Analyze Diet
PloS one2022; 17(8); e0272130; doi: 10.1371/journal.pone.0272130

Multi-season transmission model of Eastern Equine Encephalitis.

Abstract: Eastern Equine Encephalitis (EEE) is an arbovirus that, while it has been known to exist since the 1930's, recently had a spike in cases. This increased prevalence is particularly concerning due to the severity of the disease with 1 in 3 symptomatic patients dying. The cause of this peak is currently unknown but could be due to changes in climate, the virus itself, or host behavior. In this paper we propose a novel multi-season deterministic model of EEE spread and its stochastic counterpart. Models were parameterized using a dataset from the Florida Department of Health with sixteen years of sentinel chicken seroconversion rates. The different roles of the enzootic and bridge mosquito vectors were explored. As expected, enzootic mosquitoes like Culiseta melanura were more important for EEE persistence, while bridge vectors were implicated in the disease burden in humans. These models were used to explore hypothetical viral mutations and host behavior changes, including increased infectivity, vertical transmission, and host feeding preferences. Results showed that changes in the enzootic vector transmission increased cases among birds more drastically than equivalent changes in the bridge vector. Additionally, a 5% difference in the bridge vector's bird feeding preference can increase cumulative dead-end host infections more than 20-fold. Taken together, this suggests changes in many parts of the transmission cycle can augment cases in birds, but the bridge vectors feeding preference acts as a valve limiting the enzootic circulation from its impact on dead-end hosts, such as humans. Our what-if scenario analysis reveals and measures possible threats regarding EEE and relevant environmental changes and hypothetically suggests how to prevent potential damage to public health and the equine economy.
Publication Date: 2022-08-17 PubMed ID: 35976903PubMed Central: PMC9385034DOI: 10.1371/journal.pone.0272130Google 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

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 study conceptualizes and tests a novel mathematical model to understand the spread of Eastern Equine Encephalitis (EEE), a severe and often deadly virus. Results from the model shed light on the roles different types of mosquitoes play in EEE transmission and how changes in virus behavior could potentially lead to more cases in humans and birds.

Background

  • Eastern Equine Encephalitis (EEE) is a virus transmitted by mosquitoes. Its grim mortality rate, killing one in three symptomatic patients, is troubling, especially in the wake of a recent surge in cases.
  • The reason behind this surge in cases isn’t clear but potential factors include changes in climate, the virus itself or host behavior.
  • The purpose of this research was to better understand the virus’s spread through a novel multi-season deterministic model and its stochastic counterpart, using data accumulated over sixteen years from the Florida Department of Health.

Roles of Different Mosquitoes in Spreading EEE

  • The researchers developed models to investigate the roles enzootic (animal-infecting) and bridge (both bird and human-infecting) mosquito vectors play in the spread of the EEE.
  • Enzootic mosquitoes like Culiseta melanura were found to be more essential for the virus’s persistence, whilst the bridge vectors were more linked with the disease burden in humans.

Investigating Hypothetical Scenarios

  • The researchers simulated scenarios involving viral mutations and changes in host behavior and observed increases in infectivity, vertical transmission, and host feeding preferences.
  • Results revealed that changes in the enzootic vector transmission augmented cases among birds more substantially than equivalent alterations in the bridge vector.
  • The researchers also discovered that small differences, of about 5%, in the bridge vector’s preference for feeding on birds, could fuel a more than 20-fold increase in cumulative infections in dead-end hosts (those who cannot further transmit the infection), including humans.

Conclusion and Implications

  • The outcomes pointed out that changes in various parts of the EEE transmission cycle can increase cases in birds, but the feeding preference of bridge vectors can limit the disease’s spread to humans.
  • The study’s findings serve as an early warning system, flagging possible dangers associated with EEE and environmental changes, and offering preventative strategies to protect public health and the equine economy.

