ORIGINALCinar ARTICLE et al
Toothbrushing: A Link Between Noncommunicable and Communicable Diseases? Ayse Basak Cinara/Inci Oktayb/Lone Schouc Purpose: To assess the correlation between toothbrushing (TB) and the common biological (HDL) and quality-of-life–related risk factors for noncommunicable diseases (NCDs) and communicable diseases among patients with diabetes mellitus type 2 (DM2). Materials and Methods: The present study is part of a prospective intervention study among DM2 patients (n = 200), randomly selected from the outpatient clinics, Istanbul, Turkey. The assessed variables were: TB, self-reported gingival bleeding (SRGB), HDL, BMI, body-fat proportion, modified quality of life scale (WHOQOL-BrefPhPs). Descriptive statistics, frequency distributions, Spearman rank correlation, the chi-square test and factor analysis were applied. Results: A minority of the patients brushed their teeth twice a day or more (27%) and reported no gingival bleeding (37%). Favourable HDL and high WHOQOL-BrefPhPs were 77% and 57%, respectively. A majority of patients had unhealthy BMI (83%) and body-fat proportions (63%). SRGB was negatively correlated with WHOQOL-BrefPhPs (rs = -0.24, p < 0.05) and TB (rs = -0.25, p < 0.01). The patients who reported less than daily TB were more likely to have unfavourable HDL and low WHOQOL-BrefPhPs (32% vs 54%) than those brushing their teeth daily (17% vs 35%, p < 0.05). Principal component analysis revealed two clusters: ‘healthy weight’ (WHOQOL-BrefPhPs, TB, BMI) and ‘oral health’ (SRGB, HDL). Conclusion: The present results demonstrate a correlation between TB and biological and quality-of-life–related risk markers of NCDs and communicable diseases. There seems to be a need to increase the awareness of the significance TB’s potential intermediatory role between NCDs and communicable diseases. Key words: diabetes type II, health coaching, toothbrushing, toothbrushing self-efficacy, quality of life Oral Health Prev Dent 2015;13:515-522 doi: 10.3290/j.ohpd.a34054
N
oncommunicable diseases (NCDs; e.g. cardiovascular diseases, type II diabetes, obesity) are defined by the WHO as ‘slowly progressing, long duration largely preventable illnesses caused due to numerous common modifiable risk factors resulta
Assistant Professor, Oral Public Health Department, Section of Periodontology, Institute of Odontology, University of Copenhagen, Denmark. Idea, hypothesis, experimental design, wrote the manuscript, consulted on statistical evaluation, contributed substantially to discussion.
b
Professor and Head, Oral Public Health Department, Yeditepe Dental Faculty, University of Yeditepe, Istanbul, Turkey. Performed the experiments in fulfilment of requirements for a degree, proofread the manuscript.
c
Professor and Head, Global Oral Health Promotion Section, Institute of Odontology, University of Copenhagen, Denmark. Contributed substantially to writing the manuscript and discussion, consulted on statistical evaluation, language revision, proofread the manuscript.
Correspondence: Ayse Basak Cinar, Department of Odontology, University of Copenhagen, Norre Alle 20, DK-2200 Copenhagen. Tel: +45-27-557-6552. Email: [email protected]
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Submitted for publication: 20.11.13; accepted for publication: 24.02.14
ing from poor lifestyle choices’. By 2020, the contribution of NCDs is expected to rise to 73% of all deaths and 60% of the global burden of disease.46 Communicable diseases (infectious diseases) are caused by pathogenic microorganisms, such as bacteria, viruses, parasites or fungi; the diseases can be spread, directly or indirectly, from one person to another.47 Common public health promotion and campaigns are necessary to prevent NCDs and communicable diseases as proposed by the WHO strategic objectives for 2020.48 Periodontal disease is one of the major oral diseases contributing to the global burden of NCDs;7,43 the disease is highly prevalent worldwide and therefore represents a major global public health problem. Periodontal disease may be caused by local factors, such as dental biofilm, or it may reflect an inadequate immune response. It can also be a manifestation of certain communicable diseases, for example, in people with general infection or
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among people infected with HIV.25 Gingival bleeding is one of the chief signs of the disease.21 The most important method of preventing the initiation/progression of periodontal diseases is daily toothbrushing,26 which can act as a common preventive strategy for both NCDs and communicable diseases. This has been a neglected issue. The current literature supports the concept that NCDs and communicable diseases share synergistic biological and psychological (behavioural) risk factors.9,27,39,41,49 Low blood levels of high density lipoprotein (HDL), a synergistic biological risk factor,3,19,40 is an integral component of innate immunity, mediating diverse functions that defend against viral, bacterial and parasitic infections.19 The evidence shows that low HDL cholesterol concentration may be associated with periodontitis.34,35 Periodontitis is also associated with obesity, which is another synergistic biological risk factor for NCDs46,48 and communicable diseases.22 The impact of toothbrushing on the synergistic biological markers of NCDs and communicable diseases is not known. A WHO quality of life measure, WHOQOL-Bref, provides a valid, reliable, synergistic, self-assessed physical and psychological health measure of the health-related quality-of-life status of persons with NCDs44 and communicable diseases.15,36,50 Although it is well known that oral diseases affect the quality of life,14,30,31 the impact of preventive oral behaviours, in particular toothbrushing, has been poorly explored.18 The aim of the present study was to assess the correlation between a preventive oral health behaviour (toothbrushing) and the common biological (HDL) and self-assessed quality-of-life–related risk factors (modified WHOQOL-Bref) for NCDs and communicable diseases among patients with diabetes mellitus type 2 (DM2).
