Guillaume Sallé, Makoy Yibi Logora, Hayley M. Bennett, Stephen R. Doyle, Geetha Sankaranarayanan, Michael J. Yabsley, Mesfin Wossen, Zahra Abdellah, Mark L. Eberhard, Magda E. Lotkowska, Jeremy M. Foster, Matthew Berriman, Cheick Oumar Coulibaly, Christopher A. Cleveland, Nancy Holroyd, Adam Weiss, Thomas Huckvale, Alan Tracey, James Cotton, Albrecht I. Schulte-Hostedde, Ouakou Tchindebet, Caroline Durrant, Elizabeth A. Thiele, Ernesto Ruiz-Tiben, Parasites and Microbes, The Wellcome Trust Sanger Institute [Cambridge], Department of Biology, Vassar College, Infectiologie et Santé Publique (UMR ISP), Université de Tours-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Guinea Worm Eradication Program, The Carter Center, Partenaires INRAE-Partenaires INRAE, Laurentian University, New England Biolabs, Southeastern Cooperative Wildlife Disease Study, University of Georgia [USA], Warnell School of Forestry and Natural Resources, Parasitic Diseases Branch, Centers for Disease Control and Prevention (CDC), Wellcome (https://wellcome.ac.uk/, n° 098051 and 206194), BBSRC (https://bbsrc.ukri.org/, n° BB/M003949/1), and Université de Tours (UT)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
Background Guinea worm–Dracunculus medinensis–was historically one of the major parasites of humans and has been known since antiquity. Now, Guinea worm is on the brink of eradication, as efforts to interrupt transmission have reduced the annual burden of disease from millions of infections per year in the 1980s to only 54 human cases reported globally in 2019. Despite the enormous success of eradication efforts to date, one complication has arisen. Over the last few years, hundreds of dogs have been found infected with this previously apparently anthroponotic parasite, almost all in Chad. Moreover, the relative numbers of infections in humans and dogs suggests that dogs are currently the principal reservoir on infection and key to maintaining transmission in that country. Principal findings In an effort to shed light on this peculiar epidemiology of Guinea worm in Chad, we have sequenced and compared the genomes of worms from dog, human and other animal infections. Confirming previous work with other molecular markers, we show that all of these worms are D. medinensis, and that the same population of worms are causing both infections, can confirm the suspected transmission between host species and detect signs of a population bottleneck due to the eradication efforts. The diversity of worms in Chad appears to exclude the possibility that there were no, or very few, worms present in the country during a 10-year absence of reported cases. Conclusions This work reinforces the importance of adequate surveillance of both human and dog populations in the Guinea worm eradication campaign and suggests that control programs aiming to interrupt disease transmission should stay aware of the possible emergence of unusual epidemiology as pathogens approach elimination., Author summary Guinea worm–Dracunculus medinensis–was historically one of the major parasites of humans and has been known since antiquity. Guinea worm is now on the brink of eradication, as a global effort seeking to make this parasite extinct has reduced the number of people infected each year from millions in the 1980s to only 54 human cases in 2019. Despite the enormous success of eradication efforts to date, one complication has arisen. Over the last few years, hundreds of dogs have been found infected with Guinea worm, which was previously considered to be transmitted between people. Almost all of these infected animals are in Chad. We have used whole-genome sequence data to try and understand this peculiar situation. We confirm that the same population of worms are causing both infections and show suspected transmission from humans to dogs. The diversity of worms in Chad appears to exclude the possibility that there were no, or very few, worms present in the country during a 10-year absence of reported cases. This work reinforces the importance of adequate surveillance of both human and dog populations and suggests that control programs should stay aware of the emergence of unusual epidemiology as pathogens approach elimination.