Human Breast Milk: The Key Role in the Maturation of Immune, Gastrointestinal and Central Nervous Systems: A Narrative Review

Margarita Dimitroglou, Zoi Iliodromiti, Evangelos Christou, Paraskevi Volaki, Chrysa Petropoulou, Rozeta Sokou, Theodora Boutsikou, Nicoletta Iacovidou, Margarita Dimitroglou, Zoi Iliodromiti, Evangelos Christou, Paraskevi Volaki, Chrysa Petropoulou, Rozeta Sokou, Theodora Boutsikou, Nicoletta Iacovidou

Abstract

Premature birth is a major cause of mortality and morbidity in the pediatric population. Because their immune, gastrointestinal and nervous systems are not fully developed, preterm infants (<37 weeks of gestation) and especially very preterm infants (VPIs, <32 weeks of gestation) are more prone to infectious diseases, tissue damage and future neurodevelopmental impairment. The aim of this narrative review is to report the immaturity of VPI systems and examine the role of Human Breast Milk (HBM) in their development and protection against infectious diseases, inflammation and tissue damage. For this purpose, we searched and synthesized the data from the existing literature published in the English language. Studies revealed the significance of HBM and indicate HBM as the best dietary choice for VPIs.

Keywords: breast milk; central nervous system; gastrointestinal system; immune system; neonate.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Figure 1
Figure 1
Immaturity of immune, gastrointestinal and nervous systems in very preterm neonates [13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44].
Figure 2
Figure 2
Nutrients of HBM that provide passive immunity, have anti-inflammatory action and induce the maturation of immune, gastrointestinal and nervous systems in VPIs [83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116,117,118,119,120,121,122,123,124,125,126,127,128].

References

    1. Preterm Birth. [(accessed on 22 August 2022)]. Available online: .
    1. Baroutis G., Mousiolis A., Mesogitis S., Costalos C., Antsaklis A. Preterm birth trends in Greece, 1980–2008: A rising concern. Acta Obstet. Gynecol. Scand. 2013;92:575–582. doi: 10.1111/aogs.12089.
    1. Torchin H., Ancel P.Y., Jarreau P.H., Goffinet F. Epidemiology of preterm birth: Prevalence, recent trends, short- and long-term outcomes. J. Gynecol. Obstet. Biol. Reprod. 2015;44:723–731. doi: 10.1016/j.jgyn.2015.06.010.
    1. Barfield W.D. Public Health Implications of Very Preterm Birth. Clin. Perinatol. 2018;45:565. doi: 10.1016/j.clp.2018.05.007.
    1. Thompson T., Reynolds J. The results of intensive care therapy for neonates with respiratory distress syndrome: I. Neonatal mortality rates for neonates with RDS II. Long-term prognosis for survivors with RDS. J. Perinat. Med. 1977;5:149–171. doi: 10.1515/JPME.1977.5.4.149/HTML.
    1. Iliodromiti Z., Christou E., Vrachnis N., Sokou R., Vrachnis D., Mihopoulou G., Boutsikou T., Iacovidou N. Serum and Urinary N-Terminal Pro-brain Natriuretic Peptides as Biomarkers for Bronchopulmonary Dysplasia of Preterm Neonates. Front. Pediatr. 2020;8:588738. doi: 10.3389/fped.2020.588738.
    1. Cavallin F., Doglioni N., Brombin L., Cavallin F., Doglioni N., Brombin L., Lolli E., Loddo C., Cavicchiolo M.E., Mardegan V., et al. Trends in respiratory management of transferred very preterm infants in the last two decades. Pediatr. Pulmonol. 2021;56:2604–2610. doi: 10.1002/ppul.25532.
    1. Stevens T., Blennow M., Soll R. Early surfactant administration with brief ventilation vs selective surfactant and continued mechanical ventilation for preterm infants with or at risk for respiratory distress syndrome. Cochrane Database Syst. Rev. 2007;2007:CD003063. doi: 10.1002/14651858.CD003063.pub3.
    1. Aldana-Aguirre J.C., Pinto M., Featherstone R.M., Kumar M. Less invasive surfactant administration versus intubation for surfactant delivery in preterm infants with respiratory distress syndrome: A systematic review and meta-analysis. Arch. Dis. Child. Fetal Neonatal Ed. 2017;102:F17–F23. doi: 10.1136/archdischild-2015-310299.
    1. Miller J., Tonkin E., Damarell R.A., McPhee A.J., Suganuma M., Suganuma H., Middleton P.F., Makrides M., Collins C.T. A Systematic Review and Meta-Analysis of Human Milk Feeding and Morbidity in Very Low Birth Weight Infants. Nutrients. 2018;10:707. doi: 10.3390/nu10060707.
    1. Underwood M.A. Human milk for the premature infant. Pediatr. Clin. North Am. 2013;60:189–207. doi: 10.1016/j.pcl.2012.09.008.
    1. Patel A.L., Kim J.H. Human milk and necrotizing enterocolitis. Semin. Pediatr. Surg. 2018;27:34–38. doi: 10.1053/j.sempedsurg.2017.11.007.
    1. Taïeb A. Skin barrier in the neonate. Pediatr. Dermatol. 2018;35((Suppl. S1)):s5–s9. doi: 10.1111/pde.13482.
    1. Kusari A., Han A.M., Virgen C.A., Matiz C., Rasmussen M., Friedlander S.F., Eichenfield D.Z. Evidence-based skin care in preterm infants. Pediatr. Dermatol. 2019;36:16–23. doi: 10.1111/pde.13725.
    1. Melville J.M., Moss T.J.M. The immune consequences of preterm birth. Front. Neurosci. 2013;7:79. doi: 10.3389/fnins.2013.00079.
