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July2013 Vol.50 Issue:      3 (Supp.) Table of Contents
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Assessment of Therapeutic Effects of Repetitive Transcranial Magnetic Stimulation in Radiculopathic Pain

Hala R. El-Habashy1, Ahmed M. Abou Mousa2, Neveen M. El-Fayoumy1,

Husam S. Mourad2, Mostafa M. El-Kholy3

Departments of Clinical Neurophysiology1, Neurology2, Cairo University;

Clinical Neurophysiology3, Beni Suef University; Egypt



ABSTRACT

Background: Cervical radiculopathy (CR) is largely a clinical diagnosis and cortical stimulation has emerged as an effective and promising modality in the investigation of novel approaches for pain relief. Objective: The aim of this work is to investigate whether high and low frequencies of repetitive transcranial magnetic stimulation (rTMS) have a pain relieving effect in patients with radicular pain assessed by different pain scales and if these effects are prolonged or only short lasting. Subjects and Methods: This study was carried out on 20 patients, 10 received 20 hertz rTMS protocol and the others received 1hertz rTMS protocol. Pain scales: visual analogue scale(VAS), brief pain inventory (BPI): pain severity score(PSS) and pain interference score (PIS) used to assess the clinical efficacy of rTMS sessions on pain. Results: There was a highly statistically significant reduction of pain scores (VAS, PSS, PIS) after treatment compared to before treatment (p<0.01). In spite of that the pain scores increased 4 weeks after the last treatment session, these scores were still significantly less than those before treatment in both groups. Conclusion: rTMS can be used as a noninvasive therapeutic test for patients with drug-resistant chronic pain with more reduction of pain scales ratings in the high frequency group. [Egypt J Neurol Psychiat Neurosurg.  2013; 50(3): 227-234]

 

Key Words: repetitive transcranial magnetic stimulation(rTMS) – pain scales –  radicular pain – cervical radiculopathy.

Correspondence to Hala R. ElHabashy, Department of Clinical Neurophysiology, Cairo University, Egypt. Tel.: +201002330040   E-mail: hala.elhabashy@hotmail.com





INTRODUCTION

 

Cervical radiculopathy (CR) is largely a clinical diagnosis1 and refers to any disease process that causes the impairment of cervical nerve roots; its hallmark clinical manifestations are pain in the neck and an upper extremity associated with abnormal neurologic findings such as sensory loss, motor loss or diminished reflex in a corresponding nerve root.2

The incidence of cervical radiculopathy is estimated to be approximately 85 per 100 000 people, with a higher rate in men than women (107.3 per 100 000 versus 63.4 per 100 000, respectively) and peak incidence in the sixth decade of life in both sexes.3

Treatment of chronic pain in particular that associated with damage to the nervous system is difficult and there is no such thing as a miraculous cure for neuropathic pain. Pharmacological treatment has been the major choice in neuropathic pain but is not doing particularly well. For example, using existing pharmacological treatments for these neurogenic conditions, less than 1/3 of patients obtain a pain relief that is better than moderate.4

Cortical stimulation has emerged as an interesting, effective and promising modality in the investigation of novel approaches for pain relief. Cortical stimulation is based on the delivery of electric current to the motor cortex of the brain.5

 

One such procedure is repetitive transcranial magnetic stimulation (rTMS) which is a safe non-invasive technique for stimulating the cerebral cortex based on focal electromagnetic induction and was introduced in 1985.6

 

Repetitive transcranial magnetic stimulation is a painless technique that can interfere with neural functions related to a target cortical area with high temporal accuracy.7a,7b

 

Aim of Work

Aim of the work is to investigate whether high and low frequencies of repetitive transcranial magnetic stimulation (rTMS) have a pain relieving effect in patients with radicular pain assessed by different pain scales and if these effects are prolonged or only short lasting.

 

 

PATIENTS AND METHODS

 

This is a non-randomized controlled clinical trial to investigate the pain relieving effect of repetitive transcranial magnetic stimulation (rTMS) in patients with cervical radicular pain.

This study was carried out on 20 patients comprising 13 females and 7 males with cervical radicular pain affecting predominantly or exclusively one upper limb. They were recruited from Neurology, Rheumatology and Orthopedic Outpatient Departments (OPDs) of Kasr El Aini University Hospitals. Their ages were ranging from 17 to 62 years. The study took place in the period from January 2012 to May 2012 in the Clinical Neurophysiology Unit in Kasr El-Aini University Hospitals.

Inclusion criteria were patients with radicular upper limb pain caused by cervical radiculopathy as diagnosed clinically and with magnetic resonance imaging (MRI) or electrophysiological tests (Electromyography "EMG" and Nerve Conduction Studies "NCS").

Exclusion criteria were patients with pacemaker, previous skull opening, presence of metallic foreign body,  pregnancy.

 

All patients underwent:

1.      Clinical assessment to establish clinical diagnosis of cervical radiculopathy including:

a.      Thorough clinical history taking with special emphasis on:

·          Complete analysis of pain: with special stress on site, severity, radiation, aggravating and relieving factors.

·          Effect of pain on mood, work, daily activities, walking, sleep.

·          Associated symptoms: parasthesia, tingling, numbness, weakness.

·          Intake of analgesics and their effects.

b.      Neurological examination with special emphasis on sensory examination, assessment of power and reflexes, neck examination.

2.      Radiological assessment: MRI findings were used to support the clinical diagnosis of cervical radiculopathy.

3.            Neurophysiological assessment:

-        NCS: median and ulnar nerves, sensorimotor fibers.

-        F wave studies: recorded after stimulation of median and ulnar nerves.

-        EMG Examination: Electrodiagnosis of radiculopathy is based on needle EMG which shows abnormalities (denervation potentials, motor unit action potential (MUAP) abnormalities or reduced recruitment pattern) in a myotomal pattern of affected nerve roots.

 

All participants received repetitive transcranial magnetic stimulation (rTMS) as follows:

(A)   Repetitive Transcranial Magnetic Stimulation (rTMS) therapeutic sessions:

The patients were divided into two groups: (A) and (B).

In group (A), the patients were 10 and received four sessions of high-frequency (20 Hz) rTMS protocol on alternative days.

         In group (B), the patients were 10 and received four sessions of low-frequency (1 Hz) rTMS protocol on alternative days.

 

Stimulation protocols were as follows:

The rTMS parameters were similar to those used in the previous studies reporting clinical effects of rTMS in chronic focal pain.8a, 7a,7b

       Group A: High-frequency rTMS: Fifteen rTMS trains of 100 stimuli at 20 Hz frequency and at 73% of motor threshold (train duration: 5 seconds) separated by a 25-second pause were delivered for a total of 1500 pulses in each session.

       Group B: Low-frequency rTMS: One train of 1500 pulses at stimulation frequency of 1 Hz and intensity of 80% of motor threshold was applied in each session.

 

A MagStim Rapid magnetic stimulator (Magstim Company, Whitland, Wales, UK), connected with a figure-of-eight coil with a diameter of 70 mm, was used to deliver rTMS over the scalp site of identified motor cortical area corresponding to the hand of the painful side. In general, it approximates to the sites of C3 or C4 of the international 10-20 system.

The position of the coil was systematically adjusted at the beginning of each session to find the optimal scalp position ("motor hot spot").Using a figure-of-eight coil, this procedure allows one to stimulate selectively the hand area of the chosen hemisphere. The figure-of-eight coil was applied tangentially to the subject's head surface, with the handle pointing posteriorly and positioned at 45° with respect to midsagittal axis of the head.

 

Determination of the motor threshold:

The motor threshold (MT) was determined before the first session, using single-pulse stimulation over the primary motor cortex. Motor evoked potentials were recorded from the hypothenar muscles of the painful side, using a standard EMG machine and surface electrodes.

The MT was defined as the lowest intensity required eliciting a motor evoked potential in 50% of successive trials.

(B)          Pain Scales:

For each patient, the following pain scales were used to assess the clinical efficacy of the rTMS sessions on pain:

a.      Visual analogue Scale (VAS):  a single question that measures the degree of pain between (0: no pain) and (10: very severe pain).

This was taken before the first session, after each session, after end of sessions and one month later.

b.      Brief Pain Inventory (BPI) : It is formed of two parts:

1.      Pain Severity Score (PSS): measure the average degree of pain.

This was taken before the first session, after the last session and one month later.

2.      Pain Interference Score (PIS):  (from 0: does not interfere, to 10: complete interference) was used to measure the impact of pain on general activity, mood, walking ability, normal work, relations with other people, sleep and enjoyment of life.

This was taken before the first session, after the last session and one month later.

 

Statistical Methods Used

All data were expressed as mean and S.D. Descriptive statistics for parametric data and frequency Tables for categorical data. T-Test was used for comparison of parametric data between two groups.

Non-parametric Kruskal-Wallis test in more than 2 group comparison: It is a test of equality of medians rather than means, it is based on a rank order of the observations then it tests whether one variable tends to have values higher than the others.

Pearson correlation coefficients was used when examining the strength between two parametric values.

All tests have been performed using SPSS 11. P value of 0.05 or less considered significant.

 

RESULTS

 

The age of patients  ranged from 17 to 62 years with a mean age 39.5±12.2, regarding the sex distribution this study included 13 females(65%) and 7 males (35%).

All  patients were right handed. Their complaint was neck pain radiating to the left upper limb (shoulder, arm or the whole limb) in 11 patients, to the right upper limb in 4 patients and to both arms (with a predominant one side) in 5 patients.

The duration of their pain ranged from one month to about 6 years (more than one year in 12 patients, between 3-6 months in 2 patients and less than 3 months in 6 patients).

Their pain was precipitated by neck motion, making effort or lifting objects and partially relieved by lying down, wearing a neck collar or physiotherapy.

Most of the patients had -in addition to the pain- parasthesia, headache or neck spasm.

Most of our patients were having different analgesics, anti-inflammatory, muscle relaxants, anti-rheumatic, antiepileptic, antidepressant and corticosteroids with a resulting only temporary and partial improvement or no improvement at all.

As regarding Neurological examination, only one patient had mild C5/6 weakness and another one had hyposthesia in C5/6 distribution.

 

Radiological Assessment:

Results of cervical spine MRI studies showed the following:

·                  Straightened cervical curvature.

·                  Cervical spondylodegenerative changes.

·          Variable multi-levels (C4/5, C5/6, C6/7) disc herniation (posterior or posterolateral) and compressing exit foramina.

·          Formation of marginal bony osteophyte complex.

 

Neurophysiological Assessment:

Patients performed EMG and NCS of upper limbs and showed:

a-                Nerve Conduction Studies:

The median and ulnar nerves showed normal sensory and motor conduction studies (latencies, conduction velocities and amplitudes of the motor and sensory responses).

b-                F-wave Studies:

They showed normal ulnar, median F-wave latency and persistence.

c-                EMG Examination:

It showed some MUAP abnormalities (broad and highly polyphasic) and reduced recruitment pattern in variable myotomal distribution (four patients at C5/6/7 level and one patient at C8/T1 level).

 

 I.            Comparative Results:

There was no statistically significant difference observed between the high and low frequency groups before treatment as regards age and pain scales (VAS, PSS, PIS) P>0.05, (Table 1). Regarding pain scales before and after treatment for group A, there was a highly statistically significant reduction of pain scores (VAS, PSS, PIS) after treatment compared to before treatment p≤0.01. In spite of that the pain scores increased 4 weeks after the last treatment session, these scores were still significantly less than those before treatment. Regarding group B, There was a statistically significant and highly statistically significant reduction of pain scores after treatment compared to before treatment p≤0.05, p≤0.01, we also found that the pain scores increased 4 weeks after the last treatment session, however these scores were still significantly less than those before treatment as in group A (Table 3).

There was a highly statistically significant gradual reduction of the pain score (VAS) after each of the four session of rTMS, p≤0.01 (Table 4).

 

II.           Correlative Results:

There was a very highly statistically significant positive correlation between different pain scales, p<0.001 (Table 5).

 


 

Table 1. Comparison of age and pain scales between the two groups before treatment.

 

Age, pain scales

Group

Mean

Std. Deviation

P-value

Age

A

36.30

10.40

0.24

B

42.80

13.50

VAS  Before Treatment

A

6.00

2.36

0.64

B

5.50

2.37

PSS  Before Treatment

A

5.60

2.21

0.90

B

5.70

2.32

PIS  Before Treatment

A

5.01

2.18

0.67

B

4.54

2.60

 

 

Table 2. Comparison between the pain scales before and after treatment for group A.

 

Pain Scales

Mean ± Std. Deviation

P-value

VAS  Before Treatment

6±2.36

0.008**

VAS  After Treatment

2.9±2.6

PSS  Before Treatment

5.6±2.12

0.005**

PSS  After Treatment

2.92±2.5

PIS  Before Treatment

5±2.18

0.01**

PIS  After Treatment

2.87±2.21

VAS  Before Treatment

6±2.36

0.01**

VAS  4 weeks later

3.65±2.91

PSS  Before Treatment

5.6±2.12

0.008**

PSS  4 weeks later

3.51±2.69

PIS  Before Treatment

5±2.18

0.05*

PIS  4 weeks later

3.5±2.32

* Significant at  p≤ 0.05     ** Significant at  p≤0.01

 

Table 3. Comparison between the pain scales before and after treatment for group B.

 

Pain Scales

Mean ± Std. Deviation

P-value

VAS  Before Treatment

5.50±2.37

0.011*

VAS  After Treatment

3.05±2.65

PSS  Before Treatment

5.72±2.32

0.029*

PSS  After Treatment

3.22±2.40

PIS  Before Treatment

4.54±2.60

0.004**

PIS  After Treatment

2.81±2.79

VAS  Before Treatment

5.50±2.36

0.015*

VAS  4 weeks later

3.70±2.63

PSS  Before Treatment

5.72±2.31

0.047*

PSS  4 weeks later

3.67±2.41

PIS  Before Treatment

4.54±2.60

0.001**

PIS  4 weeks later

3.38±2.85

* Significant at  p≤ 0.05     ** Significant at  p≤0.01

 

Table 4. Comparison between the VAS scores before, after each session of rTMS and 4 weeks later for both Groups.

 

Group

VAS

Mean Rank

P-value

(A)

  Before

5.75

0.001**

 After the 1st session

4.65

After the 2nd   session

3.50

After the 3rd   session

2.30

After the 4th  session

1.60

4 weeks  later

3.20

(B)

  Before

5.75

0.001**

 After the 1st session

4.25

After the 2nd  session

3.25

After the 3rd  session

2.30

After the 4th  session

1.90

4 weeks later

3.55

*Significant at  p≤ 0.05     **Significant at  p≤0.01

 

Table 5. Correlation between different pain scales after treatment for both groups.

 

VAS After Treatment   

PSS After Treatment

PIS After Treatment

r

P

r

P

(A)               

0.996

0.00***

0.730

0.01*

(B)               

0.977

0.00***

0.926

0.00*

VAS 4 weeks After Treatment   

PSS 4 weeks After Treatment

PIS 4 weeks After Treatment

r

P

r

P

(A)               

0.988

0.00***

0.823

0.00*

(B)               

0.964

0.00***

0.908

0.00*

(C)               

 

 

 

 

* Significant at  p≤0.01

 

 


DISCUSSION

 

In this study, We found a highly statistically significant reduction of all pain scales ratings immediately after the end of the sessions in both groups compared to the basal ratings and despite these ratings showed some increase 4 weeks after the end of the sessions, however they did not return to the basal ratings and  were still significantly lower than the basal ratings. We also found a statistically significant gradual reduction of the VAS ratings after each of the four sessions indicating the immediate analgesic effects of the rTMS sessions and augmentation of these effects by repeated sessions.

Our results regarding the pain relieving effects of rTMS were supported by several studies that have tested and showed that sessions of noninvasive brain stimulation using the technique of rTMS could also relieve chronic neuropathic pain at least transiently.9b,10

However, others found the effect to be small and not significant versus placebo.11,12

Since the physiological effects of rTMS depend heavily on stimulation parameters such as frequency, train duration and inter-train intervals that were not equally applied in these reports, inconsistent results may have arisen from methodological differences in experimental protocols. In particular, stimulation frequency, which ranged from 0.2 to 20 Hz in previous studies, may have heavily influenced rTMS effects, as pulse rates of 1 Hz or less are considered to produce cortical inhibition, while rates around 20 Hz induce facilitation of cortical motor networks.13

Differences in the timing of pain evaluation, which ranged from a few minutes after rTMS14,15a,b to several days after the session9a,b, and the absence of double-blind active vs sham (placebo) stimulation may have also contributed to the results changeability.

Despite the pain scales ratings in the high frequency group were reduced more than those in the low frequency group, yet this difference did not reach  statistically significant values.

Some studies showed that the low frequency stimulation was effective in pain such as Tsubokawa  et al. 16 who showed that low-frequency rTMS (1 Hz) delivered over M1 of normal subjects decreased C fiber-mediated pain produced by intradermal capsaicin application  and Canavero et al.17 also applied rTMS pulses at 0.2 Hz in a series of patients with chronic pain secondary to stroke or spinal cord lesion, among the nine patients enrolled in this placebo-controlled study, one patient was relieved from allodynia and four patients from both spontaneous pain and allodynia.

However, most studies have been performed at higher frequencies. In a controlled trial, Lefaucheur et al.9b demonstrated that rTMS was able to relieve neuropathic pain when administered over M1 at 10 Hz but not at 0.5 Hz A second group showed that rTMS provided better alleviation of pain at 20 Hz than at 1 Hz.8 A third group found that 10-Hz rTMS was more efficacious than 5-Hz rTMS, whereas 1-Hz rTMS did not produce significant effects.19

As low and high frequencies have opposite effects on cortical excitability, the mechanisms of pain relief induced by the application of rTMS to the motor cortex  are unclear.20

Concerning rTMS, M1 stimulation at high frequency was shown to reduce pain scores by 20% to 45% after active stimulation and by less than 10% after sham stimulation. Regarding individual results, 35% to 60% of the published patients have been considered as good responders to rTMS (more than 30% pain relief after active rTMS).21

This is matched with our results that showed reduction of  pain scores by about 40-50%.

Significant reductions in ratings of pain have been reported following single sessions of high frequency rTMS to the motor cortex with the effects lasting from minutes up to 8 days. 8a,9a,b,11,14,22-25

This is consistent with our finding of significant reduction of VAS score which was taken 24-48 hours after the first rTMS session.

Longer-term effects on pain relief from multiple sessions of rTMS have also been demonstrated in single case studies26,8b and in larger groups of chronic pain patients.10

This is also consistent with our results showing the gradual and increasing improvement of pain as reflected by the gradual significant decline in pain scales ratings after each session that reached its maximal improvement after the last session.

The study of Khedr et al.10 showed that rTMS at 20 Hz given every day for five days can reduce pain ratings in patients with trigeminal neuralgia and post-stroke pain for at least two weeks after the end of treatment and concluded that repeated sessions of rTMS over the motor cortex may be, at least in some groups of patients, an effective way of providing  relatively lasting relief of painful symptoms.

We also found that the reduction of pain scales ratings were prolonged and lasted at least 3-4 weeks, However showing minimal increase compared  to those taken immediately after the last session but were still significantly lower than the basal ratings before treartment.

In addition, Johnson et al.  demonstrated that a single session of rTMS can alter sensory thresholds in individuals suffering from chronic pain. Cold was first detected and then became painful. Furthermore, rTMS significantly increased the temperature at which the application of heat became painful. The threshold changes following rTMS appear to be real effects, as the administration of sham TMS failed to produce any significant threshold alterations.26

Other studies have pointed also to changes of brain opioid receptor availability in neuropathic pain, and their possible modulation by motor cortex stimulation27,28, and such mechanisms might be also relevant in case of rTMS.

Among the hypothesis adduced for rTMS effects, long-term potentiation (LTP) and depression (LTD), have been suggested as possible mechanisms of rTMS.29 However, modulation of synaptic connections by electrical cortical stimulation needs repeated sessions of high frequency stimulation. Daily rTMS sessions over several days have been recently proposed to enhance the analgesic effects of rTMS10, which may be in accordance with a LTP mechanism.

Thus, non-invasive transcranial cortical stimulation requires some substantial improvements in therapeutic strategies for chronic pain before being considered as a therapeutic technique in chronic pain in the future.

Several parameters of stimulation have been quite satisfactorily determined, such as the frequency of stimulation, which parallels analgesic efficacy (better for 10–20 Hz than for lower frequencies)18,19, the number of pulses, which needs to be high, at least 1200 per session and repeating the sessions for several days or weeks to enhance and prolong rTMS-induced analgesia10 and the use of a figure-of-eight coil, which is mandatory because non-focal coils lead to non-significant results.11

 

In conclusion, motor cortex rTMS effects on chronic pain are quite low or modest (pain relief ranged between 40% and 50%) and short-lasting on clinical grounds and there are immediate analgesic effects of the rTMS sessions and augmentation of these effects by repeated sessions, pain scales ratings in the high frequency group are reduced more than those in the low frequency group.

 

[Disclosure: Authors report no conflict of interest]

 

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الملخص العربي

 

تقييم التأثير العلاجى للتنبيه المغناطيسى المتكرر عبر المخ فى الألم الناتج عن اعتلال جذور الأعصاب

 

إن الألم الناتج عن اعتلال جذور الأعصاب يؤثر بشدة على راحة المريض ولا يوجد له علاج ناجع تماماً حتى الآن ولذا كانت أهمية تقديم بدائل جديدة لعلاجه. يساعد التنبيه المغناطيسى المتكرر عبر المخعلى إحداث تغييرات في إثارة القشرة المخية والتأثير على الوظائف العصبية عند موقع التحفيز وفي المواقع البعيدة، يؤدى إما إلى المنع أَو التسهيل اعتمادا على تردد النبض، وأنه وجد أن التنبيه المغناطيسى المتكرر عبر المخ لمركز الحركة بالمخ قد يساعد على علاج الآلام المزمنة الناتجة عن الأمراض العصبية.

تهدف هذه الدراسة لاستعراض إمكانية علاج الألم الناتج عن اعتلال جذور الأعصاب العنقية باستخدام التنبيه المغناطيسى المتكرر عبر المخ بالترددين السريع (20 نبضة فى الثانية) والبطئ (نبضة واحدة فى الثانية)، واستعراض ما إذا كانت هذه التأثيرات طويلة أم قصيرة المدى.

تم إجراء الدراسة على 20 مريض (تشمل 13 من الإناث و 7 من الذكور، وتتراوح أعمارهم بين 17 و 62 عام) يعانون من الألم الناتج عن اعتلال جذور الأعصاب العنقية بشكل خاص على أحد الطرفين العلويين، وهذا الألم غير مستجيب لوسائل العلاج الأخرى.

كل المشاركين أُخضعوا إلى قياسين إكلينيكيين لمستوى الألم ومدى تأثيره على الأنشطة اليومية المعتادة قبل بدء الجلسات العلاجية، ثم تم تقسيمهم بطريقة عشوائية إلى مجموعتين تلقت كلاهما 4 جلسات تنبيه مغناطيسى متكرر عبر المخعلى على مدى أسبوعين: الأولى (أ) باستخدام التردد السريع للنبضات (20 نبضة فى الثانية)، والثانية (ب) باستخدام التردد البطئ للنبضات (نبضة واحدة فى الثانية).

خضعت جميع الحالات لنفس القياسين السابقين عقب انتهاء الجلسات وبعد مرور شهر من نهاية العلاج.

أثبتت نتائجنا أن جلسات التنبيه المغناطيسى المتكرر عبر المخ للمنطقة القشرية بالمخ المسئولة عن حركة الذراع بكلا الترددين السريع والبطئ قد أدت إلى انخفاض مستوى الألم بشكل ملحوظ تتراوح بين 40-50% مقارنةً بما قبل جلسات العلاج، وقد لوحظ أن هذا التأثير يزداد تدريجياً بعد كل جلسة علاجية، كما لوحظ أن هذا التأثير قد تلاشى جزئيا عند قياس مستوى الألم بعد مرور شهر من جلسات العلاج، إلا أنه قد ظل بمعدل أقل منه قبل بدء العلاج.

 



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