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DOI: 10.1055/s-0034-1366089
Ultrasound Imaging of the Axillary Nerve and its Role in the Diagnosis of Traumatic Impairment
Sonografie des Nervus Axillaris und ihre Rolle in der Diagnostik der traumatischen Läsion- Abstract
- Zusammenfassung
- Introduction
- Materials and Methods
- Results
- Discussion
- Conclusion
- References
Abstract
Purpose: The axillary nerve (AN) is frequently injured during shoulder trauma and imaging is required to define the site and extent of nerve injury. However, the AN has a rather complex course through several soft tissue compartments of the shoulder and axilla. Therefore, imaging of the nerve with MRI and sonography is troublesome. Thus detection and sonographic assessment bases on thorough knowledge of local topography.
Materials and Methods: This investigation aimed at defining reliable anatomical landmarks for AN-sonography in 5 volunteers and later validating the proposed sonographic examination protocol in 10 unselected patients.
Results: With strict adherence to the proposed examination algorithm, sonography of the AN was feasible in all volunteers and patients. Furthermore, sonographic findings correlated nicely with the golden standard “surgical exploration” concerning severity and topography of neural impairment.
Conclusion: Based on our study results we propose our algorithm for AN-sonography as the first-line imaging tool for the assessment of axillary nerve trauma.
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Zusammenfassung
Ziel: Der N. axillaris wird relativ häufig im Rahmen von Schulterverletzungen lädiert und die Bildgebung sollte dazu dienen, die exakte Lokalisation und das Ausmaß der Schädigung zu definieren. Der Nerv zeichnet sich allerdings durch einen ziemlich komplizierten Verlauf durch mehrere Kompartimente des Schultergürtels und der Axilla aus. Daher ist die Darstellung des Nervens sowohl mit MRT als auch Sonografie schwierig und basiert auf profunder Kenntnis der lokalen Topografie.
Material und Methode: Diese Studie zielte einerseits darauf ab klare Landmarken für die Sonografie des Nervus axillaris an 5 Probanden zu definieren und deren Nutzen anschließend an 10 unselektierten Patienten zu verifizieren.
Ergebnisse: Bei strikter Befolgung des etablierten Untersuchungs-Algorithmus war eine Beurteilung des N. axillaris in allen Probanden und Patienten möglich. Darüber hinaus zeigte sich eine gute Korrelation der sonografischen Befunde mit dem goldenen Standard „chirurgische Exploration“ sowohl bezüglich Schwere als auch Topografie des neuralen Schadens.
Schlussfolgerungen: Basierend auf unseren Studienergebnissen empfehlen wir den vorgestellten Untersuchungsalgorithmus für die Sonografie des N. axillaris als Methode der ersten Wahl in der Abklärung einer Nervus axillaris Verletzung.
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Introduction
The axillary nerve (or circumflex nerve) leaves the brachial plexus, i. e.. the posterior cord together with the radial nerve. The axillary nerve (AN) contains fibers of the plexus segments C5 and C6 and is a mixed nerve: it supplies the deltoid and the teres minor muscle as well as the long head of the brachial triceps muscle and conveys sensory information of the shoulder joint and of the “regimental badge” area (i. e., the skin covering the inferior part of the deltoid muscle) via its terminal branch, the superolateral cutaneous nerve [1 – 8].
Its course is rather complex: it resembles two merging semi-circular arches running inferiorly to the gleno-humeral joint (“pseudo-coronarily” oriented 1st arch; [Fig. 1]) to accompany the posterior humeral circumflex artery, and incompletely wrapping around the surgical neck of the humerus (axially oriented 2nd arch; [Fig. 1]). It exits the proper axillary space through a quadrilateral gap formed by the teres minor muscle above, the teres major muscle below, the long head of the brachial triceps muscle medially and the surgical neck of the humerus laterally to end up in its terminal motor and sensory branches.
Because of this complex regional anatomy, imaging of the axillary nerve in any perpendicularly oriented plane (such as used in MRI) is difficult if not impossible even by using sophisticated and time-consuming thin-sliced or 3 D MRI: the only meaningful information gained with such techniques is indirect signs of impairment and/or restriction of tissue along the “assumed” course of the AN such as hematoma. Assessment of the nerve itself, i. e., clear definition of the severity of intrinsic impairment, however, is usually not achieved!
In general, peripheral nerve imaging by ultrasonography (US) has gained its role over the last decade. High resolution power of US probes with frequencies presently up to 18 MHz was shown to depict even micro-anatomic features of peripheral nerves. Free orientation of a probe in any plane allows for nerve imaging along any course, however complex the topography! US imaging happens in real-time and in a bedside manner without complicated technical prerequisites. Still anatomical knowledge on the part of the investigator is key to success. Beyond basic knowledge of the topographic position of a nerve, anatomical landmarks help in nerve identification and definition of pathology [9 – 18].
This study aims at basic clarification of ultrasound imaging of the AN, by providing data on its typical topographic course and US aspects. Furthermore, basic information on the role of US in the assessment of an impaired AN is given.
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Materials and Methods
Technical prerequisites
All sonographic exams were performed on a Philips iU22® (Philips, Bothell, Washington, USA) with a 12 – 5 MHz or 17 – 5 MHz broadband linear array probe. All regions were always scanned on two perpendicular planes according to the algorithm and landmarks defined below. All images were stored in the institution's Agfa® PACS. Data were handled according to the World Medical Association Declaration of Helsinki (59th WMA Assembly, Seoul, 2008). Institutional review board approval was further granted by means of a general waiver for studies with retrospective data analysis (Ethikkommission, Med. Univ. Innsbruck; 2009-02-20).
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US topography and technique in volunteers
The sonographic algorithm was defined in a preliminary study on 5 healthy volunteers (age: 28 – 53, mean: 37.8 years, 3 males and 2 females). Volunteers were recruited from the department staff. All volunteers had no history of previous shoulder trauma and BMI was within normal range.
For examination of the inferior brachial plexus, axilla and axillary nerve, the volunteers/patients were positioned in a comfortable position, ideally in an ABER (Abduction External Rotation) position of the gleno-humeral joint ([Fig. 2]) but at least in marked abduction to achieve sufficient accessibility of the axilla with the US probe.
For sonography of the AN, we proposed the following algorithm:
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Start by defining the posterior fascicle of the cervicobrachial plexus from an antero-inferior approach, or, if the infraclavicular plexus is not sufficiently visualized (due to hematoma etc.), start by imaging the radial nerve at the level of the proximal third of the humerus. Using the first approach follow the posterior fascicle downward until it splits into the radial and axillary nerve, or, by the second approach, follow the radial nerve upward until it joins the axillary nerve to form the posterior fascicle ([Fig. 3], plane A and [Fig. 4]).
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From here (examined in the ABER position), the axillary nerve follows a rather straight course exiting the posterior fascicle (which is neighbored by the axillary artery) directly anterior to the subscapularis muscle together with the posterior circumflex artery of the humerus ([Fig. 3], plane B and [Fig. 5]).
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Nerve and artery continue together towards the posterior axillary fold, entering the lateral axillary gap next to the minor teres muscle ([Fig. 3], plane C and [Fig. 6]) and medial to the long head of the brachial triceps muscle: finally the nerve splits into its 3 separate, terminal branches: the upper anterior branch still together with the posterior circumflex artery of the humerus, the lower posterior branch running almost exactly in the opposite direction to meet the posterior parts of the deltoid and the minor teres muscle and the motor branch for the long head of the brachial triceps muscle ([Fig. 3]).
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Patient study
A subsequent US feasibility study with application of the sonographic examination protocol as defined in the volunteers was undertaken in 10 unselected male subjects (aged 43.8; ± 12.1 years), who suffered from blunt shoulder trauma (some with proximal fracture of the humerus) ± glenohumeral joint dislocation ([Table 1]). US was the initial imaging modality in these patients and the US investigator (HG) was blinded to any other clinical information beyond the suspicion of traumatic AN impairment. All subjects underwent a standard US investigation of the infraclavicular plexus with the main focus on the assessment of the posterior fascicle and its division into the axillary and radial nerve. Then the AN was followed according to the topographical landmarks and the procedure specified above.
pat. no. , sex, age |
incidence |
clinical presentation |
US |
surgery |
MRI |
electrophysiologic testing |
#1, male, 51 |
posterior glenohumeral dislocation |
deltoid muscle-paresis & anesthesia |
proximal, partial tear of AN[1], scar |
partial tear of the AN1 at the exit out of the posterior plexus-fascicle |
np |
complete block of AN1 |
#2, male, 50 |
anterior glenohumeral dislocation |
deltoid muscle-paresis & anesthesia |
strain of AN1, scar |
np |
np |
rapid reinnervation potential |
#3, male, 31 |
blunt shoulder trauma |
deltoid muscle-paresis |
strain of AN, scar |
np |
np |
np; rapid spontaneous improvement |
#4, male, 40 |
spontaneous |
regional pain |
diffuse swelling of AN1 |
np |
no pathologic finding |
No lesion |
#5, male, 51 |
blunt shoulder trauma |
deltoid muscle-paresis & anesthesia |
complete avulsion of AN1 |
complete avulsion of AN1 at the exit out of the posterior plexus-fascicle, scars |
np |
upper plexus damage |
#6, male, 15 |
posterior glenohumeral dislocation |
deltoid muscle-paresis & anesthesia |
complete, chronic avulsion of AN1 and neuroma at teres minor muscle |
complete avulsion of AN1 and neuroma at the teres minor muscle |
np |
complete block AN1 |
#7, male, 48 |
posterior glenohumeral dislocation |
deltoid muscle-paresis & anesthesia |
incomplete, chronic avulsion of posterior plexus-fascicle |
incomplete, chronic avulsion of posterior plexus-fascicle |
no pathologic finding |
complete block AN1 |
#8, male, 50 |
posterior glenohumeral dislocation |
deltoid muscle-paresis & anesthesia |
strain of AN1 |
np |
np |
mild signs of axonal damage |
#9, male, 50 |
posterior glenohumeral dislocation and prox. humerus fracture |
deltoid muscle-paresis & anesthesia |
restriction of AN1 by a scar |
np |
np |
signs of axonal and upper plexus damage |
#10, male, 52 |
bony tear of the major humerus tubercle |
deltoid muscle-paresis & anesthesia |
restriction of AN1 by a scar |
np |
no pathologic finding |
incomplete block at the level of AN1/radial nerve/ posterior plexus-fascicle (?) |
1 AN = axillary nerve; np = not performed
Nerve damage was assessed as minor (no rupture) or major (incompletely or completely ruptured). A minimally damaged nerve without interrupted fascicular elements was defined as sectional nerve thickening with reduced or lost fascicular pattern, more intense hypoechogenic texture including loss of a sharp outer lining, thus indicating segmental neural edema.
Data of electrophysiologic testing, MRI or other investigations were evaluated retrospectively for this study but were not initially known to the investigator!
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Results
Topographic definition of the AN
With strict adherence to the proposed examination protocol ([Fig. 3], [4], [5], [6]) depiction of the AN in its 3 crucial segments (proximal segment: exit off the posterior fascicle of the plexus; middle segment: course of the AN through the subscapular muscle and next to the glenohumeral joint capsule, respectively; distal segment: course through the axillary gap) was feasible in all volunteers and patients. The volunteers showed normal axillary nerve anatomy, without presence of any variations in the course or size of the nerve.
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Patient study
In 4 subjects major lesions (i. e., lesions requiring immediate surgical exploration) were detected by US. 3 of these were proper axillary-nerve lesions ([Fig. 5 a, b]) and 1 of these was a partial rupture of the posterior fascicle (neuroma-in-continuity; [Fig. 6 a, b]). In 6 other subjects US excluded major impairment, thus indicating observation of the patients under conservative management.
In all but one subject, electrophysiological data (EP) was available for retrospective correlation with ultrasound findings. In one of the 6 minor lesions, EP indicated major impairment and in 2 the localization of the site of impairment was equivocal ([Table 1]). In one of the 4 major lesions, EP data indicated superior brachial plexus damage although US demonstrated rupture of the AN ([Table 1]).
All patients with sonographically proven “major impairment” underwent surgery and data of surgical exploration were available to serve as the gold standard for correlation with ultrasound findings. Both the US definition of severity (major vs. minor lesions) and the topography/location of impairment were confirmed during surgery in all patients ([Table 1]).
