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July2011 Vol.48 Issue:      3 (Supp.) Table of Contents
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Effect of Deep Brain Stimulation on Motor and Mental Status of Parkinson’s Disease Patients: A Preliminary Egyptian Study

Ahmed Shakal1, Ehab Ramadan2, Waleed Fawaz2

 

Departments of Neurosurgery1, Neuropsychiatry2, Tanta University; Egypt

 



ABSTRACT

Background: Parkinson’s disease (PD) ranks second in prevalence of degenerative disease of the nervous system. Objective: Is to study the effect of deep brain stimulation (DBS) of the subthalamic nucleus (STN) in Parkinson's disease patients on motor and psychiatric profile including cognition and also its impact on quality of life. Methods: Fourteen patients with idiopathic Parkinson’s disease were carefully considered for bilateral STN DBS. Clinical and neuropsychological evaluation was performed preoperatively and 6-9 months postoperatively. Parkinson Disease questionnaire (PDQ-39) is used to assess parameters of quality of life. Results: A significant reduction in motor disability, equal to 50 % was found 6 months after surgery. No evidence of memory, reasoning or attention changes after surgery. Executive functions showed significant improvement regarding WCST performance. Significant improvement was found in mood but the state and trait anxiety did not show any significant change. Only significant paranoid traits appeared on one patient in the post-operative period. Significant correlation was found between mood state improvement and motor improvement. Regarding quality of life, there was significant improvement in the items of mobility, activity of daily living, emotional wellbeing, communication and bodily discomfort. Conclusion: Beside the marvelous motor effect, careful patient selection for STN DBS in Parkinson disease does not permit any deleterious effect on psychiatric and cognitive state of the patients. On the contrary, mood, quality of life and some cognitive functions may be better after surgery. [Egypt J Neurol Psychiat Neurosurg.  2011; 48(3): 257-264]

 

Key Words:  Parkinsonism, DBS, STN, cognitive function, quality of life

 

Correspondence to Ehab Ramadan, Department of Neuropsychiatry, Tanta University, Egypt

Tel.: +20127552626        Email: ehab_ramadan@yahoo.com





INTRODUCTION

 

Parkinson’s disease (PD) ranks second in prevalence of degenerative disease of the nervous system, after Alzheimer’s disease, and it is estimated that 0.3% of population is affected1. Especially in its initial stages, PD symptoms are mainly motor, later on cognitive dysfunctions and mood disorders appear. Although levodopa still is the cornerstone of PD treatment, its prolonged use is associated to motor and non-motor complications. Non-motor    complications include nausea,vomiting, orthostatic hypotension  sleepiness, hallucinations and delusions2. The precise effect of optimal PD treatment on life expectancy is unclear, but living with this chronic degenerative illness is thought to have a profound negative impact on quality of life due to both disease manifestations, and the adverse effects of medical and surgical management strategies3. As such, the public health burden of PD is significant and increasing, and ways of assessing the impact of therapeutic interventions on

 

quality of life are needed for optimal patient care and for allocation of scarce healthcare resources4. Treatment algorithms for PD include both pharmacological and surgical intervention. Before the introduction of Levodopa in 1967, surgical intervention was widely used and took different form of inducing lesions  until the Stereotaxy came up. With Stereotaxy, the lesions could be placed more accurately with better results5. Subsequent better understanding of the basal ganglia circuits and its malfunction in PD lead to the use of non-destructive surgical techniques such as high frequency deep brain stimulation and discovery of more effective surgical locations such as the subthalamic nucleus6. Deep brain stimulation (DBS) of subthalamic nucleus (STN) is hypothesized to reduce cognitive morbidity risk  compared to other areas like thalamic or Globus Pallidus deep brain stimulation7. The neuropsychological effects of DBS  of the STN in Parkinson's disease started to emerge and some results indicate the safety of the surgical procedure8 with relatively rare post surgical cognitive deterioration9,10. Nevertheless psychiatric and behavioral effects of this surgical procedure are still controversial. A wide range of complications were reported in the postoperative period including mild to severe depressive symptoms, apathy, mania, aggression and psychosis11,12. The majority of these complications appear to be transient  and not permanent8. There are a lot of studies focusing on the motor symptoms of DBS but few focused on the psychiatric aspects.

The aim of the present study is to assess cognition, mood,  personality and quality of life in Parkinson's disease patients submitted to STN deep brain stimulation.

 

SUBJECTS AND METHODS

 

Selection Criteria

Patients with idiopathic Parkinson’s disease were considered for bilateral DBS in the STN if they met the following inclusion criteria: Substantial disability due to frequent off period and presence of severe motor fluctuations and drug related dyskinesia despite optimization of antiparkinsonian  medications with significant improvement (at least 40-50%) of the Unified Parkinson Disease Rating Scale (UPDRS)13. Exclusion criteria include: prior neurosurgical procedure, dementia, unstable medical status, MRI evidence of cerebral atrophy or other CNS diseases and psychiatric complications that could affect patient capacity to give informed consent or to follow postoperative DBS device adjustment.

 

Patients

Preoperative and postoperative clinical examinations were performed at the Department of Neuropsychiatry, Tanta University Hospital. Table 1 show the demographic data for the 14 patients included in this study. They were 11 men and 3 woman. The mean age was 48.1 (SD12.5), the mean illness duration was 19.7 (SD 5.2). All patient were on Levodopa regimen  was  17.8 years (SD 1.2). The mean Hoehn and Yahr (1967) stage was 2.7 (SD 0.4) in the on phase and 4.2 (SD 1.3) in the off phase. All Participating patients gave informed consent and the study was approved by the hospital internal review board.


 

Table 1. Patients’ Characteristics.

 

Variable

Number

Mean (SD)

Range

n

14

.

.

Females

3

.

.

Males

11

.

.

Handedness

 

 

 

Right

14

.

.

Left

0

.

.

Age (years)

14

48.1 (12.5)

2968

Education (years)

14

14.5 (4.5)

3–20

Estimated premorbid IQ

14

117.4 (11.2)

87–128

Current WAIS-R VIQ

14

113.8 (12.1)

94–130

Duration of disease (years)

14

19.7 (5.2)

12–24

Severity of disease (H&Y)

 

 

 

    `Off' medication

14

4.2( 1.3)

2.5-5.0

    `On' medication

14

2.7(0.4)

2.5-3.0

Duration of L-dopa therapy

 

17.8(1.2)

13-21

Medication regime at baseline

(l-dopa equivalents in mg/day)

14

925.8 (400.1)

700–1500

MMSE

Before surgery

14

28.17(01.3)

24-28

 

After surgery

14

29.25(01.1)

25-29

H & Y =  Hoehn and Yahr Rating Scale14

 


Surgical Procedure

The STN-DBS procedures were performed at the Neurosurgery Department, Tanta University Hospital, Egypt. Nonstereotactic MR imaging was performed 2 to 3 days before surgery. Thin-slice axial (T1- and T2-weighted) were obtained using a 1.5-tesla MR scanner. Data acquisition was achieved without interslice spacing or interslice overlapping (2-mm slice thickness). Following overnight withdrawal from medication, the patient’s head was immobilized by placement in a modified Riechert–Mundinger stereotactic head ring under local anesthesia. A stereotactic contrast-enhanced cranial CT was performed using 2-mm slice thickness, no inter-slice spacing, and 2-mm table increments. The CT data were transferred through the hospital’s data network to a workstation located in the operating room (OR). After stereotactic registration, the cranial CT was basically used as a distortion-free reference system for MR images. The data obtained from MR images were integrated into the 3D stereotactic coordinate system by using landmark-based image fusion[15]. Briefly, a set of corresponding anatomical landmarks, which were clearly visible on both CT and MR images, was manually defined by the neurosurgeon on the computer screen. For each pair of points an algorithm, which is part of the treatment-planning software, was used to calculate particular correlation accuracy. Points with a difference exceeding 2 mm were rejected before image fusion. The fusion was accepted by the neurosurgeon if the mean deviation was below 1.2 mm. The course of characteristic anatomical contours (large intracranial vessels, ventricular walls, gyri, and/or sulci) at the CT/MR–image interfaces provided additional visual control for the validity of the fusion process (Fig. 1).


