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ORIGINAL RESEARCH
In Vivo Measurement of Rotator Cuff Tendon Strain With Ultrasound Elastography An Investigation Using a Porcine Model Taku Hatta, MD, PhD, Nobuyuki Yamamoto, MD, PhD, Hirotaka Sano, MD, PhD, Eiji Itoi, MD, PhD
Objectives—To clarify the relationship between the strain ratio measured by ultrasound elastography and the mechanical properties of the tendon measured by a universal testing machine. We also attempted to determine the effect of the type and depth of soft tissue overlying the tendon on the elastographic measurement. Methods—Twelve fresh porcine shoulders were prepared. Elastographic measurement was performed on the infraspinatus tendon by manually applying repetitive compressions from an ultrasound probe with an acoustic coupler consisting of an elastomer with definite elasticity as a reference material. The strain ratio, defined as tendon/reference strain, was obtained by 4 different approaches: with the probe placed on the skin, on the subcutaneous fat after removing the skin, on the muscle after removing the subcutaneous fat, and directly on the tendon. The strain ratios measured by these approaches were compared statistically. The relationship between the depth of the tendon measured on elastography and the strain ratio was also investigated. We also attempted to clarify the relationship between the strain ratio of the tendon and its elastic property. The tendon was mounted on a testing machine, and compressive force was applied. Tendon compliance was calculated as the reciprocal of the Young modulus in the range of 5% to 10% strain, which was compared to its strain ratio. Results—The tendon/reference strain ratio significantly correlated with the tendon compliance (r = 0.73; P < .01). The strain ratio was not affected by differences in the measuring approaches (P = .4) or by the depth to the tendon level (P = .8). Received September 5, 2013, from the Department of Orthopedic Surgery, Tohoku University Graduate School of Medicine, Sendai, Japan. Revision requested September 26, 2013. Revised manuscript accepted for publication December 23, 2013. We thank Hitachi Aloka Medical, Ltd, for providing the acoustic coupler and Hideaki Nagamoto, MD, Hiroyuki Takahashi, MD, PhD, Hiroaki Shimokawa, MD, PhD, Kenta Ito, MD, PhD, Yoshitaka Ito, MD, PhD, and the staff of the Department of Cardiovascular Medicine, Tohoku University Graduate School of Medicine, for help with collection of samples. Address correspondence to Eiji Itoi, MD, PhD, Department of Orthopedic Surgery, Tohoku University School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan. E-mail: [email protected] doi:10.7863/ultra.33.9.1641
Conclusions—Our results indicated that the strain ratio of the rotator cuff tendon could be measured with minimal influence by overlying soft tissues if its depth from the skin was less than 22 mm. We believe that ultrasound elastography would be a useful tool for assessment of tendon elasticity in clinical practice. Key Words—elastic modulus; musculoskeletal ultrasound; rotator cuff tendon; strain ratio; ultrasound elastography
R
otator cuff tendon tears are commonly seen in the middleaged and elderly populations. Although the underlying causes remain unknown, the incidence of degenerative changes of the rotator cuff tendon and the size of rotator cuff tears are known to progress with age.1–3 Several studies using a multistage disease model have reported that the metabolism, cellular composition, and composition of the extracellular matrix of the edge of the torn tendon were altered significantly with an increase in the size of the tear.4,5
©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:1641–1646 | 0278-4297 | www.aium.org
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In addition, torn rotator cuff tendons have shown a significant alteration of their mechanical properties in comparison with intact tendons.6 These previous studies indicate that the mechanical properties of the rotator cuff tendon are potential parameters that could be involved in the mechanisms of development and progression of tears. In other words, in vivo assessment of the mechanical properties of the tendon might provide useful information for detecting subclinical abnormalities even in a healthy population. Ultrasound elastography has recently been developed to allow noninvasive assessment of tissue mechanical properties.7,8 The principle of ultrasound elastography is based on real-time measurement of tissue strain by using an ultrasound probe to provide external freehand compression of the tissue; the strain rate is smaller in harder tissues than in softer tissues. According to previous studies, this method has been shown to be useful in the differential diagnosis of malignant tumors, including breast, thyroid, and prostate tumors.9–11 Moreover, the built-in software of the ultrasound system can be used to calculate the strain ratio between any two regions. In several clinical studies, measurements of the tissue strain ratio have been examined to determine its usefulness as a semiquantitative elasticity parameter for muscle12–14 as well as the Achilles tendon.15 Ariji et al12 assessed muscle hardness in human participants with the use of the strain ratio between the muscle and subcutaneous fat as a reference. They revealed the intraexaminer and interexaminer reliability as well as the responsiveness (before and after massage) of the strain ratio. Niitsu et al13 and Yanagisawa et al14 investigated the muscle strain ratio with the use of reference gel, which was placed on the skin. It is notable that Niitsu et al13 verified the validity of the strain ratio. They found a positive correlation between the strain ratio and the existing parameters for muscle hardness. Regarding the strain ratio for tendons, Drakonaki and Allen15 first measured the strain ratio between the Achilles tendon and the peripheral fat and reported the good to excellent intraexaminer and interexaminer reliability for tendon assessment. On the other hand, the feasibility of using the strain ratio as measured by ultrasound elastography as a parameter for tendon elasticity has not yet been sufficiently verified. In addition, the effect of overlying soft tissues, including the skin, subcutaneous fat, and muscle, on elastographic measurement of deeper tendon tissue has been less documented. Each soft tissue has a specific material property. Since manual compression is applied to the body surface by the ultrasound probe during elastographic measurement, it might be possible that the presence of
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overlying soft tissues affects the amount of tendon strain. Therefore, we assumed that the effect of overlying soft tissues needs to be clarified for the clinical application of ultrasound elastography. In this study, we used fresh porcine shoulder specimens to assess rotator cuff tendon elasticity. To measure the tissue strain ratio, an acoustic coupler prepared from a reference material was attached to the tip of the ultrasound probe. The purposes of the study were to clarify the relationship between the strain ratio and the elastic moduli measured by a universal testing machine and to determine the effects of soft tissues overlying the tendon and their depths (from the skin surface to the level of the tendon) on elastographic measurement of the tendon.
Materials and Methods Patients All of the experiments followed protocols approved by the Ethics Committee of the authors’ institution. The infraspinatus tendons from 12 mature adult pigs were used. Each specimen was prepared by detaching the scapula along with the forelimb from the trunk. Ultrasound Elastography A commercially available ultrasound system (HI VISION Preirus; Hitachi Aloka Medical, Ltd, Tokyo, Japan) and an electronic linear array probe (EUP-L65, 6–14 MHz; Hitachi Aloka Medical, Ltd) were used to perform the ultrasound examinations of all samples. To measure the strain values of the tendon and the reference material simultaneously, an acoustic coupler that consisted of an elastomer with definite elasticity was attached to the tip of the ultrasound probe (Figure 1). Built-in software was used
Figure 1. Ultrasound probe for measurement of the tendon/reference strain ratio. To obtain the reference strain value on ultrasound elastography, an acoustic coupler (arrowheads), which consisted of an elastomer with definite elasticity, was attached to the tip of the probe.
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to measure the strain values of the tendon (A) and the reference (B) in each elastographic image. Then, the tendon/ reference strain ratio (A/B) was calculated to assess the elasticity of the infraspinatus tendon. In this study, we always performed elastographic measurement at the same point along the tendon. The region of interest for measuring the strain values of the tendon was placed as follows: the center of the region of interest was placed 10 mm medial to the tendon-to-bone insertion, and the area was placed to include the whole thickness of the tendon. The investigator repeated the measurement 9 times for each specimen, and the mean strain ratio value was recorded to be used in the following assessment. B-mode ultrasound was initially used for percutaneous observation of the infraspinatus tendons from their humeral insertion to the myotendinous junction in longitudinal planes. Elastographic measurement was performed on the same area of the tendon. First, the tendon/reference strain ratio was measured by a percutaneous approach. After removing the skin, the strain ratio was measured by a transsubcutaneous fat approach. Next, after removing the subcutaneous fat tissue overlying the muscles, the strain ratio was measured by a transmuscular approach. Finally, the infraspinatus tendon was exposed by stripping off the overlying muscle fibers. After attaching the acoustic coupler to the tendon, the strain ratio was measured by a direct tendon approach. The strain ratio values measured by these 4 approaches were statistically compared. In addition, for the purpose of determining whether the difference in the depth to the tendon affected the strain ratio, elastographic images for percutaneous strain ratio measurement were assessed; the depth from the skin surface to the level of the tendon was measured by the built-in software. The depth measured in each specimen was statistically compared with the percutaneous strain ratio.
and the position and load data were collected at 100 Hz. A compressive load was applied perpendicularly to the tendon surface at the point 10 mm medial to the distal edge, where we measured the strain ratio on elastography. As the elastic property of the tendons, compliance was calculated as the reciprocal of the Young modulus in the range of 5% to 10% strain. To assess the positive correlation with the values obtained by elastographic measurement, the compliance of the tendon was statistically compared with the direct tendon strain ratio. Statistical Analyses The Kruskal-Wallis test with Dunn post hoc adjustment was used to evaluate the significant differences among the 4 measurement approaches for the strain ratio of the infraspinatus tendon. Pearson correlation coefficient analysis and simple regression analysis were applied to determine the relationship between the compliance and strain ratio values as well as that between the depth from the skin surface to the tendon and the strain ratio. Statistical analyses were performed with Prism version 5.0 software (GraphPad Software, San Diego, CA). The level of significance was set at P < .05.
Figure 2. Experimental conditions for measuring the elastic modulus of the infraspinatus tendon.
Elastic Modulus of the Tendon The infraspinatus tendon was detached from the scapula and mounted on a universal testing machine (model 3342; Instron, Norwood, MA). As shown in Figure 2, care was taken to maintain the same length as the predetached tendon. For fixation of the tendon, a wooden frame with a length of 100 mm was prepared. Both the distal and proximal ends of the detached tendon specimen were sutured to the frame. For the mechanical testing, a load cell rated to 10 N was used. This load cell was certified to an accuracy of 0.01 N with sensitivity of 0.001 N, and its diameter was 3.0 mm. The tendon strain was measured at a rate of 1 mm/min,
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Results Strain ratio values between the tendon and the acoustic coupler as measured by the 4 approaches (percutaneous, trans-subcutaneous fat, transmuscular, and direct tendon) were successfully obtained (Figure 3). Ultrasound elastography showed a consistent color pattern for each type of tissue. In most experiments, the tendon appeared green and blue, whereas the muscle had a red pattern. Regarding assessment of the validity of the tendon/ reference strain ratio for tissue elasticity, the strain ratio values measured by the direct tendon approach correlated significantly with the tendon compliance (r = 0.73; P < .01; Figure 4). The strain ratio of the tendon was not changed significantly during the sequential removal of overlying soft tissues. The mean tendon/reference strain ratios ± SDs as measured by the 4 approaches (percutaneous, trans-subcutaneous fat, transmuscular, and direct tendon) were 0.54 ± 0.08, 0.50 ± 0.17, 0.47 ± 0.14, and 0.48 ± 0.15, respectively. There were no significant differences among the 4 measurement approaches (P = .4; Figure 5). Overlying soft tissue depths measured from elastographic images by the
percutaneous approach ranged from 15.5 to 21.6 mm. Regarding the comparison between the strain ratio and the overlying soft tissue depth, no significant correlations between these parameters were seen as long as the depth was less than 22 mm (r = –0.05; P = .8; Figure 6).
Discussion The reliability of elastographic measurements has been investigated in several studies.15–19 In particular, for tendon tissues, Drakonaki and Allen15 reported the reliability of the strain ratio in assessing the elasticity of the normal Achilles tendon. They concluded that ultrasound elastography might be a useful measurement technique with enough intraexaminer and interexaminer reproducibility. In our study, the tendon/reference strain ratios in fresh porcine rotator cuff tendons were not affected significantly by different depths of overlying soft tissues, including the skin, subcutaneous fat, and muscles, as well as removal of any soft tissues. On the basis of previous evidence along with that from our study, we believe that elastographic measurement may be a reliable tool for assessing in vivo tendons with a variety of overlying soft tissues if their depth from the skin is less than 22 mm.
Figure 3. Tendon/reference strain ratio measurement by ultrasound elastography by the following 4 measuring approaches: percutaneous approach (A), trans-subcutaneous fat tissue approach (B), transmuscular approach (C), and direct tendon approach (D). H indicates humerus; M, muscle; S, skin; SF, subcutaneous fat; and T, tendon.
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In addition, our study indicated a significant relationship between the strain ratio and the elastic modulus of the tendons. In this study, we adopted an elastomer as a reference for the strain ratio to measure tendon elasticity. It has been reported that peripheral fat tissue could be used as a reference for measurement of Achilles tendon elasticity. However, the subcutaneous fat layer is not always thick enough to place a region of interest for elastographic measurement. Moreover, age and sex differences in the elasticity of fat tissue need to be considered. On the basis of our study, the use of a specially designed acoustic coupler, as in this study, might be recommended for measuring valid tendon strain ratio values, instead of using such an internal reference. Figure 4. Relationship between tendon compliance and the tendon/ reference strain ratio. The strain ratio for the tendon correlated positively with the compliance, which was obtained with strain of 5% to 10% (r = 0.73; P < .01).
For assessment of tendon elasticity with ultrasound elastography, there are two different imaging planes: longitudinal and transverse. According to a recent study comparing these planes for elastography, the measurement in the longitudinal plane is easier to acquire and more reproducible than that in the transverse plane.20 Based on this evidence, all experiments in our study were performed in the longitudinal plane. In the clinical setting, a rotator cuff tendon tear frequently occurs at the anterior third of the supraspinatus tendon, where the elastic modulus is greater than that in the middle third or posterior third.20,21 Recently, a number of risk and protective factors for tendon injuries have been reported to affect tendon elasticity. Burgess et al22 reported a decrease in the elastic modulus of the gastrocnemius tendon after stretching exercises, which are widely believed to prevent tendon injuries. In addition, Eliasson et al23 reported that the elastic modulus increased under conditions of disuse in a rat Achilles tendon model. Moreover, Ichinose et al24 revealed that consecutive exposures to nicotine, which is the primary chemical component of cigarettes, altered the elastic modulus of the supraspinatus tendon in a rat model. More recently, some clinical studies applied ultrasound elastography to tendon tissue for the purpose of investigating its alteration compared with the normal tendon. De Zordo et al25 compared elastographic findings in Achilles tendons between 25 patients with chronic tendinopathy and 25 healthy participants. They found marked or mild softening more frequently in symptomatic tendons than in normal tendons. Although elastography Figure 6. Distribution of percutaneous tendon/reference strain ratios and depths from the skin surface to the level of tendon. No significant correlation between the strain ratios and the depths was seen (r = –0.05; P = .8).
Figure 5. Tendon/reference strain ratios obtained by ultrasound elastography with the 4 measurement approaches: percutaneous approach (SRP), trans-subcutaneous fat tissue approach (SRTF), transmuscular approach (SRTM), and direct tendon approach (SRDT) (P = .4, KruskalWallis test).
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provides useful information concerning material properties of the rotator cuff tendon under in vivo conditions, further studies using both normal and pathologic tendons would be necessary to clarify the true pathogenesis of rotator cuff tears. There were several limitations in this study. First, the data for tendon elasticity were obtained from fresh porcine shoulders. To address the efficacy of elastographic measurement in a clinical setting, differences among species should be taken into consideration. Second, elastographic measurement has technical difficulties, especially for the rotator cuff tendon, due to the existence of adjacent bony structures (eg, acromion and greater tuberosity). As using a freehand technique to assess the elasticity of the rotator cuff tendon reliably is a major limitation, further improvement may be needed. Third, especially in the clinical use of elastography for shoulder joints, we occasionally examine patients with severely thickened subcutaneous fat tissues. In this study, there were no data for overlying soft tissues deeper than approximately 22 mm. Further studies would be necessary to determine the maximum depth for performing elastographic measurements validly. In conclusion, the tendon/reference strain ratio may be feasible for assessing tendon elasticity semiquantitatively. Elastographic measurement may be used with minimal influence by the overlying soft tissues within a 22-mm depth from the skin.
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Hijioka A, Suzuki K, Nakamura T, Hojo T. Degenerative change and rotator cuff tears: an anatomical study in 160 shoulders of 80 cadavers. Arch Orthop Trauma Surg 1993; 112:61–64. Sher JS, Uribe JW, Posada A, Murphy BJ, Zlatkin MB. Abnormal findings on magnetic resonance images of asymptomatic shoulders. J Bone Joint Surg Am 1995; 77:10–15. Minagawa H, Yamamoto N, Abe H, et al. Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: from massscreening in one village. J Orthop 2013; 10:8–12. Matthews TJ, Hand GC, Rees JL, Athanasou NA, Carr AJ. Pathology of the torn rotator cuff tendon: reduction in potential for repair as tear size increases. J Bone Joint Surg Br 2006; 88:489–495. Tashjian RZ, Farnham JM, Albright FS, Teerlink CC, Cannon-Albright LA. Evidence for an inherited predisposition contributing to the risk for rotator cuff disease. J Bone Joint Surg Am 2009; 91:1136–1142. Chaudhury S, Holland C, Vollrath F, Carr AJ. Comparing normal and torn rotator cuff tendons using dynamic shear analysis. J Bone Joint Surg Br 2011; 93:942–948. Hall TJ, Zhu Y, Spalding CS. In vivo real-time freehand palpation imaging. Ultrasound Med Biol 2003; 29:427–435. Itoh A, Ueno E, Tohno E, et al. Breast disease: clinical application of US elastography for diagnosis. Radiology 2006; 239:341–350.
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Athanasiou A, Tardivon A, Tanter M, et al. Breast lesions: quantitative elastography with supersonic shear imaging—preliminary results. Radiology 2010; 256:297–303. Lyshchik A, Higashi T, Asato R, et al. Thyroid gland tumor diagnosis at US elastography. Radiology 2005; 237:202–211. König K, Scheipers U, Pesavento A, Lorenz A, Ermert H, Senge T. Initial experiences with real-time elastography guided biopsies of the prostate. J Urol 2005; 174:115–117. Ariji Y, Katsumata A, Hiraiwa Y, et al. Use of sonographic elastography of the masseter muscles for optimizing massage pressure: a preliminary study. J Oral Rehabil 2009; 36:627–635. Niitsu M, Michizaki A, Endo A, Takei H, Yanagisawa O. Muscle hardness measurement by using ultrasound elastography: a feasibility study. Acta Radiol 2011; 52:99–105. Yanagisawa O, Niitsu M, Kurihara T, Fukubayashi T. Evaluation of human muscle hardness after dynamic exercise with ultrasound real-time tissue elastography: a feasibility study. Clin Radiol 2011; 66:815–819. Drakonaki EE, Allen GM. Magnetic resonance imaging, ultrasound and real-time ultrasound elastography of the thigh muscles in congenital muscle dystrophy. Skeletal Radiol 2010; 39:391–396. Havre RF, Elde E, Gilja OH, et al. Freehand real-time elastography: impact of scanning parameters on image quality and in vitro intra- and interobserver validations. Ultrasound Med Biol 2008; 34:1638–1650. Koizumi Y, Hirooka M, Kisaka Y, et al. Liver fibrosis in patients with chronic hepatitis C: noninvasive diagnosis by means of real-time tissue elastography—establishment of the method for measurement. Radiology 2011; 258:610–617. Yoon JH, Kim MH, Kim EK, Moon HJ, Kwak JY, Kim MJ. Interobserver variability of ultrasound elastography: how it affects the diagnosis of breast lesions. AJR Am J Roentgenol 2011; 196:730–736. Akagi R, Chino K, Dohi M, Takahashi H. Relationships between muscle size and hardness of the medial gastrocnemius at different ankle joint angles in young men. Acta Radiol 2012; 53:307–311. Tuite MJ, Turnbull JR, Orwin JF. Anterior versus posterior, and rim-rent rotator cuff tears: prevalence and MR sensitivity. Skeletal Radiol 1998; 27:237–243. Itoi E, Berglund LJ, Grabowski JJ, et al. Tensile properties of the supraspinatus tendon. J Orthop Res 1995; 13:578–584. Burgess KE, Graham-Smith P, Pearson SJ. Effect of acute tensile loading on gender-specific tendon structural and mechanical properties. J Orthop Res 2009; 27:510–516. Eliasson P, Fahlgren A, Pasternak B, Aspenberg P. Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J Appl Physiol (1985) 2007; 103:459–463. Ichinose R, Sano H, Kishimoto KN, Sakamoto N, Sato M, Itoi E. Alteration of the material properties of the normal supraspinatus tendon by nicotine treatment in a rat model. Acta Orthop 2010; 81:634–638. De Zordo T, Chem R, Smekal V, et al. Real-time sonoelastography: findings in patients with symptomatic Achilles tendons and comparison to healthy volunteers. Ultraschall Med 2010; 31:394–400.
J Ultrasound Med 2014; 33:1641–1646
ORIGINAL RESEARCH
In Vivo Measurement of Rotator Cuff Tendon Strain With Ultrasound Elastography An Investigation Using a Porcine Model Taku Hatta, MD, PhD, Nobuyuki Yamamoto, MD, PhD, Hirotaka Sano, MD, PhD, Eiji Itoi, MD, PhD
Objectives—To clarify the relationship between the strain ratio measured by ultrasound elastography and the mechanical properties of the tendon measured by a universal testing machine. We also attempted to determine the effect of the type and depth of soft tissue overlying the tendon on the elastographic measurement. Methods—Twelve fresh porcine shoulders were prepared. Elastographic measurement was performed on the infraspinatus tendon by manually applying repetitive compressions from an ultrasound probe with an acoustic coupler consisting of an elastomer with definite elasticity as a reference material. The strain ratio, defined as tendon/reference strain, was obtained by 4 different approaches: with the probe placed on the skin, on the subcutaneous fat after removing the skin, on the muscle after removing the subcutaneous fat, and directly on the tendon. The strain ratios measured by these approaches were compared statistically. The relationship between the depth of the tendon measured on elastography and the strain ratio was also investigated. We also attempted to clarify the relationship between the strain ratio of the tendon and its elastic property. The tendon was mounted on a testing machine, and compressive force was applied. Tendon compliance was calculated as the reciprocal of the Young modulus in the range of 5% to 10% strain, which was compared to its strain ratio. Results—The tendon/reference strain ratio significantly correlated with the tendon compliance (r = 0.73; P < .01). The strain ratio was not affected by differences in the measuring approaches (P = .4) or by the depth to the tendon level (P = .8). Received September 5, 2013, from the Department of Orthopedic Surgery, Tohoku University Graduate School of Medicine, Sendai, Japan. Revision requested September 26, 2013. Revised manuscript accepted for publication December 23, 2013. We thank Hitachi Aloka Medical, Ltd, for providing the acoustic coupler and Hideaki Nagamoto, MD, Hiroyuki Takahashi, MD, PhD, Hiroaki Shimokawa, MD, PhD, Kenta Ito, MD, PhD, Yoshitaka Ito, MD, PhD, and the staff of the Department of Cardiovascular Medicine, Tohoku University Graduate School of Medicine, for help with collection of samples. Address correspondence to Eiji Itoi, MD, PhD, Department of Orthopedic Surgery, Tohoku University School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan. E-mail: [email protected] doi:10.7863/ultra.33.9.1641
Conclusions—Our results indicated that the strain ratio of the rotator cuff tendon could be measured with minimal influence by overlying soft tissues if its depth from the skin was less than 22 mm. We believe that ultrasound elastography would be a useful tool for assessment of tendon elasticity in clinical practice. Key Words—elastic modulus; musculoskeletal ultrasound; rotator cuff tendon; strain ratio; ultrasound elastography
R
otator cuff tendon tears are commonly seen in the middleaged and elderly populations. Although the underlying causes remain unknown, the incidence of degenerative changes of the rotator cuff tendon and the size of rotator cuff tears are known to progress with age.1–3 Several studies using a multistage disease model have reported that the metabolism, cellular composition, and composition of the extracellular matrix of the edge of the torn tendon were altered significantly with an increase in the size of the tear.4,5
©2014 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2014; 33:1641–1646 | 0278-4297 | www.aium.org
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In addition, torn rotator cuff tendons have shown a significant alteration of their mechanical properties in comparison with intact tendons.6 These previous studies indicate that the mechanical properties of the rotator cuff tendon are potential parameters that could be involved in the mechanisms of development and progression of tears. In other words, in vivo assessment of the mechanical properties of the tendon might provide useful information for detecting subclinical abnormalities even in a healthy population. Ultrasound elastography has recently been developed to allow noninvasive assessment of tissue mechanical properties.7,8 The principle of ultrasound elastography is based on real-time measurement of tissue strain by using an ultrasound probe to provide external freehand compression of the tissue; the strain rate is smaller in harder tissues than in softer tissues. According to previous studies, this method has been shown to be useful in the differential diagnosis of malignant tumors, including breast, thyroid, and prostate tumors.9–11 Moreover, the built-in software of the ultrasound system can be used to calculate the strain ratio between any two regions. In several clinical studies, measurements of the tissue strain ratio have been examined to determine its usefulness as a semiquantitative elasticity parameter for muscle12–14 as well as the Achilles tendon.15 Ariji et al12 assessed muscle hardness in human participants with the use of the strain ratio between the muscle and subcutaneous fat as a reference. They revealed the intraexaminer and interexaminer reliability as well as the responsiveness (before and after massage) of the strain ratio. Niitsu et al13 and Yanagisawa et al14 investigated the muscle strain ratio with the use of reference gel, which was placed on the skin. It is notable that Niitsu et al13 verified the validity of the strain ratio. They found a positive correlation between the strain ratio and the existing parameters for muscle hardness. Regarding the strain ratio for tendons, Drakonaki and Allen15 first measured the strain ratio between the Achilles tendon and the peripheral fat and reported the good to excellent intraexaminer and interexaminer reliability for tendon assessment. On the other hand, the feasibility of using the strain ratio as measured by ultrasound elastography as a parameter for tendon elasticity has not yet been sufficiently verified. In addition, the effect of overlying soft tissues, including the skin, subcutaneous fat, and muscle, on elastographic measurement of deeper tendon tissue has been less documented. Each soft tissue has a specific material property. Since manual compression is applied to the body surface by the ultrasound probe during elastographic measurement, it might be possible that the presence of
1642
overlying soft tissues affects the amount of tendon strain. Therefore, we assumed that the effect of overlying soft tissues needs to be clarified for the clinical application of ultrasound elastography. In this study, we used fresh porcine shoulder specimens to assess rotator cuff tendon elasticity. To measure the tissue strain ratio, an acoustic coupler prepared from a reference material was attached to the tip of the ultrasound probe. The purposes of the study were to clarify the relationship between the strain ratio and the elastic moduli measured by a universal testing machine and to determine the effects of soft tissues overlying the tendon and their depths (from the skin surface to the level of the tendon) on elastographic measurement of the tendon.
Materials and Methods Patients All of the experiments followed protocols approved by the Ethics Committee of the authors’ institution. The infraspinatus tendons from 12 mature adult pigs were used. Each specimen was prepared by detaching the scapula along with the forelimb from the trunk. Ultrasound Elastography A commercially available ultrasound system (HI VISION Preirus; Hitachi Aloka Medical, Ltd, Tokyo, Japan) and an electronic linear array probe (EUP-L65, 6–14 MHz; Hitachi Aloka Medical, Ltd) were used to perform the ultrasound examinations of all samples. To measure the strain values of the tendon and the reference material simultaneously, an acoustic coupler that consisted of an elastomer with definite elasticity was attached to the tip of the ultrasound probe (Figure 1). Built-in software was used
Figure 1. Ultrasound probe for measurement of the tendon/reference strain ratio. To obtain the reference strain value on ultrasound elastography, an acoustic coupler (arrowheads), which consisted of an elastomer with definite elasticity, was attached to the tip of the probe.
