Hostname: page-component-77c78cf97d-v4t4b Total loading time: 0 Render date: 2026-05-02T12:52:41.065Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  23 August 2017

CÉSAR GÓMEZ-HERNÁNDEZ ,
ELAINE C. BENTO ,
KARINE REZENDE-OLIVEIRA ,
GABRIEL A. N. NASCENTES ,
CECILIA G. BARBOSA ,
LARA R. BATISTA ,
MONIQUE G. S. TIBURCIO ,
ANDRÉ L. PEDROSA ,
ELIANE LAGES-SILVA  and
JUAN D. RAMÍREZ
...Show all authors
CÉSAR GÓMEZ-HERNÁNDEZ
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
ELAINE C. BENTO
Affiliation:
Centro de Educação Profissional – CEFORES, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
KARINE REZENDE-OLIVEIRA
Affiliation:
Universidade Federal de Uberlândia, Campus do Pontal, Ituiutaba, Minas Gerais, Brazil
GABRIEL A. N. NASCENTES
Affiliation:
Instituto Federal de Educação, Ciência e Tecnologia do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
CECILIA G. BARBOSA
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
LARA R. BATISTA
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
MONIQUE G. S. TIBURCIO
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
ANDRÉ L. PEDROSA
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
ELIANE LAGES-SILVA
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
JUAN D. RAMÍREZ
Affiliation:
Grupo de Investigaciones Microbiológicas – UR (GIMUR), Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Bogotá, Colombia
LUIS E. RAMIREZ*
Affiliation:
Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil
*
*Corresponding author: Laboratório de Parasitologia, Universidade Federal do Triângulo Mineiro, Uberaba, Minas Gerais, Brazil. Rua Getúlio Guaritá S/N, Bairro Abadia, Uberaba, Minas Gerais, CEP 38025-180, Brazil. E-mail: ramirez_fmtm@yahoo.com.br
Get access Rights & Permissions [Opens in a new window]

Summary

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.

Keywords

BatsLeishmania infantumLeishmania amazonensisLeishmania braziliensisCytBHSP70Brazil

Information

Type
Research Article
Information
Parasitology , Volume 144 , Issue 14 , December 2017 , pp. 1980 - 1986
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

Footnotes

†

These authors contributed equally to this work.

References

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. 1–14. 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, 1891–1897.CrossRefGoogle ScholarPubMed
Alho, C. J. R. (1993). Distribuição da fauna num gradiente de recursos em mosaico. In Cerrado (Pinto, M. N., Org.), pp. 213–262. Editora Editora UnB/Sematec, Brasília, BR.Google Scholar
Ashford, R. W. (1996). Leishmaniasis reservoirs and their significance in control. Clinics in Dermatology 14, 523–532.Google Scholar
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.Google Scholar
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, 291–296.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, 412–414.Google 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, 2110–2115.Google Scholar
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.Google Scholar
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, 28–33.Google Scholar
Gregorin, R., Taddei, V. A. (2002). Chave artificial para a identificação de molossídeos brasileiros (Mammalia, Chiroptera). Journal of Neotropical Mammalogy 9, 13–32.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, 485–496.Google Scholar
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, 1927–1932.Google Scholar
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, 521–526.Google Scholar
Hamilton, P. B., Teixeira, M. M. and Stevens, J. R. (2012b). The evolution of Trypanosoma cruzi: the ‘bat seeding’ hypothesis. Trends in Parasitology 28, 136–141.Google Scholar
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, 1468–1473.Google Scholar
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.Google Scholar
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, 896–901.Google Scholar
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, 718–719.Google 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, 22–26.Google Scholar
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, 363–369.Google Scholar
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, 483–491.Google Scholar
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.Google Scholar
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, 3147–3153.CrossRefGoogle ScholarPubMed
Marinkellei, C. J. (1982). Prevalence of Trypanosoma cruzi-like infection of Colombian bats. Annals of Tropical Medicine & Parasitology 76, 125–134.Google 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, 902–906.Google Scholar
Millan, J., Ferroglio, E. and Solano-Gallego, L. (2014a). Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitology Research 113, 2005–2014.CrossRefGoogle ScholarPubMed
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, 1993–1995.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, 89–94.Google Scholar
Molyneux, A. J. (1991). Trypanosomes of bats. In Parasitic Protozoa (ed. Kreier, J. P. and Baker, J. R.), pp. 95–223. 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, 35–39.Google Scholar
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, 797–798.Google Scholar
Motta, P. E. F. (1993). Os solos do Triângulo Mineiro e sua aptidão agrícola. Informe Agropecuario 9(105), 57–63. Belo Horizonte, BR.Google Scholar
Mutinga, M. J. (1975). The animal reservoir of cutaneous leishmaniasis on Mount Elgon, Kenya. East African Medical Journal 52, 142–151.Google Scholar
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, 1666–1669.Google Scholar
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, 549–554.Google Scholar
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, 85–89.Google 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.Google Scholar
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, 153–158.Google Scholar
Ramirez, J. D. and Llewellyn, M. S. (2014). Reproductive clonality in protozoan pathogens--truth or artefact? Molecular Ecology 23, 4195–4202.Google Scholar
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, 77–82.Google Scholar
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.Google Scholar
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), S105–S109.Google Scholar
Rotureau, B., Catzeflis, F. and Carme, B. (2006). Absence of leishmania in Guianan bats. American Journal of Tropical Medicine and Hygiene 74, 318–321.Google Scholar
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, 5–10.Google Scholar
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, 1159–1162.Google Scholar
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, 171–174.Google Scholar
Thompson, P. N. and Etter, E. (2015). Epidemiological surveillance methods for vector-borne diseases. Revue Scientifique et Technique 34, 235–247.Google Scholar
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, 1–72.Google Scholar