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Research Paper

Human milk oligosaccharides, antimicrobial drugs, and the gut microbiota of term neonates: observations from the KOALA birth cohort study

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Article: 2164152 | Received 26 Aug 2022, Accepted 27 Dec 2022, Published online: 08 Jan 2023

References

  • Fujimura KE, Sitarik AR, Havstad S, Lin DL, Levan S, Fadrosh D, Panzer AR, LaMere B, Rackaityte E, Lukacs NW, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation. Nat Med. 2016;22(10):1187–17. doi:10.1038/nm.4176.
  • Zimmermann P, Messina N, Mohn W, Finlay B, Curtis N. Association between the intestinal microbiota and allergic sensitization, eczema, and asthma: a systematic review. J Allergy Clin Immunol. 2019;143(2):467–485. doi:10.1016/j.jaci.2018.09.025.
  • Dominguez-Bello MG, Godoy-Vitorino F, Knight R, Blaser MJ. Role of the microbiome in human development. Gut. 2019;68(6):1108–1114. doi:10.1136/gutjnl-2018-317503.
  • Mbakwa CA, Hermes GDA, Penders J, Savelkoul PHM, Thijs C, Dagnelie PC, Mommers M, Zoetendal EG, Smidt H, Arts ICW. Gut microbiota and body weight in school-aged children: the KOALA birth cohort study. Obesity. 2018;26(11):1767–1776. doi:10.1002/oby.22320.
  • Gasparrini AJ, Wang B, Sun X, Kennedy EA, Hernandez-Leyva A, Ndao IM, Tarr PI, Warner BB, Dantas G. Persistent metagenomic signatures of early-life hospitalization and antibiotic treatment in the infant gut microbiota and resistome. Nat Microbiol. 2019;4(12):2285–2297. doi:10.1038/s41564-019-0550-2.
  • van Daele E, Kamphorst K, Vlieger AM, Hermes G, Milani C, Ventura M, Belzer C, Smidt H, van ERM, Knol J. Effect of antibiotics in the first week of life on faecal microbiota development. Arch Dis Child - Fetal Neonatal Ed. 2022:fetalneonatal-2021–322861. doi:10.1136/archdischild-2021-322861.
  • Korpela K, Salonen A, Virta LJ, Kekkonen RA, Forslund K, Bork P, de VWM. Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children. Nat Commun. 2016;7(1):10410. doi:10.1038/ncomms10410.
  • van Tilburg Bernardes E, Pettersen VK, Gutierrez MW, Laforest-Lapointe I, Jendzjowsky NG, Cavin J-B, Vicentini FA, Keenan CM, Ramay HR, Samara J, et al. Intestinal fungi are causally implicated in microbiome assembly and immune development in mice. Nat Commun. 2020;11(1):2577. doi:10.1038/s41467-020-16431-1.
  • Heng X, Jiang Y, Chu W. Influence of fluconazole administration on gut microbiome, intestinal barrier, and immune response in mice. Antimicrob Agents Chemother. 2021;65(6):e02552–20. doi:10.1128/AAC.02552-20.
  • Alhasan MM, Cait AM, Heimesaat MM, Blaut M, Klopfleisch R, Wedel A, Conlon TM, Yildirim AÖ, Sodemann EB, Mohn WW, et al. Antibiotic use during pregnancy increases offspring asthma severity in a dose-dependent manner. Allergy. 2020;75(8):1979–1990. doi:10.1111/all.14234.
  • Blaser MJ, Bello MGD. Maternal antibiotic use and risk of asthma in offspring. Lancet Respir Med. 2014;2(10):e16. doi:10.1016/S2213-2600(14)70219-X.
  • Chen C-M, Chou H-C, Y-CSH Y. Maternal antibiotic treatment disrupts the intestinal microbiota and intestinal development in neonatal mice. Front Microbiol. 2021;12:1356. doi:10.3389/fmicb.2021.684233.
  • Grech A, Collins CE, Holmes AJ, Lal R, Duncanson K, Taylor RM, Gordon A. Maternal exposures and the infant gut microbiome: a systematic review with meta-analysis. Gut Microbes. 2021;13(1):1–30. doi:10.1080/19490976.2021.1897210.
  • Kuperman AA, Koren O. Antibiotic use during pregnancy: how bad is it? BMC Med. 2016;14(1):91. doi:10.1186/s12916-016-0636-0.
  • Metsälä J, Lundqvist A, Virta LJ, Kaila M, Gissler M, Virtanen SM. Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2015;45(1):137–145. doi:10.1111/cea.12356.
  • Zhang M, Differding MK, Benjamin-Neelon SE, Østbye T, Hoyo C, Mueller NT. Association of prenatal antibiotics with measures of infant adiposity and the gut microbiome. Ann Clin Microbiol Antimicrob. 2019;18(1):18. doi:10.1186/s12941-019-0318-9.
  • Ambrogi V, Bottacini F, Cao L, Kuipers B, Schoterman M, van Sinderen D. Galacto-oligosaccharides as infant prebiotics: production, application, bioactive activities and future perspectives. Crit Rev Food Sci Nutr. 2021; 1–14. doi:10.1080/10408398.2021.1953437.
  • Dogra SK, Martin F-P, Donnicola D, Julita M, Berger B, Sprenger N. Human milk oligosaccharide-stimulated Bifidobacterium species contribute to prevent later respiratory tract infections. Microorganisms. 2021;9(9):1939. doi:10.3390/microorganisms9091939.
  • Thurl S, Munzert M, Boehm G, Matthews C, Stahl B. Systematic review of the concentrations of oligosaccharides in human milk. Nutr Rev. 2017;75(11):920–933. doi:10.1093/nutrit/nux044.
  • Bode L. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology. 2012;22(9):1147–1162. doi:10.1093/glycob/cws074.
  • Borewicz K, Gu F, Saccenti E, Arts ICW, Penders J, Thijs C, van Leeuwen SS, Lindner C, Nauta A, van Leusen E, et al. Correlating infant faecal microbiota composition and human milk oligosaccharide consumption by microbiota of one-month old breastfed infants. Mol Nutr Food Res. 2019;63(13):1801214. doi:10.1002/mnfr.201801214.
  • Borewicz K, Gu F, Saccenti E, Hechler C, Beijers R, de Weerth C, van Leeuwen Ss, Schols HA, Smidt H, van Leeuwen SS. The association between breast milk oligosaccharides and faecal microbiota in healthy breastfed infants at two, six, and twelve weeks of age. Sci Rep. 2020;10(1):4270. doi:10.1038/s41598-020-61024-z.
  • Korpela K, Salonen A, Hickman B, Kunz C, Sprenger N, Kukkonen K, Savilahti E, Kuitunen M, de Vos WM. Fucosylated oligosaccharides in mother’s milk alleviate the effects of caesarean birth on infant gut microbiota. Sci Rep. 2018;8(1):13757. doi:10.1038/s41598-018-32037-6.
  • Laursen MF, Pekmez CT, Larsson MW, Lind MV, Yonemitsu C, Larnkjær A, Mølgaard C, Bode L, Dragsted LO, Michaelsen KF, et al. Maternal milk microbiota and oligosaccharides contribute to the infant gut microbiota assembly. ISME Commun. 2021;1(1):1–13. doi:10.1038/s43705-021-00021-3.
  • Bai Y, Tao J, Zhou J, Fan Q, Liu M, Hu Y, Xu Y, Zhang L, Yuan J, Li W, et al. Fucosylated human milk oligosaccharides and N-glycans in the milk of Chinese mothers regulate the gut microbiome of their breast-fed infants during different lactation stages. mSystems. 2018;3(6):e00206–18. doi: 10.1128/mSystems.00206-18.
  • Lewis ZT, Totten SM, Smilowitz JT, Popovic M, Parker E, Lemay DG, Van Tassell ML, Miller MJ, Jin Y-S, German JB, et al. Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome. 2015;3(1):13. doi:10.1186/s40168-015-0071-z.
  • Arrieta M-C, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, Kuzeljevic B, Gold MJ, Britton HM, Lefebvre DL, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015;7(307):307ra152–307ra152. doi:10.1126/scitranslmed.aab2271.
  • Galazzo G, van BN, Bervoets L, Dapaah IO, Savelkoul PH, Hornef MW, Hutton EK, Morrison K, Holloway AC, McDonald H, et al. Development of the microbiota and associations with birth mode, diet, and atopic disorders in a longitudinal analysis of stool samples, collected from infancy through early childhood. Gastroenterology. 2020;158(6):1584–1596. doi:10.1053/j.gastro.2020.01.024.
  • Mitchell CM, Mazzoni C, Hogstrom L, Bryant A, Bergerat A, Cher A, Pochan S, Herman P, Carrigan M, Sharp K, et al. Delivery mode affects stability of early infant gut microbiota. Cell Rep Med. 2020;1(9):100156. doi:10.1016/j.xcrm.2020.100156.
  • Reyman M, van Houten Ma, van Baarle D, Aatm B, Man WH, MLJN C, Arp K, Watson RL, Sanders EAM, Fuentes S, et al. Impact of delivery mode-associated gut microbiota dynamics on health in the first year of life. Nat Commun. 2019;10(1):4997. doi:10.1038/s41467-019-13014-7.
  • Shao Y, Forster SC, Tsaliki E, Vervier K, Strang A, Simpson N, Kumar N, Stares MD, Rodger A, Brocklehurst P, et al. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019;574(7776):117–121. doi:10.1038/s41586-019-1560-1.
  • Stewart CJ, Ajami NJ, O’Brien JL, Hutchinson DS, Smith DP, Wong MC, Ross MC, Lloyd RE, Doddapaneni H, Metcalf GA, et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature. 2018;562(7728):583. doi:10.1038/s41586-018-0617-x.
  • Lewis ZT, Sidamonidze K, Tsaturyan V, Tsereteli D, Khachidze N, Pepoyan A, Zhgenti E, Tevzadze L, Manvelyan A, Balayan M, et al. The fecal microbial community of breast-fed infants from Armenia and Georgia. Sci Rep. 2017;7(1):40932. doi:10.1038/srep40932.
  • Marcobal A, Barboza M, Froehlich JW, Block DE, German JB, Lebrilla CB, Mills DA. Consumption of human milk oligosaccharides by gut-related microbes. J Agric Food Chem. 2010;58(9):5334–5340. doi:10.1021/jf9044205.
  • Jost T, Lacroix C, Braegger C, Chassard C. Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr Rev. 2015;73(7):426–437. doi:10.1093/nutrit/nuu016.
  • Walsh C, Lane JA, van Sinderen D, Hickey RM. From lab bench to formulated ingredient: characterization, production, and commercialization of human milk oligosaccharides. J Funct Foods. 2020;72:104052. doi:10.1016/j.jff.2020.104052.
  • Azad MB, Robertson B, Atakora F, Becker AB, Subbarao P, Moraes TJ, Mandhane PJ, Turvey SE, Lefebvre DL, Sears MR, et al. Human milk oligosaccharide concentrations are associated with multiple fixed and modifiable maternal characteristics, environmental factors, and feeding practices. J Nutr. 2018;148(11):1733–1742. doi:10.1093/jn/nxy175.
  • Samuel TM, Binia A, Castro CAD, Thakkar SK, Billeaud C, Agosti M, Al-Jashi I, Costeira MJ, Marchini G, Martínez-Costa C, et al. Impact of maternal characteristics on human milk oligosaccharide composition over the first 4 months of lactation in a cohort of healthy European mothers. Sci Rep. 2019;9(1). doi:10.1038/s41598-019-48337-4
  • Berger B, Porta N, Foata F, Grathwohl D, Delley M, Moine D, Charpagne A, Siegwald L, Descombes P, Alliet P, et al. Linking human milk oligosaccharides, infant fecal community types, and later risk to require antibiotics. mBio. 2020;11(2):e03196–19. doi: 10.1128/mBio.03196-19.
  • Cheng L, Kiewiet MBG, Groeneveld A, Nauta A, de VP. Human milk oligosaccharides and its acid hydrolysate LNT2 show immunomodulatory effects via TLRs in a dose and structure-dependent way. J Funct Foods. 2019;59:174–184. doi:10.1016/j.jff.2019.05.023.
  • Goehring KC, Marriage BJ, Oliver JS, Wilder JA, Barrett EG, Buck RH. Similar to those who are breastfed, infants fed a formula containing 2’-fucosyllactose have lower inflammatory cytokines in a randomized controlled trial. J Nutr. 2016;146(12):2559–2566. doi:10.3945/jn.116.236919.
  • Sodhi CP, Wipf P, Yamaguchi Y, Fulton WB, Kovler M, Niño DF, Zhou Q, Banfield E, Werts AD, Ladd MR, et al. The human milk oligosaccharides 2’-fucosyllactose and 6’-sialyllactose protect against the development of necrotizing enterocolitis by inhibiting toll-like receptor 4 signaling. Pediatr Res. 2021;89(1):91–101. doi:10.1038/s41390-020-0852-3.
  • Masi AC, Embleton ND, Lamb CA, Young G, Granger CL, Najera J, Smith DP, Hoffman KL, Petrosino JF, Bode L, et al. Human milk oligosaccharide DSLNT and gut microbiome in preterm infants predicts necrotising enterocolitis. Gut. 2021;70(12):2273–2282. doi:10.1136/gutjnl-2020-322771.
  • Böger M, van Leeuwen SS, Lammerts van Bueren A, Dijkhuizen L. Structural identity of galactooligosaccharide molecules selectively utilized by single cultures of probiotic bacterial strains. J Agric Food Chem. 2019;67(50):13969–13977. doi:10.1021/acs.jafc.9b05968.
  • Schoster A, Kokotovic B, Permin A, Pedersen PD, Dal Bello F, Guardabassi L. In vitro inhibition of clostridium difficile and Clostridium perfringens by commercial probiotic strains. Anaerobe. 2013;20:36–41. doi:10.1016/j.anaerobe.2013.02.006.
  • Shieh M-J, Shang H, Liao F-H, Zhu J-S, Chien Y-W. Lactobacillus fermentum improved intestinal bacteria flora by reducing Clostridium perfringens. E-SPEN Eur E-J Clin Nutr Metab. 2011;6(2):e59–e63. doi:10.1016/j.eclnm.2011.01.001.
  • Borewicz K, Suarez-Diez M, Hechler C, Beijers R, de Weerth C, Arts I, Penders J, Thijs C, Nauta A, Lindner C, et al. The effect of prebiotic fortified infant formulas on microbiota composition and dynamics in early life. Sci Rep. 2019;9(1):2434. doi:10.1038/s41598-018-38268-x.
  • Dorado-García A, Smid JH, van Pelt W, Bonten MJM, Fluit AC, van den Bunt G, Wagenaar JA, Hordijk J, Dierikx CM, Veldman KT, et al. Molecular relatedness of ESBL/AmpC-producing Escherichia coli from humans, animals, food and the environment: a pooled analysis. J Antimicrob Chemother. 2018;73(2):339–347. doi:10.1093/jac/dkx397.
  • Kiu R, Caim S, Alexander S, Pachori P, Hall LJ, Hall LJ. Probing genomic aspects of the multi-host pathogen Clostridium perfringens reveals significant pangenome diversity, and a diverse array of virulence factors. Front Microbiol. 2017:8. doi: 10.3389/fmicb.2017.02485.
  • Gibson MK, Crofts TS, Dantas G. Antibiotics and the developing infant gut microbiota and resistome. Curr Opin Microbiol. 2015;27:51–56. doi:10.1016/j.mib.2015.07.007.
  • Shaw AG, Cornwell E, Sim K, Thrower H, Scott H, Brown JCS, Dixon RA, Kroll JS. Dynamics of toxigenic Clostridium perfringens colonisation in a cohort of prematurely born neonatal infants. BMC Pediatr. 2020;20(1):75. doi:10.1186/s12887-020-1976-7.
  • Reyman M, van Houten MA, Watson RL, Chu MLJN, Arp K, de Waal WJ, Schiering I, Plötz FB, Willems RJL, 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):893. doi:10.1038/s41467-022-28525-z.
  • Stokholm J, Blaser MJ, Thorsen J, Rasmussen MA, Waage J, Vinding RK, Schoos A-M-M, Kunøe A, Fink NR, Chawes BL, et al. Maturation of the gut microbiome and risk of asthma in childhood. Nat Commun. 2018;9(1):141. doi:10.1038/s41467-017-02573-2.
  • Penders J, Gerhold K, Stobberingh EE, Thijs C, Zimmermann K, Lau S, Hamelmann E. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol. 2013;132(3):601–607.e8. doi:10.1016/j.jaci.2013.05.043.
  • Dierikx T, Berkhout D, Eck A, Tims S, van LJ, Visser D, de BM, de BN, Touw D, Benninga M, et al. Influence of timing of maternal antibiotic administration during caesarean section on infant microbial colonisation: a randomised controlled trial. Gut. 2021;71(9):1803–1811. doi:10.1136/gutjnl-2021-324767.
  • Arnal M-E, Zhang J, Erridge C, Smidt H, Lallès J-P. Maternal antibiotic-induced early changes in microbial colonization selectively modulate colonic permeability and inducible heat shock proteins, and digesta concentrations of alkaline phosphatase and TLR-stimulants in swine offspring. PLOS ONE. 2015;10(2):e0118092. doi:10.1371/journal.pone.0118092.
  • Roswall J, Olsson LM, Kovatcheva-Datchary P, Nilsson S, Tremaroli V, Simon M-C, Kiilerich P, Akrami R, Krämer M, Uhlén M, et al. Developmental trajectory of the healthy human gut microbiota during the first 5 years of life. Cell Host Microbe. 2021;29(5):765–776.e3. doi:10.1016/j.chom.2021.02.021.
  • de AMG, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, Steinert A, Heikenwalder M, Hapfelmeier S, Sauer U, et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;351(6279):1296–1302. doi:10.1126/science.aad2571.
  • Kummeling I, Thijs C, Penders J, Snijders BEP, Stelma F, Reimerink J, Koopmans M, Dagnelie PC, Huber M, Jansen MCJF, et al. Etiology of atopy in infancy: the KOALA birth cohort study. Pediatr Allergy Immunol. 2005;16(8):679–684. doi:10.1111/j.1399-3038.2005.00333.x.
  • Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt Pa, Stobberingh EE, van den Brandt PA. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–521. doi:10.1542/peds.2005-2824.
  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci. 2011;108(Supplement 1):4516–4522. doi:10.1073/pnas.1000080107.
  • Poncheewin W, Hermes GDA, de Groot, van Dam Jcj SWJ, Koehorst JJ, Smidt H, Schaap PJ. NG-Tax 2.0: a semantic framework for high-throughput amplicon analysis. Front Genet. 2020;11:10. doi:10.3389/fgene.2019.01366.
  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–D596. doi:10.1093/nar/gks1219.
  • Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27(4):592–593. doi:10.1093/bioinformatics/btq706.
  • Gu F, ten KGA, Arts ICW, Penders J, Thijs C, Lindner C, Nauta A, van Leusen E, van Leeuwen Ss, Schols HA, et al. Combining HPAEC-PAD, PGC-LC–MS, and 1D 1 H NMR to investigate metabolic fates of human milk oligosaccharides in 1-month-Old infants: a pilot study. J Agric Food Chem. 2021;69(23):6495–6509. doi:10.1021/acs.jafc.0c07446.
  • R Core Team. 2022. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
  • Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ. Microbiome datasets are compositional: and this is not optional. Front Microbiol. 2017;8 8(NOV). doi: 10.3389/fmicb.2017.02224.
  • Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, Minchin P, O'Hara R, Solymos P, et al., Vegan: Community Ecology Package. R package version 2.6-4. Internet. https://CRAN.R-project.org/package=vegan.
  • Chen J, Bittinger K, Charlson ES, Hoffmann C, Lewis J, Wu GD, Collman RG, Bushman FD, Li H. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics. 2012;28(16):2106–2113. doi:10.1093/bioinformatics/bts342.
  • Mallick H, Rahnavard A, McIver LJ, Ma S, Zhang Y, Nguyen LH, Tickle TL, Weingart G, Ren B, Schwager EH, et al. Multivariable association discovery in population-scale meta-omics studies. PLOS Comput Biol. 2021;17(11):e1009442. doi:10.1371/journal.pcbi.1009442.
  • Barnett DJM, Arts ICW, Penders J. microViz: an R package for microbiome data visualization and statistics. J Open Source Softw. 2021;6(63):3201. doi:10.21105/joss.03201.