Canine Leishmaniasis: Update on Epidemiology, Diagnosis, Treatment, and Prevention
Abstract
:Simple Summary
Abstract
1. Introduction
2. Life Cycle, Hosts, and Vectors
3. The Disease in Dogs
3.1. Disease Mechanisms and Immune Response
3.2. Clinical Signs
4. Epidemiology
5. Diagnosis
6. Treatment
7. Prevention Measures and Vaccines
8. Conclusions and Perspective
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Baneth, G.; Nachum-Biala, Y.; Adamsky, O.; Gunther, I. Leishmania Tropica and Leishmania infantum Infection in Dogs and Cats in Central Israel. Parasit. Vectors 2022, 15, 147. [Google Scholar] [CrossRef] [PubMed]
- Jambulingam, P.; Pradeep Kumar, N.; Nandakumar, S.; Paily, K.P.; Srinivasan, R. Domestic Dogs as Reservoir Hosts for Leishmania Donovani in the Southernmost Western Ghats in India. Acta Trop. 2017, 171, 64–67. [Google Scholar] [CrossRef] [PubMed]
- Alvar, J.; Cañavate, C.; Molina, R.; Moreno, J.; Nieto, J. Canine Leishmaniasis. Adv. Parasitol. 2004, 57, 1–88. [Google Scholar] [CrossRef] [PubMed]
- Sáez, V.D.; 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. [Google Scholar] [CrossRef] [Green Version]
- Martín-Sánchez, J.; Acedo, C.; Muñoz-Pérez, M.; Pesson, B.; Marchal, O.; Morillas-Márquez, F. Infection by Leishmania infantum in Cats: Epidemiological Study in Spain. Vet. Parasitol. 2007, 145, 267–273. [Google Scholar] [CrossRef]
- Carrillo, E.; Moreno, J.; Cruz, I. What Is Responsible for a Large and Unusual Outbreak of Leishmaniasis in Madrid? Trends Parasitol. 2013, 29, 579–580. [Google Scholar] [CrossRef]
- Díaz-Sáez, V.; Merino-Espinosa, G.; Morales-Yuste, M.; Corpas-López, V.; Pratlong, F.; Morillas-Márquez, F.; Martín-Sánchez, J. High Rates of Leishmania infantum and Trypanosoma Nabiasi Infection in Wild Rabbits (Oryctolagus Cuniculus) in Sympatric and Syntrophic Conditions in an Endemic Canine Leishmaniasis Area: Epidemiological Consequences. Vet. Parasitol. 2014, 202, 119–127. [Google Scholar] [CrossRef]
- Quinnell, R.J.; Courtenay, O. Transmission, Reservoir Hosts and Control of Zoonotic Visceral Leishmaniasis. Parasitology 2009, 136, 1915–1934. [Google Scholar] [CrossRef]
- Koutinas, A.F.; Koutinas, C.K. Pathologic Mechanisms Underlying the Clinical Findings in Canine Leishmaniasis Due to Leishmania infantum/Chagasi. Vet. Pathol. 2014, 51, 527–538. [Google Scholar] [CrossRef]
- Carrillo, E.; Moreno, J. Cytokine Profiles in Canine Visceral Leishmaniasis. Vet. Immunol. Immunopathol. 2009, 128, 67–70. [Google Scholar] [CrossRef]
- Deplazes, P.; Smith, N.C.; Arnold, P.; Lutz, H.; Eckert, J. Specific IgG1 and IgG2 Antibody Responses of Dogs to Leishmania infantum and Other Parasites. Parasite Immunol. 1995, 17, 451–458. [Google Scholar] [CrossRef] [PubMed]
- Iniesta, L.; Gállego, M.; Portús, M. Immunoglobulin G and E Responses in Various Stages of Canine Leishmaniosis. Vet. Immunol. Immunopathol. 2005, 103, 77–81. [Google Scholar] [CrossRef] [PubMed]
- Day, M.J. Immunoglobulin G Subclass Distribution in Canine Leishmaniosis: A Review and Analysis of Pitfalls in Interpretation. Vet. Parasitol. 2007, 147, 2–8. [Google Scholar] [CrossRef]
- Ordeix, L.; Montserrat-Sangrà, S.; Martínez-Orellana, P.; Baxarias, M.; Solano-Gallego, L. Toll-like Receptors 2, 4 and 7, Interferon-Gamma and Interleukin 10, and Programmed Death Ligand 1 Transcripts in Skin from Dogs of Different Clinical Stages of Leishmaniosis. Parasites Vectors 2019, 12, 575. [Google Scholar] [CrossRef] [PubMed]
- Corpas-López, V.; Merino-Espinosa, G.; Acedo-Sánchez, C.; Díaz-Sáez, V.; Morillas-Márquez, F.; Martín-Sánchez, J. Hair Parasite Load as a New Biomarker for Monitoring Treatment Response in Canine Leishmaniasis. Vet. Parasitol. 2016, 223, 20–25. [Google Scholar] [CrossRef]
- Solano-Gallego, L.; Koutinas, A.; Miró, G.; Cardoso, L.; Pennisi, M.G.; Ferrer, L.; Bourdeau, P.; Oliva, G.; Baneth, G. Directions for the Diagnosis, Clinical Staging, Treatment and Prevention of Canine Leishmaniosis. Vet. Parasitol. 2009, 165, 1–18. [Google Scholar] [CrossRef]
- Rallis, T.; Day, M.J.; Saridomichelakis, M.N.; Adamama-Moraitou, K.K.; Papazoglou, L.; Fytianou, A.; Koutinas, A.F. Chronic Hepatitis Associated with Canine Leishmaniosis (Leishmania infantum): A Clinicopathological Study of 26 Cases. J. Comp. Pathol. 2005, 132, 145–152. [Google Scholar] [CrossRef]
- Reis, A.B.; Martins-Filho, O.A.; Teixeira-Carvalho, A.; Giunchetti, R.C.; Carneiro, C.M.; Mayrink, W.; Tafuri, W.L.; Corrêa-Oliveira, R. Systemic and Compartmentalized Immune Response in Canine Visceral Leishmaniasis. Vet. Immunol. Immunopathol. 2009, 128, 87–95. [Google Scholar] [CrossRef] [Green Version]
- Fontes, J.L.M.; Mesquita, B.R.; Brito, R.; Gomes, J.C.S.; de Melo, C.V.B.; Dos Santos, W.L.C. Anti-Leishmania infantum Antibody-Producing Plasma Cells in the Spleen in Canine Visceral Leishmaniasis. Pathogens 2021, 10, 1635. [Google Scholar] [CrossRef]
- Maia, C.; Campino, L. Cytokine and Phenotypic Cell Profiles of Leishmania infantum Infection in the Dog. J. Trop. Med. 2012, 2012, 541571. [Google Scholar] [CrossRef] [Green Version]
- Dos Santos, F.R.; Vieira, P.M.A.; Correa-Oliveira, R.; Giunchetti, R.C.; Carneiro, C.M.; Reis, A.B.; Malaquias, L.C.C. Qualitative and Quantitative Immunohistochemical Evaluation of INOS Expression in the Spleen of Dogs Naturally Infected with Leishmania Chagasi. Parasitol. Res. 2011, 108, 1397–1403. [Google Scholar] [CrossRef] [PubMed]
- Grano, F.G.; José, J.E.; Melo, G.D.; de Souza, M.S.; Lima, V.M.F.; Machado, G.F. Toll-like Receptors and Cytokines in the Brain and in Spleen of Dogs with Visceral Leishmaniosis. Vet. Parasitol. 2018, 253, 30–38. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kost, W.D.O.; Pereira, S.A.; Figueiredo, F.B.; Mendes Junior, A.A.V.; Madeira, M.D.F.; Miranda, L.D.F.C.; de Oliveira, R.D.V.C.; Ferreira, L.C.; Morgado, F.N.; Menezes, R.C. Frequency of Detection and Load of Amastigotes in the Pancreas of Leishmania infantum-Seropositive Dogs: Clinical Signs and Histological Changes. Parasites Vectors 2021, 14, 321. [Google Scholar] [CrossRef] [PubMed]
