Mus 27395
Mus 27395
Mus 27395
DOI: 10.1002/mus.27395
Karlien Mul MD, PhD1 | Niels Pesser BSc2,3 | Kimberly Vervaart BSc4 |
Joep Teijink MD, PhD2,3 | Bart van Nuenen MD, PhD4 | Nens van Alfen MD, PhD1
1
Department of Neurology, Donders Institute
for Brain, Cognition and Behaviour, Radboud Abstract
University Medical Center, Nijmegen, The Introduction/Aims: Neurogenic thoracic outlet syndrome (NTOS) is a heterogeneous
Netherlands
2 and often disputed entity. An electrodiagnostic pattern of T1 > C8 axon involvement
Department of Vascular surgery, Catharina
Hospital, Eindhoven, The Netherlands is considered characteristic for the diagnosis of NTOS. However, since the advent of
3
CAPHRI-Research Center, Maastricht high-resolution nerve ultrasound (US) imaging, we have encountered several patients
University, Maastricht, The Netherlands
4
with a proven entrapment of the lower brachial plexus who showed a different, vari-
Department of Neurology, Catharina
Hospital, Eindhoven, The Netherlands able electrodiagnostic pattern.
Methods: In this retrospective case series, 14 patients with an NTOS diagnosis with
Correspondence
Karlien Mul, Department of Neurology, a verified source of compression of the lower brachial plexus and abnormal findings
Radboud University Medical Center, PO Box
on their electrodiagnostic testing were included. Their medical records were
9101, 6500 HB, Nijmegen, The Netherlands.
Email: karlien.mul@radboudumc.nl reviewed to obtain clinical, imaging, and electrodiagnostic data.
Results: Seven patients showed results consistent with the “classic” T1 axon > C8
pattern of involvement. Less typical findings included equally severe involvement of
T1 and C8 axons, more severe C8 involvement, pure motor abnormalities, neurogenic
changes on needle electromyography in the flexor carpi radialis and biceps brachii
muscles, and one patient with an abnormal sensory nerve action potential (SNAP)
amplitude for the median sensory response recorded from the third digit. Patients
with atypical findings on electrodiagnostic testing underwent nerve imaging more
often compared to patients with classic findings (seven of seven patients vs. five of
seven respectively), especially nerve ultrasound.
Discussion: When there is a clinical suspicion of NTOS, an electrodiagnostic finding other
than the classic T1 > C8 pattern of involvement does not rule out the diagnosis. High resolu-
tion nerve imaging is valuable to diagnose additional patients with this treatable condition.
KEYWORDS
brachial plexopathy, clinical neurophysiology, electrodiagnostic studies, nerve ultrasound,
neurogenic thoracic outlet syndrome
Abbreviations: ADM, abductor digiti minimi muscle; APB, abductor pollicis brevis muscle; BicB, biceps brachii muscle; CMAP, compound motor action potential; ED, extensor digitorum muscle;
FCR, flexor carpi radialis muscle; FF, finger flexors; IH, intrinsic hand muscles; IO, interossei muscles; MABC, medial antebrachial cutaneous nerve; NTOS, neurogenic thoracic outlet syndrome;
SNAP, sensory nerve action potential; TOD, thoracic outlet decompression; TOS, thoracic outlet syndrome; US, ultrasound.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2021 The Authors. Muscle & Nerve published by Wiley Periodicals LLC.
2 | METHODS
2.3 | Nerve imaging
2.1 | Patients
Nerve US of the brachial plexus was performed, generally only
We searched the databases of the Neurology department of the on the symptomatic side (in six out of nine patients), according
Radboud University Medical Center, Nijmegen, the Netherlands, and to the recommended protocol,15 with systematic visualization of
the TOS-expert center (a joint effort from the Vascular Surgery and the extraforaminal nerve roots from C5 to T1 if accessible, the
Neurology departments) of the Catharina hospital, Eindhoven, the interscalene trunks, and the supraclavicular brachial plexus
Netherlands, for patients diagnosed with NTOS from 2010 to 2021 elements. Transverse measurements were made of all elements
who underwent EMG at one of these centers and imaging of the tho- at each level, measuring the cross-sectional area within the hyper-
racic outlet. Both centers host tertiary referral clinics for brachial echoic epineurial rim, and compared to our local reference values.15
MUL ET AL.
TABLE 1 Clinical features for patients with the classic electrodiagnostic pattern
Age at Surgical
ID Sex Age (y) onset (y) Side Weakness Atrophy Hypesthesia Imaging findings treatment Follow-up
1 F 46 26 Right APB, IO, OP, FF APB, IO, ADM MABC area MRI-plexus: hyperintense inferior Referred for n/a
trunk on STIR sequence surgical
US: WSS, elongated proc trans C7, intervention
enlarged inferior trunk
2 F 16 14 Right APB, ADM, IO, APB, ADM, IO Diffuse total arm MRI-plexus: cervical rib, enlarged Transaxillary TOD 3 mo:
FE, FF, WE, inferior trunk improvement
WF, SE, EE
3 F 17 17 Right APB, ADM, IO, APB, IO, ADM, MABC > median MRI-CWK: cervical rib with fibrous Resection fibrous 16 mo:
FE, FF, WE, forearm flex & and ulnar nerve band; US: elongated proc trans C7 band improvement
WF, EE, EF, SA, ext distribution with enlarged nerve root and
SE enlarged and hypoechogenic
inferior trunk
4 F 70 55 Right APB APB Superficial radial US: fibrous band from elongated No n/a
nerve domain proc trans C7 compressing
inferior trunk
5 F 22 15 Right APB, ADM n/a MABC area US: WSS, elongated proc trans C7 Transaxillary TOD 2 mo:
with fibrous band compressing with tenotomy improvement
inferior trunk m. PM
6 F 37 36 Left OP, FF, FE APB T1 dermatoma MRI-plexus: cervical rib, fibrous Transaxillary TOD n/a
band from C8 to T1
7 M 28 17 Right Hand APB, ADM, IO MABC domain X-thorax: cervical rib Transaxillary TOD 12 mo:
and dig IV-V improvement
Abbreviations: dFF, deep finger flexors; dig: digit; EE: elbow extensors; EF: elbow flexors; F, female; FE, finger extensors; FF, finger flexors (not further specified); FP, flexor pollicus muscle; IH, intrinsic hand
muscles (not further specified); IO, interossei muscles; M, male; n/a, not available; OP, opponens pollicis muscles; PM, pectoralis minor; SA, shoulder abductors; SE, shoulder external rotators; supFF, superficial
finger flexors; TOD, thoracic outlet decompression; WE, wrist extensors; WF, wrist flexors; WSS, wedge sickle sign (a hyper-echoic fibromuscular structure at the medial edge of the middle scalene muscle that
indents the lower trunk of the brachial plexus).
3
4
Age at Surgical
ID Sex Age (y) onset (y) Side Weakness Atrophy Hypesthesia Imaging findings treatment Follow-up
8 F 16 15 Right APB, ADM, IO, APB, forearm flex None MRI-plexus and US: Transaxillary TOD 14 mo:
FP, FE, FF swollen inferior trunk; improvement
CT-thorax: elongated
proc trans C7
9 M 45 44 Right IO, FE None MABC domain, MRI-plexus: cervical rib Resection fibrous 2 mo:
dig IV-V band improvement
10 F 51 10 Right IO, APB, ADM, APB, ADM, MABC domain MRI-plexus: cervical rib Resection fibrous 2 mo:
dFP, FF, FE forearm with fibrous band; US: band improvement
enlarged inferior trunk,
fibrous band, WSS,
elongated proc trans
C7
11 F 17 15 Right None None Diffuse forearm, US: WSS, swollen and Transaxillary TOD 12 mo:
dig II-IV hypoechogenic middle with tenotomy complete
and inferior trunk m. PM recovery
12 F 69 63 Right None APB, ADM, IO Diffuse arm US: WSS; X-thorax: Transaxillary TOD 12 mo:
elongated proc trans improvement
C7
13 F 34 26 Right OP, ADM, FP, APB, ADM, IO Ulnar side hand US: cervical rib, WSS, Transaxillary TOD 12 mo:
supFF, FE and dig V enlarged and with tenotomy improvement
hypoechogenic C8 and m. PM
T1
14 F 41 18 Right Hand APB dig III-IV US: WSS; X-thorax: Transaxillary TOD 3 mo:
cervical rib improvement
Abbreviations: ADM, abductor digiti minimi muscle; APB, abductor pollicis brevis muscle; dFF, deep finger flexors; dig, digit; EE, elbow extensors; EF, elbow flexors; F, female; FE, finger extensors; FF, finger
flexors (not further specified); FP, flexor pollicus muscle; IH, intrinsic hand muscles (not further specified); IO, interossei muscles; M, male; n/a, not available; OP, opponens pollicis muscles; PM, pectoralis minor;
SA, shoulder abductors; SE, shoulder external rotators; supFF, superficial finger flexors; TOD, thoracic outlet decompression; WE, wrist extensors; WF, wrist flexors; WSS, wedge sickle sign (a hyper-echoic
fibromuscular structure at the medial edge of the middle scalene muscle that indents the lower trunk of the brachial plexus).
MUL ET AL.
MUL ET AL. 5
MRI scans had been performed clinically without a specific protocol, had a normal CMAP amplitude of the APB, but her needle EMG rev-
at the discretion of the radiologist, usually prior to referral to our cen- ealed more pronounced neurogenic changes in the abductor pollicis
ters. MR images included coronal T1, T2, and STIR images in all brevis (APB) than the FDI muscle, fitting the T1 > C8 pattern.
patients. In some patients additional sequences were included such as The other seven patients (patients 8–14) had electrodiagnostic
T1 gadolinium contrast enhanced images, and/or images in transverse findings that can be seen with a lower brachial plexopathy, but
or sagittal plane. different from the classic pattern. In three patients (patients
The diagnosis of NTOS was confirmed when there was enlarge- 10, 13 and 14) C8 axons were equally or more severely affected
ment of elements of the lower trunk of the brachial plexus, including than T1 axons, and in two of them (patients 13 and 14) the SNAP
patients with nerve enlargement in whom an anatomical structure amplitude of the MABC was normal. In addition to C8 and T1
causing compression of plexus elements was seen. involvement, one patient had neurogenic changes in the C7
innervated flexor carpi radialis (FCR) muscle (patient 10), one had
neurogenic changes in both the FCR and the C6 innervated
3 | RESULTS biceps brachii muscle (BicB; patient 13), and one had a low SNAP
amplitude for the median nerve response recorded from the third
Fourteen patients were included in this study. Demographic and clini- digit (patient 14).
cal information are shown in Tables 1 and 2. Of note, data on the In two other patients (patients 8 and 11) we only found motor
involvement of certain isolated muscle groups such as the specific fin- abnormalities, and all SNAP amplitudes were within the reference
ger flexors (FF) could not be retrieved from the medical records of all ranges. The motor abnormalities found in one of these patients fit the
patients. Tables 3 and 4 show the results of the nerve conduction classic pattern with T1 > C8 involvement. In the other patient, T1 and
studies and needle electromyography, respectively, in each patient. C8 motor axons were equally affected, and additionally neurogenic
Examples of characteristic imaging findings are shown in Figures 1 changes with reinnervation and denervation potentials were found in
and 2 andSupporting Information Video S1, which is available online. the FCR muscle. One patient (patient 9) showed sensorimotor
Seven patients (patients 1–7) showed results consistent with a involvement of C8 axons, without any evidence of T1 axon involve-
T1 > C8 pattern of axonal damage. One of these patients (patient 5) ment. Finally, one patient (patient 12) only showed an abnormal SNAP
Patient MABC Uln dig V Uln dig IV Uln DUC Med dig III Med dig IV LABC APB ADM FDI
Normal value (lower limit) 5.3 19.3 10.0 9.8 <50 y: 27.0 10.0 7.7 6.2 8.4 9.2
>50 y: 18.0
Classic pattern
1 NR/10.5 10.8/70.2 39.3/n/a 69.3/101.4 35.3/n/a 1.3/13.6 10.2/n/a
2 NR/10.8 14.9/54.5 29.6/56.6 1.0/18.4 4.8/12.4
3 NR/8.3 7.3/35.1 20.3/28.1 2.3/11.6 10.9/17.7
4 NR/5.8 11.5/25.7 7.7/n/a 28.8/28.2 6.4/n/a NR/8.8 10.2/10.9 14.5/n/a
5 2.3/7.3 23.5/49.5 22.2/n/a 60.9/n/a 12.9/n/a 9.8/n/a 15.0/n/a
6 NR/9.4 16.4/23.3 7.3/n/a 41.8/n/a 10.9/n/a 15.3/12.6 1.4/n/a 7.9/n/a 8.8/n/a
7 2.6/7.7 2.4/19.3 NR/22.7 5.7/n/a
Other pattern
8 6.4/6.4 41.6/63.2 25.3/n/a 81.8/n/a 26.3/n/a 22.2/23.0 4.4/20.1 10.1/14.6
9 10.4/10.2 5.0/22.8 NR/n/a 4.0/15.6 21.2/n/a 10.4/n/a 13.6/12.2 14.1/n/a 15.7/15.6 21.4/n/a
10 3.9/7.2 7.4/51.4 44.0/42.6 0.8/n/a 4.7/n/a
11 6.7/7.3 68.9/52.1 69.4/n/a 11.9/n/a 11.8/n/a
12 11.7/n/a 31.7/n/a 18.5/n/a 20.3/n/a 8.2/n/a 13.5/n/a
13 6.9/7.1 4.2/67.6 47.2/90.4 1.1 /n/a 9.6/n/a 6.8/n/a
14 21.4/14.3 14.3/22.1 8.1/60.2
T A B L E 4 Needle electromyography
Patient APB ADM FDI ED FCR BicB Delt EPL FCU
results symptomatic side
Classic pattern
1 DE
2 DE DE nl
3 DE RE nl nl nl nl
4 DE RE RE
5 RE RE nl nl
6 RE RE RE
7 DE RE
Other pattern
8 RE RE DE
9 nl nl RE nl RE RE
10 DE DE nl RE nl
11 DE RE RE RE nl
12 nl nl nl
13 DE RE RE RE nl
14 RE RE RE
Note: Bold: abnormal values. nl: = (sampled and) normal; RE = neurogenic changes showing reinnervation
potentials; DE = neurogenic changes with reinnervation but also denervation potentials.
