Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T14:45:04.630Z Has data issue: false hasContentIssue false
  • English
  • Français

Golden hamster (Mesocricetus auratus) as an experimental model for Leishmania (Viannia) braziliensis infection

Published online by Cambridge University Press:  01 February 2013

ADRIANO GOMES-SILVA ,
JOANNA GARDEL VALVERDE ,
RAQUEL PERALVA RIBEIRO-ROMÃO ,
ROSA MARIA PLÁCIDO-PEREIRA  and
ALDA MARIA DA-CRUZ
ADRIANO GOMES-SILVA
Affiliation:
Laboratório Interdisciplinar de Pesquisas Médicas, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
JOANNA GARDEL VALVERDE
Affiliation:
Laboratório Interdisciplinar de Pesquisas Médicas, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
RAQUEL PERALVA RIBEIRO-ROMÃO
Affiliation:
Laboratório Interdisciplinar de Pesquisas Médicas, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
ROSA MARIA PLÁCIDO-PEREIRA
Affiliation:
Laboratório Interdisciplinar de Pesquisas Médicas, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
ALDA MARIA DA-CRUZ*
Affiliation:
Laboratório Interdisciplinar de Pesquisas Médicas, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
*
*Corresponding author: Av. Brasil 4365, Pavilhão Leônidas Deane 4° andar, Manguinhos, Rio de Janeiro-RJ, ZIP 21040-360, Brazil. Tel: +55 21 3865 8147. Fax: +55 21 2290 0479. E-mail: alda@ioc.fiocruz.br
Get access Rights & Permissions [Opens in a new window]

Summary

The lack of an adequate model for Leishmania (Viannia) braziliensis infection is a limiting factor for studying American tegumentary leishmaniasis (ATL). The golden hamster (Mesocricetus auratus) is a promising model because besides being highly susceptible to dermotropic Leishmania infection, the lesions are very similar to cutaneous leishmaniasis (CL) in humans. However, different Leishmania isolates or species and/or protocols have resulted in different outcomes, whereas no study has evaluated the reproducibility of L. braziliensis infection in this model. The natural history of L. braziliensis infection in 34 hamsters was evaluated by using a single parasite isolate in 8 independent experiments under similar experimental conditions. Clinical, histological and immunological analyses were performed. The hamsters presented skin ulcers similar to those observed in ATL. The intra-experiment lesion increment tended to show an intermediary variance. Histological analysis of infected skins showed granulomatous reaction, scarce amastigotes, and Schaumann's bodies. Blood lymphocytes proliferated in response to leishmanial antigens. The severity of the infection was positively correlated to spleen weight, and the titres of anti-Leishmania IgG antibodies. Our findings indicate that the hamster is an appropriate model for immunopathogenesis studies of CL caused by L. braziliensis, supporting its use in clinical, vaccine and chemotherapy experimental protocols.

Keywords

golden hamsterAmerican tegumentary leishmaniasisLeishmania (Viannia) braziliensisimmunoglobulinlymphocyteclinical outcomehistopathology
Type
Research Article
Information
Parasitology , Volume 140 , Issue 6 , May 2013 , pp. 771 - 779
Copyright
Copyright © Cambridge University Press 2013

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.)

