Matern Child Health J DOI 10.1007/s10995-015-1854-3
Relationship Between Dietary Sugar Intake and Dental Caries Among Japanese Preschool Children with Relatively Low Sugar Intake (Japan Nursery School SHOKUIKU Study): A Nationwide Cross-Sectional Study Miyuki Saido1 • Keiko Asakura1,2 • Shizuko Masayasu3 • Satoshi Sasaki1
Ó Springer Science+Business Media New York 2015
Abstract Objectives The WHO has recently proposed to halve the recommendation for free sugar intake from 10 to 5 % of energy intake to reduce the incidence of diseases such as obesity and dental caries. The Japanese population is suitable to confirm the appropriateness of this proposal, because dietary sugar intake in Japan is exceptionally low among developed countries. We sought to establish a method to estimate dietary sugar intake in Japan and to examine the relationship between sugar and the number of dental caries using data obtained from the Japan Nursery School SHOKUIKU study. Methods Dietary intake during the preceding month and the number of caries was examined in children aged 5–6 years using a brief-type self-administered diet history questionnaire for Japanese preschool children completed by their guardians and another questionnaire on lifestyle. Multivariate Poisson regression models were used for the analysis. Results When subjects were ranked into quintiles by the proportion of energy from free sugar, those in higher quintiles had more caries than those in the lowest & Satoshi Sasaki [email protected] Miyuki Saido [email protected] Keiko Asakura [email protected] Shizuko Masayasu [email protected] 1
Department of Social and Preventive Epidemiology, School of Public Health, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
2
Interfaculty Initiative in Information Studies, The University of Tokyo, Tokyo, Japan
3
Ikurien Special Nursing Home for the Elderly, Ibaragi, Japan
quintile. On close analysis, the number of caries among children with a relatively small proportion of energy intake from free sugar (3.18–3.77 %) was not significantly different from that in the lowest group (0.95–3.17 %). Conclusions The recent proposition of WHO might be valid, because the adverse effect of relatively small proportion (approximately less than 5 %) of energy intake from free sugar on caries was not detected among the subjects in this study. However, more study will be necessary to reach a conclusion. Keywords Dental caries Sugar intake Preschool children Prevention Japan
Significance There is evidence of moderate quality showing that incidence of dental caries is lower when the intake of free sugar is \10 % of total energy intake per day, but effect of more reduction (\5 % of total energy intake) of free sugar is still unclear. Our study showed that lower energy intake from free sugar, at approximately less than 5 % of total energy intake per day, did not increase the number of dental caries among preschool children in Japan. The intake of free sugars between 5 to 10 % of total energy intake possibly increased the number of dental caries.
Background Dental caries is the most common disease affecting preschool (under 5 years old) and elementary school children (6–11 years old) in Japan [1]. More than 40 % of 5-yearold children are reported to experience dental caries [1]. Dental caries can cause pain and discomfort in children and
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lead to an unbalanced diet. Thus, prevention of caries in childhood is an urgent issue. Reduction of dietary sugar intake is known as an important strategy in preventing caries. To reduce the incidence of health problems such as obesity and dental caries, the WHO has recently proposed halving the recommended free sugar (sugars include monosaccharides and disaccharides added to foods and beverages by the manufacturer, cook or consumer, and sugars naturally present in honey, syrups, fruit juices and fruit juice concentrates) intake, from 10 % of daily energy intake to 5 % [2]. However, the appropriateness of this new recommendation has been difficult to examine in developed countries, because sugar consumption by these populations, particularly among preschool children, is substantially above the WHO recommendation [3]. Japan is exceptional in this regard, with a relatively high income but low consumption of sugar (food supply of sugar and other sweeteners such as fructose syrup in 2011: Japan, 76; USA, 165; UK, 107 (g per capita per day) [4]. This low consumption makes Japan a suitable venue in which to examine the appropriateness of the WHO proposal. Despite this advantage, almost all epidemiological studies to investigate the association between dietary sugar intake and the number of dental caries in Japanese population are the ecological studies [5]. In addition, almost no quantitative and population based assessment of dietary intake of sugar has been conducted in Japan. Among the few studies that have investigated the relationship between dietary sugar intake and the number of dental caries in Japanese populations [6, 7], one measured only the frequency of sweets intake per week instead of sugar intake [6] and a second excluded non-staple foods, fruits, and juice from measurement [7]. The Standard Tables of Food Composition in Japan do not provide the sugar content of foods and beverages [8]. This lack has hindered investigations of daily dietary sugar intake in Japanese populations and prevented evaluation of the influence of characteristic low sugar intake on health. In this study, we developed a method to estimate the dietary intake of free sugar using a diet history questionnaire for Japanese preschool children. We then examined the relationship between dental caries and lifestyle factors, including dietary intake, using data obtained from the Japan Nursery School SHOKUIKU Study. We particularly focused on the relationship between low-range free sugar intake (\5 % of total energy intake per day) and dental caries.
Methods Study Setting and Participants Participants in the Japan Nursery School SHOKUIKU Study were recruited from 44 of the 47 prefectures in
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Japan. Initially, representative dietitians of councils of prefectural welfare facility dietitians at local branches of the Japan Dietetic Association and staff dietitians in municipal child welfare facilities were invited to participate. The representative and staff dietitians or nursery governesses in 416 of 437 invited nurseries agreed to participate. These then recruited the study subjects from guardians of children aged 5 or 6 years at their nursery school. Two questionnaires, one about the child’s general lifestyle and the second assessing the child’s dietary intake, were distributed to 9762 guardians and collected between February and March in 2011. Guardians were requested to complete the questionnaire with hearing from their children about what they have eaten out of home. A total of 5634 responded to the lifestyle questionnaire (response rate: 58 %) and 6257 to the diet history questionnaire (64 %). The two data sets for lifestyle and dietary intake were then merged (N = 6383: participants who submitted at least one questionnaire, either lifestyle or diet history questionnaire, or both). Children with missing values for key questions such as family structure, sex, brushing habit in the morning, or educational background of mother, and those whose guardian answered ‘‘I don’t know’’ or who had missing data for the number of guardians-reported decayed or filled caries (abbreviated as ‘‘reported caries’’ hereafter) were excluded, leaving 5244 children in the merged dataset. We then further excluded children with outliers those whose weight at birth was \100 g, height at the time of survey was 85 cm or under or 150 cm or over, or with energy intake \500 or 3000 kcal and over from the dataset, leaving 5217 children. Further, children who were receiving diet therapy was excluded, finally 5158 children were analyzed (Fig. 1). Dietary Assessment Dietary intake data of the children during the preceding month was collected using a brief-type self-administered diet history questionnaire for Japanese preschool children (BDHQ3y). The BDHQ3y is a four-page structured questionnaire that inquires about the consumption frequency of selected foods commonly consumed in Japan, general dietary behavior and usual cooking methods. It was developed based on comprehensive (16 pages) [9, 10] and brief (four pages) [11, 12] versions of a validated selfadministered diet history questionnaire for adults. Estimates of daily intake of foods (66 items in total), energy, and selected nutrients derived from those foods were calculated using an ad hoc computer algorithm for the BDHQ3y based on the Standard Tables of Food Composition in Japan [8]. In the BDHQ3y, fixed portion sizes were used for the children at the same age in month to calculate dietary intake [13]. Values of nutrient intake were
Matern Child Health J Fig. 1 Flow chart of inclusion and exclusion criteria of the study
Lifestyle quesonnaire (n=5634)
Diet history quesonnaire (n=6257) Excluding missing values
n=6383
Missing values for family structure (n=749) and sex
(n=122)
Missing data for brushing habit in the morning (n=10), educaonal background of mother (n=104) Missing data or who answered “I don’t know”
n=5244
for number of dental caries (n=154) Excluding outliers Outliers for body weight at birth (n=4) Energy intake 3000 kcal (n=23)
n=5217
Body height 85 cm or 150 cm (n=0)
Excluding children under unusual condion Under diet therapy (n=59)
Analyzed children (n=5158)
energy-adjusted using the density method (percentage of energy for energy-providing nutrients and amount per 4184 kJ (1000 kcal) of energy for other nutrients). The BDHQ3y also elicited information on the child’s weight and height. Body mass index (BMI) was calculated by dividing body weight (kg) by the square of height (m2) reported by the guardian. The BDHQ3y also collected information on date of birth, sex, physical activity level, number of reported caries, and implementation of diet therapy supervised by a doctor or dietitian. Sugar Intake Estimation Because construction of the BDHQ3y was based on the Standard Tables of Food Composition in Japan [8], which does not include values for the sugar content, we were unable to estimate sugar contents directly. Instead, we developed composition tables for three types of sugar (sucrose, glucose and fructose) for 74 of the 119 items used in the nutritional value calculations of the BDHQ3y. These 74 items were selected if residual carbohydrate content after subtraction of dietary fiber content was 5 g or more per 100 g of total food (drink) weight in the Standard Tables of Food Composition in Japan. As an exception, ‘‘mix juice’’ (vegetable juice) was included regardless of residual weight. Although residual weight for mixed juice in the food composition table is \5 g [8], labeled weight for the recent best-seller vegetable juice in Japan is far
higher than 5 g (14.9 g) per 100 g. Data for sugar content were collected as described in Fig. 2. Dental Caries The BDHQ3y also includes a multiple-choice question asking the guardians about the number of dental caries including decayed or filled teeth of their children, with six answer choices (‘‘the number of dental caries including decayed or filled teeth’’ = ‘‘0’’, ‘‘1–2’’, ‘‘3–5’’, ‘‘6–9’’, ‘‘10 and more’’, and ‘‘I don’t know’’). In this study, we used the five numbered categories and excluded subjects who responded ‘‘I don’t know’’. We assigned the median value of each category as the representative dental caries’ number for each category (0 for ‘‘0’’ category, 1 for ‘‘1–2’’, 4 for ‘‘3–5’’, 7 for ‘‘6–9’’). For the ‘‘10 and more’’ category, we used the median value between 10 and 16, namely 13, because 16 was the maximum number of decayed and filled primary teeth among children aged 3–5 in a government research program [14]. Other Variables Information about the general lifestyle of children was collected using a four-page questionnaire designed for this study. In this questionnaire, the guardians reported family structure, chronic conditions of the child requiring dietary restriction, sleeping time of the child, educational
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Matern Child Health J Fig. 2 Data collection of sugar content of the foods and drinks
ەWhen sugar analysis for a certain food or drink in the BDHQ3y were available from …
ձSingle arcle The value of the arcle was assigned as sugar content. *Informaon sources that met these criteria were two governmental reports (abbreviated as “Report 1” (33) and “Report 2” (34) hereaer), as well as two papers (35-37) and three books (3840).
