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Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth

Author

Listed:
  • Yan Shao

    (Wellcome Sanger Institute)

  • Samuel C. Forster

    (Wellcome Sanger Institute
    Hudson Institute of Medical Research
    Monash University)

  • Evdokia Tsaliki

    (University College London)

  • Kevin Vervier

    (Wellcome Sanger Institute)

  • Angela Strang

    (University College London)

  • Nandi Simpson

    (University College London)

  • Nitin Kumar

    (Wellcome Sanger Institute)

  • Mark D. Stares

    (Wellcome Sanger Institute)

  • Alison Rodger

    (University College London)

  • Peter Brocklehurst

    (University of Birmingham)

  • Nigel Field

    (University College London)

  • Trevor D. Lawley

    (Wellcome Sanger Institute)

Abstract

Immediately after birth, newborn babies experience rapid colonization by microorganisms from their mothers and the surrounding environment1. Diseases in childhood and later in life are potentially mediated by the perturbation of the colonization of the infant gut microbiota2. However, the effects of delivery via caesarean section on the earliest stages of the acquisition and development of the gut microbiota, during the neonatal period (≤1 month), remain controversial3,4. Here we report the disrupted transmission of maternal Bacteroides strains, and high-level colonization by opportunistic pathogens associated with the hospital environment (including Enterococcus, Enterobacter and Klebsiella species), in babies delivered by caesarean section. These effects were also seen, to a lesser extent, in vaginally delivered babies whose mothers underwent antibiotic prophylaxis and in babies who were not breastfed during the neonatal period. We applied longitudinal sampling and whole-genome shotgun metagenomic analysis to 1,679 gut microbiota samples (taken at several time points during the neonatal period, and in infancy) from 596 full-term babies born in UK hospitals; for a subset of these babies, we collected additional matched samples from mothers (175 mothers paired with 178 babies). This analysis demonstrates that the mode of delivery is a significant factor that affects the composition of the gut microbiota throughout the neonatal period, and into infancy. Matched large-scale culturing and whole-genome sequencing of over 800 bacterial strains from these babies identified virulence factors and clinically relevant antimicrobial resistance in opportunistic pathogens that may predispose individuals to opportunistic infections. Our findings highlight the critical role of the local environment in establishing the gut microbiota in very early life, and identify colonization with antimicrobial-resistance-containing opportunistic pathogens as a previously underappreciated risk factor in hospital births.

Suggested Citation

  • Yan Shao & Samuel C. Forster & Evdokia Tsaliki & Kevin Vervier & Angela Strang & Nandi Simpson & Nitin Kumar & Mark D. Stares & Alison Rodger & Peter Brocklehurst & Nigel Field & Trevor D. Lawley, 2019. "Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth," Nature, Nature, vol. 574(7776), pages 117-121, October.
  • Handle: RePEc:nat:nature:v:574:y:2019:i:7776:d:10.1038_s41586-019-1560-1
    DOI: 10.1038/s41586-019-1560-1
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    Cited by:

    1. Shuqin Zeng & Alexandre Almeida & Shiping Li & Junjie Ying & Hua Wang & Yi Qu & R. Paul Ross & Catherine Stanton & Zhemin Zhou & Xiaoyu Niu & Dezhi Mu & Shaopu Wang, 2024. "A metagenomic catalog of the early-life human gut virome," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Bin Zhu & David J. Edwards & Katherine M. Spaine & Laahirie Edupuganti & Andrey Matveyev & Myrna G. Serrano & Gregory A. Buck, 2024. "The association of maternal factors with the neonatal microbiota and health," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Chiara Tarracchini & Giulia Alessandri & Federico Fontana & Sonia Mirjam Rizzo & Gabriele Andrea Lugli & Massimiliano Giovanni Bianchi & Leonardo Mancabelli & Giulia Longhi & Chiara Argentini & Laura , 2023. "Genetic strategies for sex-biased persistence of gut microbes across human life," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Shuqin Zeng & Dhrati Patangia & Alexandre Almeida & Zhemin Zhou & Dezhi Mu & R. Paul Ross & Catherine Stanton & Shaopu Wang, 2022. "A compendium of 32,277 metagenome-assembled genomes and over 80 million genes from the early-life human gut microbiome," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Justine Tanoey & Christina Baechle & Hermann Brenner & Andreas Deckert & Julia Fricke & Kathrin Günther & André Karch & Thomas Keil & Alexander Kluttig & Michael Leitzmann & Rafael Mikolajczyk & Nadia, 2022. "Birth Order, Caesarean Section, or Daycare Attendance in Relation to Child- and Adult-Onset Type 1 Diabetes: Results from the German National Cohort," IJERPH, MDPI, vol. 19(17), pages 1-14, August.
    6. Aneta Słabuszewska-Jóźwiak & Jacek Krzysztof Szymański & Michał Ciebiera & Beata Sarecka-Hujar & Grzegorz Jakiel, 2020. "Pediatrics Consequences of Caesarean Section—A Systematic Review and Meta-Analysis," IJERPH, MDPI, vol. 17(21), pages 1-17, October.
    7. Dena Ennis & Shimrit Shmorak & Evelyn Jantscher-Krenn & Moran Yassour, 2024. "Longitudinal quantification of Bifidobacterium longum subsp. infantis reveals late colonization in the infant gut independent of maternal milk HMO composition," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    8. Na Chen & Lilan Hao & Zhe Zhang & Chenglu Qin & Zhuye Jie & Hongxin Pan & Jiali Duan & Xincheng Huang & Yunhong Zhang & Hongqin Gao & Ruike Lu & Tianshu Sun & Hua Yang & Jinqiu Shi & Maolian Liang & J, 2024. "Insights into the assembly of the neovaginal microbiota in Mayer-Rokitansky-Küster-Hauser (MRKH) syndrome patients," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Brandon Hickman & Anne Salonen & Alise J. Ponsero & Roosa Jokela & Kaija-Leena Kolho & Willem M. Vos & Katri Korpela, 2024. "Gut microbiota wellbeing index predicts overall health in a cohort of 1000 infants," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Tommi Mäklin & Harry A. Thorpe & Anna K. Pöntinen & Rebecca A. Gladstone & Yan Shao & Maiju Pesonen & Alan McNally & Pål J. Johnsen & Ørjan Samuelsen & Trevor D. Lawley & Antti Honkela & Jukka Corande, 2022. "Strong pathogen competition in neonatal gut colonisation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    11. Kerstin Thriene & Karin B. Michels, 2023. "Human Gut Microbiota Plasticity throughout the Life Course," IJERPH, MDPI, vol. 20(2), pages 1-14, January.
    12. Conor Feehily & Ian J. O’Neill & Calum J. Walsh & Rebecca L. Moore & Sarah Louise Killeen & Aisling A. Geraghty & Elaine M. Lawton & David Byrne & Rocio Sanchez-Gallardo & Sai Ravi Chandra Nori & Ida , 2023. "Detailed mapping of Bifidobacterium strain transmission from mother to infant via a dual culture-based and metagenomic approach," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    13. Maria Nieto-Rosado & Kirsty Sands & Edward A. R. Portal & Kathryn M. Thomson & Maria J. Carvalho & Jordan Mathias & Rebecca Milton & Calie Dyer & Chinenye Akpulu & Ian Boostrom & Patrick Hogan & Habib, 2024. "Colonisation of hospital surfaces from low- and middle-income countries by extended spectrum β-lactamase- and carbapenemase-producing bacteria," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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