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Research Paper

Maternal consumption of a fermented diet protects offspring against intestinal inflammation by regulating the gut microbiota

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Article: 2057779 | Received 29 Oct 2021, Accepted 17 Mar 2022, Published online: 04 May 2022

References

  • Lu Q, Lin Y, Chen T, Lv H, Diao FY, Liu C, Peng M, Ling X, Li H, Wang Y, et al. Alterations of gut microbiota composition in neonates conceived by assisted reproductive technology and its relation to infant growth. Gut Microbes. 2020;12(1):1794466. doi:10.1080/19490976.2020.1794466.
  • Dai X, Guo ZX, Chen DF, Li L, Song XL, Liu TY, Jin G, Li Y, Liu Y, Ajiguli A, et al. Maternal sucralose intake alters gut microbiota of offspring and exacerbates hepatic steatosis in adulthood. Gut Microbes. 2020;11(4):1043–23. doi:10.1080/19490976.2020.1738187.
  • Stiemsma LT, Michels KB. The role of the microbiome in the developmental origins of health and disease. Pediatrics. 2018;141(4):e20172437. doi:10.1542/peds.2017-2437.
  • Stinson LF. Establishment of the early-life microbiome: a DOHaD perspective. J Dev Orig Health Dis. 2020;11(3):201–210. doi:10.1017/S2040174419000588.
  • Laforest-Lapointe I, Becker AB, Mandhane PJ, Turvey SE, Moraes TJ, Sears MR, Subbarao P, Sycuro LK, Azad MB, Arrieta M-C, et al. 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.
  • Fehr K, Moossavi S, Sbihi H, Boutin RCT, Bode L, Robertson B, Yonemitsu C, Field CJ, Becker AB, Mandhane PJ, et al. Breastmilk feeding practices are associated with the co-occurrence of bacteria in mothers’ milk and the infant gut: the child cohort study. Cell Host Microbe. 2020;28(2):285–97e4. doi:10.1016/j.chom.2020.06.009.
  • Sindi AS, Geddes DT, Wlodek ME, Muhlhausler BS, Payne MS, Stinson LF. Can we modulate the breastfed infant gut microbiota through maternal diet? FEMS Microbiol Rev. 2021;45(5). doi:10.1093/femsre/fuab011.
  • Rodriguez 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.
  • 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.
  • 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. 28;. doi:10.1126/science.aaw8429.
  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi:10.1038/nature12820.
  • Tamang JP, Cotter PD, Endo A, Han NS, Kort R, Liu SQ, Mayo B, Westerik N, Hutkins R. Fermented foods in a global age: east meets West. Compr Rev Food Sci Food Saf. 2020;19(1):184–217. doi:10.1111/1541-4337.12520.
  • Díaz-López A, Bulló M, Martínez-González MA, Corella D, Estruch R, Fitó M, Gómez-Gracia E, Fiol M, García de la Corte FJ, Ros E, et al. Dairy product consumption and risk of type 2 diabetes in an elderly Spanish Mediterranean population at high cardiovascular risk. Eur J Nutr. 2016;55(1):349–360. doi:10.1007/s00394-015-0855-8.
  • Gille D, Schmid A, Walther B, Vergères G. Fermented food and non-communicable chronic diseases: a review. Nutrients. 2018;10(4):448. doi:10.3390/nu10040448.
  • Takada T, Chinda D, Mikami T, Shimizu K, Oana K, Hayamizu S, Miyazawa K, Arai T, Katto M, Nagara Y, et al. Dynamic analysis of human small intestinal microbiota after an ingestion of fermented milk by small-intestinal fluid perfusion using an endoscopic retrograde bowel insertion technique. Gut Microbes. 2020;11(6):1662–1676. doi:10.1080/19490976.2020.1766942.
  • Staudacher HM, Loughman A. Gut health: definitions and determinants. Lancet Gastroenterol Hepatol. 2021;6(4):269. doi:10.1016/S2468-1253(21)00071-6.
  • Feldsine P, Abeyta C, Andrews WH, Committee AIM. AOAC International methods committee guidelines for validation of qualitative and quantitative food microbiological official methods of analysis. J AOAC Int. 2021;85(5):1187–1200. doi:10.1093/jaoac/85.5.1187.
  • NRC. Nutrient requirements of Swine 11th revis. Washington (DC): National Academic Press; 2012.
  • Geng SJ, Cheng SS, Li Y, Wen ZS, Ma X, Jiang XM, Wang YZ, Han XY. Faecal microbiota transplantation reduces susceptibility to epithelial injury and modulates tryptophan metabolism of the microbial community in a piglet model. J Crohns Colitis. 2018;12(11):1359–1374. doi:10.1093/ecco-jcc/jjy103.
  • Martino C, Morton JT, Marotz CA, Thompson LR, Tripathi A, Knight R, Zengler K. A novel sparse compositional technique reveals microbial perturbations. mSystems. 2019;4(1):e00016–19. doi:10.1128/mSystems.00016-19.
  • Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2 ‘ s q2-feature-classifier plugin. Microbiome. 2018;6(1):90. doi:10.1186/s40168-018-0470-z.
  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–5072. doi:10.1128/AEM.03006-05.
  • Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb. 2007;73(16):5261–5267. doi:10.1128/AEM.00062-07.
  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. doi:10.1186/gb-2011-12-6-r60.
  • Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol. 2020;38(6):685–688. doi:10.1038/s41587-020-0548-6.
  • Gao PF, Ma C, Sun Z, Wang LF, Huang S, Su XQ, Xu J, Zhang H. Feed-additive probiotics accelerate yet antibiotics delay intestinal microbiota maturation in broiler chicken. Microbiome. 2017;5(1):91. doi:10.1186/s40168-017-0315-1.
  • Sobanbua S, Dolkittikul S, Nakphaichit M, Keawsompong S, Nitisinprasert S. Antimicrobial peptide presenting potential strain-specific real time polymerase chain reaction assay for detecting the probiotic Lactobacillus reuteri KUB-AC5 in chicken intestine. Poult Sci. 2020;99(1):526–535. doi:10.3382/ps/pez549.
  • Guo JL, Ren CL, Han X, Huang WD, You YL, Zhan JC. Role of IgA in the early-life establishment of the gut microbiota and immunity: implications for constructing a healthy start. Gut Microbes. 2021;13:1–21.
  • Chen CY, Chen CK, Chen YY, Fang A, Shaw GT, Hung CM, Wang D. Maternal gut microbes shape the early-life assembly of gut microbiota in passerine chicks via nests. Microbiome. 2020;8(1):129. doi:10.1186/s40168-020-00896-9.
  • Sanlier N, Gokcen BB, Sezgin AC. Health benefits of fermented foods. Crit Rev Food Sci Nutr. 2019;59(3):506–527. doi:10.1080/10408398.2017.1383355.
  • Yang B, Ding MF, Chen YQ, Han FZ, Yang CY, Zhao JX, Malard P, Stanton C, Ross RP, Zhang H, et al. Development of gut microbiota and bifidobacterial communities of neonates in the first 6 weeks and their inheritance from mother. Gut Microbes. 2021;13(1):1–13. doi:10.1080/19490976.2021.1908100.
  • Wu Y, Yu JX, Liu XY, Wang WL, Chen Z, Qiao J, Liu X, Jin H, Li X, Wen L, et al. Gestational diabetes mellitus-associated changes in the breast milk metabolome alters the neonatal growth trajectory. Clin Nutr. 2021;40(6):4043–4054.
  • Roytio 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. Brit J Nutr. 2018;120(5):599–600. doi:10.1017/S0007114518001940.
  • Mandal S, Godfrey KM, Mcdonald D, Treuren WV, Bjornholt 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.
  • Carrothers JM, York MA, Brooker SL, Lackey KA, Williams JE, Shafii B, Price WJ, Settles ML, McGuire MA, McGuire MK, et al. Fecal microbial community structure is stable over time and related to variation in macronutrient and micronutrient intakes in lactating Women. J Nutr. 2015;145(10):2379–2388. doi:10.3945/jn.115.211110.
  • Ghosh TS, Arnoux J, O’Toole PW. Metagenomic analysis reveals distinct patterns of gut lactobacillus prevalence, abundance, and geographical variation in health and disease. Gut Microbes. 2020;12(1):1–19. doi:10.1080/19490976.2020.1822729.
  • Kumbhare SV, Kumar H, Chowdhury SP, Dhotre DP, Endo A, Matto J, Ouwehand AC, Rautava S, Joshi R, Patil NP, et al. A cross-sectional comparative study of gut bacterial community of Indian and Finnish children. Sci Rep. 2017;7(1):10555. doi:10.1038/s41598-017-11215-y.
  • Rubio-Del-Campo A, Gozalbo-Rovira R, Moya-Gonzálvez EM, Alberola J, Rodríguez-Díaz J, Yebra MJ. Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2021.1914377.
  • Aaltonen J, Ojala T, Laitinen K, Poussa T, Ozanne S, Isolauri E. Impact of maternal diet during pregnancy and breastfeeding on infant metabolic programming: a prospective randomized controlled study. Eur J Clin Nutr. 2011;65:10–19.
  • Ashino NG, Saito KN, Souza FD, Nakutz FS, Roman EA, Velloso LA, Torsoni AS, Torsoni MA. Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver. J Nutr Biochem. 2012;23(4):341–348. doi:10.1016/j.jnutbio.2010.12.011.
  • 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;13:1–30.
  • Vogt MC, Paeger L, Hess S, Steculorum SM, Awazawa M, Hampel B, Neupert S, Nicholls H, Mauer J, Hausen A, et al. Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell. 2014;156(3):495–509. doi:10.1016/j.cell.2014.01.008.
  • Alderete TL, Jones RB, Shaffer JP, Holzhausen EA, Patterson WB, Kazemian E, Chatzi L, Knight R, Plows JF, Berger PK, et al. Early life gut microbiota is associated with rapid infant growth in Hispanics from Southern California. Gut Microbes. 2021;13(1):1961203. doi:10.1080/19490976.2021.1961203.
  • Babakobi MD, Reshef L, Gihaz S, Belgorodsky B, Fishman A, Bujanover Y, Gophna U. Effect of maternal diet and milk lipid composition on the infant gut and maternal milk microbiomes. Nutrients. 2020;12(9):2539. doi:10.3390/nu12092539.
  • Leblois J, Massart S, Li B, Wavreille J, Bindelle J, Everaert N. Modulation of piglets’ microbiota: differential effects by a high wheat bran maternal diet during gestation and lactation. Sci Rep. 2017;7(1):7426. doi:10.1038/s41598-017-07228-2.
  • Passlack N, Vahjen W, Zentek J. Dietary inulin affects the intestinal microbiota in sows and their suckling piglets. BMC Vet Res. 2015;11(1):51. doi:10.1186/s12917-015-0351-7.
  • Marco ML, Sanders ME, Ganzle M, Arrieta MC, Cotter PD, De Vuyst L, Hill C, Holzapfel W, Lebeer S, Merenstein D, et al. The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on fermented foods. Nat Rev Gastroenterol Hepatol. 2021;18(3):196–208. doi:10.1038/s41575-020-00390-5.
  • Peng M, Tabashsum Z, Patel P, Bernhardt C, Biswas C, Meng J, Biswas D. Prevention of enteric bacterial infections and modulation of gut microbiota with conjugated linoleic acids producing Lactobacillus in mice. Gut Microbes. 2020;11(3):433–452. doi:10.1080/19490976.2019.1638724.
  • Zhang JC, Zhao JS, Jin H, Lv R, Shi HW, De GZ, Yang B, Sun Z, Zhang H. Probiotics maintain the intestinal microbiome homeostasis of the sailors during a long sea voyage. Gut Microbes. 2020;11(4):930–943. doi:10.1080/19490976.2020.1722054.
  • Cheng SS, Ma X, Geng SJ, Jiang XM, Li Y, Hu LS, Li J, Wang Y, Han X. Fecal microbiota transplantation beneficially regulates intestinal mucosal autophagy and alleviates gut barrier injury. mSystems. 2018;3(5):e00137–18. doi:10.1128/mSystems.00137-18.
  • Rabe H, Lundell A-C, Sjöberg F, Ljung A, Strömbeck A, Gio-Batta M, Maglio C, Nordström I, Andersson K, Nookaew I, et al. Neonatal gut colonization by Bifidobacterium is associated with higher childhood cytokine responses. Gut Microbes. 2020;12(1):1–14. doi:10.1080/19490976.2020.1847628.
  • Wang C, Wei SY, Xu BC, Hao LH, Su WF, Jin ML, Wang YZ. Bacillus subtilis and Enterococcus faecium co-fermented feed regulates lactating sow’s performance, immune status and gut microbiota. Microb Biotechnol. 2021;14(2):614–627. doi:10.1111/1751-7915.13672.
  • Ramanan D, Sefik E, Galvan-Pena S, Wu M, Yang L, Yang Z, Kostic A, Golovkina TV, Kasper DL, Mathis D, et al. An immunologic mode of multigenerational transmission governs a gut Treg setpoint. Cell. 2020;181(6):1276–90 e13. doi:10.1016/j.cell.2020.04.030.
  • Liu BS, Zhu XY, Cui YL, Wang WJ, Liu H, Li ZD, Guo Z, Ma S, Li D, Wang C, et al. Consumption of dietary fiber from different sources during pregnancy alters sow gut microbiota and improves performance and reduces inflammation in sows and piglets. mSystems. 2021;6(1):e00591–20. doi:10.1128/mSystems.00591-20.
  • Neurath MF. Cytokines in inflammatory bowel disease. Nat Rev Immunol. 2014;14(5):329–342. doi:10.1038/nri3661.
  • Liu C, Huang SM, Wu ZH, Li TT, Li N, Zhang B, Han D, Wang S, Zhao J, Wang J, et al. Cohousing-mediated microbiota transfer from milk bioactive components-dosed mice ameliorate colitis by remodeling colonic mucus barrier and lamina propria macrophages. Gut Microbes. 2021;13(1):1–23. doi:10.1080/19490976.2021.1903826.
  • Rao Y, Kuang ZQ, Li C, Guo SY, Xu YH, Zhao DD, Hu Y, Song B, Jiang Z, Ge Z, et al. Gut Akkermansia muciniphila ameliorates metabolic dysfunction-associated fatty liver disease by regulating the metabolism of L-aspartate via gut-liver axis. Gut Microbes. 2021;13(1):1–19. doi:10.1080/19490976.2021.1927633.
  • Singh P, Alm EJ, Kelley JM, Cheng V, Smith M, Kassam Z, Nee J, Iturrino J, Lembo A. Effect of antibiotic pretreatment on bacterial engraftment after Fecal Microbiota Transplant (FMT) in IBS-D. Gut Microbes. 2022;14(1):2020067. doi:10.1080/19490976.2021.2020067.
  • Paul HA, Collins KH, Nicolucci AC, Urbanski SJ, Hart DA, Vogel HJ, Reimer RA. Maternal prebiotic supplementation reduces fatty liver development in offspring through altered microbial and metabolomic profiles in rats. FASEB J. 2019;33(4):5153–5167. doi:10.1096/fj.201801551R.
  • Wang C, Shi CY, Su WF, Jin ML, Xu BC, Hao LH, Zhang Y, Lu Z, Wang F, Wang Y, et al. Dynamics of the physicochemical characteristics, microbiota, and metabolic functions of soybean meal and corn mixed substrates during two-stage solid-State fermentation. mSystems. 2020;5(1):00501–19. doi:10.1128/mSystems.00501-19.
  • Holani R, Babbar A, Blyth GAD, Lopes F, Jijon H, McKay DM, Hollenberg MD, Cobo ER. Cathelicidin-mediated lipopolysaccharide signaling via intracellular TLR4 in colonic epithelial cells evokes CXCL8 production. Gut Microbes. 2020;12(1):1785802. doi:10.1080/19490976.2020.1785802.
  • Deng XC, Wang YD, Tian L, Yang ML, He SY, Liu YP, Jianxin Cao JX, Cheng GG. Anneslea fragrans wall. ameliorates ulcerative colitis via inhibiting NF-kappaB and MAPK activation and mediating intestinal barrier integrity. J Ethnopharmacol. 2021;278:114304. doi:10.1016/j.jep.2021.114304.
  • Wu HQ, Xie S, Miao JF, Li YC, Wang ZH, Wang MJ, Yu Q. Lactobacillus reuteri maintains intestinal epithelial regeneration and repairs damaged intestinal mucosa. Gut Microbes. 2020;11(4):997–1014. doi:10.1080/19490976.2020.1734423.
  • Hemarajata P, Versalovic J. Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap Adv Gastroenterol. 2013;6(1):39–51. doi:10.1177/1756283X12459294.