Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 439–454 | Cite as

The effect of dietary fucoidan on growth, immune functions, blood characteristics and oxidative stress resistance of juvenile red sea bream, Pagrus major

  • Nadia Mahjabin Sony
  • Manabu Ishikawa
  • Md. Sakhawat HossainEmail author
  • Shunsuke Koshio
  • Saichiro Yokoyama


We determined the supplementation effects of dietary fucoidan on growth, immune responses, blood characteristics, and oxidative stress resistance of juvenile red sea bream. A fishmeal (FM)-based basal diet supplemented with 0% (D1, control), 0.05% (D2), 0.1% (D3), 0.2% (D4), 0.4% (D5), and 0.8% (D6) mozuku fucoidan to formulate six experimental diets. Each diet was randomly allocated to triplicate groups of fish (3.8 g) for 60 days. Results showed that fish-fed diet D5 showed significantly higher (P < 0.05) growth performance compared to the control (D1). Diet groups D2 to D4 also showed intermediate values compared to D1. Feed conversion efficiency and protein efficiency ratio were significantly higher in diet group D5, which was not significantly different with D3. Fucoidan supplementation increased whole-body lipid, which was significantly higher in the D5 group. Condition factor (CF) was significantly higher in fish fed ≥ 0.2% fucoidan-supplemented diet groups. Diet group D5 and D4 showed significantly lower blood urea nitrogen (BUN) and aspartate aminotransferase (AST) level, respectively. Dietary fucoidan reduced the oxidative stress of fish. Among the measured nonspecific immune parameters, only peroxidase activity (PA) and total serum protein (TSP) were significantly influenced by dietary supplementation and it was higher in D4 group. Fucoidan supplementation reduces thiobarbituric acid reactive substance (TBARS) values numerically and it was lowest in fish-fed diet group D5. Under the present experimental condition, finally, we concluded that 0.3–0.4% dietary fucoidan supplementation enhanced the growth and health performance of red sea bream by increasing growth, immune response, blood characteristics, and oxidative stress resistance.


Fucoidan Growth Immune responses Blood characteristics Oxidative stress Pagrus major 



This research was supported by the Management Expenses Grants of the United Graduate School of Agricultural Sciences, Kagoshima University provided to Dr. Shunsuke Koshio. The first author would like to thank Serge Dossou, Mr. Kokubu, and Mr. Taniguchi for their valuable help during feeding trial and sample analysis.


  1. Anderson DP, Siwicki AK (1995) Basic hematology and serology for fish health programs. In: Shariff M, Arthur JR, Subasinghe RP (eds) Diseases in Asian Aquaculture, Philippines, fish health section, vol II. Asian Fisheries Society, Manila, pp 185–202Google Scholar
  2. Araújo M, Rema P, Sousa-Pinto I, Cunha L, Peixoto M, Pires M, Seixas F, Brotas V, Beltrán C, Valente LP (2016) Dietary inclusion of IMTA-cultivated Gracilaria vermiculophylla in rainbow trout (Oncorhynchus mykiss) diets: effects on growth, intestinal morphology, tissue pigmentation, and immunological response. J Appl Phycol 28(1):679–689Google Scholar
  3. Armstrong D, Browne R (1994) The analysis of free radicals, lipid peroxides, antioxidant enzymes and compounds to oxidative stress as applied to the clinical chemistry laboratory. Adv Exp Med Biol 366:43–58CrossRefGoogle Scholar
