Three-dimensional scaffolds for bioengineering of cartilage tissue

• Autorzy: Wasyłeczko Monika , Krysiak Zuzanna Joanna , Łukowska Ewa , Gruba Marcin , Sikorska Wioleta , Kruk Aleksandra , Dulnik Judyta , Czubak Jarosław , Chwojnowski Andrzej

Identyfikatory

DOI

10.1016/j.bbe.2022.03.004

• Języki publikacji: EN

Abstrakty

EN

The cartilage tissue is neither supplied with blood nor innervated, so it cannot heal by itself. Thus, its reconstruction is highly challenging and requires external support. Cartilage diseases are becoming more common due to the aging population and obesity. Among young people, it is usually a post-traumatic complication. Slight cartilage damage leads to the spontaneous formation of fibrous tissue, not resistant to abrasion and stress, resulting in cartilage degradation and the progression of the disease. For these reasons, cartilage regeneration requires further research, including use of new type of biomaterials for scaffolds. This paper shows cartilage characteristics within its most frequent problems and treatment strategies, including a promising method that combines scaffolds and human cells. Structure and material requirements, manufacturing methods, and commercially available scaffolds were described. Also, the comparison of poly(L-lactide) (PLLA) and polyethersulfone (PES) 3D membranes obtained by a phase inversion method using nonwovens as a pore-forming additives were reported. The scaffolds’ structure and the growth ability of human chondrocytes were compared. Scaffolds’ structure, cells morphology, and protein presence in the membranes were examined with a scanning electron microscope. The metabolic activity of cells was tested with the MTT assay. The structure of the scaffolds and the growth capacity of human chondrocytes were compared. Obtained results showed higher cell activity and protein content for PES scaffolds than for PLLA. The PES membrane had better mechanical properties (e.g. ripping), greater chondrocytes proliferation, and thus a better secretion of proteins which build up the cartilage structure.

Słowa kluczowe

EN

porous 3D scaffolds; membrane structure; polyethersulfone; poly(L-lactide); chondrocyte culture; cartilage regeneration

PL

skafoldy trójwymiarowe; struktura membranowa; polieterosulfon; regeneracja chrząstki

• Wydawca: Nałęcz Institute of Biocybernetics and Biomedical Engineering of the Polish Academy of Sciences ; Elsevier
• Czasopismo: Biocybernetics and Biomedical Engineering
• Rocznik: 2022
• Tom: Vol. 42, no. 2
• Strony: 494--511
• Opis fizyczny: Bibliogr. 163 poz., rys., tab., wykr.

Twórcy

autor

Wasyłeczko Monika

• Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Department of Biomaterials and Biotechnological Systems, KsieciaTrojdena 4 str., Room 142, 02-109 Warsaw, Poland

autor

Krysiak Zuzanna Joanna

• Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland
• International Center of Electron Microscopy for Material Science, Faculty of Metals Engineering and Industrial Computer Science, AGH University of Science and Technology, Cracow, Poland

autor

Łukowska Ewa

• Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland

autor

Gruba Marcin

• Gruca Orthopedic and Trauma Teaching Hospital, Centre of Postgraduate Medical Education, Otwock, Poland

autor

Sikorska Wioleta

• Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland

autor

Kruk Aleksandra

• Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland
• Faculty of Chemistry Warsaw University of Technology, Warsaw, Poland

autor

Dulnik Judyta

• Institute of Fundamental Technological Research, Polish Academy of Sciences, Warsaw, Poland

autor

Czubak Jarosław

• Gruca Orthopedic and Trauma Teaching Hospital, Centre of Postgraduate Medical Education, Otwock, Poland

autor

Chwojnowski Andrzej

• Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland

Bibliografia

• [1] Giwa S, Lewis JK, Alvarez L, Langer R, Roth AE, Church GM, et al. The promise of organ and tissue preservation to transform medicine. Nat Biotechnol 2017;35(6):530–42. https://doi.org/10.1038/nbt.3889.
• [2] Yan Q, Dong H, Su J, Han J, Song B, Wei Q, et al. A review of 3D printing technology for medical applications. Engineering 2018;4:729–42. https://doi.org/10.1016/j.eng.2018.07.021.
• [3] Popoola J, Greene H, Kyegombe M, MacPhee IA. Patient involvement in selection of immunosuppressive regimen following transplantation. Patient Preference Adherence 2014;8:1705–12. https://doi.org/10.2147/PPA.S38987.
• [4] Dzobo K, Thomford NE, Senthebane DA, Shipanga H, Rowe A, Dandara C, et al. Advances in regenerative medicine and tissue engineering: innovation and transformation of medicine. Stem Cells Int 2018;2018:1–24. https://doi.org/10.1155/2018/2495848.
• [5] Park KM, Shin YM, Kim K, Shin H. Tissue engineering and regenerative medicine 2017: a year in review. Tissue Eng -Part B 2018;24(5):327–44. https://doi.org/10.1089/ten.teb.2018.0027.
• [6] Messner F, Guo Y, Etra JW, Brandacher G. Emerging technologies in organ preservation, tissue engineering and regenerative medicine: a blessing or curse for transplantation? Transpl Int 2019;32:673–85. https://doi.org/10.1111/tri.13432.
• [7] Scarritt ME, Pashos NC, Bunnell BA. A review of cellularization strategies for tissue engineering of whole organs. Front Bioeng Biotechnol 2015;3:1–17. https://doi.org/10.3389/fbioe.2015.00043.
• [8] Mir TA, Iwanaga S, Kurooka T, Toda H, Sakai S. Biofabrication offers future hope for tackling various obstacles and challenges in tissue engineering and regenerative medicine: a perspective. Int J Bioprinting 2019;5(1):1–11.
• [9] Murphy SV, Atala A. Organ engineering - combining stem cells, biomaterials, and bioreactors to produce bioengineered organs for transplantation. BioEssays 2012;35(3):163–72. https://doi.org/10.1002/bies.201200062.
• [10] Tang X, Qin Y, Xu X, Guo D, Ye W, Wu W, et al. Fabrication and in vitro evaluation of 3D printed porous polyetherimide scaffolds for bone tissue engineering. Biomed Res Int 2019;2019:1–8. https://doi.org/10.1155/2019/2076138.
• [11] Sasaki J-I, Hashimoto M, Yamaguchi S, Itoh Y, Yoshimoto I, Matsumoto T, et al. Fabrication of biomimetic bone tissue using mesenchymal stem cell-derived three- dimensional constructs incorporating endothelial cells. PLoS ONE 2015;10(6):1–17. https://doi.org/10.1371/journal.pone.0129266.
• [12] Mazza G, Al-Akkad W, Rombouts K, Pinzani M. Liver tissue engineering: from implantable tissue to whole organ engineering. Hepatol Commun 2017;2(2):131–41. https://doi.org/10.1002/hep4.1136.
• [13] Hussein KH, Saleh T, Ahmed E, Kwak H, Park K, Yang S, et al. Biocompatibility and hemocompatibility of efficiently decellularized whole porcine kidney for tissue engineering. J Biomed Mater Res A 2018;106(7):2034–47. https://doi.org/10.1002/jbm.a.36407.
• [14] Zhang D, Wei G, Li P, Zhou X. Urine-derived stem cells: a novel and versatile progenitor source for cell-based therapy and regenerative medicine. Genes Dis 2014;1:8–17. https://doi.org/10.1016/j.gendis.2014.07.001.
• [15] Perán M, García MA, Lopez-ruiz E, Jiménez G, Marchal JA. How can nanotechnology help to repair the body? Advances in cardiac, skin, bone. Cartilage Nerve Mater 2013;6:1333–59. https://doi.org/10.3390/ma6041333.
• [16] Yeung P, Cheng KH, Yan CH, Chan BP. Collagen microsphere based 3D culture system for human osteoarthritis chondrocytes. Sci Rep 2019;9:1–14. https://doi.org/10.1038/s41598-019-47946-3.
• [17] Kirby GTS, Mills SJ, Cowin AJ, Smith LE. Stem cells for cutaneous wound healing. Biomed Res Int 2015;2015:1–11.https://doi.org/10.1155/2015/285869.
• [18] Ciechanowska A, Ladyzynski P, Hoser G, Sabalinska S, Kawiak J, Foltynski P, et al. Human endothelial cells hollow fiber membrane bioreactor as a model of the blood vessel for in vitro studies. J Artif Organs 2016;19(3):270–7. https://doi.org/10.1007/s10047-016-0902-0.
• [19] Boyce ST, Lalley AL. Tissue engineering of skin and regenerative medicine for wound care. Burns Trauma 2018;6(4):1–10. https://doi.org/10.1186/s41038-017-0103-y.
• [20] Tarassoli SP, Jessop ZM, Al-Sabah A, Gao N, Whitaker S, Doak S, et al. Skin tissue engineering using 3D bioprinting: an evolving research field. J Plastic Reconstructive Aesth Surg 2018;71:615–23. https://doi.org/10.1016/j.bjps.2017.12.006.
• [21] Lewis PL, Green RM, Shah RN. 3D-printed gelatin scaffolds of differing pore geometry modulate hepatocyte function and gene expression. Acta Biomater 2018;69:63–70. https://doi.org/10.1016/j.actbio.2017.12.042.
• [22] Moreira R, Velz T, Alves N, Gesche VN, Malischewski A, Schmitz-Rode T, et al. Tissue-engineered heart valve with a tubular leaflet design for minimally invasive transcatheter implantation. Tissue Eng Part C 2015;21(6):530–40. https://doi.org/10.1089/ten.tec.2014.0214.
• [23] Kinasiewicz A, Dudziński K, Chwojnowski A, Weryński A, Kawiak J. Three-dimensional culture of hepatocytes on spongy polyethersulfone membrane developed for cell transplantation. Transpl Proc 2007;39:2914–6. https://doi.org/10.1016/j.transproceed.2007.08.061.
• [24] Kinasiewicz A, Śmietanka A, Dudziński K, Chwojnowski A, Gajkowska B, Weryński A. Spongy polyethersulfone membrane for hepatocyte cultivation: studies on human hepatoma C3A cells. Artif Organs 2008;32(9):747–52. https://doi.org/10.1111/j.1525-1594.2008.00600.x.
• [25] Farina M, Alexander JF, Thekkedath U, Ferrari M, Grattoni A. Cell encapsulation: overcoming barriers in cell transplantation in diabetes and beyond. Adv Drug Deliv Rev 2019;139:92–115. https://doi.org/10.1016/j.addr.2018.04.018.
• [26] Liu Y, Luo J, Chen X, Liu W, Chen T. Cell membrane coating technology: a promising strategy for biomedical applications. Nano-Micro Lett 2019;11:1–46. https://doi.org/10.1007/s40820-019-0330-9.
• [27] Plichta A, Kowalczyk S, Kamiński K, Wasyłeczko M, Więckowski S, Olędzka E, et al. ATRP of methacrylic derivative of camptothecin initiated with PLA toward three-arm star block copolymer conjugates with favorable drug release. Macromolecules 2017;50:6439–50. https://doi.org/10.1021/acs.macromol.7b01350.
• [28] Walter SG, Ossendorff R, Schildberg FA. Articular cartilage regeneration and tissue engineering models: a systematic review. Arch Orthop Trauma Surg 2018;139(3):305–16. https://doi.org/10.1007/s00402-018-3057-z.
• [29] Kwon H, Brown WE, Lee CA, Wang D, Paschos N, Hu JC, et al. Surgical and tissue engineering strategies for articular cartilage and meniscus repair. Nat Rev Rheumatol 2019;15:550–70. https://doi.org/10.1038/s41584-019-0255-1.
• [30] Zhao Z, Fan C, Chen F, Sun Y, Xia Y, Ji A, et al. Progress in articular cartilage tissue engineering: a review on therapeutic cells and macromolecular scaffolds. Macromol Biosci 2019;1900278:1–13. https://doi.org/10.1002/mabi.201900278.
• [31] Orłowska J, Kurczewska U, Derwińska K, Orłowski W, Orszulak-Michalak D. The use of biodegradable polymers in design of cellular scaffolds. Postępy Higieny Medycyny Doświadczalnej 2015;69:294–301. https://doi.org/10.5604/17322693.1142717.
• [32] Pina S, Ribeiro VP, Marques CF, Maia FR, Silva TH, Reis RL, et al. Scaffolding strategies for tissue engineering and regenerative medicine applications. Materials 1824;2019(12):1–42. https://doi.org/10.3390/ma12111824.
• [33] Bružauskaitė I, Bironaitė D, Bagdonas E, Bernotienė E. Scaffolds and cells for tissue regeneration: different scaffold pore sizes—different cell effects. Cytotechnology 2016;68:355–69. https://doi.org/10.1007/s10616-015-9895-4.
• [34] Chwojnowski A, Wojciechowski C, Dudziński K, Łukowska E. Polysulphone and polyethersulphone hollow fiber membranes with developed inner surface as material for bio-medical applications. Biocybernetics Biomed Eng 2009;29:47–59.
• [35] Zhao P, Gu H, Mi H, Rao C, Fu J, Turng LS. Fabrication of scaffolds in tissue engineering: a review. Front Mech Eng 2018;13:107–19. https://doi.org/10.1007/s11465-018-0496-8.
• [36] Loh QL, Choong C. Three-dimensional scaffolds for tissue engineering applications: role of porosity and pore size. Tissue Eng Part B: Rev 2013;19:485–502. https://doi.org/10.1089/ten.teb.2012.0437.
• [37] Sophia Fox AJ, Bedi A, Rodeo SA. The basic science of articular cartilage: structure, composition, and function. Sports Health Orthopaedics 2009;1(6):461–8. https://doi.org/10.1177/1941738109350438.
• [38] Archer CW, Francis-West P. The chondrocyte. Int J Biochem Cell Biol 2003;35:401–4. https://doi.org/10.1016/S1357-2725(02)00301-1.
• [39] Grassel S, Aszodi A. Cartilage. Volume 1: Physiology and Development. Switzerland: Springer; 2016.
• [40] Krishnan Y, Grodzinsky AJ. Cartilage diseases. Matrix Biol 2018;71–72:51–69. https://doi.org/10.1016/j.matbio.2018.05.005.
• [41] Collins AT, Kulvaranon ML, Cutcliffe HC, Utturkar GM, Smith WAR, Spritzer CE, et al. Obesity alters the in vivo mechanical response and biochemical properties of cartilage as measured by MRI. Arthritis Res Ther 2018;20:1–9. https://doi.org/10.1186/s13075-018-1727-4.
• [42] Appleton CT. Osteoarthritis year in review 2017: biology. Osteoarthritis Cartilage 2018;26:296–303. https://doi.org/10.1016/j.joca.2017.10.008.
• [43] Yeung P, Zhang W, Wang XN, Yan CH, Chan BP. A human osteoarthritis osteochondral organ culture model for cartilage tissue engineering. Biomaterials 2018;162:1–21. https://doi.org/10.1016/j.biomaterials.2018.02.002.
• [44] Guilak F, Nims RJ, Dicks A. Osteoarthritis as a disease of the cartilage pericellular matrix. Matrix Biol 2018;71-72:40–50. https://doi.org/10.1016/j.matbio.2018.05.008.
• [45] Merkely G, Ackermann J, Lattermann C. Articular cartilage defects: incidence, diagnosis, and natural history. Operative Tech Sports Med 2018;26:156–61. https://doi.org/10.1053/j.otsm.2018.06.008.
• [46] Medvedeva EV, Grebenik EA, Gornostaeva SN, Telpuhov VI, Lychagin AV, Timashev PS, et al. Repair of damaged articular cartilage: current approaches and future directions. Int J Mol Sci 2018;19(2366):1–23. https://doi.org/10.3390/ijms19082366.
• [47] Armiento AR, Alini M, Stoddart MJ. Articular fibrocartilage - Why does hyaline cartilage fail to repair? Adv Drug Deliv Rev 2019;146:289–305. https://doi.org/10.1016/j.addr.2018.12.015.
• [48] Liu Y, Zhou G, Cao Y. Recent progress in cartilage tissue engineering — our experience and future directions. Engineering 2017;3:28–35. https://doi.org/10.1016/J.ENG.2017.01.010.
• [49] Mirza U, Shubeena S, Shah MS, Zaffer B. Microfracture: a technique for repair of chondral defects. J Entomol Zool Stud 2018;6(5):1092–7.
