Journal of Parkinson’s Disease 7 (2017) 183–191
DOI 10.3233/JPD-160977
IOS Press
183
Research Report
Impulsive and Compulsive Behaviors
in Parkinson’s Disease: The Norwegian
ParkWest Study
Aleksander H. Erga
a,∗
, Guido Alves
a,b
, Jan Petter Larsen
c
, Ole Bjørn Tysnes
d
and Kenn Freddy Pedersen
a,b
a
The Norwegian Centre for Movement Disorders, Stavanger University Hospital, Stavanger, Norway
b
Department of Neurology, Stavanger University Hospital, Stavanger, Norway
c
Network for Medical Sciences, University of Stavanger, Stavanger, Norway
d
Department of Neurology, Haukeland University Hospital, Bergen, Norway
Accepted 28 October 2016
Abstract.
Background: Impulsive and compulsive behaviors (ICBs) are frequent in Parkinson’s disease (PD), but data from population-
based cohorts is lacking.
Objectives: To determine the frequency and associated demographic, clinical, neuropsychiatric and cognitive features of
ICBs in a population-based PD cohort.
Methods: This cross-sectional study included 125 patients with PD and 159 age- and gender-matched normal controls
recruited from the Norwegian ParkWest study. Participants underwent comprehensive neurological, neuropsychiatric and
neuropsychological assessments. ICBs were assessed using the Questionnaire for Impulsive-Compulsive Disorders in PD
short form. Multiple logistic regression analyses were performed to compare the odds of ICBs between groups and to identify
independent correlates of ICBs in PD.
Results: 30.4% of patients reported at least one ICB, with an odds ratio (OR) of 3.2 (95% confidence interval [CI] 1.8–5.9)
compared with controls. Multiple ICBs were experienced by 8.8% of patients vs 1.3% of controls (OR 7.6, 95% CI 1.7–34.8).
Compared to controls, the ORs of having an ICB were 7.4 (95% CI 2.6–20.9) in patients taking DA without levodopa, 4.6
(95% CI 2.3–9.3) in those treated with both DA and levodopa, and 1.2 (95% CI 0.5–3.2) in patients using levodopa but not DA.
In multivariate models, ICB status in patients was independently associated with DA treatment and depressive symptoms,
but not with other dopaminergic medications, motor function, or cognitive performance.
Conclusions: Patients with PD treated with DA, but not other dopaminergic medications, have increased odds of having
ICBs compared with age- and gender-matched controls. This has implications for individualized patient management and
follow-up.
Keywords: Parkinson’s disease, impulse control disorders, QUIP, dopamine agonists, neuropsychiatry
∗
Correspondence to: Aleksander H. Erga, MSc, The Norwegian
Centre for Movement Disorders, Stavanger University Hospital;
P.O. Box 8100, N-4068 Stavanger, Norway. Tel.: +47 51515288;
Fax: +47 51515515; E-mail: aleksander.erga@gmail.com.
INTRODUCTION
Impulsive-compulsive behaviors (ICBs) are recog-
nized as serious neuropsychiatric complications in
Parkinson disease (PD), with potentially devastating
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184 A.H. Erga et al. / Impulsive and Compulsive Behaviors in PD
personal, social and financial consequences [1, 2].
These abnormal behaviors include the four major
impulse control disorders (ICD) pathological gam-
bling, compulsive shopping, binge eating and
hypersexuality [1]. These behaviors are ego-syntonic
and impulsive in nature, characterized by an effort to
obtain arousal and gratification and cognitive biases
[3–5]. In addition, a range of related behaviors have
been described in PD, including punding, hobbyism,
walkabout and compulsive dopaminergic medication
overuse [6]. The related ICBs are ego-dystonic and
compulsive in nature, associated with a calming or
anxiolytic effect on the patient [5, 6].
Reported prevalence estimates of ICBs in PD
vary considerably, ranging from 6% to almost 35%
[1, 7]. Potential explanations include differences in
the definition and assessment of ICBs, dopaminergic
treatment, and patient selection, with most studies
performed at highly-specialized movement disorders
centers. In addition, since only few studies included
normal control subjects, little is known about the
risk of ICBs in PD relative to the general population
[8–10]. Such information would, however, be impor-
tant given that social, cultural and economic factors
are likely to influence the prevalence of ICBs.
ICBs in PD have been associated most consis-
tently with dopaminergic medication, and dopamine
agonist (DA) treatment in particular [9, 11]. Other
proposed determinants include premorbid personal-
ity traits, younger age, male gender, and depression
and anxiety [12]. However, evidence in this respect
is not unequivocal and even less clear for a range
of other features within the spectrum of motor and
non-motor symptoms associated with PD.
Against this background, we investigated the risk
and determinants of ICDs and related impulsive-
compulsive behaviors in a population-based PD
cohort and normal controls (NCs) using compre-
hensive and standardized assessments of ICBs, as
well as neurological, neuropsychiatric and cognitive
functioning.
MATERIALS AND METHODS
Study design and participants
All participants were derived from the Norwegian
ParkWest project, a population-based longitudinal
study of the incidence, neurobiology and prognosis of
PD. Details of the case ascertainment and diagnostic
procedures to recruit a population-representative PD
cohort have been published elsewhere [13]. Briefly,
patients with newly diagnosed PD and NC sub-
jects were recruited from four counties in Western
and Southern Norway between 2004 and 2006, and
followed prospectively by movement disorders neu-
rologists with standardized clinical examinations.
Assessment of ICBs was introduced at the 5 year re-
examination, in which 155 patients with PD and 159
NCs participated. Of these, we excluded 28 patients
and 1 control subject due to dementia [14, 15]. Thus,
125 non-demented PD patients and 159 NC subjects
were eligible for this cross-sectional study of ICBs
in PD. All PD patients met the National Institute of
Neurological Disorders and Stroke and the United
Kingdom PD Society Brain Bank criteria for PD
[16, 17]. All participants were Caucasian.
Standard protocol approvals, registrations,
and patient consents
The study was approved by the Regional Com-
mittee for Medical and Health Research Ethics,
Western Norway. Signed written informed consent
was obtained from all participants.
Assessments
A standardized examination program was admin-
istered by trained members of the ParkWest study
group. Information regarding demographic variables,
lifestyle factors, clinical history, and medication was
obtained during semistructured interviews. Motor
severity and disease stage were assessed by the Uni-
fied PD Rating Scale (UPDRS) and Hoehn and Yahr
scale. Levodopa equivalent doses (LEDs) were calcu-
lated according to published recommendations [18].
For assessment of ICBs, the self-report short
form version of the Questionnaire for Impulsive-
Compulsive Disorders in PD (QUIP) was completed
by all participants [19]. The QUIP is designed to
detect clinically significant impulse control disorders
(compulsive gambling, sexual behavior, shopping
and eating) and related impulsive-compulsive behav-
iors (punding, hobbyism, walkabout, and compulsive
use of dopaminergic medication), and has been
demonstrated to be a valid self-assessment screen-
ing instrument for ICBs in patients with PD [20].
Participants with positive response to one or more
screening questions of the QUIP were classified to
have ICB [20].
Cognitive function was assessed using the Mini-
Mental State Examination (MMSE) as a measure of
global cognition [21]. In addition, a comprehensive
A.H. Erga et al. / Impulsive and Compulsive Behaviors in PD 185
neuropsychological test battery [Stroop test [22],
Semantic verbal fluency test [23], California Verbal
Learning Test II (CLVT-II) [24], and Silhouettes and
Cube subtests of the Visual Object and Space Per-
ception Battery (VOSP) [25]] was administered by
trained study nurses to assess a wide range of cog-
nitive domains: attention (Stroop word reading and
color naming), executive functioning (Semantic ver-
bal fluency, Stroop interference condition), verbal
memory (CVLT-II), and visuospatial skills (VOSP).
A diagnosis of PD dementia (PDD) was determined
according to published criteria [14], as described pre-
viously [26].
Neuropsychiatric symptoms were assessed using
the 12-item version of the Neuropsychiatric Inventory
(NPI) [27]. A composite score (product of frequency
and severity; range 0–12) was calculated for each neu-
ropsychiatric symptom. The validity of the NPI has
been established [27], and high reliability in PD has
been reported [28]. In addition, more comprehensive
assessments of depressive symptoms, daytime sleepi-
ness, and night-time sleep problems were performed
using the Montgomery and Aasberg Depression Rat-
ing Scale (MADRS) [29], the Epworth Sleepiness
Scale [30], and the PD Sleep Scale [31]. To identify
possible subcomponents of depressive symptoms, we
applied a three-factor model of MADRS as suggested
by Suzuki et al. [32].
Statistical methods
All statistical procedures were performed using
IBM SPSS Statistics version 22. Group differences
were analysed using t tests, Mann–Whitney tests, χ
2
tests and Fisher exact tests as appropriate. Logistic
regression analyses (enter method) without and with
adjustment for potential confounders (age, gender,
MADRS and MMSE-scores) were used to compare
the risk of ICBs in patients with PD vs controls,
expressed as odds ratios (ORs) with 95% con-
fidence intervals (CIs). Since the unadjusted and
adjusted analyses yielded similar results, unadjusted
OR and CI are reported in the manuscript. Multi-
variate logistic regression analysis (enter method)
was also applied to assess independent correlates of
ICBs in patients with PD. For this purpose, vari-
ables attaining a significance level of p < 0.10 in
univariate analyses were considered for inclusion as
independent variables in multivariate models, with
the presence or absence of ICBs as the dependent
variable. Two-tailed p values < 0.05 were considered
statistically significant.
RESULTS
Participant characteristics
Patients with PD had slightly lower MMSE and
higher MADRS scores than age- and gender-matched
NCs, but there were no between-group differences
regarding lifestyle factors, daytime sleepiness, or
night-time sleep problems (Table 1).
Frequency of ICBs
The frequencies of ICDs and related behaviors in
patients and controls are illustrated in Fig. 1. Overall,
30.4% (38/125) of patients and 11.9% (19/159) of
controls reported at least one ICB, yielding an OR
of 3.2 (95% CI 1.8–5.9; p < 0.001). Multiple ICBs
were reported by 8.8% of patients (28.9% of those
with ICBs) compared with 1.3% of controls (10.5%
of controls with ICBs). The corresponding OR for
multiple ICBs was 7.6 (95% CI 1.7–34.8; p = 0.009).
ICDs were reported by 20.8% (26/125) of patients
and 5.7% (9/159) of controls (OR 4.4, 95% CI
2.0–9.7; p < 0.001). The frequencies of ICD subtypes
in patients vs controls were as follows: compulsive
gambling 1.6% vs. 0.6%, hypersexuality 5.6% vs.
0.6%, compulsive shopping 4.8% vs. 2.5%, and com-
pulsive eating 11.2% vs. 2.5%.
Related impulsive-compulsive behaviors were
reported by 16.8% (21/125) of patients and 7.5%
(12/159) of controls (OR 2.5, 95% CI 1.3–5.3;
p = 0.018). The frequencies of related behavior sub-
types in patients vs. controls were as follows: punding
9.6% vs. 5.0%, hobbyism 10.4% vs. 4.4%, walkabout
Table 1
Characteristics of patients with PD and normal controls
Characteristics PD patients Normal controls P value
(N = 125) (N = 159)
Male, n (%) 75 (60.0%) 81 (50.9%) 0.128
Age, y 70.3 (9.4) 70.8 (9.0) 0.674
Smoking
a
, n (%) 16 (12.8) 17 (10.7) 0.161
Alcohol use
a
, n (%) 86 (68.8) 119 (74.8) 0.259
MMSE score 27.8 (2.5) 28.7 (1.5) 0.001
MADRS score 3.8 (4.4) 1.5 (2.9) 0.001
ESS score 5.8 (4.0) 6.5 (4.4) 0.244
PDSS score 124.7 (17.5) 123.6 (17.3) 0.597
Duration of PD, y 7.4 (1.8) – –
UPDRS motor score 22.7 (10.6) – –
Hoehn and Yahr stage 2.2 (0.6) – –
MMSE = Mini-Mental Status Examination; MADRS =
Montgomery and Aasberg Depression Rating Scale; ESS =
Epsworth Sleepiness Scale; PDSS = Parkinson’s Disease Sleep
Scale. Data are mean (SD) unless otherwise indicated.
a
Previous
or current use. Bold values indicate significant P-value.
186 A.H. Erga et al. / Impulsive and Compulsive Behaviors in PD
Fig. 1. Frequencies of ICBs among patients with PD and normal controls. ICB = Impulsive-compulsive behavior; PD = Parkinson disease;
ICD = Impulse control disorder. Group differences are indicated by significance levels.
4.0% vs. 0.6%, and compulsive dopaminergic medi-
cation use 2.4% vs. 0%. We did not identify a gender
difference between patients with the different ICB
types.
Demographic and clinical correlates
Patients with ICBs were younger than patients
without ICBs (p = 0.054), but there were no between-
group differences in gender distribution, lifestyle
factors, disease duration, motor severity, disease
stage, daytime sleepiness or night-time sleep prob-
lems (Table 2). No patients had a history of deep brain
stimulation.
Neuropsychiatric and neuropsychological
correlates
Compared to patients without ICBs, those with
ICBs had higher MADRS total scores and MADRS
subscores related to dysphoria and retardation
(Table 2). In addition, NPI items regarding depres-
sion, agitation, apathy, and irritability were more
common in patients with than without ICBs (Table 3).
In contrast, there were no significant between-group
differences in global cognition or neuropsycholog-
ical measures of attention, executive functioning,
verbal memory, or visuospatial abilities (Supple-
mental Table). Supplemental analyses including only
patients on DA treatment (n = 78) yielded similar
results (data not shown).
Medication effects
There were no differences in monoaminooxidase-
B inhibitor (MAO-B) use, levodopa use or dose, DA
LED, or total LED between patients with or with-
out ICBs (Table 2). However, patients with ICBs
were more likely to use DA than those without
ICBs.
The distribution of ICBs stratified by treatment is
summarized in Table 4. The highest frequency was
observed among patients using DA only (50%), fol-
lowed by those on both DAs and levodopa (38.3%),
and patients taking levodopa but not DAs (13.9%).
Compared to controls, the corresponding ORs were
7.4 (95% CI 2.6–20.9; p < 0.001) for those on DAs
only and 4.6 (95% CI 2.3–9.3; p < 0.001) for com-
bination users. Patients using levodopa only had
no increased odds of ICBs compared to controls
(OR = 1.2; 95% CI 0.5–3.2; p = 0.723). Compared
to patients with a single ICB, patients with multiple
ICBs did not use higher dosage of dopamine agonist
(t = 1.20, P = 0.240).
Combined analysis
A multivariate model with ICB status as dependent
variable and age, MADRS score, and DA treat-
ment as independent variables, showed significant
effects for higher MADRS score (OR 1.2, 95% CI
1.1–1.3; p = 0.001) and DA treatment (OR 6.4, 95%
CI 2.0–20.4; p = 0.001), but not age (OR 1.0, 95% CI
0.9–1.0; p = 0.429).
