Skip to main content

Advertisement

Log in

Type I Collagen-Based Fibrous Capsule Enhances Integration of Tissue-Engineered Cartilage with Native Articular Cartilage

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Successful integration of engineered constructs with host tissues is crucial for cartilage repair, yet achieving it remains challenging. A collagen I-based fibrous capsule characterized by increased cell density and decreased glycosaminoglycan deposition usually forms at the periphery of tissue-engineered cartilage. The current study aimed to evaluate the effects of a solid fibrous capsule on construct integration with native articular cartilage. To this end, capsule-containing (CC) and capsule-free (CF) constructs were grown by culturing chondrocyte-seeded scaffolds with insulin-like growth factor-1 and transforming growth factor-β1, respectively, in a wavy-walled bioreactor that imparts hydrodynamic forces for 4 weeks. The ability of harvested constructs to integrate with native cartilage was determined using a cartilage explant model. Our results revealed that adhesive stress between native cartilage and the CC constructs was 57% higher than that in the CF group, potentially due to the absence of glycosaminoglycans and increased cell density in the capsule region and deposition of denser and thicker collagen fibrils at the integration site. The present work demonstrates that the fibrous capsule can effectively enhance early integration of engineered and native cartilage tissues and thus suggests the need to include the capsule as a variable in the development of cartilage tissue engineering strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Ahsan, T., and R. L. Sah. Biomechanics of integrative cartilage repair. Osteoarthr. Cartilage 7:29–40, 1999.

    Article  CAS  Google Scholar 

  2. Andres, B. M., S. C. Mears, and J. F. Wenz. Surgical treatment options for cartilage defects within the knee. Orthop. Nurs. 20:27–31, 2001.

    Article  CAS  PubMed  Google Scholar 

  3. Bueno, E. M., B. Bilgen, and G. A. Barabino. Wavy-walled bioreactor supports increased cell proliferation and matrix deposition in engineered cartilage constructs. Tissue Eng. 11:1699–1709, 2005.

    Article  CAS  PubMed  Google Scholar 

  4. Dimicco, M. A., S. N. Waters, W. H. Akeson, and R. L. Sah. Integrative articular cartilage repair: dependence on developmental stage and collagen metabolism. Osteoarthr. Cartilage 10:218–225, 2002.

    Article  CAS  Google Scholar 

  5. Djouad, F., L. Rackwitz, Y. Song, S. Janjanin, and R. S. Tuan. ERK1/2 activation induced by inflammatory cytokines compromises effective host tissue integration of engineered cartilage. Tissue Eng. Part A 15:2825–2835, 2009.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Gilbert, S. J., S. K. Singhrao, I. M. Khan, L. G. Gonzalez, B. M. Thomson, D. Burdon, V. C. Duance, and C. W. Archer. Enhanced tissue integration during cartilage repair in vitro can be achieved by inhibiting chondrocyte death at the wound edge. Tissue Eng. Part A 15:1739–1749, 2009.

    Article  CAS  PubMed  Google Scholar 

  7. Hand, C. J., J. J. A. Lobo, L. M. White, and A. Miniaci. Osteochondral autograft resurfacing. Sports Med. Arthrosc. Rev. 11:245–263, 2003.

    Article  Google Scholar 

  8. Hunter, C. J., and M. E. Levenston. Maturation and integration of tissue-engineered cartilages within an in vitro defect repair model. Tissue Eng. 10:736–746, 2004.

    Article  CAS  PubMed  Google Scholar 

  9. Ignotz, R. A., and J. Massagué. Transforming growth factor-β stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261:4337–4345, 1986.

    CAS  PubMed  Google Scholar 

  10. Jürgensen, K., D. Aeschlimann, V. Cavin, M. Genge, and E. B. Hunziker. A new biological glue for cartilage–cartilage interfaces: tissue transglutaminase. J. Bone Joint Surg. Am. 79:185–193, 1997.

