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Altın Suriye Hamsterlarında Hiperlipidemik Diyet ile Oluşturulan Karaciğer Hasarı Üzerine Hodan Yağının Etkileri

Year 2019, Volume: 14 Issue: 3, 252 - 262, 25.12.2019
https://doi.org/10.17094/ataunivbd.505675

Abstract

Bu çalışma, erkek altın Suriye hamsterinda hiperlipidemik diyet ile oluşturulan karaciğer hasarına karşı Gamma Linolenik Asit (GLA) açısından zengin olan hodan yağının hepatoprotektif etkilerini incelenmek için tasarlanmıştır. Bu deneyde, erkek hamsterden oluşan toplam 60 hayvan kullanılmıştır. Bu deney iki aşamada gerçekleştirilmiştir. İlk aşama 4 hafta sürdü, bu aşamada, hamsterler 4 gruba ayrılmıştır. S1 (kontrol), sadece ticari kemirgen diyeti ile beslenmiştir. Diğer gruplar S2, S3 ve S4 ise 80% ticari kemirgen diyeti +%20 yağ içeren diyet ile beslenmiştir (hiperlipidemik diyet). İkinci aşama da yine 4 hafta sürdü, sadece S2 hiperlipidemik diyetle beslenmiştir. S4’e hodan yağı günlük olarak 2g yağ/kg vücut ağırlığı gavaj yoluyla verilmiştir. Hiperlipidemik diyetin alımı, hepatositlerde lipid birikimine neden oldu ve anlamlı olarak (P<0.05) ilk aşama sonunda S2, S3 ve S4 gruplarının her birinde ALT, AST, ALP, LDH, GGT ve CK gibi enzimlerin aktivitesini arttırdı. Bu negatif etkiler sadece S4’te hodan yağı kullanımıyla ortadan kaldırılmıştır.

