|Year : 2019 | Volume
| Issue : 1 | Page : 67-73
Effect of transcranial magnetic stimulation in patients with Parkinson disease
Wafik M El-Shiekh1, Rasha A El-Kabbany1, Aktham I El-Emam1, Ibrahim E Al-Ahmar1, Mohamed A Eltantawi2
1 Department of Neuropsychiatry, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Neurology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
|Date of Submission||16-Apr-2017|
|Date of Acceptance||02-Jul-2017|
|Date of Web Publication||17-Apr-2019|
Mohamed A Eltantawi
Source of Support: None, Conflict of Interest: None
The aim was to study the possible effect of repetitive transcranial magnetic stimulation (rTMS) as a treatment option in patients with Parkinson disease (PD) whose conditions become complicated owing to either progression of the disease or adverse effects of the drugs.
PD is the second most common neurodegenerative disease. Drug-related motor complications, for example, dyskinesias, or nonmotor complications, for example, depression, happen in the later stages of the disease, even among those on levodopa therapy. Transcranial magnetic stimulation (TMS) has been used in a wide range of diseases associated with motor dysfunction. rTMS has shown good improvement of clinical condition among patients with PD.
Patients and methods
The study is a prospective case–controlled clinical trial. A total of 40 patients with PD were included in the study and divided into two groups: group I underwent active rTMS (20 patients) and group II underwent sham stimulation (20 patients).
Overall, 40 patients with complicated PD completed the study (group I included 20 patients and group II also had 20 patients). There was no statistically significant difference between the groups regarding age, sex, duration of illness, or stage of the disease (P > 0.05). After rTMS application, group I showed significant results regarding the stage of the disease (P < 0.05) and showed highly significant results regarding the severity of motor affection and complications (P < 0.001), whereas group II showed no significance (P > 0.05).
rTMS maybe a good addition to the management of motor symptoms and complications in complicated PD.
Keywords: dyskinesia, neurodegenerative disease, Parkinson disease, transcranial magnetic stimulation, unified Parkinson's rating scale
|How to cite this article:|
El-Shiekh WM, El-Kabbany RA, El-Emam AI, Al-Ahmar IE, Eltantawi MA. Effect of transcranial magnetic stimulation in patients with Parkinson disease. Menoufia Med J 2019;32:67-73
|How to cite this URL:|
El-Shiekh WM, El-Kabbany RA, El-Emam AI, Al-Ahmar IE, Eltantawi MA. Effect of transcranial magnetic stimulation in patients with Parkinson disease. Menoufia Med J [serial online] 2019 [cited 2020 Jul 15];32:67-73. Available from: http://www.mmj.eg.net/text.asp?2019/32/1/67/256094
| Introduction|| |
Parkinson's disease (PD) is the second most common neurodegenerative disease .
Egypt has one of the highest prevalence of PD in the world, with a prevalence rate of 557/100 000 .
The pathology of PD comprises many genetic, metabolic, environmental, and inflammatory causes, as well as oxidative stress . This complication leads to widespread dysfunction of the brain and particularly affects processing in the corticobasal ganglia loop.
With time, patients with PD develop complications. These may be owing to either drug-related motor complications, such as wearing off, dyskinesias, morning dystonia, and on–off fluctuations, or nonmotor complications, such as depression, dementias, postural instability, and repeated falls .
Transcranial magnetic stimulation (TMS) is a method of noninvasive neurostimulatory and neuromodulatory technique increasingly used in clinics and research laboratories worldwide. It can modulate cortical excitability for a transient or long period by using localized magnetic pulses .
Therapeutic TMS is used in different syndromes affecting the motor system such as movement disorders, stroke, amyotrophic lateral sclerosis, and multiple sclerosis, as well as in some patients with drug-resistant depression .
