Quantitative ultrasound imaging of Achilles tendon integrity in symptomatic and asymptomatic individuals: reliability and minimal detectable change

Marie-Josée Nadeau, Amélie Desrochers, Martin Lamontagne, Christian Larivière, Dany H Gagnon, Marie-Josée Nadeau, Amélie Desrochers, Martin Lamontagne, Christian Larivière, Dany H Gagnon

Abstract

Background: Quantifying the integrity of the Achilles tendon (AT) is a rehabilitation challenge. Adopting quantitative ultrasound measurements (QUS measurements) of the AT could fill this gap by 1) evaluating the test-retest reliability and accuracy of QUS measurements of the AT; 2) determining the best protocol for collecting QUS measurements in clinical practice.

Methods: A total of 23 ATs with symptoms of Achilles tendinopathy and 63 asymptomatic ATs were evaluated. Eight images were recorded for each AT (2 visits × 2 evaluators × 2 images). Multiple sets of QUS measurements were taken: geometric (thickness, width, area), first-order statistics (computed from a grayscale histogram distribution: echogenicity, variance, skewness, kurtosis, entropy) and texture features (computed from co-occurrence matrices: contrast, energy, homogeneity). A generalizability study quantified the reliability and standard error of measurement (accuracy) of each QUS measurement, and a decision study identified the best measurement taking protocols.

Results: Geometric QUS measurements demonstrated excellent accuracy and reliability. QUS measurements computed from the grayscale histogram distribution revealed poor accuracy and reliability. QUS measurements derived from co-occurrence matrices showed variable accuracy and moderate to excellent reliability. In clinical practice, using an average of the results of three images collected by a single evaluator during a single visit is recommended.

Conclusions: The use of geometric QUS measurements enables quantification of AT integrity in clinical practice and research settings. More studies on QUS measurements derived from co-occurrence matrices are warranted.

Keywords: Achilles tendon; Computer-assisted image analysis; Measures; Musculoskeletal system; Quantitative evaluation; Rehabilitation; Reproducibility; Tendinopathy; Ultrasonography.

Figures

Fig. 1
Fig. 1
a ROI of a healthy AT in longitudinal view; b ROI of a healthy AT in transverse view; c grayscale histogram derived from the ROI of image (b); d Pathologic AT in longitudinal view; e Pathologic AT in transverse view with arrows indicating the AT’s thickness at different locations in the sagittal plane; f grayscale histogram derived from the ROI of image (e)
Fig. 2
Fig. 2
General criteria for inclusion and exclusion of participants and participants’ characteristics
Fig. 3
Fig. 3
Summary of image recording protocol

References

    1. De Jonge S, Van den Berg C, De Vos R, Van der Heide H, Weir A, Verhaar J, Bierma-Zeinstra S, Tol J. Incidence of midportion Achilles tendinopathy in the general population. Br J Sports Med. 2011;45(13):1026–1028. doi: 10.1136/bjsports-2011-090342.
    1. Alfredson H, Lorentzon R. Chronic achilles tendinosis. Sports Med. 2000;29(2):135–146. doi: 10.2165/00007256-200029020-00005.
    1. Rolf C, Movin T. Etiology, histopathology, and outcome of surgery in achillodynia. Foot Ankle Int. 1997;18(9):565–569. doi: 10.1177/107110079701800906.
    1. Kvist M. Achilles tendon injuries in athletes. Sports Med. 1994;18(3):173–201. doi: 10.2165/00007256-199418030-00004.
    1. Krolo I, Višković K, Ikić Đ, Klarić-Ćustović R, Marotti M, Cicvara T. The risk of sports activities–the injuries of the Achilles tendon in sportsmen. Coll Antropol. 2007;31(1):275–278.
    1. Lopes AD, Junior MLCH, Yeung SS, Costa LOP. What are the Main Running-Related Musculoskeletal Injuries? Sports Med. 2012;42(10):891–905. doi: 10.1007/BF03262301.
    1. Maffulli N, Sharma P, Luscombe KL. Achilles tendinopathy: aetiology and management. J R Soc Med. 2004;97(10):472–476. doi: 10.1258/jrsm.97.10.472.
    1. Alfredson H, Cook J. A treatment algorithm for managing Achilles tendinopathy: new treatment options. Br J Sports Med. 2007;41(4):211–216. doi: 10.1136/bjsm.2007.035543.
    1. McShane JM, Ostick B, McCabe F. Noninsertional Achilles tendinopathy: pathology and management. Curr Sports Med Rep. 2007;6(5):288–292.
    1. Magnussen RA, Dunn WR, Thomson AB. Nonoperative treatment of midportion Achilles tendinopathy: a systematic review. Clin J Sport Med. 2009;19(1):54–64. doi: 10.1097/JSM.0b013e31818ef090.
    1. Brasseur J, Zeitoun-Eiss D, Renoux J, Bach G. Apport de l’échographie dans l’exploration du pied et de la cheville. EM-Consulte Podologie. 2010
    1. Bianchi S, Martinoli C. Ultrasound of the Musculoskeletal System. 1. Berlin Heidelberg: Springer; 2007.
    1. Jacobson JA. Fundamentals of musculoskeletal ultrasound. 1st ed. Philadelphia: Elsevier Health Sciences; 2007.
    1. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact. 2006;6(2):181.
    1. Khan KM, Cook JL, Bonar F, Harcourt P, Åstrom M. Histopathology of common tendinopathies. Sports Med. 1999;27(6):393–408. doi: 10.2165/00007256-199927060-00004.
    1. Hertzberg BS, Kliewer MA, Bowie JD, Carroll BA, DeLong DH, Gray L, Nelson RC. Physician Training Requirements in Sonography: How Many Cases Are Needed for Competence? AJR Am J Roentgenol. 2000;174(5):1221–1227. doi: 10.2214/ajr.174.5.1741221.
    1. Krupinski EA. Computer-aided Detection in Clinical Environment: Benefits and Challenges for Radiologists1. Radiology. 2004;231(1):7–9. doi: 10.1148/radiol.2311031864.
    1. Castellano G, Bonilha L, Li L, Cendes F. Texture analysis of medical images. Clin Radiol. 2004;59(12):1061–1069. doi: 10.1016/j.crad.2004.07.008.
    1. Bharati MH, Liu JJ, MacGregor JF. Image texture analysis: methods and comparisons. Chemometr Intell Lab Syst. 2004;72(1):57–71. doi: 10.1016/j.chemolab.2004.02.005.
    1. Schie HT, Bakker EM, Jonker AM, Weeren P. Ultrasonographic tissue characterization of equine superficial digital flexor tendons by means of gray level statistics. Am J Vet Res. 2000;61(2):210–219. doi: 10.2460/ajvr.2000.61.210.
    1. Sipila S, Suominen H. Ultrasound imaging of the quadriceps muscle in elderly athletes and untrained men. Muscle Nerve. 1991;14(6):527–533. doi: 10.1002/mus.880140607.
    1. Sipilä S, Suominen H. Muscle ultrasonography and computed tomography in elderly trained and untrained women. Muscle Nerve. 1993;16(3):294–300. doi: 10.1002/mus.880160309.