MATERIALS AND METHODS The present study is part of a prospective intervention study which consists of 3 stages (baseline-initiation, maintenance and follow-up) among DM2 patients (n = 197), randomly selected from the outpatient clinics of two hospitals in Istanbul, Turkey. The power and sample size was calculated by G*power (effect size w = 0.3, α error probability = 0.05, power [1- β error probability] = 0.95).4 Patients were included if they were between 30 and 65 years old, had at least 4 functional teeth and
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had not undergone psychological treatment or hospitalisation. The data in the present study originate from the baseline measurements of the prospective study that were collected at the start and finish of each of the 3 stages by clinical measurements (BMI, body-fat proportion, HDL, LDL, HbA1c) and self-assessed questionnaires (including modified scales, e.g. PAID, WHOQOL-Bref). Ethical approval and written permission were granted by the Ministry of Health to conduct the study. The research was announced at the outpatient clinics by pamphlets, brochures, physicians and the head nurses. At baseline, the patients interested in participating in the study were selected according the eligibility criteria. Verbal and written information about the study was provided and then informed consent was obtained from patients. Afterwards, the self-assessed questionnaires were distributed and collected on the same day. Following this step, participants were invited to clinics for oral (caries and periodontal diseases) and general health examination (BMI, body-fat proportion) for the following week. Of the patients participating (n = 186, 94% of the total), 95% (n = 179) filled out the questionnaires. Back translations to and from Turkish were done for health behaviour questionnaires by two native speakers to ensure comparability with the original forms in English. The variables and scales extracted from the main intervention study for analysis are described below.
Toothbrushing behaviour and subjective oral health status These two variables were taken from an earlier study.13 Self-reported toothbrushing frequency was asked as follows: ‘How often do you brush your teeth?’ Toothbrushing, recorded on a 5-point Likert scale (never = 0, once a week or less = 1, 2–5 times/week = 2, once daily = 3, twice or more daily = 4), was reclassified into ‘less than once a day’, ‘once a day’, ‘twice a day’. For further analysis, toothbrushing was dichotomised (brushing daily = 0 vs brushing less than daily = 1).13 Self-reported gingival bleeding was ascertained to assess subjective oral health status by the question: ‘Have you ever observed your gums bleeding while brushing your teeth?’ It was recorded on a 5-point Likert scale ranging from ‘always’ to ‘never’.
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Table 1 Characteristics and response rates to modified WHOQOL-BrefPhPs (n = 158) Not at all (%)
Slightly (%)
A moderate amount (%)
Very much (%)
An extreme amount (%)
1. To what extent do you feel that physical pain prevents you from doing what you need to do?
21
20
38
10
11
2. How much do you need any medical treatment to function in your daily life?
21
20
39
12
8
3. Do you have enough energy for everyday life?
8
15
59
13
5
4. How much do you enjoy life?
7
12
45
22
14
5. To what extent do you feel your life to be meaningful?
6
7
37
26
24
Never
Rarely
Sometimes
Usually
Always
11
20
43
20
6
6. How often do you feel hopeless, depressed or anxious?
Self-reported gingival bleeding was dichotomized as ‘favourable gingival health = 0’ including ‘never or rarely’, and ‘unfavourable gingival health = 1’ consisting of ‘sometimes’, ‘usually’ or ‘always.’13
as a new variable ‘ideal fat’ (yes = 0 vs no = 1 ‘over fat’), considering there were no patients with body fat proportions under the ideal range.13 Self-assessed quality of life
Synergistic biological and psychological risk factors for NCDs and communicable diseases Biomedical Measures
HDL: Taking the target level for high-density lipoprotein (>39 mg/dl) as the cut-off point,23 the respective variable taken from the last health records was dichotomised as ‘favourable’ = 0 or ‘unfavourable’ = 1. Obesity: Weight and height, as anthropometric measures, were used to determine Body Mass Index (BMI; weight in kilograms/height in meters squared. The details of measurement have been described elsewhere.13 According to the current WHO BMI cut-off points,42 BMI was categorised as follows: 39mg/dl) Unfavourable (≤39mg/dl)
89 77 23
59 55
p*** 0.022
0.03
0.029
0.046
ns
* Toothbrushing, gingival bleeding on brushing, BMI, body fat proportion, HDL; ** based on the question with lowest rate of response (WHOQOLBrefPhPs); *** chi-square test, differences according to favourable clinical measures. ns: not significant
HDL); the variables were classified into discriminative clusters based on their factorial loadings, ranging from highest to lowest values. Body-fat proportion was not included in analysis due to its high correlation with BMI. Factors were extracted according to meeting the Kaiser criterion of an eigenvalue > 1. After conducting the factor analysis, regression factor scores for each cluster were obtained. To determine the correlation between each cluster, the regression factor score of the clusters was analysed with the Sperman rank correlation.16 Descriptive statistics, frequency distributions, the contingency co-efficient for determining associations between variables and Spearman rank correlation were applied. Chi-square tests by cross tabulation were applied to compare proportions, and the corresponding odds ratios were calculated. Statistical significance was set at p < 0.05.
