The effect of single clove Black garlic on the hemostasis status and lipid profile in male Sprague Dawley rats with non-alcoholic fatty liver disease

Authors

  • Lili Nurmawati Diponegoro University, Faculty of Medicine, Department of Nutrition Science, Jl. Prof H.Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +628122991238 https://orcid.org/0000-0002-7626-2977
  • Mohammad Sulchan Diponegoro University, Faculty of Medicine, Department of Nutrition Science, Jl. Prof H. Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +62816655235
  • Siti Fatimah-Muis Diponegoro University, Faculty of Medicine, Department of Nutrition Science, Jl. Prof H. Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +628122867895 https://orcid.org/0000-0003-3786-5844
  • Hery Djagat Purnomo Division of Gastroentero-Hepatology, Department of Internal Medicine, Dr. Kariadi Hospital – Faculty of Medicine, Diponegoro University, Jl. Prof H.Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +628122803136 https://orcid.org/0000-0003-4235-8564
  • Kis Djamiatun Diponegoro University, Faculty of Medicine, Department of Biomedical Science, Jl. Prof H. Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +6281390351351 https://orcid.org/0000-0002-0498-8808
  • Martha Ardiaria Diponegoro University, Faculty of Medicine, Department of Nutrition Science, Jl. Prof H. Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +6281316225225
  • Vega Karlowee Diponegoro University, Faculty of Medicine, Department of Pathology Anatomy, Jl. Prof H.Soedarto, SH, Tembalang, 50275, Semarang, Indonesia, Tel.: +6282221894529 https://orcid.org/0000-0003-2227-6449

DOI:

https://doi.org/10.5219/1516

Keywords:

single clove black garlic, PAI-1, lipid profile, NAFLD, cardiovascular disease

Abstract

Non-alcoholic fatty liver disease (NAFLD) patients have alteration in hemostasis components. Thus, including excess expression of plasminogen activator inhibitor-1 (PAI-1), causing fibrinolysis disorders; the majority of these patients are hypercoagulable state prone to thrombosis. Some evidence suggests that garlic and garlic supplements have antithrombotic and anti-inflammatory properties. Besides, garlic stimulates fibrinolytic activity and normalizes plasma lipid imbalances. Black garlic is processed garlic that is produced through natural aging at a controlled temperature (70 °C) and high humidity (90%) for several days, without other additives. This study aimed to prove the effect of single clove black garlic (SCBG) (Allium sativum Linn) on PAI-1 levels and lipid profiles of NAFLD rats induced by a high-fat fructose diet (HFFD) containing 1.25% cholesterol and 0.5% cholic acid.The rats were then divided into healthy control group (K1+); NAFLD control group without treatment (K2+); 0.9 mg simvastatin treatment group (K1-); 45 mg metformin treatment group (K2-); SCBG 450 mg per 200g BW (X1); 900 mg per 200 g BW (X2); and 1350 mg per 200 g BW (X3). All treatments were administered for 4 weeks via oral gavage. As a result, significant differences in PAI-1 levels and lipid profiles between groups after the administration (p = 0.001) were noted and also by simvastatin and metformin, respectively. There was a correlation between PAI-1 and lipid profile of SCBG treatment. In conclusion, the administration of SCBG (1350 mg per 200 g BB per day) for 4 weeks had a significant effect on PAI-1 levels, and the lipid profiles in Sprague Dawley rats modeled NAFLD (p = 0.001). SCBG has provided benefits that can be useful in the management of NAFLD but it’s not equivalent to medicine.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

Abe, N., Kato, S., Tsuchida, T., Sugimoto, K., Saito, R., Verschuren, L., Kleemann, R., Oka, K. 2019. Longitudinal characterization of diet-induced genetic murine models of non-alcoholic steatohepatitis with metabolic, histological, and transcriptomic hallmarks of human patients. Biology Open, vol. 8, 11 p. https://doi.org/10.1242/bio.041251 DOI: https://doi.org/10.1242/bio.041251

Agarwal, K. C. 1996. Therapeutic actions of garlic constituents. Medicinal Research Reviews, vol. 16, no. 1, p. 111-124. https://doi.org/10.1002/(SICI)1098-1128(199601)16:1<111::AID-MED4>3.0.CO;2-5 DOI: https://doi.org/10.1002/(SICI)1098-1128(199601)16:1<111::AID-MED4>3.0.CO;2-5

Alkhouri, N., Tamimi, T. A. R., Yerian, L., Lopez, R., Zein, N. N., Feldstein, A. E. 2010. The Inflamed Liver and Atherosclerosis: A Link Between Histologic Severity of Nonalcoholic Fatty Liver Disease and Increased Cardiovascular Risk. Digestive Diseases and Sciences, vol. 55, p. 2644-2650. https://doi.org/10.1007/s10620-009-1075-y DOI: https://doi.org/10.1007/s10620-009-1075-y

Arruda de Faria, C., Zanette, D. L., Silva Jr., W. A., Ribeiro Paes, J. T. 2019. PAI-1 inhibition by simvastatin as a positive adjuvant in cell therapy. Molecular Biology Reports, vol. 46, p. 1511-1517. https://doi.org/10.1007/s11033-018-4562-4 DOI: https://doi.org/10.1007/s11033-018-4562-4

Asdaq, S. M. B. 2015. Antioxidant and Hypolipidemic Potential of Aged Garlic Extract and Its Constituent, S-Allyl Cysteine, in Rats. Evidence-Based Complementary and Alternative Medicine, 7 p. https://doi.org/10.1155/2015/328545 DOI: https://doi.org/10.1155/2015/328545

Atcha, Z., Rourke, C., Neo, A. H. P., Goh, C. W. H., Lim, J. S. K., Aw, C. C., Browne, E. R., Pemberton, D. J. 2010. Alternative Method of Oral Dosing for Rats. Journal of the American Association for Laboratory Animal Science, vol. 49, no. 3, p. 335-343.

Bae, S. E., Cho, S. Y., Won, Y. D., Lee, S. H., Park, H. J. 2014. Changes in S-Allyl cysteine contents and physicochemical properties of black garlic during heat treatment. LWT - Food Science and Technology, vol. 55, no. 1, p. 397-402. https://doi.org/10.1016/j.lwt.2013.05.006 DOI: https://doi.org/10.1016/j.lwt.2013.05.006

Chang, W. T., Wu, C. H., Hsu C. L. 2015. Diallyl trisulphide inhibits adipogenesis in 3T3-L1 adipocytes through lipogenesis, fatty acid transport, and fatty acid oxidation pathways. Journal of Functional Foods, vol. 16, p. 414-422. https://doi.org/10.1016/j.jff.2015.05.002 DOI: https://doi.org/10.1016/j.jff.2015.05.002

Chang, W. T., Shiau, D. K., Cheng, M. C., Tseng, C. Y., Chen, C. S., Wu, M. F., Hsu, C. L.2017. Black Garlic Ameliorates Obesity Induced by a High-fat Diet in Rats. Journal of Food and Nutrition Research, vol. 5, no. 10, p. 736-741. https://doi.org/10.12691/jfnr-5-10-3 DOI: https://doi.org/10.12691/jfnr-5-10-3

Chang, H. S., Yamato, O., Yamasaki, M., Maede, Y. 2005. Modulatory influence of sodium 2- propenyl thiosulfate from garlic on cyclooxygenase activity in canine platelets: Possible mechanism for the anti-aggregatory effect. Prostaglandins, Leukotrienes and Essential Fatty Acids,vol.72,no.5,p.351-355. https://doi.org/10.1016/j.plefa.2005.01.003 DOI: https://doi.org/10.1016/j.plefa.2005.01.003

Chen, Y. C., Kao, T. H., Tseng, C. Y., Chang, W. T., Hsu, C. L. 2014. Methanolic extract of black garlic ameliorates diet-induced obesity via regulating adipogenesis, adipokine biosynthesis, and lipolysis. Journal of Functional Foods, vol. 9, p. 98-108. https://doi.org/10.1016/j.jff.2014.02.019 DOI: https://doi.org/10.1016/j.jff.2014.02.019

Crowther, J. R. 2009. The ELISA Guidebook. 2nd ed. New York, USA : Humana Press, 566 p. ISBN 978-1-60327-254-4. https://doi.org/10.1007/978-1-60327-254-4 DOI: https://doi.org/10.1007/978-1-60327-254-4

Darvall, K. A. L., Sam, R. C., Silverman, S. H., Bradbury, A. W., Adam, D. J. 2007. Obesity and Thrombosis. European Journal of Vascular et Endovascular Surgery, vol.33,no.2,p.223-233. https://doi.org/10.1016/j.ejvs.2006.10.006 DOI: https://doi.org/10.1016/j.ejvs.2006.10.006

Dissard, R., Klein, J., Caubet, C., Breuil, B., Siwy, J., Hoffman, J., Sicard, L., Ducassé, L., Rascalou, S., Payre, B., Buléon, M., Mullen, W., Mischak, H., Tack, I., Bascands, J. L., Buffin-Meyer, B., Schanstra, J. P. 2013. Long Term Metabolic Syndrome Induced by a High Fat High Fructose Diet Leads to Minimal Renal Injury in C57BL/6 Mice. PLoS One, vol. 8, no. 1, 14 p. https://doi.org/10.1371/journal.pone.0076703 DOI: https://doi.org/10.1371/journal.pone.0076703

