JAD)A R E S E A R C H
R E P O R T S
The relationship between type 2 diabetes mellitus and periodontal disease was evaluated in 2,878 Pima Indians of the southwestern United States. Two independent measures of periodontal disease, probing attachment loss and radiographic bone loss, were used to compare prevalence and severity o f periodontal disease in diabetic and nondiabetic subjects. In all age groups studied, subjects with diabetes had a higher prevalence of periodontal disease, indicating that diabetes may be a risk factor fo r periodontal disease.
Type 2 diabetes mellitus and periodontal disease M a rc S h lo ssm a n , D D S, MS; W illiam C . K now ler, M D , D rP H ; D av id J . P e ttitt, M D ; R o b e r t J . G e n c o , D D S, P h D
e n tists fre q u e n tly tr e a t p a tie n ts with chronic systemic conditions, such as diab etes, th a t can affect th e c o u r s e a n d m a n a g e m e n t o f p e r i o d o n ta l d is e a s e . S y stem ic d ise a se is c o n sid e re d a c o n trib u tin g fac to r r a th e r th a n th e p rim a ry etiologic facto r in th e i n it ia t io n o f p e r io d o n t itis . D ia b e te s m ellitu s is a ch ro n ic m etabolic diso rd er th a t a f f e c ts c a r b o h y d r a te a n d lip id metabolism. T he term diabetes m ellitus encompasses a g r o u p o f g e n e tic a lly a n d c lin ic a lly h etero g en o u s disorders in w hich glucose in to l e r a n c e is f o u n d . S ta n d a r d iz e d term inology, classification, an d diagnostic criteria have been established1-2 to provide greater consistency for th e description o f this disorder. Two m ajor types o f diabetes are identified. Approxim ately 80%-90% o f persons with diabetes in the U nited States h av e ty pe 2 o r n o n in s u lin - d e p e n d e n t diabetes mellitus and 10%-20% have type 1 o r in su lin-dependent diabetes mellitus. Type 1 diabetes is c h a racterize d by islet c e ll d e s tr u c tio n a n d is d e p e n d e n t on exogenous insulin for survival. In contrast, in ty p e 2 d ia b e te s , in s u lin a c tio n is im paired, with at least some preservation o f in s u lin s e c r e tio n , a lth o u g h in s u lin injections are often useful in treatm ent. T h e p r e v a le n c e s o f b o th p e r io d o n ta l
D
5 3 2 ■ JADA, Vol. 121, O cto b er 1990
disease an d type 2 diabetes increase with age. P atie n ts w ith d ia b ete s m e llitu s are su sceptible to n u m e ro u s co m p licatio n s, both chronic an d acute. T h e c o n c e p ts o f p e r io d o n ta l disease e p id e m io lo g y a n d p a th o g e n e s is a re c h a n g in g . T h e id e a th a t p e r io d o n t a l d ise ase is w id e s p re a d a n d is se e n as a single form o f disease is cu rren tly being challenged by the systemic studies done in the past 20 years.3.4 R ecent epidem iologic su rv ey s in d ic a te t h a t o n ly a sm a ll p e rc e n ta g e (75% -15% ) o f a p o p u la tio n m ay be a ffe c te d by sev ere p e r io d o n ta l
d is e a s e .4-6 I d e n ti f ic a t io n a n d c h a r a c te r iz a tio n o f h ig h - ris k g r o u p s o r individuals w ith g re a te r susceptibility to se v ere p e r io d o n titis a re n e e d e d . T h is p a p e r p r e s e n ts c ro ss-se c tio n a l d a ta o f periodontal disease in a population with a high prevalence o f type 2 diabetes. M ethods and m aterials F o r 3,219 su b je cts fro m th e G ila River In d ia n C o m m u n ity , A riz, s ta n d a rd iz e d clinical exam inations were perform ed; of these, 2,878 had d ata from a b o n e score,
Table 1 ■ Distribution of subjects by age, gender, and diabetes. No. o f subjects Age (years) 5-24 25-44 > 45 Total Total
G ender*
N ondiabetic
Diabetic
Total
Diabetes prevalence (%)
M F M F M F M F Total
753 871 241 429 82 107 1,076 1,407 2,483
22 55 120 184 122 263 264 472 736
775 896 361 613 204 370 1,340 1,879 3,219
3 3 33 30 60 71 20 25 23
* M = m ale, F = fem ale.
r
R E S E A R C H
R E P O R T S
Non diabetic subjects Age (years)
5 -2 4
>45
2 5 -4 4
96 7
n =622
n = 187
60-
Fig 1 ■ D istrib u tion o f m e 40-
dian probing attachm ent loss: )5 5
Ü s 09
171
M = m is s in g th r e e or m ore in d e x te e th ; E d e n t = fu lly
14
0 5
0 5
edentulous. The shaded areas represent subjects with “severe disease”: > 6.0 mm PAL, M, or
Diabetic subjects
a> >
Edent.
n =291
49 5
18 9 14.4
0
1-2
_
86
3-4
M
66
E cU n t
0
1-2
M
3-4
E d *n t
M edian probing attachment loss (mm)
Non diabetic subjects A ge (years)
.no
> 45
2 5 -4 4
5 - 24
9»-9 n * 1044
£ >% O
F ig 2 ■ D istrib u tion o f m e 06
dian alveolar b on e loss: M =
06
m is s in g 14 or m o re te e th ; Edent = fully edentulous. The 09 >
sh a d e d areas rep re sen t su b
Diabetic subjects
j e c t s w ith “s ev e r e d is e a s e ” : > 2.0 b o n e lo ss sco r e , M, or Edent.
0
1-2
3-6
>6
M
Ed *n t
0
1-2
3-6
>6
M
Ed*nt
0
1-2
3 -6
>6
M
Ed«nt
Median bone loss score
p r o b in g e x a m in a tio n , o r b o th , as d e s c r ib e d h e r e . M ost r e s id e n ts o f th e com m unity are Pim a o r Papago Indians, m em bers of two closely related tribes, with the w orld’s highest rep o rted prevalence of type 2 diabetes mellitus and in which type 1 diabetes is unknow n.7 T he participants
o f th e s tu d y w e re r e c r u i t e d fro m a longitudinal survey o f diabetes an d other c h r o n ic d is e a s e s , w h ic h h a s b e e n in progress since 1965. Approxim ately every 2 years, each m em b er of the com m unity older than 5 years is asked to participate in a standardized biennial exam ination7 that
in c lu d e s a m e d ic a l h is to ry , p h y sic a l exam ination, glucose tolerance test, an d a dental exam ination. P e r io d ic d e n ta l e x a m in a tio n s w ere in it ia t e d in F e b r u a r y 1 983. E ach e x a m in a tio n in c lu d e d a p a n o r a m ic rad io g rap h (Siem ens OP-IO), evaluation JADA, Vol. 121, O cto b er 1990 ■ 533
I R E S E A R C H
R E P O R T S
