Anthropometric indices are commonly used as the principal criteria in assessing the adequacy of nutrition in early childhood. This is true because realization of the genetically determined growth potential of normal infants and children depends, among other factors, on the availability of adequate amounts of nutrients. The World Health Organization (WHO) recommends that normal infants be breast-fed exclusively from birth to 4 to 6 months of age—that is, they should be given no liquids or solids other than breast-milk during this period. After this initial period of exclusive breast-feeding, infants should continue to be breast-fed up to 2 years of age or beyond while receiving nutritionally adequate and safe complementary foods (1,2). It is well documented that the growth pattern of formula-fed infants differs from that of breast-fed infants (3–12). We have recently reported preliminary data from the Euro-Growth Study that indicate that small influence of early nutrition on growth may persist until 24 months of age (13).
The universally used National Center for Health Statistics (NCHS)-WHO (14,15) growth references, aside from being technically inadequate, provide no information regarding feeding during infancy of the subjects who provided the anthropometric data. The large sample size of the Euro-Growth cohort and the detailed information regarding feeding of children from birth to age 3 years (16,17) provided the opportunity to assess the influence of feeding mode on growth. In particular, it was possible to identify a large group of infants who were fed according to the present WHO recommendations (1,2). The present report describes the growth of this group in comparison with that of children who were fed in different ways. Mid-parental height and other factors that are related to growth during early childhood (16,17) were taken into account. Growth of the children who were fed according to the present WHO recommendations (1,2) was also compared with the NCHS-WHO (14,15) and Euro-Growth (17) references.
Study Population and Protocol
The Euro-Growth Study was a longitudinal, observational multicenter study in which standardized methodology was used. Healthy term infants of gestational ages between 37 and 44 weeks who had no signs of intrauterine growth pathology and who did not meet the other exclusion criteria (16) were enrolled before 30 days of age. The cohort consisted of 2245 children from 22 study sites who visited the study sites at 1, 2, 3, 4, 5, 6, 9, 12, 18, 24, 30, and 36 months of age for anthropometric measurements and for collection of demographic data. For reasons discussed previously (16) the data from one site (at enrollment, n = 100) were not used for the construction of growth references for breast-fed boys and girls, leaving 2145 children for analysis. The sample, the experimental design, and the methods have been described in detail (16). With the use of standardized smoothing procedures, reference data (Euro-Growth references) for length, weight, and body circumferences were generated and have been published previously (17). References for gain in length and in weight have also been produced (18), as have references for body mass index (BMI) (19).
Information about feeding was obtained through interviews conducted with the infant's caretaker (almost always the mother) during each study visit. The following information was obtained: breast-feeding (frequency, exclusive, full, or partially). Based on this information, infants were classified according to WHO criteria (20) as exclusively breast-fed if breast milk was the only food source; as fully breast-fed if breast milk was the only milk source but solid foods were also fed; and as partially breast-fed if the infants received any breast milk in addition to milk and solids. Bottle feeding, if any (type, amount, and frequency); other fluids and solid foods, if any (type, amount, and frequency); and dietary supplements, if any (type, amount, and frequency).
Two approaches were used to examine the effect of feeding on growth. For the first of these, subjects were categorized according to WHO criteria (20). The WHO group comprised 319 infants who were breast fed exclusively until 4 to 6 months of age; the early solids group comprised 185 infants who were fully breast-fed until 4 to 6 months of age but who were fed solid foods before 4 months of age; and the control group, which comprised 1509 infants who did not meet the criteria for inclusion in one of the above groups. For 132 subjects insufficient information was available to permit categorization. For each of the three feeding groups, mean SD z-scores based on the overall cohort (n = 2145) (17,19) were calculated for recumbent length, weight, and body mass index for all target ages. Differences between feeding groups were examined by analysis of covariance, using mid-parent height and educational level of the mother as covariates. Mid-parent height was shown to be of significant influence on growth performance in the Euro-Growth cohort (17). Educational level of the mother was selected because it is known that educational stratum can influence growth and nutrition (16).
To check for possible selectivity in withdrawals, for each of the three feeding groups z-scores were also calculated for those children for whom complete longitudinal data were available through 36 months of age (the WHO-L, early solids-L, and control-L groups).
The second approach was primarily designed to examine the influence on growth of the duration of breast-feeding and of the introduction of solids. For this, multiple regression analysis was used. Dependent variables were increments in length (in millimeters per month) and weight (in grams per month) and change in body mass index (in kilograms per square meters per year) during the age intervals 1 to 4, 1 to 12, 1 to 24, and 1 to 36 months. Duration of breast-feeding, defined as the age (month) at which any breast-feeding ceased, and age of introduction of solids (month) were the independent variables. Interactions between breast-feeding and solids were also considered. Additional independent variables in the model were sex (0 = male; 1 = female), educational level of the mother (levels 1 through 5, 16,17), and mid-parental height (in decimeters).
Length, weight, BMI, head circumference and mid-upper arm circumference (MUAC; in centimeters) for the boys and girls in the feeding group WHO (not corrected for covariates) were calculated for all target ages. The values representing selected percentiles (P; P5, P10, P25, and P50; and P75, P90, and P95), the mean and standard deviation (SD) are presented. Mean (SD) z-scores for length and weight of the WHO feeding group were compared with the NCHS-WHO (14,15) and Euro-Growth references (17). Because the NCHS-WHO references apply to standing height between 24 and 36 months of age (21,22), for this comparison 5 mm was subtracted from the Euro-Growth references for breast-fed boys and girls (16,17).
The first section of Table 1 presents, for the entire cohort, feeding modes during the first year of life. The category fully breast-fed includes, in addition to fully breast-fed infants, those who were exclusively breast-fed. During the first 2 months of life, 54% of infants were exclusively or fully breast-fed, whereas an additional 20% received breast milk in addition to other feedings. The prevalence of breast-feeding declined during the first year of life, so that by 9 to 12 months of age 5% of the infants were fully breast fed and an additional 13% received breast milk in addition to food from other sources. Seven percent of children were breast fed into the second year of life.
The 319 infants in the WHO feeding group were, by definition, exclusively breast-fed through 4 to 5 months of age. After that period, solids were increasingly introduced and by 9 to 12 months of age, all infants received solids. Breast-feeding continued in most of these infants, and at 9 to 12 months of age 54% were still breast-fed, and 28% were breast fed beyond 12 months of age. At 24 months of age, less than 3% were breast fed (data not shown). The early solids feeding group comprised 185 infants who were fully breast fed through 4 to 5 months of age while also receiving solids before 4 to 5 months of age. At 1 to 2 months of age, 4% of these infants received solids and by 4 to 5 months of age, by definition, 100% were receiving solids. In this group, too, breast-feeding continued at a higher rate than in the entire cohort. By 9 to 12 months of age, 31% were breast fed, and a full 18% continued to be breast fed in the second year of life. In the control feeding group (n = 1509) the percentage of infants who were breast fed was substantially lower than in the two other groups at each target age. Sixty five percent were receiving formula between 1 and 2 months of age.
Mean z-scores for length, weight, and BMI of the three feeding groups are presented in Tables 2, 3, and 4. Table 2 also indicates for each target age the number of subjects for whom measurements were available. It is evident that at each target age a few subjects are missing because they missed the examination altogether or did not have the examination within the required age interval (16). Declines in numbers after 12 months and 24 months are explained by the fact that some sites did not perform measurements past those ages (16).
The WHO group had lower z-scores for length than the control group after 3 months of age. The difference was statistically significant between 4 and 12 months (Table 2). Similarly, z-scores for weight were significantly lower in the WHO group between 5 and 12 months of age than in the control group (Table 3). However, at 1 and 2 months of age, weight z-scores of the WHO group were significantly higher than in the control group. Corresponding to this greater weight during the early months of life, z-scores for BMI of the WHO group were significantly higher during months 1, 2, and 3 (Table 4). The growth pattern of the WHO group thus consisted of higher weight during the first 2 to 3 months of life (and higher BMI) and lower weight and length from 6 to 12 months of age compared with the control group. During the second year of life, differences were small and not statistically significant. However, at 30 and 36 months of age, length in the WHO group was significantly less than that of the other group.
The early solids group showed a pattern of growth that was distinctively different from that of the WHO group. That group tended to have higher z-scores for length than the WHO group throughout the first year of life (statistically significant during months 5 and 6) but lower z-scores for weight. As a consequence of these opposing differences, from 1 to 12 months of age they had significantly lower z-scores for BMI than the WHO group. Thus, growth in the early solids group showed greater leanness throughout the first year of life. During the second year of life, length and weight in the early solids group became more similar to those in the WHO group, but during the third year of life, the differences in length and weight widened again.
To check whether possible selectivity in withdrawal could have produced the observed differences in anthropometric measurements, the analysis was repeated with only the data for those subjects who participated in the study from beginning to end. The mean z-scores of the groups WHO-L (n = 160), early solids-L (n = 86), and control-L (n = 710) are included in Tables 2, 3, and 4. It is evident that the values for this longitudinal cohort show essentially the same differences as the original values. The WHO-L group had significantly lower z-scores for length than the control-L group at almost all target ages between 4 and 36 months of age. The early solids-L group had significantly lower z-scores for BMI than the WHO-L group at almost all target ages between 1 and 36 months of age. Thus the data do not indicate the presence of selectivity in withdrawals (16) in the WHO and early solids groups.
Multiple regression analysis was used to assess the influence on growth of the duration of breast-feeding and of the age of introduction of solids. There were significant interactions between breast-feeding and introduction of solids for gain in length and weight during the age interval of 1 to 4 months, making the interpretation difficult. No interactions existed during the age intervals 1 to 12, 1 to 24, and 1 to 36 months. The results are summarized in Table 5. Duration of breast-feeding was negatively correlated to gains in length and weight between 1 and 12 months and 1 and 24 months of age. A 1-month difference in duration of breast-feeding was related to differences in monthly length and weight gains (1–12 months) of 0.12 mm and 8 g. The age of introduction of solids was positively correlated to length gain between 1 and 24 months of age and weight gain between 1 and 12 months of age. A 10-cm difference in mid-parental height was related to differences in monthly length-and weight gains (1–12 months) of 0.8 mm and 34 g. Between 1 and 36 months of age, the duration of breast-feeding was no longer related to gains in length and weight, but the influence of mid-parental height remained highly significant (P < 0.001; data not shown). The duration of breast-feeding was negatively correlated to changes in BMI between 1 and 12 and 1 and 24 months but not between 1 and 36 months of age. The age of introduction of solids was positively correlated to change in BMI between 1 and 12 months of age but no longer between 1 and 24 and 1 and 36 months of age.
Euro-Growth references for breast-fed boys and girls (WHO group) are presented for length (Appendix 1), weight (Appendix 2), BMI (Appendix 3), head circumference (Appendix 4), and MUAC (Appendix 5) (Figs. 1, 2).
The Euro-Growth references for breast-fed children were compared with the NCHS-WHO (14,15) and Euro-Growth (17) references by expressing three selected z-score values of breast-fed children (-1, 0, +1,) as NCHS or Euro-Growth z-scores. Comparison with the NCHS-WHO reference (14,15) (Fig. 1) indicated that mean z-score for length at birth was slightly higher (+0.15) and the SD z-score was smaller (0.85). Differences in mean z-scores for length were small until 18 months of age (Fig. 1). At 24 months of age, the problems related to the length–height disjunction of the NCHS-WHO reference (14,15) resulted in a higher mean z-score of +0.67. The variances for length (SD z-scores between 0.83 and 1.0) were smaller at almost all target ages than the corresponding variances of the NCHS-WHO reference (14,15). Mean z-score for birth weight (Fig. 2) was higher (+0.37) and SD z-score was slightly smaller (0.92). Differences in mean z-scores for weight were large between birth and 4 months and ranged from 0.39 to 0.51 (Fig. 2). At 9 and 12 months of age, differences were small (-0.02), but they increased again thereafter. The variances for weight (0.71–1.0) were smaller at almost all target ages than the corresponding variances of the NCHS-WHO reference (14,15).
Comparison with the Euro-Growth reference (17) (Fig. 1) indicated that differences in mean z-scores for length were small and ranged from -0.26 to +0.14 at all target ages. Differences in mean z-scores for weight at 1 and 2 months of age were 0.30 and 0.28 (Fig. 2). After 2 months of age, differences in mean z-scores were <0.15. The variances for length (1-SD z-score 0.93–1.04) and weight (0.92–1.02) were similar to the Euro-Growth reference (17).
The present analysis of data from the Euro-Growth Study focused on the complex relation between nutrition and growth. With the large sample size of the Euro-Growth Study it was possible to examine the impact on growth of two key recommendations that are part of many national and international infant feeding recommendations: the duration of breast-feeding and the age of introduction of solids (1,2). The sample of the Euro-Growth Study was approximately representative of the background population surrounding the 21 study sites and included children from a range of European regions with a diversity of socioeconomic characteristics (16,17). Educational level of the mothers in the Euro-Growth population was slightly biased (+1 year) toward an above-average educational stratum of the European population (16). Factors such as mid-parental height and sex were taken into account in the present analysis, because earlier analysis (16,17) had indicated a strong effect of these two variables on infant growth. Of 319 infants in the Euro-Growth Study who were fed according to WHO feeding recommendations, 290 provided data through 12 months of age, 219 through 24 months of age, and 160 through 36 months of age. Sample size was too small to assess growth (10,16) of those children who were breast fed beyond 12 months of age.
Several well-designed studies (3–9) have provided data on length, weight, and indices of body fat in infants fed according to WHO feeding recommendations (1,2). These are the studies that provided the data used for the construction of the WHO growth reference (10,11). The cohorts were smaller (between 44 and 144 infants) than our breast-fed cohort and somewhat more highly selective (i.e., maternal educational levels were generally high; mean 15.9 years) (10,12). Factors with potential influence on early growth, such as mid-parental height, were described as potential confounders but were not included in the data analysis (10,12). Only a minority of children was monitored beyond 12 months of age. These studies (3–9) indicated that the typical growth pattern of infants who are fed according to the WHO recommendations (1,2) is to gain weight more rapidly than formula-fed infants during the first 2 months of life but to show relative deceleration thereafter. Therefore, the growth of breast-fed infants often gives the impression of faltering after the first 2 to 3 months of life (10–12). In the present study we did not select a group of formula-fed group infants for comparison. Rather, we used as reference all infants who were not fed according to WHO recommendations. Sixty-five percent of the reference group was breast-fed, but not as long and not exclusively, as postulated by WHO.
Our study confirmed that infants who are fed according to WHO recommendations have higher weight and length during the first 2 to 3 months of age than infants fed by other modes. Thereafter, they tend to be shorter and lighter, but the differences between feeding groups were small and clinically not relevant. At 24 months of age, the 219 children who had been fed according to WHO recommendations during infancy had lower length and weight (each by 0.12 z-scores) than the 1110 children who were not fed according to WHO recommendations. A difference of 0.12 z-scores corresponds to differences in length of approximately 3 mm and a difference in weight of 150 g (17). These differences were smaller than the usual measurement errors for length (6 mm) and weight (239 g) at that age (10). At 30 and 36 months of age, differences in z-scores were somehow larger, but the sample size of the children who were fed according to the WHO recommendations was already below 200 children, the target size for making comparisons.
It has been reported that infants who are fed according to the WHO recommendations are leaner at 1 year of age than formula-fed infants (10,24). The references for weight for length, which are influenced by age (19,24), and skinfold thickness (24) were used to demonstrate greater leanness. Using the z-score of BMI, which is not influenced by age (19), we observed only small and clinically unimportant differences after 3 months of age between the group who was fed according to WHO recommendations and the control group.
Of specific interest is the group that was fully breast fed to at least 4 to 5 months of age but who had solids introduced before 4 months of age. In comparison with the infants who were fed according to WHO recommendations, these infants tended to have greater length but lower body weight, which resulted in lower BMI between 1 and 36 months of age. Differences in mean BMI z-score as large as 0.3 to 0.5 from 3 to 6 months of age indicated that early introduction of solids was associated with greater leanness. It has been shown that infants fed solids at 4 to 5 months of age weigh less before 4 months than infants fed solids at 6 months of age or later (10). Low weight for age and leanness may prompt parents to introduce solids earlier. Further studies in breast-fed infants are necessary to examine weight gain, length gain, and breast-feeding practices immediately before and after the introduction of solids.
Using multiple regression analysis, we found a significantly negative correlation between duration of breast-feeding and gain in length and weight, and change in BMI until 24 months of age. However, the influence of breast-feeding was small and clinically unimportant. The influence of mid-parental height on increments in length and weight was much stronger and persisted until 36 months of age. The Euro-Growth Study had already confirmed that mid-parental height was a strong indicator for the genetic growth potential of the entire study cohort (13,17,18). Two studies (10,12) compared infants who were breast fed for at least 9 to 12 months of age with infants who were breast fed for 6 to 8 months of age. Longer duration of breast-feeding was associated with lower z-scores for weight, length, and weight for length at 12 months of age (10,12). Our regression model now indicates that the effect of full breast-feeding on growth is transient, in that it was no longer detectable after 24 months of age. Late introduction of solids was associated with higher weight gain and higher BMI only until 12 months of age. Therefore, the time of introduction of solids had only a transient influence on growth, which is no longer visible at 24 and 36 months of age.
Among the concerns that were raised regarding the adequacy of the NCHS-WHO references (14,15) were the distribution of birth weights, predominance of formula-fed babies, short duration of breast-feeding, and the early introduction of solids (10,11,21,22). The present study indicates that between birth and 6 months of age, the mean and SD z-scores for weight of the NCHS-WHO references were markedly lower than the mean and SD z-scores of infants who were fed according to WHO recommendations. Differences in birth-weight distribution between the two cohorts of infants were evident but can only partly explain the large differences in weight until 6 months of age. The -2 z-score value for weight of the NCHS-WHO references, which is often used as a cutoff value, is therefore problematic. Use of that value would classify many breast-fed infants as normal when their weight actually falls below the appropriate -2 SD value for breast-fed infants.
Our study confirmed earlier reports (10–12) showing that during the first 4 to 6 months of life breast-fed infants have higher mean weight and lower weight variance than the NCHS-WHO references. Previous studies (10–12) indicated that mean z-scores for weight of 453 breast-fed infants declined between 6 and 12 months and decreased well below the mean z-score of the NCHS-WHO references. The mean z-score for weight of the breast-fed infants was approximately 0.5 z-scores below the references between 9 and 12 months of age. No influence of the time of introduction of solids was found (10). Our study did not confirm this observation, because the mean z-score of the breast-fed infants between 9 and 12 months of age almost corresponded to the mean of the NCHS-WHO reference.
The mean and SD of the Euro-Growth references for length and weight between birth and 36 months of age (17) deviate substantially from the respective NCHS-WHO references. Among the infants in the Euro-Growth cohort, 38% were breast fed beyond 4 months of age and 36% received solids after 4 months of age. It is therefore not surprising that differences in mean z-scores for length and weight between infants fed according to the WHO feeding recommendations (WHO group) and the Euro-Growth reference were small. The mean difference in length at 9 months of age was 0.23 z-scores, which corresponded to 5 mm. The difference was in the same order of magnitude as the usual measurement error for length (6 mm) (10), and the maximum error that was introduced by the smoothing procedures used in construction of the Euro-Growth references for length (2.5 mm) (16,17). The variances for length and weight of the children who were fed according to WHO recommendations and the Euro-Growth reference (17) were similar. This indicates that the breast-fed group was not more homogeneous than the overall Euro-Growth cohort was. This characteristic is crucial to the definition of growth references because it determines the placement of z-scores, percentile lines, and statistically defined cutoff values.
The Euro-Growth references (17–19) can be used to monitor growth of breast-fed infants and children if the limitations of the weight reference during the first 2 months of life are understood. The additional Euro-Growth references for breast-fed boys and girls that are presented in this report are based on data from children who were fed according to the WHO recommendations and who lived in environments that favored achievement of the genetic potential for growth. WHO is committed to collecting data for a new international reference, and criteria for data suitable for the development of that reference have been published (22,25). The data of the Euro-Growth Study could contribute to this new reference, because the criteria set for anthropometric data were followed, and all demographic parameters are available (e.g., whether the mother smokes). Comparison with data that are now collected in seven geographical sites around the world (25) will help to decide whether one growth reference can be representative of the world's children who are fed according to health recommendations and whose mothers did not smoke during pregnancy nor plan to smoke during lactation.
EURO-GROWTH STUDY GROUP
Austria (A): C. Male, A. Golser, C. Huemer, B. Pietschnig
Croatia (HR): I. Svel, G. Armano
France (F): J. Schmitz, J. L. Muns, J. Beley, B. Digeon, J. Panis, G. Degy
Germany (D): F. Manz, E. Jekov, M. Radke
Greece (G): T. Zachou, S. Egglezou, J. Sofatzis
Hungary (H): E. Barko, S. Darvay
Italy (I): M. Salerno
Ireland (IRL): V. Freeman, H. Hoey, M. Gibney
Portugal (P): N. Teixeira Santos, A. Guerra, C. Rego, D. Silva
Spain (E): M. Hernandes, J. Molina, C. Ruiz, R. Tojo, E. Sanches, I. Rica, J. Argmeni, J. Rivera, C. Garcia-Caballero, M. Monleon, M. Manrique
Sweden (S): L. Persson, M. Lundstrom
United Kingdom (GB): J. Durnin, J. Reilly, S. Savage
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