Abstract
Phleboviruses are common human pathogens diffused on the Mediterranean area whose infection can cause the typical prodromal symptom of a mild three‑days fever. In particular, Toscana Virus (TOSV) has a great concern since its capacity to provoke central nervous system disorders like meningoencephalitis. Furthermore, as the phlebotomine arthropod vectors represent the main carrier for pathogens of the genus Leishmania as well, the purpose of the study was to investigate the presence of TOSV in Lampedusa, Italy previously reported for leishmaniosis infection cases. The survey was carried out through an initial sampling phase of sand flies, by means of CDC light traps, and a second step of molecular analyses. The genomic S‑segment of TOSV was targeted. The positive samples were sequenced and compared with those available in GenBank™ using Basic Local Alignments Tool (BLAST) analyses. The study revealed for the first time the presence of TOSV in Lampedusa, Italy. The entomological studies directed on vectors are currently widely used in sand fly surveillance, and new data on TOSV are of public health concern.
References
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Peyrefitte C.N., Grandadam M., Bessaud M., Andry P.-E., Fouque F., Caro V., et al. 2013. Diversity of Phlebotomus perniciosus in Provence, southeastern France: Detection of two putative new phlebovirus sequences. Vector Borne Zoonotic Dis, 13, 630–636.
Remoli M.E., Bongiorno G., Fortuna C., Marchi A., Bianchi R., Khoury C., et al. 2015. Experimental evaluation of sand fly collection and storage methods for the isolation and molecular detection of Phlebotomus-borne viruses. Parasites & Vectors, 8, 576.
Remoli M.E., Fortuna C., Marchi A., Bucci P., Argentini C., Bongiorno G., et al. 2014. Viral isolates of a novel putative phlebovirus in the Marche Region of Italy. Am J Trop Med Hyg, 90, 760–763.
Remoli M.E., Jiménez M., Fortuna C., Benedetti E., Marchi A., Genovese D., et al. 2016. Phleboviruses detection in Phlebotomus perniciosus from a human leishmaniasis focus in South-West Madrid region, Spain. Parasites & Vectors, 9, 205.
Valassina M., Cusi M.G. & Valensin P.E. 2003. A Mediterranean Arbovirus: The Toscana Virus. Journal of Neurovirology, 9, 577–583.
Valassina M., Cusi M.G. & Valensin P.E. 1996. Rapid identification of Toscana virus by nested PCR during an outbreak in the Siena area of Italy. J Clin Microbiol, 34, 2500–2502.
Wuerth J.D. & Weber F. 2016. Phleboviruses and the Type I Interferon Response. Viruses, 8, 174.
Zhioua E., Moureau G., Chelbi I., Ninove L., Bichaud L., Derbali M., et al. 2010. Punique virus, a novel phlebovirus, related to sandfly fever Naples virus, isolated from sandflies collected in Tunisia. J Gen Virol, 91, 1275–1283.
Alkan C., Bichaud L., de Lamballerie X., Alten B., Gould E.A. & Charrel R.N. 2013. Sandfly-borne phleboviruses of Eurasia and Africa: epidemiology, genetic diversity, geographic range, control measures. Antiviral Res, 100, 54–74.
Alvar J., Vélez I.D., Bern C., Herrero M., Desjeux P., Cano J., et al. 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS One, 7, e35671.
Amaro F., Zé-Zé L., Alves M.J., Börstler J., Clos J., Lorenzen S., et al. 2015. Co-circulation of a novel phlebovirus and Massilia virus in sandflies, Portugal. Virology Journal, 12, 174.
Ayhan N., Baklouti A., Prudhomme J., Walder G., Amaro F., Alten B., et al. 2017. Practical Guidelines for Studies on Sandfly-Borne Phleboviruses: Part I: Important Points to Consider Ante Field Work. Vector Borne Zoonotic Dis, 17, 73–80.
Baggieri M., Marchi A., Bucci P., Nicoletti L. & Magurano F. 2015. Genetic variability of the S segment of Toscana virus. Virus Res, 200, 35–44.
Baklouti A., Leparc Goffard I., Piorkowski G., Coutard B., Papageorgiou N., De Lamballerie X., et al. 2016. Complete Coding Sequences of Three Toscana Virus Strains Isolated from Sandflies in France. Genome Announc, 4, e01676-15.
Benallal K.E., Garni R., Harrat Z., Volf P. & Dvorak V. 2022. Phlebotomine sand flies (Diptera: Psychodidae) of the Maghreb region: A systematic review of distribution, morphology, and role in the transmission of the pathogens. PLOS Neglected Tropical Diseases, 16, e0009952.
Calamusa G., Valenti R.M., Vitale F., Mammina C., Romano N., Goedert J.J., et al. 2012. Seroprevalence of and risk factors for Toscana and Sicilian virus infection in a sample population of Sicily (Italy). J Infect, 64, 212–217.
Calzolari M., Romeo G., Bergamini F., Dottori M., Rugna G. & Carra E. 2022. Host preference and Leishmania infantum natural infection of the sand fly Phlebotomus perfiliewi in northern Italy. Acta Tropica, 226, 106246.
Calzolari M., Romeo G., Callegari E., Bonilauri P., Chiapponi C., Carra E., et al. 2021. Co-Circulation of Phleboviruses and Leishmania Parasites in Sand Flies from a Single Site in Italy Monitored between 2017 and 2020. Viruses, 13, 1660.
Charrel R.N., Izri A., Temmam S., Delaunay P., Toga I., Dumon H., et al. 2007. Cocirculation of 2 Genotypes of Toscana Virus, Southeastern France. Emerg Infect Dis, 13, 465–468.
Charrel R.N., Moureau G., Temmam S., Izri A., Marty P., Parola P., et al. 2009. Massilia Virus, A Novel Phlebovirus (Bunyaviridae) Isolated from Sandflies in the Mediterranean. Vector Borne Zoonotic Dis, 9, 519–530.
Dincer E., Gargari S., Ozkul A. & Ergunay K. 2015. Potential animal reservoirs of Toscana virus and coinfections with Leishmania infantum in Turkey. Am J Trop Med Hyg, 92, 690–697.
Ergunay K., Kasap O.E., Orsten S., Oter K., Gunay F., Yoldar A.Z.A., et al. 2014. Phlebovirus and Leishmania detection in sandflies from eastern Thrace and northern Cyprus. Parasites & Vectors, 7, 575.
Es-Sette N., Ajaoud M., Bichaud L., Hamdi S., Mellouki F., Charrel R.N., et al. 2014. Phlebotomus sergenti a common vector of Leishmania tropica and Toscana virus in Morocco. J Vector Borne Dis, 51, 86–90.
Fares W., Dachraoui K., Barhoumi W., Cherni S., Chelbi I. & Zhioua E. 2020. Co-circulation of Toscana virus and Leishmania infantum in a focus of zoonotic visceral leishmaniasis from Central Tunisia. Acta Tropica, 204, 105342.
Foglia Manzillo V., Gizzarelli M., Vitale F., Montagnaro S., Torina A., Sotera S., et al. 2018. Serological and entomological survey of canine leishmaniasis in Lampedusa island, Italy. BMC Veterinary Research, 14, 286.
Maia C., Alwassouf S., Cristóvão J.M., Ayhan N., Pereira A., Charrel R.N., et al. 2017. Serological association between Leishmania infantum and sand fly fever Sicilian (but not Toscana) virus in sheltered dogs from southern Portugal. Parasites Vectors, 10, 92.
Mammina C., Calamusa G., Vitale F., Amodio E., Romano N., Valenti R.M., et al. 2012. Seroprevalence of and risk factors for Toscana and Sicilian virus infection in a sample population of Sicily (Italy). The Journal of infection, 64, 212–217.
Marchi S., Trombetta C.M., 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. Journal of Infection and Public Health, 10, 866–869.
Maroli M., Feliciangeli M.D., Bichaud L., Charrel R.N. & Gradoni L. 2013. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol, 27, 123–147.
Moriconi M., Rugna G., Calzolari M., Bellini R., Albieri A., Angelini P., et al. 2017. Phlebotomine sand fly–borne pathogens in the Mediterranean Basin: Human leishmaniasis and phlebovirus infections. PLoS Negl Trop Dis, 11, e0005660.
Peyrefitte C.N., Grandadam M., Bessaud M., Andry P.-E., Fouque F., Caro V., et al. 2013. Diversity of Phlebotomus perniciosus in Provence, southeastern France: Detection of two putative new phlebovirus sequences. Vector Borne Zoonotic Dis, 13, 630–636.
Remoli M.E., Bongiorno G., Fortuna C., Marchi A., Bianchi R., Khoury C., et al. 2015. Experimental evaluation of sand fly collection and storage methods for the isolation and molecular detection of Phlebotomus-borne viruses. Parasites & Vectors, 8, 576.
Remoli M.E., Fortuna C., Marchi A., Bucci P., Argentini C., Bongiorno G., et al. 2014. Viral isolates of a novel putative phlebovirus in the Marche Region of Italy. Am J Trop Med Hyg, 90, 760–763.
Remoli M.E., Jiménez M., Fortuna C., Benedetti E., Marchi A., Genovese D., et al. 2016. Phleboviruses detection in Phlebotomus perniciosus from a human leishmaniasis focus in South-West Madrid region, Spain. Parasites & Vectors, 9, 205.
Valassina M., Cusi M.G. & Valensin P.E. 2003. A Mediterranean Arbovirus: The Toscana Virus. Journal of Neurovirology, 9, 577–583.
Valassina M., Cusi M.G. & Valensin P.E. 1996. Rapid identification of Toscana virus by nested PCR during an outbreak in the Siena area of Italy. J Clin Microbiol, 34, 2500–2502.
Wuerth J.D. & Weber F. 2016. Phleboviruses and the Type I Interferon Response. Viruses, 8, 174.
Zhioua E., Moureau G., Chelbi I., Ninove L., Bichaud L., Derbali M., et al. 2010. Punique virus, a novel phlebovirus, related to sandfly fever Naples virus, isolated from sandflies collected in Tunisia. J Gen Virol, 91, 1275–1283.