DOI: 10.1111/ipd.12110
Overweight and dental caries: the association among German children GHALIB QADRI1,2, MOHAMMED ALKILZY1,3, YOU-SHAN FENG4 & CHRISTIAN SPLIETH1 1
Preventive and Pediatric Dentistry Department, University of Greifswald, Greifswald, Germany, Al-Hada Military Hospital, Taif, Saudi Arabia, 3Department of Pediatric Dentistry, University of Aleppo, Aleppo, Syria and 4 Community Medicine Department, University of Greifswald, Greifswald, Germany 2
International Journal of Paediatric Dentistry 2014 Objectives. The aim of this study was to deter-
mine the relationship between iso-body mass index (iso-BMI) and both dental caries status and caries increment among German school children. Methods. Six hundred and ninety-four students (age range 9–12 years, mean 10.34 0.56, 48% females) were recruited from the fifth grade of 18 primary schools. Weight, height, and oral health data number of decayed, missing and filled teeth (DMFT) as well as parent/legal guardian questionnaire (measuring SES) were collected during school dental examination at baseline and after one and a half-year follow-up. The body mass index (BMI) was calculated using the international classification system for childhood overweight and obesity (iso-BMI). Statistical
Introduction
Dental caries is one of the most prevalent chronic diseases in human populations. It is a multifactorial disease with the consumption of dietary sugars as its most important etiological cause1. Unhealthful eating practices in children such as missing daily breakfast or who ate fewer than five servings of fruits and vegetables per day found with significantly greater odds of experiencing dental caries2. Besides dental caries, an unhealthy diet, particularly one high in non-milk extrinsic sugars and soft drinks, affects the incidence of many chronic diseases such as heart disease, diabetes, bone loss or bone fractures, and obesity3,4. Currently, the prevalence of childCorrespondence to: Dr. Ghalib Qadri, Preventive & Pediatric Dentistry Unit, Al-Hada Military Hospitals, P.O. Box. 1347, Taif 21944, KSA. E-mail: [email protected]
analyses were performed using Poisson regression models. Results. Iso-BMI was significantly associated with dental caries prevalence and severity in the permanent dentition (P = 0.039). Low-normal weight children had a lower mean DMFT (0.56) than did overweight/obese children (0.70). In addition, a border-line significant association was found between overweight/obese children and caries increment (P = 0.055). Conclusion. Although iso-BMI was associated with dental caries prevalence and severity, the association between caries increment and iso-BMI did not reach a statistical significance. Overweight/ obese children however acquired more additional carious lesions during the follow-up period than children with low-normal weight.
hood obesity and overweight is increasing rapidly in Europe and other parts of the world, being growing epidemic and public health crisis5–7. Childhood obesity and overweight are proved to be associated with several risk factors for later heart diseases and other chronic diseases5. As dental caries, overweight in children is also a multifactorial disease that may include several social and cultural factors. The increased consumption of soft drinks and fast food, together with the modern sedentary lifestyle, has contributed to the increasing number of overweight children worldwide5,8. Low socioeconomic level in terms of living areas could also be related to a higher prevalence of obesity in children9. In addition to that, particular dietary habits could lead to overweight/obesity in children and teenagers, such as choosing food high in fats and refined carbohydrates8,10. Given the causative relation between refined carbohydrates and dental caries11, it is logical to
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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hypothesize that high weight might also be a marker for dental caries in children and teenagers or vise versa. Therefore, the purpose of this study was to determine whether the iso-BMI might be associated with dental caries in German school children and to investigate its predictive power for one and a half-year caries increment. Methods
Subjects This is a cross-sectional, prospective study that determines the association between isobody mass index (iso-BMI) and dental caries among German school children, and investigates the prospective caries increment among those children. After the approval of the research and ethics committees of Greifswald University and the Data Protection Commissioner in the Ministry of Education, participants were recruited from the fifth grade of the primary schools in the district of Eastern Pomerania and Greifswald city (North-East Germany, 162 653 inhabitants, unemployment rate 12.7%, drinking water fluoride level 0.2–0.3 ppm) 12. Nineteen of a total of 22 targeted schools consented to take part in this prospective cohort study, comprising a sample of 914 students with an age range from 9 to 12 years. Apart from the compulsory dental school examination, the participation in this study was voluntary, and written informed consent forms were obtained from the parents/legal guardians of the children. The sampling frame consists of all fifth grade students, from all participating schools, whose parents/legal guardians have signed the written informed consent form and who were present at both ‘baseline’ and ‘followup’ examination. Students with any significant systematic disorders were excluded from the study. Clinical examinations Thorough dental and clinical examinations were conducted by three well-trained and calibrated examiners throughout participating
schools. The data were collected in two steps as part of an extended obligatory dental school examination. The baseline data were performed on the fifth grade students from September to October 2007, and the final examination (follow-up) carried out after 19 months on the same children, where they become in the 6th grade, during February and March 2009. Interclass correlation coefficient (ICC) was used to assess the interexaminer reproducibility between examiners in both the baseline and the follow-up examinations. The dental examination was conducted under natural indirect light with additional electric light, using dental mirrors and explorers based on the WHO diagnostic criteria guidelines13. All examinations were conducted with the children in upright positions with the heads tilted back. Caries experience was expressed using the DMFT index (number of decayed, missing, and filled teeth). Teeth or surfaces were considered carious (D) if there was visual evidence of a carious defect. Missing components (M) due to caries, including teeth, indicated for extraction and (F) for filled teeth. Data concerning height and weight of the children were also obtained during the clinical examination day at schools. Body height was measured using a portable stadiometer (Seca; Vogel and Halke, Type: 214, Hamburg, Germany), and the weight was measured using electronic scale (Seca Vogel and Halke, Type: 861). The children were measured without shoes or heavy clothing. Among children and teenagers, body fat changes as the body grows and development differs across gender. Unlike the body mass index (BMI) assessments for adults, assessments for children and teenagers take these growth- and gender-specific patterns differences into account14. The international classification systems for childhood obesity are referred to as ‘iso-BMI’ categories describing overweight and obesity in children, based on gender and pooled international data for body mass index and linked to the widely used adult obesity cutoff values14. This classification encompasses a wide range of acceptance among social scientists and many other authors15,16.
