Infant gut microbiota restoration: state of the art

Katri Korpela, Willem M de Vos, Katri Korpela, Willem M de Vos

Abstract

The gut microbiota has a central role in the programming of the host's metabolism and immune function, with both immediate and long-term health consequences. Recent years have witnessed an accumulation of understanding of the process of the colonization and development of the gut microbiota in infants. The natural gut microbiota colonization during birth is frequently disrupted due to C-section birth or intrapartum or postpartum antibiotic exposure, and consequently aberrant gut microbiota development is common. On a positive note, research has shown that restoration of normal gut microbiota development is feasible. We discuss here the current understanding of the infant microbiota, provide an overview of the sources of disturbances, and critically evaluate the evidence on early life gut microbiota restoration for improved health outcomes by analyzing published data from infant gut microbiota restoration studies.

Keywords: Intrapartum antibiotics; birth mode; breastfeeding; cesarean section; fecal microbiota transplant; lactic acid bacteria and bifidobacteria; vaginal seeding.

Conflict of interest statement

No potential conflict of interest were disclosed.

Figures

Figure 1.
Figure 1.
Gut microbiota development and its effects on current and later-life health.
Figure 2.
Figure 2.
Differences in gut microbiota composition between groups of infants stratified by birth mode and treatment. (a) scores on the first principal component, (b) relative abundance of bifidobacteriaceae, (c) relative abundance of bacteroidaceae. lighter colors refer to 1-month samples and darker colors to 3-month samples. asterisks indicate the significance of the difference from the vaginally born (“V”) group (blue) and the C-section born (“CS”) group (red), data from refs 4, 50, 82, 85, 86. statistical tests were conducted separately within each age group.
Figure 3.
Figure 3.
Efficacy of restoration of the microbial families that were significantly different between vaginally born and C-section born untreated infants. – indicates unsuccessful restoration (relative abundance is significantly different from the vaginally born), + indicates moderately successful restoration (no statistically significant difference in relative abundance from the vaginally born group, but difference in mean abundance > 25%), and ++ indicates full restoration (difference in mean relative abundance  .05).

References

    1. Favier CF, Vaughan EE, De Vos WM, Akkermans AD.. Molecular monitoring of succession of bacterial communities in human neonates. Applied and Environmental Microbiology. 2002;68(1):219–14. doi:10.1128/AEM.68.1.219-226.2002.
    1. Favier CF, de Vos WM, Akkermans AD. Development of bacterial and bifidobacterial communities in feces of newborn babies. Anaerobe. 2003;9(5):219–229. doi:10.1016/j.anaerobe.2003.07.001.
    1. Van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG. Duodenal infusion of donor feces for recurrent clostridium difficile. New England Journal of Medicine. 2013;368(5):407–415. doi:10.1056/NEJMoa1205037.
    1. Korpela K, Helve O, Kolho K, 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. doi:10.1016/j.cell.2020.08.047.
    1. Hanssen N, de Vos W, Nieuwdorp M. Fecal microbiota transplantation in human disease. from a murky past to a bright future? Cell Metab. 2021. in press;33(6):1098–1110. doi:10.1016/j.cmet.2021.05.005.
    1. Stiemsma LT, Michels KB. The role of the microbiome in the developmental origins of health and disease. Pediatrics. 2018;141(4). doi:10.1542/peds.2017-2437.
    1. Korpela K, de Vos WM. Early life colonization of the human gut: microbes matter everywhere. Current Opinion in Microbiology. 2018;44:70–78. doi:10.1016/j.mib.2018.06.003.
    1. Abrahamsson TR, Jakobsson HE, Andersson AF, Bjorksten B, Engstrand L, Jenmalm MC. Low diversity of the gut microbiota in infants with atopic eczema. Journal of Allergy and Clinical Immunology. 2012;129(2):434–440. doi:10.1016/j.jaci.2011.10.025.
    1. Abrahamsson T, Jakobsson H, Andersson AF, Björkstén B, Engstrand L, Jenmalm M. Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy. 2014;44(6):842–850. doi:10.1111/cea.12253.
    1. Azad MB, Konya T, Guttman DS, Field CJ, Sears MR, HayGlass KT, Mandhane PJ, Turvey SE, Subbarao P, Becker AB, et al. Infant gut microbiota and food sensitization: associations in the first year of life. Clinical & Experimental Allergy. 2015;45(3):632–643. doi:10.1111/cea.12487.
    1. Kostic AD, Gevers D, Siljander H, Vatanen T, Hyötyläinen T, Hämäläinen A, Peet A, Tillmann V, Pöhö P, Mattila I. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe. 2015;17(2):260–273. doi:10.1016/j.chom.2015.01.001.
    1. Korpela K, Zijlmans M, Kuitunen M, Kukkonen K, Savilahti E, Salonen A, de Weerth C, de Vos W. Childhood BMI in relation to microbiota in infancy and lifetime antibiotic use. Microbiome. 2017;5(1):26. doi:10.1186/s40168-017-0245-y.
    1. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PloS one. 2008;3(8):e3056. doi:10.1371/journal.pone.0003056.
    1. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Science Translational Medicine. 2014;6(237):237ra65. doi:10.1126/scitranslmed.3008599.
    1. Ardissone AN, Diomel M, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC, Murgas-Torrazza R, Sharma R, Hudak ML, Triplett EW. Meconium microbiome analysis identifies bacteria correlated with premature birth. PloS one. 2014;9(3):e90784. doi:10.1371/journal.pone.0090784.
    1. Collado MC, Rautava S, Aakko J, Isolauri E, Salminen S. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016;6(1):23129. doi:10.1038/srep23129.
    1. He Q, Kwok L, Xi X, Zhong Z, Ma T, Xu H, Meng H, Zhao F, Zhang H. The meconium microbiota shares more features with the amniotic fluid microbiota than the maternal fecal and vaginal microbiota. Gut Microbes. 2020;12(1):1794266. doi:10.1080/19490976.2020.1794266.
    1. Blaser MJ, Devkota S, McCoy KD, Relman DA, Yassour M, Young VB. Lessons learned from the prenatal microbiome controversy. Microbiome. 2021;9(1):1–7. doi:10.1186/s40168-020-00946-2.
    1. Walter J, Hornef MW. A philosophical perspective on the prenatal in utero microbiome debate. Microbiome. 2021;9(1):1–9. doi:10.1186/s40168-020-00979-7.
    1. Matsumiya Y, Kato N, Watanabe K, Kato H. Molecular epidemiological study of vertical transmission of vaginal lactobacillus species from mothers to newborn infants in Japanese, by arbitrarily primed polymerase chain reaction. J Infect Chemother. 2002;8(1):43–49. doi:10.1007/s101560200005.
    1. Makino H, Kushiro A, Ishikawa E, Kubota H, Gawad A, Sakai T, Oishi K, Martin R, Ben-Amor K, Knol J. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant’s microbiota. PloS one. 2013;8(11):e78331. doi:10.1371/journal.pone.0078331.
    1. Asnicar F, Manara S, Zolfo M, Truong DT, Scholz M, Armanini F, Ferrretti P, Gorfer V, Pedrotti A, Tett A. Studying vertical microbiome transmission from mothers to infants by strain-level metagenomic profiling. bioRxiv 2.1. 2016;e00164–16.
    1. Duranti S, Lugli GA, Mancabelli L, Armanini F, Turroni F, James K, Ferretti P, Gorfer V, Ferrario C, Milani C. Maternal inheritance of bifidobacterial communities and bifidophages in infants through vertical transmission. Microbiome. 2017;5(1):66. doi:10.1186/s40168-017-0282-6.
    1. Korpela K, Costea P, Coelho LP, Kandels-Lewis S, Willemsen G, Boomsma DI, Segata N, Bork P. Selective maternal seeding and environment shape the human gut microbiome. Genome Res. 2018;28(4):561–568. doi:10.1101/gr.233940.117.
    1. Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, Armanini F, Truong DT, Manara S, Zolfo M. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 2018;24(1):133–145. doi:10.1016/j.chom.2018.06.005.