Abbreviations: ADM, abductor digiti minimi muscle; APB, abductor pollicis brevis muscle; Delt, deltoid
muscle; EPL, extensor pollicis longus muscle; FCU, flexor carpi ulnaris muscle; FDI, first dorsal interossei
muscle.
F I G U R E 1 Nerve US of the right brachial plexus of patient 10. Elongated C7 transverse process (A, *) with enlarged C7 root (B, cross-
sectional area 0.17 cm2). Enlarged lower trunk of the brachial plexus (cross-sectional area 0.17 cm2) with wedge sickle (C, protruding edge of the
middle scalene muscle as a layer between the supraclavicular plexus and pleura) with kinking of the C8 root (D)
MUL ET AL. 7
F I G U R E 2 MRI of the brachial plexus of patient 10. A, T1 TSE coronal MRI showing right cervical rib with kinking of the C8 root below the
cervical rib (arrowhead) (fibrous edge of SCM not visible). B, T2 STIR coronal MRI with visible deviation of the C7 root on the right over cervical
rib (arrowhead)
amplitude for the median sensory response recorded from the third A notable finding was the involvement of the FCR muscle in four
digit. patients and of the extensor digitorum muscle (ED) in four patients in
Imaging of the brachial plexus was performed with US in 10 and our study, which are both considered to contain innervation from the
with MRI in seven patients (Tables 1 and 2). Patients 1, 3 and C7 root. All of these had an elongated C7 process or a cervical rib that
13 underwent MRI of the cervical spine that did not show neural could possibly explain the middle trunk involvement. However, the
foraminal narrowing. reason for the occurrence in these patients and not in the others who
Twelve patients underwent surgical treatment. One patient also demonstrated the same anatomic findings is uncertain, and again
(patient 1) was only recently referred for surgical intervention at the most likely due to individual variations in local anatomy and mechani-
time of writing of this article. Patient 4 had very severe atrophy and cal strain. Several studies have reported variability or anomalies of the
weakness of the hand muscles and it was decided not to perform sur- basic contents of the thoracic outlet, as well as considerable variability
gery as this was unlikely to result in improvement. between connections of brachial plexus elements and arm nerve anat-
The median time of post-surgery follow-up was 12 mo. All surgi- omy.16-18 To add to the complexity, muscles are often innervated by
cally treated patients experienced an improvement in their symptoms, two spinal segments with one level dominating, and electrodiagnostic
mostly relief of pain and sensory symptoms. studies cannot provide detailed information on these segmental
variations.18-20
The involvement of the median sensory response recorded from
4 | DISCUSSION digit three was found in two patients and can be explained by the fact
that the cutaneous domain of the lower plexus in approximately 20%
In our retrospective case series we found that half of the confirmed of individuals also includes the median nerve-innervated skin of the
NTOS patients had a classic electrodiagnostic pattern of abnormali- middle finger.21 In two patients we only found motor abnormalities, a
ties, but the other half did not. In the literature the SNAP amplitude finding for which we have no ready explanation at this point.
of the MABC is regarded as the most sensitive electrodiagnostic In our series, nerve imaging with either MRI or US was important
marker for NTOS, but in our study it was normal in 6/14 patients.8,9 in half of the patients to arrive at the final diagnosis. Plexus US has an
These non-classic patients showed variable electrodiagnostic patterns, advantage over MRI in having a higher resolution and a better ability
characterized by equally severe involvement of T1 and C8 nerve to detect fibromuscular bands that may compress or constrict the
fibers, or more severe or even isolated involvement of C8 plexus.11,12,22 Its use has been indicated before, in a study showing
nerve fibers. We hypothesize this is related to the individual anatomic that it can be useful in detecting early stage NTOS patients, in whom
configuration of the thoracic outlet that determines whether the T1 axonal damage is still only mild and electrodiagnostic studies subse-
or C8 nerve roots sustain the most severe injury by mechanical quently (near) normal.9 Our study now adds information that US
entrapment. detects not only these early or mildly affected patients, but also more
8 MUL ET AL.
severely affected patients who do not have the classic pattern of OR CID
compressive damage. Niels Pesser https://orcid.org/0000-0002-1413-2712
Of note is that the Reporting standards of the Society for Vascu- Nens van Alfen https://orcid.org/0000-0001-7839-8125
lar Surgery for thoracic outlet syndrome state that “electrodiagnosis
and brachial plexus imaging studies are not required” in reporting on RE FE RE NCE S
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