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ORIGINAL RESEARCH COMMUNICATION |
1 From the Program in International Nutrition, University of California, Davis, CA (MMI, KJMP, KGD, and KHB), and the International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR, B), Dhaka, Bangladesh (MMI and TA)
2 Supported by grant no. 1 D43 TW01267 from the Fogarty International Center, National Institutes of Health; the Bill and Melinda Gates–Government of Bangladesh Fund of the ICDDR, B, Dhaka, Bangladesh; and the Jastro-Shields Graduate Research Scholarship Award, University of California, Davis, CA (to MMI).
3 Reprints not available. Address correspondence to KH Brown, Program in International Nutrition, University of California, Davis, Davis, CA 95616. E-mail: khbrown{at}ucdavis.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: We evaluated the effects of varied energy density of CFs on the time until stabilization of dietary intakes and on total daily energy intakes (EIs) and breast-milk intakes.
Design: CFs with low [0.4 kcal/g (LD)] and high [1.5 kcal/g (HD)] energy density were fed 3 times/d to 10 children (aged 9–18 mo) during 2 randomly assigned sequences of three 8-d diet periods (HD-LD-HD or LD-HD-LD) along with ad libitum breastfeeding. CF and breast-milk intakes were measured.
Results: Intakes of the HD diet and breast milk did not vary by day of period, but intake of the LD diet increased progressively. During days 5–7 of the last 2 diet periods in each sequence, more of the LD than of the HD diet was consumed (752 ± 252 and 439 ± 111 g/d, respectively; P < 0.001), but EIs from CFs were greater with the HD diet. Breast-milk consumption was slightly less (192 ± 115 and 234 ± 121 g/d, respectively; P = 0.03) but total daily EI was greater (774 ± 175 and 441 ± 85 kcal/d, respectively; P < 0.001) during the HD than during the LD diet period.
Conclusions: New information on the effects of newly introduced diets on daily intakes of these diets and of breast milk can be used to design future studies. Total daily EIs were greater with the HD diet despite its negative effects on breast-milk intakes.
Key Words: Infant feeding • complementary food • energy density • breast milk • breastfeeding
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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3–15 mo) in low-income countries commonly have growth faltering in relation to international reference patterns (1). The primary explanations for slower growth during this period include insufficient or inappropriate dietary intakes and frequent infections. Infants 
6 mo old require complementary foods of appropriate energy and nutrient densities in addition to breast milk to meet their physiologic needs (2). The relatively high energy requirements of young children, together with their limited gastric capacity, make it difficult for them to eat enough food, particularly if only a few meals per day are offered or if the foods have low energy density, or both (2–4). Quantitative studies of energy intake (EI) by weanlings in low-income countries (5–10) have shown that older infants and young children often consume substantially less than the recommended amounts (11). Possible explanations for the lower EIs observed among children in these settings include 1) their smaller body size—and hence their lower energy requirements—that results from preexisting growth retardation, 2) impaired appetite resulting from infections or nutrient imbalances, 3) limited household availability of food, 4) insufficient frequency of feeding, and 5) inadequate energy density of the diet (12).
Previous clinical studies examined the effects of different frequencies of feeding and meal composition on total daily EIs by fully weaned children who were recovering from malnutrition (2). However, because these studies were conducted in nonbreastfed children, the results may not be applicable to those who are still breastfeeding. In particular, because high intakes of complementary food may suppress the child's desire to nurse at the breast, it is necessary to consider the potentially adverse effects of frequent meals or high-energy-density (HD) foods, or both, on breast-milk intakes. This, in turn, may diminish the overall quality of the diet with respect to some nutrients and may increase the infant's exposure to food-borne pathogens. Thus, to develop appropriate feeding recommendations for healthy breastfed children, further studies are required to assess the independent effects of feeding frequency and of the dietary energy density of complementary foods on EIs both from these foods and from the consumption of breast milk.
