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Original Research Communications |
1 From the Division of Epidemiology, Statistics and Prevention Research, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD.
2 Address reprint requests to MD Overpeck, Division of Epidemiology, Statistics and Prevention Research, NICHD/NIH Building 6100, Room 7B03, 9000 Rockville Pike, Bethesda, MD 20892-7510. E-mail: mary_overpeck{at}nih.gov.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: The objective of this study was to determine whether infants who are exclusively breast-fed for 4 mo differ in average size from infants who are fed in other ways and whether such differences persist through age 5 y.
Design: Data from the third National Health and Nutrition Examination Survey (NHANES III) were linked to birth certificates of US-born infants and children. Feeding groups were defined on the basis of feeding patterns over the first 4 mo of life: exclusively breast-fed for 4 mo, partially breast-fed, breast-fed for <4 mo, and never breast-fed. Growth status, indexed as internally derived z scores (SD units) for weight, length (height), weight-for-length (height), midupper arm circumference, and triceps skinfold thickness, was compared among feeding groups.
Results: The final sample consisted of 5594 non-Hispanic white, non-Hispanic black, and Mexican American infants and children aged 4–71 mo. Of these, 21% were exclusively breast-fed for 4 mo, 10% were partially breast-fed, 24% were breast-fed for <4 mo, and 45% were never breast-fed. At 8–11 mo, infants who were exclusively breast-fed for4 mo had adjusted mean z scores for weight (-0.21; -0.2 kg), weight-for-length (-0.27), and midupper arm circumference (-0.15) that differed significantly from zero (P < 0.05). By 12–23 mo, the differences had dissipated; there were no significant differences subsequent to 5 y. Triceps skinfold thickness was not related to early infant feeding.
Conclusion: Infants who were exclusively breast-fed for 4 mo weighed less at 8–11 mo than did infants who were fed in other ways, but there were few other significant differences in growth status through age 5 y associated with early infant feeding.
Key Words: Breast-feeding • growth • infants • young children • weight • length • midupper arm circumference • triceps skinfold thickness • third National Health and Nutrition Examination Survey • NHANES III
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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6 mo after birth (1). It was recommended that, after the initial period of exclusive breast-feeding, breast-feeding continue through the first year, along with the introduction of complementary solid foods. These American Academy of Pediatrics recommendations are similar to the recommendations of the World Health Organization (WHO) for the first year of life (2, 3).
However, there has been a recurring problem in evaluating the growth of breast-fed infants. Infants who are exclusively breast-fed for 
4 mo and then continuously breast-fed for the remainder of the first year have growth patterns inconsistent with the National Center for Health Statistics (NCHS) growth charts, which have served as the main international growth reference since 1978 (4, 5). The NCHS infant charts were developed on the basis of white, primarily formula-fed infants from Ohio who were measured between 1929 and 1975 and who were fed formulas that resembled breast milk less closely than do current formulas (6, 7). Exclusively breast-fed infants grow more quickly in weight in the first 2–4 mo compared with the NCHS reference. Over the second half of the first year, infants who are breast-fed continuously then show a relative deceleration in weight gain velocity. In a WHO analysis of 226 infants of European descent, infants who were exclusively breast-fed for 4 mo and then continuously breast-fed through the first year reached a low point in weight by 11–12 mo (z score -0.5 SD units) compared with the NCHS reference (2, 3, 8–10). However, in recent studies, formula-fed or predominantly formula-fed infants were shown also to follow this growth pattern of more rapid growth in weight in the first 4 mo and a subsequent decline in weight gain velocity compared with the NCHS reference, albeit to a less dramatic extent (11–14).
The weight gain deceleration among breast-fed infants relative to the NCHS reference has caused concern that mothers may be advised mistakenly to supplement with formula or stop breast-feeding entirely to encourage weight gain. For these reasons, the WHO proposed developing new international infant growth references using breast-fed infants as the physiologic norm (6, 7). In developed countries, an additional concern has been that the growth patterns of formula-fed infants may indicate that these infants are being overfed and that early overfeeding may be a significant risk factor in the development of overweight in childhood (15–18).
