LEVAMISOLE MODULATES THE CELL-MEDIATED IMMUNITY OF MATRINXí, Brycon amazonicus
DOI:
https://doi.org/10.20950/1678-2305.2019.45.2.445Keywords:
immunostimulant, cellular immunity, innate immunity, white blood cellAbstract
The use of immunomodulators is an alternative to improve the immune system of fish and avoid the excessive use of antibiotics. Levamisole is a synthetic anthelmintic which promotes a potent immunostimulation on innate and acquired variables of fish. In order to access the levamisole effects on matrinxã, Brycon amazonicus, fish were fed levamisole at 500 mg kg-1 of diet for seven days. After this period fish were submitted to blood collection. Immunological variables, such as leukocytes respiratory burst, total serum protein, albumin, globulin, albumin:globulin index and hematological variables, such as hematocrit, hemoglobin, red and white blood cell (WBC) and Wintrobe indexes were evaluated. The levamisole administration increased the WBC counts indicating that the immunostimulant modulates the cell-mediated immunity. The increased WBC indicate that the fish fed levamisole were in a better body condition, and probable more resistant to disease due to potential for phagocytosis activation, degranulation of neutrophilic granules, and consequently production of antibodies and immunological memory. Besides, these findings are important for news projects regarding the production of vaccines and deeper understanding of fish cell-mediated immunity.
References
Biller-Takahashi, J.D.; Montassier, H.J.; Takahashi, L.S.; Urbinati, E.C. 2016. Levamisole promotes an adjuvant effect on the immunityof pacu (Piaractus mesopotamicus) when immunized with Aeromonas hydrophila, even when provided in the diet. Animal Feed Science and Technology, 211(1): 164í 173. https://doi.org/10.1016/j.anifeedsci.2015.11.008
Biller-Takahashi, J.D.; Takahashi, L.S.; Mingatto, F.E., Urbinati, E.C. The immune system is limited by oxidative stress: Dietary selenium promotes optimal antioxidative status and greatest immune defense in pacu Piaractus mesopotamicus. Fish and Shellfish Immunology, 47(1): 360-367, 2015. http://dx.doi.org/10.1016/j.fsi.2015.09.022
Biller-Takahashi, J.D.; Takahashi, L.S.; Saita, M.V.; Gimbo, R.Y.; Urbinati, E.C. 2013. Leukocytes respiratory burst activity as indicator of innate immunity of pacu Piaractus mesopotamicus. Brazilian Journal of Biology, 73(2): 425-429. http://dx.doi.org/10.1590/S1519-69842013000200026
Biller-Takahashi, J.D.; Urbinati, E.C. 2014. Fish Immunology. The modification and manipulation of the innate immune system: Brazilian studies. Academia Brasileira de Ciências, 86(3): 75-87. http://dx.doi.org/10.1590/0001-3765201420130159
Costa, D.V.; Ferreira, M.W.; Navarro, R.D.; Rosa, P.V.; Murgas, L.D.S. 2014. Parí¢metros hematológicos de tilápias-do-Nilo (Oreochromis niloticus) alimentadas com diferentes fontes de óleo. Revista Brasileira de Saúde e Produção Animal, 15(3): 754-764.
Cuesta, A.; Esteban, M.A.; Meseguer, J. 2002. Levamisole is a potent enhancer of gilthead sea bream natural cytotoxic activity. Veterinary Immunology and Immunopathology 89(2): 169-174. https://doi.org/10.1016/S0165-2427(02)00220-9
Doumas, B.T.; Watson, W.A.; Biggs, H.G. 1971. Albumin standards and the measurement of serum albumin with bromocresol green. Clinical Chimica Acta, 31(1): 87-96.
Fazio, F. 2019. Fish hematology analysis as an important tool of aquaculture: A review. Aquaculture, 500(1): 237í 242. https://doi.org/10.1016/j.aquaculture.2018.10.030
Faurschou, M.; Borregaard, N. 2003. Neutrophils granules and secretory vesicles in inflamation. Microbes Infection, 5(14): 1317-1327.
