30/2020

None

Maculopapular eruption (2) (clinically suggestive for Grover disease)

Trunk

• • •

Levofloxacin and hydroxychloroquine to treat cutaneous lesions that appeared during hospitalization

Exanthema evolving to purpuric maculopapulovesicular rash (1)

Trunk and limbs

First punch: • In the upper dermis diffuse telangiectatic small blood vessels with no other peculiar features

No information

Papular erythematous exanthema (1)

Trunk

• •

Edematous dermis with many eosinophils Cuffs of lymphocytes around blood vessels in a lymphocytic vasculitis histopathological pattern

No information

Severe macular hemorrhagic eruption (1)

Lower members

•

Intravascular microthrombi in the small dermal vessels

Lopinavir 200 mg, ritonavir 50 mg, hydroxychloroquine 200 mg

Ulcer/rash

Breasts and other parts of the skin, including back and genital area

• •

Nonspecific morphological findings with some criteria suggestive of viral exanthema or urticariform dermatites Discrete blood extravasation

Blisters

Internal lip mucosa

•

No information

Desquamative gingivitis (both oral lesions regarding the confirmed case)

Gingiva

•

Intraepidermal vesicle containing scattered multinucleated and ballooned keratinocytes Mild acanthosis Epidermal detachment and confluent eratinocytic necrosis The vesicle contains fibrinoid material with acute inflammation

* Martín Carreras-Presas et al. 5/5/2020

Fernandez-Nieto et al. 5/08/2020

Herrero-Moyano et al. 5/09/2020

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1 (2 suspected cases)

Second punch: • Langerhans cells within the epidermis Third punch: • Perivascular spongiotic dermatitis with exocytosis • Large nest of Langerhans cells • Dense perivascular lymphocytic infiltration eosinophilic rich around the swollen blood vessels with extravasated erythrocytes

Vesicles, papules 7 patients: and pustule Lopinavir/ ritonavir (5), hydroxychloroquine (6) azithromycin (2)

4 patients: Fosfomycin (1), metamizole, linezolid, piperallicintazobactam, amiodarone (1), furosemide (1), piperacillintazobactam, meropenem (1)

Dyskeratotic cells Ballooning multinucleated cells Sparse necrotic keratinocytes with lymphocytic satellitosis (Grover’s disease?)

Erythematous patches and caused coalescent maculopapules

Trunk (anterior and posterior), arms, legs, palms, soles

• • •

Generalized, trunk, flexures, extremities, face

Histologically, patients presented in a variable degree: • • • • • •

Spongiosis dermatitis Non-follicular subcorneal pustules Neutrophilic exocytosis Interstitial neutrophilic infiltrate and scarce eosinophils Three patients showed signs of vascular injury with microthrombi inside the dermal capillaries and hematic leak No fibrinoid necrosis was found in the vessel walls

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Author(s) No. of Date of publication patients

Reported drugs in previous 2 weeks

Clinical aspect

Site

Histopathological findings

* Jimenez-Cauhe et al. 5/09/2020

Lopinavir/ritonavir, hydroxychloroquine, azithromycin, corticosteroids, ceftriaxone

Erythema multiforme-like (4)

Upper trunk

• • •

•

Normal basketweave stratum corneum Mild to moderate spongiosis in epidermis The dermis showed dilated vessels filled with neutrophils Extravasation of red blood cells and lymphocytic perivascular and interstitial infiltrate Basal vacuolar changes with interface dermatitis was observed in one patient Lymphocytic exocytosis in another

• •

Macules and petechiae (3)

Palate

•

No information

Trunk (anterior and posterior)

• • • •

Slight vacuolar-type interface dermatitis Occasional necrotic keratinocytes No eosinophils were encountered Erythema multiforme-like pattern

• • •

Orthokeratotic hyperkeratosis Spongiosis Focal vacuolar degeneration of basal keratinocytes Focal lymphocytic exocytosis Slight inflammatory lymphomorphonuclear infiltrate of superficial dermis with minimal perivascular neutrophilic component Occasional aspects of vessel wall damage

Rodríguez-Jiménez et al. 5/09/2020

None

Urticarial eruption

Skroza et al. 5/18/2020

Ceftriaxon, lopinavir/ritonavir, hydroxychloroquine, enoxaparin

Erythematous wheals Head, trunk and upper arms

Vancomycin, piperacillin and tazobactam levofloxacin and oseltamivir

Erythematous and papular skin rash (developed into vesicles and bullae with desquamation)

• • •

Lagziel et al. 5/19/2020

Disseminated

• • •

•

Torres-Navarro et al. 1 5/26/2020

Dominguez-Santas et al. 5/26/2020

Interferon beta, hydroxychloroquine, azithromycin, ceftriaxone, lopinavir-ritonavir, methylprednisolone, tocilizumab and cefditoren

Confluent reddish macular

None

Macules and papules

Trunk, neck, face, arms and axillary and neck folds

• • •

Legs, ankle and thigh

• • •

Detached epidermis with a basketweave stratum corneum that is separated at the dermalepidermal junction Spongiosis and subtle basilar vacuolar changes with rare dyskeratotic cells The dermis demonstrated superficial edema and a mildly dense, superficial, perivascular and interstitial infiltrate composed of lymphocytes and histiocytes with occasional eosinophils and melanophages The final dermatological clinical picture with no oral mucosal involvement was most consistent with resolving bullous interface dermatitis, not SJS/TEN Subcorneal pustules with abundant inflammatory infiltrate Papillary edema and few eosinophils within superficial dermis The diagnosis of acute generalized exanthematous pustulosis (AGEP) was confirmed Small vessel damage with fibrinoid necrosis of vessel walls Transmural infiltration by neutrophils with karyorrhexis, leukocytoclasia and extravasated erythrocytes DIF showed granular deposition of C3 within vessel walls C O N T I N U E S O N N E X T PAG E

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C O N T I N U E D F R O M P R E V I O U S PAG E

Author(s) Date of publication

No. of patients

Reported drugs in previous 2 weeks

Clinical aspect

Site

Histopathological findings

* Soares et al. 6/4/2020

No information

Reddish lesions and ulceration

Hard palate, tongue and lips

• • • •

•

* Ansari et al. 6/08/2020

Remdesivir and azithromycin

Irregular margins ulcers, varying sizes in red and nonhemorrhagic background

Hard palate

•

Azithromycin

Tongue (anterior) Small and irregular margins ulcers in red and nonhemorrhagic background

•

Epithelium with severe vacuolization and occasional exocytosis In the lamina propria, a diffuse chronic inflammatory infiltrate was associated with focal areas of necrosis and hemorrhage Conspicuous superficial and deep small vessels were obliterated by evident thrombi Small thrombi seemed to be composed mainly by endothelial cells, while the larger ones were composed by fibrin and endothelial cells, and in either cases CD34 was positive for cells in the luminal component Adjacent minor salivary glands exhibited an intense lymphocytic infiltration, mostly positive for CD3 and CD8 Tissue diffuse edema with mucosal desquamation along with granulation and ulceration under the mucosa with invasion of mononuclear cells with large and glassy nuclei Neutrophilic cell invasion was also seen following secondary bacterial infection Histopathology report was almost identical to the first patient

* Amorim dos Santos et al. 6/08/2020

Enoxaparin sodium hydroxychloroquine sulfate, ceftriaxone sodium and azithromycin meropenem, sulfamethoxazole and trimetropin

White plaque and yellowish ulcers (similar herpetic recurrent oral lesions)

Tongue dorsum

• No information

* Díaz Rodríguez et al. 08/17/2020

Topical solutions only for management of oral manifestations possibly related to a certain states of immunosuppression

Oral mucosa, Aphthous-like tongue, palate, lesions (1), tongue commissure depapillation (1), pseudomembranous candidiasis (1), angular cheilitis (1), fissures (in comissure), in addition, some symptoms were observed, such as burning sensation (2) and dry mouth (1)

• No information

* Brandão et al. 08/18/2020

Azithromycin (3), ceftriaxone (3), piperacillin/ tazobactam (2), dipyrone (1), ipratropium bromide and fenoterol hydrochloride (1), acyclovir (due to HSV-1 infection in 3 patients)

Aphthous-like ulcerations (7), hemorrhagic ulcerations (1), necrosis/shallow necrosis (4), petechia (1)

No information

*Studies with oral mucosal involvement. Parentheses represent number of patients with symptoms and number receiving drugs. 524 OC TOBER

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symptoms but had not been tested for Sars-CoV-2. One of these patients had lesions similar to herpetic stomatitis and the other had multiple small ulcers on the palate. However, the third patient, who was positive for Sars-CoV-2, developed blisters on the internal lip mucosa and squamous gingivitis.13 A series of cases reported by Brandão et al. presented eight patients infected with COVID-19, who presented oral ulcerations after symptoms of dysgeusia in most of them. Oral manifestations in these patients included painful oral necrotic ulcers and aphthous-like ulcerations that affected the tongue, lips, palate, and oropharynx. The study also shows the relationship between SARSCoV-2 and ACE2, the main receptor of the SARS-CoV-2 host cell, expressed in epithelial cells of the tongue and of the salivary glands, showing that this virus, may be implicated in the development of dysgeusia in patients with COVID-19. The author also hypothesized that after infection of the oral keratinocytes/ glandular tissues, there is an increase in the permeability of the cell walls to foreign pathogens and viral replication in the cells lining the oral mucosa, leading to ulcers and necrosis. However, future studies are necessary to discover if these oral ulcerations are directly caused by the virus of if they are a coincidental event in COVID-19 progression.17 Jimenez-Cauhe et al. (2020) reported on patients with erythema multiforme-like lesions in which the oral cavity of three of them showed macules on the palate and petechiae, whereas one developed skin lesions at the same time. Studies of hematological impairment in COVID-19 patients revealed possible thrombocytopenia. Such information should be explored, as it could be correlated with the appearance of petechial lesions.12

In our literature review, we present reports on skin and mucocutaneous manifestations in patients diagnosed with COVID-19 and histopathological characteristics of some of these lesions (TABLE). Nevertheless, it is possible that in some of these reports COVID-19 has not been properly diagnosed.

Potential Treatments and Their Implication to Oral Lesions

A treatment protocol for COVID-19 is not yet established. In an attempt to alleviate the symptoms, drugs used for

Tocilizumab was originally used for treatment of rheumatoid arthritis and was recently considered for treatment of COVID-19.

other diseases have been investigated. Wu et al. (2020) carried out a literature review to list the plausible drugs used to treat COVID-19 by separating them into groups of antiviral agents and supporting agents, among others. The efficacy of these treatment regimens remains to be verified by appropriately designed clinical trials.7,8 Among current potential drugs, chloroquine, hydroxychloroquine and tocilizumab can cause adverse effects on oral tissues in other pathological contexts. For this reason, we will discuss these drugs in more detail.

Chloroquine and Hydroxychloroquine

Chloroquine (CQ) and hydroxychloroquine (HCQ) have been tested in the treatment of COVID-19, in which both are considered broad-

spectrum antiviral drugs.50 These drugs are generally safe and routinely used to treat immunological, dermatological and rheumatological disorders51–56 including malaria.47 The potential adverse events of CQ and HCQ include retinopathy, cardiotoxicity and myelotoxicity, which are rare, and a cumulative dose-dependent effect in patients with rheumatoid arthritis and connective tissue disorders.51–56 The chronic use of CQ has been associated with hyperpigmentation of the oral mucosa in the palate region,57 but this effect is observed in patients who use this drug for more than six months.51–54,58 Mucosal hyperpigmentation may also be a sign of underlying systemic disease or a side effect of drug therapy.51,53,54 Although not supported by the literature, CQ and HCQ have been used in the treatment of SARS-CoV-2 for a short period of time, according to expert consensus.50,59 Therefore, based on the present literature review, the authors consider that there is a low risk of oral pigmentation at the doses and time of use studied. However, considering SARS-CoV-2 and the diversity of protocols and doses used, precaution is recommended with observation for possible oral implications resulting from their use in the current treatments.

Tocilizumab

Tocilizumab is an important interleukin-6 (IL-6) receptor inhibitor that may be associated with osteonecrosis of the jaws; thus, caution should be taken when using this drug in patients with COVID-19.60 Tocilizumab was originally used for treatment of rheumatoid arthritis and was recently considered for treatment OC TOBER 2 0 2 0 525

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of COVID-19. Studies have associated the chronic use of tocilizumab with osteonecrosis of the maxilla, associated or not with bisphosphonates.60,61It is unlikely that tocilizumab would cause changes in the oral tissues of patients with COVID-19, as this drug is normally used for a short period of time, but caution should be taken because this disease is new and its actual behavior in response to the current treatments is not well known.

Other Medications and Their Possible Oral Implications

Other drugs are being empirically used for the treatment of COVID-19, especially remdesivir, nitazoxanide, ivermectin, anticoagulants (enoxaparin) and corticoids (dexamethasone).7,62–66 However, in our literature review, no other possible direct adverse effects from these medications in the oral cavity were found. On the other hand, erythema multiforme-like lesions were reported in four patients with COVID-19; three of the patients showed palatal macules and petechiae during intraoral examination. The medications used for these patients were lopinavir/ritonavir, HCQ, azithromycin, corticosteroids and ceftriaxone. The authors emphasize the need for more investigation into the role of the virus, including drug intake or any other conditions associated with these lesions.12

Speculations Based on Reported Oral Manifestations Triggered by Medications

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to cite xerostomia, hairy tongue,68,69 lichenoid reactions and others. Xerostomia has been reported to be an effect of myriad medications, such as antiviral agents, corticosteroids and antibiotics.69,70 The disruption of the normal homeostasis of the oral cavity may cause a range of oral diseases, including dental caries, oral candidiasis, taste disturbance and difficulties with chewing, swallowing and speaking.70 The use of corticotherapy can predispose to candidiasis.71

One cannot forget that this virus can be potentially transmitted and spread through droplets or aerosols containing viral RNA.

Another condition is oral hairy tongue, which has been implicated with the use of many antibiotics such as penicillin, erythromycin and linezolid. Medications predisposing individuals to xerostomia are associated with hairy tongue, and there are also reports that prednisolone can be implicated with causing this manifestation.68 The mechanism of drug-induced oral hairy tongue is not known. Moreover, xerostomia may be capable of causing this pathology when combined with other predisposing factors, such as smoking and poor oral hygiene.72 These above-mentioned situations could serve as a basis for a biological reasoning for some empirical drug treatments that may arise in future

studies. In the dental context, this should also draw attention to the possible oral implications of medications in terms of side effects.

Saliva: Clues to Diagnosis and Disease Prediction

Salivary biomarkers have recently been used to diagnose various diseases, such as oral cancer, periodontal diseases, dental caries, lung cancer, breast cancer and diabetes.73 Consistent studies have shown the presence of SARS-CoV-2 in human saliva, indicating that this fluid is a viable tool for diagnosing patients who feel discomfort with nasal and oropharyngeal swabs, in addition to decreasing the risk of contamination of health care workers during sample collection.74–81 Samples of saliva can be stored at –80 C for several years with little degradation. This means that saliva can be used in future analyses and serve as a prognostic marker for COVID-19 during different stages of the infection, thus being possible to follow the progression of the disease.82 In our literature review, we found several studies reporting relevant results regarding the detection of SARS-CoV-2 in human saliva, with a concordance rate ranging from 81.8% to 100% compared to other detection techniques such as nasal and oropharyngeal swabs.74–76,79,80 A study conducted in Hong Kong examined saliva samples collected from COVID-19 suspect patients after two days of hospitalization on average (variation from zero to seven days). The authors reported concordance rates of 91.7% for positive results compared to nasopharyngeal swab and of 100% for 33 negative results. Culture method showed the presence of live virus in three saliva samples, indicating the

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transmission potential of COVID-19 through saliva.75 Another study carried out in Italy showed a concordance rate of 100% between saliva samples and nasopharyngeal swab for positive results of SARS-CoV-2, which was detected by RT-PCR. Also, two patients testing positive in the same days were considered negative after detection with nasopharyngeal swab or brochoalveolar lavage.77 In these cases, although nasopharyngeal swab had detected no virus, individuals might be infected, as the virus was present in the salivary glands. In fact, these glands are potential targets of SARS-CoV-2 because glandular cells express the receptor of angiotensinconverting enzyme 2 (ECA2).79,83–85 Some articles provide information on viral load monitoring in saliva for detection of SARS-CoV-2 in humans.74–80 Azzi et al. (2020)77 also highlighted the value of saliva in the clinical evolution of COVID-19, as there was an inverse association between lactate dehydrogenase (LDH) and cycle threshold (Ct) values. The results found in a cohort study performed by To et al. (2020)74 showed that despite the development of antibodies against surface proteins of SARS-CoV-2, viral RNA could still be detected in oropharyngeal saliva samples over several days. Moreover, the salivary viral load was found to be higher during the first week of symptoms, decreasing in onethird of the patients over time (20 days or more). In a specific patient, viral RNA was detected 25 days after the onset of symptoms, suggesting that these findings are important for guiding antiviral treatments. Therefore, it is necessary to perform more studies for standardization of saliva tests to detect COVID-19 and follow its evolution. The main advantages of using saliva for diagnosis of COVID-19 and other diseases are that

its collection is fast, easy and low cost, thus posing less risk of contamination for health care professionals, and it is well accepted by patients. In addition, serial saliva samples can be used to follow the evolution of the infection because saliva deteriorates less over time.74,84–86 The U.S. Food and Drug Administration (FDA) has recently approved a test using saliva for diagnosis of COVID-19. A sample of saliva is collected by the patient spitting into a tube under the supervision of a qualified practitioner;

It is expected that there will be an increase in mortality rates due to oral carcinoma because of dental care restrictions.

the material is analyzed based on the TaqPath SARS-CoV-2 assay, which is used in COVID-19 tests available to identify viral RNA.87 Despite the importance of diagnosing COVID-19 using saliva, one cannot forget that this virus can be potentially transmitted and spread through droplets or aerosols containing viral RNA when infected individuals cough, sneeze or speak, which are the main transmission routes of the pathogen.75,82,85,88,89 Amount, size and distance of the particles can be relevant factors influencing the risk of transmission of the pathogen, meaning that individuals who are close to transmission sources are at higher risk, particularly health care professionals performing oral and facial surgeries,

such as dentists, otolaryngologists and ophthalmologists, among others. In addition, small droplets (≤ 60 μm) can evaporate and become aerosols, reaching another host through the airflow and inhaled or settle onto the mucosas.85 Nevertheless, it should be emphasized that one cannot establish a remote spread because there is no evidence supporting that SARS-CoV-2 can survive long in an outdoor environment.82,85

Aspects of Clinical Dental Practice Versus COVID-19

Because recent studies have shown the presence of SARS-CoV-2 in human saliva, dental professionals deserve special attention in relation to the risk of infection because they are directly exposed to the fluid. Therefore, dental professionals of all specialties may be vulnerable to this risk because they are in closer contact with patients while they examine their oral cavities. The possibility of contact with asymptomatic patients is high, and consequently, strict biosafety measures must be taken.90 Dental professionals are constantly exposed to aerosols that in turn may possibly be contaminated by the virus. Aerosols are both liquid and solid particles measuring less than 50 μm, and they can be suspended in the air for protracted periods of time,91whereas splatter is a mixture of air, water and/ or solid substances measuring from 50 μm to several millimeters in diameter.92 In routine dental practice, dental drills cause the formation of aerosol and splatter commonly contaminated with bacteria, viruses, fungi and blood.92,93 In this context, some diseases are known to be spread by droplets or aerosols as occurs with pneumonic plague, tuberculosis, influenza, Legionnaires’ disease and SARS-CoV-2.91 OC TOBER 2 0 2 0 527

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Aerosol plays an important role in the spread of SARS-CoV-2 and can be considered a potential source of airborne contamination as previously reported in the other droplet-spread disease SARS.91 Experiments demonstrated that SARS-CoV-2 remained viable in aerosols for three hours as well as on plastic for up to 72 hours and stainless steel for up to 48 hours.94 The mechanism of inactivation of the new coronavirus by chemical agents is not yet well established. Human coronaviruses are known to remain viable on inanimate surfaces for up to nine days, but 0.1% sodium hypochlorite and 62% to 70% alcohol are effective in inactivating them after exposure for one minute. Therefore, the same is expected to happen to SARS-CoV-2.95 Reports have indicated that SARSCoV-2 has a higher transmissibility than SARS-CoV and MERS-CoV, meaning that a higher level of precaution and infection control regimen aimed at SARSCoV-2 is essential during this outbreak.96 In general, there is a tendency to associate dentists who perform restorative procedures with greater exposure to aerosols than those involved in other dental practices. On the other hand, the impact of the transmission of the disease on other dental practices, such as intraoral examination and biopsies typically performed by stomatologists and/or oral maxillofacial surgeons, is yet to be established. Nevertheless, simple contact with saliva is a potential risk for all dental professionals.

Oral and Maxillofacial Pathology Practice and Laboratory Routine

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a 1:10 ratio showed some effectiveness in inactivating SARS at appropriate temperatures, but virus samples can remain infectious even after three days of exposure to formalin.97 Histopathological analysis of tissues from patients with COVID-19 has been performed with samples fixed in 10% buffered formalin.98 It is suggested that formaldehyde fixation and paraffin inclusion can inactivate SARS-CoV-2.9 Since the WHO declared COVID-19 a pandemic, dental care has been considerably reduced worldwide. An oral

Telemedicine has been widely used during the pandemic and is shown to be highly effective in the diagnosis and follow-up of oral lesions.

health care center in Turin, Italy, recorded approximately 40 cases of squamous cell carcinoma in 2019. Dental emergency care is generally restricted to toothache. Thus, it is expected that there will be an increase in mortality rates due to oral carcinoma because of dental care restrictions, especially in the elderly population.99 Consequently, there will be a decrease in the number of biopsy specimens sent to histopathology laboratories, reducing the flow of laboratory activities. Some precautions must be taken by pathologists during the pandemic. The use of gloves, surgical masks, disposable gowns and caps is essential during macroscopic analysis and tissue processing. Histological slides should be handled with gloves, and contact with the face,

nose or mouth should be avoided. During microscopic analysis, it is recommended to wear masks and glasses and to avoid sharing the microscope. After use, the microscope must be disinfected and covered with a plastic cover. Stationery materials should be handled with gloves and hands should be cleaned with soap and water after using the materials.2 Telemedicine has been widely used during the pandemic and is shown to be highly effective in the diagnosis and follow-up of oral lesions.100 A letter to the editor published by Georgakopoulou cites cases where patients were being seen for the first and second times, including follow-up, for evaluation of oral lesions on the basis of photos. The diagnosis included erythema multiforme, herpetiform ulcers, temporomandibular joint pain, soft tissue reactive lesion, gingival cysts, erythematous candidiasis, oral hairy tongue, geographic tongue, oncological dental care, herpes zoster, secondary herpes, oral lichen planus, burning mouth syndrome and atopic cheilitis.101 It can be said that telemedicine is an essential tool for oral medicine in times of pandemic, thus contributing to social distancing and ensuring patient care.

