Mother's milk microbiota is associated with the developing gut microbial consortia in very-low-birth-weight infants

Sara Shama; Michelle R Asbury; Alex Kiss; Nicole Bando; James Butcher; Elena M Comelli; Julia K Copeland; Adrianna Greco; Akash Kothari; Philip M Sherman; Alain Stintzi; Amel Taibi; Christopher Tomlinson; Sharon Unger; Pauline W Wang; OptiMoM Feeding Group; Deborah L O'Connor

doi:10.1016/j.xcrm.2024.101729

Mother's milk microbiota is associated with the developing gut microbial consortia in very-low-birth-weight infants

Cell Rep Med. 2024 Sep 17;5(9):101729. doi: 10.1016/j.xcrm.2024.101729. Epub 2024 Sep 6.

Authors

Sara Shama¹, Michelle R Asbury², Alex Kiss³, Nicole Bando¹, James Butcher⁴, Elena M Comelli⁵, Julia K Copeland⁶, Adrianna Greco¹, Akash Kothari¹, Philip M Sherman⁷, Alain Stintzi⁴, Amel Taibi⁸, Christopher Tomlinson⁹, Sharon Unger¹⁰, Pauline W Wang⁶; OptiMoM Feeding Group; Deborah L O'Connor¹¹

Affiliations

¹ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Translational Medicine Program, SickKids Research Institute, The Hospital for Sick Children, Toronto, ON, Canada.
² Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Departments of Physiology & Pharmacology, and Pediatrics, University of Calgary, Calgary, AB, Canada.
³ Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, ON, Canada; Evaluative and Clinical Sciences, Sunnybrook Research Institute, Toronto, ON, Canada.
⁴ Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Ottawa, ON, Canada; Ottawa Institute of Systems Biology, Ottawa, ON, Canada.
⁵ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Joannah and Brian Lawson Centre for Child Nutrition, University of Toronto, Toronto, ON, Canada.
⁶ Centre for the Analysis of Genome Evolution and Function, University of Toronto, Toronto, ON, Canada.
⁷ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Cell Biology Program, SickKids Research Institute, The Hospital for Sick Children, Toronto, ON, Canada; Gastroenterology, Hepatology, and Nutrition, The Hospital for Sick Children, Toronto, ON, Canada; Department of Paediatrics, University of Toronto, Toronto, ON, Canada.
⁸ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada.
⁹ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Translational Medicine Program, SickKids Research Institute, The Hospital for Sick Children, Toronto, ON, Canada; Joannah and Brian Lawson Centre for Child Nutrition, University of Toronto, Toronto, ON, Canada; Department of Paediatrics, University of Toronto, Toronto, ON, Canada; Division of Neonatology, The Hospital for Sick Children, Toronto, ON, Canada.
¹⁰ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Department of Paediatrics, University of Toronto, Toronto, ON, Canada; Division of Neonatology, Izaak Walton Killam Hospital, Halifax, NS, Canada; Department of Pediatrics, Sinai Health, Toronto, ON, Canada; Rogers Hixon Ontario Human Milk Bank, Toronto, ON, Canada.
¹¹ Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Translational Medicine Program, SickKids Research Institute, The Hospital for Sick Children, Toronto, ON, Canada; Joannah and Brian Lawson Centre for Child Nutrition, University of Toronto, Toronto, ON, Canada; Department of Pediatrics, Sinai Health, Toronto, ON, Canada; Rogers Hixon Ontario Human Milk Bank, Toronto, ON, Canada. Electronic address: [email protected].

Abstract

Mother's milk contains diverse bacterial communities, although their impact on microbial colonization in very-low-birth-weight (VLBW, <1,500 g) infants remains unknown. Here, we examine relationships between the microbiota in preterm mother's milk and the VLBW infant gut across initial hospitalization (n = 94 mother-infant dyads, 422 milk-stool pairs). Shared zero-radius operational taxonomic units (zOTUs) between milk-stool pairs account for ∼30%-40% of zOTUs in the VLBW infant's gut. We show dose-response relationships between intakes of several genera from milk and their concentrations in the infant's gut. These relationships and those related to microbial sharing change temporally and are modified by in-hospital feeding practices (especially direct breastfeeding) and maternal-infant antibiotic use. Correlations also exist between milk and stool microbial consortia, suggesting that multiple milk microbes may influence overall gut communities together. These results highlight that the mother's milk microbiota may shape the gut colonization of VLBW infants by delivering specific bacteria and through intricate microbial interactions.

Keywords: antibiotics; direct breastfeeding; donor milk; human milk; microbiome; microbiota; mother’s milk; nutrient fortification; preterm infant; very-low-birth-weight infant.

MeSH terms

Adult
Bacteria / classification
Bacteria / genetics
Bacteria / isolation & purification
Breast Feeding
Feces* / microbiology
Female
Gastrointestinal Microbiome* / physiology
Humans
Infant, Newborn
Infant, Premature
Infant, Very Low Birth Weight*
Male
Microbial Consortia
Milk, Human* / microbiology
Mothers