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Review Article| Volume 49, ISSUE 2, P427-445, June 2022

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Enteral Nutrition

The Intricacies of Human Milk from the Immune System to the Microbiome

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      References

        • American Academy of Pediatrics Section on Breastfeeding
        Breastfeeding and the use of human milk.
        Pediatrics. 2012; 129: e827-e841
        • Vohr B.R.
        • Poindexter B.B.
        • Dusick A.M.
        • et al.
        • NICHD Neonatal Research Network
        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
        • Vohr B.R.
        • Poindexter B.B.
        • Dusick A.M.
        • et al.
        • National Institute of Child Health and Human Development National Research Network
        Persistent beneficial effects of breast milk ingested in the neonatal intensive care unit on outcomes of extremely low birth weight infants at 30 months of age.
        Pediatrics. 2007; 120: e953-e959
        • Sullivan S.
        • Schanler R.J.
        • Kim J.H.
        • et al.
        An exclusively human milk-based diet is associated with a lower rate of necrotizing enterocolitis than a diet of human milk and bovine milk-based products.
        J Pediatr. 2010; 156: 562-567
        • Ip S.
        • Chung M.
        • Raman G.
        • et al.
        A summary of the Agency for Healthcare Research and Quality’s evidence report on breastfeeding in developed countries.
        Breastfeed Med. 2009; 4: S17-S30
        • Delaney Manthe E.
        • Perks P.H.
        • Swanson J.R.
        Team-based implementation of an exclusive human milk diet.
        Adv Neonatal Care. 2019; 19: 460-467
        • Chetta K.E.
        • Schulz E.V.
        • Wagner C.L.
        Outcomes improved with human milk intake in preterm and full-term infants.
        Semin Perinatol. 2021; 45: 151384
        • Andreas N.J.
        • Kampmann B.
        • Le-Doare K.M.
        Human breast milk: a review on its composition and bioactivity.
        Early Hum Dev. 2015; 91: 629-635
        • Martin C.R.
        • Ling P.R.
        • Blackburn G.L.
        Review of infant feeding: key features of breast milk and infant formula.
        Nutrients. 2016; 8: 279
        • Ballard O.
        • Morrow A.L.
        Human milk composition: nutrients and bioactive factors.
        Pediatr Clin North Am. 2013; 60: 49-74
        • Kim S.Y.
        • Yi D.Y.
        Components of human breast milk: from macronutrient to microbiome and microRNA.
        Clin Exp Pediatr. 2020; 63: 301-309
        • Donovan S.M.
        Human milk proteins: composition and physiological significance.
        in: Donovan S.M. German J.B. Lonnerdal B. Human milk: composition, clinical benefits and future opportunities. Nestle nutrition workshop series. Nutrition Institute/Karger AG, Basel Switzerland2019
        • Monaco M.H.
        • Kim J.
        • Donovan S.M.
        Human milk: composition and nutritional value.
        in: Caballero B. Finglas P. Toldra F. Encyclopedia of food and health. Elsevier, 2016
        • Thai J.D.
        • Gregory K.E.
        Bioactive factors in human breast milk attenuate intestinal inflammation during early life.
        Nutrients. 2020; 12: E581
        • Gridneva Z.
        • Tie W.J.
        • Rea A.
        • et al.
        Human milk casein and whey protein and infant body composition over the first 12 months of lactation.
        Nutrients. 2018; 10: 1332
        • Stromqvist M.
        • Falk P.
        • Bergström S.
        • et al.
        Human milk kappa-casein and inhibition of Helicobacter pylori adhesion to human gastric mucosa.
        J Pediatr Gastroenterol Nutr. 1995; 21: 288-296
        • Brink L.R.
        • Lonnerdal B.
        Milk fat globule membrane: the role of its various components in infant health and development.
        J Nutr Biochem. 2020; 85: 108465
        • Dror D.K.
        • Allen L.H.
        Overview of nutrients in human milk.
        Adv Nutr. 2018; 9: 278S-294S
        • Nommsen L.A.
        • Lovelady C.A.
        • Heinig M.J.
        • et al.
        Determinants of energy, protein, lipid, and lactose concentration sin human milk during the first 12 mo of lactation: the DARLING study.
        Am J Clin Nutr. 1991; 53: 457-465
        • Narang A.P.
        • Bains H.S.
        • Kansal S.
        • et al.
        Serial composition of human milk in preterm and term mothers.
        Indian J Clin Biochem. 2006; 21: 89-94
        • Anderson G.H.
        The effect of prematurity on milk composition and its physiological basis.
        Fed Proc. 1984; 43: 2438-2442
        • Zivkovic A.M.
        • German J.B.
        • Lebrilla C.B.
        • et al.
        Human milk glycobiome and its impact on the infant gastrointestinal microbiota.
        Proc Natl Acad Sci U S A. 2011; 108: 4653-4658
        • Kulinich A.
        • Liu L.
        Human milk oligosaccharides: the role in the fine tuning of innate immune responses.
        Carbohydr Res. 2016; 432: 62-70
        • Cheng L.
        • Akkerman R.
        • Kong C.
        • et al.
        More than sugar in the milk: human milk oligosaccharides as essential bioactive molecules in breast milk and current insight in beneficial effects.
        Crit Rev Food Sci Nutr. 2021; 61: 1184-1200
        • Mitoulas L.R.
        • Kent J.C.
        • Cox D.B.
        • et al.
        Variation in fat, lactose and protein in human milk over 24 h and through the first year of lactation.
        Br J Nutr. 2002; 88: 29-37
        • Demmelmair H.
        • Koletzko B.
        Lipids in human milk.
        Best Pract Res Clin Endocrinol Metab. 2018; 32: 57-68
        • Koletzko B.
        Human milk lipids.
        Ann Nutr Metab. 2016; 69: 28-40
        • Ojo-Okunola A.
        • Cacciatore S.
        • Nicol M.P.
        • et al.
        The determinants of the human milk metabolome and its role in infant health.
        Metabolites. 2020; 10: 77
        • Mimouni F.B.
        • Lubetzky R.
        • Yochpaz S.
        • et al.
        Preterm human milk macronutrient and energy composition.
        Clin Perinatol. 2017; 44: 165-172https://doi.org/10.1016/j.clp.2016.11.010
        • Straarup E.M.
        • Lauritzen L.
        • Faerk J.
        • et al.
        The Stereospecific Triacylglycerol structures and fatty acid profiles of human milk and infant formulas.
        J Pediatr Gastroenterol Nutr March. 2006; 42: 293-299https://doi.org/10.1097/01.mpg.0000214155.51036.4f
        • Lyons K.E.
        • Ryan C.A.
        • Dempsey E.M.
        • et al.
        Breast milk, a source of beneficial microbes and associated benefits for infant health.
        Nutrients. 2020; 12https://doi.org/10.3390/nu12041039
        • Rodríguez J.M.
        The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation?.
        Adv Nutr. 2014; 5: 779-784https://doi.org/10.3945/an.114.007229
        • Kleinman R.E.
        • Walker W.A.
        The enteromammary immune system: an important new concept in breast milk host defense.
        Dig Dis Sci. 1979; 24: 876-882https://doi.org/10.1007/BF01324906
        • Biagi E.
        • Quercia S.
        • Aceti A.
        • et al.
        The bacterial ecosystem of mother’s milk and infant’s mouth and gut.
        Front Microbiol. 2017; 8: 1214https://doi.org/10.3389/fmicb.2017.01214
        • Goldman A.S.
        • Chheda S.
        • Keeney S.E.
        • et al.
        Immunology of human milk and host immunity.
        in: Polin R.A. Fox W.H. Abman S.H. Fetal and neonatal physiology. Elsevier, Philadelphia2011: 1690-1701https://doi.org/10.1016/B978-1-4160-3479-7.10158-2
        • Hayward A.R.
        The human fetus and newborn: development of the immune response.
        Birth Defects Orig Artic Ser. 1983; 19: 289-294
        • Herrmann K.
        • Carroll K.
        An exclusively human milk diet reduces necrotizing enterocolitis.
        Breastfeed Med. 2014; 9: 184-190https://doi.org/10.1089/bfm.2013.0121
        • Patel A.L.
        • Kim J.H.
        Human milk and necrotizing enterocolitis.
        Semin Pediatr Surg. 2018; 27: 34-38https://doi.org/10.1053/j.sempedsurg.2017.11.007
      1. HMOs and infant intake associated with overweight and obesity and infant growth.pdf | Powered by Box.
        (Available at:) (Accessed October 8, 2021)
        • Wiciński M.
        • Sawicka E.
        • Gębalski J.
        • et al.
        Human milk oligosaccharides: health benefits, potential applications in infant formulas, and pharmacology.
        Nutrients. 2020; 12https://doi.org/10.3390/nu12010266
        • Triantis V.
        • Bode L.
        • van Neerven R.J.J.
        Immunological effects of human milk oligosaccharides.
        Front Pediatr. 2018; 6: 190https://doi.org/10.3389/fped.2018.00190
        • Kell D.B.
        • Heyden E.L.
        • Pretorius E.
        The biology of lactoferrin, an iron-binding protein that can help defend against viruses and bacteria.
        Front Immunol. 2020; 11: 1221https://doi.org/10.3389/fimmu.2020.01221
        • Oda H.
        • Wakabayashi H.
        • Yamauchi K.
        • et al.
        Lactoferrin and Bifidobacteria.
        Biometals. 2014; 27: 915-922https://doi.org/10.1007/s10534-014-9741-8
        • He Y.
        • Lawlor N.T.
        • Newburg D.S.
        Human milk components modulate toll-like receptor-mediated inflammation.
        Adv Nutr. 2016; 7: 102-111https://doi.org/10.3945/an.115.010090
        • Tang X.
        • Liu H.
        • Yang S.
        • et al.
        Epidermal growth factor and intestinal barrier function.
        Mediators Inflamm. 2016; 2016: 1927348https://doi.org/10.1155/2016/1927348
        • Wagner C.L.
        • Taylor S.N.
        • Johnson D.
        Host factors in amniotic fluid and breast milk that contribute to gut maturation.
        Clin Rev Allergy Immunol. 2008; 34: 191-204https://doi.org/10.1007/s12016-007-8032-3
        • Radulescu A.
        • Zhang H.-Y.
        • Chen C.-L.
        • et al.
        Heparin-binding EGF-like growth factor promotes intestinal anastomotic healing.
        J Surg Res. 2011; 171: 540-550https://doi.org/10.1016/j.jss.2010.06.036
        • Saito S.
        • Yoshida M.
        • Ichijo M.
        • et al.
        Transforming growth factor-beta (TGF-beta) in human milk.
        Clin Exp Immunol. 1993; 94: 220-224https://doi.org/10.1111/j.1365-2249.1993.tb06004.x
        • Kalliomäki M.
        • Ouwehand A.
        • Arvilommi H.
        • et al.
        Transforming growth factor-β in breast milk: a potential regulator of atopic disease at an early age.
        J Allergy Clin Immunol. 1999; 104: 1251-1257https://doi.org/10.1016/S0091-6749(99)70021-7
        • Savino F.
        • Liguori S.A.
        • Petrucci E.
        • et al.
        Evaluation of leptin in breast milk, lactating mothers and their infants.
        Eur J Clin Nutr. 2010; 64: 972-977https://doi.org/10.1038/ejcn.2010.105
        • Dundar N.O.
        • Anal O.
        • Dundar B.
        • et al.
        Longitudinal investigation of the relationship between breast milk leptin levels and growth in breast-fed infants.
        J Pediatr Endocrinol Metab. 2005; 18: 181-187https://doi.org/10.1515/jpem.2005.18.2.181
        • Savino F.
        • Liguori S.A.
        Update on breast milk hormones: leptin, ghrelin and adiponectin.
        Clin Nutr. 2008; 27: 42-47https://doi.org/10.1016/j.clnu.2007.06.006
        • Emami C.N.
        • Chokshi N.
        • Wang J.
        • et al.
        Role of interleukin-10 in the pathogenesis of necrotizing enterocolitis.
        Am J Surg. 2012; 203: 428-435https://doi.org/10.1016/j.amjsurg.2011.08.016
        • Melville J.M.
        • Moss T.J.M.
        The immune consequences of preterm birth.
        Front Neurosci. 2013; 7: 79https://doi.org/10.3389/fnins.2013.00079
        • Abrams S.A.
        • Landers S.
        • Noble L.M.
        • et al.
        Donor human milk for the high- risk infant: preparation, safety, and usage options in the United States.
        Pediatrics. 2017; 139https://doi.org/10.1542/peds.2016-3440
        • Moro G.E.
        • Arslanoglu S.
        • Bertino E.
        • et al.
        Human milk in feeding premature infants.
        J Pediatr Gastroenterol Nutr. 2015; 61https://doi.org/10.1097/mpg.0000000000000897
        • Assad M.
        • Elliott M.J.
        • Abraham J.H.
        Decreased cost and improved feeding tolerance in VLBW infants fed an exclusive human milk diet.
        J Perinatol. 2016; 36: 216-220https://doi.org/10.1038/jp.2015.168
      2. Kleinman RE and Greer FR. AAP pediatric nutrition, 8th edition, 2020, Breastfeeding pp 68-69

      3. Kleinman RE and Greer FR. AAP pediatric nutrition, 8th edition, 2020, Nutritional Needs of the Preterm Infant pp 142-146

        • Picaud J.C.
        • Buffin R.
        Human milk—treatment and quality of banked human milk.
        Clin Perinatol. 2017; 44: 95-119https://doi.org/10.1016/j.clp.2016.11.003
        • Valentine C.J.
        • Dumm M.
        Pasteurized donor human milk use in the neonatal intensive care unit.
        Neoreviews. 2015; 16: e152-e159https://doi.org/10.1542/neo.16-3-e152
        • Haiden N.
        • Ziegler E.E.
        Human milk banking.
        Ann Nutr Metab. 2017; 69https://doi.org/10.1159/000452821
        • Peila C.
        • Moro G.E.
        • Bertino E.
        • et al.
        The effect of holder pasteurization on nutrients and biologically-active components in donor human milk: a review.
        Nutrients. 2016; 8https://doi.org/10.3390/nu8080477
        • Meier P.
        • Patel A.
        • Esquerra-Zwiers A.
        Donor human milk update: evidence, mechanisms, and priorities for research and practice MOM and DHM: compositional and bioactive differences that impact outcome.
        J Pediatr. 2016; https://doi.org/10.1016/j.jpeds.2016.09.027
        • Arslanoglu S.
        • Corpeleijn W.
        • Moro G.
        • et al.
        Donor human milk for preterm infants.
        J Pediatr Gastroenterol Nutr. 2013; https://doi.org/10.1097/MPG.0b013e3182a3af0a
        • Tully D.B.
        • Jones F.
        • Tully M.R.
        Donor milk: what’s in it and what’s not.
        J Hum Lact. 2001; 17: 152-155https://doi.org/10.1177/089033440101700212
        • Lima H.K.
        • Wagner-Gillespie M.
        • Perrin M.T.
        • et al.
        Bacteria and bioactivity in Holder pasteurized and shelf-stable human milk products.
        Curr Dev Nutr. 2017; 1https://doi.org/10.3945/cdn.117.001438
        • Lewin A.
        • Delage G.
        • Bernier F.
        • et al.
        Banked human milk and quantitative risk assessment of Bacillus cereus infection in premature infants: a simulation study.
