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The Superior Glenohumeral Joint Capsule Alone Does Not Prevent Superior Translation of the Humeral Head: An In Vitro Biomechanical Study
The Superior Glenohumeral Joint Capsule Alone Does Not Prevent Superior Translation of the Humeral Head: An In Vitro Biomechanical Study Qingxiang Hu, M.D., Zhenyu Ding, M.D., Haoyu Zhang, B.S., and Yaohua He, M.D.
Purpose: To answer 2 questions: What is the main structure that prevents the superior translation of the humeral head, the supraspinatus or the superior capsule (SC)? And what mechanism does the principal structure rely on to prevent the superior translation of the humeral head, the spacer effect or the tensional hammock effect? Methods: Eight shoulder specimens were assessed using a custom biomechanical testing system. Glenohumeral superior translation and subacromial peak pressure were compared using 6 models: the intact joint model, supraspinatus dysfunction model, supraspinatus defect model, SC tear model, SC defect model, and irreparable rotator cuff tear (IRCT) model. Results: Compared with the intact joint model, the supraspinatus defect model significantly increased the superior translation (by 2.6 mm; P < .001) and subacromial peak pressure (by 0.43 MPa; P ¼ .013) at 0 glenohumeral abduction, while the SC defect model unremarkably altered the superior translation at 0 (by 0.6 mm; P ¼ .582) and 45 (by 0.3 mm; P ¼ .867) of glenohumeral abduction and the subacromial peak pressure at 0 (by 0.11 MPa; P ¼ .961), 30 (by 0.03 MPa; P ¼ .997), and 45 (by -0.33 MPa; P ¼ .485) of glenohumeral abduction. The supraspinatus dysfunction model significantly increased the superior translation at 0 (by 1.7 mm; P < .001), 30 (by 1.2 mm; P ¼ .005), and 45 (by 0.8 mm; P ¼ .026) of glenohumeral abduction, but not the subacromial peak pressure compared with the intact joint model. However, no significant differences were found between the supraspinatus defect model and the supraspinatus dysfunction model with respect to the superior translation or subacromial peak pressure (all P > .05). Conclusions: The anatomic SC has a negligible role in preventing the superior translation of the humeral head. Clinical Relevance: SC reconstruction is not a simple anatomic reconstruction, and its promising clinical outcome may be due to tensional fixation technique and choice of graft.
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uperior translation of the humeral head, usually a sign of a rotator cuff rupture, may lead to abnormal shoulder biomechanics that can influence shoulder function.1,2 Restoration of the glenohumeral joint position is important in the treatment of rotator cuff
From the Department of Sports Medicine, Shanghai Jiaotong University Affiliated Sixth People’s Hospital (Q.H., Z.D., Y.H.), Shanghai, People’s Republic of China; and Department of Biostatistics, Bloomberg School of Public Health (H.Z.), Johns Hopkins University, Baltimore, Maryland, U.S.A. The authors report the following potential conflicts of interest or sources of funding: This study was funded by National Natural Science Foundation of China, Grant No. 81572106. Full ICMJE author disclosure forms are available for this article online, as supplementary material. Received January 13, 2018; accepted June 10, 2018. Address correspondence to Dr. Yaohua He, M.D., Shanghai Jiaotong University Affiliated Sixth People’s Hospital, Department of Sports Medicine, 600 Yishan Rd, Shanghai 200233, People’s Republic of China. E-mail: [email protected] Ó 2018 by the Arthroscopy Association of North America 0749-8063/1866/$36.00 https://doi.org/10.1016/j.arthro.2018.06.025
tears, especially irreparable ones (irreparable rotator cuff tear [IRCT]). The superior capsular reconstruction (SCR) technique, first proposed by Mihata et al.,3-8 restores the glenohumeral joint position and leads to satisfactory clinical outcomes at short- and medium-term followups. The technique involves the use of the fascia lata or acellular dermal matrix to reconstruct the superior capsule (SC). Despite the biomechanical and clinical studies conducted by Mihata et al.,3-7 there are more questions than answers with respect to SCR. The essential controversy revolves around whether the anatomic SC is such an important structure that it should be reconstructed during surgery. Could the anatomic SC restrict the superior translation of the humeral head? What is the role of the anatomic SC in the presence of an intact or deficient rotator cuff? Is it necessary to reconstruct the SC in the setting of rotator cuff repair? To better explore the function of the SC, Ishihara et al.9 conducted a biomechanical study demonstrating
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that a defect in the SC increased glenohumeral translations in all directions. In a review of the SC and SCR, Adams et al.10 proposed that the SC forms an overlying hammock that presses down on the humeral head. They believed that “the SC is the primary restraint for superior migration of the humeral head” and that “rotator cuff repair must restore the normal capsular anatomy to provide normal biomechanics of the joint and thus a positive clinical outcome.”10,11 However, we remain skeptical of their arguments. Ishihara et al.9 removed all muscles but the joint capsule in the specimen preparation. This simplified model may facilitate functional analysis of the SC, but it is rather arbitrary. The removal of all muscles, on the one hand, failed to simulate the glenohumeral joint under physiological conditions, while on the other, it resulted in an exaggeration of the functions of the SC in glenohumeral stabilization. It is highly possible that the functions of the SC reported by Ishihara et al. would be inconspicuous under physiological conditions. As for the hammock effect proposed by Adams et al., our previous cadaveric experience demonstrated that, after the removal of the supraspinatus, the humeral head could easily hit the undersurface of the acromion when a superiorly directed force was applied. The SC remained in a slack state without tension throughout the humeral head superior translation, meaning the hammock mechanism was not triggered. Our study was designed to answer 2 questions: What is the main structure that prevents the superior translation of the humeral head, the supraspinatus or the SC? And what mechanism does the principal structure rely on to prevent the superior translation of the humeral head, the spacer effect or the tensional hammock effect? We hypothesized that it was the supraspinatus, rather than the SC, that effectively restricted the superior translation of the humeral head through the tensional hammock mechanism.
Materials and Methods Specimen Preparation Ten fresh-frozen upper-extremity specimens were thawed overnight before preparation. After dissection, the specimens with rotator cuff tears, bone fractures, or motion restriction were excluded. The skin and subcutaneous tissue around the scapula were removed down to the midpoint of the humerus. The distal part of the extremity was left intact. The thorax and clavicle were detached. The serratus anterior, trapezius, and pectoralis minor were removed. The tendinous insertions of the deltoid, pectoralis major, latissimus dorsi, supraspinatus, infraspinatus, teres minor, and subscapularis were preserved. During dissection, the deltoid and rotator cuff were separated
carefully to avoid damage to the continuity of the capsule and coracoacromial ligament. The tendinous insertions were sutured in a locking cross-stitch manner by no. 2 FiberWire sutures (Arthrex). The deltoid, subscapularis, pectoralis major, and infraspinatus-teres minor complex were each loaded by 3 lines of pull; the latissimus dorsi and supraspinatus were each loaded by 2 lines of pull.4,12 Shoulder Jig System The custom shoulder jig included a metal tray, jig, frame, perforated steel plate, and pulley/suspension system. The frame was constructed with an aluminum profile system. The perforated steel plate was used to adjust the direction of the force loads. The pulley/suspension system consisted of pulleys, a suspension beam, and weights that provided force loads for the muscles (Fig 1). The pulley diminished friction as much as possible. Before testing, the scapula was fixed in the jig with plaster. The scapula and jig were adjusted to 20 of anterior tilt in the sagittal plane according to a previous study with the assistance of a GCL 2-160 Self-Levelling Cross-Line Laser Device (Bosch, Stuttgart, BadenWürttemberg, Germany) and goniometer.5 During the test, all specimens were kept moist with normal saline solution.
Models and Testing Positions Models There were 6 models (Fig 2). The first model was the intact joint model with a normal SC and supraspinatus. The second model was the supraspinatus dysfunction model and simulated a suprascapular nerve injury. In this model, the load of the supraspinatus was removed. The third model was the supraspinatus defect model. To continue the subsequent steps, the supraspinatus was drawn through the subacromial space laterally rather than cut off completely to expose the SC. In this model, the load of the supraspinatus was removed. The fourth model was the SC tear model. A U-shaped cut was made along the superior border of the glenoid medially and the supraspinatus border anteriorly and posteriorly, followed by position restoration of the supraspinatus. The fifth model was the SC defect model, which was constructed by removing the whole SC. The sixth model was the IRCT model. Both the SC and supraspinatus were removed, exposing the humeral head. In this model, the load of the supraspinatus was removed. Testing Positions Each model was tested at 0 , 30 , and 45 of glenohumeral abduction with the rotation angle fixed at 30 of external rotation according to a previous study (Table 1).3 The abduction and rotation degrees were determined by a GCL 2-160 Self-Levelling Cross-Line
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Fig 1. Customized shoulder jig system: (A) loadings; (B) the pulley system.
