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Improved antimicrobial effect of ginseng extract by heat transformation

  • Xue, Peng (Institute of Crop Science, Chinese Academy of Agricultural Sciences) ;
  • Yao, Yang (Institute of Crop Science, Chinese Academy of Agricultural Sciences) ;
  • Yang, Xiu-shi (Institute of Crop Science, Chinese Academy of Agricultural Sciences) ;
  • Feng, Jia (Jilin Ginseng and Pilose Antler Office) ;
  • Ren, Gui-xing (Institute of Crop Science, Chinese Academy of Agricultural Sciences)
  • Received : 2015.12.30
  • Accepted : 2016.03.02
  • Published : 2017.04.15

Abstract

Background: The incidence of halitosis has a prevalence of 22-50% throughout the world and is generally caused by anaerobic oral microorganisms, such as Fusobacterium nucleatum, Clostridium perfringens, and Porphyromonas gingivalis. Previous investigations on the structure-activity relationships of ginsenosides have led to contrasting results. Particularly, the antibacterial activity of less polar ginsenosides against halitosis-related bacteria has not been reported. Methods: Crude saponins extracted from the Panax quinquefolius leaf-stem (AGS) were treated at $130^{\circ}C$ for 3 h to obtain heat-transformed saponins (HTS). Five ginsenoside-enriched fractions (HTS-1, HTS-2, HTS-3, HTS-4, and HTS-5) and less polar ginsenosides were separated by HP-20 resin absorption and HPLC, and the antimicrobial activity and mechanism were investigated. Results: HPLC with diode-array detection analysis revealed that heat treatment induced an extensive conversion of polar ginsenosides (-Rg1/Re, -Rc, -Rb2, and -Rd) to less polar compounds (-Rg2, -Rg3, -Rg6, -F4, -Rg5, and -Rk1). The antimicrobial assays showed that HTS, HTS-3, and HTS-4 were effective at inhibiting the growth of F. nucleatum, C. perfringens, and P. gingivalis. Ginsenosides-Rg5 showed the best antimicrobial activity against the three bacteria, with the lowest values of minimum inhibitory concentration and minimum bactericidal concentration. One major reason for this result is that less polar ginsenosides can more easily damage membrane integrity. Conclusion: The results indicated that the less polar ginsenoside-enriched fraction from heat transformation can be used as an antibacterial agent to control halitosis.

References

  1. Yang WZ, Hu Y, Wu WY, Ye M, Guo DA. Saponins in the genus Panax L. (Araliaceae): a systematic review of their chemical diversity. Phytochemistry 2014;106:7-24. https://doi.org/10.1016/j.phytochem.2014.07.012
  2. Xue Y, Wen L. RP-HPLC determination of twelve ginsenosides in extract of root and stem leaf from Panax quinquefolius L. Chin J Pharmaceut Ana 2009;29:79-81.
  3. Li FL. Research Progress of Pharmacology effect about ginsenosides from stems and leaves of Panax ginseng. Guizhou Agric Sci 2013;41:54-7.
  4. Sun BS, Pan FY, Sung CK. Repetitious steaming-induced chemical transformations and global quality of black ginseng derived from Panax ginseng by $HPLC-ESI-MS/MS^{n}$ based chemical profiling approach. Biotechnol Bioproc E 2011;16:956-65. https://doi.org/10.1007/s12257-011-0079-6
  5. Kim WY, Kim JM, Han SB, Lee SK, Kim ND, Park MK, Kim CK, Park JH. Steaming of ginseng at high temperature enhances biological activity. J Nat Prod 2000;63:1702-4. https://doi.org/10.1021/np990152b
  6. Luo SL, Dang LZ, Li JF, Zou CG, Zhang KQ, Li GH. Biotransformation of saponins by endophytes isolated from Panax notoginseng. ChemBiodivers 2013;11:2021-31.
  7. Du J, Cui CH, Park SC, Kim JK, Yu HS, Jin FX, Sun CK, Kim SC, Im WT. Identification and characterization of a ginsenoside-transforming ${\beta}$-glucosidase from Pseudonocardia sp. Gsoil 1536 and its application for enhanced production of minor ginsenoside $Rg_2(S)$. PLoS ONE 2014;9:e96914. https://doi.org/10.1371/journal.pone.0096914
  8. Kim SJ, Kim JD, Ko SK. Changes in ginsenoside composition of ginseng berry extracts after a microwave and vinegar process. J Ginseng Res 2013;37:269-72. https://doi.org/10.5142/jgr.2013.37.269
  9. Wang LJ, Yang XS, Yu X, Yao Y, Ren GX. Evaluation of antibacterial and antiinflammatory activities of less polar ginsenosides produced from polar ginsenosides by heat-transformation. J Agric Food Chem 2013;61:12274-82. https://doi.org/10.1021/jf404461q
  10. Akaji EA, Folaranmi N, Ashiwaju O. Halitosis: a review of the literature on its prevalence, impact and control. Oral Health Prev Dent 2014;12:297-304.
  11. Lee SS, Zhang W, Li Y. Halitosis update: a review of causes, diagnoses, and treatments. J Calif Dent Assoc 2007;4. 258-60,262,264-8.
  12. Cortelli JR, Barbosa MD, Westphal MA. Halitosis: a review of associated factors and therapeutic approach. Braz Oral Res 2008;22:44-54. https://doi.org/10.1590/S1806-83242008000500007
  13. Carvalho MD, Tabchoury CM, Cury JA, Toledo S, Nogueira GR. Impact of mouth rinses on morning bad breath in healthy subjects. J Clin Periodontol 2004;31:85-90. https://doi.org/10.1111/j.0303-6979.2004.00452.x
  14. Fine DH, Furgang D, Sinatra K, Charles C, McGuire A, Ku LD. In vivo antimicrobial effectiveness of an essential oil-containing mouth rinse 12 h after a single use and 14 days' use. J Clin Periodontol 2005;32:335-40. https://doi.org/10.1111/j.1600-051x.2005.00674.x
  15. Muller JF, Ghosh S, Ikuma K, Stevens AM, Love NG. Chlorinated phenolinduced physiological antibiotic resistance in Pseudomonas aeruginosa. FEMS Microbiol Lett 2015;362:1-7. http://dx.doi.org/10.1093/femsle/fnv172.
  16. Sharma A, Chopra H. Chlorhexidine urticaria: a rare occurrence with a common mouthwash. Indian J Dent Res 2009;3:377-9.
  17. Park IH, Kim NY, Han SB, Kim JM, Kwon SW, Kim HJ, Park MK, Park JH. Three new dammarane glycosides from heat processed ginseng. Arch Pharm Res 2002;25:428-32. https://doi.org/10.1007/BF02976595
  18. Zhang YC, Pi ZF, Liu CM, Song FR, Liu ZQ, Liu SY. Analysis of low-polar ginsenosides in steamed panax ginseng at high-temperature by HPLC-ESI-MS/MS. Chem Res Chinese U 2012;28:31-6.
  19. In G, Ahn NG, Bae BS, Han ST, Noh KB, Kim CS. New method for simultaneous quantification of 12 ginsenosides in red ginseng powder and extract: In-house method validation. J Ginseng Res 2012;36:205-10. https://doi.org/10.5142/jgr.2012.36.2.205
  20. Wang LJ, Yang XS, Qin P, Shan F, Ren GX. Flavonoid composition, antibacterial and antioxidant properties of tartary buckwheat bran extract. Ind Crop Prod 2013;49:312-7. https://doi.org/10.1016/j.indcrop.2013.04.039
  21. Zivkovic J, Barreira JCM, Stojkovic D, Cebovic T, Santos C, Maksimovic Z, Ferreira IC. Phenolic profile, antibacterial, antimutagenic and antitumor evaluation of Veronica urticifolia Jacq. J Funct Foods 2014;9:192-201. https://doi.org/10.1016/j.jff.2014.04.024
  22. Lv F, Liang H, Yuan Q, Li C. In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res Int 2011;44:3057-64. https://doi.org/10.1016/j.foodres.2011.07.030
  23. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1975;72:248-54.
  24. Comas J, Vives-Rego J. Assessment of the effects of gramicidin, form aldehyde, and surfactants on Escherichia coli by flow cytometry using nucleic acid and membrane potential dyes. Cytometry 1997;29:58-64. https://doi.org/10.1002/(SICI)1097-0320(19970901)29:1<58::AID-CYTO6>3.0.CO;2-9
  25. Xie YY, Luo D, Chen YJ, Ma JF, Wang YM, Liang QL, Luo GA. Steaming-induced chemical transformations and holistic quality assessment of red ginseng derived from by means of HPLC-ESI-MS/MSn-based multicomponent quantification fingerprint. J Agric Food Chem 2012;60:8213-24. https://doi.org/10.1021/jf301116x
  26. Oleszek W. Alfalfa saponins: structure, biological activity, and chemotaxonomy. In: Waller GR, Yamasaki K, editors. In saponins used in food and agriculture. New York: Plenum press; 1996. p. 155-70.
  27. Oleszek W, Naidu AS. Saponins in natural food antimicrobial systems. London: CRC Press; 2000. p. 1-30.
  28. Sun H, Fang WS,Wang WZ, Hu C. Structure-activity relationships of oleananeand ursane-type triterpenoids. Bot Stud 2006;47:339-68.
  29. Wu H, Lee BL, Yang L, Wang HG, Givskov M, Molin S, Hoiby N, Song ZJ. Effects of ginseng on Pseudomonas aeruginosa motility and biofilm formation. FEMS Immunol Med Microbiol 2011;62:49-56. https://doi.org/10.1111/j.1574-695X.2011.00787.x
  30. Song ZJ, Johansen HK, Faber V, Hoiby N. Ginseng treatment enhances bacterial clearance and decreases lung pathology in athymic rats with chronic P. aeruginosa pneumonia. APMIS 1997;105:438-44. https://doi.org/10.1111/j.1699-0463.1997.tb00591.x
  31. Song ZJ, Johansen HK, Faber V, Moser C, Kharazmi A, Rygaard J, Hoiby N. Ginseng treatment reduces bacterial load and lung pathology in chronic Pseudomonas aeruginosa pneumonia in rats. Antimicrob Agents Chemother 1997;41:961-4.
  32. Bae EA, Han MJ, Choo MK, Park SY, Kim DH. Metabolism of 20 (S)- and 20 (R)-ginsenoside $Rg_3$ by human intestinal bacteria and its relation to in vitro biological activities. Biol Pharm Bull 2002;25:58-63. https://doi.org/10.1248/bpb.25.58
  33. Sung WS, Lee DG. The combination effect of Korean red ginseng saponins with kanamycin and cefotaxime against methicillin-resistant Staphylococcus aureus. Biol Pharm Bull 2008;31:1614-7. https://doi.org/10.1248/bpb.31.1614
  34. Lee KA, Kim WJ, Kim HJ, Kim KT, Paik HD. Antibacterial activity of ginseng (Panax ginseng C. A. Meyer) stems-leaves extract produced by subcritical water extraction. Int J Food Sci Tech 2013;48:947-53. https://doi.org/10.1111/ijfs.12046
  35. Norajit K, Ryu GH. Preparation and properties of antibacterial alginate films incorporating extruded white ginseng extract. J Food Process Pres 2011;35:387-93. https://doi.org/10.1111/j.1745-4549.2010.00479.x
  36. Bajpai VK, Sharma A, Baek KH. Antibacterial mode of action of Cudrania tricuspidata fruit essential oil, affecting membrane permeability and surface characteristics of food-borne pathogens. Food Control 2013;32:582-90. https://doi.org/10.1016/j.foodcont.2013.01.032
  37. Charlebois A, Jacques M, Archambault M. Biofilm formation of Clostridium perfringens and its exposure to low-dose antimicrobials. Front Microbiol 2016. http://dx.doi.org/10.3389/fmicb.2014.00183.
  38. Bachrach G, Haake SK, Glick A, Hazan R, Naor R, Andersen RN, Kolenbrander PE. Characterization of the novel Fusobacterium nucleatum plasmid pKH9 and evidence of an addiction system. Appl Environ Microbiol 2004;70:6957-62. https://doi.org/10.1128/AEM.70.12.6957-6962.2004
  39. Lasserre JF, Leprince JG, Toma S, Brecx MC. Electrical enhancement of chlorhexidine efficacy against the periodontal pathogen Porphyromonas gingivalis within a biofilm. New Microbiol 2015;38:511-9.