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The frozen shoulder - Introduction to Pathology

EBP Module
Updated
8/21/2024
Fullphysio
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Foreword

Frozen shoulder is a shoulder disorder that is frequently encountered but is still the subject of numerous uncertainties and inconsistencies in the literature. The main causes of confusion related to retractile capsulitis stem from a disagreement about how to name this pathology, classify it, and describe its natural history (Abrassart et al. 2020). In general, it is characterized by a gradual increase in spontaneous pain and a limitation in the range of movements of the glenohumeral joint (Kingston et al., 2018). Management strategies vary according to the degree of irritability, the stage of development of the pathology, and the therapist's preferences.

1 - Introduction to pathology

a - Anatomical reminders

At first, it may be appropriate to recall some notions of anatomy, in particular concerning the various structures likely to be involved in retractile capsulitis.

‍1 - The joint capsule

This fibrous structure contains numerous joint elements. The presence of joint capsules is generally observed within mobile joints (diarthrosis).

It is characterized in particular by its elasticity allowing movement and by its resistance allowing a certain passive stability of the articular surfaces between them.

The glenohumeral joint capsule has thick reinforcements called glenohumeral (superior, middle and inferior) and coracohumeral ligaments (Ferrari et al. 1990). The volume of this capsule would be on average 20 mL under healthy conditions (Kraal et al., 2020).

Moreover, due to its location, it is in close relationship with the tendons of the cuff muscles, with which it intertwines its fibers, forming a fibrous musculotendinous sleeve (Drake et al. 2006; Clark et al. 2006; Clark et al. 2006; Clark et al. 1990; Pearsall et al. 2000).

This fibrous fusion has both a proprioceptive and mechanical role (distribution of the stresses of the cuff muscles and the prevention of possible tendon injuries at the level of their entheses) (Di Giacomo et al. 2008).

Overall, the joint capsule has the following 3 tissue layers (from surface to depth) (McFarland et al. 2002):

‱ A tough connective layer rich in collagen
‍
‱ A loose connective layer
‍
‱ A synovial membrane, a structure that secretes the eponymous liquid. It lubricates and nourishes joint surfaces.

Finally, it is important to remember that this capsule is innervated by the articular branches of the suprascapular and axillary nerves and that it is well vascularized (Andary et al. 2002, Eckmann et al., 2017).

At the level of the shoulder joint capsule, the axillary pouch represents an entity of interest in the physiopathology of capsulitis. This corresponds to the glenohumeral capsule in its lower part and is delimited by the anterior and posterior bands of the inferior glenohumeral ligaments (Fields et al., 2019). As we will see later, the latter makes it possible, during arthroscopic evaluations, to determine a certain grade of capsulitis since this fold is generally reduced (The Shoulder Made Easy, 2019).

2 - The rotator interval

The rotator interval represents two triangular-shaped capsular areas that are characterized by the absence of reinforcement by the rotator cuff tendons (Le Corroller et al., 2007). While an anterior rotator interval and a posterior rotator interval could be defined, it is commonly accepted that when talking about the rotator interval, we are referring to the anterior rotator interval (Fields et al., 2019).

The latter entity forms an anatomical triangular space through the upper edge of the subscapular muscle tendon at the bottom, the anterior edge of the supraspinatus tendon at the top, the base of the coracoid process medially and the transverse humeral ligament laterally (Le Corroller et al. 2007).

This interval is closed superficially by an extension of the anterior glenohumeral joint capsule called the “rotator interval capsule” (Woertler, 2015). The latter includes the intertwining of fibers from the subscapular and supraspinous tendons, by the superior glenohumeral ligament as well as by the coracohumeral ligament (LCH). Conversely, the floor of this space consists mainly of the articular cartilage of the humeral head (Fields et al., 2019).

Note that the tendon of the long portion of the biceps brachii and the superior glenohumeral ligament (LGHS) cross the rotator interval (Le Corroller et al. 2007).

While the role of the rotator interval has not yet been fully defined, it seems clear that the rotator interval has a structural role in stabilizing dynamic shoulder movements (Fields et al., 2019). Thus, for some authors (Le Corroller et al., 2007), this interval would have 3 main roles:

  • Maintaining negative intra-articular pressure
    ‍
  • A pulley role for the tendon of the long biceps laterally
    ‍
  • Posterior and inferior stabilization of the humeral head

As a result, the experimental section of the LCH and the rotator interval capsule could lead to a destabilization of the biceps pulley (Fields et al., 2019) as well as a risk of inferior and posterior instability/dislocation (Fields et al., 2019; Harryman et al., 1992).

Moreover, this interval allows the limitation of translations:

  • Posteriors and inferiors in adduction
    ‍
  • Anterior in abduction and lateral rotation

This is why some authors indicate that the latter would present a key role in the pathogenesis of capsulitis, but also in multidirectional instability (Bain et al., 2017)

‍

3 - The coracohumeral ligament

The coracohumeral ligament (LCH) has been described as originating on the outer edge of the horizontal branch of the coracoid process and ending in a bundle on the anterior edge of the supra spinatus and the major tubercle while the second bundle terminates at the level of the minor tubercle. Note some insertions attaching to the upper fibers of the subscapular as well as to the transverse humeral ligament. Because of its path, it covers the rotator interval (Fields et al., 2019).

This ligament can be put under maximum tension during the external rotational movement (Le et al., 2017).

Functionally, the LCH has several roles:

  • Formation of the “long biceps pulley” with the superior glenohumeral ligament (Fields et al., 2019).
    ‍
  • Passive limitation of lateral rotation, especially when arming with the arm (Fields et al., 2019). Conversely, the ligament is relaxed in an internal adduction-rotation position (Woertler, 2015).
    ‍
  • postero-inferior stabilizer of the humeral head (LCH couple and superior glenohumeral ligament).
    ‍
  • Humeral head suspensor (Dufour et al. 2014).
    ‍
  • Protection of the long biceps tendons from the acromio-coracoid ligament (Corroler et al. 2007).
    ‍
  • Protection of the subscapular from the coracoid process or even the minor tubercle (Corroler et al. 2007).

Note that for some authors, the coracohumeral ligament cannot be detached from the superior glenohumeral ligament since they constitute a functional unit in the stability of the rotator interval (Petchprapa et al., 2010; Woertler, 2015).

‍

4 - The rotator cuff

The rotator cuff is a group of muscles and tendons that surround the shoulder joint. According to the latest data on the subject (Akhtar et al., 2021), the muscles that make up the rotator cuff are four in number:

  • The supraspinatus: originating in the supraspinous fossa, it is directed to the superior and medial surface of the trochiter.
    ‍
  • The infraspinatus: originating in the infraspinous fossa, it goes to the inferior and medial face of the trochiter. The latter has a tendon with the widest section of the four cuff tendons.
    ‍
  • The small circle: having its origin in the infraspinous fossa, it goes on the inferior and medial face of the trochiter.
    ‍
  • The subscapular: having its origin in the subscapular fossa, it goes over the trochin.

It should be noted that the first three muscles mentioned form digitations in order to form a continuous structure proximal to the humerus: the rotator cable (Pallot & Morichon, 2013; Rahu et al., 2017). For its part, the subscapular is increasingly linked to capsulitis through numerous studies showing the presence of trigger points in it in patients with capsulitis (Arjun & Rajaseker, 2021).

To these four muscles, some authors add the long head of the biceps, although this concept is not adopted unanimously (Redondo-Alonzo et al, 2014).

Regarding their roles, the main mission of the rotator cuff is to stabilize the humeral head during shoulder movements. In fact, by its action, the cuff creates a force torque in order to prevent any proximal “migration” of the humerus. Apart from their stabilizing role, these muscles have their own action:

  • The supraspinatus muscle participates in shoulder abduction, an action shared by the infraspinatus which also allows external rotation with the small circle. The subscapularis is an internal rotator and shoulder adductor.
    ‍
  • Finally, the long head of the biceps, associated with the short head of the biceps, form the biceps brachii muscle, which performs shoulder flexure as well as elbow flexure and supination movement.

b - Pathological context

1 - Nomenclature and definition of pathology

‍Originally described by Duplay as a “scapulohumeral periarthritis”, the term “frozen shoulder” was rapidly developed as early as 1934 by Codman (Fields et al., 2019). Since then, numerous terms have been used to refer to this pathology: “Frozen schoulder”, “Frozen shoulder”, “Frozen shoulder”, “Adhesive capsulitis”, “Primary idiopathic stiff shoulder”, “Primary idiopathic stiff shoulder”, “Fibrous capsule”... (Abrassart et al., 2020).

In 2015, Lewis proposed the adoption of the term “frozen shoulder contracture syndrome.” According to the latter, this term may be a more appropriate description to refer to this disease.

Concretely, this pathology with multiple names could be defined by ASES as “a condition of uncertain etiology characterized by a considerable restriction of active and passive mobility of the shoulder that occurs in the absence of a known intrinsic shoulder disorder” (Yip et al., 2018).

Some authors complement this definition by indicating that the loss of amplitude is initially painful and then progressively limited (Kingston et al., 2018).

2 - Natural evolution

To be more specific as to the development of this pathology, it should be noted that it is generally described in 3 or 4 phases (Chan et al., 2017; Fields et al., 2019; Kelley et al., 2013; Vaishya et al., 2013; Vaishya et al., 2016).

Thus, three phases are systematically found: the “freezing” phase, the “frozen” phase and the “Thawing” phase, which correspond to the three phases described by Reeves (Reeves, 1975):

  1. “Freezing” phase: first phase, it is characterized by a phase hot, inflammatory with significant pain and slight or even absence of stiffness, although some patients may have some amplitude limitations due to pain. Some authors report that this inflammatory phase would last from 10 to 36 weeks (Neviaser & Hannafin, 2010; Reeves, 1975).
    ‍
  2. “Frozen” phase: second phase, it is characterized by a Stiffness phase in which pain and trophic disorders will gradually decrease while stiffness sets in. Some authors speak of a duration of 4 to 12 months (Reeves, 1975).
    ‍
  3. “Thawing” phase: third phase, it is characterized by a salvage in which there is no longer any spontaneous pain or nocturnal pain. On the other hand, stiffness is still present. In general, this phase has been described as the longest given the time required for recovery (Neviaser & Hannafin, 2010; Reeves, 1975; Shaffer et al., 1992). The longer the stiffness phase, the longer the recovery phase will be.‍

To these three stages, some authors add a phase preceding the first. We are talking about the “Pre-freezing” phase. This preliminary phase would be particularly useful during arthroscopic analyses (Fields et al., 2019).

In their recent study published in 2020, Abrassart et al recommend that authors and clinicians avoid repeating the description of the disease as a “self-limiting three-phase condition”, that is, leading to complete resolution without treatment. The authors advise using instead the natural history of the most highlighted pathology “which often sees an improvement in the short term, but which carries a high probability of restriction and low intensity pain” (Abrassart et al., 2020; Srour & Nourissat, 2021). In addition, no study can confirm that subjects can recover without appropriate treatment, although some patients could adapt to the mobility deficit without complaining about it on a daily basis (Wong et al., 2017).

Therefore, it must first of all be admitted that the course of the disease is a Continuum rather than well-defined phases.

