CDA Journal - March 2022: A Dental Care Coordination System by California Dental Association

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March 2022 Adenomatoid Odontogenic Tumors Mouth-COVID-19 Connection

A S S O C I AT I O N

Nº 3

M A R C H 2022

Vol 50

A Dental Care Coordination System To Increase Access for Medicaid Dental Program Beneficiaries Experiences in Alameda County, California

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March 2022

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139 Editor/When Bad Things Bring Good Lessons 143 Impressions 183 RM Matters/Minimizing Risk While Giving Back to Your Community

187 Regulatory Compliance/ The Importance of a HIPAA Associate Agreement

189 Tech Trends

79 f e at u r e s

147 A Dental Care Coordination System To Increase Access for Medicaid Dental Program Beneficiaries: Experiences in Alameda County, California This paper focuses on the Alameda County Office of Dental Health’s LDPP, known as Healthy Teeth Healthy Communities (HTHC), as an exemplative case study of program successes, challenges and limitations to inform future dental health initiatives and policies. Benjamin W. Chaffee, DDS, MPH, PhD; Jared I. Fine, DDS, MPH; Yilak Fantaye, MPH; Kristin S. Hoeft, MPH, PhD; Rhodora Ursua, MPH; Ray Stewart, DMD, MS; and Suhaila Khan, MD, MPH, PhD C.E. Credit

159 A Mandibular Adenomatoid Odontogenic Tumor With a Novel Treatment Utilizing Platelet-Rich Fibrin This manuscript presents a case report of a tumor in a 60-year-old male with an asymptomatic mandibular lesion that radiographically presented as a mixed lesion. Tarun Mundluru, DDS, MSc; David Pilgrim, DDS; Reyes Enciso, PhD; Parish P. Sedghizadeh, DDS, MS; and Mohammad A. Khalifeh, DDS, MS

165 The Mouth-COVID-19 Connection: Importance of the Oral Cavity for the Coronavirus — Part I This narrative review addresses the role played by the oral cavity and saliva in the coronavirus disease, with particular focus on viral presence in the oral cavity. Shervin Molayem, DDS, and Carla Cruvinel Pontes, DDS, MsC, PhD

175 The Mouth-COVID-19 Connection: The Importance of the Oral Cavity for the Coronavirus Disease — Part II The second half of this narrative review addresses the role played by the oral cavity and saliva in the coronavirus disease, with particular focus on the importance of oral hygiene. Shervin Molayem, DDS, and Carla Cruvinel Pontes, DDS, MsC, PhD

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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

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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.

Editorial

C D A J O U R N A L , V O L 5 0 , Nº 3

When Bad Things Bring Good Lessons Kerry K. Carney, DDS, CDE

ome folks like to say that “everything happens for a reason.” The phrase is usually meant to comfort in times of loss and pain. However, that platitude can have the exact opposite effect when it discounts or diminishes the real and lasting emotional impact of traumatic events. If we acknowledge that bad things can happen for no reason, then it is incumbent on each of us to draw lessons from negative events in order to frame our lives as more than just a collection of random events. Lessons can guide us to improve the life experiences of others and ourselves. Take, for example, the lessons we can learn from this pandemic. I met recently with a local community service board. It was the first time we had met face to face in 20 months. The board is made up primarily of individuals at high risk for COVID-19 (most of our members are over 65). We had met a few times over Zoom, but this was not a group that felt comfortable meeting in person or over Zoom during the pandemic. We met inside. Everyone was vaccinated and boosted, but some members felt more comfortable wearing face masks. The main purpose of our meeting was to present a slate of officers for 2022. Last year, everyone agreed to extend their office terms for one year due to the difficult pandemic environment. The meeting was one I will long remember. Usually, people are hesitant to take on the duties of an office and it takes some cajoling and concession to fill the slate. This meeting was different. Everyone was enthusiastic and eager. Creative ideas and positive suggestions were contagious. By the end of the meeting,

If we acknowledge that bad things can happen for no reason, then it becomes incumbent on each of us to draw lessons from negative events.

we had a full slate of officers and had mapped out a direction for the group for 2022. Fundraising events were outlined, and an intention to reach out to other groups in our community was established and embraced. We all left the meeting energized and united by our uplifted spirits. I have thought a lot about that meeting since. Working with people can be challenging. Everyone brings so much psychological baggage with them. In groups, it is hard not to succumb to the endorphins of conquest, vindication and revenge. It is the rare individual who is satisfied to simply help another succeed and be recognized without requiring recognition for themselves. A unity of purpose can be a powerful motivator for that more positive behavior. Personal confession: I do not particularly enjoy a couple of the people in the group, but I appreciated the interaction. After our long, drawn-out COVID-19 winter of discontent, we were starved for social group interaction. After months and months of social media echo chambers that heightened tribal divisions and reinforced our biases, it was a relief. It was enjoyable to have to be nice to people I was not fond of previously. Instead of shouting insults (the equivalent of ALL CAPS texting) or “dropping the mic” after making a particularly cutting remark, we engaged in the kind of small

talk that reminded each of us that we are more alike than we are different. COVID-19 Lesson No. 1: Humans are indeed social animals. To be healthy, happy individuals, we need to play well with others. It is a lesson we learned in elementary school, and it took this disrupting pandemic to remind me of its importance. My next lesson became clear that same week when our office manager called to let me know that one of our providers had wrenched her back and was in the emergency room waiting to be seen. Pre-COVID-19 I would have launched into emergency mode. Cortisol levels would have risen as I imagined the disruption having her out for an extended period could mean. However, now after making sure she was being cared for and checking to see that her family would not be significantly impacted, there was a therapeutic calm. My first thoughts were: We were closed for 10 weeks with little notice last year and we survived. The pandemic has given us perspective. We have seen much worse and survived. With that perspective comes resilience. Here are three definitions of resilience from dictionary.com: ■ “The power or ability of a material to return to its original form, position … after being bent or stretched…” ■ “The ability of a person to adjust M ARC H 2 0 2 2

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to or recover readily from illness, adversity, major life changes, etc.” “The ability of a system or organization to respond to or recover readily from a crisis, [or] disruptive process…”

We have all been bent and stretched by the disruptions caused by this pandemic. We have had to change how we practice dentistry to some degree. We have had to deal with patients who were not just fearful of dental procedures but who were fearful for their very lives. We have dealt with fearful co-workers, colleagues, family and friends. And our professional organizations have responded and continue

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to respond effectively to the emergent needs of dental professionals in this public health crisis. COVID-19 Lesson No. 2: Resilience. We are experiencing a rebound as a result of our resilience. Finally, the COVID-19 pandemic has taught me to count my blessings. I am grateful for everyone and everything that helped us endure. I am grateful to all those who reached out to maintain those essential human connections. I am grateful to our staff who showed courage, strength and creativity in problem-solving. I am grateful to our patients who put their trust in us and made our office the first place they came to once they could leave their homes.

COVID-19 Lesson No. 3: Gratitude. It was a pleasant surprise to realize how lucky I am to have the family, friends and spouse that I have. It did not take me long to realize I was in an extended lockdown with the most charming, entertaining and caring person in the world. The pandemic is bad. These lessons are good. These are lessons we can embrace and act on. n

The Journal welcomes letters We reserve the right to edit all communications. Letters should discuss an item published in the Journal within the last two months or matters of general interest to our readership. Letters must be no more than 500 words and cite no more than five references. No illustrations will be accepted. Letters should be submitted at editorialmanager.com/ jcaldentassoc. By sending the letter, the author certifies that neither the letter nor one with substantially similar content under the writer’s authorship has been published or is being considered for publication elsewhere, and the author acknowledges and agrees that the letter and all rights with regard to the letter become the property of CDA.

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Impressions

C D A J O U R N A L , V O L 5 0 , Nº 3

Disarming Blood-Clotting Protein Prevents Periodontitis in Mice

In the oral mucosa, commensal microbiota triggers homeostatic inflammation, fibrin deposition and associated neutrophil activation, which physiologically resolves in the setting of efficient plasminogen-mediated fibrinolysis. (Reprinted with permission from Science 24 Dec 2021. doi: 10.1126/science.abl54505,491. Copyright 2021 American Association for the Advancement of Science.)

Blocking function of a blood-clotting protein prevented bone loss from periodontal disease in mice, according to research led by scientists at the National Institute of Dental and Craniofacial Research (NIDCR), part of the National Institutes of Health. Drawing on animal and human data, the researchers found that buildup of the protein, called fibrin, triggers an overactive immune response that damages the gums and underlying bone. The study, which was published in the journal Science, suggests that suppressing abnormal fibrin activity could hold promise for preventing or treating periodontal disease as well as other inflammatory disorders marked by fibrin buildup, including arthritis and multiple sclerosis. At sites of injury or inflammation, fibrin normally plays a protective role, helping to form blood clots and activating immune cells to fight infection. But too much fibrin has been linked with health problems, including a rare form of periodontitis due to a condition called plasminogen (PLG) deficiency. In affected people, mutations in the PLG gene lead to fibrin buildup and disease at various body sites, including the mouth. To explore the connection between abnormal fibrin buildup and periodontitis, the scientists, led by NIDCR investigators Niki Moutsopoulos, DDS, PhD, and Thomas Bugge, PhD, studied PLG deficiency in mice and analyzed human genetic data. Like humans with the condition, PLGdeficient mice developed periodontitis, including periodontal bone loss and elevated levels of fibrin in the gums. The mice’s gums were crowded with immune cells called neutrophils, which are also found at high levels in common forms of periodontitis. Neutrophils typically defend the oral cavity from harmful microbes. But an excessive neutrophil response is thought to cause tissue damage. To find out if fibrin was driving this overactive response, the researchers impaired its ability to interact with (bind to) protein receptors on neutrophils. The weakened binding between fibrin and neutrophils completely prevented periodontal bone loss in PLG-deficient mice. Strikingly, it also reduced bone loss in normal mice with a common, age-related form of periodontitis, suggesting that similar mechanisms were at play in both forms of the disease. A genetic analysis of over 1,000 people seemed to support the animal findings. Even in the absence of PLG deficiency, variations in the PLG gene were linked to an increased risk of severe periodontitis, consistent with the idea that similar processes contribute to rare and common forms of the disease. Taken together, the study suggests that excessive buildup of fibrin in the gums, whether due to changes in genes like PLG, chronic inflammation from a bacterial infection or some combination of the two, triggers an elevated and ultimately harmful neutrophil response that causes periodontal disease. Learn more about this study in Science (2021); doi.org/10.1126/science.abl5450. n M ARC H 2 0 2 2

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Study: How Ultrasmall Bacteria Live in Oral Microbiome Among the diverse bacterial species living within our mouths is a group belonging to the Candidate Phyla Radiation (CPR). These bugs are especially mysterious because they are ultrasmall, adopt a unique symbiotic lifestyle with their host bacteria and most have yet to be cultured by scientists and studied in the lab. The only bacteria within the CPR to be examined in-depth are a group called TM7, which were cultivated for the first time by Forsyth Institute researcher Xuesong He, DDS, PhD, in 2014. In an important step toward better understanding these elusive bacteria, Dr. He and colleagues have developed a new model system using the first isolated human oral TM7 strain, TM7x, and its host bacterium Actinomyces odontolyticus. Researchers used the model system to experimentally study these tiny bacteria, testing a hypothesis for how TM7 adapted to live inside humans and providing empirical data to confirm previous genomic studies. Their findings were published in the journal PNAS. Studies have shown that while maintaining a remarkably similar genome overall, the TM7 found in human mouths are unique from those in other environments because they have acquired a gene cluster encoding the arginine deiminase system (ADS). Researchers hypothesized that TM7 acquired ADS as an evolutionary advantage to help them adapt and survive 144

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Researchers from the University of Louisville School of Dentistry have discovered details of how proteins produced by oral epithelial cells protect humans against viruses entering the body through the mouth. They also found that oral bacteria can suppress the activity of these cells, increasing vulnerability to infection. Their study was published in the journal PNAS in December 2021. A family of proteins known as interferon lambdas produced by epithelial cells in the mouth serve to protect humans from viral infection, but the oral bacteria Porphyromonas gingivalis reduce the production and effectiveness of those important frontline defenders. “Our studies identified certain pathogenic bacterial species, P. gingivalis, can completely suppress interferon production and severely enhance susceptibility to viral infection,” said Juhi Bagaitkar, PhD, assistant professor in the U of L department of oral immunology and infectious disease. “These resident oral plaque bacteria play a key role in regulating anti-viral responses.” The mouth often is a gateway into the body for viruses that infect the gastrointestinal tract and lungs such as SARS-CoV-2, human immunodeficiency virus (HIV), herpes simplex and cancer-causing viruses such as human papillomavirus (HPV). P. gingivalis have been linked to numerous other diseases, including Alzheimer’s disease and rheumatoid arthritis. Recent clinical studies have shown that immune suppression in patients with periodontitis can enhance susceptibility to HIV, herpes simplex and HPV. Improved understanding of how interferons provide broad antiviral protection and activate antiviral genes to protect people from viruses, as well as how P. gingivalis compromise their protection, may lead researchers to clinical approaches to increase that protection. Read more of this study in PNAS (2021); doi.org/10.1073/pnas.2105170118.

in the human oral cavity. To test this hypothesis, they used the model system to experimentally investigate the function and impact of ADS on TM7x and its host bacterium. They found that ADS helped TM7x break down arginine, a process that produces the compounds Adenosine triphosphate (ATP) and ammonia. The increased abundance of ATP and ammonia benefitted TM7x by increasing its infectivity. It also protected TM7x and its host bacterium from acid stress.

Ultimately, the experiment showed TM7x were able to survive in the experimental environment for longer than they could without the addition of arginine, thanks to ADS. This study adds to a growing body of evidence that TM7 bacteria may play a more protective role in oral health than researchers initially thought. Learn more about this study in PNAS (2021); doi.org/10.1016/jchom.2021.09.009.

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A Chewing Gum To Reduce SARS-CoV-2 Transmission A chewing gum laced with a plantgrown protein serves as a “trap” for the SARS-CoV-2 virus, reducing the viral load in saliva and potentially tamping down transmission, according to a new study. The work, led by Henry Daniell, PhD, at Penn’s School of Dental Medicine, was published in the journal Molecular Therapy. Prior to the pandemic, Dr. Daniell had been studying the angiotensin-converting

enzyme 2 (ACE2) protein in the context of treating hypertension. His lab had grown this protein using a patented plantbased production system. By bombarding plant material with the DNA of target proteins, they coax plant chloroplasts to take up the DNA and begin growing the proteins. The plant material, freezedried and ground-up, could be used as a means of delivering the protein.

Gum Disease Increases Risk of Mental Health, Heart Conditions A University of Birmingham-led study published in the journal BMJ Open shows an increased risk of patients developing illnesses, including mental health and heart conditions, if they have a GP-inputted medical history of periodontal disease. Experts carried out a first of its kind study of the GP records of 64,379 patients who had a GP-inputted recorded history of periodontal disease, including gingivitis and periodontitis. Of these, 60,995 had gingivitis and 3,384 had periodontitis. These patients’ records were compared to those of 251,161 patients who had no record of periodontal disease. The researchers examined the data to establish how many of the patients with and without periodontal disease go on to develop cardiovascular disease, cardiometabolic disorders, autoimmune conditions and mental health conditions over an average follow-up of around three years. The research team discovered that those patients with a recorded history of periodontal disease at the start of the study were more likely to go on and be diagnosed with one of these additional conditions over an average of three years, compared to those in the cohort without periodontal disease at the beginning of the research. The results of the study showed, in patients with a recorded history of periodontal disease at the start of the study, the increased risk of developing a mental health disorder was 37%, while the risk of developing autoimmune disease was increased by 33%, and the risk of developing cardiovascular disease was raised by 18%, while the risk of having a cardiometabolic disorder was increased by 7%. Learn more about this study in BMJ Open (2021); doi: 10.1136/ bmjopen-2020-048296.

Dr. Daniell’s past work on ACE2 proved fortuitous in the context of the COVID-19 pandemic. The receptor for ACE2 on human cells also binds the SARS-CoV-2 spike protein. Other research groups have shown that injections of ACE2 can reduce viral load in people with severe infections. Another line of work by Dr. Daniell involved research to develop a chewing gum infused with plant-grown proteins to disrupt dental plaque. Pairing his insights about ACE2 with this technology, Dr. Daniell wondered if such a gum, infused with plant-grown ACE2 proteins, could neutralize SARS-CoV-2 in the oral cavity. To test the gum, the team grew ACE2 in plants, paired with another compound that enables the protein to cross mucosal barriers and facilitates binding, and incorporated the resulting plant material into cinnamon-flavored gum tablets. Incubating samples obtained from nasopharyngeal swabs from COVID19-positive patients with the gum, they showed that the ACE2 present could neutralize SARS-CoV-2 viruses. The scientists observed that the gum largely prevented the viruses or viral particles from entering cells, either by blocking the ACE2 receptor on the cells or by binding directly to the spike protein. Finally, the team exposed saliva samples from COVID-19 patients to the ACE2 gum and found that levels of viral RNA fell so dramatically to be almost undetectable. Learn more about this study in Molecular Therapy (2021); doi.org/ 10.1016/j.ymthe.2021.11.008. M ARC H 2 0 2 2

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MAY 12–14, 2022 ANAHEIM CONVENTION CENTER

care coordination C D A J O U R N A L , V O L 5 0 , Nº 3

A Dental Care Coordination System To Increase Access for Medicaid Dental Program Beneficiaries Experiences in Alameda County, California Benjamin W. Chaffee, DDS, MPH, PhD; Jared I. Fine, DDS, MPH; Yilak Fantaye, MPH; Kristin S. Hoeft, MPH, PhD; Rhodora Ursua, MPH; Ray Stewart, DMD, MS; and Suhaila Khan, MD, MPH, PhD

abstract Background: In 2016, the California Department of Health Care Services launched the Dental Transformation Initiative (DTI) to address statewide underperformance in providing dental services to Medicaid-eligible children and youth. The DTI allowed selected counties and other qualified organizations to create Local Dental Pilot Programs (LDPP) to enhance service utilization. Alameda County began Healthy Teeth Healthy Communities (HTHC), a multicomponent LDPP featuring community-based dental care coordination augmented with general dentist training in care for young children. Methods: This examination provides background, describes HTHC components and presents selected dental care access metrics from HTHC programmatic and state-maintained datasets during the time period of HTHC implementation. Results: From 2018-2020, 8,609 children and youth (ages 0-20 years) who received HTHC care coordination attended ≥ 1 dental appointment. Of all children and youth HTHC enrolled for care coordination, 87% were scheduled for ≥ 1 dental appointment. Of all first scheduled appointments, 83% were confirmed as attended. In total, 34,749 appointments were scheduled at nine public clinics and 25 private dental practices.

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Conclusions: HTHC dental care coordination successfully connected thousands of underserved children and youth with dental care, per program objective. However, additional, larger-scale programs are required for greater impact. Out of > 150,000 child and youth Medi-Cal beneficiaries countywide, only 47% attended a dental visit in 2019. Practical implications: Successful HTHC program elements can be adapted to other settings. Investments at larger scale and complementary actions to address other access barriers are needed to yield more dramatic increases in dental service utilization at the population level. Keywords: Dental care coordination, oral health, children, youth, underserved communities, dental care access

AUTHORS Benjamin W. Chaffee, DDS, MPH, PhD, is an associate professor of oral epidemiology and dental public health at the University of California, San Francisco, School of Dentistry. Conflict of Interest Disclosure: None reported. Jared I. Fine, DDS, MPH, is a dental public health consultant and former dental health administrator at the Alameda County Public Health Department. Conflict of Interest Disclosure: None reported. Yilak Fantaye, MPH, is with community assessment, planning and evaluation at the Alameda County Public Health Department. Conflict of Interest Disclosure: None reported. Kristin S. Hoeft, MPH, PhD, is an assistant professor of oral epidemiology and dental public health at the University of California, San Francisco, School of Dentistry. Conflict of Interest Disclosure: None reported.

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Rhodora Ursua, MPH, is the director of programs at the Alameda Health Consortium. Conflict of Interest Disclosure: None reported. Ray Stewart, DMD, MS, is professor and chair of the division of pediatric dentistry at the University of California, San Francisco, School of Dentistry. Conflict of Interest Disclosure: None reported. Suhaila Khan, MD, MPH, PhD, is the past project director of Healthy Teeth Healthy Communities of the Office of Dental Health, Alameda County Public Health Department. Conflict of Interest Disclosure: None reported

n 2016, the California Department of Health Care Services launched the Dental Transformation Initiative (DTI) under the Medi-Cal 2020 state Section 1115(a) Medicaid Waiver with the goal of improving dental health and access to dental care for California Medicaid (Medi-Cal) beneficiaries ages 0-20 years.1 State Medicaid demonstrations and waivers are federally authorized and allow states to test new strategies for health care service payment and delivery.2 The DTI was designed to respond to a history of underperforming oral health and dental utilization metrics among child and youth Medi-Cal Dental Program beneficiaries. In 2012, the California Dental Association released a landmark access report, “Phased Strategies for Reducing Barriers in Access to Care,” delineating the decades-long challenges in addressing access to care for the 1 in 3 California children eligible for Medi-Cal.3 In 2014, the California State Auditor’s Report revealed that in 2012-13, only 44% of eligible children and youth under age 20 had accessed the dental care to which they were entitled.4 By 2014, the restoration of adult dental benefits in Medi-Cal and the expansion of the Affordable Care Act witnessed a more than doubling of the

number of total Medi-Cal enrollees to > 12 million, nearly one-third of all Californians.5 These events placed even greater pressure on a dental provider network that the California State Auditor’s report had just shown to have not provided care for even half of eligible children. In 2015, the Legislature convened the Little Hoover Commission, which issued a critical report on the Medi-Cal Dental Program with a series of program and policy recommendations.6 Among the commission’s recommendations were setting a goal of 66% of children with Medi-Cal Dental coverage achieving an annual dental visit and the establishment of new pilot projects to increase access with the potential for expansion statewide. Within this setting, the DTI launched with four domains, the first three of which paid incentives to Medi-Cal Dental providers and featured the following goals: Increase delivery of preventive dental services (Domain 1); increase use of caries risk assessments to drive preventionfocused care (Domain 2); and increase patient continuity of care (Domain 3). Uniquely, Domain 4 created Local Dental Pilot Programs (LDPPs) allowing a California county, consortium of counties, tribe or University of

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California or California State University campus, among other entities, to address any of the goals of domains 1, 2 or 3 through alternative programs, such as innovative care models, delivery systems or workforce initiatives. Twelve LDPPs were supported under Domain 4. Some program elements common across the pilot programs were dental care coordination, virtual dental home services (in which allied dental personnel provide basic services in community settings with dentists connected via telehealth) and community outreach messaging.7 This paper focuses on the Alameda County Office of Dental Health’s LDPP, known as Healthy Teeth Healthy Communities (HTHC), as an exemplative case study of program successes, challenges and limitations to inform future dental health initiatives and policies. Described are outcomes of dental care coordination according to internally tracked outcome metrics, such as success in connecting clients with a dental appointment and appointment attendance. Alameda County is located in the East Bay region of the San Francisco Bay Area. Geographically, the county ranges from urban marinas to rolling open spaces, parklands and large urban and suburban communities. With over 1.6 million residents, Alameda is the seventh most populous county in California and has 14 incorporated cities and several unincorporated communities. Alameda County is characterized by rich diversity and culture, is home to the University of California Berkeley and 29 other colleges and is a center for the arts, music and international cuisine. Alameda County is one of the most racially/ethnically diverse regions in the San Francisco Bay Area and the nation.8

Approximately 6% of Alameda County residents fall below the federal poverty level (federal income threshold adjusted for family size), which is less than the statewide percentage (10%) but does not take costs of living into account.9

Healthy Teeth Healthy Communities

The Alameda County HTHC was a multicomponent, countywide program supported through the DTI and built upon existing community resources and infrastructure. Many HTHC components were first implemented as

One key aspect of the HTHC was its ability to leverage and/or forge partnerships with other local programs and organizations.

part of the Alameda County Healthy Kids Healthy Teeth program, which was limited to children ages 0-5 years at four partner Special Supplemental Nutrition Program for Women, Infants and Children sites. HTHC sought to expand and improve Healthy Kids Healthy Teeth initiatives. The primary aim of HTHC was to increase children’s access to dental services, particularly use of preventive service, via dental care coordination, as stated in its program goal and objective (below). The HTHC goals: To increase access to and utilization of dental care services emphasizing prevention for child and youth Medi-Cal beneficiaries (ages 0-20 years) in Alameda County. By the end of the project period, 15,000 children will utilize

dental care. This will be achieved by creating and implementing a new model of countywide dental care coordination in Alameda County.

