Surveillance and Genetic Analysis of Jamestown Canyon Virus in New York State: 2001–2022

Kiet A. Ngo New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;

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Joseph G. Maffei New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;

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Cheri A. Koetzner New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;

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Steven D. Zink New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;

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Anne F. Payne New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;

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P. Bryon Backenson New York State Department of Health, Bureau of Communicable Disease Control, Albany, New York;

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Jennifer L. White New York State Department of Health, Bureau of Communicable Disease Control, Albany, New York;

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Alan P. Dupuis II New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;

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Laura D. Kramer New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;
Department of Biomedical Sciences, School of Public Health, State University of New York at Albany, Rensselaer, New York

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Alexander T. Ciota New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, New York;
Department of Biomedical Sciences, School of Public Health, State University of New York at Albany, Rensselaer, New York

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ABSTRACT.

Jamestown Canyon virus (JCV) (Peribunyavirdae; Orthobunyavirus) is a mosquito-borne pathogen endemic to North America. The genome is composed of three segmented negative-sense RNA fragments designated as small, medium, and large. Jamestown Canyon virus is an emerging threat to public health, and infection in humans can cause severe neurological diseases, including encephalitis and meningitis. We report JCV mosquito surveillance data from 2001 to 2022 in New York state. Jamestown Canyon virus was detected in 12 mosquito species, with the greatest prevalence in Aedes canadensis and Anopheles punctipennis. Detection fluctuated annually, with the highest levels recorded in 2020. Overall, JCV infection rates were significantly greater from 2012 to 2022 compared with 2001 to 2011. Full-genome sequencing and phylogenetic analysis were also performed with representative JCV isolates collected from 2003 to 2022. These data demonstrated the circulation of numerous genetic variants, broad geographic separation, and the first identification of lineage B JCV in New York state in 2022.

Jamestown Canyon virus (JCV) (Peribunyavirdae; Orthobunyavirus) belongs to the California serogroup of viruses that are known to cause human disease, including La Crosse virus (LACV) and Snowshoe hare virus (SSHV).1 The genome is negative-sense, single-stranded RNA composed of three segments—small (S), medium (M), and large (L)—that are approximately 1, 4.5, and 7 kilobases in size, respectively. The S segment encodes the nucleocapsid, whereas the M segment encodes the two structural glycoproteins; the L segment encodes the RNA-dependent RNA polymerase.

Jamestown Canyon virus was originally isolated from Culiseta inornata collected in Jamestown, Colorado, in 1961 and has since been isolated throughout North America.2,3 The virus has been found in numerous mosquito species, and white-tailed deer (WTD) (Odocoileus virginianus) have been implicated as the primary amplifying host.4,5 Approximately 55% of hunter-harvested WTD throughout New York state between 2007 and 2015 were found to be seropositive for JCV.6 Jamestown Canyon virus can be transmitted by mosquitoes both vertically and horizontally.7

Although most JCV infections in humans are generally asymptomatic or result in a mild febrile illness, severe infections can lead to encephalitis or meningitis. Neuroinvasive cases have been reported throughout the United States and Canada.8,9 In the past 6 years, there have been at least seven deaths linked to JCV infection in humans.8

We tested mosquito pools collected in New York state for JCV from 2001 to 2022, and we completed full-genome sequencing and phylogenetic analysis for 32 JCV isolates collected from 2003 to 2022.

Adult mosquitoes were collected using CDC light traps, identified by species, pooled (10–60 individuals), and processed as described previously.10 RNA extraction was performed as described previously10 and was tested for JCV by TaqMan real-time reverse transcription–polymerase chain reaction (RT-PCR) with the primer pairs (5′-GTC TGG TCG AGT GTG ATA TAC G-3′) and (5′-CAG CAC AAA TCC GGT TAC AG-3′), and probe (5′-/56-TAMN/CCG GCA CTA CAG TTA AAT CTG GAT GGT/3IAbRQSP/-3′). These primers and probe do not detect lineage B; however, all mosquito pools besides Culex pipiens and Culex restuans (bird feeders that are unlikely to be infected with JCV) were inoculated onto mammalian cell cultures for virus isolation. All cultures displaying pathology consistent with viral infection were then harvested and identified using molecular testing and sequencing. This pipeline includes standard RT-PCR with generic Orthobunyavirus primers (5-ATGACTGAGTTGGAGTTTCATGATGTCGC-3′ and 5′-TGTTCCTGTTGCCAGGAAAAT-3′). All amplified products were subjected to sequencing at the Wadsworth Center Advanced Genomic Technologies Core (WCAGTC) followed by identification using the Basic Local Alignment Search Tool available through the National Center for Biotechnology Information.11

Infection rates, defined as the number of infected mosquitoes per 1,000, were calculated by the maximum likelihood estimation method using an excel plug-in program developed by Dr. Brad Biggerstaff.

Coding regions of the S, M, and L segments were amplified (primers available upon request) using one-step superscript III RT-PCR with platinum Taq (Life Technologies, Carlsbad, CA) according to the manufacturer’s instructions. The products were purified for next-generation sequencing at the WCAGTC. Briefly, library preparations were performed using the Nextera XT kit (Illumina, San Diego, CA). The sequencing was performed on the MiSeq Illumina platform, resulting in 250-bp paired-end reads. Full coding sequences for the S, M, and L segments were aligned, and phylogenetic trees were generated in Geneious (version 11.1.5; Geneious Prime, San Diego, CA) using PhyML with the Jukes-Cantor substitution model. The robustness of the nodes was evaluated by performing 500 bootstrap replicates. Trees were rooted to Inkoo virus S, M, and L segments (GenBank nos. KT288286, KT288285, and KT288284, respectively). Genetic distances were calculated using Mega10 X (Pennsylvania State University).

From 2001 to 2022, we tested 75,035 mosquito pools comprising approximately 2.45 million individuals, primarily representing five genera: Aedes (Ae.), Coquilletidia (Cq.), Culiseta (Cs.), Culex (Cx.), and Anopheles (An.). The infection rates were calculated by mosquito species (Figure 1A) and year (Figure 1B). Positive pools for the JCV were detected in 16 mosquito species: Ae. cantator (n = 1), Ae. sollicitans (n = 1), Ae. japonicus (n = 1), Ae. communis group (n = 2), Ae. triseriatus (n = 2), Ae. sticticus (n = 2), Cs. melanura (n = 4), An. quadrimaculatus (n = 6), Ae. trivittatus (n = 8), Ae. vexans (n = 9), Ae. stimulans group (n = 18, Ae. stimulans, Ae. excrucians, and Ae. fitchii combined), An. punctipennis (n = 25), Cq. perturbans (n = 30), and Ae. canadensis (n = 42). The highest infection rates were observed in An. punctipennis (0.57) and in the Ae. stimulans group (0.47), followed by Ae. canadensis (0.15). Aedes canadensis and An. punctipennis have been associated with many viruses, and their feeding preferences strongly affect their potential for human disease transmission.12 Aedes canadensis is a mammalian feeder that has been implicated as a bridge vector of viruses associated with human disease, including the Eastern equine encephalitis virus, LACV, and SSHV.13,14 In New York state, An. punctipennis and An. quadramaculatis, both mammalian feeders, have been implicated recently in driving increased transmission of Cache Valley virus,15 another medically important Orthobunyavirus.16

Figure 1.
Figure 1.

Jamestown Canyon virus infection rates from 2001 to 2022 in New York state. Infection rates were calculated by the maximum likelihood estimation method using a program developed by Dr. Brad Biggerstaff by (A) mosquito species and (B) year. The infection rate is defined as the number of infected mosquitoes per 1,000 tested. The numbers above the bars represent the total number of pools tested. Error bars represent 95% CIs intervals. Others: Aedes (Ae.) communis group Ae. sticticus, Ae. japonicus, Ae. triseriatus, Ae. sollicitans, and Ae. cantator.

