Skip to main content

Advertisement

SpringerLink
Log in

Temporal Healing in Rat Achilles Tendon: Ultrasound Correlations

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

Abstract

The purpose of this study was to explore whether a new ultrasound-based technique correlates with mechanical and biological metrics that describe the tendon healing. Achilles tendons in 32 rats were unilaterally transected and allowed to heal without repair. At 7, 9, 14, or 29 days post-injury, tendons were collected and examined for healing via ultrasound image analysis, mechanical testing, and immunohistochemistry. Consistent with previous studies, we observe that the healing tendons are mechanically inferior (ultimate stress, ultimate load, and normalized stiffness) and biologically altered (cellular and ECM factors) compared to contralateral controls with an incomplete recovery over healing time. Unique to this study, we report: (1) Echo intensity (defined by gray-scale brightness in the ultrasound image) in the healing tissue is related to stress and normalized stiffness. (2) Elongation to failure is relatively constant so that tissue normalized stiffness is linearly correlated with ultimate stress. Together, 1 and 2 suggest a method to quantify mechanical compromise in healing tendons. (3) The amount and type of collagen in healing tendons associates with their strength and normalized stiffness as well as their ultrasound echo intensity. (4) A significant increase of periostin in the healing tissues suggests an important but unexplored role for this ECM protein in tendon healing.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Abrahams, M. Mechanical behaviour of tendon in vitro. A preliminary report. Med. Biol. Eng. 5:433–443, 1967.

    Article  PubMed  CAS  Google Scholar 

  2. Chamberlain, C. S., S. H. Brounts, D. G. Sterken, K. I. Rolnick, G. S. Baer, and R. Vanderby. Gene profiling of the rat medial collateral ligament during early healing using microarray analysis. J. Appl. Physiol. 111:552–565, 2011.

    Article  PubMed  CAS  Google Scholar 

  3. Chamberlain, C. S., E. M. Crowley, H. Kobayashi, K. W. Eliceiri, and R. Vanderby. Quantification of collagen organization and extracellular matrix factors within the healing ligament. Microsc. Microanal. 17:779–787, 2011.

    Article  PubMed  CAS  Google Scholar 

  4. Chamberlain, C. S., E. Crowley, and R. Vanderby. The spatio-temporal dynamics of ligament healing. Wound Repair Regen. 17:206–215, 2009.

    Article  PubMed  Google Scholar 

  5. Cohen, R. E., C. J. Hooley, and N. G. McCrum. Viscoelastic creep of collagenous tissue. J. Biomech. 9:175–184, 1976.

    Article  PubMed  CAS  Google Scholar 

  6. Duenwald, S., H. Kobayashi, K. Frisch, R. Lakes, and R. Vanderby, Jr. Ultrasound echo is related to stress and strain in tendon. J. Biomech. 44:424–429, 2011.

    Article  PubMed  Google Scholar 

  7. Eliasson, P., A. Fahlgren, B. Pasternak, and P. Aspenberg. Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J. Appl. Physiol. 103:459–463, 2007.

    Article  PubMed  Google Scholar 

  8. Hughes, D. S., and J. L. Kelly. Second-order elastic deformation of solids. Phys. Rev. 92:1145–1149, 1953.

    Article  Google Scholar 

  9. Ker, R. F. Mechanics of tendon, from an engineering perspective. Int. J. Fatigue 29:1001–1009, 2007.

    Article  CAS  Google Scholar 

  10. Kobayashi, H., and R. Vanderby. New strain energy function for acoustoelastic analysis of dilatational waves in nearly incompressible, hyper-elastic materials. Transactions of the ASME. J. Appl. Mech. 72:843–851, 2005.

    Article  Google Scholar 

  11. Kobayashi, H., and R. Vanderby. Acoustoelastic analysis of reflected waves in nearly incompressible, hyper-elastic materials: forward and inverse problems. J. Acoust. Soc. Am. 121:879–887, 2007.

    Article  PubMed  Google Scholar 

  12. Levenson, S. M., E. F. Geever, L. V. Crowley, J. F. Oates, 3rd, C. W. Berard, and H. Rosen. The healing of rat skin wounds. Ann. Surg. 161:293–308, 1965.

    Article  PubMed  CAS  Google Scholar 

  13. Lin, T. W., L. Cardenas, and L. J. Soslowsky. Biomechanics of tendon injury and repair. J. Biomech. 37:865–877, 2004.

    Article  PubMed  Google Scholar 

  14. Maganaris, C. N., and J. P. Paul. In vivo human tendon mechanical properties. J. Physiol. 521(Pt 1):307–313, 1999.

    Article  PubMed  CAS  Google Scholar 

  15. Maganaris, C. N., and J. P. Paul. In vivo human tendinous tissue stretch upon maximum muscle force generation. J. Biomech. 33:1453–1459, 2000.

    Article  PubMed  CAS  Google Scholar 

  16. Okotie, G., S. Duenwald-Kuehl, H. Kobayashi, M. J. Wu, and R. Vanderby. Tendon strain measurements with dynamic ultrasound images: evaluation of digital image correlation. J. Biomech. Eng. 134:024504, 2012.

    Article  PubMed  Google Scholar 

  17. Provenzano, P. P., K. Hayashi, D. N. Kunz, M. D. Markel, and R. Vanderby, Jr. Healing of subfailure ligament injury: comparison between immature and mature ligaments in a rat model. J. Orthop. Res. 20:975–983, 2002.

    Article  PubMed  Google Scholar 

  18. Rigby, B. J., N. Hirai, J. D. Spikes, and H. Eyring. The mechanical properties of rat tail tendon. J. Gen. Physiol. 43:265–283, 1959.

    Article  PubMed  CAS  Google Scholar 

  19. Samani, A., J. Zubovits, and D. Plewes. Elastic moduli of normal and pathological human breast tissues: an inversion-technique-based investigation of 169 samples. Phys. Med. Biol. 52:1565–1576, 2007.

    Article  PubMed  Google Scholar 

  20. Skovoroda, A. R., S. Y. Emelianov, M. A. Lubinski, A. P. Sarvazyan, and M. O’Donnell. Theoretical analysis and verification of ultrasound displacement and strain imaging. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 41:302–313, 1994.

    Article  Google Scholar 

  21. Skovoroda, A. R., S. Y. Emelianov, and M. O’Donnell. Tissue elasticity reconstruction based on ultrasonic displacement and strain images. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 42:747–765, 1995.

    Article  Google Scholar 

  22. Suchak, A. A., G. Bostick, D. Reid, S. Blitz, and N. Jomha. The incidence of Achilles tendon ruptures in Edmonton, Canada. Foot Ankle Int. 26:932–936, 2005.

    PubMed  Google Scholar 

  23. Thermann, H., O. Frerichs, M. Holch, and A. Biewener. Healing of Achilles tendon, an experimental study: part 2—histological, immunohistological and ultrasonographic analysis. Foot Ankle Int. 23:606–613, 2002.

    PubMed  CAS  Google Scholar 

  24. Zhang, F., H. Liu, F. Stile, M. P. Lei, Y. Pang, T. M. Oswald, J. Beck, W. Dorsett-Martin, and W. C. Lineaweaver. Effect of vascular endothelial growth factor on rat Achilles tendon healing. Plast. Reconstr. Surg. 112:1613–1619, 2003.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Authors wish to thank Kevin I. Rolnick, David G. Sterken, Paul Lund, Kayt E. Frisch, Ph.D., Hirohito Kobayashi, Ph.D., and Ron McCabe for their technical assistance. Financial support was provided by the National Institutes of Health (NIH), Grant No. AR049266 and AR059916. Ray Vanderby holds intellectual property on some aspects of the ultrasound technique. Authors acknowledge Echometrix, LLC (Madison, WI, USA) for use of ultrasound analysis software.

Author information

Authors and Affiliations

  1. Department of Orthopedics and Rehabilitation, University of Wisconsin, 1111 Highland Ave., 5059 WIMR, Madison, WI, 53705, USA

    Connie S. Chamberlain, Geoffrey S. Baer & Ray Vanderby

  2. Department of Biomedical Engineering, University of Wisconsin, Madison, WI, 53705, USA

    Sarah E. Duenwald-Kuehl, Gregory Okotie & Ray Vanderby

  3. Department of Veterinary Medicine Surgical Sciences, University of Wisconsin, Madison, WI, 53705, USA

    Sabrina H. Brounts

Authors
  1. Connie S. Chamberlain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah E. Duenwald-Kuehl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregory Okotie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sabrina H. Brounts
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Geoffrey S. Baer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ray Vanderby
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ray Vanderby.

Additional information

Associate Editor Kent Leach oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chamberlain, C.S., Duenwald-Kuehl, S.E., Okotie, G. et al. Temporal Healing in Rat Achilles Tendon: Ultrasound Correlations. Ann Biomed Eng 41, 477–487 (2013). https://doi.org/10.1007/s10439-012-0689-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-012-0689-y

Keywords

Search

Navigation