REVIEW |
|
|
|
|
|
Natural compounds proposed for the management of non-alcoholic fatty liver disease |
Théodora Merenda1, Florian Juszczak2, Elisabeth Ferier2,3, Pierre Duez3, Stéphanie Patris1, Anne-Émilie Declèves2, Amandine Nachtergael3 |
1 Unit of Clinical Pharmacy, Research Institute for Health Sciences and Technology, University of Mons(UMONS), Mons, Belgium; 2 Department of Metabolic and Molecular Biochemistry, Research Institute for Health Sciences and Technology, University of Mons(UMONS), Mons, Belgium; 3 Unit of Therapeutic Chemistry and Pharmacognosy, Research Institute for Health Sciences and Technology, University of Mons(UMONS), Mons, Belgium |
|
|
Abstract Although non-alcoholic fatty liver disease (NAFLD) presents as an intricate condition characterized by a growing prevalence, the often-recommended lifestyle interventions mostly lack high-level evidence of efficacy and there are currently no effective drugs proposed for this indication. The present review delves into NAFLD pathology, its diverse underlying physiopathological mechanisms and the available in vitro, in vivo, and clinical evidence regarding the use of natural compounds for its management, through three pivotal targets (oxidative stress, cellular inflammation, and insulin resistance). The promising perspectives that natural compounds offer for NAFLD management underscore the need for additional clinical and lifestyle intervention trials. Encouraging further research will contribute to establishing more robust evidence and practical recommendations tailored to patients with varying NAFLD grades.
|
Keywords
Non-alcoholic fatty liver disease
Natural compound
Sylimarin
Curcumin
Biochanin A
Oleanolic acid
Ginsenoside K
6-Gingerol
Naringenin
Hesperidin
Chenopodium quinoa
|
Fund:T. Merenda is supported by a doctoral fellowship from “UMONS-Les Amis des Aveugles et des Malvoyants” Academic chair. This work was partly funded by the multidisciplinary inter-institute “Health-Bioscience” projects 2020—QUINOACT. |
Corresponding Authors:
Amandine Nachtergael,E-mail:amandine.nachtergael@umons.ac.be
E-mail: amandine.nachtergael@umons.ac.be
|
Issue Date: 14 June 2024
|
|
|
1. George J, Anstee Q, Ratziu V, Sanyal A. NAFLD: the evolving landscape. J Hepatol. 2018;68(2):227–9. 2. Pappachan JM, Babu S, Krishnan B, Ravindran NC. Non-alcoholic fatty liver disease: a clinical update. J Clin Transl Hepatol. 2017;5(4):384–93. 3. Younossi ZM, Golabi P, Paik JM, Henry A, Van Dongen C, Henry L. The global epidemiology of nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH): a systematic review. Hepatology. 2023;77(4):1335–47. 4. Eslam M, Newsome PN, Sarin SK, Anstee QM, Targher G, Romero-Gomez M, et al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol. 2020;73(1):202–9. 5. Anty R, Gual P. Physiopathologie des stéatoses hépatiques métaboliques. Presse Med. 2019;48(12):1468–83. 6. EASL, EASD, EASO. EASL–EASD–EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol. 2016;64(6):1388–402. 7. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64(1):73–84. 8. Rong L, Zou J, Ran W, Qi X, Chen Y, Cui H, et al. Advancements in the treatment of non-alcoholic fatty liver disease (NAFLD). Front Endocrinol. 2023;13:1087260. 9. Chauhan M, Singh K, Thuluvath PJ. Bariatric surgery in NAFLD. Dig Dis Sci. 2022;67(2):408–22. 10. Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American association for the study of liver diseases. Hepatology. 2018;67(1):328–57. 11. Bedossa P. Pathology of non-alcoholic fatty liver disease. Liver Int. 2017;37(S1):85–9. 12. Elsheikh E, Henry LL, Younossi ZM. Current management of patients with nonalcoholic fatty liver disease. Expert Rev Endocrinol Metab. 