Community Dent Oral Epidemiol 2014; 42; 5360 All rights reserved

2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Association between body mass index and caries among children and adolescents
Lempert SM, Froberg K, Christensen LB, Kristensen PL, Heitmann BL. Association between body mass index and caries among children and adolescents. Community Dent Oral Epidemiol 2014; 42: 5360. 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Abstract Objective: The aim of this article was to examine the relationship between childhood caries, body mass index (BMI) and subsequent changes in BMI over 6 years, and to investigate whether these associations were modied by social class. Methods: Data were from the European Youth Heart Study (EYHS) merged with data on caries experience from the Danish National Board of Health, (SCOR register). Results: At baseline, 26.2% of the children/ adolescents were caries free and 39% at follow-up. A larger percentage of normal weight children/adolescents were caries free, compared with the overweight/obese group of children/adolescents. The linear regression analysis showed that childhood caries was generally not associated with either BMI or subsequent changes in BMI. However, among children whose mothers were well educated, there was an inverse association between caries at baseline and subsequent changes in BMI over a period of 6 years, for example, a high caries experience was associated with a smaller increment in BMI, compared with the group of children with a low caries experience. No association was found for those with lower SES. Conclusion: An inverse association between caries and subsequent changes in BMI was found, but only among children with well-educated mothers, suggesting that high caries experience may be a marker for low future risk of overweight among the more advantaged. Associations did not appear to be signicant among the less advantaged; however, numbers in this group were low, and an association may have been overlooked. Hence, more studies are needed to conrm these ndings.

Susanne M. Lempert1, Karsten Froberg3, Lisa B. Christensen4, Peter L. Kristensen3 and Berit L. Heitmann1,2
National Institute of Public Health, University of Southern Denmark, Copenhagen, Denmark, 2Institute of Preventive Medicine, Bispebjerg and Frederiksberg Hospital, Copenhagen University Hospital, The Capital Region, Denmark, 3Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark, Odense, Denmark, 4 Institute of Odontology, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
1

Key words: childhood; BMI; caries; EYHS; SES; SCOR Susanne Merethe Lempert, National Institute of Public Health, University of Southern Denmark, ster Farimagsgade 5 A, 2.sal, 1353 Copenhagen, Denmark e-mail: slempert@niph.dk Submitted 11 February 2013; accepted 11 May 2013

Childhood obesity is a rapidly increasing serious public health problem worldwide (14). The risk of obesity persisting into adult life is higher with more severe overweight and obesity; hence, the most concerning increase in childhood obesity is at the upper extreme of the BMI distribution (1, 311). While overweight and obesity in children has been increasing over the past couple of decades, while dental caries, another chronic disease, has decreased markedly over the last 20 years in most countries in the Western world (1214). There has been growing interest in the relationship between dental caries and childhood/adolesdoi: 10.1111/cdoe.12055

cent overweight/obesity, but the results from previous studies are inconclusive (1538). Childhood/adolescent overweight/obesity and caries are both multifactorial diseases that coexist in many populations (21). The association between dental caries and obesity is not a causal relation, but might coexist in a population because of a clustering of the same contributing factors, including genetic, socioeconomic, cultural, sugar intake, environmental, and lifestyle issues (7, 3440). The challenge in exploring the relationship lies in measuring possible confounders or effect modiers (37).

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It is generally agreed that prevention is more effective than treatment as means of reversing current secular trends in, for example, obesity (1, 9). In this regard, the dental professionals might be able to prole children at future risk for developing obesity, and, in the dental setting, to approach parents about the childs diet in relation to his or her dental health as well as general health. The aim of this article was to investigate associations between BMI and caries and to examine if caries experience can represent a marker of subsequent development in body fatness. Furthermore, the aim was to examine whether these associations differed between subjects from different socioeconomic levels.

Study population
The study population consisted of 385 children (207 girls and 178 boys) on whom we had complete information on dietary intake and anthropometric and dental measures at baseline, and 280 children (153 girls and 127 boys) at follow-up (Fig. 1). The study design, sampling, and methods have been described more detailed elsewhere (41, 42). Baseline examinations were conducted from 1997 to 1998 and follow-up from 2003 to 2004. Information on nonresponders, from the participating schools, were collected, and no signicant difference between responders and nonresponders regarding age, mean BMI, mean height, mean weight, and mean caries experience was found, which indicates that the dropout is not selective.

