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Low energy intakes and growth velocities of breast-fed infants: Are there functional consequences?

Abstract
1. Introduction
2. Methods

2.1. Study design
2.2. Anthropometry
2.3. Morbidity
2.4. Energy intake
2.5. Activity
2.6. Data analysis

3. Results
4. Conclusions
Acknowledgements
References
Discussion (summarized by A.M. Prentice)

K.G. DEWEY, M.J. HEINIG, L.A. NOMMSEN and B. LONNERDAL *

* Department of Nutrition, University of California, Davis, CA 95616, U.S.A.

Abstract

Data from the DARLING (Davis Area Research on Lactation, Infant Nutrition and Growth) study were analyzed to determine whether the slower growth velocity of breast-fed infants should be considered 'growth faltering' or is a normal outcome even under optimal conditions. Anthropometry was completed monthly for 46 infants who were breast-fed for at least 12 months. Energy intake was calculated from 4-day records of breast-milk and food intake at 3, 6, 9 and 12 months. Morbidity was recorded weekly. Activity level was assessed at 9 months by a 7-day sleep record and three 30-minute observations of spontaneous activity while awake. At 3, 6, 9 and 12 months, gross energy intake averaged 569, 642, 738 and 844 kcal, or 91, 84, 87 and 92 kcal/kg, respectively. There was no relationship between energy intake at any time point and morbidity during the subsequent 3-month period, nor between intake and activity level or time sleeping at 9 months. Similarly, infants with slow growth velocity (below the 5th percentile) during each quarter were just as healthy and active in the subsequent quarter as those with more rapid growth. Preliminary data from a matched group of formula-fed infants show the expected differences: higher energy intake and growth velocity, but no advantage in activity or risk of illness. These results indicate that relatively low energy intakes and growth velocities among breast-fed infants are normal patterns with no apparent deleterious consequences in this population.

1. Introduction

It has been documented that growth patterns of breast-fed infants differ from those of formula-fed infants, upon whom most reference data are based (WHITEHEAD and PAUL, 1981). The slower growth velocity of breast-fed infants after the first 2-3 months has been called 'growth faltering' by some, but it might just as easily be claimed that the growth pattern of formula-fed infants represents 'excessive' growth. The problem is not just a semantic issue, however, as evaluation of the health status of individual infants as well as groups of children requires an appropriate standard. Historically, we have relied on growth measures as a reflection of nutritional adequacy, but most would agree that bigger is not necessarily better. What is needed, therefore, are alternative indices of functional outcomes to judge whether a particular pattern of growth is optimal in a given environment.

The major objective of the DARLING study was to assess growth and nutrient intake of breast-fed and formula-fed infants during the first 18 months of life, and to include several functional indices, such as morbidity and activity levels, which are then examined in relation to intake and growth patterns. This paper presents an overview of the results pertaining to the breast-fed cohort during the first 15 months. A more detailed description of methods and results will be published elsewhere.

2. Methods

2.1. Study design
2.2. Anthropometry
2.3. Morbidity
2.4. Energy intake
2.5. Activity
2.6. Data analysis

2.1. Study design

The study was designed to follow prospectively 40-50 infants who were breast-fed for at least 12 months. This means that breast milk was the sole source of milk, but other foods were introduced by parental choice sometime after 4 months of age. Recruitment of a comparison group of formula-fed infants, matching the breast-fed cohort, was begun in 1988. The sample population for both groups was predominantly white, middle-to-upper income, highly educated women living in the Davis, California area.

We recruited a total of 92 women who intended to breast-feed for at least 12 months, of whom 73, 60, 51 and 46 remained in the study at 3, 6, 9 and 23 months, respectively. Those who dropped out did so for primarily two reasons, either because the infant stopped breast-feeding, or the study procedures were no longer convenient, for instance because of changes in schedules or maternal illness.

2.2. Anthropometry

Home visits were conducted once a month to measure both infant and mother and record infant feeding patterns. Infant anthropometry included weight, length, arm and crown-rump lengths, head, arm, leg and chest circumferences, and triceps, biceps, subscapular, flank and quadriceps skinfolds.

2.3. Morbidity

All mothers were contacted once a week to record all symptoms of illness of the infant and mother. The nature and duration of symptoms and any diagnoses made by physicians were noted. Morbidity data were subsequently coded and grouped into four major categories: respiratory (coded as ill if any upper or lower respiratory symptoms other than a clear nasal discharge were present), diarrhea (defined as two or more runny stools per day that differed from the child's usual stools), otitis media (diagnosed by a physician, with duration defined on the basis of symptoms of fever or continued discomfort), and 'other' (unexplained fevers, vomiting, chicken pox, and other non-respiratory, presumed viral infections). For the present analysis, the total number of days ill with any illness, and by each category of illness, was calculated in 3-month intervals: 0-3, 3-6, 6-9, 9-12 and 12-15 months. Incidence was calculated as the number of episodes per 100 days at risk and is also presented as the crude rate of episodes in each 3-month interval for convenience.

