Characterization of enteropathy in mice infected with Giardia duodenalis and treated with differing anti-parasite drugs
DOI:
https://doi.org/10.5433/1679-0359.2020v41n5p1625Keywords:
Giardia spp, Giardiasis, Parasitosis, Duodenum, Antiparasitic.Abstract
Our aim was to analyze the duodena of mice infected with Giardia duodenalis (assemblage A) after four different types of parasite treatment for enteropathy. Methods: Forty-eight male Swiss mice, 21 days of age, received 1000 parasite cysts orally. The animals were divided into six groups: negative (G1) and positive control (G2), and groups treated with nitazoxanide (G3), albendazole (G4), metronidazole (G5), and secnidazole (G6). After treatment they were sacrificed and the duodena were examined histopathologically. Results: In the positive control group G2, increased levels of neutral and acidic goblet cells, intraepithelial lymphocytes, and Paneth cells were found. There was a reduction in villus height and an increase in villus width; and crypts presented increased widths and depths. Hypertrophy in all layers of the intestinal wall and enterocytes was also observed. Conclusions: Metronidazole was the most effective in attenuating the enteropathy caused by G. duodenalis infection; reversing the increase in intraepithelial lymphocytes and Paneth cells, and attenuating the other elements investigated.Downloads
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References
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Mohammad, K. A., & Koshak, E. A. (2011). A prospective study on parasites among expatriate workers in Al-Baha from 2009-2011, Saudi Arabia. Journal of the Egyptian Society of Parasitology., 41(2), 423-432.
Mokrzycka, M., Kolasa, A., Kosierkiewicz, A., & Wiszniewska, B. (2010). Inducible nitric oxide synthase in duodenum of children with Giardia lamblia infection. Folia Histochemica et Cytobiolica, 48(2), 191-196. doi: 10.2478/v10042-008-0111-7
Muller, N., & Allmen, N. (2005). Recent insights into the mucosal reactions associated with Giardia lamblia infections. International Journal Parasitology., 35(13), 1339-1347. doi: 10.1016/j.ijpara.2005.07.008
Myers, B. M. (2008). Carbohydrates. In J. D. Bancroft, M. Gamble, Theory and practice of histological techniques (7nd ed., pp. 110). Philadelphia: Elsevier.
Neiva, V. A., Ribeiro, M. N. S., Nascimento, F. R.F., Cartagenes M. S. S., Moraes, D. F. C, Amaral, F. M. M. (2014). Plant species used in giardiasis treatment: ethnopharmacology and in vitro evaluation of anti-Giardia activity. Revista Brasileira de Farmacognosia., 24(2), 215-224. doi: 10.1016/j.bjp. 2014.04.004
Pavanelli, M. F., Garcia, T. I., & Colli, C. M. (2016). Eficácia de fármacos contra Giardia muris em camundongos swiss naturalmente infectados. Campo Digit@l, 11(1), 1-7.
Pérez, R. A., Hernandez, J. M., Castilio, R. A., Yepez, M. L., Castilio, R., Nogueda, B.,… Hernandez, L. F. (2013). Albendazole and its derivative JVG9 induce encystation on Giardia intestinalis trophozoites. Parasitology Research, 112(9), 3251-3257. doi: 10.1007/s00436-013-3521-1
Ponce-Macotela, M., Gonzalez, M. A., Reunoso, R. R., & Martinez, G. M. N. (2008). Goblet cells: are they an unspecific barrier against Giardia intestinalis or a gate? Parasitology Research, 102(3), 509-513. doi: 10.1007/s00436-007-0790-6
Pupulin, A. R. T., Gomes, M. L., Dias, M. L. G., & Araujo, S. M. (2004) Giardíase em creches do município de Maringá, PR. Revista Brasileira de Analises Clinicas, 36(3), 147-149.
Read, C. M., Monis, P. T., & Thompson, R. C. A. (2004). Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infection Genetics and Evolution, 4(2), 125-130. doi: 10.1016/j.meegid.2004.02.001
Rey, L. (2011). Bases da parasitologia médica (4nd ed.). Rio de Janeiro: Guanabara Koogan.
Reynoldson, J. A., Thompson, R. C. A., & Meloni, B. P. (1991). In vivo efficacy of albendazole against Giardia duodenalis in mice. Parasitology Research, 77(4), 325-328. doi: 10.1007/BF00930909
Rossignol, J. F. (2010). Cryptosporidium and Giardia: treatment options and prospects for new drugs. Experimental Parasitoly, 124(1), 45-53. doi: 10.1016/j.exppara.2009.07.005
Savioli, L., Smith, H., & Thompson, A. (2006). Giardia and Cryptosporidium join the “neglected diseases initiative”. Trends in Parasitology, 22(5), 203-208. doi: 10.1016/j.pt.2006.02.015
Shukla, G., Klaur, H., & Sharma, L. (2013). Comparative therapeutic effect of probiotic Lactobacillus casei alone and in conjunction with antiprotozoal drugs in murine giardiasis. Parasitology Research, 112(6), 2143-2149. doi: 10.1007/s00436-013-3394-3
Shukla, G., Sidhu, R. K., & Verma, A. (2012). Restoration of anthropometric, biochemical and histopathological alterations by Lactobacillus casei supplementation in Giardia intestinalis infected renourished BALB/c mice. Antonie Van Leeuwenhoek, 102(1), 61-72. doi: 10.1007/s10482-012-9713-3
Tako, E. A., Hassimi, M. F., Li, E., & Singer, S. M. (2013). Transcriptomic analysis of the host response to Giardia duodenalis infection reveals redundant mechanisms for parasite control. The American Society for Microbiology, 4(6), 660-663. doi: 10.1128/mBio.00660-13.
Troeger, H., Epple, H. J., Schneider, T., Wahnschaffe, U., Ullrich, R., Fromm, M.,… Burchard, G. D. (2013). Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut Journal in Gastroenterology and Hepatology, 56(3), 328-335. doi: 10.1136/gut.2006.100198
Upcroft, P., & Upcroft, J. A. (2001). Drug targets and mechanisms of resistance in the anaerobic protozoa. Clinical Microbiology Review, 14(1), 150-164. doi: 10.1128/CMR.14.1.150-164.2001
Ventura, L. L. A., Oliveira, D. R., Viana, J. C., Santos, J. F., Calliarim, V., & Gomes, M. A. (2013). Impact of protein malnutrition on histological parameters of experimentally infected animals with Giardia lamblia. Experimental Parasitology, 133(4), 391-395. doi: 10.1016/j.exppara.2013.01.007
Venturini, C. D., Engrof, P., Ely, L. S., Tasca, T., & Cart, G. A. (2014). Interações entre antiparasitários e alimentos. Revista de Ciências Farmacêuticas Básica Aplicada, 35(1), 17-23.
Vivas, L. A. M., Jamel, N., & Refinetti, R. A. (2007). Anesthetic experimental device for small animal. Acta Cirúrgica Brasileira, 22(3), 229-233. doi: 10.1590/S0102-86502007000300012
Zieske, J. D., & Bernstein, I. A. (1982). Modification of cell surface glycoprotein: addition of fucosyl residues during epidermal differentiation. Journal of Cell Biology, 95(2), 626-631. doi: 10.1083/jcb.95.2.626
Arevalo, F., Aragón, V., Morales, D., Caramutti, D., Arandia J., Alcocer, G. (2010). Duodenal villous atrophy, an unexpectedly common finding in Giardia lamblia infestation. Revista de Gastroenterologia del Peru, 30(4), 272-276.
Arguello, G. R., Cruz, S. M., Romero, M. L., & Ortega, P. G. (2004). Variability and variation in drug susceptibility among Giardia duodenalis isolates and clones exposed to 5-nitroimidazoles and benzimidazoles in vitro. Journal of Antimicrobial Chemotherapy, 54(4), 711-721. doi: 10.1093/jac/dkh388
Bailey, C., Lopez, S., Camero, A., Taiquiri, C., Arthuary, Y., & Moore, D. A. (2013). Factors associated with parasitic infection amongst street children in orphanages across Lima, Peru. Pathogens and Global Health, 107(2), 52-57. doi: 10.1179/2047773213Y.0000000073
Bartelt, A. L., Roche, J., Kolling, G., Bolick, D., Noronha, F., Naylor, C.,… Guerant, R. (2013). Persistent G. lamblia impairs growth in a murine malnutrition model. The Journal of Clinical Invesigationt, 123(6), 2672-2684. doi: 10.1172/JCI67294
Beamish, R. J. (1972). Lethal pH for white sucker Catostomus commersoni (Lacépedè). Transation of the American Fisheries Society, 101(2), 335-358. doi: 10.1577/1548-8659(1972)101<355:LPFTWS> 2.0.CO;2
Coelho, C. H., Durigan, M., Leal, D. A. G., Schneider, A. D. B., Franco, R. M. B., & Singer S. M. (2017). Giardiasis as a neglected disease in Brazil: Systematic review of 20 years of publications. PLoS Neglected Tropical Diseases, 11(10): e0006005. doi: 10.1371/journal.pntd.0006005
Cruz, C. C. P., Ferrari, L., & Sogayar, R. (1997). Ensaio terapêutico na infecção por Giardia muris em camundongo com metronidazole, tinidazole, secnidazole e furazolidone. Revista da Sociedade Brasileira de Medicina Tropical, 30(3), 223-228. doi: 10.1590/S0037-86821997000300009
Eckmann, L. (2003). Mucosal defences against Giardia. Parasite Immunology., 25(5), 259-279. doi: 10.1046/j.1365-3024.2003.00634.x
Elia, C. C. S., & Souza, H. S. P. (2001). Imunologia da mucosa intestinal: da bancada ao leito. Rio de Janeiro: Atheneu.
Eligio, G., Cortes, C., & Jimenes, C. (2008). Classification of Giardia intestinalis isolates by multiple polymerase chain reaction (multiplex). Parasitol Research., 103(4), 797-800. doi: 10.1007/s00436-008-1042-0
Faust, E. C., D'antoni, J. S., Odom, V., Miller, M. J., Peres, C., Sawitz, W.,… Walker, H., (1938). A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces. I. Preliminary communication. The American Journal Of Tropical Medicine and Hygiene., 18(2), 169-183. doi: 10.4269/ajtmh.1938.s1-18.169
Feng, Y., Xiao, L. (2011). Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Reviews., 24(1), 110-140. doi: 10.1128/CMR.00033-10.
Gartner, L. P., & Hiatt, J. L. (2007). Tratado de histologia em cores (3a ed.). Rio de Janeiro: Guanabara Koogan.
Hellard, F. P., Sinclair, M. L., Hogg, G. G., & Fairley, C. K. (2000). Prevalence of enteric pathogens among community based asymptomatic individuals. Journal of Gastroenterology and Hepatololy Resserch., 15(3), 290-293. doi: 10.1046/j.1440-1746.2000.02089.x
Hensel, K. O., Boland, V., Postberg, J., Zilbauer, M., Heuschkel, R., Godde, D.,… Vogel, S. (2014). Differential expression of mucosal trefoil factors and mucins in pediatric inflammatory bowel diseases. Scientifc Reports., 4, 7343. doi: 10.1038/srep07343
Karanis, P., Kourenti, C., & Smith, H. (2007). Waterborne transmission of protozoan parasites worldwide review of outbreaks and lessons learnt. Jounal Water Health., 5(1), 1-38. doi: 10.1016/j.watres.2017.01.036
Linda, C. H., Huang, C. Y., Kuo, W. T., Sayer, H., Turner, J. R., & Buret, A. G. (2008). SGLT-1-mediated glucose uptake protects human intestinal epithelial cells against Giardia duodenalis-induced apoptosis. International Jounal Parasitology., 38(8), 923-934. doi: 10.1016/j.ijpara.2007.12.
Mohammad, K. A., & Koshak, E. A. (2011). A prospective study on parasites among expatriate workers in Al-Baha from 2009-2011, Saudi Arabia. Journal of the Egyptian Society of Parasitology., 41(2), 423-432.
Mokrzycka, M., Kolasa, A., Kosierkiewicz, A., & Wiszniewska, B. (2010). Inducible nitric oxide synthase in duodenum of children with Giardia lamblia infection. Folia Histochemica et Cytobiolica, 48(2), 191-196. doi: 10.2478/v10042-008-0111-7
Muller, N., & Allmen, N. (2005). Recent insights into the mucosal reactions associated with Giardia lamblia infections. International Journal Parasitology., 35(13), 1339-1347. doi: 10.1016/j.ijpara.2005.07.008
Myers, B. M. (2008). Carbohydrates. In J. D. Bancroft, M. Gamble, Theory and practice of histological techniques (7nd ed., pp. 110). Philadelphia: Elsevier.
Neiva, V. A., Ribeiro, M. N. S., Nascimento, F. R.F., Cartagenes M. S. S., Moraes, D. F. C, Amaral, F. M. M. (2014). Plant species used in giardiasis treatment: ethnopharmacology and in vitro evaluation of anti-Giardia activity. Revista Brasileira de Farmacognosia., 24(2), 215-224. doi: 10.1016/j.bjp. 2014.04.004
Pavanelli, M. F., Garcia, T. I., & Colli, C. M. (2016). Eficácia de fármacos contra Giardia muris em camundongos swiss naturalmente infectados. Campo Digit@l, 11(1), 1-7.
Pérez, R. A., Hernandez, J. M., Castilio, R. A., Yepez, M. L., Castilio, R., Nogueda, B.,… Hernandez, L. F. (2013). Albendazole and its derivative JVG9 induce encystation on Giardia intestinalis trophozoites. Parasitology Research, 112(9), 3251-3257. doi: 10.1007/s00436-013-3521-1
Ponce-Macotela, M., Gonzalez, M. A., Reunoso, R. R., & Martinez, G. M. N. (2008). Goblet cells: are they an unspecific barrier against Giardia intestinalis or a gate? Parasitology Research, 102(3), 509-513. doi: 10.1007/s00436-007-0790-6
Pupulin, A. R. T., Gomes, M. L., Dias, M. L. G., & Araujo, S. M. (2004) Giardíase em creches do município de Maringá, PR. Revista Brasileira de Analises Clinicas, 36(3), 147-149.
Read, C. M., Monis, P. T., & Thompson, R. C. A. (2004). Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infection Genetics and Evolution, 4(2), 125-130. doi: 10.1016/j.meegid.2004.02.001
Rey, L. (2011). Bases da parasitologia médica (4nd ed.). Rio de Janeiro: Guanabara Koogan.
Reynoldson, J. A., Thompson, R. C. A., & Meloni, B. P. (1991). In vivo efficacy of albendazole against Giardia duodenalis in mice. Parasitology Research, 77(4), 325-328. doi: 10.1007/BF00930909
Rossignol, J. F. (2010). Cryptosporidium and Giardia: treatment options and prospects for new drugs. Experimental Parasitoly, 124(1), 45-53. doi: 10.1016/j.exppara.2009.07.005
Savioli, L., Smith, H., & Thompson, A. (2006). Giardia and Cryptosporidium join the “neglected diseases initiative”. Trends in Parasitology, 22(5), 203-208. doi: 10.1016/j.pt.2006.02.015
Shukla, G., Klaur, H., & Sharma, L. (2013). Comparative therapeutic effect of probiotic Lactobacillus casei alone and in conjunction with antiprotozoal drugs in murine giardiasis. Parasitology Research, 112(6), 2143-2149. doi: 10.1007/s00436-013-3394-3
Shukla, G., Sidhu, R. K., & Verma, A. (2012). Restoration of anthropometric, biochemical and histopathological alterations by Lactobacillus casei supplementation in Giardia intestinalis infected renourished BALB/c mice. Antonie Van Leeuwenhoek, 102(1), 61-72. doi: 10.1007/s10482-012-9713-3
Tako, E. A., Hassimi, M. F., Li, E., & Singer, S. M. (2013). Transcriptomic analysis of the host response to Giardia duodenalis infection reveals redundant mechanisms for parasite control. The American Society for Microbiology, 4(6), 660-663. doi: 10.1128/mBio.00660-13.
Troeger, H., Epple, H. J., Schneider, T., Wahnschaffe, U., Ullrich, R., Fromm, M.,… Burchard, G. D. (2013). Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut Journal in Gastroenterology and Hepatology, 56(3), 328-335. doi: 10.1136/gut.2006.100198
Upcroft, P., & Upcroft, J. A. (2001). Drug targets and mechanisms of resistance in the anaerobic protozoa. Clinical Microbiology Review, 14(1), 150-164. doi: 10.1128/CMR.14.1.150-164.2001
Ventura, L. L. A., Oliveira, D. R., Viana, J. C., Santos, J. F., Calliarim, V., & Gomes, M. A. (2013). Impact of protein malnutrition on histological parameters of experimentally infected animals with Giardia lamblia. Experimental Parasitology, 133(4), 391-395. doi: 10.1016/j.exppara.2013.01.007
Venturini, C. D., Engrof, P., Ely, L. S., Tasca, T., & Cart, G. A. (2014). Interações entre antiparasitários e alimentos. Revista de Ciências Farmacêuticas Básica Aplicada, 35(1), 17-23.
Vivas, L. A. M., Jamel, N., & Refinetti, R. A. (2007). Anesthetic experimental device for small animal. Acta Cirúrgica Brasileira, 22(3), 229-233. doi: 10.1590/S0102-86502007000300012
Zieske, J. D., & Bernstein, I. A. (1982). Modification of cell surface glycoprotein: addition of fucosyl residues during epidermal differentiation. Journal of Cell Biology, 95(2), 626-631. doi: 10.1083/jcb.95.2.626
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2020-06-17
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Elias, M. A., Pavanelli, M. F., Melo, G. de A. N. de, & Sant´Ana, D. de M. G. (2020). Characterization of enteropathy in mice infected with Giardia duodenalis and treated with differing anti-parasite drugs. Semina: Ciências Agrárias, 41(5), 1625–1638. https://doi.org/10.5433/1679-0359.2020v41n5p1625
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