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


Cite item

Full Text

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.

Conclusions: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.

About the authors

Mahmood Jahangirnezhad

Department of Periodontics, School of Dentistry, Ahvaz Jundishapur University of Medical Sciences

Email: info@benthamscience.net

Sadaf Mahmoudinezhad

Department of Periodontics, School of Dentistry, Ahvaz Jundishapur University of Medical Sciences

Email: info@benthamscience.net

Melika Moradi

Department of Periodontics, School of Dentistry, Ahvaz Jundishapur University of Medical Sciences

Email: info@benthamscience.net

Kooshan Moradi

Department of Periodontics, School of Dentistry, Ahvaz Jundishapur University of Medical Sciences

Email: info@benthamscience.net

Ali Rohani

Department of Periodontics, School of Dentistry, Ahvaz Jundishapur University of Medical Sciences

Email: info@benthamscience.net

Lobat Tayebi

School of Dentistry, Marquette University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Peres MA, Macpherson LMD, Weyant RJ, et al. Oral diseases: a global public health challenge. Lancet 2019; 394(10194): 249-60. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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: doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1002/adhm.201700670 PMID: 29076281

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Bentham Science Publishers