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Articles

Full Breast-Feeding for at Least Four Months Has Differential Effects on Growth before and after Six Months of Age among Children in a Mexican Community^{1 ,2}

Cara L. Eckhardt³, Juan Rivera^*, Linda S. Adair and Reynaldo Martorell

Department of Nutrition, University of North Carolina at Chapel Hill, NC; ^* National Institute of Public Health, Cuernavaca, Mexico; and Department of International Health, Rollins School of Public Health, Emory University, Atlanta, GA

³To whom correspondence should be addressed. E-mail: roberts9{at}email.unc.edu.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
This study examines the relationship between breast-feeding and growth from 0 to 6 and 6 to 20 mo among 185 children in a Mexican community. Infants from a previous 6-mo longitudinal study were followed up for additional anthropometric measurements at a mean age of 19.9 mo. Size at 6 mo and at follow-up were modeled as outcomes of whether infants were fully breast-fed (exclusively or predominantly breast-fed) for at least 4 mo, controlling for size at birth and 6 mo, respectively, and potential confounders. From birth to 6 mo, fully breast-fed infants had ponderal index increments of 0.07 units larger (P = 0.04) than comparison infants. There were no differences in weight. For length, an interaction between full breast-feeding and socioeconomic status (SES) was found, with fully breast-fed infants of low SES growing more than comparison infants, whereas the opposite was seen at upper SES levels. From 6 to 20 mo, fully breast-fed infants had weight and length increments of 0.53 cm (P < 0.001) and 0.72 kg (P = 0.01) smaller than those of comparison infants. For ponderal index, an interaction between mother’s education and breast-feeding revealed an inverted U-shaped response across levels of education. Additionally, logistic regressions of monthly breast-feeding on lagged measurements revealed that relatively heavier infants had higher odds of being fully breast-fed at 2 and 3 mo. Our findings indicate that the benefits of full breast-feeding on growth may be most pronounced early in life. Further research of unmeasured confounders may explain the association of full breast-feeding with slower growth beyond 6 mo.

KEY WORDS: • breast-feeding • growth • Mexico • infant feeding

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Research shows that the growth of children who were breast-fed differs considerably from that of children who were not breast-fed during infancy (1 ,2) . Breast-fed children usually grow more quickly than nonbreast-fed children during the first 3 mo of life, and then go through a period of slower growth (3) . This general pattern has been observed in populations from both developed (3 ,4) and developing countries (2 ,5 ,6) . However, evidence from developed countries suggests that there are no poor functional outcomes associated with the slower growth of breast-fed infants (3) . Rather, this slower growth likely results from self-regulated lower energy intake (1 ,7) among breast-fed infants, rather than lack of breast milk availability.

The many benefits of breast-feeding, including protection against exposure to harmful pathogens, provision of superior nutrition, transfer of antibodies and reduction in morbidity and mortality, are indisputable. Thus, it is acknowledged that optimal growth, the normal trajectory of healthy breast-fed children, is not necessarily synonymous with maximal growth (1) , and breast-feeding continues to be internationally recommended (8) . However, debate about the optimal duration of breast-feeding and a need for more research about the effects of different patterns of breast-feeding on growth and other outcomes (8) remain.

The WHO released revised international breast-feeding recommendations in April 2001 (8) . The previous recommendations indicated exclusive breast-feeding for 4-6 mo followed by the introduction of appropriate complementary foods (9) , whereas the revised recommendations extend the exclusive breast-feeding period to a firm 6 mo (8) . These recommendations were made after reviewing literature comparing the growth of children who were mainly predominantly breast-fed (rather than exclusively breast-fed, due to the low frequency of exclusive breast-feeding) with that of other children. In making their recommendation, the WHO recognized the limitations of the available literature and called for further research to generate more generalizable and precise estimates of the effects of different durations of breast-feeding (8) .

