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Journal of Medical Ultrasonics

https://doi.org/10.1007/s10396-017-0855-9

ORIGINAL ARTICLE

Investigation of the effectiveness of therapeutic ultrasound


with high‑resolution ultrasonographic cross‑sectional area
measurement of cervical nerve roots in patients with chronic cervical
radiculopathy: a prospective, controlled, single‑blind study
Burcu Metin Ökmen1   · Korgün Ökmen2 · Lale Altan1,3

Received: 7 July 2017 / Accepted: 6 December 2017


© The Japan Society of Ultrasonics in Medicine 2018

Abstract
Purpose  The purpose of our study was to evaluate the effects of therapeutic ultrasound (US) on chronic cervical radiculopathy
(CR) patients using both the clinical parameters and the cross-sectional area (CSA) values of the cervical nerve roots (NR)
measured by high-resolution ultrasonography (HRUS).
Methods  Thirty-two patients with chronic CR were included in this prospective, controlled, and single-blind study. All
of the patients received therapeutic US at continuous mode, 1-MHz frequency, and 1.5-W/cm2 intensity for 10 sessions.
The patients were assessed using VAS for pain, Modified Neck Disability Index, and Short-form 12, and cervical NR were
examined with HRUS. The data were obtained before treatment (W0), the second week immediately after treatment (W2),
and at the sixth week (W6).
Results  Twenty-nine patients and a total of 42 affected cervical NR and 42 unaffected cervical NR (control group) were
evaluated. A significant improvement was observed for all clinical parameters and CSA values of affected cervical NR both
at W2 and W6 compared to pre-treatment values (p < 0.05).
Conclusions  We found therapeutic US to be beneficial in improvement of pain, disability, and quality of life of patients
with chronic CR. We suggest that CSA measurements may also contribute to both diagnosis and post-treatment evaluation
in chronic CR.

Keywords  Chronic cervical radiculopathy · Therapeutic ultrasound · High-resolution ultrasonography · Cervical nerve
root · Cross-sectional area

Introduction

Cervical radiculopathy (CR) is a pathological process


involving entrapment and inflammation of the cervical nerve
roots (NR) [1]. Diagnosis of CR is usually made based on
the symptoms of pain and paresthesia in the dermatome of
* Burcu Metin Ökmen the affected segment, neurological examination, radiology,
burcumetinokmen@gmail.com and electrodiagnostic tests [1, 2]. While magnetic resonance
1 imaging (MRI) is an established diagnostic tool for CR,
Department of Physical Medicine and Rehabilitation, Bursa
Yuksek Ihtisas Training and Research Hospital, University some patients do not have access to MRI because of its cost
of Health Sciences, Mimar Sinan Mah, Emniyet Street, and scheduling problems [3]. High-resolution ultrasonogra-
Yıldırım, Bursa, Turkey phy (HRUS) has been gaining popularity in diagnosis and
2
Department of Anesthesiology and Reanimation, Bursa monitoring of several peripheral and central nervous sys-
Yuksek Ihtisas Training and Research Hospital, University tem disorders as a portable, noninvasive, radiation-free, less
of Health Sciences, Bursa, Turkey
expensive, and easily accessible tool [4].
3
Department of Physical Medicine and Rehabilitation, Uludag
University Faculty of Medicine, Bursa, Turkey

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Journal of Medical Ultrasonics

Ultrasonographic imaging allows measurement of the Thirty-two patients who were eligible for the study were
cross-sectional area (CSA) of the peripheral nerve and detec- given detailed information about the study, and an informed
tion of segmentary or diffuse constriction or swelling of the consent form was signed by each of them. Forms detailing
affected nerve as well as the changes in its echogenicity [5]. the patients’ demographic characteristics and pre-treatment
It has been previously documented that CSAs of the cervical (W0) measurements were filled in. All US measurements
NR on the affected side are larger compared to the unaf- were performed by a single physician trained and specialized
fected side in CR patients according to measurements made in musculoskeletal nerve US. Patient histories, clinical find-
by HRUS [6, 7]. ings, and MRI results were not accessible by the researcher
Immobilization, manipulation, medical treatment, and who made the measurements (Fig. 1).
several physical therapy modalities are used for treatment
of CR. Therapeutic ultrasound (US) is frequently used in
conservative treatment of CR because of its thermal and Interventions
non-thermal effects [8, 9]. Typically, the thermal effects are
employed for treatment of pain, reduction of subacute and A BTL 4625 US device (BTL, Czech Republic) was applied
chronic inflammation and muscle spasm, and stretching of in continuous mode, 1-MHz frequency, and 1.5-W/cm2
collagenous tissue in joint and connective tissue contractures intensity over the neck surface area. The headpiece area of
[10]. Low-dose non-thermal US is used for stimulation of the device was 5 cm2. The headpiece was placed on the para-
tissue repair [11] and reduction of edema [10]. US has also vertebral muscles and trapezius muscle in the posterolateral
been shown to increase muscle temperature and blood flow, zone of the neck. The application was performed with the
nerve conduction velocity, and extensibility of the connec- head of the device positioned perpendicular to and in full
tive tissue [12–15]. contact with the skin for 10 min using gel and a continuous
While there have been several studies assessing the effects circular motion for 5 consecutive days a week for 2 weeks
of therapeutic US on chronic neck pain [16, 17], we could (a total of 10 sessions).
not find a report as to its specific effects on chronic CR. For
this reason, the purpose of our study was to evaluate the
effects of therapeutic US on chronic CR patients primarily Evaluation parameters
based on the CSA values of the cervical NR measured by
HRUS and secondarily using the clinical parameters. Primary outcome measures

High-resolution ultrasonography measurements were


Materials and methods performed using a 12- to 18-MHz linear probe (Esaote
Mylab30, Genova, Italy). All patients were seated with lat-
This study was planned as a prospective, controlled, and eral flexion of the neck with their heads facing the opposite
single-blind study. After receiving local ethics committee side of the NR examined. Contralateral unaffected NR were
approval (Decision number 2011-KAEK-25 2016/16-09), 40 also evaluated as a control. To prevent anisotropy during
patients with CR were evaluated for eligibility. measurement with HRUS, the transducer was held at right
angles, applied with minimum pressure, and the transducer
Patients was rotated to find the point where the CSA was minimal.
C5 and C6 transverse processes have apical anterior and
The inclusion criteria were: (1) ages between 30 and posterior tubercles, and the C7 transverse process has a
65 years; (2) neck pain for more than 3 months; (3) CR rudimentary anterior tubercle and a distinctive posterior
diagnosis with history and physical examination findings tubercle. For this reason, the level of C7 vertebra was first
[segmental sensory disturbances corresponding to MRI find- detected by ultrasound scanning [6]. The anterior and pos-
ings, minimal motor deficits (muscle strength 4 or 4 +/5)]; terior tubercles of C6 were scanned in the transverse plane
(4) C5, C6, and C7 NR pressure evident on cervical MRI; where the nerve root passed between the tubercles for imag-
and (5) electromyography findings consistent with cervical ing of the nerve root. The transducer was moved superiorly
MRI and clinical examination. from the C6 transverse process to image the C5 nerve root or
The exclusion criteria were: (1) diabetes mellitus, (2) otherwise inferiorly to image the C7 root [6]. C5, C6, and C7
peripheral and central nervous system disease, (3) poly- cervical NR were evaluated in an axial view in accordance
neuropathy, (4) inflammatory rheumatic disease, (5) malig- with the shapes of the transverse processes. The transducer
nancy, (6) history of surgical intervention on the neck area, was maintained at the most proximal location possible, typi-
and (7) certain surgical indications (e.g., progressive neu- cally at the point where the nerve root exited over the trans-
rological deficit). verse process [6] (Fig. 2).

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Journal of Medical Ultrasonics

Enrollment
Patients Assessed ForEligibity (n=40)

Not Included (n=8)


• Diabetes Mellitus (n=5)
• with a history of surgical
intervention of neck area (n=1)
• polyneuropathy (n=2)

Patients Included the Study (n=32)

Patients evaluated with VAS, mNDI, SF-12


and CNR were examined with CSA at W0
(n=32)

Patients Received Therapeutic Ultrasound


Therapy (n=32)

Patients evaluated with VAS, mNDI, SF-12 Patients did not attend follow-ups
and CNR were examined with CSA at W2 because of the private reasons (n=3)
(n=32)

Patients evaluated with VAS, mNDI, SF-12


and CNR were examined with CSA at W6
(n=29)

Patient analyzed (n=29)

W0:Week 0 (Pretreatment), W2:Week 2 (Immediately after treatment ), W6: Week 6


CNR: Cervical nerve roots, CSA: Cross-Sectional Area
VAS: Visual Analog Scale, mNDI: Modified Neck Disability Index, SF-12: Short form 12

Fig. 1  Flowchart of the study

Secondary outcome measures Modified Neck Disability Index (mNDI) Disability was
assessed using mNDI, which comprises ten parts evaluating
Visual analog scale (VAS) The VAS is a widely used scale neck pain intensity, self-care, lifting load, reading, headache,
developed by Price and colleagues to assess the severity of concentration, working, driving, sleeping, and leisure time
the pain felt by the patient. The patient rated pain on a 0–10 activities. Each part has six possible answers scored from 0
scale, with 0 representing no pain and 10 representing the (no disability) to 5 (complete disability) giving a total score
worst pain imaginable [18]. of 0 (no disability) to 50 (total disability) or a percentage

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Journal of Medical Ultrasonics

Fig. 2  Measurement of CSA of a C7 cervical spinal nerve roots, b C6 cervical spinal nerve roots, and c C5 cervical spinal nerve roots via US in
patients with cervical radiculopathy

of 0–100. Turkish validity and reliability was performed by of the data was tested using the Shapiro–Wilk test. Nor-
Kesiktaş and colleagues [19]. mal distribution was found. Paired samples t test was used
Short-form 12 (SF-12): Twelve different items were to compare the difference in the CSA between the affected
taken from the eight different headings of SF-36, and the and unaffected nerve roots, and it was also used in intra-
shorter SF-12 form was created. The SF-12 has physical group analysis of other evaluation parameters. Spearman
(SF-12-PCS) and mental (SF-12-MCS) state assessment rank-order correlations were assessed between the CSA
scales, of which regression analyses have been performed of the affected nerve root and the duration of symptoms.
in the general public. The physical and mental health sum Values with a probability of (p) α < 0.05 were accepted as
scales were computed using the scores of twelve questions significant.
and range from 0 to 100, where a zero score indicates the
lowest level of health measured by the scales and 100 indi-
cates the highest level of health [20].
No drug was given to the patients throughout the study. Results
The same researcher completed the second (W2) and
sixth week (W6) evaluations. The researcher who performed Three patients abandoned the study for personal reasons.
W0 HRUS measurements again performed NR CSA meas- The present study was completed with 29 patients. No
urements in W2 and W6 (Figs. 1, 3). patient was left out of the study due to any side effect of the
treatment (Fig. 1).
Statistical analysis The distribution of age, sex, body mass index, and com-
plaint duration of the patients are presented in Table 1. Pre-
Analysis of the collected data was performed using IBM treatment (W0), second (W2), and sixth (W6) week evalua-
SPSS 22.0 statistical package program. Descriptive statistics tion of the parameters are presented in Table 2. A significant
were calculated to summarize the data. Normal distribution improvement was observed for all parameters both at W2

Fig. 3  Pre- and post-treatment HRUS images of C7 cervical spinal nerve root. a Pre-treatment image, b post-treatment image. PT posterior
tubercle, VA vertebral artery

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Journal of Medical Ultrasonics

Table 1  Analysis of the demographic data of the patients pre-treatment values (p  <  0.05). In unaffected (control
Patients (n = 29)
group) NR, there was no statistically significant difference
in CSA values both at W2 and W6 compared to the pre-
Age 44.97 ± 7.90 treatment values (p > 0.05) (Table 3).
Gender (F/M) 20/9 (69%/31%) Comparison of the affected and control NR showed that
BMI (kg/m2) 24.55 ± 2.25 CSA values were significantly higher on the affected side
Symptom duration (month) 26.83 ± 36.2 at all evaluation periods (W0, W2, and W6) (p < 0.05)
Mean ± SD (Table 3).
BMI body mass index
A statistically significant correlation in the positive direc-
tion was found by correlation analysis of symptom duration
and affected NR (Spearman’s R for C5: 0.707, p = 0.001,
and W6 compared to the pre-treatment values (p < 0.05) Spearman’s R for C6: 0.842, p < 0.001, Spearman’s R for
(Table 2). C7: 0.777, p = 0.040) (Fig. 4).
Nine of 29 patients were affected in only the C5 root
(n = 9), four in only the C6 root (n = 4), three in only the
C7 root (n = 3), nine in both the C5 (n = 9) and C6 (n = 9) Discussion
roots (a total of 18 roots), and four in both the C6 (n = 4)
and C7 (n = 4) roots (a total of 8 roots). Thus, a total of 42 The results of our study showed that therapeutic US pro-
affected NR (which were correlated with electromyography vided improvement in the parameters of pain, disability, and
findings consistent with cervical MRI and clinical examina- quality of life in patients with chronic CR. HRUS meas-
tion) and 42 unaffected NR (control group) were evaluated urements revealed a significant decrease in CSAs of the
in our study. The distribution of the affected NR according affected NR. However, CSA values of the affected NR were
to their level is presented in Table 3. still higher than those of the control side at W6, despite the
In affected NR, a significant improvement was observed significant decrease in the former at W6 compared to W0
for CSA values both at W2 and W6 compared to the measurements.

Table 2  Intra-group comparison W0 W2 p (W2–W0) W6 p (W6–W0)


of W0, W2, and W6 values
VAS 7.07 ± 1.36 5.00 ± 1.34 < 0.001 2.59 ± 1.24 < 0.001
mNDI 36.02 ± 15.66 24.11 ± 11.07 < 0.001 14.21 ± 7.20 < 0.001
SF-12
 PCS 37.63 ± 6.22 42.31 ± 4.82 < 0.001 47.83 ± 3.67 < 0.001
 MCS 32.67 ± 6.13 38.18 ± 5.10 0.003 44.56 ± 4.00 < 0.001

Mean ± SD
W0 week 0 (pre-treatment), W2 week 2 (immediately after treatment), W6 week 6, VAS Visual Analog
Scale, mNDI Modified Neck Disability Index, SF-12 short-form 12, PCS physical component score, MCS
mental component score

Table 3  Comparison of W0, Nerve roots W0 W2 W6 p (W2–W0) p (W6–W0)


W2, and W6 values of affected
and unaffected nerve CSA Affected C5 (n = 18) 8.83 ± 0.99 7.67 ± 0.97 6.94 ± 1.06 < 0.001 < 0.001
­(mm2) values
Unaffected C5 (n = 18) 5.78 ± 0.73 5.67 ± 0.97 5.67 ± 0.97 0.430 0.430
p < 0.001 < 0.001 0.002
Affected C6 (n = 17) 14.18 ± 2.40 12.94 ± 2.25 11.12 ± 1.90 < 0.001 < 0.001
Unaffected C6 (n = 17) 9.88 ± 1.27 9.76 ± 1.48 9.76 ± 1.48 0.163 0.163
p < 0.001 < 0.001 0.005
Affected C7 (n = 7) 14.00 ± 2.38 12.57 ± 2.07 11.71 ± 1.70 0.003 0.002
Unaffected C7 (n = 7) 10.57 ± 1.51 10.29 ± 1.80 10.14 ± 1.68 0.172 0.078
p 0.008 0.015 0.033

Mean ± SD
W0 week 0 (pre-treatment), W2 week 2 (immediately after treatment), W6 week 6, CSA cross-sectional area

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Journal of Medical Ultrasonics

Fig. 4  Correlation analysis of symptom duration and CSA values of the affected NR. a Correlation of C5 roots, b correlation of C6 roots, and c
correlation of C7 roots

CR is characterized by inflammation of the dorsal or used the continuous mode in our study to treat chronic CR
ventral NR in the proximal segment of the intervertebral in accordance with the latter suggestion.
foramen [1]. Disk herniation is known to be the most fre- In one of the few studies [16, 17, 31, 32] investigating
quent etiologic factor in CR [21]. the efficiency of therapeutic US in chronic neck pain, Reda
In entrapment neuropathies, external compression on a et al. compared the effects of continuous US therapy applied
peripheral nerve causes impairment of the internal neural at 1 MHz with an intensity of 1.0 W/cm2 for 5 min and
structure [22]. In cases where herniation accompanies the for a total of eight sessions versus static stretch (SS) of the
neuropathic process, degeneration of the axons and the upper fibers of the trapezius (UT) in patients with chronic
myelin sheath and derangement of venous flow result in mechanical neck pain and obtained similar improvement in
increased intraneural interstitial pressure and reversible both treatment groups [31]. Celik et al. compared the effects
intraneural edema. Compression of the NR for longer peri- of US alone, US + TENS, and sham US + TENS in 71
ods has been reported to gradually decrease intraneural patients with acute non-specific neck pain who were ran-
blood flow and lead to chronic edema and fibrosis in the domized into three groups and concluded that therapeutic
NR [23–26]. US was effective in reducing the pain and sensitivity level
HRUS has been used in several studies to detect struc- of painful points on the cervical region and improving the
tural changes in neural tissue [6, 7]. Using HRUS measure- functional status by increasing the cervical range of motion.
ments, Kim et al. found that the CSA values were signifi- They also reported that continuous application was observed
cantly higher in the affected NR than in the control side to be more effective for functional recovery [32]. However,
in patients with herniated neuropathy at C5, C6, and C7 there have been a number of studies that do not corroborate
[6]. In another study performed with a larger number of the above results [16, 17]. Costello et al. failed to obtain
CR patients and also healthy volunteers, Takeuchi et al. improvement in 23 patients with neck and arm pain and
observed that the CRA values were higher in the affected neural mechanical sensitivity with a single session of pulse
NR than both in the unaffected side of the patients and the US treatment at a dose of 0.5 W/cm2, sonication time of
volunteers based on HRUS measurements [7]. 50%, and frequency of 1 MHz [16]. However, much of the
Therapeutic US has often been used for treatment of research that has demonstrated significant clinical benefit
various muscular conditions because of its beneficial ther- has employed treatments at regular and relatively frequent
mal effects on the affected tissue [27]. It has been shown intervals [30]. In another randomized clinical study, continu-
in previous studies [14, 15, 28] that mild heating of mus- ous US at 0.5 W/cm2 for 15 sessions in addition to exercise
cle accelerates the metabolic rate, and moderate heating and TENS was not found to be significantly superior to sham
reduces muscle spasms, pain, and chronic inflammation US plus exercise and TENS in 100 patients with neck pain
and increases blood flow. The pulse mode has been sug- [17]. However, it is possible to speculate at this point that the
gested to be more effective during acute inflammation failure to observe beneficial effects of the therapeutic effects
because of its positive effect on macrophage activity and of US in the latter studies may have been due to the rela-
angiogenesis [29]. Since the pulse mode does not have a tively low US dose based on the suggestion of Draper et al.
substantial effect on angiogenesis beyond the acute stage that the dose of 0.5 W/cm2 is not sufficient to elicit substan-
[29], the continuous mode has been suggested to better tial thermal effects of US [33]. We observed improvement
provide a heating effect during the chronic stage [30]. We in pain, disability, and quality of life, and also a significant

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Journal of Medical Ultrasonics

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