A systematic review and meta-analysis of the nutrient content of preterm and term breast milk

Dominica A Gidrewicz, Tanis R Fenton, Dominica A Gidrewicz, Tanis R Fenton

Abstract

Background: Breast milk nutrient content varies with prematurity and postnatal age. Our aims were to conduct a meta-analysis of preterm and term breast milk nutrient content (energy, protein, lactose, oligosaccharides, fat, calcium, and phosphorus); and to assess the influence of gestational and postnatal age. Additionally we assessed for differences by laboratory methods for: energy (measured vs. calculated estimates) and protein (true protein measurement vs. the total nitrogen estimates).

Methods: Systematic review results were summarized graphically to illustrate the changes in composition over time for term and preterm milk. Since breast milk fat content varies within feeds and diurnally, to obtain accurate estimates we limited the meta-analyses for fat and energy to 24-hour breast milk collections.

Results: Forty-one studies met the inclusion criteria: 26 (843 mothers) preterm studies and 30 (2299 mothers) term studies of breast milk composition. Preterm milk was higher in true protein than term milk, with differences up to 35% (0.7 g/dL) in colostrum, however, after postnatal day 3, most of the differences in true protein between preterm and term milk were within 0.2 g/dL, and the week 10-12 estimates suggested that term milk may be the same as preterm milk by that age. Colostrum was higher than mature milk for protein, and lower than mature milk for energy, fat and lactose for both preterm and term milk. Breast milk composition was relatively stable between 2 and 12 weeks. With milk maturation, there was a narrowing of the protein variance. Energy estimates differed whether measured or calculated, from -9 to 13%; true protein measurement vs. the total nitrogen estimates differed by 1 to 37%.

Conclusions: Although breast milk is highly variable between individuals, postnatal age and gestational stage (preterm versus term) were found to be important predictors of breast milk content. Energy content of breast milk calculated from the macronutrients provides poor estimates of measured energy, and protein estimated from the nitrogen over-estimates the protein milk content. When breast milk energy, macronutrient and mineral content cannot be directly measured the average values from these meta-analyses may provide useful estimates of mother's milk energy and nutrient content.

Figures

Figure 1
Figure 1
Flow diagram of the literature search process.
Figure 2
Figure 2
Measured Energy distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 3
Figure 3
Calculated Energy estimates distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 4
Figure 4
True Protein content distribution of preterm and term breast milk in by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 5
Figure 5
Fat content distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 6
Figure 6
Lactose content distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 7
Figure 7
Oligosaccharide content distribution of preterm and term breast milk oligosaccharide content in by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 8
Figure 8
Calcium content distribution of preterm and term breast milk calcium content in by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.
Figure 9
Figure 9
Phosphate content distribution of preterm and term breast milk by postnatal age over the first 12 weeks of lactation, weighted mean and 95% reference interval. Preterm milk …. Term milk ---- : mean +/- 2 standard deviations.

References

    1. American Academy of Pediatrics Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics. 2012;129(3):e827–e841.
    1. The Canadian Paediatric Society Nutrition Committee. Exclusive breastfeeding should continue to six months. Paediatrics Child Health. 2005;10(3):148.
    1. Kramer MS, Kakuma R. Optimal duration of exclusive breastfeeding. Cochrane Database Syst Rev. 2002;1:003517.
    1. Agostoni C, Buonocore G, Carnielli VP, De Curtis M, Darmaun D, Decsi T, Domellof M, Embleton ND, Fusch C, Genzel-Boroviczeny O, Goulet O, Kalhan SC, Kolacek S, Koletzko B, Lapillonne A, Mihatsch W, Moreno L, Neu J, Poindexter B, Puntis J, Putet G, Rigo J, Riskin A, Salle B, Sauer P, Shamir R, Szajewska H, Thureen P, Turck D, van Goudoever JB, Ziegler EE. ESPGHAN Committee on N. Enteral nutrient supply for preterm infants: commentary from the European Society of Paediatric Gastroenterology, Hepatology and Nutrition Committee on Nutrition. J Pediatric Gastroenterol Nutr. 2010;50(1):85–91. doi: 10.1097/MPG.0b013e3181adaee0.
    1. Committee N. Canadian Paediatric Society. Nutrient needs and feeding of premature infants. Can Med Assoc J. 1995;152(11):1765–1785.
    1. Saarela T, Kokkonen J, Koivisto M. Macronutrient and energy contents of human milk fractions during the first six months of lactation. Acta Paediatr. 2005;94(9):1176–1181. doi: 10.1080/08035250510036499.
    1. Khan S, Hepworth AR, Prime DK, Lai CT, Trengove NJ, Hartmann PE. Variation in fat, lactose, and protein composition in breast milk over 24 hours: associations with infant feeding patterns. J Hum Lact. 2013;29(1):81–89. doi: 10.1177/0890334412448841.
    1. Kociszewska-Najman B, Borek-Dzieciol B, Szpotanska-Sikorska M, Wilkos E, Pietrzak B, Wielgos M. The creamatocrit, fat and energy concentration in human milk produced by mothers of preterm and term infants. J Matern Fetal Neonatal Med. 2012;25(9):1599–1602. doi: 10.3109/14767058.2011.648239.
    1. Lubetzky R, Littner Y, Mimouni FB, Dollberg S, Mandel D. Circadian variations in fat content of expressed breast milk from mothers of preterm infants. J Am Coll Nutr. 2006;25(2):151–154. doi: 10.1080/07315724.2006.10719526.
    1. Nichols BL. Atwater and USDA nutrition research and service: a prologue of the past century. J Nutr. 1994;124(9 Suppl):1718S–1727S.
    1. Hibberd CM, Brooke OG, Carter ND, Haug M, Harzer G. Variation in the composition of breast milk during the first 5 weeks of lactation: implications for the feeding of preterm infants. Arch Dis Child. 1982;57(9):658–662. doi: 10.1136/adc.57.9.658.
    1. Lemons JA, Moye L, Hall D, Simmons M. Differences in the composition of preterm and term human milk during early lactation. Pediatr Res. 1982;16(2):113–117. doi: 10.1203/00006450-198202000-00007.
    1. Butte NF, Garza C, Johnson CA, Smith EO, Nichols BL. Longitudinal changes in milk composition of mothers delivering preterm and term infants. Early Hum Dev. 1984;9(2):153–162. doi: 10.1016/0378-3782(84)90096-3.
    1. Schanler RJ, Oh W. Composition of breast milk obtained from mothers of premature infants as compared to breast milk obtained from donors. J Pediatr. 1980;96(4):679–681. doi: 10.1016/S0022-3476(80)80738-4.
    1. Atkinson SA, Radde IC, Chance GW, Bryan MH, Anderson GH. Macro-mineral content of milk obtained during early lactation from mothers of premature infants. Early Hum Dev. 1980;4(1):5–14. doi: 10.1016/0378-3782(80)90003-1.
    1. United Nations. Composition of macro geographical (continental) regions, geographical sub-regions, and selected economic and other groupings. .
    1. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(15):2008–2012. doi: 10.1001/jama.283.15.2008.
    1. Anderson DM, Williams FH, Merkatz RB, Schulman PK, Kerr DS, Pittard WB. 3rd, Length of gestation and nutritional composition of human milk. Am J Clin Nutr. 1983;37(5):810–814.
    1. 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(4):617–624. doi: 10.1016/S0022-3476(81)80275-2.
    1. Corvaglia L, Battistini B, Paoletti V, Aceti A, Capretti MG, Faldella G. Near-infrared reflectance analysis to evaluate the nitrogen and fat content of human milk in neonatal intensive care units. Arch Dis Child Fetal Neonatal. 2008;93(5):F372–F375. doi: 10.1136/adc.2007.133280.
    1. Ferris AM, Dotts MA, Clark RM, Ezrin M, Jensen RG. Macronutrients in human milk at 2, 12, and 16 weeks postpartum. J Am Diet Assoc. 1988;88(6):694–697.
    1. Maas YG, Gerritsen J, Hart AA, Hadders-Algra M, Ruijter JM, Tamminga P, Mirmiran M, Spekreijse H. Development of macronutrient composition of very preterm human milk. Br J Nutr. 1998;80(1):35–40. doi: 10.1017/S0007114598001743.
    1. Yamawaki N, Yamada M, Kan-no T, Kojima T, Kaneko T, Yonekubo A. Macronutrient, mineral and trace element composition of breast milk from Japanese women. J Trace Elem Med Biol. 2005;19(2–3):171–181.
    1. Neville MC, Keller R, Seacat J, Lutes V, Neifert M, Casey C, Allen J, Archer P. Studies in human lactation: milk volumes in lactating women during the onset of lactation and full lactation. Am J Clin Nutr. 1988;48(6):1375–1386.
    1. Ballard O, Morrow AL. Human milk composition: nutrients and bioactive factors. Pediatr Clin North Am. 2013;60(1):49–74. doi: 10.1016/j.pcl.2012.10.002.
    1. Baumgartner G. The composition of breast milk. Kinderkrankenschwester. 2004;23(6):232–234.
    1. Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 2012;22(9):1147–1162. doi: 10.1093/glycob/cws074.
    1. Bokor S, Koletzko B, Decsi T. Systematic review of fatty acid composition of human milk from mothers of preterm compared to full-term infants. Ann Nutr Metab. 2007;51(6):550–556. doi: 10.1159/000114209.
