1185

Periodontal Status of Diabetic andNon-Diabetic Men: Effects of Smoking,Glycémie Control, and SocioeconomicFactorsRaymond B. Bridges,* James W. Anderson,* Stanley R. Saxe,* Kevin Gregory,* andSusan R. Bridges*

Periodontal disease is more prevalent and more severe in diabetic than in non-

diabetic individuals but the magnitude of this increase is still being debated. Thisprospective, cross-sectional study compared the periodontal status of 118 diabetic men

and 115 age-matched non-diabetic men. Plaque and gingival indices, bleeding scores,probing depth, losa of attachment, and number of missing teeth were measured in a

blinded manner. Smoking status, glycémie control, socioeconomic status, and previousdental care were also assessed. These parameters were significantly higher in diabeticthan non-diabetic men: plaque index, < 0.0001; gingival index, < 0.0002; bleed-ing score, < 0.0001; probing depth, = 0.0059; loss of attachment, < 0.0001;and missing teeth, < 0.005. These parameters were significantly higher in smokersthan non-smokers: gingival index, probing depth, and loss of attachment. The durationof diabetes was not significantly related to the periodontal measures. Glycémie controlas assessed by fasting plasma glucose and glycohemoglobin values was not signifi-cantly correlated to periodontal status. These studies indicate, for this study group,that diabetes significantly affects all measured parameters of periodontal status. J Peri-odontol 1996;67:1185-1192.

Key Words: Periodontal diseases/epidemiology; diabetes mellitus, smoking/adverseeffects.

Diabetes mellitus is a chronic disease which is increasingin prevalence worldwide; in the United States, for ex-

ample, it affects an estimated 11 to 15 million persons.'The association between diabetes and periodontal diseasehas been well recognized for nearly 40 years.2 Carefullycontrolled clinical studies indicate that periodontal dis-ease is more prevalent in diabetic than non-diabetic in-dividuals,3-" but the magnitude of the increase and itsmanifestations are still debated.1213 Furthermore, the ef-fects of the type of diabetes, glycémie control, and du-ration of diabetes on the prevalence of periodontal diseaseare still unclear.51012-13

This prospective, cross-sectional controlled study com-

pared the periodontal status of 118 diabetic men and 115age-matched non-diabetic men. Plaque and gingival in-

*Department of Oral Health Science, College of Dentistry, Universityof Kentucky, Lexington, KY.•Metabolic Research Group, va Medical Center, College of Medicine.*Departments of Oral Health Science and Practice, College of Dentistry.College of Dentistry.

dices, bleeding score, probing depth, loss of attachment,and the number of missing teeth were assessed and com-

pared in matched diabetic and non-diabetic men. The pur-pose of the study was to determine if there were signifi-cant differences for these measures of periodontal statusbetween diabetic and matched-control subjects. Smokingstatus, glycémie control, and socioeconomic data werealso evaluated and compared to periodontal status. Thisstudy demonstrated that diabetic men had significantlymore evidence of periodontal disease than matched non-

diabetic men.

MATERIALS AND METHODS

Study GroupsDiabetic men were recruited from the outpatient diabetesclinic at this Veterans Affairs (VA) Medical Center; non-diabetic men were recruited from the lipid clinic, cardi-ology clinic, and other medical clinics at the same VAMedical Center. Men aged 24 to 78 years old were re-

1186 DIABETES AND PERIODONTAL STATUS IN MENJ Periodontol

November 1996

cruited from all racial and ethnic groups. After a diabeticman was recruited, we attempted to recruit a non-diabeticman of approximately the same age and body mass index.Men were excluded if they had less than 20 teeth, lessthan 8 teeth per arch, less than one molar tooth per arch,serum Creatinine exceeding 2.0 mg/dl (since renal dys-function can affect nutritional and periodontal status14), orwere taking medications, such as diphenylhydantoin, thatcould affect gingival status. Non-diabetic men were ex-

cluded if they had a first degree relative with diabetes.Men were recruited without regard to smoking status or

periodontal status. This study was approved by the Uni-versity of Kentucky Institutional Review Board for hu-man subjects and all subjects signed an informed consentform.

QuestionnaireAll men completed an extensive health survey which in-cluded 60 questions related to demographics, tobacco use,medical history, history of diabetes and its treatment andcomplications, dental care and health, and use of medi-cations. Smoking was self-reported and included, forthese analyses, reported use of cigarettes, pipe, or cigars.

ProceduresMen were initially screened by a dental hygienist to de-termine eligibility and obtain volunteers for the study.They did not eat food for 12 hours and did not take in-sulin or oral hypoglycémie agents before reporting at 8a.m. After venipuncture, subjects took their diabetes med-ication, ate breakfast, and reported to the dental clinic forperiodontal assessment.

Laboratory MeasurementsSerum glucose was measured by the glucose oxidasemethod,15 serum insulin and C-peptide were determinedby radioimmunoassay using commercially available kitsand standards,11 and glycosylated hemoglobin was deter-mined using commercially available columns and stan-dards.11

Diabetes ClassificationUsing the criteria of the National Diabetes Group,16 dia-betic men were divided into Type I (insulin-dependent)or Type II (non-insulin-dependent) diabetes mellitus. Aclinical diabetologist (TWA) made this assignment basedon a review of the following information: the subject'smedical chart, self-reported history, serum insulin, andC-peptide measurements. Briefly, Type I men had a cleardependence on insulin, a proneness to ketoacidosis, andsubnormal serum insulin and C-peptide values; Type IImen were managed without insulin or had not received

insulin for a number of years after diagnosis of diabetes,were not prone to ketoacidosis, and had normal or ele-vated serum insulin and C-peptide values.

Periodontal StatusPeriodontal status was assessed by a single examiner(SRS) equipped with 2.5 magnification surgical tele-scopes and a fiberoptic headlamp. One diabetic and one

non-diabetic subject were assessed each morning and theexaminer was unaware of the diabetes status of subjects.Six representative teeth were assessed for dental plaque.The periodontium of all teeth except third molars wasassessed for gingival color and swelling, bleeding uponprobing, probing depth, and clinical attachment level.Standardized Michigan O probes with Williams markingswere used. Plaque was assessed using the plaque indexof Silness and Loe.17 Gingival color and swelling were

assessed based on the criteria of the gingival index (GI)of Löe and Silness18 and designated as a modified GI. Thegingiva adjacent to four tooth surfaces (mesio-facial, fa-cial, disto-facial, and mid-lingual) was scored. To assess

bleeding the probe was inserted until resistance was feltbut not more than 2 mm and run gently along the sulcusin contact with the sulcular epithelium; scoring was ac-

cording to Cowell and colleagues.19 Probing depth wasmeasured from the gingival margin to the bottom of thecrevice and the greatest depth was noted for each of sixsites (mesio-facial, facial, disto-facial, mesio-lingual, lin-gual, and disto-lingual) and recorded to the next highestwhole millimeter. Clinical attachment level was calculatedby measuring from the margin of the gingiva to the iden-tified site of the cemento-enamel junction and subtractingthis measurement from the probing depth measurement;in the case of gingival recession, this measurement wasadded to the probing depth measurement. Intra-examinerreliability was tested by having the recorder draw a cardat the end of each subject's clinical assessment to deter-mine by chance which part, if any, of the assessment (ex-cept for bleeding) was to be repeated and in which quad-rant.

Statistical AnalysisData of diabetic and non-diabetic men were comparedusing Student r-test for unpaired data. A three-way anal-ysis of variance (ANOVA) was done to compare inter-actions between diabetic status, smoking status, and typeof diabetes (Type I or Type II). Pearson's correlation co-

efficients and values for multiple linear regressionswere performed with the appropriate software program.*

"Immuno Nuclear, Stillwater, MN.Isolab, Inc., Akron, OH. "Statistical Analysis System, SAS Institute, Inc., Cary, NC.

