Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
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Influence of Panax ginseng on obesity and gut microbiota in obese middle-aged Korean women

  • Song, Mi-Young (Department of Rehabilitation Medicine of Korean Medicine, Dongguk University) ;
  • Kim, Bong-Soo (Chunlab Inc., Seoul National University) ;
  • Kim, Hojun (Department of Rehabilitation Medicine of Korean Medicine, Dongguk University)
  • Received : 2013.09.12
  • Accepted : 2013.12.13
  • Published : 2014.04.15
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Abstract

Background: Gut microbiota is regarded as one of the major factors involved in the control of body weight. The antiobesity effects of ginseng and its main constituents have been demonstrated, but the effects on gut microbiota are still unknown. Methods: To investigate the effect of ginseng on gut microbiota, 10 obese middle-aged Korean women took Panax ginseng extracts for 8 wk and assessment of body composition parameters, metabolic biomarkers, and gut microbiota composition was performed using 16S rRNA gene-based pyrosequencing at baseline and at 8 wk. Significant changes were observed in body weight and body mass index; however, slight changes were observed in gut microbiota. We divided the participants into two groups, the effective and the ineffective weight loss groups, depending on weight loss effect, in order to determine whether the antiobesity effect was influenced by the composition of gut microbiota, and the composition of gut microbiota was compared between the two groups. Results: Prior to ginseng intake, significant differences of gut microbiota were observed between both at phyla and genera and the gut microbiota of the effective and ineffective weight loss groups was segregated on a principal coordinate analysis plot. Conclusion: Results of this study indicate that ginseng exerted a weight loss effect and slight effects on gut microbiota in all participants. In addition, its antiobesity effects differed depending on the composition of gut microbiota prior to ginseng intake.

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References

  1. Li CP, Li RC. An introductory note to ginseng. Am J Chin Med 1973;1:249-61. https://doi.org/10.1142/S0192415X73000279
  2. Kim DH. Chemical diversity of Panax ginseng, Panax quinquifolium and Panax notoginseng. J Ginseng Res 2012;6:1-15.
  3. Joh EH, Lee IA, Jung IH, Kim DH. Ginsenoside Rb1 and its metabolite compound K inhibit IRAK-1 activationdthe key step of inflammation. Biochem Pharmacol 2011;2:278-86.
  4. Choo MK, Sakurai H, Kim DH, Saiki I. A ginseng saponin metabolite suppresses tumor necrosis factor-alpha-promoted metastasis by suppressing nuclear factor- kappaB signaling in murine colon cancer cells. Oncol Rep 2008;9:595-600.
  5. Kang S, Min H. Ginseng, the 'immunity boost': the effects of Panax ginseng on immune system. J Ginseng Res 2012;36:354-68. https://doi.org/10.5142/jgr.2012.36.4.354
  6. Gu J, Li W, Xiao D, Wei S, Cui W, Chen W, Hu Y, Bi X, Kim Y, Li J, et al. Compound K, a final intestinal metabolite of ginsenosides, enhances insulin secretion in MIN6 pancreatic b-cells by upregulation of GLUT2. Fitoterapia 2013;7:84-8.
  7. Oh J, Lee H, Park D, Ahn J, Shin SS, Yoon M. Ginseng and its active components ginsenosides inhibit adipogenesis in 3T3-L1 cells by regulating MMP-2 and MMP-9. Evid Based Complement Alternat Med 2012;2012:265023.
  8. 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;58:1170-7. https://doi.org/10.1016/j.metabol.2009.03.015
  9. 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 SpragueeDawley rats. Phytother Res 2012;26:142-7. https://doi.org/10.1002/ptr.3610
  10. 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;60:3086-91. https://doi.org/10.1021/jf204447y
  11. James PT, Rigby N, Leach R, International Obesity Task Force. The obesity epidemic, metabolic syndrome and future prevention strategies. Eur J Cardiovasc Prev Rehabil 2004;11:3-8. https://doi.org/10.1097/01.hjr.0000114707.27531.48
  12. Bäckhed F, Crawford PA. Coordinated regulation of the metabolome and lipidome at the host-microbial interface. Biochim Biophys Acta 2010;1801:240-5. https://doi.org/10.1016/j.bbalip.2009.09.009
  13. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008;3:213-23. https://doi.org/10.1016/j.chom.2008.02.015
  14. Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 2009;15:1546-58. https://doi.org/10.2174/138161209788168164
  15. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M. Gut microbiota in human adults with type 2 diabetes differs from nondiabetic adults. PLoS One 2010;5:e9085. https://doi.org/10.1371/journal.pone.0009085
  16. Angelakis E, Armougom F, Million M, Raoult D. The relationship between gut microbiota and weight gain in humans. Future Microbiol 2012;7:91-109. https://doi.org/10.2217/fmb.11.142
  17. Harris K, Kassis A, Major G, Chou CJ. Is the gut microbiota a new factor contributing to obesity and its metabolic disorders? J Obes 2012;2012:879151.
  18. Million M, Raoult D. The role of the manipulation of the gut microbiota in obesity. Curr Infect Dis Rep 2013;15:25-30. https://doi.org/10.1007/s11908-012-0301-5
  19. Choi JR, Hong SW, Kim Y, Jang SE, Kim NJ, Han MJ, Kim DH. Metabolic activities of ginseng and its constituents, ginsenoside Rb1 and Rg1, by human intestinal microflora. J Ginseng Res 2011;35:301-7. https://doi.org/10.5142/jgr.2011.35.3.301
  20. Kim KA, Jung IH, Park SH, Ahn YT, Huh CS, Kim DH. Comparative analysis of the gut microbiota in people with different levels of ginsenoside Rb1 degradation to compound K. PLoS One 2013;8:e62409. https://doi.org/10.1371/journal.pone.0062409
  21. World Health Organization. Measuring obesity: classification and distribution of anthropometric data. Copenhagen: WHO; 1989.
  22. Hur M, Kim Y, Song HR, Kim JM, Choi YI, Yi H. Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings. Appl Environ Microbiol 2011;77:7611-9. https://doi.org/10.1128/AEM.06102-11
  23. Chunlab, Technical note_454 amplicon primer design [Internet]. 2013 [cited 2013 Mar 5]. Available from: http://oklbb.ezbiocloud.net/content/1001.
  24. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol 2011;7: e1002195. https://doi.org/10.1371/journal.pcbi.1002195
  25. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012;62:716-21. https://doi.org/10.1099/ijs.0.038075-0
  26. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194-200. https://doi.org/10.1093/bioinformatics/btr381
  27. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 2009;75:7537-41. https://doi.org/10.1128/AEM.01541-09
  28. Chunlab, Sequence data for influence of Panax Ginseng on gut microbiota [Internet]. 2013 [cited 2013 May 5]. Available from: http://www.ebi.ac.uk/ ena/data/view/PRJEB4531.
  29. Mueller S, Saunier K, Hanisch C, Norin E, Alm L, Midtvedt T, Cresci A, Silvi S, Orpianesi C, Verdenelli MC, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a crosssectional study. Appl Environ Microbiol 2006;2:1027-33.
  30. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature 2012;486:222-7.
  31. Kwon DH, Bose S, Song MY, Lee MJ, Lim CY, Kwon BS, Kim HJ. Efficacy of Korean Red Ginseng by single nucleotide polymorphism in obese women: randomized, double-blind, placebo-controlled trial. J Ginseng Res 2012;36: 176-89. https://doi.org/10.5142/jgr.2012.36.2.176
  32. 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;22:365-71.
  33. Wang HY, Qi LW, Wang CZ, Li P. Bioactivity enhancement of herbal supplements by intestinal microbiota focusing on ginsenosides. Am J Chin Med 2011;39(6):1103-15. https://doi.org/10.1142/S0192415X11009433
  34. Wakabayashi C, Hasegawa H, Murata J, Saiki I. In vivo antimetastatic action of ginseng protopanaxadiol saponins is based on their intestinal bacterial metabolites after oral administration. Oncol Res 1997;9:411-7.
  35. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The human microbiome project. Nature 2007;449:804-10. https://doi.org/10.1038/nature06244
  36. Lee J, Lee E, Kim D, Lee J, Yoo J, Koh B. Studies on absorption, distribution and metabolism of ginseng in humans after administration. J Ethnopharmaol 2009;122:143-8. https://doi.org/10.1016/j.jep.2008.12.012

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