Spatial and temporal distribution of West Nile virus in horses in Israel (1997-2013)–from endemic to epidemics.
Abstract: With the rapid global spread of West Nile virus (WNV) and the endemic state it has acquired in new geographical areas, we hereby bring a thorough serological investigation of WNV in horses in a longstanding endemic region, such as Israel. This study evaluates the environmental and demographic risk factors for WNV infection in horses and suggests possible factors associated with the transition from endemic to epidemic state. West Nile virus seroprevalence in horses in Israel was determined throughout a period of more than a decade, before (1997) and after (2002 and 2013) the massive West Nile fever outbreak in humans and horses in 2000. An increase in seroprevalence was observed, from 39% (113/290) in 1997 to 66.1% (547/827) in 2002 and 85.5% (153/179) in 2013, with persistent significantly higher seroprevalence in horses situated along the Great Rift Valley (GRV) area, the major birds' migration route in Israel. Demographic risk factors included age and breed of the horse. Significantly lower spring precipitation was observed during years with increased human incidence rate that occurred between 1997-2007. Hence, we suggest referring to Israel as two WNV distinct epidemiological regions; an endemic region along the birds' migration route (GRV) and the rest of the country which perhaps suffers from cyclic epidemics. In addition, weather conditions, such as periods of spring drought, might be associated with the transition from endemic state to epidemic state of WNV.
Publication Date: 2014-11-17 PubMed ID: 25402217PubMed Central: PMC4234662DOI: 10.1371/journal.pone.0113149Google 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.
The research article explores the geographical and temporal spread of the West Nile virus (WNV) in horses in Israel over a period of 16 years (1997 – 2013), detailing the transition from the disease being endemic to reaching epidemic levels.
Study Objectives and Method
- The study aims to present a detailed serological report of the West Nile virus detected in horses in Israel, where the virus has been endemic for an extended time.
- The researchers assessed environmental and demographic risk factors for WNV infection in horses and suggested factors that could be linked to the virus’s transition from endemic to epidemic status.
- Seroprevalence of the West Nile virus in horses in Israel was tracked over more than a decade, before (1997) and after (2002 and 2013) an extensive West Nile fever outbreak in humans and horses that occurred in 2000.
Findings and Implications
- There was a noted increase in seroprevalence from 39% in 1997 to 85.5% in 2013.
- The higher prevalence was consistently found in horses located along the Great Rift Valley (GRV), which aligns with the major bird migration route in Israel. This part of the country is described as an endemic region for WNV.
- Risk factors associated with WNV infection included the age and breed of the horse, suggesting that certain horse breeds and mature horses might be more susceptible to the virus.
- Regarding the correlation with environmental factors, significantly lower spring precipitation was noted in years with increased human incidence rate, which occurred between 1997 and 2007. This suggests that drier spring weather could be associated with virus spreading, possibly facilitating the transition from endemic to epidemic spread.
- The research proposes that Israel could be considered as twofold in terms of WNV epidemiology, with an endemic region along the bird migration route and the rest of the country experiencing cyclic epidemics.
Concluding Remarks
- This study provides insights into the factors influencing the spread of WNV from a localized, endemic spread to a widespread epidemic.
- It emphasizes the potential role of factors like demographic characteristics, geography, climate conditions, and bird migration routes in disease spread.
- The findings could inform public health strategies, predicting and potentially mitigating WNV outbreaks in horses and possibly in humans as well.
Cite This Article
APA
Aharonson-Raz K, Lichter-Peled A, Tal S, Gelman B, Cohen D, Klement E, Steinman A.
(2014).
Spatial and temporal distribution of West Nile virus in horses in Israel (1997-2013)–from endemic to epidemics.
PLoS One, 9(11), e113149.
https://doi.org/10.1371/journal.pone.0113149 Publication
Researcher Affiliations
- Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
- Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
- School of Public Health, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, 39040, Israel.
- Kimron Veterinary Institute, Bet-Dagan, 50250, Israel.
- School of Public Health, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, 39040, Israel.
- Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
- Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
MeSH Terms
- Age Factors
- Animals
- Antibodies, Viral / blood
- Environment
- Enzyme-Linked Immunosorbent Assay / veterinary
- Epidemics / veterinary
- Female
- Horse Diseases / epidemiology
- Horse Diseases / virology
- Horses
- Humans
- Israel / epidemiology
- Male
- Risk Factors
- Seasons
- Seroepidemiologic Studies
- West Nile Fever / epidemiology
- West Nile Fever / pathology
- West Nile Fever / veterinary
- West Nile virus / immunology
Conflict of Interest Statement
The authors have declared that no competing interests exist.
References
This article includes 54 references
- Beck C, Jimenez-Clavero MA, Leblond A, Durand B, Nowotny N, Leparc-Goffart I, Zientara S, Jourdain E, Lecollinet S. Flaviviruses in Europe: complex circulation patterns and their consequences for the diagnosis and control of West Nile disease.. Int J Environ Res Public Health 2013 Nov 12;10(11):6049-83.
- Smithburn KC, Hughes TP, Burke AW, Paul JH. A Neurotropic Virus Isolated from the Blood of a Native of Uganda. Am J Trop Med 20: 471–492.
- Murgue B, Murri S, Triki H, Deubel V, Zeller HG. West Nile in the Mediterranean basin: 1950-2000.. Ann N Y Acad Sci 2001 Dec;951:117-26.
- SCHMIDT JR, ELMANSOURY HK. NATURAL AND EXPERIMENTAL INFECTION OF EGYPTIAN EQUINES WITH WEST NILE VIRUS.. Ann Trop Med Parasitol 1963 Dec;57:415-27.
- Akov Y, Goldwasser R. Prevalence of antibodies to arboviruses in various animals in Israel.. Bull World Health Organ 1966;34(6):901-9.
- Cantile C, Di Guardo G, Eleni C, Arispici M. Clinical and neuropathological features of West Nile virus equine encephalomyelitis in Italy.. Equine Vet J 2000 Jan;32(1):31-5.
- Murgue B, Murri S, Zientara S, Durand B, Durand JP, Zeller H. West Nile outbreak in horses in southern France, 2000: the return after 35 years.. Emerg Infect Dis 2001 Jul-Aug;7(4):692-6.
- Steinman A, Banet C, Sutton GA, Yadin H, Hadar S, Brill A. Clinical signs of West Nile virus encephalomyelitis in horses during the outbreak in Israel in 2000.. Vet Rec 2002 Jul 13;151(2):47-9.
- Centers for Disease Control, Atlanta, GA. Available: http://www.cdc.gov/westnile/resources/pdfs/cummulative/99_2012_NeuroInvasivebyYear.pdf.
- Monath TP. Vaccines against diseases transmitted from animals to humans: a one health paradigm.. Vaccine 2013 Nov 4;31(46):5321-38.
- Klee AL, Maidin B, Edwin B, Poshni I, Mostashari F, Fine A, Layton M, Nash D. Long-term prognosis for clinical West Nile virus infection.. Emerg Infect Dis 2004 Aug;10(8):1405-11.
- Paz S, Malkinson D, Green MS, Tsioni G, Papa A, Danis K, Sirbu A, Ceianu C, Katalin K, Ferenczi E, Zeller H, Semenza JC. Permissive summer temperatures of the 2010 European West Nile fever upsurge.. PLoS One 2013;8(2):e56398.
- Rios LM, Sheu JJ, Day JF, Maruniak JE, Seino K, Zaretsky H, Long MT. Environmental risk factors associated with West Nile virus clinical disease in Florida horses.. Med Vet Entomol 2009 Dec;23(4):357-66.
- Jansen CC, Ritchie SA, van den Hurk AF. The role of Australian mosquito species in the transmission of endemic and exotic West Nile virus strains.. Int J Environ Res Public Health 2013 Aug 19;10(8):3735-52.
- Kramer LD, Styer LM, Ebel GD. A global perspective on the epidemiology of West Nile virus.. Annu Rev Entomol 2008;53:61-81.
- Lindsey NP, Staples JE, Delorey MJ, Fischer M. Lack of evidence of increased West Nile virus disease severity in the United States in 2012.. Am J Trop Med Hyg 2014 Jan;90(1):163-8.
- Bakonyi T, Ivanics E, Erdélyi K, Ursu K, Ferenczi E, Weissenböck H, Nowotny N. Lineage 1 and 2 strains of encephalitic West Nile virus, central Europe.. Emerg Infect Dis 2006 Apr;12(4):618-23.
- Bakonyi T, Ferenczi E, Erdélyi K, Kutasi O, Csörgő T, Seidel B, Weissenböck H, Brugger K, Bán E, Nowotny N. Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009.. Vet Microbiol 2013 Jul 26;165(1-2):61-70.
- Papa A, Bakonyi T, Xanthopoulou K, Vázquez A, Tenorio A, Nowotny N. Genetic characterization of West Nile virus lineage 2, Greece, 2010.. Emerg Infect Dis 2011 May;17(5):920-2.
- Paz S, Semenza JC. Environmental drivers of West Nile fever epidemiology in Europe and Western Asia--a review.. Int J Environ Res Public Health 2013 Aug 9;10(8):3543-62.
- Sambri V, Capobianchi M, Charrel R, Fyodorova M, Gaibani P, Gould E, Niedrig M, Papa A, Pierro A, Rossini G, Varani S, Vocale C, Landini MP. West Nile virus in Europe: emergence, epidemiology, diagnosis, treatment, and prevention.. Clin Microbiol Infect 2013 Aug;19(8):699-704.
- Weinberger M, Pitlik SD, Gandacu D, Lang R, Nassar F, Ben David D, Rubinstein E, Izthaki A, Mishal J, Kitzes R, Siegman-Igra Y, Giladi M, Pick N, Mendelson E, Bin H, Shohat T. West Nile fever outbreak, Israel, 2000: epidemiologic aspects.. Emerg Infect Dis 2001 Jul-Aug;7(4):686-91.
- Malkinson M, Banet C, Weisman Y, Pokamunski S, King R, Drouet MT, Deubel V. Introduction of West Nile virus in the Middle East by migrating white storks.. Emerg Infect Dis 2002 Apr;8(4):392-7.
- Anis E, Grotto I, Mendelson E, Bin H, Orshan L, Gandacu D, Warshavsky B, Shinar E, Slater PE, Lev B. West Nile fever in Israel: the reemergence of an endemic disease.. J Infect 2014 Feb;68(2):170-5.
- Reiter P. West Nile virus in Europe: understanding the present to gauge the future.. Euro Surveill 2010 Mar 11;15(10):19508.
- Banet-Noach C, Malkinson M, Brill A, Samina I, Yadin H, Weisman Y, Pokamunski S, King R, Deubel V, Stram Y. Phylogenetic relationships of West Nile viruses isolated from birds and horses in Israel from 1997 to 2001.. Virus Genes 2003;26(2):135-41.
- Banet-Noach C, Simanov L, Malkinson M. Direct (non-vector) transmission of West Nile virus in geese.. Avian Pathol 2003 Oct;32(5):489-94.
- Cohen DI, Davidovici BB, Smetana Z, Balicer RD, Klement E, Mendelson E, Green MS. Seroepidemiology of Varicella zoster in Israel prior to large-scale use of varicella vaccines.. Infection 2006 Aug;34(4):208-13.
- Nir Y, Lasowski Y, Avivi A, Cgoldwasser R. Survey for antibodies to arboviruses in the serum of various animals in Israel during 1965-1966.. Am J Trop Med Hyg 1969 May;18(3):416-22.
- Chowers MY, Green MS, Bin H, Weinberger M, Schlaeffer F, Pitlik S, Bishara J, Kaufman Z, Dichtiar R, Mendelson E, Segev S. Post-epidemic serosurvey of West Nile fever in Israel.. Eur J Clin Microbiol Infect Dis 2005 Dec;24(12):851-3.
- Sanchini A, Donoso-Mantke O, Papa A, Sambri V, Teichmann A, Niedrig M. Second international diagnostic accuracy study for the serological detection of West Nile virus infection.. PLoS Negl Trop Dis 2013;7(4):e2184.
- Ziegler U, Skrypnyk A, Keller M, Staubach C, Bezymennyi M, Damiani AM, Osterrieder N, Groschup MH. West nile virus antibody prevalence in horses of Ukraine.. Viruses 2013 Oct 4;5(10):2469-82.
- Ziegler U, Angenvoort J, Klaus C, Nagel-Kohl U, Sauerwald C, Thalheim S, Horner S, Braun B, Kenklies S, Tyczka J, Keller M, Groschup MH. Use of competition ELISA for monitoring of West Nile virus infections in horses in Germany.. Int J Environ Res Public Health 2013 Jul 24;10(8):3112-20.
- Armstrong PM, Andreadis TG. Eastern equine encephalitis virus--old enemy, new threat.. N Engl J Med 2013 May 2;368(18):1670-3.
- Paz S. The West Nile Virus outbreak in Israel (2000) from a new perspective: the regional impact of climate change.. Int J Environ Health Res 2006 Feb;16(1):1-13.
- Stanke C, Kerac M, Prudhomme C, Medlock J, Murray V. Health effects of drought: a systematic review of the evidence.. PLoS Curr 2013 Jun 5;5.
- Wang G, Minnis RB, Belant JL, Wax CL. Dry weather induces outbreaks of human West Nile virus infections.. BMC Infect Dis 2010 Feb 24;10:38.
- Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, Haramis L, Goldberg TL, Kitron UD. Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA.. Parasit Vectors 2010 Mar 19;3(1):19.
- Shaman J, Day JF, Komar N. Hydrologic conditions describe West Nile virus risk in Colorado.. Int J Environ Res Public Health 2010 Feb;7(2):494-508.
- Shaman J, Day JF, Stieglitz M. Drought-induced amplification and epidemic transmission of West Nile virus in southern Florida.. J Med Entomol 2005 Mar;42(2):134-41.
- Savage HM, Ceianu C, Nicolescu G, Karabatsos N, Lanciotti R, Vladimirescu A, Laiv L, Ungureanu A, Romanca C, Tsai TF. Entomologic and avian investigations of an epidemic of West Nile fever in Romania in 1996, with serologic and molecular characterization of a virus isolate from mosquitoes.. Am J Trop Med Hyg 1999 Oct;61(4):600-11.
- Platonov AE, Shipulin GA, Shipulina OY, Tyutyunnik EN, Frolochkina TI, Lanciotti RS, Yazyshina S, Platonova OV, Obukhov IL, Zhukov AN, Vengerov YY, Pokrovskii VI. Outbreak of West Nile virus infection, Volgograd Region, Russia, 1999.. Emerg Infect Dis 2001 Jan-Feb;7(1):128-32.
- Beasley DW, Barrett AD, Tesh RB. Resurgence of West Nile neurologic disease in the United States in 2012: what happened? What needs to be done?. Antiviral Res 2013 Jul;99(1):1-5.
- Barzon L, Pacenti M, Franchin E, Squarzon L, Lavezzo E, Cattai M, Cusinato R, Palù G. The complex epidemiological scenario of West Nile virus in Italy.. Int J Environ Res Public Health 2013 Sep 30;10(10):4669-89.
- Jourdain E, Toussaint Y, Leblond A, Bicout DJ, Sabatier P, Gauthier-Clerc M. Bird species potentially involved in introduction, amplification, and spread of West Nile virus in a Mediterranean wetland, the Camargue (Southern France).. Vector Borne Zoonotic Dis 2007 Spring;7(1):15-33.
- Pradier S, Lecollinet S, Leblond A. West Nile virus epidemiology and factors triggering change in its distribution in Europe.. Rev Sci Tech 2012 Dec;31(3):829-44.
- Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P. Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands.. Emerg Infect Dis 2007 Mar;13(3):365-72.
- Leshem Y, Yom-Tov Y. Routes of migrating soaring birds. Ibis 140: 41–52.
- WORK TH, HURLBUT HS, TAYLOR RM. Indigenous wild birds of the Nile Delta as potential West Nile virus circulating reservoirs.. Am J Trop Med Hyg 1955 Sep;4(5):872-88.
- Murgue B, Zeller H, Deubel V. The ecology and epidemiology of West Nile virus in Africa, Europe and Asia.. Curr Top Microbiol Immunol 2002;267:195-221.
- Cabre O, Grandadam M, Marié JL, Gravier P, Prangé A, Santinelli Y, Rous V, Bourry O, Durand JP, Tolou H, Davoust B. West Nile Virus in horses, sub-Saharan Africa.. Emerg Infect Dis 2006 Dec;12(12):1958-60.
- Cohen D, Zaide Y, Karasenty E, Schwarz M, LeDuc JW, Slepon R, Ksiazek TG, Shemer J, Green MS. Prevalence of antibodies to West Nile fever, sandfly fever Sicilian, and sandfly fever Naples viruses in healthy adults in Israel.. Public Health Rev 1999;27(1-3):217-30.
- Ahmadnejad F, Otarod V, Fallah MH, Lowenski S, Sedighi-Moghaddam R, Zavareh A, Durand B, Lecollinet S, Sabatier P. Spread of West Nile virus in Iran: a cross-sectional serosurvey in equines, 2008-2009.. Epidemiol Infect 2011 Oct;139(10):1587-93.
- Epp T, Waldner C, West K, Townsend H. Factors associated with West Nile virus disease fatalities in horses.. Can Vet J 2007 Nov;48(11):1137-45.
Citations
This article has been cited 13 times.- Sun H, Lesio J, Chen Q. Development of Antibody-Based Therapeutics Against West Nile Virus in Plants.. Methods Mol Biol 2023;2585:211-225.
- Ganzenberg S, Sieg M, Ziegler U, Pfeffer M, Vahlenkamp TW, Hörügel U, Groschup MH, Lohmann KL. Seroprevalence and Risk Factors for Equine West Nile Virus Infections in Eastern Germany, 2020.. Viruses 2022 May 30;14(6).
- Defilippo F, Dottori M, Lelli D, Chiari M, Cereda D, Farioli M, Chianese R, Cerioli MP, Faccin F, Canziani S, Trogu T, Sozzi E, Moreno A, Lavazza A, Restelli U. Assessment of the Costs Related to West Nile Virus Monitoring in Lombardy Region (Italy) between 2014 and 2018.. Int J Environ Res Public Health 2022 May 3;19(9).
- Selim A, Megahed A, Kandeel S, Alouffi A, Almutairi MM. West Nile virus seroprevalence and associated risk factors among horses in Egypt.. Sci Rep 2021 Oct 22;11(1):20932.
- de Heus P, Kolodziejek J, Hubálek Z, Dimmel K, Racher V, Nowotny N, Cavalleri JV. West Nile Virus and Tick-Borne Encephalitis Virus Are Endemic in Equids in Eastern Austria.. Viruses 2021 Sep 19;13(9).
- 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).
- Schvartz G, Farnoushi Y, Berkowitz A, Edery N, Hahn S, Steinman A, Lublin A, Erster O. Molecular characterization of the re-emerging West Nile virus in avian species and equids in Israel, 2018, and pathological description of the disease.. Parasit Vectors 2020 Oct 22;13(1):528.
- Tirosh-Levy S, Steinman A, Minderigiu A, Arieli O, Savitski I, Fleiderovitz L, Edery N, Schvartz G, Mazuz ML. High Exposure to Toxoplasma gondii and Neospora Spp. in Donkeys in Israel: Serological Survey and Case Reports.. Animals (Basel) 2020 Oct 19;10(10).
- Schvartz G, Tirosh-Levy S, Erester O, Shenhar R, Levy H, Bazanow B, Gelman B, Steinman A. Exposure of Horses in Israel to West Nile Virus and Usutu Virus.. Viruses 2020 Sep 28;12(10).
- Johnson N, Fernández de Marco M, Giovannini A, Ippoliti C, Danzetta ML, Svartz G, Erster O, Groschup MH, Ziegler U, Mirazimi A, Monteil V, Beck C, Gonzalez G, Lecollinet S, Attoui H, Moutailler S. Emerging Mosquito-Borne Threats and the Response from European and Eastern Mediterranean Countries.. Int J Environ Res Public Health 2018 Dec 7;15(12).
- Tirosh-Levy S, Gelman B, Zivotofsky D, Quraan L, Khinich E, Nasereddin A, Abdeen Z, Steinman A. Seroprevalence and risk factor analysis for exposure to equine encephalosis virus in Israel, Palestine and Jordan.. Vet Med Sci 2017 May;3(2):82-90.
- 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.
- Marcantonio M, Rizzoli A, Metz M, Rosà R, Marini G, Chadwick E, Neteler M. Identifying the environmental conditions favouring West Nile Virus outbreaks in Europe.. PLoS One 2015;10(3):e0121158.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists