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Original Article

Protective effect of ursodeoxycholic acid, resveratrol, and N-acetylcysteine on nonalcoholic fatty liver disease in rats

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Pages 1198-1208 | Received 16 Feb 2015, Accepted 05 Jun 2015, Published online: 01 Jul 2015

References

  • Adams LA, Sanderson S, Lindor KD, Angulo P. (2005). The histological course of nonalcoholic fatty liver disease, a longitudinal study of 103 patients with sequential liver biopsies. J Hepatol 42:132–8
  • Aires V, Delmas D. (2015). Common pathways in health benefit properties of RSV in cardiovascular diseases, cancers and degenerative pathologies. Curr Pharm Biotechnol 16:219–44
  • Al Maruf A, O'Brien P. (2014). Flutamide-induced cytotoxicity and oxidative stress in an in vitro rat hepatocyte system. Oxid Med Cell Longev 2014:398285
  • Alfawwaz RA, Alhamdan AA. (2006). The modulatory effect of N-acetyl cysteine supplementation on hepatic glutathione concentration and lipid peroxidation status in old rats fed a low-protein diet. Pak J Nutr 5:156–65
  • Amacher DE, Schomaker SJ, Aubrecht J. (2013). Development of blood biomarkers for drug-induced liver injury, an evaluation of their potential for risk assessment and diagnostics. Mol Diagn Ther 17:343–54
  • Anderson R, Prolla T. (2009). PGC-1α in aging and anti-aging interventions. Biochim Biophys Acta 1790:1059–66
  • Anglo P, Keach JC, Batts KP, Lindor KD. (1999). Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis. Hepatology 30:1356–62
  • Aykac M, Uysal M, Yalcin AS, et al. (1985). The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione peroxidase and glutathione transferase in rats. Toxicology 36:71–6
  • Bajaj S, Khan A. (2012). Antioxidants and diabetes. Ind J Endocrinol Metab 16:S267–71
  • Banchroft GD, Steven A. (1983). Theory and Practice of Histological Technique. 4th ed. Edinburgh: Churchill Livingstone Publications
  • Bartles H, Bohmer M, Heierli C. (1972). Serum creatinine determination without protein precipitation. Clin Chim Acta 37:193–7
  • Belonovskaia EB, Naruta EE, Lukivskaia OI, et al. (2013). Preventive administration of new UDCA derivatives in experimental alcoholic steatohepatitis. Eksp Klin Farmakol 76:25–9
  • Berlanga A, Guiu-Jurado E, Porras JA, Auguet T. (2014). Molecular pathways in non-alcoholic fatty liver disease. Clin Exp Gastroenterol 7:221–39
  • Bonavida B. (1991). Immunomodulatory effect of tumor necrosis factor. Biotherapy 3:127–33
  • Braga MF, Grace MG, Lenis J, et al. (2009). Efficacy and safety of ursodeoxycholic acid in primary, type IIa or IIb hypercholesterolemia, a multicenter, randomized, double-blind clinical trial. Atherosclerosis 203:479–82
  • Buckley NA, Whyte IM, O'Connell DL, Dawson AH. (1999). Oral or intravenous N-acetylcysteine, which is the treatment of choice for acetaminophen (paracetamol) poisoning? J Toxicol Clin Toxicol 37:759–67
  • Bucolo G, David H. (1973). Quantitative determination of serum tri-glycerides by the use of enzymes. Clin Chem 19:476–82
  • Bujanda L, Hijona E, Larzabal M, et al. (2008). Resveratrol inhibits nonalcoholic fatty liver disease in rats. BMC Gastroenterol 8:40–7
  • Buryova H, Chalupsky K, Zbodakova O, et al. (2013). Liver protective effect of ursodeoxycholic acid includes regulation of ADAM17 activity. BMC Gastroenterol 13:155–66