MR studies were additionally evaluated retrospectively if available. Although MRI is still considered by many to be the imaging modality of choice for soft tissue and also peripheral nerve trauma, in our evaluation there was no correlation with US findings and presentation at surgical exploration: MRI suspected major lesions in two subjects with only minor impairment shown by US and electrophysiological testing. In the patient with partial rupture of the posterior fascicle that was surgically confirmed/correctly identified by US, MRI suggested a major AN lesion ([Table 1]).
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Discussion
According to our data, US is a suitable method for the evaluation of the AN after trauma. Clinical neurological estimation of the grade of axillary nerve damage is generally difficult especially in the acute/subacute setting. Electrophysiological testing is definitely important for definition of the degree of nerve impairment and especially for the demonstration of regeneration during post-injury follow-up, but the ability of electrophysiological testing for localization of the exact site of nerve damage is limited and so is the definition of the type of nerve damage [19 – 21]. Special forms of nerve discontinuity such as severe internal derangement combined with an intact outer nerve sheath or severe damage to surrounding tissue with indirect, i. e., extrinsic, compromise and restriction of a nerve by hematoma, bone fragments, etc. are clearly beyond the scope of electrophysiological testing and require high-resolution imaging. In this regard, even according to our admittedly limited data, US could serve as the imaging method of choice.
Data of MRI studies were available for comparison in only three of our patients, so we cannot draw any conclusions regarding the true potential of MRI for imaging the axillary nerve (i. e., with more sophisticated imaging protocols, 3 D MRI, higher field strength, or else). This must be gained from future prospective case-controlled studies. Still MR imaging – in contrast to sonography – was not able to definitively answer the clinician’s/surgeon’s most important question in any of our cases, i. e., regarding the presence of a lesion needing surgical exploration of the axillary nerve (with all its potentially harmful implications for the patient!).
With US we were able to demonstrate the severity and focus of damage in all of our patients. Although the topography of the course of the AN is rather complex and several compartments are met, the taxonomy is rather simple. Once the posterior fascicle of the brachial plexus and the radial nerve are identified, the branch-off of the axillary nerve is rather “self-explanatory”, i. e., the nerve which leaves the “axis” of the posterior fascicle towards the radial nerve must be the axillary nerve.
In our patients 50 % of the major lesions were located at the root of the axillary nerve, maybe due to considerable underlying mechanical load at this site. Here the AN must sustain strain forces and thus trauma may not only affect the AN but even extend into the posterior fascicle of the brachial-plexus. This segment of the nerve is the most easily accessible for sonography.
The more distal course of the nerve – where it passes the rather fatty, loose and sonographically inhomogeneous axillary fascia – is “rather” straight and this segment of the nerve was never found to be damaged in our patients presumably due to the minimal mechanical load in this area.
A second predilection for damage, however, was the axillary gap, where the AN exits the actual axillary compartment next to the teres minor muscle to enter the dorsal shoulder compartment. Here one of the 4 subjects with major nerve damage presented a complete avulsion most likely also due to underlying specific mechanical load and strain forces and thus specific neural stress.
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Conclusion
Under consideration of specific landmarks for defining the AN in its course through different distinct anatomical compartments, the AN can be reliably imaged by US. The so-called ABER (Abduction External Rotation) position provides good accessibility of all anatomical AN segments, and was feasible in our patients at least in a subacute and chronic setting. In some patients positioning in the ABER position may, however, be impossible in the acute setting because of injury and pain due to periarticular tissue damage or internal joint derangement of the shoulder.
Based on our data, we suggest that sonographic assessment must include:
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the posterior plexus-fascicle
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the proximal axillary nerve (the “leaving segment”)
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the segment of the axillary nerve neighboring the teres minor muscle (the “axillary gap-segment”)
as these seem to be the segments most probably impaired presumably due to specific mechanical load and thus neural stress.
While our results gained in a small patient sample are promising (although not ample for reliable statistical evaluation), the definitive role of US (and of MRI) in the definition of AN damage must be assessed in future prospective studies.
However, US should serve as the first-line (bedside) imaging modality for the assessment of suspected nerve damage in the acute/subacute and chronic setting to exclude major impairment at least in “regions of risk”. However, the very acute setting may be problematic as edema and suffusion can impair US imaging.
The true potential of US, however, lies in the ability to triage patients into “major” and “minor” categories, i. e., patients being inevitable candidates for surgery and patients who should be followed under conservative management without a need for further costly investigations with limited diagnostic value.