    1. Marcobal A, Sonnenburg J. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect. 2012;18:12–15. doi:10.1111/j.1469-0691.2012.03863.x.
    1. Browne HP, Forster SC, Anonye BO, Kumar N, Neville BA, Stares MD, Goulding D, Lawley TD. Culturing of ‘unculturable’human microbiota reveals novel taxa and extensive sporulation. Nature. 2016;533(7604):543–546. doi:10.1038/nature17645.
    1. Thurl S, Munzert M, Boehm G, Matthews C, Stahl B. Systematic review of the concentrations of oligosaccharides in human milk. Nutrition Reviews. 2017;75(11):920–933. doi:10.1093/nutrit/nux044.
    1. Coppa G, Pierani P, Zampini L, Bruni S, Carloni I, Gabrielli O. Characterization of oligosaccharides in milk and feces of breast-fed infants by high-performance anion-exchange chromatography. Advances in Experimental Medicine and Biology. 2001;501:307–314. doi:10.1007/978-1-4615-1371-1_38.
    1. Ho NT, Li F, Lee-Sarwar KA, Tun HM, Brown BP, Pannaraj PS, Bender J, Azad M, Thompson A, Weiss S, et al. Meta-analysis of effects of exclusive breastfeeding on infant gut microbiota across populations. Nat Commun. 2018;9(1):1–13. doi:10.1038/s41467-018-06473-x.
    1. Zoetendal EG, Akkermans AD, Vliet WM A-V, de Visser JAGM, de Vos WM. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb Ecol Health Dis. 2001;13:129–134.
    1. Goodrich JK, Davenport ER, Clark AG, Ley RE. The relationship between the human genome and microbiome comes into view. Annual Review of Genetics. 2017;51(1):413–433. doi:10.1146/annurev-genet-110711-155532.
    1. Wacklin P, Tuimala J, Nikkilä J, Tims S, Mäkivuokko H, Alakulppi N, Laine P, Rajilic-Stojanovic M, Paulin L, de Vos WM. Faecal microbiota composition in adults is associated with the FUT2 gene determining the secretor status. PLoS One. 2014;9(4):e94863. doi:10.1371/journal.pone.0094863.
    1. 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.
    1. Nissilä E, Korpela K, Lokki AI, Paakkanen R, Jokiranta S, de Vos WM, Lokki M, Kolho K, Meri S. C4 gene influences intestinal microbiota through complement activation in patients with paediatric-onset inflammatory bowel disease. Clinical and Experimental Immunology. 2017;190(3):394–405. doi:10.1111/cei.13040.
    1. Zijlmans MA, Korpela K, Riksen-Walraven JM, de Vos WM, de Weerth C. Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology. 2015;53:233–245. doi:10.1016/j.psyneuen.2015.01.006.
    1. McLean C, Jun S, Kozyrskyj A. Impact of maternal smoking on the infant gut microbiota and its association with child overweight: a scoping review. World J Pediatr. 2019;15(4):341–349. doi:10.1007/s12519-019-00278-8.
    1. Stanislawski MA, Dabelea D, Wagner BD, Sontag MK, Lozupone CA, Eggesbø M. Pre-pregnancy weight, gestational weight gain, and the gut microbiota of mothers and their infants. Microbiome. 2017;5(1):1–12. doi:10.1186/s40168-017-0332-0.
    1. Koleva PT, Tun HM, Konya T, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, Subbarao P, Sears MR, Scott JA, et al. Sex-specific impact of asthma during pregnancy on infant gut microbiota. European Respiratory Journal. 2017;50(5):10.1183/13993003.00280–2017. doi:10.1183/13993003.00280-2017.
    1. Soderborg TK, Carpenter CM, Janssen RC, Weir TL, Robertson CE, Ir D, Young BE, Krebs NF, Hernandez TL, Barbour LA. Gestational diabetes is uniquely associated with altered early seeding of the infant gut microbiota. Front Endocrinol (Lausanne). 2020;11:603021. doi:10.3389/fendo.2020.603021.