RESULTS A minority of the patients brushed their teeth twice a day or more (27%; 37% once a day) and reported favourable gingival health (never/rare gingival bleeding, 37%). 77% had a favourable HDL and 57% high WHOQOL-BrefPhPs (above the mean). A majority of patients had unhealthy BMI (83%) and ranged within the unhealthy body-fat proportions (63%). The
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mean BMI was 30.59 (± 5.77) and the mean for body-fat proportion was 27.75 (± 11.77). Self-reported gingival bleeding was negatively correlated with WHOQOL-BrefPhPs (rs = -0.24, p < 0.05) and toothbrushing frequency (rs = -0.25, p < 0.01). Toothbrushing was positively correlated with HDL (r s = 0.23) and WHOQOL-BrefPhPs (rs = 0.26) (p < 0.001): the participants who brushed their teeth less than daily were more likely to have unfavourable HDL and low WHOQOL-BrefPhPs (32% vs 54%) than those who brushed their teeth daily (17% vs 35%) (OR = 1.84 and 95% CI = 1.02–3.32 vs OR = 1.53 and 95% CI = 1.07– 2.18, p < 0.05). WHOQOL-BrefPhPs was negatively correlated with BMI (rs = - 0.26) and body-fat proportion (rs = -0.30) (p < 0.01). Those with high WHOQOL-BrefPhPs were more likely to have healthy BMI (77%) and body-fat proportion (68%) than those with low WHOQOL-BrefPhPs (23% vs 32%) (OR = 3.15 and 95% CI = 1.08– 9.17 vs OR = 2.13 and 95% CI = 1.01–4.51, p < 0.05). A similiar association was observed between low WHOQOL-BrefPhPs and unfavourable gingival health (p < 0.05) (Table 2). Those with unhealthy BMI were more likely to have unhealthy fat proportions (76%) and unfavourable HDL (28%) than those with healthy BMI (0% vs 4.5%) (OR = 4.23 and 95% CI = 3.11–5.74, p < 0.01 vs OR = 8.03 and 95% CI = 1.03–62.3, p < 0.05).
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Table 3 Factor analysis using Varimax rotated solution† to assess interrelated clusters of toothbrushing frequency, considering the synergistic biological and behavioural risk factors for NCDs and communicable diseases, among Turkish patients with diabetes mellitus type 2 Component 1
Component 2
Healthy weight
Oral health
Favourable toothbrushing
0.610
*
High WHOQOL-BrefPhPs
0.591
*
Favourable gingival health
*
0.798
Healthy BMI
0.642
*
Favourable HDL
0.509
0.593
The clusters in the study group, in total, accounted for 49.6% of the total variance (composed of component 1 with 29.0% and component 2 with 20.5%). † All variables either favourable (0) or unfavourable (1). Body-fat proportion was not included in analysis due to its high correlation with BMI. *Loading values below 0.25 were extracted for ease of communication. The clusters are named based on the variable with the highest loading.
PREVENTIVE ORAL HEALTH BEHAVIOR – TOOTHBRUSHING –
Acute/chronic infectious aetiologies
Modifiable risk factors/lifestyle
BIOLOGICAL FACTORS (HDL) QUALITY OF LIFE RELATED HEALTH DOMAINS (physical and psychological health)
Communicable diseases
Principal component analysis revealed two clusters: 1. modified WHOQOL-BrefPhPs, toothbrushing, and BMI contributed to the ‘healthy weight’ cluster (Table 3); 2. The ‘oral health’ cluster included selfreported gingival bleeding and HDL. The two clusters were correlated with each other (rs = 0.23, p < 0.05).
DISCUSSION To our knowledge, the present study is the first to assess the association of daily toothbrushing with
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Noncommunicable diseases
Fig 1 Relation between daily toothbrushing and biological and qualityof-life–related risk markers of NCDs and communicable diseases.