  4. Association of Official Analytical Chemists (AOAC) (1995) Official methods of analysis, 16th edn. INTERNATIONAL, ArlingtonGoogle Scholar
  5. Assreuy AMS, Gomes DM, Silva MSJ, Torres VM, Siqueira RCL, Pires AF, Criddle DN, Alencar NMN, Cavada BS, Sampaio AH, Farias WRL (2008) Biological effects of a sulfated-polysaccharide isolated from the marine red algae Champia feldmannii. Biol Pharm Bull 31(4):691–695CrossRefGoogle Scholar
  6. Atashrazm F, Lowenthal RM, Woods GM, Holloway AF, Dickinson JL (2015) Fucoidan and cancer: a multifunctional molecule with anti-tumor potential. Mar Drugs 13:2327–2346CrossRefGoogle Scholar
  7. Bager F, Aarestrup FM, Wegner HG (2000) Dealing with antimicrobial resistance—the Danish experience. Can J Anim Sci 80:223–228CrossRefGoogle Scholar
  8. Ballerini A, Civitareale C, FIori M, Regini M, Brambilla G (2003) Traceability of inbred and crossbred Cinta Senese pigs by evaluating the oxidative stress. J Veterinary Med Ser A 50(3):113–116CrossRefGoogle Scholar
  9. Cerezuela R, Guardiola FA, González P, Meseguer J, Esteban MÁ (2012) Effects of dietary Bacillus subtilis, Tetraselmis chuii, and Phaeodactylum tricornutum, singularly or in combination, on the immune response and disease resistance of sea bream (Sparus aurata L.). Fish Shellfish Immunol 33(2):342–349CrossRefGoogle Scholar
  10. Choi EM, Kim AJ, Kim YO, Hwang JK (2005) Immunomodulating activity of arabinogalactan and fucoidan in vitro. Med Food 8(4):446–453CrossRefGoogle Scholar
  11. Chotigeat W, Tongsupa S, Supamataya K, Phongdara A (2004) Effect of fucoidan on disease resistance of black tiger shrimp. Aquaculture 233:23–30CrossRefGoogle Scholar
  12. El-Boshy M, El-Ashram A, Risha E, Abdelhamid F, Zahran E, Gab-Alla A (2014) Dietary fucoidan enhance the non-specific immune response and disease resistance in African catfish, Clarias gariepinus, immunosuppressed by cadmium chloride. Vet Immunol Immunopathol 162:168–173CrossRefGoogle Scholar
  13. Eslamloo K, Falahatkar B, Yokoyama S (2012) Effects of dietary bovine lactoferrin on growth, physiological performance, iron metabolism and non-specific immune responses of Siberian sturgeon Acipenser baeri. Fish Shellfish Immunol 32:976–985CrossRefGoogle Scholar
  14. Fitton JH (2011) Therapies from fucoidan; multifunctional marine polymers. Mar Drugs 9:1731–1760CrossRefGoogle Scholar
  15. Goth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–152CrossRefGoogle Scholar
  16. Haroun-Bouhedja F, Ellouali M, Sinquin C, Boisson-Vidal C (2000) Relationship between sulfate groups and biological activities of fucans. Thromb Res 100:453–459CrossRefGoogle Scholar
  17. Hossain MS, Koshio S (2017) Dietary substitution of fishmeal by alternative protein with guanosine monophosphate supplementation influences growth, digestibility, blood chemistry profile, immunity and stress resistance of red sea bream, Pagrus major. Fish Physiol Biochem 43(6):1629–1644CrossRefGoogle Scholar
  18. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM (2016a) Dietary effects of adenosine monophosphate to enhance growth, digestibility, innate immune responses and stress resistance of juvenile red sea bream, Pagrus major. Fish Shellfish Immunol 56:523–533CrossRefGoogle Scholar
  19. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM, Ono S, Fujieda T (2016b) Comparison of the effects of inosine and inosine monophosphate on growth, immune response, stress resistance and gut morphology of juvenile red sea bream, Pagrus major. Aquaculture 458:64–74CrossRefGoogle Scholar
