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      Australian vertebrate hosts of Japanese encephalitis virus; a review of the evidence

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          Abstract

          Japanese Encephalitis Virus (JEV) transmission in temperate Australia has underscored a critical need to characterise transmission pathways and identify probable hosts of infection within the country. This systematic review consolidates existing research on the vertebrate hosts of JEV that are known to exist in Australia. Specifically, we aim to identify probable species for JEV transmission, their potential role as either a spillover or maintenance host and identify critical knowledge gaps. Data were extracted from studies involving experimental infection, seroprevalence, and virus isolation and were available for 22 vertebrate species known to reside in Australia. A host competence score was calculated to assess the potential for a given species to infect JEV vectors and to quantity their possible role in JEV transmission. Based on the host competence score and ecology of each species, we find ardeid birds, feral pigs, and flying foxes have potential as maintenance hosts for JEV in the Australian context. We also note that brushtail possums and domestic pigs have potential as spillover hosts under certain outbreak conditions. However, evidence to confirm these roles in localized transmission or outbreaks is sparse, emphasizing the need for further targeted research. This review provides a foundation for future investigations into JEV transmission in Australia, advocating for enhanced surveillance and standardized research methodologies to better understand and mitigate the virus’s impact.

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          Japanese encephalitis virus infection, diagnosis and control in domestic animals.

          Japanese encephalitis virus (JEV) is a significant cause of neurological disease in humans throughout Asia causing an estimated 70,000 human cases each year with approximately 10,000 fatalities. The virus contains a positive sense RNA genome within a host-derived membrane and is classified within the family Flaviviridae. Like many flaviviruses, it is transmitted by mosquitoes, particularly those of the genus Culex in a natural cycle involving birds and some livestock species. Spill-over into domestic animals results in a spectrum of disease ranging from asymptomatic infection in some species to acute neurological signs in others. The impact of JEV infection is particularly apparent in pigs. Although infection in adult swine does not result in symptomatic disease, it is considered a significant reproductive problem causing abortion, still-birth and birth defects. Infected piglets can display fatal neurological disease. Equines are also infected, resulting in non-specific signs including pyrexia, but occasionally leading to overt neurological disease that in extreme cases can lead to death. Veterinary vaccination is available for both pigs and horses. This review of JEV disease in livestock considers the current diagnostic techniques available for detection of the virus. Options for disease control and prevention within the veterinary sector are discussed. Such measures are critical in breaking the link to zoonotic transmission into the human population where humans are dead-end hosts.
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            An outbreak of Japanese encephalitis in the Torres Strait, Australia, 1995.

            To determine the distribution of virus infection during an outbreak of Japanese encephalitis (JE) in the Torres Strait, and to describe the environmental factors facilitating the outbreak. Human and porcine serological surveys for JE virus activity throughout the Torres Strait, and mosquito and household surveys on the island of Badu. The island of Badu (where the clinical cases occurred) and the other islands of the Torres Strait, Australia, during April-May 1995. The serological surveys identified recent JE virus infection among residents or domestic pigs on at least nine outer Torres Strait islands. A JE virus, confirmed by nucleotide sequencing, was isolated from two asymptomatic Badu residents. Virus isolations and mosquito surveys implicated Culex annulirostris as the major vector involved in the outbreak. There was prolific Cx. annulirostris breeding in a variety of water bodies close to and within the Badu community. Over half (53%) of the households kept pigs in pens, and many (63%) of the pigpens were situated near standing water; in 56% of these "wet" pigpens Cx. annulirostris was breeding. There was evidence of widespread JE virus activity throughout the outer islands of the Torres Strait. We suggest that migratory birds and/or wind-blown mosquitoes could have imported the virus into the Torres Strait from a focus of viral activity, possibly in Papua New Guinea, thereby initiating the outbreak. A combination of environmental factors, with large numbers of domestic pigs in close proximity to human dwellings and mosquito breeding sites, undoubtedly facilitated the outbreak on Badu.
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              Japanese encephalitis in north Queensland, Australia, 1998.

              To describe the circumstances of two cases of Japanese encephalitis (JE) in north Queensland in 1998, including one acquired on the Australian mainland. Serological surveillance of sentinel pigs for JE virus activity; serological surveys of humans and pigs and viral cultures of mosquito collections. Islands in the Torres Strait and communities in the Northern Peninsula Area (NPA) and near the mouth of the Mitchell River in Cape York, Queensland, in the 1998 wet season (December 1997-May 1998). Sentinel pigs in the Torres Strait began to seroconvert to JE virus in February 1998, just before onset of JE in an unvaccinated 12-year-old boy on Badu island. By mid-April, most sentinel pigs had seroconverted. Numerous JE viruses were isolated from Culex annulirostris mosquitoes collected on Badu. In early March, a person working at the mouth of the Mitchell River developed JE. Serological surveys showed recent JE virus infection in 13 young pigs on a nearby farm, but not in 488 nearby residents. In NPA communities, sentinel pigs seroconverted slowly and JE viruses were isolated from three, but none of 604 residents showed evidence of recent infection. Nucleotide sequencing showed that 1998 JE virus isolates from the Torres Strait were virtually identical not only to the 1998 isolate from an NPA pig, but also to previous (1995) Badu isolates. JE virus activity was more widespread in north Queensland in the 1998 wet season than in the three previous wet seasons, but ecological circumstances (e.g., less intensive pig husbandry, fewer mosquitoes) appear to have limited transmission on the mainland. Nucleotide sequencing indicated a common source for the 1995 and 1998 JE viruses. Circumstantial evidence suggests that cyclonic winds carried infected mosquitoes from Papua New Guinea.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: methodologyRole: formal analysisRole: writing—original draft preparationRole: writing—review and editing
                Role: ConceptualizationRole: methodologyRole: formal analysisRole: writing—review and editing
                Role: formal analysisRole: writing—review and editing
                Role: formal analysisRole: writing—review and editing
                Role: ConceptualizationRole: writing—review and editing
                Role: ConceptualizationRole: writing—review and editing
                Role: ConceptualizationRole: methodologyRole: formal analysisRole: writing—review and editing
                Journal
                bioRxiv
                BIORXIV
                bioRxiv
                Cold Spring Harbor Laboratory
                26 April 2024
                : 2024.04.23.590833
                Affiliations
                [a ]Centre for Planetary Health and Food Security, Griffith University, Gold Coast, QLD 4222, Australia
                [b ]Harvard Medical School, Boston, MA 02115, USA
                [c ]CSIRO, Health and Biosecurity, Brisbane, QLD 4102, Australia
                [d ]Department of Biology, Stanford University, Stanford, CA 94305, USA
                Author notes

                Author Contributions:

                All authors have read and agreed to the published version of the manuscript.

                [* ]Corresponding author: kevin.moore@ 123456griffithuni.edu.au
                Author information
                http://orcid.org/0000-0003-0712-2222
                http://orcid.org/0000-0003-0687-4852
                http://orcid.org/0009-0001-3014-0245
                http://orcid.org/0000-0002-6336-0826
                http://orcid.org/0000-0002-3493-0412
                http://orcid.org/0000-0002-7244-4044
                http://orcid.org/0000-0002-9032-2710
                Article
                10.1101/2024.04.23.590833
                11071400
                38712158
                ad5e08da-7696-445d-80a3-784e811a0301

                This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.

                History
                Funding
                K.T.M. was supported by a Griffith University Postgraduate Research Scholarship. T.S.A. was supported by the National Institute of General Medical Sciences under grant number T32GM144273. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of General Medical Sciences or the National Institutes of Health. E.B.S. was supported by the National Institutes of Health (grant no. R35GM133439).
                Categories
                Article

                host competence,maintenance host,spillover host,transmission cycle,experimental infection,viraemia

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