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Maternal Health and the Placental Microbiome Placenta xxx (2016) 1e8 Contents lists available at ScienceDirect Placenta journal homepage: www.elsevier.com/locate/placenta Review Maternal health and the placental microbiome * Elise Pelzer a, , Luisa F. Gomez-Arango b, c, Helen L. Barrett b, c, d, Marloes Dekker Nitert b, e a School of Biomedical Sciences, Queensland University of Technology, Brisbane, Australia b UQ Centre for Clinical Research, The University of Queensland, Brisbane, Australia c School of Medicine, The University of Queensland, Brisbane, Australia d Obstetric Medicine, Royal Brisbane and Women's Hospital, Brisbane, Australia e School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Australia article info abstract Article history: Over the past decade, the role of the microbiome in regulating metabolism, immune function and Received 19 October 2016 behavior in humans has become apparent. It has become clear that the placenta is not a sterile organ, but Received in revised form rather has its own endogenous microbiome. The composition of the placental microbiome is distinct 28 November 2016 from that of the vagina and has been reported to resemble the oral microbiome. Compared to the gut Accepted 2 December 2016 microbiome, the placental microbiome exhibits limited microbial diversity. This review will focus on the current understanding of the placental microbiota in normal healthy pregnancy and also in disease states Keywords: including preterm birth, chorioamnionitis and maternal conditions such as obesity, gestational diabetes Placenta Microbiome mellitus and preeclampsia. Factors known to alter the composition of the placental microbiota will be fi Pregnancy discussed in the nal part of this review. Preterm delivery © 2016 Published by Elsevier Ltd. Probiotics Contents 1. The microbiome in pregnancy . ................................................ 00 2. The placental microbiota in healthy pregnancy . .................................... 00 2.1. The community composition of the placental microbiota in healthy term pregnancies . ...................... 00 2.2. Seeding of the placental microbiota: how do microorganisms and their products passage into the placenta? . ............ 00 3. Other pregnancy microbiomes . ................................................ 00 3.1. Roles for the placental microbiota . ....................... 00 4. The placental microbiota and adverse pregnancy outcomes . .................................... 00 4.1. The placental microbiota composition in pregnancies with adverse outcomes . ....................... 00 4.2. Where do placental microorganisms and microbial products in placental pathology arise? . ................. 00 4.3. How does the placental microbiota precipitate adverse pregnancy outcomes? . ....................... 00 5. Factors changing the placental microbiota . .................................... 00 5.1. Maternal obesity . ....................... 00 5.2. Gestational diabetes mellitus (GDM) . ....................... 00 5.3. Probiotics and antibiotics . ....................... 00 6. Conclusions . ................................................. 00 Conflict of interest . ................................................. 00 Acknowledgements . ....................... 00 References................................................................. ................................ ....................... 00 1. The microbiome in pregnancy Over the past decade, the role of the microbiome (i.e. the * Corresponding author. composite of microorganisms and its genomes on the body) in E-mail address: [email protected] (E. Pelzer). regulating metabolism, immune function and behavior in http://dx.doi.org/10.1016/j.placenta.2016.12.003 0143-4004/© 2016 Published by Elsevier Ltd. Please cite this article in press as: E. Pelzer, et al., Maternal health and the placental microbiome, Placenta (2016), http://dx.doi.org/10.1016/ j.placenta.2016.12.003 2 E. Pelzer et al. / Placenta xxx (2016) 1e8 humans has become apparent. The main focus of attention has studies report that cultivation-dependent studies likely signifi- been on the microbiota (i.e. the microorganisms present on a cantly underestimate the incidence of microbial presence within certain body site) of the gastrointestinal tract but microbiota are the placenta, which is likely due to the presence of bacteria that also present in the oral cavity, the skin, the lungs, the genito- are hard to culture due to their preference for anaerobic envi- urinary tract and in pregnancy also in the placenta and the am- ronments or requirement for specific unidentified nutrients niotic fluid. [15,16,18e20]. The composition of the microbiome is dependent on body site, More recent DNA-based studies provide evidence for the pres- host-dependent factors including genetic make-up [1], dietary ence of a low biomass endogenous microbial community within intake [2], disease state [3] as well geographic location [4] and the placenta [21]. The microbiota of placentae from healthy term bacterial species present [5]. For the gut microbiota, there is wide deliveries have a high abundance of Lactobacillus sp., Propioni- inter- and intra-individual diversity; however, a healthy gut bacterium spp. and members of the Enterobacteriaceae family microbiota in adults is mainly comprised of bacteria belonging to [13,22,23]. Lactobacilli sp. are less abundant in placental tissues of the phyla Firmicutes and Bacteroidetes. An imbalance in the preterm deliveries, possibly supporting a role for this genera in composition of the microbiota is known as dysbiosis. Dysbiosis of positive pregnancy outcomes [16]. the gut microbiota is associated with diverse disease states including inflammatory bowel disease, diabetes and asthma but 2.2. Seeding of the placental microbiota: how do microorganisms also with obesity. and their products passage into the placenta? In pregnancy, the gut microbiota is altered with the progression of the pregnancy [6]. In the first trimester of pregnancy, the gut It is still not entirely clear how microorganisms enter the microbiota resembles that of outside pregnancy. At the start of the placental fetal compartment. The current hypotheses is that second trimester, abundance of specific bacterial genera have been microorganisms ascend from the vagina, maternal dendritic associated with physiological parameters in the mother: abun- cells sample bacteria from the intestinal lumen which are dance of Collinsella is positively correlated with insulin levels [7] internalized and transported to the placenta or enter via the whereas abundance of Odoribacter is negatively correlated with blood supply to seed the microbiota of the placenta (Fig. 1) blood pressure [8]. In the third trimester of pregnancy, the intra- [24]. The evidence for vaginally-derived bacteria is strong and individual diversity decreases with a higher abundance of bacte- Lactobacillus-dominant microbiota, resembling the Lactobacilli ria belonging to the pro-inflammatory Proteobacteria phylum [6]. sp. present in the vagina, are positively correlated with gesta- However, the inter-individual diversity increases in the third tional age [21,25e27]. Bacterial translocation via dissemination trimester due to the loss of different species in different women. through the blood supply is enhanced during pregnancy and When gut microbiota samples from women in the third trimester lactation. Gaps in the epithelium in for example the intestinal were transfected into a murine model, the mice became insulin and the oral mucosa enable the transfer of low numbers of resistant and gained weight, resembling the changes seen in bacteria into the circulation that can then seed the placenta pregnant women across gestation [6]. These results suggest that in [28]. The oral microbiota has recently been implicated as a pregnancy, the gut microbiota significantly contribute to the primary source of placental bacteria; however, data compari- metabolic changes observed in the mother. sons were performed against oral microbiota data from an Until recently, the intra-uterine environment was considered unrelated, non-pregnant population [21]. Animal studies have sterile except in the case of pathological infections usually associ- also demonstrated transmission of oral bacteria to the placenta ated with adverse pregnancy outcomes including preterm birth. [29,30], providing additional support for the seeding of the However, it is now clear that the placenta has its own microbiota placenta microbiome from the oral cavity. and that this is not necessarily associated with infections. This re- view will focus on the current understanding of the placental microbiota in normal pregnancy and also in disease states including 3. Other pregnancy microbiomes preterm birth, chorioamnionitis and maternal conditions such as obesity, gestational diabetes mellitus and preeclampsia. Factors Characterization of the vaginal microbiota using cultivation- known to alter the composition of the placental microbiota will be independent techniques demonstrates significant individual vari- discussed in the final part of this review. ability [31]. Notably, the vaginal microbiota appears to become more stable as gestation progresses, with less intra-individual 2. The placental microbiota in healthy pregnancy variability [13,32,33]. Further, the vaginal microbiota demon- strates enrichment of members of the orders Lactobacilliales, Clos- 2.1. The community composition of the placental microbiota in tridiales, Bacteroidales and Actinomycetales [34]. This further healthy
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