Effects of supplementation with vitamins C and E on the acute inflammatory response in Piaractus mesopotamicus

Fabiana  Rizzo Bozzo; Gustavo da Silva Claudiano; Jefferson Yunis-Aguinaga; Paulo Fernandes Marcusso; Jair Rodini Engrácia Filho; Julieta Rodini Engrácia de Moraes

doi:10.1590/1809-6891v24e-73661E

Authors

Fabiana Rizzo Bozzo Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Jaboticabal, São Paulo, Brazil https://orcid.org/0000-0001-6528-7549
Gustavo da Silva Claudiano Universidade federal do Oeste do Pará (UFOPA), Santarém, Pará, Brasil https://orcid.org/0000-0002-5063-9123
Jefferson Yunis-Aguinaga Universidad Científica del Sur, Lima, Peru https://orcid.org/0000-0002-1959-4350
Paulo Fernandes Marcusso Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Botucatu, São Paulo, Brasil https://orcid.org/0000-0002-2677-4915
Jair Rodini Engrácia Filho Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Jaboticabal, São Paulo, Brasil https://orcid.org/0000-0002-2043-0652
Julieta Rodini Engrácia de Moraes Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Jaboticabal, São Paulo, Brasil https://orcid.org/0000-0002-8384-8781

DOI:

https://doi.org/10.1590/1809-6891v24e-73661E

Abstract

Vitamins C and E are potent antioxidants that reduces the harmful effects of stress in several species including fish. In this study, it was evaluated the effect of vitamins C, E and their combination in the acute aerocystitis induced by inactivated Aeromonas hydrophila in pacu. 288 fish were distributed into 4 groups supplemented for 90 days: G1-control; G2-supplemented with 500 mg of Vitamin C; G3-supplemented with 500 mg of Vitamin E; G4-supplemented with 500 mg of Vitamin C + 500 mg of Vitamin E. The fish were divided in three groups, the first was not inoculated; second were inoculated in the swim bladder with 3 x 109 CFU of inactivated A. hydrophila and the last one with saline. The inflammatory exudate was collected from the swim bladder for assessment of cellular component and cytochemistry. The results showed higher accumulation of leukocytes in fish inoculated with bacteria. Cytochemistry was effective identifying thrombocytes, lymphocytes, macrophages and, granulocytes present in the exudate. It was also observed fish that received supplementation with vitamins presented higher accumulation of total cells in the exudate with a predominance of lymphocytes and thrombocytes. These results suggested that supplementation with vitamins improved the immunological responses.
Keywords: Aeromonas hydrophila; cytochemistry; pacu; swim bladder.

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References

R. E Ibrahim, S.A. Ahmed, S.A Amer, N.A Al-Gabri, A.I Ahmed, A.A. Abdel-Warith, M.I. Younis, A.E. Metwally Influence of vitamin C feed supplementation on the growth, antioxidant activity, immune status, tissue histomorphology, and disease resistance in Nile tilapia, Oreochromis niloticus. Aquaculture Reports, 18 (2020), p. 100545

Keen CL, Uriu-Adams JY, Emsimsa JL, Gershwin ME. Trace elements/minerals and immunity. In: Gershwin, M.E., Nestel, P., Keen, C.L., Totowa, N.J. (Eds.), Handbook of Nutrition and Immunity. Humana Press, 2004; 117–140.

Ekiz C, Agaoglu L, Karakas Z, Gurel N, Yalcin I. The effect of iron deficiency anemia on the function of the immune system. Hematol. J. 2005; 5, 579–583.

Koshio S, Angeles M. Beneficial roles of feed additives as immunostimulants in aquaculture: a review Rev. Aquac. 2017; 1–25. 10.1111/raq.12209

Khan, K.U., Zuberi, A., Nazir, S., Fernandes, J.B.K., Jamil, Z., Sarwar, H. Effects of dietary selenium nanoparticles on physiological and biochemical aspects of juvenile Tor putitora, Turk. J. Zool. 2016. 40, 704–712.

Liang XP, Li Y, Hou YM, Qiu H, Zhou QC. Effect of dietary vitamin C on the growth performance, antioxidant ability and innate immunity of juvenile yellow catfish (Pelteobagrus fulvidraco Richardson). Aquac. Res. 2017; (48): 149-160.

Etsuo N. Lipid oxidation that is, and is not, inhibited by vitamin E: Consideration about physiological functions of vitamin E. Free Radical Biology and Medicine. 2021; 176(20): 1-15.

Pan JH, Feng L, Jiang WD, Wu P, Kuang SY, Tang L, Zhang YA, Zhou XQ, Liu Y. Vitamin E deficiency depressed fish growth, disease resistance, and the immunity and structural integrity of immune organs in grass carp (Ctenopharyngodon idella): Referring to NF-κB, TOR and Nrf2 signaling. Fish and Shellfish Immunology. 2017; 60:219-236. Disponível em: 10.1016/j.fsi.2016.11.044

Ortuño J, Cuesta A, Esteban MA, Meseguer J. Effect of oral administration of high vitamin C and E dosages on the gilthead seabream (Spaurus aurata L.) innate immune system. Veterinary Immunology and Immunopathology. 2001. 200; 79(3-4): 167-180. Disponível em: 10.1016/s0165-2427(01)00264-1

Wahli T, Verlhac V, Gabaudan J, Schuep W, Meier W. Influence of combined vitamins C and E on non-specific immunity and disease resistance of rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases. 1998; 21(2): 127–137. Disponível em: 10.1046/j.1365-2761.1998.00088.x

Sealey WM, Gatlin DM. Dietary vitamin C and vitamin E interact to influence growth and tissue composition of juvenile hybrid striped bass (Morone chrysops (female) x M. saxatilis (male) but have limited effects on immune responses. The Journal of Nutrition 2002; 132(4): 748–755. DOI: 10.1093/jn/132.4.748

Le TS, Nguyen TH, Vo HP, Doan VC, Nguyen HL, Tran MT, Tran TT, Southgate PC, Kurtboke DI. Protective fffects of bacteriophages against Aeromonas hydrophila species Causing Motile Aeromonas Septicemia (MAS) in striped catfish. Antibiotics (Basel). 2018; 7(1). https://doi.org/10.3390/antibiotics7010016

Peterman MA, Posadas BC. Direct economic impact of fish diseases on the East Mississippi catfish industry. North American Journal of Aquaculture. 2019; 81(3): 222–229. https://doi.org/10.1002/naaq.10090

Kuebutornye FKA, Abarike ED. The contribution of medicinal plants to tilapia aquaculture: a review Aquac. Int. 2020; (28): 965-983. 10.1007/s10499-020-00506-3

Thépot V, Campbell AH, Rimmer MA, Paul NA. Meta-analysis of the use of seaweeds and their extracts as immunostimulants for fish: a systematic review Rev. Aquac. 2021; (13): 907-933,

Claudiano GS, Yunis-aguinaga J, Marinho-neto, FA, Miranda, R, Martins, IM, Otani FS, Mundim AV, Marzocchi-machado CM, Moraes JRE, de Moraes, FR. Hematological and immune changes in Piaractus mesopotamicus in the sepsis induced by Aeromonas hydrophila. Fish & Shellfish Immunology. 2019; 88: 259-265.

Yunis-Aguinaga J, Claudiano GS, Marcusso PF, Manrique WG, De Moraes JRE, De Moraes FR, Fernandes JB. Uncaria tomentosa increases growth and immune activity in Oreochromis niloticus challenged with Streptococcus agalactiae. Fish and Shellfish Immunology. 2015; 47(1), 630-638. Disponível em: 10.1016/j.fsi.2015.09.051

Moraes JR, Freitas JB, Bozzo FR, Moraes FR, Martins ML. A suplementação alimentar com vitamina c acelera a evolução do processo cicatricial em Piaractus mesopotamicus (Holmberg, 1887). Boletim do Instituto de Pesc. 2003;29:57 – 67.

