A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome
Abstract 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,...
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| Format: | Article |
| Language: | English |
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BMC
2017-04-01
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| Series: | Microbiome |
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| Online Access: | http://link.springer.com/article/10.1186/s40168-017-0268-4 |
| _version_ | 1818379849693134848 |
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| author | Maria Elisa Perez-Muñoz Marie-Claire Arrieta Amanda E. Ramer-Tait Jens Walter |
| author_facet | Maria Elisa Perez-Muñoz Marie-Claire Arrieta Amanda E. Ramer-Tait Jens Walter |
| author_sort | Maria Elisa Perez-Muñoz |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-14T02:09:20Z |
| format | Article |
| id | doaj.art-826b896c0ce140819a44bd1b7701e150 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-14T02:09:20Z |
| publishDate | 2017-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-826b896c0ce140819a44bd1b7701e1502022-12-21T23:20:48ZengBMCMicrobiome2049-26182017-04-015111910.1186/s40168-017-0268-4A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiomeMaria Elisa Perez-Muñoz0Marie-Claire Arrieta1Amanda E. Ramer-Tait2Jens Walter3Department of Agriculture, Food and Nutritional Sciences, 4-126 Li Ka Shing Centre for Health Research Innovation, University of AlbertaDepartment of Physiology and Pharmacology, University of Calgary, Cumming School of MedicineDepartment of Food Science and Technology, 260 Food Innovation Center, University of Nebraska-LincolnDepartment of Agriculture, Food and Nutritional Sciences, 4-126 Li Ka Shing Centre for Health Research Innovation, University of AlbertaAbstract 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.http://link.springer.com/article/10.1186/s40168-017-0268-4Sterile wombIn utero colonizationMicrobiomePlacentaContaminationAxenic animals |
| spellingShingle | Maria Elisa Perez-Muñoz Marie-Claire Arrieta Amanda E. Ramer-Tait Jens Walter A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome Microbiome Sterile womb In utero colonization Microbiome Placenta Contamination Axenic animals |
| title | A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome |
| title_full | A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome |
| title_fullStr | A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome |
| title_full_unstemmed | A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome |
| title_short | A critical assessment of the “sterile womb” and “in utero colonization” hypotheses: implications for research on the pioneer infant microbiome |
| title_sort | critical assessment of the sterile womb and in utero colonization hypotheses implications for research on the pioneer infant microbiome |
| topic | Sterile womb In utero colonization Microbiome Placenta Contamination Axenic animals |
| url | http://link.springer.com/article/10.1186/s40168-017-0268-4 |
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