Maternal microbial transmission

fetus
Amidst all the hype about your microbiota (all the microbes living in and on you) and what it is beneficial for, have you ever taken the time to ponder when and where you acquired all those microbes to start with?

For a century or so, it has been generally assumed by the medical community, scientists and the public alike that human fetuses develop in a sterile environment and that babies acquire their first bacterial inoculum during and after birth. Human infants are certainly exposed to a copious amount of maternal vaginal and fecal microbes as they go through the birth canal, and more microbes are subsequently transferred to babies through breastfeeding and handling, but is that all? In an essay published in PLoS Biology, Funkhouser and Bordenstein question the paradigm of the human sterile womb by suggesting that microbes might also be transferred to fetuses before birth.

It is a fact that bacteria can find their way to the uterus: intrauterine infections can occur, and they have been found to correlate with preterm deliveries (especially for births occurring at less than 30 weeks of pregnancy). However since this presence of bacteria in the womb was associated with pathogenic consequences, it only served to further reinforce the hypothesis that the uterus was a sterile environment and that any microbial presence was a dangerous one. As a result, the presence of bacteria in healthy pregnancies in humans has never really been investigated, and considering the ethical and technical difficulties of doing so, it is understandable that the idea of human infants being born “sterile” is still widely accepted, despite the lack of evidence one way or the other.

In their essay, Funkhouser and Bordenstein question the sterile womb hypothesis by casting a wider look at the evidence available for maternal microbial transmission in different phyla of the animal kingdom. They suggest that microbial transmission from mother to offspring may be a universal phenomenon in animals, and that humans might not make exception.

If you want to know more about how microbes can be passed from mother to offspring in a wide range of animals, I highly recommend reading the original article (boxes 1, 2 and 3, open access). The authors give detailed examples of maternal transmission in different species, from marine and terrestrial invertebrates (sponges, clams, insects) to vertebrates. The mechanisms vary, from direct internal transmission of symbiotic bacteria to the egg/embryo (so, happening before birth) to external transmission via coating of eggs with microbes or provision of fecal pellets (consumed by the larvae after hatching).

An example I found particularly interesting as it brings us closer to understand what is happening in mammals, and thus in humans, is the experiment performed by Jimenez and colleagues: the researchers fed genetically-labeled bacteria to pregnant mice and later on looked for the presence of these bacteria in the meconium of pups delivered by sterile C-section (the meconium is an infant’s first postpartum bowel movement of ingested amniotic fluid). They found that the labeled bacteria were indeed present, which suggest that they had somehow been transferred from the maternal gut to the fetuses in utero.

The investigation of the origins of the human microbiota, how and when it is established, is only beginning. More studies are needed to reliably determine whether bacteria can indeed be transmitted from mother to fetus in utero. But if it is the case, then another question is how such a transfer may be accomplished: in the case of intrauterine infections associated with preterm births, there seems to be ascension of microbes from the vagina; however, in the case of healthy pregnancies, the question of how bacteria would reach the fetus remains open. Incidentally, the question also applies to microbes found in breast milk. Until recently, breast milk was thought to be sterile, but now that it turns out not to be so, it will be interesting to investigate further what microbes get there and how. Several types of microbes found in breast milk are also common on sebaceous skin tissue around the nipple, and the presence of Streptococcus bacteria in breast milk could be accounted for by retrograde flow from the baby’s oral cavity to the milk ducts during suckling. However, the presence of other types of bacteria in breast milk and their origin remain to be investigated.

Given the increasing evidence of the important role played by the microbiota in immune system maturation and gut development, understanding how an infant gets its first dose of bacteria and what species it comprises seems a topic worthy of attention. Studies have shown that the microbiota of infants delivered vaginally initially differs from that of infants born via C-section, and that children delivered by C-section have a higher risk of developing immune-related disorders later in life, such as asthma, celiac disease or type 1 diabetes. Such preliminary epidemiological findings should perhaps already encourage the medical community as well as the public to give some thought to the use of C-section for convenience reasons, a practice that has increased a lot, especially in the US. In any case, a better understanding of what kind of bacteria are passed on to an infant early on (regardless of whether it is transferred before or after birth) may one day provide a basis for supplementation that could benefit the babies in need of it. Of course, manipulating one’s microbiota is not without consequences, but after all, that’s what we inevitably do when we take antibiotics, so why not try to find a way to manipulate it to our advantage?

Reference
Mom Knows Best: The Universality of Maternal Microbial Transmission. Funkhouser LJ, Bordenstein SR (2013). PLoS Biol 11(8): e1001631. doi:10.1371/journal.pbio.1001631
(Open access)

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