Why Are Bifidobacteria Important for Infants?

Gerrit A Stuivenberg, Jeremy P Burton, Peter A Bron, Gregor Reid, Gerrit A Stuivenberg, Jeremy P Burton, Peter A Bron, Gregor Reid

Abstract

The presence of Bifidobacterium species in the maternal vaginal and fecal microbiota is arguably an evolutionary trait that allows these organisms to be primary colonizers of the newborn intestinal tract. Their ability to utilize human milk oligosaccharides fosters their establishment as core health-promoting organisms throughout life. A reduction in their abundance in infants has been shown to increase the prevalence of obesity, diabetes, metabolic disorder, and all-cause mortality later in life. Probiotic strains have been developed as supplements for premature babies and to counter some of these ailments as well as to confer a range of health benefits. The ability to modulate the immune response and produce short-chain fatty acids, particularly acetate and butyrate, that strengthen the gut barrier and regulate the gut microbiome, makes Bifidobacterium a core component of a healthy infant through adulthood.

Keywords: Bifidobacterium; gut microbiome; infants; probiotics.

Conflict of interest statement

P.A.B. is an employee of SEED, a producer of a synbiotic product. G.R. consults for SEED and KGK Science.

Figures

Figure 1
Figure 1
Influence of bifidobacteria on promoting a healthy gut microbiota and factors that affect their colonization.

References

    1. Hinde K., German J.B. Food in an evolutionary context: Insights from mother’s milk. J. Sci. Food Agric. 2012;92:2219–2223. doi: 10.1002/jsfa.5720.
    1. Aagaard K., Ma J., Antony K.M., Ganu R., Petrosino J., Versalovic J. The Placenta Harbors a Unique Microbiome. Sci. Transl. Med. 2014;6:237ra65. doi: 10.1126/scitranslmed.3008599.
    1. Dudley D.J. The placental microbiome: Yea, nay or maybe? Brit. J. Obstet. Gynecol. 2020;127:170. doi: 10.1111/1471-0528.15994.
    1. Fricke W.F., Ravel J. Microbiome or no microbiome: Are we looking at the prenatal environment through the right lens? Microbiome. 2021;9:9. doi: 10.1186/s40168-020-00947-1.
    1. Burton J., Dixon J., Reid G. Detection of Bifidobacterium species and Gardnerella vaginalis in the vagina using PCR and denaturing gradient gel electrophoresis (DGGE) Int. J. Gynecol. Obstet. 2003;81:61–63. doi: 10.1016/S0020-7292(02)00408-3.
    1. Sirilun S., Takahashi H., Boonyaritichaikij S., Chaiyasut C., Lertruangpanya P., Koga Y., Mikami K. Impact of maternal bifidobacteria and the mode of delivery on Bifidobacterium microbiota in infants. Benef. Microbes. 2015;6:767–774. doi: 10.3920/BM2014.0124.
    1. Freitas A.C., Hill J.E. Bifidobacteria isolated from vaginal and gut microbiomes are indistinguishable by comparative genomics. PLoS One. 2018;13:e0196290. doi: 10.1371/journal.pone.0196290.
    1. Turroni F., Marchesi J.R., Foroni E., Gueimonde M., Shanahan F., Margolles A., Van Sinderen D., Ventura M. Microbiomic analysis of the bifidobacterial population in the human distal gut. ISME J. 2009;3:745–751. doi: 10.1038/ismej.2009.19.
    1. Tojo R., Suárez A., Clemente M.G., de los Reyes-Gavilán C.G., Margolles A., Gueimonde M., Ruas-Madiedo P. Intestinal microbiota in health and disease: Role of bifidobacteria in gut homeostasis. World J. Gastroenterol. 2014;20:15163–15176. doi: 10.3748/wjg.v20.i41.15163.
    1. Stappenbeck T.S., Hooper L.V., Gordon J.I. Nonlinear partial differential equations and applications: Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA. 2002;99:15451–15455. doi: 10.1073/pnas.202604299.
    1. Wilmanski T., Diener C., Rappaport N., Patwardhan S., Wiedrick J., Lapidus J., Earls J.C., Zimmer A., Glusman G., Robinson M., et al. Gut microbiome pattern reflects healthy ageing and predicts survival in humans. Nat. Metab. 2021;3:274–286. doi: 10.1038/s42255-021-00348-0.
