Bone Scaffold Materials in Periodontal and Tooth-supporting Tissue
Regeneration: A Review

Mahmood      Jahangirnezhad; Sadaf   Sadat   Mahmoudinezhad; Melika      Moradi; Kooshan      Moradi; Ali      Rohani; Lobat      Tayebi
doi:10.2174/1574888X18666221227142055
Abstract

Background and Objectives: Periodontium is an important tooth-supporting tissue composed of both hard (alveolar bone and cementum) and soft (gingival and periodontal ligament) sections. Due to the multi-tissue architecture of periodontium, reconstruction of each part can be influenced by others. This review focuses on the bone section of the periodontium and presents the materials used in tissue engineering scaffolds for its reconstruction.
Materials and Methods: The following databases (2015 to 2021) were electronically searched: ProQuest, EMBASE, SciFinder, MRS Online Proceedings Library, Medline, and Compendex. The search was limited to English-language publications and in vivo studies.
Results: Eighty-three articles were found in primary searching. After applying the inclusion criteria, seventeen articles were incorporated into this study.
Conclusion: In complex periodontal defects, various types of scaffolds, including multilayered ones, have been used for the functional reconstruction of different parts of periodontium. While there are some multilayered scaffolds designed to regenerate alveolar bone/periodontal ligament/cementum tissues of periodontium in a hierarchically organized construct, no scaffold could so far consider all four tissues involved in a complete periodontal defect. The progress and material considerations in the regeneration of the bony part of periodontium are presented in this work to help investigators develop tissue engineering scaffolds suitable for complete periodontal regeneration.
Keywords: Bone scaffold, periodontal regeneration, periodontal tissue engineering, bone regeneration materials, progenitor cells, periodontal ligament.
« Previous Next »
Graphical Abstract

[1]
Peres MA, Macpherson LMD, Weyant RJ, et al. Oral diseases: a global public health challenge. Lancet  2019; 394(10194): 249-60.
 [http://dx.doi.org/10.1016/S0140-6736(19)31146-8] [PMID:  31327369]

[2]
Frencken JE, Sharma P, Stenhouse L, Green D, Laverty D, Dietrich T. Global epidemiology of dental caries and severe periodontitis - a comprehensive review. J Clin Periodontol  2017; 44 (Suppl. 18): S94-S105.
 [http://dx.doi.org/10.1111/jcpe.12677] [PMID:  28266116]

[3]
Woo HN, Cho YJ, Tarafder S, Lee CH. The recent advances in scaffolds for integrated periodontal regeneration. Bioact Mater  2021; 6(10): 3328-42.
 [http://dx.doi.org/10.1016/j.bioactmat.2021.03.012] [PMID:  33817414]

[4]
Bottino MC, Thomas V, Schmidt G, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration—A materials perspective. Dent Mater  2012; 28(7): 703-21.
 [http://dx.doi.org/10.1016/j.dental.2012.04.022] [PMID:  22592164]

[5]
Liang Y, Luan X, Liu X. Recent advances in periodontal regeneration: A biomaterial perspective. Bioact Mater  2020; 5(2): 297-308.
 [http://dx.doi.org/10.1016/j.bioactmat.2020.02.012] [PMID:  32154444]

[6]
Hasani-Sadrabadi MM, Sarrion P, Nakatsuka N, et al. Hierarchically patterned polydopamine-containingmembranesfor periodontal tissue engineering. ACS Nano  2019; 13(4): 3830-8.
 [http://dx.doi.org/10.1021/acsnano.8b09623] [PMID:  30895772]

[7]
Tan J, Zhang M, Hai Z, et al. Sustained release of two bioactive factors from supramolecular hydrogel promotes periodontal bone regeneration. ACS Nano  2019; 13(5): 5616-22.
 [http://dx.doi.org/10.1021/acsnano.9b00788] [PMID:  31059238]

[8]
Aytac Z, Dubey N, Daghrery A, et al. Innovations in craniofacial bone and periodontal tissueengineering–fromelectrospinning to converged biofabrication. Int Mater Rev  2021; 67(4): 347-84.
 [PMID:  35754978]

[9]
Kao RT, Murakami S, Beirne OR. The use of biologic mediators and tissue engineering in dentistry. Periodontol 2000  2009; 50(1): 127-53.
 [http://dx.doi.org/10.1111/j.1600-0757.2008.00287.x] [PMID:  19388957]

[10]
Dabra S, Chhina K, Soni N, Bhatnagar R. Tissue engineering in periodontal regeneration: A brief review. Dent Res J (Isfahan)  2012; 9(6): 671-80.
 [PMID:  23559940]

[11]
Oldham JB, Lu L, Zhu X, Porter BD, Hefferan TE, Larson DR, et al. Biological activity of rhBMP-2 released from PLGA microspheres. J Biomech Eng  2000; 122(3): 289-92. [Available from]:
 [http://dx.doi.org/10.1115/1.429662]

[12]
Henkel J, Woodruff MA, Epari DR, et al. Bone regeneration based on tissue engineering conceptions—a 21st century perspective. Bone Res  2013; 1(3): 216-48.
 [http://dx.doi.org/10.4248/BR201303002] [PMID:  26273505]

[13]
Wang CY, Chiu YC, Lee AKX, Lin YA, Lin PY, Shie MY. Biofabrication of gingival fibroblast cell-laden collagen/strontium-doped calcium silicate 3D-printed bi-layered scaffold for osteoporotic periodontal regeneration. Biomedicines  2021; 9(4): 431.
 [http://dx.doi.org/10.3390/biomedicines9040431] [PMID:  33923505]

[14]
Smith BD, Grande DA. The current state of scaffolds for musculoskeletal regenerative applications. Nat Rev Rheumatol  2015; 11(4): 213-22.
 [http://dx.doi.org/10.1038/nrrheum.2015.27] [PMID:  25776947]

[15]
Chen FM, Liu X. Advancing biomaterials of human origin for tissue engineering. Prog Polym Sci  2016; 53: 86-168.
 [http://dx.doi.org/10.1016/j.progpolymsci.2015.02.004] [PMID:  27022202]

[16]
Park SB, Lih E, Park KS, Joung YK, Han DK. Biopolymer-based functional composites for medical applications. Prog Polym Sci  2017; 68: 77-105.
 [http://dx.doi.org/10.1016/j.progpolymsci.2016.12.003]

[17]
Stoppel WL, Ghezzi CE, McNamara SL, Iii LDB, Kaplan DL. Clinical applications of naturally derived biopolymer-based scaffolds for regenerative medicine. Ann Biomed Eng  2015; 43(3): 657-80.
 [http://dx.doi.org/10.1007/s10439-014-1206-2] [PMID:  25537688]

[18]
Hussey GS, Dziki JL, Badylak SF. Extracellular matrix-based materials for regenerative medicine. Nat Rev Mater  2018; 3(7): 159-73.
 [http://dx.doi.org/10.1038/s41578-018-0023-x]

[19]
Chan G, Mooney DJ. New materials for tissue engineering: towards greater control over the biological response. Trends Biotechnol  2008; 26(7): 382-92.
 [http://dx.doi.org/10.1016/j.tibtech.2008.03.011] [PMID:  18501452]

[20]
Zhuang Y, Lin K, Yu H. Advance of nano-composite electrospun fibers in periodontal regeneration. Front Chem  2019; 7: 495.
 [http://dx.doi.org/10.3389/fchem.2019.00495] [PMID:  31355186]

[21]
Zhu L, Luo D, Liu Y. Effect of the nano/microscale structure of biomaterial scaffolds on bone regeneration. Int J Oral Sci  2020; 12(1): 6.
 [http://dx.doi.org/10.1038/s41368-020-0073-y] [PMID:  32024822]

[22]
Tcacencu I, Rodrigues N, Alharbi N, et al. Osseointegration of porous apatite-wollastonite and poly(lactic acid) composite structures created using 3D printing techniques. Mater Sci Eng C  2018; 90: 1-7.
 [http://dx.doi.org/10.1016/j.msec.2018.04.022] [PMID:  29853072]

[23]
Chen Q, Zhu C, Thouas GA. Progress and challenges in biomaterials used for bone tissue engineering: bioactive glasses and elastomeric composites. Prog Biomater  2012; 1(1): 2.
 [http://dx.doi.org/10.1186/2194-0517-1-2] [PMID:  29470743]

[24]
Abbasi N, Hamlet S, Dau VT, Nguyen N-T. Calcium phosphate stability on melt electrowritten PCL scaffolds. J Sci Adv Mater Devices  2020; 5(1): 30-9.
 [http://dx.doi.org/10.1016/j.jsamd.2020.01.001]

[25]
Liu J, Jin T, Chang S, et al. The effect of novel fluorapatite surfaces on osteoblast-like cell adhesion, growth, and mineralization. Tissue Eng Part A  2010; 16(9): 2977-86.
 [http://dx.doi.org/10.1089/ten.tea.2009.0632] [PMID:  20412028]

[26]
Bartold PM, Gronthos S, Ivanovski S, Fisher A, Hutmacher DW. Tissue engineered periodontal products. J Periodontal Res  2016; 51(1): 1-15.
 [http://dx.doi.org/10.1111/jre.12275] [PMID:  25900048]

[27]
Rasperini G, Pilipchuk SP, Flanagan CL, et al. 3D-printed bioresorbable scaffold for periodontal repair. J Dent Res  2015; 94 (Suppl. 9): 153S-7S.
 [http://dx.doi.org/10.1177/0022034515588303] [PMID:  26124215]

[28]
Yilgor P, Sousa RA, Reis RL, Hasirci N, Hasirci V. 3D plotted PCL scaffolds for stem cell based bone tissue engineering. Macromol Symp  2008; 269(1): 92-9.

[29]
Dwivedi R, Kumar S, Pandey R, et al. Polycaprolactone as biomaterial for bone scaffolds: Review of literature. J Oral Biol Craniofac Res  2020; 10(1): 381-8.
 [http://dx.doi.org/10.1016/j.jobcr.2019.10.003] [PMID:  31754598]

[30]
Rotbaum Y, Puiu C, Rittel D, Domingos M. Quasi-static and dynamic in vitro mechanical response of 3D printed scaffolds with tailored pore size and architectures. Mater Sci Eng C  2019; 96: 176-82.
 [http://dx.doi.org/10.1016/j.msec.2018.11.019] [PMID:  30606523]

[31]
Kashirina A, Yao Y, Liu Y, Leng J. Biopolymers as bone substitutes: a review. Biomater Sci  2019; 7(10): 3961-83.
 [http://dx.doi.org/10.1039/C9BM00664H] [PMID:  31364613]

[32]
Bayani M, Torabi S, Shahnaz A, Pourali M. Main properties of nanocrystalline hydroxyapatite as a bone graft material in treatment of periodontal defects. A review of literature. Biotechnol Biotechnol Equip  2017; 31(2): 215-20.
 [http://dx.doi.org/10.1080/13102818.2017.1281760]

[33]
Brunello G, Panda S, Schiavon L, Sivolella S, Biasetto L, Del Fabbro M. The impact of bioceramic scaffolds on bone regeneration in preclinical in vivo studies: a systematic review. Materials (Basel)  2020; 13(7): 1500.
 [http://dx.doi.org/10.3390/ma13071500] [PMID:  32218290]

[34]
Salinas AJ, Esbrit P, Vallet-Regí M. A tissue engineering approach based on the use of bioceramics for bone repair. Biomater Sci  2013; 1(1): 40-51.
 [http://dx.doi.org/10.1039/C2BM00071G] [PMID:  32481996]

[35]
Mancuso E, Bretcanu OA, Marshall M, Birch MA, McCaskie AW, Dalgarno KW. Novel bioglasses for bone tissue repair and regeneration: Effect of glass design on sintering ability, ion release and biocompatibility. Mater Des  2017; 129: 239-48.
 [http://dx.doi.org/10.1016/j.matdes.2017.05.037] [PMID:  28883669]

[36]
Carter SSD, Costa PF, Vaquette C, Ivanovski S, Hutmacher DW, Malda J. Additive biomanufacturing: an advancedapproach for periodontal tissue regeneration. Ann Biomed Eng  2017; 45(1): 12-22.
 [http://dx.doi.org/10.1007/s10439-016-1687-2] [PMID:  27473707]

[37]
Eap S, Ferrand A, Mendoza Palomares C, et al. Electrospun nanofibrous 3D scaffold for bone tissue engineering. Biomed Mater Eng  2012; 22(1-3): 137-41.
 [http://dx.doi.org/10.3233/BME-2012-0699] [PMID:  22766712]

[38]
Vaquette C, Fan W, Xiao Y, Hamlet S, Hutmacher DW, Ivanovski S. A biphasic scaffold design combined with cell sheet technology for simultaneous regeneration of alveolar bone/periodontal ligament complex. Biomaterials  2012; 33(22): 5560-73.
 [http://dx.doi.org/10.1016/j.biomaterials.2012.04.038] [PMID:  22575832]

[39]
Farag A, Vaquette C, Theodoropoulos C, Hamlet SM, Hutmacher DW, Ivanovski S. Decellularized periodontal ligament cell sheets with recellularization potential. J Dent Res  2014; 93(12): 1313-9.
 [http://dx.doi.org/10.1177/0022034514547762] [PMID:  25270757]

[40]
Eap S, Keller L, Schiavi J, et al. A living thick nanofibrous implant bifunctionalized with active growth factor and stem cells for bone regeneration. Int J Nanomedicine  2015; 10: 1061-75.
 [PMID:  25709432]

[41]
Mathew A, Vaquette C, Hashimi S, et al. Antimicrobial and immunomodulatory surface‐functionalized electrospun membranes for bone regeneration. Adv Healthc Mater  2017; 6(10): 1601345.
 [http://dx.doi.org/10.1002/adhm.201601345] [PMID:  28240815]

[42]
Ferrand A, Eap S, Richert L, et al. Osteogenetic properties of electrospun nanofibrous PCL scaffolds equipped with chitosan-based nanoreservoirs of growth factors. Macromol Biosci  2014; 14(1): 45-55.
 [http://dx.doi.org/10.1002/mabi.201300283] [PMID:  23956214]

[43]
Ren K, Wang Y, Sun T, Yue W, Zhang H. Electrospun PCL/gelatin composite nanofiber structures for effective guided bone regeneration membranes. Mater Sci Eng C  2017; 78: 324-32.
 [http://dx.doi.org/10.1016/j.msec.2017.04.084] [PMID:  28575991]

[44]
Lam CXF, Savalani MM, Teoh SH, Hutmacher DW. Dynamics of in vitro polymer degradation of polycaprolactone-based scaffolds: accelerated versus simulated physiological conditions. Biomed Mater  2008; 3(3): 034108.
 [http://dx.doi.org/10.1088/1748-6041/3/3/034108] [PMID:  18689929]

[45]
Woodruff MA, Hutmacher DW. The return of a forgotten polymer—Polycaprolactone in the 21st century. Prog Polym Sci  2010; 35(10): 1217-56.
 [http://dx.doi.org/10.1016/j.progpolymsci.2010.04.002]

[46]
Campbell JH, Efendy JL, Campbell GR. Novel vascular graft grown within recipient’s own peritoneal cavity. Circ Res  1999; 85(12): 1173-8.
 [http://dx.doi.org/10.1161/01.RES.85.12.1173] [PMID:  10590244]

[47]
Kim CH, Khil MS, Kim HY, Lee HU, Jahng KY. An improved hydrophilicity via electrospinning for enhanced cell attachment and proliferation. J Biomed Mater Res B Appl Biomater  2006; 78B(2): 283-90.
 [http://dx.doi.org/10.1002/jbm.b.30484] [PMID:  16362963]

[48]
Fabbri P, Bondioli F, Messori M, Bartoli C, Dinucci D, Chiellini F. Porous scaffolds of polycaprolactone reinforced with in situ generated hydroxyapatite for bone tissue engineering. J Mater Sci Mater Med  2010; 21(1): 343-51.
 [http://dx.doi.org/10.1007/s10856-009-3839-5] [PMID:  19653069]

[49]
Chen JP, Chang YS. Preparation and characterization of composite nanofibers of polycaprolactone and nanohydroxyapatite for osteogenic differentiation of mesenchymal stem cells. Colloids Surf B Biointerfaces  2011; 86(1): 169-75.
 [http://dx.doi.org/10.1016/j.colsurfb.2011.03.038] [PMID:  21514800]

[50]
Hassan MI, Sultana N. Characterization, drug loading and antibacterial activity of nanohydroxyapatite/polycaprolactone (nHA/PCL) electrospun membrane. 3 Biotech  2017; 7(4): 1-9.

[51]
Groppo MF, Caria PH, Freire AR, et al. The effect of a hydroxyapatite impregnated PCL membrane in rat subcritical calvarial bone defects. Arch Oral Biol  2017; 82: 209-15.
 [http://dx.doi.org/10.1016/j.archoralbio.2017.06.018] [PMID:  28651093]

[52]
Park SH, Kim TI, Ku Y, et al. Effect of hydroxyapatite-coated nanofibrous membrane on the responses of human periodontal ligament fibroblast. J Ceram Soc Jpn  2008; 116(1349): 31-5.
 [http://dx.doi.org/10.2109/jcersj2.116.31]

[53]
Peng F, Yu X, Wei M. In vitro cell performance on hydroxyapatite particles/poly(l-lactic acid) nanofibrous scaffolds with an excellent particle along nanofiber orientation. Acta Biomater  2011; 7(6): 2585-92.
 [http://dx.doi.org/10.1016/j.actbio.2011.02.021] [PMID:  21333762]

[54]
Chiara G, Letizia F, Lorenzo F, et al. Nanostructured biomaterials for tissue engineered bone tissue reconstruction. Int J Mol Sci  2012; 13(1): 737-57.
 [http://dx.doi.org/10.3390/ijms13010737] [PMID:  22312283]

[55]
Kasaj A, Willershausen B, Reichert C, Röhrig B, Smeets R, Schmidt M. Ability of nanocrystalline hydroxyapatite paste to promote human periodontal ligament cell proliferation. J Oral Sci  2008; 50(3): 279-85.
 [http://dx.doi.org/10.2334/josnusd.50.279] [PMID:  18818463]

[56]
Higuchi J, Fortunato G, Woźniak B, et al. Polymer membranes sonocoated and electrosprayed with nano-hydroxyapatite for periodontal tissues regeneration. Nanomaterials (Basel)  2019; 9(11): 1625.
 [http://dx.doi.org/10.3390/nano9111625] [PMID:  31731775]

[57]
Sattary M, Khorasani MT, Rafienia M, Rozve HS. Incorporation of nanohydroxyapatite and vitamin D3 into electrospun PCL/Gelatin scaffolds: The influence on the physical and chemical properties and cell behavior for bone tissue engineering. Polym Adv Technol  2018; 29(1): 451-62.
 [http://dx.doi.org/10.1002/pat.4134]

[58]
Kanaya S, Nemoto E, Sakisaka Y, Shimauchi H. Calcium-mediated increased expression of fibroblast growth factor-2 acts through NF-κB and PGE2/EP4 receptor signaling pathways in cementoblasts. Bone  2013; 56(2): 398-405.
 [http://dx.doi.org/10.1016/j.bone.2013.06.031] [PMID:  23851295]

[59]
Roopavath UK, Malferrari S, Van Haver A, Verstreken F, Rath SN, Kalaskar DM. Optimization of extrusion based ceramic 3D printing process for complex bony designs. Mater Des  2019; 162: 263-70.
 [http://dx.doi.org/10.1016/j.matdes.2018.11.054]

[60]
Ye X, Leeflang S, Wu C, Chang J, Zhou J, Huan Z. Mesoporous bioactive glass functionalized 3D Ti-6Al-4V scaffolds with improved surface bioactivity. Materials (Basel)  2017; 10(11): 1244.
 [http://dx.doi.org/10.3390/ma10111244] [PMID:  29077014]

[61]
Chai YC, Carlier A, Bolander J, et al. Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies. Acta Biomater  2012; 8(11): 3876-87.
 [http://dx.doi.org/10.1016/j.actbio.2012.07.002] [PMID:  22796326]

[62]
Shimauchi H, Nemoto E, Ishihata H, Shimomura M. Possible functional scaffolds for periodontal regeneration. Jpn Dent Sci Rev  2013; 49(4): 118-30.
 [http://dx.doi.org/10.1016/j.jdsr.2013.05.001]

[63]
Tada H, Nemoto E, Kanaya S, Hamaji N, Sato H, Shimauchi H. Elevated extracellular calcium increases expression of bone morphogenetic protein-2 gene via a calcium channel and ERK pathway in human dental pulp cells. Biochem Biophys Res Commun  2010; 394(4): 1093-7.
 [http://dx.doi.org/10.1016/j.bbrc.2010.03.135] [PMID:  20346918]

[64]
(a) Bouhadir KH, Lee KY, Alsberg E, Damm KL, Anderson KW, Mooney DJ. Degradation of partially oxidized alginate and its potential application for tissue engineering. Biotechnol Prog  2001; 17(5): 945-50.
 [http://dx.doi.org/10.1021/bp010070p] [PMID: 11587588]; 
(b) Shirafkan S, Gholamian M, Rohani A, Mahmoudinezhad SS, Razavi M, Moradi K. Complete Spontaneous Bone Regeneration following Surgical Enucleation of a Mandibular Cemento-Ossifying Fibroma. Case Rep Dent 2022. Aug 5; 2022.

[65]
Drury JL, Mooney DJ. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials  2003; 24(24): 4337-51.
 [http://dx.doi.org/10.1016/S0142-9612(03)00340-5] [PMID:  12922147]

[66]
Li L, Davidovich AE, Schloss JM, et al. Neural lineage differentiation of embryonic stem cells within alginate microbeads. Biomaterials  2011; 32(20): 4489-97.
 [http://dx.doi.org/10.1016/j.biomaterials.2011.03.019] [PMID:  21481927]

[67]
Liu J, Sato C, Cerletti M, Wagers A. Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol  2010; 92: 367-409.
 [http://dx.doi.org/10.1016/S0070-2153(10)92012-7] [PMID:  20816402]

[68]
Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M. Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science  2005; 308(5727): 1472-7.
 [http://dx.doi.org/10.1126/science.1107627] [PMID:  15933201]

[69]
Cantu DA, Hematti P, Kao WJ. Cell encapsulating biomaterial regulates mesenchymal stromal/stem cell differentiation and macrophage immunophenotype. Stem Cells Transl Med  2012; 1(10): 740-9.
 [http://dx.doi.org/10.5966/sctm.2012-0061] [PMID:  23197666]

[70]
Ansari S, Moshaverinia A, Han A, Pi SP, Abdelhamid AI, Zadeh HH. Biomaterials  2013; 34: 0191.

[71]
Moshaverinia A, Chen C, Akiyama K, et al. Encapsulated dental-derived mesenchymal stem cells in an injectable and biodegradable scaffold for applications in bone tissue engineering. J Biomed Mater Res A  2013; 101(11): 3285-94.
 [http://dx.doi.org/10.1002/jbm.a.34546] [PMID:  23983201]

[72]
Moshaverinia A, Chen C, Akiyama K, et al. Alginate hydrogel as a promising scaffold for dental-derived stem cells: An in vitro study. J Mater Sci Mater Med  2012; 23(12): 3041-51.
 [http://dx.doi.org/10.1007/s10856-012-4759-3] [PMID:  22945383]

[73]
Ansari S, Chen C, Xu X, et al. Muscle tissue engineering using gingival mesenchymal stem cells encapsulated in alginate hydrogels containing multiple growth factors. Ann Biomed Eng  2016; 44(6): 1908-20.
 [http://dx.doi.org/10.1007/s10439-016-1594-6] [PMID:  27009085]

[74]
Margolis RU, Margolis RK, Chang LB, Preti C. Glycosaminoglycans of brain during development. Biochemistry  1975; 14(1): 85-8.
 [http://dx.doi.org/10.1021/bi00672a014] [PMID:  122810]

[75]
Preston M, Sherman LS. Neural stem cell niches: critical roles for the hyaluronan-based extracellular matrix inneural stem cell proliferation and differentiation. Front Biosci (Schol Ed)  2012; 3: 1165.
 [PMID:  21622263]

[76]
Bandtlow CE, Zimmermann DR. Proteoglycans in the developing brain: New conceptual insights for old proteins. Physiol Rev  2000; 80(4): 1267-90.
 [http://dx.doi.org/10.1152/physrev.2000.80.4.1267] [PMID:  11015614]

[77]
Knudson CB. Hyaluronan and CD44: Strategic players for cell-matrix interactions during chondrogenesis and matrix assembly. Birth Defects Res C Embryo Today  2003; 69(2): 174-96.
 [http://dx.doi.org/10.1002/bdrc.10013] [PMID:  12955860]

[78]
Huang KH, Wang CY, Chen CY, Hsu TT, Lin CP. Incorporation of calcium sulfate dihydrate into a mesoporous calcium silicate/poly-ε-caprolactone scaffold to regulate the release of bone morphogenetic protein-2 and accelerate bone regeneration. Biomedicines  2021; 9(2): 128.
 [http://dx.doi.org/10.3390/biomedicines9020128] [PMID:  33572786]

[79]
Seol YJ, Kim KH, Kang YM, Kim IA, Rhee SH. Bioactivity, pre-osteoblastic cell responses, and osteoconductivity evaluations of the electrospun non-woven SiO 2 -CaO gel fabrics. J Biomed Mater Res B Appl Biomater  2009; 90B(2): 679-87.
 [http://dx.doi.org/10.1002/jbm.b.31334] [PMID:  19213049]

[80]
Münchow EA, Albuquerque MTP, Zero B, et al. Development and characterization of novel ZnO-loaded electrospun membranes for periodontal regeneration. Dent Mater  2015; 31(9): 1038-51.
 [http://dx.doi.org/10.1016/j.dental.2015.06.004] [PMID:  26116414]

[81]
Münchow EA, Pankajakshan D, Albuquerque MTP, et al. Synthesis and characterization of CaO-loaded electrospun matrices for bone tissue engineering. Clin Oral Investig  2016; 20(8): 1921-33.
 [http://dx.doi.org/10.1007/s00784-015-1671-5] [PMID:  26612403]

[82]
Yu CT, Wang FM, Liu YT, et al. Effect of bone morphogenic protein-2-loaded mesoporous strontium substitution calcium silicate/recycled fish gelatin 3D Cell-Laden scaffold for bone tissue engineering. Processes (Basel)  2020; 8(4): 493.
 [http://dx.doi.org/10.3390/pr8040493]

[83]
Lee SH, Lee KG, Hwang JH, et al. Evaluation of mechanical strength and bone regeneration ability of 3D printed kagome-structure scaffold using rabbit calvarial defect model. Mater Sci Eng C  2019; 98: 949-59.
 [http://dx.doi.org/10.1016/j.msec.2019.01.050] [PMID:  30813102]

[84]
Huang TH, Kao CT, Shen YF, et al. Substitutions of strontium in bioactive calcium silicate bone cements stimulate osteogenic differentiation in human mesenchymal stem cells. J Mater Sci Mater Med  2019; 30(6): 68.
 [http://dx.doi.org/10.1007/s10856-019-6274-2] [PMID:  31165270]

[85]
Zhang S, Dong Y, Chen M, et al. Recent developments in strontium-based biocomposites for bone regeneration. J Artif Organs  2020; 23(3): 191-202.
 [http://dx.doi.org/10.1007/s10047-020-01159-y] [PMID:  32100147]

[86]
Ni GX, Shu B, Huang G, Lu WW, Pan HB. The effect of strontium incorporation into hydroxyapatites on their physical and biological properties. J Biomed Mater Res B Appl Biomater  2012; 100B(2): 562-8.
 [http://dx.doi.org/10.1002/jbm.b.31986] [PMID:  22114002]

[87]
Pierantozzi D, Scalzone A, Jindal S, et al. 3D printed Sr-containing composite scaffolds: Effect of structural design and material formulation towards new strategies for bone tissue engineering. Compos Sci Technol  2020; 191: 108069.
 [http://dx.doi.org/10.1016/j.compscitech.2020.108069]

[88]
Panzavolta S, Torricelli P, Casolari S, Parrilli A, Fini M, Bigi A. Strontium‐substituted hydroxyapatite‐gelatin biomimetic scaffolds modulate bone cell response. Macromol Biosci  2018; 18(7): 1800096.
 [http://dx.doi.org/10.1002/mabi.201800096] [PMID:  29877029]

[89]
Saidak Z, Marie PJ. Strontium signaling: Molecular mechanisms and therapeutic implications in osteoporosis. Pharmacol Ther  2012; 136(2): 216-26.
 [http://dx.doi.org/10.1016/j.pharmthera.2012.07.009] [PMID:  22820094]

[90]
Zhang W, Shen Y, Pan H, et al. Effects of strontium in modified biomaterials. Acta Biomater  2011; 7(2): 800-8.
 [http://dx.doi.org/10.1016/j.actbio.2010.08.031] [PMID:  20826233]

[91]
Liu D, Nie W, Li D, et al. 3D printed PCL/SrHA scaffold for enhanced bone regeneration. Chem Eng J  2019; 362: 269-79.
 [http://dx.doi.org/10.1016/j.cej.2019.01.015]

[92]
Lin YH, Chiu YC, Shen YF, Wu YHA, Shie MY. Bioactive calcium silicate/poly-ε-caprolactone composite scaffolds 3D printed under mild conditions for bone tissue engineering. J Mater Sci Mater Med  2018; 29(1): 11.
 [http://dx.doi.org/10.1007/s10856-017-6020-6] [PMID:  29282550]

[93]
Vijaykumar A, Dyrkacz P, Vidovic-Zdrilic I, Maye P, Mina M. Expression of BSP-GFPtpz transgene during osteogenesis and reparative dentinogenesis. J Dent Res  2020; 99(1): 89-97.
 [http://dx.doi.org/10.1177/0022034519885089] [PMID:  31682548]

[94]
He F, Lu T, Fang X, et al. Effects of strontium amount on the mechanical strength and cell-biological performance of magnesium-strontium phosphate bioceramics for bone regeneration. Mater Sci Eng C  2020; 112: 110892.
 [http://dx.doi.org/10.1016/j.msec.2020.110892] [PMID:  32409050]

[95]
Daghrery A, Ferreira JA, de Souza Araújo IJ, et al. A highly ordered, nanostructured fluorinated CaP‐Coated melt electrowritten scaffold for periodontal tissue regeneration. Adv Healthc Mater  2021; 10(21): 2101152.
 [http://dx.doi.org/10.1002/adhm.202101152] [PMID:  34342173]

[96]
Abbasi N, Abdal-hay A, Hamlet S, Graham E, Ivanovski S. Effects of gradient and offset architectures on the mechanical and biological properties of 3-D melt electrowritten (MEW) scaffolds. ACS Biomater Sci Eng  2019; 5(7): 3448-61.
 [http://dx.doi.org/10.1021/acsbiomaterials.8b01456] [PMID:  33405729]

[97]
Vaquette C, Ivanovski S, Hamlet SM, Hutmacher DW. Effect of culture conditions and calcium phosphate coating on ectopic bone formation. Biomaterials  2013; 34(22): 5538-51.
 [http://dx.doi.org/10.1016/j.biomaterials.2013.03.088] [PMID:  23623428]

[98]
Ge X, Leng Y, Bao C, Xu SL, Wang R, Ren F. Antibacterial coatings of fluoridated hydroxyapatite for percutaneous implants. J Biomed Mater Res A  2010; 95A(2): 588-99.
 [http://dx.doi.org/10.1002/jbm.a.32862] [PMID:  20725973]

[99]
Bozza A, Coates EE, Incitti T, et al. Neural differentiation of pluripotent cells in 3D alginate-based cultures. Biomaterials  2014; 35(16): 4636-45.
 [http://dx.doi.org/10.1016/j.biomaterials.2014.02.039] [PMID:  24631250]

[100]
Nandakumar A, Yang L, Habibovic P, van Blitterswijk C. Calcium phosphate coated electrospun fiber matrices as scaffolds for bone tissue engineering. Langmuir  2010; 26(10): 7380-7.
 [http://dx.doi.org/10.1021/la904406b] [PMID:  20039599]

[101]
Sundararaj SC, Thomas MV, Peyyala R, Dziubla TD, Puleo DA. Design of a multiple drug delivery system directed at periodontitis. Biomaterials  2013; 34(34): 8835-42.
 [http://dx.doi.org/10.1016/j.biomaterials.2013.07.093] [PMID:  23948165]

[102]
Brager U, Mühle T, Fourmousis L, Lang NP, Mombelli A. Effect of the NSAID flurbiprofen on remodelling after periodontal surgery. J Periodontal Res  1997; 32(7): 575-82.
 [http://dx.doi.org/10.1111/j.1600-0765.1997.tb00934.x] [PMID:  9401929]

[103]
Hortensius RA, Harley BAC. Naturally derived biomaterials for addressing inflammation in tissue regeneration. Exp Biol Med (Maywood)  2016; 241(10): 1015-24.
 [http://dx.doi.org/10.1177/1535370216648022] [PMID:  27190254]

[104]
Noguchi K, Ishikawa I. The roles of cyclooxygenase-2 and prostaglandin E 2 in periodontal disease. Periodontol 2000  2007; 43(1): 85-101.
 [http://dx.doi.org/10.1111/j.1600-0757.2006.00170.x] [PMID:  17214837]

[105]
Yar M, Farooq A, Shahzadi L, et al. Novel meloxicam releasing electrospun polymer/ceramic reinforced biodegradable membranes for periodontal regeneration applications. Mater Sci Eng C  2016; 64: 148-56.
 [http://dx.doi.org/10.1016/j.msec.2016.03.072] [PMID:  27127039]

[106]
Van Dyke TE, Hasturk H, Kantarci A, et al. Proresolving nanomedicines activate bone regeneration in periodontitis. J Dent Res  2015; 94(1): 148-56.
 [http://dx.doi.org/10.1177/0022034514557331] [PMID:  25389003]

[107]
Zupancic S, Kocbek P, Baumgartner S, Kristl J. Contribution of nanotechnology to improved treatment of periodontal disease. Curr Pharm Des  2015; 21(22): 3257-71.
 [http://dx.doi.org/10.2174/1381612821666150531171829] [PMID:  26027560]

[108]
Cantón I, Mckean R, Charnley M, et al. Development of an Ibuprofen-releasing biodegradable PLA/PGA electrospun scaffold for tissue regeneration. Biotechnol Bioeng  2010; 105(2): 396-408.
 [http://dx.doi.org/10.1002/bit.22530] [PMID:  19731254]

[109]
Kasaj A, Reichert C, Götz H, Röhrig B, Smeets R, Willershausen B. In vitro evaluation of various bioabsorbable and nonresorbable barrier membranes for guided tissue regeneration. Head Face Med  2008; 4(1): 22.
 [http://dx.doi.org/10.1186/1746-160X-4-22] [PMID:  18854011]

[110]
Larjava H, Koivisto L, Häkkinen L, Heino J. Epithelial integrins with special reference to oral epithelia. J Dent Res  2011; 90(12): 1367-76.
 [http://dx.doi.org/10.1177/0022034511402207] [PMID:  21441220]

[111]
Gräber HG, Conrads G, Wilharm J, Lampert F. Role of interactions between integrins and extracellular matrix components in healthy epithelial tissue and establishment of a long junctional epithelium during periodontal wound healing: a review. J Periodontol  1999; 70(12): 1511-22.
 [http://dx.doi.org/10.1902/jop.1999.70.12.1511] [PMID:  10632527]

[112]
Preeja C, Janam P, Nayar BR. Fibrin clot adhesion to root surface treated with tetracycline hydrochloride and ethylenediaminetetraacetic acid: A scanning electron microscopic study. Dent Res J (Isfahan)  2013; 10(3): 382-8.
 [PMID:  24019809]

[113]
Fairweather M, Heit YI, Buie J, et al. Celecoxib inhibits early cutaneous wound healing. J Surg Res  2015; 194(2): 717-24.
 [http://dx.doi.org/10.1016/j.jss.2014.12.026] [PMID:  25588948]

[114]
Zhang W, Ullah I, Shi L, et al. Fabrication and characterization of porous polycaprolactone scaffold via extrusion-based cryogenic 3D printing for tissue engineering. Mater Des  2019; 180: 107946.
 [http://dx.doi.org/10.1016/j.matdes.2019.107946]

[115]
Salgado AJ, Coutinho OP, Reis RL. Bone tissue engineering: state of the art and future trends. Macromol Biosci  2004; 4(8): 743-65.
 [http://dx.doi.org/10.1002/mabi.200400026] [PMID:  15468269]

[116]
Velasco MA, Narváez-Tovar CA, Garzón-Alvarado DA. Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering. BioMed Res Int  2015; 2015: 1-21.
 [http://dx.doi.org/10.1155/2015/729076] [PMID:  25883972]

[117]
Bose S, Roy M, Bandyopadhyay A. Recent advances in bone tissue engineering scaffolds. Trends Biotechnol  2012; 30(10): 546-54.
 [http://dx.doi.org/10.1016/j.tibtech.2012.07.005] [PMID:  22939815]

[118]
Burg KJL, Porter S, Kellam JF. Biomaterial developments for bone tissue engineering. Biomaterials  2000; 21(23): 2347-59.
 [http://dx.doi.org/10.1016/S0142-9612(00)00102-2] [PMID:  11055282]

[119]
Wei G, Ma PX. Structure and properties of nano-hydroxyapatite/polymer composite scaffolds for bone tissue engineering. Biomaterials  2004; 25(19): 4749-57.
 [http://dx.doi.org/10.1016/j.biomaterials.2003.12.005] [PMID:  15120521]

[120]
Abbasi N, Ivanovski S, Gulati K, Love RM, Hamlet S. Role of offset and gradient architectures of 3-D melt electrowritten scaffold on differentiation and mineralization of osteoblasts. Biomater Res  2020; 24(1): 2.
 [http://dx.doi.org/10.1186/s40824-019-0180-z] [PMID:  31911842]

[121]
Xie C, Gao Q, Wang P, et al. Structure-induced cell growth by 3D printing of heterogeneous scaffolds with ultrafine fibers. Mater Des  2019; 181: 108092.
 [http://dx.doi.org/10.1016/j.matdes.2019.108092]

[122]
Fuchs A, Youssef A, Seher A, et al. Medical-grade polycaprolactone scaffolds made by melt electrospinning writing for oral bone regeneration-a pilot study in vitro. BMC Oral Health  2019; 19(1): 28.
 [http://dx.doi.org/10.1186/s12903-019-0717-5] [PMID:  30709394]

[123]
Fuchs A, Youssef A, Seher A, et al. A new multilayered membrane for tissue engineering of oral hard- and soft tissue by means of melt electrospinning writing and film casting – An in vitro study. J Craniomaxillofac Surg  2019; 47(4): 695-703.
 [http://dx.doi.org/10.1016/j.jcms.2019.01.043] [PMID:  30826113]

[124]
Babaie E, Bhaduri SB. Fabrication aspects of porous biomaterials in orthopedic applications: A review. ACS Biomater Sci Eng  2018; 4(1): 1-39.
 [http://dx.doi.org/10.1021/acsbiomaterials.7b00615] [PMID:  33418675]

[125]
Porta M, Tonda-Turo C, Pierantozzi D, Ciardelli G, Mancuso E. Towards 3D multi-layer scaffolds for periodontal tissue engineering applications: Addressing manufacturing and architectural challenges. Polymers (Basel)  2020; 12(10): 2233.
 [http://dx.doi.org/10.3390/polym12102233] [PMID:  32998365]

[126]
Meifeng Zhu M, Li W, Dong X, et al. In vivo engineered extracellular matrix scaffolds with instructive niches for oriented tissue regeneration. Nat Commun  2019; 10(1): 1-14.
 [PMID:  30602773]

[127]
Yamada S, Murakami S, Matoba R, et al. Expression profile of active genes in human periodontal ligament and isolation of PLAP-1, a novel SLRP family gene. Gene  2001; 275(2): 279-86.
 [http://dx.doi.org/10.1016/S0378-1119(01)00683-7] [PMID:  11587855]

[128]
Yamada S, Tomoeda M, Ozawa Y, et al. PLAP-1/asporin, a novel negative regulator of periodontal ligament mineralization. J Biol Chem  2007; 282(32): 23070-80.
 [http://dx.doi.org/10.1074/jbc.M611181200] [PMID:  17522060]

[129]
Ueda M, Goto T, Kuroishi KN, et al. Asporin in compressed periodontal ligament cells inhibits bone formation. Arch Oral Biol  2016; 62: 86-92.
 [http://dx.doi.org/10.1016/j.archoralbio.2015.11.010] [PMID:  26655952]

[130]
Horiuchi K, Amizuka N, Takeshita S, et al. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor β. J Bone Miner Res  1999; 14(7): 1239-49.
 [http://dx.doi.org/10.1359/jbmr.1999.14.7.1239] [PMID:  10404027]

[131]
Kii I, Ito H. Periostin and its interacting proteins in the construction of extracellular architectures. Cell Mol Life Sci  2017; 74(23): 4269-77.
 [http://dx.doi.org/10.1007/s00018-017-2644-4] [PMID:  28887577]

[132]
Rios H, Koushik SV, Wang H, et al. periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol  2005; 25(24): 11131-44.
 [http://dx.doi.org/10.1128/MCB.25.24.11131-11144.2005] [PMID:  16314533]

[133]
Ríos HF, Ma D, Xie Y, et al. Periostin is essential for the integrity and function of the periodontal ligament during occlusal loading in mice. J Periodontol  2008; 79(8): 1480-90.
 [http://dx.doi.org/10.1902/jop.2008.070624] [PMID:  18672999]

[134]
Osorio R, Alfonso-Rodríguez CA, Osorio E, et al. Novel potential scaffold for periodontal tissue engineering. Clin Oral Investig  2017; 21(9): 2695-707.
 [http://dx.doi.org/10.1007/s00784-017-2072-8] [PMID:  28214952]

[135]
Sukpaita T, Chirachanchai S, Suwattanachai P, Everts V, Pimkhaokham A, Ampornaramveth RS. In vivo bone regeneration induced by a scaffold of chitosan/dicarboxylic acid seeded with human periodontal ligament cells. Int J Mol Sci  2019; 20(19): 4883.
 [http://dx.doi.org/10.3390/ijms20194883] [PMID:  31581495]

[136]
Basu A, Rothermund K, Ahmed MN, Syed-Picard FN. Self-assembly of an organized cementum-periodontal ligament-like complex using scaffold-free tissue engineering. Front Physiol  2019; 10: 422.
 [http://dx.doi.org/10.3389/fphys.2019.00422] [PMID:  31031642]

[137]
Batool F, Morand DN, Thomas L, et al. Synthesis of a novel electrospun polycaprolactone scaffold functionalized with ibuprofen for periodontal regeneration: An in vitro and in vivo study. Materials (Basel)  2018; 11(4): 580.
 [http://dx.doi.org/10.3390/ma11040580] [PMID:  29642582]

[138]
Ansari S, Diniz IM, Chen C, et al. Human periodontal ligament‐and gingiva‐derived mesenchymal stem cells promote nerve regeneration when encapsulated in alginate/hyaluronic acid 3D scaffold. Adv Healthc Mater  2017; 6(24): 1700670.
 [http://dx.doi.org/10.1002/adhm.201700670] [PMID:  29076281]
Rights & Permissions Print Cite
Article Metrics
34
2
Journal Information
For Authors
For Editors
For Reviewers
Explore Articles
Open Access
Open Access Articles
For Visitors
DOI https://dx.doi.org/10.2174/1574888X18666221227142055	Print ISSN 1574-888X
Publisher Name Bentham Science Publisher	Online ISSN 2212-3946
Current Stem Cell Research & Therapy

Bone Scaffold Materials in Periodontal and Tooth-supporting Tissue Regeneration: A Review

Abstract

Graphical Abstract

Related Journals

Related Books

Related Articles
