Seminars in Fetal & Neonatal Medicine
Volume 12, Issue 1 , Pages 26-34 , February 2007

Enteral nutrition for premature infants: The role of human milk

  • Howard Heiman

      Affiliations

    • Division of Neonatal–Perinatal Medicine, Schneider Children's Hospital at North Shore, Manhasset, NY, USA
    • ,
  • Richard J. Schanler

      Affiliations

    • Division of Neonatal–Perinatal Medicine, Schneider Children's Hospital at North Shore, Manhasset, NY, USA
    • Department of Pediatrics, Albert Einstein College of Medicine, Bronx, NY, USA
    • Corresponding Author InformationCorresponding author. Neonatal–Perinatal Medicine, North Shore University Hospital, 300 Community Drive, Manhasset, NY 11030, USA. Tel.: +1 516 562 4665; fax: +1 516 562 4516.

References 

  1. Ziegler EE, O'Donnell AM, Nelson SE, Fomon SJ. Body composition of the reference fetus. Growth. 1976;40:329–341
  2. Polberger S. Quality of growth in preterm neonates fed individually fortified human milk. In:  Battaglia FC,  Pedraz C,  Sawatzki G,  Falkner F,  Doménech E,  Morán J, et al. editor. Maternal and extrauterine nutritional factors. Their influence on fetal and infant growth. Madrid: Ediciones Ergon; 1996;p. 395–403
  3. Neville MC, Keller RP, Seacat J, Casey CE, Allen JC, Archer P. Studies on human lactation. I. Within-feed and between-breast variation in selected components of human milk. Am J Clin Nutr. 1984;40:635–646
  4. Valentine CJ, Hurst NM, Schanler RJ. Hindmilk improves weight gain in low-birth-weight infants fed human milk. J Pediatr Gastroenterol Nutr. 1994;18:474–477
  5. Greer FR, McCormick A, Loker J. Changes in fat concentration of human milk during delivery by intermittent bolus and continuous mechanical pump infusion. J Pediatr. 1984;105:745–749
  6. Schanler RJ. Special methods in feeding the preterm infant. In:  Tsang RC,  Nichols BL editor. Nutrition during infancy. Philadelphia: Hanley and Belfus; 1988;p. 314–325
  7. Weber A, Loui A, Jochum F, Bührer C, Obladen M. Breast milk from mothers of very low birthweight infants: variability in fat and protein content. Acta Pædiatr. 2001;90:772–775
  8. Wight NE. Donor human milk for preterm infants. J Perinatol. 2001;21:249–254
  9. Garza C, Hopkinson JM, Schanler RJ. Human milk banking. In:  Howell RR,  Morriss FH,  Pickering LK editor. Human milk in infant nutrition and health. Springfield, IL: Charles C. Thomas; 1986;p. 225–255
  10. Oxtoby MJ. Human immunodeficiency virus and other viruses in human milk: placing the issues in broader perspective. Pediatr Infect Dis J. 1988;7:825–835
  11. Bjorksten B, Burman LG, DeChateau P, Fredrikzon B, Gothefors L, Hernell O. Collecting and banking human milk: to heat or not to heat?. Br Med J. 1980;281:765–769
  12. Koenig A, Diniz EMA, Barbarosa SFC, Vaz FAC. Immunologic factors in human milk: the effects of gestational age and pasteurization. J Hum Lact. 2005;21:439–443
  13. Hamprecht K, Maschmann J, Muller D, Dietz K, Besenthal I, Goelz R, et al. Cytomegalovirus (CMV) inactivation in breast milk: reassessment of pasteurization and freeze-thawing. Pediatr Res. 2004;56:529–535
  14. Giorgi M, Heiman H, Codipilly C, Potak D, Schanler R. Pasteurization preserves the concentration of IL-8 in human milk. E-PAS. 2006;59.3850.4 2006.
  15. Goldblum RM, Dill CW, Albrecht TB, Alford ES, Garza C, Goldman AS. Rapid high-temperature treatment of human milk. J Pediatr. 1984;104:380–385
  16. Prolacta Bioscience . Processing of donor human milk. Manufacturer's documentation. 2006;
  17. Atkinson SA, Bryan MH, Anderson GH. Human milk feeding in premature infants: Protein, fat and carbohydrate balances in the first two weeks of life. J Pediatr. 1981;99:617–624
  18. Atkinson SA, Radde IC, Anderson GH. Macromineral balances in premature infants fed their own mothers’ milk or formula. J Pediatr. 1983;102:99–106
  19. Cooper PA, Rothberg AD, Pettifor JM, Bolton KD, Devenhuis S. Growth and biochemical response of premature infants fed pooled preterm milk or special formula. J Pediatr Gastroenterol Nutr. 1984;3:749–754
  20. Kashyap S, Schulze KF, Forsyth M, Dell RB, Ramakrishnan R, Heird WC. Growth, nutrient retention, and metabolic response of low-birth-weight infants fed supplemented and unsupplemented preterm human milk. Am J Clin Nutr. 1990;52:254–262
  21. Gross SJ. Growth and biochemical response of preterm infants fed human milk or modified infant formula. N Engl J Med. 1983;308:237–241
  22. Tyson JE, Lasky RE, Mize CE, Richards CJ, Blair-Smith N, Whyte R, et al. Growth, metabolic response, and development in very-low-birth-weight infants fed banked human milk or enriched formula. I. Neonatal findings. J Pediatr. 1983;103:95–104
  23. Boyd CA, Quigley MA, Brocklehurst P. Donor breast milk versus infant formula for preterm infants: a systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed, in press. doi:10.1136/adc.2005.089490 [published online 5 Apr 2006] .
  24. Polberger SKT, Axelsson IE, Räihä NCR. Urinary and serum urea as indicators of protein metabolism in very low birthweight infants fed varying human milk protein intakes. Acta Paediatr. Scand. 1990;79:737–742
  25. Rowe JC, Wood DH, Rowe DW, Raisz LG. Nutritional hypophosphatemic rickets in a premature infant fed breast milk. N Engl J Med. 1979;300:293–296
  26. Pettifor JM, Rajah R, Venter A. Bone mineralization and mineral homeostasis in very low-birth- weight infants fed either human milk or fortified human milk. J Pediatr Gastroenterol Nutr. 1989;8:217–224
  27. Lucas A, Brooke OG, Baker BA, Bishop N, Morley R. High alkaline phosphatase activity and growth in preterm neonates. Arch Dis Child. 1989;64:902–909
  28. Fewtrell MS, Prentice A, Cole TJ, Lucas A. Effects of growth during infancy and childhood on bone mineralization and turnover in preterm children aged 8-12 years. Acta Pædiatr. 2000;89:148–153
  29. Roy RN, Chance GW, Radde IC, Hill DE, Willis DM, Sheepers J. Late hyponatremia in very low birthweight infants. Pediatr Res. 1976;10:526–531
  30. Obladen M, Loui A, Kampmann W, Renz H. Zinc deficiency in rapidly growing preterm infants. Acta Paediatr. 1998;87:685–691
  31. Narayanan I, Prakash K, Bala S, Verma RK, Gujral VV. Partial supplementation with expressed breast-milk for prevention of infection in low-birth-weight infants. Lancet. 1980;2:561–563
  32. Narayanan I, Prakash K, Murthy NS, Gujral VV. Randomised controlled trial of effect of raw and holder pasteurised human milk and of formula supplements on incidence of neonatal infection. Lancet. 1984;ii:1111–1113
  33. Lucas A, Cole TJ. Breast milk and neonatal necrotizing enterocolitis. Lancet. 1990;336:1519–1523
  34. Contreras-Lemus J, Flores-Huerta S, Cisneros-Silva I, Orozco-Vigueras H, Hernandez-Gutierrez J, Fernandez-Morales J, et al. Disminucion de la morbilidad en neonatos pretermino alimentados con leche de su propia madre. Biol Med Hosp Infant Mex. 1992;49:671–677