o f the oral m ucous m em branes by visual an d digital exam ination, and recording o f d ec ay e d , m issing, a n d fille d te e th . Six index teeth or their substitutes8 were used f o r th e p e r io d o n t a l e v a lu a tio n th a t in clu d ed plaque index,» gingival in d e x ,1“ a n d calculus index (presence o r absence o f supra- o r subgingival calculus). P robing pocket d ep th s w ere m easured to the nearest m illim eter from the gingival m argin with calibrated periodontal probes (PCP-10, Hu-Friedy). P robing attachm ent lev el to th e n e a r e s t m illim e te r was m e asu red w ith c a lib ra te d p ro b es as th e d is ta n c e b e tw e e n th e c e m e n to e n a m e l ju n c tio n (CEJ) and the base of the pocket. M easu rem ents o f p ro b in g p o ck e t d ep th w ere p e r f o rm e d a t six sites p e r to o th : m e s io b u c c a l, m id b u c c a l, m id lin g u a l, m e s io lin g u a l, d is to b u c c a l, a n d d isto lin g u al. P ro b in g a tta c h m e n t levels were m e a s u r e d a t f o u r site s: m id b u c c a l, m id lin g u al, an d th e d e e p e st m esial and distal interproxim al points. T h e panoram ic films were evaluated for p a th o sis a n d u se d to d e te r m in e in te r p r o x im a l c r e s ta l a lv e o la r b o n e loss. A lveolar b o n e loss was m e asu red with a m odified Schei ruler.11 This was scored as a percen tag e o f b o n e loss from th e CEJ to th e a p e x a t th e d e e p e s t p o in t o n th e m e sia l o r d is ta l s u rfa c e o f e a c h to o th present, excluding third molars. Bone loss score o f 0 in d icates no radiographically detectable bone loss; 1 = 1% to 24% bone loss; 2 = 25% or 49% bo n e loss; 3 = 50% to 74% b o n e loss; a n d 4 = 75% o r m o re b o n e lo ss. A ll e x a m in a tio n s w e re c o n d u c te d from F eb ru ary 1983 th ro u g h Ja n u a ry 1988 by a single exam iner (MS) w ithout knowledge o f a p atien t’s diabetes s ta tu s . All d a ta p r e s e n te d a r e cro ssse ctio n al. F o r su b je cts seen m o re th a n o n c e , o n ly th e in itia l e x a m in a tio n is included. P atient data could be excluded from a p a rtic u la r m e a su re fo r specific reaso n s including: p atien t refusal (no radiograph o r p robing), pregnancy (no radiograph), h e a r t c o n d itio n s r e q u ir in g a n tib io tic p r o p h y la x is ( n o p r o b in g ) , m ix e d dentition (no bone loss score), equipm ent f a ilu r e ( n o r a d i o g r a p h ) , in a b ility to p o sitio n p a tie n t (n o ra d io g ra p h ) o r no c lin ic a l e x a m in a tio n (n o p r o b in g ) . A radiographic exam ination was perform ed by a trained dental assistant for all eligible patients even when a clinical exam ination was n o t d o n e . O f th e 3 ,2 1 9 p e r s o n s e x a m in e d , p r o b in g e x a m in a tio n s w ere p e rfo rm e d o n 2,304, b o n e scores w ere available from 2,718, and 2,878 had one or both o f these exam inations. 5 3 4 ■ ADA, Vol. 121, O cto b er 1990
T he b iennial ex am in atio n includes an o r a l g lu c o s e to le r a n c e te s t. A fa s tin g plasma sam ple is taken, the patien t ingests 75 g o f carbohydrate (Glucola Ames Co) an d a seco n d p lasm a sam p le is tak en 2
hours later for glucose analysis. T he results o f this test are used to diagnose diabetes.2 Diabetes is diagnosed in any patient if the 2-hour postload plasm a glucose is > 11.1 m mol (200 m g /d L ) or if in the course of
Non diabetic subjects
Diabetic subjects
' I 7 ' l 6 ' l 5 ' U ' l 3 ' l 2*11 ' 2 r 2 2 ' 2 3 ‘ 2 4 ' 2 5 ' 2 6 ' 2 7 ‘
’ l 7 ' l 6 1 S ' l 4 ' l 3 ' l 2 ' 1 1 ' 2 1 2 2 2 3 24 2 8 * 2 4 ' 2 7
n = 1190
n = 43
4 7 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 3 4 3 5 36 37
4 7 4 6 4 5 44 4 3 4 2 4 1 31 3 2 3 3 3 4 35 3 6 37
17 16 15 14 13 12 11 21 2 2 2 3 24 2 5 2 6 2 7
17 16 15 14 13 12 11 21 22 2 3 2 4 2 5 2 6 2 7
>w — o
'5 o
2 CM o LO
o 3
£> V
c o
n « 266
n = 619
>-
5 X O
II..... .
If)
CM
.Q T3 C
o 2
100 in
4 7 4 6 4S 4 4 4 3 4 2 41 31 32 3 3 34 35 3 6 37
47 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 3 4 3 6 36 37
17 16 I S 14 13 12 11 21 2 2 23 24 2 5 2 6 27
17 14 I S 14 1 3 12 11 21 2 2 2 3 24 2 6 2 6 27
n = 1S5
n * 209
47 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 34 3 5 3 6 37
47 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 3 4 3S 3 6 37
k—
o K o 2 i/> Al
D &
o -
(V o>
< Tooth number
Fig 3 ■ Distribution o f interproxim al alveolar bone loss by tooth. The shaded areas represent the percent o f teeth affected by 25% or more bone loss determ ined by m easurem ent from panoramic radiographs.
R E S E A R C H
routine m edical care a fasting, casual, o r 2h o u r p o stlo a d p la sm a g lu c o se c o n c e n tr a tio n >11.1 m m o l is d o c u m e n te d , as described.7 All dental exam inations were p erform ed by a single exam iner (MS). Thirty subjects exam ined at a biennial exam ination were recalled within 14 to 21 days for duplicate e x a m in a tio n s (p ro b in g a tta c h m e n t loss an d radiographic evaluation) to establish in traex am in er reproducibility, w hich was assessed by the kappa statistic.12 T he kappa statistics for probing attachm ent loss and bone loss were 76% an d 88%, respectively. T he associations betw een various dental co n d itio n s an d diabetes, co n tro llin g for c o n f o u n d in g by a g e w ere a sse ss e d in th re e -w a y c o n tin g e n c y ta b le s .13 T h e m e d ia n p r o b in g a t ta c h m e n t lo ss a n d m e d ia n alv eo la r b o n e loss sc o re s w ere u s e d as two m e a su re s o f p re s e n c e a n d severity o f p e rio d o n ta l disease. P ro b in g a tta c h m e n t level m easures fo r all in d e x te e th w ere a n a ly z e d a n d a m e d ia n attac h m e n t loss was established fo r each subject. For this analysis, a missing tooth w as a s sig n e d a v a lu e h ig h e r th a n th e m axim um recorded m easurem ent so that even edentulous patients o r patients with m issing in d e x te e th co u ld be in c lu d ed . Alveolar b o n e loss was m easu red fo r all te e th p re s e n t, a n d a m e d ia n b o n e loss sc o re was c o m p u te d fo r e a c h p a tie n t. M issing te e th w ere assig n ed a v alu e o f higher th an the m axim um score, again to in clu d e m issing te e th in com p u tatio n of the m edian. A p r e o p e ra tiv e r a d io g r a p h ic e x a m in a tio n a n d c h a r t rev iew f ro m 100 r a n d o m ly s e le c te d p a tie n t r e c o r d s o f subjects w ho h a d lost te e th b efo re th e ir initial oral health survey was com pleted to d e t e r m in e r e a s o n s f o r to o th loss. R ad io g raphs from p atien ts who becam e e d e n tu lo u s d u r in g th e stu d y w e re evaluated for bone loss and caries.
Results T h e distribution o f the subjects according to age, gender, a n d diabetes is shown in T a b le 1. T h e p r e v a le n c e o f d ia b e te s increased with age from 3% in th e 5- to 24y ear g ro u p to 60% in m en a n d 71% in women aged > 45 years. T h e review o f preoperative radiographs an d dental records from patients who had lost teeth before th e ir initial o ral h ealth survey show ed th a t 72% o f to o th losses w ere th e re s u lt o f p e rio d o n ta l disease. Preoperative radiographic exam inations in 28 patients who lost their rem aining teeth d u rin g th e course o f th e study revealed
th a t 95% o f th e e x tr a c tio n s w e re th e results o f periodontal disease, an d 51% o f th e te e th h ad lo st a t le ast 75% o f th e ir b one support. Only 5% o f th e teeth were extracted because o f severe decay. T he frequency distributions o f m edian probing attachm ent loss (PAL) are shown in Figure 1. T he distributions were shifted toward m ore perio d o n tal disease at older ages an d am o n g th o se w ith d ia b ete s in ea ch age g ro u p . T h e p rev a len c e o f th e m ost healthy PAL category (m edian PAL = 0, indicating th at at least h alf the sites had n o evidence o f a tta c h m e n t loss) ran g ed from 99% to 27% in th e th ree age groups am ong the nondiabetic subjects an d from 88% to 12% am ong those with diabetes. T h e p r e v a le n c e o f e d e n tu lo u s n e s s in c r e a s e d w ith ag e f ro m 0% to 21% am ong nondiabetic subjects an d from 0% to 58% am ong diabetic subjects. In th e age g ro u p s 25-44 a n d > 45 y ea rs, th e PAL frequency distributions w ere significantly d if f e r e n t b e tw e e n d ia b e tic a n d n o n d ia b etic subjects (by C h i2, P < 0.001 in each age group). Controlling for age, the su m m a ry C h i2 f o r th e a s s o c ia tio n o f d ia b e te s w ith PAL was 185, d f = 5, P < 0.001. T he frequency distributions o f m edian alveolar bone loss scores (BUS) are shown in F ig u re 2. T h e p r e v a le n c e o f th e h e a lth ie s t c a te g o ry ( m e d ia n BLS = 0, indicating that at least h alf the teeth had no evidence o f bone loss) decreased from 97% to 7% in n o n d ia b e tic subjects an d from 79% to 2% in diabetic subjects with in c r e a s in g ag e . T h e p r e v a le n c e o f edentulousness increased from 0% to 17% in no n d iab etic subjects an d from 0% to 45% in diabetic subjects w ith increasing ag e . In all th r e e ag e g r o u p s , th e BLS frequency distributions in diabetic subjects were significandy d ifferen t from those in nondiabetic subjects (P < 0.01). C ontrol lin g f o r a g e , th e s u m m a ry x2 f o r th e association o f diabetes with BLS was 218, df= 4, P< 0.001. Figure 3 illustrates th e g re a te r loss o f in te rp ro x im a l alveolar b o n e in subjects w ith d ia b e te s th a n in su b je c ts w ith o u t d iab etes, as w ell as th e e a rlie r o n se t o f alveolar bone loss in those with diabetes. Bone loss was g reatest in th e m o lar and in c is o r s e g m e n ts in th e y o u n g e r age groups, b u t there was a m ore generalized pattern in older age groups.
Discussion T h e P im a In d ia n s o f th e so u th w e ste rn U n ited States have th e h ig h est re p o rte d incidence an d prevalence o f d iab etes in
R E P O R T S
th e w orld. Fifty p e r c e n t o f th o se o ld e r th a n 35 years a re a f f e c te d .714 D iab e te s m ellitus in this p o p u la tio n is exclusively ty p e 2 1516 a n d is a s s o c ia te d w ith c o m plications at rates similar to those o f oth er populations. C onsiderable research d ealing with the relatio n sh ip o f d iab etes an d p e rio d o n tal d ise ase h as b e e n p u b lis h e d .1723 U n fo r tunately, th e fin d in g s have b e e n in c o n sistent. C on trad icto ry d ata have failed to e s ta b lis h a n a s s o c ia tio n b e tw e e n th e periodontal status o f diabetic subjects and the nondiabetic controls. O th er studies do n o t specify the type o f diabetes p resen t or include only patients with type 1 diabetes, while type 2 diabetes accounts fo r 80% of diabetic cases today. Diabetes mellitus encom passes a variety o f d is o r d e r s th a t d if f e r in th e ir p a th o g e n e s is a n d n a tu ra l h isto ry . I t is im p o r ta n t to u se c o m m o n ly a c c e p te d te rm in o lo g y a n d s ta n d a r d iz e d classif ic a tio n a n d d ia g n o s tic c r i t e r i a w h e n d e s c rib in g su b je cts w ith g lu c o se in to l erance. In some previous reports, uniform criteria were lacking for the diagnosis and classification of diabetes an d p erio d o n tal disease. T h e a g e s p a n a n d th e n u m b e r s o f d ia b e tic a n d n o n d ia b e ti c s u b je c ts e x a m in e d in th is stu d y a r e m o re com prehensive an d extensive th a n those rep o rted in previous studies.192223 A wide variety o f clinical in d ex es have b ee n used to estim ate th e prevalen ce o f periodontal disease in past epidem iologic s tu d ie s . In p re v io u s s tu d ie s , th e p e r i o d o n ta l statu s o f p a tie n ts w ith d ia b ete s m ellitu s has b e e n assessed w ith clinical p a r a m e te r s b a s e d o n th e s ig n s a n d sy m p to m s o f p e r io d o n t a l d is e a s e a n d fa c to rs th o u g h t p r e d is p o s in g to p e r i odontitis.23-26 Today, quantitative m easures o f p eriodontal disease are used to m onitor a n d d e te c t p e r io d o n titis . S ev ere p e r i o d o n titis has recently b e e n d e fin e d as a loss o f attachm ent o f 6 m m o r m ore at one o r m o r e s ite s .6 R a d io g r a p h ic q u a n tific a tio n o f crestal b o n e h e ig h t is also v alu ab le in e v a lu a tin g th e p e r io d o n ta l s u p p o r t o f t e e t h . 27 R e lia b ility a n d r e p r o d u c ib ility o f m e a s u r e m e n ts a re essential to their inco rp o ratio n in a study. A tta ch m e n t loss by p ro b e m e a su re m e n t a n d b o n e loss by ra d io g rap h ic m easu re m e n t a r e th e tw o p r im a r y c lin ic a l assessments used to indicate the presence o f periodontal disease.2» Tooth loss in this pop u latio n is prim arily caused by p e rio d o n ta l d e s tru c tio n . T his finding is n o t unique to this p opulation,2« b u t e v id e n c e h as b e e n p r e s e n te d th a t JADA, Vol. 131, October 1990 ■ 535
R E S E A R C H
R E P O R T S
p eriodontal disease is n o longer the m ajor c a u s e o f to o th lo ss in a d u l ts .30 D a ta g ath ered from p re tre a tm e n t radiographs a n d c h a r t review show to o th loss as a fu rth e r indicator o f destructive periodon titis. F o r th is re a so n , m issing te e th are in c lu d ed in this analysis o f p erio d o n titis an d , fo r p urposes o f co m p u tin g m edian values, are given a value h ig h e r than the m easured m axim um . T h e cross-sectional data presented show th a t th e prevalence o f periodontal disease is g reater in persons with type 2 diabetes. T his conclusion is based on two separate q u a n tita tiv e m e a s u r e s o f p e r io d o n t a l d e s t r u c t i o n th a t c a n b e p e r f o r m e d in d e p e n d e n tly : th e loss o f p e rio d o n ta l a tta c h m e n t a n d loss o f in te r p ro x im a l crestal alveolar bone. F urtherm ore, these s tu d ie s h a v e sh o w n th a t p e r io d o n t a l disease occurs at an earlier age in persons with type 2 diabetes. T h e c u rre n t study has several strengths f o r e v a lu a tin g th e im p lic a tio n th a t p e rio d o n ta l disease is a com plication o f diabetes. O ne asset is th e large n um ber o f s u b je c ts e x a m in e d a n d e v a lu a te d . In a d d i tio n , th e s tu d y w as m a sk e d . T h e p e rio d o n ta l e x a m in e r d id n o t know the d ia b etic status o f subjects, a n d diabetes w as d ia g n o s e d o b je c tiv e ly by g lu c o se tolerance testing. Also, this population has an extrem ely high prevalence o f diabetes, w hich allowed for a large n u m b e r (736) o f diabetic subjects to be studied. Finally, two m e an s o f m e a su rin g p e rio d o n titis w ere used: th e assessm ent o f a tta c h m e n t loss fro m th e c e m e n to e n a m e l ju n c tio n , an d th e m e a s u r e o f in te r p r o x im a l c re s ta l a lv e o la r b o n e lo ss. B o th q u a n tita tiv e m easures, although correlated, were used independently. T hey are well accepted as in d ic ato rs o f d estru ctiv e p erio d o n titis.28 U sing e ith e r m easure, th e prevalence o f p e r io d o n ta l d ise ase was clea rly h ig h e r am ong diabetic subjects. Localization of alveolar b o n e loss shows th a t in th e y o u n g er age g ro u p s th e first m olars a n d incisors were p redom inantly a f f e c te d , c o n s is te n t w ith o th e r e p id e m io lo g ic s tu d ie s .5’31 H o w ev er, w ith a d v a n c in g ag e a n d m o re se v e re p e r i o d o n tit is , th e p a t t e r n w as m o r e generalized.
Conclusions T hese findings, along with earlier studies a s s o c ia tin g p e r io d o n t itis a n d ty p e 1 diabetes in teenagers an d young adults3233 suggest th a t periodontitis is a com plication o f b oth type 1 and type 2 diabetes mellitus. I f so,' t h e r e a r e s ig n if ic a n t c lin ic a l 536 ■ JADA, Vol. 121, October 1990
im plications th a t d iab etes may be a risk f a c to r fo r d e v e lo p m e n t o f p e r io d o n ta l d ise ase . T h is h y p o th e sis will b e in v e s tigated in th e lo n g itu d in al phase o f this study. ---------------------- J'A O A -----------------------
The inform ed consent o f all hum an subjects who p a r tic ip a te d in th e e x p e r im e n ta l in v e s tig a tio n reported or described in this manuscript was obtained a fte r th e n a tu re o f th e p r o c e d u r e a n d p o s s ib le discomforts and risks had been explained fully. This study was supported in part by USPHS Grant D E 0 6 5 1 4 fro m th e N a tio n a l I n stitu te o f D e n ta l Research, NIH, Bethesda, MD 20205. The authors thank the Gila River Indian community fo r its c o o p e r a tio n an d p a r tic ip a tio n a n d th e physicians, technical, and clerical staff o f the Diabetes and Arthritis Epidemiology Section, National Institute o f Diabetes and Digestive and Kidney Diseases, and the Indian H ealth Service, Phoenix Area; Ana CabreraArevalo, Robert Dunford, and Dr. Lawrence Emrich for their statistical and computer analysis; Joyce Moyah a n d S h a n n o n Irw in fo r p a t ie n t care an d data collection; Drs. Lars Christerson, Lynn Budding, and R ich a rd D u n n fo r th e review an d c o m m e n ts concerning the manuscript; Dr. Peter B ennett for his advice and support; and Dr. Anthony A. Rizzo for his advice and encouragem ent from the inception o f this study. Dr. Shlossman is assistant professor or oral biology, SUNY-Buffalo School o f Dental M edicine, and is in priv a te p r a c tic e , C h an d ler, AZ. Dr. G e n c o is distinguished professor and chairman, department o f oral biology at SUNY; Dr. Knowler is c h ie f and Dr. P e ttitt is a ssista n t c h ie f, d ia b e te s a n d a rth ritis epidem iology section, National Institute o f Diabetes and Digestive and Kidney Diseases, Phoenix,. Address req uests for reprints to Dr. G en co, 3435 M ain St, FosterHall-135, Buffalo 14214.
1. National Diabetes Data Group. Classification and diagnosis o f diabetes and other categories o f glucose intolerance. Diabetes 1979;28:1039. 2. World Health Organization, Expert C om m ittee o n Diabetes. Second Report. 1980 Technical Report Service No. 646, Geneva. 3. Burt BA. Public health im plications o f recent research in periodontal diseases. J Public Health Dent 1988;48:252. 4. Johnson NW, et al. Detection o f high-risk groups and individuals for periodontal diseases. Evidence for the existence o f high-risk groups and individuals and app roaches to th eir d e tectio n . J Clin P eriod on tol 1988;15:276. 5. Loe H, Anerud A, Boysen H, Morrison E. Natural h isto r y o f p e r io d o n ta l d is e a se in m an . J C lin Periodontol 1986;13:431. 6. N a tio n a l In stitu te o f D e n ta l R esearch , Oral h ea lth o f US adults. T he N ation al Survey o f Oral Health in US Employed Adults and Seniors: 1985-1986. National findings; 1987 NIH publication no. 87-2868. 7. Knowler WC, Bennett PH, Hamman RF, Miller M. Diabetes incidence and prevalence in Pima Indians: A 19-fold greater incidence than in Rochester, Minn. Am J Epidemiol 1978;108:497. 8. Ramfjord SP. Indices for th e prevalence and in c id e n c e o f p e r io d o n ta l d is e a se . J P e r io d o n to l 1959;30:51.
9. S iln e ss J, L oe H . P e r io d o n ta l d is e a se in pregnancy. C orrelation betw een oral h y gien e and p e r io d o n ta l c o n d it io n . A cta O d o n to l Scand 1964;22:121. 10. L oe H , S iln e ss J. P e r io d o n ta l d is e a se in pregnancy. P revalence and severity. A cta O d on tol Scand 1963;21:533. 11. Schei O, WaerhaugJ, Lovdal A, Arno A. Alveolar b o n e lo ss as r ela te d to oral h y g ie n e an d a g e . J Periodontol 1959;30:7. 12. Fleiss JL. S tatistical m e th o d s fo r rates and proportions. New York: Wiley;1981. 13. L andis JR, H eym an ER, Koch GG. A verage partial association in three-way contingency tables: a review and discussion o f alternative tests. Int Stat Rev 1978;46:237-54. 14. B en n e tt PH, Burch TA, M iller M. D iabetes m e llitu s in A m erica n (P im a) In d ia n s. L a n c et 1971;ii:125. 15. Knowler WC, Bennett PH, Bottazzo GF, Doniach D. Islet cell antibodies and diabetes mellitus in Pima Indians. Diabetologia 1979;17:161. 16. Savage PJ, B ennett PH, Senter RG, M iller M. P r e v a le n c e o f d ia b e te s in y o u n g P im a In d ia n s. Diabetes 1979;28:937. 17. Sheridan RCJr, Cheraskin E, Flynn FH, Hutto AC. Epidemiology o f diabetes mellitus— II. A study of 100 dental patients. J Periodontol 1959;30:298. 18. Mackenzie RS, Mallard DH. Interrelated effects o f diabetes, arteriosclerosis and calculus on alveolar bone loss. JADA 1963;66:53. 19. Belting CM, Hiniker JJ, Dummett CO. Influence o f diabetes m ellitus on the severity o f periodontal disease. J. Periodontol 1964;35:476. 20. Finestone AJ, Boorujy SR. Diabetes mellitus and periodontal disease. Diabetes 1967;16:336. 21. B en v e n iste R, B ix le r D , C o n n e a lly PM. P e r io d o n ta l d ise a se in d ia b e te s . J P e r io d o n to l 1967;38:271. 22. C ohen DW, Friedman LA, Shapiro J, Kyle GC, Franklin S. Diabetes mellitus and periodontal disease: tw o year lo n g itu d in a l o b s e r v a tio n s — P art I. J Periodontol 1970;41:709. 23 . H o v e KA, S tallard RE. D ia b e te s an d th e periodontal patient. J Periodontol 1970;41:713. 24. Glavind L, Lund B, L oe H . T he relationship b etw een p eriod on tal state and d iab etes du ration, insu lin d osage and retinal changes. J P eriod on tol 1968;39:341. 25. Sznajder N , Carraro JJ, R ugna S, Seredy M. P eriod on tal fin d in gs in d iab etic and n o n d ia b e tic patients. J Periodontol 1978;49:445. 26. Ervasti T, Knuuttila M, Pohjamo L, Haukipuro K. Relation between control o f diabetes and gingival bleeding. J Periodontol 1985;56:154. 27. Lang NP, Hill RW. Radiographs in periodontics. J Clin Periodontol 1977;4:16. 28. G oodson JM, Haffajee AD, Socransky SS. The relationship between attachment level loss and alveolar bone loss.J Clin Periodontol 1984;11:348. 29. L oe H , A nerud A, Sm ith M. B oysen H. T he natural history o f p erio d o n ta l d ise a se s in m an. J Periodontol 1978;49:67. 30. Bailit HL, Braun R, Maryniuk GA, Camp P. Is p e r io d o n ta l d ise a se th e p rim ary c a u s e o f to o th extraction in adults? JADA 1987;114:40. 31. Page RC, Schroeder HE. Periodontitis in man and other animals. Basel:Karger; 1982. 32. Faulconbridge AR, Bradshaw WCC, Jenkins PA, Baum JD. T he dental status o f a group o f diabetic children. Br D entJ 1981;151:253. 33. Cianciola LJ, Park BH, Bruck E, M oscovich L, Genco RJ. Prevalence o f periodontal disease in insulindependent diabetes mellitus (juvenile diabetes). JADA 1982;104:653.
R E P O R T S
The relationship between type 2 diabetes mellitus and periodontal disease was evaluated in 2,878 Pima Indians of the southwestern United States. Two independent measures of periodontal disease, probing attachment loss and radiographic bone loss, were used to compare prevalence and severity o f periodontal disease in diabetic and nondiabetic subjects. In all age groups studied, subjects with diabetes had a higher prevalence of periodontal disease, indicating that diabetes may be a risk factor fo r periodontal disease.
Type 2 diabetes mellitus and periodontal disease M a rc S h lo ssm a n , D D S, MS; W illiam C . K now ler, M D , D rP H ; D av id J . P e ttitt, M D ; R o b e r t J . G e n c o , D D S, P h D
e n tists fre q u e n tly tr e a t p a tie n ts with chronic systemic conditions, such as diab etes, th a t can affect th e c o u r s e a n d m a n a g e m e n t o f p e r i o d o n ta l d is e a s e . S y stem ic d ise a se is c o n sid e re d a c o n trib u tin g fac to r r a th e r th a n th e p rim a ry etiologic facto r in th e i n it ia t io n o f p e r io d o n t itis . D ia b e te s m ellitu s is a ch ro n ic m etabolic diso rd er th a t a f f e c ts c a r b o h y d r a te a n d lip id metabolism. T he term diabetes m ellitus encompasses a g r o u p o f g e n e tic a lly a n d c lin ic a lly h etero g en o u s disorders in w hich glucose in to l e r a n c e is f o u n d . S ta n d a r d iz e d term inology, classification, an d diagnostic criteria have been established1-2 to provide greater consistency for th e description o f this disorder. Two m ajor types o f diabetes are identified. Approxim ately 80%-90% o f persons with diabetes in the U nited States h av e ty pe 2 o r n o n in s u lin - d e p e n d e n t diabetes mellitus and 10%-20% have type 1 o r in su lin-dependent diabetes mellitus. Type 1 diabetes is c h a racterize d by islet c e ll d e s tr u c tio n a n d is d e p e n d e n t on exogenous insulin for survival. In contrast, in ty p e 2 d ia b e te s , in s u lin a c tio n is im paired, with at least some preservation o f in s u lin s e c r e tio n , a lth o u g h in s u lin injections are often useful in treatm ent. T h e p r e v a le n c e s o f b o th p e r io d o n ta l
D
5 3 2 ■ JADA, Vol. 121, O cto b er 1990
disease an d type 2 diabetes increase with age. P atie n ts w ith d ia b ete s m e llitu s are su sceptible to n u m e ro u s co m p licatio n s, both chronic an d acute. T h e c o n c e p ts o f p e r io d o n ta l disease e p id e m io lo g y a n d p a th o g e n e s is a re c h a n g in g . T h e id e a th a t p e r io d o n t a l d ise ase is w id e s p re a d a n d is se e n as a single form o f disease is cu rren tly being challenged by the systemic studies done in the past 20 years.3.4 R ecent epidem iologic su rv ey s in d ic a te t h a t o n ly a sm a ll p e rc e n ta g e (75% -15% ) o f a p o p u la tio n m ay be a ffe c te d by sev ere p e r io d o n ta l
d is e a s e .4-6 I d e n ti f ic a t io n a n d c h a r a c te r iz a tio n o f h ig h - ris k g r o u p s o r individuals w ith g re a te r susceptibility to se v ere p e r io d o n titis a re n e e d e d . T h is p a p e r p r e s e n ts c ro ss-se c tio n a l d a ta o f periodontal disease in a population with a high prevalence o f type 2 diabetes. M ethods and m aterials F o r 3,219 su b je cts fro m th e G ila River In d ia n C o m m u n ity , A riz, s ta n d a rd iz e d clinical exam inations were perform ed; of these, 2,878 had d ata from a b o n e score,
Table 1 ■ Distribution of subjects by age, gender, and diabetes. No. o f subjects Age (years) 5-24 25-44 > 45 Total Total
G ender*
N ondiabetic
Diabetic
Total
Diabetes prevalence (%)
M F M F M F M F Total
753 871 241 429 82 107 1,076 1,407 2,483
22 55 120 184 122 263 264 472 736
775 896 361 613 204 370 1,340 1,879 3,219
3 3 33 30 60 71 20 25 23
* M = m ale, F = fem ale.
r
R E S E A R C H
R E P O R T S
Non diabetic subjects Age (years)
5 -2 4
>45
2 5 -4 4
96 7
n =622
n = 187
60-
Fig 1 ■ D istrib u tion o f m e 40-
dian probing attachm ent loss: )5 5
Ü s 09
171
M = m is s in g th r e e or m ore in d e x te e th ; E d e n t = fu lly
14
0 5
0 5
edentulous. The shaded areas represent subjects with “severe disease”: > 6.0 mm PAL, M, or
Diabetic subjects
a> >
Edent.
n =291
49 5
18 9 14.4
0
1-2
_
86
3-4
M
66
E cU n t
0
1-2
M
3-4
E d *n t
M edian probing attachment loss (mm)
Non diabetic subjects A ge (years)
.no
> 45
2 5 -4 4
5 - 24
9»-9 n * 1044
£ >% O
F ig 2 ■ D istrib u tion o f m e 06
dian alveolar b on e loss: M =
06
m is s in g 14 or m o re te e th ; Edent = fully edentulous. The 09 >
sh a d e d areas rep re sen t su b
Diabetic subjects
j e c t s w ith “s ev e r e d is e a s e ” : > 2.0 b o n e lo ss sco r e , M, or Edent.
0
1-2
3-6
>6
M
Ed *n t
0
1-2
3-6
>6
M
Ed*nt
0
1-2
3 -6
>6
M
Ed«nt
Median bone loss score
p r o b in g e x a m in a tio n , o r b o th , as d e s c r ib e d h e r e . M ost r e s id e n ts o f th e com m unity are Pim a o r Papago Indians, m em bers of two closely related tribes, with the w orld’s highest rep o rted prevalence of type 2 diabetes mellitus and in which type 1 diabetes is unknow n.7 T he participants
o f th e s tu d y w e re r e c r u i t e d fro m a longitudinal survey o f diabetes an d other c h r o n ic d is e a s e s , w h ic h h a s b e e n in progress since 1965. Approxim ately every 2 years, each m em b er of the com m unity older than 5 years is asked to participate in a standardized biennial exam ination7 that
in c lu d e s a m e d ic a l h is to ry , p h y sic a l exam ination, glucose tolerance test, an d a dental exam ination. P e r io d ic d e n ta l e x a m in a tio n s w ere in it ia t e d in F e b r u a r y 1 983. E ach e x a m in a tio n in c lu d e d a p a n o r a m ic rad io g rap h (Siem ens OP-IO), evaluation JADA, Vol. 121, O cto b er 1990 ■ 533
I R E S E A R C H
R E P O R T S
