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The Role of Reservoirs: Canine Leishmaniasis

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Drug Resistance in Leishmania Parasites

Abstract

Canine leishmaniasis caused by Leishmania (Leishmania) infantum species (syn. L. (L.) chagasi species in Latin America), which is transmitted by the bite of phlebotomine sand flies, is endemic and affects millions of dogs in Asia, Europe, North Africa, and South America and is considered as an emergent disease in North America. Domestic dogs (Canis familiaris) are the major hosts for these parasites and the main reservoir host for human infection.

Recent years have seen important advances on the epidemiology, pathology, and canine genetic factors linked with animal resistance or susceptibility to leishmaniasis. Despite the lack of pathognomonic manifestations, infection by Leishmania can be suspected if a combination of clinical signs is present, namely, lymphadenomegaly, cutaneous alterations, loss of body weight, ocular disturbs, epistaxis, onychogryphosis, and lameness. However, the definitive diagnosis of canine leishmaniasis is complex since not all infected animals develop signs of disease. This fact cannot be ignored since asymptomatic (without clinical signs) dogs are infectious to phlebotomine vectors, although at a lower risk than symptomatic (with clinical signs) dogs. The fact that dogs never achieve parasitological cure together with the widespread use of the available anti-Leishmania drugs for both canine and human treatment certainly contributes to the spread of drug-resistant parasites with the natural consequences for the clinical outcome of the disease.

Early detection of infection and close surveillance or treatment of infected animals together with the development of effective molecules for therapy (ideally different from the ones used for humans) and, more importantly, for immunoprophylaxis are essential to control the dissemination of the disease among other dogs, being also a crucial element for the control of human zoonotic leishmaniasis.

This chapter reviews the role of dogs as reservoir hosts of L. (L.) infantum and as accidental hosts of other Leishmania species, as well as the role of other mammals as potential reservoir hosts of parasites belonging to the L. (L.) donovani complex. The potential generation and spread of drug resistance by the use of the same compounds in both canine and human hosts are also discussed.

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References

  1. Bray R. The zoonotic potential of reservoirs of leishmaniasis in the Old World. Ecol Dis. 1982;1:257–67.

    PubMed  CAS  Google Scholar 

  2. Ashford R. Leishmaniasis reservoirs and their significance in control. Clin Dermatol. 1996;14:523–32.

    Article  PubMed  CAS  Google Scholar 

  3. WHO. Working to Overcome the Global Impact of Neglected Tropical Diseases; 2010. http://www.who.int/neglected_diseases/2010report/NTD_2010report_web.pdf

  4. Duprey ZH, Steurer FJ, Rooney JA, Kirchhoff LV, et al. Canine visceral leishmaniasis, United States and Canada, 2000–2003. Emerg Infect Dis. 2006;12:440–6.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Petersen CA. Leishmaniasis, an emerging disease found in companion animals in the United States. Top Companion Anim Med. 2009;24:182–8.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Lukes J, Mauricio IL, Schönian G, Dujardin JC, et al. Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc Natl Acad Sci USA. 2007;104:9375–80.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Solano-Gallego L, Koutinas A, Miró G, Cardoso L, et al. Directions for the diagnosis, clinical staging, treatment and prevention of canine leishmaniosis. Vet Parasitol. 2009;165:1–18.

    Article  PubMed  CAS  Google Scholar 

  8. Baneth G, Koutinas AF, Solano-Gallego L, Bourdeau P, et al. Canine leishmaniosis – new concepts and insights on an expanding zoonosis: part one. Trends Parasitol. 2008;24:324–30.

    Article  PubMed  Google Scholar 

  9. Campino L. Canine reservoirs and leishmaniasis: epidemiology and disease. In: Farrel JP, editor. World Class Parasites Leishmania, vol. 4. Boston, Dordrecht, London: Kluwer Academic; 2002. p. 45–57.

    Google Scholar 

  10. Cortes S, Afonso MO, Alves-Pires C, Campino L. Stray dogs and leishmaniasis in urban areas, Portugal. Emerg Infect Dis. 2007;13:1431–2.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Miró G, Cardoso L, Pennisi MG, Oliva G, et al. Canine leishmaniosis-new concepts and insights on an expanding zoonosis: part two. Trends Parasitol. 2008;24:371–7.

    Article  PubMed  Google Scholar 

  12. Marty P, Le Fichoux Y, Giordana D, Brugnetti A. Leishmanin reaction in the human population of a highly endemic focus of canine leishmaniasis in Alpes-Maritimes, France. Trans R Soc Trop Med Hyg. 1992;86:249–50.

    Article  PubMed  CAS  Google Scholar 

  13. Cunha S, Freire M, Eulalio C, Cristóvão J, et al. Visceral leishmaniasis in a new ecological niche near a major metropolitan area of Brazil. Trans R Soc Trop Med Hyg. 1995;89:155–8.

    Article  PubMed  CAS  Google Scholar 

  14. Antoniou M, Gramiccia M, Molina R, Dvorak V, et al. The role of indigenous phlebotomine sandflies and mammals in the spreading of leishmaniasis agents in the Mediterranean region. Euro Surveill. 2013;18:20540.

    Article  PubMed  CAS  Google Scholar 

  15. Shaw S, Langton D, Hillman T. Canine leishmaniosis in the United Kingdom: a zoonotic disease waiting for a vector? Vet Parasitol. 2009;163:281–5.

    Article  PubMed  Google Scholar 

  16. Svobodova V, Svoboda M, Friedlaenderova L, Drahotsky P, et al. Canine leishmaniosis in three consecutive generations of dogs in Czech Republic. Vet Parasitol. 2017;237:122–4.

