Antibodies against Phlebotomus perniciosus sandfly salivary gland homogenate (SGH) and recombinant protein rSP03B, sandfly-borne Toscana virus (TOSV), Sandfly Fever Sicilian virus (SFSV) and Leishmania, as well as DNA of the latter parasite, were investigated in 670 blood samples from 575 human donors in Murcia Region, southeast Spain, in 2017 and 2018. The estimated SGH and rSP03B seroprevalences were 69% and 88%, respectively, although correlation between test results was relatively low (ρ = 0.39). Similarly, TOSV, SFSV and Leishmania seroprevalences were 26%, 0% and 1%, respectively, and Leishmania PCR prevalence was 2%. Prevalences were significantly greater in 2017, overdispersed and not spatially related to each other although both were positively associated with SGH but not to rSP03B antibody optical densities, questioning the value of the latter as a diagnostic marker for these infections in humans.

Departamento de Sanidad Animal Facultad de Veterinaria Campus de Excelencia Internacional Regional 'Campus Mare Nostrum' Universidad de Murcia Murcia Spain

Department of Parasitology Faculty of Science Charles University Prague Czech Republic

Grupo de Erosión y Conservación de Suelos Centro de Edafología y Biología Aplicada del Segura Consejo Superior de Investigaciones Científicas Murcia Spain

Servicio de Microbiología Hospital Universitario 'Virgen de la Arrixaca' Murcia Spain

Unite des Virus Emergents Aix Marseille Université IRD 190 Inserm 1207 IHU Mediterranée Infection Marseille France

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Acedo Sánchez, C. , Martín Sánchez, J. , Vélez Bernal, I. D. , Sanchís Marín, M. C. , Louassini, M. , Maldonado, J. A. , & Morillas Márquez, F. (1996). Leishmaniasis eco‐epidemiology in the Alpujarra region (Granada Province, southern Spain). International Journal for Parasitology, 26(3), 303–310. 10.1016/0020-7519(95)00124-7 PubMed DOI

Aliaga, L. , Ceballos, J. , Sampedro, A. , Cobo, F. , López‐Nevot, M. Á. , Merino‐Espinosa, G. , Morillas‐Márquez, F. , & Martín‐Sánchez, J. (2019). Asymptomatic Leishmania infection in blood donors from the Southern of Spain. Infection, 47(5), 739–747. 10.1007/s15010-019-01297-3 PubMed DOI

Alkan, C. , Allal‐Ikhlef, A. B. , Alwassouf, S. , Baklouti, A. , Piorkowski, G. , de Lamballerie, X. , Izri, A. , & Charrel, R. N. (2015). Virus isolation, genetic characterization and seroprevalence of Toscana virus in Algeria. Clinical Microbiology and Infection, 21(11), 1040. e1–9. 10.1016/j.cmi.2015.07.012 PubMed DOI

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 Research, 100(1), 54–74. 10.1016/j.antiviral.2013.07.005 PubMed DOI

Alten, B. , Maia, C. , Afonso, M. O. , Campino, L. , Jiménez, M. , & González, E. (2016). Seasonal dynamics of phlebotomine sand fly species proven vectors of Mediterranean leishmaniasis caused by Leishmania infantum . PLoS Neglected Tropical Diseases, 10(2), e0004458. 10.1371/journal.pntd.0004458 PubMed DOI PMC

Amaro, F. , Luz, T. , Parreira, P. , Ciufolini, M. G. , Marchi, A. , Janeiro, N. , Zagalo, A. , Proença, P. , Ramos, M. I. , & Alves, M. J. (2011). Vírus Toscana na população Portuguesa: Vigilância sero‐epidemiológica e casos clínicos [Toscana virus in the Portuguese population: Serosurvey and clinical cases.]. Acta Medica Portuguesa, 24(Suppl. 2), 503–508. PubMed

Amodio, E. , Valentini, M. , Gori‐Savellini, G. , Valenti, R. M. , Romano, N. , Goedert, J. J. , & Cusi, M. G. (2011). Prevalence of Toscana and Sicilian phlebovirus antibodies in classic Kaposi sarcoma case patients and control subjects in Sicily. The Journal of Infectious Diseases, 204(9), 1423–1426. 10.1093/infdis/jir546 PubMed DOI PMC

Ayhan, N. , & Charrel, R. N. (2020). An update on Toscana virus distribution, genetics, medical and diagnostic aspects. Clinical Microbiology and Infection, 26(8), 1017–1023. 10.1016/j.cmi.2019.12.015 PubMed DOI

Baneth, G. , Koutinas, A. F. , Solano‐Gallego, L. , Bourdeau, P. , & Ferrer, L. (2008). Canine leishmaniosis—New concepts and insights on an expanding zoonosis: Part one. Trends in Parasitology, 24(7), 324–330. 10.1016/j.pt.2008.04.001 PubMed DOI

Barral, A. , Honda, E. , Caldas, A. , Costa, J. , Vinhas, V. , Rowton, E. D. , Valenzuela, J. G. , Charlab, R. , Barral‐Netto, M. , & Ribeiro, J. M. (2000). Human immune response to sand fly salivary gland antigens: A useful epidemiological marker? The American Journal of Tropical Medicine and Hygiene, 62(6), 740–745. 10.4269/AJTMH.2000.62.740 PubMed DOI

Bichaud, L. , Piarroux, R. P. , Izri, A. , Ninove, L. , Mary, C. , de Lamballerie, X. , & Charrel, R. N. (2011a). Low seroprevalence of sandfly fever Sicilian virus antibodies in humans, Marseille, France. Clinical Microbiology and Infection, 17(8), 1189–1190. 10.1111/j.1469-0691.2011.03509.x PubMed DOI

Bichaud, L. , Souris, M. , Mary, C. , Ninove, L. , Thirion, L. , Piarroux, R. P. , Piarroux, R. , De Lamballerie, X. , & Charrel, R. N. (2011b). Epidemiologic relationship between Toscana virus infection and Leishmania infantum due to common exposure to Phlebotomus perniciosus sandfly vector. PLoS Neglected Tropical Diseases, 5(9), e1328. 10.1371/journal.pntd.0001328 PubMed DOI PMC

Bravo‐Barriga, D. , Parreira, R. , Maia, C. , Afonso, M. O. , Blanco‐Ciudad, J. , Serrano, F. J. , Pérez‐Martín, J. E. , Gómez‐Gordo, L. , Campino, L. , Reina, D. , & Frontera, E. (2016). Detection of Leishmania DNA and blood meal sources in phlebotomine sand flies (Diptera: Psychodidae) in western of Spain: Update on distribution and risk factors associated. Acta Tropica, 164, 414–424. 10.1016/j.actatropica.2016.10.003 PubMed DOI

Buezo Montero, S. , Gabrieli, P. , Montarsi, F. , Borean, A. , Capelli, S. , De Silvestro, G. , Forneris, F. , Pombi, M. , Breda, A. , Capelli, G. , & Arcà, B. (2020). IgG Antibody responses to the Aedes albopictus 34k2 salivary protein as novel candidate marker of human exposure to the tiger mosquito. Frontiers in Cellular and Infection Microbiology, 10, 377. 10.3389/fcimb.2020.00377 PubMed DOI PMC

Calamusa, G. , Valenti, R. M. , Vitale, F. , Mammina, C. , Romano, N. , Goedert, J. J. , Gori‐Savellini, G. , Cusi, M. G. , & Amodio, E. (2012). Seroprevalence of and risk factors for Toscana and Sicilian virus infection in a sample population of Sicily (Italy). Journal of Infection, 64(2), 212–217. 10.1016/j.jinf.2011.11.012 PubMed DOI PMC

Cardeñosa, N. , Kaptoul, D. , Fernández‐Viladrich, P. , Aranda, C. , De Ory, F. , Niubó, J. , Plans, P. , Domínguez, A. , Fedele, G. , Tenorio, A. , & Sánchez‐Seco, M. P. (2013). Toscana virus infection in Catalonia (Spain). Vector‐Borne and Zoonotic Diseases, 13(4), 273–275. 10.1089/vbz.2011.0903 PubMed DOI

Charrel, R. N. , & de Lamballerie, X. (2013). Viral febrile illnesses: Sandfly fever. In Magill A. J., Hill D. R., Solomon T., & Ryan E. T. (Eds.), Hunter's tropical medicine and emerging infectious disease (9th edn., pp. 320–321). Elsevier Inc. 10.1016/B978-1-4160-4390-4.00184-3 DOI