Measurements

Materials and methods

Study design
European Youth Heart Study (EYHS) is a multicenter, cross-cultural prospective study of the associations between lifestyle and cardiovascular disease (CVD) risk factors among children and adolescents. This study used data from the Danish part of EYHS and data from The National Board of Healths Recording System for the Danish Child Dental Services (SCOR). The study is school based, and schools in the municipality of Odense, Denmark, were stratied according to school type (age range, selection procedures), location (urban, suburban, rural), and socioeconomic status of the uptake area (41). Each school was allocated a weighted equivalent to the number of children enrolled in the school who were eligible for selection into the study. Three replacement schools were sampled to substitute schools refusing to participate and to act as reserves in case of low response rates. Children within 810 and 14 16 years of age were allocated code numbers and randomly selected using random number tables (41). A total of 35 schools were randomly sampled, of which 25(71%) agreed to participate. Three of these schools were lost to follow-up: one was rural, one was urban from a middle class area, and one was urban from a low-income area. All 3 schools gave interference with the educational process as reason for the drop out. The study was approved by the local ethics committee and performed according to the Helsinki Declaration. All children gave verbal consent, and their parents gave written consent (41).

Body height was measured to the nearest 5 mm using a stadiometer and body weight was measured to the nearest 0.1 kg using a beam-scale weight, with the participants lightly dressed (underwear or t-shirt, no shoes) (42). Measures used are as follows: (i) BMI and (ii) BMIz, a measure of pediatric and adolescent under- or overweight, taking sex-, age- and growth-specic considerations into account (43). In the present study, we applied national reference z-scores to the study population under examination. Syntax was received with equations for calculating L, M, and S values based on large national population cohorts. The obtained equations were merged to the present data, and z-scores were generated (44). Test variables (outcome) were BMI and changes in BMI (DBMI), where changes in BMI were dened as the differences in BMI values between follow-up and baseline, changes in BMIz (DBMIz) were dened as the differences in BMIz between follow-up and baseline. Test variables were used as continuous variables, and BMI cut-off points were age adjusted.

Fig. 1. European Youth Heart Study (EYHS), participation owchart.

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Caries experience was recorded from the SCOR database. SCOR data used for this investigation were collected in 1997 (baseline) and 2003 (followup). The data were collected by dentists in the Municipality of Odense. Children were recalled for visits regularly, and standardized dental examinations were performed for registration of oral health status; these examinations include X-rays when the dentist found it was indicated. Caries was recorded at cavity level, in both the primary and the permanent dentition. Explanatory variable (exposure) was caries experience. Caries experience was included as the sum of decayed, missing, and lled surfaces, in the primary and the permanent dentition (dmfs/DMFS). Caries-free children are dened as children with no prior caries experience. Caries was used as a continuous variable. Parents socioeconomic status was based on information on educational level and income obtained through questionnaires. The variables mothers and fathers educational level were recoded into binary variables, one category including a maximum of 10 years of elementary school or a vocational education and the second category including high school diploma or education above this level. Mothers and fathers income levels were recorded into three levels. These variables were used as ordinal variables. Information on dietary intake was obtained by a 24-hour dietary recall method, which was supported by a qualitative food record and food frequency questionnaire (FFQ). The 24-hour dietary recall record concerns the type and amount of food and drinks taken during the previous day and a description of the food in macro nutrients. The parents of the participants lled in a qualitative food record on food and drinks consumed, a description of the food and where the food was consumed. Afterward, this information on dietary intake was computed into a database, from which nutrient intake from single food items, whole meals, or the entire diet was calculated using national food composition tables. The use of the 24-hour recall in children has been validated in a subsample against a 4-day weighed food intake, and a validation with doubly labeled water was performed on a smaller subsample (42, 45). The co-variates were included as possible confounders or mediators: Total energy intake measured in MJ/day as a continuous variable. Total intake of sugar was dened as all monosaccharide and disaccharides in the diet. Intake of sugar was

used as continuous variable. Intake of carbohydrates was recoded by subtracting the total content of sugar (gram) from the total intake of carbohydrates. Carbohydrate was used as continuous variable. Frequency of soft drink/sweet intake was recoded into a binary variable. Ethnicity was used as a categorical variable. Puberty was measured according to Tanner stadia. The person assessing puberty stage was the same gender as the child (42). Tanner stadia were used as an ordinal variable. Gender was used as a categorical binary variable.