ղMulple arcles •When those arcles included either of the governmental reports (Reports 1 and 2), the values in them were given priority. •When one item was reported in both of these reports, the values in Report 2 was used, because this is the more comprehensive and recent of the two. •When food was not included in these two governmental reports, values for which the measurement method was most clearly described (31, 37-40) was adopted.
ճNo reliable arcles The following esmaon methods were used. •Bread and noodles: the sugar content of ingredients reported in “Report 1” and the Standard Tables of Food Composion in Japan (33) were summed to esmate the sugar content in the product. •Jam: Since the amount of carbohydrate in jam reported in the Standard Tables of Food Composion in Japan was thought to include sugar and fiber, fiber content was subtracted from carbohydrate content and the residual carbohydrate value was used as sugar content. • Potato chips and French fries: The sugar content of raw potato reported in “Report 1” was used as the sugar content of these foods. • Other foods such as mixed juice, tomato juice, ketchup and soy source: the product having the top market share in its category was idenfied using POS (point of sales) data between April 2009 and March 2010 (31). Then, the sugar content shown in the website of the product was used. When sugar content was not provided, dietary fiber content was subtracted from carbohydrate content and the residual carbohydrate content was regarded as the sugar content.
background of the parents, and weekly frequency of teeth brushing of the child in the morning and evening. Statistical Analysis The associations between dental caries and a number of lifestyle factors including dietary intake were examined. First, basic characteristics were compared between children with and without reported caries using the t test and Chi square test. Dietary intakes were then categorized into quintile points based on distribution, and crude and multivariable adjusted ratios of the mean number of reported caries and 95 % confidence intervals for each quintile category compared to the lowest category of the dietary variable were calculated using a Poisson regression model. With regard to sugar intake, we investigated the association between caries and the proportion of energy intake from free sugar in total energy intake per day. In addition, to examine the effect of the relatively small proportion of energy intake from free sugar on dental caries, we divided each quintile of energy proportion into five further groups (G1–G25; 25 groups in total), and used the same multivariate Poisson regression model. We selected lifestyle factors for inclusion in the model as possible confounding factors by comparing the basic
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characteristics of children with and without reported caries. Among variables which were statistically significantly different (p \ 0.05), educational background of the mother, frequency of brushing in the morning, frequency of brushing in the evening, and residential area were included in the model. Educational background of the father was excluded to avoid decreasing sample size, as there were 600 participants with missing value for father’s education. Mother’s educational background is supposed to be enough as a covariate to adjust the effect of parents’ educational level, because mothers generally spend more time in childraising than fathers in Japan [15], so the mother’s knowledge of health and diet should more strongly affect the child’s health status than the father’s knowledge. Although sleeping time also significantly differed, it was excluded because the mean difference was only 3 min. All statistical analyses were performed using SAS statistical software (version 9.3, 2011, SAS Institute Inc., Cary, NC, USA). A two-sided p value of \0.05 was considered statistically significant. Ethical Considerations The study protocol was approved by the Ethics Committee of the Japanese Society of Nutrition and Dietetics
Matern Child Health J Table 1 Characteristics of subjects Variables
n (%) or mean ± SD
p value
All children (n = 5158)
Children with reported cariesa (n = 2686)b
Children without reported cariesa (n = 2472)b
6.76 ± 0.42
6.78 ± 0.42
6.75 ± 0.43
0.02c
5
381 (7.4)
178 (6.6)
203 (8.2)
0.03d
6
4777 (92.6)
2508 (93.4)
2269 (91.8)
Age (years)
0.93d
Sex Male
2732 (53.0)
1421 (52.9)
Female
2426 (47.0)
1265 (47.1)
1161 (47.0)
Height (cm)
115.2 ± 5.4
115.1 ± 5.5
115.3 ± 5.4
0.23c
Weight (kg)
20.6 ± 3.2
20.6 ± 3.3
20.7 ± 3.1
0.39c
15.5 ± 1.8
15.5 ± 1.8
15.5 ± 1.7
0.87c
-2
BMI (kg m )
1311 (53.0)
\0.01d
Residence area Hokkaido and Tohoku
686 (13.3)
362 (13.5)
324 (13.1)
Kanto
1403 (27.2)
738 (27.5)
665 (26.9)
Hokuriku and Tokai
908 (17.6)
485 (18.1)
423 (17.1)
Kinki
607 (11.8)
279 (10.4)
328 (13.3)
Tyugoku and Shikoku
774 (15.0)
383 (14.3)
391 (15.8)
Kyusyu and Okinawa
780 (15.1)
439 (16.3)
341 (13.8) 0.50d
Physical activity level Low
227 (4.4)
112 (4.2)
115 (4.7)
Middle
1079 (20.9)
575 (21.4)
504 (20.4)
High
3848 (74.7)
1997 (74.4)
1851 (74.9)
567.7 ± 36.1
566.1 ± 36.7
569.3 ± 35.3
Sleeping time (min)
\0.01c \0.01d
Educational background of mother Junior high or high school
2195 (42.6)
1248 (46.5)
947 (38.3)
Junior college or higher
2963 (57.4)
1438 (53.5)
1525 (61.7) \0.01d
Educational background of father Junior high or high school
2330 (51.1)
1270 (54.2)
1060 (47.9)
Junior college or higher
2228 (48.9)
1074 (45.8)
1154 (52.1)
1133 ± 307.0
1144 ± 308.4
1122 ± 305.2
0.01c
Q1 (508.7–884.2)e
1031 (19.8)
506 (18.8)
525 (21.2)
0.04d
Q2 (884.3–1024.1)e
1032 (20.1)
523 (19.5)
509 (20.6)
Q3 (1024.2–1164.8)e
1032 (20.3)
530 (19.7)
502 (20.3)
Q4 (1165.0–1354.2)e
1032 (20.0)
564 (21.0)
468 (18.9)
Q5 (1354.7–2948.7)e
1031 (19.8)
563 (21.0)
468 (18.9)
3342 (64.8)
1674 (62.3)
1668 (67.5)
Energy intake (kcal per day)
\0.01d
Frequency of brushing in the morning 4–7 times per week 1–3 times per week
630 (12.2)
369 (13.7)
261 (10.6)
None
1186 (23.0)
643 (23.9)
543 (22.0)
Frequency of brushing in the evening
a
4–7 times per week
4737 (91.8)
2437 (90.7)
2300 (93.0)
1–3 times per week
273 (5.3)
166 (6.2)
107 (4.3)
None
148 (2.9)
83 (3.1)
65 (2.6)
\0.01d
Decayed or filled teeth reported by guardians
b
Children whose guardians answered that their number of decayed or filled teeth was ‘‘0’’ were classified into the ‘‘children without reported caries’’ category. Those whose guardians answered ‘‘1–2,’’ ‘‘3–5,’’ ‘‘6–9,’’ and ‘‘10 or more’’ were classified into the ‘‘children with reported caries’’ category c Two-sided p value of the t test d
Two-sided p value of the Chi squared test
e
Range of intake in each quintile
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(approved on October 21 2010, approval number: 2010_09_01). Response to the questionnaire was regarded as an agreement to participate, in accordance with Ethical Guidelines for Epidemiological Research, published by Ministry of Health, Labor and Welfare.
The relationships between the intake of other nutrients and dental caries are shown in Table 4. Higher intakes of calcium, phosphate, starch (residual carbohydrate after subtraction of sugar and dietary fiber), and vitamins D were associated with fewer reported caries.
Results
Discussion
The demographic characteristics of analyzed children (n = 5158) are described in Table 1. The absence of reported caries was associated with higher educational level of parents, longer sleeping time, residential area, lower energy intake, more frequent teeth brushing habit. Crude and multivariate adjusted ratios for mean number of reported caries by quintile of proportion of energy intake from free sugar in total energy intake per day are shown in Table 2. The mean number of caries of children in quintiles 2–5 was higher than that in the reference group (p \ 0.01). Further, to examine the relationship between reported caries and the relatively small proportion of energy intake from free sugar, which was close to the WHO recommendation, we divided the participants into 25 equal groups (five groups for each quintile) and observed the ratio of the mean number of reported caries between the reference group (G1: lowest proportion group) and the lower nine groups (G2–G10; Table 3). In addition, to clearly show the change in ratio of mean caries number, we show the ratios between G1 and all the other groups (G2– G25) in Fig. 3. Overall, this figure shows that a higher proportion of energy from free sugar was positively associated with a higher mean number of caries. Nevertheless, this association was too small to be detected when the proportion of energy from free sugar was relatively small (G2 in Table 3).