o f the oral m ucous m em branes by visual an d digital exam ination, and recording o f d ec ay e d , m issing, a n d fille d te e th . Six index teeth or their substitutes8 were used f o r th e p e r io d o n t a l e v a lu a tio n th a t in clu d ed plaque index,» gingival in d e x ,1“ a n d calculus index (presence o r absence o f supra- o r subgingival calculus). P robing pocket d ep th s w ere m easured to the nearest m illim eter from the gingival m argin with calibrated periodontal probes (PCP-10, Hu-Friedy). P robing attachm ent lev el to th e n e a r e s t m illim e te r was m e asu red w ith c a lib ra te d p ro b es as th e d is ta n c e b e tw e e n th e c e m e n to e n a m e l ju n c tio n (CEJ) and the base of the pocket. M easu rem ents o f p ro b in g p o ck e t d ep th w ere p e r f o rm e d a t six sites p e r to o th : m e s io b u c c a l, m id b u c c a l, m id lin g u a l, m e s io lin g u a l, d is to b u c c a l, a n d d isto lin g u al. P ro b in g a tta c h m e n t levels were m e a s u r e d a t f o u r site s: m id b u c c a l, m id lin g u al, an d th e d e e p e st m esial and distal interproxim al points. T h e panoram ic films were evaluated for p a th o sis a n d u se d to d e te r m in e in te r p r o x im a l c r e s ta l a lv e o la r b o n e loss. A lveolar b o n e loss was m e asu red with a m odified Schei ruler.11 This was scored as a percen tag e o f b o n e loss from th e CEJ to th e a p e x a t th e d e e p e s t p o in t o n th e m e sia l o r d is ta l s u rfa c e o f e a c h to o th present, excluding third molars. Bone loss score o f 0 in d icates no radiographically detectable bone loss; 1 = 1% to 24% bone loss; 2 = 25% or 49% bo n e loss; 3 = 50% to 74% b o n e loss; a n d 4 = 75% o r m o re b o n e lo ss. A ll e x a m in a tio n s w e re c o n d u c te d from F eb ru ary 1983 th ro u g h Ja n u a ry 1988 by a single exam iner (MS) w ithout knowledge o f a p atien t’s diabetes s ta tu s . All d a ta p r e s e n te d a r e cro ssse ctio n al. F o r su b je cts seen m o re th a n o n c e , o n ly th e in itia l e x a m in a tio n is included. P atient data could be excluded from a p a rtic u la r m e a su re fo r specific reaso n s including: p atien t refusal (no radiograph o r p robing), pregnancy (no radiograph), h e a r t c o n d itio n s r e q u ir in g a n tib io tic p r o p h y la x is ( n o p r o b in g ) , m ix e d dentition (no bone loss score), equipm ent f a ilu r e ( n o r a d i o g r a p h ) , in a b ility to p o sitio n p a tie n t (n o ra d io g ra p h ) o r no c lin ic a l e x a m in a tio n (n o p r o b in g ) . A radiographic exam ination was perform ed by a trained dental assistant for all eligible patients even when a clinical exam ination was n o t d o n e . O f th e 3 ,2 1 9 p e r s o n s e x a m in e d , p r o b in g e x a m in a tio n s w ere p e rfo rm e d o n 2,304, b o n e scores w ere available from 2,718, and 2,878 had one or both o f these exam inations. 5 3 4 ■ ADA, Vol. 121, O cto b er 1990
T he b iennial ex am in atio n includes an o r a l g lu c o s e to le r a n c e te s t. A fa s tin g plasma sam ple is taken, the patien t ingests 75 g o f carbohydrate (Glucola Ames Co) an d a seco n d p lasm a sam p le is tak en 2
hours later for glucose analysis. T he results o f this test are used to diagnose diabetes.2 Diabetes is diagnosed in any patient if the 2-hour postload plasm a glucose is > 11.1 m mol (200 m g /d L ) or if in the course of
Non diabetic subjects
Diabetic subjects
' I 7 ' l 6 ' l 5 ' U ' l 3 ' l 2*11 ' 2 r 2 2 ' 2 3 ‘ 2 4 ' 2 5 ' 2 6 ' 2 7 ‘
’ l 7 ' l 6 1 S ' l 4 ' l 3 ' l 2 ' 1 1 ' 2 1 2 2 2 3 24 2 8 * 2 4 ' 2 7
n = 1190
n = 43
4 7 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 3 4 3 5 36 37
4 7 4 6 4 5 44 4 3 4 2 4 1 31 3 2 3 3 3 4 35 3 6 37
17 16 15 14 13 12 11 21 2 2 2 3 24 2 5 2 6 2 7
17 16 15 14 13 12 11 21 22 2 3 2 4 2 5 2 6 2 7
>w — o
'5 o
2 CM o LO
o 3
£> V
c o
n « 266
n = 619
>-
5 X O
II..... .
If)
CM
.Q T3 C
o 2
100 in
4 7 4 6 4S 4 4 4 3 4 2 41 31 32 3 3 34 35 3 6 37
47 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 3 4 3 6 36 37
17 16 I S 14 13 12 11 21 2 2 23 24 2 5 2 6 27
17 14 I S 14 1 3 12 11 21 2 2 2 3 24 2 6 2 6 27
n = 1S5
n * 209
47 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 34 3 5 3 6 37
47 4 6 4 5 4 4 4 3 4 2 41 31 3 2 3 3 3 4 3S 3 6 37
k—
o K o 2 i/> Al
D &
o -
(V o>
< Tooth number
Fig 3 ■ Distribution o f interproxim al alveolar bone loss by tooth. The shaded areas represent the percent o f teeth affected by 25% or more bone loss determ ined by m easurem ent from panoramic radiographs.
R E S E A R C H
routine m edical care a fasting, casual, o r 2h o u r p o stlo a d p la sm a g lu c o se c o n c e n tr a tio n >11.1 m m o l is d o c u m e n te d , as described.7 All dental exam inations were p erform ed by a single exam iner (MS). Thirty subjects exam ined at a biennial exam ination were recalled within 14 to 21 days for duplicate e x a m in a tio n s (p ro b in g a tta c h m e n t loss an d radiographic evaluation) to establish in traex am in er reproducibility, w hich was assessed by the kappa statistic.12 T he kappa statistics for probing attachm ent loss and bone loss were 76% an d 88%, respectively. T he associations betw een various dental co n d itio n s an d diabetes, co n tro llin g for c o n f o u n d in g by a g e w ere a sse ss e d in th re e -w a y c o n tin g e n c y ta b le s .13 T h e m e d ia n p r o b in g a t ta c h m e n t lo ss a n d m e d ia n alv eo la r b o n e loss sc o re s w ere u s e d as two m e a su re s o f p re s e n c e a n d severity o f p e rio d o n ta l disease. P ro b in g a tta c h m e n t level m easures fo r all in d e x te e th w ere a n a ly z e d a n d a m e d ia n attac h m e n t loss was established fo r each subject. For this analysis, a missing tooth w as a s sig n e d a v a lu e h ig h e r th a n th e m axim um recorded m easurem ent so that even edentulous patients o r patients with m issing in d e x te e th co u ld be in c lu d ed . Alveolar b o n e loss was m easu red fo r all te e th p re s e n t, a n d a m e d ia n b o n e loss sc o re was c o m p u te d fo r e a c h p a tie n t. M issing te e th w ere assig n ed a v alu e o f higher th an the m axim um score, again to in clu d e m issing te e th in com p u tatio n of the m edian. A p r e o p e ra tiv e r a d io g r a p h ic e x a m in a tio n a n d c h a r t rev iew f ro m 100 r a n d o m ly s e le c te d p a tie n t r e c o r d s o f subjects w ho h a d lost te e th b efo re th e ir initial oral health survey was com pleted to d e t e r m in e r e a s o n s f o r to o th loss. R ad io g raphs from p atien ts who becam e e d e n tu lo u s d u r in g th e stu d y w e re evaluated for bone loss and caries.