    1. Sipilä S, Suominen H. Quantitative ultrasonography of muscle: detection of adaptations to training in elderly women. Arch Phys Med Rehabil. 1996;77(11):1173–1178. doi: 10.1016/S0003-9993(96)90143-4.
    1. Nielsen PK, Jensen BR, Darvann T, Jørgensen K, Bakke M. Quantitative ultrasound tissue characterization in shoulder and thigh muscles–a new approach. BMC Musculoskelet Disord. 2006;7(1):2. doi: 10.1186/1471-2474-7-2.
    1. Pillen S, Verrips A, Van Alfen N, Arts I, Sie L, Zwarts M. Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease. Neuromuscul Disord. 2007;17(7):509–516. doi: 10.1016/j.nmd.2007.03.008.
    1. Bashford GR, Tomsen N, Arya S, Burnfield JM, Kulig K. Tendinopathy discrimination by use of spatial frequency parameters in ultrasound B-mode images. IEEE Trans Med Imaging. 2008;27(5):608–615. doi: 10.1109/TMI.2007.912389.
    1. van Schie H, De Vos R, De Jonge S, Bakker E, Heijboer M, Verhaar J, Tol J, Weinans H. Ultrasonographic tissue characterisation of human Achilles tendons: quantification of tendon structure through a novel non-invasive approach. Br J Sports Med. 2010;44(16):1153–1159. doi: 10.1136/bjsm.2009.061010.
    1. Tuthill TA, Rubin JM, Fowlkes JB, Jamadar DA, Bude RO. Frequency analysis of echo texture in tendon. Ultrasound Med Biol. 1999;25(6):959–968. doi: 10.1016/S0301-5629(99)00031-9.
    1. O’Connor PJ, Grainger AJ, Morgan S, Smith K, Waterton J, Nash A. Ultrasound assessment of tendons in asymptomatic volunteers: a study of reproducibility. Eur Radiol. 2004;14(11):1968–1973. doi: 10.1007/s00330-004-2448-4.
    1. Wearing SC, Grigg NL, Hooper SL, Smeathers JE. Conditioning of the Achilles tendon via ankle exercise improves correlations between sonographic measures of tendon thickness and body anthropometry. J Appl Physiol. 2011;110(5):1384–1389. doi: 10.1152/japplphysiol.00075.2011.
    1. Schmidt W, Schmidt H, Schicke B, Gromnica-Ihle E. Standard reference values for musculoskeletal ultrasonography. Ann Rheum Dis. 2004;63(8):988–994. doi: 10.1136/ard.2003.015081.
    1. Fredberg U, Bolvig L, Andersen NT, Stengaard-Pedersen K. Ultrasonography in evaluation of Achilles and patella tendon thickness. Ultraschall Med. 2008;29(01):60–65. doi: 10.1055/s-2007-963027.
    1. Brushøj C, Henriksen B, Albrecht-Beste E, Hölmich P, Larsen K, Nielsen MB. Reproducibility of ultrasound and magnetic resonance imaging measurements of tendon size. Acta Radiol. 2006;47(9):954–959. doi: 10.1080/02841850600854936.
    1. Ying M, Yeung E, Li B, Li W, Lui M, Tsoi C-W. Sonographic evaluation of the size of Achilles tendon: the effect of exercise and dominance of the ankle. Ultrasound Med Biol. 2003;29(5):637–642. doi: 10.1016/S0301-5629(03)00008-5.
    1. Larivière C, Gagnon D, De Oliveira JE, Henry SM, Mecheri H, Dumas J-P. Reliability of Ultrasound Measures of the Transversus Abdominis: Effect of Task and Transducer Position. PM R. 2013;5(2):104–113. doi: 10.1016/j.pmrj.2012.11.002.
    1. Lariviere C, Gagnon D, De Oliveira JE, Henry SM, Mecheri H, Dumas J-P. Ultrasound Measures of the Lumbar Multifidus: Effect of Task and Transducer Position on Reliability. PM R. 2013;5(8):678–687. doi: 10.1016/j.pmrj.2013.03.010.
    1. Robinson J, Cook JL, Purdam C, Visentini P, Ross J, Maffulli N, Taunton J, Khan K. The VISA-A questionnaire: a valid and reliable index of the clinical severity of Achilles tendinopathy. Br J Sports Med. 2001;35(5):335–341. doi: 10.1136/bjsm.35.5.335.
    1. Vestergrd Iversen J, Bartels EM, Langberg H. The Victorian Institute of Sports Assessment-Achilles Questionnaire (VISA-A)-reliable tool for measuring Achilles tendinopathy. Int J Sports Phys Ther. 2012;7(1):76–84.
    1. Collinger JL, Gagnon D, Jacobson J, Impink BG, Boninger ML. Reliability of quantitative ultrasound measures of the biceps and supraspinatus tendons. Acad Radiol. 2009;16(11):1424–1432. doi: 10.1016/j.acra.2009.05.001.
    1. Collinger JL, Fullerton B, Impink BG, Koontz AM, Boninger ML. Validation of greyscale-based quantitative ultrasound in manual wheelchair users: relationship to established clinical measures of shoulder pathology. Am J Phys Med Rehabil. 2010;89(5):390. doi: 10.1097/PHM.0b013e3181d8a238.
    1. Collinger JL, Impink BG, Ozawa H, Boninger ML. Effect of an intense wheelchair propulsion task on quantitative ultrasound of shoulder tendons. PM R. 2010;2(10):920–925. doi: 10.1016/j.pmrj.2010.06.007.
    1. Roebroeck ME, Harlaar J, Lankhorst GJ. The application of generalizability theory to reliability assessment: an illustration using isometric force measurements. Phys Ther. 1993;73(6):386–395.
    1. Portney LG, Watkins MP. Foundations of clinical research: Applications to practice. 3rd ed. Prentice Hall; 2007
    1. McCreesh KM, Crotty JM, Lewis JS. Acromiohumeral distance measurement in rotator cuff tendinopathy: is there a reliable, clinically applicable method? A systematic review. Br J Sports Med. 2015;49(5):298–305. doi: 10.1136/bjsports-2012-092063.
    1. Gellhorn AC, Carlson MJ. Inter-rater, intra-rater, and inter-machine reliability of quantitative ultrasound measurements of the patellar tendon. Ultrasound Med Biol. 2013;39(5):791–796. doi: 10.1016/j.ultrasmedbio.2012.12.001.
    1. Tweedell AJ, Ryan ED, Scharville MJ, Rosenberg JG, Sobolewski EJ, Kleinberg CR. The influence of ultrasound measurement techniques on the age-related differences in Achilles tendon size. Exp Gerontol. 2016;76:68–71. doi: 10.1016/j.exger.2016.01.015.
    1. Scholten R, Pillen S, Verrips A, Zwarts M. Quantitative ultrasonography of skeletal muscles in children: normal values. Muscle Nerve. 2003;27(6):693–698. doi: 10.1002/mus.10384.
    1. Reimers CD, Schlotter B, Eicke BM, Witt TN. Calf enlargement in neuromuscular diseases: a quantitative ultrasound study in 350 patients and review of the literature. J Neurol Sci. 1996;143(1):46–56. doi: 10.1016/S0022-510X(96)00037-8.
    1. Nielsen PK, Jensen BR, Darvann T, Jørgensen K, Bakke M. Quantitative ultrasound image analysis of the supraspinatus muscle. Clin Biomech (Bristol, Avon) 2000;15:S13–S16. doi: 10.1016/S0268-0033(00)00053-X.
    1. Arend CF. Top ten pitfalls to avoid when performing musculoskeletal sonography: what you should know before entering the examination room. Eur J Radiol. 2013;82(11):1933–1939. doi: 10.1016/j.ejrad.2013.01.022.
    1. Haralick RM, Shanmugam K, Dinstein IH. Textural features for image classification. IEEE Trans Syst Man Cybern Syst. 1973;3(6):610–621. doi: 10.1109/TSMC.1973.4309314.
    1. Lagergren C, Lindholm Å. Vascular distribution in the Achilles tendon; an angiographic and microangiographic study. Acta Chir Scand. 1959;116(5–6):491.
    1. Clain MR, Baxter DE. Achilles tendinitis. Foot Ankle Int. 1992;13(8):482–487. doi: 10.1177/107110079201300810.
    1. Syha R, Peters M, Birnesser H, Niess A, Hirschmueller A, Dickhuth H, Sandrock M. Computer-based quantification of the mean Achilles tendon thickness in ultrasound images–effect of tendinosis. Br J Sports Med. 2007;41(12):897–902. doi: 10.1136/bjsm.2007.037812.
    1. Syha R, Grau S, Nieß AM, Hein T, Werner M, Ketelsen D, Schick F, Best R. Computer-based quantification of the Achilles tendon thickness in sequential B-mode ultrasound images: a study of feasibility and reliability. Arch Orthop Trauma Surg. 2014;134(10):1443–1449. doi: 10.1007/s00402-014-2043-3.

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera