Innovative Tissue-Engineered Strategies for Osteochondral Defect Repair and Regeneration: Current Progress and Challenges.

clinical applications osteochondral defect repair and regeneration scaffolds tissue-engineered strategies

Journal

Advanced healthcare materials
ISSN: 2192-2659
Titre abrégé: Adv Healthc Mater
Pays: Germany
ID NLM: 101581613

Informations de publication

Date de publication:
26 Oct 2020
Historique:
received: 15 06 2020
revised: 19 09 2020
entrez: 26 10 2020
pubmed: 27 10 2020
medline: 27 10 2020
Statut: aheadofprint

Résumé

Clinical treatments for the repair of osteochondral defects (OCD) are merely palliative, not completely curative, and thus enormously unfulfilled challenges. With the in-depth studies of biology, medicine, materials, and engineering technology, the conception of OCD repair and regeneration should be renewed. During the past decades, many innovative tissue-engineered approaches for repairing and regenerating damaged osteochondral units have been widely explored. Various scaffold-free and scaffold-based strategies, such as monophasic, biphasic, and currently fabricated multiphasic and gradient architectures have been proposed and evaluated. Meanwhile, progenitor cells and tissue-specific cells have also been intensively investigated in vivo as well as ex vivo. Concerning bioactive factors and drugs, they have been combined with scaffolds and/or living cells, and even released in a spatiotemporally controlled manner. Although tremendous progress has been achieved, further research and development (R&D) is needed to convert preclinical outcomes into clinical applications. Here, the osteochondral unit structure, its defect classifications, and diagnosis are summarized. Commonly used clinical reparative techniques, tissue-engineered strategies, emerging 3D-bioprinting technologies, and the status of their clinical applications are discussed. Existing challenges to translation are also discussed and potential solutions for future R&D directions are proposed.

Identifiants

pubmed: 33103381
doi: 10.1002/adhm.202001008
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2001008

Subventions

Organisme : AO Foundation
ID : TA1711481
Organisme : Hong Kong RGC Theme-based Research Scheme
ID : T13-402/17-N
Organisme : Bureau of Industry and Information Technology of Shenzhen
ID : 201908141541

Informations de copyright

© 2020 Wiley-VCH GmbH.

