lfil
Guest Editorial Diabetes and Periodontal Disease "The
may not be to the swift nor the victory to the but that's the way you bet." strong, .Damon Runyon race
.
.
Should a patient with Type 2, non-insulin-dependent, diabetes mellitus (NIDDM) bet that he is more or less likely
develop Periodontitis
because of his metabolic disease? the odds either way? Until now, a periodontist might answer that the chances of suffering periodontal breakdown related to diabetes were either more or the same as for non-diabetics. Now, with the publication of the paper by Emrich et al. in this issue of the Journal,1 the periodontist can respond with confidence. "About 3 times more than if you did not have diabetes. (That is, if you are a Pirna Indian over the age of 15)." On the other hand, if the concerned patient is a young Brazilian with Type 1, insulin-dependent diabetes mellitus (IDDM), the periodontist could say, on the basis of the report by Novaes et al., also in this issue of the Journal,2 "Not any more than a non-diabetic person of your age." By their juxtaposition, these two articles dramatically illustrate several of the reasons why there has been so much confusion and disagreement in the literature about a diabetes-periodontal disease interrelationship: 1) there are two different types of diabetes, each with its own set of characteristics, but they frequently have been mixed in the groups being studied; 2) controls have often been presumed to be non-diabetic without documentation of normal glucose tolerance; 3) different measures and indices of periodontal destruction have been used: 4) variable and non-comparable data sets have been collected and analyzed by widely varying statistical methods; and 5) study populations have frequently been too small to allow age cohort subsets to include sufficient numbers to be meaningful. Therefore, much of the early search for a possible diabetes mellitus-periodontal disease relationship is, with a few noteworthy exceptions, inconclusive. Both of the entities being compared were ill-defined. Worse, control subjects, presumably non-diabetic, might have shown abnormal or diabetic glucose tolerance curves had they been tested. It was not until 1956 that Russell's periodontal index (PI) appeared,3 and 1959 that Ramfjord described the periodontal disease index (PDI), a systematic procedure for measuring, scoring, and classifying periodontal diseases.4 The gingival index (GI) and the plaque index (PI) were not published until 4 years later. Prior to such standardization, epidemiological studies of prevalence and severity of periodontal disease were uncertain at best and frequently to
What
are
misleading.
Similarly, definition and classification of diabetes mellitus was confused and controversial until the 1970s. The 1979 report of the National Diabetes Data Group established clear guidelines for the various categories of glucose intolerance, based chiefly on standardized fasting blood glucose levels or glucose tolerance tests.5 Yet, despite clearer definition and standardization, recent reports still disagree. Some investigators find a diabetesperiodontal disease relationship while others do not. The contradictory findings hold for both IDDM and NIDDM. The two articles in this issue illustrate this point, as well as some of the other difficulties, such as methodology, inherent in comparing one diabetes-perio correlation study with others. Emrich et al.,1 studying NIDDM among the Pirna Indians, in sharp contrast to the equivocal conclusions of many previous investigators, firmly state, "Diabetes is consistently and strongly related to destructive periodontal disease among young and middle-aged adults. It is reasonable to suggest that diabetes is a predictor of periodontal disease and, furthermore, that periodontal disease can be considered a complication of diabetes mellitus." On the other hand, Novaes et al,2 looking at IDDM, find that the only periodontal difference between 30 IDDM subjects ages 5 to 18 and 30 same age-range presumably non-diabetic controls was a moderate but statistically significant (0.4 mm) increase in bone loss about the upper and lower anterior teeth. There was also more plaque accumulation and higher gingival index in the diabetic subjects. The forceful conclusions stated by Emrich and associates certainly seem to be warranted by the data they collected in this large scale, elegant, and meticulously executed study. Whether these results may be generalized to other racial and ethnic groups, however, must, as the authors point out, await further confirmation. "However," they remark, "there is evidence in several Caucasian groups for greater severity of periodontal disease among diabetic subjects with both insulin and non-insulin dependent diabetes 6"13" (authors' references). Yet, when one searches for clues about the racial and ethnic mix of the diabetic or control groups in many referenced publications, the information is frequently not given. From study to study, there may well be differences in race and ethnicity in the subject populations that might affect the findings and certainly their comparability. Epidemiological studies from many parts of the world clearly demonstrate variations in prevalence and incidence of NIDDM among different populations. In the United States, which has been studied more intensively than other countries, it has been shown that prevalence and incidence rates of NIDDM among blacks, Mexican Americans, and American Indians are higher
