1 Introduction

The intact shoulder joint has been described as a perfect compromise between mobility and stability.¹ The discrepancy between the size of the humeral head and the glenoid fossa (“ball and socket joint”²) creates a wide range of motion³ and effective dynamic and static stabilizers are crucial to provide stability.⁴

The muscles of the rotator cuff dynamically stabilize the shoulder joint by three mechanisms: compression of the humeral head into the glenoid fossa (“cavity compression”), pretension of the articular capsule via force transmission through tendinous attachments, and muscular balance (“muscle patterning).⁵ Static stabilizers include the intact bony configuration of the humeral head and glenoid, the glenoid labrum, the articular capsule and the glenohumeral ligaments that reinforce the articular capsule.^5,6 The specific configuration of the shoulder joint allows for extreme range of motion and can be of great advantage in certain athletic disciplines like throwing or gymnastics.^3,7,8 On the other hand, glenohumeral instability and impingement are well described conditions in overhead athletes with maximum range of external rotation prior to the throwing motion.⁹

With one of the stabilizing components injured, the complex becomes biomechanically imbalanced and, depending on the amount of injury, instability results. Injury to the static stabilizers after a traumatic first-time dislocation is very likely, particularly in active young patients (under 24 years of age), in whom a Bankart lesion (antero-inferior labrum lesion) must be expected in up to 97% of the cases.¹⁰ Bony lesions of the postero-lateral humeral head (Hill-Sachs lesion) can be found in up to 100%^11,12 and glenoid bone loss was described to occur in 22% after a traumatic first-time dislocation, becoming even more likely with repetitive events of dislocation.^11–13 The risk of an injury of the rotator cuff muscles (dynamic stabilizers) was reported to be between seven and 32% and rises with age related tendon degeneration prior to the injury.¹⁴ The majority of these injuries can be easily verified with the help of magnetic resonance imaging (MRI).

Capsule laxity is another important aspect that has been described for patients with recurrent shoulder instability^7,15,16; however, MRI or even arthrography might not be sufficient diagnostic tools due to a highly variable anatomy and a bursa of varying size and shape surrounding the coracoid process.¹⁷ As capsule elongation is assumed to weaken the static stability of the shoulder joint, the purpose of this biomechanical study was to demonstrate that capsule elongation occurs immediately after a first-time shoulder dislocation and not just after recurrent dislocation events. We hypothesize an increment in joint clearance due to joint capsule elongation after a first-time dislocation.

2 Material and methods

An experimental in-vitro study was conducted on 6 paired fresh frozen human shoulders (4 females; 2 males; 12 specimen). This study was approved by the research ethics committee.

The mean donor data was as follows: an age of 80 (SD ± 7.5, Range 67–89) years, a height of 164 ± 14 cm, a weight of 55 ± 12 kg, and a body mass index of 21 ± 5 kg/m². The authors received a complete donor report including the medical history of each specimen. Exclusion criteria were a history of injury or surgery to the shoulder, cancer/metastasis related to the shoulder region and connective tissue disorders. Prior to dissection, all specimens had plain radiographs to confirm a centered humeral head position and to detect bony lesions.

2.2

2.2 Testing

2.2.1

2.2.1 Experimental technique

The following steps were undertaken to simulate a standardized first-time antero-inferior shoulder dislocation of each shoulder joint:

The scapula was fixated to the surgery table with a metal clamp. In the start position, a static tension force of 2.5 N was applied to the humerus via a custom-made Force Gauge (Macro-Line, Pesola, Switzerland) in an antero-inferior direction to create moderate pre-tensioning of the capsule. To simulate the first-time dislocation, a slow, continuous antero-inferior force was manually applied by one of the investigators (blinded for review) until the humeral head dislocated from its centered position into a dislocated position anterior to the inferior aspect of the glenoid (Fig. 1). The dislocation was performed manually in order to move the humeral head with a minimum force. The dislocated humeral head position was confirmed by antero-posterior radiographs. The head of the humerus was immediately returned back to the starting position and a static tensile force of 2.5 N was applied again. During dislocation and reduction capsule deformation was visualized with an optical measurement system (PONTOS- GOM – Gesellschaft für Optische Messtechnik mbH, Germany) and radiographs (MOBILETT Elara Max, Siemens Healthcare GmbH, Germany) were undertaken to investigate the position and gap of the humeral head in the glenoid fossa.