Results T h e distribution o f the subjects according to age, gender, a n d diabetes is shown in T a b le 1. T h e p r e v a le n c e o f d ia b e te s increased with age from 3% in th e 5- to 24y ear g ro u p to 60% in m en a n d 71% in women aged > 45 years. T h e review o f preoperative radiographs an d dental records from patients who had lost teeth before th e ir initial o ral h ealth survey show ed th a t 72% o f to o th losses w ere th e re s u lt o f p e rio d o n ta l disease. Preoperative radiographic exam inations in 28 patients who lost their rem aining teeth d u rin g th e course o f th e study revealed
th a t 95% o f th e e x tr a c tio n s w e re th e results o f periodontal disease, an d 51% o f th e te e th h ad lo st a t le ast 75% o f th e ir b one support. Only 5% o f th e teeth were extracted because o f severe decay. T he frequency distributions o f m edian probing attachm ent loss (PAL) are shown in Figure 1. T he distributions were shifted toward m ore perio d o n tal disease at older ages an d am o n g th o se w ith d ia b ete s in ea ch age g ro u p . T h e p rev a len c e o f th e m ost healthy PAL category (m edian PAL = 0, indicating th at at least h alf the sites had n o evidence o f a tta c h m e n t loss) ran g ed from 99% to 27% in th e th ree age groups am ong the nondiabetic subjects an d from 88% to 12% am ong those with diabetes. T h e p r e v a le n c e o f e d e n tu lo u s n e s s in c r e a s e d w ith ag e f ro m 0% to 21% am ong nondiabetic subjects an d from 0% to 58% am ong diabetic subjects. In th e age g ro u p s 25-44 a n d > 45 y ea rs, th e PAL frequency distributions w ere significantly d if f e r e n t b e tw e e n d ia b e tic a n d n o n d ia b etic subjects (by C h i2, P < 0.001 in each age group). Controlling for age, the su m m a ry C h i2 f o r th e a s s o c ia tio n o f d ia b e te s w ith PAL was 185, d f = 5, P < 0.001. T he frequency distributions o f m edian alveolar bone loss scores (BUS) are shown in F ig u re 2. T h e p r e v a le n c e o f th e h e a lth ie s t c a te g o ry ( m e d ia n BLS = 0, indicating that at least h alf the teeth had no evidence o f bone loss) decreased from 97% to 7% in n o n d ia b e tic subjects an d from 79% to 2% in diabetic subjects with in c r e a s in g ag e . T h e p r e v a le n c e o f edentulousness increased from 0% to 17% in no n d iab etic subjects an d from 0% to 45% in diabetic subjects w ith increasing ag e . In all th r e e ag e g r o u p s , th e BLS frequency distributions in diabetic subjects were significandy d ifferen t from those in nondiabetic subjects (P < 0.01). C ontrol lin g f o r a g e , th e s u m m a ry x2 f o r th e association o f diabetes with BLS was 218, df= 4, P< 0.001. Figure 3 illustrates th e g re a te r loss o f in te rp ro x im a l alveolar b o n e in subjects w ith d ia b e te s th a n in su b je c ts w ith o u t d iab etes, as w ell as th e e a rlie r o n se t o f alveolar bone loss in those with diabetes. Bone loss was g reatest in th e m o lar and in c is o r s e g m e n ts in th e y o u n g e r age groups, b u t there was a m ore generalized pattern in older age groups.
Discussion T h e P im a In d ia n s o f th e so u th w e ste rn U n ited States have th e h ig h est re p o rte d incidence an d prevalence o f d iab etes in
R E P O R T S
th e w orld. Fifty p e r c e n t o f th o se o ld e r th a n 35 years a re a f f e c te d .714 D iab e te s m ellitus in this p o p u la tio n is exclusively ty p e 2 1516 a n d is a s s o c ia te d w ith c o m plications at rates similar to those o f oth er populations. C onsiderable research d ealing with the relatio n sh ip o f d iab etes an d p e rio d o n tal d ise ase h as b e e n p u b lis h e d .1723 U n fo r tunately, th e fin d in g s have b e e n in c o n sistent. C on trad icto ry d ata have failed to e s ta b lis h a n a s s o c ia tio n b e tw e e n th e periodontal status o f diabetic subjects and the nondiabetic controls. O th er studies do n o t specify the type o f diabetes p resen t or include only patients with type 1 diabetes, while type 2 diabetes accounts fo r 80% of diabetic cases today. Diabetes mellitus encom passes a variety o f d is o r d e r s th a t d if f e r in th e ir p a th o g e n e s is a n d n a tu ra l h isto ry . I t is im p o r ta n t to u se c o m m o n ly a c c e p te d te rm in o lo g y a n d s ta n d a r d iz e d classif ic a tio n a n d d ia g n o s tic c r i t e r i a w h e n d e s c rib in g su b je cts w ith g lu c o se in to l erance. In some previous reports, uniform criteria were lacking for the diagnosis and classification of diabetes an d p erio d o n tal disease. T h e a g e s p a n a n d th e n u m b e r s o f d ia b e tic a n d n o n d ia b e ti c s u b je c ts e x a m in e d in th is stu d y a r e m o re com prehensive an d extensive th a n those rep o rted in previous studies.192223 A wide variety o f clinical in d ex es have b ee n used to estim ate th e prevalen ce o f periodontal disease in past epidem iologic s tu d ie s . In p re v io u s s tu d ie s , th e p e r i o d o n ta l statu s o f p a tie n ts w ith d ia b ete s m ellitu s has b e e n assessed w ith clinical p a r a m e te r s b a s e d o n th e s ig n s a n d sy m p to m s o f p e r io d o n t a l d is e a s e a n d fa c to rs th o u g h t p r e d is p o s in g to p e r i odontitis.23-26 Today, quantitative m easures o f p eriodontal disease are used to m onitor a n d d e te c t p e r io d o n titis . S ev ere p e r i o d o n titis has recently b e e n d e fin e d as a loss o f attachm ent o f 6 m m o r m ore at one o r m o r e s ite s .6 R a d io g r a p h ic q u a n tific a tio n o f crestal b o n e h e ig h t is also v alu ab le in e v a lu a tin g th e p e r io d o n ta l s u p p o r t o f t e e t h . 27 R e lia b ility a n d r e p r o d u c ib ility o f m e a s u r e m e n ts a re essential to their inco rp o ratio n in a study. A tta ch m e n t loss by p ro b e m e a su re m e n t a n d b o n e loss by ra d io g rap h ic m easu re m e n t a r e th e tw o p r im a r y c lin ic a l assessments used to indicate the presence o f periodontal disease.2» Tooth loss in this pop u latio n is prim arily caused by p e rio d o n ta l d e s tru c tio n . T his finding is n o t unique to this p opulation,2« b u t e v id e n c e h as b e e n p r e s e n te d th a t JADA, Vol. 131, October 1990 ■ 535
R E S E A R C H
R E P O R T S
p eriodontal disease is n o longer the m ajor c a u s e o f to o th lo ss in a d u l ts .30 D a ta g ath ered from p re tre a tm e n t radiographs a n d c h a r t review show to o th loss as a fu rth e r indicator o f destructive periodon titis. F o r th is re a so n , m issing te e th are in c lu d ed in this analysis o f p erio d o n titis an d , fo r p urposes o f co m p u tin g m edian values, are given a value h ig h e r than the m easured m axim um . T h e cross-sectional data presented show th a t th e prevalence o f periodontal disease is g reater in persons with type 2 diabetes. T his conclusion is based on two separate q u a n tita tiv e m e a s u r e s o f p e r io d o n t a l d e s t r u c t i o n th a t c a n b e p e r f o r m e d in d e p e n d e n tly : th e loss o f p e rio d o n ta l a tta c h m e n t a n d loss o f in te r p ro x im a l crestal alveolar bone. F urtherm ore, these s tu d ie s h a v e sh o w n th a t p e r io d o n t a l disease occurs at an earlier age in persons with type 2 diabetes. T h e c u rre n t study has several strengths f o r e v a lu a tin g th e im p lic a tio n th a t p e rio d o n ta l disease is a com plication o f diabetes. O ne asset is th e large n um ber o f s u b je c ts e x a m in e d a n d e v a lu a te d . In a d d i tio n , th e s tu d y w as m a sk e d . T h e p e rio d o n ta l e x a m in e r d id n o t know the d ia b etic status o f subjects, a n d diabetes w as d ia g n o s e d o b je c tiv e ly by g lu c o se tolerance testing. Also, this population has an extrem ely high prevalence o f diabetes, w hich allowed for a large n u m b e r (736) o f diabetic subjects to be studied. Finally, two m e an s o f m e a su rin g p e rio d o n titis w ere used: th e assessm ent o f a tta c h m e n t loss fro m th e c e m e n to e n a m e l ju n c tio n , an d th e m e a s u r e o f in te r p r o x im a l c re s ta l a lv e o la r b o n e lo ss. B o th q u a n tita tiv e m easures, although correlated, were used independently. T hey are well accepted as in d ic ato rs o f d estru ctiv e p erio d o n titis.28 U sing e ith e r m easure, th e prevalence o f p e r io d o n ta l d ise ase was clea rly h ig h e r am ong diabetic subjects. Localization of alveolar b o n e loss shows th a t in th e y o u n g er age g ro u p s th e first m olars a n d incisors were p redom inantly a f f e c te d , c o n s is te n t w ith o th e r e p id e m io lo g ic s tu d ie s .5’31 H o w ev er, w ith a d v a n c in g ag e a n d m o re se v e re p e r i o d o n tit is , th e p a t t e r n w as m o r e generalized.
Conclusions T hese findings, along with earlier studies a s s o c ia tin g p e r io d o n t itis a n d ty p e 1 diabetes in teenagers an d young adults3233 suggest th a t periodontitis is a com plication o f b oth type 1 and type 2 diabetes mellitus. I f so,' t h e r e a r e s ig n if ic a n t c lin ic a l 536 ■ JADA, Vol. 121, October 1990
im plications th a t d iab etes may be a risk f a c to r fo r d e v e lo p m e n t o f p e r io d o n ta l d ise ase . T h is h y p o th e sis will b e in v e s tigated in th e lo n g itu d in al phase o f this study. ---------------------- J'A O A -----------------------
The inform ed consent o f all hum an subjects who p a r tic ip a te d in th e e x p e r im e n ta l in v e s tig a tio n reported or described in this manuscript was obtained a fte r th e n a tu re o f th e p r o c e d u r e a n d p o s s ib le discomforts and risks had been explained fully. This study was supported in part by USPHS Grant D E 0 6 5 1 4 fro m th e N a tio n a l I n stitu te o f D e n ta l Research, NIH, Bethesda, MD 20205. The authors thank the Gila River Indian community fo r its c o o p e r a tio n an d p a r tic ip a tio n a n d th e physicians, technical, and clerical staff o f the Diabetes and Arthritis Epidemiology Section, National Institute o f Diabetes and Digestive and Kidney Diseases, and the Indian H ealth Service, Phoenix Area; Ana CabreraArevalo, Robert Dunford, and Dr. Lawrence Emrich for their statistical and computer analysis; Joyce Moyah a n d S h a n n o n Irw in fo r p a t ie n t care an d data collection; Drs. Lars Christerson, Lynn Budding, and R ich a rd D u n n fo r th e review an d c o m m e n ts concerning the manuscript; Dr. Peter B ennett for his advice and support; and Dr. Anthony A. Rizzo for his advice and encouragem ent from the inception o f this study. Dr. Shlossman is assistant professor or oral biology, SUNY-Buffalo School o f Dental M edicine, and is in priv a te p r a c tic e , C h an d ler, AZ. Dr. G e n c o is distinguished professor and chairman, department o f oral biology at SUNY; Dr. Knowler is c h ie f and Dr. P e ttitt is a ssista n t c h ie f, d ia b e te s a n d a rth ritis epidem iology section, National Institute o f Diabetes and Digestive and Kidney Diseases, Phoenix,. Address req uests for reprints to Dr. G en co, 3435 M ain St, FosterHall-135, Buffalo 14214.
1. National Diabetes Data Group. Classification and diagnosis o f diabetes and other categories o f glucose intolerance. Diabetes 1979;28:1039. 2. World Health Organization, Expert C om m ittee o n Diabetes. Second Report. 1980 Technical Report Service No. 646, Geneva. 3. Burt BA. Public health im plications o f recent research in periodontal diseases. J Public Health Dent 1988;48:252. 4. Johnson NW, et al. Detection o f high-risk groups and individuals for periodontal diseases. Evidence for the existence o f high-risk groups and individuals and app roaches to th eir d e tectio n . J Clin P eriod on tol 1988;15:276. 5. Loe H, Anerud A, Boysen H, Morrison E. Natural h isto r y o f p e r io d o n ta l d is e a se in m an . J C lin Periodontol 1986;13:431. 6. N a tio n a l In stitu te o f D e n ta l R esearch , Oral h ea lth o f US adults. T he N ation al Survey o f Oral Health in US Employed Adults and Seniors: 1985-1986. National findings; 1987 NIH publication no. 87-2868. 7. Knowler WC, Bennett PH, Hamman RF, Miller M. Diabetes incidence and prevalence in Pima Indians: A 19-fold greater incidence than in Rochester, Minn. Am J Epidemiol 1978;108:497. 8. Ramfjord SP. Indices for th e prevalence and in c id e n c e o f p e r io d o n ta l d is e a se . J P e r io d o n to l 1959;30:51.
9. S iln e ss J, L oe H . P e r io d o n ta l d is e a se in pregnancy. C orrelation betw een oral h y gien e and p e r io d o n ta l c o n d it io n . A cta O d o n to l Scand 1964;22:121. 10. L oe H , S iln e ss J. P e r io d o n ta l d is e a se in pregnancy. P revalence and severity. A cta O d on tol Scand 1963;21:533. 11. Schei O, WaerhaugJ, Lovdal A, Arno A. Alveolar b o n e lo ss as r ela te d to oral h y g ie n e an d a g e . J Periodontol 1959;30:7. 12. Fleiss JL. S tatistical m e th o d s fo r rates and proportions. New York: Wiley;1981. 13. L andis JR, H eym an ER, Koch GG. A verage partial association in three-way contingency tables: a review and discussion o f alternative tests. Int Stat Rev 1978;46:237-54. 14. B en n e tt PH, Burch TA, M iller M. D iabetes m e llitu s in A m erica n (P im a) In d ia n s. L a n c et 1971;ii:125. 15. Knowler WC, Bennett PH, Bottazzo GF, Doniach D. Islet cell antibodies and diabetes mellitus in Pima Indians. Diabetologia 1979;17:161. 16. Savage PJ, B ennett PH, Senter RG, M iller M. P r e v a le n c e o f d ia b e te s in y o u n g P im a In d ia n s. Diabetes 1979;28:937. 17. Sheridan RCJr, Cheraskin E, Flynn FH, Hutto AC. Epidemiology o f diabetes mellitus— II. A study of 100 dental patients. J Periodontol 1959;30:298. 18. Mackenzie RS, Mallard DH. Interrelated effects o f diabetes, arteriosclerosis and calculus on alveolar bone loss. JADA 1963;66:53. 19. Belting CM, Hiniker JJ, Dummett CO. Influence o f diabetes m ellitus on the severity o f periodontal disease. J. Periodontol 1964;35:476. 20. Finestone AJ, Boorujy SR. Diabetes mellitus and periodontal disease. Diabetes 1967;16:336. 21. B en v e n iste R, B ix le r D , C o n n e a lly PM. P e r io d o n ta l d ise a se in d ia b e te s . J P e r io d o n to l 1967;38:271. 22. C ohen DW, Friedman LA, Shapiro J, Kyle GC, Franklin S. Diabetes mellitus and periodontal disease: tw o year lo n g itu d in a l o b s e r v a tio n s — P art I. J Periodontol 1970;41:709. 23 . H o v e KA, S tallard RE. D ia b e te s an d th e periodontal patient. J Periodontol 1970;41:713. 24. Glavind L, Lund B, L oe H . T he relationship b etw een p eriod on tal state and d iab etes du ration, insu lin d osage and retinal changes. J P eriod on tol 1968;39:341. 25. Sznajder N , Carraro JJ, R ugna S, Seredy M. P eriod on tal fin d in gs in d iab etic and n o n d ia b e tic patients. J Periodontol 1978;49:445. 26. Ervasti T, Knuuttila M, Pohjamo L, Haukipuro K. Relation between control o f diabetes and gingival bleeding. J Periodontol 1985;56:154. 27. Lang NP, Hill RW. Radiographs in periodontics. J Clin Periodontol 1977;4:16. 28. G oodson JM, Haffajee AD, Socransky SS. The relationship between attachment level loss and alveolar bone loss.J Clin Periodontol 1984;11:348. 29. L oe H , A nerud A, Sm ith M. B oysen H. T he natural history o f p erio d o n ta l d ise a se s in m an. J Periodontol 1978;49:67. 30. Bailit HL, Braun R, Maryniuk GA, Camp P. Is p e r io d o n ta l d ise a se th e p rim ary c a u s e o f to o th extraction in adults? JADA 1987;114:40. 31. Page RC, Schroeder HE. Periodontitis in man and other animals. Basel:Karger; 1982. 32. Faulconbridge AR, Bradshaw WCC, Jenkins PA, Baum JD. T he dental status o f a group o f diabetic children. Br D entJ 1981;151:253. 33. Cianciola LJ, Park BH, Bruck E, M oscovich L, Genco RJ. Prevalence o f periodontal disease in insulindependent diabetes mellitus (juvenile diabetes). JADA 1982;104:653.
