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Journal of the American College of Nutrition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uacn20
Energy requirements of breast-fed infants. a
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N F Butte , W W Wong , C Garza , J E Stuff , E O Smith , P D Klein & B L Nichols
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USDA/ARS Children's Nutrition Research Center, Houston, Texas 77030. Published online: 02 Sep 2013.
To cite this article: N F Butte, W W Wong, C Garza, J E Stuff, E O Smith, P D Klein & B L Nichols (1991) Energy requirements of breast-fed infants., Journal of the American College of Nutrition, 10:3, 190-195, DOI: 10.1080/07315724.1991.10718143 To link to this article: http://dx.doi.org/10.1080/07315724.1991.10718143
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Energy Requirements of Breast-Fed Infants Nancy F. Butte, PhD, William W. Wong, PhD, Cutberto Garza, MD, PhD, Janice E. Stuff, MS, E. 0'Brian Smith, PhD, Peter D. Klein, PhD, and Buford L. Nichols, MD USDAlARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, and Texas Children's Hospital, Houston Key words: energy requirements, infants, breast-feeding, growth rate Current recommendations for energy intake are reviewed in light of emerging data on energy intakes of breast-fed infants and on total daily energy expenditure of infants. For determination of energy requirements, the historical approach based on observed intakes of healthy infants is compared with a newly proposed approach based on energy expenditure and deposition. A data set of exclusively breast-fed infants is used to illustrate the circuity of either approach. Energy intake, expenditure, and stores must be evaluated in an assessment of dietary adequacy. Ultimately, energy requirements of infants should reflect growth rate, body composition, and level of physical activity conducive to optimal health and neurobehavioral development.
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Abbreviations: MOEE = minimal observable energy expenditure, NCHS = National Center for Health Statistics, SMR = sleeping meta bolic rate, TDEE = total daily energy expenditure
INTRODUCTION The energy requirements of infants reflect levels of energy intake that will promote health, adequate growth, optimal body composition, and levels of physical ac tivity appropriate for the developmental age of the child. It is the opinion of an FAO/WHO/UNU expert commit tee [1] that energy requirements should be based on es timates of energy expenditures, whether actual or desirable. To determine requirements from observed in takes is largely a circular argument, since actual intakes are not necessarily those that support optimal growth and development. It has not been possible to apply this prin ciple to infants, because sufficient data on energy expen diture were not available. Basal metabolism of infants has been studied extensively; however, the allowance for physical activity was indeterminate. Also, in young in fants the requirement for growth is a substantial com ponent of the total energy requirement. Uncertainties in the energy cost of growth persist. Therefore, scientific
committees have based energy requirements on observed energy intakes of "thriving" infants [1,2]. We shall review this historical approach and a newly proposed approach based on energy expenditure and deposition, using data from the Children's Nutrition Research Cen ter. Neither approach is exempt from underlying assump tions regarding the constituents of adequate growth and development. Ultimately, growth rates, body composi tion, and levels of physical activity should be tied to outcomes of health and neurobehavioral development. Until such information is available, however, recommen dations should be based on currently available data on energy intake, deposition, and expenditure, because all are interdependent.
CURRENT RECOMMENDED ENERGY ALLOWANCES DURING INFANCY The 1985 FAO/WHO/UNU [1] estimated energy re quirements were based on energy intakes compiled from
This work is a publication of the USDA/ARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children's Hospital, Houston. This project has been funded in part with federal funds from the U.S. Department of Agriculture, Agriculture Research Service, under Cooperative Agreement number 58-7MN1-6-I00. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government. Address reprint requests to Nancy F. Butte, Ph.D., USDA/ARS Children's Nutrition Research Center, 1100 Bates, Room 8068, Houston, Texas 77030.
Journal of the American College of Nutrition, Vol. 10, No. 3, 190-195 (1991) Not subject to copyright within the United States Published by John Wiley & Sons, Inc.
CCC 0731-5724/91/030190-06$04.00
Energy Requirements of Breast-Fed Infants Table 1. Human Milk and Energy Intakes of Exclusively Breast-Fed Infants Age (months) 1 (n = 64)
2 (n = 40)
3 (n = 37)
4 (n=lll)
5 (n = 26)
6 (n = 8)
Human milk (g/day) (g/kg/day)
738 (158)a 157 (24)
725 (131) 129 (19)
723 (114) 117 (20)
755 (124) 113 (18)
741 (175) 103 (23)
818 (166) 107 (21)
Energy intake (kcal/day) (kcal/kg/day)
499 (129) 106 (21)
468 (115) 83 (19)
458 (124) 74 (20)
483 72
500 (135) 69 (17)
542 71
(98) (14)
(94) (12)
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"Mean (SD).
Table 2. Growth of Exclusively Breast-Fed Infants Age (months)
Weight (kg)
1 (n = 64)
2 (n = 40)
4.7 (0.5)a
5.6 (0.7)
4 ( n = 111)
5 (n = 26)
6 (n = 8)
6.3 (0.3)
6.7 (0.8)
7.1 (1.0)
7.7 (1.0)
3 (n = 37)
Length (cm)
55.5 (2.1)
59.0 (2.6)
61.8 (2.4)
63.2 (1.3)
64.4 (1.7)
65.6 (1.7)
Weight gain (g/day) (g/kg/day)
36 (12) 10 (4)
32 (14) 7 (3)
22 4
18 3
17 2
11 2
69 (23)
73 (22)
70 (22)
66 (24)
66 (29)
63 (32)
61 (28)
62 (29)
63 (26)
59 (25)
56 (22)
42 (17)
62 (23)
62 (26)
57 (23)
56 (26)
59 (26)
59 (32)
Weight-for-age pctb Length-for-age pct
b
Weight-for-length pct
b
(8) (1)
(7) (1)
(6) (1)
(4) (1)
"Mean (SD). b NCHS percentiles [16].
studies conducted in Canada, Sweden, the United Kingdom, and the United States [3]. The infants were fed human milk, formula, and/or solids. Energy requirements were set at 116, 99,96, and 100 kcal/kg/day at 0-3, 3-6, 6-9, and 9-12 months of age. Estimates were set 5% above observed intakes to correct for any underestima tion of intake. This pattern of intake seemed consistent with rapid growth early and increased physical activity later in infancy. The NRC/NAS committee [2] for recommended dietary allowances elected to adopt the 1985 FAO/WHO/UNU energy requirements for infants. These figures, 108 kcal/kg/day from birth through 6 months of age and 98 kcal/kg/day from 6 through 12 months of age, are 6-7% less than previous recommen dations.
Although the FAO/WHO/UNU and NRC/NAS com mittees did not adopt the breast-fed infant as the con struct upon which to base energy requirements, the appropriateness of such a reference standard could be argued. It is generally accepted that a well-nourished lactating women is capable of producing enough milk to provide sole support of the nutrient needs of her infant for 4-6 months of age [4,5]. The intake of the recipient infant, who is fed truly on demand, is driven by hunger, and is less susceptible to external influence. Reported intakes of infants fed formula and supplements, however, have shown secular trends over the past decades which reflected changes in the formulation of milk substitutes and infant feeding practices [3]. If nutrient recommenda tions for infants are to be derived from nutrient intakes
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Energy Requirements
of Breast-Fed
Infants
of breast-fed infants, differences in nutrient availability and utilization between human milk and formula must be accounted for.
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OBSERVED ENERGY INTAKES OF EXCLUSIVELY BREAST-FED INFANTS Energy intakes of exclusively breast-fed infants have been compiled from a series of studies conducted at the Children's Nutrition Research Center in Houston (Table 1), and these findings are inconsistent with current recommendations. In our first study, 45 infants were fol lowed longitudinally for 4 months [6]. Two cross-sec tional studies were conducted when infants were 1 (n = 17, 10) and 4 months (n = 15, 10) of age [7,8]. In a longitudinal study, we followed 45 infants through the transitional period from exclusive breast-feeding to mixed feeding [9]. Human milk intakes were measured by test weighing for 1 to 5 days, depending on the study design. The energy content of human milk was analyzed by bomb calorimetry on representative 24-hr samples. Human milk intakes averaged 750 g/day over the first 6 months of exclusive breast-feeding (Table 1). Gross energy intakes decreased over the first 3 months of life and plateaued thereafter at approximately 72 kcal/kg/day. The energy intake of exclusively breast-fed infants has been documented in a number of studies [1015]. Although the intakes of human milk in these studies were similar to those in our study, the techniques used to estimate the energy content of human milk differed: both milk sampling and analytical methods differed among investigations. The stated mean energy content of human milk ranged from 0.64 to 0.75 kcal/g. Consequently, the range of energy intakes reported in the literature is greater than that reported for human milk intakes. Never theless, all studies indicated that observed energy intakes of exclusively breast-fed infants after the first month of life are less than current energy intake recommendations.
GROWTH OF EXCLUSIVELY BREAST-FED INFANTS The absolute weights and lengths and corresponding National Center for Health Statistics (NCHS) percentiles of the infants [16] are summarized in Table 2. The weight-for-age and length-for-age percentiles increased initially and then declined gradually. The weight-forlength percentiles decreased slightly after the second month. The growth pattern of infants in this series of studies is in agreement with other reports in the litera ture. Ann and MacLean [17] observed deviations from
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NCHS standards at 3 months for boys and 5 months for girls. In a study from Cambridge, growth velocities ex ceeded expected rates initially, but after 4 months velocities decelerated relative to those of the NCHS standards; the resulting weights were slightly below the 50th percentile at 6 months [3]. Duncan et al [18] studied 33 exclusively breast-fed infants and found that, on the basis of the NCHS reference, weight-for-age percentiles dropped from 67 at birth to 47 at 6 months. In our series of infants, length-for-age percentiles decreased slightly from 61 at birth to 56-42 at 5-6 months; sample size at 6 months was too small to con firm a definite trend. Similar deviations from expected NCHS length-for-age percentiles were reported for ex clusively breast-fed infants during the first 6 months of life [3,17,18]. The interpretation of this deviation in the growth of breast-fed infants from NCHS growth standards is con troversial. The contention that human milk is inadequate is countered by the argument that the NCHS growth standards are inappropriate for the evaluation of the growth performance of breast-fed infants [19]. The NCHS standards were compiled between 1929 and 1972 from cross-sectional measurements of infants who were predominantly fed artificial formulations. Since that time, growth rates (as well as skinfold thicknesses) of formula-fed infants have been falling, whereas those of breast-fed infants have remained virtually constant [20]. This secular change is probably due to modifications in infant formulas and changing attitudes toward the early introduction of solid foods.
ENERGY INTAKES AND GROWTH OF SUPPLEMENTED BREAST-FED INFANTS If human milk were inadequate to sustain infant growth for 4-6 months, ad libitum addition of solid foods to the diet of exclusively breast-fed infants would be expected to increase energy intakes and reverse the decline in weight-for-age percentiles observed during the exclusive breast-feeding period. A study was designed precisely to ascertain the effect of supplementation on energy intake [9]. Forty-five infants were studied through the transitional period of exclusive breast-feed ing to mixed feeding. Weekly or biweekly measurements of weight and length were made from 0 to 36 weeks, and monthly measurements of human milk and supplements were made from 16 weeks until 10 weeks after sup plemental foods were added. The timing of supplementa tion was determined at the discretion of the parents and the child's pediatrician. After the introduction of solids,
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Energy Requirements of Breast-Fed Infants Table 3. Growth of Supplemented Breast-Fed Infants [9] Age (months)
Weight (kg) Length (cm) Weight-for-age pct Length-for-age pct
b
b
Weight-for-length pct
b
8 (n = 23)
9 (n = 9)
8.0 (0.8)
8.3 (1.0)
8.6 (0.9)
67.0 (2.0)
67.9 (2.4)
68.9 (2.5)
69.9 (2.2)
66 (20)
60 (25)
57 (28)
51 (29)
53 (28)
66 (25)
60 (24)
54 (26)
46 (28)
44 (25)
52 (33)
46 (29)
53 (27)
53 (26)
53 (29)
5 (n = 19)
6 (n = 37)
7.2 (0.6)a
7.6 (0.8)
65.5 (2.0)
7 (n = 41)
"Mean (SD). NCHSpercentiles[16]. c Note. Mean birth weight = 70th percentile: length at 1 week = 55th percentile.
