First neurological symptoms in degenerative cervical myelopathy: does it predict the outcome?

Abstract

Purpose
Degenerative cervical myelopathy (DCM) is the most common non-traumatic cause of spinal cord dysfunction. Prediction of the neurological outcome after surgery is important. The aim of this study was to analyze the relationship between first symptoms of DCM and the neurological outcome after surgery.

Methods
A retrospective analysis over a period of 10 years was performed. First symptoms such as cervicobrachial neuralgia, sensory and motor deficits and gait disturbances were evaluated regarding the postoperative neurological outcome. The modified Japanese Orthopedic Association Score (mJOA Score) was used to evaluate neurological outcome.

Results
In total, 411 patients (263 males, 64%) with a median age of 62.6 ± 12.1 years were included. Cervicobrachial neuralgia was described in 40.2%, gait disturbance in 31.6%, sensory deficits in 19% and motor deficits in 9.2% as first symptom. Patients with cervicobrachial neuralgia were significantly younger (median age of 58 years, p = 0.0005) than patients with gait disturbances (median age of 68 years, p = 0.0005). Patients with gait disturbances and motor deficits as first symptom showed significantly lower mJOA Scores than other patients ( p = 0.0005). Additionally, motor deficits and gait disturbance were negative predictors for postoperative outcome according to the mJOA Score.

Conclusion
Motor deficits and gait disturbances as the first symptom of DCM are negative predictors for postoperative neurological outcome. Nevertheless, patients with motor deficits and gait disturbance significantly profit from the surgical treatment despite poor preoperative mJOA Score.

Full text

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European Spine Journal (2022) 31:327–333
https://doi.org/10.1007/s00586-021-07060-3
ORIGINAL ARTICLE
First neurological symptoms indegenerative cervical myelopathy:
does it predict theoutcome?
NerimanÖzkan1· MehdiChihi1· TobiasSchoemberg1· ThiemoFlorinDinger1· MoritzHelsper1· AhmetParlak1·
RamazanJabbarli1· YahyaAhmadipour1· UlrichSure1· NicolaiElHindy1,2· OliverGembruch1
Received: 17 June 2021 / Revised: 27 September 2021 / Accepted: 10 November 2021 / Published online: 25 November 2021
© The Author(s) 2021
Abstract
Purpose Degenerative cervical myelopathy (DCM) is the most common non-traumatic cause of spinal cord dysfunction.
Prediction of the neurological outcome after surgery is important. The aim of this study was to analyze the relationship
between first symptoms of DCM and the neurological outcome after surgery.
Methods A retrospective analysis over a period of 10years was performed. First symptoms such as cervicobrachial neural-
gia, sensory and motor deficits and gait disturbances were evaluated regarding the postoperative neurological outcome. The
modified Japanese Orthopedic Association Score (mJOA Score) was used to evaluate neurological outcome.
Results In total, 411 patients (263 males, 64%) with a median age of 62.6 ± 12.1years were included. Cervicobrachial neu-
ralgia was described in 40.2%, gait disturbance in 31.6%, sensory deficits in 19% and motor deficits in 9.2% as first symptom.
Patients with cervicobrachial neuralgia were significantly younger (median age of 58years, p = 0.0005) than patients with
gait disturbances (median age of 68years, p = 0.0005). Patients with gait disturbances and motor deficits as first symptom
showed significantly lower mJOA Scores than other patients (p = 0.0005). Additionally, motor deficits and gait disturbance
were negative predictors for postoperative outcome according to the mJOA Score.
Conclusion Motor deficits and gait disturbances as the first symptom of DCM are negative predictors for postoperative
neurological outcome. Nevertheless, patients with motor deficits and gait disturbance significantly profit from the surgical
treatment despite poor preoperative mJOA Score.
Keywords Degenerative cervical myelopathy· First neurological symptom· Surgery· Neurological outcome· Outcome
prediction
Abbreviations
DCM Degenerative cervical myelopathy
mJOA Modified Japanese Orthopedic Association Score
SI Signal intensity
Introduction
Degenerative cervical myelopathy (DCM) is an age-depend-
ent deterioration of the spinal cord with an increasing epi-
demiologic relevance. It is the most common non-traumatic
cause of spinal cord dysfunction in adults [1, 2], with a
great impact on worldwide health, society and economy
[3]. Approximately 1.6 per 100,000 inhabitants per annum
require surgical treatment for symptomatic DCM [4].
The variable presentation of the DCM is an expression
of the complex interaction of mechanic and vascular factors.
The degenerative process with a progressive spinal stenosis
leads to an ongoing static compression of the spinal cord and
the nerve roots with subsequent demyelination. This may
result in necrosis of both, gray and white matter. In addi-
tion, a dynamic component resulting through the mobility of
the cervical spine might increase the pressure on the spinal
cord [5, 6].
* Oliver Gembruch
oliver.gembruch@uk-essen.de
1 Department ofNeurosurgery, University Hospital Essen,
University ofDuisburg-Essen, Hufelandstrasse 55,
45122Essen, Germany
2 Present Address: Spine-Center Werne,
Katholisches Klinikum Lünen/Werne GmbH
St. Christophorus-Krankenhaus, Am See 1, Werne, Germany
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328 European Spine Journal (2022) 31:327–333
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Moreover, vascular factors are discussed to cause myelop-
athy due to a reduced blood supply or due to a reduced venal
drain caused by a higher pressure due to the chronic and
progressive compression of the spinal cord. Furthermore, a
chronic pressure induces the activation of microglia and the
recruitment of macrophages at the site of the compression
and leads to a neuroinflammation [7]. Additionally, genetic
predisposition causing the degenerative spondylotic trans-
formation has been discussed in the current literature [8].
Surgical treatment is recommended for severe and moder-
ate DCM, while the treatment of mild DCM is still discussed
[9]. In particular, Kalsi-Ryan etal. showed that patients with
mild DCM failed to improve their neurological function sig-
nificantly after structured conservative treatment and that
23–54% of those patients underwent delayed surgical treat-
ment [10].
The clinical presentation of DCM is various and in gen-
eral unspecific at the early beginning. Therefore, the clinical
diagnosis of mild DCM might be difficult and delayed due to
comorbidities mimicking DCM. The patients usually suffer
from neck and shoulder pain with or without radiculopathy,
numbness and fine motor deficits, ataxic gait disturbance,
and sphincter dysfunction [11]. Additionally, hyperreflexia,
a positive Hoffmann’s sign, and general weakness may be
signs of myelopathy [12, 13]. Furthermore, DCM and its
neurological symptoms can be stable for a long period of
time and deteriorate episodically [2, 14].
Several predictors like duration of symptoms, high sig-
nal intensity (SI) on T2-weighted MRI, preoperative modi-
fied Japanese Orthopedic Association Score (mJOA Score),
age, comorbidities, or smoking status were identified over
the recent years to influence the neurological outcome of
DCM patients. Interestingly, other factors like the type of
stenosis, the number of affected levels, ventral or posterior
approach or the type of surgical treatment do not affect the
postoperative neurological outcome [13–18]. To our best
knowledge, first symptom of DCM was not evaluated as a
possible predictor of neurological outcome after surgery in
detail. Therefore, we aimed to analyze the first symptoms
of patients suffering from DCM and to evaluate possible
correlation between the first symptom and the neurological
outcome after surgery.
Patients andmethods
Patients andclinical data
Clinical data of patients suffering from cervical degenerative
disorders treated surgically in our department between 2007
and 2016 were retrospectively analyzed. All patients with
DCM were included. Patients with other diseases, which
might induce a myelopathy, were excluded: congenital
abnormalities of the cervical spine, metastatic diseases,
rheumatoid disorders, fractures of cervical vertebral bod-
ies, traumatic spinal cord injury or myelopathy in relation
with a cervical spine instability.
The study was conducted in accordance with the
STROBE guidelines after the approval by the Institutional
Review Board (Medical Faculty, University of Duisburg-
Essen, Registration number: 16–6270-BO).
Neurological symptoms
Neurological symptoms were recorded at admission and
divided into cervicobrachial neuralgia, sensory deficits,
motor deficits and gait disturbance. The preoperative status
and the postoperative outcome were analyzed during in-
patient treatment, and at three and six months after surgery.
The mJOA Score [19] was used for neurological assessment.
Statistics
The data were analyzed using SPSS 25.0 (Statistical Package
for the Social Sciences, SPSS Inc., Chicago, IL). Metrics
were described by median and range and nominal data by
frequency and valid percentage. P values < 0.05 in two-sided
testing were considered significant.
Demographics, clinical, and radiographic parameters
were analyzed in a univariate way regarding their associa-
tion or correlation with pre- and postoperative mJOA Scores.
Pearson Chi2 statistics or Fischer exact test was used for
dichotomous variables. As the data were not normally dis-
tributed, Kendall-Tau-b was assessed for continuous and
ordinal variables, Spearman Rho for continuous and dichoto-
mous, and Mann–Whitney U test for ordinal and continuous
variables. Significant parameters selected through univariate
analysis as well as parameters with P values < 0.1 were sub-
sequently evaluated using multivariate analysis.
A multiple regression analysis was then conducted,
wherein mJOA Score was considered a continuous variable.
A stringent confidence level of 99% was used. Therefore,
only P values < 0.01 were considered significant. Patients,
who were lost to follow-up, were not included in statistical
analyses at those time points.
Results
Demographics
We included 411 patients with a median age of
62.6 ± 12.1years (range from 31 to 96years). Of those, 263
patients were males (64%), and 148 patients were females
(36%). DCM developed due to a spinal stenosis in 249
patients (60.6%), and due to a herniated disk in 162 patients
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329European Spine Journal (2022) 31:327–333
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(39.4%). A high SI on T2-weighted MRI was detected in
248 patients (60.3%).
First neurological symptom
Cervicobrachial neuralgia was the most common first symp-
tom in majority of the patients suffering from DCM (n = 165,
40.2%). Gait disturbance was described less frequently
(n = 130, 31.6%). Sensory deficits and motor deficits were
seen in 78 patients (19%) and in 38 patients (9.2%) as the
first symptom of DCM (Fig.1).
First neurological symptom andsymptom duration
Symptom duration until surgery in patients with motor defi-
cits was significantly shorter than in patients without motor
deficits as the first symptom (7.5weeks versus 16weeks,
p = 0.002) Interestingly, diagnosis of DCM in patients with
gait disturbances took the longest time with an average
of 19.5weeks, showing a significant difference between
patients without gait disturbance as the first symptom of
DCM (16weeks, p = 0.046). Patients with cervicobrachial
neuralgia and sensory deficits as descripted first symptom
admitted after 15–16weeks in average (Table1).
First neurological symptom anddemographic
characteristics
Patients with cervicobrachial neuralgia were significantly
younger (median age: 58years) than patients without cer-
vicobrachial neuralgia as the first symptoms (median age:
66years, p = 0.0005). Significant difference in age was
also seen in patients with gait disturbance (median age:
68years) versus patients without gait disturbance (median
age: 60years, p = 0.0005). Sensory deficits and motor defi-
cits showed no significant differences in age. Regarding the
patients’ sex, the statistical analysis showed no significant
association with the first symptom of DCM (Table1).
First neurological symptom andhigh SI
onT2‑weighted MRI
High SI on T2-weighted MRI was most common in patients
with motor deficits (n = 28/38, 73.7%), but without sig-
nificant correlation (p = 0.084). A high SI on T2-weighted
MRI was present in majority of patients with cervicobrachial
neuralgia (n = 96/165 patients, 58.2%), gait disturbances (n
= 79/130, 60.8%) and sensory deficits (n = 45/78, 57.7%,
Table1).
First neurological symptom inrelation withmedian
mJOA Score
Median mJOA Score was significant higher in patients
with cervicobrachial neuralgia as the first symptom than in
Fig. 1 The first presenting symptoms of all patients suffering from
DCM
Table 1 Analysis of multiple factors in relation to the first symptom. High signal intensity (SI) on T2-weighted MRI, Age (years) and symptom
duration until surgery (weeks)
First symptom Cervicobrachial neu-
ralgia
Sensory deficit Motor deficit Gait disturbance
Medians P Value Medians P Value Medians P Value Medians P Value
Age (years) Yes 58 0.0005 62.5 0.466 66 0.229 68 0.0005
No 66 63 63 60
Symptom duration Yes 16 0.502 15 0.384 7.5 0.002 19,5 0.046
No 16 16 16 16
Frequency P Value Frequency P Value Frequency P Value Frequency P Value
Sex (female/male) 67/98 0.117 23/55 0.193 11/27 0.380 47/83 1.000
High SI 96/165 0.473 45/78 0.609 28/38 0.084 79/130 0.914
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330 European Spine Journal (2022) 31:327–333
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patients with other symptoms (median 15 versus 14 preop-
erative and median 18 versus 17 6months postoperative,
p = 0.0005) at all times of observation. The median mJOA
Score did not differ significantly in patients with or with-
out sensory deficits as first symptom, whereas patients with
motor deficits as first symptom showed significant lower pre-
operative mJOA Scores than patients without motor deficits
as first symptom (median 12.5 versus 15, p = 0.0005). Dur-
ing the postoperative follow-up, there was an improvement
of the mJOA Score in that cohort (median: 12.5–16.5), but
the significant difference compared to patients without motor
deficits remained (16.5 versus 17, p = 0.0005). Although the
patients with gait disturbance as first symptom showed sig-
nificantly lower initial mJOA Scores (median 14 versus 15,
p = 0.0005), the postoperative improvement was comparable
in all subgroups (mJOA score improvement by 3 points)
regarding the first clinical symptom (Table2).
Multivariate analysis
Multiple regression analysis of the first symptoms of DCM
showed that motor deficits are negative predictors for worse
neurological outcome at all times of observation accord-
ing to the mJOA Score. Gait disturbance was also a nega-
tive predictor for worse neurological outcome preoperative,
postoperative and 3months after surgery. Cervicobrachial
neuralgia was not associated with a worse neurological out-
come (Table3).
Table 2 First symptom of DCM and the relating median mJOA Score
Mann–Whitney U test First symptom Preoperative Postoperative 3months postoperative 6months postoperative
Median mJOA P value Median mJOA P value Median mJOA P value Median mJOA P value
Cervicobrachial neu-
ralgia
Yes 15 0.0005 16 0.0005 17 0.0005 18 0.0005
No 14 15 16 17
Sensory deficit Yes 15 0.200 15 0.200 16.5 0.285 17.5 0.431
No 15 15 17 17
Motor deficit Yes 12.5 0.0005 14 0.0005 15 0.0005 16.5 0.0005
No 15 16 17 17
Gait disturbance Yes 14 0.0005 15 0.0005 16 0.0005 17 0.010
No 15 16 17 18
Table 3 Multiple regression
analysis evaluating first
symptoms of DCM as
possible predictors for worse
neurological outcome according
to the mJOA Score
P values < 0.01 were considered significant
BSig 95.0% Confidence interval
for B
Lower bound Upper bound
preoperative mJOA Score 14.987 – 14.487 15.488
Cervicobrachial neuralgia − .084 0.785 − 0.691 0.523
Motor deficits − 2.750 0.000 − 3.625 − 1.876
Gait disturbance − 1.210 0.000 − 1.843 − 0.577
Postoperative mJOA Score 15.590 – 15.075 16.105
Cervicobrachial neuralgia 0.119 0.708 − 0.506 0.745
Motor deficits − 2.458 0.000 − 3.358 − 1.558
Gait disturbance − 1.005 0.003 − 1.657 − 0.353
3months postoperative mJOA Score 16.434 – 16.007 16.862
Cervicobrachial neuralgia 0.126 0.635 − 0.394 0.645
Motor deficits − 1.756 0.000 − 2.579 − 0.932
Gait disturbance − 0.814 0.004 − 1.360 − 0.269
6months postoperative mJOA Score 17.032 – 16.663 17.401
Cervicobrachial neuralgia 0.076 0.737 − 0.368 0.519
Motor deficits − 1.260 0.001 − 1.980 − 0.539
Gait disturbance − 0.458 0.059 − 0.933 0.017
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331European Spine Journal (2022) 31:327–333
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Lost tofollow‑up
The lost to follow-up was 6.6% (27 patients) three months
after surgery and 23.1% (95 patients) six months after surgery.
Discussion
The best treatment of mild DCM is still a matter of debate
[9]. Fehlings etal. identified regional differences in demo-
graphics, severity of myelopathy and extent of postopera-
tive improvements [20], which makes recommendations of
therapy even more difficult. It is possible that the sever-
ity of symptoms does not change over a long time, but
episodic deterioration is described [2, 14]. Therefore, the
timeframe of surgical intervention varies. Due to the vari-
ety of different symptoms and its expression, timely diag-
nosis of DCM, especially of mild DCM, might be difficult
in some cases [18, 21, 22]. The most common symptoms
of DCM are cervicobrachial neuralgia, sensory deficits,
motor deficits and gait disturbance [1].
Age, preoperative mJOA Score and the high SI on
T2-weighted MRI are known to have a negative influ-
ence on the postoperative neurological outcome [16–18].
Evaluation of the first symptoms and their influence on the
neurological outcome could also play an important role in
decision making, especially in timing of surgery.
Symptom duration was described as a negative outcome
predictor in several studies [18, 23, 24]. Holly etal. high-
light the importance of symptom duration and age for the
postoperative outcome of DCM patients [17]. In contrast,
Zika etal. found no correlation between symptom dura-
tion and neurological outcome after surgery for DCM [25].
The onset of the first symptoms of DCM might be unspe-
cific and covered by comorbidities. In our cohort, patients
with severe motor deficits showed a significant shorter
period from the beginning of symptoms until surgery of
DCM (7.5weeks) than patients without motor deficits as
first symptom (16weeks). Contrary, DCM was detected later
in patients with unspecific cervicobrachial neuralgia or gait
disturbance. Gait disturbances had the longest period with
19.5weeks. The age-dependent physical weakness in major-
ity of the elderly patients and the known comorbidities such
as hip and knee osteoarthritis, cerebral vascular disorders,
diabetic neuropathy, benign prostatic hypertrophy, or uri-
nary stress incontinence, or known entrapment of peripheral
neuropathy (carpal or cubital tunnel syndrome) might mimic
symptoms of DCM and therefore, prolong its diagnosis [26].
In our analysis, symptom duration was not a predictor
for worse neurological outcome. The favorable recovery
of preoperative deficits and the wide variance of symptom
duration until surgery (1 until 350weeks, median dura-
tion: 35.4weeks) could be reasonable. Additionally, the
retrospective character of the study itself could bias the
results and explain the different results compared to pro-
spective analysis of the current literature.
Cervicobrachial neuralgia was the most common first
symptom in our cohort. The preoperative and postopera-
tive mJOA Score was significantly higher in those patients
than in patients with other first symptoms (Table2). Cer-
vicobrachial neuralgia was seen in majority of mild DCM
(Table1). Therefore, cervicobrachial neuralgia failed to be
a predictor for a worse neurological outcome. Nevertheless,
Kadanka Jr. etal. were able to show in a prospective obser-
vational follow-up study of 112 patients suffering from
“non-myelopathic” degenerative cervical cord compression
that radiculopathy is an independent significant predictor
for progression into symptomatic DCM [27]. Therefore,
ongoing cervicobrachial neuralgia in mild DCM should be
consequently followed-up if conservative therapy is per-
formed. Surgery might be offered in those cases to prevent
possible deterioration of neurological symptoms.
Preoperative mJOA Score is known to be a negative pre-
dictor for postoperative neurological outcome [17, 18, 28].
Those results are comparable with our study. Baseline mJOA
Score was significant less in patients with motor deficits
compared to patients without motor deficits (12.5 versus 15,
p = 0.0005), and in patients with gait disturbance compared to
patients without gait disturbance (14 versus 15, p = 0.0005).
Therefore, preoperative motor deficit as the first symptom of
DCM was an independent predictor for worse neurological
outcome over the complete observational period, while gait
disturbance was an independent predictor of worse postop-
erative neurological outcome until three months postopera-
tive. However, the postoperative mJOA Score in patients with
motor deficits as first symptom of DCM improved compara-
ble to the patients with cervicobrachial neuralgia or sensory
deficits as the first symptom. Surgical treatment and the sig-
nificant shorter symptom duration until surgery (7.5weeks
for patients with motor deficits versus 16weeks for the other
patients) might have played a role in the favorable postopera-
tive, but still worse recovery of patients with preoperative
motor deficits and gait disturbance. Additionally, cervicobra-
chial neuralgia and sensory deficits do not predict the neu-
rological outcome, because they do not influence the mJOA
Score in a way motor deficits or gait disturbance do.
Neurological recovery in our study is in accordance with
the results of Goh etal., who were able to show that patients
with a severe DCM showed significantly greater improve-
ment in JOA, Neurogenic Symptoms, Neck Disability Index,
SF-36 Physical Component Summary, and Mental Component
Summary and a larger proportion attained Minimal clinically
important differencefor Neck Disability Index and SF-36
Physical Component Summary after surgery than patients with
moderate and mild DCM, while Minimal clinically impor-
tant differencewas equal for JOA Score [29]. Furthermore,
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332 European Spine Journal (2022) 31:327–333
1 3
surgical intervention for DCM is reducing the incidence rate
of falls (decreased significantly from 497.4 to 90.3 falls per
100 person-years) and the incidence of motor deterioration
per fall (decreased significantly from 34 to 8%) [30]. Surgery
can improve motor deficits and decrease nursing care require-
ments among elderly patients with DCM [31]. Therefore, early
surgery might be the treatment of choice to interfere the natural
history of DCM and improve the neurological prognosis [15,
16, 18, 21].
The signal change in T1- and T2-weighted MRI is well
known in DCM [12, 32, 33], but might be absent in 21% of
patients [34]. The high SI on T2-weighted MRI has been
attributed to edema, inflammation, gliosis and myelomalacia
after long-standing compression of the spinal cord [35]. There
is a significant correlation between T2-weighted SI and the
degree of spinal cord compression [12, 32]. Furthermore, high
SI on T2-weighted MRI is known to be a negative predictor
for neurological outcome [16, 36, 37]. For example, Vedantam
etal. demonstrated that a high SI in T2- weighted MRI is asso-
ciated with a lower rate on postoperative recovery [38]. Gibson
etal. reported a high correlation of Babinski sign, Hoffman’s
sign, inverted brachioradialis reflex and hyperreflexia with
the myelopathy and the consecutive spinal cord damage [13].
However, in our cohortthe symptoms at the onset of DCM
showed no significant correlation with SI in T2- weighted
MRI, but a statistical trend was seen in patients with motor
deficits. The statistical trend that motor deficits were associ-
ated with a significant higher amount of signal changes on
T2-weighted MRI might be caused by the small number of
patients presented with motor deficits as first symptom of
DCM. Only 38 patients (9.2%) suffered from motor deficits
as first symptom of DCM. Of those, 73.7% showed high SI
on T2-weighted MRI compared to patients with cervicobra-
chial neuralgia (58.2%), gait disturbances (60.8%) and sensory
deficits (57.7%). Therefore, significance might be reached in
a cohort with more patients suffering from motor deficits.
Additionally, cervicobrachial neuralgia, sensory deficits and
gait disturbance are symptoms, which might not result from
SI changes on MRI as a result of spinal cord damage alone.
Those symptoms are influenced by multiple other causes such
as comorbidities like diabetes mellitus or polyneuropathy, age,
and simply mislead of the cervical spine.
Study limitations
The main limitation of our study is the retrospective, non-rand-
omized character of the study with its associated inherent bias.
The incomplete follow-up and the short follow-up period of six
months limited the prediction and carries the risk of additional
information and selection bias. However, future prospective
studies with a longer follow-up are needed to evaluate the neu-
rological long-term outcome and to strengthen the predictive
analysis in patients.
Conclusion
Patients with motor deficits and gait disturbance as first
symptom of DCM showed significant lower mJOA Scores
than patients with cervicobrachial neuralgia or sensory
deficits and are, therefore, negative predictors for postop-
erative neurological outcome. Nevertheless, patients with
motor deficits and gait disturbance might significantly
profit from the surgical treatment, despite lower preop-
erative mJOA Score.
Author contributions NÖ, OG was involved in conceptualization
and methodology; NÖ, OG, MC contributed to formal analysis and
investigation; NÖ, OG, MC, TS were involved in writing—original
draft preparation; NÖ, MC, TS, TFD, MH, AP, RJ, YA, US, NEH,
OG contributed to writing—review and editing; US was involved in
supervision.
Funding Open Access funding enabled and organized by Projekt
DEAL. The authors did not receive support from any organization for
the submitted work.
Declarations
Conflict of interest The authors declare no conflict of interest.
Ethical approval The study has been carried out in accordance with
The Code of Ethics of the World Medical Association (Declaration of
Helsinki) and was approved by the Institutional Review Board (Medi-
cal Faculty of the University of Duisburg-Essen, registration number:
16–6270-BO).
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
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permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.
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