    1. Rinninella E., Raoul P., Cintoni M., Franceschi F., Miggiano G.A., Gasbarrini A., Mele M.C. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019;7:14. doi: 10.3390/microorganisms7010014.
    1. Laterza L., Rizzatti G., Gaetani E., Chiusolo P., Gasbarrini A. The gut microbiota and immune system relationship in human graft-versus-host disease. Mediterr. J. Hematol. Infect. Dis. 2016;8:2016025. doi: 10.4084/mjhid.2016.025.
    1. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., Fernandes G.D.R., Tap J., Bruls T., Batto J.M., et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–180. doi: 10.1038/nature09944.
    1. 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;17:690–703. doi: 10.1016/j.chom.2015.04.004.
    1. Lewis Z.T., Mills D.A. Global Landscape of Nutrition Challenges in Infants and Children. Volume 88. Karger Medical and Scientific Publishers; Basel, Switzerland: 2017. Differential establishment of bifidobacteria in the breastfed infant gut; pp. 149–159.
    1. Milani C., Duranti S., Bottacini F., Casey E., Turroni F., Mahony J., Belzer C., Delgado Palacio S., Arboleya Montes S., Mancabelli L., et al. The first microbial colonizers of the human gut: Composition, activities, and health implications of the infant gut microbiota. Microbiol. Mol. Biol. Rev. 2017;81:e00036-17. doi: 10.1128/MMBR.00036-17.
    1. Turroni F., Milani C., Duranti S., Ferrario C., Lugli G.A., Mancabelli L., Van Sinderen D., Ventura M. Bifidobacteria and the infant gut: An example of co-evolution and natural selection. Cell. Mol. Life Sci. 2018;75:103–118. doi: 10.1007/s00018-017-2672-0.
    1. Sakanaka M., Gotoh A., Yoshida K., Odamaki T., Koguchi H., Xiao J.-Z., Kitaoka M., Katayama T. Varied pathways of infant gut-associated Bifidobacterium to assimilate human milk oligosaccharides: Prevalence of the gene set and its correlation with bifidobacteria-rich microbiota formation. Nutrients. 2019;12:71. doi: 10.3390/nu12010071.
    1. Devika N.T., Raman K. Deciphering the metabolic capabilities of bifidobacteria using genome-scale metabolic models. Sci. Rep. 2019;9:18222. doi: 10.1038/s41598-019-54696-9.
    1. Duar R.M., Casaburi G., Mitchell R.D., Scofield L.N., Ramirez C.A.O., Barile D., Henrick B.M., Frese S.A. Comparative genome analysis of Bifidobacterium longum subsp. infantis strains reveals variation in human milk oligosaccharide utilization genes among commercial probiotics. Nutrients. 2020;12:3247. doi: 10.3390/nu12113247.
    1. Lawson M.A.E., O’neill I.J., Kujawska M., Javvadi S.G., Wijeyesekera A., Flegg Z., Chalklen L., Hall L.J. Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem. ISME J. 2019;14:635–648. doi: 10.1038/s41396-019-0553-2.
    1. Taft D.H., Liu J., Maldonado-Gomez M.X., Akre S., Huda M.N., Ahmad S.M., Stephensen C.B., Mills D.A. Bifidobacterial dominance of the gut in early life and acquisition of antimicrobial resistance. mSphere. 2018;3:e00441-18. doi: 10.1128/mSphere.00441-18.
    1. Grzeskowiak L., Collado M.C., Mangani C., Maleta K., Laitinen K., Ashorn P., Isolauri E., Salminen S. Distinct gut microbiota in southeastern African and northern European infants. J. Pediatr. Gastroenterol. Nutr. 2012;54:812–816. doi: 10.1097/MPG.0b013e318249039c.
    1. Garrido D., Ruiz-Moyano S., Lemay D., Sela D.A., German J.B., Mills D.A. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci. Rep. 2015;5:13517. doi: 10.1038/srep13517.
    1. Underwood M.A., German J.B., Lebrilla C.B., Mills D.A. Bifidobacterium longum subspecies infantis: Champion colonizer of the infant gut. Pediatr. Res. 2015;77:229–235. doi: 10.1038/pr.2014.156.
