Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania

de Glanville, W. A. et al. (2022) Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania. PLoS Neglected Tropical Diseases, 16(10), e0010871. (doi: 10.1371/journal.pntd.0010871) (PMID:36306281) (PMCID:PMC9665400)

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Abstract

Rift Valley fever virus (RVFV) is a mosquito-borne pathogen that has caused epidemics involving people and animals across Africa and the Arabian Peninsula. A number of studies have found evidence for the circulation of RVFV among livestock between these epidemics but the population-level incidence of infection during this inter-epidemic period (IEP) is rarely reported. General force of infection (FOI) models were applied to age-adjusted cross-sectional serological data to reconstruct the annual FOI and population-level incidence of RVFV infection among cattle, goats, and sheep in northern Tanzania from 2009 through 2015, a period without reported Rift Valley fever (RVF) cases in people or animals. To evaluate the potential for zoonotic RVFV spillover during this period, the relationship between village-level livestock RVFV FOI and human RVFV seropositivity was quantified using multi-level logistic regression. The predicted average annual incidence was 72 (95% Credible Interval [CrI] 63, 81) RVFV infections per 10,000 animals and 96 (95% CrI 81, 113), 79 (95% CrI 62, 98), and 39 (95% CrI 28, 52) per 10,000 cattle, sheep, and goats, respectively. There was variation in transmission intensity between study villages, with the highest estimated village-level FOI 2.49% (95% CrI 1.89, 3.23) and the lowest 0.12% (95% CrI 0.02, 0.43). The human RVFV seroprevalence was 8.2% (95% Confidence Interval 6.2, 10.9). Human seropositivity was strongly associated with the village-level FOI in livestock, with the odds of seropositivity in an individual person increasing by around 1.2 times (95% CrI 1.1, 1.3) for each additional annual RVFV seroconversion per 1,000 animals. A history of raw milk consumption was also positively associated with human seropositivity. RVFV has circulated at apparently low levels among livestock in northern Tanzania in the period since the last reported epidemic. Although our data do not allow us to confirm human RVFV infections during the IEP, a strong association between human seropositivity and the FOI in cattle, goats, and sheep supports the hypothesis that RVFV circulation among livestock during the IEP poses a risk for undetected zoonotic spillover in northern Tanzania. We provide further evidence for the likely role of raw milk consumption in RVFV transmission from animals to people.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:De Glanville, Dr William and Lankester, Dr Felix and Johnson, Dr Paul and Halliday, Dr Jo and MMBAGA, Professor Blandina Theoph and Willett, Professor Brian and Rostal, Melinda Kathleen and Allan, Dr Kathryn and Cleaveland, Professor Sarah and De Jong, Ms Rosanne and Carter, Mr Ryan and Davis, Dr Alicia and Claxton, Dr John and Thomas, Dr Kate
Creator Roles:
De Glanville, W.Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Visualization, Writing – original draft, Writing – review and editing
Halliday, J.Data curation, Investigation, Writing – review and editing
Thomas, K.Investigation, Writing – review and editing
Allan, K.Investigation, Writing – review and editing
Johnson, P.Investigation, Writing – review and editing
Davis, A.Investigation, Writing – review and editing
Lankester, F.Investigation, Writing – review and editing
Claxton, J.Investigation, Project administration, Writing – review and editing
Rostal, M. K.Methodology, Writing – review and editing
Carter, R.Investigation, Writing – review and editing
De Jong, R.Investigation, Writing – review and editing
MMBAGA, B. T.Investigation, Project administration, Writing – review and editing
Willett, B.Investigation, Writing – review and editing
Cleaveland, S.Conceptualization, Funding acquisition, Investigation, Supervision, Writing – review and editing
Authors: de Glanville, W. A., Nyarobi, J. M., Kibona, T., Halliday, J. E.B., Thomas, K. M., Allan, K. J., Johnson, P. C.D., Davis, A., Lankester, F., Claxton, J. R., Rostal, M. K., Carter, R. W., de Jong, R. M.F., Rubach, M. P., Crump, J. A., Mmbaga, B. T., Nyasebwa, O. M., Swai, E. S., Willett, B., and Cleaveland, S.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
College of Medical Veterinary and Life Sciences > School of Infection & Immunity > Centre for Virus Research
College of Social Sciences > School of Social and Political Sciences > Sociology Anthropology and Applied Social Sciences
Journal Name:PLoS Neglected Tropical Diseases
Publisher:Public Library of Science
ISSN:1935-2727
ISSN (Online):1935-2735
Published Online:28 October 2022
Copyright Holders:Copyright © 2022 de Glanville et al.
First Published:First published in PLoS Neglected Tropical Diseases 16(10): e0010871
Publisher Policy:Reproduced under a Creative Commons License
Data DOI:10.5525/gla.researchdata.1239

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
190825Social, economic and environmental drivers of zoonoses in Tanzania (SEEDZ)Sarah CleavelandBiotechnology and Biological Sciences Research Council (BBSRC)BB/L018926/1Institute of Biodiversity, Animal Health and Comparative Medicine
190821Hazards associated with zoonotic enteric pathogens in emerging livestock meat pathways (HAZEL)Ruth ZadoksBiotechnology and Biological Sciences Research Council (BBSRC)BB/L017679/1Institute of Biodiversity, Animal Health and Comparative Medicine
171979Zoonoses and Emerging Livestock Systems ZELS Reducing the risk to livestock and people programme associated studentships - ZELS-ASSarah CleavelandBiotechnology and Biological Sciences Research Council (BBSRC)BB/N503563/1Institute of Biodiversity, Animal Health and Comparative Medicine
190437Impact, ecology and social determinants of bacterial zoonoses in northern TanzaniaSarah CleavelandBiotechnology and Biological Sciences Research Council (BBSRC)BB/J010367/1Institute of Biodiversity, Animal Health and Comparative Medicine