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Overweight and dental caries
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Using the iso-BMI values, children were categorized with the following cutoff values: lownormal weight = BMI ≤25, overweight = BMI >25–29.9, obesity = BMI ≥3014. Dental and clinical examinations took about 45 min per class with around 25 students per class. Parents additionally answered a self-completion questionnaire containing questions on their socioeconomic status (SES), which were distributed during parent–teacher meetings. The questionnaire was adopted from Lange et al. based on four main factors defining the SES: education, vocational training, net household income, and employment status17. The domains of the questionnaires were compatible with the research tools of another, representative national study, for example, German Health Interview and Examination Survey for Children and Adolescents18.
Whitney U-test and Poisson regression analysis were employed. Poisson regression analyses were conducted for the dependent variables (DMFT and caries increment). The primary independent variable was BMI category. Additionally, age and gender were included in the models as covariates. Poisson regression analyses were conducted for outcomes that are counting data (DMFT, caries increment, and BMI). We also stratified the analysis over three SES categories of high, middle, and low. The incidence rate ratio (IRR) was calculated for the discrete dependent variables to study the effect of independent variables on oral health status. All data were processed and analyzed using SPSS (version 15.0.1) and STATA program (version 10). In all the analyses, the level of statistical significance was set at P < 0.05.
Statistical analysis
Results
During clinical examination, all data were entered directly in Microsoft Office Excel 2003â data bank and then into the SPSSâ software (Statistical Package for the Social Sciences; version 15.0.1; SPSS Inc., Chicago, IL, USA). The questionnaires were automatically scanned with Teleformâ (Version 10.2) and then transferred to SPSSâ. Descriptive analyses using distributions, means, and standard deviations (SDs) were prepared. Then, after dichotomizing several variables (DMFT, caries increment, and isoBMI categories), proportions for each of these variables were calculated. In the subsidiary analyses, the standard iso-BMI categories were used, but the categories overweight and obese were combined in one variable, for a statistical point of view, referred to it in the text as ‘overweight/obese’, and as similarly indicated in the literature10,19–21. These terms were referring to iso-BMI values of >25 kg/ m2. Caries increment in the permanent teeth was calculated by subtracting the DMFT values at baseline examination from that of the final examination (follow-up). For parametric data, chi-squared tests and independent t-tests were used. For the nonparametric data (DMFT and BMI), the Mann–
Baseline examination All of the fifth grade children in the 18 participating schools in the district of East Pomerania and Greifswald city were examined. Of a total 914 students, only 694 students (from 18 schools) were finally included in the study (mean 10.34 years 0.56, 48% females). Reasons for nonresponse were lack of parental interest (18.9%), refusal (1.7%), and moving out of the research region before the questionnaire was distributed (0.1%). In the follow-up period, 4.2% of the students dropped out as they failed to attend either one or both examinations (neutral dropout). In randomly selected students, the ICC values for the first and final examinations were 0.93 and 0.97, respectively. The interpretations of these ICC values give excellent agreements between the examiners in both examinations22. At baseline examination, 76% of the students were low-normal weight (iso-BMI ≤25; n = 525), and 24% were overweight/obese (iso-BMI >25; n = 169). The iso-BMI was significantly associated with gender (P = 0.026). Age was not associated with different iso-BMI categories (P = 0.55), as Table 1 shows below.
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Table 1. Age, gender, and caries experience distribution according to iso-BMI.
