The current international growth reference from the National Center for Health Statistics (NCHS) is widely used to compare the nutritional status of populations and to assess the growth of individual children worldwide. Recently, concern has been raised regarding the adequacy of these references for assessing the growth of breast-fed (BF) infants.
The NCHS reference was developed in the United States in 1975 by pooling four different sources of data (1). The reference for 2- to 18-year-old children was based on data from three representative surveys conducted in the United States between 1960 and 1975. Data on younger children came from the Fels Longitudinal Study conducted in Yellow Springs, Ohio, during a 46-year period (1929–1975). The children in the Fels study were predominantly bottle fed (BOF) and were all from restricted socioeconomic and genetic backgrounds. In addition, the NCHS reference is characterized by a positive skew in the weight distribution, reflecting substantial levels of childhood obesity (2). Another major concern is that negative deviations of exclusively BF children from the NCHS reference have caused health professionals to diagnose growth faltering, thereby leading to the early introduction of nonhuman milk or other complement. This, in turn, often causes the early introduction of complementary foods with consequent faltering. This concept has gained some attention recently (3–5).
Women often stop breast feeding because they are dissatisfied with the child's growth (6). Health care profes-sionals who notice that the BF child is not reaching the expected achievements based on the NCHS growth curve often encourage bottle feeding. However, prolonged breast feeding has repeatedly been shown to protect against diarrheal disease (7–8) and other infections (9). Dewey et al. (10) suggested that new growth charts are needed for BF infants. Agostoni et al. (5) demonstrated differences in height and weight between BF and BOF infants in Italy, and the differences were later confirmed by Hediger et al. (11) based on a US population. Most studies have been cross-sectional. Moreover, it is difficult to compare the few longitudinal studies. The World Health Organization (WHO) Working Group on the Growth Reference Protocol (12) compared growth data from seven countries and found that Chinese infants were approximately 3% shorter at 12 months of age and Indian infants weighed as much as 15% less than did Australian infants. In Bangladeshi children, a low growth velocity persisted to 3 years of age (12). Controversy exists concerning the long-term effects of breast feeding. Whether breast feeding is protective against obesity in children and adolescents is under debate; while von Kries et al. (13) and Tulldahl et al. (14) report a protective effect of breast feeding against obesity, Hediger et al. (15) found no support for the theory. The purpose of this study was to evaluate the growth of BF infants from different ethnic origins in relation to the NCHS reference for growth. The uniquely diverse population that exists in Israel, with people immigrating from both affluent and developing societies, enabled us to evaluate any potential differences between infants of mothers coming from different cultural and socioeconomic backgrounds. It should be stressed that most of the studies reported to date have been cross-sectional, whereas our report is longitudinal to final height.
CHILDREN AND METHODS
Subjects: A database of Israeli-born children was initiated in 1977. Longitudinal data were collected on all children. A total of 1960 healthy children (961 boys) who reached final height at the time of analysis were included in the study. Six hundred thirteen of these children were breast fed for 1 year and 218 for 6 months.
Anthropometry: Weight and length from birth to 2 years of age were measured with the infants naked and with standing height using a wall mounted Stadiometer; weight was measured in underwear thereafter. The weight and length measurement errors were 35 g and 4 mm, respectively, for infants, and 100 g and 2 mm, respectively, for adults.
Catch-up growth was defined as an increase of at least 0.02 SD in Z score for weight and length during a period of 3 months (twice the standard deviation of the expected change in observations of BOF children measured between 3 and 6, 6 and 9, and 9 and 12 months of age) in two consecutive 3-month periods. BOF children were used as our reference base (n = 1129).
Final height was defined as that at which, within 1 year, the growth increment was <0.5 cm. Adult weight was recorded at that time and BMI calculated.
Clinic visiting intervals were 1 to 2 months for the first 6 months of life, no more than 3 months during the following 18 months of life, and yearly measurements thereafter, until they reached final height. At each visit, anthropometric measurements were obtained and recorded.
Inclusion criteria: gestational age 37 to 42 weeks, birth weight of 2.5–5.0 kg.
Exclusion criteria: Apgar score of < 7 or any chronic disease or birth defect.
