European Spine Journal (2021) 30:547–553

[Link]

ORIGINAL ARTICLE

Cervical arteriosclerosis is associated with preoperative clinical

symptoms in patients with cervical spondylotic myelopathy
Gentaro Kumagai1 · Kanichiro Wada1 · Sunao Tanaka1 · Toru Asari1 · Yasuyuki Ishibashi1

Received: 15 May 2020 / Accepted: 20 October 2020 / Published online: 9 November 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Purpose This study aims to clarify the association between cervical spondylotic myelopathy (CSM) and cervical arterio-
sclerosis using ultrasonography that comprehensively includes spinal cord stenosis.
Methods Eighty-two consecutive patients aged over 60 years who underwent spine surgery were divided into those with
CSM (n = 31; CSM group) and those with lumbar spinal stenosis without cervical myelopathy (n = 51; LSS group). Maximum
spinal cord compression (MSCC) was evaluated for cervical stenosis severity using magnetic resonance (MR) images. The
intima–media thickness (IMT) of the common carotid artery (CCA) and pulsatility index (PI) of the bilateral internal carotid
artery (ICA) and vertebral artery (VA) were evaluated for cervical arteriosclerosis using pulsed-wave Doppler ultrasonog-
raphy. Symptom severity was evaluated using the Japanese Orthopaedic Association (JOA) score. Spearman’s correlation
coefficient was used to determine the relationship between the JOA score and MSCC or IMT and PI in each group. Stepwise
multiple linear regression analyses were conducted with the JOA score as a dependent variable and age, sex, body mass
index, cervical arteriosclerosis assessment, and MSCC as independent variables.
Results Bilateral IMT and left-side ICA-PI were significantly negatively correlated with JOA scores in the CSM group
(Right-CCA-IMT: R =  − 0.412, Left-IMT: R =  − 0.549, Left-ICA -PI: R =  − 0.205, P < 0.05), but not in the LSS group.
Multiple linear regression analyses showed that CCA-IMT was the strongest independent factor associated with the preop-
erative JOA score.
Conclusions Cervical arteriosclerosis was associated with preoperative clinical symptoms in CSM patients.

Keywords Cervical spondylotic myelopathy · Cervical arteriosclerosis · Ultrasonography · Cervical stenosis

Introduction arch calcification was associated with significantly worse

clinical outcomes after laminoplasty for CSM [6]. However,
Cervical spondylotic myelopathy (CSM) is a common prob- the association between cervical myelopathy and cervical
lem affecting elderly individuals. Myelopathy is a serious arteriosclerosis remains unclear. The aim of this study is
spondylosis sequela, occurring in approximately 5–10% of to clarify the association between the clinical symptoms of
spondylosis patients [1], and most of whom require surgical CSM patients and cervical arteriosclerosis using ultrasonog-
management. raphy that comprehensively included spinal cord stenosis.
Although static or dynamic mechanical factors are asso-
ciated with cervical myelopathy, these mechanisms remain
unclear. Recently, the associations between arteriosclero- Materials and methods
sis and renal disease [2, 3], heart disease [4], and stroke
[5] have been reported. Sakaura et al. reported that aortic Subjects

Eighty-two consecutive patients aged over 60 years who

* Gentaro Kumagai
gengen722@[Link] underwent spine surgery were enrolled in this retrospective
cohort study. Patients with trauma, rheumatoid arthritis, or
1
Department of Orthopaedic Surgery, Hirosaki University posterior longitudinal ligament ossification were excluded
Graduate School of Medicine, 5 Zaifu‑cho, Hirosaki, from this study. The patients were divided into 2 groups:
Aomori 036‑8562, Japan

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548 European Spine Journal (2021) 30:547–553

those with cervical myelopathy (CSM group; n = 31, 18 lipoprotein cholesterol (mg/dl), triglyceride (mg/dl), glu-
men and 13 women; average age, 71.7 years, follow-up cose (mg/dl), and hemoglobin A1c (HbA1c, %) levels.
period, 17.1 months) and the control group including those Arteriosclerosis assessments were performed using ultra-
with lumbar spinal stenosis without cervical myelopathy sound (a Prosound Alpha-7; Aloka Co. Ltd, Tokyo) and a
(LSS group; n = 51, 21 men and 30 women; average age, 7.5–10.0 MHz linear-array probe by laboratory technicians
70.9 years, follow-up period, 29.5 months). All patients pro- with over 5 years of experience after admission and at least
vided written informed consent before the assessment. This 1 week prior to surgery as described previously [8, 9]. The
study was approved by the institutional ethics committee. ultrasound examiner was blinded regarding assessment
All patients underwent magnetic resonance imag- results. Cervical artery plaque and stenosis prevalence, com-
ing (MRI) (Exelart 1.5 T MRI system; Toshiba Co., Ltd., mon carotid artery (CCA) intima–media thickness (IMT),
Japan) for cervical spine examination prior to surgery. We and bilateral internal carotid artery (ICA) and vertebral
confirmed the absence of cervical stenosis among patients artery (VA) pulsatility indexes (PIs) were evaluated for
in the LSS group. The prevalence of the high intensity of the cervical arteriosclerosis using pulsed-wave Doppler ultra-
cervical spinal cord, which indicates pathological changes, sonography measurement (Fig. 2a). CCA-IMT was defined
was evaluated by preoperative T2-weighted midsagittal MR as the greatest thickness of the carotid arteries intima–media
images among patients in the CSM group (Fig. 1a). Maxi- complex (Fig. 2b). The intraobserver variation coefficient
mum cervical spine spinal cord compression (MSCC), using for CCA-IMT was 3.6% as previously described [8]. Flow
method modifications described by Nouri et al. [7], was velocity waveforms were measured using range-gated spec-
measured by preoperative T1-weighted midsagittal images tral Doppler signals averaged along the Doppler beam. ICA-
to assess the severity of cervical stenosis in the CSM group and VA-PI were calculated as follows: (Vs − Vd)/Vm, where
and was defined using the formula maximum compressed Vs is the peak systolic velocity, Vd is the diastolic velocity,
rate of the spinal cord (%) = (distance at spinal cord where and Vm is the mean velocity (Fig. 2c, d) [9]. The examina-
the maximum stenosis level is found)/(distance at spinal tion reliability of measures in healthy adults suggested good
cord, with normal level measurements, immediately adjacent reproducibility (overall intraclass correlation coefficient:
to 1 or 2 above sites) × 100 (Fig. 1b). Two examiners, with 0.90–0.99) [9]. High IMT and PI indicate arteriosclerosis
15 and 16 years of experience as spine surgeons, analyzed progression and peripheral tissue ischemia.
the prevalence of high intensity and MSCC in MR images. For CSM patients, a laminectomy was performed at C3,
The examiners were blinded regarding patient demographic and the semispinalis cervicis muscle insertion in C2 was
data, such as age and sex. preserved entirely as previously described [10]. We per-
Laboratory data, ankle brachial pressure index (ABI), formed a C4–C7 or C4–C6 laminoplasty using a procedure
systolic blood pressure (mmHg), diastolic blood pressure adapted from the spinous process. The laminoplasty was
(mmHg), and cervical arteriosclerosis were evaluated for split using hydroxyapatite spinous process spacers [11], and
arteriosclerosis assessment. Laboratory tests for arterio- the spinous process was split using a thread-wire saw [12].
sclerosis assessment included total cholesterol (mg/dl), A suction tube placed between the laminae and the deep
high-density lipoprotein cholesterol (mg/dl), low-density muscle to drain postoperative bleeding was removed within

Fig. 1  a The prevalence of

high intensity was evaluated
using preoperative T2-weighted
midsagittal magnetic resonance
imaging (white arrow head).
b The spinal cord maximum
compressed rate (MCR)
was measured on preopera-
tive T1-weighted midsagittal
images: spinal cord MCR
(%) = (distance at spinal cord
where the maximum steno-
sis level is found)/(distance
at spinal cord, with normal
level measurements, immedi-
ately adjacent to 1 or 2 above
sites) × 100 (white arrows)

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European Spine Journal (2021) 30:547–553 549

Fig. 2  a Cervical artery evaluation. b Representative ultrasonogra- ity index (PI) is measured as the internal carotid artery c and verte-
phy shows plaque in the common carotid artery (CCA). intima–media bral artery d resistance. High IMT and PI indicates peripheral tissue
thickness (IMT), which is the CCA plaque thickness, is measured. ischemia. CCA​ common carotid artery, IMT intima–media thickness,
Right-side measure mean IMT was 1.522 mm. (c, d) The pulsatil- PI pulsatility index, ICA internal carotid artery, VA vertebral artery

2 days postoperatively. Postoperative collars were not used. correlation coefficient [13]. We compared the CSM and
Patients began exercises one day postoperatively and were LSS groups using the Mann–Whitney U test and Chi-
allowed to sit up or walk on the second day postoperatively. squared test for quantitative and qualitative data, respec-
Clinical symptom severity was evaluated using the Japa- tively. We compared the preoperative and postoperative
nese Orthopaedic Association (JOA) score prior to surgery JOA score using Wilcoxon rank-sum test in the CSM
in both groups and at final follow-up in the CSM group; group. We used the Spearman’s rank correlation coeffi-
further, the JOA recovery rate was evaluated. The JOA score cient to analyze the correlations between the JOA score
recovery rate at final follow-up was calculated as follows: and laboratory results, ABI, BP, MSCC or IMT/PI in both
recovery rate (%) = (postoperative JOA score − preoperative groups. We also used the Spearman’s rank correlation
JOA score)/(17 − preoperative JOA score) × 100. coefficient to analyze the correlations between the JOA
recovery rate and MSCC or IMT/PI in the CSM group.
Statistical analysis Stepwise multiple linear regression analyses were con-
ducted using preoperative JOA scores as the dependent
The Statistical Package for the Social Sciences (SPSS variable. The independent variables used were age, sex,
Inc., Chicago, IL, USA) version 12.0 J was used for data body mass index (BMI), MSCC, and cervical arterioscle-
input and statistical calculations. The reliability of the rosis parameters. Values were expressed as means ± stand-
prevalence of high intensity and MSCC in MR images ard deviation, and a p value higher than 0.05 was consid-
was determined regarding the kappa value and intraclass ered statistically significant.

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Table 1  Patient characteristics Table 2  Arteriosclerosis assessment

a b
CSM Group LSS Group P value CSMh Group LSSi Group P value
(31 patients) (51 patients) (31 patients) (51 patients)

