Green periurban residential areas in Mediterranean countries have flourished in the last decades and become foci for leishmaniasis. To remedy the absence of information on vector ecology in these environments, we examined phlebotomine sand fly distribution in 29 sites in Murcia City over a 3-year period, including the plots of 20 detached houses and nine non-urbanized sites nearby. We collected 5,066 specimens from five species using "sticky" interception and light attraction traps. The relative frequency of the main Leishmania infantum vector Phlebotomus perniciosus in these traps was 32% and 63%, respectively. Sand fly density was widely variable spatially and temporally and greatest in non-urbanized sites, particularly in caves and abandoned buildings close to domestic animal holdings. Phlebotomus perniciosus density in house plots was positively correlated with those in non-urbanized sites, greatest in larger properties with extensive vegetation and non-permanently lived, but not associated to dog presence or a history of canine leishmaniasis. Within house plots, sand fly density was highest in traps closest to walls. Furthermore, the study provides a guideline for insect density assessment and reporting and is envisioned as a building block towards the development of a pan-European database for robust investigation of environmental determinants of sand fly distribution.

Área de Biología Animal Departamento de Zoología Y Antropología Física Facultad de Veterinaria Regional Campus of International Excellence Campus Mare Nostrum Universidad de Murcia Murcia Spain

Departamento de Genética Y Microbiología Facultad de Medicina Regional Campus of International Excellence Campus Mare Nostrum Universidad de Murcia Murcia Spain

Departamento de Geografía Universidad de Murcia Murcia Spain

Departamento de Medicina Y Cirugía Animal Facultad de Veterinaria Regional Campus of International Excellence Campus Mare Nostrum Universidad de Murcia Murcia Spain

Departamento de Sanidad Animal Facultad de Veterinaria Regional Campus of International Excellence Campus Mare Nostrum Universidad de Murcia Murcia Spain

Departamento de Zoología Y Antropología Física Facultad de Biología Regional Campus of International Excellence Campus Mare Nostrum Universidad de Murcia Murcia Spain

Department of Parasitology Faculty of Science Charles University Vinicna 7 128 44 Prague 2 Czech Republic

Department of Parasitology Faculty of Veterinary Medicine Alexandria University Alexandria Egypt

Servicio de Sanidad Ambiental Dirección General de Salud Pública Y Adicciones Consejería de Salud de La Región de Murcia Murcia Spain

Zobrazit více v PubMed

Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, Sereno D. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis. 2016;10:e0004349. doi: 10.1371/journal.pntd.0004349. PubMed DOI PMC

Alcover MM, Ballart C, Martín-Sánchez J, Serra T, Castillejo S, Portús M, Gállego M. Factors influencing the presence of sand flies in Majorca (Balearic Islands, Spain) with special reference to Phlebotomus pernicious, vector of Leishmania infantum. Parasit Vectors. 2014;7:421. doi: 10.1186/1756-3305-7-421. PubMed DOI PMC

Alexander B. Sampling methods for phlebotomine sandflies. Med Vet Entomol. 2000;14:109–122. doi: 10.1046/j.1365-2915.2000.00237.x. PubMed DOI

Alten B, Ozbel Y, Ergunay K, Kasap OE, Cull B, Antoniou M, Velo E, Prudhomme J, Molina R, Bañuls A-L, Schaffner F, Hendrickx G, Van Bortel W, Medlock JM. Sampling strategies for phlebotomine sand flies (Diptera: Psychodidae) in Europe. Bull Entomol Res. 2015;105:664–678. doi: 10.1017/S0007485315000127. PubMed DOI

Alten B, Maia C, Afonso MO, Campino L, Jiménez M, González E, Molina R, Bañuls AL, Prudhomme J, Vergnes B, Toty C, Cassan C, Rahola N, Thierry M, Sereno D, Bongiorno G, Bianchi R, Khoury C, Tsirigotakis N, Dokianakis E, Antoniou M, Christodoulou V, Mazeris A, Karakus M, Ozbel Y, Arserim SK, Erisoz Kasap O, Gunay F, Oguz G, Kaynas S, Tsertsvadze N, Tskhvaradze L, Giorgobiani E, Gramiccia M, Volf P, Gradoni L. Seasonal dynamics of phlebotomine sand fly species proven vectors of Mediterranean leishmaniasis caused by Leishmania infantum. PLoS Negl Trop Dis. 2016;10:e0004458. doi: 10.1371/journal.pntd.0004458. PubMed DOI PMC

Arce A, Estirado A, Ordobas M, Sevilla S, García N, Moratilla L, de la Fuente S, Martínez AM, Pérez AM, Aránguez E, Iriso A, Sevillano O, Bernal J, Vilas F. Re-emergence of leishmaniasis in Spain: community outbreak in Madrid, Spain, 2009 to 2012. Euro Surveill. 2013;18:20546. doi: 10.2807/1560-7917.es2013.18.30.20546. PubMed DOI

Ayhan N, Charrel RN. Of phlebotomines (sandflies) and viruses: a comprehensive perspective on a complex situation. Curr Opin Insect Sci. 2017;22:117–124. doi: 10.1016/j.cois.2017.05.019. PubMed DOI

Ballart C, Guerrero I, Castells X, Barón S, Castillejo S, Alcover MM, Portús M, Gállego M. Importance of individual analysis of environmental and climatic factors affecting the density of Leishmania vectors living in the same geographical area: the example of Phlebotomus ariasi and P. perniciosus in northeast Spain. Geospat Health. 2014;8:389–403. doi: 10.4081/gh.2014.28. PubMed DOI

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Collantes F, Martínez Ortega E. Sobre la validez taxonómica de Phlebotomus longicuspis (Nitzulescu, 1931) (Diptera: Psychodidae) Bol Asoc Esp Entomol. 1997;21:141–146.

