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Meta-Analysis
. 2020 Sep 23;9(9):CD000433.
doi: 10.1002/14651858.CD000433.pub3.

Protein supplementation of human milk for promoting growth in preterm infants

Emma A Amissah  1 , Julie Brown  2 , Jane E Harding  1
Affiliations
Meta-Analysis

Protein supplementation of human milk for promoting growth in preterm infants

Emma A Amissah et al. Cochrane Database Syst Rev. .

Abstract

Background: Preterm infants require high protein intake to achieve adequate growth and development. Although breast milk feeding has many benefits for this population, the protein content is highly variable, and inadequate to support rapid infant growth. This is a 2020 update of a Cochrane Review first published in 1999.

Objectives: To determine whether protein-supplemented human milk compared with unsupplemented human milk, fed to preterm infants, improves growth, body composition, cardio-metabolic, and neurodevelopmental outcomes, without significant adverse effects.

Search methods: We used the standard search strategy of Cochrane Neonatal to search Cochrane Central Register of Controlled Trials (CENTRAL 2019, Issue 8) in the Cochrane Library and MEDLINE via PubMed on 23 August 2019. We also searched clinical trials databases and the reference lists of retrieved articles for randomised controlled trials and quasi-randomised trials.

Selection criteria: Published and unpublished RCTs were eligible if they used random or quasi-random methods to allocate hospitalised preterm infants who were being fed human milk, to additional protein supplementation or no supplementation.

Data collection and analysis: Two review authors independently abstracted data, assessed risk of bias and the quality of evidence at the outcome level, using GRADE methodology. We performed meta-analyses, using risk ratio (RR) for dichotomous data, and mean difference (MD) for continuous data, with their respective 95% confidence intervals (CIs). We used a fixed-effect model and had planned to explore potential causes of heterogeneity via subgroup or sensitivity analyses.

Main results: We included six RCTs, involving 204 preterm infants. The risk of bias for most methodological domains was unclear as there was insufficient detail reported. Low-quality evidence showed that protein supplementation of human milk may increase in-hospital rates of growth in weight (MD 3.82 g/kg/day, 95% CI 2.94 to 4.7; five RCTs, 101 infants; I² = 73%), length (MD 0.12 cm/wk, 95% CI 0.07 to 0.17; four RCTs, 68 infants; I² = 89%), and head circumference (MD 0.06 cm/wk, 95% CI 0.01 to 0.12; four RCTs, 68 infants; I² = 84%). Protein supplementation may lead to longer hospital stays (MD 18.5 days, 95% CI 4.39 to 32.61; one RCT, 20 infants; very low-quality evidence). Very low quality evidence means that the effect of protein supplementation on the risk of feeding intolerance (RR 2.70, 95% CI 0.13 to 58.24; one RCT, 17 infants), or necrotizing enterocolitis (RR 1.11, 95% CI 0.07 to 17.12; one RCT, 76 infants) remains uncertain. No data were available about the effects of protein supplementation on neurodevelopmental outcomes.

Authors' conclusions: Low-quality evidence showed that protein supplementation of human milk, fed to preterm infants, increased short-term growth. However, the small sample sizes, low precision, and very low-quality evidence regarding duration of hospital stay, feeding intolerance, and necrotising enterocolitis precluded any conclusions about these outcomes. There were no data on outcomes after hospital discharge. Our findings may not be generalisable to low-resource settings, as none of the included studies were conducted in these settings. Since protein supplementation of human milk is now usually done as a component of multi-nutrient fortifiers, future studies should compare different amounts of protein in multi-component fortifiers, and be designed to determine the effects on duration of hospital stay and safety, as well as on long-term growth, body composition, cardio-metabolic, and neurodevelopmental outcomes.

Trial registration: ClinicalTrials.gov NCT01487928 NCT01103219.

PubMed Disclaimer

Conflict of interest statement

EA receives a scholarship in the form of a stipend from the University of Auckland as a PhD student.

JB is currently employed by a medical writing company. The preparation of this review took place prior to this employment and her current work is not related to the topic of this review.

