Skip to main content

Advertisement

SpringerLink
Log in

Thermal annealed silk fibroin membranes for periodontal guided tissue regeneration

  • Tissue Engineering Constructs and Cell Substrates
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Guided tissue regeneration (GTR) is a surgical procedure applied in the reconstruction of periodontal defects, where an occlusive membrane is used to prevent the fast-growing connective tissue from migrating into the defect. In this work, silk fibroin (SF) membranes were developed for periodontal guided tissue regeneration. Solutions of SF with glycerol (GLY) or polyvinyl alcohol (PVA) where prepared at several weight ratios up to 30%, followed by solvent casting and thermal annealing at 85 °C for periods of 6 and 12 h to produce high flexible and stable membranes. These were characterized in terms of their morphology, physical integrity, chemical structure, mechanical and thermal properties, swelling capability and in vitro degradation behavior. The developed blended membranes exhibited high ductility, which is particular relevant considering the need for physical handling and adaptability to the defect. Moreover, the membranes were cultured with human periodontal ligament fibroblast cells (hPDLs) up to 7 days. Also, the higher hydrophilicity and consequent in vitro proteolytic degradability of these blends was superior to pure silk fibroin membranes. In particular SF/GLY blends demonstrated to support high cell adhesion and viability with an adequate hPDLs’ morphology, make them excellent candidates for applications in periodontal regeneration.

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

Access this article

Log in via an institution

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
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Polimeni G, Xiropaidis AV, Wikesjö UME. Biology and principles of periodontal wound healing/regeneration. Periodontol 2000. 2006;41:30–47.

    Article  Google Scholar 

  2. Nanci A, Bosshardt DD. Periodontal tissues in health and disease. Periodontol 2000. 2006;40:11–28.

    Article  Google Scholar 

  3. Nanci A, Bosshardt DD. Structure of periodontal tissues in health and disease. Periodontol 2000. Periodontol 2000. 2006;40:11–28.

    Article  Google Scholar 

  4. Tariq M, Iqbal Z, Ali J, Baboota S, Talegaonkar S, Ahmad Z, et al. Treatment modalities and evaluation models for periodontitis. Int J Pharm Investig. 2012;2:106–22.

    Article  Google Scholar 

  5. Eke PI, Dye BA, Wei L, Slade GD, Thornton-Evans GO, Borgnakke WS, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol. 2015;86:611–22.

    Article  Google Scholar 

  6. Deas DE, Moritz AJ, Sagun RS, Gruwell SF, Powell CA. Scaling and root planing vs. conservative surgery in the treatment of chronic periodontitis. Periodontol 2000. 2016;71:128–39.

    Article  Google Scholar 

  7. Sbordone L, Ramaglia L, Gulletta E, Iacono V. Recolonization of the subgingival microflora after scaling and root planing in human periodontitis. J Periodontol. 1990;61:579–84.

    Article  CAS  Google Scholar 

  8. Crea A, Deli G, Littarru C, Lajolo C, Orgeas GV, Tatakis DN. Intrabony defects, open-flap debridement, and decortication: a randomized clinical trial. J Periodontol. 2014;85:34–42.

    Article  Google Scholar 

  9. Mitani A, Takasu H, Horibe T, Furuta H, Nagasaka T, Aino M, et al. Five‐year clinical results for treatment of intrabony defects with EMD, guided tissue regeneration and open‐flap debridement: a case series. J Periodontal Res. 2015;50:123–30.

    Article  CAS  Google Scholar 

  10. Hanes PJ. Bone replacement grafts for the treatment of periodontal intrabony defects. Oral Maxillofac Surg Clin North Am Elsevier. 2007;19:499–512.

    Article  Google Scholar 

  11. Mathur A, Bains VK, Gupta V, Jhingran R, Singh GP. Evaluation of intrabony defects treated with platelet-rich fibrin or autogenous bone graft: a comparative analysis. Eur J Dent. 2015;9:100.

    Article  Google Scholar 

  12. Campana V, Milano G, Pagano E, Barba M, Cicione C, Salonna G, et al. Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J Mater Sci Mater Med. 2014;25:2445–61.

    Article  CAS  Google Scholar 

  13. Hämmerle CHF, Jung RE. Bone augmentation by means of barrier membranes. Periodontol 2000. 2003;33:36–53.

    Article  Google Scholar 

  14. Gamal AY, Iacono VJ. Enhancing guided tissue regeneration of periodontal defects by using a novel perforated barrier membrane. J Periodontol. 2013;84:905–13.