Final Remarks

The COVID-19 pandemic has shown an uncertain evolution in infected patients due to the influence of several factors. Our literature review compiled recent information on the new coronavirus by providing general data that were gradually tapered to more relevant ones for dental practice and finally stomatology and oral maxillofacial pathology. Under the classic perspective of biosafety, the new coronavirus pandemic has a direct impact on all areas of health care including dentistry in terms of both clinical practice

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(i.e., direct care of patients) and laboratory routine procedures (i.e., oral pathologists performing histopathological analysis of tissue samples). A rapid-spread disease results in several extrapulmonary manifestations, including possible oral repercussions that may be directly related to SARS-CoV-2 or result from the adverse effects of medications used as possible treatments of the disease. Under this perspective, the impairment of oral and maxillofacial structures by the SARS-CoV-2 infection needs to be better investigated by stomatologists and oral pathologists who should be aware of these possibilities during routine diagnostic process. Also, as more literature becomes available, the oral and mucosal effects from the SARS-CoV-2 virus can be separated from the potential drug interactions/reactions. Telemedicine should also be considered during diagnosis and follow-up of oral lesions. It is also necessary to highlight the role played by saliva in three aspects, namely its diagnostic potential for detection of the virus, its predictive value regarding the possibility to follow the viral load in different moments during the course of the disease and its potential of transmission through droplets and bioaerosols. This literature review of the pandemic caused by SARS-CoV-2 and its potential impact on the dental practice makes clear that in order to be prepared to deal with COVID-19, the dental professional including stomatologists and oral pathologists, must stay current with new evidence and think critically about the possible direct and indirect implications that SARS-CoV-2 can have on oral and maxillofacial structures. n REFERENCES 1. Wu D, Wu T, Liu Q, Yang Z. The SARS-CoV-2 outbreak: What we know. Int J Infect Dis 2020; May;94:44–48. doi:10.1016/j.ijid.2020.03.004. Epub 2020 Mar 12. 2. Saxena S. Coronavirus disease-2019: A brief

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46. Galván Casas C, Català A, Carretero Hernández G, et al. Classification of the cutaneous manifestations of COVID-19: A rapid prospective nationwide consensus study in Spain with 375 cases. Br J Dermatol 2020 Jul;183(1):71–77. doi: 10.1111/bjd.19163. Epub 2020 Jun 10. 47. Marzano AV, Cassano N, Genovese G, Moltrasio C, Vena GA. Cutaneous manifestations in patients with COVID‐19: A preliminary review of an emerging issue.]. Br J Dermatol July 2020:bjd.19264. doi:10.1111/ bjd.19264. Published online ahead of print June 1, 2020. 48. Sachdeva M, Gianotti R, Shah M, et al. Cutaneous manifestations of COVID-19: Report of three cases and a review of literature. J Dermatol Sci 2020 May;98(2):75– 81. doi:10.1016/j.jdermsci.2020.04.011. Epub 2020 Apr 29. 49. Lagziel T, Quiroga L, Ramos M, Hultman CS, Asif M. Two False Negative Test Results in a Symptomatic Patient with a Confirmed Case of Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2) and Suspected Stevens-Johnson Syndrome/Toxic Epidermal Necrolysis (SJS/TEN). Cureus 2020 May; 12(5):e8198. doi:10.7759/cureus.8198. 50. Zhang J, Xie B, Hashimoto K. Current status of potential therapeutic candidates for the COVID-19 crisis. Brain Behav Immun 2020 Jul;87:59–73. doi:10.1016/j. bbi.2020.04.046. 51. de Melo Filho MR, da Silva CAD, da Rocha Dourado M, de Oliveira Pires MB, Pêgo SPB, de Freitas EM. Palate hyperpigmentation caused by prolonged use of the antimalarial chloroquine. Head Neck Pathol 2012 Mar;6(1):48–50. doi:10.1007/s12105-011-0288-5. 52. de Andrade BAB, Padron-Alvarado NA, MuñozCampos EM, Morais TM de L, Martinez-Pedraza R. Hyperpigmentation of hard palate induced by chloroquine therapy. J Clin Exp Dent 2017 Dec;9(12):e1487–e1491. doi:10.4317/jced.54387. 53. Gallo CB, Luiz AC, Ferrazzo KL, Migliari DA, Sugaya NN. Drug-induced pigmentation of hard palate and skin due to chronic chloroquine therapy: Report of two cases. Clin Exp Dermatol 2009 Oct;34(7):e266–e267. doi:10.1111/j.1365-2230.2008.03185.x. Epub 2009 May 5. 54. de Andrade BAB, Fonseca FP, Pires FR, et al. Hard palate hyperpigmentation secondary to chronic chloroquine therapy: Report of five cases. J Cutan Pathol 2013 Sep;40(9):833–838. doi:10.1111/cup.12182. Epub 2013 Jun 19. 55. Horta-Baas G. Chloroquine-induced oral mucosal hyperpigmentation and nail dyschromia. Reumatol Clin May–Jun 2018;14(3):177–178. doi:10.1016/j. reumae.2017.06.001. 56. Tosios KI, Kalogirou EM, Sklavounou A. Drugassociated hyperpigmentation of the oral mucosa: Report of four cases. Oral Surg Oral Med Oral Pathol Oral Radiol 2018 Mar;125(3):e54–e66. doi:10.1016/j. oooo.2017.10.006. 57. Godinho GV, Paz ALLM, Araújo Gomes EPA, Garcia CL, Volpato LER. Extensive hard palate hyperpigmentation associated with chloroquine use. Br J Clin Pharmacol. April 2020:bcp.14313. doi:10.1111/bcp.14313. 58. Bahloul E, Jallouli M, Garbaa S, et al. Hydroxychloroquine-induced hyperpigmentation

in systemic diseases: Prevalence, clinical features and risk factors: A cross-sectional study of 41 cases. Lupus 2017 Oct;26(12):1304–1308. doi: 10.1177/0961203317700486. Epub 2017 Mar 29. 59. Perricone C, Triggianese P, Bartoloni E, et al. The antiviral facet of anti-rheumatic drugs: Lessons from COVID-19. J Autoimmun 2020 Jul;111:102468. doi:10.1016/j. jaut.2020.102468. 60. Bindakhil MA, Mupparapu M. Osteomyelitis of the mandible exhibiting features of medication-related osteonecrosis in a patient with history of tocilizumab treatment. J Orofac Sci 2018;10(1):53–55. doi: 10.4103/jofs.jofs_46_18. 61. Bennardo F, Buffone C, Giudice A. New therapeutic opportunities for COVID-19 patients with tocilizumab: Possible correlation of interleukin-6 receptor inhibitors with osteonecrosis of the jaws. Oral Oncol 2020 Jul;106:104659. doi:10.1016/j. oraloncology.2020.104659. Epub 2020 Mar 21. 62. Tang N, Bai H, Chen X, Gong J, Li D, Sun Z. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost 2020 May;18(5):1094–1099. doi:10.1111/jth.14817. Epub 2020 Apr 27. 63. University of Oxford. Low-cost dexamethasone reduces death by up to one third in hospitalised patients with severe respiratory complications of COVID-19. www.recoverytrial. net/news/low-cost-dexamethasone-reduces-death-by-upto-one-third-in-hospitalised-patients-with-severe-respiratorycomplications-of-covid-19. 64. Caly L, Druce JD, Catton MG, Jans DA, Wagstaff KM. The FDA-approved drug ivermectin inhibits the replication of SARS-CoV-2 in vitro. Antiviral Res 2020 Jun;178:104787. doi:10.1016/j.antiviral.2020.104787. Epub 2020 Apr 3. 65. Grein J, Ohmagari N, Shin D, et al. Compassionate use of remdesivir for patients with severe COVID-19. N Engl J Med 2020 Jun;382(24):2327–2336. doi:10.1056/ NEJMoa2007016. 66. Wang Y, Zhang D, Du G, et al. Remdesivir in adults with severe COVID-19: A randomised, double-blind, placebo-controlled, multicentre trial. Lancet 2020 May 16;395(10236):1569–1578. doi:10.1016/S01406736(20)31022-9. 67. Wolff A, Joshi RK, Ekström J, et al. A guide to medications inducing salivary gland dysfunction, xerostomia and subjective sialorrhea: A systematic review sponsored by the World Workshop on Oral Medicine VI. Drugs R D 2017 Mar;17(1):1–28. doi:10.1007/s40268016-0153-9. 68. Uğur S, Cahit K. Prednisolone-induced hairy tongue: A case report. Arch Rheumatol 2019 Feb 1;34(3):348–351. doi:10.5606/ArchRheumatol.2019.7239. eCollection 2019 Sep. 69. Assery MA. Efficacy of artificial salivary substitutes in treatment of xerostomia: A systematic review. J Pharm Bioallied Sci 2019 Feb;11(Suppl 1):S1–S12. doi:10.4103/JPBS.JPBS_220_18. 70. Villa A, Wolff A, Aframian D, et al. World Workshop on Oral Medicine VI: A systematic review of medicationinduced salivary gland dysfunction: Prevalence, diagnosis and treatment. Clin Oral Investig 2015 Sep;19(7):1563–

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1580. doi:10.1007/s00784-015-1488-2. Epub 2015 May 22. 71. Ellepola AN, Samaranayake LP. Inhalational and topical steroids and oral candidosis: A mini review. Oral Dis 2001 Jul;7(4):211–6. doi:10.1034/j.16010825.2001.70402.x. 72. Thompson DF, Kessler TL. Drug-induced black hairy tongue. Pharmacotherapy 2010 Jun;30(6):585–593. doi:10.1592/phco.30.6.585. 73. Khurshid Z, Asiri FYI, Al Wadaani H. Human saliva: Noninvasive fluid for detecting novel coronavirus (2019-nCoV). Int J Environ Res Public Health 2020 Mar 26;17(7):2225. doi:10.3390/ijerph17072225. 74. To KK-W, Tsang OT-Y, Leung W-S, et al. Temporal profiles of viral load in posterior oropharyngeal saliva samples and serum antibody responses during infection by SARS-CoV-2: An observational cohort study. Lancet Infect Dis 2020 May;20(5):565–574. doi:10.1016/S14733099(20)30196-1. 75. To KK-W, Tsang OT-Y, Yip CC-Y, et al. Consistent detection of 2019 novel coronavirus in saliva. Clin Infect Dis 2020 Jul 28;71(15):841–843. doi:10.1093/cid/ ciaa149. 76. Williams E, Bond K, Zhang B, Putland M, Williamson DA. Saliva as a non-invasive specimen for detection of SARS-CoV-2. J Clin Microbiol 2020 Jul 23;58(8)e00776– 20. doi:10.1128/JCM.00776-20. Print 2020 Jul 23. 77. Azzi L, Carcano G, Gianfagna F, et al. Saliva is a reliable tool to detect SARS-CoV-2. J Infect 2020 Jul;81(1):e45–e50. doi:10.1016/j.jinf.2020.04.005. Epub 2020 Apr 14. 78. Pasomsub E, Watcharananan SP, Boonyawat K, et al. Saliva sample as a noninvasive specimen for the diagnosis of coronavirus disease 2019: A cross-sectional study. Clin Microbiol Infect 2020 May 15;S1198-743X(20)30278-0. doi: 10.1016/j.cmi.2020.05.001. Online ahead of print. 79. Chen JH-K, Yip CC-Y, Poon RW-S, et al. Evaluating the use of posterior oropharyngeal saliva in a point-of-care assay for the detection of SARS-CoV-2. Emerg Microbes Infect 2020 Dec;9(1):1356–1359. doi:10.1080/222217 51.2020.1775133. 80. Kam K, Yung CF, Maiwald M, et al. Clinical utility of buccal swabs for severe acute respiratory syndrome coronavirus 2 detection in coronavirus disease 2019 — infected children. J Pediatric Infect Dis Soc 2020 Jul 13;9(3):370–372. doi:10.1093/jpids/piaa068. 81. Henrique Braz‐Silva P, Pallos D, Giannecchini S, To KK. SARS‐CoV‐2: What can saliva tell us? Oral Dis 2020;(April):odi.13365. doi:10.1111/odi.13365. 82. Han P, Ivanovski S. Saliva — Friend and foe in the COVID-19 outbreak. Diagnostics (Basel) 2020 May 9;10(5):290. doi:10.3390/diagnostics10050290. 83. Alizargar J, Etemadi Sh M, Aghamohammadi M, Hatefi S. Saliva samples as an alternative for novel coronavirus (COVID-19) diagnosis. J Formos Med Assoc 2020 Jul;119(7):1234–1235. doi:10.1016/j.jfma.2020.04.030. 84. Ceron JJ, Lamy E, Martinez-Subiela S, et al. Use of saliva for diagnosis and monitoring the SARS-CoV-2: A general perspective. J Clin Med 2020 May 15;9(5):1491. doi:10.3390/jcm9051491. 85. Xu R, Cui B, Duan X, Zhang P, Zhou X, Yuan Q. Saliva: Potential diagnostic value and transmission of 2019-nCoV. Int J Oral Sci 2020;12(1):9. doi:10.1038/s41368-020-0080-z.

86. Sri Santosh T, Parmar R, Anand H, Srikanth K, Saritha M. A review of salivary diagnostics and its potential implication in detection of COVID-19. Cureus 2020 Apr 17;12(4):e7708. doi:10.7759/cureus.7708. 87. Winter L. First saliva test for COVID-19 approved for emergency use by FDA. www.the-scientist.com/ news-opinion/first-saliva-test-for-covid-19-approved-foremergency-use-by-fda-67416. Apr 14, 2020. Accessed May 25, 2020. 88. Sharma S, Kumar V, Chawla A, Logani A. Rapid detection of SARS‐CoV‐2 in saliva: Can an endodontist take the lead in point‐of‐care COVID‐19 testing? Int Endod J 2020 Jul;53(7):1017–1019. doi:10.1111/iej.13317. Epub 2020 May 17. 89. Song J, Li Y, Huang X, et al. Systematic analysis of ACE2 and TMPRSS2 expression in salivary glands reveals underlying transmission mechanism caused by SARS‐CoV‐2. J Med Virol 2020 May 22;10.1002/jmv.26045. doi: 10.1002/jmv.26045. Online ahead of print. 90. Sabino-Silva R, Carolina A, Jardim G, Siqueira WL. Coronavirus COVID-19 impacts to dentistry and potential salivary diagnosis. Clin Oral Investig 2020 Apr;24(4):1619–1621. doi: 10.1007/s00784-02003248-x. Epub 2020 Feb 20. 91. Harrel SK, Molinari J. Aerosols and splatter in dentistry. J Am Dent Assoc 2004 Apr;135(4):429–437. doi:10.14219/jada.archive.2004.0207. 92. Coulthard P. Dentistry and coronavirus (COVID-19) — moral decision-making. Br Dent J 2020 Apr;228(7):503– 505. doi:10.1038/s41415-020-1482-1. 93. Ge Z, Yang L, Xia J, Fu X, Zhang Y. Possible aerosol transmission of COVID-19 and special precautions in dentistry. J Zhejiang Univ B 2020 May;21(5):361–368. doi:10.1631/jzus.B2010010. 94. van Doremalen N, Bushmaker T, Morris DH, et al. Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med 2020 Apr 16;382(16):1564–1567. doi:10.1056/NEJMc2004973. 95. Kampf G, Todt D, Pfaender S, Steinmann E. Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. J Hosp Infect 2020 Mar;104(3):246–251. doi:10.1016/j.jhin.2020.01.022. 96. Chen J. Pathogenicity and transmissibility of 2019-nCoV—A quick overview and comparison with other emerging viruses. Microbes Infect 2020 Mar;22(2):69– 71. doi:10.1016/j.micinf.2020.01.004. 97. Darnell MER, Subbarao K, Feinstone SM, Taylor DR. Inactivation of the coronavirus that induces severe acute respiratory syndrome, SARS-CoV. J Virol Methods 2004 Oct;121(1):85–91. doi:10.1016/j.jviromet.2004.06.006. 98. Bradley BT, Maioli H, Johnston R, et al. Histopathology and ultrastructural findings of fatal COVID-19 infections. medRxiv 2020:2020.04.17.20058545. doi.org/10.1101 /2020.04.17.20058545. 99. Arduino PG, Conrotto D, Broccoletti R. The outbreak of novel coronavirus disease (COVID‐19) caused a worrying delay in the diagnosis of oral cancer in northwest Italy: The Turin Metropolitan Area experience. Oral Dis 2020 Apr 19;10.1111/odi.13362. doi: 10.1111/odi.13362. Online ahead of print. 100. Villa A, Sankar V, Shiboski C. Tele(oral)medicine: BA new approach during the COVID‐19 crisis. Oral Dis 2020 Apr 20;10.1111/odi.13364. doi: 10.1111/

odi.13364. Online ahead of print. 101. Georgakopoulou EA. Digitally aided telemedicine during the SARS‐CoV‐2 pandemic to screen oral medicine emergencies. Oral Dis 2020 May 5;10.1111/odi.13383. doi: 10.1111/odi.13383. Online ahead of print. THE CORRESPONDING AUTHOR, Tatiana Nayara Libório-Kimura, DDS, PhD, can be reached at tliborio@ufam.edu.br.

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respiratory protection C D A J O U R N A L , V O L 4 8 , Nº 1 0

Face Masks and Respirators for the Dental Health Care Provider: A Review Emma Bhaskar, BS

a b s t r a c t As protocols and standards of personal protective equipment are

changing in the time of COVID-19, dental health care providers must brief themselves on the appropriate products to keep them and their staff safe. This article reviews the current respiratory protection devices used to minimize the risk of SARS-CoV-2 infection.

AUTHOR Emma Bhaskar, BS, is a third-year dental student at the University of the Pacific, Arthur A. Dugoni School of Dentistry. She is from Monterey, Calif., and is a third-generation dentist in her family. She plans to attend a GPR or AEGD program and is particularly passionate about dental public and global health projects. Conflict of Interest Disclosure: None reported.

edical masks were first developed and tested in the early 1900s with their use promoted in the 1920s to reduce infections. One of the first studies of the effectiveness of face masks demonstrated a zero incidence of diphtheria in the attendants who wore masks while caring for infected patients. In the 1930s, surgical teams began wearing masks to reduce postoperative infections.1 Dentistry adopted the practice of universal precautions in the 1980s, mostly in response to the bloodborne human immunodeficiency virus (HIV) epidemic. Universal precautions are a set of protective guidelines set with the goal of preventing transmission of bloodborne pathogens from exposure to blood or other fluids containing blood by using gloves, masks, eye protection and gowns as protective clothing. In 1996, the Centers for Disease Control and Prevention (CDC) broadened the concept with standard precautions to include protection from bloodborne pathogens as well as

pathogens in any bodily fluid, secreted or excreted.2 The next level of precautions are specific to the pathogen and are called transmission-based precautions, including airborne precautions for severe acute respiratory syndrome (SARS), measles, varicella (chickenpox) and Mycobacterium tuberculosis.3 SARS-CoV-2 is a respiratory coronavirus that originated in Asia and has spread worldwide. The disease process is called novel coronavirus 2019 (COVID-19) and is caused by the coronavirus SARS-CoV-2. The World Health Organization (WHO) declared the COVID-19 disease a pandemic on March 11, 2020. COVID-19 is thought to spread person to person via respiratory transmission. Respiratory droplets are formed when an infected person talks, coughs or sneezes and the virus becomes suspended in a droplet for a period of time. This airborne transmission is thought to occur during close contact, specifically 6 feet or less.4 This is of particular concern in the dental setting due to the close contact OC TOBER 2 0 2 0 533

respiratory protection C D A J O U R N A L , V O L 4 8 , Nº 1 0

TABLE 1

ASTM Classifications8

to patients and aerosols created during dental procedures. Dental procedures can create droplets when the dental health care provider (DHCP) uses aerosol-generating instruments such as a handpiece or cavitron. The DHCP should institute airborne precautions with respiratory protection devices while continuing to use standard precautions including handwashing, gowns, gloves and eye protection. This article reviews the current respiratory protection devices used to minimize the risk of SARS-CoV-2 infection. There are two types of respiratory protection devices used in dentistry: the surgical mask, otherwise known as a face mask, and the respirator. Face masks are intended to prevent the spread of respiratory infections by the user with minimal protection for the user. Its function is to cover the mouth and nose, preventing the spread of viruses via large droplets created during talking, coughing or sneezing. The face mask protects the user from splashes of fluid and large airborne droplets but does not filter the smaller particles produced from dental procedures or a patient’s coughing and sneezing.5 In addition, these masks fit loosely on the face and allow airborne pathogens and droplets to bypass the mask entirely through the gaps between the skin and mask. However, the presence of a face mask blocks handto-face/mouth/nose transmission of disease for the user. Face masks do not protect healthy people from respiratory infections.6 Respirators, such as the N95, are worn tightly around the health care provider’s mouth and nose to prevent the inhalation of airborne particles such as dust or infectious particles. Respirators are used to prevent infections such as tuberculosis, varicella6 and, most recently, SARS.

Face Masks

A face mask, or surgical mask, is a loose-fitting, disposable, protective device

534 OC TOBER

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ASTM classification

Bacterial filtration efficiency

Particulate filtration efficiency at 0.1 micrograms

Fluid resistance

Differential pressure (breathability)

Level 1

≥ 95%

80 mmHg

< 4.0mm H2O/cm3

Level 2

≥ 98%

120 mmHg

< 5.0 mm H2O/cm3

Level 3

≥ 98%

160 mmHg

< 5.0 mm H2O/cm3

that covers the mouth and nose of the user. The edges of the mask do not form a seal around the mouth and nose. Three types of surgical masks are rated by the American Society of Testing and Materials (ASTM) on the following criteria: bacterial filtration, submicron particulate filtration, differential pressure, resistance to penetration of synthetic blood and flammability.7 The masks are designated as Level 1, Level 2 or Level 3 based on these testing results and are detailed in TABLE 1 . ASTM Level 1 masks provide lowlevel protection and can be used for administrative duties, previsit screening and nonfluid-producing appointments. Level 2 masks are used for lab and instrument processing tasks and low fluid-producing procedures such as simple restorative procedures, sealants and endodontics. If an N95 mask is not available, Level 3 can be used with a face shield for moderate to heavy spray and aerosol-producing procedures such as oral surgery, crown and bridge and the use of ultrasonic cleaners.7 All three levels of masks have a Class 1 flame spread rating.7 Masks that do not meet the ASTM testing criteria are considered “low-performance” face masks and should not be used in the dental office during the COVID-19 pandemic (TABLE 3) .

Respirators

Respirators are tightly fitted protective devices that cover the wearer’s mouth, nose and, in some cases, the entire face. These devices significantly reduce the risk of inhalation of airborne viruses and bacteria and can also filter dust particles, gases and vapors. There are three types of respirators available for

use: the disposable or filtered facepiece respirator (FFR), the reusable elastomeric respirator with filter cartridges and the powered air-purifying respirator (PAPR). Respirators are given an assigned protection factor (APF) by the Occupational Safety and Health Administration (OSHA).8 The number varies with each type of respirator, with the higher number being more protective to the wearer. If a respirator has an APF of 10, one would expect it to reduce exposure of contaminant by a factor of 10. An APF of 1,000 will reduce the exposure of a contaminant by 1,000.9 Factors such as environmental conditions, mask fit and the type of contaminant affect the protective factor of a respirator. The N95 disposable filtering facepiece is the most commonly used respirator in health care. It is one of nine types of particulate disposable filtered respirators outlined in TABLE 2 . These masks protect the wearer from biological threats such as viruses or bacteria but not gases or vapors. Each mask is categorized with a letter and number to signify its effectiveness. The respirators are rated as N, R or P for the mask’s protection against industrial oils (such as solvents or pesticides) that can degrade them. “N” masks are not resistant to oils, “R” masks are resistant to oils and masks labeled “P” are oil-proof. Because bacteria and viruses are not oil-based, there is little benefit to using the R- or P-rated masks in health care environments, but they are useful in the industrial setting. However, any of the nine disposable filtered respirators will protect the DHCP from biological threats and can be used. The numeric rating that follows each letter

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TABLE 2

Categorization of the Nine Types of Particulate Disposable Filtered Respirators9 Family of protection

95% filtering capacity

99% filtering capacity

≥ 99.97% filtering capacity

Not resistant to oil (N)

N-95

N-99

N-100

Resistant to oil (R)

R-95

R-99

R-100

Oil-proof (P)

P-95

P-99

P-100

reflects the number of airborne particles that are filtered. At least 95% of airborne particles are filtered during a “worst-case” testing scenario with the most penetrating particle size. Respirators with 99% filtering capacity are rated 99, and those with 99.97% and higher receive the 100 rating. The National Institute for Occupational Safety and Health (NIOSH) is responsible for testing and rating respirators for use. All approved respirators have NIOSH markings and are listed on the NIOSH online database of approved respirators. Surgical N95 respirators are approved by the FDA as fluid resistant and referred to as N95s. Standard N95 respirators are not fluid resistant and the DHCP should use the N95s respirator if available.10 The APF of N95 respirators is 10.7 Elastomeric respirators are face masks (full or half) that are made of natural or synthetic rubber and can be reused after disinfection of the unit. They have replaceable filters, adjustable straps and sealing edges for a tight fit. Elastomeric respirators offer an alternative to disposable N95 respirators, as they can be repeatedly used after disinfection. Thorough cleaning between patients is required with the manufacturer’s recommended disinfection solution, as improper cleaning can degrade or damage the device. Filters can be changed when clogged, soiled or contaminated. The respirator should be examined by a trained individual after each cleaning before use to ensure proper function and sanitation.11 Filter ratings follow the same as disposable masks (N/P/R and 95/99/100); as with an N95 respirator, fit and seal are very important for the effectiveness of the respirator. Elastomeric respirators are generally not approved by the FDA as fluid resistant

though they can provide equivalent protection of the N95 disposable filtered respirators. During shortages of respirators, the same elastomeric respirator can be used by multiple DHCP if it is properly cleaned, disinfected and inspected. The APF of half-mask elastomeric respirators is 10 and the full mask is 50.7 PAPRs are not commonly used in the dental setting but offer another option for the DHCP. PAPRs are air-purifying respirators that blow air through a highefficiency particulate air filter (HEPA) and then into the breathing zone of the user. A PAPR may have either a tight- or a loose-fitting full facepiece in a hood or helmet design. This airflow provides a higher level of protection for the user than either the N95 disposable respirator or elastomeric respirators.10 PAPRs should be disinfected between uses and can be reused by others. Conventionally, filters are changed when they are soiled, damaged or there is reduced airflow, but in times of crisis or necessity, practices may demand cleaning and disinfecting the filter.12 Some complications that may be involved with PAPR use include limited visual field and reduced ability to hear due to the loud blower noise. Concurrent use of an N95 with a PAPR has been shown to decrease inspired airborne particles even further.13 PAPR systems have APF values of at least 25 for loose-fitting hoods and helmets, 50 for tight-fitting half masks and up to 1,000 for full-facepiece types and some loose-fitting hoods and helmets.7,12 The use of an N95 respirator or a respirator with a higher level of protection (PAPR, facepiece respirator or elastomeric respirator) is recommended for any aerosolgenerating procedure. If an N95 is not available, an ASTM Level 3 mask can

be used with a full-face shield. If neither is available, it is not recommended to perform the aerosol-producing procedure. Due to the shortage of N95 respirators, OSHA and the CDC have published guidelines for alternative non-NIOSHapproved respirators and filters certified in other countries as a replacement for the N95 respirators. These approved alternative respirators are listed on the CDC website and include, but are not limited to, the KN/KP95 from China, P2 from Australia, Special 1st from Korea and N95 from Mexico.17 Many of these alternative respirators utilize the ear loop design, which may make a proper fit more difficult.18 OSHA and the CDC consider the use of homemade masks or modified masks in the care of patients as a last resort. Homemade masks are not considered acceptable personal protective equipment (PPE) because the ability to protect the user is unknown. The use of face shields is recommended with all masks and respirators and is especially necessary with alternative masks and respirators.19

Fit Test

OSHA requires that before an employee is required to use any respirator with a negative or positive pressure tight-fitting facepiece, the employee must be fit tested with the same make, model, style and size of respirator that will be used. The two approved tests that OSHA accepts are the qualitative fit test (QLFT) and the quantitative fit test (QNFT). Traditionally, a fit test must be done annually with all employees who are required to wear tight-fitting respirators, but as of March 2020, the OSHA enforcement will exercise discretion concerning the annual fit testing requirements in response to the shortage of filtering facepiece respirators due to COVID-19 as long as employers have made “good-faith efforts” to comply with fit testing standards.20 A fit test is OC TOBER 2 0 2 0 535

respiratory protection C D A J O U R N A L , V O L 4 8 , Nº 1 0

TABLE 3

Guide to the Selection of Common Face Masks and Respirators Used by DHCPs8,14–16

not required for PAPRs with loose-fitting headgear such as hoods and helmets. The QLFT is usually performed for halfface respirators like the N95 mask.21 As discussed, surgical masks often fit loosely, functioning to prevent the wearer from spreading large sprays and droplets and from hand-to-face contact but fail to protect the wearer from smaller airborne droplets. When using respirators, a key component for protection is providing the wearer with an appropriate fit test to improve the efficacy of the respirator in use. In a study that focused on respirator efficacy and fit performance, researchers found that even when using respirators with high filtering capacity, 10% to 40% of particles penetrated a facial seal as a result of improper fit. For aerosols containing organisms with a low infectious dose, such as tuberculosis, the level of facial seal leakage would not prevent exposure during a brief encounter with an infected patient generating an abundant amount of aerosol.22 Due to close proximity to patients and high aerosol concentrations generated by routine dental procedures, the DHCP should demonstrate strict airborne precautions to avoid exposure. A respirator’s assigned protection factor (APF) is only valid if it fits correctly.7 Respirator fit is important because it involves concerns such as seal, compatibility and stability. A seal ensures that the respirator is being worn properly and protects the wearer from aerosol exposure. A mask cannot properly seal if the wearer has any facial hair, including beards, mustaches or even stubble, so the wearer must be clean-shaven when present for a fit test.21 Compatibility ensures that other PPE, such as eye shields and hard hats, will not disrupt the effectiveness of the respirator being worn. For this reason, any additional PPE that will be worn with the mask should be worn during the fit test. And lastly, 536 OC TOBER

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Category

Type of mask

Use in dental office

Maximum performance

Respirators such as N95

Recommended for moderate to heavy spray/aerosolgenerating procedures.