Chitimia, L. , Muñoz‐García, C. I. , Sánchez‐Velasco, D. , Lizana, V. , del Río, L. , Murcia, L. , Fisa, R. , Riera, C. , Giménez‐Font, P. , Jiménez‐Montalbán, P. , Martínez‐Ramírez, Á. , Meseguer‐Meseguer, J. M. , García‐Bacete, I. , Sánchez‐Isarria, M. A. , Sanchis‐Monsonís, G. , García‐Martínez, J. D. , Vicente, V. , Segovia, M. , & Berriatua, E. (2011). Cryptic Leishmaniosis by Leishmania infantum, a feature of canines only? A study of natural infection in wild rabbits, humans and dogs in southeastern Spain. Veterinary Parasitology, 181(1), 12–16. 10.1016/j.vetpar.2011.04.016 PubMed DOI

Cusi, M. G. , Gandolfo, C. , Valentini, M. , & Savellini, G. G. (2013). Seroprevalence of antibodies to sandfly fever Sicilian virus in a sample population in Tuscany, Italy. Vector Borne and Zoonotic Diseases, 13(5), 345–346. 10.1089/vbz.2011.0945 PubMed DOI

Dantas‐Torres, F. , da Silva Sales, K. G. , Gomes da Silva, L. , Otranto, D. , & Figueredo, L. A. (2017). Leishmania‐FAST15: A rapid, sensitive and low‐cost real‐time PCR assay for the detection of Leishmania infantum and Leishmania braziliensis kinetoplast DNA in canine blood samples. Molecular and Cellular Probes, 31, 65–69. 10.1016/j.mcp.2016.08.006 PubMed DOI

De Ory‐Manchón, F. , Sanz‐Moreno, J. C. , Aranguez‐Ruiz, E. , & Ramírez‐Fernández, R. (2007). Seroprevalencia edad dependiente frente al virus Toscana en la Comunidad de Madrid: Años 1993–1994 y 1999–2000. Enfermedades Infecciosas y Microbiologia Clinica, 25(3), 187–189. 10.1157/13099371 PubMed DOI

De Ory, F. , Gegúndez, M. I. , Fedele, C. G. , & Sánchez‐Seco, M. P. (2009). Virus Toscana, West Nile y de la coriomeningitis linfocitaria como causantes de meningitis aséptica en España. Medicina Clinica, 132(15), 587–590. 10.1016/j.medcli.2008.10.057 PubMed DOI

Dehghani, R. , Kassiri, H. , Khodkar, I. , Karami, S. (2021). A comprehensive overview on sandfly fever. Journal of Acute Disease, 10(3), 98–106. 10.4103/2221-6189.316673 DOI

Díaz‐Sáez, V. , Corpas‐López, V. , Merino‐Espinosa, G. , Morillas‐Mancilla, M. J. , Abattouy, N. , & Martín‐Sánchez, J. (2021). Seasonal dynamics of phlebotomine sand flies and autochthonous transmission of Leishmania infantum in high‐altitude ecosystems in southern Spain. Acta Tropica, 213, 105749. 10.1016/j.actatropica.2020.105749 PubMed DOI

Díaz‐Sáez, V. , Morillas‐Márquez, F. , Merino‐Espinosa, G. , Corpas‐López, V. , Morales‐Yuste, M. , Pesson, B. , Barón‐López, S. , Lucientes‐Curdi, J. , & Martín‐Sánchez, J. (2018). Phlebotomus langeroni Nitzulescu (Diptera, Psychodidae) a new vector for Leishmania infantum in Europe. Parasitology Research, 117(4), 1105–1113. 10.1007/s00436-018-5788-8 PubMed DOI

Servicio de Epid (2018). Boletín Epidemiológico de la Comunidad de Madrid, 24(11), 17. Available from: http://www.madrid.org/bvirtual/BVCM020343.pdf

Drahota, J. , Martin‐Martin, I. , Sumova, P. , Rohoušová, I. , Jimenez, M. , Molina, R. , & Volf, P. (2014). Recombinant antigens from Phlebotomus perniciosus saliva as markers of canine exposure to visceral leishmaniases vector. PLoS Neglected Tropical Diseases, 8(1), 45. 10.1371/journal.pntd.0002597 PubMed DOI PMC

ECDC (European Centre for Disease Prevention and Control) (2020). Phlebotomine sand flies—Factsheet for experts. Retrieved from: https://www.ecdc.europa.eu/en/disease‐vectors/facts/phlebotomine‐sand‐flies

