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A critical assessment of the sterile womb and in utero colonization hypotheses: implications for research on the pioneer infant microbiome

机译：对无菌子宫和子宫内定植假说的批判性评估：对先锋微生物学研究的启示

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After more than a century of active research, the notion that the human fetal environment is sterile and that the neonate’s microbiome is acquired during and after birth was an accepted dogma. However, recent studies using molecular techniques suggest bacterial communities in the placenta, amniotic fluid, and meconium from healthy pregnancies. These findings have led many scientists to challenge the “sterile womb paradigm” and propose that microbiome acquisition instead begins in utero, an idea that would fundamentally change our understanding of gut microbiota acquisition and its role in human development. In this review, we provide a critical assessment of the evidence supporting these two opposing hypotheses, specifically as it relates to (i) anatomical, immunological, and physiological characteristics of the placenta and fetus; (ii) the research methods currently used to study microbial populations in the intrauterine environment; (iii) the fecal microbiome during the first days of life; and (iv) the generation of axenic animals and humans. Based on this analysis, we argue that the evidence in support of the “in utero colonization hypothesis” is extremely weak as it is founded almost entirely on studies that (i) used molecular approaches with an insufficient detection limit to study “low-biomass” microbial populations, (ii) lacked appropriate controls for contamination, and (iii) failed to provide evidence of bacterial viability. Most importantly, the ability to reliably derive axenic animals via cesarean sections strongly supports sterility of the fetal environment in mammals. We conclude that current scientific evidence does not support the existence of microbiomes within the healthy fetal milieu, which has implications for the development of clinical practices that prevent microbiome perturbations after birth and the establishment of future research priorities.
机译：经过一个多世纪的积极研究，人们认为胎儿的环境是不育的，并且新生儿的微生物组是在出生时和出生后获得的。但是，最近使用分子技术的研究表明，健康怀孕的胎盘，羊水和胎粪中的细菌群落。这些发现导致许多科学家挑战“无菌子宫范式”，并提出微生物组的获取开始于子宫，这一观念将从根本上改变我们对肠道微生物群及其在人类发展中的作用的理解。在这篇综述中，我们对支持这两个相反假设的证据进行了严格的评估，尤其是与（i）胎盘和胎儿的解剖学，免疫学和生理学特征有关； （ii）目前用于研究宫内环境中微生物种群的研究方法； （iii）生命初期的粪便微生物组； （iv）轴生动物和人类的产生。基于此分析，我们认为支持“子宫内定植假说”的证据非常薄弱，因为它几乎完全基于以下研究：（i）使用检测限不足的分子方法来研究“低生物量” （ii）缺乏适当的污染控制措施，并且（iii）无法提供细菌生存力的证据。最重要的是，通过剖宫产可靠地衍生出轴生动物的能力有力地支持了哺乳动物胎儿环境的无菌性。我们得出结论，当前的科学证据不支持在健康的胎儿环境中存在微生物组，这对防止出生后微生物组扰动的临床实践的发展和未来研究重点的建立具有影响。

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