    1. Underwood M.A., Kalanetra K.M., Bokulich N.A., Lewis Z.T., Mirmiran M., Tancredi D., Mills D.A. A comparison of two probiotic strains of bifidobacteria in premature infants. J. Pediatr. 2013;163:1585–1591.e9. doi: 10.1016/j.jpeds.2013.07.017.
    1. De Simone C. The unregulated probiotic market. Clin. Gastroenterol. Hepatol. 2019;17:809–817. doi: 10.1016/j.cgh.2018.01.018.
    1. Stuivenberg G., Daisley B., Akouris P., Reid G. In vitro assessment of histamine and lactate production by a multi-strain synbiotic. J. Food Sci. Technol. 2021:1–9. doi: 10.1007/s13197-021-05327-7.
    1. Puebla-Barragan S., Watson E., van der Veer C., Chmiel J., Carr C., Burton J., Sumarah M., Kort R., Reid G. Interstrain variability of human vaginal Lactobacillus crispatus for metabolism of biogenic amines and antimicrobial activity against urogenital pathogens. Molecules. 2021;26:4538. doi: 10.3390/molecules26154538.
    1. E Silva A.C.S., Oliveira E.A., Mak R.H. Urinary tract infection in pediatrics: An overview. J. Pediatr. 2020;96((Suppl. S1)):65–79. doi: 10.1016/j.jped.2019.10.006.
    1. Ewaschuk J.B., Diaz H., Meddings L., Diederichs B., Dmytrash A., Backer J., Looijer-van Langen M., Madsen K.L. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Liver Physiol. 2008;295:G1025–G1034.
    1. Alessandri G., Ossiprandi M.C., Mac Sharry J., Van Sinderen D., Ventura M. Bifidobacterial dialogue with its human host and consequent modulation of the immune system. Front. Immunol. 2019;10:2348. doi: 10.3389/fimmu.2019.02348.
    1. Deo P.N., Deshmukh R. Oral microbiome: Unveiling the fundamentals. J. Oral Maxillofac. Pathol. 2019;23:122–128. doi: 10.4103/jomfp.JOMFP_304_18.
    1. Reid G., Gadir A.A., Barragan S.P., Dhir R. Deconstructing then priming gut microbiota resilience. OBM Hepatol. Gastroenterol. 2021;5:9. doi: 10.21926/obm.hg.2101055.
    1. Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–227. doi: 10.1038/nature11053.
    1. La Rosa P.S., Warner B.B., Zhou Y., Weinstock G.M., Sodergren E., Hall-Moore C.M., Stevens H.J., Bennett W.E., Shaikh N., Linneman L.A., et al. Patterned progression of bacterial populations in the premature infant gut. Proc. Natl. Acad. Sci. USA. 2014;111:12522–12527. doi: 10.1073/pnas.1409497111.
    1. Eggesbø M., Moen B., Peddada S., Baird D., Rugtveit J., Midtvedt T., Bushel P.R., Sekelja M., Rudi K. Development of gut microbiota in infants not exposed to medical interventions. Apmis. 2010;119:17–35. doi: 10.1111/j.1600-0463.2010.02688.x.
    1. Dominguez-Bello M.G., Costello E.K., Contreras M., Magris M., Hidalgo G., Fierer N., Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. USA. 2010;107:11971–11975. doi: 10.1073/pnas.1002601107.
    1. Ding T., Schloss P.D. Dynamics and associations of microbial community types across the human body. Nature. 2014;509:357–360. doi: 10.1038/nature13178.
    1. Derrien M., Alvarez A.-S., de Vos W.M. The gut microbiota in the first decade of life. Trends Microbiol. 2019;27:997–1010. doi: 10.1016/j.tim.2019.08.001.
    1. Avershina E., Lundgård K., Sekelja M., Dotterud C., Storrø O., Øien T., Johnsen R., Rudi K. Transition from infant- to adult-like gut microbiota. Environ. Microbiol. 2016;18:2226–2236. doi: 10.1111/1462-2920.13248.
    1. Sutharsan R., Mannan M., Doi S.A., Al Mamun A. Caesarean delivery and the risk of offspring overweight and obesity over the life course: A systematic review and bias-adjusted meta-analysis. Clin. Obes. 2015;5:293–301. doi: 10.1111/cob.12114.
    1. Korpela K., Zijlmans M.A.C., Kuitunen M., Kukkonen K., Savilahti E., Salonen A., De Weerth C., De Vos W.M. Childhood BMI in relation to microbiota in infancy and lifetime antibiotic use. Microbiome. 2017;5:26. doi: 10.1186/s40168-017-0245-y.
    1. Moens F., Verce M., De Vuyst L. Lactate- and acetate-based cross-feeding interactions between selected strains of lactobacilli, bifidobacteria and colon bacteria in the presence of inulin-type fructans. Int. J. Food Microbiol. 2017;241:225–236. doi: 10.1016/j.ijfoodmicro.2016.10.019.
    1. 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.
    1. Özcan E., Sela D.A. Inefficient metabolism of the human milk oligosaccharides Lacto-N-tetraose and Lacto-N-neotetraose shifts Bifidobacterium longum subsp. infantis physiology. Front. Nutr. 2018;5:46. doi: 10.3389/fnut.2018.00046.
    1. Stanford J., Charlton K., Stefoska-Needham A., Ibrahim R., Lambert K. The gut microbiota profile of adults with kidney disease and kidney stones: A systematic review of the literature. BMC Nephrol. 2020;21:215. doi: 10.1186/s12882-020-01805-w.
    1. Canani R.B., Di Costanzo M., Leone L., Pedata M., Meli R., Calignano A. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J. Gastroenterol. 2011;17:1519–1528. doi: 10.3748/wjg.v17.i12.1519.
    1. Clayton D.B., Pope J.C. The increasing pediatric stone disease problem. Ther. Adv. Urol. 2011;3:3–12. doi: 10.1177/1756287211400491.
    1. Bikbov B., Purcell C.A., Levey A.S., Smith M., Abdoli A., Abebe M., Adebayo O.M., Afarideh M., Agarwal S.K., Agudelo-Botero M., et al. Global, regional, and national burden of chronic kidney disease, 1990–2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2020;395:709–733. doi: 10.1016/S0140-6736(20)30045-3.
    1. Kelly S.M., Munoz-Munoz J., van Sinderen D. Plant glycan metabolism by bifidobacteria. Front. Microbiol. 2021;12:25. doi: 10.3389/fmicb.2021.609418.
    1. Turroni F., Özcan E., Milani C., Mancabelli L., Viappiani A., van Sinderen D., Sela D., Ventura M. Glycan cross-feeding activities between bifidobacteria under in vitro conditions. Front. Microbiol. 2015;6:1030. doi: 10.3389/fmicb.2015.01030.
    1. Egan M., Motherway M.O., Kilcoyne M., Kane M., Joshi L., Ventura M., Van Sinderen D. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucin-based medium. BMC Microbiol. 2014;14:282. doi: 10.1186/s12866-014-0282-7.
    1. Bunesova V., Lacroix C., Schwab C. Mucin cross-feeding of infant bifidobacteria and Eubacterium hallii. Microb. Ecol. 2018;75:228–238. doi: 10.1007/s00248-017-1037-4.
    1. Rios-Covian D., Gueimonde M., Duncan S.H., Flint H.J., de Los Reyes-Gavilan C. Enhanced butyrate formation by cross-feeding between Faecalibacterium prausnitzii and Bifidobacterium adolescentis. FEMS Microbiol. Lett. 2015;362:fnv176. doi: 10.1093/femsle/fnv176.
    1. Boger M.C.L., van Bueren A.L., Dijkhuizen L. Cross-feeding among probiotic bacterial strains on prebiotic inulin involves the extracellular exo-inulinase of Lactobacillus paracasei strain W20. Appl. Environ. Microbiol. 2018;84:e01539-18. doi: 10.1128/AEM.01539-18.
    1. Cheng C.C., Duar R.M., Lin X., Perez-Munoz M.E., Tollenaar S., Oh J.-H., van Pijkeren J.-P., Li F., van Sinderen D., Gänzle M.G., et al. Ecological importance of cross-feeding of the intermediate metabolite 1,2-propanediol between bacterial gut symbionts. Appl. Environ. Microbiol. 2020;86:e00190-20. doi: 10.1128/AEM.00190-20.
    1. Munoz J., James K., Bottacini F., Van Sinderen D. Biochemical analysis of cross-feeding behaviour between two common gut commensals when cultivated on plant-derived arabinogalactan. Microb. Biotechnol. 2020;13:1733–1747. doi: 10.1111/1751-7915.13577.
    1. Neu J., Rushing J. Cesarean versus vaginal delivery: Long-term infant outcomes and the hygiene hypothesis. Clin. Perinatol. 2011;38:321–331. doi: 10.1016/j.clp.2011.03.008.
    1. Yang W., Tian L., Luo J., Yu J. Ongoing supplementation of probiotics to caesarean-born neonates during the first month of life may impact the gut microbial. Am. J. Perinatol. 2021;38:1181–1191. doi: 10.1055/s-0040-1710559.
    1. Korpela K., Salonen A., Vepsäläinen O., Suomalainen M., Kolmeder C., Varjosalo M., Miettinen S., Kukkonen K., Savilahti E., Kuitunen M., et al. Probiotic supplementation restores normal microbiota composition and function in antibiotic-treated and in caesarean-born infants. Microbiome. 2018;6:182. doi: 10.1186/s40168-018-0567-4.
    1. Motherway M.O., Houston A., O’Callaghan G., Reunanen J., O’brien F., O’driscoll T., Casey P.G., De Vos W.M., Van Sinderen D., Shanahan F. A bifidobacterial pilus-associated protein promotes colonic epithelial proliferation. Mol. Microbiol. 2019;111:287–301. doi: 10.1111/mmi.14155.
    1. Penders J., Thijs C., Vink C., Stelma F.F., Snijders B., Kummeling I., Van den Brandt P.A., Stobberingh E.E. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118:511–521. doi: 10.1542/peds.2005-2824.
    1. Rutayisire E., Huang K., Liu Y., Tao F. The mode of delivery affects the diversity and colonization pattern of the gut microbiota during the first year of infants’ life: A systematic review. BMC Gastroenterol. 2016;16:86. doi: 10.1186/s12876-016-0498-0.
    1. Werlang I.C.R., Mueller N.T., Pizoni A., Wisintainer H., Matte U., de Almeida Martins Costa S.H., Ramos J.G.L., Goldani M.Z., Dominguez-Bello M.G., Goldani H.A.S. Associations of birth mode with cord blood cytokines, white blood cells, and newborn intestinal bifidobacteria. PLoS One. 2018;13:e0205962. doi: 10.1371/journal.pone.0205962.
    1. Morais L.H., Golubeva A.V., Moloney G.M., Moya-Pérez A., Ventura-Silva A.P., Arboleya S., Bastiaanssen T.F., O’sullivan O., Rea K., Borre Y., et al. Enduring behavioral effects induced by birth by caesarean section in the mouse. Curr. Biol. 2020;30:3761–3774.e6. doi: 10.1016/j.cub.2020.07.044.
    1. Fukuda S., Toh H., Hase K., Oshima K., Nakanishi Y., Yoshimura K., Tobe T., Clarke J.M., Topping D.L., Suzuki T., et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469:543–547. doi: 10.1038/nature09646.
    1. Henrick B.M., 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;184:3884–3898.e11. doi: 10.1016/j.cell.2021.05.030.
    1. He F., Ouwehand A.C., Isolauri E., Hashimoto H., Benno Y., Salminen S. Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. FEMS Immunol. Med. Microbiol. 2001;30:43–47. doi: 10.1111/j.1574-695X.2001.tb01548.x.
    1. Sun S., Luo L., Liang W., Yin Q., Guo J., Rush A.M., Lv Z., Liang Q., Fischbach M.A., Sonnenburg J.L., et al. Bifidobacterium alters the gut microbiota and modulates the functional metabolism of T regulatory cells in the context of immune checkpoint blockade. Proc. Natl. Acad. Sci. USA. 2020;177:27509–27515. doi: 10.1073/pnas.1921223117.
    1. Mansfield J.A., Bergin S.W., Cooper J.R., Olsen C.H. Comparative probiotic strain efficacy in the prevention of eczema in infants and children: A systematic review and meta-analysis. Mil. Med. 2014;179:580–592. doi: 10.7205/MILMED-D-13-00546.
    1. Xiao J.Z., Kondo S., Yanagisawa N., Takahashi N., Odamaki T., Iwabuchi N., Iwatsuki K., Kokubo S., Togashi H., Enomoto K., et al. Effect of probiotic Bifidobacterium longum BB536 [corrected] in relieving clinical symptoms and modulating plasma cytokine levels of Japanese cedar pollinosis during the pollen season. A randomized double-blind, placebo-controlled trial. J. Investig. Allergol. Clin. Immunol. 2006;16:86–93.
    1. Reid G., Gaudier E., Guarner F., Huffnagle G.B., Macklaim J.M., Munoz A.M., Martini M., Ringel-Kulka T., Sartor B.R., Unal R.R., et al. Responders and non-responders to probiotic interventions: How can we improve the odds? Gut Microbes. 2010;1:200–204. doi: 10.4161/gmic.1.3.12013.
    1. Ojima M.N., Gotoh A., Takada H., Odamaki T., Xiao J.-Z., Katoh T., Katayama T. Bifidobacterium bifidum suppresses gut inflammation caused by repeated antibiotic disturbance without recovering gut microbiome diversity in mice. Front. Microbiol. 2020;11:1349. doi: 10.3389/fmicb.2020.01349.
    1. Guardamagna O., Amaretti A., Puddu P.E., Raimondi S., Abello F., Cagliero P., Rossi M. Bifidobacteria supplementation: Effects on plasma lipid profiles in dyslipidemic children. Nutrition. 2014;30:831–836. doi: 10.1016/j.nut.2014.01.014.
    1. Van den Akker C.H., van Goudoever J.B., Shamir R., Domellöf M., Embleton N.D., Hojsak I., Lapillonne A., Mihatsch W.A., Canani R.B., Bronsky J., et al. Probiotics and preterm infants: A position paper by the European Society for Paediatric Gastroenterology Hepatology and Nutrition Committee on Nutrition and the European Society for Paediatric Gastroenterology Hepatology and Nutrition Working Group for Probiotics and Prebiotics. J. Pediatr. Gastroenterol. Nutr. 2020;70:664–680.
    1. Cheng L., Kiewiet M.B.G., Logtenberg M.J., Groeneveld A., Nauta A., Schols H.A., Walvoort M.T.C., Harmsen H.J.M., De Vos P. Effects of different human milk oligosaccharides on growth of bifidobacteria in monoculture and co-culture with Faecalibacterium prausnitzii. Front. Microbiol. 2020;11:569700. doi: 10.3389/fmicb.2020.569700.
    1. Silva Y.P., Bernardi A., Frozza R.L. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front. Endocrinol. 2020;11:25. doi: 10.3389/fendo.2020.00025.
    1. Dalile B., Van Oudenhove L., Vervliet B., Verbeke K. The role of short-chain fatty acids in microbiota-gut-brain communication. Nat. Rev. Gastroenterol. Hepatol. 2019;160:461–478. doi: 10.1038/s41575-019-0157-3.
    1. Townsend S., Caubillabarron J., Loc-Carrillo C., Forsythe S. The presence of endotoxin in powdered infant formula milk and the influence of endotoxin and Enterobacter sakazakii on bacterial translocation in the infant rat. Food Microbiol. 2007;24:67–74. doi: 10.1016/j.fm.2006.03.009.
    1. Liu G., Chen H., Chen J., Wang X., Gu Q., Yin Y. Effects of bifidobacteria-produced exopolysaccharides on human gut microbiota in vitro. Appl. Microbiol. Biotechnol. 2019;103:1693–1702. doi: 10.1007/s00253-018-9572-6.
    1. Collins S., Reid G. Distant site effects of ingested prebiotics. Nutrition. 2016;8:523. doi: 10.3390/nu8090523.
    1. Li L.-Z., Tao S.-B., Ma L., Fu P. Roles of short-chain fatty acids in kidney diseases. Chin. Med. J. 2019;132:1228–1232. doi: 10.1097/CM9.0000000000000228.
    1. Wang S., Lv D., Jiang S., Jiang J., Liang M., Hou F., Chen Y. Quantitative reduction in short-chain fatty acids, especially butyrate, contributes to the progression of chronic kidney disease. Clin. Sci. 2019;133:1857–1870. doi: 10.1042/CS20190171.
    1. Daisley B.A., Koenig D., Engelbrecht K., Doney L., Hards K., Al K.F., Reid G., Burton J.P. Emerging connections between gut microbiome bioenergetics and chronic metabolic diseases. Cell Rep. 2021;37:1–19. doi: 10.1016/j.celrep.2021.110087.
    1. Daisley B.A., Chanyi R.M., Abdur-Rashid K., Al K.F., Gibbons S., Chmiel J.A., Wilcox H., Reid G., Anderson A., Dewar M., et al. Abiraterone acetate preferentially enriches for the gut commensal Akkermansia muciniphila in castrate-resistant prostate cancer patients. Nat. Commun. 2020;11:4822. doi: 10.1038/s41467-020-18649-5.
    1. Duncan S.H., Hold G.L., Barcenilla A., Stewart C.S., Flint H.J. Roseburia intestinalis sp. nov., a novel saccharolytic, butyrate-producing bacterium from human faeces. Int. J. Syst. Evol. Microbiol. 2002;52:1615–1620. doi: 10.1099/00207713-52-5-1615.
    1. Shetty S.A., Boeren S., Bui T.P.N., Smidt H., De Vos W.M. Unravelling lactate-acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics. Environ. Microbiol. 2020;22:4863–4875. doi: 10.1111/1462-2920.15269.
    1. Dordević D., Jančíková S., Vítězová M., Kushkevych I. Hydrogen sulfide toxicity in the gut environment: Meta-analysis of sulfate-reducing and lactic acid bacteria in inflammatory processes. J. Adv. Res. 2021;27:55–69. doi: 10.1016/j.jare.2020.03.003.
    1. Wang G., Wang D., Huang L., Song Y., Chen Z., Du M. Enhanced production of volatile fatty acids by adding a kind of sulfate reducing bacteria under alkaline pH. Colloids Surf. B Biointerfaces. 2020;195:111249. doi: 10.1016/j.colsurfb.2020.111249.
    1. Sagheddu V., Patrone V., Miragoli F., Morelli L. Abundance and diversity of hydrogenotrophic microorganisms in the infant gut before the weaning period assessed by denaturing gradient gel electrophoresis and quantitative PCR. Front. Nutr. 2017;4:29. doi: 10.3389/fnut.2017.00029.
    1. Infante D., Segarra O., Le Luyer B. Dietary treatment of colic caused by excess gas in infants: Biochemical evidence. World J. Gastroenterol. 2011;17:2104–2108. doi: 10.3748/wjg.v17.i16.2104.
    1. Fukuda S., Toh H., Taylor T., Ohno H., Hattori M. Acetate-producing bifidobacteria protect the host from enteropathogenic infection via carbohydrate transporters. Gut Microbes. 2012;3:449–454. doi: 10.4161/gmic.21214.
    1. Golubeva A.V., Joyce S.A., Moloney G., Burokas A., Sherwin E., Arboleya S., Flynn I., Khochanskiy D., Moya-Pérez A., Peterson V., et al. Microbiota-related changes in bileaAcid & tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine. 2017;24:166–178. doi: 10.1016/j.ebiom.2017.09.020.
    1. Persico A.M., Napolioni V. Urinary p-cresol in autism spectrum disorder. Neurotoxicol. Teratol. 2013;36:82–90. doi: 10.1016/j.ntt.2012.09.002.
    1. Gabriele S., Sacco R., Altieri L., Neri C., Urbani A., Bravaccio C., Riccio M.P., Iovene M.R., Bombace F., De Magistris L., et al. Slow intestinal transit contributes to elevate urinary p-cresol level in Italian autistic children. Autism Res. 2016;9:752–759. doi: 10.1002/aur.1571.
    1. Pascucci T., Colamartino M., Fiori E., Sacco R., Coviello A., Ventura R., Puglisi-Allegra S., Turriziani L., Persico A.M. p-cresol alters brain dopamine metabolism and exacerbates autism-like behaviors in the BTBR mouse. Brain Sci. 2020;10:233. doi: 10.3390/brainsci10040233.
    1. Harambat J., Van Stralen K.J., Kim J.J., Tizard E.J. Epidemiology of chronic kidney disease in children. Pediatr. Nephrol. 2012;27:363–373. doi: 10.1007/s00467-011-1939-1.
    1. Nada A., Bonachea E.M., Askenazi D.J. Acute kidney injury in the fetus and neonate. Semin. Fetal Neonatal Med. 2017;22:90–97. doi: 10.1016/j.siny.2016.12.001.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner