Abstract
This study was carried out to evaluate the effects of dietary supplementation of aqueous extract of Withania somnifera (W. somnifera) against cadmium chloride–induced toxicity in the Nile tilapia, Oreochromis niloticus. Five experimental groups were designed: group (I) was free from cadmium chloride and W. somnifera and served as a control, group (II) was exposed to 1.775 mg L−1 of cadmium chloride only (which is equivalent to 1/4 96-h LC50), while groups (III), (IV), and (V) were exposed to 1.775 mg cadmium chloride L−1 with co-supplementation of dietary W. somnifera in doses of 1.0, 2.0, and 3.0 mL kg−1 body weight (bwt), respectively. The experiment lasted for 4 weeks. In the second and fourth weeks of the experiment, the following indicators were evaluated: hematological (hemogram and blood protein profile), biochemical (activities of serum liver enzymes, namely alanine transaminase (ALT) and aspartate transaminase (AST)), immunological (immunoglobulin M (IgM), serum lysozyme), and tissue antioxidant changes (malondialdehyde (MDA) levels and activities of catalase (CAT) and superoxide dismutase (SOD)). Additionally, gene expressions of glutathione-S-transferase (GST) in the liver were assessed. At the end of the experiment, all fish in all groups were experimentally challenged with Aeromonas hydrophila and the relative protection survival (RPS) was demonstrated. The results revealed that groups exposed to cadmium chloride toxicity and co-supplemented with dietary aqueous extract of W. somnifera at high doses showed significant ameliorative effects in hemogram parameters, total protein, globulin, IgM, and lysozyme against cadmium chloride–induced toxicity compared to the control group and the group exposed to a sublethal dose of cadmium chloride without co-suplemntation of W. somnifera. The results showed also that groups supplemented orally with W. somnifera at high doses have higher antioxidant activities of CAT and SOD and reduction of MDA formation. Levels of gene expressions of GST in the liver were higher in W. somnifera extract-supplemented groups more than those in the group exposed to cadmium chloride–induced toxicity without W. somnifera supplementation. In addition, the results revealed improved RPS with the dietary supply of W. somnifera extract in high doses. In conclusion, this study showed that the dietary supplementation of W. somnifera extract to diets of O. niloticus could be suggested as an effective way to overcome cadmium chloride–induced toxicity because it improves blood parameters and antioxidants, and it can be used as an immunostimulant against the invading bacterial pathogens.
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Abdel-Daim MM, Eissa IA, Abdeen A, Abdel-Latif HM, Ismail M, Dawood MA, Hassan AM (2019) Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ Toxicol Pharmacol 69:44–50
Abdelkhalek NKM, 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
Adedapo AA, Abatan MO, Olorunsogo OO (2004) Toxic effects of some plants in the genus Euphorbiaceae on haematological and biochemical parameters of rats. Vet Arh 74(1):53–62
Aebi H (1984) Catalase in Vitro. Methods Enzymol 105:121–126
Akanji MA, Yakubu MT, Kazeem MI (2013) Hypolipidemic and toxicological potential of aqueous extract of Rauwolfia vomitoria Afzel root in Wistar rats. J Med Sci 13:253–260
Akbarsha MA, Vijendrakumar S, Kadalmani B, Girija R, Faridha A (2000) Curative property of Withania somnifera Dunal root in the context of carbendazim-induced histopathological changes in the liver and kidney of rat. Phytomedicine 7(6):499–507
Alam N, Hossain M, Abdul Mottalib M, Sulaiman SA, Gan SH, Khalil MDI (2012) Methanolic extracts of Withania somnifera leaves, fruits and roots possess antioxidant properties and antibacterial activities. BMC Complement Altern Med 12:175
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
APHA. 2005. Standard methods for the examination of water and wastewater, 21st Edn., Washington DC.
Bagenstose LM, Mentink־Kane MM, Brittingham A, Mosser DM, Monesties M (2001) Mercury enhances susceptibility to murine Leishmaniasis. Parasite Immunol 23(12):633–640
Bancroft J, Stevens A, Turnor D (1996) Theory and practice of histological techniques, 4th edn. Chemical Living Stom, New York, London, Tokyo
Bariweni MW, Yibala OI, Ozolua RI (2018) Toxicological studies on the aqueous leaf extract of Pavetta crassipes (K. Schum) in rodents. J Pharm Pharmacogn Res 6(1):1–16
Bii C, Korir KR, Rugutt J, Mutai C (2010) The potential use of Prunus africana for the control, treatment and management of common fungal and bacterial infections. J Med Plant Res 4(11):995–998
Bindu MP, kuzhiveli, B.T. (2006) Effective of cadmium on total protein of liver Oreochromis mossambicus. Res Rev 5:27–36
Brautbar N, Williams IJ (2002) Industrial solvents and liver toxicity: risk assessment, risk factors and mechanisms. Int J Hyg Environ Health 25(6):479–491
Bujjamma B, Padmavathi P (2018) Effect of cadmium on Haematological changes in a freshwater catfish, Heteropneustes fossilis. Int J Zool Stud 3(1):132–141
Carvalho CDS, Bernusso VA, de Araújo HSH, Espíndola ELG, Fernandes MN (2012). Biomarker responses as indication of contaminant effects in Oreochromis niloticus. 89(1):60–69
Centre d’Analyse des Politiques Economiques et Sociales (CAPES). 2006. Etat des lieux des savoirs locaux au Burkina Faso. Inventaire des bonnes pratiques et propositions pour leur contribution au développement. Ouagadougou. 448 p.
Chen J, Xu Y, Han Q, Yao Y, Xing H, Teng X (2019) Immunosuppression, oxidative stress, and glycometabolism disorder caused by cadmium in common carp (Cyprinus carpio L.): Application of transcriptome analysis in risk assessment of environmental contaminant cadmium. J Hazard Mater 366:386–394
Chen D, Ning F, Zhang J, Tang Y, Teng X (2020a) NF-κB pathway took part in the development of apoptosis mediated by miR-15a and oxidative stress via mitochondrial pathway in ammonia-treated chicken splenic lymphocytes. Sci Total Environ 729:139017
Chen J, Zhanga S, Tonga J, Teng Z, Zhang Z, Li S, Tengad Z (2020b) Whole transcriptome-based miRNA-mRNA network analysis revealed the mechanism of inflammation-immunosuppressive damage caused by cadmium in common carp spleens. Sci Total Environ 717:137081
Chen J, Chen D, Li J, Liu Y, Gu X, Teng X (2021) Cadmium-induced oxidative stress and immunosuppression mediated mitochondrial apoptosis via JNK-FoxO3a-PUMA pathway in Common Carp (Cyprinus carpio L.) Gills. Aquat Toxicol 233:105775
Coulombe JJ, Favreau L (1963) A New simple semimicro method for colourimetric determination of urea. Clin Chem 9:102–108
Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582
Désert Margins Program. 2004. Les savoirs traditionnels de préservation des terres et de la diversité biologique dans les sites de recherches du programme d’action sur les zones en marge du désert (DMP). Rapport 07/ CNRST, Ouagadougou, 61 p.
Doumas BT, Watson W, Biggs HG (1971) albumin standards and the measurement of serum albumin with Bromcresol Green. Clin Chim Acta 31:87–96
Drubkin D (1964) Spectrophotometric methods XIV. The crystographic and optical properties of the haemoglobin of man in comparison with those of other species. J.Biol.Chem 164:703–723
Duncan DB (1955) Multiple ranges and multiple F test. Biometrics 11:1–42
Environmental Protection Agency. 1984. Updated mutagenicity and carcinogenicity assessment of cadmium. (Addendum to the health assessment for cadmium May 1981, EPA-600/8-81-023).
Fırat O, Cogun HY, Yüzereroğlu TA, Gök G, Fırat O, Kargin F, Kötemen YA (2011) 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
Gagnon J, Chen XL, Forand-Boulerice M, Leblanc C, Raman C, Ramanathan S, Ilangumaran S (2010) Increased antigen responsiveness of naive CD8 T cells exposed to IL-7 and IL- 21 is associated with decreased CD5 expression. Immunol Cell Biol 88:451–460
Ganong WF (2001). Review of medical physiology, Twentieth ed. Lange Medical Books, McGraw Hill Co., New York. Guide for the Care and Use of Laboratory Animals, eighth ed., 2011. The National Academies Press
Guiyan W, Qi-xing Z, Xiao-min H, Tao H, Feng L (2007) Single and joint toxicity of perchloroethylene and cadmium on Ctenopharyngodon idellus. Ying Yong Sheng Tai Xue Bao 18(5):1120–1124
Hamilton MA, Russo RC, Thurston RV (1977) Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719
Han Q, Tong J, Sun Q, Teng X, Zhang H, Teng X (2020) The involvement of miR-6615-5p/Smad7 axis and immune imbalance in ammonia-caused inflammatory injury via NF-κB pathway in broiler kidneys. Poult Sci 99(11):5378–5388
Harikrishnan R, Balasundaram C, Jawahar S, Heo MS (2012) Immunomodulatory effect of Withania somnifera supplementation diet in the giant freshwater prawn Macrobrachium rosenbergii (de Man) against Aeromonas hydrophila. Fish Shellfish Immunol 32(1):94–100
Hawak PB, Oscar BL, Summerson W (1965) Hawk’s physiological chemistry, 14th edn. J., and A. Churchill Ltd, London
Hemdan NVA, Lehmann I, Wichmann G, Lehmann J, Emmrich F, Sack U (2007) Immunomodulation of mercuric chloride in vitro: application of different cell activation pathways. Clin Exp Immunol 148(2):325–337
Hilmy AM, Shabana MB, Daabees AY (1985) Effects of cadmium toxicity upon the in vivo and in vitro activity of proteins and five enzymes in blood serum and tissue homogenates of Mugil cephalus. Comp Biochem Physiol C Comp Pharmacol Toxicol 81(1):145–153
ICRAF (2009) Agroforestry Tree Database. A tree species reference and selection guide. ICRAF, Nairobi
Ighodaro OM, Akinloyem OA (2017) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54(4):287–293
Iwama, G., Nakanishi, T. 1987. The fish immune system, organism, pathogen and environment. Academic Press, San Diego, London, Boston, Schultz, L.A, Methods in clinical chemistry The C.V Mosby Co. St. Louis, 1987, pp. 742-746.
Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Jiao X, Yang K, Yang A, Teng X (2017) Alleviation of lead-induced oxidative stress and immune damage by selenium in chicken bursa of Fabricius. Environ Sci Pollut Res 24(8):7555–7564
Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283(2–3):65–87
Kalay M, Canli M (2000) Elimination of essential (Cu, Zn) and non-essential (Cd, Pb.) metals from tissues of a freshwater fish Tilapia zilli. Turk J Zool 24:429–436
Kalay M, Erdem C (2003) Effect of cadmium accumulation on total protein levels in Tilapia nilotica. Turk J Vet Anim Sci 27(6):1367–1374
Kaoud HA, Mekawy MM (2011) Bioremediation the toxic effect of Mercury-exposure in Nile tilapia (Oreochromis niloticus) by using Lemna gibba L. J Am Sci 7(3):336–343
Kaur K, Rani G, Widodo N, Nagpal A, Taira K, Kaul SC, Wadhwa R (2004) Evaluation of the antiproliferative and antioxidative activities of leaf extract from in vivo and in vitro raised Ashwagandha. Food Chem Toxicol 42:2015–2020
Khadiga GA, Sherifa SH, Hama MI, Ramadan AS (2002) Impaired function in Nile tilapia Oreochromis niloticus from polluted waters. Acta Hydrochim Hydrobiol 29:278–288
Khadre SEM (1988) The effect of experimentally induced inflammation on the blood pattern and haemopoietic organs of the teleost, Clarias lazera. Bull Inst Oceanogr Fish 14:191–203
Klinck JS, Ng TYT, Wood CM (2009) Cadmium accumulation and in vitro analysis of calcium and cadmium transport functions in the gastro-intestinal tract of trout following chronic dietary cadmium and calcium feeding. Comp Biochem Physiol C Toxicol Pharmacol 150(3):349–360
Laltlanmawia C, Saha RK, Saha H, Biswas P (2019) Ameliorating effects of dietary mixture of Withania somnifera root extract and vitamin C in Labeo rohita against low pH and waterborne iron stresses. Fish Shellfish Immunol 88:170–178
Larsen K (1972) Creatinine assay in the presence of protein with LKB 8600 reaction rate analyser. Clin Chim Acta 38:475–476
Lawreuce DA, Mitchell D, Rudofsky U (1983) Heavy metal modulation of lymphocytes and macrophage activity. In: Proceeding of the 13th Annual Conference on Environmental Toxicology. AFAMRL-TR-82-101. National Technical Information Service, Springfield, VA, pp 63–79
Lee CF, Han CK, Tsau JL (2004) In vitro inhibitory activity of natural honey from aromatic and medicinal plants on antibiotic resistant strains of bacteria. Int J Agric Biol 6:289–293
Lequin RM (2005) Enzyme immunoassay (EIA)/enzyme-linked immunosorbent assay (ELISA). Clin Chem 51(12):2415–2418
Lide D (1992) CRC Handbook of Chemistry and Physics. CRC Press, Boca Raton, FL
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Lucky Z (1977) Methods for the diagnosis of fish diseases. Ameruno Publishing Co, PVT, Ltd, New Delhi, Bomby, New York
Lum G, Leal-Khouri S (1989) Significance of low serum urea nitrogen concentrations. J Clin Chem 35(4):639–640
Miao Z, Zhang K, Bao R, Li J (2021) Th1/Th2 imbalance and heat shock protein mediated inflammatory damage triggered by manganese via activating NF-κB pathway in chicken nervous system in vivo and in vitro. Environ Sci Pollut Res 28:44361–44373
Mihara M, Uchiyama M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278
Mishra LC, Singh BB, Dagenais S (2000) Scientific basis for the therapeutic use of Withania somnifera. Ashwagandha. Altern Med Rev 5(4):334–346
Nishikimi M, Roa NA, Yogi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854
Nwani CD, Lakra WS, Nagpure NS, Kumar R, Kushwaha B, Srivastava SK (2010) Toxicity of the herbicide atrazine: effects on lipid peroxidation and activities of antioxidant enzymes in the freshwater fish Channa Punctatus (Bloch). Int J Environ Res Public Health 7:3298–3312
Obaiah J, Usha AR (2012) Protective role of trace elements against cadmium induced alteration in the second oxidative stress enzyme in liver and kidney of fresh water teleost, Oreochromis mossambicus (Tilapia). Int J Pharm Pharm Sci 4(15):303–310
Omer SA, El-Obeid MA, Fouad D, Daghestani M, Al Olayan EM, Elamin MH, Virk P, El-Mahasna A (2012) Cadmium bioaccumulation and toxicity in Tilapia Fish (Oreochromis niloticus). J Anim Vet Adv 11(10):1601–1606
Pearce EL, Poffenberger MC, Chang CH, Jones RG (2013) Fueling immunity: insights into metabolism and lymphocyte function. Science 342(6155):1242454
Pellegrini M, Calzascia T, Toe JG, Preston SP, Lin AE, Paterson, SP, Lin AE, Elford AR, Shahinian A, Lang, PA, Lang KS, Morre M, Assouline B, Lahl K, Sparwasser T, Tedder TF, Paik JH, DePinho RA, Basta S, Ohashi PS, Mak TW (2011) IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell. 144: 601–613
Prusty AK, Kohli MPS, Sahu NP, Pal AK, Saharan N, Mohapatra S, Gupta SK (2011) Effect of Short term exposure of Fenvalerate on biochemical and haematological responses in Labeo rohita (Hamilton) Fingerlings. Pestic Biochem Physiol 100:124–129
Puerto M, Gutierrez-Praena D, Prieto AI, Pichardo S, Jos A, Miguel-Carrasco JL, Vazquez CM, Camean A (2011) Subchronic effects of cyanobacterial cells on the transcription of antioxidant enzyme genes in tilapia (Oreochromis sp.). Ecotoxicology 20:479–490
Rajesh S, Shraddha N, Vikas S, Gousia C (2015) A comparative anticancer activity of Plumbago zeylanica collected from northern and southern parts of india. World J Pharm Res 4990(4):1145–1151
Rangsayatorn N, Kruatrachue M, Pokethitiyook P, Upatham ES, Lanza GR, Singhakaew S (2004) Ultrastructural changes in various organs of the fish Puntius gonionotus fed cadmium-enriched cyanobacteria. Environ Toxicol 19(6):585–593
Rao YV, Das BK, Jyotymayee P, Chakraborli R (2006) Effect of Achyranthes Aspera on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. Fish Shellfish Immunol 20(3):263–273
Rashed MN (2001) Cadmium and lead levels in fish (Tilapia niloticus) tissues as biological indicator for lake water pollution. Environ Monit Assess 68:75–89
Reitman S, Frankel S (1957) A colourimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol 28:56–63
Ruangroupan L, Kiato T, Yoshida T (1986) Protective efficacy of Aeromonas hydrophila vaccines in Nile tilapia. Vet Immunol Immunopathol 12(1-4):345–350
Sadek MFA (2020) The effect of some dietary medicinal herbal extracts on growth performance and economic efficiency of Nile Tilapia. JAPFP 9(1):47–54
Schalm OW (1986) Veterinary hematology, 4th edn. Lea and Febiger, Philadelphia
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative ct method. Nat Protoc 3:1101–1108
Sevcikova M, Modra H, Slaninova A, Svobodova Z (2011) Metals as a cause of oxidative stress in fish: a review. Vet Med 56(11):537–546
Sharma A, Deo AD, Riteshkumar ST, Chanu TI, Das A (2010) Effect of Withania somnifera (L. Dunal) root as a feed additive on immunological parameters and disease resistance to Aeromonas hydrophila in Labeo rohita (Hamilton) fingerlings. Fish Shellfish Immunol 29(3):508–512
Shenker BJ, Berthold P, Rooney C, Vitale L, Debolt K, Shapiro IM (1993) Immunototic effect of mercuric compound of human lymphocytes and monocytes. III Alteration in B- cell function and viability. Immunopharmacol Immunototicol 15(1):87–112
Simsek N, Karadeniz A, Kalkan Y, Keles ON (2009) Spirulina platensis feeding inhibited the ammonia and levco penta induced lead and cadmium in rats. J Hazard Mater 164:1304–1039
Snedecor OW, Cochran WO Statistical methods. Iowa University Press, Ames, Iowa. Sparks T., 2000. Statistics in ecotoxicology. John Wiley and Sons, Ltd., West Sussex, England, 1982. Pp 320
Sobha K, Poornima A, Harini P, Veeraiah K (2007) A study on biochemical changes in the fresh water fish, Catla catla (Hamilton) exposed to the heavy metal toxicant cadmium chloride. Kathmandu University J Sci Eng Technol 3(2):1–11
Sprague JB (1971) Measurement of pollutant toxicity to fish. III. Sublethal effects and safe concentrations. Water Res 3:793–821
Stacey NH, Kappus H (1982) Cellular toxicity and lipid peroxidation in response to mercury. Toxicol Appl Pharmacol 63(1):29–35
Stoskopf M (1993) Fish medicine. WB Saunders Company, Philadelphia, London, Toronto, Montreal, Sydney, Tokyo pp. 113-131&149-159
Uddin SA, Siddque MAM, Romkey SS, Shelton W (2017) Antibacterial function of herbal extracts on growth, survival and immunoprotection in the black tiger shrimp Penaeus monodon. Fish Shellfish Immunol 65:52–58
Velez D, Montoro R (1998) Arsenic speciation in manufactured seafood products: a review. J Food Prot 61(9):1240–1245
Verma P, Nath A (2015) Modulatory role of withenia somnifera root extract mixed pelleted feed on pesticide induced hepatic anomalies’ in fresh water catfish clarias batrachus (linn.). J Pharm Pharm Sci 6(10):4243–4251
Vinodhini R, Narayanan M (2008) Bioaccumulation of heavy metals in organs of freshwater fish Cyprinus carpio. Int J Environ Sci Technol 5(2):179–182
Waalkes M (2000) Cadmium carcinogenesis in review. J Inorg Biochem 79:241–244
Weir DM (1983) Immunology: an outline for students of medicine and biology, 5th edn. Churchil Livingstone, London. Melbourne, New York, pp 15–16
Welman M (2011) South African National Biodiversity Institute, South Africa. NATIONAL HERBARIUM, PRETORIA Available: www.plantzafrica.com
WHO (1992) Environmental Health Criteria, No. 134, Environmental aspects. WHO, Geneva
Worth RG, Esper RM, Warra NS, Kindzelskii AL, Rosenspire AL, Todd RF, Petty HR (2001) Mercury inhibition of neutrophil activity: evidence of aberrant cellular signaling and incoherent cellular metabolism. Scand J Immunol 53(1):49–55
Yilmaz M, Gul A, Erbasli K (2004) Acute toxicity of Alpha Cypermethrin to guppy (Poecilia reticulata, Pallas, 1859). Chemosphere 56:381–385
Zahran E, El-Gawad EAA, Risha E (2018) Dietary Withania sominefera root confers protective and immunotherapeutic effects against Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 80:641–650
Zhang Y, Liu Q, Yin L, Li S (2020) Cadmium exposure induces pyroptosis of lymphocytes in carp pronephros and spleens by activating NLRP3. Ecotoxicol Environ Saf 202:110903
Acknowledgments
All authors are thankful for Dr. Salamah El Darer, a taxonomist in the Department of Plant Botany, Faculty of Science, Alexandria University, Egypt, for his kind help during the taxonomic identification and authentication of W. somnifera used in the study.
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- Design of the study: R.H Khalil, N.M. El-Sabbagh, H.A. Ghetas.
- Data Collection: N.M. El-Sabbagh, M.M. Khallaf, M.S. Shakweer, M.M. Attalah, H.A. Ghetas.
- Statistical analysis: M.M. Atallah, M.S. Shakweer.
- Data analysis and interpretation of results: N.M. El-Sabbagh, H.A. Ghetas, M.M. Kallaf, M.S. Shakweer, R.H. Khalil.
- Drafting the manuscript: N.M. El-Sabbagh, R.H. Khalil.
- Revision of the manuscript: N.M. El-Sabbagh.
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All applicable international, national, and/or institutional guidelines for the care and use of fish were followed by the authors. Nile tilapia fish (Oreochromis niloticus) were obtained from earthen ponds of a private fish farm, Edku, El-Behera, Egypt. No human participants, human data, or human tissue were used in this study.
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El-Sabbagh, N.M., Khalil, R.H., Khallaf, M.M. et al. Pharmacological and ameliorative effects of Withania somnifera against cadmium chloride–induced oxidative stress and immune suppression in Nile tilapia, Oreochromis niloticus. Environ Sci Pollut Res 29, 6777–6792 (2022). https://doi.org/10.1007/s11356-021-15630-7
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DOI: https://doi.org/10.1007/s11356-021-15630-7