    Article  Google Scholar 

  15. Al Machot E, Hoffmann T, Lorenz K, Khalili I, Noack B. Clinical outcomes after treatment of periodontal intrabony defects with nanocrystalline hydroxyapatite (Ostim) or enamel matrix derivatives (Emdogain): a randomized controlled clinical trial. Biomed Res Int. 2014;786353:1–9.

  16. Hoffmann T, Al-Machot E, Meyle J, Jervøe-Storm P-M, Jepsen S. Three-year results following regenerative periodontal surgery of advanced intrabony defects with enamel matrix derivative alone or combined with a synthetic bone graft. Clin Oral Investig. 2016;20:357–64.

    Article  Google Scholar 

  17. Anitha CM, Senthilkumar S, Rajasekar S, Arun RT, Srinivasan S. Platelet rich fibrin and nanocrystalline hydroxyapatite: hope for regeneration in aggressive periodontitis: a novel clinical approach. Int J Appl Dent Sci. 2017;3:209–14.

  18. Ajwani H, Shetty S, Gopalakrishnan D, Kathariya R, Kulloli A, Dolas RS, et al. Comparative evaluation of platelet-rich fibrin biomaterial and open flap debridement in the treatment of two and three wall intrabony defects. J Int Oral Health. 2015;7:32.

    Google Scholar 

  19. Sam G, Madhavan Pillai BR. Evolution of barrier membranes in periodontal regeneration—“are the third generation membranes really here?”. J Clin Diagn Res. 2014;8:ZE14–7.

    Google Scholar 

  20. Bottino MC, Thomas V, Schmidt G, Vohra YK, Chu TMG, Kowolik MJ, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration—a materials perspective. Dent Mater. 2012;28:703–21.

    Article  CAS  Google Scholar 

  21. Karring T, Nyman S, Gottlow J, Laurel L. Development of the biological concept of guided tissue regeneration-animal and human studies. Periodontol 2000. 1993;1:26–35.

    Article  Google Scholar 

  22. Llambés F, Silvestre F-J, Caffesse R. Vertical guided bone regeneration with bioabsorbable barriers. J Periodontol. 2007;78:2036–42.

    Article  Google Scholar 

  23. Scantlebury TV. 1982–1992: a decade of technology development for guided tissue regeneration. J Periodontol. 1993;64:1129–37.

    Article  CAS  Google Scholar 

  24. Simian M, Dahlin C, Blair K, Schenk RK. Effect of different microstructures of e‐PTFE membranes on bone regeneration and soft tissue response: a histologic study in canine mandible. Clin Oral Implants Res. 1999;10:73–84.

    Article  Google Scholar 

  25. Donos N, Kostopoulos L, Karring T. Alveolar ridge augmentation using a resorbable copolymer membrane and autogenous bone grafts. Clin Oral Implants Res. 2002;13:203–13.

    Article  Google Scholar 

  26. Rothamel D, Schwarz F, Sager M, Herten M, Sculean A, Becker J. Biodegradation of differently cross‐linked collagen membranes: an experimental study in the rat. Clin Oral Implants Res. 2005;16:369–78.

    Article  Google Scholar 

  27. Bunyaratavej P, Wang H-L. Collagen membranes: a review. J Periodontol. 2001;72:215–29.

    Article  CAS  Google Scholar 

  28. Zhang JG, Mo XM. Current research on electrospinning of silk fibroin and its blends with natural and synthetic biodegradable polymers. Front Mater Sci. 2013;7:129–42.

    Article  CAS  Google Scholar 

  29. Sheikh Z, Qureshi J, Alshahrani AM, Nassar H, Ikeda Y, Glogauer M, et al. Collagen based barrier membranes for periodontal guided bone regeneration applications. Odontology. 2017;105:1–12.

    Article  CAS  Google Scholar 

  30. Ueyama Y, Ishikawa K, Mano T, Koyama T, Nagatsuka H, Suzuki K, et al. Usefulness as guided bone regeneration membrane of the alginate membrane. Biomaterials. 2002;23:2027–33.

