Journal of Ginseng Research

  • 제46권2호
  • /
  • Pages.188-205
  • /
  • 2022
  • /
  • 1226-8453(pISSN)
  • /
  • 2093-4947(eISSN)
고려인삼학회 (The Korean Society of Ginseng)
권호 표지
DOI QR코드

DOI QR Code

Effects of Panax ginseng on hyperglycemia, hypertension, and hyperlipidemia: A systematic review and meta-analysis

  • Park, Soo Hyun (Research Group of Healthcare, Korea Food Research Institute) ;
  • Chung, Sangwon (Research Group of Healthcare, Korea Food Research Institute) ;
  • Chung, Min-Yu (Research Group of Healthcare, Korea Food Research Institute) ;
  • Choi, Hyo-Kyoung (Research Group of Healthcare, Korea Food Research Institute) ;
  • Hwang, Jin-Taek (Research Group of Healthcare, Korea Food Research Institute) ;
  • Park, Jae Ho (Research Group of Healthcare, Korea Food Research Institute)
  • 투고 : 2020.12.09
  • 심사 : 2021.10.06
  • 발행 : 2022.03.01
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Panax ginseng is a medicinal plant is a material with various pharmacological activities and research suggests that it is particularly effective in representative metabolic diseases such as hyperglycemia, hypertension, and hyperlipidemia. Therefore, in this study, systematic review and meta-analysis were performed to investigate the comprehensive effect of P. ginseng on metabolic parameters representing these metabolic diseases. A total of 23 papers were collected for inclusion in the study, from which 27 datasets were collected. The investigational products included P. ginseng and Korean Red ginseng. Across the included studies, the dose ranged from 200 mg to 8 g and the supplementation period lasted from four to 24 weeks. The study subjects varied from healthy adults to those with diabetes, hypertension, obesity, and/or hyperlipidemia. As a result of the analysis, the levels of glucose and insulin area under the curves, % body fat, systolic and diastolic blood pressures, total cholesterol, triglycerides, and low-density lipoprotein cholesterol were significantly reduced in the P. ginseng group as compared with in the placebo group. In conclusion, P. ginseng supplementation may act as an adjuvant to prevent the development of metabolic diseases by improving markers related to blood glucose, blood pressure, and blood lipids.

키워드

과제정보

This study was supported by the Main Research Program from the Korea Food Research Institute (KFRI), funded by the Ministry of Science, ICT and Future Planning (E0210601-01).

참고문헌

  1. Doyle SL, Donohoe CL, Lysaght J, Reynolds JV. Visceral obesity, metabolic syndrome, insulin resistance and cancer. Proc Nutr Soc 2012;71(1):181-9. https://doi.org/10.1017/S002966511100320X
  2. Hess PL, Al-Khalidi HR, Friedman DJ, Mulder H, Kucharska-Newton A, Rosamond WR, Lopes RD, Gersh BJ, Mark DB, Curtis LH, et al. The metabolic syndrome and risk of sudden cardiac death: the atherosclerosis risk in communities study. J Am Heart Assoc 2017;6(8).
  3. Tune JD, Goodwill AG, Sassoon DJ, Mather KJ. Cardiovascular consequences of metabolic syndrome. Transl Res 2017;183:57-70. https://doi.org/10.1016/j.trsl.2017.01.001
  4. Bagry HS, Raghavendran S, Carli F. Metabolic syndrome and insulin resistance: perioperative considerations. Anesthesiology 2008;108(3):506-23. https://doi.org/10.1097/ALN.0b013e3181649314
  5. Gallagher EJ, LeRoith D, Karnieli E. The metabolic syndrome-from insulin resistance to obesity and diabetes. Endocrinol Metab Clin N Am 2008;37(3):559-79 [vii]. https://doi.org/10.1016/j.ecl.2008.05.002
  6. Baeg IH, So SH. The world ginseng market and the ginseng (Korea). J Ginseng Res 2013;37(1):1-7. https://doi.org/10.5142/jgr.2013.37.1
  7. Hong HD, Choi SY, Kim YC, Cho CW. Rapid determination of ginsenosides Rb1, Rf, and Rg1 in Korean ginseng using HPLC. J Ginseng Res 2009;33(1):8-12. https://doi.org/10.5142/JGR.2009.33.1.008
  8. Kim JH, Yi YS, Kim MY, Cho JY. Role of ginsenosides, the main active components of Panax ginseng, in inflammatory responses and diseases. J Ginseng Res 2017;41(4):435-43. https://doi.org/10.1016/j.jgr.2016.08.004
  9. Lee SM, Bae BS, Park HW, Ahn NG, Cho BG, Cho YL, Kwak YS. Characterization of Korean red ginseng (Panax ginseng Meyer): history, preparation method, and chemical composition. J Ginseng Res 2015;39(4):384-91. https://doi.org/10.1016/j.jgr.2015.04.009
  10. Metwaly AM, Lianlian Z, Luqi H, Deqiang D. Black ginseng and its saponins: preparation, phytochemistry and pharmacological effects. Molecules 2019;24(10).
  11. Ryu JS, Lee HJ, Bae SH, Kim SY, Park Y, Suh HJ, Jeong YH. The bioavailability of red ginseng extract fermented by Phellinus linteus. J Ginseng Res 2013;37(1):108-16. https://doi.org/10.5142/jgr.2013.37.108
  12. Li X, Chu S, Lin M, Gao Y, Liu Y, Yang S, Zhou X, Zhang Y, Hu Y, Wang H, et al. Anticancer property of ginsenoside Rh2 from ginseng. Eur J Med Chem 2020;203:112627. https://doi.org/10.1016/j.ejmech.2020.112627
  13. Ahuja A, Kim JH, Kim JH, Yi YS, Cho JY. Functional role of ginseng-derived compounds in cancer. J Ginseng Res 2018;42(3):248-54. https://doi.org/10.1016/j.jgr.2017.04.009
  14. Guo YH, Kuruganti R, Gao Y. Recent advances in ginsenosides as potential therapeutics against breast cancer. Curr Top Med Chem 2019;19(25):2334-47. https://doi.org/10.2174/1568026619666191018100848
  15. Wang CZ, Anderson S, Du W, He TC, Yuan CS. Red ginseng and cancer treatment. Chin J Nat Med 2016;14(1):7-16. https://doi.org/10.3724/SP.J.1009.2016.00007
  16. Zhou P, Xie W, He S, Sun Y, Meng X, Sun G, Sun X. Ginsenoside Rb1 as an anti-diabetic agent and its underlying mechanism analysis. Cells 2019;8(3).
  17. Ng TB, Yeung HW. Hypoglycemic constituents of Panax ginseng. Gen Pharmacol 1985;16(6):549-52. https://doi.org/10.1016/0306-3623(85)90140-5
  18. Kim S, Shin BC, Lee MS, Lee H, Ernst E. Red ginseng for type 2 diabetes mellitus: a systematic review of randomized controlled trials. Chin J Integr Med 2011;17(12):937-44. https://doi.org/10.1007/s11655-011-0937-2
  19. Bai L, Gao J, Wei F, Zhao J, Wang D, Wei J. Therapeutic potential of ginsenosides as an adjuvant treatment for diabetes. Front Pharmacol 2018;9:423. https://doi.org/10.3389/fphar.2018.00423
  20. Irfan M, Kim M, Rhee MH. Anti-platelet role of Korean ginseng and ginsenosides in cardiovascular diseases. J Ginseng Res 2020;44(1):24-32. https://doi.org/10.1016/j.jgr.2019.05.005
  21. Chen X. Cardiovascular protection by ginsenosides and their nitric oxide releasing action. Clin Exp Pharmacol Physiol 1996;23(8):728-32. https://doi.org/10.1111/j.1440-1681.1996.tb01767.x
  22. Luo BY, Jiang JL, Fang YF, Yang F, Yin MD, Zhang BC, Zhao RR, Shao JW. The effects of ginsenosides on platelet aggregation and vascular intima in the treatment of cardiovascular diseases: from molecular mechanisms to clinical applications. Pharmacol Res 2020;159:105031. https://doi.org/10.1016/j.phrs.2020.105031
  23. Kim JH. Pharmacological and medical applications of Panax ginseng and ginsenosides: a review for use in cardiovascular diseases. J Ginseng Res 2018;42(3):264-9. https://doi.org/10.1016/j.jgr.2017.10.004
  24. Zheng SD, Wu HJ, Wu DL. Roles and mechanisms of ginseng in protecting heart. Chin J Integr Med 2012;18(7):548-55. https://doi.org/10.1007/s11655-012-1148-1
  25. Kim KH, Lee D, Lee HL, Kim CE, Jung K, Kang KS. Beneficial effects of Panax ginseng for the treatment and prevention of neurodegenerative diseases: past findings and future directions. J Ginseng Res 2018;42(3):239-47. https://doi.org/10.1016/j.jgr.2017.03.011
  26. Hou W, Wang Y, Zheng P, Cui R. Effects of ginseng on neurological disorders. Front Cell Neurosci 2020;14:55. https://doi.org/10.3389/fncel.2020.00055
  27. Huang X, Li N, Pu Y, Zhang T, Wang B. Neuroprotective effects of ginseng phytochemicals: recent perspectives. Molecules 2019;24(16).
  28. Kim HJ, Jung SW, Kim SY, Cho IH, Kim HC, Rhim H, Kim M, Nah SY. Panax ginseng as an adjuvant treatment for Alzheimer's disease. J Ginseng Res 2018;42(4):401-11. https://doi.org/10.1016/j.jgr.2017.12.008
  29. Razgonova MP, Veselov VV, Zakharenko AM, Golokhvast KS, Nosyrev AE, Cravotto G, Tsatsakis A, Spandidos DA. Panax ginseng components and the pathogenesis of Alzheimer's disease (Review). Mol Med Rep 2019;19(4):2975-98.
  30. Hernandez-Garcia D, Granado-Serrano AB, Martin-Gari M, Naudi A, Serrano JC. Efficacy of Panax ginseng supplementation on blood lipid profile. A meta-analysis and systematic review of clinical randomized trials. J Ethnopharmacol 2019;243:112090. https://doi.org/10.1016/j.jep.2019.112090
  31. Park HS, Cho JH, Kim KW, Chung WS, Song MY. Effects of Panax ginseng on obesity in animal models: a systematic review and meta-analysis. Evid Based Complement Alternat Med 2018;2018:2719794.
  32. Zhang L, Virgous C, Si H. Ginseng and obesity: observations and understanding in cultured cells, animals and humans. J Nutr Biochem 2017;44:1-10. https://doi.org/10.1016/j.jnutbio.2016.11.010
  33. Duval S, Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000;56(2):455-63. https://doi.org/10.1111/j.0006-341X.2000.00455.x
  34. Kim JY, Park JY, Kang HJ, Kim OY, Lee JH. Beneficial effects of Korean red ginseng on lymphocyte DNA damage, antioxidant enzyme activity, and LDL oxidation in healthy participants: a randomized, double-blind, placebo-controlled trial. Nutr J 2012;11:47. https://doi.org/10.1186/1475-2891-11-47
  35. Reay JL, Scholey AB, Milne A, Fenwick J, Kennedy DO. Panax ginseng has no effect on indices of glucose regulation following acute or chronic ingestion in healthy volunteers. Br J Nutr 2009;101(11):1673-8. https://doi.org/10.1017/S0007114508123418
  36. Bang H, Kwak JH, Ahn HY, Shin DY, Lee JH. Korean red ginseng improves glucose control in subjects with impaired fasting glucose, impaired glucose tolerance, or newly diagnosed type 2 diabetes mellitus. J Med Food 2014;17(1):128-34. https://doi.org/10.1089/jmf.2013.2889
  37. Choi HS, Kim S, Kim MJ, Kim MS, Kim J, Park CW, Seo D, Shin SS, Oh SW. Efficacy and safety of Panax ginseng berry extract on glycemic control: a 12-wk randomized, double-blind, and placebo-controlled clinical trial. J Ginseng Res 2018;42(1):90-7. https://doi.org/10.1016/j.jgr.2017.01.003
  38. Kim HO, Park MJ, Han JS. Effects of fermented red ginseng supplementation on blood glucose and insulin resistance in type 2 diabetic patients. J Korean Soc Food Sci Nutr 2011;40(5):696-703. https://doi.org/10.3746/JKFN.2011.40.5.696
  39. Ma SW, Benzie IF, Chu TT, Fok BS, Tomlinson B, Critchley LA. Effect of Panax ginseng supplementation on biomarkers of glucose tolerance, antioxidant status and oxidative stress in type 2 diabetic subjects: results of a placebo-controlled human intervention trial. Diabetes Obes Metabol 2008;10(11):1125-7. https://doi.org/10.1111/j.1463-1326.2008.00858.x
  40. Oh MR, Park SH, Kim SY, Back HI, Kim MG, Jeon JY, Ha KC, Na WT, Cha YS, Park BH, et al. Postprandial glucose-lowering effects of fermented red ginseng in subjects with impaired fasting glucose or type 2 diabetes: a randomized, double-blind, placebo-controlled clinical trial. BMC Compl Alternative Med 2014;14:237. https://doi.org/10.1186/1472-6882-14-237
  41. Park K, Ahn CW, Kim Y, Nam JS. The effect of Korean red ginseng on sarcopenia biomarkers in type 2 diabetes patients. Arch Gerontol Geriatr 2020;90:104108. https://doi.org/10.1016/j.archger.2020.104108
  42. Park K, Kim Y, Kim J, Kang S, Park JS, Ahn CW, Nam JS. Supplementation with Korean red ginseng improves current perception threshold in Korean type 2 diabetes patients: a randomized, double-blind, placebo-controlled trial. J Diabetes Res 2020;2020:5295328.
  43. Park SH, Oh MR, Choi EK, Kim MG, Ha KC, Lee SK, Kim YG, Park BH, Kim DS, Chae SW. An 8-wk, randomized, double-blind, placebo-controlled clinical trial for the antidiabetic effects of hydrolyzed ginseng extract. J Ginseng Res 2014;38(4):239-43. https://doi.org/10.1016/j.jgr.2014.05.006
  44. Reeds DN, Patterson BW, Okunade A, Holloszy JO, Polonsky KS, Klein S. Ginseng and ginsenoside Re do not improve beta-cell function or insulin sensitivity in overweight and obese subjects with impaired glucose tolerance or diabetes. Diabetes Care 2011;34(5):1071-6. https://doi.org/10.2337/dc10-2299
  45. Vuksan V, Sung MK, Sievenpiper JL, Stavro PM, Jenkins AL, Di Buono M, Lee KS, Leiter LA, Nam KY, Arnason JT, et al. Korean red ginseng (Panax ginseng) improves glucose and insulin regulation in well-controlled, type 2 diabetes: results of a randomized, double-blind, placebo-controlled study of efficacy and safety. Nutr Metabol Cardiovasc Dis 2008;18(1):46-56. https://doi.org/10.1016/j.numecd.2006.04.003
  46. Yoon JW, Kang SM, Vassy JL, Shin H, Lee YH, Ahn HY, Choi SH, Park KS, Jang HC, Lim S. Efficacy and safety of ginsam, a vinegar extract from Panax ginseng, in type 2 diabetic patients: results of a double-blind, placebo-controlled study. J Diabetes Investig 2012;3(3):309-17. https://doi.org/10.1111/j.2040-1124.2011.00185.x
  47. Cha TW, Kim M, Kim M, Chae JS, Lee JH. Blood pressure-lowering effect of Korean red ginseng associated with decreased circulating Lp-PLA2 activity and lysophosphatidylcholines and increased dihydrobiopterin level in prehypertensive subjects. Hypertens Res 2016;39(6):449-56. https://doi.org/10.1038/hr.2016.7
  48. Rhee MY, Kim YS, Bae JH, Nah DY, Kim YK, Lee MM, Kim HY. Effect of Korean red ginseng on arterial stiffness in subjects with hypertension. J Alternative Compl Med 2011;17(1):45-9. https://doi.org/10.1089/acm.2010.0065
  49. Cho YH, Ahn SC, Lee SY, Jeong DW, Choi EJ, Kim YJ, Lee JG, Lee YH, Shin BC. Effect of Korean red ginseng on insulin sensitivity in non-diabetic healthy overweight and obese adults. Asia Pac J Clin Nutr 2013;22(3):365-71.
  50. Kim SS, Kim JD, Kim H, Shin MS, Park CK, Park MH, Yang JW. The effects of red ginseng product and combined exercise on blood lipids and body composition of obese women in their twenties. J Ginseng Res 2002;26(2):59-66. https://doi.org/10.5142/JGR.2002.26.2.059
  51. Kim SS, Park HY, Byun YH, Hwang BG, Lee JH, Shim YJ, Park CK, Yang JW. The effects on the blood lipid profiles and body fat by long term administration of red ginseng product. J Ginseng Res 2002;26(2):67-73. https://doi.org/10.5142/JGR.2002.26.2.067
  52. Delui MH, Fatehi H, Manavifar M, Amini M, Ghayour-Mobarhan M, Zahedi M, Ferns G. The effects of Panax ginseng on lipid profile, pro-oxidant: antioxidant status and high-sensitivity C reactive protein levels in hyperlipidemic patients in Iran. Int J Prev Med 2013;4(9):1045-51.
  53. Jung DH, Lee YJ, Kim CB, Kim JY, Shin SH, Park JK. Effects of ginseng on peripheral blood mitochondrial DNA copy number and hormones in men with metabolic syndrome: a randomized clinical and pilot study. Compl Ther Med 2016;24:40-6. https://doi.org/10.1016/j.ctim.2015.12.001
  54. Park BJ, Lee YJ, Lee HR, Jung DH, Na HY, Kim HB, Shim JY. Effects of Korean red ginseng on cardiovascular risks in subjects with metabolic syndrome: a double-blind randomized controlled study. Korean J Fam Med 2012;33(4):190-6. https://doi.org/10.4082/kjfm.2012.33.4.190
  55. Shim JY. Korean red ginseng and metabolic syndrome. In: ClinicalTrials.gov;2012.
  56. Kim SY, Seo SK, Choi YM, Jeon YE, Lim KJ, Cho S, Choi YS, Lee BS. Effects of red ginseng supplementation on menopausal symptoms and cardiovascular risk factors in postmenopausal women: a double-blind randomized controlled trial. Menopause 2012;19(4):461-6. https://doi.org/10.1097/gme.0b013e3182325e4b
  57. Kuzuya T, Nakagawa S, Satoh J, Kanazawa Y, Iwamoto Y, Kobayashi M, Nanjo K, Sasaki A, Seino Y, Ito C, et al. Report of the Committee on the classification and diagnostic criteria of diabetes mellitus. Diabetes Res Clin Pract 2002;55(1):65-85. https://doi.org/10.1016/S0168-8227(01)00365-5
  58. Sakaguchi K, Takeda K, Maeda M, Ogawa W, Sato T, Okada S, Ohnishi Y, Nakajima H, Kashiwagi A. Glucose area under the curve during oral glucose tolerance test as an index of glucose intolerance. Diabetol Int 2016;7(1):53-8. https://doi.org/10.1007/s13340-015-0212-4
  59. Lee HJ, Lee YH, Park SK, Kang ES, Kim HJ, Lee YC, Choi CS, Park SE, Ahn CW, Cha BS, et al. Korean red ginseng (Panax ginseng) improves insulin sensitivity and attenuates the development of diabetes in Otsuka Long-Evans Tokushima fatty rats. Metabolism 2009;58(8):1170-7. https://doi.org/10.1016/j.metabol.2009.03.015
  60. Lee SH, Lee HJ, Lee YH, Lee BW, Cha BS, Kang ES, Ahn CW, Park JS, Kim HJ, Lee EY, et al. Korean red ginseng (Panax ginseng) improves insulin sensitivity in high fat fed Sprague-Dawley rats. Phytother Res 2012;26(1):142-7. https://doi.org/10.1002/ptr.3610
  61. Joseph L, Wasir JS, Misra A, Vikram NK, Goel K, Pandey RM, Chandra M, Poddar P, Kondal D. Appropriate values of adiposity and lean body mass indices to detect cardiovascular risk factors in Asian Indians. Diabetes Technol Therapeut 2011;13(9):899-906. https://doi.org/10.1089/dia.2011.0014
  62. Prentice AM, Jebb SA. Beyond body mass index. Obes Rev 2001;2(3):141-7. https://doi.org/10.1046/j.1467-789X.2001.00031.x
  63. Pi-Sunyer FX. Obesity: criteria and classification. Proc Nutr Soc 2000;59(4):505-9. https://doi.org/10.1017/S0029665100000732
  64. Chen G, Li H, Zhao Y, Zhu H, Cai E, Gao Y, Liu S, Yang H, Zhang L. Saponins from stems and leaves of Panax ginseng prevent obesity via regulating thermogenesis, lipogenesis and lipolysis in high-fat diet-induced obese C57BL/6 mice. Food Chem Toxicol 2017;106(Pt A):393-403. https://doi.org/10.1016/j.fct.2017.06.012
  65. Shin SS, Yoon M. Korean red ginseng (Panax ginseng) inhibits obesity and improves lipid metabolism in high fat diet-fed castrated mice. J Ethnopharmacol 2018;210:80-7. https://doi.org/10.1016/j.jep.2017.08.032
  66. Klop B, Elte JW, Cabezas MC. Dyslipidemia in obesity: mechanisms and potential targets. Nutrients 2013;5(4):1218-40. https://doi.org/10.3390/nu5041218
  67. Phan BA, Toth PP. Dyslipidemia in women: etiology and management. Int J Womens Health 2014;6:185-94.
  68. O'Brien T, Nguyen TT, Zimmerman BR. Hyperlipidemia and diabetes mellitus. Mayo Clin Proc 1998;73(10):969-76. https://doi.org/10.4065/73.10.969
  69. Hong SY, Kim JY, Ahn HY, Shin JH, Kwon O. Panax ginseng extract rich in ginsenoside protopanaxatriol attenuates blood pressure elevation in spontaneously hypertensive rats by affecting the Akt-dependent phosphorylation of endothelial nitric oxide synthase. J Agric Food Chem 2012;60(12):3086-91. https://doi.org/10.1021/jf204447y
  70. Nagar H, Choi S, Jung SB, Jeon BH, Kim CS. Rg3-enriched Korean Red Ginseng enhances blood pressure stability in spontaneously hypertensive rats. Integr Med Res 2016;5(3):223-9. https://doi.org/10.1016/j.imr.2016.05.006