    PubMed  Google Scholar 

  11. Kelly, T.-A. N., M. B. Fisher, E. S. Oswald, T. Tai, R. L. Mauck, G. A. Ateshian, and C. T. Hung. Low-serum media and dynamic deformational loading in tissue engineering of articular cartilage. Ann. Biomed. Eng. 36:769–779, 2008.

    Article  PubMed  Google Scholar 

  12. Khan, I. M., S. J. Gilbert, S. K. Singhrao, V. C. Duance, and C. W. Archer. Cartilage integration: evaluation of the reasons for failure of integration during cartilage repair. A review. Eur. Cell. Mater. 16:26–39, 2008.

    CAS  PubMed  Google Scholar 

  13. Kisiday, J. D., B. Kurz, M. A. Dimicco, and A. J. Grodzinsky. Evaluation of medium supplemented with insulin-transferrin-selenium for culture of primary bovine calf chondrocytes in three-dimensional hydrogel scaffolds. Tissue Eng. 11:141–151, 2005.

    Article  CAS  PubMed  Google Scholar 

  14. Knutsen, G., L. Engebretsen, T. C. Ludvigsen, J. O. Drogset, T. Grøntvedt, E. Solheim, T. Strand, S. Roberts, V. Isaksen, and O. Johansen. Autologous chondrocyte implantation compared with microfracture in the knee. J. Bone Joint Surg. Am. 86:455–464, 2004.

    PubMed  Google Scholar 

  15. Lee, M. C., K. L. P. Sung, M. S. Kurtis, W. H. Akeson, and R. L. Sah. Adhesive force of chondrocytes to cartilage: effects of chondroitinase ABC. Clin. Orthop. Relat. Res. 370:286–294, 2000.

    Article  PubMed  Google Scholar 

  16. Lohmann, C. H., Z. Schwartz, G. G. Niederauer, D. L. Carnes, D. D. Dean, and B. D. Boyan. Pretreatment with platelet derived growth factor-bb modulates the ability of costochondral resting zone chondrocytes incorporated into PLA/PGA scaffolds to form new cartilage in vivo. Biomaterials 21:49–61, 2000.

    Article  CAS  PubMed  Google Scholar 

  17. Moretti, M., D. Wendt, D. Schaefer, M. Jakob, E. B. Hunziker, M. Heberer, and I. Martin. Structural characterization and reliable biomechanical assessment of integrative cartilage repair. J. Biomech. 38:1846–1854, 2005.

    Article  CAS  PubMed  Google Scholar 

  18. Moyer, H. R., Y. Wang, T. Farooque, T. Wick, K. A. Singh, L. Xie, R. E. Guldberg, J. K. Williams, B. D. Boyan, and Z. Schwartz. A new animal model for assessing cartilage repair and regeneration at a nonarticular site. Tissue Eng. Part A 16:2321–2330, 2010.

    Article  CAS  PubMed  Google Scholar 

  19. Obradovic, B., I. Martin, R. F. Padera, S. Treppo, L. E. Freed, and G. Vunjak-Navakovic. Integration of engineered cartilage. J. Orthop. Res. 19:1089–1097, 2001.

    Article  CAS  PubMed  Google Scholar 

  20. Peretti, G. M., V. Campo-Ruiz, S. Gonzalez, M. A. Randolph, J. Wei Xu, K. R. Morse, R. E. Roses, and M. J. Yaremchuk. Tissue engineered cartilage integration to live and devitalized cartilage: a study by reflectance mode confocal microscopy and standard histology. Connect. Tissue Res. 47:190–199, 2006.

    Google Scholar 

  21. Peretti, G. M., V. Zaporojan, K. M. Spangenberg, M. A. Randolph, J. Fellers, and L. J. Bonassar. Cell-based bonding of articular cartilage: an extended study. J. Biomed. Mater. Res. A 64A:517–524, 2003.

    Article  CAS  Google Scholar 

  22. Sgaglione, N. A., A. Miniaci, S. D. Gillogly, and T. R. Carter. Update on advanced surgical techniques in the treatment of traumatic focal articular cartilage lesions in the knee. Arthroscopy 18:9–32, 2002.

    Article  PubMed  Google Scholar 

  23. Shapiro, F., S. Koide, and M. J. Glimcher. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J. Bone Joint Surg. Am. 75:532–553, 1993.

    CAS  PubMed  Google Scholar 

  24. Silverman, R. P., L. Bonasser, D. Passaretti, M. A. Randolph, and M. J. Yaremchuk. Adhesion of tissue-engineered cartilage to native cartilage. Plast. Reconstr. Surg. 105:1393–1398, 2000.

    CAS  PubMed  Google Scholar 

  25. Tew, S. R., A. P. L. Kwan, A. Hann, B. M. Thomson, and C. W. Archer. The reactions of articular cartilage to experimental wounding: role of apoptosis. Arthritis Rheum. 43:215–225, 2000.

    Article  CAS  PubMed  Google Scholar 

  26. Theodoropoulos, J., J. De Croos, S. Park, R. Pilliar, and R. Kandel. Integration of tissue-engineered cartilage with host cartilage: an in vitro model. Clin. Orthop. Relat. Res. 469:2785–2795, 2011.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Tognana, E., F. Chen, R. F. Padera, H. A. Leddy, S. E. Christensen, F. Guilak, G. Vunjak-Novakovic, and L. E. Freed. Adjacent tissues (cartilage, bone) affect the functional integration of engineered calf cartilage in vitro. Osteoarthr. Cartilage 13:129–138, 2005.

    Article  CAS  Google Scholar 

  28. Tsao, Y. D., and S. R. Gonda. A new technology for three-dimensional cell culture: the hydrodynamic focusing bioreactor. Adv. Heat Mass Transf. Biotechnol. 44:37–38, 1999.

    Google Scholar 

  29. Vinardell, T., S. Thorpe, C. Buckley, and D. Kelly. Chondrogenesis and integration of mesenchymal stem cells within an in vitro cartilage defect repair model. Ann. Biomed. Eng. 37:2556–2565, 2009.

    Article  CAS  PubMed  Google Scholar 

  30. Vunjak-Novakovic, G., L. E. Freed, R. J. Biron, and R. Langer. Effects of mixing on the composition and morphology of tissue-engineered cartilage. AIChE J. 42:850–860, 1996.

    Article  CAS  Google Scholar 

  31. Vunjak-Novakovic, G., I. Martin, B. Obradovic, S. Treppo, A. J. Grodzinsky, R. Langer, and L. E. Freed. Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage. J. Orthop. Res. 17:130–138, 1999.

    Article  CAS  PubMed  Google Scholar 

  32. Yang, Y.-H., and G. A. Barabino. Requirement for serum in medium supplemented with insulin-transferrin-selenium for hydrodynamic cultivation of engineered cartilage. Tissue Eng. Part A 17:2025–2035, 2011.

    Article  CAS  PubMed  Google Scholar 

  33. Yang, Y.-H., and G. A. Barabino. Differential morphology and homogeneity of tissue-engineered cartilage in hydrodynamic cultivation with transient exposure to insulin-like growth factor-1 and transforming growth factor-β1. Tissue Eng. Part A 19:2349–2360, 2013.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Science Foundation [NSF0602608].

Conflict of interest

No competing financial interests exist.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gilda A. Barabino.

Additional information

Associate Editor Michael S. Detamore oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, YH., Ard, M.B., Halper, J.T. et al. Type I Collagen-Based Fibrous Capsule Enhances Integration of Tissue-Engineered Cartilage with Native Articular Cartilage. Ann Biomed Eng 42, 716–726 (2014). https://doi.org/10.1007/s10439-013-0958-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-013-0958-4

Keywords

Navigation