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Body mass index as a proxy indicator for poor oral hygiene habits in adult diabetic patients


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Introduction

Oral health is an integral part of general health, and oral diseases have a significant impact on the quality of life and lead to higher healthcare costs (1). Oral health and general health are associated (2), as well as oral health-related and health-related quality of life (3). Many diseases show signs or symptoms in the oral cavity. Health problems in the oral cavity can either be the first, only or even the most severe manifestation of a systemic disease, additionally oral health problems can be a leading cause in a deterioration in quality of life (4). Different untreated oral diseases can lead to tooth loss, which affects self-rated general health (2) not to mention the ability to eat, speak and interact with people. Although oral health problems usually do not represent health emergencies, they prolong the state of pain and suffering, and cause-functional, aesthetic, nutritional and psychological problems (5).

Periodontitis, which is one of the most prevalent oral diseases, could be a potential contributing risk factor for a wide array of clinically important systemic diseases, such as cardiovascular diseases, autoimmune disorders, pregnancy complications as well as diabetes mellitus (DM) (6). The main factor for developing periodontitis is formation of bacterial plaque on tooth surfaces. However, some studies also suggest that poor glycaemic control is associated with higher risk for developing periodontitis (7). On the other hand, conventional periodontal treatment (scaling and root planning) results in a statistically significant reduction in glycated haemoglobin levels (8).

The evidence supports a two-way relationship between oral health and DM, namely that DM has adverse effects on periodontal health, while periodontal infections have an adverse effect on glycaemic control (9, 10). The research shows that DM with a persistent hyperglycaemia leads to an exaggerated inflammatory response to the periodontal bacteria in dental plaque. The high vascularity of the inflamed periodontium, on the other hand, serves as an endocrine-like source for TNF-α and other inflammatory mediators, which affect the glucose and lipid metabolism and can act as an insulin antagonist (9).

There is also an association between obesity and periodontitis, as the data indicates that an increased BMI is associated with a higher risk of developing periodontitis and that the underlying biological mechanisms of this association involve adipose tissue-derived cytokines (11). Furthermore, there is some evidence of a triangular association among DM, obesity and periodontitis (12). Diabetics with poorer anthropometric indices (e.g., high BMI values) have poorer values of periodontal indices. But on the other hand, the reduction in BMI seems to be associated with improvements in periodontal status in patients with type 2 DM (13). Good oral health which is achieved with adequate oral self-care (e.g., hygiene, dental check-ups and a healthy lifestyle) is thus important in obese, diabetic patients. Unfortunately, focusing on oral health in diabetics is sometimes considered of lower importance compared to other diabetic complications. General practitioners thus rarely inform their patients with DM about the association of their main disease and periodontal disease (14).

An important part of oral self-care is oral hygiene (e.g., regular tooth brushing), which is imperative for maintaining a proper level of oral health and for its improvement. A recent systematic review with meta-analysis showed that the risk of periodontitis is increased approximately two to five times by poor oral hygiene compared to good oral hygiene (15).

According to the International Diabetes Federation, the prevalence of DM (the age-adjusted comparative prevalence in adults from 20-79 years as a percentage) in Slovenia is about 5.8% (e.g., in Europe it is 7.0%) (16), while according to the Institute for Health Metrics and Evaluation Global Burden of Disease Study the prevalence is even higher, being 8.9% (17). Additionally, as a single disease it is in 7th place in terms of disabilities (18). On the other hand, in the Slovenia poor oral hygiene habits, with tooth brushing only once a day or less, are present in 35.7% of the population, and are more prevalent in men and those with lower education (19). The reported prevalence of inadequate oral hygiene habits is higher compared to some other European countries (20). The relatively high prevalence of DM and a high prevalence of poor tooth-brushing habits means that dentists and general practitioners in Slovenia will meet such patients quite often.

