DOI QR코드

DOI QR Code

Advances in the design of macroporous polymer scaffolds for potential applications in dentistry

  • Bencherif, Sidi A. (School of Engineering and Applied Sciences, Harvard University) ;
  • Braschler, Thomas M. (School of Engineering and Applied Sciences, Harvard University) ;
  • Renaud, Philippe (Laboratory of Microsystems, STI-LMIS4, Ecole Polytechnique Federale de Lausanne (EPFL))
  • Received : 2013.12.01
  • Accepted : 2013.12.22
  • Published : 2013.12.31

Abstract

A paradigm shift is taking place in medicine and dentistry from using synthetic implants and tissue grafts to a tissue engineering approach that uses degradable porous three-dimensional (3D) material hydrogels integrated with cells and bioactive factors to regenerate tissues such as dental bone and other oral tissues. Hydrogels have been established as a biomaterial of choice for many years, as they offer diverse properties that make them ideal in regenerative medicine, including dental applications. Being highly biocompatible and similar to native extracellular matrix, hydrogels have emerged as ideal candidates in the design of 3D scaffolds for tissue regeneration and drug delivery applications. However, precise control over hydrogel properties, such as porosity, pore size, and pore interconnectivity, remains a challenge. Traditional techniques for creating conventional crosslinked polymers have demonstrated limited success in the formation of hydrogels with large pore size, thus limiting cellular infiltration, tissue ingrowth, vascularization, and matrix mineralization (in the case of bone) of tissue-engineered constructs. Emerging technologies have demonstrated the ability to control microarchitectural features in hydrogels such as the creation of large pore size, porosity, and pore interconnectivity, thus allowing the creation of engineered hydrogel scaffolds with a structure and function closely mimicking native tissues. In this review, we explore the various technologies available for the preparation of macroporous scaffolds and their potential applications.

Keywords

References

  1. Peppas NA, Hilt JZ, Khademhosseini A, Langer R. Hydrogels in biology and medicine: from molecular principles to bionanotechnology. Adv Mater 2006;181345-60.
  2. Annabi N, Nichol JW, Zhong X, Ji C, Koshy S, Khademhosseini A, et al. Controlling the porosity and microarchitecture of hydrogels for tissue engineering. Tissue Eng Part B Rev 2010;16:371-83. https://doi.org/10.1089/ten.teb.2009.0639
  3. Park S, Kim G, Jeon YC, Koh Y, Kim W. 3D polycaprolactone scaffolds with controlled pore structure using a rapid prototyping system. J Mater Sci Mater Med 2009;20:229-34.
  4. Kennedy S, Bencherif S, Norton D, Weinstock L, Mehta M, Mooney D. Rapid and extensive collapse from electrically responsive macroporous hydrogels. Adv Healthc Mater 2013 Sep 12 [Epub]. http:dx.doi.org/10.1002/adhm.201300260.
  5. Bencherif SA, Sands RW, Bhatta D, Arany P, Verbeke CS, Edwards DA, et al. Injectable preformed scaffolds with shape-memory properties. Proc Natl Acad Sci U S A 2012;109:19590-5. https://doi.org/10.1073/pnas.1211516109
  6. Bencherif SA, Guillemot F, Huebsch N, Edwards DA, Mooney DJ. Cell-traction mediated configuration of the cell/extracellular-matrix interface plays a key role in stem cell fate. Med Sci (Paris) 2011;27:19-21. https://doi.org/10.1051/medsci/201127119
  7. Yoon JA, Bencherif SA, Aksak B, Kim EK, Kowalewski T, Oh JK, et al. Thermoresponsive hydrogel scaffolds with tailored hydrophilic pores. Chem Asian J 2011;6:128-36. https://doi.org/10.1002/asia.201000514
  8. Cho HY, Gao H, Srinivasan A, Hong J, Bencherif SA, Siegwart DJ, et al. Rapid cellular internalization of multifunctional star polymers prepared by atom transfer radical polymerization. Biomacromolecules 2010;11:2199-203. https://doi.org/10.1021/bm1006272
  9. Sun LT, Bencherif SA, Gilbert TW, Lotze MT, Washburn NR. Design principles for cytokine-neutralizing gels: Cross-linking effects. Acta Biomater 2010;6:4708-15. https://doi.org/10.1016/j.actbio.2010.06.029
  10. Huebsch N, Arany PR, Mao AS, Shvartsman D, Ali OA, Bencherif SA, et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 2010;9:518-26. https://doi.org/10.1038/nmat2732
  11. Bencherif SA, Washburn NR, Matyjaszewski K. Synthesis by AGET ATRP of degradable nanogel precursors for in situ formation of nanostructured hyaluronic acid hydrogel. Biomacromolecules 2009;10:2499-507. https://doi.org/10.1021/bm9004639
  12. Bencherif SA, Siegwart DJ, Srinivasan A, Horkay F, Hollinger JO, Washburn NR, et al. Nanostructured hybrid hydrogels prepared by a combination of atom transfer radical polymerization and free radical polymerization. Biomaterials 2009;30:5270-8. https://doi.org/10.1016/j.biomaterials.2009.06.011
  13. Bencherif SA, Gao H, Srinivasan A, Siegwart DJ, Hollinger JO, Washburn NR, et al. Cell-adhesive star polymers prepared by ATRP. Biomacromolecules 2009;10:1795-803. https://doi.org/10.1021/bm900213u
  14. Bencherif SA, Srinivasan A, Sheehan JA, Walker LM, Gayathri C, Gil R, et al. End-group effects on the properties of PEG-co-PGA hydrogels. Acta Biomater 2009;5:1872-83. https://doi.org/10.1016/j.actbio.2009.02.030
  15. Bencherif SA, Sheehan JA, Hollinger JO, Walker LM, Matyjaszewski K, Washburn NR. Influence of cross-linker chemistry on release kinetics of PEG-co-PGA hydrogels. J Biomed Mater Res A 2009;90:142-53.
  16. Bencherif SA, Srinivasan A, Horkay F, Hollinger JO, Matyjaszewski K, Washburn NR. Influence of the degree of methacrylation on hyaluronic acid hydrogels properties. Biomaterials 2008;29:1739-49. https://doi.org/10.1016/j.biomaterials.2007.11.047
  17. Lin-Gibson S, Bencherif S, Antonucci JM, Jones RL, Horkay F. Synthesis and characterization of poly(ethylene glycol) dimethacrylate hydrogels. Macromol Symp 2005;227:243-54. https://doi.org/10.1002/masy.200550924
  18. Lin-Gibson S, Bencherif S, Cooper JA, Wetzel SJ, Antonucci JM, Vogel BM, et al. Synthesis and characterization of PEG dimethacrylates and their hydrogels. Biomacromolecules 2004;5:1280-7. https://doi.org/10.1021/bm0498777
  19. Siegwart DJ, Srinivasan A, Bencherif SA, Karunanidhi A, Oh JK, Vaidya S, et al. Cellular uptake of functional nanogels prepared by inverse miniemulsion ATRP with encapsulated proteins, carbohydrates, and gold nanoparticles. Biomacromolecules 2009;10:2300-9. https://doi.org/10.1021/bm9004904
  20. Siegwart DJ, Bencherif SA, Srinivasan A, Hollinger JO, Matyjaszewski K. Synthesis, characterization, and in vitro cell culture viability of degradable poly(N-isopropylacrylamide-co-5,6-benzo-2-methylene-1,3-dioxepane)-based polymers and crosslinked gels. J Biomed Mater Res A 2008;87:345-58.
  21. Ekaputra AK, Prestwich GD, Cool SM, Hutmacher DW. The three-dimensional vascularization of growth factor-releasing hybrid scaffold of poly (epsilon-caprolactone)/collagen fibers and hyaluronic acid hydrogel. Biomaterials 2011;32:8108-17. https://doi.org/10.1016/j.biomaterials.2011.07.022
  22. Novosel EC, Kleinhans C, Kluger PJ. Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 2011;63:300-11. https://doi.org/10.1016/j.addr.2011.03.004
  23. Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, Ferrara N, et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A 2002;99:9656-61. https://doi.org/10.1073/pnas.152324099
  24. Taboas JM, Maddox RD, Krebsbach PH, Hollister SJ. Indirect solid free form fabrication of local and global porous, biomimetic and composite 3D polymer-ceramic scaffolds. Biomaterials 2003;24:181-94. https://doi.org/10.1016/S0142-9612(02)00276-4
  25. O'Brien FJ, Harley BA, Waller MA, Yannas IV, Gibson LJ, Prendergast PJ. The effect of pore size on permeability and cell attachment in collagen scaffolds for tissue engineering. Technol Health Care 2007;15:3-17.
  26. Murphy CM, O'Brien FJ. Understanding the effect of mean pore size on cell activity in collagen-glycosaminoglycan scaffolds. Cell Adh Migr 2010;4:377-81. https://doi.org/10.4161/cam.4.3.11747
  27. Murphy CM, O'Brien FJ, Little DG, Schindeler A. Cell-scaffold interactions in the bone tissue engineering triad. Eur Cell Mater 2013;26:120-32. https://doi.org/10.22203/eCM.v026a09
  28. Chen GP, Ushida T, Tateishi T. Scaffold design for tissue engineering. Macromol Biosci 2002;2:67-77. https://doi.org/10.1002/1616-5195(20020201)2:2<67::AID-MABI67>3.0.CO;2-F
  29. Battistella E, Varoni E, Cochis A, Palazzo B, Rimondini L. Degradable polymers may improve dental practice. J Appl Biomater Biomech 2011;9:223-31.
  30. Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 2005;26:5474-91. https://doi.org/10.1016/j.biomaterials.2005.02.002
  31. Chirila TV, Constable IJ, Crawford GJ, Vijayasekaran S, Thompson DE, Chen YC, et al. Poly(2-hydroxyethyl methacrylate) sponges as implant materials: in vivo and in vitro evaluation of cellular invasion. Biomaterials 1993;14:26-38. https://doi.org/10.1016/0142-9612(93)90072-A
  32. Gavrilas C, Han W, Li G, Omidian H, Rocca JG, inventors; Abbott Laboratories, assignee. Very-pure superporous hydrogels having outstanding swelling propertles. United States patent WO/2009/029087. 2009 March 5.
  33. Huang X, Zhang Y, Donahue HJ, Lowe TL. Porous thermoresponsive-co-biodegradable hydrogels as tissue-engineering scaffolds for 3-dimensional in vitro culture of chondrocytes. Tissue Eng 2007;13:2645-52. https://doi.org/10.1089/ten.2007.0084
  34. Wei G, Ma PX. Partially nanofibrous architecture of 3D tissue engineering scaffolds. Biomaterials 2009;30:6426-34. https://doi.org/10.1016/j.biomaterials.2009.08.012
  35. Xu F, Sridharan B, Durmus NG, Wang S, Yavuz AS, Gurkan UA, et al. Living bacterial sacrificial porogens to engineer decellularized porous scaffolds. PLoS One 2011;6:e19344. https://doi.org/10.1371/journal.pone.0019344
  36. Stachowiak AN, Bershteyn A, Tzatzalos E, Irvine DJ. Bioactive hydrogels with an ordered cellular structure combine interconnected macroporosity and robust mechanical properties. Adv Mater 2005;17:399-403. https://doi.org/10.1002/adma.200400507
  37. Draghi L, Resta S, Pirozzolo MG, Tanzi MC. Microspheres leaching for scaffold porosity control. Mater Sci Mater Med 2005;16:1093-7. https://doi.org/10.1007/s10856-005-4711-x
  38. Davis HE, Leach JK. Hybrid and composite biomaterials for tissue engineering. In: Ashammakhi N, editor. Topics in multifunctional biomaterials and devices e-book. Davis (CA): Biomedical Engineering UC Davis; 2008. p. 1-26.
  39. Capes JS, Ando HY, Cameron RE. Fabrication of polymeric scaffolds with a controlled distribution of pores. J Mater Sci Mater Med 2005;16:1069-75. https://doi.org/10.1007/s10856-005-4708-5
  40. Tran RT, Naseri E, Kolasnikov A, Bai X, Yang J. A new generation of sodium chloride porogen for tissue engineering. Biotechnol Appl Biochem 2011;58:335-44. https://doi.org/10.1002/bab.44
  41. Qu T, Liu X. Nano-structured gelatin/bioactive glass hybrid scaffolds for the enhancement of odontogenic differentiation of human dental pulp stem cells. J Mater Chem B Mater Biol Med 2013;1:4764-72. https://doi.org/10.1039/c3tb21002b
  42. Sultana N, Wang M. Fabrication of HA/PHBV composite scaffolds through the emulsion freezing/freeze-drying process and characterisation of the scaffolds. J Mater Sci Mater Med 2008;19:2555-61. https://doi.org/10.1007/s10856-007-3214-3
  43. Sultana N, Wang M. PHBV/PLLA-based composite scaffolds containing nano-sized hydroxyapatite particles for bone tissue engineering. J Exp Nanosci 2008;3:121-32. https://doi.org/10.1080/17458080701867429
  44. Thomson RC, Yaszemski MJ, Mikos AG. Polymer scaffold processing. In: Lanza RP, Langer R, Chick WL, editors. Principles of tissue engineering. Austin (TX): Academic Press; 1997. p. 263-72
  45. Hu Y, Grainger DW, Winn SR, Hollinger JO. Fabrication of poly(alpha-hydroxy acid) foam scaffolds using multiple solvent systems. J Biomed Mater Res 2002;59:563-72. https://doi.org/10.1002/jbm.1269
  46. Pandit N, Malik R, Philips D. Tissue engineering: a new vista in periodontal regeneration. J Indian Soc Periodontol 2011;15:328-37. https://doi.org/10.4103/0972-124X.92564
  47. Wang Y, Zhao Q, Hu Y, Sun L, Bai L, Jiang T, et al. Ordered nanoporous silica as carriers for improved delivery of water insoluble drugs: a comparative study between three dimensional and two dimensional macroporous silica. Int J Nanomedicine 2013;8:4015-31.
  48. Lytle JC, Stein A. Recent progress in syntheses and applications of inverse opals and related macroporous materials prepared by colloidal crystal templating. In: Cao G, Brinker CJ, editors. Annual reviews of nano research. New Jersey: World Scientific Publishing Co.: 2006. p. 1-79.
  49. Zhang K, Yan H, Bell DC, Stein A, Francis LF. Effects of materials parameters on mineralization and degradation of sol-gel bioactive glasses with 3D-ordered macroporous structures. J Biomed Mater Res A 2003;66:860-9.
  50. Zhang K, Simon CG Jr, Washburn NR, Antonucci JM, Lin-Gibson S. In situ formation of blends by photopolymerization of poly(ethylene glycol) dimethacrylate and polylactide. Biomacromolecules 2005;6:1615-22. https://doi.org/10.1021/bm0500648
  51. Zhang K, Washburn NR, Simon CG Jr. Cytotoxicity of three-dimensionally ordered macroporous sol-gel bioactive glass (3DOM-BG). Biomaterials 2005;26:4532-9. https://doi.org/10.1016/j.biomaterials.2004.11.030
  52. Henderson TM, Ladewig K, Haylock DN, McLean KM, O'Connor AJ. Cryogels for biomedical applications. J Mater Chem B 2013;1:2682-95. https://doi.org/10.1039/c3tb20280a
  53. Plieva FM, Karlsson M, Aguilar MR, Gomez D, Mikhalovsky S, Galaev IY. Pore structure in supermacroporous polyacrylamide based cryogels. Soft Matter 2005;1:303-9. https://doi.org/10.1039/b510010k
  54. Lozinsky VI, Plieva FM, Galaev IY, Mattiasson B. The potential of polymeric cryogels in bioseparation. Bioseparation 2001;10:163-88. https://doi.org/10.1023/A:1016386902611
  55. Plieva FM, Galaev IY, Mattiasson B. Macroporous gels prepared at subzero temperatures as novel materials for chromatography of particulate-containing fluids and cell culture applications. J Sep Sci 2007;30:1657-71. https://doi.org/10.1002/jssc.200700127
  56. Dainiak MB, Galaev IY, Kumar A, Plieva FM, Mattiasson B. Chromatography of living cells using supermacroporous hydrogels, cryogels. In: Kumar A, Galaev IY, Mattiasson B, editors. Cell separation: fundamentals, analytical and preparative methods. Berlin: Springer; 2007. p. 101-27
  57. Hwang Y, Sangaj N, Varghese S. Interconnected macroporous poly(ethylene glycol) cryogels as a cell scaffold for cartilage tissue engineering. Tissue Eng Part A 2010;16:3033-41. https://doi.org/10.1089/ten.tea.2010.0045
  58. Singh D, Tripathi A, Nayak V, Kumar A. Proliferation of chondrocytes on a 3-d modelled macroporous poly(hydroxyethyl methacrylate)-gelatin cryogel. J Biomater Sci Polym Ed 2011;22:1733-51. https://doi.org/10.1163/092050610X522486
  59. Mishra R, Goel SK, Gupta KC, Kumar A. Biocomposite cryogels as tissue engineered biomaterials for regeneration of critical-sized cranial bone defects. Tissue Eng Part A 2013 Dec 11 [Epub]. http://dx.doi.org/ 10.1089/ten.tea.2013.0072.
  60. Pham QP, Sharma U, Mikos AG. Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng 2006;12:1197-211. https://doi.org/10.1089/ten.2006.12.1197
  61. Brown AN, Kim BS, Alsberg E, Mooney DJ. Combining chondrocytes and smooth muscle cells to engineer hybrid soft tissue constructs. Tissue Eng 2000;6:297-305. https://doi.org/10.1089/107632700418029
  62. Takei T, Sakai S, Ijima H, Kawakami K. Development of mammalian cell-enclosing calcium-alginate hydrogel fibers in a co-flowing stream. Biotechnol J 2006;1:1014-7. https://doi.org/10.1002/biot.200600055
  63. Tuzlakoglu K, Alves CM, Mano JF, Reis RL. Production and characterization of chitosan fibers and 3-D fiber mesh scaffolds for tissue engineering applications. Macromol Biosci 2004;4:811-9. https://doi.org/10.1002/mabi.200300100
  64. Vasilev MP, Volf LA, Kotetskin VV, Pukhova ZI, Meos AI. The spinning of collagen fibres. Fibre Chem 1972;4:48-50. https://doi.org/10.1007/BF00548430
  65. Lovett ML, Cannizzaro CM, Vunjak-Novakovic G, Kaplan DL. Gel spinning of silk tubes for tissue engineering. Biomaterials 2008;29:4650-7. https://doi.org/10.1016/j.biomaterials.2008.08.025
  66. Li D, Xia Y. Electrospinning of nanofibers: reinventing the wheel? Adv Mater 2004;16:1151-70. https://doi.org/10.1002/adma.200400719
  67. Zhong S, Zhang Y, Lim CT. Fabrication of large pores in electrospun nanofibrous scaffolds for cellular infiltration: a review. Tissue Eng Part B Rev 2012;18:77-87. https://doi.org/10.1089/ten.teb.2011.0390
  68. Barnes CP, Sell SA, Boland ED, Simpson DG, Bowlin GL. Nanofiber technology: designing the next generation of tissue engineering scaffolds. Adv Drug Deliv Rev 2007;59:1413-33. https://doi.org/10.1016/j.addr.2007.04.022
  69. Sequeira SJ, Soscia DA, Oztan B, Mosier AP, Jean-Gilles R, Gadre A, et al. The regulation of focal adhesion complex formation and salivary gland epithelial cell organization by nanofibrous PLGA scaffolds. Biomaterials 2012;33:3175-86. https://doi.org/10.1016/j.biomaterials.2012.01.010
  70. Parrag IC, Zandstra PW, Woodhouse KA. Fiber alignment and coculture with fibroblasts improves the differentiated phenotype of murine embryonic stem cell-derived cardiomyocytes for cardiac tissue engineering. Biotechnol Bioeng 2012;109:813-22. https://doi.org/10.1002/bit.23353
  71. Shabani I, Haddadi-Asl V, Seyedjafari E, Soleimani M. Cellular infiltration on nanofibrous scaffolds using a modified electrospinning technique. Biochem Biophys Res Commun 2012;423:50-4. https://doi.org/10.1016/j.bbrc.2012.05.069
  72. Li L, Qian Y, Jiang C, Lv Y, Liu W, Zhong L, et al. The use of hyaluronan to regulate protein adsorption and cell infiltration in nanofibrous scaffolds. Biomaterials 2012;33:3428-45. https://doi.org/10.1016/j.biomaterials.2012.01.038
  73. Baker BM, Gee AO, Metter RB, Nathan AS, Marklein RA, Burdick JA, et al. The potential to improve cell infiltration in composite fiber-aligned electrospun scaffolds by the selective removal of sacrificial fibers. Biomaterials 2008;29:2348-58. https://doi.org/10.1016/j.biomaterials.2008.01.032
  74. Leong MF, Rasheed MZ, Lim TC, Chian KS. In vitro cell infiltration and in vivo cell infiltration and vascularization in a fibrous, highly porous poly(D,L-lactide) scaffold fabricated by cryogenic electrospinning technique. J Biomed Mater Res A 2009;91:231-40.
  75. Lee YH, Lee JH, An IG, Kim C, Lee DS, Lee YK, et al. Electrospun dual-porosity structure and biodegradation morphology of Montmorillonite reinforced PLLA nanocomposite scaffolds. Biomaterials 2005;26:3165-72. https://doi.org/10.1016/j.biomaterials.2004.08.018
  76. Brown TD, Dalton PD, Hutmacher DW. Direct writing by way of melt electrospinning. Adv Mater 2011;23:5651-7. https://doi.org/10.1002/adma.201103482
  77. Leong MF, Chan WY, Chian KS, Rasheed MZ, Anderson JM. Fabrication and in vitro and in vivo cell infiltration study of a bilayered cryogenic electrospun poly(D,L-lactide) scaffold. J Biomed Mater Res A 2010;94:1141-9.
  78. Jayasinghe SN, Irvine S, McEwan JR. Cell electrospinning highly concentrated cellular suspensions containing primary living organisms into cell-bearing threads and scaffolds. Nanomedicine (Lond) 2007;2:555-67. https://doi.org/10.2217/17435889.2.4.555
  79. Townsend-Nicholson A, Jayasinghe SN. Cell electrospinning: a unique biotechnique for encapsulating living organisms for generating active biological microthreads/scaffolds. Biomacromolecules 2006;7:3364-9. https://doi.org/10.1021/bm060649h
  80. Andreu N, Thomas D, Saraiva L, Ward N, Gustafsson K, Jayasinghe SN, et al. In vitro and in vivo interrogation of bio-sprayed cells. Small 2012;8:2495-500. https://doi.org/10.1002/smll.201200138
  81. Stankus JJ, Guan J, Fujimoto K, Wagner WR. Microintegrating smooth muscle cells into a biodegradable, elastomeric fiber matrix. Biomaterials 2006;27:735-44. https://doi.org/10.1016/j.biomaterials.2005.06.020
  82. Dehghani F, Annabi N. Engineering porous scaffolds using gas-based techniques. Curr Opin Biotechnol 2011;22:661-6. https://doi.org/10.1016/j.copbio.2011.04.005
  83. Keskar V, Marion NW, Mao JJ, Gemeinhart RA. In vitro evaluation of macroporous hydrogels to facilitate stem cell infiltration, growth, and mineralization. Tissue Eng Part A 2009;15:1695-707. https://doi.org/10.1089/ten.tea.2008.0238
  84. Barbetta A, Barigelli E, Dentini M. Porous alginate hydrogels: synthetic methods for tailoring the porous texture. Biomacromolecules 2009;10:2328-37. https://doi.org/10.1021/bm900517q
  85. Huang GY, Zhou LH, Zhang QC, Chen YM, Sun W, Xu F, et al. Microfluidic hydrogels for tissue engineering. Biofabrication 2011;3:012001. https://doi.org/10.1088/1758-5082/3/1/012001
  86. Silva DS, Wallace DB, Cooley PW, Radulescu D, Hayes DJ. An inkjet printing station for neuroregenerative tissue engineering. In: Engineering in Medicine and Biology Workshop; 2007 Nov 11-12; Dallas (TX), USA. IEEE; 2007. p.71-3.
  87. Marga F, Jakab K, Khatiwala C, Shepherd B, Dorfman S, Hubbard B, et al. Toward engineering functional organ modules by additive manufacturing. Biofabrication 2012;4:022001. https://doi.org/10.1088/1758-5082/4/2/022001
  88. Hockaday LA, Kang KH, Colangelo NW, Cheung PY, Duan B, Malone E, et al. Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication 2012;4:035005. https://doi.org/10.1088/1758-5082/4/3/035005
  89. Pataky K, Braschler T, Negro A, Renaud P, Lutolf MP, Brugger J. Microdrop printing of hydrogel bioinks into 3D tissue-like geometries. Adv Mater 2012;24:391-6. https://doi.org/10.1002/adma.201102800
  90. Lee W, Lee V, Polio S, Keegan P, Lee JH, Fischer K, et al. On-demand three-dimensional freeform fabrication of multi-layered hydrogel scaffold with fluidic channels. Biotechnol Bioeng 2010;105:1178-86.
  91. Stampfl J, Schuster M, Baudis S, Lichtenegger H, Liska R. Biodegradable stereolithography resins with defined mechanical properties. In: Bartolo PJ, de Tecnologia e Gestao ES, editors. Virtual and rapid manufacturing. London: Taylor & Francis Group; 2008. p.283-6
  92. Nguyen AK, Gittard SD, Koroleva A, Schlie S, Gaidukeviciute A, Chichkov BN, et al. Two-photon polymerization of polyethylene glycol diacrylate scaffolds with riboflavin and triethanolamine used as a water-soluble photoinitiator. Regen Med 2013;8:725-38. https://doi.org/10.2217/rme.13.60
  93. Jeon O, Bouhadir KH, Mansour JM, Alsberg E. Photocrosslinked alginate hydrogels with tunable biodegradation rates and mechanical properties. Biomaterials 2009;30:2724-34. https://doi.org/10.1016/j.biomaterials.2009.01.034
  94. Lo CW, Jiang H. Photopatterning and degradation study of dextran-glycidyl methacrylate hydrogels. Polym Eng Sci 2009;50:232-39.
