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Effects of fucoidan on the hematic indicators and antioxidative responses of Nile tilapia (Oreochromis niloticus) fed diets contaminated with aflatoxin B1

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Abstract

Fucoidan is a rich source of medicinally active immunostimulants that possess various pharmacological properties. This study examined the potential impact of fucoidan on the hematic indicators and antioxidative responses of Nile tilapia fed diets contaminated with aflatoxin B1 (AFB1). Fish (60 ± 6.1 g) were allocated to five groups; the first (control) and second groups were fed 0% or 1% fucoidan–supplemented diets without AFB1 contamination, while the third, fourth, and fifth groups were fed diets contaminated with AFB1 and supplemented with 0%, 0.5%, and 1% fucoidan, respectively. After 30 days, fish fed AFB1 showed high ALT, AST, ALP, cholesterol, urea, and creatinine levels; furthermore, total blood protein and tissue (liver, kidney, and gill) glutathione (GSH), glutathione peroxidase (GPx), superoxide dismutase (SOD), and catalase (CAT) activity significantly (P ≤ 0.05) decreased in fish fed AFB1, while tissue malondialdehyde significantly increased (P ≤ 0.05). Interestingly, fish fed fucoidan showed decreased ALT, AST, ALP, cholesterol, urea, and creatinine, as well as increased blood protein, GSH, GPx, SOD, and CAT activity. The results suggested that fucoidan is capable of inducing protective activity against AFB1 toxicity in Nile tilapia by enhancing the serum biochemical and tissue antioxidant responses of fish.

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References

  • Abdel-Daim MM, Eissa IAM, Abdeen A, Abdel-Latif HMR, Ismail M, Dawood MAO, Hassan AM (2019) Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ Toxicol Pharmacol 69:44–50

    CAS  Google Scholar 

  • Abdelkhalek NK, Eissa IA, Ahmed E, Kilany OE, El-Adl M, Dawood MA, Hassan AM, Abdel-Daim MM (2017a) Protective role of dietary Spirulina platensis against diazinon-induced oxidative damage in Nile tilapia; Oreochromis niloticus. Environ Toxicol Pharmacol 54:99–104

    CAS  Google Scholar 

  • Abdelkhalek NK, Ghazy EW, Abdel-Daim MM (2015) Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Environ Sci Pollut Res Int 22:3023–3031

    CAS  Google Scholar 

  • Abdelkhalek NKM, Eissa IAM, Ahmed E, Kilany OE, El-Adl M, Dawood MAO, Hassan AM, Abdel-Daim MM (2017b) Protective role of dietary Spirulina platensis against diazinon-induced oxidative damage in Nile tilapia; Oreochromis niloticus. Environ Toxicol Pharmacol 54:99–104

    CAS  Google Scholar 

  • Adel M, Dadar M, Khajavi SH, Pourgholam R, Karimí B, Velisek J (2017) Hematological, biochemical and histopathological changes in Caspian brown trout (Salmo trutta caspius Kessler, 1877) following exposure to sublethal concentrations of chlorpyrifos. Toxin Rev 36:73–79

    CAS  Google Scholar 

  • Aebi H (1984) [13] Catalase in vitro. In Methods in enzymology (Vol. 105, pp. 121-126). Academic Press.

  • Ahmadifar E, Dawood MAO, Moghadam MS, Sheikhzadeh N, Hoseinifar SH, Musthafa MS (2019) Modulation of immune parameters and antioxidant defense in zebrafish (Danio rerio) using dietary apple cider vinegar. Aquaculture 513:734412

  • Aliko V, Qirjo M, Sula E, Morina V, Faggio C (2018) Antioxidant defense system, immune response and erythron profile modulation in gold fish, Carassius auratus, after acute manganese treatment. Fish Shellfish Immunol 76:101–109