- Baneth, G.; Aroch, I. Canine Leishmaniasis: A Diagnostic and Clinical Challenge. Vet. J. 2008, 175, 14–15. [Google Scholar] [CrossRef]
- Foglia Manzillo, V.; Restucci, B.; Pagano, A.; Gradoni, L.; Oliva, G. Pathological Changes in the Bone Marrow of Dogs with Leishmaniosis. Vet. Rec. 2006, 158, 690–694. [Google Scholar] [CrossRef]
- Courtenay, O.; Carson, C.; Calvo-Bado, L.; Garcez, L.M.; Quinnell, R.J. Heterogeneities in Leishmania infantum Infection: Using Skin Parasite Burdens to Identify Highly Infectious Dogs. PLoS Negl. Trop. Dis. 2014, 8, e2583. [Google Scholar] [CrossRef]
- Scorza, B.M.; Mahachi, K.G.; Cox, A.C.; Toepp, A.J.; Leal-Lima, A.; Kushwaha, A.K.; Kelly, P.; Meneses, C.; Wilson, G.; Gibson-Corley, K.N.; et al. Leishmania infantum Xenodiagnosis from Vertically Infected Dogs Reveals Significant Skin Tropism. PLoS Negl. Trop. Dis. 2021, 15, e0009366. [Google Scholar] [CrossRef]
- Lima, I.S.; Solcá, M.S.; Tafuri, W.L.; Dos-Santos, W.L.C.; De Freitas, L.A.R. Assessment of Histological Liver Alterations in Dogs Naturally Infected with Leishmania infantum. Parasites Vectors 2019, 12, 487. [Google Scholar] [CrossRef]
- Rodrigues, A.; Alexandre-Pires, G.; Valério-Bolas, A.; Santos-Mateus, D.; Rafael-Fernandes, M.; Pereira, M.A.; Ligeiro, D.; Nunes, T.; Alves-Azevedo, R.; Lopes-Ventura, S.; et al. Dog Hepatocytes Are Key Effector Cells in the Liver Innate Immune Response to Leishmania infantum. Parasitology 2019, 146, 753–764. [Google Scholar] [CrossRef]
- Kaye, P.M.; Beattie, L. Lessons from Other Diseases: Granulomatous Inflammation in Leishmaniasis. Semin. Immunopathol. 2016, 38, 249–260. [Google Scholar] [CrossRef] [Green Version]
- Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2021—6ème Èdition. Available online: https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/A_summry.htm (accessed on 29 June 2022).
- Sánchez, C.A.; Sánchez, J.M.; Bernal, I.D.V.; Marín, M.C.S.; Louassini, M.; Maldonado, J.A.; Márquez, F.M. Leishmaniasis Eco-Epidemiology in the Alpujarra Region (Granada Province, Southern Spain). Int. J. Parasitol. 1996, 26, 303–310. [Google Scholar] [CrossRef] [Green Version]
- Morales-Yuste, M.; Morillas-Márquez, F.; Díaz-Sáez, V.; Barón-López, S.; Acedo-Sánchez, C.; Martín-Sánchez, J. 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. 2012, 111, 155–164. [Google Scholar] [CrossRef] [PubMed]
- Marty, P.; Izri, A.; Ozon, C.; Haas, P.; Rosenthal, E.; Del Giudice, P.; Godenir, J.; Coulibaly, E.; Gari-Toussaint, M.; Delaunay, P.; et al. A Century of Leishmaniasis in Alpes-Maritimes, France. Ann. Trop. Med. Parasitol. 2007, 101, 563–574. [Google Scholar] [CrossRef]
- Martín-Sánchez, J.; Rodríguez-Granger, J.; Morillas-Márquez, F.; Merino-Espinosa, G.; Sampedro, A.; Aliaga, L.; Corpas-López, V.; Tercedor-Sánchez, J.; Aneiros-Fernández, J.; Acedo-Sánchez, C.; et al. Leishmaniasis Due to Leishmania infantum: Integration of Human, Animal and Environmental Data through a One Health Approach. Transbound. Emerg. Dis. 2020, 67, 2423–2434. [Google Scholar] [CrossRef] [PubMed]
- Morillas, F.; Sanchez Rabasco, F.; Ocaña, J.; Martin-Sanchez, J.; Ocaña-Wihelmi, J.; Acedo, C.; Sanchiz-Marin, M.C. Leishmaniosis in the Focus of the Axarquía Region, Malaga Province, Southern Spain: A Survey of the Human, Dog, and Vector. Parasitol. Res. 1996, 82, 569–570. [Google Scholar] [CrossRef] [PubMed]
- Miró, G.; Müller, A.; Montoya, A.; Checa, R.; Marino, V.; Marino, E.; Fuster, F.; Escacena, C.; Descalzo, M.A.; Gálvez, R. Epidemiological Role of Dogs since the Human Leishmaniosis Outbreak in Madrid. Parasites Vectors 2017, 10, 209. [Google Scholar] [CrossRef] [Green Version]
- 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. Parasites Vectors 2020, 13, 204. [Google Scholar] [CrossRef] [Green Version]
- Montoya-Alonso, J.A.; Morchón, R.; Costa-Rodríguez, N.; Matos, J.I.; Falcón-Cordón, Y.; Carretón, E. Current Distribution of Selected Vector-Borne Diseases in Dogs in Spain. Front. Vet. Sci. 2020, 7, 564429. [Google Scholar] [CrossRef]
- Velez, R.; Ballart, C.; Domenech, E.; Abras, A.; Fernández-Arévalo, A.; Gómez, S.A.; Tebar, S.; Muñoz, C.; Cairó, J.; Gállego, M. Seroprevalence of Canine Leishmania infantum Infection in the Mediterranean Region and Identification of Risk Factors: The Example of North-Eastern and Pyrenean Areas of Spain. Prev. Vet. Med. 2019, 162, 67–75. [Google Scholar] [CrossRef]
- Morillas-Márquez, F.; Díaz-Sáez, V.; Morillas-Mancilla, M.J.; Corpas-López, V.; Merino-Espinosa, G.; Gijón-Robles, P.; Martín-Sánchez, J. Phlebotomine Sandflies (Diptera, Phlebotomidae) of Lanzarote Island (Canary Islands, Spain): Ecological Survey and Evaluation of the Risk of Leishmania Transmission. Acta Trop. 2017, 168, 16–20. [Google Scholar] [CrossRef]
- Cortes, S.; Vaz, Y.; Neves, R.; Maia, C.; Cardoso, L.; Campino, L. Risk Factors for Canine Leishmaniasis in an Endemic Mediterranean Region. Vet. Parasitol. 2012, 189, 189–196. [Google Scholar] [CrossRef]
- Gramiccia, M.; Scalone, A.; Di Muccio, T.; Orsini, S.; Fiorentino, E.; Gradoni, L. The Burden of Visceral Leishmaniasis in Italy from 1982 to 2012: A Retrospective Analysis of the Multi-Annual Epidemic That Occurred from 1989 to 2009. Eurosurveillance 2013, 18, 20535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lachaud, L.; Dedet, J.P.; Marty, P.; Faraut, F.; Buffet, P.; Gangneux, J.P.; Ravel, C.; Bastien, P. Working Group for the Notification of Human Leishmanioses in France Surveillance of Leishmaniases in France, 1999 to 2012. Eurosurveillance 2013, 18, 20534. [Google Scholar] [CrossRef] [Green Version]
- Morosetti, G.; Bongiorno, G.; Beran, B.; Scalone, A.; Moser, J.; Gramiccia, M.; Gradoni, L.; Maroli, M. Risk Assessment for Canine Leishmaniasis Spreading in the North of Italy. Geospat. Health 2009, 4, 115–127. [Google Scholar] [CrossRef] [PubMed]
- Ballart, C.; Barón, S.; Alcover, M.M.; Portús, M.; Gállego, M. Distribution of Phlebotomine Sand Flies (Diptera: Psychodidae) in Andorra: First Finding of P. Perniciosus and Wide Distribution of P. ariasi. Acta Trop. 2012, 122, 155–159. [Google Scholar] [CrossRef]
- Barón, S.D.; Morillas-Márquez, F.; Morales-Yuste, M.; Díaz-Sáez, V.; Irigaray, C.; Martín-Sánchez, J. 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 2011, 138, 1234–1244. [Google Scholar] [CrossRef] [PubMed]
- Martín-Sánchez, J.; Morales-Yuste, M.; Acedo-Sánchez, C.; Barón, S.; Díaz, V.; Morillas-Márquez, F. Canine Leishmaniasis in Southeastern Spain. Emerg. Infect. Dis. 2009, 15, 795–798. [Google Scholar] [CrossRef]
- Ferroglio, E.; Maroli, M.; Gastaldo, S.; Mignone, W.; Rossi, L. Canine Leishmaniasis, Italy. Emerg. Infect. Dis. 2005, 11, 1618–1620. [Google Scholar] [CrossRef]
- Campino, L.; Maia, C. Epidemiology of Leishmaniases in Portugal. Acta Med. Port. 2010, 23, 859–864. [Google Scholar]
- Díaz-Sáez, V.; Corpas-López, V.; Merino-Espinosa, G.; Morillas-Mancilla, M.J.; Abattouy, N.; Martín-Sánchez, J. Seasonal Dynamics of Phlebotomine Sand Flies and Autochthonous Transmission of Leishmania infantum in High-Altitude Ecosystems in Southern Spain. Acta Trop. 2021, 213, 105749. [Google Scholar] [CrossRef]
- Ntais, P.; Sifaki-Pistola, D.; Christodoulou, V.; Messaritakis, I.; Pratlong, F.; Poupalos, G.; Antoniou, M. Leishmaniases in Greece. Am. J. Trop. Med. Hyg. 2013, 89, 906. [Google Scholar] [CrossRef] [Green Version]
- Symeonidou, I.; Angelou, A.; Theodoridis, A.; Sioutas, G.; Papadopoulos, E. Canine Leishmaniosis in Greece: An Updated Countrywide Serological Study and Associated Risk Factors. Pathogens 2021, 10, 1129. [Google Scholar] [CrossRef]
- Vaselek, S. Canine Leishmaniasis in Balkan—A Review of Occurrence and Epidemiology. Acta Trop. 2021, 224, 106110. [Google Scholar] [CrossRef]
- Kotnik, T.; Moreno, J.; Šoba, B.; Krt, B.; Skvarc, M.; Rataj, A.V.; Bajc, M.G.; Verbic, U.R. Canine Leishmaniasis Prevalence in the Slovenian Dog Population. J. Vet. Res. 2021, 65, 161–167. [Google Scholar] [CrossRef]
- Poeppl, W.; Obwaller, A.G.; Weiler, M.; Burgmann, H.; Mooseder, G.; Lorentz, S.; Rauchenwald, F.; Aspöck, H.; Walochnik, J.; Naucke, T.J. Emergence of Sandflies (Phlebotominae) in Austria, a Central European Country. Parasitol. Res. 2013, 112, 4231–4237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oerther, S.; Jöst, H.; Heitmann, A.; Lühken, R.; Krüger, A.; Steinhausen, I.; Brinker, C.; Lorentz, S.; Marx, M.; Schmidt-Chanasit, J.; et al. Phlebotomine Sand Flies in Southwest Germany: An Update with Records in New Locations. Parasites Vectors 2020, 13, 173. [Google Scholar] [CrossRef] [Green Version]
- Naucke, T.J.; Amelung, S.; Lorentz, S. First Report of Transmission of Canine Leishmaniosis through Bite Wounds from a Naturally Infected Dog in Germany. Parasites Vectors 2016, 9, 256. [Google Scholar] [CrossRef] [Green Version]
- Naucke, T.J.; Lorentz, S. First Report of Venereal and Vertical Transmission of Canine Leishmaniosis from Naturally Infected Dogs in Germany. Parasites Vectors 2012, 5, 67. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Svobodova, V.; Svoboda, M.; Friedlaenderova, L.; Drahotsky, P.; Bohacova, E.; Baneth, G. Canine Leishmaniosis in Three Consecutive Generations of Dogs in Czech Republic. Vet. Parasitol. 2017, 237, 122–124. [Google Scholar] [CrossRef] [PubMed]
- McKenna, M.; Attipa, C.; Tasker, S.; Augusto, M. Leishmaniosis in a Dog with No Travel History Outside of the UK. Vet. Rec. 2019, 184, 441. [Google Scholar] [CrossRef] [Green Version]
- Mihalca, A.D.; Cazan, C.D.; Sulesco, T.; Dumitrache, M.O. A Historical Review on Vector Distribution and Epidemiology of Human and Animal Leishmanioses in Eastern Europe. Res. Vet. Sci. 2019, 123, 185–191. [Google Scholar] [CrossRef]
- Alonso, F.H.; Vasilatis, D.M.; Veluvolu, S.M.; Willcox, J.L.; Scorza, B.M.; Petersen, C.A.; Kol, A. Canine Leishmaniasis in Northern California—A Case Report. Vet. Clin. Pathol. 2021, 50, 71–75. [Google Scholar] [CrossRef]
- Schaut, R.G.; Robles-Murguia, M.; Juelsgaard, R.; Esch, K.J.; Bartholomay, L.C.; Ramalho-Ortigao, M.; Petersen, C.A. Vectorborne Transmission of Leishmania infantum from Hounds, United States. Emerg. Infect. Dis. 2015, 21, 2209. [Google Scholar] [CrossRef] [Green Version]
- Paltrinieri, S.; Gradoni, L.; Roura, X.; Zatelli, A.; Zini, E. Laboratory Tests for Diagnosing and Monitoring Canine Leishmaniasis. Vet. Clin. Pathol. 2016, 45, 552–578. [Google Scholar] [CrossRef] [Green Version]
- Maia, C.; Campino, L. Methods for Diagnosis of Canine Leishmaniasis and Immune Response to Infection. Vet. Parasitol. 2008, 158, 274–287. [Google Scholar] [CrossRef] [PubMed]
- Martin Sanchez, J.; Morillas Marquez, F.; Sanchiz Marin, M.C.; Acedo Sanchez, C. Isoenzymatic Characterization of the Etiologic Agent of Canine Leishmaniasis in the Granada Region of Southern Spain. Am. J. Trop. Med. Hyg. 1994, 50, 758–762. [Google Scholar] [CrossRef] [PubMed]
- Martin-Sanchez, J.; Gramiccia, M.; Di Muccio, T.; Ludovisi, A.; Morillas-Márquez, F. Isoenzymatic Polymorphism of Leishmania infantum in Southern Spain. Trans. R. Soc. Trop. Med. Hyg. 2004, 98, 228–232. [Google Scholar] [CrossRef]
- Fisa, R.; Gállego, M.; Castillejo, S.; Aisa, M.J.; Serra, T.; Riera, C.; Carrió, J.; Gállego, J.; Portús, M. Epidemiology of Canine Leishmaniosis in Catalonia (Spain) the Example of the Priorat Focus. Vet. Parasitol. 1999, 83, 87–97. [Google Scholar] [CrossRef]
- Jiménez, M.; Ferrer-Dufol, M.; Cañavate, C.; Gutiérrez-Solar, B.; Molina, R.; Lagun, F.; López-Vélez, R.; Cercenado, E.; Daudén, E.; Blazquez, J.; et al. Variability of Leishmania (Leishmania) Infantum among Stocks from Immunocompromised, Immunocompetent Patients and Dogs in Spain. FEMS Microbiol. Lett. 1995, 131, 197–204. [Google Scholar] [CrossRef]
- Martín-Sánchez, J.; Lepe, J.A.; Toledo, A.; Ubeda, J.M.; Guevara, D.C.; Morillas-Márquez, F.; Gramiccia, M. Leishmania (Leishmania) Infantum Enzymatic Variants Causing Canine Leishmaniasis in the Huelva Province (South-West Spain). Trans. R. Soc. Trop. Med. Hyg. 1999, 93, 495–496. [Google Scholar] [CrossRef]
- Lombardo, G.; Pennisi, M.G.; Lupo, T.; Migliazzo, A.; Caprì, A.; Solano-Gallego, L. Detection of Leishmania infantum DNA by Real-Time PCR in Canine Oral and Conjunctival Swabs and Comparison with Other Diagnostic Techniques. Vet. Parasitol. 2012, 184, 10–17. [Google Scholar] [CrossRef]
- Belinchón-Lorenzo, S.; Iniesta, V.; Parejo, J.C.; Fernández-Cotrina, J.; Muñoz-Madrid, R.; Soto, M.; Alonso, C.; Gómez Nieto, L.C. Detection of Leishmania infantum Kinetoplast Minicircle DNA by Real Time PCR in Hair of Dogs with Leishmaniosis. Vet. Parasitol. 2013, 192, 43–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merino-Espinosa, G.; Corpas-López, V.; Díaz-Sáez, V.; Morillas-Márquez, F.; Tercedor-Sánchez, J.; Azaña-Defez, J.M.; López-Hidalgo, J.; Aneiros-Fernández, J.; Martín-Sánchez, J. Cutaneous Leishmaniasis by Leishmania Infantum: Behind Granulomatous Lesions of Unknown Aetiology. J. Eur. Acad. Dermatol. Venereol. 2018, 32, 117–124. [Google Scholar] [CrossRef]
- Di Pietro, S.; Crinò, C.; Falcone, A.; Crupi, R.; Francaviglia, F.; Vitale, F.; Giudice, E. Parasitemia and Its Daily Variation in Canine Leishmaniasis. Parasitol. Res. 2020, 119, 3541–3548. [Google Scholar] [CrossRef]
- Pilatti, M.M.; de Almeida Ferreira, S.; de Melo, M.N.; de Andrade, A.S.R. Comparison of PCR Methods for Diagnosis of Canine Visceral Leishmaniasis in Conjunctival Swab Samples. Res. Vet. Sci. 2009, 87, 255–257. [Google Scholar] [CrossRef] [PubMed]
- Kovalenko, D.A.; Razakov, S.A.; Ponirovsky, E.N.; Warburg, A.; Nasyrova, R.M.; Ponomareva, V.I.; Fatullaeva, A.A.; Nasereddin, A.; Klement, E.; Alam, M.Z.; et al. Canine Leishmaniosis and Its Relationship to Human Visceral Leishmaniasis in Eastern Uzbekistan. Parasites Vectors 2011, 4, 58. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Francino, O.; Altet, L.; Sánchez-Robert, E.; Rodriguez, A.; Solano-Gallego, L.; Alberola, J.; Ferrer, L.; Sánchez, A.; Roura, X. Advantages of Real-Time PCR Assay for Diagnosis and Monitoring of Canine Leishmaniosis. Vet. Parasitol. 2006, 137, 214–221. [Google Scholar] [CrossRef]
- Martin-Sanchez, J.; Lopez-Lopez, M.C.; Acedo-Sanchez, C.; Castro-Fajardo, J.J.; Pineda, J.A.; Morillas-Marquez, F. Diagnosis of Infections with Leishmania infantum Using PCR-ELISA. Parasitology 2001, 122, 607–615. [Google Scholar] [CrossRef]
- Corpas-López, V.; Merino-Espinosa, G.; Acedo-Sánchez, C.; Díaz-Sáez, V.; Navarro-Moll, M.C.; Morillas-Márquez, F.; Martín-Sánchez, J. Effectiveness of the Sesquiterpene (-)-α-Bisabolol in Dogs with Naturally Acquired Canine Leishmaniosis: An Exploratory Clinical Trial. Vet. Res. Commun. 2018, 42, 121–130. [Google Scholar] [CrossRef]
- Gijón-Robles, P.; Abattouy, N.; Merino-Espinosa, G.; El Khalfaoui, N.; Morillas-Márquez, F.; Corpas-López, V.; Porcel-Rodríguez, L.; Jaaouani, N.; Díaz-Sáez, V.; Riyad, M.; et al. Risk Factors for the Expansion of Cutaneous Leishmaniasis by Leishmania Tropica: Possible Implications for Control Programmes. Transbound. Emerg. Dis. 2018, 65, 1615–1626. [Google Scholar] [CrossRef]
- Manna, L.; Gravino, A.E.; Picillo, E.; Decaro, N.; Buonavoglia, C. Leishmania DNA Quantification by Real-Time PCR in Naturally Infected Dogs Treated with Miltefosine. Ann. N. Y. Acad. Sci. 2008, 1149, 358–360. [Google Scholar] [CrossRef] [PubMed]
- Scalone, A.; De Luna, R.; Oliva, G.; Baldi, L.; Satta, G.; Vesco, G.; Mignone, W.; Turilli, C.; Mondesire, R.R.; Simpson, D.; et al. Evaluation of the Leishmania Recombinant K39 Antigen as a Diagnostic Marker for Canine Leishmaniasis and Validation of a Standardized Enzyme-Linked Immunosorbent Assay. Vet. Parasitol. 2002, 104, 275–285. [Google Scholar] [CrossRef]
- Adel, A.; Berkvens, D.; Abatih, E.; Soukehal, A.; Bianchini, J.; Saegerman, C. Evaluation of Immunofluorescence Antibody Test Used for the Diagnosis of Canine Leishmaniasis in the Mediterranean Basin: A Systematic Review and Meta-Analysis. PLoS ONE 2016, 11, e0161051. [Google Scholar] [CrossRef]
- Mettler, M.; Grimm, F.; Capelli, G.; Camp, H.; Deplazes, P. Evaluation of Enzyme-Linked Immunosorbent Assays, an Immunofluorescent-Antibody Test, and Two Rapid Tests (Immunochromatographic-Dipstick and Gel Tests) for Serological Diagnosis of Symptomatic and Asymptomatic Leishmania Infections in Dogs. J. Clin. Microbiol. 2005, 43, 5515–5519. [Google Scholar] [CrossRef] [Green Version]
- Fujimori, M.; de Almeida, A.D.B.P.F.; Barrouin-Melo, S.M.; Cortez, L.R.P.D.B.; Duthie, M.S.; Hiramoto, R.M.; de Pinho, F.A.; Reed, S.G.; Sousa, V.R.F.; Souza, N.F.; et al. Validation of ELISA with Recombinant Antigens in Serological Diagnosis of Canine Leishmania infantum Infection. Mem. Inst. Oswaldo Cruz 2021, 116. [Google Scholar] [CrossRef]
- Siqueira, W.F.; Viana, A.G.; Cunha, J.L.R.; Rosa, L.M.; Bueno, L.L.; Bartholomeu, D.C.; Cardoso, M.S.; Fujiwara, R.T. The Increased Presence of Repetitive Motifs in the KDDR-plus Recombinant Protein, a Kinesin-Derived Antigen from Leishmania infantum, Improves the Diagnostic Performance of Serological Tests for Human and Canine Visceral Leishmaniasis. PLoS Negl. Trop. Dis. 2021, 15, e0009759. [Google Scholar] [CrossRef] [PubMed]
- Noli, C.; Saridomichelakis, M.N. An Update on the Diagnosis and Treatment of Canine Leishmaniosis Caused by Leishmania infantum (Syn. L. Chagasi). Vet. J. 2014, 202, 425–435. [Google Scholar] [CrossRef]
- Baneth, G.; Shaw, S.E. Chemotherapy of Canine Leishmaniosis. Vet. Parasitol. 2002, 106, 315–324. [Google Scholar] [CrossRef]
- Marcondes, M.; Day, M.J. Current Status and Management of Canine Leishmaniasis in Latin America. Res. Vet. Sci. 2019, 123, 261–272. [Google Scholar] [CrossRef]
- Solano-Gallego, L.; Miró, G.; Koutinas, A.; Cardoso, L.; Pennisi, M.G.; Ferrer, L.; Bourdeau, P.; Oliva, G.; Baneth, G. LeishVet Guidelines for the Practical Management of Canine Leishmaniosis. Parasites Vectors 2011, 4, 86. [Google Scholar] [CrossRef] [Green Version]
- World Health Organozation Handbook: Non-Clínical Safety Testing. WHO Drug Inf. 2004, 18, 125.
- Noli, C.; Auxilia, S.T. Treatment of Canine Old World Visceral Leishmaniasis: A systematic review. Vet. Dermatol. 2005, 16, 213–232. [Google Scholar] [CrossRef]
- Torres, M.; Bardagí, M.; Roura, X.; Zanna, G.; Ravera, I.; Ferrer, L. Long Term Follow-up of Dogs Diagnosed with Leishmaniosis (Clinical Stage II) and Treated with Meglumine Antimoniate and Allopurinol. Vet. J. 2011, 188, 346–351. [Google Scholar] [CrossRef] [PubMed]
- Yasur-Landau, D.; Jaffe, C.L.; David, L.; Baneth, G. Allopurinol Resistance in Leishmania infantum from Dogs with Disease Relapse. PLoS Negl. Trop. Dis. 2016, 10, e0004341. [Google Scholar] [CrossRef]
- Yasur-Landau, D.; Jaffe, C.L.; Doron-Faigenboim, A.; David, L.; Baneth, G. Induction of Allopurinol Resistance in Leishmania infantum Isolated from Dogs. PLoS Negl. Trop. Dis. 2017, 11, e0005910. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yasur-Landau, D.; Jaffe, C.L.; David, L.; Doron-Faigenboim, A.; Baneth, G. Resistance of Leishmania infantum to Allopurinol Is Associated with Chromosome and Gene Copy Number Variations Including Decrease in the S-Adenosylmethionine Synthetase (METK) Gene Copy Number. Int. J. Parasitol. Drugs Drug Resist. 2018, 8, 403–410. [Google Scholar] [CrossRef]
- 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, 613–620. [Google Scholar] [CrossRef] [PubMed]
- Gómez-Pérez, V.; García-Hernández, R.; Corpas-López, V.; Tomás, A.M.; Martín-Sánchez, J.; Castanys, S.; Gamarro, F. Resistance to Antimonials in L. infantum from a Dog with Canine Leishmaniasis. Int. J. Parasitol. Drugs Drug Resist. 2016, 10, e0004341. [Google Scholar]
- Eddaikra, N.; Ait-Oudhia, K.; Kherrachi, I.; Oury, B.; Moulti-Mati, F.; Benikhlef, R.; Harrat, Z.; Sereno, D. Antimony Susceptibility of Leishmania Isolates Collected over a 30-Year Period in Algeria. PLoS Negl. Trop. Dis. 2018, 12, e0006310. [Google Scholar] [CrossRef] [Green Version]
- Miret, J.A.; Moreno, J.; Nieto, J.; Carter, K.C.; Mullen, A.B.; Ambros, L.; Rodríguez, C.; San Andrés, M.I.; González, F. Antileishmanial Efficacy and Tolerability of Combined Treatment with Non-Ionic Surfactant Vesicle Formulations of Sodium Stibogluconate and Paromomycin in Dogs. Exp. Parasitol. 2021, 220, 108033. [Google Scholar] [CrossRef]
- Ortega, V.; Radaic, A.; de Jesus, M.B.; de Paula, E.; Giorgio, S. Improved Efficacy of Meglumine Antimoniate Incorporated in Anionic Liposomes against Leishmania infantum Infecting Canine Macrophages. J. Pharm. Pharmacol. 2022, 74, 896–904. [Google Scholar] [CrossRef] [PubMed]
- Dos Santos, C.C.P.; Ramos, G.S.; De Paula, R.C.; Faria, K.F.; Moreira, P.O.L.; Pereira, R.A.; Melo, M.N.; Tafuri, W.L.; Demicheli, C.; Ribeiro, R.R.; et al. Therapeutic Efficacy of a Mixed Formulation of Conventional and PEGylated Liposomes Containing Meglumine Antimoniate, Combined with Allopurinol, in Dogs Naturally Infected with Leishmania infantum. Antimicrob. Agents Chemother. 2020, 64, e00234-20. [Google Scholar] [CrossRef] [PubMed]
- Corpas-López, V.; Tabraue-Chávez, M.; Sixto-Lopez, Y.; Panadero-Fajardo, S.; Alves de Lima Franco, F.; Dominguez-Seglar, J.F.; Morillas-Márquez, F.; Franco-Montalban, F.; Díaz-Gavilán, M.; Correa-Basurto, J.; et al. O-Alkyl Hydroxamates Display Potent and Selective Antileishmanial Activity. J. Med. Chem. 2020, 63, 5734–5751. [Google Scholar] [CrossRef]
- Bhattacharya, S.K.; Sinha, P.K.; Sundar, S.; Thakur, C.P.; Jha, T.K.; Pandey, K.; Das, V.R.; Kumar, N.; Lal, C.; Verma, N.; et al. Phase 4 Trial of Miltefosine for the Treatment of Indian Visceral Leishmaniasis. J. Infect. Dis. 2007, 196, 591–598. [Google Scholar] [CrossRef] [Green Version]
- Dorlo, T.P.C.; Balasegaram, M.; Beijnen, J.H.; de Vries, P.J. Miltefosine: A Review of Its Pharmacology and Therapeutic Efficacy in the Treatment of Leishmaniasis. J. Antimicrob. Chemother. 2012, 67, 2576–2597. [Google Scholar] [CrossRef]
- Manna, L.; Vitale, F.; Reale, S.; Picillo, E.; Neglia, G.; Vescio, F.; Gravino, A.E. Study of Efficacy of Miltefosine and Allopurinol in Dogs with Leishmaniosis. Vet. J. 2009, 182, 441–445. [Google Scholar] [CrossRef]
- Andrade, H.M.; Toledo, V.P.C.P.; Pinheiro, M.B.; Guimarães, T.M.P.D.; Oliveira, N.C.; Castro, J.A.; Silva, R.N.; Amorim, A.C.; Brandão, R.M.S.S.; Yoko, M.; et al. Evaluation of Miltefosine for the Treatment of Dogs Naturally Infected with L. infantum (=L. chagasi) in Brazil. Vet. Parasitol. 2011, 181, 83–90. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miró, G.; Oliva, G.; Cruz, I.; Cañavate, C.; Mortarino, M.; Vischer, C.; Bianciardi, P. Multicentric, Controlled Clinical Study to Evaluate Effectiveness and Safety of Miltefosine and Allopurinol for Canine Leishmaniosis. Vet. Dermatol. 2009, 20, 397–404. [Google Scholar] [CrossRef] [PubMed]
- Manna, L.; Corso, R.; Galiero, G.; Cerrone, A.; Muzj, P.; Gravino, A.E. Long-Term Follow-up of Dogs with Leishmaniosis Treated with Meglumine Antimoniate plus Allopurinol versus Miltefosine plus Allopurinol. Parasites Vectors 2015, 8, 289. [Google Scholar] [CrossRef] [Green Version]
- Iarussi, F.; Paradies, P.; Foglia Manzillo, V.; Gizzarelli, M.; Caratozzolo, M.F.; Navarro, C.; Greco, B.; Rubino, G.T.R.; Oliva, G.; Sasanelli, M. Comparison of Two Dosing Regimens of Miltefosine, Both in Combination with Allopurinol, on Clinical and Parasitological Findings of Dogs with Leishmaniosis: A Pilot Study. Front. Vet. Sci. 2020, 7, 577395. [Google Scholar] [CrossRef]
- de Lima Ruy Dias, A.F.; da Cruz Boa Sorte Ayres, E.; Maruyama, F.H.; Monteiro, B.R.G.; de Freitas, M.S.; do Bom Parto Ferreira de Almeida, A.; Mendonça, A.J.; Sousa, V.R.F. Monitoring of Serum and Urinary Biomarkers during Treatment of Canine Visceral Leishmaniasis. Vet. World 2020, 13, 1620. [Google Scholar] [CrossRef] [PubMed]
- Dias, Á.F.D.L.R.; Ayres, E.D.C.B.S.; de Oliveira Martins, D.T.; Maruyama, F.H.; de Oliveira, R.G.; de Carvalho, M.R.; Almeida, A.D.B.P.F.D.; Teixeira, A.L.D.S.; Mendonça, A.J.; Sousa, V.R.F. Comparative Study of the Use of Miltefosine, Miltefosine plus Allopurinol, and Allopurinol in Dogs with Visceral Leishmaniasis. Exp. Parasitol. 2020, 217, 107947. [Google Scholar] [CrossRef] [PubMed]
- Daza González, M.A.; Fragío Arnold, C.; Fermín Rodríguez, M.; Checa, R.; Montoya, A.; Portero Fuentes, M.; Rupérez Noguer, C.; Martínez Subiela, S.; Cerón, J.J.; Miró, G. Effect of Two Treatments on Changes in Serum Acute Phase Protein Concentrations in Dogs with Clinical Leishmaniosis. Vet. J. 2019, 245, 22–28. [Google Scholar] [CrossRef]
- Dos Santos Nogueira, F.; Avino, V.C.; Galvis-Ovallos, F.; Pereira-Chioccola, V.L.; Moreira, M.A.B.; Romariz, A.P.P.L.; Molla, L.M.; Menz, I. Use of Miltefosine to Treat Canine Visceral Leishmaniasis Caused by Leishmania infantum in Brazil. Parasites Vectors 2019, 12, 79. [Google Scholar] [CrossRef]
- Santos, M.F.; Alexandre-Pires, G.; Pereira, M.A.; Marques, C.S.; Gomes, J.; Correia, J.; Duarte, A.; Gomes, L.; Rodrigues, A.V.; Basso, A.; et al. Meglumine Antimoniate and Miltefosine Combined with Allopurinol Sustain Pro-Inflammatory Immune Environments during Canine Leishmaniosis Treatment. Front. Vet. Sci. 2019, 6, 362. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Proverbio, D.; Spada, E.; de Giorgi, G.B.; Perego, R. Proteinuria Reduction after Treatment with Miltefosine and Allopurinol in Dogs Naturally Infected with Leishmaniasis. Vet. World 2016, 9, 904. [Google Scholar] [CrossRef] [Green Version]
- Gonçalves, G.; Campos, M.P.; Gonçalves, A.S.; Medeiros, L.C.S.; Figueiredo, F.B. Increased Leishmania infantum Resistance to Miltefosine and Amphotericin B after Treatment of a Dog with Miltefosine and Allopurinol. Parasites Vectors 2021, 14, 599. [Google Scholar] [CrossRef]
- Hirokawa, G.; Kaji, H.; Kaji, A. Inhibition of Antiassociation Activity of Translation Initiation Factor 3 by Paromomycin. Antimicrob. Agents Chemother. 2007, 51, 175–180. [Google Scholar] [CrossRef] [Green Version]
- Kasabalis, D.; Chatzis, M.K.; Apostolidis, K.; Xenoulis, P.G.; Buono, A.; Petanides, T.; Leontides, L.S.; Polizopoulou, Z.S.; Steiner, J.M.; Suchodolski, J.S.; et al. Evaluation of Nephrotoxicity and Ototoxicity of Aminosidine (Paromomycin)-Allopurinol Combination in Dogs with Leishmaniosis Due to Leishmania infantum: A Randomized, Blinded, Controlled Study. Exp. Parasitol. 2019, 206, 107768. [Google Scholar] [CrossRef]
- Kasabalis, D.; Chatzis, M.K.; Apostolidis, K.; Petanides, T.; Athanasiou, L.V.; Xenoulis, P.G.; Mataragka, A.; Ikonomopoulos, J.; Leontides, L.S.; Saridomichelakis, M.N. A Randomized, Blinded, Controlled Clinical Trial Comparing the Efficacy of Aminosidine (Paromomycin)-Allopurinol Combination with the Efficacy of Meglumine Antimoniate-Allopurinol Combination for the Treatment of Canine Leishmaniosis Due to Leishmania infantum. Exp. Parasitol. 2020, 214, 107903. [Google Scholar] [CrossRef]
- Athanasiou, L.V.; Saridomichelakis, M.N.; Kontos, V.I.; Spanakos, G.; Rallis, T.S. Treatment of Canine Leishmaniosis with Aminosidine at an Optimized Dosage Regimen: A Pilot Open Clinical Trial. Vet. Parasitol. 2013, 192, 91–97. [Google Scholar] [CrossRef] [PubMed]
- Roberts, C.W.; McLeod, R.; Rice, D.W.; Ginger, M.; Chance, M.L.; Goad, L.J. Fatty Acid and Sterol Metabolism: Potential Antimicrobial Targets in Apicomplexan and Trypanosomatid Parasitic Protozoa. Mol. Biochem. Parasitol. 2003, 126, 129–142. [Google Scholar] [CrossRef]
- Freitas-Junior, L.H.; Chatelain, E.; Kim, H.A.; Siqueira-Neto, J.L. Visceral Leishmaniasis Treatment: What Do We Have, What Do We Need and How to Deliver It? Int. J. Parasitol. Drugs Drug Resist. 2012, 2, 11–19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lamothe, J. Activity of Amphotericin B in Lipid Emulsion in the Initial Treatment of Canine Leishmaniasis. J. Small Anim. Pract. 2001, 42, 170–175. [Google Scholar] [CrossRef] [PubMed]
- Oliva, G.; Gradoni, L.; Ciaramella, P.; Luna, R.D.; Cortese, L.; Orsini, S.; Davidson, R.N.; Persechino, A. Activity of Liposomal Amphotericin B (AmBisome) in Dogs Naturally Infected with Leishmania infantum. J. Antimicrob. Chemother. 1995, 36, 1013–1019. [Google Scholar] [CrossRef]
- Hernández, L.; Bolás-Fernández, F.; Montoya, A.; Checa, R.; Dado, D.; Gálvez, R.; Serrano, D.R.; Torrado, J.J.; Otranto, D.; Latrofa, M.S.; et al. Unresponsiveness of Experimental Canine Leishmaniosis to a New Amphotericin B Formulation. Adv. Pharm. 2015, 2015, 160208. [Google Scholar] [CrossRef]
- Rougier, S.; Vouldoukis, I.; Fournel, S.; Pérès, S.; Woehrlé, F. Efficacy of Different Treatment Regimens of Marbofloxacin in Canine Visceral Leishmaniosis: A Pilot Study. Vet. Parasitol. 2008, 153, 244–254. [Google Scholar] [CrossRef]
- Rougier, S.; Hasseine, L.; Delaunay, P.; Michel, G.; Marty, P. One-Year Clinical and Parasitological Follow-up of Dogs Treated with Marbofloxacin for Canine Leishmaniosis. Vet. Parasitol. 2012, 186, 245–253. [Google Scholar] [CrossRef]
- Pineda, C.; Aguilera-Tejero, E.; Morales, M.C.; Belinchon-Lorenzo, S.; Gomez-Nieto, L.C.; Garcia, P.; Martinez-Moreno, J.M.; Rodriguez-Ortiz, M.E.; Lopez, I. Treatment of Canine Leishmaniasis with Marbofloxacin in Dogs with Renal Disease. PLoS ONE 2017, 12, e0185981. [Google Scholar] [CrossRef] [Green Version]
- Gómez-Ochoa, P.; Castillo, J.A.; Gascón, M.; Zarate, J.J.; Alvarez, F.; Couto, C.G. Use of Domperidone in the Treatment of Canine Visceral Leishmaniasis: A Clinical Trial. Vet. J. 2009, 179, 259–263. [Google Scholar] [CrossRef]
- Sabaté, D.; Llinás, J.; Homedes, J.; Sust, M.; Ferrer, L. 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. [Google Scholar] [CrossRef]
- Wylie, C.E.; Carbonell-Antoñanzas, M.; Aiassa, E.; Dhollander, S.; Zagmutt, F.J.; Brodbelt, D.C.; Solano-Gallego, L. A Systematic Review of the Efficacy of Prophylactic Control Measures for Naturally Occurring Canine Leishmaniosis. Part II: Topically Applied Insecticide Treatments and Prophylactic Medications. Prev. Vet. Med. 2014, 117, 19–27. [Google Scholar] [CrossRef]
- Fernandez, M.; Tabar, M.D.; Arcas, A.; Mateu, C.; Homedes, J.; Roura, X. Comparison of Efficacy and Safety of Preventive Measures Used against Canine Leishmaniasis in Southern European Countries: Longitudinal Retrospective Study in 1647 Client-Owned Dogs (2012–2016). Vet. Parasitol. 2018, 263, 10–17. [Google Scholar] [CrossRef]
- Rodriguez-Cortes, A.; Martori, C.; Martinez-Florez, A.; Clop, A.; Amills, M.; Kubejko, J.; Llull, J.; Nadal, J.M.; Alberola, J. Canine Leishmaniasis Progression Is Associated with Vitamin D Deficiency. Sci. Rep. 2017, 7, 3346. [Google Scholar] [CrossRef] [Green Version]
- Martori, C.; Velez, R.; Gállego, M.; Mesa, I.; Ferreira, R.; Alberola, J.; Rodríguez-Cortés, A. Vitamin d and Leishmaniasis: Neither Seasonal nor Risk Factor in Canine Host but Potential Adjuvant Treatment through Cbd103 Expression. PLoS Negl. Trop. Dis. 2021, 15, e0009681. [Google Scholar] [CrossRef] [PubMed]
- Roura, X.; Fondati, A.; Lubas, G.; Gradoni, L.; Maroli, M.; Oliva, G.; Paltrinieri, S.; Zatelli, A.; Zini, E. Prognosis and Monitoring of Leishmaniasis in Dogs: A Working Group Report. Vet. J. 2013, 198, 43–47. [Google Scholar] [CrossRef] [PubMed]
- Martínez, V.; Quilez, J.; Sanchez, A.; Roura, X.; Francino, O.; Altet, L. Canine Leishmaniasis: The Key Points for QPCR Result Interpretation. Parasites Vectors 2011, 4, 57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oliva, G.; Roura, X.; Crotti, A.; Maroli, M.; Castagnaro, M.; Gradoni, L.; Lubas, G.; Paltrinieri, S.; Zatelli, A.; Zini, E. Guidelines for Treatment of Leishmaniasis in Dogs. J. Am. Vet. Med. Assoc. 2010, 236, 1192–1198. [Google Scholar] [CrossRef]
- Medkour, H.; Bitam, I.; Laidoudi, Y.; Lafri, I.; Lounas, A.; Hamidat, H.K.; Mekroud, A.; Varloud, M.; Davoust, B.; Mediannikov, O. Potential of Artesunate in the Treatment of Visceral Leishmaniasis in Dogs Naturally Infected by Leishmania infantum: Efficacy Evidence from a Randomized Field Trial. PLoS Negl. Trop. Dis. 2020, 14, e0008947. [Google Scholar] [CrossRef]
- Segarra, S.; Miró, G.; Montoya, A.; Pardo-Marín, L.; Boqué, N.; Ferrer, L.; Cerón, J. Randomized, Allopurinol-Controlled Trial of the Effects of Dietary Nucleotides and Active Hexose Correlated Compound in the Treatment of Canine Leishmaniosis. Vet. Parasitol. 2017, 239, 50–56. [Google Scholar] [CrossRef] [PubMed]
- de Oliveira Cardoso, J.M.; de Brito, R.C.F.; Mathias, F.A.S.; Reis, L.E.S.; Vieira, J.F.P.; Ostolin, T.L.V.D.P.; de Andrade, H.M.; Ramos, G.S.; Frézard, F.; de Oliveira Aguiar-Soares, R.D.; et al. Comparative Evaluation of Meglumine Antimoniate Encapsulated in a Mixture of Conventional and PEGylated Liposomes and Immunotherapy Using an Anti-Canine IL-10 Receptor-Blocking Monoclonal Antibody on Canine Visceral Leishmaniasis. Mol. Immunol. 2022, 141, 70–78. [Google Scholar] [CrossRef] [PubMed]
- Apostolopoulos, N.; Mitropoulou, A.; Thom, N.; Moritz, A. Update on Therapy and Prevention of Canine Leishmaniasis. Tierarztl. Praxis. Ausg. K Kleintiere/Heimtiere 2018, 46, 315–322. [Google Scholar] [CrossRef]
- Baxarias, M.; Homedes, J.; Mateu, C.; Attipa, C.; Solano-Gallego, L. Use of Preventive Measures and Serological Screening Tools for Leishmania infantum Infection in Dogs from Europe. Parasites Vectors 2022, 15, 134. [Google Scholar] [CrossRef] [PubMed]
- de Almeida Rocha, D.; da Costa, L.M.; Pessoa, G.D.Á.C.; Obara, M.T. Methods for Detecting Insecticide Resistance in Sand Flies: A Systematic Review. Acta Trop. 2021, 213, 105747. [Google Scholar] [CrossRef] [PubMed]
- Molina, R.; Jiménez, M. Assessing the Susceptibility to Permethrin and Deltamethrin of Two Laboratory Strains of Phlebotomus Perniciosus from Madrid Region, Spain. Acta Trop. 2022, 231, 106453. [Google Scholar] [CrossRef]
- Chaskopoulou, A.; Miaoulis, M.; Kashefi, J. Ground Ultra Low Volume (ULV) Space Spray Applications for the Control of Wild Sand Fly Populations (Psychodidae: Phlebotominae) in Europe. Acta Trop. 2018, 182, 54–59. [Google Scholar] [CrossRef]
- Karakus, M.; Gocmen, B.; özbel, Y. Insecticide Susceptibility Status of Wild-Caught Sand Fly Populations Collected from Two Leishmaniasis Endemic Areas in Western Turkey. J. Arthropod. Borne. Dis. 2017, 11, 86. [Google Scholar]
- Pugliese, M.; Gaglio, G.; Passantino, A.; Brianti, E.; Napoli, E. Natural Products against Sand Fly Vectors of Leishmaniosis: A Systematic Review. Vet. Sci. 2021, 8, 150. [Google Scholar] [CrossRef] [PubMed]
- Montoya, A.; Checa, R.; Marino, V.; Gálvez, R.; Portero, M.; De Mari, K.; Navarro, C.; Miró, G. Antibodies Elicited by the CaniLeish® Vaccine: Long-Term Clinical Follow-up Study of Dogs in Spain. Parasitol. Res. 2021, 120, 1471–1479. [Google Scholar] [CrossRef]
- Dantas-Torres, F.; dos Santos Nogueira, F.; Menz, I.; Tabanez, P.; da Silva, S.M.; Ribeiro, V.M.; Miró, G.; Cardoso, L.; Petersen, C.; Baneth, G.; et al. Vaccination against Canine Leishmaniasis in Brazil. Int. J. Parasitol. 2020, 50, 171–176. [Google Scholar] [CrossRef]
- Velez, R.; Domenech, E.; Cairó, J.; Gállego, M. The Impact of Canine Leishmaniosis Vaccination with Canileish® in Leishmania infantum Infection Seroprevalence Studies. Acta Trop. 2020, 202, 105259. [Google Scholar] [CrossRef]
- Travi, B.L.; Cordeiro-da-Silva, A.; Dantas-Torres, F.; Miró, G. Canine Visceral Leishmaniasis: Diagnosis and Management of the Reservoir Living among Us. PLoS Negl. Trop. Dis. 2018, 12, e0006082. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grimaldi, G.; Teva, A.; Dos-Santos, C.B.; Santos, F.N.; Pinto, I.D.S.; Fux, B.; Leite, G.R.; Falqueto, A. Field Trial of Efficacy of the Leish-Tec® Vaccine against Canine Leishmaniasis Caused by Leishmania infantum in an Endemic Area with High Transmission Rates. PLoS ONE 2017, 12, e0185438. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gradoni, L. Canine Leishmania Vaccines: Still a Long Way to Go. Vet. Parasitol. 2015, 208, 94–100. [Google Scholar] [CrossRef] [PubMed]
- Bongiorno, G.; Paparcone, R.; Manzillo, V.F.; Oliva, G.; Cuisinier, A.M.; Gradoni, L. 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, 691–695. [Google Scholar] [CrossRef] [Green Version]
- Palatnik-de-Sousa, C.B. Vaccines for Canine Leishmaniasis. Front. Immunol. 2012, 3, 69. [Google Scholar] [CrossRef] [Green Version]
- Moreno, J. Assessment of Vaccine-Induced Immunity Against Canine Visceral Leishmaniasis. Front. Vet. Sci. 2019, 6, 168. [Google Scholar] [CrossRef]
- Maia, C.; Campino, L. Biomarkers Associated with Leishmania infantum Exposure, Infection, and Disease in Dogs. Front. Cell. Infect. Microbiol. 2018, 8, 302. [Google Scholar] [CrossRef]
- Toepp, A.J.; Petersen, C.A. The Balancing Act: Immunology of Leishmaniosis. Res. Vet. Sci. 2020, 130, 19–25. [Google Scholar] [CrossRef]
- Foroughi-Parvar, F.; Hatam, G. Vaccines for Canine Leishmaniasis. Adv. Prev. Med. 2014, 2014, 569193. [Google Scholar] [CrossRef]
- Kedzierski, L.; Zhu, Y.; Handman, E. Leishmania Vaccines: Progress and Problems. Parasitology 2006, 133 (Suppl. 2), S87–S112. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gonçalves, A.A.M.; Leite, J.C.; Resende, L.A.; Mariano, R.M.D.S.; Silveira, P.; Melo-Júnior, O.A.D.O.; Ribeiro, H.S.; de Oliveira, D.S.; Soares, D.F.; Santos, T.A.P.; et al. An Overview of Immunotherapeutic Approaches against Canine Visceral Leishmaniasis: What Has Been Tested on Dogs and a New Perspective on Improving Treatment Efficacy. Front. Cell. Infect. Microbiol. 2019, 9, 427. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Velez, R.; Gállego, M. Commercially Approved Vaccines for Canine Leishmaniosis: A Review of Available Data on Their Safety and Efficacy. Trop. Med. Int. Health 2020, 25, 540–557. [Google Scholar] [CrossRef] [Green Version]
- Calzetta, L.; Pistocchini, E.; Ritondo, B.L.; Roncada, P.; Palma, E.; di Cave, D.; Mattei, M.; Britti, D. Immunoprophylaxis Pharmacotherapy against Canine Leishmaniosis: A Systematic Review and Meta-Analysis on the Efficacy of Vaccines Approved in European Union. Vaccine 2020, 38, 6695–6703. [Google Scholar] [CrossRef]
- Martin, V.; Vouldoukis, I.; Moreno, J.; McGahie, D.; Gueguen, S.; Cuisinier, A.M. The Protective Immune Response Produced in Dogs after Primary Vaccination with the LiESP/QA-21 Vaccine (CaniLeish®) Remains Effective against an Experimental Challenge One Year Later. Vet. Res. 2014, 45, 69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bourdoiseau, G.; Hugnet, C.; Gonçalves, R.B.; Vézilier, F.; Petit-Didier, E.; Papierok, G.; Lemesre, J.L. Effective Humoral and Cellular Immunoprotective Responses in Li ESAp-MDP Vaccinated Protected Dogs. Vet. Immunol. Immunopathol. 2009, 128, 71–78. [Google Scholar] [CrossRef]
- Reguera, R.M.; Morán, M.; Pérez-Pertejo, Y.; García-Estrada, C.; Balaña-Fouce, R. Current Status on Prevention and Treatment of Canine Leishmaniasis. Vet. Parasitol. 2016, 227, 98–114. [Google Scholar] [CrossRef]
- Martín-Martín, I.; Molina, R.; Rohoušová, I.; Drahota, J.; Volf, P.; Jiménez, M. High Levels of Anti-Phlebotomus Perniciosus Saliva Antibodies in Different Vertebrate Hosts from the Re-Emerging Leishmaniosis Focus in Madrid, Spain. Vet. Parasitol. 2014, 202, 207–216. [Google Scholar] [CrossRef]
Tissue/Sample | Sensitivity (%) | Specificity (%) | Reference |
---|---|---|---|
Hair | 99.0, 69.2, 84.6 | 99.0, 100, NA | [15,73,74] |
Skin | 74.4 | NA | [75] |
Conjunctival swab | 43.8, 53.8 | 85.7 | [73,76] |
Oral swab | 15.6 | 93.3 | [72] |
Lymph node | 43.8, 100.0, 100.0, 77.2 | 82.3, 100, NA, NA | [15,73,74,76] |
Bone marrow | 72.7 | NA | [15] |
Peripheral blood | 11.3, 61.5, 30.8, 77.2 | 96.6, 100, NA, NA | [15,73,74,76] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Morales-Yuste, M.; Martín-Sánchez, J.; Corpas-Lopez, V. Canine Leishmaniasis: Update on Epidemiology, Diagnosis, Treatment, and Prevention. Vet. Sci. 2022, 9, 387. https://doi.org/10.3390/vetsci9080387
Morales-Yuste M, Martín-Sánchez J, Corpas-Lopez V. Canine Leishmaniasis: Update on Epidemiology, Diagnosis, Treatment, and Prevention. Veterinary Sciences. 2022; 9(8):387. https://doi.org/10.3390/vetsci9080387
Chicago/Turabian StyleMorales-Yuste, Manuel, Joaquina Martín-Sánchez, and Victoriano Corpas-Lopez. 2022. "Canine Leishmaniasis: Update on Epidemiology, Diagnosis, Treatment, and Prevention" Veterinary Sciences 9, no. 8: 387. https://doi.org/10.3390/vetsci9080387