NUTRIENT ADEQUACY OF EXCLUSIVE BREASTFEEDING FOR THE TERM INFANT DURING THE FIRST SIX MONTHS OF LIFE DEPARTMENT OF NUTRITION FOR HEALTH AND DEVELOPMENT DEPARTMENT OF CHILD AND ADOLESCENT HEALTH AND DEVELOPMENT WORLD HEALTH ORGANIZATION The World Health Organization was established in 1948 as a specialized agency of the United Nations serving as the directing and coordinating authority for international health matters and public health. One of WHO’s constitutional functions is to provide objective and reliable information and advice in the field of human health, a responsibility that it fulfils in part through its extensive programme of publications. The Organization seeks through its publications to support national health strategies and address the most pressing public health concerns of populations around the world. 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To ensure the widest possible availability of authoritative information and guidance on health matters, WHO secures the broad international distribution of its publications and encourages their translation and adaptation. By helping to promote and protect health and prevent and control disease throughout the world, WHO’s books contribute to achieving the Organization’s principal objective — the attainment by all people of the highest possible level of health. NUTRIENT ADEQUACY OF EXCLUSIVE BREASTFEEDING FOR THE TERM INFANT DURING THE FIRST SIX MONTHS OF LIFE NANCY F. BUTTE, PHD USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA MARDIA G. LOPEZ-ALARCON, MD, PHD Nutrition Investigation Unit, Pediatric Hospital, CMN, Mexico City, Mexico CUTBERTO GARZA, MD, PHD Division of Nutritional Sciences, Cornell University, Ithaca, NY, USA GENEVA WORLD HEALTH ORGANIZATION 2002 WHO Library Cataloguing-in-Publication Data Butte, Nancy F. Nutrient adequacy of exclusive breastfeeding for the term infant during the first six months of life / Nancy F. Butte, Mardia G. Lopez-Alarcon, Cutberto Garza. 1.Breastfeeding2.Milk, Human – chemistry3.Nutritive value4.Nutritional requirements5.InfantI.Lopez-Alarcon, Mardia G. II.Garza, CutbertoIII.Expert Consultation on the Optimal Duration of Exclusive Breastfeeding (2001:Geneva, Switzerland) IV.Title. ISBN 92 4 156211 0 (NLM Classification: WS 125) © World Health Organization 2002 All rights reserved. Publications of the World Health Organization can be obtained from Marketing and Dissemination, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland (tel: +41 22 791 2476; fax: +41 22 791 4857; email: [email protected]). Requests for permission to reproduce or translate WHO publications – whether for sale or for non- commercial distribution – should be addressed to Publications, at the above address (fax: +41 22 791 4806; email: [email protected]). The designations employed and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines on maps represent approximate border lines for which there may not yet be full agreement. The mention of specific companies or of certain manufacturers’ products does not imply that they are endorsed or recommended by the World Health Organization in preference to others of a similar nature that are not mentioned. Errors and omissions excepted, the names of proprietary products are distinguished by initial capital letters. The World Health Organization does not warrant that the information contained in this publication is complete and correct and shall not be liable for any damages incurred as a result of its use. The named authors alone are responsible for the views expressed in this publication. Designed by minimum graphics Printed in France REFERENCES Contents Abbreviations & acronyms v Foreword vii Executive summary 1 1. Conceptual framework 3 1.1 Introduction 3 1.2 Using ad libitum intakes to assess adequate nutrient levels 3 1.3 Factorial approaches 4 1.4 Balance methods 5 1.5 Other issues 6 1.5.1 Morbidity patterns 6 1.5.2 Non-continuous growth 6 1.5.3 Estimating the proportion of a group at risk for specific nutrient deficiencies 6 1.5.4 Summary 7 2. Human-milk intake during exclusive breastfeeding in the first year of life 8 2.1 Human-milk intakes 8 2.2 Nutrient intakes of exclusively breastfed infants 8 2.3 Duration of exclusive breastfeeding 8 2.4 Summary 14 3. Energy and specific nutrients 15 3.1 Energy 15 3.1.1 Energy content of human milk 15 3.1.2 Estimates of energy requirements 15 3.1.3 Summary 15 3.2 Proteins 16 3.2.1 Dietary proteins 16 3.2.2 Protein composition of human milk 16 3.2.3 Total nitrogen content of human milk 17 3.2.4 Approaches used to estimate protein requirements 17 3.2.5 Protein intake and growth 20 3.2.6 Plasma amino acids 21 3.2.7 Immune function 21 3.2.8 Infant behaviour 22 3.2.9 Summary 22 iii NUTRIENT ADEQUACY OF EXCLUSIVE BREASTFEEDING FOR THE TERM INFANT DURING THE FIRST SIX MONTHS OF LIFE 3.3 Vitamin A 22 3.3.1 Introduction 22 3.3.2 Vitamin A in human milk 22 3.3.3 Estimates of vitamin A requirements 23 3.3.4 Plasma retinol 23 3.3.5 Functional end-points 24 3.3.6 Summary 26 3.4 Vitamin D 26 3.4.1 Introduction 26 3.4.2 Factors influencing the vitamin D content of human milk 26 3.4.3 Estimates of vitamin D requirements 27 3.4.4 Vitamin D status and rickets 29 3.4.5 Vitamin D and growth in young infants 29 3.4.6 Vitamin D and growth in older infants 30 3.4.7 Summary 30 3.5 Vitamin B6 30 3.5.1 Introduction 30 3.5.2 Vitamin B6 content in human milk 30 3.5.3 Approaches used to estimate vitamin B6 requirements 31 3.5.4 Estimates of requirements 31 3.5.5 Vitamin B6 status of breastfed infants and lactating women 31 3.5.6 Growth of breastfed infants in relation to vitamin B6 status 32 3.5.7 Summary 32 3.6 Calcium 32 3.6.1 Human milk composition 32 3.6.2 Estimates of calcium requirements 32 3.6.3 Summary 33 3.7 Iron 34 3.7.1 Human milk composition 34 3.7.2 Estimates of iron requirements 34 3.7.3 Summary 35 3.8 Zinc 35 3.8.1 Human milk composition 35 3.8.2 Estimates of zinc requirements 35 3.8.3 Summary 37 References 38 iv REFERENCES Abbreviations & acronyms AI Adequate intake BMD Bone mineral density BMC Bone mineral content CDC Centers for Disease Control and Prevention (USA) DPT Triple vaccine against diphtheria, pertussis and tetanus DXA Dual-energy X-ray absorptiometry EAR Estimated average requirement EAST Erythrocyte aspartate transaminase EPLP Erythrocyte pyridoxal phosphate ESPGAN European Society of Paediatric Gastroenterology FAO Food and Agriculture Organization of the United Nations IDECG International Dietary Energy Consultative Group IU International units NCHS National Center for Health Statistics (USA) NPN Non-protein nitrogen PLP Pyridoxal phosphate PMP Pyridoxamine phosphate PNP Pyridoxine phosphate PTH Parathyroid hormone RE Retinol equivalents SD Standard deviation SDS Standard deviation score UNICEF United Nations Children’s Fund UNU United Nations University WHO World Health Organization v REFERENCES Foreword This review, which was prepared as part of the back- adequacy is most commonly evaluated in terms of ground documentation for a WHO expert consultation,1 growth, but other functional outcomes, e.g. immune evaluates the nutrient adequacy of exclusive breast- response and neurodevelopment, are also considered to feeding for term infants during the first 6 months of the extent that available data permit. life. Nutrient intakes provided by human milk are This review is limited to the nutrient needs of infants. compared with infant nutrient requirements. To avoid It does not evaluate functional outcomes that depend circular arguments, biochemical and physiological on other bioactive factors in human milk, or behaviours methods, independent of human milk, are used to define and practices that are inseparable from breastfeeding, these requirements. nor does it consider consequences for mothers. In The review focuses on human-milk nutrients, which determining the optimal duration of exclusive breast- may become growth limiting, and on nutrients for which feeding in specific contexts, it is important that func- there is a high prevalence of maternal dietary deficiency tional outcomes, e.g. infant morbidity and mortality, in some parts of the world; it assesses the adequacy of also are taken into consideration. energy, protein, calcium, iron, zinc, and vitamins A, The authors would like to thank the World Health B6, and D. This task is confounded by the fact that the Organization for the opportunity to participate in physiological needs for vitamins A and D, iron, zinc – the expert consultation;1 and Nancy Krebs, Kim and possibly other nutrients – are met by the combined Michaelson, Sean Lynch, Donald McCormick, Paul availability of nutrients in human milk and endogenous Pencharz, Mary Frances Picciano, Ann Prentice, Bonny nutrient stores. Specker and Barbara Underwood for reviewing the draft In evaluating the nutrient adequacy of exclusive breast- manuscript. They also express special appreciation for feeding, infant nutrient requirements are assessed in the financial support provided by the United Nations terms of relevant functional outcomes. Nutrient University. 1 Expert consultation on the optimal duration of exclusive breastfeeding, Geneva, World Health Organization, 28–30 March 2001. vii EXECUTIVE SUMMARY Executive summary In this review nutrient adequacy of exclusive The dual dependency on exogenous dietary sources and breastfeeding is most commonly evaluated in terms of endogenous stores to meet requirements needs to be growth. Other functional outcomes, e.g. immune borne in mind particularly when assessing the adequacy response and neurodevelopment, are considered when of iron and zinc in human milk. Human milk, which is a data are available. The dual dependency on exogenous poor source of iron and zinc, cannot be altered by dietary sources and endogenous stores for meeting maternal supplementation with these two nutrients. It requirements is also considered in evaluating human is clear that the estimated iron requirements of infants milk’s nutrient adequacy. When evaluating the nutrient cannot be met by human milk alone at any stage of adequacy of human milk, it is essential to recognize the infancy. The iron endowment at birth meets the iron incomplete knowledge of infant nutrient requirements needs of the breastfed infant in the first half of infancy, in terms of relevant functional outcomes. Particularly i.e. 0 to 6 months. If an exogenous source of iron is not evident is the inadequacy of crucial data for evaluating provided, exclusively breastfed infants are at risk of the nutrient adequacy of exclusive breastfeeding for the becoming iron deficient during the second half of first 4 to 6 months. infancy. Net zinc absorption from human milk falls short of zinc needs, which appear to be subsidized by prenatal Mean intakes of human milk provide sufficient energy stores. and protein to meet mean requirements during the first 6 months of infancy. Since infant growth potential In the absence of studies specifically designed to evaluate drives milk production, the distribution of intakes likely the time at which prenatal stores become depleted, matches the distribution of energy and protein circumstantial evidence has to be used. Available requirements. evidence suggests that the older the exclusively breastfed infant the greater the risk of specific nutrient The adequacy of vitamin A and vitamin B6 in human deficiencies. milk is highly dependent upon maternal diet and nutritional status. In well-nourished populations the The inability to estimate the proportion of exclusively amounts of vitamins A and B6 in human milk are breastfed infants at risk of specific deficiencies is a major adequate to meet the requirements for infants during drawback in terms of developing appropriate public the first 6 months of life. In populations deficient in health policies. Conventional methodologies require vitamins A and B6, the amount of these vitamins in that a nutrient’s average dietary requirement and its human milk will be sub-optimal and corrective measures distribution are known along with the mean and are called for, either through maternal and/or infant distribution of intakes and endogenous stores. supplementation, or complementary feeding for infants. Moreover, exclusive breastfeeding at 6 months is not a The vitamin D content of human milk is insufficient to common practice in developed countries, and it is rarer meet infant requirements. Infants depend on sunlight still in developing countries. There is a serious lack of exposure or exogenous intakes of vitamin D; if these measurement, which impedes evaluation, of the human- are inadequate, the risk of vitamin D deficiency rises milk intakes of 6-month-old exclusively breastfed with age as stores become depleted in the exclusively infants from developing countries. The marked attrition breastfed infant. rates in exclusive breastfeeding through 6 months postpartum, even among women who are both well The calcium content of human milk is fairly constant nourished and highly motivated, is a major gap in our throughout lactation and is not influenced by maternal understanding of the biological, cultural and social diet. Based on the estimated calcium intakes of determinants of the duration of exclusive breastfeeding. exclusively breastfed infants and an estimated A limitation to promoting exclusive breastfeeding for absorption efficiency of > 70%, human milk meets the the first 6 months of life is our lack of understanding of calcium requirements of infants during the first the reasons for the attrition rates. Improved 6months of life. understanding of the biological, socioeconomic and 1 NUTRIENT ADEQUACY OF EXCLUSIVE BREASTFEEDING FOR THE TERM INFANT DURING THE FIRST SIX MONTHS OF LIFE cultural factors influencing the timing of supplemen- for mothers been considered. It is important that tation of the breastfed infant’s diet is an important part functional outcomes, e.g. infant morbidity and mortality, of advocating a globally uniform infant-feeding policy be taken carefully into account in determining the that accurately weighs both this policy’s benefits and optimal duration of exclusive breastfeeding in specific possible negative outcomes. environments. It is important to recognize that this review is limited This review was prepared parallel to, but separate from, to the nutrient needs of infants. No attempt has been a systematic review of the scientific literature on the made to evaluate functional outcomes that depend on optimal duration of exclusive breastfeeding.1 These other bioactive factors in human milk, or behaviours assessments served as the basis for discussion during an and practices that are inseparable from breastfeeding. expert consultation (Geneva, 28–30 March 2001), Neither have the consequences, positive or negative, whose report is found elsewhere.2 1 Kramer MS, Kakuma R. The optimal duration of exclusive breastfeeding: a systematic review. Geneva, World Health Organization, document WHO/NHD/01.08–WHO/FCH/CAH/ 01.23, 2001. 2 The optimal duration of exclusive breastfeeding: report of an expert consultation. Geneva, World Health Organization, document WHO/NHD/01.09–WHO/FCH/CAH/01.24, 2001. 2
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