Combination of immunostimulants with moxidectin in the treatment of animals experimentally infected with Haemonchus contortus
DOI:
https://doi.org/10.5433/1679-0359.2021v42n2p707Palabras clave:
Infection, Treatment, Adjuvants, Anthelmintics.Resumen
Considering the importance of Haemonchus contortus infection in herds along with parasitic resistance, the goal of this study was to evaluate the influence of the administration of adjuvants alone or in combination with anthelmintics for the treatment of H. contortus, in experimentally infected sheep. Thirty sheep of the Texel breed of both genders, raised in a herd located in the subtropical region of Brazil, were used in this experiment. Experimental infection with H. contortus was performed in sheep, and the infected sheep were then separated into groups for the administration of antiparasitic and immunostimulant drugs. The results obtained from the excretion of eggs per gram of feces and the count of parasites during necropsy affirm that the use of adjuvants in combination with anthelmintics is associated with higher efficacy of treatment, lower rate of reinfection, and retardation in the development of anthelmintic drug resistance by H. contortus. Based on these results, we can conclude that the combination of anthelmintics and immunostimulants may favor potential anthelmintic treatments for H. contortus.Métricas
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Alba-Hurtado, F., & Muñoz-Guzmán, M. A. (2013). Immune responses associated with resistance to haemonchosis in sheep. BioMed Research International, 2013, 1-11. doi: 10.1155/2013/162158
Albers, G. A. A., Gray, G. D., Piper, L. R., Barker, J. S. F., Jambre, L. F., & Barger, I. A. (1987). The genetics of resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal of Parasitology, 17(7), 1355-1363. doi: 10.1016/0020-7519(87)90103-2
Almeida, F. A., Garcia, K. C., Torgerson, P. R., & Amarante, A. F. T. (2010). Multiple resistance to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International, 59, 622-625. doi: 10.1016/j.parint.2010.09.006
Amarante, A. F. T. (2001). Controle de endoparasitoses dos ovinos. In W. R. S. Mattos (Ed.), A produção animal na visão dos brasileiros (pp. 461-473). Piracicaba: Fealq/SBZ.
Amarante, A. F. T. (2014). Os parasitas de ovinos. São Paulo: Editora UNESP.
Amarante, A. F. T., & Amarante, M. R. V. (2003). Breeding sheep for resistance to nematode infections. Journal of Animal and Veterinary Advances, 2(3), 147-161. doi: 10.1079/9781845935559.0279
Amarante, A. F. T., Bricarello, P. A., Rocha, R. A., & Gennari, S. M. (2004). Resistance of Santa Ines, Suffolk and Ile de France sheep to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 120(1), 91-106. doi: 10.1016/j.vetpar.2003.12.004
Amarante, F. A., Garcia, K. C., Togerson, P. R., & Amarante, A. F. T. (2010). Multiple resitence to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International, 59, 622-625. doi: 10.1016/j.parint.2010.09.006.
ArunKumar, S., Abdul Basith, S., & Gomathinayagam, S. (2012). A comparative analysis on serum antibody levels of sheep immunized with crude and thiol-purified excretory secretory antigen of Haemonchus contortus. Veterinary World, 5(5), 279-284. doi: 10.5455/vetworld.2012.279-284
Audibert, F. (2003). Adjuvants for vaccines, a quest. International Immunopharmacology, 3, 1187-1193. doi: 10.1016/S1567-5769(03)00011-0
Bartley, D. J., Mcarthur, C. L., Devin, L. M., Sutra, J. F., Morrison, A. A., Lespine, A., & Matthews, J. B. (2012). Characterization of macrocyclic lactone resistance in two field-derived isolates of Cooperia oncophora. Veterinary Parasitology, 190, 454-460. doi: 10.1016/j.vetpar.2012.07.022
Bowman, D. D. (2006). Parasitologia veterinária de Georgis (8a ed.). Barueri: Manole.
