Abstract
Background:
Available treatment options for Parkinson's disease (PD) are primarily aimed at pharmacological and/or neurosurgical management of motor symptoms. However, many patients also experience chronic non-motor symptoms (NMS), including significant cognitive and mood changes. Currently, there is a gap in the neuropsychological literature regarding the efficacy of nonpharmacological treatment options for cognitive and mood changes in PD.
Objective:
We sought to evaluate the efficacy and patient satisfaction of a pilot nonpharmacological intervention for alleviating NMS in patients with PD.
Methods:
Twenty-three independently functioning nondemented patients with PD participated in a 5-week Parkinson’s Disease Enrichment Program. Each 4-hour weekly session included content which addressed the following components: education, exercise, recreation, and socialization/support. Participants received a pre-assessment, including cognitive tests and questionnaires for depression and quality of life. After the completion of the program, participants completed post-assessment batteries to measure changes in neurocognitive and psychiatric status, as well as patient satisfaction regarding the program.
Results:
Neuropsychological data from pre- and post-assessments revealed significant improvements in measures of executive functioning, memory, and depressive symptoms. No significant changes were observed on the remaining mood or cognitive measures. One hundred percent of participants reported enjoyment from socialization with other participants with PD and satisfaction with the program overall.
Conclusions:
Positive preliminary results suggest that further expansion of this nonpharmacological pilot program for treatment of NMS may be beneficial for patients with PD. Future studies will investigate a larger cohort of participants with PD and cross-validate findings in demographically diverse samples.
Parkinson's disease (PD) is the second most common neurodegenerative disorder after Alzheimer disease, 1,2 affecting over half a million adults in the United States. 3 Although PD is clinically diagnosed by motor symptoms, non-motor symptoms (NMS) are increasingly becoming a focus of research and clinical treatment. NMS have been shown to contribute to reduced quality of life (QOL), 1,4–5 disability, and shortened life expectancy. 4 Furthermore, NMS in PD have also been associated with higher rates of caregiver distress and burnout. 1,6
Cognitive changes, in particular, have been recognized as a common NMS in patients with PD throughout the course of the disease, with up to 50% of patients exhibiting symptoms of mild cognitive impairment 7 –9 and 25% to 30% developing dementia. 10,11 As many as 80% of patients with PD become affected by cognitive impairment in the late stage of the disease. 12 Cognitive changes associated with PD include executive functioning impairments 7,13,14 such as difficulty sorting and planning 15,16 and mental inflexibility, 17 impaired memory, 15,16,18 and overall cognitive slowing. 19 Considerable heterogeneity in cognitive impairment phenotypes among patients indicates that further research is needed to understand the etiology and pathology of cognitive impairment in PD.
Neuropsychiatric changes are also commonly observed among patients with PD, with the highest incidence rates reported for depression, 20,21 affecting approximately one-third to one-half of all patients with PD. 22,23 However, depression in PD often goes undiagnosed and therefore untreated in as many as 70% of all patients with PD. 24,25 Depressive symptoms can significantly reduce functional ability, accelerate cognitive deterioration, and increase caregiver distress. 20,25 Treating depression in patients with PD may aid in resolving these issues, resulting in improved disease management and QOL. Currently, pharmacological treatment is the most common avenue for managing PD NMS, including cognitive and emotional functioning. However, some patients may experience uncomfortable side effects 12,26 –28 such as confusion, 14 hallucinations, 29 or disruption of higher order mental operations, such as problem-solving and learning. 30
Evidence on the efficacy and effectiveness of nonpharmacological interventions for cognitive and neuropsychiatric symptoms in patients with PD is lacking. 26,31,32 Studies evaluating the efficacy of cognitive behavioral therapy (CBT), active music, and dance therapy for treating nonmotor symptoms in PD 26,33 –35 have yielded positive results. 1 Cognitive training and rehabilitation programs have also yielded promising preliminary results 36 –39 ; however, this research is limited and lacks replication. Additionally, studies that address NMS of PD often target either cognitive or emotional functioning but not both.
This study was designed to evaluate patient satisfaction and feasibility of a pilot recreational day program, the Parkinson’s Enrichment Program (PEP), for improving cognitive and emotional functioning and QOL in patients with PD. Although the PEP was not specifically designed to target cognitive and emotional functioning or QOL in patients with PD, we focused on this subset of NMS due to their salience and prevalence in PD. Our goal was to determine whether participation in a general recreation program would have downstream effects on cognitive and emotional functioning and QOL. We hypothesized that measures of cognitive and emotional functioning would demonstrate improvements from pre- to post-program participation.
Methods
A prospective cohort study was completed to measure changes in cognitive and emotional functioning in patients with PD before and after participating in the PEP. Methods for participant recruitment, assessment, and analyses are described below.