The objective of this analysis was to first determine the extent to which the average size of infants aged <1 y who are exclusively breast-fed for 4 mo differs from that of same-aged infants who are fed in other ways, particularly formula-fed infants. A second objective was to determine whether any differences in the first year associated with methods of early infant feeding, which might be expected on the basis of the WHO findings (2, 3), persist through age 5 y. In this analysis, these questions were addressed in a national, cross-sectional sample of infants and young children. Drawing on the strengths of the national data set, we adjusted the findings on growth status for factors related to both mode of infant feeding and growth status in childhood.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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After NHANES III enrollment was complete and the data collection phases ended, birth certificates were sought from each state for the US-born infants and young children in NHANES III who were aged <83 mo at interview (20, 21). The demographic and medical information from the birth certificates stored electronically by birth year (national natality files) for the years 1982–1994 at the Centers for Disease Control and Prevention were linked to the NHANES III file. This linked file formed the basis for the subsequent analyses.
Infant feeding definitions
For the sample of infants and children aged <72 mo, NHANES III obtained current or retrospective information on infant feeding practices at the time of interview (19). Questions included whether or not the infant was ever breast-fed and the age (converted into mo) at which the infant completely stopped breast-feeding, was first fed formula regularly (ie, daily), completely stopped drinking formula, was first fed milk daily, and started eating solid foods daily. Four feeding groups were defined on the basis of infant feeding patterns over the first 4 mo of life (or, 15 wk): exclusively breast-fed for 4 mo, partially breast-fed, breast-fed for <4 mo, and never breast-fed. Because of the rapid drop in the prevalence of breast-feeding between 4 and 6 mo (25%), the cutoff of 4 mo was chosen so that comparisons could be made for later growth status among groups on the basis of feeding patterns reflecting the most common practice.
Exclusively breast-fed infants and children were defined as those who received no supplements (formula, milk, or solids) for at least the first 4 mo of life (through 15 wk). Partially breast-fed infants and children were defined as those who received supplementation (formula, milk, or solids) daily before 4 mo, although breast-feeding continued for 4 mo. Infants and children breast-fed for <4 mo were defined as those who were breast-fed but who were completely weaned before 4 mo of age. Finally, never-breast-fed infants and children were defined as those who reportedly were never breast-fed and were formula-fed from birth. These definitions were necessarily constrained by the nature of the questions asked and the cross-sectional design of NHANES III but were consistent with the definitions used in several other large recent studies that examined the long-term effects of early infant feeding on risk of overweight in childhood (18) and the development of asthma (22).
The prevalence of full breast-feeding was also calculated for each defined month in the first year; the definition used was exclusive breast-feeding for 4 mo followed by continuous breast-feeding with no supplementary formula or milk given. In these prevalence estimates, the denominator was the number of infants and children in the sample who were the defined age or older so that only infants or children with completed behavior were included in the denominator. In other words, infants who were <5 mo of age were excluded from the denominator when they reached 5 mo of age.
Other variables
Birth certificates
Other variables used as exclusion criteria and in the analysis were taken from both the birth certificates and the NHANES III data. The infant's sex and whether the infant was a singleton, a twin, or a triplet were taken from the birth certificate. Maternal parity and infant birth order were based on the number of prior births reported on the birth certificate.
In the national natality files, the standard measure of length of gestation is the number of completed weeks from the mother's last menstrual period (LMP) (23). On the birth certificates, length of gestation from the LMP was examined for completeness and validity. Length of gestation was considered valid if it was between 20 and 44 wk and if birth weight was consistent with gestational age. Gestational age was considered invalid at >44 wk or if, at 
35 wk, birth weight was inconsistent with gestational age from the LMP (24). Clinical estimates of gestational age based on ultrasonography or neonatal examination were not used to replace invalid or missing times from the LMP because clinical estimates were not reported on birth certificates before 1989 and birth certificates were obtained for 1982–1994. Very-preterm delivery was defined as delivery at <33 wk, preterm delivery as delivery at 33–36 wk, and term delivery as delivery at 37 wk.