JH has partial salary support from research grants from the Health Research Council of New Zealand. The Council has no role in the production of this review. An undirected research grant is pending from Biomed Ltd, Auckland, New Zealand. This company makes dextrose gel.

The methods section of this review is based on a standard template used by Cochrane Neonatal.

Core editorial and administrative support for the 2020 update of this review has been provided by a grant from The Gerber Foundation. The Gerber Foundation is a separately endowed, private foundation, independent from the Gerber Products Company. The grantor has no input on the content of the review or the editorial process.

Figures

1
1
Study flow diagram: review update
2
2
Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies
3
3
Risk of bias summary: review authors' judgements about each risk of bias item for each included study
1.1
1.1. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 1: Growth: weight
1.2
1.2. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 2: Growth: length
1.3
1.3. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 3: Growth: head circumference
1.4
1.4. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 4: Growth: skin fold thickness
1.5
1.5. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 5: Duration of hospital stay (days)
1.6
1.6. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 6: Feeding intolerance
1.7
1.7. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 7: Necrotising enterocolitis
1.8
1.8. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 8: Blood urea (mmol/L)
1.9
1.9. Analysis
Comparison 1: Protein supplementation versus no supplementation, Outcome 9: Serum albumin (g/L)
See this image and copyright information in PMC

Update of

References

References to studies included in this review

Boehm 1988a {published data only}
    1. Boehm G, Müller DM, Beyreiss K, Räihä NC. Evidence of functional immaturity of the ornithine-urea cycle in very-low-birthweight infants. Biology of the Neonate 1988;54(3):121-5. [DOI: 10.1159/000242842] [PMID: ] - PubMed
Faerk 2001 {published data only}
    1. Faerk J, Petersen S, Peitersen B, Michaelsen KF. Diet, growth, and bone mineralization in premature infants. Advances in Experimental Medicine and Biology 2001;501:479-83. [PMID: ] - PubMed
    1. Faerk J, Petersen S, Peitersen B, Michaelsen KF. Diet and bone mineral content at term in premature infants. Pediatric Research 2000;47(1):148-56. [PMID: ] - PubMed
Greer 1986 {published data only}
    1. Greer FR, McCormick A, Loker J. Increased urinary excretion of inorganic sulfate in premature infants fed bovine milk protein. Journal of Pediatrics 1986;109(4):692-7. [PMID: ] - PubMed
    1. Greer FR, McCormick A. Improved bone mineralization and growth in premature infants fed fortified own mother’s milk. Journal of Pediatrics 1988;112(6):961-9; Erratum in: Journal of Pediatrics 1988; 113(6):1118. [PMID: ] - PubMed
Polberger 1989 {published and unpublished data}
    1. Polberger SK, Axelsson IA, Räihä NC. Growth of very low birth weight infants on varying amounts of human milk protein. Pediatric Research 1989;25(4):414-9. [DOI: 10.1203/00006450-198904000-00022] [PMID: 2726319 ] - DOI - PubMed
    1. Polberger SK, Axelsson IE, Räihä NC. Amino acid concentrations in plasma and urine in very low birth weight infants fed protein-unenriched or human milk protein-enriched human milk. Pediatrics 1990;86(6):909-15. [PMID: ] - PubMed
    1. Polberger SK, Fex GA, Axelsson IE, Räihä NC. Eleven plasma proteins as indicators of protein nutritional status in very low birth weight infants. Pediatrics 1990;86(6):916-21. [PMID: ] - PubMed
Putet 1987 {published and unpublished data}
    1. Putet G, Rigo J, Salle B, Senterre J. Supplementation of pooled human milk with casein hydrolysate: energy and nitrogen balance and weight gain composition in very low birth weight infants. Pediatric Research 1987;21(5):458-61. [DOI: 10.1203/00006450-198705000-00007] [PMID: ] - DOI - PubMed
Rönnholm 1982 {published data only}
    1. Rönnholm KA, Perheentupa J, Siimes MA. Supplementation with human milk protein improves growth of small premature infants fed human milk. Pediatrics 1986;77(5):649-53. [PMID: ] - PubMed
    1. Rönnholm KA, Siimes MA. Haemoglobin concentration depends on protein intake in small preterm infants fed human milk. Archives of Disease in Childhood 1985;60(2):99-104. [PMID: ] - PMC - PubMed
    1. Rönnholm KA, Simell O, Siimes MA. Human milk protein and medium-chain triglyceride oil supplementation of human milk: plasma amino acids in very low-birth-weight infants. Pediatrics 1984;74(5):792-9. [PMID: ] - PubMed
    1. Rönnholm KA, Sipila O, Siimes MA. Human milk protein supplementation for the prevention of hypoproteinemia without metabolic imbalance in breast milk-fed, very low-birth-weight infants. Journal of Pediatrics 1982;101(2):243-7. [PMID: ] - PubMed

