Highly Segregated Biocomposite Membrane as a Functionally Graded Template for Periodontal Tissue Regeneration
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Fabrication of CH:HA Membranes
2.3. Scanning Electron Microscope (SEM) Analysis
2.4. Fourier Transform Infrared (FTIR) Spectroscopy
2.5. Mechanical Testing
2.6. Swelling Ratio and Degradation
2.7. Water Contact Angle Measurement
2.8. Cytotoxicity
2.9. Alamar Blue® Staining
2.10. Mineralised Matrix Deposition (Calcium/Collagen)
2.11. Statistical Analysis
3. Results
3.1. Optical Images and SEM Analysis
3.2. FTIR Spectroscopy
3.3. Mechanical Analysis
3.4. Swelling and Weight Loss Analysis
3.5. Wetting Contact Angle Analysis
3.6. Cytotoxicity Assay
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Foey, A.D.; Habil, N.; Al-Shaghdali, K.; Crean, S.J. Porphyromonas gingivalis-stimulated macrophage subsets exhibit differential induction and responsiveness to interleukin-10. Arch. Oral Biol. 2017, 73, 282–288. [Google Scholar] [CrossRef] [Green Version]
- Sculean, A.; Nikolidakis, D.; Nikou, G.; Ivanovic, A.; Chapple, I.L.C.; Stavropoulos, A. Biomaterials for promoting periodontal regeneration in human intrabony defects: A systematic review. Periodontol. 2000 2015, 68, 182–216. [Google Scholar] [CrossRef]
- Susin, C.; Wikesjö, U.M.E. Regenerative periodontal therapy: 30 years of lessons learned and unlearned. Periodontol. 2000 2013, 62, 232–242. [Google Scholar] [CrossRef]
- Chen, F.-M.M.; Jin, Y. Periodontal tissue engineering and regeneration: Current approaches and expanding opportunities. Tissue Eng. Part B-Rev. 2010, 16, 219–255. [Google Scholar] [CrossRef]
- Menicanin, D.; Hynes, K.; Han, J.; Gronthos, S.; Bartold, P.M. Cementum and periodontal ligament regeneration. Adv. Exp. Med. Biol. 2015, 881, 207–236. [Google Scholar] [CrossRef] [PubMed]
- Bottino, M.C.; Thomas, V.; Schmidt, G.; Vohra, Y.K.; Chu, T.-M.G.; Kowolik, M.J.; Janowski, G.M. Recent advances in the development of GTR/GBR membranes for periodontal regeneration—A materials perspective. Dent. Mater. 2012, 28, 703–721. [Google Scholar] [CrossRef] [PubMed]
- Bosshardt, D.D.; Sculean, A. Does periodontal tissue regeneration really work? Periodontol. 2000 2009, 51, 208–219. [Google Scholar] [CrossRef]
- Leal, A.I.; Caridade, S.G.; Ma, J.; Yu, N.; Gomes, M.E.; Reis, R.L.; Jansen, J.A.; Walboomers, X.F.; Mano, J.F. Asymmetric PDLLA membranes containing Bioglass® for guided tissue regeneration: Characterization and in vitro biological behavior. Dent. Mater. 2013, 29, 427–436. [Google Scholar] [CrossRef]
- Dentino, A.; Lee, S.; Mailhot, J.; Hefti, A.F. Principles of periodontology. Periodontol. 2000 2013, 61, 16–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bottino, M.C.; Thomas, V.; Janowski, G.M. A novel spatially designed and functionally graded electrospun membrane for periodontal regeneration. Acta Biomater. 2011, 7, 216–224. [Google Scholar] [CrossRef]
- Husain, S.; Al-Samadani, K.H.; Najeeb, S.; Zafar, M.S.; Khurshid, Z.; Zohaib, S.; Qasim, S.B. Chitosan biomaterials for current and potential dental applications. Materials 2017, 10, 602. [Google Scholar] [CrossRef] [Green Version]
