23
ment. The greatest periodontal destruction has been found among diabetics who have had the disease for over 10 years and those who have had retinal changes. In the present study the prevalence and severity of periodontal disease were investigated in two groups of patients, diabetics and nondiabetics, with an analysis of possible relationships between the local factors (plaque and calculus) and the clinical manifestations of perio dontal disease (gingival inflammation and loss of attach ment) in both groups.
Periodontal Findings in Diabetic and Nondiabetic Patients
24
by N O R M A SZNAJDER*,
MATERIALS AND METHODS
JUAN JOSE CARRARO*
Subjects for the study were 148 patients, 120 females and 28 males, aged between 9 and 50 years with an average age of 30. They were referred from the Endocri nology and Nutrition Department to the Department of Periodontics of Fiorito Hospital in Buenos Aires. The large sex difference in the sample (81% of the patients were females) was presumably due to the fact that women are more likely than men to seek medical atten tion. The experimental group consisted of 83 diabetics and there were 65 nondiabetic controls. All data con cerning age and sex are shown in Table I. Taking into account the mean age of both groups (x 30 years), the patients were divided into those under and over 30 years of age. Most of the younger diabetics had had an early start of the illness.
SUSANA R U G N A *
MARTA SEREDAY† THE PROBABLE influence of diabetes on the onset and development of periodontal disease has been studied for many years. On the basis of experimental and clinical investigations, it is generally accepted that diabetes may result in a greater severity of periodontal disease, espe cially in juvenile diabetics. Periodontal alterations in diabetes mellitus have been studied in laboratory animals to determine the biologic mechanisms which may stimulate destruction of perio dontal tissues, as well as the possible relationship be tween diabetes and local etiologic factors. Diabetes may be experimentally induced by administering alloxan, which can destroy the ß cells of the pancreas, or by performing a partial pancreatectomy. It also may occur spontaneously in certain types of hamsters or mice. These investigations consistently have shown a greater severity of periodontal disease in diabetic animals, which increases gradually with age. However, in none of these studies has it been possible to induce periodontal disease experimentally without local irritational factors. Diabe tes apparently serves as a predisposing factor which can accelerate the periodontal destruction originated by mi crobial agents. Results of histologic studies performed with light and electron microscopy have been variously interpreted, but they suggest a higher preva lence of gingival vascular changes in diabetics than in nondiabetics. These vascular changes are neither specific nor different from those found in control groups, both in experimental animals and in humans. Clinical investigations of the influence of diabetes on the onset and development of periodontal disease have produced results which differ significantly. Some studies indicate a greater prevalence and severity in diabetics than in nondiabetics with similar levels of Plaque and Calculus Indices while others show no differ ences. The clinical parameters that showed impor tant changes are the Gingival Index and loss of attach 1,2
3
Systemic Examination This study consisted of the analysis of tests for blood sugar, glycosuria and glucose tolerance. Diabetic patients were considered to be those who under fasting conditions exhibited two or more blood sugars higher than 1.50 gm% with positive glycosurias or glucose tolerance test scores higher than 2 gm% after one hour, higher than 1.80 gm/100 ml after 2 hours, and a positive family history of diabetes. Patients considered as nondiabetics (control group) had glucose tolerance test scores lower than 1.40 gm/100 ml after 1 hour, lower than 1.20 gm/100 ml after 2 hours and a negative family history of diabetes. The blood sugars and glycosurias were quantitated through the orthotoluidine method. Patients who exhibited intermediate values relative to the above cri teria were eliminated in order to exclude all doubtful cases. Patients weighing more than 20% of their ideal body weight were excluded as well as patients with nephritis, hepatitis, cardiac and collagen diseases and severe endocrinopathy (Cushing's disease, hypophyseal adenoma, etc.), and all chronic diseases liable to alter the carbohydrate metabolism. In selecting the control patients, their family histories were carefully checked for diabetes and obstetrical rec ords were investigated for toxaemia, gestational obesity, fetus weighing more than 4,000 gm at delivery, and perinatal mortality. Patients over 50 were not included in the study since the prevalence and the severity of periodontal disease increase gradually with age, probably as a result of the cumulative effect of tissue destruction.
4
5
6-13
14-16
25,26
17-20
13,21,22
* Departamentos de Odontología, Hospital Pedro Fiorito, Belgrano 851, Avellaneda, Buenos Aires, Argentina. †Departamentos de Endocrinología y Nutricíon, Hospital Pedro Fiorito. 445
446
J. Periodontal. September, 1978
Sznajder, Carraro, Rugna, Sereday TABLE I. Age and Sex Distribution in Diabetic and Control Group Sex
Males
Age
Females
Diabetics Controls
20 8
63 57
Total
28
120
≤30 years
Whole group Range
Range
Mean
9-49 9-50
9-29 9-29
31.0 30.6
>30 years
Mean
Range
Mean
18.5 19.5
30-49 30-50
43.4 41.6
TABLE II. Gingival Index in Diabetic and Control Subjects Over and Under 30 Years of Age
Periodontal Examination The periodontal examination was performed without knowledge of the patient's systemic status. Gingival, Calculus and Plaque Indices were computed in all cases according to the Periodontal Disease Index of Ramfjord while loss of attachment was measured in millimeters from the cementoenamel junction to the bottom of the pocket for the same teeth that are exam ined for the P.D.I. The measurements were made on the buccal, lingual, mesial and distal surfaces of each tooth. Of the four, the one indicating the deepest loss of attach ment was taken as the individual measurement of each tooth. The total loss of attachment was computed by adding the individual losses of attachment and dividing the sum by the number of scored teeth. The mean error in measurement was calculated with Eramko's method and agreement was found in 96%. All data were statistically analyzed. Average values for each Index in the diabetic and control patients and between both age groups were compared by means of a two-way analysis of variance with unequal replications. Correlations between local factors (Plaque and Calculus) and clinical manifestations of periodontal disease (Gin gival Index and loss of attachment) were analyzed.
Age years ≤30
27
>30
Group
No.
Mean
SD
Diabetics Controls
20 26
1.32 1.01
± ±
0.73* 0.60*
Diabetics Controls
63 39
1.69 1.53
± ±
0.66* 0.58*
* The differences are statistically significant, P < 0.05.
TABLE III. Plaque Index in Diabetics and Controls Over and Under 30 Years of Age Age years ≤30
28
>30
Group
No.
Mean
SD
Diabetics Controls
20 26
1.98 1.77
± ±
0.55 0.53
Diabetics Controls
63 39
2.12 1.95
± ±
0.56 0.57
29
RESULTS
TABLE IV. Calculus Index in Diabetics and Controls Over and Under 30 Years of Age Age years ≤30
Gingival Index In patients under 30 the diabetic group showed a higher level of gingival inflammation (1.32 ± 0.7) than the control group (1.01 ± 0.6). Diabetics over 30 also showed a more severe gingival condition (1.60 ± 0.66) than the control patients (1.53 ± 0.58). The differences between the diabetic and control patients were statisti cally significant in both age groups (Table II). Plaque and Calculus Indices The Plaque Index was higher in the under-30 diabetic group (1.98 ± 0.55) than in the control group (1.77 ± 0.56). The same result was found in the over-30 group, with a mean Index score of 2.12 ± 0.56 in the diabetics, and 1.95 ± 0.57 in the control patients. In neither age classification were the differences statistically significant (Tables III and IV). Loss of Attachment The mean loss of attachment in patients under 30 was 1.54 ± 0.58 mm in diabetics and 1.55 ± 0.79 mm in the
>30
SD
Group
No.
Mean
Diabetics Controls
20 26
0.36 0.49
± ±
0.65 0.55
Diabetics Controls
63 39
1.21 1.07
± ±
0.73 0.67
controls. The difference was not statistically significant (P > 0.8). In patients over 30 the mean loss was 3.36 ± 1.67 mm in diabetics and 2.51 ± 1.61 mm in the controls. The difference was statistically significant (P < 0.005) (Table V). The Gingival, Calculus and Plaque Indices and the scores for loss of attachment for all diabetic and control subjects, regardless of age, are shown in Table VI. Correlations In the under-30 diabetic group a significant correlation was found between: (1) Plaque Index and Gingival Index, (2) Calculus Index and Loss of Attachment and (3) Gingival Index and Loss of Attachment. In the control group there were significant correlations only between the Gingival Index and Plaque Index and be tween the Gingival Index and Calculus Index.
Volume 49 Number 9
Diabetic and Nondiabetic Patients 447
TABLE V. LOSS of Attachment in Diabetics and Controls Over and urements and observations. It was not unusual to find Under JO Years ofAge diabetic patients with normal or almost normal gingiva Age
No.
Group
Mean
SD
and supporting structures. These cases coincided rather consistently with reduced levels of plaque and calculus. Comparing the results of various controlled clinical 1.54 ± 20 2.18 Diabetics 26 1.55 ± 1.79 Controls studies on periodontal disease and diabetes is difficult for the following reasons: (a) different Periodontal Indi1.67* 63 3.36 >30 Diabetics ces have been used in many instances and (b) the 39 2.51 ± 1.61* Controls methods of classifying the diabetic subjects have not * The differences are statistically significant, P < 0.005. been uniform. Uniformity in the classification of diaTABLE VI. Gingival, Calculus and Plaque Indices and Loss of Attachbetics is essential if greater consistency is to be achieved ment in the Entire Group of Diabetic and Control Subjects in investigations of the relationship between periodontal Mean SD Group No. disease and diabetes. Uniformity is difficult to attain since the continuing discussion involving the diabetic Gingival Index syndrome makes it difficult to accurately outline a clinDiabetics 83 1.60 ± 0.69* ical taxonomy which permits an analysis of the diabetic Controls 65 0.64* 132 ± influence on periodontal tissues. In some studies diaCalculus Index betics have been classified as prediabetes, juvenile diaDiabetics 83 1.00 ± 0.78 betics, chemical diabetics and clinical diabetics, although Controls 65 0.70 0.83 ± this division appears arbitrary. Diabetic patients Plaque Index frequently go from a classification of clinical to chemical Diabetics 83 2.08 ± 0.56 diabetes and vice versa. Controls 65 1.87 ± 0.56 Insulinrequirementsdo not constitute sufficient data years ≤30
20,22,24
31
2,7,32
Diabetics Controls
Loss of Attachment 83 2.91 65 2.12
± ±
1.96 1.74
* The differences are statistically significant, P < 0.05.
In the over-30 group not only the diabetic patients but also the control patients showed a statistically significant correlation between the Indices which express the local factors (Plaque Index and Calculus Index) and those which express clinical manifestations of the disease (Gingival Index and Loss of Attachment). DISCUSSION
The results show that in both diabetic and nondiabetic patients, loss of attachment increases with age. It also becomes significantly more severe in the over-30 diabetic group in the presence of approximately similar levels of local factors. Nevertheless, the standard deviations (Table V) suggest that a careful evaluation should be made. In the present study juvenile diabetic patients with different levels of clinical severity, even in acidotic coma, have been observed. Some of them showed normal periodontal tissues whereas others had severe periodontal destruction. These variations might be accounted for either by a difference in the effect on the tissue of the altered carbohydrate metabolism or by plaque composition. Socransky et aL suggested that different microbial constituents of the dental plaque would cause a different degree of periodontal destruction. The Gingival Index was higher in diabetic patients than in the controls. This parameter, together with the increase in loss of attachment in the over-30 diabetic group, shows the presence of more severe clinical manifestations in diabetics than in nondiabetics. However, this must be accepted as an average of the total meas30
for assessing the severity of diabetes since it has been demonstrated that the complications of diabetes are not related to them. The results of this study corroborate the prevalent opinion that diabetes is a predisposing factor which is capable of reducing the resistance of periodontal tissues to microbial activity. 33
SUMMARY
This study was conducted to determine the possible influence of diabetes on the pathogenesis of periodontal disease. A total of 148 patients, 120 females and 28 males, were surveyed. Their ages ranged between 9 and 50 years, with an average age of 30. The experimental group consisted of 83 diabetics and there was a control group of 65 nondiabetics. Both groups were divided into patients under and over the age of 30. The results showed: 1. Loss of attachment was higher in the over-30 diabetic group in the presence of similar local factors. 2. A higher Gingival Index was reported in diabetics of the combined age groups than in the controls (P < 0.05). 3. The Plaque and Calculus Indices did not differ significantly between the diabetic and control subjects. 4. The correlation between the Plaque Index and loss of attachment in diabetics was the most relevant of the correlation analyses. The correlation between the gingival inflammation and loss of attachment indices in the combined diabetic group was also significant. 5. In both groups, diabetics and controls, periodontal destruction increased significantly with age. 6. Juvenile diabetics with severe periodontal disease, as well as others with normal periodontal structures, were found in the course of this study. These findings coincided with the presence or absence of local factors.
448
J. Periodontal. September, 1978
Sznajder, Carraro, Rugna, Sereday ACKNOWLEDGMENT
J., and Cohen, D. W.: Vascular basement lamina thickness in the normal and inflamed gingiva of diabetics and nondiabetics. J Periodontol 45: 676, 1974. 17. Sheridan, R. C , Cheraskin, E., Flynn, F. H., and Hutto, REFERENCES A. C : Epidemiology of diabetes mellitus. II. A study of 100 1. Glickman, L: Clinical Periodontology, p 386. Philadel- dental patients. J Periodontol 30: 298, 1959. phia, W. B. Saunders Co., 1972. 18. Boorujy, S. R., and Ship, I. I.: An epidemiologic and 2. McMullen, J. A., Legg, M , Gottsegen R., and Cameriniclinical study of the prevalence of periodontal disease in diaDavalos, R.: Microangiopathy within the gingival tissues of betics. Abstract. 58,1.A.D.R., 1965. diabetic subjects with special reference to the pre-diabetic state. 19. Finestone, A. J., and Boorujy, S. R.: Diabetes mellitus Periodontics 5: 61, 1967. and periodontal disease. Diabetes 16: 336, 1967. 20. Cohen, D. W., Friedman, L. A., Shapiro, J., Clayton, 3. Glickman, I.: The periodontal structures in experimental K., and Franklin, S.: Diabetes mellitus and periodontal disease. diabetes. NY J Dent 16: 226, 1946. Two year longitudinal observations. Part I. J Periodontol 41: 4. Borghelli, R. F., Devoto, F. C , Foglia, V. G., and 709, 1970. Erausquin, J.: Periodontal changes and dental caries in exper21. Benveniste, R., Bixler, D., and Conneally, P. M.: Perioimental prediabetes. Diabetes 16: 803, 1967. dontal disease in diabetics. J Periodontol 38: 271, 1967. 5. Shklar, G., Cohen, M. M., and Yerganian, G.: Histo22. Campbell, M. J.: Epidemiology of periodontal disease pathologic study of periodontal disease in the Chinese Hamster in the diabetic and the nondiabetic. Aust Dent J17: 274, 1972. with hereditary diabetes. J Periodontol 33: 14, 1962. 23. Carraro, J. J., Sznajder, N., Sereday, M., and Rugna, S. 6. Ray, H. G.: Study of the histopathology of the gingiva in patients with diabetes mellitus. J Periodontol 19: 128, 1948. M.: Diabetes mellitus and periodontal disease. Abstract 28, I.A.D.R., 1972. 7. Ray, H. C , and Orban, B.: Gingival structures in dia24. Glavind, L., Lund, B., and Löe, H.: The relationship betes mellitus. J Periodontol 21: 85, 1950. between periodontal state and diabetes duration, insulin dosage 8. Quintarelli, G.: Histopathology of the human mandiband retinal changes. J Periodontol 39: 341, 1968. ular artery and arterioles in periodontal disease. O. Surg., O. 25. Nelson, W. E.: Tratado de Pediatria, p 50. Barcelona, Med. & O. Path., 10: 1047, 1957. Ed. Salvat, 1959. 9. Stahl, S. S., Witkin, G. J., and Scopp, I. W.: Degenera26. Documenta Geigy: Tablas científicas, ed 6, p 634. Basitive vascular changes observed in selected gingival specimens. lea, Suiza, Barcelona, J. R. Geigy S. A., 1965. Oral Surg 15: 1495, 1962. 27. Ramfjord, S.: Indices of prevalence and incidence of 10. Russell, B. G.: Gingival changes in diabetes mellitus. periodontal disease. J Periodontol 30: 51, 1959. Acta Path Microbiol Scand 68: 161, 1966. 28. Erämkö, O.: Quantitative Methods in Histologic and Mi11. Russell, B. G.: The periodontal membrane in diabetes croscopic Histochemistry, ed 1, p 23. Basel-New York, Karger, mellitus. Acta Pathol Microbiol Scand 70: 318, 1967. 1955. 12. Keene, J. J.: Observations of small blood vessels in 29. Schieffe, H.: The Analysis of Variances, ch 4, sec 4, pp human nondiabetic and diabetic gingiva. J Dent Res 48: 967, 112-119. New York, J. Wiley & Sons, 1957. 1969. 30. Socransky, S. S.: Relationship of bacteria to the etiology 13. Hove, K. A . , and Stallard, R. E.: Diabetes and the of periodontal disease. J Dent Res (suppl) 49: 203, 1970. periodontal patient. J Periodontol 41: 713, 1970. 31. Feinstein, A. R.: Clinical Judgement, p 138. Baltimore, 14. Frantzis, T. G., Reeve, C M., and Brown, A . L. Jr.: The The Williams and Wilkins Co., 1967. ultrastructure of capillary basement membranes in the attached 32. Kjellman, O., Henriksson, C. D., Berghagen, N., and gingiva of diabetic and nondiabetic patients with periodontal Anderson, B.: Oral conditions in 105 subjects with insulindisease. J Periodontol 42: 406, 1971. treated diabetes mellitus. Swed Dent J 63: 99, 1970. 15. Campbell, M. J. A . : A light and electron microscope 33. Bercovici, E., Solomon, L. M., and Beerman, H.: Mistudy of blood vessels from the gingival tissues of nondiabetic croangiopathy in diabetes mellitus and nondiabetic dermatoses. and diabetic patients. Aust Dent J 16: 235, 1971. Am J Med Sci 248: 54, 1964. 16. Listgarten, M. A., Ricker, F. H. Jr., Laster, L., Shapiro, We wish to thank statistician Silvia Hartman for performing the statistical analyses for this paper.
In Memoriam Thomas C. Raymond, Sr. 1899-1978 Life member Thomas C. Raymond, Sr. died on March 12th after a short illness in Des Moines, Iowa. He had limited his practice to periodontics for 33 years and was a strong supporter of the specialty. A graduate of the University of Iowa Dental College (1923), he was selected State University of Iowa Dad of the Year (1960). He actively participated in numerous professional and civic organizations and was elected to responsible offices in many of them. Dr. Raymond is survived by his wife Isabel, a son Dr. Thomas C. Raymond, Jr., and a daughter Mrs. Minov Barnes, three sisters and five grandchildren. Memorials may be made to Des Moines Central Presbyterian Church or to the State University of Iowa Dental College Class of 1923 scholarship fund.
ment. The greatest periodontal destruction has been found among diabetics who have had the disease for over 10 years and those who have had retinal changes. In the present study the prevalence and severity of periodontal disease were investigated in two groups of patients, diabetics and nondiabetics, with an analysis of possible relationships between the local factors (plaque and calculus) and the clinical manifestations of perio dontal disease (gingival inflammation and loss of attach ment) in both groups.
Periodontal Findings in Diabetic and Nondiabetic Patients
24
by N O R M A SZNAJDER*,
MATERIALS AND METHODS
JUAN JOSE CARRARO*
Subjects for the study were 148 patients, 120 females and 28 males, aged between 9 and 50 years with an average age of 30. They were referred from the Endocri nology and Nutrition Department to the Department of Periodontics of Fiorito Hospital in Buenos Aires. The large sex difference in the sample (81% of the patients were females) was presumably due to the fact that women are more likely than men to seek medical atten tion. The experimental group consisted of 83 diabetics and there were 65 nondiabetic controls. All data con cerning age and sex are shown in Table I. Taking into account the mean age of both groups (x 30 years), the patients were divided into those under and over 30 years of age. Most of the younger diabetics had had an early start of the illness.
SUSANA R U G N A *
MARTA SEREDAY† THE PROBABLE influence of diabetes on the onset and development of periodontal disease has been studied for many years. On the basis of experimental and clinical investigations, it is generally accepted that diabetes may result in a greater severity of periodontal disease, espe cially in juvenile diabetics. Periodontal alterations in diabetes mellitus have been studied in laboratory animals to determine the biologic mechanisms which may stimulate destruction of perio dontal tissues, as well as the possible relationship be tween diabetes and local etiologic factors. Diabetes may be experimentally induced by administering alloxan, which can destroy the ß cells of the pancreas, or by performing a partial pancreatectomy. It also may occur spontaneously in certain types of hamsters or mice. These investigations consistently have shown a greater severity of periodontal disease in diabetic animals, which increases gradually with age. However, in none of these studies has it been possible to induce periodontal disease experimentally without local irritational factors. Diabe tes apparently serves as a predisposing factor which can accelerate the periodontal destruction originated by mi crobial agents. Results of histologic studies performed with light and electron microscopy have been variously interpreted, but they suggest a higher preva lence of gingival vascular changes in diabetics than in nondiabetics. These vascular changes are neither specific nor different from those found in control groups, both in experimental animals and in humans. Clinical investigations of the influence of diabetes on the onset and development of periodontal disease have produced results which differ significantly. Some studies indicate a greater prevalence and severity in diabetics than in nondiabetics with similar levels of Plaque and Calculus Indices while others show no differ ences. The clinical parameters that showed impor tant changes are the Gingival Index and loss of attach 1,2
3
Systemic Examination This study consisted of the analysis of tests for blood sugar, glycosuria and glucose tolerance. Diabetic patients were considered to be those who under fasting conditions exhibited two or more blood sugars higher than 1.50 gm% with positive glycosurias or glucose tolerance test scores higher than 2 gm% after one hour, higher than 1.80 gm/100 ml after 2 hours, and a positive family history of diabetes. Patients considered as nondiabetics (control group) had glucose tolerance test scores lower than 1.40 gm/100 ml after 1 hour, lower than 1.20 gm/100 ml after 2 hours and a negative family history of diabetes. The blood sugars and glycosurias were quantitated through the orthotoluidine method. Patients who exhibited intermediate values relative to the above cri teria were eliminated in order to exclude all doubtful cases. Patients weighing more than 20% of their ideal body weight were excluded as well as patients with nephritis, hepatitis, cardiac and collagen diseases and severe endocrinopathy (Cushing's disease, hypophyseal adenoma, etc.), and all chronic diseases liable to alter the carbohydrate metabolism. In selecting the control patients, their family histories were carefully checked for diabetes and obstetrical rec ords were investigated for toxaemia, gestational obesity, fetus weighing more than 4,000 gm at delivery, and perinatal mortality. Patients over 50 were not included in the study since the prevalence and the severity of periodontal disease increase gradually with age, probably as a result of the cumulative effect of tissue destruction.
4
5
6-13
14-16
25,26
17-20
13,21,22
* Departamentos de Odontología, Hospital Pedro Fiorito, Belgrano 851, Avellaneda, Buenos Aires, Argentina. †Departamentos de Endocrinología y Nutricíon, Hospital Pedro Fiorito. 445
446
J. Periodontal. September, 1978
Sznajder, Carraro, Rugna, Sereday TABLE I. Age and Sex Distribution in Diabetic and Control Group Sex
Males
Age
Females
Diabetics Controls
20 8
63 57
Total
28
120
≤30 years
Whole group Range
Range
Mean
9-49 9-50
9-29 9-29
31.0 30.6
>30 years
Mean
Range
Mean
18.5 19.5
30-49 30-50
43.4 41.6
TABLE II. Gingival Index in Diabetic and Control Subjects Over and Under 30 Years of Age
Periodontal Examination The periodontal examination was performed without knowledge of the patient's systemic status. Gingival, Calculus and Plaque Indices were computed in all cases according to the Periodontal Disease Index of Ramfjord while loss of attachment was measured in millimeters from the cementoenamel junction to the bottom of the pocket for the same teeth that are exam ined for the P.D.I. The measurements were made on the buccal, lingual, mesial and distal surfaces of each tooth. Of the four, the one indicating the deepest loss of attach ment was taken as the individual measurement of each tooth. The total loss of attachment was computed by adding the individual losses of attachment and dividing the sum by the number of scored teeth. The mean error in measurement was calculated with Eramko's method and agreement was found in 96%. All data were statistically analyzed. Average values for each Index in the diabetic and control patients and between both age groups were compared by means of a two-way analysis of variance with unequal replications. Correlations between local factors (Plaque and Calculus) and clinical manifestations of periodontal disease (Gin gival Index and loss of attachment) were analyzed.
Age years ≤30
27
>30
Group
No.
Mean
SD
Diabetics Controls
20 26
1.32 1.01
± ±
0.73* 0.60*
Diabetics Controls
63 39
1.69 1.53
± ±
0.66* 0.58*
* The differences are statistically significant, P < 0.05.
TABLE III. Plaque Index in Diabetics and Controls Over and Under 30 Years of Age Age years ≤30
28
>30
Group
No.
Mean
SD
Diabetics Controls
20 26
1.98 1.77
± ±
0.55 0.53
Diabetics Controls
63 39
2.12 1.95
± ±
0.56 0.57
29
RESULTS
TABLE IV. Calculus Index in Diabetics and Controls Over and Under 30 Years of Age Age years ≤30
Gingival Index In patients under 30 the diabetic group showed a higher level of gingival inflammation (1.32 ± 0.7) than the control group (1.01 ± 0.6). Diabetics over 30 also showed a more severe gingival condition (1.60 ± 0.66) than the control patients (1.53 ± 0.58). The differences between the diabetic and control patients were statisti cally significant in both age groups (Table II). Plaque and Calculus Indices The Plaque Index was higher in the under-30 diabetic group (1.98 ± 0.55) than in the control group (1.77 ± 0.56). The same result was found in the over-30 group, with a mean Index score of 2.12 ± 0.56 in the diabetics, and 1.95 ± 0.57 in the control patients. In neither age classification were the differences statistically significant (Tables III and IV). Loss of Attachment The mean loss of attachment in patients under 30 was 1.54 ± 0.58 mm in diabetics and 1.55 ± 0.79 mm in the
>30
SD
Group
No.
Mean
Diabetics Controls
20 26
0.36 0.49
± ±
0.65 0.55
Diabetics Controls
63 39
1.21 1.07
± ±
0.73 0.67
controls. The difference was not statistically significant (P > 0.8). In patients over 30 the mean loss was 3.36 ± 1.67 mm in diabetics and 2.51 ± 1.61 mm in the controls. The difference was statistically significant (P < 0.005) (Table V). The Gingival, Calculus and Plaque Indices and the scores for loss of attachment for all diabetic and control subjects, regardless of age, are shown in Table VI. Correlations In the under-30 diabetic group a significant correlation was found between: (1) Plaque Index and Gingival Index, (2) Calculus Index and Loss of Attachment and (3) Gingival Index and Loss of Attachment. In the control group there were significant correlations only between the Gingival Index and Plaque Index and be tween the Gingival Index and Calculus Index.
Volume 49 Number 9
Diabetic and Nondiabetic Patients 447
TABLE V. LOSS of Attachment in Diabetics and Controls Over and urements and observations. It was not unusual to find Under JO Years ofAge diabetic patients with normal or almost normal gingiva Age
No.
Group
Mean
SD
and supporting structures. These cases coincided rather consistently with reduced levels of plaque and calculus. Comparing the results of various controlled clinical 1.54 ± 20 2.18 Diabetics 26 1.55 ± 1.79 Controls studies on periodontal disease and diabetes is difficult for the following reasons: (a) different Periodontal Indi1.67* 63 3.36 >30 Diabetics ces have been used in many instances and (b) the 39 2.51 ± 1.61* Controls methods of classifying the diabetic subjects have not * The differences are statistically significant, P < 0.005. been uniform. Uniformity in the classification of diaTABLE VI. Gingival, Calculus and Plaque Indices and Loss of Attachbetics is essential if greater consistency is to be achieved ment in the Entire Group of Diabetic and Control Subjects in investigations of the relationship between periodontal Mean SD Group No. disease and diabetes. Uniformity is difficult to attain since the continuing discussion involving the diabetic Gingival Index syndrome makes it difficult to accurately outline a clinDiabetics 83 1.60 ± 0.69* ical taxonomy which permits an analysis of the diabetic Controls 65 0.64* 132 ± influence on periodontal tissues. In some studies diaCalculus Index betics have been classified as prediabetes, juvenile diaDiabetics 83 1.00 ± 0.78 betics, chemical diabetics and clinical diabetics, although Controls 65 0.70 0.83 ± this division appears arbitrary. Diabetic patients Plaque Index frequently go from a classification of clinical to chemical Diabetics 83 2.08 ± 0.56 diabetes and vice versa. Controls 65 1.87 ± 0.56 Insulinrequirementsdo not constitute sufficient data years ≤30
20,22,24
31
2,7,32
Diabetics Controls
Loss of Attachment 83 2.91 65 2.12
± ±
1.96 1.74
* The differences are statistically significant, P < 0.05.
In the over-30 group not only the diabetic patients but also the control patients showed a statistically significant correlation between the Indices which express the local factors (Plaque Index and Calculus Index) and those which express clinical manifestations of the disease (Gingival Index and Loss of Attachment). DISCUSSION
The results show that in both diabetic and nondiabetic patients, loss of attachment increases with age. It also becomes significantly more severe in the over-30 diabetic group in the presence of approximately similar levels of local factors. Nevertheless, the standard deviations (Table V) suggest that a careful evaluation should be made. In the present study juvenile diabetic patients with different levels of clinical severity, even in acidotic coma, have been observed. Some of them showed normal periodontal tissues whereas others had severe periodontal destruction. These variations might be accounted for either by a difference in the effect on the tissue of the altered carbohydrate metabolism or by plaque composition. Socransky et aL suggested that different microbial constituents of the dental plaque would cause a different degree of periodontal destruction. The Gingival Index was higher in diabetic patients than in the controls. This parameter, together with the increase in loss of attachment in the over-30 diabetic group, shows the presence of more severe clinical manifestations in diabetics than in nondiabetics. However, this must be accepted as an average of the total meas30
for assessing the severity of diabetes since it has been demonstrated that the complications of diabetes are not related to them. The results of this study corroborate the prevalent opinion that diabetes is a predisposing factor which is capable of reducing the resistance of periodontal tissues to microbial activity. 33
SUMMARY
This study was conducted to determine the possible influence of diabetes on the pathogenesis of periodontal disease. A total of 148 patients, 120 females and 28 males, were surveyed. Their ages ranged between 9 and 50 years, with an average age of 30. The experimental group consisted of 83 diabetics and there was a control group of 65 nondiabetics. Both groups were divided into patients under and over the age of 30. The results showed: 1. Loss of attachment was higher in the over-30 diabetic group in the presence of similar local factors. 2. A higher Gingival Index was reported in diabetics of the combined age groups than in the controls (P < 0.05). 3. The Plaque and Calculus Indices did not differ significantly between the diabetic and control subjects. 4. The correlation between the Plaque Index and loss of attachment in diabetics was the most relevant of the correlation analyses. The correlation between the gingival inflammation and loss of attachment indices in the combined diabetic group was also significant. 5. In both groups, diabetics and controls, periodontal destruction increased significantly with age. 6. Juvenile diabetics with severe periodontal disease, as well as others with normal periodontal structures, were found in the course of this study. These findings coincided with the presence or absence of local factors.
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J. Periodontal. September, 1978
Sznajder, Carraro, Rugna, Sereday ACKNOWLEDGMENT
J., and Cohen, D. W.: Vascular basement lamina thickness in the normal and inflamed gingiva of diabetics and nondiabetics. J Periodontol 45: 676, 1974. 17. Sheridan, R. C , Cheraskin, E., Flynn, F. H., and Hutto, REFERENCES A. C : Epidemiology of diabetes mellitus. II. A study of 100 1. Glickman, L: Clinical Periodontology, p 386. Philadel- dental patients. J Periodontol 30: 298, 1959. phia, W. B. Saunders Co., 1972. 18. Boorujy, S. R., and Ship, I. I.: An epidemiologic and 2. McMullen, J. A., Legg, M , Gottsegen R., and Cameriniclinical study of the prevalence of periodontal disease in diaDavalos, R.: Microangiopathy within the gingival tissues of betics. Abstract. 58,1.A.D.R., 1965. diabetic subjects with special reference to the pre-diabetic state. 19. Finestone, A. J., and Boorujy, S. R.: Diabetes mellitus Periodontics 5: 61, 1967. and periodontal disease. Diabetes 16: 336, 1967. 20. Cohen, D. W., Friedman, L. A., Shapiro, J., Clayton, 3. Glickman, I.: The periodontal structures in experimental K., and Franklin, S.: Diabetes mellitus and periodontal disease. diabetes. NY J Dent 16: 226, 1946. Two year longitudinal observations. Part I. J Periodontol 41: 4. Borghelli, R. F., Devoto, F. C , Foglia, V. G., and 709, 1970. Erausquin, J.: Periodontal changes and dental caries in exper21. Benveniste, R., Bixler, D., and Conneally, P. M.: Perioimental prediabetes. Diabetes 16: 803, 1967. dontal disease in diabetics. J Periodontol 38: 271, 1967. 5. Shklar, G., Cohen, M. M., and Yerganian, G.: Histo22. Campbell, M. J.: Epidemiology of periodontal disease pathologic study of periodontal disease in the Chinese Hamster in the diabetic and the nondiabetic. Aust Dent J17: 274, 1972. with hereditary diabetes. J Periodontol 33: 14, 1962. 23. Carraro, J. J., Sznajder, N., Sereday, M., and Rugna, S. 6. Ray, H. G.: Study of the histopathology of the gingiva in patients with diabetes mellitus. J Periodontol 19: 128, 1948. M.: Diabetes mellitus and periodontal disease. Abstract 28, I.A.D.R., 1972. 7. Ray, H. C , and Orban, B.: Gingival structures in dia24. Glavind, L., Lund, B., and Löe, H.: The relationship betes mellitus. J Periodontol 21: 85, 1950. between periodontal state and diabetes duration, insulin dosage 8. Quintarelli, G.: Histopathology of the human mandiband retinal changes. J Periodontol 39: 341, 1968. ular artery and arterioles in periodontal disease. O. Surg., O. 25. Nelson, W. E.: Tratado de Pediatria, p 50. Barcelona, Med. & O. Path., 10: 1047, 1957. Ed. Salvat, 1959. 9. Stahl, S. S., Witkin, G. J., and Scopp, I. W.: Degenera26. Documenta Geigy: Tablas científicas, ed 6, p 634. Basitive vascular changes observed in selected gingival specimens. lea, Suiza, Barcelona, J. R. Geigy S. A., 1965. Oral Surg 15: 1495, 1962. 27. Ramfjord, S.: Indices of prevalence and incidence of 10. Russell, B. G.: Gingival changes in diabetes mellitus. periodontal disease. J Periodontol 30: 51, 1959. Acta Path Microbiol Scand 68: 161, 1966. 28. Erämkö, O.: Quantitative Methods in Histologic and Mi11. Russell, B. G.: The periodontal membrane in diabetes croscopic Histochemistry, ed 1, p 23. Basel-New York, Karger, mellitus. Acta Pathol Microbiol Scand 70: 318, 1967. 1955. 12. Keene, J. J.: Observations of small blood vessels in 29. Schieffe, H.: The Analysis of Variances, ch 4, sec 4, pp human nondiabetic and diabetic gingiva. J Dent Res 48: 967, 112-119. New York, J. Wiley & Sons, 1957. 1969. 30. Socransky, S. S.: Relationship of bacteria to the etiology 13. Hove, K. A . , and Stallard, R. E.: Diabetes and the of periodontal disease. J Dent Res (suppl) 49: 203, 1970. periodontal patient. J Periodontol 41: 713, 1970. 31. Feinstein, A. R.: Clinical Judgement, p 138. Baltimore, 14. Frantzis, T. G., Reeve, C M., and Brown, A . L. Jr.: The The Williams and Wilkins Co., 1967. ultrastructure of capillary basement membranes in the attached 32. Kjellman, O., Henriksson, C. D., Berghagen, N., and gingiva of diabetic and nondiabetic patients with periodontal Anderson, B.: Oral conditions in 105 subjects with insulindisease. J Periodontol 42: 406, 1971. treated diabetes mellitus. Swed Dent J 63: 99, 1970. 15. Campbell, M. J. A . : A light and electron microscope 33. Bercovici, E., Solomon, L. M., and Beerman, H.: Mistudy of blood vessels from the gingival tissues of nondiabetic croangiopathy in diabetes mellitus and nondiabetic dermatoses. and diabetic patients. Aust Dent J 16: 235, 1971. Am J Med Sci 248: 54, 1964. 16. Listgarten, M. A., Ricker, F. H. Jr., Laster, L., Shapiro, We wish to thank statistician Silvia Hartman for performing the statistical analyses for this paper.
In Memoriam Thomas C. Raymond, Sr. 1899-1978 Life member Thomas C. Raymond, Sr. died on March 12th after a short illness in Des Moines, Iowa. He had limited his practice to periodontics for 33 years and was a strong supporter of the specialty. A graduate of the University of Iowa Dental College (1923), he was selected State University of Iowa Dad of the Year (1960). He actively participated in numerous professional and civic organizations and was elected to responsible offices in many of them. Dr. Raymond is survived by his wife Isabel, a son Dr. Thomas C. Raymond, Jr., and a daughter Mrs. Minov Barnes, three sisters and five grandchildren. Memorials may be made to Des Moines Central Presbyterian Church or to the State University of Iowa Dental College Class of 1923 scholarship fund.
