The Prevalence of Antibodies against Sandfly Fever Viruses and West Nile Virus in Cyprus
Abstract
Background: Sandfly fever is an incapacitating disease caused by sandfly-borne Phleboviruses that can lead to meningitis, encephalitis or meningoencephalitis. West Nile virus (WNV), a mosquito-borne Flavivirus, can induce neuroinvasive disease manifested by meningitis, encephalitis or acute flaccid paralysis. Both vectors are endemic in Cyprus and very active during summer. The aims of this study were to determine first the prevalence of sandfly fever viruses (SFV) and WNV infections in Cyprus and second, to investigate their role in central nervous system (CNS) infections.
Methods: For the prevalence study, 327 sera collected in 2013 and 2014 were tested for anti-SFV and anti-WNV IgG using indirect immunofluorescence assay and ELISA, respectively. In order to investigate a possible role of SFV and WNV in CNS infections, 127 sera of patients presenting symptoms of SFV or WNV infections were screened for IgM specific to SFV and WNV.
Results: The overall anti-SFV IgG seroprevalence was 28% and was increasing with age (P< 0.01). The seroprevalence rate for anti-WNV IgG in Cyprus was 5%. Concerning the role of SFVs in CNS infections, anti-SFV IgM was detected in 8 out of 127 sera from selected patients presenting relevant symptoms of infections during vector’s active period. In addition, anti-WNV IgM were detected in 17 out of the 127 patients with compatible symptoms.
Conclusion: The findings confirm the presence of sandfly fever and WNV in Cyprus and should, therefore, be considered in the differential diagnosis of patients with febrile illness/meningitis.
1. Adams MJ, Lefkowitz EJ, King AMQ, Harrach B, Harrison RL, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Mushegian AR, Nibert M, Sabanad-zovic S, Sanfaçon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Gorbalenya AE, Davison AJ (2017) Changes to taxonomy and the International Code of Virus Classification and Nomenclature rati-fied by the International Committee on Taxonomy of Viruses (2017). Arch Virol. 162 (8): 2505–2538.
2. Guler S, Guler E, Caglayik DY, Kokoglu OF, Ucmak H, Bayrakdar F, Uyar Y (2012) A sandfly fever virus outbreak in the East Mediterranean region of Turkey. Int J Infect Dis. 16(4): e244–246.
3. Schultze D, Korte W, Rafeiner P, Niedrig M (2012) First report of sandfly fever virus infection imported from Malta into Switzerland, October 2011. Euro Surveill. 17(27).
4. Charrel RN, Bichaud L, de Lamballerie X (2012) Emergence of Toscana virus in the mediterranean area. World J Virol. 1 (5): 135–141.
5. Ayhan N, Charrel RN (2017) Of phlebotomines (sandflies) and viruses: a comprehensive perspective on a complex situation. Curr Opin Insect Sci. 22: 117–124.
6. Kocak Tufan Z, Weidmann M, Bulut C, Kinikli S, Hufert FT, Dobler G, Demiroz AP (2011) Clinical and laboratory findings of a sandfly fever Turkey Virus outbreak in Ankara. J Infect. 63(5): 375–381.
7. Alkan C, Moin Vaziri V, Ayhan N, Ba-dakhshan M, Bichaud L, Rahbarian N, Javadian EA, Alten B, de Lamballerie X, Charrel RN (2017) Isolation and sequencing of Dashli virus, a novel Sicilian-like virus in sandflies from Iran; genetic and phylogenetic evidence for the creation of one novel species within the Phlebovirus genus in the Phenuiviridae family. PLoS Negl Trop Dis. 11(12): e0005978.
8. Ergunay K, Ayhan N, Charrel RN (2017) Novel and emergent sandfly-borne phlebo¬viruses in Asia Minor: a systematic review. Rev Med Virol. 27(2).
9. Calzolari M, Ferrarini G, Bonilauri P, Lelli D, Chiapponi C, Bellini R, Dottori M (2018) Co-circulation of eight different phleboviruses in sand flies collected in the Northern Apennine Mountains (Italy). Infect Genet Evol. 64: 131–134.
10. Marchi S, Trombetta CM, Kistner O, Montomoli E (2017) Seroprevalence study of Toscana virus and viruses belonging to the Sandfly fever Naples antigenic complex in central and southern Italy. J Infect Public Health. 10(6): 866–869.
11. Dokianakis E, Tsirigotakis N, Chris-todoulou V, Poulakakis N, Antoniou M (2018) Identification of wild-caught phlebotomine sand flies from Crete and Cyprus using DNA barcoding. Parasit Vectors. 11(1): 94.
12. Leger N, Depaquit J, Ferte H (2000) Phlebotom¬ine sandflies (Diptera-Psychodidae) of the isle of Cyprus. I-Description of Phlebotomus (Transphlebotomus) economidesi n. sp. Parasite. 7(2): 135–141.
13. Niklasson B, Eitrem R (1985) Sandfly fever among Swedish UN troops in Cy¬prus. Lancet. 1(8439): 1212.
14. Eitrem R, Vene S, Niklasson B (1990) Incidence of sand fly fever among Swe¬dish United Nations soldiers on Cyprus during 1985. Am J Trop Med Hyg. 43 (2): 207–211.
15. Papa A, Konstantinou G, Pavlidou V, Antoniadis A (2006) Sandfly fever virus outbreak in Cyprus. Clin Microbiol Infect. 12(2): 192–194.
16. Konstantinou GN, Papa A, Antoniadis A (2007) Sandfly-fever outbreak in Cyprus: are phleboviruses still a health problem? Travel Med Infect Dis. 5(4): 239–242.
17. Petersen LR, Brault AC, Nasci RS (2013) West Nile virus: review of the literature. JAMA. 310(3): 308–315.
18. Hayes EB, Sejvar JJ, Zaki SR, Lanciotti RS, Bode AV, Campbell GL (2005) Vi¬rology, pathology, and clinical manifestations of West Nile virus disease. Emerg Infect Dis. 11(8): 1174–1179.
19. Violaris M, Vasquez MI, Samanidou A, Wirth MC, Hadjivassilis A (2009) The mosquito fauna of the Republic of Cyprus: a revised list. J Am Mosq Control Assoc. 25(2): 199–202.
20. Ergunay K, Gunay F, Erisoz Kasap O, Oter K, Gargari S, Karaoglu T, Tezcan S, Cabalar M, Yildirim Y, Emekdas G, Alten B, Ozkul A (2014) Serological, mo¬lecular and entomological surveil-lance demonstrates widespread circulation of West Nile virus in Turkey. PLoS Negl Trop Dis. 8(7): e3028.
21. Kilpatrick AM (2011) Globalization, land use, and the invasion of West Nile virus. Science. 334(6054): 323–327.
22. Papa A (2017) Emerging arboviral human diseases in Southern Europe. J Med Virol. 89(8): 1315–1322.
23. Burki T (2018) Increase of West Nile virus cases in Europe for 2018. Lancet. 392 (10152): 1000.
24. Paphitou NI, Tourvas A, Floridou D, Richter J, Tryfonos C, Christodoulou C (2017) The first human case of neuroinvasive West Nile virus infection identified in Cyprus. J Infect Public Health. 10(6): 891–893.
25. Richter J, Tryfonos C, Tourvas A, Flori-dou D, Paphitou NI, Christodoulou C (2017) Complete Genome Sequence of West Nile Virus (WNV) from the First Human Case of Neuroinvasive WNV Infection in Cyprus. Genome Announc. 5 (43).
26. Perez-Ruiz M, Collao X, Navarro-Mari JM, Tenorio A (2007) Reverse transcription, real-time PCR assay for detection of Toscana virus. J Clin Virol. 39(4): 276–281.
27. Cordey S, Bel M, Petty TJ, Docquier M, Sacco L, Turin L, Cherpillod P, Emonet S, Louis-Simonet M, Zdobnov EM, Ambrosioni J, Kaiser L (2015) Toscana virus meningitis case in Switzerland: an ex¬ample of the ezVIR bioinformatics pipeline utility for the identification of emerging viruses. Clin Microbiol Infect. 21 (4): 387. e1–4.
28. Patel P, Landt O, Kaiser M, Faye O, Koppe T, Lass U, Sall AA, Niedrig M (2013) Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol J. 10: 58.
29. Ergunay K, Kasap OE, Orsten S, Oter K, Gunay F, Yoldar AZ, Dincer E, Alten B, Ozkul A (2014) Phlebovirus and Leishmania detection in sandflies from east¬ern Thrace and northern Cyprus. Parasit Vectors. 7: 575.
30. Sellers RF, Herniman KA (1981) Neutralising antibodies to Akabane virus in ruminants in Cyprus. Trop Anim Health Prod. 13(1): 57–60.
31. Polydorou K (1978) The 1977 outbreak of bluetongue in Cyprus. Trop Anim Health Prod. 10(4): 229–232.
32. Stahn B, Sudeck H, Frickmann H, Kruger A, Burchard HG, Wiemer D (2018) [Sandfly fever-a "neglected" disease]. Hautarzt. 69(11): 928–937.
33. Eitrem R, Vene S, Niklasson B (1991) ELISA for detection of IgM and IgG antibodies to sandfly fever Sicilian virus. Res Virol. 142(5): 387–394.
34. Eitrem R, Stylianou M, Niklasson B (1991) High prevalence rates of antibody to three sandfly fever viruses (Sicilian, Naples, and Toscana) among Cypriots. Epidemiol Infect. 107(3): 685–691.
35. Alwassouf S, Christodoulou V, Bichaud L, Ntais P, Mazeris A, Antoniou M, Charrel RN (2016) Seroprevalence of Sandfly-Borne Phleboviruses Belonging to Three Serocomplexes (Sandfly fever Naples, Sandfly fever Sicilian and Salehabad) in Dogs from Greece and Cyprus Using Neutralization Test. PLoS Negl Trop Dis. 10(10): e0005063.
36. Ergunay K, Litzba N, Lo MM, Aydogan S, Saygan MB, Us D, Weidmann M, Niedrig M (2011) Performance of various commercial assays for the detection of Toscana virus antibodies. Vector Borne Zoonotic Dis. 11(6): 781–787.
37. Vasquez MI, Violaris M, Hadjivassilis A, Wirth MC (2009) Susceptibility of Culex pipiens (Diptera: Culicidae) field populations in Cyprus to conventional organic insecticides, Bacillus thuringiensis subsp. israelensis, and methoprene. J Med Entomol. 46(4): 881–887.
38. Ergunay K, Saygan MB, Aydogan S, Lo MM, Weidmann M, Dilcher M, Sener B, Hascelik G, Pinar A, Us D (2011) Sandfly fever virus activity in central/northern Anatolia, Turkey: first report of Toscana virus infections. Clin Microbiol Infect. 17(4): 575–581.
39. Tezcan S, Dincer E, Ulger M, Ozgur D, Erdogan S, Ozkul A, Emekdas G, Ergunay K (2015) Serological investigation of phlebovirus exposure in blood donors from the Mediterranean Province of Mersin, Turkey. Mikrobiyol Bul. 49(3): 403–413.
40. de Ory-Manchon F, Sanz-Moreno JC, Aranguez-Ruiz E, Ramirez-Fernandez R (2007) Age-dependent seroprevalence of Toscana virus in the Community of Madrid: 1993–1994 and 1999–2000. Enferm Infecc Microbiol Clin. 25(3): 187–189.
41. Anagnostou V, Papa A (2013) Prevalence of antibodies to phleboviruses within the sand fly fever Naples virus species in humans, northern Greece. Clin Microbiol Infect. 19(6): 566–570.
42. Hadjichristodoulou C, Pournaras S, Mavrouli M, Marka A, Tserkezou P, Baka A, Billinis C, Katsioulis A, Psaroulaki A, Papa A, Papadopoulos N, Mamuris Z, Tsakris A, Kremastinou J, Project M (2015) West Nile Virus Seroprevalence in the Greek Population in 2013: A Nationwide Cross-Sectional Survey. PLoS One. 10(11): e0143803.
43. Barzon L, Pacenti M, Franchin E, Squarzon L, Lavezzo E, Cattai M, Cusinato R, Palu G (2013) The complex epidemiological scenario of West Nile virus in Italy. Int J Environ Res Public Health. 10(10): 4669–4689.
44. Bahri O, Dhifallah I, Ben Alaya-Bouafif N, Fekih H, Gargouri J, Triki H (2011) Seroepidemiological study of West Nile virus circulation in human in Tunisia. Bull Soc Pathol Exot. 104(4): 272–276.
45. Ergünay K, Tufan ZK (2014) Overview of West Nile virus and sandfly-borne Phlebovirus infections in Anatolia. J Microbiol Infect Dis. Special Issue 1: S22–S31.
46. Failloux AB, Bouattour A, Faraj C, Gunay F, Haddad N, Harrat Z, Jancheska E, Kanani K, Kenawy MA, Kota M, Pajovic I, Paronyan L, Petric D, Sarih M, Sawalha S, Shaibi T, Sherifi K, Sulesco T, Velo E, Gaayeb L, Victoir K, Robert V (2017) Surveillance of arthropod-borne viruses and their vectors in the Mediterranean and Black Sea Regions within the MediLabSecure Network. Curr Trop Med Rep. 4(1): 27–39.
47. Alkan C, Bichaud L, de Lamballerie X, Alten B, Gould EA, Charrel RN (2013) Sandfly-borne phleboviruses of Eurasia and Africa: epidemiology, genetic di-versity, geographic range, control measures. Antiviral Res. 100(1): 54–74.
48. Chochlakis D, Ioannou I, Sandalakis V, Dimitriou T, Kassinis N, Papadopoulos B, Tselentis Y, Psaroulaki A (2012) Spotted fever group Rickettsiae in ticks in Cyprus. Microb Ecol. 63(2): 314–323.
49. ECDC (2017) West Nile fever maps_ Historical data. European Centre for Disease Prevention and Control. Available at: http://ecdc.europa.eu/en/healthtopics/west_nile_fever/West-Nile-fever-maps/Pages/historical-data.aspx.
2. Guler S, Guler E, Caglayik DY, Kokoglu OF, Ucmak H, Bayrakdar F, Uyar Y (2012) A sandfly fever virus outbreak in the East Mediterranean region of Turkey. Int J Infect Dis. 16(4): e244–246.
3. Schultze D, Korte W, Rafeiner P, Niedrig M (2012) First report of sandfly fever virus infection imported from Malta into Switzerland, October 2011. Euro Surveill. 17(27).
4. Charrel RN, Bichaud L, de Lamballerie X (2012) Emergence of Toscana virus in the mediterranean area. World J Virol. 1 (5): 135–141.
5. Ayhan N, Charrel RN (2017) Of phlebotomines (sandflies) and viruses: a comprehensive perspective on a complex situation. Curr Opin Insect Sci. 22: 117–124.
6. Kocak Tufan Z, Weidmann M, Bulut C, Kinikli S, Hufert FT, Dobler G, Demiroz AP (2011) Clinical and laboratory findings of a sandfly fever Turkey Virus outbreak in Ankara. J Infect. 63(5): 375–381.
7. Alkan C, Moin Vaziri V, Ayhan N, Ba-dakhshan M, Bichaud L, Rahbarian N, Javadian EA, Alten B, de Lamballerie X, Charrel RN (2017) Isolation and sequencing of Dashli virus, a novel Sicilian-like virus in sandflies from Iran; genetic and phylogenetic evidence for the creation of one novel species within the Phlebovirus genus in the Phenuiviridae family. PLoS Negl Trop Dis. 11(12): e0005978.
8. Ergunay K, Ayhan N, Charrel RN (2017) Novel and emergent sandfly-borne phlebo¬viruses in Asia Minor: a systematic review. Rev Med Virol. 27(2).
9. Calzolari M, Ferrarini G, Bonilauri P, Lelli D, Chiapponi C, Bellini R, Dottori M (2018) Co-circulation of eight different phleboviruses in sand flies collected in the Northern Apennine Mountains (Italy). Infect Genet Evol. 64: 131–134.
10. Marchi S, Trombetta CM, Kistner O, Montomoli E (2017) Seroprevalence study of Toscana virus and viruses belonging to the Sandfly fever Naples antigenic complex in central and southern Italy. J Infect Public Health. 10(6): 866–869.
11. Dokianakis E, Tsirigotakis N, Chris-todoulou V, Poulakakis N, Antoniou M (2018) Identification of wild-caught phlebotomine sand flies from Crete and Cyprus using DNA barcoding. Parasit Vectors. 11(1): 94.
12. Leger N, Depaquit J, Ferte H (2000) Phlebotom¬ine sandflies (Diptera-Psychodidae) of the isle of Cyprus. I-Description of Phlebotomus (Transphlebotomus) economidesi n. sp. Parasite. 7(2): 135–141.
13. Niklasson B, Eitrem R (1985) Sandfly fever among Swedish UN troops in Cy¬prus. Lancet. 1(8439): 1212.
14. Eitrem R, Vene S, Niklasson B (1990) Incidence of sand fly fever among Swe¬dish United Nations soldiers on Cyprus during 1985. Am J Trop Med Hyg. 43 (2): 207–211.
15. Papa A, Konstantinou G, Pavlidou V, Antoniadis A (2006) Sandfly fever virus outbreak in Cyprus. Clin Microbiol Infect. 12(2): 192–194.
16. Konstantinou GN, Papa A, Antoniadis A (2007) Sandfly-fever outbreak in Cyprus: are phleboviruses still a health problem? Travel Med Infect Dis. 5(4): 239–242.
17. Petersen LR, Brault AC, Nasci RS (2013) West Nile virus: review of the literature. JAMA. 310(3): 308–315.
18. Hayes EB, Sejvar JJ, Zaki SR, Lanciotti RS, Bode AV, Campbell GL (2005) Vi¬rology, pathology, and clinical manifestations of West Nile virus disease. Emerg Infect Dis. 11(8): 1174–1179.
19. Violaris M, Vasquez MI, Samanidou A, Wirth MC, Hadjivassilis A (2009) The mosquito fauna of the Republic of Cyprus: a revised list. J Am Mosq Control Assoc. 25(2): 199–202.
20. Ergunay K, Gunay F, Erisoz Kasap O, Oter K, Gargari S, Karaoglu T, Tezcan S, Cabalar M, Yildirim Y, Emekdas G, Alten B, Ozkul A (2014) Serological, mo¬lecular and entomological surveil-lance demonstrates widespread circulation of West Nile virus in Turkey. PLoS Negl Trop Dis. 8(7): e3028.
21. Kilpatrick AM (2011) Globalization, land use, and the invasion of West Nile virus. Science. 334(6054): 323–327.
22. Papa A (2017) Emerging arboviral human diseases in Southern Europe. J Med Virol. 89(8): 1315–1322.
23. Burki T (2018) Increase of West Nile virus cases in Europe for 2018. Lancet. 392 (10152): 1000.
24. Paphitou NI, Tourvas A, Floridou D, Richter J, Tryfonos C, Christodoulou C (2017) The first human case of neuroinvasive West Nile virus infection identified in Cyprus. J Infect Public Health. 10(6): 891–893.
25. Richter J, Tryfonos C, Tourvas A, Flori-dou D, Paphitou NI, Christodoulou C (2017) Complete Genome Sequence of West Nile Virus (WNV) from the First Human Case of Neuroinvasive WNV Infection in Cyprus. Genome Announc. 5 (43).
26. Perez-Ruiz M, Collao X, Navarro-Mari JM, Tenorio A (2007) Reverse transcription, real-time PCR assay for detection of Toscana virus. J Clin Virol. 39(4): 276–281.
27. Cordey S, Bel M, Petty TJ, Docquier M, Sacco L, Turin L, Cherpillod P, Emonet S, Louis-Simonet M, Zdobnov EM, Ambrosioni J, Kaiser L (2015) Toscana virus meningitis case in Switzerland: an ex¬ample of the ezVIR bioinformatics pipeline utility for the identification of emerging viruses. Clin Microbiol Infect. 21 (4): 387. e1–4.
28. Patel P, Landt O, Kaiser M, Faye O, Koppe T, Lass U, Sall AA, Niedrig M (2013) Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol J. 10: 58.
29. Ergunay K, Kasap OE, Orsten S, Oter K, Gunay F, Yoldar AZ, Dincer E, Alten B, Ozkul A (2014) Phlebovirus and Leishmania detection in sandflies from east¬ern Thrace and northern Cyprus. Parasit Vectors. 7: 575.
30. Sellers RF, Herniman KA (1981) Neutralising antibodies to Akabane virus in ruminants in Cyprus. Trop Anim Health Prod. 13(1): 57–60.
31. Polydorou K (1978) The 1977 outbreak of bluetongue in Cyprus. Trop Anim Health Prod. 10(4): 229–232.
32. Stahn B, Sudeck H, Frickmann H, Kruger A, Burchard HG, Wiemer D (2018) [Sandfly fever-a "neglected" disease]. Hautarzt. 69(11): 928–937.
33. Eitrem R, Vene S, Niklasson B (1991) ELISA for detection of IgM and IgG antibodies to sandfly fever Sicilian virus. Res Virol. 142(5): 387–394.
34. Eitrem R, Stylianou M, Niklasson B (1991) High prevalence rates of antibody to three sandfly fever viruses (Sicilian, Naples, and Toscana) among Cypriots. Epidemiol Infect. 107(3): 685–691.
35. Alwassouf S, Christodoulou V, Bichaud L, Ntais P, Mazeris A, Antoniou M, Charrel RN (2016) Seroprevalence of Sandfly-Borne Phleboviruses Belonging to Three Serocomplexes (Sandfly fever Naples, Sandfly fever Sicilian and Salehabad) in Dogs from Greece and Cyprus Using Neutralization Test. PLoS Negl Trop Dis. 10(10): e0005063.
36. Ergunay K, Litzba N, Lo MM, Aydogan S, Saygan MB, Us D, Weidmann M, Niedrig M (2011) Performance of various commercial assays for the detection of Toscana virus antibodies. Vector Borne Zoonotic Dis. 11(6): 781–787.
37. Vasquez MI, Violaris M, Hadjivassilis A, Wirth MC (2009) Susceptibility of Culex pipiens (Diptera: Culicidae) field populations in Cyprus to conventional organic insecticides, Bacillus thuringiensis subsp. israelensis, and methoprene. J Med Entomol. 46(4): 881–887.
38. Ergunay K, Saygan MB, Aydogan S, Lo MM, Weidmann M, Dilcher M, Sener B, Hascelik G, Pinar A, Us D (2011) Sandfly fever virus activity in central/northern Anatolia, Turkey: first report of Toscana virus infections. Clin Microbiol Infect. 17(4): 575–581.
39. Tezcan S, Dincer E, Ulger M, Ozgur D, Erdogan S, Ozkul A, Emekdas G, Ergunay K (2015) Serological investigation of phlebovirus exposure in blood donors from the Mediterranean Province of Mersin, Turkey. Mikrobiyol Bul. 49(3): 403–413.
40. de Ory-Manchon F, Sanz-Moreno JC, Aranguez-Ruiz E, Ramirez-Fernandez R (2007) Age-dependent seroprevalence of Toscana virus in the Community of Madrid: 1993–1994 and 1999–2000. Enferm Infecc Microbiol Clin. 25(3): 187–189.
41. Anagnostou V, Papa A (2013) Prevalence of antibodies to phleboviruses within the sand fly fever Naples virus species in humans, northern Greece. Clin Microbiol Infect. 19(6): 566–570.
42. Hadjichristodoulou C, Pournaras S, Mavrouli M, Marka A, Tserkezou P, Baka A, Billinis C, Katsioulis A, Psaroulaki A, Papa A, Papadopoulos N, Mamuris Z, Tsakris A, Kremastinou J, Project M (2015) West Nile Virus Seroprevalence in the Greek Population in 2013: A Nationwide Cross-Sectional Survey. PLoS One. 10(11): e0143803.
43. Barzon L, Pacenti M, Franchin E, Squarzon L, Lavezzo E, Cattai M, Cusinato R, Palu G (2013) The complex epidemiological scenario of West Nile virus in Italy. Int J Environ Res Public Health. 10(10): 4669–4689.
44. Bahri O, Dhifallah I, Ben Alaya-Bouafif N, Fekih H, Gargouri J, Triki H (2011) Seroepidemiological study of West Nile virus circulation in human in Tunisia. Bull Soc Pathol Exot. 104(4): 272–276.
45. Ergünay K, Tufan ZK (2014) Overview of West Nile virus and sandfly-borne Phlebovirus infections in Anatolia. J Microbiol Infect Dis. Special Issue 1: S22–S31.
46. Failloux AB, Bouattour A, Faraj C, Gunay F, Haddad N, Harrat Z, Jancheska E, Kanani K, Kenawy MA, Kota M, Pajovic I, Paronyan L, Petric D, Sarih M, Sawalha S, Shaibi T, Sherifi K, Sulesco T, Velo E, Gaayeb L, Victoir K, Robert V (2017) Surveillance of arthropod-borne viruses and their vectors in the Mediterranean and Black Sea Regions within the MediLabSecure Network. Curr Trop Med Rep. 4(1): 27–39.
47. Alkan C, Bichaud L, de Lamballerie X, Alten B, Gould EA, Charrel RN (2013) Sandfly-borne phleboviruses of Eurasia and Africa: epidemiology, genetic di-versity, geographic range, control measures. Antiviral Res. 100(1): 54–74.
48. Chochlakis D, Ioannou I, Sandalakis V, Dimitriou T, Kassinis N, Papadopoulos B, Tselentis Y, Psaroulaki A (2012) Spotted fever group Rickettsiae in ticks in Cyprus. Microb Ecol. 63(2): 314–323.
49. ECDC (2017) West Nile fever maps_ Historical data. European Centre for Disease Prevention and Control. Available at: http://ecdc.europa.eu/en/healthtopics/west_nile_fever/West-Nile-fever-maps/Pages/historical-data.aspx.
| Files | ||
| Issue | Vol 13 No 1 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i1.938 | |
| Keywords | ||
| Phleboviruses West-Nile virus Cyprus Seroprevalence | ||
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How to Cite
1.
Billioud G, Tryfonos C, Richter J. The Prevalence of Antibodies against Sandfly Fever Viruses and West Nile Virus in Cyprus. J Arthropod Borne Dis. 2018;13(1):116.