    Google Scholar 

  • Alinezhad S, Tolouee M, Kamalzadeh A, Motalebi A, Nazeri M, Yasemi M, Shams-Ghahfarokhi M, Tolouei R, Razzaghi-Abyaneh M (2011) Mycobiota and aflatoxin B1 contamination of rainbow trout (Oncorhinchus mykiss) feed with emphasis to Aspergillus section Flavi. Iran J Fish Sci 10:363–374

    Google Scholar 

  • Amin A, El Asely A, Abd El-Naby AS, Samir F, El-Ashram A, Sudhakaran R, Dawood MAO (2019) Growth performance, intestinal histomorphology and growth-related gene expression in response to dietary Ziziphus mauritiana in Nile tilapia (Oreochromis niloticus). Aquaculture 512:734301

    CAS  Google Scholar 

  • Atashrazm F, Lowenthal R, Woods G, Holloway A, Dickinson J (2015) Fucoidan and cancer: a multifunctional molecule with anti-tumor potential. Marine drugs 13:2327–2346

    CAS  Google Scholar 

  • Burgos-Aceves MA, Cohen A, Paolella G, Lepretti M, Smith Y, Faggio C, Lionetti L (2018a) Modulation of mitochondrial functions by xenobiotic-induced microRNA: from environmental sentinel organisms to mammals. Sci Total Environ 645:79–88

    CAS  Google Scholar 

  • Burgos-Aceves MA, Cohen A, Smith Y, Faggio C (2018b) MicroRNAs and their role on fish oxidative stress during xenobiotic environmental exposures. Ecotoxicol Environ Saf 148:995–1000

    CAS  Google Scholar 

  • Cagauan A G, Tayaban R H, Somga J, Bartolome R M (2004) Effect of aflatoxin-contaminated feeds in Nile tilapia (Oreochromis niloticus L.). In Abstract of the 6th international symposium on tilapia in aquaculture (ISTA 6) section: health management and diseases Manila, Philippines (Vol. 12, p. 16).

  • Carbone D, Faggio C (2016) Importance of prebiotics in aquaculture as immunostimulants. Effects on immune system of Sparus aurata and Dicentrarchus labrax. Fish Shellfish Immunol 54:172–178

    CAS  Google Scholar 

  • Chestnut A, Anderson P, Cochran M, Fribourg H, Gwinn K (1992) Effects of hydrated sodium calcium aluminosilicate on fescue toxicosis and mineral absorption. J Anim Sci 70:2838–2846

    CAS  Google Scholar 

  • Chotigeat W, Tongsupa S, Supamataya K, Phongdara A (2004) Effect of fucoidan on disease resistance of black tiger shrimp. Aquaculture 233:23–30

    CAS  Google Scholar 

  • Cotty PJ, Jaime-Garcia R (2007) Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int J Food Microbiol 119:109–115

    CAS  Google Scholar 

  • Dawood MA, Shukry M, Zayed MM, Omar AA, Zaineldin AI, El Basuini MF (2019a) Digestive enzymes, immunity and oxidative status of Nile tilapia (Oreochromis niloticus) reared in intensive conditions.  Slov Vet Res 56 56(22-Suppl)

  • Dawood MAO, Abo-Al-Ela HG, Hasan MT (2020a) Modulation of transcriptomic profile in aquatic animals: probiotics, prebiotics and synbiotics scenarios. Fish Shellfish Immunol 97:268–282

    CAS  Google Scholar 

  • Dawood MAO, Koshio S (2019) Application of fermentation strategy in aquafeed for sustainable aquaculture. Rev Aquac. https://doi.org/10.1111/raq.12368

  • Dawood MAO, Koshio S, Esteban MÁ (2018) Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Rev Aquac 10:950–974

    Google Scholar 

  • Dawood MAO, Moustafa EM, Gewaily MS, Abdo SE, AbdEl-kader MF, SaadAllah MS, Hamouda AH (2019b) Ameliorative effects of Lactobacillus plantarum L-137 on Nile tilapia (Oreochromis niloticus) exposed to deltamethrin toxicity in rearing water. Aquat Toxicol 219:105377

  • Dawood MAO, Moustafa EM, Gewaily MS, Abdo SE, AbdEl-kader MF, SaadAllah MS, Hamouda AH (2020b) Ameliorative effects of Lactobacillus plantarum L-137 on Nile tilapia (Oreochromis niloticus) exposed to deltamethrin toxicity in rearing water. Aquat Toxicol 219:105377

    Google Scholar 

  • Dawood MAO, Zommara M, Eweedah NM, Helal AI (2019c) Synergistic effects of selenium nanoparticles and vitamin E on growth, immune-related gene expression, and regulation of antioxidant status of Nile tilapia (Oreochromis niloticus). Biol Trace Elem Res. https://doi.org/10.1007/s12011-019-01857-6

  • Deng S-X, Tian L-X, Liu F-J, Jin S-J, Liang G-Y, Yang H-J, Du Z-Y, Liu Y-J (2010) Toxic effects and residue of aflatoxin B1 in tilapia (Oreochromis niloticus × O. aureus) during long-term dietary exposure. Aquaculture 307:233–240

    CAS  Google Scholar 

  • 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 162:168–173

    CAS  Google Scholar 

  • El-Sayed YS, Khalil RH (2009) Toxicity, biochemical effects and residue of aflatoxin B1 in marine water-reared sea bass (Dicentrarchus labrax L.). Food Chem Toxicol 47:1606–1609

    CAS  Google Scholar 

  • El Megid AA, Abd Al Fatah ME, El Asely A, El Senosi Y, Moustafa MMA, Dawood MAO (2020) Impact of pyrethroids and organochlorine pesticides residue on IGF-1 and CYP1A genes expression and muscle protein patterns of cultured Mugil capito. Ecotoxicol Environ Saf 188:109876

    Google Scholar 

  • Ellis AE, Hastings TS, Munro ALS (1981) The role of Aeromonas salmonicida extracellular products in the pathology of furunculosis. J Fish Dis 4:41–51

    Google Scholar 

  • FAO (2018) Food and Agriculture Organization. The State of World Fisheries and Aquaculture; FAO: Rome, Italy.

  • Fitton JH (2011) Therapies from fucoidan; multifunctional marine polymers. Marine drugs 9:1731–1760

    CAS  Google Scholar 

  • Gobi N, Vaseeharan B, Rekha R, Vijayakumar S, Faggio C (2018) Bioaccumulation, cytotoxicity and oxidative stress of the acute exposure selenium in Oreochromis mossambicus. Ecotoxicol Environ Saf 162:147–159

    CAS  Google Scholar 

  • Guardiola FA, Porcino C, Cerezuela R, Cuesta A, Faggio C, Esteban MA (2016) Impact of date palm fruits extracts and probiotic enriched diet on antioxidant status, innate immune response and immune-related gene expression of European seabass (Dicentrarchus labrax). Fish Shellfish Immunol 52:298–308

    CAS  Google Scholar 

  • Haroun-Bouhedja F, Ellouali M, Sinquin C, Boisson-Vidal C (2000) Relationship between sulfate groups and biological activities of fucans. Thromb Res 100:453–459

    CAS  Google Scholar 

  • Hessein A, Marakby H, Abd Rahamn G, Ayyat M (2014) Aflatoxin B 1 toxicity and its reduction by using coumarine and vitamin E in Nile tilapia. Zagazig J Agric Res 73:83

    Google Scholar 

  • Immanuel G, Sivagnanavelmurugan M, Marudhupandi T, Radhakrishnan S, Palavesam A (2012) The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon (Fab). Fish Shellfish Immunol 32:551–564

    CAS  Google Scholar 

  • Jyothi B, Narayan G (1999) Certain pesticide-induced carbohydrate metabolic disorders in the serum of freshwater fish Clarias batrachus (Linn.). Food Chem Toxicol 37:417–421

    CAS  Google Scholar 

  • Kumar N, Antony Jesu Prabhu P, Pal AK, Remya S, Aklakur M, Rana RS, Gupta S, Raman RP, Jadhao SB (2011) Anti-oxidative and immuno-hematological status of tilapia (Oreochromis mossambicus) during acute toxicity test of endosulfan. Pestic Biochem Physiol 99:45–52

    CAS  Google Scholar 

  • Li Z, Xue C, 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 antioxidation in vivo. J Fish China 25:64–68

    CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Marin DE, Taranu I (2012) Overview on aflatoxins and oxidative stress. Toxin Rev 31:32–43

    CAS  Google Scholar 

  • Mohapatra S, Sahu N, Pal A, Prusty A, Kumar V, Kumar S (2011) Haemato-immunology and histo-architectural changes in Labeo rohita fingerlings: effect of dietary aflatoxin and mould inhibitor. Fish Physiol Biochem 37:177–186

    CAS  Google Scholar 

  • Moustafa EM, Dawood MAO, Assar DH, Omar AA, Elbialy ZI, Farrag FA, Shukry M, Zayed MM (2019) Modulatory effects of fenugreek seeds powder on the histopathology, oxidative status, and immune related gene expression in Nile tilapia (Oreochromis niloticus) infected with Aeromonas hydrophila. Aquaculture 515:734589

  • Ngethe S, Horsberg TE, Mitema E, Ingebrigtsen K (1993) Species differences in hepatic concentration of orally administered 3H-AFB1 between rainbow trout (Oncorhynchus mykiss) and tilapia (Oreochromis niloticus). Aquaculture 114:355–358

    CAS  Google Scholar 

  • Nishikimi M, Rao NA, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854

    CAS  Google Scholar 

  • Peixoto MJ, Salas-Leitón E, Pereira LF, Queiroz A, Magalhães F, Pereira R, Abreu H, Reis PA, Gonçalves JFM, de Almeida ORO (2016) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquac Rep 3:189–197

    Google Scholar 

  • Racicot J, Gaudet M, Leray C (1975) Blood and liver enzymes in rainbow trout (Salmo gairdneri rich.) with emphasis on their diagnostic use: study of CCl4 toxicity and a case of Aeromonas infection. J Fish Biol 7:825–835

    CAS  Google Scholar 

  • Rahman ANA, Abdellatief SA, Mahboub HHH (2017) Protection of Nile tilapia, Oreochromis niloticus from aflatoxin B1 toxicity by dietary supplementation with fennel essential oil and Saccharomyces cerevisiae. Egypt J Aquat Res 43:235–240

    Google Scholar 

  • Rashidian G, Bahrami Gorji S, Farsani MN, Prokic MD, Faggio C (2018) The oak (Quercus brantii) acorn as a growth promotor for rainbow trout (Oncorhynchus mykiss): growth performance, body composition, liver enzymes activity and blood biochemical parameters. Nat Prod Res 23:1–11

  • Santacroce MP, Conversano M, Casalino E, Lai O, Zizzadoro C, Centoducati G, Crescenzo G (2008) Aflatoxins in aquatic species: metabolism, toxicity and perspectives. Rev Fish Biol Fish 18:99–130

    Google Scholar 

  • Sharbidre AA, Metkari V, Patode P (2011) Effect of methyl parathion and chlorpyrifos on certain biomarkers in various tissues of guppy fish, Poecilia reticulata. Pestic Biochem Physiol 101:132–141

    CAS  Google Scholar 

  • Sharma G, Kar S, Ball WB, Ghosh K, Das PK (2014) The curative effect of fucoidan on visceral leishmaniasis is mediated by activation of MAP kinases through specific protein kinase C isoforms. Cell Mol Immunol 11:263

    CAS  Google Scholar 

  • Shekarabi S P H, Omidi A H, Dawood M A, Adel M, Avazeh A, Heidari F J A o AS (2019) Effect of black mulberry (Morus nigra) powder on growth performance, biochemical parameters, blood carotenoid concentration, and fillet color of rainbow trout. Annals of Animal Science (published online ahead of print). doi: https://doi.org/10.2478/aoas-2019-0068