Références

D. J. Hunter, Osteoarthritis Cartilage 2009, 17, 1402.
C. Deng, J. Chang, C. Wu, J. Orthop. Translat. 2019, 17, 15.
P. Nooeaid, V. Salih, J. P. Beier, A. R. Boccaccini, J. Cell. Mol. Med. 2012, 16, 2247.
H. Madry, C. N.van Dijk, M. Mueller-Gerbl, Knee Surg. Sports Traumatol. Arthrosc. 2010, 18, 419.
a) P. Orth, H. Madry, Tissue Eng., Part B 2015, 21, 504;
b) E. Kon, M. Ronga, G. Filardo, J. Farr, H. Madry, G. Milano, L. Andriolo, N. Shabshin, Knee Surgery, Sports Traumatology, Arthroscopy 2016, 24, 1797;
c) M. L.de Vries-van Melle, M. S. Tihaya, N. Kops, W. Koevoet, J. M. Murphy, J. Verhaar, M. Alini, D. Eglin, G.van Osch, Eur. Cell Mater. 2014, 27, 112;
d) M. B. Fisher, N. S. Belkin, A. H. Milby, E. A. Henning, M. Bostrom, M. Kim, C. Pfeifer, G. Meloni, G. R. Dodge, J. A. Burdick, Tissue Eng., Part A 2015, 21, 850.
a) H. Madry, P. Orth, M. Cucchiarini, J. Am. Acad. Orthop. Surg. 2016, 24, e45;
b) M. L.de Vries-van Melle, R. Narcisi, N. Kops, W. J. Koevoet, P. K. Bos, J. M. Murphy, J. A. Verhaar, P. M.van der Kraan, G. J.van Osch, Tissue Eng., Part A 2014, 20, 23.
a) T. Badekas, M. Takvorian, N. Souras, Int. Orthop. 2013, 37, 1697;
b) R. D'Ambrosi, V. Ragone, N. Ursino, Ann. Transl. Med. 2018, 6, S100.
J. M. Pestka, G. Bode, G. Salzmann, N. P. Südkamp, P. Niemeyer, Am. J. Sports Med. 2012, 40, 325.
M. Brittberg, A. Lindahl, A. Nilsson, C. Ohlsson, O. Isaksson, L. Peterson, N. Engl. J. Med. 1994, 331, 889.
W. Bartlett, J. Skinner, C. Gooding, R. Carrington, A. Flanagan, T. Briggs, G. Bentley, J. Bone Jt. Surg. Br.Vol. 2005, 87-B, 640.
T. J. Dekker, P. K. Dekker, D. M. Tainter, M. E. Easley, S. B. Adams, JBJS Rev. 2017, 5, 01874474.
a) S. P. Nukavarapu, D. L. Dorcemus, Biotechnol. Adv. 2013, 31, 706;
b) S. Panseri, A. Russo, C. Cunha, A. Bondi, A. Di Martino, S. Patella, E. Kon, Knee Surgery, Sports Traumatology, Arthroscopy 2012, 20, 1182.
E. J. Sheehy, T. Vinardell, C. T. Buckley, D. J. Kelly, Acta Biomater. 2013, 9, 5484.
a) X. Li, J. Ding, J. Wang, X. Zhuang, X. Chen, Regener. Biomater. 2015, 2, 221;
b) K. Shimomura, Y. Moriguchi, C. D. Murawski, H. Yoshikawa, N. Nakamura, Tissue Eng., Part B 2014, 20, 468.
R. M. Jeuken, A. K. Roth, R. J. Peters, C. C. Van Donkelaar, J. C. Thies, L. W. Van Rhijn, P. J. Emans, Polymers 2016, 8, 219.
S. Stratton, N. B. Shelke, K. Hoshino, S. Rudraiah, S. G. Kumbar, Bioact. Mater. 2016, 1, 93.
F. Asghari, M. Samiei, K. Adibkia, A. Akbarzadeh, S. Davaran, Artif. Cells, Nanomed., Biotechnol. 2017, 45, 185.
R. Trombetta, J. A. Inzana, E. M. Schwarz, S. L. Kates, H. A. Awad, Ann. Biomed. Eng. 2017, 45, 23.
P. Gao, H. Zhang, Y. Liu, B. Fan, X. Li, X. Xiao, P. Lan, M. Li, L. Geng, D. Liu, Sci. Rep. 2016, 6, 23367, https://doi.org/10.1038/srep23367.
M. Mucalo, Hydroxyapatite (HAp) for Biomedical Applications, Elsevier, Amsterdam 2015.
F. Shah, J. Czechowska, Bioactive Glasses, Elsevier, Amsterdam 2018, p. 201.
a) A. Marionneaux, J. Walters, H. Guo, J. Mercuri, Acta Biomater. 2018, 78, 351;
b) F. Gao, Z. Xu, Q. Liang, B. Liu, H. Li, Y. Wu, Y. Zhang, Z. Lin, M. Wu, C. Ruan, Adv. Funct. Mater. 2018, 28, 1706644.
J. Radhakrishnan, A. Manigandan, P. Chinnaswamy, A. Subramanian, S. Sethuraman, Biomaterials 2018, 162, 82.
a) A. Gannon, T. Nagel, A. Bell, N. Avery, D. Kelly, Eur. Cell Mater. 2015, 29, 121;
b) J. Antons, M. G. M. Marascio, J. Nohava, R. Martin, L. Applegate, P. Bourban, D. Pioletti, J. Mater. Sci.: Mater. Med. 2018, 29, 57.
a) H. Madry, M. Alini, M. Stoddart, C. Evans, T. Miclau, S. Steiner, Eur. Cell Mater. 2014, 27s, 17;
b) H. Madry, Knee Surg Sports Traumatol A rthrosc 2010, 18, 417, https://doi.org/10.1007/s00167-010-1071-y.
a) C. B. Carballo, Y. Nakagawa, I. Sekiya, S. A. Rodeo, Clin. Sports Med. 2017, 36, 413;
b) A. J. Sophia Fox, A. Bedi, S. A. Rodeo, Sports Health 2009, 1, 461;
c) K. A. Athanasiou, E. M. Darling, J. C. Hu, G. D. DuRaine, A. H. Reddi, Articular Cartilage, CRC Press, Boca Raton, FL 2013.
A. G. Bajpayee, A. J. Grodzinsky, Nat. Rev. Rheumatol. 2017, 13, 183.
E. Han, S. S. Chen, S. M. Klisch, R. L. Sah, Biophys. J. 2011, 101, 916.
C. K. Jung, Techniques in Cartilage Repair Surgery, Springer, Berlin 2014, p. 17.
G. Musumeci, P. Castrogiovanni, V. Mazzone, M. Szychlinska, S. Castorina, C. Loreto, Eur. J. Histochem. 2014, 58, 2371.
D. Goyal, A. Goyal, N. Adachi, Bio-orthopaedics, Springer, Berlin 2017, p. 479.
a) E. L. Radin, H. G. Parker, J. W. Pugh, R. S. Steinberg, I. L. Paul, R. M. Rose, J. Biomech. 1973, 6, 51;
b) E. L. Radin, I. L. Paul, Arthritis Rheum. 1971, 14, 356;
c) S. R. Simon, E. L. Radin, I. L. Paul, R. M. Rose, J. Biomech. 1972, 5, 267.
D. Frisbie, Musculoskeletal System: Medical Treatment of Joint Disease, 4th ed., Elsevier Saunders, St Louis, MO 2012, p. 1114.
T. Funck-Brentano, M. Cohen-Solal, Curr. Opin. Rheumatol. 2015, 27, 420.
a) F. Eymard, C. Parsons, M. Edwards, F. Petit-Dop, J.-Y. Reginster, O. Bruyère, P. Richette, C. Cooper, X. Chevalier, Osteoarthritis Cartilage 2015, 23, 851;
b) C. Lou, G. Xiang, Q. Weng, Z. Chen, D. Chen, Q. Wang, D. Zhang, B. Zhou, D. He, H. Chen, Menopause 2016, 23, 1239;
c) T. M. Simon, D. W. Jackson, Sports Med. Arthrosc. Rev. 2018, 26, 31.
B. J. Chilelli, B. J. Cole, J. Farr, C. Lattermann, A. H. Gomoll, Instr. Course Lect. 2017, 66, 507.
C. Slattery, C. Y. Kweon, Clin. Orthop. Relat. Res. 2018, 476, 2101.
F. R. Noyes, C. L. Stabler, Am. J. Sports Med. 1989, 17, 505.
C. Acebes, J. Roman-Blas, E. Delgado-Baeza, I. Palacios, G. Herrero-Beaumont, Osteoarthritis Cartilage 2009, 17, 205.
R. Custers, L. Creemers, A. Verbout, M. Van Rijen, W. Dhert, D. Saris, Osteoarthritis Cartilage 2007, 15, 1241.
A. H. Gomoll, T. Minas, Wound Repair Regener. 2014, 22, 30.
F. W. Roemer, M. D. Crema, S. Trattnig, A. Guermazi, Radiology 2011, 260, 332.
T. Nakasa, N. Adachi, T. Kato, M. Ochi, Foot Ankle Int. 2014, 35, 600.
S. Trattnig, G. H. Welsch, S. Röhrich, M. M. Schreiner, M. Zalaudek, Articular Cartilage of the Knee, Springer, Berlin 2020, p. 343.
a) M. Posadzy, J. Desimpel, F. Vanhoenacker, J. Belgian Soc. Radiol. 2017, 101;
b) K. I.van den Ende, R. Keijsers, M. P.van den Bekerom, D. Eygendaal, Shoulder Elbow 2019, 11, 129.
L. Felli, G. Garlaschi, A. Muda, A. Tagliafico, M. Formica, A. Zanirato, M. Alessio-Mazzola, Musculoskeletal Surg. 2016, 100, 231.
X. Ayral, Baillière's Clin. Rheumatol. 1996, 10, 477.
Y.-P. Huang, J. Zhong, J. Chen, C.-H. Yan, Y.-P. Zheng, C.-Y. Wen, Ultrasound Med. Biol. 2018, 44, 94.
W. W. Curl, J. Krome, E. S. Gordon, J. Rushing, B. P. Smith, G. G. Poehling, Arthroscopy 1997, 13, 456.
R. F. Loeser, Curr. Opin. Rheumatol. 2013, 25, 108.
J. Farr, B. Cole, A. Dhawan, J. Kercher, S. Sherman, Clin. Orthop. Relat. Res. 2011, 469, 2696.
J. Steadman, W. Rodkey, K. Briggs, J. Rodrigo, Der Orthopade 1999, 28, 26.
P. Angermann, P. Riegels-Nielsen, H. Pedersen, Acta Orthop. Scand. 1998, 69, 595.
S. Bouwmeester, J. Beckers, R. Kuijer, A. Van Der Linden, S. Bulstra, Int. Orthop. 1997, 21, 313.
L. Bartha, A. Vajda, Z. Duska, H. Rahmeh, L. Hangody, J. Orthop. Sports Phys. Ther. 2006, 36, 739.
B. R. Mandelbaum, M. B. Gerhardt, L. Peterson, Arthroscopy 2003, 19, 129.
P. Behrens, T. Bitter, B. Kurz, M. Russlies, Knee 2006, 13, 194.
H. Kim, M. Moran, R. B. Salter, JBJS 1991, 73, 1301.
H. Mistry, M. Connock, J. Pink, D. Shyangdan, C. Clar, P. Royle, R. Court, L. C. Biant, A. Metcalfe, N. Waugh, 2017. Available from: https://www.ncbi.nlm.nih.gov/books/NBK424075/ https://doi.org/10.3310/hta2106
R. Bexkens, P. T. Ogink, J. N. Doornberg, G. M. Kerkhoffs, D. Eygendaal, L. S. Oh, M. P.van den Bekerom, Knee Surg. Sports Traumatol. Arthrosc. 2017, 25, 2237.
J. Huntley, A. Simpson, A. Hall, Eur. Cell Mater. 2005, 9, 13.
B. D. Smith, D. A. Grande, Nat. Rev. Rheumatol. 2015, 11, 213.
Y. C. Cheuk, M. W. N. Wong, K. M. Lee, S. C. Fu, J. Orthop. Res. 2011, 29, 1343.
A. He, L. Liu, X. Luo, Y. Liu, Y. Liu, F. Liu, X. Wang, Z. Zhang, W. Zhang, W. Liu, Sci. Rep. 2017, 7, 40489, https://doi.org/10.1038/srep40489.
T. Oshima, J. Nakase, T. Toratani, H. Numata, Y. Takata, K. Nakayama, H. Tsuchiya, Arthroscopy 2019, 35, 583.
a) M. Thornemo, T. Tallheden, E. S. Jansson, A. Larsson, K. Lövstedt, U. Nannmark, M. Brittberg, A. Lindahl, Cells Tissues Organs 2005, 180, 141;
b) G. P. Dowthwaite, J. C. Bishop, S. N. Redman, I. M. Khan, P. Rooney, D. J. Evans, L. Haughton, Z. Bayram, S. Boyer, B. Thomson, J. Cell Sci. 2004, 117, 889.
H. Li, J. Qian, J. Chen, K. Zhong, S. Chen, Mol. Med. Rep. 2016, 13, 2071.
J.-Y. Ko, K.-I. Kim, S. Park, G.-I. Im, Biomaterials 2014, 35, 3571.
M. Itokazu, S. Wakitani, H. Mera, Y. Tamamura, Y. Sato, M. Takagi, H. Nakamura, Cartilage 2016, 7, 361.
J. D. Kisiday, Regener. Med. Front. 2019, 2, e200002.
A. M. Mackay, S. C. Beck, J. M. Murphy, F. P. Barry, C. O. Chichester, M. F. Pittenger, Tissue Eng. 1998, 4, 415.
N. Jaiswal, S. E. Haynesworth, A. I. Caplan, S. P. Bruder, J. Cell. Biochem. 1997, 64, 295.
T. Fink, V. Zachar, in Mesenchymal Stem Cell Assays and Applications, Springer, Berlin 2011, p. 243.
B. Sacchetti, A. Funari, C. Remoli, G. Giannicola, G. Kogler, S. Liedtke, G. Cossu, M. Serafini, M. Sampaolesi, E. Tagliafico, Stem Cell Rep. 2016, 6, 897.
A. Friedenstein, F. AJ, P. AF, 1974.
L. Bacakova, J. Zarubova, M. Travnickova, J. Musilkova, J. Pajorova, P. Slepicka, N. S. Kasalkova, V. Svorcik, Z. Kolska, H. Motarjemi, Biotechnol. Adv. 2018, 36, 1111.
B. H. Lee, J. N. Park, E. J. Lee, Y. W. Moon, J. H. Wang, Am. J. Sports Med. 2018, 46, 2242.
T. Zhou, X. Li, G. Li, T. Tian, S. Lin, S. Shi, J. Liao, X. Cai, Y. Lin, Sci. Rep. 2017, 7, 10553, https://doi.org/10.1038/s41598-017-11322-w.
R. Reyes, A. Delgado, E. Sanchez, A. Fernandez, A. Hernandez, C. Evora, J. Tissue Eng. Regener. Med. 2014, 8, 521.
a) C. R. Rowland, K. A. Glass, A. R. Ettyreddy, C. C. Gloss, J. R. Matthews, N. P. Huynh, F. Guilak, Biomaterials 2018, 177, 161;
b) F. T. Moutos, K. A. Glass, S. A. Compton, A. K. Ross, C. A. Gersbach, F. Guilak, B. T. Estes, Proc. Natl. Acad. Sci. USA 2016, 113, E4513;
c) J. M. Brunger, N. P. Huynh, C. M. Guenther, P. Perez-Pinera, F. T. Moutos, J. Sanchez-Adams, C. A. Gersbach, F. Guilak, Proc. Natl. Acad. Sci. USA 2014, 111, E798.
M. Barsoum, Fundamentals of Ceramics, CRC Press, Boca Raton, FL 2019.
a) M. Yazdimamaghani, M. Razavi, D. Vashaee, K. Moharamzadeh, A. R. Boccaccini, L. Tayebi, Mater. Sci. Eng., C 2017, 71, 1253;
b) J. L. Wang, J. K. Xu, C. Hopkins, D. H. K. Chow, L. Qin, Adv. Sci. 2020, 7, 1902443.
L. Tian, N. Tang, T. Ngai, C. Wu, Y. Ruan, L. Huang, L. Qin, J. Orthop. Translat. 2019, 16, 1.
L. Tian, Y. Sheng, L. Huang, D. H.-K. Chow, W. H. Chau, N. Tang, T. Ngai, C. Wu, J. Lu, L. Qin, Biomaterials 2018, 180, 173.
Y. Zhang, J. Xu, Y. C. Ruan, M. K. Yu, M. O'Laughlin, H. Wise, D. Chen, L. Tian, D. Shi, J. Wang, Nat. Med. 2016, 22, 1160.
C. G. Jeong, H. Zhang, S. J. Hollister, J. Biomed. Mater. Res., Part A 2012, 100A, 2088.
C. R. Chu, J. S. Dounchis, M. Yoshioka, R. L. Sah, R. D. Coutts, D. Amiel, Clin. Orthop. Relat. Res. 1997, 340, 220.
L. Keller, P. Schwinté, E. Gomez-Barrena, M. Arruebo, N. Benkirane-Jessel, Trends Biotechnol. 2017, 35, 8.
L. Keller, Q. Wagner, P. Schwinté, N. Benkirane-Jessel, Nanomedicine 2015, 10, 2833.
L. Keller, L. Pijnenburg, Y. Idoux-Gillet, F. Bornert, L. Benameur, M. Tabrizian, P. Auvray, P. Rosset, R. M. Gonzalo-Daganzo, E. G. Barrena, Nat. Commun. 2019, 10, 2156.
D. Lin, B. Cai, L. Wang, L. Cai, Z. Wang, J. Xie, Q.-x. Lv, Y. Yuan, C. Liu, S. G. Shen, Biomaterials 2020, 253, 120095.
S. Liu, J. Wu, X. Liu, D. Chen, G. L. Bowlin, L. Cao, J. Lu, F. Li, X. Mo, C. Fan, J. Biomed. Mater. Res., Part A 2015, 103, 581.
E. Kon, G. Filardo, J. Shani, N. Altschuler, A. Levy, K. Zaslav, J. E. Eisman, D. Robinson, J. Orthop. Surg. Res. 2015, 10, 81.
Y. Zhu, L. Kong, F. Farhadi, W. Xia, J. Chang, Y. He, H. Li, Biomaterials 2019, 192, 149.
P. Duan, Z. Pan, L. Cao, J. Gao, H. Yao, X. Liu, R. Guo, X. Liang, J. Dong, J. Ding, J. Orthop. Translat. 2019, 19, 68.
S. Frenkel, G. Bradica, J. Brekke, S. Goldman, K. Ieska, P. Issack, M. Bong, H. Tian, J. Gokhale, R. Coutts, Osteoarthritis Cartilage 2005, 13, 798.
J. Liao, T. Tian, S. Shi, X. Xie, Q. Ma, G. Li, Y. Lin, Bone Res. 2017, 5, 17018.
X. Liu, S. Liu, S. Liu, W. Cui, J. Biomed. Mater. Res., Part B 2014, 102, 1407.
T. J. Levingstone, A. Ramesh, R. T. Brady, P. A. Brama, C. Kearney, J. P. Gleeson, F. J. O'Brien, Biomaterials 2016, 87, 69.
T. J. Levingstone, E. Thompson, A. Matsiko, A. Schepens, J. P. Gleeson, F. J. O'Brien, Acta Biomater. 2016, 32, 149.
M. Singh, N. Dormer, J. R. Salash, J. M. Christian, D. S. Moore, C. Berkland, M. S. Detamore, J. Biomed. Mater. Res., Part A 2010, 94, 870.
A. Di Luca, K. Szlazak, I. Lorenzo-Moldero, C. A. Ghebes, A. Lepedda, W. Swieszkowski, C. Van Blitterswijk, L. Moroni, Acta Biomater. 2016, 36, 210.
A. Di Luca, B. Ostrowska, I. Lorenzo-Moldero, A. Lepedda, W. Swieszkowski, C. Van Blitterswijk, L. Moroni, Sci. Rep. 2016, 6, 22898, https://doi.org/10.1038/srep22898.
A. Di Luca, I. Lorenzo-Moldero, C. Mota, A. Lepedda, D. Auhl, C. Van Blitterswijk, L. Moroni, Adv. Healthcare Mater. 2016, 5, 1753.
Y. Du, H. Liu, Q. Yang, S. Wang, J. Wang, J. Ma, I. Noh, A. G. Mikos, S. Zhang, Biomaterials 2017, 137, 37.
F. Gao, Z. Xu, Q. Liang, H. Li, L. Peng, M. Wu, X. Zhao, X. Cui, C. Ruan, W. Liu, Adv. Sci. 2019, 6, 1900867.
N. Mohan, N. H. Dormer, K. L. Caldwell, V. H. Key, C. J. Berkland, M. S. Detamore, Tissue Eng., Part A 2011, 17, 2845.
P. Chen, L. Zheng, Y. Wang, M. Tao, Z. Xie, C. Xia, C. Gu, J. Chen, P. Qiu, S. Mei, Theranostics 2019, 9, 2439.
a) S. Toosi, J. Behravan, BioFactors 2019, 46, 326;
b) M. A. Meyer, A. Urita, B. J. Cole, S. Chubinskaya, Cartilage, Springer, Berlin 2017, p. 109;
c) M. Qasim, D. S. Chae, N. Y. Lee, J. Biomed. Mater. Res., Part A 2020, 108, 394;
d) H. Yao, J. Xu, N. Zheng, J. Wang, S. Mok, Y. Lee, L. Shi, J. Wang, J. Yue, S. Yung, Osteoarthritis Cartilage 2019, 27, 1811.
E. López-Ruiz, G. Jiménez, M. Á. García, C. Antich, H. Boulaiz, J. A. Marchal, M. Perán, Expert Opin. Ther. Pat. 2016, 26, 877.
a) J. Wang, F. Witte, T. Xi, Y. Zheng, K. Yang, Y. Yang, D. Zhao, J. Meng, Y. Li, W. Li, Acta Biomater. 2015, 21, 237;
b) J. Xu, The Chinese University of Hong Kong 2017.
Y. Lai, Y. Li, H. Cao, J. Long, X. Wang, L. Li, C. Li, Q. Jia, B. Teng, T. Tang, Biomaterials 2019, 197, 207.
L. Mendes, H. Katagiri, W. Tam, Y. Chai, L. Geris, S. Roberts, F. Luyten, Stem Cell Res. Ther. 2018, 9, 42.
P. Chen, J. Tao, S. Zhu, Y. Cai, Q. Mao, D. Yu, J. Dai, H. Ouyang, Biomaterials 2015, 39, 114.
M. B. Gugjoo, A. Abdelbaset-Ismail, H. P. Aithal, P. Kinjavdekar, A. M. Pawde, G. S. Kumar, G. T. Sharma, Biomed. Pharmacother. 2017, 93, 1165.
A. Di Luca, M. Klein-Gunnewiek, J. G. Vancso, C. A. Van Blitterswijk, E. M. Benetti, L. Moroni, Biotechnol. J. 2017, 12, 1700072.
J. Liu, L. Li, H. Suo, M. Yan, J. Yin, J. Fu, Mater. Des. 2019, 171, 107708.
S. M. Bittner, B. T. Smith, L. Diaz-Gomez, C. D. Hudgins, A. J. Melchiorri, D. W. Scott, J. P. Fisher, A. G. Mikos, Acta Biomater. 2019, 90, 37.
A. C. Daly, D. J. Kelly, Biomaterials 2019, 197, 194.
E. Pintus, M. Baldassarri, L. Perazzo, S. Natali, D. Ghinelli, R. Buda, in Osteochondral Tissue Engineering, Springer, Berlin 2018, p. 359.
D. A. Rennerfeldt, K. J. Van Vliet, Stem Cells 2016, 34, 1135.
M. Marędziak, K. Marycz, K. A. Tomaszewski, K. Kornicka, B. M. Henry, Stem Cells Int. 2016, 2016, 2152435.
H. Elkhenany, L. Amelse, M. Caldwell, R. Abdelwahed, M. Dhar, J. Anim. Sci. Biotechnol. 2016, 7, 16.
S. W. Volk, Y. Wang, K. D. Hankenson, Cell Transplant. 2012, 21, 2189.
C. J. Moran, A. Ramesh, P. A. Brama, J. M. O'Byrne, F. J. O'Brien, T. J. Levingstone, J. Exp. Orthop. 2016, 3, 1.
a) A. Gwynn, J. Microsc. 2000, 197, 159;
b) M. Kääb, I. Ap Gwynn, H. Nötzli, J. Anat. 1998, 193, 23.
a) L. Moroni, J. A. Burdick, C. Highley, S. J. Lee, Y. Morimoto, S. Takeuchi, J. J. Yoo, Nat. Rev. Mater. 2018, 3, 21;
b) J. Vanderburgh, J. A. Sterling, S. A. Guelcher, Ann. Biomed. Eng. 2017, 45, 164.
W. Zhang, B. C. Heng, Y.-Z. Jiang, H.-W. Ouyang, J. Orthop. Translat. 2014, 2, 56.
G. Ebihara, M. Sato, M. Yamato, G. Mitani, T. Kutsuna, T. Nagai, S. Ito, T. Ukai, M. Kobayashi, M. Kokubo, Biomaterials 2012, 33, 3846.
J. M. Coburn, M. Gibson, S. Monagle, Z. Patterson, J. H. Elisseeff, Proc. Natl. Acad. Sci. USA 2012, 109, 10012.
H. V. Almeida, Y. Liu, G. M. Cunniffe, K. J. Mulhall, A. Matsiko, C. T. Buckley, F. J. O'Brien, D. J. Kelly, Acta Biomater. 2014, 10, 4400.
K. Kim, J. Lam, S. Lu, P. P. Spicer, A. Lueckgen, Y. Tabata, M. E. Wong, J. A. Jansen, A. G. Mikos, F. K. Kasper, J. Controlled Release 2013, 168, 166.
R. Reyes, M. Pec, E. Sanchez, C. Del Rosario, A. Delgado, C. Evora, Eur. Cell Mater. 2013, 25, 351.
Q. Wang, H. Zhang, H. Gan, H. Wang, Q. Li, Z. Wang, Int. Orthop. 2018, 42, 1437.