    1. Laforest-Lapointe I, Becker AB, Mandhane PJ, Turvey SE, Moraes TJ, Sears MR, Subbarao P, Sycuro LK, Azad MB, Arrieta M. 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.
    1. Penders J, Thijs C, Vink C, Stelma FF, Snijders B, Kummeling I, van den Brandt PA, Stobberingh EE. Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics. 2006;118(2):511–521. doi:10.1542/peds.2005-2824.
    1. Fallani M, Young D, Scott J, Norin E, Amarri S, Adam R, Aguilera M, Khanna S, Gil A, Edwards CA, et al. Intestinal microbiota of 6-week-old infants across Europe: geographic influence beyond delivery mode, breast-feeding, and antibiotics. Journal of Pediatric Gastroenterology & Nutrition. 2010;51(1):77–84. doi:10.1097/MPG.0b013e3181d1b11e.
    1. Stokholm J, Thorsen J, Chawes BL, Schjørring S, Krogfelt KA, Bønnelykke K, Bisgaard H. Cesarean section changes neonatal gut colonization. Journal of Allergy and Clinical Immunology. 2016;138(3):881–889. doi:10.1016/j.jaci.2016.01.028.
    1. Shao Y, Forster SC, Tsaliki E, Vervier K, Strang A, Simpson N, Kumar N, Stares MD, Rodger A, Brocklehurst P. Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature. 2019;574(7776):117–121. doi:10.1038/s41586-019-1560-1.
    1. Galazzo G, van Best N, Bervoets L, Dapaah IO, Savelkoul PH, Hornef MW, Hutton EK, Morrison K, Holloway AC, McDonald H, et al., “Development of the microbiota and associations with birth mode, diet, and atopic disorders in a longitudinal analysis of stool samples, collected from infancy through early childhood,” Gastroenterology 158, no. 6 (2020. 1): 1584–1596. doi:10.1053/j.gastro.2020.01.024.
    1. Brooks B, Olm MR, Firek BA, Baker R, Thomas BC, Morowitz MJ, Banfield JF. Strain-resolved analysis of hospital rooms and infants reveals overlap between the human and room microbiome. Nat Commun. 2017;8(1):1–7. doi:10.1038/s41467-017-02018-w.
    1. Azad MB, Konya T, Persaud RR, Guttman DS, Chari RS, Field CJ, Sears MR, Mandhane P, Turvey S, Subbarao P. Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: a prospective cohort study. BJOG: Int J Obstet Gynaecol. 2016;123(6):983–993. doi:10.1111/1471-0528.13601.
    1. Stearns JC, Simioni J, Gunn E, McDonald H, Holloway AC, Thabane L, Mousseau A, Schertzer JD, Ratcliffe EM, Rossi L. Intrapartum antibiotics for GBS prophylaxis alter colonization patterns in the early infant gut microbiome of low risk infants. Sci Rep. 2017;7(1):1–9.90. doi:10.1038/s41598-017-16606-9.
    1. Jokela J, Korpela K, Jian C, Dikareva E, Nikkonen A, Saisto T, Skogberg K, de Vos W, Kolho K-L, Salonen A. Quantitative insights into effects of intrapartum antibiotics and birth mode on infant gut microbiota in relation to well-being during the first year of life. Gut Microbes. 2022. doi:10.1080/19490976.2022.2095775.
    1. Bossung V, Lupatsii M, Dashdorj L, Tassiello O, Jonassen S, Pagel J, Demmert M, Wolf EA, Rody A, Waschina S, et al. Timing of antimicrobial prophylaxis for cesarean section is critical for gut microbiome development in term born infants. Gut Microbes. 2022 Dec 31;14(1):2038855. doi:10.1080/19490976.2022.2038855.
    1. Kamal SS, Hyldig N, Ł K, Greisen G, Krogfelt KA, Zachariassen G, Nielsen DS. Impact of early exposure to cefuroxime on the composition of the gut microbiota in infants following cesarean delivery. J Pediatr. 2019;210:99–105.e2. doi:10.1016/j.jpeds.2019.03.001.
