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Maternal Influences on Fetal Microbial Colonization and Immune Development

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Maternal Influences on Fetal Microbial Colonization and Immune Development nature publishing group Review Maternal influences on fetal microbial colonization and immune development Joann Romano-Keeler1 and Jörn-Hendrik Weitkamp1 While critical for normal development, the exact timing of with intact membranes, a strong inverse correlation exists establishment of the intestinal microbiome is unknown. For between intra-amniotic detection of bacteria via culture or example, although preterm labor and birth have been asso- polymerase chain reaction and gestational age at delivery. The ciated with bacterial colonization of the amniotic cavity and type and number of bacteria in the amniotic cavity likely are fetal membranes for many years, the prevailing dogma of a important for pregnancy outcomes since amniotic fluid con- sterile intrauterine environment during normal term pregnan- centrations of white blood cells and interleukin-6 were highest cies has been challenged more recently. While found to be a when bacteria were detected by both culture and polymerase key contributor of evolution in the animal kingdom, maternal chain reaction. transmission of commensal bacteria may also constitute a Historically, Ureaplasma species of the Firmicutes phylum critical process during healthy pregnancies in humans with yet were implicated as culprits of perinatal infection and severe unclear developmental importance. Metagenomic sequenc- neonatal morbidity and mortality (6). Ureaplasma has been ing has elucidated a rich placental microbiome in normal isolated from amniotic fluid as early as 16–20 wk gestation and term pregnancies likely providing important metabolic and its presence in the chorioamnion alone or in the company of immune contributions to the growing fetus. Conversely, an other microbes has been strongly associated with histologic altered microbial composition during pregnancy may produce chorioamnionitis and preterm birth (7,8). Though originally aberrant metabolites impairing fetal brain development and suspected to ascend from the genitourinary tract secondary to life-long neurological outcomes. Here we review the current maternal colonization, hematogenous transmission via placen- understanding of microbial colonization at the feto-maternal tal infection or at delivery through an infected birth canal are interface and explain how normal gut colonization drives a considered an additional source of fetal and perinatal exposure balanced neonatal mucosal immune system, while dysbio- (9). The exact role of Ureaplasma spp. in chorioamnionitis and sis contributes to aberrant immune function early in life and adverse pregnancy outcomes remains controversial since up to beyond. We discuss how maternal genetics, diet, medications, 60–80% of women are colonized and only a small percentage and probiotics inform the fetal microbiome in preparation for of pregnancies develop histologically proven chorioamnion- perinatal and postnatal bacterial colonization. itis (10,11). In addition, clinical studies in which women were treated for Ureaplasma before and after birth demonstrated no MICROBIAL COLONIZATION IN UTERO differences in neonatal outcomes (11). Compelling data has Although critically important for normal development of the recently emerged associating in utero Ureaplasma exposure intestinal mucosal immune system (1), the exact timing of bac- with increased rates of bronchopulmonary dysplasia, intraven- terial colonization of the intestinal flora is unknown. Microbial tricular hemorrhage, and necrotizing enterocolitis (12–14). invasion of the amniotic cavity has been well described in Causal relationships and exact timing of Ureaplasma exposure women with preterm rupture of membranes (2). In fact, in relation to the postnatal sequelae require further inves- intrauterine infection is considered the most common cause tigation. As may be the case for Ureaplasma exposure, some of spontaneous preterm birth (3). However bacteria can also degree of bacterial colonization in utero may underlie normal be cultured from chorioamniotic tissue using sterile proce- fetal development. Because not all microbes cause preterm dures during cesarean sections in cases of preterm labor with labor, only specific bacteria within fetal membranes, other intact membranes, indicating a possible transmission of bac- areas of the feto-maternal unit or even the fetal gastrointesti- teria from the maternal blood stream into the amniotic cavity nal tract may drive adverse pregnancy outcomes during criti- (3). Recently, the combination of bacterial culture techniques cal developmental windows (15). It remains elusive whether with culture independent molecular methods revealed that the “pathologic” bacterial colonization is always a primary factor amniotic cavity harbors a greater diversity of microbes than in premature birth. previously suspected (4), including uncultivated, previously It is possible that maternal immune factors play an impor- uncharacterized taxa (5). In this cohort of pregnant women tant role in bacterial invasion of the amniotic cavity and/or 1Department of Pediatrics, Vanderbilt University, Nashville, Tennessee. Correspondence: Jörn-Hendrik Weitkamp ([email protected]) Received 9 May 2014; accepted 22 August 2014; advance online publication 12 November 2014. doi:10.1038/pr.2014.163 Copyright © 2015 International Pediatric Research Foundation, Inc. Volume 77 | Number 1 | January 2015 Pediatric RESEarch 189 Review Romano-Keeler and Weitkamp promote an inflammatory cascade resulting in preterm labor of microbiota in meconium and a microbial community pres- (16). For example, prostaglandin E2 expression is a potent ent in amniotic fluid and rich in proinflammatory cytokines negative regulator of innate immunity in the human placenta (24). Specific phyla were more abundant at lower gestation, and has been shown to foster bacterial dissemination (17). however, the exact mechanism of these potentially immuno- Surprisingly, little is known about the innate immune capaci- reactive bacteria in triggering a fetal inflammatory response ties of intact fetal membranes, which serve as the final barrier syndrome followed by preterm birth remains to be studied. between the external environment and the incubating fetus. Recently, we detected an unprecedented microbial diversity Innate immune responses including antimicrobial peptide in intestinal tissue samples obtained directly from the operating expression, such as human beta defensins (hβds), were studied room during resection for anatomic gut anomalies shortly after ex vivo in human extraplacental membranes after inoculation birth and prior to initiation of feeds in infants delivered via cesar- with live Streptococcus agalactiae (GBS) (18). After GBS inocu- ean section (25). Diversity measures such as Simpson’s inverse lation, hβd expression increased concomitant with markedly index, Shannon-Wiener, and Chao 1 estimator were statistically diminished recovery of GBS from fetal membranes. This robust significantly higher in the small intestinal mucosa compared to innate immune response inhibited subsequent GBS coloniza- parallel collected fecal samples, suggesting a “top-to-bottom” tion of the placenta and fetus. Additional studies are necessary pattern of microbial colonization that likely occurred in utero. to further examine the role of the maternal immune response in fetal microbial colonization and outcomes of pregnancy. THE FETAL MICROBIOME AND IMMUNE DEVELOPMENT Despite an appreciation for in utero bacterial colonization Perhaps exposure to various microbial antigens in the human in the setting of preterm labor and preterm rupture of mem- fetus explains the relative early development of a functional branes, the amniotic environment has traditionally been immune system. For example, CD4+ and CD8+ T cells can considered sterile in normal term pregnancies. Though this already be identified toward the end of the first trimester in paradigm is conceptionally attractive, it’s long-held dogma is the human fetus (26). More recently, Michaëlsson et al. (27). nevertheless surprising considering that maternal microbial discovered that fetal T cells are highly responsive to stimula- transmission is a universal phenomenon in the animal king- tion and require control by an abundant and functional pool dom and recently has been thought to play a critical role in of FOXP3+ T regulatory (Treg) cells. Interestingly, fetal Treg evolutionary development (19,20). In addition to a potential cells appear to have been informed by substantial numbers of “signature” fetal microbiome, a vibrant placental microbiome maternal cells that crossed the placenta and induced antigen- has been uncovered with the application of whole metage- specific tolerance (28). nomic shotgun sequencing. In studies with human placental Maternal mononuclear blood cells carry whole bacteria or tissue, investigators revealed a vibrant placental microbiome their genetic material at higher frequency and diversity during harboring specific metabolic functions (21). The overlap pregnancy (29). As some of these bacterial signatures are repre- between the metabolic functions of the placenta and the devel- sented in infant feces, it is fascinating to speculate that in utero oping fetus are largely unknown. transfer of maternal microbial antigens during fetal develop- Multiple recent studies employing meconium as a proxy for ment enables a balanced immune response in the newborn to in utero bacterial communities suggest that bacterial trans- the rapidly developing microbiome postpartum. This is espe- mission from the
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