Pathogen Spillover to an Invasive Tick Species: First Detection of Bourbon Virus in Haemaphysalis longicornis in the United States

Cumbie, Alexandra N.; Trimble, Rebecca N.; Eastwood, Gillian

doi:10.3390/pathogens11040454

Cited by 46 publications

(50 citation statements)

References 47 publications

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“…In its native range, this species is a vector for a suite of human pathogens, including severe fever with thrombocytopenia syndrome virus (SFTSV; [ 33 ]) and Japanese spotted fever [ 34 ]. Longhorned ticks have also been demonstrated to be competent for Bourbon virus [ 35 ] and Heartland bandavirus, a virus genetically similar to SFTSV, with both primarily vectored by the lone star tick [ 36 ].…”

Section: Introductionmentioning

confidence: 99%

Risk of tick-borne pathogen spillover into urban yards in New York City

2022

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Background The incidence of tick-borne disease has increased dramatically in recent decades, with urban areas increasingly recognized as high-risk environments for exposure to infected ticks. Green spaces may play a key role in facilitating the invasion of ticks, hosts and pathogens into residential areas, particularly where they connect residential yards with larger natural areas (e.g. parks). However, the factors mediating tick distribution across heterogeneous urban landscapes remain poorly characterized. Methods Using generalized linear models in a multimodel inference framework, we determined the residential yard- and local landscape-level features associated with the presence of three tick species of current and growing public health importance in residential yards across Staten Island, a borough of New York City, in the state of New York, USA. Results The amount and configuration of canopy cover immediately surrounding residential yards was found to strongly predict the presence of Ixodes scapularis and Amblyomma americanum, but not that of Haemaphysalis longicornis. Within yards, we found a protective effect of fencing against I. scapularis and A. americanum, but not against H. longicornis. For all species, the presence of log and brush piles strongly increased the odds of finding ticks in yards. Conclusions The results highlight a considerable risk of tick exposure in residential yards in Staten Island and identify both yard- and landscape-level features associated with their distribution. In particular, the significance of log and brush piles for all three species supports recommendations for yard management as a means of reducing contact with ticks. Graphical Abstract

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Section: Introductionmentioning

confidence: 99%

Risk of tick-borne pathogen spillover into urban yards in New York City

2022

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“…In both its endemic and invaded ranges, H. longicornis can acquire and carry pathogens of human importance, including the agents causing Lyme disease and spotted fever group rickettsiosis ( Qin et al 2019 , Zhao et al 2020 , Price et al 2021a ). Their broad host range coupled with habitat overlap and high prevalence of co-feeding with native vector tick species could facilitate pathogen acquisition and spillover, as recently described for arboviruses ( Price et al 2021b , Tufts et al 2021 , White et al 2021 , Cumbie et al 2022 ). However, important factors in pathogen transmission risk, including blood-feeding behavior and engorgement dynamics, remain poorly documented in natural field conditions ( Piesman 1993 , Tahir et al 2020 ).…”

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confidence: 97%

Recovery of Partially Engorged Haemaphysalis longicornis (Acari: Ixodidae) Ticks from Active Surveillance

Price

Witmier

Eckert

et al. 2022

Journal of Medical Entomology

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The invasive Asian longhorned tick, Haemaphysalis longicornis, has rapidly spread across the northeastern United States and is associated with pathogens of public health and veterinary concern. Despite its importance in pathogen dynamics, H. longicornis blood-feeding behavior in nature, specifically the likelihood of interrupted feeding, remains poorly documented. Here, we report the recovery of partially engorged, questing H. longicornis from active tick surveillance in Pennsylvania. Significantly more engorged H. longicornis nymphs (1.54%) and adults (3.07%) were recovered compared to Ixodes scapularis nymphs (0.22%) and adults (zero). Mean Scutal Index difference between unengorged and engorged nymph specimens was 0.65 and 0.42 for I. scapularis and H. longicornis, respectively, suggesting the questing, engorged H. longicornis also engorged to a comparatively lesser extent. These data are among the first to document recovery of engorged, host-seeking H. longicornis ticks and provide initial evidence for interrupted feeding and repeated successful questing events bearing implications for pathogen transmission and warranting consideration in vector dynamics models.

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“…A recent laboratory study showed that H. longicornis is capable of transovarially transmitting Heartland virus, the North American relative to Dabie bandavirus (Raney et al, 2022). Another study confirmed the presence of viral RNA from Bourbon virus (Family: Orthomyxoviridae, Genus: Thogotovirus) in field-collected H. longicornis in Virginia (Cumbie et al, 2022). The present study assesses the vector competence of H. longicornis for the North American tick-borne flavivirus, Powassan virus (POWV; Family: Flaviviridae, Genus: Flavivirus).…”

Section: Introductionmentioning

confidence: 93%

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

Raney

Herslebs

Langohr

et al. 2022

Front. Cell. Infect. Microbiol.

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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.

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Pathogen Spillover to an Invasive Tick Species: First Detection of Bourbon Virus in Haemaphysalis longicornis in the United States

Cited by 46 publications

References 47 publications

Risk of tick-borne pathogen spillover into urban yards in New York City

Risk of tick-borne pathogen spillover into urban yards in New York City

Recovery of Partially Engorged Haemaphysalis longicornis (Acari: Ixodidae) Ticks from Active Surveillance

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

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