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Predicting the risk of an endemic focus of Leishmania tropica becoming established in south-western Europe through the presence of its main vector, Phlebotomus sergenti Parrot, 1917

Published online by Cambridge University Press:  21 August 2013

S. D. BARÓN ,
F. MORILLAS-MÁRQUEZ ,
M. MORALES-YUSTE ,
V. DÍAZ-SÁEZ ,
M. GÁLLEGO ,
R. MOLINA  and
J. MARTÍN-SÁNCHEZ
S. D. BARÓN
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, Campus Universitario de Cartuja, 18071 Granada, Spain
F. MORILLAS-MÁRQUEZ
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, Campus Universitario de Cartuja, 18071 Granada, Spain
M. MORALES-YUSTE
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, Campus Universitario de Cartuja, 18071 Granada, Spain
V. DÍAZ-SÁEZ
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, Campus Universitario de Cartuja, 18071 Granada, Spain
M. GÁLLEGO
Affiliation:
Laboratorio de Parasitología, Facultad de Farmacia, Universidad de Barcelona, Barcelona, Spain
R. MOLINA
Affiliation:
Servicio de Parasitología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Ctra. Majadahonda-Pozuelo S/N, 28220, Majadahonda, Madrid, Spain
J. MARTÍN-SÁNCHEZ*
Affiliation:
Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, Campus Universitario de Cartuja, 18071 Granada, Spain
*
*Corresponding author: Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, Campus Universitario de Cartuja, 18071 Granada, Spain. E-mail: joaquina@ugr.es
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Summary

The aim of the study was the construction of risk maps for exposure to Phlebotomus sergenti, the main vector of Leishmania tropica, with a view to identifying hot spots for the potential establishment of this parasite in the southwest of Europe. Data were collected on the presence/absence of this vector and the ecological and climatic characteristics of 662 sampling sites located in the southeast, centre and northeast of the Iberian Peninsula (south-western Europe). The environmental factors associated with the distribution of P. sergenti were determined. The best predictors for the presence of this dipteran were ‘altitude’, ‘land use’, ‘land surface temperature’, ‘aspect’, ‘adjacent land cover’, ‘absence of vegetation in wall’ and the ‘absence of PVC pipes in the drainage holes of retaining walls’. Risk maps for exposure to the vector were drawn up based on these variables. The validation of the predictive risk model confirmed its usefulness in the detection of areas with a high risk of P. sergenti being present. These locations represent potential hot spots for an autochthonous focus of L. tropica becoming established. The risk maps produced for P. sergenti presence revealed several areas in the centre and south of the Iberian Peninsula to be the most prone to this process, which would make it possible for the disease to enter south-western Europe.

Keywords

anthroponotic cutaneous leishmaniasisLeishmania tropicapredictive distribution of Phlebotomus sergentiGeographic Information Systems (GIS)environmental factorsrisk mapssouth-western Europe
Type
Research Article
Information
Parasitology , Volume 140 , Issue 11 , September 2013 , pp. 1413 - 1421
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Alvar, J., Vélez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., den Boer, M. and WHO Leishmaniasis Control Team (2012). Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.CrossRefGoogle ScholarPubMed
Al-Zahrani, M. A., Peters, W., Evans, P. A., Ching-Chin, I., Smith, V. and Lane, R. P. (1988). Phlebotomus sergenti, a vector of Leishmania tropica in Saudi Arabia. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 416.CrossRefGoogle Scholar
Al-Zahrani, M. A., Peters, W., Evans, P. A., Smith, V. and Ching-Chin, I. (1989). Leishmania infecting man and wild animals in Saudi Arabia. 6. Cutaneous leishmaniasis of man in the south-west. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 621–628.CrossRefGoogle ScholarPubMed