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Fig. 1 Demonstration of a dissected right shoulder prior to dislocation (A) and at the timepoint of a simulated dislocation (B). A = joint capsule; B = spina scapula with optical markers moulded in a synthetic resin; C = humeral bone with optical markers; D = musculus (m.) subscapularis; E = m. Pectoralis minor and short head of biceps; F = long head of biceps.

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2.2.2

2.2.2 Radiographic examinations with determination of the joint gap

A metal sphere with a diameter of 25 mm served as a reference object. An antero-posterior radiograph was undertaken prior to dislocation and after reduction. The joint gap was assessed using the Autodesk Inventor 2021 Software system (Autodesk Inc., USA). Therefore, radiographs were imported in a jpeg format into the software system. A best fit circle was drawn on the glenoid fossa and the humeral head. The distance between both circle centers (prior to dislocation and after reduction) was then measured and interpretated as the joint gap.

2.2.3

2.2.3 Joint capsule deformation and digital image correlation (DIC)

The measurement of the joint capsule deformation between scapula and humerus was assessed using optical, camera-based measurement techniques (PONTOS- GOM – Gesellschaft für Optische Messtechnik mbH, Braunschweig, Germany).¹⁸ Bone markers were applied to the scapula and humeral bone in a standardized fashion (Fig. 1) and the three-dimensional motions between the markers were recorded. The deformation was calculated from the 3-dimensional (3D) length changes between the optical markers. For this purpose, the length change delta L (μm) at the individual measurement times was divided by the initial length L0 (m) and the result was expressed as a percent. After radiographic and optical measurements, the capsule tissue was removed and the joint was evaluated for signs of labrum or bony lesions.

3 Results

The capsule was critically evaluated before and after a simulated first-time antero-inferior shoulder dislocation by two independent examiners. One examiner was a certified shoulder and elbow surgeon and the other one was an experienced biomechanical engineer who professionally works in the field of orthopaedic research.

In all cases the capsule was intact prior to dislocation of the humeral head. In one case, a tear of the posterior capsule occurred during the dislocation maneuver. In all other cases, the capsule remained intact. After radiographic and optical measurements, the capsule was removed and no cases of labrum lesions (Bankart lesion) or bony lesions (fractures, Hill-Sachs impression) were identified.

3.1

3.1 Radiographic joint gap

The t-test revealed a statistically significant increment of the radiographic joint gap at the time point of joint reduction 18.1 ± 6.5 mm, t (11) = −5.655 compared to the joint gap size prior to dislocation (13.7 ± 6.9 mm) (p < .001). The increase in joint clearance was 4.4 mm (Fig. 2).

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Fig. 2 Increment of the radiographic joint gap: the radiographic joint gap increased from prior to a simulated dislocation (A) (13.7 ± 6.9 mm) to 18.1 ± 6.5 mm at the time point of joint reduction (B) (p < .001). The mean increase in joint clearance was 4.4 mm.

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3.2

3.2 Capsule elongation

The Wilcoxon signed rank test revealed statistically significant difference in joint capsule elongation. Capsule elongation increased from 5.9 ± 0.005 % (prior to dislocation) to 9.4 ± 0.007 %, z = −9.506 in the reduced joint position (p < .001). The mean increase in joint capsule elongation was 3.5 % (Fig. 3).

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Fig. 3 Capsule elongation: Capsule elongation increased from 5.9 ± 0.005 % (prior to dislocation) (A) to 9.4 ± 0.007 %, z = −9.506 in the reduced joint position (B) (p < .001). The mean increase in joint capsule elongation was 3.5 %.

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4 Discussion

The most important finding of this study was that the centered position of the humeral head in the glenoid fossa before the event of a first-time antero-inferior dislocation, simulated with inferior tension force, was different from the humeral head position after reduction. A statistically significant increment of the radiographic joint gap at the timepoint of joint reduction 18.1 ± 6.5 mm, t (11) = −5.655 compared to the joint gap size prior to dislocation (13.7 ± 6.9 mm) (p < .001) was found. The total increase of joint clearance was 4.4 mm. This result was interpreted as an indirect proof of capsule elongation, as in all but one case, the joint capsule remained intact.

Moreover, a statistically significant difference in joint capsule elongation was detected with an optical, camera-based measurement technique. Capsule elongation increased from 5.9 ± 0.005 % (prior to dislocation) to 9.4 ± 0.007 %, z = −9.506 in the reduced joint position (p < .001). The mean increase in joint capsule elongation was 3.5 % and was interpreted as a direct proof of capsule elongation.