Age, years 71.7 ± 8.0 70.9 ± 6.7 0.622 Laboratory results

Males, % of group 58.1% 41.2% 0.173 TCa (mg/dl) 193.2 ± 43.5 195.8 ± 45.1 0.779
BMIc, kg/m2 23.7 ± 4.0 25.1 ± 4.8 0.158 HDLb cholesterol (mg/dl) 55.5 ± 11.9 53.8 ± 14.8 0.645
DMd, N (%) 11 (35.4) 14 (27.5) 0.468 LDLc cholesterol (mg/dl) 104.8 ± 30.9 115.0 ± 46.1 0.063
HLe, N (%) 1 (3.2) 2 (3.9) 0.681 Triglycerides (mg/dl) 143.1 ± 90.7 136.5 ± 82.6 0.981
HTf, N (%) 14 (48.4) 27 (52.9) 0.820 Glucose (mg/dl) 132.0 ± 53.7 119.3 ± 34.7 0.392
Preoperative ­JOAg score 9.8 ± 4.0 13.7 ± 2.0 < 0.001h HbA1cd (%) 6.1 ± 1.0 5.7 ± 0.7 0.169
Postoperative JOA score 11.3 ± 3.1i – ABIe Left 1.1 ± 0.1 1.1 ± 0.1 0.496
JOA recovery rate (%) 22.8 ± 47.8 – – Right 1.1 ± 0.1 1.1 ± 0.1 0.652
SBPf (mmHg) 131.3 ± 16.5 132.7 ± 20.0 0.922
P < 0.05 DBPg (mmHg) 82.2 ± 13.4 83.6 ± 12.5 0.711
a
Cervical spondylotic myelopathy; blumbar spinal stenosis; cbody Cervical arteriosclerosis
mass index; ddiabetes mellitus; ehyperlipemia; fhypertension; gJapa-
Plaque, N (%) 23 (74.2) 32 (62.8) 0.228
nese Orthopaedic Association; hMann–Whitney U test; iWilcoxon
rank-sum testversus preoperative JOA score Stenosis, N (%) 0 (0) 2 (3.9) 0.820
CCA​j-IMTk Left 0.8 ± 0.2 0.9 ± 0.3 0.672
Right 0.9 ± 0.2 0.9 ± 0.3 0.913
Results ICAl-PIm Left 1.1 ± 0.3 1.1 ± 0.3 0.968
Right 1.1 ± 0.3 1.1 ± 0.2 0.590
Patient characteristics and JOA score
VAn-PI Left 1.3 ± 0.3 1.1 ± 0.5 0.586
Right 1.4 ± 0.4 1.3 ± 0.4 0.090
The CSM and LSS groups did not differ significantly in
a
age, sex, BMI, or prevalence of medical history (Table 1). Total cholesterol; bhigh-density lipoproteins; clow-density lipopro-
The preoperative JOA score was significantly lower in teins; dhemoglobin A1c; eAnkle Brachial Pressure Index; fsystolic
blood pressure; gdiastolic blood pressure; hcervical spondylotic mye-
the CSM group (9.8 ± 4.0) than that in the LSS group lopathy; ilumbar spinal stenosis; jcommon carotid artery; kintima–
(13.7 ± 2.0, P < 0.001) (Table 1). The postoperative JOA media ­thicknesslInternal carotid artery; mpulsability index; nvertebral
score (11.3 ± 3.1) was significantly higher than the preop- artery
erative JOA score in the CSM group (P = 0.031) (Table 1).
The JOA recovery score was 22.8 ± 47.8% in the CSM group
(Table 1). correlated with the preoperative JOA score in the CSM group
(Table 3). The bilateral IMT and Left-ICA-PI were signifi-
Cervical spine high intensity and MSCC on MR cantly negatively correlated with the preoperative JOA scores
images in the CSM group (Right-CCA-IMT: R =  − 0.412, Left-IMT:
R =  − 0.549, Left-ICA -PI: R =  − 0.205, P < 0.05), though not
The kappa value for judgment of high intensity was 0.608, in the LSS group (Table 3). MSCC was significantly posi-
and good interobserver reliability was observed. The intra- tively correlated with JOA recovery rate in the CSM group
class correlation coefficient for MSSC measurement was (R = 0.386, P = 0.032) (Table 4). IMT and PI did not correlate
0.928, and high interobserver reliability was observed. with the JOA recovery rate in the CSM group (Table 4). Step-
The prevalence of the spinal cord high intensity was 83.9% wise multiple linear analyses showed a significant correlation
(26/31 patients) in the CSM group. The preoperative JOA between the preoperative JOA score and CCA-IMT left side
score (with high intensity: 9.7 ± 4.2, without: 10.1 ± 2.6) (B =  − 11.773, 95%CI: − 21.249 to − 2.298) (Table 5). In
and JOA recovery (with high intensity: 26.2 ± 46.1, without: this analysis, the cervical arteriosclerosis parameters corre-
5.2 ± 58.3) did not differ significantly between patients with lated with the preoperative JOA score in the single correlation
or without spinal cord high intensity. The average MSCC analysis (bilateral of CCA-IMT and left side of ICA-PI).
was 37.5% (maximum rate: 62.2%, minimum rate: 8.6%) in
the CSM group.
Laboratory results, ABI, BP, plaque and stenosis preva- Discussion
lence, IMT, and ICA and VA PIs did not differ significantly
between the CSM and LSS groups (Table 2). Laboratory To the best our knowledge, this is the first study to analyze
results, ABI, and BP were not correlated with the JOA the association between cervical arteriosclerosis and pre-
score in both groups (data not shown). The MSCC was not operative symptoms for CSM patients and between LSS

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Table 3  Correlations between Partial correlation CSMj group LSSk group

the preoperative Japanese coefficient:
Orthopaedic Association score rg P value n R P value n
and MSCC or IMT/PI in both
a
groups MSCC − 0.246 0.183 31 – –
CCA​b–IMTe
Left − 0.549 0.0003* 31 − 0.035 0.819 51
Right − 0.412 0.026* 31 − 0.033 0.825 51
ICAc–PIf
Left − 0.412 0.021* 31 0.061 0.683 51
Right − 0.226 0.221 31 − 0.120 0.412 51
VAd–PI
Left − 0.158 0.397 31 0.102 0.481 51
Right − 0.205 0.269 31 0.005 0.975 51
a
Maximum spinal cord compression; bcommon carotid artery; cInternal carotid artery; dvertebral artery;
e
intima–media thickness; fpulsatility index; gcorrelation coefficient; jcervical spondylotic myelopathy;
k
lumbar spinal stenosis
*
P < 0.05. Relationships between the preoperative Japanese Orthopaedic Association score and IMT/PI
were analyzed by Spearman’s rank partial correlation analysis. P values below 0.05 (*) indicate signifi-
cance

Table 4  Correlations between the Japanese Orthopaedic Association Ogino et al. showed an association between cord com-
recovery rate and IMT/PI in CSM group pression and cord pathology in patients with cervical mye-
Partial correlation coef- CSMb group lopathy [14]. Several studies showed that the degree of cord
ficient: compression was related to worse neurological performance
r P value n
in the quantitative MRI study [7, 15, 16]. In our study,
MSCCa 0.386 0.032* 31 although the preoperative JOA score was not correlated
CCA​c-IMTd with cord compression, JOA recovery rate increased with
Left 0.142 0.481 31 increased cord compression in the CSM group. This finding
Right 0.317 0.094 31 suggested that spinal cord decompression may affect clini-
ICAe-PIf cal recovery. However, multiple linear regression analysis
Left − 0.139 0.456 31 showed that MSCC was not associated with the preclinical
Right 0.093 0.619 31 JOA score. However, the relationships between T2 signal
VAg-PI change and symptoms were stronger than those in MSCC
Left 0.032 0.866 31 [7]. Our study showed that the preoperative JOA score
Right 0.092 0.623 31 and JOA recovery rate did not differ significantly between
a patients with and without spinal cord high intensity. This
Maximum spinal cord compression; bcervical spondylotic myelopa-
thy; ccommon carotid artery; dmaximum spinal cord compression; may be attributed to the need for surgery in our study owing
e
Internal carotid artery; fpulsatility index; gvertebral artery to the high prevalence of spinal cord high intensity (83.9%).
*
P < 0.05. Relationships between the JOA recovery rate and IMT/PI We showed that cervical arteriosclerosis was associ-
were analyzed by Spearman’s rank partial correlation analysis. P val- ated with preoperative clinical symptoms in CSM patients.
ues below 0.05 (*) indicate significance
Recently, a study on spinal cords of patients with cervical
myelopathy has demonstrated the underlying phenomena
and surgical outcomes for the aforementioned patients. related to chronic and progressive compression and impli-
Although laboratory results, ABI, and BP were not cor- cated chronic stretching in important pathophysiological
related with the preoperative JOA score, cervical arte- events [17]. In addition to stretching and static compres-
riosclerosis was significantly negatively correlated with sion, the spinal cord may be injured through dynamic injury
preoperative JOA scores in the CSM group, but not in mechanisms [18–21]. Particularly, chronic cervical spinal
the LSS group in single-variable correlation analyses. cord compression results in chronic intraparenchymal spinal
Multiple linear regression analyses that comprehensively cord blood flow reduction [22, 23]. However, it is difficult
included MSCC showed that CCA-IMT was the strongest to evaluate spinal cord blood flow using computed tomog-
independent factor associated with the preoperative JOA raphy or MRI. Tsuji et al. investigated intraoperative power
score. Cervical arteriosclerosis was not associated with Doppler ultrasonography, which was used to evaluate the
surgical outcomes in the CSM group. spinal cord blood flow in CSM patients during hypotensive

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Table 5  Stepwise multiple Logistic regression (the preopera- Bc βd 95% CI P value

regression analysis relative to tive JOA score), ­r2b = 0.658
the preoperative J­ OAa ­score*
Age − 0.056 − 0.109 − 0.244–0.133 0.541
Sex − 1.446 − 0.176 − 4.303–1.411 0.299
BMI, kg/m2 0.731 0.656 0.260–1.201 0.367
MSCCe, % − 0.088 − 0.295 − 0.199–0.23 0.113
CCA​f-IMTg
Left − 11.773 − 0.456 − 21.249 to − 2.298 0.017
Right 0.229 0.011 − 7.803–8.260 0.953
ICAh-PIi
Left − 1.587 3.401 − 16.704–1.714 0.104
a
Japanese Orthopedic Association; coefficient of determination (adjeusted); regression coefficient; dstand-
b c

ardized regression coefficient; emaximum spinal cord compression; fcommon carotid artery; gintima–media
thickness; hInternal carotid artery; ipulsatility index
*
Stepwise multiple regression analysis performed using the preoperative JOA score as the dependent vari-
able and age, sex, BMI, MSCC, and cervical arteriosclerosis parameters as the independent variables. The
cervical arteriosclerosis parameters are correlated with the preoperative JOA score in the single correlation
analysis (bilateral of CCA-IMT and left side of ICA-PI)

anesthesia [24]. This study showed that the blood flow in with CSM. Therefore, evaluating cervical arteriosclerosis
the anterior spinal cord artery was measured and associated may be a supportive tool for CSM severity, and improve-
with induced hypotension. Although anterior spinal cord ment in arteriosclerosis without surgical intervention may
artery measurement may be useful for evaluating spinal cord provide a novel strategy for cervical myelopathy treatment
function, its use is limited in intraoperative ultrasonography. in the future.
Our cervical artery findings, using ultrasonography, may be In conclusion, cervical arteriosclerosis that comprehen-
useful for preclinical evaluation. Previous studies suggested sively included the spinal cord compression was associated
that systemic arteriosclerosis such as chronic kidney disease with preoperative clinical symptoms in patients with CSM.
(CDK), hyperlipidemia, hypertension, and diabetes mellitus
in patients may induce spine degeneration and neural tissue Acknowledgements This study was supported by Dr Toshihiro Tan-
aka from the Department of Orthopaedic Surgery, Takaoka Seishikai
damage, and lack of blood flow to nerves or spinal cord Hospital, Toyama, Japan and Dr Hitoshi Kudo from the Department
owing to advanced systemic arteriosclerosis may result in of Orthopaedic Surgery, Mutsu General Hospital, Aomori, Japan. We
poor neurological recovery after decompression surgery [6, would like to thank Editage ([Link]​[Link]) for English language
25]. In this study, although cervical arteriosclerosis was not editing.
associated with surgical outcomes, it was associated with
Author contributions GK, KW, and YI conceived and designed the
preoperative clinical symptoms in CSM patients. Certain experiments; GK, WK, ST, and TA performed the experiments; and
renal diseases produced states of increased renal vascular GK analyzed the data and wrote the paper.
resistance calculated from the duplex Doppler waveform
[2]. We also hypothesized that cervical resistance induced Funding None.
by cervical arteriosclerosis was associated with spinal cord
function. Our results may support the association between Compliance with ethical standards
cervical artery resistance and spinal function.
This study had the following limitations. First, we did Conflict of interest The authors have no relevant financial or non-fi-
nancial interests to disclose.
not evaluate normal subjects without cervical and lumbar
stenosis. Second, the patients were analyzed while under Ethics approval This study was approved by the institutional ethics
medications for hypertension, dyslipidemia, and other meta- committee.
bolic abnormalities associated with cervical arteriosclerosis.
Therefore, our data might have underestimated the effects of
these factors on arteriosclerosis. Third, we did not evaluate
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