  • Carreras A, Zhang SX, Peris E, et al. (2015). Effect of resveratrol on visceral white adipose tissue inflammation and insulin sensitivity in a mouse model of sleep apnea. Int J Obes 39:418–23
  • Chan WK, Ida NH, Cheah PL, Goh KL. (2014). Progression of liver disease in non-alcoholic fatty liver disease. A prospective clinicopathological follow-up study. J Dig Dis 15:545–52
  • Chander V, Chopra K. (2006). Protective effect of nitric oxide pathway in resveratrol renal ischemia–reperfusion injury in rats. Arch Med Res 37:19–26
  • Chatterjee S, Ganini D, Tokar EJ, et al. (2013). Leptin is key to peroxynitrite-mediated oxidative stress and Kupffer cell activation in experimental non-alcoholic steatohepatitis. J Hepatol 58:778–84
  • Chen X, Lou G, Meng Z, Huang W. (2011). TGR5, a novel target for weight maintenance and glucose metabolism. Exp Diabetes Res 2011:853501
  • Chitturi S, Farrell GC, Hashimoto E, et al. (2007). Non-alcoholic fatty liver disease in the Asia-Pacific region, definitions and overview of proposed guidelines. J Gastroenterol Hepatol 22:778–87
  • Chitturi S, Farrell GC. (2001). Etiopathogenesis of nonalcoholic steatohepatitis. Semin Liver Dis 21:27–41
  • Chiu CJ, Taylor A. (2011). Dietary hyperglycemia, glycemic index and metabolic retinal diseases. Prog Retin Eye Res 30:18–53
  • Clark JM, Brancati FL, Diehl AM. (2003). The prevalence and etiology of elevated aminotransferase levels in the United States. Am J Gastroenterol 98:960–7
  • Costa ML, Lima-Júnior RC, Aragão KS, et al. (2014). Chemotherapy-associated steatohepatitis induced by irinotecan, a novel animal model. Cancer Chemother Pharmacol 74:711–20
  • Cu A, Ye Q, Sarria R, Nakamura S, et al. (2009). N-Acetylcysteine inhibits TNF-alpha, sTNFR, and TGF-beta1 release by alveolar macrophages in idiopathic pulmonary fibrosis in vitro. Sarcoidosis Vasc Diffuse Lung Dis 26:147–54
  • Czaja AJ. (2011). Cryptogenic chronic hepatitis and its changing guise in adults. Dig Dis Sci 56:3421–38
  • Das SK, Mukherjee S, Gupta G, et al. (2010). Protective effect of resveratrol and vitamin E against ethanol-induced oxidative damage in mice, biochemical and immunological basis. Ind J Biochem Biophys 47:32–7
  • Day CP, James OF. (1998). Steatohepatitis, a tale of two “hits”. Gastroenterology 114:842–5
  • De Souza V, Hadj-Aissa A, Dolomanova O, et al. (2014). Creatinine- versus cystatine C-based equations in assessing the renal function of candidates for liver transplantation with cirrhosis. Hepatology 59:1522–31
  • Delzenne NM, Hernaux NA, Taper HS. (1997). A new model of acute liver steatosis induced in rats by fasting followed by refeeding a high carbohydrate-fat free diet: Biochemical and morphological analysis. J Hepatol 26:880–5
  • Deng XQ, Chen LL, Li NX. (2007). The expression of SIRT1 in non-alcoholic fatty liver disease induced by high fat diet in rats. Liver Int 27:708–15
  • Diehl AM, Goodman Z, Ishak KG. (1988). Alcohol like liver disease in nonalcoholics, a clinical and histologic comparison with alcohol-induced liver injury. Gastroenterology 95:1056–62
  • Ding Y, Sun X, Chen Y, et al. (2015). Epigallocatechin gallate attenuated non-alcoholic steatohepatitis induced by methionine- and choline-deficient diet. Eur J Pharmacol. [Epub ahead of print]. doi: 10.1016/j.ejphar.2015.05.005