Ferraz, F.B.; Gomes, L.C. 2009. Social relationship as inducer of immunological and stress responses in matrinxã (Brycon amazonicus). Comparative Biochemistry and Physiology Part A, 153(3): 293-296. https://doi.org/10.1016/j.cbpa.2009.03.002
Ishikawa, N.M.; Ranzani-Paiva, M.J.T.; Lombardi, J.V. 2008. Metodologia para quantificação de leucócitos totais em peixes, Oreochromis niloticus. Archives of Veterinary Science, 13(1): 54-63. http://dx.doi.org/10.5380/avs.v13i1.11560
Ispir, U.; Yonar, M.E. 2007. The effects of levamisole on phagocytic activity of rainbow trout (Oncorhynchus mykiss W.). Acta Veterinária BRNO, 76(3): 493-497. https://doi.org/10.2754/avb200776030493
Ispir, U.; Dorucu, M. 2005. A study on the effects of levamisole on the immune system of rainbow trout (Oncorhynchus mykiss, Walbaum). Turkish Journal of Veterinary and Animal Science, 29(1): 1169-1176.
Jeney, G.; Anderson, D.P. 1993. Enhanced immune response and protection in rainbow trout to Aeromonas salmonicida bacterin following prior immersion in immunostimulants. Fish and Shellfish Immunology, 3(1): 51-58. https://doi.org/10.1006/fsim.1993.1005
Kajita, Y.; Sakai, M.; Atsuta, S.; Kobayashi, M. 1990. The immunomodulatory effects of levamisole on rainbow trout, Oncorhynchus mykiss. Fish Pathology, 25(1): 93-98. https://doi.org/10.3147/jsfp.25.93
Korytá, T.; Thi, D.; Takizawa, H.; Kí¶llner, F. .2013. Multicolour flow cytometry identifying defined leukocyte subsets of rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology, 35(6): 2017-2019. https://doi.org/10.1016/j.fsi.2013.09.025.
Li, P.; Li, P.; Wang, X.; Gatliniii, D.M. 2006. Evaluation of levamisole as a feed additive for growth and health management of hybrid striped bass (Morone chrysopsí"”Morone saxatilis). Aquaculture, 251(2-4): 201-209. https://doi.org/10.1016/j.aquaculture.2005.11.015
Maqsood, S.; Samoon, M.H.; Singh, P. 2009. Immunomodulatory and growth promoting effect of dietary levamisole in Cyprinus carpio fingerlings against the challenge of Aeromonas hydrophila. Turkish Journal of Fisheries and Aquatic Sciences, 9(1): 111-120.
Misra, C.K.; Das, B.K.; Mukherjee, S.C. 2009. Immune response, growth and survival of Labeo rohita fingerlings fed with levamisole supplemented diets for longer duration. Aquaculture Nutrition, 15(4): 356-365. https://doi.org/10.1111/j.1365-2095.2008.00600.x
Morrison, R.N; Nowak, B.F.; Carson, J. 2001. The histopathological effects of a levamisole-adjuvanted Vibrio anguillarum vaccine on Atlantic salmon (Salmo salar L.). Aquaculture, 195(1-2): 23-33. https://doi.org/10.1016/S0044-8486(00)00546-9
Morrison, R.N; Fast, M.D.; Muise, D.M.; Easy, R.E.; Ross, N.W.; Johnson, S.C. 2000. The Effect of Levamisole as an Adjuvant on the Humoral Immune Response of Atlantic Salmon (Salmo solar L.). Bulletin of the European Association of Fish Pathologists, 20(3): 101-105. https://doi.org/10.1016/j.fsi.2005.11.010
Mulero, M.; Esteban, A.; Meseguer, J. 1998. In vitro levamisole fails to increase sea bream (Sparus aurata L.) phagocyte functions. Fish and Shellfish Immunology, 8(4): 315-318.
Ranzani-Paiva, M.J.T.; Silva-Souza, E.A.T. 2004. Hematologia de peixes brasileiros. In: Ranzani-Paiva M.J.T. et al. (Ed.). Sanidade de organismos aquáticos. São Paulo: Editora Varela, cap.4, 89-120.
Reich, R.; Mulvaney, P.; Robinson-Bostom, L. 2014. Antihelminthic Drugs. Side Effects of Drugs Annual, 36(1): 457-464.
