Reinforcement of hydrogels using three-dimensionally printed microfibres

Nature Communications

Volumn 6, Issue , 2015, Pages

  Visser, Jetze ^a,b   Melchels, Ferry P W ^a,b   Jeon, June E ^b   Van Bussel, Erik M ^a,b   Kimpton, Laura S ^c   Byrne, Helen M ^c   Dhert, Wouter J A ^a,d   Dalton, Paul D ^b,e   Hutmacher, Dietmar W ^b,f,g   Malda, Jos ^a,b,d  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UTRECHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^g TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 2; ACRYLAMIDE DERIVATIVE; ALGINIC ACID; GLUCURONIC ACID; HEXURONIC ACID; HYDROGEL; METHACRYLAMIDE; POLYCAPROLACTONE; POLYESTER;

GEL; GENE EXPRESSION; POROSITY; THREE-DIMENSIONAL MODELING;

ARTICLE; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL VIABILITY; CELLULAR STRESS RESPONSE; COMPRESSIVE STRENGTH; CONTROLLED STUDY; CROSS LINKING; ELASTICITY; FLOW RATE; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; HYDROPHILICITY; MELT ELECTROSPINNING WRITING; MUSCULOSKELETAL SYSTEM; POROSITY; RIGIDITY; SURFACE AREA; THREE DIMENSIONAL PRINTING; TISSUE REPAIR; TISSUE SCAFFOLD; YOUNG MODULUS; ANIMAL; CELL CULTURE; CHONDROGENESIS; CYTOLOGY; HORSE; PHYSIOLOGY; THEORETICAL MODEL;

ACRYLAMIDES; ALGINATES; ANIMALS; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COMPRESSIVE STRENGTH; ELASTICITY; GLUCURONIC ACID; HEXURONIC ACIDS; HORSES; HUMANS; HYDROGELS; MODELS, THEORETICAL; POLYESTERS; PRINTING, THREE-DIMENSIONAL; TISSUE SCAFFOLDS;

EID: 84929119055     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7933     Document Type: Article

References (52)