References

  • 1. Leung PS., 2016. The Gastrointestinal System: Gastrointestinal, Nutritional and Hepatobiliary Physiology; Springer: New York, NY, USA,24-36. 2. Araujo AR., Rosso N., Bedogni G., Tiribelli C., Bellentani S., 2018. Global epidemiology of non-alcoholic fatty liver disease/non-alcoholic steatohepatitis: What we need in the future. Liver Int, 38, 47-51. 3. Chalasani N., Younossi Z., Lavine JE., Charlton M., Cusi K., Rinella M., Harrison SA., Brunt EM., Sanyal AJ., 2018. The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the study of liver diseases. Hepatology, 67, 328-357. 4. Browning JD., Horton JD., 2004. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest, 114, 147-152. 5. Nabavi SY., Silva AS.,2018. Nonvitamin and Nonmineral Nutritional Supplements. In “Borage (Borago officinalis L.)”, Tewari D., Bawari S., Patni P., Sah AN, 1st ed., 165-170, London, United Kingdom ; San Diego, CA, United States : Academic Press. 6. Singh H., Du J., Yi TH., 2017. Green and rapid synthesis of silver nanoparticles using Borago officinalis leaf extract: anticancer and antibacterial activities. Artif Cells, Nanomedicine, Biotechnol, 45, 1310-1316. 7. Asadi-Samani M., Bahmani M., Rafieian-Kopaei M., 2014. The chemical composition, botanical characteristic and biological activities of Borago officinalis: a review. Asian Pac J Trop Med,7, 22-28. 8. Shewale SV., Boudyguina E., Zhu X., Shen L., Hutchins PM., Barkley RM., Murphy RC., Parks J S., 2015. Botanical oils enriched in n-6 and n-3 FADS2 products are equally effective in preventing atherosclerosis and fatty liver. J Lipid Res, 56, 1191-1205. 9. Moelants EAV., Mortier A., Van Damme J., Proost P., 2013. Regulation of TNF-alpha with a focus on rheumatoid arthritis. Immunol Cell Biol, 91, 393-401. 10. Gilania AH., Bashira S., Khana AU., 2007. Pharmacological basis for the use of Borago officinalis in gastrointestinal, respiratory and cardiovascular disorders. J Ethnopharmacol, 114, 393-399. 11. Hamilton LA., Trobaugh KA., 2011. Acute respiratory distress syndrome: use of specialized nutrients in pediatric patients and infants. Nutr Clin Pract, 26, 26-30. 12. Segarnick DJ., Mandio Cordasco D., Agura V., Cooper NS., Rotrosen J., 1985. Gamma-linolenic acid inhibits the development of the ethanol-induced fatty liver. Prostaglandins Leukot Med, 17, 277-282. 13. Lukivskaya OY., Naruta E., Sadovnichy V., Kirko S., Buko VU., 2012. Reversal of experimental ethanol-induced liver steatosis by borage oil. Phytother Res, 26, 1626-1631. 14. Garces R., Mancha M., 1993. One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Analytical Biochem, 211, 139-143. 15. Adams RP., 2007. Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. Allured Publishing, carol stream, IL. J Am Soc Mass Spectrom, 18, 803-806. 16. Wilson TA., Kritchevsky D., Kotyla T., Nicolosi RJ., 2006. Structured triglycerides containing caprylic (8:0) and oleic (18:1) fatty acids reduce blood cholesterol concentrations and aortic cholesterol accumulation in hamsters. Biochim Biophys Acta, 1761, 345-349. 17. Imaizumi K., Abe K., Kuroiwa C., Sugano M., 1993. Fat containing stearic acid increases fecal neutral steroid excretion and catabolism of low density lipoproteins without affecting plasma cholesterol concentration in hamsters fed a cholesterol containing dite. Nutr, 123, 1693-1702. 18. Trautwein EA., Kunath-Rau A., Dietrich J., Srusch S., Erbersdobler HF., 1997. Effect of dietary fats rich in lauric, myristic, plamitic, oleic or linoleic acid on plasma, hepatic and biliary lipids in cholesterol-fed hamsters. Br J Nutr, 77, 605-620. 19. Del Rio-Celestino M., Font R., de Haro-Bailon A., 2008. Distribution of fatty acids in edible organs and seed fractions of borage (Borago officinalis L.) J Sci Food Agric, 88, 248-255. 20. Hamrouni I., Touati S., Marzouk B., 2002. Evolution des lipides au cours de la formation et de la maturation de la graine de bourrache (Borago officinalis L.). Riv Ital Sostanze Gr, 79, 113-118. 21. Gomez A., Martinez De La Ossa E., 2002. Quality of borage seed oil extracted by liquid and supercritical carbon dioxide. Chem Eng J, 88, 103-109. 22. Mhamdi B., Wannes WA., Bourgou S., Marzouk B., 2007. Biochemical charaterization of borage (Borago Officinalis L.) seeds. J Food Biochem, 33, 331-341. 