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Maternal and Breast Milk Influences on the Infant Gut Microbiome, Enteric Health and Growth Outcomes of Rhesus Monkeys

Rendina, Danielle N.*; Lubach, Gabriele R.*; Phillips, Gregory J.; Lyte, Mark; Coe, Christopher L.*

Journal of Pediatric Gastroenterology and Nutrition: May 9, 2019 - Volume Publish Ahead of Print - Issue - p
doi: 10.1097/MPG.0000000000002394
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Objectives: Gut bacteria play an essential role during infancy and are strongly influenced by the mode of birth and feeding. A primate model was used to investigate the benefits of exposure to the mother or conversely the negative impact of early nursery rearing on microbial colonization.

Method: Rectal swabs were obtained from rhesus macaques born vaginally and mother-reared (MR, N = 35) or delivered primarily via cesarean-section and human-reared (HR, N = 19). Microbiome composition was determined by rRNA gene amplicon sequencing at 2, 4 and 8 weeks of age and KEGG orthologs used to assess influences on functional metabolic pathways in the gut. Growth trajectories and incidence of diarrheic symptoms were evaluated.

Results: The microbial community structure was different between MR and HR infants with respect to phylogeny and abundance at all 3 ages. When examining dominant phyla, HR infants had a higher Firmicutes-to-Bacteroidetes ratio. At the genus level, breast milk-dependent commensal taxa and adult-typical genera were more abundant in MR infants. This difference resulted in a corresponding shift in the predicted metabolic effects, specifically for microbial genes associated with metabolism and immune function. HR infants had faster growth trajectories (p < 0.001), but more diarrheic symptoms by 6 months postnatal (p = 0.008).

Conclusions: MR infants acquired adult-typical microbiota more quickly, and had higher levels of several beneficial commensal taxa. Cesarean-delivered and formula-fed infants had different developmental trajectories of bacterial colonization. Establishment of the gut microbiome was associated with an infant's growth trajectory, and implicated in the subsequent vulnerability to Campylobacter infections associated with diarrhea in infant monkeys.

*Harlow Center, University of Wisconsin, Madison, WI

College of Veterinary Medicine, Iowa State University, Ames IA.

Address correspondence and reprint requests to Danielle N. Rendina, MS, Harlow Center for Biological Psychology, University of Wisconsin, 22N Charter Street, Madison, WI 53715 (e-mail: rendina@wisc.edu).

Received 27 September, 2018

Accepted 30 April, 2019

Conflicts of Interest: The authors have no conflicts of interest to declare.

Source of Funding: This research was supported by a grant from the National Institute of Mental Health investigating the significance of the gut microbiome for gut health and the gut-brain axis during infancy (MH104198).

AUTHOR CONTRIBUTIONS: Danielle N. Rendina: contributed in the collection of specimens, the microbiome and KEGG predictions, was responsible for interpretation of data, the literature review and drafted the initial version of the manuscript.

Christopher L. Coe: is the Principal Investigator for the NIH grant award that covered the costs of the research, is the director of a primate facility that generated infant monkeys for this research, help to conceptualize the study questions and hypotheses and contributed to the drafting and review of the manuscript.

Gabriele R. Lubach: was critical in breeding the monkeys, evaluating the infants, collecting the specimens, and provided feedback on the initial manuscript.

Gregory J. Phillips: is a co-PI on the NIH grant award that supported this research, and oversees the laboratory that extracted the bacterial rRNA for sequencing.

Mark Lyte: is a co-PI on the NIH grant that supported this research, helped to conceptualize the focus of the microbiology of young infant, and co-leads the laboratory that processed the fecal specimens to extract the bacterial rRNA for sequencing. His microbiology expertise was of value for identifying Campylobacter jejuni as the enteric pathogen of primary concern for the young monkey.

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© 2019 by European Society for Pediatric Gastroenterology, Hepatology, and Nutrition and North American Society for Pediatric Gastroenterology,