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Effects of Fermented Red Ginseng Supplementation on Blood Glucose and Insulin Resistance in Type 2 Diabetic Patients

발효홍삼이 제2형 당뇨병 환자의 혈당 및 인슐린저항성에 미치는 영향

  • Kim, Hey-Ok (Dept. of Food Science and Nutrition, Pusan National University) ;
  • Park, Min-Jung (Dept. of Food Science and Nutrition, Pusan National University) ;
  • Han, Ji-Sook (Dept. of Food Science and Nutrition, Pusan National University)
  • 김혜옥 (부산대학교 식품영양학과) ;
  • 박민정 (부산대학교 식품영양학과) ;
  • 한지숙 (부산대학교 식품영양학과)
  • Received : 2011.03.07
  • Accepted : 2011.05.02
  • Published : 2011.05.31

Abstract

We performed a randomized placebo-controlled trial to determine whether or not fermented red ginseng supplementation modulates blood glucose and insulin resistance in type 2 diabetic patients. A total of 38 patients were randomized to either a fermented red ginseng group or placebo group. The patients in the experimental or placebo group consumed 780 mg of fermented red ginseng or cellulose supplement per day for 12 weeks, respectively. Lifestyle factors and dietary intakes of the patients were not altered during the 12-weeks period. In the fermented red ginseng group after 12 weeks, the fasting blood glucose levels were significantly decreased ($136.29{\pm}16.45$ mg/dL to $127.71{\pm}17.74$ mg/dL) and $HbA_1c$ was also decreased. Especially, high HbA1c (HbA1c $\geq$8%, $8.45{\pm}0.56%$ to $7.82{\pm}0.53%$) was significantly decreased compared to low HbA1c (HbA1c <8%, $6.71{\pm}0.85%$ to $6.44{\pm}0.49%$) in the fermented red ginseng group. Serum low-density lipoprotein was slightly decreased in the fermented red ginseng group compared to the placebo group. Homeostasis model assessment-insulin resistance was significantly reduced in the fermented red ginseng group compared to the placebo group. These results suggest that fermented red ginseng supplementation could be helpful to reduce blood glucose by improving insulin resistance in type 2 diabetic patients.

본 연구는 홍삼추출물을 Bifidobacterium longum H-1으로 발효시켜 인삼사포닌을 체내에서 흡수가 잘 되는 형태로 변화시킨 발효홍삼을 제2형 당뇨병환자에게 아침과 저녁 식전에 한 캡슐씩 하루 780 mg을 섭취하였다. 위약군은 동량의 cellulose를 실험군과 동일하게 제조한 후 같은 방법으로 섭취하도록 하였다. 연구대상자는 약물이나 식사로만 치료하는 총 38명의 제2형 당뇨병 환자로 발효홍삼군 20명(남자 12, 여자 8), 위약군 18명(남자 11, 여자 7)으로 구성되었으며, 두 군의 일반적 특성 및 생활습관은 유의적인 차이가 없었다. 연구결과 발효홍삼을 섭취한 군에서의 공복혈당은 $136.29{\pm}16.45$ mg/dL에서 $127.71{\pm}17.74$ mg/dL로 유의하게(p<0.05) 감소하였으며, 당화혈색소 역시 $7.36{\pm}1.02%$에서 $6.96{\pm}0.93%$로 감소하였다. 특히 당화혈색소가 8% 이상인 고당화혈색소군에서 유의적으로(p<0.05) 감소하는 것으로 나타났다. 인슐린 저항성은 대조군에서는 유의적 변화가 없는 반면, 발효홍삼군에서는 섭취 전 $3.11{\pm}1.13$ mmol/L에서 섭취 후 $2.23{\pm}0.71$ mmol/L로 유의한(p<0.01) 감소를 나타내었다. 혈청지질 변화는 없었으며, LDL-콜레스테롤도 발효홍삼군에서 유의한 변화가 없었다. 간 기능 지표인 AST, ALT, ${\gamma}$-GTP와 신장기능 지표인 BUN, creatinine에서 유의적인 차이를 나타내지 않았으며, 정상범위에 속하여 발효홍삼의 안전성을 확인하였다. 이상의 연구 결과 한국인 제2형 당뇨병 환자에 있어 발효홍삼은 혈당 및 당화혈색소 감소와 인슐린 저항성 개선에 효과적인 것으로 나타났으며, 인체 안전성 지표인 간 및 신장 기능도 정상으로 확인되었으므로 당뇨병 환자의 혈당 개선을 통해 합병증지연 또는 예방에 있어 효과를 기대할 수 있을 것으로 사료된다.

Keywords

References

  1. Van de Laar FA. 2008. Alpha-glucosidase inhibitors in the early treatment of type 2 diabetes. Vasc Health Risk Manag 4: 1189-1195. https://doi.org/10.2147/VHRM.S3119
  2. Hillebrand I, Boehme K, Frank G, Fink H, Berchtold P. 1979. The effects of the alpha-glucosidase inhibitor BAY g 5421 (Acarbose) on meal-stimulated elevations of circulating glucose, insulin and triglyceride levels in man. Res Exp Med 175: 81-86. https://doi.org/10.1007/BF01851236
  3. Fonteles MC, Huang LC, Larner J. 1996. Infusion of pH 2.0 D-chiro-inositol glycan insulin putative mediator normalizes plasma glucose in streptozotocin diabetic rats at a dose equivalent to insulin without inducing hypoglycaemia. Diabetologia 39: 731-734. https://doi.org/10.1007/BF00418546
  4. Melander A, Lebovitz HE, Faber OK. 1990. Sulfonylureas. Why, which, and how? Diabetes Care 13: 18-25.
  5. Grover JK, Vats V, Rathi SS. 2000. Anti-hyperglycemic effect of Eugenia jambolana and Tinospora cordifolia in experimental diabetes and their effects on key metabolic enzymes involved in carbohydrate metabolism. J Ethnopharmacol 73: 461-470. https://doi.org/10.1016/S0378-8741(00)00319-6
  6. Vuksan V, Sung MK, Sievenpiper JL, Stavro PM, Jenkins AL, Di Buono M, Lee KS, Leiter LA, Nam KY, Arnason JT, Choi M, Naeem A. 2006. Korean red ginseng (Panax ginseng) improves glucose and insulin regulation in wellcontrolled, type 2 diabetes: Results of a randomized, double- blind, placebo-controlled study of efficacy and safety. Nutr Metab Cardiovasc Dis 18: 46-56.
  7. Sievenpiper JL, Sung MK, Buono MD, Lee KS, Nam KY, Arnason JT, Leiter LA, Vuksan V. 2006. Korean red ginseng rootlets decrease acute postprandial glycemia: Results from sequential preparation- and dose-finding studies. J Am Coll Nutr 25: 100-107. https://doi.org/10.1080/07315724.2006.10719519
  8. Vuksan V, Sievenpiper JL, Koo VY, Francis T, Beljan- Zdravkovic U, Xu Z, Vidgen E. 2000. American ginseng (Panax quinquefolius L.) reduces postprandial glycemia in nondiabetic subjects and subjects with type 2 diabetes mellitus. Arch Intern Med 160: 1009-1013. https://doi.org/10.1001/archinte.160.7.1009
  9. Vuksan V, Stavro MP, Sievenpiper JL, Koo VY, Wong E, Beljan-Zdravkovic U, Francis T, Jenkins AL, Leiter LA, Josse RG, Xu Z. 2000. American ginseng improves glycemia in individuals with normal glucose tolerance: effect of dose and time escalation. J Am Coll Nutr 19: 738-744. https://doi.org/10.1080/07315724.2000.10718073
  10. Vuksan V, Sievenpiper JL, Wong J, Xu Z, Beljan-Zdravkovic U, Arnason JT, Assinewe V, Stavro MP, Jenkins AL, Leiter LA, Francis T. 2001. American ginseng (Panax quinquefolius L.) attenuates postprandial glycemia in a time-dependent but not dose-dependent manner in healthy individuals. Am J Clin Nutr 73: 753-758.
  11. Kim DJ, Seong KS, Kim DW, Ko SR, Chang CC. 2004. Antioxidative effects of red ginseng saponins on paraquat- induced oxidative stress. J Ginseng Res 28: 5-10. https://doi.org/10.5142/JGR.2004.28.1.005
  12. Choi JE, Han JS, Kang SJ, Kim KH, Kim KH, Yook HS. 2010. Saponin contents and physicochemical properties of red ginseng extract pouch products collected from ginseng markets in Korea. J Korean Soc Food Sci Nutr 39: 1660-1665. https://doi.org/10.3746/jkfn.2010.39.11.1660
  13. Shin YS. 2010. Comparisons of ginsenosides and anti-inflammatory effects of white ginseng and puffed red ginseng. Korean J Food Sci 26: 475-480.
  14. Sanata S, Kondo N, Shoji J, Tanaka O, Shibata S. 1974. Studies on the saponins of ginseng. I. Structure of ginsenoside- $R_0$, $Rb_1$, $Rb_2$, Rc and Rd. Chem Pharm Bull (Tokyo) 22: 421-428. https://doi.org/10.1248/cpb.22.421
  15. Kitagawa I, Taniyama T, Shibuya H, Nota T, Yoshikawa M. 1987. Chemical studies on crude drug processing. V. On the constituents of ginseng radix ruba (2): Comparison of the constituents of white ginseng and red ginseng prepared from the same Panax ginseng root. Yakugaku Zasshi 107: 495-505. https://doi.org/10.1248/yakushi1947.107.7_495
  16. Kimura M, Waki L, Chujo T, Kikuchi T, Hiyama C, Yamazaki K, Tanaka O. 1981. Effects of hypoglycemic components in ginseng radix on blood insulin level in alloxan diabetic mice and on insulin release from perfused rat pancreas. J Pharm Dyn 4: 410-417. https://doi.org/10.1248/bpb1978.4.410
  17. Yokozawa, KobaYashi T, Oura H, Kawashima Y. 1985. Studies on the mechanism of the hypoglycemic activity of ginsenoside-$Rb_2$ in streptozotocin-diabetic rats. Chem Pharm Bull (Tokyo) 33: 869-872. https://doi.org/10.1248/cpb.33.869
  18. Kim CM, Han GS. 1985. Radioprotective effects of ginseng proteins. Yakhak Hoeji 29: 246-252.
  19. Park SJ, Kim DH, Kim SS. 2006. Preparation and quality characteristics of the fermentation product of ginseng by lactic acid bacteria (FGL). J Ginseng Res 30: 88-94. https://doi.org/10.5142/JGR.2006.30.2.088
  20. Je JH. 2007. Antidiabetic and oxidative stress relieving effects of fermented red ginseng. MS Thesis. Pusan National University, Busan, Korea.
  21. Seoul Medical Science Institute. 2005. SCL examination guidebook.
  22. Friedewald WT, Levy RI, Fredrickson DS. 1972. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18: 499-502.
  23. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Tuner RC. 1985. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419. https://doi.org/10.1007/BF00280883
  24. Buckingham KW. 1985. Effect of dietary polyunsaturated/ saturated fatty acid ratio and dietary vitamin E on lipid peroxidation in the rat. J Nutr 115: 1425-1435.
  25. Lee KH. 2010. A comparative study on obesity judgment criteria in the frequently used obesity indices. The Res J Costume Culture 18: 93-108.
  26. Cho NH. 2005. Prevalence of diabetes and management status in Korean population. Kor J Medicine 68: 1-3.
  27. Korean National Health and Nutrition Examination Survey. 2008. Ministry for Health and Welfare, Korea.
  28. The Korean Nutrition Society. 2006. Dietary Reference Intakes for Koreans.
  29. Ng TB, Yeung HW, Lee HB. 1985. Hypoglycemic constituents of Panax ginseng. Gen Pharmacol 16: 549-552. https://doi.org/10.1016/0306-3623(85)90140-5
  30. Lee HA, Kwon SO. 1997. Hypoglycemic action of components from red ginseng: (I) Investigation of the effect of ginsenosides from red ginseng on enzymes related to glucose metabolism in cultured rat hepatocytes. Korean J Ginseng Sci 21: 174-186.
  31. Takagi H, Umemoto T. 2011. Low-density lipoprotein cholesterol- independent effects of statins on coronary artery disease. Am J Cardiol 107: 336-343.
  32. Remsberg KE, Talbott EO, Zborowski JV, Evans RW, McHugh-Pemu K. 2002. Evidence for competing effects of body mass, hyperinsulinemia, insulin resistance, and androgens on leptin levels among lean, overweight, and obese women with polycystic ovary syndrome. Fertil Steril 78: 479-486. https://doi.org/10.1016/S0015-0282(02)03303-4
  33. Kang JM, Lee WY, Kim JY, Yun JW, Kim SW. 2002. Relationship between C-peptide, metabolic control and chronic complications in type 2 diabetes. Korean Diabetes J 26: 490-499.
  34. Isomaa B. 2003. A major health hazard: the metabolic syndrome. Life Sci 73: 2395-2411. https://doi.org/10.1016/S0024-3205(03)00646-5
  35. Beck-Nielsen H. 1999. General characteristics of the insulin resistance syndrome: prevalence and heritability. European Group for the study of Insulin Resistance (EGIR). Drugs 58 (Suppl. I: 7-10); discussion 75-82.
  36. Rhee SY, Chon S, Oh S, Kim SW, Kim JW, Kim YS, Woo JT. 2007. Insulin secretion and insulin resistance in newly diagnosed, drug naive prediabetes and type 2 diabetes patients with/without metabolic syndrome. Diabetes Res Clin Pract 76: 397-403. https://doi.org/10.1016/j.diabres.2006.09.035
  37. Qu X, Pan X, Weidner J, Yu W, Alonzi D, Xu X, Butters T, Block T, Guo JT, Chang J. 2011. Inhibitors of endoplasmic reticulum {alpha}-glucosidases potently suppress hepatitis C virus virion assembly and release. Antimicrob Agents Chemother 55: 1036-1044. https://doi.org/10.1128/AAC.01319-10
  38. Singh N, Rana SV. 2009. Effect of insulin on arsenic toxicity in diabetic rats-liver function studies. Biol Trace Elem Res 132: 215-226. https://doi.org/10.1007/s12011-009-8396-8
  39. Kim HS, Lee JH, Park EJ, Yoon JY, Kim JM, Lim HS, Lee HC, Huh KB. 1994. Effect of enteral nutrition supplementation on glucose metabolism in patients with NIDDM. Korean J Nutr 27: 805-818.

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