ASTM Level 3 masks

See TABLE 1

Procedures in which a moderate to heavy number of spray/aerosols are produced and if N95 is unavailable.*

ASTM Level 2 masks

See TABLE 1

Recommended for lab/ instrument processing or procedures generating low fluid/aerosol.

ASTM Level 1 masks

See TABLE 1

Administrative procedures, previsit patient temperature screening, visits with no fluids, spray or aerosol.

Low performance

Surgical-molded utility mask

Best used as a comfortable substitute for ear loop face masks. Used for a physical barrier. Not recommended for DHCP use.

Minimum performance

Standard utility ear loop mask

Physical barrier only. Not recommended for DHCP use.

Example image

*The use of a Level 3 surgical mask instead of a respirator carries a higher risk of exposure due to lack of a facial seal. Mask images provided courtesy of Crosstex International Inc. © 2020 and (Johnny Greig)/(Getty Images)

stability determines the respirator’s ability to retain a seal while the wearer is in motion. The QLFT may only be used to fit test negative-pressure, air-purifying respirators such as the N95 mask. The test relies on the subject to be able to detect leakage into the mask with smell or taste. Rather than measuring the amount of leakage, it is a pass/fail test assessing the user’s ability to detect isoamyl acetate, saccharin, Bitrex and irritant smoke. The isoamyl acetate (banana smell) test is an odor detection

test, the saccharin (sweet) and Bitrex (bitter) tests are taste-detection tests and the irritant smoke test relies on an involuntary irritation (cough) response by the wearer. In order for a QLFT test to be meaningful, care must be taken so that the substances may only enter through a facial leak, meaning that the respirator must have the capacity to filter all substances. Isoamyl acetate is only for testing respirators with organic vapor cartridges, and the irritant smoke can only be used for respirators with level 100

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particulate filters. Saccharin and Bitrex can test respirators with particulate filters of any class. Each QLFT method uses each of these seven exercises performed for one minute: normal breathing, deep breathing, moving head side to side, moving head up and down, bending over or jogging in place, talking and then normal breathing once again.21 The test must be done with the respirator the user will use in the office because the fit test is respirator specific. The QNFT can be used to fit test any tight-fitting respirator, usually a full-face respirator. The test involves using an instrument to measure leakage around the face seal and produces a numerical result called a fit factor. A fit factor is defined as the ratio of the test agent concentration outside the respirator to the test agent concentration inside the respirator or the ratio of total airflow through the respirator to the airflow through face seal leaks. OSHA accepts three QNFT protocols. The first accepted protocol is generated aerosol, which uses a nonhazardous aerosol such as corn oil generated in a test chamber. The second is a condensation nuclei counter (CNC), which uses environmental aerosol and does not require a test chamber. The third is a controlled negative pressure test, which creates a vacuum by temporarily cutting off air. QNFT uses the same seven exercises described in the QLFT plus an additional test where the participant “grimaces” (smiles or frowns) for 15 seconds. A fit factor of at least 100 is required for half-mask respirators and a minimum fit factor of 500 for a fullfacepiece negative pressure respirator.7,21 Different types of N95 respirators should be available for testing if there is a failure of the fit test due to respirator contour. Any change in facial contours including extensive dental work, weight change, facial surgery or facial scarring will dictate a new fit test.

PPE in the Dental Setting

Once employees in a dental office have been properly fit tested for a respirator, the CDC recommends that the DHCP receives education on factors including when to use specific PPE, what PPE is necessary for each procedure, how to properly don, wear, doff and dispose of their protective equipment and the limitations of their PPE. The CDC recommends that when treating patients who are assumed to be noncontagious during an aerosolgenerating procedure, the DHCP should use an N95 respirator or other respirator

The CDC has developed a series of guidelines to optimize PPE supplies, including a PPE Burn Rate Calculator that offices may use to ration their supplies. with a higher level of protection.23 When donning a face mask or a respirator, one must wash their hands thoroughly and secure the top strap or tie on the crown of the head and the bottom strap on the base of the neck. Face masks with ear loops may be worn by placing the loops securely around the ears. Users should perform a seal check with every use of their respirator. Positive pressure seal checks are done with respirators without valves. After donning the respirator, place hands over respirator amd exhale gently; the fit is considered acceptable if positive pressure is built up in the mask without leakage. Any air movement at the borders of the respirator, fogging of glasses or lack of pressure is a failure.24 After completion of care, the DHCP should perform hand hygiene once again and exit the patient

care area to remove their face mask or respirator. A face mask may be removed by pulling it away from the face by the ear loops or ties without touching the front of the mask. A respirator should be removed by pulling the bottom strap up over the head, followed by the top strap, and pulling the respirator away from the face without touching the front of the respirator. The DHCP should perform hand hygiene once more after removing their face mask or respirator.23 Major distributors have reported a shortage of PPE in the U.S., specifically face masks and respirators. The CDC has developed a series of guidelines to optimize PPE supplies in the workplace, including decontamination strategies and a PPE Burn Rate Calculator that offices may use to ration their supplies.25 In times of contingency, the reuse of N95 respirators may be considered. However, it is unclear how reuse affects the respirator function and contamination. In general, respirators contaminated with blood, saliva or respiratory secretion should be discarded after aerosol procedures. Other used respirators can be hung in designated areas or stored in a paper bag between uses to minimize cross-contamination.26 Ultraviolet germicidal irradiation, vaporous hydrogen peroxide and moist heat have been discussed as effective methods of decontamination. The use of dry heat, autoclave, isopropyl alcohol, soap, microwave, bleach, disinfectant wipes and ethylene oxide should not be used due to degradation to the mask or harm to the wearer. The manufacturers of N95 respirators should be contacted for reuse guidance and recommendations.27 Respirators may also be used past their shelf life in times of limited supply. However, the expired respirator may not perform at the same capacity once past its manufacturer’s designated expiration date. The straps may OC TOBER 2 0 2 0 537

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degrade, causing the fit and seal to be unsatisfactory.28 It is recommended that expired respirators only be used for nonaerosol-producing procedures.

Physiologic Effects

Heart rate, temperature, humidity and subjective comfort are influenced by the wearing of different kinds of face masks and respirators. The temperature inside of a mask increases with exercise and movement, which in many wearers may give the perception of breathing resistance, leading to an increased breathing rate.29 High breathing rates make it difficult to take in sufficient oxygen, which triggers the sympathetic nervous system to increase heart rate. This chain of events can lead the wearer to feel fatigued, faint and uncomfortable. While both surgical masks and respirators can cause these effects, notable differences have been made between N95 and surgical masks in terms of comfort and altered sensations. Overall humidity, skin temperature inside the mask, perceptions of breathing resistance and discomfort have been found to be higher among N95 than surgical masks.29 Headaches have also been noted to have a higher incidence following the extended (> 4hr) use of N95 masks due to increased respiratory rate and discomfort.30 Surgical masks, with higher moisture and air permeability, are thinner than N95 respirators, making them more breathable and in turn more comfortable for the wearer. All these factors may be reasons for reluctance to wear respirators in the workplace. However, the respirator’s superior fit and filtration should override these inconveniences.

Conclusion

A thorough understanding of the types and uses of face masks and respirators in the dental office is paramount for the DHCP’s respiratory health. In addition,

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every dental practice should institute a respiratory protection program that includes mitigation strategies, respirator selection, medical evaluations, fit testing, training and maintenance of respirators.31 A respiratory protection program, along with the PPE required for standard and airborne precautions, will ensure the safety of the dental team and dental patient. n REFERENCES 1. Rockwood CA, O’Donoghue DH. The surgical mask: Its development, usage and efficiency. Arch Surg 1960 Jun;80:963– 71. doi: 10.1001/archsurg.1960.01290230081010. 2. Centers for Disease Control and Prevention. Guidelines for Infection Control in Dental Health-Care Settings — 2003. www.cdc. gov/mmwr/preview/mmwrhtml/rr5217a1.htm. 3. Centers for Disease Control and Prevention. Transmission-Based Precautions. www.cdc.gov/infectioncontrol/basics/transmissionbased-precautions.html. 4. Xie X, Li Y, Sun H, Liu L. Exhaled droplets due to talking and coughing. J of R Soc Interface, 2009 Dec 6;6 Suppl 6(Suppl 6):S703-14. doi: 10.1098/rsif.2009.0388.focus. Epub 2009 Oct 7. 5. U.S. Food and Drug Administration. N95 Respirators, Surgical Masks and Face Masks. www.fda.gov/medical-devices/personalprotective-equipment-infection-control/n95-respirators-surgicalmasks-and-face-masks. 6. Desai AN, Mehrotra P. Medical Masks. JAMA 2020 Mar 4. doi: 10.1001/jama.2020.2331. Online ahead of print. 7. ASTM International. Standard Specification for Performance of Materials Used in Medical Face Masks F2100-19. www.astm.org/ COVID-19. 8. Occupational Safety and Health Administration. Assigned Protection Factors for the Revised Respiratory Protection Standard. www.osha.gov/Publications/3352-APF-respirators.pdf. 9. University of California, Santa Cruz. Filtering Facepiece Respirators (Particle Masks N-95 to P-100). ehs.ucsc.edu/ programs/safety-ih/documents/n95.pd. 10. CDC–NIOSH. Respirator Fact Sheet: Understanding Respiratory Protection Against SARS. www.cdc.gov/niosh/npptl/ topics/respirators/factsheets/respsars.html. 11. Centers for Disease Control and Prevention. Elastomeric Respirators: Strategies During Conventional and Surge Demand Situations. www.cdc.gov/coronavirus/2019-ncov/hcp/ elastomeric-respirators-strategy/index.html. 12. Centers for Disease Control and Prevention. Considerations for Optimizing the Supply of Powered Air-Purifying Respirators (PAPRs). www.cdc.gov/coronavirus/2019-ncov/hcp/ppe-strategy/ powered-air-purifying-respirators-strategy.html. 13. Roberge MR, Vojtko MR, Roberge R, Vojtko RJ, Landsittel DP. Wearing an N95 Respirator Concurrently With a Powered AirPurifying Respirator: Effect on Protection Factor. Respir Care 2008 Dec;53(12):1685–1690. 14. California Dental Association. Preparing Your Practice: PPE Recommendations for Dental Practices. www.cda.org/ Home/Practice/Back-to-Practice/Preparing-your-Practice/pperecommendations-for-dental-practice. 15. Crosstex: A Cantel Medical Company. Guide to Face Mask

Selection and Use. www.primedentalsupply.com/files/facemaskselection-guide.pdf. 16. Cardinal Health. N95 Respirators. www.cardinalhealth.com/ en/product-solutions/medical/infection-control/facial-protection/ respirators.html. 17. U.S. Department of Labor. Enforcement guidance for use of respiratory protection equipment certified under standards of other countries or jurisdictions during the pandemic. www.osha. gov/memos/2020-04-03/enforcement-guidance-use-respiratoryprotection-equipment-certified-under. 18. Centers for Disease Control and Prevention. International Assessment Results. www.cdc.gov/niosh/npptl/respirators/testing/ NonNIOSHresults.html. 19. Centers for Disease Control and Prevention. Strategies for Optimizing the Supply of Facemasks: COVID-19. www.cdc.gov/ coronavirus/2019-ncov/hcp/ppe-strategy/face-masks.html. 20. U.S. Department of Labor. Temporary Enforcement Guidance — Healthcare Respiratory Protection Annual Fit-Testing for N95 Filtering Facepieces During the COVID-19 Outbreak. www.osha. gov/memos/2020-03-14/temporary-enforcement-guidancehealthcare-respiratory-protection-annual-fit. 21. U.S. Department of Labor. Part I. OSHA-Accepted Fit Test Protocols A. Fit Testing Procedures—General Requirements. www. osha.gov/laws-regs/regulations/standardnumber/1910/1910. 134AppA. 22. Oberg T, Brosseau LM. Surgical mask filter and fit performance. Am J Infect Control 2008 May;36(4):276–82. doi: 10.1016/j. ajic.2007.07.008. 23. Centers for Disease Control and Prevention. Guidance for Dental Settings. www.cdc.gov/coronavirus/2019-ncov/hcp/ dental-settings.html. 24. National Institute for Occupational Safety and Health. Filtering out confusion: Frequently asked questions about respiratory protection — user seal check. doi:10.26616/nioshpub2018130. 25. Personal Protective Equipment (PPE) Burn Rate Calculator. www.cdc.gov/coronavirus/2019-ncov/hcp/ppe-strategy/burncalculator.html. 26. Centers for Disease Control and Prevention. Recommended Guidance for Extended Use and Limited Reuse of N95 Filtering Facepiece Respirators in Healthcare Settings. www.cdc.gov/niosh/ topics/hcwcontrols/recommendedguidanceextuse.html. 27. Centers for Disease Control and Prevention. COVID-19 Decontamination and Reuse of Filtering Facepiece Respirators. www.cdc.gov/coronavirus/2019-ncov/hcp/ppe-strategy/ decontamination-reuse-respirators.html. 28. Centers for Disease Control and Prevention. Strategies for Optimizing the Supply of N95 Respirators: COVID-19. www.cdc. gov/coronavirus/2019-ncov/hcp/respirators-strategy/index.html. 29. Li Y, Tokura H, Guo YP, et al. Effects of wearing N95 and surgical facemasks on heart rate, thermal stress and subjective sensations. Int Arch Occup Environ Health 2005 Jul;78(6):501–9. doi: 10.1007/s00420-004-0584-4. 30. Lim ECH, Seet RCS, Lee K-H, et al. Headaches and the N95 face-mask amongst healthcare providers. Acta Neurologica Scandinavica 113(3), 199–202. doi: 10.1111/j.16000404.2005.00560.x 31. California Dental Association. Respiratory Protection Program. www.cda.org/Home/Practice/Back-to-Practice/Preparing-yourPractice/respiratory-protection-program. THE AUTHOR, Emma Bhaskar, BS, can be reached at e_bhaskar@u.pacific.edu.

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literature review

COVID -19: New Considerations for Respiratory Protection in Dental Practice Bruce L. Whitcher, DDS

a b s t r a c t Dentistry has been identified as a “very high-risk” occupation due to

the risk of SARS-CoV-2 transmission via aerosol-generating procedures, which are integral to the practice of dentistry. This makes respiratory protection a concern for every practicing dentist, their staff and their patients.

AUTHOR Bruce L. Whitcher, DDS, practices oral and maxillofacial surgery in Paso Robles, Calif. He served as a member of the Dental Board of California from 2009 to 2019, serving on the licensing, enforcement and anesthesia committees as well as on the Dental Assisting Council. Dr. Whitcher is a past CDA trustee and a past member of the California Association of Oral and Maxillofacial Surgeons board of directors, serving as president in 2007. Conflict of Interest Disclosure: None reported.

n July 13, 2020, Gov. Gavin Newsom announced statewide restrictions to again halt all indoor dining and close bars, movie theaters, zoos and museums. In addition to these restrictions, more than 25 counties, including Los Angeles, were forced to close gyms, places of worship, hair salons, malls and nail salons. On Aug. 22, 2020, California reported 644,751 confirmed positive cases of COVID-19, the most of any state.1 This includes 5,920 new cases representing a 0.9% increase. California’s positivity rate — a key indicator of community spread (the positivity rate is the percent of tests that come back positive) — is at the time of this writing 5.7% and decreasing. Hospitalization rates are also decreasing in the 14-day average, with 4,890 new hospitalizations reported for a 3.3% decrease and a 2.1% decrease in ICU patients. As of Aug. 21, 2020, a total of 11,686 deaths were attributed to COVID-19 in the state. There is currently no vaccine

to prevent COVID-19. The best way to prevent illness is to avoid being exposed to this virus. The virus spreads mainly from person to person between people who are in close contact with one another (within about 6 feet). This occurs by respiratory droplets produced when an infected person coughs or sneezes. These droplets can land in the mouths or noses of people who are nearby or can possibly be inhaled into the lungs. Surfaces can also transmit infection. Older adults and people who have severe underlying medical conditions such as hypertension, obesity (BMI > 30), heart or lung disease, diabetes, chronic kidney disease, sickle cell disease or immunocompromised systems seem to be at higher risk for developing more serious complications from the COVID-19 illness.2 The differences in health outcomes related to COVID-19 are most stark in COVID-19 deaths. We have nearly complete data on race and ethnicity for COVID-19 deaths, and we are seeing the following trends: Latinos, African OC TOBER 2 0 2 0 539

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Americans and Native Hawaiians and Pacific Islanders are dying at disproportionately higher levels. More males are dying from COVID-19 than females, in line with national trends.3 In early July, some California counties began utilizing the “attestation process” to certify that the spread of COVID-19 was under control locally. To qualify, counties had to prove they had stable hospitalizations, COVID-19 cases on the decline, adequate contact tracing and other criteria. In response to the increasing numbers of cases, the state created a monitoring list of counties where COVID-19 trends were particularly concerning. It started with about a dozen counties at the end of May. As of late July, more than half of California counties were on the monitoring list. On July 13, 2020, the state health director issued an order to require specified indoor businesses to cease operations. In addition, counties that remained on the county monitoring list for three consecutive days were required to shut down specified industries including gyms, fitness centers, places of worship, personal care services and other activities unless they could be modified to operate outside. Due to difficulties with data transmission from testing laboratories to the California Reportable Disease Information Exchange (Cal REDIE) tracking system, the county monitoring list was frozen between Aug. 1 and Aug. 16. There was considerable concern about the effects of inadequate transmission of testing data on COVID-19 case statistics because this affected the day-over-day reported case data.4 The backlog of 300,000 cases was quickly cleared by collaboration between the California Department of Public Health (CDPH) and the California Department of 540 OC TOBER

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Technology (CDT) and was most likely the result of overburdened data management systems.

Government Oversight

Several state and federal government agencies provide guidance or oversee the health care workplace, including the Centers for Disease Control and Prevention (CDC), Occupational Health and Safety Administration (OSHA), Cal/OSHA, CDPH, the Dental Board of California and international organizations such as the World Health Organization (WHO).

In early July, some California counties began utilizing the “attestation process” to certify that the spread of COVID-19 was under control locally.

CDC Recommendations for Dental Care

The CDC recommends respiratory protection during treatment of patients with suspected or confirmed COVID-19 disease and that these patients should receive medically necessary emergency dental care according to the CDC’s Interim Infection Prevention and Control Recommendations for Patients with Suspected or Confirmed Coronavirus Disease 2019 (COVID-19) in Health Care Settings.5 The decision to treat these patients should be made in conjunction with the patient’s medical provider to determine the appropriate setting for care. Due to evidence of transmission by asymptomatic individuals, the CDC recommends that during aerosolgenerating procedures (AGPs) conducted

on patients assumed to be noncontagious, dental health care workers (DHCWs) should use an N95 respirator or a respirator that offers a higher level of protection such as other disposable filtering facepiece respirators, powered air purifying respirators (PAPRs) or elastomeric respirators, if available.6 Respirators should be used in the context of a respiratory protection program, which includes medical evaluations, training and fit testing if necessary. Of note, it is uncertain if respirators with exhalation valves provide source control though they provide adequate respiratory protection for the DHCW. Cal/OSHA approves their use during respirator shortages and recommends using a full-face shield to deflect expiration. If a respirator is not available for an AGP, use both a surgical mask and a full-face shield. Ensure that the mask is cleared by the U.S. Food and Drug Administration as a surgical mask. Use the highest-level mask available. If a surgical mask and a full-face shield are not available, do not perform any AGPs.

Cal/OSHA

The California Division of Occupational Health and Safety (Cal/OSHA) is the state’s agency that regulates employee safety under the California Department of Industrial Relations. Unlike the CDC, Cal/OSHA has enforcement authority and may carry out workplace inspections. Cal/OSHA recently proposed new industry guidance for dentistry. An early version is similar to CDC and OSHA guidance published to date.

OSHA

OSHA has identified dentistry as a “very high-risk” occupation due to the risk of SARS-CoV-2 transmission by AGPs utilized during dental practice.7

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AGPs are integral to the practice of dentistry, making respiratory protection a major concern for every practicing dentist, their staff and their patients. Although the CDC, OSHA, CDPH and others have indicated that wearing an effective N95 mask or, under some circumstances, an approved Level 3 surgical mask provides adequate respiratory protection, these guidelines recommend use of the highest level of respiratory protection available for highrisk procedures. The CDC currently recommends that dentists not treat known or suspected COVID-19 patients in a dental practice setting because they typically lack a negative-pressure room to contain virus spread. To date, the CDC reports no cases of clinical transmission due to dental treatment. Dentists may wish to consider whether a higher level of protection is advisable for procedures that generate significant amounts of aerosol, may involve mucosa with a high viral load or where the duration of exposure is extensive. Until more is known about how COVID-19 spreads, OSHA recommends using a combination of standard precautions, contact precautions, airborne precautions and eye protection (e.g., goggles, face shields) to protect health care workers.8 OSHA regulations require that respirators appropriate for workplace safety must be provided through a respiratory protection program. Any employee using a respirator voluntarily must be medically able to use that respirator. The respirator must be cleaned, stored and maintained so that its use does not present a health hazard to the user. The employer shall designate a qualified program to administer or oversee the respiratory protection program and conduct the required evaluations of program

effectiveness. The employer shall provide respirators, training and medical evaluations at no cost to the employee. OSHA specifies that the employer shall provide a powered air-purifying respirator (PAPR) if the medical evaluation finds that the employee cannot use a negative-pressure respirator; if a subsequent medical evaluation finds that the employee is medically able to use a negative-pressure respirator, then the employer is no longer required to provide a PAPR. A negative-pressure respirator means

Dentists may wish to consider whether a higher level of protection is advisable for procedures that generate significant amounts of aerosol.

any tight-fitting respirator in which the air pressure inside the facepiece is negative during inhalation with respect to the ambient air pressure outside the respirator. The disposable N95 filtering facepiece respirator is a negative-pressure respirator. OSHA requires fit testing for negative-pressure respirators.9 Nearly all PAPRs are positive-pressure respirators that use a blower to provide clean filtered air; PAPRs do not require fit testing.

Review of SARS-CoV-2 Transmission Among Dental Health Care Workers Reports of SARS-CoV-2 transmission to health care workers appeared early in the pandemic. By the end of January 2020, 11 hospitals in Wuhan, China, had reported over

15 confirmed cases among health care workers.10 Unfortunately, a substantial number of health care workers were infected in health care settings before the end of January 2020. On Feb. 24, 2020, the WHO-China Expert Group conference stated that a total of 3,387 infected cases (2,055 confirmed cases, 1,070 diagnosed cases and 157 suspected cases) were health care workers in 476 health care settings, of whom 3,062 were in Hubei, China (90.4%). Although SARS-CoV-2 itself is significantly infectious, it should not be held fully responsible for the extensive spread of the infection. In fact, the main reasons for earlier virus transmission to health care workers were due to lack of awareness of adequate protection of health care workers and leaders in health care settings, and later transmissions were the result of an insufficient supply of PPE.9 The risk of SARS-CoV-2 transmission to DHCWs by aerosolgenerating dental and medical procedures was identified early in the pandemic. The Center for EvidenceBased Stomatology, School and Hospital of Stomatology, Wuhan University in Wuhan, China, reported nine cases of COVID-19 among 169 staff members after treating more than 700 patients at their facility since January 2020.11 There have been no further cases among colleagues or patients who had close contact with them. According to analyses of epidemiologic investigation and medical history, all of these cases are without documented association, except two nurses from the same department (patients 2 and 3), one of whom (3) had been in contact with a family member with COVID-19. For cases 1 and 2, the staff and the student with confirmed COVID-19 stated that they did not contact one another OC TOBER 2 0 2 0 541

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closely, and most of them had been away since Jan. 22 or 23, 2020, because of the Chinese Spring Festival. These cases were therefore determined unlikely to result from cross infection among staff members. Treatment at this facility was limited to dental emergencies and utilized infection control measures that included prescreening patients for signs and symptoms of COVID-19. The lack of transmission among staff members was attributed to the use of PPE, including masks, gloves, gowns and goggles or face shields. As respiratory droplets are the main route of SARS-CoV-2 transmission, N95 masks were worn in clinical treatment areas.12 A report from Zhejiang University Hospital in Hangzhou, China, reported no cases of COVID-19 transmission in the dental setting but described the difficulty of identifying asymptomatic patients who may carry and transmit the virus.11 In addition to the “standard precautions,” the authors recommend specific precautions for dental practices to reduce the risk of transmission of SARS-CoV-2 that can be applied in dental care settings during this outbreak. These recommendations are based on the COVID-19 interim guidance set forth by the WHO (2020) and current clinical practice in China. It remains unclear if any DHCWs are being infected in the work setting despite effective droplet precautions as opposed to those who are infected because of inadequate PPE. Wang et al.14 suggest that the considerable number of early health care infections and deaths may have been due to a combination of inadequate PPE due to lack of awareness early in the epidemic, large-scale exposure to infected patients, shortage of PPE and inadequate infection prevention training.

significant knowledge gap regarding AGPs and the lack of agreement as to which procedures should be included. Guidance is based on the widely referenced systematic review by Tran et al.15 that identifies tracheal intubation as the only procedure that is consistently associated with SARS transmission. At present, no guidelines can be established based on specific evidence of infectivity of SARS-CoV-2 during AGPs. This knowledge gap leaves clinicians unsure whether procedures are safe to undertake. Lack of clarity of risk may in turn lead to preventable infections of health care workers if procedures are

WHO Guidance

It is likely that there is a hierarchy of AGPs in the sense that each will convey a different degree of risk of infection transmission. It is generally advised that for

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The lack of transmission among staff members was attributed to the use of PPE, including masks, gloves, gowns and goggles or face shields. undertaken without appropriate PPE or to worse outcomes for patients if procedures are withheld due to safety concerns.16,17 AGPs are performed worldwide in oral health care settings. AGPs are defined as any medical, dental or patient care procedure that results in the production of airborne particles < 5 μm in size that can remain suspended in air, travel over a distance and may cause infection if they are inhaled. The risk of airborne COVID-19 transmission when AGPs are performed can therefore not be excluded.

Management of AGPs in the COVID-19 Era

AGPs in addition to standard precautions, patients suspected or known to be infected with SARS-CoV-2 should, if possible, be treated in a negative-pressure room, that health care workers (HCWs) should always wear a gown, gloves, face shield and goggles and an N95-level mask and that these procedures should only be undertaken when absolutely necessary.18 Givi et al.19 suggest that health care workers should consider using PAPRs for certain high-risk ear, nose and throat aerosol-generating medical procedures performed on patients with probable or confirmed COVID-19.

Does Airborne Transmission of SARS-CoV-2 Occur?

The role of airborne transmission of SARs-CoV-2 is debated extensively in the literature.20 WHO guidance indicates that the possibility of airborne transmission during dental procedures cannot be excluded. Much remains unknown about whether the aerosolized virus is infectious and what amount of virus one needs to be exposed to become sick, known as the minimal infectious dose. Even if aerosol transmission does occur, it is not clear how common it is compared with other transmission routes, such as droplets or surfaces.21 It has been shown that SARSCoV-2 can survive in aerosols for at least three hours (with a similar reduction in titer as occurs with SARS-CoV-1). This does not confirm airborne transmission, but it establishes that airborne transmission is feasible and supports comparisons between SARS-CoV-2 and SARS-CoV-1 transmission routes.

Testing

Is preprocedural laboratory testing for COVID-19 advisable to apply more effective use of PPE for respiratory protection? Depending on testing availability and how rapidly results are available, facilities may consider

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TABLE

Respirator Selection Guide for Aerosol Transmissible Diseases

implementing preadmission or preprocedure testing for COVID-19, which might inform implementation of PPE for respiratory protection, especially in the situation of PPE shortages. However, limitations of this approach should be considered, including negative results from patients during their incubation period who could become infectious later and false negative tests depending on the test method used. Due to difficulties with contact tracing, the CDC has advised facilities to consider forgoing formal contact tracing and work restrictions for DHCWs with exposures in favor of universally applied symptom screening and source control strategies. HCWs who have been present in a room during an AGP for a patient with COVID-19 while not wearing the full complement of PPE, such as a gown, gloves, eye protection and a respirator, are classified as having high-risk exposure and should be excluded from work for 14 days and monitored for symptoms. HCWs who were in the room during an AGP while wearing the full complement of PPE, such as a gown, gloves, eye protection and respirator, do not need to be placed on work restrictions but should be monitored for fever and symptoms of COVID-19.18 Data are insufficient to precisely define the duration of time that constitutes a prolonged exposure. Until more is known about transmission risks, it is reasonable to consider an exposure of 15 minutes or more as prolonged. However, any duration should be considered prolonged if the exposure occurred during performance of an aerosol-generating procedure (TABLE). The employer is responsible for selecting PPE, including but not limited to respiratory protection, appropriate for the hazard and the environment. The employer can always choose to select a higher level of respiratory protection than the minimum required.

Disease

Job task

Respirator

Airborne infectious disease* (suspected or confirmed)

Routine patient care and support operations

At least N95

High-hazard procedures

At least PAPR

Routine patient care and support operations

In accordance with facility policy; CDPH recommends at least permitting optional N95 use

High-hazard procedures**

At least N95

In accordance with facility policy

Seasonal influenza (suspected or confirmed)

Other disease requiring droplet precautions***

The employer is responsible for selecting PPE, including but not limited to respiratory protection, appropriate for the hazard and the environment. The employer can always choose to select a higher level of respiratory protection than the minimum required. * See list on cdph.gov / ** See definition on cdph.gov / *** See list on cdph.gov California Department of Public Health, Occupational Health Branch, August 2015

Do PAPRs, Elastomeric Respirators or N95 Filtering Facepiece Respirators Provide Greater Protection?

PAPRs, reusable elastomeric respirators and filtering facepiece respirators (e.g., N95 masks) represent different methods of filtering out aerosols in the air. Although cost estimates vary, a PAPR has the highest initial cost, as much as $1,400. A PAPR22 contains a battery-powered, high-efficiency particulate air filter that delivers clean air into a hood or a full-face mask and blows off exhaled air. The hood is either hard and tight fitting or loose. The risk of leakage with PAPRs is negligible and, unlike reusable elastomeric respirators and N95 masks, there is no need for a fit test or additional eye protection because the head is completely enclosed within the system. This feature of the PAPR benefits individuals who fail fit tests and those whose religious beliefs prevent them from shaving. Decontamination protocols for PAPRs must be in place and adhered to meticulously before they are reused. Reusable elastomeric respirators, which typically cost less than $100, are used more commonly in heavy industry than health care. Such devices are made to meet National Institute for Occupational Safety and Health (NIOSH) standards and are defined by the ability of the device to filter out oil or nonoil particulate. They may either cover the lower half of the face (and

require additional eye protection) or cover the entire face.23 Like PAPRS, they are not often used in dentistry, but have advantages over the N95 for high-level respiratory protection, including a single fit test, lower long-term costs because only the filters are replaced, more comfort breathing especially over long periods and can be reused for future aerosol transmissible disease protection.24 Respirators are classified according to their particulate filtration efficiency. Both reusable elastomeric respirators and filtering facepiece respirators come in N100 (99.7%), N99 (99% filtration efficiency) and N95 (95% filtration efficiency) varieties. An “N, R or P” prefix indicates the relative resistance to oil. A highefficiency filter has at least 99.7% efficiency and is found only in PAPRs. The familiar N95 mask can cost more than $10 each, and the cost is highly dependent on availability. In addition, the cost of annual fit testing can be substantial and there have been persistent problems with the availability of quality N95 masks. The use of PAPRs could help alleviate N95 supply chain problems until production of N95 masks can be increased to meet the demand.22 Although PAPRs have long been used in hazardous industrial environments and to some extent in hospital and medical research environments, they are a new option for OC TOBER 2 0 2 0 543

respiratory protection C D A J O U R N A L , V O L 4 8 , Nº 1 0

hazard reduction in dentistry. A combination of N95 masks and PAPRs is being used in some health care facilities to help overcome shortages of masks.26 Other facilities have successfully adopted a PAPR-only approach when there is an ongoing need for respiratory protection. No studies exist that directly compare the different respirators’ abilities to prevent transmission of viral illness in the health care setting. Such studies would need to incorporate doffing and reprocessing procedures in the experimental design because there is high risk of transmission if doffing is performed incorrectly, and the risk may be modified by the type of PPE used. Experimental studies in the occupational health literature compared how well different respirators filter aerosols (typically sodium chloride aerosols) in simulated industrial environments. Respirators are assigned a protection factor (APF) that is a measure of the ratio of airborne contaminant inside and outside the respirator.23 The APF for PAPRs is usually 25 versus 10 for filtering facepiece respirators, 10 for half-mask elastomeric respirators and 50 for full-facepiece elastomeric respirators. Higher APFs from 1,000 up to 10,000 are usually assigned to atmosphere supplying systems such as supplied air systems (SARs) and selfcontained breathing apparatus (SCBA) designed for immediately dangerous to life or health (IDLH) environments. A major risk with filtering facepiece respirators and reusable elastomeric respirators is that the airtight seal can leak during a procedure, compromising their performance. In a study of eight subjects each tested on six different N95 masks, thermal imaging showed that leakage (mainly in the nasal and malar regions) occurred in all failed leak tests and the majority (26 of 35) passed fit tests. The risk of leakage 544 OC TOBER

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would be expected to increase with the length of time the N95 mask is worn, for example, during long cases.25 There is concern that the unfiltered exhaust from PAPRs may increase the risk of transmission of virus particles to patients from users who are unknowingly infected with COVID-19, but this risk would likely be diminished if PAPR users wore surgical masks. PAPRs may be cumbersome to use, may fog up and prevent the use of headlights, but these concerns are also true of masks, face shields and goggles. The balance of evidence suggests that PAPRs and full-facepiece elastomeric

The risk of leakage would be expected to increase with the length of time the N95 mask is worn, for example, during long cases.

respirators, when properly used, doffed and reprocessed, would be expected to reduce the risk of transmission of infection and/or severity of illness by reducing exposure during high-risk cases compared to N95 masks. Cost-effectiveness studies comparing different respirator types have not been performed, but it may be feasible for some dental practices to acquire a limited number of PAPRs for use during high-risk procedures. One of the challenges facing those considering using a PAPR is that very few dentists have experience using them. This limits the exchange of information among colleagues that traditionally occurs when dentists consider purchasing a new piece of equipment or adopting a new technique. Although a handful of manufacturers have provided virtual demonstrations

of PAPRs for use in dentistry, this is a limited form of evaluation and does not give the dentist considering an expensive piece of equipment the opportunity to “try before they buy.” In 2015, the Institute of Medicine convened a symposium to review the use of PAPRs in several medical facilities.24 We interviewed for this article three dentists about their experience wearing PAPRs. They reported an experience similar to findings from this symposium that includes several studies of PAPRs conducted by the Veterans Administration (VA).26 California dentists reported that PAPRs were more comfortable than an N95 mask worn with a face shield and other PPE, but that at times there were difficulties with missing PAPR components. Donning and doffing the units requires a trained assistant. Users experienced some difficulty with communication due to reduced hearing and some had heavy air-supply units that were difficult to wear for long cases. In addition, one dentist experienced drying of the cornea due to the constant flow of air from the supply duct. VA employees found PAPRs more comfortable than half-face elastomeric masks or N95 respirators. However, among a variety of respirators studied, none of the tested devices were well tolerated for an entire eight-hour shift by all test participants. In one 2009 study, half of the study subjects had removed their respiratory protective device by the end of an eight-hour work shift, regardless of the type of respirator used. VA researchers found that PAPRs were primarily disliked, not because they were uncomfortable but because they might interfere with occupational activities and might be somewhat challenging to use in certain situations. The major challenge with respirators lies not in designing an effective one, but in persuading people to wear it and to wear it correctly. Respiratory training is not taken as seriously as

C D A J O U R N A L , V O L 4 8 , Nº 1 0

bloodborne pathogen training even though both promote a safe health care workplace. All respiratory protection devices have advantages and disadvantages. The major advantage of PAPRs is that many types do not require fit testing. It is estimated that close to 10% of workers cannot be fitted for an elastomeric or N95 respirator due to facial hair or other reasons. Another advantage to using PAPRs is their reusability. The major disadvantages are maintenance and cost. Disposable N95 respirators, while costing much less for an individual respirator, are not as economical if workers need to use respirators day after day for weeks during a pandemic. Other disadvantages that will have to be overcome before PAPRs become common alternatives for respiratory protection in dentistry include auditory communication, comfort, reduced bulk, headlight accommodation, airflow control and ease of donning and doffing. The increasing risk of SARS-CoV-2 transmission now facing the public at large as well as the dental profession bears a striking similarity to the emergence of bloodborne pathogens as a health and safety issue during the AIDS epidemic of the 1980s. Although the transmission of bloodborne pathogens was and continues to be extremely rare, the profession quickly adopted enhanced infection control practices based on CDC guidance, primarily to reduce the risk of disease transmission and improve the quality of care for patients as well as to protect the health of DHCWs. At one time, glove wearing, eye protection and instrument sterilization were viewed as obstacles to the practice of dentistry, but infection control is now considered fundamental to the standard of care. The adoption of infection control in the 1980s conveyed an important message to the public: The dental profession makes patient safety its highest priority.

We may be experiencing now the same kind of shift in thought required by the AIDS crisis. We submit that one day, improved respiratory protection through the use of PAPRs in dentistry may also become commonplace and may eventually be considered integral to the practice of dentistry. n REFERENCES 1. California Department of Public Health. COVID-19 updates. www.cdph.ca.gov/Programs/CID/DCDC/Pages/ Immunization/nCOV2019.aspx. Accessed Aug. 21, 2020. 2. Centers for Disease Control and Prevention. People with certain medical conditions. www.cdc.gov/coronavirus/2019ncov/need-extra-precautions/people-with-medical-conditions. html. Accessed Aug. 21, 2020. 3. California Department of Public Health. COVID-19 statewide update. update.covid19.ca.gov. Accessed Aug. 21, 2020. 4. California Department of Public Health. State officials announce latest COVID-19 facts www.cdph.ca.gov/Programs/ OPA/Pages/NR20-194.aspx. Accessed Aug. 23, 2020. 5. Centers for Disease Control and Prevention. Guidance for dental settings. www.cdc.gov/coronavirus/2019-ncov/hcp/ dental-settings.html. Accessed Aug. 23, 2020. 6. Centers for Disease Control and Prevention. Recommended infection prevention and control (IPC) practices for routine dental healthcare delivery during the pandemic. www.cdc.gov/ coronavirus/2019-ncov/hcp/dental-settings.html#section-1. Accessed Aug. 23, 2020. 7. U.S. Department of Labor, Occupational Health and Safety Administration. Dentistry workers and employers. www.osha. gov/SLTC/covid-19/dentistry.html. Accessed July 21, 2020. 8. U.S. Department of Labor, Occupational Health and Safety Administration. Dentistry Workers and Employers. www.osha. gov/SLTC/covid-19/dentistry.html. Accessed July 21, 2020. 9. Xiang B, Li P, Yang X, Zhong S, Manyande A, Feng M. The impact of novel coronavirus SARS-CoV-2 among healthcare workers in hospitals: An aerial overview. Am J Infect Control 2020 Aug;48(8):915–917. doi: 10.1016/j.ajic.2020.05.020. 10. Meng L, Hua F, Bia Z. Coronavirus disease 2019 (COVID-19): Emerging and future challenges for dental and oral medicine. J Dent Res 2020 May;99(5):481–487. doi: 10.1177/0022034520914246. Epub 2020 Mar 12. 11. Ge ZY, Yang LM, Xia JJ, Zhang YZ. Possible aerosol transmission of COVID-19 and special precautions in dentistry. J Zhejiang Univ Sci B 2020 May;21(5):361–368. doi: 10.1631/jzus.B2010010. Epub 2020 Mar 16. 12. Wang J, Zhou M, Liu F. Reasons for healthcare workers becoming infected with novel coronavirus disease 2019 (COVID-19) in China. J Hosp Infect 2020 May;105(1):100– 101. doi: 10.1016/j.jhin.2020.03.002. Epub 2020 Mar 6. 13. Tran K, Cimon K, Severn M, Pessoa-Silva CL, Conly J. Aerosol generating procedures and risk of transmission of acute respiratory infections to healthcare workers: A systematic review. PLoS One 2012;7(4):e35797. doi: 10.1371/journal. pone.0035797. Epub 2012 Apr 26. 14. Harding H, Broom A, Broom J. Aerosol generating procedures and infective risk to healthcare workers: SARS-CoV-2 — the limits of the evidence. J Hosp Infect 2020

Aug;105(4):717–725. doi: 10.1016/j.jhin.2020.05.037. 15. World Health Organization. Considerations for the provision of essential oral health services in the context of COVID-19. www. who.int/publications/i/item/who-2019-nCoV-oral-health-2020.1. Accessed Aug. 21, 2020. 16. Centers for Disease Control and Prevention. Interim infection prevention and control recommendations for patients with suspected or confirmed coronavirus disease 2019 (COVID-19) in health care settings. www.cdc.gov/coronavirus/2019-ncov/hcp/ guidance-risk-assesment-hcp.html. Accessed Aug. 21, 2020. 17. Givi B, Schiff BA, Chinn SB, et al. Safety Recommendations for Evaluation and Surgery of the Head and Neck During the COVID-19 Pandemic. JAMA Otolaryngol Head Neck Surg 2020 Mar 31. doi: 10.1001/jamaoto.2020.0780. Online ahead of print. 18. Liu Y, Ning Z, Chen Y, et al. Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature 2020 Jun; 582(7813):557–560. doi: 10.1038/s41586-020-2271-3. Epub 2020 Apr 27. 19. Lewis T. How coronavirus spreads through the air: What we know so far. www.scientificamerican.com/article/howcoronavirus-spreads-through-the-air-what-we-know-so-far1. 20. Centers for Disease Control and Prevention. Considerations for optimizing the supply of powered air-purifying respirators (PAPRs) for health care practitioners (HCP). Updated Apr. 19, 2020. www.cdc.gov/coronavirus/2019-ncov/hcp/ppe-strategy/ powered-air-purifying-respirators-strategy.html. Accessed July 22, 2020. 21. Centers for Disease Control and Prevention. Elastomeric respirators: Strategies during conventional and surge demand situations conventional, contingency and crisis strategies. April 2020. www.cdc.gov/coronavirus/2019-ncov/hcp/elastomericrespirators-strategy/index.html. 22. Sreeramoju PV, Cadena J. Airborne Precautions and Personal Protective Equipment: The Powered Air-Purifying Respirator-Only Approach. In: Bearman G, Munoz-Price S, Morgan D, Murthy R eds. Infection Prevention. Cham, Switzerland: Springer. doi.org/10.1007/978-3-319-60980-5_30. 23. U.S. Department of Labor, Occupational Safety and Health Administration. Assigned Protection Factors for the Revised Respiratory Protection Standard. www.osha.gov/Publications/ 3352-APF-respirators.html. Accessed Aug. 22, 2020. 24. National Academies of Sciences, Engineering and Medicine; Health and Medicine Division; Board on Health Sciences Policy; Committee on the Use of Elastomeric Respirators in Health Care; Liverman CT, Yost OC, Rogers BME, et al., ed. Reusable Elastomeric Respirators in Health Care: Considerations for Routine and Surge Use. Washington D.C: National Academies Press; 2018 Dec 6:2, Elastomeric Respirators. 25. Mick P, Murphy R. Aerosol-generating otolaryngology procedures and the need for enhanced PPE during the COVID-19 pandemic: A literature review. J Otolaryngol Head Neck Surg 2020 May 11;49(1):29. doi: 10.1186/s40463-020-00424-7. 26. Liverman CT, Domnitz SB, Mccoy MA. The Use and Effectiveness of Powered Air Purifying Respirators in Health Care. Institute of Medicine. Washington D.C.: The National Academies Press; 2020. THE AUTHOR, Bruce L. Whitcher, DDS, can be reached at whitcher.bruce@gmail.com.

OC TOBER 2 0 2 0 545

Making your transition a reality.