  20. Hossain MS, Koshio S, Ishikawa M, Yokoyama S, Sony NM (2016c) Effects of dietary administration of guanosine monophosphate on the growth, digestibility, innate immune responses and stress resistance of juvenile red sea bream, Pagrus major. Fish Shellfish Immunol 57:96–106CrossRefGoogle Scholar
  21. Huang XH, Zhou H, Zhang H (2006) The effect of Sargassum fusiforme polysaccharides extracts on vibriosis resistance and immune activity of the shrimp Fenneropenaeus chinensis. Fish Shellfish Immunol 20:750–757CrossRefGoogle Scholar
  22. Kalimuthu S, Kim S (2015) Fucoidan, a sulfated polysaccharides from brown algae as therapeutic target for cancer. In: Kim S (ed) Handbook of anticancer drugs from marine origin. Springer International Publishing, Cham, p 147Google Scholar
  23. Kim EA, Lee S-H, Ko C, Cha SH, Kang MC, Kang SM, Ko SC, Lee WW, Ko JY, Lee JH, Kang N, Oh JY, Ahn G, Jee YH, Jeon YJ (2014) Protective effect of fucoidan against AAPH-induced oxidative stress in zebrafish model. Carbohydr Polym 102:185–191CrossRefGoogle Scholar
  24. Kitikiew S, Chen JC, Putra DF, Lin YC, Yeh ST, Liou CH (2013) Fucoidan effectively provokes the innate immunity of white shrimp Litopenaeus vannamei and its resistance against experimental Vibrio alginolyticus infection. Fish Shellfish Immunol 34:280–290CrossRefGoogle Scholar
  25. Kumar S, Sahu NP, Pal AK, Choudhury D, Yengkokpam S, Mukherjee SC (2005) Effect of dietary carbohydrate on haematology, respiratory burst activity and histological changes in L. rohita juveniles. Fish Shellfish Immunol 19:331–344CrossRefGoogle Scholar
  26. Lemaire P, Drai P, Mathieu A, Lemaire S, Carriere S, Giudicelli J, Lafaurie M (1991) Changes with different diets in plasma enzymes (GOT, GPT, LDH, ALP) and plasma lipids (cholesterol, triglycerides) of sea-bass (Dicentrarchus labrax). Aquaculture 93:63–75CrossRefGoogle Scholar
  27. Li ZJ, Xue CH, Chen L, Fang Y, Lin H (2001) Scavenging effects of fucoidan fractions of low molecular weight extracted from Laminaria japonica on radicals of active oxygen and antioxidant in vivo. J Fish China 25(1):64–68Google Scholar
  28. Li P, Burr GS, Goff JB, Whiteman KW, Davis KB, Vega RR, Neill WH, Gatlin DMIII (2005) A preliminary study on the effects of dietary supplementation of brewers yeast and nucleotides, singularly or in combination, on juvenile red drum (Sciaenops ocellatus). Aquac Res 36:1120–1127CrossRefGoogle Scholar
  29. Li B, Lu F, Wei XJ, Zhao RX (2008) Fucoidan: structure and bioactivity. Molecules 13(8):1671–1695CrossRefGoogle Scholar
  30. Li SS, Wang QK, He YH, Ren DD, Zhang ZY (2013) The extraction of serum lipids reducing function of fucoidan from seaweed Costaria costata. J Dalian Ocean Univ 28(1):93–98Google Scholar
  31. Lygren B, Sveier H, Hjeltnes B, Waagbo R (1999) Examination of the immunomodulatory properties and the effect on disease resistance of dietary bovine lactoferrin and vitamin C fed to Atlantic salmon (Salmo salar) for a short-term period. Fish Shellfish Immunol 9:95–107CrossRefGoogle Scholar
  32. Martinez-Alvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish 15:75–88CrossRefGoogle Scholar
  33. Morganti P, Bruno C, Guarneri F, Cardillo A, Del Ciotto P, Valenzano F (2002) Role of topical and nutritional supplement to modify the oxidative stress. Int J Cosmet Sci 24(6):331–339CrossRefGoogle Scholar
