Effects of Silymarin on Growth Performance, Internal Organs and Some Blood Parameters in Japanese Quail Subjected to Oxidative Stress Induced by Carbon Tetrachloride

Document Type: Original Paper


1 Department of Animal and Poultry Physiology, Faculty of Animal Science, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

2 Department of Animal and Poultry Nutrition, Faculty of Animal Science, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

3 Department of Biology, Faculty of Science, Golestan University, Gorgan, Iran

4 Department of Horticulture, College of Agriculture, Shiraz University, Shiraz, Iran


The effects of Silymarin on growth performance, internal organs, and some blood parameters were investigated in Japanese quail that were subjected to oxidative stress induced by carbon tetrachloride (CCl4). An experiment was conducted as a completely randomized design in a factorial arrangement (2 × 2) with four replicates of 30 birds each. Factors included two levels of Silymarin (0 and 1 mL/kg of body weight (BW)) and two levels of CCl4 (0 and 1 mL/kg of BW). Results showed that Silymarin did not affect productive parameters, whilst CCl4 significantly (P < 0.05) reduced feed intake and body weight gain. Silymarin did not affect the relative weights of breast, gizzard and heart, whereas CCl4 reduced relative weights of breast and heart. Both Silymarin and CCl4 administration resulted in higher pancreases relative weight. Birds treated with Silymarin had greater blood serum concentration of total protein and lower concentrations of glucose, triglyceride and total cholesterol (P < 0.05). In contrast, birds that received CCl4 showed decreased total protein and increased glucose concentrations of blood serum (P < 0.05). The interaction effect between Silymarin and CCL4 showed that Silymarin ameliorated the adverse effects of CCl4 on blood albumin. Treatment of CCl4 increased blood concentration of alkaline phosphatase compared with Silymarin (P < 0.05). This study showed that Silymarin may be a useful antioxidant source to ameliorate the adverse effects of oxidative stressors in Japanese quail.


Abascal K & Yarnell E. 2003a. The many faces of silybum marianum (Milk Thistle): Part 1 - Treating cancer and hyperlipidemia and restoring kidney function. Alternative and Complementary Therapies, 9: 170-175. DOI: 10.1089/107628003322256878

Abascal K & Yarnell E. 2003b. The Many Faces of Silybum marianum (Milk Thistle): Part 2 - Clinical uses, safety, and types of preparations. Alternative and Complementary Therapies, 9: 251-256. DOI: 10.1089/107628003322490698

Applegate TJ, Schatzmayr G, Pricket K, Troche C & Jiang Z. 2009. Effect of aflatoxin culture on intestinal function and nutrient loss in laying hens. Poultry Science, 88: 1235-1241. DOI: 10.3382/ps.2008-00494

Bahraminejad S, Asenstorfer RE, Riley IT, & Schultz CJ. 2008. Analysis of the antimicrobial activity of flavonoids and saponins isolated from the shoots of oats (Avena sativa L.). Journal              of Phytopathology, 156: 1-7. DOI: 10.1111/j.1439-0434.2007.01309.x

Banaee M, Sureda A, Mirvaghefi, AR & Rafei GR. 2011. Effects of long-term silymarin oral supplementation on the blood biochemical profile of rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry, 37:885-896. DOI: 10.1007/s10695-011-9486-z

Boll M, Lutz WD, Weber E & Stampfl A. 2001. Pathogenesis of carbon tetrachloride-induced hepathocyte injury bioactivation of CCL4 by cytochrome P450 and effects on lipid homeostasis. Zeitschrift für Naturforschung C, 56: 111-121. DOI: 10.1515/znc-2001-1-218 

Campbell TW & Coles EH. 1986. Avian clinical pathology. In: Coles EH. (Eds). Veterinary Clinical Pathology. Saunders Company. Philadelfia. Pages. 203-209.

