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Level I PD‐MCI Using Global Cognitive Tests and the Risk for Parkinson's Disease Dementia

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  • University of Canterbury and New Zealand Brain Research Institute

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Background: The criteria for PD-MCI allow the use of global cognitive tests. Their predictive value for conversion from PD-MCI to PDD, especially compared to comprehensive neuropsychological assessment, is unknown. Methods: The MDS PD-MCI Study Group combined four datasets containing global cognitive tests as well as a comprehensive neuropsychological assessment to define PD-MCI (n = 467). Risk for developing PDD was examined using a Cox model. Global cognitive tests were compared to neuropsychological test batteries (Level I&II) in determining risk for PDD. Results: PD-MCI based on a global cognitive test (MMSE or MoCA) increases the hazard for developing PDD (respectively HR = 2.57, P = 0.001; HR = 4.14, P = <0.001). The C-statistics for MMSE (0.72) and MoCA (0.70) were lower than those based on neuropsychological tests (Level I = 0.82; Level II = 0.81). Sensitivity, specificity and diagnostic accuracy balance was best in Level II. Conclusion: MMSE and MoCA predict conversion to PDD. However, Level II neuropsychological assessment seems the preferred assessment for PD-MCI.
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Level I PD-MCI Using Global Cognitive Tests
and the Risk for Parkinsons Disease
Dementia
Judith A. Boel, PhD,
1,2
Rob M.A. de Bie, MD, PhD,
1,3
Ben A. Schmand, PhD,
2,4
John C. Dalrymple-Alford, PhD,
5
Connie Marras, MD, PhD,
6
Charles H. Adler, MD, PhD,
7
Jennifer G. Goldman, MD, PhD,
8
Alexander I. Tröster, PhD,
9
David J. Burn, MD, PhD,
10
Irene Litvan, PhD,
11
and Gert J. Geurtsen PhD,
3,4,
*MDS Study Group Mild Cognitive Impairment in Parkinsons Disease
ABSTRACT: BackgroundBackground: The criteria for PD-MCI allow the use of global cognitive tests. Their predictive value
for conversion from PD-MCI to PDD, especially compared to comprehensive neuropsychological assessment, is
unknown.
MethodsMethods: The MDS PD-MCI Study Group combined four datasets containing global cognitive tests as well as a
comprehensive neuropsychological assessment to dene PD-MCI (n =467). Risk for developing PDD was
examined using a Cox model. Global cognitive tests were compared to neuropsychological test batteries (Level
I&II) in determining risk for PDD.
ResultsResults: PD-MCI based on a global cognitive test (MMSE or MoCA) increases the hazard for developing PDD
(respectively HR =2.57, P=0.001; HR =4.14, P=<0.001). The C-statistics for MMSE (0.72) and MoCA (0.70)
were lower than those based on neuropsychological tests (Level I =0.82; Level II =0.81). Sensitivity, specicity
and diagnostic accuracy balance was best in Level II.
ConclusionConclusion: MMSE and MoCA predict conversion to PDD. However, Level II neuropsychological assessment
seems the preferred assessment for PD-MCI.
The MDS PD Mild Cognitive Impairment (PD-MCI) diagnostic
criteria
1
operationalize two levels of cognitive assessment. Level I
assessment is based on a global cognitive test (Level I-GCT) or
an abbreviated neuropsychological assessment (Level I-NPA);
and Level II is based on a comprehensive neuropsychological
assessment. The use of a global cognitive test has some practical
advantages over both Level I-NPA and Level II in terms of time,
ease of administration, and costs. However, the diagnostic accu-
racy for current cognitive status (i.e. PD-MCI) when using
global cognitive tests is low compared to Level I-NPA and Level
II criteria.
2
The predictive value of global cognitive tests for pro-
gression from PD-MCI to Parkinson Disease Dementia (PDD)
needs to be determined.
Prior analyses using Level I-NPA and Level II methods
showed that PD-MCI diagnosed in these ways increases the haz-
ard of PDD and aids in the prediction of PDD (Level I-NPA
Hazard Ratio (HR) 2.0211.25; Level II HR 2.6914.10:
depending on cut-off used).
3,4
This study investigates the predic-
tive value of Level I-GCT, i.e. the Mini-Mental State Examina-
tion (MMSE) and Montreal Cognitive Assessment (MoCA), for
1
Department of Neurology, Amsterdam UMC Location University of Amsterdam, Amsterdam, The Netherlands;
2
Department of Psychology, University of Amsterdam,
Amsterdam, The Netherlands;
3
Amsterdam Neuroscience, Amsterdam, The Netherlands;
4
Department of Medical Psychology, Amsterdam UMC Location University of
Amsterdam, Amsterdam, The Netherlands;
5
New Zealand Brain Research Institute and School of Psychology, Speech and Hearing, University of Canterbury,
Christchurch, New Zealand;
6
Morton and Gloria Shulman Movement Disorders Centre and the Edmond J Safra Program in Parkinsons Disease, Toronto Western
Hospital, University of Toronto, Toronto, Canada;
7
Arizona Study of Aging and Neurodegenerative Disorders, Mayo Clinic Arizona, Scottsdale, Arizona, USA and
Banner Sun Health Research Institute, Sun City, Arizona, USA;
8
Department of Physical Medicine and Rehabilitation and Neurology, Shirley Ryan AbilityLab and
Northwestern University, Chicago, Illinois, USA;
9
Department of Clinical Neuropsychology and Center for Neuromodulation, Barrow Neurological Institute, Phoenix,
Arizona, USA;
10
Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, UK;
11
Parkinson and Other Movement Disorder Center, Department of
Neurosciences, University of California, San Diego, California, USA
*Correspondence to: Gert J. Geurtsen PhD, Meibergdreef 9, 1105AZ Amsterdam, The Netherlands. E-mail: g.j.geurtsen@amsterdamumc.nl
Keywords: dementia, mild cognitive impairment, global cognitive tests, Parkinsons disease, diagnostic accuracy.