Breast-fed (BF) group: Growth data on infants being fully breast fed, i.e., given no solids and only minimal fluids (less than 50 mL/day) other than human milk. Two hundred eighteen children were BF for 0.5 year, 613 for 1 year.
Bottle-fed group (BOF): One thousand one hundred twenty-nine children were bottle fed for 2 years. This group included infants who were BF ≤ 2 weeks. Children breast fed 5.5 to 6.4 months were included in the breast fed for 6 months group. Children breast fed 11.5 to 12.4 months were included in the breast-fed for 12 months group. Children breast fed > 2 weeks but < 5.5 months were not included in the analysis. Likewise, children breast fed > 6.5 months and < 11.5 months were not included in the analysis.
Reference growth charts
The 50th percentile of our population corresponds to the 50th percentile of Tanner-Whitehouse growth charts (16). Cole's reference charts were used for BMI and BMI SDS calculations (17)
Nutrition: On each visit food intake history was recorded and dietary recommendations were made. Each child had a personal health chart record, with information on the duration of breast feeding, the use of supplemental milk formulas and solid foods and the timing of their introduction recorded at each visit.
Statistical analysis was performed using Sigmastat (version 2) and Table Curve (version 4), SPSS Inc. (Chicago, IL). For each child, measurement accuracy was monitored by analysis of the regression line of the child's growth curve (3rd order polynom). Data measurements that deviated more than 2.5 SD from the regression line were eliminated.
Data were interpolated to the nearest month of age using cubic interpolation. Comparison of groups was performed by two-way analysis of variance and t test.
A total of 1960 children (961 boys) reached final height by the time the statistics were calculated; their results are presented in the study. Others did not reach final height by the time the analysis was performed.
Because the difference in size between the boys and girls was ≤ 5%, the groups were combined. Less than 5% of the children were lost to follow-up. Data were collected from eight well-baby clinics, randomly selected, and located in different parts of the country.
Ethnicity, education and socioeconomic level: Children were divided into six ethnic categories: Western European (21.4%), North African (23.1%), Iraqi-Irani (19.2%), Yemenite (15.6%), Ethiopian (6.2%), and Middle Eastern (14.5%). Clinics varied in terms of the lifestyles and socioeconomic backgrounds of the families, with 22% in urban areas, 22% in rural areas, and 56% in suburban zones; educational background: 6% never attended school, 14.3% completed primary school, 66.7% completed high school, and 13% had a higher education. Of the study participants, 5.5% had a very low income, 16.5% a borderline income, and 78% an average income; 19.6% of the BF infants came from borderline- or low-income families.
The first component of our analysis demonstrates that growth patterns of the Israeli-born BF and BOF infants were similar among different ethnic groups who immigrated to Israel from Africa, Asia, and Europe. As an example, Table 1 demonstrates height data of BF boys of different ethnic origin who were followed up to 24 months. There was no significant difference in length or weight within the individual groups (ANOVA within each age group was measured every 3 months from birth to 2 years of age).
The magnitude of the decline between birth and 1 year of age in Z scores of BF versus BOF infants was not as great for height as for weight, −0.2 and −0.3, respectively, and disappeared at 2 years of age. Differences in Z score among groups were analyzed by two-factor repeated-measure ANOVA (gender and length of BF) for each age group (Tables 2, 3, and 4). A similar analysis on the weight for height demonstrated a decrease in Z score between birth and the end of the first year in BF compared with BOF children by 0.3 Z score. The main decline in Z score of weight was noted in BOF boys and girls for weight between 9 and 15 months of age (Table 2), in Z score of length in boys and girls between 9 and 18 months of age (Table 3), and in BMI SD (Table 4) between 9 and 12 months of age.
Children who were switched to bottle feeding exhibited a growth spurt. No differences in final anthropometries were detected between children of different ethnic origins. Table 5 compares final heights of BF and BOF children and their parents. There was no difference in final heights of BOF and BF children of the same sex (t test).
The percentage of children reaching adult height by 18 years of age who were > 2 SD above the BMI mean for gender and age was similar in the BF and BOF groups (12/256 = 4.69% and 18/381 = 4.72%, respectively). Adult BMI was similar between the BF and BOF groups (Table 5). Maternal BMI SD correlated with offspring BMI-SD at 18 years of age (r = 0.883, P < 0.001, n = 256 for BF and r = 0.870 for BOF, and r = 0.873, P < 0.001 for all subjects, n = 637).
