Analyze Diet
Current biology : CB2023; 33(12); 2515-2527.e6; doi: 10.1016/j.cub.2023.05.047

Dynamics of eastern equine encephalitis virus during the 2019 outbreak in the Northeast United States.

Abstract: Eastern equine encephalitis virus (EEEV) causes a rare but severe disease in horses and humans and is maintained in an enzootic transmission cycle between songbirds and Culiseta melanura mosquitoes. In 2019, the largest EEEV outbreak in the United States for more than 50 years occurred, centered in the Northeast. To explore the dynamics of the outbreak, we sequenced 80 isolates of EEEV and combined them with existing genomic data. We found that, similar to previous years, cases were driven by multiple independent but short-lived virus introductions into the Northeast from Florida. Once in the Northeast, we found that Massachusetts was important for regional spread. We found no evidence of any changes in viral, human, or bird factors which would explain the increase in cases in 2019, although the ecology of EEEV is complex and further data is required to explore these in more detail. By using detailed mosquito surveillance data collected by Massachusetts and Connecticut, however, we found that the abundance of Cs. melanura was exceptionally high in 2019, as was the EEEV infection rate. We employed these mosquito data to build a negative binomial regression model and applied it to estimate early season risks of human or horse cases. We found that the month of first detection of EEEV in mosquito surveillance data and vector index (abundance multiplied by infection rate) were predictive of cases later in the season. We therefore highlight the importance of mosquito surveillance programs as an integral part of public health and disease control.
Publication Date: 2023-06-08 PubMed ID: 37295427PubMed Central: PMC10316540DOI: 10.1016/j.cub.2023.05.047Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • N.I.H.
  • Extramural

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research explores the dynamics of the Eastern equine encephalitis virus (EEEV) outbreak that occurred in the Northeast United States in 2019. Researchers discovered that the outbreak, which had not last this extreme for over 50 years, resulted from multiple, isolated introductions of the virus from Florida and spread substantially from Massachusetts. The research underscores the importance of mosquito surveillance in public health and disease control.

Introduction and Overview on EEEV

  • Eastern equine encephalitis virus (EEEV) is a severe disease that affects both humans and horses. The virus is primarily transmitted through songbirds and Culiseta melanura mosquitoes.
  • In 2019, a record-breaking outbreak of EEEV occurred in the United States, specifically centered in the Northeast region — the largest in over half a century.

Findings and Analysis

  • To better understand the dynamics of this outbreak, researchers sequenced 80 isolates of EEEV, combining this new information with existing genomic data.
  • The researchers discovered that the cases were likely caused through multiple independent–yet short-lived–introductions of the virus into the Northeast from Florida.
  • They noted Massachusetts as a significant point of regional virus propagation. However, there was no indication in changes in the viral, human, or bird factors that could clarify the increase in cases in 2019.
  • The research points out the complexity of investigating EEEV ecology and expresses the need for more data for deeper examination.

The Role of Mosquito Surveillance and Risk Estimation

  • Detailed mosquito surveillance data was obtained from Massachusetts and Connecticut. The researchers found that the abundance of Cs. melanura mosquitoes and the EEEV infection rate were exceptionally high during 2019.
  • The mosquito data was used to create a negative binomial regression model, and this was applied to estimate the early-season risks of human or horse cases of EEEV.
  • The findings showed that both the month of the first detection of EEEV in the mosquito surveillance data and the vector index (based on mosquito abundance and infection rate) were indictors of EEEV cases appearing later in the season.
  • The study concludes by emphasizing the importance of mosquito surveillance programs for public health and disease control.

Cite This Article

APA
Hill V, Koch RT, Bialosuknia SM, Ngo K, Zink SD, Koetzner CA, Maffei JG, Dupuis AP, Backenson PB, Oliver J, Bransfield AB, Misencik MJ, Petruff TA, Shepard JJ, Warren JL, Gill MS, Baele G, Vogels CBF, Gallagher G, Burns P, Hentoff A, Smole S, Brown C, Osborne M, Kramer LD, Armstrong PM, Ciota AT, Grubaugh ND. (2023). Dynamics of eastern equine encephalitis virus during the 2019 outbreak in the Northeast United States. Curr Biol, 33(12), 2515-2527.e6. https://doi.org/10.1016/j.cub.2023.05.047