- Qasim, S.B.; Zafar, M.S.; Najeeb, S.; Khurshid, Z.; Shah, A.H.; Husain, S.; Rehman, I.U. Electrospinning of chitosan-based solutions for tissue engineering and regenerative medicine. Int. J. Mol. Sci. 2018, 19, 407. [Google Scholar] [CrossRef] [Green Version]
- Rinaudo, M. Chitin and chitosan: Properties and applications. Prog. Polym. Sci. 2006, 31, 603–632. [Google Scholar] [CrossRef]
- Di Martino, A.; Sittinger, M.; Risbud, M.V. Chitosan: A versatile biopolymer for orthopaedic tissue-engineering. Biomaterials 2005, 26, 5983–5990. [Google Scholar] [CrossRef]
- Lord, M.S.; Cheng, B.; McCarthy, S.J.; Jung, M.S.; Whitelock, J.M. The modulation of platelet adhesion and activation by chitosan through plasma and extracellular matrix proteins. Biomaterials 2011, 32, 6655–6662. [Google Scholar] [CrossRef] [PubMed]
- Muzzarelli, R.A.A. Chitins and chitosans for the repair of wounded skin, nerve, cartilage and bone. Carbohydr. Polym. 2009, 76, 167–182. [Google Scholar] [CrossRef]
- Van Hong Thien, D.; Hsiao, S.W.; Ho, M.H.; Li, C.H.; Shih, J.L. Electrospun chitosan/hydroxyapatite nanofibers for bone tissue engineering. J. Mater. Sci. 2013, 48, 1640–1645. [Google Scholar] [CrossRef]
- Madhumathi, K.; Shalumon, K.T.; Rani, V.V.; Tamura, H.; Furuike, T.; Selvamurugan, N.; Nair, S.V.; Jayakumar, R. Wet chemical synthesis of chitosan hydrogel-hydroxyapatite composite membranes for tissue engineering applications. Int. J. Biol. Macromol. 2009, 45, 12–15. [Google Scholar] [CrossRef] [PubMed]
- Fraga, A.F.; de Filho, E.A.; da Rigo, E.C.S.; Boschi, A.O. Synthesis of chitosan/hydroxyapatite membranes coated with hydroxycarbonate apatite for guided tissue regeneration purposes. Appl. Surf. Sci. 2011, 257, 3888–3892. [Google Scholar] [CrossRef] [Green Version]
- Qasim, S.B.; Delaine-Smith, R.M.; Rawlinson, A.; Ur Rehman, I. Freeze gelated porous membranes for periodontal tissue regeneration. Acta Biomater. 2015, 23, 317–328. [Google Scholar] [CrossRef] [Green Version]
- Frohbergh, M.E.; Katsman, A.; Botta, G.P.; Lazarovici, P.; Schauer, C.L.; Wegst, U.G.K.; Lelkes, P.I. Electrospun hydroxyapatite-containing chitosan nanofibers crosslinked with genipin for bone tissue engineering. Biomaterials 2012, 33, 9167–9178. [Google Scholar] [CrossRef] [Green Version]
- Xianmiao, C.; Yubao, L.; Yi, Z.; Li, Z.; Jidong, L.; Huanan, W. Properties and in vitro biological evaluation of nano-hydroxyapatite/chitosan membranes for bone guided regeneration. Mater. Sci. Eng. C 2009, 29, 29–35. [Google Scholar] [CrossRef]
- Qasim, S.B.; Najeeb, S.; Delaine-Smith, R.M.; Rawlinson, A.; Ur Rehman, I. Potential of electrospun chitosan fibers as a surface layer in functionally graded GTR membrane for periodontal regeneration. Dent. Mater. 2017, 33, 71–83. [Google Scholar] [CrossRef] [Green Version]
- Qasim, S.B.; Husain, S.; Huang, Y.; Pogorielov, M.; Deineka, V.; Lyndin, M.; Rawlinson, A.; Rehman, I.U. In-vitro and in-vivo degradation studies of freeze gelated porous chitosan composite scaffolds for tissue engineering applications. Polym. Degrad. Stab. 2017, 136, 31–38. [Google Scholar] [CrossRef]
- Qasim, S.B.; Delaine-Smith, R.; Rawlinson, A.; Rehman, I.U. Development of a Novel Bioactive Functionally Guided Tissue Graded Membrane for Periodontal Lesions. In Proceedings of the USES Conference Proceedings, Sheffield, UK, 13–16 July 2015; Volume 1, pp. 25–26. [Google Scholar]