2.4. Energy intake

Infant intake was assessed at 3, 6, 9, 12, 15 and 18 months by having mothers complete a 4-day weighed record of all foods and fluids. Breast-milk intake was determined by test-weighing, using a Sartorius 3826 (Brinkmann, Westbury, NY) electronic balance, accurate to the nearest gram and programmed to average 40 consecutive weights, using an infant swing seat suspended from below for older infants. All subjects were instructed to choose a 'typical' 4-day period for the test-weighing record, i.e., days when the infant was not on an extended trip away from home and had no overt symptoms of illness.

Because there is a systematic error from test-weighing due to insensible water loss (IWL) during feedings, we corrected breast-milk intake by estimating IWL for each infant. First, an adjustment factor was determined by measuring IWL directly during both summer and winter months in a subsample of infants. From a total of 342 measurements of 37 infants, an average loss of 0.05 g/kg/min was calculated, which was relatively constant from 3 to 12 months. This factor was then multiplied by each infant's weight (in kilos) and by the total time of nursing (in minutes) determined for each infant from the 4-day test-weighing record, and the product (total IWL during feedings, in grams) was added to the breast-milk intake measured by test-weighing.

Samples of human milk representative of a 24-hour period were collected from each mother after the 4-day test-weighing period, using the alternate breast-expression method (BUTTE et al., 1984). Milk was analyzed for protein by a modified Lowry technique (PETERSON, 1977), fat by the modified Folch extraction procedures (FOLCH et al., 1957; FERRIS and JENSEN, 1984), and lactose by the method described by DAHLQUIST (1964). Gross energy content was calculated from values for protein, fat and lactose using the factors of 5.65, 9.25 and 3.95 kcal/g, respectively (GARZA et al., 1985). Gross energy intake of infants was calculated by multiplying the gross energy density of their mothers' milk by the corrected breast-milk intake, and adding energy from other foods using the factors of 9.4 kcal/g for fat, 5.65 kcal/g for protein, and 4.15 kcal/g for carbohydrate (PIKE and BROWN, 1984).

2.5. Activity

At 9 and 18 months of age, infant activity level was assessed in two ways: (1) by having the mother record all time that her infant spent sleeping on seven consecutive days, and (2) by observation of each infant for 30 minutes on three separate days. The 7-day record was used to obtain an overall picture of time awake vs time asleep, while the second method was chosen to reflect spontaneous activity level of infants while awake. The latter procedure was adapted from an activity assessment method for preschool children developed by KLESGES et al. (1984). A trained assistant went to the home at a time when the infant was healthy, rested and recently fed to observe it for 30 minutes. Mothers were instructed not to hold or constrain the child more than necessary so that the infant's voluntary level of physical activity could be observed. After the infant became accustomed to the presence of the observer, recording was begun using a standardized form. During the 30-minute period, activity was observed for 10 seconds, then recorded for 10 seconds alternately for a total of 90 ratings each time. Activity was recorded by six categories of behavior (lying down, sitting supported, sitting unsupported, creeping, crawling and cruising/walking), each with three levels of movement, for a total of 18 subcategories. A score was calculated, based on time spent in each subcategory, and averaged over the three days of observation. Further details of this method and the scoring system utilized are available from the authors on request.

2.6. Data analysis

Data were analyzed using the Statistical Package for the Social Sciences (1983). Energy intake data for infants whose mothers had difficulty with either the test-weighing record or the milk sample collection procedure were excluded from analysis. Several methods were used to determine whether the outcome measures of morbidity and activity showed any relationship to prior energy intake or growth velocity. First, simple correlation analysis and inspection of scatterplots were used to examine whether any trends were evident, and if so, whether the relationships were linear or non-linear. Second, at each time point, infants were divided into groups with lower versus higher energy intake (divided at the median) and lower versus higher growth velocity (divided at the 5th percentile of recent data published by ROCHE et al. (1989)). Both parametric (Student's t-tests) and non-parametric (Mann-Whitney U-tests) methods were used to compare subsequent morbidity and activity of groups, as some of the dependent variables were highly skewed. Analysis of variance and multiple regression were then used to control for potentially confounding variables in the morbidity comparisons, such as season, time spent in day care, sex, and socioeconomic status. Because there were only two mothers in the breast-fed cohort who smoked, this variable could not be included in the analysis.

3. Results

Breast-milk intake, corrected for insensible water loss, averaged 813, 769, 637 and 445 g/d at 3, 6, 9 and 12 months, respectively, with the corresponding gross energy densities of milk being 70.2, 71.8, 74.2 and 73.7 kcal/100 9. Gross energy intakes, including both breast milk and other foods after 4 months of age, are shown in Table 1, with preliminary data for the formula-fed group shown for comparison. The percentage of energy intake contributed by breast milk averaged 100% at 3 months, 86% at 6 months, 65% at 9 months, and 39% at 12 months.