Parameters No. of subjects Age in years, Mean (SD) Gender Male% Female% DMFT mean (SD)
Low-normal weight
Overweight/ Obese
P-value
525 (76%) 10.34 (0.55)
169 (24%) 10.37 (0.57)
– 0.545†
259 (72%) 266 (79%) 0.56 (1.18)
100 (28%) 79 (21%) 0.70 (1.19)
0.026*‡ 0.050*‡
†t-test. ‡Chi-square test. *P-value 25) had more caries experience (DMFT indices) compared with low-normal weight individuals (iso-BMI 0), 30% (n = 59) of these children were overweight/obese (BMI >25) compared with only 22% (n = 110) in the caries-free group (DMFT = 0). Statistical analysis using the chi-squared for independence test indicated a significant difference (P = 0.039). Follow-up Almost sixteen percent (n = 106) of the children in the sample study who were free of caries (DMFT = 0) at baseline acquired new carious defects or fillings during the follow-up period. The majority of new lesions in permanent teeth during the follow-up period were located on the first molars (50%). Fourteen percent (n = 74) of the students in the low-normal weight acquired additional carious lesions during the follow-up period, whereas 19% (n = 32) of the overweight/ obese students acquired new carious lesions. Basic Poisson regression (crude) demonstrated a border-line significant association between caries increment and weight status (IRR 1.37, P = 0.055). Gender and age did not have a strong confounding effect when adjusted in the model (Table 2). An interesting significant interaction was observed for the socioeconomic status; therefore, the analysis was stratified by three levels of SES. Among those with high SES, overweight/obesity had four times higher caries risk increment than low-normal weight students (P < 0.001). Adjusting for age and gender did not change the effect. In contrast to this, no statistical significant associations were found in the middle and low SES (P = 0.530 and P = 0.826, respectively). Table 2. Caries increment rate ratio (IRR) from Poisson regression analysis for overweight/obese children in comparison with low-normal weight.
Figure 1. Mean DMFT and DT values among different body mass index groups.
Caries increment
IRR*
95% CI
P-values*
Crude Adjusted for gender Adjusted for age Adjusted for SES Fully adjusted
1.37 1.37 1.35 1.42 1.38
0.99–1.90 0.99–1.89 0.98–1.87 0.99–2.05 0.96–2.00
0.055 0.059 0.069 0.058 0.084
*Data are reported as IRR using Poisson regression analysis.
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Overweight and dental caries
Discussion
The findings of this study indicated a significant association between caries experience and different iso-BMI categories among German primary school children in the district of Mecklenburg-Vorpommern. When considering the findings, it should be kept in mind that these findings were based on a cross-sectional design, which facilitates collecting information from large healthy groups of children with more confined age limits. Turning to the follow-up stage of the study, which provided a clear comparison between students’ current and future caries experience, which confirmed the actual relationship between iso-BMI and caries experience. A high prevalence of overweight and obese students was observed in the study population, affecting almost one quarter of the study sample (24%, n = 169). This supports what the WHO described as a ‘global epidemic disease’, where overweight and obesity in fact are an increasing public health problems in Germany and worldwide5,23,24. Our results reflect a previous German study where the prevalence of overweight and obese 6- to 10year-old students was 26%25. Similarly, high numbers were reported for many other European Western countries5,26,27. The multifactorial etiology of obesity and/or overweight includes social and cultural factors. In the literature, a low SES in terms of living area conditions appears to be related to a higher prevalence of obesity9,28. But this study shows that even after adjusting for the SES, the factor ‘overweight/obesity’ was still significantly associated with caries prevalence at baseline and after one and a half-year follow-up. In the high SES group, this association was very pronounced as overweight and obese children in this group showed four times higher caries risk compared to the low-normal weight children. These results are in agreement with a German study in which children with high DMFT indices had significantly higher BMI values than caries-free children29. In this study, caries experience was more pronounced in the overweight/obese group than
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in the normal-underweight group. The overweight/obese group had an average DMFT index of 0.70, compared to 0.56 for the lownormal weight group. After the follow-up period, around 16% (106) of the students acquired new carious lesions. This trend is well described in the literature as the age range of the student during the follow-up period was from 10–12 year old, which is usually associated with an extensive need of dental treatment30. The rest of the students either remained free of caries (DMFT = 0), their caries experience stayed constant or they experienced caries reversals. Caries reversal means that the net sum of caries ended up negatively, and this is a common problem in longitudinal epidemiologic studies of dental caries31. In this study, this problem was taken into account to minimize its occurrence, through presenting all the baseline records at the time of re-examination, so if caries reversals had occurred, a double check with a confirmation would be indicated. A noteworthy observation in this context is that the majority of new lesions in permanent teeth during the follow-up period were located on the first molars (50%). This result confirms previous findings by Mejare et al., [1998]: the most caries-susceptible tooth in the young permanent dentition is the first permanent molar accounting for more than 60% of all restored surfaces32,33. Obesity and dental caries have common ‘risk determinants’ that increase the likelihood of both diseases, such as dietary habits. For example, a sugar-rich diet, including beverages, is associated with various health problems such as obesity, dental caries, and poor diet quality4,34. Therefore, a high sugar intake, especially in drinks, could be a causal factor for caries and overweight/obesity in children, which is still not confirmed in many studies and reviews. Interestingly, the analysis for different socioeconomic levels showed that the overweight/obese students who belong to the high socioeconomic status had four times higher caries risk than low-normal weight students in the same socioeconomic status, whereas no significant difference was found in the middle or low socioeconomic status.
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Definitely, both variables (caries and obesity) are dietary-related cumulative conditions and thus the group who belong to the high SES is more likely to exhibit a stronger relationship, where eating and, especially, drinking patterns vary among this particular category of socioeconomic level35. In a recent study on dental school pediatric clinic, Werner et al. found that a smaller proportion of obese and overweight children presented with more primary tooth caries than low-normal weight children in the mixed dentition24 which is in agreement with our results. They, however, did not find any significant association between SES and overweight/obesity or caries24. Unlike this study, a strong and significant relationship was found between overweight/obese students who belong to the high SES and caries increment compared to low-normal weight students. This association was found only in the high SES groups and not in the middle or low SES. This could be attributed to the different methods of identifying SES and the way that the SES (as a variable) was assessed in the statistical analysis. For example, in the recently mentioned study, the authors depend on patients’ zip codes and their residence addresses as indicators for SES (which is a common method in many American studies)24. This method, however, lacks for sensitivity and specificity particularly if taken on an individual level, and areas of lower and higher SES can exist in every zip code. In this study and others representative studies17,18, the SES was assessed on an individual level based on four main items: family income, parental level of education, vocational training, and employment status. The SES as a single variable may not have a significant confounding effect on the study samples, as found in this study. But stratifying and analyzing the SES in its different levels is an important distinction and may explain differences reported in other study results. In a systematic review by Kantovitz et al.4, the authors concluded conflicting results, showing the need for further well-designed studies to demonstrate the real relationship
between dental caries and obesity. In another recently published study by D’Mello et al., caries experience was assessed in 8-year-old children who were receiving treatment in Otago pediatric dental clinic. The authors found that there was no significant association between BMI and dental caries21. Hilgers et al.30 and Willerhausen et al.20,24, also reported an association between high weight and high caries frequency in children. On the other hand, many other studies did not find a significant association between body weight and dental caries10,36,37. One possible explanation for the understanding of the results is the structure of the German National Health System which includes dental treatment for children at private practitioners of their choice. Children with high SES background and their parents often utilize services more on their own account than families with low SES. During the follow-up period of this study, the overweight/obese students acquired more additional carious lesions than students with low-normal weight with a borderline statistical significance. These results are in agreement with many studies that have suggested that obese children run an increased risk of caries development29,38,39. On the other hand, many other studies have not provided evidence to suggest that overweight children run an increased risk of dental caries10,36,37. The samples of the study were recruited among the community and directly from the targeted study region schools, unlike the clinical samples that will be biased in terms of oral and general health. Because of that, clear skews in caries prevalence and distribution among the samples of the study were noted, representing children with zero-value DMFT index. A non-Gaussian distribution (skewed to the right) was the result, which is a very common distribution in the DMFT and epidemiological studies, particularly in Western developed countries, where DMFT = 0 may count for most of the samples. Therefore, in the statistical analysis, Poisson regressions were used, which took in account such skews and the fact that count outcomes are discrete variables with no negative values.
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Overweight and dental caries
The sample taken from this study only represented the children attending schools in fifth grade at baseline. Thus, the results can only be generalized for this age range. The number of children examined and the response rate, even for the parent questionnaire, were large enough to represent the population attending schools at that age. Considering that the clinical examinations were carried out by three well-trained examiners, the interexaminer reproducibility values for the baseline and follow-up examinations produced excellent agreement (0.93 and 0.97, respectively). The values for the interexaminer reproducibility were within the same range of other studies 40 or even higher than others 41,42 which reported an interexaminer reproducibility of j = 0.90 and 0.85. After discussing the study findings, it is more appropriate to examine the limitations of this study. First, some of the included schools were running a preventive program during the data collection phase of this study. It is important, however, to note that the research questions that suggested earlier were mainly depending on the cross-sectional design of this study. In most of the previously mentioned studies, dental caries recordings were performed by oral examination and diagnosed at cavity level. Only one study diagnosed proximal caries including initial caries lesions using bitewing radiographs38. In Germany, however, such a procedure could cause a particular difficulty during ethical committee review, especially in health preventive studies. The findings of this study are also meant to be used in future preventive programs. In conclusion, this study showed a strong association between iso-BMI and dental caries prevalence. The association between caries increment and iso-BMI, however, failed to reach a statistically significant level after 1 year and half at follow-up. Knowledge of these relationships could reorient health policies and guidelines to incorporate dentists in multidisciplinary medical teams to promote oral health in conjunction with general health and healthy diet. This integrated approach is likely to be more cost-effective, and a major benefit could be gained by focusing on improving the general health condi-
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tions for the whole population, particularly groups with high risk. These characteristics could also be used in adjunct to other factors to identify children at risk of developing caries early and used to target preventive dental care for those children in advance. Acknowledegment
The authors would like to acknowledge and thank the high cooperation of the parents, schools, and children who agreed to participate in the study. Conflict of interest
The authors declare that they have no conflict of interest.
Why this paper is important to pediatric dentists? ● These results highlight the important role of pediatric dentists to identify and to reduce the risk of childhood obesity as well as dental caries. ● Preventive and pediatric dentistry departments should participate in any multidisciplinary health-promoting programs to promote a healthy diet and general health not only to prevent dental caries but also to reduce the risk factors for overweight and obesity in children.