HTHC Key Components

Three key components of the HTHC program included: ■ Establishing a linguistically and culturally diverse workforce of community dental care coordinators to strengthen connections between families and dental providers. ■ Offering active outreach, education, technical assistance, consultation and a menu of incentives to local dentists working in federally qualified health centers (FQHCs), community clinics and private practices to enhance their capacity for providing dental services emphasizing prevention to MediCal Dental beneficiaries ages 0-20. ■ Creating a web-based data management system to support care coordination, data tracking, evaluation and quality improvement. This paper describes each of these key components, assesses client-level outcome measures, such as dental service utilization, and discusses achievements, challenges and lessons learned from the HTHC program.

Collaborations and Partnerships

One key aspect of the HTHC was its ability to leverage and/or forge partnerships with other local programs and organizations. These linkages included public-private entities, dentalmedical-behavioral providers and academia. The 41 contracted HTHC partners included 17 large agencies and 24 private dental practices (In addition, one of the participating private dental offices did not contract with the project). M ARC H 2 0 2 2

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The Alameda County Public Health Department had longtime relationships with most of the agency partners.

Healthy Teeth Healthy Communities: Program Components Dental Care Coordination

At the core of the Alameda County Dental Health Care Coordination system is the dental care coordinator workforce and the dental providers. The dental care coordinators are the bridge that connects the dental providers and clients. A working dental care coordination model relies on active data collection, analysis and utilization as well as continuous quality assurance through communication and partnerships/collaborations between program leadership and clinical and community partners. The HTHC model follows dental public health principles. It aims to reduce access barriers (as mentioned in the Little Hoover Commission report) to increase dental care utilization by Medi-Cal beneficiaries. Although this model was developed for families with children or youth ages 0-20 years, dental care coordination has the potential to be adapted for other target populations (e.g., adults, seniors, children with special needs, pregnant women or people with unstable housing). As operationalized in HTHC, dental care coordination required creating a workforce at the community level. The individuals carrying out care coordination were called the community dental care coordinators (CDCCs). The CDCCs’ role is to connect patients, providers and systems. A CDCC is a community health worker, field staff or similar paraprofessional with some specific prerequisite skills, knowledge and experience related to interpersonal communications and working with public health agencies. Any community health worker with these attributes can be trained in dental care coordination; 150

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dental knowledge is not a prerequisite. CDCCs primarily helped clients to make dental appointments at service locations convenient for their clients, including locations that had agreed to hold appointment slots open for HTHC referrals. CDCCs were empowered to engage with families who were already existing clients of partnering agencies and health centers (known as “in-reach”) as well as outreach in the community to both individuals and groups. These initial contacts afforded the opportunity to provide motivational information, stress the importance of early

Improving skills and self-efficacy in providing preventive dental services to young children was a key COP goal.

preventive dental care and emphasize the value of home hygiene practices and health-promoting dietary practices. Once an initial dental appointment was made by a CDCC, follow-up support was provided with appointment keeping, such as reminder calls. This included ongoing liaising with the dental service location to support continuity of ongoing dental care. In order to maximize their successful engagement with the beneficiary population, the HTHC CDCCs were recruited as a cross-agency workforce, linguistically and culturally reflective of the community. Twenty-six dental care coordinators from 14 agencies (two county programs, eight FQHCs, two community health centers of which one had a dental clinic and two community-based organizations) were

hired and trained. Care coordination sites reflected a leveraging of existing infrastructures for community and patient outreach. The majority (69%) of the CDCCs identified as female, and seven had prior experience working as a dental assistant. As a group, the CDCCs spoke 10 languages fluently: Bengali, Chinese-Cantonese, Chinese-Mandarin, English, Farsi, Korean, Portuguese, Spanish, Tagalog and Vietnamese.

Dental Provider Outreach, Incentivization and Community of Practice

The Community of Practice (COP) was created to address provider-related barriers to access to care for MediCal beneficiaries. The members of this dentist network were supported, trained and mentored to recognize the importance of equitable access to care and overcome the barriers to adequate services often experienced by Medi-Cal beneficiaries. This network recruited 169 dentists (136 from eight FQHCs, two from one community health center and 31 from 25 private dental practices). Most COP members were general dentists who provided care for children but had varying levels of comfort and training in pediatric dentistry. Thus, improving skills and self-efficacy in providing preventive dental services to young children was a key COP goal. Dental provider outreach, incentivization and recruitment were designed to address potential provider concerns related to working with underserved children. Recruitment began with a mailed invitation to all licensed Alameda County dentists to attend the inaugural convening. That inaugural meeting covered the goals of the DTI, the specific goals and objectives of the HTHC pilot and the incentives available to participating dentists. In addition

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to statewide Medi-Cal Dental rate increases specially designed to reward increased numbers of preventive services and continuity of care, HTHC would also directly reimburse private-practice providers for family oral health education (FOHE) for families with young children (for private-practice providers: $20 per visit, up to two visits per year). FOHE consisted of a brief counseling with parents of children ages 0-5 years, emphasizing home oral hygiene practices and healthy dietary behaviors. FQHC providers were also encouraged to deliver FOHE but without monetary incentives. COP member dentists were assigned one or more CDCC to support families in navigating their way to dental appointments. While the HTHC program prioritized care for young children, member dentists could determine the number and ages of children for whom they would make appointments available. Over three years, the COP offered 14 continuing dental education (C.E.) courses at no cost, mostly led by faculty from the University of California, San Francisco, School of Dentistry. C.E. topics focused on increasing the confidence and competence of dentists to serve young children. COP dentists were overwhelmingly general practitioners. Thus, 17 pediatric dentistry specialists were recruited to serve as mentors to COP members, offering support on treatment planning and accepting referrals of complex cases. C.E. courses were offered quarterly and served as a tangible benefit to COP member dentists. The COP strove to become “a learning community of dentists.” Beyond the C.E. courses, COP gatherings were an opportunity to bring together dental professionals who shared a commitment to providing care to Medi-Cal-enrolled children and youth

with the greatest need and, often, the most barriers to accessing the services to which they were entitled. Some individual COP dentists convened with HTHC staff to delineate programmatic and contractual details, including the role of the CDCC, scheduling appointments, use of dental encounter forms and invoicing. Frequently, it was in these person-to-person meetings and regular visits by CDCCs where any difficulties in working with the HTHC pilot or Medi-Cal administrative requirements were addressed.

C.E. courses were offered quarterly and served as a tangible benefit to COP member dentists.

Dental Care Coordination Management System

The care coordination management system (CCMS) is a web-based, HIPPAcompliant data hub, linking the various CDCC employers, dental care service providers and other HTHC participating organizations. The CCMS uses an innovative, structured data approach, similar to coding systems, such as CDT and ICD-10, to document care coordination activities. The CCMS allows dental care coordination data aggregation across multiple providers to deliver a broad picture at both the individual patient and the population level. The user interface is readily navigated and allows for client enrollment and appointment tracking (both scheduling and recording appointment outcomes). The CCMS database enabled

the 26 CDCCs to simultaneously enter and use data. HTHC project performance was monitored with the data from the CCMS database, and relevant feedback was given to the partners monthly and quarterly. The CCMS was designed specifically for HTHC and is not widely available as commercial software as of this writing.

Data Sources Alameda County Dental Care Coordination

Data from the HTHC care coordination management system, covering clients who were enrolled in dental care coordination from Jan. 1, 2018, through Dec. 31, 2020, are presented as descriptive counts and percentages. After describing the client population, two main outcome metrics were calculated: 1) dental appointment scheduling (of all unique children enrolled in care coordination, how many were scheduled for ≥ 1 dental appointments); and 2) scheduled dental appointment outcomes (of all children with a scheduled appointment, how many of those appointments were confirmed as kept).

Publicly Available State and County Data

For this case study, measures of Medi-Cal Dental service utilization in Alameda County and California were calculated from publicly available reports posted at the California Health and Human Services Open Data Portal.10

Dental Access: Quantitative Results HTHC Care Coordination

Over three years (2018 to 2020), 8,609 children and youth (ages 0-20 years) who received care coordination through HTHC successfully attended ≥ 1 dental appointments. These young people represented the majority (72%) of the 11,930 unique child clients the HTHC dental care coordination program enrolled M ARC H 2 0 2 2

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TABLE 1

Characteristics of Children Enrolled in Healthy Teeth Healthy Communities Care Coordination Program, 2018-2020 Number of Clients

Percent of Total

0–5 years

5,726

48.0

6–11 years

3,412

28.6

12–17 years

2,278

19.1

≥ 18 years

514

4.3

Female

5,558

50.6

Male

5,421

49.4

No data*

951

Age group

Gender

Race/ethnicity Hispanic or Latino

6,444

54.0

Asian Pacific Islander

2,015

16.9

African American or Black

1,638

13.7

White

436

3.7

American Indian or Alaska Native

157

1.3

Other, including unknown

1,240

10.4

9,700

81.7

Within the past 12 months

2,167

18.3

No data*

Most recent dental visit Never or > 12 months ago

Urgency of treatment needs** Nonurgent

11,194

94.0

Urgent–Class 3

604

5.1

Urgent–Class 4

115

1.0

No data*

Referred to dental appointment At public clinic or FQHC

6,092

51.3

At private practice

4,257

35.8

No appointment made

1,534

12.9

No data*

* Missing values excluded from percentage calculations. ** As assessed by care coordinator based on clients’ reported symptoms; Class 3 indicates a dental condition expected to lead to an emergency within 12 months; Class 4 is the highest level of urgency and indicates the need for a dental visit as soon as feasible. FQHC: Federally qualified health center

during this time period. Nearly half the enrolled clients (48%) were age 5 or younger and 82% had not visited a dentist in the 12 months preceding program enrollment (TA BLE 1), demonstrating a programmatic emphasis on increasing access for young children. 152

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While some clients presented with urgent dental treatment needs, the vast majority (94%) did not, suggesting an opportunity for early preventive care. More than half of clients (54%) identified as Hispanic or Latino (TA BLE 1 ).

Of all HTHC clients, 87% were scheduled for ≥ 1 dental appointments via care coordination (TA BLE 2 ). Most who were connected with a dental appointment were scheduled at an FQHC or public clinic (TA BLE 1 ). Appointments were made at dental service locations throughout Alameda County (including clinics with multiple sites). From 2018-2020, of 34,749 scheduled appointments (including multiple appointments per child), 23,090 were scheduled at nine public clinics (eight FQHCs and one community health center) and 11,659 were scheduled at 25 private dental practices. First-appointment scheduling success exceeded 80% in all demographic groups assessed, with the exception of clients aged ≥ 18 years, among whom only 66% were scheduled for a dental appointment. Despite widespread success, some racial/ ethnic disparities persisted (TA BLE 2 ). For example, clients identified as Asian Pacific Islander were more likely to be scheduled for a dental appointment (93%) than clients identified as African American or Black (80%). While client volume decreased substantially in 2020 during the COVID-19 pandemic, the percentage of clients scheduled for a dental appointment remained high (TA BLE 2 ). Most HTHC-scheduled dental appointments resulted in a successful dental encounter on the date of the appointment (TA BLE 3 ). HTHC care coordinators were able to record the dental appointment outcome (kept, no show or rescheduled) for 99% of all first dental appointments made for HTHC clients, and 83% of those appointments were kept. While success in keeping dental appointments was high in all demographic groups examined, some disparities emerged. Similar to appointment scheduling, clients identified as Asian Pacific

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TABLE 2

Care Coordination Appointment Scheduling by Child Characteristics

Islander were more likely to keep their first dental appointment (90%) than clients identified as African American or Black (74%). Clients appointed at a public clinic or FQHC were more likely to keep their first appointment as scheduled (91%) than clients appointed at a private-practice location (72%), with fewer no-show, reschedule and unknown outcomes (TA BLE 3 ). Children categorized with the highest urgency of treatment needs were more likely to keep their scheduled appointment (94%) than children with less urgent needs (TA BLE 3 ). Of the 10,396 clients scheduled for a first dental appointment, most (74%) were scheduled for a subsequent appointment, either for continued treatment or a routine recall visit. Success in keeping a scheduled visit was somewhat diminished for subsequent appointments: 70% of all follow-up appointments were confirmed as kept, with a greater percentage of no-show (21%), reschedule (5%) and unknown (4%) outcomes than for first appointments.

State and County Trends

According to publicly available California state data, > 150,000 children and youth ages 0-20 years were eligible for Medicaid benefits in Alameda County in 2019 (TA BLE 4 ), more than 1 in 3 children and youth in the county. Of eligible beneficiaries, 47% had at least one dental service provided, slightly below the statewide dental service utilization percentage (50%) for this age group (TA BLE 4 ). Both statewide and in Alameda County overall, utilization differed by age and race/ethnicity (TA BLE 4 ). Children ages 3-14 years were more likely to receive dental services than younger or older children. Racial/ethnic differences in Alameda County mirrored those in the state, with utilization highest among children identifying as Asian or Hispanic/

Number of Clients

Percent With Dental Appointment*

11,930

87.1

0–5 years

5,726

89.3

6–11 years

3,412

87.0

12–17 years

2,278

86.5

≥ 18 years

514

66.1

All clients

p-value** < 0.001

Age group

0.384

Gender Female

5,558

87.7

Male

5,421

87.2 < 0.001

Race/ethnicity Hispanic or Latino

6,444

87.7

Asian Pacific Islander

2,015

93.0

African American or Black

1,638

80.0

White

436

86.7

American Indian or Alaska Native

157

86.0

Other, including unknown

1,240

84.6 < 0.001

Most recent dental visit Never or > 12 months ago

9,700

88.3

Within the past 12 months

2,167

84.2

Nonurgent

11,194

87.0

Urgent–Class 3

604

91.1

Urgent–Class 4

115

93.9

0.001

Urgency of treatment needs***

< 0.001

Program enrollment year 2018

4,817

92.1

2019

5,316

83.0

2020

1,797

86.1

* Defined as having ≥ 1 dental appointments scheduled on the client’s behalf via care coordination. ** Chi-square test *** As assessed by care coordinator based on clients’ reported symptoms; Class 3 indicates a dental condition expected to lead to an emergency within 12 months; Class 4 is the highest level of urgency and indicates the need for a dental visit as soon as feasible.

Latino and lower among children identifying as Black or white. Dental service utilization among Alameda County Medicaid-eligible children followed statewide trends from 2013-2019 (FIGURE 1 ). Alameda County utilization matched statewide utilization among children ages 0-5 years but trailed by a few percentage points among older

children (FIGURE 1 ). Compared to years 2013-2016, both statewide and countywide dental utilization was higher following DTI implementation in 2017; however, increased utilization in 2019 likely reflects the inclusion of fluoride varnish applications in medical settings, which was not counted as a dental service in utilization calculations for M ARC H 2 0 2 1

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TABLE 3

Scheduled Dental Appointment Outcomes by Child Characteristics Appointment Outcome* (percent)

All appointed clients

Number of clients

Kept

No show

Rescheduled

Unknown

10,396

82.8

13.7

2.4

1.1 < 0.001

Age group 0–5 years

5,116

82.0

14.2

2.9

0.9

6–11 years

2,970

84.6

12.1

1.9

1.4

12–17 years

1,970

82.8

14.1

1.9

1.2

≥ 18 years

340

78.8

17.4

1.8

2.1 0.367

Gender Female

4,876

83.9

12.7

2.3

1.2

Male

4,726

82.9

13.1

2.8

1.2

5,650

83.0

13.9

2.0

1.1

Asian Pacific Islander

1,873

90.5

7.4

1.7

0.5

African American or Black

1,311

73.6

20.7

4.3

1.4

< 0.001

Race/ethnicity Hispanic or Latino

p-value**

White

378

80.7

14.0

4.8

0.5

American Indian or Alaska Native

135

83.0

14.1

3.0

0.0

Other, including unknown

1,049

80.0

15.3

2.5

2.2

Never or > 12 months ago

8,564

82.7

13.9

2.3

1.1

Within the past 12 months

1,824

83.6

12.8

2.7

0.9

0.284

Most recent dental visit

< 0.001

Urgency of treatment needs*** Nonurgent

9,738

82.9

13.7

2.5

1.0

Urgent–Class 3

550

79.6

15.8

0.7

3.8

Urgent–Class 4

108

94.4

5.6

0.0

0.0 < 0.001

Referred to dental appointment At public clinic or FQHC

6,092

90.5

8.1

0.8

0.6

At private practice

4,257

71.8

21.7

4.6

1.9 < 0.001

Appointment year 2018

4,394

83.7

15.5

0.4

2019

4,317

83.7

13.1

2.8

0.5

2020

1,680

78.2

10.8

6.4

4.6

* Includes first dental appointments (i.e., one appointment per client) with scheduled dates from 2018 through 2020; outcomes as recorded by the care coordinator. ** Chi-square test *** As assessed by care coordinator based on clients’ reported symptoms; Class 3 indicates a dental condition expected to lead to an emergency within 12 months; Class 4 is the highest level of urgency and indicates the need for a dental visit as soon as feasible.

years 2013-2018. Thus, increases cannot necessarily be attributed to the DTI.

Discussion

Over a three-year period, the dental care coordination component of 154

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the Alameda Healthy Teeth Healthy Communities program successfully connected more than 8,000 children and youth with dental services by overcoming system navigation barriers via linguistically and culturally sensitive

support, motivation and anticipatory guidance from CDCCs. Not only were clients scheduled for dental appointments, but with prompting and assistance from CDCCs, the vast majority of appointments were attended as scheduled, benefiting

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TABLE 4

California and Alameda County Dental Service Utilization, Medicaid Eligible Children, 2019

patients and dental providers alike. Care coordination was especially successful for younger children (ages < 5 years) and for those connected with care at FQHCs or other public clinics. This focus on younger children, especially those without a prior dental visit, suggests that the program was able to direct children for preventive care before more serious dental problems developed. While care coordinators served as a bridge between patients and dental providers, the overall HTHC program also strengthened collaboration between the Alameda County Office of Dental Health, dental care providers and organizations and other local partners, all of whom shared information and resources to build the HTHC program. To date, care coordination in dentistry has generally been more limited than analogous efforts in medicine, with many existing dental care coordination programs focused on increasing dental care access for specific vulnerable populations, such as persons living with HIV/AIDS11,12 or patients with disabilities.13 The American Dental Association supports care coordination as a solution to access-to-care barriers, launching its own Community Dental Health Coordinator program in 2006.14 In a large multispecialty group dental practice in the Pacific Northwest, existing office staff were recently “upskilled” to dental care coordinators to improve patient attendance and strengthen connections between providers and patients.15 Under strong managerial support, the new role was largely viewed positively within the organization, but long-term outcomes are yet to be evaluated.15 Among care coordination programs aiming to enhance dental utilization among Medicaid-eligible children, a retrospective analysis of patient records from one urban pediatric dentistry clinic reported only modest improvements in appointment attendance, although

California Statewide*

Alameda County

N**

Utilization†

N**

Utilization†

5,519,097

50.0%

155,353

47.3%

0–1 years

190,723

4.9%

5,077

2.9%

1–2 years

514,382

32.7%

14,569

35.7%

All beneficiaries (ages 0-20 years) Age

3–5 years

821,102

55.8%

22,810

53.5%

6–9 years

1,090,999

62.5%

30,421

59.2%

10–14 years

1,419,735

56.9%

39,581

53.5%

15–18 years

1,039,477

47.6%

29,582

43.3%

19–20 years

442,679

31.5%

13,313

29.1%

18,351

45.7%

256

45.3%

Race/ethnicity‡ American Indian or Alaska Native Asian

243,609

55.1%

17,942

58.1%

African American or Black

392,869

40.7%

26,478

41.0%

Hispanic or Latino

3,291,919

55.2%

66,432

53.6%

Native Hawaiian or Pacific Islander

119,904

44.5%

5,813

44.7%

White

758,508

41.4%

9,199

34.1%

Other, including unknown

693,937

39.2%

26,240

38.8%

* California totals include Alameda County. ** Number of full-scope Medi-Cal (Medicaid) members (beneficiaries) with no share of cost and with at least three months of continuous enrollment in the same plan in calendar year 2019. † Percentage of beneficiaries receiving at least one dental service through the Medi-Cal Dental Program in calendar year 2019; includes any Code on Dental Procedures and Nomenclature (CDT Codes) D0100 - D9999, Safety Net Clinic Dental Encounter and/or fluoride varnish, caries risk assessment and dental referral in a medical setting (Current Procedural Terminology code 99188). ‡ Race/ethnicity-specific calculations for Alameda County exclude N = 2,993 (total) beneficiaries due to small cell sizes that prevented reporting of age and race/ethnicity-specific metrics in publicly posted datasets. Data source: California Health and Human Services Open Data Portal.

care coordination primarily consisted of appointment-reminder telephone calls.16 A dental care coordination intervention trial featuring case managers in Louisville, Kentucky, also reported improvements in dental appointment access, but the number of patients involved was small.17 On a somewhat larger scale, a dental care coordination pilot project in New York successfully recruited dental providers and clients, leading to substantial countywide increases in dental utilization by Medicaid eligible beneficiaries in the one small rural county where the program focused.18 To our knowledge,

there are no existing reports describing a public health agency-driven dental care coordination program in as populous or diverse a setting as Alameda County. A unique aspect of HTHC care coordination was an electronic data management system that allowed opportunities for near real-time data monitoring, evaluation and program improvement. Undoubtably valuable, there were drawbacks to conducting care coordination through a single electronic platform. Learning the system required dedicated training time, and assuring highquality data required frequent centralized M ARC H 2 0 2 1

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Utilization of Any Dental Service Among Medi-Cal Members, California and Alameda County, by Age, 2013-2019 45%

40%

California 38.1%

Alameda County

37.5%

41.7%

37.0%

38.1%

38.0%

37.4%

37.3%

41.4%

35.7%

35% 35.1%

34.8%

35.0%

34.8% Ages 0-5 years

30% 2013

2014

California

2015

2016

50%

54.2%

57.6%

57.9%

55.2%

54.7%

2019

59.3%

55.1% 56.0%

52.8%

2013

45%

2018

Alameda County

60%

55%

2017

53.8%

53.4% 51.6% 2014

California

2015

Ages 6-14 years

50.9% 2016

2017

38.8%

35%

37.3%

37.6%

37.0%

2018

2019 42.8%

Alameda County 40.2%

40%

54.0%

41.3%

37.3% 38.9% 36.7%

35.0%

34.1%

33.7%

2015

2016

Ages 15-20 years

30% 2013

2014

37.5%

2017

2018

2019

FIGURE 1. Percentages reflect utilization of any dental service within the calendar year. Denominator is the number of full-scope Medi-Cal (California’s Medicaid program) beneficiaries with no share of cost and with at least three months of continuous eligibility in the same plan. Numerator is the number of beneficiaries with at least one dental visit, including any Code on Dental Procedures and Nomenclature (CDT codes) D0100 - D9999 or Safety Net Clinic Dental encounter. In 2019 only, the numerator also includes fluoride varnish, caries risk assessment and dental referral in a medical setting (Current Procedural Terminology code 99188). California percentages include Alameda County. Data source: California Health and Human Services Open Data Portal. data.chhs.ca.gov.

monitoring. Data entry was a timeconsuming responsibility for CDCCs, who often balanced additional job duties. The CCMS system was custom designed for HTHC, making transfer to other settings more challenging. HTHC care coordination was particularly effective with young 156

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children and at well-established FQHCs. Encouragingly, participating private practices also accounted for a sizable portion of patient appointments. Appointments were more likely to be kept at public clinics than private practices, on average, but there was considerable variation across individual sites.

Speculatively, the fact that many FQHC appointments were for clients identified via in-reach (for example, patients who had received medical, but not dental, care from the same FQHC site and were thus familiar with the clinic and setting) may have contributed to better appointment success. While the Little Hoover Commission recommended that California counties steer more Medi-Cal-eligible patients to FQHCs with capacity to treat them,6 greater involvement from private practices may be essential to reach utilization goals when FQHCs are at or near their capacity limits. Alameda County is home to multiple FQHCS with ample capacity to provide dental services; a greater role for private practices might be needed in other settings. In HTHC, provider incentives made available through the Community of Practice may have played a role in bringing private providers into the program. Nonetheless, the total number of private practices that agreed to accept HTHC appointments was only a fraction of all practices throughout the county. Despite impressive utilization metrics overall, access disparities within the HTHC enrollee population mirrored those observed at the county and state level, particularly for Black children and youth. Should HTHC or similar programs continue, a greater level of outreach and involvement of Black communities, along with greater representation among CDCCs and dental providers, is strongly recommended. Positively, HTHC was highly successful in enrolling young children. Whereas children ages 0-5 make up slightly more than 27% of Medi-Cal beneficiaries in Alameda County, this age group comprised nearly half (48%) of HTHC enrollees. Connecting young children with a dental home early in life, before dental caries necessitates more costly and invasive treatment, is a critical

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component of prevention-focused dental care, especially for high-risk children.19 Children with existing urgent treatment needs comprised a small portion of the HTHC client population. These children, particularly urgent Class 4, may experience oral pain or infection. Notably, these children were the most likely to be connected with (and keep) a dental appointment, indicating both programmatic success and, potentially, heightened caregiver motivation. As with nearly all health systems worldwide, the COVID-19 pandemic severely disrupted the HTHC program. The volume of HTHC referrals dropped substantially in 2020, especially in the spring months when most dental service locations were closed to all but emergency care. Serious concerns remain about families forgoing, postponing or being unable to access needed dental care. One innovative approach to lessen pandemic-related access barriers in Alameda County was the launching of a drive-through dental clinic at one FQHC.20 Multiple service locations turned to teledentistry visits to reach their patients during the pandemic, potentially accelerating widespread uptake of this technology, which could lead to long-term access improvements.21 During the pandemic, the HTHC COP maintained ongoing opportunities for interaction and continuing education through quarterly sessions conducted over a virtual meeting platform. The HTHC program connected more than 8,000 children and youth with dental appointments, many of whom reported not having visited a dentist in the prior 12 months. HTHC was internally successful in achieving very high percentages of appointment scheduling and attendance among its clients. However, when looking at Alameda County as a whole, the overall percentage of Alameda County

Medi-Cal beneficiaries ages 0-20 years with a dental appointment in 2019 (the most recent data available) was not meaningfully improved from prior years relative to the analogous percentage statewide. While HTHC achieved success among the children it reached, given resource constraints, the capacity of the HTHC dental care coordination program was at least an order of magnitude smaller than the number of child and youth Medi-Cal beneficiaries in the county. Thus, driving meaningful changes in dental utilization at the county and

As with nearly all health systems worldwide, the COVID-19 pandemic severely disrupted the HTHC program.

state levels will require much greater investment of resources than was available for local pilot projects through the DTI. Among limitations in evaluating the HTHC program is the lack of an experimental design. For practical and ethical reasons, there was no noncare coordination control group, limiting the ability to draw conclusions about program effectiveness. Also, HTHC was designed with multiple components, including dental provider education and incentivization. Untangling the specific contributions of each component to any access to care improvements was not possible.

Conclusions

The Alameda County Healthy Teeth Healthy Communities program, developed under the California Dental

Transformation Initiative, successfully utilized dental care coordination and a network of support for local dental providers to connect underserved children with access to dental care. The ability of dental care coordination and other program components to address potential access barriers at the patient, provider and system levels all plausibly contributed to programmatic success. Investments at larger scale and complementary actions to address other potential access barriers are recommended to yield more dramatic increases in dental service utilization at the population level. n AC KN OW L E DG M E N T Heathy Teeth Healthy Communities is a project (Domain 4) of the Local Dental Pilot Program (LDPP) under the Dental Transformation Initiative (DTI), funded by the California Department of Health Care Services (DHCS). The authors thank the leadership of Alameda County for their constant support for this project: Colleen Chawla, director, health care service agency, Kimi Watkins-Tartt, director, public health department, and Quamrun Eldridge, director, community health services division. They also thank Arash Aslami, Office of Dental Health, Alameda County Public Health Department, for support and administration of the Heathy Teeth Healthy Communities Project. RE F E RE N C E S 1. California Department of Health Care Services. Dental Transformation Initiative. Accessed June 10, 2021. 2. Medicaid.gov. State Waivers List. Accessed June 10, 2021. 3. California Dental Association. Access Report Phased Strategies for Reducing the Barriers to Dental Care in California. Accessed June 10, 2021. 4. California State Auditor. California Department of Health Care Services. Weaknesses in its Medi‐Cal Dental Program limit children’s access to dental care. Report 2013–125. 2014. Accessed June 10, 2021. 5. California Department of Health Care Services. Medi-Cal Statistical Brief. Medi-Cal’s Historic Period of Growth. August 2015. Accessed June 10, 2021. 6. Little Hoover Commission. Fixing Denti-Cal. Report 230. April 2016. Accessed June 10, 2021. 7. Children Now and Sacramento County Public Health. Dental Care Coordination and Access to Care. (unpublished report). 2020. 8. Alameda County California. About Us. Accessed June 10, 2021. 9. Healthy Alameda County. Community Health Dashboards. Accessed October 21, 2021. 10. California Health and Human Services Open Data Portal. Accessed June 10, 2021. 11. Lemay CA, Cashman SB, McDonald A, Graves JR. A new approach to ensuring oral health care for people living M ARC H 2 0 2 2

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with HIV/AIDS: The dental case manager. Prev Chronic Dis 2012;9:E158. doi: 10.5888/pcd9.110297. 12. Metsch LR, Pereyra M, Messinger S, et al. Effects of a brief case management intervention linking people with HIV to oral health care: Project SMILE. Am J Public Health 2015 Jan;105(1):77–84. doi: 10.2105/AJPH.2014.301871. PMCID: PMC4265910. 13. Gondlach C, Catteau C, Hennequin M, Faulks D. Evaluation of a care coordination initiative in improving access to dental care for persons with disability. Int J Environ Res Public Health 2019 Aug 1;16(15):2753. doi: 10.3390/ ijerph16152753. 14. American Dental Association Solutions: About CDHCs. Accessed June 10, 2021. 15. Kottek AM, Hoeft KS, White JM, Simmons K, Mertz EA. Implementing care coordination in a large dental care organization in the United States by upskilling front office personnel. Hum Resour Health 2021;19(1):48. doi. org/10.1186/s12960-021-00593-0. 16. Casaverde NB, Douglass JM. The effect of care coordination on pediatric dental patient attendance. J Dent Child (Chic) May–Aug 2007;74(2):124–9. 17. Binkley CJ, Garrett B, Johnson KW. Increasing

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dental care utilization by Medicaid-eligible children: A dental care coordinator intervention. J Public Health Dent Winter 2010;70(1):76–84. doi: 10.1111/j.17527325.2009.00146.x. PMCID: PMC4060152. 18. Greenberg BJ, Kumar JV, Stevenson H. Dental case management: Increasing access to oral health care for families and children with low incomes. J Am Dent Assoc 2008 Aug;139(8):1114–21. doi: 10.14219/jada. archive.2008.0314. 19. Hale KJ. Oral health risk assessment timing and establishment of the dental home. Pediatrics 2003 May;111 (5 Pt 1):1113–6. doi: 10.1542/peds.111.5.1113. 20. Miyahara K. Asian Health Services “Clinic Drive-Thru” for the Kindergarten Oral Health Assessment and Fluoride Varnish Program. 2020. Accessed June 25, 2021. 21. Ghai S. Teledentistry during COVID-19 pandemic. Diabetes Metab Syndr Sep–Oct 2020;14(5):933–935. doi: 10.1016/j.dsx.2020.06.029. Epub 2020 Jun 16. TH E CO RRE S P ON DIN G AU T HOR , Benjamin W. Chaffee, DDS, MPH, PhD, can be reached at Benjamin.Chaffee@ucsf.edu.

January 1, 2022: Electronic Prescriptions R for All Medication

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C.E. Credit

A Mandibular Adenomatoid Odontogenic Tumor With a Novel Treatment Utilizing Platelet-Rich Fibrin Tarun Mundluru, DDS, MSc; David Pilgrim, DDS; Reyes Enciso, PhD; Parish P. Sedghizadeh, DDS, MS; and Mohammad A. Khalifeh, DDS, MS

abstract Background: Adenomatoid odontogenic tumor (AOT) is an uncommon odontogenic tumor that originates from odontogenic epithelium. It is predominantly found in young women, particularly in the maxilla in association with an unerupted permanent tooth. Case description: This is a case report of an AOT in a 60-year-old male with an asymptomatic mandibular lesion that radiographically presented as a mixed lesion. Conclusions: Enucleation was performed and the defect was treated with bone grafting and platelet-rich fibrin with no recurrence at follow-up. Keywords: Adenomatoid odontogenic tumor, platelet-rich fibrin, bone graft, mandibular lesion

AUTHORS Tarun Mundluru, DDS, MSc, is a graduate of the orofacial pain and oral medicine advanced specialty program at the Herman Ostrow School of Dentistry of USC. He practices in Pecos, Texas. Conflict of Interest Disclosure: None reported. David Pilgrim, DDS, is a graduate of the advanced graduate program, Master of Science program in orofacial pain and oral medicine at the Herman

Ostrow School of Dentistry of USC. He is a dental surgeon in Barbados. Conflict of Interest Disclosure: None reported. Reyes Enciso, PhD, is an associate professor in the department of geriatrics, special needs and behavioral sciences at the Herman Ostrow School of Dentistry of USC. Conflict of Interest Disclosure: None reported.

Parish P. Sedghizadeh, DDS, MS, is an associate professor in the clinical dentistry division of periodontology, diagnostic sciences and dental hygiene at the Herman Ostrow School of Dentistry of USC. Conflict of Interest Disclosure: None reported.

Mohammad A. Khalifeh, DDS, MS, is an adjunct instructor of clinical dentistry in the division of periodontology, diagnostic sciences and dental hygiene at the Herman Ostrow School of Dentistry of USC. Conflict of Interest Disclosure: None reported.

he adenomatoid odontogenic tumor (AOT) has been categorized by the World Health Organization (WHO) as a benign odontogenic tumor of epithelial origin even though there is admission that this lesion has always been difficult to classify.1 The nomenclature of this lesion has changed several times over its history, and the term AOT was accepted by the WHO in 1971. This tumor has also been dubbed the “tumor of two-thirds,” because about two-thirds of the cases occur in females, two-thirds of the cases occur in the second to third decade of life, two-thirds of the cases M ARC H 2 0 2 2

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FIGURE S 1. Clinical image shows a mandibular expansile lesion with tooth displacement (1A). Axial CT slice of a mixed lesion of the right mandible with cortical expansion and thinning (1B). Intraoperative view of the enucleated lesion to healthy bleeding bone (1C). Placement of PRF into the defect prior to bone graft placement (1D). Clinical image shows healing of the surgical site after six months (1E). Panoramic film six months postoperatively shows bone fill in the area and no signs of recurrence (1F).

occur in the anterior maxilla and twothirds of the cases occur in association with an unerupted permanent canine.2 AOT has been described as having three variant types,3 a follicular type, an extrafollicular type and a peripheral variant. The follicular variant has been described as being associated with the crown of an unerupted tooth, usually a canine. The extrafollicular type has no direct tooth association, while the peripheral variant occurs in gingival tissues.4 Recurrence of AOT has been found to be rare,5 and conservative treatment options of curettage or enucleation are implemented even though cases treated with marginal and segmental resection have also been reported. We present a case of AOT in a 60-year-old male. The tumor created a large and expansile defect in the mandible, which can be challenging to surgically manage and reconstruct given the amount of bone destruction, less than ideal blood supply and potential for tumor recurrence without adequate excision. The tumor was treated by a novel technique involving enucleation with repair using xenograft bone mixed with injectable platelet-rich fibrin (I-PRF) and advanced platelet-rich fibrin (A-PRF). 160

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This graft type was implemented with the aim of improving the rate of healing and the quality of bone fill in the critical size defect. Experimental models have shown that cell-based tissue engineering with the use of PRF can augment new bone formation and thus can have direct positive effects on bone healing.6

Case Report

A 60-year-old male patient of African ethnicity presented to the Herman Ostrow School of Dentistry of USC with a referral from his dentist with concerns of a right mandibular swelling in the premolar area. The patient indicated that he had been observing this swelling for several years, and it had remained relatively constant in size for the past two years. The patient indicated no pain, discomfort or changes in sensation with respect to this swelling. His medical history was significant only for Type II diabetes mellitus, which was controlled with metformin. Clinical examination revealed a 3 x 3 cm, smooth, unifocal circumscribed swelling, with thin mucosa covering the buccal surface of dentoalveolar bone, extending from the right mandibular canine to the right mandibular first molar (FIGURE 1A ). Palpation of the

growth revealed a smooth surface with well-defined borders, and an eggshell consistency was appreciated on palpation and application of firm pressure; however, this pressure was not associated with pain or discomfort. Teeth associated with the swelling had pathological migration, and Grade 2 to Grade 3 mobility of right mandibular incisors and canine was recorded. Vitality testing on the teeth associated with or adjacent to the lesion was performed, and these teeth were found to be normally responsive to cold stimulus similar to healthy control teeth tested in other quadrants. The lesion was subjected to panoramic radiography and CT imaging without intravenous contrast (FIGURE 1B ). CT report findings indicated a large cystic lesion of the right mandible with multiple internal calcifications, thinning of the buccal and lingual cortical plates of bone with perforation of the buccal plate. Based on these findings, an incisional biopsy was recommended to the patient. The working differential diagnosis based on clinical and radiographic findings at this point included central odontogenic fibroma, calcifying odontogenic cyst, ossifying fibroma, calcifying epithelial odontogenic tumor and AOT. An incisional biopsy on which histopathology was performed followed (FIGURE 2 ). The subsequent pathology report indicated the lesion was consistent with an AOT (ICD-10 No. D16.5). Microscopic findings indicated a wellcircumscribed proliferation of duct-like epithelium surrounding small foci of mineralization with various architecture including rosettes, trabeculae and cribriform patterns. Polyhedral, spindled and columnar type cells with basal nuclei and clear cytoplasm were noted. Given the diagnosis of AOT, enucleation of the lesion was carried out under local

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anesthesia, and the right mandibular lateral incisor and canine were also extracted (FIGURES 1C and 1D ). Care was taken not to perforate the lingual plate, and the inferior alveolar/mental nerve was identified and preserved throughout the procedure. The bony defect created by the enucleation was repaired with the use of a combination of bone graft (which utilized xenograft bone, A-PRF and I-PRF membranes) and tension- free closure obtained using interrupted polyglycolic acid 4.0 sutures. For this patient, the PRF fractions were produced by using blood taken from the patient’s left antecubital vein and centrifuged using the Choukroun DUO Quattro system. A-PRF was made under protocol of 1300 RPM spin for eight minutes in silica-coated tubes and I-PRF with 700 RPM spin for four minutes in noncoated tubes. The enucleated bony site was then filled and repaired with a mixture of 0.5 grams of xenograft bone (Bio-Oss, Geistlich Pharma North America, Princeton, N.J.) and I-PRF and membranes of A-PRF (FIGURES 3A–3D ). This site was then closed using interrupted sutures of 4.0 polyglycolic acid suture. The patient was dismissed with postoperative instructions (soft diet, oral hygiene, Medrol dosepak, chlorhexidine gluconate 0.16% rinses, 500 mg of nabumetone and amoxicillin three times daily for one week). The patient was recalled every three months after an initial visit and two-week follow-up for postoperative evaluations. Postoperative results six months after enucleation of the cyst are shown (FIGURES 1E and 1F ). No signs of inferior alveolar nerve dysesthesia, anesthesia, numbness or paresthesia were noted, and no recurrence was detected on one-year follow-up. Periodontal management and prosthodontic restoration are currently being planned now that the

FIGURE 2 . Histological section of the lesion showing sheets, strands and whorled masses of odontogenic epithelial cells set in scant fibrous stroma. Duct-like structures are noted and osteoid or basophilic mineralized material are present.

FIGURE S 3 . Centrifuged whole blood (3A ); withdrawn I-PRF fraction (3B ); A-PRF fraction (3C ); and preparation of bone graft (3D ).

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pathology has been successfully treated without recurrence. Discussions for teeth replacement are ongoing with the patient and his general dentist.

Discussion

AOT constitutes between 3% to 7% of all benign odontogenic tumors.7 This lesion usually presents in the anterior maxilla in association with an impacted tooth (generally a canine), has a female preponderance and occurs most commonly in the second to third decade of life. AOT occurs in three variants, the follicular, extrafollicular and the peripheral, where each variant is slow growing and has similar histology. The follicular and the extrafollicular variants account for 96% of all AOTs, of which 71% of these are of the follicular variant.8 The follicular variant is intraosseous and associated with an impacted tooth, most commonly a maxillary canine. The extrafollicular type has no such relation to an impacted tooth, but more associated with the apex or sides of the tooth or with gingival tissues.9 PRF is a hematological fraction produced by the centrifugation of whole blood in a blood collection tube without heparin. The variation of centrifuge speed and centrifuge time will govern the production of the type of PRF product. A-PRF and I-PRF vary from standard PRF (S-PRF) both in preparation and composition. A-PRF and I-PRF are produced using slower centrifuge speeds, and these fractions have been shown to produce more neutrophils in the useful portion of the PRF clot.10 A-PRF and I-PRF have been reported to provide platelet-derived growth factors, bone morphogenic proteins 2 and 7, transforming growth factor beta and thrombospondin and to stimulate formation of new blood vessels.11 These growth factors can aid in the healing process. The platelets of the fraction also 162

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influence host response by their action on granulocytes, monocytes, endothelial cells and lymphocyte recruitment to the site of activity. These cells play a role in the regulation of the host response to foreign bodies, osteogenic and angiogenic initiation and tissue restoration potential brought about by the effects of macrophages.12 I-PRF is a more liquid fraction and is better for mixing with bone substitute materials for grafting than the firmer A-PRF. The case reported here is unique in several aspects in that it is a mandibular lesion, extrafollicular and not associated with an impacted tooth, developed in an older adult male and radiographically presented as a mixed and not lucent lesion. This is also the first case reporting management of AOT using bone graft substitute in combination with PRF congeners.

