[en] In recent years, multicomponent hydrogels such as interpenetrating polymer networks (IPNs) have emerged as innovative biomaterials due to the synergistic combination of the properties of each network. We hypothesized that an innovative non-animal IPN hydrogel combining self-setting silanized hydroxypropyl methylcellulose (Si-HPMC) with photochemically cross-linkable dextran methacrylate (DexMA) could be a valid alternative to porcine collagen membranes in guided bone regeneration. Calvaria critical-size defects in rabbits were filled with synthetic biphasic calcium phosphate granules in conjunction with Si-HPMC; DexMA; or Si-HPMC/DexMA experimental membranes; and in a control group with a porcine collagen membrane. The synergistic effect obtained by interpenetration of the two polymer networks improved the physicochemical properties, and the gel point under visible light was reached instantaneously. Neutral red staining of murine L929 fibroblasts confirmed the cytocompatibility of the IPN. At 8 weeks, the photo-crosslinked membranes induced a similar degree of mineral deposition in the calvaria defects compared to the positive control, with 30.5 ± 5.2% for the IPN and 34.3 ± 8.2% for the collagen membrane. The barrier effect appeared to be similar in the IPN test group compared with the collagen membrane. In conclusion, this novel, easy-to-handle and apply, photochemically cross-linkable IPN hydrogel is an excellent non-animal alternative to porcine collagen membrane in guided bone regeneration procedures.
Disciplines :
Chimie
Auteur, co-auteur :
Chichiricco, Pauline Marie; CESAM Research Unit, Center for Education and Research on Macromolecules (CERM), University of Liège, B-4000 Liège, Belgium ; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Matricardi, Pietro ; Department of Drug Chemistry and Technologies, Sapienza University, 000185 Rome, Italy
Colaço, Bruno ; Department of Animal Sciences, Animal and Veterinary Research Centre, University of Trás-os-Montes and Alto Douro, 500-801 Vila Real, Portugal
Gomes, Pedro; FMDUP, Laboratory for Bone Metabolism and Regeneration, Faculty of Dental Medicine, University of Porto, 500-801 Porto, Portugal
Jérôme, Christine ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie des macromolécules et des matériaux organiques (CERM)
Lesoeur, Julie; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Veziers, Joëlle; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Réthoré, Gildas; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Weiss, Pierre ; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Struillou, Xavier ; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Le Visage, Catherine ; Nantes Université, Oniris, Univ Angers, INSERM, Regenerative Medicine and Skeleton, RMeS, UMR 1229, F-44000 Nantes, France
Langue du document :
Anglais
Titre :
Injectable Hydrogel Membrane for Guided Bone Regeneration.
EU - European Union ANR - French National Research Agency
Subventionnement (détails) :
This research was supported by supported by the Erasmus Mundus Doctoral School NanoFar from the European Community, the ERA-NET EuroNanoMed II (POSTURE: Photocrosslinked hydrogels for guided periodontal Tissue Regeneration) and the French National Research Agency (ANR-14-ENM2-0003-01).
Yu L. Ding J. Injectable hydrogels as unique biomedical materials Chem. Soc. Rev. 2008 37 1473 10.1039/b713009k 18648673
Liu M. Zeng X. Ma C. Yi H. Ali Z. Mou X. Li S. Deng Y. He N. Injectable hydrogels for cartilage and bone tissue engineering Bone Res. 2017 5 14 10.1038/boneres.2017.14 28584674
Dragan E. Design and applications of interpenetrating polymer network hydrogels. A review Chem. Eng. J. 2014 243 572 590 10.1016/j.cej.2014.01.065
Annabi N. Tamayol A. Uquillas J.A. Akbari M. Bertassoni E.L. Cha C. Camci-Unal G. Dokmeci R.M. Peppas A.N. Khademhosseini A. 25th Anniversary Article: Rational design and applications of hydrogels in regenerative medicine Adv. Mater. 2014 26 85 124 10.1002/adma.201303233 24741694
Edalat F. Bae H. Manoucheri S. Cha J.M. Khademhosseini A. Engineering Approaches Toward Deconstructing and Controlling the Stem Cell Environment Ann. Biomed. Eng. 2012 40 1301 1315 10.1007/s10439-011-0452-9
Ma F. Zhang Y. Hu L. Peng Y. Deng Y. He W. Ge Y. Tang B. Strontium Laminarin polysaccharide modulates osteogenesis-angiogenesis for bone regenera-tion Int. J. Biol. Macromol. 2021 181 452 461 10.1016/j.ijbiomac.2021.03.136
Matricardi P. Di Meo C. Coviello T. Hennink W. Alhaique F. Interpenetrating polymer networks polysaccharide hydrogels for drug delivery and tissue engineering Adv. Drug Deliv. Rev. 2013 65 1172 1187 10.1016/j.addr.2013.04.002
Khan M.U.A. Razak S.I.A. Rehman S. Hasan A. Qureshi S. Stojanović G.M. Bioactive scaffold (sodium alginate)-g-(nHAp@SiO2@GO) for bone tissue engineering Int. J. Biol. Macromol. 2022 222 462 472 10.1016/j.ijbiomac.2022.09.153
Hached F. Vinatier C. Pinta P. Hulin P. Le Visage C. Weiss P. Guicheux J. Billon-Chabaud A. Grimandi G. Polysaccharide hydrogels support the long-Term viability of encapsulated human mesenchymal stem cells and their ability to secrete immunomodulatory factors Stem Cells Int. 2017 6 8 10.1155/2017/9303598
Dimitriou R. Jones E. McGonagle D. Giannoudis P. Bone regeneration: Current concepts and future directions BMC Med. 2011 9 66 10.1186/1741-7015-9-66
Retzepi M. Donos N. Guided Bone Regeneration: Biological principle and therapeutic applications Clin. Oral Implants Res. 2010 21 567 576 10.1111/j.1600-0501.2010.01922.x
Elgali I. Omar O. Dahlin C. Thomsen P. Guided bone regeneration: Materials and biological mechanisms revisited Eur. J. Oral Sci. 2017 125 315 337 10.1111/eos.12364
Milella E. Ramires P. Brescia E. La Sala G. Di Paola L. Bruno V. Physicochemical, mechanical, and biological properties of commercial membranes for GTR J. Biomed. Mater. Res. 2001 58 427 435 10.1002/jbm.1038
Bottino M. Thomas V. Schmidt G. Vohra Y. Chu T. Kowolik M. Janowski G. Lafayette W. Recent advances in the development of GTR/GBR membranes for periodontal regeneration — A materials perspective Dent. Mater. 2012 28 703 721 10.1016/j.dental.2012.04.022
Nasser N. Friedman A. Friedman M. Moor E. Mosheiff R. Guided bone regeneration in the treatment of segmental diaphyseal defects: A comparison between resorbable and non-resorbable membranes Injury 2005 36 1460 1466 10.1016/j.injury.2005.05.015
Jose R. Rodriguez M. Dixon T. Omenetto F. Kaplan D. Evolution of Bioinks and Additive Manufacturing Technologies for 3D Bioprinting Biomater. Sci. Eng. 2016 2 1662 1678 10.1021/acsbiomaterials.6b00088
Dimitriou R. Mataliotakis G. Calori G. Giannoudis P. The role of barrier membranes for guided bone regeneration and restoration of large bone defects: Current experimental and clinical evidence BMC Med. 2012 10 81 10.1186/1741-7015-10-81
Jung R.E. Hälg G.A. Thoma D.S. Hämmerle C.H.F. A randomized, controlled clinical trial to evaluate a new membrane for guided bone regeneration around dental implants Clin. Oral Implants Res. 2009 20 162 168 10.1111/j.1600-0501.2008.01634.x
Coonts B.A. Whitman S.L. Donnell M.O. Polson A.M. Bogle G. Garrett S. Swanbom D.D. Fulfs J.C. Rodgers P.W. Southard G.L. et al. Biodegradation and biocompatibility of a guided tissue regeneration barrier membrane formed from a liquid polymer material J. Biomed. Mater. Res. 1998 42 303 311 10.1002/(SICI)1097-4636(199811)42:2<303::AID-JBM16>3.0.CO;2-J
Fatimi A. Tassin J.F. Quillard S. Axelos M.A.V. Weiss P. The rheological properties of silated hydroxypropylmethylcellulose tissue engineering matrices Biomaterials 2008 29 533 543 10.1016/j.biomaterials.2007.10.032
Fatimi A. Tassin J.F. Turczyn R. Axelos M.A.V. Weiss P. Gelation studies of a cellulose-based biohydrogel: The influence of pH, temperature and sterilization Acta Biomater. 2009 5 3423 3432 10.1016/j.actbio.2009.05.030 19481183
Bourges X. Weiss P. Daculsi G. Legeay G. Synthesis and general properties of silated-hydroxypropyl methylcellulose in prospect of biomedical use Adv. Colloid Interface Sci. 2002 99 215 228 10.1016/S0001-8686(02)00035-0 12509115
