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

Abstract

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.

Author summary

Since the mid-1980’s, when Guinea worm ( Dracunculus medinensis) was formally targeted for eradication, the associated national and international efforts to control and eliminate the parasite have been remarkably successful. As of 2017, 16 of the 21 countries with endemic transmission have been certified free of the disease by World Health Organization, and one country (Sudan) is in the pre-certification stage. However, recent and unprecedented prevalence of apparent Guinea worm infection in Chadian dogs has caused concern. That this seemingly sudden emergence in non-human hosts also coincided with an apparent reemergence of infection among humans in Chad after almost 10 years without reported cases raised questions about the population history of Guinea worm in Chad and whether worms from human and non-human hosts were, in fact, the same species. To address these questions, we characterized the genetic variation in Guinea worms collected from various host species and locations in Chad and in the other three endemic countries. Genetic variation was measured in adult female worms using sequence variation of mitochondrial DNA genes and repeat number polymorphism at 23 nuclear microsatellite loci. We found that, regardless of host species, all worms sampled from the remaining endemic countries in Africa are D. medinensis and show no evidence of isolated transmission on the basis of host species.