  35. El-Mohandes AE, Picard MB, Simmens SJ, Keiser JF. Use of human milk in the intensive care nursery decreases the incidence of nosocomial sepsis. J Perinatol. 1998;17:130–134
  36. Schultz K, Soltesz G, Mestyan J. The metabolic consequences of human milk and formula feeding in premature infants. Acta Paediatr Scand. 1980;69:647–652
  37. Lucas A, McLaughlan P, Coombs RRA. Latent anaphylactic sensitisation of infants of low birth weight to cows’ milk proteins. Br Med J. 1986;289:1254–1256
  38. Polberger SKT, Axelsson IA, Raiha NCR. Growth of very low birth weight infants on varying amounts of human milk protein. Pediatr Res. 1989;25:414–419
  39. Funkquist E, Tuvemo T, Jonsson B, Serenius F, Hedberg-Nyqvist K. Growth and breastfeeding among low birth weight infants fed with or without protein enrichment of human milk. Uppsala J Med Sci. 2006;111:97–108
  40. Kuschel CA, Harding JE. Protein supplementation of human milk for promoting growth in preterm infants (Cochrane Review). The Cochrane Library. 2001;
  41. Rowe J, Rowe D, Horak E, Spackman T, Saltzman R, Robinson S, et al. Hypophosphatemia and hypercalciuria in small premature infants fed human milk: evidence for inadequate dietary phosphorus. J Pediatr. 1984;104:112–117
  42. Schanler RJ, Garza C. Improved mineral balance in very low birth weight infants fed fortified human milk. J Pediatr. 1987;112:452–456
  43. Kuschel CA, Harding JE. Multicomponent fortified human milk for promoting growth in preterm infants. The Cochrane Library. 2005;p. 1–36
  44. Kumar SP, Sacks LM. Hyponatremia in very low-birth-weight infants and human milk feedings. J Pediatr. 1978;93:1026–1027
  45. Hylander MA, Strobino DM, Dhanireddy R. Human milk feedings and infection among very low birth weight infants. Pediatrics. 1998;102:e38
  46. Lucas A, Fewtrell MS, Morley R, Lucas PJ, Baker BA, Lister G, et al. Randomized outcome trial of human milk fortification and developmental outcome in preterm infants. Am J Clin Nutr. 1996;64:142–151
  47. Schanler RJ. Human milk fortification for premature infants. Am J Clin Nutr. 1996;64:249–250
  48. Schanler RJ, Shulman RJ, Lau C. Feeding strategies for premature infants: Beneficial outcomes of feeding fortified human milk vs preterm formula. Pediatrics. 1999;103:1150–1157
  49. Schanler RJ, Lau C, Hurst NM, Smith EO. Randomized trial of donor human milk versus preterm formula as substitutes for mothers’ own milk in the feeding of extremely premature infants. Pediatrics. 2005;116:400–406
  50. Furman L, Taylor G, Minich N, Hack M. The effect of maternal milk on neonatal morbidity of very low-birth-weight infants. Arch Pediatr Adolesc Med. 2003;157:66–71
  51. Meinzen-Derr J, Poindexter BB, Donovan EF, Stoll BJ, Warner BB, Morrow A, et al. The role of human milk feedings in risk of late-onset sepsis. Pediatr Res. 2004;55:393A
  52. Ronnestad A, Abrahamsen TG, Medbo S, Reigstad H, Lossius K, Kaaresen PI, et al. Late-onset septicemia in a Norwegian national cohort of extremely premature infants receiving very early full human milk feeding. Pediatrics. 2006;115:269–276
  53. de Silva A, Jones PW, Spenser SA. Does human milk reduce infection rates in preterm infants? A systematic review. Arch Dis Child Fetal Neonatal Ed. 2004;89:F509–F513
  54. Lucas A, Cole TJ, Morley R, Lucas PJ, David JA, Bamford MF, et al. Factors associated with maternal choice to provide breastmilk for low birth weight infants. Arch Dis Child. 1988;59:722–730
  55. Anderson JW, Johnstone BM, Remley DT. Breastfeeding and cognitive development: a meta-analysis. Am J Clin Nutr. 1999;70:525–535
  56. Lucas A, Morley R, Cole TJ, Lister G, Leeson-Payne C. Breast milk and subsequent intelligence quotient in children born preterm. Lancet. 1992;339:261–264
  57. Horwood LJ, Fergusson DM. Breastfeeding and later cognitive and academic outcomes. Pediatrics. 1998;101:E91–E97
  58. Horwood LJ, Mogridge N, Darlow BA. Cognitive, educational, and behavioral outcomes at 7 to 8 years in a national very low birthweight cohort. Arch Dis Child Fetal Neonatal Ed. 1998;79:F12–F20
  59. Horwood LJ, Darlow BA, Mogridge N. Breast milk feeding and cognitive ability at 7-8 years. Arch Dis Child Fetal Neonatal Ed. 2001;84:F23–F27
  60. O'Connor DL, Jacobs J, Hall R, Adamkin D, Auestad N, Castillo M, et al. Growth and development of premature infants fed predominantly human milk, predominantly premature infant formula, or a combination of human milk and premature formula. J Pediatr Gastroenterol Nutr. 2003;37:437–446
  61. Vohr BR, Poindexter BB, Dusick AM, McKinley LT, Wright LL, Langer JC, et al. Beneficial effects of breast milk in the neonatal intensive care unit on the developmental outcome of extremely low birth weight infants at 18 months of age. Pediatrics. 2006;118:e115–e123
  62. Hack M, Flannery DJ, Schluchter M, Cartar L, Borawski E, Klein N. Outcomes in young adulthood for very-low-birth-weight infants. N Engl J Med. 2002;346:149–157
  63. Lucas A, Morley R, Cole TJ, Gore SM. A randomised multicentre study of human milk versus formula and later development in preterm infants. Arch Dis Child. 1994;70:F141–F146
  64. Lucas A, Gore SM, Cole TJ, Bamford MF, Dossetor JFB, Barr I, et al. Multicenter trial on feeding low birthweight infants: effects of diet on early growth. Arch Dis Child. 1984;59:722–730
  65. Moody GJ, Schanler RJ, Lau C, Shulman RJ. Feeding tolerance in premature infants fed fortified human milk. J Pediatr Gastroenterol Nutr. 2000;30:408–412
  66. Barrett-Reis B, Hall RT, Schanler RJ, Berseth CL, Chan G, Ernst JA, et al. Enhanced growth of preterm infants fed a new powdered human milk fortifier: a randomized controlled trial. Pediatrics. 2000;106:581–588
  67. Porcelli P, Schanler R, Greer F, Chan G, Gross S, Mehta N, et al. Growth in human milk-fed very low birth weight infants receiving a new human milk fortifier. Ann Nutr Metab. 2000;44:2–10
  68. Berseth CL, Van Aerde JE, Gross S, Stolz SI, Haris CL, Hansen JW. Growth, efficacy, and safety of feeding an iron-fortified human milk fortifier. Pediatrics. 2004;114:e699–e706
  69. Greer FR, McCormick A. Improved bone mineralization and growth in premature infants fed fortified own mother's milk. J Pediatr. 1988;112:961–969
  70. Ziegler EE. Breast-milk fortification. Acta Paediatr. 2001;90:720–723
  71. Schanler RJ. Human milk supplementation for preterm infants. Acta Paediatr. 2005;94:64–67
  72. Santiago MS, Codipilly CN, Potak DC, Schanler RJ. Effect of human milk fortifiers on bacterial growth in human milk. J Perinatol. 2005;25:647–649
  73. Lucas A, Fewtrell MS, Morley R, Singhal A, Abbott RA, Isaacs E, et al. Randomized trial of nutrient-enriched formulas versus standard formula for postdischarge preterm infants. Pediatrics. 2001;108:703–711
  74. Chan GM. Growth and bone mineral status of discharged very low birth weight infants fed different formulas or human milk. J Pediatr. 1993;123:439–443
