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Review

Maternal microbe-specific modulation of the offspring microbiome and development during pregnancy and lactation

, , , , , & ORCID Icon show all
Article: 2206505 | Received 24 Aug 2022, Accepted 17 Apr 2023, Published online: 15 May 2023

References

  • D’Argenio V, Salvatore F. The role of the gut microbiome in the healthy adult status. Clin Chim Acta. 2015;451(Pt A):97–24. doi:10.1016/j.cca.2015.01.003.
  • Sartor RB. Therapeutic correction of bacterial dysbiosis discovered by molecular techniques. Proc Natl Acad Sci U S A. 2008;105(43):16413–16414. doi:10.1073/pnas.0809363105.
  • Kerr CA, Grice DM, Tran CD, Bauer DC, Li D, Hendry P, Hannan GN. Early life events influence whole-of-life metabolic health via gut microflora and gut permeability. Crit Rev Microbiol. 2015;41(3):326–340. doi:10.3109/1040841X.2013.837863.
  • Sanidad KZ, Zeng MY. Neonatal gut microbiome and immunity. Curr Opin Microbiol. 2020;56:30–37. doi:10.1016/j.mib.2020.05.011.
  • Meckel KR, Kiraly DD. Maternal microbes support fetal brain wiring. Nature. 2020;586(7828):203–205. doi:10.1038/d41586-020-02657-y.
  • Koboziev I, Webb CR, Furr KL, Grisham MB. Role of the enteric microbiota in intestinal homeostasis and inflammation. Free Radical Biol Med. 2014;68:122–133. doi:10.1016/j.freeradbiomed.2013.11.008.
  • Warner BB, Deych E, Zhou Y, Hall-Moore C, Weinstock GM, Sodergren E, Shaikh N, Hoffmann JA, Linneman LA, Hamvas A, et al. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: a prospective case-control study. Lancet. 2016;387(10031):1928–1936. doi:10.1016/s0140-6736(16)00081-7.
  • Pammi M, Cope J, Tarr PI, Warner BB, Morrow AL, Mai V, Gregory KE, Kroll JS, McMurtry V, Ferris MJ, et al. Intestinal dysbiosis in preterm infants preceding necrotizing enterocolitis: a systematic review and meta-analysis. Microbiome. 2017;5(1):31. doi:10.1186/s40168-017-0248-8.
  • Stewart CJ, Embleton ND, Marrs ECL, Smith DP, Fofanova T, Nelson A, Skeath T, Perry JD, Petrosino JF, Berrington JE, et al. Longitudinal development of the gut microbiome and metabolome in preterm neonates with late onset sepsis and healthy controls. Microbiome. 2017;5(1):75. doi:10.1186/s40168-017-0295-1.
  • Mischke M, Arora T, Tims S, Engels E, Sommer N, van Limpt K, Baars A, Oozeer R, Oosting A, Bäckhed F, et al. Specific synbiotics in early life protect against diet‐induced obesity in adult mice. Diabetes Obes Metab. 2018;20(6):1408–1418. doi:10.1111/dom.13240.
  • Livanos AE, Greiner TU, Vangay P, Pathmasiri W, Stewart D, McRitchie S, Li H, Chung J, Sohn J, Kim S, et al. Antibiotic-mediated gut microbiome perturbation accelerates development of type 1 diabetes in mice. Nat Microbiol. 2016;1(11):16140. doi:10.1038/nmicrobiol.2016.140.
  • Stokholm J, Blaser MJ, Thorsen J, Rasmussen MA, Waage J, Vinding RK, Schoos AMM, 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.
  • Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO, Ruan Y. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5(7):e177. doi:10.1371/journal.pbio.0050177.
  • Lou YC, Olm MR, Diamond S, Crits-Christoph A, Firek BA, Baker R, Morowitz MJ, Banfield JF. Infant gut strain persistence is associated with maternal origin, phylogeny, and traits including surface adhesion and iron acquisition. Cell Rep Med. 2021;2(9):100393. doi:10.1016/j.xcrm.2021.100393.
  • Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470–480. doi:10.1016/j.cell.2012.07.008.
  • Yang HL, Guo RC, Li SC, Liang F, Tian C, Zhao XQ, Long Y, Liu F, Jiang M, Zhang Y, et al. Systematic analysis of gut microbiota in pregnant women and its correlations with individual heterogeneity. NPJ Biofilms Microbiomes. 2020;6(1):1–12. doi:10.1038/s41522-020-00142-y.
  • Jost T, Lacroix C, Braegger C, Chassard C. Stability of the maternal gut microbiota during late pregnancy and early lactation. Curr Microbiol. 2014;68(4):419–427. doi:10.1007/s00284-013-0491-6.
  • Collado MC, Isolauri E, Laitinen K, Salminen S. Effect of mother’s weight on infant’s microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am J Clin Nutr. 2010;92(5):1023–1030. doi:10.3945/ajcn.2010.29877.
  • Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008;88(4):894–899. doi:10.1093/ajcn/88.4.894.
  • Santacruz A, Collado MC, Garcia-Valdes L, Segura MT, Martin-Lagos JA, Anjos T, Marti-Romero M, Lopez RM, Florido J, Campoy C, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010;104(1):83–92. doi:10.1017/S0007114510000176.
  • Gomez-Arango LF, Barrett HL, McIntyre HD, Callaway LK, Morrison M, Nitert MD. Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes. 2016;65(8):2214–2223. doi:10.2337/db16-0278.
  • Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102(31):11070–11075. doi:10.1073/pnas.0504978102.
  • Grech A, Collins CE, Holmes A, Lal R, Duncanson K, Taylor R, 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.
  • Mann PE, Huynh K, Widmer G. Maternal high fat diet and its consequence on the gut microbiome: a rat model. Gut Microbes. 2018;9(2):143–154. doi:10.1080/19490976.2017.1395122.
  • Röytiö H, Mokkala K, Vahlberg T, Laitinen K. Dietary intake of fat and fibre according to reference values relates to higher gut microbiota richness in overweight pregnant women. Br J Nutr. 2017;118(5):343–352. doi:10.1017/S0007114517002100.
  • Barrett HL, Gomez-Arango LF, Wilkinson SA, McIntyre HD, Callaway LK, Morrison M, Dekker Nitert M. A vegetarian diet is a major determinant of gut microbiota composition in early pregnancy. Nutrients. 2018;10(7):890. doi:10.3390/nu10070890.
  • Gomez-Arango LF, Barrett HL, Wilkinson SA, Callaway LK, McIntyre HD, Morrison M, Dekker Nitert M. Low dietary fiber intake increases Collinsella abundance in the gut microbiota of overweight and obese pregnant women. Gut Microbes. 2018;9(3):189–201. doi:10.1080/19490976.2017.1406584.
  • García-Mantrana I, Selma-Royo M, González S, Parra-Llorca A, Martínez-Costa C, Collado MC. Distinct maternal microbiota clusters are associated with diet during pregnancy: impact on neonatal microbiota and infant growth during the first 18 months of life. Gut Microbes. 2020;11(4):962–978. doi:10.1080/19490976.2020.1730294.
  • Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol. 2016;7:979. doi:10.3389/fmicb.2016.00979.
  • Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol. 2017;19(1):29–41. doi:10.1111/1462-2920.13589.
  • Mandal S, Godfrey KM, McDonald D, Treuren WV, Bjørnholt JV, Midtvedt T, Moen B, Rudi K, Knight R, Brantsæter AL, et al. Fat and vitamin intakes during pregnancy have stronger relations with a pro-inflammatory maternal microbiota than does carbohydrate intake. Microbiome. 2016;4(1):55. doi:10.1186/s40168-016-0200-3.
  • Kaakoush NO. Sutterella species, IgA-degrading bacteria in ulcerative colitis. Trends Microbiol. 2020;28(7):519–522. doi:10.1016/j.tim.2020.02.018.
  • Williams BL, Hornig M, Parekh T, Lipkin WI, Biron C. Application of novel PCR-based methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances. mBio. 2012;3(1):e00261–11. doi:10.1128/mBio.00261-11.
  • Wang L, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA. Increased abundance of Sutterella spp. and Ruminococcus torques in feces of children with autism spectrum disorder. Mol Autism. 2013;4(1):42. doi:10.1186/2040-2392-4-42.
  • Ami N, Bernstein M, Boucher F, Rieder M, Parker L. Folate and neural tube defects: the role of supplements and food fortification. Paediatr Child Health. 2016;21(3):145–154. doi:10.1093/pch/21.3.145.
  • King JC. A Summary of pathways or mechanisms linking preconception maternal nutrition with birth outcomes. J Nutr. 2016;146(7):1437s–1444s. doi:10.3945/jn.115.223479.
  • Chia AR, Chen LW, Lai JS, Wong CH, Neelakantan N, Van Dam RM, Chong MF. Maternal dietary patterns and birth outcomes: a systematic review and meta-analysis. Adv Nutr. 2019;10(4):685–695. doi:10.1093/advances/nmy123.
  • Chu DM, Antony KM, Ma J, Prince AL, Showalter L, Moller M, Aagaard KM. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med. 2016;8(1):77. doi:10.1186/s13073-016-0330-z.
  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031. doi:10.1038/nature05414.
  • Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci U S A. 2009;106(7):2365–2370. doi:10.1073/pnas.0812600106.
  • Vuillermin PJ, O’Hely M, Collier F, Allen KJ, Tang MLK, Harrison LC, Carlin JB, Saffery R, Ranganathan S, Sly PD, et al. Maternal carriage of Prevotella during pregnancy associates with protection against food allergy in the offspring. Nat Commun. 2020;11(1):1452. doi:10.1038/s41467-020-14552-1.
  • De Tejada BM. Antibiotic use and misuse during pregnancy and delivery: benefits and risks. Int J Env Res Public Health. 2014;11(8):7993–8009. doi:10.3390/ijerph110807993.
  • Stokholm J, Schjørring S, Pedersen L, Bischoff AL, Følsgaard N, Carson CG, Chawes BL, Bønnelykke K, Mølgaard A, Krogfelt KA, et al. Prevalence and predictors of antibiotic administration during pregnancy and birth. PLoS One. 2013;8(12):e82932. doi:10.1371/journal.pone.0082932.
  • Broe A, Pottegård A, Lamont RF, Jørgensen JS, Damkier P. Increasing use of antibiotics in pregnancy during the period 2000–2010: prevalence, timing, category, and demographics. BJOG. 2014;121(8):988–996. doi:10.1111/1471-0528.12806.
  • Petersen I, Gilbert R, Evans S, Ridolfi A, Nazareth I. Oral antibiotic prescribing during pregnancy in primary care: uK population-based study. J Antimicrob Chemother. 2010;65(10):2238–2246. doi:10.1093/jac/dkq307.
  • Palmsten K, Hernández-Díaz S, Chambers CD, Mogun H, Lai S, Gilmer TP, Huybrechts KF. The most commonly dispensed prescription medications among pregnant women enrolled in the United States Medicaid program. Obstet Gynecol. 2015;126(3):465–473. doi:10.1097/AOG.0000000000000982.
  • Nogacka A, Salazar N, Suárez M, Milani C, Arboleya S, Solís G, Fernández N, Alaez L, Hernández-Barranco AM, de Los Reyes-Gavilán CG, et al. Impact of intrapartum antimicrobial prophylaxis upon the intestinal microbiota and the prevalence of antibiotic resistance genes in vaginally delivered full-term neonates. Microbiome. 2017;5(1):93. doi:10.1186/s40168-017-0313-3.
  • Aloisio I, Quagliariello A, De Fanti S, Luiselli D, De Filippo C, Albanese D, Corvaglia LT, Faldella G, Di Gioia D. Evaluation of the effects of intrapartum antibiotic prophylaxis on newborn intestinal microbiota using a sequencing approach targeted to multi hypervariable 16S rDNA regions. Appl Microbiol Biotechnol. 2016;100(12):5537–5546. doi:10.1007/s00253-016-7410-2.
  • Tissier H. Recherches sur la flore intestinale des nourrissons:(état normal et pathologique). Paris: Master’s Thesis of G.Carre and C.Naud; 1900.
  • Goldenberg RL, Hauth JC, Andrews WW, Epstein FH. Intrauterine infection and preterm delivery. N Engl J Med. 2000;342(20):1500–1507. doi:10.1056/NEJM200005183422007.
  • Gonçalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev. 2002;8(1):3–13. doi:10.1002/mrdd.10008.
