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Effects of Artichoke Supplementation on Liver Enzymes: A Systematic Review and Meta-Analysis of Randomized Controlled Trials

  • Mohammad Reza Amini (Student Research Committee, Department of Clinical Nutrition and Dietetics, Faculty of Nutrition Sciences and Food Technology, National Nutrition & Food Technology Research Institute, Shahid Beheshti University of Medical Sciences) ;
  • Fatemeh Sheikhhossein (Department of Clinical Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences (TUMS)) ;
  • Alireza Talebyan (Department of Community Nutrition, School of Nutrition and Food Sciences, Shiraz University of Medical Sciences) ;
  • Elham Bazshahi (Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences (TUMS)) ;
  • Farhang Djafari (Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences (TUMS)) ;
  • Azita Hekmatdoost (Department of Clinical Nutrition & Dietetics, National Nutrition & Food Technology Research Institute, Shahid Beheshti University of Medical Sciences)
  • Received : 2022.04.02
  • Accepted : 2022.06.08
  • Published : 2022.07.31

Abstract

Studies examining the effect of artichoke on liver enzymes have reported inconsistent results. This systematic review and meta-analysis aimed to assess the effects of artichoke administration on the liver enzymes. PubMed, Embase, the Cochrane Library, and Scopus databases were searched for articles published up to January 2022. Standardized mean difference (Hedges' g) were analyzed using a random-effects model. Heterogeneity, publication bias, and sensitivity analysis were assessed for the liver enzymes. Pooled analysis of seven randomized controlled trials (RCTs) suggested that the artichoke administration has an effect on both alanine aminotransferase (ALT) (Hedges' g, -1.08; 95% confidence interval [CI], -1.76 to -0.40; p = 0.002), and aspartate aminotransferase (AST) (Hedges' g, -1.02; 95% CI, -1.76 to -0.28; p = 0.007). Greater effects on ALT were detected in trials that lasted ≤8 weeks. Also, greater effects on AST were detected in trials using > 500 mg artichoke. Overall, this meta-analysis demonstrated artichoke supplementation decreased ALT and AST.

Keywords

Acknowledgement

This study is related to the project NO. 1400/65026 from Student Research Committee, Shahid Beheshti University of Medical Sciences, Tehran, Iran. We also appreciate the "Student Research Committee" and "Research & Technology Chancellor" in Shahid Beheshti University of Medical Sciences for their financial support of this study.

