Published online June 2, 2008
PEDIATRICS Vol. 121 No. 6 June 2008, pp. e1676-e1685 (doi:10.1542/peds.2007-1642)
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ARTICLE

High Sucrose Intake Is Associated With Poor Quality of Diet and Growth Between 13 Months and 9 Years of Age: The Special Turku Coronary Risk Factor Intervention Project

Soile Ruottinen, MSca, Harri Niinikoski, MD, PhDb, Hanna Lagström, PhDc, Tapani Rönnemaa, MD, PhDd, Maarit Hakanen, MDa, Jorma Viikari, MD, PhDd, Eero Jokinen, MD, PhDe and Olli Simell, MD, PhDb

a Research Centre of Applied and Preventive Cardiovascular Medicine, Departments of
b Pediatrics
d Medicine
c Turku Institute for Child and Youth Research, University of Turku, Turku, Finland
e Hospital for Children and Adolescents, University of Helsinki, Helsinki, Finland


    ABSTRACT
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
BACKGROUND. Previous studies have suggested that interventions to lower dietary fat content and improved fat quality lead to a compensatory increase in sucrose content.

OBJECTIVE. The purpose of this work was to determine what associations exist between sucrose intake and intake of nutrients, intake of specific foods, and growth in children aged 13 months to 9 years of age in the prospective, randomized Special Turku Coronary Risk Factor Intervention Project.

SUBJECTS AND METHODS. Nutrient intake and food consumption were evaluated annually at ages 13 months through 9 years by using food records. Altogether, 543 children were divided into 3 groups according to mean sucrose intake: constantly high sucrose intake (highest 10%), constantly low sucrose intake (lowest 10%), and average sucrose intake (80%). Absolute and relative weights and heights were recorded at 7, 13, and 24 months of age and annually thereafter until 9 years old.

RESULTS. The high sucrose-intake group exceeded the recommended sucrose intake (<10% of energy intake, World Health Organization) already at the age of 2 years. Energy and total fat intake did not differ between the sucrose-intake groups. Children with low and average sucrose intake consumed more protein and had a better dietary fat quality than children with high sucrose intake. They also tended to receive more vitamin E, niacin, calcium, iron, zinc, and dietary fiber than children who consumed a high sucrose diet. Children in the low sucrose-intake group consumed more grains, vegetables, and dairy products than the other children. Sugar intake had no direct association with obesity, but weight, height, and BMI of children differed between the sucrose-intake groups between 7 months and 9 years of age.

CONCLUSIONS. In children aged 13 months to 9 years, long-term low sucrose intake is associated with better nutrient intake and growth than high sucrose intake.


Key Words: sucrose intake • children • nutrition • food groups • growth

Abbreviations: STRIP—Special Turku Coronary Risk Factor Intervention Project • E%—percentage of energy intake • ANOVA—analysis of variance • NNR—Nordic Nutrition Recommendations

Sugar contributes to the energy density of the food consumed.1,2 Given that foods rich in sugar may replace other nutrients in the diet, high sucrose intake may adversely influence the nutritional quality of the diet. Excessive consumption of sugar-sweetened drinks by children is associated with obesity,3 but studies regarding effects of children's sugar intake on the displacement of other nutrients and development of obesity have been inconclusive.1,410

There has been a concern that counseling aiming at a low saturated-fat diet might lead to inappropriately increased sugar intake,11 and some studies suggest that an inverse relationship exists between the intake of fat and simple sugars.2,7,12 In the Bogalusa Heart Study, children who, at 10 years of age received <30% of their energy from fat, received more carbohydrates, mainly sucrose, than those whose diets contained >40% fat.13 Recent studies in children have shown that mean sugar intake among children is high compared with the recommendations, and as the dietary sugar intake rises, densities in the diet of several essential nutrients tend to decline.2,7,1419 Nevertheless, several studies show that a reasonable dietary quality is achievable within a wide range of sugar intakes and that the nutritional quality of high-sugar diets may still be adequate regarding the intake of most vitamins and minerals.1,2,14,17,19

