Progression of Periodontitis and ToothLoss Associated with Glycemic Controlin Individuals Undergoing PeriodontalMaintenance Therapy: A 5-YearFollow-Up StudyFernando Oliveira Costa,* Luıs Otavio Miranda Cota,* Eugenio Jose Pereira Lages,*Alcione Maria Soares Dutra Oliveira,† Peterson Antonio Dutra Oliveira,† Renata Magalhaes Cyrino,*Telma Campos Medeiros Lorentz,* Sheila Cavalca Cortelli,‡ and Jose Roberto Cortelli‡

Background: Prospective studies that investigated the influence ofglycemic control in the progression of periodontitis and tooth lossduring periodontal maintenance therapy (PMT) programs have notpreviously been reported. The aim of the present study is to evaluateassociations between glycemic control status and progression ofperiodontitis and tooth loss among individuals during PMT.

Methods:A total of 92 individuals, all recruited from a prospectivecohort with 238 participants undergoing PMT, participated in thisstudy. Diabetes control was assessed according to percentage of gly-cated hemoglobin (HbA1c). Individuals were matched for sex andsmoking and were divided into three groups: 23 individuals with dia-betes and poor glycemic control (PGC), 23 individuals with diabetesand good glycemic control (GGC), and 46 controls with no diabetes(NDC). Full-mouth periodontal examination, including bleeding onprobing (BOP), probing depth (PD), and clinical attachment level,was performed at all PMT visits during a 5-year interval.

Results: Progression of periodontitis and tooth loss were signifi-cantly higher among PGC compared to GGC and NDC. The finallogistic model in the final examination included: 1) for the progres-sion of periodontitis, HbA1c ‡6.5% (odds ratio [OR] = 2.9), smoking(OR = 3.7), and BOP in >30% of sites (OR = 4.1); and 2) for toothloss, HbA1c ‡6.5% (OR = 3.1), smoking (OR = 4.1), and PD 4 to 6mm in £10% of sites (OR = 3.3).

Conclusions: PGC individuals, especially smokers, presented witha higher progression of periodontitis and tooth loss compared toNDC and GGC individuals. This result highlights the influence ofglycemic control in maintaining a good periodontal status. J Peri-odontol 2013;84:595-605.

KEY WORDS

Diabetes; maintenance; periodontal attachment loss; periodontitis;risk factors; tooth loss.

Several studies have empha-sized the benefits of peri-odontal maintenance therapy

(PMT) in preserving the homeo-stasis of periodontal tissues ob-tained after active periodontaltherapy (APT), which can includesurgical and/or nonsurgical pro-cedures.1-4 However, without es-tablishing a regular program ofclinical reevaluation, adequatebiofilm control, and reinforce-ment of oral hygiene instruc-tions, the benefits of PMT couldnot be maintained.5,6 Severalindicators or risk factors, includ-ing biologic, behavioral, and socialvariables, can influence the peri-odontal status of individualsunder PMT.3,4 Among thesevariables, the periodontal lit-erature is unanimous in high-lighting poor biofilm control,diabetes mellitus (DM), andsmoking.1,4,7,8

The chronic diseases peri-odontitis and DM have long beenconsidered to be biologicallylinked.9-11 Current evidence re-garding the biologic link between

* Department ofPeriodontology,DentistrySchool, FederalUniversity ofMinasGerais, BeloHorizonte,Brazil.

† Department of Periodontology, Faculty of Dentistry, Pontific Catholic University of Minas Gerais,Brazil.

‡ Department of Dentistry, Periodontics Research Division, University of Taubate, Taubate, SaoPaulo, Brazil.

doi: 10.1902/jop.2012.120255

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DM and periodontitis supports persistent hypergly-cemia leading to an exaggerated immuno-inflam-matory response to the periodontal pathogenicbacterial challenge, resulting in a more rapid andsevere destruction of periodontal tissues.9,10,12

A large amount of case reports, cross-sectionaland longitudinal studies, and literature reviews havereported the adverse effects of DM on the onset,progression, and severity of periodontitis.9,13-17

Additionally, several studies reported a two- to five-fold higher risk for periodontitis among individualswith DM.9,12,18

However, there is a growing interest among re-searchers to examine the effect of periodontal changeson glycemic control of individuals with DM and viceversa, wherein an inflammatory process can triggera context of insulin resistance.10,14,16,17,19-21 Thesestudies until now have shown conflicting results.

