| Literature DB >> 30120723 |
Rui Prado-Costa1, João Rebelo2, João Monteiro-Barroso1, Ana Sofia Preto3.
Abstract
Ultrasound elastography (USE) is a recent technology that has experienced major developments in the past two decades. The assessment of the main mechanical properties of tissues can be made with this technology by characterisation of their response to stress. This article reviews the two major techniques used in musculoskeletal elastography, compression elastography (CE) and shear-wave elastography (SWE), and evaluates the studies published on major electronic databases that use both techniques in the context of tendon pathology. CE accounts for more studies than SWE. The mechanical properties of tendons, particularly their stiffness, may be altered in the presence of tendon injury. CE and SWE have already been used for the assessment of Achilles tendons, patellar tendon, quadriceps tendon, epicondylar tendons and rotator cuff tendons and muscles. Achilles tendinopathy is the most studied tendon injury with USE, including the postoperative period after surgical repair of Achilles rupture tendon. In relation to conventional ultrasound (US), USE potentially increases the sensitivity and diagnostic accuracy in tendinopathy, and can detect pathological changes before they are visible in conventional US imaging. Several technical limitations are recognised, and standardisation is necessary to ensure repeatability and comparability of the results when using these techniques. Still, USE is a promising technique under development and may be used not only to promote an early diagnosis, but also to identify the risk of injury and to support the evaluation of rehabilitation interventions. KEY POINTS: • USE is used for the assessment of the mechanical properties of tissues, including the tendons. • USE increases diagnostic performance when coupled to conventional US imaging modalities. • USE will be useful in early diagnosis, tracking outcomes and monitoring treatments of tendon injury. • Technical issues and lack of standardisation limits USE use in the assessment of tendon injury.Entities:
Keywords: Elastography; Sonoelastography; Tendinopathy; Tendon injury; Ultrasound
Year: 2018 PMID: 30120723 PMCID: PMC6206379 DOI: 10.1007/s13244-018-0642-1
Source DB: PubMed Journal: Insights Imaging ISSN: 1869-4101
Fig. 1Basic physical principle of compression elastography (CE). The operator exerts compression on the tissue, generating a displacement (δ) that can be estimated by comparing the structure at rest and under compression. The strain (ε) is the ratio difference in displacement between two points to their distance pre-compression (L). The strain measurements are displayed as a colour map, called an elastogram, which is overlaid on the B-mode image. Typically, low strain (stiff tissue) is displayed in blue and high strain (soft tissue) is displayed in red
Fig. 2Basic physical principle of shear-wave elastography (SWE). A perpendicular stress force (acoustic radiation force) is applied to the tissue, which causes the generation of shear waves. The velocity of the shear wave could be measured by obtaining radiofrequency images with a high frame rate, which can be used to generate a tissue displacement map. Tissue displacements are used to calculate the shear-wave velocity (Vs) and shear modulus (G)
Studies found using compression elastography (CE) in the assessment of injured or pathologic tendons
| Authors year [reference] | Subjects (symptomatic and asymptomatic; structures assessed) | Study design, comparison modality | Major findings | Diagnostic performance and correlations (including comparison with clinical examination, functional scores, conventional US and MRI) |
|---|---|---|---|---|
| Achilles tendon | ||||
| De Zordo et al. 2010 [ | 25 volunteers/50 asymptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons were softer. | USE detected more alterations in contralateral asymptomatic tendons than conventional US. |
| Sconfienza et al. 2010 [ | 18 volunteers/36 asymptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons were harder. | USE showed good correlation with conventional US and MRI. |
| Tan et al. 2012 [ | 20 volunteers/40 asymptomatic tendons. | Cross-sectional, case–control study. | Healing tendons demonstrated a harder and heterogeneous texture compared to the healthy ones. | |
| Gehmert et al. 2012 [ | 9 rabbits: 12 ruptured tendons, 6 tendons treated with stem cells, 6 ruptured tendons not treated, 6 healthy tendons. | Laboratory study with New Zealand white rabbits. | Treated tendons with stem cells had higher elasticity compared with those not treated. | |
| Klauser et al. 2013 [ | 10 cadavers/13 tendons. | Laboratory study using cadaveric models. | Injured tendons were softer than asymptomatic tendons. | USE showed perfect agreement with histology results and moderate agreement with conventional US ( |
| Turan et al. 2013 [ | 41 patients with ankylosing spondylitis (AE)/82 tendons. | Cross-sectional, case–control study. | Distal third of Achilles tendon was softer on patients with AE compared with healthy individuals ( | USE had moderate to good correlation with conventional US ( |
| Evranos et al. 2015 [ | 78 patients with diabetes: 35 patients with foot ulcers, 43 patients without foot ulcers, 33 healthy individuals | Cross-sectional, case–control study. | The Achilles tendon was softer in diabetic patients with foot ulcers than in patients without ulcers ( | |
| Ooi et al. 2015 [ | 120 patients/120 symptomatic tendons | Cross-sectional, case–control study. | Symptomatic tendons were softer than asymptomatic tendons (SR = 1.70 ± 0.84 vs. 0.76 ± 0.30, | USE had excellent sensitivity, specificity and diagnostic accuracy (Sv: 97.5%, Sp: 94.5%, Ac: 97.8%). |
| Busilacchi et al. 2016 [ | 30 volunteers/60 asymptomatic tendons. | Prospective cohort study. | After surgery, the tendons were harder and achieved a peak thickness 6 months after, compared to contralateral and control group tendons. | SR had a negative correlation with functional score ( |
| Onal et al. 2016 [ | 42 acromegaly patients/84 tendons. | Cross-sectional, case–control study. | Achilles tendons in patients with acromegaly were softer than the healthy ones ( | No significant correlation between USE and biological markers of the disease. |
| Yamamoto et al. 2017 [ | 24 New Zealand rabbits with Achilles tendon transection. | Laboratory study. | Mean SR at the healing site after Achilles tendon rupture gradually decreased and the Achilles tendon became significantly harder over time ( | SR showed correlation with all mechanical evaluations [ultimate stress ( |
| Patellar tendon | ||||
| Rist and Mauch 2012 [ | 75 athletes: 37 asymptomatic tendons, 38 symptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons showed higher strain scores than asymptomatic ones in longitudinal and cross-section. | |
| Ooi et al. 2016 [ | 35 volleyball athletes: 40 symptomatic tendons, 30 asymptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons were softer than asymptomatic tendons. | USE alone: Ac: 62.9%, Sv: 70%; Sp: 53.3%. |
| Epicondylar tendons | ||||
| De Zordo et al. 2009 [ | 28 volunteers/44 asymptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons were softer than asymptomatic tendons ( | Sv: 100%, Sp: 89%, Ac: 94%. |
| Ahn et al. 2014 [ | 79 patients and 14 healthy volunteers. | Cross-sectional, case–control study. | Symptomatic tendons were softer (mean SR = 1.45 ± 0.45) than asymptomatic tendons (mean SR = 2.07 ± 0.70) ( | Significant correlation with conventional US ( |
| Park et al. 2014 [ | 28 patients with unilateral lateral epicondylitis: 14 symptomatic tendons, 14 asymptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons were softer than asymptomatic tendons. | USE alone: Sv: 96.4%, Sp: 96.4%, Ac: 96.4% ( |
| Kocyigit et al. 2016 [ | 17 volunteers with lateral epicondylitis/34 tendons. | Cross-sectional, case–control study. | Symptomatic tendons were softer than asymptomatic tendons ( | USE was superior to conventional US distinguishing healthy tendons from those with tendinopathy. |
| Klauser et al. 2017 [ | 16 cadavers/25 common flexor tendons. | Laboratory study using cadaveric models. | Tendons with tendinopathy were softer than normal tendons. | USE combined with conventional US had better correlation ( |
| Klauser et al. 2017 [ | 17 cadavers/26 common flexor tendons. | Laboratory study using cadaveric models. | Tendons with tendinopathy were softer than normal tendons. | USE alone: Sv: 85%, Sp: 86%, Ac: 86%. |
| Rotator cuff tendons | ||||
| Seo et al. 2014 [ | 98 patients/101 shoulders with lesions (cuff tears, tendinopathies, adhesive capsulitis, calcific tendinitis, labral lesions). | Cross-sectional. | USE allowed quantification of the severity of adipose involution on the supraspinatus muscle tendon. | Sv: 95.6%, Sp: 87.5%, Ac: 91.1%. |
| Seo et al. 2014 [ | 118 patients/118 shoulders with supraspinatus tendinopathy. | Cross-sectional. | Tendons with tendinopathy had focal areas of softness. | Positive correlation between grades of MRI and USE ( |
| Tudisco et al. 2015 [ | 100 shoulders: 50 with supraspinatus tear, 50 healthy contralateral shoulders. | Cross-sectional, case–control study. | Mean SR in the affected shoulder (0.75 ± 0.08) was lower than the contralateral healthy shoulder (1.01 ± 0.07) ( | Negative correlation between SR and VAS (Visual Analogue Scale) score for pain ( |
| Kocyigit et al. 2016 [ | 50 shoulders: 25 patients diagnosed with unilateral subacromial impingement, 25 healthy shoulders. | Cross-sectional, case–control study. | Decreased stiffness of the supraspinatus tendon of the affected shoulder compared to healthy shoulder ( | There was no correlation between the findings in USE and functional scores, gender and age. |
| Lee et al. 2016 [ | 39 patients with chronic supraspinatus tendinopathy. | Cross-sectional. | Positive correlation of SR with degree of tendinosis in MRI ( | |
| Long head of biceps tendon (LHBT) | ||||
| Seo et al. 2014 [ | 34 patients/38 shoulders with tendinopathy of LHBT. | Cross-sectional, case–control study. | Focal areas of softening in affected tendons. | Positive correlation between USE and conventional ultrasound ( |
| Quadriceps tendon | ||||
| Teber et al. 2015 [ | 53 patients with chronic renal failure undergoing dialysis/106 quadriceps tendons. | Cross-sectional, case–control study. | Quadriceps tendons in patients with chronic renal failure were softer (right knee, | |
Ac accuracy; MRI magnetic resonance imaging; Sp specificity; Sv sensitivity; SR strain ratio; ρ Spearman rank correlation coefficient; r Pearson correlation coefficient; k kappa coefficient
Studies found for shear-wave elastography (SWE) in the assessment of injured or pathologic tendons
| Authorsyear [reference] | Subjects (symptomatic and asymptomatic; structures assessed) | Study design, comparison modality | Major findings | Diagnostic performance and correlations (including comparison with clinical examination, conventional US and MRI) |
|---|---|---|---|---|
| Patellar, Achilles and epicondylar tendons | ||||
| Dirrichs et al. 2016 [ | 112 patients. | Prospective cohort study. | Decreased stiffness in symptomatic tendons. | Conventional imaging + SWE: Sv 94.3%, Sp: 69.1%, Ac 84.8%. |
| Coombes et al. 2018 [ | 67 participants: 22 patients with Achilles tendinopathy, 17 patients with patellar tendinopathy, 28 healthy controls. | Cross-sectional, case–control study. | Achilles tendinopathy: decreased stiffness at the distal insertion ( | Achilles tendinopathy: Vs < 9.7 m/s, Sp: 81%, Sv: 79%. |
| Achilles tendon | ||||
| Chen et al. 2013 [ | 80 volunteers/36 normal tendons. | Cross-sectional, case–control study. | Lower and heterogeneous elasticity of torn tendons compared to normal ones, including throughout healing in the subacute stage ( | |
| Aubry et al. 2015 [ | 80 volunteers/160 asymptomatic tendons. | Cross-sectional, case–control study. | Symptomatic tendons were softer ( | Sagittal SWE with tendon in neutral position: Vs < 5.7 m/s for tendinopathy diagnosis, Sv 41.7%, Sp 81.8%. |
| Zhang et al. 2016 [ | 26 volunteers with rupture of the tendon treated surgically. | Prospective cohort study. | Tendon stiffness had increased over time ( | Positive correlation between functional scores and elasticity ( |
| Patellar tendon | ||||
| Zhang et al. 2014 [ | 20 volunteers/40 asymptomatic tendons. | Cross-sectional, case–control study. | Increased stiffness on tendons with tendinopathy ( | Significant correlation between increased stiffness in the painful tendon and the intensity of pain and degree of dysfunction. |
| Rotator cuff tendons | ||||
| Lin et al. 2015 [ | 39 patients with calcifying tendinopathy/39 tendons. | Cross-sectional. | USE allowed predicting of calcifications that benefit from fine needle aspiration ( | |
| Rosskopf et al. 2016 [ | 22 asymptomatic volunteers. | Prospective cohort study. | Mean total Vs in tendinopathy of 2.5 ± 0.5 m/s vs. Vs of 3.0 ± 0.5 m/s in asymptomatic shoulders ( | |
| Capalbo et al. 2016 [ | 17 asymptomatic volleyball players/17 upper trapezius on dominant side. | Cross-sectional, case–control study. | Upper trapezius shear modulus was higher in athletes with rotator cuff tendinopathy than the asymptomatic athletes ( | |
| Hou et al. 2017 [ | 35 patients: 21 symptomatic shoulder assessments, 55 asymptomatic shoulder assessments with B-mode US and SWE. | Retrospective and prospective cohort study. | Proximal supraspinatus tendon ( | Weak-to-moderate negative correlation between Vs of the deltoid muscle and morphologic grade of supraspinatus tendon on conventional US: proximal tendon: |
| Hatta et al. 2017 [ | 45 cadaveric shoulders: 25 shoulders with intact rotator cuff, 20 shoulders with rotator cuff tear. | Laboratory study. | Moderately significant positive correlation of SWE stiffness with stiffness of the supraspinatus muscle measured by a mechanical device. | |
| Kreplin et al. 2017 [ | 8 patients: 9 shoulders: 5 with full-thickness supraspinatus tendon tear, 2 with partial thickness supraspinatus tendon tear and 1 with tendinosis without tear. | Cross-sectional. | Average Vs = 9.4 ± 2.6 m/s. | Significant negative correlation between T2* and Vs ( |
| Baumer et al. 2018 [ | 19 asymptomatic subjects. | Retrospective case–control study. | Shoulder with supraspinatus tendon tear had lower mean Vs in supraspinatus muscle and tendon under active conditions (~ 30° scapular plane active abduction) than healthy, asymptomatic shoulders: mean Vs = 3.3 ± 0.8 m/s vs. 4.0 ± 0.4 m/s, | Sv ≥ 0.67 and Sp ≥ 0.63 to distinguish between asymptomatic control subjects and patients with a rotator cuff tear. |
Ac accuracy, BMI body mass index, MRI magnetic resonance imaging, Sp specificity, Sv sensitivity, Vs shear-wave velocity, ρ Spearman rank correlation coefficient, r Pearson correlation coefficient, R2 coefficient of determination
Fig. 3Images of a normal Achilles tendon using CE and histological correlation. a Conventional ultrasound (US) image of the middle portion of the Achilles tendon in the longitudinal plane. The star indicates the homogenous fibrillar pattern defining normal tendon appearance. b Image of ultrasound elastography (USE) at the same level as in a. The blue-green area of the elastogram represented by the star indicates tissue stiffness where biopsy was subsequently performed. c Histological image obtained with orcein staining showing parallel collagen fibrils, without adipose infiltration and capillary proliferation. Reproduced, with permission, from Klauser et al. [31], copyright (2013) by the Radiological Society of North America, Inc. (RSNA)
Fig. 4Images of an Achilles tendon with tendinopathy using CE and histological correlation. a Conventional US image of the insertion of the Achilles tendon in the longitudinal plane. The asterisks indicate the hypoechoic area without tendon thickening. CAL: calcaneus. b Image of USE at the same level as a. The red area of the elastogram represented by asterisks is indicative of anomalous decrease of stiffness where biopsy was subsequently performed. c Histological image obtained with azan staining showing loss of the parallel fibrillar structure of the collagen, loss of fibre integrity (asterisks), adipose infiltration (circles), capillary proliferation (plus) and mucoid deposition (star). Reproduced, with permission, from Klauser et al. [31], copyright (2013) by the Radiological Society of North America, Inc. (RSNA)
Fig. 5CE in the evaluation of the common tendon of the lateral epicondyle. a USE image of the common extensor tendon in the longitudinal plane in a healthy individual. The tendon insertion is shown to have a rigid homogeneous structure (arrows). b (a) The B-mode conventional US image of the extensor tendon in the longitudinal plane. High-grade tendinosis is seen with fibre dehiscence (yellow arrows). At the same level, Doppler (b) demonstrates hypervascularisation and the elastogram (c) shows pathological decrease of the common extensor tendon stiffness. c (a) B-mode conventional US image of the common extensor tendon in the longitudinal plane demonstrating bulging and thickening of the insertion (white arrows). At the same level, the elastogram (b) shows irregular stiffness, involving the peritendinous fascia (black arrows), with pathological adhesion between the tendon and the surrounding tissue. LE: lateral epicondyle, RH: radiohead. Reproduced, with permission, from Klauser et al. [26], copyright (2014) by the Radiological Society of North America, Inc. (RSNA)
Fig. 6Images of supraspinatus tendon using SWE. a Appearance of a normal supraspinatus tendon showing anisotropy (white arrow) due to curvilinear orientation of the tendon. b Corresponding elastogram showing heterogeneous stiffness in the region of anisotropy and absence of measurement in the deepest region in the humeral head (which is expected since it is a high stiffness structure with limited propagation of the shear waves). c Longitudinal elastography by shear waves of the supraspinatus tendon with tendinopathy. An elastographic pattern of disorganisation and heterogeneity is evidenced, in contrast to the more homogenous pattern of a normal tendon (b). Adapted, with permission, from Winn et al. [18], copyright (2016) The Author(s). Published by Baishideng Publishing Group Inc. All rights reserved