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Journal of General Virology header logo Journal of General Virology

Volume 105, Issue 11

Toscana virus – an emerging Mediterranean arbovirus transmitted by sand flies Open Access

Abstract

Toscana virus (TOSV) is an emerging arthropod-borne virus (arbovirus) of medical importance that is increasing its range across much of the Mediterranean Basin, Europe and the Middle East. Transmitted by spp. sand flies, it is the most clinically relevant sand fly-borne phlebovirus. Initially isolated in the Tuscany region of Central Italy, it has now been detected in multiple countries that surround this geographical area. Infection of the vertebrate host can cause fever and neurological disease, following the dissemination of the virus to the brain. The prevalence is high in some regions, with a notable percentage of individuals showing seroconversion. TOSV can be a leading cause of acute meningitis and encephalitis (AME) during the summer months. In this comprehensive review, we will focus on several key topics. We discuss how TOSV has spread to establish outbreaks of infection in both humans and animals around the Mediterranean and the wider region. Clinical aspects of TOSV infection in humans are described, along with the best standards in diagnosis. Finally, we focus our discussion on the role of the sand fly vector, describing their biology, vector competency, implications for putative vertebrate reservoirs, the effect of the climate emergency on sand fly distribution and the putative role that sand fly-derived salivary factors may have on modulating host susceptibility to TOSV infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): arbovirus , diagnostics , epidemiology , pathogenesis and vector-borne disease
Funding
This study was supported by the:
  • Republic of Türkiye Ministry of National Education (Award MEB1416)
    • Principal Award Recipient: YoncaKeskek Turk
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2025-12-11

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References

  1. Kuhn JH, Abe J, Adkins S, Alkhovsky SV, Avšič-Županc T et al. Annual (2023) taxonomic update of RNA-directed RNA polymerase-encoding negative-sense RNA viruses (realm Riboviria: kingdom Orthornavirae: phylum Negarnaviricota). J Gen Virol 2023; 104:1–55
     [Google Scholar]
  2. King AMQ, Lefkowitz EJ, Mushegian AR, Adams MJ, Dutilh BE et al. Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2018). Arch Virol 2018; 163:2601–2631 [View Article] [PubMed]
     [Google Scholar]
  3. Verani P, Ciufolini MG, Nicoletti L, Balducci M, Sabatinelli G et al. Ecological and epidemiological studies of Toscana virus, an arbovirus isolated from Phlebotomus. Ann Ist Super Sanita 1982; 18:397–399 [PubMed]
     [Google Scholar]
  4. Ehrnst A, Peters CJ, Niklasson B, Svedmyr A, Holmgren B. Neurovirulent Toscana virus (a sandfly fever virus) in Swedish man after visit to Portugal. Lancet 1985; 1:1212–1213 [View Article] [PubMed]
     [Google Scholar]
  5. Nicoletti L, Verani P, Caciolli S, Ciufolini MG, Renzi A et al. Central nervous system involvement during infection by Phlebovirus toscana of residents in natural foci in central Italy (1977-1988). Am J Trop Med Hyg 1991; 45:429–434 [View Article] [PubMed]
     [Google Scholar]
  6. Ayhan N, Charrel RN. An update on Toscana virus distribution, genetics, medical and diagnostic aspects. Clin Microbiol Infect 2020; 26:1017–1023 [View Article] [PubMed]
     [Google Scholar]
  7. Elliott RM. The Bunyaviridae Springer Science & Business Media; 2013
     [Google Scholar]
  8. Koch J, Xin Q, Tischler ND, Lozach PY. Entry of Phenuiviruses into mammalian host cells. Viruses 2021; 13:11–14 [View Article] [PubMed]
     [Google Scholar]
  9. Lozach P-Y, Kühbacher A, Meier R, Mancini R, Bitto D et al. DC-SIGN as a receptor for phleboviruses. Cell Host Microbe 2011; 10:75–88 [View Article] [PubMed]
     [Google Scholar]
  10. Spiegel M, Plegge T, Pöhlmann S. The role of Phlebovirus glycoproteins in viral entry, assembly and release. Viruses 2016; 8:202 [View Article] [PubMed]
     [Google Scholar]
  11. Lozach P-Y, Mancini R, Bitto D, Meier R, Oestereich L et al. Entry of bunyaviruses into mammalian cells. Cell Host Microbe 2010; 7:488–499 [View Article] [PubMed]
     [Google Scholar]
  12. Hornak KE, Lanchy J-M, Lodmell JS. RNA encapsidation and packaging in the phleboviruses. Viruses 2016; 8:194 [View Article] [PubMed]
     [Google Scholar]
  13. Wuerth JD, Weber F. Phleboviruses and the type I interferon response. Viruses 2016; 8:174 [View Article] [PubMed]
     [Google Scholar]
  14. Koch J, Xin Q, Obr M, Schäfer A, Rolfs N et al. The phenuivirus Toscana virus makes an atypical use of vacuolar acidity to enter host cells. PLoS Pathog 2023; 19:e1011562 [View Article]
     [Google Scholar]
  15. Walter CT, Barr JN. Recent advances in the molecular and cellular biology of bunyaviruses. J Gen Virol 2011; 92:2467–2484 [View Article] [PubMed]
     [Google Scholar]
  16. Piper ME, Sorenson DR, Gerrard SR. Efficient cellular release of Rift Valley fever virus requires genomic RNA. PLoS One 2011; 6:e18070 [View Article] [PubMed]
     [Google Scholar]
  17. Woelfl F, Léger P, Oreshkova N, Pahmeier F, Windhaber S et al. Novel Toscana virus reverse genetics system establishes NSS as an antagonist of type I interferon responses. Viruses 2020; 12:400 [View Article] [PubMed]
     [Google Scholar]
  18. Gori-Savellini G, Valentini M, Cusi MG. Toscana virus NSs protein inhibits the induction of type I interferon by interacting with RIG-I. J Virol 2013; 87:6660–6667 [View Article] [PubMed]
     [Google Scholar]
  19. Gori Savellini G, Anichini G, Gandolfo C, Prathyumnan S, Cusi MG. Toscana virus non-structural protein NSs acts as E3 ubiquitin ligase promoting RIG-I degradation. PLoS Pathog 2019; 15:e1008186 [View Article]
     [Google Scholar]
  20. Kalveram B, Ikegami T. Toscana virus NSs protein promotes degradation of double-stranded RNA-dependent protein kinase. J Virol 2013; 87:3710–3718 [View Article] [PubMed]
     [Google Scholar]
  21. Valassina M, Cusi MG, Valensin PE. A Mediterranean arbovirus: the Toscana virus. J Neurovirol 2003; 9:577–583 [View Article] [PubMed]
     [Google Scholar]
  22. Elliott RM. Emerging viruses: the Bunyaviridae. Mol Med 1997; 3:572–577 [PubMed]
     [Google Scholar]
  23. Barker J, daSilva LLP, Crump CM. Mechanisms of bunyavirus morphogenesis and egress. J Gen Virol 2023; 104:1–11 [View Article] [PubMed]
     [Google Scholar]
  24. Alexander AJT, Confort M-P, Desloire S, Dunlop JI, Kuchi S et al. Development of A reverse genetics system for Toscana virus (Lineage A). Viruses 2020; 12:1–15 [View Article] [PubMed]
     [Google Scholar]
  25. Ayhan N, Baklouti A, Prudhomme J, Walder G, Amaro F et al. Practical guidelines for studies on sandfly-borne Phleboviruses: Part I: important points to consider ante field work. Vector-Borne Zoo Dis 2017; 17:73–80 [View Article]
     [Google Scholar]
  26. Sabin AB, Philip CB, Paul JR. Phlebotomus (pappataci or sandfly) fever: a disease of military importance summary of existing knowledge and preliminary report of original investigations. J Am Med Assoc 1944; 125:693–699
     [Google Scholar]
  27. Eitrem R, Stylianou M, Niklasson B. High prevalence rates of antibody to three sandfly fever viruses (Sicilian, Naples, and Toscana) among Cypriots. Epidemiol Infect 1991; 107:685–691 [View Article] [PubMed]
     [Google Scholar]
  28. Karabatsos N. Supplement to International Catalogue of Arboviruses including certain other viruses of vertebrates. Am J Trop Med Hyg 1978; 27:372–440 [View Article] [PubMed]
     [Google Scholar]
  29. Eitrem R, Vene S, Niklasson B. Incidence of sand fly fever among Swedish United Nations soldiers on Cyprus during 1985. Am J Trop Med Hyg 1990; 43:207–211 [View Article] [PubMed]
     [Google Scholar]
  30. Niklasson B, Eitrem R. Sandfly fever among Swedish UN troops in Cyprus. Lancet 1985; 325:1212 [View Article]
     [Google Scholar]
  31. Calisher C, Weinberg A, Muth D, Lazuick J. Toscana virus infection in United States citizen returning from Italy. Lancet 1987; 329:165–166 [View Article]
     [Google Scholar]
  32. Schwarz T, Gilch S, Jäger G. Travel-related Toscana virus infection. Lancet 1993; 342:803–804 [View Article]
     [Google Scholar]
  33. Schwarz TF, Jäger G, Gilch S, Pauli C. Serosurvey and laboratory diagnosis of imported sandfly fever virus, serotype toscana, infection in Germany. Epidemiol Infect 1995; 114:501–510
     [Google Scholar]
  34. Depaquit J, Grandadam M, Fouque F, Andry PE, Peyrefitte C. Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: a review. Euro Surveill 2010; 15:40–47 [View Article]
     [Google Scholar]
  35. Braito A, Corbisiero R, Corradini S, Fiorentini C, Ciufolini MG. Toscana virus infections of the central nervous system in children: a report of 14 cases. J Pediatr 1998; 132:144–148 [View Article]
     [Google Scholar]
  36. Valassina M, Meacci F, Valensin PE, Cusi MG. Detection of neurotropic viruses circulating in Tuscany: the incisive role of Toscana virus. J Med Virol 2000; 60:86–90 [View Article] [PubMed]
     [Google Scholar]
  37. Valassina M, Cuppone AM, Bianchi S, Santini L, Cusi MG. Evidence of Toscana virus variants circulating in Tuscany, Italy, during the Summers of 1995 to 1997. J Clin Microbiol 1998; 36:2103–2104 [View Article]
     [Google Scholar]
  38. Mendoza-Montero J, Gámez-Rueda MI, Navarro-Marí JM, de la Rosa-Fraile M, Oyonarte-Gómez S. Infections due to sandfly fever virus serotype Toscana in Spain. Clin Infect Dis 1998; 27:434–436 [View Article] [PubMed]
     [Google Scholar]
  39. Cusi MG, Savellini GG, Zanelli G. Toscana virus epidemiology: from Italy to beyond. Open Virol J 2010; 4:22–28 [View Article]
     [Google Scholar]
  40. Terrosi C, Olivieri R, Bianco C, Cellesi C, Cusi MG. Age-dependent seroprevalence of Toscana virus in central Italy and correlation with the clinical profile. Clin Vaccine Immunol 2009; 16:1251–1252 [View Article] [PubMed]
     [Google Scholar]
  41. Valassina M, Valentini M, Pugliese A, Valensin PE, Cusi MG. Serological survey of Toscana virus infections in a high-risk population in Italy. Clin Vaccine Immunol 2003; 10:483–484 [View Article]
     [Google Scholar]
  42. Marchi S, Trombetta CM, Kistner O, Montomoli E. Seroprevalence study of Toscana virus and viruses belonging to the sandfly fever naples antigenic complex in central and southern Italy. J Infect Public Health 2017; 10:866–869
     [Google Scholar]
  43. Christova I, Panayotova E, Trifonova I, Taseva E, Gladnishka T et al. Serologic evidence of widespread Toscana virus infection in Bulgaria. J Infect Public Health 2020; 13:164–166 [View Article]
     [Google Scholar]
  44. Dersch R, Sophocleous A, Cadar D, Emmerich P, Schmidt-Chanasit J et al. Toscana virus encephalitis in Southwest Germany: a retrospective study. BMC Neurol 2021; 21:495 [View Article] [PubMed]
     [Google Scholar]
  45. Ortuño M, Muñoz C, Spitzová T, Sumova P, Iborra MA et al. Exposure to Phlebotomus perniciosus sandfly vectors is positively associated with Toscana virus and Leishmania infantum infection in human blood donors in Murcia Region, southeast Spain. Transbound Emerg Dis 2022; 69:e1854–e1864 [View Article] [PubMed]
     [Google Scholar]
  46. Erguler K, Pontiki I, Zittis G, Proestos Y, Christodoulou V et al. A climate-driven and field data-assimilated population dynamics model of sand flies. Sci Rep 2019; 9:2469 [View Article] [PubMed]
     [Google Scholar]
  47. Fischer D, Moeller P, Thomas SM, Naucke TJ, Beierkuhnlein C. Combining climatic projections and dispersal ability: a method for estimating the responses of sandfly vector species to climate change. PLoS Negl Trop Dis 2011; 5:e1407 [View Article] [PubMed]
     [Google Scholar]
  48. Weaver SC, Charlier C, Nikos V, Viral LM. Other emerging vector-borne. Annu Rev Med 2018; 69:395–408 [View Article]
     [Google Scholar]
  49. Martínez-García FA, Moreno-Docón A, Segovia-Hernández M, Fernández-Barreiro A. Deafness as a sequela of Toscana virus meningitis. Med Clin 2008; 130:639 [View Article] [PubMed]
     [Google Scholar]
  50. Amaro F, Luz T, Parreira P, Marchi A, Ciufolini MG et al. Serological evidence of Toscana virus infection in Portuguese patients. Epidemiol Infect 2012; 140:1147–1150 [View Article] [PubMed]
     [Google Scholar]
  51. Papa A, Kesisidou C, Kontana A, Arapidou Z, Petropoulou D. Phlebovirus infection in Greece: a case report. Hippokratia 2015; 19:189–191
     [Google Scholar]
  52. Howell BA, Azar MM, Landry ML, Shaw AC. Toscana virus encephalitis in a traveler returning to the United States. J Clin Microbiol 2015; 53:1445–1447 [View Article] [PubMed]
     [Google Scholar]
  53. Laroche L, Jourdain F, Ayhan N, Bañuls A-L, Charrel R et al. Incubation period for neuroinvasive Toscana virus infections. Emerg Infect Dis 2021; 27:3147–3150 [View Article] [PubMed]
     [Google Scholar]
  54. Ergunay K, Kaplan B, Okar S, Akkutay-Yoldar Z, Kurne A et al. Urinary detection of Toscana virus nucleic acids in neuroinvasive infections. J Clin Virol 2015; 70:89–92 [View Article] [PubMed]
     [Google Scholar]
  55. Popescu CP, Cotar AI, Dinu S, Zaharia M, Tardei G et al. Emergence of Toscana virus, Romania, 2017-2018. Emerg Infect Dis 2021; 27:1482–1485 [View Article] [PubMed]
     [Google Scholar]
  56. Mathur A, Khanna N, Kulshreshtha R, Maitra SC, Chaturvedi UC. Viruria during acute Japanese encephalitis virus infection. Int J Exp Pathol 1995; 76:103–109 [PubMed]
     [Google Scholar]
  57. Barzon L, Pacenti M, Franchin E, Pagni S, Martello T et al. Excretion of West Nile virus in urine during acute infection. J Infect Dis 2013; 208:1086–1092 [View Article] [PubMed]
     [Google Scholar]
  58. Ludlow M, Kortekaas J, Herden C, Hoffmann B, Tappe D et al. Neurotropic virus infections as the cause of immediate and delayed neuropathology. Acta Neuropathol 2016; 131:159–184 [View Article] [PubMed]
     [Google Scholar]
  59. García San Miguel L, Sierra MJ, Vazquez A, Fernandez-Martínez B, Molina R et al. Phlebovirus-associated diseases transmitted by phlebotominae in Spain: are we at risk?. Enfermedades Infecc y Microbiol Clin 2021; 39:345–351 [View Article]
     [Google Scholar]
  60. Serata D, Rapinesi C, Del Casale A, Simonetti A, Mazzarini L et al. Personality changes after Toscana virus (TOSV) encephalitis in a 49-year-old man: a case report. Int J Neurosci 2011; 121:165–169 [View Article] [PubMed]
     [Google Scholar]
  61. Dionisio D, Valassina M, Ciufolini MG, Vivarelli A, Esperti F et al. Encephalitis without meningitis due to sandfly fever virus serotype toscana. Clin Infect Dis 2001; 32:1241–1243 [View Article] [PubMed]
     [Google Scholar]
  62. Papa A, Paraforou T, Papakonstantinou I, Pagdatoglou K, Kontana A et al. Severe encephalitis caused by Toscana virus, Greece. Emerg Infect Dis 2014; 20:1417–1419 [View Article] [PubMed]
