Gender Differences in Periodontal Status and Oral Hygiene of Non-Diabetic and Type 2 Diabetic Patients

Study Population and Clinical Measurements

The data of 517 patients of the Outpatient Ambulance of Sports Medicine at the University of Leipzig were analysed. Measurements of dental health and metabolic state are generally part of the baseline examination in the ambulance. All relevant clinical characteristics are given in Table 1. Patients were mostly obese and placed in three major groups, separated by gender: non-diabetic subjects (ND: 114 females: aged 37 to 77 years; 57 males: aged 37 to 75 years), diabetic patients with oral medication (OAD: 108 females: aged 35 to 79 years; 97 males: aged 35 to 78 years), and diabetic patients with insulin regimen (INS: 86 females, aged 36 to 79 years, 55 males, aged 38 to 74 years). The body mass index (BMI) was computed by dividing weight in kilograms by the squared height in meters (mean 30.5 ± 5.1 to 34.6 ± 7.4). The control of diabetes was classified by the percentage of glycated hemoglobin in blood (HbA1c). All subjects had a clinical periodontal examination to measure the gingival index (GI), papillary bleeding index (PBI), visible plaque index (VPI), probing pocket depth (PPD), percentage of bleeding teeth (PBT), periodontal screening and recording (PSR), and number of teeth (Tn). Subjects who participated in this study had a minimum of five (mean 19-20) teeth. (Rationale: The number of 5 teeth is a compromise due to a possible statistical interaction between Tn and PPD. On one hand Tn is a relevant clinical parameter of long lasting periodontitis, which is not age dependent in this study since the age does not markedly vary between the groups. On the other hand fewer teeth increase the variance of pocket depth, which is also an “independent” indicator of periodonitis). Diabetes due to pregnancy or pancreatitis was a further exclusion criterion. The clinical dental examination was done by the same examiner dentist to avoid differences in measurements. The depth of the periodontal pockets was measured by probing the sulcus (pocket) of each tooth using a periodontal probe with a coloured strip (running from 3.5 to 5.5 mm) and a 0.5 mm ball at the tip. The probe was inserted into the crevice until resistance was met. Readings were taken at the mesiofacial, midfacial and distofacial areas as well as the corresponding lingual or palatal areas. The highest reading for each sextant was then recorded. Each sextant was rated according to the PSR scale of criteria: PSR code 0: health, code 1: gingivitis, code 2: calculus and gingivitis, code 3: chronic periodontitis with early or moderate attachment loss, code 4: chronic periodontitis with moderate attachment loss or a form of aggressive periodontitis. A PSR code 3 is determined when the coloured band of the probe remains partially visible (pockets = 4-5 mm). A PSR code 4 implies that the coloured band is not visible (pockets ≥ 5.5 mm). The periodontal status was assessed by means of the PSR scoring system. The GI score (Loe and Silness) describes the clinical severity of gingival inflammation. The GI scale criteria are: GI code 0: no bleeding and inflammation, code 1: slight change in colour and mild edema with slight change in texture, mild inflammation, code 2: redness, hypertrophy, edema and glazing, bleeding on probing, moderate inflammation, code 3: marked redness, hypertrophy, edema, ulceration, spontaneous bleeding, severe inflammation.

Questionnaire

Data were collected using a self-completed oral health questionnaire before the clinical examination. Levels of self-care were estimated using indicators of oral health hygiene including frequencies and amount of time used for tooth brushing, approximal cleaning per day, and regularity of dental checkups. Information on smoking habits, and medication use was also obtained using a self-administered questionnaire.

Statistical Analyses

All data are presented as means ± SD. Analysis of groups across time was done using the Mann-Whitney U test, and independent t-test. A p-value of p < 0.05 was considered to indicate significance, and p < 0.005 as very significant.

Low Performing Index

For a summarizing comparison of the groups, an additional mathematical attempt was made to show relative differences of the periodontal and oral hygiene status between the various groups.

The main parameters periodontitis and oral hygiene status were each defined by 5 sub-parameters in this study. So, complementary to the clinical data analyses and to sum up the results of the clinical statistics each of the 5 sub-parameters is set as 0.2 (20 %), therefore each main parameter is 1.0 (100 %).

