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Estimation of Rift Valley fever virus spillover to humans during the Mayotte 2018-2019 epidemic.

ABSTRACT: Rift Valley fever (RVF) is an emerging, zoonotic, arboviral hemorrhagic fever threatening livestock and humans mainly in Africa. RVF is of global concern, having expanded its geographical range over the last decades. The impact of control measures on epidemic dynamics using empirical data has not been assessed. Here, we fitted a mathematical model to seroprevalence livestock and human RVF case data from the 2018-2019 epidemic in Mayotte to estimate viral transmission among livestock, and spillover from livestock to humans through both direct contact and vector-mediated routes. Model simulations were used to assess the impact of vaccination on reducing the epidemic size. The rate of spillover by direct contact was about twice as high as vector transmission. Assuming 30% of the population were farmers, each transmission route contributed to 45% and 55% of the number of human infections, respectively. Reactive vaccination immunizing 20% of the livestock population reduced the number of human cases by 30%. Vaccinating 1 mo later required using 50% more vaccine doses for a similar reduction. Vaccinating only farmers required 10 times as more vaccine doses for a similar reduction in human cases. Finally, with 52.0% (95% credible interval [CrI] [42.9-59.4]) of livestock immune at the end of the epidemic wave, viral reemergence in the next rainy season (2019-2020) is unlikely. Coordinated human and animal health surveillance, and timely livestock vaccination appear to be key to controlling RVF in this setting. We furthermore demonstrate the value of a One Health quantitative approach to surveillance and control of zoonotic infectious diseases.

SUBMITTER: Metras R

PROVIDER: S-EPMC7533885 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Estimation of Rift Valley fever virus spillover to humans during the Mayotte 2018-2019 epidemic.

Métras Raphaëlle R Edmunds W John WJ Youssouffi Chouanibou C Dommergues Laure L Fournié Guillaume G Camacho Anton A Funk Sebastian S Cardinale Eric E Le Godais Gilles G Combo Soihibou S Filleul Laurent L Youssouf Hassani H Subiros Marion M

Proceedings of the National Academy of Sciences of the United States of America 20200914 39

Rift Valley fever (RVF) is an emerging, zoonotic, arboviral hemorrhagic fever threatening livestock and humans mainly in Africa. RVF is of global concern, having expanded its geographical range over the last decades. The impact of control measures on epidemic dynamics using empirical data has not been assessed. Here, we fitted a mathematical model to seroprevalence livestock and human RVF case data from the 2018-2019 epidemic in Mayotte to estimate viral transmission among livestock, and spillov ...[more]

PMID: 32929025

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Project description:BackgroundIn East Africa, epidemics of Rift Valley fever (RVF) occur in cycles of 5-15 years following unusually high rainfall. RVF transmission during inter-epidemic periods (IEP) generally passes undetected in absence of surveillance in mammalian hosts and vectors. We studied IEP transmission of RVF and evaluated the demographic, behavioural, occupational and spatial determinants of past RVF infection.MethodologyBetween March and August 2012 we collected blood samples, and administered a risk factor questionnaire among 606 inhabitants of 6 villages in the seasonally inundated Kilombero Valley, Tanzania. ELISA tests were used to detect RVFV IgM and IgG antibodies in serum samples. Risk factors were examined by mixed effects logistic regression.FindingsRVF virus IgM antibodies, indicating recent RVFV acquisition, were detected in 16 participants, representing 2.6% overall and in 22.5% of inhibition ELISA positives (n = 71). Four of 16 (25.0%) IgM positives and 11/71 (15.5%) of individuals with inhibition ELISA sero-positivity reported they had had no previous contact with host animals. Sero-positivity on inhibition ELISA was 11.7% (95% CI 9.2-14.5) and risk was elevated with age (odds ratio (OR) 1.03 per year; 95% CI 1.01-1.04), among milkers (OR 2.19; 95% CI 1.23-3.91), and individuals eating raw meat (OR 4.17; 95% CI 1.18-14.66). Households keeping livestock had a higher probability of having members with evidence of past infection (OR = 3.04, 95% CI = 1.42-6.48) than those that do not keep livestock.ConclusionThere is inter-epidemic acquisition of RVFV in Kilombero Valley inhabitants. In the wake of declining malaria incidence, these findings underscore the need for clinicians to consider RVF in the differential diagnosis for febrile illnesses. Several types of direct contact with livestock are important risk factors for past infection with RVFV in this study's population. However, at least part of RVFV transmission appears to have occurred through bites of infected mosquitoes.

Project 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.

Project description:Rift Valley fever (RVF) is a vector-borne disease transmitted by different mosquito species, especially Aedes and Culex genus, to animals and humans. In November 2018, RVF re-emerged in Mayotte (France) after 11 years. Up to the end of October 2019, 126 outbreaks in animals and 143 human cases were reported. RVF mortality was 0.01%, and the number of abortions reported in polymerase chain reaction (PCR)-positive ruminants was fivefold greater than the previous 7 years. Milk loss production in 2019 compared to 2015-2018 was estimated to be 18%, corresponding to an economic loss of around €191,000 in all of Mayotte. The tropical climate in Mayotte provides conditions for the presence of mosquitoes during the whole year, and illegal introductions of animals represent a continuous risk of (re)introduction of RVF. The probability of RVF virus (RVFV) persisting in Mayotte for 5 or more years was estimated to be < 10% but could be much lower if vertical transmission in vectors does not occur. Persistence of RVF by vertical transmission in Mayotte and Réunion appears to be of minor relevance compared to other pathways of re-introduction (i.e. animal movement). However, there is a high uncertainty since there is limited information about the vertical transmission of some of the major species of vectors of RVFV in Mayotte and Réunion. The only identified pathways for the risk of spread of RVF from Mayotte to other countries were by infected vectors transported in airplanes or by wind currents. For the former, the risk of introduction of RVF to continental France was estimated to 4 × 10-6 epidemic per year (median value; 95% CI: 2 × 10-8; 0.0007), and 0.001 epidemic per year to Réunion (95% CI: 4 × 10-6; 0.16). For the latter pathway, mosquitoes dispersing on the wind from Mayotte between January and April 2019 could have reached the Comoros Islands, Madagascar, Mozambique and, possibly, Tanzania. However, these countries are already endemic for RVF, and an incursion of RVFV-infected mosquitoes would have negligible impact.

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Estimation of Rift Valley fever virus spillover to humans during the Mayotte 2018-2019 epidemic.

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Estimation of Rift Valley fever virus spillover to humans during the Mayotte 2018-2019 epidemic.

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