     [Google Scholar]
  63. Bartels S, de Boni L, Kretzschmar HA, Heckmann JG. Lethal encephalitis caused by the Toscana virus in an elderly patient. J Neurol 2012; 259:175–177 [View Article] [PubMed]
     [Google Scholar]
  64. Baldelli F, Ciufolini MG, Francisci D, Marchi A, Venturi G et al. Unusual presentation of life-threatening Toscana virus meningoencephalitis. Clin Infect Dis 2004; 38:515–520 [View Article] [PubMed]
     [Google Scholar]
  65. Zanelli G, Bianco C, Cusi MG. Testicular involvement during Toscana virus infection: an unusual manifestation?. Infection 2013; 41:735–736 [View Article] [PubMed]
     [Google Scholar]
  66. Gonen OM, Sacagiu T. Sensory polymyeloradiculopathy associated with Toscana virus infection. J Neurovirol 2013; 19:508–510 [View Article]
     [Google Scholar]
  67. Tschumi F, Schmutz S, Kufner V, Heider M, Pigny F et al. Meningitis and epididymitis caused by Toscana virus infection imported to Switzerland diagnosed by metagenomic sequencing: a case report. BMC Infect Dis 2019; 19:591 [View Article] [PubMed]
     [Google Scholar]
  68. Mascitti H, Calin R, Dinh A, Makhloufi S, Davido B. Testicular pain associated with clear fluid meningitis: how many cases of Toscana virus are we missing?. Int J Infect Dis 2020; 93:198–200 [View Article]
     [Google Scholar]
  69. Matusali G, D’Abramo A, Terrosi C, Carletti F, Colavita F et al. Infectious Toscana virus in seminal fluid of young man returning from Elba Island, Italy. Emerg Infect Dis 2022; 28:865–869 [View Article] [PubMed]
     [Google Scholar]
  70. Oechtering J, Petzold GC. Acute hydrocephalus due to impaired CSF resorption in Toscana virus meningoencephalitis. Neurology 2012; 79:829–831 [View Article]
     [Google Scholar]
  71. Rota E, Morelli N, Immovilli P, De Mitri P, Guidetti D. Guillain-Barré-like axonal polyneuropathy associated with Toscana virus infection. Medicine 2017; 96:e8081 [View Article]
     [Google Scholar]
  72. Okar SV, Bekircan-Kurt CE, Hacıoğlu S, Erdem-Özdamar S, Özkul A et al. Toscana virus associated with Guillain-Barré syndrome: a case-control study. Acta Neurol Belg 2021; 121:661–668 [View Article] [PubMed]
     [Google Scholar]
  73. Sanbonmatsu-Gámez S, Pérez-Ruiz M, Palop-Borrás B, Navarro-Marí JM. Unusual manifestation of toscana virus infection, Spain. Emerg Infect Dis 2009; 15:347–348 [View Article] [PubMed]
     [Google Scholar]
  74. Vilibic-Cavlek T, Zidovec-Lepej S, Ledina D, Knezevic S, Savic V et al. Clinical, virological, and immunological findings in patients with Toscana neuroinvasive disease in Croatia: report of three cases. Trop Med Infect Dis 2020; 5:144 [View Article] [PubMed]
     [Google Scholar]
  75. Braito A, Corbisiero R, Corradini S, Marchi B, Sancasciani N et al. Evidence of Toscana virus infections without central nervous system involvement: a serological study. Eur J Epidemiol 1997; 13:761–764 [View Article] [PubMed]
     [Google Scholar]
  76. Ranaldi R, Goteri G, Biagetti S, Cusi MG, Rossini S. Histological description of the lymphadenopathy related to Toscana virus infection. Report of a case. Pathol - Res Pract 2011; 207:197–201 [View Article]
     [Google Scholar]
  77. Ocal M, Orsten S, Inkaya AC, Yetim E, Acar NP et al. Ongoing activity of Toscana virus genotype A and West Nile virus lineage 1 strains in Turkey: a clinical and field survey. Zoonos Public Health 2014; 61:480–491 [View Article] [PubMed]
     [Google Scholar]
  78. Mosnier E, Charrel R, Vidal B, Ninove L, Schleinitz N et al. Toscana virus myositis and fasciitis. Med Mal Infect 2013; 43:208–210 [View Article] [PubMed]
     [Google Scholar]
  79. Crum-Cianflone NF. Bacterial, fungal, parasitic, and viral myositis. Clin Microbiol Rev 2008; 21:473–494 [View Article] [PubMed]
     [Google Scholar]
  80. Charrel RN, Bichaud L, de Lamballerie X. Emergence of Toscana virus in the Mediterranean area. World J Virol 2012; 1:135–141 [View Article] [PubMed]
     [Google Scholar]
  81. Valassina M, Valentini M, Valensin PE, Cusi MG. Fast duplex one-step RT-PCR for rapid differential diagnosis of entero- or Toscana virus meningitis. Diagn Microbiol Infect Dis 2002; 43:201–205 [View Article] [PubMed]
     [Google Scholar]
  82. Valassina M, Cusi MG, Valensin PE. Rapid identification of Toscana virus by nested PCR during an outbreak in the Siena area of Italy. J Clin Microbiol 1996; 34:2500–2502 [View Article] [PubMed]
     [Google Scholar]
  83. Sánchez-Seco M-P, Echevarría J-M, Hernández L, Estévez D, Navarro-Marí J-M et al. Detection and identification of Toscana and other phleboviruses by RT-nested-PCR assays with degenerated primers. J Med Virol 2003; 71:140–149 [View Article] [PubMed]
     [Google Scholar]
  84. Pérez-Ruiz M, Collao X, Navarro-Marí JM, Tenorio A. Reverse transcription, real-time PCR assay for detection of Toscana virus. J Clin Virol 2007; 39:276–281 [View Article] [PubMed]
     [Google Scholar]
  85. Ergünay K, Saygan MB, Aydoğan S, Lo MM, Weidmann M et al. Sandfly fever virus activity in central/northern Anatolia, Turkey: first report of Toscana virus infections. Clin Microbiol Infect 2011; 17:575–581 [View Article] [PubMed]
     [Google Scholar]
  86. Weidmann M, Sanchez-Seco MP, Sall AA, Ly PO, Thiongane Y et al. Rapid detection of important human pathogenic Phleboviruses. J Clin Virol 2008; 41:138–142 [View Article] [PubMed]
     [Google Scholar]
  87. Brisbarre N, Plumet S, Cotteaux-Lautard C, Emonet SF, Pages F et al. A rapid and specific real time RT-PCR assay for diagnosis of Toscana virus infection. J Clin Virol 2015; 66:107–111 [View Article] [PubMed]
     [Google Scholar]
  88. Thirion L, Pezzi L, Pedrosa-Corral I, Sanbonmatsu-Gamez S, de Lamballerie X et al. Evaluation of a trio Toscana virus real-time RT-PCR assay targeting three genomic regions within nucleoprotein gene. Pathogens 2021; 10:1–11 [View Article] [PubMed]
     [Google Scholar]
  89. Mori A, Matucci A, Pomari E, Accordini S, Piubelli C et al. Urine: a pitfall for molecular detection of Toscana virus? An analytical proof-of-concept study. Viruses 2024; 16:98 [View Article] [PubMed]
     [Google Scholar]
  90. Amodio E, Cusi MG, Valenti RM, Valentini M, Mammina C et al. Immunoglobulin M seropositivity for Toscana virus in a random population sample in Sicily. Int J Infect Dis 2012; 16:e633–5 [View Article] [PubMed]
     [Google Scholar]
  91. Zhioua E, Moureau G, Chelbi I, Ninove L, Bichaud L et al. Punique virus, a novel phlebovirus, related to sandfly fever Naples virus, isolated from sandflies collected in Tunisia. J Gen Virol 2010; 91:1275–1283 [View Article] [PubMed]
     [Google Scholar]
  92. Ergünay K, Litzba N, Lo MM, Aydoğan S, Saygan MB et al. Performance of various commercial assays for the detection of Toscana virus antibodies. Vector Borne Zoonotic Dis 2011; 11:781–787 [View Article] [PubMed]
     [Google Scholar]
  93. Charrel RN, Gallian P, Navarro-Mari J-M, Nicoletti L, Papa A et al. Emergence of Toscana virus in Europe. Emerg Infect Dis 2005; 11:1657–1663 [View Article] [PubMed]
     [Google Scholar]
  94. Gámbaro F, Pérez AB, Prot M, Agüera E, Baidaliuk A et al. Untargeted metagenomic sequencing identifies Toscana virus in patients with idiopathic meningitis, southern Spain, 2015 to 2019. Euro Surveill 2023; 28:1–12 [View Article] [PubMed]
     [Google Scholar]
  95. Cusi MG, Savellini GG. Diagnostic tools for Toscana virus infection. Expert Rev Anti Infect Ther 2011; 9:799–805 [View Article] [PubMed]
     [Google Scholar]