 

 

 

Figure 1. The MR image is overlaid as a square on the stereotactic CT scan at the level of the ventricles (Image Fusion). Left: The MR imaging-defined AC-PC on the CT scan. Right: STN is visualized on T2-weighted images within the stereotactic system.

 


Target Definition and Trajectory Control

Trephinations were defined with regard to the main axis of the STN referred to a line running perpendicular through the middle (MCP) of the AC–PC line. In the Schaltenbrand atlas  on the sagittal plane 12 mm lateral from the AC–PC line, the rostrocaudal angulation is approximately 70°. In the coronal section (3 mm posterior to the MCP) the lateromedial angulation is approximately 65°. The entry points were defined according to these angulations 2.5 to 3 cm rostral to the coronal suture and approximately 3.5 cm lateral to the midline of the skull. The prescribed target within the STN lay 2 to 3 mm behind the MCP, 3.7 mm below this point and 12 mm lateral from the midline of the third ventricle6,16. Additionally, the contour of the STN was outlined on the axial T2-weighted MR images, in which the STN was visible as a hypointense ovoid structure located lateral to the red nucleus. Because the ventral border of the STN was not always easy to delineate from the SN on the MR images, we used the largest horizontal diameter of the red nucleus as an indirect marker of the ventral third of the STN. This definition was in agreement with the topography of the STN as provided in the atlas published by Schaltenbrand and Wharen16. The tip of the electrode had to be positioned inside this area. To minimize operative risks, each trajectory was carefully controlled on MR images. Displays of the trajectories in various reconstruction planes provided slice by slice information on the position of the probe and surrounding structures so that the surgeon could avoid crossing a sulcus, ventricle walls, vessels (if visible on the images), and/or larger fiber tracts. Particular attention was paid to the trephination, which was placed over a vessel free area.

 

Intraoperative Examinations and Target Verification

A bipolar electrode (outer diameter, 2 mm; distance between the poles, 2 mm) was stereotactically introduced at a point 4 mm above the target, and this position was controlled on C-Arm fluoroscopy. If the electrode was placed in accordance with the planned trajectory, stepwise macrostimulation (in 1-mm steps) was performed using a frequency of 130 Hz and a pulse width of 0.1 msec. The intraoperative improvement in symptoms was recorded by a neurologist, and the electrode position that provided the optimum clinical effect was documented. The implantable stimulation lead was then introduced with the aid of fluoroscopic guidance, placing the most distal electrode pole (defined as pole 0 on a scale ranging from 0 to 3) at the clinically defined optimum target point. The lead was affixed with a suture and additionally stabilized by application of methyl methacrylate. The leads were connected to subcutaneously implanted impulse generators.

 

Postoperative Management

The stimulation parameters were definitively adapted by testing the effect of stimulation for each electrode pole in a monopolar mode under a controlled medication-off condition and by choosing the contact for long-term stimulation that resulted in the best clinical improvement at the lowest stimulation intensity and largest therapeutic range before induction of side effects. During the following months, stimulation parameters and medication were adjusted according to patient needs. Normally, only minor changes were necessary after the 3-month follow-up examination. The patients were readmitted to the neurology department at regular intervals (3, 6, and 12 months, and later in yearly intervals) and examined according to the protocol. The stimulation parameters used for long-term stimulation, including impedance of the active contact and medication, were documented along with the patients’ clinical scores at each follow-up examination.

 

Clinical Evaluation

The patient were evaluated before and after the surgery according to the Core Assessment Program for Intracerebral Transplantation (CAPIT)[17]. According to the CAPIT there was unanimous agreement on the need for at least one pharmacological test. The test was performed while patient is in off state (i.e. 12 h since the last levodopa intake, for example, the last levodopa dose was at 20.00 h the night before, then the test can not start before 8.00 h the next morning). The patients were tested one hour after the patient has gotten from bed in the morning . Patients were fasted from midnight, no food or fluid  other than water or one  cup of coffee or tea are allowed prior to the test  and until the test was over. Before administering levodopa the Unified Parkinson's Disease Rating  Scale  UPDRS[13] should be performed. Then the patient's levodopa 1.5 times higher than regular morning dose was given and then performs UPDRS in the on-state. Table 2 shows the mean values of the DBS parameters of the stimulation at the time of the first post operative neuropsychological evaluation.


 

Table 2. Stimulation parameters at the time of the postoperative assessment.

 

 

Right STN

Left STN

Voltage, V              

3.6 V (1.6 SD)

3.5 V (1.5 SD)

Pulse width, µs              

83.6 µs (15 SD)

87.9 µs (15 SD)

Rate, Hz

137.9 Hz (25 SD)

 


Neuropsychological and Psychiatric Evaluations

A thorough clinical interview and neuropsychological evaluation were performed preoperatively to assess the baseline cognitive profile. Patients were re-assessed at 6-9 months postoperatively. Components of the neuropsychological test battery were selected with some consideration in mind first the battery should be brief, second should be able to evaluate different cognitive domains affected by Parkinson's disease, third should cover aspects of cognitive, emotional and behavioral aspects that have been shown to be affected by DBS and fourth consider cultural difference. Patients were assessed for visuo-spatial reasoning using Raven Color Matrices[18]. This requires the patient to select one piece from six pictures to complete one figure and to find a logical correlations among those pictures. Short term memory was evaluated using the verbal span and digit span. The verbal learning assessment was achieved by the Paired Associate Learning, Weschler Memory Scale subtest[19]. In simplified form of the Wisconsin Card Sorting test (WCST), a series of cards of different numbers, shapes and colors where patients choose the card according to the rule that must change after six corrected items[20]. The Trail Making B assess the patient's ability to link letters and  numbers alternatively. The State Trait Anxiety test[21] was used to assess anxiety as a reaction to stress conditions and as a predisposition to experience persistent anxious behavior. Mood was evaluated by Beck Depression Inventory (BDI) Scale a 21 item self rated scale[22]. The semi-structured Clinical Interview for the DSM-IV Axis II Disorders (SCID-II) was used to evaluate personality traits. The SCID-II is composed of a 12-subscore questionnaire (113 items), each related to a different diagnostic category (avoidant, dependent, obsessive-compulsive, passive-aggressive, self-defeating, paranoid, schizotypal, schizoid, histrionic, narcissistic, borderline and antisocial).

Quality of life assessment: 

Parkinson Disease questionnaire (PDQ-39)23 is used to assess parameters of quality of life in those patients. First, a non-healthcare professional translated the original English version of the PDQ-39 into Arabic. The back-translation was done by another translator to check possible mistakes or cultural biases. The questionnaire was then reviewed by its authors to make it easily accessible and compatible with the patients. The PDQ-39 comprises 39 questions with five different options of answer related to the frequency of the disease manifestation. The answers refer to impact of the illness on the patient’s life in the previous month, as explained before the interview. The 39 questions are divided into 8 dimensions: mobility (10 questions), activities of daily living (ADL) (6), emotional well-being (6), stigma (4), social support (3), cognition (4), communication (3), and bodily discomfort (3). The score for each question ranges from zero (0) to four (4): “never” = 0; “occasionally” = 1; “sometimes” = 2; “often” = 3; “always” = 4. The final score is the result of the following equation: the sum of each question score divided by the result times 4 (the maximal score for each question), divided by the total number of questions. This result is multiplied times by 100. Each dimension score ranges from 0 to 100 in a linear scale, in which zero is the best and 100 the worst quality of life.

 

Statistical Analysis

T-Test for paired samples were run to compare pre and post operative test scores. Pearson correlation analysis was used  to assess the correlation between variables .Each raw score was converted to standard z score using means and standard deviation in order to assess changes among patients after surgery. The standard deviation (+1) was used to consider a patient as improved or deteriorated. A p value < 0.05 was considered statistically significant.

 

RESULTS

 

Motor Effectiveness

A significant reduction in motor disability, equal to 50 % was found 6 months after surgery. STN stimulation allowed PD patients to reduce the daily dose of anti-parkinsonian drugs by more than 50 %.

 

Neuropsychological Data

All neuropsychological tests scores are shown in table 3. No evidence of memory and reasoning changes after STN DBS. Both verbal and spatial short term memory and verbal learning did not show significant changes. Concerning the executive functions, there was significant improvement regarding WCST performance but no significant change was observed regarding the ability to shift attention between different stimuli during Trail Marking Test part B.

 

Behavioral Data (mental status)

Data of the behavioral scales are shown in table 4&5, significant improvement was found in mood ( P <0.05 ) tested by BDI, the patient showed less depressive symptoms after the surgical procedure  but the state and trait anxiety did not show any significant change.

Regarding the personality traits (SCID-II), we found significant paranoid traits appeared in the post-operative period in one patient but there was no apparent difference regarding other personality traits. Significant correlation was found between mood state improvement (BDI) and motor improvement (UPDRS part 3) (r 60=0.3;p< 0.04).


 

Table 3. Neuropsychological test scores before and 6 months after DBS of STN.

 

 

Number

Before surgery

After surgery

t

p

Raven Color Matrices

14

26.4(4.1)

26.9(4.2)

-0.51

0.51

Verbal span

14

3.83(0.82)

4.18(0.86)

0.79

0.12

Digital span 

14

4.39(1.19)

4.66(1.21)

0.85

0.2

Trail Making test  Part B

14

275.1(169)

276(168)

0.01

0.89

Wisconsin card sorting test

Categories

Errors

Perseveration

14

 

5.0(1.3)

7.8(9.4)

3.2(4.9)

 

5.8(1.2)

5.3(6.9)

1.5(3.2)

 

-1.65

2.56

1.9

 

0.07

0.02*

0.03*

Paired association

14

10.1(3.4)

10.3(3.1)

0.22

0.79

 

Table 4. Mood changes before and 6 months after DBS of STN.

 

 

Number

Before Surgery

After Surgery

t-test

P

BDI

14

15.3(7.9)

11.7(7.2)

2.35

0.006*

STAI

14

43.6(8.9)

41.9(8.8)

1.31

0.316

* Significant at p<0.01

Table 5. Personality profile before and 6 months after surgery.

 

SDID II

Schizoid

Schizotypal

Paranoid

Borderline

Narcissistic

Histrionic

Antisocial

Obsessive compulsive

Avoidant

Dependent

Passive aggressive

 

14

14

14

14

14

14

14

14

14

14

14

 

1.9(1.1)

1.4(0.9)

2.9(1.4)

0.1(0.7)

0.3(1.1)

0.1(0.3)

0.7(0.9)

1.2(0.9)

1.9(1.4)

0.8(0.6)

1.2(0.9)

 

1.8(1.3)

1.6(1.1)

1.8(1.5)

0.3(0.9)

0.3(1.4)

0.1(0.7)

0.6(1.1)

1.4(1.1)

1.8(1.5)

0.7(1.2)

1.4(1.1)

 

1.24

-0.19

3.33

-0.79

-0.34

-0.27

-0.84

-0.16

1.1

-0.81

-0.16

 

0.177

0.782

0.003*

0.288

0.632

0.669

0.313

0.217

0.187

0.239

0.217

* Significant at p<0.01

 

Table 6. Quality of life assessment before and 6 months after DBS of STN.

 

 

Number

Before Surgery

After Surgery

Mann-Whitney test

(significance)

Mobility

14

68.6(24.1)

27.5(28.5)

P < 0.05*

Activity of daily living

14

53.7(26.0)

32.8(28.2)

P < 0.05*

Emotional wellbeing

14

56.2(24.9)

30.5(26.3)

P < 0.05*

Stigma

14

40.1(33.5)

25.2(27.6)

P > 0.05

Emotional support

14

67.4(13.0)

68.0(13.1)

P > 0.05

Cognition

14

33.9(19.6)

30.7(20.3)

P > 0.05

Communication

14

58.4(26.8)

21.3(27.4)

P < 0.05*

Bodily discomfort

14

55.7(26.9)

20.7(23.6)

P < 0.05*

* Significant improvement in the items of mobility, activity of daily living, emotional wellbeing, communication and bodily discomfort.

 

 


DISCUSSION

 

In this study, the data confirm that deep brain stimulation of the sub-thalamic nucleus considered as a safe procedure regarding the cognitive and behavioral effects. In our study, we did not found decline in the phonemic and semantic verbal fluency tasks after the surgical procedure. Some investigators10,24 found decline in those tasks and they stated that this decline could be due to increase in apathy after surgery but this was not rated in this study.

The patients in this study showed a global stabilization of cognitive functions pre and post-surgery as declared through the non-significant change in MMSE scores, a significantly lower number of preservative and total errors on the WCST after surgery than before surgery. These results agreed with other research work24,25. No patients in this study showed any relevant cognitive decline. The surgical procedure itself showed far superiority over other surgical techniques reported to adversely affect cognitive functions in PD patients as being reported by Jahanshahi el al (2002) on their work on 13 PD patients undergoing post ventral pallidotomy (PVP) using the WCST, self-ordered random number sequences, missing digit test, paced visual serial addition test and visual conditional learning test26. As mentioned in researches, PD patients commonly display impairment in executive functions and this executive deficits are typically associated with damage to either dorsolateral or the orbitomedial circuits of the prefrontal cortex27. 

In this study, some improvement in mood state was found after surgery which is agreement with some other studies8,9 Also, a significant correlation was found between postoperative reduction in depressive symptoms and motor benefit induced by the STN stimulation and probably the improvement in mood could be a consequence of the reduction in the motor disabilities. No worsening in mood was experienced by any patients in this study and this disagrees with some studies that showed some worsening in depressive symptoms post-DBS12,28.

This study showed also no change in the anxiety symptoms after surgery a finding which contradicts with the findings of other studies that reported reduction in anxiety after surgery29.

An interesting finding of the present study is that one patient had a significant increase in paranoid traits that became more distrustful of other people; suspicious and more worried about negative judgments of others in social situations. At variance with other studies30,31, there were no significant change in other personality traits. As for depression, such behavioral changes could be due to many factors such as stimulation per se, the procedure as a whole or the progression of the disease.

According to PDQ-39, Quality of life items showed significant improvement in the items of mobility, activity of daily living, emotional wellbeing, communication and bodily discomfort. The item cognition according to this questionnaire showed non-significant improvement. In spite of this, the previously mentioned cognitive subtests applied to those patients in this study showed more precise detailed results. The item stigma also showed non-significant change which necessitates further investigation and special concern to this issue which appear that it has a little relation to just the mere motor and emotional improvement after surgery.

Conclusion: In comparison to a variety of alternative surgical procedures reported as a treatment strategy for Parkinson disease, subthalamic deep brain stimulation stands as one of the most beneficial surgical interventions in this respect. Not only motor improvement which distinguish this procedure, but also its protective effect on mental status which carries an increasing concern in recent researches. Further researches are also needed to throw light on the effect of deep brain stimulation on different psychiatric disorders when other non-pharmacotherapy methods are thought of. 

 

[Disclosure: Authors report no conflict of interest]

 

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الملخص العربي

 

تأثير الاستثارة العميقة للمخ علي الحالة الحركية و العقلية لدي مرضي الشلل الرعاش دراسة مصرية مبدئية

 

يهدف هذا البحث إلي دراسة تأثير الاستثارة العميقة للمخ علي الحالة الحركية والنفسية والوظائف المعرفية وأيضا جودة الحياة لدي مرضي باركنسون. وقد اختير لهذا البحث أربعة عشر مريضا تم إجراء عملية الاستثارة العميقة للمخ عليهم وقد تم إجراء قياسات الوظائف المعرفية ومعايير الشخصية وأيضا جودة الحياة قبل وبعد العملية بستة – تسعة أشهر. وقد وجد تحسن في الوضع الحركي لدي هؤلاء المرضي وأيضا وجد أن الوظائف المعرفية لم تتأثر سلبا بعد العملية كما هو الحال في الأنواع الأخري للجراحات الخاصة بهذا المرض بل علي العكس وجد تحسن في الوظائف التنفيذية بمقياس ويسكونسن وأيضا وجد تحسن في الحالة المزاجية بمقياس بك للإكتئاب. كما وجد أيضا تحسن في بعض عناصر جودة الحياة بعد العملية.



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