Mother-to-infant microbiota transmission and infant microbiota development across multiple body sites

Bogaert, Debby; Beveren, Gina J. van; Koff, Emma M. de; Parga, Paula Lusarreta; Lopez, Carlos E. Balcazar; Koppensteiner, Lilian; Clerc, Melanie; Hasrat, Raiza; Arp, Kayleigh; Chu, Mei Ling J N; Groot, Pieter C. M. de; Sanders, Elisabeth A. M.; Houten, Marlies A. van; Piters, Wouter A A de Steenhuijsen

doi:10.1016/j.chom.2023.01.018

Cited by 88 publications

(61 citation statements)

References 56 publications

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“…For example, in 6-week cross-sectional analyzes stratified by delivery mode, the effect of the 6wBMT on the 6wIGMT was primarily observed in infants delivered by Cesarean section, although a similar pattern was also observed in vaginally delivered infants. Additionally, infants delivered by Cesarean section had greater proportions of microbial reads from ASVs that were present in the breast milk they consumed compared to infants who were delivered vaginally, which is in line with the recent finding that while infants delivered by Cesarean section have a reduced colonization by maternal stool microbiota, their colonization by breast milk microbiota is higher than vaginally delivered infants (Bogaert et al, 2023). Previous research indicates that the intestinal microbiome of infants delivered by Cesarean section persistently differs significantly from that of infants delivered vaginally, most profoundly in a depletion of Bacteroides (Dominguez-Bello et al, 2010;Azad et al, 2013;Jakobsson et al, 2014;Backhed et al, 2015;Madan et al, 2016) past the first week of life (Shao et al, 2019;Mitchell et al, 2020;Bogaert et al, 2023) as well as a decrease in microbial diversity (Jakobsson et al, 2014;Bokulich et al, 2016), which in theory could cause this group to be more susceptible to colonization by the pre-and probiotics derived from breast milk (Grönberg et al, 1992;Thurl et al, 2010;Jost et al, 2013).…”

Section: Discussionsupporting

confidence: 87%

“…These microbial communities are highly variable between individuals and are thought to be influenced by factors such as maternal body mass, delivery mode, pumping of breast milk, antibiotic exposure, and maternal diet ( Cabrera-Rubio et al, 2012 ; Khodayar-Pardo et al, 2014 ; Hermansson et al, 2019 ; Moossavi et al, 2019 ; Padilha et al, 2019 ; LeMay-Nedjelski et al, 2021 ), as well as by infant factors such as pacifier usage ( Sindi et al, 2023 ) and whether a baby has ever latched ( Kordy et al, 2020 ). Current evidence suggests that these bacteria along with those colonizing the skin around the mother’s nipple may be transferred to and may colonize the infant gut through breastfeeding ( Solis et al, 2010 ; Pannaraj et al, 2017 ; Biagi et al, 2018 ; Bogaert et al, 2023 ), including evidence from preterm infants showing associations between the overall microbial profile of human milk and both the infant gut and oral microbiomes ( Biagi et al, 2018 ). The vertical transfer of bacteria in breast milk to the infant gut appears to be facilitated by secretory immunoglobulin A coating of milk bacteria ( Qi et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

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Human milk-associated bacterial communities associate with the infant gut microbiome over the first year of life

et al. 2023

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IntroductionMicrobial communities inhabiting the human infant gut are important for immune system development and lifelong health. One critical exposure affecting the bacterial colonization of the infant gut is consumption of human milk, which contains diverse microbial communities and prebiotics. We hypothesized that human milk-associated microbial profiles are associated with those of the infant gut.MethodsMaternal–infant dyads enrolled in the New Hampshire Birth Cohort Study (n = 189 dyads) contributed breast milk and infant stool samples collected approximately at 6 weeks, 4 months, 6 months, 9 months, and 12 months postpartum (n = 572 samples). Microbial DNA was extracted from milk and stool and the V4-V5 region of the bacterial 16S rRNA gene was sequenced.ResultsClustering analysis identified three breast milk microbiome types (BMTs), characterized by differences in Streptococcus, Staphylococcus, Pseudomonas, Acinetobacter, and microbial diversity. Four 6-week infant gut microbiome types (6wIGMTs) were identified, differing in abundances of Bifidobacterium, Bacteroides, Clostridium, Streptococcus, and Escherichia/Shigella, while two 12-month IGMTs (12mIGMTs) differed primarily by Bacteroides presence. At 6 weeks, BMT was associated with 6wIGMT (Fisher’s exact test value of p = 0.039); this association was strongest among infants delivered by Cesarean section (Fisher’s exact test value of p = 0.0028). The strongest correlations between overall breast milk and infant stool microbial community structures were observed when comparing breast milk samples to infant stool samples collected at a subsequent time point, e.g., the 6-week breast milk microbiome associated with the 6-month infant gut microbiome (Mantel test Z-statistic = 0.53, value of p = 0.001). Streptoccous and Veillonella species abundance were correlated in 6-week milk and infant stool, and 4- and 6-month milk Pantoea species were associated with infant stool Lachnospiraceae genera at 9 and 12 months.DiscussionWe identified clusters of human milk and infant stool microbial communities that were associated in maternal–infant dyads at 6 weeks of life and found that milk microbial communities were more strongly associated with infant gut microbial communities in infants delivered operatively and after a lag period. These results suggest that milk microbial communities have a long-term effect on the infant gut microbiome both through sharing of microbes and other molecular mechanisms.

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Section: Discussionsupporting

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Human milk-associated bacterial communities associate with the infant gut microbiome over the first year of life

et al. 2023

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“…It has previously been shown that delivery mode is a major factor influencing early life skin bacterial colonization. [1][2][3] Furthermore, skin microbiome differences by delivery mode correlate with variations in later skin barrier function and possibly health outcomes. 2 Although reports vary, CS delivery has been associated with an increased risk of developing atopic dermatitis compared to VD in a recent large meta-analysis.…”

Section: E T T E R T O T H E J O U R N a Lmentioning

confidence: 99%

Vaginal delivery provides skin colonization resistance from environmental microbes in the NICU

Chaudhary,

O'Laughlin,

Kumar

et al. 2023

Clinical & Translational Med

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“…Two competing theories describe initial gut microbiota colonization in humans; either colonization occurs in utero 1 or alternatively following placental barrier breach during labor or Csection 1 . Recent work shows the importance of breastmilk, skin and feces bacteria transferred by the mothers to the infant when seeding the neonate 3 . However, a large amount of the early colonizers are not found in any of the mother body sites indicating alternative sources of bacteria 3,4 .…”

Section: Introductionmentioning

confidence: 99%

“…Recent work shows the importance of breastmilk, skin and feces bacteria transferred by the mothers to the infant when seeding the neonate 3 . However, a large amount of the early colonizers are not found in any of the mother body sites indicating alternative sources of bacteria 3,4 . Nevertheless, birth route [5][6][7] and breastfeeding 8,9 are implicated in early-life microbiota colonization and have been associated with later clinical outcomes 10 .…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota and maternal immune transfer at birth influence pre-allergic clinical outcome

Villette

Traore

Dhilly

et al. 2023

Preprint

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The gut microbiota of 2-3 month-old infants is associated with later allergic signs, while the microbiota at the time of allergic manifestation is not. We hypothesized that the infant gut microbiota and immune system are primed shortly after birth, and that this is influenced by maternal transfer of humoral immunity. We investigated the association between allergic outcomes and composition and humoral immunity to gut microbiota at birth, 2 months, and 2 years-of-age. Meconium gut microbiota clustered into three groups dominated by Escherichia, Enterococcus, and mixed genera. The Escherichia cluster was associated with protection against later allergic manifestations. We moreover studied the proportion and specificity of humoral immunity to gut microbiota. Humoral immunity to gut microbiota at birth was associated with future allergies. Future studies should evaluate if interventions to alter gut microbiota and humoral immunity in early-life protects against allergy.

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Mother-to-infant microbiota transmission and infant microbiota development across multiple body sites

Cited by 88 publications

References 56 publications

Human milk-associated bacterial communities associate with the infant gut microbiome over the first year of life

Human milk-associated bacterial communities associate with the infant gut microbiome over the first year of life

Vaginal delivery provides skin colonization resistance from environmental microbes in the NICU

Gut microbiota and maternal immune transfer at birth influence pre-allergic clinical outcome

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