Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection

Abstract

Microbial infection of the intrauterine environment is a major cause of preterm birth. The current paradigm indicates that intrauterine infections predominantly originate from the vaginal tract, with the organisms ascending into the sterile uterus. With the improvements in technology, an increasing number of bacterial species have been identified in intrauterine infections that do not belong to the vaginal microflora. We have demonstrated previously that intrauterine infections can originate from the oral cavity following hematogenous transmission. In this study, we begin to systemically examine what proportion of the oral microbiome can translocate to the placenta. Pooled saliva and pooled subgingival plaque samples were injected into pregnant mice through tail veins to mimic bacteremia, which occurs frequently during periodontal infections. The microbial species colonizing the murine placenta were detected using 16S rRNA gene-based PCR and clone analysis. A diverse group of bacterial species were identified, many of which have been associated with adverse pregnancy outcomes in humans although their sources of infection were not determined. Interestingly, the majority of these species were oral commensal organisms. This may be due to a dose effect but may also indicate a unique role of commensal species in intrauterine infection. In addition, a number of species were selectively "enriched" during the translocation, with a higher prevalence in the placenta than in the pooled saliva or subgingival plaque samples. These observations indicate that the placental translocation was species specific. This study provides the first insight into the diversity of oral bacteria associated with intrauterine infection.

FIG. 1.

Transmission of salivary bacteria to murine placentas. The relative abundance of each bacterial genus/species in pooled saliva samples (solid bars) and placentas from all seven infected mice (striped bars) were expressed as the percentage of the species out of the total number of clones analyzed for the pooled saliva samples (n = 41) and the murine placentas (n = 56), respectively.

FIG. 2.

Transmission of bacteria from pooled subgingival plaque to murine placentas. The relative abundance of each bacterial genus/species in pooled subgingival plaque samples (solid bars) and placentas from all 10 infected mice (slashed bars) were expressed as the percentage of the species out of the total number of clones analyzed for the pooled subgingival plaque samples (n = 81) and the murine placentas (n = 104), respectively.