In 1994, the WHO Working Group on Infant Growth summarized the data gathered by investigators from six countries in 1992 (18). Additional work along these lines was continued (12). All studies complied with consecutive anthropometric measurements for at least 12 months of term BF infants. The slower growth of BF infants after the first 2 months was more evident in terms of weight than length. The slower growth of BF infants relative to the current NCHS WHO reference may reflect inadequacies in human milk volume or composition, and thus should not necessarily be considered “normal” or “optimal.” However, the most striking deviation from the current NCHS WHO reference occurred during the second 6 months of life, when the infants in these studies were receiving solid foods. The data apply to infants with heterogeneous diets. If the infants were not receiving sufficient human milk, they presumably could have made up for this by consuming more solids, unless meal frequency was inadequate or the nutrient quality of complementary foods was poor. Other studies have shown that BF infants self-regulate not only their milk intake (19) but also their energy intake from solid foods (20), and that their energy intakes are not a function of inadequate maternal milk production (19).
There is no way of systematically evaluating the assumption that maximal growth is desirable. One way to determine whether the growth patterns of BF infants are “optimal” is to examine functional outcomes, such as activity, behavioral development, and morbidity. Current evidence indicates that the slower weight gain of BF infants living under desirable conditions is not associated with obvious deleterious functional consequences (20). In fact, there is some evidence that cognitive development is enhanced (21) and that BF infants have lower rates of illness than do their formula-fed counterparts (20,22). One limitation also appreciated by the WHO committee itself in its comprehensive report was the sample size of the data available to the committee: 226 BF children, which is smaller than desirable for estimating the extreme percentiles (i.e., 95% and 5%) of distribution. A sample size of at least 400 (200 males and 200 females) is necessary to estimate the +2 and −2 SD cut-off with 95% confidence within 239 g for weight and 0.6 cm for length. In addition, data were lacking with respect to the second year, when malnutrition is more prevalent. BF children who do not receive supplementation as their nutritional needs increase are at risk for malnutrition. Breast milk alone is probably not sufficient for optimal growth after about 6 months of life (23), and inadequate supplementation at this stage (i.e., the second half of the first year of life) is the most likely mechanism via which prolonged breast feeding could impair growth.
Some investigators have observed that BF children have a reduced appetite for added foods (24–25). It is not clear whether breast milk truly causes anorexia or whether it simply satisfies the child's nutritional requirements (26). Recently, a WHO Working Group compared, in a pilot study, growth patterns of breast-fed infants in seven countries (12), with approximately 120 infants per site. Two to four weekly length measurements were done of breast-fed infants from selected sites in Australia, Chile, China, Guatemala, India, Nigeria, and Sweden. The researchers concluded that the growth pattern of infants from most sites were strikingly similar, but relative to the Australians (the reference category), the Chinese infants were approximately 3% shorter at 12 months of age and the Indian infants weighed as much as 15% less. Could there be genetic or regional differences in growth? Although these results are suggestive, a larger study is needed.
A large-scale longitudinal study, which follows the growth of children from birth, may overcome many of the problems encountered in previous studies. In the study presented here, we monitored the mother's nutritional status, socioeconomic status, ethnicity, and cultural habits through close monitoring at mother and child health care centers and were able to exclude the possibility of malnutrition being a confounding factor in the observed growth pattern.
By restricting our study to these facilities, the suspicion of a relationship between breast feeding and malnutrition can be withdrawn. Nevertheless, the long-term effect of infant nutrition on adult habitus needs to be further explored. Reports on the protective effect of breast feeding against adult obesity were not conclusive (14,15). From our data, it appears that adult obesity in this sample population was correlated with maternal obesity but not with breast feeding.
At this time, mothers should be encouraged to breast feed. The health care provider should take into account that BF children grow in a particular way as long as they are breast fed, and no supplementation should be offered if the child follows a reasonable growth pattern. The final height and weight of BF children does not differ from that of BOF children. Because the NCHS growth curves may not express the growth patterns of BF children, a different growth curve should be established for this group. Such curves, sponsored by WHO, are now in progress.
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