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References
- 1 Loomer R, Graham B. Anatomy of the axillary nerve and its relation to inferior capsular shift. Clin Orthop Relat Res 1989; 100-105
- 2 Apaydin N, Tubbs RS, Loukas M et al. Review of the surgical anatomy of the axillary nerve and the anatomic basis of its iatrogenic and traumatic injury. Surg Radiol Anat 2010; 32: 193-201
- 3 Apaydin N, Uz A, Bozkurt M et al. The anatomic relationships of the axillary nerve and surgical landmarks for its localization from the anterior aspect of the shoulder. Clin Anat 2007; 20: 273-277
- 4 Uz A, Apaydin N, Bozkurt M et al. The anatomic branch pattern of the axillary nerve. J Shoulder Elbow Surg 2007; 16: 240-244
- 5 Brown TD, Newton PM, Steinmann SP et al. Rotator cuff tears and associated nerve injuries. Orthopedics 2000; 23: 329-332
- 6 Hertel R, Lambert SM, Ballmer FT. The deltoid extension lag sign for diagnosis and grading of axillary nerve palsy. J Shoulder Elbow Surg 1998; 7: 97-99
- 7 Artico M, Salvati M, D'Andrea V et al. Isolated lesion of the axillary nerve: surgical treatment and outcome in 12 cases. Neurosurgery 1991; 29: 697-700
- 8 McIlveen SJ, Duralde XA, D'Alessandro DF et al. Isolated nerve injuries about the shoulder. Clin Orthop Relat Res 1994; 54-63
- 9 Peer S, Kovacs P, Harpf C et al. High-resolution sonography of lower extremity peripheral nerves: anatomic correlation and spectrum of disease. J Ultrasound Med 2002; 21: 315-322
- 10 Kopf H, Loizides A, Mostbeck GH et al. Diagnostic sonography of peripheral nerves: indications, examination techniques and pathological findings. Ultraschall in Med 2011; 32: 242-263 ; quiz 64–66
- 11 Kopf H, Mostbeck GH, Loizides A et al. Ultrasound-guided interventions at peripheral nerves: diagnostic and therapeutic indications. Ultraschall in Med 2011; 32: 440-456 ; quiz 57–59
- 12 Unterholzner V, Loizides A, Gruber H et al. Acute Carpal Tunnel Syndrome Due to Excessive Blood-Pressure-Measurement at the Wrist. Ultraschall in Med 2012; 33: 352-356
- 13 Gruber H, Peer S. The depiction of the cubital segment of the ulnar nerve by high resolution sonography--is it a helpful diagnostic tool for the assessment of the cubital tunnel syndrome?. Handchir Mikrochir Plast Chir 2009; 41: 13-17
- 14 Peer S, Bodner G, Meirer R et al. Examination of postoperative peripheral nerve lesions with high-resolution sonography. AJR Am J Roentgenol 2001; 177: 415-419
- 15 Bianchi S, Montet X, Martinoli C et al. High-resolution sonography of compressive neuropathies of the wrist. J Clin Ultrasound 2004; 32: 451-461
- 16 Loizides A, Peer S, Plaikner M et al. Punched nerve syndrome: ultrasonographic appearance of functional vascular nerve impairment. Ultraschall in Med 2012; 33: 352-356
- 17 Bodner G, Buchberger W, Schocke M et al. Radial nerve palsy associated with humeral shaft fracture: evaluation with US--initial experience. Radiology 2001; 219: 811-816
- 18 Bodner G, Huber B, Schwabegger A et al. Sonographic detection of radial nerve entrapment within a humerus fracture. J Ultrasound Med 1999; 18: 703-706
- 19 de Laat EA, Visser CP, Coene LN et al. Nerve lesions in primary shoulder dislocations and humeral neck fractures. A prospective clinical and EMG study. J Bone Joint Surg Br 1994; 76: 381-383
- 20 Berry H, Bril V. Axillary nerve palsy following blunt trauma to the shoulder region: a clinical and electrophysiological review. J Neurol Neurosurg Psychiatry 1982; 45: 1027-1032
- 21 Blom S, Dahlback LO. Nerve injuries in dislocations of the shoulder joint and fractures of the neck of the humerus. A clinical and electromyographical study. Acta Chir Scand 1970; 136: 461-466
Correspondence
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References
- 1 Loomer R, Graham B. Anatomy of the axillary nerve and its relation to inferior capsular shift. Clin Orthop Relat Res 1989; 100-105
- 2 Apaydin N, Tubbs RS, Loukas M et al. Review of the surgical anatomy of the axillary nerve and the anatomic basis of its iatrogenic and traumatic injury. Surg Radiol Anat 2010; 32: 193-201
- 3 Apaydin N, Uz A, Bozkurt M et al. The anatomic relationships of the axillary nerve and surgical landmarks for its localization from the anterior aspect of the shoulder. Clin Anat 2007; 20: 273-277
- 4 Uz A, Apaydin N, Bozkurt M et al. The anatomic branch pattern of the axillary nerve. J Shoulder Elbow Surg 2007; 16: 240-244
- 5 Brown TD, Newton PM, Steinmann SP et al. Rotator cuff tears and associated nerve injuries. Orthopedics 2000; 23: 329-332
- 6 Hertel R, Lambert SM, Ballmer FT. The deltoid extension lag sign for diagnosis and grading of axillary nerve palsy. J Shoulder Elbow Surg 1998; 7: 97-99
- 7 Artico M, Salvati M, D'Andrea V et al. Isolated lesion of the axillary nerve: surgical treatment and outcome in 12 cases. Neurosurgery 1991; 29: 697-700
- 8 McIlveen SJ, Duralde XA, D'Alessandro DF et al. Isolated nerve injuries about the shoulder. Clin Orthop Relat Res 1994; 54-63
- 9 Peer S, Kovacs P, Harpf C et al. High-resolution sonography of lower extremity peripheral nerves: anatomic correlation and spectrum of disease. J Ultrasound Med 2002; 21: 315-322
- 10 Kopf H, Loizides A, Mostbeck GH et al. Diagnostic sonography of peripheral nerves: indications, examination techniques and pathological findings. Ultraschall in Med 2011; 32: 242-263 ; quiz 64–66
- 11 Kopf H, Mostbeck GH, Loizides A et al. Ultrasound-guided interventions at peripheral nerves: diagnostic and therapeutic indications. Ultraschall in Med 2011; 32: 440-456 ; quiz 57–59
- 12 Unterholzner V, Loizides A, Gruber H et al. Acute Carpal Tunnel Syndrome Due to Excessive Blood-Pressure-Measurement at the Wrist. Ultraschall in Med 2012; 33: 352-356
- 13 Gruber H, Peer S. The depiction of the cubital segment of the ulnar nerve by high resolution sonography--is it a helpful diagnostic tool for the assessment of the cubital tunnel syndrome?. Handchir Mikrochir Plast Chir 2009; 41: 13-17
- 14 Peer S, Bodner G, Meirer R et al. Examination of postoperative peripheral nerve lesions with high-resolution sonography. AJR Am J Roentgenol 2001; 177: 415-419
- 15 Bianchi S, Montet X, Martinoli C et al. High-resolution sonography of compressive neuropathies of the wrist. J Clin Ultrasound 2004; 32: 451-461
- 16 Loizides A, Peer S, Plaikner M et al. Punched nerve syndrome: ultrasonographic appearance of functional vascular nerve impairment. Ultraschall in Med 2012; 33: 352-356
- 17 Bodner G, Buchberger W, Schocke M et al. Radial nerve palsy associated with humeral shaft fracture: evaluation with US--initial experience. Radiology 2001; 219: 811-816
- 18 Bodner G, Huber B, Schwabegger A et al. Sonographic detection of radial nerve entrapment within a humerus fracture. J Ultrasound Med 1999; 18: 703-706
- 19 de Laat EA, Visser CP, Coene LN et al. Nerve lesions in primary shoulder dislocations and humeral neck fractures. A prospective clinical and EMG study. J Bone Joint Surg Br 1994; 76: 381-383
- 20 Berry H, Bril V. Axillary nerve palsy following blunt trauma to the shoulder region: a clinical and electrophysiological review. J Neurol Neurosurg Psychiatry 1982; 45: 1027-1032
- 21 Blom S, Dahlback LO. Nerve injuries in dislocations of the shoulder joint and fractures of the neck of the humerus. A clinical and electromyographical study. Acta Chir Scand 1970; 136: 461-466