Conclusion

We present a rare case of mandibular adenomatoid odontogenic tumor with a novel treatment approach utilizing bone graft in combination with I-PRF and A-PRF membranes. Wound closure after surgical enucleation has not been standardized. In this case report, we sought to propose the use of bone graft in association with A-PRF and I-PRF as a useful technique for grafting and site closure, as there are indications that bone restitution time and healing time are improved. This work was presented as a poster at 2019 Research Day organized by the Herman Ostrow School of Dentistry of USC. n

AC KN OW L E DG M E N T The authors thank Daniel Kohanchi, DDS, and Jasmine El Khoury, DDS, who assisted during the surgery, and advanced periodontology resident Sara Elhusseini DDS, MS. RE F E RE N C E S 1. Soluk-Tekkeşin M, Wright JM. The World Health Organization classification of odontogenic lesions: A summary of the changes of the 2017. 4th ed. Turk Patoloji Derg 2018;34(1). doi: 10.5146/tjpath.2017.01410. 2. Miyazaki Y, Kikuchi K, Kusama K, et al. An expanded and revised early history of the adenomatoid odontogenic tumor. Oral Surg Oral Med Oral Pathol Oral Radiol 2013 May;115(5):646–51. doi: 10.1016/j.oooo.2013.01.023. 3. Samman N, Reichart PA, Wu PC, Ormiston IW, Philipsen HP. Variants of the adenomatoid odontogenic tumor with a note on tumor origin. J Oral Pathol Med 2006;21(8):348– 352. doi.org/10.1111/j.1600-0714.1992.tb01363.x. 4. Tiwari M. Adenomatoid odontogenic tumor: An extra follicular variant in the mandible of 12-year-old pediatric female patient. Oral Heal Case Reports 2016;02(01):1–2. doi: 10.4172/2471-8726.1000104. 5. Chrcanovic BR, Gomez RS. Adenomatoid odontogenic tumor: An updated analysis of the cases reported in the literature. J Oral Pathol Med 2019 Jan;48(1):10–16. doi: 10.1111/jop.12783. Epub 2018 Oct 7. 6. Kökdere NN, Baykul T, Findik Y. The use of platelet-rich fibrin (PRF) and PRF-mixed particulated autogenous bone graft in the treatment of bone defects: An experimental and histomorphometrical study. Dent Res J (Isfahan) Sep–Oct 2015;12(5):418–24. doi: 10.4103/1735-3327.166188. 7. Vasudevan K, Kumar S, Vigneswari S. Adenomatoid odontogenic tumor, an uncommon tumor. Contemp Clin Dent 2012 Apr–Jun;3(2):245–247. doi: 10.4103/0976237X.96837. 8. Philipsen HP, Reichart PA. Adenomatoid odontogenic tumour: Facts and figures. Oral Oncol 1999 Mar;35(2):125– 31. doi: 10.1016/s1368-8375(98)00111-0. 9. Kundoor R, Maloth KN, Guguloth NN, Kesidi S. Extrafollicular adenomatoid odontogenic tumor: An unusual case presentation. J Dent (Shiraz) 2016 Dec;17(4):370– 374. PMCID: PMC5136418. 10. Ghanaati S, Booms P, Orlowska A, et al. Advanced platelet-rich fibrin: A new concept for cell-based tissue engineering by means of inflammatory cells. J Oral Implant 2014 Dec;40(6):679–89. doi: 10.1563/aaidjoi-D-14-00138. 11. Mitrea M, Rusu A, Călin D. The management of periapical maxillary cyst by using the A-PRF (platelet rich advanced fibrin): A case report. Rom J Oral Rehabil 2015;7(2):12–19. 12. Thanasrisuebwong P, Surarit R, Bencharit S, Ruangsawasdi N. Influence of fractionation methods on physical and biological properties of injectable platelet-rich fibrin: An exploratory study. Int J Mol Sci 2019 Apr;20(7):1657. doi: 10.3390/ijms20071657. T HE CORRE S P ON DIN G AU T HOR , Tarun Mundluru, DDS, MSc, can be reached at tarunvsdc@gmail.com.

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C .E. CREDIT QUESTIONS

March 2022 Continuing Education Worksheet

This worksheet provides readers an opportunity to review C.E. questions for the article “A Mandibular Adenomatoid Odontogenic Tumor With a Novel Treatment Utilizing PRF: A Case Report” before taking the C.E. test online. You must first be registered at cdapresents360.com. To take the test online, please click here. This activity counts as 0.5 of Core C.E.

1. The adenomatoid odontogenic tumor (AOT) has been dubbed the “tumor of two-thirds” for all but which one of the following reasons? a. Approximately two-thirds of the cases occur in females. b. Approximately two-thirds of the cases occur in the second to third decade of life. c. Approximately two-thirds of the cases occur in the mandible. d. Approximately two-thirds of the cases occur in association with an unerupted canine. 2. Which of the following describe the variant types associated with AOT (mark all that apply)? a. Follicular b. Marginal c. Extrafollicular d. Peripheral e. All of the above 3. In the case presented, the working differential diagnosis based on clinical and radiographic findings included: a. Central odontogenic fibroma b. Calcifying odontogenic cyst c. Ossifying fibroma d. Calcifying epithelial odontogenic tumor e. All of the above 4. The surgical aspects in this case included all but which one of the following? a. Sedation utilizing oral medication b. Enucleation of the lesion c. Extraction of the right mandibular lateral incisor and canine d. Grafting for bony defect repair 5. True or False: The I-PRF and A-PRF used to repair the surgical site were produced by centrifuging blood obtained from the patient.

6. Which of the following were not part of the postsurgical protocol for this patient? a. Chlorhexidine gluconate rinse b. Soft diet c. Amoxicillin three times daily for one week d. Oxycodone PRN to manage pain 7. What is the most common AOT variant? a. Follicular b. Marginal c. Extrafollicular d. Peripheral 8. Which of the following statements apply to PRF (mark all that apply)? a. PRF is a hematological fraction produced by centrifuging whole blood in a blood collection tube without heparin. b. The variation of centrifuge speed and centrifuge time will govern the production of the type of PRF product. c. A-PRF and I-PRF are produced using slower centrifuge speeds. d. All of the above 9. A-PRF and I-PRF have been reported to stimulate formation of new blood vessels by providing all but which one of the following? a. Platelet-derived growth factors b. T-cell proliferation c. Bone morphogenic proteins d. Transforming growth factor beta 10. True or False: The authors conclude that the successful treatment of this mandibular adenomatoid odontogenic tumor utilizing bone graft in combination with I-PRF and A-PRF membranes to repair the surgical site reaffirms this standardized and reliable method for AOT treatment.

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oral hygiene and covid-19 C D A J O U R N A L , V O L 5 0 , Nº 3

The Mouth-COVID-19 Connection: Importance of the Oral Cavity for the Coronavirus — Part I Shervin Molayem, DDS, and Carla Cruvinel Pontes, DDS, MsC, PhD

abstract Background: The mouth plays a crucial role as an entry point for the SARS-CoV-2 virus. The new coronavirus has been identified in saliva, and its viral load has been linked to the severity of COVID-19. Types of studies reviewed: This study was designed as a narrative review. Medline, Scopus and Google Scholar were searched up to January 2021 for articles in English that addressed the role played by the oral cavity and saliva in the coronavirus disease, with particular focus on viral presence in the oral cavity. All relevant scientific articles were included. Results: Hyposalivation can increase the risk for respiratory infections and COVID-19. Oral lesions are rare in COVID-19 patients, with reports of sialadenitis, mucositis, geographic tongue, burning mouth, necrotizing gingivitis and viral enanthema. Transient loss of taste and smell are highly prevalent symptoms, likely related to neurological changes. Practical implications: Given the importance of the oral cavity and saliva in the development and transmission of the coronavirus disease, as health care professionals, dentists have a crucial role to play during the pandemic. Keywords: Mouth COVID-19, saliva COVID-19, oral health COVID-19, oral inflammation

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 the director of the Mouth Body Research Institute and 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.

s the coronavirus disease pandemic unfolds, health care providers are expected to keep their knowledge on the disease and related protocols up to date so they can better play their part in this unique global health crisis. The COVID-19 pandemic is caused by the novel SARS-CoV-2, a beta coronavirus closely related to SARSCoV, which resulted in the occurrence of acute respiratory syndrome (SARS) in over 30 different countries in 2002. Five other coronaviruses have been found in

humans, including -229E, HCoV-OC43, HKU1, HCoV-NL63 and the Middle East Respiratory Syndrome (MERS)CoV. Coronaviruses constitute enveloped single-stranded RNA viruses that rely on the receptor angiotensin-converting enzyme 2 (ACE2) to infect human cells.1 During the pandemic, dentists are being called to the important task of reducing infection and inflammation in the mouth, particularly in the form of periodontal disease, while adhering to severe infection control measures to avoid the spread of COVID-19 between M ARC H 2 0 2 2

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patients and staff.2 Since up to 75% of infected individuals can be asymptomatic, in dental practices, all patients must be treated with extensive precautions.3 The identification of SARS-CoV-2 in saliva droplets of infected patients has shed light on the high risk of transmission through saliva, placing the oral cavity in a pivotal position as an entry point for the virus, together with the nasal cavity and the ocular mucosa.4 Saliva can be used as a diagnostic tool for the identification of SARS-CoV-2, which points to the potential for the oral cavity to become a target for preventive interventions during the early stages of infection.5 This review aims at exploring the role of the oral cavity in COVID-19 as well as its implications for dental practitioners and patients, including viral presence in the oral cavity, saliva’s role, diagnosis of COVID-19 and alterations in the oral cavity of COVID-19 patients.

but replicate in the respiratory system and the gut. However, a few viruses, such as herpes and papillomaviruses, proliferate in oral epithelial cells and release viral particles to saliva, increasing the risk for development of mucosal lesions.8

COVID-19 Receptors in the Oral Cavity

Infection by SARS-CoV-2 starts after the virus binds to host cells through ACE-2 receptors, which mediate viral entry. In an in vitro study, Xu et al. (2020) confirmed the expression of

One single infected cell can produce approximately 103 virions, which is also known as the per-cell viral yield.

Oral Cavity as a Portal to COVID-19 Infection

The oral cavity provides an adequate niche for colonization and growth of microorganisms, presenting the second most diverse microbiota in the body after the gut. The oral microbiome is composed of over 700 species of microorganisms, including bacteria, viruses, fungi and protozoa. While culture studies provided a limited approach to explore the microbiome, genomic technologies have greatly increased our understanding of the highly complex oral environment.6 Adequate conditions in the oral cavity that favor microorganisms include stable temperature (37 C), salivary pH 65–7 and the presence of different niches, from hard dental tissues to soft mucosa.7 Despite the favorable conditions, studies suggest that most viruses do not replicate in the oral cavity, 166

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ACE-2 in the oral mucosa, with the highest expression in epithelial cells from the tongue and salivary glands.9,10 ACE-2 receptors are expressed in a variety of human cells, including alveolar epithelial cells, pneumocytes and vascular epithelium, and expression increases with aging.11 High ACE-2 expression has been linked to increased susceptibility to COVID-19 infection, thus the oral cavity plays a crucial role in the viral infection.11 In addition to the ACE-2 receptor, furin has also been linked to viral invasion of host cells. Furin is a host protease suggested to facilitate cleavage of SARS-CoV-2 glycoproteins on the viral envelope and infection. In the oral cavity, furin is mostly expressed on the tongue and in mucosal epithelial cells.12,13

SARS-CoV-2 in the Oral Cavity

In vitro studies on SARS-CoV indicate that it takes about 10 minutes for the virus to enter a host cell and 10 hours for the host cell to produce and release virions (viral particles) to the extracellular environment. One single infected cell can produce approximately 103 virions, which is also known as the per-cell viral yield.14 In the transmission of SARS-CoV-2, the oral cavity, nasal cavity and eyes constitute entry points to viral particles from the environment and/or from other infected hosts.15 Besides direct exposure to the virus, Sabino-Silva et al. suggest three indirect mechanisms to explain the presence of SARS-CoV-2 in the oral cavity:4 ■ Viruses in the respiratory tract can reach the oral cavity through droplets of respiratory mucous, which are often exchanged between the mouth and respiratory tract through coughing and sneezing. ■ Viruses in the systemic circulation can reach the oral cavity through the gingival crevicular fluid. ■ Minor and major salivary glands can harbor the virus and release infective particles to saliva through salivary ducts. Studies have confirmed the presence of SARS-CoV-2 in saliva samples from COVID-19 patients,16–20 with 25% of patients from one study showing live viruses.16 However, the behavior of the virus in the oral cavity is unknown, with factors such as the composition of the oral microbiota, the composition and production of saliva and oral diseases potentially influencing the virus’s ability to infect oral cells.21 Based on findings from previous studies, it can be suggested that once in the oral cavity, SARS-CoV-2 can: 22 ■ Interact with the oral microbiome. ■ Invade oral cells and replicate, with the potential to cause local lesions.21

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■

Invade and replicate in minor salivary glands, forming a reservoir for infection.9 Access the respiratory tract through aspiration.23 Be swallowed and lead to local changes in the gut, resulting in digestive symptoms such as diarrhea, vomiting or abdominal pain.24

The Role of Saliva in COVID-19 Infection Transmission Routes for SARS-CoV-2

The most common transmission routes for SARS-CoV-2 include contact and direct transmission. Direct transmission includes exposure to the virus through coughing, sneezing and/or inhalation of droplets from infected individuals, which contain a mixture of saliva and respiratory mucous. Indirect transmission occurs when the oral, nasal or ocular mucosa gets in contact with contaminated hands, objects or surfaces. Transmission through aerosols and the fecal-oral route are also thought to contribute to the spread of COVID-19.25,26

Viral Load in Saliva

In 2004, a study on the first coronavirus outbreak (SARS-CoV) suggested that transmission occurred mainly through droplets from the oral cavity or respiratory tract during conversation, coughing or sneezing, indicating the importance of saliva droplets. The authors reported high amounts of virus RNA in saliva (7.08 x 103 to 6.38 x 108 copies/mL) and throat wash (9.58 x 102 to 5.93 x 106 copies/mL) of SARS patients.27 A recent study on SARS-CoV-2 showed a high salivary viral load in samples from the posterior throat of COVID-19 patients (104–106 copies/ mL). The highest viral load was

observed up to a week after onset of symptoms, and despite the decline with time, viral RNA was still detected after 14 days in 40% of the evaluated patients.28 The elevated salivary viral load can be linked to the high person-to-person transmissibility. Yoon et al. evaluated the viral load in two hospitalized COVID-19 patients in saliva, sputum, nasopharynx, oropharynx and urine. Saliva presented a consistently high viral load, which was higher than the oropharynx in the early stages of the disease.29

Dental-generated aerosols typically result from water and air spray, with the potential to markedly dilute viruses.

One of the biggest challenges regarding the transmission of COVID-19 relates to the spread of droplets. It has been estimated that sneezing spreads around 40,000 droplet nuclei, coughing spreads around 3,000 and talking generates 600 droplet nuclei per minute. While saliva droplets over 60 µm in diameter tend to settle quickly on surfaces, smaller droplets are likely to be involved in interindividual transmission. Droplets with diameter of > 10 μm tend to evaporate and turn into droplet nuclei, potentially contributing to aerosol transmission.30–32 Studies on SARS coronaviruses report that droplets can persist for four hours on copper, 24 hours on cardboard and at least four days on wood, glass and plastic surfaces, which highlights the importance of strict infection control measures.33

COVID-19 and the Risk for Aerosol Transmission

The importance of aerosols for the transmission of COVID-19 has been discussed. Aerosols consist of small particles ranging from 0.001 to > 100 μm, which remain suspended in the air. The World Health Organization (WHO) has suggested that aerosol-generating dental procedures can lead to the spreading of SARS-CoV-2. This is one of the reasons why early in the pandemic, before infection control and respiratory protection procedures were established for dentistry, they recommended postponing elective dental procedures. In order for aerosols to be infective, three main factors need to be considered: the time that saliva droplets remain in the air (physical decay), the time that the virus remains infectious (biological decay) and the acquisition of droplets by a susceptible host.34 A study from China tested35 aerosol samples from two hospitals in Wuhan, and the results showed low to undetectable SARSCoV-2 RNA in samples from patient areas and positive samples from floor surfaces (deposition aerosol), suggesting that droplets in the air are not a problem; however, infection control measures are crucial for floors and surfaces.35 Dental-generated aerosols typically result from water and air spray, with the potential to markedly dilute viruses. Furthermore, high-volume evacuation systems used in dental clinics reduce aerosol significantly.36 Lastly, dental professionals have routinely used personal protective equipment (PPE) due to the possibility of transmission of HIV, hepatitis and other contagious diseases. High standards of infection control have been the norm in daily dental practice. It has been suggested that oral rinsing before dental procedures can reduce the viral load. In a meta-analysis from M ARC H 2 0 2 2

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TABLE 1

Advantages and Limitations of Salivary Testing To Diagnose COVID-19 Infection Advantages

Limitations

Noninvasiveness Can be used for diagnosis and monitoring

Reliability Studies required on sensitivity and specificity

Convenience Large supply, no discomfort during sampling

Variation Method of collection can influence results

Easiness of collection Self-collection, multisampling possible Only requires sterile container

Salvia production Affected by medications and conditions

Adaptability Suitable for children, adults, elderly, disabled

endocrine, neurologic and infectious diseases, use of medications (antidepressants, antipsychotics and antihistamine drugs) and radiotherapy for head and neck cancer. Treatment strategies for hyposalivation are mostly palliative, including saliva substitutes, salivary stimulants, topical agents and systemic sialogogues.42

Safety Safe for health professionals, easy handling, lower risk for operator error

SARS-CoV-2 Salivary Diagnosis Diagnostic Tests

Cost-effectiveness Quick, suitable for large populations

Marui et al. (2019), chlorhexidine, essential oils and cetylpyridinium chloride mouthwashes reduced the number of disseminated microorganisms by 64.8% when used before dental procedures.37

Salivary Glands and SARS-CoV-2

In an experimental study on SARSCoV in rhesus macaques, epithelial cells from salivary glands expressed ACE-2 and became infected.38 Findings from another SARS-CoV study showed that viral RNA was detected in saliva before the development of lung infection.27 In an in vitro study of human tissues, Xu et al. reported mean expression of ACE-2 in salivary glands of 1.8 protein-coding transcripts per million (pTPM), which is the 10th highest expression in the body, higher than in pulmonary tissues.9 Liu et al. (2020) reported a high expression of ACE-2 receptors on epithelial cells of salivary ducts.38 Together, these findings suggest that salivary glands can be initial targets for COVID-19 infection, functioning as a reservoir for the virus, particularly in asymptomatic patients.9

Hyposalivation Can Be a Risk Factor for COVID-19 A series of proteins present in human saliva has demonstrated 168

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anti-viral activity, such as mucins, cathelicidin, lysozyme, peroxidase, agglutinin, cystatins, lactoferrin and alpha and beta-defensins.6 Although the antiviral role of saliva against SARS-CoV-2 has not been explored, it can be speculated that invasion of oral cells is a challenging viral task. Thus, hyposalivation, which describes a decrease in saliva flow, is likely to increase the risk for respiratory infection in COVID-19 patients.39 A prospective study from Iwabuchi et al. reported a higher incidence of acute respiratory infections in subjects with hyposalivation, with an odds ratio of 1.76, meaning that a patient with hyposalivation has nearly 1.8 more chance of developing respiratory infections. The authors suggested that hyposalivation can lead to impaired protection of the oral and respiratory mucosa and to a higher risk for viral adhesion and replication.40 Criteria for diagnosis of hyposalivation:41 ■ Stimulated salivary flow rate = ≤ 0.5–0.7 mL/min. ■ Unstimulated salivary flow rate = ≤ 0.1 mL/min. Hyposalivation often manifests as xerostomia, particularly in the elderly. The etiological factors for hyposalivation include autoimmune,

COVID-19 tests to detect current infection are based on nucleic acid amplification to identify viral RNA, typically through polymerase chain reaction (PCR). For diagnosis, samples are collected from the nasopharynx, oropharynx or sputum using a swab, which is transferred to a liquid, where viral RNA is released, extracted and amplified.43 Nasopharyngeal swabs collected by health care professionals are the gold standard for diagnostic testing of SARS-CoV-2 due to their high sensitivity and specificity. Nonetheless, they are invasive, can cause discomfort and, if handled incorrectly, can lead to coughing, bleeding and lower test accuracy.28 Saliva tests present the advantages of being noninvasive, convenient due to large supply and painless nature of the test, presenting easy collection with potential for self-collection (TA BLE 1 ). Salivary tests are safe, present lower risk for operator error and can be performed in most patients, including children, the elderly and the disabled. In the diagnosis of respiratory viruses in hospitalized patients, a high correlation between nasopharyngeal fluids and saliva has been reported.44 Few studies have evaluated different methods for saliva collection, including swab, coughed out or spit out saliva and collection from salivary gland ducts. The limitations of salivary diagnosis for COVID-19 include the limited number

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of studies, the influence of the collection method and salivary changes on test results.

Saliva Swabs

In a study by Zhang et al. (2020), saliva swabs were positive in only 50% of confirmed COVID-19 patients.19 In another study that used the saliva drooling technique, all samples (n = 25) tested positive, and the authors concluded that saliva was a reliable diagnostic tool.45

Coughed-Out or Spit-Out Saliva

Deep throat saliva can have higher diagnostic value, as suggested by results from two studies from the same group. In one study, positive results were present in 91.7% of positive patients, and in the second study, virus RNA was detected in 86.9% of saliva samples.16,28 Yoon et al. (2020) reported a remarkably high viral load of SARS-CoV-2 in the saliva of two hospitalized patients, who were instructed to self-collect saliva by spitting into collection tubes.29 In a more recent study that included 1,104 samples from 386 patients, selfcollected spit-out saliva was as effective as nasopharyngeal swabs collected by health care professionals. Interestingly, saliva presented higher reliability than anterior nasal swab in the study.46

Salivary Gland Duct

Chen et al. (2020) collected saliva from a salivary gland duct and reported that only 12.9% of confirmed COVID-19 cases tested positive. Because three of the four patients who tested positive for salivary gland saliva were on ventilators, the authors suggested that this method can indicate the severity of the disease.20 Further confirmation on salivary diagnosis comes from the study by Wyllie et al. (2020). Using PCR tests, higher viral RNA was found in saliva

as compared to nasopharynx swabs in 70 hospitalized COVID-19 patients. Furthermore, one to five days after the initial diagnosis, 71% of the nasopharynx samples and 81% of salivary samples remained positive, suggesting that saliva is at least as sensitive as nasopharyngeal swabs to detect SARS-CoV-2.47 Thus, the diagnostic value of saliva for COVID-19 is increasing rapidly. It can become the new gold standard in the near future, as more studies are reporting its comparability to nasopharyngeal samples.

Antigen tests can decrease time and cost, however, their reliability seems to be lower than PCR-based tests.