References to studies excluded from this review

Abrams 2014 {published data only}
    1. Abrams SA, Schanler RJ, Lee M, Rechtman DJ. Greater mortality and morbidity in extremely preterm infants fed a diet containing cow milk protein products. Breastfeeding Medicine 2014;9(6):281-5. [DOI: 10.1089/bfm.2014.0024] [PMID: ] - DOI - PMC - PubMed
Barrington 2016 {published data only}
    1. Barrington KJ, Assaad MA, Janvier A. The Lacuna Trial: a double-blind randomized controlled pilot trial of lactoferrin supplementation in the very preterm infant. Journal of Perinatology 2016;36(8):666-9. [DOI: 10.1038/jp.2016.24] [PMID: ] - DOI - PubMed
Berseth 2012 {published data only}
    1. Berseth C, Harris C, Mitmesser S. Weight gain in very premature human milk fed infants Is significantly related to protein and non-protein intake. In: Pediatric Academic Societies Annual Meeting; 2012 April 28 - May 1; Boston MA, United States. 2012.
Bhat 2001 {published data only}
    1. Bhat BA, Gupta B. Effects of human milk fortification on morbidity factors in very low birth weight infants. Annals of Saudi Medicine 2001;21(5-6):292-5. [PMID: ] - PubMed
    1. Bhat BA, Gupta B. Effects of human milk fortification on morbidity factors in very low birth weight infants. Annals of Saudi Medicine 2003;23(1-2):28-31. [PMID: ] - PubMed
Bishara 2017 {published data only}
    1. Bishara R, Ng D, Asbury M, Ng E, Unger S, Gibbins S, et al. Nutrient intake and growth of infants enrolled in the donor milk for improved neurodevelopmental outcomes (GTA-DoMINO) trial: comparison to clinical targets. FASEB Journal 2017;31(1 Suppl 1):lb295.
Boehm 1988b {published data only}
    1. Boehm G, Senger H, Muller D, Beyreiss K, Raiha NC. Metabolic differences between AGA- and SGA-infants of very low birthweight. II. Relationship to protein intake. Acta Paediatrica Scandinavica Sep 1988;77(5):642-6. [PMID: ] - PubMed
Ditzenberger 2013 {published data only}
    1. Ditzenberger GR, Wallen LD, Phelan L, Escoe S, Collins SD. Supplemental protein and postnatal growth of very low birth weight infants: a randomized trial. Journal of Neonatal-perinatal Medicine 2013;6(4):285-94. [DOI: 10.3233/NPM-1371213] [PMID: ] - DOI - PubMed
Gathwala 2012 {published data only}
    1. Gathwala G, Shaw CK, Shaw P, Batra R. Effect of fortification of breast milk on the growth of preterm neonates. Eastern Journal of Medicine 2012;17(1):30-5.
