Integrating contact tracing and whole-genome sequencing to track the elimination of dog-mediated rabies: an observational and genomic study

Lushasi, K. et al. (2023) Integrating contact tracing and whole-genome sequencing to track the elimination of dog-mediated rabies: an observational and genomic study. eLife, 12, e85262. (doi: 10.7554/elife.85262) (PMID:37227428) (PMCID:PMC10299823)

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Abstract

Background: Dog-mediated rabies is endemic across Africa causing thousands of human deaths annually. A One Health approach to rabies is advocated, comprising emergency post-exposure vaccination of bite victims and mass dog vaccination to break the transmission cycle. However, the impacts and cost-effectiveness of these components are difficult to disentangle. Methods: We combined contact tracing with whole-genome sequencing to track rabies transmission in the animal reservoir and spillover risk to humans from 2010-2020, investigating how the components of a One Health approach reduced the disease burden and eliminated rabies from Pemba Island, Tanzania. With the resulting high-resolution spatiotemporal and genomic data we inferred transmission chains and estimated case detection. Using a decision tree model we quantified the public health burden and evaluated the impact and cost-effectiveness of interventions over a ten-year time horizon. Results: We resolved five transmission chains co-circulating on Pemba from 2010 that were all eliminated by May 2014. During this period, rabid dogs, human rabies exposures and deaths all progressively declined following initiation and improved implementation of annual islandwide dog vaccination. We identified two introductions to Pemba in late 2016 that seeded re-emergence after dog vaccination had lapsed. The ensuing outbreak was eliminated in October 2018 through reinstated islandwide dog vaccination. While post-exposure vaccines were projected to be highly cost-effective ($256 per death averted), only dog vaccination interrupts transmission. A combined One Health approach of routine annual dog vaccination together with free post-exposure vaccines for bite victims, rapidly eliminates rabies, is highly cost-effective ($1657 per death averted) and by maintaining rabies freedom prevents over 30 families from suffering traumatic rabid dog bites annually on Pemba island. Conclusions: A One Health approach underpinned by dog vaccination is an efficient, cost-effective, equitable and feasible approach to rabies elimination, but needs scaling up across connected populations to sustain the benefits of elimination, as seen on Pemba, and for similar progress to be achieved elsewhere. Funding: Wellcome [207569/Z/17/Z, 095787/Z/11/Z, 103270/Z/13/Z], the UBS Optimus Foundation, the Department of Health and Human Services of the National Institutes of Health [R01AI141712] and the DELTAS Africa Initiative [Afrique One-ASPIRE/DEL-15-008] comprising a donor consortium of the African Academy of Sciences (AAS), Alliance for Accelerating Excellence in Science in Africa (AESA), the New Partnership for Africa's Development Planning and Coordinating (NEPAD) Agency, Wellcome [107753/A/15/Z], Royal Society of Tropical Medicine and Hygiene Small Grant 2017 [GR000892] and the UK government. The rabies elimination demonstration project from 2010-2015 was supported by the Bill & Melinda Gates Foundation [OPP49679]. Whole-genome sequencing was partially supported from APHA by funding from the UK Department for Environment, Food and Rural Affairs (Defra), Scottish government and Welsh government under projects SEV3500 & SE0421.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Johnson, Dr Paul and Haydon, Professor Daniel and jaswant, gurdeep and changalucha, Mr joel and Lembo, Dr Tiziana and Rajeev, Dr Malavika and Cleaveland, Professor Sarah and Brunker, Dr Kirstyn and Baker, Miss Laurie and Hampson, Professor Katie and Rysava, Ms Kristyna and Czupryna, Dr Anna and Steenson, Miss Rachel and Mpolya, Dr Emmanuel and Sikana, Mr Lwitiko and Sambo, Dr Maganga and Biek, Professor Roman and Lushasi, Mr Kennedy and Ferguson, Dr Elaine
Authors: Lushasi, K., Brunker, K., Rajeev, M., Ferguson, E. A., Jaswant, G., Baker, L. L., Biek, R., Changalucha, J., Cleaveland, S., Czupryna, A., Fooks, A. R., Govella, N. J., Haydon, D. T., Johnson, P. C.D., Kazwala, R., Lembo, T., Marston, D., Masoud, M., Maziku, M., Mbunda, E., Mchau, G., Mohamed, A. Z., Mpolya, E., Ngeleja, C., Ng'habi, K., Nonga, H., Omar, K., Rysava, K., Sambo, M., Sikana, L., Steenson, R., and Hampson, K.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:eLife
Publisher:eLife Sciences Publications
ISSN:2050-084X
ISSN (Online):2050-084X
Published Online:25 May 2023
Copyright Holders:Copyright © 2023 Lushasi et al.
First Published:First published in eLife 12: e85262
Publisher Policy:Reproduced under a Creative Commons License
Data DOI:10.5281/zenodo.7922464

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
301620The Science of Rabies EliminationKatie HampsonWellcome Trust (WELLCOTR)207569/Z/17/ZInstitute of Biodiversity, Animal Health and Comparative Medicine
165644Hierarchical epidemiology: the spread and persistence of infectious diseases in complex landscapesKatie HampsonWellcome Trust (WELLCOTR)095787/Z/11/ZInstitute of Biodiversity, Animal Health and Comparative Medicine
170566Rabies persistance and elimination from Pemba Island, TanzaniaKatie HampsonWellcome Trust (WELLCOTR)103270/Z/13/ZInstitute of Biodiversity, Animal Health and Comparative Medicine