Volume 67Number 11 BRIDGES, ANDERSON, SAXE, GREGORY, BRIDGES 1187

Table 1. Characteristics of Diabetic and Non-Diabetic PopulationsAccording to Group*

Table 2. Unadjusted Periodontal Data for Total Teeth for DiabeticPatients According to Type and Their Respective Age-Matched Non-Diabetic Controls*

Non-Diabetic Diabetic(Non-Diabeticvs. Diabetic)

47.0 ± 1.657.1 ± 1.3

0.0001

Kg/m226.0 ± 0.625.7 ± 0.5

0.72

Age, yearsType IType IIP(I vs II)

Body mass index,Type IType IIP(I vs II)

Duration of diabetes, yearsType I NAType II NAP(I vs II) NA

Fasting blood glucose, mg/dLType I 98.1 ± 7.6Type II 101.1 ± 6.2P(I vs II) 0.76

Glycosylated hemoglobin, %Type I 5.4 ±

Type II 5.5 ±P(I vs II) 0.76

Serum insulin µ/mLType I 13.6 ±

Type II 14.0 ±P(I vs II) 0.87

Serum C-peptide, ng/mLType I 2.8 ±

Type II 3.0 ±P(I vs II) 0.64

0.30.2

2.01.6

0.20.2

47.5 ± 1.658.8 ± 1.2

0.0001

24.2 ± 0.628.8 ± 0.5

0.0001

14.9 ± 1.18.2 ± 0.90.0001

232.7 ± 7.6185.8 ± 6.1

0.0001

11.1 ± 0.39.2 ± 0.20.0001

11.7 ± 2.022.5 ± 1.6

0.0001

1.4 ± 0.23.8 ± 0.20.0001

0.850.33

0.030.0001

NANANA

0.00010.0001

0.00010.0001

0.480.0001

0.00010.003

Values are expressed as mean ± SEM for 46 Type I and 69 Type IInon-diabetic men and 46 Type I and 72 Type II diabetic men.

RESULTS

Characteristics of Study GroupsNon-diabetic men included 46 matched to the Type I di-abetes group and 69 matched to the Type II diabetesgroup (Table 1). Diabetic men included 46 with Type Iand 72 with Type II diabetes. Subjects were successfullyage-matched; thus, the ages of non-diabetic and diabeticmen were similar. Most of the men who volunteered forthis study were Caucasian and only 3.5% of non-diabeticand 6.8% of diabetic men were non-Caucasian. Type IIdiabetic men and their matched controls were signifi-cantly older than Type I diabetic and control men. Bodymass indices (BMI) were similar for the two groups ofnon-diabetic men. Type II diabetic men had significantlyhigher BMI than Type I men and age-matched non-dia-betic men. The duration of diabetes for Type I subjects,14.9 years, was significantly longer than for Type II di-abetes, 8.2 years.

Non-diabetic men had normal fasting plasma glucoseand glycosylated hemoglobin values. Fasting plasma glu-cose values were significantly higher in Type I than in

Measure Non-Diabetic Diabetic

(Diabetic vs.

Non-Diabetic)Plaque index

Type I 0.88 ± 0.06Type II 1.03 ± 0.05P(I vs II) 0.06

Gingival indexType I 0.45 ± 0.07Type II 0.52 ± 0.06P(I vs II) 0.43

Bleeding score

Type I 0.49 ± 0.04Type II 0.52 ± 0.03P(I vs II) 0.58

Probing depth, mm

Type I 2.91 ± 0.09Type II 3.15 ± 0.07P(I vs II) 0.03

Loss of attachment, mm

Type I 2.29 ± 0.16Type II 3.03 ± 0.13P(I vs II) 0.0003

Missing teeth, numberType I 2.22 ± 0.60Type II 4.93 ± 0.49P(I vs II) 0.0006

1.10 ± 0.061.29 ± 0.05

0.02

0.66 ± 0.070.76 ± 0.06

0.27

0.63 ± 0.040.66 ± 0.03

0.61

3.17 ± 0.093.33 ± 0.07

0.15

3.10 ± 0.163.61 ± 0.13

0.012

4.70 ± 0.606.86 ± 0.48

0.005

0.0140.001

0.0290.002

0.0140.003

0.0340.065

0.0010.002

0.0040.005

*Values are expressed as mean ± SEM for 46 Type I and 69 Type IInon-diabetic men and 46 Type I and 72 Type II diabetic men.

