Skip to main content

Advertisement

Log in

Antibacterial properties of poly (octanediol citrate)/gallium-containing bioglass composite scaffolds

  • Delivery Systems
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Bioactive glasses may function as antimicrobial delivery systems through the incorporation and subsequent release of therapeutic ions. The aim of this study was to evaluate the antimicrobial properties of a series of composite scaffolds composed of poly(octanediol citrate) with increased loads of a bioactive glass that releases zinc (Zn2+) and gallium (Ga3+) ions in a controlled manner. The antibacterial activity of these scaffolds was investigated against both Gram-positive (Staphylococcus aureus) and Gram-negative (Escherichia coli) bacteria. The ability of the scaffolds to release ions and the subsequent ingress of these ions into hard tissue was evaluated using a bovine bone model. Scaffolds containing bioactive glass exhibited antibacterial activity and this increased in vitro with higher bioactive glass loads; viable cells decreased to about 20 % for the composite scaffold containing 30 % bioactive glass. The Ga3+ release rate increased as a function of time and Zn2+ was shown to incorporate into the surrounding bone.

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.

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

Similar content being viewed by others

References

  1. Alvarez K, Nakajima H. Metallic scaffolds for bone regeneration. Materials. 2009;2(3):790–832. doi:10.3390/ma2030790.

    Article  Google Scholar 

  2. Puppi D, Chiellini F, Piras AM, Chiellini E. Polymeric materials for bone and cartilage repair. Prog Polym Sci. 2010;35(4):403–40. doi:10.1016/j.progpolymsci.2010.01.006.

    Article  Google Scholar 

  3. Belt HVd, Neut D, Schenk W, Horn JRV, Mei HCVD, Busscher HJ. Infection of orthopedic implants and the use of antibiotic-loaded bone cements: a review. Acta Orthop. 2001;72(6):557–71. doi:10.1080/000164701317268978.

    Article  Google Scholar 

  4. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15(2):167–93. doi:10.1128/CMR.15.2.167-193.2002.

    Article  Google Scholar 

  5. Malchau H, Meeting AAOOS. Prognosis of total hip replacement: update of results and risk-ratio. Analysis for Revision and Re-revision from the Swedish National Hip Arthroplasty Register 1979–2000. 2002.

  6. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–8. doi:10.1016/S0140-6736(01)05321-1.

    Article  Google Scholar 

  7. Campoccia D, Montanaro L, Arciola CR. A review of the clinical implications of anti-infective biomaterials and infection-resistant surfaces. Biomaterials. 2013;34(33):8018–29. doi:10.1016/j.biomaterials.2013.07.048.

    Article  Google Scholar 

  8. Chaieb K, Mahdouani K, Bakhrouf A. Detection of icaA and icaD loci by polymerase chain reaction and biofilm formation by Staphylococcus epidermidis isolated from dialysate and needles in a dialysis unit. J Hosp Infect. 2005;61(3):225–30. doi:10.1016/j.jhin.2005.05.014.

    Article  Google Scholar 

  9. Brown M, Gilbert P. Sensitivity of biofilms to antimicrobial agents. J Appl Bacteriol. 1993;74(S22):87S–97S. doi:10.1111/j.1365-2672.1993.tb04345.x.

    Article  Google Scholar 

  10. Stewart PS. Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol. 2002;292(2):107–13. doi:10.1078/1438-4221-00196.

    Article  Google Scholar 

  11. Meyer B. Approaches to prevention, removal and killing of biofilms. Int Biodeter Biodegr. 2003;51(4):249–53. doi:10.1016/S0964-8305(03)00047-7.

    Article  Google Scholar 

  12. Logghe C, Van Ossel C, D’Hoore W, Ezzedine H, Wauters G, Haxhe J-J. Evaluation of chlorhexidine and silver-sulfadiazine impregnated central venous catheters for the prevention of bloodstream infection in leukaemic patients: a randomized controlled trial. J Hosp Infect. 1997;37(2):145–56. doi:10.1016/S0195-6701(97)90184-5.

    Article  Google Scholar 

  13. Gottenbos B, van der Mei HC, Klatter F, Nieuwenhuis P, Busscher HJ. In vitro and in vivo antimicrobial activity of covalently coupled quaternary ammonium silane coatings on silicone rubber. Biomaterials. 2002;23(6):1417–23. doi:10.1016/S0142-9612(01)00263-0.

    Article  Google Scholar 

  14. Cerca N, Martins S, Cerca F, Jefferson KK, Pier GB, Oliveira R, et al. Comparative assessment of antibiotic susceptibility of coagulase-negative staphylococci in biofilm versus planktonic culture as assessed by bacterial enumeration or rapid XTT colorimetry. J Antimicrob Chemother. 2005;56(2):331–6. doi:10.1093/jac/dki217.

    Article  Google Scholar 

  15. Langsrud S, Sidhu MS, Heir E, Holck AL. Bacterial disinfectant resistance—a challenge for the food industry. Int Biodeter Biodegr. 2003;51(4):283–90. doi:10.1016/S0964-8305(03)00039-8.

    Article  Google Scholar 

  16. Hench LL, Splinter RJ, Allen W, Greenlee T. Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res. 1971;5(6):117–41. doi:10.1002/jbm.820050611.

    Article  Google Scholar 

  17. Kaur G, Pandey OP, Singh K, Homa D, Scott B, Pickrell G. A review of bioactive glasses: their structure, properties, fabrication and apatite formation. J Biomed Mater Res A. 2014;102(1):254–74. doi:10.1002/jbm.a.34690.

    Article  Google Scholar 

  18. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest. 2007;117(4):877. doi:10.1172/JCI30783.

    Article  Google Scholar 

  19. Stoor P, Söderling E, Salonen JI. Antibacterial effects of a bioactive glass paste on oral microorganisms. Acta Odontol Scand. 1998;56(3):161–5. doi:10.1080/000163598422901.

    Article  Google Scholar 

  20. Valappil SP, Ready D, Neel EAA, Pickup DM, Chrzanowski W, O’Dell LA, et al. Antimicrobial gallium-doped phosphate-based glasses. Adv Funct Mater. 2008;18(5):732–41. doi:10.1002/adfm.200700931.

    Article  Google Scholar 

  21. Yang J, Webb AR, Ameer GA. Novel citric acid-based biodegradable elastomers for tissue engineering. Adv Mater. 2004;16(6):511–6. doi:10.1002/adma.200306264.

    Article  Google Scholar 

  22. Yang J, Webb AR, Pickerill SJ, Hageman G, Ameer GA. Synthesis and evaluation of poly (diol citrate) biodegradable elastomers. Biomaterials. 2006;27(9):1889–98. doi:10.1016/j.biomaterials.2005.05.106.

    Article  Google Scholar 

  23. Zeimaran E, Pourshahrestani S, Pingguan-Murphy B, Kadri NA, Rothan HA, Yusof R, et al. Fabrication and characterization of poly (octanediol citrate)/gallium-containing bioglass microcomposite scaffolds. J Mater Sci. 2015;50:1–13. doi:10.1007/s10853-014-8782-2.

    Article  Google Scholar 

  24. Qiu H, Yang J, Kodali P, Koh J, Ameer GA. A citric acid-based hydroxyapatite composite for orthopedic implants. Biomaterials. 2006;27(34):5845–54. doi:10.1016/j.biomaterials.2006.07.042.

    Article  Google Scholar 

  25. Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials. 2006;27(15):2907–15. doi:10.1016/j.biomaterials.2006.01.017.

    Article  Google Scholar 

  26. Lansdown A. Zinc in the healing wound. Lancet. 1996;347(9003):706–7. doi:10.1016/S0140-6736(96)90072-0.

    Article  Google Scholar 

  27. Yamamoto A, Honma R, Sumita M. Cytotoxicity evaluation of 43 metal salts using murine fibroblasts and osteoblastic cells. J Biomed Mater Res. 1998;39(2):331–40. doi:10.1002/(SICI)1097-4636(199802)39:2<331:AID-JBM22>3.0.CO;2-E.

    Article  Google Scholar 

  28. Ito A, Kawamura H, Otsuka M, Ikeuchi M, Ohgushi H, Ishikawa K, et al. Zinc-releasing calcium phosphate for stimulating bone formation. Mater Sci Eng, C. 2002;22(1):21–5.

    Article  Google Scholar 

  29. Fuierer TA, LoRe M, Puckett SA, Nancollas GH. A mineralization adsorption and mobility study of hydroxyapatite surfaces in the presence of zinc and magnesium ions. Langmuir. 1994;10(12):4721–5. doi:10.1021/la00024a054.

    Article  Google Scholar 

  30. Du RL, Chang J, Ni SY, Zhai WY, Wang JY. Characterization and in vitro bioactivity of zinc-containing bioactive glass and glass-ceramics. J Biomater Appl. 2006;20(4):341–60. doi:10.1177/0885328206054535.

    Article  Google Scholar 

  31. Boyd D, Towler M, Wren A, Clarkin O, Tanner D. TEM analysis of apatite surface layers observed on zinc based glass polyalkenoate cements. J Mater Sci. 2008;43(3):1170–3. doi:10.1007/s10853-007-2362-7.

    Article  Google Scholar 

  32. Blumenthal NC, Cosma V, Levine S. Effect of gallium on thein vitro formation, growth, and solubility of hydroxyapatite. Calcif Tissue Int. 1989;45(2):81–7. doi:10.1007/BF02561406.

    Article  Google Scholar 

  33. Korbas M, Rokita E, Meyer-Klaucke W, Ryczek J. Bone tissue incorporates in vitro gallium with a local structure similar to gallium-doped brushite. J Biol Inorg Chem. 2004;9(1):67–76. doi:10.1007/s00775-003-0497-9.

    Article  Google Scholar 

  34. Franchini M, Lusvardi G, Malavasi G, Menabue L. Gallium-containing phospho-silicate glasses: synthesis and in vitro bioactivity. Mater Sci Eng, C. 2012;32(6):1401–6. doi:10.1016/j.msec.2012.04.016.

    Article  Google Scholar 

  35. Aina V, Morterra C, Lusvardi G, Malavasi G, Menabue L, Shruti S, et al. Ga-modified (Si–Ca–P) sol-gel glasses: possible relationships between surface chemical properties and bioactivity. J Phys Chem C. 2011;115(45):22461–74. doi:10.1021/jp207217a.

    Article  Google Scholar 

  36. Wren A, Boyd D, Thornton R, Cooney J, Towler M. Antibacterial properties of a tri-sodium citrate modified glass polyalkenoate cement. J Biomed Mater Res B. 2009;90(2):700–9. doi:10.1002/jbm.b.31337.

    Article  Google Scholar 

  37. Kuhn LT, Grynpas MD, Rey CC, Wu Y, Ackerman JL, Glimcher MJ. A comparison of the physical and chemical differences between cancellous and cortical bovine bone mineral at two ages. Calcif Tissue Int. 2008;83(2):146–54. doi:10.1007/s00223-008-9164-z.

    Article  Google Scholar 

  38. Grynpas M, Pritzker K, Hancock R. Neutron activation analysis of bulk and selected trace elements in bones using a low flux SLOWPOKE reactor. Biol Trace Elem Res. 1987;13(1):333–44. doi:10.1007/BF02796644.

    Article  Google Scholar 

  39. Pasquet J, Chevalier Y, Pelletier J, Couval E, Bouvier D, Bolzinger M-A. The contribution of zinc ions to the antimicrobial activity of zinc oxide. Colloid Surface A. 2014;457:263–74. doi:10.1016/j.colsurfa.2014.05.057.

    Article  Google Scholar 

  40. Foley J, Blackwell A. In vivo cariostatic effect of black copper cement on carious dentine. Caries Res. 2002;37(4):254–60. doi:10.1159/000070867.

    Article  Google Scholar 

  41. Osinaga PW, Grande RHM, Ballester RY, Simionato MRL, Rodrigues CRMD, Muench A. Zinc sulfate addition to glass-ionomer-based cements: influence on physical and antibacterial properties, zinc and fluoride release. Dental Mater. 2003;19(3):212–7. doi:10.1016/S0109-5641(02)00032-5.

    Article  Google Scholar 

  42. Yamaguchi M. Role of zinc in bone formation and bone resorption. J Trace Elem Exp Med. 1998;11(2–3):119–35. doi:10.1002/(SICI)1520-670X(1998)11:2/3<119:AID-JTRA5>3.0.CO;2-3.

    Article  Google Scholar 

  43. Calhoun NR, Smith JC Jr, Becker KL. The role of zinc in bone metabolism. Clin Orthop Relat R. 1974;103:212–34. doi:10.1097/00003086-197409000-00084.

    Article  Google Scholar 

  44. Ripa S, Ripa R. Zinc and immune function. Minerva Med. 1994;86(7–8):315–8.

    Google Scholar 

  45. Reginster J-Y, Strause L, Saltman P, Franchimont P. Trace elements and postmenopausal osteoporosis: a preliminary report of decreased serum manganese. Med Sci Res. 1988;16:337–338.

    Google Scholar 

  46. Zhang L, Jiang Y, Ding Y, Povey M, York D. Investigation into the antibacterial behaviour of suspensions of ZnO nanoparticles (ZnO nanofluids). J Nanopart Res. 2007;9(3):479–89. doi:10.1007/s11051-006-9150-1.

    Article  Google Scholar 

  47. Don T-M, Chen C-C, Lee C-K, Cheng W-Y, Cheng L-P. Preparation and antibacterial test of chitosan/PAA/PEGDA bi-layer composite membranes. J Biomat Sci-Polym E. 2005;16(12):1503–19. doi:10.1163/156856205774576718.