Authors from the MDS Study Group Mild Cognitive Impairment in Parkinsons Disease are listed in the Acknowledgments.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited.
Received 27 December 2021; revised 7 March 2022; accepted 24 March 2022.
Published online 29 April 2022 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/mdc3.13451
MOVEMENT DISORDERS CLINICAL PRACTICE 2022; 9(4): 479483. doi: 10.1002/mdc3.13451 479
© 2022 AmsterdamUMC. Movement Disorders Clinical Practice published by Wiley Periodicals LLC on behalf of Movement Disorder Society.
BRIEF REPORT
CLINICAL PRACTICE
developing PDD. In addition, the predictive value of global cog-
nitive tests will be compared to Level I-NPA and Level II. This
will help to make a substantiated choice on how to assess PD-
MCI in research and clinical practice.
Methods
This study is based on data from the MDS Study Group Mild
Cognitive Impairment in Parkinsons Disease.
5
The methods are
briey described below (see publications for additional details).
3,4
Data Inclusion
This retrospective study combined four datasets containing global
cognitive tests and additional data suitable for both Level I and
Level II PD-MCI assessment based on neuropsychological tests.
Individual studies were included if they allowed Level II PD-
MCI assessment (i.e. at least two neuropsychological tests in each
of the ve cognitive domains at baseline
1
), included 75 patients
at baseline, had follow-up on PDD status for 67% of the base-
line population and had used the MMSE and/or the MoCA to
assess the global cognitive functioning. Four studies were
included.
2,68
Supplementary Figure S1 displays the inclusion
owchart and Supplementary Table S1 provides cohort details,
including PDD criteria. Demographic and clinical data were col-
lected. MDS-Unied Parkinsons disease rating scale (UPDRS)
9
scores were converted to have a uniform measure of UPDRS-
III,
3
subsequently referred to as UPDRS-III.
Application of the PD-MCI
Criteria
To determine PD-MCI by global cognitive tests, a cut-off of
<26 for the MoCA
10
and < 29 for the MMSE
11
were used con-
sidering these match prevailing cut-offs for PD-MCI used in PD
research and practice. Measures for subjective cognitive decline
varied between studies and are described in Supplementary
Table S1. A measure for functional independence at baseline was
not included as PDD was an exclusion criterion.
In short, for the neuropsychological assessment (NPA), either
one test per cognitive domain (Level I-NPA) or two tests per
cognitive domain (Level II) were used. PD-MCI based on the
NPA was dened as scores 1.5SD below the normative data
for at least two tests (respectively out of ve or ten).
3,4
Statistics
Multiple imputation (MI) was used to account for incomplete
data. Cox proportional hazards models were used to evaluate
whether Level I-CGT PD-MCI at baseline compared to no PD-
MCI adds to the risk of PDD as estimated by age, gender, level of
education, disease duration, UPDRS-III, and depression. Time
was measured from PD symptom onset until PDD or censoring.
To compare various operationalizations of the criteria, C-statistics
(bootstrap-corrected) which indicate discriminative ability between
models as a measure of goodness-of-t were calculated. PDD risk
factors, like time since symptom onset, were taken into consider-
ation. Two patients who develop PDD can be ordered by their
time to event (PDD). If the model rightly predicts a shorter time to
PDD for the one who developed PDD rst, the C-statistic
increases. Two patients, one of which develops PDD, can be
ordered as well. If the model rightly predicts a shorter time to PDD
for the one who developed PDD, the C statistic also increases.
In addition, at baseline we determined sensitivity, specicity,
positive predictive value (PPV), negative predictive value (NPV)
and diagnostic accuracy (DA) for PDD. This was done for Level
I-CGT as well as for Level I-NPA and Level II PD-MCI
assessment.
Results
A total of 467 patients were included (Table 1). Sixty-nine
patients (14.3%) developed PDD during follow-up (range 0.5
9 years).
Frequencies of PD-MCI
MMSE scores were available in all four datasets; MoCA scores
were available in three datasets. A total of 172 out of
467 (36.8%) patients fullled the criteria for PD-MCI based on
the MMSE. A total of 111 out of 365 (30.4%) patients fullled
the criteria for PD-MCI based on the MoCA. Applying Level II
resulted in 120/467 PD-MCI patients (25.7%), while level I-
NPA based on 5 tests resulted in 46/467 PD-MCI patients
(9.9%). Compared to Level I NPA, both Level II and Level I-
GCT identied more PD-MCI cases.
Predictive Value
The Cox proportional hazards models indicated a signicant
contribution of PD-MCI as dened by MMSE and MoCA cut-
off scores to the hazard of PDD (HRs respectively 2.57 and
4.14; see Supplementary Table 2). Age as well as UPDRS scores
TABLE 1 Baseline characteristics
N=467
Age, years (mean, SD) 68.7 (8.8)
Gender, male (frequency, %) 293 (62.7)
Education, years (mean, SD) 14.0 (3.1)
MMSE (median, IQR) 28.0 (2729)
MoCA (median, IQR) 25.0 (2328)
PD symptom duration, years (median, IQR) 4.0 (2.08.0)
UPDRS III (median, IQR) 20 (1328)
IQR, InterQuartile Range.
480 MOVEMENT DISORDERS CLINICAL PRACTICE 2022; 9(4): 479483. doi: 10.1002/mdc3.13451
BRIEF REPORT PD-MCI BASED ON GLOBAL COGNITIVE TESTS AND PDD RISK
were signicant contributors in the model including the MMSE
but not in the model including the MoCA.
Comparison of PD-MCI
Assessment Methods
The sensitivity and specicity were respectively: 67.7 and 68.1% for
Level I-GCT based on the MMSE; 57.1 and 75.9% for Level I-
CGT based on the MoCA; 32.8 and 94.7% for Level I-NPA; and
66.7 and 80.0% for level II (see Table 2). The Diagnostic Accuracy
(DA) was sufcient for the MMSE (67.7), good for MoCA (73.3)
and Level II (78.4) and very good for Level I-NPA (86.1). The
results in the three datasets with both MMSE and MoCA were
comparable. The MMSE has sufcient but limited sensitivity, speci-
city and DA. Level I-NPA and MoCA have a low sensitivity and
miss many cases. Specicity of the Level I-NPA is very high
resulting in a very good DA. Level II seems to have the most opti-
mal balance of sensitivity and specicity and a good DA.
The C-statistics were as follows: 0.72 for Level I-CGT based
on the MMSE; 0.70 for Level I-CGT based on the MoCA; 0.82
for Level I-NPA
4
; and 0.81 for level II.
4
The lower C-statistics
for MMSE and MoCA indicate lower added value to the risk for
PDD in comparison to level I-NPA and level II PD-MCI.
Discussion
Our results show that PD-MCI based on the global cognitive tests
MMSE and MoCA have predictive value for PDD. However,
given the higher hazard ratios of Level I-NPA and Level II
3,4
the
predictive value of MMSE and MoCA are lower. The ndings
were corrected for demographic and clinical characteristics known
to contribute to the hazard for PDD (age, sex, UDPRS III score).
The results are in line with previous studies indicating PD-MCI
based on neuropsychological assessment to be a risk factor for
PDD.
4,12
The signicantly higher hazard ratios for the develop-
ment of PDD for PD-MCI patients compared to patients with
normal cognition concurs with the concept of MCI as a transi-
tional stage between normal cognition and PDD.
No difference was found in the predictive value when com-
paring the MMSE and the MoCA. However, the C-statistic is
not well suited to pick up small differences between models and
comparisons based on this statistic should be interpreted with
caution. The reason we nd little difference in PDD prediction
between MMSE and MOCA in contrast to other mostly smaller
studies is unclear. The size of the studies as well as the variation
in cut-off points used for PD-MCI and PDD could have been of
inuence.
13
In a study including 132 patients Hoops et al.
(2009)
13
found the % correctly diagnosed based on MMSE and
MoCA to be equal as well, when using the same cut-offs. They
advised using MoCA due to the ceiling effect on the MMSE.
13
The MMSE and MoCA resulted in the higher percentage of
patients classied as PD-MCI (36.8 and 30.4% respectively) than
did the neuropsychological assessment (9.9% for level I-NPA;
25.7% for Level II). Global cognitive tests seemed to identify
PD-MCI cases who do not develop PDD, possibly false
positive,leading to lower C-statistics as well as a lower balance
in sensitivity and specicity. On the other hand, Level I-NPA
seems to be too limited and strict, as scores on 2 out of 5 tests
need to be below the cut-off, and therefore may miss patients
who actually have PD-MCI.
Overall we determined the sensitivity, specicity and DA in
the same patients. For the MMSE these values are sufcient but
limited, which corresponds with Hoops et al. (2009).
13
The sen-
sitivity of Level I-NPA and MoCA is lower indicating that many
cases are missed. However, the specicity of the Level I-NPA is
very high resulting in a good DA. Level II seems to have the
most optimal balance of sensitivity and specicity and has a good
DA, thus indicating that a Level II neuropsychological assessment
is preferred over the global cognitive tests.
Strengths of our study include the use of a large multicenter,
international sample, uniform application of the MDS PD-MCI
criteria, and direct comparison of the different prevailing
operationalizations of PD-MCI. Furthermore, while the relation
between PD-MCI, demographic and clinical characteristics, and
PDD has been reported separately in previous studies,
12,14
the
current study analyzed the effects jointly in the predictive
models. Limitations included different methods between cohorts
for patient recruitment, neuropsychological assessment, assess-
ment of motor signs and clinical PDD criteria. The length of
follow-up of the studies included differed. Therefore, the PDD
frequency varies. This potentially could inuence the determina-
tion of the sensitivity, specicity and diagnostic accuracy. How-
ever, as the analyses of sensitivity, specicity and diagnostic
accuracy were performed in the same groups comparability seems
TABLE 2 Sensitivity, specicity, NPV, PPV and diagnostic accuracy
MMSE MoCA Level I-NPA Level II
Sensitivity 67.7 57.1 32.8 66.7
Specicity 68.1 75.9 94.7 80.0
PPV 27.7 25.7 50.0 31.9
NPV 91.6 91.9 89.8 94.5
Diagnostic Accuracy 67.6 73.3 86.1 78.4
PPV, Positive Predictive Value; NPV, Negative Predictive Value.
MOVEMENT DISORDERS CLINICAL PRACTICE 2022; 9(4): 479483. doi: 10.1002/mdc3.13451 481
BOEL J.A. ET AL. BRIEF REPORT
adequate. When using a one point lower cut-off the % correctly
diagnosed in Level I-CGT hardly changed in a mixed PD-MCI
and PDD sample.
13
In conclusion, PD-MCI assessed by global cognitive tests
increases the hazard ratio for the development of PDD after tak-
ing age, sex, education, PD motor symptom severity, and
depression into account. This nding supports PD-MCI being a
risk factor for PDD. PD-MCI assessed by neuropsychological
assessment (both Level I and Level II) had higher predictive value
over PD-MCI assessed by MMSE or MoCA. Given better bal-
ance of sensitivity and specicity and Diagnostic Accuracy com-
pared to the use of global cognitive tests and Level I
neuropsychological assessment, Level II neuropsychological
assessment seems the optimal method for detecting PD-MCI.
Acknowledgments
This study was conducted on behalf of the International
Parkinson and Movement Disorders Society Mild Cognitive
Impairment (MCI) Study Group, consisting of the byline authors
as well as the members listed here: Bryan Bernard PhD, Glenn
Stebbins PhD, J. Vincent Filoteo PhD, Daniel Weintraub PhD,
John N. Caviness MD, Christine Belden PhD, Cyrus
P. Zabetian MD, Brenna A. Cholerton PhD, Xuemei Huang
PhD, Paul J. Eslinger PhD, James B. Leverenz MD, Sarah Duff-
Canning PhD, Matt Farrer PhD, Tim J. Anderson FRACP,
Daniel J Myall PhD, Sharon L. Naismith PhD, Simon JG Lewis
MD, Glenda M. Halliday PhD, Ruey-Meei Wu MD PhD, Car-
oline H. Williams-Gray MRCP PhD, David P. Breen MRCP
PhD, Roger A. Barker MRCP PhD, Alison J. Yarnall MRCP
PhD, Martin Klein PhD, Brit Mollenhauer MD, Claudia
Trenkwalder MD. Jaime Kulisevsky MD PhD. Javier
Pagonabarraga MD. PhD. Carmen Gasca-Salas MD. PhD. Maria
C. Rodriguez-Oroz MD. PhD. Carme Junque PhD. Barbara
Segura PhD. Paolo Barone PhD, Gabriella Santangelo PhD,
Davide M Cammisuli PhD, Roberta Biundo PhD, Angelo
Antonini PhD, Luca Weis PhD, Kenn Freddy Pedersen PhD
and Guido Alves PhD. Additional details on these authors are
available in the Supplemental Appendix 1.
Author Roles
(1) Research project: A. Conception, B. Organization, C. Execution;
(2) Statistical Analysis: A. Design, B. Execution, C. Review and Cri-
tique; (3) Manuscript: A. Writing of the rst draft, B. Review and
Critique.
JAB: 1A, 1B, 1C, 2A, 2B, 2C, 2A, 2B, 2C.
RMAB: 1A, 3A, 3B.
BAS: 1A, 1B, 2C, 3A, 3B.
JDA: 1A, 1B, 3B.
CM: 1A, 3B.
CHA: 1A, 3B.
JGG: 1A, 3B.
AIT: 1A, 3B.
DJB: 1A, 3B.
IL: 1A, 3B.
GJG: 1A, 1B, 1C, 2A, 2C, 3A, 3B.
Disclosures
Ethical Compliance Statement: The Medical Ethics Com-
mittee of the University of Amsterdam stated that the approval
of an institutional review board was not required for this work
(reference number W12_31 # 13.17.0003). Each study site
obtained informed consent obtained. We conrm that we have
read the Journals position on issues involved in ethical publica-
tion and afrm that this work is consistent with those guidelines.
Funding Sources and Conicts of Interest: Funding was
received from the Michael J. Fox Foundation. The authors have
no conicts of Interest for this study.
Financial Disclosures for the Previous 12 Months: Judith A.
Boel, Rob M.A. de Bie, Ben A. Schmand, Jennifer G. Goldman,
Alexander I. Tröster, David J. Burn, and Gert J. Geurtsen have no
disclosures to report. John C. Dalrymple-Alford, None, only grants
from Tertiary Education Commission, New Zealand, Health
Research Council of New Zealand, Canterbury Medical Research
Foundation and Neurological Foundation of New Zealand. Con-
nie Marras is a consultant for Gray Matter Technologies and
receives nancial compensation as a steering committee member
from the Michael J Fox Foundation. She received grants from The
Michael J Fox Foundation, Canadian Institutes of Health Research,
Parkinsons Foundation (US), International Parkinson and Move-
ment Disorders Society, Weston Brain Institute, Theravance Inc,
Centogene. Charles H. Adler has Stock Ownership in medically-
related elds: Cionic; Consultancies: Avion, CND Life Science,
Jazz Pharm, Neurocrine; Grants: NIH, Michael J. Fox Foundation,
Arizona Biomedical Research Commission. Irene Litvansresearch
is supported by the National Institutes of Health grants:
2R01AG038791-06A, U01NS100610, U01NS80818,
R25NS098999; U19 AG063911-1 and 1R21NS114764-01A1;
the Michael J Fox Foundation, Parkinson Foundation, Lewy Body
Association, CurePSP, Roche, Abbvie, Biogen, Centogene. EIP-
Pharma, Biohaven Pharmaceuticals, Novartis, Brain Neurotherapy
Bio and United Biopharma SRLUCB. She was a member of
the Scientic Advisory Board of Lundbeck and is a Scienticadvi-
sor for Amydis. She receives her salary from the University of Cali-
fornia San Diego and as Chief Editor of Frontiers in Neurology.
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Supporting Information
Supporting information may be found in the online version of
this article.
Supplementary Figure S1. Flowchart showing the data
inclusion process
Supplementary Table S1. Cohort details of the included
studies.
Supplementary Table S2. Hazard ratios of models con-
taining MMSE and MoCA.
Supplementary Text S1. Members of the International
Parkinson and Movement Disorders Society Mild Cognitive
Impairment (MCI) Study Group.
MOVEMENT DISORDERS CLINICAL PRACTICE 2022; 9(4): 479483. doi: 10.1002/mdc3.13451 483
BOEL J.A. ET AL. BRIEF REPORT
... For instance, an assessment with at least one test for each of the five cognitive domains independently contributed to the hazard of PDD [32]. Similarly, Boel et al. [33] found that MMSE and MoCA predicted the conversion to PDD and level I neuropsychological assessment showed good diagnostic accuracy (86%); (iii) we could not enroll a sufficient number of early-stage patients with PD due to the selection bias in our Parkinson Center (tertiary referral hospital for PD). However, meaningful information regarding distinct cognitive trajectories was provided by including patients with at least 3 years of consecutive neuropsychological assessments. ...
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Background and Objectives: Cognitive impairment is common at all stages in Parkinson's disease (PD). However, the field is hampered by consensus over which neuropsychological tests to use and how to utilize the results generated by a cognitive battery. An option that combines the richness of a neuropsychological battery with the simplicity of a single test score is a cognitive summary score (CSS). The objective was to determine if a CSS created using robust norming is sensitive in detecting early cognitive deficits in de novo, untreated PD. Methods: Using baseline cognitive data from PD participants and healthy controls (HCs) in the Parkinson's Progression Markers Initiative, these steps were taken: (1) creating a robust HC subgroup that did not demonstrate cognitive decline over time; (2) using the robust HC subgroup to create regression-based internally-derived standardized scores (z-scores) for six cognitive scores across five tests; and (3) creating a CSS by averaging all standardized test z-scores. Results: PD participants scored worse than HCs on all cognitive tests, with a larger effect size (PD versus HCs) when the comparison group was the robust HC subgroup compared with all HCs. Applying internally-derived norms rather than published norms, the largest cognitive domain effect sizes (PD vs. robust HCs) were for processing speed/working memory (Cohen's d= -0.55) and verbal episodic memory (Cohen's d= -0.48 and -0.52). In addition, using robust norming shifted PD performance from the middle of the average range (CSS z-score= -0.01) closer to low average (CSS z-score= -0.40), with the CSS having a larger effect size (PD vs. robust HC subgroup; Cohen's d= -0.60) compared with all individual cognitive tests. Discussion: PD patients perform worse cognitively than HC at disease diagnosis on multiple cognitive domains, particularly information processing speed and verbal memory. Using robust norming increases effect sizes and lowers the scores of PD patients to "expected" levels. The CSS performed better than all individual cognitive tests. A CSS developed using a robust norming process may be sensitive to cognitive changes in the earliest stages of PD and have utility as an outcome measure in clinical research, including clinical trials.
... Assess the full spectrum of PD-related CI (i.e., PD-SCD, PD-MCI, PD-D) using validated and sensitive methods (i.e., level-II neuropsychological assessment) [87] Include prodromal PD patients (e.g., RBD) to explore whether early multimodal cognitionbased approaches may slow the onset of cognitive decline Neuropsychiatric non-motor comorbidities Assess neuropsychiatric non-motor symptoms (e.g., apathy, depression, anxiety, ICD) given their potential impact on PD-related CI [82] Other individual patient variables potentially moderating treatment effects ...
Article
Purpose of review. Cognitive impairment is one of the most challenging non-motor symptoms of Parkinson’s disease (PD) and may occur during all PD stages. There are no established pharmacological treatments for PD-related cognitive impairment, which may be improved by cognition-based interventions (i.e., cognitive stimulation, cognitive training, cognitive rehabilitation). Multimodal cognition-based interventions by adjunctive drugs, exercise, non-invasive brain stimulation and technologies may be effective in PD. Recent findings. Exercise combined with cognitive training may enhance global, memory, visuospatial and executive functioning, transcranial direct current stimulation delivered alongside cognitive training may improve attention and executive functioning, and exergames, semi-immersive virtual reality (VR) and telerehabilitation plus non-immersive VR combined with cognitive training may ameliorate global and executive functioning in PD patients. Summary. The evidence reviewed here, despite preliminary, is very encouraging and suggests strong rationale for combining pharmacological and non-pharmacological interventions with cognition-based treatments in PD. To overcome limitations of current studies, we propose some recommendations for future trials on drugs, exercise, non-invasive brain stimulation and technologies combined with cognition-based treatments for cognitive impairment in PD.
... Due to the relative scarcity of suitable subjects, further studies should encompass multi-site endeavours to collect datasets of sufficient size where more detailed hypotheses related to cognitive decline in STN DBS could be evaluated Secondly, the only outcome measure of cognitive function in the presented study was DRS-2. Although previously validated for use in PD patients in a Czech population and appropriately suitable for cognitive screening of global cognition, DRS-2 does not appear to have utility in evaluating single cognitive functions in PD (Lopez et al., 2023;Boel et al., 2022). Further studies using more complex assessment of cognition (e.g. level II diagnosis of PD-MCI) will be necessary to evaluate whether our results correspond to the type of cognitive deficit which may develop after DBS implantation. ...
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Background and objectives The intricate relationship between deep brain stimulation (DBS) in Parkinson’s disease (PD) and cognitive impairment has lately garnered substantial attention. The presented study evaluated pre-DBS structural and microstructural cerebral patterns as possible predictors of future cognitive decline in PD DBS patients. Methods Pre-DBS MRI data in 72 PD patients were combined with neuropsychological examinations and follow-up for an average of 2.3 years after DBS implantation procedure using a screening cognitive test validated for diagnosis of mild cognitive impairment in PD in a Czech population – Dementia Rating Scale 2. Results PD patients who would exhibit post-DBS cognitive decline were found to have, already at the pre-DBS stage, significantly lower cortical thickness and lower microstructural complexity than cognitively stable PD patients. Differences in the regions directly related to cognition as bilateral parietal, insular and cingulate cortices, but also occipital and sensorimotor cortex were detected. Furthermore, hippocampi, putamina, cerebellum and upper brainstem were implicated as well, all despite the absence of pre-DBS differences in cognitive performance and in the position of DBS leads or stimulation parameters between the two groups. Conclusions Our findings indicate that the cognitive decline in the presented PD cohort was not attributable primarily to DBS of the subthalamic nucleus but was associated with a clinically silent structural and microstructural predisposition to future cognitive deterioration present already before the DBS system implantation.
Article
Background Cognitive impairment is common at all stages of Parkinson's disease (PD), but there is no consensus on which neuropsychological tests to use or how to interpret cognitive battery results. A cognitive summary score (CSS) combines the richness of a neuropsychological battery with the simplicity of a single score. Objective The objective of this study was to determine whether a CSS created using robust norming can detect early cognitive deficits in de novo, untreated PD. Methods Baseline cognitive data from PD participants and healthy control participants (HCs) in the Parkinson's Progression Markers Initiative were used to (1) create a robust HC subgroup without cognitive decline, (2) generate regression‐based z scores for six cognitive measures using this subgroup, and (3) create a CSS by averaging all z scores. Results PD participants scored worse than HCs on all cognitive tests, with larger effects when compared with the robust HC subgroup rather than all HCs. Applying internally derived norms, the largest effects were for processing speed/working memory (Cohen's d = −0.55) and verbal episodic memory (Cohen's d = −0.48 and −0.52). Robust norming shifted PD performance from average (CSS z score = −0.01) to low average (CSS z score = −0.40), with a larger effect for the CSS (PD vs. robust HC subgroup; Cohen's d = −0.60) compared with individual tests. Conclusions Patients with PD perform worse cognitively than HCs, particularly in processing speed and verbal memory. Robust norming increases effect sizes and decreases PD scores to expected levels. The CSS outperformed individual tests and may detect cognitive changes in early PD, making it a useful outcome measure in clinical research. © 2025 The Author(s). Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.
Article
OBJECTIVE Lewy body dementia (LBD) is an umbrella term describing two closely related conditions: Parkinson disease dementia (PDD) and dementia with Lewy bodies (DLB). LBD is the second most common cause of neurodegenerative dementia but is often underrecognized in clinical practice. This review covers the key epidemiologic, clinical, cognitive, behavioral, and biomarker features of LBD and discusses current treatment options. LATEST DEVELOPMENTS Indicative biomarkers of LBD improve the ability to make a diagnosis and include single-photon emission computed tomography (SPECT) of the dopamine system (brain) and the noradrenergic system (cardiac), and polysomnography. α-Synuclein–specific biomarkers in spinal fluid, skin, plasma, and brain imaging are in active development with some available for clinical use. Prodromal stages of PDD and DLB have been contextualized, and diagnostic criteria have been published. An emerging theme is whether an integrated staging system focusing on protein aggregation, rather than clinical symptoms, may advance research efforts. ESSENTIAL POINTS LBD is a common cause of cognitive impairment in older adults but is often subject to significant delays in diagnosis and treatment, increasing the burden on patients and family care partners. Understanding key features of disease and the use of biomarkers will improve recognition. Earlier detection may also facilitate the development of new therapeutics and enrollment in clinical trials.
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Background and objective Cognitive impairment and dementia as well as affective disorders are common and debilitating syndromes that develop in people with Parkinson’s disease (PwPD). The authors summarized recommendations for the 2023 updated German guidelines on “Parkinson’s disease” from the German Neurological Society (DGN), focusing on the diagnosis and treatment of these disorders. Methods The recommendations were based on literature reviews, other relevant guidelines, and expert opinions. Results Measurements to assess cognitive and affective states were reviewed for psychometric properties, use in routine clinical practice, and availability in German. To improve mild cognitive impairment, cognitive training and physical aerobic training are recommended. To treat Parkinson’s disease (PD)-related dementia, cognitive stimulation (as a non-pharmacological intervention) and acetylcholinesterase inhibitors (AChEIs, i.e., rivastigmine) are recommended. Cognitive behavioral therapy is recommended to treat depression, anxiety, and fear of progression. Physical interventions are recommended to treat depression, fatigue, and apathy. Optimized dopaminergic treatment is the first-line pharmacological strategy recommended to manage depression, apathy, anhedonia, fatigue, and mood swings. Major depression can be additionally treated using venlafaxine or desipramine, while moderate depression can be treated pharmacologically according to its clinical phenotype (psychomotor retardation or agitation) and comorbidities (e.g., sleep disturbances, pain). Venlafaxine and nortriptyline can be used to treat anhedonia, while citalopram can be used for anxiety. Conclusions In addition to the updated pharmacological treatment options, new insights into recommendations for standardized diagnostics and non-pharmacological interventions were provided for the German health care system. However, more studies are needed to explore the full potential of non-pharmacological interventions to treat and prevent cognitive impairment and affective disorders.
Article
Background: Mild cognitive impairment in Parkinson's disease (PD-MCI) includes deficits in different cognitive domains, and one domain to explore for neurocognitive impairment following the DSM-V is social cognition. However, this domain is not included in current criteria for PD-MCI diagnosis. Moreover, tests vary across studies. It is, therefore, crucial to optimize cognitive assessment in PD-MCI. We aimed to do so by using Machine Learning. Methods: 275 PD patients were included. Four cognitive batteries were created: two Standard ones (Levels I and II), applying current criteria and “traditional” tests; two Alternative ones (Levels I and II), which incorporated a test of social cognition. These batteries were included in the Random Forest (RF) classifier. To assess RF performance, the AUC was considered, and the Variable Importance Index was estimated to understand the contribution of each test in PD-MCI classification. Results: Standard Level I and II showed an AUC of 0.852 and 0.892, while Alternative Level I and II showed an AUC of 0.898 and of 0.906. Variable Importance Index revealed that TMT B-A, Ekman test, RAVLT-IR, MoCA, and Action Naming were tests that most contributed to PD-MCI classification. Conclusion: The alternative level I assessment demonstrated a similar classification capacity to the standard level II assessment. This finding suggests that in the cognitive assessment of PD patients, it is crucial to consider the most affected cognitive domains in this clinical population, including social cognition. Taken together, these results suggest to revise current criteria for the diagnosis of PD-MCI.
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Background Cognitive impairment is a common nonmotor manifestation of Parkinson's disease, with deficits ranging from mild cognitive difficulties in 1 or more of the cognitive domains to severe dementia. The International Parkinson and Movement Disorder Society commissioned the assessment of the clinimetric properties of cognitive rating scales measuring global cognitive performance in PD to make recommendations regarding their use. Methods A systematic literature search was conducted to identify the scales used to assess global cognitive performance in PD, and the identified scales were reviewed and rated as “recommended,” “recommended with caveats,” “suggested,” or “listed” by the panel using previously established criteria. Results A total of 12 cognitive scales were included in this review. Three scales, the Montreal Cognitive Assessment, the Mattis Dementia Rating Scale Second Edition, and the Parkinson's Disease-Cognitive Rating Scale, were classified as “recommended.” Two scales were classified as “recommended with caveats”: the Mini-Mental Parkinson, because of limited coverage of executive abilities, and the Scales for Outcomes in Parkinson's Disease-Cognition, which has limited data on sensitivity to change. Six other scales were classified as “suggested” and 1 scale as “listed.” Conclusions Because of the existence of “recommended” scales for assessment of global cognitive performance in PD, this task force suggests that the development of a new scale for this purpose is not needed at this time. However, global cognitive scales are not a substitute for comprehensive neuropsychological testing. © 2017 International Parkinson and Movement Disorder Society
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Dementia in Parkinson's disease (PD) is a serious health issue and a major concern for many patients. In most cases mild cognitive impairment (MCI) is considered a transitional stage between normal cognitive functioning and dementia which is of potential importance in the early identification of patients at risk for dementia. Recently, the Movement Disorder Society (MDS) proposed diagnostic criteria for MCI in PD (PD-MCI). These criteria comprise two operationalizations: Level I (based on an abbreviated assessment) and Level II (based on comprehensive neuropsychological evaluation permitting MCI subtyping). These criteria need to be validated. This paper describes a project aiming to validate the MDS PD-MCI criteria by pooling and analyzing cross-sectional and longitudinal neuropsychological databases comprising ≥5,500 PD patients and ≥1,700 controls. After applying the MDS PD-MCI Level I and Level II criteria, rates of conversion to PD-dementia and predictive variables for conversion to PD-dementia will be established. This study will also assist in identifying whether revisions of the PD-MCI criteria are required.
Article
Background The International Parkinson and Movement Disorders Society criteria for mild cognitive impairment in PD need validation. The objectives of this present study were to evaluate prognostic validity of level I (abbreviated) International Parkinson and Movement Disorders Society mild cognitive impairment in PD criteria for development of PD dementia and compared them with level II (comprehensive) criteria. Methods We analyzed data from 8 international studies (1045 patients) from our consortium that included baseline data on demographics, motor signs, depression, detailed neuropsychological testing, and longitudinal follow‐up for conversion to Parkinson's disease dementia. Survival analysis evaluated their contribution to the hazard of Parkinson's disease dementia. Results Level I mild cognitive impairment in PD, increasing age, male sex, and severity of PD motor signs independently increased the hazard of Parkinson's disease dementia. Level I and level II mild cognitive impairment in PD classification had similar discriminative ability with respect to the time to Parkinson's disease dementia. Conclusions Level I mild cognitive impairment in PD classification independently contributes to the hazard of Parkinson's disease dementia. This finding supports the prognostic validity of the abbreviated mild cognitive impairment in PD criteria. © 2019 International Parkinson and Movement Disorder Society
Article
Background: The International Parkinson and Movement Disorder Society criteria for mild cognitive impairment in PD were recently formulated. Objectives: The aim of this international study was to evaluate the predictive validity of the comprehensive (level II) version of these criteria by assessment of their contribution to the hazard of PD dementia. Methods: Individual patient data were selected from four separate studies on cognition in PD that provided information on demographics, motor examination, depression, neuropsychological examination suitable for application of level II criteria, and longitudinal follow-up for conversion to dementia. Survival analysis evaluated the predictive value of level II criteria for cognitive decline toward dementia as expressed by the relative hazard of dementia. Results: A total of 467 patients were included. The analyses showed a clear contribution of impairment according to level II mild cognitive impairment criteria, age, and severity of PD motor symptoms to the hazard of dementia. There was a trend of increasing hazard of dementia with declining neuropsychological performance. Conclusions: This is the first large international study evaluating the predictive validity of level II mild cognitive impairment criteria for PD. The results showed a clear and unique contribution of classification according to level II criteria to the hazard of PD dementia. This finding supports their predictive validity and shows that they contribute important new information on the hazard of dementia, beyond known demographic and PD-specific factors of influence. © 2017 International Parkinson and Movement Disorder Society.
Article
Background The International Parkinson and Movement Disorders Society criteria for mild cognitive impairment in Parkinson’s disease were recently formulated. Objectives The aim of this international study was to evaluate the predictive validity of the comprehensive (level II) version of these criteria by assessment of their contribution to the hazard of Parkinson’s disease dementia. Methods Individual patient data were selected from four separate studies on cognition in Parkinson’s disease that provided information on demographics, motor examination, depression, neuropsychological examination suitable for application of level II criteria, and longitudinal follow-up for conversion to dementia. Survival analysis evaluated the predictive value of level II criteria for cognitive decline towards dementia as expressed by the relative hazard of dementia. Results A total of 467 patients were included. The analyses showed a clear contribution of impairment according to level II mild cognitive impairment criteria, age and severity of Parkinson’s disease motor symptoms to the hazard of dementia. There was a trend of increasing hazard of dementia with declining neuropsychological performance. Conclusions This is the first large international study evaluating the predictive validity of level II mild cognitive impairment criteria for Parkinson’s disease. The results showed a clear and unique contribution of classification according to level II criteria to the hazard of Parkinson’s disease dementia. This finding supports their predictive validity and shows that they contribute important new information on the hazard of dementia, beyond known demographic and Parkinson’s disease specific factors of influence.
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Introduction: Mild cognitive impairment is common in nondemented Parkinson disease patients (PD-MCI) and is considered as a risk factor for dementia (PDD). Recently, the Movement Disorder Society (MDS) published guidelines for PD-MCI, although the studies available are still limited. The aim of this work was to characterize PD-MCI and its progression to dementia. Moreover, the study variables could be considered as predictors for the progression of cognitive impairment. Method: The study included 43 patients with idiopathic PD (mean age = 59.19 years, SD = 9.64) and 20 healthy and neurologically normal controls (mean age = 60.85 years, SD = 12.26). The criteria proposed by the MDS Task Force were applied for the PD-MCI diagnosis. Follow-up assessments were conducted within six to eight years after the diagnosis of PD-MCI. Results: The results showed that 60.5% of the patients were diagnosed with PD-MCI when a comprehensive assessment was performed (MDS criteria Level 2), while 23.3% of the patients met MCI criteria when a brief assessment was used (MDS criteria Level 1). Multiple domain impairment was the most frequent impairment (96.2%). A total of 42.3% of PD-MCI patients had dementia in the follow-up study. Logistic regression showed that the Hoehn and Yahr stage and education significantly contributed to the prediction of PD-MCI. Moreover, the Hoehn and Yahr stage and memory domain significantly contributed to the prediction of dementia. Conclusions: The results of the study: (a) provide relevant data about the process of validation of the MDS PD-MCI criteria, (b) reinforce the hypothesis that PD-MCI is more frequent than previous studies showed without applying MDS criteria, and (c) confirm that PD-MCI is a risk factor for the onset of dementia. Finally, the study shows that neurological impairment, educational level and memory impairment were predictors for the progression of cognitive impairment.
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The Brain and Body Donation Program (BBDP) at Banner Sun Health Research Institute (http://www.brainandbodydonationprogram.org) started in 1987 with brain-only donations and currently has banked more than 1600 brains. More than 430 whole-body donations have been received since this service was commenced in 2005. The collective academic output of the BBDP is now described as the Arizona Study of Aging and Neurodegenerative Disorders (AZSAND). Most BBDP subjects are enrolled as cognitively normal volunteers residing in the retirement communities of metropolitan Phoenix, Arizona. Specific recruitment efforts are also directed at subjects with Alzheimer's disease, Parkinson's disease and cancer. The median age at death is 82. Subjects receive standardized general medical, neurological, neuropsychological and movement disorders assessments during life and more than 90% receive full pathological examinations by medically licensed pathologists after death. The Program has been funded through a combination of internal, federal and state of Arizona grants as well as user fees and pharmaceutical industry collaborations. Subsets of the Program are utilized by the US National Institute on Aging Arizona Alzheimer's Disease Core Center and the US National Institute of Neurological Disorders and Stroke National Brain and Tissue Resource for Parkinson's Disease and Related Disorders. Substantial funding has also been received from the Michael J. Fox Foundation for Parkinson's Research. The Program has made rapid autopsy a priority, with a 3.0-hour median post-mortem interval for the entire collection. The median RNA Integrity Number (RIN) for frozen brain and body tissue is 8.9 and 7.4, respectively. More than 2500 tissue requests have been served and currently about 200 are served annually. These requests have been made by more than 400 investigators located in 32 US states and 15 countries. Tissue from the BBDP has contributed to more than 350 publications and more than 200 grant-funded projects. © 2015 Japanese Society of Neuropathology.
Article
Cognitive impairment is one of the earliest, most common, and most disabling non-motor symptoms in Parkinson's disease (PD). Thus, routine screening of global cognitive abilities is important for the optimal management of PD patients. Few global cognitive screening instruments have been developed for or validated in PD patients. The Mini-Mental State Examination (MMSE), Montreal Cognitive Assessment (MoCA), and Dementia Rating Scale-2 (DRS-2) have been used extensively for cognitive screening in both clinical and research settings. Determining how to convert the scores between instruments would facilitate the longitudinal assessment of cognition in clinical settings and the comparison and synthesis of cognitive data in multicenter and longitudinal cohort studies. The primary aim of this study was to apply a simple and reliable algorithm for the conversion of MoCA to MMSE scores in PD patients. A secondary aim was to apply this algorithm for the conversion of DRS-2 to both MMSE and MoCA scores. The cognitive performance of a convenience sample of 360 patients with idiopathic PD was assessed by at least two of these cognitive screening instruments. We then developed conversion scores between the MMSE, MoCA, and DRS-2 using equipercentile equating and log-linear smoothing. The conversion score tables reported here enable direct and easy comparison of three routinely used cognitive screening assessments in PD patients. © 2014 International Parkinson and Movement Disorder Society
Article
We examined the frequency of Parkinson disease with mild cognitive impairment (PD-MCI) and its subtypes and the accuracy of 3 cognitive scales for detecting PD-MCI using the new criteria for PD-MCI proposed by the Movement Disorders Society. Nondemented patients with Parkinson's disease completed a clinical visit with the 3 screening tests followed 1 to 3 weeks later by neuropsychological testing. Of 139 patients, 46 met Level 2 Task Force criteria for PD-MCI when impaired performance was based on comparisons with normative scores. Forty-two patients (93%) had multi-domain MCI. At the lowest cutoff levels that provided at least 80% sensitivity, specificity was 44% for the Montreal Cognitive Assessment and 33% for the Scales for Outcomes in Parkinson's Disease-Cognition. The Mini-Mental State Examination could not achieve 80% sensitivity at any cutoff score. At the highest cutoff levels that provided specificity of at least 80%, sensitivities were low (≤44%) for all tests. When decline from estimated premorbid levels was considered evidence of cognitive impairment, 110 of 139 patients were classified with PD-MCI, and 103 (94%) had multi-domain MCI. We observed dramatic differences in the proportion of patients who had PD-MCI using the new Level 2 criteria, depending on whether or not decline from premorbid level of intellectual function was considered. Recommendations for methods of operationalizing decline from premorbid levels constitute an unmet need. Among the 3 screening tests examined, none of the instruments provided good combined sensitivity and specificity for PD-MCI. Other tests recommended by the Task Force Level 1 criteria may represent better choices, and these should be the subject of future research. © 2013 Movement Disorder Society.
Article
Mild cognitive impairment is common in nondemented Parkinson's disease (PD) patients and may be a harbinger of dementia. In view of its importance, the Movement Disorder Society commissioned a task force to delineate diagnostic criteria for mild cognitive impairment in PD. The proposed diagnostic criteria are based on a literature review and expert consensus. This article provides guidelines to characterize the clinical syndrome and methods for its diagnosis. The criteria will require validation, and possibly refinement, as additional research improves our understanding of the epidemiology, presentation, neurobiology, assessment, and long-term course of this clinical syndrome. These diagnostic criteria will support future research efforts to identify at the earliest stage those PD patients at increased risk of progressive cognitive decline and dementia who may benefit from clinical interventions at a predementia stage.