    1. Cockburn F. Milk composition–the infant human diet. Proc Nutr Soc. 1983;42(3):361–373. doi: 10.1079/PNS19830044.
    1. Donovan SM. In: Nutrition in Pediatrics: Basic Science and Clinical Applications. 4. Duggan C, Watkins JB, Walker WA, editor. Hamilton, Ontario, Canada: BC Decker, Inc; Human milk: Nutritional properties; pp. 341–353. Chapter 30.
    1. Fomon SJ, Ziegler EE. Milk of the premature infant’s mother: interpretation of data. J Pediatr. 1978;93(1):164. doi: 10.1016/S0022-3476(78)80651-9.
    1. Picciano MF. Nutrient composition of human milk. Pediatr Clin North Am. 2001;48(1):53–67. doi: 10.1016/S0031-3955(05)70285-6.
    1. Raiha NC. Milk protein quantity and quality and protein requirements during development. Adv Pediatr. 1989;36:347–368.
    1. Reali A, Greco F, Fanaro S, Atzei A, Puddu M, Moi M, Fanos V. Fortification of maternal milk for very low birth weight (VLBW) pre-term neonates. Early Hum Dev. 2010;86(Suppl 1):33–36.
    1. Schanler RJ. Suitability of human milk for the low-birthweight infant. Clin Perinatol. 1995;22(1):207–222.
    1. Tudehope DI, Mitchell F, Cowley DM. A comparative study of a premature infant formula and preterm breast milk for low birthweight infants. Aust Paediatr J. 1986;22(3):199–205.
    1. Davies DP. How suitable is human milk for pre-term babies? Acta Paediatr Jpn. 1989;31(4):439–454. doi: 10.1111/j.1442-200X.1989.tb01331.x.
    1. Tudehope D, Vento M, Bhutta Z, Pachi P. Nutritional requirements and feeding recommendations for small for gestational age infants. J Pediatr. 2013;162(3 Suppl):S81–S89.
    1. Butte NF, Wong WW, Garza C, Stuff JE, Smith EO, Klein PD, Nichols BL. Energy requirements of breast-fed infants. J Am Coll Nutr. 1991;10(3):190–195. doi: 10.1080/07315724.1991.10718143.
    1. Aprile Mda M, Feferbaum R, Andreassa N, Leone C. Growth of very low birth weight infants fed with milk from a human milk bank selected according to the caloric and protein value. Clinics (Sao Paulo) 2010;65(8):751–756. doi: 10.1590/S1807-59322010000800002.
    1. Atinmo T, Omololu A. Trace element content of breastmilk from mothers of preterm infants in Nigeria. Early Hum Dev. 1982;6(3):309–313. doi: 10.1016/0378-3782(82)90125-6.
    1. Braga LP, Palhares DB. Effect of evaporation and pasteurization in the biochemical and immunological composition of human milk. J Pediatr (Rio J) 2007;83(1):59–63.
    1. Charpak N, Ruiz JG, KMC T. Breast milk composition in a cohort of pre-term infants’ mothers followed in an ambulatory programme in Colombia. Acta Paediatr. 2007;96(12):1755–1759. doi: 10.1111/j.1651-2227.2007.00521.x.
    1. Grumach AS, Jeronimo SE, Hage M, Carneiro-Sampaio MM. Nutritional factors in milk from Brazilian mothers delivering small for gestational age neonates. Rev Saude Publica. 1993;27(6):455–462. doi: 10.1590/S0034-89101993000600008.
    1. Gupta AP, Bhandari B, Gupta A, Goyal S. Mineral content of breast milk from north Indian mothers giving birth preterm and at term–implication for mineral nutrition of preterm infants. J Trop Pediatr. 1984;30(5):286–288. doi: 10.1093/tropej/30.5.286.
    1. Jitta JN, Musoke RN, Bwibo NO, Kioni J. Composition of early human milk of Kenyan mothers of preterm and term infants. East Afr Med J. 1986;63(11):693–698.
    1. Narang AP, Bains HS, Kansal S, Singh D. Serial composition of human milk in preterm and term mothers. Indian J Clin Biochem. 2006;21(1):89–94. doi: 10.1007/BF02913072.
    1. Trugo NM, Donangelo CM, Koury JC, Silva MI, Freitas LA. Concentration and distribution pattern of selected micronutrients in preterm and term milk from urban Brazilian mothers during early lactation. Eur J Clin Nutr. 1988;42(6):497–507.
    1. Anderson GH, Atkinson SA, Bryan MH. Energy and macronutrient content of human milk during early lactation from mothers giving birth prematurely and at term. Am J Clin Nutr. 1981;34(2):258–265.
    1. Bauer J, Gerss J. Longitudinal analysis of macronutrients and minerals in human milk produced by mothers of preterm infants. Clin Nutr. 2011;30(2):215–220. doi: 10.1016/j.clnu.2010.08.003.
    1. Bertino E, Coppa GV, Giuliani F, Coscia A, Gabrielli O, Sabatino G, Sgarrella M, Testa T, Zampini L, Fabris C. Effects of Holder pasteurization on human milk oligosaccharides. Int J Immunopathol Pharmacol. 2008;21(2):381–385.
