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The Federal University of São Paulo, Escola Paulista de Medicina, São Paulo, Brazil and * The Jean Mayer U.S. Department of Agriculture Human Nutrition Research Center on Aging at Tufts University, Boston, MA 02111
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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EI:
+460 ± 1574 vs. -103 ± 1916 kJ/d, P = 0.25). These data provide preliminary evidence consistent with the
suggestion that stunted children tend to overeat opportunistically, but
further studies are required to confirm these results in a larger
study.
KEY WORDS: • humans • energy intake • malnutrition • hunger • satiety
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, WHO 1997
). Countries in economic transition from developing to
developed, such as China, Brazil and South Africa, are particularly
affected and have an increasing prevalence of obesity across all
economic levels and age groups (Popkin 1994
).
Traditional explanations for these observations include reduced
physical activity and consumption of high fat diets (Popkin 1994
). However, no consensus exists over the importance of
these factors even in developed countries (Blair 1993
,
Garrow 1995
, Roberts et al. 1998
,
Willett 1998
, Wilmore et al. 1999
).
Research by two independent groups has recently suggested a role for
childhood undernutrition in the increasing prevalence of adolescent and
adult obesity in developing countries. In particular, nutritional
stunting (an indicator of chronic childhood undernutrition [see
Must (1999)
and Waterlow (1992)
] has
been reported to increase the risk of obesity in adolescents and adults
in several studies worldwide (Monteiro et al. 1992
,
Popkin et al. 1996
, Sawaya et al. 1995
,
Schroeder et al. 1999
). There is also some evidence that
women may be particularly susceptible to the influence of stunting on
the risk of obesity. One recent investigation observed a 35%
prevalence of obesity among stunted adolescent girls compared with an
11% prevalence among stunted adolescent boys (13 and 8% among
nonstunted adolescent boys and girls, respectively, living in the same
population) (Sawaya et al. 1995
). Currently, however,
little is known about the underlying mechanisms linking stunting and
later obesity.
In studies conducted in shantytowns in São Paulo, Brazil, we
recently identified impaired fat oxidation as one mechanism that may
contribute to excess weight gain over time in stunted adolescents and
adults (Hoffman et al. 2000a
). We also observed
decreased total energy expenditure in girls compared with boys after
accounting for differences in body composition, a factor that may help
to explain the higher prevalence of obesity among stunted adolescent
girls and women compared with men (Hoffman et al. 2000b
). The regulation of food intake is another major factor
that may potentially contribute to energy disregulation in stunted
individuals. Impaired regulation of energy intake has the potential to
be more important quantitatively than either decreased energy
expenditure or reduced fat oxidation. This is because energy intake
usually varies substantially on a day-to-day basis (Edholm et al. 1970
), and the capacity for overeating is large
(Bouchard et al. 1990
, Roberts et al. 1990
) compared with the observed magnitude of decreases in
energy expenditure in response to different physiologic stimuli
(Saltzman et al. 1997
). In general, infants and children
are thought to regulate energy intake more precisely than adults, with
tighter meal-to-meal regulation of energy intake (Birch et al. 1991
, Edholm et al. 1970
) and a stronger ability
to compensate for alterations in dietary energy density by adaptive
variations in food quantity (Fomon 1993
, van Stratum et al. 1978
). We therefore hypothesized that a
decreased ability to regulate energy intake in childhood (whether of
biological or psychological origin) could contribute to an increased
risk associated with nutritional stunting in developing countries; in
particular, we identified an increased tendency to overeat
opportunistically as an important focus for investigation.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Children (n = 56) were selected from population
surveys of three shantytowns in the city of São Paulo, Brazil.
More than 300 children aged 8–11 y old were weighed and measured to
determine their eligibility for the study. All study participants had
to have a weight-for-height Z-score
(WHZ)4
< 2.0 according to the National Center for Health Statistics
standards. Children recruited for the stunted group had a
height-for-age Z-score (HAZ) -1.50 or below and those for the
control group had HAZ above -1.50. In addition, the two groups were
matched for age, gender balance and WHZ. Although it was not possible
to match stunted and control children for parental height and weight,
these values were measured in all families in which the biological
parents lived with the children; there were no significant differences
between the groups in parental height or body mass index (BMI)
(Table 1
).
|
),
blood collection for glucose and hemoglobin levels, and fecal and urine
screening for acute infection. Children were excluded from the study if
they were taking any medication, if Tanner staging for more than one
criterion was > 1, or if any past medical problems were
identified that might influence current health status and/or metabolic
condition (such as hyperthyroidism or chronic anemia). Any child that
presented with acute health problems such as intestinal or urinary
infections was treated according to the usual procedure of the
São Paulo Hospital and began the study only after successful
completion of treatment. Ethical approval for the study was obtained from Federal University of São Paulo Hospital and Human Investigations Review Board at the New England Medical Center, Tufts University, and written informed consent was obtained from both the children and their parent(s) before the start of the study.