  • Dongiovanni P, Romeo S, Valenti L. (2014). Hepatocellular carcinoma in nonalcoholic fatty liver, role of environmental and genetic factors. World J Gastroenterol 20:12945–55
  • Doumas BT, Watson WA, Biggs HG. (1971). Albumin standards and the measurement of serum albumin with bromcresol green. Clin Chem Acta 31:87–96
  • Fawcett JK, Scott JE. (1960). A rapid and precise method for the determination of urea. J Clin Pathol 13:156–9
  • Friedewald WT, Levy RI, Donald S, Fredrickson DS. (1972). Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502
  • Georgieva NV. (2005). Oxidative stress as a factor of disrupted ecological oxidative balance in biological systems – A review. Bulg J Vet Med 8:1–11
  • Giby VG, Ajith TA. (2014). Role of adipokines and peroxisome proliferator-activated receptors in nonalcoholic fatty liver disease. World J Hepatol 6:570–9
  • Grove TH. (1979). Effect of reagent pH on determination of HDL-C by precipitation with Na–phosphotungstate–magnesium. Clin Chem 25:560–4
  • Habig WH, Pabst MJ, Jakoby WB. (1974). Glutathione-S-transferases; the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–9
  • Hardwick RN, Fisher CD, Canet MJ, et al. (2010). Diversity in antioxidant response enzymes in progressive stages of human nonalcoholic fatty liver disease. Drug Metab Dispos 38:2293–301
  • Hempfling W, Dilger K, Beuers U. (2003). Systematic review: Ursodeoxycholic acid – Adverse effects and drug interactions. Aliment Pharmacol Ther 18:963–72
  • Higashi T, Tateishi N, Naruse A, Sakamoto Y. (1977). A novel physiological role of liver glutathione as reservoir of l-cysteine. J Biochem 82:117–24
  • Huang HY, Korivi M, Yang HT, et al. (2014). Effect of Pleurotus tuber-regium polysaccharides supplementation on the progression of diabetes complications in obese-diabetic rats. Chin J Physiol 57:198–208
  • Jaeschke H. (2011). Reactive oxygen and mechanisms of inflammatory liver injury, present concepts. J Gastroenterol Hepatol 26:173–9
  • Janero DR. (1990). Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 9:515–40
  • Jha P, Knopf A, Koefeler H, et al. (2014). Role of adipose tissue in methionine–choline-deficient model of non-alcoholic steatohepatitis (NASH). Biochim Biophys Acta 1842:959–70
  • Kacew S, Festing MF. (1996). Role of rat strain in the differential sensitivity to pharmaceutical agents and naturally occurring substances. J Toxicol Environ Health 47:1–30
  • Kang H, Koppula S. (2015). Houttuynia cordata alleviates high-fat diet-induced non-alcoholic fatty liver in experimental rats. Pharm Biol 53:414–22
  • Khoshbaten M, Aliasgarzadeh A, Masnadi K, et al. (2010). N-acetylcysteine improves liver function in patients with non-alcoholic fatty liver disease. Hepat Mon 10:12–16
  • Kim KS, Oh HJ, Kim DJ, et al. (2013). The association between non-alcoholic fatty liver disease and carotid atherosclerosis in subjects with within-reference range alanine aminotransferase levels. Endocr J 60:1295–301
  • Kopeć A, Piątkowska E. (2013). Effect of resveratrol on selected biochemical parameters in rats fed high fructose diet. Acta Sci Pol Technol Aliment 12:395–402
  • Korou LM, Agrogiannis G, Pantopoulou A, et al. (2010). Comparative antilipidemic effect of N-acetylcysteine and sesame oil administration in diet-induced hypercholesterolemic mice. Lipids Health Dis 9:23–9
  • Kucera O, Cervinkova Z. (2014). Experimental models of non-alcoholic fatty liver disease in rats. World J Gastroenterol 20:8364–76
  • Kumar A, Singh V. (2010). Atherogenic dyslipidemia and diabetes mellitus, what's new in the management arena? Vasc Health Risk Manag 6:665–9
  • Latha P, Chaitanya D, Rukkumani R. (2010). Protective effect of Phyllanthus niruri on alcohol and heated sunflower oil induced hyperlipidemia in Wistar rats. Toxicol Mech Methods 20:498–503
  • Lee GS, Yan JS, Ng RK, et al. (2007). Polyunsaturated fat in the methionine–choline deficient diet influences hepatic inflammation but not hepatocellular injury. J Lipid Res 48:1885–96
  • Lodhi P, Tandan N, Singh N, Kumar D, Kumar M. (2014). Camellia sinensis (L.) Kuntze extract ameliorates chronic ethanol-induced hepatotoxicity in albino rats. Evid Based Complement Alternat Med 2014:787153
  • Lukivskaya O, Lis R, Egorov A, et al. (2004). The protective effect of ursodeoxycholic acid in alloxan-induced diabetes. Cell Biochem Funct 22:97–103
  • Maffei M, Halaas J, Ravussin E, et al. (1995). Leptin levels in human and rodent, measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1:1155–61
  • Mahmoud AA, Elshazly SM. (2014). Ursodeoxycholic acid ameliorates fructose-induced metabolic syndrome in rats. PLoS One 9:e106993
  • Maier-Salamon A, Böhmdorfer M, Riha J, et al. (2013). Interplay between metabolism and transport of resveratrol. Ann N Y Acad Sci 1290:98–106
  • Männistö VT, Simonen M, Soininen P, et al. (2014). Lipoprotein subclass metabolism in non-alcoholic steatohepatitis. J Lipid Res 55:2676–84
  • Marchesini G, Bugianesi E, Forlani G, et al. (2003). Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 37:917–23
  • Martius G, Alwahsh SM, Rave-Fränk M, et al. (2014). Hepatic fat accumulation and regulation of FAT/CD36, an effect of hepatic irradiation. Int J Clin Exp Pathol 7:5379–92
  • Mas N, Tasci I, Comert B, et al. (2008). Ursodeoxycholic acid treatment improves hepatocyte ultrastructure in rat liver fibrosis. World J Gastroenterol 14:1108–11
  • Meiattini F, Prencipe L, Bardelli F, et al. (1978). The 4 hydroxybenzoate/4-aminophenazone chromogenic system used in the enzymic determination of serum cholesterol. Clin Chem 24:2161–5
  • Mikolasevic I, Racki S, Bubic I, et al. (2013). Chronic kidney disease and nonalcoholic fatty liver disease proven by transient elastography. Kidney Blood Press Res 37:305–10
  • Movahed A, Nabipour I, Lieben Louis X, et al. (2013). Antihyperglycemic effects of short term resveratrol supplementation in type 2 diabetic patients. Evid Based Complement Alternat Med 2013:851267
  • Murata Y, Amao M, Hamuro J. (2003). Sequential conversion of the redox status of macrophages dictates the pathological progression of autoimmune diabetes. Eur J Immunol 33:1001–11
  • Nihei T, Miura Y, Yagasaki K. (2001). Inhibitory effect of resveratrol on proteinuria, hypoalbuminemia and hyperlipidemia in nephritic rats. Life Sci 68:2845–52
  • Ohkawa HN, Ohishi K, Yagi K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–8
  • Olas B, Nowak P, Kolodziejczyk J, et al. (2006). Protective effects of resveratrol against oxidative/nitrative modifications of plasma proteins and lipids exposed to peroxynitrite. J Nutr Biochem 17:96–102
  • Osawa Y, Hoshi M, Yasuda I, et al. (2013). Tumor necrosis factor-α promotes cholestasis-induced liver fibrosis in the mouse through tissue inhibitor of metalloproteinase-1 production in hepatic stellate cells. PLoS One 8:e65251
  • Ota T, Takamura T, Kurita S, et al. (2007). Insulin resistance accelerates a dietary rat model of nonalcoholic steatohepatitis. Gastroenterology 132:282–93
  • Pangeni R, Sharma S, Mustafa G, Ali J, Baboota S. (2014). Vitamin E loaded resveratrol nanoemulsion for brain targeting for the treatment of Parkinson's disease by reducing oxidative stress. Nanotechnology 25:485102
  • Parekh S, Anania FA. (2007). Abnormal lipid and glucose metabolism in obesity, implications for nonalcoholic fatty liver disease. Gastroenterology 132:2191–207
  • Pfluger PT, Herranz D, Velasco-Miguel S, et al. (2008). SIRT1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci USA 105:9793–8
  • Pinzone MR, Celesia BM, Di Rosa M, et al. (2012). Microbial translocation in chronic liver diseases. Int J Microbiol 2012:694629
  • Prasad K. (2012). Resveratrol, wine, and atherosclerosis. Int J Angiol 21:7–18
  • Pratt DS, Kaplan MM. (2000). Evaluation of abnormal liver enzyme results in asymptomatic patients. N Engl J Med 342:1266–71
  • Radcke S, Dillon JF, Murray AL. (2015). A systematic review of the prevalence of mildly abnormal liver function tests and associated health outcomes. Eur J Gastroenterol Hepatol 27:1–7
  • Reitman S, Frankel SA. (1957). Colorimetric method for determination of serum glutamic oxalo-acetic and glutamic pyruvate transaminases. Am J Clin Pathol 28:56–63
  • Ronis MJ, Butura A, Sampey BP, et al. (2005). Effects of N-acetylcysteine on ethanol-induced hepatotoxicity in rats fed via total enteral nutrition. Free Radic Biol Med 39:619–30
  • Rushworth GF, Megson IL. (2014). Existing and potential therapeutic uses for N-acetylcysteine: The need for conversion to intracellular glutathione for antioxidant benefits. Pharmacol Ther 141:150–9
  • Sahin S, Alatas O. (2013). The protective effects of N-acetylcysteine against acute hepatotoxicity. Indian J Gastroenterol 32:311–15
  • Samuhasaneeto S, Thong-Ngam D, Kulaputana O, et al. (2007). Effects of N-acetylcysteine on oxidative stress in rats with non-alcoholic steatohepatitis. J Med Assoc Thai 90:788–97
  • Seifi B, Kadkhodaee M, Delavari F, et al. (2012). Pretreatment with pentoxifylline and N-acetylcysteine in liver ischemia reperfusion-induced renal injury. Ren Fail 34:610–15
  • Siddiqui MS, Fuchs M, Idowu M, et al. (2015). Severity of nonalcoholic fatty liver disease and progression to cirrhosis associate with atherogenic lipoprotein profile. Clin Gastroenterol Hepatol 13:1000–8
  • Silva AM, Oliveira MI, Sette L, et al. (2014). Resveratrol as a natural anti-tumor necrosis factor-α molecule, implications to dendritic cells and their crosstalk with mesenchymal stromal cells. PLoS One 9:e91406
  • Singh D, Das CJ, Baruah MP. (2013). Imaging of non alcoholic fatty liver disease: A road less travelled. Indian J Endocrinol Metab 17:990–5
  • Skelly MM, James PD, Ryder SD. (2001). Findings on liver biopsy to investigate abnormal liver function tests in the absence of diagnostic serology. J Hepatol 35:195–9
  • Sokolovic D, Nikolic J, Kocic G, et al. (2013). The effect of ursodeoxycholic acid on oxidative stress level and DNAse activity in rat liver after bile duct ligation. Drug Chem Toxicol 36:141–8
  • Sugimoto K, Takei Y. (2011). Clinicopathological features of non-alcoholic fatty liver disease. Hepatol Res 41:911–20
  • Sukemori S, Kurosawa A, Ikeda S, Kurihara Y. (2006). Investigation on the growth of coprophagy-prevented rats with supplemented vitamin B12. J Anim Physiol Anim Nutr 90:402–6
  • Suwalsky M, Villena F, Gallardo MJ. (2015). In vitro protective effects of resveratrol against oxidative damage in human erythrocytes. Biochim Biophys Acta 1848:76–82
  • Szkudelska K, Nogowski L, Szkudelski T. (2009). The inhibitory effect of resveratrol on leptin secretion from rat adipocytes. Eur J Clin Invest 39:899–905
  • Tamaki N, Cristina Orihuela-Campos R, Inagaki Y, et al. (2014). Resveratrol improves oxidative stress and prevents the progression of periodontitis via the activation of the Sirt1/AMPK and the Nrf2/antioxidant defense pathways in a rat periodontitis model. Free Radic Biol Med 75:222–9
  • Tarantino G. (2014). Nutrition: A promising route for prevention and management of obesity-related nonalcoholic fatty liver disease. Horm Mol Biol Clin Investig 20:39–41
  • Trinder P. (1969). Determination of glucose in body fluids. Ann Clin Biochem 6:24–7
  • Tsochatzis EA, Papatheodoridis GV, Archimandritis AJ. (2009). Adipokines in nonalcoholic steatohepatitis, from pathogenesis to implications in diagnosis and therapy. Mediators Inflamm 2009:831670
  • Tsochatzis EA, Feudjo M, Rigamonti C, et al. (2013). Ursodeoxycholic acid improves bilirubin but not albumin in primary biliary cirrhosis, further evidence for nonefficacy. BioMed Res Int 2013:139763
  • Veena J, Muragundla A, Sidgiddi S, Subramaniam S. (2014). Non-alcoholic fatty liver disease: Need for a balanced nutritional source. Br J Nutr 112:1858–72
  • Vidyashankar S, Sandeep Varma R, Patki PS. (2013). Quercetin ameliorate insulin resistance and up-regulates cellular antioxidants during oleic acid induced hepatic steatosis in HepG2 cells. Toxicol In Vitro 27:945–53
  • Vital Durand D, Lega JC, Fassier T, et al. (2013). Unexplained, subclinical chronically elevated transaminases. Rev Med Interne 34:472–8
  • Wang J, Zhu H, Liu X, Liu Z. (2014). N-Acetylcysteine protects against cadmium-induced oxidative stress in rat hepatocytes. J Vet Sci 15:485–93
  • Wang JQ, Zou YH, Huang C, et al. (2012). Protective effects of tiopronin against high fat diet-induced non-alcoholic steatohepatitis in rats. Acta Pharmacol Sin 33:791–7
  • Weiβ J, Rau M, Geier A. (2014). Non-alcoholic fatty liver disease, epidemiology, clinical course, investigation, and treatment. Dtsch Arztebl Int 111:447–52
  • Xia N, Förstermann U, Li H. (2014). Resveratrol and endothelial nitric oxide. Molecules 19:16102–21
  • Xie HC, Han HP, Chen Z, He JP. (2013). A study on the effect of resveratrol on lipid metabolism in hyperlipidemic mice. Afr J Tradit Complement Altern Med 11:209–12
  • Yang Q, Xie RJ, Geng XX, et al. (2005). Effect of Danshao Huaxian capsule on expression of matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 in fibrotic liver of rats. World J Gastroenterol 11:4953–6
  • Zhang Y, Edwards PA. (2008). FXR signaling in metabolic disease. FEBS Lett 582:10–18
  • Zheng J, Chen L, Zhang H, et al. (2012). Resveratrol improves insulin resistance of catch-up growth by increasing mitochondrial complexes and antioxidant function in skeletal muscle. Metabolism 61:954–6
  • Zhu X, Liu Q, Wang M, et al. (2011). Activation of Sirt1 by resveratrol inhibits TNF-α induced inflammation in fibroblasts. PLoS One 6:e27081

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