High prevalence of Leishmania spp. in dogs from Central West Colombia
DOI:
https://doi.org/10.12834/VetIt.2632.16820.2Keywords:
Canine leishmaniasis, canine, hsp70, ITS-1, risk factorsAbstract
Leishmaniasis is a widespread disease caused by species of the genus Leishmania. In Colombia, this zoonosis is endemic in rural areas with a high prevalence in the departments of Antioquia, Santander, Meta, Tolima and Nariño. Dogs are the most important domestic reservoirs of the pathogen, given the epidemiological importance of dogs in the control of leishmaniasis is needed to determine the prevalence of Leishmania spp. in canine population of the rural area of Ibagué and to identify potential risk factors related to the presence of this parasite. A cross-sectional study was carried out in 173 dogs from the rural area of Ibagué. Leishmania spp. was detected by amplifying the Internal Transcribed Spacer (ITS-1) and two regions of the hsp70 gene through PCR. Factor associations were calculated through the Chisquare and odds ratio. Prevalence of Leishmania spp. infection in dogs was of 91.33% (158/173), where 36.71% (58/158) of the Leishmania spp. positive dogs showed one or more clinical signs of canine leishmaniasis and 63.29% (100/158) of the dogs were asymptomatic. Factors associated with the presence of the parasite did not show significance. In addition, hsp70D-PCR was proved to be highly efficient for the detection of Leishmania spp.
References
Akhoundi M., Kuhls K., Cannet A., Votýpka J., Marty P., Delaunay P. & Sereno, D. 2016. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl Trop Dis, 10(3), e0004349.
Albuquerque A., Campino L. & Cardoso L. 2017. Evaluation of four molecular methods to detect Leishmania infection in dogs. Parasit Vectors, 10, 57.
Almeida A., Mendonça A. & Sousa V. 2010. Prevalência e epidemiologia da leishmaniose visceral em cães e humanos, na cidade de Cuiabá, Mato Grosso, Brasil. Cienc Rural, 40, 1610-1615.
Alvar J., Cañavate C., Molina R., Moreno J. & Nieto, J. 2004. Canine leishmaniasis. Adv Parasitol , 57, 1-88.
Alvar J., Vélez I. D., 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.
Alves W. A. & Bevilacqua P. D. 2004. Reflexões sobre a qualidade do diagnóstico da leishmaniose visceral canina em inquéritos epidemiológicos: o caso da epidemia de Belo Horizonte, Minas Gerais, Brasil, 1993-1997. Cad Saude Publica, 20(1), 259-265.
Bejarano E. E. 2006. Lista actualizada de los psicódidos (Diptera: psychodidae) de Colombia. Folia Entomológica Mexicana, 45(1),47-56.
Bejarano E. E., Sierra D. & Vélez I. D. 2003. Novedades en la distribución geográfica del grupo verrucarum (Diptera: Psychodidae) en Colombia. Biomédica , 23, 341-350.
Belo V. S., Struchiner C. J., Werneck G. L., Barbosa D. S., de Oliveira R. B., Neto R. G. & da Silva E. S. 2013a. A systematic review and meta-analysis of the factors associated with Leishmania infantum infection in dogs in Brazil. Vet Parasitol , 195(1-2), 1–13.
Belo V. S., Werneck G. L., Barbosa D. S., Simões T. C., Nascimento B W. L., da Silva E. S. & Struchiner C. J. 2013b. Factors Associated with Visceral Leishmaniasis in the Americas: A Systematic Review and Meta-Analysis. PLoS Negl Trop Dis, 7(4), e2182.
Berrahal F., Mary C., Roze M., Berenger A., Escoffier K., Lamoroux D. & Dunan S. 1996. Canine leishmaniasis: identification of asymptomatic carriers by polymerase chain reaction and immunoblotting. Am J Trop Med Hyg, 55, 273–277. https://doi.org/10.4269/ajtmh.1996.55.273
Cárdenas R., Romo G., Santamaría E., Bello F. & Ferro, C. 1999. Lutzomyia longiflocosa (Diptera: Psychodidae) posible vector en el foco de leishmaniasis cutánea del municipio de Planadas, zona cafetera del Tolima. Biomédica, 19, 239-244.
Carvalho D., Oliveira T. M. F. S., Baldani C. D. & Machado R. Z. 2009. An enzyme-linked immunosorbent assay (ELISA) for the detection of IgM antibodies against Leishmania chagasi in dogs. Pesquisa Veterinária Brasileira, 29, 120-124.
Cavalcanti A., Lobo R., Cupolillo E., Bustamante F. & Porrozzi R. 2012. Canine cutaneous leishmaniasis caused by neotropical Leishmania infantum despite of systemic disease: A case report. Parasitol Int, 61(4), 738-740.
Centro de información municipal para planeación participativa (CIMPP). 2021. Demografía: Dane 1938-2018. http://cimpp.ibague.gov.co/demografia/
Chinchilla E. & Vanessa M. 2010. Estudio serológico y molecular de Leishmania spp. en cánidos domésticos de dos cantones del municipio de San Ildefonso, Departamento de San Vicente, El Salvador [Doctoral dissertation]. Universidad de El Salvador. https://catalogosiidca.csuca.org/Record/UES.111736
Contreras M. A., Vivero R. J., Bejarano E. E., Carrillo L. M. & Vélez I. D. 2012. Nuevos registros de flebotomíneos (Diptera: Psychodidae) en el área de influencia del río Amoyá en Chaparral, Tolima. Biomédica, 32(2), 263-268.
Corporación autónoma regional del Tolima (CORTOLIMA). 2002. Agenda ambiental del municipio de Ibagué. https://www.cortolima.gov.co/
Coura-Vital W., Marques M. J., Veloso V. M., Roatt B. M., de Oliveira Aguiar-Soares R. D., Reis L. E. S., Leoncio-Braga S., Franco-Morais M. H., Barbosa-Reis A. & Carneiro M. 2011. Prevalence and factors associated with Leishmania infantum infection of dogs from an urban area of Brazil as identified by molecular methods. PLoS Negl Trop Dis, 5(8), e1291
Curi N. H., Paschoal A. M., Massara R. L., Marcelino A. P., Ribeiro A. A., Passamani M., Demétrio G. R., Chiarello A. G. & Carvalho L. H. 2014. Factors Associated with the Seroprevalence of Leishmaniasis in Dogs Living around Atlantic Forest Fragments. PLoS ONE, 9(8), e104003.
Dabirzadeh M., Hashemi M. & Maroufi Y. 2016. Study of Genetic Variation of Leishmania major Based on Internal Transcribed Spacer 1 (ITS1) in Chabahar, Iran. Jundishapur J Microbio, 9(6), e33498.
Dantas-Torres F. & Brandao-Filho, S. P. 2006. Visceral leishmaniasis in Brazil: Revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo, 48, 151-156.
de Paiva C M., Felinto D.B. M. E., de Souza W. V., de Miranda G Y. & Abath F. G. 2009. The development of a real-time PCR assay for the quantification of Leishmania infantum DNA in canine blood. Vet J, 182(2), 356–358.
Flórez M., Martínez J. P., Gutiérrez R., Luna K. P., Serrano V. H., Ferro C., Angulo V. M. & Sandoval C. M. 2006. Lutzomyia longipalpis (Diptera: Psychodidae) en un foco suburbano de leishmaniosis visceral en el Cañón del Chicamocha en Santander, Colombia. Biomédica, 26(1), 109-120.
França-Silva J. C., da Costa R. T., Siqueira A. M., Machado-Coelho G. L., da Costa C. A., Mayrink W., Vieira E. P., Costa J. S., Genaro O. & Nascimento E. 2003. Epidemiology of canine visceral leishmaniosis in the endemic area of Montes Claros Municipality, Minas Gerais State, Brazil. Vet Parasitol, 111(2-3), 161–173.
Graça G. C. D., Volpini A. C., Romero G. A. S., Oliveira Neto M. P. D., Hueb M., Porrozzi R., & Cupolillo E.2012. Development and validation of PCR-based assays for diagnosis of American cutaneous leishmaniasis and identification of the parasite species. Memórias do Instituto Oswaldo Cruz, 107(5), 664-674.
Guarga J. L., Lucientes J., Peribáñez M. A., Molina R., Gracia M. J. & Castillo J. A. 2000. Experimental infection of Phlebotomus perniciosus and determination of the natural infection rates of Leishmania infantum in dogs. Acta Trop, 77(2), 203–207.
Guzmán-Barragán B. L., Ballesteros-González C., Torres-González D. & Guzman Y. L. 2021. Brote inusitado de leishmaniasis cutánea en zona rural de Ibagué: desafíos de la notificación. Rev UDCA Actual Divulg Cient, 24(1), 1501.
Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P. & Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Lachaud, L., Marchergui-Hammami, S., Chabbert, E., Dereure, J., Dedet, J. P., Bastien, P. 2002. Comparison of six PCR methods using peripheral blood for detection of canine visceral leishmaniasis. J Clin Microbiol. 40(1), 210-215.
Lombardo G., Pennisi M. G., Lupo T., Migliazzo A., Caprì A. & Solano-Gallego L. 2012. Detection of Leishmania infantum DNA by real-time PCR in canine oral and conjunctival swabs and comparison with other diagnostic techniques. Vet Parasitol, 184(1), 10–17.
Macedo T. & Urrego D. 2020. Mesa intersectorial de vectores [Conference presentation]. Secretaría de Salud Municipal de Ibagué. November 20.
Manna L., Vitale F., Reale S., Caracappa S., Pavone L. M., Morte R. D., Cringoli G., Staiano N., & Gravino A. E. 2004. Comparison of different tissue sampling for PCR-based diagnosis and follow-up of canine visceral leishmaniosis. Vet Parasitol, 125(3-4), 251–262.
Marcondes M. & Day M. J. 2019. Current status and management of canine leishmaniasis in Latin America. Res Vet Sci, 123, 261-272.
Membrive N. A., Rodrigues G., Gualda K. P., Bernal M. V. Z., Oliveira D. M., Lonardoni M. V. C. & Silveira T. G. V. 2012. Environmental and animal characteristics as factors associated with American cutaneous leishmaniasis in rural locations with presence of dogs, Brazil. PLoS One, 7(11), e47050.
Mendigaña P, F. A. 2019. Plan estratégico leishmaniasis 2018-2022. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/ET/plan-estrategico-leishmaniasis-2018-2022.pdf
Ministerio de Salud y Protección Social de Colombia (MINSALUD). 2018. Cobertura nacional de vacunación antirrábica de perros y gatos, año 2018. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/SA/coberturas-vacunacion-antirrabica-perros-gatos-2018.zip
Molina R., Amela C., Nieto, J., San-Andrés M., González F., Castillo J. A., Lucientes J. & Alvar J. 1994. Infectivity of dogs naturally infected with Leishmania infantum to colonized Phlebotomus perniciosus. Trans R Soc Trop Med Hyg, 88(4), 491–493.
Monteiro F. M., Machado A. S., Rocha-Silva F., Assunção C. B., Graciele-Melo C., Costa L. E., Portela A. S., Ferraz C E. A., de Figueiredo S. M., Caligiorne R. B. 2019. Canine visceral leishmaniasis: Detection of Leishmania spp. genome in peripheral blood of seropositive dogs by real-time polymerase chain reaction (rt-PCR). Microb Pathog, 126, 263-268.
Morales A., Corredor A., Cáceres E., Ibagos A. L. & de Rodriguez C. 1981. Aislamiento de tres cepas de Leishmania a partir de Lutzomyia trapidoi en colombia. Biomédica, 1,198-206
Moreno J. & Alvar J. 2002. Canine leishmaniasis: epidemiological risk and the experimental model. Trends Parasitol, 18(9), 399–405.
Moreno J., Nieto J., Chamizo C., González F., Blanco F., Barker D. C. & Alvar J. 1999. The immune response and PBMC subsets in canine visceral leishmaniasis before, and after chemotherapy. Vet Immunol Immunopathol, 71(3-4), 181–195.
Moshfe A., Mohebali M., Edrissian G., Zarei Z., Akhoundi B., Kazemi B., Jamshidi S. & Mahmoodi M. 2009. Canine visceral leishmaniasis: asymptomatic infected dogs as a source of L. infantum infection. Acta Trop, 112(2), 101–105.
Mümtaz G. 2018. An Overview of Leishmaniasis: Historic to Future Perspectives. IntechOpen, https://doi.org/10.5772/intechopen.81643
Organización Mundial de la Salud (OMS). 2019. Leishmaniasis. Marzo de 2019. https://www.who.int/en/news-room/fact-sheets/detail/leishmaniasis
Oryan A. & Akbari M. 2016. Worldwide risk factors in leishmaniasis. Asian Pac J Trop Med, 9(10), 925-932.
Paradies P., Capelli G., Cafarchia C., De Caprariis D., Sasanelli M. & Otranto D. 2006. Incidences of Canine Leishmaniasis in an Endemic Area of Southern Italy. J Vet Med B, 53(6), 295–298.
Pardo R., Ferro C., Lozano G., Lozano C., Cabrera O. & Davies C. 1999. Flebótomos (Diptera: Psychodidae) vectores de leishmaniasis cutánea y sus determinantes ecológicos en la zona cafetera del Departamento del Huila. Memorias, XXVI Congreso de la Sociedad Colombiana de Entomología, Santa Fé de Bogotá, Colombia. 147-163.
Pardo R. H., Cabrera O. L., Becerra J., Fuya P. & Ferro C. 2006. Lutzomyia longiflocosa, posible vector en un foco de leishmaniasis cutánea en la región subandina del departamento del Tolima, Colombia, y el conocimiento que tiene la población sobre este insecto. Biomédica, 26(Suppl. 1), 95-108.
Paternina-Gómez M., Díaz-Olmos Y., Paternina L. E. & Bejarano E. E. 2013. Alta prevalencia de infección por Leishmania (Kinetoplastidae: Trypanosomatidae) en caninos del norte de Colombia. Biomédica, 33(3), 375-382.
Quinnell R. J., Courtenay O., Garcez L. M., Kaye P. M., Shaw M. A., Dye C. & Day M. J. 2003. IgG subclass responses in a longitudinal study of canine visceral leishmaniasis. Vet Immunol Immunopathol, 91(3-4), 161–168.
Ramírez C. A., Requena J. M. & Puerta C. J. 2011. Identification of the HSP70-II gene in Leishmania braziliensis HSP70 locus: genomic organization and UTRs characterization. Parasit Vectors, 4, 166.
Ramírez J. D., Hernández C., León C. M., Ayala M. S., Flórez C. & González C. 2016. Taxonomy, diversity, temporal and geographical distribution of Cutaneous Leishmaniasis in Colombia: A retrospective study. Sci Rep, 6, 28266.
Reale S., Maxia L., Vitale F., Glorioso N. S., Caracappa S. & Vesco G. 1999. Detection of Leishmania infantum in dogs by PCR with lymph node aspirates and blood. J Clin Microbiol, 37(9), 2931–2935.
Reis A. B., Martins-Filho O. A., Teixeira-Carvalho A., Giunchetti R. C., Carneiro C. M., Mayrink W., Tafuri W. L. & Corrêa-Oliveira R. 2009. Systemic and compartmentalized immune response in canine visceral leishmaniasis. Vet Immunol Immunopathol, 128(1-3), 87–95.
Reis L. E., Coura-Vital W., Roatt B. M., Bouillet L. É., Ker H. G., Fortes de Brito R. C., Resende D., Carneiro M., Giunchetti R. C., Marques M. J., Carneiro C. M. & Reis, A. B. 2013. Molecular diagnosis of canine visceral leishmaniasis: a comparative study of three methods using skin and spleen from dogs with natural Leishmania infantum infection. Vet Parasitol, 197(3-4), 498–503.
Ribeiro R. R., Michalick M. S. M., da Silva M. E., dos Santos C. C. P., Frézard F. J. G. & da Silva S. M. 2018. Canine leishmaniasis: an overview of the current status and strategies for control. BioMed research international, 2018, 3296893.
Salgado-Almario J., Hernández C. A. & Ovalle B C. 2019. Geographical distribution of Leishmania species in Colombia, 1985-2017. Biomédica, 39(2), 278-290.
Santaella J., Ocampo C. B., Saravia N. G., Méndez F., Góngora R., Gomez M. A. & Quinnell R. J. 2011. Leishmania (Viannia) infection in the domestic dog in Chaparral, Colombia. Am J Trop Med Hyg, 84(5), 674-680.
Schönian G., Nasereddin A., Dinse N., Schweynoch C., Schallig H. D., Presber W. & Jaffe C. L. 2003. PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagn Microbiol Infect Dis, 47(1), 349-358.
Shang L. M., Peng W. P., Jin H. T., Xu D., Zhong N., Wang W., Wu Y. % Liu Q. 2011. The prevalence of canine Leishmania infantum infection in Sichuan Province, southwestern China detected by real time PCR. Parasit Vectors, 4, 173.
Sierra D., Vélez I. D. & Uribe S. 2000. Identificación de Lutzomyia spp. (Diptera: Psychodidae) grupo verrucarum por medio de microscopía electrónica de sus huevos. Rev Biol Trop, 48, 615-622.
Silva R. B. S., Porto M. L., Barbosa W. D. O., Souza H. C. D., Marques N. F. D. S. P., Azevedo S. S., Andrade P. & Melo M. A. D. 2018. Seroprevalence and risk factors associated with canine visceral leishmaniasis in the State of Paraíba, Brazil. Rev Soc Bras Med Trop, 51(5), 683-688.
Sistema de Vigilancia en Salud Pública (SIVIGILA). (2019). Leishmaniasis cutánea, periodo epidemiológico VI, Colombia. https://www.ins.gov.co/buscador-eventos/Informesdeevento/LEISHMANIASIS%20CUT%C3%81NEA%20PE%20VI%202019.pdf
Soares M. R., de Mendonça I. L., do Bonfim J. M., Rodrigues J. A., Werneck G. L. & Costa C. H. 2011. Canine visceral leishmaniasis in Teresina, Brazil: Relationship between clinical features and infectivity for sand flies. Acta Trop, 117(1), 6–9.
Solano-Gallego L., Morell P., Arboix M., Alberola J. & Ferrer L. 2001. Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology. J Clin Microbiol, 39(2), 560–563.
Sundar S. & Rai M. 2002. Laboratory diagnosis of visceral leishmaniasis. Clin Diagn Lab Immunol, 9(5), 951–958.
Thrusfield M. 2018. Veterinary epidemiology . 4th ed. John Wiley & Sons.
Torres G. E., Quintanilla C. M. R., Ruiz E. J. & Arenas R. 2017. Leishmaniasis: a review. F1000Res. 6. https://doi.org/10.12688/f1000research.11120.1
Toz S. O., Culha G., Zeyrek F. Y., Ertabaklar H., Alkan M. Z., Vardarlı A. T., Gunduz C. & Ozbel Y. 2013. A real-time ITS1-PCR based method in the diagnosis and species identification of Leishmania parasite from human and dog clinical samples in Turkey. PLoS Negl Trop Dis, 7(5), e2205.
Travi B. L., Tabares C. J., Cadena H., Ferro C. & Osorio Y. 2001. Canine visceral leishmaniasis in Colombia: relationship between clinical and parasitologic status and infectivity for sand flies. Am J Trop Med Hyg, 64(3), 119-124.
Trevisan D. A. C., Lonardoni M. V. C. & Demarchi I. G. 2015. Diagnostic methods to cutaneous leishmaniasis detection in domestic dogs and cats. An Bras Dermatol, 90(6), 868-872.
Verçosa B. L. A., Lemos C. M., Mendonca I. L., Silva,S. M. M. S., De Carvalho S. M., Goto H., & Costa F. A. L. 2008. Transmission potential, skin inflammatory response, and parasitism of symptomatic and asymptomatic dogs with visceral leishmaniasis. BMC Vet Res, 4(1), 1-7.
Wang J. Y., Ha Y., Gao C. H., Wang Y., Yang Y. T. & Chen H. T. 2011. The prevalence of canine Leishmania infantum infection in western China detected by PCR and serological tests. Parasit Vectors, 4(1), 69.
Zoghlami Z., Chouihi E., Barhoumi W., Dachraoui K., Massoudi N., Helel K. B. & Gharbi M. 2014. Interaction between canine and human visceral leishmaniases in a holoendemic focus of Central Tunisia. Acta Trop, 139, 32-38.