Journal of Clinical Medicine Review Suprascapular Neuropathy around the Shoulder: A Current Concept Review Federico Bozzi 1, * , Sergi Alabau-Rodriguez 2 , Sergi Barrera-Ochoa 2 , Atesch Ateschrang 3 , Anna J. Schreiner 4 , Juan Carlos Monllau 2,5 and Simone Perelli 2,5 1 Department of Orthopaedics and Traumatology, Fondazione Poliambulanza (Brescia)—Università Cattolica del Sacro Cuore, 00168 Rome, Italy 2 Institut Català de Traumatologia i Medicina de l’Esport (ICATME)—Hospital Universitari Quiròn-Dexeus. Universitat Autònoma de Barcelona, 08028 Barcelona, Spain; sralabau89@gmail.com (S.A.-R.); dr.barreraochoa@gmail.com (S.B.-O.); JMonllau@parcdesalutmar.cat (J.C.M.); perelli.simone@gmail.com (S.P.) 3 Orthopedic department, Gemeinschaftsklinikum Mittelrhein, 56073 Koblenz, Germany; ateschrang@gmx.de 4 Department of Traumatology and Reconstructive Surgery, BG Trauma Center Tübingen, Eberhard-Karls University of Tübingen, 72076 Tübingen, Germany; annajschreiner@yahoo.de 5 Department of Orthopaedic Surgery, Hospital del Mar. Universitat Autònoma de Barcelona (UAB), 08028 Barcelona, Spain * Correspondence: federico.bozzi88@gmail.com  Received: 17 May 2020; Accepted: 18 July 2020; Published: 22 July 2020  Abstract: Suprascapular neuropathy is an uncommon but increasingly recognized cause of shoulder pain and dysfunction due to nerve entrapment. The aim of this review is to summarize some important aspects of this shoulder pathology. An extensive research was performed on PubMed and Clinical Key. The goal was to collect all the anatomical, biomechanical and clinical studies to conduct an extensive overview of the issue. Attention was focused on researching the state of art of the diagnosis and treatment. A total of 59 studies were found suitable and included. This condition is more frequently diagnosed in over-head athletes or patients with massive rotator cuff tears. Diagnosis may be complex, whereas its treatment is safe, and it has a great success rate. Prompt diagnosis is crucial as chronic conditions have worse outcomes compared to acute lesions. Proper instrumental evaluation and imaging are essential. Dynamic compression must initially be treated non-operatively. If there is no improvement, surgical release should be considered. On the other hand, soft tissue lesions may first be treated non-operatively. However, surgical treatment by arthroscopic means is advisable when possible as it represents the gold standard therapy. Other concomitant shoulder lesions must be recognized and treated accordingly. Keywords: suprascapular nerve palsy; spinoglenoid notch; suprascapular notch; Arthroscopic nerve release; shoulder neuropathy; over-head activities 1. Introduction Suprascapular neuropathy is of increasing interest as a cause of shoulder pain and weakness. It was first described by the Frenchman Andre Thomas in 1936, and further defined by Kopell and Thompson in 1959 [1,2]. It is considered a rare cause of shoulder pain even though the real incidence rate remains unknown and so may be underestimated [3,4]. The difficulty is to remember this specific and other coexisting shoulder pathologies [5]. However, the diagnosis and recognition rates of this disease are increasing and might represent 1%–2% of all causes of shoulder pain [6]. It mainly occurs in patients under J. Clin. Med. 2020, 9, 2331; doi:10.3390/jcm9082331 www.mdpi.com/journal/jcm J. Clin. Med. 2020, 9, 2331 2 of 15 40 years of age and prevalence seems to extend widely from 12% to 33% in all athletes, representing an important cause of shoulder pain in overhead athletes [6,7]. Several studies found infraspinatus muscle impairment, suprascapular muscle atrophy and weakness in 20% to 45% of volleyball athletes [4,5,8]. Another one third of all those volleyball athletes were asymptomatic [9,10]. Some reports investigate the correlation between suprascapular neuropathy and retracted rotator cuff tears. In any case, it is still impossible to define how suprascapular neuropathy contributes to symptoms in patients affected by massive cuff-tear lesions. Moreover, some authors consider this condition as a possible cause of shoulder pain and weakness in patients with symptoms suggesting a rotator cuff tear while having normal imaging [3,11–13]. Only anecdotal reports of iatrogenic cases after supraclavicular block for upper extremity surgery have been described [14,15]. 2. Materials and Method An extensive research was performed on PubMed and Clinical Key. Search terms included suprascapular nerve palsy, spinoglenoid notch, suprascapular notch, arthroscopic nerve release, shoulder neuropathy and overhead activities. Additionally, citation tracking was performed by manually screening the reference lists of eligible studies. Reviewers assessed the studies considering whether they met the following inclusion criteria: anatomical study paper, clinical trial, systematic literature review and meta-analysis. The only exclusion criterion was: article not written in English. The goal was to collect all the anatomical, biomechanical and clinical studies in order to have an extensive overview of the issue. Attention was focused on researching the state of art of the diagnosis and treatment. A total of 66 studies were found but only 59 of them were found suitable and included. 