To assist with the planning of such studies, additional information is needed to ascertain the number of days that are required for intakes of breast milk and food to stabilize after the introduction of HD foods into the diet of children who have been receiving a diet with low energy density and vice versa. The current (preliminary) study was therefore designed to collect information on the effects of varying dietary energy density on intakes of breast milk and on the number of days needed until the intakes of breast milk and food approach equilibrium after manipulations of the diet. We hypothesized 1) that EIs from complementary foods would be positively related to their energy density and frequency of feeding, as was observed in previous studies of nonbreastfed children (2), and 2) that the amount of breast milk consumed by healthy children would decrease when they are offered an HD diet after a period of consumption of a low-energy-density (LD) diet and vice versa. We assumed that intakes would stabilize within 1 wk of introduction of each of the dietary changes.
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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6 times/d and receiving other foods at home were recruited from a neighboring community. Only children with weight-for-length and length-for-age z scores between –1.5 and 1.5 with respect to international reference data were eligible to participate, and all mothers were required to have a body mass index (in kg/m2) > 18.5. Children who were bottle-feeding or who had symptomatic illnesses were excluded from the study. Written informed consent was obtained from the mother of each child. The research protocol was approved by the institutional review boards of the University of California, Davis, and ICDDR, B.
Study protocol
The children and their mothers were admitted to the research ward for a total of 27 d of study. During an initial 3-d period of adaptation to the study ward, the children were provided 3 times a day with a diet containing 1.0 kcal/g. They were then randomly assigned to 1 of 2 possible sets of 3 sequential dietary periods in which the energy densities were changed every ninth day. Half of the children received an LD diet (0.4 kcal/g) during the first 8-d study period (period 1), an HD diet (1.5 kcal/g) during the second study period (period 2), and the same LD diet during the third study period (period 3). The other group of children received the same diets in the reverse sequence (ie, HD-LD-HD) during the respective study periods. During all study periods, the complementary foods were offered 3 times a day at fixed intervals (from 0900 to 1000, from 1500 to 1600, and from 2100 to 2200) along with ad libitum breastfeeding. On the last day of each dietary period (days 3, 11, 19, and 27), breast milk was collected by using the alternate-breast expression method (13). However, because of some breaks in the milk collection protocol, the resulting pooled samples were not truly representative of the total daily milk production, and so those results are not presented. A schematic diagram of the feeding protocol is shown in Figure 1
. Plans were developed to discontinue the feeding protocol in case of intervening acute infections, but none of the children developed symptoms of illness during the course of the study.
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Study diets and feeding protocols
Semisolid purees were prepared from rice powder, rice starch (CalNatural StarchPlus; California Natural Products, Lathrop, CA), milk powder, and soybean oil. Amylase (Validase; Valley Research, South Bend, IN), Sucralose (Splenda; McNeil Nutritionals, McIntosh, AL), chocolate powder, and vanilla were added to the 2 study diets to ensure that their organoleptic characteristics were as similar as possible (Table 1). Adult volunteers who participated in preliminary taste trials did not detect any differences in the diets' general appearance, color, consistency, or sweetness, although they did identify minor differences in flavor and mouthfeel.
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The mothers were encouraged to breastfeed day and night, according to their usual feeding practices at home before the study, except that they were requested not to breastfeed during the hour before each of the scheduled complementary feeds. During each nursing episode, breast milk was offered until the child refused further intake, and the amounts consumed were measured by weighing the infant before and after feeds by using an electronic balance sensitive to 1.0 g (Sartorius 3826MP8, 1A48; Sartorius, Gottingen, Germany). The duration of each breastfeeding episode was also measured. Milk intakes were corrected for insensible losses by using published values (15), and the energy density of the milk was assumed to be 0.6 kcal/g (16).
Study outcomes, sample size estimates, and statistical analysis
The major outcomes of the study were the number of days required for the intakes of breast milk and each of the study diets to stabilize, the amounts of the diets and breast milk that were consumed (g/d and g · kg body wt–1 · d–1), EIs from each of these dietary sources (kcal · kg body wt–1 · d–1), and changes in body weight (BW) during each of the dietary periods. Only data from the second and third dietary periods were included in the analyses of the effect of dietary energy density on dietary intake. This permitted us to examine the effects of changing from an HD diet of known composition to an LD diet and vice versa.
