Little pig, little pig, let me come in: The influence of landscape structure and La Niña climatic anomalies on the emergence of Japanese encephalitis virus in Australian piggeries in 2022

Abstract

The widespread activity of Japanese encephalitis virus (JEV) in previously unaffected regions of eastern and southern Australia in 2022 represents the most significant local arbovirus emergency in almost 50 years. Japanese encephalitis virus is transmitted by mosquitoes and maintained in wild ardeid birds and amplified in pigs, the latter of which suffer significant reproductive losses as a result of infection. The landscape of JEV outbreak risk in mainland Australia is almost entirely unknown, particularly in the eastern and southern parts of the country where the virus has not been previously documented. Although other areas with endemic JEV circulation in the Indo-Pacific region have demonstrated the importance of wild waterbird-livestock interface in agricultural-wetland mosaics, no such investigation has yet determined the configuration of pathogenic landscapes for Australia. Moreover, the recent emergence in Australia has followed substantial precipitation and temperature anomalies associated with the La Niña phase of the El Niño Southern Oscillation. This study investigated the landscape epidemiology of JEV outbreaks in Australian piggeries recorded between January and April of 2022 to determine the influence of ardeid habitat suitability, hydrogeography, hydrology, land cover and La Niña-associated climate anomalies in demarcating risk. Outbreaks of JEV in domestic pigs were associated with ardeid species richness, agricultural and riparian landscape mosaics, hydrological flow accumulation, and grasslands. This study has identified the composition and configuration of landscape features that delineated risk for piggeries during the 2022 emergence of JEV in Australia. Although preliminary, these findings can inform actionable strategies for the development of new One Health JEV surveillance specific to the needs of Australia.

Landscapes associated with Japanese encephalitis virus reflect the functional biogeography of waterbird species across Australia and the Central Indo-Pacific region

“…Australian piggery outbreaks (N = 54) reported to the World Organisation for Animal Health (WOAH) by the Australian government between 19 January, 2022 and 4 April, 2022(42) have been described in a previous epidemiological investigation (10). Briefly, outbreak occurrence was defined as one or more cases reported at the level of the piggery.…”

“…All 14 species of ardeid birds extant in mainland Australia were modelled using the GBIF data (Table S1). The modelling of habitat suitability for these species has been previously described (10).…”

“…Adjusted individual species presence at landscape-scale was computed by applying interspecific biotic constraints at a scale of 5 arc minutes (~ 10 km), which was the scale of piggery outbreak reporting as well as the scale at which key landscape structure influencing outbreak occurrence was previously described (10). These biotic constraints were based on spatially-explicit species assemblage modelling (SESAM) to adjust each species' habitat suitability estimate by sympatric species (80)(81)(82).…”

“…It has been hypothesised that the anomalous La Niña-associated weather patterns may have contributed to the widespread distribution of JEV outbreaks in 2022 due to modulation of the distribution of vector populations or maintenance host populations (8). Notably, an extensive investigation of landscape composition and configuration and La Niña-associated anomalies showed that landscape structure was substantially more influential to outbreak occurrence than were specific precipitation or temperature anomalies associated with La Niña (10). However, certain aspects of high-risk landscape structure, such as the composition of transient wetlands and the propensity to flooding, would also have been affected by both proximal and distal precipitation events, and so La Niña-associated weather anomalies may have influenced outbreak occurrence indirectly, particularly if the influence varied by scale.…”

“…Japanese encephalitis virus circulates in wild ardeid bird maintenance hosts (11)(12)(13)(14)(15)(16)(17) vectored by mosquitoes (primarily Culex annulirostris in Australia (18)) and can spillover to pigs (19)(20)(21)(22)(23)(24) and humans, which are competent and non-competent hosts, respectively. Previous work has examined the distribution of ardeid species richness as a key nidus of the maintenance community, identifying a strong quadratic relationship between richness and JEV piggery outbreak occurrence, whereby intermediate richness was associated with greatest risk (10). Nevertheless, neither the association between outbreaks and individual species, nor the influence of the structure and functional distribution of species assemblages were assessed with respect to the 2022 piggery outbreaks in Australia, and the latter has not been assessed with respect to outbreaks anywhere in the Indo-Pacific region to date.…”