Statistics
The statistical analysis was performed in SPSS 16.0 (SPSS Inc., Chicago, IL, USA) for Windows. All variables were tested by the ShapiroWilk test for normality. Differences between groups including categorical variables were tested by means of a Chi-square test (46). Data were analyzed stepwise using simple and multiple linear regression analyses (GLM) (46). First, a basic linear regression analysis was conducted with only the test and explanatory variables included in the basic model; secondly, four models were examined using multiple linear regression analyses: Model 1 adjusted for outcome-specic co-variates: Age, Tanner stadia, gender, and ethnicity. Model 2 adjusted for outcome-specic co-variates: Age, Tanner stadia, gender, ethnicity, total energy intake, total intake of complex carbohydrates, total intake of sugar, and frequency of soft drink intake. Model 3 included interaction variables, parental education, and parental income, in addition to variables from Model 2. Model 4 adjusted for outcome-specic co-variates: Age, Tanner stadia, gender, ethnicity, total intake of sugar, frequency of soft drink intake, and mothers education. A P-value of 0.05 was chosen as cut-off for significance. Cluster sampling may cause inated P-values; thus, school codes were included in all models to control for this effect. All residuals were tested for normal distribution by performing QQ plots.

Results
Table 1 gives the distribution of anthropometric and caries variables at baseline and follow-up by

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Lempert et al. Table 1. Baseline and follow-up distribution of age, BMI, BMIz, height, weight and caries by gender Baseline Age (years) BMI (kg/m2) BMIz Height (cm) Weight (kg) Caries (dmfs/DMFS) Follow-up Age (years) BMI (kg/m2) BMIz Height (cm) Weight (kg) Caries (dmfs/DMFS) Girls (n = 207) Mean SD 9.6 17.1 0.3 138.9 33.2 5.8 0.3 2.4 1.1 6.1 6.1 6.8 Min. 8.8 12.6 2.8 122.0 21.3 0.0 Max. 10.3 27.3 3.1 156.0 56.5 45 Boys (n = 178) Mean SD 9.6 17.2 0.4 139.2 33.4 6.8 0.4 2.1 1.1 6.2 5.5 7.3 Min. 8.7 13.0 2.8 121.2 20.3 0.0 Max. 10.3 25.7 3.5 158.8 56.8 34

Girls (n = 153) 15.7 21.2 0.4 165.8 58.3 2.5 0.3 2.9 0.9 6.5 9.2 3.8 15.0 16.3 1.8 146.5 39.3 0.0 16.3 37.3 3.4 186.0 107.7 21.0

Boys (n = 127) 15.7 21.2 0.6 176.5 65.9 3.3 0.3 2.7 1.0 7.1 10.1 4.3 14.9 16.8 1.5 156.5 41.6 0.0 16.2 30.1 2.9 194 94.8 26.0

gender. The decrease in caries experience observed between baseline and follow-up is not a true decrease but an artifact due to tooth exfoliation from the mixed dentition. No signicant differences between girls and boys regarding age, mean BMI, mean BMIz, mean weight, or mean caries experience were observed. The percentage of caries-free (dmfs/DMFS = 0) children/adolescents was lower in the overweight/obese group compared with the normal weight group, illustrated in Fig. 2. At baseline, 86.2% of the children were normal weight, whereas 13.8% were overweight/obese. This distribution, remained stable during follow-up, and the corresponding numbers at follow-up are 86.1% for the normal weight children and 13.9% for the overweight/obese children. In total, 89 of the normal weight children/adolescents were caries free at baseline and 99 at the follow-up examination. The corresponding numbers for the overweight/obese group were that 12 were caries free at baseline and 13 at the follow-up examination. Children/

adolescents, who were overweight/obese at the baseline examination, had a tendency towards a higher mean caries experience than the normal weight children. However, this difference was not statistically signicant, possibly because of lack of power (data not shown). The results from the linear regression analysis showed that caries experience, neither at baseline nor at follow-up, was associated with BMI or BMIz. The results remained non-signicant after adjustment for outcome-specic co-variates as shown in Table 2. The association between caries experience and body fatness remained virtually unchanged after the stepwise inclusion of total energy intake, total carbohydrate intake, total sugar intake, or intake frequency of soft drinks. Same results were found after the inclusion of parental education and parental income as co-variates.
Table 2. Linear regression analyses of associations between caries experience (dmfs/DMFS) and body fatness Model 1 Basic (n = 385) SE 0.020 0.008 0.017 0.008 Model 1a (n = 373) b SE 0.012 0.005 0.018 0.008

Baseline BMI (kg/m2) BMIz Follow-up BMI (kg/m2) BMIZ DBMI (kg/m2) DBMIz Fig. 2. Association between % of caries free children and BMI.