  • Thomas J, Govender N, McCarthy KM, Erasmus LK, Doyle TJ, Allam M, Ismail A, Ramalwa N, Sekwadi P, Ntshoe G, et al. Outbreak of listeriosis in South Africa associated with processed meat. N Engl J Med. 2020;382(7):632–643. doi:10.1056/NEJMoa1907462.
  • Elinav H, Hershko-Klement A, Valinsky L, Jaffe J, Wiseman A, Shimon H, Braun E, Paitan Y, Block C, Sorek R, et al. Pregnancy-associated listeriosis: clinical characteristics and geospatial analysis of a 10-year period in Israel. Clin Infect Dis. 2014;59(7):953–961. doi:10.1093/cid/ciu504.
  • De Santis M, De Luca C, Mappa I, Spagnuolo T, Licameli A, Straface G, Scambia G. Syphilis Infection during pregnancy: fetal risks and clinical management. Infect Dis Obstet Gynecol. 2012;2012:430585. doi:10.1155/2012/430585.
  • Rac MW, Bryant SN, McIntire DD, Cantey JB, Twickler DM, Wendel GD Jr., Sheffield JS. Progression of ultrasound findings of fetal syphilis after maternal treatment. Am J Obstet Gynecol. 2014;211(4):426.e1–6. doi:10.1016/j.ajog.2014.05.049.
  • Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro‐organism infection and microflora in the mouth. BJOG Inter J Obstet Gynaecol. 2002;109(5):527–533. doi:10.1111/j.1471-0528.2002.01349.x.
  • Rautava S, Collado MC, Salminen S, Isolauri E. Probiotics modulate host-microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology. 2012;102(3):178–184. doi:10.1159/000339182.
  • Jiménez E, Fernández L, Marín ML, Martín R, Odriozola JM, Nueno-Palop C, Narbad A, Olivares M, Xaus J, Rodríguez JM. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol. 2005;51(4):270–274. doi:10.1007/s00284-005-0020-3.
  • Steel JH, Malatos S, Kennea N, Edwards AD, Miles L, Duggan P, Reynolds PR, Feldman RG, Sullivan MH. Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor. Pediatr Res. 2005;57(3):404–411. doi:10.1203/01.PDR.0000153869.96337.90.
  • Calatayud M, Koren O, Collado MC. Maternal microbiome and metabolic health program microbiome development and health of the offspring. Trends Endocrinol Metab. 2019;30(10):735–744. doi:10.1016/j.tem.2019.07.021.
  • Vuong HE, Pronovost GN, Williams DW, Coley EJL, Siegler EL, Qiu A, Kazantsev M, Wilson CJ, Rendon T, Hsiao EY. The maternal microbiome modulates fetal neurodevelopment in mice. Nature. 2020;586(7828):281–286. doi:10.1038/s41586-020-2745-3.
  • Kimura I, Miyamoto J, Ohue-Kitano R, Watanabe K, Yamada T, Onuki M, Aoki R, Isobe Y, Kashihara D, Inoue D, et al. Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice. Science. 2020;367(6481):eaaw8429. doi:10.1126/science.aaw8429.
  • Laforest-Lapointe I, Becker AB, Mandhane PJ, Turvey SE, Moraes TJ, Sears MR, Subbarao P, Sycuro LK, Azad MB, Arrieta M-C. Maternal consumption of artificially sweetened beverages during pregnancy is associated with infant gut microbiota and metabolic modifications and increased infant body mass index. Gut Microbes. 2021;13(1):1–15. doi:10.1080/19490976.2020.1857513.
  • Adams-Chapman I, Heyne RJ, DeMauro SB, Duncan AF, Hintz SR, Pappas A, Vohr BR, McDonald SA, Das A, Newman JE, et al. Neurodevelopmental impairment among extremely preterm infants in the neonatal research network. Pediatrics. 2018;141(5):e20173091. doi:10.1542/peds.2017-3091.
  • Matthews LG, Walsh BH, Knutsen C, Neil JJ, Smyser CD, Rogers CE, Inder TE. Brain growth in the NICU: critical periods of tissue-specific expansion. Pediatr Res. 2018;83(5):976–981. doi:10.1038/pr.2018.4.
  • Liu XN, Li X, Xia B, Jin X, Zou QH, Zeng ZH, Zhao WY, Yan SK, Li L, Yuan S, et al. High-fiber diet mitigates maternal obesity-induced cognitive and social dysfunction in the offspring via gut-brain axis. Cell Metab. 2021;33(5):923–938. e6. doi:10.1016/j.cmet.2021.02.002.
  • Kalish BT, Kim E, Finander B, Duffy EE, Kim H, Gilman CK, Yim YS, Tong L, Kaufman RJ, Griffith EC, et al. Maternal immune activation in mice disrupts proteostasis in the fetal brain. Nat Neurosci. 2021;24(2):204–213. doi:10.1038/s41593-020-00762-9.
  • Choi GB, Yim YS, Wong H, Kim S, Kim H, Kim SV, Hoeffer CA, Littman DR, Huh JR. The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science. 2016;351(6276):933–939. doi:10.1126/science.aad0314.
  • Qu WH, Liu LS, Miao LY. Exposure to antibiotics during pregnancy alters offspring outcomes. Expert Opin Drug Metab Toxicol. 2021;17(10):1165–1174. doi:10.1080/17425255.2021.1974000.
  • Hapfelmeier S, Lawson MA, Slack E, Kirundi JK, Stoel M, Heikenwalder M, Cahenzli J, Velykoredko Y, Balmer ML, Endt K, et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science. 2010;328(5986):1705–1709. doi:10.1126/science.1188454.
  • Gomez de Agüero M, 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.
  • Arpaia N, Campbell C, Fan X, Dikiy S, Van Der Veeken J, Deroos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–455. doi:10.1038/nature12726.
  • Hu M, Eviston D, Hsu P, Mariño E, Chidgey A, Santner-Nanan B, Wong K, Richards JL, Yap YA, Collier F, et al. Decreased maternal serum acetate and impaired fetal thymic and regulatory T cell development in preeclampsia. Nat Commun. 2019;10(1):3031. doi:10.1038/s41467-019-10703-1.
  • Gray LEK, O’Hely M, Ranganathan S, Sly PD, Vuillermin P. The maternal diet, gut bacteria, and bacterial metabolites during pregnancy influence offspring asthma. Front Immunol. 2017;8:365. doi:10.3389/fimmu.2017.00365.
  • Lim AI, McFadden T, Link VM, Han S-J, Karlsson R-M, Stacy A, Farley TK, Lima-Junior DS, Harrison OJ, Desai JV, et al. Prenatal maternal infection promotes tissue-specific immunity and inflammation in offspring. Science. 2021;373(6558):eabf3002. doi:10.1126/science.abf3002.
  • Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, McCoy KD, Macpherson AJ. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity. 2011;34(5):794–806. doi:10.1016/j.immuni.2011.03.021.
  • Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol. 2007;19(2):59–69. doi:10.1016/j.smim.2006.10.002.
  • Nyangahu DD, Lennard KS, Brown BP, Darby MG, Wendoh JM, Havyarimana E, Smith P, Butcher J, Stintzi A, Mulder N et al. Disruption of maternal gut microbiota during gestation alters offspring microbiota and immunity. Microbiome. 2018;6(1):124. doi:10.1186/s40168-018-0511-7.
  • Hu YJ, Peng J, Tai NW, Hu CY, Zhang XJ, Wong FS, Wen L. Maternal antibiotic treatment protects offspring from diabetes development in nonobese diabeticmice by generation of tolerogenic APCs. J Immunol. 2015;195(9):4176-4184. doi:10.4049/jimmunol.1500884.
  • Gonzalez-Perez G, Hicks AL, Tekieli TM, Radens CM, Williams BL, Lamousé-Smith ES. Maternal antibiotic treatment impacts development of the neonatal intestinal microbiome and antiviral immunity. J Immunol. 2016;196(9):3768–3779. doi:10.4049/jimmunol.1502322.
  • Gonzalez-Perez G, Lamousé-Smith ES. Gastrointestinal microbiome dysbiosis in infant mice alters peripheral CD8+ T cell receptor signaling. Front Immunol. 2017;8:265. doi:10.3389/fimmu.2017.00265.
  • Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, Armanini F, Truong DT, Manara S, Zolfo M, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host & Microbe. 2018;24(1):133–145. e5. doi:10.1016/j.chom.2018.06.005.
  • Hamilton MK, Ronveaux CC, Rust BM, Newman JW, Hawley M, Barile D, Mills DA, Raybould HE. Prebiotic milk oligosaccharides prevent development of obese phenotype, impairment of gut permeability, and microbial dysbiosis in high fat-fed mice. Am J Physiol Gastrointest Liver Physiol. 2017;312(5):G474–487. doi:10.1152/ajpgi.00427.2016.
  • Gregory KE, Samuel BS, Houghteling P, Shan G, Ausubel FM, Sadreyev RI, Walker WA. Influence of maternal breast milk ingestion on acquisition of the intestinal microbiome in preterm infants. Microbiome. 2016;4(1):68. doi:10.1186/s40168-016-0214-x.
  • Dong TS, Gupta A. Influence of early life, diet, and the environment on the microbiome. Clin Gastroenterol Hepatol. 2019;17(2):231–242. doi:10.1016/j.cgh.2018.08.067.
  • Liu HB, Hou CL, Li N, Zhang XY, Zhang GL, Yang FY, Zeng XF, Liu ZH, Qiao SY. Microbial and metabolic alterations in gut microbiota of sows during pregnancy and lactation. FASEB J. 2019;33(3):4490–4501. doi:10.1096/fj.201801221RR.
  • Jost T, Lacroix C, Braegger CP, Rochat F, Chassard C. Vertical mother–neonate transfer of maternal gut bacteria via breastfeeding. Environ Microbiol. 2014;16(9):2891–2904. doi:10.1111/1462-2920.12238.
  • DiGiulio DB, Callahan BJ, McMurdie PJ, Costello EK, Lyell DJ, Robaczewska A, Sun CL, Goltsman DS, Wong RJ, Shaw G, et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc Natl Acad Sci U S A. 2015;112(35):11060–11065. doi:10.1073/pnas.1502875112.
  • Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Nikita L, Galuppi M, Lamont RF, Chaemsaithong P, Miranda J, et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1):1–19. doi:10.1186/2049-2618-2-10.
  • Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4680–4687. doi:10.1073/pnas.1002611107.
  • Dominguez-Bello MG, Costello EK, 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 U S A. 2010;107(26):11971–11975. doi:10.1073/pnas.1002601107.
  • Walther-António MR, Jeraldo P, Berg Miller ME, Yeoman CJ, Nelson KE, Wilson BA, White BA, Chia N, Creedon DJ, Gilbert JA. Pregnancy’s Stronghold on the Vaginal Microbiome. PLoS One. 2014;9(6):e98514. doi:10.1371/journal.pone.0098514.
  • Kindinger LM, Bennett PR, Lee YS, Marchesi JR, Smith A, Cacciatore S, Holmes E, Nicholson JK, Teoh TG, MacIntyre DA. The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome. 2017;5(1):6. doi:10.1186/s40168-016-0223-9.
  • Fettweis JM, Serrano MG, Brooks JP, Edwards DJ, Girerd PH, Parikh HI, Huang B, Arodz TJ, Edupuganti L, Glascock AL, et al. The vaginal microbiome and preterm birth. Nat Med. 2019;25(6):1012–1021. doi:10.1038/s41591-019-0450-2.
  • Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host & Microbe. 2015;17(5):690–703. doi:10.1016/j.chom.2015.04.004.
  • 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.
  • Wampach L, Heintz-Buschart A, Fritz JV, Ramiro-Garcia J, Habier J, Herold M, Narayanasamy S, Kaysen A, Hogan AH, Bindl L, et al. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nat Commun. 2018;9(1):5091. doi:10.1038/s41467-018-07631-x.
  • Chu DM, Ma J, Prince AL, Antony KM, Seferovic MD, Aagaard KM. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat Med. 2017;23(3):314–326. doi:10.1038/nm.4272.
  • Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, Subbarao P, Sears MR, et al. Roles of birth mode and infant gut microbiota in intergenerational transmission of overweight and obesity from mother to offspring. JAMA Pediatr. 2018;172(4):368–377. doi:10.1001/jamapediatrics.2017.5535.
