CLINICS 2010;65(2):181-7

CLINICAL SCIENCE

EARLY WEANING AND OTHER POTENTIAL RISK

FACTORS FOR OVERWEIGHT AMONG PRESCHOOL
CHILDREN

Geni Balaban,I Maria Eugênia Farias Almeida Motta, II Giselia Alves Pontes
SilvaI,III

doi: 10.1590/S1807-59322010000200010

Balaban G, Motta MEFA, Silva GAP. Early weaning and other potential risk factors for overweight among preschool children.
Clinics. 2010;65(2):181-7.

OBJECTIVE: To investigate whether early weaning constitutes a risk factor for overweight at preschool age and to identify other
factors that affect this association.
METHODS: This was a case-control study of 366 children aged 2 to 6 years (176 boys and 190 girls) from three cities. The case
group comprised overweight children, as defined by body mass index (BMI) for age greater than or equal to the 85th percentile. The
main exposure analyzed was early weaning (exclusive or predominant breastfeeding for less than four months).
RESULTS: Early weaning was a significant risk factor for overweight in univariate analysis (OR = 1.69; 95% CI: 1.10-2.60; p =
0.02), but not in multivariate analysis (OR = 1.42; 95% CI: 0.86-2.34; p = 0.17). Maternal overweight, birth weight ≥ 3,500 g and
sedentarism were the main risk factors for overweight in multivariate analysis.
DISCUSSION: In our study, the protective effect of breastfeeding against overweight was only shown in univariate analysis; it did
not persist after controlling for other variables. It is possible that breastfeeding has only a small protective role against overweight
in comparison with other variables of greater importance.
CONCLUSION: Our results suggest that the potential protective effect of breastfeeding against overweight among preschool
children is weaker than genetic and other environmental factors.

KEYWORDS: Children; Overweight; Obesity; Breastfeeding; Risk factor.

INTRODUCTION Because obesity is a difficult-to-treat chronic disease that

is associated with a variety of adverse consequences relating
In recent years, a significant increase in the prevalence to morbidity and mortality, special emphasis should be given
of obesity has been observed in many countries and across to preventive measures. Simple, low-cost measures without
different age groups, including children.1,2 The increase in potential adverse effects are particularly attractive. Within
the prevalence of childhood obesity is worrying because of this context, several authors have raised the hypothesis
obese children’s higher risk of becoming obese adults and that breastfeeding might have a protective effect against
because of the various morbid conditions associated with obesity.4-14
obesity.3 Epidemiological studies and experimental studies on
animals have suggested that individuals’ first nutritional
I
Federal University of Ceará and School of Medicine of Juazeiro do Norte experiences may affect their susceptibility to chronic
- Ceará/PE, Brazil diseases in adulthood, such as obesity, hypertension,
II
Mother-Child Department of the Health Sciences Center, Federal University
of Pernambuco - Recife/PE, Brazil
cardiovascular disease and type 2 diabetes. This notion has
III
Federal University of São Paulo/UNIFESP - São Paulo/SP, Brazil been named “metabolic imprinting”.15 This term describes a
Email: [email protected]
Tel.: 55 81 2126.8514
phenomenon through which an early nutritional experience
Received for publication on October 13, 2009 during a critical and specific period of development might
Accepted for publication on November 26, 2009 cause an enduring effect that continues throughout an

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Early weaning and other potential risk factors for overweight among preschool children CLINICS 2010;65(2):181-7
Balaban G et al.

individual’s life, thereby predisposing him or her to certain A free and informed consent form was sent to all parents
diseases.15 or guardians responsible for the children within the desired
Breastfeeding represents newborns’ first nutritional age group. All children whose parents authorized their
experience and provides continuity with the nutrition participation were included in the study (1,610 children).
provided during intrauterine development. Many bioactive Their heights and weights were measured, and their BMIs
factors are present in human milk, including hormones and were calculated.
growth factors, which affect the growth, differentiation The case group was formed by the children who were
and functional maturation of specific organs, thus affecting overweight, which was defined as BMI greater than or
various aspects of development.16 Therefore, the unique equal to the 85th percentile for their age group. The curves
composition of maternal milk might be implicated in the and tables of BMI percentiles of the Centers for Disease
process of metabolic imprinting, for example, by changing Control and Prevention (CDC, United States), 2000 version
the number and/or size of adipocytes or by inducing the (revised version of the NCHS 1977 tables), for individuals
phenomenon of metabolic differentiation. aged two to twenty years according to sex and age were
The etiology of obesity has a multifactorial nature. A used as the reference standard (www.cdc.org/growthcharts;
tendency for obesity to run in families can be seen such accessed on Aug 12, 2002). The control group was formed
that children of obese parents have a higher risk of being by children whose BMIs were lower than the 85th percentile.
obese themselves. In addition to genetic factors, parents Children presenting diseases or using medications capable
and children usually share dietary habits and have similar of interfering with their weights and/or heights were not
physical activity levels, thus contributing towards the greater included in the study.
risk of obesity in certain families.17 Among the 1,610 preschool children assessed, 183 cases
High energy intake and low energy expenditure are were identified. To make up the control group, 183 children
among the main causal factors of obesity.18 In addition to were randomly drawn from among the pupils attending the
total caloric intake, the composition of one’s diet is also same schools as the cases.
important: diets rich in simple carbohydrates and lipids are The main exposure studied was early weaning. Children
a risk factor for obesity.18 Therefore, in analyzing a possible were considered to present this exposure if they had received
protective role for breastfeeding against overweight and exclusive breastfeeding or predominant breastfeeding (i.e.,
obesity, it becomes necessary to take into consideration other maternal milk accompanied by water and/or tea) for a
variables that could be involved in this association. period of less than four months. Other variables were also
The aim of the present study was to investigate whether evaluated, such as birth weight, maternal BMI, variables
early weaning constitutes a risk factor for overweight relating to the children’s current diet and variables relating
at preschool age and to determine whether children’s to the children’s level of physical activity. Socioeconomic
current diet, physical activity level and birth weight and variables were also gathered, with the aim of characterizing
their mothers’ body mass index (BMI) are associated with the sample.
overweight. The children’s current frequencies of intake of the
following were analyzed: fruits and greens/vegetables
METHODS (variables used as markers for a healthier diet). bread
(representing the intake of dough from grain), soft drinks
A case-control study was carried out among children and biscuits (representing the intake of carbohydrates and
of both sexes aged two to six years who attended private sweets/candies) and chips/French fries (representing the
schools in 2003 and 2004. The research project was assessed intake of fatty and fried foods).
and approved by the research ethics committee. The following variables related to the children’s physical
The sample size of 144 cases and 144 controls was activity levels were analyzed: average number of hours per
calculated with the aid of the Statcalc program in the Epi- day (on weekdays) of watching television, average number
Info software, version 6.0, using a confidence interval of of hours per day (on weekdays) of playing outside and
95%, a power of 80%, a ratio of 1:1 between the numbers of their most frequent means of locomotion (walking, car,
cases and controls, an expected frequency of the principal motorcycle or bus).
exposure in the control group (early weaning) of 40% and an The weights and heights of the children and their
odds ratio of 2.0, in accordance with data in the literature.10 mothers were measured by a team of trained research
Assuming the prevalence of overweight to be 11%,2 around assistants in accordance with standardized methods.19 Each
1,309 children would need to be evaluated in order to measurement was taken twice, and the mean was used.
identify 144 cases. The BMI was calculated using the formula of weight (in

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CLINICS 2010;65(2):181-7 Early weaning and other potential risk factors for overweight among preschool children
Balaban G et al.

kilograms) divided by the square of the height (in meters). risk of overweight than did those who had received exclusive
Data relating to breastfeeding and the other variables or predominant breastfeeding for four months or more (OR
were gathered by the same team by means of interviews = 1.69; 95% CI: 1.10-2.60; p = 0.02).
with the children’s mothers. This information was stored Maternal overweight (BMI ≥ 25 kg/m2), birth weight
in a database using double data entry and correction of greater than or equal to 3,500 g, fruit intake less than
inconsistencies. twice a day, greens and/or vegetable intake less than
The data were analyzed using Epi-Info version 6.0 and three times a week, consumption of one or more bread
SPSS version 8.0 software. First, each variable was evaluated rolls per day, consumption of soft drinks every day and
separately to determine whether it was a risk factor for consumption of biscuits every day constituted risk factors
overweight, with calculation of odds ratios and their 95% for overweight in the univariate analysis. Furthermore, in
confidence intervals. Following this, multivariate analysis was the univariate analysis, it was observed that the children
performed using the standard multiple regression method, in who played outside for an average of two or more hours
which all variables are simultaneously entered into the model. a day on weekdays and those whose most frequent means
A statistical confidence level of 95% was adopted. of locomotion was walking presented lower risks of
overweight.
RESULTS It was also observed that the children who consumed
chips/French fries every day and those who watched
Among the 366 children studied, 176 were male (48.2%) television for an average of five or more hours a day on
and 190 were female (51.9%). There was no statistically weekdays presented higher risks of overweight. However,
significant association between sex and overweight (OR these associations were not statistically significant.
= 1.36; 95% CI: 0.88-2.10; p = 0.17). The mothers’ mean In the multivariate analysis, only maternal overweight,
schooling level was 12.5 years, and the fathers’ was 11.6 birth weight greater than or equal to 3,500 g, playing outside
years. Most of the families had one or more cars (67.8%), for less than two hours a day and main means of locomotion
were homeowners (73.2%) and had health insurance other than walking remained as risk factors for overweight.
for their children (51.9%). There was no statistically The association between early weaning (receiving exclusive
significant association between overweight and any of these or predominant breastfeeding for less than four months)
socioeconomic variables (Table 1). and overweight did not reach statistical significance in the
multivariate analysis.
Table 1 – Socioeconomic variables and risk of overweight among pre- Table 2 presents the unadjusted and adjusted odds ratios
school children.
with their respective 95% confidence intervals.
Overweight Statistical
analysis DISCUSSION
Variables Yes No Total OR
n (%) n (%) n (%) (95% CI)
In the present study, the protective effect of breastfeeding
Homeowner against overweight was only shown in univariate analysis;
Yes 132 (49.3) 136 (50.7) 268 (73.2) OR = 0.89 it did not persist after controlling for other variables. It
No 51 (52.0) 47 (48.0) 98 (26.8%) (0.55-1.47) is possible that breastfeeding has only a small protective
Cars (one or more) role against overweight in comparison to other variables of
Yes 130 (52.4) 118 (47.6) 248 (67.8) OR = 1.35 greater importance.11,18
No 53 (44.9) 65 (55.1) 118 (32.2) (0.85-2.15) Different definitions of both the exposure and the
Health insurance (for the child)
outcome make it difficult to compare this study with similar
studies in the literature. The time that elapses between the
Yes 95 (50.0) 95 (50.0) 190 (51.9) OR = 1.00
exposure and the outcome also causes difficulty in analyzing
No 88 (50.0) 88 (50.0) 176 (48.1) (0.65-1.55)
this possible association. It may give rise to recall bias,
Note: OR = odds ratio; 95% CI = 95% confidence interval.
or, in the case of longitudinal studies, it may impose high
costs, long study durations and operational difficulties.
The percentage of the children who had received Furthermore, the extended time that elapses between the
exclusive or predominant breastfeeding for less than four exposure and the outcome may make it difficult to take all
months was 36.2% (132/366). In univariate analysis, the confounding variables into consideration.7-20;26-32
the children who had received exclusive or predominant Dewey, 26 in a review article, also reported that the
breastfeeding for less than four months presented a greater protective effect of breastfeeding seemed to be small

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Balaban G et al.

Table 2 – Logistic regression model of the risk factors for overweight among preschool children.

Variables Overweight Unadjusted OR Adjusted OR

Yes No (95% CI) (95% CI)
Breastfeeding
> 4 months 106 128 1.00 1.00
< 4 months 77 55 1.69 (1.10-2.60) 1.42 (0.86-2.34)
p=0.02 p=0.17
Maternal BMI
< 25 kg/m2 108 147 1.00 1.00
> 25 kg/m2 75 36 2.84 (1.72-4.68) 2.39 (1.42-4.02)
p<0.0001 p=0.001
Birth weight (g)
3000-3499 54 84 1.00 1.00
> 3500 81 57 2.21 (1.37-3.58) 2.00 (1.17-3.42);
p=0.001 p=0.01
2500-2999 39 35 1.73 (0.98-3.07) 1.68 (0.90-3.13);
p=0.06 p=0.10
1500-2499 9 7 2.00 (0.70-5.69) 1.78 (0.54-5.80);
p=0.19 p=0.34
Fruit intake
> twice/day 47 68 1.00 1.00
< twice/day 136 115 1.71 (1.09-2.68) 1.49 (0.89-2.49)
p=0.02 p=0.13
Greens/vegetable intake
> 3 times/week 81 109 1.00 1.00
< 3 times/week 102 74 1.86 (1.23-2.81) 1.57 (0.97-2.54)
p=0.004 p=0.06
Bread consumption
< 1 roll/day 63 85 1.00 1.00
≥ 1 roll/day 120 98 1.65 (1.06-2.59) 1.38 (0.85-2.26)
p=0.02 p=0.20
Soft drink consumption
< 7 times/week 139 157 1.00 1.00
Daily 44 26 1.91 (1.08-3.40) 1.69 (0.92-3.11)
p=0.02 p=0.09
Biscuit consumption
< 7 times/week 57 78 1.00 1.00
Daily 126 105 1.64 (1.04-2.59) 1.32 (0.81-2.17)
p=0.03 p=0.27
Consumption of chips/French fries
< 7 times/week 136 150 1.00 1.00
Daily 47 33 1.57 (0.92-2.69) 1.38 (0.79-2.41)
p=0.10 p=0.26
Number of hours of television (weekdays)
< 5 h/day 161 170 1.00 1.00
> 5 h/day 22 13 1.79 (0.82-3.92) 1.18 (0.51-2.70)
p=0.16 p=0.70
Number of hours playing outside (weekdays)
> 2 h/day 60 100 1.00 1.00
< 2 h/day 123 83 2.47 (1.62-3.78) 2.43 (1.52-3.88)
p<0.001 p<0.001
Most frequent means of locomotion
Walking 48 72 1.00 1.00
Others 135 111 1.82 (1.17-2.84) 1.82 (1.10-3.03)
p=0.008 p=0.02
Note: OR = odds ratio; 95% CI = 95% confidence interval.

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Balaban G et al.

compared with the effects of other factors, particularly It is possible that information given by individuals about
having overweight parents. Even so, the effect of their own energy intake is not a valid measurement. 23
breastfeeding could be important from a public health point Moreover, there is evidence that genetic factors are capable
of view considering the present epidemic of obesity seen in of modulating an organism’s response to variations in
many countries. environmental factors such as diet and physical activity.36
Wadsworth et al.13 did not find a significant association In the same way as for energy intake, measurement of
between breastfeeding and the prevalence of overweight at physical activity is also a complex task. Several methods
6 years of age in an analysis of 3,731 children in the United can be used, such as calorimetry, systematic observation,
Kingdom. In a cross-sectional study of 9,357 German movement sensors, heart rate monitors and questionnaires.37
children aged 5 and 6 years, von Kries et al. (15) found Questionnaires present several advantages, such as low
that the prevalence of obesity was 4.5% among children cost, practicality, lack of changes to individuals’ behavior
who had never been breastfed and 2.8% among those who and possibility of adaptation of the questionnaire to the
had breastfed. A dose-dependent effect of the duration of population in question. However, the literature is sparse
breastfeeding was observed. After adjusting for potential regarding questionnaires for evaluating physical activity
confounding factors, breastfeeding remained a protective among preschool children. Even the extensive collection of
factor against overweight and obesity. Obesity was defined questionnaires presented by Kriska et al.37 does not privilege
as BMI greater than the 97th percentile, whereas overweight this age group.
was defined as BMI greater than the 90th percentile. The mechanisms through which maternal milk may
In the recent review by Owen et al.,30 the authors play a protective role against obesity have not yet been
concluded that breastfeeding has a protective effect against determined. In a review article, Singhal & Lanigan38 grouped
obesity, but that the magnitude of this effect is still poorly potential protection mechanisms into two major groups:
defined. These authors found 61 articles analyzing the those that were associated with behavioral factors and those
possible relationship between breastfeeding and the risk of related to the composition of maternal milk.
obesity and concentrated their attention on the 28 studies It is possible that maternal milk is involved in the
that reported odds ratios that supported a protective effect phenomenon of metabolic imprinting. Waterland & Garza21
of breastfeeding. They observed that, in several studies, put forward some potential mechanisms through which the
controlling for confounding variables led to a reduction of phenomenon of metabolic imprinting could occur. Among
the protective effect of breastfeeding but did not eliminate these are induction of variations in the structures of some
it, and they emphasized the need to carry out other studies to organs, changes in the number of cells, and metabolic
determine the roles of the confounding factors. differentiation (changes in the expression of certain genes
In a wide-ranging meta-analysis, Harder et al.31 included causing variations in the production of enzymes, hormones,
17 studies that reported odds ratios and 95% confidence hormonal receptors, transmembrane transporters, etc).
intervals or sufficient data to calculate them; reported In terms of nutrients, the composition of maternal milk
the duration of breastfeeding; and included children fed differs qualitatively and quantitatively from infant formulas.
exclusively with infant formula for comparison. Based Moreover, several bioactive factors are present in human
on these data, these authors reported that the duration of milk, including hormones like insulin, adrenal steroids, T3
breastfeeding was inversely associated with the risk of and T4.22 Casabiell et al.39 identified the presence of leptin
overweight, independent of the definition of overweight used in human milk, which could play a regulatory role in the
and the age of the participants in the studies. One month of newborn’s metabolism, given that the hormone acts to inhibit
breastfeeding was associated with a 4% decrease in the risk appetite and anabolic pathways and to stimulate catabolic
of obesity. pathways.40
Evaluation of food intake is a complex task, which may Miralles et al.41 analyzed the concentrations of leptin
at least partially explain the divergences in the literature. in samples of blood and maternal milk from 28 non-obese
Several methods have been used for such evaluations, for women and assessed the growth of their children, who were
example, 24-hour recall, food diaries, direct weighing of breastfed for at least 6 months, over their first years of life.
foods, home consumption of foods, the food frequency These authors observed a negative correlation between the
questionnaire and dietary history. Each of these has its concentration of leptin in maternal milk after one month of
advantages and limitations.33 Evaluation of food intake lactation and the children’s BMIs at the ages of 18 and 24
among preschool children is an even more difficult task months.
because there is little data on this age group. Older age Lucas et al.42 reported differences in endocrine responses
groups have been investigated much more thoroughly.34, 35 with regard to the release of pancreatic and intestinal

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Balaban G et al.

hormones between newborns breastfed with maternal milk immunological and psychological advantages.
and those fed with infant formula. It is also possible that In summary, the results of our study suggest that the
the newborns who were breastfed developed more effective possible protective effect of breastfeeding against overweight
mechanisms for regulating their energy intake.43 among preschool children is of a lower magnitude than the
Evidently, even though no significant protective effect effects of genetic factors and other environmental factors.
of maternal milk against overweight and obesity has been Maternal overweight, birth weight and sedentarism are
proven, breastfeeding should continue to be strongly important risk factors for overweight in this age group.
recommended because of its unquestionable nutritional,

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