Citation: The American Journal of Tropical Medicine and Hygiene 109, 6; 10.4269/ajtmh.23-0392

The mean annual JCV infection rate from 2001 to 2022 was 0.06, with significant yearly variation (0.01–0.24) (Figure 1). Above-average infection rates (> 0.06) were observed in 2008, 2009, 2012, 2014, 2015, 2018, 2020, and 2022, with the highest in 2020 (0.24). The mean infection rate from 2012 to 2022 (0.09) was significantly greater than the mean infection rate from 2001 to 2011 (0.04; χ2 test with Yates’ correction, P = 0.0003). At least one JCV-positive mosquito pool has been detected since 2001, with the highest number of positive pools in 2020 (n = 16). Human cases of JCV have been reported to the CDC since 2012, yet mosquito infection rates in New York state are not well correlated with reported cases.9 For example, no cases were reported in New York state in 2020, when the highest infection rate was measured, yet three cases were reported in 2013, when a relatively low infection rate was measured. It is unclear how accurately reported cases reflect regional JCV burdens, given that most infections are undiagnosed. More comprehensive serosurveys could help clarify the relationship between JCV prevalence in mosquitoes and spillover to humans.

We selected 32 JCV isolates for sequencing (Table 1), representing different mosquito species and locations throughout our 22-year surveillance period. Our phylogenetic analyses also included 15 previously sequenced isolates from Connecticut (CT): CT1044, CT1627, CT2989, CT339, CT4078, CT4095, CT1262, CT2286, CT23, CT3573, CT3682, CT810, CT1064, CT4148, and CT4473.17 Phylogenies of the S, M, and L segments showed no evidence of strong temporal clustering, yet suggested broad geographic clustering (Figure 2A-D). Specifically, we identified the existence of a distinct cluster within lineage A in which all southern New York strains grouped together with Connecticut strains. Additional well-supported clusters comprising predominately western and central/northern strains were also identified, yet more mixing was apparent among these groups. The JCV L segment showed the strongest regional clustering (Figure 2D). All New York state JCV isolates were grouped into lineage A, except for one isolate (JCV 278) from 2022 that clusters with lineage B Connecticut isolates. This represents the first identification of lineage B in New York state, although it has been detected in previous years in Connecticut18 and Massachusetts.19 We observed disagreement among segment phylogenies with one central New York state JCV isolate: JCV9. The JCV9 M and L segments grouped with other central New York strains, whereas the JCV9 S segment grouped with the southern cluster. These data suggest the possibility of reassortment among clusters, which could drive further genetic and phenotypic diversification. Reassortants leading to new viral strains with consequences for human disease have been well documented for Orthobunyaviruses.17,20

Table 1

Jamestown Canyon virus strains used for genetic analysis

Year Mosquito species County (region) Strain
2003 Coquillettidia (Cq.) perturbans Westchester (southern) JCV02
2004 Aedes (Ae.) canadensis Oneida (central) JCV04
2004 Ae. stimulans group Clinton (northern) JCV05
2005 Ae. trivittatus Cattaraugus (western) JCV06
2006 Ae. canadensis Onondaga (central) JCV07
2007 Ae. triseriatus Westchester (southern) JCV08
2007 Ae. canadensis Onondaga (central) JCV09
2008 Anopheles (An.) punctipennis Putnam (southern) JCV10
2008 Ae. vexans Oneida (central) JCV11
2009 Ae. canadensis Chautauqua (western) JCV12
2009 Ae. stimulans group Erie (western) JCV13
2010 Ae. stimulans group Erie (western) JCV14
2010 Ae. canadensis Westchester (southern) JCV15
2011 Ae. triseriatus Westchester (southern) JCV16
2011 An. punctipennis Rockland (southern) JCV17
2012 Cq. Perturbans Onondaga (central) JCV18
2012 Ae. canadensis Oswego (central) JCV19
2013 Ae. canadensis Madison (central) JCV21
2014 An. punctipennis Rockland (southern) JCV22
2014 Ae. canadensis Onondaga (central) JCV23
2015 Ae. sticticus Cattaraugus (western) JCV25
2016 An. punctipennis Cattaraugus (western) JCV26
2016 Ae. canadensis Erie (western) JCV27
2017 An. quadrimaculatus Cattaraugus (western) JCV28
2017 Ae. vexans Suffolk (southern) JCV29
2018 An. punctipennis Chautauqua (western) JCV30
2018 An. punctipennis Erie (western) JCV31
2019 Cq. Perturbans Orange (southern) JCV32
2019 Ae. stimulans group Erie (western) JCV33
2022 Ae. canadensis Suffolk (southern) JCV278
2022 Ae. canadensis Madison (central) JCV060
2022 Cq. Perturbans Onondaga (central) JCV333
Figure 2.
Figure 2.