Among the specific recommendations for research made by the WHO is a comparison of growth outcomes after 6 mo between infants who were exclusively/predominantly breast-fed and those who were partially breast-fed for the first 4–6 mo of life (8) . We used longitudinal data from rural Mexico to assess the differences in growth from birth to 6 mo and from 6 mo to 20 mo between children who were and were not exclusively/predominantly breast-fed for at least 4 mo. In addition, to aid in the interpretation of our findings, we assessed the degree to which feeding behaviors were altered by mothers in response to infant size.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Study design.

The data presented come from a cohort study of infant feeding in the first 6 mo of life, and from a follow-up study of the original cohort. The original cohort study was conducted in 1996 and 1997 by the Instituto Nacional de Salud Pública (INSP)⁴ of Mexico in the semirural agricultural community of Xoxocotla (population 16,800), Morelos State, Mexico and was approved by the ethics committee at INSP. All expectant mothers in the community were invited to participate in the original observational study, and all term babies (>37 wk gestation) from consenting mothers were enrolled (n = 220). Participating infants were followed from birth to 6 mo. Weight and length measurements were collected at birth and monthly thereafter. Monthly feeding practices were determined through maternal report of breast-feeding and age at introduction of various liquids and other complementary foods. Other health and demographic data were collected as well.

The follow-up study, originating from the INSP and approved by their ethics committee, took place from June through August 1998, when the mean age of the children was 19.9 mo. Informed consent was obtained from mothers at the beginning of the follow-up visit, during which weight and length measurements were collected along with demographic data. At follow-up, the children’s feeding histories were not known to the data collectors. Of the 220 children who completed the original study, 209 (95%) were included in the follow-up. Of the 11 children not included, three did not participate because their mothers declined, three had died and five had moved away. Of the 209 children included in the follow-up study, a further 24 were excluded from analysis. Two were excluded because they were twins, one was excluded due to congenital anomalies, and 21 were excluded due to missing data for one or more key variables. Thus, 185 (84% of the original cohort) children were included in the final analyses.

Anthropometry.

Children were weighed on a Tanita electronic pediatric scale (Model 1583; Tanita, Arlington Heights, IL), and weight was recorded to the nearest 10 g. Most children were weighed without clothing. For those children weighed clothed, similar clothing provided by the mother was weighed separately and its weight was subtracted from the weight of the clothed child to obtain the child’s weight. Length was measured to the nearest 1 mm using the same locally made wooden anthropometer with fixed headboard that was used in the original study. Weight was measured by the first author. Length was measured by both the first author and a field worker, and the mean of the two measurements was used for analysis. Both the author and the field worker were trained at the INSP in standard anthropometric methods (10) . Ponderal index (weight/length³), the WHO recommended measure of relative heaviness for infants (11) , was calculated for each child. Weight-for-length, length-for-age and weight-for-age Z-scores at 6 mo of age were calculated using Epi Info (Release 6.0, CDC, Atlanta, GA).

Feeding practices.

