Abstract
Background:
Impulse control disorders and related behaviors (ICDs-RBs) significantly affect the quality of life of Parkinson’s disease (PD) patients. The Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease–Rating Scale (QUIP-RS) was developed to identify and monitor these behaviors. This study aimed to translate and validate the Turkish version of QUIP-RS.
Methods:
The translation process involved back-translation and expert review. Ninety-three patients with PD completed the Turkish QUIP-RS, Movement Disorder Society-Unified PD Rating Scale part III, Hoehn-Yahr stage, Standardized Mini-Mental State Examination, Frontal Assessment Battery, and self-report tools for depression, anxiety, and impulsivity. Internal consistency, factor analysis, convergent and divergent validity were assessed, along with relationships between QUIP-RS domains, clinical features, and dopaminergic medication.
Results:
Eighty-seven patients were included in this analysis. The QUIP-RS’s total Cronbach’s alpha value was 0.925, demonstrating good reliability. Factor analysis showed a good model fit, reflecting different ICDs-RBs domains. Thirty-nine percent of the patients were screened with at least 1 ICDs-RB, 17.2% of participants had single ICDs-RBs, and 21.8% had multiple ICDs-RBs. The most prevalent ICDs-RBs were punding, compulsive eating, and dopamine dysregulation syndrome (DDS). Total levodopa equivalent daily dose (LEDD) was related to only ICD-related behaviors (hobbyism, punding, DDS). In contrast, the dopamine agonist LEDD was significantly correlated with all ICDs-RBs except pathological gambling.
Conclusion:
ICD-RBs are common in the sample recruited fromTürkiye, and the Turkish version of the QUIP-RS is a valid and reliable tool for assessing ICD-RBs in Turkish-speaking groups.
Main Points
A large proportion of patients with Parkinson’s disease (PD) (39%) in this sample had at least 1 impulse control disorder and related behavior (ICD-RB), with the most common being punding (27.6%), compulsive eating (21.8%), and dopamine dysregulation syndrome (19.5%).
Significant correlations were found between ICDs-RBs and treatments used in Parkinson’s disease.
While Total Levodopa Equivalent Daily Dose (LEDD) is significantly correlated with ICD-RBs, Dopamine Agonist Levodopa Equivalent Daily Dose (DA LEDD) is associated with a greater number of ICD-RBs and shows stronger relationships.
The Turkish version of QUIP-RS is a valid and reliable tool to assess ICDs-RBs affecting PD patients’ quality of life.
Introduction
Parkinson’s disease (PD), a multifaceted neurodegenerative disorder characterized by a combination of motor and non-motor symptoms, profoundly affects the quality of life of patients with PD. The cardinal motor symptoms of PD include tremors, rigidity, and bradykinesia. Non-motor symptoms such as anxiety, depression, anhedonia, and impulse control disorders (ICDs) are common in PD.1 ICDs are reward-based and include repetitive, excessive, and compulsive actions motivated by powerful urges, and they are defined as the failure to control the impulse or urge to engage in behavior harmful to self or others.2 Several subtypes of ICDs have been recognized in PD, including pathological gambling, hypersexuality, compulsive shopping, and compulsive eating. Additionally, a spectrum of ICD-related behaviors has been observed, such as hobbyism, which refers to higher-level repetitive extreme engagement in hobbies (excessive exercise, internet use, reading, painting). Punding refers to repetitive, purposeless actions driven by an intense focus on specific objects, such as collecting, arranging, or disassembling them. Dopamine dysregulation syndrome (DDS) is characterized by compulsive overuse of dopaminergic medication beyond therapeutic needs, resembling substance use disorders and leading to addiction-like behavior, mood disturbances, behavioral impairments, and exacerbation of motor symptoms such as dyskinesias and impulse control disorders.3
Patients with PD appear to have an increased risk of developing ICDs compared to healthy controls.3,4 A longitudinal study of ICDs in PD revealed that the prevalence of ICDs increased from 19.7% at the start of the study to 32.8% over a 5-year period, with a 5-year total incidence rate of 45% and multiple ICDs in 6.3%.5 Another study that investigated ICDs in PD reported an ICD prevalence of 29-35% among individuals with PD.6
Dopaminergic medications play a crucial role in PD treatment and are considered among the most effective options, as dopamine agonists and levodopa are considered the primary treatment options. However, concerns have been raised about these drugs due to their relationship with ICDs.5-8 There is a crucial need for clinicians to identify and monitor these symptoms for early detection, aiming to mitigate potentially severe psychosocial and financial consequences in patients with PD. Recognizing these behaviors early allows for timely intervention, such as adjusting medications or incorporating behavioral therapies. For early detection of impulse control disorders and related behaviors (ICDs-RBs), Weintraub et al. (2012) developed the Questionnaire for Impulsive-Compulsive Disorders in PD-Rating Scale (QUIP-RS).9 It is a self-rated scale created to assess a spectrum of ICDs-RBs in PD patients. It enables the detection of ICDs-RBs and follows up on changes in the intensity of symptoms across time. Research spanning various countries and languages, including French, German, Italian, Korean, and Japanese have demonstrated the usability of the questionnaire in both clinical practice and research.10-14 Until recently, there was no validated tool available in the Turkish language to evaluate these ICDs-RBs in PD patients. The objective of this study was to validate the Turkish version of the QUIP-RS and to investigate the relationships between ICDs and various demographic and clinical factors (dopaminergic treatment, dopamine agonist usage, disease duration, and psychiatric and cognitive characteristics).
Materials and Methods
QUIP-RS
Permission from the developer of the scale was obtained to translate the QUIP-RS into Turkish. The translation was performed in 4 steps. Two different researchers independently translated the English version of the questionnaire version into Turkish. The 2 Turkish versions were proofread by the researchers and the supervising professor, and a common Turkish translation was agreed upon. The agreed Turkish version was translated back into English by a native speaker, and the back translation was then compared with the original version. Any discrepancies were addressed and revised through discussion among the research team to produce the final Turkish version.
Population and Sample
As a tertiary reference hospital, Koç University Hospital accepts patients from all socioeconomic groups and all regions of Türkiye, in addition to international patients. Approximately 200-250 patients with parkinsonism are admitted annually to the outpatient unit of this clinic. The inclusion criteria for this study were being over 18 years of age, having a confirmed diagnosis of PD,15 and possessing the ability to provide informed consent. Additionally, participants were required to understand and write in Turkish and be at least primary school graduates. Exclusion criteria were having a diagnosis of atypical parkinsonism diagnosis, dementia, known malignancy, alcohol or substance use disorders, or any disease that may impair cognitive functions, and having a Standardized Mini-Mental State Examination (SMMSE) score of 19 or below. Participants who were unable to read, comprehend, or respond to written questionnaires were also excluded. Overall, 93 patients were recruited between February 2023 and March 2024.
All the participants provided written informed consent. This study was approved by the by Koç University Ethics Committee (2022.315.IRB1.124/28.09.2022) and was conducted according to the principles of the Helsinki Declaration.
Procedure
Patients underwent evaluation while continuing their regular medication regimen and were examined during their ‘On’ state. They were first evaluated by a neurologist for PD-related variables, Movement Disorder Society-Unified PD Rating Scale part III (MDS-UPDRS III), and Hoehn-Yarr stage (H&Y stage). The Standardized Mini-Mental State Examination and the Frontal Assessment Battery (FAB) were administered face-to-face on the same day by trained research assistants. Immediately after the face-to-face assessments, the participant completed the Qualtrics questionnaire on the computer under the monitoring of the research assistant, or if needed, with the help of the research assistant. This questionnaire included socio-demographic characteristics such as age, sex, employment, and education, and self-report scales.
Data Collection Tools
Clinician-Based Assessments:
Pharmacological treatments for PD were noted for each patient by the clinician. For dopaminergic treatment, the total levodopa equivalent daily dose (LEDD) was computed in milligrams, using conversion ratios as follows: standard levodopa multiplied × 1; entacapone × 0.33; tolcapone × 0.5; ropinirole × 20; rasagiline × 100; amantadine × 1; levodopa-carbidopa intestinal gel × 1.10; pramipexole × 100; rotigotine × 30; and selegiline × 10.16 For Dopamine Agonist Levodopa Equivalent Daily Dose (DA LEDD), it was computed with only dopamine agonist treatment milligrams.
Movement Disorder Society-Unified Parkinson’s Disease Rating Scale (MDS-UPDRS III):
It is the most commonly used PD-related scale to assess and monitor disease-related symptoms in patients diagnosed with PD.17,18 Its most important feature is that it is a unified scale that addresses many different aspects of the disease. It evaluates all symptoms of PD, complications of treatment, and activities of daily living of patients with PD. This scale consists of 4 parts. In this study, the third part of the scale, the motor examination, was evaluated by a neurologist trained in the evaluation of this scale. Cronbach’s alpha value for MDS-UPDRS III was reported as 0.92 in the original study17 and calculated as 0.90 in the present study.
Hoehn-Yarr stage (H&Y stage):
The scale examines the disease in 5 stages, and an increase in the stage of the disease on the scale indicates that the disease is progressing to a more advanced stage.19 Stage 0: no signs of disease, stage 1: unilateral signs, stage 2: bilateral involvement but no balance impairment, Stage 3: mild to moderate bilateral signs and some postural instability, but the patient is physically independent and needs assistance to recover on a pull test, Stage 4: significant disability and patients may be able to walk and stand unassisted, Stage 5: the patient is wheelchair-bound or bedridden.
Frontal Assessment Battery (FAB):
The FAB is a widely used test to assess the frontal lobe functions of the brain.20,21 It consists of 6 sections and is scored between 0 and 18. These sections are conceptualization, mental flexibility, programming, interference sensitivity, inhibitory control, and environmental autonomy. Cronbach’s alpha value for FAB was reported as 0.78 in the original study20 and calculated as 0.66 in the present study.
Standardized Mini-Mental State Examination (SMMSE):
The test is organized under the following headings: orientation, working memory, attention, recall memory, language, and visuospatial skills. The version of the SMMSE for educated people was used in this study. The cut-off score of the brief mental examination test for mild or moderate cognitive impairment in Türkiye was determined as 19/20.22,23
Self-report Assessments
Sociodemographic Data Form:
The sociodemographic data form used in the study was developed by the researchers who planned the study and was previously used by another study.24 In this form, patients’ age, education level, sex, marital status, employment status, cigarette and alcohol usage, presence of psychiatric disorder, family history of psychiatric disorder, medications used for PD treatment, other comorbidities, and their treatments were questioned.
QUIP-RS:
Weintraub et al (2012) developed the QUIP-RS.9 It is structured around a set of 4 questions per each of the 7 subdomains, as pathological gambling, hypersexuality, compulsive shopping, compulsive eating, hobbyism, punding, and DDS. Respondents assess using a 5-point Likert scale ranging from 0 to 4. Each subscale’s total score spans from 0 to 16. The total score is scaled from 0 to 112. In this study, patients are identified as positive for each ICDs-RBs based on the cut-off proposed by Probst et al (2014) (pathological gambling ≥3, hypersexuality≥5, compulsive shopping≥5, compulsive eating≥4, punding≥3, hobbyism≥4 and DDS≥3)11 The Cronbach’s alpha value of QUIP-RS was reported as 0.89 in the original study.9
Patient Health Questionnaire-9 (PHQ-9):
Kroenke et al (2001) created the PHQ-9, and it has been used to question depressive symptoms.25,26 It was developed to be a new tool for making criterion-based diagnoses of depression and other mental disorders. The scale has 9 questions scored in the range of 0-3. Cronbach’s alpha value for the PHQ-9 was reported as 0.86-0.89 in the original study25 and calculated as 0.67 in the present study.
Generalized Anxiety Disorder-7 (GAD-7):
Spitzer et al (2006) created the GAD-7 Scale, and it has been used to assess anxiety symptoms.27,28 It was developed as a short clinical scale to assess generalized anxiety disorder. The scale consists of 7 questions scored in the range of 0-3. Cronbach’s alpha value for GAD-7 was reported as 0.92 in the original study27 and calculated as 0.81 in the present study.
Barratt Impulsivity Scale-11 (BIS-11):
Dopamine diseasecale-11 (BIS-11) BIS-11 was developed by Patton et al (1995) to assess impulsivity.29,30 The scale contains 30 items and follows a Likert-type format with items scored ranging from 1 to 4. BIS-11 is the most widely used tool globally for assessing impulsivity. Cronbach’s alpha value for BIS-11 was reported as 0.83 in the original study29 and calculated as 0.73 in the present study.
Statistical Analysis
Statistical analyses were conducted using IBM SPSS Statistics, version 28 (IBM SPSS Corp.; Armonk, NY, USA). Descriptive statistics were gathered for variables such as age, sex, education level, marital status, and employment status, along with SMMSE and FAB scores and self-reported psychometric scales. To assess the reliability of the QUIP-RS, Cronbach’s alpha coefficient (0.70 or higher), item-total score correlation, and Cronbach’s alpha if an item was removed were utilized. The item-total correlation was deemed a critical measure, with a minimum threshold of 0.30, or at least above 0.25. The Kaiser-Meyer-Olkin (KMO) measure and Bartlett’s test were used to evaluate sampling adequacy. An exploratory factor analysis was performed, considering items with factor loadings greater than 0.35. Correlation of QUIP-RS with other clinical characteristics and measures, such as disease duration, total LEDD, DA LEDD, H&Y stage, MDS-UPDRS III, PHQ-9, GAD-7, sMMSE, and FAB, was conducted using the Spearman correlation test for convergent and divergent validity. A p-value below 0.05 was considered significant.
Results
Study Sample
In total, 93 PD patients were evaluated in the study. After data quality control, 3 patients were excluded for not responding reliably to the questionnaire, and another 3 for not completing all scales. Among the 87 PD patients analyzed (44 males, 43 females), the mean age was 66.74±9.81 years (range: 43-87). The mean disease duration was 61.01±49.02 months (range: 1-204), and the MDS-UPDRS III score averaged 20.47±12.06 (range: 4-60). A family history of PD was present in 21.8% (n=19) of the participants, and 27.6% (n=24) of participants had a comorbid psychiatric disorder. Additionally, 11 participants (12.6%) were tobacco users, and 21 (24.1%) were alcohol users. Table 1 provides an overview of the sociodemographic information and clinical characteristics of the sample.
Table 1.
Sociodemographic and Clinical Characteristics of the Sample.
| Sociodemographic Characteristics (n = 87) | Min-Max | Mean (SD) or n (%) |
|---|---|---|
| Age Sex Female Male Marital Status Married Non-married/divorced Employment Active worker Retired-unemployment Education Primary/middle school High school or above | 43-87 | 66.74 (9.81) 43 (49.4) 44 (50.6) 63 (72.4) 24 (27.6) 15 (17.2) 72 (82.8) 33 (38) 54 (62) |
| Clinical characteristics | Min-Max | Mean (SD) or n (%) |
| PD duration (month) MDS-UPDRS III score Hoehn & Yahr stage DA Usage DA LEDD Total LEDD | 1-204 4-60 1-3 0-450 0-1275 | 61.01 (49.02) 20.47 (12.06) 1.75 (0.67) 42 (48.3) 112.989 (145.87) 458.621 (324.71) |
| PHQ-9 (Depression) GAD-7 (Anxiety) BIS-11 (Impulsivity) SMMSE FAB | 0-19 0-20 34-83 19-30 5-18 | 7.39 (4.30) 4.95 (4.39) 54.93 (9.77) 26.77 (2.77) 13.46 (3.11) |
BIS-11, Barratt Impulsivity Scale; DA LEDD, Dopamine Agonist Levodopa equivalent daily dose; FAB, Frontal Battery Assessment; GAD-7, General Anxiety Disorder-7; LEDD, Levodopa equivalent daily dose; MDS-UPDRS III, Movement Disorder Society-Unified Parkinson’s disease rating scale part III; PD, Parkinson’s Disease; PHQ-9, Patient Health Questionnaire-9; SMMSE, Standardized Mini-Mental State Examination.
Internal consistency reliability and exploratory factor analysis
Table 2 shows findings for the internal consistency of the QUIP-RS for all 28 items. The lowest Cronbach’s alpha value for all items was 0.91, and total Cronbach’s alpha values were found to be 0.93.
Table 2.
Internal Consistency Reliability for QUIP-RS All Items, Item-Total Correlation Coefficients, Cronbach’s Alpha Values If Item Deleted, and Total Cronbach’s Alpha Values of All Items
| Item-Total Correlation | Cronbach’s Alpha If Item Deleted | |
|---|---|---|
| 1. How much do you think about the following behaviors (such as having trouble keeping thoughts out of your mind or feeling guilty)? | ||
| Pathological gambling Hypersexuality Compulsive shopping Compulsive eating Hobbyism Punding Dopamine dysregulation syndrome | 0.46 0.61 0.66 0.72 0.60 0.42 0.42 | 0.91 0.91 0.91 0.91 0.91 0.91 0.91 |
| 2. Do you have urges or desires for the following behaviors that you feel are excessive or cause you distress (including becoming restless or irritable when unable to participate in them)? | ||
| Pathological gambling Hypersexuality Compulsive shopping Compulsive eating Hobbyism Punding Dopamine dysregulation syndrome | 0.43 0.57 0.68 0.71 0.47 0.63 0.62 | 0.91 0.91 0.91 0.91 0.91 0.91 0.91 |
| 3. Do you have difficulty controlling the following behaviors (such as increasing them over time or having trouble cutting down or stopping them)? | ||
| Pathological gambling Hypersexuality Compulsive shopping Compulsive eating Punding Hobbyism Dopamine dysregulation syndrome | 0.55 0.63 0.61 0.57 0.66 0.69 0.47 | 0.91 0.91 0.91 0.91 0.91 0.91 0.91 |
| 4. Do you engage in activities specifically to continue the following behaviors (such as hiding what you are doing, lying, hoarding things, borrowing from others, accumulating debt, stealing, or being involved in illegal acts)? | ||
| Pathological gambling Hypersexuality Compulsive shopping Compulsive eating Hobbyism Punding Dopamine dysregulation syndrome | 0.42 0.28 0.42 0.54 0.40 0.33 0.06 | 0.91 0.91 0.91 0.91 0.91 0.91 0.92 |
| Total QUIP-RS | 0.93 | |
QUIP-RS, Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease—Rating Scale; SD, standard deviation.
Table 3 shows findings regarding the internal reliability of the QUIP-RS for 7 domains. Cronbach’s alpha coefficient was 0.88. The lowest Cronbach’s alpha value for all domains was 0.85. The QUIP-RS total, all domains, and items Cronbach’s alpha values exceeded 0.70, the scale's good reliability.