Female Groups

Male Groups

Gender Differences

The insulin group had the worst periodontal status; hygiene behaviour was worse in both diabetic groups, relative to non-diabetics.

In summary, male subjects had worse values than women in almost all groups. Only the periodontal status was similar in male or female insulin-dependent subjects.

Oral Hygiene, Periodontitis and Diabetes in Women

The present results demonstrate less success to maintain oral health in diabetic women, independently of the medication (OAD or insulin), though this difference was limited to the visible plaque index and interdental cleaning (Table 3). Whereas a minor number of teeth were the only difference between non diabetics and OAD, indices of periodontitis were markedly increased in women with insulin regimen in relation to non-diabetics and the gingival index was significantly higher than in OAD patients (Table 3). Body weight and age in the groups were similar; HbA1c was higher in the insulin group only (Table 1). So a less accentuated care for oral health apparently is a major factor for more severe periodontitis in diabetes. Worse blood glucose management together with higher HbA1c values may further contribute to reduced immune defence and increased low grade inflammation in the insulin group. Other factors, such as age or body weight were similar between the groups and therefore play apparently no major role for the observed differences. Further a cause-effect relationship of increased body weight and periodontitis has not been proven [21, 22], and more studies with longitudinal prospective design are needed. A recent studies reported that increases in BMI were associated with worsening periodontal status in Japanese students [23], whereas another recent study found no correlation between BMI and severity of periodontal disease in non smokers without diabetes mellitus [24].

An explanation for a possible minor interest in oral hygiene cannot be derived from the present results. Depressive mood which may act as a relevant pathogenetic factor for periodontitis [25-27] may [28] or may not [29] occur in diabetes. In our study women took more frequently antidepressant medicals than men, especially non-diabetic females (17.5 % vs. 3.5 %), and diabetic women with oral therapy (7.4 % vs. 2.1 %). It cannot be determined if the better oral hygiene was influenced by the antidepressant therapy.

Oral Hygiene, Periodontitis and Diabetes in Men

No significant differences were found in men with respect to oral hygiene behaviour. Only a worse PSR and a minor number of teeth were seen in OAD patients, all other parameters or groups showed no relevant differences (Table 3).

These are interesting results since a worse periodontal status in diabetic patients is generally assumed [30]. This yields, at least in part, for the female group in our present study. In men there was only a minor difference between OAD and non-diabetic male subjects, but not in non-diabetic or OAD vs. insulin dependent patients. Since there was a significant difference in body weight and BMI between non diabetic and diabetic males, it again appears that weight differences alone may not account for a higher risk for periodontitis.

From an absolute point of view oral hygiene and periodontal status were bad in all male groups.

Therefore these facts strengthen the results in women indicating that hygiene behaviour may be the major reason for a better or worse periodontal status, independently of a further systemic disease.

General Gender Differences

Data concerning worse oral hygiene behaviour in males were found in the following studies: Alcouffe 1989 [31] reported in a very small group (26 women, 28 men) a better oral hygiene in women. Strauss and Stefanou 2014 [32] reported in 573 adults with diabetes that females practise more often daily interdental cleaning. A better oral hygiene care among dentate adult women [33], and elderly women [34] were found.

In this present study men performed significantly lower in all groups with respect to oral hygiene and periodontal status with the exception of the insulin therapy group. This is in line with other reports about apparent gender effects on periodontitis.

Desvarieux et al. 2004 [35] reported that male subjects between the age of 45 and 75 years and without history of myocardial infarction had nearly 50 % more periodontal disease compared with females. Karikoski et al. 2001 [36] assessed the effects of oral self-care on periodontal health indicators among adults with diabetes. Women reported brushing their teeth more frequently, and differences in plaque were significantly lower than those of men.

Merchant et al. 2002, 2003 [37, 38] did not find an association between oral hygiene practices and periodontitis in a sample of men in the study cohort. In contrast our present results show a strong correlation between plaque and periodontal parameters, and further indicate that diabetes alone does not necessarily induce higher grades of periodontitis.