Recent Advancements in 3D Printing of Polysaccharide Hydrogels in Cartilage Tissue Engineering
Abstract
:1. Introduction
2. Materials and Methods
3. 3D Printing of Hydrogels in CTE
3.1. Polysaccharides-Based Hydrogels for 3D Printing in CTE
3.1.1. Alginate Hydrogels for CTE
3.1.2. Agarose Hydrogels for CTE
3.1.3. Chitosan Hydrogels for CTE
3.1.4. Hydrogels from Cellulose Derivatives for CTE
3.1.5. Hyaluronic Acid (HA) Hydrogels for CTE
3.1.6. Dextran Hydrogels for CTE
4. Cell Source for Cartilage Tissue Engineering (CTE)
5. Further Consideration—Crucial Testing Methods for an Effective Translation from CTE Research to Clinical Practice
6. Conclusion and Future Perspective of 3D Printing of Polysaccharide–Protein-Based Hydrogels
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Eftekhari, A.; Maleki Dizaj, S.; Sharifi, S.; Salatin, S.; Rahbar Saadat, Y.; Zununi Vahed, S.; Samiei, M.; Ardalan, M.; Rameshrad, M.; Ahmadian, E.; et al. The Use of Nanomaterials in Tissue Engineering for Cartilage Regeneration; Current Approaches and Future Perspectives. Int. J. Mol. Sci. 2020, 21, 536. [Google Scholar] [CrossRef] [Green Version]
- Del Bakhshayesh, A.R.; Asadi, N.; Alihemmati, A.; Tayefi Nasrabadi, H.; Montaseri, A.; Davaran, S.; Saghati, S.; Akbarzadeh, A.; Abedelahi, A. An Overview of Advanced Biocompatible and Biomimetic Materials for Creation of Replacement Structures in the Musculoskeletal Systems: Focusing on Cartilage Tissue Engineering. J. Biol. Eng. 2019, 13, 85. [Google Scholar] [CrossRef] [Green Version]
- Rai, V.; Dilisio, M.F.; Dietz, N.E.; Agrawal, D.K. Recent Strategies in Cartilage Repair: A Systemic Review of the Scaffold Development and Tissue Engineering. J. Biomed. Mater. Res. A 2017, 105, 2343–2354. [Google Scholar] [CrossRef] [PubMed]
- Lammi, M.J.; Piltti, J.; Prittinen, J.; Qu, C. Challenges in Fabrication of Tissue-Engineered Cartilage with Correct Cellular Colonization and Extracellular Matrix Assembly. Int. J. Mol. Sci. 2018, 19, 2700. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perez, R.A.; Mestres, G. Role of Pore Size and Morphology in Musculo-Skeletal Tissue Regeneration. Mater. Sci. Eng. C Mater. Biol. Appl. 2016, 61, 922–939. [Google Scholar] [CrossRef]
- Tran, H.D.N.; Park, K.D.; Ching, Y.C.; Huynh, C.; Nguyen, D.H. A Comprehensive Review on Polymeric Hydrogel and Its Composite: Matrices of Choice for Bone and Cartilage Tissue Engineering. J. Ind. Eng. Chem. 2020, 89, 58–82. [Google Scholar] [CrossRef]
- Billiet, T.; Vandenhaute, M.; Schelfhout, J.; Van Vlierberghe, S.; Dubruel, P. A Review of Trends and Limitations in Hydrogel-Rapid Prototyping for Tissue Engineering. Biomaterials 2012, 33, 6020–6041. [Google Scholar] [CrossRef]
- De Mori, A.; Peña Fernández, M.; Blunn, G.; Tozzi, G.; Roldo, M. 3D Printing and Electrospinning of Composite Hydrogels for Cartilage and Bone Tissue Engineering. Polymers 2018, 10, 285. [Google Scholar] [CrossRef] [Green Version]
- Hospodiuk, M.; Dey, M.; Sosnoski, D.; Ozbolat, I.T. The Bioink: A Comprehensive Review on Bioprintable Materials. Biotechnol. Adv. 2017, 35, 217–239. [Google Scholar] [CrossRef] [Green Version]
- Mandrycky, C.; Wang, Z.; Kim, K.; Kim, D.-H. 3D Bioprinting for Engineering Complex Tissues. Biotechnol. Adv. 2016, 34, 422–434. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Heid, S.; Boccaccini, A.R. Advancing Bioinks for 3D Bioprinting Using Reactive Fillers: A Review. Acta Biomater. 2020, 113, 1–22. [Google Scholar] [CrossRef] [PubMed]
- Abdulghani, S.; Morouço, P.G. Biofabrication for Osteochondral Tissue Regeneration: Bioink Printability Requirements. J. Mater. Sci. Mater. Med. 2019, 30, 20. [Google Scholar] [CrossRef] [PubMed]
- Hoffman, A.S. Hydrogels for Biomedical Applications. Adv. Drug Deliv. Rev. 2012, 64, 18–23. [Google Scholar] [CrossRef]
- Zhao, W.; Jin, X.; Cong, Y.; Liu, Y.; Fu, J. Degradable Natural Polymer Hydrogels for Articular Cartilage Tissue Engineering. J. Chem. Technol. Biotechnol. 2013, 88, 327–339. [Google Scholar] [CrossRef]
- Wu, D.; Yu, Y.; Tan, J.; Huang, L.; Luo, B.; Lu, L.; Zhou, C. 3D Bioprinting of Gellan Gum and Poly (Ethylene Glycol) Diacrylate Based Hydrogels to Produce Human-Scale Constructs with High-Fidelity. Mater. Des. 2018, 160, 486–495. [Google Scholar] [CrossRef]
- Oliveira, J.T.; Reis, R.L. Polysaccharide-Based Materials for Cartilage Tissue Engineering Applications. J. Tissue Eng. Regen. Med. 2011, 5, 421–436. [Google Scholar] [CrossRef]
- Chen, F.-M.; Liu, X. Advancing Biomaterials of Human Origin for Tissue Engineering. Prog. Polym. Sci. 2016, 53, 86–168. [Google Scholar] [CrossRef] [Green Version]
- Lim, Y.-S.; Ok, Y.-J.; Hwang, S.-Y.; Kwak, J.-Y.; Yoon, S. Marine Collagen as A Promising Biomaterial for Biomedical Applications. Mar. Drugs 2019, 17, 467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raftery, R.M.; Woods, B.; Marques, A.L.P.; Moreira-Silva, J.; Silva, T.H.; Cryan, S.-A.; Reis, R.L.; O’Brien, F.J. Multifunctional Biomaterials from the Sea: Assessing the Effects of Chitosan Incorporation into Collagen Scaffolds on Mechanical and Biological Functionality. Acta Biomater. 2016, 43, 160–169. [Google Scholar] [CrossRef] [Green Version]
- Naghieh, S.; Sarker, M.D.; Sharma, N.K.; Barhoumi, Z.; Chen, X. Printability of 3D Printed Hydrogel Scaffolds: Influence of Hydrogel Composition and Printing Parameters. Appl. Sci. 2020, 10, 292. [Google Scholar] [CrossRef] [Green Version]
- Radhakrishnan, J.; Subramanian, A.; Krishnan, U.; Sethuraman, S. Injectable and 3D Bioprinted Polysaccharide Hydrogels: From Cartilage to Osteochondral Tissue Engineering. Biomacromolecules 2016, 18, 1–26. [Google Scholar] [CrossRef]
- Zhu, J.; Marchant, R.E. Design Properties of Hydrogel Tissue-Engineering Scaffolds. Expert Rev. Med. Devices 2011, 8, 607–626. [Google Scholar] [CrossRef]
- Sánchez-Téllez, D.A.; Téllez-Jurado, L.; Rodríguez-Lorenzo, L.M. Hydrogels for Cartilage Regeneration, from Polysaccharides to Hybrids. Polymers 2017, 9, 671. [Google Scholar] [CrossRef] [Green Version]
- Nikolova, M.P.; Chavali, M.S. Recent Advances in Biomaterials for 3D Scaffolds: A Review. Bioact. Mater. 2019, 4, 271–292. [Google Scholar] [CrossRef] [PubMed]
- Catoira, M.C.; Fusaro, L.; Di Francesco, D.; Ramella, M.; Boccafoschi, F. Overview of Natural Hydrogels for Regenerative Medicine Applications. J. Mater. Sci. Mater. Med. 2019, 30, 115. [Google Scholar] [CrossRef] [Green Version]
- Hollister, S.; Hollister, S.J. Porous Scaffold Design for Tissue Engineering. Nat. Mater. 2005, 4, 518–524. [Google Scholar] [CrossRef]
- Nia, H.T.; Bozchalooi, I.S.; Li, Y.; Han, L.; Hung, H.-H.; Frank, E.; Youcef-Toumi, K.; Ortiz, C.; Grodzinsky, A. High-Bandwidth AFM-Based Rheology Reveals That Cartilage Is Most Sensitive to High Loading Rates at Early Stages of Impairment. Biophys. J. 2013, 104, 1529–1537. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cigan, A.D.; Roach, B.L.; Nims, R.J.; Tan, A.R.; Albro, M.B.; Stoker, A.M.; Cook, J.L.; Vunjak-Novakovic, G.; Hung, C.T.; Ateshian, G.A. High Seeding Density of Human Chondrocytes in Agarose Produces Tissue-Engineered Cartilage Approaching Native Mechanical and Biochemical Properties. J. Biomech. 2016, 49, 1909–1917. [Google Scholar] [CrossRef] [Green Version]
- López-Marcial, G.; Zeng, A.; Osuna, C.; Dennis, J.; Garcia, J.; O’Connell, G. Agarose-Based Hydrogels as Suitable Bioprinting Materials for Tissue Engineering. ACS Biomater. Sci. Eng. 2018, 4, 3610–3616. [Google Scholar] [CrossRef]
- Sultankulov, B.; Berillo, D.; Sultankulova, K.; Tokay, T.; Saparov, A. Progress in the Development of Chitosan-Based Biomaterials for Tissue Engineering and Regenerative Medicine. Biomolecules 2019, 9, 470. [Google Scholar] [CrossRef] [Green Version]
- Fan, Y.; Shi, T.; Yue, X.; Sun, F.; Yao, D. 3D Composite Cell Printing Gelatin/Sodium Alginate/n-HAP Bioscaffold. J. Phys. Conf. Ser. 2019, 1213, 042020. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Wu, C.; Chu, P.K.; Gelinsky, M. 3D Printing of Hydrogels: Rational Design Strategies and Emerging Biomedical Applications. Mater. Sci. Eng. R Rep. 2020, 140, 100543. [Google Scholar] [CrossRef]
- Lee, N.K.; Oh, H.J.; Hong, C.M.; Suh, H.; Hong, S.H. Comparison of the Synthetic Biodegradable Polymers, Polylactide (PLA), and Polylactic-Co-Glycolic Acid (PLGA) as Scaffolds for Artificial Cartilage. Biotechnol. Bioprocess Eng. 2009, 14, 180–186. [Google Scholar] [CrossRef]
- Dai, W.; Kawazoe, N.; Lin, X.; Dong, J.; Chen, G. The Influence of Structural Design of PLGA/Collagen Hybrid Scaffolds in Cartilage Tissue Engineering. Biomaterials 2010, 31, 2141–2152. [Google Scholar] [CrossRef]
- Gungor-Ozkerim, P.S.; Inci, I.; Zhang, Y.S.; Khademhosseini, A.; Dokmeci, M.R. Bioinks for 3D Bioprinting: An Overview. Biomater. Sci. 2018, 6, 915–946. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Daly, A.C.; Freeman, F.E.; Gonzalez-Fernandez, T.; Critchley, S.E.; Nulty, J.; Kelly, D.J. 3D Bioprinting for Cartilage and Osteochondral Tissue Engineering. Adv. Healthc. Mater. 2017, 6, 1700298. [Google Scholar] [CrossRef]