With these results it was demonstrated that the shoulder capsule elongates after just one single controlled first-time shoulder dislocation in an in-vitro situation. The typical mechanism of a first-time traumatic shoulder dislocation in-vivo however, would be a fall or hit on the externally rotated and abducted arm.⁵ In this case the impact forces upon the shoulder joint would be even higher, resulting in increased stress to the shoulder capsule. Based on the current study results, the authors postulate that the shoulder capsule gets at least elongated (or even torn) during a first-time traumatic dislocation in-vivo.

Since there is a probability of up to 97% for a labrum tear after a first-time traumatic shoulder dislocation¹⁰ and given the results of the current study, it may further be assumed that injury to the shoulder occurs always after a first-time traumatic dislocation. This is even the case if magnetic resonance imaging (MRI) does not demonstrate any typical signs of injury (like a Bankart lesion) because MRI or even arthrography are not sufficient diagnostic tools for capsule injuries due to highly variable anatomy and a bursa of varying size and shape surrounding the coracoid process.¹⁷ This observation might be of importance if a surgeon wants to prescribe physiotherapy treatment and needs justification in front of the patient's health insurance.

Elongation of parts of the capsule has been previously demonstrated in an experimental study by Rainis et al..²⁰ The study group investigated changes in the microstructure of inferior glenohumeral ligaments (IGHL) after a simulated dislocation. In detail, the stiffness and material properties of six cadaveric samples of inferior glenohumeral ligaments (IGHL) were examined during a simulated ligament elongation. The IGHL was elongated to a maximum extend (mean 12.7%) which resulted in a 2.5% (mean) non-recoverable strain. Specimens were younger than the specimens tested in this study (57 ± 8 years versus 80 ± 7.5 years). However, increases in region stiffness and changes in stress-stretch curves were found and supported the hypothesis, that changes in the capsular tissue microstructure occurs following simulated injury.²⁰

The clinical relevance of capsule integrity remains not fully understood, however, some physiological facts implicate the importance of an intact capsule for the shoulder function. The articular capsule of the shoulder appears to be extremely lax in comparison to other joint capsules of the human body²¹ which allows for an extreme range of motion and can be of great advantage in certain athletic disciplines like throwing or gymnastics.^3,7,8 The capsule is supported by the tendons of the rotator cuff muscles and the glenohumeral ligaments (inferior glenohumeral ligament (IGHL), superior glenohumeral ligament (SGHL), middle glenohumeral ligament (MGHL).⁵ Capsular and synovial tissues are innervated, which is an important aspect for active protection of the capsule and the attached ligaments by reflex control of the rotator cuff muscles.²¹ A deficient capsule provides inferior stability due to a decrease in intraarticular pressure.⁶ Excessive external rotational stretching of the capsule was demonstrated to result in elongation of the attached glenohumeral ligaments and causes an increase in glenohumeral translation and external rotation.²² Shoulder pain, glenohumeral impingement and instability are well described conditions in overhead athletes with maximum range of external rotation prior to the throwing motion.⁹ On the other hand, capsule stiffness as present in frozen shoulders, after trauma or long-term immobility leads to an enormous restriction of shoulder mobility through thickening and shrinking of the capsule.²³

Given the knowledge about capsule tissue innervation and its proprioceptive function within the reflex control circle²¹ the authors of this article aim to create awareness amongst physicians and physiotherapists for the elongated or even torn capsule of patients and especially athletes after first-time dislocations and also after sub-dislocations.^24,25 Parallels to the importance of proprioceptive training after injury of ligaments and capsular tissue can be found in the literature for the entity of ankle sprains, where the positive effects of proprioception training (increase of dynamic neuromuscular control, postural sway, and joint position sense) are well described.²⁶ Proprioceptive training after a first-time shoulder dislocation is therefore recommended by the authors of this study, however, further clinical follow-up is needed to support this thesis.

While functional training after shoulder dislocation seems to be a logical conclusion with a low risk of negative effects, the need for immobilization remains a matter of controversy. Immobilization of the shoulder with a sling for three to four weeks is a common recommendation²⁷ and is followed by many physicians despite the knowledge that recurrence rates, which are especially high in patients under the age of 25 years,²⁸ are most likely not influenced by the duration of immobilization.^28,29 Among others, Hovelius et al.^28,30 observed that patients who removed the immobilization sling once they felt comfortable enough, did not have higher recurrence rates compared to patients who were immobilized for several weeks. It remains unclear, whether temporary immobilization is advantageous and if capsule elongation is reversible over time at all. It further remains unclear, if immobilization supports posttraumatic capsule stiffness and therefore prevents recurrent dislocations. To answer the question of reversibility, further examination of capsular collagen fiber kinematics will be necessary.²⁰

To our best knowledge there is a lack of studies investigating capsule elongation after first-time dislocation, which was the motivation for this study. Throughout the literature it has been demonstrated multiple times that the shoulder capsule elongates after a dislocation and keeps elongating with repetitive dislocations,³¹ however, these statements result from investigations on multidirectional instability cases³² and studies with heterogeneous cohorts.^15,16 While there are several limitations to this biomechanical basic science study the strength is that it shows capsule elongation of human shoulders in a controlled setting, demonstrating the pure effect of the dislocated head on the capsule tissue.

In further biomechanical studies it could be beneficial to investigate capsule elongation of younger cadaveric specimen with and without an intact rotator cuff. The authors of this article further recommend future studies on capsule recovery via modern MRI and histopathological investigations over time.

5 Limitations

This study was conducted on cadaveric shoulders in which less quality of capsule tissue is expected than in patients. Specimens had an older (biological) age than the typical patient with first-time traumatic shoulder dislocation and therefore age-related capsuloligamentous degeneration must be expected. The static stabilizers were observed isolated from the dynamic stabilizers of the shoulder joint (muscles), so it was not tested under in-vivo conditions. No high impact force was used to simulate a true “traumatic” first-time shoulder dislocation since the goal was to investigate the isolated effect of a dislocated humeral head position on the capsule as the minimal effect that occurs after a dislocation event. No microscopic or histological investigations were undertaken and it remains unknown, whether there was any history of connective tissue disorder (such as Elhers-Danlos Syndrome) or general hyperlaxity in the tested specimens. The (theoretically possible) recovery of the capsule tissue over time was no subject of this investigation due to the character of an in-vivo study on cadavers.

6 Conclusions

Capsule elongation was observed immediately after a simulated first-time shoulder dislocation in an in-vitro model of elderly human cadavers. It might therefore not only be a phenomenon of recurrent dislocation events.

Conduction of experimental work

The experimental work was conducted at the Laboratory of Biomechanics and Implant Research, Department of Orthopaedics, Heidelberg University Hospital, Schlierbacher Landstraβe 200a, 69118 Heidelberg Germany.

Ethics approval and consent to participate

Institutional review board approval was obtained prior to the start of the study; Ethical Commission, University Clinic of Heidelberg (S-077/2022). The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Funding

Anna-Katharina Nolte, as the corresponding author, Benjamin Panzram, Matthias Bülhoff and Sebastian Jäger, as Co-authors, received financial support by the University Clinic of Heidelberg (research support for researches employed by the University Clinic of Heidelberg) for this project. No financial support from an external organization was granted.

Consent for participation in the study

Not applicable.

CRediT authorship contribution statement

Anna-Katharina Nolte: Conceptualization, Methodology, of the work, Substantial contribution to the acquisition of data for the work, Substantial contribution to the interpretation of data of the work, Writing – original draft, preparation, final approval of the version to be published, Investigation. Sebastian Jager: Methodology, of the work, Formal analysis, Writing – original draft, preparation, final approval of the version to be published, Investigation. Maxime Marie Seifert: Substantial contribution to the acquisition of data for the work, final approval of the version to be published, Investigation. Matthias Bulhoff: Supervision, of the work, Writing – review & editing, final approval of the version to be published, Investigation. Marcus Schiltenwolf: Supervision, of the work, Writing – review & editing, final approval of the version to be published, Investigation. Mareike Schonhoff: Substantial contribution to the acquisition of data for the work, final approval of the version to be published, Investigation. Patric Raiss: Formal analysis, Substantial contribution to the interpretation of data for the work, Writing – review & editing, final approval of the version to be published, Investigation. Tobias Renkawitz: Supervision, Writing – review & editing, final approval of the version to be published, Investigation. J. Philippe Kretzer: Substantial contribution to the interpretation of data for the work, Formal analysis, Writing – review & editing, Supervision, final approval of the version to be published, Investigation. Benjamin Panzram: Supervision, of the work, Writing – review & editing, final approval of the version to be published, Investigation.