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b
Table 4. Energy Intake, Energy Expenditure, and Growth of Breast-Fed and Formula-Fed Infants Breast-fed infants
Formula-fed infants
1 month (n = 27)
4 months (n = 25)
1 month (n = 27)
4 months (n = 26)
Energy intake (kcal/kg/day)
99.9 (I6.6)a
73.2 (11.1)
111.7 (18.0)
95.2 (11.9)
SMR (kcal/kg/day)b
51.5
(4.1)
50.0
(6.0)
53.7
(5.5)
52.3
(4.4)
MOEE (kcal/kg/day)
45.2
(3.9)
44.1
(4.9)
48.0
(4.9)
47.1
(4.4)
Weight gain (g/day)
35.3 (10.7)
16.1
(7.7)
36.9 (12.7)
22.4
(7.9)
2.5
(1.2)
3.5
(1.2)
c
Weight gain (g/kg/day)
8.2
(2.5)
8.6
(2.9)
"Mean (SD). b SMR = sleeping metabolic rate. c MOEE = minimal observable energy expenditure.
the number of nursings per day and the intake of human milk decreased significantly. Human milk intakes averaged 703 (156), 621 (188), 594 (180), 560 (247), and 565 (164) g/day for months 5-9 postpartum, respec tively. No change in energy intake, on a body weight basis, was noted in the transition from exclusive human milk to mixed feeding. Mean energy intakes were 70 (14), 70 (16), 73 (15), 69 (20), and 69 (19) kcal/kg/day during months 5-9. The deviation from NCHS growth standards observed during exclusive breast-feeding was not reversed with supplementation (Table 3). When compared with NCHS percentiles at 28 weeks, weight was 13 centiles lower than that at birth and length was 1 centile lower than that at week 1. Weight and length values at 28 weeks, when
compared with peak values at 8 weeks, had dropped 19 and 14 centiles, respectively. During the period of mixed feeding, energy intakes remained approximately 20% below NRC/NAS recom mendations. After the introduction of solid foods, the percentage of total energy intake provided by human milk was 88% at 5 months, 76% at 6 months, 70% at 7 months, 65% at 8 months, and 68% at 9 months. Ade quate infant growth and development have been among the criteria used by the NRC/NAS to estimate energy requirements. The distinct growth pattern of the ex clusively breast-fed infant persisted throughout the tran sitional period of mixed feeding: The decline in NCHS weight-for-age and length-for-age percentiles continued for 10 weeks after supplements were added to the diet.
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Energy Requirements of Breast-Fed Infants As with the period of exclusive breast-feeding, the constituents of normal growth and the consequences of deviations in growth should be evaluated in terms of infant health and development. Although rigorous mor bidity data were not collected in our series of studies, maternal recall revealed only minor illnesses. Although developmental assessments were not performed on these infants, we have begun to measure the energy expendi ture and physical activity of infants to evaluate the func tional consequence of energy intake.
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ENERGY EXPENDITURE OF BREAST-FED INFANTS Energy expenditure of breast-fed infants during the period of exclusive breast-feeding was measured [7,8]. Study designs included cohorts of formula-fed infants, because their energy intakes reportedly approached NRC/NAS recommendations [21]. Energy intakes, growth, body composition, sleeping metabolic rate, and total daily energy expenditure were investigated at 1 and 4 months of age. The combined results from these two studies indi cated that the energy intakes of the breast-fed infants were significantly lower than those of the formula-fed infants at 1 and 4 months of age, although the difference was greater at 4 months (22 kcal/kg/day) than at 1 month (12 kcal/kg/day) (Table 4). At the time of the study, there were no significant differences in attained length or weight between the breast-fed and formula-fed infants. Combined analysis indicated that weight gain (g/day) was higher among the formula-fed infants, particularly at 4 months. No defini tive differences in skinfold thicknesses were seen be tween feeding groups. Because of the low sensitivity of these anthropométrie measurements, subtle differences in body composition between feeding groups may not have been detectable. Total body water, estimated by deuterium and oxygen-18 dilution spaces, however, did not differ between the breast-fed and formula-fed in fants. Thus, our evidence up to 4 months of age indicates that infants on higher energy intakes were getting larger, not fatter. A determination of the optimal pattern of growth requires study of the functional consequences of different rates of weight gain. Using indirect calorimetry, we have measured two proxies of basal metabolism: sleeping metabolic rate (SMR) and minimal observable energy expenditure (MOEE). SMR was defined as the mean energy expendi ture of sleeping infants observed either 2-3 or 3-4 hr postprandially. The minimal 5-min interval observed during the SMR was identified and designated as
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MOEE. Combined results (Table 4) indicated a sig nificant difference in SMR between breast-fed and for mula-fed infants. SMR did not differ between feeding groups in our first study [7]. In the second study, how ever, SMR was 5 and 12% higher at 1 and 4 months, respectively, among the formula-fed compared with the breast-fed infants [8]. MOEE was consistently higher among the formula-fed infants. In the second study, total daily energy expenditure (TDEE) was estimated by the doubly labeled water tech nique [8]. TDEE, in absolute terms or relative to body weight, was significantly higher among the formula-fed infants compared with the breast-fed infants. The mean TDEE was 64 kcal/kg/day for the 1- and 4-month-old breast-fed infants, and 67 and 73 kcal/kg/day for the 1and 4-month-old formula-fed infants, respectively. Using the factorial approach, the energy available for activity is estimated as TDEE minus SMR. By this ap proach, the energy available for activity was equal to approximately 13 kcal/kg/day (20% TDEE) at 1 month and approximately 18 kcalylcg/day (25% TDEE) at 4 months, and did not differ between feeding groups. This approach may not be appropriate in infant studies, be cause it cannot be assumed that SMR represents a con stant metabolic baseline throughout the day. Under the conditions of measurement, SMR may be influenced by fluctuations in biosynthesis and sympathetic activity, residual thermic effect of feeding, and spontaneous ac tivity during sleep. In addition, an energy available for activity value does not indicate the specific activities in which an infant has been engaged. High energy expendi tures are not necessarily advantageous or desirable. We do know, however, that reductions in basal meta bolism and activity levels occur with severe malnutri tion. Assurance that diet does not limit an infant's ability to interact and explore the environment is of paramount importance. Although SMR was somewhat responsive to energy intake in our studies, the lower levels were not as low as those reported for malnourished infants. Our measurements of the energy available for activity do not suggest that the breast-fed infant is less active than the formula-fed infant, but these quantitative findings must be related to qualitative observations on infant behavior and activity.
ENERGY REQUIREMENTS BASED ON ENERGY EXPENDITURE AND DEPOSITION On the basis of the emerging body of data on the TDEE of infants, the dietary guidelines for energy may warrant revision, as proposed by Prentice et al [22]. Al-
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Energy Requirements of Breast-Fed Infants though this approach has merits and advantages over the historical approach based on energy intakes, energy ex penditure is influenced, among other factors, by nutri tional status, growth rate, body composition, and energy intake. Establishing energy requirements on the basis of energy expenditure is circular because eriergy intake af fects expenditure. Nevertheless, Prentice et al [22] derived the following new estimates of energy require ments by combining TDEE with energy deposition: 110, 95, 85, 83, and 83 kcal/kg/day at 1, 3, 6, 9, and 12 months. Applying this approach to our data, the energy requirements of the formula-fed infants would be 105 and 87 kcal/kg/day at 1 and 4 months, respectively. The energy requirements of the breast-fed infants would be 102 and 72 kcal/kg/day at 1 and 4 months, respectively. On the basis of observed energy intakes and the emerging body of data on TDEE of infants, current recommendations for the energy intake of infants are probably too high; however, the level to which they should be lowered has not been completely resolved. Further research is needed to reconcile the discrepancy in "apparent" energy requirements of breast-fed and for mula-fed infants. In the assessment of dietary adequacy, energy intake, expenditure, and stores must be evaluated since all are interdependent. Ultimately, energy require ments should reflect growth rates, body composition, and levels of physical activity conducive to optimal health and neurobehavioral development.
REFERENCES 1. FAO/WHO/UNU Expert Consultation: "Energy and protein requirements." World Health Organization Techni cal Report Series 724. Geneva: WHO, 1985. 2. Subcommittee on the Tenth Edition of the Recommended Dietary Allowances, Food and Nutrition Board: "Recom mended Dietary Allowances." Washington, DC: National Academy of Sciences, 1989. 3. Whitehead RG, Paul AA: Infant growth and human milk requirements: a fresh approach. Lancet 2:161-163, 1981. 4. American Academy of Pediatrics, Committee on Nutri tion: Commentary on breast-feeding and infant formulas, including proposed standards for formulas. Pediatrics 57:278-285,1976. 5. American Academy of Pediatrics, Committee on Nutri tion: On the feeding of supplemental foods to infants. Pediatrics 65:1178-1181, 1980. 6. Butte N, Garza C, Smith EO, Nichols BL: Human milk intake and growth in exclusively breast-fed infants. J Pediatr 104:187-195, 1984.
7. Butte NF, Smith EO, Garza C: Energy utilization of human milk-fed and formula-fed infants. Am J Clin Nutr 51:350-358,1990. 8. Butte N, Wong W, Garza C, Ferlic L, Smith EO, Klein PD, Garza C: Energy expenditure and deposition of breast-fed and formula-fed infants during early infancy. Pediatrics 28:631-640, 1990. 9. Stuff JE, Nichols BL: Nutrient intake and growth perfor mance of older breast-fed infants. J Pediatr 115:959-968, 1989. 10. Wallgren A: Breast milk consumption of healthy, full-term infants. Acta Paediatr Scand 32:778-790, 1945. 11. Whitehead RG, Paul AA: Growth and nutritional ade quacy in the human infant. In Filer LG, Fomon SD (eds): "The Breast-Fed Infant: A Model for Performance." Columbus, OH: Ross Laboratories, pp 60-67, 1986. 12. Hofvander Y, Hagman U, Hillervik C, Sjolin S: The amount of milk consumed by 1-3 months old breast- or bottle-fed infants. Acta Paediatr Scand 71:953-958, 1982. 13. Dewey KG, Lonnerdal B: Milk and nutrient intake of breast-fed infants from 1 to 6 months: relation to growth and fatness. J Pediatr Gastroenterol Nutr 2:497-506,1983. 14. Köhler L, Meeumisse G, Mortensson W: Food intake and growth of infants between six and twenty-six weeks of age on breast milk, cow's milk formula, or soy formula. Acta Paediatr Scand 73:40-48, 1984. 15. Wood CS, Isaacs PC, Jensen M, Hilton HG: Exclusively breast-fed infants: growth and caloric intake. Pediatr Nurs ing 14:117-124, 1988. 16. National Center for Health Statistics: "NCHS Growth Cur ves for Children: Birth-18 Years," DHEW Publication No (PHS)78-1650. Washington, DC: DHEW, 1977. 17. Ahn CH, MacLean WC: Growth of the exclusively breast fed infant. Am J Clin Nutr 33:183-192, 1980. 18. Duncan B, Schaefer C, Sibley B, Fonseca NM: Reduced growth velocity in exclusively breast-fed infants. Am J Dis Child 138:309-313, 1984. 19. Whitehead RG, Paul AA: Growth charts and the assess ment of infant feeding practices in the western world and in developing countries. Early Hum Dev 9:187-207,1984. 20. Whitehead RG, Paul AA: Human lactation, infant feeding and growth: secular trends. In Gracey M, Falkner F (eds): "Nutritio.ial Needs and Assessment of Normal Growth: Nestle Nutrition." New York, Raven, pp 85-122, 1985. 21. Butte NF, Garza C: Energy and protein intakes of ex clusively breast-fed infants during the first four months of life. In Gracey M, Falkner F (eds): "Nutritional Needs and Assessment of Normal Growth: Nestle Nutrition." New York: Raven, pp 63-84,1985. 22. Prentice AM, Lucas A, Vasquez-Velasquez L, Davies PSW, Whitehead RG: Are current dietary guidelines for young children a prescription for overfeeding? Lancet 2:1066-1069, 1988. Received October J 989 ; revision acceptedApril J 990.