23. De spirt S., Stahl W., Tronnier H., Sies H., Bejot M., Maurette JM., Heinrich U., 2009. Intervention with flaxseed and borage oil supplements modulates skin condition in women. BJN, 101, 440-445. 24. Garcia IJP., Cezar JS., Lemos BS., Silva LN., Ribeiro RIMA., Santana CC., Grillo LAM., Pinto FCH., Buzelle SL., Cortes VF., Santos HL., Santos MESM., Barbosa LA., 2008. Effects of high fat diet on kidney lipid content and the Na, K-ATPase activity. Braz J Pharm, Sci, 54, 1-13. 25. Tzang BS., Yang SF., Fu SG., Yang HC., Sun HL., Chen YC., 2009. Effects of dietary flaxseed oil on cholesterol metabolism of hamsters. Food Chem, 114, 1450-1455. 26. Schirmer MA., Phinney SD., 2007. Gammalinolenate reduces weight regain in formerly obese humans. J Nutr, 137, 1430-1435. 27. Guil-Guerrero JL., Gomez-Mercado F., Ramos-Bueno RP., Gonzalez-Fernandez MJ., Urrestarazu M., Rincon-Cervera MA., 2017. Sardinian boraginaceae are new potential sources of gamma-linolenic acid. Food Chem, 218, 435-439. 28. Horrobin DF., 1992. Nutritional and medical importance of gamma-linolenic acid. Progress Lipid Res, 31, 163-194. 29. Rump P., Popp-Snijders C., Heine RJ., Hornstra G., 2002. Diabetologia, 45, 349-355. 30. Huo HZ., Wang B., Liang YK., Bao YY., Gu Y., 2011. Hepatoprotective and antioxidant effects of licorice extract against CCl4-induced oxidative damage in rats. Int J Mol Sci, 12, 6529-6543. 31. Ozer J., Ratner M., Shaw M., Bailey W., Schomaker S., 2008. The current state of serum biomarkers of hepatotoxicity. Toxicol, 245, 194- 205. 32. Kinosian B., Glick H., Garland G., 1994. Cholesterol and coronary heart disease: Predicting risks by levels and ratios. Ann Intern Med, 121, 641-647. 33. Hauptman K., Tich F., Knotek Z., 2001. Clinical diagnostics of hepatopathies in small mammals: Evaluation of importance of individual methods. Review article. Acta Vet Brno, 70, 297-311. 34. Giannini EG., Testa R., Savarino V., 2005. Liver enzyme alteration: A guide for clinicians. CAMJ, 172, 367-379. 35. Mc farland MB., 1994. Nursing Implication of Laboratory Testes. 3rd ed., 190-205. Delmar Publishers, Inc. 36. Gloria AO., Oyelola BO., Adenike TO., Anthony AA., 2010. Effects of diet-induced hypercholesterolemia on the lipid profile and some enzyme activities in female Wistar rats. Afr J Biochem Res, 4, 149-154. 37. Joanna C., Henryk B., Jadwiga K., Renata F., 2013. The effect of buckwheat (Fagopyrum esculentum Moench) groats addition to the lard diet on antioxidant parameters of plasma and selected tissues in Wistar Rats. World Acad Sci, ETJ, 79, 203-211. 38. Abreu ICME., Guerra JFC., Pereira RR., Silva M., Lima WG., Silva ME., Pedrosa ML., 2014. Hypercholesterolemic diet induces hepatic steatosis and alterations in mRNA expression of NADPH oxidase in rat livers. Arq Bras Endocrinol Metab, 58, 251-259. 39. Law M., Rudnicka AR., 2006. Statin Safety: A Systematic Review. Am J Cardiol, 97, 52-60 40. Tsai CH., Wu MY., Changl HH., Lin HC., Lee TY., 2008. Obesity induced hepatic oxidative stress down-regulate the level of circulating endothelial progenitor cells. J Hepatol, 48, 364-365. 41. Stolcpart RS., Olson KL., Delate T., Rasmussen J., Rehring TF., Merenich, JA., 2010. The risk for significant creatine kinase elevation with statins. Am J Cardiovas Drugs, 10, 92-187. 42. Qin Y., Zhou Y., Chen SH., Zhao XL., Ran L., Zeng XL., Wu Y., Chen JL., Kang C., Shu FR., Zhang QY., Mi MT., 2015. Fish oil supplements lower serum lipids and glucose in correlation with a reduction in plasma fibroblast growth factor 21 and PG E2 in nonalcoholic fatty liver disease associated with hyperlipidemia: A randomized clinical trial. PLoS ONE, 10, 1-13. 43. He XX., Wu XL., Chen RP., Chen C., Liu XG., Wu BJ., Huang ZM., 2016. Effectiveness of omega-3 in NAFLD: A meta-analysis of randomized controlled trials. PLoS ONE, 11, 1-22. 44. Kapoor V., Glover R., Malviya MN., 2015. Alternative lipid emulsions versus pure soy oil based lipid emulsions for parenterally fed preterm infants. Cochrane Database Syst Rev, 1-171. 45. Alhilal MK., Supuh AM., Hapra N., 2014. Borage oil rich in gama linolenic acid (GLA) reduces cardiovascular disease (CVD) risk factors in hamsters fed in diet rich in saturated fatty acids (SFAS) and cholesterol. Bas J Vet Res, 1, 54-65.

