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Phylogenetic analysis of West Nile virus: first report of lineage 1 in donkey in Turkey

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Abstract

West Nile virus (WNV), a member of the Flaviviridae, is a major arbovirus that causes West Nile fever. Previous data showed the prevalence of the WNV serologically and molecular in Turkey, and the presence of lineage 1 in horses and humans has been reported. This is the first notification of partial phylogeny of WNV detected in donkeys in the northeast of Turkey (on the Iranian border). Blood serum samples collected from 25 donkeys without clinical symptoms were tested by RT-PCR. Sequence analysis of the sample detected as positive was performed. Multiple sequence alignments of reference sequences taken from GenBank were performed using the ClustalW method using the MEGA6 program. Partial nucleotide sequences of the capsid gene coding region revealed that the strains are closely related to viruses of lineage 1, clade 1a. According to the phylogenetic tree, the TUR/Igdir/donkey strain was included in the same cluster as the strain (KJ958922) previously obtained from horses in Turkey and the strain (GQ851658) from the Central African Republic. This study is the first report to show the circulation of WNV lineage 1 in donkeys in Turkey.

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References

  • Akiner, M.M., Öztürk, M., Başer, A.B., Günay, F., Hacioglu, S., Brinkmann, A., Emenat, N., Alten, B., Ozkul, A., Nitsche, A., Linton, Y.M., and Ergunay, K., 2019. Arboviral screening of invasive Aedes species in northeastern Turkey: West Nile virus circulation and detection of insect-only viruses. Plos Neglected Tropical Diseases, 13: e0007334. https://doi.org/10.1371/journal.pntd.0007334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andreadis, T.G., 2012. The contribution of Culex pipiens complex mosquitoes to transmission and persistence of West Nile virus in North America. Journal of the American Mosquito Control Association, 28(4): 137–152. https://doi.org/10.2987/8756-971X-28.4s.137

    Article  PubMed  Google Scholar 

  • Azmi, K., Tirosh-Levy, S., Manasrah, M., Mizrahi, R., Nasereddin, A., Al-Jawabreh, A., Ereqat, S., Abdeen, Z., Lustig, Y., Gelman, B., Schvartz, G., and Steinman, A., 2017. West Nile Virus: Seroprevalence in Animals in Palestine and Israel. Vector-Borne Zoonotic Diseases, 17: 558–566. https://doi.org/10.1089/vbz.2016.2090

    Article  PubMed  Google Scholar 

  • Baba, S.S., NNnadi, O.D., Hamman, K.D., Saidu, A., El-Yuguda, A., and Oderinde, B.S., 2014. Preliminary Study on the Prevalence of West Nile Virus Antibody among Horses, Donkeys and Camels in Borno State, Nigeria. Journal of Medical Virology, 4(3): 39–45. https://doi.org/10.21092/jav.v3i2.43

    Article  Google Scholar 

  • Bakhshi, H., Mousson, L., Vazeille, M., Zakeri, S., Raz, A., Lamballerie, X., Dinparast-Djadid, N., and Failloux, A.B., 2020. High Transmission Potential of West Nile Virus Lineage 1 for Cx. pipiens s.l. of Iran. Viruses, 12(4): 397. https://doi.org/10.3390/v12040397

  • Bakonyi, T., Ivanics, E., Erdélyi, K., Ursu, K., Ferenczi, E., Weissenböck, H., and Nowotny, N., 2006. Lineage 1 and 2 strains of encephalitic West Nile virus, Central Europe. Emerging Infectious Diseases, 12(4): 618–623. https://stacks.cdc.gov/view/cdc/16130. Accessed 16/03/2021

  • Blitvich, B.J., 2008. Transmission dynamics and changing epidemiology of West Nile virus. Animal Health Research Reviews, 9(1): 71–86. https://doi.org/10.1017/S1466252307001430

    Article  PubMed  Google Scholar 

  • Burke, D., and Monath, T., 2001. In: Knipe DM, Howley PM, (Eds): Flaviviruses. Lippincott William & Wilkins, Philadelphia. Fields virology, 1043–126.

  • Caraballo, H., and King, K., 2014. Emergency department management of mosquito-borne illness: Malaria, dengue, and West Nile virus. Emergency Medicine Practice, 16(5): 1–23. https://www.ebmedicine.net/topics/infectious-disease/mosquito-borne. Accessed 16/03/2021

  • Chambers, T.J., Hahn, C.S., Galler, R., Rice, C.M., 1990. Flavivirus genome organization, expression, and replication. Annual Review of Microbiology, 44: 649–88.

    Article  CAS  Google Scholar 

  • Davoust, B., Maquart, M., Roqueplo, C., Gravier, P., Sambou, M., Mediannikov, O., and Leparc-Goffart, I., 2016. Serological Survey of West Nile Virus in Domestic Animals from Northwest Senegal. Vector-Borne Zoonotic Diseases, 16(5): 359–361. https://doi.org/10.1089/vbz.2015.1881

    Article  PubMed  Google Scholar 

  • Ergunay, K., Bakonyi, T., Nowotny, N., and Ozkul, A., 2015. Close relationship between West Nile virus from Turkey and lineage 1 strain from Central African Republic. Emerging Infectious Diseases, 21(2): 352–355. https://doi.org/10.3201/eid2102.141135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ergunay, K., Gunay, F., Erisoz Kasap, O., Oter, K., Gargari, S., Karaoglu, T., Tezcan, S., Cabalar, M., Yildirim, Y., Emekdas, G., Alten, B., and Ozkul, A., 2014. Serological, molecular and entomological surveillance demonstrates widespread circulation of West Nile virus in Turkey. Plos Neglected Tropical Diseases, 8: e3028. https://doi.org/10.1371/journal.pntd.0003028

    Article  PubMed  PubMed Central  Google Scholar 

  • Ergunay, K., Gunay, F., Oter, K., Kasap, O.E., Orsten, S., Akkutay, A.Z., Erdem, H., Ozkul, A., and Alten, B., 2013. Arboviral surveillance of field-collected mosquitoes reveals circulation of West Nile virus lineage 1 strains in Eastern Thrace, Turkey. Vector-Borne and Zoonotic Diseases, 13(10): 744–752. https://doi.org/10.1089/vbz.2012.1288

    Article  PubMed  Google Scholar 

  • Ergunay, K., Litzba, N., Brinkmann, A., Gunay, F., Sarıkaya, Y., Kar, S., Orsten, S., Oter, K., Domingo, C., Erisoz Kasap, O., Özkul, A., Mitchell, L., Nitsche, A., Alten, B., and Linton, Y.M., 2017. Co-circulation of West Nile virus and distinct insect-specific flaviviruses in Turkey. Parasites & Vectors, 10(1): 149. https://parasitesandvectors.biomedcentral.com/articles/https://doi.org/10.1186/s13071-017-2087-7

  • Fall, G., Di Paola, N., Faye, M., Dia, M., Freire, C.C.M., Loucoubar, C., Zanotto, P.M.A., Faye, O., and Sall, A.A., 2017. Biological and phylogenetic characteristics of West African lineages of West Nile virus. Plos Neglected Tropical Diseases, 11: e0006078. https://doi.org/10.1371/journal.pntd.0006078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farfan-Ale, J.A., Loroño-Pino, M.A., Garcia-Rejon, J.E., Hovav, E., Powers, A.M., Lin, M., Dorman, K.S., Platt, K.B., Bartholomay, L.C., Soto, V., Beaty, B.J., Lanciotti, R.S., and Blitvich B.J., 2009. Detection of RNA from a Novel West Nile-like Virus and High Prevalence of an Insect-specific Flavivirus in Mosquitoes in the Yucatan Peninsula of Mexico. American Journal of Tropical Medicine and Hygiene, 80: 85–95. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2663380/. Accessed 16/03/2021

  • Gould, E., Zanotto, P.M.A., and Holmes, E.C., 1997. The genetic evolution of flaviviruses. In: Saluzzo JF, Dodet B (Eds): Factors in the emergence of arbovirus diseases. Elsevier, Paris, France. pp. 51–63.

    Google Scholar 

  • Gunay, F., Alten, B., Simsek, F., Aldemir, A., and Linton, Y.M., 2015. Barcoding Turkish Culex mosquitoes to facilitate arbovirus vector incrimination studies reveals hidden diversity and new potential vectors. Acta tropica, 143: 112–20. https://doi.org/10.1016/j.actatropica.2014.10.013

    Article  PubMed  Google Scholar 

  • Hall, R., Scherret, J.H., and Mackenzie, J.S., 2001. Kunjin virus: an Australian variant of West Nile? Annals of the New York Academy of Sciences, 951: 153–60. https://doi.org/10.1111/j.1749-6632.2001.tb02693.x

    Article  CAS  PubMed  Google Scholar 

  • Hayes, E.B., and Gubler, D.J., 2006. West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annual Review of Medicine, 57:181–94. https://doi.org/10.1146/annurev.med.57.121304.131418

    Article  CAS  PubMed  Google Scholar 

  • Kalaycioglu, H., Korukluoglu, G., Ozkul, A., Oncul, O., Tosun, S., Karabay, O., Gozalan, A., Uyar, Y., Caglayık, D.Y., Atasoylu, G., Altas, A.B., Yolbakan, S., Ozden, T.N., Bayrakdar, F., Sezak, N., Pelıtlı, T.S., Kurtcebe, Z.O., Aydın, E., and Ertek, M., 2012. Emergence of West Nile virus infections in humans in Turkey, 2010 to 2011. Euro Surveillance, 17(21): 20182. https://www.eurosurveillance.org/content/https://doi.org/10.2807/ese.17.21.20182-en

  • Kale, M., Gur, S., Mamak, N., and Yavru, S. 2017. Serological Investigation of West Nile Virus Infection in Domestic Horses and Donkeys in Turkey. Pakistan Veterinary Journal, 37(1): 51–54. http://www.pvj.com.pk/pdf-files/37_1/51-54.pdf. Accessed 16/03/2021

  • Kramer, L.D., Styer, L.M., and Ebel, G.D., 2008. A global perspective on the epidemiology of West Nile virus. Annual Review of Entomology, 53: 61–81. https://doi.org/10.1146/annurev.ento.53.103106.093258

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K., 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35: 1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lafri, I., Prat, C.M., Bitam, I., Gravier, P., Besbaci, M., Zeroual, F., Ben-Mahdi, M.H., Davoust, B., and Leparc-Goffart, I., 2017. Seroprevalence of West Nile virus antibodies in equids in the North-East of Algeria and detection of virus circulation in 2014. Comparative Immunology, Microbiology & Infectious Diseases, 50: 8–12. https://doi.org/10.1016/j.cimid.2016.11.005

    Article  Google Scholar 

  • Lanciotti, R.S., Kerst, A.J., Nasci, R.S., Godsey, M.S., Mitchell, C.J., Savage, H.M., Komar, N., Panella, N.A., Allen, B.C., Volpe, K.E., Davis, B.S., and Roehrig, J.T., 2000. Rapid detection of West Nile Virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. Journal of Clinical Microbiology, 38: 4066–4071. https://jcm.asm.org/content/38/11/4066. Accessed 16/03/2021

  • Nei, M., and Kumar, S., 2000. Molecular Evolution and Phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Ocal, M., Önder, H., Arsava, E.M., Alp, S., Ozkul, A., and Ergünay, K., 2013. A case of central nervous system ınfection due to West Nile Virus lineage-1 in Ankara province, Turkey. Mikrobiyoloji Bulteni, 47(1): 164–72. http://www.mikrobiyolbul.org/linkout.aspx?pmid=23390915. Accessed 16/03/2021 

  • Ozkul, A., Ergunay, K., Koysuren, A., Alkan, F., Arsava, E.M., Tezcan, S., Emekdas, G., Hacioglu, S., Turan, M., and Us, D., 2013. Concurrent occurrence of human and equine West Nile virus infections in Central Anatolia, Turkey: the first evidence for circulation of lineage 1 viruses. International Journal of Infectious Diseases, 17: 546–551. https://doi.org/10.1016/j.ijid.2013.02.005

    Article  Google Scholar 

  • Ozkul, A., Yildirim, Y., Pinar, D., Akcali, A., Yilmaz, V., and Colak, D., 2006. Serological evidence of West Nile Virus (WNV) in mammalian species in Turkey. Epidemiology and Infection, 134:826–829. https://doi.org/10.1017/S0950268805005492

    Article  CAS  PubMed  Google Scholar 

  • Pachler, K., Lebl, K., Berer, D., Rudolf, I., Hubalek, Z., and Nowotny, N., 2014. Putative new West Nile virus lineage in Uranotaenia unguiculata mosquitoes, Austria, 2013. Emerging Infectious Diseases, 20(12): 2119–22. https://wwwnc.cdc.gov/eid/article/20/12/14-0921_article. Accessed 16/03/2021

  • Shah-Hosseini, N., Chinikar, S., Ataei, B., Fooks, A.R., and Groschup, M.H., 2014. Phylogenetic analysis of West Nile virus genome, Iran. Emerging Infectious Diseases, 20: 1419–21. https://wwwnc.cdc.gov/eid/article/20/8/13-1321_article. Accessed 16/03/2021

  • Smithburn, K., Hughes, T., Burke, A., and Paul, J., 1940. A neurotropic virus isolated from the blood of a native of Uganda. American Journal of Tropical Medicine and Hygiene, 1: 471–492.

    Article  Google Scholar 

  • Venter, M., Human, S., Zaayman, D., Gerdes, G.H., Williams, J., Steyl, J., Leman, P.A., Paweska, J.T., Setzkorn, H., Rous, G., Murray, S., Parker, R., Donnellan, C., and Swanepoel, R., 2009. Lineage 2 West Nile virus as cause of fatal neurological disease in horses, South Africa. Emerging Infectious Diseases, 15: 877–84. https://wwwnc.cdc.gov/eid/article/15/6/08-1515_article

  • Ward, M.P., Levy, M., Thacker, H.L., Ash, M., Norman, S.K.L., Moore, G.E., and Webb, P.W., 2004. Investigation of an outbreak of encephalomyelitis caused by West Nile virus in 136 horses. Javma-Journal of The American Veterinary Medical Association, 225: 84–9. https://doi.org/10.2460/javma.2004.225.84

    Article  Google Scholar 

  • Yildirim, Y., Yilmaz, V., Yazici, K., Ozic, C., and Ozkul, A., 2018. Molecular and serological investigation of West Nile virus (WNV) infection in donkeys, horses and native geese in Turkey. Revue de Médecine Vétérinaire, 169(4–6): 87–92. https://www.revmedvet.com/2018/RMV169_87_92.pdf. Accessed 16/03/2021

  • Zehender, G., Veo, C., Ebranati, E., Carta, V., Rovida, F., Percivalle, E., Moreno, A., Lelli, D., Calzolari, M., Lavazza, A., Chiapponi, C., Baioni, L., Capelli, G., Ravagnan, S., Da Rold, G., Lavezzo, E., Palu, G., Baldanti, F., Barzon, L., and Galli, M., 2017. Reconstructing the recent West Nile virus lineage 2 epidemic in Europe and Italy using discrete and continuous phylogeography. PLoS One, 12: e0179679. https://doi.org/10.1371/journal.pone.0179679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zohaib, A., Saqib, M., Beck, C., Hussain, M.H., Lowenski, S., Lecollinet, S., Sial., A, Asi, M.N., Mansoor, M.K., Saqalein, M., Sajid, M.S., Ashfaq, K., Muhammad, G., and Cao, S., 2015. High prevalence of West Nile virus in equines from the two provinces of Pakistan. Epidemiology and Infection, 143(9): 1931-1935. https://doi.org/10.1017/S0950268814002878

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Virology, Faculty of Veterinary Medicine, Mehmet Akif Ersoy University, Burdur, 15100, Turkey

    Yakup Yıldırım

  2. Department of Virology, Faculty of Veterinary Medicine, Kafkas University, Kars, Turkey

    Volkan Yılmaz

  3. Vocational School of Technical Sciences, Ardahan University, Ardahan, Turkey

    Kemal Yazıcı

  4. Department of Bioengineering, Faculty of Engineering-Architecture, Kafkas University, Kars, Turkey

    Cem Öziç

  5. Department of Virology, Faculty of Veterinary Medicine, Ankara University, Ankara, Turkey

    Aykut Ozkul

  6. Department of Virology, Izmir/Bornova Veterinary Control Institute, Izmir, Turkey

    Abdurrahman Anıl Çağırgan

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  1. Yakup Yıldırım
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  2. Volkan Yılmaz
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  3. Kemal Yazıcı
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  4. Cem Öziç
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  5. Aykut Ozkul
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Contributions

YY and VY conceived and designed research. YY, VY, and KY conducted experiments. CÖ and AO contributed new reagents or analytical tools. YY and AAÇ analyzed data. YY and AAÇ wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Yakup Yıldırım.

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Approval was obtained from the animal testing local ethics committee of University Erciyes. The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

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Yıldırım, Y., Yılmaz, V., Yazıcı, K. et al. Phylogenetic analysis of West Nile virus: first report of lineage 1 in donkey in Turkey. Trop Anim Health Prod 53, 453 (2021). https://doi.org/10.1007/s11250-021-02892-z

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