  34. Mulloy B, Ribeiro A, Alves A, Vieira R, Mourao P (1994) Sulfated fucans from echinoderms have a regular tetra saccharide repeating unit defined by specific patterns of sulfation at the o-2 and o-4 positions. J Biol Chem 269(35):22113–22123Google Scholar
  35. Nakagawa H, Umino T, Tasaka Y (1997) Usefulness of Ascophyllum meal as a feed additive for red sea bream, Pagrus major. Aquaculture 151:275–281CrossRefGoogle Scholar
  36. Okai Y, Higashi-Okai K, Ishizaka S, Ohtani K, Mastsui-Yuasa I, Yamashita U (1996) Possible immunodulating activities in an extract of edible brown alga, Hijikia fusiforme (Hijiki). J Sci Food Agric 72(4):455–460CrossRefGoogle Scholar
  37. Ozório RA, Lopes RG, Góes BS, Silva CP, Derner RB, Fracalossi DM (2015) Growth and enzymatic profile of the pacific white shrimp fed with Porphyridium cruentum extract. Bol Inst Pesca São Paulo 41(1):123–131Google Scholar
  38. Pasquini A, Luchetti E, Marchetti V, Cardini G (2008) Analytical performances of d-ROMs test and BAP test in canine plasma. Definition of the normal range in healthy Labrador dogs. Vet Res Commun 32:137–143CrossRefGoogle Scholar
  39. Peixoto MJ, Leitón ES, Pereira LF, Queiroz A, Magalhães F, Pereira R, Abreu H, Reis PA, Goncalves JFM, Ozório ROA (2016) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquacult Rep 3:189–197CrossRefGoogle Scholar
  40. Pomin VH (2012) Fucanomics and galactanomics: current status in drug discovery, mechanisms of action and role of the well-defined structures. Biochim Biophys Acta 1820:1971–1979CrossRefGoogle Scholar
  41. Prabu DL, Sahu NP, Pal AK, Dasgupta S, Narendra A (2016) Immunomodulation and interferon gamma gene expression in sutchi cat fish, Pangasianodon hypophthalmus: effect of dietary fucoidan rich seaweed extract (FRSE) on pre and post challenge period. Aquac Res 47(1):199–218CrossRefGoogle Scholar
  42. Ramazanov Z, Jimenez del Rio M, Ziegenfuss T (2003) Sulfated polysaccharides of brown seaweed Cystoseira canariensis bind to serum myostatin protein. Acta Physiol Pharmacol Bulg 27:101–106Google Scholar
  43. Ribeiro A, Vieira R, Mourao P, Mulloy B (1994) A sulfated a-l-fucan from sea cucumber. Carbohydr Res 255:225–240CrossRefGoogle Scholar
  44. Rosmini MR, Perlo F, Pérez-Alvarez JA, Pagán-Moreno MJ, Gago-Gago A, López-Santoveña F, Aranda-Catalá V (1996) TBA test by an extractive method applied to ‘Paté’. Meat Sci 42:103–110CrossRefGoogle Scholar
  45. Salinas I, Abelli L, Bertoni F, Picchietti S, Roque A, Furones D, Cuesta A, Meseguer J, Esteban MA (2008) Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 25:114–123CrossRefGoogle Scholar
  46. Sivagnanavelmurugan M, Thaddaeus BJ, Palavesam A, Immanuel G (2014) Dietary effect of Sargassum wightii fucoidan to enhance growth, prophenoloxidase gene expression of Penaeus monodon and immune resistance to Vibrio parahaemolyticus. Fish Shellfish Immunol 39:439–449CrossRefGoogle Scholar
  47. Sole M, Rodríguez V, Papiol F, Maynou F, Cartes E (2009) Xenobiotic metabolism in marine fish with different trophic strategies and their relationship to ecological variables. Comp Biochem Physiol 149C:83–89Google Scholar
  48. Swain P, Dash S, Sahoo P, Routray P, Sahoo S, Gupta SD, Meher PK, Sarangi N (2007) Non-specific immune parameters of brood Indian major carp Labeo rohita and their seasonal variations. Fish Shellfish Immunol 22(1–2):38–43CrossRefGoogle Scholar
  49. Takahashi Y, Uehara K, Watanabe R, Okumura T, Yamashita T, Omura H et al (1998) Efficacy of oral administration of fucoidan, a sulfated polysaccharide in controlling white spot syndrome in kuruma shrimp in Japan. In: Flegel TW (ed) Advance in shrimp biotechnology. National Center for Genetic Engineering and Biotechnology, Bangkok, pp 171–173Google Scholar
  50. Traifalgar RF, Kira H, Tung HT, Michael FR, Yokoyama ALS, Ishikaw MA, Koshio S (2010) Influence of dietary fucoidan supplementation on growth and immunological response of juvenile Marsupenaeus japonicus. J World Aquacult Soc 41:235–244CrossRefGoogle Scholar
  51. Trichet VV (2010) Nutrition and immunity: an update. Aquac Res 41:356–372CrossRefGoogle Scholar
  52. Tuller J, Santis CD, Jerry DR (2014) Dietary influence of Fucoidan supplementation on growth of Lates calcarifer (Bloch). Aquac Res 45:749–754CrossRefGoogle Scholar
  53. Wei WQ, Cong JB, Xian H, Zhang QJ, Hu YJ, Wu K et al (2001) The effect of polysaccharides from seaweed (SPS) on regulating the immune function in mice. Chin J New Drugs 10(9):35–37Google Scholar
  54. Xing YH (2005) The regulation of FPS on blood lipids and its mechanism in hyperlipidmia animals. MS thesis, Guangzhou University of Chinese Medicine; 2005. p. 1–43Google Scholar
  55. Yagi K (1998) Simple assay for the level of total lipid peroxides in serum or plasma. Methods Mol Biol 108:101–106Google Scholar
  56. Yang MX, Ma CH, Sun JT, Shao QQ, Gao WJ, Zhang Y, Li Z, Xie Q, Dong Z, Qu X (2008) Fucoidan stimulation induces a functional maturation of hunman monocyte-derived dendritic cells. Int Immunopharmacol 8(13–14):1754–1760CrossRefGoogle Scholar
  57. Yang Q, Yang R, Li M, Zhou Q, Liang X, Elmada ZC (2014) Effects of dietary fucoidan on the blood constituents, anti-oxidation and innate immunity of juvenile yellow catfish (Pelteobagrus fulvidraco). Fish Shellfish Immunol 41:264–270CrossRefGoogle Scholar
  58. Ye H, Wang KQ, Zhou CH, Liu J, Zeng XX (2008) Purification, antitumor and antioxidant activities in vitro of polysaccharides from the brown seaweed Sargassum pallidum. Food Chem 111(2):428–432CrossRefGoogle Scholar
  59. Yone Y, Furuichi M, Urano K (1986) Effects of dietary wakame Undaria pinnatifida and Ascophyllum nodosum supplements on growth, feed efficiency, and proximate compositions of liver and muscle of red sea bream. Bull Jpn Soc Sci Fish 52:1465–1488CrossRefGoogle Scholar
  60. Zhao X, Xue CH, Wang JF, Li ZJ, Qi HT (2003) Hepatoprotective activity of low molecular fucoidan oligosaccharides from Laminaria Japonica in mice with liver injury. Acta Nutr Sin 25(3):286–289Google Scholar
  61. Zhou MJ (2006) The extraction, structural analysis and antioxidation of fucoidan. MS thesis, Zhejiang University, p. 1–78Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Nadia Mahjabin Sony
    • 1
    • 2
  • Manabu Ishikawa
    • 1
    • 2
  • Md. Sakhawat Hossain
    • 2
    • 3
    Email author
  • Shunsuke Koshio
    • 1
    • 2
  • Saichiro Yokoyama
    • 2
  1. 1.The Graduate School of FisheriesKagoshima UniversityKagoshimaJapan
  2. 2.Laboratory of Aquatic Animal Nutrition, Faculty of FisheriesKagoshima UniversityKagoshima CityJapan
  3. 3.Department of Aquaculture, Faculty of FisheriesSylhet Agricultural UniversitySylhetBangladesh

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