  • Korpela K, Helve O, Kolho K-L, Saisto T, Skogberg K, Dikareva E, Stefanovic V, Salonen A, Andersson S, de Vos WM. Maternal fecal microbiota transplantation in cesarean-born infants rapidly restores normal gut microbial development: a proof-of-concept study. Cell. 2020;183(2):324–334.e5. doi:10.1016/j.cell.2020.08.047.
  • Stencel‐gabriel K, Gabriel I, Wiczkowski A, Paul M, Olejek A. Prenatal priming of cord blood T lymphocytes by microbiota in the maternal vagina. Am J Reprod Immunol. 2009;61(3):246–252. doi:10.1111/j.1600-0897.2009.00687.x.
  • Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, Bokulich NA, Song SJ, Hoashi M, Rivera-Vinas JI, et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat Med. 2016;22(3):250–253. doi:10.1038/nm.4039.
  • Wilson BC, Butler ÉM, Grigg CP, Derraik JGB, Chiavaroli V, Walker N, Thampi S, Creagh C, Reynolds AJ, Vatanen T, et al. Oral administration of maternal vaginal microbes at birth to restore gut microbiome development in infants born by caesarean section: a pilot randomised placebo-controlled trial. EBioMedicine. 2021;69:103443. doi:10.1016/j.ebiom.2021.103443.
  • Parigi SM, Eldh M, Larssen P, Gabrielsson S, Villablanca EJ. Breast milk and solid food shaping intestinal immunity. Front Immunol. 2015;6:415. doi:10.3389/fimmu.2015.00415.
  • Kordy K, Gaufin T, Mwangi M, Li F, Cerini C, Lee DJ, Adisetiyo H, Woodward C, Pannaraj PS, Tobin NH, et al. Contributions to human breast milk microbiome and enteromammary transfer of Bifidobacterium breve. PLoS One. 2020;15(1):e0219633. doi:10.1371/journal.pone.0219633.
  • Williams JE, Carrothers JM, Lackey KA, Beatty NF, Brooker SL, Peterson HK, Steinkamp KM, York MA, Shafii B, Price WJ, et al. Strong multivariate relations exist among milk, oral, and fecal microbiomes in mother-infant dyads during the first six months postpartum. J Nutr. 2019;149(6):902–914. doi:10.1093/jn/nxy299.
  • Moossavi S, Sepehri S, Robertson B, Bode L, Goruk S, Field CJ, Lix LM, de Souza RJ, Becker AB, Mandhane PJ, et al. Composition and variation of the human milk microbiota are influenced by maternal and early-life factors. Cell Host & Microbe. 2019;25(2):324–335.e4. doi:10.1016/j.chom.2019.01.011.
  • Rodríguez JM. The origin of human milk bacteria: is there a bacterial entero-mammary pathway during late pregnancy and lactation? Adv Nutr. 2014;5(6):779–784. doi:10.3945/an.114.007229.
  • Biagi E, Quercia S, Aceti A, Beghetti I, Rampelli S, Turroni S, Faldella G, Candela M, Brigidi P, Corvaglia L. The bacterial ecosystem of mother’s milk and infant’s mouth and gut. Front Microbiol. 2017;8:1214. doi:10.3389/fmicb.2017.01214.
  • Ramsay DT, Kent JC, Owens RA, Hartmann PE. Ultrasound imaging of milk ejection in the breast of lactating women. Pediatrics. 2004;113(2):361–367. doi:10.1542/peds.113.2.361.
  • Perez PF, Doré J, Leclerc M, Levenez F, Benyacoub J, Serrant P, Segura-Roggero I, Schiffrin EJ, Donnet-Hughes A. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics. 2007;119(3):e724–732. doi:10.1542/peds.2006-1649.
  • McGuire MK, McGuire MA. Got bacteria? The astounding, yet not-so-surprising, microbiome of human milk. Curr Opin Biotechnol. 2017;44:63–68. doi:10.1016/j.copbio.2016.11.013.
  • Damaceno QS, Souza JP, Nicoli JR, Paula RL, Assis GB, Figueiredo HC, Azevedo V, Martins FS. Evaluation of potential probiotics isolated from human milk and colostrum. Probiotics Antimicrob Proteins. 2017;9(4):371–379. doi:10.1007/s12602-017-9270-1.
  • Sakwinska O, Bosco N. Host microbe interactions in the lactating mammary gland. Front Microbiol. 2019;10:1863. doi:10.3389/fmicb.2019.01863.
  • Kumar H, du Toit E, Kulkarni A, Aakko J, Linderborg KM, Zhang Y, Nicol MP, Isolauri E, Yang B, Collado MC, et al. Distinct patterns in human milk microbiota and fatty acid profiles across specific geographic locations. Front Microbiol. 2016;7:1619. doi:10.3389/fmicb.2016.01619.
  • Gomez-Gallego C, Garcia-Mantrana I, Salminen S, Collado MC. The human milk microbiome and factors influencing its composition and activity. Semin Fetal Neonatal Med. 2016;21(6):400–405. doi:10.1016/j.siny.2016.05.003.
  • Ding M, Qi C, Yang Z, Jiang S, Bi Y, Lai J, Sun J. Geographical location specific composition of cultured microbiota and Lactobacillus occurrence in human breast milk in China. Food Funct. 2019;10(2):554–564. doi:10.1039/c8fo02182a.
  • 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.
  • Collado MC, Laitinen K, Salminen S, Isolauri E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatric Res. 2012;72(1):77–85. doi:10.1038/pr.2012.42.
  • Indiani CMDSP, Rizzardi KF, Castelo PM, Ferraz LFC, Darrieux M, Parisotto TM. Childhood obesity and Firmicutes/Bacteroidetes ratio in the gut microbiota: a systematic review. Child Obes. 2018;14(8):501–509. doi:10.1089/chi.2018.0040.
  • Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19(1):55–71. doi:10.1038/s41579-020-0433-9.
  • Arboleya S, Binetti A, Salazar N, Fernández N, Solís G, Hernández-Barranco A, Margolles A, de Los Reyes-Gavilán CG, Gueimonde M. Establishment and development of intestinal microbiota in preterm neonates. FEMS Microbiol Ecol. 2012;79(3):763–772. doi:10.1111/j.1574-6941.2011.01261.x.
  • Arboleya S, Sánchez B, Milani C, Duranti S, Solís G, Fernández N, de Los Reyes-Gavilán CG, Ventura M, Margolles A, Gueimonde M. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J Pediatr. 2015;166(3):538–544. doi:10.1016/j.jpeds.2014.09.041.
  • Mai V, Torrazza RM, Ukhanova M, Wang X, Sun Y, Li N, Shuster J, Sharma R, Hudak ML, Neu J, et al. Distortions in development of intestinal microbiota associated with late onset sepsis in preterm infants. PLoS One. 2013;8(1):e52876. doi:10.1371/journal.pone.0052876.
  • Arrieta MC, 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. doi:10.1126/scitranslmed.aab2271.
  • McCloskey K, Vuillermin P, Carlin JB, Cheung M, Skilton MR, Tang ML, Allen K, Gilbert GL, Ranganathan S, Collier F, et al. Perinatal microbial exposure may influence aortic intima-media thickness in early infancy. Int J Epidemiol. 2017;46(1):209–218. doi:10.1093/ije/dyw042.
  • Mu Q, Swartwout BK, Edwards M, Zhu J, Lee G, Eden K, Cabana-Puig X, McDaniel DK, Mao J, Abdelhamid L, et al. Regulation of neonatal IgA production by the maternal microbiota. Proc Natl Acad Sci U S A. 2021;118(9). doi:10.1073/pnas.2015691118.
  • Laursen MF, Sakanaka M, von Burg N, Mörbe U, Andersen D, Moll JM, Pekmez CT, Rivollier A, Michaelsen KF, Mølgaard C, et al. Bifidobacterium species associated with breastfeeding produce aromatic lactic acids in the infant gut. Nat Microbiol. 2021;6(11):1367–1382. doi:10.1038/s41564-021-00970-4.
  • Sela DA, Mills DA. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 2010;18(7):298–307. doi:10.1016/j.tim.2010.03.008.
  • Henrick BM, Rodriguez L, Lakshmikanth T, Pou C, Henckel E, Arzoomand A, Olin A, Wang J, Mikes J, Tan Z, et al. Bifidobacteria-mediated immune system imprinting early in life. Cell. 2021;184(15):3884–3898.e11. doi:10.1016/j.cell.2021.05.030.
  • Bode L. The functional biology of human milk oligosaccharides. Early Hum Dev. 2015;91(11):619–622. doi:10.1016/j.earlhumdev.2015.09.001.
  • Boumahrou N, Chevaleyre C, Berri M, Martin P, Bellier S, Salmon H. An increase in milk IgA correlates with both pIgr expression and IgA plasma cell accumulation in the lactating mammary gland of PRM/Alf mice. J Reprod Immunol. 2012;96(1–2):25–33. doi:10.1016/j.jri.2012.08.001.
  • Johansen F-E, Braathen R, Brandtzaeg P. The J chain is essential for polymeric Ig receptor-mediated epithelial transport of IgA. J Immunol. 2001;167(9):5185–5192. doi:10.4049/jimmunol.167.9.5185.
  • Wilson E, Butcher EC. CCL28 controls immunoglobulin (Ig) a plasma cell accumulation in the lactating mammary gland and IgA antibody transfer to the neonate. J Exp Med. 2004;200(6):805–809. doi:10.1084/jem.20041069.
  • Usami K, Niimi K, Matsuo A, Suyama Y, Sakai Y, Sato S, Fujihashi K, Kiyono H, Uchino S, Furukawa M, et al. The gut microbiota induces Peyer’s-patch-dependent secretion of maternal IgA into milk. Cell Rep. 2021;36(10):109655. doi:10.1016/j.celrep.2021.109655.
  • Ding MF, Yang B, Ross RP, Stanton C, Zhao JX, Zhang HX, Chen W. Crosstalk between sIgA-Coated bacteria in infant gut and early-life health. Trends Microbiol. 2021;29(8):725–735. doi:10.1016/j.tim.2021.01.012.
  • Dunne-Castagna VP, Taft DH. Mother’s Touch: milk IgA and Protection from Necrotizing Enterocolitis. Cell Host & Microbe. 2019;26(2):147–148. doi:10.1016/j.chom.2019.07.013.
  • Donaldson GP, Ladinsky MS, Yu KB, Sanders JG, Yoo B, Chou W-C, Conner M, Earl A, Knight R, Bjorkman P, et al. Gut microbiota utilize immunoglobulin a for mucosal colonization. Science. 2018;360(6390):795–800. doi:10.1126/science.aaq0926.
  • Peterson DA, McNulty NP, Guruge JL, Gordon JI. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host & Microbe. 2007;2(5):328–339. doi:10.1016/j.chom.2007.09.013.
  • Zimmermann J, Macpherson AJ. Breast Milk Modulates Transgenerational Immune Inheritance. Cell. 2020;181(6):1202–1204. doi:10.1016/j.cell.2020.05.030.
  • Wu W, Liu HP, Chen F, Liu H, Cao AT, Yao S, Sun M, Evans‐marin HL, Zhao Y, Zhao Q, et al. Commensal A4 bacteria inhibit intestinal Th2‐cell responses through induction of dendritic cell TGF‐β production. Eur J Immunol. 2016;46(5):1162–1167. doi:10.1002/eji.201546160.
  • Liu X, Zeng B, Zhang J, Li W, Mou F, Wang H, Zou Q, Zhong B, Wu L, Wei H, et al. Role of the gut microbiome in modulating arthritis progression in mice. Sci Rep. 2016;6(1):30594. doi:10.1038/srep30594.
  • D’Auria G, Peris-Bondia F, Džunková M, Mira A, Collado MC, Latorre A, Moya A. Active and secreted IgA-coated bacterial fractions from the human gut reveal an under-represented microbiota core. Sci Rep. 2013;3(1):3515. doi:10.1038/srep03515.
  • Planer JD, Peng Y, Kau AL, Blanton LV, Ndao IM, Tarr PI, Warner BB, Gordon JI. Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice. Nature. 2016;534(7606):263–266. doi:10.1038/nature17940.
  • Palm NW, De Zoete MR, Cullen TW, Barry NA, Stefanowski J, Hao L, Degnan PH, Hu J, Peter I, Zhang W, et al. Immunoglobulin a coating identifies colitogenic bacteria in inflammatory bowel disease. Cell. 2014;158(5):1000–1010. doi:10.1016/j.cell.2014.08.006.
  • Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, et al. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209–222. doi:10.1016/S0140-6736(13)60844-2.
  • Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. Citrobacter rodentium of mice and man. Cell Microbiol. 2005;7(12):1697–1706. doi:10.1111/j.1462-5822.2005.00625.x.
  • Caballero-Flores G, Sakamoto K, Zeng MY, Wang Y, Hakim J, Matus-Acuña V, Inohara N, Núñez G. Maternal immunization confers protection to the offspring against an attaching and effacing pathogen through delivery of IgG in breast milk. Cell Host & Microbe. 2019;25(2):313–323.e4. doi:10.1016/j.chom.2018.12.015.
  • Umetsu DT, DeKruyff RH. The regulation of allergy and asthma. Immunol Rev. 2006;212(1):238–255. doi:10.1111/j.0105-2896.2006.00413.x.
  • Weidinger S, Novak N. Atopic dermatitis. Lancet. 2016;387(10023):1109–1122. doi:10.1016/s0140-6736(15)00149-x.
  • Ta LDH, Chan JCY, Yap GC, Purbojati RW, Drautz-Moses DI, Koh YM, Tay CJX, Huang CH, Kioh DYQ, Woon JY, et al. A compromised developmental trajectory of the infant gut microbiome and metabolome in atopic eczema. Gut Microbes. 2020;12(1):1–22. doi:10.1080/19490976.2020.1801964.
  • Fiocchi A, Pawankar R, Cuello-Garcia C, Ahn K, Al-Hammadi S, Agarwal A, Beyer K, Burks W, Canonica GW, Ebisawa M, et al. World Allergy Organization-McMaster University Guidelines for Allergic Disease Prevention (GLAD-P): probiotics. World Allergy Organ J. 2015;8(1):4. doi:10.1186/s40413-015-0055-2.
  • López-Serrano P, Pérez-Calle JL, Pérez-Fernández MT, Fernández-Font JM, Boixeda de Miguel D, Fernández-Rodríguez CM. Environmental risk factors in inflammatory bowel diseases. Investigating the hygiene hypothesis: a Spanish case-control study. Scand J Gastroenterol. 2010;45(12):1464–1471. doi:10.3109/00365521.2010.510575.
  • Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrländer C, Heederik D, Piarroux R, von Mutius E. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364(8):701–709. doi:10.1056/NEJMoa1007302.
  • Hebert JC, Radford-Smith DE, Probert F, Ilott N, Chan KW, Anthony DC, Burnet PW. Mom’s diet matters: maternal prebiotic intake in mice reduces anxiety and alters brain gene expression and the fecal microbiome in offspring. Brain Behav Immun. 2021;91:230–244. doi:10.1016/j.bbi.2020.09.034.
  • Lee YM, Mu A, Wallace M, Gengatharan JM, Furst AJ, Bode L, Metallo CM, Ayres JS. Microbiota control of maternal behavior regulates early postnatal growth of offspring. Sci Adv. 2021;7(5):eabe6563. doi:10.1126/sciadv.abe6563.
  • Jiménez E, Marín ML, Martín R, Odriozola JM, Olivares M, Xaus J, Fernández L, Rodríguez JM. Is meconium from healthy newborns actually sterile? Res Microbiol. 2008;159(3):187–193. doi:10.1016/j.resmic.2007.12.007.
  • Blaser MJ, Devkota S, McCoy KD, Relman DA, Yassour M, Young VB. Lessons learned from the prenatal microbiome controversy. Microbiome. 2021;9(1):8. doi:10.1186/s40168-020-00946-2.
  • Kennedy KM, Gerlach MJ, Adam T, Heimesaat MM, Rossi L, Surette MG, Sloboda DM, Braun T. Fetal meconium does not have a detectable microbiota before birth. Nat Microbiol. 2021;6(7):865–873. doi:10.1038/s41564-021-00904-0.
  • Mishra A, Lai GC, Yao LJ, Aung TT, Shental N, Rotter-Maskowitz A, Shepherdson E, Singh GSN, Pai R, Shanti A, et al. Microbial exposure during early human development primes fetal immune cells. Cell. 2021;184(13):3394–3409.e20. doi:10.1016/j.cell.2021.04.039.
  • Lebovitz Y, Kowalski EA, Wang X, Kelly C, Lee M, McDonald V, Ward R, Creasey M, Mills W, Basso EKG, et al. Lactobacillus rescues postnatal neurobehavioral and microglial dysfunction in a model of maternal microbiome dysbiosis. Brain Behav Immun. 2019;81:617–629. doi:10.1016/j.bbi.2019.07.025.
  • Wang X, Yang J, Zhang H, Yu J, Yao Z. Oral probiotic administration during pregnancy prevents autism‐related behaviors in offspring induced by maternal immune activation via anti‐inflammation in mice. Autism Res. 2019;12(4):576–588. doi:10.1002/aur.2079.
  • Cowan CS, Stylianakis AA, Richardson R. Early-life stress, microbiota, and brain development: probiotics reverse the effects of maternal separation on neural circuits underpinning fear expression and extinction in infant rats. Dev Cog Neurosci. 2019;37:100627. doi:10.1016/j.dcn.2019.100627.
  • Krishna G, Divyashri G, Prapulla S. A combination supplement of fructo-and xylo-oligosaccharides significantly abrogates oxidative impairments and neurotoxicity in maternal/fetal milieu following gestational exposure to acrylamide in rat. Neurochem Res. 2015;40(9):1904–1918. doi:10.1007/s11064-015-1687-x.
  • Cho NA, Nicolucci AC, Klancic T, Wang W, Sharkey KA, Mychasiuk R, Reimer RA. Impaired hypothalamic microglial activation in offspring of antibiotic-treated pregnant/lactating rats is attenuated by prebiotic oligofructose co-administration. Microorganisms. 2020;8(7):1085. doi:10.3390/microorganisms8071085.
  • de Oliveira Y, Cavalcante RGS, Neto MPC, Magnani M, de Andrade Braga V, de Souza EL, de Brito Alves JL. Oral administration of Lactobacillus fermentum post-weaning improves the lipid profile and autonomic dysfunction in rat offspring exposed to maternal dyslipidemia. Food Funct. 2020;11(6):5581–5594. doi:10.1039/d0fo00514b.