Braga, E. G., Ananias, R. Z., Mussalem, J. S., Squaiella, C. C., Longhini, A. L. F., Mariano, M.,... Longo-Maugéri, I. M. (2003). Treatment with Propionibacterium acnes modulates the late phase reaction of immediate hypersensitivity in mice. Immunology Letters, 88(2), 163-169. doi: 10.1016/S0165-2478(03) 00079-8
Buzzulin, C., Costa, A. J., Santos, T. R., Borges, F. A., & Soares, V. E. (2007). Eficácia anti-helmíntica comparativa da associação albendazole, levamisole e ivermectina à moxidectina em ovinos. Pesquisa Agropecuária Brasileira, 42(6), 891-895. doi: 10.1590/S0100-204X2007000600017
Cezar, A. S., Toscan, G., Camillo, G., Sangioni, L. A., Ribas, H. O., & Vogel, F. S. F. (2010). Multiple resistance of gastrointestinal nematodes to nine different drugs in a sheep flock in southern Brazil. Veterinary Parasitology, 173, 157-160. doi: 10.1016/j.vetpar.2010.06.013
Climeni, B. S. O., Monteiro, M. V., Cicoti, C. A., & Neves, M. F. (2008). Hemoncose ovina. São Paulo: Editora FAEF.
Coles, G. C., Coles, G. C., Bauer, C., Borgsteede, F. H. M., Geerts, S., Klei, T. R.,... Waller, P. J. World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology, 44, 35-44. doi: 10.1016/0304-4017(92)90141-U
Cunha, L. F. C. D., Fº., Pereira, A. B. D. L., & Yamamura, M. H. (1998). Resistência a anti-helmínticos em ovinos da região de Londrina - Paraná - Brasil. Semina: Ciências Agrárias, 19(1), 31-37.
Domke, A. V., Chartier, C., Gjerde, B., Höglund, J., Leine, N., Vatn, S., & Stuen, S. (2012) Prevalence of anthelmintic resistance in gastrointestinal nematodes of sheep and goats in Norway. Parasitology Research, 111, 185-193. doi: 10.1007/s00436-012-2817-x
Fausto, G. C., Pivoto, F. L., Costa, M. M., Lopes, S. T. A., França, R. T., Molento, M. B.,... Leal, M. L. R. (2014). Protein profile of lambs experimentally infected with Haemonchus contortus and supplemented with selenium and copper. Parasites & Vectors, 7355. doi: 10.1186/1756-3305-7-355
Hohenhaus, M. A., & Outteridge, P. M. (1995). The immunogenetics of resistance to Trichostrongylus colubriformis and Haemonchus contortus parasites in sheep. British Veterinary Journal, 151, 119-141. doi: 10.1016/S0007-1935(95)80004-2
Howell, S. B., Burke, J. M., Miller, J. E., Terrill, T. H., Valencia, E., Williams, M. J.,… Kaplan, R. M. (2008). Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. Journal of the American Veterinary Medical Association, 233(12), 1913-1919. doi: 10.2460/javma.233. 12.1913
Keane, O. M., Keegan, J. D., Good, B., Waal, T., Fanning, J., Gottstein, M.,… Sheehan, M. (2014). High level of treatment failure with commonly used anthelmintics on Irish sheep farms. Irish Veterinary Journal, 67, 16. doi: 10.1186/2046-0481-67-16
Kooyman, F. N., Van Kooten, P. J., Huntley, J. F., Mackellar, A., Cornelissen, A. W., & Schallig, H. D. (1997). Production of a monoclonal antibody specific for ovine immunoglobulin E and its application to monitor serum IgE responses to Haemonchus contortus infection. Parasitolology, 114, 395-406. doi: 10. 1017/S0031182096008633
Kotze, A. C., & Prichard, R. K. (2016). Chapter nine - anthelmintic resistance in Haemonchus contortus: history, mechanisms and diagnosis. Advances in Parasitology, 93, 397-428. doi: 10.1016/bs.apar.2016. 02.012
Lawrence, C. E. (2003). Is there a common mechanism of gastrointestinal nematode expulsion? Parasite Immunology, 25, 271-281. doi: 10.1046/j.1365-3024.2003.00630.x
Le Jambre, L. F. (1995). Relationship of blood loss to worm numbers, biomass and egg production in Haemonchus infected sheep. International Journal of Parasitology, 25(3), 269-273. doi: 10.1016/0020-7519(94)00118-8
Love, S., Neilson, F., Biddle, A. J., & Mckinnon, R. (2003). Moxidectin-resistant Haemonchus contortus in sheep in northern New South Wales. Australian Veterinary Journal, 81(6), 359-360. doi: 10.1111/j. 1751-0813.2003.tb11514.x
Martins, S. M. F. M., Garcia, M., Chate, S. C., Tavolari, F. A., Teixeira, R. B. C., Matins, L. R., Jr.,… Abel, L. J. (2012). (2012). Association of immunostimulant with anthelmintic on the treatment of sheep verminosis. Ciência Rural, 4(12), 2229-2234. doi: 10.1590/S0103-84782012005000142
Martínez-Valladares, M., Geurden, T., Bartram, D. J., Martínez-Pérez, J. M., Robles-Pérez, D., Bohórquez, A.,… Rojo-Vázquez, F. A. (2015). Resistance of gastrointestinal nematodes to the most commonly used anthelmintics in sheep, cattle and horses in Spain. Veterinary Parasitology, 211, 228-233. doi: 10.1016/ j.vetpar.2015.05.024
Mitchell, E. S. E., Hunt, K. R., Wood, R., & McLean, B. (2010). Anthelmintic resistance on sheep farms in wales. Veterinary Record, 166, 651-652. doi: 10.1136/vr.b4840
Molento, M. B., Tasca, C., Gallo, A., Ferreira, M., Bononi, R., & Stecca, E. (2004). Método Famacha como parâmetro clínico individual de infecção por Haemonchus contortus em pequenos ruminantes. Ciência Rural, 34(4), 1139-1145.
Nagata, W. B., Panegossi, M. F. C., Bresciani, K. D. S., Gomes, J. F., Kaneto, C. N., & Perri, S. H. (2019). Resistance of gastrointestinal nematodes to five different active principles ins sheep infected naturally in São Paulo State, Brazil. Small Ruminant Research, 172, 48-50. doi: 10.1016/j.smallrumres.2018.10.001
Neves, J. H. D., Carvalho, N., Rinaldi, L., Gringoli, G., & Amarante, A. F. T. (2014). Diagnosis of anthelmintic resistance in cattle in Brazil: a comparison of different methodologies. Veterinary Parasitology, 206, 216-226. doi: 10.1016/j.vetpar.2014.10.015
Onyiah, L. C., & Arslan, O. (2005). Simulating the development period of a parasite of sheep on pasture under varying temperature conditions. Journal of Thermal Biology, 30, 203-211. doi: 10.1016/j. jtherbio .2004.10.003
Pappaterra Mendoza, G. J., Mateu de Antonio, E., Novel Badal, M. E., Castillo, M. M., Fábrega, J. C., & Puig, J. M. (2000). In vitro and in vivo effects of an immunomodulator composed of Escherichia coli lipo-polysaccharide and Propionibacterium granulosum -inactivated cells in pigs. Journal of Veterinary and Medicine B, Infectious Diseases and Veterinary Public Health, 47, 619-627. doi: 10.1046/j.1439-04 50.2000.00395.x
Pivoto, F. L., Machado, F. A., Nezi, P. A., Jr., Weber, A., Cezar, A. S., Sangioni, L. A., & Vogel, F. S. F. (2014). Improving liveweight gain of lambs infected by multidrug-resistant nematodes using a FECRT-based schedule of treatments. Parasitology Research, 113, 2303-2310. doi: 10.1007/s00436-014-3885-x
Pugh, D. G., & Baird, A. N. (2012). Sheep and goat medicine (2nd ed.). Saunders: Maryland Heights.
Quinn, P. J. (1990). Mechanisms of action of some immunomodulators used in veterinary medicine. Advances in Veterinary Science and Comparative Medicine, 35, 43-99. doi: 10.1016/B978-0-12-0392 35-3.50009-5
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Albers, G. A. A., Gray, G. D., Piper, L. R., Barker, J. S. F., Jambre, L. F., & Barger, I. A. (1987). The genetics of resistance and resilience to Haemonchus contortus infection in young Merino sheep. International Journal of Parasitology, 17(7), 1355-1363. doi: 10.1016/0020-7519(87)90103-2
Almeida, F. A., Garcia, K. C., Torgerson, P. R., & Amarante, A. F. T. (2010). Multiple resistance to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International, 59, 622-625. doi: 10.1016/j.parint.2010.09.006
Amarante, A. F. T. (2001). Controle de endoparasitoses dos ovinos. In W. R. S. Mattos (Ed.), A produção animal na visão dos brasileiros (pp. 461-473). Piracicaba: Fealq/SBZ.
Amarante, A. F. T. (2014). Os parasitas de ovinos. São Paulo: Editora UNESP.
Amarante, A. F. T., & Amarante, M. R. V. (2003). Breeding sheep for resistance to nematode infections. Journal of Animal and Veterinary Advances, 2(3), 147-161. doi: 10.1079/9781845935559.0279
Amarante, A. F. T., Bricarello, P. A., Rocha, R. A., & Gennari, S. M. (2004). Resistance of Santa Ines, Suffolk and Ile de France sheep to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 120(1), 91-106. doi: 10.1016/j.vetpar.2003.12.004
Amarante, F. A., Garcia, K. C., Togerson, P. R., & Amarante, A. F. T. (2010). Multiple resitence to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International, 59, 622-625. doi: 10.1016/j.parint.2010.09.006.
ArunKumar, S., Abdul Basith, S., & Gomathinayagam, S. (2012). A comparative analysis on serum antibody levels of sheep immunized with crude and thiol-purified excretory secretory antigen of Haemonchus contortus. Veterinary World, 5(5), 279-284. doi: 10.5455/vetworld.2012.279-284
Audibert, F. (2003). Adjuvants for vaccines, a quest. International Immunopharmacology, 3, 1187-1193. doi: 10.1016/S1567-5769(03)00011-0
Bartley, D. J., Mcarthur, C. L., Devin, L. M., Sutra, J. F., Morrison, A. A., Lespine, A., & Matthews, J. B. (2012). Characterization of macrocyclic lactone resistance in two field-derived isolates of Cooperia oncophora. Veterinary Parasitology, 190, 454-460. doi: 10.1016/j.vetpar.2012.07.022
Bowman, D. D. (2006). Parasitologia veterinária de Georgis (8a ed.). Barueri: Manole.
Braga, E. G., Ananias, R. Z., Mussalem, J. S., Squaiella, C. C., Longhini, A. L. F., Mariano, M.,... Longo-Maugéri, I. M. (2003). Treatment with Propionibacterium acnes modulates the late phase reaction of immediate hypersensitivity in mice. Immunology Letters, 88(2), 163-169. doi: 10.1016/S0165-2478(03) 00079-8
Buzzulin, C., Costa, A. J., Santos, T. R., Borges, F. A., & Soares, V. E. (2007). Eficácia anti-helmíntica comparativa da associação albendazole, levamisole e ivermectina à moxidectina em ovinos. Pesquisa Agropecuária Brasileira, 42(6), 891-895. doi: 10.1590/S0100-204X2007000600017
Cezar, A. S., Toscan, G., Camillo, G., Sangioni, L. A., Ribas, H. O., & Vogel, F. S. F. (2010). Multiple resistance of gastrointestinal nematodes to nine different drugs in a sheep flock in southern Brazil. Veterinary Parasitology, 173, 157-160. doi: 10.1016/j.vetpar.2010.06.013
Climeni, B. S. O., Monteiro, M. V., Cicoti, C. A., & Neves, M. F. (2008). Hemoncose ovina. São Paulo: Editora FAEF.
Coles, G. C., Coles, G. C., Bauer, C., Borgsteede, F. H. M., Geerts, S., Klei, T. R.,... Waller, P. J. World Association for the Advancement of Veterinary Parasitology (WAAVP) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology, 44, 35-44. doi: 10.1016/0304-4017(92)90141-U
Cunha, L. F. C. D., Fº., Pereira, A. B. D. L., & Yamamura, M. H. (1998). Resistência a anti-helmínticos em ovinos da região de Londrina - Paraná - Brasil. Semina: Ciências Agrárias, 19(1), 31-37.
Domke, A. V., Chartier, C., Gjerde, B., Höglund, J., Leine, N., Vatn, S., & Stuen, S. (2012) Prevalence of anthelmintic resistance in gastrointestinal nematodes of sheep and goats in Norway. Parasitology Research, 111, 185-193. doi: 10.1007/s00436-012-2817-x
Fausto, G. C., Pivoto, F. L., Costa, M. M., Lopes, S. T. A., França, R. T., Molento, M. B.,... Leal, M. L. R. (2014). Protein profile of lambs experimentally infected with Haemonchus contortus and supplemented with selenium and copper. Parasites & Vectors, 7355. doi: 10.1186/1756-3305-7-355
Hohenhaus, M. A., & Outteridge, P. M. (1995). The immunogenetics of resistance to Trichostrongylus colubriformis and Haemonchus contortus parasites in sheep. British Veterinary Journal, 151, 119-141. doi: 10.1016/S0007-1935(95)80004-2
Howell, S. B., Burke, J. M., Miller, J. E., Terrill, T. H., Valencia, E., Williams, M. J.,… Kaplan, R. M. (2008). Prevalence of anthelmintic resistance on sheep and goat farms in the southeastern United States. Journal of the American Veterinary Medical Association, 233(12), 1913-1919. doi: 10.2460/javma.233. 12.1913
Keane, O. M., Keegan, J. D., Good, B., Waal, T., Fanning, J., Gottstein, M.,… Sheehan, M. (2014). High level of treatment failure with commonly used anthelmintics on Irish sheep farms. Irish Veterinary Journal, 67, 16. doi: 10.1186/2046-0481-67-16
Kooyman, F. N., Van Kooten, P. J., Huntley, J. F., Mackellar, A., Cornelissen, A. W., & Schallig, H. D. (1997). Production of a monoclonal antibody specific for ovine immunoglobulin E and its application to monitor serum IgE responses to Haemonchus contortus infection. Parasitolology, 114, 395-406. doi: 10. 1017/S0031182096008633
Kotze, A. C., & Prichard, R. K. (2016). Chapter nine - anthelmintic resistance in Haemonchus contortus: history, mechanisms and diagnosis. Advances in Parasitology, 93, 397-428. doi: 10.1016/bs.apar.2016. 02.012
Lawrence, C. E. (2003). Is there a common mechanism of gastrointestinal nematode expulsion? Parasite Immunology, 25, 271-281. doi: 10.1046/j.1365-3024.2003.00630.x
Le Jambre, L. F. (1995). Relationship of blood loss to worm numbers, biomass and egg production in Haemonchus infected sheep. International Journal of Parasitology, 25(3), 269-273. doi: 10.1016/0020-7519(94)00118-8
Love, S., Neilson, F., Biddle, A. J., & Mckinnon, R. (2003). Moxidectin-resistant Haemonchus contortus in sheep in northern New South Wales. Australian Veterinary Journal, 81(6), 359-360. doi: 10.1111/j. 1751-0813.2003.tb11514.x
Martins, S. M. F. M., Garcia, M., Chate, S. C., Tavolari, F. A., Teixeira, R. B. C., Matins, L. R., Jr.,… Abel, L. J. (2012). (2012). Association of immunostimulant with anthelmintic on the treatment of sheep verminosis. Ciência Rural, 4(12), 2229-2234. doi: 10.1590/S0103-84782012005000142
Martínez-Valladares, M., Geurden, T., Bartram, D. J., Martínez-Pérez, J. M., Robles-Pérez, D., Bohórquez, A.,… Rojo-Vázquez, F. A. (2015). Resistance of gastrointestinal nematodes to the most commonly used anthelmintics in sheep, cattle and horses in Spain. Veterinary Parasitology, 211, 228-233. doi: 10.1016/ j.vetpar.2015.05.024
Mitchell, E. S. E., Hunt, K. R., Wood, R., & McLean, B. (2010). Anthelmintic resistance on sheep farms in wales. Veterinary Record, 166, 651-652. doi: 10.1136/vr.b4840
Molento, M. B., Tasca, C., Gallo, A., Ferreira, M., Bononi, R., & Stecca, E. (2004). Método Famacha como parâmetro clínico individual de infecção por Haemonchus contortus em pequenos ruminantes. Ciência Rural, 34(4), 1139-1145.
Nagata, W. B., Panegossi, M. F. C., Bresciani, K. D. S., Gomes, J. F., Kaneto, C. N., & Perri, S. H. (2019). Resistance of gastrointestinal nematodes to five different active principles ins sheep infected naturally in São Paulo State, Brazil. Small Ruminant Research, 172, 48-50. doi: 10.1016/j.smallrumres.2018.10.001
Neves, J. H. D., Carvalho, N., Rinaldi, L., Gringoli, G., & Amarante, A. F. T. (2014). Diagnosis of anthelmintic resistance in cattle in Brazil: a comparison of different methodologies. Veterinary Parasitology, 206, 216-226. doi: 10.1016/j.vetpar.2014.10.015
Onyiah, L. C., & Arslan, O. (2005). Simulating the development period of a parasite of sheep on pasture under varying temperature conditions. Journal of Thermal Biology, 30, 203-211. doi: 10.1016/j. jtherbio .2004.10.003
Pappaterra Mendoza, G. J., Mateu de Antonio, E., Novel Badal, M. E., Castillo, M. M., Fábrega, J. C., & Puig, J. M. (2000). In vitro and in vivo effects of an immunomodulator composed of Escherichia coli lipo-polysaccharide and Propionibacterium granulosum -inactivated cells in pigs. Journal of Veterinary and Medicine B, Infectious Diseases and Veterinary Public Health, 47, 619-627. doi: 10.1046/j.1439-04 50.2000.00395.x
Pivoto, F. L., Machado, F. A., Nezi, P. A., Jr., Weber, A., Cezar, A. S., Sangioni, L. A., & Vogel, F. S. F. (2014). Improving liveweight gain of lambs infected by multidrug-resistant nematodes using a FECRT-based schedule of treatments. Parasitology Research, 113, 2303-2310. doi: 10.1007/s00436-014-3885-x
Pugh, D. G., & Baird, A. N. (2012). Sheep and goat medicine (2nd ed.). Saunders: Maryland Heights.
Quinn, P. J. (1990). Mechanisms of action of some immunomodulators used in veterinary medicine. Advances in Veterinary Science and Comparative Medicine, 35, 43-99. doi: 10.1016/B978-0-12-0392 35-3.50009-5
Roberts, F. H. S., & O’Sullivan, P. J. (1950). Methods for eggs counts and larval cultures for strongyles infecting the gastrointestinal tract of catlle. Australian Journal Agriculture Research, 1(1), 99-102.
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2021-02-24
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Portella, L. P., Fernandes, F. D., Sangioni, L. A., Ramos, F., Rodrigues, F. de S., Menezes, F. R. de, Cezar, A. S., Faccin, T. C., Kommers, G. D., & Vogel, F. S. F. (2021). Combination of immunostimulants with moxidectin in the treatment of animals experimentally infected with Haemonchus contortus. Semina: Ciências Agrárias, 42(2), 707–720. https://doi.org/10.5433/1679-0359.2021v42n2p707
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