The statistical power of the available sample size was estimated by using data collected previously during single-day dietary studies in rural Bangladesh, which indicated that children aged 9–12 mo who were nursing 6 times/d consumed 396 ± 109 g breast-milk/d (17), and information from infants observed on multiple occasions in studies in Peru from 1982 to 1984 and in Guatemala from 1997 to 1999 (KH Brown, unpublished observations, 1982–1984 and 1977–1999), which suggested that within-child variations accounted for 70% of the total SDs. With the use of these sets of information, we estimated that a sample size of 10 children (the maximum number the budget would allow) would be sufficient to detect a within-child difference of 135 g in the amount of breast milk consumed by diet period (
< 0.05; power (1–ß) = 0.80).
Statistical analyses were carried out with the use of SAS for WINDOWS software (release 8; SAS Inc, Cary, NC). Outcome variables were assessed for homogeneity of variance and conformance to the normal distribution and were transformed if appropriate. All comparisons were made by using an analysis of variance model that included dietary energy density (HD or LD), day of diet period (from day 1 to day 7), the number of the diet period (period 2 or 3), a random individual effect, and all 2-way interactions among fixed effects. Nonsignificant interactions were removed in a stepwise, hierarchical manner. To explore the relation between BW and dietary intakes, we repeated these analyses with the inclusion of a main effect for BW (above or below the median) and all interactions by nesting a random subject effect within each BW category.
The number of days required for the intakes of each of the diets to approach a plateau was estimated as follows. If the diet x day interaction was significant, analysis was done separately within each diet; otherwise, diets were combined. If the effect of the day of the diet period was not significant, we concluded that there was no evidence of adjustment, or adaptation, of intake after introduction of the new diet. Otherwise, a series of separate t tests were carried out to estimate on which day the intakes differed significantly from the subsequent intakes; specifically, we compared the mean intakes on day 6 with those on day 7, and then we compared the mean intakes on day 5 with those on days 6 and 7, and so on until a significant difference was found. Daily means were also compared by using Tukey's test.
To compare the outcome variables by dietary energy density, data from period 2 for children in dietary sequence HD-LD-HD and from period 3 for those in sequence LD-HD-LD were pooled as the LD diet, and data from period 3 for children in sequence HD-LD-HD and from period 2 for those in sequence LD-HD-LD were pooled as the HD diet. This strategy allowed us to compare the effect of introducing the HD diet to children who had been receiving the LD diet immediately beforehand, and vice versa. The mean intakes were compared by dietary energy density for days 5–7 only, because these were the days on which intakes of the LD diet were significantly greater than the intakes on previous days, according to the analyses described above.
Because the observed mean intakes of breast milk during dietary periods 2 and 3 were less than those reported from the earlier community-based studies in Bangladesh, we also compared the intakes of breast milk and complementary foods during these periods with those during the initial adaptation period and with diet-specific mean intakes during days 5–7 of periods 1 and 3, evaluated separately for the children in the 2 diet sequences.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Their mean age was nearly 12 mo. All children had reportedly been breastfeeding 6 times/d and had been receiving complementary foods at home. The children's mean length-for-age and weight-for-length z scores were less than the reference population medians, but all values were within the normal range, as per the study entry criteria.
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. The diet x day interaction was significant (P = 0.004), so the mean daily intakes were compared separately for each diet by using Tukey's test. The differences between days for the HD diet period were not significant (P = 0.39). By contrast, complementary food intakes increased progressively during the LD diet period (P < 0.0001). Day 4 was the first day that was significantly different from the mean of the subsequent days, so intakes on days 5–7 were used for subsequent comparisons.
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. The diet x day interactions were not significant, so the results of the 2 diets were pooled. Analysis of the combined data indicated that the differences by the day of the diet period were not significant (P = 0.153). Thus, breast-milk intakes remained stable within each period of exposure to the different dietary energy densities, although there were energy density–related differences in intakes when the diet periods were compared, as described below.
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). The children consumed a significantly (P < 0.001) greater amount of the LD diet but ingested significantly (P < 0.001) more energy from complementary foods when the HD diet was provided. The differences between the amounts of time spent consuming the respective diets were not significant (P = 0.54), which indicated that the children consumed the LD diet more rapidly (g/min) than the HD diet (P < 0.001). It is interesting that the interaction between the children's BW category (above or below the median weight of 8.3 kg) and diet with regard to food intake was significant (P = 0.003). Specifically, the heavier children consumed significantly more of the LD diet than did the lighter children (
intakes: 843 and 660 g/d, respectively; P < 0.001), but the intakes of the HD diet did not differ significantly by weight category ( intakes: 448 and 441 g/d, respectively; P = 0.98). Notably, the within-diet comparisons by weight category were no longer statistically significant when intakes were expressed per kg BW. Thus, it appears that, because of their larger body size (and, hence, greater gastric capacity), the heavier children may have been able to consume more of the LD diet than were the lighter children.
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intakes: 281 and 208 g/d, respectively; P = 0.04), whereas the breast-milk intakes did not differ significantly by diet period in the heavier children ( intakes: 188 and 176 g/d during the LD and HD diet periods, respectively; P = 0.97). Despite their lower breast-milk intakes during the HD diet periods, the children's total daily EIs were significantly (P < 0.001) greater when they received the HD diet than when they received the LD diet.
The children's mean BWs by day of diet period, after adjustment for the study period (study period 2 or 3), are shown in Figure 4. The diet x day interaction was significant (P < 0.001), so the differences in BW were compared separately for each level of dietary energy density. The children's mean BWs increased progressively during the HD diet period. In contrast, the change in BW during the LD diet period was not significant.
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To further explore this latter possibility, dietary intakes and other study outcomes during periods 1 and 3 were compared separately for the children in the 2 diet sequences (ie, HD-LD-HD and LD-HD-LD), as shown in Table 4. Complementary food intakes increased from period 1 to period 3 in children who received the LD diet during these periods, but not in those who received the HD diet. Notably, breast-milk intake, breastfeeding frequency, and total amount of time nursing were slightly less in period 3 than in period 1, regardless of the diet sequence.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Because the mean amounts of consumption of the LD diet continued to increase, albeit not significantly, even after day 5 (Figure 2
), we cannot state unequivocally that the children reached a stable level of intake. Longer studies would be required to know definitively how much time may be needed for the intakes to become truly constant, but the desirability of any added degree of certainty would have to be balanced against the greater cost and subject burden imposed by longer studies. It seems that a delay of 4 d after the introduction of a new diet would be sufficient in most cases to permit comparisons of the effects of dietary factors on young children's EIs. In contrast with the intakes of the LD diet, intakes of the HD diet remained stable after the first exposure to the diet. Notably, during days 5–7 after the introduction of the new diets, the children consumed greater amounts of the LD diet than of the HD diet, although EIs were greater with the HD preparations than with the LD preparations, as was seen previously among nonbreastfed children (12).
The current study was conducted under carefully controlled conditions in a research ward, where it was possible to prepare well-defined, masked diets and to measure precisely the children's intakes of food and breast milk around the clock. The mothers were requested to feed the children according to a specific protocol and to nurse them according to their usual pattern at home. Because other characteristics of the diet, such as sweetness and viscosity, could confound measurement of food intakes in relation to their energy density (18, 19), we attempted to control those aspects of the diet as much as possible. To a panel of adult volunteers, the final fed preparations were indistinguishable in general appearance, color, consistency, and sweetness. Although the volunteers did detect minor differences in the flavor and mouthfeel of the diets, those dietary characteristics would not have been discerned by the parents who fed the children or the nursing aides who supervised the procedures, because they were not permitted to sample the diets. Thus, it is unlikely that those differences would have exerted an important independent effect on the feeding behaviors or the children's intakes.
One of the objectives of the study was to ascertain whether increases in the energy density of complementary foods would have an adverse effect on breast-milk consumption. Breast-milk intake was slightly less with the HD diet than with the LD diet, a difference that was associated with simultaneous decreases in the number of breastfeeding episodes and the amount of time spent nursing. Equally important, perhaps, was the observation that breast-milk intakes decreased during the course of the study, presumably because the children or their mothers became more accustomed to having access to the unrestricted amounts of complementary foods that were provided. It is not certain whether these changes in breast-milk intake represent a modification of maternal breastfeeding behaviors or the children's response to decreased hunger. However, it seems more likely that the change in feeding patterns was primarily due to the children, because the mothers were advised to continue breastfeeding according to their usual home practices, and they were not aware of which diet was being fed during each period of the study. It is interesting that the effect of dietary density on breast-milk intake was significant only in children whose BWs were below the median. Thus, it is possible that the mothers of the smaller (and younger) children were able to increase their milk outputs in response to the presumably greater infant demand during the LD diet period, whereas mothers of the heavier (and older) children no longer had the same response capacity. Alternatively, it is possible that the heavier children were able to meet their energy needs with the LD diet, and thus they did not increase their sucking to the same extent as did the lighter children.
Because the decrease in breast-milk intakes that occurred with the introduction of the HD diet was accompanied by greater EIs from the complementary food and greater total daily EIs, it could be argued that this modification of the diet was beneficial for the children. However, it must be recognized that breast milk is the primary source of some nutrients, such as vitamin A, in the usual diets of these children, so reductions in breast-milk intake might jeopardize their status with regard to these specific nutrients (19). Moreover, reductions in breast-milk intakes may predispose infants to infectious diseases (20) and may hasten their mothers' return to fertility (21), although it is not known whether the small changes in breast-milk intakes that were observed would produce either of these effects. Nevertheless, it would seem to be desirable to protect maximal breast-milk intakes for as long as possible but also to continue providing adequate amounts of complementary foods of appropriate energy and nutrient densities to satisfy the children's theoretical requirements.
Estimates of young children's average energy requirements are available from longitudinal studies of energy expenditure and body composition in different age groups (22). With the use of this information, the minimum adequate energy density of complementary foods were calculated for children of different ages according to their specific frequency of feeding (23). However, these estimates assumed that breast-milk intakes remain constant regardless of the complementary feeding regimen, but that assumption no longer seems tenable. Thus, empirical data are needed from studies of a broad range of feeding frequencies and energy densities of complementary foods carried out in different age groups of children.
According to the results of the current study, it seems that an energy density of 0.4 kcal/g, if provided just 3 times a day (ie, a total of 686 kcal/d), would not be adequate to supply the average theoretical needs of breastfed infants aged 9 mo. This conclusion is consistent with the observation that the children did not gain weight during the diet periods when the LD diet was offered. It is perhaps surprising that these infants did not attempt to compensate for the lower EIs from complementary foods during the LD diet periods by increasing their breast-milk consumption. If the mothers were not able to respond to increased infant sucking with greater milk transfer (possibly because of their relatively late stage of lactation or because their mammary glands were already beginning the process of involution), it is conceivable that the infants may not have persisted in trying to extract more milk. A previous study suggested that, in later lactation, milk consumption begins to show changes consistent with glandular involution when milk volume falls below 300 g/d (24), which is somewhat more than the mean milk intakes of the infants in the current study during the LD and HD diet periods. Alternatively, the infants' inability to increase their milk intakes during the LD diet periods may have been due to their mothers' failure to respond behaviorally to the infants' increased demand or to a period of observation that was not long enough to allow detection of such changes.
In summary, the current results provide a basis for designing future studies of the effects of varying the energy density and frequency of feeding complementary foods on young children's total EIs and consumption of breast milk. Further study is now warranted to examine a broader range of energy densities and feeding frequencies to obtain the empirical information that will be needed to establish appropriate complementary feeding recommendations for young children and also to ensure minimum displacement of breast-milk consumption.
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ACKNOWLEDGMENTS |
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MMI, KGD, and KHB were responsible for the conceptualization and the design of the study. MMI and TA implemented the clinical procedures and supervised the data collection. JMP assisted with the data analysis and statistical modeling procedures. MMI and KHB drafted the manuscript, which was reviewed by all authors. None of the authors had any personal or financial conflicts of interest.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
, low-density diet: 0.4 kcal/g; •, high-density diet: 1.5 kcal/g) and day of dietary period. n = 10. The data were analyzed by using a 2-factor repeated-measures ANOVA. The diet x day interaction was statistically significant, P = 0.004. Within each dietary energy density level, days with different superscript letters were significantly different, P < 0.05 (Tukey's test).