    1. Boehm G, Springer S, Kirchner B. Consequences of the composition of breast milk for the nutrition of underweight newborn infants. I. Calcium and phosphorus. Kinderarztl Prax. 1988;56(9):429–435.
    1. Boehm G, Springer S, Lorenz I, Muller DM, Beyreiss K. Consequences of various protein contents in breast milk for the nutrition of the underweight newborn infant. Kinderarztl Prax. 1986;54(1):25–30.
    1. Boehm G, Springer S, Muller DM, Senger H. Consequences of the composition of breast milk for the nutrition of underweight newborn infants. II. Lipids and lactose. Kinderarztl Prax. 1989;57(9):443–450.
    1. Davis TA, Nguyen HV, Garcia-Bravo R, Fiorotto ML, Jackson EM, Lewis DS, Lee DR, Reeds PJ. Amino acid composition of human milk is not unique. J Nutr. 1994;124(7):1126–1132.
    1. Friel JK, Andrews WL, Jackson SE, Longerich HP, Mercer C, McDonald A, Dawson B, Sutradhar B. Elemental composition of human milk from mothers of premature and full-term infants during the first 3 months of lactation. Biol Trace Elem Res. 1999;67(3):225–247. doi: 10.1007/BF02784423.
    1. Galeotti F, Coppa GV, Zampini L, Maccari F, Galeazzi T, Padella L, Santoro L, Gabrielli O, Volpi N. On-line high-performance liquid chromatography-fluorescence detection-electrospray ionization-mass spectrometry profiling of human milk oligosaccharides derivatized with 2-aminoacridone. Anal Biochem. 2012;430(1):97–104. doi: 10.1016/j.ab.2012.07.027.
    1. Gross SJ, Geller J, Tomarelli RM. Composition of breast milk from mothers of preterm infants. Pediatrics. 1981;68(4):490–493.
    1. Simonin C, Ruegg M, Sidiropoulos D. Comparison of the fat content and fat globule size distribution of breast milk from mothers delivering term and preterm. Am J Clin Nutr. 1984;40(4):820–826.
    1. Bishara R, Dunn MS, Merko SE, Darling P. Nutrient composition of hindmilk produced by mothers of very low birth weight infants born at less than 28 weeks’ gestation. J Hum Lact. 2008;24(2):159–167. doi: 10.1177/0890334408316085.
    1. Bortolozo EA, Tiboni EB, Candido LM. Milk from human milk banks for low birthweight newborns: nutritional contents and supplementation. Rev Panam Salud Publica. 2004;16(3):199–205.
    1. de Halleux V, Rigo J. Variability in human milk composition: benefit of individualized fortification in very-low-birth-weight infants. Am J Clin Nutr. 2013;98(2):529S–535S. doi: 10.3945/ajcn.112.042689.
    1. Genzel-Boroviczeny O, Wahle J, Koletzko B. Fatty acid composition of human milk during the 1st month after term and preterm delivery. Eur J Pediatr. 1997;156(2):142–147. doi: 10.1007/s004310050573.
    1. Harzer G, Haug M, Dieterich I, Gentner PR. Changing patterns of human milk lipids in the course of the lactation and during the day. Am J Clin Nutr. 1983;37(4):612–621.
    1. Lonnerdal B, Woodhouse LR, Glazier C. Compartmentalization and quantitation of protein in human milk. J Nutr. 1987;117(8):1385–1395.
    1. Lucas A, Ewing G, Roberts SB, Coward WA. How much energy does the breast fed infant consume and expend? Br Med J (Clin Res Ed) 1987;295(6590):75–77. doi: 10.1136/bmj.295.6590.75.
    1. Mitoulas LR, Kent JC, Cox DB, Owens RA, Sherriff JL, Hartmann PE. Variation in fat, lactose and protein in human milk over 24 h and throughout the first year of lactation. Br J Nutr. 2002;88(1):29–37. doi: 10.1079/BJNBJN2002579.
    1. Molto-Puigmarti C, Castellote AI, Carbonell-Estrany X, Lopez-Sabater MC. Differences in fat content and fatty acid proportions among colostrum, transitional, and mature milk from women delivering very preterm, preterm, and term infants. Clin Nutr. 2011;30(1):116–123. doi: 10.1016/j.clnu.2010.07.013.
    1. Velona T, Abbiati L, Beretta B, Gaiaschi A, Flauto U, Tagliabue P, Galli CL, Restani P. Protein profiles in breast milk from mothers delivering term and preterm babies. Pediatr Res. 1999;45(5 Pt 1):658–663.
    1. Bitman J, Wood L, Hamosh M, Hamosh P, Mehta NR. Comparison of the lipid composition of breast milk from mothers of term and preterm infants. Am J Clin Nutr. 1983;38(2):300–312.
