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How much does direct transmission between pigs contribute to Japanese Encephalitis virus circulation? A modelling approach in Cambodia.

ABSTRACT: Japanese Encephalitis (JE) is the most important cause of human encephalitis throughout Asia and the Pacific. Although JE is a vector-borne disease, it has been demonstrated experimentally that transmission between pigs can occur through direct contact. Whether pig-to-pig transmission plays a role in the natural epidemiological cycle of JE remains unknown. To assess whether direct transmission between pigs may occur under field conditions, we built two mathematical models of JE transmission incorporating vector-borne transmission alone or a combination of vector-borne and direct transmission. We used Markov Chain Monte Carlo (MCMC) techniques to estimate the parameters of the models. We fitted the models to (i) two serological datasets collected longitudinally from two pig cohorts (C1 and C2) during two periods of four months on a farm on the outskirts of Phnom-Penh, Cambodia and to (ii) a cross-sectional (CS) serological survey dataset collected from 505 swine coming from eight different provinces of Cambodia. In both cases, the model incorporating both vector-borne and direct transmission better explained the data. We computed the value of the basic reproduction number R0 (2.93 for C1, 2.66 for C2 and 2.27 for CS), as well as the vector-borne reproduction number Rpv and the direct transmission reproduction number Rpp. We then determined the contribution of direct transmission on R0 (11.90% for C1, 11.62% for C2 and 7.51% for CS). According to our results, the existence of pig-to-pig transmission is consistent with our swine serological data. Thus, direct transmission may contribute to the epidemiological cycle of JE in Cambodia. These results need to be confirmed in other eco-climatic settings, in particular in temperate areas where pig-to-pig transmission may facilitate the persistence of JE virus (JEV) during cold seasons when there are no or few mosquitoes.

SUBMITTER: Diallo AOI

PROVIDER: S-EPMC6095498 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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How much does direct transmission between pigs contribute to Japanese Encephalitis virus circulation? A modelling approach in Cambodia.

Diallo Alpha Oumar II AOI Chevalier Véronique V Cappelle Julien J Duong Veasna V Fontenille Didier D Duboz Raphaël R

PloS one 20180816 8

Japanese Encephalitis (JE) is the most important cause of human encephalitis throughout Asia and the Pacific. Although JE is a vector-borne disease, it has been demonstrated experimentally that transmission between pigs can occur through direct contact. Whether pig-to-pig transmission plays a role in the natural epidemiological cycle of JE remains unknown. To assess whether direct transmission between pigs may occur under field conditions, we built two mathematical models of JE transmission inco ...[more]

PMID: 30114197

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Project description:Japanese encephalitis (JE) is a vector-borne zoonosis and the leading cause of human viral encephalitis in Asia. Its transmission cycle is usually described as involving wild birds as reservoirs and pigs as amplifying hosts. JE is endemic in Cambodia, where it circulates in areas with low pig densities (<70 pigs per km2), and could be maintained in a multi-host system composed of pigs, but also poultry as competent hosts, and dogs, cattle and humans as non-competent hosts. We used a mathematical model representing Japanese encephalitis virus (JEV) transmission in a traditional Cambodian village that we calibrated with field data collected in 3 districts of Kandal province, Cambodia. First, R0 calculations allowed us to assess the capacity of the epidemiological system to be invaded by JEV and sustain virus transmission in villages in the 3 districts, and we predicted human exposure at the epidemiological equilibrium, based on simulations. Changes in spatial density of livestock, in agricultural practices, and epizootics (e.g., African swine fever), can profoundly alter the composition of host communities, which could affect JEV transmission and its impact on human health. In a second step, we then used the model to analyse how host community composition affected R0 and the predicted human exposure. Lastly, we evaluated the potential use of dog JE seroprevalence as an indicator of human exposure to JEV. In the modeled villages, the calculated R0 ranged from 1.07 to 1.38. Once the equilibrium reached, predicted annual probability of human exposure ranged from 9% to 47%, and predicted average age at infection was low, between 2 and 11 years old, highlighting the risk of severe forms of JEV infection and the need to intensify child immunization. According to the model, increasing the proportion of competent hosts induced a decrease in age at infection. The simulations also showed that JEV could invade a multi-host system with no pigs, reinforcing the assumption of poultry acting as reservoirs. Finally, the annual human exposure probability appeared linearly correlated with dog seroprevalence, suggesting that in our specific study area, dog seroprevalence would be a good proxy for human exposure.

Project description:Japanese encephalitis (JE) is endemic in Cambodia, but circulation of JE virus (JEV) among domestic pigs has previously only been studied in the southern part of the country. The main purpose of this study was to determine the seroprevalence of JEV antibodies in smallholder pigs held in rural areas of Kampong Thom, Preah Vihear, Ratanakiri, and Stung Treng provinces, northeastern Cambodia. Another purpose was to identify possible associations between serologic status and other factors, such as reproductive disorders, and to investigate the farmers' knowledge of mosquito-borne diseases and use of preventive measures. In October 2019, 139 households were visited throughout the study area, and 242 pigs were sampled for blood. The sera were analysed with ELISA for JEV antibodies. Household representatives were interviewed, and data were recorded for each sampled pig. The apparent seroprevalence was 89.1% in pigs between 3 and 6 months of age, and 100% in pigs over 6 months of age. In total, 93.0% of the pigs tested positive. Province appeared to be the only factor significantly associated with serologic status (p < 0.001). Almost all (97.8%) respondents knew that mosquitos could transmit diseases, and 70.5% had heard of JE. However, only one respondent knew that JEV is transmitted to people through mosquito bites. Very few respondents knew that pigs can become infected with JEV, and no one knew that mosquitos transmit the virus. All families used some sort of mosquito protection for themselves, but only 15.1% protected their pigs from mosquito bites. The children were vaccinated against JE in 93 households, while adults only were vaccinated in eight households. The results suggest that JEV transmission is intense in northeastern Cambodia, and that people's knowledge about the transmission route of JEV and the role of pigs in the transmission cycle is low. Fortunately, people are well aware of mosquito-borne diseases in general and use mosquito protection, and many children are vaccinated against JE. Nonetheless, it is important that national vaccination is continued, and that people-especially in rural areas where pigs are commonly kept-are educated on the ecology and transmission of JEV.

Project description:Mosquito-borne flaviviruses with an enzootic transmission cycle like Japanese encephalitis virus (JEV) and West Nile virus (WNV) are a major public health concern. The circulation of JEV in Southeast Asia is well-documented, and the important role of pigs as amplification hosts for the virus is long known. The influence of other domestic animals especially poultry that lives in high abundance and close proximity to humans is not intensively analyzed. Another understudied field in Asia is the presence of the closely related WNV. Such analyses are difficult to perform due to the intense antigenic cross-reactivity between these viruses and the lack of suitable standardized serological assays. The main objective of this study was to assess the prevalence of JEV and WNV flaviviruses in domestic birds, detailed in chickens and ducks, in three different Cambodian provinces. We determined the flavivirus seroprevalence using an hemagglutination inhibition assay (HIA). Additionally, we investigated in positive samples the presence of JEV and WNV neutralizing antibodies (nAb) using foci reduction neutralization test (FRNT). We found 29% (180/620) of the investigated birds positive for flavivirus antibodies with an age-depended increase of the seroprevalence (OR = 1.04) and a higher prevalence in ducks compared to chicken (OR = 3.01). Within the flavivirus-positive birds, we found 43% (28/65) with nAb against JEV. We also observed the expected cross-reactivity between JEV and WNV, by identifying 18.5% double-positive birds that had higher titers of nAb than single-positive birds. Additionally, seven domestic birds (10.7%) showed only nAb against WNV and no nAb against JEV. Our study provides evidence for an intense JEV circulation in domestic birds in Cambodia, and the first serological evidence for WNV presence in Southeast Asia since decades. These findings mark the need for a re-definition of areas at risk for JEV and WNV transmission, and the need for further and intensified surveillance of mosquito-transmitted diseases in domestic animals.

Dataset Information

How much does direct transmission between pigs contribute to Japanese Encephalitis virus circulation? A modelling approach in Cambodia.

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How much does direct transmission between pigs contribute to Japanese Encephalitis virus circulation? A modelling approach in Cambodia.

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