    Article  CAS  Google Scholar 

  31. Ishikawa K, Ueyama Y, Mano T, Koyama T, Suzuki K, Matsumura T. Self‐setting barrier membrane for guided tissue regeneration method: initial evaluation of alginate membrane made with sodium alginate and calcium chloride aqueous solutions. J Biomed Mater Res. 1999;47:111–5.

    Article  CAS  Google Scholar 

  32. Xu C, Lei C, Meng L, Wang C, Song Y. Chitosan as a barrier membrane material in periodontal tissue regeneration. J Biomed Mater Res B Appl Biomater. 2012.1435–43.

  33. Zhang S, Huang Y, Yang X, Mei F, Ma Q, Chen G, et al. Gelatin nanofibrous membrane fabricated by electrospinning of aqueous gelatin solution for guided tissue regeneration. J Biomed Mater Res A. 2009;90:671–9.

    Article  Google Scholar 

  34. Wang J, Wang L, Zhou Z, Lai H, Xu P, Liao L, et al. Biodegradable polymer membranes applied in guided bone/tissue regeneration: a review. Polym (Basel). 2016;8:115.

    Article  Google Scholar 

  35. Vepari C, Kaplan DL. Silk as a biomaterial. Prog Polym Sci. 2007;32:991–1007.

  36. Kim J-Y, Yang B-E, Ahn J-H, Park SO, Shim H-W. Comparable efficacy of silk fibroin with the collagen membranes for guided bone regeneration in rat calvarial defects. J Adv Prosthodont. 2014;6:539–46.

    Article  Google Scholar 

  37. Zhang C, Song D, Lu Q, Hu X, Kaplan DL, Zhu H. Flexibility regeneration of silk fibroin in vitro. Biomacromolecules. 2012;13:2148–53.

    Article  CAS  Google Scholar 

  38. Silva MF, De Moraes MA, Nogueira GM, Rodas ACD, Higa OZ, Beppu MM. Glycerin and ethanol as additives on silk fibroin films: Insoluble and malleable films. J Appl Polym Sci. 2013;128:115–22.

    Article  CAS  Google Scholar 

  39. Lu Q, Hu X, Wang X, Kluge JA, Lu S, Cebe P, et al. Water-insoluble silk films with silk I structure. Acta Biomater. 2010;6:1380–7.

    Article  CAS  Google Scholar 

  40. Motta A, Fambri L, Migliaresi C. Regenerated silk fibroin films: thermal and dynamic mechanical analysis. Macromol Chem Phys. 2002;203:1658–65.

    Article  CAS  Google Scholar 

  41. Correia C, Bhumiratana S, Yan L-P, Oliveira AL, Gimble JM, Rockwood D, et al. Development of silk-based scaffolds for tissue engineering of bone from human adipose-derived stem cells. Acta Biomater. 2012;8:2483–92.

    Article  CAS  Google Scholar 

  42. Owens DK, Wendt RC. Estimation of the surface free energy of polymers. J Appl Polym Sci. 1969;13:1741–7.

    Article  CAS  Google Scholar 

  43. Kaelble DH. Dispersion-polar surface tension properties of organic solids. J Adhes. 1970;2:66–81.

    Article  CAS  Google Scholar 

  44. Horan RL, Antle K, Collette AL, Wang Y, Huang J, Moreau JE, et al. In vitro degradation of silk fibroin. Biomaterials. 2005;26:3385–93.

    Article  CAS  Google Scholar 

  45. Almeida LR, Martins AR, Fernandes EM, Oliveira MB, Correlo VM, Pashkuleva I, et al. New biotextiles for tissue engineering: development, characterization and in vitro cellular viability. Acta Biomater. 2013;9:8167–81.

    Article  CAS  Google Scholar 

  46. Lu S, Wang X, Lu Q, Zhang X, Kluge JA, Uppal N, et al. Insoluble and flexible silk films containing glycerol. Biomacromolecules ACS Publ. 2009;11:143–50.

    Article  Google Scholar 

  47. Tsukada M, Freddi G, Crighton JS. Structure and compatibility of poly (vinyl alcohol)‐silk fibroin (PVA/SA) blend films. J Polym Sci B Polym Phys. 1994;32:243–8.

    Article  Google Scholar 

  48. Tanaka T, Tanigami T, Yamaura K. Phase separation structure in poly (vinyl alcohol)/silk fibroin blend films. Polym Int. 1998;45:175–84.