Type II diabetic subjects. Glycosylated hemoglobin val-ues were significantly increased in both groups of diabeticmen with Type I men having significantly higher valuesthan Type II men.

Serum insulin and C-peptide concentrations were nor-mal in both groups of non-diabetic men. Serum insulinconcentrations in Type I diabetic men were in the normalrange because of insulin injections required for their man-

agement. Type II diabetic men had significantly higherserum insulin values than non-diabetic men and Type Idiabetic men. Serum C-peptide values were significantlylower in Type I diabetic men than for non-diabetic men

and Type II men. Type II diabetic men had serum C-pep-tide values that were significantly higher than any othergroup.

Diabetes Effects on Periodontal StatusPlaque index (PI). Diabetic men had significantly higherPI than non-diabetic men for anterior teeth (P < 0.001),molars (P < 0.0002), and overall (P < 0.0001). As Table2 illustrates, Type I and Type II diabetic men had signif-icantly higher PI than non-diabetic men. PI was signifi-cantly related to age for diabetic (r = 0.267, < 0.01)and non-diabetic (r = 0.207, < 0.05) men. When PIwas adjusted for age, there were no significant differences

1188 DIABETES AND PERIODONTAL STATUS IN MENJ Periodontol

November 1996

p- 0001

Anteriore Premolare Molars Total Teeth

V/ Nondiabetic I I Diabetic

Figure 1. Mean loss of attachment by tooth type; Values are expressedas mean ± S.E.M.

5 P-.043 p-013

1 2 3 4 5

// Nondiabetic I I Diabetic

Figure 2. Age trend in loss of attachment by quintiles of age; values are

expressed as mean ± S.E.M.

between Type I and Type II diabetic groups and youngerand older non-diabetic groups. However, differences be-tween diabetic and non-diabetic men, including differ-ences between Type I and Type II diabetic men and theircontrol groups, persisted after adjustment for age.

Gingival index (GI). Diabetic men had significantlyhigher GI than non-diabetic men for anterior teeth (P <

0.0002), premolare ( = 0.009), molars ( < 0.0002),and overall (P < 0.0002). Both Type I and Type II dia-betic men had significantly higher GI than non-diabeticmen (Table 2). However, when GI was adjusted for PIthere were no significant differences between diabetic andnon-diabetic men.

Bleeding score (BS). Diabetic men had significantlyhigher BS than non-diabetic men for anterior teeth (P <

0.003), premolars (P = 0.003), molars (P < 0.0009), andoverall (P < 0.0007). Both Type I and Type II diabeticmen had significantly higher BS than non-diabetic men

(Table 2). When age comparisons were made, BS was not

significantly affected by age. However, when BS was ad-justed for PI there were no significant differences betweendiabetic and non-diabetic men.

Probing depth (PD). Diabetic men had significantlyhigher PD than non-diabetic men for anterior teeth (P <

0.0001), premolars (P = 0.048), and overall teeth (P =

0.0059). Type I, but not Type II, diabetic men had sig-nificantly higher PD than non-diabetic men (Table 2).However, when PD was adjusted for PI there were no

significant differences between diabetic and non-diabeticmen.

Loss of attachment (LA). Diabetic men had signifi-cantly greater LA than non-diabetic men for anteriorteeth, premolars, molars, and overall teeth (Fig. 1). BothType I and Type II diabetic men had significantly greaterLoA than non-diabetic men (Table 2). LA was signifi-cantly related to age for diabetic (r = 0.496) and non-diabetic (r = 0.467) men (Fig. 2). When LA was adjustedfor PI, Type I and Type II diabetic men still had signifi-cantly higher LA than non-diabetic men.