Procedures.
The children were studied in groups of 4 (because of practical reasons and also because being studied alone would have perhaps had very adverse effects on food intake); they were collected from their homes by car at 0700 h on study d 1 and returned at 2030 h on study d 3. The study was conducted in the Metabolic Research Unit of the Center for Nutritional Recovery and Education at the Federal University of São Paulo, and continuous supervision of the children was provided by the investigators during the day (D.H., C.N. and P.M.) and by a nurse at night.
On arrival at the research center on study d 1, the children were
weighed and measured and had blood drawn for fasting glucose and
hormone assays (data not shown). Energy intake (EI) was determined
throughout the 3-d study, and resting energy expenditure (REE) was
measured each morning. In addition the thermic effect of feeding was
measured over 3 h on one morning as described elsewhere
(Hoffman et al. 2000a
). The children were required to
remain at the center throughout the study and refrain from vigorous
activity. They were allowed to watch videos both during testing and
other times, and participate in activities that required mild physical
activity (playing catch, hide-and-seek and drawing). In an outpatient
component of the study described elsewhere, body fat and fat-free
mass (FFM) were also measured by dual X-ray absorptiometry.
Menus and measurement of food intake.
Breakfast, lunch and dinner consisted of the same foods on each study
day to minimize the effects of different daily menus and individual
food preferences on EI. The menus were based on the usual foods eaten
by this population, and a list of the foods served and the schedule of
meals and snacks is shown in Table 2
. The only beverage allowed at meals other than those listed in the
table was water. Meals and snacks were prepared daily by the staff of
the metabolic research unit, and meals were served at fixed times each
day with the children eating together around a small table. Snacks were
served upon request (this occurred in 
70% of children with no
difference between genders and groups) during a 2-h period in the
afternoon.
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Breakfast was provided in fixed amounts based on body weight (42 kJ/kg body weight, with 15% of energy from fat, 35% from protein and 50% from carbohydrate); however, at lunch and dinner, children served themselves from a buffet that contained more of each item than the subjects could eat. The order in which the children first approached the table was rotated on a meal-by-meal basis. A standard instruction form was read out to the children at the start of the study explaining that they could take as much or little of each item as they chose, and could (and usually did) have additional helpings as desired. Food weights were determined by weighing plates before use, after the child’s addition of each food from the buffet and at the end of meal. Foods that were mixed together during the meal were separated and reweighed individually after the meal.
On one study day, the effect of a supplement given at breakfast on total daily EI was evaluated. This procedure consisted of giving each child a small cup of yogurt (753 kJ) 2–3 min after breakfast that was to be consumed completely. The supplement days were organized so that an equal number of children from each group (i.e., stunted versus nonstunted) consumed the yogurt on each day of the 3 d. This was done to minimize possible day bias. Two stunted children did not participate in this measurement.
Daily energy intakes were determined from the macronutrient content of each food and calculated recipe using a Brazilian food data base (NUTRI, Nutritional Content Database, Federal University of São Paulo). The macronutrient content of commercial foods was obtained by calculation from recipes after contacting the manufacturer directly.
Measurement of resting energy expenditure (REE) and body composition.
REE was measured as described previously (Hoffman et al. 2000b
). Briefly, after an 12-h fast, REE was measured on
three occasions under thermoneutral conditions by indirect calorimetry
using a DeltaTrac metabolic monitor (SensorMedics, Yorba Linda, CA).
Subjects were instructed to lie prone, relax and avoid
hyperventilation, fidgeting and sleeping during the measurements. The
calorimeter was calibrated using a standard gas mixture (96%
O2/4% CO2) before each measurement and alcohol
burn tests were conducted every 2 wk to ensure the accuracy of the
calorimeter. Values for REE were determined from values for
VO2 and VCO2 on each measurement day (de Weir 1949
); the mean of the 3 d was used in data analysis.
