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Leishmania infantum in wild rodents: reservoirs or just irrelevant incidental hosts?

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Abstract

Wild rodents constitute a very large biomass of potential reservoirs for Leishmania spp. Therefore, an epidemiological study was carried out in a well-known focus of canine leishmaniasis from southern Spain, with the objective of detecting and characterizing Leishmania infantum infection in wild rodents. Blood, liver, spleen, bone marrow, and skin from 37 rodents (24 Apodemus sylvaticus, 9 Rattus rattus, and 4 Mus musculus) were analyzed by optical microscopy, culture, and two different polymerase chain reactions. L. infantum DNA was found in 27 % (10 out of 37) of the trapped rodents, in a variety of tissues: bone marrow, spleen, or healthy skin (ear lobe). High prevalences of L. infantum infection were found in the three investigated rodent species. The presence of other trypanosomatids was also evidenced. These rodent species are abundant, widely distributed in Europe, and have a long enough lifespan to overcome the low sandfly activity season. They live in a suitable habitat for sandflies and serve as blood sources for these insects, which can become infected when induced to feed on Leishmania-infected animals. Whether they are reservoirs or just irrelevant incidental hosts, it is clear that the epidemiology of L. infantum is more complex than previously thought, and so is its control. The classic epidemiological cycle dog-sandfly-human is turning into a network of animal species that collaborate with the dog in the maintenance of the parasite under natural conditions and probably showing local differences.

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References

  • Acedo-Sánchez C, Martín-Sánchez J, Velez-Bernal ID, Sanchiz-Marín MC, Maldonado JA, Louassini M, Morillas-Márquez F (1996) Leishmaniasis eco-epidemiology in the Alpujarra Region (Granada province, Southern Spain). Int J Parasitol 26(3):303–310

    Article  PubMed  Google Scholar 

  • Aliaga L, Cobo F, Mediavilla JD, Bravo J, Osuna A, Amador JM, Martín-Sánchez J, Cordero E, Navarro JM (2003) Localized mucosal leishmaniasis due to Leishmania (Leishmania) infantum: clinical and microbiologic findings in 31 patients. Medicine (Baltimore) 82(3):147–158

    Google Scholar 

  • Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M, WHO Leishmaniasis Control Team (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7(5):e35671. doi:10.1371/journal.pone.0035671

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Antoniou M, Gramiccia M, Molina R, Dvorak V, Volf P (2013) The role of indigenous phlebotomine sandflies and mammals in the spreading of leishmaniasis agents in the Mediterranean region. Euro Surveill 18(30):20540

    CAS  PubMed  Google Scholar 

  • Ashford RW (1996) Leishmaniasis reservoirs and their significance in control. Clin Dermatol 14(5):523–532

    Article  CAS  PubMed  Google Scholar 

  • Ballart C, Alcover MM, Portús M, Gállego M (2012) Is leishmaniasis widespread in Spain? First data on canine leishmaniasis in the province of Lleida, Catalonia, northeast Spain. Trans R Soc Trop Med Hyg 106(2):134–136

    Article  CAS  PubMed  Google Scholar 

  • Barón SD, Morillas-Márquez F, Morales-Yuste M, Díaz-Sáez V, Irigaray C, Martín-Sánchez J (2011) Risk maps for the presence and absence of Phlebotomusperniciosusin an endemic area of leishmaniasis in southern Spain: implications for the control of the disease. Parasitology 138(10):1234–1244

    Article  PubMed  Google Scholar 

  • Bongiorno G, Habluetzel A, Khoury C, Maroli M (2003) Host preferences of phlebotomine sand flies at a hypoendemic focus of canine leishmaniasis in central Italy. Acta Trop 88(2):109–116

    Article  CAS  PubMed  Google Scholar 

  • Burton M (1978) Guía de los mamíferos de España y de Europa. Ediciones Omega, Barcelona

    Google Scholar 

  • Criado-Fornelio A, Gutiérrez-García L, Rodríguez-Caabeiro F, Reus-García E, Roldan-Soriano MA, Díaz-Sánchez MA (2000) A parasitological survey of wild red foxes (Vulpesvulpes) from the province of Guadalajara, Spain. Vet Parasitol 92(4):245–251

    Article  CAS  PubMed  Google Scholar 

  • De Colmenares M, Portús M, Botet J, Dobaño C, Gállego M, Wolff M, Seguí G (1995) Identification of blood meals of Phlebotomus perniciosus (Diptera: Psychodidae) in Spain by a competitive enzyme-linked immunosorbent assay biotin/avidin method. J Med Entomol 32(3):229–233

    Article  PubMed  Google Scholar 

  • Desjeux P (2001) The increase in risk factors for leishmaniasis worldwide. Trans R Soc Trop Med Hyg 95(3):239–243

    Article  CAS  PubMed  Google Scholar 

  • Di Bella C, Vitale F, Russo G, Greco A, Milazzo C, Aloise G, Cagnin M (2003) Are rodents a potential reservoir for Leishmania infantum in Italy? J Mt Ecol 7:125–129

    Google Scholar 

  • Díaz-Sáez V, Merino-Espinosa G, Morales-Yuste M, Corpas-López V, Pratlong F, Morillas-Márquez F, Martín-Sánchez J (2014) High rates of Leishmania infantum and Trypanosoma nabiasi infection in wild rabbits (Oryctolaguscuniculus) in sympatric and syntrophic conditions in an endemic canine leishmaniasis area: epidemiological consequences. Vet Parasitol 202(3–4):119–127. doi:10.1016/j.vetpar.2014.03.029

    Article  PubMed  Google Scholar 

  • Dipineto L, Manna L, Baiano A, Gala M, Fioretti A, Gravino AE, Menna LF (2007) Presence of Leishmania infantum in red foxes (Vulpesvulpes) in southern Italy. J Wildl Dis 43(3):518–520

    Article  PubMed  Google Scholar 

  • Fernández-Bellón H, Solano-Gallego L, Bardagí M, Alberola J, Ramis A, Ferrer L (2006) Immune response to Leishmania infantum in healthy horses in Spain. Vet Parasitol 135(2):181–185

    Article  PubMed  Google Scholar 

  • Fisa R, Gállego M, Castillejo S, Aisa MJ, Serra T, Riera C, Carrió J, Gállego J, Portús M (1999) Epidemiology of canine leishmaniosis in Catalonia (Spain) the example of the Priorat focus. Vet Parasitol 83(2):87–97

    Article  CAS  PubMed  Google Scholar 

  • Gálvez R, Miró G, Descalzo MA, Nieto J, Dado D, Martín O, Cubero E, Molina R (2010) Emerging trends in the seroprevalence of canine leishmaniasis in the Madrid region (central Spain). Vet Parasitol 169(3–4):327–334. doi:10.1016/j.vetpar.2009.11.025

    Article  PubMed  Google Scholar 

  • Gradoni L, Pozio E, Gramiccia M, Maroli M, Bettini S (1983) Leishmaniasis in Tuscani (Italy): VII. Studies on the role of the black rat, Rattusrattus, in the epidemiology of visceral leishmaniasis. Trans R Soc Trop Med Hyg 77(4):427–431

    Article  CAS  PubMed  Google Scholar 

  • Gramiccia M, Maazoun R, Lanotte G, Rioux JA, Le Blancq S, Evans DA, Peters V, Bettini S, Gradoni L, Pozio E (1982) Typage enzymatique de onze souches de Leishmania isolées, en Italie Continentale, a partir de formes viscérales murines, canines et vulpines. Mise en évidence d’un varianten zymatique chez le renard (Vulpesvulpes) et le chien. Ann Parasitol Hum Comp 57(6):527–531

    CAS  PubMed  Google Scholar 

  • Helhazar M, Leitao J, Duarte A, Tavares L, Pereira da Fonseca I (2013) Natural infection of synathropic rodent species Mus musculus and Rattus norvegicus by Leishmania infantum in Sesimbra and Sintra–Portugal. Parasit Vectors 6:88. doi:10.1186/1756-3305-6-88

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiménez M, González E, Martín-Martín I, Hernández S, Molina R (2014) Could wild rabbits (Oryctolaguscuniculus) be reservoirs for Leishmania infantum in the focus of Madrid, Spain? Vet Parasitol 202(3–4):296–300. doi:10.1016/j.vetpar.2014.03.027

    Article  PubMed  Google Scholar 

  • Maia C, Dionísio L, Afonso MO, Neto L, Cristóvão JM, Campino L (2013) Leishmania infection and host-blood feeding preferences of phletobomine sandflies and canine leishmaniasis in an endemic European area, the Algarve Region in Portugal. Mem Inst Oswaldo Cruz Rio de Janeiro 108(4):481–487. doi:10.1590/S0074-0276108042013014

    Article  Google Scholar 

  • Martín-Sánchez J, López-López MC, Acedo-Sánchez C, Castro-Fajardo JJ, Pineda JA, Morillas-Márquez F (2001) Diagnosis of infections with Leishmania infantum using PCR-ELISA. Parasitology 122(Pt 6):607–615

    PubMed  Google Scholar 

  • Martín-Sánchez J, Gramiccia M, Di Muccio T, Ludovisi A, Morillas-Márquez F (2004) Isoenzymatic polymorphism of Leishmania infantum in southern Spain. Trans R Soc Trop Med Hyg 98(4):228–232

    Article  PubMed  Google Scholar 

  • Martín-Sánchez J, Acedo C, Muñoz-Pérez M, Pesson B, Marchal O, Morillas-Márquez F (2007) Infection by Leishmania infantum in cats: epidemiological study in Spain. Vet Parasitol 145(3–4):267–273

    Article  PubMed  Google Scholar 

  • Martín-Sánchez J, Morales-Yuste M, Acedo-Sánchez C, Barón S, Díaz V, Morillas-Márquez F (2009) Canine leishmaniasis in southeastern Spain. Emerg Infect Dis 15(5):795–798. doi:10.3201/eid1505.080969

    Article  PubMed Central  PubMed  Google Scholar 

  • Millán J, Ferroglio E, Solano-Gallego L (2014) Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitol Res 113(6):2005–2014. doi:10.1007/s00436-014-3929-2

    Article  PubMed  Google Scholar 

  • Miró G, Cardoso L, Pennisi MG, Oliva G, Baneth G (2008) Canine leishmaniosis—new concepts and insights on an expanding zoonosis: part two. Trends Parasitol 24(8):371–377. doi:10.1016/j.pt.2008.05.003

    Article  PubMed  Google Scholar 

  • Mohebali M, Javadian E, Yaghoobi-Ershadi MR, Akhavan AA, Hajjaran H, Abaei MR (2004) Characterization of Leishmania infection in rodents from endemic areas of the Islamic Republic of Iran. East Mediterr Health J10(4–5):591–599

    Google Scholar 

  • Molina R, Jiménez MI, Cruz I, Iriso A, Martín-Martín I, Sevillano O, Melero S, Bernal J (2012) The hare (Lepus granatensis) as potential sylvatic reservoir of Leishmania infantum in Spain. Vet Parasitol 190(1–2):268–271. doi:10.1016/j.vetpar.2012.05.006

    Article  CAS  PubMed  Google Scholar 

  • Molyneux DH (1970) Developmental patterns in trypanosomes of the subgenus Herpetosoma. Ann Soc Belges Med Trop Parasitol Mycol 50(2):229–237

    CAS  PubMed  Google Scholar 

  • Morales-Yuste M, Morillas-Márquez F, Díaz-Sáez V, Barón-López S, Acedo-Sánchez C, Martín-Sánchez J (2012) Epidemiological implications of the use of various methods for the diagnosis of canine leishmaniasis in dogs with different characteristics and in differing prevalence scenarios. Parasitol Res 111(1):155–164. doi:10.1007/s00436-011-2812-7

    Article  PubMed  Google Scholar 

  • Morillas F, Sánchez-Rabasco F, Ocaña J, Martín-Sánchez J, Ocaña-Wihelmi J, Acedo C, Sanchís-Marín MC (1996) Leishmaniosis in the focus of the Axarquia region, Malaga province, southern Spain: a survey of the human, dog, and vector. Parasitol Res 82(6):569–570

    Article  CAS  PubMed  Google Scholar 

  • Morillas-Márquez F, Benavides-Delgado I, González-Castro J, Reyes-Magaña A, Valero-López A (1985) Ocurrence of Leishmania sp in Rattusrattus in the province of Granada. Ann Parasitol Hum Comp 60:768–770

    Google Scholar 

  • Motazedian MH, Parhizkari M, Mehrabani D, Hatam G, Asgari Q (2010) First detection of Leishmania major in Rattus norvegicus from Fars Province, Southern Iran. Vector Borne Zoonotic Dis 10(10):969–975. doi:10.1089/vbz.2008.0214

    Article  PubMed  Google Scholar 

  • Oliveira FS, Pirmez C, Pires MQ, Brazil RP, Pacheco RS (2005) PCR-based diagnosis for detection of Leishmania in skin and blood of rodents from an endemic area of cutaneous and visceral leishmaniasis in Brazil. Vet Parasitol 129(3–4):219–227

    Article  CAS  PubMed  Google Scholar 

  • Papadogiannakis E, Spanakos G, Kontos V, Menounos PG, Tegos N, Vakalis N (2010) Molecular detection of Leishmania infantum in wild rodents (Rattus norvegicus) in Greece. Zoonoses Public Health 57(7–8):e23–e25. doi:10.1111/j.1863-2378.2009.01264.x

    Article  CAS  PubMed  Google Scholar 

  • Portús M, Gállego M, Riera C, Aisa MJ, Fisa R, Castillejo S (2002) Wild and domestic mammals in the life cycle of Leishmania infantum in Southwest Europe. A literature review and studies performed in Catalonia (Spain). Rev Iber Parasitol 62:72–76

    Google Scholar 

  • Psaroulaki A, Antoniou M, Toumazos P, Mazeris A, Ioannou I, Chochlakis D, Christophi N, Loukaides P, Patsias A, Moschandrea I, Tselentis Y (2010) Rats as indicators of the presence and dispersal of six zoonotic microbial agents in Cyprus, an island ecosystem: a seroepidemiological study. Trans R Soc Trop Med Hyg 104(11):733–739. doi:10.1016/j.trstmh.2010.08.005

    Article  PubMed  Google Scholar 

  • Quinnell RJ, Courtenay O (2009) Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology 136(14):1915–1934. doi:10.1017/S0031182009991156

    Article  CAS  PubMed  Google Scholar 

  • Rioux JA, Golvan YJ (1968) Epidémiologie des leishmaniosesdans le sud de la France. Monographie INSERM 37, 223pp

  • Rioux JA, Albaret L, Houin R, Dedet JP, Lanotte G (1968) Ecologie des Leishmanioses dans le sud de la France. 2. Les réservoirs selvatiques. Infestation spontanée du Renard (Vulpes vulpes L.). Ann Parasitol Hum Comp 43:421–428

    CAS  PubMed  Google Scholar 

  • Rossi E, Bongiorno G, Ciolli E, Di Muccio T, Scalone A, Gramiccia M, Gradoni L, Maroli M (2008) Seasonal phenology, host-blood feeding preferences and natural Leishmania infection of Phlebotomus pernicious (Diptera, Psychodidae) in a high-endemic focus of canine leishmaniasis in Rome province, Italy. Acta Trop 105(2):158–165

    Article  CAS  PubMed  Google Scholar 

  • Schönian G, Nasereddin A, Dinse N, Schweynoch C, Schallig HD, Presber W, Jaffe CL (2003) PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis 47(1):349–358

    Article  PubMed  Google Scholar 

  • Sobrino R, Ferroglio E, Oleaga A, Romano A, Millán J, Revilla M, Arnal MC, Trisciuoglio A, Gortázar C (2008) Characterization of widespread canine leishmaniasis among wild carnivores from Spain. Vet Parasitol 155(3–4):198–203. doi:10.1016/j.vetpar.2008.05.003

    Article  CAS  PubMed  Google Scholar 

  • Svobodová M, Votýpka J (2003) Experimental transmission of Leishmania tropica to hamsters and mice by the bite of Phlebotomus sergenti. Microbes Infect 5(6):471–474

    Article  PubMed  Google Scholar 

  • Zanet S, Sposimo P, Trisciuoglio A, Giannini F, Strumia F, Ferroglio E (2014) Epidemiology of Leishmania infantum, Toxoplasma gondii, and Neospora caninum in Rattus rattus in absence of domestic reservoir and definitive hosts. Vet Parasitol 199(3–4):247–249. doi:10.1016/j.vetpar.2013.10.023

    Article  CAS  PubMed  Google Scholar 

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Funding

This study was funded by the Junta de Andalucía (research group BIO 176).

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None declared.

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Authors and Affiliations

  1. Departamento de Parasitología, Facultad de Farmacia, Universidad de Granada, 18071, Granada, Spain

    H. M. Navea-Pérez, V. Díaz-Sáez, V. Corpas-López, G. Merino-Espinosa, F. Morillas-Márquez & J. Martín-Sánchez

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  1. H. M. Navea-Pérez
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  2. V. Díaz-Sáez
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  3. V. Corpas-López
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  4. G. Merino-Espinosa
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  5. F. Morillas-Márquez
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  6. J. Martín-Sánchez
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Correspondence to J. Martín-Sánchez.

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Victoriano Diaz-Saez holds a doctorate, Universidad de Granada

Francisco Morillas-Marquez holds a doctorate, Universidad de Granada

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Navea-Pérez, H.M., Díaz-Sáez, V., Corpas-López, V. et al. Leishmania infantum in wild rodents: reservoirs or just irrelevant incidental hosts?. Parasitol Res 114, 2363–2370 (2015). https://doi.org/10.1007/s00436-015-4434-y

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