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Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study
Journal of Biomechanics xxx (xxxx) xxx
Contents lists available at ScienceDirect
Journal of Biomechanics journal homepage: www.elsevier.com/locate/jbiomech www.JBiomech.com
Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study Naoya Iida a,b, Keigo Taniguchi c,⇑, Kota Watanabe c, Hiroki Miyamoto a, Tatsuya Taniguchi a, Mineko Fujimiya d, Masaki Katayose c a
Graduate School of Health Sciences, Sapporo Medical University, Sapporo, Japan Department of Rehabilitation, Sapporo Medical University Hospital, Sapporo, Japan c Second Division of Physical Therapy, School of Health Sciences, Sapporo Medical University, Sapporo, Japan d Second Division of Anatomy, School of Medicine, Sapporo Medical University, Sapporo, Japan b
a r t i c l e
i n f o
Article history: Accepted 5 November 2019 Available online xxxx Keywords: Elasticity Stiffness Posterior shoulder tightness Stretching
a b s t r a c t Although shear wave elastography (SWE) has been used to indirectly measure passive tension in muscle tissues, it is unknown whether SWE can adequately evaluate passive tension in capsule tissues. This study investigated the relationship between the shear modulus and passive tension in the posterior shoulder capsule using SWE. Ten posterior middle and ten posterior inferior shoulder capsules were dissected from ten fresh-frozen cadavers; humeral head–capsule–glenoid specimens were created from each capsule. The humeral head and glenoid were immobilized with clamps in a custom-built device. Loads (0–400 g, in 25-g increments) were applied to each capsule via a pulley system; elasticity was simultaneously measured using SWE. The elasticity-load relationship of each tested capsule was analyzed by fitting a least-squares regression line to the data. Elasticity change due to creep or hysteresis effects was evaluated by comparing the elastic modulus for a 100-g load during and after the stepwise application of the loads. The observed relationship between the shear modulus and passive capsule tension was highly linear for all twenty tested capsules (p < 0.01). The mean coefficient of determination was 0.882 ± 0.075 and 0.901 ± 0.050 for the posterior middle and posterior inferior capsules, respectively. There was no difference in the shear modulus between the two 100-g load assessments for both the posterior middle (p = 0.205) and posterior inferior capsules (p = 0.161). Thus, SWE is a valid and useful method for indirectly evaluating the change in the passive tension under loading in specific posterior shoulder capsule. Ó 2019 Elsevier Ltd. All rights reserved.
1. Introduction The condition of the joint capsules intimately relates to articular disease. In particular, tightness of the posterior shoulder capsule is a common finding in overhead athletes, such as baseball players, and is considered to induce shoulder pathology (Astolfi et al., 2015; Takenaga et al., 2015; Thomas et al., 2011). Previous biomechanical studies using fresh-frozen cadavers have shown that posterior shoulder capsule tightness induces an abnormal translation of the humeral head during shoulder flexion and external rotation at shoulder abduction (Gates et al., 2012; Harryman et al., 1990; Huffman et al., 2006; Mihata et al., 2015; Muraki ⇑ Corresponding author at: West 17, South 1, Chuo-ku, Sapporo City, Japan.
et al., 2012). Thus, posterior shoulder capsule tightness is a factor of subacromial and internal impingement, and can lead to rotator cuff tears and labrum lesions. The abnormal translation of the humeral head can be explained by the concept of ‘‘obligate translation” (Harryman et al., 1990), in which the capsule excessively tightens and forcibly translates the humeral head to the opposite direction by extending the capsule before the terminal range of motion. Therefore, it is essential to objectively evaluate the degree of biomechanical stress in the capsule during joint motion to better understand clinical conditions and develop effective treatments for the above pathologies. Shear wave elastography (SWE) is an ultrasound-based imaging modality that provides a non-invasive estimate of tissue properties by measuring the speed of the shear wave propagation through soft tissues. Recently, studies utilizing SWE have reported that
E-mail address: [email protected] (K. Taniguchi). https://doi.org/10.1016/j.jbiomech.2019.109498 0021-9290/Ó 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
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the shear modulus is strongly correlated to the passive tension in muscle tissues (Koo et al., 2013; Maisetti et al., 2012). Based on these results, SWE has been recognized as a useful tool for noninvasively estimating passive muscle tension. However, the relationship between the shear modulus and passive tension has not been measured in the capsule, which is intimately related to musculoskeletal disease. Changes in the tissue elasticity when a passive tension is applied may not be similar between the muscle and capsule, as the mechanical characteristics of the capsule differ from that of muscle. In particular, stress-strain relationship is markedly different between the muscle and capsule; the amount of strain caused by the same stress is much higher for the muscle than that for the capsule (Eby et al., 2013; Moore et al., 2005). Therefore, the purpose of the current study was to investigate the relationship between the shear modulus and passive tension for the posterior shoulder capsules using fresh-frozen cadavers. In addition, we also aimed to investigate the test-retest reliability of SWE measurements for the posterior shoulder capsule. 2. Methods The study protocol was reviewed and approved by the Sapporo Medical University Ethical Committee. Ten fresh-frozen glenohumeral joints without osteoarthritis or rotator cuff tears were harvested from fresh-frozen cadavers (mean age at death, 87.0 years; range, 74–93 years). All specimens were thawed at room temperature for approximately 24 h before preparation. After thawing, the specimens were harvested by disarticulating the scapula from the thorax. Subsequently, all remaining soft tissues, except the posterior capsule, were removed. The humerus was cut at the surgical neck, and the glenoid was transected at the base of the scapular neck. Subsequently, the posterior capsule was divided into the superior posterior capsule (Sup-PC), middle posterior capsule (Mid-PC), and inferior posterior capsule (Inf-PC) (Bey et al., 2005). For the right shoulder, the Sup-PC, Mid-PC, and InfPC were defined as the areas corresponding to that between 10 and 11 o’clock, around 9 o’clock, and between 7 and 8 o’clock on a clock face, respectively (Borstad and Dashottar, 2011; Izumi et al., 2008). The glenoid was then cut according to the incisions between the Sup-PC and Mid-PC, and between the Mid-PC and Inf-PC, to create bone-capsule-bone specimens with a width of approximately 10 mm (Bey et al., 2005) (Fig. 1). The Sup-PC was
Fig. 1. Posterior view of posterior capsule specimens of the right shoulder. The posterior capsule was divided into the Sup-PC, the Mid-PC, and Inf-PC. The glenoid was cut according to the incisions between the Sup-PC and Mid-PC, and between the Mid-PC and Inf-PC, to create bone-capsule-bone specimens with a width of approximately 10 mm. Sup-PC: superior posterior capsule; Mid-PC: middle posterior capsule; Inf-PC: inferior posterior capsule.