Participant Recruitment
Participants were recruited from the Houston Area Parkinson Society (HAPS) pool of PEP participants using the following inclusion criteria: a neurologist-confirmed diagnosis of mild-to-moderate, idiopathic PD, age between 45 and 80 years, English-speaking ability, a score of at least 19 out of 30 on the Montreal Cognitive Assessment (MoCA), 40 and a score equal to or less than 30 out of 63 on the Beck Depression Inventory II (BDI-II). 41 This study was completed with adequate understanding and written consent of the participants and with the ethical approval of the institutional review board of Baylor College of Medicine.
Program
The PEP was designed to promote enrichment and education through therapeutic recreational programs and health education for individuals with PD. The PEP was sponsored and administered by 2 master’s level social workers from HAPS. The PEP groups were conducted over the course of 5 weeks and contained a maximum of 12 participants per groups, resulting in a maximum participant to facilitator ratio of 6:1. Local experts and instructors regularly served as co-facilitators of specific activities or educational discussions throughout the course of the PEP, allowing for more individualized attention per participant. In this study, 3 PEP groups were evaluated, and our analyses are based on the cumulative group. Each week, participants met for 4 hours, resulting in a total of 20 hours of contact over the course of the 5-week PEP. Each 4-hour weekly session consisted of structured activities which addressed the following components: education, exercise, recreation, peer-led discussion, professionally facilitated support, and socialization. Examples of structured activities included virtual travel, watercolor painting, photography, tai chi, tango, yoga, group exercise, singing, Wii games, and musical instrumentation. For more information on PEP, please contact the HAPS at www.hapsonline.org.
Assessment and Outcome Measures
Participants were evaluated the week prior to the beginning of each PEP group by a trained psychometrician or neuropsychologist. Participants were then reevaluated within the 2 weeks following the end of each PEP group by the same psychometrician/neuropsychologist using the same administration procedures. All testing was completed in English, and each testing session was approximately 45 minutes long. Empirically validated cognitive measures were selected to assess global mental functioning, memory, attention and concentration, and executive function, as these are the cognitive domains commonly found to be affected in patients with PD. The following measures were used during both pre- and post-assessments: MoCA, 40 Hopkins Verbal Learning Test–Revised (HVLT-R), 42 Wechsler Adult Intelligence Scale III (WAIS-III) Digit Span, 43 Trail Making Tests A and B, 44 Stroop Color-Word Interference, 45 and Delis-Kaplan Executive Function System (D-KEFS) Verbal Fluency. 46 Alternate forms of memory and verbal fluency measures were used to reduce practice effects.
Participants also completed self-report measures of psychiatric symptomatology and QOL: BDI-II, 41 Behavioral Assessment of the Dysexecutive Syndrome–Dysexecutive Questionnaire, 47 and the Parkinson’s Disease Quality of Life Questionnaire (PDQ-8). 48 Post-test assessments also included a 10-item survey measuring program satisfaction. Items were scored using a 5-point Likert scale, with responses ranging from “strongly disagree” to “strongly agree.” Items included on this measure were “This program improved my problem-solving skills” and “I enjoyed the social interaction with other PD patients.” Data were stored and managed in a secure, password-protected database accessible only to study personnel.
Analyses
All tests were scored using Western normative data stratified by gender, age, education level, and/or ethnicity when available. Data were analyzed using a paired samples t test using IBM SPSS Statistics 24 to determine changes in mood and cognitive functioning before and after the intervention. The threshold for significance was set at p ≤ .05 for this pilot study. Effect sizes (Cohen's d) 49 were calculated using the correlation correction formula for within-subjects repeated measures data. 50
Results
Participants
Twenty-six community-dwelling, independently functioning patients with PD participated in the pre-screening/assessment and the PEP. Three participants did not complete post-assessment, due to medical emergency, transportation difficulty, or scheduling conflict, resulting in an attrition rate of 11.5% and a final sample size of n = 23. These 23 participants attended every session of the PEP. Forty-eight percent of participants were female (n = 11). Mean age was 69.2 years (standard deviation [SD] = 6.9) and mean education level was 16.6 years (SD = 2.0). Eighty-seven percent of participants were Caucasian (n = 20) and 92% were right-handed (n = 21). Mean time since diagnosis was 6.2 years (SD = 4.9).
Baseline cognitive and psychiatric statuses were established using the MoCA, BDI-II, and PDQ-8. Mean MoCA score was 24.3 out of 30 (SD = 3.4); scores ranged from 19 to 30. Forty-four percent of participants scored within the “cognitively normal” range (score ≥ 26), 39% scored within the “mild cognitive impairment” range (21 ≤ score < 26), and 17% scored within the Parkinson disease dementia range (score < 21). No additional data were used to characterize cognitive status at baseline. Mean BDI-II score was 11.8 out of 63 (SD = 7.6); scores ranged from 4 to 30. Seventy percent of participants scored within the “minimal” range (score ≤ 13), 13% scored within the “mild” range (14 ≤ score ≤ 19), 9% scored within the “moderate” range (20 ≤ score ≤ 28), and 9% scored within the “severe” range (score ≥ 29). Mean PDQ-8 total score was 8.5 of 32 (SD = 4.8); scores ranged from 1 to 21.
Pre to Post Changes in Cognitive and Emotional Functioning
Tables 1 and 2 summarize pre to post results from all outcome measures.
Pre to Post Outcome Measure Results (T Scores).a
Abbreviations: MoCA, Montreal Cognitive Assessment; HVLTTot, Hopkins Verbal Learning Test Total Recall; HVLTDel, Hopkins Verbal Learning Test Delayed Recall; HVLTRecog, Hopkins Verbal Learning Test Recognition; LDSF, Wechsler Adult Intelligence Scale Longest Digit Sequenced Forward; LDSB, Wechsler Adult Intelligence Scale Longest Digit Sequenced Backwards; DSTot, Wechsler Adult Intelligence Scale Longest Digit Span Total; TrailsA, Trail Making Test A; StroopW, Stroop Word Reading; StroopC, Stroop Color Identification; StroopCW, Stroop Color-Word Interference; DKEFSLet, Delis-Kaplan Executive Function System Letter Fluency; DKEFSCat, Delis-Kaplan Executive Function System Category Fluency; DKEFSSwi, Delis-Kaplan Executive Function System Switching Fluency; DKEFSAcc, Delis-Kaplan Executive Function System Switching Accuracy; TrailsB, Trail Making Test B; SD, standard deviation.
a T scores have a mean of 50 and a standard deviation of 10. For all measures, higher T scores correspond to higher levels of functioning.
b A measure for which a statistically significant difference was found pre- to post-testing.
Pre to Post Outcome Measure Results (Raw Scores).
Abbreviations: BDI-II, Beck Depression Inventory II; DEX, Behavioral Assessment of the Dysexecutive Syndrome–Dysexecutive Questionnaire; PDQ-8, Parkinson’s Disease Quality of Life Questionnaire.
a A measure for which a statistically significant difference was found pre- to post-testing. For all measures, an increase in raw score corresponds to worse functioning.
From before to after PEP participation, significant improvements were observed for depression scores on the BDI-II (p = .01; d = −.56). Regarding changes in cognitive performance after PEP participation, significant improvements were observed on D-KEFS switching (p = .05; d = −.44) and D-KEFS accuracy (p = .03; d = −.48), with a positive trend observed for HVLT delayed recall (p = .06; d = −.41). No significant changes were observed on the remaining mood or cognitive measures. Figures 1 and 2 illustrate these findings.
Pre to post changes in cognitive functioning. MoCA indicates Montreal Cognitive Assessment; StroopW, Stroop Word Reading; StroopC, Stroop Color Identification; StroopCW, Stroop Color-Word Interference; DKEFSLet, Delis-Kaplan Executive Function System Letter Fluency; DKEFSCat, Delis-Kaplan Executive Function System Category Fluency; DKEFSSwi, Delis-Kaplan Executive Function System Switching Fluency; DKEFSAcc, Delis-Kaplan Executive Function System Switching Accuracy; TrailsA, Trail Making Test A; TrailsB, Trail Making Test B; HVLTTot, Hopkins Verbal Learning Test Total Recall; HVLTDel, Hopkins Verbal Learning Test Delayed Recall; HVLTRecog, Hopkins Verbal Learning Test Recognition; LDSF, Wechsler Adult Intelligence Scale Longest Digit Sequenced Forward; LDSB, Wechsler Adult Intelligence Scale Longest Digit Sequenced Backwards; DSTot, Wechsler Adult Intelligence Scale Longest Digit Span Total.
Pre to post changes in emotional functioning. BDI-II indicates Beck Depression Inventory II; DEX, Behavioural Assessment of the Dysexecutive Syndrome–Dysexecutive Questionnaire; PDQ-8, Parkinson’s Disease Quality of Life Questionnaire.
Results from the postprogram satisfaction survey were collapsed across the 10 items into 4 subgroups of items: effects on cognitive functioning, effects on emotional functioning, socialization with peers, and overall program satisfaction. Seventy percent of participants self-reported both improved cognition and emotional status. Furthermore, 100% of participants reported enjoyment from socialization with other PD participants and satisfaction with the program overall (Figure 3). Participants also provided qualitative feedback indicating their satisfaction with the program.
Post program feedback.
Discussion
This study was designed to evaluate the efficacy and patient satisfaction of a pilot recreational day program (PEP) for patients with PD. Although the PEP was not specifically designed to target cognitive and emotional functioning or QOL in patients with PD, we focused on this subset of NMS due to their salience and prevalence in PD. Our goal was not to evaluate a pilot program designed to improve cognitive or emotional functioning; rather, we sought to determine whether participation in a general recreation program would have downstream effects on cognitive and emotional functioning or QOL. The neuropsychological testing and self-report mood questionnaires showed significant improvements in measures of executive functioning and memory, declines in self-reported depressive symptoms, and positive qualitative and quantitative participant feedback. Moderate effect sizes (Cohen’s d) were observed for all measures that evidenced significant change, suggesting that further expansion of this program for treatment of NMS may be beneficial for patients with PD. No marked declines or adverse outcomes were observed on any of the cognitive or emotional functioning measures or from qualitative feedback. Given baseline cognitive and neuropsychiatric status of the sample, the PEP will most likely be beneficial for patients with PD who are grossly cognitively intact and report little to no depressive symptomatology or functional impairments/reduced QOL caused by their PD symptoms.
As discussed previously, various pilot studies evaluating the efficacy of traditional therapeutic interventions, such as CBT 1,26,33 –35 and cognitive training, 36 –39 and nontraditional interventions, such as active dance therapy, 51 –53 have demonstrated promising preliminary results, including improved mood, cognitive functioning, and QOL. Although self-reported improvements in mood were the primary effects of the PEP intervention, cognitive improvements were noted on selected neuropsychological measures, and participants in all 3 PEP groups self-reported improvements in cognition following the program. As such, PEP is unique in its demonstrated positive effects on both cognitive and emotional functioning. Preliminary results of this pilot feasibility study suggest that participation in a semi-structured recreational program for individuals with PD, such as PEP, may be beneficial in reducing PD-related NMS, such as depression and cognitive functioning, with reduced medical risk and fewer side effects.
Our findings are compelling when considered within the larger context of treatment of cognitive and mood impairments in patients with PD, with significant improvements found on measures of executive functioning (specifically, set-shifting and switching). Although the neurobiological or physiological mechanism through which improvements in cognitive flexibility were achieved remains unclear, previous studies of the effects of aerobic exercise, 54 mindfulness meditation, 55 and various other nonpharmacological interventions on cognitive flexibility have yielded promising hypotheses. Increased physical activity and psychotherapeutic care may be correlated with positive neurophysiological processes, such as enhanced cerebral blood flow and oxygen delivery 56 –58 and increased production of brain-derived neurotrophin factor. 59 –61 Based on these studies and the multidisciplinary nature of PEP, we hypothesize that a similar effect may have occurred. Improvements in cognitive flexibility may have also been secondary to improvements in mood that were observed among PEP participants. 54
There are limitations to this clinical study. Most notably, the small sample size (n = 23) obtained from 3 PEP groups reduces statistical power and external validity. Our sample size was subject to several factors, including the pilot status of the program, the maximum capacity of the PEP groups, and recruitment and retention challenges typical of patients with PD. 62 Additional PEPs should be evaluated to augment sample size and strengthen external validity. Our sample was also ethnically homogenous (87% Caucasian) but was otherwise demographically diverse. This overrepresentation of Caucasian patients reflects the increased prevalence of PD among Caucasian patients compared to their non-Caucasian counterparts demonstrated in the literature, 63 but future research should investigate outcomes of nonpharmacological interventions for more ethnically diverse populations. Variables that may have impacted performance that we did not document or control for include medication changes or concurrent enrollment in another therapeutic program. Psychometric limitations associated with the selected measures are acknowledged; all of the chosen measures are well documented in the literature for reliability and validity. Practice effects may have also affected the cognitive results due to the short test–retest period, but alternate forms were used whenever possible to offset this confound. Finally, as the PEP is a pilot program, it is not manualized. The 3 programs that were evaluated were not identical interventions. However, each 5-week term comprised the same general domains of content and was administered by the same trained personnel, increasing consistency across terms. Manualization of the PEP may address this limitation and facilitate future cross-validation research. Through manualization, the content and structure of the PEP may be adapted to target specific NMS or domains of impairment. Additionally, future research should focus on longer term follow-up outcome studies to determine the longitudinal effects of PEP participation.
There is a clear, demonstrated need for empirically validated interventions to alleviate NMS and improve outcomes in patients with PD. The PEP demonstrated positive preliminary findings of improved cognitive and emotional functioning, with extremely high participant satisfaction. Continued development and evaluation of pilot programs targeted at treating the NMS of PD through nonpharmacological strategies, such as PEP, is needed to maximize the efficacy and participant satisfaction of such interventions and to better serve the PD population.
Footnotes
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: PEP was funded by the Houston Area Parkinson Society (HAPS) and a charitable grant from the Cullen Foundation.