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Overweight and dental caries: the association among German children GHALIB QADRI1,2, MOHAMMED ALKILZY1,3, YOU-SHAN FENG4 & CHRISTIAN SPLIETH1 1
Preventive and Pediatric Dentistry Department, University of Greifswald, Greifswald, Germany, Al-Hada Military Hospital, Taif, Saudi Arabia, 3Department of Pediatric Dentistry, University of Aleppo, Aleppo, Syria and 4 Community Medicine Department, University of Greifswald, Greifswald, Germany 2
International Journal of Paediatric Dentistry 2014 Objectives. The aim of this study was to deter-
mine the relationship between iso-body mass index (iso-BMI) and both dental caries status and caries increment among German school children. Methods. Six hundred and ninety-four students (age range 9–12 years, mean 10.34 0.56, 48% females) were recruited from the fifth grade of 18 primary schools. Weight, height, and oral health data number of decayed, missing and filled teeth (DMFT) as well as parent/legal guardian questionnaire (measuring SES) were collected during school dental examination at baseline and after one and a half-year follow-up. The body mass index (BMI) was calculated using the international classification system for childhood overweight and obesity (iso-BMI). Statistical
Introduction
Dental caries is one of the most prevalent chronic diseases in human populations. It is a multifactorial disease with the consumption of dietary sugars as its most important etiological cause1. Unhealthful eating practices in children such as missing daily breakfast or who ate fewer than five servings of fruits and vegetables per day found with significantly greater odds of experiencing dental caries2. Besides dental caries, an unhealthy diet, particularly one high in non-milk extrinsic sugars and soft drinks, affects the incidence of many chronic diseases such as heart disease, diabetes, bone loss or bone fractures, and obesity3,4. Currently, the prevalence of childCorrespondence to: Dr. Ghalib Qadri, Preventive & Pediatric Dentistry Unit, Al-Hada Military Hospitals, P.O. Box. 1347, Taif 21944, KSA. E-mail: [email protected]
analyses were performed using Poisson regression models. Results. Iso-BMI was significantly associated with dental caries prevalence and severity in the permanent dentition (P = 0.039). Low-normal weight children had a lower mean DMFT (0.56) than did overweight/obese children (0.70). In addition, a border-line significant association was found between overweight/obese children and caries increment (P = 0.055). Conclusion. Although iso-BMI was associated with dental caries prevalence and severity, the association between caries increment and iso-BMI did not reach a statistical significance. Overweight/ obese children however acquired more additional carious lesions during the follow-up period than children with low-normal weight.
hood obesity and overweight is increasing rapidly in Europe and other parts of the world, being growing epidemic and public health crisis5–7. Childhood obesity and overweight are proved to be associated with several risk factors for later heart diseases and other chronic diseases5. As dental caries, overweight in children is also a multifactorial disease that may include several social and cultural factors. The increased consumption of soft drinks and fast food, together with the modern sedentary lifestyle, has contributed to the increasing number of overweight children worldwide5,8. Low socioeconomic level in terms of living areas could also be related to a higher prevalence of obesity in children9. In addition to that, particular dietary habits could lead to overweight/obesity in children and teenagers, such as choosing food high in fats and refined carbohydrates8,10. Given the causative relation between refined carbohydrates and dental caries11, it is logical to
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hypothesize that high weight might also be a marker for dental caries in children and teenagers or vise versa. Therefore, the purpose of this study was to determine whether the iso-BMI might be associated with dental caries in German school children and to investigate its predictive power for one and a half-year caries increment. Methods
Subjects This is a cross-sectional, prospective study that determines the association between isobody mass index (iso-BMI) and dental caries among German school children, and investigates the prospective caries increment among those children. After the approval of the research and ethics committees of Greifswald University and the Data Protection Commissioner in the Ministry of Education, participants were recruited from the fifth grade of the primary schools in the district of Eastern Pomerania and Greifswald city (North-East Germany, 162 653 inhabitants, unemployment rate 12.7%, drinking water fluoride level 0.2–0.3 ppm) 12. Nineteen of a total of 22 targeted schools consented to take part in this prospective cohort study, comprising a sample of 914 students with an age range from 9 to 12 years. Apart from the compulsory dental school examination, the participation in this study was voluntary, and written informed consent forms were obtained from the parents/legal guardians of the children. The sampling frame consists of all fifth grade students, from all participating schools, whose parents/legal guardians have signed the written informed consent form and who were present at both ‘baseline’ and ‘followup’ examination. Students with any significant systematic disorders were excluded from the study. Clinical examinations Thorough dental and clinical examinations were conducted by three well-trained and calibrated examiners throughout participating
schools. The data were collected in two steps as part of an extended obligatory dental school examination. The baseline data were performed on the fifth grade students from September to October 2007, and the final examination (follow-up) carried out after 19 months on the same children, where they become in the 6th grade, during February and March 2009. Interclass correlation coefficient (ICC) was used to assess the interexaminer reproducibility between examiners in both the baseline and the follow-up examinations. The dental examination was conducted under natural indirect light with additional electric light, using dental mirrors and explorers based on the WHO diagnostic criteria guidelines13. All examinations were conducted with the children in upright positions with the heads tilted back. Caries experience was expressed using the DMFT index (number of decayed, missing, and filled teeth). Teeth or surfaces were considered carious (D) if there was visual evidence of a carious defect. Missing components (M) due to caries, including teeth, indicated for extraction and (F) for filled teeth. Data concerning height and weight of the children were also obtained during the clinical examination day at schools. Body height was measured using a portable stadiometer (Seca; Vogel and Halke, Type: 214, Hamburg, Germany), and the weight was measured using electronic scale (Seca Vogel and Halke, Type: 861). The children were measured without shoes or heavy clothing. Among children and teenagers, body fat changes as the body grows and development differs across gender. Unlike the body mass index (BMI) assessments for adults, assessments for children and teenagers take these growth- and gender-specific patterns differences into account14. The international classification systems for childhood obesity are referred to as ‘iso-BMI’ categories describing overweight and obesity in children, based on gender and pooled international data for body mass index and linked to the widely used adult obesity cutoff values14. This classification encompasses a wide range of acceptance among social scientists and many other authors15,16.
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Using the iso-BMI values, children were categorized with the following cutoff values: lownormal weight = BMI ≤25, overweight = BMI >25–29.9, obesity = BMI ≥3014. Dental and clinical examinations took about 45 min per class with around 25 students per class. Parents additionally answered a self-completion questionnaire containing questions on their socioeconomic status (SES), which were distributed during parent–teacher meetings. The questionnaire was adopted from Lange et al. based on four main factors defining the SES: education, vocational training, net household income, and employment status17. The domains of the questionnaires were compatible with the research tools of another, representative national study, for example, German Health Interview and Examination Survey for Children and Adolescents18.
Whitney U-test and Poisson regression analysis were employed. Poisson regression analyses were conducted for the dependent variables (DMFT and caries increment). The primary independent variable was BMI category. Additionally, age and gender were included in the models as covariates. Poisson regression analyses were conducted for outcomes that are counting data (DMFT, caries increment, and BMI). We also stratified the analysis over three SES categories of high, middle, and low. The incidence rate ratio (IRR) was calculated for the discrete dependent variables to study the effect of independent variables on oral health status. All data were processed and analyzed using SPSS (version 15.0.1) and STATA program (version 10). In all the analyses, the level of statistical significance was set at P < 0.05.
Statistical analysis
Results
During clinical examination, all data were entered directly in Microsoft Office Excel 2003â data bank and then into the SPSSâ software (Statistical Package for the Social Sciences; version 15.0.1; SPSS Inc., Chicago, IL, USA). The questionnaires were automatically scanned with Teleformâ (Version 10.2) and then transferred to SPSSâ. Descriptive analyses using distributions, means, and standard deviations (SDs) were prepared. Then, after dichotomizing several variables (DMFT, caries increment, and isoBMI categories), proportions for each of these variables were calculated. In the subsidiary analyses, the standard iso-BMI categories were used, but the categories overweight and obese were combined in one variable, for a statistical point of view, referred to it in the text as ‘overweight/obese’, and as similarly indicated in the literature10,19–21. These terms were referring to iso-BMI values of >25 kg/ m2. Caries increment in the permanent teeth was calculated by subtracting the DMFT values at baseline examination from that of the final examination (follow-up). For parametric data, chi-squared tests and independent t-tests were used. For the nonparametric data (DMFT and BMI), the Mann–
Baseline examination All of the fifth grade children in the 18 participating schools in the district of East Pomerania and Greifswald city were examined. Of a total 914 students, only 694 students (from 18 schools) were finally included in the study (mean 10.34 years 0.56, 48% females). Reasons for nonresponse were lack of parental interest (18.9%), refusal (1.7%), and moving out of the research region before the questionnaire was distributed (0.1%). In the follow-up period, 4.2% of the students dropped out as they failed to attend either one or both examinations (neutral dropout). In randomly selected students, the ICC values for the first and final examinations were 0.93 and 0.97, respectively. The interpretations of these ICC values give excellent agreements between the examiners in both examinations22. At baseline examination, 76% of the students were low-normal weight (iso-BMI ≤25; n = 525), and 24% were overweight/obese (iso-BMI >25; n = 169). The iso-BMI was significantly associated with gender (P = 0.026). Age was not associated with different iso-BMI categories (P = 0.55), as Table 1 shows below.
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Table 1. Age, gender, and caries experience distribution according to iso-BMI.
