The protective effects of fish oil and artichoke on hepatocellular carcinoma in rats

European Review for Medical and Pharmacological Sciences

Volumn 15, Issue 12, 2011, Pages 1429-1444

  Metwally, N S ^a   Kholeif, T E ^b   Ghanem, K Z ^a   Farrag, A R H ^a   Ammar, Naglaa M ^a   Abdel Hamid, A H Z ^a  

^a NATIONAL RESEARCH CENTRE   (Egypt)

^b AIN SHAMS UNIVERSITY   (Egypt)

Author keywords

Artichoke; Diethylnitrosamine; Fish oil; Hepatocellular carcinoma

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ALPHA FETOPROTEIN; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; DIETHYLNITROSAMINE; FERRITIN; FISH OIL; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; LIVER PROTECTIVE AGENT; MALONALDEHYDE; NITRIC OXIDE; VASCULOTROPIN; XANTHINE OXIDASE; PLANT EXTRACT;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICHOKE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; CELL SHAPE; CHROMATIN; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; FEMALE; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; HISTOPATHOLOGY; LIVER CELL; LIVER CELL CARCINOMA; LIVER PROTECTION; LIVER WEIGHT; NONHUMAN; NUCLEOLUS; PLANT LEAF; RAT; REVIEW; SUPPLEMENTATION; ANIMAL; ARTICLE; CHEMISTRY; DOSE RESPONSE; LIVER TUMOR; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CYNARA SCOLYMUS; DIETHYLNITROSAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FISH OILS; LIVER NEOPLASMS, EXPERIMENTAL; PLANT EXTRACTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84857028309     PISSN: 11283602     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. RUDDON RW. Characteristic of human cancer in cancer biology. Ruddon, RW. Ed. Oxford, U K, 1995.
2. FERY RJ, RUTH L. Liver cancer. In: The Gale of encyclopedia of cancer, a guide to cancer and its treatments, volume (2). Edited by Thackery, E., 2003.
3. EL-SERAG HB, RUDOLPH KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007; 132: 2557-2576. (Pubitemid 46890874)
4. EL-ZAYADI AR, BADRAN HM, BARAKAT EMF, ATTIA MED, SHAWKY S, MOHAMED MK, SELIM O, SAEID A. Hepato-cellular carcinoma in Egypt: a single center study over a decade. World J Gastroenterol 2005; 11: 5193-5198. (Pubitemid 41410338)
5. AKTAY G, DELIORMAN D, ERGUN E, ERGUN F, YESILADA E, CEVIK C. Hepatoprotective effects of Turkish folk remedies on experimental liver injury. J Ethnopharmacol 2000; 73: 121-129.
6. STORLIEN LH, HIGGINS JA, THOMAS TC, LEN H, STOR-LIEN JA, HIGGINS TC, THOMAS M A, BROWN H Q, WANG X F, HUANG PL. Diet composition and insulin action in animal models. Br J Nutr 2000; 83: S85-S90. (Pubitemid 30319087)
7. BOUGNOUX P. n-3 polyunsaturated fatty acids and cancer. Curr Opin Clin Nutr Metab Care 1999; 2: 121-126. (Pubitemid 129627808)
8. CALVIELLO G, PALOZZA P, PICCIONI E, MAGGIANO N, FRATTUCCI A, FRANCESCHELLI P, BARTOLI GM. Dietary supplementation with eicosapentaenoic and do-cosahexaenoic acid inhibits growth of Morris he-patocarcinoma 3924A in rats: effects on proliferation and apoptosis. Int J Cancer 1998; 75: 699-705. (Pubitemid 28145816)
9. ROSE DP, COHEN LA. Effects of dietary menhaden oil and retinyl acetate on the growth of DU 145 human prostatic adenocarcinoma cells trans planted into athymic nude mice. Carcinogenesis 1988; 9: 603-605.
10. RAHMAN KM, SUGIE S, OKAMOTO K, WATANABE T, TANA-KA T, MORI H. Modulation effects of diets high in n-3 and n-6 fatty acids in initiation and postinitiation stages of diethylnitrosamine-induced hepatocar-cinogenesis in rats. Jpn J Cancer Res 1999; 90: 31-39. (Pubitemid 29084308)
11. HAN S, SUN X, RITZENTHALER JD, ROMAN J. Fish oil inhibits human lung carcinoma cell growth by suppressing integrin-linked kinase. Mol Cancer Res 2009; 7:1 08-117.
12. CHAVARRO JE, STAMPFER MJ, HALL MN, SESSO HD, MA J. A 22-y prospective study of fish intake in relation to prostate cancer incidence and mortality. Am J Clin Nutr 2008; 88: 1297-303.
13. ZHU X F, ZHANG HX, LO R. Antifungal activity of Cy-nara scolymus L. extracts. Fitoterapia 2005; 76: 108-111. (Pubitemid 40139012)
14. GEBHARDT R. Anticholestatic activity of flavonoids from artichoke (Cynara scolymus L.) and of their metabolites. Med Sci Monit 2001; 7: 316-320.
15. GEBHARDT R. Inhibition of cholesterol biosynthesis in HepG2 cells by artichoke extracts is reinforced by glucosidase pretreatment. Phytother Res 2002; 16: 368-372. (Pubitemid 34704631)
16. BROWN JE, RICE-EVANS CA. Luteolin-rich artichoke extract protects low-density lipoprotein from oxidation in vitro. Free Radical Res 1998; 29: 247-255. (Pubitemid 28499598)
17. MICCADEI S, VENERA DD, CARDINALI A, ROMANO F, DU-RAZZO A, FODDAI MS, FRAIOLI R, MOBARHAN S, MAIANI G. Antioxidative and apoptotic properties of polyphenolic extracts from edible part of artichoke (Cynara scolymus L.) on cultured rat hepatocytes and on human hepatoma cells. J Nutr Cancer 2008; 60: 276-283. (Pubitemid 351451282)
18. GUNSTONE FD, HARWOOD JL, PADLEY FB. The lipid Hand book, 2nd ed. Chapman and Hall, 722, London, 1994.
19. GHANEM K, RAMADAN M, FARRAG AR, GHANEM H, FAROUK A. Egyptian artichoke volatile compounds protect against lead-induced hepatic and renal toxicity in male rats. Pol J Food Nutr Sci 2009; 59: 175-181.
20. REEVES PG, ROSSOW KL, LINDLAUF J. Development and testing of the Ain-93 purified diets for rodents: results on growth, kidney calcification and bone mineralization in rats and mice. J Nutr 1993; 123: 1923-1931. (Pubitemid 23342489)
21. BARBISAN L F, MIYAMOTO M, SCOLASTICI C, SALVADORI DMF, RIBEIRO LR, EIRA A F, DE CAMARGO JLV. Influence of aqueous extract of Agaricus blazei on rat liver toxicity induced by different doses of di-ethylnitrosamine. J Ethnopharmacol 2002; 83: 25-32. (Pubitemid 36164724)
22. CHEN HW, KO JJ, LII, CK, OU CC, SHEEN, LY. Corn oil enhances gamma-glutamyl transpeptidase-posi-tive foci development in the presence of phenobarbital during hepatocarcinogenesis in rats. Nutr Cancer 1997; 28: 252-257.
23. FRIED R, FRIED LW. Xanthine oxidase (xanthine de-hydrogenase). In: "Methods of enzymatic analysis" 2nd ed. Vol. 2, Bergmeyer H U, ed; pp. 222-226 Verlag Chemie, Weinheim, Academic press. London, 1974.
24. MOSHAGE H, KOK B, HUIZENGA JR, JANSEN PL. Nitrite and nitrate determination in plasma: a critical evaluation. Clin Chem 1995; 41: 892-896.
25. BEUTLER E, DURON O, KELLY MB. Improved method for determination of blood glutathione. J Lab Clin Med 1963; 61: 882-888.
26. HABIG WH, PABST MJ, JAKOBY WB. Glutathione S-transferases. The first enzymatic step in mercap-turic acid formation. J Biol Chem 1974; 249: 7130-7139.
27. BUEGE JA, AUST SD. Microsomal lipid peroxidation. Method Enzymol 1978; 52: 302-310.
28. KIM K J, LI B, HOUCK K, WINER J, FERRARA N. The vascular endothelial growth factor proteins: identification of biologically monoclonal antibodies. Growth Factors 1992; 7: 53-64.
29. LI D, MALLORY T, SATOMURA S. AFP: a new generation of tumor marker for hepatocellular carcinoma. Clin Chem Acta 2001; 313: 15-19. (Pubitemid 33016686)
30. STEIENE-MARTIN EA, LOTSPEICH-STEININGER CA, KOEPKE JA. Clinical hematology: principles, procedures, correlations. 2nd ed. Lippincott-Raven. Philadelphia, 1997.
31. YOUNG DS. Effects of drugs on clinical laboratory tests. 4 th Editition. AACC press; 1995.
32. PERSIJN J P, VANDER SLIK, W. A new method for the determination of gamma-glutamyltransferase in serum. J Clin Chem Clin Biochem 1976; 14: 421-427.
33. DEMETRIOU JA, DREWES DA, GIN JB. Enzymes: In: Clinical chemistry, principles and technics 2nd. Henry RJ, Cannon DC, Winkelman JW. Eds. Harper and Row Hagerstown MD, 1974.
34. YOUNG DS. Effects of drugs on clinical laboratory tests. 3 rd ed. AACC Press,1997.
35. WEBSTER D. A study of the interaction of bromocre-sol green with isolated serum globulin fractions. Clin Chim Acta 1974; 53: 109-115.
36. CANNON DC, HENRY RJ, WINKELMAN JW. Proteins: In clinical chemistry, principles and techniques 2nd. Harper and Row Hagerstown MD; 1974.
37. DRURY RAB, WALLINGTON EA. Carleton's Histological Technique, 5th ed. Oxford University Press, Oxford, UK, 1980.
38. GRANADO-SERRANO A, MARTIN M, BRAVO L, GOYA L, RAMOS S. A diet rich in cocoa attenuates N-ni-trosodiethylamine-induced liver injury in rats. Food Chem Toxicol 2009; 47: 2499-2506.
39. SREEPRIYA M, BALI G. Chemopreventive effects of embelin and curcumin against N-nitrosodiethy-lamine/phenobarbital-induced hepatocarcino-genesis in Wistar rats. Fitoterapia 2005; 76: 549-555. (Pubitemid 41749743)
40. SIVARAMAKRISHNAN V, SHILPA PNM, KUMAR VRP, DE-VARAJ SN. Attenuation of N-nitrosodiethylamine-in-duced hepatocellular carcinoma by a novel flavonol-Morin. Chem Biol Interact 2008; 171: 79-88. (Pubitemid 350191846)
41. STRIPE F, RAVAIOLI M, BATTELLI MG, MUSIANI S, GRAZI GL. Xanthine oxidoreductase activity in human liver disease. Am Coll Gastroenterol 2002; 97: 2079-2085.
42. SADIK NAH, EL-MARAGHY SA, ISMAIL MF. Diethylni-trosamine-induced hepatocarcino-genesis in rats: possible chemoprevention by blueberries. African J Bioch Res 2008; 2: 081-087.
43. YAMANOI A, NAGASUE N, KOHNO H, KIMOTO T, NAKA-MURA T. Clinical and enzymatic investigation of induction of oxygen free radicals by ischemia and reperfusion in human hepatocellular carcinoma and adjacent liver. HPB Surg 1995; 8: 93-199.
