Horizontal and Vertical Transmission of Powassan Virus by the Invasive Asian Longhorned Tick, Haemaphysalis longicornis, Under Laboratory Conditions

Abstract

The Asian longhorned tick, Haemaphysalis longicornis, is an ixodid tick native to East Asia that was first detected in North America outside a port of entry in 2017. This invasive species has since been detected in 17 states. As the invasive range of the tick continues to expand, the vector competence of H. longicornis for pathogens native to North America must be assessed. Here, we evaluate the vector competence of H. longicornis for Powassan virus (POWV) under laboratory conditions. POWV is a North American tick-borne flavivirus that is typically transmitted through the bite of Ixodes species ticks. The invasive range of H. longicornis is expected to overlap heavily with the geographic range of Ixodes scapularis and POWV cases, highlighting the potential for this invasive tick species to amplify POWV transmission in natural foci should the native tick vectors and H. longicornis share similar hosts. In these studies, adult female H. longicornis ticks were infected with POWV via anal pore microinjection. Viral RNA and infectious virions were detected in tick tissues via q‐RT‐PCR and focus‐forming assay, respectively. POWV‐injected female ticks were infested on mice, and virus was transmitted to mice during tick feeding, as shown by clinical signs of disease and seroconversion in the tick-exposed mice, as well as the detection of viral RNA in various mouse tissues. A POWV-injected female tick transmitted virus to her larval progeny, indicating that H. longicornis can vertically transmit POWV. These naturally-infected larval ticks were also able to transmit POWV to the mouse on which they fed and to the nymphal stage after molting, further demonstrating that H. longicornis can transmit POWV in the horizontal and transstadial modes. Larval and nymphal ticks were also orally infected with POWV while feeding on viremic mice. Additionally, this study provides the first report of POWV neuropathology based on a natural tick transmission model of POWV. Together, our results suggest that the invasive H. longicornis tick is a competent vector of POWV. These findings underline the growing danger this tick may pose to human health in the United States. Additional scholarship on the tick’s biology, ecology, and pathogen transmission dynamics in nature will be important towards understanding the full public health impact of this invasive species.

Towards modelling tick-virus interactions using the weakly pathogenic Sindbis virus: Evidence that ticks are competent vectors

“…Research on TBPs has focused on studying the interactions between ticks and bacteria ( Khanal et al., 2017 ; Taank et al., 2018 ; Dahmani et al., 2020 ; Kurokawa et al., 2020 ; Ramasamy et al., 2020 ) while we are in the early stages of our understanding of tick-virus interactions ( Mansfield et al., 2017a ; Damian et al., 2020 ; Maqbool et al., 2022 ; Migné et al, 2022 ). Most TBVs are virulent and the requirements for biosafety research are high, which severely restricts and hinders relevant basic research on TBVs ( Kaiser, 2008 ; He et al., 2010 ; Maffioli et al., 2014 ; Adouchief et al., 2016 ; Grabowski et al., 2016 ; Grabowski and Hill, 2017 ; Kazimirová et al., 2017 ; Mansfield et al., 2017b ; Grabowski et al., 2018 ; Shi et al., 2018 ; Zhuang et al., 2018 ; Kemenesi and Banyai, 2019 ; Salata et al., 2021 ; Ahmed et al., 2022 ; Maqbool et al., 2022 ; Raney et al., 2022 ).…”

An established population of Asian longhorned ticks (Acari: Ixodidae) in Ohio, USA

“…Within the United States, field-collected ALTs have tested positive for the agents of Lyme disease, Borrelia burgdorferi sensu stricto (Price et al 2021), human granulocytic anaplasmosis, Anaplasma phagocytophilum (AP-ha) (Price et al 2022), and Bourbon virus disease (Cumbie et al 2022). Under laboratory conditions, the ALT can transmit Rickettsia rickettsii , the causative agent of Rocky Mountain spotted fever (Stanley et al 2020), Powassan virus (Raney et al 2022a), and Heartland virus (Raney et al 2022b), but to date, no field-collected ALT have tested positive for these agents.…”

Management of Haemaphysalis longicornis (Acari: Ixodidae) on a cow–calf farm in East Tennessee, USA

“…This species biology and life history make it essential to manage quickly because of its parthenogenic reproductive strategies, rapid population growth, and use of multiple host species for blood feeding and dispersal (Heath 2016). Questing ticks in the field have been identified with Bourbon virus (Cumbie et al 2022), and laboratory reports indicate that the US field-collected populations can transmit Rickettsia rickettsii (Stanley et al 2020) and Powassan virus (Raney et al 2022). Importantly, this species is also capable of transmitting additional pathogens found in its native and exotic ranges outside of the United States (reviewed in Beard et al 2018).…”