In order to be able to develop evidence-based guidelines for public health activities in terms of promoting oral hygiene in the diabetic population and provide a readily accessible indicator for poor oral hygiene for general practitioners, the aim of our study was to assess if body mass index (BMI) could be used as a fast proxy indicator of poor oral hygiene habits (POHH) among the adult population with diabetes mellitus. Within this framework, the objective of the study was to assess the strength of association between BMI and POHH in Slovenian adults.

Methods
Study design and time frame

We used data from the last series of the nationwide cross-sectional health-related lifestyle studies based on the World Health Organization Countrywide Integrated Non-Communicable Disease Intervention (CINDI) (21) methodology, which was conducted in Slovenia in 2016 by the National Institute of Public Health.

Sampling procedure, data collection process and inclusion criteria

The Statistical Office of Slovenia prepared a representative sample of N=15,639 residents, aged 25-74, using a simple random sampling method. An invitation letter with a printed questionnaire was sent to the participants, who could choose to respond through a postal or online version of the questionnaire. Every participant in the sample could answer only once, which was achieved with unique codes assigned to the participants. To increase the response rate, three reminder letters were sent.

For the purpose of our study, we selected participants with DM based on the question whether or not they had previously been diagnosed with DM by their general practitioner or diabetologist. Those diabetics who had all their teeth missing, based on self-reports, were excluded from the study.

Observed outcome

Oral hygiene habits were assessed with the question “How often do you brush your teeth?”, which was also the only oral hygiene related question. The participants could choose between five available answers (multiple times daily, twice daily, once daily, less than once daily, never). For the purpose of the analysis, we combined the answers into two categories: brushing teeth twice daily or more and brushing teeth once daily or less. Poor oral hygiene habits (POHH) were chosen as the observed outcome and were defined as brushing teeth once daily or less (0-no, 1-yes).

Risk factors for POHH

BMI, as a main factor, was calculated from self-reported data about body weight (in kg) and body height (in m). For the purpose of the analysis the participants were categorized into four groups. Depending on the value of their BMI, they were classified into the underweight (<18.5), normal (18.5-24.9), overweight (25.0-29.9) or obese group (≥30.0).

Other factors included in our analysis were sociodemographic: gender, age, educational level and type of work. Age of the participants was calculated from the reported year of birth and was aggregated into five 10-year categories (25-34, 35-44, 45-54, 55-64, 65-74). Regarding the educational level, participants could choose one of seven categories (incomplete primary, primary, vocational, secondary, college, university and postgraduate level of education). For the purpose of analysis, the data were aggregated in four categories (primary or less, vocational, secondary, college and higher). The category primary or less combined the incomplete primary and primary levels of education, and the category college and higher combined the college, university and postgraduate levels of education. The question about employment status had seven categories (employed, self-employed, student, housekeeper, pensioner, unemployed and other). For the purpose of analysis, the data were combined into four categories (employed, self-employed, retired/housekeeper and unemployed). Those who chose the category “other” were excluded. The category “employed” consisted of those who were employed and those who were students, and the category “retired/housekeeper” consisted of those who were housekeepers and pensioners. In order to get the clearest possible estimate of the strength of the relationship between BMI and POHH, all listed factors were considered as confounding factors in the analysis.

Methods of analysis

The association among POHH, BMI and other confounding factors, was assessed univariately using the chi-square test. Additionally, the odds ratio for POHH between groups with different BMI values was calculated. The reference group consisted of participants with normal BMI.

The association among POHH, BMI as the main factor and the confounding factors was assessed also multivariately by using binary multiple logistic regression. For this purpose, a direct method was used. Dummy variables were created for BMI and all confounding variables with the simple method. In all statistical tests, p≤0.05 was considered significant. The IBM SPSS for Windows Version 21.0 (SPSS Inc., Chicago, IL., USA) software was used.

Results
Sample description

A total of 8,590 invitees responded to the invitation to participate in the survey (response rate: 54.9%). Among them, there were 560 participants with self-reported DM (6.6%).

