The influence of breastfeeding duration and introduction of animal source foods , fruit juice and vegetables on the risk of weight gain in Thai children

Objective: To examine the influence of infant feeding practices on weight gain in children at 24 months of age. Method: Study data were from 4,245 children from the prospective cohort study of Thai children conducted in 2000-2002. Information on breast feeding duration and timing of specific types of complementary foods introduction was collected in infancy. Overweight (BMI-for-age >2 SD from WHO standard median) and weight gain (weight at birth minus body weight at 24 months) were evaluated. Results: Breastfeeding for 12 months or more reduced the weight gain (ß=-0.0101, p<0.0001) and the risk of overweight (aOR=0.24, 95% CI=0.150.40) after adjustment for confounders. In light of specific types of foods, overweight risk decreased with increasing age at introduction of animal source foods (aOR=0.78, 95% CI=0.67-0.91), vegetables (aOR=0.85, 95% CI=0.76-0.96), and fruit juices (aOR=0.92, 95% CI=0.83-1.01), whereas weight gain had an inverse association with animal source foods (p=0.0004) and vegetables (p<0.0001). _________________________________________ ASEAN Institute for Health Development, Mahidol University, Thailand, Institute for Health and Society, Hanyang University, Seoul, Republic of Korea, College of Medicine and Public Health, Ubon Ratchathani University, Thailand *Correspondence: aroonsri.mon@mahidol.edu (Received on 29 May 2016: Accepted after revision on 15 July 2016) The authors declare that there are no conflicts of interest The study was supported by Thailand Research Fund, Health System Research Institute, Ministry of Public Health, DUMEX Science, ASEAN Institute for Health Development, Mahidol University, and World Health Organization. Open Access Article published under the Creative Commons Attribution CC-BY License. Conclusion: This study concluded that longer duration of breastfeeding and late introduction of animal source foods, fruit juices and vegetables decreased weight gain or overweight risk in children at 24 months of age. DOI: http://dx.doi.org/10.4038/sljch.v46i2.8264 (


Introduction
Obesity starts early and tends to persist into childhood and adulthood 1 .Research has therefore focused on identifying the factors attributable to the development of obesity with emphasis on the first year of life as a critical period to target 2 .Appropriate feeding practices during infancy are essential for the development of children 3 .There are many studies on the effects of proper infant feeding on the child development.Nevertheless, effects of breastfeeding (BF) and timing of complementary food (CF) introduction on the development of obesity are not conclusive even today.Furthermore, the effect in low-and middle-income countries is questionable, because most studies were evaluated in high income countries [4][5][6] .In addition, infant feeding practice, such as types of CF when stopping BF between high-and low-income countries is different.Therefore, studies on the effect of infant feeding practice, such as BF and timing of CF introduction in low-and middle-income countries were suggested 7 .But only one Danish study has evaluated the effect of timing of complementary food introduction, particularly in terms of specific types of foods.
Thailand has recently experienced significant economic growth, and as a result, prevalence of obesity and obesity-related diseases has been increasing at an alarming rate 8 .The prevalence of obesity defined with BMI 25 or more in Thai adults almost doubled from 18.2% in 1991 1,9 to 34% in 2008-9 8 .Among under five children, the overweight also sharply increased from 6.9 % in 2006 10 to 11% in 2012 2,11 .The dramatic increase led to increment in health care usage resulting from obesity-related diseases, which has had a significant economic impact on the health care system in Thailand.The total cost of obesity was estimated at 12,142 million Baht, accounting for 0.13% of Thailand's Gross Domestic Product (GDP) 8 .These make it clear that Thailand is facing an obesity epidemic that can no longer be ignored.This entails a need to identify early determinants of overweight for prompt intervention to prevent obesity in early year settings.Therefore, we aimed to evaluate the association of duration of any BF and timing of CF introduced with weight gain and the risk of overweight in 2 year-old children.We used data from the Prospective Cohort study of Thai Children (PCTC) in Thailand.Findings from this study have significant implications for other developing countries in transition 12 .

Objective
To examine the influence of infant feeding practices on weight gain in children at 24 months of age.

Study dataset and subjects
A total of 4,245 24-month-old children from the prospective cohort study of Thai children (PCTC), based on 5 regions reflecting socioeconomic and cultural characteristics (Panomtuan District in Kanchanaburi, Thepa District in Songkla, Kranuan District in Konkaen, Muang District in Nan, and Bangkok) were recruited from October 2000 to September 2002.Study methods have been described in detail elsewhere 3,13 .Infants born as twins (N=60) or who died before 24 months due to significant health problems, such as birth defects, deficits of physical development (N=34) or born from teenage mothers (N=487), who tended to deliver abnormally and have babies with low birth weight and lower education level than adult mothers 3,14 , were excluded.In addition, infants with no information on infant feeding practice and child growth, such as weight and height were excluded (N=63).Therefore, 3,601 mother and infant pairs were included in the analysis.Present study was approved by the National Ethical Committee, Ministry of Public Health in Thailand.All families were informed about study procedures and possible risks before signing the consent form.

Exposure: Infant feeding practice variables
Data of timing of complementary feeding introduction and types and duration of BF were collected by interviewer-administered questionnaires at 6, 12, 18 and 24 months.A similar set of questions was asked at each study period: 1) "Was the baby (still) breast-fed?"; "if no longer breast-fed, what was the age (months) at which BF stopped?" 2) "Was the baby (still) formula-fed?";"if yes, when was the age (months) at which formulafeeding started (before 6 months or after 6 months)?".Data on timing of CF introduction was recorded by using a food calendar.A colourful picture of food calendar was provided to mothers after giving birth to child and mothers were asked to stick the food stickers of individual food items corresponding to the month, when the food items were introduced to the child.The following set of questions was asked at 6 and 12 months: 1) "If after 6 or 12 months, specify the starting age (months)" and 2) some questions related to types of CF were asked aside from milk; "What age and what kind of food with preparing method was your child fed?".Breastfeeding duration (≤ 3, 4-5 and ≥6 months), type of milk fed during the first 6 months (yes, no), continuous breastfeeding at 12 and 24 months of age (yes, no), and age of complementary food introduction (< 4 and ≥4 months OR ≤ 2, 3 and ≥ 4 months as appropriate) were created and used in the analysis.

Outcome: Weight gain and overweight variables
Height and weight of children were measured by physician and specially trained research assistants.The measurements were taken according to recumbent length using a graduate board with a fixed headboard and movable footboard (1 m/0.1 cm), and recorded to the nearest 0.1 cm.Age-and sex-specific body mass index (BMI) was calculated using the WHO child growth standard 14 .Children with a BMI-for-age >2 SDs from the WHO growth standard median were classified as overweight.In this study, weight gain (kg) was defined as weight at birth minus body weight at the 24-month examination.

Statistical analysis
We examined approximate linear associations of covariates according to three doses of either starting age of CF or BF duration and the trend tests for linearity were conducted by treating the median value for each either BF or age of CF group as a continuous variable in the analyses.The associations of two exposure variables on the weight gain (kg) and overweight risk after adjustment for selected confounders were investigated by multiple linear regression and logistic regression analysis, respectively.Statistical analyses were conducted with SAS for Windows (version 9.2). 1.Approximately 20% of mothers had college education or more and high BMI (≥23 kg/m 2 ), and lived in urban areas.Mean birth weight was 3.1 kg and 10.5% of infants weighed 2.5 kg or less at birth.Approximately 35% infants were breastfed for less than 6 months.Mean age of introduction of any CF was 2.7 months.Tables 2 and 3 show some potential confounding factors by using duration of BF and age of CF introduction.With increase of duration of BF (Table 2), maternal pre-pregnancy BMI, number of parity, and the proportion of normal delivery increased, but education level, weight gain during pregnancy, and living in urban decreased.In terms of type of food introduced, the age of animal source foods, fruit juice, and vegetable showed positively linear trend with increased BF duration, but sweetened foods, and fruits showed the reverse association.Characteristics of subjects according to age of CF introduction are shown in Table 3. Delayed introduction of complementary feeding had a significant positive association with higher maternal age at delivery, educational level, weight gain during pregnancy, non-smoking status, assisted or caesarean delivery and lower gestational age at birth of baby.

All values were adjusted for maternal age (years)
Table 4 shows the association between infant feeding practice and the risk of high weight gain and overweight after adjustment for the potential confounders.Longer BF for 12 months or more was inversely related to high weight gain (ß=-0.0101,p<0.0001) and a risk of overweight [adjusted Odds Ratio (aOR) = 0.24, 95% confidence interval (CI) = 0.15-0.40)after adjustment for confounders.
Starting age of any CF was not associated with either high weight gain or overweight risk.In light of specific types of foods, overweight risk decreased with increasing age (months) at introduction of animal source foods (aOR=0.78,95% CI=0.67-0.91),vegetables (aOR=0.85,95% CI=0.76-0.96),and fruit juices (aOR=0.92,95% CI=0.83-1.01),while higher weight gain had an inverse association with animal source foods (p=0.0004) and vegetables (p<0.0001).The effect of animal source foods and vegetable did not change much even after additional adjustment of breastfeeding duration (data not shown).In a comparison of the effect of late (≥4 months) compared with early (<4 months) introduction of CF, the protective effects of their late introduction were observed.This study showed that longer duration of BF is inversely related with weight gain and an overweight risk in early childhood, which is consistent with other studies 6,[18][19][20][21][22] .However, the beneficial effect in adulthood is not consistent between studies.A recent meta-analysis review using five cohorts in low-and middle-income countries 23 reported that prolonged BF was associated with lower risk of hypertension, diabetes or overweight even in adults, while two cohort studies in USA 5 and Denmark 24 reported no relationships in adulthood 5,24 .Meanwhile, although the protective effect was reported in India 22 and China 20 , studies in early childhood were mostly conducted in high countries 6,18,19,21 .In highincome settings, highly educated mothers tend more to breastfeed exclusively than those less educated and their infants are less likely to become overweight or obesity.The patterned confounding of socioeconomic position (SEP) in breastfeeding in high-income countries may affect the causal inference 5,25 .The impact of residual confounding was examined by comparing cohorts from high income and low-or middle-income countries.Effect of longer duration of BF on BMI (kg/m 2 ) was protective in ALSPAC study in UK, but not in Pelotas study in Brazil.Indeed, many studies showing their protective effect came from high income countries 6,18,19,21 .In our study, Thai infant breastfed longer were mostly from low socioeconomic status and live in rural area, while those likely to be overweight were mostly from higher SEP.Although we cannot control the residual confounding by SEP completely, careful selection of potential confounders related to pattern of breastfeeding or timing of CF introduction may minimize the effect.
Although stronger effect of late introduction of CF rather than BF either in early childhood 4,6 or in adulthood 23,24 was reported in some studies, we found no protective effect of early introduction of any CF, supported by the previous studies 26,27  A possible explanation of the beneficial effect of longer BF and late introduction of CF is biological programming.For example, formula-fed infants have fat deposition and increased number of adipocytes through a greater insulin response compared to those breast-fed 1,29 .In addition, displacement of breast milk containing low protein by earlier introduction of CF including higher energy and protein 30 may lead to high energy 31 and protein intake 32 in early life.It was supported by some previous studies 4,31,32 .In the ALSPAC birth cohort study in UK, higher intake at 4 months was related to higher weight gain and BMI at 1, 2, 3, or 5 years of age but only found in formula-or mixedfed children at 4 months 32 .The result was also found in the Project Viva, a USA cohort study, showing a positive association between introduction of CF before 4 months and odds of obesity only in formula-fed infants 4 .In addition, higher protein intakes were associated with faster weight gain in an EU Childhood Obesity Trial study 32 .
Several limitations of the present study should be acknowledged.Residual confounding may distort the true relationship.To minimize the effect, we have included many confounding variables and adjusted for the potential confounders with consideration of the relation of breastfeeding or timing of complementary feeding.Secondly, we collected information on infant feeding from mothers' recall and it may result in recall bias.The prospective nature of the information presented decreased the likelihood of recall bias.Finally, misclassification of breastfeeding or timing of CF introduced can be an issue that should be taken into consideration.It is likely to be non-differential so that this may lead to the results towards the null.

Conclusion
Longer duration of breastfeeding for at least 12 months and late introduction of animal source foods, fruit juices and vegetables after 4 months reduce the risk of overweight and weight gain in children at 24 months of age in this Thai study population.