Of the various biological and environmental factors that affect weight gain and obesity during infancy and childhood,1 infant feeding is recognised as one of the most influential. Recent reviews2^–6 on the association between infant feeding and obesity suggest a small, but protective, effect of breastfeeding initiation and duration. The early introduction of solid foods appears to be less of a risk factor for obesity.7 8 Infants who gain weight rapidly during infancy are at increased risk of childhood obesity9^–11 and other adult outcomes;12 it is therefore important to examine factors associated with weight gain, and specifically the relationship between infant feeding practices and weight gain as this is one of the few potentially modifiable risk factors for childhood obesity. The limited evidence available suggests that breastfed infants are reported to gain weight more slowly than formula-fed infants,13 particularly beyond the first few months of life,14 15 whereas prolonged breastfeeding is also inversely associated with the risk of elevated weight gain.16 17 There is less and conflicting evidence for the effect of the early introduction of solid foods on early growth. This has been found to be associated with greater infant weight gain up to 1218 and 14 months.19 However, other studies have found that differences in growth are less apparent from birth to 6 months,13 or by 18 months20 or 24 months.21

We examined the association between breastfeeding initiation, breastfeeding duration and age of introduction of solid foods and weight gain from birth to 3 years of age. We addressed some of the limitations of previous research by exploring the influence of height and by adjusting for important confounding factors, including maternal sociodemographic characteristics and maternal body size. We also considered these associations in contemporary infants born in the UK, at a time when many mothers are not adhering to recommended infant feeding practices22 23 and children may therefore face an increasing risk of obesity.

PARTICIPANTS AND METHODS

Study population

The Millennium Cohort Study (MCS) is a longitudinal study, which was set up to examine the social, economic and health-related circumstances of the new century’s babies and their families.24 The first contact with the cohort was during infancy at 9 months; the cohort comprised 18 819 babies born between September 2000 and January 2002 who were living in the UK and were eligible to receive Child Benefit (a universal benefit of families with children; response rate 72%). The representativeness of the sample has been reported elsewhere.25 Surviving children were eligible to participate in the second survey, which took place between September 2003 and April 2005, when the children were approximately 3 years old.26 Overall, 14 630 (80%) of the 18 296 singleton infants in the first survey participated in the second.

Survey interviews were conducted, in the home, with the main carer (over 99% were natural mothers) and their partner at both contacts; information was obtained on a large number of factors, including infant feeding practices and the child’s birthweight. In addition, at the second contact, trained interviewers measured the children’s weight and height without shoes or outdoor clothing. The children were weighed using Tanita HD-305 scales (Tanita UK Ltd, Middlesex, UK), recorded to the nearest 0.1 kg, and height was measured using Leicester Height Measure Stadiometers (Seca Ltd, Birmingham, UK), recorded to the nearest 0.1 cm. Data from both surveys were obtained from the UK Data Archive, University of Essex.

Ethnic minority children (2362) were excluded due to established differences in infant feeding practices and weight gain patterns by ethnicity.23 27 Among the 12 268 singleton white infants, we excluded singletons from multiple conceptions (eg, single surviving twins; 78), dual families (two infants in the cohort; 10), those not born at term (37–41 weeks; 812), or those with missing or implausible data for birthweight (22) or weight at 3 years (927). Some participants had more than one exclusion criteria. As a result, the study included 10 533 children, as illustrated in fig 1. Children whose mothers had lower socioeconomic circumstances or educational qualifications were less likely to be included in the final study sample (p<0.05).

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Figure 1

Flow chart of attrition in the Millennium Cohort Study and the inclusion of cohort members in this study.

The MCS was given ethics approval from the South West and London Multi-Centre Research Ethics Committees for the first and second contacts, respectively.28

Outcome measures

Birthweight and weight at 3 years were converted to z-scores adjusted for age and sex using the British 1990 growth references.29 30 A z-score refers to the number of standard deviations the measurement lies above or below the 50th centile.31 Conditional weight gain z-scores were calculated as the standardised residuals from the linear regression of the 3-year weight z-score on birthweight z-score, with age and sex entered as covariates. The standardised residual is the 3-year weight z-score minus its value predicted from the regression, divided by the residual standard deviation from the regression. To clarify, this weight gain variable therefore took account of the potential confounding influence of birthweight, age and sex.

The conditional weight gain z-score has a mean of 0 and a standard deviation of 1 and is normally distributed. A positive value indicates a faster, and a negative value a slower, rate of weight gain compared with the population mean weight gain.

Explanatory measures

Three infant feeding practices (exposure variables) were examined: (1) Breastfeeding initiation: in which the mother put her baby to the breast at least once;23 (2) Duration of breastfeeding: in which the mother, having started breastfeeding, stopped before four calendar months (17.4 weeks), ie, stopped early; (3) Age at introduction of solid foods: in which the mother introduced solids before four calendar months (17.4 weeks), ie, introduced solid foods early.

The World Health Organization (WHO) and Department of Health (England) recommend exclusive breastfeeding for the first 6 months, before introducing complementary foods or drink.32 This study focused on 4 months, as this was the UK government recommendation when the MCS babies were born.33 MCS data were available on both partial versus full breastfeeding, but this study used partial breastfeeding because only 4% of infants were fully breastfed at 4 months.23

We also explored the influence of height as a causal factor on the association between infant feeding and weight gain. This was examined using 3-year height z-score, derived and adjusted for age and sex using the British 1990 growth references.29 30

Potential confounding factors

Maternal socioeconomic status, education, prepregnancy body mass index (BMI), parity and smoking during pregnancy were identified from the literature as potential confounding factors. Data were available in the MCS for all of these factors. Maternal socioeconomic status was classified according to the National Statistics Socioeconomic Classification,34 with women classified into: managerial and professional occupations; small employers and own account workers; intermediate occupations; lower supervisory and technical occupations; semiroutine and routine occupations; or, never worked or long-term unemployed. Maternal educational qualifications were classified as some (higher degree, degree, diploma, A/AS/S levels, General Certificate of Secondary Education (GCSE) grades A–C, other or overseas qualifications) versus none or minimal (GCSE grades D–E). GCSE are qualifications taken by secondary school students aged 14–16 years. Maternal heights and weights, self-reported at the first contact, were used to calculate BMI (weight (kg) ÷ height (m)²). Universal cut-off points were used to define women as “normal” weight (BMI <25) or overweight/obese (BMI ⩾25). Mothers were coded as primiparous if their infant was first born, or multiparous if not. Mothers were coded as smokers if they smoked any cigarettes during pregnancy, or non-smokers if not.

Statistics

All analyses were conducted using STATA/SE 9.2. Results were calculated using sample and non-response weights and survey commands35 to allow for the cluster sampling design effect of the MCS and attrition between contacts. Associations between conditional weight gain and each infant feeding practice were tested by linear regression, adjusted for the following confounding factors: maternal socioeconomic status, education, prepregnancy BMI, parity and smoking during pregnancy. All factors were significantly (p<0.05) related to the three exposure variables, and all except education were significantly related to the outcome variable. Education was therefore excluded from further analyses. In addition, age at introduction of solid foods was found to be a confounder in the association between weight gain and breastfeeding duration, and breastfeeding duration in the association between weight gain and age at introduction of solids. All associations were adjusted subsequently for height z-score.

RESULTS

Table 1 presents sample characteristics of the MCS mothers and children; 68% of mothers initiated breastfeeding; however, of these, 60% stopped breastfeeding before 4 months and 39% introduced solids before 4 months.

After adjustment for confounding factors, conditional weight gain was significantly associated with breastfeeding initiation (table 2); infants given no breast milk gained weight more quickly than those receiving any breast milk. Conditional weight gain was also significantly associated with breastfeeding duration (table 3): infants breastfed for less than 4 months gained weight more quickly than those breastfed for longer, and this association remained after adjustment for age at introduction of solid foods. Both of these associations remained even after adjustment for the child’s height z-score at 3 years. Conditional weight gain was associated with age at introduction of solid foods (table 4) with and without adjustment for maternal social class, prepregnancy BMI, parity, smoking during pregnancy and duration of breastfeeding; however, this association was no longer significant after adjustment for the child’s height z-score at 3 years.

DISCUSSION

Key findings and comparisons with existing research

This study has analysed data from a large, prospective, contemporary cohort to examine the effect of infant feeding practices on conditional weight gain from birth to 3 years of age. Non-breastfed children gained weight more quickly than breastfed children from birth to 3 years, supporting previous research showing the same pattern between birth and 12 months,13 14 36 and demonstrating that breastfeeding can influence growth in the longer term. We also found that the duration of breastfeeding was associated with more rapid weight gain; those breastfed for less than 4 months, and therefore given formula or other milk at an early age, gained more weight than those breastfed for 4 months or longer. The observation of prolonged breastfeeding and less rapid weight gain has previously been reported.16 Our findings for both breastfeeding initiation and duration remained after adjustment for height at 3 years, suggesting that children who are not breastfed, or breastfed for less than 4 months, are at risk of obesity as they were both heavier and fatter at 3 years. Whereas the early introduction of solid foods has been shown to increase weight gain in infancy,18 19 previous research has also shown that infants weaned early do not have accelerated growth weight gain during early childhood compared with those weaned later.13 20 21 In support of this, we found that the early introduction of solid foods was not associated with greater conditional weight gain to 3 years after adjustment for height. This suggests that children introduced to solids early were heavier but not fatter at 3 years of age. This is consistent with the findings of studies reporting no association between the early introduction of solid foods and obesity at age 5 years7 and 7 years,37 but not those of one study reporting a detrimental effect on obesity at 7 years.38

Strengths and limitations

The MCS represents a large cohort with detailed information on child health and development within the context of children’s social, demographic and economic conditions. It is one of the few UK studies to investigate the influence of infant feeding on weight gain during early childhood. Most studies in this area have instead examined weight status, eg, obesity, as the outcome. Furthermore, appropriate adjustment was made for measured confounding factors and the effect of introducing solid foods was considered in addition to that of breast milk.

However, several potential limitations are acknowledged. First, information on infant feeding was obtained retrospectively at the first contact (infant age 9 months) presenting the possibility of recall bias. However, our figures for breastfeeding are in accordance with those collected prospectively in the UK Infant Feeding Survey 200022 and others have shown maternal recall of breastfeeding practices to be reliable and valid.39 Previous surveys of early weaning practices across the UK have suggested relatively more women introducing solids earlier than reported here.22 40 41 Our findings may reflect differences in survey questions and maternal reporting practices in rounding to the nearest month.

Although birth weight was also based on maternal recall, the quality of reporting was high, with good agreement between MCS reported birthweights and birth registration data.42 Weight and height at 3 years was measured by trained interviewers using calibrated scales with implausible values removed, as described previously.43

Reverse causation should also be considered in the association between growth and infant feeding, as increased feeding can be a consequence of increased growth as well as its consequence. For example, mothers whose infants gain weight rapidly may feel that breastmilk does not meet their child’s energy requirements adequately and therefore either supplement their diets with solid foods, or discontinue breastfeeding and provide formula milk. Although we were unable to examine this hypothesis, studies with more frequent measures of weight gain and infant feeding during infancy40 describe this phenomenon, as does the work of Kramer et al44 on the Promotion of Breastfeeding Intervention Trial.

Although z-scores standardise measurements, weight gain z-scores do not directly translate to children’s weight gain and may be difficult to interpret. A comparison of the mean weight gain from birth to 3 years can provide some evidence for the size of effect. For example, among children initially breastfed, those who were breastfed for at least 4 months had a mean weight gain from birth to 3 years of 11.86 kg, whereas those breastfed for less than 4 months gained an average of 12.08 kg; a difference of 0.22 kg (95% CI 0.11 to 0.33). Furthermore, the average weight of children breastfed for at least 4 months was 15.55 kg compared with 15.38 kg for those not; a difference of 0.16 kg (95% CI 0.05 to 0.27). Although these differences in weight gain and weight per se at 3 years are small at an individual level, they are of public health importance at a population level as breastfeeding is a modifiable risk factor for the very large proportion of UK mothers who never initiate or do not continue breastfeeding for the recommended period.

Mechanisms

Weight gain in infancy is likely to be directly and causally linked with feeding practices during the first year of life. Whereas the mechanisms by which infant feeding influences weight gain or obesity in later life are unclear, a number of possible behavioural and biological explanations have been proposed. There has been increasing interest in the contribution of early infant feeding practices to early programming of appetite regulation and satiety.45 It is suggested that breastfeeding enables infants to develop a healthier pattern of self-regulation, as they can respond to hunger and satiety cues by exerting more control over the amount of milk they take from the breast and therefore their energy intake.46 Infants in whom appetite regulation is impaired may be more vulnerable to the effects of an energy-dense dietary environment. Therefore, infants who are never breastfed, or in whom breast milk is rapidly replaced by formula milk or solids, may have higher total energy and protein intake,36 which stimulates greater fat deposition via greater insulin response.47 These mechanisms, alone or in combination, may explain why we found a significant, although small, association between breastfeeding and weight gain to 3 years of age.

Having adjusted for height in the analyses, we have shown that this is not a causal factor in the relationship between breastfeeding initiation or duration and obesity at 3 years. However, adjustment for height attenuated the significant association between rapid weight gain and the early introduction of solids, suggesting that height mediates this association. This is consistent with the findings of Buchan et al48 who first recognised the importance of tall stature as a risk factor for childhood obesity, and suggested that this may be driven by larger appetites in taller children who have been growing faster.

CONCLUSION AND RECOMMENDATIONS

Rapid weight gain in developed countries is of concern as it is associated with an increased risk of obesity.9 The findings of our study suggest that breastfeeding, in particular, has a small but important influence on conditional weight gain from birth to 3 years of age. Infants of mothers who adopted infant feeding practices not in accordance with the then current Department of Health guidelines33 gained weight more rapidly. It will be important to follow this cohort long-term to ascertain the effect of infant feeding practices, especially early weaning, on longer-term obesity risk. The identification of other modifiable risk factors for rapid weight gain during infancy and early childhood is required to address childhood obesity.49

The public health problem of childhood obesity calls for international collaboration in curbing the rising trend, such as the WHO’s European Charter on Counteracting Obesity50 and the US Healthy People 2010 goals.51 The UK government has responded by developing a public service agreement target to reduce the proportion of overweight and obese children to 2000 levels by 2020.52 In the UK,22 like many other countries,53 most mothers are not adhering to the WHO infant feeding recommendations.32 Our findings suggest that this could be facilitated through local/national policies and initiatives to promote the recommended infant feeding guidelines. Growth monitoring, using published WHO reference charts,54 based on babies who were breastfed, will also help to evaluate the success of these policies.55