Hair 2014 {published data only}
    1. Hair AB, Blanco CL, Moreira AG, Hawthorne KM, Lee ML, Rechtman DJ, et al. Randomized trial of human milk cream as a supplement to standard fortification of an exclusive human milk-based diet in infants 750-1250 g birth weight. Journal of Pediatrics 2014;165(5):915-20. [DOI: 10.1016/j.jpeds.2014.07.005] [PMID: ] - DOI - PubMed
Hayashi 1994 {published data only}
    1. Hayashi T, Takeuchi T, Itabashi K, Okuyama K. Nutrient balance, metabolic response, and bone growth in VLBW infants fed fortified human milk. Early Human Development 1994;39(1):27-36. [PMID: ] - PubMed
Hill 1997 {published data only}
    1. Hill R. Abstracts of podium presentations. Infants and children... proceedings of the Communicating Nursing Research Conference and WIN Assembly held May 1-3, 1997 in Portland, Oregon. Communicating Nursing Research 1997;30:153-6.
Kashaki 2018 {published data only}
    1. Kashaki M, Mazouri A, Bordhar A, Saboute M, Behnamfar Z, Talebi A. Effect of protein supplementation on the growth of infants weighing less than 1,000 grams hospitalized on the neonatal intensive care unit of Akbar Abadi Hospital in Tehran, Iran (2015-2016). Iranian Journal of Neonatology 2018;9(3):49-56. [DOI: 10.22038/ijn.2019.27558.1368] - DOI
Modanlou 1986 {published data only}
    1. Modanlou HD, Lim MO, Hansen JW, Sickles V. Growth, biochemical status, and mineral metabolism in very-low-birth-weight infants receiving fortified preterm human milk. Journal of Pediatric Gastroenterology and Nutrition 1986;5(5):762-7. [PMID: ] - PubMed
Moltu 2013 {published data only}
    1. Moltu SJ, Strommen K, Blakstad EW, Almaas AN, Westerberg AC, Braekke K, et al. Enhanced feeding in very-low-birth-weight infants may cause electrolyte disturbances and septicemia--a randomized, controlled trial. Clinical Nutrition (Edinburgh, Scotland) 2013;32(2):207-12. [DOI: 10.1016/j.clnu.2012.09.004] [PMID: ] - DOI - PubMed
Polberger 1997 {published data only}
    1. Polberger S, Raiha NC, Juvonen P, Moro G, Minoli I. A new human milk fortifier (HMF). A comparison of growth and metabolic indices with human milk protein (HMP) fortification in preterm infants. Pediatric Research 1997;41(4 Pt 2):238A.
Valman 1971 {published data only}
    1. Valman HB, Brown RJ, Palmer T, Oberholzer VG, Levin B. Protein intake and plasma amino-acids of infants of low birth weight. BMJ 1971;4(5790):789-91. [PMID: ] - PMC - PubMed