Infants and children were categorized by birth weight for gestational age status by using reference percentiles derived for singleton infants from recent US vital statistics (25). With use of these reference data, infants were categorized separately by race or ethnicity (non-Hispanic white, Mexican American, or non-Hispanic black) and within race or ethnicity by infant sex and maternal parity (infants of primiparae separate from multiparae). Small for gestational age (SGA), indicating intrauterine growth retardation, was defined as less than the 10th percentile of birth weight for gestation; appropriate for gestational age was defined as the 10th to 89th percentile; and large for gestational age was defined as at or above the 90th percentile.
NHANES III
Race or ethnicity was determined from self-reported NHANES III data, which used categories developed by the US Bureau of the Census (19). Bureau of the Census definitions were used in NHANES III to define type of residence (metropolitan or nonmetropolitan county) and region of residence (northeast, midwest, south, or west), except that Texas was included in the south census region in NHANES III. A metropolitan county was defined as a central or fringe county with a population 1 million. Information on maternal age when the infant was born, maternal smoking status during pregnancy, and whether or not the infant received special care at birth (other than routine neonatal nursery care) and the duration of that care was taken from the questionnaire administered to the infant's or child's parent or other respondent in the home. The education level of the family reference person (FRP) in NHANES III was used as a measure of the educational level of the household.
Anthropometry and growth status
The infants and children were grouped into 7 chronologic age groups: 4–7 mo, 8–11 mo, 12–23 mo (1 y), 24–35 mo (2 y), 36–47 mo (3 y), 48–59 mo (4 y), and 60–71 mo (5 y) based on age at examination. The anthropometric measurements considered as growth status outcomes for these age groups were body weight (in kg), recumbent length (in cm) or standing height (in cm), weight-for-length or weight-for-height, midupper arm circumference (MUAC; in cm), and triceps skinfold thickness (in mm). All body measurements were taken by using standard anthropometric protocols (26, 27). For infants and children aged <36 mo (3 y), measures of recumbent length (in cm) were used to indicate linear growth; standing height (in cm) was used from 36 to 71 mo (3–5 y). Weighted means and SDs of the growth outcomes were estimated separately by sex and age groups by using SAS for WINDOWS (28).
Because there are concerns about differences in length compared with height, to control for group differences (notably, racial or ethnic differences in triceps skinfold thickness) and to scale the values for comparison across age groups (29, 30), the anthropometric outcomes were converted into z scores within chronologic age, sex, and race or ethnicity groups in the final analytic sample. Because race or ethnicity and sex were used as criteria to convert the anthropometric measures to z scores, these variables were not included in the models that compared feeding groups. The z scores were scaled so that for each age group the mean was zero and the SD was 1 (30). Contrasts for growth status were thus made within groups of same-aged infants and children who were fed in different ways in infancy without reliance on external growth references.
Statistical methods
Statistical sample weights were used to account for the oversampling and unit nonresponse. SUDAAN software, which uses a Taylor series expansion to adjust variance estimates to account for the sample design, was used to estimate SEs of the descriptive and prevalent characteristics for the final analytic sample (31).
