Parkinsons Disease and Obsessive-Compulsive Phenomena: A Systematic Review

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Current Psychiatry Reviews, 2009, 5, 55-61

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Parkinson’s Disease and Obsessive-Compulsive Phenomena: A Systematic Review Arthur Kummer* and Antonio L. Teixeira* Neuropsychiatric Branch, Department of Internal Medicine, School of Medicine, Federal University of Minas Gerais (UFMG), Belo Horizonte, Brazil Abstract: Objective: To review the literature regarding the occurrence of obsessive-compulsive disorder (OCD), obsessive-compulsive symptoms (OCS), and related personality traits in Parkinson’s disease (PD). Methods: A PsycInfo, Medline, Embase and Lilacs search of English, French, Spanish and Portuguese-language publication was conducted. The search terms used were Parkinson’s and any of the textual words: obsessive, compulsive or personality. Some of the terms were also truncated to improve the search sensitivity. Data concerning personality traits in PD were also considered. Results: The literature concerning OCD, OCS and a particular “parkinsonian personality” in PD is still contradictory. One of the main problems identified was the diversity of instruments used to assess obsessive-compulsive symptoms or traits. However, some studies have highlighted the correlation of motor symptoms asymmetry and specific OCS or personality traits. Other relevant data of the selected studies are also presented and discussed. Conclusion: The available data have critical methodological problems. Although it is well known that PD and OCD share dysfunction of the frontostriatal circuitry, the relationship between them has to be confirmed.

Keywords: Parkinson, obsessive-compulsive, personality, review. INTRODUCTION Parkinson’s disease (PD) is pathologically defined by the neuronal loss predominantly in the substantia nigra pars compacta, and the presence of Lewy bodies in the remaining neurons [1]. This process affects frontostriatal circuitry, which is also involved in the pathogenesis of some psychiatric disorders, mainly obsessive-compulsive disorder (OCD) [2]. Despite controversies concerning the exact prevalence of psychiatric disorders in PD, it is well recognized that depression, anxiety and sleep disturbances are more prevalent in PD patients than in general population [3]. Nevertheless, it is debatable whether the prevalence of OCD in PD is greater than in the general population. The aim of this review is to describe the current evidence of the association between PD and OCD, obsessive-compulsive symptoms (OCS) and personality traits, specially the obsessive-compulsive ones. METHODS The MEDLINE (1966 to August, 2008), PsycInfo (1806 to August, 2008), EMBASE (1888 to August, 2008) and Lilacs (1982 to August, 2008) databases were searched. Reference lists of journal articles were also hand searched for other relevant studies. The search was performed with the term Parkinson’s and the textual terms obsessive, compulsive or personality. Some of the terms were also truncated to

*Address correspondence to these authors at the Departamento de Clínica Médica, Faculdade de Medicina, UFMG. Av. Alfredo Balena, 190, Santa Efigênia, Belo Horizonte, 30130-100, Brazil; Tel/Fax: +55-31-34092651; E-mail: [email protected] or [email protected] 1573-4005/09 $55.00+.00

improve the search sensitivity (parkinson*, obsess*, compuls*). All articles addressing obsessive-compulsive phenomena in PD were considered and referenced in this review. With respect to the review on personality profile in PD, we focused attention on studies which investigated systematically the personality of PD patients with standardized instruments in order to make possible the comparison with the existing data concerning the personality profile of individuals with OCD or anancastic traits. RESULTS Eleven studies have sought to identify OCS and OCD in PD (Table 1). The study of Gibb and Lees evaluated the presence and severity of OCS using the Leyton Obsessional Inventory (LOI) in young-onset PD (disease onset before 45 years of age) and old-onset PD (disease onset was after 70 years of age) [4]. There was no control group for PD patients. The authors did not find any difference between both groups and stated that the LOI’s scores of PD patients were within the normative data according to previously established cut-off points. A total of six patients presented symptoms indicating obsessional state, but in only two of them (both with youngonset PD) these symptoms were distressing. Lauterbach published results of a study with 38 patients with familial PD on which he found a rate of OCD five times higher than of the general population [5]. In some of these patients, OCD followed the onset of parkinsonism.

