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The protective role of spirulina and β-glucan in African catfish (Clarias gariepinus) against chronic toxicity of chlorpyrifos: hemato-biochemistry, histopathology, and oxidative stress traits

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Abstract

Chlorpyrifos (CPF) is an insecticide that is commonly applied in the agriculture sector. However, little is known about the protective role of Spirulina platensis (SP) and/or β-glucan (BG) on African catfish exposed to chronic CPF toxicity. The fish (95 ± 5 g, initial weight) were assigned to 5 fiberglass tanks (500 L, 50 fish/tank) where the 1st and 2nd fed the basal diet, while the 3rd, 4th, and 5th fed diets with SP, BG, and SP+BG at 0.5%, respectively. Fish in 2nd, 3rd, 4th, and 5th groups were exposed to CPF at a dose of 1.5 mg/L and fed the respective diets for 60 days. In comparison with the control group, CPF-exposed fish exhibited significantly lower (P ≤ 0.05) body weights, feed intake, red blood cells count, hemoglobin concentration, packed cell volume (PCV) (%), lymphocytes, monocytes, phagocytic activity, and phagocytic index, while feed conversion ratio, white blood cell count, and neutrophils count were significantly increased. Fish exposed to CPF also revealed a significant elevation in aspartate aminotransferase (AST), alanine aminotransferase (ALT), cholesterol, triglycerides, low-density lipoproteins (LDL), very-low-density lipoproteins (vLDL), glucose concentration, urea, and creatinine as well as low total proteins, albumin, globulins, and high-density lipoprotein (HDL) concentration. Fish exposed to CPF also exhibited a high concentration of malondialdehyde while glutathione content, glutathione peroxidase, and catalase activities were significantly decreased in the liver, gills, brain, and intestine tissues. Moreover, exposure to CPF resulted in higher transcription of cytochrome P450 (CYP1A-P450) gene expression than the 1st group. Histopathological investigations revealed various degrees of pathological lesions in different organs like the liver, kidney, brain, spleen, and intestine tissues. Interestingly, dietary SP supplementation either alone or combined with BG significantly ameliorated the alterations mitigated by CPF-induced organ injuries and genotoxicity. Therefore, it could be concluded that SP or/and BG are able to induce the protective consequences on health status, immunity, and antioxidative response of African catfish exposed to CPF.

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References

  • Abdel-Daim MM (2014) Pharmacodynamic interaction of Spirulina platensis with erythromycin in Egyptian Baladi bucks (Capra hircus). Small Rumin Res 120:234–241

    Google Scholar 

  • Abdel-Daim MM, Dawood MAO, Elbadawy M, Aleya L, Alkahtani S (2020) Spirulina platensis reduced oxidative damage induced by chlorpyrifos toxicity in Nile tilapia (Oreochromis niloticus). Animals. 10:473

    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 22:3023–3031

    CAS  Google Scholar 

  • Abdelkhalek NK, Eissa IA, Ahmed E, Kilany OE, El-Adl M, Dawood MA, Hassan AM, Abdel-Daim MM (2017) 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 

  • Abdel-Tawwab M, Adeshina I, Jenyo-Oni A, Ajani EK, Emikpe BO (2018) Growth, physiological, antioxidants, and immune response of African catfish, Clarias gariepinus (B.), to dietary clove basil, Ocimum gratissimum, leaf extract and its susceptibility to Listeria monocytogenes infection. Fish Shellfish Immunol 78:346–354

    CAS  Google Scholar 

  • Adel M, Yeganeh S, Dadar M, Sakai M, Dawood MAO (2016) Effects of dietary Spirulina platensis on growth performance, humoral and mucosal immune responses and disease resistance in juvenile great sturgeon (Huso huso Linnaeus, 1754). Fish Shellfish Immunol 56:436–444

    CAS  Google Scholar 

  • Aebi H (1984) [13] Catalase in vitro, Methods in enzymology. Elsevier, Amsterdam, pp 121–126

    Google Scholar 

  • Ahmed OM, Mahmoud AM, Abdel-Moneim A, Ashour MB (2012) Antidiabetic effects of hesperidin and naringin in type 2 diabetic rats. Diabetol Croat 41

  • Akinrotimi O, Gabriel U, Ariweriokuma S (2012) Haematotoxicity of cypermethrin to African catfish (Clarias gariepinus) under laboratory conditions. J Environ Eng Technol 1(2):13–19