Antibody Tests

In addition to genetic tests, serological tests have been used to detect antiSARS-CoV-2 antibodies, including IgM, IgG and IgA. However, serological tests are more suitable to evaluate the host response and identify previous infection, while genetic tests are the best option to identify current infection.48 Saliva has the potential to not only provide a diagnosis for COVID-19, but also for monitoring viral loading during disease. At this point, there are no studies investigating salivary antibodies against SARS-CoV-2.12

New Salivary Tests for COVID-19

A new quick test to detect SARSCoV-2 in saliva through simplified PCR has been developed by the Yale

School of Public Health, and its use has recently been authorized by the U.S. Food and Drug Administration (FDA).49 A spectroscopy-based portable diagnostic test that relies on artificial intelligence has been developed and preclinically evaluated for dengue and Chikungunya Virus with promising results (99% success). It can be used with serum or saliva samples for diagnosis and estimation of viral load.50 Another diagnostic development comes from Virginia Tech, where engineering professors have created a test to detect the virus in droplets through biosensing. This nanotechnology combined with laser beams will be able to give results within minutes.51 While most current diagnostic tests rely on PCR, new antigen tests are being developed, since SARSCoV-2 present multiple surface proteins that function as antigens.52 Antigen tests can decrease time and cost, however, their reliability seems to be lower than PCR-based tests. Different laboratories have antigen tests in the market; however, recent studies suggest the low sensitivity (30.2% in one study and 11.1-45.7% in another study) makes these tests more appropriate for rapid screening than confirmed diagnosis of COVID-19. In a recent comprehensive review, findings from 28 studies that evaluated the presence of SARS-CoV-2 in saliva samples were summarized. In saliva, the viral load ranged from 9.9 × 102 to 1.2 × 108 copies/mL. When compared to the gold standard, the sensitivity of saliva tests ranged 66% to 91.7% and specificity ranged 97% to 100%, with saliva presenting considerably lower costs. Factors that are likely to affect salivary results include time for collection during the day, collection method and stage of the disease.54 M ARC H 2 0 2 2

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Oral Findings in COVID-19 Patients Gustatory Dysfunction

Loss of taste (ageusia) has been strongly linked to COVID-19, being often associated with total or partial loss of smell (anosmia or hyposmia, respectively). In a multicenter study, over 80% of COVID-19 patients with mild to moderate symptoms had olfactory and/ or gustatory dysfunction.55 A metaanalysis from Tong et al. (2020) reported prevalence of olfactory dysfunction (anosmia) of 52.7% (range 5.61% to 92.65%) and gustatory dysfunction of 43.9% (5.61% to 92.65%) in COVID-19 patients. The authors highlighted the well-established link between olfactory function and taste, hence it is not clear whether gustatory dysfunction is an independent condition or a consequence of olfactory dysfunction, with 10.2% to 22.5% of patients presenting gustatory dysfunction alone.55–58 In 35.5% of the patients included in the study from Beltrán-Corbellini et al., olfactory or gustatory dysfunction was the first clinical symptoms of COVID-19.59 Anosmia and hypogeusia can be present in the absence of other symptoms and typically develop during the initial phase of the coronavirus disease.60 The pathophysiology of gustatory and olfactory alterations related to SARS-CoV-2 is not fully understood. Because these symptoms can be present in the absence of inflammation, they are most likely linked to neurological alterations and damage to receptors.61 Taken together, these findings indicate that olfactory and/or gustatory dysfunction can be diagnostic markers that suggest the need for diagnostic testing and self-isolation.56

Salivary Gland Conditions

In the literature, acute parotitis and submandibular sialadenitis have 170

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been reported in two COVID-19 patients. Both patients had systemic comorbidities and presented preauricular swelling, with one patient also presenting submandibular swelling.62 In another report, acute parotitis was diagnosed in an otherwise healthy COVID-19 patient.63 In both case reports, the alterations disappeared after resolution of the viral infection. Despite the infrequency of salivary glands changes, dentists and physicians should be aware of this potential manifestation of COVID-19.

In another report, acute parotitis was diagnosed in an otherwise healthy COVID-19 patient.

Oral Mucosal Lesions

With the increase in studies reporting COVID-19-related cutaneous conditions, known as viral exanthem or skin rashes, the mouth has received more attention during clinical examination. In the oral cavity, viral lesions can be present in the form of viral enanthem, typically manifesting as vesicular, macular, papular and/or petechial lesions. A few case reports present oral lesions in COVID-19 patients, with most resembling viral enanthem (TA BLE 2). Viral enanthem has been reported for dengue, chikungunya, Ebola, herpes, HIV, Epstein-Barr, varicella‐zoster and Paramyxoviridae viruses.64 According to Jimenes-Cauhe et al. (2020), 29% of COVID-19 patients presenting

exanthem also presented enanthem, with petechiae in the palate being the most common clinical presentation.65 In a case report from France, a COVID-19 patient presented with an irregular ulcer on the tongue dorsum that started as a painful papillae inflammation and erythema, and the lesion disappeared after three days.66 In another report from Spain, one confirmed patient and two patients suspected to be infected presented minor palatal ulcers, small blisters in the vermillion border and generalized desquamative gingivitis.67 Ulcers in the gingiva, palate and tongue were also described in one case report from Italy68 and two patients from Iran.69 An erythematous palatal lesion that extended to the oropharynx was report in a Turkish COVID-19 patient.70 In a case report from Brazil, a COVID-19 patient who had other systemic conditions presented a macular white plaque on the tongue dorsum, diagnosed as a fungal infection and small ulcers in the oral mucosa.71 Soares et al. (2020) reported oral lesions in another COVID-19 patient from Brazil who was admitted to hospital, in the form of a red diffuse lesion in the hard palate, an ischemic ulcer in the buccal mucosa as well as multiple macules in the tongue, palate and lips.72 Three patients who developed cutaneous erythema multiformlike lesions related to COVID-19 presented palatal macules and petechiae, according to a short correspondence article from Spain.73 In one single case report from England, a COVID-19 patient developed necrotizing gingivitis.74 Currently, it is not clear if oral lesions in COVID-19 patients are a primary or secondary consequence of the viral infection.65 The role of previous systemic conditions, the host immune reaction and the use of medications have been suggested as contributing factors

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TABLE 2

Study

CarreraPresas et al.67

Country

Spain

Age

Gender Health conditions

Oral lesions

Skin lesions

Features

Onset

Management

Duration

Tentative diagnosis

Topical mouthwash, systemic prednisone 30 mg/day

3 days

Viral enanthema

Rash under breasts, back and genital area

Female

Obesity, hypertension

Blisters in lower lip mucosa, desquamative gingivitis

With initial general symptoms

Male

Ulcers in hard palate (similar to herpetic ulcers)

Valaciclovir 500 mg 2 days after fever every 8 h, onset chlorhexidine and hyaluronic acid mouthwash for 10 days

10 days

Recurrent herpetic stomatitis

Male

Diabetes, hypertension

Herpetic-like ulcers in left palate

Not clear

Topical antiseptic mouthwash

1 week

Recurrent herpetic stomatitis

Soares et al.72

Brazil

Male

Diabetes, hypertension

Ischemic ulcer in buccal mucosa, multiple red macules in hard palate, tongue, and lips

Not clear

Follow-up

3 weeks

Viral enanthema

Petechia, small vesicobullous lesions

Ciccarese et al.68

Italy

Female

Ulcers, erosions on inner lip, petechiae on palate and gingiva

5 days after general symptoms

Palliative

5 days

Petechiae

Erythematous macules, papules and petechiae on lower extremities

Ansari et al.69

Iran

Female

Diabetes

Painful ulcers with irregular margins in hard palate

5 days after general symptoms

1 week Topical diphenhydramine, dexamethasone, tetracycline, lidocaine

Opportunistic No bacterial infection

Male

Hypertension

Small ulcers, with irregular margins, in anterior tongue

1 week after hospital admission

Topical diphenhydramine, dexamethasone, tetracycline with lidocaine

1 week

Opportunistic No bacterial infection

dos Santos et al.71

Brazil

Male

Coronary heart disease, kidney transplant

White plaque, multiple ulcers in tongue dorsum

24 days after hospital admission

Fluconazole, nystatin, chlorhexidine digluconate (0.12%), topical daily 1% hydrogen peroxide

2 weeks

Fungal infection (tongue scrape culture)

Kahraman, Çaşkurlu70

Turkey

Male

Erythematous lesion in oropharynx and hard palate, petechiae and pustular enanthema near soft palate

With general symptoms

Antibiotics

Unclear

Oral mucositis

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TABLE 1, CONTINUED

Study

Country

Age

Gender Health conditions

Oral lesions

Skin lesions

Features

Onset

Management

Duration

Tentative diagnosis

ChauxBodard et al.66

France

Female

Irregular ulcer in dorsum of tongue

8 days after initial general symptoms

Follow-up

10 days

Viral enanthema

Erythematous lesion on big toe

Patel, Wooley74

England

Female

Erythematous, edematous gingiva, necrotic papillae

400 mg 3 days after fever metronidazole 3x daily for 5 days, onset 0.12% chlorhexidine for 10 days

5 days

Necrotizing gingivitis

Tomo et al.75

Brazil

Female

Diffuse bilateral erythema, depapillated tongue borders

9 days after initial general symptoms

Chlorhexidine 0.12%

2 weeks

Oral mucositis

JimenezCauhe et al.65

Spain

5877

3 Females

Unclear

Palatal macules and petechiae

Unclear

Systemic corticosteroids

2-3 weeks Unclear

in the development of oral lesions in those patients. Oral lesions are rare in COVID-19 patients, and the current evidence is not strong enough to suggest viral damage to oral cells. The lesions described so far probably result from drug-related reactions, opportunistic infections and/or hypersensitivity.75

Take-Home Message

Oral cavity infection and transmission. The oral cavity is an important entry point to the body, and its unique environment is favorable for microorganisms. ACE-2 receptors are expressed in the oral mucosa, particularly in salivary glands, suggesting that they can harbor viruses in the early stages of infection. Direct and indirect transmission through oral fluid droplets play a pivotal role in the spread of the disease. Viral behavior in the oral cavity. Once in the mouth, the virus can potentially interact with the microbiome, invade oral cells and salivary glands and reach other organs, such as lungs and intestines, through aspiration and swallowing, respectively. 172

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Viral load. SARS-CoV-2 has been identified in high levels in the oral cavity, and salivary viral load has been linked to the severity of COVID-19 infection. Saliva’s role. Saliva can be a culprit when it comes to transmission, but it also presents anti-viral properties. Hyposalivation can increase the risk for COVID-19 due to impaired protection of the mucosa. Dentists should be aware of the diagnostic criteria for hyposalivation and offer adequate treatment approaches when necessary. Diagnosis. For the diagnosis of COVID-19, saliva is likely to become the new gold standard, presenting comparable results to nasopharyngeal swabs. New diagnostic salivary approaches are being developed for quicker and more affordable tests, which will be a game-changer for health professionals. Oral lesions. Oral lesions are rare in COVID-19 patients, with reports of sialadenitis, mucositis, geographic tongue, burning mouth and viral enanthema that can manifest as petechiae, macules, papules or ulcers. Transient loss of taste and smell is highly prevalent.

Erythema multiform-like lesions

Despite the ethical challenges that might limit the conduction of studies during the pandemic, it is imperative to highlight the need for high-level evidence research to help elucidate the possible connection between COVID-19 and the oral cavity.

Conclusion

The oral cavity is a crucial entry point for microorganisms. SARS-CoV-2 has been identified in high levels in the oral cavity, and salivary viral load has been linked to the severity of COVID-19 infection. Saliva plays a pivotal role in infection and transmission, with hyposalivation potentially increasing the risk for COVID-19 due to impaired mucosal protection. Due to the multiple advantages of salivary tests, they are likely to become the new gold standard for COVID-19 diagnosis. While oral mucosal lesions are rare in COVID-19 patients and possibly develop as a secondary reaction to the virus, loss of taste and smell are a frequent symptom. Due to the importance of the oral cavity and saliva in the development and transmission of the coronavirus disease, dentists have a crucial role to play as health care professionals during the pandemic. n

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RE FEREN CE S 1. Marra MA, Jones SJM, Astell CR, et al. The genome sequence of the SARS-associated coronavirus. Science 2003 May 30;300(5624):1399–404. doi: 10.1126/ science.1085953. Epub 2003 May 1. 2. Molayem S, Pontes C. The Mouth-COVID Connection: Il-6 Levels in Periodontal Disease — Potential Role in COVID19-Related Respiratory Complications. J Calif Dent Assoc 2020;48(10):485–499. doi:10.35481/jcda-48-10-01. 3. Yanes-Lane M, Winters N, Fregonese F, et al. Proportion of asymptomatic infection among COVID-19 positive persons and their transmission potential: A systematic review and meta-analysis. PLoS One 2020 Nov 3;15(11):e0241536. doi: 10.1371/journal.pone.0241536. eCollection 2020. 4. Sabino-Silva R, Jardim ACG, Siqueira WL. Coronavirus COVID-19 impacts to dentistry and potential salivary diagnosis. Clin Oral Investig 2020 Apr;24(4):1619–1621. doi: 10.1007/s00784-020-03248-x. Epub 2020 Feb 20. 5. Kirk-Bayley J, Challacombe S, Sunkaraneni V, Combes J. The use of povidone iodine nasal spray and mouthwash during the current COVID-19 pandemic may protect healthcare workers and reduce cross infection. SSRN Electron J 2020 Mar:3563092. doi:10.2139/ssrn.3563092. 6. Baghizadeh Fini M. Oral saliva and COVID-19. Oral Oncol 2020 Sep;108:104821. doi: 10.1016/j. oraloncology.2020.104821. Epub 2020 May 27. PMCID: PMC7250788. 7. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005 Nov;43(11):5721–5732. doi:10.1128/ JCM.43.11.5721-5732.2005. 8. Grinde B, Olsen I. The role of viruses in oral disease. J Oral Microbiol 2010 Feb 12;2(2010). doi:10.3402/jom. v2i0.2127. 9. Xu J, Li Y, Gan F, Du Y, Yao Y. Salivary glands: Potential reservoirs for COVID-19 asymptomatic infection. J Dent Res 2020 Jul;99(8):989. doi: 10.1177/0022034520918518. Epub 2020 Apr 9. 10. Xu H, Zhong L, Deng J, et al. High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa. Int J Oral Sci 2020;12(1):1–5. doi:10.1038/s41368-0200074-x. 11. Zou X, Chen K, Zou J, Han P, Hao J, Han Z. Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection. Front Med 2020 Apr;14(2):185– 192. doi:10.1007/s11684-020-0754-0. Epub 2020 Mar 12. PMCID: PMC7088738. 12. Sapkota D, Søland TM, Galtung HK, et al. COVID-19 salivary signature: Diagnostic and research opportunities. J Clin Pathol 2020 Aug 7;jclinpath-2020-206834. doi: 10.1136/ jclinpath-2020-206834. Online ahead of print. 13. Zhong M, Lin B, Gao H, et al. Significant expression of FURIN and ACE2 on oral epithelial cells may facilitate the efficiency of SARS-CoV-2 entry. bioRxiv 2020 Apr:2020.04.18.047951. doi:10.1101/2020.04.18.047951. 14. Bar-On YM, Flamholz A, Phillips R, Milo R. SARS-CoV-2 (COVID-19) by the numbers. Elife 2020 Apr 2;9:e57309. doi:10.7554/eLife.57309. PMCID: PMC7224694. 15. Luo L, Liu D, Liao X, et al. Modes of contact and risk of transmission in COVID-19 among close contacts. medRxiv 2020 Mar: 2020.03.24.20042606. doi:10.1101/2020.03

.24.20042606. 16. KKW To, Tsang OTY, Chik-Yan Yip C, et al. Consistent detection of 2019 novel coronavirus in saliva. Clin Infect Dis Aug 71(15):841–843. doi:10.1093/cid/ciaa149. 17. Kojima N, Turner F, Klausner. Self-collected oral fluid and nasal swabs demonstrate comparable sensitivity to clinician collected nasopharyngeal swabs for coronavirus 2019 detection. Clin Infect Dis 2021 Nov 2;73(9):e3106–e3109. doi: 10.1093/cid/ciaa1589. 18. Williams E, Bond K, Zhang B, Putland M, Williamson DA. Saliva as a noninvasive specimen for detection of SARSCoV-2. J Clin Microbiol 2020 Jul 23;58(8):e00776–20. doi: 10.1128/JCM.00776-20. Print 2020 Jul 23. PMCID: PMC7383524. 19. Zhang W, Du RH, Li B, et al. Molecular and serological investigation of 2019-nCoV infected patients: Implication of multiple shedding routes. Emerg Microbes Infect 2020;9(1):386–389. doi:10.1080/22221751.2020.17290 71. PMCID: PMC7048229. 20. Chen L, Zhao J, Peng J, et al. Detection of 2019-nCoV in saliva and characterization of oral symptoms in COVID-19 patients. SSRN Electron J 2020 Apr:3556665. doi:10.2139/ ssrn.3556665. 21. Earar K, Arbune M, Schipor O, et al. Oral mucosa Gate for COVID-19 infection and correlation with chemical structures of the biocides. Rev Chim 2020;71(4):410–415. doi:10.37358/RC.20.4.8081. 22. Bao L, Zhang C, Dong J, Zhao L, Li Y, Sun J. Oral Microbiome and SARS-CoV-2: Beware of Lung Coinfection. Front Microbiol 2020;11:1840. doi:10.3389/ fmicb.2020.01840. PMCID: PMC7411080. 23. Panagakos F, Scannapieco FA. Periodontal inflammation: From gingivitis to systemic disease? Compend Contin Educ Dent 2004;25(7 Suppl 1):16–25. doi:10.5772/37923. 24. Pan L, Mu M, Yang P, et al. Clinical characteristics of COVID-19 patients with digestive symptoms in Hubei, China: A descriptive, cross-sectional, multicenter study. Am J Gastroenterol 2020;115(5):766–773. doi:10.14309/ ajg.0000000000000620. 25. Centers for Disease Control and Prevention. Transmission of coronavirus disease 2019 (COVID-19). 26. Peng X, Xu X, Li Y, Cheng L, Zhou X, Ren B. Transmission routes of 2019-nCoV and controls in dental practice. Int J Oral Sci 2020;12(1):1–6. doi:10.1038/s41368-020-0075-9. 27. Wang WK, Chen SY, Liu IJ, et al. Detection of SARSassociated coronavirus in throat wash and saliva in early diagnosis. Emerg Infect Dis 2004;10(7):1213–1219. doi:10.3201/eid1007.031113. PMCID: PMC3323313. 28. To KKW, Tsang OTY, Leung WS, 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;20(5):565–574. doi:10.1016/S14733099(20)30196-1. 29. Yoon JG, Yoon J, Song JY, et al. Clinical significance of a high SARS-CoV-2 viral load in the saliva. J Korean Med Sci 2020;35(20):e195. doi:10.3346/JKMS.2020.35.E195. 30. Yu ITS, Li Y, Wong TW, et al. Evidence of Airborne Transmission of the Severe Acute Respiratory Syndrome Virus. N Engl J Med 2004;350(17):1731–1739. doi:10.1056/ NEJMoa032867. 31. Zhang H, Li X, Ma R, et al. Airborne spread and infection

of a novel swine-origin influenza A (H1N1) virus. Virol J 2013;10(1):204. doi:10.1186/1743-422X-10-204. PMCID: PMC3700749. 32. 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). doi:10.1038/s41368-020-0080-z. 33. 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. Epub 2020 Feb 6. PMCID: PMC7132493. 34. Roy CJ, Milton DK. Airborne transmission of communicable infection — the elusive pathway. N Engl J Med 2004 Apr 22;350(17):1710–2. doi: 10.1056/NEJMp048051. 35. Yuan L, Zhi N, Yu C, et al. Aerodynamic characteristics and RNA concentration of SARS-CoV-2 aerosol in Wuhan Hospitals during COVID-19 outbreak. Biorxiv 2020 Mar. doi:10.1101/2020.03.08.982637. 36. Epstein JB, Chow K, Mathias R. Dental procedure aerosols and COVID-19. Lancet Infect Dis 2020;0(0). doi:10.1016/ S1473-3099(20)30636-8. 37. Marui VC, Souto MLS, Rovai ES, Romito GA, Chambrone L, Pannuti CM. Efficacy of preprocedural mouthrinses 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. 38. Liu L, Wei Q, Alvarez X, et al. Epithelial cells lining salivary gland ducts are early target cells of severe acute respiratory syndrome coronavirus infection in the upper respiratory tracts of rhesus macaques. J Virol 2011 Apr;85(8):4025–30. doi: 10.1128/JVI.02292-10. Epub 2011 Feb 2. 39. Farshidfar N, Hamedani S. Hyposalivation as a potential risk for SARS-CoV-2 infection: Inhibitory role of saliva. Oral Dis 2020 Apr 29;10.1111/odi.13375. doi: 10.1111/ odi.13375. Online ahead of print. 40. Iwabuchi H, Fujibayashi T, Yamane GY, Imai H, Nakao H. Relationship between hyposalivation and acute respiratory infection in dental outpatients. Gerontology 2012;58(3):205– 11. doi: 10.1159/000333147. Epub 2011 Nov 18. 41. Pedersen AM, Bardow A, Jensen SB, Nauntofte B. Saliva and gastrointestinal functions of taste, mastication, swallowing and digestion. Oral Dis 2002 May;8(3):117–29. doi: 10.1034/j.1601-0825.2002.02851.x.v. 42. Tschoppe P, Wolgin M, Pischon N. Etiologic factors of hyposalivation and consequences for oral health. Quintessence Int 2010 Ap;41(4):321–333. 43. Patel R, Babady E, Theel ES, et al. Report from the American society for microbiology COVID-19 international summit, 23 March 2020: Value of diagnostic testing for SARSCoV-2/COVID-19. mBio 2020 Mar 26;11(2):e00722–20. doi: 10.1128/mBio.00722-20. 44. To KKW, Yip CCY, Lai CYW, et al. Saliva as a diagnostic specimen for testing respiratory virus by a point-of-care molecular assay: A diagnostic validity study. Clin Microbiol Infect 2019 Mar;25(3):372–378. doi: 10.1016/j. cmi.2018.06.009. Epub 2018 Jun 12. 45. 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. 46. Hanson KE, Barker AP, Hillyard DR, et al. Self-collected anterior nasal and saliva specimens versus health care workercollected nasopharyngeal swabs for the molecular detection of M ARC H 2 0 2 1

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SARS-CoV-2. J Clin Microbiol 2020 Oct 21;58(11):e01824– 20. doi: 10.1128/JCM.01824-20. Print 2020 Oct 21. 47. Wyllie AL, Fournier J, Casanovas-Massana A, et al. Saliva or nasopharyngeal swab specimens for detection of SARSCoV-2. N Engl J Med 2020 Sep 24;383(13):1283–1286. doi: 10.1056/NEJMc2016359. Epub 2020 Aug 28. 48. Lisboa Bastos M, Tavaziva G, Abidi SK, et al. Diagnostic accuracy of serological tests for COVID-19: Systematic review and meta-analysis. BMJ 2020;370:2516. doi:10.1136/bmj. m2516. 49. Vogels CB, Brackney DE, Wang J, et al. SalivaDirect: Simple and sensitive molecular diagnostic test for SARSCoV-2 surveillance one sentence summary. medRxiv 2020 Aug:2020.08.03.20167791. doi:10.1101/2020.08.03.2 0167791. 50. Sheba Medical Center. Pilot program for rapid COVID-19 testing to be held at Sheba. www.shebaonline.org/pilotprogram-for-rapid-covid-19-testing-to-be-held-at-sheba. August 2020. Accessed Aug. 24, 2020. 51. Song J, Cheng W, Nie M, et al. Partial Leidenfrost Evaporation-Assisted Ultrasensitive Surface-Enhanced Raman Spectroscopy in a Janus Water Droplet on Hierarchical Plasmonic Micro-/Nanostructures. ACS Nano 2020 Aug 25;14(8):9521–9531. doi: 10.1021/acsnano.0c04239. Epub 2020 Jul 6. 52. Mak GC, Cheng PK, Lau SS, et al. Evaluation of rapid antigen test for detection of SARS-CoV-2 virus. J Clin Virol 2020 Aug;129:104500. doi: 10.1016/j.jcv.2020.104500. Epub 2020 Jun 8. 53. Scohy A, Anantharajah A, Bodéus M, Kabamba-Mukadi B, Verroken A, Rodriguez-Villalobos H. Low performance of rapid antigen detection test as frontline testing for COVID-19 diagnosis. J Clin Virol 2020 Aug;129:104455. doi: 10.1016/j.jcv.2020.104455. Epub 2020 May 21. 54. Fernandes LL, Pacheco VB, Borges L, et al. Saliva in the diagnosis of COVID-19: A review and new research directions. J Dent Res 2020 Dec;99(13):1435–1443. doi: 10.1177/0022034520960070. Epub 2020 Sep 16. 55. Lechien JR, Chiesa-Estomba CM, De Siati DR, et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): A multicenter European study. Eur Arch Otorhinolaryngol 2020 Aug;277(8):2251–2261. doi: 10.1007/s00405-020-05965-1. Epub 2020 Apr 6. 56. Tong JY, Wong A, Zhu D, Fastenberg JH, Tham T. The prevalence of olfactory and gustatory dysfunction in COVID-19 patients: A systematic review and meta-analysis. Otolaryngol Head Neck Surg 2020 Jul;163(1):3–11. doi: 10.1177/0194599820926473. Epub 2020 May 5. 57. Giacomelli A, Pezzati L, Conti F, et al. Self-reported olfactory and taste disorders in patients with severe acute respiratory coronavirus 2 infection: A cross-sectional study. Clin Infect Dis 2020 Jul 28;71(15):889–890. doi: 10.1093/cid/ ciaa330. 58. Rezaei F, Mozaffari HR, Tavasoli J, Zavattaro E, Imani MM, Sadeghi M. Evaluation of serum and salivary interleukin-6 and interleukin-8 levels in oral squamous cell carcinoma patients: Systematic review and meta-analysis. J Interf Cytokine Res 2019 Dec;39(12):727–739. doi: 10.1089/jir.2019.0070. Epub 2019 Jul 17. 59. Beltrán-Corbellini Á, Chico-García JL, Martínez-Poles J, et al. Acute-onset smell and taste disorders in the context of COVID-19: A pilot multicenter PCR-based case-control study.