1. Seliktar, D. Designing cell-compatible hydrogels for biomedical applications. Science 336, 1124-1128 (2012).
2. Malda, J. et al. 25th anniversary article: engineering hydrogels for biofabrication. Adv. Mater. 25, 5011-5028 (2013).
3. DeForest, C. A. & Anseth, K. S. Advances in bioactive hydrogels to probe and direct cell fate. Annu. Rev. Chem. Biomol. Eng. 3, 421-444 (2012).
4. Hunt, N. C. & Grover, L. M. Cell encapsulation using biopolymer gels for regenerative medicine. Biotechnol Lett. 32, 733-742 (2010).
5. Mastbergen, S. C., Saris, D. B. & Lafeber, F. P. Functional articular cartilage repair: here, near, or is the best approach not yet clear? Nat. Rev. Rheumatol. 9, 277-290 (2013).
6. Ben-David, D. et al. Low dose BMP-2 treatment for bone repair using a PEGylated fibrinogen hydrogel matrix. Biomaterials 34, 2902-2910 (2013).
7. Anseth, K. S., Bowman, C. N. & Brannon-Peppas, L. Mechanical properties of hydrogels and their experimental determination. Biomaterials 17, 1647-1657 (1996).
8. Moutos, F. T., Freed, L. E. & Guilak, F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat. Mater. 6, 162-167 (2007).
9. Coburn, J. M., Gibson, M., Monagle, S., Patterson, Z. & Elisseeff, J. H. Bioinspired nanofibers support chondrogenesis for articular cartilage repair. Proc. Natl Acad. Sci. USA 109, 10012-10017 (2012).
10. Discher, D. E., Janmey, P. & Wang, Y. L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143 (2005).
11. Kouwer, P. H. et al. Responsive biomimetic networks from polyisocyanopeptide hydrogels. Nature 493, 651-655 (2013).
12. Jeon, J. E. et al. Effect of preculture and loading on expression of matrix molecules, matrix metalloproteinases, and cytokines by expanded osteoarthritic chondrocytes. Arthritis Rheum. 65, 2356-2367 (2013).
13. Nguyen, Q. T., Hwang, Y., Chen, A. C., Varghese, S. & Sah, R. L. Cartilage-like mechanical properties of poly (ethylene glycol)-diacrylate hydrogels. Biomaterials 33, 6682-6690 (2012).
14. Levett, P. A. et al. A biomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate. Acta Biomater. 10, 214-223 (2014).
15. Wan, L. Q. et al. Matrix deposition modulates the viscoelastic shear properties of hydrogel-based cartilage grafts. Tissue Eng. 17, 1111-1122 (2011).
16. Abbott, A. Cell culture: biology's new dimension. Nature 424, 870-872 (2003).
17. Shin, S. R. et al. Carbon nanotube reinforced hybrid microgels as scaffold materials for cell encapsulation. ACS Nano 6, 362-372 (2012).
18. Saez-Martinez, V, G.-G., S., Vera, C, Olalde, B, Madarieta, I, Obieta, I & Garagorri, N New hybrid system: poly(ethylene glycol) hydrogel with covalently bonded pegylated nanotubes. J. Appl. Polym. Sci. 120, 124-132 (2010).
19. Maranchi, J. P., Trexler, M. M., Guo, Q. & Elisseeff, J. Fibre-reinforced hydrogels with high optical transparency. Int. Mater. Rev. 59, 264-296 (2014).
20. Yodmuang, S. et al. Silk microfiber-reinforced silk hydrogel composites for functional cartilage tissue repair. Acta Biomater. 11, 27-36 (2015).
21. Moutos, F. T., Estes, B. T. & Guilak, F. Multifunctional hybrid threedimensionally woven scaffolds for cartilage tissue engineering. Macromol. Biosci. 10, 1355-1364 (2010).
22. Liao, I. C., Moutos, F. T., Estes, B. T., Zhao, X. & Guilak, F. Composite three-dimensional woven scaffolds with interpenetrating network hydrogels to create functional synthetic articular cartilage. Adv. Funct. Mater. 23, 5833-5839 (2013).
23. Marijnissen, W. J. et al. Alginate as a chondrocyte-delivery substance in combination with a non-woven scaffold for cartilage tissue engineering. Biomaterials 23, 1511-1517 (2002).
24. Coburn, J. et al. Biomimetics of the extracellular matrix: an integrated threedimensional fiber-hydrogel composite for cartilage tissue engineering. Smart Struct. Syst. 7, 213-222 (2011).
25. Xu, T. et al. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication 5, 015001 (2012).
26. Kim, M. et al. Composite system of PLCL scaffold and heparin-based hydrogel for regeneration of partial-thickness cartilage defects. Biomacromolecules 13, 2287-2298 (2012).
27. Bosworth, L. A., Turner, L. A. & Cartmell, S. H. State of the art composites comprising electrospun fibres coupled with hydrogels: a review. Nanomedicine 9, 322-335 (2013).
28. Pati, F. et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat. Commun. 5, 3935 (2014).
29. Boere, K. W. et al. Covalent attachment of a three-dimensionally printed thermoplast to a gelatin hydrogel for mechanically enhanced cartilage constructs. Acta Biomater. 10, 2602-2611 (2014).
30. Schuurman, W. et al. Bioprinting of hybrid tissue constructs with tailorable mechanical properties. Biofabrication 3, 021001 (2011).
31. Agrawal, A., Rahbar, N. & Calvert, P. D. Strong fiber-reinforced hydrogel. Acta Biomater. 9, 5313-5318 (2013).
32. Cha, C. et al. Structural reinforcement of cell-laden hydrogels with microfabricated three dimensional scaffolds. Biomater. Sci. 2, 703-709 (2014).
33. Lee, H., Ahn, S., Bonassar, L. J. & Kim, G. Cell(MC3T3-E1)-printed Poly(-caprolactone)/alginate hybrid scaffolds for tissue regeneration. Macromol. Rapid Commun. 34, 142-149 (2012).
34. Brown, T. D., Dalton, P. D. & Hutmacher, D. W. Direct writing by way of melt electrospinning. Adv. Mater. 23, 5651-5657 (2011).
35. Farrugia, B. L. et al. Dermal fibroblast infiltration of poly(epsilon-caprolactone) scaffolds fabricated by melt electrospinning in a direct writing mode. Biofabrication 5, 025001 (2013).
36. Schuurman, W. et al. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol. Biosci. 13, 551-561 (2013).
37. Chen, Y. C. et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv. Funct. Mater. 22, 2027-2039 (2012).
38. Hong, W., Zhao, X. H., Zhou, J. X. & Suo, Z. G. A theory of coupled diffusion and large deformation in polymeric gels. J. Mech. Phys. Solids 56, 1779-1793 (2008).
39. Hutmacher, D. W. Scaffolds in tissue engineering bone and cartilage. Biomaterials 21, 2529-2543 (2000).
40. Pham, Q. P., Sharma, U. & Mikos, A. G. Electrospun poly(epsiloncaprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules 7, 2796-2805 (2006).
41. Pierce, D. M., Ricken, T. & Holzapfel, G. A. A hyperelastic biphasic fibrereinforced model of articular cartilage considering distributed collagen fibre orientations: continuum basis, computational aspects and applications. Comput. Methods Biomech. Biomed. Eng. 16, 1344-1361 (2013).
42. Hosseini, S. M., Wilson, W., Ito, K. & van Donkelaar, C. C. How preconditioning affects the measurement of poro-viscoelastic mechanical properties in biological tissues. Biomech. Model Mechanobiol. 13, 503-513 (2014).
43. Athanasiou, K. A., Agarwal, A. & Dzida, F. J. Comparative study of the intrinsic mechanical properties of the human acetabular and femoral head cartilage. J. Orthopaed. Res. 12, 340-349 (1994).
44. Jurvelin, J. S., Buschmann, M. D. & Hunziker, E. B. Optical and mechanical determination of Poisson's ratio of adult bovine humeral articular cartilage. J. Biomech. 30, 235-241 (1997).
45. Chen, A. C., Bae, W. C., Schinagl, R. M. & Sah, R. L. Depth-and straindependent mechanical and electromechanical properties of full-thickness bovine articular cartilage in confined compression. J. Biomech. 34, 1-12 (2001).
46. Visser, J. et al. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication 5, 035007 (2013).
47. Moroni, L., de Wijn, J. R. & van Blitterswijk, C. A. 3D fiber-deposited scaffolds for tissue engineering: influence of pores geometry and architecture on dynamic mechanical properties. Biomaterials 27, 974-985 (2006).
48. Kwan, M. K., Lai, W. M. & Mow, V. C. Fundamentals of fluid transport through cartilage in compression. Ann. Biomed. Eng. 12, 537-558 (1984).
49. Grodzinsky, A. J., Levenston, M. E., Jin, M. & Frank, E. H. Cartilage tissue remodeling in response to mechanical forces. Annu. Rev. Biomed. Eng. 2, 691-713 (2000).
50. Woodruff, M. A. & Hutmacher, D. W. The return of a forgotten polymer-Polycaprolactone in the 21st century. Progr. Polym. Sci. 35, 1217-1256 (2010).
51. Malda, J. et al. Comparative study of depth-dependent characteristics of equine and human osteochondral tissue from the medial and lateral femoral condyles. Osteoarthritis and cartilage/OARS, Osteoarthritis Research Society 20, 1147-1151 (2012).
52. Mansour, J. M. & Welter, J. F. Multimodal evaluation of tissue-engineered cartilage. J. Med. Biol. Eng. 33, 1-16 (2013).