The effect of Sorghum Tempeh (Sorghum bicolor L. Moench) on low-density lipoprotein (LDL) and malondialdehyde (MDA) levels in atherogenic diet-induced rats

Authors

  • Ana Khoirun Nisa Diponegoro University, Faculty of Medicine, Department of Nutrition, Tembalang, 50275, Semarang, Indonesia, Tel.: +6282131515799 https://orcid.org/0000-0003-4874-8643
  • Diana Nur Afifah Diponegoro University, Faculty of Medicine, Department of Nutrition, Tembalang, 50275, Semarang, Indonesia, Tel.: +6287770380468 https://orcid.org/0000-0001-8808-1826
  • Kis Djamiatun Diponegoro University, Faculty of Medicine, Department of Nutrition, Tembalang, 50275, Semarang, Indonesia, Tel.: +6281390351351 https://orcid.org/0000-0002-0498-8808
  • Ahmad Syauqy Diponegoro University, Faculty of Medicine, Department of Nutrition, Tembalang, 50275, Semarang, Indonesia, Tel.: +886979040064 https://orcid.org/0000-0002-9552-2834

DOI:

https://doi.org/10.5219/1589

Keywords:

sorghum tempeh, sorghum flour, LDL, MDA, atherosclerosis

Abstract

An atherogenic diet induces oxidative stress leading to hypercholesterolemia. This condition causes atherosclerosis followed by increased LDL and MDA. Sorghum tempeh contains fiber and antioxidants that can protectively improve LDL and MDA levels. Therefore, this research aims to determine the effect of sorghum tempeh on LDL and MDA levels in atherogenic diet-induced rats compared to sorghum flour. It used a randomized pre-post test with a control group design. The test subjects were 30 male Sprague Dawley rats, consisting of 6 normal conditioned rats (C1), and 24 that were induced by an atherogenic diet (C2, T1, T2, T3) for 2 weeks. Sorghum flour was administered at a dose of 4.095 g (T1) and the sorghum tempeh at 3.041 g (T2) and 6.081 g (T3) for 4 weeks. Furthermore, C2 was constantly induced through an atherogenic diet. Total cholesterol and LDL levels were then analyzed using the CHOD-PAP method, and MDA levels, using the ELISA method. Meanwhile, statistical analysis for these variables was carried out using IBM SPSS Statistics 21 software. The results showed that the administration of sorghum flour and tempeh significantly reduced total cholesterol, LDL, MDA levels in each group (p = 0.001). Furthermore, it showed that there was a significantly strong correlation between LDL and MDA levels before and after treatment (r = 0.610, r = 0.805, and p = 0.001). The administration of sorghum tempeh at a dose of 6.081 g caused the greatest reduction (∆) in LDL levels at -44.19 ±2.58 mg.dL-1, although, it was not the same as normal control. Meanwhile, sorghum flour at a dose of 4.095 g was the most influential in reducing MDA levels to the same as normal control with delta (∆) at -7.67 ±0.37 ng.mL-1. In conclusion, sorghum tempeh and flour were the most effective at reducing LDL and MDA levels, respectively.

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References

Afify, A. E. M. R., El-Beltagi, H. S., El-Salam, S. M. A., Omran, A. A. 2012. Biochemical changes in phenols, flavonoids, tannins, vitamin E, β-carotene and antioxidant activity during soaking of three white sorghum varieties. Asian Pacific Journal of Tropical Biomedicine, vol. 2, no. 3, p. 203-209. https://doi.org/10.1016/S2221-1691(12)60042-2

Akyol, S., Lu, J., Akyol, O., Akcay, F., Armutcu, F., Ke, L. Y., Chen, C. H. 2017. The role of electronegative low-density lipoprotein in cardiovascular diseases and its therapeutic implications. Trends in Cardiovascular Medicine, vol. 27, no. 4, p. 239-246. https://doi.org/10.1016/j.tcm.2016.11.002

Chen, Y., Xu, C., Huang, R., Song, J., Li, D., Xia, M. 2018. Butyrate from pectin fermentation inhibits intestinal cholesterol absorption and attenuates atherosclerosis in apolipoprotein E-deficient mice. Journal of Nutritional Biochemistry, vol. 56, p. 175-182. https://doi.org/10.1016/j.jnutbio.2018.02.011

Cruz, R. A. O., López, J. L. C., Aguilar, G. A. G., García, H. A., Gorinstein, S., Romero, R. C., Sánchez, M. R. 2015. Influence of Sorghum Kafirin on Serum Lipid Profile and Antioxidant Activity in Hyperlipidemic Rats (In Vitro and In Vivo Studies). BioMed Research International, vol. 2015, 8 p. https://doi.org/10.1155/2015/164725

Czerska, M., Mikołajewska, K., Zieliński, M., Gromadzińska, J., Wąsowicz, W. 2015. Today’s Oxidative Stress Markers. Medycyna Pracy, vol. 66, no. 3, p. 393-405. https://doi.org/10.13075/mp.5893.00137

Dimidi, E., Cox, S. R., Rossi, M., Whelan, K. 2019. Fermented Foods: Definitions and Characteristics, Impact on the Gut Microbiota and Effects on Gastrointestinal Health and Disease. Nutrients, vol. 11, no. 8, 26 p. https://doi.org/10.3390/nu11081806

Dykes, L. 2019. Sorghum Phytochemicals and Their Potential Impact on Human Health. In Zhao, Z. Y., Dahlberg, J. Shorgum. Methods in Molecular Biology. New York, USA : Humana Press, vol. 1931, p. 121-140. ISBN: 978-1-4939-9039-9. https://doi.org/10.1007/978-1-4939-9039-9_9

Ermawar, R. A., Collins, H. M., Byrt, C. S., Betts, N. S, Henderson, M., Shirley, N. J., Schwerdt, J., Lahnstein, J., Fincher G. B., Burton, R. A. 2015. Distribution, structure and biosyntetic gene families of (1,3;1,4) Gen cellulose synthase-like (Csl) pada (1,3;1,4)-β-glucan in Shorgum bicolor. Journal of Integrative Plant Biology, vol. 57, no. 4, p. 429-445. https://doi.org/10.1111/jipb.12338

Endrawati, D., Kusumaningtyas, E. 2017. Beberapa Fungsi Rhizopus sp dalam Meningkatkan Nilai Nutrisi Bahan Pakan (Several Functions of Rhizopus sp on Inceasing Nutritional Value of Feed Ingredient). Wartazoa, vol. 27, no. 2, p. 081-088. (In Indonesia) https://doi.org/10.14334/wartazoa.v27i2.1181

Espitia-Hernández, P., González, M. L. C., Ascacio-Valdés, J. A., Dávila-Medina, D., Flores-Naveda, A., Silva, T., Chacón, X. R., Sepúlveda, L. 2020. Sorghum (Sorghum bicolor L.) as a potential source of bioactive substances and their biological properties. Critical Reviews in Food Science and Nutrition, 12 p. https://doi.org/10.1080/10408398.2020.1852389

Estruch, M., Sanchez-Quesada, J. L., Ordoñez-Llanos, J., Benitez, S. 2016. Inflammatory Intracellular Pathways Activated by Electronegative LDL in Monocytes. Molecular and Cell Biology of Lipids, vol. 1861, no. 9, p. 963-969. https://doi.org/10.1016/j.bbalip.2016.05.010

Feingold, K. R. 2000. Introduction to Lipids and Lipoproteins. In Feingold K. R., Anawalt, B., Boyce, A, et al. Endotext : Comprehensive Free Online Endocrinology Book. South Dartmouth, USA : MDText.com, Inc, p. 1-46. Bookshelf ID: NBK278943.

Gisterå, A., Hansson, G. K. 2017. The immunology of atherosclerosis. Nature Reviews Nephrology, vol. 13, no. 6, p. 368-380. https://doi.org/10.1038/nrneph.2017.51

Hartanti, A. T., Rahayu, G., Hidayat, I. 2015. Rhizopus Species from Fresh Tempeh Collected from Several Regions in Indonesia. HAYATI Journal of Biosciences, vol. 22, no. 3, p. 136-142. https://doi.org/10.1016/j.hjb.2015.10.004

Harun, I., Susanto, H., Rosidi, A. 2017. Pemberian Tempe Menurunkan Kadar Malondialdehyde (MDA) dan Meningkatkan Aktivitas Enzim Superoxide Dismutase (SOD) pada Tikus dengan Aktivitas Fisik Tinggi (The tempe giving decrease malondialdehyde (MDA) level and increase the activities of superoxide dismutase enzyme (SOD) on rats with high physical activities). Jurnal Gizi Pangan, vol. 12, no. 3, p. 211-216. (In Indonesia) https://doi.org/10.25182/jgp.2017.12.3.211-216

Hasanuzzaman, M., Borhannuddin Bhuyan, M. H. M., Zulfiqar, F., Raza, A., Mohsin, S. M., Malmud, J. A., Fujita, M., Fotopoulos, V. 2020. Reactive Oxygen Spesies and Antioxidant Defense in Plants under Abiotis Stress: Revisiting the Crucial Role of a Universal Defense Regulator. Antioxidants, vol. 9, no. 8, 52 p. https://doi.org/10.3390/antiox9080681

Ho, H. V. T., Sievenpiper, J. L., Zurbau, A., Mejia, S. B., Jovanovski, E., Au-Yeung, F., Jenkins, A. L., Vuksan, V. 2016. The effect of oat β-glucan on LDL-cholesterol, non-HDL-cholesterol and apoB for CVD risk reduction : a systematic review and meta-analysis of randomised-controlled trials. British Journal of Nutrition, vol. 116, no. 8, p. 1369-1382. https://doi.org/10.1017/S000711451600341X

Hu, S., Kuwabara, R., de Haan, B. J, Smink, A. M., de Vos, P. 2020. Acetate and Butyrate Improve β-cell Metabolism and Mitochondrial Respiration under Oxidative Stress. International Journal of Molecular Science, vol. 21, 17 p. https://doi.org/10.3390/ijms21041542

Huang, Y. C., Wu, B. H., Chu, Y. L., Chang, W. C., Wu, M. C. 2018. Effects of Tempeh Fermentation with Lactobacillus plantarum and Rhizopus oligosporus on StreptozotocinInduced Type II Diabetes Mellitus in Rats. nutrients. 2018, vol. 10, no. 1143, p. 1–15. https://doi.org/10.3390/nu10091143

Hur, J., Nguyen, T. T. H., Park, N., Kim, J., Kim, D. 2018. Characterization of quinoa (Chenopodium quinoa) fermented by Rhizopus oligosporus and its bioactive properties. AMB Express, vol. 8, 8 p. https://doi.org/10.1186/s13568-018-0675-3

ISO 9001:2008. 2008. Quality management systems – Requirements.

ISO 13485:2003. Medical devices – Quality management systems – Requirements for regulatory purposes.

Kaida, H., Tahara, N., Tahara, A., Honda, A., Nitta, Y., Igata, S., Ishibashi, M., Yamagishi, S. I., Fukumoto, Y. 2014. Positive correlation between malondialdehyde-modified low-density lipoprotein cholesterol and vascular inflammation evaluated by 18F-FDG PET/CT. Atherosclerosis, vol. 237, no. 2, p. 404-409. https://doi.org/10.1016/j.atherosclerosis.2014.10.001

Kurniasari, R., Sulchan, M., Afifah, D. N., Anjani, G., Rustanti, N. 2017. Influence Variation of Tempe Gembus (An Indonesian Fermented Food) on Homocystein and Malondialdehyde of Rats Fed An Atherogenic Diet. Romanian Journal of Diabetes Nutrition & Metabolic Diseases, vol. 24, no. 3, p. 204-211. https://doi.org/10.1515/rjdnmd-2017-0026

Laleye, S. A., Aderiye, B. I., David O. M. 2016. Hypolipidemic Activity of Fermented Sorghum (Sorghum bicolor L. Moench) Gruel (Ogi) in Hypercholesterolemic Rats (Rattus nervegicus). International Journal of Biochemistry Research & Review, vol. 9, no. 1, p. 1-15. https://doi.org/10.9734/IJBCRR/2016/19659

Lee, J., Jung, S., Kim, N., Shin, M. J., Ryu, D. H., Hwang, G. S. 2017. Myocardial metabolic alterations in mice with diet-induced atherosclerosis: linking sulfur amino acid and lipid metabolism. Scientific Reports, vol. 7, p. 1-13. https://doi.org/10.1038/s41598-017-13991-z

Liu, H., Huang, L., Pei, X. 2021. Effects of sorghum rice and black rice on genes associated with cholesterol metabolism in hypercholesterolemic mice liver and intestine. Food Science and Nutrition, vol. 9, no. 1, p. 217-229. https://doi.org/10.1002/fsn3.1986

Liu, Y., Ragaee, S., Marcone, M. F., Abdel-Aal, E. S. M. 2020. Composition of Phenolic Acids and Antioxidant Properties of Selected Pulses Cooked with Different Heating Conditions. Foods, vol. 9, no. 7, 18 p. https://doi.org/10.3390/foods9070908

Marchio, P., Guerra-Ojeda, S., Vila, J. M., Aldasoro, M., Victor, V. M., Mauricio, M. D. 2019. Targeting Early Atherosclerosis: A Focus on Oxidative Stress and Inflammation. Oxidative Medicine and Cellular Longevity, vol. 2019, 32 p. https://doi.org/10.1155/2019/8563845

Matsuo, M. 2005. In Vivo Antioxidant Activity of Methanol Extract from Quinoa Fermented with Rhizopus oligosporus. Journal of Nutritional Science and Vitaminology, vol. 51, no. 6, p. 449-452. https://doi.org/10.3177/jnsv.51.449

Papac-Milicevic, N., Busch, C. J. L., Binder, C. J. 2016. Malondialdehyde epitopes as targets of immunity and the implications for atherosclerosis. Advances in Immunology, vol. 131, p. 1-59. https://doi.org/10.1016/bs.ai.2016.02.001

NCEP. 2001. ATP III Guidelines At-A-Glance Quick Desk Reference. In 2013 ACC/AHA Guideline on the Treatment of Blood Cholesterol to Reduce Atherosclerotic Cardiobascular Risk in Adults. National Heart, Lung, and Blood Institute (NHLBI).

Ohira, H., Tsutsui, W., Fujioka, Y. 2017. Are Short Chain Fatty Acids in Gut Microbiota Defensive Players for Inflammation and Atherosclerosis? Journal of Atherosclerosis and Thrombosis, vol. 24, no. 7, p. 660-672. https://doi.org/10.5551/jat.RV17006

Pirillo, A., Bonacina, F., Norata, G. D., Catapano, A. L. 2018. The Interplay of Lipids, Lipoproteins, and Immunity in Atherosclerosis. Current Atherosclerosis Reports, vol. 20, 9 p. https://doi.org/10.1007/s11883-018-0715-0

Pisoschi, A. M., Pop, A. 2015. The role of antioxidants in the chemistry of oxidative stress: A review. European Journal of Medicinal Chemistry, vol. 97, p. 55-74. https://doi.org/10.1016/j.ejmech.2015.04.040

Ramatoulaye, F., Mady, C., Fallou, S., Amadou, K., Cyril, D., Massamba D. 2016. Production and Use Sorghum: A Literature Review. Journal of Nutritional Health and Food Science, vol. 4, no. 1, p. 1-4. https://doi.org/10.15226/jnhfs.2016.00157

Ratnasari, M., Santosa, A., Rachmawati, D. A. 2018. The Correlation between Fat Consumption and Atherogenic Index on Type 2 Diabetes Mellitus Patients in dr.Soebandi Hospital. Journal of Agromedicine and Medical Sciences, vol. 4, no. 1, p. 7-12. https://doi.org/10.19184/ams.v4i1.6317

Salazar-López, N. J., Gonzáles-Aguilar, G., Rouzaud-Sández, O., Robles-Sánchez, M. 2018. Technologies applied to sorghum (Sorghum bicolor L.Moench) : changes in phenolic compounds and antioxidant capacity. Food Science and Technology, vol. 38, no. 3, 14 p. https://doi.org/10.1590/fst.16017

Salvayre, R., Negre-Salvayre, A., Camaré, C. 2016. Oxidative theory of atherosclerosis and antioxidants. Biochimie, vol. 125, p. 281-296. https://doi.org/10.1016/j.biochi.2015.12.014

Şanlier, N., Gökcen, B. B., Sezgin, A. C. 2019. Health benefits of fermented foods. Critical Reviews in Food Science and Nutrition, vol. 59, no. 3, p. 506-527. https://doi.org/10.1080/10408398.2017.1383355

Silva, T. L., Lacerda, U. V., da Matta, S. L. P., Queiroz, V. A. V., Stringheta, P. C., Martino, H. S. D., Ribeiro de Barros, F. A. 2020. Evaluation of the efficacy of toasted white and tannin sorghum fluors to improve oxidative stress and lipid profile in vivo. Journal of Food Science, vol. 85, no. 7, p. 2236-2244. https://doi.org/10.1111/1750-3841.15301

Sun, Y., Wang, Y., Song, P., Wang, H., Xu, N., Wang, Y., Zhang, Z., Yue, P., Gao, X. 2019. Anti-obesity effects of instant fermented teas in vitro and in mice with high-fat-diet-induced obesity. Food & Function, vol. 10, no. 6, p. 3502-3513. https://doi.org/10.1039/C9FO00162J

Tan, B. L., Norhaizan, M. E., Liew, W. P. P. 2018. Nutrients and Oxidative Stress: Friend or Foe? Oxidative Medicine and Cellular Longevity, vol. 2018, 24 p. https://doi.org/10.1155/2018/9719584

Tian, X., Yu, Q., Wu, W., Dai, R. 2018. Inactivation of Microorganisms in Foods by Ohmic Heating: A Review. Journal of Food Protection, vol. 81, no. 7, p. 1093-1107. https://doi.org/10.4315/0362-028X.JFP-17-343

Tsikas, D. 2017. Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: Analytical and biological challenges. Analytical Biochemistry, vol. 524, p. 13-30. https://doi.org/10.1016/j.ab.2016.10.021

Verni, M., Verardo, V., Rizzello, C. G. 2019. How Fermentation Affects the Antioxidant Properties of Cereals and Legumes. Foods, vol. 8, no. 9, 21 p. https://doi.org/10.3390/foods8090362

Yamada, S., Kawaguchi, H., Yamada, T., Guo, X., Matsuo, K., Hamada, T., Miura, N., Tasaki, T., Tanimoto, A. 2017. Cholid Acid Enhaces Visceral Adiposity, Atherosclerosis and Nonalcoholic Fatty Liver Disease in Microminipigs. Journal of Atherosclerosis and Thrombosis, vol. 24, no. 11, p. 1150-1166. https://doi.org/10.5551/jat.39909

Zakaria, F. R., Prangdimurti, E., Puspawati, K. D, Thahir, R., Suismono. 2011. Diet Berbasis Sorgum (Sorghum bicolor L Moench) Memperbaiki Proliferasi Limfosit Limfa dan Kapasitas Antioksidan Hati Tikus (Sorghum-Based Diet (Sorghum bicolor L Moench) Improves Lymphocyte Proliferation and Antioxidant Capacity of Rat Liver). Pangan, vol. 20, no. 3, p. 209-222. (In Indonesia) https://doi.org/10.33964/jp.v20i3.155

Zárate, A., Manuel-Apolinar, L., Basurto, L., De la Chesnaye, E., Saldívar, I. 2016. Colesterol y aterosclerosis. Consideraciones históricas y tratamiento (Cholesterol and atherosclerosis. Historical considerations and treatment). Archivos de Cardiologia de Mexico, vol. 86, no. 2, p. 163-169. (In Spanish) https://doi.org/10.1016/j.acmx.2015.12.002

Published

2021-09-28

How to Cite

Khoirun Nisa, A. ., Afifah, D. N., Djamiatun, K., & Syauqy, A. (2021). The effect of Sorghum Tempeh (Sorghum bicolor L. Moench) on low-density lipoprotein (LDL) and malondialdehyde (MDA) levels in atherogenic diet-induced rats . Potravinarstvo Slovak Journal of Food Sciences, 15, 662–671. https://doi.org/10.5219/1589

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