In this study, we found that the proportion of Japanese children with reported caries was 52.0 %. This is as high as the prevalence of decayed or filled teeth of children aged 6–11 in the United States (average of values observed in 1994–2004) [16]. Although we saw a significantly positive overall association between a higher proportion of energy intake from free sugar and larger number of reported caries, our results imply the possibility of a threshold level of dietary sugar intake in the increased occurrence of reported caries. As shown in Table 3 and Fig. 3, we found no statistically significant relationship between a relatively small proportion, that is, up to 3.77 % (upper limit of G2) of energy intake from free sugar and mean number of reported caries. This finding suggests that free sugar intake of \3.77 % of total energy intake per day (upper limit of G2) was not associated with an increased number of reported caries in this population. However, it is possible that the true threshold is higher than the value suggested above for several reasons. The number of food items included in the BDHQ3y is limited, meaning that sugar intake might have been underestimated. In addition, the positive association observed in the subanalysis was thought to be unstable from G2 (3.18–3.77 % of total energy intake) to G6 (4.88–5.15 % of total energy intake), as the results of the statistical tests at these levels were unstable, that is, some results were significant but
Table 2 Relationship between proportion of energy intake from free sugar and number of decayed or filled teeth reported by guardians (reported caries) among 5158 Japanese preschool children aged 5–6 years: ratios for mean number of reported caries and 95 % CI Proportion of energy intake from free sugara (range; % of total energy intake per day)
n
Whole number of reported cariesb
Q1 (0.95–4.88)
1031
1318
1 (reference)
1 (reference)
Q2 (4.88–6.39)
1032
1504
1.14 (1.06, 1.23)*
1.14 (1.06, 1.23)*
Q3 (6.39–7.89) Q4 (7.89–10.1)
1032 1032
1583 1728
1.20 (1.12, 1.29)* 1.31 (1.22, 1.41)*
1.18 (1.10, 1.27)* 1.28 (1.19, 1.37)*
Q5 (10.1–30.7)
1031
2139
1.62 (1.52, 1.74)*
1.55 (1.44, 1.66)*
Crude ratio of mean number of reported cariesb (95 % CI)
Adjusted ratioc of mean number of reported cariesb (95 % CI)
* Statistically significant at the p B 0.05 level a
Sum of the intake of sucrose, glucose, and fructose added by home cooking and that from confectionaries, ice creams, snacks, chocolates, pastries, sweetened drinks, fruit juice, jam, and seasonings
b
Decayed or filled teeth reported by guardians
c
Ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression
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Matern Child Health J Table 3 Relationship between small proportion of energy intake from free sugar and number of decayed or filled teeth reported by guardians (reported caries) among 2063 Japanese preschool children aged 5–6 years: ratios for mean number of reported caries and 95 % CI Proportion of energy intake from free sugara (range; % of total energy intake per day)
n
Whole number of reported cariesb
G1 (0.95–3.17)
206
234
G2 (3.18–3.77)
206
239
1.02 (0.85, 1.22)
1.03 (0.86, 1.23)
G3 (3.77–4.19) G4 (4.19–4.53)
207 206
277 270
1.18 (0.99, 1.40) 1.15 (0.97, 1.37)
1.22 (1.03, 1.46)* 1.14 (0.96, 1.36)
G5 (4.53–4.88)
206
298
1.27 (1.07, 1.51)*
1.27 (1.07, 1.51)*
G6 (4.88–5.15)
207
242
1.03 (0.86, 1.23)
1.05 (0.88, 1.26)
G7 (5.15–5.46)
206
317
1.35 (1.14, 1.60)*
1.38 (1.17, 1.64)*
G8 (5.46–5.81)
206
310
1.32 (1.12, 1.57)*
1.33 (1.12, 1.58)*
G9 (5.81–6.13)
207
306
1.30 (1.10, 1.54)*
1.31 (1.11, 1.55)*
G10 (6.13–6.39)
206
329
1.41 (1.19, 1.66)*
1.40 (1.18, 1.65)*
Crude ratio of mean number of reported cariesb (95 % CI) 1 (reference)
Adjusted ratioc of mean number of reported cariesb (95 % CI) 1 (reference)
* Statistically significant at the p B 0.05 level a
Sum of the intake of sucrose, glucose, and fructose added by home cooking and that from confectionaries, ice creams, snacks, chocolates, pastries, sweetened drinks, fruit juice, jam, and seasonings
b
Decayed or filled teeth reported by guardians
c
Ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression
Fig. 3 Relationship between proportion of energy intake from free sugar and reported number of decayed or filled teeth (reported caries) in 5158 Japanese preschool children. G1–G25 indicates 25 groups which included almost the same number of subjects (206 or 207 subjects in each group) divided based on the proportion of energy intake from free sugar in the total daily energy intake. G1 is the lowest group (0.95–3.17 %, reference) and G25 is the highest
(15.4–30.7 %). The ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression model and shown in the chart. Significance of the ratios (*p \ 0.05) means that the mean number of reported caries in a certain group is significantly higher or lower than the reference group. The vertical lines on each ratio show 95 % confidence intervals for the ratios
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Matern Child Health J Table 4 Relationship between intake of selected four nutrients and number of decayed or filled teeth reported by guardians (reported caries) among 2063 Japanese preschool children aged 5–6 years: ratios for mean number of reported caries and 95 % CI Intake categories (range)
Crude ratio of mean number of reported cariesa (95 % CI)
Adjusted ratiob of mean number of reported cariesa (95 % CI)
n
Whole number of reported cariesa
Q1 (94.5–255)
1031
2042
1 (reference)
1 (reference)
Q2 (255–306)
1032
1721
0.84 (0.80, 0.90)*
0.86 (0.81, 0.92)*
Q3 (306–360)
1032
1586
0.78 (0.73, 0.83)*
0.81 (0.76, 0.87)*
Q4 (360–444)
1032
1598
0.78 (0.73, 0.83)*
0.82 (0.77, 0.88)*
Q5 (444–1043)
1031
1325
0.65 (0.61, 0.70)*
0.70 (0.66, 0.75)*
Q1 (299–460)
1031
2098
1 (reference)
1 (reference)
Q2 (460–509)
1032
1772
0.84 (0.79, 0.90)*
0.87 (0.82, 0.93)*
Q3 (509–556) Q4 (556–621)
1032 1032
1663 1400
0.79 (0.74, 0.84)* 0.67 (0.62, 0.71)*
0.84 (0.78, 0.89)* 0.72 (0.67, 0.77)*
Q5 (621–1026)
1031
1339
0.64 (0.60, 0.68)*
0.69 (0.65, 0.74)*
1031
1819
1 (reference)
1 (reference)
Q2 (99.3–108)
1032
1617
0.89 (0.83, 0.95)*
0.91 (0.85, 0.97)*
Q3 (108–116)
1032
1645
0.90 (0.85, 0.97)*
0.91 (0.85, 0.97)*
Q4 (116–126)
1032
1552
0.85 (0.80, 0.91)*
0.85 (0.80, 0.91)*
Q5 (126–177)
1031
1639
0.90 (0.84, 0.96)*
0.88 (0.82, 0.93)*
Q1 (0.23–2.24)
1031
1950
1 (reference)
1 (reference)
Q2 (2.24–2.92)
1032
1683
0.86 (0.81, 0.92)*
0.89 (0.83, 0.95)*
Q3 (2.92–3.65)
1032
1592
0.82 (0.76, 0.87)*
0.86 (0.80, 0.92)*
Q4 (3.65–4.82)
1032
1509
0.77 (0.72, 0.83)*
0.82 (0.76, 0.87)*
Q5 (4.82–22.0)
1031
1538
0.79 (0.74, 0.84)*
0.82 (0. 76, 0.87)*
Calcium (mg per 1000 kcal)
Phosphate (mg per 1000 kcal)
Starchc (g per 1000 kcal) Q1 (53.8–99.3)
Vitamin D (lg per 1000 kcal)
* Statistically significant at the p B 0.05 level a
Decayed or filled teeth reported by guardians
b
Ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression
c
Residual carbohydrate after subtraction of sugar and dietary fiber
others were non-significant. The statistical significance becomes more consistent for groups G7 and above, we therefore speculate that the possible threshold was around 5 % of total energy intake per day. These results might suggest that the proposed WHO recommendation to lower the limit of energy from free sugar from \10 to \5 % of total energy intake is reasonable. Among our participants, the proportion of children whose sugar intake was\5.00 % of total energy intake per day was 21.8 %, and thus considerably high. One implication of our results is that interventions for dental caries prevention should extend to a range of other strategies in addition to sugar intake reduction, particularly in populations whose mean sugar intake is not so high. Data from 2009 suggest that several other east and southeast Asian countries share Japan’s low sugar supply (Food supply of sugar and other sweeteners
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such as fructose syrup in 2011: Japan, 76; Republic of Korea, 95; Thailand, 79; Philippines, 63 (g per capita per day) [4]. Our present results might accordingly be useful in improving caries prevention strategies in these populations. According to the adjusted ratios of the mean number of reported caries by nutrient, intake of calcium and phosphate was associated with the greatest decrease in the number of caries. Ashley et al. [17] reported that exposure to foods containing dicalcium phosphate increased the concentrations of calcium and inorganic phosphorus in plaque. In addition, several studies showed that higher concentrations of calcium and phosphate in plaque were associated with fewer dental caries [18, 19]. The results of our study are compatible with these studies. In contrast, it is also possible that a higher intake of calcium and phosphate is related to a healthy lifestyle or parental
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socioeconomic status. Larson et al. [20] reported that a higher dietary intake of calcium was related to healthier lifestyle (more frequent intake of breakfast and lower intake of sweet drinks and junk food) among students in junior and senior high school in the US. Our addition of ‘‘frequency of teeth brushing in the morning’’ and ‘‘educational background of the mother’’ to the model may have adjusted for the confounding effect of these factors, to some extent at least. In our study, higher intake of vitamin D was also statistically significantly associated with a lower number of dental caries. Hujoel [21] stated that a systematic review of controlled clinical studies showed a significant caries-preventing effect of vitamin D. The results of our study are consistent with it. In addition, our results also showed the relatively weak association between a higher intake of starch and fewer caries. Lingstro¨m et al. [22] stated that the effect of starch intake on the occurrence of dental caries in daily living in humans was uncertain. The anti-cavity effect of starch intake observed in our study might owe to the negative correlation between dietary intake of starch and sugar (r = -0.55; p \ 0.0001), which might suggest that children who have more meals tend to have less sweet snacks and drinks. Several limitations of our study warrant mention. First, since this is the first study to measure dietary intake of sugar in community-dwelling Japanese, the estimation method has not been validated yet. Sugar content is included as carbohydrate in the Standard Tables of Food Composition in Japan [8]. To estimate sugar intake as precisely as possible, we scrutinized other articles describing the sugar content of foods and drinks in Japan, and selected the most reliable chemically analyzed values for each item included in the BDHQ3y. In addition, the BDHQ has satisfactory estimating and ranking ability for carbohydrate intake [9–12], and the child-specific estimation performed with the BDHQ3y shared similar nutritional value calculation algorithms with those of the BDHQ. Besides, the dietary estimation was conducted with the BDHQ3y, which define portion size as fixed, except for the portion size of meat fat and soup of noodle. Though these fixed portion sizes were decided counting the effect from age of children, according to the survey on Japanese children conducted by Asakura et al. [23], it could be possible that misreporting of dietary intake of the children occurred from this characteristics of the BDHQ3y. Second, validity of the number of dental caries reported by guardians in Japan is unknown. Among children in the US, Beltra´n et al. [24] showed that the presence of restored caries estimated by a questionnaire completed by guardians has high sensitivity and specificity, whereas that of untreated caries has low sensitivity and high specificity. On this basis, underreporting was highly possible in our study