‍

However, care should be taken to understand these phases. Indeed, currently, no published objective data make it possible to validate either the theory of the spontaneous resolution of retractile capsule, or that of its progression through the phases of pain, then stiffness, then resolution (Abrassart et al., 2020; Wong et al., 2017).

Thus, some authors (Srour & Nourissat, 2021) consider that while it is difficult to divide pathophysiology into 3 phases, it is however appropriate to validate two main phases in this pathology:

  1. A first phase ofgradual onset of pain lasting 4 to 6 months with a possible loss of shoulder mobility.
    ‍
  2. A second phase of gradual reduction in pain with a possible maintenance or even an increase in stiffness.

‍

In the continuity of these different phases of evolution, some authors indicate that a certain correspondence between clinical evolution and imaging is observable. This is the case of Fields and his collaborators who, in 2019, exposed possible links between the various physiopathological phases and arthroscopic anatomy (Fields et al., 2019):

‍

3 - Physiopathology

Regarding physiopathology, it would be interesting to split it into two in order to facilitate its understanding even though they are simultaneous processes. Thus, let us first address “capsular” physiopathology before focusing on “other” factors in a second step.

  • From a capsular point of view, it has been possible to objectify a reduction in the volume of the joint capsule. Indeed, the latter would go from 20 mL under healthy conditions to less than 5 mL in some cases (Kraal et al., 2020).
    ‍
  • At the same time, the capsule would thicken and congest with a densification of the collagen fibers as well as a contraction of the myofibroblasts. This densification would be linked to an imbalance in the turnover of the extracellular matrix (in other words, in the production and degradation of collagen fibers) in favor of an increase in the number of collagen fibers (Kraal et al., 2020). In addition, inflammation of the rotator interval ligaments would appear, and more particularly on the coracohumeral ligament, the glenohumeral ligament and the synovia (Cho et al., 2019; Lewis, 2019; Lewis, 2019; Lewis, 2015; Lewis, 2015; Whelton & Peach, 2018). Note that the thickening of the coracohumeral ligament is considered to be one of the main barriers to external rotation (Hagiwara et al., 2018; Ozaki et al., 1989).
    ‍
  • This inflammation would result in the release of fibroblasts, mast cells, mast cells, macrophages and T lymphocytes in the glenohumeral capsule, thus increasing collagen production via the inflammatory phenomenon (Cho et al., 2019; Tamai et al., 2014).
  • --> All of these tissue modifications would appear preferentially in the anterosuperior part of the capsule, and more precisely with respect to the coracohumeral ligament (Srour & Nourissat, 2021). This would result in stiffness, pain and fibrosis of the rotator interval space.
    ‍
  • --> Note that while the fibroproliferative and inflammatory aspects seem established, the role of each person in the development of this pathology remained unknown for a long time (Gordon et al., 2016). Recently, some authors have been able to support the hypothesis that a persistent activation of fibroblasts could develop the inflammatory and fibrotic process (Akbar et al., 2019) while others consider that an immune response with an exaggerated inflammatory response would be the first step in the development of capsulitis, preceding tissue fibrosis (Cho et al., 2018; Lho et al., 2013).

In addition to tissue changes specific to the joint capsule, other changes would appear such as:

  • New nerve and vascular growth in the capsule ligament complex in affected patients. The latter could explain the increased pain response (Andersson et al., 2011; Backman et al., 2011; Hand et al., 2007).
    ‍
  • A phenomenon of muscular contracture would appear and could explain the patient's loss of mobility (Srour & Nourissat, 2021). This would also correlate with certain studies showing the presence of trigger points in the subscapular (Arjun & Rajaseker, 2021) or with those showing an improvement in mobility in abduction and lateral rotation under general anesthesia (Hollmann et al., 2018). Moreover, some authors consider that capsulitis is mainly linked to muscular dysfunction (Simons et al., 1999). Note that this protective muscular contracture could be linked to a fear of movement.
    ‍
  • Regarding “psychological” factors, some studies have been able to show that expanded pain areas would be linked to a higher level of catastrophism, of pain awareness (Balasch-Bernat et al., 2021)

Thus, it is therefore clear that pathophysiology is mainly of inflammatory and fibroproliferative origin (Akbar et al., 2019).

‍

4 - Etiology

After having addressed pathophysiology, it is now time to focus on the etiology of this pathology. Indeed, while we have been able to see that capsulitis is mainly characterized by inflammation and fibroproliferation, it is now time to understand the origins of these disorders.

First of all, it is essential to note that while many etiologies have been advanced, capsulitis is considered to be a systemic pathology that links many different mechanisms and can lead to the onset of this pathology (de la Serna et al., 2021). Among the mechanisms that may be involved in the development of pathology, we find:

