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Low Amplitude Characterization Tests Conducted at Regular Intervals Can Affect Tendon Mechanobiological Response

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Abstract

In bioreactor studies of tissue mechanobiology, characterizing changes in tissue quality is essential for understanding and predicting the response to mechanical stimuli. Unfortunately, current methods are often destructive and cannot be used at regular intervals on the same sample to characterize progression over time. Non-destructive methods such as low amplitude stress relaxation tests could be used, but then, the following dilemma comes into play: how can we accurately measure live tissue progression over time if the tissue is reacting to our measurement methods? In this study, we investigated the hypothesis that stress relaxation tests at physiological amplitudes conducted at regular intervals between stimulation periods do not modify tissue progression over time. Live, healthy tendons were subjected to mechanical stimuli inside a bioreactor for 3 days. The tendons were grouped based on the daily characterization protocol (24 or 0 stress relaxation tests) and their progression over time were compared. Stress relaxation tests at physiological amplitudes modified the tendon response to mechanical stimulation as observed through mechanical and histologic analyses. Possible solutions to eliminate or minimize the effect of stress relaxation tests are to use the mechanical stimuli to characterize tissue progression or to limit the number of stress relaxation tests.

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References

  1. Androjna, C., R. K. Spragg, and K. A. Derwin. Mechanical conditioning of cell-seeded small intestine submucosa: a potential tissue-engineering strategy for tendon repair. Tissue Eng. 13:233–243, 2007.

    Article  CAS  PubMed  Google Scholar 

  2. Arnoczky, S. P., M. Lavagnino, M. Egerbacher, O. Caballero, K. Gardner, and M. A. Shender. Loss of homeostatic strain alters mechanostat ‘‘set point’’ of tendon cells in vitro. Clin. Orthop. Relat. Res. 466:1583–1591, 2008.

    Article  PubMed  Google Scholar 

  3. Bao, G., and S. Suresh. Cell and molecular mechanics of biological materials. Nat. Mater. 2:715–725, 2003.

    Article  CAS  PubMed  Google Scholar 

  4. Bruneau, A., C. Champagne, P. Cousineau-Pelletier, G. Parent, and E. Langelier. Preparation of rat tail tendons for biomechanical and mechanobiological studies. J. Vis. Exp. 41, 2010. DOI:10.3791/2176.

  5. Cook, J., J. Feller, S. Bonar, and K. Khan. Abnormal tenocyte morphology is more prevalent than collagen disruption in asymptomatic athletes’ patellar tendons. J. Orthop. Res. 22:334–338, 2004.

    Article  CAS  PubMed  Google Scholar 

  6. Cousineau-Pelletier, P., and E. Langelier. Relative contributions of mechanical degradation, enzymatic degradation and repair of the extracellular matrix on the response of tendons when subjected to under- and over- mechanical stimulations in vitro. J. Orthop. Res. 28:204–210, 2010.

    PubMed  Google Scholar 

  7. Devkota, A. C., M. Tsuzaki, L. C. Almekinders, A. J. Banes, and P. S. Weinhold. Distributing a fixed amount of cyclic loading to tendon explants over longer periods induces greater cellular and mechanical responses. J. Orthop. Res. 25:1078–1086, 2007.

    Article  PubMed  Google Scholar 

  8. Duenwald, S. E., R. Vanderby, Jr., and R. S. Lakes. Viscoelastic relaxation and recovery of tendon. Ann. Biomed. Eng. 37:1131–1140, 2009.

    Article  PubMed  Google Scholar 

  9. Egerbacher, M., S. P. Arnoczky, O. Caballero, M. Lavagnino, and K. L. Gardner. Loss of homeostatic tension induces apoptosis in tendon cells: an in vitro study. Clin. Orthop. Relat. Res. 466:1562–1568, 2008.

    Article  PubMed  Google Scholar 

  10. Fearon, A., J. E. Dahlstrom, J. Twin, J. Cook, and A. Scott. The Bonar score revisited: Region of evaluation significantly influences the standardized assessment of tendon degeneration. J. Sci. Med. Sport, 2013. DOI:10.1016/j.jsams.2013.07.008.

  11. Freed, L. E., F. Guilak, X. E. Guo, M. L. Gray, R. Tranquillo, J. W. Holmes, M. Radisic, M. V. Sefton, D. Kaplan, and G. Vunjak-Novakovi. Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. Tissue Eng. 12:3285–3305, 2006.

    Article  CAS  PubMed  Google Scholar 

  12. Gardner, K., M. Lavagnino, M. Egerbacher, and S. P. Arnoczky. Re-establishment of cytoskeletal tensional homeostasis in lax tendons occurs through an actin-mediated cellular contraction of the extracellular matrix. J. Orthop. Res. 30:1695–1701, 2012.

    Article  CAS  PubMed  Google Scholar 

  13. Guilak, F., D. L. Butler, S. A. Goldstein, and D. J. Mooney. Functional Tissue Engineering. New York: Springer-Verlag, p. 426, 2003.

    Book  Google Scholar 

  14. Kortsmit, J., N. J. Driessen, M. C. Rutten, and F. P. Baaijens. Nondestructive and noninvasive assessment of mechanical properties in heart valve tissue engineering. Tissue Eng. Part A 15:797–806, 2009.

    Article  CAS  PubMed  Google Scholar 

  15. Langelier, E., and M. D. Buschmann. Increasing strain and strain rate strengthen transient stiffness but weaken the response to subsequent compression for articular cartilage in unconfined compression. J. Biomech. 36:853–859, 2003.

    Article  PubMed  Google Scholar 

  16. Lujann, T. J., K. M. Wirtz, C. S. Bahney, S. M. Madey, B. Johnstone, and M. Bottlang. A novel bioreactor for the dynamic stimulation and mechanical evaluation of multiple tissue-engineered constructs. Tissue Eng. C 17:367–374, 2011.

    Article  Google Scholar 

  17. Maffulli, N., U. G. Longo, F. Franceschi, C. Rabitti, and V. Denaro. Movin and Bonar scores assess the same characteristics of tendon histology. Clin. Orthop. Relat. Res. 466:1605–1611, 2008.

    Article  PubMed  Google Scholar 

  18. McCulloch, A. D., A. B. Harris, C. E. Sarraf, and M. Eastwood. New multi-cue bioreactor for tissue engineering of tubular cardiovascular samples under physiological conditions. Tissue Eng. 10:565–573, 2004.

    Article  CAS  PubMed  Google Scholar 

  19. Parent, G., M. Cyr, F. Desbiens-Blais, and E. Langelier. Bias and precision of algorithms in estimating cross-sectional area of rat tail tendons. Meas. Sci. Technol. 10:100–102, 2010. doi:10.1088/0957-0233/21/12/125802.

    Google Scholar 

  20. Parent, G., N. Huppé, and E. Langelier. Low Stress Tendon Fatigue is a Relatively Rapid Process in the Context of Overuse Injuries. Ann. Biomed. Eng. 39:1535–1545, 2011.

    Article  PubMed  Google Scholar 

  21. Preiss-Bloom, O., J. Mizrahi, J. Elisseeff, and D. Seliktar. Real-time monitoring of force response measured in mechanically stimulated tissue-engineered cartilage. Artif. Organs 33:318–327, 2009.

    Article  CAS  PubMed  Google Scholar 

  22. Schulz, R. M., N. Wüstneck, C. C. van Donkelaar, J. C. Shelton, and A. Bader. Development and validation of a novel bioreactor system for load- and perfusion-controlled tissue engineering of chondrocyte-constructs. Biotechnol. Bioeng. 101:714–728, 2008.

    Article  CAS  PubMed  Google Scholar 

  23. Scott, A., J. L. Cook, D. A. Hart, D. C. Walker, V. Duronio, and K. M. Khan. Tenocyte responses to mechanical loading in vivo: a role for local insulin-like growth factor 1 signaling in early tendinosis in rats. Arthritis Rheum. 56:871–881, 2007.

    Article  CAS  PubMed  Google Scholar 

  24. Solomonow, M. Time dependent spine stability: the wise old man and the six blind elephants. Clin. Biomech. (Bristol, Avon). 26:219–228, 2011.

    Article  PubMed  Google Scholar 

  25. Tran, S. C., A. J. Cooley, and S. H. Elder. Effect of a mechanical stimulation bioreactor on tissue engineered, scaffold-free cartilage. Biotechnol. Bioeng., 2011. DOI:10.1002/bit.23061.

  26. van der Meulen, M. C., and R. Huiskes. Why mechanobiology? A survey article. J. Biomech. 35:401–414, 2002.

    Article  PubMed  Google Scholar 

  27. Wang, J. H. Mechanobiology of tendon. J. Biomech. 39:1563–1582, 2006.

    Article  PubMed  Google Scholar 

  28. Wang, J. H., and B. P. Thampatty. An introductory review of cell mechanobiology. Biomech. Model. Mechanobiol. 5:1–16, 2006.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Fonds québécois de recherche sur la nature et les technologies and a CIRUS scholarship awarded to Leila Jafari. We thank Debbie Tacium for the English proofreading.

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We have nothing to disclose.

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Authors and Affiliations

  1. Department of Mechanical Engineering, Université de Sherbrooke, Sherbrooke, QC, J1K 2R1, Canada

    Leila Jafari, Yoan Lemieux-LaNeuville & Eve Langelier

  2. Department of Kinanthropology, Université de Sherbrooke, Sherbrooke, QC, J1K 2R1, Canada

    Yoan Lemieux-LaNeuville & Denis Gagnon

Authors
  1. Leila Jafari
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  2. Yoan Lemieux-LaNeuville
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  3. Denis Gagnon
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  4. Eve Langelier
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Corresponding author

Correspondence to Eve Langelier.

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Associate Editor Catherine Disselhorst-Klug oversaw the review of this article.

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Jafari, L., Lemieux-LaNeuville, Y., Gagnon, D. et al. Low Amplitude Characterization Tests Conducted at Regular Intervals Can Affect Tendon Mechanobiological Response. Ann Biomed Eng 42, 589–599 (2014). https://doi.org/10.1007/s10439-013-0916-1

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  • DOI: https://doi.org/10.1007/s10439-013-0916-1

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