Abstract
BackgroundEmerging evidence suggests that the in utero environment is not sterile as once presumed. Work in the mouse demonstrated transmission of commensal bacteria from mother to fetus during gestation, though it is unclear what modulates this process. We have previously shown in the nonhuman primate that, independent of obesity, a maternal high-fat diet during gestation and lactation persistently shapes the juvenile gut microbiome. We therefore sought to interrogate in a population-based human longitudinal cohort whether a maternal high-fat diet similarly alters the neonatal and infant gut microbiome in early life.MethodsA representative cohort was prospectively enrolled either in the early third trimester or intrapartum (n = 163), with a subset consented to longitudinal sampling through the postpartum interval (n = 81). Multiple body site samples, including stool and meconium, were collected from neonates at delivery and by 6 weeks of age. A rapid dietary questionnaire was administered to estimate intake of fat, added sugars, and fiber over the past month (National Health and Examination Survey). DNA was extracted from each infant meconium/stool sample (MoBio) and subjected to 16S rRNA gene sequencing and analysis.ResultsOn average, the maternal dietary intake of fat ranged from 14.0 to 55.2 %, with an average intake of 33.1 % (σ = 6.1 %). Mothers whose diets significantly differed from the mean (±1 standard deviation) were separated into two distinct groups, a control group (n = 13, μ = 24.4 %) and a high-fat group (n = 13, μ = 43.1 %). Principal coordinate analysis revealed that the microbiome of the neonatal stool at birth (meconium) clustered differently by virtue of maternal gestational diet (PERMANOVA p = 0.001). LEfSe feature selection identified several taxa that discriminated the groups, with a notable relative depletion of Bacteroides in the neonates exposed to a maternal high-fat gestational diet (Student’s t-test, p < 0.05) that persisted to 6 weeks of age.ConclusionsSimilar to the primate, independent of maternal body mass index, a maternal high-fat diet is associated with distinct changes in the neonatal gut microbiome at birth which persist through 4–6 weeks of age. Our findings underscore the importance of counseling pregnant mothers on macronutrient consumption during pregnancy and lactation.Electronic supplementary materialThe online version of this article (doi:10.1186/s13073-016-0330-z) contains supplementary material, which is available to authorized users.
Highlights
Emerging evidence suggests that the in utero environment is not sterile as once presumed
We recently demonstrated in a nonhuman primate model that, independent of obesity, a maternal high-fat diet throughout gestation and lactation altered the composition of the offspring microbiome, which persisted up to one year of age regardless of the infant’s post-weaning diet [17]
Study cohort and demographics To interrogate the impact of maternal gestational diet on the neonatal gut microbiome, we examined stool samples collected from neonates enrolled in a larger, prospective, population-based study that sought to characterize the early neonatal microbiome across multiple body sites
Summary
Emerging evidence suggests that the in utero environment is not sterile as once presumed. We have previously shown in the nonhuman primate that, independent of obesity, a maternal high-fat diet during gestation and lactation persistently shapes the juvenile gut microbiome. We sought to interrogate in a population-based human longitudinal cohort whether a maternal high-fat diet alters the neonatal and infant gut microbiome in early life. In a murine model, orally administered bacteria have been cultured from the meconium of pups delivered by sterile cesarean, indicating that mother to fetus transmission of bacteria may occur during gestation [15]. These findings suggest that colonization of the infant gut is likely to occur prior to parturition. Additional studies in well-controlled animal models are required to further characterize the mechanism of transmission
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