Quantitative US Elastography Can Be Used to Quantify Mechanical and Histologic Tendon Healing in a Rabbit Model of Achilles Tendon Transection

Published Online:https://doi.org/10.1148/radiol.2016160695

Quantitative US elastography may be a useful method with which to evaluate tissue healing after Achilles tendon rupture.


To determine the time-dependent change in strain ratios (SRs) at the healing site of an Achilles tendon rupture in a rabbit model of tendon transection and to assess the correlation between SRs and the mechanical and histologic properties of the healing tissue.

Materials and Methods

Experimental methods were approved by the institutional animal care and use committee. The Achilles tendons of 24 New Zealand white rabbits (48 limbs) were surgically transected. The SRs of Achilles tendons were calculated by using compression-based quantitative ultrasonographic elastography measurements obtained 2, 4, 8, and 12 weeks after transection. After in vivo elastography, the left Achilles tendon was harvested for mechanical testing of ultimate load, ultimate stress, elastic modulus, and linear stiffness, and the right tendons were harvested for tissue histologic analysis with the Bonar scale. Time-dependent changes in SRs, mechanical parameters, and Bonar scale scores were evaluated by using repeated-measures analysis of variance. The correlation between SRs and each measured variable was evaluated by using the Spearman rank correlation coefficient.


Mean SRs and Bonar scale values decreased as a function of time after transection, whereas mechanical parameters increased (P < .001). SR correlated with ultimate stress (ρ = 0.68, P <.001,) elastic modulus (ρ = 0.74, P <.001), and the Bonar scale (ρ = 0.87, P <.001).


Quantitative elastography could be a useful method with which to evaluate mechanical and histologic properties of the healing tendon.

© RSNA, 2017

Online supplemental material is available for this article.


  • 1. Raikin SM, Garras DN, Krapchev PV. Achilles tendon injuries in a United States population. Foot Ankle Int 2013;34(4):475–480. Crossref, MedlineGoogle Scholar
  • 2. Huttunen TT, Kannus P, Rolf C, Felländer-Tsai L, Mattila VM. Acute achilles tendon ruptures: incidence of injury and surgery in Sweden between 2001 and 2012. Am J Sports Med 2014;42(10):2419–2423. Crossref, MedlineGoogle Scholar
  • 3. Kannus P, Józsa L. Histopathological changes preceding spontaneous rupture of a tendon. a controlled study of 891 patients. J Bone Joint Surg Am 1991;73(10):1507–1525. Crossref, MedlineGoogle Scholar
  • 4. Holm C, Kjaer M, Eliasson P. Achilles tendon rupture: treatment and complications—a systematic review. Scand J Med Sci Sports 2015;25(1):e1–e10. Crossref, MedlineGoogle Scholar
  • 5. Jiang N, Wang B, Chen A, Dong F, Yu B. Operative versus nonoperative treatment for acute Achilles tendon rupture: a meta-analysis based on current evidence. Int Orthop 2012;36(4):765–773. Crossref, MedlineGoogle Scholar
  • 6. Mortensen HM, Skov O, Jensen PE. Early motion of the ankle after operative treatment of a rupture of the Achilles tendon: a prospective, randomized clinical and radiographic study. J Bone Joint Surg Am 1999;81(7):983–990. Crossref, MedlineGoogle Scholar
  • 7. Möller M, Movin T, Granhed H, Lind K, Faxén E, Karlsson J. Acute rupture of tendon Achillis. a prospective randomised study of comparison between surgical and non-surgical treatment. J Bone Joint Surg Br 2001;83(6):843–848. Crossref, MedlineGoogle Scholar
  • 8. Khan KM, Forster BB, Robinson J, et al. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? a two year prospective study. Br J Sports Med 2003;37(2):149–153. Crossref, MedlineGoogle Scholar
  • 9. Archambault JM, Wiley JP, Bray RC, Verhoef M, Wiseman DA, Elliott PD. Can sonography predict the outcome in patients with achillodynia? J Clin Ultrasound 1998;26(7):335–339. Crossref, MedlineGoogle Scholar
  • 10. De Zordo T, Chhem R, Smekal V, et al. Real-time sonoelastography: findings in patients with symptomatic achilles tendons and comparison to healthy volunteers. Ultraschall Med 2010;31(4):394–400. Crossref, MedlineGoogle Scholar
  • 11. Tan S, Kudaş S, Özcan AS, et al. Real-time sonoelastography of the Achilles tendon: pattern description in healthy subjects and patients with surgically repaired complete ruptures. Skeletal Radiol 2012;41(9):1067–1072. Crossref, MedlineGoogle Scholar
  • 12. Yang Z, Zhang H, Wang K, Cui G, Fu F. Assessment of diffuse thyroid disease by strain ratio in ultrasound elastography. Ultrasound Med Biol 2015;41(11):2884–2889. Crossref, MedlineGoogle Scholar
  • 13. Drakonaki EE, Allen GM, Wilson DJ. Real-time ultrasound elastography of the normal Achilles tendon: reproducibility and pattern description. Clin Radiol 2009;64(12):1196–1202. Crossref, MedlineGoogle Scholar
  • 14. Fujihara Y, Matsumura T, Murayama N. Development of acoustic coupler for elastography. MEDIX 2011;55:40–44. Google Scholar
  • 15. Yamamoto Y, Yamaguchi S, Sasho T, et al. Quantitative ultrasound elastography with an acoustic coupler for Achilles tendon elasticity: measurement repeatability and normative values. J Ultrasound Med 2016;35(1):159–166. Crossref, MedlineGoogle Scholar
  • 16. Fukawa T, Yamaguchi S, Watanabe A, et al. Quantitative assessment of tendon healing by using MR T2 mapping in a rabbit Achilles tendon transection model treated with platelet-rich plasma. Radiology 2015;276(3):748–755. LinkGoogle Scholar
  • 17. Nagasawa K, Noguchi M, Ikoma K, Kubo T. Static and dynamic biomechanical properties of the regenerating rabbit Achilles tendon. Clin Biomech (Bristol, Avon) 2008;23(6):832–838. Crossref, MedlineGoogle Scholar
  • 18. Kapetanos G. The effect of the local corticosteroids on the healing and biomechanical properties of the partially injured tendon. Clin Orthop Relat Res 1982 (163):170–179. Google Scholar
  • 19. Thermann H, Frerichs O, Biewener A, Krettek C. Healing of the Achilles tendon: an experimental study. Foot Ankle Int 2001;22(6):478–483. Crossref, MedlineGoogle Scholar
  • 20. Thermann H, Frerichs O, Holch M, Biewener A. Healing of Achilles tendon, an experimental study: part 2—histological, immunohistological and ultrasonographic analysis. Foot Ankle Int 2002;23(7):606–613. Crossref, MedlineGoogle Scholar
  • 21. Akatsu Y, Yamaguchi S, Mukoyama S, et al. Accuracy of high-resolution ultrasound in the detection of meniscal tears and determination of the visible area of menisci. J Bone Joint Surg Am 2015;97(10):799–806. Crossref, MedlineGoogle Scholar
  • 22. Turan A, Tufan A, Mercan R, et al. Real-time sonoelastography of Achilles tendon in patients with ankylosing spondylitis. Skeletal Radiol 2013;42(8):1113–1118. Crossref, MedlineGoogle Scholar
  • 23. Klauser AS, Miyamoto H, Tamegger M, et al. Achilles tendon assessed with sonoelastography: histologic agreement. Radiology 2013;267(3):837–842. LinkGoogle Scholar
  • 24. De Zordo T, Fink C, Feuchtner GM, Smekal V, Reindl M, Klauser AS. Real-time sonoelastography findings in healthy Achilles tendons. AJR Am J Roentgenol 2009;193(2):W134–W138. Crossref, MedlineGoogle Scholar
  • 25. Frey H. Realtime elastography. a new ultrasound procedure for the reconstruction of tissue elasticity [in German]. Radiologe 2003;43(10):850–855. Crossref, MedlineGoogle Scholar
  • 26. Krouskop TA, Wheeler TM, Kallel F, Garra BS, Hall T. Elastic moduli of breast and prostate tissues under compression. Ultrason Imaging 1998;20(4):260–274. Crossref, MedlineGoogle Scholar
  • 27. Niitsu M, Michizaki A, Endo A, Takei H, Yanagisawa O. Muscle hardness measurement by using ultrasound elastography: a feasibility study. Acta Radiol 2011;52(1):99–105. Crossref, MedlineGoogle Scholar
  • 28. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 1979;86(2):420–428. Crossref, MedlineGoogle Scholar
  • 29. Hugate R, Pennypacker J, Saunders M, Juliano P. The effects of intratendinous and retrocalcaneal intrabursal injections of corticosteroid on the biomechanical properties of rabbit Achilles tendons. J Bone Joint Surg Am 2004;86-A(4):794–801. Crossref, MedlineGoogle Scholar
  • 30. Ilhami K, Gokhan M, Ulukan I, Eray BM, Levent A, Cig˘dem T. Biomechanical and histologic comparison of Achilles tendon ruptures reinforced with intratendinous and peritendinous plantaris tendon grafts in rabbits: an experimental study. Arch Orthop Trauma Surg 2004;124(9):608–613. Crossref, MedlineGoogle Scholar
  • 31. Okamoto N, Kushida T, Oe K, Umeda M, Ikehara S, Iida H. Treating Achilles tendon rupture in rats with bone-marrow-cell transplantation therapy. J Bone Joint Surg Am 2010;92(17):2776–2784. Crossref, MedlineGoogle Scholar
  • 32. Kim HJ, Nam HW, Hur CY, et al. The effect of platelet rich plasma from bone marrow aspirate with added bone morphogenetic protein-2 on the Achilles tendon-bone junction in rabbits. Clin Orthop Surg 2011;3(4):325–331. Crossref, MedlineGoogle Scholar
  • 33. Murray MM, Magarian E, Zurakowski D, Fleming BC. Bone-to-bone fixation enhances functional healing of the porcine anterior cruciate ligament using a collagen-platelet composite. Arthroscopy 2010;26(9,Suppl):S49–S57. Crossref, MedlineGoogle Scholar
  • 34. Cook JL, Feller JA, Bonar SF, Khan KM. Abnormal tenocyte morphology is more prevalent than collagen disruption in asymptomatic athletes’ patellar tendons. J Orthop Res 2004;22(2):334–338. Crossref, MedlineGoogle Scholar
  • 35. Fitzmaurice G, Laird N, Ware J. Applied longitudinal analysis. 2nd ed. New York, NY: Wiley, 2011. CrossrefGoogle Scholar
  • 36. Keppel G, Wickens T. Design and analysis: a researchers handbook. 4th ed. Upper Saddle River, NJ: Pearson Education International, 2004. Google Scholar
  • 37. Itoh A, Ueno E, Tohno E, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006;239(2):341–350. LinkGoogle Scholar
  • 38. Dudea SM, Giurgiu CR, Dumitriu D, et al. Value of ultrasound elastography in the diagnosis and management of prostate carcinoma. Med Ultrason 2011;13(1):45–53. MedlineGoogle Scholar
  • 39. Onur MR, Poyraz AK, Ucak EE, Bozgeyik Z, Özercan IH, Ogur E. Semiquantitative strain elastography of liver masses. J Ultrasound Med 2012;31(7):1061–1067. Crossref, MedlineGoogle Scholar
  • 40. Turan A, Teber MA, Yakut ZI, Unlu HA, Hekimoglu B. Sonoelastographıc assessment of the age-related changes of the Achilles tendon. Med Ultrason 2015;17(1):58–61. Crossref, MedlineGoogle Scholar
  • 41. Martin JA, Biedrzycki AH, Lee KS, et al. In vivo measures of shear wave speed as a predictor of tendon elasticity and strength. Ultrasound Med Biol 2015;41(10):2722–2730. Crossref, MedlineGoogle Scholar
  • 42. Sconfienza LM, Silvestri E, Orlandi D, et al. Real-time sonoelastography of the plantar fascia: comparison between patients with plantar fasciitis and healthy control subjects. Radiology 2013;267(1):195–200. LinkGoogle Scholar
  • 43. Havre RF, Waage JR, Gilja OH, Odegaard S, Nesje LB. Real-time elastography: strain ratio measurements are influenced by the position of the reference area. Ultraschall Med 2011 Jun 10. [Epub ahead of print] Crossref, MedlineGoogle Scholar
  • 44. Oryan A, Moshiri A, Parizi Meimandi A, Silver IA. A long-term in vivo investigation on the effects of xenogenous based, electrospun, collagen implants on the healing of experimentally-induced large tendon defects. J Musculoskelet Neuronal Interact 2013;13(3):353–367. MedlineGoogle Scholar
  • 45. Geremia JM, Bobbert MF, Casa Nova M, et al. The structural and mechanical properties of the Achilles tendon 2 years after surgical repair. Clin Biomech (Bristol, Avon) 2015;30(5):485–492. Crossref, MedlineGoogle Scholar
  • 46. Bleakney RR, Tallon C, Wong JK, Lim KP, Maffulli N. Long-term ultrasonographic features of the Achilles tendon after rupture. Clin J Sport Med 2002;12(5):273–278. Crossref, MedlineGoogle Scholar
  • 47. Grieco PW, Frumberg DB, Weinberg M, Pivec R, Naziri Q, Uribe JA. Biomechanical evaluation of varying the number of loops in a repair of a physiological model of Achilles tendon rupture. Foot Ankle Int 2015;36(4):444–449. Crossref, MedlineGoogle Scholar

Article History

Received March 22, 2016; revision requested May 27; revision received September 16; accepted September 18; final version accepted October 4.
Published online: Jan 31 2017
Published in print: May 2017