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

epidemiology global health infectious disease microbiology next generation sequencing one health surveillance vaccine-preventable viruses zoonotic disease

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
25 05 2023
Historique:
received: 30 11 2022
accepted: 24 05 2023
medline: 29 6 2023
pubmed: 25 5 2023
entrez: 25 5 2023
Statut: epublish

Résumé

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. We combined contact tracing with whole-genome sequencing to track rabies transmission in the animal reservoir and spillover risk to humans from 2010 to 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 10-year time horizon. 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. 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. 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 and SE0421.

Sections du résumé

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 to 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 10-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 and SE0421.

Identifiants

pubmed: 37227428
doi: 10.7554/eLife.85262
pii: 85262
pmc: PMC10299823
doi:
pii:

Substances chimiques

Rabies Vaccines 0

Types de publication

Observational Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Wellcome Trust
ID : 107753/A/15/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 095787/Z/11/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 207569/Z/17/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 103270/Z/13/Z
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : R01 AI141712
Pays : United States
Organisme : EPA
ID : EP-C-15-008
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

© 2023, Lushasi, Brunker et al.

Déclaration de conflit d'intérêts

KL, KB, MR, EF, GJ, LB, RB, JC, SC, AC, AF, NG, DH, PJ, RK, TL, DM, MM, MM, EM, GM, AM, EM, CN, KN, HN, KO, KR, MS, LS, RS, KH No competing interests declared

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Auteurs

Kennedy Lushasi (K)

Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Dar es salaam, United Republic of Tanzania.
Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.
Department of Global Health and Biomedical Sciences, School of Life Sciences and Bioengineering, Nelson Mandela African Institution of Science and Technology, Arusha, United Republic of Tanzania.

Kirstyn Brunker (K)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Malavika Rajeev (M)

Department of Ecology and Evolutionary Biology, Princeton University, Princeton, United States.

Elaine A Ferguson (EA)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Gurdeep Jaswant (G)

Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Dar es salaam, United Republic of Tanzania.
The University of Nairobi, Nairobi, Kenya.

Laurie Louise Baker (LL)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.
College of the Atlantic, Bar Harbor, United States.

Roman Biek (R)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Joel Changalucha (J)

Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Dar es salaam, United Republic of Tanzania.
Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.
Animal & Plant Health Agency, Weybridge, United Kingdom.

Sarah Cleaveland (S)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Anna Czupryna (A)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Anthony R Fooks (AR)

Animal & Plant Health Agency, Weybridge, United Kingdom.

Nicodemus J Govella (NJ)

Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Dar es salaam, United Republic of Tanzania.

Daniel T Haydon (DT)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Paul C D Johnson (PCD)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Rudovick Kazwala (R)

Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, Morogoro, United Republic of Tanzania.

Tiziana Lembo (T)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Denise Marston (D)

Animal & Plant Health Agency, Weybridge, United Kingdom.
Department of Comparative Biomedical Sciences, School of Veterinary Medicine, University of Surrey, Guildford, Surrey, United Kingdom.

Msanif Masoud (M)

Ministry for Health and Social Welfare, Zanzibar, United Republic of Tanzania.

Matthew Maziku (M)

Ministry of Livestock Development and Fisheries, Dodoma, United Republic of Tanzania.

Eberhard Mbunda (E)

Ministry of Livestock Development and Fisheries, Dodoma, United Republic of Tanzania.

Geofrey Mchau (G)

Department of Epidemiology, Ministry of Health, Community Development, Gender, Elderly and Children (MoHCDGEC), Dodoma, United Republic of Tanzania.

Ally Z Mohamed (AZ)

Department of Livestock Development, Pemba, Ministry of Livestock Development and Fisheries, Zanzibar, United Republic of Tanzania.

Emmanuel Mpolya (E)

Department of Global Health and Biomedical Sciences, School of Life Sciences and Bioengineering, Nelson Mandela African Institution of Science and Technology, Arusha, United Republic of Tanzania.

Chanasa Ngeleja (C)

Tanzania Veterinary Laboratory Agency, Dar es salaam, United Republic of Tanzania.

Kija Ng'habi (K)

Mbeya college of Health and Allied Sciences, University of Dar es Salaam, Mbeya, United Republic of Tanzania.

Hezron Nonga (H)

Ministry of Livestock Development and Fisheries, Dodoma, United Republic of Tanzania.

Kassim Omar (K)

Department of Livestock Development, Pemba, Ministry of Livestock Development and Fisheries, Zanzibar, United Republic of Tanzania.

Kristyna Rysava (K)

University of Warwick, Coventry, United Kingdom.

Maganga Sambo (M)

Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Dar es salaam, United Republic of Tanzania.

Lwitiko Sikana (L)

Environmental Health and Ecological Sciences Department, Ifakara Health Institute, Dar es salaam, United Republic of Tanzania.

Rachel Steenson (R)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

Katie Hampson (K)

Boyd Orr Centre for Population and Ecosystem Health, School of Biodiversity, One Health & Veterinary Medicine, University of Glasgow, Glasgow, United Kingdom.

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