Dr. Thomas Wagner

Dr. Russell Okihara

LIC #01418359

LIC #01886221

Dr. Rishi Salwan LIC #02085289

Jim Engel LIC #01898522

(916) 812-3255 (619) 694-7077 (925) 330-2207 (909) 239-2800 45 Years in Business 38 Years in Business 10 Years in Business 46 Years in Business

Jay Harter LIC #01008086

Kerri McCullough LIC #01382259

Gina Miller LIC #02015193

Steve Caudill LIC #00411157

Jaci Hardison LIC #01927713

Kim Ta LIC #02085576

Thinh Tran LIC #01863784

(916) 812-0500 (949) 300-0312 (707) 391-7048 (949) 675-5578 (951) 314-5542 (408) 687-5001 (949) 675-5578 36 Years in Business 35 Years in Business 30 Years in Business 30 Years in Business 26 Years in Business 16 Years in Business 11 Years in Business

PRACTICE SALES • VALUATIONS/APPRAISALS • TRANSITION PLANNING • PARTNERSHIPS • MERGERS • ASSOCIATESHIPS SACRAMENTO: Price Reduced $70K! Hi-traffic location, Digital, Room to grow as specialties referred out. #CA590 ALAMEDA: New Listing! 4 Ops in busy shopping center. 29 yrs Goodwill. 2019 GR SACRAMENTO: Northern area, 50+ yrs. $246K on 27 hrs/wk. Room to grow!#CA1268 Goodwill, 3 Ops +1, Digital, Paperless, Digital Pano. Specialty referred out. 2019 GR $616K. ALAMEDA: New Listing! 4 Ops, Practice housed in a beautiful Victorian home. 2019 GR #CA667 $1.4M+. Real estate also available if desired. SACRAMENTO: 5 Ops, 4 Equip. 50+ yrs. #CA1287 Goodwill. Digital, CBCT, New computers, 2019 GR $434K (seller took 3 mo. off) #CA678 AUBURN & FOOTHILLS AREA: Fast growing practice in 2,500 sf w/ 6 equip. Ops, SACRAMENTO AREA: GP & Specialty HMO/ 1 add’l plumbed. 2019 GR on track to exceed PPO Practice. 9 Ops+RE, I/O Cam, Digital Pano. $1.2M on 3 avg. Dr. days/wk. #CA632 GR $680K. #CA567 CONTRA COSTA COUNTY WEST: New SAN FRANCISCO FACILITY ONLY: 3 Ops in Listing! 7 Ops, 48 yrs Goodwill with 2019 GR the heart of the city! Leasehold and equipment $1.6M+. Adj. Net $700K+. New computers, only, low rent. Asking $125K. #CA677 Nearly completed paperless charts, Digital Xray, Diagnodent & Diode Laser. 8 hyg days/wk. SAN FRANCISCO: Low Rent! 30+ yrs Goodwill. Beautiful 4 Op office w/ strong hyg program. 2019 and 25 NP/mo. #CA1487 GR $740K+. #CA657 EAST BAY: 4 Ops, 3 equipped. Beautiful SAN JOSE: Great cash flow in beautiful retail updated digital office with 23 yrs Goodwill, Digital, Pano, Lasers, and Nitrous Oxide-ready. space with high traffic/visibility. Spacious 3,150 sf with 10 Ops, 6 Equip. 2019 GR $745K. #CA600 Avg 30 NP/mo. Open 4 days, this is a CASH AND PPO office! 2019 GR $614K. #CA684 SAN JOSE: New Listing! 6 Ops, Paperless, Digital, CAD/CAM, Digital Pano. Seller will stay EAST BAY: Central beautiful location with 4 on P/T, if desired. 2019 GR $1.3M+. #CA1140 Ops in 1,350 sf. 2019 GR $659K on only 4 doctor days/week. #CA644 SONOMA COUNTY: Large GP, 2019 GR above FOLSOM/RESCUE/EDH AREA: 5 Op digital $2.3M. Stand-alone 3,000 sf prime Real Estate, 72 NP/mo.10 hyg days. 6 Ops, Pano X-ray, Dexis, practice, modern space w/ low overhead. 2019 GR $802K. Office condo also for sale. #CA581 Cameras, Laser, Dentrix. Both Business & Real Estate for sale or Lease. Doctor Retiring. #CA544 GREATER EL DORADO HILLS: Multidoctor, 3,000 sf office, 8 Ops, 7 Equip, I/O Cam, SONOMA COUNTY: 2019 GR $939K. 1,000 sf, Digital X-rays & Pano. 2019 GR $2.2M. Sellers 3 Ops w/opportunity to expand. Paperless, Dentrix, Digital, I/O Cam. Selling both Practice and portion will consider working back P/T. #CA578 of dental building ownership. #CA594 GREATER SACRAMENTO: Price Reduced VACAVILLE AREA: Centrally-located & hiby $50K! PPO Practice with 4 Ops, digital sensors, imaging system, I/O Cam. Practice open traffic location with 25+ yrs Goodwill. 5 Ops in 1,700 sf. 2019 GR $556K on 32 hrs/wk. #CA645 33 yrs. 2017 GR $652K; Office Condo available for purchase. #CA561 VALLEJO: 4 Ops, 1,650 sf w/ below-market rent. 2019 GR $791K, 4 hyg days/wk, low OH. GREATER SACRAMENTO: Great area w/ 38 yrs Goodwill. 4 Ops in 1,100 sf. 2018 GR of #CA469 $1M+ on 32 hrs/wk. #CA656 CENTRAL CALIFORNIA LAKE TAHOE AREA ENDO PRACTICE: 3 Ops, 3 digital sensors, Cone Beam in 1,100 sf. CENTRAL COAST: New Listing! 5 Ops, digital, Consistent GR $525K for the last three years on 25+ yrs of goodwill. Newly renovated, the practice sees 30 NP/mo with strong hygiene program. 32 avg. Dr. hrs/wk. #CA602 Beautiful Location. 2019 GR $1.1M+. #CA1218 LAKE TAHOE AREA: GP practice with 5 CENTRAL VALLEY: New Listing! 11 Ops, Ops w/ 6th Open, Operatory views of Lake Tahoe, only 34 Delta Premier patients, 2,100 sf. Digital, Strong hyg. Bldg for sale with practice. 2019 GR $579K on 22 avg. Dr. hrs/wk. #CA608 2019 GR $3.4M w/ high Adj. Net income. #CA1444 MENLO PARK: 4 Ops, rare opp in desirable CENTRAL VALLEY PEDO PRACTICE: area, Digital, Itero Scanner, Paperless, 6 hyg Shared space w/ Ortho, 7 Op, 3,800 sf. 2019 GR days 2019 GR $1M+. #CA686 $610K as part-time practice. Great starter practice NORTHERN CA PERIO: New Listing! 4 Ops, or satellite office. #CA660 Consult Rm, Upgraded Tech with Digital, GREATER FRESNO: 4 Ops, Digital, PPO/DentiLANAP, Paperless. 2019 GR $900K+. Draws Cal, fast-growing area, 22 yrs. Goodwill, Digital. from lg area with little competition. #CA1553 Bldg avail to purchase. #CA676 NORTHERN CA PEDO: Large practice in downtown location, 5,000 sf with 7 equip Ops, 2 MODESTO AREA: Established neighborhood with 60+ yrs Goodwill. 5 Ops, 1,450 sf. 2018 GR add'l plumbed. 2018 GR $3M+. #CA658 $1.1M+ on 3 day/wk. Dental Condo also available OAKLAND: New Listing! 3 Ops, Room to for purchase or lease. #CA635 expand, Digital X-rays, Paperless, 40+ yrs MONTEREY: 4 Op, 1,600 sf in highly desirable Goodwill. 2019 GR $675K with room to grow area with plenty of free parking. 2019 GR $938K Specialties. Prime location, retiring doctor will help with a smooth transition. Seller-owned RE on 32 hrs/wk. #CA650 to purchase or lease. #CA1380 STOCKTON: New Listing! Unique opportunity to REDDING AREA: Modern practice in 1,600 sf buy 1/3 share of a 3 GP, Mostly PPO, Digital, Partner practice. 2019 GR $462K on 32 hrs/wk. with 4 equipped Ops, 1 additional plumbed. Add’l 1/3 ownership of separately listed practice in 2019 GR $558K on 32 hrs/wk. #CA648 REDDING AREA: 6 Ops, Dentrix, Digital, 8 group also available, allowing 2/3 ownership. hyg days/mo. PPO/Cash. Motivated seller, low #CA1624 STOCKTON AREA: 7 Ops, Associate-run, asking price. #CA668 Digital, Paperless, Digital Pano, HMO/PPO, ROCKLIN/LINCOLN AREA: 10 Ops, 6 Paperless.GR $679K. #CA572 equip, 4 plumbed, 2,619 sf. Growth potential in STOCKTON AREA: Great opportunity to all Specialties, 2018 GR $747K on 4 days/wk. purchase practice and bldg, 3,000+ sf, 6 Ops, Good #CA641 hyg recall. 2018 GR $1M+ on avg 37 hrs/wk. #CA616

NORTHERN CALIFORNIA

Northern California Office

1.800.519.3458

Henry Schein Corporate Broker #01230466

SOUTHERN CALIFORNIA BAKERSFIELD: New Listing! 6 Ops, 40 yrs Goodwill, with a great reputation in the area. 6 hyg days/wk. Most specialty work referred. Digital Pano and X-rays. 2019 GR $600K. RE is also for sale. #CA1274 BAKERSFIELD: New Listing! 7 Ops, Hi-end, CEREC, Digital X-rays, Cone beam, Implant motor. 7 hyg days/wk. Room to grow. GR $1M+ w/ low OH. Bldg for sale at $650K. #CA1120 BAKERSFIELD: Well-established, 5 Ops, 4 Equip. In-house dental lab. Condo also for sale. 2019 GR $363K on 3 days/wk. #CA674 BAKERSFIELD PEDO: Rare opportunity to purchase a successful 30+ yr old Pedo practice with Ortho and Oral Surgery services. Over 4K active patients, avg. 40 NP/mo. $2.5M+ GR for past 3 yrs. #CA599 COASTAL ORANGE COUNTY: 3 Ops, Steps from beach, CEREC, Digital, CBCT, Microscope. Priced to sell. 2019 GR $169K. #CA683 COVINA: 4 Ops, 67 yrs in location, 22 w/ seller. Strong hyg prog, room to grow w/ Specialties. 2019 GR $804K. #CA692 EL CENTRO: Great location with low rent. 4 Ops, 3 Equipped, Digital, 25 Yrs Goodwill.2019 GR $850K. #CA680 HUNTINGTON BEACH: 5 Ops, desirable location, Digital, Strong hygiene program. 2019 GR $604K. #CA685 HUNTINGTON BEACH: 4 Ops, located in a busy retail center with great visibility. Practice utilizes Digital X-rays and Easy Dental PMS. 2019 GR $466K. #CA673 INLAND EMPIRE: 2 Dental Offices next to each other, One GP, One Ortho/Pedo. Digital, 13 Ops total. GR $850K. #CA681 INLAND EMPIRE: 4 Ops, Across from busy hospital. Digital, Real Estate also for sale. 2019 GR $432K. #CA682 LONG BEACH: Family practice est. in 1950. 3 Ops, Digital, Strong hyg program. Great area. 2019 GR $651K. #CA671 LOS ALAMITOS: Beautiful state-of-the-art practice with 4 Ops, and mostly associate-run. Digital, cash and PPO in a great location. GR $900K w/ $390K Adj. Net. #CA662 LOS ANGELES: Price Reduced! West Side, 5 Ops, 4 Equip, EagleSoft, Digital, 40 yrs Goodwill, 2019 GR $610K. #CA640 NORTH ORANGE COUNTY PEDO: New Listing! 2 quiet rooms, 2 open bay chairs. Room to expand in affluent loc. Digital, Paperless, welltrained staff. Many referrals. 2019 GR $557K w/ high profit margin. 18 yrs Goodwill. #CA1351 NORTH ORANGE COUNTY: 5 Ops, open since 1965. Dentrix, digital Pano. Retiring seller will assist w/ smooth transition. One-story prof. bldg. 2018 GR $231K. Room to grow. Most Specialty procedures referred out. #CA558 ORANGE COUNTY: 5 Ops, Beautiful office, Digital, Paperless, hi-traffic area with great signage and low-rent. 2019 GR $501K. #CA670 ORANGE COUNTY: New Listing! 5 Ops, Digital, Retiring seller. Excellent reputation in affluent area for high quality care. Modern, welcoming office with strong hyg prog. Room to grow with Specialties. #CA1676 OXNARD: New Listing! 4 Ops, Digital X-rays, originally established over 35 yrs ago. Seller has owned it for 3 yrs and has a primary office in LA and wants to sell. 2019 GR $662K. #CA1164 PALM SPRINGS AREA MULTISPECIALTY: Priced to sell @ $775K! 5 Ops, lecture room, 28 yrs Goodwill. Hi-end, mostly cash patient base. Dentrix, Digital, CT Scan & Gemini Dual Wave Laser. History of $1.2M+/yr on 4 days/wk. #CA604

www.henryscheinppt.com

SAN FERNANDO VALLEY: 10 Ops, 8 Equip, hi-tech, fantastic location. Digital, Pano, CT Scan. GR $1.1M+. #CA664 SAN GABRIEL VALLEY: 4 Ops, Digital X-rays, 65 yrs Goodwill. Most specialty work referred out, most PPO plans are accepted. Busy road with great visibility, open 4 days/wk. Nicely appointed; excellent opportunity. #CA596 SHERMAN OAKS: 5 Ops, 4 Equip, 44 yrs Goodwill. Nicely appointed, hi-end bldg. Strong hyg prog, room to grow, Specialty referred out. Legacy practice. 2019 GR $940K. #CA688 SIMI VALLEY: 6 Ops, 5 Equip, Great location, low rent, 45 yrs goodwill. 2018 GR $297K w/ $89K Adj. Net. #CA637 SOUTH BAY LOS ANGELES: New Listing! Ready to retire! 7 Ops, RE for sale. 50% DentiCal, some HMO/PPO. 2019 GR $568K. #CA1050 SOUTH ORANGE COUNTY PERIO: 4 Ops, 3 Equip, Coastal Community, Modern, Busy strip center location near hi-end residential. 2019 GR $845K. #CA643 SO CAL DESERT AREA: 4 Ops 27 yrs Goodwill. Strong hyg prog w/ hi-end patient base. 2019 GR $809K. #CA691 WEST COVINA: State-of-the-art practice with 3 Ops and is all digital and modern with 1 day of Hygiene/wk. 2019 GR $1.2M+ with Adj. Net of $420K in a great location with low rent. #CA661

SAN DIEGO EAST COUNTY: New Listing! Established practice in a convenient location with 3 Ops, 2 Equipped and Digital X-Rays. Retiring seller refers out most specialty work, opportunity for growth. 2019 GR $309K. #CA1236 ENCINITAS: 4 Ops. Busy retail center. Remodeled 5 yrs. ago with new equipment. Dentrix, Digital, Pano, and Laser. 4 hyg days/wk. 2018 GR $813K. #CA574 LA JOLLA: UTC Area, Leasehold with patients. 7 Ops Digital in retail center with strong anchors. Priced to sell! #CA663 NORTH COUNTY: 5 Ops, 46 yrs. Goodwill, Dentrix, Digital, E4D, strong hyg program, most specialty referred. 2019 GR $1.1M+. #CA689 POWAY: New Listing! 4 Ops, priced for quick sale! Desirable strip mall location. Digital, clean and modern. GR $264K. #CA1111 SAN DIEGO: New Listing! Rare opportunity in prime location. Solid practice with 17 yrs Goodwill. 5 hyg days/wk. 6 Ops, 5 Equip, digital X-rays, Pano. Most specialty work referred out. 2019 GR $1.1M+. #CA1448 SAN DIEGO: 7 Ops, 5 Equipped, located in a large retail center. EagleSoft, PPO/Cash, 3 year average collections of $509K. #CA687

OUT OF CALIFORNIA HONOLULU, HAWAII: New Listing! Highly desirable area, 40 yrs Goodwill, 3 Ops. Digital XRays, DigiDoc, Planmeca E4D, Laser, Densys Operating System. Seller is retiring. #HI1112 CENTRAL COAST, OREGON: Mins to ocean. 3 Dr. days/wk, 2 hyg days/wk. 2019 GR $404K, positioned for growth, Doctor is retiring. #OR112 HILLSBORO, OR: New Listing! 5 Ops, Scan-X, Pano, Laser, and recent cosmetic upgrade. Great NP flow with 7 hyg days/wk. and 4 Doctor days. Near key employers, on a major thoroughfare. Room to expand. GR $1.1M+. #OR1355 SOUTHWEST PORTLAND: 7 Ops, 6 Equip, Dentrix, Digital, Pano. Well-maintained leased space. 2019 GR $598K. #OR115 BURIEN AREA, WA: 3 Ops, Busy Area w/foot traffic. Very low overhead and good cash flow. Could relocate in Bldg to bigger suite. #WA102

Southern California Office

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literature review

Teledentistry 101: A Primer for Dental Professionals for the New Normal Parvati Iyer, DDS; Shuba Anantha, DDS; Amy Griffith, DDS; and Casey Farrand, BS

a b s t r a c t As dental practices prepare to reopen after the COVID-19 pandemic,

dentists have to overcome myriad challenges including low patient volume, shortage of PPE and additional operational expenses on top of lost revenue during the pandemic. Teledentistry could be a viable option to connect with patients and to triage before scheduling emergency appointments. This article provides essential tips to launch teledentistry in your office for the new normal and for the foreseeable future.

AUTHORS Parvati Iyer, DDS, is an assistant professor in the department of diagnostic sciences and the course director for integrated clinical sciences I at the University of the Pacific, Arthur A. Dugoni School of Dentistry. She is a graduate of the University of Michigan School of Dentistry. Conflict of Interest Disclosure: None reported. Shuba Anantha, DDS, is a part-time instructor in the department of preventive and restorative dentistry at the University of the Pacific, Arthur A. Dugoni School of Dentistry and works as a part-time associate. She graduated from the University of Illinois at Chicago’s international dentist program. Conflict of Interest Disclosure: None reported.

Amy Griffith, DDS, practices full time in Sunnyvale, Calif. She earned a degree in psychology from the University of California, San Diego and a Doctor of Dental Surgery from Creighton University School of Dentistry in Omaha. Conflict of Interest Disclosure: None reported. Casey Farrand, BS, graduated summa cum laude from Arizona State University with a bachelor’s degree in health science. She is a consultant for dental practices. Conflict of Interest Disclosure: Ms. Farrand is a freelance practice consultant for dental practices.

eledentistry is not new to the industry. In 1994, the Department of Defense1 launched Total Dental Access (TDA) with the sole purpose of increasing access to care, continuing education and providing effective communication between dentists and specialists. Prior to the COVID-19 pandemic, teledentistry was used as a cost-effective measure2 to improve oral health in nontraditional settings, nursing homes, schools in rural areas and in federally qualified health centers (FQHCs). Now more than ever, the COVID-19 pandemic has brought to light this underutilized option in dentistry. The Oral Disease Burden and Prevention Report (2017)3 for California cites a severe shortage of dental workforce in rural areas as an important factor in contributing to oral health disparities. About 59 million people living in these “health professional shortage areas”4 have no access to oral health care. The

COVID-19 pandemic may be the muchneeded catalyst for change. Patient flow has been disrupted and altered, and this might be the perfect opportunity for urban dentists to extend care to these underserved populations by using teledentistry. This type of delivery of care has been tested in public health settings and has proved to be effective in reducing oral disease5 in high-risk populations. Marko Vujicic, PhD, from the American Dental Association’s Health Policy Institute, hypothesized that based on preliminary data gathered from dental practices that reopened the first week of May, lack of PPE and perception of risk of transmission were the two important factors6 that impacted the dental economics of the COVID-19 pandemic. Previously, a patient would be seen for a face-to-face consultation to discuss a concern before scheduling treatment. Now, with PPE constraints and other limitations, it is possible to optimize OC TOBER 2 0 2 0 547

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TABLE 1

Teledentistry for Solo Practices Patient

scheduling because these initial consults could be triaged and handled remotely with the same personalization, care and payment parity from insurances. There has been research from the Center for Infectious Disease Research and Policy about the resurgence of COVID-19 infection7 over the next 18–24 months. So, while some dental professionals may view teledentistry as a temporary solution for a temporary problem, it could easily, effectively and favorably be incorporated into the new normal. Dental practice staff could further utilize these teledentistry platforms for a more personalized remote appointment check-in than just a text or phone call, with utilization of virtual waiting rooms. Overall, teledentistry would increase patient satisfaction8 and strengthen the connection to the practice by giving above-and-beyond service, while the practice gets loyalty and referrals. While innovative, teledentistry could foster a collegial relationship with patients and deliver a personal touch similar to house calls from a physician. A virtual visit for a child in pain could be perceived as an invaluable service in the eyes of the parent. Other advantages for patients using teledentistry services would be immediate access to dental professionals for consultations, reduced anxiety, reduced travel costs, timely referrals to specialists, mobile applications to monitor and relay relevant health data and possibly reduced visits to the hospital emergency department for dental issues.9

Teledentistry Basics

Teledentistry is the use of technology and communications in the field of dentistry to provide services including screening, consultations, 548 OC TOBER

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• Patient has a need (pain, consult, questions, etc.)

Office staff

Dentist

• Office staff receives email notification and coordinates appointment

• Patient reaches out via contact form on website

referrals and patient education. Teledentistry uses four different modalities10 to deliver care and educate patients.

Synchronous or Real Time

Synchronous or real-time audiovisual conferencing is a two-way communication between the health care provider and the patient using telecommunications technology. For example, solo practices could start with slight modifications to their existing infrastructure by using affordable, HIPAA-compliant software and applications such as MS Teams,11 Skype12 for business, VSee,13 Zoom for health care,14 Doxy.me,15 Google G Suite16 and WebEx.17 Patients could contact the office via the website or a phone call and schedule a teledentistry appointment with the dentist or a trained staff member. The patient would have access to paperwork on the website or a patient portal and would complete it prior to the appointment. During the teledentistry appointment, the dentist would ask relevant questions and also guide the patient to retract their lip or cheek to show the tooth/lesion in question. The dentist would then virtually evaluate the problem and make a referral to a specialist if needed.

Asynchronous or Store and Forward The asynchronous or store-andforward method uses another telehealth provider to capture patient information such as photos,

• Dentist joins virtual waiting room at appointment time • Discussion is problem-focused, evaluation via audio/video and storeand-forward photos/records • Outcome: Recommendation, book an in-person appointment, referral, prescribe

radiographs, etc., that are then forwarded to the dentist. The dentist would access the diagnostic records at a later time and make appropriate treatment recommendations to the allied dental personnel. In California, registered dental hygienists in alternative practice (RDHAP), registered dental hygienists (RDH) and registered dental assistants in extended function (RDAEF) are permitted to acquire diagnostic information such as charting, intraoral images, radiographs, etc., and upload it to a cloud software for dentist review at a later time. This type of asynchronous teledentistry is commonly used by large group practices and in public health settings to provide care to populations who may otherwise not have access to care. Teledentistry companies like TeleDent,18 PBHS,19 Dentulu,20 Teledentix,21 OperaDDS22 and RevenueWell23 offer comprehensive packages including a dashboard, encrypted chat, video-/audioconferencing, scheduling, payment, etc., that consolidate multiple components of this process. When the allied dental team stores and forwards the diagnostic records, it is called the store-andforward method. Mobile vans offering preventive services to schoolchildren do not have axiUm software available. If the patient information needs to be transferred to the dental school for continuity of care, additional technological applications and support are required.

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TABLE 2

Teledentistry Workflow for Group Practice: Key Consideration for Multi-Office Practices

Remote Patient Monitoring

Remote patient monitoring (RPM) is a modality where the patient’s dental and medical data are collected from a telehealth provider in one location and transmitted to a provider in another location for treatment and guidance of care. With the oral systemic connection, elderly patients in long-term care facilities could benefit from this modality and prevent health complications during and after this pandemic. Compliance with sleep apnea appliances and blood glucose monitoring are examples where this modality could aid in the management of chronic diseases and help with timely interventions. This modality of telehealth could expand health services to rural areas and improve health outcomes for patients.

Mobile Health (mHealth)

Mobile health (mHealth) involves cellphones and other hand-held devices that monitor health statistics of patients and relay information to health care providers. Several applications for mobile devices are available to download to help motivate patients to improve their oral health and connect with a dentist when they have a question regarding an issue.

Decisions on Teledentistry

The first step is to decide which level of teledentistry service to implement in a practice based on the dentist’s beliefs, practice philosophy, budget and demand in their community. Once that decision is made, the next step is to set up the infrastructure, train the staff and then inform patients and the community that teledentistry is now an available option. The synchronous modality is easily adopted in any solo practice with minimal training of staff

Online scheduling, bill pay and patient intake forms should be available online

Ideally, each patient is triaged to their usual provider; each provider has appointment slots reserved for teledentistry

Patient records should be electronically accessible across offices and providers

Each provider should follow a universal teledentistry encounter notes template for consistent billing and follow-up

and utilizing existing resources. The asynchronous modality is an excellent option for group practices, dental support organizations (DSOs) and public health settings and may require set-up time and additional training.

way to reconnect with inactive patients. Real-time audio-/videoconferencing with the dental lab for such patients would improve communication and accuracy, thereby minimizing redos25 and increasing patient satisfaction.

Teledentistry for Solo Practices

Teledentistry for Group Practices

The American Dental Association Health Policy Institute’s recent report showed that solo practitioners were slower to bounce back24 from the COVID-19 restrictions to patient care compared to group practices. Teledentistry could be a big booster for patient flow in a solo practice. Teledentistry could be useful to screen and triage existing patients before giving them an appointment for treatment (TABLE 1 ). With the shortage of PPE and staff members, it may be the best way to streamline patient care in the post COVID-19 pandemic era. It could help retain existing patients, acquire new patients and reach across geographical barriers to provide care. Hygiene hours could be extended with teledentistry consultations to increase patient volume. In California, dentists are allowed to supervise up to five hygienists at a time in satellite offices. By increasing hygiene to after-hours and by doing real-time or asynchronous dental examinations, more patients could be seen for recall care. This would also reduce dental emergencies from developing while patients are waiting to be seen. Teledentistry could be utilized after-hours to do treatment plan presentations to patients with complex restorative needs. This would be a great

Teledentistry in group practices would facilitate better communication by coordinating care between general dentists, specialists, hygienists and support staff within group practices. Directors of larger dental practices could calibrate their associates and staff in satellite offices using teledentistry (TABLE 2). RDHAPs could provide care for patients after-hours in long-term care facilities and virtual dental homes26 and coordinate care with a licensed dentist synchronously or asynchronously. Research shows that asynchronous teledentistry modality is equivalent to screening done face to face27 in schoolbased programs, long-term care facilities and community outreach programs. DSOs could use this technology as a marketing strategy to attract patients who prefer the efficiency of quick referrals, shorter in-person visits and better collaboration with other nondental members. Teledentistry could also be used for training, continuing education and remote mentoring of younger associates in the organization.