The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters

Year 2019, Volume: 14 Issue: 3, 252 - 262, 25.12.2019
https://doi.org/10.17094/ataunivbd.505675

Abstract

This study was designed to examine the hepatoprotective effects of Borage seed oil rich in Gamma Linolenic acid (GLA) against hyperlipidemic diet-induced liver damage in the male golden Syrian hamster. In this experiment a total of 60 animals of male hamsters were used. This experiment was carried out in 2 periods. The first period lasted 4 weeks, in which hamsters were segregated into 4 groups. S1 served as control (given a commercial rodent diet only). Other groups, S2, S3 and S4 were fed with a diet containing of %80 commercial rodent diet + 20% fats (Hyperlipidemic Diet). The second period lasted 4 weeks, in which S2 only that continued fed with hyperlipidemic diet. S4 was orally gavaged with borage oil at 2 g/kg of the body weight daily. Hyperlipidemic diet intake caused lipid accumulation in hepatocytes and significantly (P<0.05) increased the activities of ALT, AST, ALP, LDH, GGT and CK enzymes in each of the S2, S3 and S4 groups at the end of the first period. These negative effects were removed only in S4 by the use of borage oil.

References

  • 1. Leung PS., 2016. The Gastrointestinal System: Gastrointestinal, Nutritional and Hepatobiliary Physiology; Springer: New York, NY, USA,24-36. 2. Araujo AR., Rosso N., Bedogni G., Tiribelli C., Bellentani S., 2018. Global epidemiology of non-alcoholic fatty liver disease/non-alcoholic steatohepatitis: What we need in the future. Liver Int, 38, 47-51. 3. Chalasani N., Younossi Z., Lavine JE., Charlton M., Cusi K., Rinella M., Harrison SA., Brunt EM., Sanyal AJ., 2018. The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the study of liver diseases. Hepatology, 67, 328-357. 4. Browning JD., Horton JD., 2004. Molecular mediators of hepatic steatosis and liver injury. J Clin Invest, 114, 147-152. 5. Nabavi SY., Silva AS.,2018. Nonvitamin and Nonmineral Nutritional Supplements. In “Borage (Borago officinalis L.)”, Tewari D., Bawari S., Patni P., Sah AN, 1st ed., 165-170, London, United Kingdom ; San Diego, CA, United States : Academic Press. 6. Singh H., Du J., Yi TH., 2017. Green and rapid synthesis of silver nanoparticles using Borago officinalis leaf extract: anticancer and antibacterial activities. Artif Cells, Nanomedicine, Biotechnol, 45, 1310-1316. 7. Asadi-Samani M., Bahmani M., Rafieian-Kopaei M., 2014. The chemical composition, botanical characteristic and biological activities of Borago officinalis: a review. Asian Pac J Trop Med,7, 22-28. 8. Shewale SV., Boudyguina E., Zhu X., Shen L., Hutchins PM., Barkley RM., Murphy RC., Parks J S., 2015. Botanical oils enriched in n-6 and n-3 FADS2 products are equally effective in preventing atherosclerosis and fatty liver. J Lipid Res, 56, 1191-1205. 9. Moelants EAV., Mortier A., Van Damme J., Proost P., 2013. Regulation of TNF-alpha with a focus on rheumatoid arthritis. Immunol Cell Biol, 91, 393-401. 10. Gilania AH., Bashira S., Khana AU., 2007. Pharmacological basis for the use of Borago officinalis in gastrointestinal, respiratory and cardiovascular disorders. J Ethnopharmacol, 114, 393-399. 11. Hamilton LA., Trobaugh KA., 2011. Acute respiratory distress syndrome: use of specialized nutrients in pediatric patients and infants. Nutr Clin Pract, 26, 26-30. 12. Segarnick DJ., Mandio Cordasco D., Agura V., Cooper NS., Rotrosen J., 1985. Gamma-linolenic acid inhibits the development of the ethanol-induced fatty liver. Prostaglandins Leukot Med, 17, 277-282. 13. Lukivskaya OY., Naruta E., Sadovnichy V., Kirko S., Buko VU., 2012. Reversal of experimental ethanol-induced liver steatosis by borage oil. Phytother Res, 26, 1626-1631. 14. Garces R., Mancha M., 1993. One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Analytical Biochem, 211, 139-143. 15. Adams RP., 2007. Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. Allured Publishing, carol stream, IL. J Am Soc Mass Spectrom, 18, 803-806. 16. Wilson TA., Kritchevsky D., Kotyla T., Nicolosi RJ., 2006. Structured triglycerides containing caprylic (8:0) and oleic (18:1) fatty acids reduce blood cholesterol concentrations and aortic cholesterol accumulation in hamsters. Biochim Biophys Acta, 1761, 345-349. 17. Imaizumi K., Abe K., Kuroiwa C., Sugano M., 1993. Fat containing stearic acid increases fecal neutral steroid excretion and catabolism of low density lipoproteins without affecting plasma cholesterol concentration in hamsters fed a cholesterol containing dite. Nutr, 123, 1693-1702. 18. Trautwein EA., Kunath-Rau A., Dietrich J., Srusch S., Erbersdobler HF., 1997. Effect of dietary fats rich in lauric, myristic, plamitic, oleic or linoleic acid on plasma, hepatic and biliary lipids in cholesterol-fed hamsters. Br J Nutr, 77, 605-620. 