Effects of Dietary Supplementation with Broccoli Sprouts (Brassica oleracea) on the Hematology and Immunological Responses of Nile Tilapia (Oreochromis niloticus)

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Duangjai Pisuttharachai
Warrapong Nalinanon
Nontawith Areechon

Abstract

We analyzed the effects of dietary administration of broccoli sprouts (Brassica oleracea) at varying concentrations (0, 10, 15, 20 and 25 g·kg-1 diet, for one and two weeks) on the hematology and select immunological parameters of Nile tilapia (Oreochromis niloticus). Subsequent results showed that the hematocrit level and red blood cell count remained unchanged following ingestion of broccoli sprouts for one and two weeks. However, the fish fed the supplemented diets of 20 and 25 g·kg-1 for two weeks displayed significant increase in white blood cell counts. Further analyses revealed that Nile tilapia fed with 10, 15, 20 and 25 g broccoli sprouts·kg-1 for two weeks displayed significant (p<0.05) improvement in phagocytic activity compared to that of the control group. In addition, serum bactericidal activity against Aeromonas hydrophila and Streptococcus agalactiae was enhanced in broccoli sprout-fed groups as early as one week after feeding. These results suggest that broccoli sprouts can enhance immune response in Nile tilapia by increasing total white blood cells and stimulating both cellular and humoral immunity.

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References

1. Adams, A. 1991. Response of penaeid shrimp to exposure to Vibrio species. Fish and Shellfish Immunology 1: 59-70.

2. Aly, S.M., Y.A.G. Ahmed, A.A.A. Ghareeb and M.F. Mohamed. 2008. Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish and Shellfish Immunology 25: 128-136.

3. Barman, D., P. Nen, S.C. Mandal and V. Kumar. 2013. Immunostimulants for aquaculture health management. Journal of Marine Science: Research and Development 3: 134. doi: 10.4172/2155-9910.1000134

4. Bessler, H. and M. Djaldetti. 2018. Broccoli and human health: Immunomodulatory effect of sulforaphane in a model of colon cancer. International Journal of Food Sciences and Nutrition 69: 946-953.

5. Cheung, K.L. and A.N. Kong. 2010. Molecular targets of dietary phenethyl isothiocyanate and sulforaphane for cancer chemoprevention. Journal of the American Association of Pharmaceutical Scientists 12: 87-97.

6. Clauss, T.M., A.D.M. Dove and J.E. Arnold. 2008. Hematologic disorders of fish. Veterinary Clinics Exotic Animal Practice 11: 445-462.

7. Danilov, C.A., K. Chandrasekaran, J. Racz, L. Soane, C. Zielke and G. Fiskum. 2009. Sulforaphane protects astrocytes against oxidative stress and delayed death caused by oxygen and glucose deprivation. Glia 57: 645-656.

8. Dugenci, S.K., N. Arda and A. Candan. 2003. Some medicinal plants as immunostimulant for fish. Journal of Ethnopharmacology 88: 99-106.

9. Esteban, M.A., A. Cuesta, E. Chaves-Pozo and J. Meseguer. 2015. Phagocytosis in teleosts. Implications of the new cells involved. Biology 4: 907-922.

10. Fahey, J.W., X. Haristoy, P.M. Dolan, T.W. Kensler, I. Scholtus, K.K. Stephenson, P. Talalay and A. Lozniewski. 2002. Sulforaphane inhibits extracellular, intracellular, and antibiotic-resistant strains of Helicobacter pylori and prevents benzo[a]pyrene- induced stomach tumors. Proceedings of the National Academy of Sciences of the United States of America 99(11): 7610-7615.

11. Food and Agriculture Organization (FAO). 2017. Global aquaculture production. http://www.fao.org/fishery/statistics/global-aquaculture-production/query/en. Cited 10 Nov 2019.

12. Fazio, F., S. Marafioti, F. Filiciotto, G. Buscaino, M. Panzera and C. Faggio. 2013. Blood hemogram profiles of farmed onshore and offshore gilthead sea bream (Sparus aurata) from Sicily, Italy. Turkish Journal of Fisheries and Aquatic Sciences 13: 415-422.

13. Harikrishnan, R., C. Balasundaram, M.C. Kim, J.S. Kim, Y.J. Han and M.S. Heo. 2009. Innate immune response and disease resistance in Carassius auratus by triherbal solvent extracts. Fish and Shellfish Immunology 27: 508-515.

14. Hirayama, D., T. Iida and H. Nakase. 2017. The phagocytic function of macrophage- enforcing innate immunity and tissue homeostasis. International Journal of Molecular Sciences 19: 92-105.

15. Itami, T., Y. Takahashi, E. Tsuchihira, H. Igusa and M. Kondo. 1994. Enhancement of disease resistance of kuruma prawn Penaeus japonicus and increase in phagocytic activity of prawn hemocytes after oral administration of ß-1, 3-glucan (Schizophyllan). Proceeding of the 3rd Asian Fisheries Forum. Asian Fisheries Society: 375-378.

16. Jian, J. and Z. Wu. 2003. Effects of traditional Chinese medicine on nonspecific immunity and disease resistance of large yellow croaker, Pseudosciaena crocea (Richardson). Aquaculture 218: 1-9.