common biological and quality-of-life–related risk markers of NCDs and communicable diseases (Fig 1). Toothbrushing frequency was correlated with common risk factors for NCDs and communicable diseases, measured in terms of WHOQOLBrefPhPs and HDL, among patients with diabetes mellitus type 2. The association between toothbrushing and quality of life is in line with studies confirming that oral health directly affects quality of life,1,10 which may be explained by the possible impact of toothbrushing on physical health. In the present study, those who reported a higher quality of
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life were more likely to brush their teeth and to have favourable gingival health. HDL is an essential part of the immune system, and periodontal disease, a common chronic subclinical inflammation, is a risk marker for low HDL.34 This is supported by the findings of the present study, in which HDL and gingival bleeding, an initial sign of periodontal disease, share the same cluster. Daily toothbrushing is the most effective method of preventing periodontal disease26 and it has been found to correlate directly with HDL.18 This may explain the observation in the present study that participants who brushed their teeth regularly were more likely to enjoy better oral health and hence better physical health, as specifically shown by favourable HDL levels. This may lead to improvement in quality of life, in terms of having less treatment need, physical pain and depression. This is in line with studies showing that improvement in HDL was accompanied by improvements in quality of life and other health parameters (BMI, fasting blood glucose sugar, heart rate).5,9,29 Toothbrushing behaviour can be a common preventive factor for NCDs and communicable diseases, in terms its interrelation with BMI. In the present study, toothbrushing shared the same cluster with BMI and WHOQOL-BrefPhPs. Individuals with obesity/increased BMI are more likely to have reduced HDL;20 this is more critical for DM2 patients, considering that they are more prone to infections and inflammations. As toothbrushing is correlated with HDL,18 irregular toothbrushing and increased BMI may double the risk of reduced levels of HDL, thus increasing the risk of immune system impairment. Daily toothbrushing may facilitate having a healthy BMI, as it is correlated regular physical activity and healthy eating habits.32,38 The evidence also indicated a correlation between caries and obesity, as they share the same behavioural risk factors.11,12 All this may be explained by the fact that health and/or oral health behaviors co-occur as separate clusters as either health-enhancing or health-damaging behaviours in the same individual.2,17 Maintenance of regular toothbrushing may facilitate other healthy weight-related behaviours such as physical activity and healthy eating habits, which will contribute to a healthy BMI. In turn, a healthy BMI will decrease the risk of low HDL, which is supported by the decreased risk of periodontal inflammation due to regular toothbrushing habits. Taken together, these factors may improve the quality of life both in terms of physical and psychological health. Impaired physical health may lead to a decreased quality of life; obese individuals per-
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ceive their quality of life as poorer than do healthyweight individuals.8,24,28 Richards et al37 found that functional status and psychological health were significantly lower in obese participants than in those with normal weight. Similarly, participants with higher BMI and body-fat proportion in the current study were more likely to have a poorer quality of life, measured in terms of physical functioning in daily life and stress. It is remarkable that those with daily toothbrushing habits were more likely to have a healthy BMI and to report a better quality of life. There is a need for further studies to assess the complex relation between these three health markers. Self-reported toothbrushing frequencies and gingival bleeding may sometimes be imprecise and affected by the perceived social desirability of these behaviours in society, but there is evidence supporting the reliability of the self-reported TB and gingival bleeding.14,39 In addition, self-reported measures comprising these two oral-health–related factors are among the essential oral health indicators in Europe.6 Another limitation of these findings is that they do not include oral health outcomes (periodontal disease, caries) or refer to a clinical intervention. However, this study presents baseline results of a prospective study aiming to highlight the possible interactions between toothbrushing, quality of life, and a biological risk marker of NCDs and communicable diseases. There seems to be a need for clinical studies exploring this interrelation between toothbrushing, NCDs and communicable diseases. Such studies should include periodontal disease, as its inflammatory markers are closely related with some of these diseases.7,25,43,45 Follow-up studies on the impact of regular toothbrushing on the maintenance of good oral health, NCDs and communicable diseases are also needed to identify risk factors and improve the well-being of DM2 patients. Furthermore, the present study, based on a limited number of participants, should be replicated with a larger sample. The role of toothbrushing, a key element for good oral health, for better NCD management has been a neglected issue. Even though common lifestyle interventions have been proposed to reduce the global pandemic of DM2 and oral diseases, such an intervention has not been yet been implemented to our knowledge. In keeping with the WHO’s strategic objectives for 2020,48 interventions are needed that focus on simple common preventive methods for oral diseases and NCDs to improve chronic
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disease management. These preventive methods should also support the prevention of communicable diseases. The present results demonstrate a correlation between toothbrushing, biological and self-assessed quality-of-life–related risk markers of NCDs and communicable disease. The interrelation between regular toothbrushing, better quality of life and healthy weight may indicate common biological and/or behavioural factors. A similar observation supports the correlation between gingival bleeding and HDL. These factors are also potential risks for communicable diseases, as emphasised in the literature.
8.
9.
10.
11.
12.
CONCLUSION Toothbrushing is a simple but effective and easily adjustable health behaviour. Performing it regularly may prevent inflammatory mechanisms and facilitate the maintenance of health-enhancing behaviours, thus improving the physical and emotional health of individuals as well as the quality of life. There seems to be a need for public health promotion and campaigns to increase the awareness among health care professionals and patients about the possible links between NCDs and communicable diseases and the potential intermediary role toothbrushing can play between these two diseases.
13.
14.
15.
16.
17.
18.
