Study of Fermented Food Intervention on the Serum Lipid Profile of Hypercholesterolemia Animals Trial (Meta-analysis)
DOI:
https://doi.org/10.22437/ifstj.v8i2.36353Keywords:
Fermented, food, hypercholesterolemia, in vivo, lipidAbstract
Abstract— Individuals with hypercholesterolemia (HC) require specific therapy, such as statin medication, to maintain their blood lipid profile (total cholesterol, triglycerides, HDL-C, LDL-C) within the normal range. In vivo, studies have shown that consuming fermented foods for a particular duration can help improve the blood lipid profile of HC animal models. However, meta-analysis studies have not investigated which type of fermented food has the most significant effect on improving the blood lipid profile. The studies included were in vivo research that examined the effects of fermented food interventions on improving the blood lipid profile in HC animal models. The results of this study indicate that fermented food interventions (both plant-based and animal-based) have a highly significant effect (p-value <0.001) on improving the blood lipid profile compared to the HC animal model group without intervention. However, the plant-based fermented food source group tends to show a more significant effect on lipid profiles than those sourced from animals.
Downloads
References
[1] DA. Natalia, Sugiyarto, E. Darmawan. Side Effects of Hypoglycemic Experienced by Geriatric Patients Who are at Risk of Metabolic Syndrome. J Sains Kes 2022, vol 4 no 4. doi: 10.25026/jsk.v4i4.1282
[2] P. Mumthaj, P. Natarajan, AM. Janani, J. Vijay, V. Gokul. A Global Review Article on Hyperlipidemia. Int. J. Pharm. Sci. Rev Res 2021, vol 68(1), pp: 104-110. doi: 10.47583/ijpsrr.2021.v68i01.018
[3] MG. Saklayen. The Global Epidemic of the Metabolic Syndrome. Current Hypertension Reports 2018, vol 20:12. doi: 10.1007/s11906-018-0812-z.
[4] Association of Indonesian Endocrinology - Perkumpulan Endokrinologi Indonesia (PERKENI). Guidelines for Management of Dyslipidemia in Indonesia 2019.
[5] A. Pirillo, GD. Norata. The burden of hypercholesterolemia and ischemic heart disease in an ageing world. Pharmacological Research 2023, vol 193 (106814). doi: 10.1016/j.phrs.2023.106814
[6] G. Deveci, E. Çelik, D. A˘gagündüz, E. Bartkiene, JMF, Rocha, F. Özogul. Certain Fermented Foods and Their Possible Health Effects with a Focus on Bioactive Compounds and Microorganisms. Fermentation 2023, vol 9 no 923. doi: 10.3390/fermentation9110923
[7] M. Astawan, T. Wresdiyati, Suliantari, II. Arief II, R. Septiawan. Production of synbiotic yogurt-like using indigenous lactic acid bacteria as functional food. Journal of Animal Science and Technology 2012, vol 35, no 1, pp: 9-14. doi: 10.5398/medpet.2012.35.1.9
[8] M. Kobayashi, S. Egusa, M. Fukuda. Isoflavone and Protein Constituents of Lactic Acid-Fermented Soy Milk Combine to Prevent Dyslipidemia in Rats Fed a High Cholesterol Diet. Nutrients 2014, vol 6, pp: 5704-5723. doi: 10.3390/nu6125704
[9] T. Kameda, H. Aoki, Y. Yang, DE. Nirmagustina, A. Iwamoto, T. Kumrungsee, N. Kato, N. Yanaka. Beneficial Effects of Dietary Tempeh Prepared with Rhizopus stolonifera on Liver Funtion in Rats Fed with a High Fat Diet. J Nutr. Sci. Vitaminol 2018, Vol 64, pp: 379-383. doi: 10.3177/jnsv.64.379
[10] R. Yang, C. Wang, H. Ye, F. Gao, J. Cheng, T. Zhang, M. Guo. Effects of feeding hyperlipidemia rats with symbiotic oat-based frozen yogurt on serum triglycerides and cholesterol. Wiley Food Science and Nutrition 2018, vol 7, pp: 1096-1103. doi: 10.1002/fsn3.949
[11] AI. Aji, NE. Suyatma, M. Arpah, A. Jayanegara,. Evaluation of different parameters of zinc oxide nanoparticles on bionanocomposite film properties: a meta-analysis. IJFS 2022. doi: 10.1111/ijfs.16226
[12] Yang. L, Junrui. W, ChengXu. C, XinYuan. Z, XueTing. S, Rina W. Effects of skim milk fermented with Lactobacillus plantarum WW on the constitutions of rats fed a high-fat diet. J. Dairy Sci 2020, vol 103, pp: 5019-5029. doi: 10.3168/jds.2019-17560
[13] AM. Martone, F. Landi, L. Petricca, A. Paglionico, R. Liperoti, MS. Cipriani, F. Ciciarello, S. Rocchi, R. Calvani, A. Picca, E. Marzetti, L. Santoro. Prevalence of dyslipidemia and hypercholesterolemia awareness: results from the Lookup 71 online project. European Journal of Public Health 2022, vol 32 no 3, pp: 402-407. doi: 10.1093/eurpub/ckab224
[14] E. Jung, SY. Kong, YS. Ro, HH. Ryu, SD. Shin. Serum Cholesterol Levels and Risk of Cardiovascular Death: A Systematic Review Dorgand a Dose-Response Meta-Analysis of Prospective Cohort Studies. Int. J. Environ. Res. Public Health 2022, vol 19 no 8272. doi: 10.3390/ijerph19148272
[15] HH. Wang, G. Garruti, M. Liu, P. Portincasa, DQH. Wang DQH. Cholesterol and Lipoprotein Metabolism and Atherosclerosis: Recent Advances in Reverse Cholesterol Transport. Hepatology 2017, vol 16, Suppl.1, pp: s27-s42. doi: 10.5604/01.3001.0010.5495
[16] P. Putnik 1, JM. Lorenzo, FJ. Barba, S. Roohinejad, AR. Jambrak, D. Granato, D. Montesano, DB. Kovaˇcevi´c,. Novel Food Processing and Extraction Technologies of High-Added Value Compounds from Plant Materials. Foods 2018, vol 7 no 106. doi: 10.3390/foods7070106
[17] AO. Obadina, OJ. Akinola, TA. Shittu, HA. Bakare. Effect of Natural Fermentation on the Chemical and Nutritional Composition of Fermented Soymilk Nono. NIFOJ 2013, vol 31 no 2, pp: 91-97. doi: 10.1016/S0189-7241(15)30081-3
[18] DD. Ramdath, EMT. Padhi, S. Sarfaraz, S. Renwick, AM. Duncan. Beyond the Cholesterol-Lowering Effect of Soy Protein: A Review of the Effects of Dietary Soy and Its Constituents on Risk Factors for Cardiovascular Disease. MDPI Nutrients 2017 vol 9 no 324. doi: 10.3390/nu9040324
[19] GR. Caponio, DQH. Wang, AD. Ciaula, MDAP. Portincasa. Regulation of Cholesterol Metabolism by Bioactive Components of Soy Proteins: Novel Translational Evidence. MDPI. e. Int. J. Mol. Sci 2020, vol 22 no 227. doi: 10.3390/ijms22010227.
[20] JS. Han, JY. Joung, HW. Kim, JH. Kim, HS. Choi, HJ. Bae, JH. Jang, NS. Oh. Enhanced Cholesterol-Lowering and Antioxidant Activities of Soymilk by Fermentation with Lactiplantibacillus plantarum KML06. J. Microbiol. Biotechnol 2023, vol 33 no 11, pp: 1475-1483. doi: 10.3390/ijms22010227.
[21] M. Astawan, AP. Cahyani, T. Wresdiyati. Antioxidant activity and isoflavone content of overripe Indonesian tempe. Food Research 2023, vol 7 (Suppl. 1), pp: 42 – 50. doi: 10.26656/fr.2017.7(S1).16
[22] R. Chadha, Y. Bhalla, AJ. Jain, K. Chadha, M. Karan. Dietary Soy Isoflavone: A Mechanistic Insight. NPC 2017, vol 12 no 4, pp: 627-634. doi: 10.3177/jnsv.66.S215. 2020.
[23] H. Tada, A. Nohara, M. Kawashiri. Serum Triglycerides and Atherosclerotic Cardiovascular Disease: Insights from Clinical and Genetic Studies. Nutrients 2018, vol 10 no 1789. doi: 10.3390/nu10111789.
[24] J. Farizal, L. Marlina, Halimatussadiah. Hubungan Kadar Trigliserida dengan Mahasiswa Obesitas. Avicenna 2019, vol 14 no 2, pp: 1-51. doi:10.36085/avicenna.v14i02.391
[25] JR. Liu, SY. Wang, MJ. Chen, Hl. Chen, PY. Yueh, CW. Lin. Hypocholesterolaemic effects of milk-kefir and soyamilk-kefir in cholesterol-fed hamsters. British Journal of Nutrition 2006, vol 95, pp: 939-946. doi: 10.1590/S1517-83822013000200001
[26] W. Qiu-ping, P. Chun-xiu, g. Bin, G. Jia-shun. Influence of large molecular polymeric pigments isolated from fermented Zijuan tea on the activity of key enzymes involved in lipid metabolism in rat. Experimental Gerontology 2012, vol 47, pp: 672-679. doi: 10.1016/j.jallcom.2021.159962
[27] M. Astawan, IS. Rahmawati, AP. Cahyani, T. Wresdiyati, SP. Putri, E. Fukusaki. Comparison between the potential of tempe flour made from germinated and nongerminated soybeans in preventing diabetes mellitus. Hayati Journal of Bioscience 2020, vol 27 no 1, pp: 17-23. doi: 10.4308/hjb.27.1.16
[28] M. Astawan, T. Wresdiyati, RM. Yoshari, NA. Rachmawati, R. Fadilla. The physicochemical Properties of Tempe Protein Isolated from Germinated and Non-Germinated Soybeans. J Nutr Sci Vitaminol. 2020;66(Supplement):S215-s221. doi: 10.3177/jnsv.66.S215. 2020.
[29] EJ. Parks. Effect of Dietary Carbohydrate on Triglyceride Metabolism in Humans. J. Nutr 2001, vol 131 no 10, pp: 2772s-2774s. doi: 10.1093/jn/131.10.2772S.
[30] A. Muscella, E. Stefano, S. Marsigliante. The effects of exercise training on lipid metabolism and coronary heart disease. Am J Physiol Heart Circ Physiol 2020, vol 319, pp: 76-88. doi: 10.1152/ajpheart.00708.2019
[31] T. Sun, M. Chen, H. Shen, PingYin, L. Fan, X. Chen, J. Wu, Z. Xu, J. Zhang. Predictive value of LDL/HDL ratio in coronary atherosclerotic heart disease. BMC Cardiovascular Disorders 2022, vol 22 no 273. doi: 10.1186/s12872-022-02706-6.
[32] l. Hernaez, MT. Soria-Florido, H. Schro¨der, E. Ros, X. Pinto, R. Estruch, J. Salas-Salvado, D. Corella, F. Aros, L. Serra-Majem, MA. Martınez-Gonzalez, M. Fiol, J. LapetraI, R. Elosua, RM. Lamuela-Ravento, M. Fito. Role of HDL function and LDL atherogenicity on cardiovascular risk: A comprehensive examination. PLoS ONE 2019, vol 14 no 6. doi: 10.3945/ajcn.2009.27597.
[33] F. Retiaty, F. Dany, F. Ernawati, N. Nurjanah, E. Efriwati, AY. Arifin, D. Sundari, M. Prihatini, W. Widoretno, E. Sahara, N. Imanningsih, AN. HerawatI. Dyslipidemia in Renal Dysfunction among Non-diabetic Individuals from the 2019 Indonesian Cohort Study: A Cross-Sectional Study. J. Gizi Pangan 2023, vol 18 no 2, pp: 71-78. doi: 10.25182/jgp.2023.18.2.71-78
[34] KRJ. Pou. Fermentation: The Key Step in the Processing of Black Tea. J. of Biosystem Eng 2016, vol 41 no 2, pp: 85-92. doi: 10.5307/JBE.2016.41.2.085
[35] L. Jiang, X. Shen, T. Shoji, T. Kanda, J. Zhou, L. Zhao. Characterization and Activity of Anthocyanins in Zijuan Tea (Camellia sinensis var. kitamura). J. Agric. Food. Chem 2013. doi: 10.1021/jf304860u
[36] Y. Qin, M. Xia, J. Ma, YT, Hao, J. Liu, HY. Mou, L. Cao, WH. L. Anthocyanin supplementation improves serum LDL- and HDL-cholesterol concentrations associated with the inhibition of cholesteryl ester transfer protein in dyslipidemic subjects. Am J Clin Nutr 2009, vol 90 no 485. doi: 10.3945/ajcn.2009.27814.
[37] X. Zhang, Y. Zhu, F. Song, Y. Yao, F. Ya, D. Li, W. Ling, Y. Yang. Effects of purified anthocyanin supplementation on platelet chemokines in hypocholesterolemic individuals: a randomized controlled trial. Nutrition & Metabolism 2016, vol 13 no 86. doi: 10.1186/s12986-016-0146-2.
[38] O. Ginting, E. Julianti, RJ. Nainggolan. Hypocholesterolemic Effect of Biscuit Made from Purple Sweet Potato Flour, Starch, and Fiber Rich Flour on Rats. Advance in Biological Science Research 2021, vol 16. doi: 10.2991/absr.k.220101.041
[39] HE. Popeijus, W. Zwaan, JZ. Tayyeb, J. Plat. Potential Contribution of Short Chain Fatty Acids to Hepatic Apolipoprotein A-I Production. Int. J. Mol. Sci 2021, vol 22 no 5986. doi: 10.3390/ijms22115986
[40] I. Susanti, RHB. Setiarto, J. Kahfi, R. Giarni, Muhamaludin, DP. Ramadhaningtyas, A. Randy. The Mechanism of Probiotics in Preventing the Risk of Hypercholesterolemia. Reviews in Agricultural Science 2023, vol 11 no 156, pp: 156-170. doi: 10.7831/ras.11.0_156
[41] SA. Joyce, A. Kamil, L. Fleige, CGM. Gahan. The Cholesterol-Lowering Effect of Oats and Oat Beta Glucan: Modes of Action and Potential Role of Bile Acids and the Microbiome. Front. Nutr 2019, vol 27. doi: 10.3389/fnut.2019.00171
[42] D. Rizwan, FA. Masoodi, SM. Wani, SA. Mir. Bioactive peptides from fermented foods and their relevance in COVID-19 mitigation. Food Production, Processing and Nutrition 2023, vol 5 no 53. doi: 10.1186/s43014-023-00165-w
[43] YS. Zhao, AS. Eweys, JY. Zhang, Y. Zhu, J. Bai, OM. Darwesh, HB. Zhang, X. Xiao 1. Fermentation Affects the Antioxidant Activity of Plant-Based Food Material through the Release and Production of Bioactive Components. Antioxidants 2021, vol 10 no 2004. doi: 10.3390/antiox10122004.
[44] MN. Iman, DE. Haslam, L. Liang, K. Guo, KCM. Perez, C. Clish, KL. Tucker, JE. Manson, SN. Bhupathiraju, E. Fukusaki, J. Lasky-Su, SP. Putri. Multidisciplinary approach combining food metabolomics and epidemiology identifies meglutol as an important bioactive metabolite in tempe, an Indonesian fermented food. Food Chemistry 2024, vol 446. doi: 10.1016/j.foodchem.2024.138744.
[45] SH. Baek, S. Park, HG. Lee. Hypocholesterolemic Action of Fermented Brown Rice Supplement in Cholesterol-Fed Rats: Cholesterol-lowering Action of Fermented Brown Rice. JFS sensory and nutritive qualities of food, vol 70 no 8. 2005. SH. Baek, S. Park, HG. Lee. Hypocholesterolemic Action of Fermented Brown Rice Supplement in Cholesterol-Fed Rats: Cholesterol-lowering Action of Fermented Brown Rice. JFS sensory and nutritive qualities of food, vol 70 no 8. 2005. doi:10.1111/J.1365-2621.2005.TB11529.X
[46] CH. Chiu, TY. Lu, YY. Tseng, TM. Pan. The effects of Lactobacillus-fermented milk on lipid metabolism in hamsters fed on high-cholesterol diet. Appl Microbiol Biotechnol, vol 71 no 238, pp: 238-245. 2006. doi: 10.1007/s00253-005-0145-0
[47] EA. Rossi, DCU. Cavallini, IZ. Carlos, RC. Vendramini, AR. Dâmaso, GF. deValdez. Intake of isoXavone-supplemented soy yogurt fermented with Enterococcus faecium lowers serum total cholesterol and non-HDL cholesterol of hypercholesterolemic rats. Eur Food Res Technol, vol 228, pp: 275-282. 2008. doi: 10.1007/s00217-008-0932-9
[48] ZW. Yang, BP. Ji, F. Zhou, B. Li, Y. Luo, L. Yang, T. Li. Hypocholesterolaemic and antioxidant effects of kombucha tea in high-cholesterol fed mice. J. Sci. Food Agric, vol 89, pp: 150-156. 2008. doi: 10.1002/jsfa.3422
[49] T. Tsung, C. Lihan, LL, Chun, MP, Tzu. Atherosclerosis-Preventing Activity of Lactic Acid Bacteria-Fermented Milk-Soymilk Supplemented with Momordica charantia. J. Agric. Food Chem, vol 57, pp: 2065-2071. 2009. doi: 10.1002/jsfa.3422
[50] YH. Pyo, KS, Seong. Hypolipidemic Effects of Monascus-Fermented Soybean Extracts in Rats Fed a High-Fat and -Cholesterol Diet. J. Agric. Food Chem, vol 57, pp: 8617-8622. 2009. doi: 10.1021/jf901878c
[51] SK. Yeap, BK. Beh, J. Kong, WY. Ho, HM. Yusof, NE. Mohamad, Ab. Hussin, IB. Jaganath, NB. Alitheen, A. Jamaluddin, K. Long. In vivo Hypocholesterolemic Effect of MARDI Fermented Red Yeast Rice Water Extract in High Cholesterol Diet Fed Mice. Evidence-Based Complementary and Alternative Medicine. 2014. doi: 10.1155/2014/707829.
[52] SJ. Yeon, GE. Hong, CK. Kim, WJ. Park, SK. Kim, CH. Lee. Effects of Yogurt Containing Fermented Pepper Juice on the Body Fat and Cholesterol Level in High Fat and High Cholesterol Diet Fed Rat. Korean J. Food Sci. An, Vol. 35, No. 4, pp: 479~485. 2015. doi: 10.5851/kosfa.2015.35.4.479
[53] SK. Yeap, BK. Beh, J. Kong, WY. Ho, HM. Yusof, NE. Mohamad, NM. Ali, IB. Jaganath, NB. Alitheen, SP. Koh, K. Long. In vivo Antioxidant and Hypolipidemic Effects of Fermented Mung Bean on Hypercholesterolemic Mice. Evidence-Based Complementary and Alternative Medicine. 2015. doi: 10.1155/2015/508029.
[54] R. Pothuraju1, RK. Sharma, PK. Kavadi, J. Chagalamarri, S. Jangra, G. Bhakri, S. De. Anti-obesity effect of milk fermented by Lactobacillus plantarum NCDC 625 alone and in combination with herbs on high fat diet fed C57BL/6J mice. Beneficial Microbes, vol 7 no 3, pp: 375-387. 2016. doi: 10.3920/BM2015.0083.
[55] S. Sengupta, H. Koley, S. Dutta, J. Bhowal. Hypocholesterolemic effect of Spirulina platensis (SP) fortified functional soy yogurts on diet-induced hypercholesterolemia. Journal of Functional Foods, Vol 48, pp: 54-64. 2018. doi: 10.1016/j.jff.2018.07.007
[56] YB. Jeon, JJ. Lee, HC. Chang, “Characterization of juice fermented with Lactobacillus plantarum EM and its cholesterol‐lowering effects on rats fed a high‐fat and high‐cholesterol diet”, Food Science and Nutrition, Vol 7, pp: 3622-3624, (2019). doi: 10.1002/fsn3.1217
[57] S. Park, HK. Son, HC. Chang, JJ. Lee. Effects of Cabbage-Apple Juice Fermented by Lactobacillus plantarum EM on Lipid Profile Improvement and Obesity Amelioration in Rats. Nutrients, Vol 12. 2020. doi: 10.3390/nu12041135.
[58] KM. El-Zahar, MFY. Hassan, SF. Al-Qaba,. Protective Effect of Fermented Camel Milk Containing Bifidobacterium longum BB536 on Blood Lipid Profile in Hypercholesterolemic Rats. Journal of Nutrition and Metabolism. 2021. doi: 10.1155/2021/1557945.
[59] YM. Alharbi, KM. El-Zahar, HM. Mousa. Beneficial Effects of Fermented Camel and Cow’s Milk in Lipid Profile, Liver, and Renal Function in Hypercholesterolemic Rats. Fermentation, vol 8 no 171. 2021. doi: 10.3390/fermentation8040171
[60] MS. Al-Anazi, KM. El-Zahar, NAH. Rabie,. Nutritional and Therapeutic Properties of Fermented Camel Milk Fortified with Red Chenopodium quinoa Flour on Hypercholesterolemia Rats. Molecules, Vol 27. 2022. doi: 10.3390/molecules27227695.
[61] SA. Althwab, SA. Alamro, WA. Abdulmonem, KS. Allemailem, SA. Alarifi, EM. Hamad. Fermented camel milk enriched with plant sterols improves lipid profile and atherogenic index in rats fed high -fat and -cholesterol diets. Heliyon,Vol 8. 2022. doi: 10.1016/j.heliyon.2022.e10871
[62] ESH. Atwaa, MR. Shahein, E. Raya-Álvarez, ES. Abd El-Sattar, MAA. Hassan, MA. Hashim, N. Dahran, MF. El-Khadragy, A. Agil, EK. Elmahallawy. Assessment of the physicochemical and sensory characteristics of fermented camel milk fortified with Cordia myxa and its biological effects against oxidative stress and hyperlipidemia in rats. Front. Nutr. 2022. doi: 10.3389/fnut.2023.1130224.
[63] S. Melia, I. Juliyarsi, YF. Kurnia, SN. Aritonang, E. Purwati, A. Sukma, N. Fitria, S. Susmiati, M. Meinapuri, YE. Pratama, N. Ramadhanti. Effect of fermented milk Pediococcus acidilactici BK01 on cholesterol and microbiota in Wistar mice intestine. Javar, Vol 10, No 1, pp: 64-71.2023. doi: 10.5455/javar.2023.j653 A periodical of the Network for the Veterinar.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Indonesian Food Science and Technology Journal
This work is licensed under a Creative Commons Attribution 4.0 International License.