- Vega, S.L.; Kwon, M.Y.; Burdick, J.A. Recent Advances in Hydrogels for Cartilage Tissue Engineering. Eur. Cell. Mater. 2017, 33, 59–75. [Google Scholar] [CrossRef] [PubMed]
- Yanagawa, F.; Sugiura, S.; Kanamori, T. Hydrogel Microfabrication Technology toward Three Dimensional Tissue Engineering. Regen. Ther. 2016, 3, 45–57. [Google Scholar] [CrossRef] [Green Version]
- Jang, T.-S.; Jung, H.-D.; Pan, H.M.; Han, W.T.; Chen, S.; Song, J. 3D Printing of Hydrogel Composite Systems: Recent Advances in Technology for Tissue Engineering. Int. J. Bioprinting 2018, 4, 126. [Google Scholar] [CrossRef]
- Tamay, D.G.; Dursun Usal, T.; Alagoz, A.S.; Yucel, D.; Hasirci, N.; Hasirci, V. 3D and 4D Printing of Polymers for Tissue Engineering Applications. Front. Bioeng. Biotechnol. 2019, 7, 164. [Google Scholar] [CrossRef]
- Semba, J.A.; Mieloch, A.A.; Rybka, J.D. Introduction to the State-of-the-Art 3D Bioprinting Methods, Design, and Applications in Orthopedics. Bioprinting 2020, 18, e00070. [Google Scholar] [CrossRef]
- Bian, L. Functional Hydrogel Bioink, a Key Challenge of 3D Cellular Bioprinting. APL Bioeng. 2020, 4, 030401. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, S.; Patil, R.; Bahadur, P. Polysaccharide Based Scaffolds for Soft Tissue Engineering Applications. Polymers 2018, 11, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, W.; Li, J.; Qi, X.; Zhong, Y.; Zuo, G.; Pan, X.; Su, T.; Zhang, J.; Dong, W. Synthesis and Characterization of a Multi-Sensitive Polysaccharide Hydrogel for Drug Delivery. Carbohydr. Polym. 2017, 177, 275–283. [Google Scholar] [CrossRef]
- Zhu, T.; Mao, J.; Cheng, Y.; Liu, H.; Lv, L.; Ge, M.; Li, S.; Huang, J.; Chen, Z.; Li, H.; et al. Recent Progress of Polysaccharide-Based Hydrogel Interfaces for Wound Healing and Tissue Engineering. Adv. Mater. Interfaces 2019, 6, 1900761. [Google Scholar] [CrossRef] [Green Version]
- Afewerki, S.; Sheikhi, A.; Kannan, S.; Ahadian, S.; Khademhosseini, A. Gelatin-Polysaccharide Composite Scaffolds for 3D Cell Culture and Tissue Engineering: Towards Natural Therapeutics. Bioeng. Transl. Med. 2019, 4, 96–115. [Google Scholar] [CrossRef]
- Cassimjee, H.; Kumar, P.; Choonara, Y.E.; Pillay, V. Proteosaccharide Combinations for Tissue Engineering Applications. Carbohydr. Polym. 2020, 235, 115932. [Google Scholar] [CrossRef]
- Noh, I.; Kim, N.; Tran, H.N.; Lee, J.; Lee, C. 3D Printable Hyaluronic Acid-Based Hydrogel for Its Potential Application as a Bioink in Tissue Engineering. Biomater. Res. 2019, 23, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henrionnet, C.; Pourchet, L.; Neybecker, P.; Messaoudi, O.; Gillet, P.; Loeuille, D.; Mainard, D.; Marquette, C.; Pinzano, A. Combining Innovative Bioink and Low Cell Density for the Production of 3D-Bioprinted Cartilage Substitutes: A Pilot Study. Stem Cells Int. 2020, 2020, 2487072. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, S.-H.; Song, T.; Bae, T.S.; Khang, G.; Choi, B.H.; Park, S.; Min, B.-H. Synergistic Effects of Alginate Coating Method on Cartilage Tissue Engineering Using Fibrin/HA Composite Gel. Int. J. Precis. Eng. Manuf. 2012, 13, 2067–2074. [Google Scholar] [CrossRef]
- García-Martínez, L.; Campos, F.; Godoy-Guzmán, C.; del Carmen Sánchez-Quevedo, M.; Garzón, I.; Alaminos, M.; Campos, A.; Carriel, V. Encapsulation of Human Elastic Cartilage-Derived Chondrocytes in Nanostructured Fibrin-Agarose Hydrogels. Histochem. Cell Biol. 2017, 147, 83–95. [Google Scholar] [CrossRef] [PubMed]
- Lin, H.; Beck, A.M.; Shimomura, K.; Sohn, J.; Fritch, M.R.; Deng, Y.; Kilroy, E.J.; Tang, Y.; Alexander, P.G.; Tuan, R.S. Optimization of Photocrosslinked Gelatin/Hyaluronic Acid Hybrid Scaffold for the Repair of Cartilage Defect. J. Tissue Eng. Regen. Med. 2019, 13, 1418–1429. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.J.; Kim, K.K.; Park, I.K.; Choi, B.S.; Kim, J.H.; Kim, M.S. Hybrid Scaffolds Composed of Hyaluronic Acid and Collagen for Cartilage Regeneration. Tissue Eng. Regen. Med. 2012, 9, 57–62. [Google Scholar] [CrossRef]
- Axpe, E.; Oyen, M.L. Applications of Alginate-Based Bioinks in 3D Bioprinting. Int. J. Mol. Sci. 2016, 17, 1976. [Google Scholar] [CrossRef] [Green Version]
- Lee, K.Y.; Mooney, D.J. Alginate: Properties and Biomedical Applications. Prog. Polym. Sci. 2012, 37, 106–126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Unagolla, J.M.; Jayasuriya, A.C. Hydrogel-Based 3D Bioprinting: A Comprehensive Review on Cell-Laden Hydrogels, Bioink Formulations, and Future Perspectives. Appl. Mater. Today 2020, 18, 100479. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Li, Q.; Xu, S.; Zheng, Q.; Cao, X. Preparation and Properties of 3D Printed Alginate–Chitosan Polyion Complex Hydrogels for Tissue Engineering. Polymers 2018, 10, 664. [Google Scholar] [CrossRef] [Green Version]
- Rathan, S.; Dejob, L.; Schipani, R.; Haffner, B.; Möbius, M.E.; Kelly, D.J. Fiber Reinforced Cartilage ECM Functionalized Bioinks for Functional Cartilage Tissue Engineering. Adv. Healthc. Mater. 2019, 8, 1801501. [Google Scholar] [CrossRef] [PubMed]
- Maver, U.; Gradišnik, L.; Smrke, D.M.; Stana Kleinschek, K.; Maver, T. Impact of Growth Factors on Wound Healing in Polysaccharide Blend Thin Films. Appl. Surf. Sci. 2019, 489, 485–493. [Google Scholar] [CrossRef]
- Daly, A.C.; Cunniffe, G.M.; Sathy, B.N.; Jeon, O.; Alsberg, E.; Kelly, D.J. 3D Bioprinting of Developmentally Inspired Templates for Whole Bone Organ Engineering. Adv. Healthc. Mater. 2016, 5, 2353–2362. [Google Scholar] [CrossRef]
- Stana, J.; Stergar, J.; Gradišnik, L.; Flis, V.; Kargl, R.; Fröhlich, E.; Stana Kleinschek, K.; Mohan, T.; Maver, U. Multilayered Polysaccharide Nanofilms for Controlled Delivery of Pentoxifylline and Possible Treatment of Chronic Venous Ulceration. Biomacromolecules 2017, 18, 2732–2746. [Google Scholar] [CrossRef]
- Ma, K.; Titan, A.L.; Stafford, M.; Zheng, C.H.; Levenston, M.E. Variations in Chondrogenesis of Human Bone Marrow-Derived Mesenchymal Stem Cells in Fibrin/Alginate Blended Hydrogels. Acta Biomater. 2012, 8, 3754–3764. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, T.; Gillispie, G.J.; Copus, J.S.; Pr, A.K.; Seol, Y.-J.; Atala, A.; Yoo, J.J.; Lee, S.J. Optimization of Gelatin-Alginate Composite Bioink Printability Using Rheological Parameters: A Systematic Approach. Biofabrication 2018, 10, 034106. [Google Scholar] [CrossRef]
- Yang, X.; Lu, Z.; Wu, H.; Li, W.; Zheng, L.; Zhao, J. Collagen-Alginate as Bioink for Three-Dimensional (3D) Cell Printing Based Cartilage Tissue Engineering. Mater. Sci. Eng. C Mater. Biol. Appl. 2018, 83, 195–201. [Google Scholar] [CrossRef] [PubMed]
- Müller, M.; Öztürk, E.; Arlov, Ø.; Gatenholm, P.; Zenobi-Wong, M. Alginate Sulfate-Nanocellulose Bioinks for Cartilage Bioprinting Applications. Ann. Biomed. Eng. 2017, 45, 210–223. [Google Scholar] [CrossRef]
- 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, 1489–1496. [Google Scholar] [CrossRef]
- Zarrintaj, P.; Manouchehri, S.; Ahmadi, Z.; Saeb, M.R.; Urbanska, A.M.; Kaplan, D.L.; Mozafari, M. Agarose-Based Biomaterials for Tissue Engineering. Carbohydr. Polym. 2018, 187, 66–84. [Google Scholar] [CrossRef] [PubMed]
- Salati, M.A.; Khazai, J.; Tahmuri, A.M.; Samadi, A.; Taghizadeh, A.; Taghizadeh, M.; Zarrintaj, P.; Ramsey, J.D.; Habibzadeh, S.; Seidi, F.; et al. Agarose-Based Biomaterials: Opportunities and Challenges in Cartilage Tissue Engineering. Polymers 2020, 12, 1150. [Google Scholar] [CrossRef]
- Yin, Z.; Yang, X.; Jiang, Y.; Xing, L.; Xu, Y.; Lu, Y.; Ding, P.; Ma, J.; Xu, Y.; Gui, J. Platelet-Rich Plasma Combined with Agarose as a Bioactive Scaffold to Enhance Cartilage Repair: An in Vitro Study. J. Biomater. Appl. 2014, 28, 1039–1050. [Google Scholar] [CrossRef]
- Singh, Y.P.; Bhardwaj, N.; Mandal, B.B. Potential of Agarose/Silk Fibroin Blended Hydrogel for in Vitro Cartilage Tissue Engineering. ACS Appl. Mater. Interfaces 2016, 8, 21236–21249. [Google Scholar] [CrossRef]
- Sadeghianmaryan, A.; Naghieh, S.; Alizadeh Sardroud, H.; Yazdanpanah, Z.; Afzal Soltani, Y.; Sernaglia, J.; Chen, X. Extrusion-Based Printing of Chitosan Scaffolds and Their in Vitro Characterization for Cartilage Tissue Engineering. Int. J. Biol. Macromol. 2020, 164, 3179–3192. [Google Scholar] [CrossRef]
- Ye, K.; Felimban, R.; Traianedes, K.; Moulton, S.E.; Wallace, G.G.; Chung, J.; Quigley, A.; Choong, P.F.M.; Myers, D.E. Chondrogenesis of Infrapatellar Fat Pad Derived Adipose Stem Cells in 3D Printed Chitosan Scaffold. PLoS ONE 2014, 9, e99410. [Google Scholar] [CrossRef]
- He, Y.; Derakhshanfar, S.; Zhong, W.; Li, B.; Lu, F.; Xing, M.; Li, X.; Licoccia, S. Characterization and Application of Carboxymethyl Chitosan-Based Bioink in Cartilage Tissue Engineering. J. Nanomater. 2020, 2020, 2057097. [Google Scholar] [CrossRef]
- Huang, Y.; Seitz, D.; König, F.; Müller, P.E.; Jansson, V.; Klar, R.M. Induction of Articular Chondrogenesis by Chitosan/Hyaluronic-Acid-Based Biomimetic Matrices Using Human Adipose-Derived Stem Cells. Int. J. Mol. Sci. 2019, 20, 4487. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, D.; Hägg, D.A.; Forsman, A.; Ekholm, J.; Nimkingratana, P.; Brantsing, C.; Kalogeropoulos, T.; Zaunz, S.; Concaro, S.; Brittberg, M.; et al. Cartilage Tissue Engineering by the 3D Bioprinting of IPS Cells in a Nanocellulose/Alginate Bioink. Sci. Rep. 2017, 7, 658. [Google Scholar] [CrossRef]
- Hodder, E.; Duin, S.; Kilian, D.; Ahlfeld, T.; Seidel, J.; Nachtigall, C.; Bush, P.; Covill, D.; Gelinsky, M.; Lode, A. Investigating the Effect of Sterilisation Methods on the Physical Properties and Cytocompatibility of Methyl Cellulose Used in Combination with Alginate for 3D-Bioplotting of Chondrocytes. J. Mater. Sci. Mater. Med. 2019, 30, 10. [Google Scholar] [CrossRef] [PubMed]
- Unterman, S.A.; Gibson, M.; Lee, J.H.; Crist, J.; Chansakul, T.; Yang, E.C.; Elisseeff, J.H. Hyaluronic Acid-Binding Scaffold for Articular Cartilage Repair. Tissue Eng. Part A 2012, 18, 2497–2506. [Google Scholar] [CrossRef] [Green Version]
- Antich, C.; de Vicente, J.; Jiménez, G.; Chocarro, C.; Carrillo, E.; Montañez, E.; Gálvez-Martín, P.; Marchal, J.A. Bio-Inspired Hydrogel Composed of Hyaluronic Acid and Alginate as a Potential Bioink for 3D Bioprinting of Articular Cartilage Engineering Constructs. Acta Biomater. 2020, 106, 114–123. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.H.; Kim, J.S.; Kim, W.K.; Lee, W.; Kim, N.; Song, C.U.; Jung, J.J.; Song, J.E.; Khang, G. Evaluation of Hyaluronic Acid/Agarose Hydrogel for Cartilage Tissue Engineering Biomaterial. Macromol. Res. 2020, 28, 979–985. [Google Scholar] [CrossRef]
- Mohan, N.; Mohanan, P.V.; Sabareeswaran, A.; Nair, P. Chitosan-Hyaluronic Acid Hydrogel for Cartilage Repair. Int. J. Biol. Macromol. 2017, 104, 1936–1945. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Hu, C.; Yu, H.; Chen, C. Chitosan Composite Scaffolds for Articular Cartilage Defect Repair: A Review. RSC Adv. 2018, 8, 3736–3749. [Google Scholar] [CrossRef]
- Subramanian, A.; Vasanthan, K.S.; Krishnan, U.M.; Sethuraman, S. Chitosan and Its Derivatives in Clinical Use and Applications. In Biodegradable Polymers in Clinical Use and Clinical Development; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2011; pp. 111–135. ISBN 978-1-118-01581-0. [Google Scholar]
- Nettles, D.L.; Elder, S.H.; Gilbert, J.A. Potential Use of Chitosan as a Cell Scaffold Material for Cartilage Tissue Engineering. Tissue Eng. 2002, 8, 1009–1016. [Google Scholar] [CrossRef] [PubMed]
- Li, Z.; Zhang, M. Chitosan–Alginate as Scaffolding Material for Cartilage Tissue Engineering. J. Biomed. Mater. Res. A 2005, 75, 485–493. [Google Scholar] [CrossRef]
- Li, C.; Wang, K.; Zhou, X.; Li, T.; Xu, Y.; Qiang, L.; Peng, M.; Xu, Y.; Xie, L.; He, C.; et al. Controllable Fabrication of Hydroxybutyl Chitosan/Oxidized Chondroitin Sulfate Hydrogels by 3D Bioprinting Technique for Cartilage Tissue Engineering. Biomed. Mater. 2019, 14, 025006. [Google Scholar] [CrossRef]
- Peng, L.; Zhou, Y.; Lu, W.; Zhu, W.; Li, Y.; Chen, K.; Zhang, G.; Xu, J.; Deng, Z.; Wang, D. Characterization of a Novel Polyvinyl Alcohol/Chitosan Porous Hydrogel Combined with Bone Marrow Mesenchymal Stem Cells and Its Application in Articular Cartilage Repair. BMC Musculoskelet. Disord. 2019, 20, 257. [Google Scholar] [CrossRef] [Green Version]
- Tan, H.; Chu, C.R.; Payne, K.A.; Marra, K.G. Injectable in Situ Forming Biodegradable Chitosan-Hyaluronic Acid Based Hydrogels for Cartilage Tissue Engineering. Biomaterials 2009, 30, 2499–2506. [Google Scholar] [CrossRef] [Green Version]
- Sechriest, V.F.; Miao, Y.J.; Niyibizi, C.; Westerhausen-Larson, A.; Matthew, H.W.; Evans, C.H.; Fu, F.H.; Suh, J.K. GAG-Augmented Polysaccharide Hydrogel: A Novel Biocompatible and Biodegradable Material to Support Chondrogenesis. J. Biomed. Mater. Res. 2000, 49, 534–541. [Google Scholar] [CrossRef]
- Frizziero, L.; Govoni, E.; Bacchini, P. Intra-Articular Hyaluronic Acid in the Treatment of Osteoarthritis of the Knee: Clinical and Morphological Study. Clin. Exp. Rheumatol. 1998, 16, 441–449. [Google Scholar]
- Iwasaki, N.; Yamane, S.-T.; Majima, T.; Kasahara, Y.; Minami, A.; Harada, K.; Nonaka, S.; Maekawa, N.; Tamura, H.; Tokura, S.; et al. Feasibility of Polysaccharide Hybrid Materials for Scaffolds in Cartilage Tissue Engineering: Evaluation of Chondrocyte Adhesion to Polyion Complex Fibers Prepared from Alginate and Chitosan. Biomacromolecules 2004, 5, 828–833. [Google Scholar] [CrossRef]
- Pahlevanzadeh, F.; Emadi, R.; Valiani, A.; Kharaziha, M.; Poursamar, S.A.; Bakhsheshi-Rad, H.R.; Ismail, A.F.; RamaKrishna, S.; Berto, F. Three-Dimensional Printing Constructs Based on the Chitosan for Tissue Regeneration: State of the Art, Developing Directions and Prospect Trends. Materials 2020, 13, 2663. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.-C.; Tan, F.; Marra, K.G.; Jan, S.-S.; Liu, D.-C. Synthesis and Characterization of Collagen/Hyaluronan/Chitosan Composite Sponges for Potential Biomedical Applications. Acta Biomater. 2009, 5, 2591–2600. [Google Scholar] [CrossRef]
- Adhikari, J.; Perwez, M.S.; Das, A.; Saha, P. Development of Hydroxyapatite Reinforced Alginate–Chitosan Based Printable Biomaterial-Ink. Nano-Struct. Nano-Objects 2021, 25, 100630. [Google Scholar] [CrossRef]
- Suh, J.K.; Matthew, H.W. Application of Chitosan-Based Polysaccharide Biomaterials in Cartilage Tissue Engineering: A Review. Biomaterials 2000, 21, 2589–2598. [Google Scholar] [CrossRef]
- Nasatto, P.L.; Pignon, F.; Silveira, J.L.M.; Duarte, M.E.R.; Noseda, M.D.; Rinaudo, M. Methylcellulose, a Cellulose Derivative with Original Physical Properties and Extended Applications. Polymers 2015, 7, 777–803. [Google Scholar] [CrossRef] [Green Version]
- Ahlfeld, T.; Guduric, V.; Duin, S.; Akkineni, A.R.; Schütz, K.; Kilian, D.; Emmermacher, J.; Cubo-Mateo, N.; Dani, S.; Witzleben, M.V.; et al. Methylcellulose—A Versatile Printing Material That Enables Biofabrication of Tissue Equivalents with High Shape Fidelity. Biomater. Sci. 2020, 8, 2102–2110. [Google Scholar] [CrossRef] [PubMed]
- Ahlfeld, T.; Köhler, T.; Czichy, C.; Lode, A.; Gelinsky, M. A Methylcellulose Hydrogel as Support for 3D Plotting of Complex Shaped Calcium Phosphate Scaffolds. Gels 2018, 4, 68. [Google Scholar] [CrossRef] [Green Version]
- Contessi Negrini, N.; Bonetti, L.; Contili, L.; Farè, S. 3D Printing of Methylcellulose-Based Hydrogels. Bioprinting 2018, 10, e00024. [Google Scholar] [CrossRef]
- Li, H.; Tan, Y.J.; Leong, K.F.; Li, L. 3D Bioprinting of Highly Thixotropic Alginate/Methylcellulose Hydrogel with Strong Interface Bonding. ACS Appl. Mater. Interfaces 2017, 9, 20086–20097. [Google Scholar] [CrossRef]
- Habib, A.; Sathish, V.; Mallik, S.; Khoda, B. 3D Printability of Alginate-Carboxymethyl Cellulose Hydrogel. Materials 2018, 11, 454. [Google Scholar] [CrossRef] [Green Version]
- Leone, G.; Fini, M.; Torricelli, P.; Giardino, R.; Barbucci, R. An Amidated Carboxymethylcellulose Hydrogel for Cartilage Regeneration. J. Mater. Sci. Mater. Med. 2008, 19, 2873–2880. [Google Scholar] [CrossRef] [PubMed]
- Mohan, T.; Dobaj Štiglic, A.; Beaumont, M.; Konnerth, J.; Gürer, F.; Makuc, D.; Maver, U.; Gradisnik, L.; Plavec, J.; Kargl, R.; et al. Generic Method for Designing Self-Standing and Dual Porous 3D Bioscaffolds from Cellulosic Nanomaterials for Tissue Engineering Applications. ACS Appl. Bio Mater. 2020, 3, 1197–1209. [Google Scholar] [CrossRef] [Green Version]
- Xu, X.; Jha, A.K.; Harrington, D.A.; Farach-Carson, M.C.; Jia, X. Hyaluronic Acid-Based Hydrogels: From a Natural Polysaccharide to Complex Networks. Soft Matter 2012, 8, 3280–3294. [Google Scholar] [CrossRef] [Green Version]
- Chung, C.; Burdick, J.A. Influence of Three-Dimensional Hyaluronic Acid Microenvironments on Mesenchymal Stem Cell Chondrogenesis. Tissue Eng. Part A 2009, 15, 243–254. [Google Scholar] [CrossRef] [PubMed]
- Garcia, J.; Stein, J.; Cai, Y.; Wexselblatt, E.; Creemers, L.; Wengel, J.; Howard, K.; Saris, D.; Yayon, A. Fibrin/Hyaluronic Acid Hydrogel for Combined Delivery of Gapmers and Chondrocytes as a Gene Therapy Approach for Osteoarthritis. Osteoarthritis Cartilage 2018, 26, S145. [Google Scholar] [CrossRef] [Green Version]
- Maia, J.; Evangelista, M.; Gil, H.; Ferreira, L. Dextran-based materials for biomedical applications. In Carbohydrates Applications in Medicine; Trivandrum: Kerala, India, 2014; pp. 31–53. ISBN 978-81-308-0523-8. [Google Scholar]
- Jin, R.; Moreira Teixeira, L.S.; Dijkstra, P.J.; Zhong, Z.; van Blitterswijk, C.A.; Karperien, M.; Feijen, J. Enzymatically Crosslinked Dextran-Tyramine Hydrogels as Injectable Scaffolds for Cartilage Tissue Engineering. Tissue Eng. Part A 2010, 16, 2429–2440. [Google Scholar] [CrossRef] [PubMed]
- Jin, R.; Moreira Teixeira, L.S.; Dijkstra, P.J.; van Blitterswijk, C.A.; Karperien, M.; Feijen, J. Chondrogenesis in Injectable Enzymatically Crosslinked Heparin/Dextran Hydrogels. J. Control. Release Off. J. Control. Release Soc. 2011, 152, 186–195. [Google Scholar] [CrossRef] [PubMed]
- Jin, R.; Teixeira, L.S.M.; Dijkstra, P.J.; van Blitterswijk, C.A.; Karperien, M.; Feijen, J. Enzymatically-Crosslinked Injectable Hydrogels Based on Biomimetic Dextran-Hyaluronic Acid Conjugates for Cartilage Tissue Engineering. Biomaterials 2010, 31, 3103–3113. [Google Scholar] [CrossRef]
- Wang, X.; Li, Z.; Shi, T.; Zhao, P.; An, K.; Lin, C.; Liu, H. Injectable Dextran Hydrogels Fabricated by Metal-Free Click Chemistry for Cartilage Tissue Engineering. Mater. Sci. Eng. C 2017, 73, 21–30. [Google Scholar] [CrossRef]
- Confalonieri, D.; Schwab, A.; Walles, H.; Ehlicke, F. Advanced Therapy Medicinal Products: A Guide for Bone Marrow-Derived MSC Application in Bone and Cartilage Tissue Engineering. Tissue Eng. Part B Rev. 2018, 24, 155–169. [Google Scholar] [CrossRef] [PubMed]
- Kubosch, E.J.; Lang, G.; Furst, D.; Kubosch, D.; Izadpanah, K.; Rolauffs, B.; Sudkamp, N.P.; Schmal, H. The Potential for Synovium-Derived Stem Cells in Cartilage Repair. Curr. Stem Cell Res. Ther. 2018, 13, 174–184. [Google Scholar] [CrossRef]
- Gugjoo, M.B.; Amarpal, G.T.; Aithal, H.P.; Kinjavdekar, P. Cartilage Tissue Engineering: Role of Mesenchymal Stem Cells along with Growth Factors & Scaffolds. Indian J. Med. Res. 2016, 144, 339–347. [Google Scholar] [CrossRef] [PubMed]
- Somoza, R.A.; Welter, J.F.; Correa, D.; Caplan, A.I. Chondrogenic Differentiation of Mesenchymal Stem Cells: Challenges and Unfulfilled Expectations. Tissue Eng. Part B Rev. 2014, 20, 596–608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kang, S.-W.; Yoo, S.P.; Kim, B.-S. Effect of Chondrocyte Passage Number on Histological Aspects of Tissue-Engineered Cartilage. Biomed. Mater. Eng. 2007, 17, 269–276. [Google Scholar]
- Lee, W.Y.-W.; Wang, B. Cartilage Repair by Mesenchymal Stem Cells: Clinical Trial Update and Perspectives. J. Orthop. Transl. 2017, 9, 76–88. [Google Scholar] [CrossRef] [PubMed]
- Francis, S.L.; Di Bella, C.; Wallace, G.G.; Choong, P.F.M. Cartilage Tissue Engineering Using Stem Cells and Bioprinting Technology—Barriers to Clinical Translation. Front. Surg. 2018, 5, 70. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, J.K.; Responte, D.J.; Cissell, D.D.; Hu, J.C.; Nolta, J.A.; Athanasiou, K.A. Clinical Translation of Stem Cells: Insight for Cartilage Therapies. Crit. Rev. Biotechnol. 2014, 34, 89–100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Crovace, A.M.; Giancamillo, A.D.; Gervaso, F.; Mangiavini, L.; Zani, D.; Scalera, F.; Palazzo, B.; Izzo, D.; Agnoletto, M.; Domenicucci, M.; et al. Evaluation of in Vivo Response of Three Biphasic Scaffolds for Osteochondral Tissue Regeneration in a Sheep Model. Vet. Sci. 2019, 6, 90. [Google Scholar] [CrossRef] [Green Version]
- Meng, X.; Ziadlou, R.; Grad, S.; Alini, M.; Wen, C.; Lai, Y.-X.; Qin, L.; Zhao, Y.; Wang, X. Animal Models of Osteochondral Defect for Testing Biomaterials. Biochem. Res. Int. 2020, 2020, 9659412. [Google Scholar] [CrossRef] [Green Version]
- Chu, C.R.; Szczodry, M.; Bruno, S. Animal Models for Cartilage Regeneration and Repair. Tissue Eng. Part B Rev. 2010, 16, 105–115. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Wang, Z.; Huang, P.; Jiang, G.; Xu, C.; Zhang, W.; Guo, R.; Li, W.; Zhang, X. Real-Time and Noninvasive Tracking of Injectable Hydrogel Degradation Using Functionalized AIE Nanoparticles. Nanophotonics 2020, 9, 2063–2075. [Google Scholar] [CrossRef]
- Zhang, Y.; Rossi, F.; Papa, S.; Violatto, M.B.; Bigini, P.; Sorbona, M.; Redaelli, F.; Veglianese, P.; Hilborn, J.; Ossipov, D.A. Non-Invasive in Vitro and in Vivo Monitoring of Degradation of Fluorescently Labeled Hyaluronan Hydrogels for Tissue Engineering Applications. Acta Biomater. 2016, 30, 188–198. [Google Scholar] [CrossRef]
- Yang, J.; Zhang, Y.S.; Yue, K.; Khademhosseini, A. Cell-Laden Hydrogels for Osteochondral and Cartilage Tissue Engineering. Acta Biomater. 2017, 57, 1–25. [Google Scholar] [CrossRef] [PubMed]
- Tang, G.; Zhou, B.; Li, F.; Wang, W.; Liu, Y.; Wang, X.; Liu, C.; Ye, X. Advances of Naturally Derived and Synthetic Hydrogels for Intervertebral Disk Regeneration. Front. Bioeng. Biotechnol. 2020, 8, 745. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, E.M. Hydrogel: Preparation, Characterization, and Applications: A Review. J. Adv. Res. 2015, 6, 105–121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Li, B.; Xu, F.; Li, Y.; Xu, Z.; Wei, D.; Feng, Y.; Wang, Y.; Jia, D.; Zhou, Y. Visual in Vivo Degradation of Injectable Hydrogel by Real-Time and Non-Invasive Tracking Using Carbon Nanodots as Fluorescent Indicator. Biomaterials 2017, 145, 192–206. [Google Scholar] [CrossRef] [PubMed]
Hydrogels | Cell Type | Scaffold Formation | Main Features |
---|---|---|---|
Alginate [32,54] | various | Alginate-based bioinks | biocompatibility, degradability, process flexibility and excellent printability |
Fibrin [62] | hBM-MSC | Blended hydrogel | promoted cell proliferation |
Gelatin and Nhap [31] | Mouse chondrocytes | 3D printed hydrogel | high cell viability, supported cellular adhesion and growth |
Gelatin and fibrinogen [49] | Human bone MCS | 3D bioprinting | chondrogenic differentiation, ECM synthesis, chondrogenic phenotype |
Fibrin and HA [50] | Rabbit chondrocytes | 3D bioprinting bioinks | proper environment for cartilage formation |
Collagen [64] | Rats’ chondrocytes | 3D bioprinting bioinks | cell adhesion, proliferation and expression of cartilage specific genes |
Nanocellulose [65] | Articular cartilage (calves) | Printable bioink | promoted cell spreading, proliferation, and collagen II synthesis by the encapsulated cells |
Agarose [28,69] | various | Agarose-based hydrogels | biocompatibility, water solubility, adaptable mechanical properties, printability |
Silk Fibroin [70] | Cartilaginous tissue | Blended hydrogels | immunocompatibility, deposition of glycosaminoglycans (GAG) and collagen, upregulation of cartilage genes |
Fibrin [51] | HECDC | Nanostructured hydrogels | biodegradable and biologically active constructs |
Chitosan [71,72], | Chondrocyte, IFP-ASCs | 3D-printed hydrogels | biocompatibility, cellular morphology, mechanical properties, chondrogenesis |
CM Chitosan [73] | Rabbit chondrocytes | 3D bioprinting bioinks | cell attachment, favorable mechanical property, chondrogenic gene expression |
Chitosan-HA [74] | ADSC | Biomimetic Matrices | supports stem cell differentiation towards cartilage matrix producing chondrocytes |
Cellulose | |||
NFC-Alginate [66] | human chondrocytes | 3D bioprinting | potential use of nanocellulose for 3D bioprinting of living tissues and organs |
NFC-Alginate and HA [75] | iPSCs | 3D bioprinting | NFC/A bioink is suitable for bioprinting iPSCs to support cartilage production |
Methylcellulose (MC) | |||
Alginate-MC [76] | bovine chondrocytes | Bioink for bioprinting | 3D-printing-based fabrication, bioengineered tissue for cartilage regeneration |
Hyaluronic acid [77,78], | various | Hydrogels | stimulates the chondrogenic differentiation, produce essential cartilage ECM |
Alginate-HA [78] | hAC | HA-based bioink (hydrogel) | cell functionality, expression of chondrogenic gene markers, specific matrix deposition |
Agarose-HA [79] | rabbit chondrocytes | Hydrogels | improved viability, proliferation, morphology and adhesion of the chondrocytes |
Chitosan-HA [80] | rabbit chondrocytes | Hydrogels | in vivo study (rabbits); implant had a mixture of hyaline and fibro cartilage |
Chitosan-HA [74] | ADSC | Biomimetic Matrices | supports stem cell differentiation towards cartilage matrix producing chondrocytes |
Gelatin-HA [52] | hBMSCs | Hybrid hydrogel | in vivo study (rabbit femoral condyle) promising scaffold for repair and resurfacing |
Collagen-HA [53] | rabbit | Hybrid scaffolds | in vivo study (cartilage defects of rabbit ear) |
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Naranda, J.; Bračič, M.; Vogrin, M.; Maver, U. Recent Advancements in 3D Printing of Polysaccharide Hydrogels in Cartilage Tissue Engineering. Materials 2021, 14, 3977. https://doi.org/10.3390/ma14143977
Naranda J, Bračič M, Vogrin M, Maver U. Recent Advancements in 3D Printing of Polysaccharide Hydrogels in Cartilage Tissue Engineering. Materials. 2021; 14(14):3977. https://doi.org/10.3390/ma14143977
Chicago/Turabian StyleNaranda, Jakob, Matej Bračič, Matjaž Vogrin, and Uroš Maver. 2021. "Recent Advancements in 3D Printing of Polysaccharide Hydrogels in Cartilage Tissue Engineering" Materials 14, no. 14: 3977. https://doi.org/10.3390/ma14143977