  95. Prado SS, Weaver JM, Love BJ. Gelation of photopolymerized hyaluronic acid grafted with glycidyl methacrylate. Mater Sci Eng C 2011;31:1767-71. https://doi.org/10.1016/j.msec.2011.08.008
  96. Bartolo P. Stereolithography: materials, processes and applications. New York: Springer; 2011.
  97. Jhaveri SJ, McMullen JD, Sijbesma R, Tan LS, Zipfel W, Ober CK. Direct three-dimensional microfabrication of hydrogels via two-photon lithography in aqueous solution. Chem Mater 2009;21:2003-6. https://doi.org/10.1021/cm803174e
  98. Xue SH, Lv PJ, Wang Y, Zhao Y, Zhang T. Three dimensional bioprinting technology of human dental pulp cells mixtures. Beijing Da Xue Xue Bao 2013;45:105-8.
  99. Kim K, Lee CH, Kim BK, Mao JJ. Anatomically shaped tooth and periodontal regeneration by cell homing. J Dent Res 2010;89:842-7. https://doi.org/10.1177/0022034510370803
  100. Lee M, Wu BM. Recent advances in 3D printing of tissue engineering scaffolds. Methods Mol Biol 2012;868:257-67. https://doi.org/10.1007/978-1-61779-764-4_15

Cited by

  1. Advanced functional polymers for regenerative and therapeutic dentistry vol.21, pp.5, 2013, https://doi.org/10.1111/odi.12281
  2. The performance of bone tissue engineering scaffolds in in vivo animal models: A systematic review vol.31, pp.5, 2013, https://doi.org/10.1177/0885328216656476
  3. Nanomaterials for Tissue Engineering In Dentistry vol.6, pp.7, 2013, https://doi.org/10.3390/nano6070134
  4. Construction of 3D multicellular microfluidic chip for an in vitro skin model vol.19, pp.2, 2013, https://doi.org/10.1007/s10544-017-0156-5
  5. Structural, morphological and thermal characterization of poly (2-hydroxyethyl methacrylate-co-acrylonitrile) (P (HEMA-co-AN)) Cryogels: evaluation of water sorption potential and cytotoxicity vol.24, pp.7, 2013, https://doi.org/10.1007/s10965-017-1276-6
  6. Investigate the Effect of Thawing Process on the Self-Assembly of Silk Protein for Tissue Applications vol.2017, pp.None, 2017, https://doi.org/10.1155/2017/4263762
  7. Evaluation of Fibrin-Based Interpenetrating Polymer Networks as Potential Biomaterials for Tissue Engineering vol.7, pp.12, 2013, https://doi.org/10.3390/nano7120436
  8. Preparation and characteristics of gelatin sponges crosslinked by microbial transglutaminase vol.5, pp.None, 2013, https://doi.org/10.7717/peerj.3665
  9. Chitosan‐based hydrogels: recent design concepts to tailor properties and functions vol.66, pp.7, 2013, https://doi.org/10.1002/pi.5331
  10. Pore Size Manipulation in 3D Printed Cryogels Enables Selective Cell Seeding vol.3, pp.4, 2013, https://doi.org/10.1002/admt.201700340
  11. Gelatin-Based Microribbon Hydrogels Accelerate Cartilage Formation by Mesenchymal Stem Cells in Three Dimensions vol.24, pp.21, 2013, https://doi.org/10.1089/ten.tea.2018.0011
  12. Feasibility of Defect Tunable Bone Engineering Using Electroblown Bioactive Fibrous Scaffolds with Dental Stem Cells vol.4, pp.3, 2018, https://doi.org/10.1021/acsbiomaterials.7b00810
  13. Parallel fabrication of macroporous scaffolds vol.115, pp.7, 2013, https://doi.org/10.1002/bit.26593
  14. Polycaprolactone‐hydroxy apatite composites for tissue engineering applications vol.24, pp.3, 2018, https://doi.org/10.1002/vnl.21569
  15. Injectable Hyaluronic Acid- co -Gelatin Cryogels for Tissue-Engineering Applications vol.11, pp.8, 2013, https://doi.org/10.3390/ma11081374
  16. 3D scaffolds for brain tissue regeneration: architectural challenges vol.6, pp.11, 2018, https://doi.org/10.1039/c8bm00422f
  17. Milieu for Endothelial Differentiation of Human Adipose-Derived Stem Cells vol.5, pp.4, 2013, https://doi.org/10.3390/bioengineering5040082
  18. Delivery of targeted gene therapies using a hybrid cryogel-coated prosthetic vascular graft vol.7, pp.None, 2019, https://doi.org/10.7717/peerj.7377
  19. Latest Advances in Cryogel Technology for Biomedical Applications vol.2, pp.4, 2013, https://doi.org/10.1002/adtp.201800114
  20. Electrospun Polyvinylidene Fluoride-Based Fibrous Scaffolds with Piezoelectric Characteristics for Bone and Neural Tissue Engineering vol.9, pp.7, 2013, https://doi.org/10.3390/nano9070952
  21. Smart Hydrogels in Tissue Engineering and Regenerative Medicine vol.12, pp.20, 2013, https://doi.org/10.3390/ma12203323
  22. Evaluation of Strontium-Doped Nanobioactive Glass Cement for Dentin-Pulp Complex Regeneration Therapy vol.5, pp.11, 2013, https://doi.org/10.1021/acsbiomaterials.9b01018
  23. Recent advances in biomaterials for 3D scaffolds: A review vol.4, pp.None, 2013, https://doi.org/10.1016/j.bioactmat.2019.10.005
  24. Injectable and in situ crosslinkable gelatin microribbon hydrogels for stem cell delivery and bone regeneration in vivo vol.10, pp.13, 2013, https://doi.org/10.7150/thno.41096
  25. Advances in biomaterials for adipose tissue reconstruction in plastic surgery vol.9, pp.1, 2013, https://doi.org/10.1515/ntrev-2020-0028
  26. A new classification method of nanotechnology for design integration in biomaterials vol.9, pp.1, 2013, https://doi.org/10.1515/ntrev-2020-0063
  27. Porous titanium fiber mesh with tailored elasticity and its effect on stromal cells vol.108, pp.5, 2020, https://doi.org/10.1002/jbm.b.34556
  28. Electroconductive Hydrogels for Tissue Engineering: Current Status and Future Perspectives vol.2, pp.3, 2013, https://doi.org/10.1089/bioe.2020.0025
  29. Biomaterials as Local Niches for Immunomodulation vol.53, pp.9, 2013, https://doi.org/10.1021/acs.accounts.0c00341
  30. Needle-injectable microcomposite cryogel scaffolds with antimicrobial properties vol.10, pp.1, 2013, https://doi.org/10.1038/s41598-020-75196-1
  31. Hydroxyl Groups Induce Bioactivity in Silica/Chitosan Aerogels Designed for Bone Tissue Engineering. In Vitro Model for the Assessment of Osteoblasts Behavior vol.12, pp.12, 2013, https://doi.org/10.3390/polym12122802
  32. Engineering a macroporous fibrin-based sequential interpenetrating polymer network for dermal tissue engineering vol.8, pp.24, 2013, https://doi.org/10.1039/d0bm01161d
  33. Hydrogel Properties and Their Impact on Regenerative Medicine and Tissue Engineering vol.25, pp.24, 2013, https://doi.org/10.3390/molecules25245795
  34. Recent advances in heavy metal removal by chitosan based adsorbents vol.251, pp.None, 2013, https://doi.org/10.1016/j.carbpol.2020.117000
  35. Biocompatible and Biomaterials Application in Drug Delivery System in Oral Cavity vol.2021, pp.None, 2013, https://doi.org/10.1155/2021/9011226
  36. Synthesis and Characterization of Biocompatible Methacrylated Kefiran Hydrogels: Towards Tissue Engineering Applications vol.13, pp.8, 2021, https://doi.org/10.3390/polym13081342
  37. Photopolymerized Porous Hydrogels vol.22, pp.4, 2013, https://doi.org/10.1021/acs.biomac.0c01671
  38. Structural Diversity in Cryoaerogel Synthesis vol.37, pp.17, 2013, https://doi.org/10.1021/acs.langmuir.0c03619
  39. Hyaluronic Acid-Based Shape-Memory Cryogel Scaffolds for Focal Cartilage Defect Repair vol.27, pp.11, 2013, https://doi.org/10.1089/ten.tea.2020.0264
  40. Cryogel-Integrated Biochip for Liver Tissue Engineering vol.4, pp.7, 2013, https://doi.org/10.1021/acsabm.1c00425
  41. Mechanical Properties of Compact Bone Defined by the Stress-Strain Curve Measured Using Uniaxial Tensile Test: A Concise Review and Practical Guide vol.14, pp.15, 2013, https://doi.org/10.3390/ma14154224
  42. Hydrogel, a novel therapeutic and delivery strategy, in the treatment of intrauterine adhesions vol.9, pp.33, 2013, https://doi.org/10.1039/d1tb01005k
  43. The latest achievements in plant cellulose-based biomaterials for tissue engineering focusing on skin repair vol.288, pp.p2, 2013, https://doi.org/10.1016/j.chemosphere.2021.132529