Unique humoral immune response of pigs to repeated natural Japanese encephalitis virus infections: an amplifying host perspective

Abstract

Japanese encephalitis virus (JEV) is the leading cause of viral encephalitis in the Asia-Pacific region. Amplification of JEV in pigs is a potent driver for spillover of the infection to humans, and hence monitoring of virus dynamics in pigs can provide insights into JEV ecology. To study the dynamics of natural JEV infection in a tropical region, two groups of immunologically naïve pigs consisting of six animals per group were kept as sentinels on two different farms in the district of Thanjavur, Tamil Nadu, India. In a longitudinal study conducted from May 2022 to October 2023, nested RT-PCR and indirect ELISA were used to track the dynamics of JEV and the humoral response in pigs. Synchronous and asynchronous seroconversion in pigs was recorded on two different farms with different management practices. Repeated infections with JEV were recorded in all of the sentinel animals throughout the study period, irrespective of the season. Phylogenetic analysis revealed the presence of JEV genotype III in the region. It was observed that the IgG response to natural JEV infection did not last long, which might have been the reason for repeated infections in the sentinel animals. The longest period during which IgG was present at detectable levels in this study was two months, after which the pigs could once again amplify the virus. A significant positive correlation was found between wind speed and JEV incidence in sentinel animals. Our results offer a different perspective on the relationship between JEV and its amplifying host that contradicts the assumption that pre-immune pigs are resistant to JEV amplification. Our findings could have a major impact on our understanding of the ecology of JEV in tropical regions, where there is a high burden of JE despite coordinated prevention efforts that have relied on achieving a long-lasting immune response.