    Article  CAS  Google Scholar 

  49. Hofmann S, CTWP Foo, Rossetti, Textor F, Vunjak-Novakovic M, Kaplan G. DL, et al. Silk fibroin as an organic polymer for controlled drug delivery. J Control Release. 2006;111:219–27.

    Article  CAS  Google Scholar 

  50. Ayub ZH, Arai M, Hirabayashi K. Quantitative structural analysis and physical properties of silk fibroin hydrogels. Polym. 1994;35:2197–200.

    Article  CAS  Google Scholar 

  51. Chen X, Shao Z, Marinkovic NS, Miller LM, Zhou P, Chance MR. Conformation transition kinetics of regenerated Bombyx mori silk fibroin membrane monitored by time-resolved FTIR spectroscopy. Biophys Chem. 2001;89:25–34.

    Article  CAS  Google Scholar 

  52. Indran VP, Zuhaimi NAS, Deraman MA, Maniam GP, Yusoff MM, Hin T-YY, et al. An accelerated route of glycerol carbonate formation from glycerol using waste boiler ash as catalyst. RSC Adv. 2014;4:25257–67.

    Article  CAS  Google Scholar 

  53. Sudhamani SR, Prasad MS, Sankar KU.DSC and FTIR studies on gellan and polyvinyl alcohol (PVA) blend films. Food Hydrocoll. 2003;17:245–50.

    Article  CAS  Google Scholar 

  54. Dai L, Li J, Yamada E. Effect of glycerin on structure transition of PVA/SF blends. J Appl Polym Sci. 2002;86:2342–7.

    Article  CAS  Google Scholar 

  55. Magoshi J, Nakamura S. Studies on physical properties and structure of silk. Glass transition and crystallization of silk fibroin. J Appl Polym Sci. 1975;19:1013–5.

    Article  CAS  Google Scholar 

  56. Koosha M, Mirzadeh H, Shokrgozar MA, Farokhi M. Nanoclay-reinforced electrospun chitosan/PVA nanocomposite nanofibers for biomedical applications. RSC Adv. 2015;5:10479–87.

    Article  CAS  Google Scholar 

  57. Freddi G, Tsukada M, Beretta S. Structure and physical properties of silk fibroin/polyacrylamide blend films. J Appl Polym Sci. 1999;71:1563–71.

    Article  CAS  Google Scholar 

  58. Wang X, Zhang X, Castellot J, Herman I, Iafrati M, Kaplan DL. Controlled release from multilayer silk biomaterial coatings to modulate vascular cell responses. Biomater. 2008;29:894–903.

    Article  CAS  Google Scholar 

  59. Sofia S, McCarthy MB, Gronowicz G, Kaplan DL. Functionalized silk‐based biomaterials for bone formation. J Biomed Mater Res. 2001;54:139–48.

    Article  CAS  Google Scholar 

  60. Asakura T, Kuzuhara A, Tabeta R, Saito H. Conformational characterization of Bombyx mori silk fibroin in the solid state by high-frequency carbon-13 cross polarization-magic angle spinning NMR, X-ray diffraction, and infrared spectroscopy. Macromoles. 1985;18:1841–5.

    Article  CAS  Google Scholar 

  61. Chen X, Li W, Yu T. Conformation transition of silk fibroin induced by blending chitosan. J Polym Sci Phys. 1997;35:2293–6.

    Article  CAS  Google Scholar 

  62. Kweon H, Woo SO, Park YH. Effect of heat treatment on the structural and conformational changes of regenerated Antheraea pernyi silk fibroin films. J Appl Polym Sci. 2001;81:2271–6.

    Article  CAS  Google Scholar 

  63. Vieira MGA, Da Silva MA, Dos Santos LO, Beppu MM. Natural-based plasticizers and biopolymer films: a review. Eur Polym J. 2011;47:254–63.

  64. Fill TS, Carey JP, Toogood RW, Major PW, Experimentally determined mechanical properties of, and models for, the periodontal ligament: critical review of current literature. J Dent Biomech. 2011;312980:1–10.

  65. Coïc M, Placet V, Jacquet E, Meyer C. [Mechanical properties of collagen membranes used in guided bone regeneration: a comparative study of three models]. Rev Stomatol Chir Maxillofac. 2009;111:286–90.