Missing teeth (MT). Diabetic men had significantlymore MT than non-diabetic men for anterior teeth (P <

0.05), molars (P < 0.0001), and overall (P < 0.005). BothType I and Type II diabetic men had significantly more

MT than non-diabetic men (Table 2). The number of MTwere significantly related to age for diabetic (r = 0.503)and non-diabetic (r = 0.519) men. After adjustment forage, significant differences in numbers of MT were stillpresent when diabetic were compared to non-diabeticmen. However, after adjustment for age, differences be-tween Type I and Type II diabetic men and younger andolder non-diabetic men were not significant.Correlations Between Smoking and PeriodontalStatusSmoking had a distinct effect on all parameters of peri-odontal status. Smoking diabetic men had higher averagescores for all six measures of periodontal status than theother three groups (i.e., smoking, non-diabetic; non-

smoking, diabetic; and non-smoking, non-diabetic). Forthe three-way ANOVA, smoking status had a significanteffect on GI, PD, and LA.

Table 3 summarizes the Pearson correlation coefficientsand the significant relations with multiple linear regres-sion analysis. Pearson correlation coefficients showed thefollowing significant relationships: in diabetic men, smok-ing was related to BS and PD while in non-diabetic men,smoking was related to PD and LA. Multiple linear re-

gression analysis indicated the following significant re-

lationships: in diabetic men, smoking was related to PI,BS, PD, and LA while in non-diabetic men, smoking was

related to BS, PD, and LA.

Age Effects on Periodontal StatusAge had differing effects on different parameters of peri-odontal status (Table 3). With Pearson correlation analysisthe following significant correlations were observed: forthe combined group of diabetic and non-diabetic men, age

Volume 67Number 11 BRIDGES, ANDERSON, SAXE, GREGORY, BRIDGES 1189

Table 3. Pearson Correlation Coefficients Between Independent Variables and Periodontal Status ofNon-Diabetic and Diabetic Subjects (statistically significant (P < 0.05) values are presented and non-

significant values are indicated by NS; significant values (P < 0.05) for multiple linear regressionanalysis are indicated by an asterisk)

Category/GroupPlaqueIndex

Gingival BleedingScore Score

ProbingDepth

Loss of MissingAttachment Teeth

AgeNon-diabeticDiabetic

Blood glucoseDiabetic

GlycohemoglobinDiabetic

IncomeNon-diabeticDiabetic

EducationNon-diabeticDiabetic

BrushingNon-diabeticDiabetic

FlossingNon-diabeticDiabetic

Dental care

Non-diabeticDiabetic

SmokingNon-diabeticDiabetic

0.210.27*

NS*

NS

-0.47*-0.27

-0.27*-0.22

-0.45*-0.26

-0.35NS

NS-0.20

NSNS*

NSNS*

0.20

NS

-0.38-0.29

-0.25-0.26*

-0.42-0.27

-0.39NS

-0.39*-0.20

NSNS

NSNS*

NS

NS

-0.24NS

NSNS

-0.41-0.25

-0.37*NS

-0.27NS

NS*0.26*

NSNS

NS

NS

-0.25NS

NS-0.24

NS-0.25*

-0.24NS

NSNS

0.25*0.23*

0.47*0.50*

NS

NS*

-0.42NS*

-0.34-0.36*

NSNS

NSNS

-0.19*NS

0.34*NS*

0.52*0.50*

NS

NS

-0.43*-0.24

-0.36-0.32

NSNS

-0.24NS

NS-0.23*

NSNS

*Multiple linear regression analysis significant.

was correlated to PI, Gl, BS, LA, and MT (data not

shown); for diabetic as well as non-diabetic men age was

correlated with PI, LA, and MT (Table 3). With multipleregression analysis, the following significant correlationswere observed: for the combined group of diabetic andnon-diabetic men, age was correlated with PI, Gl, BS,LA, and MT (data not shown); for diabetic men, age was

correlated with PI, Gl, BS, LA, and MT; and for non-

diabetic men, age was correlated with LA and MT (Table3).

Duration of Diabetes and Periodontal StatusDuration of diabetes was not significantly related to mea-

sured parameters of periodontal status with either thePearson correlation coefficients or with multiple linear re-

gression analysis.