Moreover, several retrospective and prospectivestudies in PMT have shown that smoking, DM, andthe number of maintenance visits have a strong in-fluence on periodontal status.6,22-25 However, pro-spective studies on PMT reporting the effect ofglycemic control on the progression of periodontitisand tooth loss have not yet been reported.

Therefore, the aim of the present study is toevaluate associations between glycemic controlstatus and the progression of periodontitis and toothloss among individuals undergoing PMT.

MATERIALS AND METHODS

Study Design and Sampling StrategyThe study was a case-control design nested in anopen cohort study comprising 238 participants underPMT, monitored in a private dental clinic in the cityof Belo Horizonte, Brazil, from November 2006 toFebruary 2012. All individuals from this cohort hadthe following initial characteristics: 1) 18 to 66 years ofage; 2) in good general health (except diagnosisand history of diabetes); 3) had undergone basic peri-odontal therapy (comprising non-surgical and/or sur-gical procedures); 4) had received a diagnosis ofchronic moderate to advanced periodontitis beforeAPT, with at least four sites with probing depth (PD)‡5 mm and clinical attachment loss (AL) ‡3 mm,bleeding on probing (BOP) and/or suppuration (SU),and radiographic evidence of bone loss; 5) had com-pleted APT <4 months before entry in the PMT pro-gram; and 6) had ‡14 teeth.2-4,26

Individuals were excluded from the study if they: 1)were pregnant (n = 3); 2) showed debilitating dis-eases that could impair the immune system (suchas human immunodeficiency virus/acquired immu-nodeficiency syndrome, cancer, and auto-immunediseases; n = 4); 3) presented with drug-induced gingi-val hyperplasia (n = 6); 4) had Type 1 DM (n = 3); 5)

had <14 teeth (n = 19); 6) were irregular compliers(intervals between PMT visits >12 months [n = 53]);or 7) showed glycemic status oscillation between>6.5% and <6.5% of glycated hemoglobin (HbA1c)in at least two PMT visits (n = 4).

Based on the above criteria, a convenience sampleof 146 volunteers with regular compliance were eli-gible for the present case-control study. It should benoted that great effort was made to achieve PMTrecall intervals of 4 to 6 months for all participants.Type 2 DM control was assessed according to thepercentage of HbA1c at all visits of PMT; definition ofType 2 DM and cut-off points regarding HbA1c per-centages were based on American Diabetes Associa-tion (ADA) parameters.27 After 5 years of PMT, thefollowing individuals were selected: 23 individualswith diabetes with poor glycemic control (HbA1c‡6.5%), 35 individuals with diabetes with good gly-cemic control (HbA1c <6.5%), and 88 individualswith no diabetes with good general health (fastingblood glucose levels <126 mg/dL recorded annu-ally).27 HbA1c tests were performed on all patientswith diabetes 1 to 3 days before the PMT visit, in tworeferral laboratories (Hermes Pardini and HumbertoAbrao in Belo Horizonte, Brazil), according to eachindividual’s choice and convenience. These tests wereperformed according to the international standardsrecommended by the ADA.27 After being matched forsex and smoking, the final sample for the presentstudy comprised three groups: 1) 23 individuals withdiabetes with poor glycemic control (PGC); 2) 23 in-dividuals with diabetes with good glycemic control(GGC); and 3) 46 individuals with no diabetes(NDC). Groups were matched in an attempt to mini-mize the effects of confounders; if more than onematch could be achieved, GGC and NDC individualswere randomly selected among the matches. Dataobtained after APT and designated as baseline werecompared to data obtained after 5-year follow-upfinal examination.

All individuals provided written informed consentto participate in this study. The study was approvedby the Research Ethics Committee of the FederalUniversity of Minas Gerais (protocol #060/05).

Data CollectionData regarding sex, age, cohabitation status, bodymass index (BMI), education level, smoking status(smokers reported consumption of ‡100 cigarettesin their life and smoked at the time of examination;former smokers reported consumption of ‡100cigarettes in their life and did not smoke in at leasttwo PMT visits; and non-smokers never smoked)28

were collected and recorded for all individuals. Alldata that might have changed with time were con-firmed at each PMT visit.