The WHO defines exclusive breast-feeding as the provision of breast milk with no other liquids or solids other than vitamin/mineral supplements or medicines, and defines predominant breast-feeding as the provision of breast milk accompanied by water, tea, juice, other water-based drinks, vitamin/mineral supplements or medicines (12) . For each of the first 6 mo of life, infants were either classified as fully breast-fed (exclusively or predominantly breast-fed according to the WHO definitions) or not fully breast-fed. These monthly breast-feeding variables were used in monthly logistic regressions to explore whether infant size influenced mothers’ feeding choices. Based on the monthly breast-feeding variables, infants were further categorized as fully breast-fed for at least the first 4 mo of life (n = 114) or as not fully breast-fed for at least the first 4 mo of life (n = 71) for comparison in terms of growth outcomes. Due to the worldwide low frequency of exclusive breast-feeding beyond the first few months of life, the practice of combining exclusively and predominantly breast-fed infants for analysis purposes was indicated in the research recommendations recently made by the WHO (8) and has been used by others, including Victora and colleagues (6) and the WHO itself (13) in the research for its forthcoming growth references for children <5 y of age. Indeed, in our study population, only 9 infants (5%) were exclusively breast-fed for at least the first 4 mo of life. Among those children classified as not fully breast-fed for at least 4 mo, 11 (15%) children were never breast-fed, 4 (6%) children received some breast milk but were never fully breast-fed, 8 (11%) children were fully breast-fed for only 1 mo, 14 (20%) children were fully breast-fed for 2 mo and 34 (48%) children were fully breast-fed for 3 mo. Although there is heterogeneity in the reference group, the inclusion of children who were fully breast-fed, but for <4 mo, biases our results toward the null, and thus provides conservative estimates. Similar methods were used recently by Haschke et al. (14) in a study comparing children who were fed according to the WHO breast-feeding recommendations with all those who were not, and by Hop et al. (15) who combined partially breast-fed and fully weaned children together for comparison with other breast-fed groups.

Although it is often assumed that children naturally progress from exclusive breast-feeding to predominant breast-feeding to partial breast-feeding in a unidirectional manner, Zohoori and colleagues (16) have shown that infants may move back and forth between the different levels of breast-feeding during infancy. Eight (4%) of the children in our analysis sample shifted back and forth between full and nonfull breast-feeding during the first 4 mo of life. We used a consistent approach in dealing with these cases. For those cases in which one instance of nonfull breast-feeding was recorded between months of consistent full-breast-feeding, it was assumed that only a brief and unsustained attempt at introducing solid or semisolid foods into the diet took place, and was disregarded. In these cases, full breast-feeding was not considered to have ended. However if more than one data point representing nonfull breast-feeding appeared consecutively, even if followed by other months in which full breast-feeding was reported, it was assumed that a more sustained introduction of foods occurred, and full-breast-feeding was considered to have ended before the reported consecutive instances of nonfull breast-feeding.

Covariates.

Socioeconomic status (SES) categories of low, medium and high were defined by principal components analysis using the varimax rotation. The analysis assessed variables regarding home construction materials (i.e., type of floor, roof and walls), availability of piped water and drainage system, presence of latrine or toilet, number of household appliances and number of persons per room. The three levels of SES were modeled using two dummy variables for low and high SES, with medium SES serving as the reference group.

Mother’s education was categorized as low (did not complete primary school), medium (completed primary school but did not continue) or high (completed any amount of schooling beyond primary school). Like SES, mother’s education (low and high) was modeled as dummy variables, with medium education as the reference group.

Statistical analyses.

Multiple linear regression models were used to explore growth from birth to 6 mo and from 6 mo to follow-up, as a function of whether infants were fully breast-fed for at least 4 mo. Size at 6 mo and size at follow-up were modeled separately in terms of weight (kg), length (cm) and ponderal index. The models of size at 6 mo controlled for size at birth, allowing us to interpret our coefficients for the breast-feeding variable as differences in growth increments from birth to 6 mo between children who were and were not fully breast-fed for at least 4 mo. The models were also adjusted for the exact ages at which the birth and 6-mo measurements were taken, to account for small variations in timing. All models were additionally adjusted for sex, mother’s education and SES. Similarly, in the regressions of size at follow-up, size at 6 mo was included in the models, allowing us to explore differences in growth increments from 6 mo to follow-up. Exact ages at the 6-mo and follow-up measurements, sex, mother’s education and SES variables were also included in the models. Coefficients for main effects with P-values of <0.05 were considered statistically significant. Interactions between SES and the breast-feeding variable, and between mother’s education and the breast-feeding variable were tested in the models. Interaction terms that were significant at P < 0.10 are presented.