Laser Device and goniometer. The supraspinatus defect model was only tested at the 0 abduction/30 external rotation position because the insertion of the supraspinatus impinged on the undersurface of the acromion at higher degree abduction positions. Measurement In a given model, the superior translation and subacromial peak pressure were measured at each testing position. The superior translation measurement was performed using a GCL 2-160 Self-Levelling Cross-Line Laser Device. Two marks were made on the specimen, one on the acromion and the other on the humeral head. With the help of the laser device, the vertical distance between the 2 marks was measured. To measure superior translation, 2 loads were used. One was the balanced load, and the other was the superiorly directed load. The value of these loads was determined on the basis of the cross-sectional area of the muscle, a common practice used in previous studies.3,13,14 The balanced load was 40 N for the deltoid, 20 N for the pectoralis major, 10 N for the subscapularis, 10 N for the supraspinatus, 10 N for the infraspinatus-teres minor complex, and 20 N for the latissimus dorsi. The glenohumeral joint position under the balanced load was the initial position.4 The superiorly directed load was 80 N for the deltoid, 0 N for the pectoralis major, 10 N for the subscapularis, 10 N for the supraspinatus, 10 N for the infraspinatus-teres minor complex, and 0 N for the latissimus dorsi. The supraspinatus force load was removed when we tested the supraspinatus dysfunction, supraspinatus defect, and IRCT models, as
was explained in the Models section. The superiorly directed load aimed to shift the humeral head upward. The superior translation is the change of the vertical distance between the 2 markers under the balanced and superiorly directed loads. Subacromial pressure was obtained using the Fuji Prescale System, a pressure test system adopted in many biomechanical studies.15-17 Super low-pressure type (LLW, 0.5-2.5 MPa) and ultra-super low-pressure type (LLLW, 0.2-0.6 MPa) were chosen according to the pressure ranges suggested by previous studies.3-6 To detect the subacromial pressure, a double-layer film was inserted between the coracoacromial arch and humeral head and was maintained under a superiorly directed load for 2 minutes.4-6,16 The film was scanned and then analyzed by Matlab R2017b software (The MathWorks, Natick, MA). Data Analysis When we performed the comparison, the joint position was a controlled variable, meaning that comparisons between the various models were made at the same joint position. To investigate which was the main structure that prevents the superior translation of the humeral head, the data from the intact joint, supraspinatus defect, SC defect, and IRCT models were compared. If the supraspinatus played a major role in preventing the humeral head from undergoing a superior translation, the data from the intact joint, supraspinatus dysfunction, and supraspinatus defect models would be compared to explore the underlying mechanism. If the SC proved to be the major contributor of superior stability, the data from the intact joint,
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Fig 2. Cadaveric models in the study. (A) The intact joint model. The superior capsule (SC) and supraspinatus were preserved intact from a lateral view (right shoulder). Loading of 10 N was given to the supraspinatus. (B) The supraspinatus dysfunction model. The SC and supraspinatus were preserved intact from a lateral view (right shoulder). All muscles were loaded except the supraspinatus to simulate supraspinatus dysfunction. (C) Anterior view of a right shoulder. The supraspinatus defect model. The supraspinatus was drawn through the subacromial space laterally, exposing the SC and mimicking a supraspinatus defect scenario. (D) Lateral view of a right shoulder. The SC tear model. A U-shaped cut was made along the superior border of the glenoid medially and the supraspinatus border anteriorly and posteriorly. (E) Lateral view of a right shoulder. The SC defect model. The SC was removed completely. (F) Lateral view of a right shoulder. The irreparable rotator cuff tear model. Both the SC and supraspinatus were removed. (B, biceps tendon; C, coracoid; CAL, coracoacromial ligament; CHL, coracohumeral ligament; G, glenoid; H, humeral head; Infra, infraspinatus tendon; Tmin, teres minor tendon; Sups, supraspinatus tendon.)
SC tear, and SC defect models would be compared to explore the underlying mechanism. Statistical analyses were performed using SPSS 22.0 (IBM) software. Repeated-measures analysis of variance was performed for each independent variable, including the superior translation and subacromial peak pressures. A post hoc Tukey test was conducted after repeated-measures analysis of variance. The data are presented in the form of means standard errors. P < .05 was considered statistically significant. As for the sample size, 8 specimens were finally included in our study according to previous biomechanical studies.3-6 A post hoc power calculation by
Power Analysis and Sample Size software version 11.0 (PASS, NCSS statistical software, LLC, Kaysville, UT) indicated that 8 specimens provided more than 80% of the power to detect significant differences in the superior translation and subacromial peak pressure.
Results A total of 10 specimens were thawed and dissected. Two were excluded because of rotator cuff tears. The other 8 specimens were included (from 3 male donors and 5 female donors). The donor age of the included specimens ranged between 60 and 84 years old (with a mean age of 73.5 years old).
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BIOMECHANICS OF SUPERIOR CAPSULE Table 1. Models and Testing Positions Models 1. Intact joint 2. Sups dysfunction (SSN injury) 3. Sups defect 4. SC tear 5. SC defect 6. Irreparable rotator cuff tear
Loadings Load pair Load pair without Sups force Load pair without Sups force Load pair Load pair Load pair without Sups force
Joint Positions 0 , 30 , 45 ABD 0 , 30 , 45 ABD 0 ABD* 0 , 30 , 45 ABD 0 , 30 , 45 ABD 0 , 30 , 45 ABD
ABD, abduction; SC, superior capsule; SSN, suprascapular nerve; Sups, supraspinatus. *The supraspinatus defect model was only tested at the 0 abduction because the insertion of the supraspinatus impinged on the undersurface of the acromion at higher degree abduction positions.
Superior Translation and Subacromial Peak Pressure Were Increased in the IRCT Compared with the intact joint model, the IRCT model notably increased the superior translation at 0 (by 3.0 mm; P < .001), 30 (by 2.1 mm; P < .001), and 45 (by 0.9 mm; P ¼ .007) of glenohumeral abduction and increased the subacromial peak pressure at 0 (by 0.68 MPa; P < .001) and 30 (by 0.30 MPa; P < .001) of glenohumeral abduction (Tables 2 and 3). The Supraspinatus, Rather Than the SC, Played a Primary Role in Preventing Superior Translation The supraspinatus defect model significantly increased the superior translation (by 2.6 mm; P < .001) and subacromial peak pressure (by 0.43 MPa; P ¼ .013) at 0 glenohumeral abduction compared with those of the intact joint model. Nevertheless, there were no significant differences in the superior translation or subacromial peak pressure between the supraspinatus defect model and the IRCT model (P > .05). The SC defect model unremarkably altered the superior translation at 0 (by 0.6 mm; P ¼ .582) and 45 (by 0.3 mm; P ¼ .867) of glenohumeral abduction and subacromial peak pressure at 0 (by 0.11 MPa; P ¼ .961), 30 (by -0.03 MPa; P ¼ .997), and 45 (by 0.33 MPa; P ¼ .485) of glenohumeral abduction. However, compared with the IRCT model, the SC defect model had notably smaller superior translation at 0 (by 2.4 mm; P < .001) and a significantly lower subacromial peak pressure at 0 (by 0.57 MPa; P < .001), 30 (by 0.33 MPa; P < .001), and 45 (by 0.71 MPa; P ¼ .004) of glenohumeral abduction (Tables 2 and 3). Mechanism of the Supraspinatus in Preventing Superior Translation The supraspinatus dysfunction model significantly increased the superior translation at 0 (by 1.7 mm; P < .001), 30 (by 1.2 mm; P ¼ .005), and 45 (by 0.8 mm; P ¼ .026) of glenohumeral abduction but not the subacromial peak pressure compared with those of
the intact joint model. The supraspinatus defect model significantly increased the superior translation (by 2.6 mm; P < .001) and subacromial peak pressure (by 0.43 MPa; P ¼ .013) at 0 glenohumeral abduction compared with those of the intact joint model. However, no significant differences were found between the supraspinatus defect model and supraspinatus dysfunction model in superior translation or subacromial peak pressure (all P > .05; Tables 2 and 3).