but over-reporting was unlikely. However, dental checkup conducted yearly by a dentist, is mandatory in Japanese nursery schools. The guardians are usually aware of the presence of dental carries among their children, as the examination results are reported by the school. Although there might be a possibility that some guardians are indifferent to their children’s oral health and not paying attention to the examination results, the prevalence of reported caries in our subjects was higher than that of decayed or filled caries reported in dental checkup by dentists in the School Health Statistics Research conducted by the Ministry of Education, Culture, Sports, Science and Technology (present study, 52 %; School Health Statistics Research [1], 46 %) which suggested that the likelihood of underreporting was small. In addition, the number of reported caries was collected by the multiple-choice question with six choices in this study. For this characteristic of our study, the accuracy of the number of reported caries might be lower than when the number was asked as continuous variable. However, it is also possible that the categorical choice buffered the effect of misreporting of guardians about the exact number of caries. Third, selection bias is possible in the present study. The children (participants) were not selected randomly, but were volunteers. The guardians of the children might be health-conscious than the general population. However, the educational and physical characteristics of the guardians are supposed to be similar to the general population in Japan. The age-adjusted proportion of married, divorced, or bereaved people whose educational background is junior high or high school in Japan (female: 46.1 %, male: 48.2 %; the 2010 population census in Japan [25]) is almost the same as that of the guardians in our study (mother: 42.6 %, father: 51.1 %). In addition, the mean body height and weight of the general adults in Japan aged 20–59 (female’s height: 157.9 cm, weight: 52.8 kg, male’s height: 171.2 cm, weight 69.7 kg; the 2012 National Health and Nutrition Survey [26]) are similar to those of guardians in our research (mother’s height: 158.2 cm, weight 52.5 kg, father’s height: 171.7 cm, weight 69.2 kg). Thus, the selection bias might be minimal in the present study. Fourth, due to the cross-sectional design of the present study, we cannot exclude the possibility of reverse causality. Children experiencing pain from dental caries or under professional advice to decrease sugar intake to prevent caries are hardly likely to increase sugar intake. If the presence of dental caries does in fact lead to changes in sugar intake in children, this relationship would work to mask the association between higher sugar intake and more caries. Our study found a significantly positive association between a higher number of reported caries and higher proportion of energy intake from free sugar if the
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proportion was over 3.77 % of energy intake per day (higher limit of G2). Even if reverse causality masked the association, the threshold proportion of energy intake from free sugar which produced an increase in the number of caries might be lower than the present result. If so, the WHO’s proposed recommendation to limit energy from free sugar to \5 % of total energy intake remains reasonable. In addition, results of additional analysis which excluded children with a change in dietary habits within the preceding year (n = 761, data not shown) were closely similar to those of analysis which included them. We therefore consider that, if present, the impact of any reverse causality was minimal. Besides, it is also possible that the presence of cavities in the children can cause the reporting bias in the guardians. However, there are possibilities of both under- and over-reporting of sugar intake in the children. When the guardians underreport the sugar intake of their children to hide their poor care, the true threshold of proportion of energy intake from free sugar which produced an increase in the number of caries might be higher. On the other hand, when the amount of sugar intake was over-reported due to recall bias, the true threshold might be lower than that of our result. As described before, effect of underreporting and over-reporting might have been attenuated each other because both were possible in the present study. Thus, the potential for the parent to influence the survey should not be so large. Finally, adjustment for some confounding factors may have been insufficient or absent. In particular, we did not measure several potentially important factors, including fluoride exposure, frequency of snacking, or the percentage of sugar-free products in total dietary intake. Although tap water in Japan is not artificially fluoridated (concentration of natural fluoride—min: \0.05 mg L-1, max: 0.21 mg L-1 [27]), 82 % of Japanese children use fluoridecontaining toothpaste [28]. The preventive effect of fluoride on dental caries might have been partially adjusted for by the addition of ‘‘frequency of teeth brushing in the morning’’ to the model. Johansson et al. [29] reported that the frequency of consuming snacks and drinks was associated with caries status in preschool children. Children who eat snacks more frequently are speculated to consume more sugars, so the participants in higher sugar intake group in the present study might have had more frequent snacking. On this basis, the effect of sugar intake alone on dental caries might have been overestimated, and the true intake threshold for dental caries development might be higher than our estimated value. Moreover, Llena et al. [30] also showed that consumption of sugar-free sweets was not associated with caries experience in 6- to 10-yearold children. In our study, since we did not differentiate sweet drinks with and without sugar, sugar intake might have been overestimated. However, the market share of
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non-sugar sweet drink products in Japan is small (8.1 %) [31]. In addition, Marshall et al. [32] reported that the average intake of sugar-free beverages by children aged 1–5 in the US was zero. It is therefore possible that sugarfree beverage consumption of Japanese children is also small, and the possibility of overestimating sugar intake for this reason is likely small. In conclusion, we found that the association between a relatively low proportion of energy intake from free sugar, at approximately \5 % of total energy intake per day, and an increased number of reported caries among preschool children in Japan was too small to be detected. In contrast, higher intake above this proportion was associated with a higher number of dental caries. The recent proposition of WHO to halve the recommended added sugar intake from 10 % of daily energy intake to 5 % might be valid, though more study will be necessary to examine the effect of relatively low intake of free sugar. Acknowledgments The authors are deeply grateful to the dietitians who assisted the fieldwork, especially to Ms. Yuko Takano, Ms. Machiko Tanaka, and Ms. Yukiko Takahashi, as well as the nursery school staff who facilitated the study. This research was financially supported by the Japan Dietetic Association. Author Contributions Miyuki Saido designed and carried out the analysis and drafted the manuscript. Keiko Asakura edited the manuscript. Shizuko Masayasu designed, prepared, and conducted the dietary survey and arranged the data set. Satoshi Sasaki oversaw the design and analytical strategy of the study. Compliance with Ethical Standards Conflict of interest peting interests.
The authors declare that they have no com-
References 1. Ministry of Education, Culture, Sports, Science and Technology (Japan). (2012). Annual report of School Health Statistics Research 2011. Tokyo: Nikkei Printing Inc. (in Japanese). 2. Owens, B. (2014). Storm brewing over WHO sugar proposal. Nature, 507(7491), 150. 3. Moynihan, P. J., & Kelly, S. A. (2014). Effect on caries of restricting sugars intake: Systematic review to inform WHO guidelines. Journal of Dental Research, 93(1), 8–18. 4. Food and Agriculture Organization of the United Nations Statistics Division. (2014). Food supply—Crops primary equivalent. http://faostat3.fao.org/download/FB/CC/E. Accessed 3 Nov 2014. 5. Koike, H. (1962). Studies on caries incidence in the first molar in relation to amount on sugar consumption on primary school children in Kyoto City. Bulletin of Tokyo Dental College, 3(1), 44–56. 6. Honma, S., & Wakamatsu, H. (2003). Influence of children’s life style on their dental health. Health Science, 19, 127–135 (in Japanese). 7. Kurose, M., Morita, M., & Watanabe, T. (1997). Dental caries and sucrose intake in Japanese preschool children. Journal of Dental Health, 47, 683–692 (in Japanese).
Matern Child Health J 8. Ministry of Education, Culture, Sports, Science and technology (Japan). (2005). Standard tables of food composition in Japan (Fifth Revised and Enlarged ed.). Tokyo: National Printing Bureau (Japan) (in Japanese). 9. Sasaki, S., Yanagibori, R., & Amano, K. (1998). Self-administered diet history questionnaire developed for health education: A relative validation of the test-version by comparison with 3-day diet record in women. Journal of Epidemiology, 8(4), 203–215. 10. Sasaki, S., Ushio, F., Amano, K., Morihara, M., Todoriki, O., Uehara, Y., & Toyooka, E. (2000). Serum biomarker-based validation of a self-administered diet history questionnaire for Japanese subjects. J Nutritional Science and Vitaminology (Tokyo), 46(6), 285–296. 11. Kobayashi, S., Murakami, K., Sasaki, S., Okubo, H., Hirota, N., Notsu, A., et al. (2011). Comparison of relative validity of food group intakes estimated by comprehensive and brief-type self-administered diet history questionnaires against 16 d dietary records in Japanese adults. Public Health Nutrition, 14(7), 1200–1211. 12. Kobayashi, S., Honda, S., Murakami, K., Sasaki, S., Okubo, H., Hirota, N., et al. (2012). Both comprehensive and brief-type selfadministered diet history questionnaires have reasonable ranking ability for nutrient intakes compared with 16-day dietary records in Japanese adults. Journal of Epidemiology, 22(2), 151–159. 13. Asakura, K., Haga, M., Adachi, M., Sakai, H., Takahashi, C., & Sasaki, S. (2014). Estimation of food portion sizes frequently consumed by children 3–6 years old in Japan. Journal of Nutritional Science and Vitaminology, 60, 387–396. 14. Ministry of Health, Labor and Welfare (Japan). (2011). Survey of dental diseases. http://www.mhlw.go.jp/toukei/list/xls/62-17c231.xlsx. Accessed 23 Oct 2014. 15. Statistics Bureau, Ministry of Internal Affairs and Communications (Japan). (2013). 2011 Survey on time use and leisure activities. Tokyo: National Statistics Center. 16. National Institute of Dental and Craniofacial Research (internet). Dental caries (tooth decay) in children (age 2–11). http://www. nidcr.nih.gov/DataStatistics/FindDataByTopic/DentalCaries/Den talCariesChildren2to11.htm. Accessed 23 Oct 2014. 17. Ashley, F. P., & Wilson, R. F. (1977). Effect of sweets supplemented with dicalcium phosphate on dental plaque composition. Caries Research, 11(6), 336–344. 18. Ashley, F. P. (1975). Calcium and phosphorus concentrations of dental plaque related to dental caries in 11- to 14-year-old male subjects. Caries Research, 9(5), 351–362. 19. Shaw, L., Murray, J. J., Burchell, C. K., & Best, J. S. (1983). Calcium and phosphorus content of plaque and saliva in relation to dental caries. Caries Research, 17(6), 543–548. 20. Larson, N., Story, M., Wall, M., & Neumark-Sztainer, D. (2006). Calcium and dairy intake of adolescents are associated with their home environment, taste, preference, personal health beliefs, and meal patterns. Journal of the American Dietetic Association, 106(11), 1816–1824. 21. Hujoel, P. P. (2013). Vitamin D and dental caries in controlled clinical trials: Systematic review and meta-analysis. Nutrition Reviews, 71(2), 88–97. 22. Lingstro¨m, P., van Houte, J., & Kashket, S. (2000). Food starches and dental caries. Critical Reviews in Oral Biology and Medicine, 11(3), 366–380. 23. Asakura, K., Haga, M., Adachi, M., Sakai, H., Takahashi, C., & Sasaki, S. (2014). Estimation of food portion sizes frequently consumed by children 3–6 years old in Japan. Journal of Nutritional Science and Vitaminology, 60, 387–396.