• [50] Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L. Treatment of deep cartilage defect in knee with autologous chondrocyte transplantation. N Engl J Med 1994;331:889–95. https://doi.org/10.1056/NEJM199410063311401.
• [51] Kraeutler MJ, Belk JW, Purcell JM, McCarty EC. Microfracture versus autologous chondrocyte implantation for articular cartilage lesions in the knee: a systematic review of 5-year outcomes. Am J Sports Med 2018;46:995–9. https://doi.org/10.1177/0363546517701912.
• [52] Minas T, Von Keudell A, Bryant T, Gomoll AH. The John Insall Award: a minimum 10-year outcome study of autologous chondrocyte implantation knee. Clin Orthop Relat Res 2014;472:41–51. https://doi.org/10.1007/s11999-013-3146-9.
• [53] Gao L, Orth P, Cucchiarini M, Madry H. Autologous matrix-induced chondrogenesis: a systematic review of the clinical evidence. Am J Sports Med 2019;47:222–31. https://doi.org/10.1177/0363546517740575.
• [54] Schiavone Panni A, Del Regno C, Mazzitelli G, D’Apolito R, Corona K, Vasso M. Good clinical results with autologous matrix-induced chondrogenesis (Amic) technique in large knee chondral defects. Knee Surg Sports Traumatol Arthrosc 2018;26:1130–6. https://doi.org/10.1007/s00167-017-4503-0.
• [55] Lee YHD, Suzer F, Thermann H. Autologous matrix-induced chondrogenesis in the knee: a review. Cartilage 2014;5:145–53. https://doi.org/10.1177/1947603514529445.
• [56] Erickson BJ, Strickland SM, Gomoll AH. Indications, techniques, outcomes for matrix-induced autologous chondrocyte implantation (MACI). Oper Tech Sports Med 2018;26:175–82. https://doi.org/10.1053/j.otsm.2018.06.002.
• [57] Dunkin BS, Lattermann C. New and emerging techniques in cartilage repair: Matrix-induced autologous chondrocyte implantation. Oper Tech Sports Med 2013;21:100–7. https://doi.org/10.1053/j.otsm.2013.03.003.
• [58] Brittberg M. Scaffold based autologous chondrocyte implantation: the surgical technique. Asian J Arthroscopy 2019;4(1):23–6. https://doi.org/10.13107/aja.2456-1169. v04i01.006.
• [59] Cao C, Zhang Y, Ye Y, Sun T. Effects of cell phenotype and seeding density on the chondrogenic capacity of human osteoarthritic chondrocytes in type I collagen scaffolds. J Orthop Surg Res 2020;15(120):1–11.
• [60] Fahy N, Alini M, Stoddart MJ. Mechanical stimulation of mesenchymal stem cells: implications for cartilage tissue engineering. J Orthop Res 2018;36:52–63. https://doi.org/10.1002/jor.23670.
• [61] Mastrolia I, Foppiani EM, Murgia A, Candini O, Samarelli AV, Grisendi G, et al. Challenges in clinical development of mesenchymal stromal/stem cells: concise review. Stem Cells Transl Med 2019;8(11):1135–48. https://doi.org/10.1002/sctm.19-0044.
• [62] Li X, Liang Y, Xu X, Xiong J, Ouyang K, Duan L, et al. Cell-tocell culture inhibits dedifferentiation of chondrocytes and induces differentiation of human umbilical cord-derived mesenchymal stem cells. Biomed Res Int 2019;2019:1–11. https://doi.org/10.1155/2019/5871698.
• [63] Okubo R, Asawa Y, Watanabe M, Nagata S, Nio M. Proliferation medium in three-dimensional culture of auricular chondrocytes promotes effective cartilage regeneration in vivo. Regenerative Ther 2019;11:306–15. https://doi.org/10.1016/j.reth.2019.10.002.
• [64] Bružauskaite I, Bironait D, Bagdonas E, Bernotiene E. Scaffolds and cells for tissue regeneration : different scaffold pore sizes — different cell effects. Cytotechnology 2015;68:355–69. https://doi.org/10.1007/s10616-015-9895-4.
• [65] Kalkan R, Nwekwo CW, Adali T. The use of scaffolds in cartilage regeneration. Eukaryotic Gene Express 2018;28(4):343–8.
• [66] Eltom A, Zhong G, Muhammad A. Scaffold techniques and designs in tissue engineering functions and purposes: a review. Adv Mater Sci Eng 2019;2019:1–14. https://doi.org/10.1155/2019/3429527.
• [67] Irawan V, Sung TC, Higuchi A, Ikoma T. Collagen scaffolds in cartilage tissue engineering and relevant approaches for future development. Tissue Eng Regenerative Med 2018;15:673–97. https://doi.org/10.1007/s13770-018-0135-9.
• [68] Panadero JA, Lanceros-Mendez S, Ribelles JLG. Differentiation of mesenchymal stem cells for cartilage tissue engineering: individual and synergetic effects of three-dimensional environment and mechanical loading. Acta Biomater 2016;33:1–12. https://doi.org/10.1016/j.actbio.2016.01.037.
• [69] Conoscenti G, Schneider T, Stoelzel K, Carfí Pavia F, Brucato V, Goegele C, et al. PLLA scaffolds produced by thermally induced phase separation (TIPS) allow human chondrocyte growth and extracellular matrix formation dependent on pore size. Mater Sci Eng, C 2017;80:449–59.
• [70] Demoor M, Ollitrault D, Gomez-Leduc T, Bouyoucef M, Hervieu M, Fabre H, et al. Cartilage tissue engineering: molecular control of chondrocyte differentiation for proper cartilage matrix reconstruction. Biochim Biophys Acta - General Subjects 2014;1840(8):2414–40. https://doi.org/10.1016/j.bbagen.2014.02.030.
• [71] Huang BJ, Hu JC, Athanasiou KA. Cell-based tissue engineering strategies used in the clinical repair of articular cartilage. Biomaterials 2016;98:1–22. https://doi.org/10.1016/j.biomaterials.2016.04.018.
• [72] Zhao Y, Tan K, Zhou Y, Ye Z, Tan WS. A combinatorial variation in surface chemistry and pore size of three-dimensional porous poly(e-caprolactone) scaffolds modulates the behaviors of mesenchymal stem cells. MaterSci Eng, C 2016;59:193–202. https://doi.org/10.1016/j.msec.2015.10.017.
• [73] Nava MM, Draghi L, Giordano C, Pietrabissa R. The effect of scaffold pore size in cartilage tissue engineering. J Appl Biomater Funct Mater 2016;14:e223–9. https://doi.org/10.5301/jabfm.5000302.
• [74] Matsiko A, Gleeson JP, O’Brien FJ. Scaffold mean pore size influences mesenchymal stem cell chondrogenic differentiation and matrix deposition. Tissue Eng - Part A 2015;21:486–97. https://doi.org/10.1089/ten.tea.2013.0545.
• [75] Lai YS, Chen WC, Huang CH, Cheng CK, Chan KK, Chang TK, et al. The effect of graft strength on knee laxity and graft insitu forces after posterior cruciate ligament reconstruction. PLoS ONE 2015;10:1–11. https://doi.org/10.1371/journal.pone.0127293.
• [76] Koh YG, Lee JA, Kim YS, Lee HY, Kim HJ, Kang KT. Optimal mechanical properties of a scaffold for cartilage regeneration using finite element analysis. J Tissue Eng 2019;10:1–10. https://doi.org/10.1177/2041731419832133.
• [77] Depends C, Anderer U. Tissue specific differentiation of human chondrocytes depends on cell microenvironment and serum selection. Cells 2019;8(934):1–15.
• [78] Dulnik J, Sajkiewicz P. Characterization of biocomponent polycaprolactone/gelatin electrospun nanofibres crosslinked with EDC/NHS. Eng Biomater 2019;153:26.
• [79] Chwojnowsk A, Kruk A, Wojciechowski C, Łukowska E, Dulnik J, Sajkiewicz P. The dependence of the membrane structure on the nonwoven forming the macropores in the 3D scaffolds preparation. Desalin Water Treat 2017;64:324–31. https://doi.org/10.5004/dwt.2017.11394.
• [80] Kruk A, Gadomska-Gajadhur AA, Dulnik J. Preparation of biodegradable semi-permeable membranes as 3D scaffolds for cell cultures preparation of biodegradable semi-permeable membranes as 3D scaffolds for cell cultures. Desalin Water Treat 2017;64:317–23. https://doi.org/10.5004/dwt.2016.11415.
• [81] Dudziński K, Chwojnowski A, Gutowska M, Płończak M, Czubak J, Łukowska E, et al. Three dimensional polyethersulphone scaffold for chondrocytes cultivation - the future supportive material for articular cartilage regeneration. Biocyber Biomed Eng 2010;30:65–76.
• [82] Gadomska-Gajadhur A, Kruk A, Ruśkowski P, Sajkiewicz P, Dulnik J, Chwojnowski A. Original method of imprinting pores in scaffolds for tissue engineering. Polym Adv Technol 2021;32:1–13. https://doi.org/10.1002/pat.5091.
• [83] Chwojnowski A, Wojciechowski C, Nowak J, Kupikowska-Stobba B, Grzeczkowicz M. Studies on the structure of semi-permeable membranes by means of SEM problems and potential sources of errors. Biocyber Biomed Eng 2012;32(1):51–64. https://doi.org/10.1016/S0208-5216(12)70032-3.
• [84] Chwojnowski A, Przytulska M, Wierzbicka D, Kulikowski J, Wojciechowski C. Membranes’ porosity evaluation by computer-aided analysis of sem images – a preliminary study. Biocyber Biomed Eng 2012;32(4):65–75. https://doi.org/10.1016/S0208-5216(12)70050-5.
• [85] Przytulska M, Kruk A, Kulikowski JL, Wojciechowski C, Gadomska-Gajadhur A, Chwojnowski A. Comparative assessment of polyvinylpyrrolidone type of membranes based on porosity analysis. Desalin Water Treat 2017;75:18–25. https://doi.org/10.5004/dwt.2017.20586.
• [86] Kulikowski JL, Przytulska M, Chwojnowski A. Computer-aided analysis of micro-morphological structure of porous membranes. Biomed Eng Online 2018;17:1–15. https://doi.org/10.1186/s12938-018-0481-9.
• [87] Przytulska M, Kulikowski JL, Wasyłeczko M, Chwojnowski A, Pietka D. The evaluation of 3D morphological structure of porous membranes based on a computer-aided analysis of their 2D images. Desalin Water Treat 2018;128:11–9. https://doi.org/10.5004/dwt.2018.22569.
• [88] Sikorska W, Wojciechowski C, Przytulska M, Rokicki G, Wasyłeczko M, Kulikowski JL, et al. Polysulfone–polyurethane (PSf-PUR) blend partly degradable hollow fiber membranes: preparation, characterization, and computer image analysis. Desalin Water Treat 2018;128:383–91. https://doi.org/10.5004/dwt.2018.23101.
• [89] Nikolova MP, Chavali MS. Recent advances in biomaterials for 3D scaffolds: a review. Bioact Mater 2019;4:271–92. https://doi.org/10.1016/j.bioactmat.2019.10.005.
• [90] Ahmadi F, Giti R, Mohammadi-Samani S, Mohammadi F. Biodegradable scaffolds for cartilage tissue engineering. Galen Med J 2017;6:70–80. https://doi.org/10.22086/GMJ. V6I2.696.
• [91] Armiento AR, Stoddart MJ, Alini M, Eglin D. Biomaterials for articular cartilage tissue engineering: learning from biology. Acta Biomater 2018;65:1–20. https://doi.org/10.1016/j.actbio.2017.11.021.
• [92] Setayeshmehr M, Esfandiari E, Rafieinia M, Hashemibeni B, Taheri-kafrani A, Samadikuchaksaraei A. Hybrid and composite scaffolds based on extracellular. Tissue Eng Part B 2019;25:202–24. https://doi.org/10.1089/ten.teb.2018.0245.
• [93] Jafari M, Paknejad Z, Rad MR, Motamedian SR, Eghbal MJ, Nadjmi N, et al. Polymeric scaffolds in tissue engineering: a literature review. J Biomed Mater Res - Part B Appl Biomater 2017;105(2):431–59. https://doi.org/10.1002/jbm.b.33547.
• [94] Jeuken RM, Roth AK, Peters RJRW, van Donkelaar CC, Thies JC, van Rhijn LW, et al. Polymers in cartilage defect repair of the knee: current status and future prospects. Polymers 2016;8:1–30. https://doi.org/10.3390/polym8060219.
• [95] Ulery BD, Nair LS, Laurencin CT. Biomedical applications of biodegradable polymers. J Polym Sci, Part B: Polym Phys 2011;49:832–64. https://doi.org/10.1002/polb.22259.
• [96] Daranarong D, Techaikool P, Intatue W, Daengngern R, Thomson KA, Molloy R, et al. Effect of surface modification of poly(L-lactide-co-e-caprolactone) membranes by low-pressure plasma on support cell biocompatibility. Surf Coat Technol 2016;306:328–35.
• [97] Ye H, Zhang K, Kai D, Li Z, Loh XJ. Polyester elastomers for soft tissue engineering. Chem Soc Rev 2018;47:4545–80. https://doi.org/10.1039/c8cs00161h.
• [98] Nofar M, Sacligil D, Carreau PJ, Kamal MR, Heuzey MC. Poly (lactic acid) blends: processing, properties and applications. Int J Biol Macromol 2019;125:307–60. https://doi.org/10.1016/j.ijbiomac.2018.12.002.
• [99] Shuai C, Li Y, Wang G, Yang W, Peng S, Feng P. Surface modification of nanodiamond: toward the dispersion of reinforced phase in poly-L-lactic acid scaffolds. Int J Biol Macromol 2019;126:1116–24. https://doi.org/10.1016/j.ijbiomac.2019.01.004.
• [100] He Y, Wang WR, Ding JD. Effects of L-lactic acid and D, L-lactic acid on viability and osteogenic differentiation of mesenchymal stem cells. Chin Sci Bull 2013;58:2404–11. https://doi.org/10.1007/s11434-013-5798-y.
• [101] Filimon A, Olaru N, Doroftei F, Logigan C, Dunca S. Design of biological active surface based on functionalized polysulfones by electrospinning. Proceedings 2019; 41:1–8. https://doi.org/10.3390/ecsoc-23-06495.
• [102] Irfan M, Idris A. Overview of PES biocompatible/hemodialysis membranes: PES-blood interactions and modification techniques. Mater Sci Eng, C 2015;56:574–92. https://doi.org/10.1016/j.msec.2015.06.035.
• [103] Mahboudi H, Soleimani M, Enderami SE, Kehtari M, Hanaee-Ahvaz H, Ghanbarian H, et al. The effect of nanofibre-based polyethersulfone (PES) scaffold on the chondrogenesis of human induced pluripotent stem cells. Artif Cells Nanomed Biotechnol 2018:1–9.
• [104] Lam ATL, Reuveny S, Oh SKW. Human mesenchymal stem cell therapy for cartilage repair: review on isolation, expansion, and constructs. Stem Cell Res 2020;44. https://doi.org/10.1016/j.scr.2020.101738 101738.
• [105] Xu Y, Kim C, Saylor DM, Koo D. Polymer degradation and drug delivery in PLGA-based drug – polymer applications: a review of experiments and theories. Society For Biomater 2016;105(6):1692–716. https://doi.org/10.1002/jbm.b.33648.
• [106] Jiang L, Xu L, Ma B, Ding H, Tang C. Effect of component and surface structure on poly (L-lactide-co-e-caprolactone) (PLCA)-based composite membrane. Compos B 2019;174. https://doi.org/10.1016/j.compositesb.2019.107031 107031.
• [107] Prasanna S, Narayan B, Rastogi A, Srivastava P. Design and evaluation of chitosan/poly (L-lactide)/ pectin based composite scaffolds for cartilage tissue regeneration. Int J Biol Macromol 2018;112:909–20. https://doi.org/10.1016/j.ijbiomac.2018.02.049.
• [108] Zhang X, Wu Y, Pan Z, Sun H,Wang J, Yu D, et al. The effects of lactate and acid on articular chondrocytes function: implications for polymeric cartilage scaffold design. Acta Biomater 2016;42:329–40. https://doi.org/10.1016/j.actbio.2016.06.029.
• [109] Dutta RC, Dey M, Dutta AK, Basu B. Competent processing techniques for scaffolds in tissue engineering. Biotechnol Adv 2017;35:240–50. https://doi.org/10.1016/j.biotechadv.2017.01.001.
• [110] Lu T, Li Y, Chen T. Techniques for fabrication and construction of three-dimensional scaffolds for tissue engineering. Int J Nanomed 2013;8:337–50.
• [111] Kim JW, Shin KH, Koh YH, Hah MJ, Moon J, Kim HE. Production of Poly(e-Caprolactone)/Hydroxyapatite composite scaffolds with a tailored macro/micro-porous structure, high mechanical properties, and excellent bioactivity. Materials 10(10):1-13. https://doi.org/10.3390/ma10101123.
• [112] Plisko TV, Penkova AV, Burts KS, Bildyukevich AV, Dmitrenko ME, Melnikova GB, et al. Effect of Pluronic F127 on porous and dense membrane structure formation via non-solvent induced and evaporation induced phase separation. J Membr Sci 2019;580:336–49. https://doi.org/10.1016/j.memsci.2019.03.028.
• [113] Mannella GA, Conoscenti G, Pavia FC, La CV, Brucato V. Preparation of polymeric foams with a pore size gradient via Thermally Induced Phase Separation (TIPS). Mater Lett 2015;160:31–3. https://doi.org/10.1016/j.matlet.2015.07.055.
• [114] Sultana N, Hassana MI, Ridzuana N, Ibrahima Z, Soonc CF. Fabrication of gelatin scaffolds using thermally induced phase separation technique. Int J Eng 2018;31:1302–7.
• [115] Buzarovska A, Gualandi C, Parrilli A, Scandola M. Effect of TiO2 nanoparticle loading on Poly(L-lactic acid) porous scaffolds fabricated by TIPS. Compos B 2015;81:189–95. https://doi.org/10.1016/j.compositesb.2015.07.016.
• [116] Semitela  , Girão AF, Fernandes C, Ramalho G, Bdikin I, Completo A, et al. Electrospinning of bioactive polycaprolactone-gelatin nanofibres with increased pore size for cartilage tissue engineering applications. J Biomater Appl 2020;35:471–84. https://doi.org/10.1177/0885328220940194.
• [117] Sharifi F, Irani S, Azadegan G, Pezeshki-modaress M. Coelectrospun gelatin-chondroitin sulfate/polycaprolactone nanofibrous scaffolds for cartilage tissue engineering. Bioactive Carbohydrates Dietary Fibre 2020;22:100215. https://doi.org/10.1016/j.bcdf.2020.100215.
• [118] Zhou Y, Chyu J, Zumwalt M. Recent progress of fabrication of cell scaffold by electrospinning technique for articular cartilage tissue engineering. Int J Biomater 2018;2018:1–10. https://doi.org/10.1155/2018/1953636.
• [119] Canton TT, Kunert LR, Suellen B, Ana I, Serafini P. Nonwoven membranes for tissue engineering: an overview of cartilage, epithelium, and bone regeneration. J Biomater Sci Polym Ed 2019;30:1026–49. https://doi.org/10.1080/09205063.2019.1620592.
• [120] Girão AF, Semitela Â, Ramalho G, Completo A, Marques PAAP. Mimicking nature-fabrication of 3D anisotropic electrospun polycaprolactone scaffolds for cartilage tissue engineering applications. Compos B 2018;154:99–107. https://doi.org/10.1016/j.compositesb.2018.08.001.
• [121] Li K, Wang D, Zhao K, Song K, Liang J. Electrohydrodynamic jet 3D printing of PCL/PVP composite scaffold for cell culture. Talanta 2020;211:1–11. https://doi.org/10.1016/j.talanta.2020.120750.
• [122] Baena JM, Jiménez G, López-Ruiz E, Antich C, Griñán-Lisón C, Perán M, et al. Volume-by-volume bioprinting of chondrocytes-alginate bioinks in high temperature thermoplastic scaffolds for cartilage regeneration. Exp Biol Med 2019;244:13–21. https://doi.org/10.1177/1535370218821128.
• [123] Markstedt K, Mantas A, Tournier I, Martínez Ávila H, Hägg D, Gatenholm P. 3D bioprinting human chondrocytes with nanocellulose - alginate bioink for cartilage tissue engineering applications. Biomacromolecules 2015;16:1489–96. https://doi.org/10.1021/acs.biomac.5b00188.
• [124] Daly AC, Freeman FE, Gonzalez-fernandez T, Critchley SE, Nulty J, Kelly DJ. 3D bioprinting for cartilage and osteochondral tissue engineering. Adv Healthcare Mater 2017;6:1–20. https://doi.org/10.1002/adhm.201700298.
• [125] Seung J, Sang H, Jung H, Lee H, Hong H, Jin Y, et al. 3D-printable photocurable bioink for cartilage regeneration of tonsil-derived mesenchymal stem cells. Additive Manuf 2020;33:101136. https://doi.org/10.1016/j.addma.2020.101136.
• [126] Wu J, Yang R, Zheng J, Pan L, Liu X. Fabrication and improvement of PCL/alginate/PAAm scaffold via selective laser sintering for tissue engineering. Micro Nano Lett 2019;14(8):852–5. https://doi.org/10.1049/mnl.2018.5806.
• [127] Chen C, Shyu VB, Chen J, Lee M. Selective laser sintered poly-e-caprolactone scaffold hybridized with collagen hydrogel for cartilage tissue engineering. Biofabrication 2014;6(1):1–11. https://doi.org/10.1088/1758-5082/6/1/015004.
• [128] Longley R, Ferreira AM, Gentile P. Recent approaches to the manufacturing of biomimetic multi-phasic scaffolds for osteochondral regeneration. Mol Sci 2018;19(6):1–17. https://doi.org/10.3390/ijms19061755.
• [129] Benwood C, Anstey A, Andrzejweski J, Misra M, Mohanty AK. Improving the impact strength and heat resistance of 3D printed models: structure, property, and processing correlationships during fused deposition modeling (FDM) of poly(lactic acid). Am Chem Soc Omega 2018;3(4):4400–11. https://doi.org/10.1021/acsomega.8b00129.
• [130] Cheng A, Schwartz Z, Kahn A, Li X, Shao Z, Sun M, et al. Advances in porous scaffold design for bone and cartilage tissue engineering and regeneration. Tissue Eng Part B 2019;25(1):14–29. https://doi.org/10.1089/ten.TEB.2018.0119.
• [131] Abdelaal OAM, Darwish SMH. Review of rapid prototyping techniques for tissue engineering scaffolds fabrication. Adv Struct Mater 2013;29:33–54. https://doi.org/10.1007/978-3-642-31470-4.
• [132] Chen W, Xu Y, Liu Y, Wang Z, Li Y, Jiang G, et al. Three-dimensional printed electrospun fiber-based scaffold for cartilage regeneration. Mater Des 2019;179:107886.
• [133] Xu T, Binder KW, Albanna MZ, Dice D, Zhao W, Yoo JJ, et al. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication 2013;5(1):1–10. https://doi.org/10.1088/1758-5082/5/1/015001.
• [134] Garrigues NW, Little D, Sanchez-adams J, Ruch DS, Guilak F. Electrospun cartilage-derived matrix scaffolds for cartilage tissue engineering. J Biomed Mater Res Part A 2014;102:3998–4008. https://doi.org/10.1002/jbm.a.35068.
• [135] Correa D, Lietman SA. Articular cartilage repair: current needs, methods and research directions. Semin Cell Dev Biol 2017;62:67–77. https://doi.org/10.1016/j.semcdb.2016.07.013.
• [136] Hoffman AS. Hydrogels for biomedical applications. Adv Drug Deliv Rev 2012;64:18–23. https://doi.org/10.1016/j.addr.2012.09.010.
• [137] Janoušková O. Synthetic polymer scaffolds for soft tissue engineering department of biological models. Physiol Res 2018;67(2):335–48. https://doi.org/10.33549/physiolres.933983.
• [138] Bistolfi A, Ferracini R, Galletta C, Tosto F, Sgarminato V, Digo E, et al. Regeneration of articular cartilage: scaffold used in orthopedic surgery. A short handbook of available products for regenerative joints surgery. Clin Sci Res Rep 2017;1:1–7. https://doi.org/10.15761/CSRR.1000101.
• [139] Urbanek O, Kołbuk D, Wróbel M. Articular cartilage: new directions and barriers of scaffolds development – review. Int J Polym Mater Polym Biomater 2019;68:1–15. https://doi.org/10.1080/00914037.2018.1452224.
• [140] Brittberg M, Recker D, Ilgenfritz J, Saris DBF. Matrix-Applied characterized autologous cultured chondrocytes versus microfracture: five-year follow-up of a prospective randomized trial. Am J Sports Med 2018;46:1343–51. https://doi.org/10.1177/0363546518756976.
• [141] Kreuz PC, Müller S, Freymann U, Erggelet C, Niemeyer P, Kaps C, et al. Repair of focal cartilage defects with scaffold-assisted autologous chondrocyte grafts. Am J Sports Med 2011;39:1697–706. https://doi.org/10.1177/0363546511403279.
• [142] Siclari A, Mascaro G, Kaps C, Boux E. A 5-year follow-up after cartilage repair in the knee using a platelet-rich plasma-immersed polymer-based implant. Open Orthop J 2014;8:346–54.
• [143] Plończak M, Czubak J, Hoser G, Chwojnowskl A, Kawiak J, Dudziński K, et al. Repair of articular cartilage full thickness defects with cultured chondrocytes placed on polysulphonic membrane - experimental studies in rabbits. Biocyber Biomed Eng 2008;28:87–93.
• [144] Płończak M, Czubak J. Culture of human autologous chondrocytes on polysulphonic membrane – preliminary studies. Biocyber Biomed Eng 2012;32(3):63–7. https://doi.org/10.1016/S0208-5216(12)70042-6.
• [145] Płończak M. The value of autogenous cartilage cell transplants in the experimental treatment of articular cartilage defects in rabbits [in Polish]. In: doctoral thesis, Poland: Otwock; 2008.
• [146] Tsai M, Hung K, Hung S, Hsu S. Evaluation of biodegradable elastic scaffolds made of anionic polyurethane for cartilage tissue engineering. Colloids Surf, B 2015;125:34–44. https://doi.org/10.1016/j.colsurfb.2014.11.003.
• [147] Liao J, Qu Y, Chu B, Zhang X, Qian Z. Biodegradable CSMA/PECA/graphene porous hybrid scaffold for cartilage tissue engineering. Sci Rep 2015;9879:1–16. https://doi.org/10.1038/srep09879.
• [148] Setayeshmehr M, Esfandiari E, Hashemibeni B, Tavakoli AH, Rafienia M, Samadikuchaksaraei A, et al. Chondrogenesis of human adipose-derived mesenchymal stromal cells on the [devitalized costal cartilage matrix/poly(vinylalcohol)/fibrin] hybrid scaffolds. Eur Polym J2019;118:528–41. https://doi.org/10.1016/j.eurpolymj.2019.04.044.
• [149] He Y, LiuW, Guan L, Chen J, Duan L, Jia Z, et al. A 3D-printed PLCL scaffold coated with collagen type I and its biocompatibility. Biomed Res Int 2018;2018:1–10. https://doi.org/10.1155/2018/5147156.
• [150] Rofiqoh N, Putri E, Wang X, Chen Y, Li X, Kawazoe N, et al. Preparation of PLGA-collagen hybrid scaffolds with controlled pore structures for cartilage tissue engineering. Prog Nat Sci: Mater Int 2020;30:642–50. https://doi.org/10.1016/j.pnsc.2020.07.003.
• [151] Nogami M, Kimura T, Seki S, Matsui Y, Yoshida T, Koike-Soko C, et al. A human amnion-derived extracellular matrix-coated cell-free scaffold for cartilage repair- in vitro and in vivo studies. Tissue Eng Part A 2016;22(7-8):680–8. https://doi.org/10.1089/ten.TEA.2015.0285.
• [152] Kamath SM, Jaison D, Krishna S, Sridhar K, Kasthuri N, Gopinath V, et al. In vitro augmentation of chondrogenesis by Epigallocatechin gallate in primary Human chondrocytes - sustained release model for cartilage regeneration. J Drug Deliv Sci Technol 2020;60. https://doi.org/10.1016/j.jddst.2020.101992.
• [153] So C, Silva JC, Fernandes PR, Lobato C, Manuel J, Cabral S, et al. Chondrogenic differentiation of mesenchymal stem/stromal cells on 3D porous poly (e-caprolactone) scaffolds: effects of material alkaline treatment and chondroitin sulfate supplementation. J Biosci Bioeng 2020;129:756–64. https://doi.org/10.1016/j.jbiosc.2020.01.004.
• [154] Denis P, Dulnik J, Sajkiewicz P. Electrospinning and structure of bicomponent polycaprolactone/gelatin nanofibers obtained using alternative solvent system. Int J Polymeric Mater Polymeric Biomater 2015;64:354–64. https://doi.org/10.1080/00914037.2014.945208.
• [155] Dulnik J, Ko D, Denis P, Sajkiewicz P. The effect of a solvent on cellular response to PCL/gelatin and PCL/collagen electrospun nano fibres. Eur Polym J 2018;104:147–56. https://doi.org/10.1016/j.eurpolymj.2018.05.010.
• [156] Chwojnowski A, Kruk A, Wojciechowski C, Łukowska E, Dulnik J, Sajkiewicz P. The dependence of the membrane structure on the non-woven forming the macropores in the 3D scaffolds preparation. Desalin Water Treat 2017;64:324–31. https://doi.org/10.5004/dwt.2017.11394.
• [157] Chwojnowski A, Dudziński K. Method for producing semipermeable polysulfone and polyethersulfone membranes and their applications, PL 211793 B1, 2012.
• [158] Kruk A, Gadomska-Gajadhur A, Ruśkowski P, Chwojnowski A, Dulnik J, Synoradzki L. Preparation of biodegradable semi-permeable membranes as 3D scaffolds for cell cultures. Desalin Water Treat 2017;64:317–23. https://doi.org/10.5004/dwt.2017.11415.
• [159] Gadomska-Gajadhur A, Kruk A, Synoradzki L, Chwojnowski A. Patent PL 229497 B1; Method for producing three-dimensional polylactide scaffolds, 2015.
• [160] Ho ST, Hutmacher DW. A comparison of micro CT with other techniques used in the characterization of scaffolds. Biomaterials 2006;27:1362–76. https://doi.org/10.1016/j.biomaterials.2005.08.035.
• [161] Oh SH, Kim TH, Il IG, Lee JH. Investigation of pore size effect on chondrogenic differentiation of adipose stem cells using a pore size gradient scaffold. Biomacromolecules 2010;11:1948–55. https://doi.org/10.1021/bm100199m.
• [162] van Susante JLC, Pieper J, Buma P, van Kuppevelt TH, van Beuningen H, van der Kraan PM, et al. Linkage of chondroitin-sulfate to type I collagen scaffolds stimulates the bioactivity of seeded chondrocytes in vitro. Biomaterials 2001;22:2359–69. https://doi.org/10.1016/S0142-9612(00)00423-3.
• [163] Narumi K, Furugen A, Kobayashi M, Otake S, Itagaki S, Iseki K. Regulation of monocarboxylate transporter 1 in skeletal muscle cells by intracellular signaling pathways. Biol Pharm Bull 2010;33:1568–73. https://doi.org/10.1248/bpb.33.1568.