The possibility of mothers altering their feeding choices in response to infant size was assessed for each of the first 6 mo of life using a set of logistic regressions, with monthly full breast-feeding as the dependent variable, and ponderal index (modeled in terms of tenths of a unit), length (cm) or weight (kg) from the prior month as the independent variable. A significant effect [confidence interval (CI) not containing one] of prior infant size (hereafter referred to as lagged size) on the odds of subsequent full breast-feeding was interpreted as evidence of infant size having had an influence on the level of breast-feeding provided. Ponderal index was modeled in tenths of units for the logistic regressions, because one tenth of a unit represents a more biologically plausible difference in relative heaviness between children of the same age than one whole unit. For example, a 6-mo old child of average length (65 cm) and weight (7 kg) in our study, would have a ponderal index of 2.5. An increase of 2.6 kg (to 9.6 kg) would be needed to raise the ponderal index from 2.5 to 3.5 for a child of that same length. All statistical analyses were completed using Stata for Windows (Release 6.0, Stata Corporation, College Station, TX).

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Descriptive statistics.

There were no significant differences in sex, SES, mother’s education level, age at follow-up, birth weight, birth length or ponderal index at birth between the infants who were fully breast-fed for at least 4 mo and those who were not (Table 1 ). There were some differences in size at 6 mo and follow-up. At 6 mo of age, infants who were fully breast-fed for at least 4 mo had a mean ponderal index of 0.03 units more than infants who were not (P = 0.04). There were no differences in weight or length at 6 mo. By follow-up (mean age 19.9 mo), there were no differences in ponderal index, but children who were fully breast-fed for at least 4 mo were 0.52 kg lighter (P < 0.001) and 1.21 cm shorter (P = 0.01) than other children.

Growth from birth to 6 mo of age.

Feeding group had no significant effect on weight increments from birth to 6 mo (Table 2 ). In contrast, infants who were fully breast-fed for at least 4 mo had ponderal index increments that were 0.07 units larger (P = 0.04) than children who were not.

Growth from 6 mo to follow-up.

Between 6 mo and follow-up, infants who were fully breast-fed for at least 4 mo had significantly lower weight and length increments than those who were not (Table 3 ). Infants fully breast-fed for at least 4 mo had a mean weight increment of 0.53 kg smaller (P < 0.001), and a mean length increment of 0.72 cm smaller (P = 0.01).

Changes in infant feeding in response to infant size.

As described earlier, whether infant size influenced mothers’ feeding choices was assessed by three sets of logistic regressions of the monthly full breast-feeding variable on either lagged ponderal index, weight or length measures for each of the first 6 mo of life (i.e., full breast-feeding at each month as a function of size in the prior month; Table 4 ). A one tenth of a unit increase in lagged ponderal index was associated with higher odds of being fully breast-fed at two [odds ratio (OR) = 1.30, 95% CI: 1.07–1.59) and 3 mo (OR = 1.34, 95% CI: 1.11–1.62) of age. This tendency was also suggested at 4 and 5 mo of age. At 2 mo of age, a 1-kg increase in lagged weight was associated with higher odds of being fully breast-fed (OR = 2.45 CI: 1.01–5.93). No other weight measurements and no length measurements were significantly associated with the monthly breast-feeding variable.

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Although we feel that our study is important in that it joins only a handful of other studies (3 ,15) in attempting to investigate the effects of infant feeding beyond 1 y of life, our main limitation is lack of data between the end of the original study at 6 mo and the follow-up study at 20 mo. This period in an infant’s life is a time of high growth velocity, high morbidity in developing countries and distinct diet changes. Without data to investigate what happened during this gap, it is impossible to attribute differences in growth solely to the effects of prior infant feeding practices.