  • Si-si L, Qiu-kuan W, Yun-hai H, Dan-dan R, Ze-yu Z (2013) The extraction and serum lipids reducing function of fucoidan from seaweed Costaria costata. J Dalian Ocean Univ 20

  • Srichaiyo N, Tongsiri S, Hoseinifar SH, Dawood MAO, Jaturasitha S, Esteban MÁ, Ringø E, Van Doan H (2020) The effects gotu kola (Centella asiatica) powder on growth performance, skin mucus, and serum immunity of Nile tilapia (Oreochromis niloticus) fingerlings. Aquac Rep 16:100239

    Google Scholar 

  • Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G (2009) Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shellfish Immunol 27:105–111

    Google Scholar 

  • Tuan NA, Grizzle JM, Lovell RT, Manning BB, Rottinghaus GE (2002) Growth and hepatic lesions of Nile tilapia (Oreochromis niloticus) fed diets containing aflatoxin B1. Aquaculture 212:311–319

    Google Scholar 

  • Tuller J, De Santis C, Jerry DR (2014) Dietary influence of fucoidan supplementation on growth of Lates calcarifer (Bloch). Aquac Res 45:749–754

    CAS  Google Scholar 

  • Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278

    CAS  Google Scholar 

  • Van Doan H, Hoseinifar SH, Ringø E, Ángeles Esteban M, Dadar M, Dawood MA, Faggio C (2020) Host-associated probiotics: a key factor in sustainable aquaculture. Rev Fish Sci Aquac 28:16-42

  • Van Doan H, Hoseinifar SH, Sringarm K, Jaturasitha S, Yuangsoi B, Dawood MAO, Esteban MÁ, Ringø E, Faggio C (2019) Effects of Assam tea extract on growth, skin mucus, serum immunity and disease resistance of Nile tilapia (Oreochromis niloticus) against Streptococcus agalactiae. Fish Shellfish Immunol 93:428–435

    Google Scholar 

  • Wang J, Zhang Q, Zhang Z, Song H, Li P (2010) Potential antioxidant and anticoagulant capacity of low molecular weight fucoidan fractions extracted from Laminaria japonica. Int J Biol Macromol 46:6–12

    CAS  Google Scholar 

  • Wu Q, Xing Y, Rong X, Huang P (2007) Influence of FPS on the expression of LDL-R mRNA in the liver tissues of hyperlipidemic rats. J Chin Med Mater 30:968–970

    CAS  Google Scholar 

  • Yan J, Guo C, Dawood MAO, Gao J (2017) Effects of dietary chitosan on growth, lipid metabolism, immune response and antioxidant-related gene expression in Misgurnus anguillicaudatus. Benefic Microbes 8:439–449

    CAS  Google Scholar 

  • 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 41:264–270

    CAS  Google Scholar 

  • Yao J, Wang J-Y, Liu L, Li Y-X, Xun A-Y, Zeng W-S, Jia C-H, Wei X-X, Feng J-L, Zhao L, Wang L-S (2010) Anti-oxidant effects of resveratrol on mice with DSS-induced ulcerative colitis. Arch Med Res 41:288–294

    CAS  Google Scholar 

  • Zhao X, Xue C, Wang J, Zhaojie L, Hongtao Q (2003) Hepatoprotective activity of low molecular fucoidan oligosaccharides from Laminaria japonica in mice with liver injury. Acta Nutrimenta Sin 25:286-289  

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This work was funded by Researchers Supporting Project number (RSP 2019/ 121), King Saud University, Riyadh, Saudi Arabia.

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Abdel-Daim, M.M., Dawood, M.A., Aleya, L. et al. Effects of fucoidan on the hematic indicators and antioxidative responses of Nile tilapia (Oreochromis niloticus) fed diets contaminated with aflatoxin B1. Environ Sci Pollut Res 27, 12579–12586 (2020). https://doi.org/10.1007/s11356-020-07854-w

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