        Can J Infect Dis Med Microbiol. 2019; https://doi.org/10.1155/2019/6348281
        • Riskin A.
        Immunomodulatory constituents of human donor milk.
        Breastfeed Med. 2020; 15: 563-567https://doi.org/10.1089/bfm.2020.0192
        • Paulaviciene I.J.
        • Liubsys A.
        • Eidukaite A.
        • et al.
        The effect of prolonged freezing and holder pasteurization on the macronutrient and bioactive protein compositions of human milk.
        Breastfeed Med. 2020; 15: 583-588https://doi.org/10.1089/bfm.2020.0219
        • Dussault N.
        • Cayer M.P.
        • Landry P.
        • et al.
        Girard, Mélissa comparison of the effect of holder pasteurization and high-pressure processing on human milk bacterial load and bioactive factors preservation.
        J Pediatr Gastroenterol Nutr. 2021; https://doi.org/10.1097/MPG.0000000000003065
        • Meredith-Dennis L.
        • Xu G.
        • Goonatilleke E.
        • et al.
        Composition and variation of macronutrients, immune proteins, and human milk oligosaccharides in human milk from nonprofit and commercial milk banks.
        J Hum Lact. 2018; 34: 120-129https://doi.org/10.1177/0890334417710635
        • Moro G.E.
        • Billeaud C.
        • Rachel B.
        • et al.
        Processing of donor human milk: update and recommendations from the European milk bank association (EMBA).
        Front Pediatr. 2019; 7: 49https://doi.org/10.3389/fped.2019.00049
        • Marx C.
        • Bridge R.
        • Wolf A.K.
        • et al.
        Human milk oligosaccharide composition differs between donor milk and mother’s own milk in the NICU.
        J Hum Lact. 2014; https://doi.org/10.1177/0890334413513923
        • Vázquez D.C.
        • García S.S.
        • Renau M.I.
        • et al.
        Availability of donor milk for very preterm infants decreased the risk of necrotizing enterocolitis without adversely impacting growth or rates of breastfeeding.
        Nutrients. 2019; 11https://doi.org/10.3390/nu11081895
        • Colaizy T.T.
        Effects of milk banking procedures on nutritional and bioactive components of donor human milk.
        Semin Perinatol. 2021; 45: 151382https://doi.org/10.1016/j.semperi.2020.151382
        • Eglash A.
        • Simon L.
        • the Academy of Breastfeeding Medicine
        ABM clinical protocol #8: human milk storage information for home use for full-term infants, revised 2017.
        Breastfeed Med. 2017; 12: 390-395https://doi.org/10.1089/bfm.2017.29047.aje
        • Quigley M.
        • Embleton N.D.
        • Mcguire W.
        Formula versus donor breast milk for feeding preterm or low birth weight infants.
        Cochrane Database Syst Rev. 2018; 2018https://doi.org/10.1002/14651858.CD002971.pub4
        • Beghetti I.
        • Biagi E.
        • Martini S.
        • et al.
        Human milk’s hidden gift: implications of the milk microbiome for preterm infants’ health.
        Nutrients. 2019; 11: 1-13https://doi.org/10.3390/nu11122944
        • Hair A.B.
        • Hawthorne K.M.
        • Chetta K.E.
        • et al.
        Human milk feeding supports adequate growth in infants ≤ 1250 grams birth weight.
        BMC Res Notes. 2013; 6: 459https://doi.org/10.1186/1756-0500-6-459
        • Huston R.K.
        • Markell A.M.
        • McCulley E.A.
        • et al.
        Improving growth for infants ≤1250 grams receiving an exclusive human milk diet.
        Nutr Clin Pract. 2018; https://doi.org/10.1002/ncp.10054
        • Genoni G.
        • Binotti M.
        • Monzani A.
        • et al.
        Nonrandomized interventional study showed that early aggressive nutrition was effective in reducing postnatal growth restriction in preterm infants.