Fig. 2. Experimental setup. The humeral head and glenoid were fixed. A passive load on the capsule was applied to the glenoid through a pulley system.
not used because Mid-PC and Inf-PC tightness is a characteristic of overhead athletes (Gates et al., 2012; Harryman et al., 1990; Huffman et al., 2006; Mihata et al., 2015; Muraki et al., 2012). We used a custom-built device (Uchida Systems Co., Ltd., Tokyo, Japan), composed of two clamps, a pulley, and a cable, to provide passive loads to the capsule (Fig. 2). The humeral head and glenoid were each immobilized with different clamps. A height-adjustable jack on very smooth tires was attached under the base of the clamp immobilizing the glenoid, rendering the long axis of the capsule horizontal to the floor. The base of the clamp immobilizing the glenoid was connected to a cable, which provided the passive load to the capsule via a pulley. The passive load was increased stepwise from 0 to 400 g in 25-g increments (Koo et al., 2013). SWE with a 5–14 MHz linear ultrasound transducer (Aixplorer Ver. 6. MSK mode; Supersonic Imagine, Aix-en-Provence, France) was used to measure the shear modulus of the capsule. After the specimen was set into the device, an ultrasound diagnostic echo pad (Echo PAD; Yasojima Proceed Co., Ltd., Amagasaki, Japan), with thickness of 5 mm, was placed on the capsule; another echo pad, with a thickness of 30 mm, was set beneath the capsule. The transducer was placed on the capsule along its longitudinal axis. Ultrasound gel was applied between each echo pad and the capsule, and between each echo pad and the transducer. A flexible arm was used to position and hold the transducer to ensure that the same measurement site could be imaged at the same orientation throughout the passive loading experiment. For each load, the shear modulus was measured three times. In accordance with a previous study (Koo et al., 2013), the 1st elastographic image was acquired after approximately 5 s from the application of the passive load in order to stabilize the elastographic window. The 2nd and 3rd elastographic images were then captured 3 and 6 s later, respectively. The load was then at once removed from the glenoid and the next load was applied after a sufficient rest in order to minimize creep or hysteresis effects due to repetitive load applications. Additionally, after finishing the elasticity measurements for all loads in a stepwise manner, the elasticity was again measured for the 100-g load condition in 10 specimens to evaluate the presence of elasticity changes due to creep or hysteresis effects. The elasticity analysis software embedded in the SWE was not sufficient for the purposes of this study, as it did not allow a circular region of interest (ROI) with a diameter of less than 1 mm, and capsules often have a thickness of less than 1 mm. Thus, we exported the elasticity images in JPEG format and analyzed the elasticity using custom analysis software (S-14133 Ver.1.2; Takei Scientific Instrument Co., Ltd., Niigata, Japan). In this software, the ROI can be arbitrary in size and shape and place anywhere
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
N. Iida et al. / Journal of Biomechanics xxx (xxxx) xxx
Fig. 3. Location of the ROI. The superior figure shows the elasticity image and the inferior figure shows the B-mode image. The ROI, which had a width of 3 mm and a height of 0.5 mm, was set at 5 mm lateral to the edge of the labrum. ROI: region of interest.
Table 1 Regression coefficients for all tested capsules. Specimen ID
Age (years)
Mid-PC
Inf-PC
1 2 3 4 5 6 7 8 9 10
79 74 92 90 91 97 79 86 89 93
0.860 0.742 0.873 0.931 0.890 0.948 0.765 0.956 0.932 0.920
0.926 0.921 0.841 0.865 0.963 0.960 0.945 0.883 0.883 0.822
Mean Standard deviation
87.0 7.4
0.882 0.075
0.901 0.050
on the elasticity image, and the elastic modulus calculation is based on the color map scale. In the current study, a rectangular ROI (width, 3 mm; height, 0.5 mm) was set at 5 mm lateral to
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the edge of the labrum (Takenaga et al., 2015) (Fig. 3). The center of the height of the ROI was aligned with the center of the thickness of the capsule. In the SWE software, the Young’s modulus was quantified in kPa based on the shear wave propagation speed, c. For each ROI, Young’s modulus, E, was deduced from E = 3qc2 where q, density, is assumed to be constant (1000 kg/m3) in human soft tissues. This SWE software calculated the Young’s modulus on the supposition that biological tissue is an isotropic material, but the capsule is not (Bey et al., 2005; Moore et al., 2005). Therefore, we determined the shear modulus by dividing the Young’s modulus by 3. For each image in each load condition, the average shear modulus within the rectangular ROI was calculated, and the ensemble mean across the 3 images was regarded as the shear modulus of the tested capsule at that load. Furthermore, the thickness of capsules was measured at 5 mm lateral to the edge of the labrum for load of 0 g and 400 g using analysis software embedded in the SWE. The ensemble mean across the 3 images was regarded as the thickness of the tested capsule at that load. The elasticity-load relationship of each tested capsule was analyzed by fitting a least-squares regression line to the data using statistical software (SPSS Statistics Ver.25.0, J for Windows; IBM, Armonk, USA). Intraclass correlation coefficient (ICC) estimates were calculated based on a mean-rating (k = 3), absoluteagreement, 2-way mixed-effect model to evaluate test–retest reliability of the SWE measurement (Koo et al., 2016). In addition, the coefficient of variation (CV) and the standard error of measurement (SEM) were evaluated. Furthermore, the100-g load assessments during and after the stepwise load applications were compared using a paired t-test. The level of significance was set at p < 0.05. 3. Results The relationship between the shear modulus and passive capsule tension was highly linear for all twenty tested capsules (p < 0.01). The mean (±standard deviation) coefficient of determination (R2) was 0.882 (±0.075; range, 0.742–0.956) and 0.901 (±0.050; range, 0.822–0.963) for the Mid-PC and Inf-PC, respectively. The R2 of all tested capsules and typical examples of the elasticity-load plot and elasticity image are shown in Table 1 and Fig. 4, respectively.
Fig. 4. A typical elasticity–load plot and elasticity image (specimen ID 3; age at death, 91 years; female). In the elasticity image, red indicates that the tissue is stiff and blue indicates that the tissue is soft. Mid-PC: middle posterior capsule; Inf-PC: inferior posterior capsule; ROI: region of interest. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
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The test-retest reliability of SWE measurements was excellent at all loads for both the Mid-PC (mean ICC = 0.998; 95% confidence interval (CI): 0.997–0.998; CV: 3.5 ± 3.3%; SEM: 1.13 kPa) and InfPC (mean ICC = 0.997; CI: 0.996–0.997; CV: 3.4 ± 3.0%; SEM: 1.18 kPa). There was no difference between the shear modulus at a load of 100 g during and after the stepwise load application for both the Mid-PC (p = 0.205) and Inf-PC (p = 0.161).
4. Discussion The present study aimed to investigate the relationship between the shear modulus and passive tension and the testretest reliability of SWE measurements of the posterior shoulder capsule. We hypothesized that the shear modulus would be strongly correlated with passive tension and that the SWE measurement of the posterior shoulder capsule would show high reliability. The present study demonstrated that a strong, positive correlation exists between the shear modulus and passive tension in the Mid-PC and Inf-PC (R2 = 0.882 and 0.901, respectively), indicating that the shear modulus can account for approximately 90% of the passive tension in posterior capsules. Thus, SWE can indirectly evaluate the change in passive tension under loading in specific posterior capsules. Furthermore, the ICCs of the SWE measurements were excellent. Several previous studies on the relationship between the shear modulus and passive muscle tension have demonstrated that the shear modulus reflects the force of stretching in muscle tissues. For example, Maisetti et al. (2012) demonstrated that the elasticity–length relationship is highly correlated (R2 = 0.979) with the force–length curve in the gastrocnemius muscle during passive ankle dorsiflexion. Similarly, Koo et al. (2013) showed that the shear modulus is almost perfectly correlated (R2 = 0.988) with the passive tension in the gastrocnemius and tibialis anterior muscles of fresh chickens. The results of the current study also indicate the validity of SWE for the evaluation of the passive tension in the posterior capsule, even though the R2 was not higher than that for muscle tissues. Although the elasticity of capsule tissues has been evaluated in static conditions (Bey et al., 2005; Itoi et al., 1993), the present study is the first known study to measure the change in elasticity associated with an increase of passive tension in capsule tissues. Takenaga et al. (2015) reported that the posterior shoulder capsule of the dominant side was stiffer than that of the non-dominant side using SWE. Stretching is commonly used as a treatment or prevention method for stiff soft tissues. Based on the results of current study, future studies may identify effective stretching positions that apply the greatest passive tension on the posterior shoulder capsule by evaluating elastic characteristics in various stretching positions using SWE in-vivo. In fact, similar studies have been recently done for muscle tissues (Nishishita et al., 2018; Umegaki et al., 2015; Umehara et al., 2015, 2017). The present study has some limitations. Firstly, the SWE may not directly measure the passive capsule tension itself because the slope of the elasticity-load relationship and the shear modulus at the tension-free state may be different between capsules. SWE can be used to evaluate the change in passive capsule tension under loading because there was a strong positive correlation between the shear modulus and passive tension. Secondly, it is unknown whether reliable measurement of the elasticity of the capsule can be translated into in vivo human subject measurements. Thus, future study should investigate the reliability of SWE measurements for the capsule in vivo. Thirdly, it is unclear whether the ROI set in this study, which was small, reflects elasticity in the entire capsule. The elasticity–load relationship should be
evaluated in large ROIs that reflect the entire capsule in future studies because the elasticity of capsule tissue may be heterogeneous. Fourthly, we only measured the shear modulus of Mid-PC and Inf-PC. It is unclear whether the elasticity–load relationship shown in the current study applies to the Sup-PC. However, the elasticity–load relationship of Mid-PC and Inf-PC showed the same tendency. In addition, previous studies indicated there were no regional differences in the elastic properties of the quadriceps muscle during passive stretching (Freitas et al., 2019). Thus, there might be no difference in the elasticity-load relationship between capsule regions. Future study needs to similarly measure the elasticity of Sup-PC to understand the validity and reliability of SWE measurements. Lastly, the depth in measurement and the tissue form may influence tissue elasticity. However, the depth in measurement can be considered to remain almost unchanged during measurements, as the equal-thickness echo pad was set between the capsule and the transducer. In addition, measurements of the capsule thickness in three randomly selected samples from all specimens showed that the difference in thickness between loads of 0 g and 400 g was small (Mid-PC: 1.8%, <0.1 mm; Inf-PC: 4.4%, <0.1 mm). Therefore, these factors would not greatly influence the current results. In conclusion, our results showed that the shear modulus measured by SWE is highly correlated with the passive tension in posterior shoulder capsules. Based on this result, SWE can be utilized in future studies to identify effective stretching positions for the posterior shoulder capsule and to monitor whether passive tension is applied on the capsule during joint movement by evaluating elastic characteristics in-vivo. Acknowledgment The authors would like to thank all members of the Sports Physical Therapy Laboratory at Sapporo Medical University for providing useful advice. This study was supported by Grant-in-Aid for Early Career Scientist (19K19797) and Grants-in-Aid for Regional R&D Proposal-Based Program from Northern Advancement Center for Science & Technology of Hokkaido, Japan. Conflict of interest statement None of the authors have any conflict of interest to disclose. References Astolfi, M.M., Struminger, A.H., Royer, T.D., Kaminski, T.W., Swanik, C.B., 2015. Adaptations of the shoulder to overhead throwing in youth athletes. J. Athletic Train. 50, 726–732. Bey, M.J., Hunter, S.A., Kilambi, N., Butler, D.L., Lindenfeld, T.N., 2005. Structural and mechanical properties of the glenohumeral joint posterior capsule. J. Shoulder Elbow Surg. 14, 201–206. Borstad, J.D., Dashottar, A., 2011. Quantifying strain on posterior shoulder tissues during 5 simulated clinical tests: a cadaver study. J. Orthop. Sports Phys. Ther. 41, 90–99. Eby, J.D., Song, P., Chen, S., Chen, Q., Greenleaf, J.F., An, K.N., 2013. Validation of shear wave elastography in skeletal muscle. J. Biomech. 46, 2381–2387. Freitas, S.R., Antunes, A., Salmon, P., Mendes, B., Firmino, T., Cruz-Montecinos, C., Cerda, M., Vaz, J.R., 2019. Does epimuscular myofascial force transmission occur between the human quadriceps muscles in vivo during passive stretching?. J. Biomech. 83, 91–96. Gates, J.J., Gupta, A., McGarry, M.H., Tibone, J.E., Lee, T.Q., 2012. The effect of glenohumeral internal rotation deficit due to posterior capsular contracture on passive glenohumeral joint motion. Am. J. Sports Med. 40, 2794–2800. Harryman 2nd, D.T., Sidles, J.A., Clark, J.M., McQuade, K.J., Gibb, T.D., Matsen 3rd, F. A., 1990. Translation of the humeral head on the glenoid with passive glenohumeral motion. J. Bone Joint Surg., Am. 72, 1334–1343. Huffman, G.R., Tibone, J.E., McGarry, M.H., Phipps, B.M., Lee, Y.S., Lee, T.Q., 2006. Path of glenohumeral articulation throughout the rotational range of motion in a thrower’s shoulder model. Am. J. Sports Med. 34, 1662–1669. Itoi, E., Grabowski, J.J., Morrey, B.F., An, K.N., 1993. Capsular properties of the shoulder. Tohoku J. Exp. Med. 171, 203–210.
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
N. Iida et al. / Journal of Biomechanics xxx (xxxx) xxx Izumi, T., Aoki, M., Muraki, T., Hidaka, E., Miyamoto, S., 2008. Stretching positions for the posterior capsule of the glenohumeral joint: strain measurement using cadaver specimens. Am. J. Sports Med. 36, 2014–2022. Koo, T.K., Li, M.Y., 2016. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J. Chiropractic Med. 15, 155–163. Koo, T.K., Guo, J.Y., Cohen, J.H., Parker, K.J., 2013. Relationship between shear elastic modulus and passive muscle force: an ex-vivo study. J. Biomech. 46, 2053– 2059. Maisetti, O., Hug, F., Bouillard, K., Nordez, A., 2012. Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging. J. Biomech. 45, 978–984. Mihata, T., Gates, J., McGarry, M.H., Neo, M., Lee, T.Q., 2015. Effect of posterior shoulder tightness on internal impingement in a cadaveric model of throwing. Knee Surg. Sports Traumatol. Arthrosc. 23, 548–554. Moore, S.M., McMahon, P.J., Azemi, E., Debski, R.E., 2005. Bi-directional mechanical properties of the posterior region of the glenohumeral capsule. J. Biomech. 38, 1365–1369. Muraki, T., Yamamoto, N., Zhao, K.D., Sperling, J.W., Steinmann, S.P., Cofield, R.H., An, K.N., 2012. Effects of posterior capsule tightness on subacromial contact behavior during shoulder motions. J. Shoulder Elbow Surg. 21, 1160–1167. Nishishita, S., Hasegawa, S., Nakamura, M., Umegaki, H., Kobayashi, T., Ichihashi, N., 2018. Effective stretching position for the supraspinatus muscle evaluated by shear wave elastography in vivo. J. Shoulder Elbow Surg. 27, 2242–2248.
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Takenaga, T., Sugimoto, K., Goto, H., Nozaki, M., Fukuyoshi, M., Tsuchiya, A., Murase, A., Ono, T., Otsuka, T., 2015. Posterior shoulder capsules are thicker and stiffer in the throwing shoulders of healthy college baseball players: a quantitative assessment using shear-wave ultrasound elastography. Am. J. Sports Med. 43, 2935–2942. Thomas, S.J., Swanik, C.B., Higginson, J.S., Kaminski, T.W., Swanik, K.A., Bartolozzi, A. R., Abboud, J.A., Nazarian, L.N., 2011. A bilateral comparison of posterior capsule thickness and its correlation with glenohumeral range of motion and scapular upward rotation in collegiate baseball players. J. Shoulder Elbow Surg. 20, 708– 716. Umegaki, H., Ikezoe, T., Nakamura, M., Nishishita, S., Kobayashi, T., Fujita, K., Tanaka, H., Ichihashi, N., 2015. The effect of hip rotation on shear elastic modulus of the medial and lateral hamstrings during stretching. Manual Therapy 20, 134–137. Umehara, J., Nakamura, M., Fujita, K., Kusano, K., Nishishita, S., Araki, K., Tanaka, H., Yanase, K., Ichihashi, N., 2017. Shoulder horizontal abduction stretching effectively increases shear elastic modulus of pectoralis minor muscle. J. Shoulder Elbow Surg. 26, 1159–1165. Umehara, J., Ikezoe, T., Nishishita, S., Nakamura, M., Umegaki, H., Kobayashi, T., Fujita, K., Ichihashi, N., 2015. Effect of hip and knee position on tensor fasciae latae elongation during stretching: an ultrasonic shear wave elastography study. Clin. Biomech. (Bristol, Avon) 30, 1056–1059.
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
Contents lists available at ScienceDirect
Journal of Biomechanics journal homepage: www.elsevier.com/locate/jbiomech www.JBiomech.com
Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study Naoya Iida a,b, Keigo Taniguchi c,⇑, Kota Watanabe c, Hiroki Miyamoto a, Tatsuya Taniguchi a, Mineko Fujimiya d, Masaki Katayose c a
Graduate School of Health Sciences, Sapporo Medical University, Sapporo, Japan Department of Rehabilitation, Sapporo Medical University Hospital, Sapporo, Japan c Second Division of Physical Therapy, School of Health Sciences, Sapporo Medical University, Sapporo, Japan d Second Division of Anatomy, School of Medicine, Sapporo Medical University, Sapporo, Japan b
a r t i c l e
i n f o
Article history: Accepted 5 November 2019 Available online xxxx Keywords: Elasticity Stiffness Posterior shoulder tightness Stretching
a b s t r a c t Although shear wave elastography (SWE) has been used to indirectly measure passive tension in muscle tissues, it is unknown whether SWE can adequately evaluate passive tension in capsule tissues. This study investigated the relationship between the shear modulus and passive tension in the posterior shoulder capsule using SWE. Ten posterior middle and ten posterior inferior shoulder capsules were dissected from ten fresh-frozen cadavers; humeral head–capsule–glenoid specimens were created from each capsule. The humeral head and glenoid were immobilized with clamps in a custom-built device. Loads (0–400 g, in 25-g increments) were applied to each capsule via a pulley system; elasticity was simultaneously measured using SWE. The elasticity-load relationship of each tested capsule was analyzed by fitting a least-squares regression line to the data. Elasticity change due to creep or hysteresis effects was evaluated by comparing the elastic modulus for a 100-g load during and after the stepwise application of the loads. The observed relationship between the shear modulus and passive capsule tension was highly linear for all twenty tested capsules (p < 0.01). The mean coefficient of determination was 0.882 ± 0.075 and 0.901 ± 0.050 for the posterior middle and posterior inferior capsules, respectively. There was no difference in the shear modulus between the two 100-g load assessments for both the posterior middle (p = 0.205) and posterior inferior capsules (p = 0.161). Thus, SWE is a valid and useful method for indirectly evaluating the change in the passive tension under loading in specific posterior shoulder capsule. Ó 2019 Elsevier Ltd. All rights reserved.
1. Introduction The condition of the joint capsules intimately relates to articular disease. In particular, tightness of the posterior shoulder capsule is a common finding in overhead athletes, such as baseball players, and is considered to induce shoulder pathology (Astolfi et al., 2015; Takenaga et al., 2015; Thomas et al., 2011). Previous biomechanical studies using fresh-frozen cadavers have shown that posterior shoulder capsule tightness induces an abnormal translation of the humeral head during shoulder flexion and external rotation at shoulder abduction (Gates et al., 2012; Harryman et al., 1990; Huffman et al., 2006; Mihata et al., 2015; Muraki ⇑ Corresponding author at: West 17, South 1, Chuo-ku, Sapporo City, Japan.
et al., 2012). Thus, posterior shoulder capsule tightness is a factor of subacromial and internal impingement, and can lead to rotator cuff tears and labrum lesions. The abnormal translation of the humeral head can be explained by the concept of ‘‘obligate translation” (Harryman et al., 1990), in which the capsule excessively tightens and forcibly translates the humeral head to the opposite direction by extending the capsule before the terminal range of motion. Therefore, it is essential to objectively evaluate the degree of biomechanical stress in the capsule during joint motion to better understand clinical conditions and develop effective treatments for the above pathologies. Shear wave elastography (SWE) is an ultrasound-based imaging modality that provides a non-invasive estimate of tissue properties by measuring the speed of the shear wave propagation through soft tissues. Recently, studies utilizing SWE have reported that
E-mail address: [email protected] (K. Taniguchi). https://doi.org/10.1016/j.jbiomech.2019.109498 0021-9290/Ó 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
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the shear modulus is strongly correlated to the passive tension in muscle tissues (Koo et al., 2013; Maisetti et al., 2012). Based on these results, SWE has been recognized as a useful tool for noninvasively estimating passive muscle tension. However, the relationship between the shear modulus and passive tension has not been measured in the capsule, which is intimately related to musculoskeletal disease. Changes in the tissue elasticity when a passive tension is applied may not be similar between the muscle and capsule, as the mechanical characteristics of the capsule differ from that of muscle. In particular, stress-strain relationship is markedly different between the muscle and capsule; the amount of strain caused by the same stress is much higher for the muscle than that for the capsule (Eby et al., 2013; Moore et al., 2005). Therefore, the purpose of the current study was to investigate the relationship between the shear modulus and passive tension for the posterior shoulder capsules using fresh-frozen cadavers. In addition, we also aimed to investigate the test-retest reliability of SWE measurements for the posterior shoulder capsule. 2. Methods The study protocol was reviewed and approved by the Sapporo Medical University Ethical Committee. Ten fresh-frozen glenohumeral joints without osteoarthritis or rotator cuff tears were harvested from fresh-frozen cadavers (mean age at death, 87.0 years; range, 74–93 years). All specimens were thawed at room temperature for approximately 24 h before preparation. After thawing, the specimens were harvested by disarticulating the scapula from the thorax. Subsequently, all remaining soft tissues, except the posterior capsule, were removed. The humerus was cut at the surgical neck, and the glenoid was transected at the base of the scapular neck. Subsequently, the posterior capsule was divided into the superior posterior capsule (Sup-PC), middle posterior capsule (Mid-PC), and inferior posterior capsule (Inf-PC) (Bey et al., 2005). For the right shoulder, the Sup-PC, Mid-PC, and InfPC were defined as the areas corresponding to that between 10 and 11 o’clock, around 9 o’clock, and between 7 and 8 o’clock on a clock face, respectively (Borstad and Dashottar, 2011; Izumi et al., 2008). The glenoid was then cut according to the incisions between the Sup-PC and Mid-PC, and between the Mid-PC and Inf-PC, to create bone-capsule-bone specimens with a width of approximately 10 mm (Bey et al., 2005) (Fig. 1). The Sup-PC was
Fig. 1. Posterior view of posterior capsule specimens of the right shoulder. The posterior capsule was divided into the Sup-PC, the Mid-PC, and Inf-PC. The glenoid was cut according to the incisions between the Sup-PC and Mid-PC, and between the Mid-PC and Inf-PC, to create bone-capsule-bone specimens with a width of approximately 10 mm. Sup-PC: superior posterior capsule; Mid-PC: middle posterior capsule; Inf-PC: inferior posterior capsule.
Fig. 2. Experimental setup. The humeral head and glenoid were fixed. A passive load on the capsule was applied to the glenoid through a pulley system.
not used because Mid-PC and Inf-PC tightness is a characteristic of overhead athletes (Gates et al., 2012; Harryman et al., 1990; Huffman et al., 2006; Mihata et al., 2015; Muraki et al., 2012). We used a custom-built device (Uchida Systems Co., Ltd., Tokyo, Japan), composed of two clamps, a pulley, and a cable, to provide passive loads to the capsule (Fig. 2). The humeral head and glenoid were each immobilized with different clamps. A height-adjustable jack on very smooth tires was attached under the base of the clamp immobilizing the glenoid, rendering the long axis of the capsule horizontal to the floor. The base of the clamp immobilizing the glenoid was connected to a cable, which provided the passive load to the capsule via a pulley. The passive load was increased stepwise from 0 to 400 g in 25-g increments (Koo et al., 2013). SWE with a 5–14 MHz linear ultrasound transducer (Aixplorer Ver. 6. MSK mode; Supersonic Imagine, Aix-en-Provence, France) was used to measure the shear modulus of the capsule. After the specimen was set into the device, an ultrasound diagnostic echo pad (Echo PAD; Yasojima Proceed Co., Ltd., Amagasaki, Japan), with thickness of 5 mm, was placed on the capsule; another echo pad, with a thickness of 30 mm, was set beneath the capsule. The transducer was placed on the capsule along its longitudinal axis. Ultrasound gel was applied between each echo pad and the capsule, and between each echo pad and the transducer. A flexible arm was used to position and hold the transducer to ensure that the same measurement site could be imaged at the same orientation throughout the passive loading experiment. For each load, the shear modulus was measured three times. In accordance with a previous study (Koo et al., 2013), the 1st elastographic image was acquired after approximately 5 s from the application of the passive load in order to stabilize the elastographic window. The 2nd and 3rd elastographic images were then captured 3 and 6 s later, respectively. The load was then at once removed from the glenoid and the next load was applied after a sufficient rest in order to minimize creep or hysteresis effects due to repetitive load applications. Additionally, after finishing the elasticity measurements for all loads in a stepwise manner, the elasticity was again measured for the 100-g load condition in 10 specimens to evaluate the presence of elasticity changes due to creep or hysteresis effects. The elasticity analysis software embedded in the SWE was not sufficient for the purposes of this study, as it did not allow a circular region of interest (ROI) with a diameter of less than 1 mm, and capsules often have a thickness of less than 1 mm. Thus, we exported the elasticity images in JPEG format and analyzed the elasticity using custom analysis software (S-14133 Ver.1.2; Takei Scientific Instrument Co., Ltd., Niigata, Japan). In this software, the ROI can be arbitrary in size and shape and place anywhere
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
N. Iida et al. / Journal of Biomechanics xxx (xxxx) xxx
Fig. 3. Location of the ROI. The superior figure shows the elasticity image and the inferior figure shows the B-mode image. The ROI, which had a width of 3 mm and a height of 0.5 mm, was set at 5 mm lateral to the edge of the labrum. ROI: region of interest.
Table 1 Regression coefficients for all tested capsules. Specimen ID
Age (years)
Mid-PC
Inf-PC
1 2 3 4 5 6 7 8 9 10
79 74 92 90 91 97 79 86 89 93
0.860 0.742 0.873 0.931 0.890 0.948 0.765 0.956 0.932 0.920
0.926 0.921 0.841 0.865 0.963 0.960 0.945 0.883 0.883 0.822
Mean Standard deviation
87.0 7.4
0.882 0.075
0.901 0.050
on the elasticity image, and the elastic modulus calculation is based on the color map scale. In the current study, a rectangular ROI (width, 3 mm; height, 0.5 mm) was set at 5 mm lateral to
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the edge of the labrum (Takenaga et al., 2015) (Fig. 3). The center of the height of the ROI was aligned with the center of the thickness of the capsule. In the SWE software, the Young’s modulus was quantified in kPa based on the shear wave propagation speed, c. For each ROI, Young’s modulus, E, was deduced from E = 3qc2 where q, density, is assumed to be constant (1000 kg/m3) in human soft tissues. This SWE software calculated the Young’s modulus on the supposition that biological tissue is an isotropic material, but the capsule is not (Bey et al., 2005; Moore et al., 2005). Therefore, we determined the shear modulus by dividing the Young’s modulus by 3. For each image in each load condition, the average shear modulus within the rectangular ROI was calculated, and the ensemble mean across the 3 images was regarded as the shear modulus of the tested capsule at that load. Furthermore, the thickness of capsules was measured at 5 mm lateral to the edge of the labrum for load of 0 g and 400 g using analysis software embedded in the SWE. The ensemble mean across the 3 images was regarded as the thickness of the tested capsule at that load. The elasticity-load relationship of each tested capsule was analyzed by fitting a least-squares regression line to the data using statistical software (SPSS Statistics Ver.25.0, J for Windows; IBM, Armonk, USA). Intraclass correlation coefficient (ICC) estimates were calculated based on a mean-rating (k = 3), absoluteagreement, 2-way mixed-effect model to evaluate test–retest reliability of the SWE measurement (Koo et al., 2016). In addition, the coefficient of variation (CV) and the standard error of measurement (SEM) were evaluated. Furthermore, the100-g load assessments during and after the stepwise load applications were compared using a paired t-test. The level of significance was set at p < 0.05. 3. Results The relationship between the shear modulus and passive capsule tension was highly linear for all twenty tested capsules (p < 0.01). The mean (±standard deviation) coefficient of determination (R2) was 0.882 (±0.075; range, 0.742–0.956) and 0.901 (±0.050; range, 0.822–0.963) for the Mid-PC and Inf-PC, respectively. The R2 of all tested capsules and typical examples of the elasticity-load plot and elasticity image are shown in Table 1 and Fig. 4, respectively.
Fig. 4. A typical elasticity–load plot and elasticity image (specimen ID 3; age at death, 91 years; female). In the elasticity image, red indicates that the tissue is stiff and blue indicates that the tissue is soft. Mid-PC: middle posterior capsule; Inf-PC: inferior posterior capsule; ROI: region of interest. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
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N. Iida et al. / Journal of Biomechanics xxx (xxxx) xxx
The test-retest reliability of SWE measurements was excellent at all loads for both the Mid-PC (mean ICC = 0.998; 95% confidence interval (CI): 0.997–0.998; CV: 3.5 ± 3.3%; SEM: 1.13 kPa) and InfPC (mean ICC = 0.997; CI: 0.996–0.997; CV: 3.4 ± 3.0%; SEM: 1.18 kPa). There was no difference between the shear modulus at a load of 100 g during and after the stepwise load application for both the Mid-PC (p = 0.205) and Inf-PC (p = 0.161).
4. Discussion The present study aimed to investigate the relationship between the shear modulus and passive tension and the testretest reliability of SWE measurements of the posterior shoulder capsule. We hypothesized that the shear modulus would be strongly correlated with passive tension and that the SWE measurement of the posterior shoulder capsule would show high reliability. The present study demonstrated that a strong, positive correlation exists between the shear modulus and passive tension in the Mid-PC and Inf-PC (R2 = 0.882 and 0.901, respectively), indicating that the shear modulus can account for approximately 90% of the passive tension in posterior capsules. Thus, SWE can indirectly evaluate the change in passive tension under loading in specific posterior capsules. Furthermore, the ICCs of the SWE measurements were excellent. Several previous studies on the relationship between the shear modulus and passive muscle tension have demonstrated that the shear modulus reflects the force of stretching in muscle tissues. For example, Maisetti et al. (2012) demonstrated that the elasticity–length relationship is highly correlated (R2 = 0.979) with the force–length curve in the gastrocnemius muscle during passive ankle dorsiflexion. Similarly, Koo et al. (2013) showed that the shear modulus is almost perfectly correlated (R2 = 0.988) with the passive tension in the gastrocnemius and tibialis anterior muscles of fresh chickens. The results of the current study also indicate the validity of SWE for the evaluation of the passive tension in the posterior capsule, even though the R2 was not higher than that for muscle tissues. Although the elasticity of capsule tissues has been evaluated in static conditions (Bey et al., 2005; Itoi et al., 1993), the present study is the first known study to measure the change in elasticity associated with an increase of passive tension in capsule tissues. Takenaga et al. (2015) reported that the posterior shoulder capsule of the dominant side was stiffer than that of the non-dominant side using SWE. Stretching is commonly used as a treatment or prevention method for stiff soft tissues. Based on the results of current study, future studies may identify effective stretching positions that apply the greatest passive tension on the posterior shoulder capsule by evaluating elastic characteristics in various stretching positions using SWE in-vivo. In fact, similar studies have been recently done for muscle tissues (Nishishita et al., 2018; Umegaki et al., 2015; Umehara et al., 2015, 2017). The present study has some limitations. Firstly, the SWE may not directly measure the passive capsule tension itself because the slope of the elasticity-load relationship and the shear modulus at the tension-free state may be different between capsules. SWE can be used to evaluate the change in passive capsule tension under loading because there was a strong positive correlation between the shear modulus and passive tension. Secondly, it is unknown whether reliable measurement of the elasticity of the capsule can be translated into in vivo human subject measurements. Thus, future study should investigate the reliability of SWE measurements for the capsule in vivo. Thirdly, it is unclear whether the ROI set in this study, which was small, reflects elasticity in the entire capsule. The elasticity–load relationship should be
evaluated in large ROIs that reflect the entire capsule in future studies because the elasticity of capsule tissue may be heterogeneous. Fourthly, we only measured the shear modulus of Mid-PC and Inf-PC. It is unclear whether the elasticity–load relationship shown in the current study applies to the Sup-PC. However, the elasticity–load relationship of Mid-PC and Inf-PC showed the same tendency. In addition, previous studies indicated there were no regional differences in the elastic properties of the quadriceps muscle during passive stretching (Freitas et al., 2019). Thus, there might be no difference in the elasticity-load relationship between capsule regions. Future study needs to similarly measure the elasticity of Sup-PC to understand the validity and reliability of SWE measurements. Lastly, the depth in measurement and the tissue form may influence tissue elasticity. However, the depth in measurement can be considered to remain almost unchanged during measurements, as the equal-thickness echo pad was set between the capsule and the transducer. In addition, measurements of the capsule thickness in three randomly selected samples from all specimens showed that the difference in thickness between loads of 0 g and 400 g was small (Mid-PC: 1.8%, <0.1 mm; Inf-PC: 4.4%, <0.1 mm). Therefore, these factors would not greatly influence the current results. In conclusion, our results showed that the shear modulus measured by SWE is highly correlated with the passive tension in posterior shoulder capsules. Based on this result, SWE can be utilized in future studies to identify effective stretching positions for the posterior shoulder capsule and to monitor whether passive tension is applied on the capsule during joint movement by evaluating elastic characteristics in-vivo. Acknowledgment The authors would like to thank all members of the Sports Physical Therapy Laboratory at Sapporo Medical University for providing useful advice. This study was supported by Grant-in-Aid for Early Career Scientist (19K19797) and Grants-in-Aid for Regional R&D Proposal-Based Program from Northern Advancement Center for Science & Technology of Hokkaido, Japan. Conflict of interest statement None of the authors have any conflict of interest to disclose. References Astolfi, M.M., Struminger, A.H., Royer, T.D., Kaminski, T.W., Swanik, C.B., 2015. Adaptations of the shoulder to overhead throwing in youth athletes. J. Athletic Train. 50, 726–732. Bey, M.J., Hunter, S.A., Kilambi, N., Butler, D.L., Lindenfeld, T.N., 2005. Structural and mechanical properties of the glenohumeral joint posterior capsule. J. Shoulder Elbow Surg. 14, 201–206. Borstad, J.D., Dashottar, A., 2011. Quantifying strain on posterior shoulder tissues during 5 simulated clinical tests: a cadaver study. J. Orthop. Sports Phys. Ther. 41, 90–99. Eby, J.D., Song, P., Chen, S., Chen, Q., Greenleaf, J.F., An, K.N., 2013. Validation of shear wave elastography in skeletal muscle. J. Biomech. 46, 2381–2387. Freitas, S.R., Antunes, A., Salmon, P., Mendes, B., Firmino, T., Cruz-Montecinos, C., Cerda, M., Vaz, J.R., 2019. Does epimuscular myofascial force transmission occur between the human quadriceps muscles in vivo during passive stretching?. J. Biomech. 83, 91–96. Gates, J.J., Gupta, A., McGarry, M.H., Tibone, J.E., Lee, T.Q., 2012. The effect of glenohumeral internal rotation deficit due to posterior capsular contracture on passive glenohumeral joint motion. Am. J. Sports Med. 40, 2794–2800. Harryman 2nd, D.T., Sidles, J.A., Clark, J.M., McQuade, K.J., Gibb, T.D., Matsen 3rd, F. A., 1990. Translation of the humeral head on the glenoid with passive glenohumeral motion. J. Bone Joint Surg., Am. 72, 1334–1343. Huffman, G.R., Tibone, J.E., McGarry, M.H., Phipps, B.M., Lee, Y.S., Lee, T.Q., 2006. Path of glenohumeral articulation throughout the rotational range of motion in a thrower’s shoulder model. Am. J. Sports Med. 34, 1662–1669. Itoi, E., Grabowski, J.J., Morrey, B.F., An, K.N., 1993. Capsular properties of the shoulder. Tohoku J. Exp. Med. 171, 203–210.
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498
N. Iida et al. / Journal of Biomechanics xxx (xxxx) xxx Izumi, T., Aoki, M., Muraki, T., Hidaka, E., Miyamoto, S., 2008. Stretching positions for the posterior capsule of the glenohumeral joint: strain measurement using cadaver specimens. Am. J. Sports Med. 36, 2014–2022. Koo, T.K., Li, M.Y., 2016. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J. Chiropractic Med. 15, 155–163. Koo, T.K., Guo, J.Y., Cohen, J.H., Parker, K.J., 2013. Relationship between shear elastic modulus and passive muscle force: an ex-vivo study. J. Biomech. 46, 2053– 2059. Maisetti, O., Hug, F., Bouillard, K., Nordez, A., 2012. Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging. J. Biomech. 45, 978–984. Mihata, T., Gates, J., McGarry, M.H., Neo, M., Lee, T.Q., 2015. Effect of posterior shoulder tightness on internal impingement in a cadaveric model of throwing. Knee Surg. Sports Traumatol. Arthrosc. 23, 548–554. Moore, S.M., McMahon, P.J., Azemi, E., Debski, R.E., 2005. Bi-directional mechanical properties of the posterior region of the glenohumeral capsule. J. Biomech. 38, 1365–1369. Muraki, T., Yamamoto, N., Zhao, K.D., Sperling, J.W., Steinmann, S.P., Cofield, R.H., An, K.N., 2012. Effects of posterior capsule tightness on subacromial contact behavior during shoulder motions. J. Shoulder Elbow Surg. 21, 1160–1167. Nishishita, S., Hasegawa, S., Nakamura, M., Umegaki, H., Kobayashi, T., Ichihashi, N., 2018. Effective stretching position for the supraspinatus muscle evaluated by shear wave elastography in vivo. J. Shoulder Elbow Surg. 27, 2242–2248.
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Takenaga, T., Sugimoto, K., Goto, H., Nozaki, M., Fukuyoshi, M., Tsuchiya, A., Murase, A., Ono, T., Otsuka, T., 2015. Posterior shoulder capsules are thicker and stiffer in the throwing shoulders of healthy college baseball players: a quantitative assessment using shear-wave ultrasound elastography. Am. J. Sports Med. 43, 2935–2942. Thomas, S.J., Swanik, C.B., Higginson, J.S., Kaminski, T.W., Swanik, K.A., Bartolozzi, A. R., Abboud, J.A., Nazarian, L.N., 2011. A bilateral comparison of posterior capsule thickness and its correlation with glenohumeral range of motion and scapular upward rotation in collegiate baseball players. J. Shoulder Elbow Surg. 20, 708– 716. Umegaki, H., Ikezoe, T., Nakamura, M., Nishishita, S., Kobayashi, T., Fujita, K., Tanaka, H., Ichihashi, N., 2015. The effect of hip rotation on shear elastic modulus of the medial and lateral hamstrings during stretching. Manual Therapy 20, 134–137. Umehara, J., Nakamura, M., Fujita, K., Kusano, K., Nishishita, S., Araki, K., Tanaka, H., Yanase, K., Ichihashi, N., 2017. Shoulder horizontal abduction stretching effectively increases shear elastic modulus of pectoralis minor muscle. J. Shoulder Elbow Surg. 26, 1159–1165. Umehara, J., Ikezoe, T., Nishishita, S., Nakamura, M., Umegaki, H., Kobayashi, T., Fujita, K., Ichihashi, N., 2015. Effect of hip and knee position on tensor fasciae latae elongation during stretching: an ultrasonic shear wave elastography study. Clin. Biomech. (Bristol, Avon) 30, 1056–1059.
Please cite this article as: N. Iida, K. Taniguchi, K. Watanabe et al., Relationship between shear modulus and passive tension of the posterior shoulder capsule using ultrasound shear wave elastography: A cadaveric study, Journal of Biomechanics, https://doi.org/10.1016/j.jbiomech.2019.109498