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Eur J Neurol 2020 Sep;27(9):1738–1741. doi: 10.1111/ ene.14273. Epub 2020 May 16. 60. Levinson R, Elbaz M, Ben-Ami R, et al. Time course of anosmia and dysgeusia in patients with mild SARS-CoV-2 infection. Infect Dis (London) 2020 Aug;52(8):600–602. doi: 10.1080/23744235.2020.1772992. 61. Ellul MA, Benjamin L, Singh B, et al. Neurological associations of COVID-19. Lancet Neurol 2020 Sep;19(9):767–783. doi: 10.1016/S1474-4422(20)302210. Epub 2020 Jul 2. 62. Chern A, Famuyide AO, Moonis G, Lalwani AK. Sialadenitis: A possible early manifestation of COVID-19. Laryngoscope 2020 Aug:29083. doi:10.1002/lary.29083. 63. Capaccio P, Pignataro L, Corbellino M, Popescu-Dutruit S, Torretta S. Acute parotitis: A possible precocious clinical manifestation of SARS-CoV-2 infection? Otolaryngol Head Neck Surg 2020 Jul;163(1):182–183. doi: 10.1177/0194599820926992. Epub 2020 May 5. 64. Rocha BA, Souto GR, Grossmann S de MC, et al. Viral enanthema in oral mucosa: A possible diagnostic challenge in the COVID‐19 pandemic. Oral Dis 2020 Jun 10;10.1111/ odi.13473. doi: 10.1111/odi.13473. Online ahead of print. 65. Jimenez-Cauhe J, Ortega-Quijano D, De Perosanz-Lobo D, et al. Enanthem in patients with COVID-19 and skin rash. JAMA Dermatol 2020 Jul 15;156(10):1134–1136. doi: 10.1001/jamadermatol.2020.2550. Online ahead of print. 66. Chaux-Bodard AG, Deneuve S, Desoutter A. Oral manifestation of COVID-19 as an inaugural symptom? J Oral Med Oral Surg 2020;26(2):18. doi:10.1051/ mbcb/2020011. 67. Martín Carreras‐Presas C, Amaro Sánchez J, López‐ Sánchez AF, Jané‐Salas E, Somacarrera Pérez ML. Oral vesiculobullous lesions associated with SARS‐CoV‐2 infection. Oral Dis 2020 May 5;10.1111/odi.13382. doi: 10.1111/ odi.13382. Online ahead of print. 68. Ciccarese G, Drago F, Boatti M, Porro A, Muzic SI, Parodi A. Oral erosions and petechiae during SARS-CoV-2 infection. J Med Virol 2020 Jun 24;10.1002/jmv.26221. doi: 10.1002/ jmv.26221. Online ahead of print. 69. Ansari R, Gheitani M, Heidari F, Heidari F. Oral cavity lesions as a manifestation of the novel virus (COVID‐19). Oral Dis 2020 Jun 8. doi: 10.1111/odi.13465. Online ahead of print. 70. Cebeci Kahraman F, Çaşkurlu H. Mucosal involvement in a COVID‐19‐positive patient: A case report. Dermatol Ther 2020 Jul;33(4):e13797. doi: 10.1111/dth.13797. Epub 2020 Jul 3. 71. Amorim dos Santos J, Normando AGC, Carvalho da Silva RL, et al. Oral mucosal lesions in a COVID-19 patient: New signs or secondary manifestations? Int J Infect Dis 2020 Aug;97:326–328. doi:10.1016/j.ijid.2020.06.012. Epub 2020 Jun 9. 72. Soares CD, de Carvalho RA, de Carvalho KA, de Carvalho MGF, de Almeida OP. Letter to editor: Oral lesions in a patient with COVID-19. Med Oral Patol Oral y Cir Bucal 2020;25(4):e563-e564. doi:10.4317/medoral.24044. 73. Jimenez-Cauhe J, Ortega-Quijano D, Carretero-Barrio I, et al. Erythema multiforme-like eruption in patients with COVID-19 infection: Clinical and histological findings. Clin Exp Dermatol 2020 Oct;45(7):892–895. doi: 10.1111/ced.14281. Epub 2020 Jun 25. 74. Patel J, Woolley J. Necrotizing periodontal disease: Oral manifestation of COVID‐19. Oral Dis 2020 Jun 7;10.1111/

odi.13462. doi: 10.1111/odi.13462. Online ahead of print. 75. Tomo S, Miyahara GI, Simonato LE. Oral mucositis in a SARS‐CoV‐2‐infected patient: Secondary or truly associated condition? Oral Dis 2020 Jul 29. doi: 10.1111/odi.13570. Online ahead of print. T HE CORRE S P ON DIN G AU T HOR , Shervin Molayem, DDS, can be reached at drmolayem@synergyspecialists.com.

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The Mouth-COVID-19 Connection: The Importance of the Oral Cavity for the Coronavirus Disease — Part II Shervin Molayem, DDS, and Carla Cruvinel Pontes, DDS, MsC, PhD

abstract Background: The pandemic has significantly disrupted dental practice. However, the dental community has risen to the challenges of maintaining oral health care delivery. Untreated oral conditions can adversely affect the systemic environment, influencing respiratory conditions and COVID-19. Types of studies reviewed: This study was designed as a narrative review. Medline, Scopus and Google Scholar were searched up to January 2021 for articles in English that addressed the role played by the oral cavity and saliva in the coronavirus disease, with particular focus on the importance of oral hygiene. All relevant scientific articles were included. Results: Several studies have linked poor plaque control to worse lung function and pneumonia, particularly in hospitalized patients and institutionalized elderly. COVID-19 patients with poor plaque control can carry the virus for longer periods. Because saliva can be highly infective, pretreatment oral rinsing has been recommended to decrease the viral load and transmission of COVID-19. Practical implications: Findings from this review suggest that promoting oral health and plaque control are vital to prevent respiratory diseases and potentially decrease the severity of COVID-19. Keywords: Mouth COVID-19, saliva COVID-19, oral health COVID-19, oral inflammation

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he COVID-19 pandemic caused by the novel SARS-CoV-2 has disrupted multiple health care professions, including dentistry.1 The dental community has slowly risen to the challenges imposed by the coronavirus disease in order to maintain the delivery of oral health care. Untreated oral conditions can become a challenge, as they can cause pain, affect important functions, such as speech and mastication, decrease general quality of life and contribute to systemic inflammation.2 The coronavirus disease is adversely affected by systemic inflammation, this is why dentists have an important role to play in the elimination of infection and inflammation in the mouth.3 Due to the frequent exposure to body fluids and close proximity to patients, dental treatments during the pandemic require strict use of personal protective equipment (PPE) and extraordinary infection control measures to decrease the risk of transmission of COVID-19 to dentists, dental staff and patients.4 Findings from previous studies have shown that poor plaque control negatively influences the prevalence and severity of respiratory diseases such as pneumonia. In a case report from Japan, the persistence of SARS-CoV-2 in saliva samples for extended periods after clinical recovery suggests a link between viral shedding and the oral biofilm.5 Furthermore, secondary bacterial infection can be a challenge in the context of COVID-19, and the oral biofilm can act as a reservoir for pathogenic bacteria.6 Given the spread of COVID-19, the extent of its complications and the link between poor oral hygiene and increased risk for respiratory infections, adequate plaque control can help prevent COVID-19 secondary infection and complications, with special relevance for elderly residents and hospitalized patients.7

Considering the infectivity of saliva droplets, mouthwashes constitute a promising approach to prevent viral replication in the oral cavity and oropharynx.8 Oral rinses can potentially inactivate and decrease the number of infective virus particles in mucous membranes.9 The use of antiseptic oral rinses has been part of routine oral health care, particularly pre- and postoperatively, as a measure to reduce the number of oral microorganisms.10 During the pandemic, the American Dental Association (ADA), the Centers for Disease Control and Prevention (CDC) and other regulating bodies around the globe have recommended preprocedural oral rinsing with hydrogen peroxide or iodine before delivery of oral health care to reduce the risk of COVID-19 transmission.4 In part I of this review, the presence of SARS-Cov-2 in the oral cavity, the role of saliva in the coronavirus disease, diagnostic considerations of COVID-19 and alterations in the oral cavity of COVID-19 patients are discussed. In this part of this review, the role of the oral cavity in COVID-19 is further explored, including the use of mouthwashes to decrease transmission, the importance of the oral biofilm for respiratory infections and COVID-19 and the contribution of oral conditions to systemic inflammation.

Poor Oral Hygiene, Oral Microbiome and Risk for Pulmonary Infection

The oral microbiome is composed of more than 700 different species of microorganisms. Poor oral hygiene favors plaque accumulation and increases bacterial load. Because there is a frequent microbial exchange between the lungs and the oral cavity through aspiration and inhalation, oral microorganisms can promote infection of the lower respiratory tract, which can possibly contribute to increased severity of COVID-19.6,7

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Oral Hygiene, Respiratory Function and Pneumonia

Adequate oral hygiene has been linked to lower incidence and mortality due to pneumonia.11 In ICU patients, oral hygiene measures resulted in decreased incidence of ventilator-induced pneumonia.12 In a study on ventilationassociated pneumonia, plaque accumulation and poor salivary flow were positively associated with increased risk for respiratory infection in critically ill patients.13 Analysis of respiratory tract samples from ICU patients on mechanical ventilation detected the presence of the periodontal pathogens Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Fusobacterium nucleatum, Treponema denticola and Veillonella parvula. The bacterial load increased with longer intubation time, and the authors suggested that oral bacteria can contribute to ventilator-associated pneumonia.14 In the absence of adequate plaque control, periodontal pathogens accumulate and the consequent dysbiosis in the oral cavity and periodontal deterioration can negatively affect respiratory function, leading to a higher risk for pneumonia.15 In a large group of dentate male participants from Northern Ireland, there was a significant association between chronic periodontitis and worse respiratory function, measured as the forced expiratory volume in one second.16 In another study on institutionalized elderly, the risk of pneumonia increased with poor oral hygiene, as it led to the accumulation of the respiratory pathogens H. influenzae and P. aeruginosa in the tongue and dental calculus, suggesting that plaque and calculus removal can decrease the risk for pneumonia.17 These findings have been corroborated by many studies that report lower risk for respiratory infections linked to adequate oral hygiene in both hospitalized and home-care patients.18–21

In a systematic review, oral hygiene decreased incidence and mortality from pneumonia in elderly hospitalized individuals and nursing home residents. The authors concluded that in every 10 deaths from pneumonia, one can be prevented through simple oral hygiene measures.22

COVID-19, Secondary Infections and Poor Oral Hygiene The development of COVID-19 complications in young and otherwise healthy individuals has led to the search for alternative risk factors. In a study from

In ICU patients, oral hygiene measures resulted in decreased incidence of ventilator-induced pneumonia.

Zhou et al. (2020), half of the COVID19-related deaths were associated with secondary infection.23 Results from other studies on the use of antibiotics further confirm the high prevalence of bacterial infections and their negative impact on mortality rates of COVID-19.24,25 While many studies have included antibiotics in their treatment approaches, few have discussed potential sources for bacterial infection in COVID-19.7 The literature provides compelling evidence on the detrimental role of poor oral hygiene in general health in healthy individuals and in those who suffer from chronic diseases, such as diabetes and cardiovascular disease, which are comorbidities for COVID-19.26 In COVID-19 patients, the risk for coinfection is likely to increase with poor oral hygiene, coughing and mechanical

ventilation, as those mechanisms can facilitate the entrance of oral microorganisms into the upper and lower respiratory tract. It has also been suggested that lung hypoxia, which is typically present in COVID-19, can promote the growth of anaerobic and facultative oral bacteria in the lungs.6 Segal et al. (2016) reported that 50% of bronchoalveolar lavage samples from healthy subjects contained oral bacteria, suggesting a close relationship between the oral microbiome and the lungs. In COVID-19 patients and pneumonia patients, high levels of Capnocytophaga, Veillonella and other oral bacteria were detected in bronchoalveolar lavage samples.27 In Japan, eight COVID-19 patients were followed after hospital admission. All patients had underlying systemic diseases, had overcome the acute phase of the disease, but remained positive for the virus for an average of 15.1 days. However, in two patients, the viral shedding period was much longer than the average (44 and 53 days). Those two patients did not perform oral hygiene during their hospital stay due to mental and psychological issues. After the introduction of monitored daily oral hygiene, both patients tested negative after four to nine days.5 Thus, previous research provides evidence that dental plaque can function as a viral and bacterial reservoir, increasing the risk for pulmonary infection in COVID-19 patients. Bao et al. suggest that lung hypoxia, a common COVID-19 symptom, can be beneficial for oral facultative and anaerobe bacteria in the respiratory tract.6 The importance of plaque control cannot be underestimated, particularly in the context of transmissibility, hospitalization and mechanical intubation. Based on findings from studies on dental plaque and respiratory conditions, adequate oral hygiene is vital to decrease the risk of lung infection, including COVID 19, M ARC H 2 0 2 2

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particularly in hospitalized patients and home-care residents. Poor oral hygiene can influence lung conditions directly through changes in the oral microbiome that favor the accumulation of periodontal and respiratory pathogens. It can also increase the risk of lung disease indirectly by promoting periodontal disease and consequent systemic inflammation.

Oral Rinses for Prevention of COVID-19 Transmission and Infection

Oral rinses have been investigated due to their potential to decrease the viral load, severity of the disease and transmission, given that the virus accumulates in the oral cavity, nasal and pharyngeal area before symptoms develop; salivary glands present high expression of ACE-2 receptor; and saliva droplets represent a crucial route of transmission.28 Previous studies on coronaviruses indicate that oral rinses targeting the viral lipid envelope can have a virucidal effect.9

the viral load increased again after two to four hours.34 At this point, the benefits of CHX in the reduction of SARS-CoV-2 in the oral cavity are controversial.

Povidone-Iodine

Povidone-iodine has been widely used as an antiseptic and mouthwash because of the antimicrobial and virucidal properties of iodine against nonenveloped and enveloped viruses. Multiple in vitro studies have demonstrated the effectiveness of povidoneiodine in the inactivation of coronaviruses.35 In vitro, povidone-iodine was able to

Multiple in vitro studies have demonstrated the effectiveness of povidone iodine in the inactivation of coronaviruses.

Chlorhexidine

As a well-known disinfectant and antiseptic, chlorhexidine (CHX) presents broad-spectrum antimicrobial activity against gram-negative bacteria, some viruses and fungus.29,30 Although pretreatment oral rinse with CHX has been suggested to reduce transmission of microorganisms through dental aerosols,31 the efficacy of its antiviral properties has not been fully investigated. A 30-second exposure to 0.12% CHX has been shown to inactivate certain enveloped viruses in vitro, such as herpes simplex, cytomegalovirus, influenza A, parainfluenza and hepatitis.32 A study from Wood and Payne (1998) demonstrated that CHX was not able to inactivate human coronaviruses.33 Recently, CHX mouthwash effectively decreased the viral load of SARS-CoV-2 in the saliva of two hospitalized COVID-19 patients. However, this effect was transient and 178

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inactivate SARS-CoV-2 when exposed for at least 15 seconds with a minimum concentration of 0.5%.36 Contrary to CHX, oral rinsing with povidoneiodine has not been linked to teeth discoloration nor taste alterations, with substantivity in the oral cavity estimated at four hours. The contraindications for povidone-iodine include allergy to iodine, active thyroid disease, pregnancy and radioactive iodine therapy.9

Quaternary Ammonium Compounds

Different quaternary ammonium compounds have been used in mouthwashes, including benzalkonium chloride, cetylpyridinium chloride and dequalinium chloride, because of their effect on cell surface lipids and proteins and plaque inhibiting effect. Cetylpyridinium

chloride (CPC) has been shown to destroy influenza virus’s envelope in vitro and in vivo and to decrease the incidence of upper respiratory infections in healthy adults.37,38 However, the literature is scarce regarding the virucidal effects of these quaternary compounds on SARS-CoV-2.

Ethanol

Oral rinses containing ethanol (21% to 26%) combined or not with essential oils such as eucalyptol, menthol and thymol have shown inactivation of enveloped viruses such as herpes simplex and influenza virus, both in vitro and in clinical studies.39,40 In a study from Meiller et al., when used as an oral rinse, Listerine (ethanol-based mouthwash) reduced the load of herpes virus in saliva and the effect lasted for at least 30 minutes, suggesting a potential beneficial effect against SARS-CoV-2.40

Hydrogen Peroxide

Hydrogen peroxide is an oxidative agent that has been used in dentistry for many years. Through the production of free oxygen radicals, hydrogen peroxide can destroy viral lipid membranes. However, in lower concentrations, it is quickly broken down by salivary catalase. In a study on periodontitis treatment, regular use of 1% to 1.5% hydrogen peroxide was not linked to side effects on the oral mucosa.41 Hydrogen peroxide has shown virucidal activity against coronaviruses when used as a surface disinfectant,42 and because SARS-CoV-2 seems to be susceptible to oxidation, it has been suggested that rinsing with 1% hydrogen peroxide can decrease the viral load in saliva.4 During the pandemic, oral rinsing with 1% hydrogen peroxide or 0.2% povidone-iodine has been recommended as a preprocedure oral rinse by the American Dental Association and other regulatory bodies from different countries.43

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Comparative Studies

When hydrogen peroxide (1.5% and 3.0% for 30 seconds) was compared to povidone-iodine (at least 0.5% for a minimum of 30 seconds) in vitro, it was marginally effective as opposed to the high effectiveness of povidone-iodine.44 In a recent in vitro study from Germany, eight commercially available mouthwashes were evaluated for their ability to inactivate SARS-CoV-2. All evaluated products had a beneficial effect on viral load, but the most effective were the formulations containing ethanol, povidone-iodine and dequalinium and benzalkonium chloride, which nearly eliminated the virus in saliva.45 Povidone-iodine (0.5% for a minimum of 30 seconds) presents the highest amount of evidence in terms of antiviral activity against SARS-CoV-2 in vitro. Oral rinses containing hydrogen peroxide, ethanol and dequalinium/benzalkonium chloride also seem to have been effective in vitro virucidal effects. In conclusion, there is a scarcity of clinical data on the efficacy of mouthwashes in COVID-19 patients, and clinical trials are warranted.

Oral Cavity as a Source of Inflammation Periodontitis

Elevated levels of pro-inflammatory cytokines, particularly interleukin 6 (IL-6), have been linked to respiratory complications in COVID-19 patients. In hospitalized COVID-19 patients, IL-6 levels above 80 pg/ml were a strong predictor for respiratory failure and the consequent need for mechanical ventilation.46 As highlighted in a previous review from our group, because serum IL-6 levels are elevated as a consequence of gingival inflammation, untreated periodontitis can be an overlooked source of inflammation. Hence, because periodontal treatment can decrease systemic IL-6 levels, it should be regarded as an essential part of general health care

to decrease inflammation and the risk for lung complications in COVID-19 patients.3

Pulpitis and Periapical Lesions

Pulpitis and periapical lesions are typically caused by infection originating from caries lesions. In vitro studies report that pulp cells and cells from periapical lesions increase IL-6 production when exposed to bacterial products.47 IL-6 has been identified in inflamed pulp and periapical tissues, and its expression seems to be proportional to the size of the lesion and clinical symptoms.48 A meta-analysis

Topical corticosteroid treatment of oral lichen planus has been reported to decrease IL-6 levels.

has reported increased local and serum CRP, IL-1 and IL-6 expression in patients with periapical lesions.49 Collectively, these data indicate that periapical lesions can contribute to systemic inflammation.50,51

Mucosal Lesions

Oral lichen planus is a T-cell mediated autoimmune disorder characterized by erosive or white lesions in the oral mucosa, being associated with higher IL-6 levels in saliva and serum (particularly ulcerative forms).52 In a study from Larsen et al. (2017), patients with oral lichen planus, oral lichenoid lesions and generalized stomatitis presented higher IL-6 levels than healthy controls, with oral lichen planus presenting the highest expression of IL-6 (average of

89.6 pg/ml).53 Topical corticosteroid treatment of oral lichen planus has been reported to decrease IL-6 levels.54 Cytokines have also been implied in the pathophysiology of oral cancer, particularly oral squamous cell carcinoma (OSCC), which accounts for over 90% of all cancers in the oral cavity. Higher serum and saliva IL-6 levels have been associated with increased severity and worse prognosis of OSCC.50,55

Sleep Apnea

Obstructive sleep apnea, defined as repetitive closure of the upper airway during sleep, leads to interrupted sleep, lower alveolar ventilation and hypoxia. This sleep disorder has been linked to increased risk for periodontal disease, inflammation in the oral mucosa and upper airways and systemic inflammation characterized by higher expression of pro-inflammatory markers in serum. Furthermore, patients with sleep apnea present an elevated risk for cardiovascular disease.56,57 Thus, given the serious local and systemic consequences of sleep apnea, which include changes in the airways, it can potentially increase the risk for COVID-19 complications. Even though most studies on the link between oral diseases and systemic inflammation have focused on periodontitis, other conditions have the potential to further increase IL-6 levels, although these associations have been investigated to a lesser degree. Thus, the importance of maintaining good oral health goes beyond the oral cavity. It does not only affect the capacity to eat and chew and the nutritional intake, but it can also negatively affect general health, particularly COVID-19, through mechanisms that involve local chronic infection and inflammation. As the literature on the importance of cytokine storms for COVID-19 increases, so does M ARC H 2 0 2 2

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the responsibility of dental practitioners in preventing and treating oral conditions that can improve general inflammation.