2.1. Anatomy The suprascapular nerve (SN), a mixed nerve that includes sensory and motor fibers, arises from upper trunk of the brachial plexus (C5, C6 and sporadically C4 roots). It runs laterally through the posterior cervical triangle and backwards to the clavicle, reaching the superior border of the scapula at the suprascapular notch underneath the superior transverse scapular ligament. The suprascapular artery and vein pass over the transverse ligament [5]. The suprascapular notch represents the most common site of compression of the suprascapular nerve. Several anatomic variations of the notch have been described that range from a simple bony tunnel to a wide and soft bony depression. It has been classified into 6 morphotypes by Rengachary (Figure 1). In type IV, the transverse scapular ligament is ossified and may form a nearly complete or complete bony foramen. This morphotype can compress the suprascapular nerve and increase the risk of entrapment [2,16,17]. After passing through the suprascapular notch, the nerve passes laterally along the supraspinous fossa, emitting motor branches to the supraspinatus muscle and receiving sensory branches from the coracohumeral and coracoacromial ligaments, the subacromial bursa and the acromioclavicular and glenohumeral joints [18–20]. It then proceeds underneath the supraspinatus muscle and reaches and passes through the spinoglenoid notch under the spinoglenoid ligament (or inferior transverse scapular ligament). The spinoglenoid notch, a bony depression at the lateral third of the scapular spine, is considered the second typical compression site of the suprascapular nerve [10]. The anterior coraco-scapular ligament (ACSL) is an independent ligament extending along the anterior side of the suprascapular notch below the superior transverse scapular ligament (STSL). Avery et al. recently described different anatomic variations while pointing out that the presence and the position of this specific ligament as well as the location of the suprascapular bundle vessels can cause compression or protect the suprascapular nerve from compression [21]. The spinoglenoid ligament is present in 14% to 100% of patients and links the spine of the scapula, the glenoid neck and the posterior shoulder capsule. This capsular attachment causes ligament tightening during cross-body adduction J. Clin. Med. 2020, 9, 2331 3 of 15 and internal rotation of the limb and may cause dynamic nerve compression [5,22]. From this point, the nerve proceeds downwards and spreads innervation to the infraspinatus muscle. Suprascapular nerve sensitive branches arise proximal to the spinoglenoid notch and innervate the posterior and superior shoulder regions and contribute to glenohumeral joint proprioception. Additionally, secondary sensitive branches innervate the coraco-humeral and coraco-acromial ligaments, the subacromial bursa and the acromioclavicular joint [10,23–25]. J. Clin. Med. 2020, 9, x FOR PEER REVIEW 3 of 14 Figure Figure 1. 1. Rengachary Rengachary morphothypes morphothypes classification classification of of the the suprascapular suprascapular notch. notch. 2.2. 2.2.Aetiology Aetiology Suprascapular Suprascapularnerve entrapment nerve entrapment can occur can occur due to different due pathologies to different at the pathologies at suprascapular notch the suprascapular and/or spinoglenoid notch [2]. Compression is defined as primary when notch and/or spinoglenoid notch [2]. Compression is defined as primary when it is caused byit is caused by dynamic entrapment of the nerveofwhereas dynamic entrapment it is whereas the nerve called secondary when it is called it is provoked secondary when byit space occupying is provoked lesions, by space traumatic occupying conditions, post traumatic lesions, traumatic disorders conditions, and systemic post traumatic conditions. disorders Other conditions. and systemic possible causes Other of suprascapular possible causesneuropathy are hormonal of suprascapular alterationsare neuropathy or iatrogenic hormonalconditions alterations[17,26]. A complete or iatrogenic summary conditions of[17,26]. the causes is provided A complete in Table summary of1.the causes is provided in Table 1. Secondary Aetiologies Examples Space occupying lesions Table 1. Summary Neoplasm, ganglion cyst,etiologies. of the main secondary ossified scapular ligament Scapula fractures, shoulder dislocation, massive cuff tear, distractive Secondary TraumaticAetiologies conditions Examples trauma, penetrating trauma Space Post occupying lesions traumatic disorders Neoplasm, ganglionheterotopic Hematomas, cyst, ossified scapular ligament ossification, scars Systemic conditions Scapula fractures,Pregnancy, shoulder dislocation, massivehypertiroidism diabetes mellitus, cuff tear, distractive trauma, Traumatic conditions Iatrogenic conditions Arthroscopicpenetrating trauma tear cuff repair, Latarjet procedure Post traumatic disorders Hematomas, heterotopic ossification, scars Systemic conditions Table 1. Summary ofPregnancy, the main secondary etiologies. diabetes mellitus, hypertiroidism Primary: This etiology is relatively common Iatrogenic conditions Arthroscopicin tear overhead athletes, cuff repair, Latarjet such as in basketball, procedure volleyball and baseball. The reported prevalence of suprascapular neuropathy in elite volleyball players is up to 33% in the dominant arm [27]. Repeated throwing results in a backward and forward Primary: This etiology is relatively common in overhead athletes, such as in basketball, volleyball rotation of the scapula. This significant mechanical strain can cause suprascapular nerve compression and baseball. The reported prevalence of suprascapular neuropathy in elite volleyball players is up to 33% [9]. The specific mechanisms are yet not fully understood, but some hypotheses have been put in the dominant arm [27]. Repeated throwing results in a backward and forward rotation of the scapula. forward. The suprascapular nerve gets stretched between two relatively fixed sites, the brachial This significant mechanical strain can cause suprascapular nerve compression [9]. The specific mechanisms plexus medially and the infraspinatus muscle laterally. Nerve compression by the suprascapular are yet not fully understood, but some hypotheses have been put forward. The suprascapular nerve gets ligament is enhanced by depression, retraction and overhead abduction of the shoulder or extreme stretched between two relatively fixed sites, the brachial plexus medially and the infraspinatus muscle scapular motion, as in the case of repetitive pitching or throwing. Compression at the spinoglenoid laterally. Nerve compression by the suprascapular ligament is enhanced by depression, retraction and notch may be caused by compression of the motor branch of the suprascapular nerve by the overhead abduction of the shoulder or extreme scapular motion, as in the case of repetitive pitching supraspinatus or superior side of the infraspinatus muscle adjacent to the scapular spine when the or throwing. Compression at the spinoglenoid notch may be caused by compression of the motor shoulder is extremely abducted or internally and externally rotated [3,10,11,18,28,29]. All these branch of the suprascapular nerve by the supraspinatus or superior side of the infraspinatus muscle motions occur frequently during throwing or pitching. Accordingly, there is an additional association between increased shoulder range of motion and isolated infraspinatus muscle weakness [30]. Recent studies proposed another mechanism related to a tightening of the spinoglenoid ligament that cause compression of the nerve at the end of an overhead serve [4,10,22,31,32]. Rengachary et al. proposed the hypothesis of the so called “sling effect”. It consists of repeated kinking of the nerve against the borders of osteofibrous tunnel (suprascapular notch) during shoulder motion, causing suprascapular J. Clin. Med. 2020, 9, 2331 4 of 15 adjacent to the scapular spine when the shoulder is extremely abducted or internally and externally rotated [3,10,11,18,28,29]. All these motions occur frequently during throwing or pitching. Accordingly, there is an additional association between increased shoulder range of motion and isolated infraspinatus muscle weakness [30]. Recent studies proposed another mechanism related to a tightening of the spinoglenoid ligament that cause compression of the nerve at the end of an overhead serve [4,10,22,31,32]. Rengachary et al. proposed the hypothesis of the so called “sling effect”. It consists of repeated kinking of the nerve against the borders of osteofibrous tunnel (suprascapular notch) during shoulder motion, causing suprascapular neuropathy [1,8,21,23]. Some authors have advanced two hypotheses of vascular etiologies in athletes. One speculates on intimal lesions of the suprascapular or axillar artery resulting in microemboli in the vasa nervorum of suprascapular nerve [3,5,8,33]. The second contemplates a dilatation of the suprascapular veins that could lead to nerve compression at the spinoglenoid notch [28]. Secondary: Space occupying lesions, such as cysts or tumors, can compress nerves at either the suprascapular notch or spinoglenoid notch [4,10,34]. Paralabral cysts are related to labral tears and glenohumeral instability. Other causes that may lead to compression are the above-mentioned suprascapular notch and anterior anatomical variations of coraco-scapular ligament, degenerative conditions like suprascapular ligament ossifications or traumatic conditions like suprascapular notch fractures, scar tissue after a distal clavicle fracture and shoulder dislocations or distraction. Post-traumatic conditions like arthritis, heterotopic ossifications and iatrogenic anesthesiological injuries or shoulder injections have also been described [1,3,14,15,23,35,36]. Furthermore, surgical procedures, such as distal clavicle excision or any posterior approach to the shoulder, can injure the nerve [37,38]. Recent research suggests rotator cuff tears as a cause of suprascapular neuropathy. Some authors have shown that medial retraction of the supraspinatus tendon causes a reduction in the angle along the nerve course with increased traction of the nerve at the spinoglenoid notch [39]. There is an additional group of secondary etiologies provoked by systemic conditions. It includes a wide range of conditions including diabetes, pregnancy, hypothyroidism and viral neuritis. Although these conditions are quite frequent, they very rarely affect the suprascapular nerve. 2.3. Clinical Evaluation Diagnosis of suprascapular nerve entrapment is difficult and must be considered in all patients with unexplained shoulder pain, especially in patients involved in repeated overhead activities [23]. The medical history and clinical evaluation are almost never pathognomonic because clinical presentation of the suprascapular neuropathy often mimics other more common shoulder pathologies, radiculopathy and a plexus pathology, with which the suprascapular neuropathy can coexist. This is the reason for missed, misdiagnosed or late clinical confirmation [10]. Few years ago, suprascapular entrapment was considered a diagnosis for exclusion by some authors [4,11]. After a focused anamnesis emphasizing a history of penetrating trauma, previous shoulder surgeries, anesthetic shoulder injections or overhead activities, a clinical examination should be made. Symptoms can start suddenly after a specific shoulder trauma or insidiously without any history of injury. In these cases, the clinician should consider the differential diagnosis along with neuralgic amyotrophy and the hourglass-like constriction neuropathy. Neuralgic amyotrophy is a rare neurological disorder that affects the peripheral nervous system. It is characterized by an acute and sudden onset of pain in the upper limb followed by multiple atrophy and motor weakness and slow recovery. On the other hand, hourglass-like constriction neuropathy is considered a neurological disorder brought on by fascicular constriction of one or more peripheral nerves, unrelated to intrinsic or extrinsic compression or trauma. The presentation often mimics suprascapular nerve palsy. The diagnosis is challenging as it is not observed in conventional magnetic resonance imaging (MRI) and is usually detected during exploratory surgery, which has even been proven to be beneficial. Patients with a suprascapular nerve palsy typically report a non-specific, deep, dull and J. Clin. Med. 2020, 9, 2331 5 of 15 continuous pain located in the upper-posterior-lateral region of the shoulder. In some instances, there is accompanying neck and arm irradiation, with or without suprascapular muscle atrophy (Figure 2) and weakness. A complete glenohumeral and acromioclavicular joint assessment is called for to exclude other concomitant pathologies [10,40]. Moreover, both shoulders must be inspected comparatively. Patients with spinoglenoid notch compression often present isolated infraspinatus muscle atrophy. If the nerve injury is distal to the sensory supraspinatus nerve fibers, there will not be a history of shoulder pain [41]. On the other hand, supraspinatus and infraspinatus atrophy suggest a more proximal compression [10]. Supraspinatus fossa atrophy is considered a pathognomonic sign of suprascapular entrapment [4,11]. Additionally, tenderness over the suprascapular or spinoglenoid notch may be found [34]. Clinical evidence shows that adduction and internal rotation can exacerbate pain because this position stretches the spinoglenoid ligament, increasing nerve compression [9]. Lafosse has described the suprascapular stretch test. While standing behind the patient, the clinician gently turns the patient’s head to the side opposite to the shoulder that needs to be evaluated while pressing down on the patient’s shoulder with the other hand. This test is positive if the patient reports pain at the posterior aspect of the shoulder (Figure 3A) [23,29]. Another helpful test is the “cross arm adduction test” described by Plancher. The patients are asked to over adduct and internally rotate the arm. If the patient refers to an exacerbation of the pain at the posterior aspect of the shoulder, the test is positive (Figure 3B). Nerve compression at the suprascapular notch may lead to over a 75% loss in strength in abduction and external rotation [10]. Conversely, entrapment at the spinoglenoid notch is better tolerated thanks to the compensation mechanisms of the muscles in the shoulder region involving the deltoid and infraspinatus muscles. A helpful way to differentiate the suprascapular entrapment from other shoulder pathologies is the local injection of anesthetic in the notch. The use of fast-acting anesthetic is strongly recommended. It may be injected into the spinoglenoid notch to confirm the diagnosis of suprascapular nerve entrapment. The needle is placed 4cm medial to the posterolateral corner of the acromion. Plancher et al. suggested performing US ultra-sound guided injection into the spinoglenoid notch to increase precision. This test is positive if the patients reports pain relief. Additionally, a cross-arm adduction test is then performed with reduced or no pain. 2.4. Radiological Evaluation The medical history and clinical evaluation must guide any request for diagnostic studies. If suprascapular neuropathy is suspected, plain radiographs are mandatory. Standard X-rays like the anteroposterior, lateral, axial, Grashey and scapular outlet views may reveal concomitant shoulder diseases. The “Stryker notch” view is a specific view for suprascapular and spinoglenoid notch evaluation that should be included in the radiographic evaluation (Table 2). Additionally, the Zanca view can be useful to evaluate the acromioclavicular joint [39]. A CT scan may be useful to detect bone lesions like fractures or anatomic variations that might compress the nerve. An MRI is the best way to identify space occupying lesions (Figure 4), to assess supra-spinatus and infra-spinatus muscles atrophy and to examine the course of the nerve through bony prominences [10,28]. Three main signs must be looked for in the MRI. These are edema, atrophy and fatty degeneration of the muscles. Edema of the supra-spinate and infra-spinate muscles is a pathognomonic sign of suprascapular neuropathy. It may be detected some days after a trauma or, in some cases, at the onset of electromyography (EMG) abnormalities. Generally, muscle edema continues to increase after a trauma, reaching a maximum after 2–4 weeks [28,41]. Its intensity and duration are proportional to the severity and the onset of the lesion. However, neuropathy-related muscle edema in sportspeople can be seen even more than 6 months after the trauma. While muscle atrophy usually occurs quickly, fatty degeneration of the muscles has a late onset. Both are less useful signs in the evaluation of the neuropathy because they are not predictive of the severity [28]. Mucoid cysts are the most frequent space occupying lesions causing secondary compression of the suprascapular nerve. They are J.J. Clin. Clin. Med. Med. 2020, 2020, 9, 9, xx FOR FOR PEER PEER REVIEW REVIEW 66 of of 14 14 J. Clin. Med. 2020, 9, 2331 6 of 15 fatty degeneration of the muscles has a late onset. Both are less useful signs in the evaluation of the neuropathy because they are not predictive of the severity [28]. Mucoid cysts are the most frequent linked to three main shoulder lesions, the type 2 SLAP lesion, the postero-superior impingement syndrome space space occupying occupying lesions lesions causing causing secondary secondary compression compression of of the the suprascapular suprascapular nerve. nerve. They They are are linked linked or posterior instability. Mucoid cysts are usually clearly identified with ultrasounds, but these lesions to to three three main main shoulder shoulder lesions, lesions, the the type type 22 SLAP SLAP lesion, lesion, the the postero-superior postero-superior impingement impingement syndrome syndrome always communicate with the joint. Therefore, they can be easily found by means of MRI-arthrography or or posterior instability. Mucoid cysts are usually clearly identified with ultrasounds, bu CT-arthrography. Unfortunately, some lesions may be undetectable because of obstructed communication tt these these lesions lesions always always communicate communicate withwith the the joint. joint. Therefore, Therefore, theythey can can be be easily easily found found by by means means with the joint and could lead to a missed diagnosis. Finally, CT angiography can be useful in some rare of of MRI-arthrography MRI-arthrography or or CT-arthrography. CT-arthrography. Unfortunately, Unfortunately, some some lesions lesions may may be be undetectable undetectable because because cases caused by suprascapular artery compression due to its anatomical variation [28]. A further method of of obstructed obstructed communication communication with with the the joint joint and and could could lead lead toto aa missed missed diagnosis. diagnosis. Finally, Finally, CTCT for studying angiography the can morphology and be useful in therare some course casesofcaused the nerve is the high-resolution by suprascapular 3T MR Neurography. artery compression due to its This technique is quite helpful. Sadly, it is not widely available. It can directly show the nerve abnormality anatomical anatomical variation variation [28]. [28]. A A further further method method forfor studying studying thethe morphology morphology and and the the course course ofof the the nerve nerve as well as secondary muscle denervation changes. [42]. is is the the high-resolution high-resolution 3T3T MR MR Neurography. Neurography. This This technique technique is is quite quite helpful. helpful. Sadly, Sadly, it it is is not not widely widely available. It can directly show the nerve abnormality as well as secondary muscle denervation Table 2. Name, description and sample of the main specific x-ray views. changes. [42]. X-ray X-ray Views Views X-ray Views Description Description Description Sample Sample Sample Grashey Grashey view view Obtained Obtained with with the the patient Obtained patient rotated rotated with the 35–45° 35–45° patient rotated (or AP towards towards Grashey view (or AP oblique the the affected35–45 towards the affected has affected shoulder ◦ shoulder or or the the beam beam has oblique oblique to be tilted laterally shoulder view) from shoulder or the standard the beam has toAP view. be tilted shoulder shoulder laterally from the standard AP view. view) view) The patient is in supine position; the The The patient patient is is in supine inupper supine position; position; thethe upper upper limb is abducted and limb is abducted and externally rotated with externally rotated with the hand Stryker Stryker notch notch the the hand hand supporting supporting the back thethe supporting back of the ofof back thethehead headand head and and Stryker notch view view view the the elbow elbow pointed pointedthe towards elbow towardspointed the towardsX-ray the ceiling. ceiling. the X-ray◦ beam is angledceiling. X-ray beam 10° cephalad, is angled centered on 10 the cephalad, centered on the coracoid process. coracoid process. The The patient patient is is placed placed in in 60° 60° anterior anterior oblique oblique The patient is placed in 60◦ anterior position. The arm position. The arm is left in neutral is leftposition. oblique in neutral position arm is leftor Theposition orinin in Scapular the sling. By feeling the scapula, adjust the neutral position or in the sling. By Scapular outlet view outlet outlet view view position position to to get get the scapula thefeeling scapula theperpendicular perpendicular to to the scapula, adjust the the position film. to get the scapula film. perpendicular to the film. Table Table 2. 2. Name, Name, description description and and sample sample of of the the main main specific specific x-ray x-ray views. views. local local injection injection of of anesthetic anesthetic in in thethe notch. notch. The The use use of of fast-acting fast-acting anesthetic anesthetic is is strongly strongly recommended. recommended. It It maymay bebe injected injected into into thethe spinoglenoid spinoglenoid notchto to notch confirm confirm thethe diagnosis diagnosis of ofsuprascapular suprascapular nerve nerve entrapment. The needle is placed 4cm medial to the posterolateral corner of entrapment. The needle is placed 4cm medial to the posterolateral corner of the acromion. Plancher the acromion. Plancher et et al.al. suggested suggested performing performing USUS ultra-sound ultra-sound guided guided injection injection intointo thethe spinoglenoid spinoglenoid notch notch to to increase increase precision. precision. This This test test is is positive positive if if the the patients patients reports reports pain pain relief. relief. Additionally, Additionally, a a cross-arm cross-arm adduction adduction J. Clin. Med. 2020, 9, 2331 7 of 15 test test is is then then performed performed with with reduced reduced oror nono pain. pain. Figure Figure 2. A Figure 2. AA clinical 2. clinical clinical photograph photograph of a of photograph of a patient patient with suprascapular with suprascapular a patient with nerve compression nerve compression suprascapular nerve shows shows the compression thethe resultant shows resultant atrophy in the resultant atrophy in in thethe supraspinatus atrophy supraspinatus fossa. supraspinatus fossa. fossa. (A) (A) (B)(B) J. Clin. Med. 2020, 9, x FOR PEER REVIEW 7 of 14 Figure Figure 3. 3. (A)(A) Suprascapular Suprascapular stretch stretch test; test; (B)(B) Cross-arm Cross-arm adduction adduction test. test. 2.4. 2.4. Radiological Radiological Evaluation Evaluation TheThe medical medical history history andand clinical clinical evaluation evaluation must must guide guide anyany request request forfor diagnostic diagnostic studies. studies. If If suprascapular suprascapular neuropathy neuropathy is is suspected, suspected, plain plain radiographs radiographs areare mandatory. mandatory. Standard Standard X-rays X-rays like like thethe anteroposterior, anteroposterior, lateral, lateral, axial, axial, Grashey Grashey andand scapular scapular outlet outlet views views may may reveal reveal concomitant concomitant shoulder shoulder diseases. diseases. The The “Stryker “Stryker notch” notch” view view is is a specific a specific view view forfor suprascapular suprascapular andand spinoglenoid spinoglenoid notch notch evaluation evaluation thatthat should should bebe included included in in thethe radiographic radiographic evaluation evaluation (Table (Table 2).2). Additionally, Additionally, thethe Zanca Zanca view can be useful to evaluate the acromioclavicular joint [39]. view can be useful to evaluate the acromioclavicular joint [39]. A CT scan may be useful to detect A CT scan may be useful to detect bone bone lesions lesions likelike fractures fractures oror anatomic anatomic variations variations that that might might compress compress thethe nerve. nerve. AnAn MRIMRI is is thethe best best waywayto toidentify identifyspace spaceoccupying occupyinglesionslesions(Figure (Figure4),4),to toassess assesssupra-spinatus supra-spinatusand andinfra-spinatus infra-spinatus muscles muscles atrophy atrophy andand to to examine examine thethe course course of of thethe nerve nerve through through bony bony prominences prominences [10,28]. [10,28]. Three Three main main signs signs mustmust bebe looked looked forfor in in thethe MRI. MRI. These These areare edema, edema, atrophy atrophy and and fatty fatty degeneration degeneration of of thethe muscles.Edema muscles. Edemaof ofthethesupra-spinate supra-spinateand andinfra-spinate infra-spinatemusclesmusclesis isa apathognomonic pathognomonicsign signof of suprascapular suprascapular neuropathy. neuropathy. It may It may bebe detected detected some some daysdays after after a trauma a trauma or,or, in in some some cases, cases, at at thethe onset onset of of electromyography electromyography (EMG) (EMG) abnormalities. abnormalities. Generally, Generally, muscle muscle edema edema continues continues to to increase increase after after a a trauma, reaching a maximum after 2–4 weeks [28,41]. Its intensity and duration are proportional to to trauma, reaching a maximum after 2–4 weeks [28,41]. Its intensity and duration are proportional Figure thethe severity Figure 4. 