Our study is also limited in a way in which most studies of breast-feeding are limited. Although the WHO recommends exclusive breast-feeding for the first 6 mo of life, exclusive breast-feeding is a rare practice in reality. In our study, the frequency of exclusive breast-feeding at 4 mo was only 5% and dwindled to 0 by 6 mo. Indeed, although the recent press release from the WHO providing the revised feeding recommendations cites evidence that exclusive breast-feeding for 6 mo is superior, a footnote indicates that the studies of "exclusive" breast-feeding reviewed by the WHO actually combined predominantly and exclusively breast-fed children in their analyses (8) . Also, the forthcoming WHO growth references for children <5 y of age will be based on a combination of exclusive and predominantly breast-fed children due to the low frequency of exclusive breast-feeding (13) . Thus the limitations of real breast-feeding practices prohibit the literal testing of the WHO feeding recommendations both in our study and elsewhere. We point out this limitation, not to question the merits of exclusive breast-feeding, but rather to call attention to the difficulties in precisely measuring those benefits where true exclusive breast-feeding is unfortunately rare, and full breast-feeding more common.

We chose to compare infants who were fully breast-fed for at least 4 mo with those who were not. The comparison group is therefore heterogeneous in that it includes those who were fully breast-fed for 3 mo with those who were not breast-fed at all. The heterogeneity in the reference group is likely to decrease the likelihood of finding an effect of full breast-feeding for 4 mo. Therefore, our analysis strategy is conservative for estimating the relationship between full breast-feeding for at least 4 mo and growth.

From birth to 6 mo of life, infants who were fully breast-fed for at least 4 mo had larger growth increments in terms of weight relative to length, as measured by ponderal index. This result fits with other evidence of faster growth among breast-fed children during the early months of life in developed (3 ,4) and developing countries (2 ,5 ,6) . It also suggests that, although others have shown differences in growth between breast-fed and nonbreast-fed children, there may also be differences in growth among children who were breast-fed for different durations and intensities.

The interaction between SES and breast-feeding with regard to length during the first 6 mo of life also makes intuitive sense. When compared with other infants, the birth to 6-mo length increments of infants fully breast-fed for at least 4 mo were larger in the low SES group, yet were slightly smaller in the medium and high SES groups. The families of low SES infants likely could not afford appropriate complementary foods and probably used contaminated water for food preparation, whereas medium and high SES families may have had access to cleaner water and more energy-dense complementary foods. Thus, low SES children would have had much to gain from full breast-feeding through the reduction of pathogen exposure and the provision of appropriate nutrition. Among the children of medium and high SES, there was likely less risk from partial breast-feeding, and thus less effect from full breast-feeding seen. In a study of prolonged breast-feeding, Victora et al. (17) also found that, among low SES children, those who were breast-fed tended to be larger than those who were not, whereas the inverse was true in the higher SES groups. However, in that study (17) , the benefit of breast-feeding in the low SES group disappeared after controlling for size at birth, mother’s education and parity. Our analysis controlled for mother’s education and size at birth yet still found effect modification by SES, but it is possible that there were additional unmeasured confounders.

Growth from 6 mo to follow-up differed substantially in its association with full breast-feeding compared with growth from birth to 6 mo. In contrast to their larger birth to 6-mo ponderal index increments, infants who were fully breast-fed for at least 4 mo of life had had statistically smaller ponderal index, weight and length increments from 6 mo to follow-up. Further research is warranted to gain an understanding of whether such disparity after 6 mo is due directly to differences in breast-feeding practices, or whether it is due to other unmeasured factors that may differ in association with breast-feeding practices, such as physical activity or quality of complementary foods.

One hypothesis relating directly to infant feeding reflects the association of breast-feeding with reduced morbidity. It is likely that children who were not fully breast-fed for at least 4 mo were exposed to pathogens through contaminated weaning foods at an earlier age. This repeated exposure might have caused slower growth in the first 6 mo as a result of infections, yet allowed for faster growth after 6 mo as a result of acquired immunities and reduced infections. In contrast, perhaps children who were fully breast-fed for at least 4 mo grew faster in the first 6 mo due to reduced infections resulting from greater avoidance of pathogens in contaminated complementary foods. Their slower growth after 6 mo may then have been due to their later introduction to pathogens through contaminated weaning foods and resulting later bouts of diarrhea.