- Shahzadi, L.; Zeeshan, R.; Yar, M.; Bin Qasim, S.; Chaudhry, A.A.; Khan, A.F.; Muhammad, N. Biocompatibility Through Cell Attachment and Cell Proliferation Studies of Nylon 6/Chitosan/Ha Electrospun Mats. J. Polym. Environ. 2018, 26, 2030–2038. [Google Scholar] [CrossRef]
- Li, X.Y.; Nan, K.H.; Shi, S.; Chen, H. Preparation and characterization of nano-hydroxyapatite/chitosan cross-linking composite membrane intended for tissue engineering. Int. J. Biol. Macromol. 2012, 50, 43–49. [Google Scholar] [CrossRef]
- Thein-Han, W.W.; Misra, R.D.K. Biomimetic chitosan–nanohydroxyapatite composite scaffolds for bone tissue engineering. Acta Biomater. 2009, 5, 1182–1197. [Google Scholar] [CrossRef] [PubMed]
- Maganti, N.; Venkat Surya, P.K.C.; Thein-Han, W.W.; Pesacreta, T.C.; Misra, R.D.K. Structure-process-property relationship of biomimetic chitosan-based nanocomposite scaffolds for tissue engineering: Biological, physico-chemical, and mechanical functions. Adv. Eng. Mater. 2011, 13, B108–B122. [Google Scholar] [CrossRef]
- Teng, S.-H.H.; Lee, E.-J.J.; Yoon, B.-H.H.; Shin, D.-S.S.; Kim, H.-E.E.; Oh, J.-S.S. Chitosan/nanohydroxyapatite composite membranes via dynamic filtration for guided bone regeneration. J. Biomed. Mater. Res. Part A 2009, 88, 569–580. [Google Scholar] [CrossRef]
- Brugnerotto, J.; Lizardi, J.; Goycoolea, F.M.; Argüelles-Monal, W.; Desbrières, J.; Rinaudo, M. An infrared investigation in relation with chitin and chitosan characterization. Polymer 2001, 42, 3569–3580. [Google Scholar] [CrossRef]
- Kim, H.W.; Song, J.H.; Kim, H.E. Nanofiber Generation of Gelatin–Hydroxyapatite Biomimetics for Guided Tissue Regeneration. Adv. Funct. Mater. 2005, 15, 1988–1994. [Google Scholar] [CrossRef]
- Pandey, A.; Jan, E.; Aswath, P.B. Physical and mechanical behavior of hot rolled HDPE/HA composites. J. Mater. Sci. 2006, 41, 3369–3376. [Google Scholar] [CrossRef]
- Abere, D.V.; Oyatogun, G.M.; Akinwole, I.E.; Abioye, A.A.; Rominiyi, A.L.; T., I.M. Effects of Increasing Chitosan Nanofibre Volume Fraction on the Mechanical Property of Hydroxyapatite. Am. J. Mater. Sci. Eng. 2017, 5, 6–16. [Google Scholar] [CrossRef]
- Breuls, R.G.; Jiya, T.U.; Smit, T.H. Scaffold Stiffness Influences Cell Behavior: Opportunities for Skeletal Tissue Engineering. Open Orthop. J. 2008, 2, 103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prasadh, S.; Wong, R.C.W. Unraveling the mechanical strength of biomaterials used as a bone scaffold in oral and maxillofacial defects. Oral Sci. Int. 2018, 15, 48–55. [Google Scholar] [CrossRef]
- Caballé-Serrano, J.; Munar-Frau, A.; Delgado, L.; Pérez, R.; Hernández-Alfaro, F. Physicochemical characterization of barrier membranes for bone regeneration. J. Mech. Behav. Biomed. Mater. 2019, 97, 13–20. [Google Scholar] [CrossRef] [PubMed]
- Raz, P.; Brosh, T.; Ronen, G.; Tal, H. Tensile Properties of Three Selected Collagen Membranes. BioMed Res. Int. 2019, 2019. [Google Scholar] [CrossRef]
- Hunter, K.T.; Ma, T. In vitro evaluation of hydroxyapatite-chitosan-gelatin composite membrane in guided tissue regeneration. J. Biomed. Mater. Res. Part A 2013, 101A, 1016–1025. [Google Scholar] [CrossRef]
- Mohamed, K.R.; Beherei, H.H.; El-Rashidy, Z.M. In vitro study of nano-hydroxyapatite/chitosan–gelatin composites for bio-applications. J. Adv. Res. 2014, 5, 201–208. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Wang, X.; Tan, Y.; Zhang, B.; Gu, Z.; Li, X. Synthesis and evaluation of collagen-chitosan- hydroxyapatite nanocomposites for bone grafting. J. Biomed. Mater. Res. Part A 2009, 89, 1079–1087. [Google Scholar] [CrossRef]
- Mota, J.; Yu, N.; Caridade, S.G.; Luz, G.M.; Gomes, M.E.; Reis, R.L.; Jansen, J.A.; Frank Walboomers, X.; Mano, J.F.; Walboomers, X.F.; et al. Chitosan/bioactive glass nanoparticle composite membranes for periodontal regeneration. Acta Biomater. 2012, 8, 4173–4180. [Google Scholar] [CrossRef] [Green Version]
- Ren, D.; Yi, H.; Wang, W.; Ma, X. The enzymatic degradation and swelling properties of chitosan matrices with different degrees of N-acetylation. Carbohydr. Res. 2005, 340, 2403–2410. [Google Scholar] [CrossRef]
- von Burkersroda, F.; Schedl, L.; Gopferich, A. Why degradable polymers undergo surface erosion or bulk erosion. Biomaterials 2002, 23, 4221–4231. [Google Scholar] [CrossRef]
- Tu, Y.; Chen, C.; Li, Y.; Hou, Y.; Huang, M.; Zhang, L. Fabrication of nano-hydroxyapatite/chitosan membrane with asymmetric structure and its applications in guided bone regeneration. Biomed. Mater. Eng. 2017, 28, 223. [Google Scholar] [CrossRef] [PubMed]
- Aktug, S.L.; Durdu, S.; Kalkan, S.; Cavusoglu, K.; Usta, M. In vitro biological and antimicrobial properties of chitosan-based bioceramic coatings on zirconium. Sci. Rep. 2021, 11, 1–13. [Google Scholar] [CrossRef] [PubMed]
- Paital, S.R.; Dahotre, N.B. Wettability and kinetics of hydroxyapatite precipitation on a laser-textured Ca–P bioceramic coating. Acta Biomater. 2009, 5, 2763–2772. [Google Scholar] [CrossRef]
- Jung, U.-W.; Hwang, J.-W.; Choi, D.-Y.; Hu, K.-S.; Kwon, M.-K.; Choi, S.-H.; Kim, H.-J. Surface characteristics of a novel hydroxyapatite-coated dental implant. J. Periodontal Implant Sci. 2012, 42, 63. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, F.; Wei, M.; Zhang, X.; Song, Y.; Zhou, W.; Wang, Y. How Pore Hydrophilicity Influences Water Permeability? Research 2019, 2019, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Wan, Y.; Yu, A.; Wu, H.; Wang, Z.; Wen, D. Porous-conductive chitosan scaffolds for tissue engineering II. In vitro and in vivo degradation. J. Mater. Sci. Mater. Med. 2005, 16, 1017–1028. [Google Scholar] [CrossRef]
- Liuyun, J.; Yubao, L.; Chengdong, X. Preparation and biological properties of a novel composite scaffold of nano-hydroxyapatite/chitosan/carboxymethyl cellulose for bone tissue engineering. J. Biomed. Sci. 2009, 16, 65–75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tomihata, K.; Ikada, Y. In vitro and in vivo degradation of films of chitin and its deacetylated derivatives. Biomaterials 1997, 18, 567–575. [Google Scholar] [CrossRef]
- Freier, T.; Koh, H.S.; Kazazian, K.; Shoichet, M.S. Controlling cell adhesion and degradation of chitosan films by N-acetylation. Biomaterials 2005, 26, 5872–5878. [Google Scholar] [CrossRef]
- Hankiewicz, J.; Swierczek, E. Lysozyme in human body fluids. Clin. Chim. Acta 1974, 57, 205–209. [Google Scholar] [CrossRef]
- Hamilton, V.; Yuan, Y.L.; Rigney, D.A.; Chesnutt, B.M.; Puckett, A.D.; Ong, J.L.; Yang, Y.Z.; Haggard, W.O.; Elder, S.H.; Bumgardner, J.D. Bone cell attachment and growth on well-characterized chitosan films. Polym. Int. 2007, 56, 641–647. [Google Scholar] [CrossRef]