© 2009 Bentham Science Publishers Ltd.

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Table 1.

Kummer and Teixeira

Current Evidence of Association Between Obsessive-Compulsive Disorder and Parkinson’s Disease

Reference

Population

Instruments

Results

Gibb and Lees, 1988 [4]

29 patients with young-onset PD and 11 patients with old-onset PD

LOI

Symptom and trait scores were similar between groups and under the established cut-off point compatible with an obsessional state. The scores of four patients with young-onset and of two patients with oldonset were suggestive of an obsessional state.

Lauterbach, 1993 [5]

38 patients with familial parkinsonism

Non-structured interview according with DSM-III criteria

6 patients identified with OCD (15.8%).

Tomer et al., 1993 [6]

30 patients with PD were compared to the normative data from the original Leyton’s instrument

LOI

17 patients (56.6%) with higher symptom score, and 19 (63.3%) with a higher trait score than the mean of normal controls. The severity of left-side motor symptoms was associated with the intensity of some OCS (overconscientiousness, repetitions, disturbing thoughts and cleanliness worries). Severity of right-sided symptoms was related to OCS of order and routine.

Cole et al., 1996 [7]

31 patients with PD (M/F; 17/14)

Structured Clinical Interview for DSM-III-R

Lifetime rate was 3.2% for previous OCD. No patient with current OCD.

Müller et al., 1997 [8]

20 patients with PD (M/F; 14/6) and 43 controls (healthy people, patients with OCD and with Tourette’s Syndrome)

MOCI and short version of HZI

No difference between PD patients and healthy controls in MOCI. Patients with PD scored higher than healthy controls in ordering subscale of HZI. PD patients had fewer OCS than patients with OCD and Tourette’s Syndrome.

Alegret et al., 2001 [9]

A subgroup of 72 patients (M/F; 36/36) received the MOCI and a subgroup of 54 (M/F; 27/27) received the LOI. An equal number of healthy controls paired by age, gender and educational level was included

MOCI and a modified version of the LOI

Maia et al., 2003 [10]

100 patients with PD (M/F; 64/36) and 100 controls matched by age and gender

Y-BOCS and Structured Clinical Interview for DSM-IV

Nuti et al., 2004 [11]

90 patients with PD (M/F; 48/42) and 90 healthy controls matched by age and gender

Semi-structured interview according to DSM-IV criteria

Harbishettar et al., 2005 [12]

69 patients with PD (M/F; 56/13) and 69 medically ill controls matched by age and gender

Y-BOCS, STOBS, and structured interview for OCD

No difference between groups. No correlation between Y-BOCS scores and motor symptoms severity.

Bruneau, 2005 [13]

35 patients with PD and 35 healthy paired controls

Y-BOCS

Patients with PD scored higher than controls. The most common OCS were of the ordering, symmetry, or checking type.

Kummer et al., 2008 [14]

50 patients with young-onset PD (M/F; 29/21) and 40 patients with typical-onset PD (M/F; 25/15).

MINI-Plus

Frequency of OCD was 10% in the young-onset group and 17.5% in the typical-onset group. The difference was not statistically significant.

Patients with severe PD scored higher in both inventories. Positive correlation between disease duration and MOCI global scores. Severe PD patients scored higher on checking, cleaning and doubting subscales of MOCI. No patient with PD had OCD according to DSM-IV criteria. No difference between groups in the frequency of OCS, OCD and related disorders. Predominance of bilateral or left-sided symptoms correlated with symmetry obsessions and ordering/arranging compulsions, and with contamination obsessions and cleaning compulsions. Frequency of OCD in PD of 5.5%. No significant difference in the frequency of OCD between groups.

Abbreviations: DSM: Diagnostic and Statistical Manual of Mental Disorders; HZI: Hamburg Obsessive-Compulsive Inventory; LOI: Leyton Obsessional Inventory; MOCI: Maudsley Obsessive-Compulsive Inventory; OCD: Obsessive-compulsive disorder; OCS: Obsessive-compulsive symptoms; PD: Parkinson’s disease; Y-BOCS: Yale-Brown ObsessiveCompulsive Scale; STOBS: Schedule for Tourette and Other Behavioral Syndromes; MINI-Plus: Mini-International Neuropsychiatric Interview-Plus; M/F: male/female.

Tomer et al. aimed to investigate the relationship between OCS and lateralization of motor symptoms in patients with PD using the LOI [6]. They have described higher scores of OCS in PD patients when compared to the normative data. Interestingly, the severity of motor symptoms on the left hemibody, but not on the right, predicted reliably overall severity of OCS. The authors proposed that OCS in PD could reflect increased dopaminergic deficiency in the right basal ganglia. In another study, 31 patients with PD were examined by Cole et al. [7]. The sample were composed by 14 female and 17 male, with a mean age of 65 (range 28-83) and a mean age of onset of 57 (range 24-79). The authors used a structured interview based on DSM-III-R and found a lifetime

frequency of 3.2% for OCD, but no patient presented the disorder at the moment of the study. A study from Müller et al. [8] tried to compare the frequency and clinical features of OCS from PD patients with OCS, patients with Tourette’s syndrome, patients with OCD and healthy controls. The group of PD patients consisted of 20 subjects (14 men and six women) with a mean age of 64 (range 48-83). PD patients scored higher than healthy controls only in ordering subscale of the Hamburg ObsessiveCompulsive Inventory (HZI), but they had significantly lower frequency of OCS than the other groups preventing the comparison of the clinical features of their OCS. A systematic investigation of OCS and traits in PD was also conducted by Alegret et al. [9]. The sample included a

Parkinson’s Disease and Obsessive-Compulsive Phenomena

subgroup of 36 men and 36 women with PD, with a mean age of 63 and a mean age of onset of 52 years, in whom the Maudsley Obsessive-Compulsive Inventory (MOCI) was administered. The other subgroup received a modified version of the LOI, and included 27 men and 27 women, with a mean age of 64 years. Patients with severe PD had greater intensity of both OCS and traits. Interestingly, no PD patient had OCD according to DSM-IV criteria. This could be due to several reasons: the symptoms were not time consuming (i.e., took less than one hour a day), they did not cause marked distress or significant impairment, or even the OCS were considered as a result of a “general medical condition” (i.e., PD itself). If no patient had OCD due to the first two reasons, one must assume that OCS are frequently subclinical in PD. Maia et al. evaluated the frequency of OCS, OCD and related disorders (e.g., tics, trichotillomania, body dysmorphic disorder) in a hundred PD patients (64 male and 36 female; mean age of 62 years) and matched healthy controls [10]. They also examined the relationship between OCS and the lateralized expression of motor symptoms. The only correlation found was between motor asymmetry and the incidence of some specific OCS. Symmetry obsessions and ordering/arranging compulsions, and, less significantly, contamination obsessions and cleaning compulsions were correlated with the predominance of bilateral or left-sided motor symptoms. There was also observed that an early age of onset of OCS (before 18 years-old) was linked to left and bilateral motor parkinsonian symptoms. The study conducted by Nuti et al. compared the frequency of psychiatric disorders between PD patients and healthy controls, but no difference in OCD frequency was found [11]. The sample was composed of 48 men and 42 women, with a mean age of 63 years. In another study, Harbishettar et al. used the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS), the Schedule for Tourette and other Behavioral Syndromes (STOBS) and a structured clinical interview to assess OCS and OCD in PD patients and matched controls [12]. Sixty-nine subjects (56 men and 13 women) were enrolled, with a mean age of 58 and a mean age of onset of 55 years. The family history was also systematically investigated. There was no difference between the two groups with respect to the rates of OCD, subthreshold OCS, type and severity of OCS, and family history of OCD, tics and other psychiatry disorders. No relationship was found between the Y-BOCS scores and the severity of the PD. On the other side, Bruneau found that PD patients scored higher in the Y-BOCS than matched controls [13]. She considered that a score under 8 indicated negligible OCS, while above this cut-off indicated presence of OCS. Ordering, symmetry and checking were the most common OCS and they were frequently egosyntonic which could possibly indicate personality traits. Furthermore, her findings suggested a relationship between obsessionality and perseveration (executive dysfunction) which could be related to a disruption of the cortico-striatal circuitry. Our group have recently compared the frequency of psychiatric disorders between patients with young-onset PD (disease onset at or before 50 years of age) and patients with

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typical-onset PD (onset after age 50 years) [14]. A structured psychiatric interview (MINI-Plus) based on DSM-IV and ICD-10 criteria was used to diagnose OCD. Despite the absence of a control group, the frequency of OCD was remarkably high in both groups. The difference in rates of OCD between both groups was not statistically significant. Other studies investigated whether a characteristic personality profile exists in PD, namely, a profile with obsessive personality traits. Although the existence of a “parkinsonian personality” remains a matter of debate, this concept is supported by some case reports, and cross-sectional, casecontrol, and twin studies [15-21]. On account of some evidences supporting a continuum hypothesis between OCS and obsessive personality traits [22], we reviewed the studies which investigated personality profile in PD. However, as the purpose of this article concerns the presence of obsessive-compulsive phenomena in PD, we confronted the studies about personality in PD with the data about personality in OCD or about anancastic subjects. Menza et al. using the Tridimensional Personality Questionnaire found significantly less novelty-seeking behavior in PD patients compared to matched medical controls [23, 24]. Although the total score for the harm avoidance dimension was higher for the PD patients than for the control group, this difference did not reach statistical significance [24]. Likewise, other three studies found statistical significance that PD patients scored low in novelty seeking and high in harm avoidance dimension [25-27]. Personality features of OCD patients have been consistently associated by some authors to low novelty seeking scores and a high harm avoidance scores [28, 29]. This personality profile was also considered as a possible factor that could predict the severity of OCS [29]. In addition, Menza et al. reported that novelty seeking scores correlated with dopaminergic function in left, but not right, caudate [23], suggesting that novelty seeking is dependent upon the integrity of left dopamine hemisphere systems. Similarly, Tomer and Aharon-Peretz examined if personality traits were also related to motor asymmetries [30]. They verified that only patients with dopamine loss in the left side of the brain showed reduced novelty seeking, whereas increased harm avoidance is associated with dopamine loss in the right striatum [30]. On the other hand, Fujii et al. observed that PD patients undergoing anti-depressive treatment obtained higher scores in harm avoidance supporting the hypothesis that depressive symptoms may overlap this particular personality trait [25]. The studies of Menza and Mark [31] and Jacobs et al. [32] strengthened this hypothesis, as they have showed a strong correlation between harm avoidance, which is a characteristic of personality thought to be dependent on brain serotonergic system, and higher frequency of depressive disorders. However, McNamara et al., who also found that PD patients in comparison with other chronically disabled patients scored lower in novelty seeking and higher in harm avoidance dimension, suggested that these alterations, especially harm avoidance, were related more strongly to executive dysfunction than to mood changes [27]. Of note, PD patients examined by Jacobs et al. exhibited higher “persistence”, another temperament dimension of the Tridimensional Per-

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sonality Questionnaire, but they did not differ from healthy controls in novelty seeking [32]. Some studies found other personality characteristics in PD. Bell et al. clustered the “parkinsonian personality” into a “shyness” trait characterized by introversion, timidity and subordinate behavior, and a “repressive defensiveness” trait, described as being responsible and morally rigid [33]. Macías et al. showed that PD patients had lower levels of external expression of anger and higher levels of control of anger [34]. Interestingly, it has been suggested that OCD patients also have a shyness trait and do not have a great anger expression [35, 36]. By contrast, four studies found no specific personality traits in PD [37-40]. Glosser et al. verified that there was no evidence for a specific personality profile for PD patients either premorbid or following the development of motor symptoms, when compared to patients with Alzheimer’s disease or healthy controls. Nevertheless, after disease onset PD and Alzheimer’s disease patients were described as less extroverted, exploratory and curious, characteristics which could be related to a low novelty seeking profile. These patients were also more disorganized, purposeless and less disciplined, features that could actually indicate executive dysfunction [37]. The studies of Glosser et al. and Poewe et al., who found that PD patients, though differing from healthy controls, did not differ from patients with essential tremor [41], show that patients with neurological disorder might exhibit a similar pattern of behavioral adaptation after disease onset [37, 41]. It should be highlighted that Glosser et al. used the NEO-Personality Inventory, and personality of patients with OCD or pronounced obsessional traits has not been adequately assessed by this instrument yet. On the study of Pluck and Brown, who used the Tridimensional Personality Questionnaire, no differences in personality traits was detected in comparisons between patients with PD and the matched control medical group of osteoarthritis, or between patients in the PD group with high or low levels of apathy [38]. Leiva-Santana et al. and Eatough et al. also found no differences between patients with PD, individuals with rheumatoid arthritis and healthy controls in any of the instruments used to assess personality characteristics, such as novelty seeking, harm avoidance, psychoticism, neuroticism and extroversion [39, 40]. In both studies, patients were administered the Eysenck Personality Questionnaire. According to Fullana et al., OCD patients score higher in Eysenck’s psychoticism – a construct related to antisocial behavior, novelty seeking and impulsivity – and neuroticism subscales [42]. DISCUSSION In the early twentieth century a relationship between OCD and post-encephalitic parkinsonism was established. An outbreak of OCS was noticed following epidemic encephalitis, also known as encephalitis lethargica or von Economo’s encephalitis [43-45]. These findings anticipated current concepts of the role of the basal ganglia in human behavior and then was suggested that OCD could be more frequent in patients with PD [46]. OCD has been previously studied in many diseases which affect the basal ganglia, i.e. Huntington’s disease, Sydenham’s chorea and Tourette’s Syndrome [47, 48]. Nev-

Kummer and Teixeira

ertheless, bona fide studies involving patients with PD are still lacking. The available data have several methodological difficulties. Different questionnaires and scales used make the comparison across studies difficult. For example, while MOCI is used to investigate different types and severity of OCS, LOI is used to evaluate both OCS and traits. Most of the studies did not employ the widely used instrument Y-BOCS which is the standard instrument for tapping a wide range of OCS and their severity [5-8, 11, 14]. In addition, some previous studies had particularly small sample sizes and studied a heterogeneous PD population [5-8, 13]. Another major problem with the reviewed articles is that, at the time some studies were carried on, the authors were not aware of repetitive phenomena in PD such as punding. The relevance of this information concerns the intimate relationship between dopamimetic drugs and the repetitive behaviors. This influence of pharmacotherapy was not taken in account by the studies on OCD and PD. Despite the differences in the phenomenology of punding and OCS [49], unadvised clinicians or structured questionnaires may confound them and diagnose punding as OCS. Nevertheless, some relevant findings may be observed from these studies. Besides the controversy whether a correlation between PD and OCD exists, the relationship between OCS and lateralization of motor symptoms in patients with PD established by some studies may turn future attention to this feature which could improve our comprehension on neurobiological basis of the different types of OCS. For instance, contamination/cleaning-related OCS were related to the predominance of bilateral or left-sided motor symptoms by two studies [6, 10]. This finding is in accordance with a previous neuroimaging study which found that patients with contamination/cleaning-related OCS demonstrated greater activation than controls in bilateral ventromedial prefrontal cortex and in right caudate nucleus [50]. Data concerning some other symptom dimensions, such as ordering/symmetry, are still inconsistent. Until now, no functional neuroimaging or neuropathological study evaluated if OCS in PD could reflect an asymmetric dopaminergic deficiency, as proposed by Tomer et al. [6]. One pertinent reservation is that recent studies have show that PD neuropathology seems to be widespread. PD is not just a simple deficiency of dopamine, but also a shortfall in norepinephrine, serotonin, GABA, corticotropin-releasing factor, and neurotensin [51]. In addition, cellular losses occur not only in substantia nigra, but include the locus ceruleus, the nucleus basalis Meynert, and the cortex [51]. Probably these brain regions are also asymmetric in PD and may influence motor asymmetry [52, 53]. Thus, studies which correlate the association of non-motor symptoms and motor asymmetries to an asymmetric brainstem dopaminergic deficiency underestimate the influence of other brain regions on PD clinical picture. Future studies with larger samples and uniformly using instruments considered “gold pattern” in evaluating OCD and OCS should investigate the existence of these symptoms and their relationship to age of onset, motor symptoms characteristics, laterality, duration and severity of the disease and its treatment.

Parkinson’s Disease and Obsessive-Compulsive Phenomena

A special attention should be directed to PD personality traits. Unlike OCS or OCD, traits are defined as enduring patterns of perceiving, relating to, and thinking about an environment and oneself that are exhibited in a wide range of social and personal contents and are part of the personality of any person [54]. Individuals with PD and OCD patients may share a specific personality profile. For instance, there is an inverse correlation between smoking and the incidence of PD. Although it has been proposed – and not proved yet – that tobacco may have a protective effect against PD, this correlation could be due to personality (reduced likelihood of addiction) issues. Indeed, subjects with OCD smoke less than the general population [55]. Furthermore, non-smokers with OCD, compared to smokers with OCD, have more anancastic personality disorder, are more anxious, less selfconfident, more easily fatigued, and less impulsive [56]. Their personality profile has been characterized by a low novelty seeking behavior and a high harm avoidance behavior [23-27]. Based on a hypothetical involvement of dopamine in novelty seeking behavior, most of the studies that found a low novelty seeking behavior in PD related this finding to a decrease in dopaminergic function in PD, especially in left brain hemisphere, which commence many years before the motor symptoms onset [15, 23-25]. Hence, what is thought to be part of someone’s personality may actually be part of the disease process. However, Kaasinen et al. in a study with unmedicated PD patients showed that novelty seeking is not associated with striatal presynaptic dopaminergic function [26]. Actually, studies which investigated the link between dopamine and novelty seeking or any other personality traits are still discrepant. In addition, no prospective studies were conducted to assess personality changes in PD patients, and whether they start prior or after the disease onset remains a matter of debate [24, 57-59].

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choanalytical one. According to Freud’s ideas, anal eroticism would influence the development of obsessive neurosis [66]. The features of an “anal character” included orderliness, obstinacy, parsimony, emotional constriction, perseverance and rigidity. Curiously, Janet considered the motor symptoms of PD as a result of an unconscious behavior [67]. Other psychoanalysts also associated PD to the repression of instinctive impulses and emotions, a lack of selfassertiveness and due to inner inhibitions [67]. Thus, it is noticeable that even in the first descriptions of both disorders they shared some similarities. The advance in neurobiological and pharmacological researches brought a more plausible etiological comprehension of both OCD and PD. The basal ganglia structures were recognized to be of utmost importance for these conditions. Nevertheless, it is still unknown which is the exact relationship between them. Although much has to be done to confirm the connection between obsessive-compulsive phenomena (obsessive compulsive symptoms and traits) and idiopathic PD, this issue is of both clinical and theoretical relevance. Clinically, undiagnosed OCD in PD could contribute to the aggravation of distress in PD. Their association with anti-parkinsonian medication, if any, must be further explored. Experimental models (e.g. analysis of compulsive-like behaviors in animal models of PD) could also bring insightful contributions. In addition, further controlled studies with large cohorts and using standardized instruments, such as the Y-BOCS, are still necessary. The improvement on the methodology of the retrospective studies investigating if there is any relationship between PD onset and personality traits is essential. These researches may contribute to a better understanding of the obsessive compulsive phenomena and of the non-motor symptoms of PD. REFERENCES

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Received: March 02, 2008

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Revised: September 27, 2008

Accepted: October 22, 2008

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