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Veterinary sciences2024; 11(5); 209; doi: 10.3390/vetsci11050209

Seroprevalence of West Nile Virus among Equids in Bulgaria in 2022 and Assessment of Some Risk Factors.

Abstract: The aim of this study was to analyze the seroprevalence of West Nile virus (WNV) among equids in Bulgaria, confirm the results of a competitive ELISA versus the virus neutralization test (VNT) and investigate some predisposing factors for WNV seropositivity. A total of 378 serum samples from 15 provinces in northern and southern Bulgaria were tested. The samples originated from 314 horses and 64 donkeys, 135 males and 243 females, aged from 1 to 30 years. IgG and IgM antibodies against WNV protein E were detected by ELISA. ELISA-positive samples were additionally tested via VNT for WNV and Usutu virus. Thirty-five samples were WNV-positive by ELISA (9.26% [CI = 6.45-12.88]), of which 15 were confirmed by VNT; hence, the seroprevalence was 3.97% (CI = 2.22-6.55). No virus-neutralizing antibodies to Usutu virus were detected among the 35 WNV-ELISA-positive equids in Bulgaria. When compared with VNT, ELISA showed 100.0% sensitivity and 94.5% specificity. A statistical analysis showed that the risk factors associated with WNV seropositivity were the region ( < 0.0001), altitude of the locality ( < 0.0001), type of housing ( < 0.0001) and breed ( = 0.0365). The results of the study demonstrate, albeit indirectly, that WNV circulates among equids in northern and southern Bulgaria, indicating that they could be suitable sentinel animals for predicting human cases and determining the risk in these areas or regions of the country.
Publication Date: 2024-05-09 PubMed ID: 38787181PubMed Central: PMC11126025DOI: 10.3390/vetsci11050209Google Scholar: Lookup
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  • Journal Article

Summary

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Overview

  • This study evaluated the presence of West Nile virus antibodies in horses and donkeys across Bulgaria in 2022 to understand how widespread the virus is among these animals.
  • It compared two testing methods for detecting antibodies and analyzed factors that might influence the likelihood of animals being infected.

Study Objectives

  • Determine the seroprevalence (presence of virus-specific antibodies) of West Nile virus (WNV) among equids (horses and donkeys) in Bulgaria.
  • Compare the results of a competitive ELISA test with the virus neutralization test (VNT), which is considered the gold standard, to assess the accuracy of ELISA.
  • Investigate risk factors that might affect WNV seropositivity such as geographic region, altitude, housing type, and breed.

Sample Collection and Testing Methods

  • Collected 378 serum samples from 314 horses and 64 donkeys across 15 provinces of northern and southern Bulgaria.
  • The animals were of various ages (1 to 30 years old) and included 135 males and 243 females.
  • Used ELISA to detect IgG and IgM antibodies against the WNV envelope protein (protein E), indicating past or recent infections.
  • All ELISA-positive samples were further tested with VNT to confirm the presence of neutralizing antibodies specific to WNV and to rule out cross-reactivity with Usutu virus, another related flavivirus.

Key Findings

  • 9.26% of animals tested positive for WNV antibodies by ELISA.
  • Of the ELISA-positive samples, 15 were confirmed positive by VNT, resulting in an overall confirmed seroprevalence of 3.97%.
  • No neutralizing antibodies against Usutu virus were detected among the ELISA-positive samples, indicating that the antibodies detected were specific to WNV.
  • ELISA testing showed perfect sensitivity (100%) and high specificity (94.5%) compared to VNT, suggesting ELISA is a reliable initial screening tool.

Risk Factors for WNV Seropositivity

  • Region: Significant differences in seropositivity were observed between different geographic areas (p < 0.0001), indicating some regions had higher exposure risks.
  • Altitude: The altitude of the location where the animals lived was also associated with WNV antibody presence (p < 0.0001), possibly reflecting environmental or vector-related factors.
  • Type of housing: Whether animals were kept indoors, outdoors, or in mixed housing was significantly related to their risk of seropositivity (p < 0.0001), likely due to exposure to mosquito vectors.
  • Breed: The breed of the equids showed a smaller but statistically significant association with seroprevalence (p = 0.0365), suggesting genetic or management differences may impact infection risk.

Implications and Conclusions

  • The study provides strong evidence that West Nile virus is actively circulating among equids in both northern and southern Bulgaria.
  • Equids, especially horses and donkeys, could serve as sentinel animals — early indicators of WNV activity — which is valuable for predicting and managing human risk.
  • The findings support the use of ELISA as a screening method in surveillance programs with follow-up confirmation by VNT.
  • Identifying risk factors such as location, altitude, and housing helps target prevention efforts and vector control measures more effectively.

Cite This Article

APA
Rusenova N, Rusenov A, Chervenkov M, Sirakov I. (2024). Seroprevalence of West Nile Virus among Equids in Bulgaria in 2022 and Assessment of Some Risk Factors. Vet Sci, 11(5), 209. https://doi.org/10.3390/vetsci11050209

Publication

ISSN: 2306-7381
NlmUniqueID: 101680127
Country: Switzerland
Language: English
Volume: 11
Issue: 5
PII: 209

Researcher Affiliations

Rusenova, Nikolina
  • Department of Veterinary Microbiology, Infectious and Parasitic Diseases, Faculty of Veterinary Medicine, Trakia University, 6000 Stara Zagora, Bulgaria.
Rusenov, Anton
  • Department of Internal Diseases, Faculty of Veterinary Medicine, Trakia University, 6000 Stara Zagora, Bulgaria.
Chervenkov, Mihail
  • Faculty of Veterinary Medicine, University of Forestry, 1797 Sofia, Bulgaria.
  • Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria.
Sirakov, Ivo
  • Department of Medical Microbiology, Faculty of Medicine, Medical University-Sofia, 2 Zdrave Str., 1431 Sofia, Bulgaria.

Grant Funding

  • 5 FVM/02.06.2022 / Trakia University
  • BG-RRP-2.004-0006 / Bulgarian Ministry of Education and Science

Conflict of Interest Statement

The authors declare no conflicts of interest.

References

This article includes 60 references
  1. Postler TS, Beer M, Blitvich BJ, Bukh J, de Lamballerie X, Drexler JF, Imrie A, Kapoor A, Karganova GG, Lemey P. Renaming of the genus Flavivirus to Orthoflavivirus and extension of binomial species names within the family Flaviviridae. Arch. Virol. 2023;168:224.
    doi: 10.1007/s00705-023-05835-1pubmed: 37561168google scholar: lookup
  2. Khare B, Kuhn RJ. The Japanese Encephalitis Antigenic Complex Viruses: From Structure to Immunity. Viruses 2022;14:2213.
    doi: 10.3390/V14102213pmc: PMC9607441pubmed: 36298768google scholar: lookup
  3. Ciota AT. West Nile Virus and Its Vectors. Curr. Opin. Insect Sci. 2017;22:28–36.
    doi: 10.1016/J.COIS.2017.05.002pubmed: 28805636google scholar: lookup
  4. Mencattelli G, Ndione MHD, Rosà R, Marini G, Diagne CT, Diagne MM, Fall G, Faye O, Diallo M, Faye O. Epidemiology of West Nile virus in Africa: An underestimated threat. PLoS Negl. Trop. Dis. 2022;16:e0010075.
  5. Bakonyi T, Ivanics É, Erdélyi K, Ursu K, Ferenczi E, Weissenböck H, Nowotny N. Lineage 1 and 2 Strains of Encephalitic West Nile Virus, Central. Emerg. Infect. Dis. 2006;12:618–623.
    doi: 10.3201/EID1204.051379pmc: PMC3294705pubmed: 16704810google scholar: lookup
  6. Fall G, Di Paola N, Faye M, Dia M, Freire CCDM, Loucoubar C, Zanotto PMDA, Faye O, Sall AA. Biological and Phylogenetic Characteristics of West African Lineages of West Nile Virus. PLoS Negl. Trop. Dis. 2017;11:e0006078.
  7. Blitvich BJ. Transmission Dynamics and Changing Epidemiology of West Nile Virus. Anim. Health Res. Rev. 2008;9:71–86.
    doi: 10.1017/S1466252307001430pubmed: 18348742google scholar: lookup
  8. Fesce E, Marini G, Rosà R, Lelli D, Cerioli MP, Chiari M, Farioli M, Ferrari N. Understanding West Nile Virus Transmission: Mathematical Modelling to Quantify the Most Critical Parameters to Predict Infection Dynamics. PLoS Negl. Trop. Dis. 2023;17:e0010252.
  9. Bowen RA, Nemeth NM. Experimental Infections with West Nile Virus. Curr. Opin. Infect. Dis. 2007;20:293–297.
    doi: 10.1097/QCO.0B013E32816B5CADpubmed: 17471040google scholar: lookup
  10. Yeung MW, Shing E, Nelder M, Sander B. Epidemiologic and Clinical Parameters of West Nile Virus Infections in Humans: A Scoping Review. BMC Infect. Dis. 2017;17:609.
    pmc: PMC5588625pubmed: 28877682
  11. Schwarz ER, Long MT. Comparison of West Nile Virus Disease in Humans and Horses: Exploiting Similarities for Enhancing Syndromic Surveillance. Viruses 2023;15:1230.
    doi: 10.3390/V15061230pmc: PMC10303507pubmed: 37376530google scholar: lookup
  12. Leblond A, Lecollinet S. Clinical Screening of Horses and Early Warning for West Nile Virus. Equine Vet. Educ. 2017;29:325–327.
    doi: 10.1111/EVE.12571google scholar: lookup
  13. Schmidt JR, El Mansoury HK. Natural and Experimental Infection of Egyptian Equines with West Nile Virus. Ann. Trop. Med. Parasitol. 1963;57:415–427.
  14. WOAH Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 12th Edition. 2023. [(accessed on 12 February 2024)]. Available online: https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/A_summry.htm.
  15. Paré J, Moore A. West Nile Virus in Horses—What Do You Need to Know to Diagnose the Disease?. Can. Vet. J. 2018;59:1119.
    pmc: PMC6135266pubmed: 30510321
  16. Dauphin G, Zientara S, Zeller H, Murgue B. West Nile: Worldwide Current Situation in Animals and Humans. Comp. Immunol. Microbiol. Infect. Dis. 2004;27:343–355.
    doi: 10.1016/J.CIMID.2004.03.009pubmed: 15225984google scholar: lookup
  17. Beck C, Lowenski S, Durand B, Bahuon C, Zientara S, Lecollinet S. Improved Reliability of Serological Tools for the Diagnosis of West Nile Fever in Horses within Europe. PLoS Negl. Trop. Dis. 2017;11:e0005936.
  18. García-Bocanegra I, Arenas-Montes A, Napp S, Jaén-Téllez JA, Fernández-Morente M, Fernández-Molera V, Arenas A. Seroprevalence and Risk Factors Associated to West Nile Virus in Horses from Andalusia, Southern Spain. Vet. Microbiol. 2012;160:341–346.
    doi: 10.1016/J.VETMIC.2012.06.027pubmed: 22776513google scholar: lookup
  19. 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;14:1191.
    pmc: PMC9229339pubmed: 35746662
  20. Bergmann F, Trachsel DS, Stoeckle SD, Sierra JB, Lübke S, Groschup MH, Gehlen H, Ziegler U. Seroepidemiological Survey of West Nile Virus Infections in Horses from Berlin/Brandenburg and North Rhine-Westphalia, Germany. Viruses 2022;14:243.
    pmc: PMC8877243pubmed: 35215837
  21. Medić S, van den Hoven R, Petrović T, Lupulović D, Nowotny N. Serological Evidence of West Nile Virus Infection in the Horse Population of Northern Serbia. J. Infect. Dev. Ctries. 2014;8:914–918.
    doi: 10.3855/JIDC.3885pubmed: 25022304google scholar: lookup
  22. Rusenova N, Rusenov A, Monaco F. A Retrospective Study on the Seroprevalence of West Nile Virus Among Donkeys and Mules in Bulgaria. Vector-Borne Zoonotic Dis. 2024.
    doi: 10.1089/VBZ.2023.0095pubmed: 38294797google scholar: lookup
  23. Christova I, Panayotova E, Tchakarova S, Taseva E, Trifonova I, Gladnishka T. A Nationwide Seroprevalence Screening for West Nile Virus and Tick-Borne Encephalitis Virus in the Population of Bulgaria. J. Med. Virol. 2017;89:1875–1878.
    doi: 10.1002/JMV.24855pubmed: 28504357google scholar: lookup
  24. Panayotova E, Christova I, Trifonova I, Taseva E, Gladnishka T, Ivanova V. Seroprevalence of West Nile Virus in Bulgaria, 2018. Probl. Infect. Parasit. Dis. 2019;47:15–17.
    doi: 10.58395/PIPD.V47I2.6google scholar: lookup
  25. Trifonova I, Christova I, Ivanova-Aleksandrova N, Gladnishka T, Ivanova V, Panayotova E, Taseva E, Dimitrov D, Marinov M, Kamenov G. Survey of Borrelia Burgdorferi Sensu Lato and West Nile Fever Virus in Wild Birds in Bulgaria. Biologia 2022;77:3519–3524.
  26. Christova I, Papa A, Trifonova I, Panayotova E, Pappa S, Mikov O. West Nile Virus Lineage 2 in Humans and Mosquitoes in Bulgaria, 2018–2019. J. Clin. Virol. 2020;127:104365.
    doi: 10.1016/J.JCV.2020.104365pubmed: 32305885google scholar: lookup
  27. Di Gennaro A, Lorusso A, Casaccia C, Conte A, Monaco F, Savini G. Serum Neutralization Assay Can Efficiently Replace Plaque Reduction Neutralization Test for Detection and Quantitation of West Nile Virus Antibodies in Human and Animal Serum Samples. Clin. Vaccine Immunol. 2014;21:1460–1462.
    doi: 10.1128/CVI.00426-14pmc: PMC4266345pubmed: 25100824google scholar: lookup
  28. Nahm FS. Receiver Operating Characteristic Curve: Overview and Practical Use for Clinicians. Korean J Anesth. 2022;75:25–36.
    doi: 10.4097/KJA.21209pmc: PMC8831439pubmed: 35124947google scholar: lookup
  29. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the Areas under Two or More Correlated Receiver Operating Characteristic Curves: A Nonparametric Approach. Biometrics 1988;44:845.
    doi: 10.2307/2531595pubmed: 3203132google scholar: lookup
  30. Bargaoui R, Lecollinet S, Lancelot R. Mapping the Serological Prevalence Rate of West Nile Fever in Equids, Tunisia. Transbound. Emerg. Dis. 2015;62:55–66.
    doi: 10.1111/TBED.12077pubmed: 23906318google scholar: lookup
  31. Pérez-Ramírez E, Cano-Gómez C, Llorente F, Vodica A, Veljović L, Toklikishvilli N, Sherifi K, Sghaier S, Omani A, Kustura A. Evaluation of West Nile Virus Diagnostic Capacities in Veterinary Laboratories of the Mediterranean and Black Sea Regions. Pathogens 2020;9:1038.
    doi: 10.3390/PATHOGENS9121038pmc: PMC7763240pubmed: 33322276google scholar: lookup
  32. Sirakov I, Peshev R, Koburova K, Ivanova T, Chervenkov M. Development of Blocking Enzyme-Linked Immunosorbent Assay for Detection of Caprine Herpesvirus 1 Antibodies in Bulgaria. Comptes Rendus L’académie Bulg. Des Sci. 2016;69:1159–1166.
  33. Vilibic-Cavlek T, Savic V, Petrovic T, Toplak I, Barbic L, Petric D, Tabain I, Hrnjakovic-Cvjetkovic I, Bogdanic M, Klobucar A. Emerging Trends in the Epidemiology of West Nile and Usutu Virus Infections in Southern Europe. Front. Vet. Sci. 2019;6:501214.
    pmc: PMC6908483pubmed: 31867347
  34. Llorente F, García-Irazábal A, Pérez-Ramírez E, Cano-Gómez C, Sarasa M, Vázquez A, Jiménez-Clavero MÁ. Influence of Flavivirus Co-Circulation in Serological Diagnostics and Surveillance: A Model of Study Using West Nile, Usutu and Bagaza Viruses. Transbound. Emerg. Dis. 2019;66:2100–2106.
    doi: 10.1111/TBED.13262pubmed: 31150146google scholar: lookup
  35. Gómez-Vicente E, Garcia R, Calatrava E, Olivares Duran MJ, Gutiérrez-Bautista JF, Rodriguez-Granger J, Cobo F, Navarro Mari JM, Sampedro-Martinez A. Comparative Evaluation of Chemiluminescent Immunoassay and Enzyme-Linked Immunosorbent Assays for the Diagnosis of West Nile Virus Infections. J. Pathol. Microbiol. Immunol. 2022;130:215–220.
    doi: 10.1111/APM.13207pubmed: 35060204google scholar: lookup
  36. Michev T, Profirov L, Karaivanov N, Michev B. Migration of Soaring Birds over Bulgaria. Acta Zool Bulg. 2012;64:33–41.
  37. Srihi H, Chatti N, Ben Mhadheb M, Gharbi J, Abid N. Phylodynamic and Phylogeographic Analysis of the Complete Genome of the West Nile Virus Lineage 2 (WNV-2) in the Mediterranean Basin. BMC Ecol. Evol. 2021;21:183.
    doi: 10.1186/S12862-021-01902-Wpmc: PMC8477494pubmed: 34579648google scholar: lookup
  38. Baymakova M, Popov G, Tsanev I, Andonova R. West Nile Fever: The Epidemiological Situations in Europe, USA and Bulgaria. Gen. Med. 2019;21:52–58.
  39. Bakonyi T, Haussig JM. West Nile Virus Keeps on Moving up in Europe. Eurosurveillance 2020;25:2001938.
  40. Kirov P, Iancu I, Panayotova E, Imre M, Herman V, Gligor A, Petrov R, Alexandrova R, Hristov H, Abudalleh A. International Seminar of Ecology—2023. IBER-BAS/USB Sofia, Bulgaria: 2023. First Serological Evidence for West Nile Virus Infection Amongst Horse Population in Northern Bulgaria; p. 49.
  41. Ludu Oslobanu LE, Pâslaru A, Savuţa G. West Nile Virus Seroprevalence in Horses from Romania: First Step in the Infection Risk Assessment. Bull. Univ. Agric. Sci. Vet. Med. Cluj-Napoca. Vet. Med. 2015;72:34–36.
  42. Savuta G, Ionescu A, Anita A, Anita D, Ludu L. Serological Investigations of WNV Infection in Horses from the South-East of Romania. Bull. Univ. Agric. Sci. Vet. Med. Cluj-Napoca. Vet. Med. 2007;64:527–530.
  43. Vasić A, Răileanu C, Körsten C, Vojinović D, Manić M, Urošević A, Nikolić N, Dulović O, Tews BA, Petrović T. West Nile Virus in the Republic of Serbia-Diagnostic Performance of Five Serological Tests in Dog and Horse Sera. Transbound. Emerg. Dis. 2022;69:e2506–e2515.
    doi: 10.1111/TBED.14593pubmed: 35538046google scholar: lookup
  44. Petrović T, Šekler M, Petrić D, Vidanović D, Debeljak Z, Lazić G, Lupulović D, Kavran M, Samojlović M, Ignjatović Ćupina A. Intensive West Nile Virus Circulation in Serbia in 2018-Results of Integrated Surveillance Program. Pathogens 2021;10:1294.
    doi: 10.3390/PATHOGENS10101294pmc: PMC8540029pubmed: 34684243google scholar: lookup
  45. Ergunay K, Gunay F, Erisoz Kasap O, Oter K, Gargari S, Karaoglu T, Tezcan S, Cabalar M, Yildirim Y, Emekdas G. Serological, Molecular and Entomological Surveillance Demonstrates Widespread Circulation of West Nile Virus in Turkey. PLoS Negl. Trop. Dis. 2014;8:e3028.
  46. Yilderim Y, Yilmaz V, Yazici K, Ozic C, Özkul A. Molecular and Serological Investigation of West Nile Virus (WNV) Infection in Donkeys, Horses and Native Geese in Turkey. Rev. Med. Vet. 2018;169:87–92.
  47. Afentoglou P-M, Patsoula E, Komarou E. Epidemiological Data for WNV in Greece during Last Decade. Hell. J. Nurs. Sci. 2023;16:36.
    doi: 10.24283/hjns.202336google scholar: lookup
  48. European Centre for Disease Prevention and Control Epidemiological Update: West Nile Virus Transmission Season in Europe. 2023. [(accessed on 27 February 2024)]. Available online: https://www.ecdc.europa.eu/en/news-events/epidemiological-update-west-nile-virus-transmission-season-europe-2023-0.
  49. de Heus P, Kolodziejek J, Hubálek Z, Dimmel K, Racher V, Nowotny N, Cavalleri JMV. West Nile Virus and Tick-Borne Encephalitis Virus Are Endemic in Equids in Eastern Austria. Viruses 2021;13:1873.
    pmc: PMC8473302pubmed: 34578454
  50. Heinz FX, Stiasny K, Holzmann H, Kundi M, Six W, Wenk M, Kainz W, Essl A, Kunz C. Emergence of Tick-Borne Encephalitis in New Endemic Areas in Austria: 42 Years of Surveillance. Eurosurveillance 2015;20:21077.
  51. Bogovic P, Strle F. Tick-Borne Encephalitis: A Review of Epidemiology, Clinical Characteristics, and Management. World J. Clin Cases 2015;3:430.
    doi: 10.12998/WJCC.V3.I5.430pmc: PMC4419106pubmed: 25984517google scholar: lookup
  52. Mohareb E, Christova I, Soliman A, Younan R, Kantardjiev T. Tick-Borne Encephalitis in Bulgaria, 2009 to 2012. Eurosurveillance 2013;18:20635.
    pubmed: 24256889
  53. Angenvoort J, Brault AC, Bowen RA, Groschup MH. West Nile Viral Infection of Equids. Vet. Microbiol. 2013;167:168–180.
  54. Castillo-Olivares J, Wood J. West Nile Virus Infection of Horses. Vet. Res. 2004;35:467–483.
    doi: 10.1051/VETRES:2004022pubmed: 15236677google scholar: lookup
  55. Abutarbush SM, Al-Majali AM. West Nile Virus Infection in Horses in Jordan: Clinical Cases, Seroprevalence and Risk Factors. Transbound. Emerg. Dis. 2014;61:1–6.
    doi: 10.1111/TBED.12191pubmed: 24393369google scholar: lookup
  56. Aharonson-Raz K, Lichter-Peled A, Tal S, Gelman B, Cohen D, Klement E, Steinman A. Spatial and Temporal Distribution of West Nile Virus in Horses in Israel (1997–2013)—From Endemic to Epidemics. PLoS ONE 2014;9:e113149.
  57. Alzuheir I, Fayyad A, Jalboush N, Abdallah R, Abutarbush S, Gharaibeh M, Bdarneh M, Khraim N, Helal MA, Helal BA. Seroprevalence and Risk Factors of West Nile Virus Infection in Veterinarians and Horses in Northern Palestine. Vet. World 2021;14:1246.
  58. 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;11:20932.
    doi: 10.1038/s41598-021-00449-6pmc: PMC8536702pubmed: 34686730google scholar: lookup
  59. Hassine BT, De Massis F, Calistri P, Savini G, BelHaj Mohamed B, Ranen A, Di Gennaro A, Sghaier S, Hammami S. First Detection of Co-Circulation of West Nile and Usutu Viruses in Equids in the South-West of Tunisia. Transbound Emerg. Dis. 2014;61:385–389.
    doi: 10.1111/TBED.12259pubmed: 25065813google scholar: lookup
  60. Gangoso L, Aragonés D, Martínez-de la Puente J, Lucientes J, Delacour-Estrella S, Estrada Peña R, Montalvo T, Bueno-Marí R, Bravo-Barriga D, Frontera E. Determinants of the Current and Future Distribution of the West Nile Virus Mosquito Vector Culex Pipiens in Spain. Environ. Res. 2020;188:109837.
    doi: 10.1016/J.ENVRES.2020.109837pubmed: 32798954google scholar: lookup

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