Parameters No. of subjects Age in years, Mean (SD) Gender Male% Female% DMFT mean (SD)
Low-normal weight
Overweight/ Obese
P-value
525 (76%) 10.34 (0.55)
169 (24%) 10.37 (0.57)
– 0.545†
259 (72%) 266 (79%) 0.56 (1.18)
100 (28%) 79 (21%) 0.70 (1.19)
0.026*‡ 0.050*‡
†t-test. ‡Chi-square test. *P-value 25) had more caries experience (DMFT indices) compared with low-normal weight individuals (iso-BMI 0), 30% (n = 59) of these children were overweight/obese (BMI >25) compared with only 22% (n = 110) in the caries-free group (DMFT = 0). Statistical analysis using the chi-squared for independence test indicated a significant difference (P = 0.039). Follow-up Almost sixteen percent (n = 106) of the children in the sample study who were free of caries (DMFT = 0) at baseline acquired new carious defects or fillings during the follow-up period. The majority of new lesions in permanent teeth during the follow-up period were located on the first molars (50%). Fourteen percent (n = 74) of the students in the low-normal weight acquired additional carious lesions during the follow-up period, whereas 19% (n = 32) of the overweight/ obese students acquired new carious lesions. Basic Poisson regression (crude) demonstrated a border-line significant association between caries increment and weight status (IRR 1.37, P = 0.055). Gender and age did not have a strong confounding effect when adjusted in the model (Table 2). An interesting significant interaction was observed for the socioeconomic status; therefore, the analysis was stratified by three levels of SES. Among those with high SES, overweight/obesity had four times higher caries risk increment than low-normal weight students (P < 0.001). Adjusting for age and gender did not change the effect. In contrast to this, no statistical significant associations were found in the middle and low SES (P = 0.530 and P = 0.826, respectively). Table 2. Caries increment rate ratio (IRR) from Poisson regression analysis for overweight/obese children in comparison with low-normal weight.
Figure 1. Mean DMFT and DT values among different body mass index groups.
Caries increment
IRR*
95% CI
P-values*
Crude Adjusted for gender Adjusted for age Adjusted for SES Fully adjusted
1.37 1.37 1.35 1.42 1.38
0.99–1.90 0.99–1.89 0.98–1.87 0.99–2.05 0.96–2.00
0.055 0.059 0.069 0.058 0.084
*Data are reported as IRR using Poisson regression analysis.
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Discussion
The findings of this study indicated a significant association between caries experience and different iso-BMI categories among German primary school children in the district of Mecklenburg-Vorpommern. When considering the findings, it should be kept in mind that these findings were based on a cross-sectional design, which facilitates collecting information from large healthy groups of children with more confined age limits. Turning to the follow-up stage of the study, which provided a clear comparison between students’ current and future caries experience, which confirmed the actual relationship between iso-BMI and caries experience. A high prevalence of overweight and obese students was observed in the study population, affecting almost one quarter of the study sample (24%, n = 169). This supports what the WHO described as a ‘global epidemic disease’, where overweight and obesity in fact are an increasing public health problems in Germany and worldwide5,23,24. Our results reflect a previous German study where the prevalence of overweight and obese 6- to 10year-old students was 26%25. Similarly, high numbers were reported for many other European Western countries5,26,27. The multifactorial etiology of obesity and/or overweight includes social and cultural factors. In the literature, a low SES in terms of living area conditions appears to be related to a higher prevalence of obesity9,28. But this study shows that even after adjusting for the SES, the factor ‘overweight/obesity’ was still significantly associated with caries prevalence at baseline and after one and a half-year follow-up. In the high SES group, this association was very pronounced as overweight and obese children in this group showed four times higher caries risk compared to the low-normal weight children. These results are in agreement with a German study in which children with high DMFT indices had significantly higher BMI values than caries-free children29. In this study, caries experience was more pronounced in the overweight/obese group than
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in the normal-underweight group. The overweight/obese group had an average DMFT index of 0.70, compared to 0.56 for the lownormal weight group. After the follow-up period, around 16% (106) of the students acquired new carious lesions. This trend is well described in the literature as the age range of the student during the follow-up period was from 10–12 year old, which is usually associated with an extensive need of dental treatment30. The rest of the students either remained free of caries (DMFT = 0), their caries experience stayed constant or they experienced caries reversals. Caries reversal means that the net sum of caries ended up negatively, and this is a common problem in longitudinal epidemiologic studies of dental caries31. In this study, this problem was taken into account to minimize its occurrence, through presenting all the baseline records at the time of re-examination, so if caries reversals had occurred, a double check with a confirmation would be indicated. A noteworthy observation in this context is that the majority of new lesions in permanent teeth during the follow-up period were located on the first molars (50%). This result confirms previous findings by Mejare et al., [1998]: the most caries-susceptible tooth in the young permanent dentition is the first permanent molar accounting for more than 60% of all restored surfaces32,33. Obesity and dental caries have common ‘risk determinants’ that increase the likelihood of both diseases, such as dietary habits. For example, a sugar-rich diet, including beverages, is associated with various health problems such as obesity, dental caries, and poor diet quality4,34. Therefore, a high sugar intake, especially in drinks, could be a causal factor for caries and overweight/obesity in children, which is still not confirmed in many studies and reviews. Interestingly, the analysis for different socioeconomic levels showed that the overweight/obese students who belong to the high socioeconomic status had four times higher caries risk than low-normal weight students in the same socioeconomic status, whereas no significant difference was found in the middle or low socioeconomic status.
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Definitely, both variables (caries and obesity) are dietary-related cumulative conditions and thus the group who belong to the high SES is more likely to exhibit a stronger relationship, where eating and, especially, drinking patterns vary among this particular category of socioeconomic level35. In a recent study on dental school pediatric clinic, Werner et al. found that a smaller proportion of obese and overweight children presented with more primary tooth caries than low-normal weight children in the mixed dentition24 which is in agreement with our results. They, however, did not find any significant association between SES and overweight/obesity or caries24. Unlike this study, a strong and significant relationship was found between overweight/obese students who belong to the high SES and caries increment compared to low-normal weight students. This association was found only in the high SES groups and not in the middle or low SES. This could be attributed to the different methods of identifying SES and the way that the SES (as a variable) was assessed in the statistical analysis. For example, in the recently mentioned study, the authors depend on patients’ zip codes and their residence addresses as indicators for SES (which is a common method in many American studies)24. This method, however, lacks for sensitivity and specificity particularly if taken on an individual level, and areas of lower and higher SES can exist in every zip code. In this study and others representative studies17,18, the SES was assessed on an individual level based on four main items: family income, parental level of education, vocational training, and employment status. The SES as a single variable may not have a significant confounding effect on the study samples, as found in this study. But stratifying and analyzing the SES in its different levels is an important distinction and may explain differences reported in other study results. In a systematic review by Kantovitz et al.4, the authors concluded conflicting results, showing the need for further well-designed studies to demonstrate the real relationship
between dental caries and obesity. In another recently published study by D’Mello et al., caries experience was assessed in 8-year-old children who were receiving treatment in Otago pediatric dental clinic. The authors found that there was no significant association between BMI and dental caries21. Hilgers et al.30 and Willerhausen et al.20,24, also reported an association between high weight and high caries frequency in children. On the other hand, many other studies did not find a significant association between body weight and dental caries10,36,37. One possible explanation for the understanding of the results is the structure of the German National Health System which includes dental treatment for children at private practitioners of their choice. Children with high SES background and their parents often utilize services more on their own account than families with low SES. During the follow-up period of this study, the overweight/obese students acquired more additional carious lesions than students with low-normal weight with a borderline statistical significance. These results are in agreement with many studies that have suggested that obese children run an increased risk of caries development29,38,39. On the other hand, many other studies have not provided evidence to suggest that overweight children run an increased risk of dental caries10,36,37. The samples of the study were recruited among the community and directly from the targeted study region schools, unlike the clinical samples that will be biased in terms of oral and general health. Because of that, clear skews in caries prevalence and distribution among the samples of the study were noted, representing children with zero-value DMFT index. A non-Gaussian distribution (skewed to the right) was the result, which is a very common distribution in the DMFT and epidemiological studies, particularly in Western developed countries, where DMFT = 0 may count for most of the samples. Therefore, in the statistical analysis, Poisson regressions were used, which took in account such skews and the fact that count outcomes are discrete variables with no negative values.
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Overweight and dental caries
The sample taken from this study only represented the children attending schools in fifth grade at baseline. Thus, the results can only be generalized for this age range. The number of children examined and the response rate, even for the parent questionnaire, were large enough to represent the population attending schools at that age. Considering that the clinical examinations were carried out by three well-trained examiners, the interexaminer reproducibility values for the baseline and follow-up examinations produced excellent agreement (0.93 and 0.97, respectively). The values for the interexaminer reproducibility were within the same range of other studies 40 or even higher than others 41,42 which reported an interexaminer reproducibility of j = 0.90 and 0.85. After discussing the study findings, it is more appropriate to examine the limitations of this study. First, some of the included schools were running a preventive program during the data collection phase of this study. It is important, however, to note that the research questions that suggested earlier were mainly depending on the cross-sectional design of this study. In most of the previously mentioned studies, dental caries recordings were performed by oral examination and diagnosed at cavity level. Only one study diagnosed proximal caries including initial caries lesions using bitewing radiographs38. In Germany, however, such a procedure could cause a particular difficulty during ethical committee review, especially in health preventive studies. The findings of this study are also meant to be used in future preventive programs. In conclusion, this study showed a strong association between iso-BMI and dental caries prevalence. The association between caries increment and iso-BMI, however, failed to reach a statistically significant level after 1 year and half at follow-up. Knowledge of these relationships could reorient health policies and guidelines to incorporate dentists in multidisciplinary medical teams to promote oral health in conjunction with general health and healthy diet. This integrated approach is likely to be more cost-effective, and a major benefit could be gained by focusing on improving the general health condi-
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tions for the whole population, particularly groups with high risk. These characteristics could also be used in adjunct to other factors to identify children at risk of developing caries early and used to target preventive dental care for those children in advance. Acknowledegment
The authors would like to acknowledge and thank the high cooperation of the parents, schools, and children who agreed to participate in the study. Conflict of interest
The authors declare that they have no conflict of interest.
Why this paper is important to pediatric dentists? ● These results highlight the important role of pediatric dentists to identify and to reduce the risk of childhood obesity as well as dental caries. ● Preventive and pediatric dentistry departments should participate in any multidisciplinary health-promoting programs to promote a healthy diet and general health not only to prevent dental caries but also to reduce the risk factors for overweight and obesity in children.
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