With use of SUDAAN regression procedures, least-squares means (±SEMs) were derived for birth weight and for z scores, which were derived for the anthropometric variables after adjustment for factors found to be related both to the mode of feeding and to size in infancy and childhood. Birth weight (in g) was adjusted for length of gestation, race or ethnicity, sex, maternal parity, and maternal smoking status during pregnancy. The factors used in the models to adjust growth status were birth weight status (birth weight for gestational age), the timing of the introduction of solid foods, maternal age, mother's smoking status during pregnancy, and the education level of the FRP. Significance was set at 
= 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Twins and triplets (n = 151) and infants and children with missing or invalid information on length of gestation (n = 435) were excluded from the analysis. Infants and children born very preterm (n = 68) also were excluded because they were not likely to have been sufficiently mature at birth for breast-feeding to have been initiated and such children remain small through childhood. For the same reasons, infants with extended periods (14 d) of special neonatal care (n = 111) were excluded. A few infants and children were excluded because of other missing or discrepant key information, ie, birth weight (n = 8), sex (n = 5), and infant feeding practices (n = 6).
The final analytic sample numbered 5594, comprising 73% non-Hispanic white, 17% non-Hispanic black, and 10% Mexican American infants and children, after statistical sample weights were applied to the data (Table 1
). In the final sample, there were slightly fewer SGA infants than expected, which is consistent with the exclusion of infants with very-preterm delivery (<33 wk) and extended special neonatal care. Solid foods were introduced daily at <4 mo for 25% of the sample; just <25% of the mothers smoked during pregnancy.
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). The total percentage of infants or children who were exclusively breast-fed for 4 mo was 21.0%, whereas another 24.0% were breast-fed for <4 mo. A much smaller percentage (9.8%) was partially breast-fed (breast- and formula-fed) for 4 mo.
After 4 mo, the prevalence of full breast-feeding declined monthly (Table 2). At age 6 mo, 15.8% of the infants had been exclusively breast-fed for 4 mo and then breast-fed continuously through 6 mo. At age 9 mo, 8.7% of the infants had been exclusively breast-fed for 4 mo and then continuously through 9 mo. At age 12 mo, only 5.2% of the US-born infants and children in NHANES III were still being breast-fed after being exclusively breast-fed for 4 mo or had been exclusively breast-fed for 4 mo and then continuously through the first year of life.
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35 y) and nonsmokers, to reside in the west census region, and to be born into families in which the FRP had a minimum of a college education (Table 3). Infants who were exclusively breast-fed for 4 mo were much less likely to be SGA. On the other hand, never-breast-fed infants and children were much more likely to be non-Hispanic black, be SGA, be born to teenaged mothers (aged <19 y) and to smokers, reside in the south census region, and be born into families in which the FRP had less than a high school education (Table 3).
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). After adjustment for gestational age (in wk), race or ethnicity, infant sex, maternal parity, and maternal smoking status during pregnancy, the least-squares means for birth weight of exclusively and partially breast-fed infants were nearly 100 g larger than those of never-breast-fed infants. Infants who were breast-fed for <4 mo were also smaller at birth than were those who went on to be exclusively or partially breast-fed.
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for weight (in kg) and length (height; in cm). Least-squares means (±SEMs) were derived for the anthropometric z scores, with adjustment for factors associated both with infant feeding mode and with infant and child growth status. These factors were birth weight status (birth weight for gestational age), the early introduction of solid foods (at age <4 mo), maternal age, maternal smoking status during pregnancy, and the FRP’s level of education. At 4–7 mo, none of the 4 feeding groups had an average z score for weight that differed significantly from zero (Table 6; Figure 1). However, in a reversal of their standing at birth, infants who were exclusively breast-fed or partially did have average z scores slightly below zero, whereas those who were breast-fed for <4 mo or never breast-fed had scores slightly above zero.
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). Because the SD for weight at 8–11 mo of age is 1 kg for both boys and girls (Table 5), this translates into a difference of -0.2 kg for infants who weigh 8–10 kg at these ages. The weight difference is mirrored by a significantly lower weight-for-length z score at 8–11 mo (-0.27). There was also a significantly lower MUAC z score at 8–11 mo (-0.15), a discrepancy of –2 mm, affirming the association between early exclusive breast-feeding and relatively lower weight and weight-for-length z scores at age 8–11 mo (Table 6). At age 12–23 mo (1 y), the discrepancy in infant weight and weight-for-length for the exclusively breast-fed infants disappeared. At 12–23 mo and at subsequent age intervals to 5 y, none of the mean z scores were significantly different from zero. There was little evidence that never-breast-fed (formula-fed) infants and children were significantly heavier than were the infants and children in the other groups either in the first year of life or through age 5 y.