Height and weight were measured as described elsewhere (Hoffman et al. 2000a
). Fat mass and FFM were measured by
dual-energy X-ray absorptiometry using a Hologic X-ray
densitometer (Hologic, Bedford, MA) with an adult quick-scan
program that was shown to be accurate for this age and weight group
(Hoffman et al. 2000a
).
Data analysis.
Values are expressed as means ± SD and means ± SEM as noted. Differences in 3-d average energy and macronutrient intakes between nonstunted and stunted boys and girls were assessed with ANOVA. The EI response at lunch and throughout the day to the energy supplement was determined by first calculating differences in EI between the supplement day and control days, and then using ANOVA to compare this difference among stunted and nonstunted boys and girls. A second analysis was performed to test the possible influence of the particular day on which the supplement was provided on changes in EI across the 3 d. This was done using repeated-measures analysis of covariance, controlling for supplement day (d 1, 2 or 3). All data were analyzed using SPSS for Windows (Version 7) and Systat for Windows (Version 7.0) (SPSS, Chicago, IL). Differences were considered significant at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The physical characteristics of the subjects are summarized in Table 1
.
There were no significant differences between the groups in gender
breakdown, age and WHZ. The nonstunted group was taller, had a greater
HAZ, and, consequently, a greater weight compared with the stunted
group. There was no difference in body fat expressed as a percentage of
body weight between the two groups; in addition, the parents of each
group that were available for measurement did not differ in either
height or BMI (Table 1)
.
Energy intake.
There was no significant trend in EI over the 3-d study in either
stunted or nonstunted children (Fig. 1
). Body weight was the single best predictor of EI (Fig. 2
; FFM and REE also significantly predicted EI in all subjects combined
but with lower significance values, data not shown). In multiple
regression models including weight as an independent variable, stunting
was not a significant independent predictor of EI, although there was a
tendency for stunted children to have a greater EI (P = 0.12). In addition, there was no significant interaction between
stunting and weight in the prediction of EI. However, although total
daily EI did not differ between stunted and nonstunted boys and girls
(P = 0.98), EI/kg body and EI/REE were significantly
higher in stunted boys and girls than in controls (Table 3
). There was no significant influence of gender in models predicting EI
and including weight. Mean values for EI/kg in the stunted and
nonstunted boys and girls combined were 324 ± 10 and 266 ± 13 kJ/kg (P < 0.05), and mean values for EI/REE were
1.91 ± 0.34 and 1.68 ± 0.38 (P < 0.05).
The CV for day-to-day variability in EI was not influenced by stunting,
but was significantly higher in girls compared with boys.
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The effect of the supplement given after breakfast on EI at lunch and
throughout the whole day was determined by analyzing the difference in
EI between supplement and control days (for total daily EI and lunch
intake only). There was no significant effect of the supplement on EI
either at lunch of throughout the whole day (Table 4
). In stunted boys and girls combined, the absolute mean EI on
supplement days was higher than the mean EI on nonsupplement days in
the stunted children but lower in the nonstunted children. However, the
difference between groups was not significant (EI: +460 ± 1574
vs. -103 ± 1916 kJ/d, P = 0.25).
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|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, WHO 1997
). This increase may be attributed
potentially to several social and/or environmental factors. For
example, many countries in economic transition have experienced a shift
in dietary habits from traditional low fat foods to the Western high
fat foods (Popkin 1994
) that are associated with high EI
and obesity in some (Hill et al. 2000
) but not all
(Willett 1998
) analyses of data from developed
countries. In addition, as traditionally poor countries develop, there
is a trend for individuals living in rural areas to migrate to urban
districts; this shift is associated with a reduction in physical
activity that is a further risk factor for obesity (Popkin 1994
). Although changes in diet and/or physical activity may
affect the overall population, it has been reported that socially
disadvantaged groups in developing countries, who typically continue to
eat low fat diets and perform high levels of physical activity, are
also becoming obese (Popkin et al. 1996
, Sawaya et al. 1995
). Indeed, recent studies have asked whether
undernutrition early in life may promote obesity later in life, thus
contributing to the escalating prevalence of obesity in developing
countries (Popkin et al. 1996
, Sawaya et al. 1995
). However, there has been little direct evidence on which
to accept or reject this possibility. We tested the hypothesis that chronic childhood undernutrition severe enough to cause mild stunting increases the susceptibility to obesity by altering the regulation of food intake. In particular, we investigated the extent to which stunted children tend to overeat opportunistically compared with nonstunted children in an environment in which meals and snacks are readily available. We also examined the ability of the children to compensate for a food supplement given at breakfast by decreased EI at meals and snacks consumed later in the day. By selecting stunted and nonstunted children from the same communities, and ensuring that the groups had similar values for parental heights and BMI, we reduced the number of alternative factors that could potentially explain our results.
Under the conditions of this study, EI/kg body and EI/REE were significantly higher in stunted children compared with nonstunted controls, a finding that is strongly suggestive of opportunistic overeating. In addition, in the supplement component of the study, stunted children did not tend to compensate for the additional 753 kJ given at breakfast, with the result that the mean daily EI increased on the supplement day relative to the control days; this trend was not apparent in the nonstunted children. However, the difference between the groups was not significant (P = 0.25), perhaps because of the high within-subject variability in daily EI or because increased EI at breakfast does not affect lunch and dinner intake in young children. Nevertheless, the combination of all of the study data suggests that opportunistic overeating may have occurred in the stunted children under some circumstances. Further studies with larger groups of subjects are required to confirm and extend the results obtained here.
Several potential explanations exist for the influence of stunting
(whether of prenatal or postnatal origin, which our study does not
distinguish) on the regulation of EI. In particular, our recent
observation of impaired fasting fat oxidation in stunted children
compared with nonstunted controls may be relevant. According to the
energy regulation theory of Flatt (1995)
, a depletion of
carbohydrate stores in the body is a signal for hunger. Thus, if fat
oxidation is impaired but energy expenditure is normal, as observed in
our stunted children (Hoffman et al. 2000a
),
carbohydrate oxidation is increased, leading to the more rapid
depletion of carbohydrate stores and increased hunger. Theoretically,
consumption of a high fat diet should increase the susceptibility of
stunted children to hunger and overeating, by further reducing
carbohydrate intake and hence carbohydrate stores. This suggestion is
entirely consistent with our previous observation of accelerated weight
gain during puberty among those stunted children who consume high fat
diets (Sawaya et al. 1998
).
Other factors associated with childhood stunting may also have been
important. In controlled underfeeding studies in young adults, a period
of enforced undereating is followed typically by prolonged hyperphagia,
which causes more weight gain and fat gain than the amount lost during
underfeeding (Roberts et al. 1994
). Undernutrition in
childhood of a magnitude required to cause stunting may have a similar
effect on EI also. Whether overeating associated with previously
inadequate EI is due to underlying metabolic changes or to behavioral
factors is not known, and the long-term psychological effects of
food security on eating patterns may have as much importance
potentially as any persistent metabolic effects. It is important to
note here that generalized behavior patterns developed during early
childhood tend to persist over time (Birch et al. 1984
,
Deheeger et al. 1994
); thus patterns of opportunistic
overeating developing during the prolonged undernutrition necessary to
cause stunting may represent at least one component of the explanation.
Although some of the tendency to overeat opportunistically may arise
within the children themselves, it can be speculated that parents may
also be influential. For example, children who experience high parental
control over their food choices and intake have impaired regulation of
EI and an increased tendency to gain weight compared with children with
little parental control (Johnson and Birch 1994
).
Although it was beyond the scope of our study to determine how parental
control differed between the stunted and control groups, undernutrition
can be compared with high parental control of food. Similar to the
child with an overcontrolling parent, the child with insufficient
access to quality food and a low degree of food security may be
affected by the inability to exercise free expression of his or her
choice in the quality and quantity of food.
In summary, the results of this study suggest that, compared with nonstunted children, stunted children living in the same communities may regulate their EI less well, with the direction of the disregulation increasing their risk for excess weight gain over time. Stunted children may thus be at increased risk for overeating, leading to obesity when environmental conditions are favorable. Further studies are warranted in previously malnourished children and their families to confirm the preliminary results of this study and to examine the effect of stunting on the regulation of food intake in more detail.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 To whom reprint requests should be addressed.
4 Abbreviations used: BMI, body mass index; EI, energy intake; FFM, fat-free mass; HAZ, height-for-age Z-score; REE, resting energy expenditure; WHZ, weight-for-height Z-score.
Manuscript received November 1, 1999. Initial review completed January 26, 2000. Revision accepted May 17, 2000.
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