Discussion To identify the primary structure preventing superior translation of the humeral head, the results of the intact joint, supraspinatus defect, SC defect, and IRCT models were compared. The supraspinatus defect model facilitated superior translation of the humeral head at a larger scale than the SC defect model at 0 glenohumeral abduction (P < .001). At 30 glenohumeral abduction, although the SC defect model had a significantly larger superior translation than the intact joint model, the translation value in the SC defect model was not larger than that of the supraspinatus dysfunction model, in addition to the fact that the supraspinatus defect model did not present a smaller superior shift than the supraspinatus dysfunction model. In other words, the values of superior translation in the SC defect model were not larger than those of the supraspinatus defect model. Therefore, we conclude that the role of the supraspinatus may be more primary compared with that of the anatomic SC in preventing superior translation of the humeral head. Superior translation of the humeral head is restricted by several structures. It is reported that many muscles (e.g., latissimus dorsi, long head of biceps, infraspinatus) have a powerful capacity to depress the humeral head.18 Halder et al.18 reported that the supraspinatus could depress the humeral head by 2.0 1.4 mm, providing a minor superior stabilizing effect. In our study, the anatomic SC was weaker than the supraspinatus in superior stability. Therefore, the anatomic SC has a negligible role in preventing superior translation. The nature of SCR may not be a simple anatomic reconstruction of the SC. Another focus of the study was the mechanism of the supraspinatus in preventing the superior translation of the humeral head. In our study, 2 potential mechanisms were proposed and tested, the spacer effect and the tensional hammock effect. The spacer effect is the physical blocking of an object. In the human glenohumeral joint, subacromial tissue (e.g., the supraspinatus and the SC) blocked the humeral head from a superior shift. A good clinical application of the spacer effect is the InSpace balloon placed under the acromion in IRCT patients to prevent the superior translation of the humeral head.19-21
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Table 2. Superior Glenohumeral Translation Intact Joint Angle 0 30 45
Translation, mm 1.7 0.2* 1.3 0.1* 1.1 0.2*
Supraspinatus Dysfunction 95% CI 1.2-2.2 0.9-1.5 0.7-1.6
Translation, mm 3.4 0.6*y 2.5 0.5*y 1.9 0.3y
95% CI 1.9-4.8 1.3-3.6 1.1-2.7
Supraspinatus Defect Translation, mm 4.3 0.6y d d
95% CI 2.9-5.7 d d
Superior Capsule Tear Translation, mm 2.4 0.3* 2.3 0.3*y 1.3 0.1*
95% CI 1.6-3.1 1.6-3.0 1.1-1.5
Superior Capsule Defect Translation, mm 2.3 0.3* 2.5 0.4y 1.4 0.2
95% CI 1.6-3.1 1.6-3.4 0.9-1.9
Irreparable Rotator Cuff Tear Translation, mm 4.7 0.6y 3.4 0.5y 2.0 0.4y
95% CI 3.4-6.1 2.1-4.6 1.0-3.1
NOTE. Values are presented as the mean standard error and 95% CI (95% CI). CI, confidence interval. *A significant difference was found compared with the irreparable rotator cuff tear model (P < .05). y A significant difference was found compared with the intact joint model (P < .05).
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Table 3. Subacromial Peak Contact Pressure Intact Joint Glenohumeral Abduction Pressure, Mpa 0.45 0.08* 0 30 0.59 0.04* 45 1.10 0.21
Supraspinatus Dysfunction
Supraspinatus Defect
95% CI Pressure, Mpa 95% CI Pressure, Mpa 0.26-0.64 0.76 0.14* 0.42-1.10 0.88 0.14y 0.49-0.69 0.67 0.04* 0.57-0.76 0.59-1.61 0.74 0.02* 0.68-0.79 -
95% CI 0.56-1.20 -
NOTE. Values are presented as the mean standard error and 95% confidence interval (95% CI). *A significant difference was found compared with the irreparable rotator cuff tear model (P < .05). y A significant difference was found compared with the intact joint model (P < .05).
Superior Capsule Tear Pressure, Mpa 0.55 0.05* 0.60 0.04* 0.99 0.22
95% CI 0.44-0.67 0.52-0.69 0.48-1.50
Superior Capsule Defect Irreparable Rotator Cuff Tear Pressure, Mpa 0.56 0.03* 0.56 0.03* 0.77 0.14*
95% CI 0.49-0.63 0.49-0.64 0.45-1.10
Pressure, Mpa 1.13 0.13y 0.89 0.11y 1.48 0.04
95% CI 0.81-1.45 0.63-1.16 1.38-1.58
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The tensional hammock effect is another potential mechanism. The soft tissue (e.g., the supraspinatus and the SC) forms a “hammock” overlying the humeral head. When the humeral head shifts superiorly, the hammock is tensional and presses the humeral head downward. To identify the major mechanism of the supraspinatus in preventing the superior translation of the humeral head, the intact joint, supraspinatus dysfunction, and supraspinatus defect models were compared. In the intact joint model, the supraspinatus was loaded with 10 N. In the supraspinatus dysfunction model, although the supraspinatus was present, the load of the supraspinatus was removed, meaning the tensional property was gone. In the supraspinatus defect model, neither the spacer effect nor the tensional property of the supraspinatus was preserved. The supraspinatus dysfunction model demonstrated significant increases in superior translation, but not in subacromial peak pressure, at all abduction positions compared with the intact joint model. However, no notable increases were found in the superior translation or subacromial peak pressure in the supraspinatus defect model compared with those of the supraspinatus dysfunction model at 0 glenohumeral abduction. This result indicates that the tensional hammock effect of the supraspinatus may be more significant for preventing superior translation of the humeral head. It is noteworthy that Mura et al.22 conducted a similar cadaveric study on the rotator cuff, arriving at the opposite conclusion. They found that there were no differences in superior translation in the supraspinatus unload model (similar to the supraspinatus dysfunction model) and supraspinatus resection model (similar to the supraspinatus defect model) compared with the intact joint model (similar to the intact joint model). We believe this discrepancy could be attributed to some major differences in experimental methods. In Mura et al.’s experiment, the loading settings were 32 N for the infraspinatus-teres minor complex, 30 N for the subscapularis, and 16 N for the supraspinatus. The loadings for the infraspinatus-teres minor complex and subscapularis in Mura et al.’s study were 3 times those of our experiment; however, the loading for the supraspinatus was only 1.6 times that of our experiment. As was mentioned above, the supraspinatus might only play a minor role in the superior stabilization of the humeral head compared with the role of other muscles.18 The increased loads would enhance the stabilization function provided by the infraspinatus and subscapularis, further minimizing the contribution made by the supraspinatus. In addition, Mura et al. did not take the weight of the upper extremity into consideration, which possibly influenced the translation of the humeral head. In our experiment, we preserved the weight and length of the upper extremity to
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simulate physiological conditions as much as possible.3-6 We believe that the specimen preparation and loading conditions exerted a significant influence on the results. Some clinical studies indicated that suprascapular nerve blocking would not increase superior translation at 0 and 30 shoulder abduction positions.23,24 It is undeniable that the interrelationships among various structures under physiological conditions make it difficult to study the function of a specific structure separately in an in vivo study. The force changes in other muscles after nerve blocking might easily compensate for the loss of the tensional effect of the supraspinatus. Failure to reflect changes of muscle forces in a timely and accurate fashion is a limitation of our biomechanical study. Our results indicated that it is the supraspinatus rather than the SC that plays a primary role in preventing superior translation of the humeral head. Therefore, the nature of SCR may not be simple anatomic reconstruction. Clinical studies indicated that SCR successfully decreased pain and improved function in IRCT patients.7,25-27 Patients undergoing the surgery were able to resume recreational sports and physical work.26 The successful clinical results are seemingly contradictory to our biomechanical findings. Possible explanations for these contradictory results are as follows: First, the dermal allograft used in SCR had a thickness ranging from 3 to 8 mm, greater than that of the SC.7,28-34 The graft might display a spacer effect. The biomechanical study of Mihata et al.6 confirmed that an 8 mm thick fascia lata provided better stability in SCR than a 4 mm thick graft. Second, the tensional fixation technique in SCR alters the biomechanical properties of the graft. In SCR, the graft is attached at 30 glenohumeral abduction. This fixation procedure results in a nonanatomic functional restraint.11 According to Mihata et al.’s study, fixing the graft at 30 glenohumeral abduction gave a smaller superior translation of the humeral head and subacromial contact pressure than fixation at 10 glenohumeral abduction. Thus, SCR may not be a simple anatomic reconstruction of the SC, but rather a functional modification of the graft. The choice of the graft and tensional fixation technique may be important for surgery and should be studied in the future. Two clinical scenarios were proposed by Adams et al. in the review “The Rotator Cuff and the Superior Capsule: Why We Need Both.”10 The first scenario was described in a patient who had a suprascapular nerve injury with an intact rotator cuff. The patient was able to abduct and manage overhead movements despite a loss of 75% of strength due to nerve dysfunction.35 Adams et al.,10 therefore, believed that the preserved abduction and overhead movements were due to static stabilization provided by the SC.10
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First, the superior translation of the humeral head is the collective result of several forces. The infraspinatus, long head of biceps, and latissimus dorsi all play important roles in humeral head depression.18 It cannot be ruled out that the forces of the aforementioned 3 muscles might be altered after nerve blocking.24 The altered muscle forces profile has the potential to stabilize the humeral head and also explain why the patient could manage overhead movements after nerve blocking. Second, our study demonstrated that the SC had a negligible role in the superior stability of the glenohumeral joint. On the one hand, the SC tear and SC defect models did not significantly increase the superior translation of the humeral head compared with the intact joint model. On the other hand, the SC could not prevent superior translation in the supraspinatus dysfunction model or supraspinatus defect model. Therefore, the preserved function in suprascapular nerve injury should not be attributed to an intact SC. The other clinical scenario was in a patient with a massive rotator cuff tear with grade 3 or 4 fatty infiltration. Adams et al.10 noted that preoperative restricted active range of motion (ROM) or even pseudoparalysis was improved after surgery, without change of the muscle appearance on postoperative MRI. They believed that the restoration of the capsular anatomy contributed to the normal biomechanics and improved the clinical functions.10 However, their proposition was far from convincing. First, pseudoparalysis is a phenomenon rife with controversies. Pseudoparalysis was recently defined as the loss of total active ROM that cannot recover even after subacromial analgesia.36 The studies referred to in Adams et al.’s review did not mention subacromial analgesia, which means some participants recruited in the studies were not pseudoparalysis cases from a strict perspective.37,38 An active ROM below 90 is called pseudoparesis.36 The large heterogeneity in the inclusion criteria made it difficult to determine whether the loss of active ROM was due to mechanical reasons, pain, or both. In addition, arthroscopic surgery relieved pain to some extent. According to Gerber et al.,37 the pain points increased from 7.6 (pain) to 14.4 (no pain) after arthroscopy. Denard et al.38 also reported that patients with pseudoparalysis experienced pain relief from 5.7 (pain) to 1.1 (no pain) based on the visual analog scale. It is unreasonable to exclude the effect of pain relief. Therefore, what Adams et al. proposed is a complex problem that cannot be simply explained by the function of the SC. Limitations There are some limitations in our work. First, we could not avoid the intrinsic defects of biomechanical studies. This was a static biomechanical study, and the muscle loads were set on the basis of previous research.
We could not simulate all of the physiological load patterns of the shoulder joint. Second, in our IRCT model, we only removed the supraspinatus and SC. Although the modeling techniques were similar to those of previous studies, in clinical scenarios, more tendon injuries may be involved in IRCT, especially in massive IRCT. Third, we did not consider the gravitational effects of blood in the specimens. Fourth, we set the measurement positions at 0 , 30 , and 45 rather than 0 , 30 , and 60 because the laser beam would be blocked by the deltoid muscles when the abduction degree was higher.
Conclusions The anatomic SC has a negligible role in preventing the superior translation of the humeral head.
References 1. Wieser K, Rahm S, Schubert M, et al. Fluoroscopic, magnetic resonance imaging, and electrophysiologic assessment of shoulders with massive tears of the rotator cuff. J Shoulder Elbow Surg 2015;24:288-294. 2. Goutallier D, Le Guilloux P, Postel JM, Radier C, Bernageau J, Zilber S. Acromio humeral distance less than six millimeter: Its meaning in full-thickness rotator cuff tear. Orthop Traumatol Surg Res 2011;97:246-251. 3. Mihata T, McGarry MH, Pirolo JM, Kinoshita M, Lee TQ. Superior capsule reconstruction to restore superior stability in irreparable rotator cuff tears: A biomechanical cadaveric study. Am J Sports Med 2012;40:2248-2255. 4. Mihata T, McGarry MH, Kahn T, Goldberg I, Neo M, Lee TQ. Biomechanical role of capsular continuity in superior capsule reconstruction for irreparable tears of the supraspinatus tendon. Am J Sports Med 2016;44: 1423-1430. 5. Mihata T, McGarry MH, Kahn T, Goldberg I, Neo M, Lee TQ. Biomechanical effects of acromioplasty on superior capsule reconstruction for irreparable supraspinatus tendon tears. Am J Sports Med 2016;44:191-197. 6. Mihata T, McGarry MH, Kahn T, Goldberg I, Neo M, Lee TQ. Biomechanical effect of thickness and tension of fascia lata graft on glenohumeral stability for superior capsule reconstruction in irreparable supraspinatus tears. Arthroscopy 2016;32:418-426. 7. Mihata T, Lee TQ, Watanabe C, et al. Clinical results of arthroscopic superior capsule reconstruction for irreparable rotator cuff tears. Arthroscopy 2013;29:459-470. 8. Mihata T, Lee TQ. Clinical outcomes of superior capsule reconstruction for irreparable rotator cuff tears without osteoarthritis in the glenohumeral joint. J Shoulder Elbow Surg 2015;24:e107-e109. 9. Ishihara Y, Mihata T, Tamboli M, et al. Role of the superior shoulder capsule in passive stability of the glenohumeral joint. J Shoulder Elbow Surg 2014;23:642-648. 10. Adams CR, DeMartino AM, Rego G, Denard PJ, Burkhart SS. The rotator cuff and the superior capsule: Why we need both. Arthroscopy 2016;32:2628-2637. 11. Verma NN, Lubowitz JH, Brand JC, Provencher MT, Rossi MJ. Could disruption of the shoulder superior
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12.
13.
14.
15.
16.
17.
18.
19.
20.
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22.
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capsule be the “essential lesion” of rotator cuff disease? Possibly, but questions remain .. Arthroscopy 2016;32: 2421-2423. Omid R, Heckmann N, Wang L, McGarry MH, Vangsness CT Jr, Lee TQ. Biomechanical comparison between the trapezius transfer and latissimus transfer for irreparable posterosuperior rotator cuff tears. J Shoulder Elbow Surg 2015;24:1635-1643. Akagi R, Kanehisa H, Kawakami Y, Fukunaga T. Establishing a new index of muscle cross-sectional area and its relationship with isometric muscle strength. J Strength Cond Res 2008;22:82-87. Veeger HE, Van der Helm FC, Van der Woude LH, Pronk GM, Rozendal RH. Inertia and muscle contraction parameters for musculoskeletal modelling of the shoulder mechanism. J Biomech 1991;24:615-629. Takahashi T, Wada Y, Yamamoto H. Soft-tissue balancing with pressure distribution during total knee arthroplasty. J Bone Joint Surg Br 1997;79:235-239. Yildiz KI, Isik C, Tecimel O, et al. Use of contact pressuresensitive surfaces as an indicator of graft tension in medial patellofemoral ligament reconstruction. Arch Orthop Trauma Surg 2013;133:1657-1663. Hille E, Schulitz KP, Henrichs C, Schneider T. Pressure and contract-surface measurements within the femoropatellar joint and their variations following lateral release. Arch Orthop Trauma Surg 1985;104:275-282. Halder AM, Zhao KD, Odriscoll SW, Morrey BF, An KN. Dynamic contributions to superior shoulder stability. J Orthop Res 2001;19:206-212. Anley CM, Chan SK, Snow M. Arthroscopic treatment options for irreparable rotator cuff tears of the shoulder. World J Orthop 2014;5:557-565. Savarese E, Romeo R. New solution for massive, irreparable rotator cuff tears: The subacromial "biodegradable spacer.". Arthrosc Tech 2012;1:e69-e74. Szollosy G, Rosso C, Fogerty S, Petkin K, Lafosse L. Subacromial spacer placement for protection of rotator cuff repair. Arthrosc Tech 2014;3:e605-e609. Mura N, O’Driscoll SW, Zobitz ME, et al. The effect of infraspinatus disruption on glenohumeral torque and superior migration of the humeral head: A biomechanical study. J Shoulder Elbow Surg 2003;12:179-184. Werner CM, Weishaupt D, Blumenthal S, Curt A, Favre P, Gerber C. Effect of experimental suprascapular nerve block on active glenohumeral translations in vivo. J Orthop Res 2006;24:491-500. San Juan JG, Kosek P, Karduna AR. Humeral head translation after a suprascapular nerve block. J Appl Biomech 2013;29:371-379. Denard PJ, Brady PC, Adams CR, Tokish JM, Burkhart SS. Preliminary results of arthroscopic superior capsule
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32.
33.
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reconstruction with dermal allograft. Arthroscopy 2018;34: 93-99. Mihata T, Lee TQ, Fukunishi K, et al. Return to sports and physical work after arthroscopic superior capsule reconstruction among patients with irreparable rotator cuff tears. Am J Sports Med 2018:363546517753387. Pennington WT, Bartz BA, Pauli JM, Walker CE, Schmidt W. Arthroscopic superior capsular reconstruction with acellular dermal allograft for the treatment of massive irreparable rotator cuff tears: Short-term clinical outcomes and the radiographic parameter of superior capsular distance. Arthroscopy 2018;34:1764-1773. Sutter EG, Godin JA, Garrigues GE. All-arthroscopic superior shoulder capsule reconstruction with partial rotator cuff repair. Orthopedics 2017;40:e735-e738. Shishani Y, Flocken J, Gobezie R. Superior capsular reconstruction: An alternative approach to treat contained cuff tear arthropathy. Sem Arthroplasty 2016;27: 112-116. Sanchez G, Rossy WH, Lavery KP, et al. Arthroscopic superior capsule reconstruction technique in the setting of a massive, irreparable rotator cuff tear. Arthrosc Tech 2017;6:e1399-e1404. Petri M, Greenspoon JA, Millett PJ. Arthroscopic superior capsule reconstruction for irreparable rotator cuff tears. Arthrosc Tech 2015;4:e751-e755. Adams CR, Denard PJ, Brady PC, Hartzler RU, Burkhart SS. The arthroscopic superior capsular reconstruction. Am J Orthop (Belle Mead, N.J.) 2016;45:320-324. Burkhart SS, Denard PJ, Adams CR, Brady PC, Hartzler RU. Arthroscopic superior capsular reconstruction for massive irreparable rotator cuff repair. Arthrosc Tech 2016;5:e1407-e1418. Itoi E, Grabowski JJ, Morrey BF, An KN. Capsular properties of the shoulder. Tohoku J Exp Med 1993;171: 203-210. Gerber C, Blumenthal S, Curt A, Werner CM. Effect of selective experimental suprascapular nerve block on abduction and external rotation strength of the shoulder. J Shoulder Elbow Surg 2007;16:815-820. Tokish JM, Alexander TC, Kissenberth MJ, Hawkins RJ. Pseudoparalysis: A systematic review of term definitions, treatment approaches, and outcomes of management techniques. J Shoulder Elbow Surg 2017;26:e177-e187. Gerber C, Fuchs B, Hodler J. The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am 2000;82:505-515. Denard PJ, Ladermann A, Brady PC, et al. Pseudoparalysis from a massive rotator cuff tear is reliably reversed with an arthroscopic rotator cuff repair in patients without preoperative glenohumeral arthritis. Am J Sports Med 2015;43:2373-2378.
Purpose: To answer 2 questions: What is the main structure that prevents the superior translation of the humeral head, the supraspinatus or the superior capsule (SC)? And what mechanism does the principal structure rely on to prevent the superior translation of the humeral head, the spacer effect or the tensional hammock effect? Methods: Eight shoulder specimens were assessed using a custom biomechanical testing system. Glenohumeral superior translation and subacromial peak pressure were compared using 6 models: the intact joint model, supraspinatus dysfunction model, supraspinatus defect model, SC tear model, SC defect model, and irreparable rotator cuff tear (IRCT) model. Results: Compared with the intact joint model, the supraspinatus defect model significantly increased the superior translation (by 2.6 mm; P < .001) and subacromial peak pressure (by 0.43 MPa; P ¼ .013) at 0 glenohumeral abduction, while the SC defect model unremarkably altered the superior translation at 0 (by 0.6 mm; P ¼ .582) and 45 (by 0.3 mm; P ¼ .867) of glenohumeral abduction and the subacromial peak pressure at 0 (by 0.11 MPa; P ¼ .961), 30 (by 0.03 MPa; P ¼ .997), and 45 (by -0.33 MPa; P ¼ .485) of glenohumeral abduction. The supraspinatus dysfunction model significantly increased the superior translation at 0 (by 1.7 mm; P < .001), 30 (by 1.2 mm; P ¼ .005), and 45 (by 0.8 mm; P ¼ .026) of glenohumeral abduction, but not the subacromial peak pressure compared with the intact joint model. However, no significant differences were found between the supraspinatus defect model and the supraspinatus dysfunction model with respect to the superior translation or subacromial peak pressure (all P > .05). Conclusions: The anatomic SC has a negligible role in preventing the superior translation of the humeral head. Clinical Relevance: SC reconstruction is not a simple anatomic reconstruction, and its promising clinical outcome may be due to tensional fixation technique and choice of graft.
S
uperior translation of the humeral head, usually a sign of a rotator cuff rupture, may lead to abnormal shoulder biomechanics that can influence shoulder function.1,2 Restoration of the glenohumeral joint position is important in the treatment of rotator cuff
From the Department of Sports Medicine, Shanghai Jiaotong University Affiliated Sixth People’s Hospital (Q.H., Z.D., Y.H.), Shanghai, People’s Republic of China; and Department of Biostatistics, Bloomberg School of Public Health (H.Z.), Johns Hopkins University, Baltimore, Maryland, U.S.A. The authors report the following potential conflicts of interest or sources of funding: This study was funded by National Natural Science Foundation of China, Grant No. 81572106. Full ICMJE author disclosure forms are available for this article online, as supplementary material. Received January 13, 2018; accepted June 10, 2018. Address correspondence to Dr. Yaohua He, M.D., Shanghai Jiaotong University Affiliated Sixth People’s Hospital, Department of Sports Medicine, 600 Yishan Rd, Shanghai 200233, People’s Republic of China. E-mail: [email protected] Ó 2018 by the Arthroscopy Association of North America 0749-8063/1866/$36.00 https://doi.org/10.1016/j.arthro.2018.06.025
tears, especially irreparable ones (irreparable rotator cuff tear [IRCT]). The superior capsular reconstruction (SCR) technique, first proposed by Mihata et al.,3-8 restores the glenohumeral joint position and leads to satisfactory clinical outcomes at short- and medium-term followups. The technique involves the use of the fascia lata or acellular dermal matrix to reconstruct the superior capsule (SC). Despite the biomechanical and clinical studies conducted by Mihata et al.,3-7 there are more questions than answers with respect to SCR. The essential controversy revolves around whether the anatomic SC is such an important structure that it should be reconstructed during surgery. Could the anatomic SC restrict the superior translation of the humeral head? What is the role of the anatomic SC in the presence of an intact or deficient rotator cuff? Is it necessary to reconstruct the SC in the setting of rotator cuff repair? To better explore the function of the SC, Ishihara et al.9 conducted a biomechanical study demonstrating
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that a defect in the SC increased glenohumeral translations in all directions. In a review of the SC and SCR, Adams et al.10 proposed that the SC forms an overlying hammock that presses down on the humeral head. They believed that “the SC is the primary restraint for superior migration of the humeral head” and that “rotator cuff repair must restore the normal capsular anatomy to provide normal biomechanics of the joint and thus a positive clinical outcome.”10,11 However, we remain skeptical of their arguments. Ishihara et al.9 removed all muscles but the joint capsule in the specimen preparation. This simplified model may facilitate functional analysis of the SC, but it is rather arbitrary. The removal of all muscles, on the one hand, failed to simulate the glenohumeral joint under physiological conditions, while on the other, it resulted in an exaggeration of the functions of the SC in glenohumeral stabilization. It is highly possible that the functions of the SC reported by Ishihara et al. would be inconspicuous under physiological conditions. As for the hammock effect proposed by Adams et al., our previous cadaveric experience demonstrated that, after the removal of the supraspinatus, the humeral head could easily hit the undersurface of the acromion when a superiorly directed force was applied. The SC remained in a slack state without tension throughout the humeral head superior translation, meaning the hammock mechanism was not triggered. Our study was designed to answer 2 questions: What is the main structure that prevents the superior translation of the humeral head, the supraspinatus or the SC? And what mechanism does the principal structure rely on to prevent the superior translation of the humeral head, the spacer effect or the tensional hammock effect? We hypothesized that it was the supraspinatus, rather than the SC, that effectively restricted the superior translation of the humeral head through the tensional hammock mechanism.
Materials and Methods Specimen Preparation Ten fresh-frozen upper-extremity specimens were thawed overnight before preparation. After dissection, the specimens with rotator cuff tears, bone fractures, or motion restriction were excluded. The skin and subcutaneous tissue around the scapula were removed down to the midpoint of the humerus. The distal part of the extremity was left intact. The thorax and clavicle were detached. The serratus anterior, trapezius, and pectoralis minor were removed. The tendinous insertions of the deltoid, pectoralis major, latissimus dorsi, supraspinatus, infraspinatus, teres minor, and subscapularis were preserved. During dissection, the deltoid and rotator cuff were separated
carefully to avoid damage to the continuity of the capsule and coracoacromial ligament. The tendinous insertions were sutured in a locking cross-stitch manner by no. 2 FiberWire sutures (Arthrex). The deltoid, subscapularis, pectoralis major, and infraspinatus-teres minor complex were each loaded by 3 lines of pull; the latissimus dorsi and supraspinatus were each loaded by 2 lines of pull.4,12 Shoulder Jig System The custom shoulder jig included a metal tray, jig, frame, perforated steel plate, and pulley/suspension system. The frame was constructed with an aluminum profile system. The perforated steel plate was used to adjust the direction of the force loads. The pulley/suspension system consisted of pulleys, a suspension beam, and weights that provided force loads for the muscles (Fig 1). The pulley diminished friction as much as possible. Before testing, the scapula was fixed in the jig with plaster. The scapula and jig were adjusted to 20 of anterior tilt in the sagittal plane according to a previous study with the assistance of a GCL 2-160 Self-Levelling Cross-Line Laser Device (Bosch, Stuttgart, BadenWürttemberg, Germany) and goniometer.5 During the test, all specimens were kept moist with normal saline solution.
Models and Testing Positions Models There were 6 models (Fig 2). The first model was the intact joint model with a normal SC and supraspinatus. The second model was the supraspinatus dysfunction model and simulated a suprascapular nerve injury. In this model, the load of the supraspinatus was removed. The third model was the supraspinatus defect model. To continue the subsequent steps, the supraspinatus was drawn through the subacromial space laterally rather than cut off completely to expose the SC. In this model, the load of the supraspinatus was removed. The fourth model was the SC tear model. A U-shaped cut was made along the superior border of the glenoid medially and the supraspinatus border anteriorly and posteriorly, followed by position restoration of the supraspinatus. The fifth model was the SC defect model, which was constructed by removing the whole SC. The sixth model was the IRCT model. Both the SC and supraspinatus were removed, exposing the humeral head. In this model, the load of the supraspinatus was removed. Testing Positions Each model was tested at 0 , 30 , and 45 of glenohumeral abduction with the rotation angle fixed at 30 of external rotation according to a previous study (Table 1).3 The abduction and rotation degrees were determined by a GCL 2-160 Self-Levelling Cross-Line
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Fig 1. Customized shoulder jig system: (A) loadings; (B) the pulley system.
Laser Device and goniometer. The supraspinatus defect model was only tested at the 0 abduction/30 external rotation position because the insertion of the supraspinatus impinged on the undersurface of the acromion at higher degree abduction positions. Measurement In a given model, the superior translation and subacromial peak pressure were measured at each testing position. The superior translation measurement was performed using a GCL 2-160 Self-Levelling Cross-Line Laser Device. Two marks were made on the specimen, one on the acromion and the other on the humeral head. With the help of the laser device, the vertical distance between the 2 marks was measured. To measure superior translation, 2 loads were used. One was the balanced load, and the other was the superiorly directed load. The value of these loads was determined on the basis of the cross-sectional area of the muscle, a common practice used in previous studies.3,13,14 The balanced load was 40 N for the deltoid, 20 N for the pectoralis major, 10 N for the subscapularis, 10 N for the supraspinatus, 10 N for the infraspinatus-teres minor complex, and 20 N for the latissimus dorsi. The glenohumeral joint position under the balanced load was the initial position.4 The superiorly directed load was 80 N for the deltoid, 0 N for the pectoralis major, 10 N for the subscapularis, 10 N for the supraspinatus, 10 N for the infraspinatus-teres minor complex, and 0 N for the latissimus dorsi. The supraspinatus force load was removed when we tested the supraspinatus dysfunction, supraspinatus defect, and IRCT models, as
was explained in the Models section. The superiorly directed load aimed to shift the humeral head upward. The superior translation is the change of the vertical distance between the 2 markers under the balanced and superiorly directed loads. Subacromial pressure was obtained using the Fuji Prescale System, a pressure test system adopted in many biomechanical studies.15-17 Super low-pressure type (LLW, 0.5-2.5 MPa) and ultra-super low-pressure type (LLLW, 0.2-0.6 MPa) were chosen according to the pressure ranges suggested by previous studies.3-6 To detect the subacromial pressure, a double-layer film was inserted between the coracoacromial arch and humeral head and was maintained under a superiorly directed load for 2 minutes.4-6,16 The film was scanned and then analyzed by Matlab R2017b software (The MathWorks, Natick, MA). Data Analysis When we performed the comparison, the joint position was a controlled variable, meaning that comparisons between the various models were made at the same joint position. To investigate which was the main structure that prevents the superior translation of the humeral head, the data from the intact joint, supraspinatus defect, SC defect, and IRCT models were compared. If the supraspinatus played a major role in preventing the humeral head from undergoing a superior translation, the data from the intact joint, supraspinatus dysfunction, and supraspinatus defect models would be compared to explore the underlying mechanism. If the SC proved to be the major contributor of superior stability, the data from the intact joint,
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Fig 2. Cadaveric models in the study. (A) The intact joint model. The superior capsule (SC) and supraspinatus were preserved intact from a lateral view (right shoulder). Loading of 10 N was given to the supraspinatus. (B) The supraspinatus dysfunction model. The SC and supraspinatus were preserved intact from a lateral view (right shoulder). All muscles were loaded except the supraspinatus to simulate supraspinatus dysfunction. (C) Anterior view of a right shoulder. The supraspinatus defect model. The supraspinatus was drawn through the subacromial space laterally, exposing the SC and mimicking a supraspinatus defect scenario. (D) Lateral view of a right shoulder. The SC tear model. A U-shaped cut was made along the superior border of the glenoid medially and the supraspinatus border anteriorly and posteriorly. (E) Lateral view of a right shoulder. The SC defect model. The SC was removed completely. (F) Lateral view of a right shoulder. The irreparable rotator cuff tear model. Both the SC and supraspinatus were removed. (B, biceps tendon; C, coracoid; CAL, coracoacromial ligament; CHL, coracohumeral ligament; G, glenoid; H, humeral head; Infra, infraspinatus tendon; Tmin, teres minor tendon; Sups, supraspinatus tendon.)
SC tear, and SC defect models would be compared to explore the underlying mechanism. Statistical analyses were performed using SPSS 22.0 (IBM) software. Repeated-measures analysis of variance was performed for each independent variable, including the superior translation and subacromial peak pressures. A post hoc Tukey test was conducted after repeated-measures analysis of variance. The data are presented in the form of means standard errors. P < .05 was considered statistically significant. As for the sample size, 8 specimens were finally included in our study according to previous biomechanical studies.3-6 A post hoc power calculation by
Power Analysis and Sample Size software version 11.0 (PASS, NCSS statistical software, LLC, Kaysville, UT) indicated that 8 specimens provided more than 80% of the power to detect significant differences in the superior translation and subacromial peak pressure.
Results A total of 10 specimens were thawed and dissected. Two were excluded because of rotator cuff tears. The other 8 specimens were included (from 3 male donors and 5 female donors). The donor age of the included specimens ranged between 60 and 84 years old (with a mean age of 73.5 years old).
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BIOMECHANICS OF SUPERIOR CAPSULE Table 1. Models and Testing Positions Models 1. Intact joint 2. Sups dysfunction (SSN injury) 3. Sups defect 4. SC tear 5. SC defect 6. Irreparable rotator cuff tear
Loadings Load pair Load pair without Sups force Load pair without Sups force Load pair Load pair Load pair without Sups force
Joint Positions 0 , 30 , 45 ABD 0 , 30 , 45 ABD 0 ABD* 0 , 30 , 45 ABD 0 , 30 , 45 ABD 0 , 30 , 45 ABD
ABD, abduction; SC, superior capsule; SSN, suprascapular nerve; Sups, supraspinatus. *The supraspinatus defect model was only tested at the 0 abduction because the insertion of the supraspinatus impinged on the undersurface of the acromion at higher degree abduction positions.
Superior Translation and Subacromial Peak Pressure Were Increased in the IRCT Compared with the intact joint model, the IRCT model notably increased the superior translation at 0 (by 3.0 mm; P < .001), 30 (by 2.1 mm; P < .001), and 45 (by 0.9 mm; P ¼ .007) of glenohumeral abduction and increased the subacromial peak pressure at 0 (by 0.68 MPa; P < .001) and 30 (by 0.30 MPa; P < .001) of glenohumeral abduction (Tables 2 and 3). The Supraspinatus, Rather Than the SC, Played a Primary Role in Preventing Superior Translation The supraspinatus defect model significantly increased the superior translation (by 2.6 mm; P < .001) and subacromial peak pressure (by 0.43 MPa; P ¼ .013) at 0 glenohumeral abduction compared with those of the intact joint model. Nevertheless, there were no significant differences in the superior translation or subacromial peak pressure between the supraspinatus defect model and the IRCT model (P > .05). The SC defect model unremarkably altered the superior translation at 0 (by 0.6 mm; P ¼ .582) and 45 (by 0.3 mm; P ¼ .867) of glenohumeral abduction and subacromial peak pressure at 0 (by 0.11 MPa; P ¼ .961), 30 (by -0.03 MPa; P ¼ .997), and 45 (by 0.33 MPa; P ¼ .485) of glenohumeral abduction. However, compared with the IRCT model, the SC defect model had notably smaller superior translation at 0 (by 2.4 mm; P < .001) and a significantly lower subacromial peak pressure at 0 (by 0.57 MPa; P < .001), 30 (by 0.33 MPa; P < .001), and 45 (by 0.71 MPa; P ¼ .004) of glenohumeral abduction (Tables 2 and 3). Mechanism of the Supraspinatus in Preventing Superior Translation The supraspinatus dysfunction model significantly increased the superior translation at 0 (by 1.7 mm; P < .001), 30 (by 1.2 mm; P ¼ .005), and 45 (by 0.8 mm; P ¼ .026) of glenohumeral abduction but not the subacromial peak pressure compared with those of
the intact joint model. The supraspinatus defect model significantly increased the superior translation (by 2.6 mm; P < .001) and subacromial peak pressure (by 0.43 MPa; P ¼ .013) at 0 glenohumeral abduction compared with those of the intact joint model. However, no significant differences were found between the supraspinatus defect model and supraspinatus dysfunction model in superior translation or subacromial peak pressure (all P > .05; Tables 2 and 3).
Discussion To identify the primary structure preventing superior translation of the humeral head, the results of the intact joint, supraspinatus defect, SC defect, and IRCT models were compared. The supraspinatus defect model facilitated superior translation of the humeral head at a larger scale than the SC defect model at 0 glenohumeral abduction (P < .001). At 30 glenohumeral abduction, although the SC defect model had a significantly larger superior translation than the intact joint model, the translation value in the SC defect model was not larger than that of the supraspinatus dysfunction model, in addition to the fact that the supraspinatus defect model did not present a smaller superior shift than the supraspinatus dysfunction model. In other words, the values of superior translation in the SC defect model were not larger than those of the supraspinatus defect model. Therefore, we conclude that the role of the supraspinatus may be more primary compared with that of the anatomic SC in preventing superior translation of the humeral head. Superior translation of the humeral head is restricted by several structures. It is reported that many muscles (e.g., latissimus dorsi, long head of biceps, infraspinatus) have a powerful capacity to depress the humeral head.18 Halder et al.18 reported that the supraspinatus could depress the humeral head by 2.0 1.4 mm, providing a minor superior stabilizing effect. In our study, the anatomic SC was weaker than the supraspinatus in superior stability. Therefore, the anatomic SC has a negligible role in preventing superior translation. The nature of SCR may not be a simple anatomic reconstruction of the SC. Another focus of the study was the mechanism of the supraspinatus in preventing the superior translation of the humeral head. In our study, 2 potential mechanisms were proposed and tested, the spacer effect and the tensional hammock effect. The spacer effect is the physical blocking of an object. In the human glenohumeral joint, subacromial tissue (e.g., the supraspinatus and the SC) blocked the humeral head from a superior shift. A good clinical application of the spacer effect is the InSpace balloon placed under the acromion in IRCT patients to prevent the superior translation of the humeral head.19-21
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Table 2. Superior Glenohumeral Translation Intact Joint Angle 0 30 45
Translation, mm 1.7 0.2* 1.3 0.1* 1.1 0.2*
Supraspinatus Dysfunction 95% CI 1.2-2.2 0.9-1.5 0.7-1.6
Translation, mm 3.4 0.6*y 2.5 0.5*y 1.9 0.3y
95% CI 1.9-4.8 1.3-3.6 1.1-2.7
Supraspinatus Defect Translation, mm 4.3 0.6y d d
95% CI 2.9-5.7 d d
Superior Capsule Tear Translation, mm 2.4 0.3* 2.3 0.3*y 1.3 0.1*
95% CI 1.6-3.1 1.6-3.0 1.1-1.5
Superior Capsule Defect Translation, mm 2.3 0.3* 2.5 0.4y 1.4 0.2
95% CI 1.6-3.1 1.6-3.4 0.9-1.9
Irreparable Rotator Cuff Tear Translation, mm 4.7 0.6y 3.4 0.5y 2.0 0.4y
95% CI 3.4-6.1 2.1-4.6 1.0-3.1
NOTE. Values are presented as the mean standard error and 95% CI (95% CI). CI, confidence interval. *A significant difference was found compared with the irreparable rotator cuff tear model (P < .05). y A significant difference was found compared with the intact joint model (P < .05).
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Table 3. Subacromial Peak Contact Pressure Intact Joint Glenohumeral Abduction Pressure, Mpa 0.45 0.08* 0 30 0.59 0.04* 45 1.10 0.21
Supraspinatus Dysfunction
Supraspinatus Defect
95% CI Pressure, Mpa 95% CI Pressure, Mpa 0.26-0.64 0.76 0.14* 0.42-1.10 0.88 0.14y 0.49-0.69 0.67 0.04* 0.57-0.76 0.59-1.61 0.74 0.02* 0.68-0.79 -
95% CI 0.56-1.20 -
NOTE. Values are presented as the mean standard error and 95% confidence interval (95% CI). *A significant difference was found compared with the irreparable rotator cuff tear model (P < .05). y A significant difference was found compared with the intact joint model (P < .05).
Superior Capsule Tear Pressure, Mpa 0.55 0.05* 0.60 0.04* 0.99 0.22
95% CI 0.44-0.67 0.52-0.69 0.48-1.50
Superior Capsule Defect Irreparable Rotator Cuff Tear Pressure, Mpa 0.56 0.03* 0.56 0.03* 0.77 0.14*
95% CI 0.49-0.63 0.49-0.64 0.45-1.10
Pressure, Mpa 1.13 0.13y 0.89 0.11y 1.48 0.04
95% CI 0.81-1.45 0.63-1.16 1.38-1.58
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The tensional hammock effect is another potential mechanism. The soft tissue (e.g., the supraspinatus and the SC) forms a “hammock” overlying the humeral head. When the humeral head shifts superiorly, the hammock is tensional and presses the humeral head downward. To identify the major mechanism of the supraspinatus in preventing the superior translation of the humeral head, the intact joint, supraspinatus dysfunction, and supraspinatus defect models were compared. In the intact joint model, the supraspinatus was loaded with 10 N. In the supraspinatus dysfunction model, although the supraspinatus was present, the load of the supraspinatus was removed, meaning the tensional property was gone. In the supraspinatus defect model, neither the spacer effect nor the tensional property of the supraspinatus was preserved. The supraspinatus dysfunction model demonstrated significant increases in superior translation, but not in subacromial peak pressure, at all abduction positions compared with the intact joint model. However, no notable increases were found in the superior translation or subacromial peak pressure in the supraspinatus defect model compared with those of the supraspinatus dysfunction model at 0 glenohumeral abduction. This result indicates that the tensional hammock effect of the supraspinatus may be more significant for preventing superior translation of the humeral head. It is noteworthy that Mura et al.22 conducted a similar cadaveric study on the rotator cuff, arriving at the opposite conclusion. They found that there were no differences in superior translation in the supraspinatus unload model (similar to the supraspinatus dysfunction model) and supraspinatus resection model (similar to the supraspinatus defect model) compared with the intact joint model (similar to the intact joint model). We believe this discrepancy could be attributed to some major differences in experimental methods. In Mura et al.’s experiment, the loading settings were 32 N for the infraspinatus-teres minor complex, 30 N for the subscapularis, and 16 N for the supraspinatus. The loadings for the infraspinatus-teres minor complex and subscapularis in Mura et al.’s study were 3 times those of our experiment; however, the loading for the supraspinatus was only 1.6 times that of our experiment. As was mentioned above, the supraspinatus might only play a minor role in the superior stabilization of the humeral head compared with the role of other muscles.18 The increased loads would enhance the stabilization function provided by the infraspinatus and subscapularis, further minimizing the contribution made by the supraspinatus. In addition, Mura et al. did not take the weight of the upper extremity into consideration, which possibly influenced the translation of the humeral head. In our experiment, we preserved the weight and length of the upper extremity to
7
simulate physiological conditions as much as possible.3-6 We believe that the specimen preparation and loading conditions exerted a significant influence on the results. Some clinical studies indicated that suprascapular nerve blocking would not increase superior translation at 0 and 30 shoulder abduction positions.23,24 It is undeniable that the interrelationships among various structures under physiological conditions make it difficult to study the function of a specific structure separately in an in vivo study. The force changes in other muscles after nerve blocking might easily compensate for the loss of the tensional effect of the supraspinatus. Failure to reflect changes of muscle forces in a timely and accurate fashion is a limitation of our biomechanical study. Our results indicated that it is the supraspinatus rather than the SC that plays a primary role in preventing superior translation of the humeral head. Therefore, the nature of SCR may not be simple anatomic reconstruction. Clinical studies indicated that SCR successfully decreased pain and improved function in IRCT patients.7,25-27 Patients undergoing the surgery were able to resume recreational sports and physical work.26 The successful clinical results are seemingly contradictory to our biomechanical findings. Possible explanations for these contradictory results are as follows: First, the dermal allograft used in SCR had a thickness ranging from 3 to 8 mm, greater than that of the SC.7,28-34 The graft might display a spacer effect. The biomechanical study of Mihata et al.6 confirmed that an 8 mm thick fascia lata provided better stability in SCR than a 4 mm thick graft. Second, the tensional fixation technique in SCR alters the biomechanical properties of the graft. In SCR, the graft is attached at 30 glenohumeral abduction. This fixation procedure results in a nonanatomic functional restraint.11 According to Mihata et al.’s study, fixing the graft at 30 glenohumeral abduction gave a smaller superior translation of the humeral head and subacromial contact pressure than fixation at 10 glenohumeral abduction. Thus, SCR may not be a simple anatomic reconstruction of the SC, but rather a functional modification of the graft. The choice of the graft and tensional fixation technique may be important for surgery and should be studied in the future. Two clinical scenarios were proposed by Adams et al. in the review “The Rotator Cuff and the Superior Capsule: Why We Need Both.”10 The first scenario was described in a patient who had a suprascapular nerve injury with an intact rotator cuff. The patient was able to abduct and manage overhead movements despite a loss of 75% of strength due to nerve dysfunction.35 Adams et al.,10 therefore, believed that the preserved abduction and overhead movements were due to static stabilization provided by the SC.10
8
Q. HU ET AL.
First, the superior translation of the humeral head is the collective result of several forces. The infraspinatus, long head of biceps, and latissimus dorsi all play important roles in humeral head depression.18 It cannot be ruled out that the forces of the aforementioned 3 muscles might be altered after nerve blocking.24 The altered muscle forces profile has the potential to stabilize the humeral head and also explain why the patient could manage overhead movements after nerve blocking. Second, our study demonstrated that the SC had a negligible role in the superior stability of the glenohumeral joint. On the one hand, the SC tear and SC defect models did not significantly increase the superior translation of the humeral head compared with the intact joint model. On the other hand, the SC could not prevent superior translation in the supraspinatus dysfunction model or supraspinatus defect model. Therefore, the preserved function in suprascapular nerve injury should not be attributed to an intact SC. The other clinical scenario was in a patient with a massive rotator cuff tear with grade 3 or 4 fatty infiltration. Adams et al.10 noted that preoperative restricted active range of motion (ROM) or even pseudoparalysis was improved after surgery, without change of the muscle appearance on postoperative MRI. They believed that the restoration of the capsular anatomy contributed to the normal biomechanics and improved the clinical functions.10 However, their proposition was far from convincing. First, pseudoparalysis is a phenomenon rife with controversies. Pseudoparalysis was recently defined as the loss of total active ROM that cannot recover even after subacromial analgesia.36 The studies referred to in Adams et al.’s review did not mention subacromial analgesia, which means some participants recruited in the studies were not pseudoparalysis cases from a strict perspective.37,38 An active ROM below 90 is called pseudoparesis.36 The large heterogeneity in the inclusion criteria made it difficult to determine whether the loss of active ROM was due to mechanical reasons, pain, or both. In addition, arthroscopic surgery relieved pain to some extent. According to Gerber et al.,37 the pain points increased from 7.6 (pain) to 14.4 (no pain) after arthroscopy. Denard et al.38 also reported that patients with pseudoparalysis experienced pain relief from 5.7 (pain) to 1.1 (no pain) based on the visual analog scale. It is unreasonable to exclude the effect of pain relief. Therefore, what Adams et al. proposed is a complex problem that cannot be simply explained by the function of the SC. Limitations There are some limitations in our work. First, we could not avoid the intrinsic defects of biomechanical studies. This was a static biomechanical study, and the muscle loads were set on the basis of previous research.
We could not simulate all of the physiological load patterns of the shoulder joint. Second, in our IRCT model, we only removed the supraspinatus and SC. Although the modeling techniques were similar to those of previous studies, in clinical scenarios, more tendon injuries may be involved in IRCT, especially in massive IRCT. Third, we did not consider the gravitational effects of blood in the specimens. Fourth, we set the measurement positions at 0 , 30 , and 45 rather than 0 , 30 , and 60 because the laser beam would be blocked by the deltoid muscles when the abduction degree was higher.
Conclusions The anatomic SC has a negligible role in preventing the superior translation of the humeral head.
References 1. Wieser K, Rahm S, Schubert M, et al. Fluoroscopic, magnetic resonance imaging, and electrophysiologic assessment of shoulders with massive tears of the rotator cuff. J Shoulder Elbow Surg 2015;24:288-294. 2. Goutallier D, Le Guilloux P, Postel JM, Radier C, Bernageau J, Zilber S. Acromio humeral distance less than six millimeter: Its meaning in full-thickness rotator cuff tear. Orthop Traumatol Surg Res 2011;97:246-251. 3. Mihata T, McGarry MH, Pirolo JM, Kinoshita M, Lee TQ. Superior capsule reconstruction to restore superior stability in irreparable rotator cuff tears: A biomechanical cadaveric study. Am J Sports Med 2012;40:2248-2255. 4. Mihata T, McGarry MH, Kahn T, Goldberg I, Neo M, Lee TQ. Biomechanical role of capsular continuity in superior capsule reconstruction for irreparable tears of the supraspinatus tendon. Am J Sports Med 2016;44: 1423-1430. 5. Mihata T, McGarry MH, Kahn T, Goldberg I, Neo M, Lee TQ. Biomechanical effects of acromioplasty on superior capsule reconstruction for irreparable supraspinatus tendon tears. Am J Sports Med 2016;44:191-197. 6. Mihata T, McGarry MH, Kahn T, Goldberg I, Neo M, Lee TQ. Biomechanical effect of thickness and tension of fascia lata graft on glenohumeral stability for superior capsule reconstruction in irreparable supraspinatus tears. Arthroscopy 2016;32:418-426. 7. Mihata T, Lee TQ, Watanabe C, et al. Clinical results of arthroscopic superior capsule reconstruction for irreparable rotator cuff tears. Arthroscopy 2013;29:459-470. 8. Mihata T, Lee TQ. Clinical outcomes of superior capsule reconstruction for irreparable rotator cuff tears without osteoarthritis in the glenohumeral joint. J Shoulder Elbow Surg 2015;24:e107-e109. 9. Ishihara Y, Mihata T, Tamboli M, et al. Role of the superior shoulder capsule in passive stability of the glenohumeral joint. J Shoulder Elbow Surg 2014;23:642-648. 10. Adams CR, DeMartino AM, Rego G, Denard PJ, Burkhart SS. The rotator cuff and the superior capsule: Why we need both. Arthroscopy 2016;32:2628-2637. 11. Verma NN, Lubowitz JH, Brand JC, Provencher MT, Rossi MJ. Could disruption of the shoulder superior
BIOMECHANICS OF SUPERIOR CAPSULE
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
capsule be the “essential lesion” of rotator cuff disease? Possibly, but questions remain .. Arthroscopy 2016;32: 2421-2423. Omid R, Heckmann N, Wang L, McGarry MH, Vangsness CT Jr, Lee TQ. Biomechanical comparison between the trapezius transfer and latissimus transfer for irreparable posterosuperior rotator cuff tears. J Shoulder Elbow Surg 2015;24:1635-1643. Akagi R, Kanehisa H, Kawakami Y, Fukunaga T. Establishing a new index of muscle cross-sectional area and its relationship with isometric muscle strength. J Strength Cond Res 2008;22:82-87. Veeger HE, Van der Helm FC, Van der Woude LH, Pronk GM, Rozendal RH. Inertia and muscle contraction parameters for musculoskeletal modelling of the shoulder mechanism. J Biomech 1991;24:615-629. Takahashi T, Wada Y, Yamamoto H. Soft-tissue balancing with pressure distribution during total knee arthroplasty. J Bone Joint Surg Br 1997;79:235-239. Yildiz KI, Isik C, Tecimel O, et al. Use of contact pressuresensitive surfaces as an indicator of graft tension in medial patellofemoral ligament reconstruction. Arch Orthop Trauma Surg 2013;133:1657-1663. Hille E, Schulitz KP, Henrichs C, Schneider T. Pressure and contract-surface measurements within the femoropatellar joint and their variations following lateral release. Arch Orthop Trauma Surg 1985;104:275-282. Halder AM, Zhao KD, Odriscoll SW, Morrey BF, An KN. Dynamic contributions to superior shoulder stability. J Orthop Res 2001;19:206-212. Anley CM, Chan SK, Snow M. Arthroscopic treatment options for irreparable rotator cuff tears of the shoulder. World J Orthop 2014;5:557-565. Savarese E, Romeo R. New solution for massive, irreparable rotator cuff tears: The subacromial "biodegradable spacer.". Arthrosc Tech 2012;1:e69-e74. Szollosy G, Rosso C, Fogerty S, Petkin K, Lafosse L. Subacromial spacer placement for protection of rotator cuff repair. Arthrosc Tech 2014;3:e605-e609. Mura N, O’Driscoll SW, Zobitz ME, et al. The effect of infraspinatus disruption on glenohumeral torque and superior migration of the humeral head: A biomechanical study. J Shoulder Elbow Surg 2003;12:179-184. Werner CM, Weishaupt D, Blumenthal S, Curt A, Favre P, Gerber C. Effect of experimental suprascapular nerve block on active glenohumeral translations in vivo. J Orthop Res 2006;24:491-500. San Juan JG, Kosek P, Karduna AR. Humeral head translation after a suprascapular nerve block. J Appl Biomech 2013;29:371-379. Denard PJ, Brady PC, Adams CR, Tokish JM, Burkhart SS. Preliminary results of arthroscopic superior capsule
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
9
reconstruction with dermal allograft. Arthroscopy 2018;34: 93-99. Mihata T, Lee TQ, Fukunishi K, et al. Return to sports and physical work after arthroscopic superior capsule reconstruction among patients with irreparable rotator cuff tears. Am J Sports Med 2018:363546517753387. Pennington WT, Bartz BA, Pauli JM, Walker CE, Schmidt W. Arthroscopic superior capsular reconstruction with acellular dermal allograft for the treatment of massive irreparable rotator cuff tears: Short-term clinical outcomes and the radiographic parameter of superior capsular distance. Arthroscopy 2018;34:1764-1773. Sutter EG, Godin JA, Garrigues GE. All-arthroscopic superior shoulder capsule reconstruction with partial rotator cuff repair. Orthopedics 2017;40:e735-e738. Shishani Y, Flocken J, Gobezie R. Superior capsular reconstruction: An alternative approach to treat contained cuff tear arthropathy. Sem Arthroplasty 2016;27: 112-116. Sanchez G, Rossy WH, Lavery KP, et al. Arthroscopic superior capsule reconstruction technique in the setting of a massive, irreparable rotator cuff tear. Arthrosc Tech 2017;6:e1399-e1404. Petri M, Greenspoon JA, Millett PJ. Arthroscopic superior capsule reconstruction for irreparable rotator cuff tears. Arthrosc Tech 2015;4:e751-e755. Adams CR, Denard PJ, Brady PC, Hartzler RU, Burkhart SS. The arthroscopic superior capsular reconstruction. Am J Orthop (Belle Mead, N.J.) 2016;45:320-324. Burkhart SS, Denard PJ, Adams CR, Brady PC, Hartzler RU. Arthroscopic superior capsular reconstruction for massive irreparable rotator cuff repair. Arthrosc Tech 2016;5:e1407-e1418. Itoi E, Grabowski JJ, Morrey BF, An KN. Capsular properties of the shoulder. Tohoku J Exp Med 1993;171: 203-210. Gerber C, Blumenthal S, Curt A, Werner CM. Effect of selective experimental suprascapular nerve block on abduction and external rotation strength of the shoulder. J Shoulder Elbow Surg 2007;16:815-820. Tokish JM, Alexander TC, Kissenberth MJ, Hawkins RJ. Pseudoparalysis: A systematic review of term definitions, treatment approaches, and outcomes of management techniques. J Shoulder Elbow Surg 2017;26:e177-e187. Gerber C, Fuchs B, Hodler J. The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am 2000;82:505-515. Denard PJ, Ladermann A, Brady PC, et al. Pseudoparalysis from a massive rotator cuff tear is reliably reversed with an arthroscopic rotator cuff repair in patients without preoperative glenohumeral arthritis. Am J Sports Med 2015;43:2373-2378.