44. SAUGSTAD OD. Role of xanthine oxidase and its inhibitors in hypoxia: Reoxygenation injury. Pediatrics 1996; 98: 103-107. (Pubitemid 26226981)
45. RAKOV AR, BOKARIEV IN, REZVAN VV. Telomerase: perspectives of diagnosis and treatment in Oncology. Russ Med Inform 1999; 1: 34-41.
46. WINK DA, VODOVOTZ Y, LAVAL J, LAVAL F, DEWHIRST MY, MITCHELL JB. The multifaceted roles of nitric oxide in cancer. Cancerogenesis 1998; 19: 711-721. (Pubitemid 28376759)
47. JOZKOWICZ A, COOKE J, GUVARA I, HUK I, FUNOVICS P, PACHINGER O, WEIDINGER F, DULAK J. Genetic augmentation of nitric oxide synthase increases the vascular generation of VEGF. Cardiovasc Res 2001; 51: 773-783. (Pubitemid 32800719)
48. RAMANTHAN M, GILADI A, LEIBOVICH J. Regulation of vascular endothelial growth factor gene expression in murine macrophages by nitric oxide and hypoxia. Exp Biol Med 2003; 228: 697-705. (Pubitemid 37163260)
49. BOULOUMIE A, VALERIE BSK, BUSSE R. Vascular en-dothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells. Cardio-vasc Res 1999; 41: 773-780. (Pubitemid 29130642)
50. CZUCZEJKO J, ZACHARA BA, STAUBACH-TOPCZEWSKA E, HALOTA W, KEDZIORA J. Selenium, glutathione and glutathione peroxidases in blood of patients with chronic liver diseases. Acta Biochem Pol 2003; 50: 1147-1154. (Pubitemid 38608842)
51. ANDRE M, FELLEY-BOSCO E. Heme oxygenase-1-in-duction by endogenous nitric oxide: influence of intracellular glutathione. FEBS Lett 2003; 546: 223-227. (Pubitemid 36782415)
52. PRADEEP K, MOHEN CVR, GOBIANAND K, KARTHIKEYAN S. Silymarin modulates the oxidant-antioxidant imbalance during diethylnitrosamine induced oxida-tive stress in rats. Eur J Pharmacol 2007; 560: 110-116. (Pubitemid 46341309)
53. RAMAKRISHNAN G, RAGHAVENDRAN HRB, VINODHKUMAR R, DEVAKI T. Suppression of N-nitrosodiethylamine induced hepatocarcinogenesis by silymarin in rats. Chem-Biol Interact 2006; 161: 104-114. (Pubitemid 43776629)
54. JEYABAL PVS, SYED MB, VENKATARAMAN M, SAMBAND-HAM JK, SAKTHISEKARAN D. Apigenin inhibits oxida-tive stress-induced macromolecular damage in N-nitrosodiethylamine induced hepatocellular car-cinogenesis in Wistar albino rats. Mol Carcinogen 2005; 44: 11-20. (Pubitemid 41216403)
55. KLAUNIG JE, KAMENDULIS LM. The role of oxidative stress in carcinogenesis. Ann Rev Pharmacol Toxicol 2004; 44: 239-267. (Pubitemid 38263841)
56. GUTTERIDGE JMC. Lipid peroxidation and antioxi-dants as biomarkers of tissue damage.Clin Chem 1995; 41: 1819-1828.
57. YOSHIJI H, KURIYAMA S, YOSHII J, IKENAKA Y, NOGUCHI R, HICKLIN DJ, HUBER J, NAKATANI T, TSUJINOUE H, YANASE K, IMAZU H, FUKUI H. Synergistic effect of basic fi-broblast growth factor and vascular endothelial growth factor in murine hepatocellular carcinoma. Hepatology 2002; 35: 834-842. (Pubitemid 34258377)
58. MITSUHASHI N, SHIMIZU H, OHTSUKA M, WAKABAYASHI, Y, ITO H, KIMURA F, YOSHIDOME H, KATO A, NUKUI Y, MIYAZAKI M. Angiopoietins and Tie-2 expression in angiogenesis and proliferation of human hepato-cellular carcinoma. Hepatology 2003; 37: 1105-1113. (Pubitemid 36538687)
59. TORIMURA T, SATA M, UENO T, KIN M, TSUJI R, SUZAKU K, HASHIMOTO O, SUGAWARA H, TANIKAWA K. Increased expression of vascular endothelial growth factor is associated with tumor progression in hepatocellular carcinoma. Hum Pathol 1998; 29: 986-991. (Pubitemid 28422048)
60. WILLS PJ, SURESH V, ARUN M, ASHA V V. Antiangio-genic effect of Lygodium flexuosum against N-Ni-trosodiethylamine-induced hepatotoxicity in rats. Chem-Biol Interact 2006; 164: 25-38. (Pubitemid 44709709)
61. MO TALLEB G, HANACHI P, FAUZIAH O, ASMAH R. Effect of Berberis vulgaris fruit extract on alpha-feto-protein gene expression and chemical carcinogen metabolizing enzymes activities in hepato-carcinogenesis rats. Iran J Cancer Prevent 2008; 1: 33-44.
62. LEE JCK. Ferritin in malignant diseases. Bull-J Hong Kong Med Assoc 1984; 36: 57-61.
63. ASARE GA, MOSSANDA KS, KEW MC, PATERSON AC, KAHLWR-VENTER C P, SIZIBA K. Hepatocellular carcinoma caused by iron overload: A possible mechanism of direct hepatocacinogenicity. Toxicology 2006; 219: 41-52. (Pubitemid 43120705)
64. WU C, GROENINK M, BOSMA A, REITSMA PH, SANDER JH, ROBERT AFM. Rat ferritin-H: cDNA cloning, differential expression and localization during he-patocarcinogenesis. Carcinogenesis 1997, 18: 47-52. (Pubitemid 28134616)
65. HA WS, KIM CK, SONG SH, KANG CB. Study on mechanism of multistep hepatotumorigenesis in rat: development of hepatotumorigenesis. J Vet Sci 2001; 2: 53-58.
66. RAMAKRISHNAN G, AUGUSTINE TA, JAGAN S, VINODHKU-MAR R, DEVAKI T. Effect of silymarin on N-nitrosodi-ethylamine induced hepatocarcinogenesis in rats. Exp Oncol 2007; 29: 39-44. (Pubitemid 46713478)
67. BARTSCH H, HIETANEN E, MALAVEILLE C. Carcinogenic nitrosamines: free radical aspects of their action. Free Radic Biol Med 1989; 7: 637-644. (Pubitemid 20027482)
68. PADMAKUMARAN NKG, DEEPADEVI KV, ARUN P, KUMAR VM, SANTHOSH A, LEKSHMI LR, KURUP, PA. Toxic effect of systemic administration of low doses of the plasticizer di-(2-ethylhexyl) phthalate [DEHP] in rats. Indian J Exp Biol 1998; 36: 264-272.
69. BULLE F, MAVIER P, ZAFRANI ES, PREAUX AM, LESCS MC, SIEGRIST S, DHUMEAUX, D, GUELLAEN G. Mechanism of G-glutamyl transpeptidase release in serum during intrahepatic and extrahepatic cholestasis in the rat: a histochemical, biochemical and molecular approach. Hepatology 1990; 11: 545-550. (Pubitemid 20151729)
70. HUSEBY NE, INGEBRETSEN OC. The level of gamma-glutamyltransferase in serum, effect of carbohydrate heterogeneity on clearance rate. Scand J Clin Lab Invest 1993; 215: 93-100. (Pubitemid 23204333)
71. YAO D F, DONG ZZ, YAO DB, WU XH, WU W, QIU LW, WANG HM, MENG XY. Abnormal expression of he-patoma-derived gamma-glutamyltransferase subtyping and its early alteration for carcinogenesis of hepatocytes. Hepatobiliary Pancreat Dis Int 2004; 3: 564-570.
