West Nile virus infection in South-eastern Europe and in the Eastern Mediterranean area

Abstract

The West Nile virus (WNV) was identified in Uganda in 1937. This virus appeared in the Mediterranean area in the early 1950s, causing an outbreak in Egypt. Since then, WNV caused a series of outbreaks, in human and/or horses, especially in North-Africa and in the Middle East. In the last few decades, the lineage 1 of West Nile started to cause sporadic cases and outbreaks of West Nile fever and neuroinvasive disease in Southern and Eastern Europe, and a large outbreak was reported in Romania in 1997; then, sporadic cases continued to be reported in central and southern Europe for years. Since 2010, West Nile has reemerged in Europe and in the Mediterranean area. Studies of molecular epidemiology show a co-circulation of WNV lineage 1 and lineage 2 in several European countries. In particular, WNV lineage 2 appears now to be established in South-eastern Europe and in the Balkans. This suggests that WNV is continuously reintroduced in this geographical area. Specifically, the two lineages of WNV are dispersed throughout Europe after arriving through bird migration, following the western and the eastern routes. The latter route is likely to be involved in the emergence and reemergence of WNV infection in South-eastern Europe, where this viral infection represent an important public health challenge.

Keywords

• West Nile virus infections, South-eastern Europe, Eastern Mediterranean area, Emerging Infectious Diseases

West Nile virus infection in South-eastern Europe and in the Eastern Mediterranean area

Öz

Batı Nil virus (WNV) etkeni ilk olarak Uganda’da 1937 yılında identifiye edilmiştir. Bu virus 1950 yıllarının başında Mısır’da yaptığı salgınla birlikte Akdeniz bölgesinde kendini göstermiştir. O tarihten itibaren WNV özellikle Kuzey Afrika ve Orta-Doğu bölgesinde insan ve/veya atlarda birtakım salgınlara sebep olmuştur. Son bir kaç dekad içerisinde ise WNV-lineage 1 Güney Doğu ve Doğu Avrupa’da Batı Nil Virüs ateşi ve nöroinvazif hastalık şeklinde bir takım sporadik vakalar ve salgınlara sebep olmaya başlamıştır. Romanya’da 1997 yılında büyük bir salgın yaşanmış olup orta ve güney Avrupa’da yıllardır rapor edilmeye devam etmiştir. Son olarak 2010 yılından itibaren, Batı Nil Virüs enfeksiyonları Avrupa ve Akdeniz ülkelerinde yeniden önem kazanmıştır. Moleküler epidemiyoloji çalışmaları birçok Avrupa ülkesinde “WNV lineage 1 ve lineage 2’nin varlığını göstermiştir. Özellikle, WNV lineage 2’nin Güney doğu Avrupa ve Balkan ülkelerinde günümüzde dolaşmakta olduğu gözükmektedir. Bu WNV’nin sürekli olarak bu coğrafik bölgelerde yeniden önem kazandığını düşündürmektedir. Spesifik olarak, iki WNV türünün batı ve doğu yollarını takiben kuş göçleriyle birlikte tüm Avrupa’ya dağılmaktadır. Doğu hattı boyunca gerçekleşen kuş göçlerinin Güney doğu Avrupa’da önemli bir halk sağlığı problemi haline gelen WNV enfeksiyonlarının ortaya çıkması ve yeniden önem kazanmasında muhtemelen rol oynadığı değerlendirilmektedir

Anahtar Kelimeler

• Batı Nil virus infeksiyonu, Güney-doğu Avrupa, Doğu Akdeniz Bölgesi, Yeniden önem kazanan enfeksiyon hastalıkları

Kaynakça

1. Smithburn KC, Hughes TP, Burke AW, Paul JH. A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med 1940;20:471-492.
2. Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ. West Nile virus. Lancet 2002;2:519-529.
3. Tsai TF, Popovici F, Cernescu C, et al. West Nile encephalitis epidemic in southeastern Romania. Lancet 1998;352:767- 771.
4. Brinton, M.A., 2002. The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu Rev Micro- biol 56:371-402.
5. Kramer L.D, Styer L.M, Ebel G.D, 2008. A global perspective on the epidemiology of West Nile virus. Annu Rev Entomol 53:61-81.
6. Ciccozzi M, Peletto S, Cella E, et al. Epidemiological history and phylogeography of West Nile virus lineage 2. Infect Gen- et Evol 2013;17:46-50.
7. Granwehr BP, Lillibridge KM, Higgs S, et al. West Nile virus: where are we now? Lancet 2004;4:547-555.
8. Hubalek Z, Halouzka J. West Nile fever – a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 1999;5:643-650.

9. Zeller H.G, Schuffenecker I, 2004. West Nile virus: an over- view of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur J Clin Microbiol Infect Dis 23,147-156.
10. Hayes C.G, 2001. West Nile virus: Uganda, 1937, to New York City, 1999. Ann N Y Acad Sci 951:25-37.
11. Lanciotti RS, Roehrig JT, Deubel V, et al. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 1999;286:2333-2337.
12. Bardos V, Adamcova J, Dedei S, et al. Neutralizing antibod- ies against some neurotropic viruses determined in human sera in Albania. Journal of Hygiene, Epidemiology, Microbiol- ogy and Immunology (Prague) 1959;3:277-282.
13. Hannoun C, Panthier R, Mouchet J, Eouzan JP. Isolement en France du virus West Nile a partir de maladies et du vecteur Culex molestus Ficalbi. Compte Rendu de l’Academie de Sciences 1964 ; D259:4170-4172.
14. Chumakov MP, Belyaeva AP, Butenko AM. Isolation and study of an original virus from Hyalomma plumbeum plumbe- um ticks and from the blood of a febrile patient in te Astra- khan region (in Russian). Materialy XI Nauchnoi Sessii Insti- tuta Poliomielita I Virusnykh Encefalitov (Moskva) 1964:5-7.
15. Butenko AM, Chumakov MP, Stolbov DN. Serological and virological examinations in a natural focus of West Nile fever in the Astrakhan region (in Russian). Voprosy Medicinskoi Virusologii 1967;1:208-211.
16. Calistri P, Giovannini A, Hubalek Z, et al. Clinical and neuro- pathological features of West Nile virus equine encephalo- myelitis in Italy. Equine Vet J 2000;32:31-35.
17. Murgue B, Murri S, Triki H, et al. 2001. West Nile in the Medi- terranean basin: 1950-2000. Ann N Y Acad Sci 951,117-126.
18. Murgue B, Murri S, Zientara S, et al. West Nile outbreak in horses in Southern France, 2000: the return after 35 years. Emerg Infect Dis 2001;7:62-696.
19. Garcia-Bocanegra I, Jarn-Tellez JA, Napp S, et al. West Nile fever outbreak in horses and humans, Spain, 2010. Emerg Infect Dis 2011:2397-2398.
20. Feki I, Marrakchi C, Ben Hmida M, et al. Epidemic West Nile virus encephalitis in Tunisia. Neuroepidemiol 2005;24:1-7.
21. Han LL, Popovici F, Alexander JP, Jr, et al. Risk factors for West Nile virus infection and meningoencephalitis, Romania, 1996. J Infect Dis 1999;179:230-233.
22. Cernescu C, Nedelcu N-I, Tardei G, et al. Continued trans- mission of West Nile virus to humans in Southeastern Roma- nia, 1997-1998. J Infect Dis 2000;181:710-712.
23. Popovici F, Sarbu A, Nicolae O, et al. West Nile fever in a patient in Romania, August 2008: case report. Euro Surveill 2008;13.Doi:pii: 18989.
24. Sirbu A, Ceianu CS, Panculescu-Gatej RI, et al. Outbreak of West Nile virus infection in humans, Romania, July to Octo- ber 2010. Euro Surveill 2011;16. Doi:pii:19762.
25. Autorino GL, Battisti A, Deubel V, et al. West Nile virus epi- demic in horses, Tuscany region, Italy. Emerg Infect Dis 2002; 8:1372-1378.
26. Rezza G. Chikungunya and West Nile virus outbreaks: what is happening in north-eastern Italy? Eur J Publ Health 2009;19:236-237.
27. Rossini G, Cavrini F, Pierro A, et al. Fist human case of West Nile virus neuroinvasive infection in Italy, September 2008- case report. EuroSurv 2008;13:1-2.
28. Barzon L, Pacenti M, Cusinato R, et al. Human cases of West Nile Virus infection in north-eastern Italy, 15 June to 15 No- vember 2010. Euro Surveill. 2011 Aug 18;16.
29. Rizzo C, Vescio F, Declich S, et al. West Nile virus trans- mission with human cases in Italy, August–September 2009. Euro Surveill. 2009;14. Doi:pii: 19353.
30. Rizzo C, Salcuni P, Nicoletti L, et al. Epidemiological surveil- lance of West Nile neuro invasive diseases in Italy, 2008 to 2011. Eurosurv 2012;17. Doi:pii: 20171.
31. Papa A, Danis K, Baka A, et al. Ongoing outbreak of West Nile virus infections in humans in Greece, July-August 2010. Euro Surveill 2010;15. Doi:pii: 19644.
32. Danis K, Papa A, Papanikolaou E, et al. Ongoing outbreak of West Nile virus infection in humans, Greece, July to August 2011. Euro Surveill 2011;16:pii=19951.
33. ECDC. West nile fever maps, 29/09/2013. http://www.ecdc. europa.eu/en/Pages/home.aspx.
34. Erdem H, Ergunay K, Yilmaz A, et al. Emergence and co- infections of West Nile virus and Toscana virus in Eastern Thrace, Turkey. Clin Microbiol Infect 2013; Jun 25.doi: 10.1111/1469-0691.12310 [Epub ahead of print].
35. Ergunay K, Sayiner AA, Litzba N, et al. Multicentre evalu- ation of central nervous system infections due to Flavi and Phleboviruses in Turkey. J Infect 2012 Oct;65:343-349. Doi: 10.1016/j.jinf.2012.05.010. Epub 2012 Jun 13.
36. Ozkul A, Ergunay K, Koysuren A, et al. Concurrent occur- rence of human and equine West Nile virus infections in Central Anatolia, Turkey: the first evidence for circulation of lineage 1 viruses. Int J Infect Dis 2013; Jul; 17: e546-51. Doi: 10.1016/j.ijid.2013.02.005. Epub 2013 Mar 19.
37. Karakoc ZC, Tuzuner BM, Ergonul O, et al. West Nile virus infection in the Mesopotamia Region, Syria border of Tur- key. Vector Borne Zoonotic Dis 2013 Jun 29 [Epub ahead of print].
38. Kalaycioglu H, Korukluoglu G, Ozkul A, et al. Emergence of West Nile virus infections in human in Turkey, 2010 to 2011. Euro Surveill 2012 May 24;17. Doi:pii: 20182
39. Ergunay K, Saygan MB, Aydogan S, et al. West Nile virus seroprevalence in blood donors from Central Anatolia, Tur- key. Vector Borne Zoonotic Dis 2010 Oct;10:771-775. Doi: 10.1089/vbz.2009.0130. Epub 2009 Dec 20.
40. Ayturan S, Aydogan S, Ergunay K, et al. Investigation of West Nile virus seroprevalence in Hacettepe University Hospital blood donors and confirmation of the positive re- sults by plaque reduction neutralization test. Mikrobiyol Bul 2011;45:113-124.
41. Sahiner F, Avci IY, Bedir O, et al. Investigation of West Nile virus RNA in blood donors by real-time RT-PCR. Mikrobiyol Bul 2012;46:464-469.
42. Ozkul A, Yildirim Y, Pinar D, et al. Serological evidence of West Nile virus (WNV) in mammalian species in Turkey. Epi- demiol Infect 2006;134:826-829.
43. Weinberger M, Pitlik SD, Gandacu D, et al. West Nile fever outbreak, Israel, 2000 : epidemiologic aspects. Emerg Infect Dis 2001;7:686-691.
44. Kopel E, Amitai Z, Bin H, et al. Surveillance of West Nile virus disease, Tel Aviv district, Israel, 2005 to 2010. Euro Surveill 2011;16:pii=19894.
45. EpiSouth. West Nile virus circulation in the EpiSouth coun- tries and in neighbouring areas. Update 1st July 2012. http:// www.episouthnetwork.org/sites/default/files/outputs/ note_ west_nile_episouth_2010_2011_july2012.pdf
46. Savage HM, Caianu C, Nicolescu G, et al. Entomologic and avian investigations of an epidemic of West Nile fever in Ro- mania in 1996, with serologic and molecular characteriza- tion of a virus isolate from mosquitoes. Am J Trop Med Hyg 1999;61:600-611.
47. Bakonyi T, Ivanics E, Erdelyi K, et al. Lineage 1 and 2 strains of encehalitic West Nile virus, Central Europe. Emerg Infect Dis 2006;12:618-623.
48. Savini G, Monaco F, Calistri P, Lelli R. Phylogenetic analy- sis of West Nile virus isolated in Italy in 2008. Euro Srveill 2008;13. Doi:ppi: 19048.
49. Barzon L, Franchin E, Squarzon L, et al. Genome sequence analysis of the first human West Nile virus isolated in Italy in 2009. Euro Surveill 2009;14. doi:pii: 19384
50. Rossini G, Carletti F, Bordi L, et al. Phylogenetic analysis of West Nile virus isolates, Italy, 2008-2009. Emerg Infect Dis 2011;17:903-906.
51. Barzon L, Pacenti M, Franchin E, et al. Clinical and virologi- cal findings in the ongoing outbreak of West Nile virus Liv- enza strain in northern Italy, July to September 2012. Euro Surveill 2012;17:20260.
52. Zehender G, Ebranati E, Bernini F, et al. Phylogeography and epidemiological history of West Nile virus genotype 1° in Europe and the Mediterranean basin. Infect Genet Evol 2011;11:646-653.
53. Platonov AE, Fedorova MV, Shopenskaia TA, et al. Genotyp- ing of West Nile virus strains circulating in southern Russia as an epidemiological investigation method: principles and results. Zh Microbiol Epidemiol Immunobiol 2011;2:29-37 (in Russian).
54. A. Papa, T. Bakonyi, K. Xanthopoulou, ET AL. Genetic char- acterization of West Nile virus lineage 2 Greece, 2010. Emerg Infect Dis 17:2011, pp. 920–922
55. Chaskopoulou A, Dovas CI, Chaintoutis SC, ET AL. Evi- dence of enzootic circulation of West Nile virus (Nea Santa- Greece-2010, lineage 2), Greece, May to July 2011. Euro Surveill 2011;16 pii=19933.
56. Valiakos G, Touloudi A, Iacovakis C, et al. Molecular detec- tion and phylogenetic analysis of West Nile virus lineage 2 in sedentary wild birds (Eurasian magpie), Greece, 2010. Euro Surveill 2011; 16(18) pii=19862.
57. Bagnarelli P, Marinelli K, Trotta D, et al. Human case of au- tochthonous West Nile virus lineage 2 infection in Italy, Sep- tember 2011. Euro Surveill. 2011:16.
58. Magurano F, Remoli ME, Baggieri M, et al. Circulation of West Nile virus 1 and 2 during an outbreak in Italy. Clin Mi- crobiol Infect 2012;18: E545-E547.
59. .Barzon L, Pacenti M, Franchin E, et al. Whole genome se- quencing and phylogenetic analysis of West Nile virus lin- eage 1 and lineage 2 from human cases of infection, Italy, August 2013. Euro Surveill 2013.