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Periodontitis and Aging: Reviewing Recent Evidence
R E V IE W IN G BRIAN A. B URT, B .D .S .,
term “model” of disease m eans a collection of theory on etiology, transm ission, progres sion and outcome, based as far as possible on accepted research. B ut some speculation is necessarily included, so models have to be modified as new research comes out, some tim es extensively. Such is the case w ith periodontal disease (these days a term best used generically for a cluster of diseases). O ur understanding of these conditions h a s advanced so much th a t we m ust rem em ber th a t as recently as the mid1960s, th e periodontal disease model included th e following precepts: gingivitis insidiously progressed to periodontitis w ith consequent loss of bone and teeth; virtually everyone was considered susceptible to severe periodontitis; ■* susceptibility to periodontitis increased w ith age; ■* periodontal disease was the m ain cause of tooth loss after age 35. The first two points implied an aging factor, while the last two included age directly.
R E G E N T E V ID E N C E
PH.D.
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This review critically examines recent research on the relation between age and periodontitis. It concludes that some loss of periodontal attachment and alveolar bone is to be expected in older persons, but age alone in a healthy adult does not lead to a critical loss of periodontal support. Although moderate loss of alveolar bone and periodontal attachment is common in the elderly, severe periodontitis is not a natural consequence of aging.
D estructive periodontal disease h as been so consistently associated w ith aging th a t m any came to see it as an inevitable consequence of growing older. Clinical observations th a t periodontitis w as a function of age are as old as the expression “getting long in the tooth.” H orse-trading transactions often depended on the buyer’s inspection of the
horse’s tee th (a practice th a t tells us th a t em pirical folk wisdom, for w hat it’s worth, sees gingival recession as a norm al p a rt of aging). N early all studies from the early days of periodontal research511 found a close association betw een age, periodontal disease and tooth loss. B ut early d a ta a t the tim e were aggregated and crosssectional. A casual reading of cross-sectional data can lead to m isleading conclusions if no allowance is m ade for cohort effects (differences betw een age groups who grew up a t different tim es under different condi tions). Recent research has questioned th e association between age and periodontitis. (This h as been sum m arized in a series of review s.1*4) This paper critically exam ines the m ost recent epidem iologic and clinical research to define more precisely the role of aging in ad u lt periodontitis. Because assessing this relation ship has been often confounded by the problem of how to deal with m issing teeth, this review focuses, as far as possible, on clinical m easures of existing teeth. JADA, Vol. 125, March 1994
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M easuring and expressing periodontal diseases in different ways can lead to different views of the distribution of these conditions—an issue discussed later. B ut w hen th e disease is m easured by loss of periodontal attach m en t (LPA) or alveolar bone loss, nearly all crosssectional studies show more severe conditions in older populations. This is evident in th e d a ta from the 1985-86 N ational Survey of Oral H ealth in U.S. Employed Adults and Seniors1214 (Figure 1) as well as in recent studies of selected populations. A Swedish report from the early 1980s15 was one of the first epidemiologic studies to look a t the distribution of LPA and radiographic bone loss, ra th e r th a n a t average periodontal scores on a scaled index. W hat a t the tim e seem ed rem arkably few people—no more th a n 8 percent in each 10-year age group in th is Swedish popu lation—showed evidence of severe periodontitis. The authors defined the condition as gingivitis, pockets and general m arginal bone loss betw een one-third and tw o-thirds of norm al height. This sm all proportion w ith severe disease in the older age groups was only slightly higher th a n in the younger, though m oderate periodontitis (generalized m arginal bone loss up to oneth ird norm al bone height) was common a t all ages. In th e longitudinal Piedm ont study in N orth Carolina, base line findings were th a t LPA was more extensive in persons aged 65 or older th a n in younger groups.16 B ut severe LPA or 274
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bone loss is not universal among healthy elderly people. Only 15 percent of persons aged 70 or older in the Iowa Rural H ealth Study had a t least one site w ith LPA of 7 m illim eters or m ore.17 Even in countries where th ere is little access to m odern dental treatm en t, severe periodontitis is uncom mon among older age groups.18'21 W hen age has been used as a covariable in m ultivariate analyses, it’s identified as a risk indicator in cross-sectional studies,22 or a predictor in longitudinal studies2325 for LPA or radiographic bone loss. Both a retrospective cohort study26 and a sequential cross-sectional design27 have recorded greater radiographic loss of alveolar crestal bone in older persons. O ther recent cross-sectional studies have reported th a t clinically m easured LPA is more severe in older th a n in younger age groups.28’32 One finding contrary to this tren d was reported by H ailing and Bjorn,33 who exam ined a large group of Swedish women in 1968 and again 12 years later
in 1980. This study concluded th a t radiographic bone loss was slightly less in older th a n in m iddle-aged women during the 12 years. The authors acknowledge, however, th a t th eir conclusions could have been affected by tooth extractions. In addition, they used average radiographic bone loss as th eir m easure of periodontitis, which could have m asked individual changes. A nother gender difference was found in the Iowa Rural H ealth Study34 which noted th a t age was positively related to periodontal h ealth in women but not in men. The long-known differences in periodontal statu s betw een m en and women are usually a ttrib u ted to women’s b e tte r oral hygiene practices. These two studies m ay suggest fu rth e r exploration of periodontal gender differences. The few longitudinal studies of age as a risk factor in periodontitis, by necessity, have been m ostly conducted with special non-representative groups. Although several studies have supported the view
TABLE
A CURRENT MODEL FOR PERIODONTAL DISEASES. Only a sm all proportion of adults suffer advanced periodontal destruction. Mild gingivitis is common, as is mild-to-moderate periodontitis. Most adults show some loss of probing attachm ent while m aintaining a functioning dentition. Gingivitis precedes periodontitis, b u t relatively few sites w ith gingivitis la te r develop periodontitis. The bacterial flora associated w ith gingivitis and periodontitis have some sim ilarities b u t also some differences. Although usually related to age in cross-sectional surveys, severe periodontitis is not a n atu ral consequence of aging. Periodontitis is not the major cause of tooth loss in adults, except perhaps in the oldest age groups in some populations.
th a t age is a risk factor or predictor of LPA,24,25 others23,35 concluded th a t LPA is more related to baseline LPA th a n to age. H unt and colleagues,36 in the 18-month Iowa R ural H ealth Study, reported th a t periodontal conditions were weak predictors of tooth loss. By contrast, the H ailing and Bjorn study33 did not find radiographic bone loss related to baseline conditions. In a 15-year longitudinal study, 480 te a workers in Sri L anka showed a wide range of susceptibility to periodontitis.37 As the group had virtually no dental treatm en t, th is was probably the tru e s t study of the n a tu ra l history of periodontitis yet conducted. On the basis of tooth loss and interproxim al LPA, about 8 percent had rapid progression of periodontitis, some 81 percent showed m oderate progression and the rem aining 11 percent showed no progression beyond gingivitis. In the rapid- and m oderate-progression groups, periodontitis progressed w ith age (much more rapidly in the first group). B ut in the non progressing group, age was not a factor. This study showed th a t LPA became severe only for a sm all group of susceptible individuals. Age was a much sm aller factor in those with m oderately progressing or non progressing disease.
dem onstrated in other studies. C hristersson and colleagues38 related plaque and subgingival calculus to social factors and found th a t age was significantly correlated w ith supragingival plaque, b ut less strongly related th a n gender, race or presence of established periodontitis. Age was not significantly correlated w ith subgingival calculus in this study, carried out w ith 508 adults in up state New York. In 1989, Goodson39 presented a model of adult periodontitis th a t began w ith shallow pockets in early adulthood, after which LPA mostly increased by reces sion w ithout fu rth e r pocket deepening. Goodson concluded th a t LPA rem ained the prim e indicator of destructive perio dontitis, or w hat he called an “in v arian t” m easure. T hat conclusion is w orth rem em ber ing in respect to the 1986 study of Sheiham and colleagues,40 who revisited a group of English factory w orkers 14 years after
initial exam ination and found Periodontal Index41 scores substantially better. (The Periodontal Index m easures pockets and gingivitis, b u t not LPA.) The improved oral hygiene in the w orkers during the 14 years would have reduced gingivitis, so th a t even if the num ber of periodontal pockets had not changed between exam inations, the overall scores would have been improved by oral hygiene alone. The data from th is longitudinal study would have been more valuable had LPA been m easured on both occasions (though th a t sta te m e n t is easy to m ake in hindsight). A statew ide survey in Iowa found th a t only 2.1 percent of persons aged 55 or older had pockets of 6 m m or more, though nearly a th ird of this group had pockets of 3 to 6 mm.42 One analysis of d a ta from the first N ational H ealth and N utrition E xam ination Survey
PERCENT
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PROBING POCKET DEPTH
Although Figure 1 shows a linear relationship betw een age and the presence of a t least one site w ith LPA of 4 and 7 mm, the relationship is less clear when probing pocket depth is the m easure, as shown by the national survey data (Figure 2). Sim ilar relationships have been
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Figure 1. Proportion of men and women with at least one site with loss of periodontal attachment of 4 or 7 mm, by age. United States, 198586. (Source: Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loo H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: U.S. Government Printing Office, 1987.)
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AGE GROUPS Figure 2- Proportion of men and women w ith at least one site with probing pocket depth of 4 mm. United States, 1985-86. (Source: Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loe H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: U.S. Government Printing Office, 1987.)
(NHANES I, 1971-74) concluded th a t age was a less im portant determ inant of periodontal disease statu s (Periodontal Index scores again; gingivitis and pockets) in the elderly th a n was oral hygiene.43 A nother analysis of the same d a ta found th a t when com paring people w ith m ost tee th present, age differences in periodontal and oral hygiene sta tu s virtually disappeared.44 An NIDR analysis of an 1981 survey found th a t deep pockets, 6 m m or more, were no more extensive in people 65 or older th a n in more middle-aged groups.45 In a study of a low socioeconomic adult population in New Mexico, only 13 percent had pockets of 6 mm or more, despite extensive plaque and calculus deposits and extrem e gingivitis.46 There was an association betw een age and the presence of deep pockets, b u t 276
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not to the extent th a t would have been expected. Age and th e num ber of teeth w ith plaque accounted for less th a n 11 percent of the variance in prevalence of deep pockets. DISCUSSION
The relationship betw een aging and periodontitis has been reviewed several tim es in the la st 10 years. Page1 stated th a t periodontitis in most elderly people is slowly progressing adult periodontitis, which begins in early adulthood and progresses slowly (though probably in episodic bursts) throughout life. Reasonable m aintenance of oral hygiene and fairly simple dental tre a tm e n t is usually enough to ensure th a t teeth do not lose so m uch support th a t extraction becomes necessary. At most, no more th a n a few teeth are likely to be lost. Van der Velden2
concluded th a t there are agerelated changes in the periodon tium : th e periodontium can react differently to plaque, inflam m ation develops more rapidly and healing proceeds more slowly. He concluded, however, th a t individual susceptibility is more im portant th a n the age effect. Newell Johnson,3 sum m ariz ing a series of comprehensive reviews carried out by his group in London, found th a t while the effects of previous breakdown (LPA and bone loss) accum ulate w ith age, there is no evidence th a t susceptibility to perio dontal destruction increases w ith age. A sim ilar conclusion was reached by Bradley Johnson and colleagues4 from the U niversity of W ashington. They agreed w ith Van der Velden in concluding th a t clinical changes caused by aging alone are “therapeutically insignificant.” These reviews all reached the sim ilar conclusion th a t age alone is not a m ajor factor in th e development of severe periodontitis, especially when good oral hygiene is m ain tained. There is nothing in this cu rren t review of more recent evidence to modify th a t conclusion, but there are a few issues w orth discussing further. M easurem ent is a constant problem in periodontal studies, w hether they’re clinical studies dem anding the m ost meticulous recordings or a field survey in which more general m easures will suffice. Studies have exam ined all teeth, all tee th in two quadrants, the worst teeth in each sextant and selected index teeth. M easurem ents have been made on six, four, two and one site per tooth. Exam inations ru n from a few
m inutes per person to an hour or more, and the m ost appro priate use of high-technology diagnostic equipm ent (for example, computerized probes and DNA probes for bacterial identification) continues to be debated. All of these issues affect the d a ta discussed here, and probably will continue to do so u n til we develop some m easure of disease th a t does not depend on clinical oral assessm ent. If LPA is the invariant m easure of periodontitis,39 then ju s t how m uch LPA is enough to be clear evidence of disease? The stan d ard deviation of repeated LPA m easurem ents of the sam e site by an experienced exam iner w ith a m anual periodontal probe is about 0.8 m m.47 Change in attachm ent level in a clinical study needs to be a t least 2 mm—about two to th ree tim es the standard devi ation—before it can be accepted as real change ra th e r th a n a possible result of m easurem ent error.4849 LPA progression of at least 3 mm during one year was the criterion in one recent study for evidence of change.23 In epidemiology, using the 2-mm level to denote LPA in a crosssectional study is also questioned because this level of LPA is so common. To illu strate th a t point, Fig ure 3 shows the age distribution of LPA of 2 mm from the 198586 ad u lt survey. Most m en and women have a t least one site w ith 2 mm LPA, even a t young ages, and it is nearly universal in the older age groups. Because epidemiologic science is based on structured comparisons of persons w ith and w ithout disease, using the 2-mm level of LPA as a threshold for “disease” will not be fruitful since such a
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Figure 3. Proportion of men and women with at least one site with loss of periodontal attachment of 2 mm, by age. United States, 1985-86. (Source: Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loe H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: U.S. Government Printing Office, 1987.)
level, in a t least one site per person, is commonplace. Only w hen th e LPA cutoff lim it is raised to 4 mm does the d istri bution become skewed enough to discrim inate adequately betw een those w ith and w ithout disease for epidemiologic study.50 Epidemiologic and clinical research would be helped through more uniform definitions of m oderate and severe periodontitis, term s which cropped up regularly in this review. Older literatu re refers to virtually 100 percent prevalence of “periodontal disease” when gingivitis and all levels of periodontitis were included. The current m ethod of assessing gingivitis separately from periodontitis, and then classifying periodontitis according to degree of LPA or pocket depth, has brought a degree of sensitivity into
m easurem ents. This sensitivity was m issing w ith aggregated, average m easures. Even though m ean values in a group m ay rem ain unchanged, individual values can move either way.61 D isaggregated m easurem ent has also exposed the range of susceptibility in a population and perm itted research into why some people still lose teeth from periodontitis and others don’t. Identifying risk factors for loss of dental function (as an outcome of destructive perio dontitis) requires m ultivariate analysis, ideally w ith genetic, biological, clinical and social factors included. A generally accepted profile of periodontitis perm itting reliable categori zation of people into severem oderate-m ild grades would help in in terpreting this research. A num ber of recent studies have stated criteria for severity, based m ostly on JADA, Vol. 125, March 1994
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combinations of LPA and probing pocket depth,16'2223'2728'37 b u t no uniform ity has yet developed. A related issue on defining the seriousness of disease is th a t of extent vs. severity. Are data like those in Figure 1, based on no more th an one site of a possible 112 (28 teeth, four sites per tooth) or 168 (six sites), really giving an accurate profile of the condition? Or should th e num ber of sites affected be included to give a tru e r picture of the burden of disease? In the E xtent and Severity Index (ESI),52 “extent” refers to the num ber of teeth in th e m outh w ith LPA of 1 mm or more, and “severity” is the m ean LPA of those teeth. U sing th is index, Beck and col leagues16 recorded greater severity scores in older age groups, but found little agerelated difference in the m easures of extent. B ut because LPA of 1 mm is so common (Figure 3), th a t finding is hardly surprising. The concept of the ESI is useful, but it m ight be more so if applied with different LPA cutoff m easures. The in te n t of categorization is th a t th e term “severe” should refer to periodontitis where the loss of attach m en t and bony support is so deep th a t one or more teeth have to be extracted, or w here th ere is real likelihood of extraction. The clustering of m ost disease in a m inority of people, both in epidemiologic studies of u n tre a te d popula tions3753 and in clinical studies of w ell-m aintained patients,54 is a well-recognized phenomenon; it is th is m inority to whom the “serious” category should apply. The term “m oderate” perio dontitis could be used for those conditions w here some loss of 278
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periodontal support is evident, b ut enough rem ains to keep the tooth functional. Few longitudinal studies have studied the n a tu ra l history of periodontal progres sion in elderly populations. It is custom ary to call for more such studies, b u t perhaps th a t call m ight be reconsidered. For one thing, these studies are difficult to carry out. Populations of older people are h a rd to recruit and h ard to keep together for even two to th ree years. In addition, the evidence reviewed shows th a t dentate older people mostly have m oderate periodontitis, which is unlikely to lead to substantial tooth loss. Longitudinal studies for periodontal risk factors would be more productive among younger populations, because adult periodontitis begins in the young,5565 and the prognosis for a younger person with periodontitis is worse th a n th a t for an older person w ith a sim ilar level of disease.66 If the risk factors for early disease can be identified, corrective action m ight be tak en before the disease becomes established beyond the point of no return. If disease in those individuals can th en be stabilized, they have a chance to become dentate older adults. W hile there is still a great deal to be learned, recent research has led to a great # advance in our Dr. Burt is professor understanding and director, of periodontitis Program in Dental Public Health, in a relatively School of Public short tim e. As Health, University of Michigan, Ann Arbor, a result, the Mich. 48109-2029. current model Address reprint requests to Dr. Burt. of periodontitis
now reads like th a t in the table. (Note th a t th is review did not include the episodic or “b u rst” model of disease progression.) CONCLUSION
It is now clear th a t tooth retention, good oral hygiene and periodontal h ealth as indicated by little gingival inflam m ation and few deep pockets are closely associated, regardless of age. W ith age, some gingival shrink age and loss of periodontal attachm ent and bony support are expected, but these changes should not necessarily be seen as disease. They are probably as norm al in the healthy aging person as skin w rinkles and decreasing flexibility of the joints. The underlying conclusion from th e evidence in th is and previous reviews, however, is th a t the changes in the periodontium attrib u tab le solely to age are not sufficient to lead to tooth loss. Severe periodontitis should not be regarded as a n a tu ra l consequence of aging. ■ 1. Page RC. Periodontal diseases in the elderly: a critical evaluation of current information. Gerodontol 1984;3:63-70. 2. Van der Velden U. Effect of age on the per iodontium. J Clin Periodontol 1984;11:281-94. 3. Johnson NW. Detection of high-risk groups and individuals for periodontal diseases. In t Dent J 1989;39:33-47. 4. Johnson BD, Mulligan K, Kiyak HA, Marder M. Aging or disease? Periodontal changes and treatm ent considerations in the older dental patient. Gerodontology 1989;8:109-18. 5. Belting CM. A review of the epidemiology of periodontal diseases. J Periodontol 1957;28:37-46. 6. Lovdal A, Arno A, Waerhaug J. Incidence of clinical manifestation of periodontal disease in light of oral hygiene and calculus formation. JADA 1958;56:21-33. 7. Marshall Day CD, Stephens RG, Quigley LFJ. Periodontal disease: prevalence and incidence. J Periodontol 1955;26:185-203. 8. Moen D. Survey of needs for dental care. II. Dental needs according to age and sex of patients. JADA 1953;46:200-11. 9. Ramfjord SP, Emslie RD, Greene JC, Held A-J, Waerhaug J. Epidemiological studies of periodontal diseases. Am J Public Health 1968;58:1713-22.
RESEARCH 10. Russell AL. Epidemiology of periodontal disease. Int Dent J 1967;17:282-96. 11. Waerhaug J. Epidemiology of periodontal disease: a review of literature. In: Ramfjord SP, Kerr DA, Ash MM, eds. World workshop in periodontics. Ann Arbor: University of Michigan; 1966:181-211. 12. Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loe H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: Government Printing Office; 1987. 13. Brown L, Oliver R, Loe H. Evaluating periodontal status of U.S. employed adults. JADA 1990;121:226-32. 14. Oliver RC, Brown LJ, Loe H. Variations in the prevalence and extent of periodontitis. JADA 1991(6);122:43-8. 15. Hugoson A, Jordan T. Frequency distribution of individuals aged 20-70 years according to severity of periodontal disease. Community Dent Oral Epidemiol 1982;10:187-92. 16. Beck JD, Koch GG, Rozier RG, Tudor GE. Prevalence and risk indicators for periodontal attachm ent loss in a population of older community-dwelling blacks and whites. J Periodontol 1990;61:521-8. 17. Hunt RJ, Levy SM, Beck JD. The prevalence of periodontal attachm ent loss in an Iowa population aged 70 and older. J Public Health Dent 1990;50:251-6. 18. Baelum V, Fejerskov O, Karring T. Oral hygiene, gingivitis, and periodontal breakdown in adult Tanzanians. J Periodont Res 1986;21:221-32. 19. Baelum V, Fejerskov O, Manji F. Periodontal diseases in adult Kenyans. J Clin Periodontol 1988;15:445-52. 20. Baelum V, Wen-Min L, Fejerskov O, Xia C. Tooth mortality and periodontal conditions in 60-80-year-old Chinese. Scand J Dent Res 1988;96:99-107. 21. Matthesen M, Baelum V, Aarslev I, Fejerskov O. Dental health of children and adults in Guinea-Bissau, West Africa, in 1986. Community Dent Health 1990;7:123-33. 22. Locker D, Leake JL. Risk indicators and risk m arkers for periodontal disease exper ience in older adults living independently in Ontario, Canada. J Dent Res 1993;72:9-17. 23. HafTajee AD, Socransky SS, Lindhe J, Kent RL, Okamoto H, Yoneyama T. Clinical risk indicators for periodontal attachment loss. J Clin Periodontol 1991;18:117-25. 24. Ismail AI, Morrison EC, Burt BA, Caffesse RG, Kavanagh MT. Natural history of periodontal disease in adults: findings from the Tecumseh Periodontal Disease Study, 1959-87. J Dent Res 1990;69:430-5. 25. Nelson RG, Shlossman M, Budding LM, et al. Periodontal disease and NIDDM in Pima Indians. Diabetes Care 1990;13:836-40. 26. Papapanou PN, Wennstrom JL, Grondahl K. A 10-year retrospective study of periodontal disease progression. J Clin Periodontol 1989;16:403-11. 27. Hugoson A, Laurell L, Lundgren D. Frequency distribution of individuals aged 20-70 years according to severity of periodontal disease experience in 1973 and 1983. J Clin Periodontol 1992;19:227-32. 28. Machtei EE, Christersson LA, Grossi SG, Dunford R, Zambon JJ, Genco RJ. Clinical criteria for the definition of “established periodontitis.” J Periodontol 1992;63:206-14. 29. Okamoto H, Yoneyama T, Lindhe J, HafTajee A, Socransky S. Methods of evaluating periodontal disease data in
epidemiological research. J Clin Periodontol 1988;15:430-9. 30. Papapanou PN, Lindhe J, Sterrett JD, Eneroth L. Considerations on the contribution of ageing to loss of periodontal tissue support. J Clin Periodontol 1991;18:611-5. 31. Ship JA, Wolff A. Gingival and periodontal parameters in a population of healthy adults, 22-90 years of age. Gerodontol 1988;7:55-60. 32. Slade GD, Locker D, Leake JL, Wu AS, Dunkley G. The oral health status and treatm ent needs of adults aged 65+ living independently in Ottawa-Carleton. Can J Public Health 1990;81:114-9. 33. Hailing A, Bjorn A-L. Periodontal status in relation to age of dentate middle aged women. Swed Dent J 1986;10:233-42. 34. Levy SM, Heckert DA, Beck JD, Kohout FJ. Multivariate correlates of periodontally healthy teeth in an elderly population. Gerodontics 1987;3:85-8. 35. Papapanou PN, Wennstrom JL. A 10year retrospective study of periodontal disease progression. Clinical characteristics of subjects with pronounced and minimal disease development. J Clin Periodontol 1990;17:78-84. 36. Hunt RJ, Hand JS, Kohout FJ, Beck JD. Incidence of tooth loss among elderly Iowans. Am J Public Health 1988;78:1330-2. 37. Loe H, Anerud A, Boysen H, Morrison E. Natural history of periodontal disease in man. Rapid, moderate and no loss of attach ment in Sri Lankan laborers 14 to 46 years of age. J Clin Periodontol 1986;13:431-45. 38. Christersson LA, Grossi SG, Dunford RG, Machtei EE, Genco RJ. Dental plaque and calculus: risk indicators for their formation. J Dent Res 1992;71:1425-30. 39. Goodson JM. Selection of suitable indicators of periodontitis. In: Bader JD, ed. Risk assessment in dentistry. Chapel Hill: University of North Carolina Dental Ecology; 1990:69-74. 40. Sheiham A, Smales FC, Cushing AM, Cowell CR. Changes in periodontal health in a cohort of British workers over a 14-year period. Br Dent J 1986;160:125-7. 41. Russell AL. A system of classification and scoring for prevalence surveys of peri odontal disease. J Dent Res 1956;35:350-9. 42. Beck JD, Lainson PA, Field HM, Hawkins BF. Risk factors for various levels of periodontal disease and treatm ent needs of Iowa. Community Dent Oral Epidemiol 1984;12:17-22. 43. Abdellatif HM, Burt BA. An epidemio logical investigation into the relative importance of age and oral hygiene status as determinants of periodontitis. J Dent Res 1987;66:13-8. 44. Burt BA, Ismail AI, Eklund SA. Periodontal disease, tooth loss, and oral hygiene among older Americans. Community Dent Oral Epidemiol 1985;13:93-6. 45. Brown LJ, Oliver RC, Loe H. Periodontal diseases in the U.S. in 1981: prevalence, severity, extent, and role in tooth mortality. J Periodontol 1989;60:363-70. 46. Ismail AI, Eklund SA, Burt BA, Calderone JJ. Prevalence of deep periodontal pockets in New Mexico adults aged 27 to 44 years. J Public Health Dent 1986;46:199-206. 47. Haffajee AD, Socransky SS. Attachment level changes in destructive periodontal diseases. J Clin Periodontol 1986;13:461-75. 48. Haffajee AD, Socransky SS, Goodson JM. Comparison of different data analyses for
detecting changes in attachm ent level. J Clin Periodontol 1983;10:298-310. 49. Lindhe J, Haffajee AD, Socransky SS. Progression of periodontal disease in adult subjects in the absence of periodontal therapy. J Clin Periodontol 1983;10:433-42. 50. Burt BA. The distribution of periodontal destruction in the populations of industrialized countries. In: Johnson NW, ed. Risk markers for oral diseases. Vol. 3: Periodontal diseases. Cambridge: Cambridge University Press; 1991:9-26. 51. Lindhe J, Okamoto H, Yoneyama T, Haffajee A, Socransky SS. Longitudinal changes in periodontal disease in untreated subjects. J Clin Periodontol 1989;16:662-70. 52. Carlos JP, Wolfe MD, Kingman A. The extent and severity index: a simple method for use in epidemiologic studies of periodontal disease. J Clin Periodontol 1986;13:500-5. 53. Cutress TW, Powell RN, Ball ME. Dif fering profiles of periodontal disease in two similar South Pacific island populations. Community Dent Oral Epidemiol 1982;10:193-203. 54. Lindhe J, Nyman S. Long-term maintenance of patients treated for advanced periodontal disease. J Clin Periodontol 1984;11:504-14. 55. Al-Kufaishi KA, Hirschmann PN, Lennon MA. The radiographic assessment of early periodontal bone loss in adolescents. Br Dent J 1984;157:91-3. 56. Anerud KE, Robertson PB, Loe H, Anerud A, Boysen H, Patters RM. Periodontal disease in three young adult populations. J Periodont Res 1983;18:655-8. 57. Carlos JP, Wolfe MD, Zambon JJ, Kingman A. Periodontal disease in adolescents: some clinical and microbiologic correlates of attachm ent loss. J Dent Res 1988;67:1510-4. 58. Clerehugh V, Lennon MA. A two-year longitudinal study of early periodontitis in 14to 16-year-old schoolchildren. Community Dent Health 1986;3:135-41. 59. Hoover JN, Ellegaard B, Attstrom R. Radiographic and clinical examination of periodontal status of first molars in 15-16 year-old Danish schoolchildren. Scand J Dent Res 1981;89:260-3. 60. Kallestal C, Matsson L, Holm A-K. Periodontal conditions in a group of Swedish adolescents. I. A descriptive epidemiologic study. J Clin Periodontol 1990;17:601-8. 61. Latcham NL, Powell RN, Jago JD, Seymour GJ, Aitken JF. A radiographic study of chronic periodontitis in 15-year-old Queensland children. J Clin Periodontol 1983;10:37-45. 62. Mann J, Cormier PP, Green P, Ram CA, Miller MF, Ship II. Loss of periodontal attachment in adolescents. Community Dent Oral Epidemiol 1981;9:135-41. 63. Miyazaki H, Hanada N, Andoh MI, et al. Periodontal disease prevalence in different age groups in Japan as assessed according to the CPITN. Community Dent Oral Epidemiol 1989;17:71-4. 64. Van der Velden U. The onset age of periodontal destruction. J Clin Periodontol 1991;18:380-3. 65. Wolfe MD, Carlos JP. Periodontal disease in adolescents: epidemiologic findings in Navajo Indians. Community Dent Oral Epidemiol 1987;15:33-40. 66. Lindhe J, Socransky S, Nyman S, Westfelt E, Haffajee A. Effect of age on healing following periodontal therapy. J Clin Periodontol 1985;12:774-87.
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term “model” of disease m eans a collection of theory on etiology, transm ission, progres sion and outcome, based as far as possible on accepted research. B ut some speculation is necessarily included, so models have to be modified as new research comes out, some tim es extensively. Such is the case w ith periodontal disease (these days a term best used generically for a cluster of diseases). O ur understanding of these conditions h a s advanced so much th a t we m ust rem em ber th a t as recently as the mid1960s, th e periodontal disease model included th e following precepts: gingivitis insidiously progressed to periodontitis w ith consequent loss of bone and teeth; virtually everyone was considered susceptible to severe periodontitis; ■* susceptibility to periodontitis increased w ith age; ■* periodontal disease was the m ain cause of tooth loss after age 35. The first two points implied an aging factor, while the last two included age directly.
R E G E N T E V ID E N C E
PH.D.
A
B
S
T
R
A
C
T
This review critically examines recent research on the relation between age and periodontitis. It concludes that some loss of periodontal attachment and alveolar bone is to be expected in older persons, but age alone in a healthy adult does not lead to a critical loss of periodontal support. Although moderate loss of alveolar bone and periodontal attachment is common in the elderly, severe periodontitis is not a natural consequence of aging.
D estructive periodontal disease h as been so consistently associated w ith aging th a t m any came to see it as an inevitable consequence of growing older. Clinical observations th a t periodontitis w as a function of age are as old as the expression “getting long in the tooth.” H orse-trading transactions often depended on the buyer’s inspection of the
horse’s tee th (a practice th a t tells us th a t em pirical folk wisdom, for w hat it’s worth, sees gingival recession as a norm al p a rt of aging). N early all studies from the early days of periodontal research511 found a close association betw een age, periodontal disease and tooth loss. B ut early d a ta a t the tim e were aggregated and crosssectional. A casual reading of cross-sectional data can lead to m isleading conclusions if no allowance is m ade for cohort effects (differences betw een age groups who grew up a t different tim es under different condi tions). Recent research has questioned th e association between age and periodontitis. (This h as been sum m arized in a series of review s.1*4) This paper critically exam ines the m ost recent epidem iologic and clinical research to define more precisely the role of aging in ad u lt periodontitis. Because assessing this relation ship has been often confounded by the problem of how to deal with m issing teeth, this review focuses, as far as possible, on clinical m easures of existing teeth. JADA, Vol. 125, March 1994
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M easuring and expressing periodontal diseases in different ways can lead to different views of the distribution of these conditions—an issue discussed later. B ut w hen th e disease is m easured by loss of periodontal attach m en t (LPA) or alveolar bone loss, nearly all crosssectional studies show more severe conditions in older populations. This is evident in th e d a ta from the 1985-86 N ational Survey of Oral H ealth in U.S. Employed Adults and Seniors1214 (Figure 1) as well as in recent studies of selected populations. A Swedish report from the early 1980s15 was one of the first epidemiologic studies to look a t the distribution of LPA and radiographic bone loss, ra th e r th a n a t average periodontal scores on a scaled index. W hat a t the tim e seem ed rem arkably few people—no more th a n 8 percent in each 10-year age group in th is Swedish popu lation—showed evidence of severe periodontitis. The authors defined the condition as gingivitis, pockets and general m arginal bone loss betw een one-third and tw o-thirds of norm al height. This sm all proportion w ith severe disease in the older age groups was only slightly higher th a n in the younger, though m oderate periodontitis (generalized m arginal bone loss up to oneth ird norm al bone height) was common a t all ages. In th e longitudinal Piedm ont study in N orth Carolina, base line findings were th a t LPA was more extensive in persons aged 65 or older th a n in younger groups.16 B ut severe LPA or 274
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bone loss is not universal among healthy elderly people. Only 15 percent of persons aged 70 or older in the Iowa Rural H ealth Study had a t least one site w ith LPA of 7 m illim eters or m ore.17 Even in countries where th ere is little access to m odern dental treatm en t, severe periodontitis is uncom mon among older age groups.18'21 W hen age has been used as a covariable in m ultivariate analyses, it’s identified as a risk indicator in cross-sectional studies,22 or a predictor in longitudinal studies2325 for LPA or radiographic bone loss. Both a retrospective cohort study26 and a sequential cross-sectional design27 have recorded greater radiographic loss of alveolar crestal bone in older persons. O ther recent cross-sectional studies have reported th a t clinically m easured LPA is more severe in older th a n in younger age groups.28’32 One finding contrary to this tren d was reported by H ailing and Bjorn,33 who exam ined a large group of Swedish women in 1968 and again 12 years later
in 1980. This study concluded th a t radiographic bone loss was slightly less in older th a n in m iddle-aged women during the 12 years. The authors acknowledge, however, th a t th eir conclusions could have been affected by tooth extractions. In addition, they used average radiographic bone loss as th eir m easure of periodontitis, which could have m asked individual changes. A nother gender difference was found in the Iowa Rural H ealth Study34 which noted th a t age was positively related to periodontal h ealth in women but not in men. The long-known differences in periodontal statu s betw een m en and women are usually a ttrib u ted to women’s b e tte r oral hygiene practices. These two studies m ay suggest fu rth e r exploration of periodontal gender differences. The few longitudinal studies of age as a risk factor in periodontitis, by necessity, have been m ostly conducted with special non-representative groups. Although several studies have supported the view
TABLE
A CURRENT MODEL FOR PERIODONTAL DISEASES. Only a sm all proportion of adults suffer advanced periodontal destruction. Mild gingivitis is common, as is mild-to-moderate periodontitis. Most adults show some loss of probing attachm ent while m aintaining a functioning dentition. Gingivitis precedes periodontitis, b u t relatively few sites w ith gingivitis la te r develop periodontitis. The bacterial flora associated w ith gingivitis and periodontitis have some sim ilarities b u t also some differences. Although usually related to age in cross-sectional surveys, severe periodontitis is not a n atu ral consequence of aging. Periodontitis is not the major cause of tooth loss in adults, except perhaps in the oldest age groups in some populations.
th a t age is a risk factor or predictor of LPA,24,25 others23,35 concluded th a t LPA is more related to baseline LPA th a n to age. H unt and colleagues,36 in the 18-month Iowa R ural H ealth Study, reported th a t periodontal conditions were weak predictors of tooth loss. By contrast, the H ailing and Bjorn study33 did not find radiographic bone loss related to baseline conditions. In a 15-year longitudinal study, 480 te a workers in Sri L anka showed a wide range of susceptibility to periodontitis.37 As the group had virtually no dental treatm en t, th is was probably the tru e s t study of the n a tu ra l history of periodontitis yet conducted. On the basis of tooth loss and interproxim al LPA, about 8 percent had rapid progression of periodontitis, some 81 percent showed m oderate progression and the rem aining 11 percent showed no progression beyond gingivitis. In the rapid- and m oderate-progression groups, periodontitis progressed w ith age (much more rapidly in the first group). B ut in the non progressing group, age was not a factor. This study showed th a t LPA became severe only for a sm all group of susceptible individuals. Age was a much sm aller factor in those with m oderately progressing or non progressing disease.
dem onstrated in other studies. C hristersson and colleagues38 related plaque and subgingival calculus to social factors and found th a t age was significantly correlated w ith supragingival plaque, b ut less strongly related th a n gender, race or presence of established periodontitis. Age was not significantly correlated w ith subgingival calculus in this study, carried out w ith 508 adults in up state New York. In 1989, Goodson39 presented a model of adult periodontitis th a t began w ith shallow pockets in early adulthood, after which LPA mostly increased by reces sion w ithout fu rth e r pocket deepening. Goodson concluded th a t LPA rem ained the prim e indicator of destructive perio dontitis, or w hat he called an “in v arian t” m easure. T hat conclusion is w orth rem em ber ing in respect to the 1986 study of Sheiham and colleagues,40 who revisited a group of English factory w orkers 14 years after
initial exam ination and found Periodontal Index41 scores substantially better. (The Periodontal Index m easures pockets and gingivitis, b u t not LPA.) The improved oral hygiene in the w orkers during the 14 years would have reduced gingivitis, so th a t even if the num ber of periodontal pockets had not changed between exam inations, the overall scores would have been improved by oral hygiene alone. The data from th is longitudinal study would have been more valuable had LPA been m easured on both occasions (though th a t sta te m e n t is easy to m ake in hindsight). A statew ide survey in Iowa found th a t only 2.1 percent of persons aged 55 or older had pockets of 6 m m or more, though nearly a th ird of this group had pockets of 3 to 6 mm.42 One analysis of d a ta from the first N ational H ealth and N utrition E xam ination Survey
PERCENT
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PROBING POCKET DEPTH
Although Figure 1 shows a linear relationship betw een age and the presence of a t least one site w ith LPA of 4 and 7 mm, the relationship is less clear when probing pocket depth is the m easure, as shown by the national survey data (Figure 2). Sim ilar relationships have been
1 8 - 2 4
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4 4
4 5
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6 5 - 7 4
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Figure 1. Proportion of men and women with at least one site with loss of periodontal attachment of 4 or 7 mm, by age. United States, 198586. (Source: Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loo H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: U.S. Government Printing Office, 1987.)
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PERCENT 40
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30-34
40-44
50-54
60-64
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80+
AGE GROUPS Figure 2- Proportion of men and women w ith at least one site with probing pocket depth of 4 mm. United States, 1985-86. (Source: Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loe H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: U.S. Government Printing Office, 1987.)
(NHANES I, 1971-74) concluded th a t age was a less im portant determ inant of periodontal disease statu s (Periodontal Index scores again; gingivitis and pockets) in the elderly th a n was oral hygiene.43 A nother analysis of the same d a ta found th a t when com paring people w ith m ost tee th present, age differences in periodontal and oral hygiene sta tu s virtually disappeared.44 An NIDR analysis of an 1981 survey found th a t deep pockets, 6 m m or more, were no more extensive in people 65 or older th a n in more middle-aged groups.45 In a study of a low socioeconomic adult population in New Mexico, only 13 percent had pockets of 6 mm or more, despite extensive plaque and calculus deposits and extrem e gingivitis.46 There was an association betw een age and the presence of deep pockets, b u t 276
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not to the extent th a t would have been expected. Age and th e num ber of teeth w ith plaque accounted for less th a n 11 percent of the variance in prevalence of deep pockets. DISCUSSION
The relationship betw een aging and periodontitis has been reviewed several tim es in the la st 10 years. Page1 stated th a t periodontitis in most elderly people is slowly progressing adult periodontitis, which begins in early adulthood and progresses slowly (though probably in episodic bursts) throughout life. Reasonable m aintenance of oral hygiene and fairly simple dental tre a tm e n t is usually enough to ensure th a t teeth do not lose so m uch support th a t extraction becomes necessary. At most, no more th a n a few teeth are likely to be lost. Van der Velden2
concluded th a t there are agerelated changes in the periodon tium : th e periodontium can react differently to plaque, inflam m ation develops more rapidly and healing proceeds more slowly. He concluded, however, th a t individual susceptibility is more im portant th a n the age effect. Newell Johnson,3 sum m ariz ing a series of comprehensive reviews carried out by his group in London, found th a t while the effects of previous breakdown (LPA and bone loss) accum ulate w ith age, there is no evidence th a t susceptibility to perio dontal destruction increases w ith age. A sim ilar conclusion was reached by Bradley Johnson and colleagues4 from the U niversity of W ashington. They agreed w ith Van der Velden in concluding th a t clinical changes caused by aging alone are “therapeutically insignificant.” These reviews all reached the sim ilar conclusion th a t age alone is not a m ajor factor in th e development of severe periodontitis, especially when good oral hygiene is m ain tained. There is nothing in this cu rren t review of more recent evidence to modify th a t conclusion, but there are a few issues w orth discussing further. M easurem ent is a constant problem in periodontal studies, w hether they’re clinical studies dem anding the m ost meticulous recordings or a field survey in which more general m easures will suffice. Studies have exam ined all teeth, all tee th in two quadrants, the worst teeth in each sextant and selected index teeth. M easurem ents have been made on six, four, two and one site per tooth. Exam inations ru n from a few
m inutes per person to an hour or more, and the m ost appro priate use of high-technology diagnostic equipm ent (for example, computerized probes and DNA probes for bacterial identification) continues to be debated. All of these issues affect the d a ta discussed here, and probably will continue to do so u n til we develop some m easure of disease th a t does not depend on clinical oral assessm ent. If LPA is the invariant m easure of periodontitis,39 then ju s t how m uch LPA is enough to be clear evidence of disease? The stan d ard deviation of repeated LPA m easurem ents of the sam e site by an experienced exam iner w ith a m anual periodontal probe is about 0.8 m m.47 Change in attachm ent level in a clinical study needs to be a t least 2 mm—about two to th ree tim es the standard devi ation—before it can be accepted as real change ra th e r th a n a possible result of m easurem ent error.4849 LPA progression of at least 3 mm during one year was the criterion in one recent study for evidence of change.23 In epidemiology, using the 2-mm level to denote LPA in a crosssectional study is also questioned because this level of LPA is so common. To illu strate th a t point, Fig ure 3 shows the age distribution of LPA of 2 mm from the 198586 ad u lt survey. Most m en and women have a t least one site w ith 2 mm LPA, even a t young ages, and it is nearly universal in the older age groups. Because epidemiologic science is based on structured comparisons of persons w ith and w ithout disease, using the 2-mm level of LPA as a threshold for “disease” will not be fruitful since such a
PER C EN T
100
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20-24
30-34
40-44
50-54
60-64
70-74
80+
AGE GROUPS
Figure 3. Proportion of men and women with at least one site with loss of periodontal attachment of 2 mm, by age. United States, 1985-86. (Source: Miller AJ, Brunelle JA, Carlos JP, Brown LJ, Loe H. Oral health of United States adults; national findings. NIH Publication No. 87-2868. Washington, D.C.: U.S. Government Printing Office, 1987.)
level, in a t least one site per person, is commonplace. Only w hen th e LPA cutoff lim it is raised to 4 mm does the d istri bution become skewed enough to discrim inate adequately betw een those w ith and w ithout disease for epidemiologic study.50 Epidemiologic and clinical research would be helped through more uniform definitions of m oderate and severe periodontitis, term s which cropped up regularly in this review. Older literatu re refers to virtually 100 percent prevalence of “periodontal disease” when gingivitis and all levels of periodontitis were included. The current m ethod of assessing gingivitis separately from periodontitis, and then classifying periodontitis according to degree of LPA or pocket depth, has brought a degree of sensitivity into
m easurem ents. This sensitivity was m issing w ith aggregated, average m easures. Even though m ean values in a group m ay rem ain unchanged, individual values can move either way.61 D isaggregated m easurem ent has also exposed the range of susceptibility in a population and perm itted research into why some people still lose teeth from periodontitis and others don’t. Identifying risk factors for loss of dental function (as an outcome of destructive perio dontitis) requires m ultivariate analysis, ideally w ith genetic, biological, clinical and social factors included. A generally accepted profile of periodontitis perm itting reliable categori zation of people into severem oderate-m ild grades would help in in terpreting this research. A num ber of recent studies have stated criteria for severity, based m ostly on JADA, Vol. 125, March 1994
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combinations of LPA and probing pocket depth,16'2223'2728'37 b u t no uniform ity has yet developed. A related issue on defining the seriousness of disease is th a t of extent vs. severity. Are data like those in Figure 1, based on no more th an one site of a possible 112 (28 teeth, four sites per tooth) or 168 (six sites), really giving an accurate profile of the condition? Or should th e num ber of sites affected be included to give a tru e r picture of the burden of disease? In the E xtent and Severity Index (ESI),52 “extent” refers to the num ber of teeth in th e m outh w ith LPA of 1 mm or more, and “severity” is the m ean LPA of those teeth. U sing th is index, Beck and col leagues16 recorded greater severity scores in older age groups, but found little agerelated difference in the m easures of extent. B ut because LPA of 1 mm is so common (Figure 3), th a t finding is hardly surprising. The concept of the ESI is useful, but it m ight be more so if applied with different LPA cutoff m easures. The in te n t of categorization is th a t th e term “severe” should refer to periodontitis where the loss of attach m en t and bony support is so deep th a t one or more teeth have to be extracted, or w here th ere is real likelihood of extraction. The clustering of m ost disease in a m inority of people, both in epidemiologic studies of u n tre a te d popula tions3753 and in clinical studies of w ell-m aintained patients,54 is a well-recognized phenomenon; it is th is m inority to whom the “serious” category should apply. The term “m oderate” perio dontitis could be used for those conditions w here some loss of 278
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periodontal support is evident, b ut enough rem ains to keep the tooth functional. Few longitudinal studies have studied the n a tu ra l history of periodontal progres sion in elderly populations. It is custom ary to call for more such studies, b u t perhaps th a t call m ight be reconsidered. For one thing, these studies are difficult to carry out. Populations of older people are h a rd to recruit and h ard to keep together for even two to th ree years. In addition, the evidence reviewed shows th a t dentate older people mostly have m oderate periodontitis, which is unlikely to lead to substantial tooth loss. Longitudinal studies for periodontal risk factors would be more productive among younger populations, because adult periodontitis begins in the young,5565 and the prognosis for a younger person with periodontitis is worse th a n th a t for an older person w ith a sim ilar level of disease.66 If the risk factors for early disease can be identified, corrective action m ight be tak en before the disease becomes established beyond the point of no return. If disease in those individuals can th en be stabilized, they have a chance to become dentate older adults. W hile there is still a great deal to be learned, recent research has led to a great # advance in our Dr. Burt is professor understanding and director, of periodontitis Program in Dental Public Health, in a relatively School of Public short tim e. As Health, University of Michigan, Ann Arbor, a result, the Mich. 48109-2029. current model Address reprint requests to Dr. Burt. of periodontitis
now reads like th a t in the table. (Note th a t th is review did not include the episodic or “b u rst” model of disease progression.) CONCLUSION
It is now clear th a t tooth retention, good oral hygiene and periodontal h ealth as indicated by little gingival inflam m ation and few deep pockets are closely associated, regardless of age. W ith age, some gingival shrink age and loss of periodontal attachm ent and bony support are expected, but these changes should not necessarily be seen as disease. They are probably as norm al in the healthy aging person as skin w rinkles and decreasing flexibility of the joints. The underlying conclusion from th e evidence in th is and previous reviews, however, is th a t the changes in the periodontium attrib u tab le solely to age are not sufficient to lead to tooth loss. Severe periodontitis should not be regarded as a n a tu ra l consequence of aging. ■ 1. Page RC. Periodontal diseases in the elderly: a critical evaluation of current information. Gerodontol 1984;3:63-70. 2. Van der Velden U. Effect of age on the per iodontium. J Clin Periodontol 1984;11:281-94. 3. Johnson NW. Detection of high-risk groups and individuals for periodontal diseases. In t Dent J 1989;39:33-47. 4. Johnson BD, Mulligan K, Kiyak HA, Marder M. Aging or disease? Periodontal changes and treatm ent considerations in the older dental patient. Gerodontology 1989;8:109-18. 5. Belting CM. A review of the epidemiology of periodontal diseases. J Periodontol 1957;28:37-46. 6. Lovdal A, Arno A, Waerhaug J. Incidence of clinical manifestation of periodontal disease in light of oral hygiene and calculus formation. JADA 1958;56:21-33. 7. Marshall Day CD, Stephens RG, Quigley LFJ. Periodontal disease: prevalence and incidence. J Periodontol 1955;26:185-203. 8. Moen D. Survey of needs for dental care. II. Dental needs according to age and sex of patients. JADA 1953;46:200-11. 9. Ramfjord SP, Emslie RD, Greene JC, Held A-J, Waerhaug J. Epidemiological studies of periodontal diseases. Am J Public Health 1968;58:1713-22.
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