Linked surveillance and genetic data uncovers programmatically relevant geographic scale of Guinea worm transmission in Chad

Ribado, J. V. et al. (2021) Linked surveillance and genetic data uncovers programmatically relevant geographic scale of Guinea worm transmission in Chad. PLoS Neglected Tropical Diseases, 15(7), e0009609. (doi: 10.1371/journal.pntd.0009609) (PMID:34310598) (PMCID:PMC8341693)

Abstract

Background: Guinea worm (Dracunculus medinensis) was detected in Chad in 2010 after a supposed ten-year absence, posing a challenge to the global eradication effort. Initiation of a village-based surveillance system in 2012 revealed a substantial number of dogs infected with Guinea worm, raising questions about paratenic hosts and cross-species transmission. Methodology/principal findings: We coupled genomic and surveillance case data from 2012-2018 to investigate the modes of transmission between dog and human hosts and the geographic connectivity of worms. Eighty-six variants across four genes in the mitochondrial genome identified 41 genetically distinct worm genotypes. Spatiotemporal modeling revealed worms with the same genotype (‘genetically identical’) were within a median range of 18.6 kilometers of each other, but largely within approximately 50 kilometers. Genetically identical worms varied in their degree of spatial clustering, suggesting there may be different factors that favor or constrain transmission. Each worm was surrounded by five to ten genetically distinct worms within a 50 kilometer radius. As expected, we observed a change in the genetic similarity distribution between pairs of worms using variants across the complete mitochondrial genome in an independent population. Conclusions/significance: In the largest study linking genetic and surveillance data to date of Guinea worm cases in Chad, we show genetic identity and modeling can facilitate the understanding of local transmission. The co-occurrence of genetically non-identical worms in quantitatively identified transmission ranges highlights the necessity for genomic tools to link cases. The improved discrimination between pairs of worms from variants identified across the complete mitochondrial genome suggests that expanding the number of genomic markers could link cases at a finer scale. These results suggest that scaling up genomic surveillance for Guinea worm may provide additional value for programmatic decision-making critical for monitoring cases and intervention efficacy to achieve elimination.

• Item Type: Articles
• Additional Information: Funding: This publication is based on research funded in part by the Bill & Melinda Gates Foundation, including but not limited to models and data analysis performed by the Institute for Disease Modeling at the Bill & Melinda Gates Foundation by JVR, NL, HL, GCC, JLP. JAC was supported by funding from The Carter Center and Wellcome, via their core support for the Wellcome Sanger Institute (grant WT206194).
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Cotton, Professor James
• Authors: Ribado, J. V., Li, N. J., Thiele, E., Lyons, H., Cotton, J. A., Weiss, A., Tchindebet Ouakou, P., Moundai, T., Zirimwabagabo, H., Guagliardo, S. A. J., Chabot-Couture, G., and Proctor, J. L.
• College/School: College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
• Journal Name: PLoS Neglected Tropical Diseases
• Publisher: Public Library of Science
• ISSN: 1935-2727
• ISSN (Online): 1935-2735
• Published Online: 26 July 2021
• Copyright Holders: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
• First Published: First published in PLoS Neglected Tropical Diseases 15(7): e0009609
• Publisher Policy: The work is made available under the Creative Commons CC0 public domain dedication.