Periodontal diseases and caries experience of 
diabetic patients in an Arabian community

A group of diabetic patients living in an Arabian community were matched by sex and age with a non-diabetic control group. Examination for periodontal status and dental caries was carried out on the
matched pairs. Diabetics exhibited more gingival inflammation and increased probing depths when com­ pared with age-/sex-matched controls. The caries experience of diabetic patients was higher than that of normal groups. The findings of this study highlight the urgent need to develop a preventive dental program for diabetic patients so as to minimize their experience of dental disease.

  Due to the heterogenous etiology of diabetes mel-litus, it is difficult to produce art all-embracing single definition. The disease is generally recognized by a particular degree of hyperglycemia. However, diabetes mellitus is now defined as a disease charac­ terized by chronic hyperglycemia associated with disturbances of carbohydrate, lipid, and protein metabolism that leads to the development of spe­ cific microvascular complications, particularly in the eye, kidney, peripheral vessels, heart, and mouth. It is important for clinicians to recognize the oral manifestations associated with metabolic dis­ turbance. The association between diabetes mel­ litus and pathologic changes in the oral cavity, especially affecting the periodontium, has been the subject of many reports in the dental literature. While several studies on adults have demonstrated more severe periodontal disease in diabetics than in non-diabetics,1-7 Barnett et al,8 nevertheless, failed to find any correlation between diabetes and periodontal disease.
The association between diabetes and dental caries has received lesser attention than periodon­ tal disease. However, the findings have also been controversial.9-14 The relationship between diab­ etes mellitus and dental disease has, thus, been studied extensively with conflicting results.
It is also known, and worth mentioning here, that the prevalence and clinical features of diabetes mellitus vary from one ethnic group to another.15 The conflict of the results referred to might, there­ fore, be more apparent than real, the variability being related to both genetic and environmental factors such as over nutrition. According to this hypothesis, the authors felt it important to investi­ gate the relationship between diabetes mellitus and dental diseases in an Arabian community, that is, in a relatively stable ethnic group.
The aim of this study, therefore, was to compare the experience of periodontal disease and caries in age- and sex-matched adult diabetics and non-diabetics in an Arabian community.

  Two groups of 161 diabetic and 100 control sub­ jects were examined in the diabetic clinic of the Department of Medicine at King Abdulaziz Univer­ sity Hospital (KAUH), Jeddah. The hospital is located in the eastern part of Jeddah and is the main University hospital in the western region of the Kingdom of Saudi Arabia. It has a catchment popu­ lation of approximately 250,000 and acts as a refer­ ral center. Most of the diabetic patients included in this study were obtained mainly from the KAUH. However, because of the difficulty in obtaining all samples needed in this study, patients from Al Shataah and King Fahd Hospitals were requested to participate. Both hospitals are recognized as teach­ ing hospitals in Jeddah. The control group was age- and sex-matched with healthy individuals. The controlled subjects were selected randomly from the general population by choosing every second visitor who entered the general of the King Abdulaziz University Hospital. None of those selected were attending for any medical or dental treatment, or otherwise. All control subjects were subjected to a thorough historical and physical examination. The general recommendation on the standardization of blood tests for diabetes was adopted. The assessment of the diabetic patients was based on mean blood glucose (MBG), glycosylated haemoglobin (HbAIC) and diabetic complications of neuropathy and retinopathy.
Following personal data collection and record­ ing of age, sex, height and weight, each subject was submitted to a medical examination for deter­ mination of the level of metabolic control and diag­ nosis. Each subject was then sent to the dental clinics of KAUH for dental examination. Table 1 shows the distribution of the normal and diabetic subjects according to age, sex, height, and weight.
Table  1.    Distribution of the control and diabetic subjects according to age, sex, height and weight.
                    Mean            SEX               Mean         Mean

                      age        Male Female       height        weight
                     (yrs)                                   (cm)          (kg)
Normal          43.2          58        42           161.6        69.4
   subjects                                                             
Diabetic        47.9          76        85           161.7        73.5

   patien                                      
The periodontal status was assessed by means of the CPITN system.16 CPITN recordings were made for sextants containing at least two functional teeth, using the following code numbers:
Code O  =  healthy periodontal tissue (H)
Code 1  =  bleeding after probing (B)
Code 2  =  supra or subgingival calculus and/or overhanging(s) of filling(s) or crown(s) (C)
Code 3  =  pathologic pocket(s) 4 or 5 mm (P1)
Code 4  =  pathologic pocket(s) 6 or > 6 mm
(P2)
X             =  excluded sextant (X)
Besides the CPITN scores, the number of teeth with caries (D), the number of missing teeth (M), and the number of fillings (F) were separately recorded for each subject.
Following the dental examination, plaque was scraped from the subgingival area by means of a curette. Plaque samples were collected from 50 control subjects and 50 diabetic patients. The col­ lected samples of plaque were placed in special test tubes for isolating and counting anaerobic lac-tobacilli.
All dental examinations were carried out by two examiners. Duplicate examinations conducted prior to and during the course of the clinical work revealed inter- and intra-examiner reliability of over 90% for the two examiners (Table 2).
The collected data was transferred to floppy disks and analyzed at the computer unit of King Fahd Center for Medical Research, King Abdulaziz University. Student's T-test was used to test differ­ ences between means of dental parameters. Analysis of variance was used for statistical analysis of the biochemical parameters.

Table 3 shows the results of blood analysis of diabetic and non-diabetic subjects. Blood glucose and HbAIc values were markedly higher in diabetic patients as compared to non-diabetic controls (P < 0.05).
Table 2. Intra- and inter-examiner reliability in recording dental examination.

                          Examiner                         N         % of the
                                                                       same reading

Examiner No. (1) and Examiner No. (1)          20             93
Examiner No. (2) and Examiner No. (2)          20             97
Examiner No. (1) and Examiner No. (2)          20             91
N  =   number of subjects examined                             
Table 3. Blood glucose and glycosylated hemoglobin con-
centrations in diabetic and non-diabetic subjects studied.

Subject                                                 Glucose       HbAIC
                                                          (m mol/L)       (%)

Non-diabetic:                                                                                              Mean        3.57          5.77
     Minimum                                            2.30          3.50
     Maximum                                           7.40         10.30
     SD                                                     1.57          1.53
Diabetic:                                                                                                    Mean        8.71          7.48
     Minimum                                            2.10          3.38
     Maximum                                           24.10        14.40
     SD                                                     4.52          2.62
For Blood Glucose:                                                                                     F ratio  =   16.631, DF = 156, P<0.05           
For HbAIC:                                                                                                  F ratio  =   5.567, DF = 135, P<0.05             
The results of CPITN index are presented in Table 4. Healthy gingiva (H) was found in an aver­ age of 1.01 sextants in the diabetics and in 3.10 sextants in the control subjects, a difference which was statistically significant at P < 0.01.
Gingival bleeding after gentle probing (B) was found in an average of 0.29 sextants in the diabetics and in 0.43 sextants in the control subjects, a differ­ ence which was not statistically significant (P < 0.01).
Supra or subgingival calculus (C) was found in an average of 1.32 sextants in the diabetics and in 1.70 sextants in the control subjects, a difference which was not statistically significant (P< 0.01).
Pathologic pockets of 4.5 mm deep (P1) were found in an average of 2.45 sextants in the diabetics and in 0.63 sextants in the control subjects, a differ­ ence which was statistically significant at P < 0.01.
Pathologic pockets (P2) of 6 mm deep were found in an average of 0.91 sextants in the diabetic and in 0.14 sextants in the control group subjects, a differ­ ence which was statistically significant at P < 0.01.
In this study the caries prevalence among diabe­ tics (DMF = 12.76) was higher than among the controls (DMF = 10.75), and this difference was statistically significant at P <0.05 (Table 5).
Table 6 shows the results of microbiological analysis of diabetic and non-diabetic subjects. The number of positive results of anaerobic lactobacilli was higher in diabetic patients compared to non-diabetic controls. However, the difference was not statistically significant (P > 0.05).
Table 5. DMF of non-diabetic and diabetic groups.

                                                                   Caries       

                           D           M             F           Free      DMF

Non-diabetic      2.43         4.49         3.83        21.23     10.75
Diabetic             3.62        7.56         1.50        19.17     12.76
For DMFT  :  t-value = -2.51, DF =  257.66, p < 0.05
Table 6.    Anaerobic lactobacilli in control subjects and diabe­
tic patients.
                                                             Anaerobic lactobacill

                                              N                No.+ve         %

Control subjects                       50                    5             10
Diabetic patients                      50                    7             14
N   =  number of subjects, x2  = 0.3787, DF  =  Ip  >0.05

  Evidence, which indicates that patients par­ ticipating in the present study were generally diabe­ tics, was shown by comparing the results of blood analyses noted in the present group with those reported by other investigators. In effect, the values for blood glucose and HbAIc in the Arabic diabetic groups were similar to those reported elsewhere for diabetic patients.17,18
Clinical and epidemiological studies have been carried out in many parts of the world to investigate the association between diabetes and dental caries. Most studies were cross- sectional and showed either higher9, similar,10,12 or lower13,14 caries experience among diabetics than among the controls. In the present study, the caries experi­ ence of diabetics was higher than that of non-diabetics. This is surprising in view of the fact that the lower intake of refined carbohydrates, espe­ cially sucrose, and high protein content of the diet make the dietary habits of diabetic subjects clearly less cariogenic than among non-diabetics. This finding, therefore, raises the question as to why adult diabetics develop as many new carious lesions as their healthy counterparts in spite of the favorable diet. It has been reported that streptococ­ cus mutans is of major etiological significance in human dental caries. The capacity of this microor­ ganism to initiate dental caries depends on its abil­ ity to produce adhesive extracellular polysacharides19 and to release organic acids which demineralize tooth substance. The organic acids involved are end products of the metabolism of fermentable substrates, especially sucrose, by the bacteria. The more frequent the intake of suc­ rose, with the consequent production of acid, the more disastrous is the effect upon tooth substance. To avoid hypoglycemic shock, however, the diabetic may have to resort on occasions to the fre­ quent use of sucrose, thus, creating an oral envi­ ronment which facilitates the demineralization of tooth substance commonly referred to as dental caries. In other words, diabetic patients may have more frequent meals than normal subjects and repeated intakes of even small amounts of car­ bohydrates may be cariogenic.
In addition, lactobacilli are aciduric and acidogenic bacteria which are present in large numbers in the mouth of a caries-active person.20 The growth of lactobacilli is also favored by the fre­ quent intake of fermentable carbohydrates, 21 and salivary lactobacilli counts are useful in predicting future caries activity.20 Since these bacteria were found to be as numerous in diabetics as in non-diabetics (Table 6), it seems that, in spite of sucrose restriction, generally in the diet, the oral condition of diabetic patients is otherwise favorable for the growth of cariogenic bacteria.
Another reason for the higher caries experience in diabetic patients may be because of the high glu­ cose level in the saliva and in the crevicular fluid promoting acid production in the dental plaque.
In previous studies, the periodontal status of patients with diabetes mellitus was assessed by using clinical indices for plaque, gingivitis, periodontal pockets with loss of epithelial attach­ ment, or were based on epidemiological indices such as Russel's Index.22 Recently, however, the "Community Periodontal Index of Treatment Needs" (CPITN) has been widely used in epidemiological studies as a method for assessing periodontal treatment needs. Although the CPITN does not record the periodontal changes separately for all teeth, the system has been found to produce reliable information on the periodontal status and treatment needs in population groups.
The results obtained by the use of the CPITN index in this study showed that the average number of sextants displaying pathologic pockets (shallow and deep) are higher in the diabetic than in the con­ trol group. The mean number of missing sextants was also higher in the diabetic than in the control group, 2.1 and 1.3 respectively. The difference was statistically significant at P < 0.05. In addition to the mean number of missing sextants, the mean number of missing teeth was also calculated. The mean number of missing teeth was found to be higher in the diabetics than in the control group (7.59 and 4.49 respectively).
The literature on diabetes mellitus is abound with conflicting results of studies designed to investigate the association between it and dental disease in dif­ ferent communities. This apparent conflict might, however, be more readily acceptable if it was also accepted that the condition of diabetes mellitus itself might be due to genetic and environmental factors which vary from one community to another. The findings of the present study confirm that in an Arabian community, the experience of both periodontal disease and caries is greater in diabetic patients, and that periodontal disease occurs in more severe forms in this group than in non-diabetics.The results of this study highlight, in particular, the absolute necessity for adopting preventive den­ tal health care programs so as to minimize the pre­ valence of periodontal disease and, in addition, to prevent the dental decay so abundantly seen in diabetic patients. By so doing, many of the sys­ temic complications and infections seen in diabetic patients might also be controlled.

  The Research Group acknowledge, with thanks, the invaluable assistance of Scientific Research Council of King Abdulaziz University (SRCKAU), which granted us financial support during this Research Project (No. 408/ 036). Our sincere thanks are also due to Professor H.A. Zaki, DDS, MPH, MSD, who acted as external consul­ tant for this research project.