After the exclusion of all edentulous participants, we got the final sample, which included 466 dentate diabetic subjects, 255 (54.7%) men and 211 (45.3%) women. The majority of them were 55 years or older (67.6%). None of the participants had a BMI value <18.5, while 40.5% of them had a BMI value ≥30.

Results of the univariate analysis

The POHH prevalence in the total sample was 50.9%. When taking into account the BMI of the participants, POHH prevalence was the lowest in the group with a BMI value ˂25.0 (37.8%). In the overweight group POHH prevalence was 1.22 times higher, while in the obese group it was 1.63 times higher compared to the group with normal BMI values (Table 1). The odds for POHH were also much higher in the obese group than in the group of participants with a BMI value ˂25.0 (OR=2.64). Additional results showed that POHH prevalence was also much higher in males, and in those with the lowest education. Detailed results are presented in Table 1.

Estimates of the prevalence of poor oral hygiene habits (POHH) considering selected risk factors in a diabetic population and the results of the univariate analysis (chi-square) of the association between POHH and the risk factors: using data from a cross-sectional study, conducted in Slovenia in 2016.

Risk factor Category Ntot N POHH Ncat NPOHH/Ncat (%) p
BMI <18.5 456 0 0 0.0 <0.001
18.5-24.99 31 82 37.8
25-29.99 87 189 46.0
≥30 114 185 61.6
Gender Men 462 156 253 61.7 <0.001
Women 79 209 37.8
Age (years) 25-34 462 9 18 50.0 0.661
35-44 15 38 39.5
45-54 48 92 52.2
55-64 83 164 50.6
65-74 80 150 53.3
Education level Primary or less 459 60 96 62.5 0.033
Vocational 57 118 48.3
Secondary 75 147 51.0
College or higher 41 98 41.8
Employment status Employed, student 445 66 146 45.2 0.187
Self-employed 8 15 53.3
Retired/housekeeper 143 258 55.4
Unemployed 11 26 42.3

Legend: Ntot=total number of respondents, NPOHH=number of participants with poor oral hygiene, Ncat=number of respondents within the category

Results of the multivariate analysis

After adjusting the relationship between POHH and BMI for confounding factors, the odds for POHH in the obese participants decreased only slightly in comparison to the group with a BMI value ˂25.0 (Table 2). Additional results showed that in the multivariate model, gender (category males) and education level (category primary or less) remained statistically significant factors, while employment status (category retired/housekeeper) became a statistically significant factor only in the multivariate model (Table 2). The value of the model’s Nagelkerke’s R Square statistic was 0.149, while the value of the Hosmer-Lemeshow goodness of fit test was 15.244 (p=0.055).

The results of the multivariate analysis of the association between poor oral hygiene habits and selected risk factors: using data from a cross-sectional study, conducted in Slovenia in 2016 (N=437).

Risk factor Category OR 95% CI for OR limits
p
Lower Upper
BMI <25 1
25.0-29.9 1.316 0.725 2.389 0.367
≥30.0 2.454 1.355 4.445 0.003
Gender Female 1
Male 2.836 1.843 4.365 <0.001
Age (years) 65-74 1
25-34 3.238 0.936 11.197 0.063
35-44 1.233 0.463 3.282 0.675
45-54 1.719 0.778 3.801 0.181
55-64 1.108 0.651 1.887 0.705
Education level Vocational 1
Primary or less 1.989 1.076 3.677 0.028
Secondary school 1.158 0.686 1.954 0.583
College or higher 1.046 0.574 1.905 0.884
Employment status Employed, student 1
Self-employed 1.034 0.325 3.290 0.955
Retired/housekeeper 2.152 1.126 4.111 0.020
Unemployed 1.022 0.400 2.611 0.964

Legend: OR=odds ratio, CI=confidence interval

Discussion

The results of our study suggest that BMI can serve as a useful indicator in a simple and rapid assessment of diabetic patient risk for POHH, and consequently for the existence of potential oral diseases that may impair the stability of DM.

The results of our study related to the prevalence of POHH in a diabetic population are consistent with the results of other, similar studies. The systematic review of oral health attitudes, knowledge and practices presented in Poudel et al. revealed that slightly more than half of the participants with DM brushed their teeth only once daily or less (49.3% brushed their teeth twice a day, 95% CI 35.70–62.90) (22). However, there exist studies reporting higher as well as lower rates of POHH among DM patients. In a Finnish study, for example, poor oral hygiene was present in 62% (23) of the sample, while a study by Commisso et al. performed on a diabetic population in central Italy revealed that the prevalence of POHH was 28.8% (7). Similarly in the study of Bowyer et. al. performed in the United Kingdom the prevalence was 32.8% (24). Thus, the prevalence of POHH among diabetics in Slovenia is not among the highest in the literature, but this does not mean that it does not pose a problem, as it is much higher than in the general population, where it is around 36% (19). This makes oral hygiene in the Slovenian diabetic population an important public health problem, which is even greater when we consider the results of past studies which suggested that the majority of diabetics had inadequate oral health knowledge and low awareness of the association between DM and the risks for oral health complications (22, 24).

The high strength of association between POHH and obesity was unsurprising, due to the fact that regular tooth brushing is also one of the elements of a healthy lifestyle. The literature suggests that obese persons in general are less likely to brush their teeth at least twice daily, and are also more likely to have higher Decayed, Missing, Filled Teeth (DMFT) scores (25, 26), which are a direct consequence of plaque-related oral diseases.

Additional results of our study confirmed some socioeconomic risk factors for POHH i.e., gender and education. This is in line with previous research in Slovenia (19, 27), as well as in other countries. Raskiliene et al., for example showed that male gender, a lower education and living in rural environments were associated with poorer self-reported tooth brushing frequency. Additionally, poor tooth brushing frequency was associated with an unhealthy lifestyle (smoking, along with high alcohol, low vegetable and high confectionery consumption) (25). Moreover, obese diabetic patients with socio-economic risk factors are at greater risk of oral health complications which are associated with general health problems and the health-related quality of life (2, 3).

Our study has some potential limitations. First, our data were collected in a self-reported survey, and thus the actual data could be different. However, even such rough information provides a sufficient foundation for interventions at the population level. We assume that due to the self-reporting nature of our study, the results are biased towards positive answers, and consequently our conclusion about the prevalence of POHH habits in the DM population could be treated as solid. Second, only one question regarding oral hygiene habits was used in the POHH assessment. We are aware of this limitation, but we used data that are routinely collected in Slovenia in the frame of a national survey. As a result, we were able to use the data that was available. Since the survey is not only intended to study oral health, data related to oral health are limited. However, we believe that the information provided by one question is sufficient for the initial analysis. Third, one might dispute that we did not define tooth-brushing habits appropriately, as some dental experts claim that brushing once daily could be enough to maintain oral health. However, it is widely accepted that proper oral health care includes tooth brushing twice daily (28). Next, our sample was reduced as we excluded edentulous subjects, because we could not use the question on tooth brushing with this group of participants. However, the sample size was still big enough to perform the planned analysis. Next, one might think that our study highlights only a few of the biological and socio-demographic factors that influence tooth-brushing habits in the diabetic population. However, we believe that these are the most important and reasonable factors to be included in the identification of diabetics with POHH habits. Next, the p-value of the Hosmer-Lemeshow goodness-of-fit test showed a marginally good fit of the model to the data. However, the value was still within the recommended limits. Finally, one might perceive that there are many studies already published on similar topics. However, this is only true to a certain extent. Studies that were available in accessible databases, and were similar to the current work, focused on topics such as: adiposity and glycaemic control in patients with periodontal disease; on the diagnosis, treatment and prevention of oral disorders in patients with diabetes; and on the prevalence of oral health problems among diabetic patients (11, 12, 29). However, none of these earlier studies had the same focus as ours, as none of them studied the association between BMI and periodontal health in diabetics in the sense of using BMI as fast proxy indicator for risk assessment in practice. Consequently, our study presents a unique way of using BMI in clinical practice and in oral public health. On the other side, despite the potential limitations of this study one advantage is that it shows that BMI can serve as a rough, simple, cheap and always available tool to estimate which patients with DM should be referred to a preventive examination of the oral cavity. An additional advantage is that the observed relationship was controlled for with regard to selected socio-economic factors related to oral hygiene, which contributed to gaining a clearer idea of observed relationship.

This study has some important implications. Tooth brushing is the cornerstone of maintaining and improving oral health, and in the scope of the bidirectional relationship between oral and general health it is even more important in a diabetic population (8, 10). Appropriate information and advice should thus be given to the diabetic population about oral health and oral hygiene practices. As such, for public health professionals our study provides the basic information needed for developing educational workshops, and making adjustments for oral health promotion materials. The facts confirmed in our study could be used to tailor and prepare health promotion material for the diabetic population. Moreover, our study also has important implications for primary care physicians and diabetologists. Oral health should not be treated as less important in an obese diabetic population, since the abilities to bite and chew are important for a healthy diet. People with poorer periodontal status and those who are edentulous have poorer masticatory performance, and it is known that higher masticatory performance prevents the occurrence of diabetes (30). For primary care physicians, BMI could be used as an indicator for referring diabetic patients to their dentists. According to our results it is a readily assessable and good proxy for assessing high-risk groups of diabetic patients regarding their oral health. It could also have an influence on the financial burden of oral diseases, on general health and consequently on the quality of life. The referral of a diabetic patient to a dentist could also improve dental self-efficacy. As dental self-efficacy (related to brushing teeth and visiting dentists) and self-efficacy in diabetes management (nutritional habits, physical exercise and insulin management) are correlated, improving one could also improve the other (31). Improved self-efficacy could lead to a better oral and general health, and thus a better quality of life. Finally, our study could have implications for dental professionals, as the process also goes in the opposite direction – dentists should consider overweight/obese individuals with poor oral hygiene as at-risk-for-DM. They should therefore ask those patients about their medical history regarding DM and direct them to their general practitioner. The proper oral hygiene of DM patients and proper management of the diabetic population in dental offices is also important, keeping in mind the bidirectional association of oral health and DM. There is also some evidence of reducing glycosylated haemoglobin in diabetic patients by periodontal therapy (scaling and root planning) in the short term, but sadly no evidence of maintaining these results for a longer period (32). Nevertheless, based on the bidirectional relationship between DM and oral health, some experts suggest that an oral health evaluation and possible onward referral should be incorporated into the recommendations for routine diabetes care (33).

In the future, it would be interesting to identify the high-risk-for POHH profiles, which would be targeted with focused and consequently more individualised preventive activities. A similar approach has already been suggested to deal with other public health problems (34, 35). However, this extension of the analysis was out of scope of the current study. Next, for more detailed research about the factors influencing POHH, and to explore the attitudes toward oral health in a diabetic population, further research based on a bigger sample with specific oral health questions would be appropriate.

Conclusion

Our study confirmed that BMI could be used as a fast and simple proxy indicator to identify a high-risk group of diabetic patients regarding their poor oral health habits. These results are important, due to the fact that there is a low awareness of the oral-systemic health link among diabetics and some practitioners, and they could be used for more appropriate intervention planning.

Oral health has a bidirectional association with multiple conditions, including DM. Poor oral hygiene leads to worsening of oral health, and consequently to worsening of a person’s quality of life, and has also an impact on diabetes control. Professionals treating patients with DM should thus consider the association between DM and oral health, especially in obese diabetic individuals, and refer them to their dentists. On the other hand, dentists should consider the possibility of having undiscovered DM in obese patients with poor oral hygiene. Keeping in mind the association of BMI and POHH could improve the oral and general health of DM patients, which could have a positive impact on their quality of life and their diabetes management.

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