  75. Rubinacci A, Sirtori P, Moro G, Galli L, Minoli I, Tessari L. Is there an impact of birth weight and early life nutrition on bone mineral content in preterm born infants and children?. Acta Paediatr. 1993;82:711–713
  76. Wauben IP, Atkinson SA, Grad TL, Shah JK, Paes B. Moderate nutrient supplementation of mother's milk for preterm infants support adequate bone mass and short-term growth: a randomized, controlled trial. Am J Clin Nutr. 1998;67:465–472
  77. Koo WWK, Sherman R, Succop P, Oestrich AE, Tsang RC, Krug-Wispe SK, et al. Sequential bone mineral content in small preterm infants with and without fractures and rickets. J Bone Miner Res. 1988;3:193–197
  78. Tsang RC, Namgung R., Newborn bone development. In: Ross Products Division, editor. Posthospital nutrition in the preterm infant, report of the 106th Ross Conference on Pediatric Research. Columbus: Ross Products Division/Abbott Laboratories; 1996. p. 21–26.
  79. Fewtrell MS, Cole TJ, Bishop NJ, Lucas A. Neonatal factors predicting childhood height in preterm infants: Evidence for a persisting effect of early metabolic bone disease?. J Pediatr. 2000;137:668–673
  80. Wauben IPM, Atkinson SA, Shah JK, Paes B. Growth and body composition of preterm infants: influence of nutrient fortification of mother's milk in hospital and breast feeding post-hospital discharge. Acta Paediatr. 1998;87:780–785
  81. Bishop NJ, King FJ, Lucas A. Increased bone mineral content of preterm infants fed with a nutrient enriched formula after discharge from hospital. Arch Dis Child. 1993;68:573–578
  82. Lucas A, Bishop NJ, King FJ, Cole TJ. Randomized trial of nutrition for preterm infants after discharge. Arch Dis Child. 1992;67:324–327
  83. Cooke RJ, Griffin IJ, McCormick K, Wells JCK, Smith JS, Robinson SJ, et al. Feeding preterm infants after hospital discharge: effect of dietary manipulation on nutrient intake and growth. Pediatr Res. 1998;43:355–360
  84. Cooke RJ, McCormick K, Griffin IJ, Embleton N, Faulkner K, Wells JC, et al. Feeding preterm infants after hospital discharge: effect of diet on body composition. Pediatr Res. 1999;46:461–464
  85. Brunton JA, Saigal S, Atkinson SA. Growth and body composition in infants with bronchopulmonary dysplasia up to 3 months corrected age: A randomized trial of a high-energy nutrient-enriched formula fed after hospital discharge. J Pediatr. 1998;133:340–345
  86. Cooke RJ, Embleton ND, Griffin IJ, Wells JC, McCormick KP. Feeding preterm infants after hospital discharge: growth and development at 18 months of age. Pediatr Res. 2001;49:719–722
  87. Schanler RJ, Burns PA, Abrams SA, Garza C. Bone mineralization outcomes in human milk-fed preterm infants. Pediatr Res. 1992;31:583–586
  88. Bishop NJ, Dahlenburg SL, Fewtrell MS, Morley R, Lucas A. Early diet of preterm infants and bone mineralization at age five years. Acta Paediatr. 1996;85:230–236
  89. Jones G, Riley M, Dwyer T. Breastfeeding in early life and bone mass in prepubertal children: a longitudinal study. Osteoporosis Int. 2000;11:146–152
  90. Morley R, Lucas A. Randomized diet in the neonatal period and growth performance until 7.5-8 y of age in preterm children. Am J Clin Nutr. 2000;71:822–828
  91. Hall RT. Nutritional follow-up of the breastfeeding premature infant after hospital discharge. Pediatr Clin North Am. 2001;48:453–460

PII: S1744-165X(06)00099-0

doi: 10.1016/j.siny.2006.10.004

Seminars in Fetal & Neonatal Medicine
Volume 12, Issue 1 , Pages 26-34 , February 2007

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