Take-Home Message

Oral hygiene. Deficient plaque control can cause oral dysbiosis, leading to the accumulation of periodontal and respiratory pathogens in the oral cavity, higher risk for periodontal disease and pneumonia, potentially contributing to increased severity of COVID-19. The oral biofilm can also harbor SARSCoV-2, which is important in the context of viral transmission and infection. Oral rinses. Authorities around the world, including the ADA, recommend pretreatment oral rinsing to decrease the viral load, severity and transmission of COVID-19. The two most recommended agents are povidone-iodine (0.2%) and hydrogen peroxide (1%), although the evidence is still limited. Oral inflammation. Oral conditions such as periodontitis, periapical lesions, oral lichen planus, oral cancer and obstructive sleep apnea can lead to systemic inflammation, which can be detrimental to COVID-19. Untreated oral diseases need to be regarded as potential hidden sources of systemic inflammation. Oral care. Interventions to restore oral health and prevent disease are crucial to maintaining oral and general health. Measures to control plaque, remove calculus and eliminate infection and inflammation are essential to decrease the risk for respiratory infections and the severity of COVID-19.

Conclusion

Given the importance of the oral cavity and saliva for the coronavirus disease, mouthwashes are a promising 180

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approach to decrease the viral load according to in vitro studies, but there is an urgent need for clinical studies. Poor oral hygiene is highly detrimental for oral health, and it also has a negative impact on lung conditions, potentially increasing the prevalence and severity of pneumonia and COVID-19. Dental plaque and calculus can function as a reservoir for respiratory pathogens, which can increase the risk for secondary bacterial infection in COVID-19. Finally, the mouth can become a source of inflammation if oral diseases

Untreated oral diseases need to be regarded as potential hidden sources of systemic inflammation.

and conditions are left untreated, with the potential to contribute to COVID-19 complications and other respiratory diseases. Findings from this review suggest that dentists have a crucial role to play in the promotion of oral health during the pandemic. n RE FE RE N CE S 1. Marra MA, Jones SJM, Astell CR, et al. The genome sequence of the SARS-associated coronavirus. Science 2003 May 30;300(5624):1399–1404. doi:10.1126/ science.1085953. Epub 2003 May 1. 2. Jin L, Lamster I, Greenspan J, Pitts N, Scully C, Warnakulasuriya S. Global burden of oral diseases: Emerging concepts, management and interplay with systemic health. Oral Dis 2016 Oct;22(7):609–619. doi:10.1111/odi.12428. 3. Molayem S, Pontes C. The mouth-COVID connection: Il-6 levels in periodontal disease — potential role in COVID-19related respiratory complications. J Calif Dent Assoc 2020 Oct 48(10):485–499. doi: 10.35481/jcda-48-10-01. 4. Peng X, Xu X, Li Y, Cheng L, Zhou X, Ren B. Transmission routes of 2019-nCoV and controls in dental practice. Int J Oral Sci 2020 Mar 3;12(1):1–6. doi:10.1038/s41368-020-

0075-9. 5. Warabi Y, Tobisawa S, Kawazoe T, et al. Effects of oral care on prolonged viral shedding in coronavirus disease 2019 (COVID‐19). Spec Care Dent 2020 Sep;40(5):470–474. doi:10.1111/scd.12498. 6. Bao L, Zhang C, Dong J, Zhao L, Li Y, Sun J. Oral microbiome and SARS-CoV-2: Beware of lung co-infection. Front Microbiol 2020 Jul 31;11:1840. doi:10.3389/ fmicb.2020.01840. eCollection 2020. 7. Sampson V, Kamona N, Sampson A. Could there be a link between oral hygiene and the severity of SARSCoV-2 infections? Br Dent J 2020 Jun;228(12):971–975. doi:10.1038/s41415-020-1747-8. 8. Kirk-Bayley J, Challacombe S, Sunkaraneni V, Combes J. The use of povidone iodine nasal spray and mouthwash during the current COVID-19 pandemic may protect healthcare workers and reduce cross infection. SSRN Electron J March 2020. doi:10.2139/ssrn.3563092. 9. O’Donnell VB, Thomas D, Stanton R, et al. Potential role of oral rinses targeting the viral lipid envelope in SARS-CoV-2 infection. Function (Oxf) 2020;1(1):zqaa002. doi:10.1093/ function/zqaa002. Epub 2020 Jun 5. 10. Marui VC, Souto MLS, Rovai ES, Romito GA, Chambrone L, Pannuti CM. Efficacy of preprocedural mouthrinses 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. 11. Yoneyama T, Yoshida M, Ohrui T, et al. Oral care reduces pneumonia in older patients in nursing homes. J Am Geriatr Soc 2002 Mar;50(3):430–433. doi:10.1046/j.15325415.2002.50106.x. 12. Mori H, Hirasawa H, Oda S, Shiga H, Matsuda K, Nakamura M. Oral care reduces incidence of ventilatorassociated pneumonia in ICU populations. Intensive Care Med 2006 Feb;32(2):230–236. doi:10.1007/s00134-005-00144. Epub 2006 Jan 25. 13. Munro CL, Grap MJ, Elswick RK, McKinney J, Sessler CN, Hummel RS. Oral health status and development of ventilatorassociated pneumonia: A descriptive study. Am J Crit Care 2006;15(5):453–460. doi:10.4037/ajcc2006.15.5.453. 14. de Carvalho Baptista IM, Martinho FC, Nascimento GG, da Rocha Santos CE, Prado RF do, Valera MC. Colonization of oropharynx and lower respiratory tract in critical patients: Risk of ventilator-associated pneumonia. Arch Oral Biol 2018 Jan;85:64–69. doi:10.1016/j.archoralbio.2017.09.029. Epub 2017 Oct 2. 15. Kumar PS. From focal sepsis to periodontal medicine: A century of exploring the role of the oral microbiome in systemic disease. J Physiol 2017 Jan 15;595(2):465–476. doi:10.1113/JP272427. 16. Winning L, Patterson CC, Cullen KM, Kee F, Linden GJ. Chronic periodontitis and reduced respiratory function. J Clin Periodontol 2019 Mar;46(3):266–275. doi:10.1111/ jcpe.13076. 17. Hong CHL, Aung MM, Kanagasabai K, Lim CA, Liang S, Tan KS. The association between oral health status and respiratory pathogen colonization with pneumonia risk in institutionalized adults. Int J Dent Hyg 2018 May;16(2):e96– e102. doi:10.1111/idh.12321. Epub 2017 Nov 9. 18. 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(1):54–69.

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doi:10.1902/annals.2003.8.1.54. 19. Abe S, Ishihara K, Adachi M, Sasaki H, Tanaka K, Okuda K. Professional oral care reduces influenza infection in elderly. Arch Gerontol Geriatr Sep–Oct 2006;43(2):157–64. doi: 10.1016/j.archger.2005.10.004. Epub 2005 Dec 2. 20. Imsand M, Janssens JP, Auckenthaler R, Mojon P, Budtz-Jørgensen E. Bronchopneumonia and oral health in hospitalized older patients. A pilot study. Gerodontology 2002 Dec;19(2):66–72. doi:10.1111/j.17412358.2002.00066.x. 21. Quagliarello V, Ginter S, Han L, Van Ness P, Allore H, Tinetti M. Modifiable risk factors for nursing home-acquired pneumonia. Clin Infect Dis 2005 Jan 1;40(1):1–6. doi: 10.1086/426023. Epub 2004 Dec 1. 22. Sjögren P, Nilsson E, Forsell M, Johansson O, Hoogstraate J. A systematic review of the preventive effect of oral hygiene on pneumonia and respiratory tract infection in elderly people in hospitals and nursing homes: Effect estimates and methodological quality of randomized controlled trials. J Am Geriatr Soc 2008 Nov;56(11):2124–2130. doi:10.1111/ j.1532-5415.2008.01926.x. 23. Zhou F, Yu T, Du R, 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 28;395(10229):1054–1062. doi: 10.1016/S01406736(20)30566-3. Epub 2020 Mar 11. 24. Gautret P, Lagier JC, Parola P, et al. Hydroxychloroquine and azithromycin as a treatment of COVID-19: Results of an open-label non-randomized clinical trial. Int J Antimicrob Agents 2020 Jul;56(1):105949. doi: 10.1016/j. ijantimicag.2020.105949. Epub 2020 Mar 20. 25. Million M, Lagier JC, Gautret P, et al. Early treatment of COVID-19 patients with hydroxychloroquine and azithromycin: A retrospective analysis of 1061 cases in Marseille, France. Travel Med Infect Dis May–Jun 2020;35:101738. doi:10.1016/j.tmaid.2020.101738. 26. Olsen I, Yamazaki K. Can oral bacteria affect the microbiome of the gut? J Oral Microbiol 2019 Mar 18;11(1):1586422. doi: 10.1080/20002297.2019.1586422. eCollection 2019. 27. Shen Z, Xiao Y, Kang L, et al. Genomic diversity of severe acute respiratory syndrome-coronavirus 2 in patients with coronavirus disease 2019. Clin Infect Dis 2020 Jul 28;71(15):713–720. doi:10.1093/cid/ciaa203. 28. Herrera D, Serrano J, Roldán S, Sanz M. Is the oral cavity relevant in SARS-CoV-2 pandemic? Clin Oral Investig 2020 Aug;24(8):2925–2930. doi:10.1007/s00784-020-03413-2. 29. Figuero E, Herrera D, Tobías A, et al. Efficacy of adjunctive anti-plaque chemical agents in managing gingivitis: A systematic review and network meta-analyses. J Clin Periodontol 2019 Jul;46(7):723–739. doi:10.1111/ jcpe.13127. 30. Escribano M, Figuero E, Martín C, et al. Efficacy of adjunctive anti-plaque chemical agents: A systematic review and network meta-analyses of the Turesky modification of the Quigley and Hein plaque index. J Clin Periodontol 2016 Dec;43(12):1059–1073. doi:10.1111/jcpe.12616. Epub 2016 Oct 10. 31. Epstein JB, Chow K, Mathias R. Dental procedure aerosols and COVID-19. Lancet Infect Dis 2021 Apr;21(4):e73. doi: 10.1016/S1473-3099(20)30636-8. Epub 2020 Aug 10. 32. Bernstein D, Schiff G, Echler G, Prince A, Feller M, Briner W. In vitro virucidal effectiveness of a 0.12%-chlorhexidine

gluconate mouthrinse. J Dent Res 1990 Mar;69(3):874–876. doi:10.1177/00220345900690030901. 33. Wood A, Payne D. The action of three antiseptics/ disinfectants against enveloped and non-enveloped viruses. J Hosp Infect 1998 Apr;38(4):283–295. doi:10.1016/S01956701(98)90077-9. 34. Yoon JG, Yoon J, Song JY, et al. Clinical significance of a high SARS-CoV-2 viral load in the saliva. J Korean Med Sci 2020 May 25;35(20):e95. doi:10.3346/jkms.2020.35. e195. 35. Parhar HS, Tasche K, Brody RM, et al. Topical preparations to reduce SARS‐CoV‐2 aerosolization in head and neck mucosal surgery. Head Neck 2020 Jun;42(6):1268–1272. doi:10.1002/hed.26200. Epub 2020 Apr 25. 36. Bidra AS, Pelletier JS, Westover JB, Frank S, Brown SM, Tessema B. Rapid in vitro inactivation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) using povidone-iodine oral antiseptic rinse. J Prosthodont 2020 Jul;29(6):529–533. doi:10.1111/jopr.13209. Epub 202 Jun 16. 37. Popkin DL, Zilka S, Dimaano M, et al. Cetylpyridinium chloride (CPC) exhibits potent, rapid activity against influenza viruses in vitro and in vivo. Pathog Immun 2017;2(2):252. doi:10.20411/pai.v2i2.200. Epub 2017 Jun 26. 38. Mukherjee PK, Esper F, Buchheit K, et al. Randomized, double-blind, placebo-controlled clinical trial to assess the safety and effectiveness of a novel dual-action oral topical formulation against upper respiratory infections. BMC Infect Dis 2017 Jan;17(1):74. doi:10.1186/s12879-016-2177-8. 39. Dennison DK, Meredith GM, Shillitoe EJ, Caffesse RG. The antiviral spectrum of Listerine antiseptic. Oral Surg Oral Med Oral Pathol Oral Radiol 1995;79(4):442–448. doi:10.1016/S1079-2104(05)80124-6. 40. Meiller TF, Silva A, Ferreira SM, Jabra-Rizk MA, Kelley JI, DePaola LG. Efficacy of Listerine antiseptic in reducing viral contamination of saliva. J Clin Periodontol 2005 Apr;32(4):341–346. doi:10.1111/j.1600051X.2005.00673.x. 41. Gusberti FA, Sampathkumar P, Siegrist BE, Lang NP. Microbiological and clinical effects of chlorhexidine digluconate and hydrogen peroxide mouthrinses on developing plaque and gingivitis. J Clin Periodontol 1988 Jan;15(1):60– 67. doi:10.1111/j.1600-051X.1988.tb01556.x. 42. Omidbakhsh N, Sattar SA. Broad-spectrum microbicidal activity, toxicologic assessment, and materials compatibility of a new generation of accelerated hydrogen peroxide-based environmental surface disinfectant. Am J Infect Control 2006 Jun;34(5):251–257. doi:10.1016/j.ajic.2005.06.002. 43. Jamal M, Shah M, Almarzooqi SH, et al. Overview of transnational recommendations for COVID‐19 transmission control in dental care settings. Oral Dis 2021 Apr;27 Suppl 3:655–664. doi: 10.1111/odi.13431. Epub 2020 Jun 3. 44. Bidra AS, Pelletier JS, Westover JB, Frank S, Brown SM, Tessema B. Comparison of in vitro inactivation of SARS CoV‐2 with hydrogen peroxide and povidone‐iodine oral antiseptic rinses. J Prosthodont 2020 Aug;29(7):599–603. doi:10.1111/jopr.13220. Epub 2020 Jul 24. 45. Meister TL, Brüggemann Y, Todt D, et al. Virucidal efficacy of different oral rinses against severe acute respiratory syndrome coronavirus 2. J Infect Dis 2020 Sep 14;222(8):1289–1292. doi:10.1093/infdis/jiaa471. 46. Herold T, Jurinovic V, Arnreich C, et al. Elevated 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. Epub 2020 May 18. 47. Matsushima K, Ohbayashi E, Takeuchi H, Hosoya S, Abiko Y, Yamazaki M. Stimulation of interleukin-6 production in human dental pulp cells by peptidoglycans from lactobacillus casei. J Endod 1998 Apr;24(4):252–255. doi:10.1016/ S0099-2399(98)80107-6. 48. De Sá AR, Garcia Santos Pimenta FJ, Dutra WO, Gomez RS. Immunolocalization of interleukin 4, interleukin 6, and lymphotoxin α in dental granulomas. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003 Sep;96(3):356–360. doi:10.1016/S1079-2104(03)00067-2. 49. Gomes MS, Blattner TC, Sant’Ana Filho M, et al. Can apical periodontitis modify systemic levels of inflammatory markers? A systematic review and meta-analysis. J Endod 2013 Oct;39(10):1205–1217. doi:10.1016/j.joen.2013.06.014. Epub 2013 Aug 16. 50. Nibali L, Fedele S, D’Aiuto F, Donos N. Interleukin-6 in oral diseases: A review. Oral Dis 2012 Apr;18(3):236–243. doi:10.1111/j.1601-0825.2011.01867.x. Epub 2011 Nov 4. 51. Azuma MM, Samuel RO, Gomes-Filho JE, Dezan-Junior E, Cintra LTA. The role of IL-6 on apical periodontitis: A systematic review. Int Endod J 2014 Jul;47(7):615–621. doi:10.1111/ iej.12196. 52. Mozaffari HR, Sharifi R, Sadeghi M. Interleukin-6 levels in the serum and saliva of patients with oral lichen planus compared with healthy controls: A meta-analysis study. Cent Eur J Immunol 2018;43(1):103–108. doi:10.5114/ ceji.2018.74880. Epub 2018 Mar 30. 53. Larsen KR, Johansen JD, Reibel J, Zachariae C, Pedersen AML. Serum cytokine profile and clinicopathological findings in oral lichen planus, oral lichenoid lesions and stomatitis. Clin Exp Dent Res 2017 Nov 7;3(6):220–226. doi:10.1002/ cre2.91. eCollection 2017 Dec. 54. Rhodus NL, Cheng B, Bowles W, Myers S, Miller L, Ondrey F. Proinflammatory cytokine levels in saliva before and after treatment of (erosive) oral lichen planus with dexamethasone. Oral Dis 2006 Mar;12(2):112–116. doi:10.1111/j.16010825.2005.01165.x. 55. Rezaei F, Mozaffari HR, Tavasoli J, Zavattaro E, Imani MM, Sadeghi M. Evaluation of serum and salivary interleukin-6 and interleukin-8 levels in oral squamous cell carcinoma patients: Systematic review and meta-analysis. J Interf Cytokine Res 2019 Dec;39(12):727–739. doi:10.1089/jir.2019.0070. Epub 2019 Jul 17. 56. Kheirandish-Gozal L, Gozal D. Obstructive sleep apnea and inflammation: Proof of concept based on two illustrative cytokines. Int J Mol Sci 2019 Jan 22;20(3):459. doi:10.3390/ijms20030459. 57. Vicente E, Marin JM, Carrizo SJ, et al. Upper airway and systemic inflammation in obstructive sleep apnoea. Eur Respir J 2016 Oct;48(4):1108–1117. doi:10.1183/13993003.00234-2016. Epub 2016 Sep 1. T HE CORRE S P ON DIN G AU T HOR , Shervin Molayem, DDS, can be reached at drmolayem@synergyspecialists.com.

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RM Matters

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Minimizing Risk While Giving Back to Your Community TDIC Risk Management Staff

s you embark on volunteer opportunities this spring, you are in good company. The month of April is designated by the United States as National Volunteer Month. The 2021 World Giving Index (WGI), the world’s largest survey of global charitable endeavors, highlights the ongoing spirit of volunteerism in this country. For the past 10 years, the U.S. has scored higher in volunteer and charity efforts than any other nation, with 58% of Americans reporting that they participate in volunteer activities and charitable donations. Dentists are leaders in choosing to share their time and talents to serve their communities and others in need. It’s essential that dentists be able to volunteer with confidence by understanding how their professional liability policies keep them covered. There can be several different scenarios in which you provide treatment at no charge — volunteering through a nonprofit organization or community health event, delivering emergency care unexpectedly or treating a friend or family member. A few insights may help you better identify and manage potential risks in each scenario.

Organized Events and Community Service Programs

While your existing professional liability policies may already cover you, it’s prudent to contact your insurance carrier prior to volunteering services. The insurer may require additional

information about the event, services offered and your clinical role as well as with whom the dentist will be working. The latter is to ensure that policyholders are not exposed to unnecessary risk, such as working with unlicensed dentists. ■ Professional liability policyholders with The Dentists Insurance Company are covered at volunteer

■

events within the state where they are licensed; no additional coverage is necessary. Dentists insured by other carriers should contact their carriers directly to confirm their current liability coverage details before volunteering. Dentists who do not have current professional liability insurance

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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and who do not practice for a fee (like retired dentists) can apply for affordable annual coverage designed for volunteers from TDIC. This coverage is intended for licensed dentists who wish to volunteer services without remuneration other than actual expenses. ■ If your volunteer services will be offered out of state or overseas, check with the charitable organization you are partnering with to determine if they offer liability coverage. If not, reach out to a TDIC representative to discuss available options. Even though treatment at an event doesn’t establish a continuing doctor-patient relationship, the individuals you volunteer to treat deserve the same standard of care as your patients of record. ■ Be sure to review each patient’s vitals and health history prior to treatment. ■ Take time to discuss treatment outcomes, along with potential risks associated with receiving and not receiving treatment and any alternatives. ■ Before initiating any care, make certain that the patient understands the parameters and extent of the treatment, particularly if further treatment is likely to be needed. ■ Keep in mind continuity of care. In the event a patient needs further treatment, explain it in detail to the patient and document why, when and what follow-up treatment is needed. TDIC’s Risk Management Advice Line frequently receives calls from insured dentists seeking guidance as to required coverage for organized events. For example, a dentist was invited to participate in a volunteer event hosted by a community church. The church required participating providers to have a specific amount of coverage per day. In this case, the caller 184

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was already insured by TDIC, and the Service Department helped him acquire a “special event” endorsement, which would satisfy the demands of the host location. Don’t let confusion about liability coverage stand in the way of your volunteer efforts. Speak to a trusted insurance advisor to ensure your coverage is adequate for your needs.

Emergency vs. Volunteer Care

Some health care providers mistakenly believe that Good Samaritan laws exempt them from all liability when

In California, liability remains when providing nonemergency treatment or assistance in the state.

volunteering. The federal government and 43 states have passed laws to protect medical volunteerism; however, California has not. In California, liability remains when providing nonemergency treatment or assistance in the state. For care rendered in a legitimate emergency that occurs outside of a health care facility, Good Samaritan laws usually lower the standard of care to encourage private citizens, including health care professionals, to assist others in emergency circumstances without fear of litigation. For more information, check the specific standards and limitations of your state’s Good Samaritan law.

Free Services for Family and Friends Outside of an organized event or program, the risks of donating services

can be more complex. Friends and family members who receive treatment at no charge must still be treated as patients of record. This means having an informed consent discussion, signed treatment plans, detailed chart entries and a thorough review of health histories prior to providing treatment — as well as discussing options for follow-up care. It’s also important to note your liability remains the same whether the dental treatment is performed during or outside of normal office hours. And it’s the same whether the patient incurs treatment costs or not. Understanding that the liability is unchanged, the question is if no-cost care should be provided in certain situations. TDIC’s Advice Line received a call from a practice owner that highlighted the problematic nature of offering free services. Her associate dentist had asked if he could offer discounted treatment to his nephew. The nephew was a pediatric patient with special needs whose family could not afford dental insurance. The associate dentist understandably wanted to help his brother’s family. However, the extent of treatment needed and the fact that their office was not equipped to treat pediatric patients raised some concerns for the practice owner. Along with her concerns for the young patient’s well-being, the dentist felt uncomfortable with her associate’s request and was unsure how to refuse it without compromising their relationship. The Risk Management analyst advised the dentist to prioritize what was in the best interest of the patient. The patient in question would be better served by an experienced, properly equipped pediatriccentric practice. Ideally, the level of care warranted might require dentistry in a hospital setting. Since the owner’s office wasn’t equipped to manage complex pediatric cases, it was not in the patient’s best interest for his uncle, the associate

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dentist, to offer care, despite the cost savings. The owner agreed with that approach to the situation and felt more comfortable communicating a denial to her associate’s request that was framed within what was best for the patient.

Risk Awareness and Rewards

Volunteering does not absolve you of risks, but simple awareness of those risks shouldn’t deter you from offering your skills for the benefit of others. Giving back by volunteering life-changing dental treatment can be one of the most rewarding aspects of your professional life, especially when your skills help individuals and families who are experiencing emergencies or barriers to access to care. Whole communities are changed by dental and health professionals who put their compassion into action. If you find yourself with questions about your liability that may arise while volunteering, please call TDIC’s Risk Management Advice Line at 800.733.0633. n The Dentists Insurance Company’s Risk Management Advice Line is a benefit available at no cost to CDA members, as well as to policyholders protected by TDIC. To schedule a consultation, visit tdicinsurance.com/RMconsult or call 800.733.0633.

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Making your transition a reality.

Dr. Thomas Wagner

Dr. Russell Okihara

LIC #01418359

LIC #01886221

Dr. Ben Sapir LIC #02126473

Jim Engel LIC #01898522

(916) 812-3255 (619) 694-7077 (925) 330-2207 (310) 596-0961 47 Years in Business 40 Years in Business 13 Years in Business 48 Years in Business

Jay Harter LIC #01008086

Kerri McCullough LIC #01382259

Gina Miller LIC #02015193

Steve Caudill LIC #00411157

Jaci Hardison LIC #01927713

Christy Conway LIC #: #02143744

Kim Ta LIC #02085576

Thinh Tran LIC #01863784

(916) 812-0500 (949) 300-0312 (707) 391-7048 (714) 318-4911 (951) 314-5542 (408) 687-5001 (619) 889-6492 (949) 675-5578 39 Years in Business 37 Years in Business 32 Years in Business 32 Years in Business 28 Years in Business 19 Years in Business 18 Years in Business 13 Years in Business

PRACTICE SALES • VALUATIONS/APPRAISALS • TRANSITION PLANNING • PARTNERSHIPS • MERGERS • ASSOCIATESHIPS NORTHERN CALIFORNIA ALAMO: New Listing! 3 Ops, Digital, 13 Yrs Goodwill, Desirable Area, Not in Delta Network. 2019 GR $642K. #CA2968 AUBURN: 4 Ops+RE, 60 Yrs. Goodwill, Dentrix, Digital, Laser, CEREC, Room to Grow w/ specialties. 2019 GR $632K. #CA2809 CONCORD/WALNUT CREEK: New Listing! 5 Ops in affluent/established area with RE available. Digital, CEREC, Digital Pano, Soft tissue Laser and so much more. 2021 GR projected to be $630K. #CA2808 FAIR OAKS/CITRUS HEIGHTS: Price Reduced! 4 Ops in desirable area, digital, strong hygiene program. Seller highly motivated to retire! 2019 GR $9790K on 4 days/wk with plenty of vacation. #CA656 EAST BAY AREA PEDO: Well-established with 8 Ops, Digital, plumbed for Nitrous, and high NP count. Associate-driven with Delta PPO. 2019 GR $832K on 3-4 days/wk., 2020 Production $560K. #CA2523 FAIRFIELD AREA: New Listing! 4 Ops w/1 add’l +RE, Digital, Paperless, Strong Hyg. Program, Not in Delta Network. 2019 GR $714K. #CA2955 FAIRFIELD AREA: High traffic area, 7 Ops Digital, Pano/CB, 23+ NP/mo. with 8+ Hyg. days/wk. Room to grow with specialties. 2019 GR $1.7M and 2021 on track to exceed 2019. #CA1824 FREMONT ORAL SURGERY: 34 yr history, diverse high-tech community. 4 Ops Digital, 7-10 y/o equipment, Pano. 2019 GR $548K on 3.5 days/wk. #CA2754 GREATER SONORA AREA: Rural lifestyle GP/Real Estate, 5 Ops, Dentrix, Strong hyg prog in stable community. 2019 GR $698K. #CA1713 LAKE TAHOE AREA: 4 Ops, 37+ yrs Goodwill. Rural lifestyle GP in growing resort community. 2019 GR $760K. #CA1715 MILLBRAE: Great practice in the heart of the peninsula with 60 yrs goodwill. 5 Ops. 2019 GR $1M+ on 4 days/wk. and 6 Hygiene days. Owner will work back for a short time for transition. Digital, Pano, Waterlase & Periolase. #CA1139 NAPA COUNTY: Price Reduced! Beautiful wine country location, 7 Ops, stand-alone building. GR $1M+ with 7 Days of Hygiene. Computerized and Digital. Established in the community for over 37 years. #CA2912 NORTHERN SACRAMENTO: Busy location, Paperless, 3 Ops+4th shared, CEREC, Digital Pano. 2019 GR $671K on 24-32 hrs/wk. #CA1745 OAKLAND: Pill Hill area, walk to BART, 2019 GR $473K. 3 Ops, Digital Xrays and Pano. #CA2839 PLEASANTON: New Listing! 7 Ops, 5 Equipped, Dentrix, Digital, Laser, Digital Pan, no need to add $, this practice has everything. GR $1.3M. Won’t last. #CA2891 REDDING: Modern office with 5 Ops, 4 Eq., Digital, Newer CEREC, 23 NP/mo with no marketing. Strong Hygiene, specialties referred. 2019 GR $558K. #CA1742

ROCKLIN/GRANITE BAY: High-end 4 Op GP/Cosmetic practice in affluent area. Paperless, digital, iTero scanner, 8+ hyg. Days/wk. 2019 GR $1.6M+, 2021 Prod projected at $2M+. RE for sale with practice. #CA2793 ROSEVILLE/CITRUS HTS: 4 Ops with 18 Yrs Goodwill, Digital, Laser, Strong Hyg., Specialties Referred, 2021 est GR $775K. #CA2897 ROSEVILLE/CITRUS HTS: 6 Ops, high traffic area, 13 yrs goodwill, Digital, lasers, 26 NP/mo, 5 days Hygiene, specialties referred. Seller will work back. #CA2749 ROSEVILLE/ROCKLIN: 7 Ops, hi-end practice in desirable area. Digital, CAD/CAM, lasers, Pano. 10+ hyg. days/wk, 2019 GR $2.3M, 2021 projected $2.5M. Lease with purchase option. #CA2770 SACRAMENTO METRO ORTHO: New Listing! Established practice in growing area with 5 chairs, digital Pan/Ceph and sensors, paperless. Seller will assist in transition. 2021 GR $451K. #CA2986 SAN FRANCISCO PEDO: New Listing! 7 Chairs, Digital, Nitrous, Digital Pan, Beautiful Office w/ <10 y/o equipment. 2019 GR $953K. #CA2953 SAN FRANCISCO: New Listing! 4 Ops, Financial District, SoftDent, Digital sensors and Pan. FFS/PPO, GR $1.6M+. Delta PPO Practice with over 70 NP/mo. #CA2934 SAN JOSE: Est for 35 yrs, 2019 GR of $1.3M with Adj. Net of 38%. 6 Ops, Digital X-rays and Pan, CAD/CAM, Laser. Upscale building near shopping. Seller can stay on P/T. #CA1140 SAN MATEO: Price Reduced! 5 Ops, Digital, iTero Scan, CEREC, Laser, Paperless, Microscope. Seller-owned stand-alone building to lease. $1.4M GR on 4 days/wk. #CA2596 SONOMA COUNTY: Price Adjustment! Large GP, 2019 GR $2.3M+. Stand-alone 3,000 sf prime Real Estate, 72 NP/mo. & 10 Hyg Days. 6 Ops, Pano, Dexis, Cameras, Laser, Dentrix. Both Business & RE for sale or Lease. Doctor Retiring. #CA544 SONOMA COUNTY: 4 Ops in spacious layout in heart of the area off main highway. Est 22 yrs with 5 star Google reviews, Paperless with CEREC, Scope, Laser, Strong Hyg. Retiring seller. 2019 GR $782K with good post-COVID recovery. #CA2594 SONOMA COUNTY: Price Reduced! 4 Ops with room to expand into suite next door. GR over $1M for last 3 yrs. Est. 30+ years. Strong hygiene, digital, space available to lease or buy. #CA2790 SONORA AREA: 5 Ops, Producing $825K in a renovated suite. RE for sale w/practice. Strong Hyg program. Digital, Laser, and Digital Pano. #CA2850 S. SACRAMENTO-GREENHAVEN: Associate in place. 4 Ops, Digital, Cone Beam, Digital Pano, Specialties referred. Not a Delta Premier Provider. 2021 projected $800K+. #CA2741 VACAVILLE AREA: 4 Ops, 3 equipped, 45 years goodwill, Digital, paperless, most specialties referred. 2019 GR $723K on 30 hour week. #CA2748

Northern California Office

800.519.3458

Henry Schein Corporate Broker #01230466

CENTRAL CALIFORNIA FRESNO AREA: 6 Op Valley gem, great staff in desirable area. Paperless, Trios Scanner, Digital Pan/Ceph, Lasers and 12 days of hyg/wk. 2019 GR $1.4M, 2021 projected at $1.4M again. Seller may consider option to purchase RE. #CA2004 GREATER MODESTO: 7 Ops, Desirable area, Dentrix, Digital, Laser, Digital Pano. RE for sale w/practice. Not a Delta Premier provider. 2020 GR $615K and 2021 should exceed it. #CA2795 MODESTO AREA: Est. area with 60+ yrs. goodwill. 5 Ops, 2019 GR $1.1M+ on 3 days/ wk. Dental Condo also available for purchase or lease, Seller may consider financing. #CA635 MONTEREY: 4 Ops, Paperless, Digital, Pano. 2019 GR $1.1M with Adj. Net over $450K. Post-COVID revenue has grown even more! RE for sale, non-Delta Premier office, FFS and some PPOs. #CA2614 SANTA CRUZ: New Listing! 4 Ops, Minutes to beach! Digital, CEREC, Pano, CBCT. Bread and butter practice-room to grow with specialties. FFS and Delta PPO only. #CA2938 SANTA CRUZ COUNTY: 4 Ops, near beach, in strip center. Digital Pano, X-rays, CEREC, 40 years goodwill. 2019 GR $392K on 3.5 days. #CA2822 SANTA CRUZ/APTOS PERIO: 4 Ops +RE, Paperless, Digital, CBCT, 27 years goodwill. Seller will help with smooth transition of strong referral base. #CA2725

SOUTHERN CALIFORNIA BAKERSFIELD: 7 modern Ops, FFS/PPO. Eaglesoft, Digital, M11 and Digital Pano. RE potentially for sale. Doctor selling due to emergency - highly motivated. #CA2945 BAKERSFIELD: 6 Ops, 40 yrs Goodwill, great reputation in the area. 6 hyg ds/wk and most specialty work referred. Digital pano, digital X-rays. 2019 GR $600K. RE also for sale. #CA1274 BAKERSFIELD: 6 Ops, 5 Equipped, Digital, 2020 Collections $1M+ with 6 days hygiene and 2 P/T associates. #CA2587 BURBANK: Big opportunity for large practice merger, 6 Ops, Digital, seller retiring. 6 days of hygiene, specialties referred. Seller will transition, open to financing options. 2019 GR $918K. #CA2632 HUNTINGTON BEACH: New Listing! 5 Ops, established 30 yrs. RE ownership available. PPO with specialties referred - room to grow. High net income in sought-after area. #CA2937 MONTEBELLO: 3 Ops in busy strip center location with 2 Associates, Digital X-rays, and all specialty work referred out. #CA2786 ORANGE COUNTY: New Listing! 8 Ops, 6 equipped, room to bring in specialists! Digital, BioLase, iTero, Digital Pan, beautiful office, modern and clean. Premium strip center location. GR $590K. #CA2926 ORANGE COUNTY: 4 Ops in sought-after area. 34 yrs Goodwill, many hi-end procedures done in-house but room to grow other specialties. Digital. FFS/Cash. #CA2704

www.HenryScheinDPT.com

PALM DESERT: 4 Ops 27 yrs Goodwill. Strong hyg prog w/ hi-end patient base of locals/snowbirds. 2019 GR $809K on only 16 days/mo. with low overhead. Call today! #CA691 PALMDALE/LANCASTER: 7 Op office in fast-growing community. Paperless with Dentrix, digital X-rays, 8 days of hyg./week and dedicated staff. Room to grow with specialties! #CA2612 SAN BERNARDINO: 6 Ops, established 33 years, cash, HMO, Denti-Cal in a busy area with parking. Estimated GR for 2021 at $960K+. Seller offering RE for sale with 2 lease tenants adjacent to practice. Room to expand with spec. #CA2843 SANTA CLARITA VALLEY: New Listing! 6 Ops, great cash flow, seller will work back. 3D CT, Itero, Digital with 8 hyg days/wk. PPO/FFS and 2021 GR over $2.3M. #CA2992 SOUTH ORANGE COUNTY: New Listing! Beautiful coastal location with 3 Ops and digital x-rays. Retiring seller has been in area for 32 years with most specialties referred. GR $500K. #CA2948 TORRANCE: 3 Ops, room for a 4th. Dentrix, digital, refers most specialties with low overhead and high net. GR $600K. #CA2815 TORRANCE:3 Ops, retiring seller with 34 yrs goodwill. Ready to take to the next level with technology of your choosing. Amazing location in desired area. 2019 GR of $300K with low expenses, a wonderful opportunity to grow. #CA2807

SAN DIEGO CARDIFF-BY-THE-SEA: New Listing! Amazing location, legacy practice open 60+ years, 4 Ops, add technology of your choosing and grow income stream by keeping specialties in-house. GR $686K. #CA2988 CARLSBAD: 5 Ops, modern design, suburban growing area. Digital Pan, Digital sensor, Laser, Paperless. 30 NP/mo. Room to grow with marketing and specialties. #CA2933 EL CAJON: New Listing! East County highly productive practice w/modern facility. Digital, seller refers specialties, primed for future growth. 2021 GR $1M+. #CA2975 ENCINITAS: 5 bright Ops, Strip mall loc. Digital Pan, Laser, Digital X-rays, Paperless. 25 NP/mo. Grow with specialties. #CA2935 ESCONDIDO: New Listing! 6 Ops, hi-prod, CBCT, Scanner, Scope, Laser. Off main road, refers out most specialties. #CA2946 N. SAN DIEGO COUNTY: New Listing! 6 Ops, Dentrix, Dexis, CBCT, laser, solid foundation. Main road location with free parking. #CA2932 N. SAN DIEGO COUNTY: New Listing! 4 Ops highly desirable location in busy strip mall. Digital, clean, and modern, with an excellent layout. Consistent year to year collections. #CA2961 SAN DIEGO: New Listing! 4 Ops, desirable/ affluent community. CEREC, CBCT, Digital, Dentrix, Paperless. Room to grow with specialties. #CA2896 SAN DIEGO: Rare opportunity, seller retiring, 4 Ops in desirable location with good cash flow. High quality work. Digital, Dentrix. #CA2851

Southern California Office

888.685.8100

Regulatory Compliance

C D A J O U R N A L , V O L 5 0 , Nº 3

The Importance of a HIPAA Associate Agreement CDA Practice Support

ental practices that are HIPAA-covered entities should understand what a business associate’s obligations are when the business associate experiences a breach of the dental practice’s protected health information (PHI). A business associate has specific obligations to protect PHI and to inform the affected covered entity when there is a breach. A dentist should look to the agreements with their respective business associates for specific information on how each business associate will protect PHI, manage a breach and inform the dentist when a breach occurs. A HIPAA business associate is a third party that uses, accesses or stores PHI to provide nonclinical services, typically, to a covered entity. Examples of business associates include practice management consultants, electronic health record companies, encrypted email services and online data backup and storage services. Although HIPAA places the obligation on the covered entity to have HIPAA-compliant agreements with their business associates, in reality, the third party provides the covered entity with its version of a HIPAA-compliant business associate agreement. When this occurs, a dentist should review the agreement to ensure it contains the minimum required provisions. A dentist can compare the agreement to the sample business associate agreement on cda.org/practicesupport. A compliant business associate agreement requires the business associate to report to the covered entity any use or disclosure of the information not provided for by its contract, including incidents that constitute breaches of

unsecured PHI. The dentist and business associate are responsible for adding to the agreement details, such as: ■ How soon after discovery of an impermissible use or disclosure of PHI should the business associate inform the dentist. HIPAA requires a business associate to notify a covered entity no later than 60 days from the discovery of a breach at or by the business associate. However, this provides little time for a dentist to

■

notify their patients since a covered entity is required to notify affected individuals no more than 60 days from the discovery of a breach. A dentist can consider requiring that a business associate notify them soon after the discovery of an impermissible use or disclosure of PHI. Whether the dentist wants details of the business associate’s investigation and assessment of an impermissible use or disclosure of PHI.

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Who will send notification to patients if the business associate determines the incident is a breach. The covered entity is required to notify affected individuals and, with incidents involving PHI of 500 or more individuals, the media and the Department of Health and Human Services. However, the dentist may delegate the tasks to the business associate or to another business associate. The agreement also must include a provision that any subcontractor that a business associate may engage on its behalf that will have access to PHI agree to the same restrictions and conditions that apply to the business associate with respect to the PHI. HIPAA business associates are directly liable for violations of the law. Some violations include: ■ Failure to provide breach notification to a covered entity or another business associate. ■

Failure to enter into business associate agreements with subcontractors that create or receive PHI on their behalf, and failure to comply with the implementation specifications for such agreements. ■ Failure to take reasonable steps to address a material breach or violation of the subcontractor’s business associate agreement. ■ Failure to comply with the requirements of the HIPAA Security Rule. ■ Impermissible uses and disclosures of PHI. In January 2021, the Department of Health and Human Services released a proposal to update HIPAA regulations. When finalized, the updated regulation will trigger a requirement for covered entities to revise business associate agreements in order to include new provisions. Covered entities should take this opportunity and the time to review and understand their business associate agreements. n ■

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.

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Tech Trends

C D A J O U R N A L , V O L 5 0 , Nº 3

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

Vivoo ($19.90 per month; additional pricing available)

Townsend Labs Sphere ($1,799, Sweetwater)

For many people, the pandemic has changed their perceptions of the importance of personal health and wellness. While much of the world continues to live through the aftermath of extended periods of lockdowns and isolation, the shift in focus to one’s own physical and mental health has become the priority in getting through the pandemic. Tracking wellness using meaningful metrics has become a popular tool for people to take control of their health. Vivoo is a personalized tracker that uses at-home urine test strips and a mobile app to provide real-time metrics and advice to optimize health and wellness.

Once in a great while, a product comes along where an entire industry agrees that it stands alone without peer. Like Apple’s iPhone or Google’s eponymous search engine, Townsend Labs’ Sphere L22 microphone has taken on such a reputation in the recording industry. Whether for voice or instruments, virtual meetings or filmmaking, this device has a fervent fan base who believes it can accomplish almost any recording task with excellent results. For a dentist looking to generate their own media, is the Townsend too much both in cost and capability?

Users need to create a free account on the Vivoo mobile app and purchase at-home urine test strips. The strips are only available online only and can be purchased on a monthly or subscription basis. The manufacturer recommends using the strips once a week. Each strip has colored boxes on one end where the user urinates on it. After approximately two minutes have elapsed, the individual uses the app on their mobile device and follows directions to properly orient and take a photo of the strip. Results are instantly displayed on the screen, providing scores on 11 wellness categories that include vitamin C, magnesium, salinity, free radicals, calcium, pH, hydration, ketones, urinary tract infections and kidney and liver functions. The scores do not correlate to specific values compared to medical lab tests, but can be used to generate overall awareness and trend insights when subsequent strips are used weekly. The app and test strips cannot be used to diagnose diseases or conditions and do not replace the advice or routine care from a licensed medical provider. From the wellness scores and trends, the app provides personalized nutrition and lifestyle advice prepared by professionals. Users can respond to the advice by indicating that they have completed the recommendations or are unable to do them. Recommendations also can be scheduled as event reminders directly on the mobile device. When used as a tool to gain an understanding of one’s health and track its progress over time, this product provides helpful information to supplement metrics that are recorded by smart wearable devices.

To begin with, the Townsend Labs Sphere L22 is a dual-capsule XLR condenser microphone, meaning that it is essentially two separate high-quality microphones in one device. Each capsule has its own channel and allows users granular controls to fit a multitude of recording needs, e.g., stereo, mono, pattern modeling, etc. What sets the L22 apart from every other microphone is the innovative post-recording modeling capabilities. With its proprietary software, users can make the microphone sound like 34 other vintage microphones AFTER audio has been recorded and adjust microphone placement to a small degree. This is game changing for people who do not own a microphone for every situation and want the flexibility to play with sound after it has been recorded. The L22 does require quite a bit to get it to work optimally — two XLR inputs, buying into the Universal Audio ecosystem, an understanding of digital audio workstations (DAWs) — but those who persevere are rewarded with one of the most versatile, well-constructed and innovative microphones on the market. Considering its cost, relatively steep learning curve and gear needed to use, the L22 will be appealing to only tech-savvy audiophiles, but would be too complex for anyone else. — Alexander Lee, DMD

Combined with regular visits to a primary care physician, wellness trackers such as Vivoo can be used at home to help improve overall health and optimize wellness. — Hubert Chan, DDS M ARC H 2 0 2 1

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CDA member benefit: Access to education anytime Online Learning is your destination for 24/7 education. Enjoy waived fees and big discounts on popular courses, including:

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IT’S EASY TO GET STARTED! Already a CDA member? Set up your Online Learning account with the same email you use to access your cda.org account to ensure access to the member-only catalog and special pricing. Then, sign in any time to explore all your course options and start learning! Not yet a member? Set up your account and sign in to access select courses, or join CDA to benefit from discounts and expanded learning options.

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CDA Journal - March 2022: A Dental Care Coordination System

Articles inside

The Mouth-COVID-19 Connection: Part II

Tech Trends: A look into the latest dental and general technology on the market

Regulatory Compliance: The Importance of a HIPAA Associate Agreement

RM Matters: Minimizing Risk While Giving Back to Your Community

The Mouth-COVID-19 Connection: Part I

C.E. Credit: A Mandibular Adenomatoid Odontongenic Tumor With a Novel Treatment Utilizing Platelet-Rich Fibrin

A Dental Care Coordination System: Experiences in Alameda County, California

Editorial: When Bad Things Bring Good Lessons