P 0.25 0.31

P 0.50 0.60

Basic (n = 280) 0.016 0.044 0.71 0.006 0.004 0.002 0.015 0.017 0.006 0.72 0.81 0.77

Model 1a (n = 233) 0.019 0.052 0.71 0.007 0.022 0.010 0.018 0.020 0.007 0.69 0.25 0.18

a Adjusted for outcome-specic covariates, age, Tanner stadia, gender and ethnicity.

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Caries experience at baseline was not associated with subsequent changes in BMI or BMIz. The result remained nonsignicant after adjustment for outcome-specic co-variates, and after inclusion of total energy intake, total carbohydrate intake, total sugar intake, frequency of soft drink, parental education, or parental income (data not shown). A statistically signicant interaction between mothers educational level and childrens/adolescents caries experience at baseline, in relation to 6 year changes in BMI, was found (P = 0.02) (Table 3). Interaction variables such as fathers educational level/caries or parents income/caries were not statistically signicant (data not shown). Stratifying according to mothers educational level, with one group consisting of mothers holding a high school diploma or above and a second group consisting of mothers with a maximum of 10 years school experience, revealed that a low caries experience predicted larger body weight increment, for children where mothers were more educated. Among those with less-educated mothers, the association was not statistically signicant, but showed a tendency toward a direct relation between caries experience and weight development. Hence in this group the data suggested that, a high caries experience is associated with a larger subsequent increment in body weight.

Discussion
This article examined whether caries experience was associated with subsequent development of body fatness, and whether associations differed with socioeconomic status. We found no general statistically signicant association between caries experience and subsequent development of body fatness in this study population. However, among those children/adolescents, who came from more

advantaged families, where the socioeconomic status of the mother was high we surprisingly found that, a high caries experience was related to a smaller subsequent weight increment. This result was surprising as overweight, obesity, and high caries prevalence are all regarded to be related to low SES and hence would be expected to be directly rather than inversely associated (3, 8, 9, 19, 25, 33, 36, 38, 4750). Such a direct relationship was found among the children and adolescents with the lesseducated mothers; however, these associations were not signicant. To our knowledge, this article is the rst to address an association between previous caries experience and later development in BMI for children from advantaged and more disadvantaged family backgrounds. An explanation for the inverse association might be that severe dental caries, especially in young children, may affect growth in an adverse manner (25, 33, 51, 52), although clearly this may apply to height only, and not BMI. In addition, it has been shown that children, from non-poor households, with poor dietary habits are more likely to experience caries in their primary teeth compared with poor children (48). Indeed, it may be speculated that the high caries experience among the more advantaged may have led to a subsequent reduction in sugar intake, which then may have resulted in less weight gain. Furthermore, the dietary methods may not even be accurate enough to detect such changes in the intake of free sugars. Likewise, it is possible that among those with lower-educated mothers, there was no such change in diet in response to high caries levels. However, the association between caries and subsequent gain in BMI among the more disadvantaged did not reach statistical signicance. It cannot be eliminated that this lack of signicance may have been due to lack of power, as only 83 children

Table 3. Linear regression analyses of associations between caries experience and changes in body fatness over a period of 6 years stratied according to mothers educational level Model 4 All (n = 216)a DBMI (kg/m ) DBMI2
2 a

SE 0.023 0.008

P 0.30 0.20

Low education (n = 83)a+b SE 0.064 0.019 0.057 0.020

P 0.27 0.35

High education (n = 133)a+c SE 0.059 0.023 0.024 0.009

P 0.02 0.01

0.023 0.010

Adjusted for outcome-specic co-variates, total sugar intake, frequency of soft drink intake, mothers education, age, Tanner stadia, gender and ethnicity. b Adjusted for the co-variates above and stratied according to 10 years of school education and/or a vocational education. c Adjusted for 1 and stratied according to High school diploma or above.