Depaquit J, Ferté H, Léger N, Killick-Kendrick R, Rioux JA, Killick-Kendrick M, Hanafi HA, Gobert S. Molecular systematics of the phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) based on ITS2 rDNA sequences. Hypotheses of dispersion and speciation. Insect Mol Biol. 2000;9:293–300. doi: 10.1046/j.1365-2583.2000.00179.x. 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. Phlebotomus langeroni Nitzulescu (Diptera, Psychodidae) a new vector for Leishmania infantum in Europe. Parasitol Res. 2018;117:1105–1113. doi: 10.1007/s00436-018-5788-8. PubMed DOI

Gállego-Berenguer J, Botet-Fregola J, Gállego-Culleré M, Portús-Vinyeta M. Los flebotomos de la España peninsular e Islas Baleares: identificación y corología: comentarios sobre los métodos de captura. In: Hernández S, editor. Memoriam al Profesor Dr. DF de P Martínez Gómez. Córdoba: Publicaciones de la Universidad de Córdoba; 1992. pp. 581–600.

Gálvez R, Descalzo MA, Miró G, Jiménez MI, Martín O, Dos Santos-Brandao F, Guerrero I, Cubero E, Molina R. Seasonal trends and spatial relations between environmental/meteorological factors and leishmaniosis sand fly vector abundances in Central Spain. Acta Trop. 2010;115:95–102. doi: 10.1016/j.actatropica.2010.02.009. PubMed DOI

Gálvez R, Montoya A, Cruz I, Fernández C, Martín O, Checa R, Chicharro C, Migueláñez S, Marino V, Miró G. Latest trends in Leishmania infantum infection in dogs in Spain, part I: mapped seroprevalence and sand fly distributions. Parasit Vectors. 2020;13:204. doi: 10.1186/s13071-020-04081-7. PubMed DOI PMC

García San Miguel L, Sierra MJ, Vazquez A, Fernandez-Martínez B, Molina R, Sanchez-Seco MP, Lucientes J, Figuerola J, de Ory F, Monge S, Suarez B, Simón F. Phlebovirus-associated diseases transmitted by Phlebotominae in Spain: are we at risk? Enferm Infecc Microbiol Clin. 2020 doi: 10.1016/j.eimc.2020.02.026. PubMed DOI

Gil Collado J, Morillas Márquez F, Sanchís Marín MC. Los flebotomos en España. Rev San Hig Púb. 1989;63:15–34. PubMed

Goyena E, Pérez-Cutillas P, Chitimia L, Risueño J, García-Martínez JD, Bernal LJ, Berriatua E. A cross-sectional study of the impact of regular use of insecticides in dogs on canine leishmaniosis seroprevalence in southeast Spain. Prev Vet Med. 2016;124:78–84. doi: 10.1016/j.prevetmed.2015.12.009. PubMed DOI

Herrador Z, Gherasim A, Jimenez BC, Granados M, San Martín JV, Aparicio P. Epidemiological changes in leishmaniasis in Spain according to hospitalization-based records, 1997–2011: raising awareness towards leishmaniasis in non-HIV patients. PLoS Negl Trop Dis. 2015;9:e0003594. doi: 10.1371/journal.pntd.0003594. PubMed DOI PMC

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

Keskin M, Dogru AO, Balcik FB, Goksel C, Ulugtekin N, Sozen S. Comparing spatial interpolation methods for mapping meteorological data in Turkey. In: Bilge A, Toy A, Günay M, editors. Energy systems and management. Cham: Springer International Publishing; 2015. pp. 33–42.

Kleinbaum DG, Kupper LL, Muller KE, Nizam A. Applied regression analysis and other multivariable methods. Pacific Grove, CA: Duxbury Press; 1998.

Lehrter V, Bañuls A-L, Léger N, Rioux J-A, Depaquit J. Phlebotomus (Paraphlebotomus) chabaudi and Phlebotomus riouxi: closely related species or synonyms? Parasite. 2017;24:47. doi: 10.1051/parasite/2017050. PubMed DOI PMC

Martínez Ortega E, Conesa Gállego E, Goyena Salgado M, Romera Lozano E. Presencia de Phlebotomus (Larroussius) langeroni Nitzulescu, 1930 (Diptera: Psychodidae) en la Península Ibérica. Bolm Soc Port Ent. 1992;139:196.

Martínez-García FA, Moreno-Docón A, López-López M, Albert-Lacal L, Martínez-Toldos MC, Segovia-Hernández M, Fernández-Barreiro A. A case of meningitis due to Toscana virus in Murcia. Rev Neurol. 2007;45:317–318. PubMed

Martínez-Ortega E. Los flebotomos ibéricos (Diptera: Psychodidae). II. El. sureste. An Biol. 1985;3:113–119.

Martínez-Ortega E. Los flebotomos Ibéricos (Diptera: Psychodidae). I. Almería. An Biol. 1985;3:107–111.

Martínez-Ortega E. Biología de los flebotomos ibéricos (Diptera: Psychodidae) en condiciones naturales. Ann Ist Super Sanita. 1986;22:73–78. PubMed

Martínez-Ortega E, Conesa-Gallego E. Caracteres morfológicos de interés taxonómico de los flebotomos (Diptera, Psychodidae) de la Península Ibérica. An Biol. 1987;11:43–53.

Martínez-Ortega E, Romera E, Conesa-Gallego E, Goyena M. Estudio comparado de la antropofilia y el fototropismo de los flebotomos en un foco de leishmaniasis del sureste de la Península Ibérica. Parassitologia. 1991;33:413–419. PubMed

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

Molina R, Jiménez MI, Cruz I, Iriso A, Martín-Martín I, Sevillano O, Melero S, Bernal J. The hare (Lepus granatensis) as potential sylvatic reservoir of Leishmania infantum in Spain. Vet Parasitol. 2012;190:268–271. doi: 10.1016/j.vetpar.2012.05.006. PubMed DOI

Muñoz C, Risueño J, Yilmaz A, Pérez-Cutillas P, Goyena E, Ortuño M, Bernal LJ, Ortiz J, Alten B, Berriatua E. Investigations of Phlebotomus perniciosus sand flies in rural Spain reveal strongly aggregated and gender-specific spatial distributions and advocate use of light-attraction traps. Med Vet Entomol. 2018;32:186–196. doi: 10.1111/mve.12275. PubMed DOI

Muñoz C, Martínez-de la Puente J, Figuerola J, Pérez-Cutillas P, Navarro R, Ortuño M, Bernal LJ, Ortiz J, Soriguer R, Berriatua E. Molecular xenomonitoring and host identification of Leishmania sand fly vectors in a Mediterranean periurban wildlife park. Transbound Emerg Dis. 2019;66:2546–2561. doi: 10.1111/tbed.13319. PubMed DOI

Orshan L, Elbaz S, Ben-Ari Y, Akad F, Afik O, Ben-Avi I, Dias D, Ish-Shalom D, Studentsky L, Zonstein I. Distribution and dispersal of Phlebotomus papatasi (Diptera: Psychodidae) in a zoonotic cutaneous leishmaniasis focus, the Northern Negev Israel. Plos Negl Trop Dis. 2016;10:e0004819. doi: 10.1371/journal.pntd.0004819. PubMed DOI PMC

Pérez-Cutillas P, Goyena E, Chitimia L, De la Rúa P, Bernal LJ, Fisa R, Riera C, Iborra A, Murcia L, Segovia M, Berriatua E. Spatial distribution of human asymptomatic Leishmania infantum infection in southeast Spain: a study of environmental, demographic and social risk factors. Acta Trop. 2015;146:127–134. doi: 10.1016/j.actatropica.2015.03.017. PubMed DOI

Remoli ME, Jiménez M, Fortuna C, Benedetti E, Marchi A, Genovese D, Gramiccia M, Molina R, Ciufolini MG. Phleboviruses detection in Phlebotomus perniciosus from a human leishmaniasis focus in South-West Madrid region Spain. Parasit Vectors. 2016;9:205. doi: 10.1186/s13071-016-1488-3. PubMed DOI PMC

Rioux J-A, Carron S, Dereure J, Périères J, Zeraia L, Franquet E, Babinot M, Gállego M, Prudhomme J. Ecology of leishmaniasis in the South of France. 22. Reliability and representativeness of 12 Phlebotomus ariasi, P. perniciosus and Sergentomyia minuta (Diptera: Psychodidae) sampling stations in Vallespir (eastern French Pyrenees region) Parasite. 2013;20:34. doi: 10.1051/parasite/2013035. PubMed DOI PMC

Risueño J, Muñoz C, Pérez-Cutillas P, Goyena E, Gonzálvez M, Ortuño M, Bernal LJ, Ortiz J, Alten B, Berriatua E. Understanding Phlebotomus perniciosus abundance in south-east Spain: assessing the role of environmental and anthropic factors. Parasit Vectors. 2017;10:189. doi: 10.1186/s13071-017-2135-3. PubMed DOI PMC

Snijders TAB, Bosker RJ. Multilevel analysis: an introduction to basic and advanced multilevel modeling. London: SAGE Publications; 1999.

Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vector Ecol. 2011;36:S1–S9. doi: 10.1111/j.1948-7134.2011.00106.x. PubMed DOI

WHO (2010) Control of the leishmaniases: report of a meeting of the WHO Expert Commitee on the Control of Leishmaniases, Geneva, 22-26 March 2010. World Health Organization

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