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During maintenance visits, a complete periodontalexamination was performed, and data regardingplaque index (PI),29 PD, clinical AL, BOP (yes/no),furcation involvement, and SU were recorded. Allperiodontal parameters were used to determine peri-odontal status in four sites per tooth. Examinationswere performed with a manual periodontal probe.§

Methodology for data collection and periodontalclinical procedures during all PMT visits were thesame as reported by Lorentz et al.2

During PMT visits, the following procedureswere performed: 1) interview to determine possiblechanges in variables of interest (demographic, bi-ologic, and behavioral); 2) periodontal evaluationincluding the previously described clinical parame-ters; 3) application of disclosing agents and oralhygiene instructions, using the Bass technique, in-terproximal toothbrushes, and dental floss; 4) non-surgical or surgical mechanical debridement, whenappropriate, including coronal prophylaxis andfluoride application.

Inter- and Intraexaminer AgreementAll interviews, examinations, and clinical periodontalprocedures were performed by two trained and cali-brated periodontists (FOC and EJPL). Measurementsof PD and clinical AL were recorded and repeatedwithin a 1-week interval for 10 individuals randomlyselected from all study groups at baseline and finalexamination. Data were tested through non-para-metric k test (PD and clinical AL dichotomized bya cut-off point of ‡4 mm) and intraclass correlation.k coefficients for both intra- and interexaminer, aswell as intraclass correlation coefficients were >0.87.

Before the study, a training process was conductedto standardize the application of smoking question-naires during interviews. Interviews were repeated on12 individuals to verify the quality of categorical dataobtained. Because the literature has reported highinconsistency and biased information regardingsmoking,30 special attention was given to questionsrelated to smoking habits. k coefficients obtained forsmoking were 0.89. In addition, all data collected bythe questionnaire that may have changed with timewere confirmed at each PMT visit.

Determination of Recurrent Sites, RetreatmentNeeds, and Progression of PeriodontitisSites were determined as having retreatment needs ifthey showed PD ‡4 mm and clinical AL ‡3 mm, to-gether with the presence of BOP and/or SU, in anyrecall evaluation.2,31 Individuals diagnosed with re-current sites or residual PD changes were retreatedwith mechanical debridement and/or surgical pro-cedures as necessary.

Progression of periodontitis was defined as in-terproximal clinical AL ‡3 mm in at least two teeth

between two different observation points, according tothe fifth European Workshop of Periodontology.31,32 Inthe present study, this definition was used to defineprogression of periodontitis between any PMT visitsduring the 5 years of monitoring.2-4,31,32

Statistical AnalysisStatistical analysis included a descriptive charac-terization of the sample according to variables ofinterest. Group comparisons by means of x2 test,ANOVA, and Student t-test were performed whenappropriate. When equal variances were assumed,variables were compared by means of ANOVA andBonferroni post hoc test. When equal variances werenot assumed, variables were compared by means ofthe Welch test and Tamhane post hoc test.

Logistic regression analysis was performed to in-vestigate the association between the progressionof periodontitis and tooth loss for the followingindependent predictor risk variables: sex (mal-e/female), age (up to 30, 31 to 40, 41 to 49, and ‡50years), education level (‡8 years), cohabitation status(companion/no companion), smoking status (smoker/former smoker/non-smoker), number of PMT visits,BMI (>25 kg/m2), HbA1c (‡6.5% indicating PGC;<6.5% indicating GGC, and patients without diabetesas reference), duration of DM (>10 years), BOP (in>30% of sites), PD ‡4 mm in >30% of sites, PD be-tween 4 and 6 mm in £10% of sites, and clinical AL‡3 mm in 30% of sites. All predictive variables pre-senting a P value of £0.25 in the univariate analysiswere included in the multivariate regression model.Variableswere then removedmanually stepbystepuntilthe log-likelihood ratio test indicated that no variableshould be removed. Confounding variables were iden-tified if their removal from the model caused changes>15% in the b coefficient (probability of type II error).All variables included in the final multivariate modelwere determined to be independent through assess-ment of their collinearity. PI was excluded from thefinal model because of its covariance with BOP, andthe number of remaining teeth was determined to bea covariable due to its association with other predic-tive variables. Odds ratio (OR) estimates and theirconfidence intervals were calculated and reported.All tests were performed using statistical software.i

Results were considered significant if a P value <5%was attained (P <0.05).

