DOI QR코드

DOI QR Code

Plant Extracts Inhibiting Biofilm Formation by Streptococcus mutans without Antibiotic Activity

  • Ham, Youngseok (Department of Forest Products and Biotechnology, Kookmin University) ;
  • Kim, Tae-Jong (Department of Forest Products and Biotechnology, Kookmin University)
  • Received : 2018.07.10
  • Accepted : 2018.10.24
  • Published : 2018.11.25

Abstract

Streptococcus mutans causes oral diseases, including tooth decay, by producing a biofilm called plaque. Therefore, inhibition of biofilm formation is essential for maintaining oral health. Plants produce a variety of secondary metabolites, which act as starting sources for the discovery of new bioactive chemicals that inhibit biofilm formation of S. mutans. Previous studies have reported on chemicals with antibiotic activity for the inhibition of biofilm formation by S. mutans. In this study, nine plant extracts from Melonis Pedicellus, Agastachis Herba, Mori Cortex Radicis, Diospyros kaki leaves, Agrimoniae Herba, Polygoni Multiflori Radix, Lycopi Herba, Elsholtziae Herba, and Schizonepetae Spica were screened for the inhibition of biofilm formation from a plant extract library. The water-soluble compounds of the extracts did not affect cell growth but selectively inhibited biofilm formation. These results suggest that the selected plant extracts constitute novel biofilm formation inhibitors, with a novel biological mechanism, for improving oral hygiene.

Keywords

References

  1. Ahn, S.J., Ahn, S.J., Wen, Z.T., Brady, L.J., Burne, R.A. 2008. Characteristics of biofilm formation by Streptococcus mutans in the presence of saliva. Infection and Immunity 76(9): 4259-4268. https://doi.org/10.1128/IAI.00422-08
  2. Arakawa, H., Takasaki, M., Tajima, N., Fukamachi, H., Igarashi, T. 2014. Antibacterial activities of persimmon extracts relate with their hydrogen peroxide concentration. Biological and Pharmaceutical Bulletin 37(7): 1119-1123. https://doi.org/10.1248/bpb.b13-00952
  3. Beck, J., Garcia, R., Heiss, G., Vokonas, P.S., Offenbacher, S. 1996. Periodontal disease and cardiovascular disease. Journal of Periodontology 67 Suppl 10S: 1123-1137. https://doi.org/10.1902/jop.1996.67.10s.1123
  4. Berbari, E.F., Cockerill, F.R., Steckelberg, J.M. 1997. Infective endocarditis due to unusual or fastidious microorganisms. Mayo Clinic Proceedings 72(6): 532-542. https://doi.org/10.4065/72.6.532
  5. Bowen, W.H., Koo, H. 2011. Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Research 45(1): 69-86. https://doi.org/10.1159/000324598
  6. Brauner, A., Fridman, O., Gefen, O., Balaban, N.Q. 2016. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nature Reviews Microbiology 14(5): 320-330. https://doi.org/10.1038/nrmicro.2016.34
  7. Buduneli, N., Baylas, H., Buduneli, E., Turkoglu, O., Kose, T., Dahlen, G. 2005. Periodontal infections and pre-term low birth weight: a case-control study. Journal of Clinical Periodontology 32(2): 174-181. https://doi.org/10.1111/j.1600-051X.2005.00670.x
  8. Chan, Y.C., Wang, M.F., Chen, Y.C., Yang, D.Y., Lee, M.S., Cheng, F.C. 2003. Long-term administration of Polygonum multiflorum Thunb. reduces cerebral ischemia-induced infarct volume in gerbils. The American Journal of Chinese Medicine 31(1): 71-77. https://doi.org/10.1142/S0192415X03000734
  9. Choi, S.G., Kim, J., Sung, N.D., Son, K.H., Cheon, H.G., Kim, K.R., Kwon, B.M. 2007. Anthraquinones, Cdc25B phosphatase inhibitors, isolated from the roots of Polygonum multiflorum Thunb. Natural Product Research 21(6): 487-493. https://doi.org/10.1080/14786410601012265
  10. Dai, J., Mumper, R.J. 2010. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15(10): 7313-7352. https://doi.org/10.3390/molecules15107313
  11. Dixon, R.A. 2001. Natural products and plant disease resistance. Nature 411(6839): 843-847. https://doi.org/10.1038/35081178
  12. Dong, S.C., Jeon, H. 2009 Anti-inflammatory effect of MeOH extracts of the stem of Polygonum multiflorum in LPS-stimulated mouse peritoneal macrophages. Natural Product Sciences 15(2): 83-89
  13. Eley, B.M. 1999. Antibacterial agents in the control of supragingival plaque--a review. British Dental Journal 186(6): 286-296. https://doi.org/10.1038/sj.bdj.4800090a
  14. Glassman, P., Anderson, M., Jacobsen, P., Schonfeld, S., Weintraub, J., White, A., Gall, T., Hammersmark, S., Isman, R., Miller, C.E., Noel, D., Silverstein, S., Young, D. 2003. Practical protocols for the prevention of dental disease in community settings for people with special needs: the protocols. Special Care in Dentistry 23(5): 160-164. https://doi.org/10.1111/j.1754-4505.2003.tb00304.x
  15. Goncalves, M.O., Coutinho, W.P., Pimenta, F.P., Pereira, G.A., Pereira, J.A.A., Mattos-Guaraldi, A.L., Hirata, R. 2007. Periodontal disease as reservoir for multi-resistant and hydrolytic enterobacterial species. Letters in Applied Microbiology 44(5): 488-494. https://doi.org/10.1111/j.1472-765X.2007.02111.x
  16. Grech, J.N., Li, Q., Roufogalis, B.D., Duck, C.C. 1994. Novel Ca(2+)-ATPase inhibitors from the dried root tubers of Polygonum multiflorum. Journal of Natural Products 57(12): 1682-1687. https://doi.org/10.1021/np50114a010
  17. Guo, X.H., Liu, Z.H., Dai, C.S., Li, H., Liu, D., Li, L.S. 2001. Rhein inhibits renal tubular epithelial cell hypertrophy and extracellular matrix accumulation induced by transforming growth factor beta1. Acta Pharmacologica Sinica 22(10): 934-938.
  18. Ham, Y., Kim, T.J. 2016. Inhibitory activity of monoacylglycerols on biofilm formation in Aeromonas hydrophila, Streptococcus mutans, Xanthomonas oryzae, and Yersinia enterocolitica. SpringerPlus 5(1): 1526. https://doi.org/10.1186/s40064-016-3182-5
  19. Harborne, J.B. 1990. Role of secondary metabolites in chemical defence mechanisms in plants. Ciba Foundation Symposium 154: 126-134.
  20. Horikawa, K., Mohri, T., Tanaka, Y., Tokiwa, H. 1994. Moderate inhibition of mutagenicity and carcinogenicity of benzo[a]pyrene, 1,6-dinitropyrene and 3,9-dinitrofluoranthene by Chinese medicinal herbs. Mutagenesis 9(6): 523-526. https://doi.org/10.1093/mutage/9.6.523
  21. Huang, C.-H., Horng, L.-Y., Chen, C.-F., Wu, R.-T. 2007. Chinese herb Radix Polygoni Multiflori as a therapeutic drug for liver cirrhosis in mice. Journal of Ethnopharmacology 114(2): 199-206. https://doi.org/10.1016/j.jep.2007.07.034
  22. Islam, B., Khan, S.N., Haque, I., Alam, M., Mushfiq, M., Khan, A.U. 2008. Novel anti-adherence activity of mulberry leaves: inhibition of Streptococcus mutans biofilm by 1-deoxynojirimycin isolated from Morus alba. The Journal of Antimicrobial Chemotherapy 62(4): 751-757. https://doi.org/10.1093/jac/dkn253
  23. Jeon, J.G., Rosalen, P.L., Falsetta, M.L., Koo, H. 2011. Natural products in caries research: current (limited) knowledge, challenges and future perspective. Caries Research 45(3): 243-263. https://doi.org/10.1159/000327250
  24. Jeong, E.Y., Jeon, J.H., Lee, C.H., Lee, H.S. 2009. Antimicrobial activity of catechol isolated from Diospyros kaki Thunb. roots and its derivatives toward intestinal bacteria. Food Chemistry 115(3): 1006-1010. https://doi.org/10.1016/j.foodchem.2009.01.021
  25. Jeong, M.-J., Yang, J., Choi, W.-S., Kim, J.-W., Kim, S.J., Park, M.-J. 2017. Chemical compositions and antioxidant activities of essential oil extracted from Neolitsea aciculata (Blume) Koidz leaves. Journal of the Korean Wood Science and Technology 45(1): 96-106. https://doi.org/10.5658/WOOD.2017.45.1.96
  26. Jung, C.H., Kim, J.H., Park, S., Kweon, D.H., Kim, S.H., Ko, S.G. 2010. Inhibitory effect of Agrimonia pilosa Ledeb. on inflammation by suppression of iNOS and ROS production. Immunological Investigations 39(2): 159-170. https://doi.org/10.3109/08820130903501790
  27. Jung, J.-Y., Yang, J.-K., Lee, W.-H. 2017. Antioxidant and safety test of natural extract of Quercus mongolica. Journal of the Korean Wood Science and Technology 45(1): 116-125. https://doi.org/10.5658/WOOD.2017.45.1.116
  28. Kim, J.-W., Um, M., Lee, J.-W. 2018. Antioxidant activities of hot water extracts from different parts of Rugosa rose (Rosa rugosa Thunb.). Journal of the Korean Wood Science and Technology 46(1): 38-47. https://doi.org/10.5658/WOOD.2018.46.1.38
  29. Kim, S.-H., Lee, S.-Y., Cho, S.-M., Hong, C.-Y., Park, S.-Y., Park, M.-J., Choi, I.-G. 2017. Antioxidant activities of Cryptomeria japonica leaves extracts by extraction methods. Journal of the Korean Wood Science and Technology 45(5): 495-510. https://doi.org/10.5658/WOOD.2017.45.5.495
  30. Koo, H., Rosalen, P.L., Cury, J.A., Park, Y.K., Bowen, W.H. 2002. Effects of compounds found in propolis on Streptococcus mutans growth and on glucosyltransferase activity. Antimicrobial Agents and Chemotherapy 46(5): 1302-1309. https://doi.org/10.1128/AAC.46.5.1302-1309.2002
  31. Lee, S.-Y., Kim, S.-H., Park, M.-J., Lee, S.-S., Choi, I.-G. 2014. Antibacterial activity of essential oil from Abies holophylla against respiratory tract bacteria. Journal of the Korean Wood Science and Technology 42(5): 533-542. https://doi.org/10.5658/WOOD.2014.42.5.533
  32. Li, X., Kolltveit, K.M., Tronstad, L., Olsen, I. 2000. Systemic diseases caused by oral infection. Clinical Microbiology Reviews 13(4): 547-558. https://doi.org/10.1128/CMR.13.4.547
  33. Liyana-Pathirana, C., Shahidi, F. 2005. Optimization of extraction of phenolic compounds from wheat using response surface methodology. Food Chemistry 93(1): 47-56. https://doi.org/10.1016/j.foodchem.2004.08.050
  34. Loe, H. 2000. Oral hygiene in the prevention of caries and periodontal disease. International Dental Journal 50(3): 129-139. https://doi.org/10.1111/j.1875-595X.2000.tb00553.x
  35. Loesche, W.J. 1986. Role of Streptococcus mutans in human dental decay. Microbiological Reviews 50(4): 353-380.
  36. Lokegaonkar, S., Nabar, B. 2010. Inhibition of streptococcal biofilms using Morus alba leaf extract. Journal of Microbial World 12(2): 161-167.
  37. Lv, L., Gu, X., Tang, J., Ho, C.-T. 2007. Antioxidant activity of stilbene glycoside from Polygonum multiflorum Thunb in vivo. Food Chemistry 104(4): 1678-1681. https://doi.org/10.1016/j.foodchem.2007.03.022
  38. M. Ramadan, E., Abou-Taleb, K., F. Galal, G., S. Abdel-Hamid, N. 2017. Antibacterial, antibiofilm and antitumor activities of grape and mulberry leaves ethanolic extracts towards bacterial clinical strains. Annals of Agricultural Sciences 62(2): 151-159. https://doi.org/10.1016/j.aoas.2017.11.002
  39. Marsh, P.D., Head, D.A., Devine, D.A. 2015. Dental plaque as a biofilm and a microbial community-Implications for treatment. Journal of Oral Biosciences 57(4): 185-191. https://doi.org/10.1016/j.job.2015.08.002
  40. Nakahara, K., Kawabata, S., Ono, H., Ogura, K., Tanaka, T., Ooshima, T., Hamada, S. 1993. Inhibitory effect of Oolong tea polyphenols on glucosyltransferases of mutans Streptococci. Applied and Environmental Microbiology 59(4): 968-973.
  41. Nam, J.B., Oh, G.H., Yang, S.M., Lee, S.-E., Kang, S.-G. 2018. Evaluation of antioxidant activities of water extract from microwave torrefied oak wood. Journal of the Korean Wood Science and Technology 46(2): 178-188. https://doi.org/10.5658/WOOD.2018.46.2.178
  42. Ip, S.P., Tse, S.M., Poon, M.K.T., Ko, K.-M., Ma, C.Y. 1997. Antioxidant activities of Polygonum multiflorum Thunb., in vivo and in vitro. Phytotherapy Research 11(1): 42-44. https://doi.org/10.1002/(SICI)1099-1573(199702)11:1<42::AID-PTR940>3.0.CO;2-5
  43. Palombo, E.A. 2011. Traditional medicinal plant extracts and natural products with activity against oral bacteria: potential application in the prevention and treatment of oral diseases. Evidence-Based Complementary and Alternative Medicine 2011: 680354.
  44. Park, K.M., You, J.S., Lee, H.Y., Baek, N.I., Hwang, J.K. 2003. Kuwanon G: an antibacterial agent from the root bark of Morus alba against oral pathogens. Journal of Ethnopharmacology 84(2-3): 181-185. https://doi.org/10.1016/S0378-8741(02)00318-5
  45. Park, W.J., Lee, H.J., Yang, S.G. 1990. The inhibitory effect of sanggenon C from the root-bark of Morus alba L. on the growth and the cellular adherence of Streptococcus mutans Yakhak Hoeji 34(6): 434-438.
  46. Park, T., Lee, W.Y., Park, S.-Y., Ahn, J.K., Han, M.-S. 2005. Anticariogenic activity of Callistemon citrinus extract against Streptococcus mutans. Journal of the Korean Wood Science and Technology 33(2): 72-77.
  47. Paula, V.A., Modesto, A., Santos, K.R., Gleiser, R. 2010. Antimicrobial effects of the combination of chlorhexidine and xylitol. British Dental Journal 209(12): E19. https://doi.org/10.1038/sj.bdj.2010.887
  48. Peterson, S.N., Snesrud, E., Liu, J., Ong, A.C., Kilian, M., Schork, N.J., Bretz, W. 2013. The dental plaque microbiome in health and disease. PLOS ONE 8(3): e58487. https://doi.org/10.1371/journal.pone.0058487
  49. Saleem, M., Nazir, M., Ali, M.S., Hussain, H., Lee, Y.S., Riaz, N., Jabbar, A. 2010. Antimicrobial natural products: an update on future antibiotic drug candidates. Natural Product Reports 27(2): 238-254. https://doi.org/10.1039/B916096E
  50. Scannapieco, F.A. 1999. Role of oral bacteria in respiratory infection. Journal of Periodontology 70(7): 793-802. https://doi.org/10.1902/jop.1999.70.7.793
  51. Simoes, M., Bennett, R.N., Rosa, E.A. 2009. Understanding antimicrobial activities of phytochemicals against multidrug resistant bacteria and biofilms. Natural Product Reports 26(6): 746-757. https://doi.org/10.1039/b821648g
  52. Song, J.H., Yang, T.C., Chang, K.W., Han, S.K., Yi, H.K., Jeon, J.G. 2007. In vitro effects of a fraction separated from Polygonum cuspidatum root on the viability, in suspension and biofilms, and biofilm formation of mutans streptococci. Journal of Ethnopharmacol 112(3): 419-425. https://doi.org/10.1016/j.jep.2007.03.036
  53. Taira, J., Nanbu, H., Ueda, K. 2009. Nitric oxide-scavenging compounds in Agrimonia pilosa Ledeb on LPS-induced RAW264.7 macrophages. Food Chemistry 115(4): 1221-1227. https://doi.org/10.1016/j.foodchem.2009.01.030
  54. Tomiyama, K., Mukai, Y., Saito, M., Watanabe, K., Kumada, H., Nihei, T., Hamada, N., Teranaka, T. 2016. Antibacterial action of a condensed tannin extracted from astringent persimmon as a component of food addictive pancil PS-M on oral polymicrobial biofilms. BioMed Research International 2016: 5730748.
  55. Van den Bergh, B., Michiels, J.E., Wenseleers, T., Windels, E.M., Boer, P.V., Kestemont, D., De Meester, L., Verstrepen, K.J., Verstraeten, N., Fauvart, M., Michiels, J. 2016. Frequency of antibiotic application drives rapid evolutionary adaptation of Escherichia coli persistence. Nature Microbiology 1: 16020. https://doi.org/10.1038/nmicrobiol.2016.20
  56. Walker, C.B. 1996. The acquisition of antibiotic resistance in the periodontal microflora. Periodontology 2000 10(1): 79-88. https://doi.org/10.1111/j.1600-0757.1996.tb00069.x
  57. Welin-Neilands, J., Svensater, G. 2007. Acid tolerance of biofilm cells of Streptococcus mutans. Applied and Environmental Microbiology 73(17): 5633-5638. https://doi.org/10.1128/AEM.01049-07
  58. Wolff, L.F. 1985. Chemotherapeutic agents in the prevention and treatment of periodontal disease. Northwest Dentistry 64(6): 15-24.
  59. Yamada, Y., Yamamoto, A.Y.A., Yoneda, N., Nakatani, N. 1999. Identification of kaempferol from the leaves of Diospyros kaki and its antimicrobial activity against Streptococcus mutans. Biocontrol Science 4(2): 97-100. https://doi.org/10.4265/bio.4.97
  60. Yamaki, M., Kashihara, M., Ishiguro, K., Takagi, S. 1989. Antimicrobial principles of Xian he cao (Agrimonia pilosa). Planta medica 55(2): 169-170. https://doi.org/10.1055/s-2006-961915
  61. Zhu, L.C., Tan, J., Wang, B.C., He, R., Liu, Y.P., Zheng, C. 2009. Antioxidant activities of aqueous extract from Agrimonia pilosa LEDEB and its fractions. Chemistry & Biodiversity 6(10): 1716-1726. https://doi.org/10.1002/cbdv.200800248
  62. Zuo, G.Y., Wang, G.C., Zhao, Y.B., Xu, G.L., Hao, X.Y., Han, J., Zhao, Q. 2008. Screening of Chinese medicinal plants for inhibition against clinical isolates of methicillin-resistant Staphylococcus aureus (MRSA). Journal of Ethnopharmacology 120(2): 287-290. https://doi.org/10.1016/j.jep.2008.08.021