Comparison of Japanese Encephalitis Force of Infection in Pigs, Poultry and Dogs in Cambodian Villages

Abstract

Japanese encephalitis virus (JEV) is the main cause of human viral encephalitis in Asia, with a mortality rate reaching 30%, mostly affecting children. The traditionally described cycle involving wild birds as reservoirs, pigs as amplifying hosts and Culex mosquitoes as vectors is questioned, with increasing evidence of a more complex multi-host system involved in areas where densities of pigs are low, such as in Cambodia. In 2018, we examined pigs, chickens, ducks and dogs from Kandal province, Cambodia, for antibody response against JEV by hemagglutination inhibition and virus neutralization assays. Forces of infection (FOI) for flaviviruses and JEV were estimated per species and per unit of body surface area (BSA). JEV seroprevalence reached 31% (95% CI: 23–41%) in pigs, 1% (95% CI: 0.1–3%) in chickens, 12% (95% CI: 7–19%) in ducks and 35% (95% CI: 28–42%) in dogs. Pigs were most likely to be infected (FOI: 0.09 per month), but the FOI was higher in ducks than in pigs for a given BSA (ratio of 0.13). Dogs had a lower FOI than ducks but a higher FOI than chickens (0.01 per month). For a given BSA, dogs were less likely to be infected than pigs (ratio of 1.9). In Cambodia, the virus may be circulating between multiple hosts. Dogs live in close contact with humans, and estimating their exposure to JEV infection could be a relevant indicator of the risk for humans to get infected, which is poorly known due to underdiagnosis. Understanding the JEV cycle and developing tools to quantify the exposure of humans is essential to adapt and support control measures for this vaccine-preventable disease.

Host-Feeding Preference and Diel Activity of Mosquito Vectors of the Japanese Encephalitis Virus in Rural Cambodia

“…Experimentally, infected dogs showed very low viremia suggesting that dogs are not involved in JEV circulation [ 79 ]. However, dogs live alongside humans and, as suggested by the results of a serological survey carried out in the same area [ 11 ], they could be a relevant indicator of the risk for humans to get infected by JEV. In Kandal province where the present survey was carried out, the dog/human ratio was estimated to be 1:4 on average (V. Chevalier, pers.com on 20 January 2021).…”

“…The historically described JEV cycle involves water birds as wild reservoir, pigs as amplifying hosts [ 4 , 5 , 6 ], and mosquito species as vectors [ 7 , 8 ]. Domestic birds are suspected to be secondary reservoir hosts [ 9 , 10 , 11 ]. Proximity to rice fields and pig rearing, particularly backyard farming, have been identified as major risk factors of JE in humans [ 12 , 13 ].…”

“…Genetically determined factors, environment and host availability impact feeding behavior of Culex mosquitoes [ 49 , 50 ]. Although pigs are central in the JE transmission, there is evidence that JEV virus can circulate in low pig density areas, suggesting the existence of secondary reservoirs such as domestic birds [ 4 , 10 , 11 ]. In these areas, the maintenance of JE could be facilitated by a multi-host system composed of pigs, ducks, chickens and vector populations exhibiting opportunistic feeding patterns [ 11 ].…”

Changes in Rice and Livestock Production and the Potential Emergence of Japanese Encephalitis in Africa

“…I focus only on pigs as competent hosts and provide reasoning for this in the Methods. While there are data to indicate domestic birds may be important to transmission [ 26 , 27 ], there are few studies that have quantified the necessary parameters to properly implicate domestic birds or assess their relative importance to transmission in contexts with and without pigs. This has already been raised as a gap in JE research [ 14 ].…”

“…The focus on pigs and cattle only is based on: (i) the innate host preference for primary JEV vectors for cattle and the absence of similar data for domestic birds from field experiments; and (ii) the absence of large-scale duck farming in the majority of African countries, as established based on FAO data. Of the few studies that focus on the potential contribution of domestic birds, Ladreyt [ 27 ] estimated the force of infection on ducks as 0.03 per month and chickens as 0.003. While chickens produce viremia sufficient to infect mosquitoes [ 26 ], there is not convincing evidence that sufficient blood meals on chickens occur to support transmission.…”