    1. de Figueiredo CS, Palhares DB, Melnikov P, Moura AJ, dos Santos SC. Zinc and copper concentrations in human preterm milk. Biol Trace Elem Res. 2010;136(1):1–7. doi: 10.1007/s12011-009-8515-6.
    1. Aquilio E, Spagnoli R, Seri S, Bottone G, Spennati G. Trace element content in human milk during lactation of preterm newborns. Biol Trace Elem Res. 1996;51(1):63–70. doi: 10.1007/BF02790148.
    1. Arslanoglu S, Moro GE, Ziegler EE. The Wapm Working Group On, Nutrition: Optimization of human milk fortification for preterm infants: new concepts and recommendations. J Perinat Med. 2010;38(3):233–238.
    1. Bao Y, Chen C, Newburg DS. Quantification of neutral human milk oligosaccharides by graphitic carbon high-performance liquid chromatography with tandem mass spectrometry. Anal Biochem. 2013;433(1):28–35. doi: 10.1016/j.ab.2012.10.003.
    1. Barros MD, Carneiro-Sompaio MM. Milk composition of low birth weight infants’ mothers. Acta Paediatr Scand. 1984;73(5):693–694. doi: 10.1111/j.1651-2227.1984.tb09997.x.
    1. Bishara R, Dunn MS, Merko SE, Darling P. Volume of foremilk, hindmilk, and total milk produced by mothers of very preterm infants born at less than 28 weeks of gestation. J Hum Lact. 2009;25(3):272–279. doi: 10.1177/0890334409334606.
    1. Boehm G, Senger H, Friedrich M, Muller DM, Beyreiss K. Protein supplementation of human milk for the nutrition of VLBW-infants: human milk protein vs. meat protein hydrolysate. Klin Padiatr. 1990;202(5):316–320. doi: 10.1055/s-2007-1025538.
    1. Chan GM. Human milk calcium and phosphate levels of mothers delivering term and preterm infants. J Pediatric Gastroenterol Nutr. 1982;1(2):201–205. doi: 10.1097/00005176-198201020-00008.
    1. Charlwood J, Tolson D, Dwek M, Camilleri P. A detailed analysis of neutral and acidic carbohydrates in human milk. Anal Biochem. 1999;273(2):261–277. doi: 10.1006/abio.1999.4232.
    1. De Curtis M, Brooke OG. Energy and nitrogen balances in very low birthweight infants. Arch Dis Child. 1987;62(8):830–832. doi: 10.1136/adc.62.8.830.
    1. Funkquist EL, 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. Ups J Med Sci. 2006;111(1):97–108. doi: 10.3109/2000-1967-021.
    1. Fusch G, Choi A, Rochow N, Fusch C. Quantification of lactose content in human and cow’s milk using UPLC-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2011;879(31):3759–3762. doi: 10.1016/j.jchromb.2011.09.053.
    1. Hill PD, Aldag JC, Chatterton RT, Zinaman M. Comparison of milk output between mothers of preterm and term infants: the first 6 weeks after birth. J Hum Lact. 2005;21(1):22–30. doi: 10.1177/0890334404272407.
    1. Lonnerdal B. Effects of milk and milk components on calcium, magnesium, and trace element absorption during infancy. Physiol Rev. 1997;77(3):643–669.
    1. Lucas A, Hudson GJ. Preterm milk as a source of protein for low birthweight infants. Arch Dis Child. 1984;59(9):831–836. doi: 10.1136/adc.59.9.831.
    1. Lyon AJ, McIntosh N. Calcium and phosphorus balance in extremely low birthweight infants in the first six weeks of life. Arch Dis Child. 1984;59(12):1145–1150. doi: 10.1136/adc.59.12.1145.
    1. Manz F. Protein quantity and quality in term and preterm infants: effects on urine creatinine and expression of amino acid excretion data. J Pediatr Gastroenterol Nutr. 1986;5(5):830–831. doi: 10.1097/00005176-198609000-00030.
    1. Mataloun MM, Leone CR. Human milk mineral intake and serum concentrations of calcium and phosphorus in newborn term infants: influence of intrauterine growth restriction. Acta Paediatr. 2000;89(9):1093–1097. doi: 10.1111/j.1651-2227.2000.tb03357.x.
    1. Meier PP, Engstrom JL, Murtaugh MA, Vasan U, Meier WA, Schanler RJ. Mothers’ milk feedings in the neonatal intensive care unit: accuracy of the creamatocrit technique. J Perinatol. 2002;22(8):646–649. doi: 10.1038/sj.jp.7210825.
    1. Meier PP, Engstrom JL, Zuleger JL, Motykowski JE, Vasan U, Meier WA, Hartmann PE, Williams TM. Accuracy of a user-friendly centrifuge for measuring creamatocrits on mothers’ milk in the clinical setting. Breastfeed Med. 2006;1(2):79–87. doi: 10.1089/bfm.2006.1.79.
