Skip to main content Accessibility help
Hostname: page-component-77ffc5d9c7-4bjzw Total loading time: 0.331 Render date: 2021-04-23T15:31:25.774Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Leishmania infection in bats from a non-endemic region of Leishmaniasis in Brazil

Published online by Cambridge University Press:  23 August 2017

Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Centro de Educação Profissional – CEFORES, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Universidade Federal de Uberlândia, Campus do Pontal, Ituiutaba, Minas Gerais, Brazil
Instituto Federal de Educação, Ciência e Tecnologia do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
Grupo de Investigaciones Microbiológicas – UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
E-mail address:


Leishmaniasis is a complex of zoonotic diseases caused by parasites of the genus Leishmania, which can develop in domestic as well as wild animals and humans throughout the world. Currently, this disease is spreading in rural and urban areas of non-endemic regions in Brazil. Recently, bats have gained epidemiological significance in leishmaniasis due to its close relationship with human settlements. In this study, we investigated the presence of Leishmania spp. DNA in blood samples from 448 bats belonging to four families representing 20 species that were captured in the Triangulo Mineiro and Alto Paranaiba areas of Minas Gerais State (non-endemic areas for leishmaniasis), Brazil. Leishmania spp. DNA was detected in 8·0% of the blood samples, 41·6% of which were Leishmania infantum, 38·9% Leishmania amazonensis and 19·4% Leishmania braziliensis. No positive correlation was found between Leishmania spp. and bat food source. The species with more infection rates were the insectivorous bats Eumops perotis; 22·2% (4/18) of which tested positive for Leishmania DNA. The presence of Leishmania in the bat blood samples, as observed in this study, represents epidemiological importance due to the absence of Leishmaniasis cases in the region.

Research Article
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below.


These authors contributed equally to this work.