  • Sedentary lifestyle: sedentary attitudes result in a decrease in the use of the upper extremities that can lead to a fear of movement (with reflex contractures) (Hollmann et al., 2018) or chronic hypoxia in the joint leading to an increase in inflammatory processes (de la Serna et al., 2021). Moreover, these attitudes could increase oxidative stress as well as insulin resistance, which we will discuss below (LeĂłn-Latre et al., 2014).
    ‍
  • ‍Chronic low-grade inflammation: defined as: “a chronic response to illnesses, injuries, etc., that produces a consistent, low level of inflammation all over the body at all times.” It could predispose certain subjects to develop retractile capsulitis (Cucchi et al., 2017; Jublanc et al., 2011; Kraal et al., 2020; Pietrzak, 2016; Sung et al., 2014). Indeed, this inflammation could alter fibroblasts (Akbar et al., 2019). In addition, chronic low-grade inflammation is an underlying cause of diabetes and thyroid disorders, which are themselves risk factors for developing capsulitis (Blonna et al., 2017; Y.-S. Kim et al., 2013; Kraal et al., 2020).
    ‍
  • Microtraumas and tissue injuries: while microtraumas have long been suggested as possible triggers of capsulitis (Neviaser & Hannafin, 2010), recent studies have been able to show that during an “injury”, the release of alarmins (endogenous molecules that aim to alert the immune system) could stimulate capsular fibrosis and nerve growth (Cher et al., 2018).
    ‍
  • Infection through bacteria: Propionibacterium acnes has long been considered as a possible origin of capsulitis although recent studies rule out this possibility (Booker et al., 2017).
    ‍
  • Finally, some studies have even hypothesized that depressive personality traits could sometimes be linked to retractile capsulitis. For example, according to Köhler, the depression would be associated with an increase in the level of inflammatory cytokines (Köhler et al., 2017). This would correlate at the “clinical” level since studies show that if there is no significant difference in range of motion, perceived disability as well as pain would be greater in depressed or anxious patients (Ebrahimzadeh et al., 2019; Russell et al., 2014). Likewise, the fear of pain could influence the patient's behavior by causing motor adaptations (muscular protection and/or reduction in the range of movements). However, there is no scientific data to support the claim that psychological factors promote the onset of capsulitis (Srour & Nourissat, 2021).
    ‍
  • On the other hand, a recent study was able to show that after rotator cuff surgery, female gender, anxiety and “occupational” illness could be considered as risk factors for developing retractile capsulitis postoperatively (AĂŻm et al., 2022).

‍

Before finishing this part concerning etiology, it is interesting to note that some studies have been able to show an increase in the number of capsules (up to 39%) during the COVID-19 epidemic (Demyttenaere et al., 2022; Sahu & Shetty, 2022) and this in cases of infection by the SARS-COV-2 virus, which is known to have numerous effects outside the pulmonary system or after carrying out a vaccination.

‍

5 - Classification of capsules

In order to clarify the different types of retractile capsulitis. A classification into 2 categories has been proposed (Warner, 1997):

  • ‍Primary capsulitis : also called idiopathic capsulitis, it is characterized by the gradual onset of pain and stiffness in the glenohumeral joint without a specific cause (Baslund et al., 1990, p. 199). This first would be linked to a possible immunological, inflammatory, biochemical and/or endocrine alteration (Hand et al. 2007) although the “psychological” factor (patients with problems in their life, stress, etc...) could intervene (Köhler et al., 2017).
    ‍
  • ‍Secondary capsulitis : is the consequence of another problem. Numerous articles have classified these secondary factors into factors. systemic, intrinsic and extrinsic according to their nature (Kelley et al., 2013; Laubscher & Rösch, 2009).

Let's now describe the various secondary factors:

  • Les extrinsic causes correspond to causes not related to the shoulder. For example, there are cardiopulmonary problems, cervical disorders, Parkinson's disease... (Kelley et al., 2013). Note that in the case of a humerus fracture, the cause will be considered extrinsic if the fracture is distal to the humeral head. Conversely, if it is located on the humeral head, we will then speak of intrinsic cause.
    ‍
  • ‍The intrinsic causes include causes directly related to the shoulder. These include, for example, pathologies of the rotator cuff, the biceps brachii or the acromioclavicular joint... (Kelley et al., 2013). In this type of cause, it often happens that a patient initially consults for tendinopathy before seeing the tendinopathy evolve into capsulitis.
    ‍
  • ‍Systemic factors include more encompassing pathologies that are not limited to a specific area of the body. It is therefore, for example, diabetes mellitus, thyroid disorders, hypoadrenalism or dyslipidemia (Hani Zreik et al., 2019, p. 201; Kelley et al., 2013; Laubscher & Rösch, 2009; Laubscher & Rösch, 2009; 2009; Schiefer et al., 2009; Schiefer et al., 2017; Srour & Nourissat, 2021; Tasto & Elias, 2007).

Note that some authors consider that retractile capsulitis As a result of diabetes should be a category in its own right (Robinson et al., 2012). Indeed, when we look at disorders related to hyperglycemia, studies have been able to show the impact of the latter on collagenic modifications as well as on the turnover of the extracellular matrix (Kraal et al., 2020). Moreover, a recent study that looked at the genome of patients with capsulitis with and without diabetes was able to show that there could be a fundamental difference in the physiopathology of capsulitis in patients with diabetes compared to patients without diabetes compared to patients without diabetes (Gordon et al., 2022). This would correlate with a 2016 meta-analysis that found that diabetic patients were 5 times more likely than the control group to suffer from retractile capsulitis (Hani Zreik et al., 2019).

This classification system for retractile capsulitis still causes debates in literature. During the American Shoulder and Elbow Surgeons (ASES) consensus survey, 85% of respondents agreed that “capsule shrinkage” should include both “primary” and “secondary” types. On the other hand only 66% agreed on the proposed sub-division into “intrinsic”; “extrinsic”; “systemic” (Zuckerman & Rokito, 2011).

In general, a Misunderstanding of the definition of a pathology can lead to a maladaptive care patients and hinder research efforts. As with the study of the literature, if the nomenclature or definition is inconsistent from one study to another of the pathology, how can clinical conclusions be drawn?

‍

6 - Prevalence

The prevalence rate of idiopathic retractile capsulitis would be 2% to 5% and it occurs more frequently for women (Srour & Nourissat, 2021) of 40 to 60 years (D'Orsi et al., 2012), with the peak incidence occurring, on average, between 51 and 55 years of age (Kelley et al., 2013, p. 201). Among diabetic patients, the prevalence could reach 13.4% prevalence, which would represent up to 5 times more risk of developing capsulitis. Moreover, in 30% of patients with capsulitis, there would be a history of diabetes (Hani Zreik et al., 2019).