    1. Moran JR, Vaughan R, Stroop S, Coy S, Johnston H, Greene HL. Concentrations and total daily output of micronutrients in breast milk of mothers delivering preterm: a longitudinal study. J Pediatric Gastroenterol Nutr. 1983;2(4):629–634. doi: 10.1097/00005176-198311000-00010.
    1. Ogechi AA, William O, Fidelia BT. Hindmilk and weight gain in preterm very low-birthweight infants. Pediatr Int. 2007;49(2):156–160. doi: 10.1111/j.1442-200X.2007.02336.x.
    1. O’Neill EF, Radmacher PG, Sparks B, Adamkin DH. Creamatocrit analysis of human milk overestimates fat and energy content when compared to a human milk analyzer using mid-infrared spectroscopy. J Pediatr Gastroenterol Nutr. 2013;56(5):569–572. doi: 10.1097/MPG.0b013e31828390e4.
    1. Pamblanco M, Ten A, Comin J. Proteins in preterm and term milk from mothers delivering appropriate or small-for-gestational age infants. Early Hum Dev. 1986;14(3–4):267–272.
    1. Polberger S, Lonnerdal B. Simple and rapid macronutrient analysis of human milk for individualized fortification: basis for improved nutritional management of very-low-birth-weight infants? J Pediatr Gastroenterol Nutr. 1993;17(3):283–290. doi: 10.1097/00005176-199310000-00009.
    1. Svenningsen NW, Lindroth M, Lindquist B. A comparative study of varying protein intake in low birthweight infant feeding. Acta Paediatr Scand Suppl. 1982;296:28–31.
    1. Unanian GS. Level of the trace elements copper, manganese, silicon, aluminum and magnesium in the colostrum, intermediate and mature milk of mothers of full-term and premature newborn infants. Zhurnal Eksper i Klinicheskoi Med. 1967;7(6):96–99.
    1. Wang CD, Chu PS, Mellen BG, Shenai JP. Creamatocrit and the nutrient composition of human milk. J Perinatol. 1999;19(5):343–346. doi: 10.1038/sj.jp.7200204.
    1. Zofkova I, Taborsky P, Bednar J, Nedvidkova J. Lack of stimulating effect on thyrotropic and lactotropic secretion during prolonged calcitriol administration. Exp Clin Endocrinol. 1992;99(1):54–56. doi: 10.1055/s-0029-1211133.
    1. Dai D, Tang Z. Copper, iron and zinc content of preterm and term human milk and cow’s milk. Hua Xi Yi Ke Da Xue Xue Bao. 1991;22(4):428–431. Hua-Hsi i Ko Ta Hsueh Hsueh Pao.
    1. Kalhoff H, Manz F, Kiwull P, Kiwull-Schone H. Food mineral composition and acid–base balance in preterm infants. Eur J Nutr. 2007;46(4):188–195. doi: 10.1007/s00394-007-0646-y.
    1. Kovacs A, Funke S, Marosvolgyi T, Burus I, Decsi T. Fatty acids in early human milk after preterm and full-term delivery. J Pediatric Gastroenterol Nutr. 2005;41(4):454–459. doi: 10.1097/01.mpg.0000176181.66390.54.
    1. Raiha N. Quantity and quality of milk protein intake: metabolic responses in the neonate. J Pediatr Gastroenterol Nutr. 1983;2(Suppl 1):S260–S265.
    1. Reichman B, Chessex P, Verellen G, Putet G, Smith JM, Heim T, Swyer PR. Dietary composition and macronutrient storage in preterm infants. Pediatrics. 1983;72(3):322–328.
    1. Sanchez-Hidalgo VM, Flores-Huerta S, Matute G, Serrano C, Urquieta B, Espinosa R. Whey protein/casein ratio and nonprotein nitrogen in preterm human milk during the first 10 days postpartum. J Pediatric Gastroenterol Nutr. 1998;26(1):64–69. doi: 10.1097/00005176-199801000-00011.
    1. Schanler RJ, Abrams SA. Postnatal attainment of intrauterine macromineral accretion rates in low birth weight infants fed fortified human milk. J Pediatr. 1995;126(3):441–447. doi: 10.1016/S0022-3476(95)70465-5.
    1. Wharton BA, Scott PH, Berger HM. Dietary protein for low birthweight babies. Sources and assessment of requirements. Acta Paediatr Scand Suppl. 1982;296:32–37.
    1. Butte NF, Wong WW, Hopkinson JM, Heinz CJ, Mehta NR, Smith EO. Energy requirements derived from total energy expenditure and energy deposition during the first 2 y of life. Am J Clin Nutr. 2000;72(6):1558–1569.
    1. 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(5):885–896.
    1. Michaelsen KF, Skafte L, Badsberg JH, Jorgensen M. Variation in macronutrients in human bank milk: influencing factors and implications for human milk banking. J Pediatric Gastroenterol Nutr. 1990;11(2):229–239. doi: 10.1097/00005176-199008000-00013.
    1. Stein H, Cohen D, Herman AA, Rissik J, Ellis U, Bolton K, Pettifor J, MacDougall L. Pooled pasteurized breast milk and untreated own mother’s milk in the feeding of very low birth weight babies: a randomized controlled trial. J Pediatr Gastroenterol Nutr. 1986;5(2):242–247. doi: 10.1097/00005176-198605020-00014.
    1. Stellwagen LM, Vaucher YE, Chan CS, Montminy TD, Kim JH. Pooling expressed breastmilk to provide a consistent feeding composition for premature infants. Breastfeed Med. 2013;8:205–209. doi: 10.1089/bfm.2012.0007.
    1. Wojcik KY, Rechtman DJ, Lee ML, Montoya A, Medo ET. Macronutrient analysis of a nationwide sample of donor breast milk. J Am Diet Assoc. 2009;109(1):137–140. doi: 10.1016/j.jada.2008.10.008.
    1. Butte NF, Wong WW, Hopkinson JM. Energy requirements of lactating women derived from doubly labeled water and milk energy output. J Nutr. 2001;131(1):53–58.
    1. Heinig MJ, Nommsen LA, Peerson JM, Lonnerdal 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(2):152–161.
    1. Stuff JE, Nichols BL. Nutrient intake and growth performance of older infants fed human milk. J Pediatr. 1989;115(6):959–968. doi: 10.1016/S0022-3476(89)80750-4.
    1. Brooke O, Carter N, Hibberd C, Wood C, Brown I. Protein concentrations in milk from mothers of preterm and term infants. Biochem Soc Trans. 1981;9(1):69–70.
    1. Leveque B. Composition of maternal milk in the first month of lactation and milk formulas for infants. Ann Pediatr (Paris) 1986;33(4):355–358.
    1. Sadurskis A, Kabir N, Wager J, Forsum E. Energy metabolism, body composition, and milk production in healthy Swedish women during lactation. Am J Clin Nutr. 1988;48(1):44–49.
    1. Lepage G, Collet S, Bougle D, Kien LC, Lepage D, Dallaire L, Darling P, Roy CC. The composition of preterm milk in relation to the degree of prematurity. Am J Clin Nutr. 1984;40(5):1042–1049.
    1. Thomas MR, Chan GM, Book LS. Comparison of macronutrient concentration of preterm human milk between two milk expression techniques and two techniques for quantitation of energy. J Pediatric Gastroenterol Nutr. 1986;5(4):597–601. doi: 10.1097/00005176-198607000-00016.
    1. Butte NF, Garza C, Stuff JE, Smith EO, Nichols BL. Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr. 1984;39(2):296–306.
    1. Butte NF, Wong WW, Ferlic L, Smith EO, Klein PD, Garza C. Energy expenditure and deposition of breast-fed and formula-fed infants during early infancy. Pediatr Res. 1990;28(6):631–640. doi: 10.1203/00006450-199012000-00019.
    1. Garza C, Butte NF. Energy concentration of human milk estimated from 24-h pools and various abbreviated sampling schemes. J Pediatr Gastroenterol Nutr. 1986;5(6):943–948. doi: 10.1097/00005176-198611000-00022.
    1. Motil KJ, Sheng HP, Montandon CM, Wong WW. Human milk protein does not limit growth of breast-fed infants. J Pediatr Gastroenterol Nutr. 1997;24(1):10–17. doi: 10.1097/00005176-199701000-00006.
    1. Wood CS, Isaacs PC, Jensen M, Hilton HG. Exclusively breast-fed infants: growth and caloric intake. Pediatr Nurs. 1988;14(2):117–124.
    1. Nommsen LA, Lovelady CA, Heinig MJ, Lonnerdal B, Dewey KG. Determinants of energy, protein, lipid, and lactose concentrations in human milk during the first 12 mo of lactation: the DARLING Study. Am J Clin Nutr. 1991;53(2):457–465.
    1. Beijers RJ, Graaf FV, Schaafsma A, Siemensma AD. Composition of premature breast-milk during lactation: constant digestible protein content (as in full term milk) Early Hum Dev. 1992;29(1–3):351–356.
    1. Itabashi K, Miura A, Okuyama K, Takeuchi T, Kitazawa S. Estimated nutritional intake based on the reference growth curves for extremely low birthweight infants. Pediatr Int. 1999;41(1):70–77. doi: 10.1046/j.1442-200x.1999.01020.x.
    1. Arnold J, Leslie G, Chen S. Protein, lactose and fat concentration of breast milk of mothers of term and premature neonates. Aust Paediatr J. 1987;23(5):299–300.
    1. Gross SJ, David RJ, Bauman L, Tomarelli RM. Nutritional composition of milk produced by mothers delivering preterm. J Pediatr. 1980;96(4):641–644. doi: 10.1016/S0022-3476(80)80729-3.