- Sailaja, G.S.; Ramesh, P.; Kumary, T.V.; Varma, H.K. Human osteosarcoma cell adhesion behaviour on hydroxyapatite integrated chitosan-poly(acrylic acid) polyelectrolyte complex. Acta Biomater. 2006, 2, 651–657. [Google Scholar] [CrossRef] [PubMed]
- Kong, L.; Gao, Y.; Cao, W.; Gong, Y.; Zhao, N.; Zhang, X. Preparation and characterization of nano-hydroxyapatite/chitosan composite scaffolds. J. Biomed. Mater. Res. Part A 2005, 75A, 275–282. [Google Scholar] [CrossRef] [PubMed]
- Przekora, A. The summary of the most important cell-biomaterial interactions that need to be considered during in vitro biocompatibility testing of bone scaffolds for tissue engineering applications. Mater. Sci. Eng. C 2019, 97, 1036–1051. [Google Scholar] [CrossRef]
- Correlo, V.M.; Oliveira, J.M.; Mano, J.F.; Neves, N.M.; Reis, R.L. Natural Origin Materials for Bone Tissue Engineering-Properties, Processing, and Performance. In Principles of Regenerative Medicine; Academic Press: Cambridge, MA, USA, 2011; pp. 557–586. ISBN 9780123814227. [Google Scholar]
- Zomorodian, E.; Baghaban Eslaminejad, M. Mesenchymal stem cells as a potent cell source for bone regeneration. Stem Cells Int. 2012, 2012. [Google Scholar] [CrossRef]
- Jiang, T.; Zhang, Z.; Zhou, Y.; Liu, Y.; Wang, Z.; Tong, H.; Shen, X.; Wang, Y. Surface functionalization of titanium with chitosan/gelatin via electrophoretic deposition: Characterization and cell behavior. Biomacromolecules 2010, 11, 1254–1260. [Google Scholar] [CrossRef]
- Uygun, B.E.; Bou-Akl, T.; Albanna, M.; Matthew, H.W.T.T. Membrane thickness is an important variable in membrane scaffolds: Influence of chitosan membrane structure on the behavior of cells. Acta Biomater. 2010, 6, 2126–2131. [Google Scholar] [CrossRef] [Green Version]
- Park, H.; Choi, B.; Nguyen, J.; Fan, J.B.; Shafi, S.; Klokkevold, P.; Lee, M. Anionic carbohydrate-containing chitosan scaffolds for bone regeneration. Carbohydr. Polym. 2013, 97, 587–596. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, G.C.; Zheng, L.; Zhao, H.S.; Miao, J.Y.; Sun, C.H.; Ren, N.; Wang, J.Y.; Liu, H.; Tao, X.T. In Vitro Assessment of the Differentiation Potential of Bone Marrow-Derived Mesenchymal Stem Cells on Genipin-Chitosan Conjugation Scaffold with Surface Hydroxyapatite Nanostructure for Bone Tissue Engineering. Tissue Eng. Part A 2011, 17, 1341–1349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Qasim, S.S.B.; Baig, M.R.; Matinlinna, J.P.; Daood, U.; Al-Asfour, A. Highly Segregated Biocomposite Membrane as a Functionally Graded Template for Periodontal Tissue Regeneration. Membranes 2021, 11, 667. https://doi.org/10.3390/membranes11090667
Qasim SSB, Baig MR, Matinlinna JP, Daood U, Al-Asfour A. Highly Segregated Biocomposite Membrane as a Functionally Graded Template for Periodontal Tissue Regeneration. Membranes. 2021; 11(9):667. https://doi.org/10.3390/membranes11090667
Chicago/Turabian StyleQasim, Syed Saad B., Mirza Rustum Baig, Jukka Pekka Matinlinna, Umer Daood, and Adel Al-Asfour. 2021. "Highly Segregated Biocomposite Membrane as a Functionally Graded Template for Periodontal Tissue Regeneration" Membranes 11, no. 9: 667. https://doi.org/10.3390/membranes11090667