Henry N. Clouet J. Fragale A. Griveau L. Véziers J. Weiss P. Le Bideau J. Guicheux J. Henry N. Clouet J. et al. Pullulan microbeads/Si-HPMC hydrogel injectable system for the sustained delivery of GDF-5 and TGF- β 1: New insight into intervertebral disc regenerative medicine Drug Deliv. 2017 24 999 1010 10.1080/10717544.2017.1340362 28645219
Merceron C. Portron S. Masson M. Lesoeur J. Fellah B. Gauthier O. Geffroy O. Weiss P. The Effect of Two- and Three-Dimensional Cell Culture on the Chondrogenic Potential of Human Adipose-Derived Mesenchymal Stem Cells After Subcutaneous Transplantation with an Injectable Hydrogel Cell Transpl. 2011 20 1575 1588 10.3727/096368910X557191 21294960
Struillou X. Boutigny H. Badran Z. Fellah B. Gauthier O. Sourice S. Pilet P. Rouillon T. Layrolle P. Weiss P. et al. Treatment of periodontal defects in dogs using an injectable composite hydrogel/biphasic calcium phosphate J. Mater. Sci. Mater. Med. 2011 22 1707 1717 10.1007/s10856-011-4344-1
Struillou X. Fruchet A. Rakic M. Badran Z. Rethore G. Sourice S. Fellah B. Le Guehennec L. Gauthier O. Weiss P. et al. Evaluation of a hydrogel membrane on bone regeneration in furcation periodontal defects in dogs Dent. Mater. J. 2018 37 825 834 10.4012/dmj.2017-238
Davis K. Burdick J. Anseth K. New directions in photopolymerizable biomaterials Biomaterials 2003 24 2485 2495 10.1016/S0142-9612(02)00582-3
Burkoth A. Anseth K. A review of photocrosslinked polyanhydrides: In situ forming degradable networks Biomaterials 2000 21 2395 2404 10.1016/S0142-9612(00)00107-1
Ifkovits J.L. Burdick J.A. Review: Photopolymerizable and degradable biomaterials for tissue engineering applications J. Tissue Eng. 2007 13 2369 2385 10.1089/ten.2007.0093
Wu N. Zhang Y. Wang Y. Photo-polymerization efficiency of self-etch dental adhesives composed of camphorquinone or trimethylbenzoyl-diphenyl-phosphine oxide Int. J. Adhes. Adhes. 2013 45 53 58 10.1016/j.ijadhadh.2013.04.002
Steenbergenj V. Den Bosch K. Henninkt W. Synthesis, Characterization, and Polymerization of Glycidyl Methacrylate Derivatized Dextran Macromolecules 1995 28 6317 6322
Van Dijk-Wolthuis W. Kettenes-van den Bosch J.J. van der Kerk-van Hoof A. Hennink W. Reaction of Dextran with Glycidyl Methacrylate: An Unexpected Transesterification Macromolecules 1997 30 3411 3413 10.1021/ma961764v
D’Arrigo G. Di Meo C. Pescosolido L. Coviello T. Alhaique F. Matricardi P. Calcium alginate/dextran methacrylate IPN beads as protecting carriers for protein delivery J. Mater. Sci. Mater. Med. 2012 23 1715 1722 10.1007/s10856-012-4644-0
Pescosolido L. Schuurman W. Malda J. Matricardi P. Alhaique F. Coviello T. Van Weeren P. Dhert W. Hennink W. Vermonden T. Hyaluronic acid and dextran-based semi-IPN hydrogels as biomaterials for bioprinting Biomacromolecules 2011 12 1831 1838 10.1021/bm200178w
Matricardi P. Pontoriero M. Coviello T. Casadei M. Alhaique F. In situ cross-linkable novel alginate-dextran methacrylate IPN hydrogels for biomedical applications: Mechanical characterization and drug delivery properties Biomacromolecules 2008 9 2014 2020 10.1021/bm800252c
Pescosolido L. Vermonden T. Malda J. Censi R. Dhert W. Alhaique F. Hennink W. Matricardi P. In situ forming IPN hydrogels of calcium alginate and dextran-HEMA for biomedical applications Acta Biomater. 2011 7 1627 1633 10.1016/j.actbio.2010.11.040
Mirahmadi F. Tafazzoli-Shadpour M. Shokrgozar M. Bonakdar S. Enhanced mechanical properties of thermosensitive chitosan hydrogel by silk fibers for cartilage tissue engineering Mater. Sci. Eng. C 2013 33 4786 4794 10.1016/j.msec.2013.07.043
Jin R. Teixeira L.M. Dijkstra P. Karperien M. van Blitterswijk C. Zhong Z. Feijen J. Injectable chitosan-based hydrogels for cartilage tissue engineering J. Biomater. 2009 30 2544 2551 10.1016/j.biomaterials.2009.01.020
Van Dijk-Wolthuis W. Van Steenbergen M. Underberg W. Hennink W. Degradation kinetics of methacrylated dextrans in aqueous solution J. Pharm. Sci. 1997 86 413 417 10.1021/js9604220
Flégeau K. Pace R. Gautier H. Rethore G. Guicheux J. Le C. Weiss P. Toward the development of biomimetic injectable and macroporous biohydrogels for regenerative medicine Adv. Colloid Interface Sci. 2017 247 589 609 10.1016/j.cis.2017.07.012
Encinas M. Rufs A. Bertolotti S. Previtali C. Free Radical Polymerization Photoinitiated by Riboflavin/Amines. Effect of the Amine Structure Excit. States 2001 2845 2847 10.1021/ma001649r
Bertolotti S. Previtali C. Rufs A. Encinas M.V. Riboflavin/triethanolamine as photoinitiator system of vinyl polymerization. A mechanistic study by laser flash photolysis Macromolecules 1999 32 2920 2924 10.1021/ma981246f
Williams C. Malik A. Kim T. Manson P. Elisseeff J.H. Variable cytocompatibility of six cell lines with photoinitiators used for polymerizing hydrogels and cell encapsulation J. Biomater. 2005 26 1211 1218 10.1016/j.biomaterials.2004.04.024 15475050
Elbadawy H. Kamoun A. Crosslinking Behavior of Dextran Modified with Hydroxyethyl Methacrylate upon Irradiation with Visible Light—Effect of Concentration, Coinitiator Type, and Solvent InterScience 2010 21 449 456
Kim S. Chu C. Visible light induced dextran-methacrylate hydrogel formation using (-)-riboflavin vitamin B2 as a photoinitiator and L-arginine as a co-initiator Fibers Polym. 2009 10 14 20 10.1007/s12221-009-0014-z
Sheikh Z. Qureshi J. Alshahrani A. Nassar H. Ikeda Y. Glogauer M. Ganss B. Collagen based barrier membranes for periodontal guided bone regeneration applications Odontology 2017 105 1 12 10.1007/s10266-016-0267-0
SLi T. Chen H.-C. Lee N. Ringshia R. Yuen D. A Comparative study of Zimmer BioMend® and BioMend® Extend{\texttrademark} membranes made at two different manufacturing facilities Zimmer 2013 1 5
Garcia J.J. Berghezan S. Caramês J. Dard M. Marques D. Effect of cross-linked vs. non-cross-linked collagen membranes on bone: A systematic review J. Periodontal Res. 2017 52 955 964 10.1111/jre.12470
Mathieu E. Lamirault G. Toquet C. Lhommet P. Rederstorff E. Sourice S. Biteau K. Hulin P. Forest V. Weiss P. et al. Intramyocardial Delivery of Mesenchymal Stem Cell-Seeded Hydrogel Preserves Cardiac Function and Attenuates Ventricular Remodeling after Myocardial Infarction PLoS ONE 2012 7 e51991 10.1371/journal.pone.0051991
Nativel F. Renard D. Hached F. Pinta P. Arros C. Weiss P. Le Visage C. Billon-Chabaud A. Application of Millifluidics to Encapsulate and Support Viable Human Mesenchymal Stem Cells in a Polysaccharide Hydrogel Int. J. Mol. Sci. 2018 19 1952 10.3390/ijms19071952
Moussa L. Pattappa G. Doix B. Benselama S. Demarquay C. Benderitter M. Alexandra S. Weiss P. Rethore G. A biomaterial-assisted mesenchymal stromal cell therapy alleviates colonic radiation-induced damage Biomaterials 2017 115 40 52 10.1016/j.biomaterials.2016.11.017
Viguier A. Boyer C. Chassenieux C. Benyahia L. Guicheux J. Weiss P. Rethore G. Nicolai T. Interpenetrated Si-HPMC/alginate hydrogels as a potential scaffold for human tissue regeneration J. Mater. Sci. Mater. Med. 2016 27 99 10.1007/s10856-016-5709-2
Park J. Jung I. Kim Y. Lim H. Lee J. Jung U. Choi S. Guided bone regeneration using 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide (EDC)-cross-linked type-I collagen membrane with biphasic calcium phosphate at rabbit calvarial defects Biomater. Res. 2015 19 15 10.1186/s40824-015-0038-y
Park J. Kang D. Hanawa T. New bone formation induced by surface strontium-modified ceramic bone graft substitute Oral Dis. 2016 22 53 61 10.1111/odi.12381
Al-Qutub M. Al-Omar N. Ramalingam S. Javed F. Al-Kindi M. Ar-Rejaie A. Aldahmash A. Nooh N. Wang H.-L. Al-Hezaimi K. Guided Bone Regeneration Using Biphasic Calcium Phosphate with Adjunct Recombinant Human Bone Morphogenetic Protein-2 With and Without Collagen Membrane in Standardized Calvarial Defects in Rats: A Histologic and Biomechanical Analysis Int. J. Periodontics Restor. Dent. 2016 36 s1 10.11607/prd.2376