72. KOMLOSH A, VOLOHONSKY G, PORAT N, TUBY C, BLU-VSHTEIN E, STEINBERG P. Gamma-glutamyl transpepti-dase and glutathione biosynthesis in non-tumori-genic and tumorigenic rat liver oval cell lines. Car-cinogenesis 2002; 23: 671-678.
73. SHANAB G, MAHRAN M, ABDALLAH T, ABDALLAH N. Association of hepatitis C virus infection with anti-smooth muscle antibody (SMA) and rheumatoid factor (RF). Egypt J Biochem 2000; 18: 17-30.
74. RAJKAPOOR B, JAYAKAR B, MURUGESH N, SAKTHISEKARAN D. Chemoprevention and cytotoxic effect of Bauhinia variegate against N-nitrosodiethylamine induced liver tumors and human cancer cell lines. J Ethnopharmacol 2006; 104: 407-409. (Pubitemid 43356653)
75. MARX JJM. Toxicology of the blood: Pathophysiolo-gy, toxicological pathology and mechanistic aspects. In: Toxicology principles and applicants. Edited by Niesink JM, Vries J, Hollinger MA, pp. 817-837, 1996.
76. FABRIS C, PIRISI M, PANOZZO M P, SOARDO G, TONIUTTO P, HOCZA V, BARTOLI E. Intensity of inflammatory damage and lipoperoxide concentrations in liver disease. J Clin Pathol 1993; 46: 364-367. (Pubitemid 23138754)
77. STOHS SJ, BAGCHI D. Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol Med 1995; 18: 321-336.
78. CROSS C, HALLIWELL B, BORISH E, PRYOR W, AMES B, SAUL R, MCCORD J, HARMAN D. Oxygen radical and human diseases. Ann Intern Med 1987; 107: 526.
79. VANDENBERGHE J. Hepatotoxicity: Structure, Function and Toxicological pathology. In: Toxicology principles and application. Edited by Niesink, JM, Vries J, Hollinger MA, 669-721, 1996.
80. BANSAL AK, BANSAL M, SONI G, BHATNAGAR D. Protective role of vitamin E pre-treatment on N-ni-trosodiethylamine induced oxidative stress in rat liver. Chem-Biol Interact 2005; 156: 101-111. (Pubitemid 41406233)
81. SINGH BN, SINGH BR, SARMA, BK, SINGH HB. Potential chemoprevention of N-nitrosodiethylamine-in-duced hepatocarcinogenesis by polyphenolics from Acacia nilotica bark. Chem-Biol Interact 2009; 181: 20-28.
82. GUPTA C, VIKRAM A, TRIPATHI DN, RAMARAO P, JENA GB. Antioxidant and antimutagenic effect of quercetin against DEN induced hepatotoxicity in rat. Phytother Res 2009; 24: 119-128.
83. LIPPMAN SM, HONG WK. Cancer prevention science and practice. Cancer Res 2002; 62: 5119-5125. (Pubitemid 35024578)
84. MUKHERJEE P, EL-ABBADI MM, KASPERZYK JL, RANES MK, SEYFRIED TN. Dietary restriction reduces angiogen-esis and growth in an orthotopic mouse brain tumour model. Brit J Cancer 2002; 86: 1615-1621. (Pubitemid 34628116)
85. ROSE D P, CONNOLLY JM. Regulation of tumor angio-genesis by dietary fatty acids and eicosanoids. Nutr Cancer 2000; 37: 19-127.
86. OAK MH, EL BEDOUI J, SCHINI-KERTH VB. Antiangio-genic properties of natural polyphenols from red wine and green tea. J Nutr Biochem 2005; 16: 1-8. (Pubitemid 40052710)