24. Beltra´n, E. D., Malvitz, D. M., & Eklund, S. A. (1997). Validity of two methods for assessing oral health status of populations. Journal of Public Health Dentistry, 57(4), 206–214. 25. Statistic Bureau, Ministry of Internal Affairs and Communications (internet). 2010 population census. http://www.e-stat.go.jp/ SG1/estat/Csvdl.do?sinfid=000012989699. Accessed 23 Oct 2014. 26. Ministry of Health, Labour and Welfare (Japan) (Internet). 2012 national health and nutrition survey. http://www.mhlw.go.jp/ bunya/kenkou/eiyou/dl/h24-houkoku-05.pdf. Accessed 23 Oct 2014. 27. Japan Water Works Association (internet). (2006). Database of water quality of aqueduct (cited October 23, 2014). http://www. jwwa.or.jp/mizu/ent_sup.html. Accessed 23 Oct 2014. 28. Ministry of Health, Labour and Welfare (Japan). (2011). 2009 National Health and Nutrition Survey. Tokyo: Dai-ichi Shuppan. 29. Johansson, I., Holgerson, P. L., Kressin, N. R., Nunn, M. E., & Tanner, A. C. (2010). Snacking habits and caries in young children. Caries Research, 44(5), 421–430. 30. Llena, C., & Forner, L. (2008). Dietary habits in a child population in relation to caries experience. Caries Research, 42(5), 387–393. 31. Japan Food Journal. (2010). Syokuhin torenndo 2010–2011. Tokyo: Japan Food Journal (in Japanese). 32. Marshall, T. A., Levy, S. M., Broffitt, B., Warren, J. J., Eichenberger-Gilmore, J. M., Burns, T. L., & Stumbo, P. J. (2003). Dental caries and beverage consumption in young children. Pediatrics, 112, e184–e191. 33. Japan Food Research Laboratories. (2010). Nihon syokuhin hyoujun seibun-hyou ni okeru tansuikabutsu-ryou ni kansuru datousei kensyou chousa seika houkokusyo [Report of the validation research for carbohydrate contents in foods included in standard tables of food composition in Japan]. Tokyo: Ministry of Education, Culture, Sports, Science and Technology, Japan (in Japanese). 34. Japan Food Research Laboratories. (2013). Kokumin no kenkona seikatsu zoshin no tame no shokuhin seibunhyo jujitsu jigyo ni kakaru shokuhin seibun teiryo bunseki seika hokokusho [Report for quantitative analysis of food composition to enrich the standard table for food composition in Japan for promotion of healthy lives of the people]. Tokyo: Japan Food Research Laboratories (in Japanese). 35. Watanabe, T., Fuse, N., & Hagiwara, K. (2001). Saccharose contents of the confectioneries in standard table of food composition in japan fifth revised edition and that estimation. The Japanese Journal of Nutrition, 59(5), 247–252 (in Japanese). 36. Yamamoto, S., Taniguchi, H., Sarukura, N., Tsao, H., Tseng, A., & Takeichi, H. (2009). Development of a food composition database of monosaccharides and disaccharides in sweet snacks and beverages. Journal of the Japan Dietetic Association, 52(4), 22–25 (in Japanese). 37. Takeichi, H., Wakikawa, N., Taniguchi, H., Sarukura, N., Tseng, A. T., Wong, U. Y., et al. (2010). Concentrations of monosaccharide and disaccharides in commercial sweet snacks. Journal of the Japan Dietetic Association, 53(1), 23–26 (in Japanese). 38. Ito, S. (1996). Kajitsu no kagaku. Tokyo: Asakura Syobo (in Japanese). 39. Seyama, N. (2010). Nihon no ichigo. Tokyo: Yokendo (in Japanese). 40. Hoshikawa, K. (1985). Imo–Minaoso tsutsi kara no megumi. Tokyo: Kagawa Nutrition Publishing Division (in Japanese).
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Relationship Between Dietary Sugar Intake and Dental Caries Among Japanese Preschool Children with Relatively Low Sugar Intake (Japan Nursery School SHOKUIKU Study): A Nationwide Cross-Sectional Study Miyuki Saido1 • Keiko Asakura1,2 • Shizuko Masayasu3 • Satoshi Sasaki1
Ó Springer Science+Business Media New York 2015
Abstract Objectives The WHO has recently proposed to halve the recommendation for free sugar intake from 10 to 5 % of energy intake to reduce the incidence of diseases such as obesity and dental caries. The Japanese population is suitable to confirm the appropriateness of this proposal, because dietary sugar intake in Japan is exceptionally low among developed countries. We sought to establish a method to estimate dietary sugar intake in Japan and to examine the relationship between sugar and the number of dental caries using data obtained from the Japan Nursery School SHOKUIKU study. Methods Dietary intake during the preceding month and the number of caries was examined in children aged 5–6 years using a brief-type self-administered diet history questionnaire for Japanese preschool children completed by their guardians and another questionnaire on lifestyle. Multivariate Poisson regression models were used for the analysis. Results When subjects were ranked into quintiles by the proportion of energy from free sugar, those in higher quintiles had more caries than those in the lowest & Satoshi Sasaki [email protected] Miyuki Saido [email protected] Keiko Asakura [email protected] Shizuko Masayasu [email protected] 1
Department of Social and Preventive Epidemiology, School of Public Health, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
2
Interfaculty Initiative in Information Studies, The University of Tokyo, Tokyo, Japan
3
Ikurien Special Nursing Home for the Elderly, Ibaragi, Japan
quintile. On close analysis, the number of caries among children with a relatively small proportion of energy intake from free sugar (3.18–3.77 %) was not significantly different from that in the lowest group (0.95–3.17 %). Conclusions The recent proposition of WHO might be valid, because the adverse effect of relatively small proportion (approximately less than 5 %) of energy intake from free sugar on caries was not detected among the subjects in this study. However, more study will be necessary to reach a conclusion. Keywords Dental caries Sugar intake Preschool children Prevention Japan
Significance There is evidence of moderate quality showing that incidence of dental caries is lower when the intake of free sugar is \10 % of total energy intake per day, but effect of more reduction (\5 % of total energy intake) of free sugar is still unclear. Our study showed that lower energy intake from free sugar, at approximately less than 5 % of total energy intake per day, did not increase the number of dental caries among preschool children in Japan. The intake of free sugars between 5 to 10 % of total energy intake possibly increased the number of dental caries.
Background Dental caries is the most common disease affecting preschool (under 5 years old) and elementary school children (6–11 years old) in Japan [1]. More than 40 % of 5-yearold children are reported to experience dental caries [1]. Dental caries can cause pain and discomfort in children and
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lead to an unbalanced diet. Thus, prevention of caries in childhood is an urgent issue. Reduction of dietary sugar intake is known as an important strategy in preventing caries. To reduce the incidence of health problems such as obesity and dental caries, the WHO has recently proposed halving the recommended free sugar (sugars include monosaccharides and disaccharides added to foods and beverages by the manufacturer, cook or consumer, and sugars naturally present in honey, syrups, fruit juices and fruit juice concentrates) intake, from 10 % of daily energy intake to 5 % [2]. However, the appropriateness of this new recommendation has been difficult to examine in developed countries, because sugar consumption by these populations, particularly among preschool children, is substantially above the WHO recommendation [3]. Japan is exceptional in this regard, with a relatively high income but low consumption of sugar (food supply of sugar and other sweeteners such as fructose syrup in 2011: Japan, 76; USA, 165; UK, 107 (g per capita per day) [4]. This low consumption makes Japan a suitable venue in which to examine the appropriateness of the WHO proposal. Despite this advantage, almost all epidemiological studies to investigate the association between dietary sugar intake and the number of dental caries in Japanese population are the ecological studies [5]. In addition, almost no quantitative and population based assessment of dietary intake of sugar has been conducted in Japan. Among the few studies that have investigated the relationship between dietary sugar intake and the number of dental caries in Japanese populations [6, 7], one measured only the frequency of sweets intake per week instead of sugar intake [6] and a second excluded non-staple foods, fruits, and juice from measurement [7]. The Standard Tables of Food Composition in Japan do not provide the sugar content of foods and beverages [8]. This lack has hindered investigations of daily dietary sugar intake in Japanese populations and prevented evaluation of the influence of characteristic low sugar intake on health. In this study, we developed a method to estimate the dietary intake of free sugar using a diet history questionnaire for Japanese preschool children. We then examined the relationship between dental caries and lifestyle factors, including dietary intake, using data obtained from the Japan Nursery School SHOKUIKU Study. We particularly focused on the relationship between low-range free sugar intake (\5 % of total energy intake per day) and dental caries.
Methods Study Setting and Participants Participants in the Japan Nursery School SHOKUIKU Study were recruited from 44 of the 47 prefectures in
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Japan. Initially, representative dietitians of councils of prefectural welfare facility dietitians at local branches of the Japan Dietetic Association and staff dietitians in municipal child welfare facilities were invited to participate. The representative and staff dietitians or nursery governesses in 416 of 437 invited nurseries agreed to participate. These then recruited the study subjects from guardians of children aged 5 or 6 years at their nursery school. Two questionnaires, one about the child’s general lifestyle and the second assessing the child’s dietary intake, were distributed to 9762 guardians and collected between February and March in 2011. Guardians were requested to complete the questionnaire with hearing from their children about what they have eaten out of home. A total of 5634 responded to the lifestyle questionnaire (response rate: 58 %) and 6257 to the diet history questionnaire (64 %). The two data sets for lifestyle and dietary intake were then merged (N = 6383: participants who submitted at least one questionnaire, either lifestyle or diet history questionnaire, or both). Children with missing values for key questions such as family structure, sex, brushing habit in the morning, or educational background of mother, and those whose guardian answered ‘‘I don’t know’’ or who had missing data for the number of guardians-reported decayed or filled caries (abbreviated as ‘‘reported caries’’ hereafter) were excluded, leaving 5244 children in the merged dataset. We then further excluded children with outliers those whose weight at birth was \100 g, height at the time of survey was 85 cm or under or 150 cm or over, or with energy intake \500 or 3000 kcal and over from the dataset, leaving 5217 children. Further, children who were receiving diet therapy was excluded, finally 5158 children were analyzed (Fig. 1). Dietary Assessment Dietary intake data of the children during the preceding month was collected using a brief-type self-administered diet history questionnaire for Japanese preschool children (BDHQ3y). The BDHQ3y is a four-page structured questionnaire that inquires about the consumption frequency of selected foods commonly consumed in Japan, general dietary behavior and usual cooking methods. It was developed based on comprehensive (16 pages) [9, 10] and brief (four pages) [11, 12] versions of a validated selfadministered diet history questionnaire for adults. Estimates of daily intake of foods (66 items in total), energy, and selected nutrients derived from those foods were calculated using an ad hoc computer algorithm for the BDHQ3y based on the Standard Tables of Food Composition in Japan [8]. In the BDHQ3y, fixed portion sizes were used for the children at the same age in month to calculate dietary intake [13]. Values of nutrient intake were
Matern Child Health J Fig. 1 Flow chart of inclusion and exclusion criteria of the study
Lifestyle quesonnaire (n=5634)
Diet history quesonnaire (n=6257) Excluding missing values
n=6383
Missing values for family structure (n=749) and sex
(n=122)
Missing data for brushing habit in the morning (n=10), educaonal background of mother (n=104) Missing data or who answered “I don’t know”
n=5244
for number of dental caries (n=154) Excluding outliers Outliers for body weight at birth (n=4) Energy intake 3000 kcal (n=23)
n=5217
Body height 85 cm or 150 cm (n=0)
Excluding children under unusual condion Under diet therapy (n=59)
Analyzed children (n=5158)
energy-adjusted using the density method (percentage of energy for energy-providing nutrients and amount per 4184 kJ (1000 kcal) of energy for other nutrients). The BDHQ3y also elicited information on the child’s weight and height. Body mass index (BMI) was calculated by dividing body weight (kg) by the square of height (m2) reported by the guardian. The BDHQ3y also collected information on date of birth, sex, physical activity level, number of reported caries, and implementation of diet therapy supervised by a doctor or dietitian. Sugar Intake Estimation Because construction of the BDHQ3y was based on the Standard Tables of Food Composition in Japan [8], which does not include values for the sugar content, we were unable to estimate sugar contents directly. Instead, we developed composition tables for three types of sugar (sucrose, glucose and fructose) for 74 of the 119 items used in the nutritional value calculations of the BDHQ3y. These 74 items were selected if residual carbohydrate content after subtraction of dietary fiber content was 5 g or more per 100 g of total food (drink) weight in the Standard Tables of Food Composition in Japan. As an exception, ‘‘mix juice’’ (vegetable juice) was included regardless of residual weight. Although residual weight for mixed juice in the food composition table is \5 g [8], labeled weight for the recent best-seller vegetable juice in Japan is far
higher than 5 g (14.9 g) per 100 g. Data for sugar content were collected as described in Fig. 2. Dental Caries The BDHQ3y also includes a multiple-choice question asking the guardians about the number of dental caries including decayed or filled teeth of their children, with six answer choices (‘‘the number of dental caries including decayed or filled teeth’’ = ‘‘0’’, ‘‘1–2’’, ‘‘3–5’’, ‘‘6–9’’, ‘‘10 and more’’, and ‘‘I don’t know’’). In this study, we used the five numbered categories and excluded subjects who responded ‘‘I don’t know’’. We assigned the median value of each category as the representative dental caries’ number for each category (0 for ‘‘0’’ category, 1 for ‘‘1–2’’, 4 for ‘‘3–5’’, 7 for ‘‘6–9’’). For the ‘‘10 and more’’ category, we used the median value between 10 and 16, namely 13, because 16 was the maximum number of decayed and filled primary teeth among children aged 3–5 in a government research program [14]. Other Variables Information about the general lifestyle of children was collected using a four-page questionnaire designed for this study. In this questionnaire, the guardians reported family structure, chronic conditions of the child requiring dietary restriction, sleeping time of the child, educational
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Matern Child Health J Fig. 2 Data collection of sugar content of the foods and drinks
ەWhen sugar analysis for a certain food or drink in the BDHQ3y were available from …
ձSingle arcle The value of the arcle was assigned as sugar content. *Informaon sources that met these criteria were two governmental reports (abbreviated as “Report 1” (33) and “Report 2” (34) hereaer), as well as two papers (35-37) and three books (3840).
ղMulple arcles •When those arcles included either of the governmental reports (Reports 1 and 2), the values in them were given priority. •When one item was reported in both of these reports, the values in Report 2 was used, because this is the more comprehensive and recent of the two. •When food was not included in these two governmental reports, values for which the measurement method was most clearly described (31, 37-40) was adopted.
ճNo reliable arcles The following esmaon methods were used. •Bread and noodles: the sugar content of ingredients reported in “Report 1” and the Standard Tables of Food Composion in Japan (33) were summed to esmate the sugar content in the product. •Jam: Since the amount of carbohydrate in jam reported in the Standard Tables of Food Composion in Japan was thought to include sugar and fiber, fiber content was subtracted from carbohydrate content and the residual carbohydrate value was used as sugar content. • Potato chips and French fries: The sugar content of raw potato reported in “Report 1” was used as the sugar content of these foods. • Other foods such as mixed juice, tomato juice, ketchup and soy source: the product having the top market share in its category was idenfied using POS (point of sales) data between April 2009 and March 2010 (31). Then, the sugar content shown in the website of the product was used. When sugar content was not provided, dietary fiber content was subtracted from carbohydrate content and the residual carbohydrate content was regarded as the sugar content.
background of the parents, and weekly frequency of teeth brushing of the child in the morning and evening. Statistical Analysis The associations between dental caries and a number of lifestyle factors including dietary intake were examined. First, basic characteristics were compared between children with and without reported caries using the t test and Chi square test. Dietary intakes were then categorized into quintile points based on distribution, and crude and multivariable adjusted ratios of the mean number of reported caries and 95 % confidence intervals for each quintile category compared to the lowest category of the dietary variable were calculated using a Poisson regression model. With regard to sugar intake, we investigated the association between caries and the proportion of energy intake from free sugar in total energy intake per day. In addition, to examine the effect of the relatively small proportion of energy intake from free sugar on dental caries, we divided each quintile of energy proportion into five further groups (G1–G25; 25 groups in total), and used the same multivariate Poisson regression model. We selected lifestyle factors for inclusion in the model as possible confounding factors by comparing the basic
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characteristics of children with and without reported caries. Among variables which were statistically significantly different (p \ 0.05), educational background of the mother, frequency of brushing in the morning, frequency of brushing in the evening, and residential area were included in the model. Educational background of the father was excluded to avoid decreasing sample size, as there were 600 participants with missing value for father’s education. Mother’s educational background is supposed to be enough as a covariate to adjust the effect of parents’ educational level, because mothers generally spend more time in childraising than fathers in Japan [15], so the mother’s knowledge of health and diet should more strongly affect the child’s health status than the father’s knowledge. Although sleeping time also significantly differed, it was excluded because the mean difference was only 3 min. All statistical analyses were performed using SAS statistical software (version 9.3, 2011, SAS Institute Inc., Cary, NC, USA). A two-sided p value of \0.05 was considered statistically significant. Ethical Considerations The study protocol was approved by the Ethics Committee of the Japanese Society of Nutrition and Dietetics
Matern Child Health J Table 1 Characteristics of subjects Variables
n (%) or mean ± SD
p value
All children (n = 5158)
Children with reported cariesa (n = 2686)b
Children without reported cariesa (n = 2472)b
6.76 ± 0.42
6.78 ± 0.42
6.75 ± 0.43
0.02c
5
381 (7.4)
178 (6.6)
203 (8.2)
0.03d
6
4777 (92.6)
2508 (93.4)
2269 (91.8)
Age (years)
0.93d
Sex Male
2732 (53.0)
1421 (52.9)
Female
2426 (47.0)
1265 (47.1)
1161 (47.0)
Height (cm)
115.2 ± 5.4
115.1 ± 5.5
115.3 ± 5.4
0.23c
Weight (kg)
20.6 ± 3.2
20.6 ± 3.3
20.7 ± 3.1
0.39c
15.5 ± 1.8
15.5 ± 1.8
15.5 ± 1.7
0.87c
-2
BMI (kg m )
1311 (53.0)
\0.01d
Residence area Hokkaido and Tohoku
686 (13.3)
362 (13.5)
324 (13.1)
Kanto
1403 (27.2)
738 (27.5)
665 (26.9)
Hokuriku and Tokai
908 (17.6)
485 (18.1)
423 (17.1)
Kinki
607 (11.8)
279 (10.4)
328 (13.3)
Tyugoku and Shikoku
774 (15.0)
383 (14.3)
391 (15.8)
Kyusyu and Okinawa
780 (15.1)
439 (16.3)
341 (13.8) 0.50d
Physical activity level Low
227 (4.4)
112 (4.2)
115 (4.7)
Middle
1079 (20.9)
575 (21.4)
504 (20.4)
High
3848 (74.7)
1997 (74.4)
1851 (74.9)
567.7 ± 36.1
566.1 ± 36.7
569.3 ± 35.3
Sleeping time (min)
\0.01c \0.01d
Educational background of mother Junior high or high school
2195 (42.6)
1248 (46.5)
947 (38.3)
Junior college or higher
2963 (57.4)
1438 (53.5)
1525 (61.7) \0.01d
Educational background of father Junior high or high school
2330 (51.1)
1270 (54.2)
1060 (47.9)
Junior college or higher
2228 (48.9)
1074 (45.8)
1154 (52.1)
1133 ± 307.0
1144 ± 308.4
1122 ± 305.2
0.01c
Q1 (508.7–884.2)e
1031 (19.8)
506 (18.8)
525 (21.2)
0.04d
Q2 (884.3–1024.1)e
1032 (20.1)
523 (19.5)
509 (20.6)
Q3 (1024.2–1164.8)e
1032 (20.3)
530 (19.7)
502 (20.3)
Q4 (1165.0–1354.2)e
1032 (20.0)
564 (21.0)
468 (18.9)
Q5 (1354.7–2948.7)e
1031 (19.8)
563 (21.0)
468 (18.9)
3342 (64.8)
1674 (62.3)
1668 (67.5)
Energy intake (kcal per day)
\0.01d
Frequency of brushing in the morning 4–7 times per week 1–3 times per week
630 (12.2)
369 (13.7)
261 (10.6)
None
1186 (23.0)
643 (23.9)
543 (22.0)
Frequency of brushing in the evening
a
4–7 times per week
4737 (91.8)
2437 (90.7)
2300 (93.0)
1–3 times per week
273 (5.3)
166 (6.2)
107 (4.3)
None
148 (2.9)
83 (3.1)
65 (2.6)
\0.01d
Decayed or filled teeth reported by guardians
b
Children whose guardians answered that their number of decayed or filled teeth was ‘‘0’’ were classified into the ‘‘children without reported caries’’ category. Those whose guardians answered ‘‘1–2,’’ ‘‘3–5,’’ ‘‘6–9,’’ and ‘‘10 or more’’ were classified into the ‘‘children with reported caries’’ category c Two-sided p value of the t test d
Two-sided p value of the Chi squared test
e
Range of intake in each quintile
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Matern Child Health J
(approved on October 21 2010, approval number: 2010_09_01). Response to the questionnaire was regarded as an agreement to participate, in accordance with Ethical Guidelines for Epidemiological Research, published by Ministry of Health, Labor and Welfare.