    Article  Google Scholar 

  48. Gubler M, Brunner T, Zehnder M, Waltimo T, Sener B, Stark W. Do bioactive glasses convey a disinfecting mechanism beyond a mere increase in pH? Int Endod J. 2008;41(8):670–8. doi:10.1111/j.1365-2591.2008.01413.x.

    Article  Google Scholar 

  49. Pickup D, Moss R, Qiu D, Newport R, Valappil S, Knowles J, et al. Structural characterization by x-ray methods of novel antimicrobial gallium-doped phosphate-based glasses. J Chem Phys. 2009;130:064708. doi:10.1063/1.3076057.

    Article  Google Scholar 

  50. Bernstein LR. Mechanisms of therapeutic activity for gallium. Pharmacol Rev. 1998;50(4):665–82.

    Google Scholar 

  51. Chitambar CR. Medical applications and toxicities of gallium compounds. Int J Environ Res Public Health. 2010;7(5):2337–61. doi:10.3390/ijerph7052337.

    Article  Google Scholar 

  52. Murthy PS, Venugopalan V, Sahoo P, Dhara S, Das A, Tyagi A, et al. editors. Gallium oxide nanoparticle induced inhibition of bacterial adhesion and biofilm formation. IEEE International Conference on Nanoscience, Engineering and Technology (ICONSET); 2011.

  53. Wu C, Labrie J, Tremblay Y, Haine D, Mourez M, Jacques M. Zinc as an agent for the prevention of biofilm formation by pathogenic bacteria. J Appl Microbiol. 2013;115(1):30–40. doi:10.1111/jam.12197.

    Article  Google Scholar 

  54. Boyd D, Li H, Tanner D, Towler M, Wall J. The antibacterial effects of zinc ion migration from zinc-based glass polyalkenoate cements. J Mater Sci-Mater M. 2006;17(6):489–94. doi:10.1007/s10856-006-8930-6.

    Article  Google Scholar 

  55. Fang M, Chen J-H, Xu X-L, Yang P-H, Hildebrand HF. Antibacterial activities of inorganic agents on six bacteria associated with oral infections by two susceptibility tests. Int J Antimicrob Agent. 2006;27(6):513–7. doi:10.1016/j.ijantimicag.2006.01.008.

    Article  Google Scholar 

  56. Stanić V, Dimitrijević S, Antić-Stanković J, Mitrić M, Jokić B, Plećaš IB, et al. Synthesis, characterization and antimicrobial activity of copper and zinc-doped hydroxyapatite nanopowders. Appl Surf Sci. 2010;256(20):6083–9. doi:10.1016/j.apsusc.2010.03.124.

    Article  Google Scholar 

  57. Söderberg TA, Sunzel B, Holm S, Elmros T, Hallmans G, Sjöberg S. Antibacterial effect of zinc oxide in vitro. Scand J Plast Recons. 1990;24(3):193–7. doi:10.3109/02844319009041278.

    Article  Google Scholar 

  58. Alhalawani AM, Placek L, Wren AW, Curran DJ, Boyd D, Towler MR. Influence of gallium on the surface properties of zinc based glass polyalkenoate cements. Mater Chem Phys. 2014;147(3):360–4. doi:10.1016/j.matchemphys.2014.06.020.

    Article  Google Scholar 

  59. Verron E, Masson M, Khoshniat S, Duplomb L, Wittrant Y, Baud’huin M, et al. Gallium modulates osteoclastic bone resorption in vitro without affecting osteoblasts. Brit J Pharmacol. 2010;159(8):1681–92. doi:10.1111/j.1476-5381.2010.00665.x.

    Article  Google Scholar 

  60. Balamurugan A, Balossier G, Kannan S, Michel J, Rebelo AH, Ferreira JM. Development and in vitro characterization of sol–gel derived CaO–P 2 O 5–SiO 2–ZnO bioglass. Acta Biomater. 2007;3(2):255–62. doi:10.1016/j.actbio.2006.09.005.

    Article  Google Scholar 

Download references

Acknowledgments

This research is supported by a High Impact Research Grant (UM.C/625/1/HIR/MOHE/ENG/58) from the Ministry of Higher Education Malaysia and University of Malaya Research Grant (UMRG, RG156-12AET).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark R. Towler.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zeimaran, E., Pourshahrestani, S., Djordjevic, I. et al. Antibacterial properties of poly (octanediol citrate)/gallium-containing bioglass composite scaffolds. J Mater Sci: Mater Med 27, 18 (2016). https://doi.org/10.1007/s10856-015-5620-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-015-5620-2

Keywords

Navigation