Beruflich Dokumente
Kultur Dokumente
KEY WORDS
Energy density, daily energy intake, daily food
intake, obesity risk status, children, caloric compensation
INTRODUCTION
Am J Clin Nutr 2007;86:417. Printed in USA. 2007 American Society for Nutrition
41
ABSTRACT
Background: Young children adjust their short-term intake in response to variations in energy density (ED; kcal/g) from preloads in
laboratory studies. It remains unknown whether this compensation
also occurs under free-living conditions.
Objective: The aims of the study were to test whether children aged
3 6 y regulate their habitual daily food (g) and energy (kcal) intakes
in relation to ED and whether compensation differs for children born
at different risk of obesity.
Design: Participants were children born at high risk (n 22) or low
risk (n 27) of obesity on the basis of maternal prepregnancy body
mass index (BMI; in kg/m2). Daily ED, food intake, and energy
intake were assessed from 3-d food records that either included or
excluded beverages. Intake regulation was explored by relating childrens daily food and energy intakes to ED and, more importantly, by
examining residual scores derived by regressing daily food intake
on ED.
Results: For both risk groups, daily food intake was inversely correlated with ED (P 0.05), whereas daily energy intake was not
significantly correlated with ED at most ages (P 0.05). In analyses
that excluded beverages, mean residual scores significantly increased from 3 to 6 y of age in high-risk children, which indicates
relative overconsumption, but decreased in low-risk children, which
indicates relative underconsumption (risk group time interaction,
P 0.005).
Conclusions: Children adjusted their daily food intake in relation to
ED, which suggests caloric compensation under free-living conditions. Compensation ability may deteriorate with age in a manner
that favors relative food overconsumption among obesity-prone
children.
Am J Clin Nutr 2007;86:417.
42
KRAL ET AL
Subjects
The subjects in this report were part of an ongoing longitudinal
study of growth and development in early life that has been
conducted at the University of Pennsylvania and the Childrens
Hospital of Philadelphia. The children in this study were born at
either low or high risk of obesity (31). The childrens obesity risk
status was based on maternal prepregnancy body mass index
(BMI; in kg/m2). Infants born to mothers with a prepregnancy
BMI less than the 33rd percentile (mean BMI of 19.5 1.1) were
classified as being at low risk of obesity (n 37). Children born
to mothers with a prepregnancy BMI greater than the 66th percentile (mean BMI of 30.3 4.2) were classified at being at high
risk of obesity (n 35). Children were enrolled in the study at the
age of 3 mo, and their growth and development were followed up
to year 12. All children in the study were white. Further details of
parental and subject characteristics and the study design were
reported previously (3135). The present report is based on a
subsample of this cohort (low-risk: n 27; high-risk: n 22) for
whom 3-d weighed-food records were available at 3, 4, 5, and 6 y
of age. Written informed consent was obtained from the parents.
The protocol was approved by the institutional review boards of
the University of Pennsylvania and the Childrens Hospital of
Philadelphia.
Dietary assessment
Each year, within 2 wk of each childs birthday, the primary
caretakers of children in both risk groups were asked to complete
3-d weighed-food records (2 weekdays, 1 weekend day). Caretakers were provided electronic food scales to preweigh all foods
and beverages (except water) consumed by the child and to weigh
all leftovers. Food records were analyzed by research nutritionists at the General Clinical Research Center at the Childrens
Hospital of Philadelphia by using the Food Processor Nutrition
Analysis software (ESHA Research, Salem, OR). Only those
food records that were completed for 2 d were included in
the present analyses. Two- and three-day food records were
43
Age 3 y
Age 4 y
Age 5 y
Age 6 y
898 47
847 51
939 55
965 57
1064 52
1177 70
1159 45
1393 673
1145 49
1189 59
1219 62
1253 61
1311 58
1493 84
1435 43
1687 69
443 25
395 24
451 30
447 24
466 25
526 34
525 31
620 36
948 45
1062 74
1018 58
1097 58
980 54
1210 90
1104 42
1262 51
2.14 0.10
2.23 0.09
2.23 0.08
2.24 0.11
2.37 0.09
2.36 0.11
2.31 0.08
2.34 0.10
1.26 0.06
1.21 0.07
1.27 0.05
1.19 0.05
1.39 0.06
1.30 0.07
1.35 0.06
1.39 0.09
Risk group was a between-subjects variable with 2 levels (lowrisk or high-risk), and child age was a within-subjects variable
with 4 levels (3, 4, 5, or 6 y). A main effect of risk group would
imply that the tendency to overconsume food differs for high-risk
and low-risk children. Because of the repeated-measures structure of the data, the model used restricted maximum likelihood
estimates and a compound symmetry error structure. Significant
main effects or interactions were followed up by pair-wise comparisons, as well as contrasts, to test for potential linear effects of
time across all 4 ages and linear time by risk group interactions.
Again, these analyses were completed by using intakes that included or excluded all beverages.
The ANOVA model to test aim 2 was run with and without
child BMI z score as a covariate to ensure that any risk group
differences in residual scores were not merely due to differences
in childrens weight status. We identified 2 children in the lowrisk group who, at age 4 y, qualified as statistical outliers per
Tukeys criteria (39) with regard to BMI z score within their
respective risk group. We comment in the Results section that the
outcomes did not change when the outliers were removed.
We adjusted the level by using the Bonferroni correction
(ie, 0.05/n, where n equals the number of comparisons in
a given analysis). We note associations that were significant
both at the conventional 0.05 level as well as when using
the Bonferroni correction because this correction can be
overly stringent (40). We used the same approach in previous
analyses of this cohort (33).
The data were analyzed by using SPSS software (version 12.0;
SPSS Inc, Chicago, IL) and SAS software (version 9.1; SAS
Institute, Inc, Cary, NC). For all analyses, P values 0.05 were
considered statistically significant.
RESULTS
Child characteristics
The number of low-risk children included in the present study
at ages 3, 4, 5, and 6 y were 23 (13 boys, 10 girls), 27 (14 boys,
13 girls), 23 (11 boys, 12 girls), and 22 (8 boys, 14 girls); the
number of high-risk children were 22 (12 boys, 10 girls), 21 (9
boys, 12 girls), 19 (10 boys, 9 girls), and 20 (11 boys, 9 girls),
respectively. The mean (SEM) BMI z scores for high-risk
children were 0.4 0.3, 0.4 0.3, 0.5 0.4, and 0.2 0.3,
and those for low-risk children were 0.4 0.2, 0.1 0.1,
0.1 0.2, and 0.3 0.2 at ages 3, 4, 5, and 6 y, respectively.
Student t tests showed that, at each of the years, none of these
BMI z scores were significantly different between risk
groups. More detailed analyses of anthropometric measures
for this subsample (37) as well as the full cohort (34) are
provided elsewhere.
Daily food intake, energy intake, and energy density
The mean daily food intake (g), daily energy intake (kcal), and
daily energy density (kcal/g) for children in both risk groups at
ages 3, 4, 5, and 6 y are shown in Table 1. These data are
displayed for descriptive purposes only. A detailed discussion of
these results can be found in a previously published paper by Kral
et al (37) that investigated the changes in dietary energy density
in children in this cohort over time.
All values are x SEM. These data were part of a previous publication by Kral et al (37).
2 4 ANOVA indicated a significant (linear) risk group time interaction (P 0.02).
3
Significantly different from the low-risk group, P 0.05.
4
2 4 ANOVA indicated a significant main and linear effect of time (P 0.0001) but no significant risk group time interaction (P 0.19).
5
2 4 ANOVA indicated a significant risk group time interaction (P 0.02).
6
2 4 ANOVA indicated a significant linear effect of time (P 0.0001) but no risk group time interaction (P 0.40).
7
2 4 ANOVA indicated a significant linear effect of time (P 0.03) but no risk group time interaction (P 0.98).
8
2 4 ANOVA indicated a significant linear effect of time (P 0.002) but no risk group time interaction (P 0.58).
1
44
KRAL ET AL
TABLE 2
Pearson correlation coefficients summarizing the relation between dietary energy density and daily food and energy intakes (excluding beverages) by risk
group and child age
Pearsons r with daily energy density (kcal/g)1
Risk group
Low risk
High risk
Low risk
High risk
Daily intake
Age 3 y
Age 4 y
Age 5 y
Age 6 y
0.55
0.405
0.31
0.21
0.49
0.23
0.10
0.503
0.50
0.652,4
0.30
0.13
0.702,4
0.513
0.01
0.29
With the use of Fisher r-to-z transformations and a 2-tailed significance test, none of the correlation coefficients was significantly different within each
age group or across age groups.
2
Correlation significant at 0.01 level.
3
Correlation significant at 0.05 level.
4
P 0.006 (Bonferroni correction, 0.05/8).
5
P 0.06.
Residual analysis
Mean residual food intake scores for each risk group by child
age are displayed in Figure 1. The 2 (risk group) 4 (age)
ANOVA indicated a significant risk group age category interaction (P 0.005) and a linear risk group age (as a continuous variable) interaction (P 0.0005). This interaction was still
significant when applying a Bonferroni-adjusted alpha in the
respective ANOVA models (0.05/3 0.02). Specifically, mean
residual scores increased between ages 3 and 6 y among high-risk
children, reflecting a greater tendency to overconsume food relative to predicted intake, but decreased among low-risk children,
reflecting a greater tendency to underconsume food relative to
predicted intake. A pairwise follow-up comparison indicated that
the mean residual food intake score was significantly greater in
the high-risk children than in the low-risk children at age 6 y
(residual 53.4 137.0 versus 48.5 105.1; P 0.01).
The risk group age interaction remained significant (P
0.02) when BMI z score was added to the model as a covariate.
The main effect of BMI z score was significant in this model
(P 0.04), indicating that heavier children tended to overconsume food (relative to their predicted intake) compared with
thinner children. After removal of the 2 statistical outliers for
BMI z score from the model, the main effect of BMI z score was
not significant (P 0.06); however, the risk group age
interaction remained significant (P 0.02). We note that this
TABLE 3
Pearson correlation coefficients summarizing the relations between dietary energy density and daily food and energy intakes (including beverages) by risk
group and child age
Pearsons r with daily energy density (kcal/g)1
Risk group
Low risk
High risk
Low risk
High risk
1
Daily intake
Age 3 y
Age 4 y
Age 5 y
Age 6 y
0.58
0.692,3
0.28
0.002
0.45
0.494
0.13
0.40
0.64
0.622,3
0.05
0.13
0.782,3
0.612,3
0.26
0.42
2,3
2,3
With the use of Fisher r-to-z transformations and a 2-tailed significance test, none of the correlation coefficients was significantly different within each
age group or across age groups.
2
Correlation significant at 0.01 level.
3
P 0.006 (Bonferroni correction, 0.05/8).
4
Correlation significant at 0.05 level.
UC <---------------> OC
80
60
40
20
0
-20
-40
DISCUSSION
-60
-80
Age (y)
Age (y)
FIGURE 2. Mean residual food intake (food and beverages) scores by risk
group (, low risk; f, high risk) and child age. Residual food intake scores
were generated by regressing the daily food intake (including all beverages)
onto daily energy density (including all beverages). These residuals represent
the difference between childrens actual food and beverage intakes and their
predicted food and beverage intakes for a given energy density based on this
sample. UC, relative underconsumption; OC, relative overconsumption. The
risk group age interaction for residual scores was not significant (P
0.55), nor was the linear risk group age interaction (P 0.38).
The main finding of the present study was that across a range
of ED, children born at high or low risk of obesity adjusted the
daily amount of food they consumed on the basis of the ED of
their diet. Children who consumed a diet that was higher in ED
consumed less food daily than did children whose diet was lower
in ED. These findings held true regardless of whether beverages
were included or excluded. This is the first longitudinal study to
show that children aged 3 6 y also adjust their daily intake under
free-living conditions. These findings thus confirm and extend
previous research conducted under laboratory conditions.
The prospective nature of this design also allowed us to test for
changes in energy regulation ability over time. It has been suggested that developmental differences in energy compensation
ability may exist in children (24). Preschool children, on average,
show compensation (24); however, Anderson et al (41) found no
effect on food intake when varying the ED of preloads in 9 10y-old children. These findings indirectly suggest developmental
changes in compensation ability; however, this phenomenon has
never been documented in long-term prospective studies that
track children during growth.
With the use of a novel approach of residual score analysis, this
present study assessed changes in compensation ability over the
course of 4 y. The results indicated different patterns of residuals
between high- and low-risk children, which suggests that familial predisposition to obesity may partially operate through errors
in compensation. This supports theories and experimental studies regarding energy compensation ability and the development
of pediatric obesity (2224, 42). However, it should be pointed
out that the results from the residual analysis are sampledependent and therefore may not apply to other cohorts of children. The main finding of the residual analysis was that high-risk
children tended to overconsume, whereas low-risk children
tended to underconsume, relative to their predicted intake, although the results differed depending on whether beverages were
included in the analyses. For analyses that excluded beverages,
the risk group differences gradually emerged over time, with
high-risk children not showing a tendency to overconsume until
after 4 y of age. This is consistent with the notion that compensation ability gradually deteriorates during early childhood, possibly starting during the years corresponding to adiposity rebound (43), rather then being compromised consistently and as
early as 3 y of age. This gradual decline in compensation ability
was not seen when beverages were included in the analyses (see
below). Another key finding was that the risk group differences
remained significant even when the analyses were controlled for
BMI z score, which suggests that the errors in compensation
cannot be fully explained by differences in weight status. Again,
this was not the case when beverages were included in the analyses (see below).
When beverages were included in the residual score analyses,
the results indicated a trend (P 0.07) for high-risk children to
FIGURE 1. Mean residual food intake (food only) scores by risk group
(, low risk; f, high risk) and child age. Residual food intake scores were
generated by regressing daily food intake (excluding all beverages) onto
daily energy density (excluding all beverages). These residuals represent the
difference between childrens actual food intake and their predicted food
intake for a given energy density based on this sample. UC, relative underconsumption; OC, relative overconsumption. There was a significant (linear)
risk group age interaction (P 0.005) for residual scores. *Significantly
different from the low-risk group, P 0.01.
UC <---------------> OC
45
46
KRAL ET AL
REFERENCES
1. Livingstone MB. Childhood obesity in Europe: a growing concern. Public Health Nutr 2001;4:109 16.
2. James PT. Obesity: the worldwide epidemic. Clin Dermatol 2004;22:
276 80.
3. Kelishadi R, Pour MH, Sarraf-Zadegan N, et al. Obesity and associated
modifiable environmental factors in Iranian adolescents: Isfahan
Healthy Heart Program - Heart Health Promotion from Childhood. Pediatr Int 2003;45:435 42.
4. al-Nuaim AR, Bamgboye EA, al-Herbish A. The pattern of growth and
obesity in Saudi Arabian male school children. Int J Obes Relat Metab
Disord 1996;20:1000 5.
5. Freedman DS, Srinivasan SR, Valdez RA, Williamson DF, Berenson
GS. Secular increases in relative weight and adiposity among children
over two decades: the Bogalusa Heart Study. Pediatrics 1997;99:420 6.
6. Zametkin AJ, Zoon CK, Klein HW, Munson S. Psychiatric aspects of
child and adolescent obesity: a review of the past 10 years. J Am Acad
Child Adolesc Psychiatry 2004;43:134 50.
7. Kotani K, Nishida M, Yamashita S, et al. Two decades of annual medical
examinations in Japanese obese children: do obese children grow into
obese adults? Int J Obes Relat Metab Disord 1997;21:91221.
8. Lobstein TJ, James WP, Cole TJ. Increasing levels of excess weight
among children in England. Int J Obes Relat Metab Disord 2003;27:
1136 8.
9. Moreno LA, Sarria A, Popkin BM. The nutrition transition in Spain: a
European Mediterranean country. Eur J Clin Nutr 2002;56:9921003.
10. Rolland-Cachera MF, Deheeger M, Thibault H. [Epidemiologic bases of
obesity. ] Arch Pediatr 2001;8(suppl 2):287s9s (in French).
11. Bell EA, Castellanos VH, Pelkman CL, Thorwart ML, Rolls BJ. Energy
density of foods affects energy intake in normal-weight women. Am J
Clin Nutr 1998;67:41220.
12. Bell EA, Rolls BJ. Energy density of foods affects energy intake across
13.
14.
15.
16.
17.
18.
19.
20.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
21.
multiple levels of fat content in lean and obese women. Am J Clin Nutr
2001;73:1010 8.
Kral TVE, Roe LS, Rolls BJ. Does nutrition information about the
energy density of meals affect food intake in normal-weight women?
Appetite 2002;39:137 45.
Rolls BJ, Bell EA, Castellanos VH, Chow M, Pelkman CL, Thorwart
ML. Energy density but not fat content of foods affected energy intake
in lean and obese women. Am J Clin Nutr 1999;69:86371.
Poppitt SD, Prentice AM. Energy density and its role in the control of
food intake: evidence from metabolic and community studies. Appetite
1996;26:15374.
Birch LL, Deysher M. Caloric compensation and sensory specific satiety: evidence for self regulation of food intake in young children. Appetite 1986;7:32331.
Birch LL, Deysher M. Conditioned and unconditioned caloric compensation: evidence for self regulation of food intake by young children.
Learn Motiv 1985;16:34155.
Birch LL, McPhee L, Shoba C, Steinberg L, Krehbiel R. Clean up your
plate: effects of child feeding practices on the conditioning of meal size.
Learn Motiv 1987;18:30117.
Johnson SL, McPhee L, Birch LL. Conditioned preferences: young
children prefer flavors associated with high dietary fat. Physiol Behav
1991;50:124551.
Birch LL, Johnson SL, Jones MB, Peters JC. Effects of a non-energy fat
substitute on childrens energy and macronutrient intake. Am J Clin Nutr
1993;58:326 33.
Fomon SJ, Filer LJ, Thomas LN, Rogers RR, Proksch AM. Relationship
between formula concentration and rate of growth in normal infants. J
Nutr 1969;98:24154.
Cecil JE, Palmer CN, Wrieden W, et al. Energy intakes of children after
preloads: adjustment, not compensation. Am J Clin Nutr
2005;82:302 8.
Johnson SL, Taylor-Holloway LA. Non-Hispanic elementary school
childrens self-regulation of energy intake. Am J Clin Nutr 2006;83:
1276 82.
Birch LL, Fisher JO. Food intake regulation in children. Fat and sugar
substitutes and intake. Ann N Y Acad Sci 1997;819:194 220.
Birch LL, Johnson SL, Andresen G, Peters JC, Schulte MC. The variability of young childrens energy intake. N Engl J Med 1991;324:
2325.
Duncan KH, Bacon JA, Weinsier RL. The effects of high and low energy
density diets on satiety, energy intake, and eating time of obese and
nonobese subjects. Am J Clin Nutr 1983;37:7637.
Lissner L, Levitsky DA, Strupp BJ, Kalkwarf HJ, Roe DA. Dietary fat
and the regulation of energy intake in human subjects. Am J Clin Nutr
1987;46:886 92.
Kendall A, Levitsky DA, Strupp BJ, Lissner L. Weight loss on a low-fat
diet: consequence of the imprecision of the control of food intake in
humans. Am J Clin Nutr 1991;53:1124 9.
Flood JE, Roe LS, Rolls BJ. The effect of increased beverage portion size
on energy intake at a meal. J Am Diet Assoc 2006;106:1984 90.
Mattes R. Fluid calories and energy balance: the good, the bad, and the
uncertain. Physiol Behav 2006;89:66 70.
Stunkard AJ, Berkowitz RI, Stallings VA, Schoeller DA. Energy intake,
not energy output, is a determinant of body size in infants. Am J Clin Nutr
1999;69:524 30.
Faith MS, Berkowitz RI, Stallings VA, Kerns J, Storey M, Stunkard AJ.
47