The interaction between mother’s education and the WHO breast-feeding variable with respect to ponderal index from 6 mo to follow-up is difficult to explain. Stratified analysis revealed an inverted U-shaped relationship of breast-feeding with ponderal index across mother’s education groups. Again, perhaps the mother’s education groups acted as proxies for other associated unmeasured factors.

The finding that infants who were relatively heavier had increased odds of full breast-feeding at 2 and 3 mo is similar to findings made by other researchers. Studies in the Philippines (18) , Peru (19) , Chile (20) and Brazil (21) also found that infants of larger size or faster growth were less likely to be subsequently supplemented or weaned, possibly because mothers perceived smaller children as receiving inadequate breast milk and thus needing additional food to improve their growth. Work by Simondon and Simondon (22) also suggested that larger children were not as likely to be weaned as early as children of poor nutritional status. One study in Peru, however, found that mothers were more likely to respond to poor growth by continued breast-feeding (23) , perhaps in the hopes that breast-feeding would help the smaller infants catch up.

Although findings such as these help to elucidate the complexity of the relationship between growth and breast-feeding, they also complicate the interpretation of the observed differences in growth by breast-feeding group. In our regressions, we found that infants who were fully breast-fed for at least 4 mo had larger ponderal index growth increments from birth to 6 mo. However, the fact that babies who were relatively heavier had higher odds of being fully breast-fed at 2 and 3 mo of age likely influenced this finding. Unfortunately, it is impossible to tell from our analysis how much of the association between full breast-feeding and larger ponderal index growth increments is driven by the effects of infant size on feeding. Although our findings for the association between full breast-feeding for at least 4 mo and growth in terms of ponderal index may be biased away from the null, the uncorrected models presented have value in that they capture the net effects associated with full breast-feeding for at least 4 mo on change in ponderal index.

In conclusion, our data reinforce the findings that differences in infant feeding patterns are associated with differences in growth. Furthermore, the relationship may be complicated by factors such as mother’s feeding choices being affected by infant size. Our study also emphasizes the importance of exploring effect modifiers and confounders of the relationship between breast-feeding and growth. Our analysis indicates, for example, that full breast-feeding for at least 4 mo may be particularly important among infants of low SES, but that further contextual variables may be needed to clarify the long-term effects.

	ACKNOWLEDGMENTS

 
The authors thank Mario Flores for his help in assembling the data from the original study and Rosa Olivares Mejia for her tireless work in the field.

	FOOTNOTES

 
¹ Supported by the Hubert Foundation and Transcultural funds for student research in the Department of International Health, Rollins School of Public Health, Emory University.

² Similar data analyses were presented at Experimental Biology 2000, April 2000, San Diego, CA [Roberts. C. L., Rivera. J. A., Flores, M., Maulen, I. & Martorell, R. (2000) Infant feeding practices and growth outcomes at 6 and 20 months of age among Mexican children. FASEB J. 14: A502 (abs.)].

⁴ Abbreviations used: CI, confidence interval; INSP, Instituto Nacional de Salud Publica; OR, odds ratio; SES, socioeconomic status.

Manuscript received January 24, 2001. Initial review completed February 21, 2001. Revision accepted June 26, 2001.

	LITERATURE CITED

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8. World Health Organization Expert Committee (2001) Consultation on the Optimal Duration of Exclusive Breastfeeding. The optimal duration of exclusive breastfeeding. Note for the press no. 7, 2 April 2001 2001 WHO Geneva, Switzerland .

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19. Piwoz E. G., Creed de Kanashiro H., Lopez de Romana G., Black R. E. & Brown K. H. (1994) The relationship between infants’ preceding appetite, illness, and growth performance on mothers’ subsequent feeding decisions. Soc. Sci. Med. 39:851-860.

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