17. Jian, J. and Z. Wu. 2004. Influences of traditional Chinese medicine on non-specific immunity of Jian Carp (Cyprinus carpio var. Jian). Fish and Shellfish Immunology 16: 185-191.

18. Li, Z.S., Y.M. Liu, Z.Y. Fang, L.M. Yang, M. Zhuang, Y.Y. Zhang, W. Zhao and P. Sun. 2014. Variation of sulforaphane levels in broccoli (Brassica oleracea var. italica) during flower development and the role of gene AOP2. Journal of Liquid Chromatography and Related Technologies 37: 1199-1211.

19. Lin, W., R.T. Wu, T. Wu, T.O. Khor, H. Wang and A.N. Kong. 2008. Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochemical Pharmacology 76: 967-973.

20. Liu, N., X. Deng, C. Liang and H. Cai. 2018. Effect of broccoli residues fermented with probiotics on the growth performance and health status of broilers challenged with Clostridium perfringens. Brazilian Journal of Poultry Science 20: 625-632.

21. Logambal, S.M., S. Venkatalakshmi and R. Dinakaran Michael. 2000. Immunostimulatory effect of leaf extract of Ocimum sanctum Linn. in Oreochromis mossambicus (Peters). Hydrobiologia 430: 113-120.

22. Oke, I.O., A.A. Dada and A.O. Adebayo. 2017. Dietary effects of Brassica oleracea on growth performance and haematological parameters of Oreochromis niloticus fingerlings. Journal of Food Agriculture and Environment 13: 133-136.

23. Panase, P., S. Saenphet and K. Saenphet. 2018. Biochemical and physiological responses of Nile tilapia Oreochromis niloticus Lin in subjected to cold shock of water temperature. Aquaculture Reports 11: 17-23.

24. Pasko, P., M. Krosniak, E. Prochownik, M. Tyszka-Czochara, M. Folta, R. Francik, J. Sikora, M. Malinowski and P. Zagrodzki. 2018. Effect of broccoli sprouts on thyroid function, haematological, biochemical, and immunological parameters in rats with thyroid imbalance. Biomedicine and Pharmacotherapy 97: 82-90.

25. Rao, Y.V. and R. Chakrabarti. 2005. Stimulation of immunity in Indian major carp Catla catla with herbal feed ingredients. Fish and Shellfish Immunology 18: 327-334.

26. Rao, Y.V., B.K. Das, P. Jyotyrmayee and R. Chakrabarti. 2006. Effect of Achyranthes aspera on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. Fish and Shellfish Immunology 20: 263-273.

27. Rao, Y.V., M. Romesh, A. Singh and R. Chakrabarti. 2004. Potentiation of antibody production in Indian major carp Labeo rohita, rohu, by Achyranthes aspera as a herbal feed ingredient. Aquaculture 238: 67-73.

28. Rengpipat, S., S. Rukpratanporn, S. Piyatiratitivorakul and P. Menasaveta. 2000. Immunity enhancement in black tiger shrimp (Penaeus monodon) by a probiont bacterium (Bacillus S11). Aquaculture 191: 271-288.

29. Ringo, E., R.E. Olsen, T.O. Gifstad, R.A. Dalmo, H. Amlund, G.I. Hemre and A.M. Bakke. 2010. Prebiotics in aquaculture: a review. Aquaculture Nutrition 16: 117-136.

30. Seeley, K.R., P.D. Gillespie and B.A. Weeks. 1990. A simple technique for the rapid spectrophotometric determination of phagocytosis by fish macrophages. Marine Environmental Research 30: 37-41.

31. Suganuma, H., J.W. Fahey, K.E. Bryan, Z.R. Healy and P. Talalay. 2011. Stimulation of phagocytosis by sulforaphane. Biochemical and Biophysical Research Communications 405: 146-151.

32. Tarozzi, A., C. Angeloni, M. Malaguti, F. Morroni, S. Hrelia and P. Hrelia. 2013. Sulforaphane as a potential protective phytochemical against neurodegenerative diseases. Oxidative Medicine and Cellular Longevity 2013: 1-10.

33. Thejass, P. and G. Kuttan. 2006. Antimetastatic activity of sulforaphane. Life Sciences 78: 3043-3050.

34. Thejass, P. and G. Kuttan. 2007. Immunomodulatory activity of sulforaphane, a naturally occurring isothiocyanate from broccoli (Brassica oleracea). Phytomedicine 14: 538-545.

35. Van Hai, N. and R. Fotedar. 2010. A review of probiotics in shrimp aquaculture. Journal of Applied Aquaculture 22: 251-266.

36. Woyengo, T.A., E. Kiarie and C.M. Nyachoti. 2011. Growth performance, organ weights, and blood parameters of broilers fed diets containing expeller-extracted canola meal.
Poultry Science 90: 2520-2527.

37. Yin, G., G. Jeney, T. Racz, P. Xu, X. Jun and Z. Jeney. 2006. Effect of two Chinese herbs (Astragalus radix and Scutellaria radix) on non-specific immune response of tilapia (Oreochromis niloticus). Aquaculture 253: 39-47.