Pharmacological therapy for PD (e.g. levodopa) can improve the clinical condition in patients ,. Similarly, repetitive transcranial magnetic stimulation (rTMS) may show the same effect, reflecting clinical improvement. rTMS can also induce dopamine release from the basal ganglia. In healthy individuals, application of 10 Hz of rTMS over the primary motor area (M1)  or the dorsolateral prefrontal cortex  induced ipsilateral dopamine release from the putamen and caudate, respectively, as measured by raclopride binding.
rTMS as a therapeutic method in PD has proven results regarding motor symptoms through a low-intensity, high-frequency (5 Hz) rTMS over M1 .
In most cases, the hand motor area of the M1 contralateral to the most affected body side was the target for rTMS. Improvement outcome using rTMS ranged from 10 to 30%, whereas no improvement resulted after sham stimulation .
Depression is one of the important nonmotor symptoms leading to disability in PD . The use of rTMS in patients with PD with depression has gained much interest .
| Aim|| |
The aim was to study the possible therapeutic effect of rTMS in patients with PD who show complications owing to either progression of the disease or adverse effects of the drugs.
| Patients and Methods|| |
This study is a prospective case–controlled clinical trial. It was conducted from January 2015 to May 2016 on 40 patients with complicated PD; all patients fulfilled the UK Parkinson's disease brain bank criteria for PD. Patients were divided into two groups: group I included 20 patients with complicated PD who received active rTMS, 5 Hz bilaterally over the motor hand and leg areas of the cortex and group II comprised 20 patients with complicated PD who received sham rTMS as a control group, with no significant difference between both patient groups regarding severity and complications.
All patients included in the study were older than 50 years, with presence of at least two of the three cardinal signs (tremors, bradykinesia, and rigidity). They showed strong dramatic response to levodopa initially, and then the response started to wane with appearance of complications. These may be either motor complications, such as wearing off, dyskinesias, morning dystonia, and on–off fluctuations, or nonmotor complications, such as depression, dementias, postural instability, and repeated falls. Moreover, some of the patients may use other drugs such as dopamine agonists, monoamine oxidase B inhibitors, catechol-o-methyl transferase inhibitors, or anticholinergics.
No patients who developed complications suddenly or had a history of seizures, previous cerebral strokes, severe head trauma, antipsychotic drugs intake, deep brain stimulation, direct current stimulation, or electroconvulsive therapy were encountered. Also the exclusion criteria includes Parkinson associated with (multiple system atrophy, corticobasal degeneration, and progressive supranuclear palsy) and those with positive family history of Parkinsonism.
After approval was taken from the local ethical committee, the study was explained to each patient and informed written consent was taken from them. Proper history was taken of the general and neurological complaints. A full neurological examination was done with stress on the motor system. The unified Parkinson's disease rating scale (UPDRS) with the motor section was used for all patients.
During the session, the patients were seated comfortably in a reclining chair, and biphasic rTMS pulses were delivered through a circular coil (outer diameter = 14 cm; maximum field strength = 1.9 T) attached to MagPro R30 stimulator (Galaxy Medical Center, Inc. 6221 Wilshire Blvd. Suite 401 90048 Beverly Hills, USA).
TMS pulses were delivered through the coil, which is positioned perpendicular to the central sulcus line. The first (active) group received 5 Hz applied in 20 trains; each train is formed of 100 pulses, with 20 s intertrain interval. A total of 10 sessions were administered once per day for 10 successive days for each patient. The second (inactive/sham stimulation) group underwent sham stimulation. Both patient groups could not identify the difference between sham and active stimulations.
Data were analyzed using statistical package for the social sciences version 15 (SPSS; SPSS Inc., Chicago Illinois, USA). Qualitative data were presented as number and percentage. Comparison between groups was done by χ2-test. Quantitative data were presented as mean ± SD. Paired t-test was used for comparison within groups. Student's t-test was used to compare between the two groups.
| Results|| |
A total of 40 patients with complicated PD completed the study, and they were divided into two groups:
- Group I: 20 patients with complicated PD were subjected to active rTMS
- Group II: 20 patients with complicated PD were subjected to sham rTMS, being used as a control group.
Mean age of patients in group I and group II was 66.65 ± 4.58 years and 66.60 ± 5.97, respectively [Table 1]. There is no statistically significant difference between the two studied groups regarding the mean age (P = 0.976).
No statistically significant difference was found between the two studied groups regarding the mean sex (P = 0.342) and the duration of illness (P = 0.702). Moreover, there was no significant difference between both the groups regarding clinical staging before stimulation [Table 2] and [Table 3].
|Table 3: Comparison between complications in active and inactive groups before repetitive transcranial magnetic stimulation|
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UPDRS sections III and IV were used to assess the severity of motor affection and complications, respectively, for both groups, and there was no statistically significant difference between both the groups.
All patients completed the study. There was a highly significant result regarding staging of disease in group I, whereas there was no change in group II [Table 4] and [Table 5]. Moreover, there was a highly significant result regarding the severity of motor affection and complications after rTMS for group I [Table 6] whereas there was no significant difference in group II.
|Table 4: Stage of the disease in active and inactive groups after repetitive transcranial magnetic stimulation|
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|Table 5: Severity of motor affection and complications in active group before and after repetitive transcranial magnetic stimulation|
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|Table 6: Severity of motor affection and complications in active group after repetitive transcranial magnetic stimulation|
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| Discussion|| |
We studied the effect of active rTMS in 20 patients with complicated PD (group I) in comparison with 20 patients with PD, matched in each aspect, who underwent inactive stimulation (sham stimulation), as a control group (group II). Patients were diagnosed according to UK PD brain Bank criteria for idiopathic PD. Their ages ranged between 58 and 78 years. The age in group I (active rTMS group) ranged between 60 and 75 years, with mean age of 66.65 years. In group II (shame stimulation group), their age ranged between 58 and 78 years, with mean age of 66.60 years. Thus, there is no difference in age between both the groups (t = 0.030, P = 0.976).
The duration of illness in our patients ranged between 63 and 80 months, with complications observed in patients from either disease progression or cumulative adverse effects of the drugs; this result coincides with that obtained by Oertel et al. . The duration of disease in group I ranged between 65 and 80 months, with mean duration of 68.1 months, in comparison with group II, where the duration ranged between 63 and 80 months, with mean duration of 68.75 months. There is no significant difference between both the groups (P = 0.365).
Clinical staging of our patients is based on the classification criteria of Hoehn and Yahr scale. Group I included seven patients with stage 3, 10 patients with stage 4, and three patients with stage 5. In comparison, group II (control group) included nine patients with stage 3, nine patients with stage 4, and two patients with stage 5. No statistically significant difference was found regarding clinical staging before stimulation between both the groups.
Group I patients underwent active rTMS with a frequency of 5 HZ in 10 settings for 10 successive days, and this frequency is considered as fast rate stimulation according to theta burst stimulation . On the contrary, group II patients were blindly subjected to inactive stimulation (sham stimulation) without knowing the difference between active and inactive stimulation.
We used circular coil for stimulation. This made a diffuse effect in the nearby cortical areas. We stimulated primary motor areas (M1) bilaterally. Similarly, this site was stimulated by Khedr et al. .
Regarding frequency, we used 5 Hz, which coincides with Koch et al. . Others have used a frequency of 10 Hz . Moreover, others have used higher frequency (25 HZ). Khedr et al.  and Chung et al.  in their meta-analysis found no significant effects between different frequencies within the theta range.
Regarding the number of sessions, we applied 10 sessions, whereas authors such as Shirota et al. , Arias et al.  and Benninger et al.  have applied seven sessions. This is in contrast to Bornke et al.  and Koch et al.  who applied single sessions. Patients were evaluated clinically for the effect of rTMS within the same group before and after stimulation. Another comparison was made between both the groups, that is, between group I and group II before and after stimulation.
At the start of the study, patients in group I were matched in every aspect to those in group II. There was no significant difference in age, sex, duration of the disease, and clinical staging of the disease. UPDRS – motor part (UPDRS section III) was used as the best method for clinical evaluation according to Chou et al.  and Zanjani et al. . There was no significant difference regarding speech, facial expression, tremors, action or positional tremors, rigidity, finger taps, and hand movement. Moreover, there was no significant difference between both groups in other movement parameters including rapid alternating movements, foot agility, arising from chair, posture, gait, postural stability, body bradykinesia, and hypokinesia. At the start of the study, there was no significant difference between both groups regarding complications. Different items of dyskinesias (duration, disability, painful dyskinesia, and early morning dystonia) were similar with no statistical difference. Clinical fluctuations, either sudden off or proportion of sudden off to walking day, also showed no difference. Anorexia, nausea, vomiting, and sleep disturbance also showed no difference. The same was found in relation to symptomatic orthostasis. There was no significant change regarding freezing and falling.
At the end of the study, there was improvement in group I staging as nine patients improved to stage 2, where balance was regained (no patients fulfilled this criterion at the start of the study), and three patients in stage 5, as the most severe stage, where patients were chair bound or bedridden, improved partially to stage 4 and became able to walk unassisted with difficulty. On the contrary, group 2 (sham stimulation) did not show any change in the stage of the disease.
We used the motor part (group III) of UPDRS for clinical evaluation and follow-up of our patients for both group I (active rTMS) and group II (sham stimulation). There was no change in group II at the end of the study (sham stimulation), where there was no active stimulation, and this excludes the possibility of placebo effect.
In group I, there was a significant improvement in speech (P = 0.010), and facial expression also showed marked improvement (P = 0.003). Follow-up of our patients regarding tremors also showed considerable improvement in group I (P = 0.034). Action or positional tremors also showed marked improvement (P = 0.043). Rigidity improved markedly with rTMS (P = 0.008) along with finger taps (P = 0.002), hand movement (P = 0.010), and rapid alternating movement of hands (P = 0.013).
Foot agility also showed considerable improvement (P = 0.005). Arising from chair also improved (P = 0.018). Following posture in our patients, at the start of the study, 10 patients showed marked flexion with extreme abnormality of posture (stage 4), and seven of them improved at the end of the study, whereas three showed no improvement. Moreover, seven patients with severely stooped posture with kyphosis that can be moderately leaning to one side (stage 3) improved to moderate stooped posture (stage 2). However, no patients showed normal erect or slightly stooped posture (stages 0 and I) (P = 0.011).
Gait assessment showed less significant results (P = 0.222) where only one patient from stage 4 (chair bound patients that cannot walk at all) could walk with mild assistance. However, seven patients from stage 3 with severe disturbance of gait but walk with assistance improved to walking without assistance (stage 2), and only one patient walked slowly with short steps, with no festination or propulsion (stage 1). Postural stability did not improve (P = 0.104). Body bradykinesia showed good improvement (P = 0.005).
In contrast, in group II, there were no statistically significant results.
Regarding the effect of rTMS on complications, patients in group I did not show much improvement regarding dyskinesia duration (P = 0.246), disability (P = 0.45), and early morning dystonia (P = 0.059) at the end of the study, whereas they showed improvement regarding painful dyskinesia (P = 0.046).
Clinical fluctuations as a common complication of anti-Parkinsonian treatment were evaluated. Sudden offs improved in group I (P = 0.009) as well as gastrointestinal complications such as anorexia, nausea, and vomiting (P = 0.008). Other complications showed less significant results, such as sleep disturbance (P = 0.560), symptomatic orthostasis (P = 0.206), freezing (P = 0.241), and falling (P = 0.435). Group II showed no improvement regarding complications.
This coincides with the results of previous investigators in this field who found mild to moderate improvement in their study. In an interesting study, Fregni et al.  published a systematic review and meta-analysis of the literature to quantify the efficacy of rTMS in the treatment motor dysfunction in patients with PD. Only 12 studies were found in the literature up to this date to fulfill the inclusion criteria for this study. They used the motor subscale of UPDRS. They found out that rTMS can be beneficial for motor symptoms of PD.
Khedr et al.  studied the effect of rapid rTMS (frequency: 25 Hz) bilaterally on the motor areas and leg area of the brain. Patients received 6 successive sessions every day (3000 pulses for each session), and three booster sessions (on 3 consecutive days) of rTMS. After 1, 2, and 3 months, UPDRS among others was measured before and after rTMS session. They found improvement of all parameters.
Most recently, Chung and Mak  carried out a systematic review and meta-analysis about the effect of rTMS on physical functions and motor signs in PD. Their target was to examine the effectiveness of rTMS over the short and long term in PD. This was measured by the motor section of UPDRS section III. Their second subjective was to investigate whether rTMS parameters (intensity, frequency, stimulation site and total number of stimulation pulses) were associated with the effect size of rTMS on motor performance. A total of 498 patients with PD in 22 trials were included in the meta-analysis, which compared between the short-term and long-term changes by using either real and sham rTMS ,,,,,,. The results of the meta-analysis revealed that the effect magnitude was statistically significant in favor of the intervention. They also found that when stimulation site in M1 (primary motor area), the effect is better than stimulation of supplementary motor area and dorsolateral prefrontal cortex, and this coincides with our study that stimulated primary motor area (M1) bilaterally.
The rTMS long-term effect on UPDRS scores was apparent after real TMS ,,,,,. The total number of stimulation pulses in these trials ranged from 600 to 20 000 (mean: 6251.4 ± 8586.4) delivered over 1–10 sessions. This also coincides with our study as we used rTMS for 10 days (the first active group received 5 Hz applied in 20 trains; each train is formed of 100 pulses, with 20 s intertrain interval). For UPDRS III scores at long term, bigger effect was accompanied with more pulses number.
rTMS improved walking speed and hypokinesia in PD after three daily high-frequency rTMS sessions, and this coincides with our results as hypokinesia improved. Akinetic gait (i.e., small step amplitude with decreased speed) is one of the most important complications in PD , and the results of Hausdorff et al.  showed that rTMS improved walking speed in individuals with PD.
rTMS resulted in good improvement in UPDRS III score in group 1 that received active stimulation. The UPDRS III is an accurate scale to assess the motor function in patients with PD, and also it reflects the severity of the disease and quality of life .
Our findings showed that rTMS resulted in considerable improvement of UPDRS III score. The extent of the effect of UPDRS III scores found in our study is larger than previous reviews ,. The difference may be because of several methodological differences, but it is mostly owing to the difference in stage of the disease.
The inclusion of different patient phenotypes in their studies may also confound the result. In the analyses of walking and upper limb function and long-term UPDRS III scores, most of the other trials applied excitatory or high-frequency rTMS over M1. In addition, a subgroup analysis for UPDRS III scores also shows that the effect of rTMS stimulation over M1 appears to be preferable to that over other areas .
| Conclusion|| |
Our finding shows the highly beneficial effects of rTMS on motor signs measured by UPDRS III in the long term. As our patients have complicated PD after lack of response, insufficient response, or complications from either drug or disease progression, it makes additional complimentary treatment a very important add-on to such patients. Most of earlier studies agree about the positive effect of RTMS in different stages of PD.
We recommend applying rTMS for complicated PD. Further studies are required to determine the optimal stimulation preferences (such as sessions number and total stimulation pulses) to compare different target sites regarding efficacy and to clarify how different patient phenotypes and disease stages affect the response to rTMS for the development of an efficacious therapeutic strategy.
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Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]