Publication

ISSN: 1879-0445
NlmUniqueID: 9107782
Country: England
Language: English
Volume: 33
Issue: 12
Pages: 2515-2527.e6
PII: S0960-9822(23)00679-6

Researcher Affiliations

Hill, Verity
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06510, USA. Electronic address: verity.hill@yale.edu.
Koch, Robert T
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06510, USA.
Bialosuknia, Sean M
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA.
Ngo, Kiet
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA.
Zink, Steven D
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA.
Koetzner, Cheri A
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA.
Maffei, Joseph G
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA.
Dupuis, Alan P
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA.
Backenson, P Bryon
  • New York State Department of Health, Bureau of Communicable Disease Control, Albany, NY 12237, USA.
Oliver, JoAnne
  • New York State Department of Health, Bureau of Communicable Disease Control, Syracuse, NY 13202, USA; Division of Environmental and Renewable Resources, State University of New York at Morrisville - School of Agriculture, Business and Technology, Morrisville, NY 13408, USA.
Bransfield, Angela B
  • Center for Vector Biology and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, CT 06511, USA.
Misencik, Michael J
  • Center for Vector Biology and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, CT 06511, USA.
Petruff, Tanya A
  • Center for Vector Biology and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, CT 06511, USA.
Shepard, John J
  • Center for Vector Biology and Zoonotic Diseases, Department of Entomology, The Connecticut Agricultural Experiment Station, New Haven, CT 06511, USA.
Warren, Joshua L
  • Department of Biostatistics, Yale School of Public Health, New Haven, CT 06510, USA; Public Health Modeling Unit, Yale School of Public Health, New Haven, CT 06510, USA.
Gill, Mandev S
  • Department of Statistics, University of Georgia, Athens, GA 30602, USA.
Baele, Guy
  • Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Leuven BE-3000, Belgium.
Vogels, Chantal B F
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06510, USA.
Gallagher, Glen
  • Massachusetts Department of Public Health, Boston, MA 02108, USA; Rhode Island State Health Laboratory, Rhode Island Department of Health, Providence, RI 02904, USA.
Burns, Paul
  • Massachusetts Department of Public Health, Boston, MA 02108, USA.
Hentoff, Aaron
  • Massachusetts Department of Public Health, Boston, MA 02108, USA.
Smole, Sandra
  • Massachusetts Department of Public Health, Boston, MA 02108, USA.
Brown, Catherine
  • Massachusetts Department of Public Health, Boston, MA 02108, USA.
Osborne, Matthew
  • Massachusetts Department of Public Health, Boston, MA 02108, USA.
Kramer, Laura D
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA; Department of Biomedical Sciences, State University of New York at Albany School of Public Health, Albany, NY 12237, USA.
Armstrong, Philip M
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06510, USA; Division of Environmental and Renewable Resources, State University of New York at Morrisville - School of Agriculture, Business and Technology, Morrisville, NY 13408, USA. Electronic address: philip.armstrong@ct.gov.
Ciota, Alexander T
  • The Arbovirus Laboratory, New York State Department of Health, Wadsworth Center, Slingerlands, NY 12159, USA; Department of Biomedical Sciences, State University of New York at Albany School of Public Health, Albany, NY 12237, USA. Electronic address: alexander.ciota@health.ny.gov.
Grubaugh, Nathan D
  • Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06510, USA; Department of Biostatistics, Yale School of Public Health, New Haven, CT 06510, USA; Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA. Electronic address: nathan.grubaugh@yale.edu.

MeSH Terms

  • Animals
  • Horses
  • Humans
  • Encephalitis Virus, Eastern Equine / genetics
  • Mosquito Vectors
  • Encephalomyelitis, Equine / epidemiology
  • Encephalomyelitis, Equine / veterinary
  • Culicidae
  • Massachusetts / epidemiology
  • Disease Outbreaks / veterinary
  • Songbirds

Grant Funding

  • DP2 AI176740 / NIAID NIH HHS
  • U01 CK000509 / NCEZID CDC HHS
  • UL1 TR001863 / NCATS NIH HHS

Conflict of Interest Statement

Declaration of interests The authors declare no conflicts of interest related to this work.

