The Open Orthopaedics Journal




ISSN: 1874-3250 ― Volume 12, 2018
RESEARCH ARTICLE

Elastic Changes of the Coracohumeral Ligament Evaluated with Shear Wave Elastography



Kenji Kanazawa1, Yoshihiro Hagiwara2, *, Takuya Sekiguchi3, Ryo Fujita3, Kazuaki Suzuki4, Masashi Koide5, Akira Ando5, Yutaka Yabe2
1 Department of Orthopaedic Surgery, South Miyagi Medical Center, Ogawara, Miyagi, Japan
2 Department of Orthopaedic Surgery, Tohoku University School of Medicine, Sendai, Miyagi, Japan
3 Department of Orthopaedic Surgery, Iwate Prefectural Central Hospital, Morioka, Iwate, Japan
4 Department of Orthopaedic Surgery, JR Sendai Hospital, Sendai, Miyagi, Japan
5 Department of Orthopaedic Surgery, Matsuda Hospital, Sendai, Miyagi, Japan

Abstract

Background:

Although the shoulder range of motion significantly decreases with advancing age, how the natural aging process affects the joint capsule, including the Coracohumeral Ligament (CHL), in healthy subjects is still unknown.

Objective

To use shear wave elastography to investigate the correlations between age, sex, and shoulder dominance, and elasticity of the CHL in healthy individuals.

Methods:

Eighty-four healthy volunteers (mean age: 42.6; 39 men) were included in this study. They were divided into five groups based on age: 20s (20–29, n = 19), 30s (30–39, n = 17), 40s (40–49, n = 20), 50s (50–59, n = 13), and 60s (60–69, n = 15) groups. The elasticity of the CHL in the bilateral shoulders was evaluated at the neutral and 30° external rotation (ER at 30°) positions with the arm at the side while laying supine.

Results:

The elastic modulus was significantly greater in ER at 30° than in the neutral position regardless of sex or shoulder dominance (P < 0.001). Significant positive correlations between age and elasticity of the CHL were observed in both the neutral and ER at 30° positions regardless of shoulder dominance. Elasticity of the CHL was significantly greater with increasing age in both the neutral and ER at 30° positions on the dominant (P = 0.0022, P < 0.001, respectively) and non-dominant sides (P = 0.0199, 0.0014).

Conclusion:

The elasticity of the CHL increased with age, and the ER at 30° position could demonstrate faint changes in CHL elasticity.

Level of Evidence:

Level 3 Case-control study.

Keywords: Shoulder dominance, Range of motion, Coracohumeral ligament, Shear wave elastography, Ligament elasticity, Frozen shoulder.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 12
First Page: 427
Last Page: 434
Publisher Id: TOORTHJ-12-427
DOI: 10.2174/1874325001812010427

Article History:

Received Date: 8/6/2018
Revision Received Date: 11/9/2018
Acceptance Date: 24/9/2018
Electronic publication date: 30/10/2018
Collection year: 2018

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© 2018 Kanazawa et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Orthopaedic Surgery, Tohoku University School of Medicine,, 1-1 Seiryo-machi, Aoba-ku, Sendai, 980-8574, Japan, Tel: +81-22-717-7245, Fax: +81-22-717-7248, E-mail: hagi@med.tohoku.ac.jp




1. INTRODUCTION

Measurement of Range of Motion (ROM) is an important method of evaluating shoulder impairment, making a diagnosis, and planning effective treatments. Frozen shoulder is a common shoulder condition characterized by severe pain and global restrictions in ROM. Its etiology remains unclear, but the primary pathologies are assumed to affect the joint capsule including the Rotator Interval (RI) and the Coracohumeral Ligament (CHL) [1Hand GC, Athanasou NA, Matthews T, Carr AJ. The pathology of frozen shoulder. J Bone Joint Surg Br 2007; 89(7): 928-32.[http://dx.doi.org/10.1302/0301-620X.89B7.19097] [PMID: 17673588] -3Ozaki J, Nakagawa Y, Sakurai G, Tamai S. Recalcitrant chronic adhesive capsulitis of the shoulder. Role of contracture of the coracohumeral ligament and rotator interval in pathogenesis and treatment. J Bone Joint Surg Am 1989; 71(10): 1511-5.[http://dx.doi.org/10.2106/00004623-198971100-00009] [PMID: 2592391] ]. Although shoulder ROM significantly decreases with advancing age [4Boone DC, Azen SP. Normal range of motion of joints in male subjects. J Bone Joint Surg Am 1979; 61(5): 756-9.[http://dx.doi.org/10.2106/00004623-197961050-00017] [PMID: 457719] , 5Barnes CJ, Van Steyn SJ, Fischer RA. The effects of age, sex, and shoulder dominance on range of motion of the shoulder. J Shoulder Elbow Surg 2001; 10(3): 242-6.[http://dx.doi.org/10.1067/mse.2001.115270] [PMID: 11408905] ], how the natural aging process affects the joint capsule, including the CHL, in healthy subjects is still unknown.

The CHL runs between the lateral base of the coracoid process and the greater and lesser tuberosities of the humerus. It covers the RI, and the supraspinatus (SSP) and subscapularis (SSc) tendons, anchoring itself to the coracoid process, which functions as the supporting structure for both the SSP and SSc tendons [6Arai R, Nimura A, Yamaguchi K, et al. The anatomy of the coracohumeral ligament and its relation to the subscapularis muscle. J Shoulder Elbow Surg 2014; 23(10): 1575-81.[http://dx.doi.org/10.1016/j.jse.2014.02.009] [PMID: 24766789] -8Edelson JG, Taitz C, Grishkan A. The coracohumeral ligament. Anatomy of a substantial but neglected structure. J Bone Joint Surg Br 1991; 73(1): 150-3.[http://dx.doi.org/10.1302/0301-620X.73B1.1991752] [PMID: 1991752] ]. The thickness of the CHL is significantly related to ROM restriction in External Rotation (ER) [3Ozaki J, Nakagawa Y, Sakurai G, Tamai S. Recalcitrant chronic adhesive capsulitis of the shoulder. Role of contracture of the coracohumeral ligament and rotator interval in pathogenesis and treatment. J Bone Joint Surg Am 1989; 71(10): 1511-5.[http://dx.doi.org/10.2106/00004623-198971100-00009] [PMID: 2592391] , 9Neer CS II, Satterlee CC, Dalsey RM, Flatow EL. The anatomy and potential effects of contracture of the coracohumeral ligament. Clin Orthop Relat Res 1992; (280): 182-5.[PMID: 1611740] ] as well as Internal Rotation (IR) [10Kanazawa K, Hagiwara Y, Kawai N, et al. Correlations of coracohumeral ligament and range of motion restriction in patients with recurrent anterior glenohumeral instability evaluated by magnetic resonance arthrography. J Shoulder Elbow Surg 2017; 26(2): 233-40.[http://dx.doi.org/10.1016/j.jse.2016.09.016] [PMID: 27814944] , 11Lee SY, Park J, Song SW. Correlation of MR arthrographic findings and range of shoulder motions in patients with frozen shoulder. AJR Am J Roentgenol 2012; 198(1): 173-9.[http://dx.doi.org/10.2214/AJR.10.6173] [PMID: 22194494] ]. Even in patients with recurrent anterior glenohumeral instability, these changes are confirmed to be a part of the natural aging process [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. Thickening of the CHL influences multidirectional ROM restrictions and could be an indicator of certain shoulder diseases.

Ultrasound and magnetic resonance imaging have been used to evaluate and diagnose various shoulder impairments, such as rotator cuff tears [13Roy JS, Braën C, Leblond J, et al. Diagnostic accuracy of ultrasonography, MRI and MR arthrography in the characterisation of rotator cuff disorders: a systematic review and meta-analysis. Br J Sports Med 2015; 49(20): 1316-28.[http://dx.doi.org/10.1136/bjsports-2014-094148] [PMID: 25677796] ]. However, alterations in the material properties of muscles and tendons cannot be assessed properly using those radiographic modalities. Recently, Shear Wave Elastography (SWE) was developed as a new, non-invasive, ultrasound imaging technique that provides both qualitative and quantitative information. It uses a focused ultrasonic pulse to evaluate real-time elasticity of the soft tissues based on viscoelastic properties [14Bercoff J, Tanter M, Fink M. Supersonic shear imaging: A new technique for soft tissue elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 2004; 51(4): 396-409.[http://dx.doi.org/10.1109/TUFFC.2004.1295425] [PMID: 15139541] ]. The system propagates generated shear waves into the tissues and assesses their elastic modulus [15Shiina T, Nightingale KR, Palmeri ML, et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: Part 1: Basic principles and terminology. Ultrasound Med Biol 2015; 41(5): 1126-47.[http://dx.doi.org/10.1016/j.ultrasmedbio.2015.03.009] [PMID: 25805059] ]. It is useful for evaluating the elasticity of soft tissues such as the Achilles tendon [16De Zordo T, Chhem R, Smekal V, et al. Real-time sonoelastography: Findings in patients with symptomatic achilles tendons and comparison to healthy volunteers. Ultraschall Med 2010; 31(4): 394-400.[http://dx.doi.org/10.1055/s-0028-1109809] [PMID: 19946833] ] and can facilitate rotator cuff injuries [17Rosskopf AB, Ehrmann C, Buck FM, Gerber C, Flück M, Pfirrmann CW. Quantitative shear-Wave US elastography of the supraspinatus muscle: Reliability of the method and relation to tendon integrity and muscle quality. Radiology 2016; 278(2): 465-74.[http://dx.doi.org/10.1148/radiol.2015150908] [PMID: 26540450] ]. Furthermore, a recent study indicated that CHL in a frozen shoulder is stiffer than the CHL of the unaffected side based on an evaluation using SWE [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. However, there have been no reports about the changes in elasticity of the CHL resulting from the natural aging process. We hypothesized that the elasticity of the CHL on the dominant side increases with increasing age because it operates under more stressful and impaired conditions in contrast to the opposite side.

The purpose of this study was to use SWE to investigate the correlations between age, sex, and shoulder dominance, and elasticity of the CHL in healthy individuals.

2. Materials and Methods

2.1. Participants

The study protocols were approved by the institutional review board of the Iwate Prefectural Central Hospital (approved number: 2455). All study participants provided informed consent. Eighty-four healthy volunteers (39 men and 45 women) were included in this study. All the volunteers selected were Japanese nationals having a BMI that is normal for the Japanese population. The mean age was 42.6 years (range: 22–69, Standard Deviation (SD): 13.6), and they were divided into five age groups: 20s (20–29, n = 19), 30s (30–39, n = 17), 40s (40–49, n = 20), 50s (50–59, n = 13), and 60s (60–69, n = 15). The elasticity of the CHL in the bilateral shoulders in the neutral position, as well as the 30° ER positions (ER at 30°), was evaluated using SWE (Supersonic Imagine, Aix-En-Provence, France) equipped with a 4-15 MHz superficial linear transducer. We excluded patients with a history of fractures around the shoulder girdle, previous shoulder and chest operations, and rotator cuff tears confirmed by ultrasound, and individuals with diabetes mellitus.

2.2. Measuring Elasticity of the CHL

Two orthopedic surgeons with 11 and 13 years of musculoskeletal ultrasonographic experience, who had no access to each participant’s information, recorded the ultrasonic data used to determine CHL elasticity. The participants were placed in the supine position on an examination table to facilitate accurate measurements. Assistant physiotherapists maintained the elbows at 90° flexion with the arm at the side, and sequentially moved it from the neutral position to the 30° ER position. B-mode ultrasound was emitted in an axial oblique plane by placing the transducer over the lateral portion of the coracoid process, which revealed a longitudinal image of the CHL on the surface of the SSC [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. For the SWE examinations, the participants’ postures and the transducer positions were the same as for the B-mode ultrasound measurements. The tip of the transducer was covered with gel and placed smoothly on the skin without exerting pressure on the tissues. Because chest wall motion could interfere with elastogram stability, all the participants were advised to hold their breath for 5–10 seconds during the assessments. CHL elasticity on the surface of the SSC was measured and recorded in both neutral and 30° ER positions Fig. (1b). A region of interest with a diameter of 1.5 mm was set at the centermost point of the coracoid process and at the primary attachment point of the SSC as the primary measurement area Fig. (1a) based on a previous report [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. The circular regions of interest for the quantitative analysis provided the maximum, minimum, standard deviation, and mean elastic modulus in kPa. All kPa moduli were calculated from the raw data image using Osirix MD 9.5 medical imaging software. The mean elastic modulus for both shoulders was recorded for all participants in both positions. All measurements were obtained in triplicate by each of the two orthopedic surgeons and the average values were used for the statistical analysis. Ultrasonic penetration was estimated to be about 1.0 cm depending on the subject’s amount of body fat.

Fig. (1)
Measurement area of the elastic modulus of the coracohumeral ligament using shear wave elastography.


2.3. Statistical Analysis

The statistical analysis for the two positions (according to sex, age, and dominance) was performed using the Student’s t-test and Wilcoxon’s rank sum test (elastic modulus of the CHL). All continuous variables were tested for deviations from the normal distribution. Correlations between continuous variables with and without normal distributions were analyzed using Spearman’s correlation coefficient. Differences among age groups were compared using the Kruskal-Wallis test (two-tailed). Data (age and CHL elastic modulus) were expressed as mean ± SD. A value of P < 0.05 was considered statistically significant. To achieve a power of 80%, a level of 0.05 for statistical significance, and an effect size of 0.8, the sample size for each group needed to be 13. All statistical analyses were calculated using the statistical software package SPSS (version 23.0, Armonk, NY: IBM Corp). The Interclass Correlation Coefficient (ICC) was calculated to determine the intra- and inter-rater reliability of measurements of the CHL elastic modulus, both in the neutral and 30° ER positions. Agreement was classified as poor (ICC, 0.00–0.20), fair (ICC, 0.20–0.40), good (ICC, 0.40–0.75), and excellent (ICC > 0.75).

3. RESULTS

Inter-observer reliability of elastic modulus measurements in the CHL was excellent in both the neutral position (dominant; interclass correlation coefficients [ICC]: 0.876, 95% confidence interval (CI): 0.737–0.934, non-dominant; ICC: 0.865, 95% CI: 0.713–0.928) and ER at 30° position (dominant; ICC: 0.85, 95% CI: 0.559–0.932, non-dominant; ICC: 0.877, 95% CI: 0.664–0.942). The intra-observer reliability of elastic modulus measurements in the CHL was excellent in both the neutral position (dominant; ICC: 0.834, 95% CI: 0.773–0.883, non-dominant; ICC: 0.807, 95% CI: 0.737–0.863) and ER at 30° position (dominant; ICC: 0.773, 95% CI: 0.694–0.838, non-dominant: ICC: 0.803, 95% CI: 0.732–0.860).

There was no significant difference in the average ages of the men (43.9 years, SD 14.3) and the women (42 years, SD 13, P = 0.55). A comparison of the elasticity of the CHL between the neutral position and ER at 30° (n = 84) is shown in Table 1. The elastic modulus was significantly greater in the ER at 30° position than in the neutral position regardless of sex and shoulder dominance Table 1. There was no significant difference in the elasticity of the CHL between men and women for both the neutral and ER at 30° positions (P = 0.129 and 0.209, respectively). There was no significant difference in the elasticity of the CHL between the dominant and the non-dominant sides in both the neutral and ER at 30° positions (P = 0.824 and 0.386, respectively).

Table 1
Comparison of CHL elasticity between neutral and ER at 30° positions (n = 84).


Correlation coefficients for age and elasticity of the CHL on the dominant and non-dominant sides are shown in Table 2. Significant positive correlations between age and elasticity of the CHL were observed in both the neutral and ER at 30° positions, regardless of dominance. The elasticity of the CHL at the 30° ER position was strongly correlated with the neutral position on the dominant side Table 2.

Table 2
Correlation coefficient differences for age and CHL elasticity on the dominant and non-dominant sides.


Graded color images of the elastic modulus in the CHL at the ER 30° position are shown in Fig. (2). The elastic modulus of the older group was higher (red) than that of the younger group (blue) Fig. (2d) when compared to the data in the younger age groups (blue color) Fig. (2b) in both neutral and ER positions.

Elasticity of the CHL in the different age groups is shown in Table 3. CHL elasticity was significantly greater with older age in both the neutral and the ER at 30° positions on the dominant side. CHL elasticity increased with increasing age and was at its highest value in patients over the age of 50. The non-dominant side showed similar changes compared to the dominant side. In the 30s and 40s age groups, the elasticity in the neutral position was equivalent irrespective of side dominance. However, CHL elasticity in the non-dominant side was greater in the ER at 30° position Table 3.

Table 3
Comparison between age groups and CHL elastic modulus in neutral and ER at 30° positions on the dominant and non-dominant sides


4. DISCUSSION

The most important finding of this study was that CHL elasticity increased with increasing age in healthy individuals. CHL elasticity at the 30° ER position was larger and more strongly correlated to the elastic modulus than CHL elasticity at the neutral position.

Fig. (2)
Elastic modulus of CHL by shear wave elastography in a 27-year-old (a) and a 69-year-old (b) in the ER 30° position.


To date, there are no available data obtained using SWE regarding the relationships between CHL elasticity, age, sex, and side dominance in healthy adult subjects.

Naturally, shoulder ROM decreases with increasing age [18Clarke GR, Willis LA, Fish WW, Nichols PJ. Preliminary studies in measuring range of motion in normal and painful stiff shoulders. Rheumatol Rehabil 1975; 14(1): 39-46.[http://dx.doi.org/10.1093/rheumatology/14.1.39] [PMID: 1121637] ]. It is also affected by poor posture, as in the increased thoracic kyphosis with a forward head position and slouched trunk posture [19Endo K, Hamada J, Suzuki K, Hagiwara Y, Muraki T, Karasuno H. Does scapular motion regress with aging and is it restricted in patients with idiopathic frozen shoulder? Open Orthop J 2016; 10: 80-8.[http://dx.doi.org/10.2174/1874325001610010067] [PMID: 27733880] , 20Kebaetse M, McClure P, Pratt NA. Thoracic position effect on shoulder range of motion, strength, and three-dimensional scapular kinematics. Arch Phys Med Rehabil 1999; 80(8): 945-50.[http://dx.doi.org/10.1016/S0003-9993(99)90088-6] [PMID: 10453773] ]. Causes of joint stiffness can be classified as follows: arthrogenic (bone, cartilage, synovial membrane, capsule, and ligaments) and myogenic (muscle, tendon, and fascia) [21Trudel G, Uhthoff HK. Contractures secondary to immobility: is the restriction articular or muscular? An experimental longitudinal study in the rat knee. Arch Phys Med Rehabil 2000; 81(1): 6-13.[http://dx.doi.org/10.1016/S0003-9993(00)90213-2] [PMID: 10638868] ]. Among the intra-articular causes, the condition of the joint capsule is the main factor [22Nicholson GP. Arthroscopic capsular release for stiff shoulders: effect of etiology on outcomes. Arthroscopy 2003; 19(1): 40-9.[http://dx.doi.org/10.1053/jars.2003.50010] [PMID: 12522401] ] and a thickened CHL is one of the most characteristic findings of frozen shoulder [1Hand GC, Athanasou NA, Matthews T, Carr AJ. The pathology of frozen shoulder. J Bone Joint Surg Br 2007; 89(7): 928-32.[http://dx.doi.org/10.1302/0301-620X.89B7.19097] [PMID: 17673588] ]. However, the manner in which degenerative changes affect shoulder motion in healthy subjects remains unknown.

The CHL originates from the horizontal limb of the coracoid process and covers the RI [23Harryman DT II, Sidles JA, Harris SL, Matsen FA III. The role of the rotator interval capsule in passive motion and stability of the shoulder. J Bone Joint Surg Am 1992; 74(1): 53-66.[http://dx.doi.org/10.2106/00004623-199274010-00008] [PMID: 1734014] ], extending coverage to the SSP, the infraspinatus, and the SSc muscles and their direct insertions [6Arai R, Nimura A, Yamaguchi K, et al. The anatomy of the coracohumeral ligament and its relation to the subscapularis muscle. J Shoulder Elbow Surg 2014; 23(10): 1575-81.[http://dx.doi.org/10.1016/j.jse.2014.02.009] [PMID: 24766789] ]. The superficial layer of the anterior CHL continues smoothly to the SSc fascia, where it firmly covers an extensive area of the anterior surface of the SSc muscle (6). The CHL was thought to play an important role in the function of the RI [24Jost B, Koch PP, Gerber C. Anatomy and functional aspects of the rotator interval. J Shoulder Elbow Surg 2000; 9(4): 336-41.[http://dx.doi.org/10.1067/mse.2000.106746] [PMID: 10979532] ]. Biomechanical studies have indicated that tension in the CHL has a significant effect on stability and ROM, providing resistance to the inferior and posterior translations of the humeral head [23Harryman DT II, Sidles JA, Harris SL, Matsen FA III. The role of the rotator interval capsule in passive motion and stability of the shoulder. J Bone Joint Surg Am 1992; 74(1): 53-66.[http://dx.doi.org/10.2106/00004623-199274010-00008] [PMID: 1734014] , 25Boardman ND, Debski RE, Warner JJ, et al. Tensile properties of the superior glenohumeral and coracohumeral ligaments. J Shoulder Elbow Surg 1996; 5(4): 249-54.[http://dx.doi.org/10.1016/S1058-2746(96)80050-4] [PMID: 8872921] , 26Ovesen J, Nielsen S. Experimental distal subluxation in the glenohumeral joint. Arch Orthop Trauma Surg 1985; 104(2): 78-81.[http://dx.doi.org/10.1007/BF00454241] [PMID: 4051701] ]. Boardman et al. reported that the CHL had a more significant effect on increased stiffness and load failure than the superior glenohumeral ligament [25Boardman ND, Debski RE, Warner JJ, et al. Tensile properties of the superior glenohumeral and coracohumeral ligaments. J Shoulder Elbow Surg 1996; 5(4): 249-54.[http://dx.doi.org/10.1016/S1058-2746(96)80050-4] [PMID: 8872921] ], which suggests that the CHL is more important for glenohumeral joint stability than the RI.

Arm position significantly influences the elasticity of the CHL. Wu reported that the elastic modulus of the CHL in symptomatic shoulders was not significantly greater than that of unaffected shoulders in the maximal ER position [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. It is normal that the CHL tightens from the neutral to ER positions. However, after reaching the maximum ER position, it is difficult to evaluate the CHL elastic modulus appropriately. Therefore, we chose to evaluate the 30° ER position, which represents only half of the standard ER angulation. The elastic modulus in the 30° ER position was found to be increased, and its correlation coefficient tended to be greater when compared to that of the neutral position in this study. These results indicate that the CHL elastic modulus in the 30° ER position reflects faint changes in the CHL that could not be detected in the neutral position. The elastic modulus of the non-dominant side was greater than that of the dominant side in the ER at 30° position in the 30s and 40s age range groups, which suggests that age-related changes tend to occur early on the non-dominant side depending on usage frequency.

A thickened CHL is considered to be one of the most characteristic manifestations of frozen shoulder [1Hand GC, Athanasou NA, Matthews T, Carr AJ. The pathology of frozen shoulder. J Bone Joint Surg Br 2007; 89(7): 928-32.[http://dx.doi.org/10.1302/0301-620X.89B7.19097] [PMID: 17673588] , 3Ozaki J, Nakagawa Y, Sakurai G, Tamai S. Recalcitrant chronic adhesive capsulitis of the shoulder. Role of contracture of the coracohumeral ligament and rotator interval in pathogenesis and treatment. J Bone Joint Surg Am 1989; 71(10): 1511-5.[http://dx.doi.org/10.2106/00004623-198971100-00009] [PMID: 2592391] ]. The eventual thickening of the CHL combined with its dense fibrous structure causes increased ER restriction [3Ozaki J, Nakagawa Y, Sakurai G, Tamai S. Recalcitrant chronic adhesive capsulitis of the shoulder. Role of contracture of the coracohumeral ligament and rotator interval in pathogenesis and treatment. J Bone Joint Surg Am 1989; 71(10): 1511-5.[http://dx.doi.org/10.2106/00004623-198971100-00009] [PMID: 2592391] , 9Neer CS II, Satterlee CC, Dalsey RM, Flatow EL. The anatomy and potential effects of contracture of the coracohumeral ligament. Clin Orthop Relat Res 1992; (280): 182-5.[PMID: 1611740] ]. A recent study showed that the elasticity of the patellar tendon significantly decreased in healthy older subjects [27Hsiao MY, Chen YC, Lin CY, Chen WS, Wang TG. Reduced patellar tendon elasticity with aging: In vivo assessment by shear wave elastography. Ultrasound Med Biol 2015; 41(11): 2899-905.[http://dx.doi.org/10.1016/j.ultrasmedbio.2015.07.008] [PMID: 26304500] ]. On the other hands, the elasticity of the CHL at the surface of the SSC increased with increasing age in the healthy participants in this study. These changes in the elasticity of tendons and ligaments associated with aging may reflect the aging process in many body parts.

Only one study that used SWE to evaluate CHL has been reported in patients with adhesive capsulitis, which showed that the surface of the CHL in the SSC on the affected side was thicker and stiffer than on the unaffected side [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. There were no differences in the thickness or elastic modulus of the CHL between the dominant and the non-dominant shoulders in the neutral position under maximal ER in healthy subjects. These findings were consistent with our results [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ]. In previous studies, the elasticity of the CHL in healthy subjects was greater than what we observed in our data. This could be explained by different measurements and protocols. A measurement taken closer to the muscle attachment site might result in higher CHL elasticity measurements, which would be more consistent with those previous reports [12Wu CH, Chen WS, Wang TG. Elasticity of the coracohumeral ligament in patients with adhesive capsulitis of the shoulder. Radiology 2016; 278(2): 458-64.[http://dx.doi.org/10.1148/radiol.2015150888] [PMID: 26323030] ].

This study indicated that the elasticity of the CHL is directly related to the aging process regardless of shoulder dominance. This indicates that dominance-related differences are less likely to occur in response to repetitive micro traumas sustained from prior athletic activities. In the lower extremities, the semitendinosus muscle tendons in men were stiffer than those in women based on SWE evaluations [28Itoigawa Y, Takazawa Y, Maruyama Y, et al. A new technique of surgical planning for anterior cruciate ligament reconstruction: Feasibility assessment of shear wave elastography to tendon of semitendinosus muscle. Clin Anat 2018; 31(3): 404-8.[http://dx.doi.org/10.1002/ca.23000] [PMID: 29044664] ], which is contrary to our results. This could be explained by a difference in measurement locations. Previous reports stated that female subjects in general had significantly greater ROMs compared to male subjects [5Barnes CJ, Van Steyn SJ, Fischer RA. The effects of age, sex, and shoulder dominance on range of motion of the shoulder. J Shoulder Elbow Surg 2001; 10(3): 242-6.[http://dx.doi.org/10.1067/mse.2001.115270] [PMID: 11408905] ], which could be explained by differences in joint laxity related to muscle mass. This principal exception to this explanation is at the glenohumeral joint.

The limitations to this study are as follows: (1) absence of arthroscopic or histological evaluations, (2) absence of frozen shoulder comparisons, (3) absence of ROM and laxity evaluations, (4) non-exclusion of degenerative joint diseases based on imaging, (5) difficulty in assessing tissue hydration and flexion based on age within the scope and technical ability of our testing procedure adopted for this research protocol, and (6) focus on a specific CHL region of interest near the coracoid process.

CONCLUSION

CHL elasticity generally increased with age. Elasticity of the CHL in the 30° ER position was greater and correlated more strongly to the elastic modulus compared that in the neutral position. An increase in the elasticity of the CHL is one of the many age-related changes faced by healthy individuals. Further research is needed to evaluate the relationships between age-based pathological changes in CHL elasticity, and how those relationships progressively relate to frozen shoulder diagnoses.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study protocols were approved by the institutional review board of the Iwate Prefectural Central Hospital (approved number: 2455).

HUMAN AND ANIMAL RIGHTS

Both studies that originated the data used in the present secondary data analysis were conducted in accordance with the standards of the responsible ethic committee and with the Helsinki Declaration of 1975, as revised in 2000 and 2008.

CONSENT FOR PUBLICATION

Written informed consent was obtained from all participants.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

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