Accepted Manuscript Patients’ and Informants’ views on visual hallucinations in Parkinson’s disease Prabitha Urwyler, Ph.D., Tobias Nef, Ph.D., René M. Müri, M.D., Alison Killen, M.Sc., Daniel Collerton, M.Sc., David Burn, M.D., Ian McKeith, M.D., Urs Peter Mosimann, M.D., Ph.D. PII:
S1064-7481(14)00571-5
DOI:
10.1016/j.jagp.2014.12.190
Reference:
AMGP 457
To appear in:
The American Journal of Geriatric Psychiatry
Received Date: 15 April 2014 Revised Date:
18 December 2014
Accepted Date: 25 December 2014
Please cite this article as: P. Urwyler, T. Nef, R.M Müri, A. Killen, D. Collerton, D. Burn, I. McKeith, U.P. Mosimann, Patients’ and Informants’ views on visual hallucinations in Parkinson’s disease, The American Journal of Geriatric Psychiatry (2015), doi: 10.1016/j.jagp.2014.12.190. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
2813
ACCEPTED MANUSCRIPT
Patients’ and Informants’ views on visual hallucinations in Parkinson’s disease Prabitha Urwyler, Ph.D.1, Tobias Nef, Ph.D.1,2, René M Müri, M.D.1,3, Alison Killen, M.Sc.4,
RI PT
Daniel Collerton, M.Sc.4,5, David Burn, M.D.4, Ian McKeith, M.D.4, Urs Peter Mosimann, M.D., Ph.D.1,6 *
Gerontechnology & Rehabilitation Group, University of Bern, Bern, Switzerland
2
ARTORG Center for Biomedical Engineering Research, University of Bern, Bern, Switzerland
3
Perception and Eye Movement Laboratory, Departments of Neurology and Clinical Research,
M AN U
SC
1
University Hospital Inselspital, University of Bern, Bern, Switzerland 4
Institute for Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
5
Northumberland, Tyne & Wear NHS Foundation Trust, Bensham Hospital, Gateshead, United
TE D
Kingdom
University Hospital of Old Age Psychiatry, University of Bern, Bern, Switzerland
*
Corresponding author: Urs Peter Mosimann, MD, PhD
EP
6
University Hospital of Old Age Psychiatry, Murtenstrasse 21, CH-3011 Bern, Switzerland
AC C
Email: [email protected] / Telephone: +41 31 632 8817 / Fax: +41 31 632 8944
Conflicts of Interest: No Disclosures to Report. Source of Funding: This research was funded by the National Institute for Health Research Newcastle Biomedical Research Unit (DB, IM), Parkinson’s UK (DB), Michael J Fox Foundation GSK (DB), GE Healthcare (IM), Gateshead Health NHS Foundation Trust (DC, UPM). For the remaining authors none were declared.
Visual hallucinations, Parkinson’s disease, inter-rater agreement
ACCEPTED MANUSCRIPT
ABSTRACT Objective: Visual hallucinations (VH) are a very personal experience and it is not clear whether
RI PT
information about them is best provided by informants or patients. Some patients may not share their hallucinatory experiences with caregivers to avoid distress, or due to fear of being labelled insane and others do not have informants at all, which limits the use of informant based questionnaires. The aim of this study was to compare patient’s and caregiver’s views about VH in Parkinson’s disease (PD),
SC
using the North-East-Visual-Hallucinations-Interview (NEVHI). Methods: Fifty nine PD patientinformant pairs were included. PD patients and informants were interviewed separately about VH
M AN U
using the NEVHI. Informants were additionally interviewed using the four-item version of the Neuropsychiatric Inventory (NPI-4). The inter-reliability and the concurrent validity of the different measures were compared. Results: VH were more commonly reported by patients than informants. The inter-rater agreement between NEVHI-patient and NEVHI-informant was moderate for complex
TE D
VH (Cohen’s kappa = 0.44, 95% CI= 0.13 - 0.75, t = 3.43, df = 58, p = 0.001) and feeling of presence (Cohen’s kappa = 0.35, 95% CI = 0.00 – 0.70, t = 2.75, df = 58, p = 0.006), but agreement was poor for illusions (Cohen’s kappa = 0.25, 95% CI = -0.07 – 0.57, t = 2.36, df = 58, p = 0.018) and passage hallucinations (Cohen’s kappa = 0.16, 95% CI = -0.04 – 0.36, t = 2.26, df = 58, p = 0.024).
EP
Conclusions: When assessing VH in PD patients, it is best to rely on patient information, because not
AC C
all patients share the details of their hallucinations with their caregivers.
Keywords: Visual hallucinations; Parkinson’s disease; inter-rater agreement.
2
ACCEPTED MANUSCRIPT
Visual Hallucinations (VH) are common in Parkinson’s disease (PD).(1) Their prevalence and severity increase as the disease progresses.(2) In cross-sectional studies, prevalence rates for VH range from 5% to 50%,(3-7) while longitudinal studies have shown that the prevalence of VH and behaviors
RI PT
associated with VH, increases over time reaching a life-time prevalence of up to 75%.(2, 8) Hallucinations which are sensory misperceptions are a very personal experience and their phenomenology is commonly classified into simple hallucinations,(9) complex hallucinations,(10, 11)
SC
visual illusions,(12) passing shadows(3) and the feeling of presence.(3, 13) Simple VH have the lowest degree of complexity and refer to flashes, dots, lines, shapes, swirly and pattern like grids or
M AN U
tiles. (9) Complex VH are phenomenologically rich and consist of formed images, e.g. faces, figures, objects, animals and landscapes.(10) Visual illusions are defined as visual percepts which are based on stimuli present in the extracorporeal space, but which are either misperceived or misinterpreted.(12) Passing shadows are perceptions are the perception of something fleeting like a shadow in the ‘corner of the eye’.(3) Feeling of presence is the feeling of a person being present in the room or house,
TE D
usually outside the range of ordinary perception.(13)
VH constitute a major source of distress for patients and caregivers,(4, 14) but are commonly
EP
underdiagnosed because health professionals don’t ask or patients do not disclose them spontaneously.(4, 15) Some patients do not volunteer their hallucinations(4, 15) either due to fears of
AC C
embarrassment,(16) for being classified as mentally ill(15) or due to the fear of stigmatization or restrictive institutionalization.(15) Still others do not want to impose any extra burden on spouses or friends. Hence, it is important for health professionals to ask about hallucinations in an indirect way without making any direct references to the hallucinations. Questions such as “Do you feel your eyes ever play tricks with you?” or “Have you seen something that other people could not see?” have been suggested to be helpful to screen for VH.(17)
3
ACCEPTED MANUSCRIPT Existing scales assessing VH rely either on informant or patient information or both. Self-assessment of VH in PD have been reported using the Non-Motor-Symptoms scale (NMSS),(18) University of Miami Parkinson's disease Hallucinations Questionnaire (UM-PDHQ),(19) Queen Square Visual Hallucination Inventory (QSVHI),(20) Tottori University Hallucinations Rating Scale (TUHARS),(21)
RI PT
North East Visual Hallucination Inventory (NEVHI),(1, 8, 11) and the Rush Hallucination Inventory.(22) The Neuropsychiatric Inventory (NPI),(23) is a composite neuropsychiatric assessment scale including hallucination which relies on informant information only, while the TUHARS and the NEVHI utilize both patient and informant reporting of VH. TUHARS assesses hallucinations in PD
SC
evaluating the variety, frequency, severity of hallucinations, degree of caregiver burden level, and psychiatric status at nighttime,(21) but it does not touch the phenomenology of VH and other
M AN U
characteristics (e.g. emotion and cognition) associated with VH. Most interviews developed have not been used across disorders except of NEVHI, which has been designed for patients with visual and / or cognitive impairments.(17) Moreover, some scales underestimate the frequency,(3) while other scales do not take the phenomenology into account(23) and it remains unclear whether the information is
TE D
best gathered by patients and or informants.
NEVHI being a comprehensive semi-structured interview, focuses on the phenomenology of VH,
EP
recurrence of VH and emotions or cognitions associated with VH. It can be completed by either patient or informant. It has been described in more detail elsewhere.(17) It has three sections: section 1
AC C
consisting of screening questions, section 2 referring to the duration and frequency of VH and section 3 assessing other perceptions, emotions, cognitions and behaviors associated with VH. In the present study, we assessed the patient and informant views about VH by interviewing patients and informants separately using NEVHI. Our hypothesis was that due to the intimate nature of hallucinations and owing to fact that some patients are reluctant to disclose their symptoms due to the fear of stigma(15) or concern towards caregivers,(4) patients would provide the most detailed description of hallucinations. In addition, the concurrent validity of informant-NEVHI was compared to the four item version of the NPI (NPI-4).
4
ACCEPTED MANUSCRIPT METHODS Subject recruitment This cross-sectional study was approved by the National Health Service (NHS) Local Research Ethics
RI PT
Committee. All procedures related to the study were fully explained to the participants and written informed consent was obtained prior to participation. Community based PD patients and their informants were approached via the movement disorder outpatient services of Newcastle upon Tyne Hospitals Trust and Gateshead Health NHS Trust (UK). PD was diagnosed by experienced consultant
SC
neurologists specialized in movement disorders and according to the Queen Square Brain Bank Clinical Diagnostic Criteria. Inclusion criteria diagnosis of PD, age ≥ 50 years, Mini Mental State
M AN U
Examination (MMSE) score ≥ 20, an informant willing to participate in the study and sharing the household with the patient. Of the 61 consecutive patient-informants pairs recruited, 59 patients fulfilled inclusion criteria and were assessed at their homes. Assessments
TE D
Demographic and medical variables of patients were assessed using a questionnaire. Binocular visual acuity, expressed in decimals (i.e. 1.0 vision = 100% vision; equals to 6/6 vision), was examined at a test distance of 40 cm.(24) MMSE(25) was used to assess cognition. PD medication dosage was
EP
expressed as levodopa (L-dopa) equivalent dose (LED).(26) Impairment in activities of daily living (ADL) and motor function were assessed using the Unified Parkinson’s disease rating scale (UPDRS)
AC C
part II and part III, respectively.(27)
Details of VH were assessed using the NEVHI,(17) which has been used before in PD patients.(1, 8, 11) The informant version of NEVHI (I-NEVHI) is similar to the patient version of NEVHI (PNEVHI), but all questions were rephrased to the informant perspective. PD patients and their informants were interviewed separately in a random order. Informants were also interviewed using the four-item version of the NPI (NPI-4), assessing delusions, hallucinations, depression and apathy.(28, 29) Statistical analysis 5
ACCEPTED MANUSCRIPT The Statistical Package for Social Sciences (SPSS Version 20) and the R (i386 Version 3.0.2) software was used for data analysis. Normal distribution of data was examined using Kolmogorov-Smirnov test. Means and standard deviations (SD) were calculated. Patient and informant ratings (P-NEVHI vs. I-NEVHI) were compared using the McNemar’s test (exact p-value based on binomial distribution) for
RI PT
prevalence and using Cohen’s kappa for inter-rater reliability. SPSS approximates the probability associated with the kappa value using a t-statistic. A Pearson product-moment correlation coefficient was computed to assess the relationship between hearing problem and the patient-informant agreement. The informants’ reporting of hallucinations using the two different questionnaires (I-
SC
NEVHI vs. NPI-4 hallucination rating) was compared using the Chi-square test; concurrent validity was calculated with the phi-coefficient (rphi). To evaluate the impact of cognitive impairment on
M AN U
patient reporting, the ratings of PD patients with cognitive impairment (PD-MMSE
S1064-7481(14)00571-5
DOI:
10.1016/j.jagp.2014.12.190
Reference:
AMGP 457
To appear in:
The American Journal of Geriatric Psychiatry
Received Date: 15 April 2014 Revised Date:
18 December 2014
Accepted Date: 25 December 2014
Please cite this article as: P. Urwyler, T. Nef, R.M Müri, A. Killen, D. Collerton, D. Burn, I. McKeith, U.P. Mosimann, Patients’ and Informants’ views on visual hallucinations in Parkinson’s disease, The American Journal of Geriatric Psychiatry (2015), doi: 10.1016/j.jagp.2014.12.190. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
2813
ACCEPTED MANUSCRIPT
Patients’ and Informants’ views on visual hallucinations in Parkinson’s disease Prabitha Urwyler, Ph.D.1, Tobias Nef, Ph.D.1,2, René M Müri, M.D.1,3, Alison Killen, M.Sc.4,
RI PT
Daniel Collerton, M.Sc.4,5, David Burn, M.D.4, Ian McKeith, M.D.4, Urs Peter Mosimann, M.D., Ph.D.1,6 *
Gerontechnology & Rehabilitation Group, University of Bern, Bern, Switzerland
2
ARTORG Center for Biomedical Engineering Research, University of Bern, Bern, Switzerland
3
Perception and Eye Movement Laboratory, Departments of Neurology and Clinical Research,
M AN U
SC
1
University Hospital Inselspital, University of Bern, Bern, Switzerland 4
Institute for Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
5
Northumberland, Tyne & Wear NHS Foundation Trust, Bensham Hospital, Gateshead, United
TE D
Kingdom
University Hospital of Old Age Psychiatry, University of Bern, Bern, Switzerland
*
Corresponding author: Urs Peter Mosimann, MD, PhD
EP
6
University Hospital of Old Age Psychiatry, Murtenstrasse 21, CH-3011 Bern, Switzerland
AC C
Email: [email protected] / Telephone: +41 31 632 8817 / Fax: +41 31 632 8944
Conflicts of Interest: No Disclosures to Report. Source of Funding: This research was funded by the National Institute for Health Research Newcastle Biomedical Research Unit (DB, IM), Parkinson’s UK (DB), Michael J Fox Foundation GSK (DB), GE Healthcare (IM), Gateshead Health NHS Foundation Trust (DC, UPM). For the remaining authors none were declared.
Visual hallucinations, Parkinson’s disease, inter-rater agreement
ACCEPTED MANUSCRIPT
ABSTRACT Objective: Visual hallucinations (VH) are a very personal experience and it is not clear whether
RI PT
information about them is best provided by informants or patients. Some patients may not share their hallucinatory experiences with caregivers to avoid distress, or due to fear of being labelled insane and others do not have informants at all, which limits the use of informant based questionnaires. The aim of this study was to compare patient’s and caregiver’s views about VH in Parkinson’s disease (PD),
SC
using the North-East-Visual-Hallucinations-Interview (NEVHI). Methods: Fifty nine PD patientinformant pairs were included. PD patients and informants were interviewed separately about VH
M AN U
using the NEVHI. Informants were additionally interviewed using the four-item version of the Neuropsychiatric Inventory (NPI-4). The inter-reliability and the concurrent validity of the different measures were compared. Results: VH were more commonly reported by patients than informants. The inter-rater agreement between NEVHI-patient and NEVHI-informant was moderate for complex
TE D
VH (Cohen’s kappa = 0.44, 95% CI= 0.13 - 0.75, t = 3.43, df = 58, p = 0.001) and feeling of presence (Cohen’s kappa = 0.35, 95% CI = 0.00 – 0.70, t = 2.75, df = 58, p = 0.006), but agreement was poor for illusions (Cohen’s kappa = 0.25, 95% CI = -0.07 – 0.57, t = 2.36, df = 58, p = 0.018) and passage hallucinations (Cohen’s kappa = 0.16, 95% CI = -0.04 – 0.36, t = 2.26, df = 58, p = 0.024).
EP
Conclusions: When assessing VH in PD patients, it is best to rely on patient information, because not
AC C
all patients share the details of their hallucinations with their caregivers.
Keywords: Visual hallucinations; Parkinson’s disease; inter-rater agreement.
2
ACCEPTED MANUSCRIPT
Visual Hallucinations (VH) are common in Parkinson’s disease (PD).(1) Their prevalence and severity increase as the disease progresses.(2) In cross-sectional studies, prevalence rates for VH range from 5% to 50%,(3-7) while longitudinal studies have shown that the prevalence of VH and behaviors
RI PT
associated with VH, increases over time reaching a life-time prevalence of up to 75%.(2, 8) Hallucinations which are sensory misperceptions are a very personal experience and their phenomenology is commonly classified into simple hallucinations,(9) complex hallucinations,(10, 11)
SC
visual illusions,(12) passing shadows(3) and the feeling of presence.(3, 13) Simple VH have the lowest degree of complexity and refer to flashes, dots, lines, shapes, swirly and pattern like grids or
M AN U
tiles. (9) Complex VH are phenomenologically rich and consist of formed images, e.g. faces, figures, objects, animals and landscapes.(10) Visual illusions are defined as visual percepts which are based on stimuli present in the extracorporeal space, but which are either misperceived or misinterpreted.(12) Passing shadows are perceptions are the perception of something fleeting like a shadow in the ‘corner of the eye’.(3) Feeling of presence is the feeling of a person being present in the room or house,
TE D
usually outside the range of ordinary perception.(13)
VH constitute a major source of distress for patients and caregivers,(4, 14) but are commonly
EP
underdiagnosed because health professionals don’t ask or patients do not disclose them spontaneously.(4, 15) Some patients do not volunteer their hallucinations(4, 15) either due to fears of
AC C
embarrassment,(16) for being classified as mentally ill(15) or due to the fear of stigmatization or restrictive institutionalization.(15) Still others do not want to impose any extra burden on spouses or friends. Hence, it is important for health professionals to ask about hallucinations in an indirect way without making any direct references to the hallucinations. Questions such as “Do you feel your eyes ever play tricks with you?” or “Have you seen something that other people could not see?” have been suggested to be helpful to screen for VH.(17)
3
ACCEPTED MANUSCRIPT Existing scales assessing VH rely either on informant or patient information or both. Self-assessment of VH in PD have been reported using the Non-Motor-Symptoms scale (NMSS),(18) University of Miami Parkinson's disease Hallucinations Questionnaire (UM-PDHQ),(19) Queen Square Visual Hallucination Inventory (QSVHI),(20) Tottori University Hallucinations Rating Scale (TUHARS),(21)
RI PT
North East Visual Hallucination Inventory (NEVHI),(1, 8, 11) and the Rush Hallucination Inventory.(22) The Neuropsychiatric Inventory (NPI),(23) is a composite neuropsychiatric assessment scale including hallucination which relies on informant information only, while the TUHARS and the NEVHI utilize both patient and informant reporting of VH. TUHARS assesses hallucinations in PD
SC
evaluating the variety, frequency, severity of hallucinations, degree of caregiver burden level, and psychiatric status at nighttime,(21) but it does not touch the phenomenology of VH and other
M AN U
characteristics (e.g. emotion and cognition) associated with VH. Most interviews developed have not been used across disorders except of NEVHI, which has been designed for patients with visual and / or cognitive impairments.(17) Moreover, some scales underestimate the frequency,(3) while other scales do not take the phenomenology into account(23) and it remains unclear whether the information is
TE D
best gathered by patients and or informants.