This research used a prospective long-term, randomized saturated fat-oriented intervention study to analyze (1) children's sucrose intake from 13 months to 9 years, (2) the effect of sucrose intake on the intake of essential nutrients and consumption of nutrient-dense foods, and (3) whether sucrose intake is associated with growth or weight gain.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study Children
The study design of the Special Turku Coronary Risk Factor Intervention Project (STRIP) has been published previously.2022 Briefly, families for this prospective, randomized, long-term coronary heart disease risk factor intervention trial were recruited by nurses at the well-infant clinics in the city of Turku, Finland, when the child's age was 5 months. Between March 1990 and June 1992, 1054 volunteer families with 1062 infants were enrolled and randomly assigned to form an intervention group (n = 540) or a control group (n = 522).

Our study group consisted of the 543 white urban children (281 boys and 262 girls) who had returned their food records at least at the ages of 13 months and 9 years. Sucrose intake was expressed as a percentage of energy intake (E%). Mean sucrose intake was calculated for every child using all of the available food records (mean: 13[range: 10–15]) between 13 months and 9 years. Because of illness or lack of parental time, occasional food records were missing between ages 2 and 8 years. For this study, the children were divided into 3 different sucrose-intake groups (low, average, or high) according to the recorded mean sucrose consumption between 13 months and 9 years of age. The low sucrose-intake group consisted of children with the lowest mean sucrose intake (10th percentile), the high sucrose-intake group consisted of children with the highest mean sucrose intake (10th percentile), and the average sucrose-intake group consisted of the remaining 80% of children (Table 1). Statistical figures were used to determine the best separation. The proportions of intervention and control children and the number of boys and girls did not differ significantly between the sucrose-intake groups (P > .05); therefore, the intervention and control groups and the genders were combined for additional analysis.


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TABLE 1 Number of Intervention and Control Children and Boys and Girls in the Different Sucrose-Intake Groups

 
The socioeconomic status of the family was analyzed at the child's age of 9 years (range: 8–10 years of age) in the fall of 1999 using a separate questionnaire based on Statistics Finland standards.23 Parental education and the annual income of the family were recorded. Mother's or father's basic education, total duration of education, or annual income of families showed no differences among the sucrose-intake groups (for all: P > .05).

Counseling
The counseling has been described in detail previously.22,2426 In brief, in STRIP, the intervention families received individualized counseling aimed at decreasing the child's intake of saturated fat and cholesterol and at increasing the intake of monounsaturated and polyunsaturated fat at 1- to 3-months interval until the infants were 2 years old and at 6-month intervals thereafter.24,25 When the children reached the age of 7.5 years, direct counseling of the children themselves commenced.26,27 The aims of this counseling were the same as those described previously. The control families received only general dietary information as delivered at Finnish well-infant clinics and in school health care. The control families received no detailed nutritional counseling. Overall, the dietary quality of all of the study children was high except for vitamin D.26

Food Records
All of the families (parents and other caregivers, eg, staff at the day care centers and schools) kept a 3-day food record of their child's food intake every 6 months until the age of 2 years. Later, when the daily variation in the child's diet became larger, food records were kept for 4 consecutive days. After 7 years of age, the intervention children kept food records twice a year but the control children only once a year. The food records included ≥1 weekend day. The records were reviewed by a nutritionist for completeness and accuracy at each follow-up visit. Nutrient intakes were analyzed with the Micro Nutrica program developed at the Research and Development Centre of Social Insurance Institution (Turku, Finland). The program calculates 66 nutrients of commonly used foods and dishes in Finland and includes data on all of the foods commonly consumed by Finnish children. The Micro Nutrica software calculates total carbohydrates, starch, sucrose, lactose, fructose, glucose, and maltose. In this study, total carbohydrate and sucrose intake were analyzed. The data bank is flexible, permitting continuous updating of existing values and the addition of new single or composite foods. Vitamins and minerals consumed as supplements were not included in the calculations.