The findings were similar for length (height) (Figure 2). Through 35 mo, none of the mean z scores differed significantly from zero, deviating by only ±0.10 (Table 6). At 36 mo, only children who were partially breast-fed showed a consistent deviation. Children who were partially breast-fed appeared to be taller by 1.1 cm on the basis of an SD of 4.5 cm for height at 3–5 y of age.
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). There was no comparable difference at 8–11 mo for triceps skinfold thickness. At 48–59 mo (4 y), the MUAC z score of children who were never breast-fed was positive (0.17 ± 0.08) and significantly different from zero, but there was no significant effect at these ages for weight or weight-for-height and the effect did not hold through age 5 y. Triceps skinfold thickness, as a measure of arm fatness, was remarkable in showing no consistent, significant relation with method of early infant feeding. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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12 mo were exclusively breast-fed for 4 mo and then fully breast-fed (ie, no other sources of milk) continuously through the first year. Our findings are consistent both with the prevalence data on overall breast-feeding and with demographic associations reported in other national studies in the same time frame (32–34). For 1987, the prevalence of children in the National Survey of Family Growth who were ever breast-fed was 56.3% and the prevalence of breast-feeding at 1 wk in the Ross Laboratories Mothers' Survey was 54.7% (32). This latter percentage from the Ross Laboratories Mothers' Survey is identical to the combined percentage (54.7%) of infants or children who were exclusively breast-fed for 4 mo, partially breast-fed, or breast-fed for <4 mo in our analytic sample from NHANES III.
Not long after the adoption of the 1977 NCHS reference as the international benchmark for infant growth, studies in developed countries showed differences in growth for breast-fed infants compared with the NCHS reference (35, 36). In the latest WHO evaluation of infant growth, longitudinal data from 7 studies comprising 226 US, Canadian, and Northern European infants who were exclusively breast-fed for 4 mo but then continuously breast-fed through 12 mo were pooled (2, 3, 8). These 226 infants were born to mothers who were relatively older than average (aged 30.0 ± 4.4 y) and highly educated (15.9 ± 2.2 y), and the infants were all born at term with appropriate birth weights (3478 ± 412 g). The main finding of the WHO study, in which breast-fed infants were compared with the 1977 NCHS reference, was that the weight curves for the breast-fed infants showed a downward trend after 2–3 mo to –0.5 SDU at 12 mo (2, 3). In our analyses, we also found that there was a weight disparity in the latter part of the first year (8–11 mo) between infants who were exclusively breast-fed for 4 mo and infants who were fed in other ways, but the magnitude of the difference (200 g) was far less than that found in the WHO study, in which the growth of infants who were exclusively breast-fed for 4 mo and then further breast-fed to 12 mo was compared with the NCHS reference (2, 3).
In NHANES III, after adjustment for factors known to be associated with infant feeding and infant growth, infants at 8–11 mo who were exclusively breast-fed for 4 mo (21% of the sample) had a mean z score for weight of -0.2 and of weight-for-length (height) of -0.3, indicating a disparity in weight at these ages compared with infants who were partially breast-fed, breast-fed for <4 mo, or never breast-fed. This translated into a difference of -0.2 kg for infants who weigh 8–10 kg at these ages. A similar difference in MUAC was seen for exclusively breast-fed infants at 8–11 mo of age (z score, -0.15; -2 mm), confirming the relation between early infant feeding and weight.