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40. Varady KA, Bhutani S, Klempel MC, Kroeger CM. Comparison of effects of diet versus exercise weight loss regimens on LDL and HDL particle size in obese adults. Lipids Health Dis 2011;18:110–119. 41. World Health Organization and International Union against TB Lung Disease. Collaborative framework for care and control of tuberculosis and diabetes. 2011. Available at http://whqlibdoc.who.int/publications/2011/9789241502252_eng.pdf 42. World Health Organization. BMI classification. Available at http://apps.who.int/bmi/index.jsp?introPage = intro_3. html:bmi 43. World Health Organization. Oral Health. Available at http://www.who.int/mediacentre/factsheets/fs318/en/ index.html 44. World Health Organization. WHO Quality of Life-BREF (WHOQOL-BREF). 2004. Available at http://www.who.int/ substance_abuse/research_tools/whoqolbref/en/index. html, Accessed February 2012. 45. World Health Organization. Noncommunicable diseases and oral health. Available at http://www.afro.who.int/en/ clusters-a-programmes/dpc/non-communicable-diseasesmanagementndm/programme-components/oral-health. html 46. World Health Organization. Chronic Diseases and Health Promotion: Integrated chronic disease prevention and control. 2012. Available at http://www.who.int/chp/about/integrated_cd/en/ 47. World Health Organization. Infectious Diseases. 2012. Available at http://www.who.int/topics/infectious_diseases/en/ 48. World Health Organization, Regional Office for Europe. The way forward – scaling up action to prevent and control major communicable diseases. 2012. Available at http:// www.euro.who.int/__data/assets/pdf_file/0011/142022/ Brochure_communicable_diseases.pdf 49. Yusuf S, Hawken S, Ounpuu S. Dans T, Avezum A, Lanas F et al. INTERHEART Study Investigators. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case. control study. Lancet 2004;364:937–952. 50. Zhang W, Wang LQ, Liu YB. Evaluation on quality of life and analysis on its correlation with TCM syndromes in patients of chronic hepatitis B. Chin J Integr Med 2009;15:30–33.
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Toothbrushing: A Link Between Noncommunicable and Communicable Diseases? Ayse Basak Cinara/Inci Oktayb/Lone Schouc Purpose: To assess the correlation between toothbrushing (TB) and the common biological (HDL) and quality-of-life–related risk factors for noncommunicable diseases (NCDs) and communicable diseases among patients with diabetes mellitus type 2 (DM2). Materials and Methods: The present study is part of a prospective intervention study among DM2 patients (n = 200), randomly selected from the outpatient clinics, Istanbul, Turkey. The assessed variables were: TB, self-reported gingival bleeding (SRGB), HDL, BMI, body-fat proportion, modified quality of life scale (WHOQOL-BrefPhPs). Descriptive statistics, frequency distributions, Spearman rank correlation, the chi-square test and factor analysis were applied. Results: A minority of the patients brushed their teeth twice a day or more (27%) and reported no gingival bleeding (37%). Favourable HDL and high WHOQOL-BrefPhPs were 77% and 57%, respectively. A majority of patients had unhealthy BMI (83%) and body-fat proportions (63%). SRGB was negatively correlated with WHOQOL-BrefPhPs (rs = -0.24, p < 0.05) and TB (rs = -0.25, p < 0.01). The patients who reported less than daily TB were more likely to have unfavourable HDL and low WHOQOL-BrefPhPs (32% vs 54%) than those brushing their teeth daily (17% vs 35%, p < 0.05). Principal component analysis revealed two clusters: ‘healthy weight’ (WHOQOL-BrefPhPs, TB, BMI) and ‘oral health’ (SRGB, HDL). Conclusion: The present results demonstrate a correlation between TB and biological and quality-of-life–related risk markers of NCDs and communicable diseases. There seems to be a need to increase the awareness of the significance TB’s potential intermediatory role between NCDs and communicable diseases. Key words: diabetes type II, health coaching, toothbrushing, toothbrushing self-efficacy, quality of life Oral Health Prev Dent 2015;13:515-522 doi: 10.3290/j.ohpd.a34054
N
oncommunicable diseases (NCDs; e.g. cardiovascular diseases, type II diabetes, obesity) are defined by the WHO as ‘slowly progressing, long duration largely preventable illnesses caused due to numerous common modifiable risk factors resulta
Assistant Professor, Oral Public Health Department, Section of Periodontology, Institute of Odontology, University of Copenhagen, Denmark. Idea, hypothesis, experimental design, wrote the manuscript, consulted on statistical evaluation, contributed substantially to discussion.
b
Professor and Head, Oral Public Health Department, Yeditepe Dental Faculty, University of Yeditepe, Istanbul, Turkey. Performed the experiments in fulfilment of requirements for a degree, proofread the manuscript.
c
Professor and Head, Global Oral Health Promotion Section, Institute of Odontology, University of Copenhagen, Denmark. Contributed substantially to writing the manuscript and discussion, consulted on statistical evaluation, language revision, proofread the manuscript.