19. Del Rio-Celestino M., Font R., de Haro-Bailon A., 2008. Distribution of fatty acids in edible organs and seed fractions of borage (Borago officinalis L.) J Sci Food Agric, 88, 248-255. 20. Hamrouni I., Touati S., Marzouk B., 2002. Evolution des lipides au cours de la formation et de la maturation de la graine de bourrache (Borago officinalis L.). Riv Ital Sostanze Gr, 79, 113-118. 21. Gomez A., Martinez De La Ossa E., 2002. Quality of borage seed oil extracted by liquid and supercritical carbon dioxide. Chem Eng J, 88, 103-109. 22. Mhamdi B., Wannes WA., Bourgou S., Marzouk B., 2007. Biochemical charaterization of borage (Borago Officinalis L.) seeds. J Food Biochem, 33, 331-341. 23. De spirt S., Stahl W., Tronnier H., Sies H., Bejot M., Maurette JM., Heinrich U., 2009. Intervention with flaxseed and borage oil supplements modulates skin condition in women. BJN, 101, 440-445. 24. Garcia IJP., Cezar JS., Lemos BS., Silva LN., Ribeiro RIMA., Santana CC., Grillo LAM., Pinto FCH., Buzelle SL., Cortes VF., Santos HL., Santos MESM., Barbosa LA., 2008. Effects of high fat diet on kidney lipid content and the Na, K-ATPase activity. Braz J Pharm, Sci, 54, 1-13. 25. Tzang BS., Yang SF., Fu SG., Yang HC., Sun HL., Chen YC., 2009. Effects of dietary flaxseed oil on cholesterol metabolism of hamsters. Food Chem, 114, 1450-1455. 26. Schirmer MA., Phinney SD., 2007. Gammalinolenate reduces weight regain in formerly obese humans. J Nutr, 137, 1430-1435. 27. Guil-Guerrero JL., Gomez-Mercado F., Ramos-Bueno RP., Gonzalez-Fernandez MJ., Urrestarazu M., Rincon-Cervera MA., 2017. Sardinian boraginaceae are new potential sources of gamma-linolenic acid. Food Chem, 218, 435-439. 28. Horrobin DF., 1992. Nutritional and medical importance of gamma-linolenic acid. Progress Lipid Res, 31, 163-194. 29. Rump P., Popp-Snijders C., Heine RJ., Hornstra G., 2002. Diabetologia, 45, 349-355. 30. Huo HZ., Wang B., Liang YK., Bao YY., Gu Y., 2011. Hepatoprotective and antioxidant effects of licorice extract against CCl4-induced oxidative damage in rats. Int J Mol Sci, 12, 6529-6543. 31. Ozer J., Ratner M., Shaw M., Bailey W., Schomaker S., 2008. The current state of serum biomarkers of hepatotoxicity. Toxicol, 245, 194- 205. 32. Kinosian B., Glick H., Garland G., 1994. Cholesterol and coronary heart disease: Predicting risks by levels and ratios. Ann Intern Med, 121, 641-647. 33. Hauptman K., Tich F., Knotek Z., 2001. Clinical diagnostics of hepatopathies in small mammals: Evaluation of importance of individual methods. Review article. Acta Vet Brno, 70, 297-311. 34. Giannini EG., Testa R., Savarino V., 2005. Liver enzyme alteration: A guide for clinicians. CAMJ, 172, 367-379. 35. Mc farland MB., 1994. Nursing Implication of Laboratory Testes. 3rd ed., 190-205. Delmar Publishers, Inc. 36. Gloria AO., Oyelola BO., Adenike TO., Anthony AA., 2010. Effects of diet-induced hypercholesterolemia on the lipid profile and some enzyme activities in female Wistar rats. Afr J Biochem Res, 4, 149-154. 37. Joanna C., Henryk B., Jadwiga K., Renata F., 2013. The effect of buckwheat (Fagopyrum esculentum Moench) groats addition to the lard diet on antioxidant parameters of plasma and selected tissues in Wistar Rats. World Acad Sci, ETJ, 79, 203-211. 38. Abreu ICME., Guerra JFC., Pereira RR., Silva M., Lima WG., Silva ME., Pedrosa ML., 2014. Hypercholesterolemic diet induces hepatic steatosis and alterations in mRNA expression of NADPH oxidase in rat livers. Arq Bras Endocrinol Metab, 58, 251-259. 39. Law M., Rudnicka AR., 2006. Statin Safety: A Systematic Review. Am J Cardiol, 97, 52-60 40. Tsai CH., Wu MY., Changl HH., Lin HC., Lee TY., 2008. Obesity induced hepatic oxidative stress down-regulate the level of circulating endothelial progenitor cells. J Hepatol, 48, 364-365. 41. Stolcpart RS., Olson KL., Delate T., Rasmussen J., Rehring TF., Merenich, JA., 2010. The risk for significant creatine kinase elevation with statins. Am J Cardiovas Drugs, 10, 92-187. 42. Qin Y., Zhou Y., Chen SH., Zhao XL., Ran L., Zeng XL., Wu Y., Chen JL., Kang C., Shu FR., Zhang QY., Mi MT., 2015. Fish oil supplements lower serum lipids and glucose in correlation with a reduction in plasma fibroblast growth factor 21 and PG E2 in nonalcoholic fatty liver disease associated with hyperlipidemia: A randomized clinical trial. PLoS ONE, 10, 1-13. 43. He XX., Wu XL., Chen RP., Chen C., Liu XG., Wu BJ., Huang ZM., 2016. Effectiveness of omega-3 in NAFLD: A meta-analysis of randomized controlled trials. PLoS ONE, 11, 1-22. 44. Kapoor V., Glover R., Malviya MN., 2015. Alternative lipid emulsions versus pure soy oil based lipid emulsions for parenterally fed preterm infants. Cochrane Database Syst Rev, 1-171. 45. Alhilal MK., Supuh AM., Hapra N., 2014. Borage oil rich in gama linolenic acid (GLA) reduces cardiovascular disease (CVD) risk factors in hamsters fed in diet rich in saturated fatty acids (SFAS) and cholesterol. Bas J Vet Res, 1, 54-65.
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Details

Primary Language English
Subjects Health Care Administration
Journal Section Araştırma Makaleleri
Authors

Mohammad Alhilal

Suzan Alhilal This is me

Thana Albaz This is me

Publication Date December 25, 2019
Published in Issue Year 2019 Volume: 14 Issue: 3

Cite

APA Alhilal, M., Alhilal, S., & Albaz, T. (2019). The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 14(3), 252-262. https://doi.org/10.17094/ataunivbd.505675
AMA Alhilal M, Alhilal S, Albaz T. The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. December 2019;14(3):252-262. doi:10.17094/ataunivbd.505675
Chicago Alhilal, Mohammad, Suzan Alhilal, and Thana Albaz. “The Effects of Borage Oil on Hyperlipidemic Diet-Induced Liver Damage in Male Golden Syrian Hamsters”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 14, no. 3 (December 2019): 252-62. https://doi.org/10.17094/ataunivbd.505675.
EndNote Alhilal M, Alhilal S, Albaz T (December 1, 2019) The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 14 3 252–262.
IEEE M. Alhilal, S. Alhilal, and T. Albaz, “The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 14, no. 3, pp. 252–262, 2019, doi: 10.17094/ataunivbd.505675.
ISNAD Alhilal, Mohammad et al. “The Effects of Borage Oil on Hyperlipidemic Diet-Induced Liver Damage in Male Golden Syrian Hamsters”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 14/3 (December 2019), 252-262. https://doi.org/10.17094/ataunivbd.505675.
JAMA Alhilal M, Alhilal S, Albaz T. The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2019;14:252–262.
MLA Alhilal, Mohammad et al. “The Effects of Borage Oil on Hyperlipidemic Diet-Induced Liver Damage in Male Golden Syrian Hamsters”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, vol. 14, no. 3, 2019, pp. 252-6, doi:10.17094/ataunivbd.505675.
Vancouver Alhilal M, Alhilal S, Albaz T. The Effects of Borage Oil on Hyperlipidemic Diet-induced Liver Damage in Male Golden Syrian Hamsters. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2019;14(3):252-6.