Glycémie Control Effects on Periodontal StatusGlycémie control, assessed by fasting serum glucose mea-

surements and glycohemoglobin values, was not closelylinked to periodontal status. For diabetic men, GI was

significantly related to blood glucose (Table 3) but to noother periodontal variable with Pearson analysis. For di-abetic men, LA was significantly related to glycohemo-

globin (P < 0.05) but to no other periodontal variablesby multiple linear regression analysis.Socioeconomic Effects on Periodontal StatusIncome and education were associated, in a negative man-

ner, with periodontal status for both diabetic and non-diabetic men. For income, Pearson analysis indicated thefollowing significant correlations (Table 3): for diabeticmen income was correlated with PI, GI, and MT; for non-diabetic men, income was correlated with PI, Gl, BS, PD,LA, and MT. Multiple regression analysis indicated thefollowing significant correlations (Table 3): for diabeticmen, income was correlated with LA only and for non-

diabetic men, income was correlated with PI and MT. Foreducation, the pattern of correlations were similar to in-come.

The self-reported frequency of brushing teeth was neg-atively related to several parameters of periodontal status.For brushing, Pearson analysis indicated the followingsignificant correlations (Table 3): for diabetic men brush-ing was negatively correlated with PI, Gl, BS, and PD;for non-diabetic men, brushing was negatively correlatedwith PI, GI, and BS. Multiple regression analysis indi-cated the following significant correlations (Table 3): for

1190 DIABETES AND PERIODONTAL STATUS IN MENJ Periodontol

November 1996

diabetic men, brushing was negatively correlated with PDonly and for non-diabetic men, brushing was negativelycorrelated with PI only. The self-reported frequency offlossing was negatively correlated to most parameters ofperiodontal status (PI, Gl, BS, PD, and MT) in non-dia-betic men but not in diabetic men (Table 3). The historyof dental care, likewise, had a negative correlation withseveral parameters of periodontal status (Table 3).

DISCUSSIONThis study demonstrated that diabetic men at this VAMedical Center had more severe periodontal disease thanmatched, non-diabetic men. Men with Type I and II di-abetes had significantly higher plaque index, gingival in-dex, bleeding score, probing depth, loss of attachment,and missing teeth than age-matched non-diabetic men.Men with Type II diabetes and their age-matched controlshad more periodontal disease than men with Type I dia-betes but these differences were largely corrected by ad-justment for age.

Smoking was associated with significant increases inmeasures of periodontal disease. Smoking men with di-abetes had significantly higher measurements for all pa-rameters of periodontal status; smoking, non-diabetic menhad significantly higher values for probing depth and lossof attachment. Smoking was significantly and positivelycorrelated with bleeding score, probing depth, and loss ofattachment. Age was significantly and positively corre-lated with plaque index, loss of attachment, and missingteeth. Income and education were significantly and neg-atively correlated to most parameters of periodontal sta-tus. Likewise, history of brushing, flossing, and dentalcare were significantly and negatively correlated to mostparameters of periodontal status. We did not observe im-portant differences between non-diabetic and diabeticmen with respect to the effects of socioeconomic mea-

sures or history of dental care.Numerous research investigators3-13'20"31 have examined

the periodontal status of diabetic and control subjects. Aquantitative statistical analysis (meta-analysis) may be re-

quired to carefully assess the impact of diabetes on var-ious assessments of periodontal status;32 we will provideonly a qualitative evaluation. Since the report of Cianciolaand colleagues,3 most, but not all, investigators have re-

ported that diabetic subjects had significantly more peri-odontal disease than matched, non-diabetic control sub-jects.

Glycémie control, as measured by fasting plasma glu-cose and glycohemoglobin values, was not correlatedwith the severity of periodontal parameters in our sub-jects. While some investigators20'2 '·23·29·30 reported a sig-nificant relationship between periodontal disease and gly-cémie control, others410-27'31 failed to observe a significantassociation. We did not observe a significant relationshipbetween periodontal status and duration of diabetes; some

investigators5 noted a significant association while oth-ers410 did not.

Our observations that plaque index, gingival index, andbleeding score were significantly higher in diabetic thannon-diabetic men confirm the observations of some priorinvestigators.4-6-8-11-25 Other investigators20-24-27 did not findsignificant differences between diabetic and non-diabeticsubjects for these parameters.

These results indicating that probing depth and loss ofattachment were significantly greater in diabetic than non-diabetic control subjects confirm the reports of some priorinvestigators.4-7-8 "12 However, others5-6-24-27 did not findsignificant differences between diabetic and non-diabeticsubjects for these parameters. Two groups911 reported in-creased bone loss in diabetic subjects while two others5-6noted no significant differences.

Diabetic individuals had a significantly greater numberof missing teeth in our study. Three groups8-26-28 notedincreased numbers of missing teeth while threegroups51112 reported no significant differences.

All controlled studies published since 1990s-12-28-30 havereported significant differences for at least one parameterof periodontal disease between diabetic and non-diabeticpatients. However, it is difficult to compare results be-tween studies because of many differences, which includesize of population, selection criteria for both diabetic andnon-diabetic groups, glycémie control, types of periodon-tal assessments performed, number of examiners, blindingof examiners, intra- and inter-subject variance in mea-

surements, and the role of other factors such as smokingand level of prior dental care.

An association between smoking and periodontal dis-ease has been suspected for a number of years.33-34 Thenumerous clinical investigations that have examined theperiodontal status of smokers and non-smokers will notbe reviewed here. In this study we noted that the risk forperiodontal disease was significantly higher for diabeticindividuals who smoked than for any other group.

Diabetes has been linked to increased susceptibility to

periodontal disease in a number of hypotheses. Sugges-tions regarding the link between diabetes and periodontaldisease include these: altered polymorphonuclear leuko-cyte (PMN) function35-37 or other alterations in host de-fenses in diabetes;14-38 microvascular changes impairinggingival metabolism and defenses;39-41 a unique popula-tion of subgingival microflora;31-42"44 altered collagen me-tabolism with increased collagenase activity;45 altered mi-croenvironment in the crevicular space in diabetes;46 andincreased susceptibility to osteopenia in diabetes.47 Theeffects of diabetes on the lymphocyte-macrophage-cyto-kine axes, reactive oxygen production and effects, ara-chidonic acid metabolites, proteolytic enzymes, and otherlocal factors are unclear.48 Most likely, several interactingfactors such as altered PMN function and derangementsof inflammatory protein responses converge at the peri-

Volume 67Number 11 BRIDGES, ANDERSON, SAXE, GREGORY, BRIDGES 1191

odontium to result in a higher prevalence and severity ofPeriodontitis. State-of-the-art molecular biology tech-niques to assess PMN function and inflammatory proteinresponses may be required to shed further light on thisarea. Much more research is required to delineate the con-tribution of these and other factors to the pathogenesis ofaccelerated Periodontitis in diabetes.

In conclusion, this study confirms previous controlledstudies indicating that diabetes increases the prevalenceand severity of Periodontitis. Smoking also increases theprevalence and severity of Periodontitis. In this studygroup neither the duration of diabetes nor the degree ofglycémie control had a significant effect on periodontalstatus. Advances in the understanding of mechanisms re-

sponsible for increased severity of Periodontitis in dia-betes will require innovative investigation to unravel mul-tiple interacting factors.

AcknowledgmentsThis article is dedicated to Dr. Bridges who died January27, 1992. This research was supported by grants from theNational Institute of Dental Research (DE05990) andfrom Hoffmann La Roche, Inc., Nutley, NJ. We gratefullyacknowledge Drs. Hartley McKean and Mary Kay Ray-ens for the statistical analysis and Ms. Melanie Reynoldsfor assistance in collection of patient data.

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Send reprint requests to: Dr. James W. Anderson, Medical ServiceUIC, VA Medical Center, Leestown Road, Lexington, KY 40511.

Accepted for publication April 4, 1996.

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