  96. Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P et al. A historical overview of the classification, evolution, and dispersion of leishmania parasites and sandflies. PLoS Negl Trop Dis 2016; 10:e0004349 [View Article] [PubMed]
     [Google Scholar]
  97. Remadi L, Farjallah D, Chargui N, Belgacem S, Baba H et al. Blood meal analysis and molecular detection of mammalian Leishmania DNA in wild-caught Sergentomyia spp. from Tunisia and Saudi Arabia. Parasitol Res 2023; 122:2181–2191 [View Article] [PubMed]
     [Google Scholar]
  98. Cecílio P, Cordeiro-da-Silva A, Oliveira F. Sand flies: basic information on the vectors of leishmaniasis and their interactions with Leishmania parasites. Commun Biol 2022; 5:305 [View Article] [PubMed]
     [Google Scholar]
  99. Killick-Kendrick R. The biology and control of phlebotomine sand flies. Clin Dermatol 1999; 17:279–289 [View Article] [PubMed]
     [Google Scholar]
  100. Chalghaf B, Chemkhi J, Mayala B, Harrabi M, Benie GB et al. Ecological niche modeling predicting the potential distribution of Leishmania vectors in the Mediterranean basin: impact of climate change. Parasit Vectors 2018; 11:461 [View Article] [PubMed]
     [Google Scholar]
  101. Ready PD. Biology of phlebotomine sand flies as vectors of disease agents. Annu Rev Entomol 2013; 58:227–250 [View Article] [PubMed]
     [Google Scholar]
  102. Ayhan N, Charrel RN. Of phlebotomines (sandflies) and viruses: a comprehensive perspective on a complex situation. Curr Opin Insect Sci 2017; 22:117–124 [View Article] [PubMed]
     [Google Scholar]
  103. Nicoletti L, Ciufolini MG, Verani P. Sandfly fever viruses in Italy. In Imported Virus Infections Vienna, Austria: Springer Vienna; pp 41–47 [View Article]
     [Google Scholar]
  104. Verani P, Ciufolini MG, Caciolli S, Renzi A, Nicoletti L et al. Ecology of viruses isolated from sand flies in Italy and characterized of a new Phlebovirus (Arabia virus). Am J Trop Med Hyg 1988; 38:433–439 [View Article] [PubMed]
     [Google Scholar]
  105. Ayhan N, Charrel RN. Emergent sand fly–borne Phleboviruses in the Balkan region. Emerg Infect Dis 2018; 24:2324–2330 [View Article]
     [Google Scholar]
  106. Es-sette N, Ajaoud M, Anga L, Mellouki F, Lemrani M. Toscana virus isolated from sandflies, Morocco. Parasit Vectors 2015; 8:205 [View Article] [PubMed]
     [Google Scholar]
  107. Ergunay K, Kasap OE, Orsten S, Oter K, Gunay F et al. Phlebovirus and Leishmania detection in sandflies from eastern Thrace and northern Cyprus. Parasit Vectors 2014; 7:575 [View Article] [PubMed]
     [Google Scholar]
  108. Ciufolini MG, Maroli M, Verani P. Growth of two phleboviruses after experimental infection of their suspected sand fly vector, Phlebotomus perniciosus (Diptera: Psychodidae). Am J Trop Med Hyg 1985; 34:174–179 [View Article] [PubMed]
     [Google Scholar]
  109. Tesh RB, Modi GB. Studies on the biology of Phleboviruses in sand flies (Diptera: Psychodidae). I. Experimental infection of the vector. Am J Trop Med Hyg 1984; 33:1007–1016 [View Article]
     [Google Scholar]
  110. Ciufolini MG, Maroli M, Guandalini E, Marchi A, Verani P. Experimental studies on the maintenance of Toscana and Arbia viruses (Bunyaviridae: Phlebovirus). Am J Trop Med Hyg 1989; 40:669–675 [View Article]
     [Google Scholar]
  111. Tesh RB, Lubroth J, Guzman H. Simulation of arbovirus overwintering: survival of Toscana virus (Bunyaviridae:Phlebovirus) in its natural sand fly vector Phlebotomus perniciosus. Am J Trop Med Hyg 1992; 47:574–581 [View Article] [PubMed]
     [Google Scholar]
  112. Maroli M, Ciufolini MG, Verani P. Vertical transmission of Toscana virus in the sandfly, Phlebotomus perniciosus, via the second gonotrophic cycle. Med Vet Entomol 1993; 7:283–286 [View Article]
     [Google Scholar]
  113. Bergren NA, Kading RC. The ecological significance and implications of transovarial transmission among the vector-borne Bunyaviruses: a review. Insects 2018; 9:173 [View Article] [PubMed]
     [Google Scholar]
  114. Jancarova M, Bichaud L, Hlavacova J, Priet S, Ayhan N et al. Experimental infection of sand flies by Massilia virus and viral transmission by co-feeding on sugar meal. Viruses 2019; 11:332 [View Article] [PubMed]
     [Google Scholar]
  115. Charrel RN, Moureau G, Temmam S, Izri A, Marty P et al. Massilia virus, a novel Phlebovirus (Bunyaviridae) isolated from sandflies in the Mediterranean. Vector Borne Zoonotic Dis 2009; 9:519–530 [View Article] [PubMed]
     [Google Scholar]
  116. Laroche L, Ayhan N, Charrel R, Bañuls A-L, Prudhomme J. Persistence of Toscana virus in sugar and blood meals of phlebotomine sand flies: epidemiological and experimental consequences. Sci Rep 2023; 13:1–7 [View Article]
     [Google Scholar]
  117. Durden LA, Mullen GR. Medical and Veterinary Entomology Elsevier; 2018 [View Article]
     [Google Scholar]
  118. De Colmenares M, Portús M, Botet J, Dobaño C, Gállego M et al. Identification of blood meals of Phlebotomus perniciosus (Diptera: Psychodidae) in Spain by a competitive enzyme-linked immunosorbent assay biotin/avidin method. J Med Entomol 1995; 32:229–233 [View Article]
     [Google Scholar]
  119. Svobodová M, Sádlová J, Chang KP, Volf P. Short report: distribution and feeding preference of the sand flies Phlebotomus sergenti and P. papatasi in a cutaneous leishmaniasis focus in Sanliurfa, Turkey. Am J Trop Med Hyg 2003; 68:6–9 [PubMed]
     [Google Scholar]
  120. Maia C, Parreira R, Cristóvão JM, Freitas FB, Afonso MO et al. Molecular detection of Leishmania DNA and identification of blood meals in wild caught phlebotomine sand flies (Diptera: Psychodidae) from southern Portugal. Parasites Vectors 2015; 8:1–10 [View Article]
     [Google Scholar]
  121. Messahel NE, Benallal KE, Halada P, Lafri I, Manseur H et al. Identification of blood source preferences and Leishmania infection in sand flies (Diptera: Psychodidae) in north-eastern Algeria. Vet Parasitol Reg Stud Reports 2022; 31:100729 [View Article] [PubMed]
     [Google Scholar]
  122. Dincer E, Karapinar Z, Oktem M, Ozbaba M, Ozkul A et al. Canine infections and partial S segment sequence analysis of Toscana virus in Turkey. Vector Borne Zoonotic Dis 2016; 16:611–618 [View Article] [PubMed]
     [Google Scholar]
  123. Alho AM, Pita J, Amaro A, Amaro F, Schnyder M et al. Seroprevalence of vector-borne pathogens and molecular detection of Borrelia afzelii in military dogs from Portugal. Parasites Vectors 2016; 9:1–6 [View Article]
     [Google Scholar]
  124. Dahmani M, Alwassouf S, Grech-Angelini S, Marié J-L, Davoust B et al. Seroprevalence of Toscana virus in dogs from Corsica, France. Parasit Vectors 2016; 9:381 [View Article] [PubMed]
     [Google Scholar]
  125. Tahir D, Alwassouf S, Loudahi A, Davoust B, Charrel RN. Seroprevalence of Toscana virus in dogs from Kabylia (Algeria). Clin Microbiol Infect 2016; 22:e16–7 [View Article] [PubMed]
     [Google Scholar]
  126. Sellali S, Lafri I, Hachid A, Ayhan N, Benbetka C et al. Presence of the sandfly-borne phlebovirus (Toscana virus) in different bio-geographical regions of Algeria demonstrated by a microneutralisation-based seroprevalence study in owned dogs. Comp Immunol Microbiol Infect Dis 2022; 88:101861 [View Article] [PubMed]
     [Google Scholar]
  127. Sakhria S, Alwassouf S, Fares W, Bichaud L, Dachraoui K et al. Presence of sandfly-borne phleboviruses of two antigenic complexes (Sandfly fever Naples virus and Sandfly fever Sicilian virus) in two different bio-geographical regions of Tunisia demonstrated by a microneutralisation-based seroprevalence study in dogs. Parasit Vectors 2014; 7:476 [View Article] [PubMed]
     [Google Scholar]
  128. Alwassouf S, Christodoulou V, Bichaud L, Ntais P, Mazeris A et al. 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 2016; 10:e0005063 [View Article] [PubMed]
     [Google Scholar]
  129. Pereira A, Ayhan N, Cristóvão JM, Vilhena H, Martins  et al. Antibody response to Toscana virus and sandfly fever sicilian virus in cats naturally exposed to phlebotomine sand fly bites in Portugal. Microorganisms 2019; 7:339 [View Article] [PubMed]
     [Google Scholar]
  130. Muñoz C, Ayhan N, Ortuño M, Ortiz J, Gould EA et al. Experimental infection of dogs with Toscana virus and sandfly fever Sicilian virus to determine their potential as possible vertebrate hosts. Microorganisms 2020; 8:596 [View Article] [PubMed]
     [Google Scholar]
  131. Dachraoui K, Chelbi I, Labidi I, Ben Osman R, Sayadi A et al. The role of the Leishmania infantum infected dogs as a potential reservoir host for Toscana virus in a zoonotic visceral leishmaniasis focus of northern Tunisia. Viruses 2023; 15:1–16 [View Article] [PubMed]
     [Google Scholar]
  132. Dincer E, Gargari S, Ozkul A, Ergunay K. Potential animal reservoirs of Toscana virus and coinfections with Leishmania infantum in Turkey. Am J Trop Med Hyg 2015; 92:690–697 [View Article] [PubMed]
     [Google Scholar]
  133. Maia C, Alwassouf S, Cristóvão JM, Ayhan N, Pereira A et al. Serological association between Leishmania infantum and sand fly fever Sicilian (but not Toscana) virus in sheltered dogs from southern Portugal. Parasit Vectors 2017; 10:92 [View Article] [PubMed]
     [Google Scholar]
  134. Ayhan N, Sherifi K, Taraku A, Bërxholi K, Charrel RN. High rates of neutralizing antibodies to Toscana and sandfly fever Sicilian viruses in Livestock, Kosovo. Emerg Infect Dis 2017; 23:989–992 [View Article] [PubMed]
     [Google Scholar]
  135. Al-numaani SA, Al-Nemari AT, El-Kafrawy SA, Hassan AM, Tolah AM et al. Seroprevalence of Toscana and sandfly fever Sicilian viruses in humans and livestock animals from western Saudi Arabia. One Health 2023; 17:100601 [View Article]
     [Google Scholar]
  136. Navarro-Marí JM, Palop-Borrás B, Pérez-Ruiz M, Sanbonmatsu-Gámez S. Serosurvey study of Toscana virus in domestic animals, Granada, Spain. Vector Borne Zoonotic Dis 2011; 11:583–587 [View Article] [PubMed]
     [Google Scholar]
  137. Hacioglu S, Dincer E, Isler CT, Karapinar Z, Ataseven VS et al. A snapshot avian surveillance reveals West Nile virus and evidence of wild birds participating in Toscana virus circulation. Vector Borne Zoonotic Dis 2017; 17:698–708 [View Article] [PubMed]
     [Google Scholar]
  138. Ayhan N, Rodríguez-Teijeiro JD, López-Roig M, Vinyoles D, Ferreres JA et al. High rates of antibodies against Toscana and Sicilian phleboviruses in common quail Coturnix coturnix birds. Front Microbiol 2022; 13:1091908 [View Article] [PubMed]
     [Google Scholar]
  139. Hacioglu S, Ozkul A. Do birds play a role in the transmission of Toscana virus? Initial isolation results from birds in northernmost Türkiye. Zoonoses and Public Health 2024; 71:225–235 [View Article]
     [Google Scholar]
  140. Moratelli R, Calisher CH. Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses?. Mem Inst Oswaldo Cruz 2015; 110:1–22 [View Article] [PubMed]
     [Google Scholar]
  141. Ayhan N, López-Roig M, Monastiri A, Charrel RN, Serra-Cobo J. Seroprevalence of Toscana virus and sandfly fever Sicilian virus in European bat colonies measured using a neutralization test. Viruses 2021; 13:88 [View Article]
     [Google Scholar]
  142. Kraemer MUG, Reiner RC Jr, Brady OJ, Messina JP, Gilbert M et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol 2019; 4:854–863 [View Article]
     [Google Scholar]
  143. Caminade C, McIntyre KM, Jones AE. Impact of recent and future climate change on vector-borne diseases. Ann N Y Acad Sci 2019; 1436:157–173 [View Article] [PubMed]
     [Google Scholar]
  144. Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vector Ecol 2011; 36:S1–S9 [View Article]
     [Google Scholar]
  145. Aspöck H, Gerersdorfer T, Formayer H, Walochnik J. Sandflies and sandfly-borne infections of humans in central Europe in the light of climate change. Wien Klin Wochenschr 2008; 120:24–29 [View Article]
     [Google Scholar]
  146. Naucke TJ, Lorentz S, Rauchenwald F, Aspöck H. Phlebotomus (Transphlebotomus) mascittii Grassi, 1908, in Carinthia: first record of the occurrence of sandflies in Austria (Diptera: Psychodidae: Phlebotominae). Parasitol Res 2011; 109:1161–1164 [View Article]
     [Google Scholar]
  147. Poeppl W, Obwaller AG, Weiler M, Burgmann H, Mooseder G et al. Emergence of sandflies (Phlebotominae) in Austria, a Central European country. Parasitol Res 2013; 112:4231–4237 [View Article] [PubMed]
     [Google Scholar]
  148. Oerther S. Phlebotomus mascittii as potential vector of human pathogens in southwest Germany. Entomol Ornithol Herpetol 2020; 9:1–3
     [Google Scholar]
  149. Naucke TJ, Menn B, Massberg D, Lorentz S. Sandflies and leishmaniasis in Germany. Parasitol Res 2008; 103:65–68 [View Article]
     [Google Scholar]
  150. Ayhan N, Prudhomme J, Laroche L, Bañuls A-L, Charrel RN. Broader geographical distribution of Toscana virus in the mediterranean region suggests the existence of larger varieties of sand fly vectors. Microorganisms 2020; 8:114 [View Article]
     [Google Scholar]
  151. Knechtli R, Jenni L. Distribution and relative density of three sandfly (Diptera: Phlebotominae) species in southern Switzerland. Ann Parasitol Hum Comp 1989; 64:53–63 [View Article]
     [Google Scholar]
  152. Liang G, Gao X, Gould EA. Factors responsible for the emergence of arboviruses; strategies, challenges and limitations for their control. Emerg Microb Infect 2015; 4:1–5 [View Article]
     [Google Scholar]
  153. Maroli M, Feliciangeli MD, Bichaud L, Charrel RN, Gradoni L. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol 2013; 27:123–147 [View Article] [PubMed]
     [Google Scholar]
  154. Remadi L, Chargui N, Jiménez M, Molina R, Haouas N et al. Molecular detection and identification of Leishmania DNA and blood meal analysis in Phlebotomus (Larroussius) species. PLoS Negl Trop Dis 2020; 14:e0008077 [View Article] [PubMed]
     [Google Scholar]
  155. Pombi M, Giacomi A, Barlozzari G, Mendoza-Roldan J, Macrì G et al. Molecular detection of Leishmania (Sauroleishmania) tarentolae in human blood and Leishmania (Leishmania) infantum in Sergentomyia minuta: unexpected host-parasite contacts. Med Vet Entomol 2020; 34:470–475 [View Article] [PubMed]
     [Google Scholar]
  156. Campino L, Cortes S, Dionísio L, Neto L, Afonso MO et al. The first detection of Leishmania major in naturally infected Sergentomyia minuta in Portugal. Mem Inst Oswaldo Cruz 2013; 108:516–518 [View Article] [PubMed]
     [Google Scholar]
  157. Berdjane-Brouk Z, Koné AK, Djimdé AA, Charrel RN, Ravel C et al. First detection of Leishmania major DNA in Sergentomyia (Spelaeomyia) darlingi from cutaneous leishmaniasis foci in Mali. PLoS One 2012; 7:e28266 [View Article] [PubMed]
     [Google Scholar]
  158. Maia C, Depaquit J. Can Sergentomyia (Diptera, Psychodidae) play a role in the transmission of mammal-infecting Leishmania?. Parasite 2016; 23:55 [View Article] [PubMed]
     [Google Scholar]
  159. Latrofa MS, Iatta R, Dantas-Torres F, Annoscia G, Gabrielli S et al. Detection of Leishmania infantum DNA in phlebotomine sand flies from an area where canine leishmaniosis is endemic in southern Italy. Vet Parasitol 2018; 253:39–42 [View Article]
     [Google Scholar]
  160. Charrel RN, Izri A, Temmam S, de Lamballerie X, Parola P. Toscana virus RNA in Sergentomyia minuta flies. Emerg Infect Dis 2006; 12:1299–1300 [View Article] [PubMed]
     [Google Scholar]
  161. Geevarghese G, Arankalle VA, Jadi R, Kanojia PC, Joshi MV et al. Detection of Chandipura virus from sand flies in the genus Sergentomyia (Diptera: Phlebotomidae) at Karimnagar district, Andhra Pradesh, India. J Med Entomol 2005; 42:495–496 [View Article]
     [Google Scholar]
  162. Ticha L, Volfova V, Mendoza-Roldan JA, Bezerra-Santos MA, Maia C et al. Experimental feeding of Sergentomyia minuta on reptiles and mammals: comparison with Phlebotomus papatasi. Parasites Vectors 2023; 16:1–9 [View Article] [PubMed]
     [Google Scholar]
  163. Afonso MMDS, Duarte R, Miranda JC, Caranha L, Rangel EF. Studies on the feeding habits of Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva, 1912) (Diptera: Psychodidae: Phlebotominae) populations from endemic areas of American visceral Leishmaniasis in Northeastern Brazil. J Trop Med 2012; 2012:858657 [View Article] [PubMed]
     [Google Scholar]
  164. Soares VYR, Silva JC da, Silva KR da, Cruz M do SP e, Santos MPD et al. Identification of blood meal sources of Lutzomyia longipalpis using polymerase chain reaction-restriction fragment length polymorphism analysis of the cytochrome B gene. Mem Inst Oswaldo Cruz 2014; 109:379–383 [View Article]
     [Google Scholar]
  165. Dias F de OP, Lorosa ES, Rebêlo JMM. Blood feeding sources and peridomiciliation of Lutzomyia longipalpis (Lutz & Neiva, 1912) (Psychodidae, Phlebotominae). Cad saúde Pública / Ministério da Saúde, Fundação Oswaldo Cruz, Esc Nac Saúde Pública 2003; 19:1373–1380 [View Article]
     [Google Scholar]
  166. Salomon OD. Lutzomyia longipalpis, gone with the wind and other variables. Neotrop Entomol 2021; 50:161–171 [View Article] [PubMed]
     [Google Scholar]
  167. Jennings M, Boorman J. The susceptibility of Lutzomyia longipalpis (Lutz and Neiva), Diptera, Psychodidae, to artificial infection with three viruses of the Phlebotomus fever group. Ann Trop Med Parasitol 1980; 74:455–462 [View Article] [PubMed]
     [Google Scholar]
  168. Tesh RB, Chaniotis BN, Peralta PH, Johnson KM. Ecology of viruses isolated from Panamanian. Am J Trop Med Hyg 1974; 23:258–269 [View Article]
     [Google Scholar]
  169. Palacios G, Tesh R, Travassos da Rosa A, Savji N, Sze W et al. Characterization of the Candiru antigenic complex (Bunyaviridae: Phlebovirus), a highly diverse and reassorting group of viruses affecting humans in tropical America. J Virol 2011; 85:3811–3820 [View Article] [PubMed]
     [Google Scholar]
  170. De Carvalho MS, De Lara Pinto AZ, Pinheiro A, Rodrigues JSV, Melo FL et al. Viola phlebovirus is a novel phlebotomus fever serogroup member identified in lutzomyia (lutzomyia) longipalpis from brazilian pantanal. Parasit Vectors 2018; 11:1–10
     [Google Scholar]
  171. Tesh RB, Modi GB. Development of a continuous cell line from the sand fly Lutzomyia longipalpis (Diptera: Psychodidae), and its susceptibility to infection with arboviruses. J Med Entomol 1983; 20:199–202 [View Article] [PubMed]
     [Google Scholar]
  172. Ferreira FV, Aguiar ERGR, Olmo RP, de Oliveira KPV, Silva EG et al. The small non-coding RNA response to virus infection in the Leishmania vector Lutzomyia longipalpis. PLoS Negl Trop Dis 2018; 12:e0006569 [View Article] [PubMed]
     [Google Scholar]
  173. Hoch AL, Turell MJ, Bailey CL. Replication of Rift valley fever virus in the sand fly Lutzomyia longipalpis. Am J Trop Med Hyg 1984; 33:295–299 [View Article]
     [Google Scholar]
  174. Hoch AL, Gargan TP 2nd, Bailey CL. Mechanical transmission of Rift Valley fever virus by hematophagous Diptera. Am J Trop Med Hyg 1985; 34:188–193 [View Article] [PubMed]
     [Google Scholar]
  175. Peterson AT, Campbell LP, Moo-Llanes DA, Travi B, González C et al. Influences of climate change on the potential distribution of Lutzomyia longipalpis sensu lato (Psychodidae: Phlebotominae). Int J Parasitol 2017; 47:667–674 [View Article] [PubMed]
     [Google Scholar]
  176. Schneider CA, Calvo E, Peterson KE. Arboviruses: how saliva impacts the journey from vector to host. Int J Mol Sci 2021; 22:9173 [View Article] [PubMed]
     [Google Scholar]
  177. Volf P, Tesarová P, Nohýnkova EN. Salivary proteins and glycoproteins in phlebotomine sandflies of various species, sex and age. Med Vet Entomol 2000; 14:251–256 [View Article] [PubMed]
     [Google Scholar]
  178. Titus RG, Ribeiro JMC. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 1988; 239:1306–1308 [View Article]
     [Google Scholar]
  179. Samuelson J, Lerner E, Tesh R, Titus R. A mouse model of Leishmania braziliensis Braziliensis infection produced by coinjection with sand fly saliva. J Exp Med 1991; 173:49–54 [View Article] [PubMed]
     [Google Scholar]
  180. Rohousová I, Volf P. Sand fly saliva: effects on host immune response and Leishmania transmission. Folia Parasitol 2006; 53:161–171 [PubMed]
     [Google Scholar]
  181. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008; 321:970–974 [View Article]
     [Google Scholar]
  182. Pingen M, Schmid MA, Harris E, McKimmie CS. Mosquito biting modulates skin response to virus infection. Trends Parasitol 2017; 33:645–657 [View Article] [PubMed]
     [Google Scholar]
  183. Le Coupanec A, Babin D, Fiette L, Jouvion G, Ave P et al. Aedes mosquito saliva modulates Rift Valley fever virus pathogenicity. PLoS Negl Trop Dis 2013; 7:e2237 [View Article] [PubMed]
     [Google Scholar]
  184. Pingen M, Bryden SR, Pondeville E, Schnettler E, Kohl A et al. Host inflammatory response to mosquito bites enhances the severity of arbovirus infection. Immunity 2016; 44:1455–1469 [View Article]
     [Google Scholar]
  185. Edwards JF, Higgs S, Beaty BJ. Mosquito feeding-induced enhancement of Cache valley virus (Bunyaviridae) infection in mice. J Med Entomol 1998; 35:261–265 [View Article]
     [Google Scholar]
  186. Styer LM, Lim P-Y, Louie KL, Albright RG, Kramer LD et al. Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol 2011; 85:1517–1527 [View Article] [PubMed]
     [Google Scholar]
  187. Hermance ME, Thangamani S. Tick saliva enhances powassan virus transmission to the host, influencing its dissemination and the course of disease. J Virol 2015; 89:7852–7860 [View Article] [PubMed]
     [Google Scholar]
  188. Grazia Cusi M, Gori Savellini G, Terrosi C, Di Genova G, Valassina M et al. Development of a mouse model for the study of Toscana virus pathogenesis. Virology 2005; 333:66–73 [View Article]
     [Google Scholar]
  189. Abdeladhim M, V. Coutinho-Abreu I, Townsend S, Pasos-Pinto S, Sanchez L et al. Molecular diversity between salivary proteins from new world and old world sand flies with emphasis on Bichromomyia olmeca, the sand fly vector of Leishmania mexicana in Mesoamerica. PLoS Negl Trop Dis 2016; 10:e0004771 [View Article]
     [Google Scholar]
  190. Lestinova T, Rohousova I, Sima M, de Oliveira CI, Volf P. Insights into the sand fly saliva: blood-feeding and immune interactions between sand flies, hosts, and Leishmania. PLoS Negl Trop Dis 2017; 11:e0005600 [View Article] [PubMed]
     [Google Scholar]
  191. Abdeladhim M, Kamhawi S, Valenzuela JG. What’s behind a sand fly bite? The profound effect of sand fly saliva on host hemostasis, inflammation and immunity. Infect Genet Evol 2014; 28:691–703 [View Article] [PubMed]
     [Google Scholar]
  192. Soares MBP, Titus RG, Shoemaker CB, David JR, Bozza M. The vasoactive peptide maxadilan from sand fly saliva inhibits TNF-α and induces IL-6 by mouse macrophages through interaction with the Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) Receptor. J Immunol 1998; 160:1811–1816 [View Article]
     [Google Scholar]
  193. Mbow ML, Bleyenberg JA, Hall LR, Titus RG. Phlebotomus papatasi sand fly salivary gland lysate down-regulates a Th1, but up-regulates a Th2, response in mice infected with Leishmania major. J Immunol 1998; 161:5571–5577 [PubMed]
     [Google Scholar]
  194. Teixeira CR, Teixeira MJ, Gomes RBB, Santos CS, Andrade BB et al. Saliva from Lutzomyia longipalpis induces CC chemokine ligand 2/monocyte chemoattractant protein-1 expression and macrophage recruitment. J Immunol 2005; 175:8346–8353 [View Article] [PubMed]
     [Google Scholar]
  195. Costa DJ, Favali C, Clarêncio J, Afonso L, Conceição V et al. Lutzomyia longipalpis salivary gland homogenate impairs cytokine production and costimulatory molecule expression on human monocytes and dendritic cells. Infect Immun 2004; 72:1298–1305 [View Article] [PubMed]
     [Google Scholar]
  196. Carregaro V, Valenzuela JG, Cunha TM, Verri WA Jr, Grespan R et al. Phlebotomine salivas inhibit immune inflammation-induced neutrophil migration via an autocrine DC-derived PGE2/IL-10 sequential pathway. J Leukoc Biol 2008; 84:104–114 [View Article] [PubMed]
     [Google Scholar]
  197. Kay MK, Gibney KB, Riedo FX, Kosoy OL, Lanciotti RS et al. Toscana virus infection in American traveler returning from Sicily, 2009. Emerg Infect Dis 2010; 16:1498–1500 [View Article] [PubMed]
     [Google Scholar]
  198. Farrugia J, Maxwell-Scott H, Brooks T, Tang JW, Pareek M. Toscana virus as a cause of short-term fever and encephalitis in returning travellers from Mediterranean Europe. Clinical Infection in Practice 2020; 6:100018 [View Article]
     [Google Scholar]
  199. Eitrem R, Niklasson B, Weiland O. Sandfly fever among Swedish tourists. Scand J Infect Dis 1991; 23:451–457 [View Article] [PubMed]
     [Google Scholar]
  200. Di Nicuolo G, Pagliano P, Battisti S, Starace M, Mininni V et al. Toscana virus central nervous system infections in southern Italy. J Clin Microbiol 2005; 43:6186–6188 [View Article] [PubMed]
     [Google Scholar]
  201. Venturi G, Madeddu G, Rezza G, Ciccozzi M, Pettinato ML et al. Detection of Toscana virus central nervous system infections in Sardinia Island, Italy. J Clin Virol 2007; 40:90–91 [View Article] [PubMed]
     [Google Scholar]
  202. Venturi G, El-Sawaf G, Arpino C, Madeddu G, Fiorentini C et al. Arboviral infections in Egyptian and Sardinian children and adults with aseptic meningitis and meningo-encephalitis. Scand J Infect Dis 2009; 41:898–899 [View Article] [PubMed]
     [Google Scholar]
  203. Hemmersbach-Miller M, Parola P, Charrel RN, Paul Durand J, Brouqui P. Sandfly fever due to Toscana virus: an emerging infection in southern France. Eur J Intern Med 2004; 15:316–317 [View Article] [PubMed]
     [Google Scholar]
  204. Peyrefitte CN, Devetakov I, Pastorino B, Villeneuve L, Bessaud M et al. Toscana virus and acute meningitis, France. Emerg Infect Dis 2005; 11:778–780 [View Article]
     [Google Scholar]
  205. Cardeñosa N, Kaptoul D, Fernández-Viladrich P, Aranda C, Ory F et al. Toscana virus infection in catalonia (Spain). Vector-Borne Zoonotic Dis 2013; 13:273–275
     [Google Scholar]
  206. Echevarrı́a J-M, de Ory F, Guisasola M-E, Sánchez-Seco M-P, Tenorio A et al. Acute meningitis due to Toscana virus infection among patients from both the Spanish Mediterranean region and the region of Madrid. J Clin Virol 2003; 26:79–84 [View Article]
     [Google Scholar]
  207. Navarro JM, Fernández-Roldán C, Pérez-Ruiz M, Sanbonmatsu S, Rosa M et al. Meningitis by Toscana virus in Spain: description of 17 cases. Med Clin 2004; 122:420–422 [View Article]
     [Google Scholar]
  208. de Ory-Manchón F, Carlos Sanz-Moreno J, Aranguez-Ruiz E, Ramírez-Fernández R. Seroprevalencia edad dependiente frente al virus Toscana en la Comunidad de Madrid: años 1993-1994 y 1999-2000. Enfermedades Infecciosas y Microbiología Clínica 2007; 25:187–189 [View Article]
     [Google Scholar]
  209. Portolani M, Sabbatini AM, Beretti F, Gennari W, Tamassia MG et al. Symptomatic infections by Toscana virus in the Modena province in the Triennium 1999-2001. New Microbiol 2002; 25:485–488
     [Google Scholar]
  210. Francisci D, Papili R, Camanni G, Morosi S, Ferracchiato N et al. Evidence of Toscana virus circulation in Umbria: First report. Eur J Epidemiol 2002; 18:457–459 [View Article]
     [Google Scholar]
  211. Defuentes G, Rapp C, Imbert P, Debord T. Acute meningitis owing to phlebotomus fever Toscana virus imported to France. J Travel Med 2006; 12:295–296 [View Article]
     [Google Scholar]
  212. Epelboin L, Hausfater P, Schuffenecker I, Riou B, Zeller H et al. Meningoencephalitis due to Toscana virus in a French traveler returning from central Italy. J Travel Med 2008; 15:361–363 [View Article]
     [Google Scholar]
  213. Santos L, Simões J, Costa R, Martins S, Lecour H. Toscana virus meningitis in Portugal, 2002-2005. Euro Surveill 2007; 12:3–4
     [Google Scholar]
  214. Venturi G, Marchi A, Fiorentini C, Ramadani N, Quaglio G et al. Prevalence of antibodies to phleboviruses and flaviviruses in Peja, Kosovo. Clin Microbiol Infect 2011; 17:1180–1182 [View Article]
     [Google Scholar]
  215. Hukić M, Salimović-Bešić I. Sandfly – Pappataci fever in Bosnia and Herzegovina: the new-old disease. Bosn J of Basic Med Sci 2009; 9:39–43 [View Article]
     [Google Scholar]
  216. Punda-Polić V, Jerončić A, Mohar B, Kraljevićc KŠ. Prevalence of Toscana virus antibodies in residents of Croatia. Clin Microbiol Infect 2012; 18:E200–E203 [View Article]
     [Google Scholar]
  217. Papa A, Andriotis V, Tzilianos M. Prevalence of Toscana virus antibodies in residents of two Ionian islands, Greece. Travel Med Infect Dis 2010; 8:302–304 [View Article]
     [Google Scholar]
  218. Vocale C, Bartoletti M, Rossini G, Macini P, Pascucci MG et al. Toscana virus infections in northern Italy: laboratory and clinical evaluation. Vector-Borne Zoonot Dis 2012; 12:526–529 [View Article]
     [Google Scholar]
  219. Papa A, Kontana A, Tsergouli K. Phlebovirus infections in Greece. J Med Virol 2015; 87:1072–1076 [View Article]
     [Google Scholar]
  220. Papa A, Mallias J, Tsergouli K, Markou F, Poulou A et al. Neuroinvasive Phlebovirus infection in Greece: a case report. Intervirology 2014; 57:393–395 [View Article]
     [Google Scholar]
  221. Remoli ME, Fiorentini C, Marchi A, Renzi S, Vonesch N et al. Seroprevalence survey of arboviruses in workers from Tuscany, Italy; 2018; 109125–131
  222. Colomba C, Saporito L, Ciufolini MG, Marchi A, Rotolo V et al. Prevalence of Toscana sandfly fever virus antibodies in neurological patients and control subjects in Sicily. New Microbiol 2012; 35:161–165
     [Google Scholar]
  223. Calamusa G, Valenti RM, Vitale F, Mammina C, Romano N et al. Seroprevalence of and risk factors for Toscana and Sicilian virus infection in a sample population of Sicily (Italy). J Infect 2012; 64:212–217 [View Article] [PubMed]
     [Google Scholar]
  224. Pierro A, Landini MP, Gaibani P, Rossini G, Vocale C et al. A model of laboratory surveillance for neuro-arbovirosis applied during 2012 in the Emilia-Romagna region, Italy. Clin Microbiol Infect 2014; 20:672–677 [View Article] [PubMed]
     [Google Scholar]
  225. Anagnostou V, Papa A. Seroprevalence of Toscana virus among residents of Aegean Sea islands, Greece. Travel Med Infect Dis 2013; 11:98–102 [View Article] [PubMed]
     [Google Scholar]
  226. Anagnostou V, Papa A. Prevalence of antibodies to phleboviruses within the sand fly fever Naples virus species in humans, northern Greece. Clin Microbiol Infect 2013; 19:566–570 [View Article] [PubMed]
     [Google Scholar]
  227. Bichaud L, Izri A, de Lamballerie X, Moureau G, Charrel RN. First detection of Toscana virus in Corsica, France. Clin Microbiol Infect 2014; 20:O101–O104 [View Article] [PubMed]
     [Google Scholar]
  228. Amaro F, Zé-Zé L, Luz MT, Alves MJ. Toscana virus: ten years of diagnostics in Portugal. Acta Med Port 2021; 34:677–681 [View Article] [PubMed]
     [Google Scholar]
  229. Martinez JG, García SG, Walter S, Gil-Prieto R, Lacomba DL et al. Seroprevalence against Toscana virus in Spain: the case of the autonomous community of Madrid. J Vector Borne Dis 2022; 59:172–177 [View Article] [PubMed]
     [Google Scholar]
  230. Quattrone F, Mazzetti P, Aquino F, Sani S, Carneglia L et al. Two clusters of Toscana virus meningo-encephalitis in Livorno Province and Elba Island, July-September 2018. Ann di Ig Med Prev e di Comunita 2020; 32:674–681
     [Google Scholar]
  231. Gori Savellini G, Gandolfo C, Cusi MG. Epidemiology of Toscana virus in South Tuscany over the years 2011-2019. J Clin Virol 2020; 128:104452 [View Article]
     [Google Scholar]
  232. Maia C, Ayhan N, Cristóvão JM, Pereira A, Charrel R. Human seroprevalence of Toscana virus and Sicilian phlebovirus in the southwest of Portugal. Eur J Clin Microbiol Infect Dis 2022; 41:137–141 [View Article] [PubMed]
     [Google Scholar]
  233. Masse S, Ayhan N, Capai L, Bosseur F, de Lamballerie X et al. Circulation of Toscana Virus in a Sample Population of Corsica, France. Viruses 2019; 11:817 [View Article]
     [Google Scholar]
  234. Dobler G, Treib J, Haass A, Frösner G, Woesner R et al. Toscana virus infection in German travellers returning from the Mediterranean. Infection 1997; 25:325 [View Article] [PubMed]
     [Google Scholar]
  235. Schwarz TF, Gilch S, Jäger G. Travel-related Toscana virus infection. Lancet 1993; 342:803–804 [View Article] [PubMed]
     [Google Scholar]
  236. Schwarz TF, Jäger G, Gilch S, Pauli C, Eisenhut M et al. Travel-related vector-borne virus infections in Germany. In Imported Virus Infections Vienna: Springer Vienna; pp 57–65 [View Article]
     [Google Scholar]
  237. Beersma MF, Grimbergen YA, Kroon FP, Veldkamp PJ. Meningitis caused by Toscana virus during a summer stay in Italy. Ned Tijdschr Geneeskd 2004; 148:286–288 [PubMed]
     [Google Scholar]
  238. Imirzalioglu C, Schaller M, Bretzel RG. Sandfly fever Naples virus (serotype Toscana) infection with meningeal involvement after a vacation in Italy. Dtsch Med Wochenschr 2006; 131:2838–2840 [View Article] [PubMed]
     [Google Scholar]
  239. Sonderegger B, Hächler H, Dobler G, Frei M. Imported aseptic meningitis due to Toscana virus acquired on the Island of Elba, Italy, August 2008. Eurosurveillance 2009; 14:9–10 [View Article]
     [Google Scholar]
  240. Gabriel M, Resch C, Günther S, Schmidt-Chanasit J. Toscana virus infection imported from Elba into Switzerland. Emerg Infect Dis 2010; 16:1034–1036 [View Article]
     [Google Scholar]
  241. Cordey S, Bel M, Petty TJ, Docquier M, Sacco L et al. Toscana virus meningitis case in Switzerland: an example of the ezVIR bioinformatics pipeline utility for the identification of emerging viruses. Clin Microbiol Infect 2015; 21:387 [View Article]
     [Google Scholar]
  242. Bahri O, Fazaa O, Ben Alaya-Bouafif N, Bouloy M, Triki H et al. Rôle du virus Toscana dans les infections neuroméningées en Tunisie. Pathologie Biologie 2010; 59:2010–2012 [View Article] [PubMed]
     [Google Scholar]
  243. Andayi F, Charrel RN, Kieffer A, Richet H, Pastorino B et al. A sero-epidemiological study of arboviral fevers in Djibouti, Horn of Africa. PLoS Negl Trop Dis 2014; 8:e3299 [View Article] [PubMed]
     [Google Scholar]
  244. Fezaa O, Bahri O, Alaya Bouafif NB, Triki H, Bouattour A. Seroprevalence of Toscana virus infection in Tunisia. Int J Infect Dis 2013; 17:e1172-5 [View Article] [PubMed]
     [Google Scholar]
  245. Sakhria S, Bichaud L, Mensi M, Salez N, Dachraoui K et al. Co-circulation of Toscana virus and punique virus in northern Tunisia: a microneutralisation-based seroprevalence study. PLoS Negl Trop Dis 2013; 7:e2429 [View Article]
     [Google Scholar]
  246. Alkan C, Allal-Ikhlef AB, Alwassouf S, Baklouti A, Piorkowski G et al. Virus isolation, genetic characterization and seroprevalence of Toscana virus in Algeria. Clin Microbiol Infect 2015; 21:1040 [View Article] [PubMed]
     [Google Scholar]
  247. Fezaa O, M’ghirbi Y, Savellini GG, Ammari L, Hogga N et al. Serological and molecular detection of Toscana and other Phleboviruses in patients and sandflies in Tunisia. BMC Infect Dis 2014; 14:598 [View Article] [PubMed]
     [Google Scholar]
  248. Benbetka C, Hachid A, Benallal KE, Khardine FA, Ayhan N et al. Epidemiology, isolation, and genetic characterization of Toscana virus in Algerian patients displaying neurological infection, 2016-2018. IJID Reg 2023; 7:193–198 [View Article] [PubMed]
     [Google Scholar]
  249. Saadawi WK, Abozaid FD, Almukhtar M, Annajar BB, Shaibi T. Seroprevalence study of Toscana virus in Yafran area, Libya. J Vector Borne Dis 2022; 59:186–189 [View Article]
     [Google Scholar]
  250. Ergunay K, Sayiner AA, Litzba N, Lederer S, Charrel R et al. Multicentre evaluation of central nervous system infections due to Flavi and Phleboviruses in Turkey. J Infect 2012; 65:343–349 [View Article] [PubMed]
     [Google Scholar]
  251. Ergunay K, Aydogan S, Ilhami Ozcebe O, Cilek EE, Hacioglu S et al. Toscana virus (TOSV) exposure is confirmed in blood donors from Central, North and South/Southeast Anatolia, Turkey. Zoonoses Public Health 2012; 59:148–154 [View Article] [PubMed]
     [Google Scholar]
  252. Erdem H, Ergunay K, Yilmaz A, Naz H, Akata F et al. Emergence and co-infections of West Nile virus and Toscana virus in Eastern Thrace, Turkey. Clin Microbiol Infect 2014; 20:319–325 [View Article] [PubMed]
     [Google Scholar]
  253. Tezcan S, Di̇nçer E, Ülger M, Özgür D, Erdoğan S et al. Serological investigation of phlebovirus exposure in blood donors from the Mediterranean Province of Mersin, Turkey. Mikrobiyol Bul 2015; 49:403–413 [View Article]
     [Google Scholar]
  254. Shiraly R, Khosravi A, Farahangiz S. Seroprevalence of sandfly fever virus infection in military personnel on the western border of Iran. J Infect Public Health 2017; 10:59–63 [View Article] [PubMed]
     [Google Scholar]
  255. Kuşçu F, Menemenlioğlu D, Öztürk DB, Korukluoğlu G, Uyar Y. Anti-HIV Pozitif Bir Hastada Saptanan Akut Toskana Virus Enfeksiyonu. Mikrobiyol Bul 2014; 48:168–173 [View Article]
     [Google Scholar]
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Toscana virus – an emerging Mediterranean arbovirus transmitted by sand flies
J. Gen. Virol. 105, 002045 (2024); https://doi.org/10.1099/jgv.0.002045
/content/journal/jgv/10.1099/jgv.0.002045
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