Belo MAA, Moraes FR, Yoshida L, Prado EJR, Moraes JRE, Soares VE, Silva MG. Deleterious effects of low level of vitamin E and high stocking density on the hematology response of pacus, during chronic inflammatory reaction. Aquaculture. 2014; 423:124–128. Disponível em: 10.1016/j.aquaculture.2013.12.013

Belo MAA, Moraes JRE, Soares VE, Martins ML, Brum CD, Moraes FR. Vitamin C and endogenous cortisol in foreign-body inflammatory response in pacus. Pesquisa Agropecuária Brasileira. 2012; 47(7): 1015-1021. Disponível em: 10.1590/S0100-204X2012000700019

Castro MP, Claudiano GS, Bortoluzzi NL, Garrido E, Fujimoto RY, Belo MAA, Shimada MT, Moraes JRE, Moraes FR. Chromium carbochelate dietary supplementation favored the glucocorticoid response during acute inflammation of Piaractus mesopotamicus. Aquaculture. 2014a; 432:114–118a. Disponível em: 10.1016/j.aquaculture.2014.04.036

Tavares-Dias M. Cytochemical method for staining fish basophils. Journal of Fish Biology. 2006b; 69(1): 312-317b. Disponível em: 10.1111/j.1095-8649.2006.01106.x

Pregnolatto W, Pregnolatto NP. Normas analíticas do Instituto Adolfo Lutz: métodos químicos e físicos para análise de alimentos. 3.ed. São Paulo: Instituto Adolfo Lutz; 1985. 533p.

Mcmanus JFA. Histological demonstration of mucin after periodic acid. Nature, 1946; 158 (4006):202.

Tavares-Dias MA. Morphological and cytochemical study of erythrocytes, thrombocytes and leukocytes in four freshwater teleosts. Journal of Fish Biology. 2006a; 68(6):1822–1833a. Disponível em: 10.1111/j.1095-8649.2006.01089.x

Tavares-Dias M, Ono EA, Pilarski F, Moraes FR. Can thrombocytes participate in the removal of cellular debris in the blood circulation of teleost fish? A cytochemical study and ultrastructural analysis. Journal of Applied Ichthyology. 2007; 23(6): 709-712. Disponível em: 10.1111/j.1439-0426.2007.00850.x

Castro MP, Claudiano GS, Petrillo TR, Shimada MT, Belo MAA, Marzocchi-Machado CM, Moraes JRE, Manrique WG, Moraes FR. Acute aerocystitis in Nile tilapia bred in net cages and supplemented with chromium carbochelate and Saccharomyces cerevisiae. Fish Shellfish Immunol. 2014b; 36(1): 284 – 290b.

Bozzo FR, Moraes JRE, Moraes FR, Pereira GT, Tavares-Dias M, Onaka EM. Kinetics of cellular component in inflammatory response induced by different stimuli in the swim bladder of Piaractus mesopotamicus, Holmberg, 1887 (Characidae). Journal of the World Aquaculture Society. 2007; 38(2): 302-308. Disponível em: 10.1111/j.1749-7345.2007.00100.x

Li J., Barreda DR, Zhang YA, Boshra H, Gelman AE, Patra S, Tort L, Sunyer JO. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nature Immunology. 2006; 7(10): 1116-1124. Disponível em: 10.1038/ni1389

Randelli E, Buonocore F, Scapigliati G. Cell markers and determinants in fish immunology. Fish and Shellfish Immunology. 2008; 25(4): 326–340. Disponível em: 10.1016/j.fsi.2008.03.019

Shigdar S, Harford A, Ward AC. Cytochemical characterization of the leucocytes and thrombocytes from Murray cod (Maccullochella peelii peelii, Mitchell). Fish and Shellfish Immunology. 2006; 26(5): 731-736. Disponível em: 10.1016/j.fsi.2009.03.010

Belo MAA, Schalch SHC, Moraes FR, Soares VE, Otoboni AMMB, Moraes JER. Effect of dietary supplementation with vitamin E and stocking density on macrophage recruitment and giant cell formation in the Teleost Fish, Piaractus mesopotamicus. J Journal of Comparative Pathology. 2005; 54(2-3):133-146. Disponível em: 10.1016/j.jcpa.2005.04.004

Martins ML, Moraes FR, Fujimoto RY, Onaka EM, Bozzo FR, Moraes JRE. Carragenin induced inflammation in Piaractus mesopotamicus (Osteichthyes: Characidae) cultured in Brazil. Boletim do Instituto de Pesca. 2006; 32(1): 31-39.