The relationships between the intake of other nutrients and dental caries are shown in Table 4. Higher intakes of calcium, phosphate, starch (residual carbohydrate after subtraction of sugar and dietary fiber), and vitamins D were associated with fewer reported caries.
Results
Discussion
The demographic characteristics of analyzed children (n = 5158) are described in Table 1. The absence of reported caries was associated with higher educational level of parents, longer sleeping time, residential area, lower energy intake, more frequent teeth brushing habit. Crude and multivariate adjusted ratios for mean number of reported caries by quintile of proportion of energy intake from free sugar in total energy intake per day are shown in Table 2. The mean number of caries of children in quintiles 2–5 was higher than that in the reference group (p \ 0.01). Further, to examine the relationship between reported caries and the relatively small proportion of energy intake from free sugar, which was close to the WHO recommendation, we divided the participants into 25 equal groups (five groups for each quintile) and observed the ratio of the mean number of reported caries between the reference group (G1: lowest proportion group) and the lower nine groups (G2–G10; Table 3). In addition, to clearly show the change in ratio of mean caries number, we show the ratios between G1 and all the other groups (G2– G25) in Fig. 3. Overall, this figure shows that a higher proportion of energy from free sugar was positively associated with a higher mean number of caries. Nevertheless, this association was too small to be detected when the proportion of energy from free sugar was relatively small (G2 in Table 3).
In this study, we found that the proportion of Japanese children with reported caries was 52.0 %. This is as high as the prevalence of decayed or filled teeth of children aged 6–11 in the United States (average of values observed in 1994–2004) [16]. Although we saw a significantly positive overall association between a higher proportion of energy intake from free sugar and larger number of reported caries, our results imply the possibility of a threshold level of dietary sugar intake in the increased occurrence of reported caries. As shown in Table 3 and Fig. 3, we found no statistically significant relationship between a relatively small proportion, that is, up to 3.77 % (upper limit of G2) of energy intake from free sugar and mean number of reported caries. This finding suggests that free sugar intake of \3.77 % of total energy intake per day (upper limit of G2) was not associated with an increased number of reported caries in this population. However, it is possible that the true threshold is higher than the value suggested above for several reasons. The number of food items included in the BDHQ3y is limited, meaning that sugar intake might have been underestimated. In addition, the positive association observed in the subanalysis was thought to be unstable from G2 (3.18–3.77 % of total energy intake) to G6 (4.88–5.15 % of total energy intake), as the results of the statistical tests at these levels were unstable, that is, some results were significant but
Table 2 Relationship between proportion of energy intake from free sugar and number of decayed or filled teeth reported by guardians (reported caries) among 5158 Japanese preschool children aged 5–6 years: ratios for mean number of reported caries and 95 % CI Proportion of energy intake from free sugara (range; % of total energy intake per day)
n
Whole number of reported cariesb
Q1 (0.95–4.88)
1031
1318
1 (reference)
1 (reference)
Q2 (4.88–6.39)
1032
1504
1.14 (1.06, 1.23)*
1.14 (1.06, 1.23)*
Q3 (6.39–7.89) Q4 (7.89–10.1)
1032 1032
1583 1728
1.20 (1.12, 1.29)* 1.31 (1.22, 1.41)*
1.18 (1.10, 1.27)* 1.28 (1.19, 1.37)*
Q5 (10.1–30.7)
1031
2139
1.62 (1.52, 1.74)*
1.55 (1.44, 1.66)*
Crude ratio of mean number of reported cariesb (95 % CI)
Adjusted ratioc of mean number of reported cariesb (95 % CI)
* Statistically significant at the p B 0.05 level a
Sum of the intake of sucrose, glucose, and fructose added by home cooking and that from confectionaries, ice creams, snacks, chocolates, pastries, sweetened drinks, fruit juice, jam, and seasonings
b
Decayed or filled teeth reported by guardians
c
Ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression
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Matern Child Health J Table 3 Relationship between small proportion of energy intake from free sugar and number of decayed or filled teeth reported by guardians (reported caries) among 2063 Japanese preschool children aged 5–6 years: ratios for mean number of reported caries and 95 % CI Proportion of energy intake from free sugara (range; % of total energy intake per day)
n
Whole number of reported cariesb
G1 (0.95–3.17)
206
234
G2 (3.18–3.77)
206
239
1.02 (0.85, 1.22)
1.03 (0.86, 1.23)
G3 (3.77–4.19) G4 (4.19–4.53)
207 206
277 270
1.18 (0.99, 1.40) 1.15 (0.97, 1.37)
1.22 (1.03, 1.46)* 1.14 (0.96, 1.36)
G5 (4.53–4.88)
206
298
1.27 (1.07, 1.51)*
1.27 (1.07, 1.51)*
G6 (4.88–5.15)
207
242
1.03 (0.86, 1.23)
1.05 (0.88, 1.26)
G7 (5.15–5.46)
206
317
1.35 (1.14, 1.60)*
1.38 (1.17, 1.64)*
G8 (5.46–5.81)
206
310
1.32 (1.12, 1.57)*
1.33 (1.12, 1.58)*
G9 (5.81–6.13)
207
306
1.30 (1.10, 1.54)*
1.31 (1.11, 1.55)*
G10 (6.13–6.39)
206
329
1.41 (1.19, 1.66)*
1.40 (1.18, 1.65)*
Crude ratio of mean number of reported cariesb (95 % CI) 1 (reference)
Adjusted ratioc of mean number of reported cariesb (95 % CI) 1 (reference)
* Statistically significant at the p B 0.05 level a
Sum of the intake of sucrose, glucose, and fructose added by home cooking and that from confectionaries, ice creams, snacks, chocolates, pastries, sweetened drinks, fruit juice, jam, and seasonings
b
Decayed or filled teeth reported by guardians
c
Ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression
Fig. 3 Relationship between proportion of energy intake from free sugar and reported number of decayed or filled teeth (reported caries) in 5158 Japanese preschool children. G1–G25 indicates 25 groups which included almost the same number of subjects (206 or 207 subjects in each group) divided based on the proportion of energy intake from free sugar in the total daily energy intake. G1 is the lowest group (0.95–3.17 %, reference) and G25 is the highest
(15.4–30.7 %). The ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression model and shown in the chart. Significance of the ratios (*p \ 0.05) means that the mean number of reported caries in a certain group is significantly higher or lower than the reference group. The vertical lines on each ratio show 95 % confidence intervals for the ratios
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Matern Child Health J Table 4 Relationship between intake of selected four nutrients and number of decayed or filled teeth reported by guardians (reported caries) among 2063 Japanese preschool children aged 5–6 years: ratios for mean number of reported caries and 95 % CI Intake categories (range)
Crude ratio of mean number of reported cariesa (95 % CI)
Adjusted ratiob of mean number of reported cariesa (95 % CI)
n
Whole number of reported cariesa
Q1 (94.5–255)
1031
2042
1 (reference)
1 (reference)
Q2 (255–306)
1032
1721
0.84 (0.80, 0.90)*
0.86 (0.81, 0.92)*
Q3 (306–360)
1032
1586
0.78 (0.73, 0.83)*
0.81 (0.76, 0.87)*
Q4 (360–444)
1032
1598
0.78 (0.73, 0.83)*
0.82 (0.77, 0.88)*
Q5 (444–1043)
1031
1325
0.65 (0.61, 0.70)*
0.70 (0.66, 0.75)*
Q1 (299–460)
1031
2098
1 (reference)
1 (reference)
Q2 (460–509)
1032
1772
0.84 (0.79, 0.90)*
0.87 (0.82, 0.93)*
Q3 (509–556) Q4 (556–621)
1032 1032
1663 1400
0.79 (0.74, 0.84)* 0.67 (0.62, 0.71)*
0.84 (0.78, 0.89)* 0.72 (0.67, 0.77)*
Q5 (621–1026)
1031
1339
0.64 (0.60, 0.68)*
0.69 (0.65, 0.74)*
1031
1819
1 (reference)
1 (reference)
Q2 (99.3–108)
1032
1617
0.89 (0.83, 0.95)*
0.91 (0.85, 0.97)*
Q3 (108–116)
1032
1645
0.90 (0.85, 0.97)*
0.91 (0.85, 0.97)*
Q4 (116–126)
1032
1552
0.85 (0.80, 0.91)*
0.85 (0.80, 0.91)*
Q5 (126–177)
1031
1639
0.90 (0.84, 0.96)*
0.88 (0.82, 0.93)*
Q1 (0.23–2.24)
1031
1950
1 (reference)
1 (reference)
Q2 (2.24–2.92)
1032
1683
0.86 (0.81, 0.92)*
0.89 (0.83, 0.95)*
Q3 (2.92–3.65)
1032
1592
0.82 (0.76, 0.87)*
0.86 (0.80, 0.92)*
Q4 (3.65–4.82)
1032
1509
0.77 (0.72, 0.83)*
0.82 (0.76, 0.87)*
Q5 (4.82–22.0)
1031
1538
0.79 (0.74, 0.84)*
0.82 (0. 76, 0.87)*
Calcium (mg per 1000 kcal)
Phosphate (mg per 1000 kcal)
Starchc (g per 1000 kcal) Q1 (53.8–99.3)
Vitamin D (lg per 1000 kcal)
* Statistically significant at the p B 0.05 level a
Decayed or filled teeth reported by guardians
b
Ratio adjusted for ‘‘educational background of mother,’’ ‘‘frequency of brushing in the morning,’’ ‘‘frequency of brushing in the evening,’’ and residential area in Poisson regression
c
Residual carbohydrate after subtraction of sugar and dietary fiber
others were non-significant. The statistical significance becomes more consistent for groups G7 and above, we therefore speculate that the possible threshold was around 5 % of total energy intake per day. These results might suggest that the proposed WHO recommendation to lower the limit of energy from free sugar from \10 to \5 % of total energy intake is reasonable. Among our participants, the proportion of children whose sugar intake was\5.00 % of total energy intake per day was 21.8 %, and thus considerably high. One implication of our results is that interventions for dental caries prevention should extend to a range of other strategies in addition to sugar intake reduction, particularly in populations whose mean sugar intake is not so high. Data from 2009 suggest that several other east and southeast Asian countries share Japan’s low sugar supply (Food supply of sugar and other sweeteners
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such as fructose syrup in 2011: Japan, 76; Republic of Korea, 95; Thailand, 79; Philippines, 63 (g per capita per day) [4]. Our present results might accordingly be useful in improving caries prevention strategies in these populations. According to the adjusted ratios of the mean number of reported caries by nutrient, intake of calcium and phosphate was associated with the greatest decrease in the number of caries. Ashley et al. [17] reported that exposure to foods containing dicalcium phosphate increased the concentrations of calcium and inorganic phosphorus in plaque. In addition, several studies showed that higher concentrations of calcium and phosphate in plaque were associated with fewer dental caries [18, 19]. The results of our study are compatible with these studies. In contrast, it is also possible that a higher intake of calcium and phosphate is related to a healthy lifestyle or parental
Matern Child Health J
socioeconomic status. Larson et al. [20] reported that a higher dietary intake of calcium was related to healthier lifestyle (more frequent intake of breakfast and lower intake of sweet drinks and junk food) among students in junior and senior high school in the US. Our addition of ‘‘frequency of teeth brushing in the morning’’ and ‘‘educational background of the mother’’ to the model may have adjusted for the confounding effect of these factors, to some extent at least. In our study, higher intake of vitamin D was also statistically significantly associated with a lower number of dental caries. Hujoel [21] stated that a systematic review of controlled clinical studies showed a significant caries-preventing effect of vitamin D. The results of our study are consistent with it. In addition, our results also showed the relatively weak association between a higher intake of starch and fewer caries. Lingstro¨m et al. [22] stated that the effect of starch intake on the occurrence of dental caries in daily living in humans was uncertain. The anti-cavity effect of starch intake observed in our study might owe to the negative correlation between dietary intake of starch and sugar (r = -0.55; p \ 0.0001), which might suggest that children who have more meals tend to have less sweet snacks and drinks. Several limitations of our study warrant mention. First, since this is the first study to measure dietary intake of sugar in community-dwelling Japanese, the estimation method has not been validated yet. Sugar content is included as carbohydrate in the Standard Tables of Food Composition in Japan [8]. To estimate sugar intake as precisely as possible, we scrutinized other articles describing the sugar content of foods and drinks in Japan, and selected the most reliable chemically analyzed values for each item included in the BDHQ3y. In addition, the BDHQ has satisfactory estimating and ranking ability for carbohydrate intake [9–12], and the child-specific estimation performed with the BDHQ3y shared similar nutritional value calculation algorithms with those of the BDHQ. Besides, the dietary estimation was conducted with the BDHQ3y, which define portion size as fixed, except for the portion size of meat fat and soup of noodle. Though these fixed portion sizes were decided counting the effect from age of children, according to the survey on Japanese children conducted by Asakura et al. [23], it could be possible that misreporting of dietary intake of the children occurred from this characteristics of the BDHQ3y. Second, validity of the number of dental caries reported by guardians in Japan is unknown. Among children in the US, Beltra´n et al. [24] showed that the presence of restored caries estimated by a questionnaire completed by guardians has high sensitivity and specificity, whereas that of untreated caries has low sensitivity and high specificity. On this basis, underreporting was highly possible in our study
but over-reporting was unlikely. However, dental checkup conducted yearly by a dentist, is mandatory in Japanese nursery schools. The guardians are usually aware of the presence of dental carries among their children, as the examination results are reported by the school. Although there might be a possibility that some guardians are indifferent to their children’s oral health and not paying attention to the examination results, the prevalence of reported caries in our subjects was higher than that of decayed or filled caries reported in dental checkup by dentists in the School Health Statistics Research conducted by the Ministry of Education, Culture, Sports, Science and Technology (present study, 52 %; School Health Statistics Research [1], 46 %) which suggested that the likelihood of underreporting was small. In addition, the number of reported caries was collected by the multiple-choice question with six choices in this study. For this characteristic of our study, the accuracy of the number of reported caries might be lower than when the number was asked as continuous variable. However, it is also possible that the categorical choice buffered the effect of misreporting of guardians about the exact number of caries. Third, selection bias is possible in the present study. The children (participants) were not selected randomly, but were volunteers. The guardians of the children might be health-conscious than the general population. However, the educational and physical characteristics of the guardians are supposed to be similar to the general population in Japan. The age-adjusted proportion of married, divorced, or bereaved people whose educational background is junior high or high school in Japan (female: 46.1 %, male: 48.2 %; the 2010 population census in Japan [25]) is almost the same as that of the guardians in our study (mother: 42.6 %, father: 51.1 %). In addition, the mean body height and weight of the general adults in Japan aged 20–59 (female’s height: 157.9 cm, weight: 52.8 kg, male’s height: 171.2 cm, weight 69.7 kg; the 2012 National Health and Nutrition Survey [26]) are similar to those of guardians in our research (mother’s height: 158.2 cm, weight 52.5 kg, father’s height: 171.7 cm, weight 69.2 kg). Thus, the selection bias might be minimal in the present study. Fourth, due to the cross-sectional design of the present study, we cannot exclude the possibility of reverse causality. Children experiencing pain from dental caries or under professional advice to decrease sugar intake to prevent caries are hardly likely to increase sugar intake. If the presence of dental caries does in fact lead to changes in sugar intake in children, this relationship would work to mask the association between higher sugar intake and more caries. Our study found a significantly positive association between a higher number of reported caries and higher proportion of energy intake from free sugar if the
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Matern Child Health J
proportion was over 3.77 % of energy intake per day (higher limit of G2). Even if reverse causality masked the association, the threshold proportion of energy intake from free sugar which produced an increase in the number of caries might be lower than the present result. If so, the WHO’s proposed recommendation to limit energy from free sugar to \5 % of total energy intake remains reasonable. In addition, results of additional analysis which excluded children with a change in dietary habits within the preceding year (n = 761, data not shown) were closely similar to those of analysis which included them. We therefore consider that, if present, the impact of any reverse causality was minimal. Besides, it is also possible that the presence of cavities in the children can cause the reporting bias in the guardians. However, there are possibilities of both under- and over-reporting of sugar intake in the children. When the guardians underreport the sugar intake of their children to hide their poor care, the true threshold of proportion of energy intake from free sugar which produced an increase in the number of caries might be higher. On the other hand, when the amount of sugar intake was over-reported due to recall bias, the true threshold might be lower than that of our result. As described before, effect of underreporting and over-reporting might have been attenuated each other because both were possible in the present study. Thus, the potential for the parent to influence the survey should not be so large. Finally, adjustment for some confounding factors may have been insufficient or absent. In particular, we did not measure several potentially important factors, including fluoride exposure, frequency of snacking, or the percentage of sugar-free products in total dietary intake. Although tap water in Japan is not artificially fluoridated (concentration of natural fluoride—min: \0.05 mg L-1, max: 0.21 mg L-1 [27]), 82 % of Japanese children use fluoridecontaining toothpaste [28]. The preventive effect of fluoride on dental caries might have been partially adjusted for by the addition of ‘‘frequency of teeth brushing in the morning’’ to the model. Johansson et al. [29] reported that the frequency of consuming snacks and drinks was associated with caries status in preschool children. Children who eat snacks more frequently are speculated to consume more sugars, so the participants in higher sugar intake group in the present study might have had more frequent snacking. On this basis, the effect of sugar intake alone on dental caries might have been overestimated, and the true intake threshold for dental caries development might be higher than our estimated value. Moreover, Llena et al. [30] also showed that consumption of sugar-free sweets was not associated with caries experience in 6- to 10-yearold children. In our study, since we did not differentiate sweet drinks with and without sugar, sugar intake might have been overestimated. However, the market share of
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non-sugar sweet drink products in Japan is small (8.1 %) [31]. In addition, Marshall et al. [32] reported that the average intake of sugar-free beverages by children aged 1–5 in the US was zero. It is therefore possible that sugarfree beverage consumption of Japanese children is also small, and the possibility of overestimating sugar intake for this reason is likely small. In conclusion, we found that the association between a relatively low proportion of energy intake from free sugar, at approximately \5 % of total energy intake per day, and an increased number of reported caries among preschool children in Japan was too small to be detected. In contrast, higher intake above this proportion was associated with a higher number of dental caries. The recent proposition of WHO to halve the recommended added sugar intake from 10 % of daily energy intake to 5 % might be valid, though more study will be necessary to examine the effect of relatively low intake of free sugar. Acknowledgments The authors are deeply grateful to the dietitians who assisted the fieldwork, especially to Ms. Yuko Takano, Ms. Machiko Tanaka, and Ms. Yukiko Takahashi, as well as the nursery school staff who facilitated the study. This research was financially supported by the Japan Dietetic Association. Author Contributions Miyuki Saido designed and carried out the analysis and drafted the manuscript. Keiko Asakura edited the manuscript. Shizuko Masayasu designed, prepared, and conducted the dietary survey and arranged the data set. Satoshi Sasaki oversaw the design and analytical strategy of the study. Compliance with Ethical Standards Conflict of interest peting interests.
The authors declare that they have no com-
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