References

This article includes 54 references
  1. Giltner, Shahan. The 1933 outbreak of infectious equine encephalomyelitis in the eastern states. North Am. Vet. .
  2. TenBroeck C, Merrill MH. A serological difference between eastern and western equine encephalomyelitis virus. Proc. Soc. Exp. Biol. Med. 31.
  3. Lindsey NP, Staples JE, Fischer M. Eastern Equine Encephalitis Virus in the United States, 2003-2016.. Am J Trop Med Hyg 2018 May;98(5):1472-1477.
    pmc: PMC5953388pubmed: 29557336doi: 10.4269/ajtmh.17-0927google scholar: lookup
  4. Lindsey NP, Martin SW, Staples JE, Fischer M. Notes from the Field: Multistate Outbreak of Eastern Equine Encephalitis Virus - United States, 2019.. MMWR Morb Mortal Wkly Rep 2020 Jan 17;69(2):50-51.
    pmc: PMC6973353pubmed: 31945032doi: 10.15585/mmwr.mm6902a4google scholar: lookup
  5. Shamus KJ. Deaths from mosquito-borne EEE virus prompt calls to cancel outdoor events in Michigan. USA Today .
  6. Tunison J. Despite assurances, aerial mosquito spraying plan leaves some concerned. mlive .
  7. Howard J. Why did EEE cases spike this year? It’s complicated. CNN .
  8. Morris CD. Eastern equine encephalomyelitis. The Arboviruses: epidemiology and ecology pp. 1–20.
  9. Armstrong PM, Andreadis TG. Ecology and Epidemiology of Eastern Equine Encephalitis Virus in the Northeastern United States: An Historical Perspective.. J Med Entomol 2022 Jan 12;59(1):1-13.
    doi: 10.1093/jme/tjab077pmc: PMC8755988pubmed: 34734628google scholar: lookup
  10. Molaei G, Oliver J, Andreadis TG, Armstrong PM, Howard JJ. Molecular identification of blood-meal sources in Culiseta melanura and Culiseta morsitans from an endemic focus of eastern equine encephalitis virus in New York.. Am J Trop Med Hyg 2006 Dec;75(6):1140-7.
    pubmed: 17172382
  11. Mundis SJ, Harrison S, Pelley D, Durand S, Ryan SJ. Spatiotemporal Environmental Drivers of Eastern Equine Encephalitis Virus in Central Florida: Towards a Predictive Model for a Lethal Disease.. J Med Entomol 2022 Sep 14;59(5):1805-1816.
    doi: 10.1093/jme/tjac113pubmed: 35957606google scholar: lookup
  12. Tan Y, Lam TT, Heberlein-Larson LA, Smole SC, Auguste AJ, Hennigan S, Halpin RA, Fedorova N, Puri V, Stockwell TB, Shilts MH, Andreadis T, Armstrong PM, Tesh RB, Weaver SC, Unnasch TR, Ciota AT, Kramer LD, Das SR. Large-Scale Complete-Genome Sequencing and Phylodynamic Analysis of Eastern Equine Encephalitis Virus Reveals Source-Sink Transmission Dynamics in the United States.. J Virol 2018 Jun 15;92(12).
    doi: 10.1128/JVI.00074-18pmc: PMC5974483pubmed: 29618651google scholar: lookup
  13. Young DS, Kramer LD, Maffei JG, Dusek RJ, Backenson PB, Mores CN, Bernard KA, Ebel GD. Molecular epidemiology of eastern equine encephalitis virus, New York.. Emerg Infect Dis 2008 Mar;14(3):454-60.
    pmc: PMC2570827pubmed: 18325261doi: 10.3201/eid1403.070816google scholar: lookup
  14. Oliver J, Tan Y, Haight JD, Tober KJ, Gall WK, Zink SD, Kramer LD, Campbell SR, Howard JJ, Das SR, Sherwood JA. Spatial and temporal expansions of Eastern equine encephalitis virus and phylogenetic groups isolated from mosquitoes and mammalian cases in New York State from 2013 to 2019.. Emerg Microbes Infect 2020 Dec;9(1):1638-1650.
  15. Morens DM, Folkers GK, Fauci AS. Eastern Equine Encephalitis Virus - Another Emergent Arbovirus in the United States.. N Engl J Med 2019 Nov 21;381(21):1989-1992.
