Isolation, genetic characterization, and seroprevalence of Adana virus, a novel phlebovirus belonging to the Salehabad virus complex, in Turkey

Journal of Virology

Volumn 89, Issue 8, 2015, Pages 4080-4091

  Alkan, Cigdem ^a,b   Alwassouf, Sulaf ^a   Piorkowski, Géraldine ^a,b   Bichaud, Laurence ^a,b,c   Tezcan, Seda ^d   Dincer, Ender ^d   Ergunay, Koray ^e   Ozbel, Yusuf ^f   Alten, Bulent ^e   de Lamballerie, Xavier ^a,b   Charrel, Rémi N ^a,b  

^a Aix Marseille University IRD 190 Inserm 1207   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

^c CHARLES UNIVERSITY   (Czech Republic)

^d MERSIN UNIVERSITY   (Turkey)

^e HACETTEPE UNIVERSITY   (Turkey)

^f EGE UNIVERSITY SCHOOL OF MEDICINE   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY;

ADANA VIRUS; ARTICLE; CONTROLLED STUDY; DOG; ELECTRON MICROSCOPY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC DISTANCE; GENOTYPE; GOAT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHLEBOVIRUS; PHYLOGENY; PRIORITY JOURNAL; PSYCHODIDAE; SALEHABAD VIRUS; SEROPREVALENCE; SHEEP; TURKEY (REPUBLIC); VIRUS DETECTION; VIRUS GENOME; VIRUS ISOLATION; ANIMAL; BUNYAVIRIDAE INFECTIONS; CLASSIFICATION; CLUSTER ANALYSIS; DISEASE CARRIER; DNA SEQUENCE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; PHLEBOTOMUS; SERODIAGNOSIS; TURKEY; ULTRASTRUCTURE; VETERINARY; VIROLOGY;

ANIMALIA; BUNYAVIRIDAE; CANIS FAMILIARIS; CAPRA HIRCUS; DIPTERA; OVIS ARIES; PHLEBOVIRUS; PSYCHODIDAE;

ANIMALS; BASE SEQUENCE; BUNYAVIRIDAE INFECTIONS; CLUSTER ANALYSIS; DOGS; GOATS; HUMANS; INSECT VECTORS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PHLEBOTOMUS; PHLEBOVIRUS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEROEPIDEMIOLOGIC STUDIES; SHEEP; TURKEY;

EID: 84925428012     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03027-14     Document Type: Article

References (54)

1. Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Lundkvist A, Schmaljohn CS, Tesh RB. 2012. Bunyaviridae, p. 693-709. In King AMQ, AdamsMJ, Carstens EB, Lefkowitz EJ (ed),Virus taxonomy: classification and nomenclature of viruses. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, CA.
2. Collao X, Palacios G, de Ory F, Sanbonmatsu S, Pérez-Ruiz M, Navarro JM, Molina R, Hutchison SK, Lipkin WI, Tenorio A, Sánchez-Seco MP. 2010. Granada virus: a natural phlebovirus reassortant of the sandfly fever Naples serocomplex with low seroprevalence in humans. Am J Trop Med Hyg 83:760-765. http://dx.doi.org/10.4269/ajtmh.2010.09-0697.
3. Remoli ME, Fortuna C, Marchi A, Bucci P, Argentini C, Bongiorno G, Maroli M, Gradoni L, Gramiccia M, Ciufolini MG. 2014. Viral isolates of a novel putative phlebovirus in the Marche Region of Italy. Am J Trop Med Hyg 90:760-763. http://dx.doi.org/10.4269/ajtmh.13-0457.
4. Zhioua E, Moureau G, Chelbi I, Ninove L, Bichaud L, Derbali M, Champs M, Cherni S, Salez N, Cook S, de Lamballerie X, Charrel RN. 2010. Punique virus, a novel phlebovirus, related to sandfly fever Naples virus, isolated from sandflies collected in Tunisia. J Gen Virol 91:1275-1283. http://dx.doi.org/10.1099/vir.0.019240-0.
5. McMullan LK, Folk SM, Kelly AJ, MacNeil A, Goldsmith CS, Metcalfe MG, Batten BC, Albariño CG, Zaki SR, Rollin PE, Nicholson WL, Nichol ST. 2012. A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med 367:834-841. http://dx.doi.org/10.1056/NEJMoa1203378.
6. Wang J, Selleck P, Yu M, Ha W, Rootes C, Gales R, Wise T, Crameri S, Chen H, Broz I, Hyatt A, Woods R, Meehan B, McCullough S, Wang LF. 2014. Novel phlebovirus with zoonotic potential isolated from ticks, Australia. Emerg Infect Dis 20:1040-1043. http://dx.doi.org/10.3201/eid2006.140003.
7. Mourya DT, Yadav PD, Basu A, Shete A, Patil DY, Zawar D, Majumdar TD, Kokate P, Sarkale P, Raut CG, Jadhav SM. 2014. Malsoor virus, a novel bat phlebovirus, is closely related to severe fever with thrombocytopenia syndrome virus and heartland virus. J Virol 88:3605-3609. http://dx.doi.org/10.1128/JVI.02617-13.
8. Zhao G, Krishnamurthy S, Cai Z, Popov VL, Travassos da Rosa AP, Guzman H, Cao S, Virgin HW, Tesh RB, Wang D. 2013. Identification of novel viruses using VirusHunter-an automated data analysis pipeline. PLoS One 8:e78470. http://dx.doi.org/10.1371/journal.pone.0078470.
9. Liu DY, Tesh RB, Travassos da Rosa AP, Peters CJ, Yang Z, Guzman H, Xiao SY. 2003. Phylogenetic relationships among members of the genus Phlebovirus (Bunyaviridae) based on partial M segment sequence analyses. J Gen Virol 84:465-473. http://dx.doi.org/10.1099/vir.0.18765-0.
10. Suzich JA, Kakach LT, Collett MS. 1990. Expression strategy of a phlebovirus: biogenesis of proteins from the Rift Valley fever virusMsegment. J Virol 64:1549-1555.
11. Xu F, Chen H, Travassos da Rosa AP, Tesh RB, Xiao SY. 2007. Phylogenetic relationships among sandfly fever group viruses (Phlebovirus: Bunyaviridae) based on the small genome segment. J Gen Virol 88: 2312-2319. http://dx.doi.org/10.1099/vir.0.82860-0.
12. Ciufolini MG, Maroli M, Guandalini E, Marchi A, Verani P. 1989. Experimental studies on the maintenance of Toscana and Arbia viruses (Bunyaviridae: Phlebovirus). Am J Trop Med Hyg 40:669-675.
13. Ciufolini MG, Maroli M, Verani P. 1985. Growth of two phleboviruses after experimental infection of their suspected sand fly vector, Phlebotomus perniciosus (Diptera: Psychodidae). Am J Trop Med Hyg 34:174-179.
14. Ciufolini MG, Maroli M, Verani P. 1991. Laboratory reared sandflies (Diptera:Psychodidae) and studies on phleboviruses. Parassitologia 33: 137-142.
15. Maroli M, Ciufolini MG, Verani P. 1993. Vertical transmission of Toscana virus in the sandfly, Phlebotomus perniciosus, via the second gonotrophic cycle. Med Vet Entomol 7:283-286. http://dx.doi.org/10.1111/j.1365-2915.1993.tb00689.x.
16. Tesh RB, Modi GB. 1987. Maintenance of Toscana virus in Phlebotomus perniciosus by vertical transmission. Am J Trop Med Hyg 36:189-193.
17. Tesh RB, Lubroth J, Guzman H. 1992. Simulation of arbovirus overwintering: survival of Toscana virus (Bunyaviridae:Phlebovirus) in its natural sand fly vector Phlebotomus perniciosus. Am J Trop Med Hyg 47:574-558.
18. Serter D. 1980. Present status of arbovirus sero-epidemiology in the Aegean region of Turkey, p. 155-161. In Vesenjak-Hirjan J, Porterfield JS, Arslanagic E (ed), Arboviruses in the Mediterranean countries. Gustav Fisher Verlag, Stuttgart, Germany.
19. Tesh RB, Saidi S, Gajdamovic SJ, Rodhain F, Vesenjak-Hirjan J. 1976. Serological studies on the epidemiology of sandfly fever in the Old World. Bull World Health Organ 54:663-674.
20. Carhan A, Uyar Y, Ozkaya E, Ertek M, Dobler G, Dilcher M, Wang Y, Spiegel M, Hufert F, Weidmann M. 2010. Characterization of a sandfly fever Sicilian virus isolated during a sandfly fever epidemic in Turkey. J Clin Virol 48:264-269. http://dx.doi.org/10.1016/j.jcv.2010.05.011.
21. Torun Edis C, Yagci Caglayik D, Uyar Y, Korukluoglu G, Ertek M. 2010. Sandfly fever outbreak in a province at Central Anatolia, Turkey. Mikrobiyol Bul. 44:431-439.
22. 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:e244-e246. http://dx.doi.org/10.1016/j.ijid.2011.12.001.
23. Ayaslioglu E, Guliter S, Karabicak C, Ecemis K, Gulhan M, Edis CT. 2014. Sandfly fever virus as a rare cause of acute viral hepatitis. Travel Med Infect Dis 12:296-297. http://dx.doi.org/10.1016/j.tmaid.2014.02.001.
24. Ergunay K, Aydogan S, Ilhami Ozcebe O, Cilek EE, Hacioglu S, Karakaya J, Ozkul A, Us D. 2012. Toscana virus (TOSV) exposure is confirmed in blood donors from central, north and south/southeast Anatolia, Turkey. Zoonoses Public Health 59:148-154. http://dx.doi.org/10.1111/j.1863-2378.2011.01436.x.
25. Ergunay K, Sayiner AA, Litzba N, Lederer S, Charrel RN, Kreher P, Us D, Niedrig M, Ozkul A, Hascelik G. 2012. Multicentre evaluation of central nervous system infections due to flavi and phleboviruses in Turkey. J Infect 65:343-349. http://dx.doi.org/10.1016/j.jinf.2012.05.010.
26. 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 11:781-787. http://dx.doi.org/10.1089/vbz.2010.0224.
27. Ergunay K, Saygan MB, Aydogan S, Lo MM, Weidmann M, Dilcher M, Sener B, Hasçelik G, Pinar A, Us D. 2011. Sandfly fever virus activity in central/northern Anatolia, Turkey: first report of Toscana virus infections. Clin Microbiol Infect 17:575-581. http://dx.doi.org/10.1111/j.1469-0691.2010.03346.x.
28. Ocal M, Orsten S, Inkaya AC, Yetim E, Acar NP, Alp S, Kasap OE, Gunay F, Arsava EM, Alten B, Ozkul A, Us D, Niedrig M, Ergunay K. 2014. Ongoing activity of Toscana virus genotype A and West Nile virus lineage 1 strains in Turkey: a clinical and field survey. Zoonoses Public Health 61:480-491. http://dx.doi.org/10.1111/zph.12096.
29. Ergunay K, Erisoz Kasap O, Kocak Tufan Z, Turan MH, Ozkul A, Alten B. 2012. Molecular evidence indicates that Phlebotomus major sensu lato (Diptera: Psychodidae) is the vector species of the recently-identified sandfly fever Sicilian virus variant: sandfly fever turkey virus. Vector Borne Zoonotic Dis 12:690-698. http://dx.doi.org/10.1089/vbz.2011.0927.
30. Charrel RN, Moureau G, Temmam S, Izri A, Marty P, Parola P, da Rosa AT, Tesh RB, de Lamballerie X. 2009. Massilia virus, a novel Phlebovirus (Bunyaviridae) isolated from sandflies in the Mediterranean. Vector Borne Zoonotic Dis 9:519-530. http://dx.doi.org/10.1089/vbz.2008.0131.
31. Charrel RN, Izri A, Temmam S, Delaunay P, Toga I, Dumon H, Marty P, de Lamballerie X, Parola P. 2007. Cocirculation of 2 genotypes of Toscana virus, southeastern France. Emerg Infect Dis 13:465-468. http://dx.doi.org/10.3201/eid1303.061086.
32. Sánchez-Seco MP, Echevarria JM, Hermndez L, Estévez D, Navarro-Mari JM, Tenorio A. 2003. Detection and identification of Toscana and other phleboviruses by RT-nested-PCR assays with degenerated primers. J Med Virol 71:140-149. http://dx.doi.org/10.1002/jmv.10465.
33. Palacios G, Savji N, Travassos da Rosa A, Desai A, Sanchez-Seco MP, Guzman H, Lipkin WI, Tesh R. 2013. Characterization of the Salehabad virus species complex of the genus Phlebovirus (Bunyaviridae). J Gen Virol 94:837-842. http://dx.doi.org/10.1099/vir.0.048850-0.
34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
35. Charrel RN, Zaki AM, Attoui H, Fakeeh M, Billoir F, Yousef AI, de Chesse R, De Micco P, Gould EA, de Lamballerie X. 2001. Complete coding sequence of the Alkhurma virus, a tick-borne flavivirus causing severe hemorrhagic fever in humans in Saudi Arabia. Biochem Biophys Res Commun 287:455-461. http://dx.doi.org/10.1006/bbrc.2001.5610.
36. Sakhria S, Bichaud L, Mensi M, Salez N, Dachraoui K, Thirion L, Cherni S, Chelbi I, de Lamballerie X, Zhioua E, Charrel RN. 2013. Co-circulation of Toscana virus and Punique virus in northern Tunisia: a microneutralisation-based seroprevalence study. PLoS Negl Trop Dis 7:e2429. http://dx.doi.org/10.1371/journal.pntd.0002429.
37. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294-299.
38. Collao X, Palacios G, Sanbonmatsu-Gamez S, Perez-Ruiz M, Negredo AI, Navarro-Mari JM, Grandadam M, Aransay AM, Lipkin WI, Tenorio A, Sanchez-Seco MP. 2009. Genetic diversity of Toscana virus. Emerg Infect Dis 15:574-577. http://dx.doi.org/10.3201/eid1504.081111.
39. Palacios G, Tesh RB, Savji N, Travassos da Rosa AP, Guzman H, Bussetti AV, Desai A, Ladner J, Sanchez-Seco M, Lipkin WI. 2014. Characterization of the sandfly fever Naples species complex and description of a new Karimabad species complex (genus Phlebovirus, family Bunyaviridae). J Gen Virol 95:292-300. http://dx.doi.org/10.1099/vir.0.056614-0.
40. Karabatsos N. 1985. International catalogue of arboviruses including certain other viruses of vertebrates. American Society Tropical Medicine and Hygiene, San Antonio, TX.
41. Verani P, Ciufolini MG, Caciolli S, Renzi A, Nicoletti L, Sabatinelli G, Bartolozzi D, Volpi G, Amaducci L, Coluzzi M, et al. 1988. Ecology of viruses isolated from sand flies in Italy and characterized of a new Phlebovirus (Arabia virus). Am J Trop Med Hyg 38:433-439.
42. Papa A, Velo E, Bino S. 2011. A novel phlebovirus in Albanian sandflies. Clin Microbiol Infect 17:585-587. http://dx.doi.org/10.1111/j.1469-0691.2010.03371.x.
43. Anagnostou V, Pardalos G, Athanasiou-Metaxa M, Papa A. 2011. Novel phlebovirus in febrile child, Greece. Emerg Infect Dis 17:940-941. http://dx.doi.org/10.3201/eid1705.101958.
44. Ergunay K, Erisoz Kasap O, Orsten S, Oter K, Gunay F, Akkutay AZ, Dincer E, Alten B, Ozkul A. 2014. Phlebovirus and leishmania detection in sandflies from eastern Thrace and northern C yprus. Parasit Vectors 7:575. http://dx.doi.org/10.1186/s13071-014-0575-6.
45. Palacios G, Savji N, Travassos da Rosa A, Guzman H, Yu X, Desai A, Rosen GE, Hutchison S, Lipkin WI, Tesh R. 2013. Characterization of the Uukuniemi virus group (Phlebovirus: Bunyaviridae): evidence for seven distinct species. J Virol 87:3187-3195. http://dx.doi.org/10.1128/JVI.02719-12.
46. Pierro A, Gaibani P, Spadafora C, Ruggeri D, Randi V, Parenti S, Finarelli AC, Rossini G, Landini MP, Sambri V. 2013. Detection of specific antibodies against West Nile and Usutu viruses in healthy blood donors in northern Italy, 2010-2011. Clin Microbiol Infect 19:E451-E453. http://dx.doi.org/10.1111/1469-0691.12241.
47. Sakhria S, Alwassouf S, Fares W, Bichaud L, Dachraoui K, Alkan C, Zoghlami Z, de Lamballerie X, Zhioua E, Charrel RN. 2014. Presence of sandfly-borne phleboviruses of two antigenic complexes (sandfly fever Naples virus and sandfly fever Sicilian virus) in two different biogeographical regions of Tunisia demonstrated by a microneutralisationbased seroprevalence study in dogs. Parasit Vectors. 7:476. http://dx.doi.org/10.1186/s13071-014-0476-8.
48. Belen A, Alten B. 2011. Seasonal dynamics and altitudinal distributions of sand fly (Diptera: Psychodidae) populations in a cutaneous leishmaniasis endemic area of the Cukurova region of Turkey. J Vector Ecol. 36(Suppl. 1):S87-S94. http://dx.doi.org/10.1111/j.1948-7134.2011.00116.x.
49. Serin MS, Daglioglu K, Bagirova M, Allahverdiyev A, Uzun S, Vural Z, Kayar B, Tezcan S, Yetkin M, Aslan G, Emekdas G, Koksal F. 2005. Rapid diagnosis and genotyping of Leishmania isolates from cutaneous and visceral leishmaniasis by microcapillary cultivation and polymerase chain reaction-restriction fragment length polymorphism of miniexon region. Diagn Microbiol Infect Dis 53:209-214. http://dx.doi.org/10.1016/j.diagmicrobio.2005.05.007.
50. Svobodova M, Alten B, Zidkova L, Dvorak V, Hlavackova J, Myskova J, Seblova V, Erisoz Kasap O, Belen A, Votypka J, Volf P. 2009. CL caused by Leishmania infantum and transmitted by Phlebotomus tobbi. Int J Parasitol 39:251-256. http://dx.doi.org/10.1016/j.ijpara.2008.06.016.
51. Uzun S, Uslular C, Yücel A, Acar MA, Ozpoyraz M, Memişoğlu HR. 1999. Cutaneous leishmaniasis: evaluation of 3,074 cases in the Cukurova region of Turkey. Br J Dermatol 140:347-350. http://dx.doi.org/10.1046/j.1365-2133.1999.02673.x.
52. Bichaud L, Dachraoui K, Piorkowski G, Chelbi I, Moureau G, Cherni S, De Lamballerie X, Sakhria S, Charrel RN, Zhioua E. 2013. Toscana virus isolated from sandflies, Tunisia. Emerg Infect Dis 19:322-324. http://dx.doi.org/10.3201/eid1902.121463.
53. Sanbonmatsu-Gámez S, Pérez-Ruiz M, Collao X, Sánchez-Seco MP, Morillas-Márquez F, de la Rosa-Fraile M, Navarro-Mari JM, Tenorio A. 2005. Toscana virus in Spain. Emerg Infect Dis 11:1701-1707. http://dx.doi.org/10.3201/eid1111.050851.
54. Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L. 2013. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol 27:123-147. http://dx.doi.org/10.1111/j.1365-2915.2012.01034.x.