Table 1. Milk and energy intake of breast-fed (BF) and formula-fed (FF) infants

* preliminary data
^a p < 0.001
^b p < 0.05

Total energy intake of breast-fed infants increased steadily from 3 to 12 months, but was significantly lower than that of formula-fed infants at all time points, even though neither group started to consume solid foods until 4 months of age or later. When expressed as intake per kg, average values for breast-fed infants reached a nadir of 84.1 kcal/kg at 6 months, and were far below the current RDA (Food and Nutrition Board, 1989) of 108 kcal/kg from 1 to 6 months and 98 kcal/kg from 6 to 12 months, despite the fact that the latter values are for metabolizable energy intake, and our data are for gross energy intake. Intake per kg of breast-fed infants differed significantly from that of formula-fed infants at 3, 6 and 9 months.

Growth patterns of the breast-fed cohort also differ from current NCHS reference data, with high Z-scores for weight-forage initially, because of the high mean birthweight (3685 ±508 9), dropping off to Z (0 at 6-7 months and further declining to Z (-0.4 at 10-12 months (DEWEY et al., 1989). Length-for-age Z-scores show the same initial pattern but do not remain below the NCHS median after 8 months of age. The relative decline in weight-for-age is not merely an artifact of the high mean birthweight, as the same slope is observed when only the average birthweight infants are included in the plot (DEWEY et al., 1989). Preliminary data for the formula-fed group do not show the relative decline observed in the breast-fed cohort.

When presented as growth-velocity data, the difference between the breast-fed group and current reference data is even more apparent. Table 2 lists the number of breast-fed infants with velocities below the 5th percentile of recently published data from the Fels Longitudinal Study (ROCHE et al., 1989). The percentage of infants falling below this cut-off for weight gain ranged from 20% at 0-3 months to 52% at 9-12 months. Similar percentages were observed for length gain below the 5th percentile. Although expressing the data in this way is useful for comparative purposes, it should be recognized that the percentiles published are based on smoothed growth curves for each infant in the Fels data set. Because infant growth occurs in spurts, using actual increments rather than estimated increments would result in a wider distribution and hence more individuals falling below the Fels 5th percentile.

Table 2. Number of breast-fed infants with growth velocity < 5th percentile

Descriptive data on morbidity in the breast-fed cohort are shown in Table 3. Infants were ill an average of 7.5 days during the first trimester, and about 20 days per trimester from 6 to 15 months of age. The vast majority of illnesses were respiratory, with a very low prevalence of diarrhea! disease in this population. Preliminary data for the formula-fed group indicate that overall morbidity rates are similar to those observed in the breast-fed group.

Table 3. Morbidity data for breast-fed infants

Time sleeping at 9 months ranged from 9.8 to 14.8 hours, with an average of 12.0 ±1.0 for boys and 12.2 ±1.1 for girls. Activity scores ranged from 312 to 435, with an average of 384 ±27 for boys and 387 ±27 for girls. Preliminary data for the formula-fed group showed no differences in time sleeping or activity level when compared to the breast-fed group.

Regression analysis at each time point (3, 6, 9 and 12 months) showed no relationship between energy intake, either total intake or intake per kg, and total morbidity during the subsequent 3-month period, whether morbidity was expressed as total number of days ill (prevalence), incidence, or duration of episodes. Similarly, activity score and time sleeping were not related to energy intake or intake per kg at 9 months. When infants were divided into lower versus higher energy intake groups, again no differences were seen in morbidity or activity at any time point.

The same results were found when comparing morbidity and activity of infants with slow growth velocity: infants whose weight or length gain fell below the 5th percentile were not different in activity or subsequent morbidity from infants with higher growth velocities.

4. Conclusions

In conclusion we have shown that:

(a) Energy intake of breast-fed infants is far below current recommended levels throughout the first year of life, even in a population of well-nourished, high socioeconomic status families and with complementary feeding after 4-6 months. We have shown previously that these low intakes are due more to infant self-regulation of intake than to constraints on maternal breast-milk production (DEWEY and LÖNNERDAL, 1986). Furthermore, infants provided with solid foods tend to reduce their intake of breast milk initially, rather than increasing energy intake, indicating that they do not consume all of the energy made available to them (STUFF and NICHOLS, 1989; NOMMSEN et al., 1989).

(b) Growth velocity of breast-fed infants is also considerably lower than current reference data, even as late as 9-12 months of age when other foods provide the majority of the child's energy intake. However, differences in achieved growth by 12 months of age are apparent only for weight, not for length, indicating that, on the average, these infants are leaner but not shorter than the NCHS median.

(c) Morbidity, time sleeping, and activity are unrelated to low energy intake or slow growth velocity in our cohort of breast-fed infants. In other words, infants with low intakes and slow growth were just as healthy and active as infants with higher intakes and more rapid growth. Thus, the deviation of breast-fed infants from current recommendations for energy intake and growth can be considered a normal pattern with no apparent deleterious consequences in our population. Further research is necessary to establish guidelines for identifying truly inadequate intakes and growth faltering among breast-fed infants in different environments.

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