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Journal of the American College of Nutrition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uacn20
Energy requirements of breast-fed infants. a
a
a
a
a
a
N F Butte , W W Wong , C Garza , J E Stuff , E O Smith , P D Klein & B L Nichols
a
a
USDA/ARS Children's Nutrition Research Center, Houston, Texas 77030. Published online: 02 Sep 2013.
To cite this article: N F Butte, W W Wong, C Garza, J E Stuff, E O Smith, P D Klein & B L Nichols (1991) Energy requirements of breast-fed infants., Journal of the American College of Nutrition, 10:3, 190-195, DOI: 10.1080/07315724.1991.10718143 To link to this article: http://dx.doi.org/10.1080/07315724.1991.10718143
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Energy Requirements of Breast-Fed Infants Nancy F. Butte, PhD, William W. Wong, PhD, Cutberto Garza, MD, PhD, Janice E. Stuff, MS, E. 0'Brian Smith, PhD, Peter D. Klein, PhD, and Buford L. Nichols, MD USDAlARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, and Texas Children's Hospital, Houston Key words: energy requirements, infants, breast-feeding, growth rate Current recommendations for energy intake are reviewed in light of emerging data on energy intakes of breast-fed infants and on total daily energy expenditure of infants. For determination of energy requirements, the historical approach based on observed intakes of healthy infants is compared with a newly proposed approach based on energy expenditure and deposition. A data set of exclusively breast-fed infants is used to illustrate the circuity of either approach. Energy intake, expenditure, and stores must be evaluated in an assessment of dietary adequacy. Ultimately, energy requirements of infants should reflect growth rate, body composition, and level of physical activity conducive to optimal health and neurobehavioral development.
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Abbreviations: MOEE = minimal observable energy expenditure, NCHS = National Center for Health Statistics, SMR = sleeping meta bolic rate, TDEE = total daily energy expenditure
INTRODUCTION The energy requirements of infants reflect levels of energy intake that will promote health, adequate growth, optimal body composition, and levels of physical ac tivity appropriate for the developmental age of the child. It is the opinion of an FAO/WHO/UNU expert commit tee [1] that energy requirements should be based on es timates of energy expenditures, whether actual or desirable. To determine requirements from observed in takes is largely a circular argument, since actual intakes are not necessarily those that support optimal growth and development. It has not been possible to apply this prin ciple to infants, because sufficient data on energy expen diture were not available. Basal metabolism of infants has been studied extensively; however, the allowance for physical activity was indeterminate. Also, in young in fants the requirement for growth is a substantial com ponent of the total energy requirement. Uncertainties in the energy cost of growth persist. Therefore, scientific
committees have based energy requirements on observed energy intakes of "thriving" infants [1,2]. We shall review this historical approach and a newly proposed approach based on energy expenditure and deposition, using data from the Children's Nutrition Research Cen ter. Neither approach is exempt from underlying assump tions regarding the constituents of adequate growth and development. Ultimately, growth rates, body composi tion, and levels of physical activity should be tied to outcomes of health and neurobehavioral development. Until such information is available, however, recommen dations should be based on currently available data on energy intake, deposition, and expenditure, because all are interdependent.
CURRENT RECOMMENDED ENERGY ALLOWANCES DURING INFANCY The 1985 FAO/WHO/UNU [1] estimated energy re quirements were based on energy intakes compiled from
This work is a publication of the USDA/ARS Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children's Hospital, Houston. This project has been funded in part with federal funds from the U.S. Department of Agriculture, Agriculture Research Service, under Cooperative Agreement number 58-7MN1-6-I00. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government. Address reprint requests to Nancy F. Butte, Ph.D., USDA/ARS Children's Nutrition Research Center, 1100 Bates, Room 8068, Houston, Texas 77030.
Journal of the American College of Nutrition, Vol. 10, No. 3, 190-195 (1991) Not subject to copyright within the United States Published by John Wiley & Sons, Inc.
CCC 0731-5724/91/030190-06$04.00
Energy Requirements of Breast-Fed Infants Table 1. Human Milk and Energy Intakes of Exclusively Breast-Fed Infants Age (months) 1 (n = 64)
2 (n = 40)
3 (n = 37)
4 (n=lll)
5 (n = 26)
6 (n = 8)
Human milk (g/day) (g/kg/day)
738 (158)a 157 (24)
725 (131) 129 (19)
723 (114) 117 (20)
755 (124) 113 (18)
741 (175) 103 (23)
818 (166) 107 (21)
Energy intake (kcal/day) (kcal/kg/day)
499 (129) 106 (21)
468 (115) 83 (19)
458 (124) 74 (20)
483 72
500 (135) 69 (17)
542 71
(98) (14)
(94) (12)
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"Mean (SD).
Table 2. Growth of Exclusively Breast-Fed Infants Age (months)
Weight (kg)
1 (n = 64)
2 (n = 40)
4.7 (0.5)a
5.6 (0.7)
4 ( n = 111)
5 (n = 26)
6 (n = 8)
6.3 (0.3)
6.7 (0.8)
7.1 (1.0)
7.7 (1.0)
3 (n = 37)
Length (cm)
55.5 (2.1)
59.0 (2.6)
61.8 (2.4)
63.2 (1.3)
64.4 (1.7)
65.6 (1.7)
Weight gain (g/day) (g/kg/day)
36 (12) 10 (4)
32 (14) 7 (3)
22 4
18 3
17 2
11 2
69 (23)
73 (22)
70 (22)
66 (24)
66 (29)
63 (32)
61 (28)
62 (29)
63 (26)
59 (25)
56 (22)
42 (17)
62 (23)
62 (26)
57 (23)
56 (26)
59 (26)
59 (32)
Weight-for-age pctb Length-for-age pct
b
Weight-for-length pct
b
(8) (1)
(7) (1)
(6) (1)
(4) (1)
"Mean (SD). b NCHS percentiles [16].
studies conducted in Canada, Sweden, the United Kingdom, and the United States [3]. The infants were fed human milk, formula, and/or solids. Energy requirements were set at 116, 99,96, and 100 kcal/kg/day at 0-3, 3-6, 6-9, and 9-12 months of age. Estimates were set 5% above observed intakes to correct for any underestima tion of intake. This pattern of intake seemed consistent with rapid growth early and increased physical activity later in infancy. The NRC/NAS committee [2] for recommended dietary allowances elected to adopt the 1985 FAO/WHO/UNU energy requirements for infants. These figures, 108 kcal/kg/day from birth through 6 months of age and 98 kcal/kg/day from 6 through 12 months of age, are 6-7% less than previous recommen dations.
Although the FAO/WHO/UNU and NRC/NAS com mittees did not adopt the breast-fed infant as the con struct upon which to base energy requirements, the appropriateness of such a reference standard could be argued. It is generally accepted that a well-nourished lactating women is capable of producing enough milk to provide sole support of the nutrient needs of her infant for 4-6 months of age [4,5]. The intake of the recipient infant, who is fed truly on demand, is driven by hunger, and is less susceptible to external influence. Reported intakes of infants fed formula and supplements, however, have shown secular trends over the past decades which reflected changes in the formulation of milk substitutes and infant feeding practices [3]. If nutrient recommenda tions for infants are to be derived from nutrient intakes
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Energy Requirements
of Breast-Fed
Infants
of breast-fed infants, differences in nutrient availability and utilization between human milk and formula must be accounted for.
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OBSERVED ENERGY INTAKES OF EXCLUSIVELY BREAST-FED INFANTS Energy intakes of exclusively breast-fed infants have been compiled from a series of studies conducted at the Children's Nutrition Research Center in Houston (Table 1), and these findings are inconsistent with current recommendations. In our first study, 45 infants were fol lowed longitudinally for 4 months [6]. Two cross-sec tional studies were conducted when infants were 1 (n = 17, 10) and 4 months (n = 15, 10) of age [7,8]. In a longitudinal study, we followed 45 infants through the transitional period from exclusive breast-feeding to mixed feeding [9]. Human milk intakes were measured by test weighing for 1 to 5 days, depending on the study design. The energy content of human milk was analyzed by bomb calorimetry on representative 24-hr samples. Human milk intakes averaged 750 g/day over the first 6 months of exclusive breast-feeding (Table 1). Gross energy intakes decreased over the first 3 months of life and plateaued thereafter at approximately 72 kcal/kg/day. The energy intake of exclusively breast-fed infants has been documented in a number of studies [1015]. Although the intakes of human milk in these studies were similar to those in our study, the techniques used to estimate the energy content of human milk differed: both milk sampling and analytical methods differed among investigations. The stated mean energy content of human milk ranged from 0.64 to 0.75 kcal/g. Consequently, the range of energy intakes reported in the literature is greater than that reported for human milk intakes. Never theless, all studies indicated that observed energy intakes of exclusively breast-fed infants after the first month of life are less than current energy intake recommendations.
GROWTH OF EXCLUSIVELY BREAST-FED INFANTS The absolute weights and lengths and corresponding National Center for Health Statistics (NCHS) percentiles of the infants [16] are summarized in Table 2. The weight-for-age and length-for-age percentiles increased initially and then declined gradually. The weight-forlength percentiles decreased slightly after the second month. The growth pattern of infants in this series of studies is in agreement with other reports in the litera ture. Ann and MacLean [17] observed deviations from
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NCHS standards at 3 months for boys and 5 months for girls. In a study from Cambridge, growth velocities ex ceeded expected rates initially, but after 4 months velocities decelerated relative to those of the NCHS standards; the resulting weights were slightly below the 50th percentile at 6 months [3]. Duncan et al [18] studied 33 exclusively breast-fed infants and found that, on the basis of the NCHS reference, weight-for-age percentiles dropped from 67 at birth to 47 at 6 months. In our series of infants, length-for-age percentiles decreased slightly from 61 at birth to 56-42 at 5-6 months; sample size at 6 months was too small to con firm a definite trend. Similar deviations from expected NCHS length-for-age percentiles were reported for ex clusively breast-fed infants during the first 6 months of life [3,17,18]. The interpretation of this deviation in the growth of breast-fed infants from NCHS growth standards is con troversial. The contention that human milk is inadequate is countered by the argument that the NCHS growth standards are inappropriate for the evaluation of the growth performance of breast-fed infants [19]. The NCHS standards were compiled between 1929 and 1972 from cross-sectional measurements of infants who were predominantly fed artificial formulations. Since that time, growth rates (as well as skinfold thicknesses) of formula-fed infants have been falling, whereas those of breast-fed infants have remained virtually constant [20]. This secular change is probably due to modifications in infant formulas and changing attitudes toward the early introduction of solid foods.
ENERGY INTAKES AND GROWTH OF SUPPLEMENTED BREAST-FED INFANTS If human milk were inadequate to sustain infant growth for 4-6 months, ad libitum addition of solid foods to the diet of exclusively breast-fed infants would be expected to increase energy intakes and reverse the decline in weight-for-age percentiles observed during the exclusive breast-feeding period. A study was designed precisely to ascertain the effect of supplementation on energy intake [9]. Forty-five infants were studied through the transitional period of exclusive breast-feed ing to mixed feeding. Weekly or biweekly measurements of weight and length were made from 0 to 36 weeks, and monthly measurements of human milk and supplements were made from 16 weeks until 10 weeks after sup plemental foods were added. The timing of supplementa tion was determined at the discretion of the parents and the child's pediatrician. After the introduction of solids,
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Energy Requirements of Breast-Fed Infants Table 3. Growth of Supplemented Breast-Fed Infants [9] Age (months)
Weight (kg) Length (cm) Weight-for-age pct Length-for-age pct
b
b
Weight-for-length pct
b
8 (n = 23)
9 (n = 9)
8.0 (0.8)
8.3 (1.0)
8.6 (0.9)
67.0 (2.0)
67.9 (2.4)
68.9 (2.5)
69.9 (2.2)
66 (20)
60 (25)
57 (28)
51 (29)
53 (28)
66 (25)
60 (24)
54 (26)
46 (28)
44 (25)
52 (33)
46 (29)
53 (27)
53 (26)
53 (29)
5 (n = 19)
6 (n = 37)
7.2 (0.6)a
7.6 (0.8)
65.5 (2.0)
7 (n = 41)
"Mean (SD). NCHSpercentiles[16]. c Note. Mean birth weight = 70th percentile: length at 1 week = 55th percentile.
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b
Table 4. Energy Intake, Energy Expenditure, and Growth of Breast-Fed and Formula-Fed Infants Breast-fed infants
Formula-fed infants
1 month (n = 27)
4 months (n = 25)
1 month (n = 27)
4 months (n = 26)
Energy intake (kcal/kg/day)
99.9 (I6.6)a
73.2 (11.1)
111.7 (18.0)
95.2 (11.9)
SMR (kcal/kg/day)b
51.5
(4.1)
50.0
(6.0)
53.7
(5.5)
52.3
(4.4)
MOEE (kcal/kg/day)
45.2
(3.9)
44.1
(4.9)
48.0
(4.9)
47.1
(4.4)
Weight gain (g/day)
35.3 (10.7)
16.1
(7.7)
36.9 (12.7)
22.4
(7.9)
2.5
(1.2)
3.5
(1.2)
c
Weight gain (g/kg/day)
8.2
(2.5)
8.6
(2.9)
"Mean (SD). b SMR = sleeping metabolic rate. c MOEE = minimal observable energy expenditure.
the number of nursings per day and the intake of human milk decreased significantly. Human milk intakes averaged 703 (156), 621 (188), 594 (180), 560 (247), and 565 (164) g/day for months 5-9 postpartum, respec tively. No change in energy intake, on a body weight basis, was noted in the transition from exclusive human milk to mixed feeding. Mean energy intakes were 70 (14), 70 (16), 73 (15), 69 (20), and 69 (19) kcal/kg/day during months 5-9. The deviation from NCHS growth standards observed during exclusive breast-feeding was not reversed with supplementation (Table 3). When compared with NCHS percentiles at 28 weeks, weight was 13 centiles lower than that at birth and length was 1 centile lower than that at week 1. Weight and length values at 28 weeks, when
compared with peak values at 8 weeks, had dropped 19 and 14 centiles, respectively. During the period of mixed feeding, energy intakes remained approximately 20% below NRC/NAS recom mendations. After the introduction of solid foods, the percentage of total energy intake provided by human milk was 88% at 5 months, 76% at 6 months, 70% at 7 months, 65% at 8 months, and 68% at 9 months. Ade quate infant growth and development have been among the criteria used by the NRC/NAS to estimate energy requirements. The distinct growth pattern of the ex clusively breast-fed infant persisted throughout the tran sitional period of mixed feeding: The decline in NCHS weight-for-age and length-for-age percentiles continued for 10 weeks after supplements were added to the diet.
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Energy Requirements of Breast-Fed Infants As with the period of exclusive breast-feeding, the constituents of normal growth and the consequences of deviations in growth should be evaluated in terms of infant health and development. Although rigorous mor bidity data were not collected in our series of studies, maternal recall revealed only minor illnesses. Although developmental assessments were not performed on these infants, we have begun to measure the energy expendi ture and physical activity of infants to evaluate the func tional consequence of energy intake.
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ENERGY EXPENDITURE OF BREAST-FED INFANTS Energy expenditure of breast-fed infants during the period of exclusive breast-feeding was measured [7,8]. Study designs included cohorts of formula-fed infants, because their energy intakes reportedly approached NRC/NAS recommendations [21]. Energy intakes, growth, body composition, sleeping metabolic rate, and total daily energy expenditure were investigated at 1 and 4 months of age. The combined results from these two studies indi cated that the energy intakes of the breast-fed infants were significantly lower than those of the formula-fed infants at 1 and 4 months of age, although the difference was greater at 4 months (22 kcal/kg/day) than at 1 month (12 kcal/kg/day) (Table 4). At the time of the study, there were no significant differences in attained length or weight between the breast-fed and formula-fed infants. Combined analysis indicated that weight gain (g/day) was higher among the formula-fed infants, particularly at 4 months. No defini tive differences in skinfold thicknesses were seen be tween feeding groups. Because of the low sensitivity of these anthropométrie measurements, subtle differences in body composition between feeding groups may not have been detectable. Total body water, estimated by deuterium and oxygen-18 dilution spaces, however, did not differ between the breast-fed and formula-fed in fants. Thus, our evidence up to 4 months of age indicates that infants on higher energy intakes were getting larger, not fatter. A determination of the optimal pattern of growth requires study of the functional consequences of different rates of weight gain. Using indirect calorimetry, we have measured two proxies of basal metabolism: sleeping metabolic rate (SMR) and minimal observable energy expenditure (MOEE). SMR was defined as the mean energy expendi ture of sleeping infants observed either 2-3 or 3-4 hr postprandially. The minimal 5-min interval observed during the SMR was identified and designated as
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MOEE. Combined results (Table 4) indicated a sig nificant difference in SMR between breast-fed and for mula-fed infants. SMR did not differ between feeding groups in our first study [7]. In the second study, how ever, SMR was 5 and 12% higher at 1 and 4 months, respectively, among the formula-fed compared with the breast-fed infants [8]. MOEE was consistently higher among the formula-fed infants. In the second study, total daily energy expenditure (TDEE) was estimated by the doubly labeled water tech nique [8]. TDEE, in absolute terms or relative to body weight, was significantly higher among the formula-fed infants compared with the breast-fed infants. The mean TDEE was 64 kcal/kg/day for the 1- and 4-month-old breast-fed infants, and 67 and 73 kcal/kg/day for the 1and 4-month-old formula-fed infants, respectively. Using the factorial approach, the energy available for activity is estimated as TDEE minus SMR. By this ap proach, the energy available for activity was equal to approximately 13 kcal/kg/day (20% TDEE) at 1 month and approximately 18 kcalylcg/day (25% TDEE) at 4 months, and did not differ between feeding groups. This approach may not be appropriate in infant studies, be cause it cannot be assumed that SMR represents a con stant metabolic baseline throughout the day. Under the conditions of measurement, SMR may be influenced by fluctuations in biosynthesis and sympathetic activity, residual thermic effect of feeding, and spontaneous ac tivity during sleep. In addition, an energy available for activity value does not indicate the specific activities in which an infant has been engaged. High energy expendi tures are not necessarily advantageous or desirable. We do know, however, that reductions in basal meta bolism and activity levels occur with severe malnutri tion. Assurance that diet does not limit an infant's ability to interact and explore the environment is of paramount importance. Although SMR was somewhat responsive to energy intake in our studies, the lower levels were not as low as those reported for malnourished infants. Our measurements of the energy available for activity do not suggest that the breast-fed infant is less active than the formula-fed infant, but these quantitative findings must be related to qualitative observations on infant behavior and activity.
ENERGY REQUIREMENTS BASED ON ENERGY EXPENDITURE AND DEPOSITION On the basis of the emerging body of data on the TDEE of infants, the dietary guidelines for energy may warrant revision, as proposed by Prentice et al [22]. Al-
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Energy Requirements of Breast-Fed Infants though this approach has merits and advantages over the historical approach based on energy intakes, energy ex penditure is influenced, among other factors, by nutri tional status, growth rate, body composition, and energy intake. Establishing energy requirements on the basis of energy expenditure is circular because eriergy intake af fects expenditure. Nevertheless, Prentice et al [22] derived the following new estimates of energy require ments by combining TDEE with energy deposition: 110, 95, 85, 83, and 83 kcal/kg/day at 1, 3, 6, 9, and 12 months. Applying this approach to our data, the energy requirements of the formula-fed infants would be 105 and 87 kcal/kg/day at 1 and 4 months, respectively. The energy requirements of the breast-fed infants would be 102 and 72 kcal/kg/day at 1 and 4 months, respectively. On the basis of observed energy intakes and the emerging body of data on TDEE of infants, current recommendations for the energy intake of infants are probably too high; however, the level to which they should be lowered has not been completely resolved. Further research is needed to reconcile the discrepancy in "apparent" energy requirements of breast-fed and for mula-fed infants. In the assessment of dietary adequacy, energy intake, expenditure, and stores must be evaluated since all are interdependent. Ultimately, energy require ments should reflect growth rates, body composition, and levels of physical activity conducive to optimal health and neurobehavioral development.
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7. Butte NF, Smith EO, Garza C: Energy utilization of human milk-fed and formula-fed infants. Am J Clin Nutr 51:350-358,1990. 8. Butte N, Wong W, Garza C, Ferlic L, Smith EO, Klein PD, Garza C: Energy expenditure and deposition of breast-fed and formula-fed infants during early infancy. Pediatrics 28:631-640, 1990. 9. Stuff JE, Nichols BL: Nutrient intake and growth perfor mance of older breast-fed infants. J Pediatr 115:959-968, 1989. 10. Wallgren A: Breast milk consumption of healthy, full-term infants. Acta Paediatr Scand 32:778-790, 1945. 11. Whitehead RG, Paul AA: Growth and nutritional ade quacy in the human infant. In Filer LG, Fomon SD (eds): "The Breast-Fed Infant: A Model for Performance." Columbus, OH: Ross Laboratories, pp 60-67, 1986. 12. Hofvander Y, Hagman U, Hillervik C, Sjolin S: The amount of milk consumed by 1-3 months old breast- or bottle-fed infants. Acta Paediatr Scand 71:953-958, 1982. 13. Dewey KG, Lonnerdal B: Milk and nutrient intake of breast-fed infants from 1 to 6 months: relation to growth and fatness. J Pediatr Gastroenterol Nutr 2:497-506,1983. 14. Köhler L, Meeumisse G, Mortensson W: Food intake and growth of infants between six and twenty-six weeks of age on breast milk, cow's milk formula, or soy formula. Acta Paediatr Scand 73:40-48, 1984. 15. Wood CS, Isaacs PC, Jensen M, Hilton HG: Exclusively breast-fed infants: growth and caloric intake. Pediatr Nurs ing 14:117-124, 1988. 16. National Center for Health Statistics: "NCHS Growth Cur ves for Children: Birth-18 Years," DHEW Publication No (PHS)78-1650. Washington, DC: DHEW, 1977. 17. Ahn CH, MacLean WC: Growth of the exclusively breast fed infant. Am J Clin Nutr 33:183-192, 1980. 18. Duncan B, Schaefer C, Sibley B, Fonseca NM: Reduced growth velocity in exclusively breast-fed infants. Am J Dis Child 138:309-313, 1984. 19. Whitehead RG, Paul AA: Growth charts and the assess ment of infant feeding practices in the western world and in developing countries. Early Hum Dev 9:187-207,1984. 20. Whitehead RG, Paul AA: Human lactation, infant feeding and growth: secular trends. In Gracey M, Falkner F (eds): "Nutritio.ial Needs and Assessment of Normal Growth: Nestle Nutrition." New York, Raven, pp 85-122, 1985. 21. Butte NF, Garza C: Energy and protein intakes of ex clusively breast-fed infants during the first four months of life. In Gracey M, Falkner F (eds): "Nutritional Needs and Assessment of Normal Growth: Nestle Nutrition." New York: Raven, pp 63-84,1985. 22. Prentice AM, Lucas A, Vasquez-Velasquez L, Davies PSW, Whitehead RG: Are current dietary guidelines for young children a prescription for overfeeding? Lancet 2:1066-1069, 1988. Received October J 989 ; revision acceptedApril J 990.
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