Echevarría, J. M. , De Ory, F. , Guisasola, M. E. , Sánchez‐Seco, M. P. , Tenorio, A. , Lozano, Á. , Córdoba, J. , & Gobernado, M. (2003). Acute meningitis due to Toscana virus infection among patients from both the Spanish Mediterranean region and the region of Madrid. Journal of Clinical Virology, 26(1), 79–84. 10.1016/S1386-6532(02)00041-0 PubMed DOI

Eitrem, R. , Stylianou, M. , & Niklasson, B. (1991). High prevalence rates of antibody to three sandfly fever viruses (Sicilian, Naples and Toscana) among Cypriots. Epidemiology and Infection, 107(3), 685–691. 10.1017/S0950268800049384 PubMed DOI PMC

Francino, O. , Altet, L. , Sánchez‐Robert, E. , Rodriguez, A. , Solano‐Gallego, L. , Alberola, J. , Ferrer, L. , Sánchez, A. , & Roura, X. (2006). Advantages of real‐time PCR assay for diagnosis and monitoring of canine leishmaniosis. Veterinary Parasitology, 137(3–4), 214–221. 10.1016/j.vetpar.2006.01.011 PubMed DOI

González, E. , Jiménez, M. , Hernández, S. , Martín‐Martín, I. , & Molina, R. (2017). Phlebotomine sand fly survey in the focus of leishmaniasis in Madrid, Spain (2012‐2014): Seasonal dynamics, Leishmania infantum infection rates and blood meal preferences. Parasites & Vectors, 10(1), 368. 10.1186/s13071-017-2309-z PubMed DOI PMC

Izri, A. , Temmam, S. , Moureau, G. , Hamrioui, B. , de Lamballerie, X. , & Charrel, R. N. (2008). Sandfly fever Sicilian virus, Algeria. Emerging Infectious Diseases, 14(5), 795–797. 10.3201/eid1405.071487 PubMed DOI PMC

Jiménez, M. , González, E. , Iriso, A. , Marco, E. , Alegret, A. , Fúster, F. , & Molina, R. (2013). Detection of Leishmania infantum and identification of blood meals in Phlebotomus perniciosus from a focus of human leishmaniasis in Madrid, Spain. Parasitology Research, 112(7), 2453–2459. 10.1007/s00436-013-3406-3 PubMed DOI

Kirkwood, B. , & Sterne, J. (2003). Essential medical statistics. Wiley‐Blackwell.

Kostalova, T. , Lestinova, T. , Maia, C. , Sumova, P. , Vlkova, M. , Willen, L. , Polanska, N. , Fiorentino, E. , Scalone, A. , Oliva, G. , Veronesi, F. , Cristóvão, J. , Courtenay, O. , Campino, L. , Gradoni, L. , Gramiccia, M. , & Volf, P. (2017). The recombinant protein rSP03B is a valid antigen for screening dog exposure to Phlebotomus perniciosus across foci of canine leishmaniasis. Medical and Veterinary Entomology, 31(1), 88–93. 10.1111/MVE.12192 PubMed DOI

Kostalova, T. , Lestinova, T. , Sumova, P. , Vlkova, M. , Rohoušová, I. , Berriatua, E. , Oliva, G. , Fiorentino, E. , Scalone, A. , Gramiccia, M. , Gradoni, L. , & Volf, P. (2015). Canine Antibodies against salivary recombinant proteins of Phlebotomus perniciosus: A longitudinal study in an endemic focus of canine leishmaniasis. PLoS Neglected Tropical Diseases, 9(6), e0003855. 10.1371/journal.pntd.0003855 PubMed DOI PMC

Lestinova, T. , Rohoušová, I. , Sima, M. , de Oliveira, C. I. , & Volf, P. (2017). Insights into the sand fly saliva: Blood‐feeding and immune interactions between sand flies, hosts, and Leishmania. PLoS Neglected Tropical Diseases, 11(7), e0005600. 10.1371/journal.pntd.0005600 PubMed DOI PMC

Lucientes, J. , Blasco‐Zumeta, J. , Zárate, J. J. , Arbea, J. I. , & Latorre, E. (2001). Primeros registros de insectos del genero Phlebotomus (Diptera: Psychodidae) para Los Monegros (Zaragoza, España). Boletin de la SEA, 28, 123–124.