Reinhold, J.G. 1953. Manual determination of serum total protein, albumin and globulin fractions by Biuret method. In: Standard methods in clinical chemistry (Reiner, M. ed), pp.88-90. New York: Academic Press.
Renoux, G. 1980. The general immunopharmacology of levamisole. Drugs, 20(2): 89-99.
Rieger, A.M.; Barreda, D.R. 2011. Antimicrobial mechanism of fish leukocytes. Developmental and Comparative Immunology, 35(12): 1238-1245. https://doi.org/10.1016/j.dci.2011.03.009
Rocha, R.L.; Ferreira, J.M.; Miranda Lopes, T.O.; Gomes, L.C. 2018. Morphometric, bromatological, and sensory analysis of nile tilapia vaccinated against Streptococcus agalactiae. Boletim do Instituto de Pesca, 44(1): 100-104. 0. http://dx.doi.org/10.20950/1678-2305.2018.281
Rosenfeld, G. 1947. Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do May-Grünwald e do Giemsa num só corante de emprego rápido. Memórias do Instituto Butantan, 20(1): 329-334.
Sado, R.Y.; Bicudo, A.J.A.; Cyrino, J.E.P. 2010. Dietary levamisole influenced hematological variables of juvenile pacu, Piaractus mesopotamicus (Holmberg 1887). Journal of the World Aquaculture Society, 41(1): 66-75. https://doi.org/10.1111/j.1749-7345.2009.00334.x
Sahoo, P.K.; Mukherjee, S.C. 2002. The effect of dietary immunomodulation upon Edwardsiella tarda vaccination in healthy and immunocompromised Indian major carp (Labeo rohita). Fish and Shellfish Immunology, 12(1): 1-16. https://doi.org/10.1111/j.1749-7345.2009.00334.x
Sakai, M. 1999. Current research status of fish immunostimulants. Aquaculture, 72(1-2): 63- 92. https://doi.org/10.1016/S0044-8486(98)00436-0
Schell, L.M.; Blumberg, B.S. 1977. The genetics of human serum albumin, function an uses. Pergamon Press. Oxford and New York, pp. 113-141.
Siwicki, A.K. 1989. Immunostimulating influence of levamisole on nonspecific immunity in carp (Cyprinus carpio). Developmental and Comparative Immunology, 13(1): 87-91. https://doi.org/10.1016/0145-305X(89)90021-9
Stuart, L.M.; Ezekowitz, R.A. 2005. Phagocytosis: elegant complexity. Immunity, 22(5): 539-550. https://doi.org/10.1016/j.immuni.2005.05.002
Tavares-Dias, M.; Affonso, E.G.; Oliveira, S.R.; Marcon, J.L.; Egami, M.I. 2008. Comparative study on hematological variables of farmed matrinxã, Brycon amazonicus Spix and Agassiz, 1829 (Characidae: Bryconinae) with others Bryconinae species. Acta Amazonica, 38(4): 799-806. http://dx.doi.org/10.1590/S0044-59672008000400026
Tavares-Dias, M., Moraes, F.R., Imoto, M.E. 2008. Haematological parameters in two neotropical freshwater teleost, Leporinus macrocephalus (Anostomidae) and Prochilodus lineatus (Prochilodontidae). Bioscience Journal, 24(3), 96í 101.
Urbinati, E.C.; Gonçalves, F.D.; Takahashi, L.S. 2010. Pacu (Piaractus mesopotamicus). In Espécies nativas para piscicultura no Brasil (Baldisseroto, B. and Gomes, L. C. Eds), Santa Maria, Santa Catarina: Editora UFSM, 2nd ed. pp. 225-246.
Utke, K.; Kock, H.; Schuetze, H.; Bergmann, S.M.; Lorenzen, N.; Einer-Jensen, K.; Koller, B.; Dalmo, R.A.; Velsely, T.; Ototake, M.; Fischer, U. 2008. Cell-mediated immune response in rainbow trout after DNA immunization against the viral hemorrhagic septicemia virus. Developmental and Comparative Immunology, 32(3): 239-252. https://doi.org/10.1016/j.dci.2007.05.010
Wintrobe, M.M. 1934. Variations on the size and haemoglobin content of erythrocytes in the blood various vertebrates. Folia Haematologica, 51(1): 32-49.