References

  1. Krawczyk M, Bonfrate L, Portincasa P. Nonalcoholic fatty liver disease. Best Pract Res Clin Gastroenterol 2010;24:695-708.
  2. Rinella ME. Nonalcoholic fatty liver disease: a systematic review. JAMA 2015;313:2263-73.
  3. Dyson JK, Anstee QM, McPherson S. Non-alcoholic fatty liver disease: a practical approach to diagnosis and staging. Frontline Gastroenterol 2014;5:211-8.
  4. Machado MV, Cortez-Pinto H. Non-alcoholic fatty liver disease: what the clinician needs to know. World J Gastroenterol 2014;20:12956-80.
  5. Jadeja R, Devkar RV, Nammi S. Herbal medicines for the treatment of nonalcoholic steatohepatitis: current scenario and future prospects. Evid Based Complement Alternat Med 2014;2014:648308.
  6. Uhl P, Fricker G, Haberkorn U, Mier W. Current status in the therapy of liver diseases. Int J Mol Sci 2014;15:7500-12.
  7. Speroni E, Cervellati R, Govoni P, Guizzardi S, Renzulli C, Guerra MC. Efficacy of different Cynara scolymus preparations on liver complaints. J Ethnopharmacol 2003;86:203-11.
  8. Leung AT, Foster S. Encyclopedia of common natural ingredients used in food, drugs, and cosmetics. New York (NY): John Wiley & Sons, Inc.; 1996. 649 p.
  9. Barnes J, Anderson LA, Phillipson JD. Herbal medicines: a guide for healthcare professionals. London: The Pharmaceutical Press; 1996.
  10. Mulinacci N, Prucher D, Peruzzi M, Romani A, Pinelli P, Giaccherini C, Vincieri FF. Commercial and laboratory extracts from artichoke leaves: estimation of caffeoyl esters and flavonoidic compounds content. J Pharm Biomed Anal 2004;34:349-57.
  11. Zhu X, Zhang H, Lo R. Phenolic compounds from the leaf extract of artichoke (Cynara scolymus L.) and their antimicrobial activities. J Agric Food Chem 2004;52:7272-8.
  12. Kusku-Kiraz Z, Mehmetcik G, Dogru-Abbasoglu S, Uysal M. Artichoke leaf extract reduces oxidative stress and lipoprotein dyshomeostasis in rats fed on high cholesterol diet. Phytother Res 2010;24:565-70.
  13. Zapolska-Downar D, Zapolski-Downar A, Naruszewicz M, Siennicka A, Krasnodebska B, Koldziej B. Protective properties of artichoke (Cynara scolymus) against oxidative stress induced in cultured endothelial cells and monocytes. Life Sci 2002;71:2897-08.
  14. Jimenez-Escrig A, Dragsted LO, Daneshvar B, Pulido R, Saura-Calixto F. In vitro antioxidant activities of edible artichoke (Cynara scolymus L.) and effect on biomarkers of antioxidants in rats. J Agric Food Chem 2003;51:5540-5.
  15. Heidarian E, Soofiniya Y, Hajihosseini R. The effect of aerial part of Cynara scolymus extract on the hyperlipidemia, plasma antioxidant capacity, and superoxide dismutase activity in diabetic rats. J Shahrekord Univ Med Sci 2011;13:1-9.
  16. Mehmetcik G, Ozdemirler G, Kocak-Toker N, Cevikbas U, Uysal M. Effect of pretreatment with artichoke extract on carbon tetrachloride-induced liver injury and oxidative stress. Exp Toxicol Pathol 2008;60:475-80.
  17. Panahi Y, Kianpour P, Mohtashami R, Atkin SL, Butler AE, Jafari R, Badeli R, Sahebkar A. Efficacy of artichoke leaf extract in non-alcoholic fatty liver disease: a pilot double-blind randomized controlled trial. Phytother Res 2018;32:1382-7.
  18. Miccadei S, Di Venere D, Cardinali A, Romano F, Durazzo A, Foddai MS, Fraioli R, Mobarhan S, Maiani G. Antioxidative and apoptotic properties of polyphenolic extracts from edible part of artichoke (Cynara scolymus L.) on cultured rat hepatocytes and on human hepatoma cells. Nutr Cancer 2008;60:276-83.
  19. Fallah Huseini H, Kianbakht S, Heshmat R. Cynara scolymus L. in treatment of hypercholesterolemic type 2 diabetic patients: a randomized double-blind placebo-controlled clinical trial. J Med Plants 2012;11:58-65.
  20. Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097.
  21. Richardson WS, Wilson MC, Nishikawa J, Hayward RS. The well-built clinical question: a key to evidencebased decisions. ACP J Club 1995;123:A12-3.
  22. Higgins JPT, Altman DG, Sterne JAC. Chapter 8. Assessing risk of bias in included studies. In: Higgins JPT, Green S, editors. Cochrane handbook for systematic reviews of interventions. London: Cochrane Collaboration; 2008. p. 187-241.
  23. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. Introduction to meta-analysis. Hoboken (NJ): John Wiley & Sons, Ltd; 2011.
  24. Fedorov S. GetData Graph Digitizer version 2.24 [Internet]. Available from: www.getdata-graph-digitizer.com. 2002.
  25. DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 2007;28:105-14.
  26. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629-34.
  27. Englisch W, Beckers C, Unkauf M, Ruepp M, Zinserling V. Efficacy of artichoke dry extract in patients with hyperlipoproteinemia. Arzneimittelforschung 2000;50:260-5.
  28. Musolino V, Gliozzi M, Bombardelli E, Nucera S, Carresi C, Maiuolo J, Mollace R, Paone S, Bosco F, Scarano F, Scicchitano M, Macri R, Ruga S, Zito MC, Palma E, Gratteri S, Ragusa M, Volterrani M, Fini M, Mollace V. The synergistic effect of Citrus bergamia and Cynara cardunculus extracts on vascular inflammation and oxidative stress in non-alcoholic fatty liver disease. J Tradit Complement Med 2020;10:268-74.
  29. Rangboo V, Noroozi M, Zavoshy R, Rezadoost SA, Mohammadpoorasl A. The effect of artichoke leaf extract on alanine aminotransferase and aspartate aminotransferase in the patients with nonalcoholic steatohepatitis. Int J Hepatol 2016;2016:4030476.
  30. Roghani-Dehkordi F, Kamkhah AF. Artichoke leaf juice contains antihypertensive effect in patients with mild hypertension. J Diet Suppl 2009;6:328-41.
  31. Rondanelli M, Riva A, Petrangolini G, Allegrini P, Bernardinelli L, Fazia T, Peroni G, Gasparri C, Nichetti M, Faliva MA, Naso M, Perna S. The metabolic effects of Cynara supplementation in overweight and obese class I subjects with newly detected impaired fasting glycemia: a double-blind, placebo-controlled, randomized clinical trial. Nutrients 2020;12:3298.
  32. Moradi S, Shokri-Mashhadi N, Saraf-Bank S, Mohammadi H, Zobeiri M, Clark CC, Rouhani MH. The effects of Cynara scolymus L. supplementation on liver enzymes: a systematic review and meta-analysis. Int J Clin Pract 2021;75:e14726.
  33. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 2012;55:2005-23.
  34. Naik SR, Panda VS. Antioxidant and hepatoprotective effects of Ginkgo biloba phytosomes in carbon tetrachloride-induced liver injury in rodents. Liver Int 2007;27:393-9.
  35. Mouzaki M, Allard J. Non-alcoholic steatohepatitis: the therapeutic challenge of a global epidemic. Ann Gastroenterol 2012;25:207-17.
  36. Ebrahimi-Mameghani M, Asghari-Jafarabadi M, Rezazadeh K. TCF7L2-rs7903146 polymorphism modulates the effect of artichoke leaf extract supplementation on insulin resistance in metabolic syndrome: a randomized, double-blind, placebo-controlled trial. J Integr Med 2018;16:329-34.
  37. Al-Ahdab MJ. Protective effect of artichoke (Cynara scolymus L.) leaves and pulp extracts against carbon tetrachloride-induced acute hepatotoxicity in rats. World Appl Sci J 2014;32:1004-14.
  38. El Sohaimy SA. Chemical composition, antioxidant and antimicrobial potential of artichoke. Open Nutraceuticals J 2014;7:15-20.
  39. Vamanu E, Vamanu A, Nita S, Colceriu SJ. Antioxidant and antimicrobial activities of ethanol extracts of Cynara scolymus (Cynarae folium, Asteraceae family). Trop J Pharm Res 2011;10:777-83.