  • Krishna G, Muralidhara. Oral supplements of inulin during gestation offsets rotenone-induced oxidative impairments and neurotoxicity in maternal and prenatal rat brain. Biomed Pharmacother. 2018;104:751–762. doi:10.1016/j.biopha.2018.05.107.
  • Krishna G, Muralidhara. Inulin supplementation during gestation mitigates acrylamide-induced maternal and fetal brain oxidative dysfunctions and neurotoxicity in rats. Neurotoxicol Teratol. 2015;49:49–58. doi:10.1016/j.ntt.2015.03.003.
  • Selle A, Brosseau C, Dijk W, Duval A, Bouchaud G, Rousseaux A, Bruneau A, Cherbuy C, Mariadassou M, Cariou V, et al. Prebiotic supplementation during gestation induces a tolerogenic environment and a protective microbiota in offspring mitigating food allergy. Front Immunol. 2021;12:745535. doi:10.3389/fimmu.2021.745535.
  • Brosseau C, Selle A, Duval A, Misme-Aucouturier B, Chesneau M, Brouard S, Cherbuy C, Cariou V, Bouchaud G, Mincham K, et al. Prebiotic supplementation during pregnancy modifies the gut microbiota and increases metabolites in amniotic fluid, driving a tolerogenic environment in utero. Front Immunol. 2021;12:712614. doi:10.3389/fimmu.2021.712614.
  • Terada-Ikeda C, Kitabatake M, Hiraku A, Kato K, Yasui S, Imakita N, Ouji-Sageshima N, Iwabuchi N, Hamada K, Ito T, et al. Maternal supplementation with Bifidobacterium breve M-16V prevents their offspring from allergic airway inflammation accelerated by the prenatal exposure to an air pollutant aerosol. PLoS One. 2020;15(9):e0238923. doi:10.1371/journal.pone.0238923.
  • Nakajima A, Kaga N, Nakanishi Y, Ohno H, Miyamoto J, Kimura I, Hori S, Sasaki T, Hiramatsu K, Okumura K, et al. Maternal high fiber diet during pregnancy and lactation influences regulatory T cell differentiation in offspring in mice. J Immunol. 2017;199(10):3516–3524. doi:10.4049/jimmunol.1700248.
  • Azagra-Boronat I, Tres A, Massot-Cladera M, À F, Castell M, Guardiola F, Pérez-Cano FJ, Rodríguez-Lagunas MJ. Lactobacillus fermentum CECT5716 supplementation in rats during pregnancy and lactation impacts maternal and offspring lipid profile, immune system and microbiota. Cells. 2020;9(3):575. doi:10.3390/cells9030575.
  • Needell JC, Ir D, Robertson CE, Kroehl ME, Frank DN, Zipris D, Mounier C. Maternal treatment with short-chain fatty acids modulates the intestinal microbiota and immunity and ameliorates type 1 diabetes in the offspring. PLoS One. 2017;12(9):e0183786. doi:10.1371/journal.pone.0183786.
  • Hogenkamp A, Thijssen S, van Vlies N, Garssen J. Supplementing pregnant mice with a specific mixture of nondigestible oligosaccharides reduces symptoms of allergic asthma in male offspring. J Nutr. 2015;145(3):640–646. doi:10.3945/jn.114.197707.
  • Barouei J, Moussavi M, Hodgson DM, Heimesaat MM. Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS One. 2012;7(10):e46051. doi:10.1371/journal.pone.0046051.
  • Ho T, Jahan M, Haque Z, Kracht S, Wynn PC, Du Y, Gunn A, Wang B. Maternal chitosan oligosaccharide intervention optimizes the production performance and health status of gilts and their offspring. Anim Nutr. 2020;6(2):134–142. doi:10.1016/j.aninu.2020.02.001.
  • Duan XD, Tian G, Chen DW, Huang LH, Zhang D, Zheng P, Mao XB, Yu J, He J, Huang ZQ, et al. Mannan oligosaccharide supplementation in diets of sow and (or) their offspring improved immunity and regulated intestinal bacteria in piglet. J Anim Sci. 2019;97(11):4548–4556. doi:10.1093/jas/skz318.
  • Li Y, Liu HY, Zhang LJ, Yang Y, Lin Y, Zhuo Y, Fang ZF, Che LQ, Feng B, Xu SY, et al. Maternal dietary fiber composition during gestation induces changes in offspring antioxidative capacity, inflammatory response, and gut microbiota in a sow model. Int J Mol Sci. 2019;21(1):31. doi:10.3390/ijms21010031.
  • Shang QH, Liu HS, Liu SJ, He TF, Piao XS. Effects of dietary fiber sources during late gestation and lactation on sow performance, milk quality, and intestinal health in piglets. J Anim Sci. 2019;97(12):4922–4933. doi:10.1093/jas/skz278.
  • Cheng CS, Wei HS, Xu CJ, Xie XW, Jiang SW, Peng J, Björkroth J. Maternal soluble fiber diet during pregnancy changes the intestinal microbiota, improves growth performance, and reduces intestinal permeability in piglets. Appl Environ Microbiol. 2018;84(17):e01047–18. doi:10.1128/AEM.01047-18.
  • Duan XD, Chen DW, Zheng P, Tian G, Wang JP, Mao XB, Yu J, He JF, Li B, Huang ZQ, et al. Effects of dietary mannan oligosaccharide supplementation on performance and immune response of sows and their offspring. Anim Feed Sci Technol. 2016;218:17–25. doi:10.1016/j.anifeedsci.2016.05.002.
  • Le Bourgot C, Ferret-Bernard S, Le Normand L, Savary G, Menendez-Aparicio E, Blat S, Appert-Bossard E, Respondek F, Le Huërou-Luron I, Blachier F. Maternal short-chain fructooligosaccharide supplementation influences intestinal immune system maturation in piglets. PLoS One. 2014;9(9):e107508. doi:10.1371/journal.pone.0107508.
  • Leonard S, Sweeney T, Bahar B, O’Doherty J. Effect of maternal seaweed extract supplementation on suckling piglet growth, humoral immunity, selected microflora, and immune response after an ex vivo lipopolysaccharide challenge. J Anim Sci. 2012;90(2):505–514. doi:10.2527/jas.2010-3243.