Introduction

Parkinson’s disease (PD) represents the second most common neurodegenerative disorder after Alzheimer’s disease, with a prevalence of 1–2% in those over the age of sixty and 3–5% in those over 85 years old [1, 2]. Symptoms mainly involve movement, so that PD’s most well-known signs are tremor, bradykinesia, muscle stiffness and impaired balance and coordination. Nonetheless, there is well-established evidence that cognition and emotion are also impaired, with psychiatric symptoms being present in more than 60% of PD patients [3]. Among the non-motor symptoms, concern has arisen for a peculiar group of impulsive behaviors, known as Impulse Control Disorders (ICDs), which occur in up to 20% of PD patients [4]. ICDs are a group of behaviors characterized by a failure to resist an impulse, drive, or temptation to perform an act that is harmful to oneself or to others [5]. They include pathological gambling [6], hypersexuality [7], compulsive eating [8], and compulsive buying [9]. Along with them, other related impulsive-compulsive behaviors occur, including punding [10], hobbyism [11], walkabouts [12], and a peculiar condition named Dopamine Dysregulation Syndrome (DDS), defined as a compulsive use of dopamine medications despite adequate motor benefits and the annoying consequences [13].

Although evidence of ICDs in PD patients has been reported even before [14], research on this topic flourished in the 2000s, when many studies found that PD patients reported those impulsive behaviors though they had never experienced them prior to the disease [15–18]. The first case studies led to the hypothesis that the onset of those peculiar behaviors may be due to the pharmacological dopaminergic therapy used to treat PD, particularly of dopamine agonists [19, 20]. Evidence of the link between ICDs and dopaminergic therapy is provided by distinct aspects: 1) prevalence rates of ICDs seem to be higher in patients with PD rather than in the general population; for example, lifetime prevalence rates are between 3% and 8% for pathological gambling in PD versus a 0.3% to 2% rate in the latter [20–22]; 2) prevalence rates are even higher in PD patients using dopamine agonists, with an estimate of 13.7% [23]; 3) rates of pathological gambling are high also in other medical conditions that require the use of dopamine agonists [24, 25]. Referring to the onset time of ICDs, though almost all studies examining ICDs in PD have been cross-sectional, a recent prospective study found that 39% of patients developed an ICD within four years from the initiation of the dopaminergic treatment, though they had never experienced them before [26].

One possible explanation for the association between ICDs and dopaminergic therapy in PD patients is the “overstimulation hypothesis” in the ventral striatum [22, 27], that is ICDs may result from an excessive dopaminergic stimulation of those areas involved in the reward system. While dopaminergic loss in PD affects above all the dorsal striatum, responsible for movements, the ventral striatum, which regulates reward responsiveness, remains relatively intact, especially in the early stages. As such, though providing substantial benefits to motor symptoms, dopaminergic treatment may increase reward sensitivity and promote the onset of the ICDs [27, 28].

As previously mentioned, dopamine agonists seem to be strongly associated with the development of ICDs–though a lesser association was also found with high doses of levodopa [4]. This may be because, compared to levodopa, most dopamine agonists have a preferential selectivity for D3 and D2 receptors rather than D1 type [29]: while D1 receptors are mostly concentrated in dorsal striatum, where they facilitate motor function, D2-like receptors are set in the limbic areas, including ventral striatum, where they play an important role in reward and addiction circuits. Hence, dopamine agonists may activate limbic mechanisms more than motor ones.

However, dopaminergic treatment cannot be considered as the only factor responsible for ICDs in PD. In fact, though a considerable percentage of PD patients experiences at least one ICD, they represent a minority of the PD patients that are treated with dopaminergic medication [27], so other responsible factors have been proposed [28, 30]. Some of them are related to PD, such as an earlier onset of the disease, whereas some others refer to personal factors, including a familiar history of addictions, male gender, and, above all, personality traits. Among them, impulsivity is one of the main suspects [30–32].

PD patients suffering from ICDs have greater functional impairment in activities of daily living compared with PD controls [4, 19]. In fact, ICDs usually predict reduced quality of life, mainly in terms of emotional well-being, with the presence of depressed mood and/or irritability [33, 34]. They are also associated with increased social impairment, including divorce, bankruptcy, incarceration, and attempted suicide [35, 36]. Nevertheless, ICDs in PD patients tend to be under-recognized and under-managed in clinical practice [20, 33, 37]. Under-recognition may be attributed both to the fact that patients may under-report symptoms, and that routine screening is not common [4]. In fact, precisely screening for impulsive behaviors using psychometrically-based tools does not usually represent a standard procedure, since, in clinical practice physicians often ask about ICDs but do not commonly use more comprehensive screening tools. Yet, case reports suggest that ICDs often resolve after reducing the dose of the existing DA, even when compensating with an increase in levodopa dosage [38, 39]. Thus, testing the presence of those impulsive behaviors may be crucial for making adjustments to the treatment plan.

As such, the use of psychometrically-based instruments aiming to assess the presence of these aspects–and, if present, their frequency and severity–is highly recommended during the diagnostic process and the clinical evaluation, as to develop a case-by-case strategy of intervention. In support of the increasing interest towards the instruments assessing ICDs, a recent semi-systematic review reported a non-exhaustive list of some existing tools and described their main features, though it did not report any information about their psychometric properties [40]. Nonetheless, not all the existing instruments aiming to assess the same clinical feature are equally good in terms of psychometric properties; that is, there may be differences in terms of their ability to effectively and precisely measure the considered aspect. As so, to be aware of the quality of the tool before administering it, the analysis of its measurement properties would be needed.

Given the huge interest in assessing ICDs in PD patients, the aim of the present work was to systematically review the psychometric properties of the instruments used in research and practice in patients with PD. In detail, the specific aims of this study were fourfold: 1) to provide a list of the instruments assessing multiple ICDs, whose psychometric properties have been investigated in PD patients–starting with the consideration that routine screening of ICDs in PD patients is not common [4], aiming to practically help clinicians in easily, rapidly evaluating the presence of these behaviors, we decided to focus only on those instruments that assessed more than one ICD at the same time; 2) to provide information on their specific psychometric characteristics; 3) to qualitatively assess the detected instruments in light of their psychometric properties; and 4) to assess the methodological quality of the included studies. In sum, this systematic review aimed to increase knowledge about the psychometric properties of instruments assessing ICDs in PD, thus identifying potential areas for improvement and further developments in this field from a psychometric perspective.

Materials and methods

Methods of this systematic review were specified before starting the study according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Guidelines [41]. The methods are specified as follows.

Quality assessment

Regarding the investigation of psychometric properties of the identified instruments, several operationally defined indicators were examined according to the Terwee et al. criteria [44] and to the modifications proposed by Park, Reilly-Spong, and Gross [45]. The first domain was reliability, defined as the degree to which the measurement is free from measurement error. Specifically, it was analyzed in terms of three measurement properties: 1) internal consistency, which is the extent to which items in a scale are correlated (i.e., homogeneous); 2) reliability–divided into a) test-retest reliability, which is the extent to which the test for patients who have not changed produce the same results in different occasions over time; and b) inter-rater reliability, which is the extent to which scores for patients who have not changed are the same when evaluated by different raters; and 3) measurement error, which is the systematic and random error that is not attributed to true changes in the underlying construct, and it is adequate if the smallest detectable change (SDC) on the instrument is less than the minimal important change (MIC) [46].

The second domain was validity, which was examined to test whether the instruments actually measured the construct(s) they purport to measure. Different measurement properties of validity were assessed, including 1) content validity, in particular in the form of face validity, which is the degree to which the items of an instrument seem to be an adequate reflection of the construct to be measured; 2) construct validity, whose examined aspects were a) structure validity, defined as the analysis of dimensionality of the construct, the degree to which the scores of an instrument are an adequate reflection of the dimensionality of the construct to be measured; and b) hypotheses-testing, defined as the degree to which the scores of an instrument are consistent with hypotheses, e.g., with regards to relationships to scores of other instruments or differences between relevant groups; and 3) criterion validity, which is the degree to which the scores of an instrument are an adequate reflection of a ‘‘gold standard”.

Moreover, responsiveness, defined as the ability of an instrument to detect changes over time in the construct to be measured, was evaluated. Eventually, interpretability, which is the degree to which one can assign qualitative meaning to quantitative scores, was examined.

Based on Terwee et al.’s criteria [44] with the revisions of Park et al. [45], the psychometric properties of the selected articles were rated as “positive”, “negative”, or “indeterminate”. Ratings equal to “0” were given when no information was available (Table 1).

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Table 1. Relevant psychometric properties and each criterion used and relative definition adapted from Terwee et al. [44] and Park et al. [45] criteria for measurement properties.

https://doi.org/10.1371/journal.pone.0217700.t001

As a combination of the list proposed by Terwee et al. [44] and the COSMIN checklist (Consensus-based Standards for the selection of health status Measurement Instruments) [47, 48] has been recommended in assessing the quality of questionnaires [47], besides the qualitative analysis of the psychometric properties, the methodological quality of the studies on the measurement properties was examined according to the COSMIN checklist. The COSMIN contains four steps and 12 boxes. Ten of them aim to assess whether a study meets the standards for good methodological quality for each psychometric property separately (Boxes A to J), whereas two boxes examine general requirements for articles involving Item Response Theory (IRT) methods and general requirements for the generalizability of the results. Each box contains 4-to 18 items, with 119 items in total; each item is rated on a 4-point rating scale, equivalent to excellent (+++) when there is evidence that the methodological quality of that peculiar aspect is adequate, good (++) when relevant information is not reported in the article but it can be assumed that the quality aspect is adequate, fair (+) when it is doubtful whether the methodological quality aspect is adequate, and poor (0) when there is evidence that the methodological quality aspect is not adequate. The overall score per box is determined by the item with the lowest score [47, 48].

Results

The search returned 1913 publications. After excluding 1257 duplicates, we reviewed the titles and abstracts for each of the 656 remaining publications. Among them, 321 studies met the inclusion criteria of being peer-reviewed full-text articles published in English that examined ICDs in PD patients. However, of those 321 articles, 311 were removed as they administered tools assessing ICDs in PD patients, but did not examine their psychometric properties. As a final result, ten studies were identified (Fig 1).

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Fig 1. Flowchart of the search strategy and selection of articles.

https://doi.org/10.1371/journal.pone.0217700.g001

Those ten eligible articles reported the psychometric properties of seven instruments, although three of them were represented by the Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease (QUIP) [49], and two modified versions–i.e., the Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Short version (QUIP-S) [49], and the Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease-Rating Scale, which includes both the frequency and the severity of symptoms belonging to the ICDs sphere (QUIP-RS) [50]. The other tools were: The Dopamine Dysregulation Syndrome-Patient and Caregiver Inventory (DDS-PC) [51], the Ardouin Scale of Behavior in Parkinson’s Disease (ASBPD, developed by Ardouin et al. [52], and validated by Rieu et al. [42]), the Impulse Control Disorders and Related Conditions Questionnaire (ICDRC) [53], and the Parkinson’s Impulse Control Scale for the severity rating of Impulse-Control Behaviors (PICS) [54]. The selected tools are reported in Table 2, along with a brief description of their characteristics.

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Table 2. Descriptive characteristics of the selected articles.

https://doi.org/10.1371/journal.pone.0217700.t002

Qualitative analysis of the psychometric properties

Table 3 displays the assessment of the quality of the psychometric properties that were available for each of the selected instruments according to Terwee et al.’s criteria [44] revised by Park et al. [45].

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Table 3. Qualitative analysis of the psychometric properties of the selected instruments according to Terwee et al. criteria (2007) revised by Park et al. (2013).

https://doi.org/10.1371/journal.pone.0217700.t003

Reliability.

Internal consistency was provided for only one study [42], with moderate values for all the subscales around .70, so, according to Terwee et al.’s criteria [44], the quality of this psychometric property was rated positively.

Examining the second measurement property included in the reliability domain, inter-rater reliability was provided for four studies [42, 50, 54, 55]. However, the entity of different raters is various among the studies; for instance, Papay et al. [55] calculated inter-rater reliability by comparing patient’s answers with an informant’s ones (i.e., a caregiver, such as a close relative); in Weintraub et al.’s study [50], it was computed by comparing the patient’s answers with the assessment of a trained clinician. In the other two studies [42, 54], ratings from different clinicians were compared. According to Terwee et al.’s criteria [44], only Okai et al.’s and Weintraub et al.’s studies were rated positively, since results for the other two studies were lower than the defined criteria. In fact, in Papay et al.’s study kappa values for the agreement between patients and informants for reporting any ICD was .41, and in Rieu et al.’s kappa values ranged from .29 to .81, though only the Hypersexuality behavior met the criterion of kappa being .70 or higher. Referring to test-retest reliability, it was provided for four studies [42, 50, 54, 57]. However, according to Terwee et al.’s criteria, only reliability for Probst et al.’s and for Weintraub et al.’s studies was rated positively, as results met the defined criteria. Instead, weighted kappa was .42 in Okai et al.’s study and ranging in Rieu et al.’s study, from .39 to .79, though only agreement for the Hypersexuality and the Compulsive shopping behaviors reached the minimum criterion of .70.

There was no evidence to evaluate measurement error for the selected instruments.

Validity.

Concerning validity, it was provided for all studies, though the specific examined aspects of this domain were different among the studies. Referring to face validity, it was provided in few studies [49, 51]. In detail, the QUIP [49] was administered to 10 research members to gather their feedback and to five PD patients and their caregivers. Moreover, regarding the DDS-PC [51], it was reviewed by three patients and caregivers. Still referring to content validity, few studies provided information about the ability to understand the item content. To this extent, concerning the QUIP-S [58], five PD neurologists and 30 patients were asked their comment about the level of comprehension of the questions. Furthermore, eight PD patients and five healthy controls were asked to assess the items readability of the QUIP-RS [57]. However, neither the first nor the second studies reported information about the completeness and/or comprehensiveness of the items, so they were rated as intermediate according to the modifications of Terwee et al.’s criteria [44] proposed by Park et al. [45].

Concerning structural validity, Rieu et al.’ study [42] conducted an Exploratory Factor Analysis (EFA) that forced the number of factors to five, thus explaining the 77% of variance. In detail, factors were 1) Hypodopaminergic disorders, such as depressed mood, 2) Non-motor fluctuations and punding, 3) ICDs, and creativity, 4) Nocturnal hyperactivity, risk-taking behavior, and dopaminergic addiction, and 5) Diurnal somnolence and psychotic symptoms. However, the authors opted for conceptualizing the latter three factors as a unique domain assessing hyperdopaminergic symptoms. Quality of the structural validity for this study was rated positively.

Concerning the hypotheses-testing category, its quality was rated positively for all the studies included in the present review–except for Krieger et al. [58], that did not provide information about this aspect. For instance, the DDS-PC scale showed high correlations for impulsivity measured with the Italian version of the BIS-11 [61], and with the Cloninger’s Tridimensional Personality Questionnaire [62], in line with the authors’ hypotheses [51]. In addition, the ASBPD scale [42] showed low association with scales measuring different constructs, such as between each ICD and affective symptoms measured with the Montgomery and Asberg Depression Rating Scale [63], and between ICDs and psychotic symptoms assessed with the Positive and Negative Syndrome Scale [64].

Hypotheses-testing was also measured in terms of significant differences; in detail, scores at the PICS were significantly different between PD patients with and those without ICDs [54].

Criterion validity was provided for the ASBPD, which showed high correlations with McElroy et al.’s criteria [65] for compulsive shopping, with DSM-IV-TR [5] criteria for pathological gambling, and with Carnes [66] criteria for hypersexuality. Also for this study, quality of the examined psychometric property according to Terwee et al.’s criteria [44] was rated positively.

Responsiveness.

Responsiveness was tested just for two instruments, namely the QUIP-RS [50], and the PICS [54]. In both cases, the examined tools resulted to show good responsiveness to change after being involved in a clinical treatment for ICDs, and both studies were rated positively according to Terwee et al. criteria [44].

Interpretability.

There was no evidence to evaluate interpretability for the selected instruments, since mean and SD scores were not presented of at least four relevant subgroups of patients, and MIC were not defined in any of the examined studies.

Methodological quality of the selected articles

Methodological quality of the investigated measurement properties for the selected studies was judged according to the COSMIN checklist [47, 48]. Results are reported in Table 4. The overall methodological quality was fair to good because of some required information per parameter not being reported; in many cases, methodological quality was rated good instead of excellent because almost all the required data were declared, except for the percentage of missing answers or the procedure of handling missing items [42, 55]. However, there are some exceptions. For instance, both Probst et al.’s study [56] examining the QUIP-RS and Krieger et al.’s study [58] were rated poor when concerning methodological quality of content validity, because of many lacking parameters, since they both examined only the level of comprehension and readability of the questions. Moreover, in Weintraub et al.’s study [50] responsiveness to change was methodologically poor because of the small sample size (i.e., less than 30 patients). On the other hand, in Weintraub et al. study concerning the QUIP [49], methodological quality for content validity was rated excellent, as all the required standards were met. Remarkably, in most cases the generalizability box scored better than the quality of the assessment of the properties per article, as the articles reported most of the required data for this section.

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Table 4. Methodological quality of reviewed studies according to the COSMIN checklist (Mokkink et al., 2010a, 2010b).

https://doi.org/10.1371/journal.pone.0217700.t004

Discussion

Impulse Control Disorders are one of the most frequent non-motor features of PD, occurring in up to 20% of PD patients [4]. ICDs worsen quality of life and are responsible for several emotional and social impairments [33, 35, 46]. Though not being the only responsible factor for the onset of ICDs, dopaminergic treatment, mainly dopamine agonists, plays an important role [4, 27]. In fact, case reports suggested that ICDs often resolve after adjusting the therapeutic dosage [38, 39]. Thus, to better address patients’ needs and delineate a specific intervention that may include treatment modifications, an accurate assessment of the presence of ICDs is recommended.

As self-report questionnaires and interviews are extremely useful for clinicians to examine ICDs, in the last decade researchers have focused on the development and validation of tools that may support in the clinical assessment. However, despite the implications that ICDs have on PD patients’ lives, these behaviors tend to be under-recognized in clinical practice [33, 37], since routine screening for ICDs is not common [4]. Furthermore, clinicians may often opt for a qualitative, subjective assessment rather than using ad hoc designed instruments and protocols, notwithstanding their accuracy, shortness, and ease of use. In addition, not all the existing instruments aiming to assess the same clinical feature are equally good in terms of psychometric properties, since there may be differences in terms of their ability to effectively and precisely measure the considered aspect. As such, before administering a tool, testing its measurement properties would be needed.

To test for the reliability and validity of the existing instruments–so that clinicians may decide to benefit from them–in the present systematic review the quality of the psychometric properties of the included studies was assessed according to Terwee et al.’s criteria [44] revised by Park et al. [45], whereas the methodological quality of the studies was examined according to the COSMIN checklist [47, 48].

Some considerations may be advanced referring to our findings. First, although other instruments specifically assessing only one impulse control disorder in PD patients exist–such as the South Oaks Gambling Screen [67], the Sexual Addiction Screening Test for PD patients (PD-SAST) [68], the Clinician Punding Criteria and Rating Scale for punding [69], and the Saving Inventory-Revised for compulsive hoarding [70]–we decided to include only those instruments that examined more than one ICD at the same time. In fact, to help clinicians in evaluating the presence ICDs in an efficient way, we thought that it would be better to focus on instruments that allowed to assess different ICDs at the same time. Moreover, we included only those instruments whose psychometric properties have been tested. Thus, some screening tools whose psychometric properties have not been examined were not included in the present review.

The second consideration is that further evaluations on the psychometric properties of the instruments examined in this review should be performed, since most studies assessed only two or three psychometric properties. This does not mean that the included measures in this review are not reliable or valid tools. However, as analyses were not exhaustive, further investigation on their psychometric properties is needed. In detail, further information would be needed to provide evidence of internal consistency, measurement error, cross-cultural validity, criterion validity, and responsiveness to change. Additionally, the use of IRT methods for statistical analysis of psychometric properties would also need further exploration. In fact, IRT improves the accuracy of assessment instruments as it examines how well each item can discriminate between people with different levels of the latent trait–in this case, with different severity of ICDs. Furthermore, instead of providing a single value for reliability (e.g., alpha coefficient), through the test information function (TIF) IRT allows for assessment of measurement precision at different levels of the measured construct [71], meaning that the more information the test provides at a particular trait level, the smaller the error associated with estimation is and the higher reliability is.

Concerns may also arise about the quality of the examined psychometric properties, as, in some studies, results were not good enough to be rated positively according to Terwee et al.’s criteria [44]. Furthermore, in some cases methodological quality for some measurement properties was doubtful or lacking, so future studies should re-perform the analyses with a more methodologically precise procedure. For instance, studies should better focus on and report the preliminary data analyses referring to the percentage of missing answers and their handling procedure.

In sum, from an overall view that considers the quality of the measurement properties of the instruments, the methodological quality of their related article, and the number of articles that focused their analyses on a specific tool, the QUIP and the ASBPD seem to be better from a psychometric point of view. The QUIP may be selected when looking for a quick tool aiming to explicitly assess ICDs, whereas the ASBPD may be chosen when aiming to gather more information about the general psychological status of PD patients. However, these two measures–above all, the QUIP–represent the most studied, so the most available information is about them. Thus, future studies should further examine the psychometric properties of the other tools. From a clinical point of view, while the ASBPD and the ICDRC are behavioral scales that only assess the frequency and intensity of symptoms–though the ICDRC also examines their consequences–the other instruments investigate many dimensions underlying ICDs–such as thinking too much about those behaviors, having urges or desires to engage in them, and experiencing difficulty controlling them. Thus, those measures result to be more informative on which factors may contribute to ICDs, allowing to obtain a more detailed frame of the patient and his behaviors.

Despite the contribution, this review may present some limitations concerning which tools should have been included. Though EMBASE, MEDLINE, and PsycINFO index thousands of journals, some studies examining the psychometric properties of ICDs instruments in PD patients may have not been included because they were published in journals not indexed in the three examined databases. Moreover, the exclusion criterion of being meeting abstracts or materials published in the form of thesis, book chapters, and manuals may have led to the omission of relevant results.

Although the gold standard for diagnosis still remains a detailed diagnostic interview, we hope that this review will encourage clinicians to get acquainted with the use of valid and reliable tools in their everyday clinical practice, rather than relying on an incomplete evaluation to assess ICDs in PD patients. Furthermore, this review will be helpful in the process of instrument selection by allowing researchers and clinicians to easily evaluate and choose the most appropriate measures that fulfil their purpose.

Supporting information

Acknowledgments

We thank all contributors to the present paper.