    Article  PubMed  Google Scholar 

  17. Karkamo V, Kaistinen A, Näreaho A, Dillard K, et al. The first report of autochthonous non-vector-borne transmission of canine leishmaniosis in the Nordic countries. Acta Vet Scand. 2014;56:84.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Naucke T, Lorentz S. First report of venereal and vertical transmission of canine leishmaniosis from naturally infected dogs in Germany. Parasit Vectors. 2012;5:67.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Tánczos B, Balogh N, Király L, Biksi I, et al. First record of autochthonous canine leishmaniasis in Hungary. Vector Borne Zoonotic Dis. 2012;12:588–94.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Mircean V, Dumitrache MO, Mircean M, Bolfa P. Autochthonous canine leishmaniasis in Romania: neglected or (re)emerging? Parasit Vectors. 2014;7:135.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Teske E, van Knapen F, Beijer EGM, Slappendel RJ. Risk of infection with Leishmania spp. in the canine population in the Netherlands. Acta Vet Scand. 2002;43:195–201.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Maia C, Cardoso L. Spread of Leishmania infantum in Europe with dog travelling. Vet Parasitol. 2015;213:2–11.

    Article  PubMed  Google Scholar 

  23. Gaskin AA, Schantz P, Jackson J, Birkenheuer A, et al. Visceral leishmaniasis in a New York foxhound kennel. J Vet Intern Med. 2002;16:34–44.

    Article  PubMed  Google Scholar 

  24. Best MP, Ash A, Bergfeld J, Barrett J. The diagnosis and management of a case of leishmaniosis in a dog imported to Australia. Vet Parasitol. 2014;202:292–5.

    Article  PubMed  Google Scholar 

  25. Maroli M, Rossi L, Baldelli R, Capelli G, et al. The northward spread of leishmaniasis in Italy: evidence from retrospective and ongoing studies on the canine reservoir and phlebotomine vectors. Tropical Med Int Health. 2008;13:256–64.

    Article  Google Scholar 

  26. Dereure J, Vanwambeke SO, Malé P, Martinez S, et al. The potential effects of global warming on changes in canine leishmaniasis in a focus outside the classical area of the disease in southern France. Vector Borne Zoonotic Dis. 2009;9:687–94.

    Article  PubMed  Google Scholar 

  27. Ballart C, Alcover MM, Picado A, Nieto J, et al. First survey on canine leishmaniosis in a non-classical area of the disease in Spain (Lleida, Catalonia) based on a veterinary questionnaire and a cross-sectional study. Prev Vet Med. 2013;109:116–27.

    Article  PubMed  Google Scholar 

  28. Miró G, Checa R, Montoya A, Hernández L, et al. Current situation of Leishmania infantum infection in shelter dogs in northern Spain. Parasit Vectors. 2012;5:60.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Chargui N, Haouas N, Gorcii M, Akrout Messaidi F, et al. Increase of canine leishmaniasis in a previously low-endemicity area in Tunisia. Parasite. 2007;14:247–51.

    Article  PubMed  CAS  Google Scholar 

  30. Schantz P, Steurer FJ, Duprey ZH, Kurpel KP, et al. Autochthonous visceral leishmaniasis in dogs in North America. J Am Vet Med Assoc. 2005;226:1316–22.

    Article  PubMed  Google Scholar 

  31. Rosypal AC, Troy GC, Zajac AM, Frank G, et al. Transplacental transmission of a North American isolate of Leishmania infantum in an experimentally infected beagle. J Parasitol. 2005;91:970–2.

    Article  PubMed  Google Scholar 

  32. Da Silva S, Ribeiro VM, Ribeiro RR, Tafuri WL, et al. First report of vertical transmission of Leishmania (Leishmania) infantum in a naturally infected bitch from Brazil. Vet Parasitol. 2009;166:159–62.

    Article  PubMed  Google Scholar 

  33. Gibson-Corley KN, Hostetter JM, Hostetter SJ, Mullin K, et al. Disseminated Leishmania infantum infection in two siblings’ foxhounds due to possible vertical transmission. Can Vet J. 2008;49:1005–8.

    PubMed  PubMed Central  Google Scholar 

  34. Riera C, Valladares J. Viable Leishmania infantum in urine and semen in experimentally infected dogs. Parasitol Today. 1996;12:412.

    Article  PubMed  CAS  Google Scholar 

  35. Diniz SA, Melo MS, Borges AM, Bueno R, et al. Genital lesions associated with visceral leishmaniasis and shedding of Leishmania sp. in the semen of naturally infected dogs. Vet Pathol. 2005;42:650–8.

    Article  PubMed  CAS  Google Scholar 

  36. De Freitas E, Melo MN, Pimenta Da Costa-Val A, Marques Michalick MS. Transmission of Leishmania infantum via blood transfusion in dogs: potential for infection and importance of clinical factors. Vet Parasitol. 2006;137:159–67.

    Article  PubMed  Google Scholar 

  37. Tabar MD, Roura X, Francino O, Altet L, et al. Detection of Leishmania infantum by real-time PCR in a canine blood bank. J Small Anim Pract. 2008;49:325–8.

    Article  PubMed  CAS  Google Scholar 

  38. Ferreira MG, Reinaldo Fattori K, Souza F, Marçal V, et al. Potential role for dog fleas in the cycle of Leishmania spp. Vet Parasitol. 2009;165:150–4.

    Article  PubMed  Google Scholar 

  39. Dantas-Torres F, Martins TF, Paiva-Cavalcanti M, Figueredo LA, et al. Transovarial passage of Leishmania infantum kDNA in artificially infected Rhipicephalus sanguineus. Exp Parasitol. 2010;125:184–5.

    Article  PubMed  CAS  Google Scholar 

  40. Campino L, Santos-Gomes G, Pratlong F, Dedet JP, et al. The isolation of Leishmania donovani MON-18, from an AIDS patient in Portugal: possible needle transmission. Parasite. 1994;1:391–2.

    Article  PubMed  CAS  Google Scholar 

  41. Molina R, Amela C, Nieto J, San-Andrés M, et al. Infectivity of dogs naturally infected with Leishmania infantum to colonized Phlebotomus perniciosus. Trans R Soc Trop Med Hyg. 1994;88:491–3.

    Article  PubMed  CAS  Google Scholar 

  42. Travi BL, Tabares CJ, Cadena H, Ferro C, et al. Canine visceral leishmaniasis in Colombia: relationship between clinical and parasitologic status and infectivity for sand flies. Am J Trop Med Hyg. 2001;64:119–24.

    Article  PubMed  CAS  Google Scholar 

  43. Quinnell R, Courtenay O. Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis. Parasitology. 2009;136:1915–34.

    Article  PubMed  CAS  Google Scholar 

  44. Campino L. Leishmanioses em Portugal. Características emergentes da epidemiologiae do diagnóstico. Universidade Nova de Lisboa, Instituto de Higiene e Medicina Tropical, 1998; p. 192.

    Google Scholar 

  45. Blackwell J, Goswami T, Evans CAW, Sibthorpe D, et al. SLC11A1 (formerly NRAMP1) and disease resistance. Cell Microbiol. 2001;3:773–84.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Altet L, Francino O, Solano-Gallego L, Renier C, et al. Mapping and sequencing of the canine NRAMP1 gene and identification of mutations in leishmaniasis susceptible dogs. Infect Immun. 2002;70:2763–71.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Sanchez-Robert E, Altet L, Sanchez A, Francino A. Polymorphism of SLC11A1 (NRAMP1) gene and canine leishmaniasis in a case-control study. J Hered. 2005;96:755–8.

    Article  PubMed  CAS  Google Scholar 

  48. Bueno R, Carvalho Neta AV, Xavier MN, Oliveira RG, et al. cDNA sequencing and expression of NRAMP1 (SLC11A1) in dogs phenotypically resistant or susceptible to visceral leishmaniasis. Vet Immunol Immunopathol. 2009;127:332–9.

    Article  PubMed  CAS  Google Scholar 

  49. Turchetti A, da Costa LF, Romão Ede L, Fujiwara RT, et al. Transcription of innate immunity genes and cytokine secretion by canine macrophages resistant or susceptible to intracellular survival of Leishmania infantum. Vet Immunol Immunopathol. 2015;163:67–76.

    Article  PubMed  CAS  Google Scholar 

  50. Quinnell R, Kennedy LJ, Barnes A, Courtenay O, et al. Susceptibility to visceral leishmaniasis in the domestic dog is associated with MHC class II polymorphism. Immunogenetics. 2003;55:23–8.

    PubMed  CAS  Google Scholar 

  51. Ciaramella P, Oliva G, De Luna R, Gradoni L, et al. A retrospective clinical study of canine leishmaniasis in 150 dogs naturally infected by Leishmania infantum. Vet Rec. 1997;141:539–43.

    Article  PubMed  CAS  Google Scholar 

  52. Solano-Gallego L, Llull J, Ramos G, Riera C, et al. The Ibizian hound presents a predominantly cellular immune response against natural Leishmania infection. Vet Parasitol. 2000;90:37–45.

    Article  PubMed  CAS  Google Scholar 

  53. França-Silva JC, da Costa RT, Siqueira AM, Machado-Coelho GL, et al. Epidemiology of canine visceral leishmaniosis in the endemic area of Montes Claros Municipality, Minas Gerais State, Brazil. Vet Parasitol. 2003;111:161–73.

    Article  PubMed  Google Scholar 

  54. Miranda S, Roura X, Picado A, Ferrer L, et al. Characterization of sex, age, and breed for a population of canine leishmaniosis diseased dogs. Res Vet Sci. 2008;85:35–8.

    Article  PubMed  Google Scholar 

  55. Cortes S, Vaz Y, Neves R, Maia C, et al. Risk factors for canine leishmaniasis in an endemic Mediterranean region. Vet Parasitol. 2012;189:189–96.

    Article  PubMed  Google Scholar 

  56. Killick-Kendrick R. The biology and control of phlebotomine sand flies. Clin Dermatol. 1999;17:279–89.

    Article  PubMed  CAS  Google Scholar 

  57. Gálvez R, Miró G, Descalzo MA, Nieto J, et al. Emerging trends in the seroprevalence of canine leishmaniasis in the Madrid region (central Spain). Vet Parasitol. 2010;169:327–34.

    Article  PubMed  CAS  Google Scholar 

  58. Koutinas AF, Polizopoulou ZS, Saridomichelakis MN, Argyriadis D, et al. Clinical considerations on canine visceral leishmaniasis in Greece: a retrospective study of 158 cases (1989–1996). J Am Anim Hosp Assoc. 1999;35:376–83.

    Article  PubMed  CAS  Google Scholar 

  59. Zivicnjak T, Martinković F, Marinculić A, Mrljak V, et al. A seroepidemiologic survey of canine visceral leishmaniosis among apparently healthy dogs in Croatia. Vet Parasitol. 2005;131:35–43.

    Article  PubMed  CAS  Google Scholar 

  60. Fisa R, Gállego M, Castillejo S, Aisa MJ, et al. Epidemiology of canine leishmaniosis in Catalonia (Spain) the example of the Priorat focus. Vet Parasitol. 1999;83:87–97.

    Article  PubMed  CAS  Google Scholar 

  61. Queiroz PVS, Monteiro GRG, Macedo VPS, Rocha MAC, et al. Canine visceral leishmaniasis in urban and rural areas of Northeast Brazil. Res Vet Sci. 2009;86:267–73.

    Article  PubMed  Google Scholar 

  62. Abranches P, Conceição-Silva F, Silva-Pereira M. Kala-azar in Portugal. V. The sylvatic cycle in the enzootic endemic focus of Arrábida. J Trop Med Hyg. 1984;87:197–200.

    PubMed  CAS  Google Scholar 

  63. Mancianti F, Mignone W, Galastri F. Serologic survey for leishmaniasis in free-living red foxes (Vulpes vulpes) in Italy. J Wildl Dis. 1994;30:454–6.

    Article  PubMed  CAS  Google Scholar 

  64. Molina R, Fernández BI, Santos Sanz S, Sierra Moros MJ, et al. The hare (Lepus granatensis) as potential sylvatic reservoir of Leishmania infantum in Spain. Vet Parasitol. 2012;190:268–71.

    Article  PubMed  CAS  Google Scholar 

  65. Jiménez M, González E, Martín-Martín I, Hernández S, et al. Could wild rabbits (Oryctolagus cuniculus) be reservoirs for Leishmania infantum in the focus of Madrid, Spain? Vet Parasitol. 2014;202:296–300.

    Article  PubMed  Google Scholar 

  66. Jimenez M, González E, Iriso A, Marco E, et al. Detection of Leishmania infantum and identification of blood meals in Phlebotomus perniciosus from a focus of human leishmaniasis in Madrid, Spain. Parasitol Res. 2013;112:2453–9.

    Article  PubMed  Google Scholar 

  67. Ozon C, Marty P, Pratlong F, Breton C, et al. Disseminated feline leishmaniosis due to Leishmania infantum in Southern France. Vet Parasitol. 1998;75:273–7.

    Article  PubMed  CAS  Google Scholar 

  68. Martín-Sánchez J, Acedo C, Muñoz-Pérez M, Pesson B, et al. Infection by Leishmania infantum in cats: epidemiological study in Spain. Vet Parasitol. 2007;145:267–73.

    Article  PubMed  Google Scholar 

  69. Nasereddin A, Salant H, Abdeen Z. Feline leishmaniasis in Jerusalem: serological investigation. Vet Parasitol. 2008;158:364–9.

    Article  PubMed  Google Scholar 

  70. Hatam GR, Hosseini SMH, Ardehali S, Fallah E, et al. First report of natural infection in cats with Leishmania infantum in Iran. Vector Borne Zoonotic Dis. 2010;10:313–6.

    Article  PubMed  Google Scholar 

  71. Vides J, Schwardt TF, Sobrinho LS, Marinho M, et al. Leishmania chagasi infection in cats with dermatologic lesions from an endemic area of visceral leishmaniosis in Brazil. Vet Parasitol. 2011;178:22–8.

    Article  PubMed  Google Scholar 

  72. Pennisi MG, Lupo T, Malara D, Masucci M, et al. Serological and molecular prevalence of Leishmania infantum infection in cats from Southern Italy. J Feline Med Surg. 2012;14:656–7.

    Google Scholar 

  73. Chatzis M, Andreadou M, Leontides L, Kasabalis D, et al. Cytological and molecular detection of Leishmania infantum in different tissues of clinically normal and sick cats. Vet Parasitol. 2014;202:217–25.

    Article  PubMed  CAS  Google Scholar 

  74. Maia C, Ramos C, Coimbra M, Bastos F, et al. Bacterial and protozoal agents of feline vector-borne diseases in domestic and stray cats from southern Portugal. Parasit Vectors. 2014;7:115.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Maia C, Sousa C, Ramos C, Cristóvão JV, et al. First case of feline leishmaniosis caused by Leishmania infantum genotype E in a cat with concurrent nasal squamous cell carcinoma. J Feline Med Surg. 2015;1:2055116915593969.

    Google Scholar 

  76. Pennisi MG, Cardoso L, Baneth G, Bordeau P, et al. Leish Vet update and recommendations on feline leishmaniosis. Parasit Vectors. 2015;8:302.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Can H, Döşkaya M, Gökhan Özdemir H, Atalay Şahar E, et al. Seroprevalence of Leishmania infection and molecular detection of Leishmania tropica and Leishmania infantum in stray cats of İzmir, Turkey. Exp Parasitol. 2016;167:109–14.

    Article  PubMed  Google Scholar 

  78. Poli A, Abramo F, Barsotti P, Leva S, et al. Feline leishmaniosis due to Leishmania infantum in Italy. Vet Parasitol. 2002;106:181–91.

    Article  PubMed  Google Scholar 

  79. Savani E, de Oliveira Camargo MC, de Carvalho MR, Zamperi RA, et al. The first record in the Americas of an autochthonous case of Leishmania (Leishmania) infantum chagasi in a domestic cat (Felix catus) from Cotia County, São Paulo State, Brazil. Vet Parasitol. 2004;120:229–33.

    Article  PubMed  Google Scholar 

  80. Maroli M, Pennisi MG, Di Muccio T, Khoury C, et al. Infection of sandflies by a cat naturally infected with Leishmania infantum. Vet Parasitol. 2007;145:357–60.

    Article  PubMed  Google Scholar 

  81. Maia C, Nunes M, Campino L. Importance of cats in zoonotic leishmaniasis in Portugal. Vector Borne Zoonotic Dis. 2008;8:555–9.

    Article  PubMed  Google Scholar 

  82. Maia C, Gomes J, Cristóvão J, Nunes M, et al. Feline Leishmania infection in a canine leishmaniasis endemic region, Portugal. Vet Parasitol. 2010;174:336–40.

    Article  PubMed  CAS  Google Scholar 

  83. Maia C, Campino L. Can domestic cats be considered reservoir hosts of zoonotic leishmaniasis? Trends Parasitol. 2011;27:341–4.

    Article  PubMed  Google Scholar 

  84. Bettini S, Pozio E, Gradoni L. Leishmaniasis in Tuscany (Italy): (II) Leishmania form wild Bodentia and Carnivora in a human and canine leishmaniasis focus. Trans R Soc Trop Med Hyg. 1980;74:77–83.

    Article  PubMed  CAS  Google Scholar 

  85. Papadogiannakis E, Spanakos G, Kontos V, Menounos PG, et al. Molecular detection of Leishmania infantum in wild rodents (Rattus norvegicus) in Greece. Zoonoses Public Health. 2009;57:e23–5.

    Article  Google Scholar 

  86. Koehler K, Stechele M, Hetzel U, Domingo M, et al. Cutaneous leishmaniosis in a horse in Southern Germany caused by Leishmania infantum. Vet Parasitol. 2002;109:9–17.

    Article  PubMed  Google Scholar 

  87. Solano-Gallego L, Fernández-Bellon H, Serra R, Gállego M, et al. Cutaneous leishmaniosis in three horses in Spain. Equine Vet J. 2003;35:320–3.

    Article  PubMed  CAS  Google Scholar 

  88. Rolão N, Martins MJ, João A, Campino L. Equine infection with Leishmania in Portugal. Parasite. 2005;12:183–6.

    Article  PubMed  Google Scholar 

  89. Soares I, Silva SO, Moreira FM, Prado LG, et al. First evidence of autochthonous cases of Leishmania (Leishmania) infantum in horse (Equus caballus) in the Americas and mixed infection of Leishmania infantum and Leishmania (Viannia) braziliensis. Vet Parasitol. 2013;197:665–9.

    Article  PubMed  Google Scholar 

  90. Bhattarai NR, Van der Auwera G, Rijal S, Picado A, et al. Domestic animals and epidemiology of visceral leishmaniasis, Nepal. Emerg Infect Dis. 2010;16:231–7.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Rohousova I, Talmi-Frank D, Kostalova T, Polanska T, et al. Exposure to Leishmania spp. and sand flies in domestic animals in northwestern Ethiopia. Parasit Vectors. 2015;8:360.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Peters W, Elbihari S, Evans D. Leishmania infecting man and wild animals in Saudi Arabia. 2. Leishmania arabica n. sp. Trans R Soc Trop Med Hyg. 1986;80:497–502.

    Article  PubMed  CAS  Google Scholar 

  93. Elbihari S, Cheema A, el-Hassan A. Leishmania infecting man and wild animals in Saudi Arabia. 4. Canine cutaneous leishmaniasis in the Eastern Province. Trans R Soc Trop Med Hyg. 1987;81:925–7.

    Article  PubMed  CAS  Google Scholar 

  94. Dereure J, Boni M, Pratlong F, El Hadi Osman M, et al. Visceral leishmaniasis in Sudan: first identifications of Leishmania from dogs. Trans R Soc Trop Med Hyg. 2000;94:154–5.

    Article  PubMed  CAS  Google Scholar 

  95. Dereure J, El-Safi SH, Bucheton B, Boni M, et al. Visceral leishmaniasis in Eastern Sudan: parasite identification in humans and dogs; host-parasite relationships. Microbes Infect. 2003;5:1103–8.

    Article  PubMed  Google Scholar 

  96. Peters W, Elbihari S, Liu C, Le Blancq SM, et al. Leishmania infecting man and wild animals in Saudi Arabia. 1. General survey. Trans R Soc Trop Med Hyg. 1985;79:831–9.

    Article  PubMed  CAS  Google Scholar 

  97. Morsy T, Schnur LF, Feinsod FM, Salem AM, et al. Natural infections of Leishmania major in domestic dogs from Alexandria, Egypt. Am J Trop Med Hyg. 1987;37:49–52.

    Article  PubMed  CAS  Google Scholar 

  98. Dereure J, Rioux JA, Gallego M, Perières J, et al. Leishmania tropica in Morocco: infection in dogs. Trans R Soc Trop Med Hyg. 1991;85:595.

    Article  PubMed  CAS  Google Scholar 

  99. Guessous-Idrissi N, Berrag B, Riyad M, Sahibi H, et al. Short report: Leishmania tropica: etiologic agent of a case of canine visceral leishmaniasis in northern Morocco. Am J Trop Med Hyg. 1997;57:172–3.

    Article  PubMed  CAS  Google Scholar 

  100. Lemrani M, Nejjar R, Pratlong F. A new Leishmania tropica zymodeme causative agent of canine visceral leishmaniasis in northern Morocco. Ann Trop Med Parasitol. 2002;96:637–8.

    Article  PubMed  CAS  Google Scholar 

  101. Ntais P, Christodoulou V, Tsirigotakis N, Dokianakis E, et al. Will the introduction of Leishmania tropica MON-58, in the island of Crete, lead to the settlement and spread of this rare zymodeme? Acta Trop. 2014;132:125–30.

    Article  PubMed  Google Scholar 

  102. Tolezano JE, Uliana SR, Taniguchi HH, Araújo MF, et al. The first records of Leishmania (Leishmania) amazonensis in dogs (Canis familiaris) diagnosed clinically as having canine visceral leishmaniasis from Araçatuba County, São Paulo State, Brazil. Vet Parasitol. 2007;149:280–4.

    Article  PubMed  Google Scholar 

  103. Ramírez J, Hernández C, León CM, Ayala MS, et al. Taxonomy, diversity, temporal and geographical distribution of cutaneous leishmaniasis in Colombia: a retrospective study. Sci Rep. 2016;6:28266.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Aguilar C, Fernandez E, Fernandez R, Deane L. Study of an outbreak of cutaneous leishmaniasis in Venezuela. The role of domestic animals. Mem Inst Oswaldo Cruz. 1984;79:181–95.

    Article  PubMed  CAS  Google Scholar 

  105. Vélez I, Carrillo LM, López L, Rodríguez E, et al. An epidemic outbreak of canine cutaneous leishmaniasis in Colombia caused by Leishmania braziliensis and Leishmania panamensis. Am J Trop Med Hyg. 2012;86:807–11.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Delgado O, Castes M, Clinton White A Jr, Kreutzer RD. Leishmania colombiensis in Venezuela. Am J Trop Med Hyg. 1993;48:145–7.

    Article  PubMed  CAS  Google Scholar 

  107. Hashiguchi Y, Gomez EA, de Coronel VV, Mimori T, et al. Andean leishmaniasis in Ecuador caused by infection with Leishmania mexicana and L. major-like parasites. Am J Trop Med Hyg. 1991;44:205–17.

    Article  PubMed  CAS  Google Scholar 

  108. Dereure J, Espinel I, Barrera C, Guerrini F, et al. Leishmaniasis in Ecuador. 4. Natural infestation of the dog by Leishmania panamensis. Ann Soc Belg Med Trop. 1994;74:29–33.

    PubMed  CAS  Google Scholar 

  109. Llanos-Cuentas EA, Roncal N, Villaseca P, Paz L, et al. Natural infections of Leishmania peruviana in animals in the Peruvian Andes. Trans R Soc Trop Med Hyg. 1999;93:15–20.

    Article  PubMed  CAS  Google Scholar 

  110. Hassan M, Osman FO, El-Raba’a F, Schallig H, et al. Role of the domestic dog as a reservoir host of Leishmania donovani in Eastern Sudan. Parasit Vectors. 2009;2:26.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Padilla A, Marco JD, Diosque P, Segura MA, et al. Canine infection and the possible role of dogs in the transmission of American tegumentary leishmaniosis in Salta, Argentina. Vet Parasitol. 2002;110:1–10.

    Article  PubMed  CAS  Google Scholar 

  112. Reithinger R, Espinoza J, Davies C. The transmission dynamics of canine American cutaneous leishmaniasis in Huánuco, Peru. Am J Trop Med Hyg. 2003;69:473–80.

    Article  PubMed  Google Scholar 

  113. Peña M, Roura X, Davidson M. Ocular and periocular manifestations of leishmaniasis in dogs: 105 cases (1993–1998). Vet Ophtalmol. 2000;1:35–41.

    Article  Google Scholar 

  114. Giunchetti RC, Martins-Filho OA, Carneiro CM, Mayrink W, et al. Histopathology, parasite density and cell phenotypes of the popliteal lymph node in canine visceral leishmaniasis. Vet Immunol Immunopathol. 2008a;121:23–33.

    Article  PubMed  Google Scholar 

  115. Santana C, Vassallo J, De Freitas LA, Oliveira G, et al. Inflammation and structural changes of splenic lymphoid tissue in visceral leishmaniasis: a study on naturally infected dogs. Parasite Immunol. 2008;30:515–24.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Giunchetti RC, Mayrink W, Carneiro CM, Corrêa-Oliveira R, et al. Histopathological and immunohistochemical investigations of the hepatic compartment associated with parasitism and serum biochemical changes in canine visceral leishmaniasis. Res Vet Sci. 2008b;84:269–77.

    Article  PubMed  Google Scholar 

  117. Nieto C, Navarrete I, Habela MA, Serrano F, et al. Pathological changes in kidneys of dogs with natural Leishmania infection. Vet Parasitol. 1992;45:33–47.

    Article  PubMed  CAS  Google Scholar 

  118. Petanides T, Koutinas AF, Mylonakis ME, Day MJ, et al. Factors associated with the occurrence of epistaxis in natural canine leishmaniasis (Leishmania infantum). J Vet Intern Med. 2008;22:866–72.

    Article  PubMed  CAS  Google Scholar 

  119. Blavier A, Keroack S, Denerolle P, Goy-Thollot I, et al. Atypical forms of canine leishmaniosis. Vet J. 2001;162:108–20.

    Article  PubMed  CAS  Google Scholar 

  120. Maia C, Campino L. Methods for diagnosis of canine leishmaniasis and immune response to infection. Vet Parasitol. 2008;158:274–87.

    Article  PubMed  CAS  Google Scholar 

  121. Paltrinieri S, Gradoni L, Roura X, Zatelli A, et al. Laboratory tests for diagnosing and monitoring canine leishmaniasis. Vet Clin Pathol. 2016;45:552–78.

    Article  PubMed  Google Scholar 

  122. Maia C, Ramada J, Cristóvão JM, Gonçalves L, et al. Diagnosis of canine leishmaniasis: conventional and molecular techniques using different tissues. Vet J. 2009;179:142–4.

    Article  PubMed  CAS  Google Scholar 

  123. Francino O, Altet L, Sánchez-Robert E, Rodriguez A, et al. Advantages of real-time PCR assay for diagnosis and monitoring of canine leishmaniosis. Vet Parasitol. 2006;137:214–21.

    Article  PubMed  CAS  Google Scholar 

  124. Gramiccia M, Di Muccio T, Fiorentino E, Scalone A, et al. Longitudinal study on the detection of canine Leishmania infections by conjunctival swab analysis and correlation with entomological parameters. Vet Parasitol. 2010;171:223–8.

    Article  PubMed  CAS  Google Scholar 

  125. Belinchón-Lorenzo S, Iniesta V, Parejo JC, Fernández-Cotrina J, et al. Detection of Leishmania infantum kinetoplast minicircle DNA by real time PCR in hair of dogs with leishmaniosis. Vet Parasitol. 2013;192:43–50.

    Article  PubMed  CAS  Google Scholar 

  126. Belinchón-Lorenzo S, Parejo JC, Iniesta V, Fernández-Cotrina J, et al. First detection of Leishmania kDNA in canine cerumen samples by qPCR. Vet Parasitol. 2016;228:65–8.

    Article  PubMed  CAS  Google Scholar 

  127. Ferreira A, Almeida GG, de Oliveira Silva S, Vogas GP, et al. Nasal, oral and ear swabs for canine visceral leishmaniasis diagnosis: new practical approaches for detection of Leishmania infantum DNA. PLoS Negl Trop Dis. 2013;7:e2150.

    Article  PubMed Central  CAS  Google Scholar 

  128. Noli C, Auxilia S. Treatment of canine Old World visceral leishmaniasis: a systematic review. Vet Dermatol. 2005;16:213–32.

    Article  PubMed  Google Scholar 

  129. Miró G, Oliva G, Cruz I, Canavate C, et al. Multicentric, controlled clinical study to evaluate effectiveness and safety of miltefosine and allopurinol for canine leishmaniosis. Vet Dermatol. 2009;20:397–404.

    Article  PubMed  Google Scholar 

  130. Bianciardi P, Brovida C, Valente M, Aresu L, et al. Administration of miltefosine and meglumine antimoniate in healthy dogs: clinicopathological evaluation of the impact on the kidneys. Toxicol Pathol. 2009;37:770–5.

    Article  PubMed  CAS  Google Scholar 

  131. Mateo M, Maynard L, Vischer C, Bianciardi P, et al. Comparative study on the short-term efficacy and adverse effects of miltefosine and meglumine antimoniate in dogs with natural leishmaniosis. Parasitol Res. 2009;105:155–62.

    Article  PubMed  Google Scholar 

  132. Oliva G, Gradoni L, Ciaramella P, De Luna R, et al. Activity of liposomal amphotericin B (AmBisome) in dogs naturally infected with Leishmania infantum. J Antimicrob Chemother. 1995;36:1013–9.

    Article  PubMed  CAS  Google Scholar 

  133. Sabaté D, Llinás J, Homedes J, Sustc M, et al. A single-centre, open-label, controlled, randomized clinical trial to assess the preventive efficacy of a domperidone-based treatment programme against clinical canine leishmaniasis in a high prevalence area. Prev Vet Med. 2014;115:56–63.

    Article  PubMed  Google Scholar 

  134. Croft S, Sundar S, Fairlamb A. Drug resistance in leishmaniasis. Clin Microbiol Rev. 2006;19:111–26.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  135. Gramiccia M, Gradoni L, Orsini S. Decreased sensitivity to meglumine antimoniate (Glucantime) of Leishmania infantum isolated from dogs after several courses of drug treatment. Ann Trop Med Parasitol. 1992;86:613–20.

    Article  PubMed  CAS  Google Scholar 

  136. Carrió J, Portús M. In vitro susceptibility to pentavalent antimony in Leishmania infantum strains is not modified during in vitro or in vivo passages but is modified after host treatment with meglumine antimoniate. BMC Pharmacol. 2002;2:11.

    Article  PubMed  PubMed Central  Google Scholar 

  137. Luz R, Melo M, Dujardin J, Maes L. Post-treatment Sb-susceptibility of Leishmania infantum clinical isolates of dogs. In: Fourth World Congress on Leishmaniasis. Lucknow: 4th Worldleish; 2009. p. 273.

    Google Scholar 

  138. Maia C, Nunes M, Marques M, Henriques S, et al. In vitro drug susceptibility of Leishmania infantum isolated from humans and dogs. Exp Parasitol. 2013;135:36–41.

    Article  PubMed  CAS  Google Scholar 

  139. Gradoni L, Maroli M, Gramiccia M, Mancianti F. Leishmania infantum infection rates in Phlebotomus perniciosus fed on naturally infected dogs under antimonial treatment. Med Vet Entomol. 1987;4:339–42.

    Article  Google Scholar 

  140. Aït-Oudhia K, Gazanion E, Sereno D, Oury B, et al. In vitro susceptibility to antimonials and amphotericin B of Leishmania infantum strains isolated from dogs in a region lacking drug selection pressure. Vet Parasitol. 2012;187:386–93.

    Article  PubMed  CAS  Google Scholar 

  141. Seblova V, Oury B, Eddaikra N, Aït-Oudhia K, et al. Transmission potential of antimony-resistant Leishmania field isolates. Antimicrob Agents Chemother. 2014;58:6273–6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Yasur-Landau D, Jaffe CL, David L, Baneth G. Allopurinol resistance in Leishmania infantum from dogs with disease relapse. PLoS Negl Trop Dis. 2016;10:e0004341.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. WHO. Report of a WHO informal consultation on liposomal amphotericin Bin the treatment of visceral leishmaniasis Rome, Italy; 2005. WHO/CDS/NTD/IDM/2007.4

    Google Scholar 

  144. Courtenay O, Quinnell RJ, Garcez LM, Shaw JJ, et al. Infectiousness in a cohort of Brazilian dogs: why culling fails to control visceral leishmaniasis in areas of high transmission. J Infect Dis. 2002;186:1314–20.

    Article  PubMed  Google Scholar 

  145. Nunes CM, Pires MM, da Silva KM, Assis FD, et al. Relationship between dog culling and incidence of human visceral leishmaniasis in an endemic area. Vet Parasitol. 2010;170:131–3.

    Article  PubMed  Google Scholar 

  146. Killick-Kendrick R, Killick-Kendrick M, Focheux C, Dereure J, et al. Protection of dogs from bites of phlebotomine sandflies by deltamethrin collars for control of canine leishmaniasis. Med Vet Entomol. 1997;11:105–11.

    Article  PubMed  CAS  Google Scholar 

  147. Courtenay O, Kovacic V, Gomes PA, Garcez LM, et al. A long-lasting topical deltamethrin treatment to protect dogs against visceral leishmaniasis. Med Vet Entomol. 2009;23:245–56.

    Article  PubMed  CAS  Google Scholar 

  148. Gavgani A, Hodjati MH, Mohite H, Davies CR. Effect of insecticide-impregnated dog collars on incidence of zoonotic visceral leishmaniasis in Iranian children: a matched-cluster randomised trial. Lancet. 2002;360:374–9.

    Article  PubMed  Google Scholar 

  149. Manzillo VF, Oliva G, Pagano A, Manna L, et al. Deltamethrin-impregnated collars for the control of canine leishmaniasis: evaluation of the protective effect and influence on the clinical outcome of Leishmania infection in kenneled stray dogs. Vet Parasitol. 2006;142:142–5.

    Article  CAS  Google Scholar 

  150. Maroli M, Gradoni L, Oliva G, Castagnaro M, et al. Guidelines for prevention of leishmaniasis in dogs. J Am Vet Med Assoc. 2010;236:1200–6.

    Article  PubMed  CAS  Google Scholar 

  151. Gradoni L. Canine Leishmania vaccines: still a long way to go. Vet Parasitol. 2015;208:94–100.

    Article  PubMed  CAS  Google Scholar 

  152. Silva V, Borja-Cabrera GP, Correia Pontes NN, de Souza EP, et al. A phase III trial of efficacy of the FML-vaccine against canine kala-azar in an endemic area of Brazil (São Gonçalo do Amaranto, RN). Vaccine. 2000;19:1082–92.

    Article  PubMed  Google Scholar 

  153. Borja-Cabrera G, Correia Pontes NN, da Silva VO, Paraguai de Souza E, et al. Long lasting protection against canine kala-azar using the FML-Quil A saponin vaccine in an endemic area of Brazil (São Gonçalo do Amarante, RN). Vaccine. 2002;20:3277–84.

    Article  PubMed  CAS  Google Scholar 

  154. Mohebali M, Khamesipour A, Mobedi I, Zarei Z, et al. Double-blind randomized efficacy field trial of alum precipitated autoclaved Leishmania major vaccine mixed with BCG against canine visceral leishmaniasis in Meshkin-Shahr district, I.R. Iran. Vaccine. 2004;22:4097–100.

    Article  PubMed  CAS  Google Scholar 

  155. Lemesre JL, Holzmuller P, Gonçalves RB, Bourdoiseau G, et al. Long-lasting protection against canine visceral leishmaniasis using the LiESAp-MDP vaccine in endemic areas of France: double-blind randomised efficacy field trial. Vaccine. 2007;25(21):4223–34.

    Article  PubMed  CAS  Google Scholar 

  156. Daneshvar H, Namazi MJ, Kamiabi H, Burchmore R, et al. Gentamicin-attenuated Leishmania infantum vaccine: protection of dogs against canine visceral leishmaniosis in endemic area of southeast of Iran. PLoS Negl Trop Dis. 2014;8(4):e2757.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  157. Oliva G, Nieto J, Foglia Manzillo V, Cappiello S, et al. A randomised, double-blind, controlled efficacy trial of the LiESP/QA-21 vaccine in naïve dogs exposed to two Leishmania infantum transmission seasons. PLoS Negl Trop Dis. 2014;8:e3213.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  158. Regina-Silva S, Feres AM, França-Silva JC, Dias ES, et al. Field randomized trial to evaluate the efficacy of the Leish-Tec® vaccine against canine visceral leishmaniasis in an endemic area of Brazil. Vaccine. 2016;34:2233–9.

    Article  PubMed  CAS  Google Scholar 

  159. Borja-Cabrera G, Cruz Mendes A, Paraguai de Souza E, Hashimoto Okada LY, et al. Effective immunotherapy against canine visceral leishmaniasis with the FML-vaccine. Vaccine. 2004;22:2234–43.

    Article  PubMed  CAS  Google Scholar 

  160. Saraiva E, de Figueiredo Barbosa A, Santos FN, Borja-Cabrera GP, et al. The FML-vaccine (Leishmune) against canine visceral leishmaniasis: a transmission blocking vaccine. Vaccine. 2006;24:2423–31.

    Article  PubMed  CAS  Google Scholar 

  161. Bongiorno G, Paparcone R, Foglia Manzillo V, Oliva G, et al. Vaccination with LiESP/QA-21 (CaniLeish®) reduces the intensity of infection in Phlebotomus perniciosus fed on Leishmania infantum infected dogs – a preliminary xenodiagnosis study. Vet Parasitol. 2013;197:691–5.

    Article  PubMed  CAS  Google Scholar 

  162. Alvar J, Cañavate C, Molina R, Moreno J, et al. Canine leishmaniasis. Adv Parasitol. 2004;57:1–88.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank A. Pereira for his work on the references. C. Maia, DVM, PhD, holds a FCT Investigator Starting Grant (IF/01302/2015) from Fundação para a Ciência e a Tecnologia, Ministério da Ciência, Tecnologia e Ensino Superior, Portugal.

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  1. Global Health and Tropical Medicine, GHTM, Instituto de Higiene e Medicina Tropical, IHMT, Universidade Nova de Lisboa, UNL, Lisboa, Portugal

    Lenea Campino & Carla Maia

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  1. Lenea Campino
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Correspondence to Lenea Campino .

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  1. Institute of Experimental Medicine, Universidad Central de Venezuela, Caracas, Venezuela

    Alicia Ponte-Sucre

  2. Escuela Luis Razetti Fac de Medicine, Universidad Central de Venezuela, Caracas, Venezuela

    Maritza Padrón-Nieves

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Campino, L., Maia, C. (2018). The Role of Reservoirs: Canine Leishmaniasis. In: Ponte-Sucre, A., Padrón-Nieves, M. (eds) Drug Resistance in Leishmania Parasites. Springer, Cham. https://doi.org/10.1007/978-3-319-74186-4_3

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