    pubmed: 31747726doi: 10.1056/nejmp1914328google scholar: lookup
  16. Gill MS, Lemey P, Faria NR, Rambaut A, Shapiro B, Suchard MA. Improving Bayesian population dynamics inference: a coalescent-based model for multiple loci.. Mol Biol Evol 2013 Mar;30(3):713-24.
    pmc: PMC3563973pubmed: 23180580doi: 10.1093/molbev/mss265google scholar: lookup
  17. Gill MS, Lemey P, Bennett SN, Biek R, Suchard MA. Understanding Past Population Dynamics: Bayesian Coalescent-Based Modeling with Covariates.. Syst Biol 2016 Nov;65(6):1041-1056.
    pmc: PMC5066065pubmed: 27368344doi: 10.1093/sysbio/syw050google scholar: lookup
  18. Susswein Z, Rest EC, Bansal S. Disentangling the rhythms of human activity in the built environment for airborne transmission risk: An analysis of large-scale mobility data.. Elife 2023 Apr 4;12.
    pmc: PMC10118388pubmed: 37014055doi: 10.7554/elife.80466google scholar: lookup
  19. Kramer LD, Ciota AT. Dissecting vectorial capacity for mosquito-borne viruses.. Curr Opin Virol 2015 Dec;15:112-8.
  20. Molaei G, Thomas MC, Muller T, Medlock J, Shepard JJ, Armstrong PM, Andreadis TG. Dynamics of Vector-Host Interactions in Avian Communities in Four Eastern Equine Encephalitis Virus Foci in the Northeastern U.S.. PLoS Negl Trop Dis 2016 Jan;10(1):e0004347.
  21. Nasci RS, Doyle M, Biggerstaff BJ, LeBailly A. Calculation and application of a vector index (VI) reflecting the number of WN virus infected mosquitoes in a population. 71st annual meeting of the American .
  22. Fauver JR, Pecher L, Schurich JA, Bolling BG, Calhoon M, Grubaugh ND, Burkhalter KL, Eisen L, Andre BG, Nasci RS, LeBailly A, Ebel GD, Moore CG. Temporal and Spatial Variability of Entomological Risk Indices for West Nile Virus Infection in Northern Colorado: 2006-2013.. J Med Entomol 2016 Mar;53(2):425-34.
    pmc: PMC5778898pubmed: 26718715doi: 10.1093/jme/tjv234google scholar: lookup
  23. Obolski U, Perez PN, Villabona-Arenas CJ, Thézé J, Faria NR, Lourenço J. MVSE: An R-package that estimates a climate-driven mosquito-borne viral suitability index.. Methods Ecol Evol 2019 Aug;10(8):1357-1370.
    pmc: PMC7202302pubmed: 32391139doi: 10.1111/2041-210x.13205google scholar: lookup
  24. Sherwood JA, Stehman SV, Howard JJ, Oliver J. Cases of Eastern equine encephalitis in humans associated with Aedes canadensis, Coquillettidia perturbans and Culiseta melanura mosquitoes with the virus in New York State from 1971 to 2012 by analysis of aggregated published data.. Epidemiol Infect 2020 Apr 1;148:e72.
    pmc: PMC7118715pubmed: 32234110doi: 10.1017/s0950268820000308google scholar: lookup
  25. Layan M, Müller NF, Dellicour S, De Maio N, Bourhy H, Cauchemez S, Baele G. Impact and mitigation of sampling bias to determine viral spread: Evaluating discrete phylogeography through CTMC modeling and structured coalescent model approximations.. Virus Evol 2023;9(1):vead010.
    pmc: PMC9969415pubmed: 36860641doi: 10.1093/ve/vead010google scholar: lookup
  26. Lourenço J, Thompson RN, Thézé J, Obolski U. Characterising West Nile virus epidemiology in Israel using a transmission suitability index.. Euro Surveill 2020 Nov;25(46).
  27. Bigler WJ, Lassing EB, Buff EE, Prather EC, Beck EC, Hoff GL. Endemic eastern equine encephalomyelitis in Florida: a twenty-year analysis, 1955-1974.. Am J Trop Med Hyg 1976 Nov;25(6):884-90.
    pubmed: 12669doi: 10.4269/ajtmh.1976.25.884google scholar: lookup
  28. Elias SP, Keenan P, Kenney JL, Morris SR, Covino KM, Robinson S, Foss KA, Rand PW, Lubelczyk C, Lacombe EH, Mutebi JP, Evers D, Smith RP Jr. Seasonal Patterns in Eastern Equine Encephalitis Virus Antibody in Songbirds in Southern Maine.. Vector Borne Zoonotic Dis 2017 May;17(5):325-330.
    pubmed: 28287934doi: 10.1089/vbz.2016.2029google scholar: lookup
  29. Dudas G, Carvalho LM, Rambaut A, Bedford T. MERS-CoV spillover at the camel-human interface.. Elife 2018 Jan 16;7.
    doi: 10.7554/eLife.31257pmc: PMC5777824pubmed: 29336306google scholar: lookup
  30. Oliver J, Lukacik G, Kokas J, Campbell SR, Kramer LD, Sherwood JA, Howard JJ. Twenty years of surveillance for Eastern equine encephalitis virus in mosquitoes in New York State from 1993 to 2012.. Parasit Vectors 2018 Jun 25;11(1):362.
    doi: 10.1186/s13071-018-2950-1pmc: PMC6019270pubmed: 29941031google scholar: lookup
  31. Zink SD, Jones SA, Maffei JG, Kramer LD. Quadraplex qRT-PCR assay for the simultaneous detection of Eastern equine encephalitis virus and West Nile virus.. Diagn Microbiol Infect Dis 2013 Oct;77(2):129-32.
  32. Kinsella CM, Paras ML, Smole S, Mehta S, Ganesh V, Chen LH, McQuillen DP, Shah R, Chan J, Osborne M, Hennigan S, Halpern-Smith F, Brown CM, Sabeti P, Piantadosi A. Jamestown Canyon virus in Massachusetts: clinical case series and vector screening.. Emerg Microbes Infect 2020 Dec;9(1):903-912.
  33. Molaei G, Andreadis TG, Armstrong PM, Thomas MC, Deschamps T, Cuebas-Incle E, Montgomery W, Osborne M, Smole S, Matton P, Andrews W, Best C, Cornine F 3rd, Bidlack E, Texeira T. Vector-host interactions and epizootiology of eastern equine encephalitis virus in Massachusetts.. Vector Borne Zoonotic Dis 2013 May;13(5):312-23.
    pubmed: 23473221doi: 10.1089/vbz.2012.1099google scholar: lookup
  34. Petruff TA, McMillan JR, Shepard JJ, Andreadis TG, Armstrong PM. Increased mosquito abundance and species richness in Connecticut, United States 2001-2019.. Sci Rep 2020 Nov 6;10(1):19287.
    pmc: PMC7648108pubmed: 33159108doi: 10.1038/s41598-020-76231-xgoogle scholar: lookup
  35. Armstrong PM, Andreadis TG, Finan SL, Shepard JJ, Thomas MC. Detection of infectious virus from field-collected mosquitoes by vero cell culture assay.. J Vis Exp 2011 Jun 9;(52).
    doi: 10.3791/2889pmc: PMC3197060pubmed: 21694689google scholar: lookup
  36. Armstrong PM, Prince N, Andreadis TG. Development of a multi-target TaqMan assay to detect eastern equine encephalitis virus variants in mosquitoes.. Vector Borne Zoonotic Dis 2012 Oct;12(10):872-6.
    pmc: PMC3466067pubmed: 22835151doi: 10.1089/vbz.2012.1008google scholar: lookup
  37. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability.. Mol Biol Evol 2013 Apr;30(4):772-80.
    pmc: PMC3603318pubmed: 23329690doi: 10.1093/molbev/mst010google scholar: lookup
  38. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era.. Mol Biol Evol 2020 May 1;37(5):1530-1534.
    pmc: PMC7182206pubmed: 32011700doi: 10.1093/molbev/msaa015google scholar: lookup
  39. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen).. Virus Evol 2016 Jan;2(1):vew007.
    pmc: PMC4989882pubmed: 27774300doi: 10.1093/ve/vew007google scholar: lookup
  40. Hill V, Baele G. Bayesian Estimation of Past Population Dynamics in BEAST 1.10 Using the Skygrid Coalescent Model.. Mol Biol Evol 2019 Nov 1;36(11):2620-2628.
    doi: 10.1093/molbev/msz172pmc: PMC6805224pubmed: 31364710google scholar: lookup
  41. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10.. Virus Evol 2018 Jan;4(1):vey016.
    doi: 10.1093/ve/vey016pmc: PMC6007674pubmed: 29942656google scholar: lookup
  42. Baele G, Gill MS, Lemey P, Suchard MA. Hamiltonian Monte Carlo sampling to estimate past population dynamics using the skygrid coalescent model in a Bayesian phylogenetics framework.. Wellcome Open Res 2020;5:53.
  43. Hasegawa M, Kishino H, Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.. J Mol Evol 1985;22(2):160-74.
    pubmed: 3934395doi: 10.1007/bf02101694google scholar: lookup
  44. Ferreira MAR, Suchard MA. Bayesian analysis of elapsed times in continuous-time Markov chains. Can. J. Stat. 36, 355–368.
  45. Lemey P, Hong SL, Hill V, Baele G, Poletto C, Colizza V, O'Toole Á, McCrone JT, Andersen KG, Worobey M, Nelson MI, Rambaut A, Suchard MA. Accommodating individual travel history and unsampled diversity in Bayesian phylogeographic inference of SARS-CoV-2.. Nat Commun 2020 Oct 9;11(1):5110.
    pmc: PMC7547076pubmed: 33037213doi: 10.1038/s41467-020-18877-9google scholar: lookup
  46. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7.. Syst Biol 2018 Sep 1;67(5):901-904.
    pmc: PMC6101584pubmed: 29718447doi: 10.1093/sysbio/syy032google scholar: lookup
  47. Yu GY, Wiley MR, Kugelman JR, Ladner JT, Beitzel BF, Eccleston LT, Morazzani EM, Glass PJ, Palacios GF. Complete coding sequences of eastern equine encephalitis virus and venezuelan equine encephalitis virus strains isolated from human cases.. Genome Announc 2015 Apr 23;3(2).
    doi: 10.1128/genomeA.00243-15pmc: PMC4408325pubmed: 25908124google scholar: lookup
  48. Cameron AC, Trivedi PK. Regression-based tests for overdispersion in the Poisson model. J. Econom. 46, 347–364.
  49. Corrin T, Ackford R, Mascarenhas M, Greig J, Waddell LA. Eastern Equine Encephalitis Virus: A Scoping Review of the Global Evidence.. Vector Borne Zoonotic Dis 2021 May;21(5):305-320.
    pmc: PMC8086401pubmed: 33332203doi: 10.1089/vbz.2020.2671google scholar: lookup
  50. Stobierski MG, Signs K, Dinh E, Cooley TM, Melotti J, Schalow M, Patterson JS, Bolin SR, Walker ED. Eastern Equine Encephalomyelitis in Michigan: Historical Review of Equine, Human, and Wildlife Involvement, Epidemiology, Vector Associations, and Factors Contributing to Endemicity.. J Med Entomol 2022 Jan 12;59(1):27-40.
    pmc: PMC8755995pubmed: 34734638doi: 10.1093/jme/tjab153google scholar: lookup
  51. Grady GF, Maxfield HK, Hildreth SW, Timperi RJ Jr, Gilfillan RF, Rosenau BJ, Francy DB, Calisher CH, Marcus LC, Madoff MA. Eastern equine encephalitis in Massachusetts, 1957-1976. A prospective study centered upon analyses of mosquitoes.. Am J Epidemiol 1978 Feb;107(2):170-8.
  52. Feemster RF. Outbreak of Encephalitis in Man Due to the Eastern Virus of Equine Encephalomyelitis.. Am J Public Health Nations Health 1938 Dec;28(12):1403-10.
    pmc: PMC1527806pubmed: 18014957doi: 10.2105/ajph.28.12.1403google scholar: lookup
  53. . Arbovirus Surveillance Plan and historical data. Massachusetts Department of Public Health .
  54. Celis-Murillo A, Malorodova M, Nakash E. North American Bird Banding Program Dataset 1960–2022 retrieved 2022–07-14. .
    doi: 10.5066/P9BSM38Fgoogle scholar: lookup

Citations

This article has been cited 0 times.