Impact of Enterobius vermicularis infection and mebendazole treatment on intestinal microbiota and host immune response

Abstract

Background

Previous studies on the association of enterobiasis and chronic inflammatory diseases have revealed contradictory results. The interaction of Enterobius vermicularis infection in particular with gut microbiota and induced immune responses has never been thoroughly examined.

Methodology/Findings

In order to answer the question of whether exposure to pinworm and mebendazole can shift the intestinal microbial composition and immune responses, we recruited 109 (30 pinworm-negative, 79 pinworm-infected) first and fourth grade primary school children in Taichung, Taiwan, for a gut microbiome study and an intestinal cytokine and SIgA analysis. In the pinworm-infected individuals, fecal samples were collected again at 2 weeks after administration of 100 mg mebendazole. Gut microbiota diversity increased after Enterobius infection, and it peaked after administration of mebendazole. At the phylum level, pinworm infection and mebendazole deworming were associated with a decreased relative abundance of Fusobacteria and an increased proportion of Actinobacteria. At the genus level, the relative abundance of the probiotic Bifidobacterium increased after enterobiasis and mebendazole treatment. The intestinal SIgA level was found to be lower in the pinworm-infected group, and was elevated in half of the mebendazole-treated group. A higher proportion of pre-treatment Salmonella spp. was associated with a non-increase in SIgA after mebendazole deworming treatment.

Conclusions/Significance

Childhood exposure to pinworm plus mebendazole is associated with increased bacterial diversity, an increased abundance of Actinobacteria including the probiotic Bifidobacterium, and a decreased proportion of Fusobacteria. The gut SIgA level was lower in the pinworm-infected group, and was increased in half of the individuals after mebendazole deworming treatment.

Author summary

Whether human pinworm infection plus mebendazole deworming treatment can shift intestinal microbiota to a composition that is beneficial to the host and influence their mucosal immune response is currently unclear. In a cohort of 109 primary school children, we discovered that Enterobius vermicularis infection is associated with increased intestinal microbial diversity, a lowered relative abundance of Fusobacteria and an enriched proportion of Actinobacteria, including the probiotic Bifidobacterium. Mebendazole deworming was found to be correlated with a further increase in bacterial diversity. However, lower gut SIgA levels were detected in the pinworm infected group, and they were increased in only half of the subjects after mebendazole treatment.