Measurements of Height and Weight
Weights of the children were measured to the nearest 0.1 kg with an electronic scale (S10 [Soehnle, Murrhardt, Germany]). Recumbent lengths of the children younger than 2 years were recorded, and, thereafter, standing heights were measured to the nearest millimeter with a wall-mounted Harpenden stadiometer (Holtain, Crymych, United Kindom). Weights and heights were plotted on the Finnish growth charts.28 Height, relative height (deviation of height in SD units from the mean height of healthy Finnish children of the same age and gender), weight, and relative weight (deviation of weight in percentages from the mean weight of healthy Finnish children of the same height and gender)28 were recorded. BMI was calculated as kilograms per meter squared.

Ethics
The joint commission on ethics of the Turku University and the Turku University Central Hospital approved the STRIP. Informed consent was obtained from the parents of the children at the beginning of the trial.

Statistical Analyses
Long-term associations of sucrose intake with nutrient intake and growth were analyzed with repeated-measures analysis of variance (ANOVA) models using a backward selection method (exclusion criteria: P > .1), including sucrose-intake group, STRIP group, age, and the interaction of these as explanatory variables. The proportions of children receiving less of nutrients than recommended in the Nordic Nutrition Recommendation (NNR)28 were analyzed with the Cochran-Mantel-Haenszel method. Socioeconomic status data were analyzed with the Fisher's exact test and with the Cochran-Mantel-Haenszel method. The Fisher's exact test was used to study differences between genders in the groups. SAS 9.1 (SAS Institute, Inc, Cary, NC) was used for data analysis. The level of statistical significance was set at a P value of <.05.


    RESULTS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Sucrose Intake
The mean sucrose consumption of the children in the high sucrose-intake group exceeded the maximum recommended intake (10 E%) by the current NNR29 and the World Health Organization30 in all of the food records after the age of 13 months (Fig 1). The mean sucrose intake of the average-intake group was close to but never exceeded 10 E%. The sucrose-intake values of the boys and girls showed no differences (data not presented).


Figure 1
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FIGURE 1 Sucrose intake of children with high (broken line with circles), average (solid line with triangles), and low (solid line with squares) sucrose intake between 13 months and 9 years of age. Data are mean (SD) values. The P value for the group effect by time is <.001 (repeated-measures ANOVA).

 
Nutrient Intake and Food Group Consumption
There were no differences in energy intake and total fat intake expressed as E% or grams per day among the 3 sucrose-intake groups. However, the children with low sucrose intake received continuously more polyunsaturated and monounsaturated fatty acids and less saturated fat than the children with high sucrose intake (E%; Table 2). The children in the low sucrose-intake group also received more protein than children in the high sucrose-intake group when expressed as E% (Table 2) or as grams per day (data not shown).


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TABLE 2 Daily Consumption of Energy and Energy Nutrients According to Children in Groups With Low, Average, or High Sucrose Consumption

 
The children with low sucrose intake tended to receive more vitamin E, niacin, calcium, iron, and zinc than the children with high sucrose intake (Table 3). An exceptional vitamin was vitamin C, which showed no differences between the groups. The children with low sucrose intake also received more dietary fiber than the other children (Table 3). The proportion of children receiving less vitamin B1 (P < .05), pyridoxine (P < .001), iron (P < .001), zinc (P < .001), magnesium (P < .001), and calcium (P < .01) than recommended in the NNR29 was constantly higher in the high sucrose-intake group than in the other 2 sucrose-intake groups (data not shown).


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TABLE 3 Daily Consumption of Selected Vitamins, Minerals, and Dietary Fiber Relative to Energy Intake According to Children in Groups With Low, Average, or High Sucrose Consumption

 
The children in the low sucrose-intake group consumed more grain, vegetables, dairy products, and meat and fish than the other children (Table 4), whereas the children in the high sucrose-intake group consumed more juices, candies, soft drinks, and sugared dairy products (Table 5). The most common sources of sucrose in the low sucrose-intake group were fruits and berries, whereas children with high sucrose intake received most sucrose from sugared dairy products and soft drinks (Fig 2).


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TABLE 4 Daily Food Consumption of Selected Food Groups According to Children in Groups With Low, Average, or High Sucrose Consumption

 

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TABLE 5 Daily Food Consumption of Selected Food Groups According to Children in Groups With Low, Average, or High Sucrose Consumption

 

Figure 2
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FIGURE 2 Sources of sucrose as percentages of sucrose intake in children with high (broken line with circles), average (solid line with triangles), and low (solid line with squares) sucrose intake at 9 years of age.

 
Height and Weight
The children with high sucrose intake were taller than the other 2 groups of the children during the first 6 years of the study, whereas the children with low sucrose intake were taller than the children in the other 2 groups between 7 and 9 years of age. The mean height of the children with low sucrose intake increased from 70.0 cm at 7 months to 136.6 cm at 9 years, whereas the respective values were 70.3 cm to 136.0 cm in the children with average sucrose intake and 71.3 cm to 136.4 cm in children with high sucrose intake (P < .05 between groups; Fig 3). Thus, the difference in growth between 7 months and 9 years of age was 1.5 cm between the low sucrose-intake group and the high sucrose-intake group. A similar pattern was seen in the mean relative heights (P < .001; Fig 4). The children with high sucrose intake weighed more during the first few years of the study, whereas, after 4 years of age, their weights were less than those of the children in the other groups (P < .05; Fig 5). A similar pattern was seen with weight for height (P < .001; Fig 6). The BMI of children also differed between the sucrose-intake groups between 7 months and 9 years of age; the P value for the group effect by time was <.001 (Fig 7).


Figure 3
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FIGURE 3 Height of children with low (white bars), average (gray bars), and high (black bars) sucrose intake between 7 months and 9 years of age. Data are mean (SD) values. The P value for the group effect by time is <.05 (repeated-measures ANOVA).

 

Figure 4
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FIGURE 4 Mean relative height of children with high (broken line with circles), average (solid line with triangles), and low (solid line with squares) sucrose intake between 7 months and 9 years of age. The P value for the group effect by time is <.0001 (repeated-measures ANOVA).

 

Figure 5
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FIGURE 5 Weight of children with low (white bars), average (gray bars), and high (black bars) sucrose intake between 7 months and 9 years of age. Data are mean (SD) values. The P value for the group effect by time is <.05 (repeated-measures ANOVA).

 

Figure 6
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FIGURE 6 Mean relative weight (percentage deviation from mean weight) of children with high (broken line with circles), average (solid line with triangles), and low (solid line with squares) sucrose intake between 7 months and 9 years of age. The P value for the group effect by time is <.0001 (repeated-measures ANOVA).

 

Figure 7
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FIGURE 7 Mean BMI of children with high (broken line with circles), average (solid line with triangles), and low (solid line with squares) sucrose intake between 7 months and 9 years of age. The P value for the group effect by time is <.001 (repeated-measures ANOVA).

 

    DISCUSSION
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In this prospective, long-term study, the children with low sucrose intake consumed foods that were more nutrient dense and, thus, had better dietary quality and higher intake of vitamins and minerals than the children with high or average sucrose intake. The children with low sucrose intake also had higher protein intake, and their fat quality was better than in the children with high or average sucrose intake. Furthermore, the children with low sucrose intake grew better than the children with higher sucrose intake. High sucrose intake was not associated with obesity, because the children with high sucrose intake were lighter than other children after 4 years of age.

Sucrose intake in the high sucrose-intake group exceeded the recommended upper limit (10 E%)29,30 already at 2 years of age. Interestingly, in the United States, the upper limit for added sugar intake is 25% of total energy (Dietary Reference Intakes 2005).31 When comparing our results with intakes reported in other studies in the Nordic countries, the sucrose intake in our study was not high. In Norway, the added sugar intake was 15 E%, 17 E% and 18 E% in 4-, 9-, and 13-year-old children, respectively,32 whereas it was 12 E% in Swedish 4-year-old children33 and 14 E% in Danish children aged 4 to 14 years.16 The mean intake of added sugars of children and adolescents between ages 1 and 18 years was 12 to 14 E% in 3 recent German studies.15,18,34 Even higher sugar intakes have been reported in children, as intake of nonmilk extrinsic sugars in Great Britain approximated 19 E%,2 and in the United States, added sugar intake was 16 to 17 E% in 2- to 5-year-old children19,35 and 18 E% in 6- to 11-year-old children.35 However, comparison between sugar intakes in different studies is complicated by differing definitions of "sugar." Added sugars, together with sugars in fruits, berries, and fruit juices, are considered to form the group "sugar." Although the naturally occurring sugars and added sugars were not separated in our study, even the children with high sucrose intake in our study consumed less sugar than children in the above-mentioned studies.

Some earlier studies have suggested that a high-sugar diet might lead to high intake of fat.36 On the other hand, in other studies,13,37 children whose diet contained <30 E% of fat have had a higher intake of sugar than those with a higher fat intake. Furthermore, a positive correlation between sucrose and energy intakes has been reported,2,7,15 and children with low consumption of sugar have consumed more total fat.38 However, in the STRIP cohort, we found no correlation between the intake of fat and sucrose, and also the differences in total energy intake between the different sucrose-intake groups were nonsignificant. Instead, in our study, the children with low sucrose intake had a better quality of dietary fat, that is, they consumed more polyunsaturated and monounsaturated fatty acids and less saturated fatty acids than the children with high sucrose intake. Previous STRIP studies have also shown that lower fat intake does not lead to compensatorily higher sucrose intake.24,26

In the Dortmund Nutritional and Anthropometric Longitudinally Designed Study,18 it was found that added sugars led to a slight but significant nutrient dilution effect. The intakes of important nutrient-bearing food groups were also reduced when sugar intake increased.18,19 Intake of many essential micronutrients and macronutrients, especially of protein, fiber, vitamin A, vitamin B12, folate, magnesium, and iron, decreased as sugar intake increased.19,39 In the study of Forshee and Storey,17 the children who consumed more added sugars also consumed more grain, vitamin C, iron, and folates and consumed less dairy products, but the associations were weak. In our study, the nutrient dilution effect of high sucrose intake was also small but significant, but the changes in micronutrient intakes and food consumption associated with high sucrose intake were strikingly almost the opposite of the changes observed in the Forshee and Storey17 study.

Although sugared dairy products were common sources of sucrose, consumption of milk and dairy products was constantly lower in the children with high sucrose intake than in those children with low sucrose intake. Thus, children with high sucrose intake received less calcium than recommended in the NNR at 9 years of age.29 Soft drinks contribute strongly to the sugar intake of American children19,40 so that calcium intake decreases when consumption of sugar-sweetened beverages or sugar intake increases.19,41 The replacement of milk and milk products with soft drinks also probably happened in our study, although consumption of soft drinks was less than in earlier studies. Taken together, our results parallel those of Frary et al,41 suggesting that sugar intake of children correlates negatively with calcium, iron, and dietary fiber intake and positively with intake of saturated fat.

Accurate recording of children's food consumption is problematic. The primary concern relates to conscious underreporting, because consumption of fat and sugar is often considered unhealthy.42 However, Lillegaard and Andersen43 concluded that, in 9-year-old children, neither underreporters nor acceptable reporters showed a systematic misreporting related to unhealthy foods or macronutrients and that added sugar intake as E% was not significantly different between underreporters or acceptable reporters.44 The level of estimated underreporting rises significantly with age and is presumably higher among overweight individuals than among those with normal weight.45,46 Therefore, it is possible that the lack of association between sugar intake and obesity in studies may partially be because of underreporting. In our study, the reporting was done by children and their parents. Underreporting of sugar intake is unlikely in our study, because the main interest in STRIP was the amount and quality of fat. Furthermore, previous studies suggest that underreporting is not a problem in young children.47,48

The levels of parental education and/or social background and sucrose intake did not correlate, although previous studies have shown an association between these factors.4952 One possible explanation for this is that the families of the STRIP volunteered to participate in the study, and, thus, they may have had a more positive health attitude than average people in the community.

Most previous studies in children and adults have revealed no direct associations between sugar intake and obesity.6,7,38,53 Indeed, the US Department of Agriculture54 concluded recently that current evidence does not necessarily indicate sugar as the culprit for the observed obesity trend. Conversely, sugar intake seems to have a weak negative association with BMI in adults5356 and in children,38,57 and this association cannot be explained completely by confounding factors such as dieting, underreporting, or the inverse correlation between energy from sugar and fat.38,53,57 In a recent Norwegian study, a negative association was found between consumption of added sugars and BMI among 13-year-old girls, whereas this association was positive among 4-year-old boys.32 We also observed an age-dependent association between growth and sucrose intake, because between the ages of 1 and 3 years, those children with high sucrose intake weighed more than the children with average or low sucrose intake, but the opposite was seen after 4 years of age. The relative gender and height-adjusted weights of the children with high sucrose intake decreased with age, but the differences in energy or total fat intake failed to explain differences in the growth. Instead, sucrose was substituted with protein in the diet, because the children with low sucrose intake received more protein than the children with high sucrose intake. Garemo et al33 suggested that higher protein intake might also be more favorable, thus contributing to a higher degree of satiety and thus preventing obesity. In our study, the protein intake of all of the children was rather high (15–18 E%; recommendation: 10–20 E% in NNR29), and all of the children showed normal growth. High sucrose intake might also relate to other lifestyle factors that could affect growth. For example, American culture and diet are associated with increased height.58 In this study, we did not investigate the effects of children's physical activity or behavior on sucrose intake or vice versa.

Our results clearly show that long-term excessive sucrose intake worsens the quality of dietary fat, although it does not affect its amount in the diet. High sucrose intake also has a slight dilution effect on micronutrient content. Sucrose replaces dairy products, grain, and other micronutrient-dense foods in the children's diet and, thus, high sucrose intake also associates with lower protein intake. Our results suggest that high sucrose intake might even slightly affect growth.


    CONCLUSIONS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In this prospective long-term study, long-term low sucrose intake in children aged 13 months to 9 years was associated with better nutrient intake and growth when compared with high sucrose intake.


    ACKNOWLEDGMENTS
 
This study was supported by the Finnish Cultural Foundation, the Varsinais-Suomi Regional Fund, the Juho Vainio Foundation, the Academy of Finland (grant 206374), and the Finnish Cardiac Research Foundation.

We thank Maiju Saarinen for statistical analysis, Pekka Heino for assistance with data management, and Soile Kotilainen and Asta Myyrinmaa for dietary counseling and recording of the food intake of the study children.


    FOOTNOTES
 
Accepted Dec 12, 2007.

Address correspondence to Soile Ruottinen, MSc, Research Center of Applied and Preventive Cardiovascular Medicine, University of Turku, Kiinamyllynkatu 10, FI-20520 Turku, Finland. E-mail: soile.ruottinen{at}utu.fi

The authors have indicated they have no financial relationships relevant to this article to disclose.

This trial has been registered at www.clinicaltrials.gov (identifier NCT00223600).


What's Known on This Subject

Given that foods rich in sugar may replace other nutrients in the diet, high sucrose intake may adversely influence the nutritional quality of the diet. Excessive consumption of sugar in children might be associated with obesity.

 

What This Study Adds

We have found that, in a prospective long-term study, in children aged 13 months to 9 years, long-term low sucrose intake is associated with better nutrient intake and growth than high sucrose intake. A new finding was that sucrose was associated with height.

 


    REFERENCES
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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K. Casazza and O. Thomas
Do Dietary Modifications Made Prior to Pubertal Maturation Have the Potential to Decrease Obesity Later in Life? A Developmental Perspective
ICAN: Infant, Child, & Adolescent Nutrition, October 1, 2009; 1(5): 271 - 281.
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