Fakhoury-Sayegh, N., Trak-Smayra, V., Khazzaka, A., Esseily, F., Obeid, O., Lahoud-Zouein, M., Younes, H. 2015. Characteristics of nonalcoholic fatty liver disease induced in wistar rats following four different diets. Nutrition Research and Practice, vol. 9, no. 4, p. 350-357. https://doi.org/10.4162/nrp.2015.9.4.350 DOI: https://doi.org/10.4162/nrp.2015.9.4.350

Festa, A., D'Agostino, R., Mykkänen, L., Tracy, R., Howard, B. V., Haffner, S. M. 1999. Low-Density Lipoprotein Particle Size Is Inversely Related to Plasminogen Activator Inhibitor-1 Levels. The Insulin Resistance Atherosclerosis Study. Arteriosclerosis,Thrombosis, and Vascular Biology, vol. 19, no. 3, p. 605-610. https://doi.org/10.1161/01.ATV.19.3.605 DOI: https://doi.org/10.1161/01.ATV.19.3.605

Francque, S. M., van der Graaff, D., Kwanten, W. J. 2016. Non-alcoholic fatty liver disease and cardiovascular risk: Pathophysiological mechanisms and implications. Journal of Hepatology, vol. 65, no. 2, p. 425-443. https://doi.org/10.1016/j.jhep.2016.04.005 DOI: https://doi.org/10.1016/j.jhep.2016.04.005

Fukao, H., Yoshida, H., Tazawa, Y. I., Hada, T. 2007. Antithrombotic Effects of Odorless Garlic Powder Both in Vitro and in Vivo. Bioscience, Biotechnology and Biochemistry, vol. 71, no. 1, p. 84-90. https://doi.org/10.1271/bbb.60380 DOI: https://doi.org/10.1271/bbb.60380

Ha, A. W., Ying, T., Kim, W. K. 2015. The effects of black garlic (Allium satvium) extracts on lipid metabolism in rats fed a high fat diet. Nutrition Research and Practice, vol. 9, no. 1, p. 30-6. https://doi.org/10.4162/nrp.2015.9.1.30 DOI: https://doi.org/10.4162/nrp.2015.9.1.30

Hardinsyah, M. S., Supariasa, D. N. 2019. Ilmu Gizi Teori dan Aplikasi (Nutritional Science Theory and Application). 4 ed., Indonesia : Medical Book Publisher EGC. (In Indonesian) ISBN 978-979-044-725-7.

Hatton, G. B., Yadav, V., Basit A. W., Merchant, H. A. 2015. Animal Farm: Considerations in Animal Gastrointestinal Physiology and Relevance to Drug Delivery in Humans. Journal of Pharmaceutical Sciences, vol. 104, no. 9, p. 2747-2776. https://doi.org/10.1002/jps.24365 DOI: https://doi.org/10.1002/jps.24365

Jarukamjorn, K., Jearapong, N., Pimson, C., Chatuphonprasert, W. 2016. A High-Fat, High-Fructose Diet Induces Antioxidant Imbalance and Increases the Risk and Progression of Nonalcoholic Fatty Liver Disease in Mice. Scientifica, 10 p. https://doi.org/10.1155/2016/5029414 DOI: https://doi.org/10.1155/2016/5029414

Jung, Y. M., Lee, S. H., Lee, D. S., You, M. J., Chung, I. K., Cheon, W. H., Kwon, Y. S., Lee, Y. J., Ku, S. K. 2011. Fermented garlic protects diabetic, obese mice when fed a high-fat diet by antioxidant effects. Nutrition Research, vol. 31, no. 5, p. 387-396. https://doi.org/10.1016/j.nutres.2011.04.005 DOI: https://doi.org/10.1016/j.nutres.2011.04.005

Kim, D., Choi, S. Y., Park, E. H., Lee, W., Kang , J. H., Kim, W., Kim, Y. J., Yoon, J. H., Jeong, S. H., Lee, D. H., Lee, H. S., Larson, J., Therneau, T. M., Kim, W. R. 2012. Nonalcoholic fatty liver disease is associated with coronary artery calcification. Hepatology, vol. 56, no. 2, p. 605-613. https://doi.org/10.1002/hep.25593 DOI: https://doi.org/10.1002/hep.25593

Kim, I., Kim, J. Y ., Hwang, Y. J., Hwang, K. A., Om, A. S., Kim, J. H., Cho, K. J. 2011. The beneficial effects of aged black garlic extract on obesity and hyperlipidemia in rats fed a high-fat diet. Journal of Medicinal Plants. Research, vol. 5, no. 14, p. 3159-3168.

Lee, S. J., Kim, R. J., Ryu, J. H., Shin, J. H., Kang, M. J., Kim, I. S., Sung, N. J. 2011. Effects of the Red Garlic Extract for Anti-Obesity and Hypolipidemic in Obese Rats Induced High Fat Diet. Journal of Life Science, vol. 21,no.2,p.211-220. https://doi.org/10.5352/JLS.2011.21.2.211 DOI: https://doi.org/10.5352/JLS.2011.21.2.211

Mazza, A., Fruci, B., Garinis, G. A., Giuliano, S., Malaguarnera, R., Belfiore, A. 2012. The Role of Metformin in the Management of NAFLD. Journal of Diabetes Research, 13 p. https://doi.org/10.1155/2012/716404 DOI: https://doi.org/10.1155/2012/716404

McPherson, R. A., Pincus, M. R. 2016. Henry’s Clinical and Management by Laboratory Methods. 23rd ed. Canada, US : Elsevier, 433 p. ISBN 978-0323413152.

Nascimbeni, F., Aron-Wisnewsky, J., Pais, R., Tordjman, J., Poitou, C., Charlotte, F., Bedossa, P., Ponyard, T., Clément, K., Ratziu, V. 2016. Statins, Antidiabetic Medications And Liver Histology In Patients With Diabetes With Non-alcoholic Fatty Liver Disease. BMJ Open Gastroenterology, vol. 3, no. 1, 9 p. https://doi.org/10.1136/bmjgast-2015-000075 DOI: https://doi.org/10.1136/bmjgast-2015-000075

Oligschlaeger, Y., Shiri-Sverdlov, R. 2020. NAFLD Preclinical Models: More than a Handful, Less of a Concern? Biomedicines, vol. 8, no. 2, 23 p. https://doi.org/10.3390/biomedicines8020028 DOI: https://doi.org/10.3390/biomedicines8020028

Rodrigues, G., Moreira, A. J., Bona, S., Schemitt, E., Marroni, C. A., Di Naso F. C., Dias, A. S., Pires, T. R., Picada, J. N., Marroni, N. P. 2019. Simvastatin Reduces Hepatic Oxidative Stress And Endoplasmic Reticulum Stress In Nonalcoholic Steatohepatitis Experimental Model. Oxidative Medicine And Cellular Longevity, 10 p. https://doi.org/10.1155/2019/3201873 DOI: https://doi.org/10.1155/2019/3201873

Rivlin, R. S. 2001. Historical Perspective on the Use of Garlic. The Journal of Nutrition, vol. 131, no. 3, p. 951S-954S. https://doi.org/10.1093/jn/131.3.951S DOI: https://doi.org/10.1093/jn/131.3.951S

Sasaki, J., Lu, C., Machiya, E., Tanahashi, M., Hamada, K. 2007. Processed Black Garlic (Allium sativum) Extracts Enhance Anti-Tumor Potency against Mouse Tumors. Medicinal and Aromatic Plant Science and Biotechnology, vol. 1, no. 2, p. 278-281.

Sato, E., Kohno, M., Niwano, Y. 2006. Increased level of tetrahydro-b-carbolinen derivatives in short-term fermented garlic, Plant Foods for Human Nutrition, vol. 61, no. 4, p. 175-178. https://doi.org/10.1007/s11130-006-0028-2 DOI: https://doi.org/10.1007/s11130-006-0028-2

Seo, Y. J., Gweon, O. C., Im, J., Lee, Y. M., Kang, M. J., Kim, J. I. 2009. Effect of Garlic and Aged Black Garlic on Hyperglycemia and Dyslipidemia in Animal Model of Type 2 Diabetes Mellitus. Journal of Food Science and Nutrition, vol. 14, no. 1, p. 1-7. https://doi.org/10.3746/jfn.2009.14.1.001 DOI: https://doi.org/10.3746/jfn.2009.14.1.001

Sobenin, I. A., Myasoedova, V. A., Iltchuk, M. I., Zhang, D. W., Orekhov, A. N. 2019. Therapeutic effects of garlic in cardiovascular atherosclerotic disease. Chinese Journal of Natural Medicines, vol. 17, no. 10, p. 721-728.https://doi.org/10.1016/S1875-5364(19)30088-3 DOI: https://doi.org/10.1016/S1875-5364(19)30088-3

Somodi, S., Seres, I., Lőrincz, H., Harangi, M., Fülöp, P., Paragh, G. 2018. Plasminogen Activator Inhibitor-1 Level Correlates with Lipoprotein Subfractions in Obese Nondiabetic Subjects. International Journal of Endocrinology,vol.2018,9p. https://doi.org/10.1155/2018/9596054 DOI: https://doi.org/10.1155/2018/9596054

Szulińska, M., Kręgielska-Narożna, M., Świątek, J., Styś, P., Kuźnar-Kamińska, B., Jakubowski, H., Walkowiak, J., Bogdański, P. 2018. Garlic extract favorably modifies markers of endothelial function in obese patients – randomized double blind placebo-controlled nutritional intervention. Biomedicine and Pharmacotherapy, vol. 102, p. 792-797. https://doi.org/10.1016/j.biopha.2018.03.131 DOI: https://doi.org/10.1016/j.biopha.2018.03.131

Teranishi, K., Apitz-Castro, R., Robson, S. C., Romano, E., Cooper, K. C. 2003. Inhibition of baboon platelet aggregation in vitro and in vivo by the garlic derivative, ajoene. Xenotransplantation, vol. 10, no. 4, p. 374-379. https://doi.org/10.1034/j.1399-3089.2003.02068.x DOI: https://doi.org/10.1034/j.1399-3089.2003.02068.x

Toledano Medina, M. Á., Merinas-Amo, T., Fernández-Bedmar, Z., Font, R., del Río-Celestino, M., Pérez-Aparicio, J., Moreno-Ortega, A., Alonso-Moraga, Á., Moreno-Rojas, R. 2019. Physicochemical Characterization and Biological Activities of Black and White Garlic: In Vivo and In Vitro Assays. Foods, vol. 8, no. 6, 18 p.https://doi.org/10.3390/foods8060220 DOI: https://doi.org/10.3390/foods8060220

Tran, G. B., Dam, S. M., Tram Le, N. T. 2018. Amelioration of Single Clove Black Garlic Aqueous Extract on Dyslipidemia and Hepatitis in Chronic Carbon Tetrachloride Intoxicated Swiss Albino Mice. International Journal of Hepatology, vol. 2018, 9 p. https://doi.org/10.1155/2018/9383950 DOI: https://doi.org/10.1155/2018/9383950

Tomita, K., Teratani, T., Suzuki, T., Shimizu, M., Sato, H., Narimatsu, K., Okada, Y., Kurihara, C., Irie, R., Yokoyama, H., Shimamura, K., Usui, S., Ebinuma, H., Saito, H., Watanabe, C., Komoto, S., Kawaguchi, A., Nagao, S., Sugiyama, K., Hokari, R., Kanai, T., Miura, S., Hibi, T. 2014. Free cholesterol accumulation in hepatic stellate cells: Mechanism of liver fibrosis aggravation in nonalcoholic steatohepatitis in mice. Hepatology, vol. 59, no. 1, p. 154-169. https://doi.org/10.1002/hep.26604 DOI: https://doi.org/10.1002/hep.26604

Väisänen, S., Baumstark, M. W., Penttilä, I., Bouchard, C., Halonen, P., Rankinen, T., Berg, A., Rauramaa, R. 1997. Small, Dense LDL Particle Concentration Correlates with Plasminogen Activator Inhibitor Type-1 (PAI-1) Activity. Thrombosis and Haemostasis, vol. 78, no. 6, p. 1495-1499. https://doi.org/10.1055/s-0038-1665440 DOI: https://doi.org/10.1055/s-0038-1665440

Wolforth, J. B. 2000. Methods of Blood Collection in The Mouse. Lab Animal, vol. 29, no. 10, p. 47-53.

Wong, S. K., Chin, K. Y., Suhaimi, F. H., Fairus, A., Ima-Nirwana, S. 2016. Animal models of metabolic syndrome: a review. Nutrition and Metabolism, vol. 13, 12 p. https://doi.org/10.1055/s-0038-1665440 DOI: https://doi.org/10.1186/s12986-016-0123-9

Published

2021-04-28

How to Cite

Nurmawati, L., Sulchan, M., Fatimah-Muis, S., Djagat Purnomo, H., Djamiatun, K., Ardiaria, M., & Karlowee, V. (2021). The effect of single clove Black garlic on the hemostasis status and lipid profile in male Sprague Dawley rats with non-alcoholic fatty liver disease. Potravinarstvo Slovak Journal of Food Sciences, 15, 387–395. https://doi.org/10.5219/1516

Most read articles by the same author(s)