Population genomic evidence that human and animal infections in Africa come from the same populations of Dracunculus medinensis.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
11 2020
Historique:
received: 21 11 2019
accepted: 22 07 2020
revised: 10 12 2020
pubmed: 1 12 2020
medline: 23 1 2021
entrez: 30 11 2020
Statut: epublish

Résumé

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. 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. 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.

Sections du résumé

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.

Identifiants

pubmed: 33253172
doi: 10.1371/journal.pntd.0008623
pii: PNTD-D-19-01951
pmc: PMC7728184
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0008623

Subventions

Organisme : Wellcome Trust
ID : 206194
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 206194
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 098051
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/M003949/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 098051
Pays : United Kingdom

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist. Author Ouakou Tchindebet was unable to confirm their authorship contributions. On their behalf, the corresponding author has reported their contributions to the best of their knowledge.

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Auteurs

Caroline Durrant (C)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Elizabeth A Thiele (EA)

Department of Biology, Vassar College, Poughkeepsie, New York, United States of America.

Nancy Holroyd (N)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Stephen R Doyle (SR)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Guillaume Sallé (G)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.
INRA-U. Tours, UMR 1282 ISP Infectiologie et Santé Publique, Nouzilly, France.

Alan Tracey (A)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Geetha Sankaranarayanan (G)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Magda E Lotkowska (ME)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Hayley M Bennett (HM)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.
Present Address: Berkeley Lights Inc., Emeryville, California, United States of America.

Thomas Huckvale (T)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Zahra Abdellah (Z)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Ouakou Tchindebet (O)

Guinea Worm Eradication Program, The Carter Center, Atlanta, Georgia, United States of America.

Mesfin Wossen (M)

Guinea Worm Eradication Program, The Carter Center, Atlanta, Georgia, United States of America.

Makoy Samuel Yibi Logora (MSY)

Guinea Worm Eradication Program, The Carter Center, Atlanta, Georgia, United States of America.

Cheick Oumar Coulibaly (CO)

Guinea Worm Eradication Program, The Carter Center, Atlanta, Georgia, United States of America.

Adam Weiss (A)

Guinea Worm Eradication Program, The Carter Center, Atlanta, Georgia, United States of America.

Albrecht I Schulte-Hostedde (AI)

Department of Biology, Laurentian University, Sudbury, Canada.

Jeremy M Foster (JM)

New England Biolabs, Ipswich, Massachusetts, United States of America.

Christopher A Cleveland (CA)

Southeastern Cooperative Wildlife Disease Study, Department of Population Health, Veterinary Medicine, University of Georgia, Athens, Georgia, United States of America.

Michael J Yabsley (MJ)

Southeastern Cooperative Wildlife Disease Study, Department of Population Health, Veterinary Medicine, University of Georgia, Athens, Georgia, United States of America.
Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia, United States of America.

Ernesto Ruiz-Tiben (E)

Guinea Worm Eradication Program, The Carter Center, Atlanta, Georgia, United States of America.

Matthew Berriman (M)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

Mark L Eberhard (ML)

Retired, Parasitic Diseases Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America.

James A Cotton (JA)

Parasites and Microbes, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridgeshire, United Kingdom.

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