Additional references

AAP 2012
    1. Section on Breastfeeding. Breastfeeding and the use of human milk. Pediatrics 2012;129(3):e827-41. [DOI: 10.1542/peds.2011-3552] [PMID: ] - DOI - PubMed
AAP Committee on Nutrition 1985
    1. American Academy of Pediatrics Committee on Nutrition. Nutritional needs of low-birth-weight infants. Pediatrics 1985;75(5):976-86. [PMID: ] - PubMed
Agostoni 2010
    1. Agostoni C, Buonocore G, Carnielli VP, De Curtis M, Darmaun D, Decsi T, et al, ESPGHAN Committee on Nutrition. Enteral nutrient supply for preterm infants: commentary from the European Society of Paediatric Gastroenterology, Hepatology and Nutrition Committee on Nutrition. Journal of Pediatric Gastroenterology and Nutrition 2010;50(1):85-91. [DOI: 10.1097/MPG.0b013e3181adaee0] [PMID: ] - DOI - PubMed
Bertino 2012
    1. Bertino E, Nicola PD, Giuliani F, Peila C, Cester E, Vassia C, et al. Benefits of human milk in preterm infant feeding. Journal of Pediatric and Neonatal Individualized Medicine (JPNIM) 2012;1(1):19-24.
Boyd 2007
    1. Boyd CA, Quigley MA, Brocklehurst P. Donor breast milk versus infant formula for preterm infants: systematic review and meta-analysis. Archives of Disease in Childhood. Fetal and Neonatal Edition 2007;92(3):F169-75. [DOI: 10.1136/adc.2005.089490] [PMID: ] - DOI - PMC - PubMed
Brooke 1987
    1. Brooke OG, Onubogu O, Heath R, Carter ND. Human milk and preterm formula compared for effects on growth and metabolism. Archives of Disease in Childhood 1987;62(9):917-23. [PMID: ] - PMC - PubMed
Brown 2016
    1. Brown JV, Embleton ND, Harding JE, McGuire W. Multi-nutrient fortification of human milk for preterm infants. Cochrane Database of Systematic Reviews 2016, Issue 5. Art. No: CD000343. [DOI: 10.1002/14651858.CD000343.pub3] - DOI - PubMed
Chiesa 2008
    1. Chiesa C, Osborn JF, Haass C, Natale F, Spinelli M, Scapillati E, et al. Ghrelin, leptin, IGF-1, IGFBP-3, and insulin concentrations at birth: is there a relationship with fetal growth and neonatal anthropometry? Clinical Chemistry 2008;54(3):550-8. [DOI: 10.1373/clinchem.2007.095299] [PMID: ] - DOI - PubMed
Cibulskis 2015
    1. Cibulskis CC, Armbrecht ES. Association of metabolic acidosis with bovine milk-based human milk fortifiers. Journal of Perinatology 2015;35(2):115-9. [DOI: 10.1038/jp.2014.143] [PMID: ] - DOI - PubMed
Claas 2011
    1. Claas MJ, Vries LS, Koopman C, Uniken VM, Eijsermans MJ, Bruinse HW, et al. Postnatal growth of preterm born children ≤ 750 g at birth. Early Human Development 2011;87(7):495-507. [DOI: 10.1016/j.earlhumdev.2011.04.009] [PMID: ] - DOI - PubMed
Clemmons 2006
    1. Clemmons DR. Clinical utility of measurements of insulin-like growth factor 1. Nature Clinical Practice. Endocrinology & Metabolism 2006;2(8):436-46. [DOI: 10.1038/ncpendmet0244] [PMID: ] - DOI - PubMed
Covidence [Computer program]
    1. Veritas Health Innovation Covidence. Version accessed 1 September 2017. Melbourne, Australia: Veritas Health Innovation, 2015. Available at www.covidence.org.
D'Netto 2000
    1. D'Netto MA, Herson VC, Hussain N, Ricci A, Brown RT, Hyams JS, et al. Allergic gastroenteropathy in preterm infants. Journal of Pediatrics 2000;137(4):480-6. [DOI: 10.1067/mpd.2000.108563] [PMID: ] - DOI - PubMed
Di Natale 2011
    1. Di Natale C, Coclite E, Di Ventura L, Di Fabio S. Fortification of maternal milk for preterm infants. Journal of Maternal-fetal & Neonatal Medicine 2011;24(Suppl 1):41-3. [DOI: 10.3109/14767058.2011.607569] [PMID: ] - DOI - PubMed
Di Natale 2013
    1. Di Natale C, Di Fabio S. Fortification of maternal milk. Journal of Pediatric and Neonatal Individualized Medicine (JPNIM) 2013;2(2):e020224.
Ehrenkranz 2006
    1. Ehrenkranz RA, Dusick AM, Vohr BR, Wright LL, Wrage LA, Poole WK. Growth in the neonatal intensive care unit influences neurodevelopmental and growth outcomes of extremely low birth weight infants. Pediatrics 2006;117(4):1253-61. [DOI: 10.1542/peds.2005-1368] [PMID: ] - DOI - PubMed
Ehrenkranz 2010
    1. Ehrenkranz RA. Early nutritional support and outcomes in ELBW infants. Early Human Development 2010;86(Suppl 1):21-5. [DOI: 10.1016/j.earlhumdev.2010.01.014] [PMID: ] - DOI - PubMed
Embleton 2001
    1. Embleton NE, Pang N, Cooke RJ. Postnatal malnutrition and growth retardation: an inevitable consequence of current recommendations in preterm infants? Pediatrics 2001;107(2):270-3. [PMID: ] - PubMed
Freitas 2016
    1. Freitas BA, Priore SE, Lima LM, Franceschini SC. Extrauterine growth restriction: universal problem among premature infants [Restrição de crescimento extrauterino: problema universal entre os prematuros]. Revista de Nutrição, 2016;29(1):53-64.
Ghods 2011
    1. Ghods E, Kreissl A, Brandstetter S, Fuiko R, Widhalm K. Head circumference catch-up growth among preterm very low birth weight infants: effect on neurodevelopmental outcome. Journal of Perinatal Medicine 2011;39(5):579-86. [DOI: 10.1515/JPM.2011.049] [PMID: 21740330 ] - DOI - PubMed
GRADEpro GDT [Computer program]
    1. GRADE Working Group, McMaster University GRADEpro GDT. Version accessed 1 September 2017. Hamilton (ON): GRADE Working Group, McMaster University, 2014. Available at gradepro.org.
Hansen‐Pupp 2011
    1. Hansen-Pupp I, Löfqvist C, Polberger S, Niklasson A, Fellman V, Hellström A, et al. Influence of insulin-like growth factor I and nutrition during phases of postnatal growth in very preterm infants. Pediatric Research 2011;69(5 Pt 1):448-53. [DOI: 10.1203/PDR.0b013e3182115000] [PMID: ] - DOI - PubMed
Hansen‐Pupp 2013
    1. Hansen-Pupp I, Hövel H, Löfqvist C, Hellström-Westas L, Fellman V, Hüppi P, et al. Circulatory insulin-like growth factor-I and brain volumes in relation to neurodevelopmental outcome in very preterm infants. Pediatric Research 2013;74(5):564-9. [DOI: 10.1038/pr.2013.135] [PMID: ] - DOI - PubMed
Hay 2009
    1. Hay WW. Optimizing protein intake in preterm infants. Journal of Perinatology 2009;29(7):465-6. [DOI: 10.1038/jp.2009.53] [PMID: ] - DOI - PMC - PubMed
Hay 2010
    1. Hay WW, Thureen P. Protein for preterm infants: how much is needed? How much is enough? How much is too much? Pediatrics and Neonatology 2010;51(4):198-207. [DOI: 10.1016/S1875-9572(10)60039-3] [PMID: ] - DOI - PubMed
Hellström 2016
    1. Hellström A, Ley D, Hansen-Pupp I, Hallberg B, Löfqvist C, Marter L, et al. Insulin-like growth factor 1 has multisystem effects on foetal and preterm infant development. Acta Paediatrica 2016;105(6):576-86. [DOI: 10.1111/apa.13350] [PMID: ] - DOI - PMC - PubMed
Higgins 2017
    1. Higgins JPT, Green S, editor(s). Cochrane Handbook for Systematic Reviews of Interventions Version 5.2.0 (updated June 2017). The Cochrane Collaboration, 2017. Available from https://training.cochrane.org/handbook.
Kalhoff 1993
    1. Kalhoff H, Manz F, Diekmann L, Kunz C, Stock GJ, Weisser F. Decreased growth rate of low-birth-weight infants with prolonged maximum renal acid stimulation. Acta Paediatrica 1993;82(6-7):522-7. [PMID: ] - PubMed
Kalhoff 2001
    1. Kalhoff H, Manz F. Nutrition, acid-base status and growth in early childhood. European Journal of Nutrition 2001;40(5):221-30. [PMID: ] - PubMed
Kim 2016
    1. Kim MJ. Enteral nutrition for optimal growth in preterm infants. Korean Journal of Pediatrics 2016;59(12):466-70. [DOI: 10.3345/kjp.2016.59.12.466] [PMID: ] - DOI - PMC - PubMed
Koletzko 2005
    1. Koletzko B, Goulet O, Hunt J, Krohn K, Shamir R, Parenteral Nutrition Guidelines Working Group, European Society for Clinical Nutrition and Metabolism, European Society of Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN), European Society of Paediatric Research (ESPR). 1. Guidelines on Paediatric Parenteral Nutrition of the European Society of Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) and the European Society for Clinical Nutrition and Metabolism (ESPEN), Supported by the European Society of Paediatric Research (ESPR). Journal of Pediatric Gastroenterology and Nutrition 2005;41(Suppl 2):S1-87. [PMID: ] - PubMed
Kuschel 2000a
    1. Kuschel CA, Harding JE. Protein supplementation of human milk for promoting growth in preterm infants. Cochrane Database of Systematic Reviews 2000, Issue 2. Art. No: CD000433. [DOI: 10.1002/14651858.CD000433] - DOI - PubMed
Kuschel 2000b
    1. Kuschel CA, Harding JE, Kumaran VS. Fat supplementation of human milk for promoting growth in preterm infants. Cochrane Database of Systematic Reviews 2000, Issue 2. Art. No: CD000341. [DOI: 10.1002/14651858.CD000341] - DOI - PubMed
Lapillonne 2013
    1. Lapillonne A, Griffin IJ. Feeding preterm infants today for later metabolic and cardiovascular outcomes. Journal of Pediatrics 2013;162(3 Suppl):S7-16. [DOI: 10.1016/j.jpeds.2012.11.048] [PMID: ] - DOI - PubMed
Lo 2002
    1. Lo HC, Tsao LY, Hsu WY, Chen HN, Yu WK, Chi CY. Relation of cord serum levels of growth hormone, insulin-like growth factors, insulin-like growth factor binding proteins, leptin, and interleukin-6 with birth weight, birth length, and head circumference in term and preterm neonates. Nutrition 2002;18(7-8):604-8. [PMID: ] - PubMed
Manz 1997
    1. Manz F, Kalhoff H, Remer T. Renal acid excretion in early infancy. Pediatric Nephrology (Berlin, Germany) 1997;11(2):231-43. [DOI: ] - PubMed
Okamoto 2007
    1. Okamoto T, Shirai M, Kokubo M, Takahashi S, Kajino M, Takase M, et al. Human milk reduces the risk of retinal detachment in extremely low-birthweight infants. Pediatrics International 2007;49(6):894-7. [DOI: 10.1111/j.1442-200X.2007.02483.x] [PMID: ] - DOI - PubMed
Reich 2010
    1. Reich F, König R, Wiese W, Klein G. Prevalence of Cronobacter spp. in a powdered infant formula processing environment. International Journal of Food Microbiology 2010;140(2-3):214-7. [DOI: 10.1016/j.ijfoodmicro.2010.03.031] [PMID: ] - DOI - PubMed
Review Manager 2014 [Computer program]
    1. Nordic Cochrane Centre, The Cochrane Collaboration Review Manager 5 (RevMan 5). Version 5.3. Copenhagen: Nordic Cochrane Centre, The Cochrane Collaboration, 2014.
Ronholm 1986
    1. Rönnholm KA, Perheentupa J, Siimes MA. Supplementation with human milk protein improves growth of small premature infants fed human milk. Pediatrics 1986;77(5):649-53. [PMID: ] - PubMed
Schanler 1999
    1. Schanler RJ, Shulman RJ, Lau C. Feeding strategies for premature infants: beneficial outcomes of feeding fortified human milk versus preterm formula. Pediatrics 1999;103(6 Pt 1):1150-7. [PMID: ] - PubMed
Schanler 2005
    1. 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(2):400-6. [DOI: 10.1542/peds.2004-1974] [PMID: ] - DOI - PubMed
Schünemann 2013
    1. Schünemann H, Brożek J, Guyatt G, Oxman A, editor(s). Handbook for grading the quality of evidence and the strength of recommendations using the GRADE approach (updated October 2013). GRADE Working Group, 2013. Available from gdt.guidelinedevelopment.org/app/handbook/handbook.html.
Sisk 2007
    1. Sisk PM, Lovelady CA, Dillard RG, Gruber KJ, O'Shea TM. Early human milk feeding is associated with a lower risk of necrotizing enterocolitis in very low birth weight infants. Journal of Perinatology 2007;27(7):428-33. [DOI: 10.1038/sj.jp.7211758] [PMID: ] - DOI - PubMed
Socha 2011
    1. Socha P, Grote V, Gruszfeld D, Janas R, Demmelmair H, Closa-Monasterolo R, et al. Milk protein intake, the metabolic-endocrine response, and growth in infancy: data from a randomized clinical trial. American Journal of Clinical Nutrition 2011;94(6 Suppl):1776S-84S. [DOI: 10.3945/ajcn.110.000596] [PMID: ] - DOI - PubMed
Srinivasan 2010
    1. Srinivasan P, Brandler M, D'Souza A, Millman P, Moreau H. Allergic enterocolitis presenting as recurrent necrotizing enterocolitis in preterm neonates. Journal of Perinatology 2010;30(6):431-3. [DOI: 10.1038/jp.2009.153] [PMID: ] - DOI - PubMed
Su 2014
    1. Su BH. Optimizing nutrition in preterm infants. Pediatrics and Neonatology 2014;55(1):5-13. [DOI: 10.1016/j.pedneo.2013.07.003] [PMID: ] - DOI - PubMed
Thoene 2014
    1. Thoene M, Hanson C, Lyden E, Dugick L, Ruybal L, Anderson-Berry A. Comparison of the effect of two human milk fortifiers on clinical outcomes in premature infants. Nutrients 2014;6(1):261-75. [DOI: 10.3390/nu6010261] [PMID: ] - DOI - PMC - PubMed
Tonkin 2014
    1. Tonkin EL, Collins CT, Miller J. Protein intake and growth in preterm infants: a systematic review. Global Pediatric Health 2014;1:2333794X14554698. [DOI: 10.1177/2333794X14554698] [PMID: ] - DOI - PMC - PubMed
Tudehope 2013
    1. Tudehope DI. Human milk and the nutritional needs of preterm infants. Journal of Pediatrics 2013;162(3 Suppl):S17-25. [DOI: 10.1016/j.jpeds.2012.11.049] [PMID: ] - DOI - PubMed
Underwood 2013
    1. Underwood MA. Human milk for the premature infant. Pediatric Clinics of North America 2013;60(1):189-207. [DOI: 10.1016/j.pcl.2012.09.008] [PMID: ] - DOI - PMC - PubMed
Weber 2001
    1. 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 Paediatrica 2001;90(7):772-5. [PMID: ] - PubMed
WHO 1995
    1. World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. who.int/nutrition/publications/growth_physical_status/en/ (accessed 2 February 2018).
Yeung 2003
    1. Yeung MY, Smyth JP. Nutritionally regulated hormonal factors in prolonged postnatal growth retardation and its associated adverse neurodevelopmental outcome in extreme prematurity. Biology of the Neonate 2003;84(1):1-23. [DOI: 10.1159/000071438] [PMID: ] - DOI - PubMed
Ziegler 2011
    1. Ziegler EE. Meeting the nutritional needs of the low-birth-weight infant. Annals of Nutrition & Metabolism 2011;58(Suppl 1):8-18. [DOI: 10.1159/000323381] [PMID: ] - DOI - PubMed

References to other published versions of this review

Amissah 2018
    1. Amissah EA, Brown J, Harding JE. Protein supplementation of human milk for promoting growth in preterm infants. Cochrane Database of Systematic Reviews 2018, Issue Issue 6. Art. No.: CD000433. Art. No: CD000433. [DOI: 10.1002/14651858.CD000433.pub2] - DOI - PMC - PubMed
Kuschel 2000c
    1. Kuschel CA, Harding JE. Protein supplementation of human milk for promoting growth in preterm infants. Cochrane Database of Systematic Reviews 2000, Issue 2. Art. No: CD000433. [DOI: 10.1002/14651858.CD000433] - DOI - PubMed

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