Zanuzzo, F.S.; Zaiden, S.F.; Senhorini, J.A.; Marzocchi-Machado, C.M.; Urbinati, E.C. 2015. Aloe vera bathing improved physical and humoral protection in breeding stock after induced spawning in matrinxã (Brycon amazonicus). Fish and Shellfish Immunology, 45(1): 132-140. https://doi.org/10.1016/j.fsi.2015.02.017
Zanuzzo, F.S.; Biller-Takahashi, J.D.; Urbinati, E.C. 2012. Effect of Aloe vera extract on the improvement of the respiratory activity of leukocytes of matrinxã during the transport stress. Revista Brasileira de Zootecnia, 41(10): 2299-2302. http://dx.doi.org/10.1590/S1516-35982012001000023
Biller-Takahashi, J.D.; Takahashi, L.S.; Mingatto, F.E., Urbinati, E.C. The immune system is limited by oxidative stress: Dietary selenium promotes optimal antioxidative status and greatest immune defense in pacu Piaractus mesopotamicus. Fish and Shellfish Immunology, 47(1): 360-367, 2015. http://dx.doi.org/10.1016/j.fsi.2015.09.022
Biller-Takahashi, J.D.; Takahashi, L.S.; Saita, M.V.; Gimbo, R.Y.; Urbinati, E.C. 2013. Leukocytes respiratory burst activity as indicator of innate immunity of pacu Piaractus mesopotamicus. Brazilian Journal of Biology, 73(2): 425-429. http://dx.doi.org/10.1590/S1519-69842013000200026
Biller-Takahashi, J.D.; Urbinati, E.C. 2014. Fish Immunology. The modification and manipulation of the innate immune system: Brazilian studies. Academia Brasileira de Ciências, 86(3): 75-87. http://dx.doi.org/10.1590/0001-3765201420130159
Costa, D.V.; Ferreira, M.W.; Navarro, R.D.; Rosa, P.V.; Murgas, L.D.S. 2014. Parí¢metros hematológicos de tilápias-do-Nilo (Oreochromis niloticus) alimentadas com diferentes fontes de óleo. Revista Brasileira de Saúde e Produção Animal, 15(3): 754-764.
Cuesta, A.; Esteban, M.A.; Meseguer, J. 2002. Levamisole is a potent enhancer of gilthead sea bream natural cytotoxic activity. Veterinary Immunology and Immunopathology 89(2): 169-174. https://doi.org/10.1016/S0165-2427(02)00220-9
Doumas, B.T.; Watson, W.A.; Biggs, H.G. 1971. Albumin standards and the measurement of serum albumin with bromocresol green. Clinical Chimica Acta, 31(1): 87-96.
Fazio, F. 2019. Fish hematology analysis as an important tool of aquaculture: A review. Aquaculture, 500(1): 237í 242. https://doi.org/10.1016/j.aquaculture.2018.10.030
Faurschou, M.; Borregaard, N. 2003. Neutrophils granules and secretory vesicles in inflamation. Microbes Infection, 5(14): 1317-1327.
Ferraz, F.B.; Gomes, L.C. 2009. Social relationship as inducer of immunological and stress responses in matrinxã (Brycon amazonicus). Comparative Biochemistry and Physiology Part A, 153(3): 293-296. https://doi.org/10.1016/j.cbpa.2009.03.002
Ishikawa, N.M.; Ranzani-Paiva, M.J.T.; Lombardi, J.V. 2008. Metodologia para quantificação de leucócitos totais em peixes, Oreochromis niloticus. Archives of Veterinary Science, 13(1): 54-63. http://dx.doi.org/10.5380/avs.v13i1.11560
Ispir, U.; Yonar, M.E. 2007. The effects of levamisole on phagocytic activity of rainbow trout (Oncorhynchus mykiss W.). Acta Veterinária BRNO, 76(3): 493-497. https://doi.org/10.2754/avb200776030493
Ispir, U.; Dorucu, M. 2005. A study on the effects of levamisole on the immune system of rainbow trout (Oncorhynchus mykiss, Walbaum). Turkish Journal of Veterinary and Animal Science, 29(1): 1169-1176.