Phylogenetic analysis of the Jamestown Canyon virus in New York state. (A) Full-genome sequencing was completed for 32 isolates collected from four regions in New York state, including southern (red), northern (purple), central (green), and western (blue). Maximum likelihood analysis of the complete coding regions of (B) small, (C) medium, and (D) large segments was completed together with previously sequenced isolates from Connecticut (CT). The robustness of the nodes was evaluated by performing 500 bootstrap replicates. The trees were rooted to Inkoo virus small, medium, and large segments (GenBank nos. KT288286, KT288285, and KT288284, respectively). The colors of individual taxa correspond to regions of isolation. Well-supported bootstrap values of major nodes are shown on trees together with previously identified designations of lineage A (Lin A) and lineage B (Lin B).

Citation: The American Journal of Tropical Medicine and Hygiene 109, 6; 10.4269/ajtmh.23-0392

The mean genetic distance, defined as the number of nucleotide substitutions per site, was calculated for each segment. The genetic distances of the S, M, and L segments are 0.006, 0.039, 0.010 within lineage A, and 0.030, 0.004, and 0.003 within lineage B, respectively. The mean genetic distances between the two lineages for the S, M, and L segments are 0.073, 0.141, and 0.135, respectively. Within lineage A (0.039), and between lineage A and B (0.141), there were more base substitutions per site in the M segment than in the S and L segments. Interestingly, in lineage A, the S segment was the most conserved (0.006), but was the most divergent in lineage B (0.030). Further studies are needed to understand more fully the consequences of within- and between-lineage genetic variability for virus transmission and disease, which are currently not well defined for JCV.

ACKNOWLEDGMENT

We thank the county health departments and additional members of the New York State Bureau of Communicable Disease Control for mosquito collections and coordination.

REFERENCES

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    Webster D , Dimitrova K , Holloway K , Makowski K , Safronetz D , Drebot MA , 2017. California serogroup virus infection associated with encephalitis and cognitive decline, Canada, 2015. Emerg Infect Dis 23: 14231424.

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    Pastula DM , Smith DE , Beckham JD , Tyler KL , 2016. Four emerging arboviral diseases in North America: Jamestown Canyon, Powassan, Chikungunya, and Zika virus diseases. J Neurovirol 22: 257260.

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    Pastula DM , Johnson DK , White JL , Dupuis AP , Fischer M , Staples JE , 2015. Jamestown Canyon virus disease in the United States: 2000–2013. Am J Trop Med Hyg 93: 384389.

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    Patriquin G et al., 2018. High seroprevalence of Jamestown Canyon virus among deer and humans, Nova Scotia, Canada. Emerg Infect Dis 24: 118121.

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    Dupuis AP et al., 2020. Serologic survey of mosquito-borne viruses in hunter-harvested white-tailed deer (Odocoileus virginianus), New York state. Am J Trop Med Hyg 104: 593603.

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    Vosoughi R , Walkty A , Drebot MA , Kadkhoda K , 2018. Jamestown Canyon virus meningoencephalitis mimicking migraine with aura in a resident of Manitoba. CMAJ 190: 262264.

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    Bialosuknia SM , Dupuis AP , Zink SD , Koetzner CA , Maffei JG , Owen JC , Landwerlen H , Kramer LD , Ciota AT , 2022. Adaptive evolution of West Nile virus facilitated increased transmissibility and prevalence in New York state. Emerg Microbes Infect 11: 988999.

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    • Export Citation
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    • Export Citation
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    Armstrong PM , Andreadis TG , 2007. Genetic relationships of Jamestown Canyon virus strains infecting mosquitoes collected in Connecticut. Am J Trop Med Hyg 77: 11571162.

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    Kinsella CM et al., 2020. Jamestown Canyon virus in Massachusetts: clinical case series and vector screening. Emerg Microbes Infect 9: 903912.

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    Briese T , Calisher CH , Higgs S , 2013. Viruses of the family Bunyaviridae: are all available isolates reassortants? Virology 446: 207216.

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    • PubMed
    • Search Google Scholar
    • Export Citation

Author Notes

Financial support: This work was funded in part by the CDC Cooperative (Agreement no. U01CK000509).

Disclosure: The content of this work is solely the responsibility of the authors and does not necessarily represent the CDC.

Authors’ addresses: Kiet A. Ngo, Joseph G. Maffei, Cheri A. Koetzner, Steven D. Zink, Anne F. Payne, and Alan P. Dupuis II, New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, NY, E-mails: kiet.ngo@health.ny.gov, joseph.maffei@health.ny.gov, cheri.koetzner@health.ny.gov, steven.zink@health.ny.gov, anne.payne@health.ny.gov, and alan.dupuis@health.ny.gov. P. Bryon Backenson and Jennifer L. White, New York State Department of Health, Bureau of Communicable Disease Control, Albany, NY, E-mails: bryon.backenson@health.ny.gov and jennifer.white@health.ny.gov. Laura D. Kramer and Alexander T. Ciota, New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, Slingerlands, NY, and Department of Biomedical Sciences, School of Public Health, State University of New York at Albany, Rensselaer, NY, E-mails: laura.kramer@health.ny.gov and alexander.ciota@health.ny.gov.

Address correspondence to Kiet A. Ngo, New York State Department of Health, The Arbovirus Laboratory, Wadsworth Center, 5668 State Farm Rd, Slingerlands, NY 12201-0509. E-mail: kiet.ngo@health.ny.gov
  • Figure 1.

    Jamestown Canyon virus infection rates from 2001 to 2022 in New York state. Infection rates were calculated by the maximum likelihood estimation method using a program developed by Dr. Brad Biggerstaff by (A) mosquito species and (B) year. The infection rate is defined as the number of infected mosquitoes per 1,000 tested. The numbers above the bars represent the total number of pools tested. Error bars represent 95% CIs intervals. Others: Aedes (Ae.) communis group Ae. sticticus, Ae. japonicus, Ae. triseriatus, Ae. sollicitans, and Ae. cantator.

  • Figure 2.

    Phylogenetic analysis of the Jamestown Canyon virus in New York state. (A) Full-genome sequencing was completed for 32 isolates collected from four regions in New York state, including southern (red), northern (purple), central (green), and western (blue). Maximum likelihood analysis of the complete coding regions of (B) small, (C) medium, and (D) large segments was completed together with previously sequenced isolates from Connecticut (CT). The robustness of the nodes was evaluated by performing 500 bootstrap replicates. The trees were rooted to Inkoo virus small, medium, and large segments (GenBank nos. KT288286, KT288285, and KT288284, respectively). The colors of individual taxa correspond to regions of isolation. Well-supported bootstrap values of major nodes are shown on trees together with previously identified designations of lineage A (Lin A) and lineage B (Lin B).

  • 1.

    Webster D , Dimitrova K , Holloway K , Makowski K , Safronetz D , Drebot MA , 2017. California serogroup virus infection associated with encephalitis and cognitive decline, Canada, 2015. Emerg Infect Dis 23: 14231424.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Pastula DM , Smith DE , Beckham JD , Tyler KL , 2016. Four emerging arboviral diseases in North America: Jamestown Canyon, Powassan, Chikungunya, and Zika virus diseases. J Neurovirol 22: 257260.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Pastula DM , Johnson DK , White JL , Dupuis AP , Fischer M , Staples JE , 2015. Jamestown Canyon virus disease in the United States: 2000–2013. Am J Trop Med Hyg 93: 384389.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Patriquin G et al., 2018. High seroprevalence of Jamestown Canyon virus among deer and humans, Nova Scotia, Canada. Emerg Infect Dis 24: 118121.