Table 3.
Internal Consistency Reliability for QUIP-RS All Domains, Item-Total Correlation Coefficients, Cronbach’s Alpha Values if Item Deleted, and Total Cronbach’s Alpha Value of all domains
| Item-Total Correlation | Cronbach’s Alpha If Item Deleted | |
|---|---|---|
| Pathological gambling Hypersexuality Compulsive shopping Compulsive eating Hobbyism Punding DDS | 0.45 0.78 0.65 0.75 0.75 0.78 0.57 | 0.88 0.85 0.87 0.85 0.85 0.85 0.87 |
| Total QUIP-RS | 0.88 |
DDS, dopamine dysregulation syndrome; QUIP-RS, Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease—Rating Scale; SD, standard deviation.
*based on QUIP-RS cut-off values (Probst et al., 2014)
Factor Analysis
The principal components analysis was performed, and a 7-factor solution, accounting for 76.20% of the explained variance, was derived using Principal Component Analysis (PCA) with Varimax rotation and Kaiser Normalization, based on the Mineigen criterion (eigenvalues > 1) (Kaiser-Meyer-Olkin measure: 0.736, Bartlett’s Test of Sphericity χ2 = 2113.712, df = 378, P < .001). The Maximum Likelihood Analysis with Varimax with Kaiser Normalization rotation method limited the number of factors to 2, explaining 72.12% of the variance. The result of this test (χ2 = 10.441, df = 8, P = .235) indicates that the model aligns well with the data. Since the P-value is greater than .05, the model fit is considered good. The most consistent factors were overlapping within ICD-related behaviors (hobbyism, punding, and DDS) (factor 1) and ICDs (pathological gambling, hypersexuality, compulsive eating, and compulsive shopping) (factor 2) (Table 4).
Table 4.
Factor Analysis of QUIP-RS Domains
| QUIP-RS Domains | Factor Loading | |
|---|---|---|
| 1 | 2 | |
| Pathological gambling | 0.150 | 0.540 |
| Hypersexuality | 0.449 | 0.518 |
| Compulsive shopping | 0.426 | 0.719 |
| Compulsive eating | 0.391 | 0.786 |
| Hobbyism | 0.966 | 0.257 |
| Punding | 0.719 | 0.436 |
| Dopamine dysregulation syndrome | 0.506 | 0.329 |
QUIP-RS, Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease—Rating Scale; DDS, dopamine dysregulation syndrome.
Extraction Method: Maximum Likelihood. Rotation Method: Varimax with Kaiser Normalization. (Goodnes-of-fit-test: χ2 = 10.441, df = 8, P = .235).
Frequency of ICDs-RBs in the sample
Thirty-nine percent of the patients were identified as positive based on the QUIP-RS results, with pathological gambling (3.4%), hypersexuality (3.4%), shopping (10.3%), compulsive eating (21.8%), hobbyism (13.8%), punding (27.6%), and DDS (19.5%) based on cut-off values.11 While 17.2% of the participants had single ICDs-RBs, 21.8% had multiple ICDs-RBs. The most common ICDs-RBs in both groups were punding, compulsive eating, and DDS. The frequencies of ICDs-RBs in this sample are shown in Figure 1A-D.
Figure 1.
a-d. Pie charts displaying percentages of the prevalence of Impulse Control Disorders and Related Behaviors (ICDs-RBs) in the entire sample (n = 87) (a), in ICDs-RBs positive sample (n=34) (b), in single domain ICDs-RBs positive sample (n=15) (c), and in multiple domain ICDs-RBs positive sample (n=19) (d). Note that specific ICDs-RBs percentages in multi-domain positive charts exceed 100% due to comorbidity.
Convergent and Divergent Validity Analysis of QUIP-RS With Other Psychiatric Scales and Clinical Variables
We investigated the correlations between QUIP-RS and the Barratt impulsivity scale for convergent validity. Significant correlations were found between the BIS-11 and all subdomains except gambling. Additionally, the total LEDD value was only related to ICD-related behaviors, whereas DA LEDD was significantly correlated with all ICDs-RBs except gambling. Similarly, total QUIP-RS scores and some of the domains were correlated with depression and anxiety scale scores. No significant correlation was observed between ICDs-RBs and cognitive scores (SMMSE and FAB) (P >.05). All correlations between QUIP-RS total and domain scores, and sociodemographic and clinical characteristics are shown in Table 5.
Table 5.
Correlation Analysis of QUIP-RS and Clinical Characteristics
| Variables | Pathological Gambling | Compulsive Shopping | Hypersexuality | Compulsive eating | QUIP-ICDs | Hobbyism | Punding | DDS | QUIP-ICD-RBs | QUIP-RS Total | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Age | r (P) | −0.09 P = .394) | −0.11 (P = .312) | −0.44** (P < .001) | −0.20 (P = .063) | −0.18 (P = .095) | −0.13 (P = .246) | −0.01 (P = .917) | −0.26* (P = .014) | −0.14 (P = .198) | −0.19 (P = .078) |
| MDS-UPDRSIII | r (P) | 0.05 (P = .643) | 0.07 (P = .536) | 0.15 (P =.163) | −0.00 (P =.988) | −0.01 (P = .972) | 0.15 (P = .179) | 0.16 (P = .142) | 0.22* (P = .045) | 0.16 (P = 0.141) | 0.08 (P = .446) |
| Duration (m) | r (P) | −0.06 (P = .600) | −0.01 (P = .913) | 0.23* (P =.036) | 0.14 (P =.198) | 0.06 (P = 0.616) | 0.27* (P = .011) | 0.21 (P = .050) | 0.20 (P = .068) | 0.25* (P = .018) | 0.20 (P =.058) |
| Total LEDD | r (P) | −0.01 (P = .984) | 0.20 (P = .069) | −0.03 (P = .802) | 0.05 (P = .674) | 0.05 (P = .634) | 0.29** (P = .006) | 0.33* (P = .002) | 0.36** (P < .001) | 0.39** (P < .001) | 0.26* (P = .016) |
| DA LEDD | r (P) | 0.08 (P = .450) | 0.25* (P = .019) | 0.21* (P = .046) | 0.26* (P = .014) | 0.24* (P = .027) | 0.39** (P < .001) | 0.27* (P = 0.011) | 0.43** (P < .001) | 0.43** (P < .001) | 0.41** (P < .001) |
| PHQ-9 | r (P) | 0.08 (P = .461) | 0.26* (P = .014) | 0.17 (P = .120) | 0.38* (P = .070) | 0.37** (P < .001) | 0.27* (P = .013) | 0.39** (P < .001) | 0.26* (P = .014) | 0.34* (P = .001) | 0.39** (P < .001) |
| GAD-7 | r (P) | 0.16 (P = .137) | 0.26* (P = .016) | 0.29* (P = .006) | 0.26* (P < .001) | 0.32* (P = .003) | 0.22* (P =.041) | 0.33* (P = .002) | 0.26* (P = .015) | 0.33* (P = .002) | 0.36* (P < .001) |
| BIS-11 | r (P) | 0.13 (P = .241) | 0.40* (P < .001) | 0.47** (P < .001) | 0.50** (P < .001) | 0.56** (P < .001) | 0.22* (P = .041) | 0.30* (P =.011) | 0.22* (P = .039) | 0.29* (P = .006) | 0.45** (P < .001) |
| SMMT | r (P) | 0.12 (P = .271) | 0.15 (P = .180) | 0.20 (P = .070) | 0.08 (P = .449) | 0.12 (P = .275) | 0.13 (P = .246) | 0.11 (P = .321) | 0.14 (P = .205) | 0.12 (P = .268) | 0.14 (P = .188) |
| FAB | r (P) | 0.03 (P = .780) | −0.01 (P = .959) | 0.07 (P = .502) | −0.09 (P = .410) | −0.05 (P = .641) | 0.11 (P = .293) | 0.04 (P = .719) | 0.13 (P = .237) | 0.11 (P = .294) | 0.04 (P = .717) |
BIS-11, Barratt Impulsivity Scale; DA LEDD, Dopamine Agonist Levodopa equivalent daily dose; FAB, Frontal Battery Assessment; GAD-7, General Anxiety Disorder-7; LEDD, Levodopa equivalent daily dose; MDS-UPDRS III, Movement Disorder Society-Unified Parkinson’s Disease Rating Scale, part III; PHQ-9, Patient Health Questionnaire-9; QUIP-ICD-RBs, QUIP Impulse Control Disorder-related Behaviors (hobbyism, punding, dopamine dysregulation syndrome); QUIP-ICDs, QUIP Impulse Control Disorders (Pathological gambling, hypersexuality, compulsive shopping, compulsive eating); QUIP-RS, Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Rating Scale; r = Spearman Correlation Coefficient; SMMSE, Standardized Mini-Mental State Examination, *P < .05, **P < .001,
Discussion
In this study, the Turkish version of the QUIP-RS was validated as a reliable tool for evaluating ICDs-RBs in PD patients. It showed high internal consistency, with Cronbach10
Convergent and divergent validity showed strong positive correlations with impulsivity and weak correlations with depression and anxiety, with no relation to cognitive functions. Depression and anxiety are common non-motor symptoms in PD. A multicenter cohort study has reported higher depression and anxiety levels in PD patients with ICD than without ICD.6 The low levels of depression, anxiety, and QUIP-RS correlation coefficients in this study may stem from relatively lower levels of depression and anxiety. This study revealed that impulsivity (BIS-11) is positively and significantly correlated with ICD subdomains. Stronger correlations were found with compulsive shopping, hypersexuality, and compulsive eating than with ICD-related behaviors. Additionally, consistent with previous studies, no significant correlation was found between SMMSE and FAB levels and ICDs-RBs.6,10
In this study, there was a relationship between disease duration and hypersexuality and hobbyism. Previous studies have also reported that prolonged disease duration increases ICDs-RBs by increasing drug exposure.5 A notable positive correlation was observed between total LEDD and DA LEDD, and QUIP-RS total score (r=0.28, P = .016; r=0.41, P <.001, respectively). This suggests that the number of ICDs-RBs increases with increasing LEDD. The correlation between DA LEDD and QUIP-RS had higher coefficients than the total LEDD-QUIP-RS total score correlation. While no significant relationship was found between total LEDD and hypersexuality, compulsive eating, compulsive shopping, significant correlations were found between DA LEDD and hypersexuality, compulsive eating, and compulsive shopping, emphasizing the stronger effect of dopamine agonists. Dopamine agonists can trigger impulsive behaviors by acting on the ventral striatum.31 The ventral striatum is associated with reward-seeking and impulsive behaviors. Currently, pharmacological case-control studies show that ICD-positive patients have higher DA serum concentrations than controls.8 In a recent meta-analysis study, it has been reported that DA usage is related to ICDs-RBs.32 Recent studies have shown that dopamine agonists may trigger impulsive behavior in PD and that genetic polymorphisms associated with dopamine agonists can potentially elevate the risk of impulsive behaviors.33,34
ICDs-RBs are related to dopamine dysfunction and are typically associated most notably dopamine (D3) agonist treatments in PD.35,36 Dopamine agonists can interfere with the natural pauses in D2-family signaling that occur due to the phasic release of endogenous dopamine in the reward-associated ventral striatum.37 A study found that the incidence of ICDs in PD patients is similar to that in non-PD controls before starting dopaminergic drug treatment.38 Patients receiving both DA and levodopa showed a higher prevalence of ICD behaviors.39 In a large sample study, ICDs were more prevalent in patients receiving DA treatment (17.1%) compared to those not receiving DA treatment (6.9%). Additionally, DA treatment in PD was associated with a 2- to 3.5-fold higher risk of developing an ICD.40
In a study, patients who were receiving dopamine agonists at baseline were found to be 5 times more likely to develop any impulse control issues during the follow-up period. Particular risk factors were determined for various forms of ICDs in PD. The likelihood of developing compulsive eating increased 16-fold with dopamine agonist treatment, while punding was linked to higher baseline doses of levodopa and younger age. Male patients were 14 times more likely to experience or develop hypersexuality. Compulsive buying was twice as likely in patients with baseline depression and lower age.41 In this study, there was no significant relationship between age and total QUIP-RS scores and ICD subdomains in general. There was a negative relation between age, hypersexuality, and DDS. In line with the findings, previous studies have also reported that hypersexuality and DDS are more prevalent in younger male patients with PD.42,43
In this study, 39% of participants tested positive for at least 1 impulse control disorder or related behavior. The most frequent ICD-RBs were punding (27.6%), compulsive eating (21.8%), and DDS (19.5%). This rate seems to be consistent with the prevalence of ICD-RBs in PD in previous studies.12,44,45 In this study, 17.2% of the participants had a single domain positive, and 21.8% had multiple domains positive for ICD-RBs. These results of this study are similar to the results in the Italian QUIP-RS validation study.12 An Italian study found that 54% of PD patients had at least 1 impulsive-compulsive disorder, with 22% having 2 or more. The most common symptoms were hobbyism/punding (21%), DDS (20%), compulsive eating (16%), hypersexuality (15%), pathological gambling (13%), and compulsive buying (10%).12 In another study, 12.5% of the patients had ICDs, where compulsive eating was the most frequent (9.3%).10 In addition, many studies have partially overlapped the frequencies of ICDs-RBs.11,13 In this study, the number of participants with pathological gambling (n=3) and hypersexuality (n=3) was low, which may have caused these subdomains to be underrepresented. Different outcomes for ICD frequency and related behaviors may be influenced by disease duration and levodopa dose. Additionally, sample selection methods (selecting patients with ICDs to participate in the study), ICD diagnosis methods (interview-based vs. self-report), and the various scales and cut-off values used in these studies may account for the wide range of reported frequencies. Overall, all these studies underline the high prevalence of ICDs and their importance in the clinical follow-up of patients with PD.
When the sample is compared to other studies in the literature, differences in the sociodemographic properties of the sample are important for comparing the findings. The mean age range of the samples in validation studies conducted in other languages was between 62 and 69 years, while in this study, the mean age was 66.7 years.9-14 While other studies predominantly involved male participants, this study presented a balanced sex ratio of 49.4% male and 50.6% female. The mean disease duration was 5 years in this study compared to 6-10 years in other studies. Other studies reported MDS-UPDRS III scores of 15-25 and H&Y disease stages of 2.2-2.3, whereas this study found scores of 20.5 and 1.8, respectively. Additionally, the LEDD value, DA LEDD value, and DA usage rate in the sample seem to be lower than those reported in other studies. The mean total QUIP-RS score in this study was 8.89 (SD=11.99), with all domains except pathological gambling (0.38) and compulsive shopping (0.68) having mean values above 1. Different studies have reported mean total QUIP-RS values and standard deviations of 2.5 ± 5.0,13 5.1 ± 7.9,10 5.6 ± 9.7,46 6.8 ± 7.9,47 7.2 ± 10.3,14 17.3 ± 17.1,11 and 19.3 ± 18.5.9 In this study, the mean impulsivity value was found to be 55, which is lower than the values reported in 2 other studies.14,38 The mean values for depression and anxiety indicate mild levels of both conditions. Overall, the sample had lower QUIP-RS scores, shorter disease duration, lower rates of DA and total drug dosages, lower impulsivity, and lower levels of depression and anxiety.
While all ICDs-RBs correlated with other variables, pathological gambling did not show this relation, which may be due to the low number of participants who had pathological gambling. Pathological gambling may not have been well-represented in this sample. Future studies should focus on longitudinal analysis and use neurobiological methods to obtain deeper insight into the progression of ICDs-RBs in patients with PD.
This study had several limitations that should be carefully considered when interpreting the findings. The first limitation is the relatively small sample size, which could affect the extent to which the findings can be generalized. The cross-sectional design of the study limits the ability to determine causal relationships between the variables. Longitudinal studies are required to establish causal relationships. Relying on self-reported questionnaires may result in a response bias, as participants could either underreport or overreport their symptoms and behaviors. The absence of clinical interviews for the diagnosis of ICDs may affect the accuracy of the prevalence rates. Cultural differences in the expression and perception of ICDs-RBs were not accounted for, which may affect the applicability of the findings to other cultural contexts. This study did not assess the test-retest reliability of the Turkish version of the QUIP-RS, which is important for determining the stability of the measurement across time.
In conclusion, the Turkish version of the QUIP-RS is a valid and reliable tool for evaluating ICDs-RBs in patients with PD. The high internal consistency and factor structure confirm its suitability for use in both clinical practice and research fields. This tool can help clinicians identify and monitor ICDs-RBs in PD patients, allowing for timely interventions and improved management of these conditions.
Funding Statement
This study was conducted using the services and infrastructure of Koç University Research Center for Translational Medicine (KUTTAM). HYE’s studies are partially supported by Science Academy Turkey. The authors would also like to thank all the patients and participants who contributed to the study.
Footnotes
Ethics Committee Approval: The study was approved by Koç University Committee on Human Research (2022.315.IRB1.124/28.09.2022).
Informed Consent: Written informed consent was obtained from all participants in the format required by the ethics committee.
Peer-review: Externally peer-reviewed.
Author Contributions: Concept – B.Ü., B.C., H.Y.E.; Design – A.B.Ş., B.Ü., B.C., H.Y.E., Ö.Ö.Ç., F.Ö.; Supervision – H.Y.E., F.Ö.; Resources – A.B.Ş., H.Y.E.; Materials – A.B.Ş., B.Ü., B.C., H.Y.E., Ö.Ö.Ç., F.Ö.; Data Collection and/or Processing – A.B.Ş., E.S.Ö., Y.K., M.N.S., R.G., B.Ü., Ö.Ö.Ç., F.Ö., H.Y.E.; Analysis and/or Interpretation – A.B.Ş., E.S.Ö., Y.K., M.N.S., R.G., B.Ü., Ö.Ö.Ç., B.C., F.Ö., H.Y.E.; Literature Search – A.B.Ş., B.Ü., B.C., H.Y.E.; Writing – A.B.Ş., H.Y.E.; Critical Review – A.B.Ş., E.S.Ö., Y.K., M.N.S., R.G., B.Ü., Ö.Ö.Ç., B.C., F.Ö., H.Y.E.
Acknowledgments: University of Pennsylvania holds the copyright to the QUIP-RS, so a licensing agreement with Penn is required for its use in any language, which is without cost for academic use.
Declaration of Interests: The authors declare that they have no conflicts of interest.
Data Availability Statement:
The data in this study are available from the corresponding author upon reasonable request.
References
- 1. Schapira AHV Chaudhuri KR Jenner P. . Non-motor features of Parkinson disease. Nat Rev Neurosci. 2017;18(8):509. (doi: 10.1038/nrn.2017.91) [DOI] [PubMed] [Google Scholar]
- 2. American Psychiatric Association. . Diagnostic and Statistical Manual for Mental Disorders. 5th ed. Washington, DC: American Psychiatric Publishing; 2013. (doi: 10.1176/appi.books.9780890425596) [DOI] [Google Scholar]
- 3. Voon V Fox SH. . Medication-related impulse control and repetitive behaviors in Parkinson disease. Arch Neurol. 2007;64(8):1089 1096. (doi: 10.1001/archneur.64.8.1089) [DOI] [PubMed] [Google Scholar]
- 4. Molde H Moussavi Y Kopperud ST Erga AH Hansen AL Pallesen S. . Impulse-control disorders in Parkinson’s disease: A meta-analysis and review of case-control studies. Front Neurol. 2018;9:330. (doi: 10.3389/fneur.2018.00330) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Corvol JC, Artaud F, Cormier-Dequaire F. Longitudinal analysis of impulse control disorders in Parkinson disease. Neurology. 2018;91(3):e189 e201. (doi: 10.1212/WNL.0000000000005816) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Antonini A Barone P Bonuccelli U Annoni K Asgharnejad M Stanzione P. . ICARUS study: prevalence and clinical features of impulse control disorders in Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2017;88(4):317 324. (doi: 10.1136/jnnp-2016-315277) [DOI] [PubMed] [Google Scholar]
- 7. Binck S, Pauly C, Vaillant M. Contributing factors and evolution of impulse control disorder in the Luxembourg Parkinson cohort. Front Neurol. 2020;11:578924. (doi: 10.3389/fneur.2020.578924) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Staubo SC, Fuskevåg OM, Toft M. Dopamine agonist serum concentrations and impulse control disorders in Parkinson’s disease. Eur J Neurol. 2024;31(2):e16144. (doi: 10.1111/ene.16144) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Weintraub D Mamikonyan E Papay K Shea JA Xie SX Siderowf A. . Questionnaire for impulsive-compulsive disorders in Parkinson’s disease-rating scale. Mov Disord. 2012;27(2):242 247. (doi: 10.1002/mds.24023) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Marques A, Vidal T, Pereira B. French validation of the questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Rating Scale (QUIP-RS). Parkinsonism Relat Disord. 2019;63:117 123. (doi: 10.1016/j.parkreldis.2019.02.026) [DOI] [PubMed] [Google Scholar]
- 11. Probst CC, Winter LM, Möller B. Validation of the questionnaire for impulsive-compulsive disorders in Parkinson’s disease (QUIP) and the QUIP-rating scale in a German speaking sample. J Neurol. 2014;261(5):936 942. (doi: 10.1007/s00415-014-7299-6) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Maggi G, Vitale C, Giacobbe C. Validation of the Italian version of the Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Rating Scale (QUIP-RS) in an Italian Parkinson’s disease cohort. Neurol Sci. 2024;45(7):3153 3161. (doi: 10.1007/s10072-024-07304-2) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Choi JH, Lee JY, Cho JW. Validation of the Korean version of the questionnaire for impulsive-compulsive disorders in Parkinson’s disease rating scale. J Clin Neurol. 2020;16(2):245 253. (doi: 10.3988/jcn.2020.16.2.245) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Takahashi M, Koh J, Yorozu S. Validation of the Japanese version of the questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Rating Scale (QUIP-RS). Parkinsons Dis. 2022;2022:1503167. (doi: 10.1155/2022/1503167) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Postuma RB, Berg D, Stern M. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30(12):1591 1601. (doi: 10.1002/mds.26424) [DOI] [PubMed] [Google Scholar]
- 16. Tomlinson CL Stowe R Patel S Rick C Gray R Clarke CE. . Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord. 2010;25(15):2649 2653. (doi: 10.1002/mds.23429) [DOI] [PubMed] [Google Scholar]
- 17. Goetz CG, Tilley BC, Shaftman SR. Movement Disorder Society-sponsored revision of the Unified Parkinson’s disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord. 2008;23(15):2129 2170. (doi: 10.1002/mds.22340) [DOI] [PubMed] [Google Scholar]
- 18. Akbostanci MC, Bayram E, Yilmaz V. Turkish standardization of movement disorders society unified Parkinson’s disease rating scale and unified dyskinesia rating scale. Mov Disord Clin Pract. 2018;5(1):54 59. (doi: 10.1002/mdc3.12556) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Hoehn MM Yahr MD. . Parkinsonism: onset, progression and mortality. Neurology. 1967;17(5):427 442. (doi: 10.1212/wnl.17.5.427) [DOI] [PubMed] [Google Scholar]
- 20. Dubois B Slachevsky A Litvan I Pillon B. . The FAB: a Frontal Assessment Battery at bedside. Neurology. 2000;55(11):1621 1626. (doi: 10.1212/wnl.55.11.1621) [DOI] [PubMed] [Google Scholar]
- 21. Tunçay N Kayserili G Erhan E Akdede BB Zorlu Y Yener G. . Validation and reliability of the Frontal Assessment Battery (FAB) in Turkish. Front Hum Neurosci. 2008;2:3. [Google Scholar]
- 22. Folstein MF Folstein SE McHugh PR. . “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3):189 198. (doi: 10.1016/0022-3956(75)90026-6) [DOI] [PubMed] [Google Scholar]
- 23. Güngen C Ertan T Eker E Yaşar R Engin F. . Standardize Mini Mental test’in türk toplumunda hafif demans tanisinda geçerlik ve güvenilirliği [Reliability and validity of the standardized Mini Mental State Examination in the diagnosis of mild dementia in Turkish population]. Turk Psikiyatri Derg. 2002;13(4):273 281. [PubMed] [Google Scholar]
- 24. Yapici Eser H Bora HA Kuruoğlu A. . Depression and Parkinson disease: prevalence, temporal relationship, and determinants. Turk J Med Sci. 2017;47(2):499 503. (doi: 10.3906/sag-1603-101) [DOI] [PubMed] [Google Scholar]
- 25. Kroenke K Spitzer RL Williams JB. . The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med. 2001;16(9):606 613. (doi: 10.1046/j.1525-1497.2001.016009606.x) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Sari YE Kokoglu B Balcioglu H Bilge U Colak E Unluoglu I. . Turkish reliability of the patient health questionnaire‐9. Biomed Res. 2016;2016(special issue 1):S460 S462. [Google Scholar]
- 27. Spitzer RL Kroenke K Williams JBW Löwe B. . A brief measure for assessing generalized anxiety disorder: the GAD-7. Arch Intern Med. 2006;166(10):1092 1097. (doi: 10.1001/archinte.166.10.1092) [DOI] [PubMed] [Google Scholar]
- 28. Konkan R Senormanci O Guclu O Aydin E Sungur MZ. . Turkish adaptation, reliability and validity of General Anxiety Disorder-7 Scale. Arch Neurol Psychiatry. 2013;50(1):53 58. [Google Scholar]
- 29. Patton JH Stanford MS Barratt ES. . Factor structure of the Barratt impulsiveness scale. J Clin Psychol. 1995;51(6):768 774. (doi: ) [DOI] [PubMed] [Google Scholar]
- 30. Gulec H Tamam L Yazici GM Turhan M Karakus G Zengin M. . Psychometric properties of the Turkish version of the Barratt impulsiveness Scale-11. Bull Clin Psychopharmacol. 2008;18:251 258. [Google Scholar]
- 31. MacDonald HJ Ruitenberg MFL. . Dopamine system involvement in impulse control. Exp Brain Res. 2024;242(4):781 782. (doi: 10.1007/s00221-023-06775-7) [DOI] [PubMed] [Google Scholar]
- 32. Soileau LG, Talbot NC, Storey NR. Impulse control disorders in Parkinson’s disease patients treated with pramipexole and ropinirole: a systematic review and meta-analysis. Neurol Sci. 2024;45(4):1399 1408. (doi: 10.1007/s10072-023-07254-1) [DOI] [PubMed] [Google Scholar]
- 33. Fedosova A Titova N Kokaeva Z Shipilova N Katunina E Klimov E. . Genetic markers as risk factors for the development of impulsive-compulsive behaviors in patients with Parkinson’s disease receiving dopaminergic therapy. J Pers Med. 2021;11(12):1321. (doi: 10.3390/jpm11121321) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34. Toś M Grażyńska A Antoniuk S Siuda J. . Impulse control disorders in the polish population of patients with Parkinson’s disease. Medicina (Kaunas). 2023;59(8):1468. (doi: 10.3390/medicina59081468) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35. Fusaroli M, Giunchi V, Battini V. Exploring the underlying mechanisms of drug-induced impulse control disorders: a pharmacovigilance-pharmacodynamic study. Psychiatry Clin Neurosci. 2023;77(3):160 167. (doi: 10.1111/pcn.13511) [DOI] [PubMed] [Google Scholar]
- 36. Carbone F Djamshidian A. . Impulse control disorders in Parkinson’s disease: an overview of risk factors, pathogenesis and pharmacological management. CNS Drugs. 2024;38(6):443 457. (doi: 10.1007/s40263-024-01087-y) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Hirschbichler ST Rothwell JC Manohar SG. . Dopamine increases risky choice while D2 blockade shortens decision time. Exp Brain Res. 2022;240(12):3351 3360. (doi: 10.1007/s00221-022-06501-9) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38. Antonini A, Siri C, Santangelo G. Impulsivity and compulsivity in drug-naïve patients with Parkinson’s disease. Mov Disord. 2011;26(3):464 468. (doi: 10.1002/mds.23501) [DOI] [PubMed] [Google Scholar]
- 39. Antonini A, Stoessl AJ, Kleinman LS. Developing consensus among movement disorder specialists on clinical indicators for identification and management of advanced Parkinson’s disease: a multi-country Delphi-panel approach. Curr Med Res Opin. 2018;34(12):2063 2073. (doi: 10.1080/03007995.2018.1502165) [DOI] [PubMed] [Google Scholar]
- 40. Weintraub D, Koester J, Potenza MN. Impulse control disorders in Parkinson disease: a cross-sectional study of 3090 patients. Arch Neurol. 2010;67(5):589 595. (doi: 10.1001/archneurol.2010.65) [DOI] [PubMed] [Google Scholar]
- 41. Weintraub D, Simuni T, Caspell-Garcia C. Cognitive performance and neuropsychiatric symptoms in early, untreated Parkinson’s disease. Mov Disord. 2015;30(7):919 927. (doi: 10.1002/mds.26170) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42. Barbosa PM Grippe T Lees AJ O’Sullivan S Djamshidian A Warner TT. . Compulsive sexual behaviour in Parkinson’s disease is associated with higher doses of levodopa. J Neurol Neurosurg Psychiatry. 2018;89(10):1121 1123. (doi: 10.1136/jnnp-2017-317298) [DOI] [PubMed] [Google Scholar]
- 43. Warren N O’Gorman C Lehn A Siskind D. . Dopamine dysregulation syndrome in Parkinson’s disease: a systematic review of published cases. J Neurol Neurosurg Psychiatry. 2017;88(12):1060 1064. (doi: 10.1136/jnnp-2017-315985) [DOI] [PubMed] [Google Scholar]
- 44. Wang XP Wei M Xiao Q. . A survey of impulse control disorders in Parkinson’s disease patients in Shanghai area and literature review. Transl Neurodegener. 2016;5:4. (doi: 10.1186/s40035-016-0051-7) [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45. Maréchal E Denoiseux B Thys E Cras P Crosiers D. . Impulsive-compulsive behaviours in Belgian-Flemish Parkinson’s disease patients: A questionnaire-based study. Parkinsons Dis. 2019;2019:7832487. (doi: 10.1155/2019/7832487) . [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Rodríguez-Violante M González-Latapi P Cervantes-Arriaga A Camacho-Ordoñez A Weintraub D. . Impulse control and related disorders in Mexican Parkinson’s disease patients. Parkinsonism Relat Disord. 2014;20(8):907 910. (doi: 10.1016/j.parkreldis.2014.05.014) [DOI] [PubMed] [Google Scholar]
- 47. Guerra DF, Lemos Silva AE, Paz TDSR. Measurement properties from the Brazilian Portuguese version of the QUIP-RS. NPJ Parkinsons Dis. 2020;6:6. (doi: 10.1038/s41531-020-0108-2) [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data in this study are available from the corresponding author upon reasonable request.

Content of this journal is licensed under a 