Jeney, G.; Anderson, D.P. 1993. Enhanced immune response and protection in rainbow trout to Aeromonas salmonicida bacterin following prior immersion in immunostimulants. Fish and Shellfish Immunology, 3(1): 51-58. https://doi.org/10.1006/fsim.1993.1005
Kajita, Y.; Sakai, M.; Atsuta, S.; Kobayashi, M. 1990. The immunomodulatory effects of levamisole on rainbow trout, Oncorhynchus mykiss. Fish Pathology, 25(1): 93-98. https://doi.org/10.3147/jsfp.25.93
Korytá, T.; Thi, D.; Takizawa, H.; Kí¶llner, F. .2013. Multicolour flow cytometry identifying defined leukocyte subsets of rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology, 35(6): 2017-2019. https://doi.org/10.1016/j.fsi.2013.09.025.
Li, P.; Li, P.; Wang, X.; Gatliniii, D.M. 2006. Evaluation of levamisole as a feed additive for growth and health management of hybrid striped bass (Morone chrysopsí"”Morone saxatilis). Aquaculture, 251(2-4): 201-209. https://doi.org/10.1016/j.aquaculture.2005.11.015
Maqsood, S.; Samoon, M.H.; Singh, P. 2009. Immunomodulatory and growth promoting effect of dietary levamisole in Cyprinus carpio fingerlings against the challenge of Aeromonas hydrophila. Turkish Journal of Fisheries and Aquatic Sciences, 9(1): 111-120.
Misra, C.K.; Das, B.K.; Mukherjee, S.C. 2009. Immune response, growth and survival of Labeo rohita fingerlings fed with levamisole supplemented diets for longer duration. Aquaculture Nutrition, 15(4): 356-365. https://doi.org/10.1111/j.1365-2095.2008.00600.x
Morrison, R.N; Nowak, B.F.; Carson, J. 2001. The histopathological effects of a levamisole-adjuvanted Vibrio anguillarum vaccine on Atlantic salmon (Salmo salar L.). Aquaculture, 195(1-2): 23-33. https://doi.org/10.1016/S0044-8486(00)00546-9
Morrison, R.N; Fast, M.D.; Muise, D.M.; Easy, R.E.; Ross, N.W.; Johnson, S.C. 2000. The Effect of Levamisole as an Adjuvant on the Humoral Immune Response of Atlantic Salmon (Salmo solar L.). Bulletin of the European Association of Fish Pathologists, 20(3): 101-105. https://doi.org/10.1016/j.fsi.2005.11.010
Mulero, M.; Esteban, A.; Meseguer, J. 1998. In vitro levamisole fails to increase sea bream (Sparus aurata L.) phagocyte functions. Fish and Shellfish Immunology, 8(4): 315-318.
Ranzani-Paiva, M.J.T.; Silva-Souza, E.A.T. 2004. Hematologia de peixes brasileiros. In: Ranzani-Paiva M.J.T. et al. (Ed.). Sanidade de organismos aquáticos. São Paulo: Editora Varela, cap.4, 89-120.
Reich, R.; Mulvaney, P.; Robinson-Bostom, L. 2014. Antihelminthic Drugs. Side Effects of Drugs Annual, 36(1): 457-464.
Reinhold, J.G. 1953. Manual determination of serum total protein, albumin and globulin fractions by Biuret method. In: Standard methods in clinical chemistry (Reiner, M. ed), pp.88-90. New York: Academic Press.
Renoux, G. 1980. The general immunopharmacology of levamisole. Drugs, 20(2): 89-99.
Rieger, A.M.; Barreda, D.R. 2011. Antimicrobial mechanism of fish leukocytes. Developmental and Comparative Immunology, 35(12): 1238-1245. https://doi.org/10.1016/j.dci.2011.03.009
Rocha, R.L.; Ferreira, J.M.; Miranda Lopes, T.O.; Gomes, L.C. 2018. Morphometric, bromatological, and sensory analysis of nile tilapia vaccinated against Streptococcus agalactiae. Boletim do Instituto de Pesca, 44(1): 100-104. 0. http://dx.doi.org/10.20950/1678-2305.2018.281
Rosenfeld, G. 1947. Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do May-Grünwald e do Giemsa num só corante de emprego rápido. Memórias do Instituto Butantan, 20(1): 329-334.
Sado, R.Y.; Bicudo, A.J.A.; Cyrino, J.E.P. 2010. Dietary levamisole influenced hematological variables of juvenile pacu, Piaractus mesopotamicus (Holmberg 1887). Journal of the World Aquaculture Society, 41(1): 66-75. https://doi.org/10.1111/j.1749-7345.2009.00334.x
Sahoo, P.K.; Mukherjee, S.C. 2002. The effect of dietary immunomodulation upon Edwardsiella tarda vaccination in healthy and immunocompromised Indian major carp (Labeo rohita). Fish and Shellfish Immunology, 12(1): 1-16. https://doi.org/10.1111/j.1749-7345.2009.00334.x
Sakai, M. 1999. Current research status of fish immunostimulants. Aquaculture, 72(1-2): 63- 92. https://doi.org/10.1016/S0044-8486(98)00436-0
Schell, L.M.; Blumberg, B.S. 1977. The genetics of human serum albumin, function an uses. Pergamon Press. Oxford and New York, pp. 113-141.
Siwicki, A.K. 1989. Immunostimulating influence of levamisole on nonspecific immunity in carp (Cyprinus carpio). Developmental and Comparative Immunology, 13(1): 87-91. https://doi.org/10.1016/0145-305X(89)90021-9
Stuart, L.M.; Ezekowitz, R.A. 2005. Phagocytosis: elegant complexity. Immunity, 22(5): 539-550. https://doi.org/10.1016/j.immuni.2005.05.002
Tavares-Dias, M.; Affonso, E.G.; Oliveira, S.R.; Marcon, J.L.; Egami, M.I. 2008. Comparative study on hematological variables of farmed matrinxã, Brycon amazonicus Spix and Agassiz, 1829 (Characidae: Bryconinae) with others Bryconinae species. Acta Amazonica, 38(4): 799-806. http://dx.doi.org/10.1590/S0044-59672008000400026
Tavares-Dias, M., Moraes, F.R., Imoto, M.E. 2008. Haematological parameters in two neotropical freshwater teleost, Leporinus macrocephalus (Anostomidae) and Prochilodus lineatus (Prochilodontidae). Bioscience Journal, 24(3), 96í 101.
Urbinati, E.C.; Gonçalves, F.D.; Takahashi, L.S. 2010. Pacu (Piaractus mesopotamicus). In Espécies nativas para piscicultura no Brasil (Baldisseroto, B. and Gomes, L. C. Eds), Santa Maria, Santa Catarina: Editora UFSM, 2nd ed. pp. 225-246.
Utke, K.; Kock, H.; Schuetze, H.; Bergmann, S.M.; Lorenzen, N.; Einer-Jensen, K.; Koller, B.; Dalmo, R.A.; Velsely, T.; Ototake, M.; Fischer, U. 2008. Cell-mediated immune response in rainbow trout after DNA immunization against the viral hemorrhagic septicemia virus. Developmental and Comparative Immunology, 32(3): 239-252. https://doi.org/10.1016/j.dci.2007.05.010
Wintrobe, M.M. 1934. Variations on the size and haemoglobin content of erythrocytes in the blood various vertebrates. Folia Haematologica, 51(1): 32-49.
Zanuzzo, F.S.; Zaiden, S.F.; Senhorini, J.A.; Marzocchi-Machado, C.M.; Urbinati, E.C. 2015. Aloe vera bathing improved physical and humoral protection in breeding stock after induced spawning in matrinxã (Brycon amazonicus). Fish and Shellfish Immunology, 45(1): 132-140. https://doi.org/10.1016/j.fsi.2015.02.017
Zanuzzo, F.S.; Biller-Takahashi, J.D.; Urbinati, E.C. 2012. Effect of Aloe vera extract on the improvement of the respiratory activity of leukocytes of matrinxã during the transport stress. Revista Brasileira de Zootecnia, 41(10): 2299-2302. http://dx.doi.org/10.1590/S1516-35982012001000023
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2019-03-26
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