  • 5.

    Issel CJ , Trainer DO , Thompson WH , 1972. Serologic evidence of infections of white-tailed deer in Wisconsin with three California group arboviruses (La Crosse, Trivittatus, and Jamestown Canyon). Am J Trop Med Hyg 21: 985988.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Dupuis AP et al., 2020. Serologic survey of mosquito-borne viruses in hunter-harvested white-tailed deer (Odocoileus virginianus), New York state. Am J Trop Med Hyg 104: 593603.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Farquhar MR , Thrun NB , Tucker BJ , Bartholomay LC , 2022. Outbreak investigation: Jamestown Canyon virus surveillance in field-collected mosquitoes (Diptera: Culicidae) from Wisconsin, USA, 2018–2019. Front Public Health 10: 818204.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    CDC , 2023. Jamestown Canyon Virus: Data and Maps. Available at: https://www.cdc.gov/jamestown-canyon/statistics/index.html. Accessed September 7, 2023.

    • PubMed
    • Export Citation
  • 9.

    Vosoughi R , Walkty A , Drebot MA , Kadkhoda K , 2018. Jamestown Canyon virus meningoencephalitis mimicking migraine with aura in a resident of Manitoba. CMAJ 190: 262264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Bialosuknia SM , Dupuis AP , Zink SD , Koetzner CA , Maffei JG , Owen JC , Landwerlen H , Kramer LD , Ciota AT , 2022. Adaptive evolution of West Nile virus facilitated increased transmissibility and prevalence in New York state. Emerg Microbes Infect 11: 988999.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Altschul SF , Gish W , Miller W , Myers EW , Lipman DJ , 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403410.

  • 12.

    Molaei G , Andreadis TG , Armstrong PM , Diuk-Wasser M , 2008. Host-feeding patterns of potential mosquito vectors in Connecticut, USA: molecular analysis of bloodmeals from 23 species of Aedes, Anopheles, Culex, Coquillettidia, Psorophora, and Uranotaenia. J Med Entomol 45: 11431151.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Armstrong PM , Andreadis TG , 2010. Eastern equine encephalitis virus in mosquitoes and their role as bridge vectors. Emerg Infect Dis 16: 18691874.

  • 14.

    Carson PK , Holloway K , Dimitrova K , Rogers L , Chaulk AC , Lang AS , Whitney HG , Drebot MA , Chapman TW , 2017. The seasonal timing of Snowshoe hare virus transmission on the island of Newfoundland, Canada. J Med Entomol 54: 712718.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Dieme C et al., 2022. Role of Anopheles mosquitoes in Cache Valley virus lineage displacement, New York, USA. Emerg Infect Dis 28: 303313.

  • 16.

    Waddell L , Pachal N , Mascarenhas M , Greig J , Harding S , Young I , Wilhelm B , 2019. Cache Valley virus: a scoping review of the global evidence. Zoonoses Public Health 66: 739758.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Armstrong PM , Andreadis TG , 2007. Genetic relationships of Jamestown Canyon virus strains infecting mosquitoes collected in Connecticut. Am J Trop Med Hyg 77: 11571162.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Kinsella CM et al., 2020. Jamestown Canyon virus in Massachusetts: clinical case series and vector screening. Emerg Microbes Infect 9: 903912.

  • 19.

    Briese T , Calisher CH , Higgs S , 2013. Viruses of the family Bunyaviridae: are all available isolates reassortants? Virology 446: 207216.

  • 20.

    Hughes HR , Lanciotti RS , Blair CD , Lambert AJ , 2017. Full genomic characterization of California serogroup viruses, genus Orthobunyavirus, family Peribunyaviridae including phylogenetic relationships. Virology 512: 201210.

    • PubMed
    • Search Google Scholar
    • Export Citation
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