Skeletal Radiology

, Volume 46, Issue 12, pp 1643–1655 | Cite as

Ultrasound elastography in tendon pathology: state of the art

  • Romain Domenichini
  • Jean-Baptiste Pialat
  • Andrea Podda
  • Sébastien Aubry
Review Article
  • 962 Downloads

Abstract

Elastography assesses the biomechanical and structural properties of tissues by measuring their stiffness. Despite promising results, elastography has not yet earned its place in the daily practice of musculoskeletal radiologists. The purpose of this article is to present and examine the data available to date on ultrasound elastography of the tendons through a review of the literature to provide musculoskeletal radiologists with an overview that may help them better understand and use elastography routinely. The most common techniques in ultrasound elastography are described. Then, the aspects of the physiologic and pathologic tendon are presented and discussed. One must make this technique one’s own to better apprehend its contribution to the musculoskeletal imaging field, while bearing in mind that further research will be required before admitting elastography as a reliable and validated tool able to optimize our daily clinical practice.

Keywords

Elastosonography, ultrasound, elastography Tendinopathy Shear-wave elastography Quasi-static elastography Strain elastography 

References

  1. 1.
    Pallwein L, Mitterberger M, Struve P, Pinggera G, Horninger W, Bartsch G, et al. Real-time elastography for detecting prostate cancer: preliminary experience. BJU International Blackwell Publishing Ltd. 2007;100:42–6.CrossRefGoogle Scholar
  2. 2.
    Zhu Q-L, Jiang Y-X, Liu J-B, Liu H, Sun Q, Dai Q, et al. Real-time ultrasound elastography: its potential role in assessment of breast lesions. Ultrasound Med Biol. 2008;34:1232–8.CrossRefPubMedGoogle Scholar
  3. 3.
    Rubaltelli L, Corradin S, Dorigo A, Stabilito M, Tregnaghi A, Borsato S, et al. Differential diagnosis of benign and malignant thyroid nodules at elastosonography. Ultraschall Med. © Georg Thieme Verlag KG Stuttgart ·New York; 2009;30:175–9.Google Scholar
  4. 4.
    Gennisson J-L, Deffieux T, Fink M, Tanter M. Ultrasound elastography: principles and techniques. Diagn Interv Imaging. 2013;94:487–95.CrossRefPubMedGoogle Scholar
  5. 5.
    Ophir J, Céspedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason imaging. SAGE PublicationsSage CA: Los Angeles. CA. 1991;13:111–34.Google Scholar
  6. 6.
    Klauser AS, Miyamoto H, Bellmann-Weiler R, Feuchtner GM, Wick MC, Jaschke WR. Sonoelastography: musculoskeletal applications. Radiology. Radiological Society of North America. 2014;272:622–33.Google Scholar
  7. 7.
    Ponnekanti H, Ophir J, Huang Y, Céspedes I. Fundamental mechanical limitations on the visualization of elasticity contrast in elastography. Ultrasound Med Biol. 1995;21:533–43.CrossRefPubMedGoogle Scholar
  8. 8.
    Franchi-Abella S, Elie C, Corréas JM. Ultrasound elastography: advantages, limitations and artefacts of the different techniques from a study on a phantom. Diagn Interv Imaging. 2013;94:497–501.CrossRefPubMedGoogle Scholar
  9. 9.
    Klauser AS, Faschingbauer R, Jaschke WR. Is sonoelastography of value in assessing tendons? Semin Musculoskelet Radiol. 2010;14:323–33.CrossRefPubMedGoogle Scholar
  10. 10.
    Schneebeli A, Del Grande F, Vincenzo G, Cescon C, Clijsen R, Biordi F, et al. Real-time sonoelastography using an external reference material: test-retest reliability of healthy Achilles tendons. Skeletal Radiol. 5 ed. Springer Berlin Heidelberg; 2016;45:1045–52.Google Scholar
  11. 11.
    Li Y, Snedeker JG. Elastography: modality-specific approaches, clinical applications, and research horizons. Skeletal Radiol Springer-Verlag. 2011;40:389–97.CrossRefGoogle Scholar
  12. 12.
    Goertz RS, Zopf Y, Jugl V, Heide R, Janson C, Strobel D, et al. Measurement of liver elasticity with acoustic radiation force impulse (ARFI) technology: an alternative noninvasive method for staging liver fibrosis in viral hepatitis. Ultraschall Med. 2010;31:151–5.CrossRefPubMedGoogle Scholar
  13. 13.
    Tozaki M, Isobe S, Fukuma E. Preliminary study of ultrasonographic tissue quantification of the breast using the acoustic radiation force impulse (ARFI) technology. Eur J Radiol. 2011;80:e182–7.CrossRefPubMedGoogle Scholar
  14. 14.
    Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control. 2004;51:396–409.CrossRefPubMedGoogle Scholar
  15. 15.
    Parker KJ, Fu D, Graceswki SM, Yeung F, Levinson SF. Vibration sonoelastography and the detectability of lesions. Ultrasound Med Biol. 1998;24:1437–47.CrossRefPubMedGoogle Scholar
  16. 16.
    Brum J, Bernal M, Gennisson J-L, Tanter M. In vivo evaluation of the elastic anisotropy of the human Achilles tendon using shear wave dispersion analysis. Phys Med Biol IOP Publishing. 2014;59:505–23.CrossRefGoogle Scholar
  17. 17.
    O’Brien M. The anatomy of the Achilles tendon. Foot Ankle Clin. 2005;10:225–38.CrossRefPubMedGoogle Scholar
  18. 18.
    Cortez CD, Hermitte L, Ramain A, Mesmann C, Lefort T, Pialat JB. Ultrasound shear wave velocity in skeletal muscle: a reproducibility study. Diagn Interv Imaging. 2016;97:71–9.CrossRefPubMedGoogle Scholar
  19. 19.
    Dubois G, Kheireddine W, Vergari C, Bonneau D, Thoreux P, Rouch P, et al. Reliable protocol for shear wave elastography of lower limb muscles at rest and during passive stretching. Ultrasound Med Biol. 2015;41:2284–91.CrossRefPubMedGoogle Scholar
  20. 20.
    Drakonaki EE, Allen GM, Wilson DJ. Real-time ultrasound elastography of the normal Achilles tendon: reproducibility and pattern description. Clin Radiol Elsevier. 2009;64:1196–202.CrossRefGoogle Scholar
  21. 21.
    De Zordo T, Chhem R, Smekal V, Feuchtner G, Reindl M, Fink C, et al. Real-time sonoelastography: findings in patients with symptomatic Achilles tendons and comparison to healthy volunteers. Ultraschall Med. 2010;31:394–400.CrossRefPubMedGoogle Scholar
  22. 22.
    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:W134–8.CrossRefPubMedGoogle Scholar
  23. 23.
    Capalbo E, Peli M, Stradiotti P. Sonoelastography of the distal third of the Achilles tendon in asymptomatic volunteers: correlation with anthropometric data, ultrasound findings and reproducibility of the method. La Radiologia Medica Springer Milan. 2016;121:667–74.CrossRefGoogle Scholar
  24. 24.
    Chen X-M, Cui L-G, He P, Shen W-W, Qian Y-J, Wang J-R. Shear wave elastographic characterization of normal and torn Achilles tendons: a pilot study. J Ultrasound Med. 2013;32:449–55.CrossRefPubMedGoogle Scholar
  25. 25.
    Aubry S, Risson J-R, Barbier-Brion B, Tatu L, Vidal C, Kastler B. Transient elastography of calcaneal tendon: preliminary results and future prospects. J Radiol. 2011;92:421–7.CrossRefPubMedGoogle Scholar
  26. 26.
    Dirrichs T, Quack V, Gatz M, Tingart M, Kuhl CK, Schrading S. Shear wave elastography (SWE) for the evaluation of patients with tendinopathies. Acad Radiol. 2016;23:1204–13.CrossRefPubMedGoogle Scholar
  27. 27.
    Arda K, Ciledag N, Aktas E, Aribas BK, Köse K. Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography. AJR Am J Roentgenol. 2011;197:532–6.CrossRefPubMedGoogle Scholar
  28. 28.
    Slane LC, Martin J, DeWall R, Thelen D, Lee K. Quantitative ultrasound mapping of regional variations in shear wave speeds of the aging Achilles tendon. Eur Radiol. Springer Berlin Heidelberg; 2017;27:474–82.Google Scholar
  29. 29.
    Aubry S, Risson J-R, Kastler A, Barbier-Brion B, Siliman G, Runge M, et al. Biomechanical properties of the calcaneal tendon in vivo assessed by transient shear wave elastography. Skeletal Radiol. Springer-Verlag; 2013;42:1143–50.Google Scholar
  30. 30.
    Rosskopf AB, Bachmann E, Snedeker JG, Pfirrmann CWA, Buck FM. Comparison of shear wave velocity measurements assessed with two different ultrasound systems in an ex-vivo tendon strain phantom. Skeletal Radiol. Springer Berlin Heidelberg; 2016;45:1541–51.Google Scholar
  31. 31.
    Peltz CD, Haladik JA, Divine G, Siegal D, van Holsbeeck M, Bey MJ. ShearWave elastography: repeatability for measurement of tendon stiffness. Skeletal Radiol. Springer-Verlag; 2013;42:1151–6.Google Scholar
  32. 32.
    Porta F, Damjanov N, Galluccio F, Iagnocco A, Matucci-Cerinic M. Ultrasound elastography is a reproducible and feasible tool for the evaluation of the patellar tendon in healthy subjects. Int J Rheum Dis. 2014;17:762–6.CrossRefPubMedGoogle Scholar
  33. 33.
    Kot BCW, Zhang ZJ, Lee AWC, Leung VYF, Fu SN. Elastic modulus of muscle and tendon with shear wave ultrasound elastography: variations with different technical settings. Kellermayer MS, editor. PLoS ONE Public Library of Science. 2012;7:e44348.CrossRefGoogle Scholar
  34. 34.
    Berko NS, Mehta AK, Levin TL, Schulz JF. Effect of knee position on the ultrasound elastography appearance of the patellar tendon. Clin Radiol. 2015:1083–6.Google Scholar
  35. 35.
    Hsiao M-Y, Chen Y-C, Lin C-Y, Chen W-S, Wang T-G. Reduced patellar tendon elasticity with aging: in vivo assessment by shear wave elastography. Ultrasound Med Biol. 2015;41:2899–905.CrossRefPubMedGoogle Scholar
  36. 36.
    Tudisco C, Bisicchia S, Stefanini M, Antonicoli M, Masala S, Simonetti G. Tendon quality in small unilateral supraspinatus tendon tears. Real-time sonoelastography correlates with clinical findings. Knee Surg Sports Traumatol Arthrosc. Springer Berlin Heidelberg; 2015;23:393–8.Google Scholar
  37. 37.
    Järvinen TAH, Kannus P, Maffulli N, Khan KM. Achilles tendon disorders: etiology and epidemiology. Foot Ankle Clin. 2005;10:255–66.CrossRefPubMedGoogle Scholar
  38. 38.
    Longo UG, Ronga M, Maffulli N. Achilles tendinopathy. Sports Med Arthrosc. 2009;17:112–26.CrossRefPubMedGoogle Scholar
  39. 39.
    Astrӧm M, Rausing A. Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings. Clin Orthop Relat Res. 1995:151–64.Google Scholar
  40. 40.
    Kannus P, Józsa L. Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg Am. 1991;73:1507–25.CrossRefPubMedGoogle Scholar
  41. 41.
    Ooi CC, Schneider ME, Malliaras P, Chadwick M, Connell DA. Diagnostic performance of axial-strain sonoelastography in confirming clinically diagnosed Achilles tendinopathy: comparison with B-mode ultrasound and color Doppler imaging. Ultrasound Med Biol. 2015;41:15–25.CrossRefPubMedGoogle Scholar
  42. 42.
    Klauser AS, Miyamoto H, Tamegger M, Faschingbauer R, Moriggl B, Klima G, et al. Achilles tendon assessed with sonoelastography: histologic agreement. Radiology. 2013;267:837–42.CrossRefPubMedGoogle Scholar
  43. 43.
    Ooi CC, Richards PJ, Maffulli N, Ede D, Schneider ME, Connell D, et al. A soft patellar tendon on ultrasound elastography is associated with pain and functional deficit in volleyball players. J Sci Med Sport. 2016;19:373–8.CrossRefPubMedGoogle Scholar
  44. 44.
    Ooi CC, Schneider ME, Malliaras P, Counsel P, Connell DA. Prevalence of morphological and mechanical stiffness alterations of mid Achilles tendons in asymptomatic marathon runners before and after a competition. Skeletal Radiol. Springer Berlin Heidelberg; 2015;44:1119–27.Google Scholar
  45. 45.
    Balaban M, Idilman IS, Ipek A, Ikiz SS, Bektaser B, Gumus M. Elastographic findings of Achilles tendons in asymptomatic professional male volleyball players. J Ultrasound Med. 2016;35:2623–8.CrossRefPubMedGoogle Scholar
  46. 46.
    Siu W-L, Chan C-H, Lam C-H, Lee C-M, Ying M. Sonographic evaluation of the effect of long-term exercise on Achilles tendon stiffness using shear wave elastography. J Sci Med Sport. 2016;19:883–7.CrossRefPubMedGoogle Scholar
  47. 47.
    Busilacchi A, Olivieri M, Ulisse S, Gesuita R, Skrami E, Lording T, et al. Real-time sonoelastography as novel follow-up method in Achilles tendon surgery. Knee Surg Sports Traumatol Arthrosc. 2016;24:2124–32.CrossRefPubMedGoogle Scholar
  48. 48.
    Sconfienza LM, Silvestri E, Cimmino MA. Sonoelastography in the evaluation of painful Achilles tendon in amateur athletes. Clin Exp Rheumatol. 2010;28:373–8.PubMedGoogle Scholar
  49. 49.
    Aubry S, Nueffer J-P, Tanter M, Becce F, Vidal C, Michel F. Viscoelasticity in Achilles tendonopathy: quantitative assessment by using real-time shear-wave elastography. Radiology. 2015;274:821–9.CrossRefPubMedGoogle Scholar
  50. 50.
    Martin JA, Biedrzycki AH, Lee KS, DeWall RJ, Brounts SH, Murphy WL, et al. In vivo measures of shear wave speed as a predictor of tendon elasticity and strength. Ultrasound Med Biol. 2015;41:2722–30.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Zhang L-N, Wan W-B, Wang Y-X, Jiao Z-Y, Zhang L-H, Luo Y-K, et al. Evaluation of elastic stiffness in healing Achilles tendon after surgical repair of a tendon rupture using in vivo ultrasound shear wave elastography. Med Sci Monit. 2016;22:1186–91.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Lee S-U, Joo SY, Kim SK, Lee S-H, Park S-R, Jeong C. Real-time sonoelastography in the diagnosis of rotator cuff tendinopathy. J Shoulder Elb Surg. 2016;25:723–9.CrossRefGoogle Scholar
  53. 53.
    Lalitha P, Reddy MCB, Reddy KJ. Musculoskeletal applications of elastography: a pictorial essay of our initial experience. Korean J Radiol. 2011;12:365–75.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Seo J-B, Yoo J-S, Ryu J-W. Sonoelastography findings of biceps tendinitis and tendinosis. J Ultrasound. Springer International Publishing; 2014;17:271–7.Google Scholar
  55. 55.
    Lin Y-H, Chiou H-J, Wang H-K, Lai Y-C, Chou Y-H, Chang C-Y. Management of rotator cuff calcific tendinosis guided by ultrasound elastography. J Chin Med Assoc. 2015;78:603–9.CrossRefPubMedGoogle Scholar
  56. 56.
    Leong HT, Hug F, Fu SN. Increased upper trapezius muscle stiffness in overhead athletes with rotator cuff tendinopathy. Lucia A, editor. PLoS ONE. 2016;11:e0155187.Google Scholar
  57. 57.
    Hou SW, Merkle AN, Babb JS, McCabe R, Gyftopoulos S, Adler RS. Shear wave ultrasound elastographic evaluation of the rotator cuff tendon. J Ultrasound Med. 2017;36:95–106.CrossRefPubMedGoogle Scholar
  58. 58.
    Krepkin K, Bruno M, Raya JG, Adler RS, Gyftopoulos S. Quantitative assessment of the supraspinatus tendon on MRI using T2/T2* mapping and shear-wave ultrasound elastography: a pilot study. Skeletal Radiol. Springer Berlin Heidelberg; 2017;46:191–9.Google Scholar
  59. 59.
    Hatta T, Giambini H, Uehara K, Okamoto S, Chen S, Sperling JW, et al. Quantitative assessment of rotator cuff muscle elasticity: reliability and feasibility of shear wave elastography. J Biomech. 2015;48:3853–8.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Rosskopf AB, Ehrmann C, Buck FM, Gerber C, Flück M, Pfirrmann CWA. Quantitative shear-wave US elastography of the supraspinatus muscle: reliability of the method and relation to tendon integrity and muscle quality. Radiology Radiological Society of North America. 2015;278:465–74.Google Scholar
  61. 61.
    Pochini A de C, Ferretti M, Kawakami EFKI, Fernandes ADRC, Yamada AF, Oliveira GC de, et al. Analisys of pectoralis major tendon in weightlifting athletes using ultrasonography and elastography. Einstein (Sao Paulo). Instituto Israelita de Ensino e Pesquisa Albert Einstein; 2015;13:541–6.Google Scholar
  62. 62.
    Zhang ZJ, Ng GY-F, Lee WC, Fu SN. Changes in morphological and elastic properties of patellar tendon in athletes with unilateral patellar tendinopathy and their relationships with pain and functional disability. Hug FO, editor. PLoS ONE. 2014;9:e108337.Google Scholar
  63. 63.
    De Zordo T, Lill SR, Fink C, Feuchtner GM, Jaschke W, Bellmann-Weiler R, et al. Real-time sonoelastography of lateral epicondylitis: comparison of findings between patients and healthy volunteers. AJR Am J Roentgenol. 2009;193:180–5.CrossRefPubMedGoogle Scholar
  64. 64.
    Park G, Kwon D, Park J. Diagnostic confidence of sonoelastography as adjunct to greyscale ultrasonography in lateral elbow tendinopathy. Chin Med J. 2014;127:3110–5.PubMedGoogle Scholar
  65. 65.
    Klauser AS, Pamminger M, Halpern EJ, Abd Ellah MMH, Moriggl B, Taljanovic MS, et al. Extensor tendinopathy of the elbow assessed with sonoelastography: histologic correlation. Eur Radiol. Springer Berlin Heidelberg; 2017;176:777–7.Google Scholar
  66. 66.
    Klauser AS, Pamminger MJ, Halpern EJ, Abd Ellah MMH, Moriggl B, Taljanovic MS, et al. Sonoelastography of the common flexor tendon of the elbow with Histologic agreement: a cadaveric study. Radiology. 2017;283:486–91.CrossRefPubMedGoogle Scholar
  67. 67.
    Turan A, Tufan A, Mercan R, Teber MA, Tezcan ME, Bitik B, et al. Real-time sonoelastography of Achilles tendon in patients with ankylosing spondylitis. Skelet Radiol. 2013;42:1113–8.CrossRefGoogle Scholar
  68. 68.
    Evranos B, Idilman I, Ipek A, Polat SB, Cakir B, Ersoy R. Real-time sonoelastography and ultrasound evaluation of the Achilles tendon in patients with diabetes with or without foot ulcers: a cross sectional study. J Diabetes Complicat. 2015;29:1124–9.CrossRefPubMedGoogle Scholar
  69. 69.
    Onal ED, Ipek A, Evranos B, Idilman IS, Cakir B, Ersoy R. Structural tendon changes in patients with acromegaly: assessment of Achilles tendon with sonoelastography. Med Ultrason. 2016;18:30–5.CrossRefPubMedGoogle Scholar
  70. 70.
    Teber MA, Oğur T, Bozkurt A, Er B, Turan A, Gülbay M, et al. Real-time sonoelastography of the quadriceps tendon in patients undergoing chronic hemodialysis. J Ultrasound Med. 2015;34:671–7.CrossRefPubMedGoogle Scholar
  71. 71.
    Guney A, Vatansever F, Karaman I, Kafadar IH, Oner M, Turk CY. Biomechanical properties of Achilles tendon in diabetic vs. non-diabetic patients. Exp. Clin. Endocrinol. Diabetes. © Georg Thieme Verlag KG, 2015 ;123:428–32.Google Scholar

Copyright information

© ISS 2017

Authors and Affiliations

  • Romain Domenichini
    • 1
    • 2
  • Jean-Baptiste Pialat
    • 2
    • 3
  • Andrea Podda
    • 1
  • Sébastien Aubry
    • 1
    • 4
  1. 1.Department of Musculoskeletal ImagingCHRU de BesanconBesançon CedexFrance
  2. 2.Department of Radiology, Centre Hospitalier Lyon-SudHospices Civils de LyonPierre-BéniteFrance
  3. 3.LYOS INSERM UMR 1033University of LyonLyonFrance
  4. 4.Nanomedecine laboratory, INSERM EA4662University of Franche-ComteBesançonFrance

Personalised recommendations