162
J Periodontol 1991
GUEST EDITORIAL
than among other groups. The major risk factors for NIDDM are increasing age, higher blood glucose, family history of diabetes, obesity, and race. For all groups, the incidence of NIDDM increases with age, although the curves differ. Between ages 45 and 74 blacks develop NIDDM at a much higher rate than whites, so the prevalence rate of blacks among the NIDDM population ages 45 to 74 is almost 20%, although blacks make up only about 10% of the general population.14 In 1976-1980 blacks had a 50% greater prevalence of diabetes than whites.14 Future epidemiological studies of NIDDM related to periodontal disease will have to identify the racial mix of the study population and ensure that the subject and control groups are comparable. For IDDM, there are also differences in prevalence across different populations. In the United States, whites have a greater incidence and prevalence of IDDM than blacks. IDDM is unknown among the Pirna Indians.14 Just as there are racial-ethnic variations in frequency of diabetes, there are similar variations in the epidemiology of juvenile Periodontitis (JP). Reliable studies using standardized periodontal indices and yielding hard data are few, but prevalence of JP seems to vary from 0.1% in Finland15 to about 0.4% (or slightly higher) in other countries. Most authorities agree that in the United States localized JP (LJP) is more frequent in blacks than in whites. Two recent observations may be relevant. Moore has pointed out that the data describing numbers and percentages of subgingival bacteria are "influenced by the racial composition of the individuals making up the population of the study." There is an effect of race on the flora. P. gingivalis and W. recta are highly associated with blacks over whites, while F. nucleatum is more associated with whites over blacks both in cross-sectional and longitudinal studies.16 Furthermore, recent evidence gathered by Schenkein and associates in studying blackwhite pairings for healthy periodontium, juvenile and severe Periodontitis discloses that there are significant racial differences in neutrophil Chemotaxis.17 Since it has been reported that the pattern of periodontal destruction found in post-pubertal IDDM young people is most often similar to LJP, it is important in correlation studies to be able to distinguish non-diabetes related Periodontitis from that which is modified by the metabolic disease. From the foregoing, it is apparent that confidence that the prevalence rates of the Periodontitis in both test and control groups are unbiased is dependent on the close comparability of the subjects in each group. As demonstrated in the study by Barnett et al. and pointed out in their discussion,18 the racial mix in each group is crucial to their comparability. The contrasting results of several often-cited studies on IDDM-periodontal disease may be explained by one study having a different ratio of black to white subjects in the IDDM group than in the control group12 and the comparison study having black to white ratios better
balanced.8
The Pirna Indians of the Gila River Community have the highest reported incidence and prevalence of Type 2 dia-
February
betes in the world.19 Thus, this group provides a unique and immensely valuable opportunity to study the relationship between NIDDM and destructive periodontal disease. Since 50% of those above 35 years of age have diabetes, Emrich and associates had large numbers of diabetic subjects, age 15 and older, for periodontal examination. Even more important is the fact that the non-diabetic controls were documented by glucose tolerance test and are racially, ethnically, and otherwise demographically comparable to the diabetic subjects. The variables are minimized. The purity of the comparison is impressive. The results are, therefore, more meaningful than in any previous study of this type. For example, the finding that diabetic subjects aged 15 to 24 suffered 4.8 times more periodontal disease than normal subjects is powerful and unequivocal. The statistical methods employed in this study are also noteworthy. By selecting a subset, those with 6 "index teeth," these investigators were able to examine the relationship of all the oral health variables measured to destructive periodontal disease. Prevalence and severity of periodontal disease were assessed by using two measures, probing attachment loss and bone loss scores on radiographs, which were then analyzed separately. The estimate of periodontal disease risk of this group of subjects, "the magnitude of the effect of the variables," and the odds ratio are terms in a statistical language that a clinician can understand and relate to. Emrich and collaborators have made a significant contribution. In my opinion, this important study has set a standard that may be difficult to match, but that should be the goal of future investigations. Robert Gottsegen, D.D.S.,
Professor Emeritus of Dentistry, Division of Periodontics, School of Dental and Oral Surgery, Columbia University, New
York, NY.
REFERENCES 1. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in noninsulin-dependent diabetes mellitus. J Periodontol 1991; 62:123-131. 2. Novaes AB Jr., Pereira LA, deMoraes N, Novaes BN. Manifestations of insulin-dependent diabetes mellitus in the periodontium of young Brazilian patients. J Periodontol 1991; 62:116-122. 3. Russell AL. A system of classification and scoring for periodontal disease. / Dent Res 1956; 35:350. 4. Ramfjord SP. Indices for prevalence and incidence of periodontal diseases. J Periodontol 1959; 30:51. 5. National Diabetes Data Group. Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 1979; 28:1039. 6. Cohen DW, Friedman LA, Shapiro J, Kyle GC, Franklin S. Diabetes mellitus and periodontal disease: Two-year longitudinal observation. Part I. J Periodontol 1970; 41:709. 7. Finestone AJ, Boorajy SR. Diabetes mellitus and periodontal disease. Diabetes 1967; 16:336. 8. Sznajder N, Carrara JJ, Rugna S, Sereday M. Periodontal findings in diabetic and non-diabetic patients. J Periodontol 1978; 49:445. 9. Mackenzie RS, Miliard HD. Interrelated effects of diabetes, arteriosclerosis and calculus on alveolar bone loss. J Am Dent Assoc 1963; 66:191. 10. Belting CM, Hinniker JJ, Dummett CO. Influence of diabetes mellitus on the severity of periodontal diseases. J Periodontol 1964; 35:476.
Volume 62 Number 2 11. Benveniste R, Bixler D, Connealy PM. Periodontal disease in diabetics. ./ Periodontal 1967; 38:271. 12. Cianciola LJ, Park BH, Bruck E, Mosovich L, Genco RJ. Prevalence of periodontal disease in insulin-dependent diabetes mellitus (juvenile diabetes)./ Am Dent Assoc 1982; 104:653. 13. Glavind L, Lund , Loe . The relationship between periodontal state and diabetes duration, insulin dosage, and retinal changes. J Periodontal 1968; 29:341. 14. National Diabetes Data Group. Diabetes in America: Diabetes Data Compiled 1984. US Department of Health and Human Services. Public Health Service. National Institute of Arthritis, Diabetes, and Digestive and Kidney Diseases. N1H Publication 85-1468. August 1985. 15. Saxen L. Juvenile Periodontitis. A review../ Clin Periodontal 1980; 7:1.
GUEST EDITORIAL
163
16. Genco
RJ, Moore WEC. Focussed discussion. Can the majority of periodontal diseases be explained by the presence of a few specific pathogens? 8th International Conference on Periodontal Research. San
Antonio, TX. November 15-18, 1990. 17. Schenkein HA. The influence of race and periodontal clinical status on neutrophil chemotactic response. 8th International Conference on Periodontal Research. San Antonio, TX. November 15-18, 1990. 18. Barnett ML, Baker RL, Yancey JM, MacMillan DR, Kotoyan M. Absence of Periodontitis in a population of insulin-dependent diabetes mellitus (IDDM) patients../ Periodontal 1984; 55:402. 19. Knowler WC, Bennett PH, Hamman RF, Miller M. Diabetes incidence and prevalence in Pirna Indians: A 19-fold greater incidence than in Rochester, Minnesota. Am J Epidemiol 1978; 108:497.
Guest Editorial Diabetes and Periodontal Disease "The
may not be to the swift nor the victory to the but that's the way you bet." strong, .Damon Runyon race
.
.
Should a patient with Type 2, non-insulin-dependent, diabetes mellitus (NIDDM) bet that he is more or less likely
develop Periodontitis
because of his metabolic disease? the odds either way? Until now, a periodontist might answer that the chances of suffering periodontal breakdown related to diabetes were either more or the same as for non-diabetics. Now, with the publication of the paper by Emrich et al. in this issue of the Journal,1 the periodontist can respond with confidence. "About 3 times more than if you did not have diabetes. (That is, if you are a Pirna Indian over the age of 15)." On the other hand, if the concerned patient is a young Brazilian with Type 1, insulin-dependent diabetes mellitus (IDDM), the periodontist could say, on the basis of the report by Novaes et al., also in this issue of the Journal,2 "Not any more than a non-diabetic person of your age." By their juxtaposition, these two articles dramatically illustrate several of the reasons why there has been so much confusion and disagreement in the literature about a diabetes-periodontal disease interrelationship: 1) there are two different types of diabetes, each with its own set of characteristics, but they frequently have been mixed in the groups being studied; 2) controls have often been presumed to be non-diabetic without documentation of normal glucose tolerance; 3) different measures and indices of periodontal destruction have been used: 4) variable and non-comparable data sets have been collected and analyzed by widely varying statistical methods; and 5) study populations have frequently been too small to allow age cohort subsets to include sufficient numbers to be meaningful. Therefore, much of the early search for a possible diabetes mellitus-periodontal disease relationship is, with a few noteworthy exceptions, inconclusive. Both of the entities being compared were ill-defined. Worse, control subjects, presumably non-diabetic, might have shown abnormal or diabetic glucose tolerance curves had they been tested. It was not until 1956 that Russell's periodontal index (PI) appeared,3 and 1959 that Ramfjord described the periodontal disease index (PDI), a systematic procedure for measuring, scoring, and classifying periodontal diseases.4 The gingival index (GI) and the plaque index (PI) were not published until 4 years later. Prior to such standardization, epidemiological studies of prevalence and severity of periodontal disease were uncertain at best and frequently to
What
are
misleading.
Similarly, definition and classification of diabetes mellitus was confused and controversial until the 1970s. The 1979 report of the National Diabetes Data Group established clear guidelines for the various categories of glucose intolerance, based chiefly on standardized fasting blood glucose levels or glucose tolerance tests.5 Yet, despite clearer definition and standardization, recent reports still disagree. Some investigators find a diabetesperiodontal disease relationship while others do not. The contradictory findings hold for both IDDM and NIDDM. The two articles in this issue illustrate this point, as well as some of the other difficulties, such as methodology, inherent in comparing one diabetes-perio correlation study with others. Emrich et al.,1 studying NIDDM among the Pirna Indians, in sharp contrast to the equivocal conclusions of many previous investigators, firmly state, "Diabetes is consistently and strongly related to destructive periodontal disease among young and middle-aged adults. It is reasonable to suggest that diabetes is a predictor of periodontal disease and, furthermore, that periodontal disease can be considered a complication of diabetes mellitus." On the other hand, Novaes et al,2 looking at IDDM, find that the only periodontal difference between 30 IDDM subjects ages 5 to 18 and 30 same age-range presumably non-diabetic controls was a moderate but statistically significant (0.4 mm) increase in bone loss about the upper and lower anterior teeth. There was also more plaque accumulation and higher gingival index in the diabetic subjects. The forceful conclusions stated by Emrich and associates certainly seem to be warranted by the data they collected in this large scale, elegant, and meticulously executed study. Whether these results may be generalized to other racial and ethnic groups, however, must, as the authors point out, await further confirmation. "However," they remark, "there is evidence in several Caucasian groups for greater severity of periodontal disease among diabetic subjects with both insulin and non-insulin dependent diabetes 6"13" (authors' references). Yet, when one searches for clues about the racial and ethnic mix of the diabetic or control groups in many referenced publications, the information is frequently not given. From study to study, there may well be differences in race and ethnicity in the subject populations that might affect the findings and certainly their comparability. Epidemiological studies from many parts of the world clearly demonstrate variations in prevalence and incidence of NIDDM among different populations. In the United States, which has been studied more intensively than other countries, it has been shown that prevalence and incidence rates of NIDDM among blacks, Mexican Americans, and American Indians are higher
