Prevalence of Obsessive-Compulsive Symptoms in Elderly Parkinson Disease Patients: A Case-Control Study

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Prevalence of Obsessive-Compulsive Symptoms in Elderly Parkinson Disease Patients: A Case-Control Study Maria Rita Lo Monaco, M.D.#, Enrico Di Stasio, M.D.#, Giuseppe Zuccal a, M.D., Martina Petracca, M.D., Danilo Genovese, M.D., Domenico Fusco, M.D., Maria Caterina Silveri, M.D., Rosa Liperoti, M.D., Diego Ricciardi, F.T., Maria Camilla Cipriani, M.D., Alice Laudisio, M.D., Anna Rita Bentivoglio, M.D., Ph.D. ARTICLE INFO

ABSTRACT

Article history: Received June, 3 2019 Revised August, 22 2019 Accepted August, 22 2019

Background: The clinical picture of obsessive-compulsive disorder encompasses a broad range of symptoms that are related to multiple psychological domains, including perception, cognition, emotion, and social relatedness. As obsessive-compulsive symptoms (OCS) frequently have an early onset, there are limited data about OCS in older populations (≥65 years) and, in particular, in elderly subjects with Parkinson disease (PD). Objective: This study aimed to estimate the prevalence of OCS using a self-report measure (Obsessive-Compulsive Inventory-Revised) and to identify associated sociodemographic and clinical factors in a sample of elderly PD patients compared to a comparison group of similarly aged healthy volunteers. Results: The mean age was 74 § 6 years in the PD patients and 73 § 7 years in the comparison group. The mean disease duration was 9.6 § 5.8 years. Among the PD patients, 30.7% reported at least one OCS or a related disorder compared to 21.1% in the comparison group. Hoarding was significantly more common in PD patients than in the comparison group. Conclusions: Subclinical OCS were present at a high percentage in both PD patients and comparison group. The OCS phenotype in PD may present differently, as hoarding was more common in PD patients. (Am J Geriatr Psychiatry 2019; &&:&&−&&)

Key Words: Obsessive-compulsive disorder hoarding Parkinson disease elderly

From the Fondazione Policlinico Universitario Agostino Gemelli, IRCCS (MRLM, EDS, GZ, DF, RL, DR, MCC, ARB), Rome, Italy; Institute of Internal Medicine and Geriatrics, Universita Cattolica del Sacro Cuore (MRLM, GZ, DF, RL, MCC), Rome, Italy; Institute of Neurology, Universit a Cattolica del Sacro Cuore (MP, DG, ARB), Rome, Italy; Istituto di Biochimica e Biochimica Clinica, Universita Cattolica del Sacro Cuore (EDS), Rome, Italy; Department of Psychology, Universita Cattolica del Sacro Cuore (MCS), Milan, Italy; and the Unit of Geriatrics, Department of Medicine, Campus Bio-Medico di Roma University (AL), Rome, Italy. Send correspondence and reprint requests to Maria Rita Lo Monaco, MD, Fondazione Policlinico Universitario Agostino Gemelli, IRCCS, Largo A Gemelli, 8 00168 Rome, Italy. e-mails: [email protected], [email protected] © 2019 American Association for Geriatric Psychiatry. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jagp.2019.08.022 # These authors contributed equally.

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ARTICLE IN PRESS OCD in the Geriatric Population

INTRODUCTION

P

arkinson disease (PD) is a neurodegenerative disorder characterized by abnormalities in movement, behavior, cognition, and emotion. Both the disease itself and its treatment, consisting of dopaminergic replacement therapy, can cause psychiatric disorders. The DSM-V defines obsessive-compulsive disorders (OCD) as a category of behavioral disorders characterized by recurrent and persistent thoughts, urges, or images that are experienced as intrusive and inappropriate, and that cause marked anxiety and distress.1 OCD is the fourth most common mental disorder after depression, alcohol/substance misuse, and social phobia.2 The World Health Organization ranks OCD as 1 of the 10 most handicapping conditions by lost income and decreased quality of life.3 Previous studies have reported a lifetime prevalence of OCD of 1%−3%.4 The general onset of OCD occurs around 20 years of age, but it has been suggested that there is a second peak of onset in later life.5 Obsessive and compulsive symptoms (OCS) are more common than a diagnosed OCD, and OCS have an estimated weighted lifetime prevalence of 5.5% in the general population.6 Little is known about the prevalence of OCS in older age groups, particularly in the aging population affected by neurodegenerative diseases, such as PD. Indeed, OCS could be underestimated because subjects might be reluctant to disclose thoughts or behaviors that they perceive as shameful or embarrassing and because there is a lack of sensitivity in investigating these symptoms. PD is characterized by dysfunction in the frontobasal ganglia circuitry.7 Similar circuitry dysfunction has also been implicated in the pathophysiology of OCD,8 and some studies have reported a higher incidence of OCD in PD patients due to the involvement of similar circuitry9 that can lead to a pervasive executive dysfunction in both PD10 and OCD. Indeed, a neuroanatomical model of OCD proposes that clinical symptoms of obsessive thoughts, compulsive acts, and neurocognitive deficits are related to dysfunction in several parallel-running subnetworks that collectively comprise the cortico-striato-thalamo-cortical (CSTC) loop that is involved also in PD.11 Frontal lobes cortical-subcortical changes have been extensively reported in old age, although there