Cite This Article

APA
Petrucciani A, Yu G, Ventresca M. (2022). Multi-season transmission model of Eastern Equine Encephalitis. PLoS One, 17(8), e0272130. https://doi.org/10.1371/journal.pone.0272130

Publication

ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 17
Issue: 8
Pages: e0272130
PII: e0272130

Researcher Affiliations

Petrucciani, Alexa
  • Weldon School of Biomedical Engineering, Purdue University, West Lafayette, Indiana, United States of America.
Yu, Geonsik
  • School of Industrial Engineering, Purdue University, West Lafayette, Indiana, United States of America.
Ventresca, Mario
  • School of Industrial Engineering, Purdue University, West Lafayette, Indiana, United States of America.
  • Purdue Institute for Inflammation, Immunology, and Infectious Diseases, Purdue University, West Lafayette, Indiana, United States of America.

MeSH Terms

  • Animals
  • Chickens
  • Culicidae
  • Encephalitis Virus, Eastern Equine
  • Encephalomyelitis, Eastern Equine / epidemiology
  • Encephalomyelitis, Eastern Equine / veterinary
  • Encephalomyelitis, Equine
  • Horses
  • Humans
  • Insect Vectors
  • Seasons

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 68 references
  1. Armstrong PM, Andreadis TG. Eastern equine encephalitis virus--old enemy, new threat.. N Engl J Med 2013 May 2;368(18):1670-3.
    doi: 10.1056/NEJMp1213696pubmed: 23635048google scholar: lookup
  2. for Disease Control C, Prevention. Eastern Equine Enchephalitis; 2020. Available from: https://www.cdc.gov/easternequineencephalitis/index.html.
  3. 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.
    doi: 10.1056/NEJMp1914328pubmed: 31747726google scholar: lookup
  4. Turell MJ, Beaman JR, Neely GW. Experimental transmission of eastern equine encephalitis virus by strains of Aedes albopictus and A. taeniorhynchus (Diptera: Culicidae).. J Med Entomol 1994 Mar;31(2):287-90.
    doi: 10.1093/jmedent/31.2.287pubmed: 8189419google scholar: lookup
  5. Sardelis MR, Dohm DJ, Pagac B, Andre RG, Turell MJ. Experimental transmission of eastern equine encephalitis virus by Ochlerotatus j. japonicus (Diptera: Culicidae).. J Med Entomol 2002 May;39(3):480-4.
    doi: 10.1603/0022-2585-39.3.480pubmed: 12061444google scholar: lookup
  6. Bosak PJ, Reed LM, Crans WJ. Habitat preference of host-seeking Coquillettidia perturbans (Walker) in relation to birds and eastern equine encephalomyelitis virus in New Jersey.. J Vector Ecol 2001 Jun;26(1):103-9.
    pubmed: 11469178
  7. Gray KM, Burkett-Cadena ND, Eubanks MD, Unnasch TR. Crepuscular flight activity of Culex erraticus (Diptera: Culicidae).. J Med Entomol 2011 Mar;48(2):167-72.
    doi: 10.1603/ME10176pubmed: 21485351google scholar: lookup
  8. Goldfield M, Welsh JN, Taylor BF. The 1959 outbreak of Eastern encephalitis in New Jersey. 5. The inapparent infection:disease ratio.. Am J Epidemiol 1968 Jan;87(1):32-3.
  9. 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.
  10. Unnasch RS, Sprenger T, Katholi CR, Cupp EW, Hill GE, Unnasch TR. A dynamic transmission model of eastern equine encephalitis virus.. Ecol Modell 2006 Feb 25;192(3-4):425-440.
  11. Morrison A, Rowe D, Stanek D, LaCrue A, Castaneda M, Mock V. Florida Arbovirus Surveillance. The Florida Department of Health; 2019.
  12. Chen J, Gao K, Wang R, Wei GW. Prediction and mitigation of mutation threats to COVID-19 vaccines and antibody therapies.. Chem Sci 2021 Apr 13;12(20):6929-6948.
    doi: 10.1039/d1sc01203gpmc: PMC8153213pubmed: 34123321google scholar: lookup
  13. Wang R, Chen J, Gao K, Wei GW. Vaccine-escape and fast-growing mutations in the United Kingdom, the United States, Singapore, Spain, India, and other COVID-19-devastated countries.. Genomics 2021 Jul;113(4):2158-2170.
    doi: 10.1016/j.ygeno.2021.05.006pmc: PMC8123493pubmed: 34004284google scholar: lookup
  14. Ghosh N, Nandi S, Saha I. A review on evolution of emerging SARS-CoV-2 variants based on spike glycoprotein.. Int Immunopharmacol 2022 Apr;105:108565.
  15. Peck KM, Lauring AS. Complexities of Viral Mutation Rates.. J Virol 2018 Jul 15;92(14).
    doi: 10.1128/JVI.01031-17pmc: PMC6026756pubmed: 29720522google scholar: lookup
  16. Ketkar H, Herman D, Wang P. Genetic Determinants of the Re-Emergence of Arboviral Diseases.. Viruses 2019 Feb 12;11(2).
    doi: 10.3390/v11020150pmc: PMC6410223pubmed: 30759739google scholar: lookup
  17. Weaver SC, Bellew LA, Gousset L, Repik PM, Scott TW, Holland JJ. Diversity within natural populations of eastern equine encephalomyelitis virus.. Virology 1993 Aug;195(2):700-9.
    doi: 10.1006/viro.1993.1421pubmed: 8101674google scholar: lookup
  18. Weaver SC, Brault AC, Kang W, Holland JJ. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells.. J Virol 1999 May;73(5):4316-26.
  19. Gardner CL, Choi-Nurvitadhi J, Sun C, Bayer A, Hritz J, Ryman KD, Klimstra WB. Natural variation in the heparan sulfate binding domain of the eastern equine encephalitis virus E2 glycoprotein alters interactions with cell surfaces and virulence in mice.. J Virol 2013 Aug;87(15):8582-90.
    doi: 10.1128/JVI.00937-13pmc: PMC3719831pubmed: 23720725google scholar: lookup
  20. Aguilar PV, Adams AP, Wang E, Kang W, Carrara AS, Anishchenko M, Frolov I, Weaver SC. Structural and nonstructural protein genome regions of eastern equine encephalitis virus are determinants of interferon sensitivity and murine virulence.. J Virol 2008 May;82(10):4920-30.
    doi: 10.1128/JVI.02514-07pmc: PMC2346730pubmed: 18353963google scholar: lookup
  21. Aguilar PV, Leung LW, Wang E, Weaver SC, Basler CF. A five-amino-acid deletion of the eastern equine encephalitis virus capsid protein attenuates replication in mammalian systems but not in mosquito cells.. J Virol 2008 Jul;82(14):6972-83.
    doi: 10.1128/JVI.01283-07pmc: PMC2446984pubmed: 18480443google scholar: lookup
  22. Pandya J, Gorchakov R, Wang E, Leal G, Weaver SC. A vaccine candidate for eastern equine encephalitis virus based on IRES-mediated attenuation.. Vaccine 2012 Feb 8;30(7):1276-82.
  23. Trobaugh DW, Sun C, Dunn MD, Reed DS, Klimstra WB. Rational design of a live-attenuated eastern equine encephalitis virus vaccine through informed mutation of virulence determinants.. PLoS Pathog 2019 Feb;15(2):e1007584.
  24. Meshram CD, Shiliaev N, Frolova EI, Frolov I. Hypervariable Domain of nsP3 of Eastern Equine Encephalitis Virus Is a Critical Determinant of Viral Virulence.. J Virol 2020 Aug 17;94(17).
    doi: 10.1128/JVI.00617-20pmc: PMC7431797pubmed: 32581106google scholar: lookup
  25. Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, Hayes DB, Walker ED. Host selection by Culex pipiens mosquitoes and West Nile virus amplification.. Am J Trop Med Hyg 2009 Feb;80(2):268-78.
    doi: 10.4269/ajtmh.2009.80.268pubmed: 19190226google scholar: lookup
  26. Turell MJ, Dohm DJ, Sardelis MR, Oguinn ML, Andreadis TG, Blow JA. An update on the potential of north American mosquitoes (Diptera: Culicidae) to transmit West Nile Virus.. J Med Entomol 2005 Jan;42(1):57-62.
    doi: 10.1093/jmedent/42.1.57pubmed: 15691009google scholar: lookup
  27. Richards SL, Ponnusamy L, Unnasch TR, Hassan HK, Apperson CS. Host-feeding patterns of Aedes albopictus (Diptera: Culicidae) in relation to availability of human and domestic animals in suburban landscapes of central North Carolina.. J Med Entomol 2006 May;43(3):543-51.
  28. Edman JD, Webber LA, Kale HW 2nd. Host-feeding patterns of Florida mosquitoes. II. Culiseta.. J Med Entomol 1972 Sep 30;9(5):429-34.
    doi: 10.1093/jmedent/9.5.429pubmed: 4404140google scholar: lookup
  29. Molaei G, Andreadis TG, Armstrong PM, Diuk-Wasser M. Host-feeding patterns of potential mosquito vectors in Connecticut, U.S.A.: molecular analysis of bloodmeals from 23 species of Aedes, Anopheles, Culex, Coquillettidia, Psorophora, and Uranotaenia.. J Med Entomol 2008 Nov;45(6):1143-51.
  30. Burkett-Cadena ND, Bingham AM, Hunt B, Morse G, Unnasch TR. Ecology of Culiseta Melanura and Other Mosquitoes (Diptera: Culicidae) from Walton County, FL, During Winter Period 2013-2014.. J Med Entomol 2015 Sep;52(5):1074-82.
    doi: 10.1093/jme/tjv087pmc: PMC4668758pubmed: 26336227google scholar: lookup
  31. Wilke ABB, Vasquez C, Medina J, Carvajal A, Petrie W, Beier JC. Community Composition and Year-round Abundance of Vector Species of Mosquitoes make Miami-Dade County, Florida a Receptive Gateway for Arbovirus entry to the United States.. Sci Rep 2019 Jun 19;9(1):8732.
    doi: 10.1038/s41598-019-45337-2pmc: PMC6584581pubmed: 31217547google scholar: lookup
  32. Blosser EM, Lord CC, Stenn T, Acevedo C, Hassan HK, Reeves LE, Unnasch TR, Burkett-Cadena ND. Environmental Drivers of Seasonal Patterns of Host Utilization by Culiseta melanura (Diptera: Culicidae) in Florida.. J Med Entomol 2017 Sep 1;54(5):1365-1374.
    doi: 10.1093/jme/tjx140pmc: PMC5850491pubmed: 28874017google scholar: lookup
  33. Bartlett MS. Deterministic and stochastic models for recurrent epidemics. University of Manchester; 1956.
  34. van den Driessche P. Reproduction numbers of infectious disease models.. Infect Dis Model 2017 Aug;2(3):288-303.
    doi: 10.1016/j.idm.2017.06.002pmc: PMC6002118pubmed: 29928743google scholar: lookup
  35. Grassly NC, Fraser C. Seasonal infectious disease epidemiology.. Proc Biol Sci 2006 Oct 7;273(1600):2541-50.
    doi: 10.1098/rspb.2006.3604pmc: PMC1634916pubmed: 16959647google scholar: lookup
  36. Darbro JM, Harrington LC. Avian defensive behavior and blood-feeding success of the West Nile vector mosquito, Culex pipiens. Behavioral Ecology 2007;18(4):750–757.
    doi: 10.1093/beheco/arm043google scholar: lookup
  37. Allen LJ, van den Driessche P. Relations between deterministic and stochastic thresholds for disease extinction in continuous- and discrete-time infectious disease models.. Math Biosci 2013 May;243(1):99-108.
    doi: 10.1016/j.mbs.2013.02.006pubmed: 23458509google scholar: lookup
  38. Allen LJ, Lahodny GE Jr. Extinction thresholds in deterministic and stochastic epidemic models.. J Biol Dyn 2012;6:590-611.
    doi: 10.1080/17513758.2012.665502pubmed: 22873607google scholar: lookup
  39. Lahodny GE Jr, Gautam R, Ivanek R. Estimating the probability of an extinction or major outbreak for an environmentally transmitted infectious disease.. J Biol Dyn 2015;9 Suppl 1:128-55.
    doi: 10.1080/17513758.2014.954763pubmed: 25198247google scholar: lookup
  40. Mbogo RW, Luboobi LS, Odhiambo JW. A stochastic model for malaria transmission dynamics. Journal of Applied Mathematics 2018;2018.
    doi: 10.1155/2018/2439520google scholar: lookup
  41. Heberlein-Larson LA, Tan Y, Stark LM, Cannons AC, Shilts MH, Unnasch TR, Das SR. Complex Epidemiological Dynamics of Eastern Equine Encephalitis Virus in Florida.. Am J Trop Med Hyg 2019 May;100(5):1266-1274.
    doi: 10.4269/ajtmh.18-0783pmc: PMC6493969pubmed: 30860014google scholar: lookup
  42. Hribar LJ. Dataset for mosquito collections on Big Pine Key, Florida, USA.. Data Brief 2019 Oct;26:104516.
    doi: 10.1016/j.dib.2019.104516pmc: PMC6811921pubmed: 31667279google scholar: lookup
  43. Wonham M, Lewis M. A comparative analysis of models for West Nile virus. In: Mathematical epidemiology. Springer; 2008. p. 365–390.
  44. Giordano BV, Bartlett SK, Falcon DA, Lucas RP, Tressler MJ, Campbell LP. Mosquito Community Composition, Seasonal Distributions, and Trap Bias in Northeastern Florida.. J Med Entomol 2020 Sep 7;57(5):1501-1509.
    doi: 10.1093/jme/tjaa053pubmed: 32206774google scholar: lookup
  45. Molaei G, Andreadis TG, Armstrong PM, Anderson JF, Vossbrinck CR. Host feeding patterns of Culex mosquitoes and West Nile virus transmission, northeastern United States.. Emerg Infect Dis 2006 Mar;12(3):468-74.
    doi: 10.3201/eid1203.051004pmc: PMC3291451pubmed: 16704786google scholar: lookup
  46. Kraft D. A software package for sequential quadratic programming. Deutsche Forschungs- und Versuchsanstalt für Luft- und Raumfahrt Köln: Forschungsbericht. Wiss. Berichtswesen d. DFVLR 1988.
  47. Wales DJ, Scheraga HA. Global optimization of clusters, crystals, and biomolecules.. Science 1999 Aug 27;285(5432):1368-72.
    doi: 10.1126/science.285.5432.1368pubmed: 10464088google scholar: lookup
  48. Olson B, Hashmi I, Molloy K, Shehu A. Basin Hopping as a General and Versatile Optimization Framework for the Characterization of Biological Macromolecules. Advances in Artificial Intelligence (16877470) 2012.
    doi: 10.1155/2012/674832google scholar: lookup
  49. Chowell G. Fitting dynamic models to epidemic outbreaks with quantified uncertainty: A Primer for parameter uncertainty, identifiability, and forecasts.. Infect Dis Model 2017 Aug;2(3):379-398.
    doi: 10.1016/j.idm.2017.08.001pmc: PMC5726591pubmed: 29250607google scholar: lookup
  50. Hartemink NA, Davis SA, Reiter P, Hubálek Z, Heesterbeek JA. Importance of bird-to-bird transmission for the establishment of West Nile virus.. Vector Borne Zoonotic Dis 2007 Winter;7(4):575-84.
    doi: 10.1089/vbz.2006.0613pubmed: 17979541google scholar: lookup
  51. Wonham MJ, de-Camino-Beck T, Lewis MA. An epidemiological model for West Nile virus: invasion analysis and control applications.. Proc Biol Sci 2004 Mar 7;271(1538):501-7.
    doi: 10.1098/rspb.2003.2608pmc: PMC1691622pubmed: 15129960google scholar: lookup
  52. Kain MP, Bolker BM. Can existing data on West Nile virus infection in birds and mosquitos explain strain replacement?. Ecosphere 2017;8(3):e01684.
  53. Keeling MJ, Rohani P. Modeling infectious diseases in humans and animals. Princeton University; 2008.
  54. Keeling MJ, Grenfell BT. Understanding the persistence of measles: reconciling theory, simulation and observation.. Proc Biol Sci 2002 Feb 22;269(1489):335-43.
    doi: 10.1098/rspb.2001.1898pmc: PMC1690899pubmed: 11886620google scholar: lookup
  55. Agarwal A, Sharma AK, Sukumaran D, Parida M, Dash PK. Two novel epistatic mutations (E1:K211E and E2:V264A) in structural proteins of Chikungunya virus enhance fitness in Aedes aegypti.. Virology 2016 Oct;497:59-68.
    doi: 10.1016/j.virol.2016.06.025pubmed: 27423270google scholar: lookup
  56. Berman JJ. Taxonomic guide to infectious diseases: understanding the biologic classes of pathogenic organisms. Academic Press; 2019.
  57. Bustamante DM, Lord CC. Sources of error in the estimation of mosquito infection rates used to assess risk of arbovirus transmission.. Am J Trop Med Hyg 2010 Jun;82(6):1172-84.
    doi: 10.4269/ajtmh.2010.09-0323pmc: PMC2877431pubmed: 20519620google scholar: lookup
  58. Whitehorn J, Yacoub S. Global warming and arboviral infections.. Clin Med (Lond) 2019 Mar;19(2):149-152.
  59. Bremermann HJ, Pickering J. A game-theoretical model of parasite virulence.. J Theor Biol 1983 Feb 7;100(3):411-26.
    doi: 10.1016/0022-5193(83)90438-1pubmed: 6834864google scholar: lookup
  60. Porco TC, Lloyd-Smith JO, Gross KL, Galvani AP. The effect of treatment on pathogen virulence.. J Theor Biol 2005 Mar 7;233(1):91-102.
    doi: 10.1016/j.jtbi.2004.09.009pmc: PMC7126720pubmed: 15615623google scholar: lookup
  61. Bonney PJ, Malladi S, Boender GJ, Weaver JT, Ssematimba A, Halvorson DA, Cardona CJ. Spatial transmission of H5N2 highly pathogenic avian influenza between Minnesota poultry premises during the 2015 outbreak.. PLoS One 2018;13(9):e0204262.
  62. Grewar JD, Kotze JL, Parker BJ, van Helden LS, Weyer CT. An entry risk assessment of African horse sickness virus into the controlled area of South Africa through the legal movement of equids.. PLoS One 2021;16(5):e0252117.
  63. Beveroth TA, Ward MP, Lampman RL, Ringia AM, Novak RJ. Changes in seroprevalence of West Nile virus across Illinois in free-ranging birds from 2001 through 2004.. Am J Trop Med Hyg 2006 Jan;74(1):174-9.
    doi: 10.4269/ajtmh.2006.74.174pubmed: 16407365google scholar: lookup
  64. Levine RS, Mead DG, Hamer GL, Brosi BJ, Hedeen DL, Hedeen MW, McMillan JR, Bisanzio D, Kitron UD. Supersuppression: Reservoir Competency and Timing of Mosquito Host Shifts Combine to Reduce Spillover of West Nile Virus.. Am J Trop Med Hyg 2016 Nov 2;95(5):1174-1184.
    doi: 10.4269/ajtmh.15-0809pmc: PMC5094236pubmed: 27503511google scholar: lookup
  65. Maquart M, Boyer S, Rakotoharinome VM, Ravaomanana J, Tantely ML, Heraud JM, Cardinale E. High Prevalence of West Nile Virus in Domestic Birds and Detection in 2 New Mosquito Species in Madagascar.. PLoS One 2016;11(1):e0147589.
  66. Williams JE, Young OP, Watts DM. Relationship of density of Culiseta melanura mosquitoes to infection of wild birds with eastern and western equine encephalitis viruses.. J Med Entomol 1974 Jul 15;11(3):352-4.
    doi: 10.1093/jmedent/11.3.352pubmed: 4153042google scholar: lookup
  67. HAYES RO, DANIELS JB, ANDERSON KS, PARSONS MA, MAXFIELD HK, LAMOTTE LC. Detection of eastern encephalitis virus and antibody in wild and domestic birds in Massachusetts.. Am J Hyg 1962 Mar;75:183-9.
  68. for Disease Control C, Prevention. Eastern Equine Enchephalitis- Statistics & Maps; 2021. Available from: https://www.cdc.gov/easternequineencephalitis/statistics-maps/index.html.

Citations

This article has been cited 0 times.