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CLINICAL ARTICLE J Neurosurg Spine 28:621–629, 2018 I N cases of chronically progressive, painless, flaccid paresis of the upper limbs, a variety of neurological differential diagnoses have to be considered, rang- ing from motor neuron diseases (e.g., amyotrophic lateral sclerosis [ALS] 16 or spinal muscular atrophy 4 ) and autoim- mune or demyelinating polyneuropathies (e.g., multifocal motor neuropathy [MMN] 17 or hereditary neuropathy with liability to pressure palsies [HNPP] 26 ) to atypical forms of chronic neuralgic shoulder amyotrophy, 23 neuroinflam- matory diseases (such as American Lyme neuroborrelio- sis [ALN] 20 ), and entrapment syndromes of the cervical plexus and/or peripheral nerves. 2 ABBREVIATIONS ACDF = anterior cervical discectomy and fusion; ALN = American Lyme neuroborreliosis; ALS = amyotrophic lateral sclerosis; BI = Barthel Index; CMAP = compound muscle action potential; ECOG = Eastern Cooperative Oncology Group; EMG = electromyography; HNPP = hereditary neuropathy with liability to pressure palsies; KPS = Karnofsky Performance Scale; MMN = multifocal motor neuropathy; MRC = Medical Research Council; PCF = posterior cervical foraminotomy; PSI = Patient Satisfaction Index; PSS = Performance Status Scale; SF-36v2 = 36-Item Short Form Health Survey, version 2. SUBMITTED July 24, 2017. ACCEPTED October 4, 2017. INCLUDE WHEN CITING Published online March 23, 2018; DOI: 10.3171/2017.10.SPINE17821. Painless motor radiculopathy of the cervical spine: clinical and radiological characteristics and long-term outcomes after operative decompression Sebastian Siller, MD, Rami Kasem, Thomas-Nikolaus Witt, MD, Joerg-Christian Tonn, MD, and Stefan Zausinger, MD Neurosurgical Clinic, Clinic of the University of Munich (LMU), Campus Grosshadern, Munich, Germany OBJECTIVE Various neurological diseases are known to cause progressive painless paresis of the upper limbs. In this study the authors describe the previously unspecified syndrome of compression-induced painless cervical radiculopathy with predominant motor deficit and muscular atrophy, and highlight the clinical and radiological characteristics and out- comes after surgery for this rare syndrome, along with its neurological differential diagnoses. METHODS Medical records of 788 patients undergoing surgical decompression due to degenerative cervical spine diseases between 2005 and 2014 were assessed. Among those patients, 31 (3.9%, male to female ratio 4.8 to 1, mean age 60 years) presented with painless compressive cervical motor radiculopathy due to neuroforaminal stenosis without signs of myelopathy; long-term evaluation was available in 23 patients with 49 symptomatic foraminal stenoses. Clinical, imaging, and operative findings as well as the long-term course of paresis and quality of life were analyzed. RESULTS Presenting symptoms (mean duration 13.3 months) included a defining progressive flaccid radicular paresis (median grade 3/5) without any history of radiating pain (100%) and a concomitant muscular atrophy (78%); 83% of the patients were smokers and 17% patients had diabetes. Imaging revealed a predominantly anterior nerve root compres- sion at the neuroforaminal entrance in 98% of stenoses. Thirty stenoses (11 patients) were initially decompressed via an anterior surgical approach and 19 stenoses (12 patients) via a posterior surgical approach. Overall reoperation rate due to new or recurrent stenoses was 22%, with time to reoperation shorter in smokers (p = 0.033). Independently of the surgical procedure chosen, long-term follow-up (mean 3.9 years) revealed a stable or improved paresis in 87% of the patients (median grade 4/5) and an excellent general performance and quality of life. CONCLUSIONS Painless cervical motor radiculopathy predominantly occurs due to focal compression of the anterior nerve root at the neuroforaminal entrance. Surgical decompression is effective in stabilizing or improving motor function with a resulting favorable long-term outcome. https://thejns.org/doi/abs/10.3171/2017.10.SPINE17821 KEYWORDS cervical spine; motor radiculopathy; muscular atrophy; neuroforaminal stenosis; painless paresis J Neurosurg Spine Volume 28 • June 2018 621 ©AANS 2018, except where prohibited by US copyright law Unauthenticated | Downloaded 04/25/21 06:10 PM UTC

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Page 1: Painless motor radiculopathy of the cervical spine: clinical ......622 Spine Volume 28 • June 2018 In this study we describe a rare form of cervical nerve root compression syndrome

CLINICAL ARTICLEJ Neurosurg Spine 28:621–629, 2018

In cases of chronically progressive, painless, flaccid paresis of the upper limbs, a variety of neurological differential diagnoses have to be considered, rang-

ing from motor neuron diseases (e.g., amyotrophic lateral sclerosis [ALS]16 or spinal muscular atrophy4) and autoim-mune or demyelinating polyneuropathies (e.g., multifocal

motor neuropathy [MMN]17 or hereditary neuropathy with liability to pressure palsies [HNPP]26) to atypical forms of chronic neuralgic shoulder amyotrophy,23 neuroinflam-matory diseases (such as American Lyme neuroborrelio-sis [ALN]20), and entrapment syndromes of the cervical plexus and/or peripheral nerves.2

ABBREVIATIONS ACDF = anterior cervical discectomy and fusion; ALN = American Lyme neuroborreliosis; ALS = amyotrophic lateral sclerosis; BI = Barthel Index; CMAP = compound muscle action potential; ECOG = Eastern Cooperative Oncology Group; EMG = electromyography; HNPP = hereditary neuropathy with liability to pressure palsies; KPS = Karnofsky Performance Scale; MMN = multifocal motor neuropathy; MRC = Medical Research Council; PCF = posterior cervical foraminotomy; PSI = Patient Satisfaction Index; PSS = Performance Status Scale; SF-36v2 = 36-Item Short Form Health Survey, version 2.SUBMITTED July 24, 2017. ACCEPTED October 4, 2017.INCLUDE WHEN CITING Published online March 23, 2018; DOI: 10.3171/2017.10.SPINE17821.

Painless motor radiculopathy of the cervical spine: clinical and radiological characteristics and long-term outcomes after operative decompressionSebastian Siller, MD, Rami Kasem, Thomas-Nikolaus Witt, MD, Joerg-Christian Tonn, MD, and Stefan Zausinger, MD

Neurosurgical Clinic, Clinic of the University of Munich (LMU), Campus Grosshadern, Munich, Germany

OBJECTIVE Various neurological diseases are known to cause progressive painless paresis of the upper limbs. In this study the authors describe the previously unspecified syndrome of compression-induced painless cervical radiculopathy with predominant motor deficit and muscular atrophy, and highlight the clinical and radiological characteristics and out-comes after surgery for this rare syndrome, along with its neurological differential diagnoses.METHODS Medical records of 788 patients undergoing surgical decompression due to degenerative cervical spine diseases between 2005 and 2014 were assessed. Among those patients, 31 (3.9%, male to female ratio 4.8 to 1, mean age 60 years) presented with painless compressive cervical motor radiculopathy due to neuroforaminal stenosis without signs of myelopathy; long-term evaluation was available in 23 patients with 49 symptomatic foraminal stenoses. Clinical, imaging, and operative findings as well as the long-term course of paresis and quality of life were analyzed.RESULTS Presenting symptoms (mean duration 13.3 months) included a defining progressive flaccid radicular paresis (median grade 3/5) without any history of radiating pain (100%) and a concomitant muscular atrophy (78%); 83% of the patients were smokers and 17% patients had diabetes. Imaging revealed a predominantly anterior nerve root compres-sion at the neuroforaminal entrance in 98% of stenoses. Thirty stenoses (11 patients) were initially decompressed via an anterior surgical approach and 19 stenoses (12 patients) via a posterior surgical approach. Overall reoperation rate due to new or recurrent stenoses was 22%, with time to reoperation shorter in smokers (p = 0.033). Independently of the surgical procedure chosen, long-term follow-up (mean 3.9 years) revealed a stable or improved paresis in 87% of the patients (median grade 4/5) and an excellent general performance and quality of life.CONCLUSIONS Painless cervical motor radiculopathy predominantly occurs due to focal compression of the anterior nerve root at the neuroforaminal entrance. Surgical decompression is effective in stabilizing or improving motor function with a resulting favorable long-term outcome.https://thejns.org/doi/abs/10.3171/2017.10.SPINE17821KEYWORDS cervical spine; motor radiculopathy; muscular atrophy; neuroforaminal stenosis; painless paresis

J Neurosurg Spine Volume 28 • June 2018 621©AANS 2018, except where prohibited by US copyright law

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In this study we describe a rare form of cervical nerve root compression syndrome resulting from degenerative neuroforaminal stenosis with predominant radicular mo-tor deficit and muscular atrophy, but completely with-out any accompanying pain. The aim of the study was a comprehensive characterization of affected patients with special regard to clinical and imaging findings, 10-year prevalence in our clinic, and surgical management, as well as long-term prognosis and quality of life after surgi-cal decompression. The importance of thorough electro-physiological diagnostics and imaging for differentiation from the above-mentioned neurological disorders is high-lighted.

MethodsThe study was approved by the IRB of Ludwig-Max-

imilians University in Munich, Germany. A retrospective analysis of 788 patients who underwent anterior cervical discectomy and fusion (ACDF) or posterior cervical fo-raminotomy (PCF) due to degenerative cervical spine dis-eases at the Neurosurgical Clinic between January 2005 and December 2014 was performed to identify all adult patients (without exception) with painless radiculopathy and an accompanying motor deficit. Patients were ex-cluded if their surgical indication comprised myelopathy, painful radiculopathy at any time, radiculopathy with-out motor deficits or atrophy, and/or radiculopathy with compromising sensory changes. To discriminate painless paresis from the above-mentioned noncompressive neuro-logical diseases, a complete evaluation (including clinical, electrophysiological, and blood/CSF examinations) was performed by an experienced neurologist (T.N.W.). After identification of all matching patients, informed consent was obtained and the patients’ clinical characteristics, im-aging findings, operative records, complications, and indi-vidual outcomes were analyzed.

Clinical EvaluationNeurological examinations using the Medical Research

Council (MRC) grading system for muscle strength3 were performed in all patients at hospital admission, shortly af-ter surgery (mean 7.5 ± 2.1 days, range 4–12 days), and during the follow-up visits at our outpatient clinic; the mean last outpatient visit at our clinic was 1.4 ± 1.8 years (range 1–8 years) postoperatively.

Reference muscles for a specific nerve root compres-sion were trapezius and supraspinatus/infraspinatus mus-cle for C-4, deltoid muscle for C-5, biceps and brachiora-dialis muscle for C-6, triceps muscle for C-7, hypothenar muscles for C-8, and interosseous muscles for C-8 and T-1.

Radiography-based diaphragmatic motility disturbance in combination with signs of isolated, electrophysiologi-cal, chronic, and active denervation in the paravertebral muscles of C-3 were assumed to indicate a radicular deficit as a consequence of an ipsilateral neuroforaminal stenosis of C2–3 in 1 patient without additional motor deficit in the upper limbs.

Postoperative outcome of motor function was based on motor status according to MRC scale grade and was cat-egorized as improved, stable, or worse in comparison with

the preoperative status. The patients’ postoperative gen-eral clinical outcome was graded using Odom’s criteria.18

The last long-term follow-up status was assessed with a standardized telephone interview. If patients reported any change of motor function and/or neurological status compared with the last outpatient visit at our clinic, a con-firmative outpatient examination was performed between November 2015 and May 2016 with regard to residual symptoms and motor outcome. This outpatient examina-tion included a questionnaire evaluation using the Patient Satisfaction Index (PSI),24 WHO/Eastern Cooperative On-cology Group (ECOG) Performance Status Scale (PSS),19 Karnofsky Performance Scale (KPS),8 Barthel Index (BI),15 and 36-Item Short Form Health Survey, version 2 (SF-36v2). The mean long-term follow-up period was 3.9 ± 3.2 years (range 1–10 years).

Electrophysiological EvaluationElectrophysiological examinations included bilateral

neurography of the median and ulnar nerve (distal motor latency, sensory nerve conduction velocity) and electro-myography (EMG) of the upper limbs and paravertebral muscle groups.

Imaging EvaluationThe severity and distribution of neuroforaminal steno-

ses were assessed based on preoperative T2-weighted MR images or, if MRI was not possible due to ferromagnetic internal medical devices or claustrophobia, native or post-myelographic CT images were used. Grading of stenosis was conducted using a modified scoring system based on the MRI grading system by Kim et al.,9 which has been validated for its reliability and high inter- and intraobserv-er agreement for assessing cervical neuroforaminal steno-sis. The modified scoring system included a subdivision between predominantly ventral stenoses and predominant-ly dorsal/circular neuroforaminal stenoses (Fig. 1). Postop-erative imaging was performed in all patients who had not improved in motor function after initial surgical decom-pression or who suffered from further motor deterioration during the follow-up visits.

Surgical ProceduresFor initial decompression (index surgery), an anterior

approach (ACDF) was chosen in cases involving a focal anterior compression of the ventral nerve root as a conse-quence of a mediolateral disk prolapse or an osseous ste-nosis at the entrance of the neural foramen (especially un-covertebral joint arthrosis). A dorsal approach (PCF) was preferred in cases with a sequester at the neuroforaminal entrance or an osseous long-distance foraminal stenosis reaching up to the extraforaminal space.

For ACDF, patients were positioned supine and a Smith-Robinson approach25 was used. The intervertebral disc, pos-terior longitudinal ligament, and osteophytes were resected with careful endplate preparation. Uncoforaminotomy was performed for the neuroforaminal decompression. Tita-nium or polyetheretherketone cages filled with autologous bone obtained from osteophytic resection were positioned in the intervertebral space under fluoroscopic control.

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For PCF, a longitudinal midline incision was performed with exposure of the superior and inferior aspects of the laminae and involved facet joint. Then, a high-speed drill was used to create a keyhole foraminotomy with preserva-tion of at least 50% of the facet joint to maintain cervical stability. The ligamentum flavum was resected and the dorsal aspect of the nerve root was decompressed circum-ferentially. In cases of sequestrated disc material, it was removed.

Statistical AnalysisAll statistical analyses were performed using Sigma-

Plot for Windows (version 11.0, Systat Software, Inc.). The patient population was described with summary statistics. Mean values are reported as means ± SDs. To investigate risk factors (sex, age at first clinical signs, duration and type of symptoms, grade of stenosis, age at first opera-tion, and comorbidities) possibly associated with neuro-logical status, reoperation rates, time to reoperation, and outcome parameters, Spearman rank order correlations, Pearson product moment correlations, logistic regression analyses (polytomous variables), and Fisher’s exact tests (dichotomous variables) were used for univariate analysis. Statistical significance was determined by a probability value < 0.05.

ResultsClinical Characteristics

Altogether, 788 patients underwent operations due to

degenerative diseases of the cervical spine, involving 499 patients initially undergoing ACDF and 289 patients un-dergoing PCF. Fourteen of 499 patients with initial ACDF and 17 of 289 patients with initial PCF presented with symptoms of a completely painless compressive cervical motor radiculopathy. In the 10-year period between 2005 and 2014, these 31 patients accounted for 3.9% (31/788) of all patients undergoing surgical decompression of cervical nerve roots due to degenerative disease.

Of these 31 patients, 23 (19 men and 4 women, male to female ratio of 4.8 to 1) with 49 total symptomatic neu-roforaminal stenoses at index surgery were available for long-term follow-up interviews and questionnaires con-cerning quality of life and general performance evalua-tion; 8 patients were lost to follow-up, but there were no significant differences in baseline characteristics between the two groups. The mean age at first surgery was 59.9 ± 10.6 years (range 36–78 years). At the most recent follow-up, a total of 28 operations for decompression of 60 symp-tomatic stenoses had been performed with a mean of 1.2 ± 0.4 operations per patient (no patient underwent more than two operations).

In addition to a defining painless flaccid paresis with-out any history of previous or current radiating pain, pre-senting symptoms included a clinically visible muscular atrophy (78.3%) and concomitant, but negligible, sensory changes (radicular 13.0%, nonradicular/unspecific 26.1%). The mean age at first clinical signs was 58.8 ± 10.6 years (range 35–78 years) and mean duration of symptoms was 13.3 ± 10.2 months (range 1–38 months). Paresis always oc-

FIG. 1. Schematic diagrams of the grading system for cervical neuroforaminal stenosis in axial scans at the intervertebral disc level. Modified with permission from Kim et al: Korean J Radiol 16:1294–1302, 2015.

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curred in a radicular manner according to the localization of neuroforaminal stenosis and was painless throughout for all affected levels in cases of multisegmental manifes-tation. Additionally, in all patients paresis was chronically progressive with a median MRC grade of 3/5 (range 0/5–4/5) at hospital admission. None of the patients had clinical signs of myelopathy. Nineteen (82.6%) of 23 patients had a history of smoking, 4 patients (17.4%) were suffering from diabetes mellitus, two patients (8.7%) from coronary/pe-ripheral artery disease, and 1 patient (4.3%) from obesity.

Electrophysiological FindingsElectrophysiological evaluation was available in 16 pa-

tients (69.6%). In all cases, there was no indication of neu-rographical abnormalities, excluding a relevant contribu-tion of entrapment syndromes of peripheral nerves. EMG evaluation, however, consistently showed a reduced ampli-tude of the compound muscle action potentials (CMAPs) and patterns of a chronic and active denervation (spon-taneous fibrillation and fasciculation potentials, positive sharp-waves) in both the clinically affected muscle groups in the upper limbs as well as the paravertebral muscles, according to the effect on the segmental nerve root due to neuroforaminal stenosis.

Radiological and Surgical Characteristics of Neuroforaminal Stenoses and Reoperation Rates

The most common locations of neuroforaminal steno-ses were C4–5 (16 stenoses, 32.7%) and C5–6 (15 steno-ses, 30.6%), followed by C2–3 (1 stenosis, 2.0%), C3–4 (6 stenoses, 12.2%), C6–7 (5 stenoses, 10.2%), and C7–T1 (6 stenoses, 12.2%). Most neuroforaminal stenoses were mul-tisegmental (n = 41, 83.7%) and unilateral (n = 33, 67.3%).

Concerning morphology and severity, 39 (79.6%) of 49 total symptomatic foraminal stenoses were classified as

grade 2a, 9 stenoses as grade 1a (18.4%), and 1 stenosis as grade 2 (2.0%); therefore, the vast majority of stenoses (grade 2a and 1a = 98.0%) led to a focal ventral compres-sion of the anterior nerve root. Significant cord compres-sion or any signs of myelomalacia were not observed in our patient population.

Altogether, 19 neuroforaminal stenoses (38.8%) in 12 patients were caused by a laterally sequestered disc pro-lapse at the neuroforaminal entrance alone or in combi-nation with an osseous long-distance foraminal stenosis extending to the extraforaminal space, and therefore ini-tially decompressed via PCF. ACDF was performed in 11 patients to completely decompress 30 neuroforaminal stenoses (61.2%) due to a focal anterior compression of the ventral nerve root as a consequence of uncovertebral joint arthrosis with osteophytes alone or in combination with a mediolateral disc protrusion/prolapse. Examples of neuro-foraminal stenoses are shown in Fig. 2.

There was no significant difference in clinical char-acteristics between the ACDF and PCF cohorts. Surgical details and complications are described in Table 1. Post-operative complications included new sensory changes that were permanent in 1 patient after ACDF and tran-sient (< 3 months) in 1 patient each after PCF and ACDF. Transient deterioration of preoperative paresis was noted in 2 patients after PCF and in 1 patient after index ACDF (without new deficits of preoperatively unaffected mus-cles), whereas there was no case of new permanent motor deficits postoperatively.

During the mean follow-up period of 3.9 years, 3 (25.0%) of 12 patients with index PCF and 2 (18.2%) of 11 patients with index ACDF had to undergo a second operation for decompression of 11 total neuroforaminal stenoses; the total reoperation rate was 21.7%. The same level had to be reoperated ipsilaterally in 4.1% of all cases due to primarily persistent painless paresis as a result of residual stenosis, whereas in 6.1% reoperation was due to recurrent painless paresis of initially affected muscle groups as a result of secondarily relapsing stenosis. Ad-ditionally, reoperation had to be performed for the same level contralaterally in 2.0%, the adjacent segments in 6.1%, and the nonadjacent segments in 4.1% of all cases due to newly emerged stenosis and painless paresis of ini-tially unaffected muscle groups (no significant differences between index ACDF or PCF). A focal compression of the anterior nerve root at the neuroforaminal entrance was found in the majority of these stenoses (grade 2a and 1a = 90.9%) without significant differences between the same, adjacent, and nonadjacent segment. Overall mean time be-tween index and second surgery was 5.9 ± 8.2 years (range 0.1–19.8 years) without significant differences between the types of index surgery.

We calculated the correlation for patient-based and surgical variables in relation to the time to reoperation. An inverse relation was found for patients with a positive smoking history (p = 0.033, r = -0.907), indicating that smokers required a reoperation sooner than patients with-out a positive smoking history (regardless of the type of index surgery). No significant correlations were found for patient sex, age at first clinical signs, duration and type of symptoms, grade of stenosis, age at first operation, and

FIG. 2. Preoperative axial CT images (A and B) showing massive iso-lated uncovertebral joint arthrosis and T2-weighted MR images (C and D) showing uncovertebral joint arthrosis in combination with soft-tissue pathologies causing a focal compression (grade 2a) of the ventral nerve root at the neuroforaminal entrance (arrows).

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other comorbidities (diabetes, obesity, and coronary/pe-ripheral artery disease).

Outcome Analysis and Risk Factors Affecting Long-Term Prognosis

The change of MRC paresis grade between the preop-erative status and the status at discharge (mean 7.5 ± 2.1 days postoperatively) and last follow-up (mean 3.9 ± 3.2 years postoperatively) is summarized in Table 2. Over-all, the median MRC grade at the last follow-up was 4/5 (range 0/5–5/5), which therefore had improved by 1 grade compared with the preoperative grade and the grade at admission (both median of 3/5). The improvement of mo-tor function between the latest follow-up examination and the preoperative status reached significance (p = 0.046). Compression of the C-6 nerve root appeared to be less reversible than compression of other cervical nerve roots,

because the change of paresis grade between the preop-erative status and the status at last follow-up was smaller for the biceps muscle (median change 0/5) than for supra-spinatus, infraspinatus, deltoid, triceps, and interosseous muscles (each median improvement of 1/5).

The majority of patients presented with an improve-ment of general clinical outcome according to Odom’s criteria, both at admission (69.6%: 1 patient with “excel-lent,” 3 patients with “good,” and 12 patients with “fair”) and at the last follow-up evaluation (91.3%: 2 patients with “excellent,” 5 patients with “good,” and 14 patients with “fair”).

The questionnaire evaluation revealed a high rate of sat-isfaction regarding the surgical long-term outcome, with 13 patients (56.5%) giving a PSI score of I and 8 patients (34.8%) of II (overall median PSI score = I, range I–IV). Long-term performance in everyday life was excellent in 20 patients (87.0%) with a BI score of 100% indicating no

TABLE 1. Surgical details and results of index surgery

Characteristic Overall (n = 23) ACDF (n = 11) PCF (n = 12)

Mean age at first surgery ± SD (yrs) 59.9 ± 10.6 60.7 ± 9.3 59.2 ± 12.0Mean no. of index levels ± SD 1.8 ± 0.6 2.0 ± 0.6 1.6 ± 0.5Surgical complications, no. (%) Effect on the nerve root Motor deterioration 2 (8.7) 1 (9.1) 1 (8.3) Sensory changes 3 (13.0) 2 (18.2) 1 (8.3) CSF effusion, infection, extensive bleeding, and/or long-term instability 0 (0.0) 0 (0.0) 0 (0.0) Overall complication rate 5 (21.7) 3 (27.3) 2 (16.7)Mean length of inpatient stay ± SD (days) 7.5 ± 2.1 6.8 ± 1.5 8.2 ± 2.4Second surgery for restenosis during follow-up, no. (%) 5 (21.7) 2 (18.2) 3 (25.0)Levels during second surgery, no. (%) 11 (47.8) 4 (36.4) 7 (58.3) Index level (ipsilateral) 5/11 (45.5) 3/4 (75.0) 2/7 (28.6) Index level (contralateral) 1/11 (9.1) 0/4 (0.0) 1/7 (14.3) Adjacent level 3/11 (27.3) 1/4 (25.0) 2/7 (28.6) Distant level 2/11 (18.2) 0/4 (0.0) 2/7 (28.6)Average time to reoperation ± SD (mos) 71.1 ± 98.4 16.1 ± 2.1 108.8 ± 119.6

TABLE 2. Change of MRC paresis grade during follow-up

Change in MRC Grade

Preop vs Short-Term MRC Grade* Preop vs Long-Term MRC Grade†Overall (n = 23) ACDF (n = 11) PCF (n = 12) Overall ACDF PCF

Improved +2 2 (8.7) 0 (0.0) 2 (16.7) 4 (17.4) 2 (18.2) 2 (16.7) +1 7 (30.4) 4 (36.4) 3 (25.0) 11 (47.8) 5 (45.5) 6 (50.0)Stable 0 11 (47.8) 6 (54.5) 5 (41.7) 5 (21.8) 3 (27.3) 2 (16.7)Deteriorated −1 2 (8.7) 0 (0.0) 2 (16.7) 2 (8.7) 0 (0.0) 2 (16.7) −2 1 (4.3) 1 (9.1) 0 (0.0) 1 (4.3) 1 (9.1) 0 (0.0)

Data given as number of patients (%). ACDF and PCF represent index surgery.* Short term = mean 7.5 ± 2.1 days postoperatively.† Long term = mean 3.9 ± 3.2 years postoperatively.

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disability (overall median BI score = 100, range 85–100). Furthermore, 20 patients (87.0%) showed a WHO/ECOG PSS score ≤ 1 (overall median WHO/ECOG PSS score = 0, range 0–2) and all patients (100.0%) a KPS score ≥ 80 (overall median KPS score = 90, range 80–100), indicating the ability to carry on normal activity and to work with no need of special care. According to the SF-36v2, the mean physical health composite score in the long-term question-naire evaluation was 49.9 ± 14.1 (range 21.5–68.8) and the mean mental health composite score was 40.8 ± 5.8 (range 31.8–47.8), indicating only a slightly worse physical or mental health than the average population. There was no significant difference in the above-mentioned data with regard to the performed type of index surgery.

Clinical and imaging factors (such as sex, age at first clinical signs, duration and type of symptoms, grade of stenosis, age at first operation, and comorbidities) were not significantly associated with long-term motor out-come, general performance, or quality of life in univariate analysis. However, the long-term motor outcome was sig-nificantly worse in patients who suffered from a transient deterioration of muscle strength immediately after index surgery (p = 0.034).

DiscussionIn this paper we describe a rare clinical manifestation

pattern of a cervical radiculopathy leading to painless, chronically progressive, flaccid paresis and concomitant muscular atrophy of the upper limbs as a consequence of compressive anterior neuroforaminal stenosis. In our se-ries, approximately 4% of all patients with an indication for surgical decompression of the cervical nerve roots due to degenerative diseases were found to have this rare form of radiculopathy.

The vast majority of affected patients were male and suffered from diseases with effects on the vasculature, such as smoking or diabetes. In detail, both the propor-tion of smokers (82.6%) and diabetic patients (17.4%) was clearly higher than the proportion of smokers (29.7%) and diabetic patients (7.2%) in the total German population, underlining the potential disproportionately high influence of a disturbed microcirculation for this rare form of ra-diculopathy.7,12 The proportion of male individuals (82.6%; male to female ratio of 4.8 to 1) was significantly higher (p = 0.026) than in our overall study population (59.6%; male to female ratio of 1.5 to 1), which might be associated with the fact that smokers are predominantly male.12 Ac-cording to our findings, smoking and diabetes have been previously identified as important risk factors for cervical radiculopathy, perioperative complication rates, and worse postoperative outcome.1,10,14,21,22

In this cohort of painless paresis, we found C-5 and C-6 to be the most frequently affected nerve roots. Anatomi-cally, the focal compression at the entrance of the neural foramen was most often attributable to uncovertebral joint arthrosis with or without soft-tissue pathologies and led to a predominant isolated lesion of the motor ventral nerve root. Because this focal anteriorly located pathology does not cause relevant compression of the sensory and noci-ceptive dorsal nerve root or spinal ganglion, isolated mo-

tor deficits can occur without concomitant pain or sensory deficits. Because this isolated ventral nerve root compres-sion was overwhelmingly frequently identified in 98.0% of all cases and was strongly associated with the clinical syn-drome of painless severe paresis of the respective nerve root, it can therefore be classified as a highly characteristic imaging pattern, making MRI and/or CT the diagnostic tool of choice for this rare clinical syndrome.

Surgical decompression of the foraminal stenosis—by ACDF or PCF—was shown to be very effective, even in cases of previously established muscle atrophy: 87% of all patients with a preoperatively progressive disease ex-perienced a sustained stable or improved motor function postoperatively. This surgery-induced stoppage of further motor deterioration is essential for patients with compres-sive cervical motor radiculopathy who have preoperatively experienced chronically progressive paresis and its asso-ciated impairments of upper limb function and basic life skills. From this point of view, we assess the postoperative general clinical outcome of “fair” (or better) according to Odom’s criteria in 91.3% of the patients as a relevant suc-cess for the patients, which is also reflected by the reported high subjective satisfaction regarding treatment outcome. Moreover, an excellent general performance could be achieved in long-term follow-up evaluations after surgery. As a consequence, in cases of well-matched characteris-tic clinical syndrome and highly pathognomonic imaging, decompressive surgery offers an effective treatment, espe-cially given the preoperative chronically progressive pare-sis and atrophy of functionally important muscles.

There are limitations in our study. First, due to its retro-spective design, inclusion of patients without accompany-ing radicular pain depends on the accuracy of the docu-mented patient’s history. We reconfirmed this detail in all included patients, but we cannot exclude that the number of patients affected by the described syndrome is actually higher as a consequence of documentation errors or false attribution of limb pain from other sources, such as as ra-dicular. Second, only 23 (74.2%) of 31 patients were avail-able for long-term follow-up, which might have influenced the results of postoperative outcome analysis and quality-of-life questionnaires.

Due to a variety of differential diagnoses, confirming the correct diagnosis in case of progressive painless pare-sis of the upper limbs can be challenging. Table 3 summa-rizes key features of painless compression-induced cervi-cal motor radiculopathy and its clinically most challenging differential diagnoses. In case of clinical uncertainty, elec-trophysiology is the most important tool apart from the characteristic spinal MRI/CT changes that are typically found in compressive cervical motor radiculopathy. For example, both adult-onset spinal muscular atrophy type IV and ALS are neurodegenerative diseases with deletion of neurons that control voluntary muscles, leading electro-physiologically to a generalized lesion of the lower mo-tor neuron without segmental distribution patterns.4,6,11,13,16 Especially in ALS, the lesion is usually extensive and can be found even in early stages in the form of a reduction of the CMAP amplitude as well as abnormal specific (e.g., unstable or large motor unit action potentials of increased duration and proportion of polyphasic components) and

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S. Siller et al.TA

BLE

3. Di

ffere

ntia

l diag

nose

s for

chro

nica

lly p

rogr

essiv

e pain

less

par

esis

of th

e upp

er lim

bs

Char

acter

istics

Diag

nosis

Cerv

ical M

otor

Radic

ulopa

thy

Due t

o For

amina

l St

enos

isAL

SSp

inal M

uscu

lar

Atro

phy T

ype I

VM

MN

HNPP

Atyp

ical F

orms

of

Chro

nic N

eura

lgic

Shou

lder

Amyo

troph

yAL

N

Entra

pmen

t Syn

drom

es

of th

e Cer

vical

Plex

us/

Perip

hera

l Ner

ves

Clini

cal

Chro

nicall

y pro

gres

-siv

e, pa

inles

s fla

ccid

pare

sis,

atrop

hy in

as

many

as 8

0% of

th

e pati

ents

Early

stag

es: v

ari-

able

lower

> up

per

motor

neur

on ef

-fec

ts; la

ter st

ages

: up

per (

e.g., p

are-

sis, h

yper

refle

xia,

spas

ticity

) & lo

wer

(e.g.

, atro

phy,

hypo

refle

xia, fl

ac-

cid pa

resis

) moto

r ne

uron

effec

ts

Gene

raliz

ed pr

ogre

s-siv

e flac

cid m

uscle

we

akne

ss an

d pa

ralys

is w/

o pain

, alm

ost a

lway

s pr

oxim

al lim

b pr

edom

inant

Foca

l asy

m-

metri

c flac

cid

dista

l limb

pa

resis

and

atrop

hy (u

p-pe

r > lo

wer)

w/o p

ain

Recu

rrent

painl

ess

atta

cks o

f foca

l nu

mbne

ss,

flacc

id mu

scle

weak

ness

and

atrop

hy, o

ften

prec

eded

by

mino

r com

pres

-sio

n on n

erve

Up to

15%

of

cas e

s: pa

inles

s fla

ccid

pare

sis

and a

troph

y of

musc

les ar

ound

th

e sho

ulder

gir

dle

Moto

r-dom

inated

ra-

dicula

r sym

ptoms

ma

y be p

rese

nt an

d mos

tly pa

in-les

s; typ

ically

su

bacu

te me

n-ing

itis w

ithou

t or

with

asso

ci-ate

d fac

ial pa

lsy

and e

ryth

ema

migr

ans r

ash

Prog

ress

ive fla

ccid

pare

sis an

d atro

phy

of mu

scle

grou

ps of

cir

cums

cribe

d upp

er

limbs

acco

rding

to th

e af

fected

perip

hera

l ne

rve,

mostl

y in c

om-

binati

on w

ith se

nsor

y ch

ange

s and

pain

Path

ophy

siol-

ogy

Dege

nera

tive

neur

ofora

mina

l ste

nosis

Neur

odeg

ener

ative

dis

ease

of up

per

and l

ower

moto

r ne

uron

s

Neur

odeg

ener

ative

dis

ease

of lo

wer m

o-tor

neur

ons d

ue to

SM

N ge

ne m

utati

on

Immu

ne-m

edi-

ated

Demy

elina

ting

neur

opath

y due

to

PMP2

2 gen

e de

letion

Unkn

own

(immu

ne-m

edi-

ated?

)

Neur

oinfla

mmati

on

due t

o Bor

relia

bu

rgdo

rferi

infec

-tio

n

Chro

nic pe

riphe

ral n

erve

en

trapm

ent/

comp

res-

sion

Elec

troph

ysiol

-og

yEM

G: re

duce

d CM

AP, p

atter

ns

of ch

ronic

and a

c-tiv

e den

erva

tion

in se

gmen

tally

af-

fecte

d per

ipher

al an

d par

aver

tebra

l mu

scles

Gene

raliz

ed le

sion

of th

e low

er m

otor

neur

on w

/o se

g-me

ntal

distri

butio

n pa

ttern

s; EM

G:

redu

ced C

MAP

, ne

urog

enic

chan

ges

Gene

raliz

ed an

d no

nseg

ment

al les

ion of

the l

ower

mo

toneu

ron;

EMG:

ne

urog

enic

chan

ges

with

redu

ced C

MAP

Cond

uctio

n blo

ck of

moto

r ax

ons,

norm

al se

nsor

y ne

rve c

on-

ducti

on

Incr

ease

in di

stal

motor

laten

cies

(esp

ecial

ly of

media

n and

pe

rone

al ne

rve);

de

crea

se in

mo-

tor an

d sen

sory

ne

rve c

ondu

ction

Unsp

ecific

, som

e-tim

es si

gns o

f de

nerv

ation

in

EMG

Unsp

ecific

, som

e-tim

es si

gns o

f ax

onal

polyr

a-dic

ulopa

thy

Disti

nct p

atter

ns of

neur

o-gr

aphic

al im

pairm

ents

in mo

tor/se

nsor

y ner

ve

cond

uctio

n velo

city +

pr

oxim

al/dis

tal m

otor

laten

cy ac

cord

ing to

th

e diffe

rent

entra

p-me

nt sy

ndro

mes

Imag

ingFo

cal c

ompr

essio

n of

the a

nterio

r ne

rve r

oot a

t the

neur

ofora

men,

mostl

y due

to

unca

rthro

sis

± so

ft-tis

sue

path

ologie

s

Hype

rinten

sity o

f the

corti

cosp

inal tr

act

on T

2-we

ighted

M

RI, c

ortic

al th

in-nin

g & gr

ay m

atter

vo

lume l

oss

espe

cially

of th

e pr

ecen

tral g

yri

Nons

pecifi

c los

s of

musc

le vo

lume i

n up

per a

nd lo

wer

limb i

magin

g

Incr

ease

d sig

nal in

ten-

sity i

n the

T2-

weigh

ted M

RI

of th

e bra

chial

ple

xus i

n as

many

as 5

0%

of pa

tients

Some

times

nerv

e hy

pertr

ophy

at

entra

pmen

t site

s in

perip

hera

l ne

uro-

ultra

so-

nogr

aphy

Some

times

loss

of

musc

le bu

lk an

d dif

fuse

area

s of

incre

ased

sign

al int

ensit

y with

in th

e mus

cle in

T1

-weig

hted

spin-

echo

MRI

Unsp

ecific

, som

e-tim

es m

ultifo

cal

white

mat

ter

lesion

s esp

ecial

ly in

periv

entri

cular

loc

ation

Often

sign

s of n

erve

en-

trapm

ent in

perip

hera

l ne

uro-

ultra

sono

grap

hy

or M

RI, r

adiog

raph

y fo

r cer

vical

rib

First-

line t

reat-

ment

Surg

ical d

ecom

-pr

essio

nAn

tiglut

amate

rgic

drug

s (rilu

zole)

, sy

mptom

atic

Symp

tomati

cInt

rave

nous

im-

muno

globu

linSy

mptom

atic,

avoid

ing ac

tivi-

ties w

ith ri

sk fo

r pr

essu

re pa

lsies

Corti

coste

roids

, ph

ysica

l ther

apy

Antib

iotics

, sym

p-tom

atic

Cons

erva

tive t

hera

py,

surg

ical d

ecom

pres

-sio

n

Prog

nosis

Stab

le/im

prov

ed

in >9

0% of

the

patie

nts

Prog

ress

ive, le

thal

Mos

tly sl

owly

prog

res-

sive,

norm

al life

sp

an

Mos

tly sl

owly

prog

ress

iveEp

isodic

atta

cks w

/ ma

rked r

ecov

ery

in da

ys to

wee

ks

Usua

lly go

od

with

comp

lete

reco

very

Usua

lly co

mplet

e re

cove

ry af

ter

antib

iotic

ther

apy

Usua

lly go

od

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J Neurosurg Spine Volume 28 • June 2018628

unspecific (e.g., denervation activity such as spontaneous fibrillation potentials, positive sharp-waves, and fascicula-tion potentials) EMG findings.11,16 In contrast, compressive cervical motor radiculopathy leads to a strictly segmen-tal lesion of the affected nerve root that can be seen in both the corresponding peripheral as well as paravertebral muscle groups in the form of a reduced CMAP amplitude and patterns of chronic and active denervation. In contrast, MMN and HNPP as autoimmune demyelinating polyneu-ropathies lead to changes of peripheral nerve conduction velocity: while the presence of a conduction block that se-lectively affects motor axons with sparing of sensory ax-ons is strongly indicative for MMN,17 an increase of distal motor latencies in combination with a decrease of motor and sensory nerve conduction velocities can only be seen in HNPP.26 In both neuralgic shoulder amyotrophy as an idiopathic brachial plexus neuropathy,5,23 and ALN as a neuroinflammatory manifestation of the systemic infec-tion with the spirochaete Borrelia burgdorferi sensu stric-to,20 electrophysiology typically shows only unspecific changes. The clinical suspicion based on detailed patient questioning and neurological examination is mostly diag-nostically more significant than electrophysiological ex-aminations. Finally, entrapment syndromes of the cervical plexus (such as thoracic outlet syndrome) and peripheral nerves (such as carpal tunnel syndrome, supinator tunnel syndrome, or Guyon’s canal syndrome) show characteris-tic patterns of neurographical impairments of motor and sensory nerve conduction velocity including proximal and distal motor latency, which are highly discriminative from compression-induced cervical motor radiculopathy.2

ConclusionsPainless compressive cervical motor radiculopathy is a

rare but severe clinical manifestation pattern of a cervical neuroforaminal stenosis. It predominantly occurs in males with focal compression of the anterior nerve root and is associated with smoking and diabetes mellitus. A safe and effective treatment can be achieved with surgical decom-pression, as patients show a significant improvement of motor function and a convincing overall general perfor-mance in long-term evaluation.

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ropathies: Charcot-Marie-Tooth disease type 1A and heredi-tary neuropathy with liability to pressure palsies. Orphanet J Rare Dis 9:38, 2014

DisclosuresThe authors report no conflict of interest concerning the materi-als or methods used in this study or the findings specified in this paper.

Author ContributionsConception and design: Siller, Witt, Zausinger. Acquisition of data: Siller, Kasem, Witt. Analysis and interpretation of data: Siller, Witt. Drafting the article: Siller. Critically revising the article: all authors. Approved the final version of the manuscript on behalf of all authors: Siller. Statistical analysis: Siller. Admin-

istrative/technical/material support: Siller. Study supervision: Siller, Zausinger.

Supplemental InformationPrevious PresentationsParts of this paper have been presented orally at the 11th Annual Meeting of the German Spine Society held in Hannover (Germa-ny) on December 3, 2016, and at the 134th Annual Meeting of the German Society of Surgery held in Munich (Germany) on March 22, 2017. Parts of this paper have been presented as a poster at the Annual Spine Section Meeting of the German Society of Neuro-surgery held in Cologne (Germany) on September 16, 2016.

CorrespondenceSebastian Siller: Clinic of the University of Munich (Ludwig Maximilians University), Campus Grosshadern, Munich, Ger-many. [email protected].

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