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is considerable heterogeneity in the cognitive patterns of elderly adults.12 To date, only one large-scale epidemiological study examining OCD prevalence in individuals aged over 60 years has been conducted.13 In this study were carried out an extensive structured interview focusing particularly on psychiatric morbidity and cognitive assessments in subjects age 60 or older. The main finding was that obsessions and compulsions had significant prevalence in the older population and that relative impairment in executive function was found in people reporting these symptoms. So a potential implication of these findings is that older people with obsessive-compulsive symptomatology should be investigated for the presence of early cognitive impairment particularly in executive function. There are many open questions about the phenomenology of OCD in neurodegenerative diseases, and theories about the development of OCD have rarely been applied to older populations. Advanced age is a well-known risk factor for PD. The incidence of PD increases with age and affects 1%−2% of the population aged over 65 years.14 Based on these premises, an intriguing relationship could exist between the aging brain, PD, and OCD, with relevant scientific and clinical implications. To the best of our knowledge, there are no data on OCD that are specific to elderly PD patients. We conducted an observational, cross-sectional study to estimate the prevalence of OCD in a sample of elderly PD patients compared to a group of healthy subjects, and sought to identify the sociodemographic and clinical factors associated with OCD in elderly PD patients.

METHODS Study Design and Objective This study aimed to estimate the prevalence of OCS using a self-report measure (Obsessive-Compulsive Inventory-Revised) and to identify associated sociodemographic and clinical factors in a sample of elderly PD patients compared to a comparison group of similarly aged healthy volunteers. In order to assess the prevalence and clinical patterns of OCD, we included 77 consecutive nondemented elderly PD

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ARTICLE IN PRESS Lo Monaco et al. subjects and 57 healthy subjects of the same age, who completed the Obsessive-Compulsive InventoryRevised (OCI-R). We used the current World Health Organization (WHO) definition of elderly (≥65 years of age), even though there is continued debate about whether this age should be used as the cutoff.15

The study protocol was reviewed and approved by the Ethics Committee of Fondazione Policlinico Universitario “Agostino Gemelli,” IRCCS, Catholic University of the Sacred Heart, Rome, Italy. The study was carried out in agreement with legal requirements and international norms.18

Statistical Analyses

Study Procedures

Statistical analyses were performed using Statistical Package for Social Science (SPSS) software (version 21.1). Clinical, demographical, functional, and cognitive scores were first analyzed for normality of distribution using the Kolmogorov-Smirnov test of normality. Continuous variables were expressed as mean § standard deviation (SD) or median (range) and categorical variables are displayed as frequencies. The appropriate parametric (Student’s t test) or nonparametric test (Mann-Whitney U test, x2 or Fisher’s exact test) was used to assess the significance of the differences between comparison group and PD patients. After adjustment for multiple measures, a p value <0.01 was considered statistically significant. Finally, multiple linear regression with backwardstepwise method was performed to study the relationship between Hoarding Score and PD in presence of confounding factors: covariates introduced in the model were variables significantly different between the study groups (comparison group and PD patients) as reported in Table 1.

The following data were recorded for all study participants: age, sex, education level, marital status, living situation, smoking history, abilities in activities of daily living as assessed by the ADLIADL scale,19 cognitive status according to the MMSE, depression severity according to the 15-item Geriatric Depression Scale (GDS-15)20 (a self-report screening scale for depression that asks participants to answer “yes” or “no” to questions concerning depression symptoms, with a cut-off score of 5 for clinically significant depressive symptoms), and clinical characteristics including age at PD onset, disease duration, comorbid medical conditions, and concomitant medications. Clinical characteristics of PD were assessed by the Unified Parkinson’s Disease Rating Scale (UPDRS)21 and Hoehn and Yahr22 staging during the “on” state. The levodopa equivalent daily dose (LEDD, mg) was calculated according to the published conversion factors for individual antiparkinsonian drugs. The LEDD is defined as the levodopa equivalent dose of a drug that produces the same symptomatic relief as 100 mg of immediate-release levodopa combined with a dopa decarboxylase inhibitor.23 All study participants self-completed the Obsessive-Compulsive Inventory, Short Version (OCISV), a reliable and valid measure of OCD symptoms that is also quicker (administration time between 3 and 5 minutes) than other self-report (or clinician-administered) measures, and has good psychometric properties in both nonclinical and clinical populations.24 The OCI-R consists of 18 items, each scored from 0 to 4 according to the degree of associated distress, and provides subscales for specific symptom domains (i.e., washing, checking, ordering, obsessing, hoarding, and neutralizing). Scores higher than or equal to 21 (out of 72) on the OCI-SV suggest the presence of OCD.

Study Sample All PD patients were recruited from those attending the outpatient Geriatric Day Hospital and Movement Disorder Clinic of the Catholic University Hospital in Rome, Italy. Age-matched healthy volunteers were recruited from people attending the Fitness Center for seniors at the same hospital. Patients with PD were enrolled if all of the following inclusion criteria were fulfilled: 1) diagnosis of PD according to the United Kingdom Brain Bank criteria,16 2) stable dopaminergic treatment for at least 1 month prior to study enrolment, 3) Mini-Mental State Examination (MMSE)17 score >24/30, 4) age ≥65 years, and 5) signed informed consent. The inclusion criteria for the comparison group were: 1) clinical exclusion of Parkinsonism, 2) MMSE score >24/30, 3) age ≥65 years, and 4) signed informed consent. Am J Geriatr Psychiatry &&:&&, && 2019

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ARTICLE IN PRESS OCD in the Geriatric Population TABLE 1. Main Characteristics of Participants According to Parkinson Disease (PD) Status Comparison Group (n = 57)

PD Patients (n = 77)

Test Value

p

73 § 7 37%

74 § 6 9.6 § 5.8 64 § 9 64%

5.3 9.4 4.2

0.614a 0.003b 0.237c

72% 11% 3% 14% 18%

83% 7% 0% 10% 13%

0.5 6.0

0.474b 0.310c

5% 11% 26% 35% 23%

1% 18% 25% 24% 31%

65% 7% 28% 27 [24−30] 6 [1−7] 8 [5−8] 16% 12% 8% 3% 3% 2% 21.1%

61% 8% 31% 26 [24−30] 6 [0−8] 7 [0−8] 22 [6−53] 2 [1−5] 37% 10% 27% 13% 12% 3% 575 [150−1,800] 30.7%

0.2

0.900c

1,469 1,677 1,350 1,710 2,153 6.4 1,986 2,015 2,178 1.2

0.001d 0.004d <0.001d 0.008c 0.732c 0.013b 0.058c 0.089c 0.745c 0.320b

Age (y) Disease duration (y) Age at the onset (y) Gender (male frequency) Marital status  Married  Single  Divorced  Widower/widow Living alone Education  None  Primary school  Middle school  Secondary school  Degree Smoking  No smoker  Smoker  Ex-smoker MMSE ADL IADL UPDRS III H&Y Depression Benzodiazepines Total antidepressant drugs -SSRI -SNRI -Tricyclic LEDD OCD%

Notes: MMSE: Mini-Mental State Examination; ADL: activities of daily living; IADL: instrumental activities of daily living; UPDRS -III: Part III of the Unified Parkinson’s Disease Rating Scale; H&Y: Hoehn and Yahr scale; SSRI: selective serotonin reuptake inhibitor; SNRI: serotonin and norepinephrine reuptake inhibitors; LEDD: L-dopa equivalent daily dose; OCD: obsessive-compulsive disorder. a Statistical tests legend: Student’s t. b Statistical tests legend: Fisher’s test. c Statistical tests legend: x2. d Statistical tests legend: MWU.

RESULTS The study included a total of 134 participants: 77 PD patients (64% male, mean age 74.6 § 6 years, mean duration of disease 9.6 § 5.8 years), and 57 healthy subjects (37% male, mean age 73 § 7 years). Clinical and sociodemographic data of the study sample are presented in Table 1. Compared to the members of the comparison group, PD patients had a higher frequency of depressive symptoms and more significant impairment in the ADL and IADL scores, but there was no difference in psychotropic drug use between the groups. According to the OCI-R, 30.7% of PD patients and 21.1% of healthy subjects had an OCS (Pearson

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x2 = 1.161, df = 1, p = 0.281). Among the individual OCS, hoarding was more common in PD patients than in the comparison group (Table 3). Neutralizing (i.e., counting items or actions, mental counting) was also found to be more prevalent in the PD sample, but the total number of subjects (both PD and comparison group) with this disorder was very low. There was no relationship between the severity of PD and OCS.

DISCUSSION In the present study, we describe a high prevalence of OCS in both PD and healthy elderly subjects with

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ARTICLE IN PRESS Lo Monaco et al. TABLE 2.

Main Characteristics of Parkinson Disease Patients According to the Presence of Obsessive-Compulsive Disorder (OCD) Patients Without Patients With OCD (n = 54) OCD (n = 23) p Value

Age (y) Disease duration (y) Age at disease onset (y) Gender (male frequency) Marital status  Married  Single  Divorced  Widower/widow Living alone Education  None  Primary school  Middle school  Secondary school  Degree Smoking  Nonsmoker  Smoker  Ex-smoker MMSE ADL IADL UPDRS III H&Y Depression Benzodiazepines Total antidepressant drugs SSRI SNRI Tricyclic LEDD

74 § 5 9.5 § 6.0 65 § 8 64%

73 § 6 8.8 § 4.8 62 § 9 68%

79% 10% 0% 11% 17%

96% 0% 0% 4% 5%

2% 19% 25% 23% 31%

0% 19% 24% 24% 33%

59% 9% 32% 27 [24−30] 6 [0−6] 7 [0−8] 22 [6−53] 2 [1−5] 32% 11% 32% 15% 15% 4% 500 [150−1,800]

64% 4% 32% 27 [24−30] 6 [3−6] 6 [3−8] 24 [13−43] 2 [1−4] 46% 9% 14% 9% 5% 0% 712 [300−1,340]

a

0.376 0.611a 0.263a 0.738b 0.190c

0.115b 0.974c

0.766c 0.757d 0.889d 0.716d 0.164d 0.648d 0.272c 1.000b 0.152b 0.714b 0.268b 1.000b 0.496d

Notes: MMSE: Mini-Mental State Examination; ADL: activities of daily living; IADL: instrumental activities of daily living; UPDRS -III: Part III of the Unified Parkinson’s Disease Rating Scale; H&Y: Hoehn and Yahr scale; SSRI: selective serotonin reuptake inhibitor; SNRI: serotonin and norepinephrine reuptake inhibitors; LEDD: L-dopa equivalent daily dose; OCD: obsessive-compulsive disorder. a Statistical tests legend: Student’s t. b Statistical tests legend: Fisher’s test. c Statistical tests legend: x2. d Statistical tests legend: Mann-Whitney test.

hoarding more common in PD patients. In a large epidemiological survey on lifetime OCS conducted on a sample of 2,073 respondents from the National Comorbidity Survey Replication in the United States (a large-scale, nationally representative epidemiological survey of US households), more than a quarter of the respondents experienced obsessions or compulsions at some time in their lives, even though only a small proportion of respondents met the full DSM-IV

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TABLE 3.

Obsessive-Compulsive Inventory-Revised (OCI-R) Total and Subscale Means § sdv and Median [Range] for Control Subjects and Patients With Parkinson Disease (PD) Comparison Group (n = 57)

PD (n = 77)

Total 12.9 § 9.6 12 [0−45] 15.4 § 11.2 12 [1−49] Hoarding 2.9 § 2.6 2 [0−11] 4.2 § 3.1 3 [0−11] Checking 2.3 § 2.7 1 [0−11] 2.7 § 2.9 2 [0−12] Ordering 3.9 § 3.1 3 [0−12] 3.8 § 2.9 3 [0−10] Neutralizing 0.4 § 0.9 0 [0−4] 1.2 § 2.1 0 [0−9] Washing 1.6 § 2.3 0 [0−9] 1.5 § 2.4 0 [0−11] Obsessing 1.8 § 2.0 1 [0−7] 2.0 § 2.5 1 [0−11]

p Value 0.230a 0.019a 0.347a 0.847a 0.020a 0.898a 0.897a

Maximum total score = 72, maximum subscale score = 12. Significance was set at p <0.01. a Mann-Whitney test.

criteria for lifetime (2.3%) or 12-month (1.2%) OCD.4 Prevalence estimates are typically only reported for the full syndrome, although in all probability, the prevalence of subsyndromal obsessions and compulsions is higher. Furthermore, a previous study reported increasing hoarding severity with age.25 OCD is widely recognized as a serious psychiatric condition. The disorder is marked by three distinct clusters of symptoms. First one, obsessions, has been defined as intrusive and unwanted thoughts, images, or ideas. The second component, compulsions, has been defined as specific behavioral actions, including covert mental rituals, intended to neutralize the obsessions. Third, in addition to these two primary symptoms, individuals with the disorder engage in extensive avoidance to prevent the provocation of obsessions and their associated compulsions.26 So when we talk about OCD, we refer to the whole spectrum of described symptoms that are, in this study, investigated only with scales. One factor that may link dysfunctional beliefs to OCS in older populations is concern about cognitive functioning. Jorm et al.23 found that over 60% of adults aged 70+ reported that they felt their memory was worse than it had been earlier in life. Importantly, subjective cognitive complaints often do not reflect real changes in cognitive functioning,27 but concerns about cognitive functioning could possibly lead to greater monitoring of thoughts, making rational intrusive thoughts more salient and activating more effortful thought control attempts. As a result, they become more distressed in response to normal, unwanted, intrusive thoughts than they would have

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ARTICLE IN PRESS OCD in the Geriatric Population been without the appraisal of cognitive decline. In essence, subjective cognitive complaints exacerbate the effects of obsessional beliefs and promote maladaptive responses to intrusive thoughts. The thought of losing control over thought processes can lead to repeatedly controlling actions, promoting “order” of daily life and experiencing more unwanted intrusive thoughts, all factors that promote OCD symptoms. In this study, no significant differences between the groups were found for all the six subscales assessed by the OCI-R (Fig. 1); however, the PD group had higher rates of hoarding and neutralizing than the comparison group. Pathological hoarding is defined as the acquisition of and persistent difficulty in parting with possessions, leading to excessive clutter, distress, and functional impairment. Until recently, hoarding was typically classified as a symptom of OCD. In 2013, the Diagnostic and Statistical Manual of Mental Health Disorders, 5th edition (DSM-5)1 named hoarding disorder (HD) as a distinct clinical syndrome within the OCD and related disorders category. The last decade of research confirms that hoarding behavior is only

present in about 20% of individuals with clinically significant OCS, and conversely, around 83% of individuals with clinically significant hoarding symptoms do not present with clinically substantial OCS24,25. These data suggest that individuals with OCD and hoarding may represent only a fraction of the total sample suffering from HD. Among OCD cases, those with hoarding often have a more severe illness, poorer response to treatment, anxiety, and schizotypal, avoidant, dependent, and obsessive-compulsive personality traits.28 In addition, neurocognitive and neuroimaging studies have found differences in executive functioning, and level of activation in specific brain regions, between OCD cases with and without hoarding.29 A cognitive-behavioral model of hoarding was first proposed by Frost in 1996.30 This model emphasizes deficits in information processing leading to erroneous beliefs about objects, emotional attachment to the objects, and behavioral avoidance. In 2013, Ayers et al.25 reported that middleaged and older adults with HD perform significantly worse than healthy age-matched comparison

FIGURE 1. Obsessive-Compulsive Inventory-Revised (OCI-R) subscale scores for the comparison (n = 57) and Parkinson disease (PD; n = 77) groups. Mann-Whitney U test (<) (comparison group = 57, PD patients = 77); vertical lines rising out of the bars reflect 95% confidence intervals OCIRT < = 1,876 and p = 0.230, CHECKT < = 1,937 and p = 0.347, ORDERT < = 2,123 and p = 0.947, WASHT < = 2,112 and p = 0.898, OBSESST < = 2,110 and p = 0.897, HOARDT < = 1,629 and p = 0.019 (effect size = 0.24—small).

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ARTICLE IN PRESS Lo Monaco et al. group in the Wisconsin Card Sort Task (WCST), suggesting executive functioning impairment in areas such as categorization, maintaining attention and utilization of feedback. Unlike comparison group, the PD participants in this study reported symptoms related to hoarding and neutralizing. The HD could be a concurrent aspect or prodrome of neurodegenerative disorders of later life that cause cognitive impairments. The increased difficulty with discarding could represent an expression of age-related cognitive decline with premorbid executive function deficits, particularly visual memory and categorization, which are known to play a role in HD.31 Based on the existing literature, it would appear that executive dysfunction, characterized primarily by categorization dysfunction, may be a central cognitive component of OCD32 just as it has been established to be a distinctive feature of the cognitive profile of PD10 with a high prevalence.10 Additionally, this categorization dysfunction may contribute to, or be influenced by, deficient sustained attention, slowed information processing speed and memory impairments. All of the factors that can potentially be combined with an abundance of loss experiences33 or a hypersensitivity to loss experiences, which are frequent complaints of subjects in association with increasing age, can exacerbate OCD. This behavioral dysfunction may be the expression of depressive symptomatology. OCD is typically accompanied by comorbid disorders, with depression being the most common.34 Individuals with OCD tend to suffer from comorbid depression at some time during their illness. Furthermore, most studies on risk factors for mental disorders are concerned with depression. In late life, depression can result from multiple factors35; however, it is not always easy to judge what is a cause and what is a consequence of the mental disorder.

STUDY LIMITATIONS Our study has some limitations. First, the sample is relatively small, and future research in larger samples will be required to confirm our findings. Second, there were differences in the gender composition of the two groups. Although OCD affects both sexes, epidemiological studies vary in their findings on the Am J Geriatr Psychiatry &&:&&, && 2019

prevalence of sex differences. One study found increased rates of hoarding among males,36 while others report higher rates among females37 or no sex differences.25,31 Past research has identified differences in the types of OCD symptoms reported by males and females38; however, there were no differences in total score, and subscales between males and females in our sample and the multivariable regression model were adjusted for sex. The final limitation is that only one self-report measure of OCS was used. Diagnosis made by experienced clinicians using the ICD-10 research criteria would have provided additional corroboration of the diagnosis, and facilitated the in-depth assessment of characteristics such as obsessional thoughts and images. Moreover, the OCI-R has the drawback that it does not allow the measurement of overall symptom severity, as it lacks a global severity scale that could capture the extent of distress caused by specific symptoms. Even so, it is a useful screening tool although has not been validated in the PD. To further explore the validity of the OCI-R in this sample, self-reported OCS should be compared with informant reports (e.g., a clinician-administered measure). Finally, longitudinal studies are needed to determine the developmental trajectory and prognosis of OCD in elderly and PD populations.

CONCLUSIONS Although several epidemiological studies have investigated OCD over the past decade, there is a paucity of data about the incidence and prevalence of OCD and HD in elderly populations with PD. Seniors with OCD and, in particular, those with PD could represent a vulnerable population of individuals worldwide who face similar challenges, including impaired activities of daily living and psychiatric and medical comorbidities. In older PD individuals, movement disorder specialists and geriatricians should focus on identifying problems with discarding items, and combine the usual PD treatment with interventions that may be specific to the aging brain (i.e., cognitive training and physical exercise that have been shown induce profound benefits for brain function and general well-being39). Strength of this study was the comprehensive, multidimensional assessment of OCS that could help

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ARTICLE IN PRESS OCD in the Geriatric Population to identify a potential OCD phenotype in the elderly, which should be further elucidated with additional screening measures in future trials. Thus, a better understanding of the age-specific relationship between hoarding and OCS is a first step toward developing appropriate screening and intervention approaches for at-risk individuals, and the relationship between PD and OCD deserves further systematic examination.

2) Statistical analysis. Design and execution: Enrico Di Stasio, Alice Laudisio; review and critique: Giuseppe Zuccala. 3) Manuscript. Writing of the first draft: Maria Rita Lo Monaco, Martina Petracca, Danilo Genovese, and Enrico Di Stasio; review and critique: Maria Caterina Silveri, Domenico Fusco, Rossella Liperoti, and Anna Rita Bentivoglio. Conflicts of interest, financial or otherwise, related to the present manuscript: No disclosures to report.

AUTHORS’ ROLES 1) Research project. Conception: Anna Rita Bentivoglio, Maria Rita Lo Monaco, and Enrico Di Stasio; organization: Maria Rita Lo Monaco and Martina Petracca; execution: Martina Petracca, Diego Ricciardi, Danilo Genovese, and Maria Camilla Cipriani.

SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/ 10.1016/j.jagp.2019.08.022.

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