NEVHI being a comprehensive semi-structured interview, focuses on the phenomenology of VH,
EP
recurrence of VH and emotions or cognitions associated with VH. It can be completed by either patient or informant. It has been described in more detail elsewhere.(17) It has three sections: section 1
AC C
consisting of screening questions, section 2 referring to the duration and frequency of VH and section 3 assessing other perceptions, emotions, cognitions and behaviors associated with VH. In the present study, we assessed the patient and informant views about VH by interviewing patients and informants separately using NEVHI. Our hypothesis was that due to the intimate nature of hallucinations and owing to fact that some patients are reluctant to disclose their symptoms due to the fear of stigma(15) or concern towards caregivers,(4) patients would provide the most detailed description of hallucinations. In addition, the concurrent validity of informant-NEVHI was compared to the four item version of the NPI (NPI-4).
4
ACCEPTED MANUSCRIPT METHODS Subject recruitment This cross-sectional study was approved by the National Health Service (NHS) Local Research Ethics
RI PT
Committee. All procedures related to the study were fully explained to the participants and written informed consent was obtained prior to participation. Community based PD patients and their informants were approached via the movement disorder outpatient services of Newcastle upon Tyne Hospitals Trust and Gateshead Health NHS Trust (UK). PD was diagnosed by experienced consultant
SC
neurologists specialized in movement disorders and according to the Queen Square Brain Bank Clinical Diagnostic Criteria. Inclusion criteria diagnosis of PD, age ≥ 50 years, Mini Mental State
M AN U
Examination (MMSE) score ≥ 20, an informant willing to participate in the study and sharing the household with the patient. Of the 61 consecutive patient-informants pairs recruited, 59 patients fulfilled inclusion criteria and were assessed at their homes. Assessments
TE D
Demographic and medical variables of patients were assessed using a questionnaire. Binocular visual acuity, expressed in decimals (i.e. 1.0 vision = 100% vision; equals to 6/6 vision), was examined at a test distance of 40 cm.(24) MMSE(25) was used to assess cognition. PD medication dosage was
EP
expressed as levodopa (L-dopa) equivalent dose (LED).(26) Impairment in activities of daily living (ADL) and motor function were assessed using the Unified Parkinson’s disease rating scale (UPDRS)
AC C
part II and part III, respectively.(27)
Details of VH were assessed using the NEVHI,(17) which has been used before in PD patients.(1, 8, 11) The informant version of NEVHI (I-NEVHI) is similar to the patient version of NEVHI (PNEVHI), but all questions were rephrased to the informant perspective. PD patients and their informants were interviewed separately in a random order. Informants were also interviewed using the four-item version of the NPI (NPI-4), assessing delusions, hallucinations, depression and apathy.(28, 29) Statistical analysis 5
ACCEPTED MANUSCRIPT The Statistical Package for Social Sciences (SPSS Version 20) and the R (i386 Version 3.0.2) software was used for data analysis. Normal distribution of data was examined using Kolmogorov-Smirnov test. Means and standard deviations (SD) were calculated. Patient and informant ratings (P-NEVHI vs. I-NEVHI) were compared using the McNemar’s test (exact p-value based on binomial distribution) for
RI PT
prevalence and using Cohen’s kappa for inter-rater reliability. SPSS approximates the probability associated with the kappa value using a t-statistic. A Pearson product-moment correlation coefficient was computed to assess the relationship between hearing problem and the patient-informant agreement. The informants’ reporting of hallucinations using the two different questionnaires (I-
SC
NEVHI vs. NPI-4 hallucination rating) was compared using the Chi-square test; concurrent validity was calculated with the phi-coefficient (rphi). To evaluate the impact of cognitive impairment on
M AN U
patient reporting, the ratings of PD patients with cognitive impairment (PD-MMSE