162
J Periodontol 1991
GUEST EDITORIAL
than among other groups. The major risk factors for NIDDM are increasing age, higher blood glucose, family history of diabetes, obesity, and race. For all groups, the incidence of NIDDM increases with age, although the curves differ. Between ages 45 and 74 blacks develop NIDDM at a much higher rate than whites, so the prevalence rate of blacks among the NIDDM population ages 45 to 74 is almost 20%, although blacks make up only about 10% of the general population.14 In 1976-1980 blacks had a 50% greater prevalence of diabetes than whites.14 Future epidemiological studies of NIDDM related to periodontal disease will have to identify the racial mix of the study population and ensure that the subject and control groups are comparable. For IDDM, there are also differences in prevalence across different populations. In the United States, whites have a greater incidence and prevalence of IDDM than blacks. IDDM is unknown among the Pirna Indians.14 Just as there are racial-ethnic variations in frequency of diabetes, there are similar variations in the epidemiology of juvenile Periodontitis (JP). Reliable studies using standardized periodontal indices and yielding hard data are few, but prevalence of JP seems to vary from 0.1% in Finland15 to about 0.4% (or slightly higher) in other countries. Most authorities agree that in the United States localized JP (LJP) is more frequent in blacks than in whites. Two recent observations may be relevant. Moore has pointed out that the data describing numbers and percentages of subgingival bacteria are "influenced by the racial composition of the individuals making up the population of the study." There is an effect of race on the flora. P. gingivalis and W. recta are highly associated with blacks over whites, while F. nucleatum is more associated with whites over blacks both in cross-sectional and longitudinal studies.16 Furthermore, recent evidence gathered by Schenkein and associates in studying blackwhite pairings for healthy periodontium, juvenile and severe Periodontitis discloses that there are significant racial differences in neutrophil Chemotaxis.17 Since it has been reported that the pattern of periodontal destruction found in post-pubertal IDDM young people is most often similar to LJP, it is important in correlation studies to be able to distinguish non-diabetes related Periodontitis from that which is modified by the metabolic disease. From the foregoing, it is apparent that confidence that the prevalence rates of the Periodontitis in both test and control groups are unbiased is dependent on the close comparability of the subjects in each group. As demonstrated in the study by Barnett et al. and pointed out in their discussion,18 the racial mix in each group is crucial to their comparability. The contrasting results of several often-cited studies on IDDM-periodontal disease may be explained by one study having a different ratio of black to white subjects in the IDDM group than in the control group12 and the comparison study having black to white ratios better
balanced.8
The Pirna Indians of the Gila River Community have the highest reported incidence and prevalence of Type 2 dia-
February
betes in the world.19 Thus, this group provides a unique and immensely valuable opportunity to study the relationship between NIDDM and destructive periodontal disease. Since 50% of those above 35 years of age have diabetes, Emrich and associates had large numbers of diabetic subjects, age 15 and older, for periodontal examination. Even more important is the fact that the non-diabetic controls were documented by glucose tolerance test and are racially, ethnically, and otherwise demographically comparable to the diabetic subjects. The variables are minimized. The purity of the comparison is impressive. The results are, therefore, more meaningful than in any previous study of this type. For example, the finding that diabetic subjects aged 15 to 24 suffered 4.8 times more periodontal disease than normal subjects is powerful and unequivocal. The statistical methods employed in this study are also noteworthy. By selecting a subset, those with 6 "index teeth," these investigators were able to examine the relationship of all the oral health variables measured to destructive periodontal disease. Prevalence and severity of periodontal disease were assessed by using two measures, probing attachment loss and bone loss scores on radiographs, which were then analyzed separately. The estimate of periodontal disease risk of this group of subjects, "the magnitude of the effect of the variables," and the odds ratio are terms in a statistical language that a clinician can understand and relate to. Emrich and collaborators have made a significant contribution. In my opinion, this important study has set a standard that may be difficult to match, but that should be the goal of future investigations. Robert Gottsegen, D.D.S.,
Professor Emeritus of Dentistry, Division of Periodontics, School of Dental and Oral Surgery, Columbia University, New
York, NY.
REFERENCES 1. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in noninsulin-dependent diabetes mellitus. J Periodontol 1991; 62:123-131. 2. Novaes AB Jr., Pereira LA, deMoraes N, Novaes BN. Manifestations of insulin-dependent diabetes mellitus in the periodontium of young Brazilian patients. J Periodontol 1991; 62:116-122. 3. Russell AL. A system of classification and scoring for periodontal disease. / Dent Res 1956; 35:350. 4. Ramfjord SP. Indices for prevalence and incidence of periodontal diseases. J Periodontol 1959; 30:51. 5. National Diabetes Data Group. Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 1979; 28:1039. 6. Cohen DW, Friedman LA, Shapiro J, Kyle GC, Franklin S. Diabetes mellitus and periodontal disease: Two-year longitudinal observation. Part I. J Periodontol 1970; 41:709. 7. Finestone AJ, Boorajy SR. Diabetes mellitus and periodontal disease. Diabetes 1967; 16:336. 8. Sznajder N, Carrara JJ, Rugna S, Sereday M. Periodontal findings in diabetic and non-diabetic patients. J Periodontol 1978; 49:445. 9. Mackenzie RS, Miliard HD. Interrelated effects of diabetes, arteriosclerosis and calculus on alveolar bone loss. J Am Dent Assoc 1963; 66:191. 10. Belting CM, Hinniker JJ, Dummett CO. Influence of diabetes mellitus on the severity of periodontal diseases. J Periodontol 1964; 35:476.
Volume 62 Number 2 11. Benveniste R, Bixler D, Connealy PM. Periodontal disease in diabetics. ./ Periodontal 1967; 38:271. 12. Cianciola LJ, Park BH, Bruck E, Mosovich L, Genco RJ. Prevalence of periodontal disease in insulin-dependent diabetes mellitus (juvenile diabetes)./ Am Dent Assoc 1982; 104:653. 13. Glavind L, Lund , Loe . The relationship between periodontal state and diabetes duration, insulin dosage, and retinal changes. J Periodontal 1968; 29:341. 14. National Diabetes Data Group. Diabetes in America: Diabetes Data Compiled 1984. US Department of Health and Human Services. Public Health Service. National Institute of Arthritis, Diabetes, and Digestive and Kidney Diseases. N1H Publication 85-1468. August 1985. 15. Saxen L. Juvenile Periodontitis. A review../ Clin Periodontal 1980; 7:1.
GUEST EDITORIAL
163
16. Genco
RJ, Moore WEC. Focussed discussion. Can the majority of periodontal diseases be explained by the presence of a few specific pathogens? 8th International Conference on Periodontal Research. San
Antonio, TX. November 15-18, 1990. 17. Schenkein HA. The influence of race and periodontal clinical status on neutrophil chemotactic response. 8th International Conference on Periodontal Research. San Antonio, TX. November 15-18, 1990. 18. Barnett ML, Baker RL, Yancey JM, MacMillan DR, Kotoyan M. Absence of Periodontitis in a population of insulin-dependent diabetes mellitus (IDDM) patients../ Periodontal 1984; 55:402. 19. Knowler WC, Bennett PH, Hamman RF, Miller M. Diabetes incidence and prevalence in Pirna Indians: A 19-fold greater incidence than in Rochester, Minnesota. Am J Epidemiol 1978; 108:497.