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to measure the strain values of the tendon (A) and the reference (B) in each elastographic image. Then, the tendon/ reference strain ratio (A/B) was calculated to assess the elasticity of the infraspinatus tendon. In this study, we always performed elastographic measurement at the same point along the tendon. The region of interest for measuring the strain values of the tendon was placed as follows: the center of the region of interest was placed 10 mm medial to the tendon-to-bone insertion, and the area was placed to include the whole thickness of the tendon. The investigator repeated the measurement 9 times for each specimen, and the mean strain ratio value was recorded to be used in the following assessment. B-mode ultrasound was initially used for percutaneous observation of the infraspinatus tendons from their humeral insertion to the myotendinous junction in longitudinal planes. Elastographic measurement was performed on the same area of the tendon. First, the tendon/reference strain ratio was measured by a percutaneous approach. After removing the skin, the strain ratio was measured by a transsubcutaneous fat approach. Next, after removing the subcutaneous fat tissue overlying the muscles, the strain ratio was measured by a transmuscular approach. Finally, the infraspinatus tendon was exposed by stripping off the overlying muscle fibers. After attaching the acoustic coupler to the tendon, the strain ratio was measured by a direct tendon approach. The strain ratio values measured by these 4 approaches were statistically compared. In addition, for the purpose of determining whether the difference in the depth to the tendon affected the strain ratio, elastographic images for percutaneous strain ratio measurement were assessed; the depth from the skin surface to the level of the tendon was measured by the built-in software. The depth measured in each specimen was statistically compared with the percutaneous strain ratio.
and the position and load data were collected at 100 Hz. A compressive load was applied perpendicularly to the tendon surface at the point 10 mm medial to the distal edge, where we measured the strain ratio on elastography. As the elastic property of the tendons, compliance was calculated as the reciprocal of the Young modulus in the range of 5% to 10% strain. To assess the positive correlation with the values obtained by elastographic measurement, the compliance of the tendon was statistically compared with the direct tendon strain ratio. Statistical Analyses The Kruskal-Wallis test with Dunn post hoc adjustment was used to evaluate the significant differences among the 4 measurement approaches for the strain ratio of the infraspinatus tendon. Pearson correlation coefficient analysis and simple regression analysis were applied to determine the relationship between the compliance and strain ratio values as well as that between the depth from the skin surface to the tendon and the strain ratio. Statistical analyses were performed with Prism version 5.0 software (GraphPad Software, San Diego, CA). The level of significance was set at P < .05.
Figure 2. Experimental conditions for measuring the elastic modulus of the infraspinatus tendon.
Elastic Modulus of the Tendon The infraspinatus tendon was detached from the scapula and mounted on a universal testing machine (model 3342; Instron, Norwood, MA). As shown in Figure 2, care was taken to maintain the same length as the predetached tendon. For fixation of the tendon, a wooden frame with a length of 100 mm was prepared. Both the distal and proximal ends of the detached tendon specimen were sutured to the frame. For the mechanical testing, a load cell rated to 10 N was used. This load cell was certified to an accuracy of 0.01 N with sensitivity of 0.001 N, and its diameter was 3.0 mm. The tendon strain was measured at a rate of 1 mm/min,
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Results Strain ratio values between the tendon and the acoustic coupler as measured by the 4 approaches (percutaneous, trans-subcutaneous fat, transmuscular, and direct tendon) were successfully obtained (Figure 3). Ultrasound elastography showed a consistent color pattern for each type of tissue. In most experiments, the tendon appeared green and blue, whereas the muscle had a red pattern. Regarding assessment of the validity of the tendon/ reference strain ratio for tissue elasticity, the strain ratio values measured by the direct tendon approach correlated significantly with the tendon compliance (r = 0.73; P < .01; Figure 4). The strain ratio of the tendon was not changed significantly during the sequential removal of overlying soft tissues. The mean tendon/reference strain ratios ± SDs as measured by the 4 approaches (percutaneous, trans-subcutaneous fat, transmuscular, and direct tendon) were 0.54 ± 0.08, 0.50 ± 0.17, 0.47 ± 0.14, and 0.48 ± 0.15, respectively. There were no significant differences among the 4 measurement approaches (P = .4; Figure 5). Overlying soft tissue depths measured from elastographic images by the
percutaneous approach ranged from 15.5 to 21.6 mm. Regarding the comparison between the strain ratio and the overlying soft tissue depth, no significant correlations between these parameters were seen as long as the depth was less than 22 mm (r = –0.05; P = .8; Figure 6).
