Shear Wave Elastographic Characterization of Normal and Torn Achilles Tendons

Transcription

1 ORIGINAL RESEARCH Shear Wave Elastographic Characterization of Normal and Torn Achilles Tendons A Pilot Study Xiang-Mei Chen, MD, PhD, Li-Gang Cui, MD, PhD, Ping He, MD, PhD, Wei-Wei Shen, MD, MS, Ya-Jun Qian, MD, MS, Jin-Rui Wang, MD, BS Objectives The purpose of this study was to investigate the feasibility of using quantitative shear wave elastography for assessing the functional integrity of the Achilles tendon and to summarize the changes in elasticity of ruptured Achilles tendons in comparison with normal controls. Methods Thirty-six normal and 14 ruptured Achilles tendons were examined with shear wave elastography coupled with a linear array transducer (4 15 MHz). The elasticity value of each Achilles tendon in a longitudinal view was measured. Results The mean elasticity value ± SD for the normal Achilles tendons was ± 4.38 kpa (note that there are saturated measurement phenomena for the normal Achilles tendon, so the actual value will be >300 kpa), whereas the ruptured Achilles tendons had an elasticity value of ± kpa. A statistically significant difference was found in relation to the findings in healthy volunteers (P =.006). Conclusions Our results suggest that shear wave elastography is a valuable tool that can provide complementary biomechanical information for evaluating the function of the Achilles tendon. Key Words Achilles tendon; rupture; shear wave elastography; sonography Received June 4, 2012, from the Department of Ultrasonography, Peking University Third Hospital, Beijing, China. Revision requested June 25, Revised manuscript accepted for publication July 25, Address correspondence to Li-Gang Cui, MD, PhD, Department of Ultrasonography, Peking University Third Hospital, Beijing, China. cuijuegang@126.com Sonoelastography is now routinely used in medical sonography since Ophir et al 1 first described the principles of strain imaging in The technique can assess the elastic properties of tissues, and static elastography has found clinical application in diagnosing lesions of the breast, 2 thyroid, 3 lymph nodes, 4 and prostate gland. 5 The basic principle of sonoelastography is to produce displacement within the tissue by physical compression. By comparing the images taken before and after the application of compression, sonoelastography can show different degrees of displacement. 1 However, the stiffness of the tissue can only be obtained by comparing it with surrounding normal tissues. The degree of the compression applied by the operator may alter the results of sonoelastography by the American Institute of Ultrasound in Medicine

2 Shear wave elastography is a relatively new technique based on automatic generation and analysis of transient shear waves. 6 Images are produced by sending acoustic radiation force impulses through tissues to obtain an elastic modulus, followed by a local measurement to obtain the tissue elasticity in kilopascals. Its major advantages over sonoelastography are that shear wave elastography is quantitative, real-time, and user skill independent. 6 It has successfully been used in breast cancer detection 6 and liver fibrosis staging. 7 However, to our knowledge, there have been no reports on its application for assessment of tissue damage in the Achilles tendon, one of the most often ruptured tendons in sports-related injuries. The purpose of this study was to investigate the feasibility of using quantitative shear wave elastography to assess the functional and structural integrity of the Achilles tendon by comparing the elasticity of ruptured Achilles tendons with normal controls. Materials and Methods Study Population The study was approved by the Institutional Review Board. All patients and healthy volunteers enrolled gave oral and written informed consent. Fourteen ruptured Achilles tendons (all male; age range, years; 10 right side and 4 left side) and 36 normal tendons (25 male and 11 female; age range, years; all right side) were examined. The healthy volunteers enrolled in this study had no history of tendon injury, surgery, or any painful episode, showed no abnormalities on B-mode and color Doppler sonography, and acted as controls. The ruptured tendons included 2 ruptured tendons in the healing stage, which also can be called a subacute tear, and 12 freshly ruptured tendons that had complete full-thickness rupture within 24 hours. In the 12 tendons with complete full-thickness rupture, the mean distance ± SD between the two ends was 0.78 ± 0.76 cm. No participant in either group had diabetes, hypothyroidism, or collagen vascular diseases. Examination Protocol At the start of the study, the healthy volunteers and the patients with ruptured Achilles tendons underwent a routine sonographic examination, including color Doppler imaging. All patients and controls underwent sonography by a radiologist with 5 years of experience in musculoskeletal sonography. Real-time supersonic shear wave elastography (Aix- Plorer; Supersonic Imagine, Aix-en-Provence, France) coupled with a linear array transducer (4 15 MHz) was used to assess the elasticity of the Achilles tendons. Each tendon was scanned in a prone position with the foot hanging over the edge of the examination bed in a neutral position to avoid tendon stress. The tendons were examined in the longitudinal plane. The scanner was placed carefully to ensure that the ultrasound beam was perpendicular to the tendon to avoid anisotropy. Enough ultrasound gel was applied, and tissue compression was avoided during the examination. The middle third part of the normal Achilles tendons and the distal end of the ruptured tendons when they overlapped or the gap between two ends were selected for quantitative measurement. The shear wave elastographic map suspended on the B-mode image was placed at the upper part of the screen with the B-mode image at the lower part. The color scale of elasticity values displayed on right of the image ranged from 0 to 160 kpa, with red representing hardness and blue softness. Data Analysis The elasticity value of each Achilles tendon in a longitudinal view was measured using the Q-Box. The diameter of the box was set at 3.0 to 4.0 mm. The maximum, minimum, and mean elasticity values of the tissues in the box were calculated by the system automatically. The mean elasticity of each tendon was measured 3 times for statistical analysis. Results Quantitative shear wave elastography of the normal tendon tissue clearly delineated the different structures. The elasticity map of the normal Achilles tendons was homogeneous and was in accordance with the shape in the B-mode image (Figure 1). The mean elasticity values derived from those maps was ± 4.38 kpa (range, kpa; note: these are saturated measurements because the maximum output of the AixPlorer system is 300 kpa; therefore, the actual value of the normal tendon should be >300 kpa) for the normal tendons and ± kpa (range kpa) for the ruptured tendons (Figure 2). The anatomic structure of the ruptured tendons was easy to distinguish on the elasticity map. The fresh hematoma between the two ends of a ruptured tendon was anechoic and had an elasticity value of 0 (no signal was retrieved from areas with fluid). On shear wave elastography, a tendon in the healing stage also appeared soft and heterogeneous with indefinite demarcation between the tendon and the softer tissue on the ventral side (Figure 3). The elasticity values of the normal Achilles tendons were significantly higher than those of the ruptured ones (P =.006). 450

3 3203jumvonline.qxp:Layout 1 2/15/13 12:41 PM Page 451 Discussion The Achilles tendon is the strongest and largest tendon in the human body. It is also subjected to the load of the whole body weight and is therefore prone to injury and can rupture frequently. Sonography and magnetic resonance imaging are widely used in the diagnosis of Achilles tendon rupture.8,9 Both of them have the advantages of multiaxis imaging as well as high soft tissue resolution. They show good structural details and can accurately detect the exact location Figure 1. Longitudinal scans of an Achilles tendon in a healthy volunteer. A, Shear wave elastography shows that the normal tendon is hard (red) and homogeneous. The softer tissue on the ventral side is easy to distinguish. B, B-mode sonography has an excellent correlation with shear wave elastography. The boxes are the regions of interest for quantitative measurement. There were 3 different measurement spots, but we selected the values of the middle Q-Box and measured 3 times to calculate the mean elasticity. A B 451

4 and extent of rupture. However, information gathered by these techniques is mostly static and purely anatomic. Indeed, no correlations have been found between these radiologic findings and clinical parameters such as muscle strength, endurance, and range of motion. 9 A new imaging method that could assess the function of Achilles tendons has been the subject of intensive research. The elasticity modulus of the Achilles tendon is a good parameter for assessing its mechanical characteristics. However, most of the previous studies on the elasticity modulus of tendons measured the elasticity of tendons by histologic observation or a tendon tensile test. 10 These experiments could only be performed on animals or in vitro and are not suitable as clinical methods. 11,12 Some studies Figure 2. Longitudinal scans of a freshly ruptured Achilles tendon. A, Shear wave elastography shows that the ruptured end of the tendon is soft (blue), and the fresh hematoma has no elasticity. B, B-mode sonography shows that the tendon is swollen with anechoic hematoma between the ruptured ends. The boxes are the regions of interest for quantitative measurement. A B 452

5 used a force-elongation curve to calculate the Young modulus of the tendon. This method used displacement measurements of ultrasound echoes generated from the tendon during muscle contraction in vivo. 13,14 Measurement of tendon movement was based on manual tracking of anatomic landmarks such as the myotendinous junction, which limited the applicability to a small number of muscle-tendon units. Moreover, this method neglected the rotation of the joint axis during contraction. Sonoelastography is an attractive method for its noninvasiveness and convenience. There are 3 main types of sonographic elasticity imaging: (1) elastography that tracks tissue movement during compression to obtain an estimate of strain; (2) sonoelastography that uses color Doppler to Figure 3. Longitudinal scans of a ruptured Achilles tendon in the healing stage. A, Shear wave elastography shows that the tendon is soft (blue) and heterogeneous. The demarcation between the tendon and the softer tissue on the ventral side is indefinite. B, B-mode sonography shows that the tendon is thickened and heterogeneous. The boxes are the regions of interest for quantitative measurement. A B 453

6 generate an image of tissue movement in response to external vibrations; and (3) tracking of shear wave propagation through tissue to obtain the elasticity. 15 There are only a few studies of Achilles tendons using sonoelastography, most of which used the method that tracks tissue movement during compression. 16,17 This method has the disadvantages of being operator dependent, which often results in poor reproducibility and lack of quantitative information. 18 Hence, the conclusions from these studies have been confounding. Some investigators found that normal Achilles tendons appeared hard, whereas swollen and painful tendons were distinctly softer on real-time sonoelastography. 17 Other researchers found that painful and enlarged Achilles tendons showed increased stiffness compared with normal ones. 19 To date, only one study using shear wave elastography on Achilles tendons has been published. 20 The authors measured the elasticity of various normal tissues including the Achilles tendon. In our study, we focused on the feasibility of using shear wave elastography of only the Achilles tendon. Our study results showed that the quantitative shear wave elastographic map of the normal tendon tissue clearly delineated different structures. The normal Achilles tendons were found to be hard and homogeneous. The outline of the normal Achilles tendon was in accordance with that of the B-mode image. In contrast, the ruptured tendons showed lower and heterogeneous elasticity compared with the normal tendons. For acute rupture, the fresh hematoma is fluidlike, which has no signal retrieved during shear wave elastography and has an elasticity value dropping dramatically to 0. Low and heterogeneous elasticity was also observed in tendons during healing in the subacute stage, which suggesting a loss of elasticity despite being clinically healed. These results could be explained by changes in the histologic structure of normal versus ruptured tendons. It is known that a normal tendon has a multilevel hierarchical structure composed of collagen molecules, fibrils, fiber bundles, fascicles, and tendon units that run parallel to the tendon s longitudinal axis. 13,21 Therefore, the elasticity of normal Achilles tendons appears hard and homogeneous on sonography. On the other hand, ruptured tendons show a loss of the finer fiber structures, and the parallel arrangement is also lost and haphazard, 21 and tenocytes from ruptured Achilles tendons produce greater quantities of type III collagen than tenocytes from normal Achilles tendons. 11 This collagen abnormality may result in less resistance to tensile forces and reduced elasticity. 21 In addition to complete rupture, tendinosis and partial tendon tears have the same pathologic changes; therefore, they may show the same soft changes. Our next study will focus on quantitative strength assessment of this kind of tendon for both early diagnosis and monitoring for recovery, which would likely have a clinical impact on not only rehabilitation but also return to activities (specifically in high-level athletes). Arda et al 20 reported the mean real elasticity value of normal Achilles tendons to be 51.5 ± 25.1 kpa, which was very different from our measurement. Compared with other tissues, the structure of tendons is very different. The most characteristic feature is anisotropy, which means that the echo character is dependent on the incidence angle.when tendons are examined with an incidence angle far from 90, the tendons will show hypoechogenicity that is similar to tendinosis. For shear wave elastographic measurement of the Achilles tendon, a fast shear wave speed was found when measured in the longitudinal plane. This finding may be the reason for the difference in the real elasticity value of the normal Achilles tendons between the two studies. In summary, shear wave elastography is a promising technique for assessing the elasticity of the Achilles tendon. It has the advantages of being quantitative, real-time, and user skill independent. It may provide more functional information than traditional imaging techniques in evaluating the healing process after a tendon rupture, which can help optimize treatment in functional rehabilitation of a ruptured tendon. Although the sample size in this study was small and the normal tendon measurement was not actual because of the saturation limitation, to our knowledge, a study attempting to explore Achilles tendon and tendon rupture elasticity using quantitative shear wave elastography has not been reported previously. We hope that our findings will lead to more studies investigating the Achilles tendon using sonoelastography. References 1. Ophir J, Céspedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991; 13: Wojcinski S, Farrokh A, Weber S, et al. Multicenter study of ultrasound real-time tissue elastography in 779 cases for the assessment of breast lesions: improved diagnostic performance by combining the BI-RADS - US classification system with sonoelastography. Ultraschall Med 2010; 31: Lyshchik A, Higashi T, Asato R, et al. Thyroid gland tumor diagnosis at US elastography. Radiology 2005; 237: Alam F, Naito K, Horiguchi J, Fukuda H, Tachikake T, Ito K. Accuracy of sonographic elastography in the differential diagnosis of enlarged cervical lymph nodes: comparison with conventional B-mode sonography. AJR Am J Roentgenol 2008; 191:

7 5. Pallwein L, Mitterberger M, Pinggera G, et al. Sonoelastography of the prostate: comparison with systematic biopsy findings in 492 patients. Eur J Radiol 2008; 65: Athanasiou A, Tardivon A, Tanter M, et al. Breast lesions: quantitative elastography with supersonic shear imaging preliminary results. Radiology 2010; 256: Bavu E, Gennisson JL, Mallet V, et al. Supersonic shear imaging is a new potent morphological non-invasive technique to assess liver fibrosis, part 1: technical feasibility. Hepatology 2010; 52(suppl):S 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: Möller M, Kalebo P, Tidebrant G, Movin T, Karlsson J. The ultrasonographic appearance of the ruptured Achilles tendon during healing: a longitudinal evaluation of surgical and nonsurgical treatment, with comparisons to MRI appearance. Knee Surg Sports Traumatol Arthrosc 2002; 10: Hoffmeister BK, Handley SM, Wickline SA, Miller JG. Ultrasonic determination of the anisotropy of Young s modulus of fixed tendon and fixed myocardium. J Acoust Soc Am 1996; 100: Kuo PL, Li PC, Shun CT, Lai JS. Strain measurements of rabbit Achilles tendons by ultrasound. Ultrasound Med Biol 1999; 25: Kuo PL, Li PC, Li ML. Elastic properties of tendon measured by two different approaches. Ultrasound Med Biol 2001; 27: Maganaris CN, Paul JP. In vivo human tendon mechanical properties. J Physiol 1999; 521: Maganaris CN, Paul JP. Tensile properties of the in vivo human gastrocnemius tendon. J Biomech 2002; 35: Garra BS. Imaging and estimation of tissue elasticity by ultrasound. Ultrasound Q 2007; 23: Drakonaki EE, Allen GM, Wilson DJ. Real-time ultrasound elastography of the normal Achilles tendon: reproducibility and pattern description. Clin Radiol 2009; 64: 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: Klauser AS, Faschingbauer R, Jaschke WR. Is sonoelastography of value in assessing tendons? Semin Musculoskelet Radiol 2010; 14: Sconfienza LM, Silvestri E, Cimmino MA. Sonoelastography in the evaluation of painful Achilles tendon in amateur athletes. Clin Exp Rheumatol 2010; 28: Arda K, Ciledag N, Aktas E, Aribas BK, Kose K. Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography. AJR Am J Roentgenol 2011; 197: Wang JH. Mechanobiology of tendon. J Biomech 2006; 39: