Potential protective effect of Nigella sativa crude oils towards fatty liver in rats

European Journal of Lipid Science and Technology

Volumn 115, Issue 7, 2013, Pages 774-782

  Al Okbi, Sahar Y ^a   Mohamed, Doha A ^a   Hamed, Thanaa E ^a   Edris, Amr E ^a  

^a NATIONAL RESEARCH CENTRE   (Egypt)

Author keywords

Irradiation; Crude oil; Fatty liver; Liver protection; Nigella sativa

Indexed keywords

EID: 84880176832     PISSN: 14387697     EISSN: 14389312     Source Type: Journal    
DOI: 10.1002/ejlt.201200256     Document Type: Article

References (87)

1. Bayard, M., Holt, J., Boroughs, E., Nonalcoholic fatty liver disease. Am. Fam. Physician 2006, 73, 1961-1968.
2. Angulo, P., Nonalcoholic fatty liver disease. N. Engl. J. Med. 2002, 346, 1221-1231.
3. Qian, Y., Fan, G., Obesity, fatty liver and liver cancer. Hepatobiliary Pancreat. Dis. Int. 2005, 4, 173-177.
4. Alisi, A., Nobili, V., Non-alcoholic fatty liver disease in children now: Lifestyle changes and pharmacologic treatments. Nutrition 2012, 28, 722-726.
5. Mouralidarane, A., Oben, J., Soeda, J., Pathophysiology and clinical management of non-alcoholic fatty liver disease. Medicine 2011, 39, 592-596.
6. Jiménez, E., Río-Valle, J., Ferre, J., Fatty liver and its clinical management in obese adolescents. Endocrinol. Nutr. 2011, 58, 32-37.
7. Huang, A., Greenson, K., Chao, C., Anderson, L., et al., One-year intense nutritional counseling results in histological improvement in patients with non-alcoholic steatohepatitis: A pilot study. Am. J. Gastroenterol. 2005, 100, 1072-1081.
8. Fardet, A., Martin, F., Chardigny, M., Lipotropic capacity of raw plant-based foods: A new index that reflects their lipotrope density profile. J. Food Composition Anal. 2011, 24, 895-915.
9. Niebergall, L., Jacobs, R., Chaba, T., Vance, D., Phosphatidyl choline protects against steatosis in mice but not non-alcoholic steatohepatitis. Biochim. et Biophys. Acta (BBA) 2011, 1811, 1177-1185.
10. Yang, H., Tzeng, Y., Chai, C., Hsieh, A., et al., Soy protein retards the progression of non-alcoholic steatohepatitis via improvement of insulin resistance and steatosis. Nutrition 2011, 27, 943-948.
11. Pietu, F., Guillaud, O., Walter, T., Vallin, M., et al., Ursodeoxycholic acid with vitamin E in patients with nonalcoholic steatohepatitis: Long-term results. Clin. Res. Hepatol. Gastroenterol. 2012, 36, 146-155.
12. Sofer, E., Boaz, M., Matas, Z., Mashavi, M., Shargorodsky, M., Treatment with insulin sensitizer metformin improves arterial properties, metabolic parameters, and liver function in patients with nonalcoholic fatty liver disease: A randomized, placebo-controlled trial. Metabolism 2012, 60, 1278-1284.
13. Belfort, R., Harrison, A., Brown, K., et al., A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N. Engl. J. Med. 2006, 355, 2297-2307.
14. Bugianesi, E., Gentilcore, E., Manini, R., Natale, S., et al., A randomized controlled trial of metformin versus vitamin E or prescriptive diet in nonalcoholic fatty liver disease. Am. J. Gastroenterol. 2005, 100, 1082-1090.
15. Sofi, F., Giangrandi, I., Cesari, F., Corsani, I., et al., Effects of a 1-year dietary intervention with n-3 polyunsaturated fatty acid-enriched olive oil on non-alcoholic fatty liver disease patients: A preliminary study. Int. J. Food Sci. Nutr. 2010, 61, 792-802.
16. Shiba, S., Tsunoda, N., Wakutsu, M., Muraki, E., et al., Regulation of lipid metabolism by palmitoleate and eicosapentaenoic acid (EPA) in mice fed a high-fat diet. Biosci. Biotechnol. Biochem. 2011, 75, 2401-2403.
17. Yang, H., Miyahara, H., Takeo, J., Hatanaka, A., Katayama, M., Pollock oil supplementation modulates hyperlipidemia and ameliorates hepatic steatosis in mice fed a high-fat diet. Lipids Health Dis. 2011, 10, 189-199.
18. Chen, H., Li, C., Lin, H., Chien, T., Low, H., Depression by a green tea extract of alcohol-induced oxidative stress and lipogenesis in rat liver. Biosci. Biotechnol. Biochem. 2011, 75, 1668-1676.
19. Jaeschke, H., Ramachandran, A., Reactive oxygen species in the normal and acutely injured liver. J. Hepatol. 2011, 55, 227-228.
20. Dong, H., Lu, E., Zhao, L., Chinese herbal medicine in the treatment of nonalcoholic fatty liver disease. Chin. J. Integr. Med. 2012, 18, 152-160.
21. Chung, M., Park, H., Manautou, J., Koo, S., Bruno, R., Green tea extract protects against nonalcoholic steatohepatitis in ob/ob mice by decreasing oxidative and nitrative stress responses induced by proinflammatory enzymes. J. Nutr. Biochem. 2012, 23, 361-367.
22. Park, J., Lee, Y., Chung, Y., Park, K., et al., Green tea extract suppresses NFκB activation and inflammatory responses in diet-induced obese rats with nonalcoholic steatohepatitis. J. Nutr. 2012, 142, 57-63.
23. Wang, Y., Ausman, M., Greenberg, S., Russell, M., Wang, D., Dietary lycopene and tomato extract supplementations inhibit nonalcoholic steatohepatitis-promoted hepatocarcinogenesis in rats. Int. J. Cancer. 2010, 126, 1788-1796.
24. Aghazadeh, S., Amini, R., Yazdanparast, R., Ghaffari, S., Anti-apoptotic and anti-inflammatory effects of Silybum marianum in treatment of experimental steatohepatitis. Exp. Toxicol. Pathol. 2011, 63, 569-574.
25. Edris, A., Evaluation of the volatile oils from different local cultivars of Nigella sativa L. grown in Egypt with emphasis on the effect of extraction method on thymoquinone. J. Essent. Oil Bearing Plants 2010, 13, 154-164.
26. Gheita, A., Kenawy, A., Effectiveness of Nigella sativa oil in the management of reumatoid arthritis patients: A placebo controlled study. Phytother. Res. 2012, 26, 1246-1248.
27. Viuda-Martos, M., Mohamady, M., Fernández-López, J., Abd ElRazik, K., et al., In vitro antioxidant and antibacterial activities of essentials oils obtained from Egyptian aromatic plants. Food Control 2011, 22, 1715-1722.
28. Majdalawieh, A., Hmaidan, R., Carr, R., Nigella sativa exerts anti-inflammatory and anti-tumor activities in vitro. Eur. J. Pharmacol. 2011, 668, e41.
29. Lutterodt, H., Luther, M., Slavin, M., Yin, J., et al., Fatty acid profile, thymoquinone content, oxidative stability, and antioxidant properties of cold-pressed black cumin seed oils. LWT - Food Sci. Technol. 2010, 43, 1409-1413.
30. Al-Okbi, S., Ammar, N., Soroor, A., Mohamad, D., Impact of natural oils supplements on disease activity and antioxidant state of Egyptian patients with rheumatoid arthritis. Med. J. Islam Acad. Sci. 2000, 13, 161-171.
31. El-Bazza, Z., Farrag, H., El-Fouly, M., EL-Tablawy, S., Inhibitory effect of gamma radiation and Nigella sativa seeds oil on growth, spore germination and toxin production of fungi. Rad. Phys. Chem. 2001, 60, 181-189.
32. Kawasaki, T., Igarashi, K., Koeda, T., Sugimoto, K., et al., Rats fed fructose-enriched diets have characteristics of nonalcoholic hepatic steatosis. J. Nutr. 2009, 139, 2067-2071.