        Acta Pediatr. 2017; 106: 1589-1595https://doi.org/10.1111/apa.13958
        • Kantorowska A.
        • Wei J.C.
        • Cohen R.S.
        • et al.
        Impact of donor milk availability on breast milk use and necrotizing enterocolitis rates.
        Pediatrics. 2016; 137https://doi.org/10.1542/peds.2015-3123
      4. Prolacta introduces the worlds first and only human milk caloric fortifier made from human milk cream for preemies in the NICU - Prolacta bioscience.
        (Accessed April 18, 2021)
        • Yang I.
        • Corwin E.J.
        • Brennan P.A.
        • et al.
        The infant microbiome: implications for infant health and neurocognitive development.
        Nurs Res. 2016; 65: 76-88
        • Gopalakrishna K.
        • Hand T.
        Influence of maternal milk on the neonatal intestinal microbiome.
        Nutrients. 2020; 12
        • Moossavi M.
        • et al.
        Composition and variation of the human milk microbiota are influenced by maternal and early-life factors.
        Cell Host Microbe. 2019; 25: 324-335
        • Mohan P.
        • Lal C.V.
        • Wagner B.D.
        • et al.
        Airway microbiome and development of bronchopulmonary dysplasia in preterm infants: a systematic review.
        J Pediatr. 2019; 204: 126-133
        • Piersigilli F.
        • Van Grambezen B.
        • Hocq C.
        • et al.
        Nutrients and microbiota in lung diseases of prematurity: the placenta-gut-lung triangle.
        Nutrients. 2020; 12
        • Gray L.
        • O’Hely M.
        • Ranganathan S.
        • et al.
        The maternal diet, gut bacteria, bacterial metabolites during pregnancy influence offspring asthma.
        Front Immunol. 2017; 8
        • Horta B.L.
        • Loret de Mola C.
        • Victora C.G.
        Breastfeeding and intelligence: a systematic review and meta-analysis.
        Acta Paediatr Suppl. 2015; 104: 14-19
        • Belfort M.
        Breast milk feeding, brain development, and neurocognitive outcomes: a 7 year longitudinal study in infants born <39 weeks’ gestation.
        J Pediatrc. 2016; 177: 133-139
        • Keikha M.
        • Bahreynian M.
        • Saleki M.
        • et al.
        Macro-and micronutrient of human milk composition: are they related to maternal diet? A comprehensive systematic review.
        Breastfeed Med. 2017; 12
        • Aumeistere L.
        • Ciproviča I.
        • Zavadska D.
        • et al.
        Zinc content in breast milk and its association with maternal diet.
        Nutrients. 2018; 10
        • Innis S.
        Impact of maternal diet on human milk composition and neurological development of infants.
        Am J Clin Nutr. 2014; 99: 734S-741S
        • Holmes A.
        • Schmidlin H.
        • Kurzum E.
        Breastfeeding considerations for mothers of infants with neonatal abstinence syndrome.
        Pharmacotherapy. 2017; 37: 861-869
        • Metz T.
        • Stickrath E.
        Marijuana use in pregnancy and lactation: a review of the evidence.
        Am J Obstet Gynecol. 2015; : 761-777
        • Metz T.
        • Borgelt L.
        Marijuana use in pregnancy and while breastfeeding.
        Obstet Gynecol. 2018; 132: 1198-1210
        • MacVicar S.
        • Humphrey T.
        • Forbes-McKay K.
        Breastfeeding and the substance-exposed mother and baby.
        Birth. 2018; 45: 450-458
        • Lechner B.
        • Vohr B.
        Neurodevelopment outcomes of preterm infants fed human milk: a systematic review.
        Clin Perinatol. 2017; 44: 69-83
        • Manzoni P.
        • Dall'Agnola A.
        • Tomé D.
        • et al.
        Role of lactoferrin in neonates and infants: an update.
        Am J Perinatol. 2018; 35: 561-565https://doi.org/10.1055/s-0038-1639359