Speaker Articles & Recommended Reading by Seattle Study Club

2016 Seattle Study Club Symposium ®

S P EA KE R A RT I C L E S & REC O M M E N D E D R E A D I NG

PREVENTING HEART ATTACKS, STROKES AND DIABETES KNOWLEDGE IS POWER— WHAT WOMEN NEED TO KNOW ABOUT CARDIOVASCULAR HEALTH Dr. Amy L. Doneen

AN INCREDIBLE FIX FOR LOWER BACK PAIN Mr. Brian Bradley (Ergonomic Instruction)

A HOPELESS TOOTH IS NOT A USELESS TOOTH Dr. Marco A. Brindis

INFLAMMATORY PERI-IMPLANT DISEASE Dr. Paul Fletcher

SOFT TISSUE MANAGEMENT OF AESTHETIC FAILURE Prof. Giovanni Zucchelli 1

PREVENTING HEART ATTACKS, STROKES AND DIABETES KNOWLEDGE IS POWER— WHAT WOMEN NEED TO KNOW ABOUT CARDIOVASCULAR HEALTH Dr. Amy L. Doneen

Journal of Cardiovascular Nursing

Vol. 00, No. 0, pp 00Y00 x Copyright B 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins

8-Year Outcomes of a Program for Early Prevention of Cardiovascular Events A Growth-Curve Analysis Du Feng, PhD; M. Christina Esperat, PhD, RN, FAAN; Amy L. Doneen, RN, BSN, MSN, ARNP; Bradley Bale, MD; Huaxin Song, PhD; Alexia E. Green, PhD, RN, FAAN Background: Early identification of cardiovascular diseases allows us to prevent the progression of these diseases. The Bale/Doneen Method, a prevention and treatment program for heart attacks and ischemic strokes, has been adopted nationally in primary care and specialty clinics. Objectives: The main purpose of this study was to evaluate the effect of the Bale/Doneen Method on lipoproteins and carotid intima-media thickness (IMT) for cardiovascular disease prevention and reduction. A secondary purpose was to illustrate the use of latent growth-curve analysis in studying trajectories of clinical outcomes and biomarkers in individual patients over time. Method: This retrospective analysis is based on 576 patients at a nurse-managed ambulatory clinic who received the heart attack prevention and treatment program from 2000 to 2008. All patients were white; 61% were men; mean age was 55.5 years. Outcome measures include hemoglobin A1c, fasting blood sugar, plaque burden score (PBS), high-density lipoprotein, low-density lipoprotein (LDL), mean carotid artery IMT, and lipoprotein-associated phospholipase A2 test results. Latent growth-curve analysis was used in modeling changes in these outcome measures. Results: On average, mean IMT score decreased by 0.01 per year (P G .001), PBS decreased by 0.17 per year (P G .001), LDL decreased by 5.19 per year (P G .001), and lipoprotein-associated phospholipase A2 decreased by 3.6 per year (P G .05). Hemoglobin A1c increased by 0.04 per year (P G .001). Significant sex and age differences in the initial level and/or rate of change of mean IMT, PBS, fasting blood sugar, high-density lipoprotein, and LDL scores were found. Discussion: The current findings suggest that the Bale/Doneen Method is effective in generating a positive effect on the atherosclerotic disease process by achieving regression of disease in the carotid arteries. KEY WORDS:

cardiovascular disease, early prevention, treatment program

Du Feng, PhD Professor, School of Nursing, University of Nevada, Las Vegas.

M. Christina Esperat, PhD, RN, FAAN Professor,School of Nursing, Texas Tech University Health Science Center, Lubbock.

Amy L. Doneen, RN, BSN, MSN, ARNP Adjunct Professor, Texas Tech Health Science Center, School of Nursing, and Cofounder and Medical Director, the Heart Attack & Stroke Prevention Center, Spokane, Washington.

Bradley Bale, MD Adjunct Professor, Texas Tech Health Science Center, School of Nursing, and Medical Director, the Heart Health Program for Grace Clinic, Lubbock, Texas.

Huaxin Song, PhD Lead Analyst, School of Nursing, Texas Tech University Health Science Center, Lubbock.

Alexia E. Green, PhD, RN, FAAN Professor,School of Nursing, Texas Tech University Health Science Center, Lubbock. This work was supported by School of Nursing, Texas Tech University Health Science Center. The authors have no conflicts of interest to disclose.

Correspondence Du Feng, PhD, School of Nursing, University of Nevada, Las Vegas 4505 S Maryland Parkway, Box 453018 Las Vegas, NV 89154-3018 (du.feng@unlv.edu). DOI: 10.1097/JCN.0000000000000141

ardiovascular diseases (CVDs) are the leading cause of mortality in developed countries. Atherogenesis and, subsequently, atherosclerosis are cardiovascular (CV) processes that lead to most of these mortalities.1 Two leading factors that are thought to facilitate progression are oxidative stress and inflammation2; both are important in the pathogenesis of atherosclerotic changes.3Y5 Prevention of progression of these processes is at the center of the management of CVD. A hallmark in prevention is identification of biomarkers (eg, hemoglobin A1c [HgbA1C], low-density lipoprotein [LDL], plaque burden score [PBS], and intima-media thickness [IMT]) early in disease6 so that comprehensive and intensive management may be instituted to ameliorate the progression of the process. Metabolic syndrome is a prominent factor leading to the alarming increase in the incidence of chronic disease in the US population. This factor is among the most predominant precursors of the onset of CVD and therefore merits focus in the prevention efforts to control and prevent these chronic conditions. Another prominent factor, obesity, is thought to involve inflammatory 1

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2 Journal of Cardiovascular Nursing x Month 2014 processes and oxidative stress.7 In a study of the association between inflammatory markers and insulin resistance (IR) carried out in an elderly population, possible determinants of the homeostasis model assessment index, including four inflammatory markers (leukocyte count, erythrocyte sedimentation rate, high-sensitivity C-reactive protein, and C3 complement the 5 elements of the metabolic syndrome, total cholesterol, physical activity, as well as 4 indicators of adiposity (body mass index, waist circumference, percentage body fat, and hepatic steatosis) were studied.8 Of the 4 inflammatory markers simultaneously assessed in the subjects, only serum complement C3 was significantly associated with IR.8 It is imperative that more investigations be conducted to support the use of biomarkers of oxidative stress and inflammatory processes in the refinement of the classification of disease progress and to personalize the treatment approaches to the individual. Various definitions of metabolic syndrome exist in the literature. In the current study, we used the US National Cholesterol Education Program (NCEP) definition, which requires at least 3 of 5 of the following criteria: (1) central obesity, waist circumference equal to or greater than 102 cm or 40 in for men and equal to or greater than 88 cm or 35 in for women; (2) dyslipidemia, triglyceride (TG) level 1.7 mmol/L (150 mg/dL) or greater; (3) dyslipidemia, high-density lipoproteincholesterol (HDL-C) level less than 40 mg/dL for men and less than 50 mg/dL for women; (4) blood pressure (BP) 130/85 mm Hg or greater (or treated for hypertension); and (5) fasting plasma glucose level 6.1 mmol/L (110 mg/dL) or greater.9 Early Identification and Prevention of Cardiovascular Disease Another hallmark in the prevention of CVD is the early identification of the presence and progress of atherogenesis and arteriosclerosis among high-risk individuals. An important step in the diagnosis and management of individuals with risk factors for CVD is the classification of people into risk categories. Currently, in officebased practice, use of algorithms of conventional risk factors is standard practice. In the adult population within the United States, it is estimated that fully twothirds are classified as intermediate risk based on these algorithms.10 These individuals have to be managed aggressively to prevent the progression of the atherogenic process. The issue of adequately managing these individuals is fraught with challenges. Cardiovascular disease remains the number 1 cause of mortality in the United States. Cerebral vascular disease remains the number 1 cause of disability. Many individuals experience a CV event without any previous knowledge of being high risk. It is very important that early disease processes be identified if these challenges are to be over-

come and that the approach to prevention of progress of the disease be appropriately individualized. State of the science technology in the diagnosis of CVD has progressed to the point that test modalities for assessment of arterial function and structure in asymptomatic subjects are possible. Vascular ultrasonography and tonometry are some of the most promising among these modalities.6 Measurement of IMT with B-mode ultrasonography scans in the carotid arteries can now determine the presence of atherosclerotic process in the vascular structure.11,12 This diagnostic tool has the clear advantage of being a noninvasive procedure that could be conducted repeatedly or frequently. The establishment of quality control in the performance of the test and the standardization of the procedures for measurement may enable the integration of this diagnostic procedure into clinical practice, in addition to existing CV risk stratification algorithms.10 The Prevention Program: The Bale/Doneen Method The Bale/Doneen Method was developed by Dr Bradley Bale and Amy Doneen, ARNP, for the prevention and treatment of heart attacks and ischemic strokes in all primary and secondary prevention patients. This method is now being integrated nationally into primary care clinics and specialty clinics around the country. Components of this prevention/treatment program are grounded in a disease treatment paradigm and include aggressive management of CV risk factors and clinical outcomes (eg, heart attack, stroke, and diabetes mellitus) through evaluation, medication, and lifestyle management. All of the medications used are Food and Drug Administration approved. All of the lifestyle advice is guided by nutrigenomics, prescribed by the healthcare provider, which incorporates information on individual genetics and specific needs for certain nutrients.13,14 Lifestyle is emphasized as the number 1 way to reduce CV risk. Patients were educated on the importance of arterial inflammation as the reason arterial disease develops and as the trigger plaque for heart attacks and strokes. They were taught the numerous modifiable issues that can generate arterial disease and how to manage those issues to mitigate riskVnumerous lifestyle modifications that can have a positive influence on arterial inflammation. These included instructions on physical activity, proper diet, adequate sleep, anxiety management, weight control, nicotine cessation, and oral health. Thus, patients were coached about the importance of mitigating inflammation via proper lifestyle. The importance of exercise to enhance insulin sensitivity and avoid migrating on to type 2 diabetes was discussed with most of the patients. Daily exercise was encouraged with a mixture of aerobic and resistive training. Dietary advice was

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Program for Early Prevention of Cardiovascular Events 3

given with the guidance of the apolipoprotein E (apoE) genotype.15 In general, apoE 2’s were advised to limit carbohydrates and apoE 4’s were told to limit fat intake. All patients were educated about the benefit of diets rich in fruits, vegetables, nuts, seeds, and fish. Patients were advised to limit their intake of red meat. Alcohol guidance was very individualized. ApoE 4 individuals were told to avoid alcohol. Women who were apoE 2 or 3 were warned of the increased cancer risk of alcohol consumption. Alcohol was not presented as an essential element to reduce CV risk. Patients were instructed to take advantage of free phone consultation with Berkeley HeartLab dieticians. The Bale/Doneen Method is a method of delivering evidence- and outcome-based medical care using a system anchored in the disease of atherosclerosis rather than the standard practice of delivering preventative care based solely on risk factors. All decisions for assessment and treatment are based on the presence of atherosclerosis and the subsequent impact on the atherosclerotic process in this model of primary and secondary CVD prevention/treatment. Table 1 shows the 6 basic elements to the method, which hinge on patient education. It should be noted that the Bale/Doneen Method allows for a very personalized approach to maintain health and wellness. The healthcare providers are able to tailor their management for individual patients based on their most unique characteristics. Purpose of the Current Study The main purpose of current study was to evaluate the effect of a prevention/treatment program on lipoproteins, carotid IMT (cIMT), and lipoprotein-associated phospholipase A2 (Lp-PLA2) for CVD reduction in TABLE 1

Components of the Bale/Doneen Method

Components

Description

1. Education

Each patient is educated about the disease state of atherosclerosis and understands how myocardial infarctions and ischemic strokes occur. Each patient is evaluated for the presence of atherosclerosis, using noninvasive office-based techniques, to find asymptomatic vascular disease, and is monitored annually with an intima-media thickness (IMT) test to follow the individual trajectory of atherosclerotic disease. In addition, all patients are monitored annually with a carotid IMT test to follow the atherosclerotic disease over time in the individual patient. Biomarkers are used to routinely determine the inflammatory state of the vascular system. Endothelial markers include hs-C-reactive protein, microalbumen/creatinine urine ratio, and fibrinogen. Lipoprotein-associated phospholipase A2 is evaluated for intima activity. Patients were instructed to have these assessed at least biannually. The root cause or causes of the atherosclerotic process are determined and managed for each patient. Root causes of atherosclerosis can include insulin resistance, lipo(a), familial hyperlipidemia, potentially myeloperoxidase, and vitamin D deficiency.51 Appropriate follow-up testing for effective management of a root cause was done on average quarterly to semiannually. Goals of therapy are set based on peer-reviewed, reliable research and guidelines, with optimal targets in an attempt to minimize risk and often going beyond the values set for the standard of care. Attainment of goals was evaluated, on average, every 3Y6 months. Genetic information is obtained on patients to aid in the assessment of their cardiovascular risk and to help guide therapy. These tests were never repeated. Their clinical utility never expires, unlike other biomarkers. This makes them arguably the least expensive tests performed.

2. Disease

3. Inflammation

4. Root causes

5. Optimal goals

6. Genetics

patients recruited from a nurse-managed ambulatory clinic in Northwestern United States that specializes in heart attack prevention and intervention. Components of this early prevention program include aggressive management of CV risk factors and clinical outcomes (eg, heart attack, stroke, and diabetes mellitus) through evaluation, medication, and lifestyle management. All of the medications used are Food and Drug Administration approved. All of the lifestyle advice is common and could be prescribed by any healthcare provider. A secondary purpose was to illustrate the use of latent growth-curve analysis (GCA), as well as its advantages, in studying trajectories of clinical outcomes and biomarkers in individual patients over time. This multilevel statistical method can appropriately evaluate intraindividual change by modeling individual trajectories of outcomes, capture interindividual variability in change over time, and examine factors that explain the interindividual differences in growth trajectories. Although not used often in nursing research, multilevel growth-curve modeling techniques have become commonly used approaches to the study of change over time in epidemiology and social behavioral fields. The advantages of GCA over the traditional repeated-measures analysis of variance in analyzing longitudinal data have been well documented.16Y19 This article is, to the authors’ knowledge, 1 of the few to examine the use of GCA in studying changes in CV patients over a clinical trajectory. As more and more nursing researchers use longitudinal designs to study the clinical outcomes of CVD treatment and prevention, the availability of longitudinal data will create a shift toward the use of newer statistical models, such as the GCA, to the study of change over time. This statistical method can be of particular interest to nursing from a clinical point of view, as well as a way to test theoretical models.

4 Journal of Cardiovascular Nursing x Month 2014

Methods Study Design, Sample, and Setting This retrospective analysis is based on a deidentified data set containing medical, laboratory, and demographic information on 576 patients who were followed over 8 years in the Heart Attack Prevention Clinic in Northwestern United States, with at least 2 carotid imaging scans between January 2000 and June 2008. Clinic patients were referred to the clinic by their primary care physicians or self-referred because of CV risk factors such as hyperlipidemia, hypertension, diabetes, smoking, and family history or known CVD. The clinical setting for this study specializes in making a comprehensive assessment of patientsâ&#x20AC;&#x2122; CVD risk to determine their current arterial health status and, subsequently, to design a customized regimen of medication, diet, and exercise. The clinic protocols may include medications such as statins, angiotensin-converting enzyme inhibitors, niacin, fibrates, and "-blockers, all of which have been shown to slow the progression of IMT.20Y23 Procedure The institutional review board of the academic institution with which the authors are associated approved the study, and all patients provided written informed consent before their medical records were entered into an electronic registry. Participation in this registry was completely voluntary, and only arbitrary numbers were used to identify participants to ensure confidentiality. No monetary incentive was given for taking part in the registry. Data entered into the deidentified data set included a detailed medical history questionnaire filled out by participants with a focus on coronary artery disease (CAD); IMT scan results such as mean IMT and PBS; other laboratory test results such as HgbA1C, fasting blood sugar (FBS), HDL, LDL, and Lp-PLA2; as well as medication history. In most cases, participants underwent ultrasound examinations of the carotid artery at 1-year intervals and took other laboratory tests on regular schedules. All patients received the same individualized Bale/Doneen Method protocol. Measurement At enrollment, each patient completed a medical history, medication history, physical examination, a panel of blood tests, and anthropometric measurements. Current or past smokers were defined as those patients who were using cigarette, pipe, cigar, or chew tobacco or had been these in the past. The blood tests consisted standard laboratory results, including HgbA1C, FBS, HDL, and LDL. In addition, carotid artery IMT scans and Lp-PLA2 tests were performed among our study participants.

Carotid Intima-Media Thickness Assessment Carotid artery IMT is assessed by B-mode ultrasound. Mean common IMT was defined as the mean of six 10-mm measurements taken from the left and right anterior, posterior, and lateral common carotid views. One of the primary outcome measures was the presence or absence of carotid artery plaque as demonstrated by IMT. Plaque was defined as an IMT of greater than 1.2 mm in the common, bifurcation, and internal carotid artery. A PBS was defined as the sum of all plaques identified in a single patient. Research has validated the use of IMT as a reliable and noninvasive measure of disease-related arterial wall changes.24,25 Intima-media thickness has been used as a surrogate marker of CVD and risk of a CV event, as well as means of identifying atherosclerosis and following its progress.26,27 Although a small increase in IMT may be an adaptive response to changes in BP and blood flow, there is consensus that IMT levels greater than 0.9 mm are indicative of atherosclerotic vascular disease and end-organ damage.28 Atherosclerosis of the large- and medium-sized arteries is associated with plaque formation, inflammation, endothelial dysfunction, thrombosis, and acute or chronic luminal obstruction resulting in abnormal blood flow to target organs.29 Lipoprotein-Associated Phospholipase A2 Lipoprotein-associated phospholipase A2 is a fatty enzyme that is produced by inflammatory cells (macrophages, T-lymphocytes, and mast cells) and hydrolyzes oxidized phospholipids in LDL. This rupture-prone substance builds up in the artery wall from various risk factors including elevated LDL cholesterol and can be used to determine risk levels for both heart events and stroke. The Lp-PLA2 test detects the presence of the more dangerous soft, rupture-prone plaque hiding in the lining of arteries. Existing studies have indicated that Lp-PLA2 appears to be an independent marker of CV risk30Y32 and that Lp-PLA2 is strongly correlated with several CV risk factors, especially lipid fractions, and with the degree of carotid artery atherosclerosis.33 Our previous studies also suggested use of Lp-PLA2 results for finding individuals whose outcome by standard cardiac screening may be low risk but may actually be at a higher risk after evaluation of the Lp-PLA2 result. Thus, the Lp-PLA2 was monitored over the study period as a genotypic marker for CV risk. Insulin Resistance Evidence is accumulating that there is an insulinrelated CAD risk. For example, research has shown that IR is responsible for most of CVDs34Y37 and that IR is positively correlated with elevated TG, low HDL, BP, plasminogen activator inhibitor 1, and brachialankle pulse wave velocity in a clinical sample.38 This condition can be identified before a patient experiencing

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Program for Early Prevention of Cardiovascular Events 5

an heart attack or stroke or becoming diabetic. In the current study, IR risk was defined as TG/HDL-C ratio of 3.5 or greater, fasting glucose level of 100 mg/dL or greater, 2-hour glucose tolerance of 140 mg/dL or greater, or metabolic syndrome, whereas metabolic syndrome was defined by NCEP criteria.34 Framingham Risk Score The 10-year CVD risk was determined using the Framingham Risk Score (FRS) as calculated in National Cholesterol Education Program Adult Treatment Panel III (NCEP-ATP III). Risk factors included in determining FRS were age, gender, total cholesterol, HDL-C, smoking, systolic BP, and the use of antihypertensive agents. All participants were categorized, based on NCEP-ATP III, into 3 groups: FRS less than 10%, FRS 10% to 20%, and FRS greater than 20% (ie, CAD or CAD-risk equivalent). Coronary Artery Disease Patients also reported their diagnosis of CAD, angina pectoris, previous MI, heart failure, cardiac surgery, arrhythmia, or hypertension. Coronary artery disease was defined as any history of acute coronary syndrome, percutaneous coronary intervention, coronary bypass grafting, or presence of coronary artery calcification. Coronary artery disease equivalence was defined as history of cerebral vascular accident, presence of peripheral arterial disease, diabetes, or FRS of 20% or higher. Data Analysis Strategy Descriptive statistics were obtained for all background variables using SPSS 20.0.39 Bivariate correlations (Pearson r) between continuous measures at baseline (eg, mean IMTand Lp-PLA2) were calculated. Chi-square tests were performed to evaluate the association between key categorical variables (eg, presence/absence of IR risk and atherosclerosis). Furthermore, because observations (clinical outcomes or tests) over time are ‘‘nested’’ within a patient in the current study, a statistical technique known as GCA was used in modeling changes in the outcome measures among patients at the nurse-managed ambulatory clinic who received the heart attack prevention program. Specifically, the method used in the current study, the latent curve GCA, was conducted through hierarchical linear modeling.17,19,40,37 The modeling of change was accomplished by a series of 2-level analyses using linear functions. The level 1 analysis captures within-subject variability (ie, individual change over time), whereas level 2 analyses capture between-subject variability. At level 1, each subject’s measure on the outcome variable is regressed onto the time variable (in this case, years since baseline),

resulting in a regression equation (in this case, a linear equation) that represents each individual patient’s growth curve. The coefficients that make up the regression equation are the individual growth parameters: the intercept, which indicates the patient’s initial level of the outcome measure, and the linear slope, which indicates the patient’s rate of change of the outcome measure. At level 2, each growth parameter obtained from level 1 is modeled by a regression equation that captures the population main effect plus the variability resulting from each individual. The level 2 equations for the current study consist of 2 linear regression equations, linking the patient’s trajectories of change to patient-related characteristics (eg, age at enrollment, gender), which are considered as correlates of change. Similarly, level 1 and level 2 equations were used for all clinical outcome variables, to test whether male and female and older versus younger patients responded differently to the intervention. Missing data were handled using the full information maximum likelihood estimation method, based on its advantages over the traditional missing data techniques.41,42

Results Sample Descriptive Statistics All patients in this sample were white, and 61% (n = 344) were men. Mean (SD) age at the time of enrollment was 55.5 (10.2) years. Most (89%) had hyperlipidemia, 58% had hypertension, 56% had metabolic syndromes (ie, those who had at least 3 of the following risk factors: TG 9150 mg/dL; FBS 9100 mg/dL; BP 9130/85 mm Hg; waist circumference 935 or 940 in for women or men, respectively; and HDL G50 or G40 mg/dL for women or men, respectively), 5% were diabetic, and 37% were past or present smokers. Regarding adjusted FRS at baseline, 66% were at moderate risk (ie, 10% 9 FRS), 24% were at moderately high risk (ie, 20% 9 FRS 9 10%), and 10% were at high risk (ie, FRS 9 20%). Twenty-five percent of study participants showed indications of CAD or CAD equivalent. Although an initial IMT value at or above 0.9 mm is indicative of atherosclerotic vascular disease according to European Society of Hypertension-European Society of Cardiology guidelines,43 we used a more conservative cutoff point of 1.2 mm as indication of the presence of carotid plaque (ie, carotid atherosclerosis was defined as an isolated intimal thickening of Q1.2 mm). Carotid plaque was identified in 64% of patients with moderate FRS risk, 87% of patients at moderately high FRS risk, and 89% of patients at high FRS risk. It should be noted that 18% of our study population were asymptomatic primary prevention patients. Further details about the demographic and medical characteristics of the sample can be found in Table 2.

6 Journal of Cardiovascular Nursing x Month 2014 TABLE 2

Baseline Patient Demographic Characteristics (N = 576)

Characteristic

n (%) or Mean T SD

Age, y BMI, kg/m2 Male White Current or past smoker Diabetes Hyperlipidemia Hypertension CAD/CAD equivalent Metabolic syndrome Insulin resistant Adjusted Framingham Risk Score G10% 10%Y20% 920% Carotid plaqueVPBS score Q1.2 mm

55.5 27.5 344 576 209 25 512 325 143 321 417

T 10.2 T 5.0 (61) (100) (36) (5) (89) (58) (25) (56) (73)

370 (66) 141 (24) 58 (10) (85)

Abbreviations: BMI, body mass index; CAD, coronary artery disease; PBS, plaque burden score.

Effectiveness of the Prevention Fixed estimates predicting the 2 random effects, intercept (:0i) and linear slope (:1i), for each of the outcome measures are presented in Table 3. The intercepts show the initial status of each measure at baseline, and the slopes indicate the rate of change. Overall, combining male and female patients of all ages, mean IMT score decreased by 0.01 per year (P G .001) on average, PBS decreased by 0.17 per year (P G .001), LDL decreased by 5.19 per year (P G .001), and Lp-PLA2 decreased

by 3.6 per year (P G .05). The linear slope of FBS was not statistically significant, indicating that the FBS level was stable over time. On the other hand, HgbA1C increased by 0.04 per year (P G .001) on average. Variances of both the intercept and the linear slope of all the study variables are significant, indicating heterogeneity (ie, interindividual differences) in the initial level and change rate of these clinical outcomes (see Table 3). Figures 1A through H show the group growth curve of the clinical outcomes of interest. Based on the interindividual differences found at level 2 analysis, a conditional linear model was used to test sex and age at baseline as level 2 covariates. Table 4 presents the unstandardized coefficients, showing the effects of sex and age at baseline on the initial levels ("01 and C01, respectively) as well as on the rate of change ("02 and C02, respectively). For mean IMT, the coefficients revealed that men had significantly higher mean IMT scores at baseline compared with women (B = 0.04, P G .001) and older patients had significantly higher mean IMT scores at baseline compared with younger patients (B = 0.01, P G .001). However, older patients showed a faster decrease in mean IMT scores, as evidenced by the negative effect of age on linear slope (B = j0.0004, P G .01). Similarly, the second column of Table 4 shows that men had significantly higher PBS scores at baseline compared with women (B = 0.80, P G .05) and that older patients had significantly higher PBS scores at baseline compared with younger patients (B = 0.18, P G .001). However, there are no significant sex or age effects on

TABLE 3

Unstandardized Coefficients of the Unconditional Linear Growth-Curve Models of Mean Intima-Media Thickness, Plaque Burden Score, Hemoglobin A1c, Fasting Blood Sugar, Fasting Insulin Level (Insulin), High-Density Lipoprotein, Low-Density Lipoprotein, and Lipoprotein-Associated Phospholipase A2

Outcomes

IMT

PBS score

Fixed effects Intercepta, :0i 0.79b 5.30b Linear slopea, :1i j0.01b j0.17b Random effects Intercept variance 0.03 21.65 1362.48b 922.77b 22 df 438 338 Linear slope variance 0.0004 0.29 1008.97b 666.003b 22 df 438 338 Level 1 error variancea 0.002 1.42 Reliability of OLS regression coefficient estimate Initial status 0.59 0.53 Linear change rate 0.48 0.40

HgbA1C

FBS

Insulin

HDL

LDL

Lp-PLA2

5.37b 0.04b

96.61b 0.26

8.84b 0.06

46.48b 1.40b

131.14b j5.19b

189.73b j3.60c

1.85 969.60b 417 0.01 658.91b 417 0.08

638.70 682.36b 392 15.87 599.43b 392 96.61

10.95 313.43c 273 0.58 372.02b 273 24.77

303.27 1238.21b 457 3.73 807.56b 457 69.48

1280.69 1009.07b 457 15.62 762.34b 457 522.73

11605.78 360.24d 295 219.25 359.12d 295 1116.74

0.61 0.41

0.30 0.32

0.06 0.11

0.43 0.31

0.34 0.22

0.25 0.25

Abbreviations: FBS, fasting blood sugar; HDL, high-density lipoprotein; HgbA1C, hemoglobin A1c; IMT, intima-media thickness; LDL, low-density lipoprotein; OLS, ordinary least-squares; Lp-PLA2, lipoprotein-associated phospholipase A2; PBS, plaque burden score. a The level 1 equation is Yit = :0i + :1i Timeit + eit, where Yit represents the repeatedly measured outcome variable for individual i at time t; time is measured in weeks. b P G .001. c P G .05. d P G .01.

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Program for Early Prevention of Cardiovascular Events 7

FIGURE 1. A, Group growth curve of IMT mean. B, Group growth curve of the PBS score. C, Group growth curve of HgbA1C.

D, Group growth curve of fasting blood sugar. E, Group growth curve of fasting insulin level. F, Group growth curve of HDL. G, Group growth curve of LDL. H, Group growth curve of Lp-PLA2. IMT, indicates intima-media thickness; PBS, plaque burden score; HgbA1C, hemoglobin A1c; HDL, high-density lipoprotein; LDL, low-density lipoprotein; Lp-PLA2, lipoprotein-associated phospholipase A2.