4.Patient severity and and Patient affected thethe onset onset affected by of of paralabral the by the lesion. lesion. paralabral cyst of of the However, However, cyst right shoulder: coronal neuropathy-related the neuropathy-related right shoulder: coronal (leftimage) muscle muscle (left image) edema edema and and intransverse sportspeople intransverse sportspeople can (right canbe be image) seen seen (right even image) views even more viewsof more an than MRI of than an 6 with months MRI contrast 6 months after with contrast agent. after the theagent. The trauma. arrows trauma. The While arrows highlight While muscle muscle the highlight cyst. atrophy atrophy the usually cyst.usually occurs occurs quickly, quickly, 2.5. Electrodiagnostic Tests 2.5. Electrodiagnostic Tests The gold standard diagnostic tests for suprascapular neuropathy that allows for the detection of the The gold standard diagnostic tests for suprascapular neuropathy that allows for the detection of level of the injury are the EMG and nerve conduction velocity (NCS) tests [10]. They have from 70% to more the level of the injury are the EMG and nerve conduction velocity (NCS) tests [10]. They have from than 90% sensitivity in detecting muscle fiber denervation [10,23,32,34]. The main findings in peripheral 70% to more than 90% sensitivity in detecting muscle fiber denervation [10,23,32,34]. The main neuropathies are an increase in motor pulse latency and signs of denervation like fibrillation and sharp findings in peripheral neuropathies are an increase in motor pulse latency and signs of denervation like fibrillation and sharp waves. Occasionally, chronic neuropathic shoulder pain has negative results in electrodiagnostic tests [23]. It may be because they do not detect “small fiber” damage (i.e., unmyelinated and thinly myelinated pain fibers) [4,11]. J. Clin. Med. 2020, 9, 2331 8 of 15 waves. Occasionally, chronic neuropathic shoulder pain has negative results in electrodiagnostic tests [23]. It may be because they do not detect “small fiber” damage (i.e., unmyelinated and thinly myelinated pain fibers) [4,11]. 2.6. Treatment The etiology of suprascapular neuropathy is the most relevant factor in choosing the appropriate treatment [10]. There is no consensus on the first steps in the treatment of suprascapular nerve entrapment. However, most authors advise starting suprascapular neuropathy treatment non-operatively unless nerve compression is caused by a mass [10,32]. If non-operative treatment fails, surgical decompression is recommended. Furthermore, Plancher et al. suggest non-operative treatment for a minimum time for patients who present a visible atrophy of the infra-spinatus. Regardless, the optimal duration of non-operative treatment remains unclear [32,39]. When there is no atrophy, no remarkable finding on an electromyogram (EMG), and no evidence of a labral tear or ganglion cyst, but weakness and pain are present, the recommendation is a 6-month course of non-operative treatment before considering any type of operative intervention [32]. 2.6.1. Non-Operative Treatment It requires avoiding overhead activity, but a shoulder rehabilitation program and anti-inflammatory therapy with NSAIDs should be followed. Physical exercise must focus on shoulder flexibility and on periscapular and deltoid musculature strengthening. Rehabilitation exercises must be closely monitored in order to avoid any further injury to the nerve during its healing process. Evidence shows that non-operative treatment tends to have bad outcomes in patients whose symptoms continue for more than 6 months and in patients with muscle atrophy, space occupying lesions and massive rotator cuff tears. In such cases, early surgical intervention may be considered because the delay in nerve decompression could result in incomplete restoration of muscle function. The reasons why patients improve with non-operative treatment is not known but it may be explained by compensatory muscle mechanisms [10,41]. The success rate of non-operative treatment remains unclear. 2.6.2. Operative Treatment Indications for surgical treatment are nerve entrapment by space occupying lesions and the failure of nonoperative management [10]. It has been demonstrated that patients with soft tissue suprascapular nerve entrapment experience better outcomes with surgical treatment and arthroscopic intervention should be preferred to open techniques, when possible [10,23,32,43,44]. Cyst ganglion aspiration under ultrasound or CT guidance carries a 75% to 100% rate of failure or recurrence. Therefore, surgery is indicated [10,32]. There is no consensus as to whether a labral lesion and ganglion cyst should be treated all together or not [32]. Some authors recommend labral repair and cyst decompression in the same procedure [45,46]. However other authors have argued that labral repair without cyst decompression was the most appropriate treatment [47,48]. Some authors recommend wide arthroscopic decompression of the suprascapular nerve at both the spinoglenoid and the suprascapular notches in patients with dynamic nerve compression [8,10,49]. Finally, Lafosse recommends surgical release of the suprascapular nerve in symptomatic patients regardless of the electromyography findings given that it is a quick and safe procedure with great potential benefits for the patients. He underlined that suprascapular nerve entrapment is often a dynamic condition, so it is not always seen in an electromyography [23]. J. Clin. Med. 2020, 9, 2331 9 of 15 2.6.3. Open Approach Open suprascapular notch decompression: a transverse skin incision parallel with the edge of the scapular spine or a curved incision medial to the acromioclavicular joint is made. The trapezius muscle is split by blunt dissection. The supraspinatus muscle is then identified and dislocated posteriorly. The suprascapular notch is then identified at the base of the coracoid. The suprascapular neurovascular bundle and the transverse scapular ligament can be seen. The localization of the neurovascular bundle must be performed with care because of its anatomical variations. The transverse scapular ligament is then released, and the nerve can be freed. If necessary, further nerve decompression can be obtained by a deepening or widening of the notch [10,35,50,51]. Open spinoglenoid notch decompression: a skin incision is made starting approximately 3 cm medial to the posterolateral corner of the acromion and then extended downward toward the posterior axillary skin fold. The deltoid muscle is split by blunt dissection. The fascia is opened and the infraspinatus muscle belly is dislocated inferiorly to expose the spinoglenoid notch. A consistent ligamentous structure from the lateral side of the scapular spine to the posterior aspect of the shoulder capsule is now visible. This spinoglenoid ligament is cut from the edge of the scapular spine. The nerve can be released by using scissors proximally and blunt dissection inferiorly, taking care to avoid nerve and vessel injuries. If a ganglion cyst is present, it is well exposed after ligament release and can be excised [44]. 2.6.4. Arthroscopic Approach Although the arthroscopic suprascapular nerve release technique is a relatively novel technique, it must be considered the gold standard [5,10,23,29,33,43,52]. Most of the work on this procedure has been carried out on cadaveric specimens but many authors have demonstrated the procedure’s safety in experienced hands [10]. Hemostasis is critical during the whole procedure. Adequate pump pressure (50–55 mm Hg) and hypotensive anesthesia (systolic blood pressure, 100–110 mm Hg) are recommended [43]. Suprascapular notch compression: with the patient in the beach chair position, a standard diagnostic arthroscopy is performed using a posterior portal. Plancher et al. suggest avoiding doing glenohumeral joint inspection first or carrying it out as briefly as possible to prevent joint swelling [32,39]. An arthroscopic trocar is then gently introduced through the suprascapular nerve portal of Lafosse. While creating this portal, attention must be paid to the suprascapular nerve and artery, which are located about 2 mm medial to this portal (Figures 5 and 6). A blunt dissection is then carried out around the transverse scapular ligament, taking care to avoid artery and nerve damage. Then, arthroscopic scissors are introduced through the Neviaser portal from where the transverse scapular ligament can be cut, thus releasing the suprascapular nerve. As described by Krishnan et al., the suprascapular nerve can be visualized and decompressed anteriorly to the coracoclavicular ligaments [11,23,43,53]. If further decompression is needed, deepening and widening of the suprascapular notch (notchplasty) can be performed. Some authors advise against notchplasty with a burr because of the possibility of excessive postoperative scar tissue and recurrent compression of the nerve [23]. After nerve release, other concomitant lesions can be treated [10,29,52]. As previously stated, the arthroscopic procedure is now considered the gold standard technique. It is a quick and safe procedure in experienced hands. The learning curve is not predictable as it is a not frequent performed surgery. Very good clinical results have been described, especially in those patients with no signs of atrophy. Most of the patients can return to sport activities at the same level or higher within 8 months [8,10,22,39]. nerve release,procedure arthroscopic other concomitant lesions can is now considered the be treated gold [10,29,52]. standard As previously technique. It is a quick stated, the and safe arthroscopic procedure is now considered the gold standard technique. It procedure in experienced hands. The learning curve is not predictable as it is a not frequent is a quick and safe procedure performed in experienced surgery. hands. Very good Theresults clinical learning havecurve beenisdescribed, not predictable as init those especially is a not frequent patients with performed no signs ofsurgery. atrophy.VeryMostgood clinical of the results patients canhave been return to described, especially sport activities at theinsame thoselevel patients with or higher no J. Clin. signs of atrophy. Med. 82020, within Most of the patients can return to sport activities at the same level or higher 9, 2331[8,10,22,39]. months 10 of 15 within 8 months [8,10,22,39]. . Figure Figure 5. 5.Schematic Schematictop topview viewofofthe the right right shoulder shoulder with with the the refferal refferal point pointfor forestablishing establishingNeviaser Neviaser Figure (blue 5. Schematic cross) and top view(green LaFosse of the right cross)shoulder portals. with C: the refferalSN: coracoid, pointsuprascapular for establishing Neviaser nerve, SA: (blue cross) and LaFosse (green cross) portals. C: coracoid, SN: suprascapular nerve, SA: suprascapular (blue cross) suprascapular and LaFosse artery, SNo: (green cross) suprascapular portals. notch, SGNo: artery, SNo: suprascapular notch, SGNo: spino-glenoid notch. C: coracoid, spino-glenoid SN: suprascapular notch. nerve, SA: suprascapular artery, SNo: suprascapular notch, SGNo: spino-glenoid notch. Figure 6. Neviaser Figure portal 6. Neviaser (1) is(1)placed portal approximately is placed 1 cm1medial approximately to theto cm medial acromion, between the acromion, the clavicle between the Figure andclavicle6.and Neviaser the scapular the portal spine. (1) LaFosse scapular isportal spine. placed is approximately LaFosselocated portal2-3 is cm 1medial cm2-3 located medial tocm toNeviaser the acromion, themedial portal. to the between Coracoid Neviaser the (C), portal. clavicle acromion Coracoid and (C),the (A). scapular acromion spine. LaFosse portal is located 2-3 cm medial to the Neviaser portal. (A). Coracoid (C), acromion (A). Spinoglenoid Spinoglenoid notch decompression: notch decompression:the the patient is prepared patient in theinbeach-chair is prepared position. the beach-chair Two portals position. Two must be made: Spinoglenoid portals the viewing must be made:notch portal and the thedecompression: working viewing portal the portal. and patient They are is prepared the working placed in theare portal. They respectively beach-chair 8 cm andTwo position. placed respectively 8 4cm cm medially portals and 4 cm to mustthebeposterolateral made: medially cornerportal of the theposterolateral to the viewing acromion, and corner the just inferior working of the portal. acromion, toinferior justTheytheare scapula to the spine. placed The respectively scapula trocar cmis 8The spine. introduced and 4 cm into the mediallyviewing to the portal and directed posterolateral cornertowards of the the infraspinatus acromion, just fossa. inferior The to trocar the is scapula trocar is introduced into the viewing portal and directed towards the infraspinatus fossa. The trocar then directed spine. The close to the trocar working portal is introduced into into the the spinoglenoid viewing portal and notch. directedAttowards this point, the to ensure optimal infraspinatus fossa.visualization, The trocar Plancher et al. suggest sweeping the trocar under the roof of the infraspinatus spine feeling the curvature. Then, the trocar is introduced into the working portal in order to clear the soft tissue and the spinoglenoid ligament using a radiofrequency tool or non-aggressive shaver with the suction turned off. The ligament can be resected and the nerve safely released [32]. Complications after arthroscopic suprascapular nerve release are uncommon. Special care must be taken during dissection, shaving or electrocautery to avoid iatrogenic injury to the suprascapular nerve and to the relative vessels. Anatomic variations may be present and must be recognized [11,43]. Postoperative rehabilitation is guided by concomitant pathology. All patients must utilize a sling postoperatively for comfort. In cases of dynamic suprascapular neuropathy at the spinoglenoid notch, patients can start J. Clin. Med. 2020, 9, 2331 11 of 15 passive shoulder exercise and Codman’s exercise immediately [44]. In patients with a surgical labral repair, wearing a sling for 3 weeks is advisable. Shoulder strengthening exercises can start at 4–8 weeks postoperatively in cases of isolated suprascapular nerve decompression at the spinoglenoid notch or when shoulder motion is at least 80% of the contralateral shoulder in the other cases [11]. 3. Results In the cases of dynamic primary compression, the overall response to conservative management has good outcomes. Pain relief is achievable in more than 80% of the cases and almost all the patients can return to sport activities within 3 months [10]. After evaluating all clinical features, including the course of follow-up, the timing of return-to-sport activity must be carefully planned, considering the differences in patient characteristics. In patients with painless infraspinatus muscle atrophy without a space occupying lesion, function is usually recovered with non-operative care. While significant pain relief is achieved in 80% to 96% of patients, regaining muscle strength and function and atrophy is less predictable [10,54]. After surgical suprascapular notch decompression, most reports show a good return in terms of pain relief and an improvement in supraspinatus muscle strength. Some authors have found that 80% of the treated patients showed improvement in the strength and atrophy of the supraspinatus muscle, but only 50% showed improvement in the infraspinatus [9,10,39]. In the cases of spinoglenoid notch nerve compression, several authors have reported excellent results after operative management, as well. Authors described their own experience, in which the most satisfied patients (97%) were treated with labral repair and open or arthroscopic decompression of the cyst, whereas the less satisfied patients were those treated with isolated labral repair (67%) or needle aspiration of the cyst (64%), or in people treated non-operatively (53%) [2,9]. The outcomes of nerve release and rotator cuff repair vary widely as the degree of fatty degeneration of the rotator cuff, the reciprocal influence of suprascapular nerve palsy and rotator cuff tendon tears on have muscle pathology are unclear. Debate continues as to how retracted cuff tears can lead to suprascapular neuropathy and whether suprascapular palsy or tendon retraction cause muscle fat degeneration [8,13,26,55]. In all the cases without a clear mechanical cause for suprascapular neuropathy, conservative treatment can usually best resolve the symptoms (Table 3) [56–59]. Table 3. Main diagnosis with suggested treatment. Condition Treatment Pain and weakness with no atrophy, no remarkable 6months conservative treatment. If it fails, consider findings on electromyogram (EMG), and no relevance surgical arthroscopic nerve release of labral tear or ganglion cyst Attemption of conservative treatment for a minimum of 1 month; the optimal length of non-operative Patients with visible atrophy on physical examination treatment remains unclear (32,39). After that, consider the surgical treatment Surgical treatment. In case of ganglion cyst diagnosis, Space occupying lesion compression best result are given by labral repair and open or arthroscopic decompression of the cyst (2,9) 4. Conclusions Suprascapular nerve entrapment is an increasingly recognized and diagnosed shoulder lesion, but it is still rather infrequent. Diagnosis may be complex, whereas its treatment is safe, and it has a great success rate. 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