JOP Perio OSA article

Investigating the Association BetweenObstructive Sleep Apnea and PeriodontitisWeiqiang Loke,* Thomas Girvan,† Paul Ingmundson,‡ Ronald Verrett,§ John Schoolfield,*and Brian L. Mealey*

Background: Obstructive sleep apnea (OSA) is a sleep dis-order characterized by disruptions of normal sleep archit-ecture. Chronic periodontitis is a chronic disease of theperiodontium that elicits a general inflammatory response tolocal dental plaque. It has been suggested that periodontal dis-ease may increase in severity with increasingly severe OSAbecause both disease entities share common inflammatorypathways, acting synergistically to alter the host response.The aim of this study is to analyze the association between se-verity of OSA and the prevalence/severity of periodontitis.

Methods: One hundred patients from a large veterans ad-ministration sleep study center (n = 26 normal, n = 21 mild,n = 19 moderate, n = 34 severe) diagnosed with an overnightpolysomnogram underwent a comprehensive periodontal ex-amination. Periodontal parameters measured included the fol-lowing: 1) mean periodontal probing depth (PD); 2) clinicalattachment level (CAL); 3) gingival recession; and 4) percent-age of sites with bleeding on probing, plaque, PD ‡5 mm, andCAL ‡3 mm.

Results: Seventy-three percent of the sampled populationhad moderate/severe periodontal disease. x2 analysesrevealed no significant differences in the prevalence of peri-odontal disease between the apnea–hypopnea index (AHI)groups, with a negligible Spearman correlation coefficient of0.246 between AHI severity and periodontal disease severitycategories. Analysis of covariance indicated a significant asso-ciation between AHI severity categories and percentage ofsites with plaque, after adjusting for age. Multivariable logis-tic regression analysis predicting moderate/severe peri-odontitis with AHI score, age, and smoking status indicateda significant association with age (P = 0.028) but no signifi-cant association with the other two predictors.

Conclusion: OSA was not significantly associated with theprevalence of moderate/severe periodontitis and the peri-odontal parameters examined, except percentage plaque.J Periodontol 2015;86:232-243.

KEY WORDS

Chronic periodontitis; sleep apnea, obstructive.

Obstructive sleep apnea (OSA) isa sleep disorder characterizedby periodic and repetitive par-

tial or complete collapse of the upperairway during sleep, resulting in reducedventilation (hypopnea) or absent venti-lation (apnea) and, consequently, disrup-tions of normal sleep architecture andassociated arterial desaturations.1,2 OSAis currently diagnosed with an overnightsleep diagnostic test known as a poly-somnogram (PSG), which remains thegold standard of diagnosis.3 The stan-dard definition of an apneic event in-cludes a minimum 10-second intervalbetween breaths, with a neurologic arousal,a blood oxygen desaturation of 3% to4% or greater, or both arousal and de-saturation.4-6 Hypopnea is defined asan episode of shallow breathing (air-flow reduced by ‡50%) during sleep,lasting for ‡10 seconds and usuallyassociated with a fall in blood oxygensaturation attributable to partial ob-struction of the upper airway.1

The apnea–hypopnea index (AHI)4 isa commonly used index to categorizethe severity of OSA, and it representsthe average number of apneas and/orhypopneas per hour of recorded sleep.In adults, an AHI of less than five eventsper hour is considered normal. MildOSA is defined as an AHI of at least fiveto 15 events per hour, moderate OSAas >15 to 30 events per hour, and se-vere OSA as >30 events per hour.

The underlying mechanisms of OSAare primarily associated with upper airway

* Department of Periodontics, University of Texas Health Science Center at San AntonioDental School, San Antonio, TX.

† Sleep Clinic, South Texas Veterans Health Care System, Veterans AdministrationFacility, San Antonio, TX.

‡ Dental Clinic, South Texas Veterans Health Care System, Veterans AdministrationFacility.

§ Department of Comprehensive Dentistry, University of Texas Health Science Center atSan Antonio Dental School.

doi: 10.1902/jop.2014.140229

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anatomy, dilator muscle dysfunction, lung volume,or ventilatory control stability.7 Ongoing studiesalso suggest other possible pathophysiology path-ways that include local and systemic inflammation8

and clock gene dysfunction.9 Neuropsychiatric com-plications associated with OSA include daytimesomnolence, cognitive dysfunction, depression, andAlzheimer’s disease.10-12 OSA has been associatedwith an increased risk for development of vasculardisorders, such as coronary heart disease, hyperten-sion, stroke, congestive cardiac failure, and ath-erosclerosis, as well as metabolic disorders, such asimpaired glucose tolerance and insulin resistance.11

Although the exact pathogenesis pathway of OSAleading to such complications is uncertain, studieshave suggested the role of OSA in activation ofvarious inflammatory processes through hypoxiaand oxidative stress-induced reperfusion injuryfrom intermittent hypoxia during apneic events inOSA.12,13 Currently, treatment for OSA is confinedto relief of the mechanical obstruction rather thanfocusing on the functional aspect of the disease.14

Better understanding of the underlying pathophys-iology may bring about new and novel treatmentstrategies in the future.15

The biofilm derived from dental plaque in peri-odontitis is capable of adding to pre-existing sys-temic inflammatory burden through elevation ofserum levels of C-reactive protein16 and a host ofother important inflammatory cytokines and medi-ators.17-19 The resultant inflammatory response fromperiodontitis coupled with genetic and environ-mental risk factors could potentiate any existinginflammatory disease. A pilot study performed byGunaratnam et al.20 found a higher prevalence ofperiodontitis among patients with OSA, suggestinga possible association between OSA and periodontitis.Because treatment of periodontitis has been shownto improve systemic inflammation, metabolic controlof glycemia, and parameters of vascular health,21,22

treatment of periodontitis may prove to be one ofthe future, novel ways to improve OSA.

Epidemiologically, data from several OSA stud-ies accomplished with PSG suggest that the prev-alence of OSA is between 5% and 28%,23-27 withhigher prevalence in males. Periodontitis is alsoa common chronic disease with a high prevalence.According to the most recent National Health andNutrition Examination Survey 2009 to 2010, 47% ofadults aged >30 years have chronic periodontitis(CP), distributed as a prevalence of 8.7%, 30%, and8.5% with mild, moderate, and severe forms of peri-odontitis, respectively.28

The aim of this study is to determine whetherOSA has any association with periodontitis. In par-ticular, the association between OSA severity and

the prevalence of periodontitis was investigated. Inaddition, the relations between OSA severity andvarious clinical parameters of periodontal diseasestatus were examined.

MATERIALS AND METHODS

This cross-sectional study was conducted fromJune 2012 to August 2013 after approval by theInstitutional Review Board of the University of TexasHealth Science Center and the South Texas VeteransHealth Care System, Veterans Administration (VA)facility, San Antonio, Texas (protocol no. HSC12-123H).All patients provided written informed consent be-fore participation. Patients (n = 100) were recruitedby purposive consecutive sampling from the pool ofpatients who were scheduled for PSGi evaluation6 atthe South Texas Veterans Health Care System facility,San Antonio, Texas. The participants included 91males and 9 females, aged 28 to 79 years; meanage: 52.6 years), with a final total of 26 individualsin the normal, 21 in the mild, 19 in the moderate,and 34 in the severe AHI groups examined. Addi-tional patient demographics are presented in Table1. The population sampled at the VA hospital hasa bias toward males, with males accounting for 91%of the data represented (Table 1). In terms of eth-nicity, the distribution surveyed is representative ofthe U.S. population, with a majority of the pop-ulation sampled being white.

A comprehensive periodontal evaluation was per-formed for each patient by a single examiner (WL)immediately before the PSG; thus, the examinerwas masked to the patient’s OSA category. AfterPSG, the patients diagnosed with varying degrees ofOSA (test group) were stratified into the followingcategories: mild, moderate, and severe according tothe AHI. At the same time, those patients whosePSG determined that they did not have OSA actedas the control group. All patients had to have aminimum of 16 remaining natural teeth to be in-cluded in the study.

Before the periodontal examination, patient-levelvariables that are putative confounders, such as bodymass index (BMI), diabetes, and smoking history,were recorded during the patient examination indetail as follows. The BMI was calculated for eachpatient from data available in the chart. If the pa-tient had diabetes, the chart was reviewed to de-termine the most recent hemoglobin A1c (HbA1c)(laboratory results had to be taken within the 6months before the periodontal examination). Smok-ing history was determined by questioning patientsand categorized as follows: 1) non-smoker (neversmoked); 2) former smoker (smoked but quit before

i Easy III PSG System, Cadwell Laboratories, Kennewick, WA.

J Periodontol • February 2015 Loke, Girvan, Ingmundson, Verrett, Schoolfield, Mealey

233

the study; time since quitting was determined inmonths); and 3) current smoker. Current smokersand former smokers who quit within the past 6months were excluded from the study.

The inclusion criteria for the OSA patients wereas follows: 1) mild (AHI of at least five to 15 perhour), moderate (AHI >15 to 30 per hour), andsevere (AHI >30 per hour) OSA; 2) aged ‡30 years;3) non-smokers or former smokers who quit at least6 months before the examination; 4) no history ofacute coronary syndrome; 5) American Society ofAnesthesiologists (ASA) Class I or II; and 6) pa-tients with diabetes only included if glycemic con-trol was good to moderate (documented HbA1cwithin the past 6 months £8%).

The periodontal examination included a full peri-odontal charting at six points per tooth (mesio-facial,mid-facial, disto-facial, disto-lingual, mid-lingual,and medio-lingual), excluding third molars, recordingprobing depth (PD), recession (REC), and clinicalattachment level (CAL). Bleeding on probing (BOP)was assessed at six points per tooth and recordedas either present or absent within 15 seconds ofprobing. The presence of visible plaque was eval-uated at four sites per tooth (mid-mesial, mid-facial,mid-distal, and mid-lingual) and recorded as presentor absent. Periodontal variables were examined fordifferences across all four categories of OSA (none,mild OSA, moderate OSA, and severe OSA). Aftercomprehensive clinical periodontal examination,the periodontal variables were assessed for both thetest and control groups to determine relations with

sleep apnea and were recorded as follows for eachpatient: 1) mean periodontal PD; 2) mean CAL; 3)mean REC; 4) percentage of sites with BOP asa measure of gingival inflammation; 5) percentageof sites with plaque; 6) percentage of sites with PD‡5 mm; and 7) percentage of sites with CAL ‡3 mm.

The definitions of periodontitis used in this studyare the American Academy of Periodontology (AAP)/Centers for Disease Control and Prevention (CDC)definitions of periodontal disease as described byEke et al:29 1) mild periodontitis, defined as two ormore interproximal sites with attachment loss (AL)‡3 mm and at least two interproximal sites with PD‡4 mm (not on the same tooth) or one site with ‡5mm; 2) moderate periodontitis, defined as two ormore interproximal sites with AL ‡4 mm (not on thesame tooth) or two or more interproximal sites withPD ‡5 mm, also not on the same tooth; and 3) severeperiodontitis, defined as two or more interproximalsites with AL ‡6 mm (not on the same tooth) and oneor more interproximal site(s) with PD ‡5 mm.

Statistical AnalysisThe association between OSA and periodontaldisease was analyzed using statistical methods thattreated OSA as an exposure factor and periodontaldiagnosis as outcome. Because OSA was representedby both ordinal (AHI classification) and continuous(observed AHI count) measures and periodontaldiagnosis was represented by dichotomous, ordinal,and continuous measures, several statistical methodswere used.

For the purposes of a priori power analysis, aone-way analysis of variance (ANOVA) comparingmeans for a continuous value periodontal indexacross the four classifications of OSA severity wasconsidered. Based on equal sample sizes of 25patients per group, the proposed total sample of100 patients achieves 91% power to reject the nullhypothesis of equal means using an F test witha 0.05 significance level if the population effect sizeis ‡0.39. To achieve this effect size, the standarddeviation of the four group means needs to be ‡39%of the common standard deviation within groups.This effect size requires a clinically significant meandifference of one common standard deviation to bepresent for the sample population between the controlgroup and at least one of the OSA severity groups.

Statistical analyses to assess associations betweenOSA severity represented as an ordinal groupingvariable (normal, mild, moderate, severe) and de-mographic and periodontal variables were performedusing x2 tests for categoric measures, Spearman rankcorrelations for ordinal and continuous measures,and analysis of covariances (ANCOVAs) for peri-odontal indices with age as a covariate. When small

Table 1.

Frequency of Patient Characteristics (byAHI classification)

Characteristic Normal Mild Moderate Severe Total

EthnicityAfrican American 4 2 1 8 15White 16 13 13 16 58Hispanic 6 3 5 10 24Other 0 3 0 0 3

SexFemales 4 3 2 0 9Males 22 18 17 34 91

Smoking historyFormer smoker 6 2 6 11 25Non-smoker 20 19 13 23 75

DiabetesAbsent 24 17 13 22 76Present 2 4 6 12 24

Total 26 21 19 34 100

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expected frequencies were observed, Fisher exacttests were substituted for x2 tests. If the F test forthe main effect for OSA severity was significant forANCOVA, then age-adjusted mean comparisonswere performed for the severe group versus thenormal, mild, and moderate OSA groups.

Additional analyses were performed to assess as-sociations between continuous AHI scores and de-mographic and periodontal variables using Spearmanrank correlations for ordinal and continuous mea-sures and multivariable logistic regressions pre-dicting moderate/severe periodontitis using 10-unitincrements for AHI. Hosmer-Lemeshow goodness-of-fit tests were performed to verify the validity ofmultivariable logistic regression models. The num-ber of predictors for logistic regression was limitedto the smaller number of patients between negativesand positives for moderate/severe periodontitis di-vided by 10. For statistical tests, P <0.05 was con-sidered significant. The 95% confidence intervals(CIs) were calculated for correlation coefficients.Assuming all correlations to be positive, then cor-relation coefficients with a lower 95% CI bound >0.20were considered to be meaningful, between 0.10and 0.20 were considered to be small, and <0.10were considered to be negligible, similar to the ruleof thumb for interpreting the size of a correlationcoefficient proposed by Hinkle et al.30 Statisticalanalyses were performed using statistical software.¶

In addition to age, demographic variables includedcontinuous measures of BMI and categoric pa-rameters of ethnicity (classes), sex (males/females),diabetes (presence/absence), and smoking history(non-smoker/former smoker).

RESULTS

Patient EnrollmentThe mean – SD for age in the normal, mild, mod-erate, and severe AHI categories were 44.0 – 12.9,

55.4 – 13.4, 58.6 – 12.6, and54.2 – 11.8, respectively. BMI inthe normal, mild, moderate, andsevere AHI categories were 31.9 –7.1, 32.0 – 5.3, 32.5 – 4.3, and36.6 – 6.9, respectively. Fisherexact tests indicated no significantrelation among AHI classificationand ethnic categories (P = 0.174)or sex (P = 0.065). x2 analysis alsorevealed no significant relationamong AHI classification and his-tory of past smoking or nosmoking (P = 0.245) or the pres-ence or absence of diabetes (P =0.070).

Association Between AHI Classification andPeriodontal DiseaseThe main objective of this study is to examine theassociation between AHI severity and periodontaldisease prevalence and severity (Table 2). Theprevalence of moderate/severe periodontitis in thesampled population, defined according to the AAP/CDC classification, was 73%. This is almost twice ashigh as the 38.5% prevalence of moderate and se-vere periodontitis found in the most recent study ofthe United States population.28

When comparing the percentage of patients withmoderate/severe periodontitis across the four AHIgroups (Table 2), the x2 test did not indicate anystatistically significant differences among AHIgroups (P = 0.111). The largest percentage differ-ence between groups was for normal AHI (57.7%)versus severe AHI (85.3%).

Because of the high prevalence of moderate/severe periodontitis in the study population, a posthoc power analysis was performed to determine thesample size needed to detect significant AHI groupdifferences in prevalence of moderate/severe peri-odontitis. If the sample size was doubled to 200patients, then the sample size would be sufficient todetect AHI group differences by x2 test at the 0.05level with a power of 84%.

When analyzing the Spearman correlations be-tween the two main variables in this study— AHIclassification (normal, mild, moderate, severe) andperiodontal disease classification (none, mild, mod-erate, severe)—the correlation coefficient is negli-gible (r = 0.246, 95% CI = 0.052 to 0.422). Small ornegligible correlations were also found between peri-odontal disease classification and both age (r = 0.317,95% CI = 0.128 to 0.483) and BMI (r = 0.179, 95%CI = -0.018 to 0.363). Similarly, the correlation

Table 2.

Pearson x2 Test for AHI Classification and Presence orAbsence of Moderate/Severe Periodontitis

Periodontal Disease (moderate/severe)

AHI Classification No Yes Total

Normal 11 (42.3%) 15 (57.7%) 26 (100.0%)

Mild 5 (23.8%) 16 (76.2%) 21 (100.0%)

Moderate 6 (31.6%) 13 (68.4%) 19 (100.0%)

Severe 5 (14.7%) 29 (85.3%) 34 (100.0%)

Total 27 (27.0%) 73 (73.0%) 100 (100.0%)

P = 0.111.

¶ SPSS v.20.0, IBM, Chicago, IL.


235

between AHI classification and age was negligible(r = 0.276, 95% CI = 0.084 to 0.448), and the AHIclassification with BMI correlation was small (r =0.300, 95% CI = 0.110 to 0.468).

Association Between AHI (Absolute) andPeriodontal DiseaseThe relation between AHI and periodontal diseasewas also examined using absolute AHI values as acontinuous variable. When AHI was expressed as acontinuous variable, there were negligible correla-tions between AHI and periodontal disease severityclassification (r = 0.191, 95% CI = -0.006 to 0.373)and between AHI and age (r = 0.273, 95% CI =0.081 to 0.446), whereas a small correlation wasobserved between AHI and BMI (r = 0.342, 95%CI = 0.156 to 0.505).

Association Between AHI and PeriodontalDisease (Box Plot Analysis and ANCOVA)Box plot analysis was performed to evaluate therelation between AHI classification and periodontalparameters (Fig. 1). The box plot analysis provided

a visual assessment of the medians, 25th to 75thinterquartile range, minimum and maximum values,and the outliers. Percentage plaque proved tobe the only clinical periodontal parameter thathad a statistically significant relation with AHIclassification.

Because box plot analyses demonstrated a sig-nificant relation with percentage plaque and sug-gested a possible relation with percentage BOP andpercentage CAL ‡3 mm with AHI classification, theserelations were further evaluated by ANCOVA (Table 3).The significant relation between AHI class and per-centage plaque was confirmed by ANCOVA (P = 0.037),with the age-adjusted severe group mean significantlygreater than the age-adjusted mild group mean(mean difference of 21.7%, 95% CI = 7.0% to 36.3%,P = 0.004). The age covariate was also significantlyassociated with percentage plaque (P = 0.001).However, ANCOVA revealed no significant relationbetween AHI class and percentage BOP (P = 0.126)or percentage sites with CAL ‡3 mm (P = 0.842).The age covariate was significantly associated with

Figure 1.Box plot analysis of AHI category and periodontal variables. A)Mean PD. B)Mean REC. C)MeanCAL. D) Percentage of sites with BOP. E) Percentage of sites with plaque. F) Percentage of sites withPD ‡5 mm. G) Percentage of sites with CAL ‡3 mm. Open circles indicate mild outliers; asterisksindicate extreme outliers.


236

percentage BOP (P = 0.025) but not significantlyassociated with percentage CAL ‡3 mm (P = 0.266).

Analyzing Periodontal Disease as a CategoricalVariableThe relation between periodontitis classification asa categorical variable (ADA/CDC mild, moderate,or severe) and other patient-level variables wasanalyzed separately using Fisher exact tests. Theanalysis showed no statistically significant relationbetween periodontitis classification and ethnicity(P = 0.086) or sex (P = 0.902). However, periodontalclassification was significantly related to diabetes(P <0.001) and smoking history (P = 0.042). As dis-cussed above, Spearman correlation analysis alsorevealed a small correlation between periodontaldisease classification and age (r = 0.317, 95% CI =0.128 to 0.483), whereas the correlation with BMI(r = 0.179, 95% CI = -0.018 to 0.363) was negligible.

Multivariable Logistic RegressionMultivariable logistic regression analysis was used toexplore the relation between the prevalence ofmoderate/severe periodontitis and AHI. For logistic

regression, AHI absolute values weredivided into 10-unit increments, andage was divided into 10-year in-crements. Given the fact that therewere only 27 patients who did nothave moderate/severe periodontitis,the sample had sufficient power toinclude up to three predictors in themodel. Other demographic variablesconsidered for inclusion were di-abetes and smoking history. How-ever, because the average age forpatients with diabetes was 12.7years older than the average age forthose without diabetes, these mea-sures were significantly associated,whereas no such association wasfound between age and smokinghistory. Thus, the three-predictormodel included the continuous

measures of AHI and age and the categorical co-variate of smoking history, with non-smoker as thereference group (Table 4). The Hosmer-Lemeshowgoodness-of-fit test had P = 0.749, so the modelwas valid. The resulting periodontal disease severityodds ratio (OR) for 10-unit AHI was not statisticallysignificant (OR = 1.04, 95% CI = 0.88 to 1.23, P =0.615), nor was the OR of former smokers to non-smokers (OR = 3.49, 95% CI = 0.92 to 13.3, P =0.067). Conversely, the 10-year increment age ORwas significant (OR = 1.52, 95% CI = 1.05 to 2.22,P = 0.028), indicating a significant relation betweenage and diagnosis of moderate/ severe peri-odontitis.

DISCUSSION

The main objective of this study is to analyze therelation between OSA and periodontal disease prev-alence and severity using a variety of clinical param-eters. The association between OSA and periodontaldisease has been suggested by previous cross-sectional studies20,31-33 to have an OR of between1.75 and 1.84.31 Furthermore, a dose–responserelation has been proposed32 (i.e., higher AHI maybe associated with increased odds for periodontitis).The current study set out to examine dose–responserelations by stratifying the OSA population into threecategories of severity (AHI: mild, moderate, andsevere) along with a control group without OSA. Allthe patients, who were consecutively recruited at aVA hospital sleep center, were newly diagnosed andhad no previous treatment for their sleep conditionof OSA.

Strict inclusion criteria excluded possible con-founders such as current smokers, patients withpoorly controlled diabetes, other poorly controlled

Table 3.

ANCOVA of Percentage of Sites With BOP, Percentageof Sites With Plaque, and Percentage of Sites WithCAL >3 mm (means unadjusted for the age covariate)

AHI Class n

Percentage

BOP – SD*Percentage

Plaque – SD†Percentage of Sites with

CAL ‡3 mm – SD‡

Normal 26 13.1 – 12.4 34.0 – 27.6 42.5 – 20.7

Mild 21 11.3 – 9.4 31.5 – 20.5 44.4 – 23.7

Moderate 19 14.9 – 9.0 47.2 – 28.7 44.0 – 27.8

Severe 34 19.8 – 19.0 52.3 – 31.5 48.4 – 22.6

Total 100 15.3 – 14.2 42.2 – 29.0 45.2 – 23.2

* Percentage BOP: F = 1.952; P = 0.126† Percentage plaque: F = 2.938; P = 0.037‡ Percentage of sites with CAL ‡3 mm: F = 0.276; P = 0.842

Table 4.

Logistic Regression Model for PeriodontalDisease Prevalence and AHI

Variable OR 95% CI P

AHI 10-unit increments 1.044 0.883 to 1.234 0.615

Age 10-year increments 1.523 1.047 to 2.216 0.028

Smoking history (yes/no) 3.492 0.918 to 13.279 0.067


237

systemic diseases (ASA Class greater than II), andpregnant or lactating females, thus providing astudy sample with the least amount of patient-centered confounders. The examiner was maskedand performed the periodontal examination on patientsbefore their PSG sleep study, therefore limiting theeffect of examiner bias.

The sample size was calculated based on therequired number of patients per group to reject thenull hypothesis of equal group means using one-way ANOVA at the 0.05 significance level with 90%power with an effect size defined by a clinically sig-nificant mean difference of one common standarddeviation being present for the sample populationbetween the control group and at least one of theOSA severity groups. The final enrolled sample of100 patients provided the required effect size, as-suming a population prevalence of periodontitis similarto that seen in studies of the United States pop-ulation.28,29 Although this sample size was smallerthan some other studies,31-33 the study used AHI scoresand analyzed them as both categorical variables(i.e., mild OSA [AHI of at least five to 15 per hour],moderate OSA [AHI >15 to 30 per hour], and severeOSA [AHI >30 per hour]) and as continuous vari-ables based on the absolute AHI values. Becausethe prevalence of moderate/severe periodontitiswas higher in this study population than originallyexpected, a post hoc power analysis was performedto determine the sample size needed to detectsignificant AHI group differences in percentages formoderate/severe periodontitis for a population witha very high prevalence of moderate/severe disease.The sample size would need to be doubled in sucha population (n = 200) to attain a sample sizesufficient to detect AHI group differences by x2 testat the 0.05 level with power of 84%.

This study found no meaningful association be-tween OSA and the prevalence of moderate/severeperiodontitis. Furthermore, there was a negligiblecorrelation between AHI severity and periodontaldisease severity categories. It is concluded that therelation between the severity of OSA and periodontalstatus, if any, was weak in this specific patient pop-ulation. Caution should be exercised when extrap-olating the results of this study to the generalpopulation because the high prevalence of peri-odontitis recorded in this study differs from theprevalence found in the United States population asa whole.28,29 The high percentage of patients withmoderate/severe periodontitis makes evaluation ofdifferences in AHI severity among groups with no,mild, moderate and, severe periodontitis more dif-ficult. However, this patient population was selectedfrom consecutively treated VA sleep center patients,without regard to their periodontal status, and peri-

odontal examination was performed before the PSGstudy. Future studies should evaluate larger sleepstudy patient populations to provide a greaternumber of patients with little or no periodontitis. Asummary of the various study designs, definitions,and limitations of the previous studies are found inTable 5.

The findings of this study are in disagreementwith previous studies that examined the relationbetween OSA and periodontal disease.20,31-33 Thedifference in study outcomes has several possibleexplanations. First, this study used six-point com-prehensive full-mouth periodontal examination onall teeth. One of the other studies32 used partial-mouthcharting, which may lead to an underestimation ofthe prevalence of periodontal disease. Second, thedefinitions of periodontal disease used in the pre-vious studies were different from the current study.Some of the definitions may have underestimated32

the prevalence of periodontal disease and othersmay have overestimated31 the prevalence of peri-odontal disease relative to the AAP/CDC definitionused in this study.28 Third, the clinical diagnosis ofOSA in one of the previous studies33 did not use thePSG sleep test; instead, a questionnaire meant forscreening patients undergoing general anesthesiawas used. Fourth, most of the previous studies col-lapsed all the OSA groups into a dichotomousdefinition of presence or absence of sleep apnea,10

had a stratification of three OSA groups (less than5, 5 to 10, and >10 events per hour),32 or obtainedthe diagnosis from International Classification ofDiseases, Ninth Revision (ICD-9) databases.31 Thismay mask the inherent differences in prevalence ofperiodontal disease based on the AHI-defined se-verity groups from detection. The current study pro-vides the most rigorous OSA classification of anystudy published to date, using the currently acceptedstratification of the AHI groups into non-OSA (AHIof less than five per hour), mild OSA (AHI of at leastfive to 15 per hour), moderate OSA (AHI >15 to 30per hour), and severe OSA (AHI >30 per hour).4

Finally, some studies20,31 examined the periodontalstatus of OSA patients only, comparing the prev-alence of periodontitis in the OSA study populationwith that found in populations outside the studygroup, such as national demographic dental data-bases20 or insurance databases.31 The current studyexamined both OSA and non-OSA patients, newlydiagnosed with a PSG gold-standard test within theVA-eligible population.

In other studies demonstrating an association be-tween OSA and periodontal disease, the associa-tion measured by OR was relatively weak (1.75to 1.84).31,32 In the current study, the OR for AHIand prevalence of periodontitis was not statistically


238

Table

5.

SummaryofCross

-Sec

tional

StudiesonPeriodontalDisea

se–O

SA

Relations

Study

SampleSize

and

Origin

MeanAge/BMI/A

HI

Definitio

nand

DiagnosisofOSA

Definitio

nof

Periodo

ntitis

TeethExam

ined

Periodo

ntalDisease–

OSA

Relation

Limitatio

ns

Gunaratnam

etal.,

2009

20

66(54males

and12

females),Australia

Mean–SD

age:54

.9–12

.8years

AHIofmore

than

five

perho

urAAP/CDC:

Allsixsitesat

all

existingteeth

Prevalence

of

periodo

ntitiswas

77%

and79

%dependingon

definitions

used,

four

times

higher

than

therepo

rted

prevalence

inAustralia

Noconcurrent

controlgroup;used

prevalence

data

from

natio

nal

demographicstudy

comparedwith

OSA

group

OSA

group:A

HIm

ore

than

fiveperho

urMeanBMI:30

.5kg/m

2

(range:1

8.3to

51.2

kg/m

2)

Presence

oftwoor

more

interproximal

siteswith

CAL

‡4mm

noton

thesametooth,

ortw

oormore

interproximalsites

with

PD‡5

mm

not

onthesametooth.

PD,C

AL,REC

,and

BOP

Whether

control

patientshad

diagno

sedoroccult

OSA

unknown

Nocontrolgroup

for

non-OSA

patients,

used

natio

nalhealth

survey

data

Mean–SD

AHI:36

.55

–25

.77

Atleastoneperiodontal

pocket

with

aPD

‡4mm

andCAL

‡3mm

atthesame

siteon

atooth.

Lobene

modified

gingivalindex(G

I)Periodo

ntalexam

iner

notmaskedto

the

studyhypo

thesis

sopo

tentialfor

overdiagnosisof

periodo

ntitis;

SilnessandLo

eplaque

index(PI),

smallsam

plesize

Seoet

al.,

2013

32

687(460

males

and

227females),Korea

Mean–SD

age:55

.85

–6.63

years

AHIstratified

onlyby

<5,5

to10

,>10

Atleastfour

teeth

with

one

ormore

interproximalsites

with

PD>4

mm

and

CAL>6

mm

atthe

samesite

on

atooth

allexistingRam

fjord

indexteeth(teeth

#3,

#9,

#12

,#19

,#25

,and

#28

)

Overall,OSA

positivelyassociated

with

periodo

ntitis

(OR=1.84

,95%

CI=1.18

to2.87

)butonlyin

patients

‡55yearsofage

Partial-m

outh

exam

ination;

notall

teethexam

ined;

underestimationof

disease


239

Table

5.(continued)

SummaryofCross

-Sec

tional


se–O

SA

Relations

Study

SampleSize

and

Origin

MeanAge/BMI/A

HI

Definitio

nand

DiagnosisofOSA

Definitio

nof

Periodo

ntitis

TeethExam

ined

Periodo

ntalDisease–

OSA

Relation

Limitatio

ns

AHIscore

of‡

5cutoff

used

toindicate

the

presence

ofOSA

BOP,PD

,REC

,CAL,

SilnessandLo

ePI

andGI

PD(O

R=2.22

,95%

CI=1.30

to3.77

)

CAL(O

R=1.86

,95%

CI=1.07

to3.21

)

Kelleret

al.,

2013

31

7,32

1OSA

patients,

21,963

non-OSA

controlpatients(1:3

case:controlratio

matched

interm

sof

sex,agein

intervals

of10

years,

urbanizationlevel,and

indexyear),Taiwan,

>62%

weremales

Mean–SD

age:47

.6–15

.4years

Receivedfirst-time

diagno

sisofOSA

(ICD-9,C

linical

Modificationcodes

intheLo

ngitudinal

Health

Insurance

Database20

00)

Depth

of‡3

mm

constituted

diagno

sisof

periodo

ntaldisease;

confirm

edwith

mobility,bleeding,

andradiographic

alveolarbo

neloss

Full-mouthsix-site

probing

After

adjustingfor

socioecono

mic

factors,O

R=1.75

(95%

CI=1.68

to1.88

)

Noconcurrent

controlgroup;used

historicdata

from

insurancedatabase

ORforprevious

CP

among

males

was

1.81

(95%

CI=

1.67

to1.95

,P<0

.001

);am

ong

females,it

was

1.62

(95%

CI=

1.48

to1.78

)

Multiple

exam

iners

Usedsamples

with

previous

diagno

sis

ofCP;

unableto

adjustfor

anumberof

confounding

factors

that

wereno

tincluded

inthe

administrativedata


240

Table

5.(continued)

SummaryofCross

-Sec

tional


se–O

SA

Relations

Study

SampleSize

and

Origin

MeanAge/BMI/A

HI

Definitio

nand

DiagnosisofOSA

Definitio

nof

Periodo

ntitis

TeethExam

ined

Periodo

ntalDisease–

OSA

Relation

Limitatio

ns

setanalyzed

inthis

study;someof

these

factorsincluded

family

history,

cigarettesm

oking,

andoccupational

expo

sures

Ahm

adet

al.,

2013

33

154

Meanage:61

years

Definedusingafour-

item

‘‘STO

P’’O

SAscreening

questio

nnaire

ADAcase

type

definitions:

Full-mouth

periodo

ntalexam

with

PDandCALat

sixsites;based

primarily

onthe

patientschartsand

repo

rted

severity

of

AL;patientsclassified

accordingto

the

ADAcase

types

Cases

were4.1tim

esmore

likelyto

have

OSA

than

controls

(95%

CI=1.9to

11.4;P

=0.00

7)

Use

ofquestio

nnaire

falls

short

ofclinical

diagno

sisofOSA

,with

uncertain

sensitivity

or

specificity;m

aymisclassifythe

patientswith/

without

OSA

104caseswith

moderate/severe

periodo

ntitis,50

controlswith

gingivitis,61

males,

93females

Moderate

periodo

ntitisType

III:m

oderate

alveolarbo

neloss

andAL,PD

of5to

6mm,C

ALof3to

4mm,m

obility,

furcation

involvem

ent

possible

Severe

periodo

ntitis

Type

IV:severe

alveolarbo

neloss

andAL,PD

>7mm,

CAL‡5

mm,

mobility,and

furcation

involvem

ent

possible


241

significant (OR = 1.057, 95% CI = 0.896 to 1.248;P = 0.511) and, coupled with the negligible corre-lation between AHI and periodontal disease severitycategories, suggests that there is no dose–responserelation between AHI severity and prevalence ofperiodontitis. This was confirmed statistically whenAHI was expressed as an absolute value and treatedas a continuous variable (r = 0.191, 95% CI = -0.006to 0.373). In addition, the clinical parameters providinginformation on periodontitis severity and extent—meanPD, mean CAL, percentage of sites with CAL ‡3 mm,and percentage of sites with PD ‡5 mm—were notsignificantly correlated with AHI severity.

CONCLUSIONS

In conclusion, this is the first cross-sectional studyshowing that OSA, when defined in AHI severitycategories, is not significantly associated with theprevalence of periodontitis in this specific VA pop-ulation. Furthermore, none of the clinical periodontalparameters except percentage plaque were signifi-cantly related to severity of OSA. In addition, whenAHI was expressed in absolute values, there was nocorrelation with any periodontal parameters measured.

ACKNOWLEDGMENTS

The authors thank sleep technicians Amy McHenryand Larry Tho for their support in the recruitment ofpatients at the Audie L. Murphy Memorial SleepLaboratory. The authors report no conflicts of interestrelated to this study.

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Correspondence: Dr. Brian L. Mealey, University of TexasHealth Science Center at San Antonio, Department ofPeriodontics, MSC 7894, 7703 Floyd Curl Dr., SanAntonio, TX 78229-3900. Fax: 210/567-3761; e-mail:[email protected].

Submitted April 16, 2014; accepted for publicationSeptember 3, 2014.


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