A.H. Erga et al. / Impulsive and Compulsive Behaviors in PD 187
Table 2
Clinical and demographic characteristics of patients with and without ICBs
Characteristics ICB positive (n = 38) ICB negative (n = 87) P value
Demographic
Male, n (%) 26 (68.4) 49 (56.3) 0.204
Age, y 67.9 (7.7) 71.4 (9.8) 0.054
Smoking
a
, n (%) 7 (18.4) 12 (13.8) 0.507
Alcohol use
a
, n (%) 26 (68.4) 64 (73.5) 0.556
Clinical
Duration of PD, y 7.4 (1.6) 7.4 (1.9) 0.367
UPDRS motor score 23.8 (10.5) 22.2 (10.7) 0.381
Hoehn and Yahr stage 2.2 (0.5) 2.2 (0.6) 0.598
MMSE score 28.4 (1.8) 27.5 (2.8) 0.108
MADRS score 5.4 (5.1) 3.1 (3.9) 0.009
Dysphoria subscore 1.0 (1.4) 0.4 (0.9) 0.003
Retardation subscore 2.6 (2.4) 1.4 (2.1) 0.006
Vegetative subscore 1.8 (1.3) 1.3 (2.0) 0.292
ESS score
d
5.6 (5.1) 5.9 (3.5) 0.283
PDSS score
d
121.8 (22.5) 126.0 (14.5) 0.775
Medication
DA use, n (%) 32 (84.2) 46 (52.9) 0.001
Levodopa use, n (%) 29 (76.3) 74 (85.1) 0.238
Total LED
b
730.6 (343.3) 658.4 (275.9) 0.522
DA LED
b
293.7 (132.4) 289.5 (150.0) 0.896
Levodopa dose
c
505.2 (279.1) 408.7 (266.7) 0.107
MAO-B use 13 (34.2) 31 (35.6) 0.878
Antidepressant use, n (%) 5 (13.2) 11 (12.6) 0.937
MMSE = Mini-Mental Status Examination; MADRS = Montgomery and Aasberg Depression
Rating Scale; ESS = Epsworth Sleepiness Scale; PDSS = Parkinson’s Disease Sleep Scale;
DA = Dopamine agonist; LED = Levodopa equivalent dose; MAO-B = Monoaminooxidase-B
inhibitor. Data are mean (SD) unless otherwise indicated.
a
Previous or current use.
b
Among DA
users. Patients using only levodopa (n = 43) excluded.
c
Among levodopa users. Patients using
only DA (n = 18) excluded.
d
N = 102. Bold values indicate significant P-value.
Table 3
Neuropsychiatric characteristics in patients with and without ICBs
NPI item NPI score, mean (SD) Proportion with positive NPI score, n (%) P value
a
ICB positive (n = 34) ICB negative (n = 71) ICB positive (n = 34) ICB negative (n = 71)
Delusions 0.1 (0.7) 0.0 (0.4) 2 (5.9) 1 (1.4) 0.244
Hallucinations 0.1 (0.3) 0.1 (0.8) 1 (2.9) 3 (4.2) 0.999
Agitation 0.7 (1.9) 0.2 (0.8) 8 (23.5) 5 (7.0) 0.028
Depression 1.4 (2.3) 0.4 (1.3) 16 (47) 11 (15.5) 0.001
Anxiety 0.4 (1.1) 0.2 (0.9) 4 (11.8) 5 (7.0) 0.467
Euphoria 0.0 (0.2) 0.0 (0.0) 1 (2.9) 0 (0.0) 0.324
Apathy 1.3 (2.2) 0.6 (1.6) 11 (32.4) 10 (14.1) 0.029
Disinhibition 0.2 (0.7) 0.2 (1.1) 4 (11.8) 3 (4.2) 0.210
Irritability 0.9 (2.0) 0.1 (0.4) 9 (26.5) 7 (9.9) 0.027
Aberrant motor behavior 0.3 (1.4) 0.0 (0.0) 2 (5.9) 0 (0.0) 0.105
Sleep disturbance 2.8 (3.1) 1.6 (2.4) 17 (50.0) 29 (40.8) 0.337
Appetite disturbance 2.0 (3.4) 1.2 (2.7) 11 (32.4) 14 (19.7) 0.155
NPI total 10.8 (9.3) 4.8 (5.8) 28 (82.4) 43 (60.6) 0.021
ICBs = Impulsive-compulsive behaviors; NPI = Neuropsychiatric Inventory. NPI data missing in 4 with ICB and 16 without ICB.
a
χ
2
test.
Bold values indicate significant P-value.
Table 4
Frequency and odds of ICBs in patients stratified by treatment
Characteristics DA only users (n = 18) DA and levodopa users (n = 60) Levodopa only users (n = 43)
ICB positive, n (%) 9 (50.0) 23 (38.3) 6 (13.9)
Multiple ICBs, n (%) 3 (16.6) 7 (11.6) 1 (2.3)
OR
∗
for any ICB, (95% CI) 7.4 (2.6–20.9) 4.6 (2.3–9.3) 1.2 (0.5–3.2)
Bold indicates significance (p < 0.05). ICBs = Impulsive-compulsive behaviors; OR = Odds ratio; DA = Dopamine agonist.
∗
Compared to
controls (n = 159).