Correspondence: Ayse Basak Cinar, Department of Odontology, University of Copenhagen, Norre Alle 20, DK-2200 Copenhagen. Tel: +45-27-557-6552. Email: [email protected]
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Submitted for publication: 20.11.13; accepted for publication: 24.02.14
ing from poor lifestyle choices’. By 2020, the contribution of NCDs is expected to rise to 73% of all deaths and 60% of the global burden of disease.46 Communicable diseases (infectious diseases) are caused by pathogenic microorganisms, such as bacteria, viruses, parasites or fungi; the diseases can be spread, directly or indirectly, from one person to another.47 Common public health promotion and campaigns are necessary to prevent NCDs and communicable diseases as proposed by the WHO strategic objectives for 2020.48 Periodontal disease is one of the major oral diseases contributing to the global burden of NCDs;7,43 the disease is highly prevalent worldwide and therefore represents a major global public health problem. Periodontal disease may be caused by local factors, such as dental biofilm, or it may reflect an inadequate immune response. It can also be a manifestation of certain communicable diseases, for example, in people with general infection or
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among people infected with HIV.25 Gingival bleeding is one of the chief signs of the disease.21 The most important method of preventing the initiation/progression of periodontal diseases is daily toothbrushing,26 which can act as a common preventive strategy for both NCDs and communicable diseases. This has been a neglected issue. The current literature supports the concept that NCDs and communicable diseases share synergistic biological and psychological (behavioural) risk factors.9,27,39,41,49 Low blood levels of high density lipoprotein (HDL), a synergistic biological risk factor,3,19,40 is an integral component of innate immunity, mediating diverse functions that defend against viral, bacterial and parasitic infections.19 The evidence shows that low HDL cholesterol concentration may be associated with periodontitis.34,35 Periodontitis is also associated with obesity, which is another synergistic biological risk factor for NCDs46,48 and communicable diseases.22 The impact of toothbrushing on the synergistic biological markers of NCDs and communicable diseases is not known. A WHO quality of life measure, WHOQOL-Bref, provides a valid, reliable, synergistic, self-assessed physical and psychological health measure of the health-related quality-of-life status of persons with NCDs44 and communicable diseases.15,36,50 Although it is well known that oral diseases affect the quality of life,14,30,31 the impact of preventive oral behaviours, in particular toothbrushing, has been poorly explored.18 The aim of the present study was to assess the correlation between a preventive oral health behaviour (toothbrushing) and the common biological (HDL) and self-assessed quality-of-life–related risk factors (modified WHOQOL-Bref) for NCDs and communicable diseases among patients with diabetes mellitus type 2 (DM2).
MATERIALS AND METHODS The present study is part of a prospective intervention study which consists of 3 stages (baseline-initiation, maintenance and follow-up) among DM2 patients (n = 197), randomly selected from the outpatient clinics of two hospitals in Istanbul, Turkey. The power and sample size was calculated by G*power (effect size w = 0.3, α error probability = 0.05, power [1- β error probability] = 0.95).4 Patients were included if they were between 30 and 65 years old, had at least 4 functional teeth and
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had not undergone psychological treatment or hospitalisation. The data in the present study originate from the baseline measurements of the prospective study that were collected at the start and finish of each of the 3 stages by clinical measurements (BMI, body-fat proportion, HDL, LDL, HbA1c) and self-assessed questionnaires (including modified scales, e.g. PAID, WHOQOL-Bref). Ethical approval and written permission were granted by the Ministry of Health to conduct the study. The research was announced at the outpatient clinics by pamphlets, brochures, physicians and the head nurses. At baseline, the patients interested in participating in the study were selected according the eligibility criteria. Verbal and written information about the study was provided and then informed consent was obtained from patients. Afterwards, the self-assessed questionnaires were distributed and collected on the same day. Following this step, participants were invited to clinics for oral (caries and periodontal diseases) and general health examination (BMI, body-fat proportion) for the following week. Of the patients participating (n = 186, 94% of the total), 95% (n = 179) filled out the questionnaires. Back translations to and from Turkish were done for health behaviour questionnaires by two native speakers to ensure comparability with the original forms in English. The variables and scales extracted from the main intervention study for analysis are described below.
Toothbrushing behaviour and subjective oral health status These two variables were taken from an earlier study.13 Self-reported toothbrushing frequency was asked as follows: ‘How often do you brush your teeth?’ Toothbrushing, recorded on a 5-point Likert scale (never = 0, once a week or less = 1, 2–5 times/week = 2, once daily = 3, twice or more daily = 4), was reclassified into ‘less than once a day’, ‘once a day’, ‘twice a day’. For further analysis, toothbrushing was dichotomised (brushing daily = 0 vs brushing less than daily = 1).13 Self-reported gingival bleeding was ascertained to assess subjective oral health status by the question: ‘Have you ever observed your gums bleeding while brushing your teeth?’ It was recorded on a 5-point Likert scale ranging from ‘always’ to ‘never’.
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Table 1 Characteristics and response rates to modified WHOQOL-BrefPhPs (n = 158) Not at all (%)
Slightly (%)
A moderate amount (%)
Very much (%)
An extreme amount (%)
1. To what extent do you feel that physical pain prevents you from doing what you need to do?
21
20
38
10
11
2. How much do you need any medical treatment to function in your daily life?
21
20
39
12
8
3. Do you have enough energy for everyday life?
8
15
59
13
5
4. How much do you enjoy life?
7
12
45
22
14
5. To what extent do you feel your life to be meaningful?
6
7
37
26
24
Never
Rarely
Sometimes
Usually
Always
11
20
43
20
6
6. How often do you feel hopeless, depressed or anxious?
Self-reported gingival bleeding was dichotomized as ‘favourable gingival health = 0’ including ‘never or rarely’, and ‘unfavourable gingival health = 1’ consisting of ‘sometimes’, ‘usually’ or ‘always.’13
as a new variable ‘ideal fat’ (yes = 0 vs no = 1 ‘over fat’), considering there were no patients with body fat proportions under the ideal range.13 Self-assessed quality of life
Synergistic biological and psychological risk factors for NCDs and communicable diseases Biomedical Measures
HDL: Taking the target level for high-density lipoprotein (>39 mg/dl) as the cut-off point,23 the respective variable taken from the last health records was dichotomised as ‘favourable’ = 0 or ‘unfavourable’ = 1. Obesity: Weight and height, as anthropometric measures, were used to determine Body Mass Index (BMI; weight in kilograms/height in meters squared. The details of measurement have been described elsewhere.13 According to the current WHO BMI cut-off points,42 BMI was categorised as follows: 39mg/dl) Unfavourable (≤39mg/dl)
89 77 23
59 55
p*** 0.022
0.03
0.029
0.046
ns
* Toothbrushing, gingival bleeding on brushing, BMI, body fat proportion, HDL; ** based on the question with lowest rate of response (WHOQOLBrefPhPs); *** chi-square test, differences according to favourable clinical measures. ns: not significant
HDL); the variables were classified into discriminative clusters based on their factorial loadings, ranging from highest to lowest values. Body-fat proportion was not included in analysis due to its high correlation with BMI. Factors were extracted according to meeting the Kaiser criterion of an eigenvalue > 1. After conducting the factor analysis, regression factor scores for each cluster were obtained. To determine the correlation between each cluster, the regression factor score of the clusters was analysed with the Sperman rank correlation.16 Descriptive statistics, frequency distributions, the contingency co-efficient for determining associations between variables and Spearman rank correlation were applied. Chi-square tests by cross tabulation were applied to compare proportions, and the corresponding odds ratios were calculated. Statistical significance was set at p < 0.05.
RESULTS A minority of the patients brushed their teeth twice a day or more (27%; 37% once a day) and reported favourable gingival health (never/rare gingival bleeding, 37%). 77% had a favourable HDL and 57% high WHOQOL-BrefPhPs (above the mean). A majority of patients had unhealthy BMI (83%) and ranged within the unhealthy body-fat proportions (63%). The
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mean BMI was 30.59 (± 5.77) and the mean for body-fat proportion was 27.75 (± 11.77). Self-reported gingival bleeding was negatively correlated with WHOQOL-BrefPhPs (rs = -0.24, p < 0.05) and toothbrushing frequency (rs = -0.25, p < 0.01). Toothbrushing was positively correlated with HDL (r s = 0.23) and WHOQOL-BrefPhPs (rs = 0.26) (p < 0.001): the participants who brushed their teeth less than daily were more likely to have unfavourable HDL and low WHOQOL-BrefPhPs (32% vs 54%) than those who brushed their teeth daily (17% vs 35%) (OR = 1.84 and 95% CI = 1.02–3.32 vs OR = 1.53 and 95% CI = 1.07– 2.18, p < 0.05). WHOQOL-BrefPhPs was negatively correlated with BMI (rs = - 0.26) and body-fat proportion (rs = -0.30) (p < 0.01). Those with high WHOQOL-BrefPhPs were more likely to have healthy BMI (77%) and body-fat proportion (68%) than those with low WHOQOL-BrefPhPs (23% vs 32%) (OR = 3.15 and 95% CI = 1.08– 9.17 vs OR = 2.13 and 95% CI = 1.01–4.51, p < 0.05). A similiar association was observed between low WHOQOL-BrefPhPs and unfavourable gingival health (p < 0.05) (Table 2). Those with unhealthy BMI were more likely to have unhealthy fat proportions (76%) and unfavourable HDL (28%) than those with healthy BMI (0% vs 4.5%) (OR = 4.23 and 95% CI = 3.11–5.74, p < 0.01 vs OR = 8.03 and 95% CI = 1.03–62.3, p < 0.05).
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Table 3 Factor analysis using Varimax rotated solution† to assess interrelated clusters of toothbrushing frequency, considering the synergistic biological and behavioural risk factors for NCDs and communicable diseases, among Turkish patients with diabetes mellitus type 2 Component 1
Component 2
Healthy weight
Oral health
Favourable toothbrushing
0.610
*
High WHOQOL-BrefPhPs
0.591
*
Favourable gingival health
*
0.798
Healthy BMI
0.642
*
Favourable HDL
0.509
0.593
The clusters in the study group, in total, accounted for 49.6% of the total variance (composed of component 1 with 29.0% and component 2 with 20.5%). † All variables either favourable (0) or unfavourable (1). Body-fat proportion was not included in analysis due to its high correlation with BMI. *Loading values below 0.25 were extracted for ease of communication. The clusters are named based on the variable with the highest loading.
PREVENTIVE ORAL HEALTH BEHAVIOR – TOOTHBRUSHING –
Acute/chronic infectious aetiologies
Modifiable risk factors/lifestyle
BIOLOGICAL FACTORS (HDL) QUALITY OF LIFE RELATED HEALTH DOMAINS (physical and psychological health)
Communicable diseases
Principal component analysis revealed two clusters: 1. modified WHOQOL-BrefPhPs, toothbrushing, and BMI contributed to the ‘healthy weight’ cluster (Table 3); 2. The ‘oral health’ cluster included selfreported gingival bleeding and HDL. The two clusters were correlated with each other (rs = 0.23, p < 0.05).
DISCUSSION To our knowledge, the present study is the first to assess the association of daily toothbrushing with
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Noncommunicable diseases
Fig 1 Relation between daily toothbrushing and biological and qualityof-life–related risk markers of NCDs and communicable diseases.
common biological and quality-of-life–related risk markers of NCDs and communicable diseases (Fig 1). Toothbrushing frequency was correlated with common risk factors for NCDs and communicable diseases, measured in terms of WHOQOLBrefPhPs and HDL, among patients with diabetes mellitus type 2. The association between toothbrushing and quality of life is in line with studies confirming that oral health directly affects quality of life,1,10 which may be explained by the possible impact of toothbrushing on physical health. In the present study, those who reported a higher quality of
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life were more likely to brush their teeth and to have favourable gingival health. HDL is an essential part of the immune system, and periodontal disease, a common chronic subclinical inflammation, is a risk marker for low HDL.34 This is supported by the findings of the present study, in which HDL and gingival bleeding, an initial sign of periodontal disease, share the same cluster. Daily toothbrushing is the most effective method of preventing periodontal disease26 and it has been found to correlate directly with HDL.18 This may explain the observation in the present study that participants who brushed their teeth regularly were more likely to enjoy better oral health and hence better physical health, as specifically shown by favourable HDL levels. This may lead to improvement in quality of life, in terms of having less treatment need, physical pain and depression. This is in line with studies showing that improvement in HDL was accompanied by improvements in quality of life and other health parameters (BMI, fasting blood glucose sugar, heart rate).5,9,29 Toothbrushing behaviour can be a common preventive factor for NCDs and communicable diseases, in terms its interrelation with BMI. In the present study, toothbrushing shared the same cluster with BMI and WHOQOL-BrefPhPs. Individuals with obesity/increased BMI are more likely to have reduced HDL;20 this is more critical for DM2 patients, considering that they are more prone to infections and inflammations. As toothbrushing is correlated with HDL,18 irregular toothbrushing and increased BMI may double the risk of reduced levels of HDL, thus increasing the risk of immune system impairment. Daily toothbrushing may facilitate having a healthy BMI, as it is correlated regular physical activity and healthy eating habits.32,38 The evidence also indicated a correlation between caries and obesity, as they share the same behavioural risk factors.11,12 All this may be explained by the fact that health and/or oral health behaviors co-occur as separate clusters as either health-enhancing or health-damaging behaviours in the same individual.2,17 Maintenance of regular toothbrushing may facilitate other healthy weight-related behaviours such as physical activity and healthy eating habits, which will contribute to a healthy BMI. In turn, a healthy BMI will decrease the risk of low HDL, which is supported by the decreased risk of periodontal inflammation due to regular toothbrushing habits. Taken together, these factors may improve the quality of life both in terms of physical and psychological health. Impaired physical health may lead to a decreased quality of life; obese individuals per-
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ceive their quality of life as poorer than do healthyweight individuals.8,24,28 Richards et al37 found that functional status and psychological health were significantly lower in obese participants than in those with normal weight. Similarly, participants with higher BMI and body-fat proportion in the current study were more likely to have a poorer quality of life, measured in terms of physical functioning in daily life and stress. It is remarkable that those with daily toothbrushing habits were more likely to have a healthy BMI and to report a better quality of life. There is a need for further studies to assess the complex relation between these three health markers. Self-reported toothbrushing frequencies and gingival bleeding may sometimes be imprecise and affected by the perceived social desirability of these behaviours in society, but there is evidence supporting the reliability of the self-reported TB and gingival bleeding.14,39 In addition, self-reported measures comprising these two oral-health–related factors are among the essential oral health indicators in Europe.6 Another limitation of these findings is that they do not include oral health outcomes (periodontal disease, caries) or refer to a clinical intervention. However, this study presents baseline results of a prospective study aiming to highlight the possible interactions between toothbrushing, quality of life, and a biological risk marker of NCDs and communicable diseases. There seems to be a need for clinical studies exploring this interrelation between toothbrushing, NCDs and communicable diseases. Such studies should include periodontal disease, as its inflammatory markers are closely related with some of these diseases.7,25,43,45 Follow-up studies on the impact of regular toothbrushing on the maintenance of good oral health, NCDs and communicable diseases are also needed to identify risk factors and improve the well-being of DM2 patients. Furthermore, the present study, based on a limited number of participants, should be replicated with a larger sample. The role of toothbrushing, a key element for good oral health, for better NCD management has been a neglected issue. Even though common lifestyle interventions have been proposed to reduce the global pandemic of DM2 and oral diseases, such an intervention has not been yet been implemented to our knowledge. In keeping with the WHO’s strategic objectives for 2020,48 interventions are needed that focus on simple common preventive methods for oral diseases and NCDs to improve chronic
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disease management. These preventive methods should also support the prevention of communicable diseases. The present results demonstrate a correlation between toothbrushing, biological and self-assessed quality-of-life–related risk markers of NCDs and communicable disease. The interrelation between regular toothbrushing, better quality of life and healthy weight may indicate common biological and/or behavioural factors. A similar observation supports the correlation between gingival bleeding and HDL. These factors are also potential risks for communicable diseases, as emphasised in the literature.
8.
9.
10.
11.
12.
CONCLUSION Toothbrushing is a simple but effective and easily adjustable health behaviour. Performing it regularly may prevent inflammatory mechanisms and facilitate the maintenance of health-enhancing behaviours, thus improving the physical and emotional health of individuals as well as the quality of life. There seems to be a need for public health promotion and campaigns to increase the awareness among health care professionals and patients about the possible links between NCDs and communicable diseases and the potential intermediary role toothbrushing can play between these two diseases.
13.
14.
15.
16.
17.
18.
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