Cited by 1,088Gut microbiota and healthInfant Nutrition and HealthMaternal and Perinatal Health Interventions

Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth

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Shao, Yan, Forster, Samuel C., Tsaliki, Evdokia, Vervier, Kevin, Strang, Angela, Simpson, Nandi, Kumar, Nitin, Stares, Mark D. +4 more·2019·Nature

Abstract

Immediately after birth, newborn babies experience rapid colonization by microorganisms from their mothers and the surrounding environment 1. Diseases in childhood and later in life are potentially mediated by the perturbation of the colonization of the infant gut microbiota 2. 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 controversial 3,4. 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.

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  • It is unlikely that infants acquire many of such species directly from food consumption since maternal transmission is the most probable route of acquisition.

    “Although it is unlikely that infants acquire many of such species directly from food consumption since maternal transmission is the most probable route of acquisition, 103-105”

    From Unexplored microbial diversity from 2,500 food metagenomes and links with the human microbiome. (2024) · cites this paper as [105]

    The Main section reports maternal transmission of several gut bacterial species to infants, particularly after vaginal birth. It does not compare maternal transmission with acquisition through food consumption or establish that food is an unlikely source of the species in question. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Cesarean delivery predicts a more unstable neonatal microbiome and a heightened risk of infections, immune disorders, obesity, and neuroendocrine disturbances.

    “Cesarean delivery also predicts a more unstable neonatal microbiome and a heightened risk of infections, immune disorders, obesity, and neuroendocrine disturbances.31–33”
  • Phylogenetic trees produced by StrainPhlAn 3 can be used to identify identical strains across samples, which can be exploited in strain transmission analyses.

    “Phylogenetic trees produced by StrainPhlan 3 can also be used to identify identical strains across samples, which can be exploited, for example, in strain transmission analyses (Ferretti et al., 2018; Shao et al., 2019).”
  • Infants delivered by cesarean section tend to be colonized by common skin bacteria and hospital-associated opportunistic pathogens, in contrast to the initial abundance of Lactobacillus spp. seen in vaginally delivered infants.

    “Infants delivered by cesarean section (CS) tend to be colonized by common skin (e.g., Staphylococcus, Streptococcus, or Propionibacteria) ( Tamburini et al., 2016) and opportunistic pathogens associated with the hospital environment (e.g., Enterococcus, Enterobacter, and Klebsiella species) (Shao et al., 2019), in contrast to the initial abundance of Lactobacillus spp. (sensu lato) seen in infants”

    From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Shao et al., 2019

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Research works printed but not linked: 1

  1. Simonsen, M., Mailund, T. & Pedersen, C. N. S. in Algorithms in Bioinformatics 5251, 113- 122 (Springer, Berlin, Heidelberg, 2008).

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Authors
Shao, Y., Forster, S. C., Tsaliki, E., Vervier, K., Strang, A., Simpson, N., Kumar, N., Stares, M. D., Rodger, A., Brocklehurst, P., Field, N., & Lawley, T. D.
Affiliations
  • Wellcome Sanger Institute (GB)
  • University College London (GB)
  • University of Birmingham (GB)
Corresponding author
  • Field, Nigel
  • Lawley, Trevor D.
Venue
Nature
Published
2019-09-18
Volume
574
Issue
7776
Pages
117-121
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2973821866
Cited by
1,088
References
72
Citations by year
2026: 154 · 2025: 148 · 2024: 161 · 2023: 155 · 2022: 153 · 2021: 194 · 2020: 113 · 2019: 8
FWCI
39.06
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
Funders
  • Wellcome Trust (WT 098051, WT101169MA)
  • State Government of Victoria
  • Medical Research Council
  • National Health and Medical Research Council (1159239, 1141564, 1091097)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
  • Health Sciences › Medicine › Obstetrics and Gynecology › Maternal and Perinatal Health Interventions
Keywords
cesarean section, infant gut microbiota, neonatal colonization, mode of delivery, opportunistic pathogens, Enterococcus, Enterobacter, Klebsiella, antimicrobial resistance, virulence factors, breastfeeding, hospital environment
MeSH terms
Gastrointestinal Microbiome, Cesarean Section, Female, Humans, Infant, Newborn, Infant, Newborn, Diseases, Opportunistic Infections, Pregnancy, Infectious Disease Transmission, Vertical

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