Teledentistry for Dental Schools

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patients. This would preserve the personal touch patients expect and teach students how to communicate and develop decision-making skills. Teledentistry could expand the students’ abilities and prepare them for the future of dentistry. It could streamline patient care in the emergency department, minimize wait times, increase patient satisfaction and allow more patients to be treated for actual procedures. Teledentistry services have been in place at FQHCs and rural health clinics in California to successfully connect oral health care providers with patients who might otherwise not have access to care. More dental schools could form alliances with FQHCs to provide the communitydentistry experience to students and remove existing disparities in oral health.28

Teledentistry for Independent Contractors

An emerging trend29 is teledentistry services offered by third-party organizations that have adopted the “Uber” business model. Dentists could operate as independent contractors and offer teledentistry services (both synchronous and asynchronous) through these platforms to mitigate the backlog of dental patients with urgent and nonurgent needs due to the pandemic. This would be a great service in urban and rural communities and would prevent unnecessary commutes to a dental office. The dentists could sign up, logon to the website and offer their teledentistry services to patients at their convenience; the company would take care of the rest of the process including referrals to licensed dentists for in-person treatment.

Current Health Policies in Teledentistry

On Jan. 31, 2020, the Department of Health and Human Services declared a state of emergency from the COVID-19 pandemic. As a result, the Office of Civil 550 OC TOBER

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Rights waived the violations against the HIPAA Security Rule for health care providers who were acting in good faith using non-HIPAA-compliant platforms.30 For example, a health care provider would not get penalized for using a platform that is not HIPAA compliant, such as Apple FaceTime, to perform a teledentistry consultation during the COVID-19 pandemic. These modifications were applicable only for synchronous and store-and-forward modalities in teledentistry and would not expire unless otherwise notified.

Teledentistry could also be used for training, continuing education and remote mentoring of younger associates in the organization.

Medicare and Medicaid services have relaxed their restrictions on reimbursement for telehealth services. This would allow members to get telehealth services from their home (origin site) and not have to travel to health care facilities to see providers enrolled in the Medicaid program. The Drug Enforcement Administration has a regulation for prescribing controlled substances II-V, which mandates that the dental professional should evaluate a patient’s emergency in person before prescribing such medications. During the COVID-19 pandemic, this regulation, the Ryan Haight Pharmacy Consumer Protection Act of 2008,31 was modified to accept two-way videoconferencing between the health care provider and the patient before prescribing

medications. This change in the policy allowed dentists to serve more patients with dental emergencies.

Billing/Coding and Documentation for Reimbursement in Teledentistry

The ADA has specific guidelines32 for teledentistry: The dental professional and the allied dental personnel offering teledentistry services must be licensed in the state where the patient receives services. The patient must be actively involved in all decisions regarding treatment and all services must be in alignment with evidencebased practice and in compliance with the privacy laws of the patient. All teledentistry services are required by law to be documented accurately by the dental professional or the allied dental personnel in the electronic health record (EHR). The documentation must also be readily available to the patient on request and also to any entity that is the dental home of the patient. In a 2016 report on case studies of teledentistry33 programs in five states across the nation, participants reported that in spite of many advantages as an innovative model, dentists were slow to engage in teledentistry practices due to the regulations and lack of parity in reimbursement. With the new direction the state policies have taken nationally and in California, it may be the best time to revisit this as a tool to extend across geographical barriers and serve those in need. The two codes used nationally in teledentistry are: ■ D 9995: synchronous or real-time encounter with procedure codes D0190, D0140, D0170 and D0171. ■ D 9996: asynchronous or store-and-forward encounter with procedure codes D0190, D0140, D0170 and D0171.34

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TABLE 3

Documentation for Synchronous Teledentistry Modality Originating site: patient’s home address

Teledentistry CDT codes D9995 and D9996 are used in addition to the other CDT procedure codes (D0190: screening, D0140: limited oral evaluation/problem focused, D0170: reevaluation — limited, problem focused and D0171: reevaluation — postoperative visit) for billing. TABLES 3 and 4 are sample templates for a synchronous and an asynchronous teledentistry modality. TABLE 3 shows what a solo dentist would do to document a synchronous or a real-time consultation of an existing patient. TABLE 4 shows how documentation is done in a large group practice where the initial person triaging the patient acquires and stores the patient data in a cloud storage and forwards it to a specialist. Alternatively, this could be uploaded directly into the EHR and be available electronically for all providers. In the sample for synchronous teledentistry service ( TABLE 3 ), the dentist evaluated the patient, prescribed medications and referred to an endodontist. Note that the follow-up care is indicated after endodontic therapy. In the sample template for asynchronous teledentistry modality used in group practices ( TABLE 4 ), the first provider acquired patient information and stored it in a cloud storage or an EHR. The second provider, a periodontist, reviewed that information at a later time and scheduled the patient for crown lengthening. A follow-up appointment with the usual provider (general dentist) was noted for continuity of care.

Current Teledentistry Policies in California

The California Emergency Services Act35 gave the governor the power to declare a state of emergency and make some important executive orders. This law will be in effect until the emergency is terminated.

Patient presenter: patient/guardian/parent/caregiver Distant site: provider’s address (home or practice) Provider: your name with documentation Modality used: synchronous or asynchronous (store-and-forward) Platform used: _______________, business ________________ Information gathered: COVID-19 screening questions; chief concern; subjective, objective, assessment; plan (SOAP) note Rx given: ________________ Referrals: endodontist Dr. ________________ @ telephone number; website Next visit: schedule appointment for _______________________

Gov. Gavin Newsom’s executive order waived waiting periods between refills of prescription medication and allowed for more refills into a larger prescription. This order also permitted brand-name drugs to be prescribed when generic was not available and waived home delivery charges and preauthorizations. Insurance companies could waive or expedite the credentialing process for telehealth providers. Gov. Newsom also relaxed various telehealth rules and laws pertaining to the relay of patient information including unauthorized access and disclosure of patient data. Consent requirements (oral or written) were also suspended for telehealth services for the duration of the emergency. Liability originating from such violations were suspended and disciplinary action for unprofessional conduct relaxed for telehealth providers. As of now, most third-party payers in California will only reimburse the (diagnostic) procedure code and not pay for the teledentistry code separately. Documentation of the teledentistry code is still required on the paper or electronic claim when filing for reimbursement. Assembly Bill 744,36 which was passed in October 2019 (effective January 2021), requires that telehealth services covered under a health plan be subjected to the same rules as

those services for an in-person visit. This means that all teledentistry services will have “payment parity” or will be reimbursed at the same rate as in-person visits. This bill applies to all health policies that will be issued, amended or renewed on or after Jan. 1, 2021. Though health plans for managed care had payment parity for teledentistry services before the pandemic, this new bill now requires all commercial payers to adopt payment parity as well. Medi-Cal Dental37 provides coverage for both synchronous and asynchronous or store-and-forward teledentistry modalities. For the synchronous modality, it is important to include the number of minutes spent in transmission and a procedure code along with the teledentistry CDT code. Reimbursement is allowed separately for the D9995 code with a limit of 90 minutes per member, per provider, per day for this service. For the asynchronous modality, only the diagnostic procedure code is reimbursed even though both codes are required to be documented.

Challenges and Barriers to Teledentistry

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TABLE 4

Documentation for Asynchronous Teledentistry (Store-and-Forward) Modality Originating site: patient’s home address Patient presenter: patient/guardian/parent/caregiver Distant site: provider’s address (home or practice) Provider: dentist/RDHAP/RDH/RDAEF Location/ date: branch ________________ Modality used: asynchronous or store-and-forward Platform used: _______________, business ________________ Storage: cloud storage of patient data in _____________________ platform Information gathered: COVID-19 screening questions, medical history, full-mouth radiograph/panoramic radiograph, intraoral images, periodontal charting Care coordination: refer to periodontist ________________ in branch ___________________ for evaluation of tooth No. ______ Clinical notes: chief concern; subjective, objective, assessment, plan note (SOAP) Periodontist __________________/date: reviewed patient information in cloud storage Plan: schedule for crown lengthening on tooth No. _____ Follow-up: refer patient back to usual provider for final restoration on tooth No. ______

implement teledentistry and may require a professional dental consultant to aid in set up, maintenance and training. Cybersecurity is an unwanted side effect of any new technology and could potentially cripple a practice. Dental professionals need to be flexible and quick to adapt and create a customizable workflow and train their staff to benefit from this mode of delivery. Resistance to change from staff members, lack of understanding of online presence, the power of social media and inadequate follow-up with virtual visits could result in unhappy patients and negative reviews and damage the reputation of the practice. Another challenge is that patients could now expect answers right away, not placing value on the necessary diagnostics needed to arrive at the proper diagnosis. Further research is needed to make the plunge because there is not sufficient evidence on the long-term utilization of teledentistry.39

Conclusion

The American Dental Association Health Policy Institute’s recent report on dental spending predicts a 38% reduction40 this year and a possible 20% reduction next year. It makes sense to 552 OC TOBER

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capitalize on other emerging platforms to retain patients, acquire new patients and be part of the solution in overcoming health disparities in the community. The surgeon general’s report scheduled to be released this fall is expected to give direction on emerging technologies that could change the outcome of oral health. Because teledentistry has the potential to evolve with new policies and with states expanding on the range of coverage through this service, it might become a part of mainstream dental practice. Teledentistry may very well be the crucial step that closes the gap between medicine and dentistry.

Testimonial From Amy Griffith, DDS

“Teledentistry has helped me tremendously to connect with my patients, comfort them, give them a sense of control over their lives during this pandemic. It has helped me preserve my stock of PPE, minimize exposure and risk of transmission of COVID-19. Patients have thanked me for their teledentistry consultation and commented that it was very simple and easy to use and they would do it again.” n

REFERENCES 1. Rocca MA, Kudryk VL, Pajak JC, Morris T. The evolution of a teledentistry system within the Department of Defense. Proc AMIA Symp 1999;921–924. PMCID: PMC2232632. 2. Irving M, Stewart R, Spallek H, Blinkhorn A. Using teledentistry in clinical practice as an enabler to improve access to clinical care: A qualitative systematic review. J Telemed Telecare 2018 Apr;24(3):129–146. doi: 10.1177/1357633X16686776. 3. California Department of Public Health. Oral Disease Burden Report (April 2017). 4. Health Resources and Services Administration. Health Professionals Shortage Areas. data.hrsa.gov/topics/healthworkforce/shortage-areas. 5. Khan SA, Omar H. Teledentistry in practice: Literature review. Telemed J E Health 2013 Jul;19(7):565–7. doi: 10.1089/tmj.2012.0200. 6. American Dental Association Health Policy Institute. Report on COVID-19 economic impact on dental practices — Week of May 4 results. 7. Moore KA, Lipsitch M, Barry JM, Osterholm MT. The CIDRAP Viewpoint part 1: The future of the COVID-19 pandemic: Lessons learned from pandemic influenza. The CIDRAP Viewpoint April 30, 2020. 8. Böhm da Costa C, Peralta F, Ferreira de Mello A. How has teledentistry been applied in public dental health services? An integrative review. Telemed J E Health 2020 Jul;26(7):945–954. doi: 10.1089/tmj.2019.0122. Epub 2019 Oct 1. 9. Sun BC, Chi DL, Schwarz E, et al. Emergency Department Visits for Nontraumatic Dental Problems: A Mixed-Methods Study. Am J Public Health 2015 May;105(5):947–55. doi: 10.2105/AJPH.2014.302398. Epub 2015 Mar 19. 10. American Teledentistry Association. Teledental practice and teledental encounters: An American Association of Teledentistry position paper. www. americanteledentistry.org/wp-content/uploads/2018/10/ ATDA_TeledentalPracticePositionPaper.pdf. 11. Microsoft Teams. www.microsoft.com/en-us. 12. Skype. skype.com/en. 13. Vsee. vsee.com. 14. Zoom. zoom.us. 15. Doxy.me. doxy.me/en. 16. G Suite. gsuite.google.com. 17. Cisco WebEx. webex.com. 18. TeleDent software. mouthwatch.com/teledent-software. 19. PBHS. pbhs.com. 20. Dentulu. dentulu.com. 21. Teledentix. teledentix.com. 22. OperaDDS. operadds.com. 23. RevenueWell. revenuewell.com. 24. American Dental Association Health Policy Institute. COVID-19 Economic Impact on Dental Practices. 25. Herman B. Teledentistry, private practice dentistry and the virtual workflow. Dentistry Today June 18, 2018. 26. Glassman P, Harrington M, Namakian M, Subar P. The virtual dental home: Bringing oral health to vulnerable and underserved populations. J Calif Dent Assoc 2012 Jul;40(7):569–77. 27. Alabdullah JH, Daniel SJ. A systematic review on the validity of teledentistry. Telemed J E Health 2018 Aug;24(8):639–648. doi: 10.1089/tmj.2017.0132.

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Epub 2018 Jan 5. 28. Isringhausen KT, VanderWielen LM, Vanderbilt AA. Addressing health care disparities and access to dental care while improving education: Schools of dentistry and federally qualified health centers. J Health Care Poor Underserved 2014 May;25(2):670–4. doi: 10.1353/ hpu.2014.0108. 29. The TeleDentists. www.theteledentists.com/dentists.html. 30. U.S. Department of Health and Human Services. Telehealth Discretion During COVID-19 pandemic. www. hhs.gov/hipaa/for-professionals/special-topics/emergencypreparedness/notification-enforcement-discretiontelehealth/index.html. 31. U.S. Department of Justice Drug Enforcement Administration. COVID-19 information page. www. deadiversion.usdoj.gov/coronavirus.html. 32. American Dental Association. ADA Policy Teledentistry. www.ada.org/en/about-the-ada/ada-positions-policiesand-statements/statement-on-teledentistry.

33. Oral Health Workforce Research Center. Case Studies of 6 Teledentistry Programs: Strategies To Increase Access to General and Specialty Services. 34. American Dental Association. COVID-19 Coding and Billing Interim Guidance. 35. California Legislative Information. Chapter 7. California Emergency Services Act. leginfo.legislature.ca.gov/faces/ codes_displayexpandedbranch.xhtml?tocCode=GOV&divis ion=1.&title=2.&part=&chapter=7.&article. 36. Dizon R. With a stroke of a pen, Gov. Newsom continues California’s telehealth policy leadership role. Oct. 15, 2019. www.telehealthresourcecenter.org/with-a-strokeof-a-pen-gov-newsom-continues-californias-telehealth-policyleadership-role. 37. Department of Health Care Services/Medi-Cal Dental. Teledentistry resources. dental.dhcs.ca.gov/Dental_ Providers/Denti-Cal/Teledentistry_Resources. 38. Golder DT, Brennan KA. Practicing dentistry in the age of telemedicine. J Am Dent Assoc 2000 Jun;131(6):734–

44. doi: 10.14219/jada.archive.2000.0272. 39. Estai M, Kanagasingam Y, Tennant M, Bunt S. A systematic review of the research evidence for the benefits of teledentistry. J Telemed Telecare 2018 Apr;24(3):147– 156. doi: 10.1177/1357633X16689433. 40. American Dental Association/Health Policy Institute. Report on dental spending. www.ada.org/~/media/ADA/ Science%20and%20Research/HPI/Files/HPIBrief_0620_1. pdf?la=en. Accessed Aug. 7, 2020. THE CORRESPONDING AUTHOR, Parvati Iyer, DDS, can be reached at piyer@pacific.edu.

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• Lee Skarin and Associates has been serving the dental profession since 1959. • Kurt Skarin has over 30 years experience in dental practice sales. • We have sold more practices than any broker in the state within • • • •

the last 12 months. Our experienced practice appraisals are backed with credentials unequaled among dental practice brokers. We provide in-house legal counsel to advise you in all aspects of the sale and purchase, including the tax consequences of the sale. Excellent financing is available, in most cases for 100% of the purchase price. With a reputation for experienced, conscientious, and ethical performance, we give our clients personal attention in all aspects of the purchase.

With scores of Buyers, profiles of their practice interests and financial ability, Lee Skarin & Associates is able to find the right buyer for your practice.

LEE SKARIN & ASSOCIATES INC.

EXPERIENCE THE DIFFERENCE

Offices:

Experience the difference. Call Lee Skarin and Associates for responses to all of your questions - No obligation! Visit our website for current listings: www.LeeSkarinandAssociates.com Dental Practice Brokers CA DRE #00863149

805.777.7707 818.991.6552 800.752.7461

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Back to Practice Resources The following resources have been extracted from the frequently updated Back to Practice section on cda.org. They are provided here for readers’ reference. For full and free access to up-to-date materials, visit cda. org/Home/Practice/Back-to-Practice. The resources on these pages were accessed Aug. 28, 2020.

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BACK TO PRACTICE

California Dental Association

PAT I E N T C A R E

1201 K Street, Sacramento, CA 95814 800.232.7645 | cda.org

Patient Screening and Risk Management Workflow RISK ASSESMENT Use Patient Screening Form when patient contacts the office.

HIGH RISK

• COVID + • Symptomatic • Risk Factors

EMERGENCY CARE Work with medical care provider to identify appropriate care facility

LOW RISK

TRIAGE

• COVID – • Asymptomatic • No Risk Factors

NON-URGENT CARE Defer Care Defer care until after symptoms have resolved (24 hours since last fever without anti-fever medications, and improved cough or other symptoms) AND at least 10 days (20 days if patient illness was severe) have elapsed since symptom onset.

SCREEN PATIENT AGAIN Proceed with care when symptoms resolve

TREATMENT OPTIONS

PALLIATIVE CARE*

MINIMAL AEROSOL**

AEROSOL***

TREATMENT AREAS

Four zones of clinical infection control

PPE

Appropriate PPE for treatment

≤ TWO DAYS BEFORE APPOINTMENT Screen patient

AT OFFICE Take Temperature: should be <100.4F. Observe for Symptoms. Treat or defer. PATIENT DISCHARGE Advise patient to call if they experience symptoms or are COVID+ within 2 days following visit ROOM TURNOVER Disinfect room * Examples of palliative care: SDF, GI, 5000 ppm F- rinse or varnish, Antibiotics (ADA Guidelines), Pain Meds (ADA Guidelines) ** Examples of minimal aerosol: SDF, GI, Hand Scaling, TB prophy, F - application ***Examples of aerosol: Extractions, Surgery/implants, Perio/Cavitron, Endodontic, Any use of air water syringe

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California Dental Association

P R E PA R I N G YO U R PRACTICE

1201 K Street, Sacramento, CA 95814 800.232.7645 | cda.org

PPE Recommendations for Dental Practices Dental Practice Scenarios

Surgical Mask

N95/ KN95

Face Shield

Eye Protection Gloves & Side Shield

Administrative

Level 1

Pre-Visit Patient Temperature Screening

Level 1

Lab/Instrument Processing +

Level 2

Choose one

No Fluid ^

Level 1

Choose one

Low Fluid ^

Level 2

Choose one

ModerateHeavy Spray/ Aerosol Generating Procedures # Recommended

L3 if N95 unavailable

Optional

Clinical Attire**

Gown

Head Cover

Dedicated Shoes/Covers

Not Recommended

While it is understood that aerosols are produced in various ways, both organically by the patient and through various dental procedures, it is still unknown how exactly the virus is transmitted. Based on current studies and guidelines, these recommendations reflect what levels of adequate PPE will protect patients and dental team members. * During PPE shortage, surgical masks should be prioritized for dental team members providing direct patient care and may be an acceptable alternative in addition to a full-face shield when N95/KN95 or higher masks are not available. The use of a Level 3 mask instead of an N95/KN95 mask may carry a higher risk for transmission due to the lack of a respirator seal, without which limits the mask’s protection primarily to splatter and droplets. ** If consistent with office uniform policy, dental team members should change out of street clothes into clinical attire upon arrival to the office. Although clinical attire is not considered PPE under the dental practice act. Lab coats worn as the outermost garment that provide adequate protection for the employee may be considered PPE. A gown may be a more appropriate choice of protective attire for most dental procedures. = Alternatives to a face shield may include the installation of a sneeze guard or the mandate that patients wear masks in the reception area. If such a policy is implemented, dental practices should consider providing Level 1 masks to patients who arrive without a mask. ^ PPE in these scenarios should be changed between patients when visibly wet or soiled. # PPE, including gowns, should be changed between patients. Follow CDC guidelines for mask extended use, reuse, and decontamination. + For staff performing in-office laundering duties, it is recommended that a Level 1 or 2 surgical mask, face shield or eye protection, gloves, clinical attire, and gown are worn. Follow established protocols for donning and doffing for cleaning patient care areas. Resources NIOSH-Approved N95 Manufacturers Authorized Imported Non-NIOSH Approved Respirator Manufacturers CDC Recommended Guidance for Extended Use and Limited Reuse of N95 Masks CDC Crisis Standards of Care Decontamination Recommendations for Respirators CDC Strategies for Optimizing PPE Supply Copyright © 2020 California Dental Association

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California Dental Association

PAT I E N T C A R E

1201 K Street, Sacramento, CA 95814 800.232.7645 | cda.org

Dental Aerosol Management

Interim Guidance from CDA’s COVID-19 Clinical Care Workgroup Updated May 26, New: Resources for Upper-Room UV and portable HEPA room filtration, per CDC Guidance for Dental Settings, May 19

Introduction As part of its overall charge to assist dental professionals during the COVID-19 pandemic, the California Dental Association COVID-19 Clinical Care Workgroup initiated an in-depth investigation into aerosol management in dentistry. This document reflects that work. It is important to note that the environment is rapidly evolving and we are constantly learning more about the virus, its transmission and how to reduce risk during the provision of dental care. In particular, new products for dental aerosol management are being introduced almost daily and the evidence on the efficacy of these in the dental setting is just beginning to develop. We anticipate evidence on this will continue to emerge well after this resource is published. Therefore, this document should be considered a living document that will be updated over time as information becomes available. What’s more, the California Dental Association is not a regulatory agency, therefore the guidance offered here is not intended to be construed as the “standard of care,” and should be considered along with guidance from local, state, and federal government agencies, local/regional hospital systems and/or other authorities. Background The delivery of dental services routinely involves exposure of dental health personnel and patients to the contents of saliva and blood through droplets, spatter and aerosols produced during patient care. The sources are numerous, including naturally occurring patient actions, such as coughing, and operator-generated through the use of dental equipment, including high-speed and slow-speed rotary, ultrasonic, air-water syringe, air-abrasion and polishing equipment. Infection control and disease transmission prevention in the dental environment is guided by the federal Centers for Disease Control and Prevention1 and Occupational Safety and Health Administration 2 and is effectively managed through the layering of multiple tactics to identify and reduce the risks associated with treatment. These mitigation approaches are hierarchical and focus first on eliminating the risk when possible, then reducing it through administrative and engineering controls and the use of personal protective equipment. They build upon each other as depicted here:

Hierarchy of Controls most effective

Elimination

Remove the biohazard

Engineering

Physical intervention

Administrative 1 2

Standard precautions, Transmission-based precautions Dentistry Workers and Employers

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PPE least effective

Modify behavior

Prevent cross contamination by covering up

*Adapted from CDC’s Hierarchy of Controls

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In dentistry, these are: •

Screening for active disease prior to initiating treatment and implementing Aerosol Transmission Disease Standard Protocols to protect from treating patients known to be contagious for an ATD. (Elimination)

•

Determining patient-specific dental treatment options to minimize disease transmission risk. (Administrative)

•

Managing aerosols produced during treatment using equipment designed specific to that purpose. (Engineering)

•

Adhering to rigorous protocols for equipment sterilization and surface disinfection. (Elimination)

•

Utilizing PPE appropriate to transmission risk, including level of mask and gown protection and locations for donning and doffing. (PPE)

Air and aerosols in dental treatment and office spaces can be conceptualized into the following four zones:

ZONE 1

ZONE 2

Intraoral

3’ radius beyond the oral cavity

ZONE 3

ZONE 4

Operatory

General office

Operatory

General office

Aerosol mitigation and containment strategies are specific to each zone and, most importantly, build upon the other controls and layer upon each other. The more effectively aerosols are managed in Zone 1, the fewer aerosols travel on to Zone 2 and so on through the four zones, collectively reducing the disease transmission risk to patients and dental staff. While risk can never reach zero, dentistry employs a comprehensive approach to risk assessment, mitigation and infection control that demonstrates an excellent track record for the safe provision of care.

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Considerations for Aerosol Management by Zones As noted above, dental health professionals routinely make decisions at each level of patient care based on assessed risk and in consideration of the oral health diagnosis. Generally, the risk associated with low-fluid procedures with primarily naturally generated aerosols is considered to be lower than that of high-fluid procedures with dental equipment-generated aerosols, though the pathogenic load and potential for infectivity for any type of dental aerosol is not known and cannot be accurately assessed. During the COVID-19 pandemic and as dental practices that have been providing only emergency care for the last several weeks prepare to provide additional care, the CDC’s Transmission-Based Precautions and Interim Infection Prevention and Control Guidance for Dental Settings During the COVID-19 Response (dated April 27, 2020) are essential references for additional protections within the dental setting. Present evidence strongly suggests SARS-CoV-2 is likely transmitted through aerosolized infectious material. The science on this continues to emerge as data is collected and analyzed. Early evidence suggests that presymptomatic and asymptomatic individuals may carry and transmit the virus. At this time with the current level of understanding, the most important strategy to diminish the risk of transmission is to screen for active COVID-19 and NOT treat an identified or suspected case. For all other patients one must consider risk mitigation strategies for all presymptomatic or asymptomatic patients who may have COVID-19 and require dental treatment.

The following are options to consider; they are not guidelines.

Zone 1: Options for intraoral aerosol management • Choose treatment techniques that avoid, minimize, or otherwise manage aerosol production when feasible • Maximize chairside HVE evacuation, including use of multiple evacuators if available (Note: Vacuum and line equipment maintenance optimize performance) • In addition to HVE, if applicable: O O

Use additional continuous suction dental isolation systems Use dental dams

• Anticipate, manage, attempt to reduce triggers for gagging and coughing (e.g. intraoral radiography; impressions) O

Consider nitrous oxide to reduce gagging and promote nasal breathing into the scavenger

• Offer a preoperative viricidal rinse or mouth swab (e.g. hydrogen peroxide; povidone-iodine)

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Zone 2: Options for consideration to limit and manage aerosols within three ft of the oral cavity • Decrease contamination of multi-use materials during aerosol-generating treatment by: O O O

Setting out supplies and materials in the amount required for scheduled care Avoiding opening drawers or cabinets to access materials or supplies Utilizing non-treatment personnel to retrieve equipment, materials or supplies from outside treatment area and deliver to treatment personnel

• Reduce transfer of aerosol contamination outside treatment area by covering patient with large bib and hair covering or drape • Remove or cover all exposed items that cannot be cleaned (e.g. glove boxes, computer keyboard) • At this time, there is limited evidence on applicability and efficacy of the following for dental practice. Dentists may wish to evaluate emerging evidence on the value to your specific practice conditions of additional Zone 2 equipment, such as: O O

Free standing or chairside extraoral aerosol evacuation systems Treatment hoods

Zone 3: Options for consideration to limit and manage aerosols in operatory Efficient management in Zones 1 and 2 may significantly reduce additional management requirements in Zones 3 and 4. • Zone 3 aerosol management is primarily accomplished through environmental controls and will differ based on dental office or clinic layout and air flow. Depending on your conditions, you may wish to evaluate the following options: O O

Keep treatment room doors closed during aerosol-generating procedures Create barriers between adjacent operatories and/or between treatment areas and common areas, using materials such as plastic, acrylic or plexiglass for the purpose of reducing lateral spread and providing a surface upon which aerosols collect and can be disinfected

• Evaluate air flow within treatment space and consider options that improve flow if deemed useful and feasible, such as the addition of a room air filtration device or other means to increase the fresh air turnover rate in the operatory. Consider the use of a portable HEPA air filtration unit while the patient is actively undergoing, and immediately following, an aerosol-generating procedure (CDC Guidance for Dental Settings, May 19). O

The use of these units will reduce particle count (including droplets) in the room and will reduce the amount of turnover time, rather than just relying on the building HVAC system capacity. Place HEPA unit within vicinity of patient’s chair, but not behind DHCP. Ensure DHCP are not positioned between the unit and the patient’s mouth. Position the unit to ensure that it does not pull air into or past the breathing zone of the DHCP.

• At this time, there is limited evidence on applicability and efficacy of the following for dental practice. Dentists may wish to evaluate emerging evidence on the value to your specific practice conditions of additional Zone 3 equipment, such as: O

Ultraviolet-C Irradiation, hypochlorous acid (HOCl) or other viricidal foggers for air or surface decontamination

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Zone 4: Options for consideration to limit and manage aerosols in common areas Efficient management in Zones 1, 2 and 3 may significantly reduce additional management requirements in Zones 4. Evaluation of Zone 4 options is best accomplished by evaluating the air flow patterns in your office or clinic space. • Increase fresh air from outside for dilution of aerosols by opening window or increasing fresh air input at HVAC • Consider using fans to direct air flow away from common and administrative areas • Remove unnecessary items from waiting room, such as magazines and children’s toys • Regularly disinfect frequently touched materials and surfaces (e.g. telephone receivers, door handles, tables / other flat surfaces, pens, etc.) • Place posters on cough/sneeze hygiene in waiting areas; give masks to unmasked patients as they arrive • Consider placing cough shields at front desk • Evaluate existing HVAC system, consider enhanced filtration if deemed useful and feasible.

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ADDITIONAL RESOURCES General Aerosol Management Resources •

Aerosols and splatter in dentistry, A brief review of the literature and infection control implications. JADA, Vol. 135, April 2004

•

Transmission routes of 2019-nCoV and controls in dental practice. International Journal of Oral Science (2020) 12:9

•

Aerodynamic analysis of SARS-CoV-2 in two Wuhan hospitals. Nature. April 2020

•

Being a front-line dentist during the Covid19 pandemic: a literature review, Maxillofacial Plastic and Reconstructive Surgery (2020) 42:12

•

Comparative dynamic aerosol efficiencies of three emergent coronaviruses and the unusual persistence of SARS-CoV-2 in aerosol suspensions MedRxiv This version posted April 18, 2020. All rights reserved. No reuse allowed without permission.

Government Regulation for Dentistry •

CDC Interim Infection Prevention and Control Guidance for Dental Settings During the COVID-19 Response

•

CDC Infection Prevention Practices in Dental Settings

•

The California Workplace Guide to Aerosol Transmissible Diseases (CalHOSA 2020)

•

OSHA COVID-19 Dentistry Workers and Employers

Disinfection •

CDC/NIOSH, Basic Upper-Room Ultraviolet Germicidal Irradiation Guidelines for Healthcare Setting (CDC Guidance for Dental Settings, May 19)

•

Ultraviolet Air and Surface Treatment (ASHRAE)

•

Hypochlorous Acid: Harnessing an Innate Response (InfectionControl.tips)

•

Evaluation of Liquid- and Fog-Based Application of Sterilox Hypochlorous Acid Solution for Surface Inactivation of Human Norovirus (American Society for Microbiology)

•

Chemical Disinfectant: CDC Guideline for Disinfection and Sterilization in Healthcare Facilities (2008)

Stand-Alone Evacuation Systems •

Pilot Study: British Dental Journal

•

Personalized Ventilation Systems: ASHRAE Journal

HVAC •

ASHRAE Position Document on Infectious Aerosols, April 2020

•

ASHRAE position document on airborne infectious diseases, February 2020

A variety of regulatory agencies oversee the health of the nation and the supplies and equipment used in health care. If you are considering purchasing new equipment or using new types of materials or supplies, you may want to confirm their authenticity with the appropriate agency or authority. •

National Institute for Occupational Safety and Health (NIOSH) is the division of CDC responsible for worker safety and approves protective equipment.

•

U.S. Food and Drug Administration (FDA) along with CDC, OSHA and NIOSH regulate N95 masks.

•

ASHRAE advances the arts and sciences of heating, ventilation, air conditioning, refrigeration and their allied fields.

•

Environmental Protection Agency (EPA) is responsible to ensure access to clean air, land and water.

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California Dental Association

PAT I E N T C A R E

1201 K Street, Sacramento, CA 95814 800.232.7645 | cda.org

Reporting Symptoms/Positive Test for COVID-19 Regulatory Requirements PATIENT REPORTS SYMPTOMS WITHIN 2 DAYS FOLLOWING VISIT

EMPLOYEE REPORTS EXPOSURE TO SYMPTOMATIC OR COVID-19 POSITIVE INDIVIDUAL ANYWHERE

EMPLOYEE REPORTS SYMPTOMS

RECORD: Date of reporting and date pt last seen • Information provided by pt, including if testing has been done •

NEGATIVE DIAGNOSIS

OBTAIN DETAILS OF EXPOSURE AND ASSESS RISK:

RECORD DATE OF REPORT AND SYMPTOMS

• •

YES

SUSPECTED OR POSITIVE Refer for medical consult if appropriate • Assess employee “close contact” exposure; follow chart at far right

Date of exposure Was there “close contact”?

•

Instruct employee to return home immediately, if not already home, to self-monitor for 14 days, to contact their medical care provider and notify employer of results.

NEGATIVE DIAGNOSIS See below for information on CDC guidance for employees returning to work.

Employee can continue to work and should actively self-monitor for 14 days.

SUSPECTED OR POSITIVE Report to the LHD and follow instructions • Send identified employee home with direction to contact healthcare provider and to inform dental practice of results. •

Glossary of terms: • Close contact – Within 6 feet of an infected or symptomatic person or within operating area; 15 min exposure without wearing PPE that is NIOSH or CDC approved (i.e. not cloth masks). • Screening and symptoms guidance – Employee Screening Form • Contact tracing – Identifying patients and employees in the office in close contact with the infected or symptomatic patient or employee. Advise person to seek medical evaluation. • LHD – local public health department

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Symptoms/Positive Test for COVID-19

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Additional information if you have an employee diagnosed with COVID-19: Employees who are not close contacts of the employee with COVID-19 may remain working as long as they have no symptoms of the virus. Whether the dental practice remains open depends on whether it can continue to operate without the employees who are sent home. Contact your workers comp carrier if employee reports positive diagnosis for COVID -19, and believes they contracted COVID -19 at work. California employers must report to the nearest Cal/OSHA office any serious illness or injury, or death of an employee that occurred at work or in connection with work within eight hours of when they knew or should have known of the illness, injury or death. This includes a COVID-19 illness if it meets the definition of serious illness. “Serious injury or illness” is defined in Title 8 Section 330(h) and includes inpatient hospitalization for a reason other than medical observation or diagnostic testing. Eligible employees who have been advised by their health care provider to self-quarantine related to COVID -19 or are experiencing symptoms and seeking a diagnosis may be eligible for up to two weeks (80 hours, or a part-time two-week equivalent) of emergency paid sick leave under Families First Coronavirus Response Act (FFCRA). Please refer to the required notice provided by the Department of Labor for more detailed information on qualifying reasons for leave. Further, any additional COVID-19 employee policies you may wish to implement in your office should be developed in consultation with an HR professional. Following is the CDC’s guidance on when an employee suspected or having COVID-19 may return to work: Employers should not require sick employee to provide a negative COVID-19 test result or healthcare provider’s note to return to work. Employees with COVID-19 who have stayed home can stop home isolation and return to work when they have met the following criteria: • At least 10 days have passed since symptom onset (except for individuals who had severe illness and who should be isolated for an additional 10 days) • At least 24 hours have passed since resolution of fever without the use of fever-reducing medications, and • Other symptoms have improved Additionally, CDPH provides COVID-19 Workplace Outbreak Employer Guidance that includes notification and reporting requirements.

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California Dental Association

PAT I E N T C A R E

1201 K Street, Sacramento, CA 95814 800.232.7645 | cda.org

Covid -19 Patient Screening Form Instructions for use: Use one form for each patient appointment. Ask the patient these questions at the time appointment is made or with appointment reminder, and again no more than two days before the appointment. Take the patient’s temperature and note any signs of fever, coughing, or shortness of breath. Patient/Parent/Guardian Names: ____________________________________________________________________ Screening questions

Date: xx/xx/xx Date: xx/xx/

Notes

Staff initial:____ Staff initial:____

Do you have a fever or above-normal temperature (>100.0° F)? Take temperature at appointment.

 No  Yes

Are you experiencing shortness of breath or having trouble breathing?

 No  Yes

Do you have a dry cough?

 No  Yes

Do you have a runny nose?

 No  Yes

Have you recently lost or had a reduction in your sense of smell or taste?

 No  Yes

Do you have a sore throat?

 No  Yes

Are you experiencing chills or repeated shaking with chills?

 No  Yes

Do you have unexplained muscle pain?

 No  Yes

Do you have a headache?

 No  Yes

Are you experiencing nausea, vomiting or diarrhea?

 No  Yes

Even if you don’t currently have any of the above symptoms, have you experienced any of these symptoms in the last 14 days?

 No  Yes

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If patient answers “yes” to either question on shortness of breath or coughing, or answers yes to any combination of two other symptoms and the patient does not need emergency care, consider not scheduling or seeing the patient until symptoms resolve or until patient can provide proof they are not infectious for COVID-19. The dentist may want to seek additional information from the patient regarding symptoms.

If “yes” and patient does not need emergency care, do not see patient unless it has been more than 10 days since symptoms first appeared and 24 hours of no fever without use of fever-reducing medication. CDC issued guidance on July 27th

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Screening questions

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Date: xx/xx/xx Date: xx/xx/

Notes

Staff initial:____ Staff initial:____

Have you been in unprotected contact with someone who has tested positive for COVID-19 in the last 14 days? “Unprotected contact” means without the use of personal protective equipment.

 No

 Yes

Have you been tested for COVID-19 in the last 14 days? If “no,” proceed to next question.

 No

 Yes

If yes, what is the result of the testing?

 No

If negative, proceed to next question.

 Unsure

If still waiting on results, schedule appointment after results are known.

 Positive

 No

 Yes

Have you traveled more than 100 miles from your home in the last 14 days?

If yes, ask for date of last contact with COVID-positive patient and set appointment time for more than 14 days later, unless the patient needs emergency care.

If positive, determine if patient needs emergency care. If not an emergency, schedule patient to be seen when it has been more than 10 days (20 days if patient illness was severe) since symptoms first appeared and 24 hours of no fever without use of fever reducing medication. If yes, determine if patient traveled to an area where COVID-19 cases are high. Determine if patient followed physical distancing precautions and wore a mask while in public.Use professional judgement when determining whether to proceed with the appointment.

Patient signature required at appointment: I agree to notify the dental practice if within 2 days I become ill with COVID-19 symptoms or test positive for COVID-19. I understand the dental practice has a legal and ethical obligation to inform me if a staff person I had close contact with tested positive for COVID-19 within 2 days. Acepto dar aviso a la clínica dental si dentro de dos días presento síntomas de COVID-19 o tengo un resultado positivo de COVID-19. Entiendo que la clínica dental tiene la obligación legal y ética de informarme si un miembro del personal con el que tuve contacto ha tenido un resultado positivo de COVID-19 dentro de dos días. Signature ______________________________________________________________________________

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PAT I E N T C A R E

1201 K Street, Sacramento, CA 95814 800.232.7645 | cda.org

Formulario del paciente para la detección de Covid -19 Instrucciones de uso: Use un formulario para cada cita con el paciente. Hágale al paciente estas preguntas en el momento de la cita o con el recordatorio de la misma, y nuevamente no más de dos días antes de la cita. Mida la temperatura del paciente y compruebe si hay algún indicio de fiebre, tos o falta de aliento. Nombres del paciente/padre o madre/tutor: __________________________________________________________

Preguntas de evaluación

¿Tiene fiebre o una temperatura superior a la normal (>100 °F)? Mida la temperatura en la cita.

 No  Sí

¿Le falta el aire o tiene problemas para respirar?

 No  Sí

¿Tiene tos seca?

 No  Sí

¿Tiene secreción nasal?

 No  Sí

¿Tiene dolor de garganta?

 No  Sí

¿Siente escalofríos o temblores recurrentes con escalofríos?

 No  Sí

¿Tiene dolor muscular sin causa aparente?

 No  Sí

¿Tiene dolor de cabeza?

 No  Sí

¿Tiene náuseas, vómitos o diarrea?

 No  Sí

Aunque no tenga ninguno de los síntomas anteriores en este momento, ¿ha experimentado alguno de ellos en los últimos 14 días?

 No  Sí

¿Ha perdido o ha sufrido recientemente una reducción en su sentido del olfato o del gusto?

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Fecha: xx/xx/xx Fecha: xx/xx/ Iniciales del Iniciales del personal:____ personal:____

Notas

Si la respuesta del paciente es afirmativa a cualquiera de las preguntas sobre la falta de aire o la tos, o a cualquier combinación de otros dos síntomas y el paciente no necesita atención de emergencia, considere la posibilidad de no programar una cita ni ver al paciente hasta que los síntomas desaparezcan o hasta que el paciente pueda aportar pruebas de que no es contagioso de COVID -19. Se aconseja al dentista que busque información adicional del paciente con respecto a los síntomas.

Si la respuesta es afirmativa y el paciente no necesita atención de emergencia, no lo vea a menos que hayan pasado más de 10 días desde la aparición de los síntomas y 24 horas de no tener fiebre sin haber utilizado medicamentos antifebriles. CDC issued guidance on July 27th

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Formulario del paciente para la detección de Covid-19

Preguntas de evaluación

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Fecha: xx/xx/xx Fecha: xx/xx/ Iniciales del personal:____

Iniciales del personal:____

¿Ha estado en contacto sin protección con alguien que haya dado positivo para COVID-19 en los últimos 14 días? “ Contacto sin protección” significa sin el uso de equipo de protección personal.

 No

 Sí

¿Le han hecho la prueba de COVID-19 en los últimos 14 días? En caso negativo, pase a la siguiente pregunta.

 No

 Sí

 No

 No está

 Positive

 No

 Sí

En caso afirmativo, ¿cuál es el resultado de la prueba? En caso negativo, pase a la siguiente pregunta. Si todavía espera los resultados, programe una cita después de que se conozcan.

¿Ha viajado una distancia superior a 100 millas de su casa en los últimos 14 días?

seguro

Notas

En caso afirmativo, pregunte la fecha del último contacto con el paciente COVID positivo y fije una cita para más de 14 días después, a menos que el paciente necesite atención de emergencia.

Si es positivo, determine si el paciente necesita atención de emergencia. Si no es una emergencia, programe la visita del paciente para cuando hayan pasado más de 10 días (20 días si la enfermedad del paciente era grave) desde la aparición de los síntomas y 24 horas de no tener fiebre sin haber utilizado medicamentos antifebriles. En caso afirmativo, determine si el paciente viajó a una zona donde haya un alto número de casos de COVID -19. Determine si el paciente siguió las precauciones de distanciamiento físico y si usó una mascarilla en público. Use su juicio profesional para decidir si debe proceder con la cita.

Se requiere la firma del paciente en la cita: Acepto dar aviso a la clínica dental si dentro de dos días presento síntomas de COVID-19 o tengo un resultado positivo de COVID-19. Entiendo que la clínica dental tiene la obligación legal y ética de informarme si un miembro del personal con el que tuve contacto ha tenido un resultado positivo de COVID-19 dentro de dos días. Firma ___________________________________________________________________________________________

OC TOBER 2 0 2 0 569

Specialists in the Sale and Appraisal of Dental Practices

Serving California Dentists since 1966 How much is your practice worth??

Practices Wanted

The Sun will Shine again but Brighter! NORTHERN CALIFORNIA (415) 899-8580 – (800) 422-2818 Raymond and Edna Irving Ray@PPSsellsDDS.com www.PPSsellsDDS.com

SOUTHERN CALIFORNIA

(714) 832-0230 – (800) 695-2732 Thomas Fitterer and Dean George PPSincnet@aol.com www.PPSDental.com

California DRE License 1422122

California DRE License 324962

6184 SAN FRANCISCO’S EAST BAY – LAMORINDA AREA Unique opportunity for Dentist seeking nominal investment to open practice in this high income area. Revenues have averaged $390,000 a year on part-time basis. Highly regarded. 6183 REDWOOD CITY Long established practice seeks next caretaker. Collected $730,000 in 2019. 4-day Hygiene schedule. 5-ops, paperless and digital Pano. Ideal for nearby Dentist seeking larger facility, or as acquisition and vertically integrated into Buyer’s existing practice. Seller can associate back for up to a year to assist in transition. 6182 NAPA VALLEY Collections the last three years have averaged $1,000,000 per year. Available Profits in 2019 totaled $374,000. 4-days of Hygiene. Paperless charting. All specialty work referred. Well designed office. Great staff. Great location. 6181 CARMEL VALLEY VILLAGE - START-UP Slam dunk for nominal investment. 48-year history providing dental care at same location. Great curb appeal. Fully equipped & furnished 4-ops. $1+ Million/year location. Only practice in Village. Next practice 10-minutes away; then 17-minutes to practices in Carmel. Landlord is daughter of original dentist who worked as hygienist for her Dad & later her Husband; and transitioned to Manager. Shutdown April. Purchase equipment & furnishings, enter into Lease and open doors. Patients return. Operate out-of-network Great 2nd office for Monterey / Salinas Area dentist or starter for go-getter. Full Price $19,750. 6180 SAN FRANCISCO CONCIERGE PRACTICE Averages 3-to-5 Dentist patients day. Collected $796,500 in 2019. Available Profits totaled $391,500 in 2019 with 9-weeks off. Located in service & shopping area of high income zip code with average household income of $286,800. Décor, delivery systems, technology reflect $258,000 in upgrades. Fees will not change. Full Price $550,000. 6179 CENTRAL MARIN COUNTY Extremely strong foundation as evidenced by 7-days of hygiene. Beautiful office with great central location. Collections last 3-years have averaged $870,000. Owner is conservative with patients well educated on issues occurring in their mouths. 6177 SALINAS During Great Recession, Salinas dentists did well as Salinas Valley is one of California’s most productive agricultural regions and is the engine driving this area’s economy. As such, Salinas shall bounce back quickly from Covid Hangover. Under-performing practice collected $935,000 in 2019. 5-days of Hygiene. Housed in beautiful 6-op suite. Condo optional purchase. Great platform to bring in specialists. 6176 SANTA CRUZ Delta PPO practice seeks Successor skilled in placing implants. Last 2-years averaged $1,180,000 in collections and $735,000 in Available Profits. $480,000 invested in technology to make this possible. 4-days of Hygiene. Full Price $675,000. Compare to similar nearby "For Sale" practice asking $1,350,000 with another brokerage. 6174 HUMBOLDT COUNTY’S UNIVERSITY COMMUNITY – ARCATA Best location, great foundation. Owner works 3-day week by choice. 2019 collected $360,000. Practice wants to be full time. Full Price $50,000. 6172 WALNUT CREEK – OUT-OF-NETWORK 2019 collected $850,000 with Profits of $430,000. 4-days of Hygiene. Requires skilled, easy temperament and great communicator as Successor. Seller shall work-back to assist in transition. 6171 SANTA ROSA Great DNA in long-established practice. Strong patient foundation per 6+ day Hygiene Schedule. 2019 collected $990,000 with Available Profits of $338,000. Great Team. Full Price $213,750. 6165 ROSEVILLE ORTHO – OUT-OF-NETWORK Stanford Ranch. $455,000 invested in build-out, furnishings, computers and equipment. 3-chair Bay. Digital Pan with Ceph. Averages 3 New Patients per month. Full Price $125,000.

Great Time to Think about Change. Not doing the Type of Dentistry You would like to do? Look to Tom Fitterer & PPS to plan your future. BAKERSFIELD AREA Small city. Seller built 4,500 sq.ft. beautiful home for $450,000. (Cost $1.5 million in OC.) Hi identity dental building. 7 Adec ops. 3,000 sq.ft. next to Health Center for 1.2 million people. Established 32 years. Grossing $1 Million. Buy all at Bank Appraisal, 5 Dentists serving 40,000 market area patients. BEAUMONT AREA 8,000 new homes to be built 5 minutes away. Retiring DDS established 1988. 1,550 sq.ft. 3-ops. Rent $1,650. Average Gross $365,000. BEAUMONT / BANNING Senior DDS Grossing $250,000. 1-op. Rent $960 per month. Take home $200,000. EAST LOS ANGELES 60 years old. 3-ops. Rent $1,600. Part-time Senior Grossing $285,000 on 2-days. Do $500,000 on 3.5 days. Hi visibility. Bargain at $195,000. HEMET - HISPANIC AREA Includes Dental Building. Established 50-years. Absentee Seller. This is a neglected practice. Beautiful 5-op office. Open part-time. Will do $500,000 first year. $1 Million in 3-years like one prior owner. Pay Mortgage that never goes up. Part-time Seller will transition. Cerec. $250,000 buys practice. Small down buys building. Historic location. Live in apt if you like during week, live on beach on weekends. GP INNOVATOR Gross $1,700,000. Net over $1 Million. Nothing fancy, low tech dentistry. Full Price $1,500,000. INLAND EMPIRE - UNION PRACTICE Gross $550,000 2.5 days by choice. Net $350,000. 5-ops. INTERSECTION OF 210 / 57 Hi identity. 25-years old. Unbelievable state-of-art. 10-ops, new everything. Recent $500,000 renovation. Cone beam, Cerec, lasers. Grossing $1,100,000. Seller has 2-practices, cannot do both justice. This is a $2,000,000 location. LA HABRA - HUGE SHOPPING CENTER Well maintained. PT Seller will stay. 6 ops. LAGUNA WOODS Grossing $800,000 part-time. Should gross $1,000,000. MARINA DEL REY Take home $1 Million Net. HMO checks $5-to-8,000/month. Resume required ORANGE COUNTY Established 1970. Near Chapman / Tustin intersection. Grossing $400,000. Merge or Grow PALM DESERT Hi identity. Established 2007. Terrific one girl staff. Mostly Hispanic. Low overhead. Rent $1,600. Gross near $300,000. Semi-retire on 2-or-3 days. 4-ops, 2-equipped. PALM SPRINGS AREA $1,500,000 includes specialists. Grow to $2,000,000+. 8-ops. Best buy. TORRANCE – PACFIC COAST HIGHWAY Market to Palos Verdes to LAX area. 50-to-70,000 autos pass daily. Across street from major retailers with Hi Identity. High Tech Adec like-new, 6-ops, no expense spared. $5,000 HMO checks pays 56% of cost to buy. Within 36-months, Buyer will net $50,000 a month. After 5-years, Net of $1,000,000 per year is achievable goal. REDONDO BEACH Semi-retire. Work 2-to-3 days, low overhead. Established 20years. 2-ops. Super staff. Rent $1,550. Seller refers a lot. Full Price $118,000. SAN DIEGO GROUP 4-office DSO grossing $3.7 Million. SOUTH BAY OPPORTUNITY For talented GP to Net $50,000/month. TEMECULA SHOPPING CENTER High visibility. 5-ops. Grossing $40-to-50,000 month. Absentee owned. Hands on owner will double first year. Bargain. THOUSAND OAKS Classic practice. Established 42-years. One Partner willing to work back 3-to-5 years. Grossing $1 Million. Refers lots to Specialists. 5-ops. Owners own 25% of Building housing 4 Dentists including Ortho. Great for Specialist or GP. UPLAND Established 38-years. 3-ops. Grossing $330,000. 2000 active patients

RM Matters

C D A J O U R N A L , V O L 4 8 , Nº 1 0

Business Controls Reduce Employee Theft TDIC Risk Management Staff

eing the victim of theft is bad enough, but when that theft is perpetrated by a trusted member of your dental team, it’s especially harrowing. Unfortunately, theft within dental practices is surprisingly common and it’s on the rise. One of the most common types of theft in the dental office is staff embezzlement. A survey released in February 2020 by the American Dental Association found that 48% of respondents had been the victim of embezzlement — a 13% jump from a decade prior. Surprisingly, 46% of responding practice owners had been victimized more than once. One case reported to The Dentists Insurance Company involved a practice owner who oversaw two offices that were largely operated by associate dentists. He hired a bookkeeper to work for both offices. The owner became aware of possible wrongdoing after receiving a call from the bank alerting him of suspicious signatures on his company checks. Apparently, the bookkeeper had attempted to intercept the alert from the bank, but she could not successfully answer the account security questions. The bank called the office again after the employee abruptly ended the call. The owner learned that the employee had been using a signature stamp on the checks to provide herself bonuses and cash advances. She listed herself as an employee on the payroll of each office to receive duplicate paychecks. She also used her company credit card to make personal purchases for herself and pay expenses for her husband’s business as well as taking cash advances at a local casino. The employee then used company checks to pay credit card bills, which she allowed to incur late and over-limit fees. The owner filed a police report and the employee was prosecuted and ordered to pay restitution. As the former employee no longer had assets or a job,

the dentist was not able to recover any funds beyond those covered by insurance.

Employee Controls

Dental practices are typically tight-knit workplaces built on trust and camaraderie. Practice owners put their trust in their staff, especially those who have been employed many years. However, longterm employees are the most likely to be engaged in theft or embezzlement. The ADA survey found that nearly 40% of employees accused of stealing had been with the practice for four years or more. These are typically employees who handle accounts receivable, accounts payable and banking functions, said Jennifer

Duggan, a California attorney specializing in business and employment law. “The prototypical thief is a long-time employee who is extremely familiar with the financial aspects of your business,” she said. The telltale behaviors to watch for include the following: ■ Possessiveness about duties and reluctance to cross-train. Dishonest employees must keep illicit activities hidden, so they typically refuse to delegate duties or share responsibilities. They can also be territorial about their workspace. ■ Coming in early/working late. “Ever-present” employees aren’t

answers

From one-on-one risk management advice by phone to informed consent forms to expert-led seminars, we’re here to help you practice with confidence. We are The Dentists Insurance Company. Learn more at tdicinsurance.com/rm

Protecting dentists. It’s all we do.

800.733.0633 | tdicinsurance.com | Insurance Lic. #0652783

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OCT. 2020

RM MAT TERS C D A J O U R N A L , V O L 4 8 , Nº 1 0

always just hard workers. This can be a warning sign, as thieves need time in the office away from prying eyes, often before staff has arrived in the morning or after everyone has left at night. ■ Refusal to take vacation. Illicit activity often surfaces when the perpetrator takes extended leave and another employee fills in. Asking to cash in vacation or skipping it altogether is a red flag. ■ Complaints about finances. Frustrated employees who are always short on cash or those facing unexpected expenses are the most likely to commit fraud. Another red flag is an employee who appears to live well beyond their means. Other best practices, such as conducting dentist-to-dentist reference checks before hiring and cross-training employees for multiple duties, can help prevent dishonest behaviors.

Accounting Controls

Implementing accounting controls thwarts potential employee embezzlement. Unfortunately, many dentists inadvertently put their practices at risk for fraud by trusting a single employee with financial responsibility or not reviewing accounts payable and receivable. Cases reported to TDIC show instances of employees deleting appointment and ledger entries, endorsing patient checks to personal accounts, forging payroll checks, modifying payroll, misappropriating credit cards and using signature stamps without authorization. In some instances, employees have even redirected funds from dentists’ merchant account to their personal accounts or issued phony refunds to a personal account. In more sophisticated schemes, employees fabricate fictitious vendors, create nonexistent employees, 572 OC TOBER

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receive kickbacks from patients or from vendors for awarding company contracts or even coerce subordinate employees to carry out theft. “Simply reviewing your bookkeeping structure and implementing accounting measures will greatly reduce the probabilities of falling victim to employee theft,” Duggan said. “Instituting controls also communicates to employees that you are paying attention and discourages even the thought of stealing.” Other accounting controls to include: ■ Delegate financial tasks among employees, such as opening incoming mail and data entry for deposit and receivable information, to minimize opportunities for an employee to manipulate account information. ■ Separate job functions of reviewing monthly bank statements, entering online payments and preparing monthly bank reconciliations. If you have multiple authorized signers, separating the job functions of preparing the checks and signing the checks reduces risk. ■ Request that the bank mail statements to your home or personal email address and review statements regularly for unusual accountspayable names or inconsistencies. ■ Secure company checks in a location accessible only to authorized employees. ■ Require supporting documentation (a vendor invoice or credit card statement, for example) for every check you sign and review it to ensure expenditures are justified. ■ Run an accounts-payable history to review invoice numbers and amounts. ■ Provide specific instructions or guidelines to your bank that include a list of approved vendors and authorized signers. ■ Watch for an increase in patient refunds, adjustments or bad-debt write-offs. An unusual number of accounts turned over to collections

or a decline in the gross income or practice profitability is suspicious. Discrepancies between accountsreceivable records and patient statements should also be suspect. ■ Watch for increases in patient complaints regarding their accounts, which could indicate fraudulent activity or the need to develop a policy clarifying account procedures. Reviewing and responding to patients’ concerns personally is recommended. ■ Hire a practice software specialist to ensure security controls and work with a consultant to oversee changes in systems. ■ Run an audit report on patient accounts to look for an unusual amount of transactions where an account payment is posted and then the payment is reversed after the deposit has been processed. TDIC policyholders can access more guidance on employee embezzlement, including methods, prevention strategies and recovery tips, through the Embezzlement Reference Guide. TDIC Commercial Property insurance provides Business Owner’s policyholders coverage for employee dishonesty losses occurring within their practice. If the loss also involves the misappropriation of your identity, TDIC offers identitytheft recovery for the individual dentist under its Professional Liability policy. If you suspect you may have been the victim of embezzlement, contact your professional insurance carrier immediately. TDIC policyholders have access to trained analysts who will discuss the situation and next steps, including best practices for documenting the fraud. n TDIC’s Risk Management Advice Line is a benefit of CDA membership. If you need to schedule a no-cost consultation with an experienced Risk Management analyst, call 800.733.0633 or visit tdicinsurance.com/ RMconsult.

Regulatory Compliance

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Teledentistry and HIPAA CDA Practice Support

ot long after the U.S. declared a national emergency due to COVID-19, the U.S. Department of Health and Human Services Office for Civil Rights announced it would exercise enforcement discretion and waive potential penalties for HIPAA violations against health care providers who serve patients through commonly used, nonpublic-facing communications technologies.1 With shelter-in-place orders, many dentists found themselves conducting virtual limited evaluations and triage over such platforms as Apple FaceTime, Google Hangouts, Whatsapp, Skype or Zoom. OCR’s enforcement discretion allowed health care providers to immediately use these platforms without executing HIPAA business associate agreements or undertaking a risk assessment. Some months after returning to practice, dentists continue to use virtual patient encounters for any number of reasons — infection control, patient convenience and consultations, for example. It appears that now a larger number of dentists are incorporating teledentistry into their practice than before the pandemic. Now is the time for these dental practices to ensure their information security policies and procedures have been updated to ensure they are in compliance with HIPAA requirements when the pandemic ends. The first step is to obtain a HIPAA business associate agreement from any vendor that electronically transmits or stores patient information. The agreement must describe how the vendor is permitted or required to use or disclose patient information and the limits to those uses and disclosures. The agreement should make clear a vendor’s

obligation to comply with the HIPAA security rule and certain provisions of the privacy rule. The dental practice should ensure breach notification procedures and vendor obligations in case of a breach are detailed in the agreement. If a vendor stores information, the agreement should include provisions related to the return or destruction of the dental practice’s information. Next is a risk assessment, which should be documented. Consider every step in the teledentistry encounter. Identify the devices used and who controls those devices. If patient information, such as images, is stored on a device or managed using software, determine if the device or software uses encryption. If not, policies and procedures to reduce the risk of unauthorized access should be developed and implemented. If a device stores patient information temporarily, determine if secure communication is used to transfer the patient information to the permanent storage location, either the cloud or the dental practice system. Risk such as theft, loss and unauthorized access to the information should be addressed in the assessment. Consider, for example, a dentist’s use of their cellphone to manage a patient of record who is having a weekend dental emergency. After speaking with the patient, the dentist instructs the patient to take photographs of the affected area and to send the photos to the dentist via email or text (choosing the most secure method). The dentist reviews the photographs, calls the patient and assures them the situation can be taken care of on Monday and no weekend visit is necessary. Upon completing the conversation, the dentist types notes into their cellphone and

sends the notes and photos to their office email to be added to the patient record. The dentist uses secure email and texting software and an encrypted cellphone. Alternatively, the dentist can enter the information onto the patient’s record stored in the cloud by using a tablet or personal computer. The above example is teledentistry in its simplest form. Another form of teledentistry, the virtual dental home described by Glassman et al.,2 involves allied dental professionals collecting information from patients, including radiographs, and sending it to one or more dentists at remote sites, then receiving instruction from the dentists. A cloud-based electronic health record system is used and live videoconferencing is more likely. With multiple users at different locations, the scope of the necessary risk assessment is greater than the example described above. More users and more technology present more risks to the security and privacy of patient information. Dental practice owners using teledentistry must ensure their policies and procedures adequately address these risks. n REFERENCES 1. OCR announces notification of enforcement discretion for telehealth remote communications during the COVID-19 nationwide public health emergency, March 17, 2020. www.hhs.gov/about/news/2020/03/17/ocr-announcesnotification-of-enforcement-discretion-for-telehealth-remotecommunications-during-the-covid-19.html. 2. California Dental Association. Virtual Dental Home, July 2012. www.cda.org/Portals/0/journal/journal_072012.pdf.

Regulatory Compliance appears monthly and features resources about laws that impact dental practices. Visit cda.org/ practicesupport for more than 600 practice support resources, including practice management, employment practices, dental benefit plans and regulatory compliance. OC TOBER 2 0 2 0 573

CARROLL &COMPANY 4407 SAN MATEO GP Exceptional 5-operatory San Mateo practice in popular health provider neighborhood generating significant daily business draw. Beautiful 2,200 sq. ft. seller-owned facility, handsomely equipped to highest standards. Average GR $1.4M, average overhead 61%. Seasoned and loyal staff. Seller willing to help for a smooth transition. 4417 SANTA CLARA GP Offering 40+ years of goodwill in wonderful

Santa Clara location. Nicely appointed office with 4 fully equipped ops in approximately 1,500 sq. ft. Traditional family practice focused primarily on restorative dentistry and hygiene care, referring out most specialities. Average 2-3 hygiene days/week. Average GR $650K with average adj. net of $304K. Asking $415K. Seller willing to help for smooth transition. 4394 SANTA CRUZ GP Retiring seller offering 33+ years of goodwill in stunning 1,534 sq. ft. facility with 4 fully-equipped ops. Pristine leasehold improvements/gorgeous cabinetry make this a must-see! Prime corner location with dedicated parking lot, situated in one of the most desirable areas of Santa Cruz, close to shoreline and tourist attractions. 2019 GR $887K with adj. net of $353K. 1,500+ active patients with average of 19 new patients/month. Seller works 3+ days/week with 5+ days of hygiene. Asking $729K. 4405 LOS GATOS GP 30 year practice in beautiful modern, office and desireable location with two 5 year D options to extend lease. $1.2M OL average overhead. Asking $986K. average gross receipts withS56% 4382 MONTEREY COUNTY GP Established practice in Monterey County, California Coast. Multiple ops can expand, approx. 900 active patients, 4 days of hygiene per week. Ideal for a mature, experienced dentist for this adult-focused practice in an Extraordinary location. Periodontal emphasis with communicative technology in each operatory for multiple crown and implant restorative procedures. Loyal, committed staff will remain through transition. Future opportunity to purchase office building. 4351 SEBASTOPOL AREA GP & BLDG. Beautiful, modern practice in seller-owned building (available for purchase); 3 fully-equipped ops, room for a 4th. Pristine equipment including digital X-ray, most purchased 2016-2018. 2019 GR annualized at $679K+ with adj. net of $210K. Average 3.5 doctor days/week and 4 hygiene days/week. 800 active patients, all fee-for-service. 70+ years of goodwill = long-standing, loyal patient base in scenic vineyard country. Asking $305K for practice, $425K for building. Owner/doctor willing to help for smooth transition. 4406 PALO ALTO GP Offering 50+ years of goodwill in growing practice close to Stanford University. Great Palo Alto location with incredible G visibility. 7 ops in recently remodeled DIN2,152 sq. ft. office. 1,400+ active EN patients. Pre-Covid hygienePschedule running at 8 days/week. 2019 GR $1.5M+ with adj. net of $518K. Services provided are typical of practice with emphasis on Restorative dentistry. Asking $1,185,000. 4399 SAN JOSE GP Gorgeous office in pristine condition located on a well-traveled thoroughfare with incredible views of the eastern foothills. D Approx. 2,000 active patients with OL 12-13 new patients per month. Approx. S 8 hygiene days/week. Average GR $1.3M. Asking $977K.

“Matching the Right Dentist to the Right Practice”

4415 WATSONVILLE GP & BLDG Offering 35 yrs of goodwill in the growing coastal community of Watsonville. Charming and renovated 4 op office in 1,320 sq. ft. Approx. 450 active patients with an average of 10 new patients/mo. Incredible G DIN management systems in place. Endo, Oral upside potential withN excellent E P procedures referred out. Last 2 yrs average Gross Surgery and all Ortho Receipts $275K with average adj net of $159K on just 1.5 doctor days/ week. Bldg condo is also available for purchase. Asking price $175K for practice and $300K for condo. 4389 SALINAS GP Stable, 2400+ patient base. Seasoned and dedicated staff. Practice with an emphasis on Restorative treatment. 4 doctor days & 5 hygiene days per week. Average GR $910K. Asking $670k. Retiring owner. 4360 SALINAS GP Seller transitioning into retirement and offering wellestablished practice located INGnear downtown Salinas and Salinas Valley Memorial Hospital. Average ND Gross Receipts $250K. Asking $133K.

4416 SF FACILITY Located on Lyon street, closest major cross street Lombard. 1,600 sq. ft. turn-key dental facility. This street level space has over $350,000 of improvements completed for professional use and ready to go as a dental office. Asking $35K. 4392 SAN JOSE GP Offering 40+ years of goodwill. Excellent location in beautiful bldg on well-traveled thoroughfare. 6+ ops in 1,882 sq. ft. Lots of natural light with views of the eastern foothills. 1,800 active patients. 8 hygiene days/wk. Average GR $900K with adj. net of $295K. Terrific upside potential. Asking $558K. Owners will help for smooth transition. 4362 MARIN COUNTY GP 36 years of goodwill, Seller-owned 1,550 square foot facility with 5 fully-equipped ops. Prime position in charming town; desirable area known for temperate weather, easy, outdoor living and natural beauty. No Delta Premier patients. Excellent reputation and word-of-mouth referrals. Retiring seller will help for smooth transition. Average Gross Receipts last 2 yrs is $450K. Asking $248K for the practice. Bldg condo is available for purchase. 4375 LOS GATOS DENTAL FACILITY Unique opportunity in highly desirable area! Seller offering two full suites of state-of-the-art equipment and modern, 2-operatory facility including furniture, fixtures and leasehold assets in medical office building adjacent to Los Gatos Community Hospital. Asking $250K. UPCOMING: REDWOOD SHORES GP, PALO ALTO GP, SAN JOSE GP & OAKLAND GP

Mike Carroll

Pamela Carroll-Gardiner

Mary McEvoy Carroll

CalRE# - 00777682

carroll.company

dental@carrollandco.info

(650) 362-7004

(650) 362-7007

Ethics

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Food for Thought Henrik Hansen, DDS

ow that I’m in my 42nd year of practice and my hair has lost most of its color, I’m asked a lot when I’m going to retire. My answer is: God willing, not anytime soon. A few months ago, an 80-year-old patient said after I told him that he looked great, “I’m going to be around another 50 years, and you’ll be my dentist.” My comment was, “Leo, do you really want a 121-year-old dentist in your mouth?” Whereupon he said that at 130, he pretty much would not care. I enjoy my patients and would miss them. I still get excited when things go well, and the math major in me loves the problem-solving challenges. However, it’s got me thinking about when it will be time to hang it up. Most of my local contemporaries have already retired, some to travel and pursue other activities while they’re still vertical, some due to physical issues and some because they’re tired of the strain of practice. However, when is it time to retire because you just can’t provide the same level of care as you once did? Many years ago, a patient of one of the local pillars of the dental community came in to get a second opinion. It seems this elderly dentist had placed a crown on a lower molar and the patient could feel a sharp point next to the tooth. I noticed a massive “J” margin on the lingual where the point of the J was about 2 mm from the lingual wall of the crown and poking above the gums. I called the dentist and gently explained the situation. He told me it’s getting harder and harder to do the work due to poorer vision and trembling in his hands. I said that as the years go by, there are going to be changes and most not for the better. The rational thing to do is to recognize when it’s time to stop practicing – for the patients’ sake, as well as yours. He thanked me and shortly thereafter retired. Dentistry is very often

hard to do well and takes its toll on us physically, mentally and emotionally. Two years ago, when I turned 70, the DMV gave me the written test to check that dementia hadn’t gone too far and the eye test to make sure I could still see. In order to graduate from dental school and get a license to practice, we must demonstrate certain core competencies. However, unless you run afoul of the dental board, that’s the last you’ll be looked at. So, it’s up to the individual to gauge when it’s time to stop. This decision is not always an easy one, but one filled with ethical considerations. There is beneficence (do no harm), veracity (truthfulness), professionalism,

compassion, competence, integrity and justice. That’s just about the whole list. So how do you judge? My personal retirement test is when I can do an acceptable crown prep after chasing decay subgingival down the root on an endodontically treated tooth with the patient comfortable and not numb. If my eyes and hands can pull that off, I’m OK. So, it begs the question, “What’s your retirement test?” n Henrik Hansen, DDS, is a general dentist practicing in Fairfield, Calif. He served on the CDA Judicial Council and is past chair of the Council on Peer Review as well as a past member of the ADA Council on Dental Benefit Programs.

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Tech Trends

C D A J O U R N A L , V O L 4 8 , Nº 1 0

A look into the latest dental and general technology on the market

Neewer Foldable 256 LED Lighting Panel on Fabric ($99, Neewer) Ideal, consistent lighting for clinical photographs is difficult to attain in a dental practice due to an assortment of distracting light sources, inadequate space for professional lighting fixtures and the mouth itself being a difficult subject to capture. Fortunately, improved LED technology has led to capable and affordable facsimiles of professional lighting products that can improve outcomes without complicating clinical workflows. One such product, which has been gaining attention in the amateur photography world, is the fabric LED panel. These devices are pieces of cloth with small but powerful LED bulbs sewn into them to provide users with an adaptable light source that can be held and contorted in a multitude of configurations. The Neewer Foldable 256 LED Lighting Panel on Fabric is one of many similar products; however, it manages to incorporate a few features that make it rise above many of its peers. The entire product consists of the fabric panel, a carrying case, four aluminum square tubes that lock together to form an optional frame, a cloth diffuser to soften the light, an adapter to screw the frame onto a tripod, a remote control and the power adapter. All these items combined weigh about 3 pounds with the fabric panel itself weighing less than 10 ounces, and all fit well in the 12-inch carrying case. Operation is simple: Turn on the light switch and adjust brightness with the remote, which as a bonus can control two Neewer panels independently. The panel produces 4,500 lumens and is harshly bright; it is strongly recommended to use the diffuser (which attaches via Velcro on the panel lining) at all brightness levels. The panel can be wrapped around the arm of an operatory light, taped to a surface or propped on a table. Overall, the Neewer Foldable 256 LED Lighting Panel on Fabric is an affordable, small and versatile device that can help with lighting inconsistencies in a clinical setting. — Alexander Lee, DMD

Adobe Photoshop Camera (Free, Adobe) Most people enjoy taking good pictures with their smartphone camera whether for social media, art, hobby, passion or fun. With the technology and processing power packed into current smartphones, anyone can become an amateur professional photographer without advanced training. One of the tools available to take advantage of this is Adobe Photoshop Camera, an app that uses the power of artificial intelligence to bring professional-quality filters and effects to smartphone camera photos. Adobe Photoshop Camera requires an Adobe account, which is free to create. Once logged in, the app is extremely easy to use with intuitive controls and gestures organized around the shutter button to navigate through its features. The shutter button is comfortable and prominently placed where the thumb naturally rests on the lower center area of the screen, which displays a live preview of the front- or rear-facing camera. Immediately to the left of the shutter is the lens button that brings up a tray of effects organized by category. Selecting a lens immediately applies the effect to the live preview displayed. Users can swipe left or right to choose between various effects from within a category. New lenses are available weekly from Adobe and can be downloaded directly and managed from within the app. The app makes real-time intelligent lens recommendations when certain objects, such as selfies, food or scenery, are detected in the live preview by displaying an effect button above the shutter. The library button to the right of the shutter allows users to navigate through their studio of photos taken by the app or to access and apply effects to photos in their default camera roll. Other features within the app include changing the picture aspect ratio for compatibility with social media services and standard camera adjustments for focus, flash and lighting. Pictures taken by the app with applied lens effects are visually stunning and ready to share with others. With an endless library of lens effects available for users to choose from and an intuitive interface, Adobe Photoshop Camera makes professional photography easily accessible to anyone with a smartphone. — Hubert Chan, DDS

576 OC TOBER

2020

Hey, let’s keep a good thing going. CDA Presents The Art and Science of Dentistry didn’t stop delivering C.E. and expertise on the last day of the virtual convention. From the convenience of your home or office, you can continue taking part in engaging education and checking out innovative exhibitors.

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150 YEARS STRONG

CDA. WE’VE BUILT THIS TOGETHER. In 1870, the California Dental Association was founded by 23 visionary dentists. In 2020, we’ve grown into a diverse, inclusive community of 27,000 members. Today, we continue to face new challenges with passion and purpose. Working together, we’re building an enduring future.

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1870 2020

CDA Journal - October 2020: Dentistry and COVID-19

Articles inside

Letter

Tech Trends

Ethics — Food for Thought

Regulatory Compliance — Teledentistry and HIPAA

RM Matters — Business Controls Reduce Employee Theft

Teledentistry 101: A Primer for Dental Professionals for the New Normal

COVID-19: New Considerations for Respiratory Protection in Dental Practice

Face Masks and Respirators for the Dental Health Care Provider: A Review

Dentistry in the Context of COVID-19 : Oral Pathologists’ Perspectives Based on a Compilation of Data

Global Impact of COVID-19 on Service Delivery and Vulnerable Populations’ Access to Dental Care

Decoding Dental Aerosols in the Age of COVID-19

The Mouth-COVID Connection: Il-6 Levels in Periodontal Disease — Potential Role in COVID-19 -Related Respiratory Complications

Introduction — A Slice of Time

Editor — Masters of Splatter