Auteurs

Liangbin Zhou (L)

Musculoskeletal Research Laboratory of Department of Orthopedics & Traumatology, and Innovative Orthopaedic Biomaterial and Drug Translational Research Laboratory of Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong SAR, 999077, China.

Van Osch Gjvm (VO)

Department of Orthopedics and Department of Otorhinolaryngology, Erasmus MC, University Medical Center, Rotterdam, 3000 CA, The Netherlands.
Department of Biomechanical Engineering, Delft University of Technology (TU Delft), Delft, 2600 AA, The Netherlands.

Jos Malda (J)

Department of Orthopaedics of University Medical Center Utrecht, and Department of Clinical Sciences of Faculty of Veterinary Medicine, Utrecht University, Utrecht, 3584 CS, The Netherlands.

Martin J Stoddart (MJ)

AO Research Institute Davos, Clavadelerstrasse 8, Davos, CH 7270, Switzerland.

Yuxiao Lai (Y)

Centre for Translational Medicine Research and Development, Shenzhen Institutes of Advanced Technology, The Chinese Academy of Sciences, Shenzhen, 518000, China.

R Geoff Richards (RG)

AO Research Institute Davos, Clavadelerstrasse 8, Davos, CH 7270, Switzerland.

Kevin Ki-Wai Ho (K)

Musculoskeletal Research Laboratory of Department of Orthopedics & Traumatology, and Innovative Orthopaedic Biomaterial and Drug Translational Research Laboratory of Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong SAR, 999077, China.

Ling Qin (L)

Musculoskeletal Research Laboratory of Department of Orthopedics & Traumatology, and Innovative Orthopaedic Biomaterial and Drug Translational Research Laboratory of Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong SAR, 999077, China.
Centre for Translational Medicine Research and Development, Shenzhen Institutes of Advanced Technology, The Chinese Academy of Sciences, Shenzhen, 518000, China.

Classifications MeSH