Discussion The reliability of elastographic measurements has been investigated in several studies.15–19 In particular, for tendon tissues, Drakonaki and Allen15 reported the reliability of the strain ratio in assessing the elasticity of the normal Achilles tendon. They concluded that ultrasound elastography might be a useful measurement technique with enough intraexaminer and interexaminer reproducibility. In our study, the tendon/reference strain ratios in fresh porcine rotator cuff tendons were not affected significantly by different depths of overlying soft tissues, including the skin, subcutaneous fat, and muscles, as well as removal of any soft tissues. On the basis of previous evidence along with that from our study, we believe that elastographic measurement may be a reliable tool for assessing in vivo tendons with a variety of overlying soft tissues if their depth from the skin is less than 22 mm.
Figure 3. Tendon/reference strain ratio measurement by ultrasound elastography by the following 4 measuring approaches: percutaneous approach (A), trans-subcutaneous fat tissue approach (B), transmuscular approach (C), and direct tendon approach (D). H indicates humerus; M, muscle; S, skin; SF, subcutaneous fat; and T, tendon.
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In addition, our study indicated a significant relationship between the strain ratio and the elastic modulus of the tendons. In this study, we adopted an elastomer as a reference for the strain ratio to measure tendon elasticity. It has been reported that peripheral fat tissue could be used as a reference for measurement of Achilles tendon elasticity. However, the subcutaneous fat layer is not always thick enough to place a region of interest for elastographic measurement. Moreover, age and sex differences in the elasticity of fat tissue need to be considered. On the basis of our study, the use of a specially designed acoustic coupler, as in this study, might be recommended for measuring valid tendon strain ratio values, instead of using such an internal reference. Figure 4. Relationship between tendon compliance and the tendon/ reference strain ratio. The strain ratio for the tendon correlated positively with the compliance, which was obtained with strain of 5% to 10% (r = 0.73; P < .01).
For assessment of tendon elasticity with ultrasound elastography, there are two different imaging planes: longitudinal and transverse. According to a recent study comparing these planes for elastography, the measurement in the longitudinal plane is easier to acquire and more reproducible than that in the transverse plane.20 Based on this evidence, all experiments in our study were performed in the longitudinal plane. In the clinical setting, a rotator cuff tendon tear frequently occurs at the anterior third of the supraspinatus tendon, where the elastic modulus is greater than that in the middle third or posterior third.20,21 Recently, a number of risk and protective factors for tendon injuries have been reported to affect tendon elasticity. Burgess et al22 reported a decrease in the elastic modulus of the gastrocnemius tendon after stretching exercises, which are widely believed to prevent tendon injuries. In addition, Eliasson et al23 reported that the elastic modulus increased under conditions of disuse in a rat Achilles tendon model. Moreover, Ichinose et al24 revealed that consecutive exposures to nicotine, which is the primary chemical component of cigarettes, altered the elastic modulus of the supraspinatus tendon in a rat model. More recently, some clinical studies applied ultrasound elastography to tendon tissue for the purpose of investigating its alteration compared with the normal tendon. De Zordo et al25 compared elastographic findings in Achilles tendons between 25 patients with chronic tendinopathy and 25 healthy participants. They found marked or mild softening more frequently in symptomatic tendons than in normal tendons. Although elastography Figure 6. Distribution of percutaneous tendon/reference strain ratios and depths from the skin surface to the level of tendon. No significant correlation between the strain ratios and the depths was seen (r = –0.05; P = .8).
Figure 5. Tendon/reference strain ratios obtained by ultrasound elastography with the 4 measurement approaches: percutaneous approach (SRP), trans-subcutaneous fat tissue approach (SRTF), transmuscular approach (SRTM), and direct tendon approach (SRDT) (P = .4, KruskalWallis test).
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provides useful information concerning material properties of the rotator cuff tendon under in vivo conditions, further studies using both normal and pathologic tendons would be necessary to clarify the true pathogenesis of rotator cuff tears. There were several limitations in this study. First, the data for tendon elasticity were obtained from fresh porcine shoulders. To address the efficacy of elastographic measurement in a clinical setting, differences among species should be taken into consideration. Second, elastographic measurement has technical difficulties, especially for the rotator cuff tendon, due to the existence of adjacent bony structures (eg, acromion and greater tuberosity). As using a freehand technique to assess the elasticity of the rotator cuff tendon reliably is a major limitation, further improvement may be needed. Third, especially in the clinical use of elastography for shoulder joints, we occasionally examine patients with severely thickened subcutaneous fat tissues. In this study, there were no data for overlying soft tissues deeper than approximately 22 mm. Further studies would be necessary to determine the maximum depth for performing elastographic measurements validly. In conclusion, the tendon/reference strain ratio may be feasible for assessing tendon elasticity semiquantitatively. Elastographic measurement may be used with minimal influence by the overlying soft tissues within a 22-mm depth from the skin.
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