2013;8(6):549–58. 13. Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology. 2016;63(3):764–75. 14. Dehnavi Z, Razmpour F, Belghaisi Naseri M, Nematy M, Alamdaran SA, Vatanparast HA, et al. Fatty liver index (FLI) in predicting non-alcoholic fatty liver disease (NAFLD). Hepat Mon. 2018;18(2). https://doi.org/10.5812/hepat mon. 63227 15. Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M, et al. Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol. 2018;15(1):11–20. 16. Li J, Zou B, Yeo YH, Feng Y, Xie X, Lee DH, et al. Prevalence, incidence, and outcome of non-alcoholic fatty liver disease in Asia, 1999–2019: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2019;4(5):389–98. 17. Devarbhavi H, Asrani SK, Arab JP, Nartey YA, Pose E, Kamath PS. Global burden of liver disease: 2023 update. J Hepatol. 2023;79(2):516–37. 18. Zhou F, Zhou J, Wang W, Zhang X, Ji Y, Zhang P, et al. Unexpected rapid increase in the burden of NAFLD in China from 2008 to 2018: a systematic review and meta-analysis. Hepatology. 2019;70(4):1119–33. 19. Kupčová V, Fedelešová M, Bulas J, Kozmonová P, Turecký L. Overview of the pathogenesis, genetic, and non-invasive clinical, biochemical, and scoring methods in the assessment of NAFLD. Int J Environ Res Public Health. 2019;16(19):3570. 20. Van De Wier B, Koek GH, Bast A, Haenen GRMM. The potential of flavonoids in the treatment of non-alcoholic fatty liver disease. Crit Rev Food Sci Nutr. 2017;57(4):834–55. 21. Robichon C, Girard J, Postic C. L’hyperactivité de la lipogenèse peut-elle conduire à la stéatose hépatique?: Implication du facteur de transcription ChREBP. Médecine/Sciences. 2008;24(10):841–6. 22. Zeng H, Qin H, Liao M, Zheng E, Luo X, Xiao A, et al. CD36 promotes de novo lipogenesis in hepatocytes through INSIG2-dependent SREBP1 processing. Mol Metab. 2022;57: 101428. 23. Van Raalte DH, Li M, Pritchard PH, Wasan KM. Peroxisome proliferatoractivated receptor (PPAR): a pharmacological target with a promising future. Pharm Res. 2004;21(9):1531–8. 24. Malhi H, Gores G. Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin Liver Dis. 2008;28(04):360–9. 25. Rohit L, Scott LF, Gerald IS. Mechanisms and disease consequences of non-alcoholic fatty liver disease. Cell. 2021;184(10):2537–64. 26. Aron-Wisnewsky J, Warmbrunn MV, Nieuwdorp M, Clément K. Nonalcoholic fatty liver disease: modulating gut microbiota to improve severity? Gastroenterology. 2020;158(7):1881–98. 27. Hongtao Xu, Fang F, Kaizhang Wu, Song J, Li Y, Xingyu Lu, Liu J, Zhou L, Wenqing Yu, Fei Yu, Gao J. Gut microbiota-bile acid crosstalk regulates murine lipid metabolism via the intestinal FXR-FGF19 axis in dietinduced humanized dyslipidemia. Microbiome. 2023;11(1):262. 28. Zhao YK, Zhu XD, Liu R, Yang X, Liang YL, Wang Y. The role of PPARγ gene polymorphisms, gut microbiota in type 2 diabetes: current progress and future prospects. Diabetes Metab Syndr Obes Targets Ther. 2023;16:3557–66. 29. Di Rosa C, Di Francesco L, Spiezia C, Khazrai YM. Effects of animal and vegetable proteins on gut microbiota in subjects with overweight or obesity. Nutrients. 2023;15(12):2675. 30. Saponaro C, Gaggini M, Gastaldelli A. Nonalcoholic fatty liver disease and type 2 diabetes: common pathophysiologic mechanisms. Curr Diab Rep. 2015;15(6):34. 31. Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA, et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet. 2008;40(12):1461–5. 32. Basu RS. PNPLA3-I148M: a problem of plenty in non-alcoholic fatty liver disease. Adipocyte. 2019;8(1):201–8. 33. He S, McPhaul C, Li JZ, Garuti R, Kinch L, Grishin NV, et al. A sequence variation (I148M) in PNPLA3 associated with nonalcoholic fatty liver disease disrupts triglyceride hydrolysis~*. J Biol Chem. 2010;285(9):6706–15. 34. Huang Y, He S, Li JZ, Seo YK, Osborne TF, Cohen JC, et al. A feed-forward loop amplifies nutritional regulation of PNPLA3. Proc Natl Acad Sci. 2010;107(17):7892–7. 35. Lake AC, Sun Y, Li JL, Kim JE, Johnson JW, Li D, et al. Expression, regulation, and triglyceride hydrolase activity of adiponutrin family members. J Lipid Res. 2005;46(11):2477–87. 36. Chamoun Z, Vacca F, Parton RG, Gruenberg J. PNPLA3/adiponutrin functions in lipid droplet formation. Biol Cell. 2013;105(5):219–33. 37. Ruhanen H, Perttilä J, Hölttä-Vuori M, Zhou Y, Yki-Järvinen H, Ikonen E, et al. PNPLA3 mediates hepatocyte triacylglycerol remodeling. J Lipid Res. 2014;55(4):739–46. 38. Jelenik T, Kaul K, Séquaris G, Flögel U, Phielix E, Kotzka J, et al. Mechanisms of insulin resistance in primary and secondary nonalcoholic fatty liver. Diabetes. 2017;66(8):2241–53. 39. Musso G, Cassader M, Gambino R. PNPLA3 rs738409 and TM6SF2 rs58542926 gene variants affect renal disease and function in nonalcoholic fatty liver disease. Hepatology. 2015;62(2):658–9. 40. Farzanegi P, Dana A, Ebrahimpoor Z, Asadi M, Azarbayjani MA. Mechanisms of beneficial effects of exercise training on non-alcoholic fatty liver disease (NAFLD): roles of oxidative stress and inflammation. Eur J Sport Sci. 2019;19(7):994–1003. 41. Oza MJ, Kulkarni YA. Biochanin A improves insulin sensitivity and controls hyperglycemia in type 2 diabetes. Biomed Pharmacother. 2018;107:1119–27. 42. Ohtaki H. Irisin. In: Handbook of hormones. Amsterdam: Elsevier; 2016. p. 329-e37-3. 43. Zelber-Sagi S, Salomone F, Mlynarsky L. The Mediterranean dietary pattern as the diet of choice for non-alcoholic fatty liver disease: evidence and plausible mechanisms. Liver Int. 2017;37(7):936–49. 44. Belfort R, Harrison SA, Brown K, Darland C, Finch J, Hardies J, et al. A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N Engl J Med. 2006;355(22):2297–307. 45. Singh S, Khera R, Allen A, Murad MH, Loomba R. Comparative effectiveness of pharmacological interventions for non-alcoholic steatohepatitis: a systematic review and network meta-analysis. Hepatology. 2015;62(5):1417–32. 46. Armstrong MJ, Gaunt P, Aithal GP, Barton D, Hull D, Parker R, et al. Liraglutide safety and efficacy in patients with non-alcoholic steatohepatitis (LEAN): a multicentre, double-blind, randomised, placebo-controlled phase 2 study. Lancet. 2016;387(10019):679–90. 47. Ekstedt M, Franzén LE, Mathiesen UL, Holmqvist M, Bodemar G, Kechagias S. Statins in non-alcoholic fatty liver disease and chronically elevated liver enzymes: a histopathological follow-up study. J Hepatol. 2007;47(1):135–41. 48. Nassir F. NAFLD: mechanisms, treatments, and biomarkers. Biomolecules. 2022;12(6):824. 49. Neuschwander-Tetri BA, Loomba R, Sanyal AJ, Lavine JE, Van Natta ML, Abdelmalek MF, et al. Farnesoid X nuclear receptor ligand obeticholic acid for non-cirrhotic, non-alcoholic steatohepatitis (FLINT): a multicentre, randomised, placebo-controlled trial. Lancet. 2015;385(9972):956–65. 50. Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med. 2010;362(18):1675–85. 51. Raza S. Current treatment paradigms and emerging therapies for NAFLD/NASH. Front Biosci. 2021;26(2):206–37. 52. Argo CK, Patrie JT, Lackner C, Henry TD, de Lange EE, Weltman AL, et al. Effects of n-3 fish oil on metabolic and histological parameters in NASH: a double-blind, randomized, placebo-controlled trial. J Hepatol. 2015;62(1):190–7. 53. Parker HM, Johnson NA, Burdon CA, Cohn JS, O’Connor HT, George J. Omega-3 supplementation, and non-alcoholic fatty liver disease: a systematic review and meta-analysis. J Hepatol. 2012;56(4):944–51. 54. Sanyal AJ, Abdelmalek MF, Suzuki A, Cummings OW, Chojkier M, EPE-A Study Group. No significant effects of ethyl-eicosapentanoic acid on histologic features of nonalcoholic steatohepatitis in a phase 2 trial. Gastroenterology. 2014;147(2):377-384.e1. 55. Jump DB, Lytle KA, Depner CM, Tripathy S. Omega-3 polyunsaturated fatty acids as a treatment strategy for nonalcoholic fatty liver disease. Pharmacol Ther. 2018;181:108–25. 56. Šmíd V, Dvořák K, Šedivý P, Kosek V, Leníček M, Dezortová M, et al. Effect of omega-3 polyunsaturated fatty acids on lipid metabolism in patients with metabolic syndrome and NAFLD. Hepatol Commun. 2022;6(6):1336–49. 57. Campbell P, Symonds A, Barritt AS. Therapy for nonalcoholic fatty liver disease: current options and future directions. Clin Ther. 2021;43(3):500–17. 58. Bower G, Toma T, Harling L, Jiao LR, Efthimiou E, Darzi A, et al. Bariatric surgery and non-alcoholic fatty liver disease: a systematic review of liver biochemistry and histology. Obes Surg. 2015;25(12):2280–9. 59. Léveillé M, Estall JL. Mitochondrial dysfunction in the transition from NASH to HCC. Metabolites. 2019;9(10):233. 60. Bugianesi E, Moscatiello S, Ciaravella MF, Marchesini G. Insulin resistance in nonalcoholic fatty liver disease. Curr Pharm Des. 2010;16(17):1941–51. 61. Bala V, Rajagopal S, Kumar DP, Nalli AD, Mahavadi S, Sanyal AJ, et al. Release of GLP-1 and PYY in response to the activation of G proteincoupled bile acid receptor TGR5 is mediated by Epac/PLC-Îμ pathway and modulated by endogenous H2S. Front Physiol. 2014;5:420. 62. Xue C, Li Y, Lv H, Zhang L, Bi C, Dong N, et al. Oleanolic acid targets the gut-liver axis to alleviate metabolic disorders and hepatic steatosis. J Agric Food Chem. 2021;69(28):7884–97. 63. Park H, Hur HJ, Kim S, Park S, Hong MJ, Sung MJ, et al. Biochanin A improves hepatic steatosis and insulin resistance by regulating the hepatic lipid and glucose metabolic pathways in diet-induced obese mice. Mol Nutr Food Res. 2016;60(9):1944–55. 64. Fan Y, Yan LT, Yao Z, Xiong GY. Biochanin A regulates cholesterol metabolism further delays the progression of nonalcoholic fatty liver disease. Diabetes Metab Syndr Obes. 2021;14:3161–72. 65. Mueller M, Lukas B, Novak J, Simoncini T, Genazzani AR, Jungbauer A. Oregano: a source for peroxisome proliferator-activated receptor γ antagonists. J Agric Food Chem. 2008;56(24):11621–30. 66. Shen P, Liu MH, Ng TY, Chan YH, Yong EL. Differential effects of isoflavones, from Astragalus membranaceus and Pueraria thomsonii, on the activation of PPARα, PPARγ, and adipocyte differentiation in vitro. J Nutr. 2006;136(4):899–905. 67. Mueller M, Jungbauer A. Red clover extract: a putative source for simultaneous treatment of menopausal disorders and the metabolic syndrome. Menopause. 2008;15(6):1120–31. 68. Wang L, Waltenberger B, Pferschy-Wenzig EM, Blunder M, Liu X, Malainer C, et al. Natural product agonists of peroxisome proliferatoractivated receptor gamma (PPARγ): a review. Biochem Pharmacol. 2014;92(1):73–89. 69. Murgueitio M, Wolber G, Christensen L. Identification of PPARγ agonists from natural sources using different in silico approaches. Planta Med. 2014;81(06):488–94. 70. Harini R, Ezhumalai M, Pugalendi KV. Antihyperglycemic effect of biochanin A, a soy isoflavone, on streptozotocin-diabetic rats. Eur J Pharmacol. 2012;676(1–3):89–94. 71. Wu L, Guo C, Wu J. Therapeutic potential of PPARγ natural agonists in liver diseases. J Cell Mol Med. 2020;24(5):2736–48. 72. Den Hartogh DJ, Gabriel A, Tsiani E. Antidiabetic properties of curcumin I: evidence from in vitro studies. Nutrients. 2020;12(1):118. 73. Abd El-Hameed NM, Abd El-Aleem SA, Khattab MA, Ali AH, Mohammed HH. Curcumin activation of nuclear factor E2-related factor 2 gene (Nrf2): prophylactic and therapeutic effect in nonalcoholic steatohepatitis (NASH). Life Sci. 2021;285: 119983. 74. Saadati S, Sadeghi A, Mansour A, Yari Z, Poustchi H, Hedayati M, et al. Curcumin and inflammation in non-alcoholic fatty liver disease: a randomized, placebo controlled clinical trial. BMC Gastroenterol. 2019;19(1):133. 75. Saadati S, Hatami B, Yari Z, Shahrbaf MA, Eghtesad S, Mansour A, et al. The effects of curcumin supplementation on liver enzymes, lipid profile, glucose homeostasis, and hepatic steatosis and fibrosis in patients with non-alcoholic fatty liver disease. Eur J Clin Nutr. 2019;73(3):441–9. 76. Zeng Y, Luo Y, Wang L, Zhang K, Peng J, Fan G. Therapeutic effect of curcumin on metabolic diseases: evidence from clinical studies. Int J Mol Sci. 2023;24(4):3323. 77. Schiborr C, Kocher A, Behnam D, Jandasek J, Toelstede S, Frank J. The oral bioavailability of curcumin from micronized powder and liquid micelles is significantly increased in healthy humans and differs between sexes. Mol Nutr Food Res. 2014;58(3):516–27. 78. Shoba G, Joy D, Joseph T, Majeed M, Rajendran R, Srinivas PS. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med. 1998;64(4):353–6. 79. Sancilio S, Basile M, Di Pietro R. Curcuma longa hepatotoxicity: a baseless accusation. Case assessed for causality using RUCAM method. Front Pharmacol. 2021;12: 780330. 80. Almatroodi SA, Alnuqaydan AM, Babiker AY, Almogbel MA, Khan AA, Husain RA. 6-Gingerol, a bioactive compound of ginger attenuates renal damage in streptozotocin-induced diabetic rats by regulating the oxidative stress and inflammation. Pharmaceutics. 2021;13(3):317. 81. Liu Y, Li D, Wang S, Peng Z, Tan Q, He Q, et al. 6-Gingerol ameliorates hepatic steatosis, inflammation and oxidative stress in high-fat diet-fed mice through activating LKB1/AMPK signaling. Int J Mol Sci. 2023;24(7):6285. 82. Gross B, Pawlak M, Lefebvre P, Staels B. PPARs in obesity induced T2DM, dyslipidaemia and NAFLD. Nat Rev Endocrinol. 2017;13(1):36–49. 83. Tzeng TF, Liou SS, Chang CJ, Liu IM. [6]-Gingerol dampens hepatic steatosis and inflammation in experimental nonalcoholic steatohepatitis. Phytomedicine. 2015;22(4):452–61. 84. Gao H, Guan T, Li C, Zuo G, Yamahara J, Wang J, et al. Treatment with ginger ameliorates fructose-induced Fatty liver and hypertriglyceridemia in rats: modulation of the hepatic carbohydrate response element-binding protein-mediated pathway. Evid-Based Complement Altern Med. 2012;2012: 570948. 85. Iizuka K, Miller B, Uyeda K. Deficiency of carbohydrate-activated transcription factor ChREBP prevents obesity and improves plasma glucose control in leptin-deficient (ob/ob) mice. Am J Physiol Endocrinol Metab. 2006;291(2):E358-364. 86. Li Y, Tran VH, Kota BP, Nammi S, Duke CC, Roufogalis BD. Preventative effect of Zingiber officinale on insulin resistance in a high-fat highcarbohydrate diet-fed rat model and its mechanism of action. Basic Clin Pharmacol Toxicol. 2014;115(2):209–15. 87. Li XH, McGrath KCY, Tran VH, Li YM, Duke CC, Roufogalis BD, et al. Attenuation of proinflammatory responses by S-[6]-gingerol via inhibition of ROS/NF-Kappa B/COX2 activation in HuH7 cells. Evid Based Complement Alternat Med. 2013;2013: 146142. 88. Kota N, Panpatil VV, Kaleb R, Varanasi B, Polasa K. Dose-dependent effect in the inhibition of oxidative stress and anticlastogenic potential of ginger in STZ induced diabetic rats. Food Chem. 2012;135(4):2954–9. 89. Wang J, Ke W, Bao R, Hu X, Chen F. Beneficial effects of ginger Zingiber officinale Roscoe on obesity and metabolic syndrome: a review: beneficial effects of ginger in metabolic syndrome. Ann N Y Acad Sci. 2017;1398(1):83–98. 90. Ahn J, Lee H, Jung CH, Ha SY, Seo HD, Kim YI, et al. 6-Gingerol ameliorates hepatic steatosis via HNF4α/miR-467b-3p/GPAT1 cascade. Cell Mol Gastroenterol Hepatol. 2021;12(4):1201–13. 91. Li J, Wang S, Yao L, Ma P, Chen Z, Han TL, et al. 6-Gingerol ameliorates age-related hepatic steatosis: association with regulating lipogenesis, fatty acid oxidation, oxidative stress, and mitochondrial dysfunction. Toxicol Appl Pharmacol. 2019;362:125–35. 92. Chen XJ, Liu WJ, Wen ML, Liang H, Wu SM, Zhu YZ, et al. Ameliorative effects of compound K and ginsenoside Rh1 on non-alcoholic fatty liver disease in rats. Sci Rep. 2017;7(1):41144. 93. Choi SY, Park JS, Shon CH, Lee CY, Ryu JM, Son DJ, et al. Fermented Korean red ginseng extract enriched in Rd and Rg3 protects against non-alcoholic fatty liver disease through regulation of mTORC1. Nutrients. 2019;11(12):2963. 94. Hwang YC, Oh DH, Choi MC, Lee SY, Ahn KJ, Chung HY, et al. Compound K attenuates glucose intolerance and hepatic steatosis through AMPK-dependent pathways in type 2 diabetic OLETF rats. Korean J Intern Med. 2018;33(2):347–55. 95. Kim M, Lee K, Iseli TJ, Hoy AJ, George J, Grewal T, et al. Compound K modulates fatty acid-induced lipid droplet formation and expression of proteins involved in lipid metabolism in hepatocytes. Liver Int. 2013;33(10):1583–93. 96. Yue C, Li D, Fan S, Tao F, Yu Y, Lu W, et al. Long-term and liver-selected ginsenoside C-K nanoparticles retard NAFLD progression by restoring lipid homeostasis. Biomaterials. 2023;301: 122291. 97. Bessell E, Fuller NR, Markovic TP, Burk J, Picone T, Hendy C, et al. Effects of alpha-cyclodextrin on cholesterol control and compound K on glycaemic control in people with pre-diabetes: protocol for a phase III randomized controlled trial. Clin Obes. 2019;9(4): e12324. 98. Kim K, Park M, Lee YM, Rhyu MR, Kim HY. Ginsenoside metabolite compound K stimulates glucagon-like peptide-1 secretion in NCI-H716 cells via bile acid receptor activation. Arch Pharm Res. 2014;37(9):1193–200. 99. Wu J, Huang G, Li Y, Li X. Flavonoids from Aurantii fructus Immaturus and Aurantii fructus: promising phytomedicines for the treatment of liver diseases. Chin Med. 2020;15(1):89. 100. Pari L, Karthikeyan A, Karthika P, Rathinam A. Protective effects of hesperidin on oxidative stress, dyslipidaemia and histological changes in iron-induced hepatic and renal toxicity in rats. Toxicol Rep. 2015;2:46–55. 101. Jain A, Yadav A, Bozhkov AI, Padalko VI, Flora SJS. Therapeutic efficacy of silymarin and naringenin in reducing arsenic-induced hepatic damage in young rats. Ecotoxicol Environ Saf. 2011;74(4):607–14. 102. Xie Q, Gao S, Lei M, Li Z. Hesperidin suppresses ERS-induced inflammation in the pathogenesis of non-alcoholic fatty liver disease. Aging. 2022;14(3):1265–79. 103. Chen H, Nie T, Zhang P, Ma J, Shan A. Hesperidin attenuates hepatic lipid accumulation in mice fed high-fat diet and oleic acid induced HepG2 via AMPK activation. Life Sci. 2022;296: 120428. 104. Wang SW, Sheng H, Bai YF, Weng YY, Fan XY, Lou LJ, et al. Neohesperidin enhances PGC-1α-mediated mitochondrial biogenesis and alleviates hepatic steatosis in high fat diet fed mice. Nutr Diabetes. 2020;10(1):27. 105. Cheraghpour M, Imani H, Ommi S, Alavian SM, Karimi-Shahrbabak E, Hedayati M, et al. Hesperidin improves hepatic steatosis, hepatic enzymes, and metabolic and inflammatory parameters in patients with nonalcoholic fatty liver disease: a randomized, placebo-controlled, double-blind clinical trial. Phytother Res. 2019;33(8):2118–25. 106. Yari Z, Cheraghpour M, Alavian SM, Hedayati M, Eini-Zinab H, Hekmatdoost A. The efficacy of flaxseed and hesperidin on non-alcoholic fatty liver disease: an open-labeled randomized controlled trial. Eur J Clin Nutr. 2020;75(1):99–111. 107. Baxter K, Driver S, Williamson E. Stockley’s herbal medicines interactions. London: Pharmaceutical Press; 2013. 108. Jayaraman J, Jesudoss VAS, Menon VP, Namasivayam N. Anti-inflammatory role of naringenin in rats with ethanol induced liver injury. Toxicol Mech Methods. 2012;22(7):568–76. 109. Namkhah Z, Naeini F, Mahdi Rezayat S, Yaseri M, Mansouri S, Javad Hosseinzadeh-Attar M. Does naringenin supplementation improve lipid profile, severity of hepatic steatosis and probability of liver fibrosis in overweight/obese patients with NAFLD? A randomised, double-blind, placebo-controlled, clinical trial. Int J Clin Pract. 2021;75(11): e14852. 110. AbouZid SF, Ahmed HS, Moawad AS, Owis AI, Chen SN, Nachtergael A, et al. Chemotaxonomic and biosynthetic relationships between flavonolignans produced by Silybum marianum populations. Fitoterapia. 2017;119:175–84. 111. AbouZid SF, Ahmed HS, Abd El Mageed AEMA, Moawad AS, Owis AI, Chen SN, et al. Linear regression analysis of silychristin A, silybin A and silybin B contents in Silybum marianum. Nat Prod Res. 2020;34(2):305–10. 112. Cicero A, Colletti A, Bellentani S. Nutraceutical approach to nonalcoholic fatty liver disease (NAFLD): the available clinical evidence. Nutrients. 2018;10(9):1153. 113. Di Costanzo A, Angelico R. Formulation strategies for enhancing the bioavailability of silymarin: the state of the art. Molecules. 2019;24(11):2155. 114. Semalty A, Semalty M, Rawat MSM, Franceschi F. Supramolecular phospholipids–polyphenolics interactions: the PHYTOSOME® strategy to improve the bioavailability of phytochemicals. Fitoterapia. 2010;81(5):306–14. 115. Grattagliano I, Diogo CV, Mastrodonato M, de Bari O, Persichella M, Wang DQH, et al. A silybin-phospholipids complex counteracts rat fatty liver degeneration and mitochondrial oxidative changes. World J Gastroenterol. 2013;19(20):3007–17. 116. Haddad Y, Vallerand D, Brault A, Haddad PS. Antioxidant and hepatoprotective effects of silibinin in a rat model of nonalcoholic steatohepatitis. Evid Based Complement Alternat Med. 2011;2011: nep164. 117. Kim KD, Lee HJ, Lim SP, Sikder MDA, Lee SY, Lee CJ. Silibinin regulates gene expression, production and secretion of mucin from cultured airway epithelial cells. Phytother Res. 2012;26(9):1301–7. 118. Salamone F, Galvano F, Cappello F, Mangiameli A, Barbagallo I, Li VG. Silibinin modulates lipid homeostasis and inhibits nuclear factor kappa B activation in experimental nonalcoholic steatohepatitis. Transl Res J Lab Clin Med. 2012;159(6):477–86. 119. Salamone F, Galvano F, Marino Gammazza A, Marino A, Paternostro C, Tibullo D, et al. Silibinin improves hepatic and myocardial injury in mice with nonalcoholic steatohepatitis. Dig Liver Dis. 2012;44(4):334–42. 120. Serviddio G, Bellanti F, Giudetti AM, Gnoni GV, Petrella A, Tamborra R, et al. A silybin-phospholipid complex prevents mitochondrial dysfunction in a rodent model of nonalcoholic steatohepatitis. J Pharmacol Exp Ther. 2010;332(3):922–32. 121. Yao J, Zhi M, Gao X, Hu P, Li C, Yang X. Effect, and the probable mechanisms of silibinin in regulating insulin resistance in the liver of rats with non-alcoholic fatty liver. Braz J Med Biol Res Rev Bras Pesqui Medicas E Biol. 2013;46(3):270–7. 122. Yao J, Zhi M, Minhu C. Effect of silybin on high-fat-induced fatty liver in rats. Braz J Med Biol Res Rev Bras Pesqui Medicas E Biol. 2011;44(7):652–9. 123. Zhong S, Fan Y, Yan Q, Fan X, Wu B, Han Y, et al. The therapeutic effect of silymarin in the treatment of nonalcoholic fatty disease: a metaanalysis (PRISMA) of randomized control trials. Medicine (Baltimore). 2017;96(49): e9061. 124. Chantarojanasiri T. Silymarin treatment and reduction of liver enzyme levels in non-alcoholic fatty liver disease: a case report. Drugs Context. 2023;12:1–5. 125. Hashem A. Silymarin and management of liver function in nonalcoholic steatohepatitis: a case report. Drugs Context. 2023;12:1–5. 126. Zhong L, Lyu W, Lin Z, Lu J, Geng Y, Song L, et al. Quinoa ameliorates hepatic steatosis, oxidative stress, inflammation and regulates the gut microbiota in nonalcoholic fatty liver disease rats. Foods. 2023;12(9):1780. 127. Mirhashemi SH, Hakakzadeh A, Yeganeh FE, Oshidari B, Rezaee SP. Effect of 8 weeks milk thistle powder (silymarin extract) supplementation on fatty liver disease in patients candidates for bariatric surgery. Metab Open. 2022;14: 100190. 128. Poulos JE, Kalogerinis PT, Milanov V, Kalogerinis CT, Poulos EJ. The effects of vitamin E, silymarin and carnitine on the metabolic abnormalities associated with nonalcoholic liver disease. J Diet Suppl. 2021;19(3):287–302. 129. Yao Y, Yang X, Shi Z, Ren G. Anti-inflammatory activity of saponins from quinoa (Chenopodium quinoa Willd.) seeds in lipopolysaccharide-stimulated RAW 264.7 macrophages cells. J Food Sci. 2014;79(5):H1018–23. 130. An T, Liu JX, Yang XY, Lv BH, Wu YX, Jiang GJ. Supplementation of quinoa regulates glycolipid metabolism and endoplasmic reticulum stress in the high-fat diet-induced female obese mice. Nutr Metab. 2021;18(1):1–11. 131. Al-Qabba MM, El-Mowafy MA, Althwab SA, Alfheeaid HA, Aljutaily T, Barakat H. Phenolic profile, antioxidant activity, and ameliorating efficacy of Chenopodium quinoa sprouts against CCl4-induced oxidative stress in rats. Nutrients. 2020;12(10):2904. 132. Shen N, Wang T, Gan Q, Liu S, Wang L, Jin B. Plant flavonoids: classification, distribution, biosynthesis, and antioxidant activity. Food Chem. 2022;383: 132531. 133. De Carvalho FG, Ovídio PP, Padovan GJ, Jordão Junior AA, Marchini JS, Navarro AM. Metabolic parameters of postmenopausal women after quinoa or corn flakes intake—a prospective and double-blind study. Int J Food Sci Nutr. 2013;65(3):380–5. 134. Navarro-Perez D, Radcliffe J, Tierney A, Jois M. Quinoa seed lowers serum triglycerides in overweight and obese subjects: a dose-response randomized controlled clinical trial. Curr Dev Nutr. 2017;1(9): e001321. 135. Foucault A, Mathé V, Lafont R, Even P, Dioh W, Veillet S, et al. Quinoa extract enriched in 20-hydroxyecdysone protects mice from diet-induced obesity and modulates adipokines expression. Obesity. 2012;20(2):270–7. 136. Graf BL, Poulev A, Kuhn P, Grace MH, Lila MA, Raskin I. Quinoa seeds leach phytoecdysteroids and other compounds with anti-diabetic properties. Food Chem. 2014;163:178–85. 137. Foucault AS, Even P, Lafont R, Dioh W, Veillet S, Tomé D, et al. Quinoa extract enriched in 20-hydroxyecdysone affects energy homeostasis and intestinal fat absorption in mice fed a high-fat diet. Physiol Behav. 2014;128:226–31. 138. Simnadis TG, Tapsell LC, Beck EJ. Physiological effects associated with quinoa consumption and implications for research involving humans: a review. Plant Foods Hum Nutr. 2015;70(3):238–49. |
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|