Chang CC, Yang MH, Wen HM & Chern JC. 2002.  Estimation of total flavonoid content in proplis by two complementary colorimetric methods. Journal of Food and Drug Analysis, 10: 178-182.

 Chlopčiková S, Psotová J, Miketová P & Šimánek V. 2004. Chemoprotective effect of plant phenolics against anthracycline-induced toxicity on rat cardiomyocytes. Part I. Silymarin and its flavonolignans. Phytotherapy Research, 18: 107-110. DOI: 10.1002/ptr.1415

Dalloul RA, Lillehoj HS, Lee JS, Lee SH & Chung KS. 2006. Immunopotentiating effect of a Fomitella fraxinea-derived lectin on chicken immunity and resistance to coccidiosis. Poultry Science, 85: 446–451. DOI: 10.1093/ps/85.3.446

Devarshi P, Kanase A, Kanase R, Mane S, Patil S & Varute AT. 1986. Effect of mandur bhasma on lipolytic activities of liver, kidney and adipose tissue of albino rat during CCL4 induced hepatic injury. Journal of Biosciences, 10: 227-234. DOI: 10.1007/BF02703480

Ding TM, Tian SJ, Zhang ZX, Gu DZ, Chen YF, Shi YH & Sun ZP. 2001. Determination of active component in Silymarin by PR-LC and LC/MS. Journal of Pharmaceutical and Biomedical Analysis, 26: 155-161. DOI: 10.1016/S0731-7085(01)00364-8

Ebrahimi R, Mahmmadabadi T, Sari M, Sallari S, Zamiri MJ & Beygi Nasiri MT. 2013. Effect of silymarin on lead-induced oxidative stress in broilers. Iranian Journal of Animal Science Research, 5: 302-312.

Fani Makki O, Omidi A, Afzali N, Sarir H, Frouzanmehr M & Shibak A. 2014. Efficacy of Silybum Marianum Seeds in Ameliorating the Toxic Effects of Aflatoxin B1 in Broilers. Iranian Journal of Toxicology, 8: 977-982.

Gadgoli C & Mishra SH. 1999. Antihepatotoxic activity of p-methoxy benzoic acid from Capparis spinosa. Journal of Ethnopharmacology, 66: 187–192. DOI: 10.1016/S0378-8741(98)00229-3

Guo FC, Savelkoul HFJ, Kwakkel RP, Williams BA & Verstegen MWA. 2000. Immunoactive, medicinal properties of mushroom and herb polysaccharides and their potential use in chicken diets. World's Poultry Science Journal, 59: 427- 440. DOI: 10.1079/WPS20030026

Ha KT, Yoon SJ, Choi DY, Kim DW, Kim JK & Kim CH. 2005. Protective effect of lycium chinense fruit on carbon tetrachloride-induced hepatotoxicity.  Journal of Ethnopharmacology, 96: 529-535. DOI: 10.1016/j.jep.2004.09.054

Harborne AJ. 1998. Phytochemical methods, a guide to modern techniques of plant analysis. Springer Nether;ands, Pages, 270.

Hasani-Ranjbar S, Nayebi N, Moradi L, Mehri A, Larijani B & Abdollahi M. 2010. The efficacy and safety of herbal medicines used in the treatment of hyperlipidemia; a systematic review. Current Pharmaceutical Design, 16: 2935-2947. DOI: 10.2174/138161210793176464

Hetrog MGL & Hollmann PCH. 1998. Potential health effects of the dietary flavonol quercetin: review. European Journal of Clinical Nutrition. 50: 63-71.

Huseini HF, Larijani B, Heshmat R, Fakhrzadeh H, Radjabipour B, Toliat T & Raza M. 2006. The efficacy of Silybum marianum (L.) Gaertn (silymarin) in the treatment of type II diabetes: a randomized, double‐blind, placebo‐ controlled, clinical trial.  Phytotherapy Research, 20: 1036-1039. DOI: 10.1002/ptr.1988

Janbaz KH & Gilani AH. 2002. Menthol prevents liver damage induced by paracetamol and CCl4. Pakistan Journal of Biological Science, 5: 1101-1103.

Jothi G, Bhuvaneswari S & Radhika J. 2012. Antihepatotoxic activity of Samanea saman (Jacq.) Merr. against carbon tetrachloride induced hepatic injury in rats. Research Journal of Pharmacy and Technology, 5: 393-397.

Katiyar SK. 2004. Silymarin and skin cancer prevention: Anti-inflammatory, antioxidant and immunomodulatory effects (Review). International Journal of Oncology, 18: 101-112.

Khan TH & Sultana S. 2009. Antioxidant and hepatoprotective potential of Aegle
Correa. against CCl4-induced oxidative stress and early tumor events.
Journal of Enzyme Inhibition and Medicinal Chemistry, 24: 320-327 DOI: 10.1080/14756360802167754

Khodadust MR, Samadi F, Ganji F, Jafari Ahangari Y & Asadi GH. 2015. Effects of peppermint (Mentha piperita L.) alcoholic extract on carbon tetrachloride-induced hepatotoxicity in broiler chickens under heat stress condition. Poultry Science Journal, 3: 1-16. DOI: 10.22069/psj.2015.2323

Khorramshahi M, Samadi F & Ganji F. 2014. The effects of Cynara scolymus L. on carbon tetracholoride induced liver toxicity in Japanese quail. International Journal of AgriScience 4: 362-369.

Knekt P, Kumpulainen J, Järvinen R, Rissanen H, Heliövaara M, Reunanen A,  Hakulinen T & Aromaa A. 2002. Flavonoid intake and risk of chronic diseases.  American Journal of Clinical Nutrition, 76: 560–568.

Kodai S, Takemura S, Minamiyama Y, Hai S, Yamamoto S, Kubo S, Yoshida Y, Niki E, Okada S, Hirohashi K & Suehiro S. 2007. S-allyl cysteine prevents CCl4-induced acute liver injury in rats. Free radical Research, 41: 489-497. DOI: 10.1080/10715760601118361

Kris-Etherton PM, Lefevre M, Beecher GR, Gross MD, Keen CL & Etherton TD. 2004. Bioactive compounds in nutrition and health-research methodologies for establishing biological function: the antioxidant and anti-inflammatory effects of flavonoids on atherosclerosis. Annual Reviews of Nutrition, 24: 511–538. DOI: 10.1146/annurev.nutr. 23.011702.073237

Kumar SS, Kumar BR & Mohan GK. 2009. Hepatoprotective effect of Trichosanthes cucumerina Var cucumerina L. on carbon tetrachloride induced liver damage in rats. Journal of Ethnopharmacology, 123: 347-350. DOI: 10.1016/j.jep.2009.02.023

Lin H, Decuypere E & Buyse J. 2006. Acute heat stress induces oxidative stress in broiler chickens. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 144: 11–17. DOI: 10.1016/j.cbpa.2006.01.032

Manibusan MK, Odin M & Eastmond DA. 2007. Postulated carbon tetrachloride mode of action: A review, Journal of Environmental Science and Health, Part C: Environmental Carcinogenesis and Ecotoxicology Reviews, 25: 185-209. DOI: 10.1080/10590500701569398

Mehri M, Sabaghi V & Bagherzadeh-Kasmani F. 2015. Mentha piperita (peppermint) in growing Japanese quails’ diet: Serum biochemistry, meat quality, humoral immunity. Animal Feed Science and Technology, 206: 57-66. DOI: 10.1016/j.anifeedsci.2015.05.022

Muriel P & Mourelle M.  1990. Prevention by silymarin of membrane alterations in acute CCL4 liver damage. Journal of Applied Toxicology, 10: 275-279. DOI: 10.1002/jat.2550100408

Neshat Gharamaleki M & Mohajeri D. 2014. Study the protective effects of Black Cumin (Nigella sativa linn.) ethanolic extract against Rifampin-induced hepatotoxicity in rats. Qom University of Medical Sciences Journal, 8: 73-84.

NRC (National Research Council). 1994. Nutrient Requirements of Poultry. 9th Rev. Ed. National Academy Press. Washington, DC. 176 Pages.

Panovska TK, Kulevanova S, Gjorgoski I, Bogdanova M & Petrushevska G. 2007. Hepatoprotective effect of the ethyl acetate extract of Teucrium polium L. against carbontetrachloride-induced hepatic injury in rats. Acta Pharmaceutica, 57: 241–248. DOI: 10.2478/v10007-007-0020-x

Parmar MY, Shah PA, Thakkar VT, Al-Rejaie SS & Gandhi TR. 2012. Hepatoprotective effect of amomum subulatum roxb seeds on carbon tetrachloride-induced liver damage in rats. Journal of Pharamcy, 2: 38-43.

Ponte PIP and Rosado CMC. 2008. Pasture intake improves the performance and meat sensory attributes of free-range in broilers. Poultry Science, 87: 71-79. DOI: 10.3382/ps. 2007-00147

Redman CM. 1969. Biosynthesis of serum proteins and ferritin by free and attached ribosomes of rat liver. Journal of Biological Chemistry, 244: 4308-4315.

SAS Institute. 2003. SAS/STAT® 9. User’s Guide. SAS Institute Inc. Cary, NC. USA.

Schaffer S, Eckert GP, Müller WE, Llorach R, Rivera D, Grande S, Galli C & Visioli F. 2004. Hypochlorous acid scavenging properties of local mediterranean plant foods. Lipids, 39: 1239-1247. DOI: 10.1007/s11745-004-1353-9

Sharma A, Sharma MK & Kumar M. 2006. Protective effect of Mentha piperita against arsenic-induced toxicity in liver of swiss albino mice. Basic and Clinical Pharmacology and Toxicology, 100: 249–257. DOI: 10.1111/j.1742-7843.2006.00030.x

Soni B & Nishant P. 2008. Ameliorative action of cyanobacterial phycoerythrin on CCl4-induced toxicity in rats. Toxicology 248: 59-65. DOI: 10.1016/j.tox.2008.03.008

Sonkusale P, Bhandarker AG, Kurkare NV, Ravikanth K, Maini S & Sood D. 2011. Hepatoprotective activity of superliv liquid and repchol in CCl4 induced FLKS syndrome in broilers. International Journal of Poultry Science, 10: 49-55.

Soto C, Mena R, Luna J, Cerbón M, Larrieta E, Vital P, Uria E, Sánchez M, Recoba R, Barrón H, Favari L & Lara A. 2004. Silymarin induces recovery of pancreatic function after alloxan damage in rats. Life Sciences, 75: 2167-2180. DOI: 10.1016/j.lfs.2004.04.019

Soto C, Recoba R, Barrón H, Alvarez C & Favari L. 2003. Silymarin increases antioxidant enzymes in alloxan-induced diabetes in rat pancreas.  Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 136: 205-212. DOI: 10.1016/S1532-0456(03)00214-X

Tsukamoto H, Matsuoka M & French SW. 1990. Experimental models of hepatic fibrosis: a review. Seminars in Liver Disease, 10: 56-65.

Tumova L, Tuma J, Megusar K & Dolezal M. 2010. Substituted pyrazinecarboxamides as abiotic elicitors of flavolignan production in Silybum marianum (L.) gaertn cultures in vitro. Molecules, 15: 331-340. DOI: 10.3390/molecules15010331

Wang CH, Zhang T, Cul X, Li SH, Zhao X & Zhang X. 2013. Hepatoprotective effects of a Chinese herbal formula, Longyin Decoction, on carbon-tetrachloride-induced liver injury in chickens. Evidence-based Complementary and Alternative Medicine, 39: 27-43. DOI: 10.1155/2013/392743