    Article  Google Scholar 

  66. Milella E, Barra G, Ramires PA, Leo G, Aversa P, Romito A. Poly (L‐lactide) acid/alginate composite membranes for guided tissue regeneration. J Biomed Mater Res 2001;57:248–57.

    Article  CAS  Google Scholar 

  67. Holland C, Numata K, Rnjak-Kovacina J, Seib FP. The biomedical use of silk: past, present, future. Adv Health Care Mater. 2019;8:1–26.

  68. Villar CC, Cochran DL. Regeneration of periodontal tissues: guided tissue regeneration. Dent Clin North Am. 2010;54:73–92.

  69. Brown J, Lu CL, Coburn J, Kaplan DL. Impact of silk biomaterial structure on proteolysis. Acta Biomater 2015;11:212–21.

  70. Yang Y, Zhao Y, Gu Y, Yan X, Liu J, Ding F, et al. Degradation behaviors of nerve guidance conduits made up of silk fibroin in vitro and in vivo. Polym Degrad Stab. 2009;94:2213–20.

  71. Zhou J, Cao C, Ma X, Hu L, Chen L, Wang C. In vitro and in vivo degradation behavior of aqueous-derived electrospun silk fibroin scaffolds. Polym Degrad Stab. 2010;95:1679–85.

  72. Cai Y, Guo J, Chen C, Yao C, Chung SM, Yao J, et al. Silk fibroin membrane used for guided bone tissue regeneration. Mater Sci Eng C Mater Biol Appl. 2017;70:148–54.

  73. Lee JM, Sultan MT, Kim SH, Kumar V, Yeon YK, Lee OJ, et al. Artificial auricular cartilage using silk fibroin and polyvinyl alcohol hydrogel. Int J Mol Sci. 2017;18:1707.

Download references

Acknowledgements

The authors acknowledge Portuguese National Funds from FCT - Fundação para a Ciência e a Tecnologia through project UID/Multi/50016/2013; Program FCT Investigators to A.L.Oliveira (IF/00411/2013) and J.M.Oliveira (IF/00423/2012 and IF/01285/2015); PhD scholarship under the financial support from FCT/MCTES and FSE/POCH, PD/59/2013 attributed to V.P.Ribeiro (PD/BD/113806/2015); Project SERICAMED (IF/00411/2013/CP1167); Project “IBEROS” (0245_IBEROS_1_E), funded by Fundo Europeu de Desenvolvimento Regional in the frame of Programa Interreg V A Espanha - Portugal (POCTEP) 2014–2020. This article is a result of the project “Biotherapies” (NORTE-01-0145-FEDER-000012) supported by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF).

Author information

Authors and Affiliations

  1. CBQF–Centro de Biotecnologia e Química Fina, Laboratório Associado, Escola Superior de Biotecnologia, Universidade Católica Portuguesa, Rua Arquiteto Lobão Vital, 4200-072, Porto, Portugal

    Catarina Geão, Ana R. Costa-Pinto, Cassilda Cunha-Reis & Ana L. Oliveira

  2. 3B’s Research Group, I3Bs–Research Institute on Biomaterials, Biodegradable and Biomimetics, Headquarters of the European Institute of Excellence on tissue Engineering and Regenerative Medicine, AvePark, 4805-17, Barco, Guimarães, Portugal

    Catarina Geão, Viviana P. Ribeiro, Sílvia Vieira, Joaquim M. Oliveira & Rui L. Reis

  3. ICVS/3B’s–PT Government Associated Laboratory, Braga/Guimarães, Portugal

    Viviana P. Ribeiro, Sílvia Vieira, Joaquim M. Oliveira & Rui L. Reis

  4. The Discoveries Centre for Regenerative and Precision Medicine, Headquarters at University of Minho, AvePark, 4805-017, Barco, Guimarães, Portugal

    Joaquim M. Oliveira & Rui L. Reis

Authors
  1. Catarina Geão
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana R. Costa-Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cassilda Cunha-Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Viviana P. Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sílvia Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joaquim M. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rui L. Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ana L. Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ana L. Oliveira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Geão, C., Costa-Pinto, A.R., Cunha-Reis, C. et al. Thermal annealed silk fibroin membranes for periodontal guided tissue regeneration. J Mater Sci: Mater Med 30, 27 (2019). https://doi.org/10.1007/s10856-019-6225-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-019-6225-y

Search

Navigation