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8 Journal of Cardiovascular Nursing x Month 2014 Fixed Effects (Unstandardized Coefficients) of Level 2a Covariates, Sex and Age at Baseline, in Predicting Differences in the Initial Level and Change Rate in Mean Intima-Media Thickness, Plaque Burden Score, Hemoglobin A1c, Fasting Blood Sugar, Fasting Insulin Level (Insulin), High-Density Lipoprotein, Low-Density Lipoprotein, and Lipoprotein-Associated Phospholipase A2 TABLE 4

Source Intercepta Sex, "01 Baseline age, C01 Linear slopea Sex, "02 Baseline age, C02

Mean IMT

PBS

HgbA1C

0.04b 0.01b

0.80c 0.18b

0.05 0.01

5.47c j0.01

j0.004 0.001

j0.47 0.02

j0.002 j0.0004d

0.02 j0.003

FBS

Insulin 0.89 0.03 j0.07 j0.01

HDL

LDL

Lp-PLA2

j5.68b 0.29c

j5.87c j0.28

9.30 j0.36

j0.16 j0.01

0.43 j0.01

j1.38 0.10

Abbreviations: FBS, fasting blood sugar; HDL, high-density lipoprotein; HgbA1C, hemoglobin A1c; IMT, intima-media thickness; LDL, low-density lipoprotein; Lp-PLA2, lipoprotein-associated phospholipase A2; PBS, plaque burden score. a Level 2 equations are as follows: :0i = "00 + "01(sex)it + "02(age at baseline)it + ei and :1i = C00 + C01(sex)it + C02(age at baseline)it + ei. Sex is dummy coded (male = 1 and female = j1); age at baseline is not centered. b P G .001. c P G .05. d P G .01.

the rate of change in PBS. Other significant effects found at level 2 are as follows: Men had significantly higher FBS scores, higher HDL scores, and lower LDL scores at baseline compared with women (B = 5.47, P G .05) and older patients had significantly higher HDL scores at baseline compared with younger patients (B = 0.29, P G .05).

Discussion The current findings seem to suggest that the Bale/ Doneen Method is effective in generating a positive effect on the atherosclerotic disease process, namely, achieving regression of disease in the carotid arteries. This was demonstrated by a significant decrease in mean common carotid artery IMT (CCA-IMT) and PBS. It seems logical to speculate that this may result in a decrease in CV events. The medical management resulted in a positive effect on at least 3 important CV risk factors: LDL, HDL, and Lp-PLA2. Several previous studies also demonstrated regression along with a positive effect on both LDL and HDL.44Y46 Extendedrelease niacin was used in a large percentage of the patients treated with the Bale/Doneen Method, which probably accounts for the positive effect on both LDL and HDL. The slight increase in HgbA1c may be explained by the use of niacin and statins. Despite this increase, there was a positive effect on atherosclerosis. This fits some of the recently published data that question the benefit of aggressive HgbA1C targets to reduce CV events.47,48 It is interesting that the FBS did not increase significantly. Niacin is known to have a synergistic effect with statins on reducing the levels of Lp-PLA2.49 A recent study generated a strong signal that Lp-PLA2 may be causal of atherosclerosis. If that is the case, it seems logical to speculate that the positive therapeutic effect on Lp-PLA2 may have also contributed to regression of disease. There were numerous other variables measured, but not analyzed, in these data that

may have also contributed to the regression results, such as BP. Perhaps, 1 of the most salient issues regardless of knowing for sure all of the reasons for the results is that these data indicate that there is a method available to manage CV risk that is clinically applicable and that can generate regression of atherosclerosis. This data set should be analyzed further in an attempt to ferret out all significant variables that may be associated with the positive results. It seems that the GCA is a valuable technique to accomplish this. These results should generate hypotheses for future randomized placebo controlled trials. There are numerous weaknesses with the data. There was no placebo group. The patients were all white and motivated to enter a prevention clinic. Most of the patients were men. Perhaps, 1 of the greatest strengths is the fact that these data were generated in an ambulatory clinical setting and represent the first data published using long-term serial cIMT to monitor atherosclerosis in a nonacademic setting. This article, to the authorsâ&#x20AC;&#x2122; knowledge, is the first report to examine the utility of multilevel GCA in studying trajectories of clinical outcomes related to CVD. Limitations and Suggestions for Future Research The current study is based on a single group of patients who were enrolled at 1 clinic in Northwestern United States. Future studies should include a comparison group and use the randomized control treatment design to evaluate the effectiveness of the prevention method. In fact, large, prospective, randomized controlled studies are needed to evaluate the impact of novel approaches to preventing and averting CVD. The significance of specific risk factors, including those not amenable to pharmacological treatmentVdiet, exercise, many sleep, and psychological issuesVshould be sorted out in larger studies. Another limitation lies in the lack of diversity of

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Program for Early Prevention of Cardiovascular Events 9

What’s New and Important h The Bale/Doneen Method rests on a platform of assessing and monitoring arterial disease. It is anchored in inflammation being causal of atherosclerosis. The method comprehensively evaluates known sources for arterial inflammation and promotes optimal management of all identified contributors to the arterial ‘‘fire.’’ The methods of assessing and treating patients used by the Bale/Doneen Methods are available to any practitioner. h Previous studies have indicated that patients who receive prevention and treatment of CVD through the Bale/Doneen Method show stabilization of the atherosclerotic disease process, a significant conversion of plaque morphology to 100% echogenic lesions by the fifth year of follow-up, and that echogenic carotid plaque is significantly less inflamed than nonecogenic plaque. Consistent with past studies, this article shows that the Bale/Doneen Method is effective in generating a positive effect on the atherosclerotic disease process by achieving regression of disease in the carotid arteries. h The use of growth-curve modeling in examining changes in markers such as IMT and other biomarkers associated with CVD can improve the accuracy of CVD risk prediction and help identify effective treatments.

the current study sample. Nearly 100% of the samples are white. Data collection across more diverse patient populations is needed. Although cIMT testing in the clinical setting is not commonly performed, the availability of cIMT testing is increasing. Criteria for appropriate use of CIMT were published in the journal Atherosclerosis in October 2010.50 Cardiovascular and arteriosclerotic vascular diseases are multifactorial. The effective prevention methods should attempt to gain optimal control of and influence as many of those factors as possible. Future evaluation studies should also take into account patient motivation and adherence. Indeed, if the goal is to focus only on those risk factors, the patient will generally be faced with ever higher doses of statins and other pharmacotherapy, which may have lower up-front costs but higher risk of adverse reactions from such agents. In addition, if that agent needs to be withdrawn, the patient may quickly become uncontrolled and face added risk of CV events. A multifactorial disease treatment paradigm such as the Bale/Doneen Method may prove to be safer and more economical in the long run. Summary The Bale/Doneen Method for the prevention of heart attacks and strokes is a clinically based approach focused on the actual disease of atherosclerosis. The current standard of care supports managing the disease from a risk factor approach, which has proven to support recidivistic events and a lack of ability to determine asymptomatic vascular disease before the patient experiencing a clinically significant ischemic event. We have proven

that our global disease treatment paradigm can be accomplished in the ambulatory setting and can demonstrate a direct impact on the atherosclerotic process. This GCA of cIMT test results demonstrates the effectiveness of a model focused on patient education, disease identification and monitoring, routine assessment of vascular inflammation, identifying and treating the root causes of atherosclerosis, setting optimal goals for management of risk factors, and using genetics to individualize care to the unique individual needs of the patient. These data support that a disease treatment paradigm, when applied in an ambulatory setting, causes a direct impact on the disease of atherosclerosis. None of the patients in this study had a CV event during the 8 years of follow-up despite the fact that many had atherosclerotic lesions and many were secondary prevention patients. The purpose of this study was to evaluate CVD prevention/treatment methods based on data collected from a real clinical practice, a nurse-managed clinic, by examining changes in IMT and phenotypic and genotypic markers associated with CVD. Using these markers can improve the accuracy of CVD risk prediction and also help in selecting potentially effective treatment. Because the methods of assessing and treating patients used by the Bale/Doneen Methods are available to any practitioner, it is believed that analysis of this data will be beneficial in the understanding of better CV prevention programs. The multilevel growth-curve modeling technique appears to be well suited to complex modeling of multiple signs or symptoms and related outcomes. The method may enhance the ability of researchers to analyze results of the complex data that emerge when symptom clusters are being studied. The data include the process of change in clinical signs and symptoms and the relationship of such processes to other individual and clinical characteristics of patients, as well as to underlying mechanistic models. REFERENCES 1. Arbab-Zadeh A, Nakano M, Virmani R, Fuster V. Acute coronary events. Circulation. 2012;125(9):1147Y1156. 2. Collaboration IRGCERF, Sarwar N, Butterworth AS, et al. Interleukin-6 receptor pathways in coronary heart disease: a collaborative meta-analysis of 82 studies. Lancet. 2012; 379(9822):1205Y1213. 3. Devaraj S, Tang R, Adams-Huet B, et al. Effect of highdose alpha-tocopherol supplementation on biomarkers of oxidative stress and inflammation and carotid atherosclerosis in patients with coronary artery disease. Am J Clin Nutr. 2007;86(5):1392Y1398. 4. Blin J, Ahmad Z, Rampal LR, Mohtarrudin N, Tajudin AK, Adnan RS. Preliminary assessment of differential expression of candidate genes associated with atherosclerosis. Genes Genet Syst. 2013;88(3):199Y209. 5. Krychtiuk KA, Kastl SP, Speidl WS, Wojta J. Inflammation and coagulation in atherosclerosis. Hamostaseologie. 2013; 33(4):269Y282.

10 Journal of Cardiovascular Nursing x Month 2014 6. Belcaro G, Nicolaides AN, Ramaswami G, et al. Carotid and femoral ultrasound morphology screening and cardiovascular events in low risk subjects: a 10-year follow-up study (the CAFES-CAVE study(1)). Atherosclerosis. 2001; 156(2):379Y387. 7. Musa S, Haynes E. Biomarkers of obesity and subsequent cardiovascular events. Epidemiol Rev. 2007;29:1093. 8. Muscari A, Antonelli S, Bianchi G, et al. Serum C3 is a stronger inflammatory marker of insulin resistance than C-reactive protein, leukocyte count, and erythrocyte sedimentation rate: comparison study in an elderly population. Diabetes Care. 2007;30(9):2362Y2368. 9. Grundy SM, Cleeman JI, Merz CN, et al. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. J Am Coll Cardiol. 2004;44(3):720Y732. 10. Kullo IJ, Malik AR. Arterial ultrasonography and tonometry as adjuncts to cardiovascular risk stratification. J Am Coll Cardiol. 2007;49(13):1413Y1426. 11. Balestrini S, Lupidi F, Balucani C, et al. One-year progression of moderate asymptomatic carotid stenosis predicts the risk of vascular events. Stroke. 2013;44(3):792Y794. 12. Figueroa AL, Subramanian SS, Cury RC, et al. Distribution of inflammation within carotid atherosclerotic plaques with high-risk morphological features: a comparison between positron emission tomography activity, plaque morphology, and histopathology. Circulation. 2012;5(1):69Y77. 13. Superko HR, Roberts R, Agatston A, et al. Genetic testing for early detection of individuals at risk of coronary heart disease and monitoring response to therapy: challenges and promises. Curr Atheroscler Reports. 2011;13(5):396Y404. 14. Komduur R, Te Molder H. The role of genes in talking about overweight: an analysis of discourse on genetics, overweight and health risks in relation to nutrigenomics. Public Understand Sci. 2013. DOI: 10.1177/0963662512472159. 15. Eichner JE, Dunn ST, Perveen G, Thompson DM, Stewart KE, Stroehla BC. Apolipoprotein E polymorphism and cardiovascular disease: a HuGE review. Am J Epidemiol. 2002; 155(6):487Y495. 16. Dudley WN, McGuire DB, Peterson DE, Wong B. Application of multilevel growth-curve analysis in cancer treatment toxicities: the exemplar of oral mucositis and pain. Oncol Nurs Forum. 2009;36(1):E11YE19. 17. Raudenbush SW, Bryk AS. Hierarchical Linear Models: Applications and Data Analysis Methods. Thousand Oaks, CA: Sage Publications; 2002. 18. Rogosa DR. Myth and methods: ‘‘myths about longitudinal research,’’ plus supplemental questions. In: Gottman JM, ed. The Analysis of Change. Hillsdale, NJ: Erlbaum; 1995:3Y65. 19. Singer JD, Willet JB. Applied Longitudinal Data Analysis: Modeling Change and Event Occurrence. Oxford: University Press; 2003. 20. Crouse JR 3rd, Raichlen JS, Riley WA, et al. Effect of rosuvastatin on progression of carotid intima-media thickness in low-risk individuals with subclinical atherosclerosis: the METEOR Trial. JAMA. 2007;297(12):1344Y1353. 21. Salonen R, Nyyssonen K, Porkkala E, et al. Kuopio Atherosclerosis Prevention Study (KAPS): a populationbased primary preventive trial of the effect of LDL lowering on atherosclerotic progression in carotid and femoral arteries. Circulation. 1995;92(7):1758Y1764. 22. Taylor AJ, Sullenberger LE, Lee HJ, Lee JK, Grace KA. Arterial Biology for the Investigation of the Treatment Effects of Reducing Cholesterol (ARBITER) 2: a doubleblind, placebo-controlled study of extended-release niacin on atherosclerosis progression in secondary prevention

23.

24.

25.

26.

27.

28. 29.

30.

31.

32.

33.

34.

35.

36.

37.

38.

39.

patients treated with statins. Circulation. 2004;110(23): 3512Y3517. Wiklund O, Hulthe J, Wikstrand J, Schmidt C, Olofsson SO, Bondjers G. Effect of controlled release/extended release metoprolol on carotid intima-media thickness in patients with hypercholesterolemia: a 3-year randomized study. Stroke. 2002;33(2):572Y577. Bots ML, Dijk JM, Oren A, Grobbee DE. Carotid intimamedia thickness, arterial stiffness and risk of cardiovascular disease: current evidence. Journal of Hypertension. 2002; 20(23):17Y25. Lucas FL, DeLorenzo MA, Siewers AE, Wennberg DE. Temporal trends in the utilization of diagnostic testing and treatments for cardiovascular disease in the United States, 1993Y2001. Circulation. 2006;113:374Y379. Minino AM, Heron MP, Murphy SL, Kochanek KD. Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics Reports. Deaths: final data for 2004. Natl Vital Stat Rep. 2007; 55(19):1Y119. Rosamond W, Flegal K, Friday G, et al. Heart disease and stroke statisticsY2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2007;115(5):e69Ye171. Van Bortel LM. What does intima-media thickness tell us? J Hypertens. 2005;23:37Y39. Orford JL, Selwyn AP, Ganz P, Popma JJ, Rogers C. The comparative pathobiology of atherosclerosis and restenosis. Am J Cardiol. 2000;86:6HY11H. Ballantyne CM, Blazing MA, Hunninghake DB, et al. Effect on high-density lipoprotein cholesterol of maximum dose simvastatin and atorvastatin in patients with hypercholesterolemia: results of the Comparative HDL Efficacy and Safety Study (CHESS). Am Heart J. 2003;146(5):862Y869. Packard CJ, O’Reilly DS, Caslake MJ, et al. Lipoproteinassociated phospholipase A2 as an independent predictor of coronary heart disease. West of Scotland Coronary Prevention Study Group. N Engl J Med. 2000;343(16):1148Y1155. Ishida K, Cucchiara B. Therapeutic options to reduce LpPLA2 levels and the potential impact on vascular risk reduction. Curr Treat Options Cardiovasc Med. 2013;15(3): 313Y321. Persson M, Nilsson J, Nelson J, Hedblad B, Berglund G. The epidemiology of Lp-PLA2: distribution and correlation with cardiovascular risk factors in a population-based cohort Atherosclerosis. 2007;190(2):388Y396. Grundy SM, Cleeman JI, Daniels SR. Diagnosis and management of the metabolic syndrome: an American Heart Association/ National Heart, Lung, and Blood Institute scientific statement. Circulation. 2005;112:2735Y2752. Haffner SM, Valdez RA, Hazuda HP, Mitchell BD, Morales PA, Stern MP. Prospective analysis of the insulin-resistance syndrome (syndrome X). Diabetes. 1992;41(6):715Y722. Jeppesen J, Hansen TW, Rasmussen S, Ibsen H, Torp-Pedersen C, Madsbad S. Insulin resistance, the metabolic syndrome, and risk of incident cardiovascular disease: a population-based study. J Am Coll Cardiol. 2007;49(21):2112Y2119. McFarlane SI, Banerji M, Sowers JR. Insulin resistance and cardiovascular disease. J Clin Endocrinol Metab. 2001;86(2): 713Y771. Tso TK, Huang WN. Elevation of fasting insulin and its association with cardiovascular disease risk in women with systemic lupus erythematosus. Rheumatol Int. 2009;29(7): 735Y742. SPSS for Windows [computer program]. Version 16.0. Chicago, IL: SPSS Inc; 2007.

Program for Early Prevention of Cardiovascular Events 11 40. Curran PJ, Muthen BO. The application of latent curve analysis to testing developmental theories in intervention research. Am J Commun Psychol. 1999;27:567Y595. 41. Newman D. Longitudinal modeling with randomly and systematically missing data: a simulation of ad hoc, maximum likelihood, and multiple imputation techniques. Org Res Methods. 2003;6:328Y362. 42. Schafer JL, Graham JW. Missing data: our view of the state of the art. Psychol Methods. 2002;7:147Y177. 43. European Society of Hypertension-European Society of Cardiology guidelines for the management of arterial hypertension. J Hypertens. 2003;21:1011Y1053. 44. Brown BG, Zhao XQ, Chait A, et al. Simvastatin and niacin, antioxidant vitamins, or the combination for the prevention of coronary disease. N Engl J Med. 2001;345(22):1583Y1592. 45. Taylor AJ, Lee HJ, Sullenberger LE. The effect of 24 months of combination statin and extended-release niacin on carotid intima-media thickness: ARBITER 3. Curr Med Res Opin. 2006;22(11):2243Y2250. 46. Taylor AJ, Villines TC, Stanek EJ, et al. Extended-release niacin or ezetimibe and carotid intima-media thickness. N Engl J Med. 2009;361(22):2113Y2122.

47. Naito R, Miyauchi K, Ogita M, et al. Impact of admission glycemia and glycosylated hemoglobin A1c on long-term clinical outcomes of non-diabetic patients with acute coronary syndrome. J Cardiol. 2013;63(2):106Y111. 48. Nathan DM, McGee P, Steffes MW, Lachin JM, the DERG. Relationship of glycated albumin to blood glucose and glycated hemoglobin (HbA1C) values and to retinopathy, nephropathy and cardiovascular outcomes in the DCCT/EDIC Study. Diabetes. 2013;63(1):282Y290. 49. Reddy KJ, Singh M, Batsell RR, Bangit JR, Miraskar RA, Zaheer MS. Lipoprotein-associated phospholipase A2 mass is significantly reduced in dyslipidemic patients treated with lifestyle modification and combination lipidmodifying drug therapy. Prev Cardiol. 2010;13(3): 130Y134. 50. Society of Atherosclerosis Imaging and Prevention, in collaboration with the International Atherosclerosis Society. Appropriate use criteria for carotid intima media thickness testing. Atherosclerosis. 2011;214(1):43Y46. 51. Lavie CJ, Lee JH, Milani RV. Vitamin D and cardiovascular disease: will it live up to its hype? J Am Coll Cardiol. 2011;58(15):1547Y1556.

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Heart Health Open Access

http://dx.doi.org/10.14437/HHOA-1-104

Review

Received: Nov 11, 2014 Accepted: Nov 21, 2014 Published: Nov 26, 2014

Amy L. Doneen, DNP, ARNP, Heart Health Open Access 2014, 1:1

Cardiovascular Wellness and Optimal Oral Health: A symbiotic Relationship Amy L. Doneen, DNP, ARNP*, Alice Dupler, JD, APRN-BC, and Neva L. Crogan, PhD, ARNP, FAAN Corresponding Author: Amy L. Doneen, Medical Director, Heart Attack & Stroke Prevention Center, Adjunct professor Texas Tech Health Sciences Center USA; E-mail: adoneen@baledoneen.com

annually by the year 2030 [4]. One-third of all cardiovascular deaths occur in individuals less than 75 years of age [5]. Fifty percent of annual major coronary events are recidivistic and of these, fifty percent are fatal [6].

Event Reality: What causes a cardiovascular event? Cardiovascular Wellness and Optimal Oral Health In order to appreciate the oral/systemic connection as it relates to vascular wellness, it is important to understand health from the perspective of the arteries and the mouth. Arterial health (or cardiovascular wellness) is a state for which atherosclerosis is absent [1], and, if atherosclerosis is present in the arterial system, there is no inflammation driving further development of disease progression [2]. Optimal oral health, as it relates to vascular wellness, is an oral environment that lacks the inflammation to allow oral pathogens to invade the vascular system and create the opportunity for an unstable atherosclerotic disease state [3]. There are many conditions that cause vascular inflammation. Oral bacteria (periodontal disease) are one of those conditions.

Cardiovascular Disease: A costly condition Cardiovascular Disease (CVD) remains the leading cause of death and disability in developed countries, creating a catastrophic financial strain on our current health care system.

These statistics can be changed by understanding the mechanism for which heart attack and ischemic stroke occur. We can then fully appreciate the relationship between CVD and oral health. Atherosclerotic plaque silently develops in the artery wall, avoiding encroachment into the lumen resulting in an asymptomatic and potentially dangerous situation. When the artery wall weakens due to an influx of inflammation, the protective endothelial lining can rupture or erode, exposing the plaque to arterial blood flow, and subsequently creating the potential for thrombus formation. Surprisingly, the majority of these ruptures or erosions does not result in major CV events but rather create micro vascular thrombi that lead to micro vascular disease such as silent heart attacks, transient ischemic events, vascular dementia and diseases of ageing such as chronic kidney disease and peripheral arterial disease [7]. Regardless of the end result of the thrombus, the presence of an atheroma is sine qui non for a vascular event [7].

Inflammation: the keystone joining vascular and oral

The current health care paradigm is structured around treating

health

end-stage disease, treating the disease after it becomes evident.

Understanding this mechanism – the inflammatory relationship

The annual expenditure allocated to treat vascular disease has

between atherosclerotic plaque development and thrombus

skyrocketed to over 600 billion dollars, including direct and

formation is the key to CVD prevention. The symbiosis between

indirect costs. It is estimated to increase to 3.1 trillion dollars

CVD and periodontal disease starts here- at the inflammatory

Copyright: © 2014 HHOA. This is an open-access article distributed under the terms of the Creative Commons Attribution License, Version 3.0, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Volume 1 • Issue 1 • 104

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Citation: Amy L. Doneen (2014 Cardiovascular Wellness and Optimal Oral Health: A symbiotic Relationship. Heart Health Open Access 1:104

Page 2 of 4

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juncture. Periodontal Disease (PD) is one of many causes of this

toxins of Pg are directly involved in the development of

keystone ingredient – inflammation, both promoting the

atherosclerotic vascular disease.

development of plaque and the unpredictable cascade of plaque rupture and thrombus formation. The American Heart

Who’s role is it anyway?

Association’s meta-analysis determined that CVD was greatly

Appreciating the relationship between the inflammatory

increased in subjects with periodontitis and subsequently

cascades associated with oral health and CVD, a dialogue

confirmed an independent association between PD and CVD

between the medical provider and the dental provider must be

with Level A evidence [8]. Potentially even more concerning,

nurtured. A conundrum potentially exists when we find a chasm

oral bacteria associated with endodontic disease has been tied to

between the medical and dental models of care. This divide is

actual acute coronary events [9]. Cross-sectional epidemiologic

deeply rooted in academia and carried into practice. Many

studies demonstrate the association between periodontitis and

medical providers who treat vascular disease received minimal

elevated risk for CVD. Specific periodontal pathogens have

training to know how to properly assess for oral inflammation.

been shown to play a vital role in the atherogenic disease

Additionally, the dental providers may struggle to push

process [3]. Additionally, studies have focused on the systemic

boundaries of care beyond the oral cavity, potentially fearing

effect of periodontal intervention on surrogate indicators of

the public perception. For those practicing CVD prevention in

CVD, including serum inflammatory markers, serum lipid levels

the

and hemostatic factors [3].

involvement on the team, being so bold as to suggest that it is

The CORODENT study evaluated the role of periodontal

necessary if we want to mitigate the potentially devastating

pathogen burden on coronary events and PD. The controlled

effects of CVD. Statistically, 65-70% of adults see the dentist

study of 526 patients without a known history of coronary heart

annually whereas up to 20% of these patients have not had a

disease (CHD) had sub gingival samples of biofilm analyzed for

medical appointment in the preceding year.

medical

model,

celebrate

dental

professional

periodontal bacteria. The results reflected a statistically

significant association between the periodontal pathogen burden

The public agrees. Adult dental patients were surveyed as to

and the presence of CHD [10]. Additionally, the INVEST trial

their perception of receiving medical screenings while in the

[11], evaluated periodontal bacteria and hypertension in 653

dental setting and there was a 94% approval of this approach.

subjects without a history of stroke or heart attack. Findings

Specifically, 90% of the patients surveyed felt it important for

were adjusted for age, race, sex, education, BMI, smoking, DM,

dental professionals to screen for hypertension and over 80%

LDL and HDL. In subjects with the highest tertile of PD

felt it valuable to be screened for diabetes and CVD in the

pathogen burden, systolic blood pressure was 9mmHg higher

dental setting [12]. The overwhelming (>75%) opinion was that

and diastolic BP was 5 mmHg higher than in subjects with the

their view of the dental provider would improve for knowledge

lowest tertile. Lastly, and importantly, end toxins of gram-

and professionalism, competence and compassion [13]. In

negative bacteria, such as Porphyromonas gingivalis (Pg) is

addition to gaining public approval, periodontal therapy also

considered causative of periodontitis. Lipo polysaccharide end

saves healthcare costs in diabetic and CVD patients. Analyzing

toxin (LPS), a specific toxin of this bacterium, is common to

over 100,000 PD patients with diabetes and/or CVD, mean age

other bacterial diseases such as E. coli and Salmonella

48.7 (+ 10.9 years).PD treatment required > 4 dental visits

infections. Pg LPS has been shown to stimulate atherosclerotic

annually, mainly scaling and root planning along with flap

related gene expression in foam cells and to stimulate

surgeries as needed and routine cleanings. The primary outcome

transcription

adhesion

was all medical (non-dental) costs in years 2006-2009.The

molecules and growth factors [10] concluding that the end

secondary outcome was yearly hospitalizations/1000 clients in

pro-inflammatory

cytokines,

Citation: Amy L. Doneen (2014 Cardiovascular Wellness and Optimal Oral Health: A symbiotic Relationship. Heart Health Open Access 1:104

Page 3 of 4

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years 2005-2009. Treatment of PD resulted in a 40% decrease in

dental hygiene is a strong starting point. Atherosclerotic

annual dollars spent on stroke and diabetes. A 10% decrease in

vascular disease is a multi-faceted inflammatory condition that

resource

care.

involves many specialists to properly treat. The ideal medical

Hospitalizations were decreased on average 20-30% for CHD

model welcomes our dental colleagues to a team of specialists

related issues, including diabetes, stroke and heart disease [12].

that encompass providers in the areas of family practice,

expenditure

was

utilized

for

CHD

cardiology,

sleep

medicine,

endocrinology,

psychology,

Joining hands to prevent CVD

nutrition, exercise science and life coaching. We view

The language spoken between the medical and dental

inflammation driven by oral health on par with other

community in regards to CVD must be one of mutual

inflammatory causative factors such as insulin resistance, sleep

recognition. In the medical community, laboratory data is

apnea, dyslipidemia and hypertension among others. We ask for

utilized to reveal hidden causes of vascular inflammation. We

a partnership with our dental colleagues to join in the fight

utilize blood and urine tests to evaluate the effectiveness of

against the devastating effects of cardiovascular disease.

treatment, lifestyle and pharmaceutical interventions, on the

Together, we can achieve optimal wellness.

endothelium and intima layers of the artery, providing confidence to know that the patient is safe. Likewise, we embrace technology to identify asymptomatic atherosclerosis

References 1.

Belcaro G, Nicolaides AN, Ramaswami G, Cesarone MR,

and follow the disease over time. This approach, called the

De Sanctis M, et al. (2001) Carotid and femoral ultrasound

Bale/Doneen Method has been proven to be effective in

morphology screening and cardiovascular events in low

generating a positive effect on the atherosclerotic disease

risk subjects: a 10-year follow-up study (the CAFES-

process by achieving regression of disease in the carotid arteries

CAVE study). Atherosclerosis. 156:379-387.

[14]. Ultimately we are treating a disease that we hope our

Aldrovandi A, Cademartiri F, Arduini D, Lina D, Ugo F, et

patients never feel. If they were to ‘feel’ the disease, a rupture

al. (2012) Computed tomography coronary angiography in

or an erosion would have resulted in a thrombotic event.

patients

Optimal CV wellness and optimal oral health are tied together

significant coronary stenosis. Circulation. 126:3000-3007.

by a lack of inflammatory burden. Knowing that periodontal

with

acute

myocardial

infarction

without

Xiang Ying Ouyang, Wen Mei Xiao, Yi Chu, Shuang Ying

disease and endodontic pathogen burden are one of the critical

Zhou. (2011) Influence of periodontal intervention therapy

root causes of this inflammatory disease, we rely on our dental

on risk of cardiovascular disease. Periodontology 56: 227-

colleagues to participate in CVD prevention. We feel it to be

257.

our responsibility to learn how to assess for gingival

Go A, Mozaffarian D, Roger V, Benjamin E, Berry J, et al.

inflammation in the medical office and we ask our dental

(2014). Heart disease and stroke statistics – 2014 update: a

colleagues to participate in laboratory testing to determine

report from the American heart association. Circulation.

pathogen burden objectively with PCR laboratory testing so that

129: e28-e292.

the language between providers can be objective and

understood.

Roger. V, Go A, Lloyd-Jones D, Benjamin E, Berry J, et al.

(2012)

American

Heart

Association

Statistics

Committee and Stroke Statistics Subcommittee.

Heart

In addition to speaking the same laboratory language to

disease and stroke statistics: 2012 update: a report from the

diagnose PD and vascular inflammation, it is a solid idea to

American Heart Association Circulation. 125: e2-e220.

propose a care model that invites registered dental hygienists into the medical office to teach and assess patients about proper

Briffa T, Tonkin A. (2013) Put disease prevention first. Circulation. 128: 573-575.