    1. Reinken L, Dockx F. Vitamin B6- and protein concentrations in breast milk from mothers of preterm and term infants. Klin Padiatr. 1985;197(1):40–43. doi: 10.1055/s-2008-1033924.
    1. Faerk J, Skafte L, Petersen S, Peitersen B, Michaelsen KF. Macronutrients in milk from mothers delivering preterm. Adv Exp Med Biol. 2001;501:409–413. doi: 10.1007/978-1-4615-1371-1_51.
    1. Hosoi S, Honma K, Daimatsu T, Kiyokawa M, Aikawa T, Watanabe S. Lower energy content of human milk than calculated using conversion factors. Pediatr Int. 2005;47(1):7–9. doi: 10.1111/j.1442-200x.2005.02017.x.
    1. Cregan MD, De Mello TR, Kershaw D, McDougall K, Hartmann PE. Initiation of lactation in women after preterm delivery. Acta Obstet Gynecol Scand. 2002;81(9):870–877. doi: 10.1034/j.1600-0412.2002.810913.x.
    1. Montagne P, Cuilliere ML, Mole C, Bene MC, Faure G. Immunological and nutritional composition of human milk in relation to prematurity and mother’s parity during the first 2 weeks of lactation. J Pediatric Gastroenterol Nutr. 1999;29(1):75–80. doi: 10.1097/00005176-199907000-00018.
    1. Britton JR. Milk protein quality in mothers delivering prematurely: implications for infants in the intensive care unit nursery setting. J Pediatric Gastroenterol Nutr. 1986;5(1):116–121. doi: 10.1097/00005176-198601000-00021.
    1. Sanchez-Pozo A, Lopez J, Pita ML, Izquierdo A, Guerrero E, Sanchez-Medina F, Martinez Valverde A, Gil A. Changes in the protein fractions of human milk during lactation. Ann Nutr Metab. 1986;30(1):15–20.
    1. Michaelsen KF, Larsen PS, Thomsen BL, Samuelson G. The Copenhagen cohort study on infant nutrition and growth: duration of breast feeding and influencing factors. Acta Paediatr. 1994;83(6):565–571.
    1. Coppa GV, Gabrielli O, Pierani P, Catassi C, Carlucci A, Giorgi PL. Changes in carbohydrate composition in human milk over 4 months of lactation. Pediatrics. 1993;91(3):637–641.
    1. Coppa GV, Pierani P, Zampini L, Gabrielli O, Carlucci A, Catassi C, Giorgi PL. Lactose, oligosaccharide and monosaccharide content of milk from mothers delivering preterm newborns over the first month of lactation. Minerva Pediatr. 1997;49(10):471–475.
    1. Ehrenkranz RA, Ackerman BA, Nelli CM. Total lipid content and fatty acid composition of preterm human milk. J Pediatric Gastroenterol Nutr. 1984;3(5):755–758. doi: 10.1097/00005176-198411000-00021.
    1. Gabrielli O, Zampini L, Galeazzi T, Padella L, Santoro L, Peila C, Giuliani F, Bertino E, Fabris C, Coppa GV. Preterm milk oligosaccharides during the first month of lactation. Pediatrics. 2011;128(6):e1520–e1531. doi: 10.1542/peds.2011-1206.
    1. Guerrini P, Bosi G, Chierici R, Fabbri A. Human milk: relationship of fat content with gestational age. Early Hum Dev. 1981;5(2):187–194. doi: 10.1016/0378-3782(81)90051-7.
    1. Hurgoiu V, Caseanu E. Mineral composition of the milk of mothers of premature infants during early lactation. Pediatrie. 1986;41(6):469–473.
    1. Sann L, Bienvenu F, Lahet C, Bienvenu J, Bethenod M. Comparison of the composition of breast milk from mothers of term and preterm infants. Acta Paediatr Scand. 1981;70(1):115–116. doi: 10.1111/j.1651-2227.1981.tb07182.x.
    1. Viverge D, Grimmonprez L, Cassanas G, Bardet L, Solere M. Variations in oligosaccharides and lactose in human milk during the first week of lactation. J Pediatr Gastroenterol Nutr. 1990;11(3):361–364. doi: 10.1097/00005176-199010000-00013.
    1. Valentine CJ, Fernandez S, Rogers LK, Gulati P, Hayes J, Lore P, Puthoff T, Dumm M, Jones A, Collins K, Curtiss J, Hutson K, Clark K, Welty SE. Early amino-acid administration improves preterm infant weight. J Perinatol. 2009;29(6):428–432. doi: 10.1038/jp.2009.51.
    1. Donovan SM, Atkinson SA, Whyte RK, Lonnerdal B. Partition of nitrogen intake and excretion in low-birth-weight infants. Am J Dis Child. 1989;143(12):1485–1491.

Source: PubMed

3
Abonnieren