State Key Laboratory of Animal Disease Control and Prevention, College of Veterinary Medicine, Lanzhou University, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Lanzhou, Gansu 730000, China.
Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Lanzhou, Gansu 730046, China.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae213.
Human taeniasis, caused by Taenia tapeworms, is a global parasitic disease with significant implications for public health and food safety. These tapeworms can grow to considerable sizes and potentially impact the microecology of the host gut. Despite their importance, the effects of Taenia infection on host gut microbiota haven't been thoroughly investigated. In this study, we conducted a cross-sectional analysis of the gut microbiome in patients infected with Taenia asiatica (n = 87) compared to healthy controls (n = 79) in the Dali cohort, China. We also performed a longitudinal assessment of microbial changes following deworming in a subset of patients (n = 24). Our findings reveal a significant shift in gut microbial composition, characterized by increased alpha-diversity and an enrichment of Prevotella-driven enterotypes in infected patients compared to healthy controls. The stability of these microbial features post-deworming varied widely among individuals and was lower in those with lower initial alpha diversity and Prevotella-enterotype before deworming. We observed a significant depletion of Bifidobacterium species in infected individuals, regardless of enterotypes, and these prebiotics did not recover post-deworming. Metabolic network analysis and in vitro experiments suggest that the reduction of Bifidobacterium was linked to metabolic competition for ecological niches or nutrients, particularly stachyose, from other microbes rather than the parasitism itself. Furthermore, our machine learning analysis demonstrated that taxa associated with Bifidobacterium in stachyose metabolism could robustly predict infection but could not predict deworming. This study highlights the substantial impact of taeniasis on the human gut microbiome and overall gut health.
人带绦虫病是由带绦虫引起的一种全球性寄生虫病,对公共卫生和食品安全有重大影响。这些绦虫可以长到相当大的尺寸,并可能影响宿主肠道的微生态。尽管它们很重要,但带绦虫感染对宿主肠道微生物群的影响尚未得到彻底研究。在这项研究中,我们对中国大理队列中感染亚洲带绦虫的患者(n=87)与健康对照者(n=79)的肠道微生物组进行了横断面分析。我们还对一组患者(n=24)进行了驱虫后微生物变化的纵向评估。我们的研究结果表明,感染患者的肠道微生物组成发生了显著变化,与健康对照者相比,α多样性增加,普雷沃氏菌驱动的肠型富集。驱虫后这些微生物特征的稳定性在个体之间差异很大,并且在驱虫前α多样性和普雷沃氏菌肠型较低的个体中较低。我们观察到感染个体中双歧杆菌属物种的显著减少,无论肠型如何,这些益生菌在驱虫后都没有恢复。代谢网络分析和体外实验表明,双歧杆菌的减少与生态位或营养物(特别是其他微生物的棉子糖)的代谢竞争有关,而不是寄生虫本身。此外,我们的机器学习分析表明,棉子糖代谢中与双歧杆菌相关的分类群可以很好地预测感染,但不能预测驱虫。这项研究强调了带绦虫病对人类肠道微生物组和整体肠道健康的重大影响。