Citation: Amy L. Doneen (2014 Cardiovascular Wellness and Optimal Oral Health: A symbiotic Relationship. Heart Health Open Access 1:104

Page 4 of 4

http://dx.doi.org/10.14437/HHOA-1-104

7. 8.

Arbab-Zadeh A, Nakano M, Virmani R, Fuster V. (2012) Acute coronary events. Circulation. 125:1147-1156.

Sacco RL, et al. (2005) Periodontal Microbiota and

Lockhart P, Bolger A, Papapanou P, Osinbowale O,

Carotid Intima-media thickness: The oral infections and

Trevisan M, et al. (2012) Periodontal disease and

vascular

atherosclerotic vascular disease: does the evidence support

Circulation.111;576.

disease

epidemiology

Study

(INVEST)

an independent association? A scientific statement from

12. Jeffcoat, M. Impact of periodontal therapy on general

the American Heart Association. Circulation published

health: Evidence from insurance data for five systemic

online.

conditions. Am J Prev Med 47: 166-174.

Pessi T. (2013) Bacterial signatures in thrombus aspirates

13. Greenberg B. Glick M. Assessing systemic disease risk in

of patients with myocardial infarction. Circulation.

a dental setting: a public health perspective. Dent Clin

127:1219-1228.

North Am, 55: 863-874.

10. Lei

11. Desvarieux M, Demmer RT, Rundek T, Boden-Albala J,

(2011)

Porphyromonas

gingivalis

14. Feng D, Esperat C, Doneen A, Bale B, Song H, Green A.

lipopolysaccharide (LPS) alters atherosclerotic-related

8-year outcomes of a program for early prevention of

gene expression in oxidized low-density-lipoprotein-

cardiovascular

induced macrophages and foam cells. J Periodontal Res.

Cardiolvasc Nurs. 2014.

events.

growth

curve

analysis.J

Statistical Fact Sheet 2013 Update

Women & Cardiovascular Diseases Cardiovascular Disease (CVD) (ICD/10 codes I00-I99, Q20-Q28)  More than one in three female adults has some form of cardiovascular disease (CVD).  Since 1984, the number of CVD deaths for females has exceeded those for males.  In 2009, CVD was the cause of death in 401,495 females. Females represented 51.0% of deaths from CVD.  The 2009 death rate from CVD was 236.1. Death rates were 190.4 for white females and 267.9 for black females.  In 2010, CVD was the first listed diagnosis of 2.8 million females discharged from short-stay hospitals. 

In 2010, 25.1% of bypass and 32.9% of PCI patients were female. 31.3% of heart transplant patients in 2011 were female.

Major Causes of Death for Males and Females, 2009

A indicates cardiovascular disease plus congenital cardiovascular disease (ICD-10 I00-I99, Q20-Q28); B, cancer (C00-C97 ); C, accidents (V01-X59,Y85-Y86); D, chronic lower respiratory disease (J40-J47); E, diabetes mellitus (E10-E14); F, Alzheimer disease (G30). Source: NCHS.

Coronary Heart Disease (CHD) (ICD/10 codes I20-I25) (ICD/9 codes 410-414, 429.2)  About 6.6 million females alive today have CHD. Of these, 2.6 million have a history of myocardial infarction (MI, or heart attack).  Each year new and recurrent MI and fatal CHD will impact an estimated 380,000 women.  The 2009 overall CHD death rate was 116.1. Death rates were 84.9 for white females and 110.3 for black females. 

26% of women age 45 and older who have an initial recognized MI (heart attack) die within a year compared with 19% of men. In part because women have heart attacks at older ages than men do, they’re more likely to die from them within a few weeks.

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64% of women who died suddenly of CHD had no previous symptoms.

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518,000 females diagnosed with CHD were discharged from short-stay hospitals in 2010.

Women & CVD - 2013 Statistical Fact Sheet Cardiovascular Disease Mortality Trends for Males and Females United States: 1979–2009

Source: NCHS.

Angina Pectoris (ICD/10 code I20) (ICD/9 code 413)  More women than men have angina in total numbers (4.1 million vs. 3.7 million).  Among non-Hispanic women age 20 and older, 2.8% of non-Hispanic whites; 5.4% of nonHispanic blacks and 3.3% of Mexican Americans have angina.  Each year about 180,000 women over age 45 are diagnosed with stable angina. Congenital Cardiovascular Defects (ICD/10 codes Q20-Q28) (ICD/9 codes 745-747) 

The 2009 overall death rate for congenital cardiovascular defects was 1.0. Death rates were 0.9 for white females and 1.2 for black females.

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27,000 females were discharged from short-stay hospitals in 2009 with a diagnosis of congenital cardiovascular defects.

Age-Adjusted Death Rates for Coronary Heart Disease, Stroke, and Lung and Breast Cancer for White and Black Females, 2009

Source: NCHS.

Women & CVD - 2013 Statistical Fact Sheet Stroke (ICD/10 codes I60-I69) (ICD/9 codes 430-438) 

An estimated 3.8 million female stroke survivors are alive today.

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Among women age 20 and older, the following have had a stroke: 2.9% of non-Hispanic whites; 4.7% of non-Hispanic blacks and 1.4% of Mexican Americans.

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Each year about 55,000 more women than men have a stroke. This is because the average life expectancy for women is greater than for men, and the highest rates for stroke are in the oldest age groups.

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In 2009, stroke caused the death of 76,769 females (59.6% of total stroke deaths).

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The 2009 overall death rate for stroke was 38.9. Death rates were 36.6 for white females, 50.2 for black females, 28.0 for Hispanic females, 29.6 for Asian/Pacific Islander females, and 24.6 for American Indian/Alaska Native females.

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In 2010, 530,000 females were discharged from short-stay hospitals after having a stroke.

High Blood Pressure (HBP) (ICD/10 codes I10-I15) (ICD/9 codes 401-404) 

One in three adults in the United States has HBP.

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A higher percentage of men than women have HBP until age 45. From 45–64 the percentage for men and women are similar. After that a much higher percentage of women have HBP than men.

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Among women age 20 and older, the following have HBP: 30.7% of non-Hispanic whites; 47.0% of non-Hispanic blacks and 28.8% of Mexican Americans.

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In 2009, 34,094 females died from HBP. They represented 55.2% of deaths from HBP.

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The 2009 overall death rate from HBP was 18.5. Death rates were 14.4 for white females and 38.3 for black females.

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272,000 females diagnosed with HBP were discharged from short-stay hospitals in 2010.

Heart Failure (HF) (ICD/10 code I50.0) (ICD/9 code 428.0) 

About 2.4 million females alive today have HF. Each year, about 320,000 new cases are diagnosed in females.

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In 2010, the overall prevalence for people age 20 and older is 2.1%. Among women, the following have HF: 1.7% of non-Hispanic whites; 3.0% of non-Hispanic blacks and 1.1% of Mexican Americans.

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In 2009, there were 32,847 female deaths from HF (58.2% of HF deaths).

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The 2009 overall any- mention death rate from HF was 82.3. Death rates were 72.2 for white females and 79.7 for black females.

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522,000 females diagnosed with HF were discharged from short-stay hospitals in 2010.

Smoking  In 2011: 

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Females students (grades 9-12) were less likely than male students to smoke cigarettes (16.1% vs. 19.9%), smoke cigars (8.0% vs. 17.8%), or use smokeless tobacco (2.2% vs. 12.8%). Among adults, 21.3% of men and 16.7% of women smoke cigarettes.

High Blood Cholesterol and Other Lipids  Among children 4 to 11 years of age, the mean total blood cholesterol level is 161.9 mg/dL.For boys, it is 162.3 mg/ dL; for girls, it is 161.5 mg/dL.  Among adolescents 12 to 19 years of age, the mean total blood cholesterol level is 158.2 mg/dL. For boys, it is 156.1 mg/dL; for girls, it is 160.3 mg/dL. ©2013 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited.

Women & CVD - 2013 Statistical Fact Sheet 

Among adults age 20 and older:  41.3% of men and 44.9% of women have total cholesterol levels of 200 mg/dL or higher.  12.7% of men and 14.7% of women have levels of 240 mg/dL or higher.  31.9% of men and 30.0% of women have an LDL cholesterol of 130 mg/dL or higher.  31.8% of men and 12.3% of women have HDL cholesterol less than 40 mg/dL.

Physical Inactivity 

Girls are more likely than boys to report inactivity (17.7% vs. 10.0%).

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In a study of 12 812 youth 9 to 18 years of age, the physical activity level in boys and girls declined starting at the age of 13, with a significantly greater decline in activity among girls.

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Only 17.1% of adult women met the 2008 Federal Physical Activity Guidelines in 2011.

Overweight and Obesity 

An estimated 30.4% of girls age 2 to 19 are overweight or obese; 25.6% non-Hispanic whites, 41.3% non-Hispanic blacks, and 38.2% Mexican Americans.

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Of these girls, 15.0% are obese; 11.7% non-Hispanic whites, 24.3% non-Hispanic blacks, and 18.2% Mexican Americans

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An estimated 63.7% of women age 20 and older are overweight or obese; 60.2% non-Hispanic whites, 79.9% non-Hispanic blacks, and 78.2% Mexican Americans.

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Of these women, 35.6% are obese; 32.5% non-Hispanic whites, 53.9% non-Hispanic blacks, and 44.8% Mexican Americans.

Diabetes Mellitus (ICD/10 codes E10-E14) (ICD/9 code 250) 

Of the estimated 19.7 million American adults with physician-diagnosed diabetes, about 10.1 million are women; 6.2% of non-Hispanic whites, 15.4%of non-Hispanic blacks and 12.0% of Mexican Americans.

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Of the estimated 8.2 million Americans with undiagnosed diabetes, about 2.9 million are women; 1.8% of non-Hispanic whites, 2.9% of non-Hispanic blacks and 4.7% of Mexican Americans.

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Of the estimated 87.3 million Americans with pre-diabetes, about 33.6 million are women; 30.0% of non-Hispanic whites; 29.0% of non-Hispanic blacks and 31.9% of Mexican Americans.

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In 2009, diabetes killed 33,651 females. The overall death rate from diabetes was 20.9. Death rates were 15.7 for white females and 35.9 for black females.

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319,000 females diagnosed with diabetes were discharged from short-stay hospitals in 2010. For additional information, charts and tables, see Heart Disease & Stroke Statistics - 2013 Update.

Additional charts may be downloaded directly from the online publication at: http://circ.ahajournals.org/lookup/doi/10.1161/CIR.0b013e31828124ad Or at: www.heart.org/statistics The American Heart Association requests that this document be cited as follows: Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB; on behalf of the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics—2013 update: a report from the American Heart Association. Circulation. 2013; 127:e6-e245. If you have questions about statistics or any points made in the 2013 Statistical Update, please contact the American Heart Association National Center, Office of Science & Medicine at statistics@heart.org. Please direct all media inquiries to News Media Relations at inquiries@heart.org or 214-706-1173.

AN INCREDIBLE FIX FOR LOWER BACK PAIN Mr. Brian Bradley (Ergonomic Instruction)

The Real Source of Hamstring Pain “Stretching may temporarily relieve tight hamstrings, but the origin of the discomfort could be found elsewhere in the body.”

Pete Egoscue

A client wrote to us saying he was having terrible struggles with his hamstrings. He said that he stretched them every day but still endured terrible pain and asked if I had any recommendations or advice. Well, I do. This one’s for him and anyone else whose hamstrings are causing pain or constantly feel tight. Pretty much all of you in the Dental field have been rotating and flexing forward on one side of the patient for decades. Now you are paying for this pattern and NOW is the time to reverse it. In all cases of chronic stiffness or tightness, the stiff, tight muscle is not the issue. Rather, it’s the signal that the balance of the muscle action has been compromised and compensated for, probably for a prolonged period of time, and the problem is actually elsewhere. In the case of stiff hamstrings, the problem is about the loadbearing joints, the shoulders and ankles, yes, but primarily the hips and knees. The hamstring is tight for a reason and when someone tells you to just stretch your hamstrings, you are just doing the same thing 24

everyday and expecting a different result…Insanity! First, a very brief anatomy lesson. The hamstring is actually comprised of three muscles: the biceps femoris, the semitendinosus, and the semimembranosus. All three cross both the hip and knee joints, but the latter two muscles are also involved in the rotation of the knee. Put simply, because of their attachments, the hamstrings are not meant to be tight and short on a daily basis, limiting their stability and movement roles.

All muscles in the body respond to stimulus, so if the hamstring is tight, it’s because of the stimulus, or information, it is receiving from the hip and knee joints. In other words, if you have chronically stiff hamstrings, there’s nothing wrong with your hamstrings. They’re doing only what the hips and knees tell them to do. The problem lies with the hips and knees, and the upshot is that they are not balanced. Here are a couple of tests you can try to see that these joints aren’t balanced. First, grab a pair of shoes, any pair that you wear often—could be office shoes, running shoes, tennis shoes, whatever. Place them together, sole to sole, and see if the wear patterns mesh together. If you’re balanced, they will mesh, but my hunch is they don’t. Another test: throw on a pair of shorts and stand in front of a mirror. Look at your knees. You’ll most likely see that one or even both of your knees don’t point

straight at the mirror; they’re turned to the side. Or you’ll notice that one or both aren’t lined up with the feet, meaning your foot and knee aren’t pointing in the same direction. For instance, your foot might be angling out to the right while your knee still points straight ahead. Again, the problem is not the hamstring. The problem is the joints being out of position, so much so that the body thinks the hamstring needs to be shortened, which is why the hamstring is shortening and causing stiffness. (Which is also why just stretching the hamstring isn’t going to bring relief; stretching doesn’t engage or adjust the joints, where the problem is.) Or…the problem could be something else. All skeletal muscles are activated by the Central Nervous System, i.e. the nerves. The hamstrings are innervated by a nerve that originates in the lumbar spine, or lower back. With the pelvis out of position, there’s an impingement on the signal of that nerve activity, which means the pain you feel in your hamstrings could really be about pain you’re feeling from your sciatic nerve. Either way, you need to reposition and rebalance the load-bearing joints, not only the hip and knee joints but also the shoulder and ankle joints because the body is one unit, and the joints all talk to each other. The impinged nerve is just as much about the shoulders as it is the pelvis, so we need to loosen up the mid and upper 26

back, and it’s just as much about the ankles as it is the knees. Remember that test with the shoes? So anyone having problems with hamstrings, it’s probably not your hamstrings. It’s your joints, and your solution isn’t stretching your hamstrings. Your solution is balancing your body and realigning your joints so that your body performs as a single unit. Known as the Father of Postural Therapy, Pete Egoscue has helped relieve thousands of people from their chronic pain, including many of the world’s leading athletes. For more information on Pete and any of his 25 clinics worldwide, go to egoscue.com or prior to the SSC Symposium, you can email Brian Bradley (SSC Presentor) at bbradley@egoscue.com.

Understanding the Source of Back Pain

Up to 85 percent of Americans experience back pain at some point in their lives. Here's an explanation of why so many of us are suffering.

Pete Egoscue

In the United States, back pain is the #1 complaint people bring to their Doctors. What is the cause of this back pain that is so prevalent in our culture? Great question and the answer is very simple. Let’s discuss the spinal anatomy. The human spine is called “the segmented bone,” meaning, it’s a bone that the body recognizes as one bone, in the same way it recognizes, say, the femur (thigh) or humerus (upper arm), but unlike those bones, it is segmented. A bone in parts, and those parts are called vertebrae. That said, when it comes to function, the body does not recognize the individual parts of the spine; it stimulates and responds to the spine as if it is a single unit, one long lone bone. Lets call it a really flexible bone. That flexible spine is why, regarding range of motion, humans have more capability than all other vertebrates. The monkey, the zebra, your pet dog—you name it, they all have spines whose vertebrae do not allow for the full range of 28

motion that our vertebrae allow for. This is a quintessential case of the whole being greater than the sum of its parts. But there’s one catch: for that full range of motion, our spine must be in the shape of an “S” curve.

When the spine is an “S” it is considered to be in a neutral position, and its load bearing is distributed evenly among all vertebrae. As a result, people with the “S” spine have no restrictions on their range of motion, no matter what they’re doing—standing, sitting, walking, lying down, surfing, playing volleyball, gardening. People with back pain don’t have that full range of motion, at least not without some pain of degrees ranging from minor to debilitating, and that’s because their spines are no longer in an “S” position. They’ve been contorted into various forms, some going from being an “S” to a “C” (which, among other downsides, is a far less popular letter on Wheel of Fortune). The “C” curve we are talking about is very popular among Dentists and their staff. The constant forward flexion and one-sided rotation around the patient creates this dysfunctional pattern induced curvature. The result? Chronic and acute pain, performance limitations and emotional stress.

When that spine is not an “S,” the load that it bears is no longer evenly distributed among all vertebrae. Some vertebra are doing more work, more load bearing, than they were intended, and that’s when the various forms of back pain come in. But how did the spine lose its “S” shape? That’s all about the alignment of our four load-bearing joints—the 30

shoulders, hips, knees and ankles, four to each side, eight joints in total. When these joints are properly aligned, they sit directly on top of each other, and all vertical and horizontal planes are straight, and the spine remains and “S.”

But when those load bearing joints are not aligned, that’s when the best laid plans of our human design go awry and our spines become “C’s” or some other shape and acquire any range of problems that cause the load bearing of the spine to be distributed unevenly. Back pain, and everything it represents, is nothing more 31

than the body telling the host that he or she cannot load the spine the way the spine was designed to load in the position of the “S” curve. Why? Because the body is not aligned and the spine reacts by altering its shape to compensate, and in that compensation comes pain. (All of this refers to most common back pain and does not include bodies that just suffered a major trauma.) But here’s the thing. The human body is so amazing that that pain from compensation is the body doing exactly what it’s supposed to do. Discs herniate because they can and, in fact, are supposed to when the spine is being compromised in a way where the hard, boney tissue is susceptible to injury. But that herniated disc is NOT the cause of the problem. It IS the result of the underlying problem. Their Posture! The misalignment is the body’s way of signaling to us that there’s a problem. Similarly, stenosis (the bony build up along the spine causing nerve impingement) is simply a callous that the body forms to protect the nerve root from the friction occurring through misalignment. Again, the stenosis isn’t the cause of the problem. It’s the result and could explain why your low back and neck pain are constantly getting in the way of the life you want to live.

And a great number of back surgeries today do not address the problem; they address the symptom, regrettably leaving the original problem in tact.

The way to address the problem is to rebalance the body into proper alignment. Once you do that, then your muscles will tell your spine to return to an “S” curve, and any back pain you felt will be alleviated because all the weight that the spine is loading will again be distributed evenly among all the vertebrae. And then you can get back to doing all the things you used to do that the rest of the mammal world, with its less flexible spine, simply cannot. At Symposium, you will have the opportunity to discuss your posture, pain and performance issues with Brian Bradley (SSC Presentor) and his staff. If you have any questions, you can email him at bbradley@egoscue.com Known as the Father of Postural Therapy, Pete Egoscue has helped relieve thousands of people from their chronic pain, including many of the world’s leading athletes. For more information on Pete and any of his 25 clinics worldwide, go to egoscue.com.

A HOPELESS TOOTH IS NOT A USELESS TOOTH Dr. Marco A. Brindis

J Oral Maxillofac Surg 67:49-59, 2009, Suppl 3

Orthodontic Tooth Extrusion to Enhance Soft Tissue Implant Esthetics Marco A. Brindis, DDS,* and Michael S. Block, DMD† Purpose: The purpose of this report was to review the published data on orthodontic extrusion and

make recommendations for its use according to the evidence presented, including the technique for use by clinicians. Materials and Methods: A MEDLINE search was performed to identify reports in referenced journals in English. These studies were collated and reviewed for clinical and animal data on orthodontic extrusion. In addition, the experiences of our team using orthodontic extrusion was added to the evidence used to make the recommendations. Results: From this background information, orthodontic tooth extrusion is able to move the soft tissues when the sulcular attachment apparatus is intact. Bone formation as the tooth is extruded is dependent on the vector of the movement of the tooth. The rate of tooth extrusion is effected by the bone–tooth attachment. Conclusions: When used as we have described, extrusion can effectively move the facial gingival margin to allow for esthetic restoration of implants placed in the extruded tooth position. © 2009 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 67:49-59, 2009, Suppl 3 The position of the facial gingival margin and the papilla are critical for an ideal esthetic appearance of implant-supported crowns. After placement of the final crown on an implant in the anterior maxilla, the facial gingival margin can recede apically 0.5 to 1.4 mm.1-4 This recession usually occurs during the first 3 to 6 months after surgery.5 If the pretreatment position of the gingiva is at the ideal location, or if it is apical to the ideal planned position, the assumed gingival recession will result in an asymmetric esthetic result. One method to move the soft tissues toward the incisal edge is orthodontic movement of the affected tooth coronally, which will move the surrounding soft tissues with it, resulting in improved

gingival morphology and position, enhancing the final restoration.6-9 The MEDLINE search revealed studies on the histologic changes when a tooth is extruded and the experience of clinicians with tooth extrusion before implant placement. However, no well-controlled clinical trials were found, other than case series, to verify the techniques used for this method. In 1940, Oppenheim10 examined the natural phenomenon of eruption in young patients after a tooth was modified by removing the occlusal contacts. The tooth erupted coronally with bone, increasing the height of the alveolar crest.10 The coronal movement of teeth has been used to reduce pocket depth and change the architecture of both hard and soft tissues of the periodontium.11 Ingber introduced the concept of force eruption of a tooth to treat isolated, 1- and 2-wall infraosseous defects.12 When a root is orthodontically extruded, the gingiva and supporting structures will move with the tooth to a position coronal to the gingival margin present on the adjacent teeth. This therapy can be used to enhance the final esthetic result.13 Forced eruption using orthodontic appliances has been used to manage isolated nonrestorable teeth because of trauma, caries, or iatrogenic dentistry by apical movement of the attached gingiva and the tooth from the alveolar bone. This, in conjunction with fibrotomy, allows for creation of the crown margin with a healthy biologic width.13-16 Orthodontic treatment for crown lengthening to increase the fer-

*Assistant Professor, Department of Prosthodontics, Louisiana State University School of Dentistry, New Orleans, LA. †Clinical Professor, Department of Oral and Maxillofacial Surgery, Louisiana State University School of Dentistry, New Orleans, LA; and Private Practice, Metairie, LA. Drs Brindis and Block state no financial arrangement or affiliation with a corporate organization or a manufacturer of a product discussed in this article. Address correspondence and reprint requests to Dr Brindis: Department of Prosthodontics, Louisiana State University School of Dentistry, Florida Ave, Room 5465 Box 222, New Orleans, LA 70119;e-mail: mbrind@lsuhsc.edu © 2009 American Association of Oral and Maxillofacial Surgeons

0278-2391/09/6711-0307$36.00/0 doi:10.1016/j.joms.2009.07.013

ORTHODONTIC TOOTH EXTRUSION AND IMPLANT ESTHETICS

ule effect by exposing sound tooth structure is one example of using orthodontic tooth eruption for improved patient treatment.17 The period needed for this type of procedure is 4 weeks, with a 6-week period required for stabilization with passive retention. The results from animal and clinical studies have suggested that tooth extrusion produces stretching of the supracrestal and principal fibers, resulting in bone formation at the apex and within the alveolar crest.10,18 After the extrusion process has been completed, the tooth-bone attachment fibers return to the pre-extrusion orientation, and the supracrestal fibers might remain stretched for longer periods.19 The attachment apparatus follows the controlled eruption of the tooth. Partial fiber resection results in less bone formation at the coronal region of the extruded tooth.20 Ritchey and Orban21 concluded that as a tooth is extruded, the relationship between the alveolar crest and cementoenamel junction is maintained. As a tooth is extruded, the mucogingival junction will maintain a constant position, with an increased thickness of the band of keratinized gingiva.22 When the mucogingival junction stays in its original position, the gingival margin will follow the eruption, creating new keratinized gingiva. Gingival hyperplasia occurs, effectively moving the facial gingival margin coronally. By maintaining the soft tissue sulcular attachment to the tooth, the gingival margin will move coronally with the tooth. The soft tissue genesis covering the labial bone defects allows for subsequent bone grafting at extraction after extrusion and an esthetic restoration. The vector of tooth extrusion is critical to bone formation or the loss of bone on the facial aspect of the tooth. Labial bone resorption occurs when the tooth is tipped buccally, placing pressure on the labial bone. If excessive bone resorption occurs, the epithelial attachment might move less than the actual tooth movement, with the attachment migrating along the root surface.19,21,22 Reitan23 suggested that tipping adult teeth facially might cause bone destruction with little compensatory bone formation, resulting in root dehiscence. If the tooth extrusion vector is parallel to the labial bone, less resorption of the labial bone will occur. Crestal apposition of the bone can result, with 2 to 3 mm of additional bone at the crest.19,22 Crestal bone formation can occur when a tooth is moved vertically; however, if the tooth is moved along a protrusive vector, the facial aspect of the tooth will place compression on the labial bone, with loss of the facial bone.24,25 If the tooth is erupted along its axis, the bone in the interdental region should follow the tooth movement, relocating the bone on a tooth to within 5 mm of the contact point, for papilla support. When 1 implant is

proposed adjacent to a tooth with crestal bone apical to the toothâ&#x20AC;&#x2122;s cementoenamel junction, eruption of the tooth can be critical for full papilla between the tooth and implant. The bone must be relocated to 5 mm from the planned interdental contact.3,6,26-31

Orthodontic Extrusion in Proposed Implant Sites Tooth extrusion can enhance the soft and hard tissue profiles before implant placement and restoration.32-39 A tooth is connected to orthodontic appliances and extruded under controlled conditions to move the attachment apparatus and bone. This provides the necessary ridge morphology for an ideal esthetic restoration. The newly formed bone resulting from the orthodontic tooth extrusion is viable, as evidenced by the presence of osteocytes within the bony lacunae.40 After a tooth has been extruded, the placement of an implant at tooth removal can reduce recession of the facial gingival margin2 and shorten the time from tooth removal to eventual restoration.2,41,42 When labial bone is present, immediate placement of an implant has a high incidence of success without adverse effects on the total healing response.2 If, after tooth extrusion, the labial bone is deficient, the socket will require grafting and a delayed treatment protocol. In a well-controlled prospective clinic trial, gingival recession occurred 1-mm less than when the implant was placed immediately after tooth extraction using a 1-stage approach.2 If the gingival margin on the tooth to be removed is apical to the planned gingival margin, extrusion of the tooth before its removal is recommended to provide an ideal soft tissue position. Before extraction of a tooth in the esthetic zone, the facial gingival margin should be at least 2 mm coronal to its planned position after the final crown is placed. This requirement anticipates gingival margin recession during the implant and restorative process. If the patientâ&#x20AC;&#x2122;s tooth has thin labial bone or thin gingiva, most likely the gingival margin will move apically after the final restoration.1 Therefore, when using orthodontic extrusion, overcorrection of the gingival margin coronally is one goal to be achieved.43

Orthodontic Forces Necessary for Tooth Extrusion The amount of force necessary to slowly extrude a tooth will be dependent on the amount of bone on the tooth to be extruded. Brackets are placed on the tooth to be extruded and the adjacent teeth sufficient to control the extrusive movement, with no movement of the teeth used for anchorage. For extrusion, the

BRINDIS AND BLOCK

forces necessary to move the tooth slowly can be as low as 25 to 30 g.19 Depending on the length of the root and the level of ankylosis, the necessary force for extrusion can be as high as 50 to 75 g.44 These values are within the range of forces that will produce an optimal tissue response with bone formation around the tooth.45 When extruding a tooth that has had previous root canal therapy and some degree of ankylosis or dense bone around the tooth, more force might be necessary and should be monitored with a stress and tension gauge.22 The rate of tooth extrusion has not been well described in published studies. Slow movement is recommended. The tooth extrusion can be as slow as 1 mm/month46; however, tooth extrusion can also be as rapid as 1 mm/week without obvious clinical damage to the periodontal ligament space. A period of 3 to 6 weeks might be sufficient to extrude a compromised tooth in many patients. However, excessive force and an accelerated rate of movement results in the risk of tissue damage and ankylosis.44 In our experience, when less than 5 mm of bone remains at the apical region of the tooth, the tooth can move quite rapidly with minimal orthodontic force (Fig 1). These patients should be seen often, if not daily, to modify the orthodontic appliance to avoid excessively rapid tooth movement because of the minimal bone anchorage on the tooth to be extruded. Because no data are available from well-documented clinical trials or case series, the rate of extrusion should follow these general principles: 1. Avoid moving the tooth faster than the accompanying movement of the gingiva. The gingiva should move with the tooth. 2. Avoid moving the tooth rapidly, which will result in excessive tooth instability. 3. Move the tooth with maintenance of healthy gingiva. 4. Move the tooth without excessive discomfort to the patient. 5. Move the tooth with constant observation of the incisal edge, which will require modification to avoid traumatic occlusion as the tooth erupts. 6. Move the tooth at a rate that does not move the adjacent teeth used for anchorage. One of the indications for forced eruption is when the crown of the tooth is fractured or has severe decay. In these cases, it is critical to restore the tooth temporarily to have a surface to which to attach the brackets. This temporary must be at the full contour of the tooth to be restored. This prevents the anchorage teeth from tipping toward the semiedentulous space and preserves the mesiodistal distance (Fig 2).

Stabilization After Tooth Extrusion After the tooth has been extruded, it should be stabilized to allow for bone maturation. Our suggestions for the period necessary for tooth stability before removal and implant placement have not been determined from well-controlled clinical trials but from our clinical experience. After active tooth movement has been completed, 6 to 12 weeks of stabilization is usually needed to allow for tooth stability and bone consolidation.44 The interval of tooth stabilization from extrusion to tooth removal and implant placement has ranged from 6 to 34 weeks.6,14,20,22,46 Confirmation of bone consolidation in the gap created by tooth extrusion using radiography is an objective method to determine when it is appropriate to begin the next step. In general, 12 weeks should be allowed before tooth removal and implant placement, unless bone has formed earlier. As soon as is appropriate, the orthodontic appliances should be removed and the teeth stabilized using traditional dental techniques such as a temporary fixed partial denture or bonding. A removable orthodontic retainer-type vacuum form can also be used to stabilize the tooth, or orthodontic wires with a tooth bracketed to the orthodontic wire can be used.

Contraindications for Tooth Extrusion The contraindications for orthodontic extrusion include 1) the presence of chronic, uncontrollable inflammatory lesions, including combined endodontic-periodontic lesions and fractured roots; 2) an inability to control inflammation and acute infection that would adversely affect healing and the overall response to treatment; 3) an absence of attachment apparatus because forced eruption only relocates the existing attachment, it does not create a new attachment6; 4) the presence of complete bony ankylosis of tooth to be extruded because an attempt to erupt an ankylosed tooth would result in intrusion or undesirable movement of the anchorage teeth.

Limitations for Orthodontic Extrusion If the goals for using orthodontic extrusion of a tooth before implant placement include improved gingival margin position or improvement of the underlying bone levels, the limitations of extrusion include the following. In cases of severe gingival recession associated with bone loss close to the toothâ&#x20AC;&#x2122;s apex, the final position of the gingival margin after extrusion might not be

ORTHODONTIC TOOTH EXTRUSION AND IMPLANT ESTHETICS

FIGURE 1. A, Initial presentation of a patient with severe root resorption of her left central incisor and left lateral incisor. Facial gingival margins were apical to ideal location and not favorable for an esthetic result. B, Periapical radiograph showing severe resorption and lack of bone at apical region of the maxillary left central and lateral incisors. C, Orthodontic brackets placed on teeth, and extrusion process initiated. Note slight bend in wire, which will gently extrude left central incisor and lateral incisor. D, Periapical radiograph taken 2 weeks after tooth extrusion process started. Rapid tooth extrusion occurred secondary to bone tooth attachment. E, After teeth were extruded, they were stabilized in erupted position for 3 months. Two implants were placed in sequence 6 weeks apart to preserve interdental soft tissue and bone. Healing abutments placed to support soft tissue during integration period. F, Implants were provisionalized with teeth on orthodontic wire. Note improvement of gingival facial margin. Brindis and Block. Orthodontic Tooth Extrusion and Implant Esthetics. J Oral Maxillofac Surg 2009.

satisfactory to establish ideal final crown esthetics. In cases in which severe circumferential bone loss is present, preventing implant placement, orthodontic extrusion will not create adequate vertical bone formation for ideal implant positioning. The amount of vertical bone formation is difficult to predict in some

cases. Any horizontal bone deficiency will not be restored to normal width using orthodontic extrusion. If the alveolar process is protrusive in shape, the loss of labial bone before and after tooth extrusion might prevent implant placement at extraction. Finally, a lack of bone density after tooth extrusion may

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tion is computed by dividing the width of the clinical crown by its length. As a rule, a pleasing width-tolength ratio for maxillary central incisors is 75% to 80%.47 The length of the esthetic central incisor is generally 10.5 to 11.0 mm.47 A diagnostic wax-up is created to establish for the patient the ideal incisor show and ideal tooth proportion, while establishing the ideal gingival plane. This information is then used to determine the needed position of the facial gingival margin of the teeth to be restored. Knowing the specific vertical position of the planned gingival margin determines the implant position. Using the patientâ&#x20AC;&#x2122;s current soft and hard tissue profiles, the need for orthodontic extrusion is confirmed. The depth of the implant on the anterior maxilla should be 3 mm from the free gingival margin. This depth allows for development of a proper emergence profile for the final crown.43,50 FIGURE 2. A, B, By attaching orthodontic bracket to full contoured temporary crown with appropriate interproximal contacts, adjacent teeth maintained their orientation without tipping into extruded tooth space. As a tooth erupted, the full contour was maintained and might need to be revised as it is shortened owing to vertical movement of tooth. Brindis and Block. Orthodontic Tooth Extrusion and Implant Esthetics. J Oral Maxillofac Surg 2009.

necessitate additional hard tissue grafting to preserve the labial ridge form, because thin bone tends to resorb after implant placement.

Orthodontic Tooth Extrusion Technique PREOPERATIVE CLINICAL EVALUATION

For the esthetic zone, a clinical esthetic analysis, including radiographs, should be performed to identify the proper position of the incisive edge and proper length of the incisor (Figs 3A-C). Establishing the incisal reference is the first step for a predictable esthetic result.47,48 With the patientâ&#x20AC;&#x2122;s lips in a relaxed, slightly opened position, the amount of incisor showing at rest is measured and recorded. The desired amount of the central incisor showing at rest with the lips apart is 3 to 4 mm for females and 2 to 3 mm for males.49 The smile line and gingival display are recorded to determine how critical is the position of the gingival margin at the end of treatment. Any deficiencies or excess tooth show is determined and will be used to create an esthetic setup. Once the incisal edge position has been established, a diagnostic cast is mounted with that reference. Next, with the mounted casts, the esthetic tooth proportion should be established in the diagnostic setup/wax-up (Fig 3D). The tooth propor-

TOOTH PREPARATION BEFORE ORTHODONTIC THERAPY

Orthodontic brackets are needed to extrude a tooth using conventional orthodontic wires. The current status of the tooth will dictate the necessary steps needed to secure an orthodontic bracket in the correct position on the tooth. A new temporary restoration might be necessary (Figs 3E,F). Because of the need to reduce the incisor edge during the extrusion process, root canal therapy might be necessary before tooth eruption. It is important to plan for tooth length reduction to prevent tooth tipping secondary to inappropriate tooth contact as the tooth erupts. The diagnostic plan is used to determine the amount of vertical extrusion necessary to achieve the ideal result. Bracket placement should consider the planned final position of the tooth (Figs 3G-J). It might be necessary to replace brackets on the extruded tooth to carefully control the rate of extrusion. The brackets should be placed along the cervical margin, planning on its movement during the extrusion. ANCHORAGE CONSIDERATIONS

Basic orthodontic mechanical considerations must be followed for tooth extrusion. Sufficient anchorage must be established to control the rate and direction of the extrusion, without adverse compensatory movement of the teeth used as anchors. This can require using 3 or more teeth mesial and distal to the tooth to be extruded and might require full arch brackets.34 During the extrusion, the clinician must examine the positions of the anchor teeth, noting any angulation, intrusion, or flaring. If this occurs, the anchorage used was not sufficient and should be reinforced.

ORTHODONTIC TOOTH EXTRUSION AND IMPLANT ESTHETICS

FIGURE 3. A, Initial presentation of a patient with severe bone loss on the left central and left lateral incisors. Current crowns were long, with incisal edges against lower lip. At full smile, she showed ideal gingival margin position on her right central incisor, with gingival margin on her left central incisor apical to ideal location. B, Frontal view showing excessive incisal position of left central with facial gingival margin apical to adjacent tooth. Facial gingival margin on right central incisor was at ideal position. C, Periapical radiograph showing bone loss present on left central incisor and explaining apical position of facial gingival margin. D, Diagnostic wax-up created to establish proper incisal edge position, contour, teeth proportions, and gingival margin. E, Crowns removed and temporary build-ups created to receive diagnostic provisional restoration made from diagnostic wax-up. F, Provisional restoration delivered with incisal edge of teeth at proper vertical position. Note the apical position of facial gingival margin on left central and lateral incisors. G, Brackets positioned on middle third of anchorage teeth and as close as possible to cervical third on teeth to be extruded. Note the slight bend in the wire that will extrude the teeth. (Figure 3 continued on next page.)

BRACKET POSITION

The brackets should be positioned on the anchorage teeth to keep these teeth in their original position and aligned. The tooth that requires extrusion should have the bracket placed as close as possible to the

gingival margin. It is necessary to have an adequate surface and the appropriate bonding techniques to bond the bracket. If an existing crown does not have the right references and proportions, it should be replaced with a provisional crown before the forced

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FIGURE 3 (contâ&#x20AC;&#x2122;d). H, A 1-mm incisal reduction made to allow clearance during orthodontic extrusion. I, Gingival recession corrected after 2 months of extrusion. J, Defect then overcorrected, anticipating facial gingival margin movement apically after implant and crowns placed. K, Periapical radiograph after orthodontic extrusion stabilized for 3 months. L, Maxillary left central extracted and implant immediately placed. After 2 months, left lateral extracted and implant delivered. Photograph shows both implants with temporary abutments in place after 4 months of stabilization with provisional prosthesis. M, Frontal view of smile with new set of temporaries in place, after orthodontic extrusion completed. This set of temporaries stabilized erupted teeth, as well as function as immediate provisional restoration after implant placement. N, Temporary abutments modified by placing subgingival resin to simulate tooth-like sulcus anatomy and further develop interdental papilla, enhancing gingival architecture. O, Revised temporary abutments placed in mouth to develop subgingival sulcus anatomy similar to that of natural tooth. P, Final soft tissue architecture obtained after 2 months. (Figure 3 continued on next page.)

ORTHODONTIC TOOTH EXTRUSION AND IMPLANT ESTHETICS

FIGURE 3 (cont’d). Q, Final abutments designed in wax and CAD/CAM zirconium abutments fabricated. R, After the tissue matured, the teeth were prepared. S, Zirconium crowns (Katana, Noritake, Japan) cemented. Proper symmetry established with clinically acceptable esthetic result and acceptable presence of interimplant papilla. T, Close-up of smile. Improvement of dentilabial relation obtained. Brindis and Block. Orthodontic Tooth Extrusion and Implant Esthetics. J Oral Maxillofac Surg 2009.

eruption. In a case that requires extrusion exceeding 5 mm, the clinician should plan on replacing the brackets during the extrusion period to aid in careful control of the extrusion rate. Metal or ceramic brackets can be used. The disadvantage of metal is its appearance. The disadvantage of ceramic brackets is the brittle nature of the ceramic and the cost. The brackets used for orthodontic extrusion are those made for the straight wire technique.31 We use ceramic prescription brackets (MBT Prescription, Clarity Brackets; 3M Unitek, St Paul, MN). This bracket has a metal slot, which allows control of the slide of the wire. The wire type is a round, heat-activated, superelastic nickel-titanium wire. This type of wire retains its memory to straighten. When connected to the bracket on the tooth to be extruded, the memory of the wire works to extrude the tooth. To provide slow and controlled movement, a 0.014- or 0.016-size wire should be used.16,31 To place the bracket, the tooth surface needs to be prepared. A fifth generation bonding agent should be used after applying 37% phosphoric acid for 20 seconds. The bonding agent is applied and allowed to dry for 5 seconds, a second layer is applied and allowed to dry for another 5 seconds, and then it is light cured for 15 seconds. A light-cured composite is used and light cured for 20 seconds on the bracket. The wire is measured according to the size of the arch and resized. The ends of the wire are bent to-

ward the tooth surface to avoid mucosa trauma. The wire is positioned into the bracket slot and secured with rubber bands. This allows the wire to move freely, limiting movement of the adjacent anchorage teeth. CLINICAL CONSIDERATIONS

The use of the nickel-titanium wire will allow constant movement of the tooth at a rate inversely related to the tooth’s attachment to the bone. The variables that provide the clinician with insight on how the tooth will move include the amount of tooth attachment to bone, the root length, patient age, and periodontal health of the tooth being extruded. Because each patient will respond in a unique pattern, we suggest examining the patient the day after activation of the orthodontic extrusion to reevaluate the patient’s response to the extrusive movement. Very close follow-up is necessary to prevent an unusual rate of tooth movement and premature contacts that might create a buccal tipping action. The rate of tooth eruption will vary from one patient to another. If fast movement is noted, the force must be stopped and the tooth allowed to stay in the extruded position for a period of healing as determined by clinical intuition and experience. Then, after the attachment fibers are recovered, the extrusion can be continued and should be closely monitored. This will prevent los-

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ing the sulcular attachments that ultimately determine the movement of the facial gingival margin. As the tooth erupts and is observed during the follow-up appointments, the clinician might need to continuously create space incisally and lingually to preserve a vertical eruptive force. Immediately after forced eruption, the crestal fibers remain stretched. Stabilization will allow the formation of crestal bone in most, but not all, cases (Fig 3K). Depending on the specific needs of the patient, the soft tissue deficit should be overcorrected by 2 to 3 mm from the planned final, ideal position of the facial gingival margin (Figs 3I,J). Once the tissue has overcorrected, a period of up to 12 weeks of stabilization is recommended, depending on the amount of eruption obtained and the speed of the tooth extrusion. IMPLANT PLACEMENT AFTER TOOTH EXTRUSION

Before removing the tooth for implant placement, an assessment of the bone levels must be performed. The labial bone might be missing and will need to be reconstructed before implant placement. At tooth removal, an intrasocket graft can be placed, with implant placement occurring 4 months after tooth removal. A pontic can be placed to support the papilla during the healing period before implant placement. If the bone is satisfactory at tooth removal, it is advantageous to place the implant at tooth removal.41 Before the surgical procedure, a guide stent is useful to allow the surgeon to accurately place the implant at the correct angulation and depth. This can be done with cone-beam computed tomography planning or model-based planning. The depth of implant placement is determined from the planned final position of the gingival margin, which should take into account the overcorrection of the facial gingival margin after tooth extrusion. After administration of local anesthesia, a sulcular incision is made and the tooth removed using atraumatic techniques. To support the soft tissues of the facial gingival margin, immediate provisionalization (Figs 3L,M) is recommended to provide the optimal gingival architecture.51 The provisional is fabricated in the laboratory to reduce the â&#x20AC;&#x153;chairâ&#x20AC;? time, using the diagnostic wax-up with the established incisal edge position. At surgery, the implant is placed and a provisional abutment secured to the implant with a screw. The provisional is then relined and cemented or screw retained. If placement of adjacent implants is planned, an alternative immediate implant placement and provisionalization method can be used.52 One tooth is removed, and the implant is placed and provisionalized. This method preserves the blood supply to the adjacent interdental bone. After 2 months, the adjacent second tooth is removed and the second implant

placed and provisionalized. This alternative method allows for preservation and development of the interdental papilla. After 4 months of healing, the temporary abutments are modified to create anatomically correct subgingival soft tissue architecture (Figs 3N-P). The provisional is relined to match the abutment modifications. A final customized impression is made when the soft tissue form has been developed to the satisfaction of the restorative clinician and patient. The final abutments are fabricated (Fig 3Q), a new set of temporaries delivered, and an esthetic analysis performed again. Once the soft tissue is stable, a final abutment level impression is made. The final crowns are then delivered (Figs 3R-T).

Discussion The benefits of forced eruption before tooth extraction of hopeless teeth are well documented. It is key in any esthetic situation to be predictable and consistent. When considering the orthodontic movement of a tooth to enhance the esthetic appearance of the final restoration, the initial evaluation of the patient should include the following: 1. An esthetic analysis of the teeth in relation to the patientâ&#x20AC;&#x2122;s face and lips. 2. Establishment of the incisal edge position, considering the vertical position and length, the horizontal location of the incisor edge, and the angulation of the tooth. 3. A thorough evaluation of the periodontal status of the teeth, including the tooth to be extruded and the anchorage teeth. 4. Proper mounting and an accepted esthetic wax-up to establish the proper tooth proportion. 5. Establishment of the ideal gingival margin position for the proposed restoration. 6. Fabrication of an appropriate provisionalization using the diagnostic cast and previous wax-up. 7. Planning for an overcorrection of 2 to 3 mm from the programmed final gingival margin position. In the data reviewed for the present report, no well-documented evidence was available for the specifics of orthodontic extrusion. Rather, a generally accepted consensus of the techniques have been decided on the basis of personal experience. No standard clinical protocol has been described for forced eruption before implant placement. However, as a general consensus, when an attachment apparatus exists, with apical bone apposition to the tooth and sulcular attachment fibers intact, the keratinized soft

ORTHODONTIC TOOTH EXTRUSION AND IMPLANT ESTHETICS

tissue is improved, and crestal bone formation can occur. If crestal bone formation is not generated, the movement of the gingival margin will allow for successful bone graft reconstruction before implant placement. Our experience has indicated that the period required for tooth extrusion is dependent on the tooth– bone attachment of the tooth to be extruded. A tooth with dense bone surrounding it will require more time to extrude than will a tooth with minimal remaining bone, which can be extruded within a few days. Close clinical observation is critical to properly extrude the tooth within an appropriate period. Because the disadvantages are minimal to extruding a tooth to enhance the soft tissue profile, clinicians should choose this method often. When a tooth has its facial margin at a level that will result in compromised esthetics, the alternatives to orthodontic extrusion include surgical movement of the tooth with its surrounding bone. Orthodontic extrusion is a lessmorbid procedure than osteotomy. We suggest that, on the basis of our review of the published data, which showed minimal disadvantages to the technique, one should consider this type of procedure in every case in which a tooth needs to be extracted. Each case must be approached individually, depending on the needs of the patient and the status of the teeth. We recommend monitoring each step several times each week to carefully evaluate the tooth movement and the patient’s response. The rate of tooth movement will be patient-specific. The period needed for tooth stabilization will also be patient specific. After the tooth has been erupted to the prescribed level, it should be stabilized with a provisional restoration or orthodontic wires until the bone response has matured. Movement of the facial gingiva is critical for the final esthetic result. If the tooth is removed without extrusion and re-establishment of the position of the facial gingival margin, the final result will be catastrophic for the patient, with a high smile. The need for orthodontic extrusion should be planned by the restorative member of the team. It is very important to keep in mind the importance of planning before attempting to extract any tooth. That could be the difference between achieving a perfect final result or a catastrophe. Once the tooth has been removed, the ability to use nature’s capacity to grow soft tissue and bone through tooth eruption is gone. In our clinical experience, we have found that it is not always possible to build up bone, especially the buccal plate, because of the thin nature of the cortical tissue. However, the soft tissue formed is absolutely critical for the success of a preparation implant sight with bone grafting. The keratinized gingiva around the extruded tooth will have been maintained and, in

occasional cases, widened during the extrusion. The improved soft tissue matrix has allowed hard tissue grafting to achieve a ridge width sufficient for implant placement. Orthodontic extrusion is a predictable and resourceful method to move the facial gingival margin to a position that can result in an esthetic restoration. We encourage the use of this method when indicated because of the ease of the method and its exceptional results. Acknowledgment The authors thank Ms Kathy Martello for the artwork in Figure 2.

References 1. Small PN, Tarnow DP: Gingival recession around implants: A 1-year longitudinal prospective study. Int J Oral Maxillofac Implants 15:527, 2000 2. Block MS, Mercante D, Lirette D, et al: Prospective evaluation of immediate and delayed provisional single tooth restorations. J Oral Maxillofac Surg 67:89, 2009 (suppl 3) 3. Saadoun AP, LeGall M, Touati B: Selection and ideal tridimensional implant position of soft tissue aesthetics. Pract Periodontics Aesthet Dent 11:1063, 1999 4. Kois JC: Esthetic extraction site development: The biologic variables. Contemp Esthet Restorative Pract 2:10, 1998 5. Holst S, Blatz M, Hegenbarth E: Prosthodontic considerations for predictable single-implant esthetics in the anterior maxilla. J Oral Maxillofac Surg 63:89, 2005 (suppl 2) 6. Salama H, Salama M: The role of orthodontic extrusive remodeling in the enhancement of soft and hard tissue profiles prior to implant placement: A systematic approach to the management of extraction site defects. Int J Periodontics Restorative Dent 13:312, 1993 7. Kokich VG: Esthetics: The orthodontic-periodontic restorative connection. Semin OrthoOrthod 2:21, 1996 8. Mantzikos T, Shamus I: Forced eruption and implant site development: Soft tissue response. Am J Orthod Dentofac Orthop 112:596, 1997 9. Ingber JS: Forced eruption: Alteration of soft tissue deformities. Int J Periodontics Restorative Dent 9:416, 1989 10. Oppenheim A: Artificial elongation of teeth. Am J Orthod Oral Surg 26:931, 1940 11. Brown S: The effect of orthodontic therapy on certain types of periodontal defects. I—Clinical findings. J Periodontol 44:742, 1973 12. Ingber JS: Forced eruption: Part I. A method of treating isolated one and two wall infrabony osseous defects—Rationale and case report. J Periodontal 45:199, 1974 13. Ingber IS: Forced eruption. Part II. A method of treating nonrestorable teeth—Periodontal and restorative considerations. J Periodontol 47:203, 1976 14. Heithersay GS: Combined enodontic-orthodontic treatment of transverse root fractures in the region of the alveolar crest. Oral Surg Oral Med Oral Pathol 36:404, 1973 15. Chambrone L, Chambrone LA: Forced orthodontic eruption of fractured teeth before implant placement: Case report. J Can Dent Assoc 71:257, 2005 16. Stern N, Becker A: Forced eruption: Biological and clinical considerations. J Oral Rehabil 7:395, 1980 17. Potashnick SR, Rosenberg ES: Forced eruption: Principles in periodontics and restorative dentistry. J Prosthet Dent 48:141, 1982 18. Wingard BS, Browers GM: The effects on facial bone from facial tipping of incisors in monkeys. J Periodontol 47:450, 1976 19. Reitan K: Clinical and histologic observations on tooth movement during and after orthodontic treatment. Am J Orthod 53:721, 1967

BRINDIS AND BLOCK 20. Pontoriero R, Celenza F, Ricci G, et al: Rapid extrusion with fiber resection: A combined orthodontic-periodontic treatment modality. Int J Periodontics Restorative Dent 5:31, 1987 21. Ritchey B, Orban B: The crests of the interdental alveolar septa. J Periodontol 24:75, 1953 22. Batenhorst KF, Browers GM, Williams JE: Tissue changes resulting from facial tipping and extrusion of incisors in monkeys. J Periodontol 45:660, 1974 23. Reitan K: Some factors determining the evaluation of forces in orthodontics. Am J Orthod 43:32, 1957 24. Kokich VG: Surgical and orthodontic management of impacted maxillary canines. Am J Orthod Dentofac Orthop 126:278, 2004 25. Kokick VG: Maxillary lateral incisor implants: Planning with the aid of orthodontics. J Oral Maxillofac Surg 62:48, 2004 (suppl 2) 26. Tarnow DP, Magner AW, Fletcher P: The effect of the distance from the contact point to the crest of bone on presence or absence of the interproximal dental papilla. J Periodontol 71: 546, 2000 27. Salama H, Salama MA, Garber D, et al: The interproximal height of bone: A guidepost to predictable aesthetic strategies and soft tissue contours in anterior tooth replacement. Pract Periodontics Aesthet Dent 10:1131, 1998 28. Tarnow DP, Cho SC, Wallace SS: The effect of interimplant distance on the height of inter-implant bone crest. J Periodontol 71:546, 2000 29. Ryser MR, Block MS, Mercante DE: Correlation of papilla to crestal bone levels around single tooth implants in immediate or delayed crown protocols. J Oral Maxillofac Surg 63:1184, 2005 30. Lin CD, Chang SS, Liou CS, et al: Management of interdental papillae loss with forced eruption, immediate implantation and root-form pontic. J Periodontol 77:135, 2006 31. Tal M: Improving soft tissue form around implants via forced eruption. Quintessence Dent Technol 28:112, 2005 32. Mantzikos T, Shamus I: Forced eruption and implant site development: An osteophysiologic response. Am J Orthod Dentofac Orthop 115:583, 1999 33. Mantzikos T, Shamus I: Case report: Forced eruption and implant site development. Angle Orthod 68:179, 1998 34. Ziskind D, Schmidt A: Forced eruption technique: Rationale and clinical report. J Prosthet Dent 79:246, 1998 35. Erkut S, Arman A, Gulsahi A, et al: Forced eruption and implant treatment in posterior maxilla: A clinical report. J Prosthet Dent 97:70, 2007

59 36. Danesh-Meyer MJ, Brice DM: Implant site development using orthodontic extrusion: A case report. N Z Dent J 96:18, 2000 37. Chambrone L, Chambrone LA: Force eruption of fracture teeth before implant placement: Case report. J Can Dent Assoc 71:257, 2005 38. Holst S, Hegenbarth EA, Schlegel KA, et al: Restoration of a nonrestorable central incisor using forced orthodontic eruption immediate implant placement, and an all-ceramic restoration: A clinical report. J Prosthet Dent 98:251, 2007 39. Nozawa T, Sugiyama T, Yamaguchi S, et al: Buccal and coronal bone augmentation using forced eruption and buccal root toque: A case report. Int J Periodontics Restorative Dent 23: 568, 2003 40. Celenza F: The development of forced eruption as a modality for implant site enhancement. Alpha Omegan 90:40, 1997 41. Lazzara RJ: Immediate placement of implants into extraction sites. Oral Maxillofac Surg Clin North Am 3:921, 1991 42. Barzilay I, Gaser GN, Caton J, et al: Immediate implantation of pure titanium threaded implants into extraction socket. J Dent Res 67:234, 1988 43. Saadoun AP, LeGall M, Touati B: Selection and ideal tridimensional implant position for soft tissue aesthetics. Pract Periodontics Aesthet Dent 11:1063, 1999 44. Proffit WR: Contemporary Orthodontics (ed 4). St. Louis: CV Mosby, 2006 45. Burstone CJ, Groves MH: Threshold and optimum force values for maxillary anterior tooth movement. J Dent Res 39:695, 1961 46. Buskin R, Castellon P, Hochstedler JL: Orthodontic extrusion and orthodontic extraction in preprosthetic treatment using implant therapy. Pract Periodontics Aesthet Dent 12:213, 2000 47. Chiche GJ, Pinault A: Esthetics of Anterior Fixed Prosthodontics. Chicago: Quintessence, 1994, pp 13-32 48. Cohen M (ed): Interdisciplinary Treatment Planning, Principles, Design, Implementation. Chicago: Quintessence, 2008 49. Vig RG, Brundo GC: The kinetics of anterior tooth display. J Prosthet Dent 39:502, 1978 50. Kois JC, Kan JY: Predictable peri-implant gingival aesthetics: Surgical and prosthodontic rationales. Pract Proced Aesthet Dent 13:691, 2001 51. Saadoun AP: Immediate implant placement and temporization in extraction and healing sites. Compend Contin Educ Dent 23:309, 2002 52. Kan JY, Rungcharassaeng K: Interimplant papilla preservation in the esthetic zone: A report of six consecutive cases. Int J Periodontics Restorative Dent 23:249, 2003

INFLAMMATORY PERI-IMPLANT DISEASE Dr. Paul Fletcher

CASE REPORT Resolution of a Peri-Implantitis Defect Using Sterile Saline for Implant Surface Detoxification: A Case Report With Clinical Re-Entry Paul Fletcher*† and Christos Constantinides*

Introduction: Peri-implantitis is an inflammatory disease involving the soft and hard tissues surrounding a dental implant. Its prevalence is increasing, and, if left untreated, it can lead to the loss of the implant. Decontamination of the implant surface is a primary prerequisite to successfully treat this disease. The best way to accomplish this is still a source of controversy. To the best of the authors’ knowledge, this is the first report of a clinical re-entry in a human showing almost complete osseous fill of a deep circumferential infrabony peri-implantitis lesion after mechanical debridement with a curet and chemotherapeutic detoxification with only sterile saline. Case Presentation: A patient presenting with an infrabony peri-implantitis lesion was treated with mechanical debridement with a curet and chemotherapeutic detoxification of the implant surface with sterile saline, followed by osseous grafting and guided bone regeneration in an effort to eliminate the defect. At the completion of treatment, after clinical reentry, there was almost complete fill of the infrabony component of the osseous defect with a bone-like material that closely approximated the implant surface. Conclusion: It is possible to effectively clean a dental implant surface using only mechanical debridement with a curet and chemotherapeutic detoxification with sterile saline on a cotton pellet to an extent that will allow for fill of the infrabony component of an osseous defect after the use of regenerative therapy. Clin Adv Periodontics 2015;5:235-241. Key Words: Bone regeneration; bone transplantation; decontamination; dental implants; peri-implantitis.

Background Zitzmann and Berglundh defined peri-implantitis as an inflammation of the peri-implant tissues along with breakdown of the alveolar bone. Initially, it was believed that the peri-implantitis lesion was similar to periodontitis,2 but histopathologic studies showed distinct differences. Specifically, in periodontitis, there is a “self-limiting” response to the progression of 1

* Division of Periodontics, Columbia University College of Dental Medicine, New York, NY. †

Private practice, New York, NY.

Submitted March 23, 2014; accepted for publication May 11, 2014 doi: 10.1902/cap.2014.140020

the inflammation, evidenced by the presence of a connective tissue (CT) capsule separating the inflammatory cell infiltrate from the bone.3 This capsule is absent in periimplantitis, allowing the inflammatory infiltrate to become more widespread and penetrate further apically.4 Much of the research on the treatment of peri-implantitis is relatively short term, consisting of follow-ups of £3 years.5 Additionally, there are variations between studies, including disagreement as to the threshold of bone loss used in defining the disease, differences in surface texture of the implants, and variations in the configuration of the osseous defects.1 Adequate decontamination of an implant surface is of primary importance in obtaining resolution of a peri-implantitis defect. Multiple decontamination protocols were presented in the literature.6-11 Persson et al.6 in an animal study showed Clinical Advances in Periodontics, Vol. 5, No. 4, November 2015

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FIGURE 3 Two weeks after emergency therapy, the acute inflammation was resolved, but a 9-mm PD remained. Note the absence of attached gingiva and vestibular depth.

FIGURE 1 Tooth site #19 at initial presentation. 1a Buccal aspect. 1b Lingual aspect.

disease process for 3 years in humans when grafting with bone substitute in combination with a resorbable collagen membrane. More recently, a protocol for treating peri-implantitis consisting of 12 steps, including the use of enamel matrix derivative, platelet-derived growth factor, xenograft or allograft, and a CT graft or a resorbable membrane, showed success up to 7 years.9 In this case report, a regenerative approach is used, using only sterile saline for chemotherapeutic implant surface decontamination, and the surgical site was subsequently reentered for evaluation.

Clinical Presentation A 63-year-old Hispanic female presented at the Department of Periodontology of Columbia University (New York, New York) for emergency treatment in May 2012. Her chief complaint was a dull aching pain and purulence associated with an implant in tooth site #19. Three moderately rough surface external hex implants‡ were placed at Columbia University 5 years previously, and they now supported a cemented splintx from teeth #18 through #20. Clinically, a lack of attached keratinized tissue (KT), circumferential swelling, erythema, and purulence were visible (Fig. 1). Radiographically, there was an infrabony defect around tooth site #19 (Fig. 2), and it appeared as if the bridge was not fully seated on the abutments.

Case Management Emergency Treatment FIGURE 2 Preoperative radiograph showing an infrabony peri-implant defect around the implant at tooth site #19. The restorative suprastructure appears not to be fully seated on the abutments.

no difference in detoxifying an implant surface with a carbon dioxide laser and hydrogen peroxide, or sterile saline on a cotton pellet. Alhag et al.7 demonstrated in dogs that reintegration could occur after cleaning an implant surface with sterile saline, although some residual bacteria remained, and Roos-Jansa˚ker et al.8 was able to arrest the progression of the 236

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Written and oral informed consent were obtained for treatment. Under local anesthesia, titanium curets were used to debride the implant surface and the soft tissue around tooth site #19. Amoxicillin (500 mg, three times daily) was prescribed for 10 days, and the patient was instructed to rinse the surgical site twice daily with a mild saltwater solution, to brush gently with a soft-bristle brush beginning 72 hours after treatment, and to begin using an interproximal brush 2 weeks after the procedure. ‡ x

TiUnite, Nobel Biocare, Zurich, Switzerland. IMPROV temporary cement, Alvelogro, Snoqualmie, WA.

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FIGURE 5a Calcium sulfate was placed in the defect. 5b A porcine collagen barrier membrane was placed buccally and lingually.

FIGURE 4 The configuration of the residual defect was amenable to grafting. A regenerative approach was used. 4a Buccal aspect. 4b Lingual aspect.

Surgical Procedure Two weeks after the emergency treatment, the swelling was reduced, and purulence was no longer evident. Because there was still a 9-mm probing depth (PD), an incompletely

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seated bridge (Fig. 3), and radiographic bone loss, it was decided to treat the area surgically in an attempt to mitigate the effect of the subgingival open margin while simultaneously resolving the pocketing and infrabony defect. After an unsuccessful attempt to remove the crowns, buccal and lingual sulcular incisions were placed from teeth #18 through #20, and full-thickness flaps were elevated. Titanium curets were used for soft tissue degranulation and to mechanically debride the implant surface, and copious irrigation with sterile saline from a monojet syringe was used to dilute the microbial concentration in the defect and on the implant to a subinflammatory level. The implant threads and collar were then meticulously burnished with sterile saline on a small cotton pellet for additional detoxification. After degranulation, a circumferential infrabony defect was visible (Fig. 4). Because of the configuration of the defect,12 it was decided to use a regenerative approach to treat it. A microparticle size calcium sulfate (crystal range: 200 to 900 nm)|| was used as a grafting material (Fig. 5a). A porcine-derived collagen extracellular membrane{ was used as an occlusive barrier and was placed buccally and || {

NanoGen, Orthogen, Springfield, NJ. DynaMatrix, Keystone Dental, Burlington, MA.

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FIGURE 6a Flap closure with 4-0 interrupted sutures. 6b Immediate postoperative radiograph.

lingually (Fig. 5b). Because it was the patient’s preference not to replace the fixed splint, the flap was consequently positioned apical to the crown margin to eliminate the contribution of the margin to the inflammatory process. Closure was achieved with 4-0 polyglactin interrupted sutures# (Fig. 6a). Amoxicillin (500 mg) and metronidazole (500 mg) were prescribed three times daily for 10 days. The patient was advised not to brush the surgical site for 2 weeks and to rinse with 0.12% chlorhexidine for 30 seconds twice daily. Figure 6b shows an immediate postoperative radiograph of the grafted site.

Clinical Outcomes The patient was seen 2 and 4 weeks after surgery and at subsequent monthly follow-up appointments. Maintenance was performed every 3 months. Her home care was excellent, because there was no evidence of plaque around the implant at all post-treatment visits. 238

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FIGURE 7a Twelve-month follow-up showing 3-mm PD on the buccal aspect but lack of attached KT and vestibular depth. 7b Less than 3-mm PD on the lingual aspect.

Clinically, the crown margins were supragingival; there were 3-mm PDs, and there was no bleeding on probing (Fig. 7). A 12-month postoperative radiograph showed what appeared to be a radiopaque fill of the infrabony component of the lesion (Fig. 8). At 12 months after surgery, the patient began to complain of soft tissue soreness on the buccal aspect. The gingiva had receded 2 mm, and the sulcular margin was slightly retractable because of the pull of the shallow vestibule. Because there was a lack of attached KT, it was decided to deepen the vestibule using an apically positioned split-thickness flap and to augment the attached gingiva with a free gingival graft, while simultaneously clinically evaluating the results of the previous surgery. After receiving the patient’s informed consent and after the administration of local anesthetic, a buccal sulcular incision with a mesial vertical release was placed. A split-thickness #

Coated VICRYL, Ethicon, Johnson & Johnson, Somerville, NJ.

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FIGURE 8 Twelve-month postoperative radiograph showing bone fill with homogeneous radiographic appearance.

flap was elevated, with the periosteum on the buccal aspect of tooth site #19 being reflected to allow for visualization of what appeared to be osseous fill of the infrabony component of the original defect (Fig. 9) with a bone-like material closely abutting the implant surface.

Discussion The research is clear that implant surface detoxification is of primary importance if there is to be any chance of arresting the progression of inflammatory peri-implantitis or of regenerating bone that was lost previously as a result of the disease.5 The best way to accomplish this is still a source of controversy. In this case, debridement plus thorough cleansing of the implant surface with sterile saline seems to have been effective in reducing the endotoxin and diluting the bacterial concentration to a subinflammatory level so that osseous fill occurred and reintegration was possibly achieved. Although histologic verification of osseous regeneration using this surface detoxification protocol was shown in

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FIGURE 9 Sulcular incision with a mesial vertical release and splitthickness flap. The periosteum was reflected adjacent to the implant, and close bone-to-implant contact was visible.

animals,6 without histology, the best that can be claimed in this human case report is radiographic and clinical evidence of bone fill, as well as the visible clinical presence of what appears to be close approximation of a bone-like material to the implant surface. Calcium sulfate was shown to promote bone formation in both animal and human studies.13-15 It undergoes controlled degradation over a period of 10 to 12 weeks, is angiogenic, and leads to the formation of calcium phosphate, which is the main inorganic component of bone. This subsequently serves as a matrix for additional bone deposition. After re-entering this surgical site, a bone-like material was visible closely abutting the surface of the implant. It is hoped the results obtained using this protocol will stimulate additional research in finding a predictable, costeffective means of decontaminating a peri-implantitisâ&#x20AC;&#x201C; affected implant surface that would ultimately lead to the reintegration of bone around an implant. n

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Summary Why is this case new information?

What are the keys to successful management of this case?

j j j

What are the primary limitations to success in this case?

To the best of the authors’ knowledge, this is the first published human case report with re-entry clinically showing: ☐ Almost complete osseous fill of the infrabony component of a deep circumferential peri-implantitis lesion ☐ Apparent close bone-to-implant approximation after mechanical debridement and chemotherapeutic surface detoxification with only sterile saline Detoxification of the implant surface using mechanical and chemotherapeutic methods Stability of the graft and membrane Exclusion of the epithelium Meticulous oral hygiene Susceptibility of any exposed threads to plaque accumulation and difficulty for the patient to keep them clean Need for patient compliance

Acknowledgment The authors report no conflicts of interest related to this case report.

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CORRESPONDENCE: Dr. Paul Fletcher, Specialized Dentistry of New York, 150 E. 58th St., Suite 3200, New York, NY 10155. E-mail: pfletcher@sdnyonline.com.

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References

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1. Zitzmann NU, Berglundh T. Definition and prevalence of peri-implant diseases. J Clin Periodontol 2008;35(Suppl. 8):286-291.

9. Froum SJ, Froum SH, Rosen PS. Successful management of periimplantitis with a regenerative approach: A consecutive series of 51 treated implants with 3- to 7.5-year follow-up. Int J Periodontics Restorative Dent 2012;32:11-20.

2. Mombelli A, van Oosten MA, SchuÂ¨rch E Jr, Land NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 1987;2:145-151.

10. Subramani K, Wismeijer D. Decontamination of titanium implant surface and re-osseointegration to treat peri-implantitis: A literature review. Int J Oral Maxillofac Implants 2012;27:1043-1054.

3. Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C. Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants Res 1992;3:9-16.

11. Schwarz F, John G, Mainusch S, Sahm N, Becker J. Combined surgical therapy of peri-implantitis evaluating two methods of surface debridement and decontamination. A two-year clinical follow up report. J Clin Periodontol 2012;39:789-797.

4. Berglundh T, Zitzmann NU, Donati M. Are peri-implantitis lesions different from periodontitis lesions? J Clin Periodontol 2011;38(Suppl. 11):188-202. 5. Esposito M, Grusovin MG, Worthington HV. Treatment of periimplantitis: What interventions are effective? A Cochrane systematic review. Eur J Oral Implantology 2012;5(Suppl.):S21-S41.

12. Schwarz F, Sahm N, Schwarz K, Becker J. Impact of defect configuration on the clinical outcome following surgical regenerative therapy of peri-implantitis. J Clin Periodontol 2010;37:449455.

6. Persson LG, Mouhyi J, Berglundh T, Sennerby L, Lindhe J. Carbon dioxide laser and hydrogen peroxide conditioning in the treatment of peri-implantitis: An experimental study in the dog. Clin Implant Dent Relat Res 2004;6:230-238.

13. Paolantonio M, Perinetti G, Dolci M, et al. Surgical treatment of periodontal intrabony defects with calcium sulfate implant and barrier versus collagen barrier or open flap debridement alone: A 12month randomized controlled clinical trial. J Periodontol 2008;79: 1886-1893.

7. Alhag M, Renvert S, Polyzois I, Claffey N. Re-osseointegration on rough implant surfaces previously coated with bacterial biofilm: An experimental study in the dog. Clin Oral Implants Res 2008;19:182-187.

14. Pecora G, Andreana S, Margarone JE 3rd, Covani U, Sottosanti JS. Bone regeneration with a calcium sulfate barrier. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84:424-429.

8. Roos-JansaË&#x161;ker AM, Lindahl C, Persson GR, Renvert S. Long-term stability of surgical bone regenerative procedures of peri-implantitis lesions in a prospective case-control study over 3 years. J Clin Periodontol 2011;38:590-597.

15. Mazor Z, Mamidwar S, Ricci JL, Tovar NM. Bone repair in periodontal defect using a composite of allograft and calcium sulfate (DentoGen) and a calcium sulfate barrier. J Oral Implantol 2011;37: 287-292.

indicates key references.

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SOFT TISSUE MANAGEMENT OF AESTHETIC FAILURE Prof. Giovanni Zucchelli

J Clin Periodontol 2007; 34: 262â&#x20AC;&#x201C;268 doi: 10.1111/j.1600-051X.2006.01039.x

Coronally advanced flap: a modified surgical approach for isolated recession-type defects

M. de Sanctis1 and G. Zucchelli2 1

Departement of Periodontology, Siena University, Siena, Italy; 2Department of Stomatology, Bologna University, Bologna, Italy

Three-year results de Sanctis M, Zucchelli G. Coronally advanced flap: a modified surgical approach for isolated recession type defects. Three-year results. J Clin Periodontol 2007; 34: 262â&#x20AC;&#x201C;268. doi: 10.1111/j.1600-051X.2006.01039.x. Abstract Background: Various modifications of the coronally displaced flap have been proposed in the literature with the attempt of treating gingival recession with uneven predictable results. The goal of the present study was to evaluate the effectiveness with respect to root coverage of a modification of the coronally advanced flap procedure for the treatment of isolated recession-type defects in the upper jaw. Methods: Forty isolated gingival recessions with at least 1 mm of keratinized tissue apical to the defects were treated with a modified approach to the coronally advanced flap. The main change in the surgical procedure consisted in the modification of flap thickness and dimension of surgical papillae during flap elevation. All recessions fall into Miller class I or II. The clinical re-evaluation was performed 1 year and 3 years after the surgery. Results: At the 1-year examination, the average root coverage was 3.72 1.0 mm (98.6% of the pre-operative recession depth) and 3.64 1.1 mm (96.7%) at 3 years. The gain in probing attachment amounted to 3.65 1.10 mm at 1 year and to 3.70 1.09 mm at 3 years. The average increase of keratinized tissue between the baseline and the 3-year follow-up amounted to 1.78 0.90 mm. All changes of keratinized tissue (difference between baseline and 1 year, baseline and 3 years, and between 1 and 3 years) were statistically significant. Conclusion: The modified coronally advanced surgical technique is effective in the treatment of isolated gingival recession in the upper jaw.

It has been assessed that gingival recession can be successfully treated irrespective of the technique utilized, provided that the biologic conditions for accomplishing root coverage are satisfied: no loss of inter-dental soft and hard tissue height (Miller 1985). Conflict of interest and source of funding statement

The authors declare that they have no conflict of interest. The study was self-funded by the authors and their institution.

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The selection of the surgical technique in an attempt to cover a root recession depends mainly on the local anatomical characteristics and on the patientâ&#x20AC;&#x2122;s demands. Local characteristics to be evaluated are as follows: the dimensions (depth and width) of root exposure, the height and width of the inter-dental soft tissue, the number of recession defects on neighbouring teeth, the presence of root caries or cervical abrasions. Also, the height, thickness and colour of the keratinized tissues apical and lateral to the root exposure and of the inter-dental papillae neighbouring the recession must

Key words: aesthetics; gingival recession; root coverage; surgery Accepted for publication 31 October 2006

be considered. Other soft-tissue characteristics to be evaluated in the selection of the surgical procedure are the depth of the vestibulum and the presence of marginal frenuli or muscle insertions (de Sanctis & Zucchelli 1996). In patients with a residual amount of keratinized tissue apical to the recession defect, the coronal advanced flap may be recommended. Optimum root coverage results, good colour blending of the treated area with respect to adjacent soft tissues and complete recovery of the original (pre-surgical) soft tissue marginal morphology can be predictably accom-

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Coronally advanced flap plished by means of this surgical approach (Roccuzzo et al. 2002). Furthermore, the post-operative course is less troublesome for the patient as other surgical sites distant from the tooth with recession defect are not involved. Recently, the coronally advanced flap has been demonstrated to be very effective in the treatment of multiple recession defects affecting adjacent teeth with obvious advantages for the patient in terms of aesthetics and morbidity (Zucchelli & de Sanctis 2000). The coronal advanced flap was first introduced by Norberg (1926) as an aesthetic surgical procedure for root coverage. In a 1958 study, Patur and Glickman reported that the coronal advancement of a pedicle flap was not an effective means of covering exposed root. Hall, in the 1989 Proceeding of the World Workshop in Clinical Periodontology, stated that: ‘‘these techniques never have achieved general acceptance and fail on a predictable basis; nevertheless, the goal of such a procedure elusive as it has been, remains the dream of periodontists’’. The coronally advanced flap as a root coverage surgical technique has been evaluated more recently by other authors with uncertain results or limited data (Tenenbaum et al. 1980, Allen & Miller 1989, Wennstrom & Zucchelli 1996). Surgical recommendation (Allen & Miller 1989) was to utilize such a technique only in the presence of Miller’s class I root recession defect and in the presence of residual keratinized tissue with the same height of the depth of the recession. This approach was thus limited to shallow recession depth, i.e. equal to or less than 3 mm. The technique as described by Allen & Miller (1989) consisted of two oblique incisions, starting from the mesial and distal line angle of the affected tooth and directed apically in the alveolar mucosa; the flap was then elevated with a split-thickness approach to protect the underlying bone. Following root debridement, the flap was then coronally advanced and secured with interrupted sutures. Zucchelli & de Sanctis (2000) have recently introduced a modification of this procedure to treat multiple recession defects. A split–full–split approach was used to elevate the flap; this permitted to maintain the maximum soft tissue thickness above the root exposure. Coronal mobilization of the flap was achieved by means of a superficial incision eliminating lip muscle insertion residing in the

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thickness of the flap. The results reported from this study indicated that 64 of the 73 defects treated for recession showed complete coverage (88%); on average, 97% of previously exposed root surface was covered with soft tissue. The aim of the present study was to evaluate the efficacy of a modified approach of the coronally advanced flap for treating single-type recession defects.

at a force of 0.3 N with a manual pressure-sensitive probe. Full-mouth bleeding score (FMBS) and local bleeding score was recorded as the percentage of total surfaces (four sides per tooth), that revealed the presence of bleeding upon probing. The following clinical measurements were taken 1 week before the surgery and at the 1- and 3-year follow-up visits at all treated teeth:

Material and Methods

Recession depth, measured from the cemento-enamel junction (CEJ) to the most apical extension of the gingival margin. Probing pocket depth (PPD), measured from the gingival margin to the bottom of the gingival sulcus. Clinical attachment level (CAL), measured from the CEJ to the bottom of the gingival sulcus. Keratinized tissue height (KTH) measured from the most apical extension of gingival margin to the mucogingival line.

Subject and site selection

Forty young subjects (age range 20–38 years), systemically and periodontally healthy with isolated recession-type defects in the upper jaw, were enrolled in the study. The participants were selected on a consecutive basis among patients consulting two private practices: one located in Florence and the other in Bologna. A screening examination revealed that all subjects showed an unremarkable medical history and none had loss of periodontal support at other tooth surfaces than those showing recession defects. In order to be included in the study, patients should have at least one recession defect with the following characteristics: (1) isolated defect (no recessions in the neighbouring teeth), (2) class I or II according to the definitions given by Miller (no loss of inter-dental soft and hard tissue height), and (3) recession depth (RD) equal to or greater than 2 mm. Following the screening examination, all subjects received a session of prophylaxis including instruction in proper oral hygiene measures, scaling and professional tooth cleaning with the use of a rubber cup and a low abrasive polishing paste. At teeth with recession-type defects, a coronally directed roll technique was prescribed, in order to minimize the tooth-brushing trauma to the gingival margin. Surgical treatment of the recession defects was not scheduled until the patient could demonstrate an adequate standard of supra-gingival plaque control. Clinical characterization of patients and selected sites

Full-mouth plaque score (FMPS) and local plaque score was recorded as the percentage of total surfaces (four sides per tooth) that revealed the presence of plaque (O’Leary et al. 1972). Bleeding on probing was assessed dichotomously

Surgeries and measurement were performed for all the locations by the same two operators. The same single investigator performed the clinical measurements at baseline, at 1 year and at 3 years. He did not perform the surgery and was unaware of the goals of the study. All measurements were performed by means of a manual probe and were rounded up to the nearest millimetre. Surgical technique

The design of the flap consisted of the following incisions: Two horizontal bevelled incisions (3 mm in length), mesial and distal to the recession defect located at a distance from the tip of the anatomical papillae equal to the depth of the recession plus 1 mm. Two bevelled oblique, slightly divergent, incisions starting at the end of the two horizontal incisions and extending to the alveolar mucosa. The resulting trapezoidal-shaped flap was elevated with a split–full–split approach in the coronal–apical direction: the surgical papillae comprised between the horizontal incisions and the probeable sulcular area apical to the root exposure were elevated split thickness keeping the blade almost

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parallel to the root, and the soft tissue apical to the root exposure was elevated full thickness inserting a small periostium elevator in to the probeable sulcus and proceeding in the apical direction up to exposing 3–4 mm of bone apical to the bone dehiscence. This was done in order to include the periostium in the thickness of that central portion of the flap covering the avascular root exposure. The releasing vertical incisions were elevated split thickness keeping the blade parallel to the bone plane, thus leaving the periostium to protect the underlying bone in the lateral areas of the flap. Apical to bone exposure flap elevation continued split thickness and finished when it was possible to move the flap passively in the coronal direction. In order to permit the coronal advancement of the flap, all muscle insertions present in the thickness of the flap were eliminated. This was done keeping the blade parallel to the external mucosal surface. Coronal mobilization of the flap was considered ‘‘adequate’’ when the marginal portion of the flap was able to passively reach a level coronal to the CEJ of the tooth with the recession defect. In fact, the flap should be stable in its final coronal position even without the sutures. The root surface was mechanically treated with the use of curettes. It must be considered that only the portion of the root exposure with loss of clinical attachment (gingival recession1probeable gingival sulcus/pocket) was instrumented. Exposed root surfaces belonging to the area of anatomic bone dehiscence were not instrumented not to damage connective tissue fibres still inserted in to the root cementum. The facial soft tissue of the anatomic inter-dental papillae coronal to the horizontal incisions was disepithelized to create connective tissue beds to which the surgical papillae of the coronally advanced flap were sutured. By moving the flap coronally to reach the tip of the disepitelized anatomical papillae, the vestibular soft tissue was positioned 1 mm coronal to the CEJ to account for soft tissue shrinkage. The location of gingival margin after suturing has been demonstrated to be positively correlated to recession reduction (Pini Prato et al. 2005) The suture of the flap started with two interrupted periosteal sutures performed at the most apical extension of the vertical releasing incisions; then, it proceeded coronally with other interrupted

Fig. 1. (a) Upper right first pre-molar, pre-surgical. (b) Flap design; two horizontal bevelled incisions, mesial and distal to the recession defect, two bevelled oblique incisions coming from the two horizontal, extending to the alveolar mucosa are executed. (c) The flap is raised with a split–full–split thickness approach. (d) The anatomical papillae are disepithelized. (e) The flap is coronally advanced and the vertical incisions are sutured. (f) The surgical papillae are secured to the underlying bed with a suspended suture.

sutures, each of them directed, from the flap to the adjacent buccal soft tissue, in the apical–coronal direction. This was done to facilitate the coronal displacement of the flap and to reduce the tension on the last coronal sling suture. The sling suture permitted to stabilize the surgical papillae over the inter-dental connective tissue bed and allowed for a precise adaptation of the flap margin over the underlying convexity of the crown (Fig. 1). In fact, in all treated cases, at the end of the surgery, the flap resided coronal to the cemento-enamel junction.

recalled for prophylaxis 1, 3 and 5 weeks after suture removal and, subsequently, once every 3 months until the 1-year examination. In the period comprised between the 1- and the 3-year examinations, patients undertook hygienic recall visits every 6 months.

Data analysis

Statistical analysis was performed using a statistical application software (Statgraphics 5 plus; Manugistic Inc., Rockville, MD, USA). Two statistical analyses including multivariate methods were performed:

Post-surgical infection control

Patients were instructed not to brush the teeth in the treated area but to rinse with chlorhexidine solution (0.12%) twice daily for 1 min. Fourteen days after the surgical treatment, the sutures were removed. Plaque control in the surgically treated area was maintained by chlorhexidine rinsing for an additional 2 weeks. After this period, the patients were again instructed in mechanical tooth cleaning of the treated tooth region using a soft toothbrush and a roll technique. All patients were

After fitting a general linear model, a multiple regression ANOVA for repeated measures was used to evaluate any time-dependent difference (baseline, 1- and 3-year) regarding FMPS, FMBS, recession of the gingival margin (REC), PPD, CAL and KTH. The method used to discriminate between the means was Fisher’s least significant difference (LSD) procedure. The same general linear model was fitted to relate the difference

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Coronally advanced flap between baseline and 3-year KTH to two categorical (smoke, and number of sites/patient) and two continuous (baseline REC and KTH) factors as covariates (ANCOVA).

Results

Following the initially provided oral hygiene phase as well as at the posttreatment examinations, all subjects showed low frequencies of plaque harbouring tooth surfaces (o20%) and bleeding gingival units (o15%), indicating an acceptable standard of supragingival plaque control during the study period. Eight patients were identified as smokers (smoking more than 10 cigarettes/day); all other patients did not smoke. Forty isolated recession-type defects (in 40 patients) were treated with the coronally advanced surgical technique. All gingival recessions were located in the upper jaw. The tooth population consisted of incisors (6), cuspids (24) and pre-molars (10). Clinical measurements

Table 1 gives the baseline, the 1-year and 3-year mean data for the various clinical parameters assessed. At baseline, the average depth of the recession defects was 3.82 1.2 mm, with a mean clinical attachment loss amounting to 4.96 1.3 mm. The depth of the recessions ranged from 2 to 6 mm. The height of the gingival keratinized tissue apical to the recession was on the average 1.34 0.6 mm. Fourty-eight percent of the recession sites had 1 mm or less of KTH. One year and 3 years following the root coverage procedure, the mean recession depth was 0.10 0.3 and 0.18 0.6 mm, respectively. Hence, the average root coverage was

3.72 1.0 mm (98.6% of the preoperative recession) at 1 year and 3.64 1.1 mm (96.7%) at 3 years. The results of the multiple regression ANOVA for repeated measures show a significant (F 5 56.45; po0.01) relationship in the time-dependent variations of REC depth; in particular, both REC reductions (difference between baseline REC and 1-year REC and between baseline REC and 3-year REC) were statistically significant, while the increase in gingival recession that occurred between the 1- and the 3-year follow-up visits (0.08 0.53 mm) was not statistically significant. Additional information regarding the long-term effectiveness of the surgical technique used for soft tissue root coverage comes from the following data: on the average, 96.7% of the root surface initially exposed due to recession was still covered with soft tissue at the 3-year examination. At this time point, 34 of the 40 treated recession defects (85%) showed complete coverage. None of the treated sites showed greater remaining recession depth than 1.0 mm. PPD remained almost unchanged (mean value 1 mm) in the three (baseline, 1 and 3 years) observation periods. The results of multiple regression ANOVA for repeated measures show no significant (F 5 2.45) relationship in the time-dependent variations of PPD. The gain in probing attachment amounted to 3.65 1.1 mm at 1 year and to 3.60 1.2 mm at 3 years. The results of the multiple regression ANOVA for repeated measures show a significant (F 5 30.70; po0.01) relationship in the time-dependent variations of CAL; in particular, a significant difference was found between the 1- and 3-year values compared with the baseline value; while the loss of clinical attachment occurred during the 3-year observation period (0.05 0.6 mm) was not statistically significant.

Table 1. Results of the multiple regression ANOVA for repeated measures relating to oral hygiene and clinical parameters (MV SD in mm) Baseline FMPS FMBS REC PPD CAL KTH

10.45 12.70 3.82 1.14 4.96 1.34

2.1 2.2 1.2 0.3 1.3 0.6

1 year (a) (a) (a) (a) (a) (a)

10.28 10.48 0.10 1.21 1.31 2.04

2.3 2.3 0.3 0.2 0.5 0.8

3 years (a) (a) (b) (a) (b) (b)

10.12 1.8 12.18 1.8 0.18 0.6 1.18 0.3 1.36 0.6 3.12 0.9

(a) (a) (b) (a) (b) (c)

Different letters indicate a statistically significant difference between groups for each parameter. FMPS, full-mouth plaque score; FMBS, full-mouth bleeding score; REC, recession of the gingival margin; PPD, probing pocket depth; CAL, clinical attachment level, KTH, keartinized tissue height.

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Compared with the conditions before surgical treatment, the KTH showed an increase of 0.70 0.8 mm at 1 year and a further increment of 1.08 0.9 mm during the 2-year observation period and amounted to (on average) 3.12 0.5 mm at 3-year post-treatment. The average increase of keratinized tissue between the baseline and the 3-year follow-up amounted to 1.78 0.9 mm. The results of the multiple regression ANOVA for repeated measures show a significant (F 5 11.79; po0.01) relationship in the time-dependent variations of KTH. All changes of keratinized tissue (difference between baseline and 1 year, baseline and 3 years and between 1 and 3 years) were statistically significant. The results from the ANCOVA show that the difference between the baseline and 3-year KTH was significantly affected by KTH (F 5 137.01; po0.01) and REC (F 5 3.71; po0.05) at baseline: in particular, the 3-year increase in the amount of keratinized tissue was greater in sites with greater recession depth and lower amount of keratinized tissue at baseline. The limited number of subjects smokers was not sufficient to perform any analysis on this variable.

Discussion

Treatment of gingival recession is becoming an important issue in clinical periodontology due to the increasing demand for cosmetic treatment. Problems relate particularly to the fact that very often, the patient exposes only the most coronal millimitres of the recession when smiling. Thus, only surgical procedures that provide the clinician with a very high percent of complete root coverage should be included in the mucogingival plastic surgical techniques. Moreover, excessive thickness or poor colour blending of the surgically treated areas, as those resulting from soft tissue graft, should be avoided. The only limiting criteria in utilizing a coronally advanced flap is the need of a band of at least 1 mm of keratinized tissue; Wennstrom & Zucchelli (1996) have stated that the amount of root coverage utilizing coronally advanced flap with or without the presence of a connective tissue graft will not show any significante difference at the 2-year interval. More recently, the results from a systematic review on periodontal plastic surgery (Roccuzzo et al. 2002) stated that the use of a barrier membrane or

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connective tissue, together with a coronally advanced flap, do not give better results than coronally advanced flap alone when root coverage is considered. Moreover, patient-related aesthetic considerations would suggest the utilization of surgical techniques that can predictably obtain complete root coverage by using the soft tissue adjacent to the defect (de Sanctis & Zucchelli 1996). The results of the present case-series study indicate that the modified coronally advanced surgical approach was highly effective in obtaining root coverage of isolated type of gingival recession defects and that this successful outcome was well maintained for a 3-year observation period (Fig. 2). This technique, in fact, resulted, at 1 year, in a very high mean percentage of root coverage (98.6%) and complete soft tissue root coverage (up to the CEJ) was obtained in the great majority (88%) of treated cases. No statistically and clinically significant changes in root coverage outcomes were demonstrated at the 3-year re-evaluation visit. At this time point, 96.7% of the root surface initially exposed due to gingival recession was still covered with soft tissue and 85% of the treated recession defects showed complete coverage. The successful results in terms of root coverage achieved in the present study were associated with a clinically significant average increase in KTH with no change in PPD; thus, the gain in clinical attachment was well maintained during the observation period. This rate of long-term successful outcomes of the treatment was similar (Wennstrom & Zucchelli 1996, Zucchelli et al. 2004, Del Pizzo et al. 2005, Zucchelli & de Sanctis 2005) or even higher (Caffesse & Guinard 1980, Pini Prato et al. 1996, Al-Hamdan et al. 2003, Trombelli et al. 2005) than that previously reported in the literature for other root coverage procedures. Some clinical and biological advantages of the technique adopted in the present study might be related to the splitâ&#x20AC;&#x201C;fullâ&#x20AC;&#x201C;split flap elevation as already suggested by Zucchelli & de Sanctis (2000): the split-thickness elevation at the level of the surgical papilla guarantees anchorage and blood supply in the inter-proximal areas mesial and distal to the root exposure; the full-thickness portion, by including the periostium, confers more thickness, and thus better opportunity to achieve root coverage, to

Fig. 2. (a) Upper right first pre-molar, pre-surgical. (b) Root coverage 1 year following surgery. (c) Clinical results 3 years after surgery: note the increase in keratinized tissue.

Fig. 3. (a) Upper left cuspid, pre-surgical: note the minimum amount of keratinized tissue. (b) Root coverage 1 year following surgery. (c) Clinical results 3 years after surgery: a dramatic increment in keratinized tissue is evident.

that portion of the flap residing over the previously exposed avascular root surface; the more apical split-thickness flap elevation facilitates the coronal displacement of the flap. Although the technique comprises vertical releasing incisions, these did not result in unaesthetic scars. These incisions, in fact, were bevelled in such a way that the bone and periosteal tissues were not included in the superficial cut and thus did not participate to the healing process. On the contrary, the surgical papillae, outlined by the horizontal 3 mm incisions and by the vertical bevelled incision, were very wide and thus provided a larger area for anchoring the flap to the underlying vascular bed and more tissue to place the coronal sling suture. Furthermore, the partial thickness of the surgical papillae facilitated the nutritional exchanges between them and the underlying disepitelized anatomical papillae and improved the blending (in terms of colour and thickness) of the surgically treated area with respect to adjacent soft tissues.

Another important modification of the present surgical technique, with respect to the previously proposed ones (Patur & Glickman 1958, Allen & Miller 1989, Wennstrom & Zucchelli 1996), was that the coronal advancement of the flap was not obtained by means of periosteal incisions but through the elimination of muscle insertions included in the thickness of the flap. This permitted to eliminate lip tension on the flap, and to displace passively the soft tissue flap in the coronal position. The flap, in fact, was stable in a position coronal to the CEJ even without sutures, because of the absence of muscle pull. The absence of a wide band of keratinized tissue apical to the recession defect was considered to be a limitation for the coronally advanced technique. On the contrary, the present study demonstrated an inverse relationship between the apicoâ&#x20AC;&#x201C;coronal dimension of gingival tissue apical to the root exposure and the increase of keratinized tissue achieved with the surgery. Three years after the surgery, in fact, the

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Coronally advanced flap increase of keratinized tissue was greater in sites with greater recession depth and lower amount of keratinized tissue at baseline (Fig. 3). Very similar results were obtained in a previous study evaluating the 5-year outcomes of the coronally positioned flap for multiple gingival recession (Zucchelli & de Sanctis 2005). Some hypothesis can be made in an attempt to explain the 1- and 3-year increase of keratinized tissue after coronally advanced flap: the tendency of the mucogingival line, coronally displaced by means of surgery, to regain its original, ‘‘genetically determined’’ position (Ainamo et al. 1992), or the capability of the connective tissue, deriving from the periodontal ligament, to participate in the healing processes taking place at the dento-gingival interface (Karring et al. 1971, Lundberg & Wennstrom 1988, Pasquinelli 1995). The long-term increase in KTH was also reported by Pini Prato et al. (1996) for GTR-treated gingival recession. Also, in this study, the 18-month growth in KTH was followed by a further increase that occurred in the following two and half years. The similarity in the amount and trend of keratinized tissue changes obtained after a coronally advanced flap with and without the use of a barrier membrane seems to validate the importance of the tendency of the mucogingival junction to regain its genetically defined position rather then to attribute a significant role to the granulation tissue deriving from the periodontal ligament tissue to increase the dimension of the gingiva. Regardless of the biologic principle capable of explaining the increase of keratinized tissue after coronally advanced flap, the present data indicate that a residual wide band of attached gingival apical to the root exposure is not required to perform successfully the coronally advanced flap as a root coverage surgical technique. On the contrary, once the stability of the soft tissue margin has been obtained at the level of the CEJ, the keratinized tissue is able to increase with time. However, a presurgical minimal amount of keratinized tissue is advocated to provide marginal stability for the surgical flap. In conclusion, the results of the present study demonstrated that the modified approach of the coronally advanced flap technique was effective in treating isolated-type gingival recessions in the upper jaw. Successful results were

achieved at 1 year, both in terms of aesthetics (root coverage and colour blending with adjacent soft tissues) and increase of keratinized tissue, and were well maintained or even improved (in terms of height of attached gingiva) during the subsequent 2-year observation period.

References Ainamo, A., Bergenholtz, A., Hugoson, A. & Ainamo, J. (1992) Location of the mucogingival junction 18 years after apically repositioned flap surgery. Journal of Clinical Periodontology 19, 49–52. Al-Hamdan, K., Eber, R., Sarment, D., Kowalski, C. & Wang, H. L. (2003) Guided tissue regeneration-based root coverage: meta-analysis. Journal of Periodontology 74, 1520–1533. Allen, E. P. & Miller, P. D. (1989) Coronal positioning of existing gingiva: short term results in the treatment of shallow marginal tissue recession. Journal of Periodontology 60, 316–319. Caffesse, R. G. & Guinard, E. A. (1980) Treatment of localized gingival recessions. Part IV. Results after three years. Journal of Periodontology 51, 167–170. Del Pizzo, M., Zucchelli, G., Modica, F., Villa, R. & Debernardi, C. (2005) Coronally advanced flap with or without enamel matrix derivative for root coverage: a 2-year study. Journal of Clinical Periodontology 32, 1181–1187. de Sanctis, M. & Zucchelli, G. (1996) Soft tissue plastic surgery in the treatment of gingival recession. Successful criteria for root coverage. Parodontologie et d’implantologie orale 15, 7–18. Hall, W. B. (1989) Gingival augmentation/ Mucogingival surgery. Proceedings of the World Workshop in Clinical Periodontics; Section VII:1-15, Princeton, NJ, USA. Karring, T., Ostergaard, E. & Loe, H. (1971) Conservation of tissue specificity after heterotopic transplantation of gingiva and alveolar mucosa. Journal of Periodontal Research 6, 282–293. Lundberg, M. & Wennstrom, J. L. (1988) Development of gingival following surgical exposure of a facially positioned unerupted incisor. Journal of Periodontology 59, 652– 655. Miller, P. D. (1985) A classification of marginal tissue recession. International Journal of Periodontics and Restorative Dentistry 5, 9–13. Norberg, O. (1926) Ar en utlakning utan vovnadsfortust otankbar vid kirurgisk behandling av. S. K. Alveolarpyorrhoe? Svensk Tandlaekare Tidskrift 19, 171. O’Leary, T. J., Drake, R. B. & Naylor, J. E. (1972) The plaque control record. Journal of Periodontology 43, 38. Pasquinelli, K. L. (1995) The histology of new attachment utilizing a thick autogenous

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soft tissue graft in an area of deep recession: a case report. International Journal of Periodontics and Restorative Dentistry 15, 248–257. Patur, B. & Glickman, I. (1958) Gingival pedicle flaps for covering root surfaces denuded by chronic destructive periodontal disease. Journal of periodontalogy 29, 50. Pini Prato, G., Clauser, C., Cortellini, P., Tinti, C., Vincenzi, G. & Pagliaro, U. (1996) Guided tissue regeneration versus mucogingival surgery in the treatment of human buccal recessions. A 4-year follow-up study. Journal of Periodontology 67, 1216–1223. Pini Prato, G. P., Baldi, C., Nieri, M., Franseschi, D., Cortellini, P., Clauser, C., Rotundo, R. & Muzzi, L. (2005) Coronally advanced flap: the post-surgical position of the gingival margin is an important factor for achieving complete root coverage. Journal of Periodontology 76, 713–722. Roccuzzo, M., Bunino, M., Needleman, I. & Sanz, M. (2002) Periodontal plastic surgery for treatment of localized gingival recessions: a systematic review. Journal of Clinical Periodontology 29 (Suppl. 3), 178–194. Tenenbaum, H., Klewansky, P. & Roth, J. J. (1980) Clinical evaluation of gingival recession treated by coronally repositioned flap technique. Journal of Periodontology 51, 686–690. Trombelli, L., Minenna, L., Farina, R. & Scabbia, A. (2005) Guided tissue regeneration in human gingival recessions. A 10-year follow-up study. Journal of Clinical Periodontology 32, 16–20. Wennstrom, J. L. & Zucchelli, G. (1996) Increased gingival dimensions. A significant factor for successful outcome of root coverage procedures? A 2-year prospective clinical study. Journal of Clinical Periodontology 23, 770–777. Zucchelli, G., Cesari, C., Amore, C., Montebugnoli, L. & de Sanctis, M. (2004) Laterally moved, coronally advanced flap: a modified surgical approach for isolated recession-type defects. Journal of Periodontology 75, 1734–1741. Erratum in: Journal of Periodontology 2005 76(8):1425. Zucchelli, G. & de Sanctis, M. (2000) Treatment of multiple recession-type defects in patients with esthetic demands. Journal of Periodontology 71, 1506–1514. Zucchelli, G. & de Sanctis, M. (2005) Longterm outcome following treatment of multiple class I and II recession defects in esthetic areas of the mouth. Journal of Periodontology 76, 2286–2292.

Address: Prof. Massimo de Sanctis Via Gustavo Modena 10 50121 Florence Italy E-mail: massimodesanctis@tin.it

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Clinical Relevance

Scientific rationale for the study: It has been shown that a split–full–split approach in coronally advanced flap is a reliable surgical modality to obtain coverage of multiple recessions and to increase the amount of keratinized tissue. It is conceivable that similar results could be obtained with a single tooth approach. Also, longterm results of coronal advanced flap are lacking in the literature. This study reports the long-term clinical results following a modification of the coronally advanced flap on single tooth recession type defects utilizing a split– full–split surgical technique.

Principal findings: The average root coverage with the modified coronally advanced flap was 98.6% of the preoperative recession at 1 year and 96.7% at 3 years. All changes of keratinized tissue (difference between baseline and 1 year, baseline and 3 years and between 1 and 3 years) were statistically significant. At 3 years, the increase in the amount of keratinized tissue was greater in sites with greater recession depth and lower amount of keratinized tissue at baseline. Practical implications: This study supports the effectiveness of a new surgical approach in the coronal displacement of marginal tissue for root

coverage. The described technique is highly effective in obtaining root coverage and maintaining the results over a 3-year time period. Also, during the time of observation, it was possible to evidence an increase in keratinized tissue that was inversely related to the pre-surgical amount. This finding tends to support the fact that the absence of a wide band of keratinized tissue apical to the recession defect is not a limiting factor in obtaining root coverage.

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J Clin Periodontol 2010; 37: 728–738 doi: 10.1111/j.1600-051X.2010.01550.x

Patient morbidity and root coverage outcome after subepithelial connective tissue and de-epithelialized grafts: a comparative randomizedcontrolled clinical trial

Giovanni Zucchelli1, Monica Mele1, Martina Stefanini1, Claudio Mazzotti1, Matteo Marzadori1, Lucio Montebugnoli1 and Massimo de Sanctis2 1

Department of Odontostomatology, Bologna University, Bologna, Italy; 2Department of Periodontology, Siena University, Siena, Italy

Zucchelli G, Mele M, Stefanini M, Mazzotti C, Marzadori M, Montebugnoli L, de Sanctis M. Patient morbidity and root coverage outcome after subepithelial connective tissue and de-epithelialized grafts: a comparative randomized-controlled clinical trial. J Clin Periodontol 2010; 37: 728–738. doi: 10.1111/j.1600-051X.2010.01550.x. Abstract Aims: The aim of this randomized-controlled clinical trial was to compare the patient morbidity and root coverage outcomes of a coronally advanced flap (CAF) with connective tissue (CTG) or de-epithelialized gingival (DGG) grafts. Methods: Fifty patients with one recession each were treated. In the control group, the CTG was harvested using the trap-door approach while in the test group the CTG resulted from the de-epithelialization of a free gingival graft. Results: No statistically significant differences were demonstrated between groups in patients’s pain killer consumption, post-operative discomfort and bleeding. Lower stress and better ability to chew were demonstrated in the CTG group. Analgesic consumption increased with increasing height of the graft and in the case of dehiscence/necrosis of the primary flap. Pain was negatively correlated with the residual thickness of soft tissue covering the palatal bone. A statistically greater increase in buccal soft tissue thickness was observed in the DGG group. Conclusions: No differences were demonstrated in the post-operative pain and root coverage outcome in patients subjected to CAF with CTG or DGG.

A soft tissue graft is a withdrawal of soft tissue that is completely detached from its original donor site and placed in a prepared recipient bed (American Academy of Periodontology 2001). The Conflict of interest and source of funding The authors declare that there is no conflict of interest concerning the contents of the study. This study has been self-supported by the authors.

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palate is the most frequent donor site for intra-oral connective tissue (CTG) and epithelialized free gingival (FGG) grafts used for root coverage purpose. Palatal fibromucosa is characterized by a dense connective tissue (lamina propria) covered by an orthokeratinized epithelium (Mu¨ller et al. 2000). A layer of fatty and glandular tissue (submucosa) of varied thickness is present between the palatal fibromucosa and the periosteum covering the palatal bone (Harris 2003). A remarkable variation in the histologic makeup of CTG

Key words: connective tissue graft; esthetics; free gingival graft; gingival recession; mucogingival surgery Accepted for publication 9 January 2010

has been observed (Harris 2003), in terms of both the thickness and the percentage of lamina propria and submucosa. The thickness of palatal fibromucosa varies from patient to patient and, in the same patient, from site to site of the palate (Mu¨ller et al. 2000). Palatal thickness (PT) can be clinically determined, at the time of anaesthesia, by penetrating with an endodontic reamer/ needle perpendicular to the palatal bone plate (Studer et al. 1997, Paoloantonio et al. 2002, da Silva et al. 2004, Joly et al. 2007) The penetration depth can r 2010 John Wiley & Sons A/S

Patient morbidity and root coverage outcome after grafts be measured, by using an endodontic silicon disk applied to the reamer/needle, as the distance between the silicon ring and the tip of the reamer/needle. An ultrasonic device has also been used to determine soft tissue thickness around teeth and implants (Eger et al. 1996, Mu¨ller et al. 1999, 2000). A study by Eger et al. (1996) showed that a needle and an ultrasonic device yield very similar results. In addition to the measurement of the distance between the external palatal surface and the palatal bone plate, from a clinical standpoint, it is even more important to evaluate the degree of the palatal soft tissues resistance to needle penetration. In fact, while the fibromucosa (epithelium and connective tissue) has a firm consistency and thus a resistance is felt during needle penetration, the fatty and glandular tissues do not offer opposition to the needle and resistance is felt only at the bone level. This evaluation is critical, particularly when connective tissue-harvesting procedures are chosen. Different connective tissue-harvesting procedures with the purpose of achieving primary intention palatal wound healing have been described in the literature: the most common are the trap-door approach (Edel 1974) and the single-incision technique (Hu¨rzeler & Weng 1999, Lorenzana & Allen 2000). These procedures have the following common characteristics: a primary split-thickness access flap elevation, the withdrawal of CTG and the complete closure of the palatal wound with the access flap. The primary objective of these techniques is to reduce patient morbidity by alleviating the post-operative course; however, they need an adequate thickness of the palatal fibromucosa to avoid desquamation of the undermined superficial flap due to compromised vascularization (Edel 1974, Langer & Langer 1985, Jahnke et al. 1993). The FGG surgical wound heals by secondary intention within 2–4 weeks (Farnoush 1978) and has been consistently associated with greater discomfort for the patient due to post-operative pain and/or bleeding (Farnoush 1978, Jahnke et al. 1993, Del Pizzo et al. 2002). However, this technique is easy to perform and can be utilized even in the presence of a thin palatal fibromucosa. The evidence in the literature evaluating differences in patient outcomes r 2010 John Wiley & Sons A/S

following the CTG and FGG, used for root coverage procedures, is minimal. Few prospective comparative studies (Del Pizzo et al. 2002, Griffin et al. 2006, Wessel & Tatakis 2008) reported poorer patient outcomes, specifically, a greater incidence of post-operative pain, for FGG compared with CTG procedures. No randomized study has been performed comparing both patient and root coverage outcomes after the use of CTG and de-epithelialized gingival (DGG) grafts for the treatment of gingival recessions. The aim of the present randomizedcontrolled clinical study was to compare post-operative morbidity and root coverage outcomes in patients subjected to trap-door connective tissue (control group) and epithelialized (test group) graft-harvesting techniques for the treatment of gingival recession with the bilaminar procedure. The primary objective of the study was to demonstrate the superiority in terms of the post-operative course and pain of the connective tissue-harvesting technique. The secondary goal was to compare the effectiveness, in terms of root coverage and increase in buccal gingival thickness (GT), of CTG, harvested with the trap-door approach or resulting from the de-epithelialization of a free gingival graft, used in combination with a coronally advanced flap (CAF) for the treatment of gingival recessions.

Material and Methods

Fifty subjects, 22 males and 28 females (age range 21–50 years, mean age 34.7 6.0 years), were enrolled in the study. The patients were selected, on a consecutive basis, among individuals referred to the University of Bologna and the University of Siena, Dental School, in the period between February 2006 and March 2007. The study protocol, questionnaires and informed consent, in full accordance with the ethical principles of the Declaration of Helsinki of 1975, as revisited in 2000, were approved by the Institutional Review Board and received the approval by of the local ethic committee. All patients agreed to participate in the study and signed a written informed consent according to the above-mentioned principles. All participants met the study inclusion criteria: single or multiple Miller’s Class I

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and II recession defects (X2 mm in depth); presence of identifiable cemento-enamel junction (CEJ); presence of a step 41 mm at the CEJ level and/or the presence of a root abrasion, but with an identifiable CEJ, were accepted; periodontally and systemically healthy; no contraindications for periodontal surgery and not taking medications known to interfere with periodontal tissue health or healing; no anti-inflammatory drugs or antibiotics for at least 6 months; and no periodontal surgery on the involved sites. Subjects smoking more than 10 cigarettes a day were excluded. Recession defects associated with caries or restoration as well as teeth with evidence of a pulpal pathology were not included. Molar teeth were also excluded.

Study design

The study was a double-centre (one in Bologna and the other one in Siena), double-blinded, randomized-controlled clinical trial, with a parallel design, comparing CAF with CTG or with DGG for the treatment of gingival recessions. In the control group, the CTG was harvested with the trap-door approach while in the test group, the CTG resulted from the de-epithelialization, using a scalpel blade, of a free gingival graft. Both types of grafts were harvested from the palate. The study protocol involved a screening appointment to verify eligibility, followed by initial therapy to establish optimal plaque control and gingival health conditions, surgical therapy, evaluation of patient morbidity 1 week after the surgery, maintenance phase and post-operative clinical evaluation 1 year after the surgery.

Sample size

The study was powered to detect a minimum clinically significantly different pain killer consumption of 1800 mg using a 5 0.05, a power 5 85%, a hypothesized within-group sigma of 2000 mg, obtained from the only previous randomized comparative studies (Wessel and Tatakis) with patient morbidity as the primary outcome. As a minimum, 24 patients per treatment arm would have been required.

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Investigator training

All participating investigators were required to attend two training and calibration meetings. The aims of the meetings were to review the objectives of the study and the protocol, and standardize the case selection, the measurement techniques and the surgical procedures. Randomization

Patients were assigned to one of the two treatment groups using a computer-generated randomization table. All patients participated in the study with a single tooth. Twenty-five teeth were assigned to the control group and 25 teeth to the test group. In the case of patients presenting with multiple recessions, the deepest one was selected; in the case of two or more recessions of the same depth, the selection was performed by tossing a coin. Allocation concealment was achieved using a sealed coded opaque envelope containing the treatment of the specific subject. The sealed envelope containing treatment assignment was opened during the surgery immediately before the graft harvesting.

Bleeding on probing was assessed dichotomously at a force of 0.3 N using a manual pressure-sensitive probe [(PCP-UNC 15 probe tip, Hu Friedy, Chicago, IL), equipped with a Brodontic spring device (Dentramar, Waalwijk, the Netherlands)]. Full-mouth (FMBS) and local bleeding scores were recorded as the percentage of total surfaces (four aspects per tooth) that revealed the presence of bleeding upon probing. The following clinical measurements were taken 1 week before surgery and at the 1-year follow-up at the midbuccal aspect of the study teeth: (1) gingival recession depth (RD), measured from the CEJ to the most apical extension of the gingival margin; (2) probing depth (PD), measured from the gingival margin to the bottom of the gingival sulcus; (3) clinical attachment level (CAL), measured from the CEJ to the bottom of the gingival sulcus; (4) height of keratinized tissue (KTH): the distance between the gingival margin and the mucogingival junction (MGJ). The MGJ was identified by means of Lugol staining

Initial therapy and clinical measurements

Following the screening examination, all subjects received a session of prophylaxis including instruction in proper oral hygiene measures, scaling and professional tooth cleaning with the use of a rubber cup and a low abrasive polishing paste. A coronally directed roll technique was prescribed for teeth with recession-type defects in order to minimize toothbrushing trauma to the gingival margin. Surgical treatment of the recession defects was not scheduled until the patient could demonstrate an adequate standard of supragingival plaque control. All clinical measurements were carried out by a single masked examiner (M. M.) at baseline and 1 year after the surgery. MM did not perform surgery and was unaware of the treatment assignment. Before the study, the examiner was calibrated to reduce intraexaminer error (k40.75) to establish reliability and consistency. Full-mouth (FMPS) and the local plaque scores were recorded as the percentage of total surfaces (four aspects per tooth) that revealed the presence of plaque (Oâ&#x20AC;&#x2122;Leary et al. 1972).

All measurements were performed by means of the manual probe and were rounded up to the nearest millimetre: (5) GT: determined 1.5 mm apical to the gingival margin with a short needle for anaesthesia and a 3mm-diameter silicon disk stop. The needle was inserted perpendicular to the mucosal surface, through the soft tissues with light pressure until a hard surface was felt. The silicon disk stop was then placed in tight contact with the soft tissue surface with the coronal border overlapping the soft tissue margin. As the needle was located in the centre of the silicon disk, measurement of GT was performed 1.5 mm apical from the gingival margin. Once in the correct position, the disk was fixed with a drop of cyanocrylic adhesive; after careful removal of the needle, the penetration depth was measured with a calliper accurate to the nearest 0.1 mm (Paoloantonio et al. 2002, da Silva et al. 2004, Joly et al. 2007).

Intra-surgical measurement

After local anaesthesia, PT in the area selected for harvesting the graft was measured. The measurement was made at the mid palatal location about 1.5 mm apical to the gingival margin of the adjacent tooth, by means of the needle used for anaesthesia and a silicon disk stop. The needle was inserted perpendicular to the mucosal surface, through the soft tissues with light pressure until a hard surface was felt. The silicon disk stop was then placed in tight contact with the soft tissue surface and fixed by a drop of cyanocrylic adhesive; after careful removal of the needle, the penetration depth was measured with the calliper. The thickness of the grafts was measured in both test and control groups just after being harvested (GRT) and just before being sutured (GRTs), after deepithelialization (in the test group) and removal of fatty tissue when present. In the control group, the thickness of the primary flap (FT) was measured. All measurements were made 1.5 apical to the coronal border with the calliper. The width (GRW) (mesialâ&#x20AC;&#x201C;distal dimension) and the height (GRH) (apical coronal dimension) of the CTG were measured just before being sutured with the manual probe and rounded up to the nearest millimetre. Graft measurements were performed by a different examiner (C. M.). Patient morbidity

Post-operative pain was indirectly evaluated on the basis of the mean consumption (in mg) of analgesics (ibuprofene) (Wessel & Tatakis 2008, Sanz et al. 2009). Patientsâ&#x20AC;&#x2122; post-operative discomfort, bleeding, stress and inability to chew was evaluated with a questionnaire given to patients 1 week following surgery. The questionnaire included the evaluation of the intensity of the given event on a visual analogic scale (VAS) of 100 mm (Cortellini et al. 2001, 2009). Discomfort was defined as the level of soreness/pain experienced by the patients during the first post-operative week due to the palatal wound. Bleeding was considered to be the prolonged haemorrhaging during the post-surgical week reported by the patients. Stress was evaluated based on the level of apprehension and fear experienced by the patients of jeopardizing the palatal r 2010 John Wiley & Sons A/S

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Fig. 1. The connective tissue graftharvesting technique. (a) The incision design of the primary access flap. (b) The blade proceeds apically parallel to the external palatal surface. (c) Split-thickness flap elevation. (d) The graft is being harvested. The blade proceeds parallel to the external surface of the graft in order to maintain a uniform thickness in the graft and to preserve as much soft tissue covering the periosteum as possible. (e) Soft tissue protecting the bone is left. (f) External surface of the graft facing the covering flap. (g) Internal surface of the graft facing the root surface. All fatty and glandular tissue has been removed. (h) Complete closure of the palatal wound has been achieved. (i) A slight dehiscence of the primary flap can be noticed 7 days after the surgery.

wound. Inability to chew was described as the level of variation of the patient’s eating habits due to the presence of the palatal wound.

Surgical techniques

All surgeries were performed by two calibrated expert periodontologists (G. Z. and M. D. S.). G. Z. performed 26 surgeries (13 tests and 13 controls) and M. D. S. performed the remaining 24 (12 tests and 12 controls). During local anaesthesia (2% lidocain with epinephrine at a concentration of 1:100,000), the surgeon chose the harvesting site on the palate (pre-molar or molar) on the basis of the amount (PT) and quality (soft tissues resistance) of needle penetration. The surgeons were then informed as to which type of graft harvesting technique to perform, trap-door or epithelialized, by opening the envelope labelled, which contained the patient’s number with the assigned treatment. r 2010 John Wiley & Sons A/S

Control group The surgical technique adopted for harvesting the CTG in the control group was a modification of the trap-door approach described by Edel (1974) (Fig. 1). In brief, one horizontal incision of the same length of the mesial–distal dimension of the graft was traced 1– 1.5 mm apical to the gingival margin of the adjacent teeth. Two vertical releasing incisions were performed at the end of the horizontal incisions and were extended in the apical direction 1 mm more than the apical–coronal dimension of the graft. The primary flap was elevated split-thickness to maintain a uniform thickness throughout the flap. The horizontal incision of the graft was made along the horizontal incision of the flap with the blade almost perpendicular to the underlying bone. Once an adequate soft tissue thickness was obtained, the blade was rotated in order to be almost parallel to the external surface. The thickness of the graft was

maintained uniform while proceeding apically with the blade. Care was taken not to remove the periosteum protecting the underlying bone. Once the graft was removed, the fatty tissue (yellow in colour) was eliminated. The primary flap was repositioned and interrupted single 6-0 sutures (Vicryl, Johnson & Johnson, Woluwe, Belgium) were made to achieve complete closure of the palatal wound.

Test group A free (epithelialized) gingival graft was harvested in the test patients (Fig. 2). Two horizontal (the coronal incision was performed 1–1.5 mm apical to the soft tissue margin of the adjacent teeth) and two vertical incisions were traced to delimitate the area to be grafted. Along the coronal horizontal incision, the blade was oriented almost perpendicular to the bone plate and once an adequate soft tissue thickness was obtained, it was

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Fig. 2. The epithelialized gingival graft harvesting technique. (a) The incision design of the free gingival graft. (b) The blade proceeds apically parallel to the external palatal surface in order to maintain a uniform thickness in the graft. (c) Soft tissue thickness covering the periosteum has been preserved during the harvesting procedure. (d) Minimal bleeding after removal of the graft due to the superficial wound. (e) External surface of the graft before de-epithelialization. Note the reflection of the light due to the presence of the epithelium. (f) Deepithelialization made with the blade kept parallel to the external surface of the graft. (g) External surface of the graft after deepithelialization. Note the different light reflection. (h) The palatal wound has been protected with equine-derived collagen maintained in situ with a sling mattress suture. (i) Secondary intention palatal healing 7 days after the surgery. Note the rapid tissue healing.

rotated in order to be almost parallel to the superficial surface. The thickness of the graft was maintained uniform while proceeding apically with the blade. Care was taken not to remove the periosteum protecting the underlying bone. Once the graft was separated, the fatty tissue (yellow in colour) was eliminated. The palatal wound was protected with equine-derived collagen (GABA Vebas, San Giuliano Milanese, MI, Italy) maintained in situ with compressive sling 5-0 sutures anchored to the soft tissue apical to the palatal wound area. The graft was de-epithelialized with a 15c blade. The graft was positioned on a sterile gauze or a surgical cloth and its surface was made wet with a saline solution. A light was oriented to be perpendicular to the graft. The different consistency (epithelium is harder and more rough while the connective tissue is softer and smoother) allowed removal of the epithelium when cutting with the blade kept parallel to the external surface. The different light reflection (the epithelium reflects more than the connective tissue) enabled to

clinically distinguish when the epithelium was removed. The de-epithelialization of the graft and the control for epithelium removal were performed under magnification (4 ) vision. A bilaminar (CAF1CTG) technique (Zucchelli et al. 1998, 2003) was performed in both patient groups to accomplish root coverage. In brief, exposed root surfaces were mechanically treated with the use of curettes, a trapezoidal flap was raised split thickness and CTG were sutured at the level of the CEJ. The width of the graft was chosen according to the amount of tissue required to cover the exposed root and 3 mm of connective tissue mesial and distal to it. The height of the graft was based on the distance from the CEJ to the buccal bone crest. No attempt was made to cover the periosteum apical to the bone dehiscence. The remaining buccal soft tissue of the anatomic interdental papillae was deepithelalized to create connective tissue areas to which the surgical papillae of the covering flap were sutured. The flap was coronally advanced, by cutting muscle

insertions present in the thickness of the flap, and sutured with sling sutured anchored around the palatal cingulum of teeth with gingival recessions. At the time of suturing, the flap should cover the graft and the flap margin should be coronal to the CEJ of all teeth included in the flap design. No periodontal dressing was applied. Surgical chair time was measured using a chronometer from the first incision to the last suture in both groups. Post-surgical infection control

Post-operative pain and oedema were controlled with ibuprofen. Patients received 600 mg at the beginning of the surgical procedure. Subsequent doses were taken only if necessary to control pain. Patients had to record the quantity of analgesics taken during the first week post-surgery. Patients were instructed not to brush their teeth in the treated area but to rinse with chlorhexidine solution (0.12%) three times a day for 1 min. One week r 2010 John Wiley & Sons A/S

Patient morbidity and root coverage outcome after grafts

A statistical application software (SAS, version 6.09, SAS Institute, Cary, NC, USA) was used for the statistical analysis. Descriptive statistics were expressed as mean � SD. Complete coverage was evaluated after 1 year by calculating the percentage of cases, in each treatment group, with the gingival margin at the level or coronal to the CEJ. Percentage of root coverage was calculated after 12 months according to the following formula:

One-way ANOVA was used to evaluate the presence of any significant difference in pain, alarm, bleeding, chewing and discomfort, between the seven patients experiencing primary flap dehiscence/necrosis and the test patients and control patients who did not experience primary flap dehiscence/necrosis. A general linear statistical model was fitted relating analgesic consumption to RTT, GR width, GR height and area (molar versus pre-molar) of the withdrawal. General linear models were also fitted, and multiple regression ANOVA for repeated measures with a split-plot design was used to evaluate the existence of any significant difference regarding RD, CAL, PD, KTH and GT between techniques (CAF with CTG versus CAF with DGG), time (1 year versus baseline) and the interaction between techniques and time. In case of significance, the Bonferroni t test was applied as a multiple comparison test. A logistic regression model was fitted to relate complete root coverage as the outcome variable and techniques (CAF with CTG versus CAF with DGG), including baseline RD as a confounding factor. A multifactorial ANOVA was performed to evaluate the inter-group difference between GT increase at 1 year and GRTs with GRTs as a covariate. A linear model was fitted to describe the relationship between pain killer consumption (in mg) and surgical time.

ðBaseline RDÞ � ð12-month RDÞ � 100 ðBaseline RDÞ

Results

after the surgery, patients were recalled for a control visit and for the postoperative course evaluation. Fourteen days after the surgical treatment, the sutures were removed. Plaque control in the surgically treated area was maintained by chlorhexidine rinsing for an additional 1 week after suture removal. After this period, patients were again instructed in mechanical tooth cleaning of the treated tooth using an ultra-soft toothbrush and a roll technique for 1 month. During this month, chlorhexidine rinsing was used twice a day. Then the patient started to use a softtoothbrush and chlorhexidine once a day for another month. All patients were recalled for prophylaxis 2 and 4 weeks after suture removal and, subsequently, once every 2 months until the final examination (12 months). Data analysis

One-way ANOVA was used to evaluate differences between the test and the control groups regarding the mean age, mean baseline values of RD, CAL, PD, KTH, GT and the mean surgical chairtime One-way ANOVA was also used to evaluate differences between the test and the control groups in PT, GRTs, GR width, GR length, depth of the withdrawal (WD) and residual soft tissue thickness (RTT) covering the palatal bone. General linear models were fitted relating pain killer consumption (in mg), discomfort (VAS), bleeding (VAS), inability to chew (VAS) and stress (VAS) to the surgical procedures and the centres as predictive factors, and the interaction between surgical procedures and centres. r 2010 John Wiley & Sons A/S

Following the initial oral hygiene phase as well as at the post-treatment examinations, all subjects showed low percentages of plaque harbouring tooth surfaces (FMPSo20%) and bleeding gingival units (FMBSo15%), indicating a good standard of supragingival plaque control during the study period.

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All 50 patients completed the study. In the control group, the mean age of the 25 patients (10 males and 15 females) was 32.2 � 7.2 years (range 20–40). Ten maxillary (six canines and four pre-molars) and 15 mandibular (six canines, seven pre-molars and two lateral incisor) teeth with gingival recession were treated. In the test group, the mean age of the 25 patients (12 males and 13 females) was 34.2 � 6.8 years (range 22–46). Twelve maxillary (six canines, one lateral incisor and five pre-molar) and 13 mandibular (seven canines and six premolars) teeth with gingival recession were treated. Intra-surgical measurements (Table 1)

The mean PT in the area of the withdrawal, in the control and test groups, were 3.1 � 0.47 mm (range 2–4.5 mm) and 3.06 � 0.46 mm (range 2–4 mm), respectively. The difference was not statistically significant (F 5 0.9, p 5 NS). In the control group, 12 grafts were taken from the pre-molar area (mean PT was 3.32 � 0.38 mm, range 3–4.5 mm) and the remaining 13 from the molar area (mean PT was 2.89 � 0.50 mm, range 2–3.5 mm). In the test group, 10 grafts were taken from the pre-molar area (mean PT was 3.2 � 0.53 mm; range 2.5–4 mm) and the remaining 15 from the molar area (mean PT was 2.96 � 0.32 mm; range 2.5–4 mm). In the control group, the mean thickness of the graft (GRT) immediately after being harvested was 1.34 � 0.26 mm (range 1–1.8 mm). After removing the fatty and glandular tissues, the thickness of the CTG, at the time of suturing (GRTs), was 0.88 � 0.17 mm (range 0.5–1.2 mm). The mean thickness of the primary flap was 0.72 � 0.13 mm (range 0.5–0.9 mm). The mean height of the CTG (GRH) was 6.16 � 0.89 mm (range 5–8 mm), while the

Table 1. Intra-surgical measurements Parameters (in mm)

Control group

PT GRT GRTs GRH GRW WD RTT

3.1 1.34 0.88 6.16 10.72 2.06 1.04

� � � � � � �

0.47 0.26 0.17 0.89 0.84 0.27 0.49

See text for abbreviations. Significance was obtained from one-way

ANOVA

Test group

� � � � � � �

0.9 0.8 1.5 0.2 1.3 132.2 25.6

NS NS NS NS NS o0.01 o0.01

3.06 1.32 0.83 6.28 10.96 1.32 1.73

0.46 0.16 0.12 0.97 0.37 0.16 0.47

statistical analysis.

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mean width (GRW) was 10.72 0.84 mm (range 9–12 mm). Complete closure of the palatal wound was accomplished in all patients. In the test group, the mean thickness of the epithelialized graft (GRT) was 1.32 0.16 mm (range 1–1.6 mm). The mean thickness of the graft after deepithelialization and removal of fatty tissue (GRTs) was 0.83 0.12 mm (range 0.6–1 mm). The mean GRH was 6.28 0.97 mm (range 5–8 mm), while the mean GRW was 10.96 0.37 mm (range 10–12 mm). No statistically significant difference was demonstrated between the test and the control groups in any of the considered dimensions of the CTG at the time of suturing: thickness (F 5 1.5), width (F 5 1.3) and height (F 5 0.2). The depth of the withdrawal (WD), corresponding to the sum between the thickness of the primary flap and the thickness of the graft immediately after being harvested (FT1GRT 5 2.06 0.27 mm) in the control group, and to the thickness of the epithelialized graft (GRT 5 1.32 0.16 mm) in the test group, was statistically greater in the control group (F 5 132.2, po0.01). In contrast, the difference between PT and WD, that is the RTT covering the palatal bone, was statistically lower in the control group (F 5 25.6, po0.01). These data indicated that, in the control group, a greater depth was reached in the palate and a lower soft tissue thickness covering the bone was left during the harvesting procedure. Surgical chair time

The overall surgical chair-time was significantly shorter for the test group. In particular, the average time needed for performing the CAF with DGG was 35.8 3.4 min. (range 30–42 min.), while the mean time for completing the CAF with CTG was 45.0 4.3 min. (range 38–55 min.). The difference was statistically significant (F 5 63.8, po0.01). Surgical time was significantly correlated with pain killer consumption (in mg) (F 5 11.9; po0.01; correlation coefficient 0.44): analgesic consumption increased on increasing the time needed to complete the surgery. Patient morbidity (Table 2)

Healing was uneventful for all test patients. In seven (28%) control patients, a dehiscence/necrosis of the

Table 2. Post-operative morbidity Parameters

Control group

Pain killer (in mg) Discomfort (VAS) Bleeding (VAS) Inability to chew (VAS) Stress (VAS)

2016 2.65 2.9 1.95 2.1

Test group

1896.4 2.18 2.12 1.87 1.25

1656 3.1 3.65 3.85 4.5

1532.2 1.99 1.89 2.0 1.53

0.5 0.1 1.2 9.1 29.5

NS NS NS o0.01 o0.1

See text for abbreviations. Significance was obtained from General linear model statistical analysis.

primary palatal flap occurred during the first healing period (7 days). The mean pain killer consumption (in addition to the 600 mg ibuprofen given before the surgery) in the control and the test groups was 2016 1896.4 mg (range 0–5400 mg) and 1656 1532.2 mg (range 0–4200 mg), respectively. The difference was not statistically significant (F 5 0.5, p 5 NS). A separate analysis demonstrated statistically greater analgesic consumption in the seven patients experiencing primary flap dehiscence/ necrosis (4028.5 828.8 mg) than test patients with secondary intention palatal healing and control patients (1233.3 1587, 8 mg) with primary intention palatal wound healing (F 5 9.3, po0.01). In contrast, the difference in analgesic consumption between the test patients and the control patients experiencing primary intention wound healing was not statistically significant. A general linear statistical model was fitted relating analgesic consumption to GRW, GRH, area (molar versus premolar) of the withdrawal and to the RTT covering the palatal bone. The R2 statistic indicates that the model as fitted is highly significant and explains 54.9% of the variability in analgesic consumption. A significant relationship was found regarding RTT (F 5 14.5, po0.01), GRH (F 5 23.1, po0.01) but not regarding the area of the withdrawal (F 5 1.3, p 5 NS) and the GRW (F 5 1.1, p 5 NS). Pain killer consumption increased with increasing height of the withdrawal and by reducing the thickness of the soft tissue still covering the palatal bone. Very limited post-operative morbidity was reported by both patient groups. No statistically significant difference was demonstrated between the control and the test patients in terms of postoperative discomfort, (F 5 0.1, p 5 NS) and bleeding (F 5 1.2, p 5 NS)-related VAS values. Statistically significant better results in terms of post-operative inability to chew (F 5 9.1, po0.01)- and stress

(F 5 29.5, po0.01)-related VAS values were demonstrated in the control compared with the test patients. Clinical parameters

The descriptive statistics for the clinical parameters measured at baseline and 12 months after surgery for both groups, as well as the mean differences within and between groups, are shown in Table 3. At baseline, there were no statistically significant differences between the two groups for any of the considered clinical parameters, indicating that the randomization process had been effective. In the control group, the mean RD was 3.4 0.86 (range 2–5 mm) and the mean GT was 0.71 0.15. In the test group, the mean RD and GT were 3.56 0.86 (range 2–5 mm) and 0.75 0.15, respectively. One-year clinical outcome

RD The results of fitting a general linear statistical model relating RD to techniques, time and the interaction between techniques and time showed a high R2 statistic, indicating that the model as fitted is highly significant and explains 95.5% of the variability. A significant relationship was found regarding time (baseline versus 1 year) (F 5 904.9, po0.01) in both groups, but not regarding the techniques (F 5 2.21, p 5 NS). No statistically significant difference was demonstrated in the amount of root coverage (in mm) between the two bilaminar procedures. The percentage of root coverage amounted to 96.2 8.93% in the test group and to 92.28 13.06% in the control group. Complete root coverage was achieved in 21 (84%) of the test and in 18 of the control (72%) treated defects. The results of fitting a logistic regression model, including baseline RD as a confounding factor, showed no r 2010 John Wiley & Sons A/S

Patient morbidity and root coverage outcome after grafts Table 3. Clinical parameters (mean SD) at baseline and 12 months post-surgery Parameter (in mm) RD Baseline 12 months Difference CAL Baseline 12 months Difference PD Baseline 12 months Difference KTH Baseline 12 months Difference GT Baseline 12 months Difference

Control group (n 5 25)

Test group (n 5 25)

3.4 0.86 0.32 0.55 3.08 0.70

3.56 0.86 0.16 0.37 3.4 0.81

4.52 0.87 1.56 0.65 2.96 0.78

4.72 0.84 1.52 0.58 3.2 0.91

1.12 0.33 1.24 0.43 0.12 0.43

1.16 0.37 1.36 0.48 0.2 0.5

1.36 0.48 3.28 0.54 1.92 0.49

1.52 0.50 3.64 0.48 2.12 0.52

0,71 0.15 1.32 0.22 0.61 0.16

0.75 0.15 1.55 0.21 0.80 0.17

See text for abbreviations.

significant difference (w2 2.2, p 5 NS) between the procedures.

CAL The results of fitting a general linear statistical model relating CAL to techniques, time and the interaction between techniques and time showed a high R2 statistic, indicating that the model as fitted is significant and explains 94% of the variability. A significant relationship was found regarding time (baseline versus 1 year) (F 5 651.2, po0.01) in both groups, but not regarding the techniques (F 5 0.99, p 5 NS). No statistically significant difference was demonstrated in the amount of CAL gain between the two bilaminar procedures.

PD The results of fitting a general linear statistical model relating PD to techniques, time and the interaction between techniques and time showed a high R2 statistic, indicating that the model as fitted is significant and explains 68.9% of the variability. A significant relationship was found regarding time (baseline versus 1 year) (F 5 5.77, po0.05) in both groups, but not regarding the techniques (F 5 0.36, p 5 NS).

KTH The results of fitting a general linear statistical model relating KTH to techr 2010 John Wiley & Sons A/S

niques, time and the interaction between techniques and time showed a high R2 statistic, indicating that the model as fitted is significant and explains 95% of the variability. A significant relationship was found regarding time (baseline versus 1 year) (F 5 784.5, po0.01) in both groups, but not regarding the techniques (F 5 1.92, p 5 NS). No statistically significant difference was demonstrated in the increase in KTH between the two bilaminar procedures.

GT The results of fitting a general linear statistical model relating GT to techniques, time and the interaction between techniques and time showed statistically significant differences considering both time (F 5 915.7, po0.01) (baseline versus 1 year) and the interaction between techniques and time (F 5 16.2, po0.01). A greater increase in GT was observed in the test compared with the control group. The difference between GT increase at 1 year and graft thickness at the time of suturing was statistically significant (F 5 56.6, po0.01) between the two groups independent of the thickness of the graft at the time of suturing.

Discussion

Sub-epithelium CTG is the most effective and predictable root coverage surgical procedure for the treatment of

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gingival recession (Roccuzzo et al. 2002, Cairo et al. 2008). CTG harvesting techniques are widely recommended so as not to expose patients to the more painful post-operative course associated with secondary intention palatal wound healing (Farnoush 1978, Jahnke et al. 1993, Del Pizzo et al. 2002, Griffin et al. 2006, Wessel & Tatakis 2008). Nevertheless, before performing a CTG harvesting technique, it is mandatory to evaluate the palatal anatomic characteristics and in particular the thickness of the palatal fibromucosa avoiding useless or even harmful surgical procedures. The primary access flap must include both epithelium and connective tissue that is critical for its viability. In some clinical situations, there is not enough connective tissue thickness for both the primary flap and the graft. Based on the clinical experience of the authors, this is true in the palatal pre-molar area of most of the patients, where, under a thin layer of connective tissue, there is a thick area of fatty and glandular tissue, as well as in the molar area of a few patients, where the entire palatal fibromucosa is not thick enough for obtaining a double layer (one for the flap and one for the graft) of connective tissue. In these situations, if the primary access flap is of a proper thickness, there is no connective tissue left for performing the graft. The risk lies in the incorporation of fatty and glandular tissue, inadequate for root coverage, instead of the connective tissue in the buccal aspect of teeth affected by gingival recession. Sullivan & Atkins (1968) emphasized the importance of removing all fatty tissue included in the graft that ‘‘could function as a barrier both to diffusion and vascularization’’. On the other hand, if the primary flap is too thin, it consists only or prevalently of epithelium and might result in necrosis/dehiscence during the first healing phase. As a result, the palatal wound heals by secondary intention. This eventful outcome was reported frequently in the literature when the trap-door approach was used as the CTG harvesting technique (Edel 1974, Broome & Taggart 1976, Jahnke et al. 1993, Harris 1997, Del Pizzo et al. 2002). The present study demonstrated a statistically significant greater analgesic consumption in the seven patients (28%) experiencing primary flap dehiscence/necrosis, with respect to test patients healed by secondary intention and control patients healed by primary intention. This is in

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line with the opinion of several authors that indicated the sloughing of the primary flap as the main cause of marked post-operative discomfort following a trap-door approach (Edel 1974, Jahnke et al. 1993) and with the study by Harris (1997), which reported an association between extensive flap necrosis and post-operative pain. More specifically, the data of the present study indicated more analgesic intake by patients during secondary intention palatal wound healing as a result of flap necrosis/dehiscence than when it is the result of the withdrawal of an epithelialized graft. The reasons for this difference are unknown; it can be speculated that the more painful post-operative course might derive from sovra infection of the wound favoured by tissue necrosis and/or from the greater depth reached during the harvesting technique. In fact, when a CTG harvesting technique is performed, because some connective tissue has to be left to maintain the vitality of the primary flap, it is necessary to extend the dissection deeper into the palatal soft tissues. The critical role of the depth of the withdrawal and in particular of the difference between PT and the depth of the withdrawal in influencing postoperative pain was one of the main results of the present study. The present study demonstrated that the RTT covering the palatal bone was negatively correlated with pain killer consumption. These data were statistically significant considering both the entire patient sample and the single treatment groups. In other words, patient analgesic consumption was greater in those patients in whom lower soft tissue thickness covering the bone was left during the harvesting procedure. Specifically, all patients consuming more than three analgesic tablets throughout the post-operative week had o2 mm thickness of soft tissue covering the palatal bone after the harvesting procedure. It can be suggested that when 2 mm or more of soft tissue thickness can be left to cover the palatal bone, CTG harvesting techniques are preferred because primary intention wound healing results in very limited pain and a better post-operative course in terms of patient stress and ability to chew. Otherwise, if palatal soft tissue is not thick enough, connective tissue harvesting techniques are not recommended because of the risk of primary flap necrosis and/or the inadequacy of the

graft due to the presence of fatty and glandular tissues instead of connective tissue. In this situation, harvesting an FGG that is subsequently de-epithelialized with the use of the blade is recommended. When a FGG is harvested, a lower thickness of palatal fibromucosa is required to obtain both an adequate connective tissue graft and a residual thickness of soft tissue covering the bone. With the use of the blade, in fact, it is possible to clinically check (based on the difference in light reflection and tissue consistency) the removal of the epithelium and thus the most superficial connective tissue can be utilized in the graft. This approach allows for incorporating into the graft the portion of connective tissue closer to the epithelium. This tissue is denser, firmer, more stable and presumably more suitable for root coverage purpose (Harris 2003). This was confirmed by the present study data, which demonstrated a greater increase in GT at the buccal aspect of the test-treated patients despite the fact that no difference was found in the thickness of the graft at the time of suturing between the two treatment groups. Furthermore, the difference between GT increase at 1 year and graft thickness at the time of suturing was statistically significant (F 5 56.6, po0.01) between the two groups, indicating that in the test group, almost the entire thickness of the graft became buccal GT at 1 year, while in the control group, a significant part of the graft thickness was lost during the healing period. It can be speculated that differences in the quality of the connective tissue between the two treatment groups were responsible for the different performance of the grafts during the healing phase. A negative aspect of the adopted de-epithelialization technique could be the remnant of some epithelium in the graft. However, the inclusion of some epithelium did not seem to affect the clinical results in terms of root coverage (Harris 2003). The negative aspect of the epithelialized graft harvesting technique was reported to be the less favourable and more painful patientâ&#x20AC;&#x2122;s post-operative course due to the secondary intention palatal wound healing (Farnoush 1978, Jahnke et al. 1993, Del Pizzo et al. 2002, Griffin et al. 2006, Wessel & Tatakis 2008). This does not seem to be confirmed by the present data. This study in fact failed to demonstrate any increase

in terms of post-operative pain, discomfort and bleeding in patients subjected to the epithelialized graft harvesting procedure compared with patients undergoing the connective tissue harvesting technique. Furthermore, no statistically significant difference in pain killer consumption was demonstrated between control patients experiencing primary intention wound healing (thus excluding those with necrosis/dehiscence of the primary flap) and test patients healing by secondary intention. The reasons for the difference can only be speculated on; a possible explanation can be found in the surgical techniques and in particular in the dimensions of the graft or in the protection of the wound area with equine-derived collagen in the test group. In the studies comparing patientsâ&#x20AC;&#x2122; postoperative outcomes after different graftharvesting procedures (Farnoush 1978, Jahnke et al. 1993, Del pizzo et al. 2002, Griffin et al. 2006, Yen et al. 2007, Wessel & Tatakis 2008), no data are available on the thickness and height of the FGG. However, in some of these studies (Griffin et al. 2006, Yen et al. 2007) a periosteum elevator was used to free the graft from the underlying bone and the graft was extended apical to the buccal bone crest. It is conceivable that in the present study, shallower (in the apicalâ&#x20AC;&#x201C;coronal dimension) and thinner FGG were harvested. The present study data demonstrated that the height and depth of the withdrawal and not the type (primary versus secondary) of palatal wound healing influence post-operative analgesic consumption. It can be speculated that in the studies reported in the literature, the more painful postoperative course in patients experiencing FGG procedures might be due to the greater height of the graft as well as the greater depth reached in the palatal soft tissue during the harvesting technique and not (or not only) due to the different type (primary or secondary) of palatal wound healing. A possible explanation is that by inserting the blade into the depth of the palatal soft tissue and/or towards the palatal vault (height of the withdrawal), the probability of severing a largesized nerve/vessel increases, causing greater pain. In addition, it cannot be excluded that the limited patient morbidity in the test group of the present study can be ascribed to the protection of the secondary intention wound area with an equine-derived collagen matrix, which could have minimized post-operative discomfort and bleeding (Farnoush 1978, r 2010 John Wiley & Sons A/S

Patient morbidity and root coverage outcome after grafts Saroff et al. 1982). Nevertheless, Wessel & Tatakis (2008), despite using palatal stents to protect free gingival graft donor sites, reported a greater incidence of donor site pain compared with CTG. Finally, a lack of statistical significance between groups in a trial designed to demonstrate superiority does not mean that equivalence exists between the two treatment techniques Gunsolley et al. 1998). In the present data, the lack of significance between the two groups might be due to the great within-group variability, which would have required a larger then expected sample size. A study, with a larger number of patients, is ongoing to confirm the present data. Another finding of the present study was the statistically significant longer mean surgical chair time in patients undergoing the bilaminar procedure with the trap-door harvesting technique. Because the duration of the surgical grafting procedure has been correlated with post-surgical pain in both the present and the previous studies (Griffin et al. 2006, Cortellini et al. 2009), this might have contributed to balance pain killer consumption between the two patient groups. In other words, it can be hypothesized that longer surgical time and lower soft tissue thickness covering the bone in the trap-door control group might have balanced the secondary intention wound healing experienced by the test group in terms of post-operative pain suffered by the patients. The increased time to complete the CAF with CTG can be explained by the additional time required to harvest the graft (in particular, in dissecting the split thickness primary access flap) and to perform multiple interrupted sutures to achieve complete closure of the palatal wound. Better results in terms of post-operative ability to chew and patient stress were demonstrated in patients subjected to the CTG harvesting technique. A possible explanation is that the open palatal wound may render the patient more anxious; hence, he/she avoids chewing for fear of jeopardizing wound healing. It is surprising that the difference in stress and ability to chew is significant also including control patients experiencing dehiscence/necrosis of the primary flap. It can be speculated that the presence of soft tissue closing the donor site, at least in first post-operative day/s, could minimize patient stress and help forget the presence of the wound palatal area. Neverr 2010 John Wiley & Sons A/S

theless, this seems to be in contrast with the increased intake of anti-inflammatory drags in the patients with a failing trap-door approach. This rather controversial issue was also reported by Del Pizzo et al. (2002), and further studies are needed to clarify it. The results of this study also indicated that both types of CTG can be successfully used under a CAF to cover gingival recession, with no statistically significant difference between them. One year post-treatment, 91.6% of the control gingival defects and 96.5% of the test gingival recessions were covered with the soft tissue. Furthermore, complete root coverage was achieved in 70% of the control and 85% of the test treated cases. The only statistically significant difference in the clinical outcomes between the two treatment groups of the present study was the greater increase in the GT in the patients treated with the de-epithelialized graft. Any attempt to explain this difference is speculative in nature, but it might be related to the quality (better stability and less shrinkage) of the connective tissue resulting from the de-epithelialization of a free gingival graft with respect to that harvested with the trap-door approach.

Conclusions

No difference in post-operative analgesic consumption, discomfort and bleeding was demonstrated in patients subjected to CTG or epithelialized graft-harvesting techniques. However, the lack of difference could be ascribed by the considerable within-group variability. Studies with a larger number of patients are needed to confirm the present data. Better results in terms of post-operative stress and ability to chew were demonstrated in patients undergoing the CTG harvesting technique. Secondary intention palatal wound healing due to dehiscence/necrosis of the primary flap was associated with greater consumption of analgesics. Pain killer consumption increased with increasing height of the withdrawal and decreasing RTT covering the palatal bone. Both types of grafts were effective in root coverage and clinical attachment gain when associated with a CAF for the treatment of gingival recession.

737

A greater increase in GT was achieved in the test patients; this may be due to the better post-operative stability of connective tissue resulting from the de-epithelialization of free gingival grafts.

References American Academy of Periodontology. (2001) Glossary of Periodontal Terms, 4th edition, p. 23. Boston: American Academy of Periodontology. Broome, W. C. & Taggart, E. J. (1976) Free autogenous connective tissue grafting. Report of two cases. Journal of Periodontology 47, 580–585. Cairo, F., Pagliaro, U. & Nieri, M. (2008) Treatment of gingival recession with coronally advanced flap procedures. A systematic review. Journal of Clinical Periodontology 35, 141–167. Cortellini, P., Tonetti, M., Baldi, C., Francetti, L., Rasperini, G., Rotundo, R., Nieri, M., Franceschi, D., Labriola, A. & Prato, G. P. (2009) Does placement of a connective tissue graft improve the outcomes of coronally advanced flap for coverage of single gingival recessions in upper anterior teeth? A multicentre, randomized, double-blind, clinical trial. Journal of Clinical Periodontology 36, 68–79. Cortellini, P., Tonetti, M. S., Lang, N. P., Suvan, J. E., Zucchelli, G., Vangsted, T., Silvestri, M., Rossi, R., McClain, P., Fonzar, A., Dubravec, D. & Adriaens, P. (2001) The simplified papilla preservation flap in the regenerative treatment of deep intrabony defects: clinical outcomes and postoperative morbidity. Journal of Periodontology 72, 1702–1712. da Silva, R. C., Joly, J. C., de Lima, A. F. & Tatakis, D. N. (2004) Root coverage using the coronally positioned flap with or without a subepithelial connective tissue graft. Journal of Periodontology 75, 413–419. Del Pizzo, M., Modica, F., Bethaz, N., Priotto, P. & Romagnoli, R. (2002) The connective tissue graft: a comparative clinical evaluation of wound healing at the palatal donor site. Journal of Clinical Periodontology 29, 848– 854. Edel, A. (1974) Clinical evaluation of free connective tissue grafts used to increase the width of keratinised gingival. Journal of Clinical Periodontology 1, 185–196. Eger, T., Mu¨ller, H. P. & Heinecke, A. (1996) Ultrasonic determination of gingival thickness. Subject variation and influence of tooth type and clinical features. Journal of Clinical Periodontology 23, 839–845. Farnoush, A. (1978) Techniques of protection and coverage of the donor sites in free soft tissue graft. Journal of Periodontology 49, 403–405. Griffin, T. J., Cheung, W. S., Zavras, A. I. & Damoulis, P. D. (2006) Postoperative com-

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plications following gingival augmentation procedures. Journal of Periodontology 77, 2070–2079. Gunsolley, J. C., Elswick, R. K. & Davenport, J. M. (1998) Equivalence, superiority, and negative clinical trials. Journal of Periodontology 69, 521–527. Harris, R. J. (1997) A comparison of two techniques for obtaining o connective tissue graft from the palate. The International Journal of Periodontics and Restorative Dentistry 17, 261–271. Harris, R. J. (2003) Histologic evaluation of connective tissue graft in humans. The International Journal of Periodontics and Restorative Dentistry 23, 575–583. Hu¨rzeler, M. B. & Weng, D. (1999) A singleincision technique to harvest subepithelial connective tissue grafts from the palate. The International Journal of Periodontics and Restorative Dentistry 19, 279–287. Jahnke, P. V., Sandifer, J. B., Gher, M. E., Gray, J. L. & Richardson, A. C. (1993) Thick free gingival and connective tissue autografts for root coverage. Journal of Periodontology 64, 315–322. Joly, J. C., Carvalho, A. M., da Silva, R. C., Ciotti, D. L. & Cury, P. R. (2007) Root coverage in isolated gingival recessions using autograft versus allograft: a pilot study. Journal of Periodontology 78, 1017–1022. Langer, B. & Langer, L. (1985) Subepithelial connective tissue graft technique for root coverage. Journal of Periodontology 56, 715–720. Lorenzana, E. R. & Allen, E. P. (2000) The single-incision palatal harvest technique: a strategy for aesthetics and patient comfort. The International Journal of Periodontics and Restorative Dentistry 20, 297–305.

Clinical Relevance

Scientific rationale for the study: Randomized studies comparing both patient morbidity and root coverage outcomes after the use of CTG and DGG for the treatment of gingival recessions are currently not available Principal findings: This study indicated no difference in post-operative

Mu¨ller, H. P., Schaller, N. & Eger, T. (1999) Ultrasonic determination of thickness of masticatory mucosa: a methodologic study. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 88, 248– 253. Mu¨ller, H. P., Schaller, N., Eger, T. & Heinecke, A. (2000) Thickness of masticatory mucosa. Journal of Clinical Periodontology 27, 431–36. O’Leary, T. J., Drake, R. B. & Naylor, J. E. (1972) The plaque control record. Journal of Periodontology 43, 38. Paoloantonio, M., Dolci, M., Esposito, P., Darchivio, D., Lisanti, L., Di Luccio, A. & Perinetti, G. (2002) Subpedicle acellular dermal matrix graft and autogenous connective tissue graft in the treatment of gingival recessions: a comparative 1-year clinical study. Journal of Periodontology 73, 1299– 1307. Roccuzzo, M., Bunino, M., Needleman, I. & Sanz, M. (2002) Periodontal plastic surgery for treatment of localized gingival recessions: a systematic review. Journal of Clinical Periodontology 29, 178–194. Sanz, M., Lorenzo, R., Aranda, J. J., Martin, C. & Orsini, M. (2009) Clinical evaluation of a new collagen matrix (Mucografts prototype) to enhance the width of keratinized tissue in patients with fixed prosthetic restorations: a randomized prospective clinical trial. Journal of Clinical Periodontology 36, 868–876. Saroff, S. A., Chasens, A. I., Eisen, S. F. & Levey, S. H. (1982) Free soft tissue autografts. Hemostasis and protection of the palatal donor site with a microfibrillar collagen preparation. Journal of Periodontology 53, 425–428.

Studer, S. P., Allen, E. P., Rees, T. C. & Kouba A, . (1997) The thickness of masticatory mucosa in the human hard palate and tuberosity as potential donor sites for ridge augmentation procedures. Journal of Periodontology 68, 145–151. Sullivan, H. C. & Atkins, J. H. (1968) Free autogenous gingival grafts. I. Principles of successful grafting. Periodontics 6, 121–129. Wessel, J. R. & Tatakis, D. N. (2008) Patient outcomes following subepithelial connective tissue graft and free gingival graft procedures. Journal of Periodontology 79, 425– 430. Yen, C. A., Griffin, T. J., Cheung, W. S. & Chen, J. (2007) Effects of platelet concentrate on palatal wound healing after connective tissue graft harvesting. Journal of Periodontology 78, 601–610. Zucchelli, G., Amore, C., Sforza, N. M., Montebugnoli, L. & De Sanctis, M. (2003) Bilaminar techniques for the treatment of recession type defects. A comparative clinical study. Journal of Clinical Periodontology 30, 862–870. Zucchelli, G., Clauser, C., De Sanctis, M. & Calandriello, M. (1998) Mucogingival versus GTR procedures in the treatment of deep recession type defects. Journal of Periodontolology 69, 139–145.

pain, discomfort and bleeding between the two groups. Lower stress and better ability to chew were demonstrated in the CTG group. Pain increased with increasing height and depth of the withdrawal and in the case of necrosis of the primary palatal flap. A greater

increase in buccal soft tissue thickness was achieved in the DGG group. Practical implications: In sites with thick palatal fibromucosa, a trap-door approach is more patient friendly, while with thin palatal tissues, there is a greater risk of a failure of the trap-door, thereby indicating a DGG.

Address: Giovanni Zucchelli Dipartimento di Scienze Odontostomatologiche University of Bologna Via S. Vitale 59, 40125 Bologna Italy E-mail: giovanni.zucchelli@unibo.it

r 2010 John Wiley & Sons A/S

The International Journal of Periodontics & Restorative Dentistry

Esthetic Treatment of Peri-implant Soft Tissue Defects: A Case Report of a Modified Surgical–Prosthetic Approach

Giovanni Zucchelli1, /Claudio Mazzotti1, /Ilham Mounssif1, /Matteo Marzadori1, /Martina Stefanini1 [Au: Please provide academic degrees for all authors, eg, DDS, MD, PhD, DMD, etc] A major concern from the esthetic point of view is soft tissue defects around implant restorations that often result in a too long prosthetic crown. This report describes a modified prosthetic–surgical approach for the treatment of peri-implant horizontal and vertical soft tissue defects in an esthetically demanding patient. One month before surgery, the implant crown restoration was removed, the preexisting implant abutment was reduced, and a short temporary crown, at the level of the homologous controlateral incisor, was applied. A bilaminar technique, consisting in an envelope coronally advanced flap covering two connective tissue grafts was used to treat the soft tissue defects around the implant site. Four months after surgery, a new implant abutment and temporary crown were applied for soft tissue conditioning before the final impression. Nine months after surgery, the peri-implant soft tissue margin was 4 mm more coronal compared with baseline and at the same soft tissue margin level of the right central incisor. A 2.2-mm increase in buccal soft tissue thickness measured 1.5 mm apical to the soft tissue margin was accomplished. The emergence profile of the replaced tooth faithfully reproduced that of the healthy homologous controlateral central incisor. Two years after surgery, the soft tissue margin was stable and the esthetic appearance of the implant site was well maintained. This report demonstrates the possibility of fully correcting severe vertical and horizontal peri-implant soft tissue defects and achieving high patient satisfaction through a combined mucogingival and prosthetic treatment. (Int J Periodontics Restorative Dent 2013;33:XXX–XXX.)

Department of Odontostomatology, Bologna University, Bologna, Italy. [Au: Please provide titles for all authors at Bologna University, eg, Professor, Lecurer, Researcher, etc.]

Correspondence to: Profesoor Giovanni Zucchelli, Department of Odontostomatology, Bologna University, Via S. Vitale 59, 40125 Bologna, Italy; fax: +39051225208; email: giovanni.zucchelli@unibo.it.

Implant restoration is a common practice for tooth loss rehabilitation in esthetic areas. The main goals are functionality and esthetics for patient satisfaction. The clinician chooses from a variety of surgical approaches such as immediate, early, or delayed implant placement.1,2 After tooth extraction, the hard and soft tissues undergo substantial changes as a result of healing.3 Many factors influence the soft tissue level around dental implants but only a handful have been studied: peri-implant biotype, height and width of the facial bone, orofacial position of the implant head.4,5 A major concern from an esthetic point of view are soft tissue defects around implant restorations, which often result in a extra long prosthetic crowns with disharmony of the marginal soft tissue scallop in respect to the adjacent teeth. The increased esthetic demands require peri-implant soft tissue color and contour in harmony with the neighboring teeth for patient satisfaction, thus, surgical reduction of the peri-implant soft tissue defect may be indicated. Results after surgical root coverage are well reported in the literature,6–9

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4 Fig 1a (left) Patient’s smile showing a “long” implant-supported crown on the maxillary left incisor. Fig 1b (right) Disharmony of the scalloping of the buccal gingival margin of the maxillary central incisors and buccal transparency of the underlying implant surface. Fig 1c (left) Presurgical emergence profile of implant-supported crown. Fig 1d (right) Radiograph showing implant’s proximity to the root of the maxillary left lateral incisor.

Fig 1e (left) Soft tissue margins and thin buccal keratinized tissue showing by transparency the underlying implant surface. Fig 1f (right) Occlusal view showing extremely thin soft tissue covering the buccally positioned implant.

unlike peri-implant soft tissue defect reduction. Recently, a case series reported successful coverage with a bilaminar technique of soft tissue dehiscence defects around single implant restorations with esthetically satisfactory outcomes.10 This case report describes a modified prosthetic–surgical approach for the treatment of peri-implant horizontal and vertical soft tissue defects in an esthetically demanding patient.

Clinical case A 33-year-old woman was referred to the Department of Oral Science of Bologna University, Bologna, Italy, for evaluation of a single implant supported crown at the maxillary left central incisor. Her chief complaint was the unesthetic appearance during smile (Fig 1a). The tooth was lost 18 months prior after failure of previous endodontic therapy and was treated with im-

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mediate implant placement after tooth extraction. The patient was very upset with the referring dentist who performed the implant therapy, but was very concerned about the treatment proposed by another oral surgeon consisting of implant removal, provisional partial denture, reconstructive bone surgery, and new implant and crown placement. The patient’s medical history revealed no systemic contraindications for dental treatment.

5 Clinical examination showed the disharmony in scalloping of the buccal gingival margin (Fig 1b) with the marginal soft tissue of the implant restoration in a more apical position (4 mm) with respect to the adjacent natural tooth. In addition, there was a horizontal soft tissue defect with an inadequate emergence profile of the implant crown (Fig 1c). The buccal soft tissue was so thin that transparency of the underlying implant surface was visible in the patientâ&#x20AC;&#x2122;s smile (Figs 1e and 1f). No interproximal attachment loss was present at the neighboring teeth. The overall periodontal examination showed no pathologic probing depths and low full mouth bleeding (7%) and plaque (8%) scores.11 Radiographic examination (Fig 1d) revealed that the implant head was located 5 mm apical to the cementoenamel junction (CEJ) of the adjacent incisors and no sign of peri-implant bone loss was present. The implant was very close to the lateral incisor with a great risk of damaging the supporting bone in case of implant extraction. The primary goal of treatment was to reduce the vertical soft tissue defect and eliminate the marginal soft tissue discrepancy between the implant restoration and the right central incisor to improve the esthetic appearance. The secondary goal was to increase buccal soft tissue thickness to mask the implant transparency and to give the implant-supported crown a correct emergence profile. The patient received a session of prophylaxis to remove microbial deposits with ultrasonic points, a rubber cup,

and polishing paste, including instructions on using a coronally directed roll technique to minimize toothbrushing trauma to the periimplant soft tissue margin.

Provisional prosthetic phase

The implant crown restoration was removed 1 month before surgery (Fig 2a) and the underlying zirconia abutment was milled and reduced (Fig 2b) to eliminate the shoulders/chamfers and diminish the abutment proclination, creating a conic shape and a vertical finishing line with respect to the soft tissue. The present abutment was therefore used as a provisional abutment to build a short provisional restorative crown and to leave the buccal and interdental soft tissues to fill the space previously occupied by the abutment shoulder/chamfers and implant crown (Fig 2c). The distance between soft tissue margin and head of the implant was 1.5 mm, measured after removal of the abutment with a manual probe (PCP-UNC 15 probe tip, Hu Friedy). The soft tissue thickness (0.6 mm as measured with an electronic gauge [Digital calliper C041 0â&#x20AC;&#x201C;150 mm, Kennon Instruments]) was determined 1.5 mm apical to the soft tissue margin with a short needle for anesthesia and a 3-mm diameter silicon disk.12 [Au: Correct?] The provisional restoration was performed with a similar shape and height to the adjacent right central incisor and fixed with provisionally cement.

Surgical procedure

The soft tissue defect was treated with a coronally advanced flap (CAF) (Fig 2c),13 with a connective tissue graft (CTG)10,14,15 on the buccal surface of the implant (Fig 2d). Following local anesthesia, a horizontal incision was made to design an envelope flap extending from the maxillary right to left canines. This opening consisted of oblique submarginal incisions in the interdental area directed toward the midline and passing through the interincisal papilla and intrasulcular incisions at the buccal aspect. The flap was raised with a split-fullsplit approach in the coronal-apical direction. Surgical papillae were dissected split-thickness up to the buccal bone crest, than the flap was elevated at full-thickness to expose at least 2 to 3 mm of buccal bone apical to the root exposures and to the bone dehiscence at the implant site. Finally, the most apical portion of the flap was elevated split-thickness to permit the coronal displacement of the flap. The remaining facial portion of the anatomical papillae was deepithelialized to create connective tissue beds to which the surgical papillae of the coronally advanced buccal flap were secured at time of suturing. The absence of a contact point and augmented interdental soft tissues between the implant abutment and the adjacent teeth allowed for extending the deepithelialization of the interdental papillae at the implant site occlusaly towards the palatal aspect. Two different CTG were harvested

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6 Fig 2a (left) Preexisting zirconia abutment after implant-supported crown removal. Fig 2b (right) One month before surgery the reduction of the abutment by elinimation of shoulders/chamfers was performed.

Fig 2c (left) Envelope flap and implant exposure; note the increase in width and volume of the interdental soft tissue between the abutment and adjacent teeth. Fig 2d (right) The two CTG are sutured: the coronal one to compensate for soft tissue loss around the implant site and the apical one to mask the colored implant exposure. Fig 2e (left) Evidence of the greater thickness of the coronal with respect to the apical CTG. Fig 2f (right) Sling sutures of the coronally advanced envelope flap; note the good fit between the surgical papillae of the flap and the underlying anatomical deepithelialized papillae at the implant site and at the neighboring teeth.

from the palate: the thicker coronal CTG was used to compensate the soft tissue defects and the thinner apical CTG was used to mask the colored and buccaly exposed implant surface (Figs 2d and 2e). Both grafts were derived from the de-epithelialization with the knife blade of two mesial-distal adjacent palatal free gingival grafts.12 This technique was chosen with respect to the other connective tissue graft harvesting procedures16–19 because the palatal fibromucosa was not thick enough for both the primary access flap and the connective tis-

sue graft. Two adjacent grafts were harvested to minimize the patient’s postoperative pain and discomfort. A recent study12 demonstrated that patient postoperative pain and discomfort were correlated with harvesting depth and height (apical-coronal dimension) and not with the width (mesialdistal dimension) of the withdrawal. The mesiodistal length of the coronal CTG was 6 mm greater than the width of the implant abutment, the apico-coronal dimension was 6 mm and the thickness was 1.8 mm as measured with an electronic gauge. This CTG

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was positioned over the implant abutment surface 1 mm apical to the CEJ of the central incisor and sutured at the base of the anatomical papillae with two resorbable interrupted sutures. The apical CTG (8 mm wide, 4 mm high, and 1.0 mm thick) was positioned above the colored implant surface and secured with interrupted resorbable sutures anchored to the adjacent periosteum. Coronal advancement of the buccal flap was obtained by means of two split-thickness incisions: one “deep,” cutting the muscle insertions on the perios-

7 tium, and the other â&#x20AC;&#x153;superficial,â&#x20AC;? detaching the muscle inserting into the inner aspect of the mucosa lining of the flap. Flap mobilization was considered adequate when the soft tissue margin was able to passively reach a level coronal to the CEJ at all teeth included in the flap design without tension. At the implant site, care was taken to achieve passive superimposition between the surgical papillae of the flap and the occlusaly deepithelialized papillae mesial and distal to the implant abutment. The flap was anchored in a coronal position with sling sutures (6/0 PGA, Stoma) (Fig 2f). These sutures were also used to anchor the surgical papillae to the corresponding deepithelialized anatomical papillae for a precise adaptation of the keratinized tissue margin flap on the crowns and implant abutment. At the end of surgery, the provisional prosthetic crown was reduced to avoid contact with the soft tissue and fixed with provisional cement. Two weeks later, the sutures were removed. The patient was instructed not to brush in the treated area, but to rinse for 1 minute with a 0.12% chlorhexidine solution three times a day. After suture removal, plaque control in the surgically treated area was maintained by rinsing with chlorhexidine for an additional 2 weeks. The patient was instructed in mechanical tooth cleaning using an ultrasoft toothbrush for 1 month and told to rinse with chlorhexidine twice a day. After, the patient was instructed to use a soft toothbrush and rinse with chlorhexidine once a day for an-

other month. When chlorhexidine was discontinued, full mechanical interproximal cleaning was reinstituted. The patient was recalled for prophylaxis once a month until the definitive restoration was delivered.

Change of the abutment and provisional crown

Four months after surgery (Fig 3a), the modified abutment was replaced with a new zirconia abutment. The increased size of the subgingival portion of the abutment, due to the presence of shoulders/chamfers, compressed the soft tissue between the implant abutment and the adjacent teeth and provided a horizontal finishing line for the new provisional prosthetic crown built with a shape similiar to the homologous controlateral central incisor. The change in the crown emergence profiles together with the restored contact points contributed to soft tissue conditioning and growth of interdental papillae.

Final prosthetic phase

Nine months after surgery, a final impression was made and the resulting cast used for definitive crown design. A lithium disilicate restoration was used to rehabilitate the implant (Fig 3d) with the same shape of the right central incisor and a correct emergence profile with respect to the new soft tissue height and shape (Fig 3f).

Results At time of definitive impression, the distance between the soft tissue margin and head of the implant was 5 mm (Fig 3b). A comparison between baseline and the 9-month follow-up showed a periimplant soft tissue margin 4 mm more coronal, at the same level of the soft tissue margin of the right central incisor. The soft tissue thickness (Fig 3c) was 2.8 mm. Thus, a 2.2 mm increase in buccal soft tissue thickness was accomplished with the surgical procedure. The probing depth around the implantsupported crown was within the physiologic limit (< 4 mm) and no bleeding on probing was present. The color and height of the keratinized tissue of the implant was well integrated with the adjacent gingival tissue (Fig 3d). The peri-implant soft tissue scalloping was well harmonized with the adjacent gingival margin and no disalignment of the mucogingival junction was present. The emergence profile of the crown was easy to clean and reproduced faithfully the emergence of a natural tooth from its soft tissue (Fig 3f). The implant restoration had a natural appearance. The patient showed good compliance with low full-mouth plaque (4%) and bleeding scores (4%) and no pathologic probing depths. The patient was very satisfied with her new esthetic appearance. Two years after surgery (Fig 3e), the soft tissue margin was stable, the esthetic appearance at the implant site was well maintained, probing depths were physiologic (< 4 mm),

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8 Fig 3a (left) Four months postsurgery the soft tissue margin at the implant site is more coronal than the gingival margin of the homologous controlateral central incisor. The temporary crown was left â&#x20AC;&#x153;shortâ&#x20AC;? to not interfere with the healing process. Fig 3b (right) Nine months follow-up, 5mm transmucosal height was measured from the head of the implant to the soft tissue margin.

Fig 3c (left) Occlusal view showing the increase in buccal soft tissue thickness at the implant site. Fig 3d (right) One year postsurgery, the color and height of the keratinized tissue of the implant site is well integrated with the adjacent gingival tissue.

Fig 3e (left) Two years postsurgery the esthetic appearance of the implant site was maintained. Fig 3f (right) The emergence profile of the crown faithfully reproduced that of a natural tooth from its soft tissue.

and no signs of mucositis or perimplantitis were present.

Discussion Soft and hard tissue modifications are common after tooth extraction. Implant rehabilitation without soft/ hard tissue defect correction or prevention may result in poor esthetic satisfaction for patients. The bilaminar technique (CAF plus CTG) has been reported to be a suitable procedure to achieve highly pre-

dictable results in terms of complete root coverage.6,7 This patient was treated with a technique used in a recent pilot study10 where isolated peri-implant soft tissue dehiscences were covered, with results as succesfull as those reported for gingival recession treatment with the bilaminar technique. The procedure described in the present study completely solved the vertical and horizontal peri-implant soft tissue defects; in fact, at 9 months, the peri-implant soft tissue margin was at the same level as the gin-

The International Journal of Periodontics & Restorative Dentistry

gival margin of the homologous controlateral tooth and the increase in buccal soft tissue thickness allowed for masking of the implantâ&#x20AC;&#x2122;s transparency and restored a correct implant-supported crown emergence profile. Both graft type and flap design played a critical role in achieving this outcome. The CTGs used in this patient derived from the de-epithelialization of free gingival grafts.12 Advantages derived from this technique included more dense and stable connective tissue closer to the epithelium and less

a Fig 4

b Views at (a) baseline and (b) 2 years postsurgery.

prone to contraction, and closer to the bone that is rich in fatty and glandular tissue. The difference in the quality of the CTG could be particularly significant when thick grafts, such as those used to treat soft tissue defects around implants, are harvested. In a thick graft, the proportion of glandular and fatty tissue included increases with respect to the denser connective tissue closer to the epithelium that is left in the primary flap when harvesting techniques are performed. The stability of the CTG used in the present study was demonstrated by the increase in buccal soft tissue thickness that was larger than the thickness of the CTG at time of surgery, suggesting not only stability but a further thickness increase over time of de-epithelialized free gingival graft. The envelope flap design used in this report was similar to the coronally advanced flap for the treatment of multiple recession defects in the upper anterior teeth.13 Vertical releasing incisions may damage the blood supply to the

flap and often result in unpleasant visible white scars.20 The absence of vertical releasing incisions is even more important when the surgical papillae of the flap have to be shifted palatally as well as coronally to reach the de-epithelialized papillae between the implant abutment and the adjacent teeth. With such a palatal dislocation, vertical releasing incisions would have shifted mesially and farther from the adjacent firm soft tissues with a greater risk of damaging flap blood supply and inducing gingival defects at the adjacent teeth. Procuring a wide envelope flap free from deep (periosteal) and superficial (submucosal) muscle insertions allowed for the surgical papillae of the flap to passively reach the palatally shifted deepithelialized papillae neighboring the implant abutment, despite the presence of two CTG, with no damage to the flap or adjacent teeth. On the contrary gingival recessions present at the neighboring teeth, the implant could be corrected by means of a coronally advanced

flap. This led to a significant improvement in the overall esthetic appearance of the treated area with high patient satisfaction.

Conclusions The successful esthetic result achieved in the present case was associated with more than the surgical procedure. A great contribution was derived from the modifications of the prosthetic components performed before and after surgical intervention. Concerning the presurgical prosthetic phase, the removal of the implant crown together with reduction of the implant abutment provided wider interdental connective tissue beds between the implant abutment and the adjacent teeth for the graft and surgical papillae of the covering flap.10 In particular, the reduction of the abutment, performed 1 month before surgery, allowed for the interdental soft tissue to occupy the space previously in-

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10 habited by zirconia. This reduction increased the width and volume of the peri-implant soft tissues at time of surgery and improved the vascular exchange with the graft and the surgical papillae of the covering flap. The increased width of the papillae mesial and distal to the abutment and the possibility of occlusaly extending de-epithelialization toward the palatal aspect allowed for precise stabilization of the surgical papillae of the covering flap despite the coronal positioning of the CTG. The lack of graft exposure during healing on one side reduced graft resorption and shrinkage and on the other improved the esthetic outcome by avoiding the white scar appearance and disalignment of the mucogingival line typical of the free gingival graft posthealing. Besides, presurgical abutment modification by reducing abutment proclination may have contributed to minimizing the apical shift of the marginal soft tissue. Postsurgical (4 months) replacement of the implant abutment together with the new provisional crown played a critical role in conditioning interdental soft tissue and facilitating the growth of interdental papillae. Within the limits of a clinical case report, this study showed the possibility of fully correcting severe vertical and horizontal peri-implant soft tissue defects and achieving high patient satisfaction through combined mucogingival and prosthetic treatment; however, long-term maintenance of the successful outcome is not yet demonstrated.

Acknowledgment The authors reported no conflicts of interest related to this study.

References 1. Esposito M, Grusovin MG, Polyzos IP, Felice P, Worthington HV. Timing of implant placement after tooth extraction: Immediate, immediate-delayed or delayed implants? A Cochrane systematic review. Eur J Oral Implantol 2010;3:189–205. 2. Chen ST, Buser D. Clinical and esthetic outcomes of implants placed in postextraction sites. Int J Oral Maxillofac Implants 2009;24(suppl):186–217. 3. Tan WL, Wong TL, Wong MC, Lang NP. A systematic review of post-extractional alveolar hard and soft tissue dimensional changes in humans. Clin Oral Implants Res 2012;23(suppl 5):1–21. 4. Nisapakultorn K, Suphanantachat S, Silkosessak O, Rattanamongkolgul S. Factors affecting soft tissue level around anterior maxillary single-tooth implants. Clin Oral Implants Res 2010;21:662–670. 5. Sorni-Broker M, Penarrocha-Diago M, Penarrocha-Diago M. Factors that influence the position of the peri-implant soft tissues: A review. Med Oral Patol Oral Cir Bucal 2009;14:e475–e479. 6. Chambrone L, Sukekava F, Araujo MG, Pustiglioni FE, Chambrone LA, Lima LA. Root coverage procedures for the treatment of localised recession-type defects. Cochrane Database Syst Rev 2009: CD007161. 7. Cairo F, Pagliaro U, Nieri M. Treatment of gingival recession with coronally advanced flap procedures: A systematic review. J Clin Periodontol 2008;35:136–162. 8. Oates TW, Robinson M, Gunsolley JC. Surgical therapies for the treatment of gingival recession. A systematic review. Ann Periodontol 2003;8:303–320. 9. Roccuzzo M, Bunino M, Needleman I, Sanz M. Periodontal plastic surgery for treatment of localized gingival recessions: A systematic review. J Clin Periodontol 2002;29(suppl 3):178–194. 10. Zucchelli G, Mazzotti C, Mounssif I, Mele M, Stefanini M, Montebugnoli L. A novel surgical–prosthetic approach for soft tissue dehiscence coverage around single implant. Clin Oral Implants Res 2012 Aug 27, doi: 10.1111/clr.12003 [epub ahead of print].

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11. O’Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol 1972;43:38. 12. Zucchelli G, Mele M, Stefanini M, et al. Patient morbidity and root coverage outcome after subepithelial connective tissue and de-epithelialized grafts: A comparative randomized-controlled clinical trial. J Clin Periodontol 2010;37:728–738. 13. Zucchelli G, De Sanctis M. The coronally advanced flap for the treatment of multiple recession defects: A modified surgical approach for the upper anterior teeth. J Int Acad Periodontol 2007;9:96–103. 14. Zucchelli G, Amore C, Sforza NM, Montebugnoli L, De Sanctis M. Bilaminar techniques for the treatment of recessiontype defects. A comparative clinical study. J Clin Periodontol 2003;30:862–870. 15. Pini-Prato GP, Cairo F, Nieri M, Franceschi D, Rotundo R, Cortellini P. Coronally advanced flap versus connective tissue graft in the treatment of multiple gingival recessions: A split-mouth study with a 5-year follow-up. J Clin Periodontol 2010;37:644–650. 16. Edel A. Clinical evaluation of free connective tissue grafts used to increase the width of keratinised gingiva. J Clin Periodontol 1974;1:185–196. 17. Langer B, Langer L. Subepithelial connective tissue graft technique for root coverage. J Periodontol 1985;56:715–720. 18. Hurzeler MB, Weng D. A single-incision technique to harvest subepithelial connective tissue grafts from the palate. Int J Periodontics Restorative Dent 1999;19:279–287. 19. Lorenzana ER, Allen EP. The singleincision palatal harvest technique: A strategy for esthetics and patient comfort. Int J Periodontics Restorative Dent 2000;20:297–305. 20. Zucchelli G, Mele M, Mazzotti C, Marzadori M, Montebugnoli L, De Sanctis M. Coronally advanced flap with and without vertical releasing incisions for the treatment of multiple gingival recessions: A comparative controlled randomized clinical trial. J Periodontol 2009; 80:1083–1094.