  40. Gebhardt R, Fausel M. Antioxidant and hepatoprotective effects of artichoke extracts and constituents in cultured rat hepatocytes. Toxicol In Vitro 1997;11:669-72.
  41. Rezazadeh K, Rahmati-Yamchi M, Mohammadnejad L, Ebrahimi-Mameghani M, Delazar A. Effects of artichoke leaf extract supplementation on metabolic parameters in women with metabolic syndrome: Influence of TCF7L2-rs7903146 and FTO-rs9939609 polymorphisms. Phytother Res 2018;32:84-93.
  42. Rondanelli M, Opizzi A, Faliva M, Sala P, Perna S, Riva A, Morazzoni P, Bombardelli E, Giacosa A. Metabolic management in overweight subjects with naive impaired fasting glycaemia by means of a highly standardized extract from Cynara scolymus: a double-blind, placebo-controlled, randomized clinical trial. Phytother Res 2014;28:33-41.
  43. Rondanelli M, Giacosa A, Orsini F, Opizzi A, Villani S. Appetite control and glycaemia reduction in overweight subjects treated with a combination of two highly standardized extracts from Phaseolus vulgaris and Cynara scolymus. Phytother Res 2011;25:1275-82.
  44. Aksu O, Altinterim B. Hepatoprotective effects of artichoke (Cynara scolymus). Bilim ve Genclik Dergisi 2013;1:44-9.
  45. Metwally NS, Kholeif TE, Ghanem KZ, Farrag AR, Ammar NM, Abdel-Hamid AH. The protective effects of fish oil and artichoke on hepatocellular carcinoma in rats. Eur Rev Med Pharmacol Sci 2011;15:1429-44.
  46. Brown JE, Rice-Evans CA. Luteolin-rich artichoke extract protects low density lipoprotein from oxidation in vitro. Free Radic Res 1998;29:247-55.
  47. Goni I, Jimenez-Escrig A, Gudiel M, Saura-Calixto FD. Artichoke (Cynara scolymus L) modifies bacterial enzymatic activities and antioxidant status in rat cecum. Nutr Res 2005;25:607-15.
  48. Skarpanska-Stejnborn A, Pilaczynska-Szczesniak L, Basta P, Deskur-Smielcka E, Horoszkiewicz-Hassan M. The influence of supplementation with artichoke (Cynara scolymus L.) extract on selected redox parameters in rowers. Int J Sport Nutr Exerc Metab 2008;18:313-27.
  49. Gebhardt R. Inhibition of cholesterol biosynthesis in primary cultured rat hepatocytes by artichoke (Cynara scolymus L.) extracts. J Pharmacol Exp Ther 1998;286:1122-8.
  50. Azzini E, Bugianesi R, Romano F, Di Venere D, Miccadei S, Durazzo A, Foddai MS, Catasta G, Linsalata V, Maiani G. Absorption and metabolism of bioactive molecules after oral consumption of cooked edible heads of Cynara scolymus L. (cultivar Violetto di Provenza) in human subjects: a pilot study. Br J Nutr 2007;97:963-9.
  51. Wittemer SM, Ploch M, Windeck T, Muller SC, Drewelow B, Derendorf H, Veit M. Bioavailability and pharmacokinetics of caffeoylquinic acids and flavonoids after oral administration of artichoke leaf extracts in humans. Phytomedicine 2005;12:28-38.
  52. Schutz K, Kammerer D, Carle R, Schieber A. Identification and quantification of caffeoylquinic acids and flavonoids from artichoke (Cynara scolymus L.) heads, juice, and pomace by HPLC-DAD-ESI/MS(n). J Agric Food Chem 2004;52:4090-6.
  53. Mohamed SH, Ahmed HH, Harrag AR, Abdel-Azim NS, Shahat AA. Cynara scolymus for relieving on nonalcoholic steatohepatitis induced in rats. Int J Pharm Pharm Sci 2013;5:57-66.
  54. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44-84.
  55. Leonarduzzi G, Sottero B, Poli G. Targeting tissue oxidative damage by means of cell signaling modulators: the antioxidant concept revisited. Pharmacol Ther 2010;128:336-74.
  56. Salekzamani S, Ebrahimi-Mameghani M, Rezazadeh K. The antioxidant activity of artichoke (Cynara scolymus): a systematic review and meta-analysis of animal studies. Phytother Res 2019;33:55-71.
  57. Huber R, Muller M, Naumann J, Schenk T, Ludtke R. Artichoke leave extract for chronic hepatitis C - a pilot study. Phytomedicine 2009;16:801-4.