Impact of milk secretor status on the fecal metabolome and microbiota of breastfed infants

References

• Smilowitz JT, O’Sullivan A, Barile D, German JB, Lönnerdal B, Slupsky CM. The human milk metabolome reveals diverse oligosaccharide profiles. J Nutr. 2013;143(11):1709–15. doi:10.3945/jn.113.178772.
   PubMed Web of Science ®Google Scholar
• Spevacek AR, Smilowitz JT, Chin EL, Underwood MA, German JB, Slupsky CM. Infant maturity at birth reveals minor differences in the maternal milk metabolome in the first month of lactation. J Nutr. 2015;145(8):1698–1708. doi:10.3945/jn.115.210252.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Durham SD, Robinson RC, Olga L, Ong KK, Chichlowski M, Dunger DB, Barile D. A one-year study of human milk oligosaccharide profiles in the milk of healthy UK mothers and their relationship to maternal FUT2 genotype. Glycobiology. 2021;31(10):1254–1267. doi:10.1093/glycob/cwab057.
   PubMed Web of Science ®Google Scholar
• Thurl S, Munzert M, Henker J, Boehm G, Müller-Werner B, Jelinek J, Stahl B. Variation of human milk oligosaccharides in relation to milk groups and lactational periods. Br J Nutr. 2010;104(9):1261–1271. doi:10.1017/S0007114510002072.
   PubMed Web of Science ®Google Scholar
• Totten SM, Zivkovic AM, Wu S, Ngyuen U, Freeman SL, Ruhaak LR, Darboe MK, German JB, Prentice AM, Lebrilla CB, et al. Comprehensive profiles of human milk oligosaccharides yield highly sensitive and specific markers for determining secretor status in lactating mothers. J Proteome Res. 2012;11(12):6124–6133. doi:10.1021/pr300769g.
   PubMed Web of Science ®Google Scholar
• Newburg DS, Ruiz-Palacios GM, Morrow AL. Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr. 2005;25(1):37–58. doi:10.1146/annurev.nutr.25.050304.092553.
   PubMed Web of Science ®Google Scholar
• Kunz C, Meyer C, Collado MC, Geiger L, García-Mantrana I, Bertua-Ríos B, Martínez-Costa C, Borsch C, Rudloff S. Influence of gestational age, secretor, and Lewis blood group status on the oligosaccharide content of human milk. J Pediatr Gastroenterol Nutr. 2017;64(5):789–798. doi:10.1097/MPG.0000000000001402.
   PubMed Web of Science ®Google Scholar
• Underwood MA, Gaerlan S, De Leoz MLA, Dimapasoc L, Kalanetra KM, Lemay DG, German JB, Mills DA, Lebrilla CB. Human milk oligosaccharides in premature infants: absorption, excretion, and influence on the intestinal microbiota. Pediatr Res. 2015;78(6):670. doi:10.1038/pr.2015.162.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Smith-Brown P, Morrison M, Krause L, Davies PSW. Mother’s secretor status affects development of children’s microbiota composition and function: a pilot study. PloS One. 2016;11(9):e0161211. doi:10.1371/journal.pone.0161211.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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):21. doi:10.1038/s43705-021-00021-3.
   PubMedGoogle Scholar
• Wang M, Li M, Wu S, Lebrilla CB, Chapkin RS, Ivanov I, Donovan SM. Fecal microbiota composition of breast-fed infants is correlated with human milk oligosaccharides consumed. J Pediatr Gastroenterol Nutr. 2015;60(6):825–833. doi:10.1097/MPG.0000000000000752.
   PubMed Web of Science ®Google Scholar
• Medoua GN, Sajo Nana EC, Ndzana ACA, Makamto CS, Etame LS, Rikong HA, Oyono JLE. Breastfeeding practices of Cameroonian mothers determined by dietary recall since birth and the dose-to-the-mother deuterium-oxide turnover technique. Matern Child Nutr. 2012;8(3):330–339. doi:10.1111/j.1740-8709.2011.00293.x.
   PubMed Web of Science ®Google Scholar
• Mazariegos M, Slater C, Ramirez-Zea M. Validity of Guatemalan mother’s self-reported breast-feeding practices of 3-month-old infants. Food Nutr Bull. 2016;37(4):494–503. doi:10.1177/0379572116654644.
   PubMed Web of Science ®Google Scholar
• Wang A, Koleva P, du Toit E, Geddes DT, Munblit D, Prescott SL, Eggesbø M, Johnson CC, Wegienka G, Shimojo N, et al. The milk metabolome of non-secretor and Lewis negative mothers. Front Nutr. 2021;7:576966. doi:10.3389/fnut.2020.576966.
   PubMed Web of Science ®Google Scholar
• Bunesova V, Lacroix C, Schwab C. Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense. BMC Microbiol. 2016;16(1):248. doi:10.1186/s12866-016-0867-4.
   PubMedGoogle Scholar
• Henrick BM, Hutton AA, Palumbo MC, Casaburi G, Mitchell RD, Underwood MA, Smilowitz JT, Frese SA. Elevated fecal pH indicates a profound change in the breastfed infant gut microbiome due to reduction of Bifidobacterium over the past century. mSphere. 2018;3(2):e00041–18. doi:10.1128/mSphere.00041-18.
   PubMed Web of Science ®Google Scholar
• Casaburi G, Duar RM, Brown H, Mitchell RD, Kazi S, Chew S, Cagney O, Flannery RL, Sylvester KG, Frese SA, et al. Metagenomic insights of the infant microbiome community structure and function across multiple sites in the United States. Sci Rep. 2021;11(1):1472. doi:10.1038/s41598-020-80583-9.
   PubMed Web of Science ®Google Scholar
• Duranti S, Lugli GA, Mancabelli L, Turroni F, Milani C, Mangifesta M, Ferrario C, Anzalone R, Viappiani A, van Sinderen D, et al. Prevalence of antibiotic resistance genes among human gut-derived bifidobacteria. Appl Environ Microbiol. 2017;83(3). doi:10.1128/AEM.02894-16.
   PubMed Web of Science ®Google Scholar
• Betrán AP, Ye J, Moller AB, Zhang J, Gülmezoglu AM, Torloni MR, Zeeb H. The increasing trend in caesarean section rates: global, regional and national estimates: 1990-2014. PloS One. 2016;11(2):e0148343. doi:10.1371/journal.pone.0148343.
   PubMed Web of Science ®Google Scholar
• Underwood MA, German JB, Lebrilla CB, Mills DA. Bifidobacterium longum subspecies infantis: champion colonizer of the infant gut. Pediatr Res. 2014;77(1–2):229. doi:10.1038/pr.2014.156.
   PubMed Web of Science ®Google Scholar
• Ruiz-Moyano S, Totten SM, Garrido DA, Smilowitz JT, German JB, Lebrilla CB, Mills DA. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol. 2013;79(19):6040–6049. doi:10.1128/AEM.01843-13.
   PubMed Web of Science ®Google Scholar
• Zabel B, Yde CC, Roos P, Marcussen J, Jensen HM, Salli K, Hirvonen J, Ouwehand AC, Morovic W. Novel genes and metabolite trends in Bifidobacterium longum subsp. infantis bi-26 metabolism of human milk oligosaccharide 2′-fucosyllactose. Sci Rep. 2019;9(1):7983. doi:10.1038/s41598-019-43780-9.
   PubMedGoogle Scholar
• Dedon LR, Özcan E, Rani A, Sela DA. Bifidobacterium infantis metabolizes 2′fucosyllactose-derived and free fucose through a common catabolic pathway resulting in 1,2-propanediol secretion. Front Nutr. 2020;7:237. doi:10.3389/fnut.2020.583397.
   Web of Science ®Google Scholar
• Cheng CC, Duar RM, Lin X, Perez-Munoz ME, Tollenaar S, Oh J-H, van Pijkeren J-P, Li F, van Sinderen D, Gänzle MG, et al. Ecological importance of cross-feeding of the intermediate metabolite 1,2-propanediol between bacterial gut symbionts. Appl Environ Microbiol. 2020;86(11):e00190–20. doi:10.1128/AEM.00190-20.
   PubMed Web of Science ®Google Scholar
• Ariake K, Ohkusa T, Sakurazawa T, Kumagai J, Eishi Y, Hoshi S, Yajima T. Roles of mucosal bacteria and succinic acid in colitis caused by dextran sulfate sodium in mice. J Med Dent Sci. 2000;47:233–241.
   PubMedGoogle Scholar
• Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13(9):R79. doi:10.1186/gb-2012-13-9-r79.
   PubMed Web of Science ®Google Scholar
• Kim YG, Sakamoto K, Seo SU, Pickard JM, Gillilland MG, Pudlo NA, Hoostal M, Li X, Wang TD, Feehley T, et al. Neonatal acquisition of Clostridia species protects against colonization by bacterial pathogens. Sci. 2017;356(6335):315. doi:10.1126/science.aag2029.
   PubMed Web of Science ®Google Scholar
• Raheem RA, Binns CW, Chih HJ. Protective effects of breastfeeding against acute respiratory tract infections and diarrhoea: findings of a cohort study. J Paediatr Child Health. 2017;53(3):271–276. doi:10.1111/jpc.13480.
   PubMed Web of Science ®Google Scholar
• Tromp I, Kiefte-de Jong J, Raat H, Jaddoe V, Franco O, Hofman A, de Jongste J, Moll H. Breastfeeding and the risk of respiratory tract infections after infancy: the generation R study. PloS One. 2017;12(2):e0172763. doi:10.1371/journal.pone.0172763.
   PubMed Web of Science ®Google Scholar
• Stepans MBF, Wilhelm SL, Hertzog M, Rodehorst TKC, Blaney S, Clemens B, Polak JJ, Newburg DS. Early consumption of human milk oligosaccharides is inversely related to subsequent risk of respiratory and enteric disease in infants. Breastfeed Med Off J Acad Breastfeed Med. 2006;1(4):207–215. doi:10.1089/bfm.2006.1.207.
   PubMed Web of Science ®Google Scholar
• Puccio G, Alliet P, Cajozzo C, Janssens E, Corsello G, Sprenger N, Wernimont S, Egli D, Gosoniu L, Steenhout P, et al. Effects of infant formula with human milk oligosaccharides on growth and morbidity: a randomized multicenter trial. J Pediatr Gastroenterol Nutr. 2017;64(4):624–631. doi:10.1097/MPG.0000000000001520.
   PubMed Web of Science ®Google Scholar
• Duska-McEwen G, Senft AP, Ruetschilling TL, Barrett EG, Buck RH. Human milk oligosaccharides enhance innate immunity to respiratory syncytial virus and influenza in vitro. Food Nutr Sci. 2014;5:1387–1398. doi:10.4236/fns.2014.514151.
   Google Scholar
• de Souza Oliveira RP, Perego P, de Oliveira MN, Converti A. Growth, organic acids profile and sugar metabolism of Bifidobacterium lactis in co-culture with Streptococcus thermophilus: the inulin effect. Food Research International query. 2012;48(1):21–27. doi:10.1016/j.foodres.2012.02.012.
   Web of Science ®Google Scholar
• He X, Parenti M, Grip T, Lönnerdal B, Timby N, Domellöf M, Hernell O, Slupsky CM. Fecal microbiome and metabolome of infants fed bovine MFGM supplemented formula or standard formula with breast-fed infants as reference: a randomized controlled trial. Sci Rep. 2019;9(1):11589. doi:10.1038/s41598-019-47953-4.
   PubMedGoogle Scholar
• Beloborodova N, Bairamov I, Olenin A, Shubina V, Teplova V, Fedotcheva N. Effect of phenolic acids of microbial origin on production of reactive oxygen species in mitochondria and neutrophils. J Biomed Sci. 2012;19(1):89. doi:10.1186/1423-0127-19-89.
   PubMedGoogle Scholar
• Windey K, De Preter V, Verbeke K. Relevance of protein fermentation to gut health. Mol Nutr Food Res. 2012;56(1):184–196. doi:10.1002/mnfr.201100542.
   PubMed Web of Science ®Google Scholar
• Laursen MF, Sakanaka M, von Burg N, Mörbe U, Andersen D, Moll JM, Pekmez CT, Rivollier A, Michaelsen KF, Mølgaard C. Breastmilk-promoted bifidobacteria produce aromatic amino acids in the infant gut. bioRxiv. Published online 2020 Jan 1; 2020–2021. 10.1101/2020.01.22.914994.
   Google Scholar
• Peirotén A, Gaya P, Arqués JL, Medina M, Rodríguez E. Technological properties of bifidobacterial strains shared by mother and child. BioMed Res Int. 2019;2019:9814623. doi:10.1155/2019/9814623.
   PubMed Web of Science ®Google Scholar
• Yu ZT, Chen C, Newburg DS. Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology. 2013;23(11):1281–1292. doi:10.1093/glycob/cwt065.
   PubMed Web of Science ®Google Scholar
• Ehrlich AM, Pacheco AR, Henrick BM, Taft D, Xu G, Huda MN, Mishchuk D, Goodson ML, Slupsky C, Barile D, et al. Indole-3-lactic acid associated with Bifidobacterium-dominated microbiota significantly decreases inflammation in intestinal epithelial cells. BMC Microbiol. 2020;20(1):357. doi:10.1186/s12866-020-02023-y.
   PubMed Web of Science ®Google Scholar
• Sakurai T, Odamaki T, Xiao JZ. Production of indole-3-lactic acid by Bifidobacterium strains isolated from human infants. Microorganisms. 2019;7(9):340. doi:10.3390/microorganisms7090340.
   PubMed Web of Science ®Google Scholar
• Larke JA, Kuhn-Riordon K, Taft DH, Sohn K, Iqbal S, Underwood MA, Mills DA, Slupsky CM. Preterm infant fecal microbiota and metabolite profiles are modulated in a probiotic specific manner. J Pediatr Gastroenterol Nutr. 2022;75(4):535–542. doi:10.1097/MPG.0000000000003570.
   PubMed Web of Science ®Google Scholar
• Muthumuni D, Miliku K, Wade KH, Timpson NJ, Azad MB. Enhanced protection against diarrhea among breastfed infants of nonsecretor mothers. Pediatr Infect Dis J. 2021;40(3):260–263. doi:10.1097/INF.0000000000003014.
   PubMed Web of Science ®Google Scholar
• Thorven M, Grahn A, Hedlund KO, Johansson H, Wahlfrid C, Larson G, Svensson L. A homozygous nonsense mutation (428G→A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J Virol. 2005;79(24):15351. doi:10.1128/JVI.79.24.15351-15355.2005.
   PubMed Web of Science ®Google Scholar
• Liu Z, Diana A, Slater C, Preston T, Gibson RS, Houghton L, Duffull SB. Development of a nonlinear hierarchical model to describe the disposition of deuterium in mother–infant pairs to assess exclusive breastfeeding practice. J Pharmacokinet Pharmacodyn. 2019;46(1):1–13. doi:10.1007/s10928-018-9613-x.
   PubMed Web of Science ®Google Scholar
• Leong C, Gibson RS, Diana A, Haszard JJ, Rahmannia S, Ansari MB, Inayah LS, Purnamasari AD, Houghton LA. Differences in micronutrient intakes of exclusive and partially breastfed Indonesian infants from resource-poor households are not accompanied by differences in micronutrient status, morbidity, or growth. J Nutr. 2021;151(3):705–715. doi:10.1093/jn/nxaa381.
   PubMed Web of Science ®Google Scholar
• Weljie AM, Newton J, Mercier P, Carlson E, Slupsky CM. Targeted profiling: quantitative analysis of 1H NMR metabolomics data. Anal Chem. 2006;78(13):4430–4442. doi:10.1021/ac060209g.
   PubMed Web of Science ®Google Scholar
• van Leeuwen SS, Dijkhuizen L, Gerwig GJ, Kamerling JP, van Leusen-van Kan EJM, Schoemaker RJW. Rapid milk group classification by 1H NMR analysis of Le and H epitopes in human milk oligosaccharide donor samples. Glycobiology. 2014;24(8):728–739. doi:10.1093/glycob/cwu036.
   PubMed Web of Science ®Google Scholar
• Praticò G, Capuani G, Tomassini A, Baldassarre ME, Delfini M, Miccheli A. Exploring human breast milk composition by NMR-based metabolomics. Nat Prod Res. 2014;28(2):95–101. doi:10.1080/14786419.2013.843180.
   PubMed Web of Science ®Google Scholar
• Wesolowska-Andersen A, Bahl MI, Carvalho V, Kristiansen K, Sicheritz-Pontén T, Gupta R, Licht TR. Choice of bacterial DNA extraction method from fecal material influences community structure as evaluated by metagenomic analysis. Microbiome. 2014;2(1):19. doi:10.1186/2049-2618-2-19.
   PubMed Web of Science ®Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glöckner FO, et al. The SILVA and “all-species living tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42(D1):D643–D648. doi:10.1093/nar/gkt1209.
   PubMed Web of Science ®Google Scholar
• Romano J, Kromrey JD, Coraggio J, Skowronek J. Appropriate statistics for ordinal level data: should we really be using t-test and Cohen’s d for evaluating group differences on the NSSE and other surveys. Annu Meet Florida Assoc Inst Res. 2006;177:34.
   Google Scholar