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Jamestown Canyon virus in Massachusetts: clinical case series and vector screening.

ABSTRACT: Jamestown Canyon virus (JCV) is a neuroinvasive arbovirus that is found throughout North America and increasingly recognized as a public health concern. From 2004 to 2012, an average of 1.7 confirmed cases were reported annually in the United States, whereas from 2013 to 2018 this figure increased over seventeen-fold to 29.2 cases per year. The rising number of reported human infections highlights the need for better understanding of the clinical manifestations and epidemiology of JCV. Here, we describe nine patients diagnosed with neuroinvasive JCV infection in Massachusetts from 2013, the year of the first reported case in the state, to 2017. Because current diagnostic testing relies on serology, which is complicated by cross-reactivity with related orthobunyaviruses and can be negative in immunosuppressed patients, we developed and evaluated an RT-qPCR assay for detection of JCV RNA. We tested this on the available archived serum from two patients, but did not detect viral RNA. JCV is transmitted by multiple mosquito species and its primary vector in Massachusetts is unknown, so we additionally applied the RT-qPCR assay and confirmatory RNA sequencing to assess JCV prevalence in a vector candidate, Ochlerotatus canadensis. We identified JCV in 0.6% of mosquito pools, a similar prevalence to neighboring Connecticut. We assembled the first Massachusetts JCV genome directly from a mosquito sample, finding high identity to JCV isolates collected over a 60-year period. Further studies are needed to reconcile the low vector prevalence and low rate of viral evolutionary change with the increasing number of reported cases.

SUBMITTER: Kinsella CM

PROVIDER: S-EPMC7273174 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Jamestown Canyon virus (JCV), a negative-sense arbovirus, is increasingly common in the upper Midwest of the USA. Transmitted by a range of mosquito genera, JCV's primary amplifying host is white-tailed deer. Aedes aegypti is responsible for transmitting various positive-sense viruses globally including dengue (DENV), Zika, chikungunya, and Yellow Fever. Ae. aegypti's distribution, once confined to the tropics, is expanding, in part due to climate change. Wolbachia, an insect endosymbiont, limits the replication of co-infecting viruses inside insects. The release and spread of the symbiont into Ae. aegypti populations have been effective in reducing transmission of DENV to humans, although the mechanism of Wolbachia-mediated viral blocking is still poorly understood. Here we explored JCV infection potential in Ae. aegypti, the nature of the vector's immune response, and interactions with Wolbachia infection. We show that Ae. aegypti is highly competent for JCV, which grows to high loads and rapidly reaches the saliva after an infectious blood meal. The mosquito immune system responds with strong induction of RNAi and JAK/STAT. Neither the direct effect of viral infection nor the energetic investment in immunity appears to affect mosquito longevity. Wolbachia infection blocked JCV only in the early stages of infection. Wolbachia-induced immunity was small compared to that of JCV, suggesting innate immune priming does not likely explain blocking. We propose two models to explain why Wolbachia's blocking of negative-sense viruses like JCV may be less than that of positive-sense viruses, relating to the slowdown of host protein synthesis and the triggering of interferon-like factors like Vago. In conclusion, we highlight the risk for increased human disease with the predicted future overlap of Ae. aegypti and JCV ranges. We suggest that with moderate Wolbachia-mediated blocking and distinct biology, negative-sense viruses represent a fruitful comparator model to other viruses for understanding blocking mechanisms in mosquitoes.

Project description:During the summers of 2017-2019, 60 human cases of Jamestown Canyon virus-associated disease were reported in the State of Wisconsin, U.S.A; by comparison, there were 28 cases in the 5 years prior. Jamestown Canyon virus (JCV, Peribunyaviridae: Orthobunyavirus) is a zoonotic, mosquito-borne virus that is endemic throughout North America. The proposed transmission cycle for JCV involves horizontal transmission by a variety of mammal-feeding mosquito species and deer hosts, and transseasonal maintenance by vertical transmission in Aedes mosquito species. Although some of the earliest work on JCV transmission and disease was done in Wisconsin (WI), little is known about the spectrum of mosquitoes that are currently involved in transmission and maintenance of JCV, which is key to inform the approach to control and prevent JCV transmission, and to understand why case numbers have increased dramatically in recent years. Therefore, we undertook an intensive surveillance effort in Sawyer and Washburn counties, WI between April and August of 2018 and 2019, in an area with a concentration of JCV human cases. Larval and adult stages of mosquitoes were surveyed using larval dippers and emergence traps, light traps, resting boxes, a Shannon-style trap, and backpack aspirator. In total, 14,949 mosquitoes were collected in 2018, and 28,056 in 2019; these specimens represent 26 species in 7 genera. Suspect vector species were tested for JCV by polymerase chain reaction (PCR); of 23 species that were tested, only Aedes provocans yielded JCV positive results. In 2018, a single pool of Ae. provocans tested positive. In 2019, with more focused early season surveillance, we detected JCV in 4 pools of adult mosquitoes, and one pool that consisted of lab-raised adults that were collected as larvae. Material from all of these PCR-positive samples also yielded infectious virus in cell culture. Overall, these data provide new insight into the seasonality and habitat preferences for 26 mosquito species in Northern WI, which will be useful to inform future surveillance efforts for JCV. The results underscore the importance of Ae. provocans as a vector species involved in transseasonal maintenance of JCV in this region.

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Jamestown Canyon virus in Massachusetts: clinical case series and vector screening.

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