Ab'sáber, A. N. (1971). A organização natural das paisagens inter e subtropicais brasileirasp. In III Simpósio sobre o Cerrado. 1st edn. (Ferri, M.G., coord.), pp. 114. Edgar Blücher-EDUSP Press, São Paulo, BR.Google Scholar
Adams, E. R., Gomez, M. A., Scheske, L., Rios, R., Marquez, R., Cossio, A., Albertini, A., Schallig, H. and Saravia, N. G. (2014). Sensitive diagnosis of cutaneous leishmaniasis by lesion swab sampling coupled to qPCR. Parasitology 141, 18911897.CrossRefGoogle ScholarPubMed
Alho, C. J. R. (1993). Distribuição da fauna num gradiente de recursos em mosaico. In Cerrado (Pinto, M. N., Org.), pp. 213262. Editora Editora UnB/Sematec, Brasília, BR.Google Scholar
Ashford, R. W. (1996). Leishmaniasis reservoirs and their significance in control. Clinics in Dermatology 14, 523532.CrossRefGoogle ScholarPubMed
Bento, E. C. (2006). Morcegos do Triângulo Mineiro e sua associação com Tripanosomatídeos, Filarídeos, Fungos, Vírus rábico e Ectoparasitos, vol. Mestrado, p. 218. Universidade Federal do Triângulo Mineiro, Uberaba.Google Scholar
Bento, E. C. (2013). Tripanosomas isolados de diferentes reservatórios silvestres em região endêmica para doença de Chagas em Minas Gerais, Brasil, vol. Doutorado, p. 238. Universidade Federal do Triângulo Mineiro, Uberaba.Google Scholar
Berzunza-Cruz, M., Rodriguez-Moreno, A., Gutierrez-Granados, G., Gonzalez-Salazar, C., Stephens, C. R., Hidalgo-Mihart, M., Marina, C. F., Rebollar-Tellez, E. A., Bailon-Martinez, D., Balcells, C. D., Ibarra-Cerdena, C. N., Sanchez-Cordero, V. and Becker, I. (2015). Leishmania (L.) mexicana infected bats in Mexico: novel potential reservoirs. PLoS Neglected Tropical Diseases 9, e0003438.CrossRefGoogle ScholarPubMed
Brandao-Filho, S. P., Brito, M. E., Carvalho, F. G., Ishikawa, E. A., Cupolillo, E., Floeter-Winter, L. and Shaw, J. J. (2003). Wild and synanthropic hosts of Leishmania (Viannia) braziliensis in the endemic cutaneous leishmaniasis locality of Amaraji, Pernambuco State, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 291296.CrossRefGoogle ScholarPubMed
Brener, Z. and Andrade, Z. A. (1979). Trypanosoma cruzi e doença de Chagas, 1st edn. Guanabara Koogan, Rio de Janeiro, BR.Google Scholar
De Lima, H., Rodriguez, N., Barrios, M. A., Avila, A., Canizales, I. and Gutierrez, S. (2008). Isolation and molecular identification of Leishmania chagasi from a bat (Carollia perspicillata) in northeastern Venezuela. Memorias do Instituto Oswaldo Cruz 103, 412414.CrossRefGoogle Scholar
de Rezende, M. B., Herrera, H. M., Carvalho, C. M., Carvalho Anjos, E. A., Ramos, C. A., de Araujo, F. R., Torres, J. M. and de Oliveira, C. E. (2017). Detection of Leishmania spp. in bats from an area of Brazil endemic for visceral leishmaniasis. Transboundary and Emerging Diseases. doi: 10.1111/tbed.12597.CrossRefGoogle ScholarPubMed
Foulet, F., Botterel, F., Buffet, P., Morizot, G., Rivollet, D., Deniau, M., Pratlong, F., Costa, J. M. and Bretagne, S. (2007). Detection and identification of Leishmania species from clinical specimens by using a real-time PCR assay and sequencing of the cytochrome B gene. Journal of Clinical Microbiology 45, 21102115.CrossRefGoogle ScholarPubMed
Garcia, A. L., Parrado, R., De Doncker, S., Bermudez, H. and Dujardin, J. C. (2007). American tegumentary leishmaniasis: direct species identification of Leishmania in non-invasive clinical samples. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 368-371.CrossRefGoogle ScholarPubMed
Gomes, M. L., Macedo, A. M., Vago, A. R., Pena, S. D., Galvao, L. M. and Chiari, E. (1998). Trypanosoma cruzi: optimization of polymerase chain reaction for detection in human blood. Experimental Parasitology 88, 2833.CrossRefGoogle ScholarPubMed
Gregorin, R., Taddei, V. A. (2002). Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). Journal of Neotropical Mammalogy 9, 1332.Google Scholar
Guyatt, K. J., Twin, J., Davis, P., Holmes, E. C., Smith, G. A., Smith, I. L., Mackenzie, J. S. and Young, P. L. (2003). A molecular epidemiological study of Australian bat lyssavirus. Journal of General Virology 84, 485496.CrossRefGoogle ScholarPubMed
Halpin, K., Young, P. L., Field, H. E. and Mackenzie, J. S. (2000). Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. Journal of General Virology 81, 19271932.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Cruickshank, C., Stevens, J. R., Teixeira, M. M. and Mathews, F. (2012a). Parasites reveal movement of bats between the New and Old Worlds. Molecular Phylogenetics and Evolution 63, 521526.CrossRefGoogle ScholarPubMed
Hamilton, P. B., Teixeira, M. M. and Stevens, J. R. (2012b). The evolution of Trypanosoma cruzi: the ‘bat seeding’ hypothesis. Trends in Parasitology 28, 136141.CrossRefGoogle ScholarPubMed
Haydon, D. T., Cleaveland, S., Taylor, L. H. and Laurenson, M. K. (2002). Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8, 14681473.Google ScholarPubMed
Hernandez, C., Alvarez, C., Gonzalez, C., Ayala, M. S., Leon, C. M. and Ramirez, J. D. (2014). Identification of six New World Leishmania species through the implementation of a High-Resolution Melting (HRM) genotyping assay. Parasites & Vectors 7, 501.CrossRefGoogle ScholarPubMed
Kumar, R., Bumb, R. A., Ansari, N. A., Mehta, R. D. and Salotra, P. (2007). Cutaneous leishmaniasis caused by Leishmania tropica in Bikaner, India: parasite identification and characterization using molecular and immunologic tools. American Journal of Tropical Medicine and Hygiene 76, 896901.Google ScholarPubMed
Lampo, M., Feliciangeli, M. D., Marquez, L. M., Bastidas, C. and Lau, P. (2000). A possible role of bats as a blood source for the Leishmania vector Lutzomyia longipalpis (Diptera: Psychodidae). American Journal of Tropical Medicine and Hygiene 62, 718719.CrossRefGoogle Scholar
Lemos, J. C. and Lima, S. C. (2005). American cutaneous leishmaniasis: phlebotomine transmission area in the Municipality of Uberlandia, MG. Rev Soc Bras Med Trop 38, 2226.CrossRefGoogle ScholarPubMed
Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J. H., Wang, H., Crameri, G., Hu, Z., Zhang, H., Zhang, J., McEachern, J., Field, H., Daszak, P., Eaton, B. T., Zhang, S. and Wang, L. F. (2005). Bats are natural reservoirs of SARS-like coronaviruses. Science 310, 676-679.CrossRefGoogle ScholarPubMed
Liu, B., Liu, Y., Motyka, S. A., Agbo, E. E. and Englund, P. T. (2005). Fellowship of the rings: the replication of kinetoplast DNA. Trends in Parasitology 21, 363369.CrossRefGoogle ScholarPubMed
Luyo-Acero, G. E., Uezato, H., Oshiro, M., Takei, K., Kariya, K., Katakura, K., Gomez-Landires, E., Hashiguchi, Y. and Nonaka, S. (2004). Sequence variation of the cytochrome b gene of various human infecting members of the genus Leishmania and their phylogeny. Parasitology 128, 483491.CrossRefGoogle ScholarPubMed
Marcili, A., Speranca, M. A., da Costa, A. P., Madeira Mde, F., Soares, H. S., Sanches Cde, O., Acosta Ida, C., Girotto, A., Minervino, A. H., Horta, M. C., Shaw, J. J. and Gennari, S. M. (2014). Phylogenetic relationships of Leishmania species based on trypanosomatid barcode (SSU rDNA) and gGAPDH genes: taxonomic revision of Leishmania (L.) infantum chagasi in South America. Infection Genetics and Evolution 25, 44-51.CrossRefGoogle ScholarPubMed
Marfurt, J., Nasereddin, A., Niederwieser, I., Jaffe, C. L., Beck, H. P. and Felger, I. (2003). Identification and differentiation of Leishmania species in clinical samples by PCR amplification of the miniexon sequence and subsequent restriction fragment length polymorphism analysis. Journal of Clinical Microbiology 41, 31473153.CrossRefGoogle ScholarPubMed
Marinkellei, C. J. (1982). Prevalence of Trypanosoma cruzi-like infection of Colombian bats. Annals of Tropical Medicine & Parasitology 76, 125134.CrossRefGoogle Scholar
Marques, M. J., Volpini, A. C., Genaro, O., Mayrink, W. and Romanha, A. J. (2001). Simple form of clinical sample preservation and Leishmania DNA extraction from human lesions for diagnosis of American cutaneous leishmaniasis via polymerase chain reaction. American Journal of Tropical Medicine and Hygiene 65, 902906.CrossRefGoogle ScholarPubMed
Millan, J., Ferroglio, E. and Solano-Gallego, L. (2014a). Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitology Research 113, 20052014.CrossRefGoogle Scholar
Millan, J., Lopez-Roig, M., Cabezon, O. and Serra-Cobo, J. (2014b). Absence of Leishmania infantum in cave bats in an endemic area in Spain. Parasitology Research 113, 19931995.CrossRefGoogle Scholar
Mohammadiha, A., Mohebali, M., Haghighi, A., Mahdian, R., Abadi, A. R., Zarei, Z., Yeganeh, F., Kazemi, B., Taghipour, N. and Akhoundi, B. (2013). Comparison of real-time PCR and conventional PCR with two DNA targets for detection of Leishmania (Leishmania) infantum infection in human and dog blood samples. Experimental Parasitology 133, 8994.CrossRefGoogle ScholarPubMed
Molyneux, A. J. (1991). Trypanosomes of bats. In Parasitic Protozoa (ed. Kreier, J. P. and Baker, J. R.), pp. 95223. Academic Press, New York.Google Scholar
Montalvo, A. M., Fraga, J., El Safi, S., Gramiccia, M., Jaffe, C. L., Dujardin, J. C. and Van der Auwera, G. (2014). Direct Leishmania species typing in Old World clinical samples: evaluation of 3 sensitive methods based on the heat-shock protein 70 gene. Diagnostic Microbiology and Infectious Disease 80, 3539.CrossRefGoogle ScholarPubMed
Morsy, T. A., Salama, M. M. and Abdel Hamid, M. Y. (1987). Detection of Leishmania antibodies in bats. Journal of the Egyptian Society of Parasitology 17, 797798.Google ScholarPubMed
Motta, P. E. F. (1993). Os solos do Triângulo Mineiro e sua aptidão agrícola. Informe Agropecuario 9(105), 5763. Belo Horizonte, BR.Google Scholar
Mutinga, M. J. (1975). The animal reservoir of cutaneous leishmaniasis on Mount Elgon, Kenya. East African Medical Journal 52, 142151.Google ScholarPubMed
Nicolas, L., Prina, E., Lang, T. and Milon, G. (2002). Real-time PCR for detection and quantitation of leishmania in mouse tissues. Journal of Clinical Microbiology 40, 16661669.CrossRefGoogle ScholarPubMed
Ovalle Bracho, C., Porras de Quintana, L., Muvdi Arenas, S. and Rios Parra, M. (2007). Polymerase chain reaction with two molecular targets in mucosal leishmaniasis’ diagnosis: a validation study. Memorias do Instituto Oswaldo Cruz 102, 549554.CrossRefGoogle ScholarPubMed
Paula, M. B., Souza, A. A., dos Reis, A. A., Limongi, J. E., Pajuaba Neto Ade, A. and Rodrigues Ede, A. (2013). Survey of sandfly fauna (Diptera: Psychodidae) in Uberlandia, Minas Gerais State, Brazil, 2003–2004. Revista do Instituto de Medicina Tropical de Sao Paulo 55, 8589.CrossRefGoogle Scholar
Pinto, C. M., Ocana-Mayorga, S., Tapia, E. E., Lobos, S. E., Zurita, A. P., Aguirre-Villacis, F., MacDonald, A., Villacis, A. G., Lima, L., Teixeira, M. M., Grijalva, M. J. and Perkins, S. L. (2015). Bats, trypanosomes, and triatomines in ecuador: new insights into the diversity, transmission, and origins of Trypanosoma cruzi and chagas disease. PLoS ONE 10, e0139999.CrossRefGoogle ScholarPubMed
Rajendran, P., Chatterjee, S. N., Dhanda, V. and Dhiman, R. C. (1985). Observations on the role of vespertilionid bats in relation to non-human vertebrate reservoir in Indian kala-azar. Indian Journal of Pathology and Microbiology 28, 153158.Google ScholarPubMed
Ramirez, J. D. and Llewellyn, M. S. (2014). Reproductive clonality in protozoan pathogens--truth or artefact? Molecular Ecology 23, 41954202.CrossRefGoogle ScholarPubMed
Ramirez, J. L. and Galetti, P. M. Jr. (2015). DNA barcode and evolutionary relationship within Laemolyta Cope 1872 (Characiformes: Anostomidae) through molecular analyses. Molecular Phylogenetics and Evolution 93, 7782.CrossRefGoogle ScholarPubMed
Ramirez, J. D., Hernandez, C., Leon, C. M., Ayala, M. S., Florez, C. and Gonzalez, C. (2016). Taxonomy, diversity, temporal and geographical distribution of cutaneous Leishmaniasis in Colombia: a retrospective study. Scientific Reports 6, 28266.CrossRefGoogle ScholarPubMed
Reis, N. R., Peracchi, A. L., Pedro, W. A. and Lima, I. P. (2007). Morcegos do Brasil, 1st edn. Londrina, BR.Google Scholar
Rizzini, C. T. (1997). Tratado de Fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. 2nd edn. Âmbito Cultural Edições, Rio de Janeiro, BR.Google Scholar
Rodriguez, N., De Lima, H., Aguilar, C. M., Rodriguez, A., Barker, D. C. and Convit, J. (2002). Molecular epidemiology of cutaneous leishmaniasis in Venezuela. Transactions of the Royal Society of Tropical Medicine and Hygiene, 96(Suppl. 1), S105S109.CrossRefGoogle ScholarPubMed
Rotureau, B., Catzeflis, F. and Carme, B. (2006). Absence of leishmania in Guianan bats. American Journal of Tropical Medicine and Hygiene 74, 318321.Google ScholarPubMed
Savani, E. S., de Almeida, M. F., de Oliveira Camargo, M. C., D'Auria, S. R., Silva, M. M., de Oliveira, M. L. and Sacramento, D. (2010). Detection of Leishmania (Leishmania) amazonensis and Leishmania (Leishmania) infantum chagasi in Brazilian bats. Veterinary Parasitology 168, 510.CrossRefGoogle ScholarPubMed
Shahbazi, F., Shahabi, S., Kazemi, B., Mohebali, M., Abadi, A. R. and Zare, Z. (2008). Evaluation of PCR assay in diagnosis and identification of cutaneous leishmaniasis: a comparison with the parasitological methods. Parasitology Research 103, 11591162.CrossRefGoogle ScholarPubMed
Shapiro, J. T., da Costa Lima Junior, M. S., Dorval, M. E., de Oliveira Franca, A., Cepa Matos Mde, F. and Bordignon, M. O. (2013). First record of Leishmania braziliensis presence detected in bats, Mato Grosso do Sul, southwest Brazil. Acta Tropica 128, 171174.CrossRefGoogle Scholar
Thompson, P. N. and Etter, E. (2015). Epidemiological surveillance methods for vector-borne diseases. Revue Scientifique et Technique 34, 235247.CrossRefGoogle ScholarPubMed
Vizotto, L. D. and Taddei, V. A. (1973). Chave para determinação de quirópteros brasileiros. Revista Faculdade Filosofia Ciências Letras São José do Rio Preto, 1, 172.Google Scholar

Altmetric attention score

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 64
Total number of PDF views: 266 *
View data table for this chart

* Views captured on Cambridge Core between 23rd August 2017 - 23rd April 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Leishmania infection in bats from a non-endemic region of Leishmaniasis in Brazil
Available formats

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Leishmania infection in bats from a non-endemic region of Leishmaniasis in Brazil
Available formats

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Leishmania infection in bats from a non-endemic region of Leishmaniasis in Brazil
Available formats

Reply to: Submit a response

Your details

Conflicting interests

Do you have any conflicting interests? *