Journ31l of In.nderr.3d. ua.3E- researchh
..OluinITe , isSue 6 - [1.3, .' une -iu
Social Support in Relation to Outcome from Deep Brain Stimulation Surgery
Amanda Fogel, Kelly Foote, M.D., Michael Okun, M.D., Pam Zeilman, ARNP, Et Davin Boviers, Ph.D.
Success of Deep Brain Stimulation, a neurosurgical procedure for the management of Parkinson's disease, is
typically measured by motor improvements. The purpose of this study was to test the hypothesis that perception
of successful outcome by the Parkinson's disease patients following Deep Brain Stimulation surgery is related to
non-motor factors such as social support and mood. Patients with idiopathic Parkinson's disease and a history of
Deep Brain Stimulation surgery were assessed for non-motor and motor factors using both general and
Parkinson's disease-specific standardized measures. Surgery outcome was based on the Global Impression
Scale. Over 90% of the Parkinson's disease patients reported improvement on the Global Impression Scale.
Social support and mood (anxiety, apathy) were significantly correlated to perception of surgery outcome;
however, there was no relationship between patient perception of surgery outcome and changes in motor
function. These findings provide preliminary support for the hypothesis that non-motor factors play an important
role in the patient's perception of successful outcome following Deep Brain Stimulation. These factors may
be considered in counseling pre-Deep Brain Stimulation Parkinson's disease patients.
Parkinson's disease (PD) is a progressive dopamine depletion disorder that results in a variety of motor, mood,
and cognitive changes. Early on during the disease course, PD can be effectively treated with various
medications. Over time, these medications become less effective and patients develop "on/off" periods
and dyskinesias (abnormal writhing movements). These can be particularly debilitating. Recently
several neurosurgical approaches have emerged as successful treatments for the symptoms of PD. One
such approach is deep brain stimulation (DBS), which involves the placement of small stimulating electrodes
deep into the basal ganglia. Traditionally, successful outcome from DBS surgery is gauged by improvements
in motor symptoms. Recent focus on "patient oriented outcomes" and consideration of psychological factors
helped to shape the goal of the present study:to examine social support and mood factors that might contribute
to successful outcome following DBS surgery in PD patients above and beyond motor changes.
Parkinson's disease (PD) is the second most common neurodegenerative disease in the United States
(Schapria, 2006). It affects approximately 1.5 millions individuals in the U.S., with approximately 60,000 new
cases diagnosed each year (National Parkinson Foundation, 2007). The likelihood of developing PD
dramatically increases after the age of 60 and the prevalence of PD is nearly 5% in individuals over the age of
85 (Rao, Hofmann, & Shakil, 2006). Not only does PD affect the individual diagnosed with the disease, but it
also impacts caregivers and contributes to a substantial socio-economic burden. Health care costs and loss of
worker productivity equates to approximately $25 billion per year (Scheife, Schumock, Burstein, Gottwald, &
Luer, 2000). Clinically, PD is characterized by motor symptoms of tremor, slowness (bradykinesia), rigidity,
and postural instability (Gelb, Oliver, & Gilman, 1999). Other common motor symptoms include dysarthria
(soft, slurred speech), dysphagia (difficulty swallowing), and masked faces (reduced facial expressivity) (Sharma
& Richman, 2005).
Symptoms of PD are not limited to the motor system and also include cognitive and mood changes.
Mood disturbances are common including depression, apathy, and anxiety. Up to 50% of patients with PD
experience symptoms of depression and/or apathy (Allain, Schuck, & Maudult, 2000; Kirsch-Darrow,
Fernandez, Okun, & Bowers, 2006). The bases for these mood changes are unknown, but likely reflect a
normal reaction to illness coupled with dysfunction in brain areas that are important for emotion.
Pathophysiology of Parkinson's Disease. The pathophysiology of idiopathic PD appears to involve a
progressive loss of dopamine producing neurons in the substantial nigra compact (Worldwide Education
and Awareness for Movement Disorders [WEMOVE], 2006). This depletion of dopamine, an
inhibitory neurotransmitter, influences the neural circuitry of the basal ganglia (Huether & McCance,
2004). Projections from the striatum to the GPi comprise the direct neural circuitry of the basal ganglia, while
the indirect pathway projects from the striatum to the GPi via the globus pallidus externa and STN. The GPi, the
final output nuclei of the basal ganglia, is inhibitory to the motor nuclei (VA/VL complex) of the thalamus and
the thalamus is excitatory to the motor cortex (Halpern et al., 2006). In the normal neurophysiologic state,
inhibition of the GPi disinhibits the thalamus, thereby allowing for excitation of the motor cortex (Purves et
al., 2001). Thus, initiation of movement occurs. Activity of the GPi is enhanced in the indirect pathway,
thereby inhibiting the thalamus and decreasing excitation of the motor cortex (Purves et al., 2001).
Therefore, dysfunction of this system produces an increase of involuntary movement and decreased
Treatments of Parkinson's Disease: Medication and Surgical. Initially, PD typically responds well
to pharmacologic interventions. The most effective agent is levodopa, a precursor to dopamine, in combination
with carbidopa to allow passage through the blood-brain barrier (Rao, Hofmann, & Shakil, 2006). As the
disease progresses, individuals may unexpectedly experience less benefit from previously successful
medication regimens. This is manifested as unanticipated "on/off" fluctuations with progressively longer
"off" periods. Greater quantities and increased frequencies of the medications are required, often resulting
in undesired side effects such as dyskinesias.
If traditional pharmacologic treatments become ineffective, the patient may consider alternative interventions such
as surgery. There have been two types of neurosurgical interventions utilized for the management of PD. The
first involved creating permanent lesions in the basal ganglia or thalamus (i.e., pallidotomy or thalamotomy).
The more recent approach, known as deep brain stimulation (DBS), involves placement of small
stimulating electrodes into the basal ganglia, either the subthalamic nucleus (STN) or the globus pallidus
internus (GPi). In DBS, a high-frequency electrical stimulation emitted by the electrode creates a temporary
lesion, thereby obstructing neuronal activity of the dysfunctional regions without causing permanent
damage (Hashimoto, Elder, Okun, Patrick, & Vitek, 2003). The best candidates for DBS surgery are individuals
with minimal cognitive dysfunction, ideally under the age of 69 years, and diagnosed with idiopathic PD.
Additionally, optimal candidates typically experience "on/off" fluctuations, dyskinesias, and demonstrate
a considerable response to the medications exhibited by at least a 30% improvement on the movement scale of
the Unified Parkinson's Disease Rating Scale (UPDRS) in the "on" versus "off" medication states (Okun et al., 2007).
Measuring Outcomes of Surgery
The success of any treatment modality, including surgical procedures, is often difficult to objectively assess.
Consider the case of H.M.. This patient experienced epileptic seizures of severe and debilitating nature, which
were unresponsive to standard forms of treatment. Therefore, an experimental surgery, a bilateral medial
temporal lobe resection, was recommended (Scoville & Milner, 2000). H.M.'s seizure severity diminished
significantly in the year following the operation, and, although the patient eventually experienced some
generalized seizures, these seizures were less frequent, less severe, and the patient no longer suffered
a compromised level of consciousness following the attacks. However, an unexpected side effect occurred
following the procedure. H.M. developed severe anterograde and partial retrograde amnesia (Scoville &
Milner, 2000). The physicians had effectively managed H.M.'s seizures; yet, a debilitating side effect developed.
The question, then, is whether the surgery was a success or a failure.
Success may be defined as the achievement of a desired goal, whereas satisfaction is characterized by feelings
of gratification and pleasure attained from the success. Therefore, when measuring the outcome of an
elective surgical procedure, such as DBS, it is necessary for investigators to understand the importance of
the patient's perception of outcome, above and beyond changes in scores on standard motor scales. This is known
as "patient-centered outcome." Satisfaction or dissatisfaction is not determined solely by the success or failure
of motor symptom management. The patient's impression of the surgery is also influenced by non-motor
factors such as expectations, mood, and perception of social support.
Establishing realistic expectations prior to the DBS procedure is an essential element of the candidacy
screening process and significantly contributes to the patient's post-surgical perception of the intervention.
Mood may also mediate patient perception of outcome. For example, DBS may provide no symptomatic relief
and result in the side effect of significant speech and language problems due to complications during the
procedure; however, an apathetic patient may not manifest dissatisfaction due to his or her
indifference. Alternatively, a procedure with objectively favorable motor symptom improvement may not satisfy
an anxious or depressed patient. Additionally, a patient's perception of social support is believed to play a major
role in success and satisfaction of surgical procedures.
Recently, researchers have begun to understand the role of social support in predicting patient satisfaction
with surgery following elective procedures for the management of chronic medical conditions. One study focused
on a patient population of individuals diagnosed with intractable epilepsy who underwent anterior temporal
resections to reduce seizure frequency (Rogish, Bowers, Bauer, & Gilmore, 2003). Higher ratings of
satisfaction following seizure surgery were not related to reduced number of seizures. Rather satisfaction
was associated with greater perception of social support and fewer symptoms of depression following the
surgery. Basically, it was interpreted that perception of strong social support, which was negatively correlated
with depression, may be a very effective indicator of satisfaction with the surgical procedure (Rogish et al.,
2003). The role of perception of social support in relation to patient perception of satisfaction following
DBS stimulation remains unknown.
Overview and Statement of the Problem
As DBS becomes more available, it is being used in the treatment of PD with more frequency. This
elective neurosurgical procedure attempts to manage a patient's most bothersome symptoms when they are
no longer adequately controlled by oral medications. Previous studies measuring the outcome of DBS for the
PD primarily focused on changes in the severity of motor symptoms.
Although improvements in motor symptoms are the typical indicators of successful DBS outcome, other "non-
motor" factors might also be critical. Thus, the purpose of the present study was to test the hypothesis
that perception of successful outcome by PD patients following DBS surgery is related to perceived social support
and mood. To test this hypothesis, patients who had undergone DBS surgery at least six months previously
were administered a variety of standard measures that assessed their perception of surgery outcome, their
mood, and their perception of social support. Patient perception of surgery outcome was measured using the
Patient Global Impression Scale (PGIS). Mood measures included the Beck Depression Inventory-II (BDI-II),
the Beck Anxiety Inventory-II (BAI), and the Marin Apathy Inventory (MAI). Finally, perception of social support
was measured in two ways, by the Multidimensional Scale of Perceived Social Support (MSPSS) and the
Social Support subscale of the Parkinson's Disease Questionnaire-39 (PDQ-39). Other measures of PD motor
severity were obtained from the clinical database maintained by the Movement Disorders Center and included
the Unified Parkinson Disease Rating Scale (UPDRS)-motor and the Hoehn and Yahr staging of disease severity.
Participants included patients with idiopathic PD who had previously undergone DBS surgery at least six
months previously and spoke English as their primary language. Patients with a history of previous
pallidotomy, thalamotomy, or other brain surgery were excluded from this study. Participants were recruited
from the University of Florida Movement Disorders Center (MDC), which maintains an Institutional Review
Board-approved database of patients who have previously agreed to be contacted and invited to participate
in research studies. From this database, subjects were recruited via telephone or while visiting the MDC
neurology clinic for scheduled medical appointments. Approximately 54 PD patients were initially contacted.
The final sample included 35 PD patients (29 male, 6 female) ranging in age from 37 to 82 years (mean = 62.91
+ 9.160 years). The duration of PD symptoms ranged from 6 to 24 years (mean = 14.61 + 5.205) and years
of education ranged from 8 to 20 years (mean = 15.34 + 2.508).
Global Impression Scale (GIS). The GIS consists of two items. The general question asked the patient to
rate their current overall state relative to before DBS; and, the symptom-specific question asked the patient to
rate the status of their most debilitating symptom they had hoped DBS would improve. Versions of the GIS
were completed by the Patient (PGIS), the clinician (CGIS), and the caregiver.
