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Microbial colonization programs are structured by breastfeeding and guide healthy respiratory development

Affiliations
  • 1Institute for Systems Genetics, New York Grossman School of Medicine, New York University, New York, NY, USA; Department of Microbiology, New York Grossman School of Medicine, New York University, New York, NY, USA; Department of Computer Science, Courant Institute of Mathematical Sciences, New York University, New York, NY, USA. Electronic address: liat.shenhav@nyulangone.org.
  • 2Department of Pediatrics and Child Health, University of Manitoba, Winnipeg, MB, Canada; Manitoba Interdisciplinary Lactation Centre (MILC), Children’s Hospital Research Institute of Manitoba, Winnipeg, MB, Canada.
  • 3Department of Pediatrics, Hospital for Sick Children, University of Toronto, Toronto, ON, Canada.
  • 4Department of Pediatrics, BC Children’s Hospital, University of British Columbia, Vancouver, BC, Canada.
  • 5Department of Medicine, McMaster University, Hamilton, ON, Canada.
  • 6Division of Infectious Disease, Department of Pediatrics, The Children’s Hospital of Philadelphia, Philadelphia, PA, USA; Institute for Immunology and Immune Health, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA; Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
  • 7Institute for Immunology and Immune Health, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA; Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.
  • 8Department of Pediatrics, University of California, San Diego, La Jolla, CA, USA; Larsson-Rosenquist Foundation Mother-Milk-Infant Center of Research Excellence (MOMI CORE), University of California, San Diego, La Jolla, CA, USA; Human Milk Institute (HMI), University of California, San Diego, La Jolla, CA, USA.
  • 9Department of Agriculture, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada.
  • 10Department of Department of Microbiology & Immunology, Dalhousie University, Halifax, NS, Canada.
  • 11Department of Pediatrics, University of Alberta, Edmonton, AB, Canada.
  • 12Department of Pediatrics, Hospital for Sick Children, University of Toronto, Toronto, ON, Canada; Department of Physiology, University of Toronto, Toronto, ON, Canada. Electronic address: padmaja.subbarao@sickkids.ca.
  • 13Department of Medicine, McMaster University, Hamilton, ON, Canada. Electronic address: surette@mcmaster.ca.

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September 20, 2024

Abstract

Breastfeeding and microbial colonization during infancy occur within a critical time window for development, and both are thought to influence the risk of respiratory illness. However, the mechanisms underlying the protective effects of breastfeeding and the regulation of microbial colonization are poorly understood. Here, we profiled the nasal and gut microbiomes, breastfeeding characteristics, and maternal milk composition of 2,227 children from the CHILD Cohort Study. We identified robust colonization patterns that, together with milk components, predict preschool asthma and mediate the protective effects of breastfeeding. We found that early cessation of breastfeeding (before 3 months) leads to the premature acquisition of microbial species and functions, including Ruminococcus gnavus and tryptophan biosynthesis, which were previously linked to immune modulation and asthma. Conversely, longer exclusive breastfeeding supports a paced microbial development, protecting against asthma. These findings underscore the importance of extended breastfeeding for respiratory health and highlight potential microbial targets for intervention.

Keywords:

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