In most cases, this condition is one-sided on the non-dominant side (Kingston et al., 2018). Sometimes, in some cases, the condition is bilateral (20 to 30% of cases) but it is rare for it to occur on both sides simultaneously (Manske & Prohaska, 2010).

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Foreword

Retractile capsule is a shoulder disorder that is frequently encountered but is still the subject of numerous uncertainties and inconsistencies in the literature. The main causes of confusion related to retractile capsulitis stem from a disagreement about how to name this pathology, classify it, and describe its natural history (Abrassart et al. 2020). In general, it is characterized by a gradual increase in spontaneous pain and a limitation in the range of movements of the glenohumeral joint (Kingston et al., 2018). Management strategies vary according to the degree of irritability, the stage of development of the pathology, and the therapist's preferences.

1 - Introduction to pathology

a - Anatomical reminders

At first, it may be appropriate to recall some notions of anatomy, in particular concerning the various structures likely to be involved in retractile capsulitis.

‍1 - The joint capsule

This fibrous structure contains numerous joint elements. The presence of joint capsules is generally observed within mobile joints (diarthrosis).

It is characterized in particular by its elasticity allowing movement and by its resistance allowing a certain passive stability of the articular surfaces between them.

The glenohumeral joint capsule has thick reinforcements called glenohumeral (superior, middle and inferior) and coracohumeral ligaments (Ferrari et al. 1990). The volume of this capsule would be on average 20 mL under healthy conditions (Kraal et al., 2020).

Moreover, due to its location, it is in close relationship with the tendons of the cuff muscles, with which it intertwines its fibers, forming a fibrous musculotendinous sleeve (Drake et al. 2006; Clark et al. 2006; Clark et al. 2006; Clark et al. 1990; Pearsall et al. 2000).

This fibrous fusion has both a proprioceptive and mechanical role (distribution of the stresses of the cuff muscles and the prevention of possible tendon injuries at the level of their entheses) (Di Giacomo et al. 2008).

Overall, the joint capsule has the following 3 tissue layers (from surface to depth) (McFarland et al. 2002):

‱ A tough connective layer rich in collagen
‱ A loose connective layer
‱ A synovial membrane, a structure that secretes the eponymous liquid. It lubricates and nourishes joint surfaces.

Finally, it is important to remember that this capsule is innervated by the articular branches of the suprascapular and axillary nerves and that it is well vascularized (Andary et al. 2002, Eckmann et al., 2017).

At the level of the shoulder joint capsule, the axillary pouch represents an entity of interest in the physiopathology of capsulitis. This corresponds to the glenohumeral capsule in its lower part and is delimited by the anterior and posterior bands of the inferior glenohumeral ligaments (Fields et al., 2019). As we will see later, the latter makes it possible, during arthroscopic evaluations, to determine a certain grade of capsulitis since this fold is generally reduced (The Shoulder Made Easy, 2019).

2 - The rotator interval

The rotator interval represents two triangular-shaped capsular areas that are characterized by the absence of reinforcement by the rotator cuff tendons (Le Corroller et al., 2007). While an anterior rotator interval and a posterior rotator interval could be defined, it is commonly accepted that when talking about the rotator interval, we are referring to the anterior rotator interval (Fields et al., 2019).

The latter entity forms an anatomical triangular space through the upper edge of the subscapular muscle tendon at the bottom, the anterior edge of the supraspinatus tendon at the top, the base of the coracoid process medially and the transverse humeral ligament laterally (Le Corroller et al. 2007).

This interval is closed superficially by an extension of the anterior glenohumeral joint capsule called the “rotator interval capsule” (Woertler, 2015). The latter includes the intertwining of fibers from the subscapular and supraspinous tendons, by the superior glenohumeral ligament as well as by the coracohumeral ligament (LCH). Conversely, the floor of this space consists mainly of the articular cartilage of the humeral head (Fields et al., 2019).

Note that the tendon of the long portion of the biceps brachii and the superior glenohumeral ligament (LGHS) cross the rotator interval (Le Corroller et al. 2007).

While the role of the rotator interval has not yet been fully defined, it seems clear that the rotator interval has a structural role in stabilizing dynamic shoulder movements (Fields et al., 2019). Thus, for some authors (Le Corroller et al., 2007), this interval would have 3 main roles:

  • Maintaining negative intra-articular pressure
  • A pulley role for the tendon of the long biceps laterally
  • Posterior and inferior stabilization of the humeral head

As a result, the experimental section of the LCH and the rotator interval capsule could lead to a destabilization of the biceps pulley (Fields et al., 2019) as well as a risk of inferior and posterior instability/dislocation (Fields et al., 2019; Harryman et al., 1992).

Moreover, this interval allows the limitation of translations:

  • Posteriors and inferiors in adduction
  • Anterior in abduction and lateral rotation

This is why some authors indicate that the latter would present a key role in the pathogenesis of capsulitis, but also in multidirectional instability (Bain et al., 2017)

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3 - The coracohumeral ligament

The coracohumeral ligament (LCH) has been described as originating on the outer edge of the horizontal branch of the coracoid process and ending in a bundle on the anterior edge of the supra spinatus and the major tubercle while the second bundle terminates at the level of the minor tubercle. Note some insertions attaching to the upper fibers of the subscapular as well as to the transverse humeral ligament. Because of its path, it covers the rotator interval (Fields et al., 2019).

In terms of its histological conformation, the coracohumeral ligament (LCH) is composed of 5 distinct tissue layers, the most superficial and the deepest of which are in direct continuity with the superficial and deep faces of the supraspinous tendon (Clark et al. 1992). This ligament can be put under maximum tension during the external rotational movement (Le et al., 2017).

Functionally, the LCH has several roles:

  • Formation of the “long biceps pulley” with the superior glenohumeral ligament (Fields et al., 2019).
  • Passive limitation of lateral rotation, especially when arming with the arm (Fields et al., 2019). Conversely, the ligament is relaxed in an internal adduction-rotation position (Woertler, 2015).
  • postero-inferior stabilizer of the humeral head (LCH couple and superior glenohumeral ligament).
  • Humeral head suspensor (Dufour et al. 2014).
  • Protection of the long biceps tendons from the acromio-coracoid ligament (Corroler et al. 2007).
  • Protection of the subscapular from the coracoid process or even the minor tubercle (Corroler et al. 2007).

Note that for some authors, the coracohumeral ligament cannot be detached from the superior glenohumeral ligament since they constitute a functional unit in the stability of the rotator interval (Petchprapa et al., 2010; Woertler, 2015).

4 - The rotator cuff

The rotator cuff is a group of muscles and tendons that surround the shoulder joint. According to the latest data on the subject (Akhtar et al., 2021), the muscles that make up the rotator cuff are four in number:

  • The supraspinatus: originating in the supraspinous fossa, it is directed to the superior and medial surface of the trochiter.
  • The infraspinatus: originating in the infraspinous fossa, it goes to the inferior and medial face of the trochiter. The latter has a tendon with the widest section of the four cuff tendons.
  • The small circle: having its origin in the infraspinous fossa, it goes on the inferior and medial face of the trochiter.
  • The subscapular: having its origin in the subscapular fossa, it goes over the trochin.

It should be noted that the first three muscles mentioned form digitations in order to form a continuous structure proximal to the humerus: the rotator cable (Pallot & Morichon, 2013; Rahu et al., 2017). For its part, the subscapular is increasingly linked to capsulitis through numerous studies showing the presence of trigger points in it in patients with capsulitis (Arjun & Rajaseker, 2021).

To these four muscles, some authors add the long head of the biceps, although this concept is not adopted unanimously (Redondo-Alonzo et al, 2014).

Regarding their roles, the main mission of the rotator cuff is to stabilize the humeral head during shoulder movements. In fact, by its action, the cuff creates a force torque in order to prevent any proximal “migration” of the humerus. Apart from their stabilizing role, these muscles have their own action:

  • The supraspinatus muscle participates in shoulder abduction, an action shared by the infraspinatus which also allows external rotation with the small circle. The subscapularis is an internal rotator and shoulder adductor.
  • Finally, the long head of the biceps, associated with the short head of the biceps, form the biceps brachii muscle, which performs shoulder flexure as well as elbow flexure and supination movement.

b - Pathological context

1 - Nomenclature and definition of pathology

‍Originally described by Duplay as a “scapulohumeral periarthritis”, the term “frozen shoulder” was rapidly developed as early as 1934 by Codman (Fields et al., 2019). Since then, numerous terms have been used to refer to this pathology: “Frozen schoulder”, “Frozen shoulder”, “Frozen shoulder”, “Adhesive capsulitis”, “Primary idiopathic stiff shoulder”, “Primary idiopathic stiff shoulder”, “Fibrous capsule”... (Abrassart et al., 2020). In 2015, Lewis proposed the adoption of the term “frozen shoulder contracture syndrome.” According to the latter, this term may be a more appropriate description to refer to this disease. Concretely, this pathology with multiple names could be defined by ASES as “a condition of uncertain etiology characterized by a considerable restriction of active and passive mobility of the shoulder that occurs in the absence of a known intrinsic shoulder disorder” (Yip et al., 2018). Some authors complement this definition by indicating that the loss of amplitude is initially painful and then progressively limited (Kingston et al., 2018).

2 - Natural evolution

To be more specific as to the development of this pathology, it should be noted that it is generally described in 3 or 4 phases (Chan et al., 2017; Fields et al., 2019; Kelley et al., 2013; Vaishya et al., 2013; Vaishya et al., 2016).

Thus, three phases are systematically found: the “freezing” phase, the “frozen” phase and the “Thawing” phase, which correspond to the three phases described by Reeves (Reeves, 1975):

  1. “Freezing” phase: first phase, it is characterized by a phase hot, inflammatory with significant pain and slight or even absence of stiffness, although some patients may have some amplitude limitations due to pain. Some authors report that this inflammatory phase would last from 10 to 36 weeks (Neviaser & Hannafin, 2010; Reeves, 1975).
  2. “Frozen” phase: second phase, it is characterized by a Stiffness phase in which pain and trophic disorders will gradually decrease while stiffness sets in. Some authors speak of a duration of 4 to 12 months (Reeves, 1975).
  3. “Thawing” phase: third phase, it is characterized by a salvage in which there is no longer any spontaneous pain or nocturnal pain. On the other hand, stiffness is still present. In general, this phase has been described as the longest given the time required for recovery (Neviaser & Hannafin, 2010; Reeves, 1975; Shaffer et al., 1992). The longer the stiffness phase, the longer the recovery phase will be.‍

To these three stages, some authors add a phase preceding the first. We are talking about the “Pre-freezing” phase. This preliminary phase would be particularly useful during arthroscopic analyses (Fields et al., 2019).

In their recent study published in 2020, Abrassart et al recommend that authors and clinicians avoid repeating the description of the disease as a “self-limiting three-phase condition”, that is, leading to complete resolution without treatment. The authors advise using instead the natural history of the most highlighted pathology “which often sees an improvement in the short term, but which carries a high probability of restriction and low intensity pain” (Abrassart et al., 2020; Srour & Nourissat, 2021). Moreover, no study confirms that subjects can recover without appropriate treatment, although some patients could adapt to the mobility deficit without complaining about it on a daily basis (Wong et al., 2017).

Therefore, it must first of all be admitted that the evolution of the disease is a continuum rather than well-defined phases.

‍

However, care should be taken to understand these phases. Indeed, currently, no published objective data make it possible to validate either the theory of the spontaneous resolution of retractile capsule, or that of its progression through the phases of pain, then stiffness, then resolution (Abrassart et al., 2020; Wong et al., 2017).

Thus, some authors (Srour & Nourissat, 2021) consider that while it is difficult to divide pathophysiology into 3 phases, it is however appropriate to validate two main phases in this pathology:

  1. A first phase of gradual onset of pain lasting 4 to 6 months with a possible loss of shoulder mobility.
  2. A second phase of gradual reduction in pain with a possible maintenance or even an increase in stiffness.

‍

In the continuity of these different phases of evolution, some authors indicate that a certain correspondence between clinical evolution and imaging is observable. This is the case of Fields and his collaborators who, in 2019, exposed possible links between the various physiopathological phases and arthroscopic anatomy (Fields et al., 2019):

‍

3 - Physiopathology

Regarding physiopathology, it would be interesting to split it into two in order to facilitate its understanding even though they are simultaneous processes. Thus, let us first address “capsular” physiopathology before focusing on “other” factors in a second step.

  • From a capsular point of view, it has been possible to objectify a reduction in the volume of the joint capsule. Indeed, the latter would go from 20 mL under healthy conditions to less than 5 mL in some cases (Kraal et al., 2020).
  • At the same time, the capsule would thicken and congest with a densification of the collagen fibers as well as a contraction of the myofibroblasts. This densification would be linked to an imbalance in the turnover of the extracellular matrix (in other words, in the production and degradation of collagen fibers) in favor of an increase in the number of collagen fibers (Kraal et al., 2020). In addition, inflammation of the rotator interval ligaments would appear, and more particularly on the coracohumeral ligament, the glenohumeral ligament and the synovia (Cho et al., 2019; Lewis, 2019; Lewis, 2019; Lewis, 2015; Lewis, 2015; Whelton & Peach, 2018). Note that the thickening of the coracohumeral ligament is considered to be one of the main barriers to external rotation (Hagiwara et al., 2018; Ozaki et al., 1989).
  • This inflammation would result in the release of fibroblasts, mast cells, mast cells, macrophages and T lymphocytes in the glenohumeral capsule, thus increasing collagen production via the inflammatory phenomenon (Cho et al., 2019; Tamai et al., 2014).
  • --> All of these tissue modifications would appear preferentially in the anterosuperior part of the capsule, and more precisely with respect to the coracohumeral ligament (Srour & Nourissat, 2021). This would result in stiffness, pain and fibrosis of the rotator interval space.
  • --> Note that while the fibroproliferative and inflammatory aspects seem established, the role of each person in the development of this pathology remained unknown for a long time (Gordon et al., 2016). Recently, some authors have been able to support the hypothesis that a persistent activation of fibroblasts could develop the inflammatory and fibrotic process (Akbar et al., 2019) while others consider that an immune response with an exaggerated inflammatory response would be the first step in the development of capsulitis, preceding tissue fibrosis (Cho et al., 2018; Lho et al., 2013).

In addition to tissue changes specific to the joint capsule, other changes would appear such as:

  • New nerve and vascular growth in the capsule ligament complex in affected patients. The latter could explain the increased pain response (Andersson et al., 2011; Backman et al., 2011; Hand et al., 2007).
  • A phenomenon of muscular contracture would appear and could explain the patient's loss of mobility (Srour & Nourissat, 2021). This would also correlate with certain studies showing the presence of trigger points in the subscapular (Arjun & Rajaseker, 2021) or with those showing an improvement in mobility in abduction and lateral rotation under general anesthesia (Hollmann et al., 2018). Moreover, some authors consider that capsulitis is mainly linked to muscular dysfunction (Simons et al., 1999). Note that this protective muscular contracture could be linked to a fear of movement.
  • Regarding “psychological” factors, some studies have been able to show that expanded pain areas would be linked to a higher level of catastrophism, of pain awareness (Balasch-Bernat et al., 2021)

Thus, it is therefore clear that pathophysiology is mainly of inflammatory and fibroproliferative origin (Akbar et al., 2019).

‍

4 - Etiology

After having addressed pathophysiology, it is now time to focus on the etiology of this pathology. Indeed, while we have been able to see that capsulitis is mainly characterized by inflammation and fibroproliferation, it is now time to understand the origins of these disorders.

First of all, it is essential to note that while many etiologies have been advanced, capsulitis is considered to be a systemic pathology that links many different mechanisms and can lead to the onset of this pathology (de la Serna et al., 2021). Among the mechanisms that may be involved in the development of pathology, we find:

  • Sedentary lifestyle: sedentary attitudes result in a decrease in the use of the upper extremities that can lead to a fear of movement (with reflex contractures) (Hollmann et al., 2018) or chronic hypoxia in the joint leading to an increase in inflammatory processes (de la Serna et al., 2021). Moreover, these attitudes could increase oxidative stress as well as insulin resistance, which we will discuss below (LeĂłn-Latre et al., 2014).
  • ‍Chronic low-grade inflammation: defined as: “a chronic response to illnesses, injuries, etc., that produces a consistent, low level of inflammation all over the body at all times.” It could predispose certain subjects to develop retractile capsulitis (Cucchi et al., 2017; Jublanc et al., 2011; Kraal et al., 2020; Pietrzak, 2016; Sung et al., 2014). Indeed, this inflammation could alter fibroblasts (Akbar et al., 2019). In addition, chronic low-grade inflammation is an underlying cause of diabetes and thyroid disorders, which are themselves risk factors for developing capsulitis (Blonna et al., 2017; Y.-S. Kim et al., 2013; Kraal et al., 2020).
  • Microtraumas and tissue injuries: while microtraumas have long been suggested as possible triggers of capsulitis (Neviaser & Hannafin, 2010), recent studies have been able to show that during an “injury”, the release of alarmins (endogenous molecules that aim to alert the immune system) could stimulate capsular fibrosis and nerve growth (Cher et al., 2018).
  • Infection through bacteria: Propionibacterium acnes has long been considered as a possible origin of capsulitis although recent studies rule out this possibility (Booker et al., 2017).
  • Finally, some studies have even hypothesized that depressive personality traits could sometimes be linked to retractile capsulitis. For example, according to Köhler, the depression would be associated with an increase in the level of inflammatory cytokines (Köhler et al., 2017). This would correlate at the “clinical” level since studies show that if there is no significant difference in range of motion, perceived disability as well as pain would be greater in depressed or anxious patients (Ebrahimzadeh et al., 2019; Russell et al., 2014). Likewise, the fear of pain could influence the patient's behavior by causing motor adaptations (muscular protection and/or reduction in the range of movements). However, there is no scientific data to support the claim that psychological factors promote the onset of capsulitis (Srour & Nourissat, 2021).
  • On the other hand, a recent study was able to show that after rotator cuff surgery, female gender, anxiety and “occupational” illness could be considered as risk factors for developing retractile capsulitis postoperatively (AĂŻm et al., 2022).

‍

Before finishing this part concerning etiology, it is interesting to note that some studies have been able to show an increase in the number of capsules (up to 39%) during the COVID-19 epidemic (Demyttenaere et al., 2022; Sahu & Shetty, 2022) and this in cases of infection by the SARS-COV-2 virus, which is known to have numerous effects outside the pulmonary system or after carrying out a vaccination.

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5 - Classification of capsules

In order to clarify the different types of retractile capsulitis. A classification into 2 categories has been proposed (Warner, 1997):

  • ‍Primary capsulitis : also called idiopathic capsulitis, it is characterized by the gradual onset of pain and stiffness in the glenohumeral joint without a specific cause (Baslund et al., 1990, p. 199). This first would be linked to a possible immunological, inflammatory, biochemical and/or endocrine alteration (Hand et al. 2007) although the “psychological” factor (patients with problems in their life, stress, etc...) could intervene (Köhler et al., 2017).
  • ‍Secondary capsulitis : is the consequence of another problem. Numerous articles have classified these secondary factors into factors. systemic, intrinsic and extrinsic according to their nature (Kelley et al., 2013; Laubscher & Rösch, 2009).

Let's now describe the various secondary factors:

  • Les extrinsic causes correspond to causes not related to the shoulder. For example, there are cardiopulmonary problems, cervical disorders, Parkinson's disease... (Kelley et al., 2013). Note that in the case of a humerus fracture, the cause will be considered extrinsic if the fracture is distal to the humeral head. Conversely, if it is located on the humeral head, we will then speak of intrinsic cause.
  • ‍The intrinsic causes include causes directly related to the shoulder. These include, for example, pathologies of the rotator cuff, the biceps brachii or the acromioclavicular joint... (Kelley et al., 2013). In this type of cause, it often happens that a patient initially consults for tendinopathy before seeing the tendinopathy evolve into capsulitis.
  • ‍Systemic factors include more encompassing pathologies that are not limited to a specific area of the body. It is therefore, for example, diabetes mellitus, thyroid disorders, hypoadrenalism or dyslipidemia (Hani Zreik et al., 2019, p. 201; Kelley et al., 2013; Laubscher & Rösch, 2009; Laubscher & Rösch, 2009; 2009; Schiefer et al., 2009; Schiefer et al., 2017; Srour & Nourissat, 2021; Tasto & Elias, 2007).

Note that some authors consider that retractile capsulitis As a result of diabetes should be a category in its own right (Robinson et al., 2012). Indeed, when we look at disorders related to hyperglycemia, studies have been able to show the impact of the latter on collagenic modifications as well as on the turnover of the extracellular matrix (Kraal et al., 2020). Moreover, a recent study that looked at the genome of patients with capsulitis with and without diabetes was able to show that there could be a fundamental difference in the physiopathology of capsulitis in patients with diabetes compared to patients without diabetes compared to patients without diabetes (Gordon et al., 2022). This would correlate with a 2016 meta-analysis that found that diabetic patients were 5 times more likely than the control group to suffer from retractile capsulitis (Hani Zreik et al., 2019).

This classification system for retractile capsulitis still causes debates in literature. During the American Shoulder and Elbow Surgeons (ASES) consensus survey, 85% of respondents agreed that “capsule shrinkage” should include both “primary” and “secondary” types. On the other hand only 66% agreed on the proposed sub-division into “intrinsic”; “extrinsic”; “systemic” (Zuckerman & Rokito, 2011).

In general, a Misunderstanding of the definition of a pathology can lead to a maladaptive care patients and hinder research efforts. As with the study of the literature, if the nomenclature or definition is inconsistent from one study to another of the pathology, how can clinical conclusions be drawn?

‍

6 - Prevalence

The prevalence rate of idiopathic retractile capsulitis would be 2% to 5% and it occurs more frequently for women (Srour & Nourissat, 2021) of 40 to 60 years (D'Orsi et al., 2012), with the peak incidence occurring, on average, between 51 and 55 years of age (Kelley et al., 2013, p. 201). Among diabetic patients, the prevalence could reach 13.4% prevalence, which would represent up to 5 times more risk of developing capsulitis. Moreover, in 30% of patients with capsulitis, there would be a history of diabetes (Hani Zreik et al., 2019).

In most cases, this condition is one-sided on the non-dominant side (Kingston et al., 2018). Sometimes, in some cases, the condition is bilateral (20 to 30% of cases) but it is rare for it to occur on both sides simultaneously (Manske & Prohaska, 2010).

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