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Experimental mixed infection of Leishmania (Leishmania) amazonensis and Leishmania (L.) infantum in hamsters (Mesocricetus auratus)

Published online by Cambridge University Press:  10 May 2017

JORDANNA LUÍZA DE LIMA CELESTE ,
ANA PAULA VENUTO MOURA ,
JOÃO CARLOS FRANÇA-SILVA ,
GABRIELA MATOS DE SOUSA ,
SORAIA OLIVEIRA SILVA ,
MARIA NORMA MELO ,
WAGNER LUIZ TAFURI ,
CAROLINA CARVALHO SOUZA  and
HÉLIDA MONTEIRO DE ANDRADE
JORDANNA LUÍZA DE LIMA CELESTE
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
ANA PAULA VENUTO MOURA
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil Departamento de Biologia Geral, Universidade Estadual de Montes Claros, CEP: 39·401-089, Montes Claros, Minas Gerais, Brazil
JOÃO CARLOS FRANÇA-SILVA
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
GABRIELA MATOS DE SOUSA
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
SORAIA OLIVEIRA SILVA
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
MARIA NORMA MELO
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
WAGNER LUIZ TAFURI
Affiliation:
Departamento de Patologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
CAROLINA CARVALHO SOUZA
Affiliation:
Departamento de Patologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil Centro de Ciências Biológicas e da Saúde, CCBS, Universidade Federal do Oeste da Bahia, UFOB, - CEP: 47·808-020, Barreiras, Bahia, Brazil
HÉLIDA MONTEIRO DE ANDRADE*
Affiliation:
Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil
*
*Corresponding author: Departamento de Parasitologia, ICB, Universidade Federal de Minas Gerais, CP: 486 – CEP: 31·270-901, Belo Horizonte, Minas Gerais, Brazil. E-mail: helidandrade@gmail.com
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Summary

In South America, visceral leishmaniasis is frequently caused by Leishmania infantum and, at an unknown frequency, by Leishmania amazonensis. Therefore, mixed infections with these organisms are possible. Mixed infections might affect the clinical course, immune response, diagnosis, treatment and epidemiology of the disease. Here we describe the clinical course of mixed infections with L. amazonensis and L. infantum in a hamster model. We show that mixed infections are associated with more severe clinical disease than infection with L. amazonensis or L. infantum alone. In spleens with mixed infections, L. infantum outcompeted L. amazonensis in the tissue, but not in culture from tissue. We found increased levels of IgG in animals infected with L. infantum. Although more than 30 bands were revealed in a Western blot, the highest immunogenicity was observed with proteins having molecular masses of 95 and 90 kDa, whereas proteins with molecular masses of lower than 50 kDa were reactive frequently with serum from hamsters infected with L. amazonensis, and proteins with molecular masses of 80 and 70 kDa were reactive only with serum from hamsters infected with L. infantum. This finding has important implications regarding the biology of Leishmania and humoral immune responses to infections with these organisms.

Keywords

experimental infectionLeishmania infantumLeishmania amazonensismixed infectionclinical coursehumoral immune response
Type
Research Article
Information
Parasitology , Volume 144 , Issue 9 , August 2017 , pp. 1191 - 1202
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Copyright
Copyright © Cambridge University Press 2017 

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References

Abdullah, S. M., Flath, B. and Presber, W. (1998). Mixed infection of human U-937 cells by two different species of Leishmania . The American Journal of Tropical Medicine and Hygiene 59, 182–188.Google Scholar
Abreu-Silva, A. L., Calabrese, K. S., Cupolilo, S. M. N., Cardoso, F. O., Souza, C. S. F. and Gonçalves Da Costa, S. C. (2004). Histopathological studies of visceralized Leishmania (Leishmania) amazonensis in mice experimentally infected. Veterinary Parasitology 121, 179–187.Google Scholar
al-Diwany, L. J., al-Awkati, N. A., Atia, M. and Rassam, M. B. (1995). Concomitant natural infection with L. donovani and L. major: a case report from Iraq. Sozial-und Praventivmedizin 40, 234–238.Google Scholar
Antoniou, M., Doulgerakis, C., Pratlong, F., Dedet, J. P. and Tselentis, Y. (2004). Short report: treatment failure due to mixed infection by different strains of the parasite Leishmania infantum . The American Journal of Tropical Medicine and Hygiene 71, 71–72.Google Scholar
Babiker, A. M., Ravagnan, S., Fusaro, A., Hassan, M. M., Bakheit, S. M., Mukhtar, M. M., Cattoli, G. and Capelli, G. (2014). Concomitant infection with Leishmania donovani and L. major in single ulcers of cutaneous leishmaniasis patients from Sudan. Journal of Tropical Medicine 2014, Article ID 170859.Google Scholar
Bañuls, A. L., Hide, M. and Tibayrenc, M. (1999). Molecular epidemiology and evolutionary genetics of Leishmania parasites. International Journal for Parasitology 29, 1137–1147.Google Scholar
Barral, A., Badaró, R., Barral-Netto, M., Grimaldi, G. Jr., Momem, H. and Carvalho, E. M. (1986). Isolation of Leishmania mexicana amazonensis from the bone marrow in a case of american visceral leishmaniasis. The American Journal of Tropical Medicine and Hygiene 35, 732–734.Google Scholar
Barral, A., Pedral-Sampaio, D., Grimaldi, G. Jr., Momen, H., McMahon-Pratt, D., de Jesus, A. R., Almeida, R. B., Badaro, R., Barral-Netto, M., Carvalho, E. M. and Johnson, W. D. Jr. (1991). Leishmaniasis in Bahia, Brazil: evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. The American Journal of Tropical Medicine and Hygiene 44, 536–546.Google Scholar
Bretagne, S., Durand, R., Olivi, M., Garin, J. F., Sulahian, A., Rivollet, D., Vidaud, M. and Deniau, M. (2001). Real-time PCR as a new tool for quantifying Leishmania infantum in liver in infected mice. Clinical Diagnosis Laboratory Immunology 8, 828–831.Google Scholar
Bruna-Romero, O., Hafalla, C. R., González-Aseguinolaza, G., Sano, G. I., Tsuji, M. and Zavala, F. (2001). Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. International Journal for Parasitology 31, 1499–1502.Google Scholar
Bruzual, E., Arcay, L. and Parte-Pérez, M. (2008). Diseminación tisular y efectos histopatológicos producidos por Leishmania mexicana amazonensis en roedores infectados experimentalmente. Revista de la Sociedad Venezolana de Microbiología 28, 139–144.Google Scholar
Campos-Neto, A. and Bunn-Moreno, M. M. (1982). Polyclonal B cell activation in hamsters infected with parasites of the genus Leishmania . Infection and Immunity 38, 871–876.Google Scholar
Cuquerella, M., Gómez-Muñoz, M. T. and Alunda, J. M. (1991). Serum IgG response of Manchego lambs to infections with Haemonchus contortus and preliminary characterization of adult antigens. Veterinary Parasitology 38, 131–143.Google Scholar
das Moreira, N. D., Vitoriano-Souza, J., Roatt, B. M., de Vieira, P. M. A., Ker, H. G., de Oliveira Cardoso, J. M., Giunchetti, R. C., Carneiro, C. M., de Lana, M. and Reis, A. B. (2012). Parasite Burden in Hamsters infected with two different strains of Leishmania (Leishmania) infantum: “Leishman Donovan Units” versus real-time PCR. PLoS ONE 7, e-47907.Google Scholar
Evans, D. (1989). Handbook on Isolation, Characterization and Cryopreservation of Leishmania. World Health Organization, Geneva.Google Scholar
Gramiccia, M. (2011). Recent advances in leishmaniosis in pet animals: epidemiology, diagnostics and anti-vectorial prophylaxis. Veterinary Parasitology 181, 23–30.Google Scholar
Gramiccia, M. and Gradoni, L. (2005). The current status of zoonotic leishmaniasis and approaches to disease control. International Journal for Parasitology 35, 1169–1180.CrossRefGoogle ScholarPubMed
Ibrahim, M. E., Smyth, A. J., Ali, M. H., Barker, D. C. and Kharazmi, A. (1994). The polymerase chain reaction can reveal the occurrence of naturally mixed infections with Leishmania parasites. Acta Tropica 57, 327–332.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.Google Scholar
Martinez, E., Mollinedo, S., Torrez, M., Muñoz, M. and Bañuls, A. L. (2002). Co-infection by Leishmania amazonensis and L. infantum/L. chagasi in a case of diffuse cutaneous leishmaniasis in Bolivia. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 529–532.CrossRefGoogle Scholar
McLaren, M. L., Lillywhite, J. E. and Sirr, S. (1980). A Laboratory Method for IFAT and ELISA. The Ross Institute of Tropical Hygiene, London School of Hygiene and Tropical Medicine, London.Google Scholar
Mebrahtu, Y. B., Lawyer, P. G., Hendricks, L. D., Muigai, R., Oster, C. N., Perkins, P. V., Koech, D. K., Pamba, H. and Roberts, C. R. (1991). Concurrent infection with Leishmania donovani and Leishmania major in a Kenyan patient – clinical description and parasite characterization. The American Journal of Tropical Medicine and Hygiene 45, 290–296.Google Scholar
Monroy-Ostria, A., Nasereddin, A., Monteon, V. M., Guzmán-Bracho, C. and Jaffe, C. L. (2014). ITS1 PCR-RFLP diagnosis and characterization of Leishmania in clinical samples and strains from cases of human cutaneous leishmaniasis in states of the Mexican Southeast. Interdisciplinary Perspectives on Infectious Diseases 2014, Article ID 607287.Google Scholar
Oliveira Neto, M. P., Marzochi, M. C., Grimaldi, G. Jr., Pacheco, R. S., Toledo, L. M. and Momen, H. (1986). Concurrent human infection with Leishmania donovani and Leishmania braziliensis braziliensis . Annals of Tropical Medicine and Parasitology 80, 587–592.Google Scholar
Requena, J. M., Soto, M., Doria, M. D. and Alonso, C. (2000). Immune and clinical parameters associated with Leishmania infantum infection in the golden hamster model. Veterinary Immunology and Immunopathology 76, 269–281.Google Scholar
Schönian, G., Nasereddin, A., Dinse, N., Schweynoch, C., Schallig, H. d. f. H., Presber, W. and Jaffe, C. L. (2003). PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagnostic Microbiology and Infectious Disease 47, 349–358.Google Scholar
Shirian, S., Oryan, A., Hatam, G. R. and Daneshbod, Y. (2012). Mixed mucosal leishmaniasis infection caused by Leishmania tropica and Leishmania major . Journal of Clinical Microbiology 50, 3805–3808.Google Scholar
Silveira, F. T., Lainson, R., Shaw, J. J. and Ribeiro, R. S. M. (1984). Leishmaniose cutânea na Amazônia. Registro do primeiro caso humano de infecção mista, determinado por duas espécies distintas de Leishmania: Leishmania braziliensis e Leishmania mexicana amazonensis . Revista do Instituto de Medicina Tropical de São Paulo 26, 272–275.Google Scholar
Tafuri, W. L., Santos, R. L., Arantes, R. M., Gonçalves, R., De Melo, M. N., Michalick, M. S. and Tafuri, W. L. (2004). An alternative immunohistochemical method for detecting Leishmania amastigotes in paraffin-embedded canine tissues. Journal of Immunological Methods 292, 17–23.CrossRefGoogle ScholarPubMed
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