    Google Scholar 

  • Amin KA, Hashem KS (2012) Deltamethrin-induced oxidative stress and biochemical changes in tissues and blood of catfish (Clarias gariepinus): antioxidant defense and role of alpha-tocopherol. BMC Vet Res 8:45

    CAS  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 

  • Amphan S, Unajak S, Printrakoon C, Areechon N (2019) Feeding-regimen of β-glucan to enhance innate immunity and disease resistance of Nile tilapia, Oreochromis niloticus Linn., against Aeromonas hydrophila and Flavobacterium columnare. Fish Shellfish Immunol 87:120–128

    CAS  Google Scholar 

  • Anjugam M, Vaseeharan B, Iswarya A, Gobi N, Divya M, Thangaraj MP, Elumalai P (2018) Effect of β-1, 3 glucan binding protein based zinc oxide nanoparticles supplemented diet on immune response and disease resistance in Oreochromis mossambicus against Aeromonas hydrophila. Fish Shellfish Immunol 76:247–259

    CAS  Google Scholar 

  • Ansari BA, Kumar K (1988) Cypermethrin toxicity: effect on the carbohydrate metabolism of the Indian catfish, Heteropneustes fossilis. Sci Total Environ 72:161–166

    CAS  Google Scholar 

  • AOAC, 1998. Association of Official Analytical Chemists. Official methods of analysis of official analytical chemists international, 16th ed. Washington, DC

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  Google Scholar 

  • Awad E, Awaad A (2017) Role of medicinal plants on growth performance and immune status in fish. Fish Shellfish Immunol 67:40–54

    CAS  Google Scholar 

  • Banaee M, Haghi BN, Ibrahim ATA (2014) Sub-lethal toxicity of chlorpyrifos on Common carp, Cyprinus carpio (Linnaeus, 1758): biochemical response. Int J Aquat Biol 1:281–288

    Google Scholar 

  • Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Elsevier Health Sciences, Amsterdam

    Google Scholar 

  • Bello O, Olaifa F, Emikpe BJ (2014) Haematological and blood biochemical changes in African catfish, Clarias gariepinus fed walnut (Tetracarpidium conophorum Mull Arg) leaf and onion (Allium cepa Linn) bulb supplemented diets. J Exp Agric Int 4:1593–1603

    Google Scholar 

  • Bermejo P, Piñero E, Villar ÁM (2008) Iron-chelating ability and antioxidant properties of phycocyanin isolated from a protean extract of Spirulina platensis. Food Chem 110:436–445

    CAS  Google Scholar 

  • Cagauan AG, Tayaban RH, Somga J, Bartolome RM (2004) Effect of aflatoxin-contaminated feeds in Nile tilapia (Oreochromis niloticus L.), Abstract of the 6th international symposium on tilapia in aquaculture (ISTA 6) section: health management and diseases Manila, Philippines, pp 16

  • Camargo MMP, Martinez CBR (2007) Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropical Ichthyol 5:327–336

    Google Scholar 

  • Cao S, Zhang P, Zou T, Fei S, Han D, Jin J, Liu H, Yang Y, Zhu X, Xie S (2018) Replacement of fishmeal by spirulina Arthrospira platensis affects growth, immune related-gene expression in gibel carp (Carassius auratus gibelio var. CAS III), and its challenge against Aeromonas hydrophila infection. Fish Shellfish Immunol 79:265–273

    CAS  Google Scholar 

  • Cao Y, Liu H, Qin N, Ren X, Zhu B, Xia X (2020) Impact of food additives on the composition and function of gut microbiota: a review. Trends Food Sci Technol 99:295–310

    CAS  Google Scholar 

  • Dawood MAO (2016) Effect of various feed additives on the performance of aquatic animals. Kagoshima University, Kagoshima

    Google Scholar 

  • Dawood MA, Koshio S, Ishikawa M, El-Sabagh M, Yokoyama S, Wang WL, Yukun Z, Olivier A (2017a) Physiological response, blood chemistry profile and mucus secretion of red sea bream (Pagrus major) fed diets supplemented with Lactobacillus rhamnosus under low salinity stress. Fish Physiol Biochem 43:179–192

    CAS  Google Scholar 

  • Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El Basuini MF, Hossain MS, Nhu TH, Moss AS, Dossou S, Wei H (2017b) Dietary supplementation of β-glucan improves growth performance, the innate immune response and stress resistance of red sea bream, Pagrus major. Aquac Nutr 23:148–159

    CAS  Google Scholar 

  • 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, Magouz FI, Salem MFI, Abdel-Daim HA (2019a) Modulation of digestive enzyme activity, blood health, oxidative responses and growth-related gene expression in GIFT by heat-killed Lactobacillus plantarum (L-137). Aquaculture. 505:127–136

    CAS  Google Scholar 

  • Dawood MAO, Zommara M, Eweedah NM, Helal AI (2019b) 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

  • Dawood MAO, Magouz FI, Salem MFI, Elbialy ZI, Abdel-Daim HA (2019c) Synergetic effects of Lactobacillus plantarum and beta-glucan on digestive enzyme activity, intestinal morphology, growth, fatty acid, and glucose-related gene expression of genetically improved farmed tilapia. Probiotics Antimicrob Protein. https://doi.org/10.1007/s12602-019-09552-7

  • Dawood MAO, Moustafa EM, Gewaily MS, Abdo SE, AbdEl-kader MF, SaadAllah MS, Hamouda AH (2019d) Ameliorative effects of Lactobacillus plantarum L-137 on Nile tilapia (Oreochromis niloticus) exposed to deltamethrin toxicity in rearing water. Aquat Toxicol. https://doi.org/10.1016/j.aquatox.2019.105377 105377

  • 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, AbdEl-kader MF, Moustafa EM, Gewaily MS, Abdo SE (2020b) Growth performance and hemato-immunological responses of Nile tilapia (Oreochromis niloticus) exposed to deltamethrin and fed immunobiotics. Environ Sci Pollut Res 27:11608–11617. https://doi.org/10.1007/s11356-020-07775-8

    Article  CAS  Google Scholar 

  • Dawood MAO, Abdo SE, Gewaily MS, Moustafa EM, SaadAllah MS, AbdEl-kader MF, Hamouda AH, Omar AA, Alwakeel RA (2020c) The influence of dietary β-glucan on immune, transcriptomic, inflammatory and histopathology disorders caused by deltamethrin toxicity in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 98:301–311

    CAS  Google Scholar 

  • dos Santos Voloski AP, de Figueiredo Soveral L, Dazzi CC, Sutili F, Frandoloso R, Kreutz LC (2019) β-Glucan improves wound healing in silver catfish (Rhamdia quelen). Fish Shellfish Immunol 93:575–579

    Google Scholar 

  • El Basuini MF, Teiba II, Zaki MAA, Alabssawy AN, El-Hais AM, Gabr AA, Dawood MAO, Zaineldin AI, Mzengereza K, Shadrack RS, Dossou S (2020) Assessing the effectiveness of CoQ10 dietary supplementation on growth performance, digestive enzymes, blood health, immune response, and oxidative-related genes expression of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 98:420–428

    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 

  • El-Murr AEI, El Hakim YA, Neamat-Allah ANF, Baeshen M, Ali HA (2019) Immune-protective, antioxidant and relative gene expression impacts of β-glucan against fipronil toxicity in Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol. https://doi.org/10.1016/j.fsi.2019.09.033

  • Engstad RE, Robertsen Br (1993) Recognition of yeast cell wall glucan by Atlantic salmon (Salmo salar L.) macrophages. Dev Comp Immunol 17:319–330

    CAS  Google Scholar 

  • Engstad RE, Robertsen B, Frivold E (1992) Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish Shellfish Immunol 2:287–297

    Google Scholar 

  • Feldman B, Zinkl J, Jain N (2000) Schalm’s veterinary hematology. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  • Fırat Ö, Cogun HY, Yüzereroğlu TA, Gök G, Fırat Ö, Kargin F, Kötemen Y (2011) A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 37:657–666

    Google Scholar 

  • Gabriel U, Obomanu F, Edori O (2009) Haematology, plasma enzymes and organ indices of Clarias gariepinus after intramuscular injection with aqueous leaves extracts of Lepidagathis alopecuroides. Afr J Biochem Res 3:312–316

    CAS  Google Scholar 

  • Hamed HS (2016) Ameliorative effects of Spirulina platensis on deltamethrin-induced biochemical alterations and oxidative stress in the African catfish; Clarias gariepinus. Open J Mar Sci 6:10

    Google Scholar 

  • Hamed M, Soliman HAM, Sayed AE-DH (2019) Ameliorative effect of Spirulina platensis against lead nitrate–induced cytotoxicity and genotoxicity in catfish Clarias gariepinus. Environ Sci Pollut Res 26:20610–20618

    CAS  Google Scholar 

  • Han L-K, Li D-X, Xiang L, Gong X-J, Kondo Y, Suzuki I, Okuda H (2006) Isolation of pancreatic lipase activity-inhibitory component of Spirulina platensis and it reduce postprandial triacylglycerolemia. Yakugaku Zasshi 126:43–49

    CAS  Google Scholar 

  • Holman B, Malau-Aduli A (2013) Spirulina as a livestock supplement and animal feed. J Anim Physiol Anim Nutr 97:615–623

    CAS  Google Scholar 

  • Ji L, Sun G, Li J, Wang Y, Du Y, Li X, Liu Y (2017) Effect of dietary β-glucan on growth, survival and regulation of immune processes in rainbow trout (Oncorhynchus mykiss) infected by Aeromonas salmonicida. Fish Shellfish Immunol 64:56–67

    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 

  • Kawahara E, Ueda T, Nomura S (1991) In vitro phagocytic activity of white-spotted char blood cells after injection with Aeromonas salmonicida extracellular products. Fish Pathol 26:213–214

    Google Scholar 

  • Khalil SR, Reda RM, Awad A (2017) Efficacy of Spirulina platensis diet supplements on disease resistance and immune-related gene expression in Cyprinus carpio L. exposed to herbicide atrazine. Fish Shellfish Immunol 67:119–128

    CAS  Google Scholar 

  • Kumari U, Srivastava N, Shelly A, Khatri P, N S, Singh DK, Mazumder S (2016) Inducible headkidney cytochrome P450 contributes to endosulfan immunotoxicity in walking catfish Clarias gariepinus. Aquat Toxicol 179:44–54

    CAS  Google Scholar 

  • Layam A, Reddy CLK (2006) Antidiabetic property of spirulina. Diabetol Croat 35:29–33

    Google Scholar 

  • Lei-Leston AC, Murphy AG, Maloy KJ (2017) Epithelial cell inflammasomes in intestinal immunity and inflammation. Front Immunol 8

  • Mohamed FA (2009) Histopathological studies on Tilapia zillii and Solea vulgaris from Lake Qarun, Egypt. World J Fish Mar Sci 1:29–39

    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. https://doi.org/10.1016/j.aquaculture.2019.734589 734589

  • Muralidharan L (2012) Haemato-Biochemical alterations induced by chronic exposure to fenthion in Cyprinus carpio. Trends Fish Res 1:19–25

    Google Scholar 

  • Nagaoka S, Shimizu K, Kaneko H, Shibayama F, Morikawa K, Kanamaru Y, Otsuka A, Hirahashi T, Kato T (2005) A novel protein C-phycocyanin plays a crucial role in the hypocholesterolemic action of Spirulina platensis concentrate in rats. J Nutr 135:2425–2430

    CAS  Google Scholar 

  • NRC (2011) National Research Council. Nutrient requirements of fish and shrimp. National Academies Press, Washington, D.C.

    Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    CAS  Google Scholar 

  • Oliveira RJ, Salles MJ, da Silva AF, Kanno TY, Lourenco AC, Leite Vda S, Matiazi HJ, Pesarini JR, Ribeiro LR, Mantovani MS (2013) In vivo evaluation of the antimutagenic and antigenotoxic effects of beta-glucan extracted from Saccharomyces cerevisiae in acute treatment with multiple doses. Genet Mol Biol 36:413–424

    CAS  Google Scholar 

  • Öner M, Atli G, Canli M (2008) Changes in serum biochemical parameters of freshwater fish Oreochromis niloticus following prolonged metal (Ag, Cd, Cr, Cu, Zn) exposures. Environ Toxicol Chem 27:360–366

    Google Scholar 

  • Ortega-Gutiérrez S, López-Vicente M, Lostalé F, Fuentes-Broto L, Martínez-Ballarín E, García JJ (2009) Protective effect of melatonin against mitomycin C-induced genotoxic damage in peripheral blood of rats. J Biomed Biotechnol 2009:6

    Google Scholar 

  • Oruç EÖ (2010) Oxidative stress, steroid hormone concentrations and acetylcholinesterase activity in Oreochromis niloticus exposed to chlorpyrifos. Pestic Biochem Physiol 96:160–166

    Google Scholar 

  • Osman A, Hamed M, Sayed A (2019) Protective role of Spirulina platensis against UVA-induced haemato-biochemical and cellular alterations in Clarias gariepinus. J Photochem Photobiol B Biol 191:59–64

    CAS  Google Scholar 

  • Ovando CA, Carvalho JC, Vinícius de Melo Pereira G, Jacques P, Soccol VT, Soccol CR (2018) Functional properties and health benefits of bioactive peptides derived from Spirulina: a review. Food Rev Int 34:34–51

    CAS  Google Scholar 

  • Owens C, Belcher R (1965) A colorimetric micro-method for the determination of glutathione. Biochem J 94:705

    CAS  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  Google Scholar 

  • Petit J, Wiegertjes GF (2016) Long-lived effects of administering β-glucans: Indications for trained immunity in fish. Dev Comp Immunol 64:93–102

    CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e45

    CAS  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 

  • Raji AA, Alaba PA, Yusuf H, Abu Bakar NH, Mohd Taufek N, Muin H, Alias Z, Milow P, Abdul Razak S (2018) Fishmeal replacement with Spirulina Platensis and Chlorella vulgaris in African catfish (Clarias gariepinus) diet: effect on antioxidant enzyme activities and haematological parameters. Res Vet Sci 119:67–75

    CAS  Google Scholar 

  • Rjeibi I, Ben Saad A, Hfaiedh N (2016) Oxidative damage and hepatotoxicity associated with deltamethrin in rats: the protective effects of Amaranthus spinosus seed extract. Biomed Pharmacother 84:853–860

    CAS  Google Scholar 

  • Romay C, Ledon N, Gonzalez R (1998) Further studies on anti-inflammatory activity of phycocyanin in some animal models of inflammation. Inflamm Res 47:334–338

    CAS  Google Scholar 

  • Romay C, Gonzalez R, Ledon N, Remirez D, Rimbau V (2003) C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4:207–216

    CAS  Google Scholar 

  • Rosas VT, Poersch LH, Romano LA, Tesser MB (2019) Feasibility of the use of Spirulina in aquaculture diets. Rev Aquac 11:1367–1378

    Google Scholar 

  • Saha S, Kaviraj A (2009) Effects of cypermethrin on some biochemical parameters and its amelioration through dietary supplementation of ascorbic acid in freshwater catfish Heteropneustes fossilis. Chemosphere. 74:1254–1259

    CAS  Google Scholar 

  • Sayed AE-DH, Authman MMN (2018) The protective role of Spirulina platensis to alleviate the Sodium dodecyl sulfate toxic effects in the catfish Clarias gariepinus (Burchell, 1822). Ecotoxicol Environ Saf 163:136–144

    CAS  Google Scholar 

  • Sayed AE-DH, El-Sayed YS, El-Far AH (2017) Hepatoprotective efficacy of Spirulina platensis against lead-induced oxidative stress and genotoxicity in catfish, Clarias gariepinus. Ecotoxicol Environ Saf 143:344–350

    CAS  Google Scholar 

  • Shalaby A (2005) The opposing effect of ascorbic acid (vitamin C) on ochratoxin toxicity in Nile tilapia, Oreochromis niloticus. 6th Intern, Symp. Tilapia in Aquac. Philipin, pp 150–157

  • Shekarabi SPH, Omidi AH, Dawood MAO, Adel M, Avazeh A, Heidari F (2019) Effect of black mulberry (Morus nigra) powder on growth performance, biochemical parameters, blood carotenoid concentration, and fillet color of rainbow trout. Ann Anim Sci. https://doi.org/10.2478/aoas-2019-0068

  • Soliman NF, Yacout DM (2016) Aquaculture in Egypt: status, constraints and potentials. Aquac Int 24:1201–1227

    Google Scholar 

  • Sridevi P, Chaitanya RK, Prathibha Y, Balakrishna SL, Dutta-Gupta A, Senthilkumaran B (2015) Early exposure of 17α-ethynylestradiol and diethylstilbestrol induces morphological changes and alters ovarian steroidogenic pathway enzyme gene expression in catfish, Clarias gariepinus. Environ Toxicol 30:439–451

    CAS  Google Scholar 

  • Sunanda M, Rao JCS, Neelima P, Rao KG, Simhachalam G (2016) Effects of chlorpyrifos (an organophosphate pesticide) in fish. Int J Pharm Sci Rev Res Vet Sci 39:299–305

