Skip to main content

Advertisement

Log in

Sustained Release of a Purified Tannin Component of Terminalia chebula from a Titanium Implant Surface Prevents Biofilm Formation by Staphylococcus aureus

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Although biofilms are formed on a variety of surfaces, of utmost significance are those formed on prosthetic devices used as implants. Such biofilms can lead to severe device-related infections that are difficult to treat. In a search for new antibiofilm agents that can be used as “active” implant coatings, purified fraction from a tannin-rich extract of Terminalia chebula was isolated and tested for its antibiofilm properties on a titanium implant material. The fraction, named as Fraction 7, was found to significantly reduce biofilm formation by hospital isolates of Staphylococcus aureus, at sub-inhibitory concentrations that were 64 times lower than the minimum inhibitory concentration (MIC). Simulated local delivery systems of the Fraction 7 set upon the surface of titanium alloy released the fraction in a controlled manner from a biodegradable carrier (PDLLA) and were found to significantly reduce biofilm formation by a methicillin-resistant hospital isolate of S. aureus in a load concentration dependent manner without preventing growth. This study therefore identifies a novel fraction from tannin-rich extract of T. chebula that has potential to be used as an antibiofilm coat on implant surfaces.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Rochford, E. T. J., Richards, R. G., & Moriarty, T. F. (2012). Influence of material on the development of device-associated infections. Clinical Microbiology and Infection, 18(12), 1162–1167.

    Article  CAS  Google Scholar 

  2. Aviv M, Berdicevsky I, Zilberman M. (2007). Gentamicin-loaded bioresorbable films for prevention of bacterial infections associated with orthopedic implants. Journal of Biomedical Materials Research Part A 10–19.

  3. Bryers, J. D., & Ratner, B. D. (2004). Bioinspired implant materials befuddle bacteria. ASM New, 70(5), 232–237.

    Google Scholar 

  4. Navarro, M., Michiardi, A., Castaño, O., & Planell, J. A. (2008). Biomaterials in orthopaedics. Journal of the Royal Society Interface, 5(27), 1137–58.

    Article  CAS  Google Scholar 

  5. Chen, C.-P., & Wickstrom, E. (2011). Self-protecting bactericidal titanium alloy surface formed by covalent bonding of daptomycin bisphosphonates. Bioconjugate Chemistry, 21(11), 1978–1986.

    Article  Google Scholar 

  6. Harris, L. G., & Richards, R. G. (2004). Staphylococcus aureus adhesion to different treated titanium surfaces. Journal of Materials Science Materials in Medicine, 15(4), 311–4.

    Article  CAS  Google Scholar 

  7. Hetrick, E. M., & Schoenfisch, M. H. (2006). Reducing implant-related infections: active release strategies. Chemical Society Reviews, 35(9), 780–9.

    Article  CAS  Google Scholar 

  8. Darouiche, R. O. (2001). Device-associated infections: a macroproblem that starts with microadherence. Clinical Infectious Diseases : an Official Publication of the Infectious Diseases Society of America, 33(9), 1567–72.

    Article  CAS  Google Scholar 

  9. Harris, L. G., Mead, L., Muller-Oberlander, E., & Richards, R. (2006). Bacteria and cell cytocompatibility studies on coated medical grade titanium surfaces. Journal of Biomedical Materials Research, Part A, 50–58.

  10. Makadia, H. K., & Siegel, S. J. (2011). Poly Lactic-co-Glycolic Acid (PLGA) as Biodegradable Controlled Drug Delivery Carrier. Polymers, 3(3), 1377–1397.

    Article  CAS  Google Scholar 

  11. Zilberman, M., & Elsner, J. J. (2008). Antibiotic-eluting medical devices for various applications. Journal of Controlled Release, 130(3), 202–15.

    Article  CAS  Google Scholar 

  12. Bazaka, K., Jacob, M. V., Truong, V. K., et al. (2010). Plasma-enhanced synthesis of bioactive polymeric coatings from monoterpene alcohols: a combined experimental and theoretical study. Biomacromolecules, 11(8), 2016–26.

    Article  CAS  Google Scholar 

  13. Khoo, X., & Grinstaff, M. W. (2011). Novel infection-resistant surface coatings: a bioengineering approach. MRS Bulletin, 36(05), 357–366.

    Article  CAS  Google Scholar 

  14. Daniel.M. (2006) Medicinal Plants: Chemistry and Properties Science Publishers.

  15. Gupta, A., Tandon, N., & Sharma, M. (Eds.). (2003). Quality Standards of Indian Medicinal Plants Volume 1.

  16. The Ayurvedic Pharmacopoeia of India Part I Volume 1. (n.d.) (1st ed.). Government of India, Ministry of Health & Family Welfare, Dept of Indian System of Medicine and Homeopathy.

  17. Ghosh, A., Das, B. K., Roy, A., Mandal, B., & Chandra, G. (2008). Antibacterial activity of some medicinal plant extracts. Journal of Natural Medicines, 62(2), 259–62.

    Article  Google Scholar 

  18. Bag, A., Bhattacharyya, S. K., Chattopadhyay, R. R., & Rashid, R. A. (2013). The development of Terminalia chebula Retz. (Combretaceae) in clinical research. Asian Pacific Journal of Tropical Biomedicine, 3(3), 244–52.

    Article  Google Scholar 

  19. Taganna, J. C., Quanico, J. P., Perono, R. M. G., Amor, E. C., & Rivera, W. L. (2011). Tannin-rich fraction from Terminalia catappa inhibits quorum sensing (QS) in Chromobacterium violaceum and the QS-controlled biofilm maturation and LasA staphylolytic activity in Pseudomonas aeruginosa. Journal of Ethnopharmacology, 134(3), 865–71.

    Article  CAS  Google Scholar 

  20. Yarwood, J. M., Bartels, D. J., Volper, E. M., & Greenberg, E. P. (2004). Quorum Sensing in Staphylococcus aureus Biofilms. Journal of Bacteriology, 186(6), 1838–1850.

    Article  CAS  Google Scholar 

  21. Roopashree, T., Dang, R., Shobha Rani, R., & Narendra, C. (2008). Antibacterial activity of antipsoriatic herbs : Cassia tora, Momordica charantia and Calendula officinalis. International Journal od Applied Research in Natural Products, 1(May), 20–28.

    Google Scholar 

  22. Hagerman AE. Tannin Chemistry. 2011. Available at: www.users.muohio.edu/hagermae/tannin.pdf.

  23. Cortés, S., Pulgar, H., Sanhueza, V., et al. (2010). Identification of proanthocyanidins extracted from Pinus radiata D. Don bark. Ciencia e Investigacion Agreria., 37(2), 15–25.

    Google Scholar 

  24. Valgas C, de Souza S, Smânia E, Smânia A. (2007). Screening methods to determine antibacterial activity of natural products. Braz. J. Microbiol. vol.38 no.2; 38(2).

  25. Subbiahdoss, G., Pidhatika, B., Coullerez, G., Charnley, M., & Kuijer, R. (2010). Bacterial biofilm formation versus mamalian cell growth on titanium-based mono- and bi-functional coatings. European Cells and Materials., 19, 205–213.

    CAS  Google Scholar 

  26. Peng, Z., Tu, B., Shen, Y., et al. (2011). Quaternized chitosan inhibits icaA transcription and biofilm formation by Staphylococcus on a titanium surface. Antimicrobial Agents and Chemotherapy, 55(2), 860–866.

    Article  CAS  Google Scholar 

  27. Chandra, J., Mukherjee, P. K., & Ghannoum, M. A. (2008). In vitro growth and analysis of Candida biofilms. Nature Protocols, 3(12), 1909–24.

    Article  CAS  Google Scholar 

  28. Gollwitzer, H., Ibrahim, K., Meyer, H., Mittelmeier, W., Busch, R., & Stemberger, A. (2003). Antibacterial poly(D, L-lactic acid) coating of medical implants using a biodegradable drug delivery technology. Journal of Antimicrobial Chemotherapy, 51(3), 585–591.

    Article  CAS  Google Scholar 

  29. Jurcisek J a, Dickson AC, Bruggeman ME, Bakaletz, L. O. (2011). In vitro biofilm formation in an 8-well chamber slide. Journal of visualized experiments : JoVE (47):9–10.

  30. Sternberg C, Tolker-Nielsen T. (2006). Growing and analyzing biofilms in flow cells. Current protocols in microbiology; Unit 1B.2.

  31. Nikolic, L., Ristic, I., Adnadjevic, B., Nikolic, V., Jovanovic, J., & Stankovic, M. (2010). Novel microwave-assisted synthesis of poly(D,L-lactide): the influence of monomer/initiator molar ratio on the product properties. Sensors (Basel, Switzerland), 10(5), 5063–73.

    Article  CAS  Google Scholar 

  32. Quave, C. L., Plano, L. R. W., Pantuso, T., & Bennett, B. C. (2008). Effects of extracts from Italian medicinal plants on planktonic growth, biofilm formation and adherence of methicillin-resistant Staphylococcus aureus. Journal of Ethnopharmacology, 118(3), 418–28.

    Article  CAS  Google Scholar 

  33. Richards, J. J., & Melander, C. (2009). Controlling Bacterial Biofilms. ChemBioChem, 10, 2287–2294.

    Article  CAS  Google Scholar 

  34. Worthington, R. J., Richards, J. J., & Melander, C. (2012). Small molecule control of bacterial biofilms. Organic & Biomolecular Chemistry, 10(37), 7457–74.

    Article  CAS  Google Scholar 

  35. Huber, B., Eberl, L., Feucht, W., & Polster, J. (2003). Influence of polyphenols on bacterial biofilm formation and quorum-sensing. Zeitschrift für Naturforschung. C. Journal of Biosciences, 58(11–12), 879–84.

    CAS  Google Scholar 

  36. Quave, C. L., Estévez-Carmona, M., Compadre, C. M., et al. (2012). Ellagic acid derivatives from Rubus ulmifolius inhibit Staphylococcus aureus biofilm formation and improve response to antibiotics. PloS One, 7(1), e28737.

    Article  CAS  Google Scholar 

  37. Brackman, G., Cos, P., Maes, L., Nelis, H. J., & Coenye, T. (2011). Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrobial Agents and Chemotherapy, 55(6), 2655–61.

    Article  CAS  Google Scholar 

  38. Ding, X., Yin, B., Qian, L., et al. (2011). Screening for novel quorum-sensing inhibitors to interfere with the formation of Pseudomonas aeruginosa biofilm. Journal of Medical Microbiology, 60(Pt 12), 1827–34.

    Article  CAS  Google Scholar 

  39. Wu, J., & Yao, J. (2012). Fabrication and in vitro release behavior of a novel antibacterial coating containing halogenated furanone-loaded poly ( L-lactic acid ) nanoparticles on microarc-oxidized titanium. International Journal of Nanomedicine, 7, 5641–5652.

    Article  Google Scholar 

  40. Otto, M. (2009). Staphylococcal biofilms. Current Topics in Microbiology and Immunology, 322, 207–228.

    Google Scholar 

  41. Park, S.-C., Park, Y., & Hahm, K.-S. (2011). The role of antimicrobial peptides in preventing multidrug-resistant bacterial infections and biofilm formation. International Journal of Molecular Sciences, 12(9), 5971–92.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Part of this work was done under the contingency grant allotted to the first author under the Faculty development program of University Grants Commission, Govt. of India vide letter F. No. 30-23/08(WRO). The authors also wish to thank Dr. Priti Mehta, Head, Department of Microbiology, KEM hospital, for providing the cultures, Mr. Ajay Pitre of Sushrut Surgicals for providing the titanium alloy pieces, and Dr. Arne Heydron, Denmark, for sending the COMSTAT 1 program.

Conflict of interest

None declared.

Ethical approval

Not required

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Varsha Shukla.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shukla, V., Bhathena, Z. Sustained Release of a Purified Tannin Component of Terminalia chebula from a Titanium Implant Surface Prevents Biofilm Formation by Staphylococcus aureus . Appl Biochem Biotechnol 175, 3542–3556 (2015). https://doi.org/10.1007/s12010-015-1525-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-015-1525-2

Keywords

Navigation