33. AOAC. The Official Method and Recommended Practices of the American Oil Chemists Society, 5th edition, AOCA Press, Champaign, Illinois 2000.
34. Paget, P., Barnes, T., Evaluation of Drug Activities, in: R. Laurrence, L. Bacharach, (Eds.), Pharmacometrics, Vol. 1, Academic Press, London, New York 1964, pp. 135-140.
35. Watson, D., A simple method for the determination of serum cholesterol. Clin. Chem. Acta 1960, 5, 637-642.
36. Burstein, M., Scholnick, R., Morfin, R., Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J. Lipid Res. 1970, 11, 583-595.
37. 2. J. Clin. Chem. Clin. Biochem. 1984, 22, 35-40.
38. Megraw, R., Dunn, D., Biggs, H., Manual and continuous flow colorimetry of triglycerols by a fully enzymatic method. Clin. Chem. 1979, 25, 273-284.
39. Satoh, K., Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin. Chim. Acta 1978, 90, 37-43.
40. Stepaniak, J., Gould, K., Sun, D., Swanborg, H., A comparative study of experimental autoimmune encephalomyelitis in Lewis and DA rats. J. Immunol. 1995, 155, 2762-2769.
41. Reitman, S., Frankel, S., Colorimetric methods for aspartate and alanine aminotransferase. Am. J. Clin. Pathol. 1957, 28, 55-60.
42. Gambino, R., Standard Methods of Clinical Chemistry, Academic Press, New York 1965.
43. Folch, J., Lees, M., Sloane, H., A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226, 497-509.
44. Cequier-Sánchez, E., Rodríguez, C., Ravelo, G., Zárate, R., Dichloromethane as a solvent for lipid extraction and assessment of lipid classes and fatty acids from samples of different natures. J. Agric. Food Chem. 2008, 56, 4297-4303.
45. Hamrouni-Sellami, I., Kchouk, M., Marzouk, B., Lipid and aroma composition of black cumin (Nigella sativa L.) seeds from Tunisia. J. Food Biochem. 2008, 32, 335-352.
46. Tulukcu, F., A comparative study on fatty acid composition of black cumin obtained from different regions of Turkey, Iran and Syria. Afr. J. Agric. Res. 2011, 6, 892-895.
47. Cheikh-Rouhou, S., Besbes, S., Hentati, B., Blecker, C., et al., Nigella sativa L.: Chemical composition and physicochemical characteristics of lipid fraction. Food Chem. 2007, 101, 673-681.
48. Harzallah, H., Kouidhi, B., Flamini, G., Bakhrouf, A., Mahjoub, T., Chemical composition, antimicrobial potential against cariogenic bacteria and cytotoxic activity of Tunisian Nigella sativa essential oil and thymoquinone. Food Chem. 2011, 129, 1469-1474.
49. Kokoska, L., Havlik, J., Valterova, I., Sovova, H., et al., Comparison of chemical composition and antibacterial activity of Nigella sativa seed essential oils obtained by different extraction methods. J. Food Prot. 2008, 71, 2475-2480.
50. Nickavar, B., Mojab, F., Javidniab, K., Amolia, M., Chemical composition of the fixed and volatile oils of Nigella sativa L. from Iran. Z. Naturforsch. 2003, 58c, 629-631.
51. Houcher, Z., Boudiaf, K., Benboubetra, M., Houcher, B., Effects of methanolic extract and commercial oil of Nigella sativa L. on blood glucose and antioxidant capacity in alloxan-induced diabetic Rats. Pteridine 2007, 18, 8-18.
52. Al-Okbi, S., Ammar, N., Abd El-Kader, M., Studies of some biochemical, nutritional and anti-inflammatory effects of Nigella Sativa Seeds. Egypt J. Pharm. Sci. 1997, 38, 451-469.
53. Lê, A., Bortolotti, M., Role of dietary carbohydrates and macronutrients in the pathogenesis of nonalcoholic fatty liver disease. Curr. Opin. Clin. Nutr. Metab. Care. 2008, 11, 477-482.
54. Mayes, A., Intermediary metabolism of fructose. Am. J. Clin. Nutr. 1993, 58, S754-S765.
55. Kelley, L., Allan, G., Azhar, S., High dietary fructose induces a hepatic stress response resulting in cholesterol and lipid dysregulation. Endocrinology 2004, 145, 548-555.
56. Taskinen, R., Adiels, M., Westerbacka, J., Söderlund, S., et al., Dual metabolic defects are required to produce hypertriglyceridemia in obese subjects. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 2144-2150.
57. Busserolles, J., Gueux, E., Rock, E., Mazur, A., Rayssiguier, Y., Substituting honey for refined carbohydrates protects rats from hypertriglyceridemic and prooxidative effects of fructose. J. Nutr. 2002, 132, 3379-3382.
58. Hajhashemi, V., Ghannadi, A., Jafarabadi, H., Black cumin seed essential oil as a potent analgesic and anti-inflammatory drug. Phytother. Res. 2004, 18, 195-199.
59. Woo, C., Kumar, A., Sethi, G., Tan, K., Thymoquinone: Potential cure for inflammatory disorders and cancer. Biochem. Pharmacol. 2012, 83, 443-451.
60. Umar, S., Zargan, J., Ahmad, S., Katiyar, C., Khan, H., Modulation of the oxidative stress and inflammatory cytokine response by thymoquinone in the collagen induced arthritis in Wistar rats. Chem. Biol. Interact. 2012, 197, 40-46.
61. Sankaranarayanan, C., Pari, L., Thymoquinone ameliorates chemical induced oxidative stress and β-cell damage in experimental hyperglycemic rats. Chem. Biol. Interact. 2011, 190, 148-154.
62. Evirgen, O., Gökçe, A., Ozturk, O., Nacar, E., et al., Effect of thymoquinone on oxidative stress in Escherichia coli-induced pyelonephritis in rats. Curr. Ther. Res. 2011, 72, 204-215.
63. Ammar, E., Gameil, N., Shawky, N., Nader, M., Comparative evaluation of anti-inflammatory properties of thymoquinone and curcumin using an asthmatic murine model. Int. Immunopharmacol. 2011, 11, 2232-2236.
64. Marsik, P., Kokoska, L., Landa, P., Nepovim, A., et al., In vitro inhibitory effects of thymol and quinones of Nigella sativa seed on cyclooxigenase-1- and -2-catalyzed prostaglandin E2 biosyntheses. Planta. Med. 2005, 71, 739-742.
65. Khalife, H., Lupidi, G., Nonenzymatic reduction of thymoquinone in physiological conditions. Free Radic. Res. 2007, 41, 153-161.
66. Nagi, N., Almakki, A., Sayed-Ahmed, M., Al-Bekairi, M., Thymoquinone supplementation reverses acetaminophen-induced oxidative stress, nitric oxide production and energy decline in mice liver. Food Chem. Toxicol. 2010, 48, 2361-2365.
67. Nagi, N., Mansour, A., Protective effect of thymoquinone against doxorubicin-induced cardiotoxicity in rats: A possible mechanism of protection. Pharmacol. Res. 2000, 41, 283-289.
68. Kruk, I., Michalska, T., Lichszteld, K., Kladna, A., Aboul-Enein, Y., The effect of thymol and its derivatives on reactions generating reactive oxygen species. Chemosphere 2000, 41, 1059-1064.
69. Badary, A., Taha, A., Gamal el-Din, M., Abdel-Wahab, H. Thymoquinone is a potent superoxide anion scavenger. Drug Chem. Toxicol. 2003, 26, 87-98.
70. El-Mahmoudy, A., Matsuyama, H., Borgan, A., Shimizu, Y., et al., Thymoquinone suppresses expression of inducible nitric oxide synthase in rat macrophages. Int. Immunopharmacol. 2002, 2, 1603-1611.
71. Ismail, M., Al-naqeep, G., Chan, W., Nigella sativa thymoquinone-rich fraction greatly improves plasma antioxidant capacity and expression of antioxidant genes in hypercholesterolemic rats. Free Radic. Biol. Med. 2009, 48, 664-672.
72. El-Dakhakhny, M., Madi, J., Lembert, N., Ammon, P., Nigella sativa oil, nigellone and derived thymoquinone inhibit synthesis of 5-lipoxygenase products in polymorphonuclear leukocytes from rats. J. Ethnopharmacol. 2002, 81, 161-164.
73. Sayed-Ahmed, M., Nagi, N., Thymoquinone supplementation prevents the development of gentamicin-induced acute renal toxicity in rats. Clin. Exp. Pharmacol. Physiol. 2007, 34, 399-405.
74. Meddah, B., Ducroc, R., El Abbes, M., Eto, B., et al., Nigella sativa inhibits intestinal glucose absorption and improves glucose tolerance in rats. J. Ethnopharmacol. 2009, 121, 419-424.
75. Le, M., Benhaddou-Andaloussi, A., Elimadi, A., Settaf, A., et al., The petroleum ether extract of Nigella sativa exerts lipid-lowering and insulin-sensitizing actions in the rat. J. Ethnopharmacol. 2004, 94, 251-259.
76. Meral, I., Yener, Z., Kahraman, T., Mert, N., Effect of Nigella sativa on glucose concentration, lipid peroxidation, anti-oxidant defence system and liver damage in experimentally-induced diabetic rabbits. J. Vet. Med. A Physiol. Pathol. Clin. Med. 2001, 48, 593-599.
77. Asikin, Y., Taira, I., Inafuku, S., Sumi, H., et al., Volatile aroma components and antioxidant activities of the flavedo peel extract of unripe shiikuwasha (Citrus depressa Hayata). J. Food Sci. 2012, 77, C469-C475.
78. Loizou, S., Lekakis, I., Chrousos, P., Moutsatsou, P., β-sitosterol exhibits anti-inflammatory activity in human aortic endothelial cells. Mol. Nutr. Food Res. 2010, 54, 551-558.
79. Cheikh-Rouhou, S., Besbes, S., Lognay, G., Blecker, C., et al., Sterol composition of black cumin (Nigellas ativa L.) and Aleppo pine (Pinus halepensis Mill.) seed oils. J. Food Comp. Anal. 2008, 21, 162-168.
80. Ramadan, F., Wahdan, K., Blending of corn oil with black cumin (Nigella sativa) and coriander (Coriandrum sativum) seed oils: Impact on functionality, stability and radical scavenging activity. Food Chem. 2012, 132, 873-879.
81. Papackova, Z., Palenickova, E., Dankova, H., Zdychova, J., et al., Kupffer cells ameliorate hepatic insulin resistance induced by high-fat diet rich in monounsaturated fatty acids: The evidence for the involvement of alternatively activated macrophages. Nutr. Metab. (Lond.) 2012, 9, 22.
82. Petit, M., Guiu, B., Duvillard, L., Jooste, V., et al., Increased erythrocytes n-3 and n-6 polyunsaturated fatty acids is significantly associated with a lower prevalence of steatosis in patients with type 2 diabetes. Clin. Nutr. 2012, 31, 520-525.
83. Hofacer, R., Magrisso, J., Jandacek, R., Rider, T., et al., Omega-3 fatty acid deficiency increases stearoyl-CoA desaturase expression and activity indices in rat liver: Positive association with non-fasting plasma triglyceride levels. Prostaglandins Leukot. Essent. Fatty Acids 2012, 86, 71-77.
84. Fatemi, F., Allameh, A., Khalafi, H., Ashrafihelan, J., Hepatoprotective effects of γ-irradiated caraway essential oils in experimental sepsis. Appl. Rad. Isot. 2010, 68, 280-285.
85. Alsaif, A., Effect of thymoquinone on ethanol-induced hepatotoxicity in Wistar rats. J. Med. Sci. 2007, 7, 1164-1170.
86. Alsaif, A., Effect of Nigella sativa oil on metabolic responses to prolonged systemic injury in rats. J. Biol. Sci. 2008, 8, 974-983.
87. Moneim, A., El-Feki, M., Salah, E., Effect of Nigella sativa, fish oil and gliclazide on alloxan diabetic rats 1-biochemical and histo-pathological studies. J. Egypt. Ger. Soc. Zool. 1997, 23, 237-265.