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belonged to this group. The fact that SES had an impact on health outcomes such as obesity and caries is well documented in the literature (3, 9, 36, 47, 48, 53). However, the nding that mothers educational level had a greater inuence on the association between caries and changes in BMI, than fathers educational level, may indicate that mothers still are the primary cares in these families. In the data examined for this article, a larger percentage of normal weight children/adolescents were caries free compared with the overweight/ obese children/adolescents, indicating an association between obesity and caries, although the results were not statistically signicant. The general lack of signicant associations may relate to the fact that the study population was undergoing tooth exfoliation, transition from primary to permanent dentition, which with a delayed disease development due to uoride or ssure sealants, may have altered the association. Further, the exfoliation might have occurred more rapidly in the overweight/obese group (16, 40). Indeed, time of eruption or number of erupted teeth might bias the results and should be controlled for. However, this was not carried out in the present paper, as the information was not available. At the follow-up examination, transition from primary to permanent teeth had occurred, which, combined with retardation of disease development from uoride, may result in that a more extended cariogenic exposure time is needed to detect caries in the oral cavity. The use of oral X-rays for detecting the early stages of caries lesions might therefore be a useful tool when examining the relationship between BMI and caries in a population with mixed or permanent dentition. In accordance, previous cross-sectional studies included X-rays to diagnose proximal caries, found a signicant positive association between BMI and caries (29). However, in the present investigation, X-rays were not included as a standard, and the resulting underestimation of disease might have attenuated the magnitude of correlation between dental caries and BMI in the present study. Conversely, the result that overweight/obese children had a lower mean caries experience than their normal weight counterparts also nds some support in the literature (16, 18, 25, 28, 33). Our results are inconclusive regarding whether the correlation was weak per se or whether residual confounding factors attenuated the association. However, it may be argued that an organized dental care system, such as that in Denmark, the relatively high level of uoride in the drinking

water and regular use of topical uoride may weaken the association between body fatness and caries (13). Finally, a relationship between change in dental caries and change in body weight may have been expected from the present ndings, as such an association is likely if the two conditions have common risk factors. However, this could not be examined in this study due to the tooth exfoliation from the mixed dentition, that would have created false decreases in caries experience. Our nding may have several clinical implications. First, oral health professionals see patients for routine visits frequently and are therefore in a unique position to screen children/adolescents and refer those at increased risk of overweight/ obesity to a physician, school health nurse, or dietician (54, 55). Dentists may promote the intake of a healthy diet to their patients, not only to prevent dental caries but also to reduce the risk of overweight/obesity. Based on the concept that diet, and in particular sugar, contributes to development of dental caries and overweight, dental personnel have been suggested to be one of the cornerstones in weight counselling (27). Secondly, exploring the role of the dentist as screener and active member of overweight policy, presents a novel area for future research and practice. Given the evidence supporting the association of dental caries with irregular dietary patterns, such as a high frequency of food intake, and the fact that irregular dietary intake might be linked to the development of obesity at a young age, a link between caries and weight is biologically plausible (30). The challenge in exploring this relationship lies in measuring possible confounders or effect modiers in a standardized and comprehensive manner (37). Also, limitations should be noted: Both overweight/obesity and caries are conditions with multifactorial causes which can be inuenced by several factors. Therefore, the possibility of residual confounding may always be present. The 24-hour recall method used to obtain dietary information is limited by the fact that a single day of intake may not be representative of usual daily intake. Hence, residual confounding may have been present. Caries scores were obtained at regular dental checkups which limits the risk of selection bias. The criteria for the recording of oral health are dened by the National Board of Health, so the scores are obtained using the same guidelines limiting interobserver differences and limiting the

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introduction of a systematical bias. However, the data on caries are still limited; for example, dmfs/ DMFS indices are inadequate for measuring new decay in teeth, or surfaces which have already been restored. Also, the fact that only aggregated data for the primary and permanent dentition were used, might result in dilution of the examined relationship (13). Additionally, the records for the national register on dental health are obtained at age 5, 7, 12, and 15 years only. Furthermore, the SCOR data registration is made by a large number of dentists, and even among experienced dentists, caries diagnoses are subjective and most likely to be underestimated. Nevertheless, the underlying data are considered to be of acceptable validity and reliability (56).

Conclusions
Previous caries experience may be a predictor for future risk of developing overweight and obesity. This relationship, however, seems dependent on the socioeconomic position and educational level of the mother and our results suggest that a high caries experience may be a marker for low future risk of obesity among children and adolescents with well-educated mothers. However, more studies are needed to conrm these ndings.

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26. 27.

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46. 47. 48. 49.

32. 33.

34. 35.

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52. 53. 54. 55. 56.

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60