References

REFERENCES

Almeida, M. C., Cuba-Cuba, C. A., Moraes, M. A. and Miles, M. A. (1996). Dissemination of Leishmania (Viannia) braziliensis. Journal of Comparative Pathology 115, 311–316. doi: 10.1016/S0021-9975(96)80088-0.CrossRefGoogle ScholarPubMed
Brazil, R. P. (1976). Metastatic spread of Leishmania braziliensis braziliensis to the extremities of hamsters. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 89. doi: 10.1016/0035-9203(76)90017-1.CrossRefGoogle Scholar
Carvalho, L. P., Passos, S., Schriefer, A. and Carvalho, E. M. (2012). Protective and pathologic immune responses in human tegumentary leishmaniasis. Frontiers in Immunology 3, 1–9. doi: 10.3389/fimmu.2012.00301.CrossRefGoogle ScholarPubMed
Corrêa, J. R., Brazil, R. P. and Soares, M. J. (2007). Leishmania (Viannia) lainsoni (Silveira et al. 1987): ultrastructural aspects of the parasite and skin lesion in experimentally infected hamster (Mesocricetus auratus). Parasitology Research 100, 1227–1232. doi: 10.1007/s00436-006-0395-5.CrossRefGoogle Scholar
Da-Cruz, A. M., Bittar, R., Mattos, M., Oliveira-Neto, M. P., Nogueira, R., Pinho-Ribeiro, V., Azeredo-Coutinho, R. B. and Coutinho, S. G. (2002). T-cell-mediated immune responses in patients with cutaneous or mucosal leishmaniasis: long-term evaluation after therapy. Clinical and Diagnostic Laboratory Immunology 9, 251–256. doi: 10.1128/CDLI.9.2.251-256.2002.Google ScholarPubMed
De Oliveira, C. I., Teixeira, M. J., Gomes, R., Barral, A. and Brodskyn, C. I. (2004). Animal models for infectious diseases caused by parasites: leishmaniasis. Drug Discovery Today: Disease Models 1, 81–86. doi: 10.1016/j.ddmod.2004.07.005.Google Scholar
Dea-Ayuela, M. A., Rama-Iñiguez, S., Alunda, J. M. and Bolás-Fernandez, F. (2007). Setting new immunobiological parameters in the hamster model of visceral leishmaniasis for in vivo testing of antileishmanial compounds. Veterinary Research Communications 31, 703–717. doi: 10.1007/s11259-007-0040-5.CrossRefGoogle ScholarPubMed
DeKrey, G. K., Lima, H. C. and Titus, R. G. (1998). Analysis of the immune responses of mice to infection with Leishmania braziliensis. Infection and Immunity 66, 827–829. PMCID: PMC107977.CrossRefGoogle ScholarPubMed
Espitia, C. M., Zhao, W., Saldarriaga, O., Osorio, Y., Harrison, L. M., Cappello, M., Travi, B. L. and Melby, P. C. (2010). Duplex real-time reverse transcriptase PCR to determine cytokine mRNA expression in a hamster model of New World cutaneous leishmaniasis. BMC Immunology 11, 31. doi: 10.1186/1471-2172-11-31.CrossRefGoogle Scholar
Essayag, S. M., Landaeta, M. E., Hartung, C., Magaldi, S., Spencer, L., Suárez, R., García, F. and Pérez, E. (2002). Histopathologic and histochemical characterization of calcified structures in hamsters inoculated with Paracoccidioides brasiliensis. Mycoses 45, 351–357. doi: 10.1046/j.1439-0507.2002.00785.x.CrossRefGoogle ScholarPubMed
Figueiredo, E. M., Costa e Silva, J. and Brazil, R. P. (1999). Experimental treatment with sodium stibogluconate of hamsters infected with Leishmania (Leishmania) chagasi and Leishmania (Leishmania) amazonensis. Revista da Sociedade Brasileira de Medicina Tropical 32, 191–193. doi: 10.1590/S0037-86821999000200012.CrossRefGoogle ScholarPubMed
Gamboa, D., Torres, K., De Doncker, S., Zimic, M., Arevalo, J. and Dujardin, J. C. (2008). Evaluation of an in vitro and in vivo model for experimental infection with Leishmania (Viannia) braziliensis and L. (V.) peruviana. Parasitology 135, 319–326. doi: 10.1017/S0031182007003848.CrossRefGoogle Scholar
Gomes-Silva, A., Pereira-Carvalho, R., Fagundes-Silva, G. A., Oliveira-Neto, M. P. and Da-Cruz, A. M. (2009). Homeostasis of specific immune response in clinically cured cutaneous leishmaniasis subjects due to Leishmania (Viannia) braziliensis. Revista da Sociedade Brasileira de Medicina Tropical 42 (Suppl. II), S147–S150.Google Scholar
Gomes-Silva, A., Souza, M. A., Afonso-Cardoso, S. R., Lívia Resende Andrade, L. R., Dietze, R., Lemos, E., Belli, A., Favoreto Júnior, S. and Ferreira, M. S. (2008). Serological reactivity of different antigenic preparations of Leishmania (Leishmania) amazonensis and the Leishmania braziliensis complex. Revista da Sociedade Brasileira de Medicina Tropical 41, 135–141. doi: 10.1590/S0037-86822008000200001.CrossRefGoogle ScholarPubMed
Goto, H. and Lindoso, J. A. (2004). Immunity and immunosuppression in experimental visceral leishmaniasis. Brazilian Journal of Medical and Biological Research 37, 615–623. doi: 10.1590/S0100-879X2004000400020.CrossRefGoogle ScholarPubMed
Hommel, M., Jaffe, C. L., Travi, B. and Milon, G. (1995). Experimental models for leishmaniasis and for testing anti-leishmanial vaccines. Annals of Tropical Medicine and Parasitology 89, 55–73. PMID:8745928.CrossRefGoogle ScholarPubMed
Kahl, L. P., Byra, J. E. and David, J. R. (1990). Leishmania (Viannia) braziliensis isolated from cutaneous and mucosal lesions of patients residing in Três Braços, Bahia, Brazil differ in virulence for the golden hamster. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 783–784. doi: 10.1016/0035-9203(90)90078-S.CrossRefGoogle ScholarPubMed
Kahl, L. P., Byram, J. E., David, J. R., Comerford, S. A. and Von Lichtenberg, F. (1991). Leishmania (Viannia) braziliensis: comparative pathology of golden hamsters infected with isolates from cutaneous and mucosal lesions of patients residing in Três Braços, Bahia, Brazil. American Journal of Tropical Medicine and Hygiene 44, 218–232. PMID: 1849379.CrossRefGoogle ScholarPubMed
Laurenti, M. D., Sotto, M. N., Corbett, C. E., da Matta, V. L. and Duarte, M. I. (1990). Experimental visceral leishmaniasis: sequential events of granuloma formation at subcutaneous inoculation site. International Journal of Experimental Pathology 71, 791–797. PMCID: PMC2002383.Google ScholarPubMed
Magalhães, A. V., Moraes, M. A. P., Raick, A. N., Llanos-Cuentas, E. A., Costa, J. M. L., Cuba, C. C. and Marsden, P. D. (1986). Histopatologia da leishmaniose tegumentar por Leishmania b. braziliensis. Padrões histológicos e estudo evolutivo das lesões. Revista do Instituto de Medicina Tropical de São Paulo 28, 253–262.CrossRefGoogle Scholar
Martinez, J. E., Travi, B. L., Valencia, A. Z. and Saravia, N. G. (1991). Metastatic capability of Leishmania (Viannia) panamensis and Leishmania (Viannia) guyanensis in golden hamsters. Journal of Parasitology 77, 762–768. PMID:1919926.CrossRefGoogle ScholarPubMed
Mendonça, S. C., Coutinho, S. G., Amendoeira, M. R. R., Marzochi, M. C. and Pirmez, C. (1986). Human American cutaneous leishmaniasis (Leishmania b. braziliensis) in Brazil: lymphoproliferative responses and influence of therapy. Clinical and Experimental Immunology 64, 269–276. PMCID: PMC1542340.Google ScholarPubMed
Morais-Teixeira, E., Carvalho, A. S., Costa, J. C., Duarte, S. L., Mendonça, J. S., Boechat, N. and Rabello, A. (2008). In vitro and in vivo activity of meglumine antimoniate produced at Farmanguinhos-Fiocruz, Brazil, against Leishmania (Leishmania) amazonensis, L (L.) chagasi and L (Viannia) braziliensis. Memórias do Instituto Oswaldo Cruz 103, 358–362. doi: 10.1590/S0074-02762008000400008.CrossRefGoogle ScholarPubMed
Osorio, Y., Melby, P. C., Pirmez, C., Chandrasekar, B., Guarín, N. and Travi, B. L. (2003). The site of cutaneous infection influences the immunological response and clinical outcome of hamsters infected with Leishmania panamensis. Parasite Immunology 25, 139–148. doi: 10.1046/j.1365-3024.2003.00615.x.CrossRefGoogle ScholarPubMed
