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

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 o...

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Main Authors: William A de Glanville, James M Nyarobi, Tito Kibona, Jo E B Halliday, Kate M Thomas, Kathryn J Allan, Paul C D Johnson, Alicia Davis, Felix Lankester, John R Claxton, Melinda K Rostal, Ryan W Carter, Rosanne M F de Jong, Matthew P Rubach, John A Crump, Blandina T Mmbaga, Obed M Nyasebwa, Emanuel S Swai, Brian Willett, Sarah Cleaveland
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-10-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0010871
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author William A de Glanville
James M Nyarobi
Tito Kibona
Jo E B Halliday
Kate M Thomas
Kathryn J Allan
Paul C D Johnson
Alicia Davis
Felix Lankester
John R Claxton
Melinda K Rostal
Ryan W Carter
Rosanne M F de Jong
Matthew P Rubach
John A Crump
Blandina T Mmbaga
Obed M Nyasebwa
Emanuel S Swai
Brian Willett
Sarah Cleaveland
author_facet William A de Glanville
James M Nyarobi
Tito Kibona
Jo E B Halliday
Kate M Thomas
Kathryn J Allan
Paul C D Johnson
Alicia Davis
Felix Lankester
John R Claxton
Melinda K Rostal
Ryan W Carter
Rosanne M F de Jong
Matthew P Rubach
John A Crump
Blandina T Mmbaga
Obed M Nyasebwa
Emanuel S Swai
Brian Willett
Sarah Cleaveland
author_sort William A de Glanville
collection DOAJ
description 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.
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spelling doaj.art-a2872b94bf6345d38107c1f63d71a8052023-08-06T05:31:57ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352022-10-011610e001087110.1371/journal.pntd.0010871Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.William A de GlanvilleJames M NyarobiTito KibonaJo E B HallidayKate M ThomasKathryn J AllanPaul C D JohnsonAlicia DavisFelix LankesterJohn R ClaxtonMelinda K RostalRyan W CarterRosanne M F de JongMatthew P RubachJohn A CrumpBlandina T MmbagaObed M NyasebwaEmanuel S SwaiBrian WillettSarah CleavelandRift 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.https://doi.org/10.1371/journal.pntd.0010871
spellingShingle William A de Glanville
James M Nyarobi
Tito Kibona
Jo E B Halliday
Kate M Thomas
Kathryn J Allan
Paul C D Johnson
Alicia Davis
Felix Lankester
John R Claxton
Melinda K Rostal
Ryan W Carter
Rosanne M F de Jong
Matthew P Rubach
John A Crump
Blandina T Mmbaga
Obed M Nyasebwa
Emanuel S Swai
Brian Willett
Sarah Cleaveland
Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.
PLoS Neglected Tropical Diseases
title Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.
title_full Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.
title_fullStr Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.
title_full_unstemmed Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.
title_short Inter-epidemic Rift Valley fever virus infection incidence and risks for zoonotic spillover in northern Tanzania.
title_sort inter epidemic rift valley fever virus infection incidence and risks for zoonotic spillover in northern tanzania
url https://doi.org/10.1371/journal.pntd.0010871
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