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Social Support in Relation to Outcome from Deep Brain Stimulation Surgery

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Social Support in Relation to Outcome from Deep Brain Stimulation Surgery
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Fogel, Amanda
Bowers, Dawn ( Mentor )
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Gainesville, Fla.
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University of Florida
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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.


ABSTRACT


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.



INTRODUCTION


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


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

voluntary movement.



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.



Social Support


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.



METHODS


Participants






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).



Materials


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

vice versa.



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.






Procedure


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.



RESULTS


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).



DISCUSSION


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.



Limitations


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 directions


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.






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