Antinori, S., Gianelli, E., Calattini, S., Longhi, E., Gramiccia, M. and Corbellino, M. (2005). Cutaneous leishmaniasis: an increasing threat for travelers. Clinical Microbiology and Infection 11, 343–346.CrossRefGoogle Scholar
Aransay, A. M., Testa, J. M., Morillas-Márquez, F., Lucientes, J. and Ready, P. D. (2004). Distribution of sandfly species in relation to canine leishmaniasis from the Ebro Valley to Valencia, northeastern Spain. Parasitology Research 94, 416–420.CrossRefGoogle ScholarPubMed
Aspöck, H., Gerersdorfer, T., Formayer, H. and Walochnik, J. (2008). Sandflies and sandfly-borne infections of humans in Central Europe in the light of climate change. Wiener Klinische Wochenschrift 120(19–20 Suppl. 4), 24–29.CrossRefGoogle ScholarPubMed
Barón, S., Martín-Sánchez, J., Gállego, M., Morales-Yuste, M., Boussaa, S. and Morillas-Márquez, F. (2008). Intraspecific variability (rDNA ITS and mtDNA Cyt b) of Phlebotomus sergenti in Spain and Morocco. Acta Tropica 107, 259–267.CrossRefGoogle ScholarPubMed
Barón, S. D., Morillas-Márquez, F., Morales-Yuste, M., Díaz-Sáez, V., Irigaray, C. and Martín-Sánchez, J. (2011). Risk maps for the presence and absence of Phlebotomus perniciosus in an endemic area of leishmaniasis in southern Spain: implications for the control of the disease. Parasitology 138, 1234–1244.CrossRefGoogle Scholar
Berdjane-Brouk, Z., Koné, A. K., Djimdé, A. A., Charrel, R. N., Ravel, C., Delaunay, P., del Giudice, P., Diarra, A. Z., Doumbo, S., Goita, S., Thera, M. A., Depaquit, J., Marty, P., Doumbo, O. K. and Izri, A. (2012). First detection of Leishmania major DNA in Sergentomyia (Spelaeomyia) darlingi from cutaneous leishmaniasis foci in Mali. PLoS ONE 7, e28266.CrossRefGoogle ScholarPubMed
Campino, L., Pratlong, F., Abranches, P., Rioux, J. A., Santos-Gomes, G., Alves-Pires, C., Cortes, S., Ramada, J., Cristovao, J. M., Afonso, M. O. and Dedet, J. P. (2006). Leishmaniasis in Portugal: enzyme polymorphism of Leishmania infantum based on the identification of 213 strains. Tropical Medicine and International Health 2, 1708–1714.CrossRefGoogle Scholar
Depaquit, J., Ferté, H., Léger, N., Lefranc, F., Alves-Pires, C., Hanafi, H., Maroli, M., Morillas-Márquez, F., Rioux, J. A., Svobodova, M. and Volf, P. (2002). ITS 2 sequences heterogeneity in Phlebotomus sergenti and Phlebotomus similis (Diptera, Psychodidae): possible consequences in their ability to transmit Leishmania tropica. International Journal of Parasitology 32, 1123–1131.CrossRefGoogle ScholarPubMed
Dereure, J., Rioux, J. A., Gállego, M., Perières, J., Pratlong, F., Mahjour, J. and Saddiki, H. (1991). Leishmania tropica in Morocco: infection in dogs. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 595.CrossRefGoogle ScholarPubMed
D'Urso, V., Ruta, F., Khoury, C., Bianchi, R., Depaquit, J. and Maroli, M. (2004). About the presence of Phlebotomus sergenti Parrot, 1917 (Diptera: Psychodidae) in Eastern Sicily, Italy. Parasite 11, 279–283.CrossRefGoogle ScholarPubMed
Gállego-Berenguer, J., Botet-Fregola, J., Gállego-Culleré, M. and Portús-Vinyeta, M. (1992). Los flebotomos de la España peninsular e Islas Baleares. Identificación y corología. Comentarios sobre métodos de captura. In “In memoriam” al Prof D. F. de P. Martínez Gómez (ed. Hernández, S.), pp. 581–600. Publicaciones de la Universidad de Córdoba, Córdoba, Spain.Google Scholar
Gálvez, R., Descalzo, M. A., Miró, G., Jiménez, M., Martín, O., Dos Santos-Brandao, F., Guerrero, I. and Molina, R. (2010). Seasonal trends and spatial relations between environmental/meteorological factors and leishmaniosis sand fly vector abundances in Central Spain. Acta Tropica 115, 95–102.CrossRefGoogle ScholarPubMed
Gramiccia, M. and Gradoni, L. (2005). The current status of zoonotic leishmaniases and approaches to disease control. International Journal for Parasitology 35, 1169–1180.CrossRefGoogle ScholarPubMed
Grimm, F., Gessler, M. and Brun, R. (1996). Isolation and characterization of Leishmania parasites imported into Switzerland – a retrospective study. Parasitology Research 82, 563–565.CrossRefGoogle ScholarPubMed
Guessous-Idrissi, N., Chiheb, S., Hamdani, A., Riyad, M., Bichichi, M., Hamdani, S. and Krimech, A. (1997). Cutaneous leishmaniasis: an emerging epidemic focus of Leishmania tropica in north Morocco. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 660–663.CrossRefGoogle ScholarPubMed
Guevara-Benítez, D., Úbeda-Ontiveros, J. M. and Morillas-Márquez, F. (1978). Phlebotominae de la provincia de Granada: estudio de poblaciones. Revista Ibérica de Parasitología 38, 813–839.Google Scholar
Guilvard, E., Rioux, J. A., Gállego, M., Pratlong, F., Mahjour, J., Martinez-Ortega, E., Dereure, J., Saddiki, A. and Martini, A. (1991). Leishmania tropica au Maroc. III. Rôle vecteur de Phlebotomus sergenti. Annales de Parasitologie Humaine et Comparée 66, 96–99.CrossRefGoogle ScholarPubMed
Guilvard, E., Gállego, M., Moreno, G., Fisa, R., Rispail, P., Pratlong, F., Martinez-Ortega, E., Gallego, J. and Rioux, J. A. (1996). Infestation naturelle de Phlebotomus ariasi et Phlebotomus perniciosus (Diptera, Psychodidae) par Leishmania infantum (Kinetoplastida–Trypanosomatidae) en Catalogne (Espagne). Parasite 3, 191–192.CrossRefGoogle Scholar
Kamhawi, S., Modi, G. B., Pimenta, P. F., Rowton, E. and Sacks, D. L. (2000). The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology 121, 25–33.CrossRefGoogle ScholarPubMed
Kimutai, A., Kamau Ngure, P., Kiprotich Tonui, W., Muita Gicheru, M. and Bonareri Nyamwamu, L. (2009). Leishmaniasis in northern and western Africa: a review. African Journal of Infectious Diseases 3, 14–25.Google Scholar
Lewis, D. J. (1971). Phlebotomid sandflies. Bulletin of the World Health Organization 44, 535–551.Google ScholarPubMed
Martínez-Ortega, E. (1986). Biología de los flebotomos Ibéricos (Diptera, Psychodidae) en condiciones naturales. Annali dell'Istituto Superiore di Sanità 22, 73–78.Google Scholar
Martínez-Ortega, E. (1988). Caracterización de las poblaciones de flebotomos (Diptera, Psychodidae) en el sureste de la Península Ibérica. Revista Ibérica de Parasitología 48, 79–87.Google Scholar
Martínez-Ortega, E. and Conesa-Gallego, E. (1987). Estructura de las poblaciones de flebotomos (Dipt., Psychodidae) del sureste de la Península Ibérica. Mediterránea Serie de estudios Biológicos 9, 87–99.CrossRefGoogle Scholar
Martín-Sánchez, J., Gramiccia, M., Di Muccio, T., Ludovisi, A. and Morillas-Márquez, F. (2004). Isoenzymatic polymorphism of Leishmania infantum in southern Spain. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 228–232.CrossRefGoogle ScholarPubMed
Martín-Sánchez, J., Morales-Yuste, M., Acedo-Sanchez, C., Barón, S., Díaz, V. and Morillas-Márquez, F. (2009). Canine leishmaniasis in southeastern Spain. Emerging Infectious Diseases 15, 795–798.CrossRefGoogle ScholarPubMed
Morillas-Márquez, F., Guevara Benítez, D. C., Úbeda Ontiveros, J. M. and González Castro, J. (1983). Fluctuations annuelles des populations de phlébotomes (Diptera, Phlebotomidae) dans la province de Grenade (Espagne). Annales de Parasitologie Humaine et Comparée 58, 625–632.CrossRefGoogle Scholar
Morizot, G., Delgiudice, P., Caumes, E., Laffitte, E., Marty, P., Dupuy, A., Sarfati, C., Hadj-Rabia, S., Darie, H., Le Guern, A. S., Salah, A. B., Pratlong, F., Dedet, J. P., Grögl, M. and Buffet, P. A. (2007). Healing of Old World cutaneous leishmaniasis in travelers treated with fluconazole: drug effect or spontaneous evolution? American Journal of Tropical Medicine and Hygiene 76, 48–52.CrossRefGoogle ScholarPubMed
Norman, F. F., Pérez de Ayala, A., Pérez-Molina, J. A., Monge-Maillo, B., Zamarrón, P. and López-Vélez, R. (2010). Neglected tropical diseases outside the tropics. PLoS Neglected Tropical Diseases 4, e762. doi: 10.1371/journal.pntd.0000762.CrossRefGoogle ScholarPubMed
Pratlong, F., Rioux, J. A., Marty, P., Faraut-Gambarelli, F., Dereure, J., Lanotte, G. and Dedet, J. P. (2004). Isoenzymatic analysis of 712 strains of Leishmania infantum in the south of France and relationship of enzymatic polymorphism to clinical and epidemiological features. Journal of Clinical Microbiology 42, 4077–4082.CrossRefGoogle ScholarPubMed
Ramaoui, K., Guernaoui, S. and Boumezzough, A. (2008). Entomological and epidemiological study of a new focus of cutaneous leishmaniasis in Morocco. Parasitology Research 103, 859–863. doi: 10.1007/s00463-008-1068-3.CrossRefGoogle ScholarPubMed
Ready, P. D. (2010). Leishmaniasis emergence in Europe. EuroSurveillance 15, pii=19505.CrossRefGoogle ScholarPubMed
Ready, P. D. (2011). Should sand fly taxonomy predict vectorial and ecological traits? Journal of Vector Ecology 36(Suppl. 1), S17–S22.CrossRefGoogle ScholarPubMed
Rioux, J. A., Houin, R., Baudouy, J. P., Croset, H. and Tour, S. (1970). Présence en Corse de Phlebotomus (Paraphlebotomus) sergenti Parrot, 1917. Annales de Parasitologie Humaine et Comparée 45, 343–356.CrossRefGoogle ScholarPubMed
Rioux, J. A., Croset, H. and Lanotte, G. (1977). Écologie d'un foyer méditerranéen de leishmaniose viscérale. Essai de modélisation. Colloque International CNRS 39, 295–305.Google Scholar
Rioux, J. A., Jarry, D., Maazoun, R. and Wallbanks, K. (1982). Confirmation de l'existence en France continentale de Phlebotomus sergenti Parrot, 1917. Annales de Parasitologie 57, 647–648.Google Scholar
Rioux, J. A., Lanotte, G., Petter, F., Dereure, J., Akalay, O., Pratlong, F., Velez, I. D., Fikri, N. D., Maazoun, R., Denial, N.et al. (1986). Les leishmanioses cutanées du bassin méditerranéen occidental; De l'identification enzymatique à l'analyse éco-épidémiologique; L'exemple de trois “foyers”, tunisien, marocain, et français. In Leishmania. Taxonomie et Phylogenèse. Applications Eco-épidémiologiques (Int Coll CNRS/INSERM/OMS (2–6 July 1984)), pp. 365–395. Institut Méditer-ranéen d'Etudes Epidémiologiques et Ecologiques, Montpellier, France.Google Scholar
Rivas Martínez, S., Bandullo, J. M., Serrada, R., Allue Andrade, J. L., Moreno del Burgo, J. L. and González Rebollar, J. L. (1987). Memoria del Mapa de series de vegetación de España (ed. ICONA). Ministerio de Agricultura, Pesca y Alimentación, Madrid, Spain.Google Scholar
Schnur, L. F., Nasereddin, A., Eisenberger, C. L., Jaffe, C. L., El Fari, M., Azmi, K., Anders, G., Killick-Kendrick, M., Killick-Kendrick, R., Dedet, J. P., Pratlong, F., Kanaan, M., Grossman, T., Jacobson, R. L., Schonian, G. and Warburg, A. (2004). Multifarious characterization of Leishmania tropica from a judean desert focus, exposing intraspecific diversity and incriminating Phlebotomus sergenti as its vector. American Journal of Tropical Medicine and Hygiene 70, 364–372.CrossRefGoogle ScholarPubMed
Semenza, J. C. and Menne, B. (2009). Climate change and infectious diseases in Europe. Lancet Infectious Diseases 9, 365–375.CrossRefGoogle ScholarPubMed
Semião-Santos, S. J., el Harith, A., Ferreira, E., Pires, C. A., Sousa, C. and Gusmão, R. (1995). Evora district as a new focus for canine leishmaniasis in Portugal. Parasitology Research 81, 235–239.CrossRefGoogle ScholarPubMed
Senghor, M. W., Faye, M. N., Diarra, K., Elguero, E., Gay, O., Bañuls, A. L. and Niang, A. A. (2011). Ecology of phlebotomine sand flies in the rural community of Mont Rolland (Thiès Region, Sénégal): area of transmission of canine leishmaniasis. PloS ONE 6, e14773.CrossRefGoogle ScholarPubMed
Srivastava, A., Nagpal, B. N., Joshi, P. L., Paliwal, J. C. and Dash, A. P. (2009). Identification of malaria hot spots for focused intervention in tribal state of India: a GIS based approach. International Journal of Health Geographics 8, 30. doi: 10.1186/1476-072X-8-30.CrossRefGoogle ScholarPubMed
Svobodova, M., Votypka, J., Peckova, J., Dvorak, V., Nasereddin, A., Baneth, G., Sztern, J., Kravchenko, V., Orr, A., Meir, D., Schnur, L. F., Volf, P. and Warburg, A. (2006). Distinct transmission cycles of Leishmania tropica in 2 adjacent foci, northern Israel. Emerging Infectious Diseases 12, 1860–1868.CrossRefGoogle ScholarPubMed