Pereira, C. G., Silva, A. L., de Castilhos, P., Mastrantonio, E. C., Souza, R. A., Romão, R. P., Rezende, R. J., Pena, J. D., Beletti, M. E. and Souza, M. A. (2009). Different isolates from Leishmania braziliensis complex induce distinct histopathological features in a murine model of infection. Veterinary Parasitology 165, 231–240. doi: 10.1016/j.vetpar.2009.07.019.CrossRefGoogle Scholar
Pirmez, C., Marzochi, M. C. and Coutinho, S. G. (1988). Experimental canine mucocutaneous leishmaniasis (Leishmania braziliensis braziliensis). Memórias do Instituto Oswaldo Cruz 83, 145–151. doi: 10.1590/S0074-02761988000200001.CrossRefGoogle ScholarPubMed
Reithinger, R., Dujardin, J. C., Louzir, H., Pirmez, C., Alexander, B. and Brooker, S. (2007). Cutaneous leishmaniasis. Lancet Infectious Diseases 7, 581–596. http://dx.doi.org/10·1016/S1473-3099(07)70209-8.CrossRefGoogle ScholarPubMed
Rey, J. A., Travi, B. L., Valencia, A. Z. and Saravia, N. G. (1990). Infectivity of the subspecies of the Leishmania braziliensis complex in vivo and in vitro. American Journal of Tropical Medicine and Hygiene 43, 623–631. PMID: 2267967.CrossRefGoogle ScholarPubMed
Rocha, F. J., Schleicher, U., Mattner, J., Alber, G. and Bogdan, C. (2007). Cytokines, signaling pathways, and effector molecules required for the control of Leishmania (Viannia) braziliensis in mice. Infection and Immunity 75, 3823–3832. doi: 10.1128%2FIAI.01335-06.CrossRefGoogle ScholarPubMed
Salay, G., Dorta, M. L., Santos, N. M., Mortara, R. A., Brodskyn, C., Oliveira, C. I., Barbiéri, C. L. and Rodrigues, M. M. (2007). Testing of four Leishmania vaccine candidates in a mouse model of infection with Leishmania (Viannia) braziliensis, the main causative agent of cutaneous leishmaniasis in the New World. Clinical and Vaccine Immunology 14, 1173–1181. doi: 10.1128/CVI.00060-07.CrossRefGoogle Scholar
Sinagra, A., Riarte, A., Luna, C., Campanini, A. and Segura, E. L. (1997). Leishmania (Viannia) braziliensis: biological behavior in golden hamsters of isolates from Argentine patients. American Journal of Tropical Medicine and Hygiene 57, 115–118. PMID: 9242330.CrossRefGoogle ScholarPubMed
Soliman, M. F. (2006). The persistence, dissemination, and visceralization tendency of Leishmania major in Syrian hamsters. Acta Tropica 97, 146–150. doi: 10.1016/j.actatropica.2005.09.007.CrossRefGoogle ScholarPubMed
Souza-Lemos, C., de-Campos, S. N., Teva, A., Côrte-Real, S., Fonseca, E. C., Porrozzi, R. and Grimaldi, G. J. (2008). Dynamics of immune granuloma formation in a Leishmania braziliensis-induced self-limiting cutaneous infection in the primate Macaca mulatta. Journal of Pathology 216, 375–386. doi: 10.1002/path.2403.CrossRefGoogle Scholar
SVS-MS (Secretaria de Vigilância em Saúde, Ministério da Saúde, Brazil). Casos de leishmaniose tegumentar Americana. Brasil, grandes regiões e unidades federadas. http://portal.saude.gov.br/portal/arquivos/pdf/2012_11_casos_de_lta_entre_1990_e_2011.pdf.Google Scholar
Travi, B., Rey-Ladino, J. and Saravia, N. G. (1988). Behavior of Leishmania braziliensis s.l. in golden hamsters: evolution of the infection under different experimental conditions. Journal of Parasitology 74, 1059–1062. PMID: 3193329.CrossRefGoogle ScholarPubMed
Travi, B. L., Osorio, Y., Melby, P. C., Chandrasekar, B., Arteaga, L. and Saravia, N. G. (2002). Gender is a major determinant of the clinical evolution and immune response in hamsters infected with Leishmania spp. Infection and Immunity 70, 2288–2296. doi: 10.1128/IAI.70.5.2288-2296.2002.CrossRefGoogle Scholar
Wilson, H., Dieckmann, B. and Childs, G. (1979). Leishmania braziliensis and Leishmania mexicana: experimental cutaneous infections in golden hamsters. Experimental Parasitology 47, 270–283. doi: 10.1016/0014-4894(79)90079-1.CrossRefGoogle ScholarPubMed
Wilson, H. R. and Lollini, L. O. (1980). Leishmania braziliensis braziliensis: metastatic infection in a golden hamster. Transactions of Royal Society and Tropical Medicine and Hygine 74, 833. PMID: 7210144.CrossRefGoogle Scholar