Lucientes, J. , Castillo, J. A. , Gracia, M. J. , & Peribáñez, M. A. (2005). Flebotomos, de la biología al control. Revista Electrónica de Veterinaria REDVET, 6(8), 1–8. https://www.redalyc.org/articulo.oa?id=63612822003

Maia, C. , Ayhan, N. , Cristóvão, J. M. , Pereira, A. , & Charrel, R. (2021). Human seroprevalence of Toscana virus and Sicilian phlebovirus in the southwest of Portugal. European Journal of Clinical Microbiology & Infectious Diseases. Advance online publication. 10.1007/s10096-021-04332-0 PubMed DOI

Martín‐Martín, I. , Molina, R. , & Jiménez, M. (2015). Kinetics of anti‐Phlebotomus perniciosus saliva antibodies in experimentally bitten mice and rabbits. PLoS One, 10(11), e0140722. 10.1371/journal.pone.0140722 PubMed DOI PMC

Martín‐Martín, I. , Molina, R. , Rohoušová, I. , Drahota, J. , Volf, P. , & Jiménez, M. (2014). High levels of anti‐Phlebotomus perniciosus saliva antibodies in different vertebrate hosts from the re‐emerging leishmaniosis focus in Madrid, Spain. Veterinary Parasitology, 202(3–4), 207–216. 10.1016/J.VETPAR.2014.02.045 PubMed DOI

Martín‐Martín, I. , Molina, R. , & Jiménez, M. (2012). An insight into the Phlebotomus perniciosus saliva by a proteomic approach. Acta Tropica, 123(1), 22–30. 10.1016/j.actatropica.2012.03.003 PubMed DOI

Martín‐Sánchez, J. , Gramiccia, M. , Pesson, B. , & Morillas‐Márquez, F. (2000). Genetic polymorphism in sympatric species of the genus Phlebotomus, with special reference to Phlebotomus perniciosus and Phlebotomus longicuspis (Diptera, Phlebotomidae). Parasite, 7(4), 247–254. 10.1051/parasite/2000074247 PubMed DOI

Martinez, J. , Showering, A. , Oke, C. , Jones, R. T. , & Logan, J. G. (2021). Differential attraction in mosquito‐human interactions and implications for disease control. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 376(1818), 20190811. 10.1098/rstb.2019.0811 PubMed DOI PMC

Martínez‐García, F. A. , Moreno‐Docón, A. , López‐López, M. , Albert‐Lacal, L. , Martínez‐Toldos, M. C. , Segovia‐Hernández, M. , & Fernández‐Barreiro, A. (2007). A case of meningitis due to Toscana virus in Murcia. Revista de Neurologia, 45(5), 317–318. 10.33588/RN.4505.2007324 PubMed DOI

Martínez Ortega, E. , & Conesa Gallego, E. (1987). Fenología de los flebotomos del subgénero Larroussius (Dip. Psychodidae, Phlebotomus) en el sureste de la Península Ibérica. Boletín de la Asociación Española de Entomología, 11, 293–300.

Martínez Ortega, E. , Conesa Gállego, E. , Romera Lozano, H. (1996). Phlebotomus (Larroussius) langeroni Nitzulescu, 1930 (Diptera: Psychodidae), espèce nouvelle pour l'Espagne. Parasite, 3, 77–80.

Marzouki, S. , Kammoun‐Rebai, W. , Bettaieb, J. , Abdeladhim, M. , Hadj Kacem, S. , Abdelkader, R. , Gritli, S. , Chemkhi, J. , Aslan, H. , Kamhawi, S. , Ben Salah, A. , Louzir, H. , Valenzuela, J. G. , & Ben Ahmed, M. (2015). Validation of recombinant salivary protein PpSP32 as a suitable marker of human exposure to Phlebotomus papatasi, the vector of Leishmania major in Tunisia. PLoS Neglected Tropical Diseases, 9(9), e0003991. 10.1371/journal.pntd.0003991 PubMed DOI PMC

Masse, S. , Ayhan, N. , Capai, L. , Bosseur, F. , de Lamballerie, X. , Charrel, R. , Falchi, A. (2019). Circulation of Toscana virus in a sample population of Corsica, France. Viruses, 11(9), 817. 10.3390/v11090817 PubMed DOI PMC

Mendoza‐Montero, J. , Gámez‐Rueda, M.‐I. , Navarro‐Marí, J.‐M. , de la Rosa‐Fraile, M. , & Oyonarte‐Gómez, S. (1998). Infections due to sandfly fever virus serotype Toscana in Spain. Clinical Infectious Diseases, 27(3), 434–436. 10.1086/514684 PubMed DOI

Morillas, F. , Sanchez Rabasco, F. , Ocaña, J. , Martin‐Sanchez, J. , Ocaña‐Wihelmi, J. , Acedo, C. , & Sanchiz‐Marin, M. C. (1996). Leishmaniosis in the focus of the Axarquía region, Malaga province, southern Spain: A survey of the human, dog, and vector. Parasitology Research, 82(6), 569–570. 10.1007/s004360050164 PubMed DOI

Muñoz, C. , Ayhan, N. , Ortuño, M. , Ortiz, J. , Gould, E. A. , Maia, C. , Berriatua, E. , & Charrel, R. N. (2020). Experimental infection of dogs with Toscana Virus and Sandfly Fever sicilian Virus to determine their potential as possible vertebrate hosts. Microorganisms, 8(4), 596. 10.3390/MICROORGANISMS8040596 PubMed DOI PMC

Muñoz, C. , Martínez‐de la Puente, J. , Figuerola, J. , Pérez‐Cutillas, P. , Navarro, R. , Ortuño, M. , Bernal, L. J. , Ortiz, J. , Soriguer, R. , & Berriatua, E. (2019). Molecular xenomonitoring and host identification of Leishmania sand fly vectors in a Mediterranean periurban wildlife park. Transboundary and Emerging Diseases, 66(6), 2546–2561. 10.1111/tbed.13319 PubMed DOI

Muñoz, C. , Risueño, J. , Pérez‐Cutillas, P. , Bernal, L. J. , Ortiz, J. M. , Ruiz de Ybáñez, R. , Sánchez‐López, P. F. , Martínez‐Carrasco, C. , Del Río, L. , De la Rúa, P. , García‐Martínez, J. D. , Gonzálvez, M. , Murcia, L. , Collantes, F. , Goyena, E. , Spitzova, T. , Elshanat, S. , & Berriatua, E. (2021). Density assessment and reporting for Phlebotomus perniciosus and other sand fly species in periurban residential estates in Spain. Parasitology Research, 120, 3091–3103. 10.1007/s00436-021-07270-0 PubMed DOI PMC

Muñoz, C. , Risueño, J. , Yilmaz, A. , Pérez‐Cutillas, P. , Goyena, E. , Ortuño, M. , Bernal, L. J. , Ortiz, J. , Alten, B. , & Berriatua, E. (2018). Investigations of Phlebotomus perniciosus sand flies in rural Spain reveal strongly aggregated and gender‐specific spatial distributions and advocate use of light‐attraction traps. Medical and Veterinary Entomology, 32(2), 186–196. 10.1111/mve.12275 PubMed DOI

Navarro‐Marí, J. M. , Gómez‐Camarasa, C. , Pérez‐Ruiz, M. , Sanbonmatsu‐Gámez, S. , Pedrosa‐Corral, I. , & Jiménez‐Valera, M. (2013). Clinic–epidemiologic study of human infection by Granada Virus, a New Phlebovirus within the sandfly fever Naples serocomplex. The American Journal of Tropical Medicine and Hygiene, 88(5), 1006. 10.4269/AJTMH.12-0732 PubMed DOI PMC

Pereira, A. , Cristóvão, J. M. , Vilhena, H. , Martins, Â. , Cachola, P. , Henriques, J. , Coimbra, M. , Catarino, A. , Lestinova, T. , Spitzova, T. , Volf, P. , Campino, L. , & Maia, C. (2019). Antibody response to Phlebotomus perniciosus saliva in cats naturally exposed to phlebotomine sand flies is positively associated with Leishmania infection. Parasites and Vectors, 12(1), 128. 10.1186/s13071-019-3376-0 PubMed DOI PMC

Pérez‐Cutillas, P. , Goyena, E. , Chitimia, L. , Rúa, P. , Bernal, L. J. , & Fisa, R. (2015). Spatial distribution of human asymptomatic Leishmania infantum infection in southeast Spain: A study of environmental, demographic and social risk factors. Acta Tropica, 146, 127–134. 10.1016/j.actatropica.2015.03.017 PubMed DOI

Pesson, B. , Ready, J. S. , Benabdennbi, I. , Martín‐Sánchez, J. , Esseghir, S. , Cadi‐Soussi, M. , Morillas‐Marquez, F. , & Ready, P. D. (2004). Sandflies of the Phlebotomus perniciosus complex: Mitochondrial introgression and a new sibling species of P. longicuspis in the Moroccan Rif. Medical and Veterinary Entomology, 18(1), 25–37. 10.1111/j.0269-283x.2004.0471.x PubMed DOI

Pierro, A. , Ficarelli, S. , Ayhan, N. , Morini, S. , Raumer, L. , Bartoletti, M. , Mastroianni, A. , Prati, F. , Schivazappa, S. , Cenni, P. , Vocale, C. , Rossini, G. , Gaibani, P. , Sambri, V. , Landini, M. P. , Lewis, R. E. , Charrel, R. N. , & Varani, S. (2017). Characterization of antibody response in neuroinvasive infection caused by Toscana virus. Clinical Microbiology and Infection, 23(11), 868–873. 10.1016/j.cmi.2017.03.017 PubMed DOI

Prion, S. , & Haerling, K. A. (2014). Making sense of methods and measurement: Spearman‐Rho ranked‐order correlation coefficient. Clinical Simulation in Nursing, 10(10), 535–536. 10.1016/j.ecns.2014.07.005 DOI

Punda‐Polić, V. , Jerončić, A. , Mohar, B. , & Šiško Kraljević, K. (2012). Prevalence of Toscana virus antibodies in residents of Croatia. Clinical Microbiology and Infection, 18(6), E200–E203. 10.1111/j.1469-0691.2012.03840.x PubMed DOI

Remoli, M. E. , Jiménez, M. , Fortuna, C. , Benedetti, E. , Marchi, A. , Genovese, D. , Gramiccia, M. , Molina, R. , & Ciufolini, M. G. (2016). Phleboviruses detection in Phlebotomus perniciosus from a human leishmaniasis focus in South‐West Madrid region, Spain. Parasites & Vectors, 9, 205. 10.1186/s13071-016-1488-3 PubMed DOI PMC

Riera, C. , Fisa, R. , Udina, M. , Gállego, M. , & Portus, M. (2004). Detection of Leishmania infantum cryptic infection in asymptomatic blood donors living in an endemic area (Eivissa, Balearic Islands, Spain) by different diagnostic methods. Transactions of the Royal Society of Tropical Medicine and Hygiene, 98(2), 102–110. 10.1016/S0035-9203(03)00015-4 PubMed DOI

Risueño, J. , Muñoz, C. , Pérez‐Cutillas, P. , Goyena, E. , Gonzálvez, M. , Ortuño, M. , Bernal, L. , Ortiz, J. , Alten, B. , & Berriatua, E. (2017). Understanding Phlebotomus perniciosus abundance in south‐east Spain: Assessing the role of environmental and anthropic factors. Parasites & Vectors, 10(1), 189. 10.1186/s13071-017-2135-3 PubMed DOI PMC

Risueño, J. , Spitzová, T. , Bernal, L. J. , Muñoz, C. , López, M. C. , Thomas, M. C. , Infante, J. J. , Volf, P. , & Berriatua, E. (2019). Longitudinal monitoring of anti‐saliva antibodies as markers of repellent efficacy against Phlebotomus perniciosus and Phlebotomus papatasi in dogs. Medical and Veterinary Entomology, 33(1), 99–109. 10.1111/MVE.12343 PubMed DOI

Rohoušová, I. , Ozensoy, S. , Ozbel, Y. , & Volf, P. (2005). Detection of species‐specific antibody response of humans and mice bitten by sand flies. Parasitology, 130(Pt 5), 493–499. http://www.ncbi.nlm.nih.gov/pubmed/15991492 PubMed

Rohoušová, I. , Volfová, V. , Nová, S. , & Volf, P. (2012). Individual variability of salivary gland proteins in three Phlebotomus species. Acta Tropica, 122(1), 80–86. 10.1016/j.actatropica.2011.12.004 PubMed DOI

Sakhria, S. , Bichaud, L. , Mensi, M. , Salez, N. , Dachraoui, K. , Thirion, L. , Cherni, S. , Chelbi, I. , De Lamballerie, X. , Zhioua, E. , & Charrel, R. N. (2013). Co‐circulation of Toscana virus and Punique virus in Northern Tunisia: A microneutralisation‐based seroprevalence study. PLoS Neglected Tropical Diseases, 7(9), e2429. 10.1371/journal.pntd.0002429 PubMed DOI PMC

Sanbonmatsu‐Gámez, S. , Pérez‐Ruiz, M. , Collao, X. , Sánchez‐Seco, M. P. , Morillas‐Márquez, F. , De, L. a , Rosa‐Fraile, M. , Navarro‐Marí, J. M. , & Tenorio, A. (2005). Toscana virus in Spain. Emerging Infectious Diseases, 11(11), 1701–1707. 10.3201/eid1111.050851 PubMed DOI PMC

Sanchez, J. , Dohoo, I. , Markham, F. , Leslie, K. , & Conboy, G. (2002). Evaluation of the repeatability of a crude adult indirect Ostertagia ostertagi ELISA and methods of expressing test results. Veterinary Parasitology, 109(1–2), 75–90. 10.1016/S0304-4017(02)00194-2 PubMed DOI

Terrosi, C. , Olivieri, R. , Bianco, C. , Cellesi, C. , & Cusi, M. G. (2009). Age‐dependent seroprevalence of Toscana virus in central Italy and correlation with the clinical profile. Clinical and Vaccine Immunology, 16(8), 1251–1252. 10.1128/CVI.00376-08 PubMed DOI PMC

Tesh, R. B. , Saidi, S. , Gajdamovic, S. J. , Rodhain, F. , & Vesenjak‐Hirjan, J. (1976). Serological studies on the epidemiology of sandfly fever in the Old World. Bulletin of the World Health Organization, 54(6), 663–674. PubMed PMC

Thrusfield, M. (2018). Veterinary epidemiology (4th edn.). Wiley; Blackwell 10.1002/9781118280249 DOI

Tripathi, P. , Singh, V. , & Naik, S. (2007). Immune response to Leishmania: Paradox rather than paradigm. FEMS Immunology and Medical Microbiology, 51(2), 229–242. 10.1111/j.1574-695X.2007.00311.x PubMed DOI

Valassina, M. , Valentini, M. , Pugliese, A. , Valensin, P. E. , & Cusi, M. G. (2003). Serological survey of Toscana virus infections in a high‐risk population in Italy. Clinical and Vaccine Immunology, 10(3), 483–484. 10.1128/CDLI.10.3.483-484.2003 PubMed DOI PMC

Vlkova, M. , Rohoušová, I. , Hostomska, J. , Pohankova, L. , Zidkova, L. , Drahota, J. , Valenzuela, J. G. , & Volf, P. (2012). Kinetics of antibody response in BALB/c and C57BL/6 mice bitten by Phlebotomus papatasi . PLoS Neglected Tropical Diseases, 6(7), e1719. 10.1371/journal.pntd.0001719 PubMed DOI PMC

Vlkova, M. , Rohoušová, I. , Drahota, J. , Stanneck, D. , Kruedewagen, E. M. , Mencke, N. , Otranto, D. , & Volf, P. (2011). Canine antibody response to Phlebotomus perniciosus bites negatively correlates with the risk of Leishmania infantum transmission. PLoS Neglected Tropical Diseases, 5(10), e1344. 10.1371/journal.pntd.0001344 PubMed DOI PMC

Volf, P. , & Rohoušová, I. (2001). Species‐specific antigens in salivary glands of phlebotomine sandflies. Parasitology, 122(Pt 1), 37–41. 10.1017/s0031182000007046 PubMed DOI

Volf, P. , & Volfova, V. (2011). Establishment and maintenance of sand fly colonies. Journal of Vector Ecology, 36(Suppl. 1), S1–S9. 10.1111/j.1948-7134.2011.00106.x PubMed DOI

Willen, L. , Lestinova, T. , Kalousková, B. , Sumova, P. , Spitzova, T. , Velez, R. , Domenech, E. , Vaněk, O. , Gállego, M. , Mertens, P. , & Volf, P. (2019). Field study of the improved rapid sand fly exposure test in areas endemic for canine leishmaniasis. PLoS Neglected Tropical Diseases, 13(11), e0007832. 10.1371/journal.pntd.0007832 PubMed DOI PMC

Demographic characteristics and prevalence of asymptomatic Leishmania donovani infection in migrant workers working in an endemic area in Northwest Ethiopia