    1. Dierikx T, Berkhout D, Eck A, Tims S, van Limbergen J, Visser D, de Boer M, de Boer N, Touw D, Benninga M, et al. Influence of timing of maternal antibiotic administration during caesarean section on infant microbial colonisation: a randomised controlled trial. Gut. 2021;71.9(2022):324767.
    1. Aloisio I, Mazzola G, Corvaglia LT, Tonti G, Faldella G, Biavati B, Di Gioia D. Influence of intrapartum antibiotic prophylaxis against group B streptococcus on the early newborn gut composition and evaluation of the anti-streptococcus activity of bifidobacterium strains. Applied Microbiology and Biotechnology. 2014;98(13):6051–6060. doi:10.1007/s00253-014-5712-9.
    1. Stokholm J, Schjørring S, Pedersen L, Bischoff AL, Følsgaard N, Carson CG, Chawes BL, Bønnelykke K, Mølgaard A, Krogfelt KA. Prevalence and predictors of antibiotic administration during pregnancy and birth. PloS one. 2013;8(12):e82932. doi:10.1371/journal.pone.0082932.
    1. Persaud RR, Azad MB, Chari RS, Sears MR, Becker AB, Kozyrskyj AL. CHILD study investigators. perinatal antibiotic exposure of neonates in Canada and associated risk factors: a population-based study. J Matern Fetal Neonatal Med. 2015;28(10):1190–1195. doi:10.3109/14767058.2014.947578.
    1. Korpela K, Salonen A, Saxen H, Nikkonen A, Peltola V, Jaakkola T, de Vos W, Kolho K. Antibiotics in early life associate with specific gut microbiota signatures in a prospective longitudinal infant cohort. Pediatric Research. 2020;88(3):438–443. doi:10.1038/s41390-020-0761-5.
    1. Korpela K, Salonen A, Virta LJ, Kekkonen RA, de Vos WM. Association of early-life antibiotic use and protective effects of breastfeeding: role of the intestinal microbiota. JAMA Pediatr. 2016;170(8):750–757. doi:10.1001/jamapediatrics.2016.0585.
    1. Karav S, Casaburi G, Frese SA. Reduced colonic mucin degradation in breastfed infants colonized by bifidobacterium longum subsp . infantis EVC001. FEBS Open Bio. 2018;8(10):1649–1657. doi:10.1002/2211-5463.12516.
    1. Pärtty A, Kalliomäki M, Endo A, Salminen S, Isolauri E. Compositional development of bifidobacterium and lactobacillus microbiota is linked with crying and fussing in early infancy. PLoS One. 2012;7(3):e32495. doi:10.1371/journal.pone.0032495.
    1. de Weerth C, Fuentes S, Puylaert P, de Vos WM. Intestinal microbiota of infants with colic: development and specific signatures. Pediatrics. 2013;131(2):e550–8. doi:10.1542/peds.2012-1449.
    1. Schreck Bird A, Gregory PJ, Jalloh MA, Risoldi Cochrane Z, Hein DJ. Probiotics for the treatment of infantile colic: a systematic review. J Pharm Pract. 2017;30(3):366–374. doi:10.1177/0897190016634516.
    1. Hansen S, Halldorsson T, Olsen S, Rytter D, Bech B, Granström C, Henriksen T, Chavarro J. Birth by cesarean section in relation to adult offspring overweight and biomarkers of cardiometabolic risk. International Journal of Obesity. 2018;42(1):15–19. doi:10.1038/ijo.2017.175.
    1. Keag OE, Norman JE, Stock SJ. Long-term risks and benefits associated with cesarean delivery for mother, baby, and subsequent pregnancies: systematic review and meta-analysis. PLoS Med. 2018;15(1):e1002494. doi:10.1371/journal.pmed.1002494.
    1. Andersen V, Möller S, Jensen PB, Møller FT, Green A. Caesarean delivery and risk of chronic inflammatory diseases (inflammatory bowel disease, rheumatoid arthritis, coeliac disease, and diabetes mellitus): a population based registry study of 2,699,479 births in Denmark during 1973–2016. Clin Epidemiol. 2020;12:287. doi:10.2147/CLEP.S229056.
    1. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. The American Journal of Clinical Nutrition. 2008;87(3):534–538. doi:10.1093/ajcn/87.3.534.
    1. Akay HK, Tokman HB, Hatipoglu N, Hatipoglu H, Siraneci R, Demirci M, Borsa BA, Yuksel P, Karakullukcu A, Kangaba AA. The relationship between bifidobacteria and allergic asthma and/or allergic dermatitis: a prospective study of 0–3 years-old children in Turkey. Anaerobe. 2014;28:98–103. doi:10.1016/j.anaerobe.2014.05.006.
    1. Enomoto T, Sowa M, Nishimori K, Shimazu S, Yoshida A, Yamada K, Furukawa F, Nakagawa T, Yanagisawa N, Iwabuchi N. Effects of bifidobacterial supplementation to pregnant women and infants in the prevention of allergy development in infants and on fecal microbiota. Allergol Int. 2014;63:575–585.
    1. Dogra S, Sakwinska O, Soh S, Ngom-Bru C, Brück WM, Berger B, Brüssow H, Lee YS, Yap F, Chong Y. Dynamics of infant gut microbiota are influenced by delivery mode and gestational duration and are associated with subsequent adiposity. mBio. 2015;6(1):e02419–14. doi:10.1128/mBio.02419-14.
    1. Low JSY, Soh SE, Lee YK, Kwek KYC, Holbrook JD, Van der Beek EM, Shek LP, Goh AEN, Teoh OH, Godfrey KM, et al. Ratio of Klebsiella/Bifidobacterium in early life correlates with later development of paediatric allergy. Benef Microbes. 2017;8(5):681–695. doi:10.3920/BM2017.0020.
    1. Baron R, Taye M, Besseling-van der Vaart I, Ujčič-Voortman J, Szajewska H, Seidell JC, Verhoeff A. The relationship of prenatal and infant antibiotic exposure with childhood overweight and obesity: a systematic review. J Dev Orig Health Dis. 2020;11(4):335–349. doi:10.1017/S2040174419000722.
    1. Koebnick C, Sidell MA, Getahun D, Tartof SY, Rozema E, Taylor B, Xiang AH, Spiller MW, Sharma AJ, Mukhopadhyay S, et al. Intrapartum antibiotic exposure and body mass index in children. Clin Infect Dis. 2021. 15;73(4):e938–46. doi:10.1093/cid/ciab053.
    1. Wohl DL, Curry WJ, Mauger D, Miller J, Tyrie K. Intrapartum antibiotics and childhood atopic dermatitis. The Journal of the American Board of Family Medicine. 2015;28(1):82–89. doi:10.3122/jabfm.2015.01.140017.
    1. Korpela K, Salonen A, Virta L, Kekkonen R, Forslund K, Bork P, de Vos W. Intestinal microbiome is associated with lifetime antibiotic use in Finnish pre-school children. Nat Commun. 2016;7(1):10410. doi:10.1038/ncomms10410.
    1. Tun HM, Bridgman SL, Chari R, Field CJ, Guttman DS, Becker AB, Mandhane PJ, Turvey SE, Subbarao P, Sears MR. 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.
    1. Mueller NT, Shin H, Pizoni A, Werlang IC, Matte U, Goldani MZ, Goldani HA, Dominguez-Bello MG. Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Sci Rep. 2016;6(1):1–9. doi:10.1038/srep23133.
    1. Korpela K, Blakstad EW, Moltu SJ, Strømmen K, Nakstad B, Rønnestad AE, Brække K, Iversen PO, Drevon CA, de Vos W. Intestinal microbiota development and gestational age in preterm neonates. Sci Rep. 2018;8(1):1–9. doi:10.1038/s41598-018-20827-x.
    1. Chang HY, Chen JH, Chang JH, Lin HC, Lin CY, Peng CC. Multiple strains probiotics appear to be the most effective probiotics in the prevention of necrotizing enterocolitis and mortality: an updated meta-analysis. PloS one. 2017;12(2):e0171579. doi:10.1371/journal.pone.0171579.
    1. Lucas A, Cole TJ. Breast milk and neonatal necrotising enterocolitis. The Lancet. 1990;336(8730–8731):1519–1523. doi:10.1016/0140-6736(90)93304-8.
    1. Liu Y, Qin S, Song Y, Feng Y, Lv N, Xue Y, Liu F, Wang S, Zhu B, Ma J. The perturbation of infant gut microbiota caused by cesarean delivery is partially restored by exclusive breastfeeding. Front Microbiol. 2019;10:598. doi:10.3389/fmicb.2019.00598.
    1. Kuitunen M, Kukkonen K, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Haahtela T, Savilahti E. Probiotics prevent ige-associated allergy until age 5 years in cesarean-delivered children but not in the total cohort. Journal of Allergy and Clinical Immunology. 2009;123(2):335–341. doi:10.1016/j.jaci.2008.11.019.
    1. Korpela K, Salonen A, Vepsäläinen O, Suomalainen M, Kolmeder C, Varjosalo M, Miettinen S, Kukkonen K, Savilahti E, Kuitunen M. Probiotic supplementation restores normal microbiota composition and function in antibiotic-treated and in caesarean-born infants. Microbiome. 2018;6(1):182. doi:10.1186/s40168-018-0567-4.
    1. Garcia Rodenas CL, Lepage M, Ngom-Bru C, Fotiou A, Papagaroufalis K, Berger B. Effect of formula containing lactobacillus reuteri DSM 17938 on fecal microbiota of infants born by cesarean-section. J Pediatr Gastroenterol Nutr. 2016;63(6):681–687. doi:10.1097/MPG.0000000000001198.
    1. Hurkala J, Lauterbach R, Radziszewska R, Strus M, Heczko P. Effect of a short-time probiotic supplementation on the abundance of the main constituents of the gut microbiota of term Newborns delivered by cesarean section—a randomized, prospective, controlled clinical trial. Nutrients. 2020;12(10):3128. doi:10.3390/nu12103128.
    1. Wilson BC, Ém B, Grigg CP, Derraik JG, 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. 1;69:103443. doi:10.1016/j.ebiom.2021.103443.
    1. Dominguez-Bello MG, De Jesus-Laboy KM, Shen N, Cox LM, Amir A, Gonzalez A, Bokulich NA, Song SJ, Hoashi M, Rivera-Vinas JI. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nature Medicine. 2016;22(3):250–253. doi:10.1038/nm.4039.
    1. Song SJ, Wang J, Martino C, Jiang L, Thompson WK, Shenhav L, McDonald D, Marotz C, Harris P, Hernandez CD, et al. Naturalization of the microbiota developmental trajectory of Cesarean-born neonates after vaginal seeding. Med. 2021;2(8):951–964.E5. doi:10.1016/j.medj.2021.05.003.
    1. Hermansson H, Kumar H, Collado MC, Salminen S, Isolauri E, Rautava S. Breast milk microbiota is shaped by mode of delivery and intrapartum antibiotic exposure. Front Nutr. 2019;6:4. doi:10.3389/fnut.2019.00004.
    1. Lithgow KV, Buchholz VC, Ku E, Konschuh S, D’Aubeterre A, Sycuro LK. Protease activities of vaginal porphyromonas species disrupt coagulation and extracellular matrix in the cervicovaginal niche. NPJ Biofilms and Microbiomes. 2022;8(1):1–5. doi:10.1038/s41522-022-00270-7.
    1. Jian C, Luukkonen P, Yki-Järvinen H, Salonen A, Korpela K. Quantitative PCR provides a simple and accessible method for quantitative microbiota profiling. PLoS One. 2020;15(1):e0227285. doi:10.1371/journal.pone.0227285.
    1. Jian C, Salonen A, Korpela K. Commentary: how to count our microbes? the effect of different quantitative microbiome profiling approaches. Frontiers in Cellular and Infection Microbiology. 2021;6:627910. doi:10.3389/fcimb.2021.627910.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner