Composition and Variation of the Human Milk Microbiota Are Influenced by Maternal and Early-Life Factors

Shirin Moossavi; Shadi Sepehri; Bianca Robertson; Lars Bode; Sue Goruk; Catherine J Field; Lisa M Lix; Russell J de Souza; Allan B Becker; Piushkumar J Mandhane; Stuart E Turvey; Padmaja Subbarao; Theo J Moraes; Diana L Lefebvre; Malcolm R Sears; Ehsan Khafipour; Meghan B Azad

doi:10.1016/j.chom.2019.01.011

Composition and Variation of the Human Milk Microbiota Are Influenced by Maternal and Early-Life Factors

Cell Host Microbe. 2019 Feb 13;25(2):324-335.e4. doi: 10.1016/j.chom.2019.01.011.

Authors

Shirin Moossavi¹, Shadi Sepehri², Bianca Robertson³, Lars Bode⁴, Sue Goruk⁵, Catherine J Field⁵, Lisa M Lix⁶, Russell J de Souza⁷, Allan B Becker⁸, Piushkumar J Mandhane⁹, Stuart E Turvey¹⁰, Padmaja Subbarao¹¹, Theo J Moraes¹², Diana L Lefebvre¹³, Malcolm R Sears¹³, Ehsan Khafipour¹⁴, Meghan B Azad¹⁵

Affiliations

¹ Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada; Children's Hospital Research Institute of Manitoba, Pediatrics and Child Health, Winnipeg, MB, Canada; Developmental Origins of Chronic Diseases in Children Network (DEVOTION), Winnipeg, MB, Canada; Digestive Oncology Research Center, Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran.
² Children's Hospital Research Institute of Manitoba, Pediatrics and Child Health, Winnipeg, MB, Canada.
³ Pediatrics, University of California, San Diego, La Jolla, CA, USA.
⁴ Pediatrics, University of California, San Diego, La Jolla, CA, USA; Larsson-Rosenquist Foundation Mother-Milk-Infant Center of Research Excellence, University of California, San Diego, La Jolla, CA, USA.
⁵ Agricultural Food, and Nutritional Science, University of Alberta, Edmonton, AB, Canada.
⁶ Community Health Sciences, University of Manitoba, Winnipeg, MB, Canada.
⁷ Clinical Epidemiology and Biostatistics, McMaster University, Hamilton, ON, Canada; Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, ON, Canada.
⁸ Children's Hospital Research Institute of Manitoba, Pediatrics and Child Health, Winnipeg, MB, Canada; Developmental Origins of Chronic Diseases in Children Network (DEVOTION), Winnipeg, MB, Canada.
⁹ Pediatrics, University of Alberta, Edmonton, AB, Canada.
¹⁰ Pediatrics, University of British Columbia, Vancouver, BC, Canada.
¹¹ Division of Respiratory Medicine, Pediatrics, Hospital for Sick Children, University of Toronto, Toronto, ON, Canada; Physiology, University of Toronto, Toronto, ON, Canada.
¹² Division of Respiratory Medicine, Pediatrics, Hospital for Sick Children, University of Toronto, Toronto, ON, Canada.
¹³ Medicine, McMaster University, Hamilton, ON, Canada.
¹⁴ Children's Hospital Research Institute of Manitoba, Pediatrics and Child Health, Winnipeg, MB, Canada; Animal Science, University of Manitoba, Winnipeg, MB, Canada.
¹⁵ Children's Hospital Research Institute of Manitoba, Pediatrics and Child Health, Winnipeg, MB, Canada; Developmental Origins of Chronic Diseases in Children Network (DEVOTION), Winnipeg, MB, Canada. Electronic address: meghan.azad@umanitoba.ca.

PMID: 30763539
DOI: 10.1016/j.chom.2019.01.011

Abstract

Breastmilk contains a complex community of bacteria that may help seed the infant gut microbiota. The composition and determinants of milk microbiota are poorly understood. Among 393 mother-infant dyads from the CHILD cohort, we found that milk microbiota at 3-4 months postpartum was dominated by inversely correlated Proteobacteria and Firmicutes, and exhibited discrete compositional patterns. Milk microbiota composition and diversity were associated with maternal factors (BMI, parity, and mode of delivery), breastfeeding practices, and other milk components in a sex-specific manner. Causal modeling identified mode of breastfeeding as a key determinant of milk microbiota composition. Specifically, providing pumped breastmilk was consistently associated with multiple microbiota parameters including enrichment of potential pathogens and depletion of bifidobacteria. Further, these data support the retrograde inoculation hypothesis, whereby the infant oral cavity impacts the milk microbiota. Collectively, these results identify features and determinants of human milk microbiota composition, with potential implications for infant health and development.

Keywords: CHILD Study; breastfeeding; breastmilk; human milk; infant; microbiome; microbiota; mode of breastfeeding; nutrition.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Bifidobacterium / genetics
Breast Feeding*
Cohort Studies
DNA, Bacterial / genetics*
Female
Firmicutes / genetics
Humans
Infant
Longitudinal Studies
Male
Maternal Age*
Maternal Health*
Milk, Human / microbiology*
Proteobacteria / genetics
Sex Factors

Substances

DNA, Bacterial