RESULTS

Group characteristics regarding variables of interestare presented in Table 1. Significant differences werereported only for BMI and mean and percentage of

§ University of North Carolina (PCPUNC15BR) and Nabers PQ2NBR, Hu-Friedy, Chicago, IL.

i Statistical Package for Social Sciences, v. 16.0 for Windows, SPSS,Chicago, IL.

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clinical AL ‡5 mm in relation to NDC, GGC, and PGCgroups, showing a very homogeneous study sample.Important variables such as duration of DM andnumber of PMT visits also were not significantly dif-ferent among the study groups.

The periodontal status of the sample at baselineand final examination is presented in Table 2. Figure 1shows change in PD, clinical AL, BOP, and PI with timein 5 years of PMT. Overall, no significant differenceswere observed in relation to the parameters PD (Fig.1A), BOP (Fig. 1C), or PI (Fig. 1D) among groups atthe baseline examination. Figure 1B shows a differ-ence in clinical AL: PGC >GGC = NDC. Nevertheless,significant differences between NDC, GGC, and PGCgroups were observed in all clinic parameters at the

final examination, i.e., PGC >GGC (P <0.001), PGC>NDC (P <0.01), and GGC = NDC (P >0.05) (Fig. 1).The PGC group exhibited higher PI, mean BOP, PD,and clinical AL and a lower mean number of teethstill present (Table 2).

Progression of periodontitis, as well as periodontalclinical variables for NDC, GGC, and PGC groups atfinal examinationare presented in Table 3. In the NDCand GGC groups, 11 (23.9%) and five (21.7%) in-dividuals presented with progression of periodontitis,respectively, compared to nine (39.1%) individuals inthe PGC group. These differences (NDC versus PGC,and GGC versus PGC) were determined to be signif-icant (P <0.05). The mean values for BOP, PD, clinicalAL, and SU among PGC individuals were significantly

Table 1.

Characterization of the Sample (N = 92) According to Variables of Interest at FinalExamination.

Characteristics PGC Group GGC Group NDC Group

n 23 23 46

Sex, n (%)*Female 13 (56.5) 13 (56.5) 26 (56.5)Male 10 (43.5) 10 (43.5) 20 (43.5)

Age, n (%) (range: 22 to 71 years)*£30 years 3 (10.6) 2 (8.7) 5 (10.9)31 to 40 years 6 (26.1) 7 (30.4) 13 (28.3)41 to 50 years 6 (26.1) 5 (21.7) 11 (23.9)>50 years 8 (34.8) 9 (39.1) 17 (37.0)

Cohabitation status, n (%)*With companion 14 (60.8) 16 (60.0) 31(67.4)Without companion 9 (39.1) 7 (30.4) 15 (32.7)

Smoking status, n (%)*Non-smoker 16 (69.6) 16 (69.6) 32 (69.6)Smoker/former smoker 7 (30.4) 7 (30.4) 14 (30.4)

BMI, n (%)*£25 kg/m2 10 (43.5) 8 (34.8) 15 (32.7)>25 kg/m2 13 (56.5) 15 (62.3) 31 (67.3)

Education level, n (%)*<8 years 8 (34.8) 6 (26.1) 15 (32.7)‡8 years 15 (65.2) 17 (74.0) 31 (67.4)

Number of PMT visits (mean time between visits inmonths – SD)†

6 (9.4 – 0.5) 7 (8.8 – 0.5) 7 (8.9 – 0.9)

Diabetes duration (mean years – SD)* 11.4 – 8.9 10.9 – 9.7 NA

HbA1c (mean % – SD) 9.1 – 1.4 6.1 – 0.4 NA

Time elapsed since initial active therapy (meanmonths – SD)†

63.6 – 1.8 62.2 – 1.5 61.9 – 1.3

NA = not applicable.* x2 test (P >0.05).† ANOVA (P >0.05).

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higher than those among NDC and GGC individuals.Moreover, these values were higher among PGCindividuals presenting with progression of peri-odontitis compared to NDC individuals also pre-senting with progression of periodontitis, exceptfor PI. At the baseline examination, no progressionof periodontitis and no significant differencesregarding PI were observed among the groups.However, fewer individuals presented recurrenceof periodontitis (PGC: n = 2; GGC: n = 1; and NDC:n = 3). In addition, significant differences were notobserved between groups regarding PI.

Recurrence of periodontitis between baseline andfinal examination was also analyzed in relation to in-dividuals and sites in all groups. In the NDC, GGC,and PGC groups, 58 (2.8%), 55 (2.5%), and 127(6.1%) sites showed recurrence of periodontitis, re-spectively. These differences were determined to besignificant (P <0.05). In the NDC and GGC groups,15 and 16 surgical procedures (Widman modifiedflap surgery) were performed, respectively; in the

PGC group, 22 surgical procedures were performed.It is important to note that most sites in both groupsresponded favorably to conservative mechanicaldebridement procedures.

Table 4 summarizes tooth loss for all groups atbaseline and final examination. In final examination,the PCM group exhibited a significantly greaternumber of individuals having lost teeth and numbersof lost teeth than the NDC and GGC groups. Betweenthe NDC and GGC groups, these differences were notsignificant. During the 5-year monitoring period, thePGC group lost 21 teeth (4.0%), the GGC group lost11 teeth (2.0%), and the NDC group lost 25 teeth(2.3%) (P <0.05), reflecting a higher tooth loss rateamong PGC individuals.

Final multivariate logistic regression models forthe progression of periodontitis and tooth loss, ad-justed for all variables of interest, are shown in Table 5.For the progression of periodontitis, the followingvariables were significantly retained in the modelin final examination: HbA1c ‡6.5% (OR = 2.9,

Table 2.

Periodontal Variables According to Glycemic Status at Baseline and Final Examination

Total Sample (n = 92) PGC GGC NDC

n 23 23 46

PI (%)Baseline 38.6 – 10.2 37.8 – 9.4 37.2 – 10.7Final examination* 42.2 – 9.3 39.8 – 10.3 39.4 – 9.8

BOP (n)Baseline 23.9 – 14.1 22.8 – 8.4 23.7 – 9.3Final examination† 31.5 – 11.7 23.1 – 7.3 24.1 – 10.3

PD (mm)Baseline 3.6 – 0.8 3.5 – 0.9 3.3 – 0.9Final examination† 4.6 – 0.6 3.9 – 0.8 4.1 – 0.8

Mean clinical AL (mm)Baseline† 3.9 – 0.7 3.2 – 1.5 3.3 – 1.9Final examination† 6.7 – 0.5 5.7 – 0.6 5.1 – 0.7

Sites with PD ‡5 mm (%)Baseline 3.4 – 0.7 3.1 – 0.5 3.2 – 0.8Final examination† 4.1 – 0.4 3.5 – 0.4 3.4 – 0.7

Sites with clinical AL ‡5 mm (%)Baseline† 8.2 – 3.3 6.8 – 3.5 7.2 – 3.5Final examination† 8.9 – 2.7 6.2 – 3.1 6.5 – 3.4

Number of teeth present (sites)† 515 (2,060) 548 (2,192) 1,105 (4,420)

Number of teethBaseline 23.2 – 2.4 23.9 – 3.2 24.4 – 3.7Final examination† 20.5 – 2.1 22.2 – 2.8 22.9 – 3.2

Data are mean – SD unless noted otherwise.* Significant differences between groups at P <0.05, using ANOVA and Bonferroni post hoc analysis.† Significant differences between groups at P <0.001, using Welch test and Tamhane post hoc analysis.

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confidence interval [CI] = 1.43 to 9.81), smoking (OR =3.7, CI = 1.05 to 8.61), and BOP in >30% of sites (OR =4.1, CI = 1.52 to 12.8). For tooth loss, the followingvariables were significantly retained in the model:HbA1c >6.5% (OR = 3.1, CI = 1.03 to 10.89), smoking(OR = 4.1, CI = 1.98 to 11.6), and PD 4 to 6 mm in£10% sites (OR = 3.3, CI = 1.23 to 7.29). Interactionbetween HbA1c >6.5% and smoking showed ORsof 6.2 (CI = 1.58 to 14.2) and 6.9 (CI = 1.38 to 16.2)for the progression of periodontitis and tooth loss,respectively.

DISCUSSION

Several studies have supported a link between DMand periodontitis.9,13,17 The epidemiologic associ-ations between periodontitis and DM could be theresult of at least two similar, but distinct, pathogenicpathways: a direct causal relationship in which theconsequences of diabetes act as modifiers of peri-odontitis expression or a common pathologic defectthat results in a host susceptible to one or bothdiseases.17,33

An increase in the prevalence and severity ofperiodontitis in individuals with DM is due to reducedchemotaxis of polymorphonuclear leukocytes, phago-cytic defects, and depressed humoral response. Inaddition, in a hyperglycemic environment, numerousproteins undergo glycation to form advancedglycation end products (AGEs). AGE-mediatedevents are of primary importance in the path-

ogenesis of DM complicationsand may also contribute totissue changes within theperiodontium.12

The present study showedthat PGC individuals presentedwith a less healthy periodontalstatus and greater tooth losscompared with GGC and NDCindividuals. The differences ob-served among the groupsseemed to be related to glyce-mic control, since the effects oftheother riskvariables (suchasage, sex, education level, co-habitation status, BMI, numberof PMT visits, DM duration, andsmoking) were minimized bystatistical treatment, prospec-tive design, and matching.According to Ylostalo andKnuuttila,34 current studies get-ting even adequate statisticaltreatment should attempt tominimize the effect of modifiers

and confounders early in their design methodology.In the present study, among diabetic individuals in

the PGC group, the progression of periodontitis affectedapproximately three times as many individuals as inthe GGC and NDC groups (OR = 2.9). Moreover,individuals in the PGC group also showed more severeclinical indicators of periodontal disease. In severalstudies, two- to five-fold higher risks for periodontitiswere reported in individuals with diabetes comparedwith individuals with no diabetes.12-14,17,18,35,36

To the best of our knowledge, this is the first pro-spective study on PMT evaluating the progression ofperiodontitis and tooth loss in relation to glycemiccontrol in a very homogeneous sample regarding con-ventional risk indicators. From baseline to final exami-nation, we observed a significantly higher progressionof periodontitis among PGC individuals (39.1%) com-pared to GGC (21.7%) and NDC (23.9%) individuals.However, these rates in the GGC and NDC groupswere lower than in previous studies.24,37,38 It isimportant to emphasize that these comparisonsshould be carefully made because of the large meth-odologic differences between studies of periodontitisprogression.

Results from the present study reinforce the in-fluence of PGC in the progression of periodontitisand tooth loss. In addition, we observed an interestinglack of significant differences regarding disease in-dicators (periodontal parameters), as well as ratesof progression periodontitis and tooth loss, betweenthe NDC and GGC groups.

Figure 1.Change in PD (A), clinical AL (B), BOP (C), and PI (D) during 5 years of PMT. Baseline: PGC=GGC=NDC(P >0.05), except clinical AL: PGC >GGC = NDC (P <0.039). Final examination: PGC > GGC (P <0.001);*† PGC > NDC (P <0.01); *† and GGC = NDC (P >0.05). *Statistically significant increase in PI peryear, using ANOVA and Bonferroni post hoc analysis (P <0.05). †Statistically significant increase in PD,clinical AL, and BOP per year, using Welch test and Tamhane post hoc analysis (P <0.05).

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Bandyopadhyay et al.16 conducted a study to eval-uate associations between glycemic control and theprogression of periodontitis among Gullah AfricanAmericans with Type 2 DM. Authors showed sig-nificant ORs of tooth site-level clinical AL and PDprogression among Gullah with PGC versus well-controlled Type 2 DM in the absence of periodontaltherapy. A case-control study39 was conducted toevaluate the relationship between blood glucoselevels and clinical parameters of periodontal diseasein 65 and 81 individuals with and without diabetes,respectively. The authors concluded that periodontalclinical AL was increased by hyperglycemia in in-dividuals with diabetes (OR = 2.24).

PGC individuals presented with higher rates of toothloss compared to GGC and NDC individuals. Moreover,the final multivariate model for tooth loss includedHbA1c ‡6.5% (OR = 3.1, CI = 1.03 to 10.89). Severalepidemiologic studies with different designs have re-ported greater tooth loss among individuals with di-abetes.2-4,13,39,40 In a recent study, Botero et al.38

reported a positive correlation between glycemia andclinical AL, whereas a negative correlation was re-

ported between glycemia and the number of teethpresent.

No differences in relation to periodontal statusamong PGC, GGC, and NDC individuals at baselineexamination were observed (except mean and per-centage of clinical AL ‡5 mm). However, importantdifferences regarding clinical periodontal parameters(i.e., BOP, PD, clinical AL, and PI) were observed inthe final examination. Despite worse periodontalconditions reported among PGC individuals, it wasobserved that among GGC and NDC groups, ratesof progression of periodontitis and tooth loss wererelatively lower than those in other studies.36,38

This finding can be explained by the fact that duringregular PMT visits, individuals are constantly moti-vated and reinstructed regarding oral hygiene in-structions and biofilm control. Moreover, incipientinflammatory processes can be detected and treatedearly. In this manner, bursts of progression of peri-odontitis can be avoided or minimized. Similar resultshave been previously reported in PMT studies.4,33,40

In contrast, the high values of PI in all groups atfinal examination reflect a need for further and

Table 3.

Periodontal Clinical Variables of PGC, GGC, and NDC Groups at Final ExaminationAccording to the Presence/Absence of Progression of Periodontitis

Progression of Periodontitis (No/Yes) and Clinical

Variables PGC Group GGC Group NDC Group

Number of individuals (%) 23 23 46No 14 (60.8)* 18 (78.3)† 37 (80.4)†

Yes 9 (39.1)* 5 (21.7)† 11 (23.9)†

Number of sites (%) 2,015 2,192 4,420No 1,962 (97.4)* 2,162 (98.7)† 4,361 (98.8)†

Yes 53 (2.6)* 30 (1.36)† 59 (1.33)†

PD (mm)No 4.5 – 4.2* 4.0 – 3.7† 3.9 – 3.8†

Yes 6.4 – 5.1* 5.2 – 4.3† 5.4 – 3.9†

Clinical AL (mm)No 6.2 – 4.9* 5.1 – 4.8† 5.3 – 4.4†

Yes 9.2 – 6.3* 8.1 – 5.1† 7.9 – 4.9†

BOP (% of sites)No 39.3 – 12.8* 28.9 – 11.1† 29.8 – 9.9*Yes 45.3 – 13.1* 36.8 – 12.9† 35.7 – 11.8†

SU (% of sites)No 0.5 – 0.3* 0.1 – 0.8† 0.1 – 0.5†

Yes 1.1 – 0.1* 0.7 – 1.3† 0.5 – 1.1†

PI (%)No 39.8 – 8.5* 35.8 – 11.7† 33.9 – 12.4†

Yes 47.3 – 16.2* 45.8 – 12.3* 46.5 – 11.1*

Data are mean – SD unless noted otherwise. Means followed by different symbols (*,†) in rows are significantly different (P <0.05; Student t test forindependent samples); Bonferroni correction for all multiple comparisons (P <0.004).

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intensive efforts to control dental biofilm during PMT.This issue may be critical to the effectiveness of PMTprograms. Moreover, a similar result was reported inprevious studies that investigated the importance ofmotivation for oral hygiene, considering that in-dividuals have difficulty maintaining new habits withtime.2,4,23,40 Another possible explanation is that thehigh values of PI reported in the present study couldbe related to the inclusion of proximal sites29 duringexamination. These high values are similar to thosereported in previous studies.2,4,6,41

In general, subgingival debridement effectivelyreduces the population of Gram-negative microor-ganisms, while it concomitantly allows for an in-crease in the population of Gram-positive cocci androds, which is related to the microbiota of healthy gin-giva. The microbial counts in subgingival sites varyfrom 103 in shallow and healthy sites to >108 in deepperiodontal pockets.42 The recolonization of pre-viously treated periodontal pockets may occur with-out maintenance recall intervals of 3 to 4 months.Thus, the elimination or reduction of the proportionof pathogens through periodic subgingival de-bridement2,42 can compensate for inadequate pla-que control among individuals and perhaps mayjustify the good results reported in the aforemen-tioned studies which, despite showing high rates ofPI, presented reductions in PD and the number of siteswith BOP. Therefore, we consider that the periodicprofessional assistance may have compensated forthe lack of good control of plaque among the in-dividuals in the present study.

Lang et al.42 stated that the absence of BOP duringPMT visits can be considered a good predictor ofperiodontal stability. Studies have provided evidencethat sites showing constant BOP during PMT visitswere at higher risk for attachment loss compared to

healthy sites.43,44 In the present study, we observeda non-significant difference in the number of sites withBOP in GGC and NDC groups at final examination,as well as an increase in the number of sites withBOP among PGC individuals. Moreover, the anal-ysis showed that BOP in >30% of sites was associatedwith the progression of periodontitis, corroboratingprevious findings.3,4,17

Clinical AL can reflect previous occurrence ofperiodontitis and is determined to be the gold-stan-dard parameter in periodontal diagnostics. In thepresent study, changes in clinical AL ‡3 mm betweenPMT visits were used to define the progression ofperiodontitis.2,32 This cut-off point was chosen be-cause it allows reproducibility measurement errorsof 1 mm and a standard deviation around 0.84 mm.Therefore, this criterion can avoid potential super-estimated rates of progression of periodontitis.2-4,45

It is well recognized that biofilm control is a de-termining factor for the success of PMT programs.1-4

In the present study, a significant increase in PI wasobserved among all individuals at final examina-tions. Previous studies reported a worse periodontalcondition among individuals with poor biofilm con-trol during PMT, regardless of pattern of compli-ance,3,4,46,47 smoking,24 and DM.2-4

Many studies have demonstrated that smoking isassociated with an increased risk for attachment loss,bone loss, and tooth loss.2-4,24-26,47,48 In addition, ithas been demonstrated that smokers respond lesspropitiously to all forms of periodontal treatmentand present less improvement in PD and clinicalAL.25,47 In the present study, smoking was retainedin the multivariate final model as an important vari-able associated with the progression of periodontitisand tooth loss. Similar results have been reportedpreviously.2-5,24 Moreover, the interaction between

Table 4.

Tooth Loss Among NDC, GGC, and PGC Groups at Baseline and Final Examination

Clinical Variables PGC GGC NDC

n 23 23 46

BaselineNumber of teeth present 536 559 1,130Individuals with tooth loss, n (%) 20 (86.9)* 18 (78.3)† 37 (80.4)†

Final examinationNumber of teeth present 515 548 1,105Individuals with tooth loss, n (%) 21 (91.3)* 18 (78.3)† 38 (82.6)†

Number of lost teeth from baseline to finalexamination

21 (4.0)* 11 (2.0)† 25 (2.3)†

Comparisons followed by different symbols (*,†) in rows are significantly different (P <0.05; Student t test for independent samples). Bonferroni correction formultiple comparisons (P <0.05).

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PGC and smoking showed higher ORs for the pro-gression of periodontitis and tooth loss.

A current matter of discussion is the effect ofperiodontal treatment on glycemic control amongdiabetic individuals.9,10,16,17 In a recent systematicreview and meta-analysis,9 it was concluded thatperiodontal treatment leads to an improvement ofglycemic control in Type 2 diabetic individuals for‡3 months. The authors emphasized the need forfollow-up periods >6 months and larger samples toallow separate analysis of individuals with moderateto advanced periodontitis.

Some limitations, including the absence of stratifiedanalysis of dose exposure for smokers and the smallsamplesizeofindividualswithprogressionofperiodontitisfor the finalmultivariate analysis, can be attributed to thepresent study. However, a 5-year follow-up period, pro-spective design, matching for sex and smoking, andstandardization of procedures for periodontal treatmentand PMT may minimize the impact of those issues.

CONCLUSIONS

GGC and NDC individuals presented with lowerrates of progression of periodontitis and tooth losscompared to PCM individuals. This finding dem-onstrated that poorly controlled DM could aggra-vate periodontal disease.

Moreover, the interaction between smoking andPGC strongly increased the risk for the progressionof periodontitis and tooth loss. DM and smokingshould be considered important variables when de-termining risk profiles in an attempt to provide amoreefficient management of periodontally susceptibleindividuals.

ACKNOWLEDGMENTS

The authors thank Dr. Leonardo Costa Lima, Mrs.Milene Aparecida Mendes da Rocha, and Ms.Wilciane Machado da Silva (private dental clinic,Belo Horizonte, Brazil) for their assistance withthe periodontal maintenance therapy visits andmonitoring of periodontal patients. Financial sup-port was obtained from the National Council forScientific and Technological Development (CNPq),Brasılia, Brazil (protocol #471616/2007-9 and#301493). The authors report no conflicts of interestrelated to this study.

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Final Logistic Regression Models for Progression of Periodontitis and Tooth Loss at FinalExamination

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Correspondence: Prof. Fernando Oliveira Costa, FederalUniversity of Minas Gerais, Department of Periodontology,Antonio Carlos Avenue, 6627, Pampulha PO Box 359,31270-901 Belo Horizonte, MG, Brazil. Fax: 55 31 32826787; e-mail: focperio@uol.com.br.

Submitted April 23, 2012; accepted for publication June14, 2012.

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