    1. Cuenca A.G., Wynn J.L., Moldawer L.L., Levy O. Role of innate immunity in neonatal infection. Am. J. Perinatol. 2013;30:105–112. doi: 10.1055/s-0032-1333412.
    1. Grases-Pintó B., Torres-Castro P., Abril-Gil M., Castell M., Rodríguez-Lagunas M.J., Pérez-Cano F.J., Franch À. A Preterm Rat Model for Immunonutritional Studies. Nutrients. 2019;11:999. doi: 10.3390/nu11050999.
    1. Azizia M., Lloyd J., Allen M., Klein N., Peebles D. Immune status in very preterm neonates. Pediatrics. 2012;129:e967–e974. doi: 10.1542/peds.2011-1579.
    1. Segura-Cervantes E., Mancilla-Ramírez J., González-Canudas J., Alba E., Santillán-Ballesteros R., Morales-Barquet D., Sandoval-Plata G., Galindo-Sevilla N. Inflammatory Response in Preterm and Very Preterm Newborns with Sepsis. Mediat. Inflamm. 2016;2016:1–8. doi: 10.1155/2016/6740827.
    1. Walker J.C., Smolders M.A.J.C., Gemen E.F.A., Antonius T.A.J., Leuvenink J., De Vries E. Development of Lymphocyte Subpopulations in Preterm Infants. Scand. J. Immunol. 2011;73:53–58. doi: 10.1111/j.1365-3083.2010.02473.x.
    1. Simister N.E. Placental transport of immunoglobulin G. Vaccine. 2003;21:3365–3369. doi: 10.1016/S0264-410X(03)00334-7.
    1. Clements T., Rice T.F., Vamvakas G., Barnett S., Barnes M., Donaldson B., Jones C.E., Kampmann B., Holder B. Update on Transplacental Transfer of IgG Subclasses: Impact of Maternal and Fetal Factors. Front. Immunol. 2020;11:1920. doi: 10.3389/fimmu.2020.01920.
    1. Denning T.W., Bhatia A.M., Kane A.F., Patel R.M., Denning P.W. Pathogenesis of NEC: Role of the Innate and Adaptive Immune Response. Semin. Perinatol. 2017;41:15. doi: 10.1053/j.semperi.2016.09.014.
    1. Bjarnason I. Intestinal permeability. Gut. 1994;35((Suppl. S1)):S18. doi: 10.1136/gut.35.1_Suppl.S18.
    1. Van Elburg R.M., Fetter W.P.F., Bunkers C.M., Heymans H.S.A. Intestinal permeability in relation to birth weight and gestational and postnatal age. Arch. Dis. Child. Fetal Neonatal Ed. 2003;88:F52. doi: 10.1136/fn.88.1.F52.
    1. Weaver L.T., Laker M.F., Nelson R. Intestinal permeability in the newborn. Arch. Dis. Child. 1984;59:236. doi: 10.1136/adc.59.3.236.
    1. McElroy S.J., Prince L.S., Weitkamp J.H., Reese J., Slaughter J.C., Polk D.B. Tumor necrosis factor receptor 1-dependent depletion of mucus in immature small intestine: A potential role in neonatal necrotizing enterocolitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2011;301:G656. doi: 10.1152/ajpgi.00550.2010.
    1. Berseth C.L. Gastrointestinal Motility in the Neonate. Clin. Perinatol. 1996;23:179–190. doi: 10.1016/S0095-5108(18)30237-9.
    1. Montagne L., Piel C., Lalles J.P. Effect of diet on mucin kinetics and composition: Nutrition and health implications. Nutr. Rev. 2004;62:105–114. doi: 10.1111/j.1753-4887.2004.tb00031.x.
    1. Pammi M., Cope J., Tarr P.I., Warner B.B., Morrow A.L., Mai V., Gregory K.E., Kroll J.S., McMurtry V., Ferris M.J., et al. Intestinal dysbiosis in preterm infants preceding necrotizing enterocolitis: A systematic review and meta-analysis. Microbiome. 2017;5:1–15. doi: 10.1186/s40168-017-0248-8.
    1. Mai V., Young C.M., Ukhanova M., Wang X., Sun Y., Casella G., Theriaque D., Li N., Sharma R., Hudak M., et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS ONE. 2011;6:e20647. doi: 10.1371/JOURNAL.PONE.0020647.
    1. Arboleya S., Ang L., Margolles A., Yiyuan L., Dongya Z., Liang X., Solís G., Fernández N., de Los Reyes-Gavilán C.G., Gueimonde M. Deep 16S rRNA metagenomics and quantitative PCR analyses of the premature infant fecal microbiota. Anaerobe. 2012;18:378–380. doi: 10.1016/j.anaerobe.2012.04.013.
    1. Millar M., Wilks M., Costeloe K. Probiotics for preterm infants? Arch. Dis. Child. Fetal Neonatal Ed. 2003;88:F354–F358. doi: 10.1136/fn.88.5.F354.
    1. Reyman M., van Houten M.A., Watson R.L., Chu M.L.J.N., Arp K., de Waal W.J., Schiering I., Plötz F.B., Willems R.J.L., van Schaik W., et al. Effects of early-life antibiotics on the developing infant gut microbiome and resistome: A randomized trial. Nat. Commun. 2022;13:1–12. doi: 10.1038/s41467-022-28525-z.
    1. Russell J.T., Lauren Ruoss J., de la Cruz D., Li N., Bazacliu C., Patton L., McKinley K.L., Garrett T.J., Polin R.A., Triplett E.W., et al. Antibiotics and the developing intestinal microbiome, metabolome and inflammatory environment in a randomized trial of preterm infants. Sci. Rep. 2021;11:1–16. doi: 10.1038/s41598-021-80982-6.
    1. Niño D.F., Sodhi C.P., Hackam D.J. Necrotizing enterocolitis: New insights into pathogenesis and mechanisms. Nat. Rev. Gastroenterol. Hepatol. 2016;13:590. doi: 10.1038/nrgastro.2016.119.
    1. Nosarti C., Nam K.W., Walshe M., Murray R.M., Cuddy M., Rifkin L., Allin M.P. Preterm birth and structural brain alterations in early adulthood. NeuroImage Clin. 2014;6:180–191. doi: 10.1016/j.nicl.2014.08.005.
    1. Ramel S.E., Georgieff M.K. Preterm nutrition and the brain. World. Rev. Nutr. Diet. 2014;110:190–200. doi: 10.1159/000358467.
    1. El-Khoury N., Braun A., Hu F., Pandey M., Nedergaard M., Lagamma E.F., Ballabh P. Astrocyte End-Feet in Germinal Matrix, Cerebral Cortex, and White Matter in Developing Infants. Pediatr. Res. 2006;59:673–679. doi: 10.1203/01.pdr.0000214975.85311.9c.
    1. Malaeb S., Dammann O. Fetal inflammatory response and brain injury in the preterm newborn. J. Child Neurol. 2009;24:1119–1126. doi: 10.1177/0883073809338066.
    1. Raybaud C., Ahmad T., Rastegar N., Shroff M., Al Nassar M. The premature brain: Developmental and lesional anatomy. Neuroradiology. 2013;55((Suppl. S2)):23–40. doi: 10.1007/s00234-013-1231-0.
    1. Basu S.K., Pradhan S., du Plessis A.J., Ben-Ari Y., Limperopoulos C. GABA and glutamate in the preterm neonatal brain: In-vivo measurement by magnetic resonance spectroscopy. Neuroimage. 2021;238:118215. doi: 10.1016/j.neuroimage.2021.118215.
    1. Basu S.K., Pradhan S., Jacobs M.B., Said M., Kapse K., Murnick J., Whitehead M.T., Chang T., du Plessis A.J., Limperopoulos C. Age and Sex Influences Gamma-aminobutyric Acid Concentrations in the Developing Brain of Very Premature Infants. Sci. Rep. 2020;10:1–10. doi: 10.1038/s41598-020-67188-y.
    1. Kwon S.H., Scheinost D., Lacadie C., Benjamin J., Myers E., Qiu M., Schner K.C., Rothman D.L., Constable R.T., Ment L.R. GABA, resting-state connectivity and the developing brain. Neonatology. 2014;106:149–155. doi: 10.1159/000362433.
    1. Stoll B.J., Hansen N., Fanaroff A.A., Wright L.L., Carlo W.A., Ehrenkranz R.A., Lemons J.A., Donovan E.F., Stark A.R., Tyson J.E., et al. Late-onset sepsis in very low birth weight neonates: The experience of the NICHD Neonatal Research Network. Pt 1Pediatrics. 2002;110:285–291. doi: 10.1542/peds.110.2.285.
    1. Letouzey M., Foix-L’Hélias L., Torchin H., Mitha A., Morgan A.S., Zeitlin J., Kayem G., Maisonneuve E., Delorme P., Khoshnood B., et al. Cause of preterm birth and late-onset sepsis in very preterm infants: The EPIPAGE-2 cohort study. Pediatr. Res. 2021;90:584–592. doi: 10.1038/s41390-021-01411-y.
    1. Collins A., Weitkamp J.H., Wynn J.L. Why are preterm newborns at increased risk of infection? Arch. Dis. Child. Fetal Neonatal Ed. 2018;103:F391–F394. doi: 10.1136/archdischild-2017-313595.
    1. Steiner L., Diesner S.C., Voitl P. Risk of infection in the first year of life in preterm children: An Austrian observational study. PLoS ONE. 2019;14:e0224766. doi: 10.1371/journal.pone.0224766.
    1. Yu J.C., Khodadadi H., Malik A., Davidson B., Salles É.D.S.L., Bhatia J., Hale V.L., Baban B. Innate Immunity of Neonates and Infants. Front. Immunol. 2018;9:1759. doi: 10.3389/fimmu.2018.01759.
    1. Anand R.J., Leaphart C.L., Mollen K.P., Hackam D.J. The role of the intestinal barrier in the pathogenesis of necrotizing enterocolitis. Shock. 2007;27:124–133. doi: 10.1097/01.shk.0000239774.02904.65.
    1. Looi K., Evans D.J., Garratt L.W., Ang S., Hillas J.K., Kicic A., Simpson S.J. Preterm birth: Born too soon for the developing airway epithelium? Paediatr. Respir. Rev. 2019;31:82–88. doi: 10.1016/j.prrv.2018.11.003.
    1. Lewis E.D., Richard C., Larsen B.M., Field C.J. The Importance of Human Milk for Immunity in Preterm Infants. Clin. Perinatol. 2017;44:23–47. doi: 10.1016/j.clp.2016.11.008.
    1. Berrington J.E., Barge D., Fenton A.C., Cant A.J., Spickett G.P. Lymphocyte subsets in term and significantly preterm UK infants in the first year of life analysed by single platform flow cytometry. Clin. Exp. Immunol. 2005;140:289–292. doi: 10.1111/j.1365-2249.2005.02767.x.
    1. Sim K., Shaw A.G., Randell P., Cox M.J., McClure Z.E., Li M.S., Haddad M., Langford P.R., Cookson W.O., Moffatt M.F., et al. Dysbiosis Anticipating Necrotizing Enterocolitis in Very Premature Infants. Clin. Infect. Dis. 2015;60:389–397. doi: 10.1093/cid/ciu822.
    1. Patel B.K., Shah J.S. Necrotizing Enterocolitis in Very Low Birth Weight Infants: A Systemic Review. ISRN Gastroenterol. 2012;2012:1–7. doi: 10.5402/2012/562594.
    1. Bazacliu C., Neu J. Necrotizing Enterocolitis: Long Term Complications. Curr. Pediatr. Rev. 2019;15:115–124. doi: 10.2174/1573396315666190312093119.
    1. Kamity R., Kapavarapu P.K., Chandel A. Feeding Problems and Long-Term Outcomes in Preterm Infants—A Systematic Approach to Evaluation and Management. Children. 2021;8:1158. doi: 10.3390/children8121158.
    1. Thompson A.M., Bizzarro M.J. Necrotizing enterocolitis in newborns: Pathogenesis, prevention and management. Drugs. 2008;68:70–75. doi: 10.2165/00003495-200868090-00004.
    1. Baranowski J.R., Claud E.C. Necrotizing Enterocolitis and the Preterm Infant Microbiome. Adv. Exp. Med. Biol. 2019;1125:25–36. doi: 10.1007/5584_2018_313.
    1. Odenwald M.A., Turner J.R. The intestinal epithelial barrier: A therapeutic target? Nat. Rev. Gastroenterol. Hepatol. 2017;14:9–21. doi: 10.1038/nrgastro.2016.169.
    1. DiGiulio D.B., Gervasi M.T., Romero R., Vaisbuch E., Mazaki-Tovi S., Kusanovic J.P., Seok K.S., Gómez R., Mittal P., Gotsch F., et al. Microbial invasion of the amniotic cavity in pregnancies with small-for-gestational-age fetuses. J. Perinat. Med. 2010;38:495. doi: 10.1515/jpm.2010.076.
    1. Ardissone A.N., de la Cruz D.M., Davis-Richardson A.G., Rechcigl K.T., Li N., Drew J.C., Murgas-Torrazza R., Sharma R., Hudak M.L., Triplett E.W., et al. Meconium Microbiome Analysis Identifies Bacteria Correlated with Premature Birth. PLoS ONE. 2014;9:e90784. doi: 10.1371/journal.pone.0090784.
    1. Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA. 2010;107:11971–11975. doi: 10.1073/pnas.1002601107.
    1. Harmsen H.J., Wildeboer-Veloo A.C., Raangs G.C., Wagendorp A.A., Klijn N., Bindels J.G., Welling G.W. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 2000;30:61–67. doi: 10.1097/00005176-200001000-00019.
    1. Medzhitov R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 2001;1:135–145. doi: 10.1038/35100529.
    1. Sodhi C.P., Shi X.H., Richardson W.M., Grant Z.S., Shapiro R.A., Prindle T., Jr., Branca M., Russo A., Gribar S.C., Ma C., et al. Toll-like receptor-4 inhibits enterocyte proliferation via impaired beta-catenin signaling in necrotizing enterocolitis. Gastroenterology. 2010;138:185–196. doi: 10.1053/j.gastro.2009.09.045.
    1. Lu P., Sodhi C.P., Hackam D.J. Toll-like Receptor Regulation of Intestinal Development and Inflammation in the Pathogenesis of Necrotizing Enterocolitis. Pathophysiology. 2014;21:81. doi: 10.1016/j.pathophys.2013.11.007.
    1. Yazji I., Sodhi C.P., Lee E.K., Good M., Egan C.E., Afrazi A., Neal M.D., Jia H., Lin J., Ma C., et al. Endothelial TLR4 activation impairs intestinal microcirculatory perfusion in necrotizing enterocolitis via eNOS-NO-nitrite signaling. Proc. Natl. Acad. Sci. USA. 2013;110:9451–9456. doi: 10.1073/pnas.1219997110.
    1. Bora S., Pritchard V.E., Moor S., Austin N.C., Woodward L.J. Emotional and behavioural adjustment of children born very preterm at early school age. J. Paediatr. Child Health. 2011;47:863–869. doi: 10.1111/j.1440-1754.2011.02105.x.
    1. Spittle A.J., Morgan C., Olsen J.E., Novak I., Cheong J.L.Y. Early Diagnosis and Treatment of Cerebral Palsy in Children with a History of Preterm Birth. Clin. Perinatol. 2018;45:409–420. doi: 10.1016/j.clp.2018.05.011.
    1. Pritchard V.E., Clark C.A.C., Liberty K., Champion P.R., Wilson K., Woodward L.J. Early school-based learning difficulties in children born very preterm. Early Hum. Dev. 2009;85:215–224. doi: 10.1016/j.earlhumdev.2008.10.004.
    1. Williams J., Lee K.J., Anderson P.J. Prevalence of motor-skill impairment in preterm children who do not develop cerebral palsy: A systematic review. Dev. Med. Child Neurol. 2010;52:232–237. doi: 10.1111/j.1469-8749.2009.03544.x.
    1. Woodward L.J., Moor S., Hood K.M., Champion P.R., Foster-Cohen S., Inder T.E., Austin N.C. Very preterm children show impairments across multiple neurodevelopmental domains by age 4 years. Arch. Dis. Child. Fetal Neonatal Ed. 2009;94:339–344. doi: 10.1136/adc.2008.146282.
    1. Skinner A.M., Narchi H. Preterm nutrition and neurodevelopmental outcomes. World J. Methodol. 2021;11:278–293. doi: 10.5662/wjm.v11.i6.278.
    1. Malaeb S.N., Cohen S.S., Virgintino D., Stonestreet B.S. Core ConceptsDevelopment of the Blood-Brain Barrier. Neoreviews. 2012;13:e241–e250. doi: 10.1542/neo.13-4-e241.
    1. Ballabh P., Braun A., Nedergaard M. The blood–brain barrier: An overview: Structure, regulation, and clinical implications. Neurobiol. Dis. 2004;16:1–13. doi: 10.1016/j.nbd.2003.12.016.
    1. Brunse A., Abbaspour A., Sangild P.T. Brain Barrier Disruption and Region-Specific Neuronal Degeneration during Necrotizing Enterocolitis in Preterm Pigs. Dev. Neurosci. 2018;40:198–208. doi: 10.1159/000488979.
    1. Wikström S., Ley D., Hansen-Pupp I., Rosén I., Hellström-Westas L. Early amplitude-integrated EEG correlates with cord TNF-alpha and brain injury in very preterm infants. Acta Paediatr. 2008;97:915–919. doi: 10.1111/j.1651-2227.2008.00787.x.
    1. Vasconcelos A.R., Yshii L.M., Viel T.A., Buck H.S., Mattson M.P., Scavone C., Kawamoto E.M. Intermittent fasting attenuates lipopolysaccharide-induced neuroinflammation and memory impairment. J. Neuroinflammation. 2014;11:85. doi: 10.1186/1742-2094-11-85.
    1. Konnikova Y., Zaman M.M., Makda M., D’Onofrio D., Freedman S.D., Martin C.R. Late Enteral Feedings Are Associated with Intestinal Inflammation and Adverse Neonatal Outcomes. PLoS ONE. 2015;10:e0132924. doi: 10.1371/journal.pone.0132924.
    1. Kwok T.C., Dorling J., Gale C. Early enteral feeding in preterm infants. Semin. Perinatol. 2019;43:151159. doi: 10.1053/j.semperi.2019.06.007.
    1. O’Connor D.L., Gibbins S., Kiss A., Bando N., Brennan-Donnan J., Ng E., Campbell D.M., Vaz S., Fusch C., Asztalos E., et al. Effect of Supplemental Donor Human Milk Compared With Preterm Formula on Neurodevelopment of Very Low-Birth-Weight Infants at 18 Months: A Randomized Clinical Trial. JAMA. 2016;316:1897–1905. doi: 10.1001/jama.2016.16144.
    1. 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. doi: 10.1016/j.semperi.2020.151384.
    1. Palmeira P., Carneiro-Sampaio M. Immunology of breast milk. Rev. Assoc. Med. Bras. 2016;62:584–593. doi: 10.1590/1806-9282.62.06.584.
    1. Demers-Mathieu V., Huston R.K., Markell A.M., McCulley E.A., Martin R.L., Dallas D.C. Antenatal Influenza A-Specific IgA, IgM, and IgG Antibodies in Mother’s Own Breast Milk and Donor Breast Milk, and Gastric Contents and Stools from Preterm Infants. Nutrients. 2019;11:1567. doi: 10.3390/nu11071567.
    1. Demers-Mathieu V., Underwood M.A., Beverly R.L., Dallas D.C. Survival of Immunoglobulins from Human Milk to Preterm Infant Gastric Samples at 1, 2, and 3 Hours Postprandial. Neonatology. 2018;114:242. doi: 10.1159/000489387.
    1. Bryant J., Thistle J. Anatomy, Colostrum. [(accessed on 8 January 2022)];2020 Available online:
    1. Hanson L.Å., Winberg J. Breast milk and defence against infection in the newborn. Arch. Dis. Child. 1972;47:845–848. doi: 10.1136/adc.47.256.845.
    1. Mehta R., Petrova A. Biologically active breast milk proteins in association with very preterm delivery and stage of lactation. J. Perinatol. 2011;31:58–62. doi: 10.1038/jp.2010.68.
    1. Ochoa T.J., Zegarra J., Cam L., Llanos R., Pezo A., Cruz K., Zea-Vera A., Cárcamo C., Campos M., Bellomo S. Randomized Controlled Trial of Lactoferrin for Prevention of Sepsis in Peruvian Neonates <2500 Grams. Pediatr. Infect. Dis. J. 2015;34:571. doi: 10.1097/INF.0000000000000593.
    1. Pammi M., Suresh G. Enteral lactoferrin supplementation for prevention of sepsis and necrotizing enterocolitis in preterm infants. Cochrane Database Syst. Rev. 2017;2017:CD007137. doi: 10.1002/14651858.CD007137.pub5.
    1. Razak A., Hussain A. Lactoferrin Supplementation to Prevent Late-Onset Sepsis in Preterm Infants: A Meta-Analysis. Am. J. Perinatol. 2021;38:283–290. doi: 10.1055/s-0039-1696676.
    1. Ellison R.T., Giehl T.J. Killing of gram-negative bacteria by lactoferrin and lysozyme. J. Clin. Investig. 1991;88:1080–1091. doi: 10.1172/JCI115407.
    1. Isaacs C.E., Kashyap S., Heird W.C., Thormar H. Antiviral and antibacterial lipids in human milk and infant formula feeds. Arch. Dis. Child. 1990;65:861. doi: 10.1136/adc.65.8.861.
    1. Schroten H., Hanisch F.G., Plogmann R., Hacker J., Uhlenbruck G., Nobis-Bosch R., Wahn V. Inhibition of adhesion of S-fimbriated Escherichia coli to buccal epithelial cells by human milk fat globule membrane components: A novel aspect of the protective function of mucins in the nonimmunoglobulin fraction. Infect. Immun. 1992;60:2893–2899. doi: 10.1128/iai.60.7.2893-2899.1992.
    1. Salamone M., Di Nardo V. Effects of human milk oligosaccharides (HMOs) on gastrointestinal health. Front. Biosci. 2020;12:183–198. doi: 10.2741/E866.
    1. Triantis V., Bode L., van Neerven J.R.J. Immunological Effects of Human Milk Oligosaccharides. Front. Pediatr. 2018;6:190. doi: 10.3389/fped.2018.00190.
    1. Liu K.Y., Comstock S.S., Shunk J.M., Monaco M.H., Donovan S.M. Natural killer cell populations and cytotoxic activity in pigs fed mother’s milk, formula, or formula supplemented with bovine lactoferrin. Pediatr. Res. 2013;74:402–407. doi: 10.1038/pr.2013.125.
    1. Garofalo R. Cytokines in Human Milk. J. Pediatr. 2010;156:S36–S40. doi: 10.1016/j.jpeds.2009.11.019.
    1. Aspinall R., Prentice A.M., Ngom P.T. Interleukin 7 from Maternal Milk Crosses the Intestinal Barrier and Modulates T-Cell Development in Offspring. PLoS ONE. 2011;6:e20812. doi: 10.1371/journal.pone.0020812.
    1. Goldman A.S., Chheda S. The Immune System in Human Milk: A Historic Perspective. Ann. Nutr. Metab. 2021;77:189–196. doi: 10.1159/000516995.
    1. Johnnidis J.B., Harris M.H., Wheeler R.T., Stehling-Sun S., Lam M.H., Kirak O., Brummelkamp T.R., Fleming M.D., Camargo F.D. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature. 2008;451:1125–1129. doi: 10.1038/nature06607.
    1. Ventura A., Young A.G., Winslow M.M., Lintault L., Meissner A., Erkeland S.J., Newman J., Bronson R.T., Crowley D., Stone J.R., et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2018;132:875. doi: 10.1016/j.cell.2008.02.019.
    1. Nolan L.S., Rimer J.M., Good M. The Role of Human Milk Oligosaccharides and Probiotics on the Neonatal Microbiome and Risk of Necrotizing Enterocolitis: A Narrative Review. Nutrients. 2020;12:3052. doi: 10.3390/nu12103052.
    1. Young L., McGuire W. Immunologic Properties of Human Milk and Clinical Implications in the Neonatal Population. Neoreviews. 2020;21:e809–e816. doi: 10.1542/neo.21-12-e809.
    1. York D.J., Smazal A.L., Robinson D.T., De Plaen I.G. Human Milk Growth Factors and Their Role in NEC Prevention: A Narrative Review. Nutrients. 2021;13:3751. doi: 10.3390/nu13113751.
    1. Dvorak B. Milk Epidermal Growth Factor and Gut Protection. J. Pediatr. 2010;156((Suppl. S2)):S31. doi: 10.1016/j.jpeds.2009.11.018.
    1. Radulescu A., Zhang H.Y., Chen C.L., Chen Y., Zhou Y., Yu X., Otabor I., Olson J.K., Besner G.E. Heparin-Binding Egf-Like Growth Factor Promotes Intestinal Anastomotic Healing. J. Surg. Res. 2011;171:540. doi: 10.1016/j.jss.2010.06.036.
    1. Zhou Y., Wang Y., Olson J., Yang J., Besner G.E. Heparin-binding EGF-like growth factor promotes neuronal nitric oxide synthase expression and protects the enteric nervous system after necrotizing enterocolitis. Pediatr. Res. 2017;82:490–500. doi: 10.1038/pr.2017.68.
    1. Gila-Diaz A., Arribas S.M., Algara A., Martín-Cabrejas M.A., López de Pablo Á.L., Sáenz de Pipaón M., Ramiro-Cortijo D. A Review of Bioactive Factors in Human Breastmilk: A Focus on Prematurity. Nutrients. 2019;11:1307. doi: 10.3390/nu11061307.
    1. Li R., Xia W., Zhang Z., Wu K. S100B Protein, Brain-Derived Neurotrophic Factor, and Glial Cell Line-Derived Neurotrophic Factor in Human Milk. PLoS ONE. 2011;6:e21663. doi: 10.1371/journal.pone.0021663.
    1. Furukawa M., Narahara H., Yasuda K., Johnston J.M. Presence of platelet-activating factor-acetylhydrolase in milk. J. Lipid Res. 1993;34:1603–1609. doi: 10.1016/S0022-2275(20)36953-4.
    1. Maheshwari A., Lu W., Lacson A., Barleycorn A.A., Nolan S., Christensen R.D., Calhoun D.A. Effects of interleukin-8 on the developing human intestine. Cytokine. 2002;20:256–267. doi: 10.1006/cyto.2002.1996.
    1. González H.F., Visentin S. Nutrients and neurodevelopment: Lipids. Update. Arch. Argent. Pediatr. 2016;114:472–476. doi: 10.5546/aap.2016.eng.472.
    1. Martinat M., Rossitto M., Di Miceli M., Layé S. Perinatal Dietary Polyunsaturated Fatty Acids in Brain Development, Role in Neurodevelopmental Disorders. Nutrients. 2021;13:1185. doi: 10.3390/nu13041185.
    1. Agbaga M.P., Mandal N.A., Anderson R.E. Retinal very long-chain PUFAs: New insights from studies on ELOVL4 protein. J. Lipid Res. 2010;51:1624. doi: 10.1194/jlr.R005025.
    1. Dalmeijer G.W., Wijga A.H., Gehring U., Renders C.M., Koppelman G.H., Smit H.A., van Rossem L. Fatty acid composition in breastfeeding and school performance in children aged 12 years. Eur. J. Nutr. 2016;55:2199. doi: 10.1007/s00394-015-1030-y.
    1. Jasani B., Simmer K., Patole S.K., Rao S.C. Long chain polyunsaturated fatty acid supplementation in infants born at term. Cochrane Database Syst. Rev. 2017;2017:CD000376. doi: 10.1002/14651858.CD000376.pub4.
    1. Delgado-Noguera M.F., Calvache J.A., Bonfill Cosp X., Kotanidou E.P., Galli-Tsinopoulou A. Supplementation with long chain polyunsaturated fatty acids (LCPUFA) to breastfeeding mothers for improving child growth and development. Cochrane Database Syst. Rev. 2015;2015:CD007901. doi: 10.1002/14651858.CD007901.pub3.
    1. Schneider N., Hauser J., Oliveira M., Cazaubon E., Mottaz S.C., O’Neill B.V., Steiner P., Deoni S.C.L. Sphingomyelin in Brain and Cognitive Development: Preliminary Data. eNeuro. 2019;6:ENEURO.0421-18.2019. doi: 10.1523/ENEURO.0421-18.2019.
    1. Perea-Sanz L., Garcia-Llatas G., Lagarda M.J. Gangliosides in human milk and infant formula: A review on analytical techniques and contents. Food Rev. Int. 2017;34:511–538. doi: 10.1080/87559129.2017.1347671.
    1. Rahmann H. Brain gangliosides and memory formation. Behav. Brain Res. 1995;66:105–116. doi: 10.1016/0166-4328(94)00131-X.
    1. Rösner H. Developmental expression and possible roles of gangliosides in brain development. Prog. Mol. Subcell. Biol. 2003;32:49–73. doi: 10.1007/978-3-642-55557-2_3.
    1. Berger P.K., Plows J.F., Jones R.B., Alderete T.L., Yonemitsu C., Poulsen M., Ryoo J.H., Peterson B.S., Bode L., Goran M.I. Human milk oligosaccharide 2’-fucosyllactose links feedings at 1 month to cognitive development at 24 months in infants of normal and overweight mothers. PLoS ONE. 2020;15:e0228323. doi: 10.1371/journal.pone.0228323.
    1. Boylan L.M., Hart S., Porter K.B., Driskell J.A. Vitamin B-6 content of breast milk and neonatal behavioral functioning. J. Am. Diet. Assoc. 2002;102:1433–1438. doi: 10.1016/S0002-8223(02)90317-2.
    1. Zielinska M.A., Hamulka J., Grabowicz-Chadrzyńska I., Bryś J., Wesolowska A. Association between Breastmilk LC PUFA, Carotenoids and Psychomotor Development of Exclusively Breastfed Infants. Int. J. Environ. Res. Public Health. 2019;16:1144. doi: 10.3390/ijerph16071144.
    1. Chen Y., Zheng Z., Zhu X., Shi Y., Tian D., Zhao F., Liu N., Hüppi P.S., Troy F.A., 2nd, Wang B. Lactoferrin Promotes Early Neurodevelopment and Cognition in Postnatal Piglets by Upregulating the BDNF Signaling Pathway and Polysialylation. Mol. Neurobiol. 2015;52:256–269. doi: 10.1007/s12035-014-8856-9.
    1. van de Looij Y., Ginet V., Chatagner A., Toulotte A., Somm E., Hüppi P.S., Sizonenko S.V. Lactoferrin during lactation protects the immature hypoxic-ischemic rat brain. Ann. Clin. Transl. Neurol. 2014;1:955–967. doi: 10.1002/acn3.138.
    1. Patel A.L., Johnson T.J., Engstrom J.L., Fogg L.F., Jegier B.J., Bigger H.R., Meier P.P. Impact of Early Human Milk on Sepsis and Health Care Costs in Very Low Birth Weight Infants. J. Perinatol. 2013;33:514. doi: 10.1038/jp.2013.2.
    1. Hurley W.L., Theil P.K. Perspectives on Immunoglobulins in Colostrum and Milk. Nutrients. 2011;3:442–474. doi: 10.3390/nu3040442.
    1. Sørensen V., Rasmussen I.B., Sunvold V., Michaelsen T.E., Sandlie I. Structural requirements for incorporation of J chain into human IgM and IgA. Int. Immunol. 2000;12:19–27. doi: 10.1093/intimm/12.1.19.
    1. Thai J.D., Gregory K.E. Bioactive Factors in Human Breast Milk Attenuate Intestinal Inflammation during Early Life. Nutrients. 2020;12:581. doi: 10.3390/nu12020581.
    1. Newburg D.S., Peterson J.A., Ruiz-Palacios G.M., Matson D.O., Morrow A.L., Shults J., Guerrero M.L., Chaturvedi P., Newburg S.O., Scallan C.D., et al. Role of human-milk lactadherin in protectoin against symptomatic rotavirus infection. Lancet. 1998;351:1160–1164. doi: 10.1016/S0140-6736(97)10322-1.
    1. Das U.N. Arachidonic acid and other unsaturated fatty acids and some of their metabolites function as endogenous antimicrobial molecules: A review. J. Adv. Res. 2018;11:57. doi: 10.1016/j.jare.2018.01.001.
    1. Azagra-Boronat I., Massot-Cladera M., Mayneris-Perxachs J., Knipping K., Van’t Land B., Tims S., Stahl B., Garssen J., Franch À., Castell M. Immunomodulatory and Prebiotic Effects of 2’-Fucosyllactose in Suckling Rats. Front. Immunol. 2019;10:1773. doi: 10.3389/fimmu.2019.01773.
    1. M’Rabet L., Vos A.P., Boehm G., Garssen J. Breast-Feeding and Its Role in Early Development of the Immune System in Infants: Consequences for Health Later in Life. J. Nutr. 2008;138:1782S–1790S. doi: 10.1093/jn/138.9.1782S.
    1. Comstock S.S., Reznikov E.A., Contractor N., Donovan S.M. Dietary bovine lactoferrin alters mucosal and systemic immune cell responses in neonatal piglets. J. Nutr. 2014;144:525–532. doi: 10.3945/jn.113.190264.
    1. Cacho N.T., Lawrence R.M. Innate Immunity and Breast Milk. Front. Immunol. 2017;8:584. doi: 10.3389/fimmu.2017.00584.
    1. Quitadamo P.A., Comegna L., Cristalli P. Anti-Infective, Anti-Inflammatory, and Immunomodulatory Properties of Breast Milk Factors for the Protection of Infants in the Pandemic From COVID-19. Front. Public Health. 2021;8:964. doi: 10.3389/fpubh.2020.589736.
    1. Chowning R., Radmacher P., Lewis S., Serke L., Pettit N., Adamkin D.H. A retrospective analysis of the effect of human milk on prevention of necrotizing enterocolitis and postnatal growth. J. Perinatol. 2015;36:221–224. doi: 10.1038/jp.2015.179.
    1. Herrmann K., Carroll K. An exclusively human milk diet reduces necrotizing enterocolitis. Breastfeed. Med. 2014;9:184–190. doi: 10.1089/bfm.2013.0121.
    1. Thomson P., Medina D.A., Garrido D. Human milk oligosaccharides and infant gut bifidobacteria: Molecular strategies for their utilization. Food Microbiol. 2018;75:37–46. doi: 10.1016/j.fm.2017.09.001.
    1. Arboleya S., Binetti A., Salazar N., Fernández N., Solís G., Hernández-Barranco A., Margolles A., de Los Reyes-Gavilán C.G., Gueimonde M. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol. Ecol. 2012;79:763–772. doi: 10.1111/j.1574-6941.2011.01261.x.
    1. Underwood M.A., Gaerlan S., De Leoz M.L., Dimapasoc L., Kalanetra K.M., Lemay D.G., German J.B., Mills D.A., Lebrilla C.B. Human Milk Oligosaccharides in Premature Infants: Absorption, Excretion and Influence on the Intestinal Microbiota. Pediatr. Res. 2015;78:670. doi: 10.1038/pr.2015.162.
    1. Lewis Z.T., Totten S.M., Smilowitz J.T., Popovic M., Parker E., Lemay D.G., Van Tassell M.L., Miller M.J., Jin Y.S., German J.B., et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome. 2015;3:13. doi: 10.1186/s40168-015-0071-z.
    1. Singh P., Sanchez-Fernandez L.L., Ramiro-Cortijo D., Ochoa-Allemant P., Perides G., Liu Y., Medina-Morales E., Yakah W., Freedman S.D., Martin C.R. Maltodextrin-induced intestinal injury in a neonatal mouse model. Dis. Model. Mech. 2020;13:dmm044776. doi: 10.1242/dmm.044776.
    1. Guglielmi F.W., Boggio-Bertinet D., Federico A., Forte G.B., Guglielmi A., Loguercio C., Mazzuoli S., Merli M., Palmo A., Panella C., et al. Total parenteral nutrition-related gastroenterological complications. Dig. Liver Dis. 2006;38:623–642. doi: 10.1016/j.dld.2006.04.002.
    1. Franco S., Goriacko P., Rosen O., Morgan-Joseph T. Incidence of Complications Associated with Parenteral Nutrition in Preterm Infants. JPEN J. Parenter. Enter. Nutr. 2021;45:1204–1212. doi: 10.1002/jpen.2011.
    1. Vohr B.R., Poindexter B.B., Dusick A.M., McKinley L.T., Higgins R.D., Langer J.C., Poole W.K. 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. doi: 10.1542/peds.2005-2382.
    1. Vohr B.R., Poindexter B.B., Dusick A.M., McKinley L.T., Higgins R.D., Langer J.C., Poole W.K. 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. doi: 10.1542/peds.2006-3227.
    1. Belfort M.B., Anderson P.J., Nowak V.A., Lee K.J., Molesworth C., Thompson D.K., Doyle L.W., Inder T.E. Breast Milk Feeding, Brain Development, and Neurocognitive Outcomes: A 7-Year Longitudinal Study in Infants Born at Less Than 30 Weeks’ Gestation. J. Pediatr. 2016;177:133–139.e1. doi: 10.1016/j.jpeds.2016.06.045.
    1. Ong M.L., Belfort M.B. Preterm infant nutrition and growth with a human milk diet. Semin. Perinatol. 2021;45:151383. doi: 10.1016/j.semperi.2020.151383.
    1. Hegar B., Wibowo Y., Basrowi R.W., Ranuh R.G., Sudarmo S.M., Munasir Z., Atthiyah A.F., Widodo A.D., Supriatmo Kadim M. The Role of Two Human Milk Oligosaccharides, 2′-Fucosyllactose and Lacto-N-Neotetraose, in Infant Nutrition. Pediatr. Gastroenterol. Hepatol. Nutr. 2019;22:330. doi: 10.5223/pghn.2019.22.4.330.
    1. Brown Belfort M. The Science of Breastfeeding and Brain Development. Breastfeed. Med. 2017;12:459. doi: 10.1089/bfm.2017.0122.
    1. Gu X., Shi X., Zhang L., Zhou Y., Cai Y., Jiang W., Zhou Q. Evidence summary of human milk fortifier in preterm infants. Transl. Pediatr. 2021;10:3058. doi: 10.21037/tp-21-476.
    1. Ryoo C.J., Kang N.M. Maternal Factors Affecting the Macronutrient Composition of Transitional Human Milk. Int. J. Environ. Res. Public Health. 2022;19:3308. doi: 10.3390/ijerph19063308.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться