Population genetic analysis of Chadian Guinea worms reveals that human and non-human hosts share common parasite populations

Following almost 10 years of no reported cases, Guinea worm disease (GWD or dracunculiasis) reemerged in Chad in 2010 with peculiar epidemiological patterns and unprecedented prevalence of infection among non-human hosts, particularly domestic dogs. Since 2014, animal infections with Guinea worms have also been observed in the other three countries with endemic transmission (Ethiopia, Mali, and South Sudan), causing concern and generating interest in the parasites’ true taxonomic identity and population genetics. We present the first extensive population genetic data for Guinea worm, investigating mitochondrial and microsatellite variation in adult female worms from both human and non-human hosts in the four endemic countries to elucidate the origins of Chad’s current outbreak and possible host-specific differences between parasites. Genetic diversity of Chadian Guinea worms was considerably higher than that of the other three countries, even after controlling for sample size through rarefaction, and demographic analyses are consistent with a large, stable parasite population. Genealogical analyses eliminate the other three countries as possible sources of parasite reintroduction into Chad, and sequence divergence and distribution of genetic variation provide no evidence that parasites in human and non-human hosts are separate species or maintain isolated transmission cycles. Both among and within countries, geographic origin appears to have more influence on parasite population structure than host species. Guinea worm infection in non-human hosts has been occasionally reported throughout the history of the disease, particularly when elimination programs appear to be reaching their end goals. However, no previous reports have evaluated molecular support of the parasite species identity. Our data confirm that Guinea worms collected from non-human hosts in the remaining endemic countries of Africa are Dracunculus medinensis and that the same population of worms infects both humans and dogs in Chad. Our genetic data and the epidemiological evidence suggest that transmission in the Chadian context is currently being maintained by canine hosts.

在近十年无报告病例后，几内亚龙线虫病（Guinea worm disease, GWD，又称麦地那龙线虫病dracunculiasis）于2010年在乍得重现，呈现出特殊的流行病学特征，且非人宿主（尤其是家犬）的感染率达到空前水平。2014年起，另外三个存在地方性传播的国家（埃塞俄比亚、马里、南苏丹）也相继报告了几内亚龙线虫的动物感染病例，这引发了学界对该寄生虫真实分类学身份与群体遗传学的关注与研究兴趣。本研究首次提供了几内亚龙线虫的大规模群体遗传学数据，对四个流行国家中来自人类与非人宿主的成年雌虫的线粒体（mitochondrial）及微卫星（microsatellite）变异进行分析，以阐明乍得当前疫情的起源，以及寄生虫是否存在宿主特异性差异。即便通过稀疏化（rarefaction）方法校正样本量后，乍得几内亚龙线虫的遗传多样性仍显著高于另外三个国家；群体动态分析结果与该寄生虫种群规模庞大且稳定的结论一致。谱系分析（genealogical analyses）排除了另外三个国家作为乍得寄生虫重新引入源的可能性；序列分化度与遗传变异分布均未提供证据表明人类与非人宿主中的寄生虫为不同物种，或二者维持独立的传播循环。在国家间与国家内部，地理起源对寄生虫种群结构的影响均大于宿主种类。纵观几内亚龙线虫病的流行史，非人宿主感染病例时有报告，尤其在根除计划接近最终目标的阶段。但此前尚无研究通过分子手段验证该寄生虫的物种身份。本研究数据证实，非洲剩余流行国家中从非人宿主分离的几内亚龙线虫均为麦地那龙线虫（Dracunculus medinensis），且乍得地区感染人类与家犬的为同一寄生虫种群。结合遗传学数据与流行病学证据，当前乍得地区的传播循环主要由犬类宿主维持。