However, at 12–23 mo (1 y), the weight discrepancy of the infants who were exclusively breast-fed for 4 mo had disappeared, and there were no significant differences among the feeding groups in subsequent age intervals to 5 y. There was no overwhelming evidence that never-breast-fed (formula-fed) infants and children were significantly heavier on average in the first year of life or through age 5 y than were breast-fed infants. Length (height) and triceps skinfold thickness were generally unrelated to early infant feeding in these analyses, with the exception that partially breast-fed children appeared to be somewhat taller (by 1 cm) from age 3 y onward.
Many hypotheses have been put forth to explain why breast-fed infants may gain less weight in the first year of life than do formula-fed infants, or, more appropriately, why formula-fed infants may gain more weight. In comparing breast-fed with formula-fed infants, studies have shown differences related to intake and the nutritional composition of breast milk compared with formula and in activity levels (37–41).
Breast-fed infants who are fed on demand maintain lower nitrogen and energy intakes, especially over the first 4–6 mo of life, than do formula-fed infants (37–40). It has been suggested that the higher nitrogen and energy intakes of formula-fed infants may stimulate insulin and insulin-like growth factor I secretion, leading to increased weight gain without necessarily affecting linear growth.
Worobey (41) showed recently that feeding method was strongly associated with total physical activity at 3 mo of age, as measured by actometry of the limbs. Total activity, especially the activity of the upper limbs, was significantly higher for breast-fed than for formula-fed infants. This might also explain why the infants who were exclusively breast-fed for 4 mo had smaller MUACs in our analysis and, if higher activity is sustained, why breast-fed infants may gain less weight through the first year and be leaner (10, 42).
The NCHS growth charts for infants are currently being revised and will include NHANES III data. Breast-fed infants will therefore be represented in the new reference. Nevertheless, we suspect that exclusively breast-fed infants in the United States will probably still show slower weight gain in the first 12 mo of life compared with formula-fed infants when weight is plotted on the revised charts. However, because the magnitude of the discrepancy in weight gain between these 2 groups is relatively modest (200 g), it is unlikely that mothers would be alarmed and counseled to supplement a healthy, breast-fed infant on this basis. Clinicians should also be assured by the fact that such discrepancies in weight gain are usually transitory. For the smaller fraction of US infants who are breast-fed continuously for 12 mo and whose lower rate of weight gain, when plotted on the new NCHS charts, may be more substantial and alarming, clinicians can be advised to refer to the WHO reference for breast-fed infants when they become available (6, 7).
Overweight and obesity in childhood is a growing problem in the United States; findings from NHANES III (1988–1994) established that children as young as 4–5 y, especially girls and Mexican American children, show a higher prevalence of overweight than indicated by earlier surveys (43). The findings from our analyses clearly do not support the hypothesis that early formula-feeding per se is necessarily contributing to this increased prevalence in early childhood overweight by shifting the distribution of weight to the right for formula-fed infants and children. In fact, during the same time that an increase in the prevalence of overweight was observed, the numbers of women both initiating breast-feeding and still breast-feeding at 6 mo have also increased (34), and the composition of infant formulas has evolved to more closely emulate the nutrient composition of breast milk (7). After adjustment for factors associated with both infant growth status and feeding mode, no formula-fed infants or children up to the age of 5 y were heavier or fatter on average than those who were breast-fed. Therefore, attention should be focused on other aspects of the diets and physical activity of infants and children to identify factors associated with the increased prevalence of overweight in young children, while recognizing that breast-feeding is the preferred method of feeding for all infants and should be strongly encouraged (1).
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), partially breast-fed (
), breast-fed for <4 mo (
), and never-breast-fed (•). Values were derived from models in which birth weight status, education of the family reference person in the third National Health and Nutrition Examination Survey, maternal age and smoking status during pregnancy, and the early introduction of solid foods (age4 mo) were adjusted for. Only the least-squares mean at age 8–11 mo for exclusively breast-fed infants is significantly different from zero (P < 0.05).