Neurodevelopment, nutrition, and growth until 12 mo of age in infants fed a low-energy, low-proteinformula supplemented with bovine milk fat globule membranes: A randomized controlled trial

American Journal of Clinical Nutrition

Volumn 99, Issue 4, 2014, Pages 860-868

  Timby, Niklas ^a   Domellöf, Erik ^a   Hernell, Olle ^a   Lönnerdal, Bo ^b   Domellöf, Magnus ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ARTIFICIAL MILK; BAYLEY SCALES OF INFANT DEVELOPMENT; BODY FAT; BODY MASS; BREAST FEEDING; CATTLE; CHILD GROWTH; COGNITION; CONTROLLED STUDY; DIETARY COMPLIANCE; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; HEAD CIRCUMFERENCE; HUMAN; INFANT; INFANT NUTRITION; MAJOR CLINICAL STUDY; MILK; NERVOUS SYSTEM DEVELOPMENT; OUTCOME ASSESSMENT; PROTEIN CONTENT; RANDOMIZED CONTROLLED TRIAL; WEIGHT GAIN;

ANIMALS; BODY HEIGHT; BODY MASS INDEX; BREAST FEEDING; CATTLE; CHILD DEVELOPMENT; COGNITION; DIET, PROTEIN-RESTRICTED; DOUBLE-BLIND METHOD; ENERGY INTAKE; FEMALE; GLYCOLIPIDS; GLYCOPROTEINS; HUMANS; INFANT; INFANT BEHAVIOR; INFANT FORMULA; INFANT, NEWBORN; LONGITUDINAL STUDIES; MALE; MOTOR SKILLS; NEUROGENESIS; SWEDEN; VERBAL BEHAVIOR; WEIGHT GAIN;

EID: 84896906801     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.113.064295     Document Type: Article

References (62)

1. World Health Organization. Global strategy for infant and young child feeding. Geneva, Switzerland: WHO, 2003.
2. Anderson JW, Johnstone BM, Remley DT. Breast-feeding and cognitive development: a meta-analysis. Am J Clin Nutr 1999;70:525-35. (Pubitemid 29463447)
3. Kramer MS, Aboud F, Mironova E, Vanilovich I, Platt RW, Matush L, Igumnov S, Fombonne E, Bogdanovich N, Ducruet T, et al. Breastfeeding and child cognitive development: new evidence from a large randomized trial. Arch Gen Psychiatry 2008;65:578-84. (Pubitemid 351645053)
4. Spitsberg VL. Invited review: bovine milk fat globule membrane as a potential nutraceutical. J Dairy Sci 2005;88:2289-94. (Pubitemid 41044832)
5. Wang B, Brand-Miller J, McVeagh P, Petocz P. Concentration and distribution of sialic acid in human milk and infant formulas. Am J Clin Nutr 2001;74:510-5. (Pubitemid 32880262)
6. Wang B, Yu B, Karim M, Hu H, Sun Y, McGreevy P, Petocz P, Held S, Brand-Miller J. Dietary sialic acid supplementation improves learning and memory in piglets. Am J Clin Nutr 2007;85:561-9. (Pubitemid 46220963)
7. Pan XL, Izumi T. Variation of the ganglioside compositions of human milk, cow's milk and infant formulas. Early Hum Dev 2000;57:25-31. (Pubitemid 30006876)
8. McJarrow P, Schnell N, Jumpsen J, Clandinin T. Influence of dietary gangliosides on neonatal brain development. Nutr Rev 2009;67:451-63.
9. Gurnida DA, Rowan AM, Idjradinata P, Muchtadi D, Sekarwana N. Association of complex lipids containing gangliosides with cognitive development of 6-month-old infants. Early Hum Dev 2012;88:595-601.
10. Zeisel SH, Char D, Sheard NF. Choline, phosphatidylcholine and sphingomyelin in human and bovine milk and infant formulas. J Nutr 1986;116:50-8. (Pubitemid 16212055)
11. Oshida K, Shimizu T, Takase M, Tamura Y, Yamashiro Y. Effects of dietary sphingomyelin on central nervous system myelination in developing rats. Pediatr Res 2003;53:589-93. (Pubitemid 36406728)
12. Tanaka K, Hosozawa M, Kudo N, Yoshikawa N, Hisata K, Shoji H, Shinohara K, Shimizu T. The pilot study: sphingomyelin-fortified milk has a positive association with the neurobehavioural development of very low birth weight infants during infancy, randomized control trial. Brain Dev 2013;35:45-52.
13. Zeisel SH. The fetal origins of memory: the role of dietary choline in optimal brain development. J Pediatr 2006;149:S131-6. (Pubitemid 44278868)
14. Wu BT, Dyer RA, King DJ, Richardson KJ, Innis SM. Early second trimester maternal plasma choline and betaine are related to measures of early cognitive development in term infants. PLoS ONE 2012;7:e43448.
15. Wong WW, Hachey DL, Insull W, Opekun AR, Klein PD. Effect of dietary cholesterol on cholesterol synthesis in breast-fed and formulafed infants. J Lipid Res 1993;34:1403-11. (Pubitemid 23230317)
16. Haque ZU, Mozaffar Z. Importance of dietary cholesterol for the maturation of mouse brain myelin. Biosci Biotechnol Biochem 1992; 56:1351-4. (Published erratum appears in Biosci Biotechnol Biochem 1992;56:A21.)
17. Elias PK, Elias MF, D'Agostino RB, Sullivan LM, Wolf PA. Serum cholesterol and cognitive performance in the Framingham Heart Study. Psychosom Med 2005;67:24-30.
18. Baird J, Poole J, Robinson S, Marriott L, Godfrey K, Cooper C, Inskip H, Law C. Milk feeding and dietary patterns predict weight and fat gains in infancy. Paediatr Perinat Epidemiol 2008;22:575-86.
19. Dewey KG. Growth characteristics of breast-fed compared to formulafed infants. Biol Neonate 1998;74:94-105. (Pubitemid 28377139)
20. Singhal A, Lucas A. Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet 2004;363:1642-5. (Pubitemid 38625670)
21. Owen CG, Martin RM, Whincup PH, Smith GD, Cook DG. Effect of infant feeding on the risk of obesity across the life course: a quantitative review of published evidence. Pediatrics 2005;115:1367-77. (Pubitemid 43843245)
22. Baird J, Fisher D, Lucas P, Kleijnen J, Roberts H, Law C. Being big or growing fast: systematic review of size and growth in infancy and later obesity. BMJ 2005;331:929.
23. Owen CG, Whincup PH, Gilg JA, Cook DG. Effect of breast feeding in infancy on blood pressure in later life: systematic review and metaanalysis. BMJ 2003;327:1189-95.
24. Law CM, Shiell AW, Newsome CA, Syddall HE, Shinebourne EA, Fayers PM, Martyn CN, de Swiet M. Fetal, infant, and childhood growth and adult blood pressure: a longitudinal study from birth to 22 years of age. Circulation 2002;105:1088-92. (Pubitemid 34212619)
25. Owen CG, Martin RM, Whincup PH, Smith GD, Cook DG. Does breastfeeding influence risk of type 2 diabetes in later life? A quantitative analysis of published evidence. Am J Clin Nutr 2006;84:1043-54. (Pubitemid 44730374)
26. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992;35:595-601.
27. Knip M, Virtanen SM, Akerblom HK. Infant feeding and the risk of type 1 diabetes. Am J Clin Nutr 2010;91(suppl):1506S-13S.
28. Koletzko B, Broekaert I, Demmelmair H, Franke J, Hannibal I, Oberle D, Schiess S, Baumann BT, Verwied-Jorky S. Protein intake in the first year of life: a risk factor for later obesity? The E.U. childhood obesity project. Adv Exp Med Biol 2005;569:69-79. (Pubitemid 43779609)
29. Heinig MJ, Nommsen LA, Peerson JM, Lönnerdal B, Dewey KG. Energy and protein intakes of breast-fed and formula-fed infants during the first year of life and their association with growth velocity: the DARLING Study. Am J Clin Nutr 1993;58:152-61. (Pubitemid 23227885)
30. Alexy U, Kersting M, Sichert-Hellert W, Manz F, Schoch G. Macronutrient intake of 3- to 36-month-old German infants and children: results of the DONALD Study. Dortmund Nutritional and Anthropometric Longitudinally Designed Study. Ann Nutr Metab 1999;43:14-22. (Pubitemid 29267897)
31. Khan S, Prime DK, Hepworth AR, Lai CT, Trengove NJ, Hartmann PE. Investigation of short-term variations in term breast milk composition during repeated breast expression sessions. J Hum Lact 2013;29:196-204.
32. Koletzko B, Baker S, Cleghorn G, Neto UF, Gopalan S, Hernell O, Hock QS, Jirapinyo P, Lönnerdal B, Pencharz P, et al. Global standard for the composition of infant formula: recommendations of an ESPGHAN coordinated international expert group. J Pediatr Gastroenterol Nutr 2005;41:584-99. (Pubitemid 41579668)
33. The European Union. Commission Directive 2006/141/EC of 22 December 2006 on infant formulae and follow-on formulae and amending Directive 1999/21/EC. Available from: http://eur-lex.europa.eu/Lex-UriServ/LexUriServ.do?uri=CONSLEG: 2006L0141:20081028:EN:PD. (cited 1 April 2013) 2006:1-33.
34. Life Sciences Research Office Report. Assessment of nutrient requirements for infant formulas. J Nutr 1998;128(suppl):2059S-93S.
35. World Health Organization, Food and Agriculture Organization of the United Nations. Codex alimentarius: standard for infant formula and formulas for special medical purposes intended for infants. 2011. Available from: http://www.codexalimentarius.org/download/standards/288/CXS-072e.pdf (cited 1 June 2013).
36. US Department of Agriculture, Food and Nutrition Service. The Special Supplemental Nutrition Program for Women, Infants, and Children (WIC). 2013. Available from: http://www.fns.usda.gov/wic/lawsandregulations/WICRegulations- 7CFR246.pdf (cited 20 June 2013).
37. Hester SN, Hustead DS, Mackey AD, Singhal A, Marriage BJ. Is the macronutrient intake of formula-fed infants greater than breast-fed infants in early infancy? J Nutr Metab 2012;2012:891201.
38. Garza C, Butte NF. Energy intakes of human milk-fed infants during the first year. J Pediatr 1990;117:S124-31. (Pubitemid 20241585)
39. de Bruin NC, Degenhart HJ, Gal S, Westerterp KR, Stijnen T, Visser HK. Energy utilization and growth in breast-fed and formula-fed infants measured prospectively during the first year of life. Am J Clin Nutr 1998;67:885-96. (Pubitemid 28196663)
40. Sievers E, Oldigs HD, Santer R, Schaub J. Feeding patterns in breastfed and formula-fed infants. Ann Nutr Metab 2002;46:243-8. (Pubitemid 35398600)
41. Li R, Fein SB, Grummer-Strawn LM. Do infants fed from bottles lack self-regulation of milk intake compared with directly breastfed infants? Pediatrics 2010;125:e1386-93.
42. Bayley N. Bayley scales of infant and toddler development. 3rd ed. San Antonio, TX: Harcourt Assessment, 2006.
43. World Health Organization. WHO child growth standards: length/ height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. Geneva, Switzerland: World Health Organization, 2006.
44. World Health Organization. WHO child growth standards: head circumference-for-age, arm circumference-for-age, triceps skinfold-forage and subscapular skinfold-for-age: methods and development. Geneva, Switzerland: World Health Organization, 2007.