Multidimensional Scale of Perceived Social Support (MSPSS). The MSPSS questionnaire consists of
twelve questions, four from each of the three domains (Family, Friends, and Significant Other). Higher scores on
the MSPSS suggest a better perception of social support.
Social Support subscale from the Parkinson Disease Questionnaire-39 (PDQ-39). Social support was
also measured using a subscale from the PDQ-39, a disease-specific measure of health-related quality of life
with additional subscales such as Mobility and Activities of Daily Living (ADL). Three questions of the PDQ-39
focus on social support. Higher scores on the PDQ-39 correlate with a lower health related quality of life, and
Unified Parkinson Disease Rating Scale (UPDRS)-Motor and theHoehn and Yahr Staging. Administered
and rated by a clinician, the UPDRS was obtained from the MDC database. Higher scores on UPDRS-Motor
scale indicate worse motor functioning. UPDRS-Motor scores were obtained before and after patients underwent
DBS surgery. Due to missing data, only "on medication" UPDRS-Motor scores were available. Additional
functional motor scores included the modified Hoehn and Yahr staging.
Mood ratings of depression, anxiety, and apathy. Mood was assessed using self-report scales of
depression (Beck Depression Inventory-II; BDI-II), anxiety (Beck Anxiety Inventory) and apathy (Marin
Apathy Inventory, MAI). Higher scores on the BDI-II, BAI, and MAI indicate higher levels of depression,
anxiety, and apathy, relatively.
Prior to beginning the study, informed consent was obtained from all participants according to University and
federal guidelines. The participants then completed the various questionnaires described above. Pre- and
post-operative UPDRS scores and Hoehn and Yahr ratings were obtained from the UF MDC database along with
the clinician-completed CGIS.
Over 90% of the patients reported improvement in general and specific motor symptoms of PD following
DBS surgery. Because of a skewed distribution, the two items on the PGIS were combined into a single metric
during subsequent data analyses. To test the primary hypothesis of a relationship between DBS outcome
and perception of social support, a series of correlation analyses were performed. Results of this analysis
revealed the following: (a) there was a significant correlation between the PGIS and the Social Support subscale
of the PDQ-39 (r = .376, p = .029); and (b) although the PDQ-39 Social Support subscale correlated fairly well
with the MSPSS, no association was found between the MSPSS subscales and the patient impression of
surgery outcome. Correlation analyses were also conducted to examine the relationship between mood and
patient perception of outcome. Results indicated that worse patient outcome ratings were associated with
higher anxiety scores (r = .497, p = .001) and with higher apathy scores (r = .467, p = .006). There was
no relationship between depression and patient outcome ratings.
Exploratory analyses were also conducted to examine factors that influenced the clinician and caregiver
global impression ratings of DBS outcome. Although the PDQ-39 ADL subscale did not correlate with the PGIS,
there was a relationship between the PDQ-39 ADL subscale and the CGIS (r = .548, p = .007). Also notable was
the trend toward a correlation with the Mobility subscale of the PDQ-39 and the CGIS (r = .38, p = .06). The
Hoehn and Yahr staging ratings correlated with the CGIS (r = .548, p = .007). Also, clinicians rated
better improvement of patients with a younger age (r = .427, p = .029). Finally, there was a correlation between
a lower post-operative UPDRS motor score and the caretaker's GIS rating (r = .461, p = .03).
The findings of the present study support, in part, the hypothesis that the patient's impression of
improvement following DBS surgery would be related to their perception of social support. This was based on
a significant correlation between perception of social support, as measured by the PDQ-39 Social Support
subscale, and post-DBS outcome, as measured by the composite score of the PGIS. Therefore, patients with a
better perception of social support also perceived improvement following DBS. None of the MSPSS
subscales correlated with the PGIS. Perhaps this is because the MSPSS is a general measure of perception of
social support, whereas the PDQ-39 is a disease-specific measure that is validated and reliable when used to
assess sample populations with PD patients.
Depression, apathy, and anxiety are commonly comorbid with PD; therefore, the BDI-II, MAI, and BAI were
included in the study to assess the relationship between mood and perception of outcome. Higher ratings of
anxiety and higher ratings of apathy were associated with worse PGIS scores. Patients interpreting the surgery
as unsuccessful may feel anxious as a result of dissatisfaction with DBS outcome. However, this
causal relationshiprequires further research.
Various factors that might contribute to global impression ratings of DBS outcome by clinicians were also
examined. The CGIS significantly correlated with the Hoehn and Yahr staging scores and the ADL subscale of
the PDQ-39. Lower, or better, post-operative "on" medication Hoehn and Yahr staging, correlated with lower,
or better, ratings on the CGIS. Therefore, clinicians rated improvement resulting from the DBS intervention
for patients displaying fewer motor symptoms. Additionally, lower, or better, patient self-reported ADL status on
the PDQ-39 correlated with lower, or better, ratings on the CGIS. Therefore, clinicians perceived
patient improvement following the DBS procedure for those patients able to perform more ADLs
independently. There was also a recognized trend toward a relationship between the CGIS and the Mobility
subscale of the PDQ-39. With a larger sample size, there may have existed a correlation between better
motor functioning, as self-reported by the patient via the PDQ-39 subscale, and a better outcome following DBS,
as viewed by the clinician and rated using the CGIS. However, these results may merely be spurious if the
clinicians based their CGIS ratings on previously completed subjective measures. A more objective association
was found between age of the patient and post-DBS outcome. The lower the age of the patient, the better
the clinician perceived the patient's outcome.
A correlation existed between the caregiver's ratings of patient outcome and the patient's post-operative
"on" medication UPDRS-Motor scores. Lower UPDRS-Motor scores equate to better motor functioning, which
is correlated with better ratings of patient outcome as viewed by the caregivers.
In summary, the findings of the present study partially support the primary hypothesis that there is a
relationship between perception of successful outcome by PD patients following DBS surgery and "non-
motor" factors: perception of social support and mood. The results indicated a significant correlation between
the patient composite scores of DBS outcome (PGIS) and the Social Support subscale of the PDQ-39, the BAI,
and the MAI. Therefore, those with a positive perception of social support also perceived a positive
outcome following DBS, and worse patient outcome ratings were associated with higher levels of anxiety and apathy.
This study provided significant and noteworthy results regarding the relationship between various motor and
non-motor factors and outcome following DBS in the PD population. However, there are a number of
potential confounding variables and other limitations of the experimental design, measures, and statistical analyses
of this study. Although one criterion for inclusion in the study stipulated at least 6 months post-DBS, there was
no limit to the length of time since the surgery. Therefore, it is possible that those subjects who underwent
DBS within the year may still be experiencing the honeymoon effects of the procedure; whereas, those
subjects several years post-DBS may be experiencing longitudinal functional declines.
The chief complaint the patient pursued DBS to relieve may impact the perception of satisfaction with the
procedure. First of all, expectations with the surgery have an impact on interpretation of results. Additionally,
the patient's chief complaint is a critical factor in the clinician's target for the location of the DBS leads.
Current research is studying the efficacy of target sites, such as the STN and GPi, and the resulting
symptomatic relief. Medication effects and interactions, as well as post-operative complications and length of
post-operative hospital stay, may impact a patient's perception of the procedure. Also, the patient's perception of
his or her relationship, or rapport, with the clinician may contribute to or alter their perception of outcome.
The small sample size significantly limited the generalizeability of the results of this study because the ratings of
the PGIS were skewed. The measures used contributed to limited variability of the data because the Social
Support subscale of the PDQ-39 was comprised of merely three questions and the GIS was comprised of only
two questions, combined into one composite score. Additionally, the MSPSS questionnaire, although
standardized, was not a PD disease specific measure; therefore, although the PDQ-39 Social Support
subscale correlated with the PGIS, the MSPSS did not. Finally, the correlation statistical analyses used in this
study aid in demonstrating the strength and direction of a relationship between various variables; however, no
cause and effect conclusions may be drawn. In other words, this study provided evidence of a relationship
between better perception of social support and better perception of positive outcome following the DBS procedure
in the PD population.
Future studies investigating the relationships this research identified should collect data from a larger sample size
and incorporate multiple clinical sites, as well as implement pre- and post-operative questionnaires with the
potential for greater variability in the resulting data sets. The MDC already implements the PDQ-39, BDI, and
GIS. Replacing the currently provided State Trait Anxiety Inventory with the BAI or additionally incorporating the
BAI may aid in future studies of correlation or cause and effect. These tools may be relevant to the pre-
DBS screening and counseling process to identify optimal candidates for the surgery and address issues that
may impact outcome following the operation.
1. Allain, H., Schuck, S., & Maudult, N. (2000). Depression in Parkinson's disease. British Medical Journal, 320,
Gelb, D. J., Oliver, E., & Gilman, S. (1999). Diagnostic criteria for Parkinson disease. Archives of Neurology, 56,
2. Hashimoto, T., Elder C. M., Okun M. S., Patrick, S. K., & Vitek, J. L.(2003). Stimulation of the subthalamic
nucleus changes the firing pattern of pallidal neurons. The Journal of Neuroscience, 23(5).
3. Huether, S. E., & McCance, K. L. (2004). Understanding pathophysiology (3rd ed.). Missouri: Mosby.
4. Kirsch-Darrow, L., Fernandez, H., Okun, M., & Bowers, D. (2006). Dissociating apathy and depression in
Parkinson's disease. Neurology, 67(1), 20-27.
5. National Parkinson Foundation, Inc. (2004), About Parkinson disease. Retrieved January 10, 2007, from http://
6. Okun, M. S., Rodriguez, R. L., Mikos, A., Millar, K., Kellison, I., Kirsch-Darrow, L., Wint, D. P., Springer,
U., Fernandez, H. H., Foote K. D., Crucian, G., & Bowers, D (2007). Deep brain stimulation and the role of
the neuropsychologist. The Clinical Neuropsychologist, 21(1), 162-189
7. Okun, M. S. & Foote, K. D. (2005). Subthalamic nucleus vs globus pallidus internal deep brain stimulation,
the rematch. Archives of Neurology, 62, 533-536.
8. Purves, D., Augustine, G. J., Fitzpatrick, D., Katz, L. C., LaMantia, A. S., McNamara, J. 0., & Williams, S. M.
(2001). Neuroscience (2nd ed.). Massachusettes: Sinauer Associates, Inc.
9. Rao, S. S., Hofmann, L. A., & Shakil, A. (2006). Parkinson's disease: diagnosis and treatment. American
Family Physician, 74(12), 2046-2060.
10. Rogish, M. Bowers, D., Bauer, R., & Gilmore, R. (2003). The differential contribution of perceived social support
and surgical outcome on depression in post-surgical ATL epilepsy patients. Abstract: Journal of
International Neuropsychology Society, 9, 277.
11. Scheife, R. T., Schumock, G. T., Burstein, A., Gottwald, M. D., & Luer, M. S. (2000). Impact of Parkinson's
disease and its pharmacologic treatment on quality of life and economic outcomes. American Journal of
Health-System Pharmacy. 57(10), 953-962.
12. Scoville, W. B., & Milner, B. (2000). Loss of recent memory after bilateral hippocampal lesions. Journal
of Neuropsychiatry and Clinical Neurosciences, 12(1), 103-113.
13. Sharma, N., & Richman, E. (2005). Parkinson's Disease and the Family. Cambridge, Massachusetts:
Harvard University Press.
14. Worldwide Education and Awareness for Movement Disorders. (2006). The substantial nigra in PD. Retrieved
January 10, 2007, from http://www.wemove.org/par/par_subn.html
Back to the Journal of Undergraduate Research
College of Liberal Arts and Sciences I University Scholars Program I University of Florida |
ï¿½ University of Florida, Gainesville, FL 32611; (352) 846-2032.
* | UNIVERSITY of