    CAS  Google Scholar 

  • Trichet VV (2010) Nutrition and immunity: an update. Aquac Res 41:356–372

    CAS  Google Scholar 

  • Upasani CD, Balaraman R (2003) Protective effect of Spirulina on lead induced deleterious changes in the lipid peroxidation and endogenous antioxidants in rats. Phytother Res 17:330–334

    CAS  Google Scholar 

  • Ural MŞ (2013) Chlorpyrifos-induced changes in oxidant/antioxidant status and haematological parameters of Cyprinus carpio carpio: ameliorative effect of lycopene. Chemosphere. 90:2059–2064

    CAS  Google Scholar 

  • Van Doan H, Hoseinifar SH, Ringø E, Ángeles Esteban M, Dadar M, Dawood MA, Faggio C (2019) Host-associated probiotics: a key factor in sustainable aquaculture. Rev Fish Sci Aquac:1–27

  • Van Hai N (2015) The use of medicinal plants as immunostimulants in aquaculture: a review. Aquaculture. 446:88–96

    Google Scholar 

  • Yang J, Gong Y, Cai J, Zheng Y, Zhang Z (2020) Chlorpyrifos induces apoptosis and autophagy in common carp lymphocytes by influencing the TCR γ-dependent PI3K/AKT/JNK pathway. https://doi.org/10.1016/j.fsi.2020.02.039

  • 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 

  • Yousef MI, El-Demerdash F, Kamel K, Al-Salhen K (2003) Changes in some hematological and biochemical indices of rabbits induced by isoflavones and cypermethrin. Toxicology. 189:223–234

    CAS  Google Scholar 

  • Yu W, Wen G, Lin H, Yang Y, Huang X, Zhou C, Zhang Z, Duan Y, Huang Z, Li T (2018) Effects of dietary Spirulina platensis on growth performance, hematological and serum biochemical parameters, hepatic antioxidant status, immune responses and disease resistance of Coral trout Plectropomus leopardus (Lacepede, 1802). Fish & Shellfish Immunology. 74:649–655

    Google Scholar 

  • Zahran E, Risha E, Awadin W, Palić D (2018) Acute exposure to chlorpyrifos induces reversible changes in health parameters of Nile tilapia (Oreochromis niloticus). Aquat Toxicol 197:47–59

    CAS  Google Scholar 

  • Zaki MAA, Alabssawy AN, Nour AE-AM, El Basuini MF, Dawood MAO, Alkahtani S, Abdel-Daim MM (2020) The impact of stocking density and dietary carbon sources on the growth, oxidative status and stress markers of Nile tilapia (Oreochromis niloticus) reared under biofloc conditions. Aquac Rep 16:100282

    Google Scholar 

  • Zapata A, Diez B, Cejalvo T, Gutiérrez-de Frías C, Cortés A (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136

    CAS  Google Scholar 

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Authors and Affiliations

  1. Clinical Pathology Department, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh, Egypt

    Abd-Allah A. Mokhbatly, Doaa H. Assar, Emad W. Ghazy & Sally A. Rizk

  2. Fish Processing and Biotechnology Department, Faculty of Fisheries Sciences and Aquaculture, Kafrelsheikh University, Kafr El-Sheikh, Egypt

    Zizy Elbialy

  3. Fish Diseases Department, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh, Egypt

    Amira A. Omar

  4. Veterinary Research Division, National Research Centre, Giza, 12622, Egypt

    Alkhateib Y. Gaafar

  5. Department of Animal Production, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh, Egypt

    Mahmoud A. O. Dawood

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  7. Alkhateib Y. Gaafar
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  8. Mahmoud A. O. Dawood
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Corresponding authors

Correspondence to Doaa H. Assar or Mahmoud A. O. Dawood.

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The experimental procedure was approved by the “Faculty of Veterinary Medicine, Kafrelsheikh University, Egypt.”

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Responsible editor: Lotfi Aleya

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Mokhbatly, AA.A., Assar, D.H., Ghazy, E.W. et al. The protective role of spirulina and β-glucan in African catfish (Clarias gariepinus) against chronic toxicity of chlorpyrifos: hemato-biochemistry, histopathology, and oxidative stress traits. Environ Sci Pollut Res 27, 31636–31651 (2020). https://doi.org/10.1007/s11356-020-09333-8

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