45. Birch EE, Garfield S, Hoffman DR, Uauy R, Birch DG. A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants. Dev Med Child Neurol 2000;42:174-81. (Pubitemid 30145332)
46. Auestad N, Halter R, Hall RT, Blatter M, Bogle ML, Burks W, Erickson JR, Fitzgerald KM, Dobson V, Innis SM, et al. Growth and development in term infants fed long-chain polyunsaturated fatty acids: a double-masked, randomized, parallel, prospective, multivariate study. Pediatrics 2001;108:372-81.
47. Zavaleta N, Kvistgaard AS, Graverholt G, Respicio G, Guija H, Valencia N, Lönnerdal B. Efficacy of an MFGM-enriched complementary food in diarrhea, anemia, and micronutrient status in infants. J Pediatr Gastroenterol Nutr 2011;53:561-8.
48. Veereman-Wauters G, Staelens S, Rombaut R, Dewettinck K, Deboutte D, Brummer RJ, Boone M, Le Ruyet P. Milk fat globule membrane (INPULSE) enriched formula milk decreases febrile episodes and may improve behavioral regulation in young children. Nutrition 2012;28:749-52.
49. Fomon SJ, Filer LJ, Ziegler EE, Bergmann KE, Bergmann RL. Skim milk in infant feeding. Acta Paediatr Scand 1977;66:17-30. (Pubitemid 8013507)
50. Fomon SJ, Filmer LJ Jr, Thomas LN, Anderson TA, Nelson SE. Influence of formula concentration on caloric intake and growth of normal infants. Acta Paediatr Scand 1975;64:172-81.
51. Taveras EM, Scanlon KS, Birch L, Rifas-Shiman SL, Rich-Edwards JW, Gillman MW. Association of breastfeeding with maternal control of infant feeding at age 1 year. Pediatrics 2004;114:e577-83. (Pubitemid 41647665)
52. Taveras EM, Rifas-Shiman SL, Scanlon KS, Grummer-Strawn LM, Sherry B, Gillman MW. To what extent is the protective effect of breastfeeding on future overweight explained by decreased maternal feeding restriction? Pediatrics 2006;118:2341-8. (Pubitemid 46397572)
53. Farrow C, Blissett J. Does maternal control during feeding moderate early infant weight gain? Pediatrics 2006;118:e293-8. (Pubitemid 46085370)
54. Farrow C, Blissett J. Breast-feeding, maternal feeding practices and mealtime negativity at one year. Appetite 2006;46:49-56. (Pubitemid 43042347)
55. Mizuno K, Ueda A. Changes in sucking performance from nonnutritive sucking to nutritive sucking during breast- and bottle-feeding. Pediatr Res 2006;59:728-31. (Pubitemid 43740020)
56. Júlíusson PB, Roelants M, Nordal E, Furevik L, Eide GE, Moster D, Hauspie R, Bjerknes R. Growth references for 0-19 year-old Norwegian children for length/height, weight, body mass index and head circumference. Ann Hum Biol 2013;40:220-7.
57. Räihä NC, Fazzolari-Nesci A, Cajozzo C, Puccio G, Monestier A, Moro G, Minoli I, Haschke-Becher E, Bachmann C, Van't Hof M, et al. Whey predominant, whey modified infant formula with protein/energy ratio of 1.8 g/100 kcal: adequate and safe for term infants from birth to four months. J Pediatr Gastroenterol Nutr 2002;35:275-81.
58. Turck D, Grillon C, Lachambre E, Robiliard P, Beck L, Maurin JL, Kempf C, Bernet JP, Marx J, Lebrun F, et al. Adequacy and safety of an infant formula with a protein/energy ratio of 1.8 g/100 kcal and enhanced protein efficiency for term infants during the first 4 months of life. J Pediatr Gastroenterol Nutr 2006;43:364-71. (Pubitemid 44368194)
59. Koletzko B, von Kries R, Closa R, Escribano J, Scaglioni S, Giovannini M, Beyer J, Demmelmair H, Gruszfeld D, Dobrzanska A, et al. Lower protein in infant formula is associated with lower weight up to age 2 y: a randomized clinical trial. Am J Clin Nutr 2009;89:1836-45.
60. Socha P, Grote V, Gruszfeld D, Janas R, Demmelmair H, Closa- Monasterolo R, Subias JE, Scaglioni S, Verduci E, Dain E, et al. Milk protein intake, the metabolic-endocrine response, and growth in infancy: data from a randomized clinical trial. Am J Clin Nutr 2011;94:1776S-84S.
61. Sandström O, Lönnerdal B, Graverholt G, Hernell O. Effects of alpha-lactalbumin-enriched formula containing different concentrations of glycomacropeptide on infant nutrition. Am J Clin Nutr 2008;87:921-8. (Pubitemid 351549237)
62. Lönnerdal B, Hernell O. Effects of feeding ultrahigh-temperature (UHT)-treated infant formula with different protein concentrations or powdered formula, as compared with breast-feeding, on plasma amino acids, hematology, and trace element status. Am J Clin Nutr 1998;68:350-6. (Pubitemid 28355653)