ORIGINAL COMMUNICATION

The Movement Disorders Society criteria for the diagnosisof Parkinson’s disease dementia: their usefulness and limitationsin elderly patients

Michele Kiesmann • Jean-Baptiste Chanson •

Julien Godet • Thomas Vogel • Laetitia Schweiger •

Saıd Chayer • Georges Kaltenbach

Received: 25 March 2013 / Revised: 5 June 2013 / Accepted: 20 June 2013

� Springer-Verlag Berlin Heidelberg 2013

Abstract The aim of this study was to assess the per-

formance of the Movement Disorders Society (MDS) cri-

teria for the diagnosis of Parkinson’s disease dementia

(PDD) in the elderly, and also to evaluate the relevance of

applying other tests in this patient population. The MDS

criteria include a first short part in checklist form, and a

second part which is used as a basis for reference and

consists of an in-depth neuropsychological examination.

Forty consecutive PD patients presenting with cognitive

complaints were enrolled. An assessment was made of the

performances of the MDS checklist compared with the

MDS exhaustive cognitive examination which was used as

a basis for reference, and with other cognitive tests

including the Mattis Dementia Rating Scale (MDRS), the

French version of the Grober and Buschke test, the verbal

fluency test, the Rey–Osterreith complex figure and the

paced auditory serial addition test. Out of a total of 40 PD

subjects (mean age: 80.5 ± 4.9 years), 20 were diagnosed

with PDD according to the checklist and 31 on the basis of

the exhaustive examination, i.e. with 11 more patients

diagnosed via the latter. The sensitivity of the checklist for

the diagnosis of PDD was 0.64, with a specificity of 1.00.

The use of the MDRS for PDD diagnosis with a cut-off at

B120 showed a sensitivity of 0.80 and a specificity of 1.00,

while at B132 it displayed a sensitivity of 1.00 and a

specificity of 0.444. The specificity of the checklist for the

diagnosis of PDD in the elderly was confirmed, but it was

lacking in sensitivity. It was also found that the MDRS

could be helpful in the diagnosis and screening of PDD.

Keywords Parkinson’s disease � Dementia � Cognitive

disorder � Memory � Elderly

Introduction

Parkinson’s disease (PD) has been reported to affect more

than 1 % of elderly patients over the age of 65 years, and

2.6 % of those between 85 and 89 years [1]. Some studies

[2–5] have found that between 22 and 48 % of the patients

with PD have cognitive disorders, and that Parkinson’s

disease dementia (PDD) may develop in up to 80 % of

surviving PD patients after 20 years [6–8]. It is considered

that 3 to 4 % of cases of dementia are due to PDD in the

general population, and that 32 % of all subjects with PD

have dementia [5]. Factors associated with PDD include

psychiatric disorders, advanced age, excessive daytime

somnolence, falls, urinary incontinence, moderate dysar-

thria and severely impaired motor function [8]. PDD is

basically distinguished from Lewy body dementia by the

chronology of clinical events, and from Alzheimer’s dis-

ease by the neuropsychological profile at the onset of the

disease [9]. The cognitive disorders in PD patients pre-

dominate in regard to executive and visuo-spatial

M. Kiesmann (&) � T. Vogel � L. Schweiger � G. Kaltenbach

Department of Geriatrics, Robertsau Hospital, Strasbourg

University Hospitals, 83 rue Himmerich, Strasbourg 67091,

France

e-mail: michele.kiesmann@chru-strasbourg.fr

J.-B. Chanson

Department of Neurology, Hautepierre Hospital,

Strasbourg University Hospitals, Strasbourg, France

J. Godet

Department of Public Health, Biostatistics and Methodology

Sector, Strasbourg University Hospitals, Strasbourg, France

S. Chayer

Department of Clinical Research, Civil Hospital, Strasbourg

University Hospitals, Strasbourg, France

123

J Neurol

DOI 10.1007/s00415-013-7018-8

functions. In their mild form, they may be detected only in

the course of specialized assessment; when they are severe,

they are overtly expressed in the form of attention disor-

ders. New diagnostic criteria for PDD have been proposed

by the Movement Disorders Society (MDS) [10], and are

divided into several parts including a preliminary simpli-

fied checklist [11]. Elderly PD patients have not been

specifically studied until now, although they have a high

risk of developing PDD.

In this study, an investigation of cognitive functions was

carried out in elderly PD patients with cognitive complaints

who were under standard medical care, and who had a

degree of cognitive impairment that affected their daily

lives. The main aim was to assess the performance of the

MDS criteria including the shortened checklist and the

exhaustive reference examination for the diagnosis of

PDD, and to compare these tools with other cognitive tests.

Patients and methods

Patients

PD patients with cognitive complaints who had attended the

Strasbourg geriatric center for a fixed period of 2 years were

selected for potential inclusion in the study. The inclusion

criteria were as follows: patient age C65 years, PD diag-

nosed according to the United Kingdom Parkinson’s Disease

Society Brain Bank (UKPDSBB) criteria [12], and stable

motor function. Eligible patients had to complain of cogni-

tive disorders which had direct consequences on their

everyday activities, as it has been found that the incidence of

objective cognitive decline appears to be significantly higher

in subjects with subjective complaints [13]. To ensure that

the cognitive deficits would in all probability lead to prob-

lems in activities of daily living (ADL), a clinical dementia

rating scale (CDR) [14–16] score[0.5 was required as part

of the inclusion criteria, also taking into account the fact that

reduced mobility interferes with ADL especially in the

elderly. The CDR scale is based on a comparison between the

patients’ capacities before and after the onset of the disease

with the aid of a referent. The mini-mental state examination

(MMSE) [17] score had to amount to [16 to ensure the

exclusion of patients with overly severe cognitive disorders.

However, the inclusion of patients subject to hallucinations

without significant emotional impact was permitted, as was a

case of PD-associated psychosis treated with low-dose

atypical neuroleptics. Biological analyses (blood cell count

and measurement of urea, creatinine, electrolytes, proteins,

TSH and vitamin B12 in the serum) as well as brain imaging

(CT scan or MRI) were respectively carried out within 6 and

12 months prior to entry into the study to rule out any

alternative diagnosis for dementia.

The exclusion criteria included the lack of impact of

cognitive impairment on the patients’ ADL, exclusion

criteria for PD according to the UKPDSBB, dementia due

to a cause other than PD, delirium that had occurred

\3 months before study inclusion, severe depressive syn-

drome accounting for the disorders observed, previous

major stroke, anticholinergic treatment, lack of feasibility

for carrying out the tests that were part of the study, or the

impossibility to provide the patient with detailed infor-

mation about the study.

All the patients were recruited from the Strasbourg

University Hospitals’ geriatric center by a neurologist with

experience in the field of PD and dementia, and a geria-

trician. The study was approved of by the Strasbourg

University Hospitals’ scientific committee and the local

ethics committee. It was then registered with the advisory

committee on the treatment of research information in the

health sector under No. IDRCB.2010-A00113-36, and also

with Clinical Trials. Gov. under No. NCT01113242.

Informed consent was obtained from all the patients prior

to their inclusion in the study.

Methods

The preliminary selection of potentially eligible subjects

was carried out by an experienced neurologist (MK), and

included the following: a physical and neurological

examination, application of the diagnostic criteria for PD

data collection on PD-specific characteristics, medical

history, treatments, and the results of biological analyses

and brain imaging. The patient was orally informed about

the study protocol at the time he or she was given the

informed consent form and information notice. The CDR

scale, which was scored out of five, and the geriatric

depression scale (GDS) [18, 19], which was scored out of

30, were both applied. Patients who had obtained a score

C22 on the GDS were excluded from the study, as this

score over-corresponded to a state of severe depression,

which could have interfered with the diagnosis of PDD.

The MMSE, scored out of 30, was also performed. Cog-

nitive assessment included literal verbal fluency over 2 min

for the letter P to evaluate executive function [20, 21], and

is included among the eight items on the MDS checklist.

The 2-min time frame was specifically chosen as it was

better adapted to the advanced age of the study subjects

who tended to react more slowly than younger individuals.

Following this pre-selection phase, the definitive patient

selection took place 2 weeks later: study inclusion was

determined by the neurologist who received the dated and

signed informed consent form, plus information on the

patient’s educational background from the age of 6 years.

The Hoehn and Yahr rating scale (H&Y) [22] was then

applied, scored out of five; while the instrumental activities

J Neurol

123

of daily living (IADL) were evaluated for the patient’s

capacity to use the telephone, means of public transport,

organize the budget and manage medicinal drug intake,

with a maximum score of 37 for these particular items,

which are more useful indicators than basic everyday

activities [23]. The Pill questionnaire was not used due to

the high proportion of institutionalized subjects in this

study population. The assessment based on the Unified

Parkinson’s Disease Rating Scale score for Part III, motor

function [24], was only partial and focused on an evalua-

tion of the rigidity of the neck and the upper and lower

limbs, right and left hand finger tapping tested separately

and the patient’s ability to get up from a chair, with a

maximum score of 32. Cognitive assessment, which was

adapted to the evaluation of PD-associated cognitive dis-

orders, included the Mattis Dementia Rating Scale

(MDRS) [25, 26], scored out of 144, an instrument for the

assessment of impaired executive function and in particular

for the evaluation of PD-associated cognitive disorders [27,

28]. The global score is considered to be normal if it

reaches [136/144 on the MDS; a copy of the Rey–Oster-

reith Complex Figure (ROCF), scored out of 36, was also

used for the assessment of visuo-constructive capacity [29].

A follow-up visit took place 2 weeks later with a neu-

ropsychologist, and included the French version of Grober

and Buschke’s 16-item Free and Cued Selective Remind-

ing Test with immediate recall (FCSRT–IR) [30]. This test

is used for assessing immediate recall (IR) capacity: in all,

three free recalls (FR) out of 48, three cued recalls (CR),

and the sum of three total recalls (TR) out of 48, with the

calculation of the number of off-list intrusions for the

exploration of recent episodic memory. Total FR is fre-

quently altered in PD patients, while cue-induced memory

is rarely affected. The Paced Auditory Serial Addition Test

in 4 s (PASAT) [31] was used for the evaluation of

attention capacity and executive function, thereby com-

pleting the cognitive assessment. The modified French

version of this test of the capacity for sustained attention

was used [32], and the result expressed in the number of

positive responses out of 60.

The values obtained for the different tests used were

expressed in percentiles (pc) of the normal population

adapted for age and educational level. A value within the

worst 10 pc for the reference population was considered

abnormal. The MDS criteria were applied by a neurologist

(JBC) who had not performed any previous assessment in

this study in order to differentiate between the two groups,

i.e. patients likely to have PDD and those with a probable

absence of PDD.

In this study, the final diagnosis of PDD was based on an

exhaustive cognitive assessment. This evaluation included

the testing of those cognitive functions that are more fre-

quently associated with PDD, as recommended by the MDS

[10]. PDD was diagnosed if abnormal results were observed

for at least two of the following functions or domains:

memory, executive functions, visuo-spatial capacities, and

attention. Memory impairment was defined by abnormal

results in either the total FR sub-score of the FCSRT–IR, or

the MDRS memory subtest. Executive functions were

considered impaired if at least two tests were abnormal

among the MDRS overall score, the verbal fluency score

and the PASAT score. Impairment of visuo-spatial capacity

was determined if either the copy of the ROCF or the

MDRS subtest for visuo-constructive function was abnor-

mal. Attention deficit was defined by abnormal results in at

least one of the following: the MDRS attention subtest, the

IR of the FCSRT–IR, or fluctuations of attention determined

by variability in performance over time in the different tasks

involving attention, independently of motor function fluc-

tuations. The classification into normal and abnormal was

carried out by the same neurologist (JBC), based on the

results of the cognitive tests, classified by domains.

The patients likely to have PDD as determined by the

MDS checklist met all the following criteria: diagnosis of

PD established before the development of cognitive defi-

cits, MMSE score\26, impact on the IADL (i.e. an IADL

score[5), at least two errors amongst the MMSE attention

sub-scores or the seven backwards test with two incorrect

replies; negative results for the visuo-construction test with

failed copy of pentagons; for memory, FR for three words

considered altered if one word was forgotten, and executive

function impairment determined via literal fluency for the

letter P over 2 min if the result was within the worst 10 pc.

Absence of major depression, absence of delirium and

absence of other abnormalities that could obscure diagnosis

completed the rating sheet for probable PDD. However, the

presence of apathy, depressed mood, delusions or excessive

daytime sleepiness could also be indicative of a diagnosis

of probable PDD insofar as application of the MDS criteria

for PDD diagnosis were concerned.

Statistical analysis

All statistical analyses were performed using R statistical

software (version 2.15.1 http://www.R-project.org/). PDD

and PD patients’ characteristics were compared using non-

parametric tests. The Kruskal–Wallis or the Mann–Whit-

ney test was used where appropriate to compare continuous

variables. Fisher’s exact test was performed on nominal

variables. Sensitivity, specificity, positive (PPV) and neg-

ative predictive values (NPV) and area under the receiver

operating characteristic (ROC) curve were determined

using the caret (version 5.15-048) and ROC (version 1.0-4)

R packages from the Comprehensive R Archive Network

repository. The level of statistical significance was set at

5 %.

J Neurol

123

Results

Patient characteristics

Fifty-seven patients were screened, of which 17 were not

included in the study for different reasons (two patients

were non-native French speakers, one subject had severe

dysarthria, four presented with no cognitive complaints,

two developed delirium, one patient had another stroke,

four subjects presented with major attention disorders

associated with an advanced stage of dementia and thus

could not be investigated, one case of cancer was diag-

nosed, and two patients refused to participate in the study).

The 40 remaining PD subjects were included in the study

from July 2011 to April 2012. Overall patient character-

istics have been summarized in Tables 1, 2; at this point, it

should be noted that 50 % of the patients were institu-

tionalized and 50 % dwelt in the community. The study of

the above-mentioned characteristics, therefore, did not

require any adaptation for age or socio-professional level.

In the study population, moderate depression, defined

according to the GDS score with a cut-off value between

13 and 14 [33], was found in 57.5 % of cases, with recently

documented or ongoing occurrence of hallucinations being

observed in 97 % of cases, again without a statistically

significant difference between the groups compared.

PDD patients (A group) and non-PDD patients or

dementia-free patients (B group) were determined via the

MDS cognitive exhaustive assessment. The following

subgroups were differentiated in the A group: PDD deter-

mined on the basis of a positive checklist (A1 group), and

PDD with an MMSE C26 (A2 group) determined via the

MDS cognitive assessment (Fig. 1). All the patients who

had an MMSE of\26 were found in the group of subjects

who had eight positive items on the MDS checklist. The

assessments carried out in the aforementioned domains, i.e.

memory, executive function, visuo-spatial capacities and

attention, showed abnormal values distributed between the

40 patients as follows: for the dementia-free PD group–no

domain impaired: 4/40 (10 %); one domain impaired: 5/40

Table 1 Characteristics of PDD (A1 and A2 groups) and PD dementia-free (B group) patients according to the MDS exhaustive cognitive

assessment (mean and SD)

N Global (N = 40)

(A ? B)

A group (N = 31)

(A1 ? A2) PDD

A1 group

(N = 20)

A2 group

(N = 11)

B group (N = 9)

PDD free

p-value

Mean (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD) A/B A1/A2

Age (yr) 80.5 (4.9) 81.2 (5.2) 81.2 (5.2) 81.1 (5.4) 78.1 (2.9) NS NS

M/F 0.40 0.39 0.30 0.55 0.44 NS NS

Educational level (yr) 10.2 (3.5) 9.7 (2.8) 9.7 (2.7) 9.8 (3.2) 12.0 (4.9) NS NS

Disease duration (yr) 11.2 (6.9) 11.9 (7.5) 13.8 (8.3) 8.5 (4.2) 8.7 (3.3) NS NS

Age at onset (yr) 69.3 (8.7) 69.3 (9.5) 67.5 (10.3) 72.5 (9.5) 69.4 (5.3) NS NS

Hoehn & Yahr stage 0/5 3.5 (0.7) 3.6 (0.8) 3.7 (0.8) 3.4 (0.7) 3.2 (0.5) NS NS

GDS score 0/30 12.4 (3.5) 12.3 (3.8) 12.8 (2.1) 11.4 (5.7) 12.9 (2.6) NS NS

CDR score 0/5 1.5 (0.6) 1.6 (0.6) 1.8 (0.6) 1.4 (0.5) 1 (0) 0.003 NS

MMSE score 0/30 24.6 (3.3) 23.7 (3.3) 22 (2.8) 26.9 (0.7) 27.3 (1.1) 0.001 \0.001

UPDRS motor function

score 0/32

15.9 (5.2) 16 (5.1) 16.4 (5.7) 15.3 (3.8) 15.7 (5.9) NS NS

IADL score 0/37 10.4 (2.6) 10.8 (2.7) 11.4 (2.9) 9.7 (2.1) 9 (2.0) NS NS

% % % % %

L-DOPA 97 96.8 95 100 100 NS NS

DA 47.5 45.2 45 45.5 55.6 NS NS

Clozapine 25 25.8 20 36.4 22.2 NS NS

BZP 35 35.5 50 9.1 33.3 NS NS

SRI 27.5 25.8 20 36.4 33.3 NS NS

COMT inhibitor 45 48.4 45 54.4 33.3 NS NS

MAO B inhibitor 10 9.7 15 0 11.1 NS NS

ChE inhibitor 7.5 9.7 10 9.1 0 NS NS

PDD Parkinson’s disease dementia, A group Movement Disorders Society (MDS) exhaustive assessment-determined PDD, A1 group MDS

exhaustive assessment-determined PDD and 8-item checklist positive for PDD, A2 group MDS exhaustive assessment-determined PDD and

8-item checklist\8, B group MDS exhaustive assessment-determined PDD-free, yr year, M/F male and female, GDS Geriatric Depression Scale,

CDR Clinical Dementia Rating Scale, UPDRS Unified Parkinson’s Disease Rating Scale, MMSE mini-mental state examination, IADL instru-

mental activities of daily living, DA dopamine agonist, BZP benzodiazepine, SRI serotonin reuptake inhibitor, COMT catechol-O-methyl

transferase inhibitor, MAO B inhibitor monoamine oxidase B inhibitor, ChE inhibitor choline esterase inhibitor, SD standard deviation

J Neurol

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(12.5 %); for the PDD group–two domains impaired: 14/40

(35 %); three domains impaired: 14/40 (35 %); and four

domains impaired: 3/40 (7.5 %).

Performances of the different tests considered

separately and compared with the MDS exhaustive

evaluation (Tables 3, 4):

The results of the different tests used in the exhaustive

assessment classified 31 patients (A group) as having PDD,

and nine persons (B group) as being dementia-free. The

MDRS global score, the preliminary MDRS subtest and the

FCSRT Free Recall Test were those the most closely linked

to a diagnosis of PDD. The results of the seven backwards

test, the pentagons, and the free recall of three words did

not show any significant difference between the 31 PDD

patients and the nine PD dementia-free patients. It was in

fact the MMSE test for orientation in time that revealed a

significant difference (p = 0.02) between the two groups.

Using a ROC curve, the optimal cut-off values for the

diagnosis of PDD on the MDRS, the FCSRT FR and the

ROCF were determined within the framework of this study.

The cut-off values of the other tests for the diagnosis of

PDD (Table 5) were calculated on the basis of the results

Table 2 Characteristics of PDD (A1 and A2 groups) and PD dementia-free (B group) patients according to the MDS exhaustive cognitive

assessment (median and range)

N Global (N = 40)

(A ? B)

A group (N = 31)

(A1 ? A2) PDD

A1 group

(N = 20)

A2 group

(N = 11)

B Group (N = 9)

PDD-free

p-value

Median (range) Median (range) Median

(range)

Median

(range)

Median (range) A/B A1/A2

Age (yr) 80 (72–92) 81 (72–92) 82 (72–92) 80 (75–92) 78 (75–84) NS NS

Educational level (yr) 9 (6–24) 8 (6–17) 8 (6–17) 8 (8–17) 10 (8–24) NS NS

Disease duration (yr) 9.5 (3–32) 10 (3–32) 11 (3–32) 9 (3–13) 8 (5–15) NS NS

Age at onset (yr) 70 (45–83) 70 (45–83) 69 (45–83) 71(61–83) 67 (63–77) NS NS

Hoehn & Yahr stage 0/5 3 (2–5) 4 (2–5) 4 (2–5) 3 (3–5) 3 (2.5–4) NS NS

GDS score 0/30 13 (4–20) 13 (4–20) 13 (9–16) 13 (4–20) 13 (10–18) NS NS

CDR score 0/5 2 (1–3) 2 (1–3) 2 (1–3) 1 (1–2) 1 (1–1) 0.003 NS

MMSE score 0/30 25.5 (16–29) 24 (16–28) 23 (16–25) 27 (26–28) 27 (26–29) 0.001 \0.001

UPDRS motor function

score 0/32

16 (8–26) 16 (8–26) 17.5 (8–26) 16 (9–20) 17 (7–22) NS NS

IADL score 0/37 10 (5–19) 10 (7–19) 10.5 (7–19) 9 (7–13) 9 (5–12) NS NS

PDD Parkinson’s disease dementia, A group Movement Disorders Society (MDS) exhaustive assessment-determined PDD, A1 group MDS

exhaustive assessment-determined PDD and eight-item checklist positive for PDD, A2 group MDS exhaustive assessment-determined PDD and

eight-item checklist \8, B group MDS exhaustive assessment-determined PDD-free, yr year, M/F male and female, GDS Geriatric Depression

Scale, CDR Clinical Dementia Rating Scale, MMSE Mini-Mental State Examination, IADL Instrumental Activities of Daily Living, UPDRS

Unified Parkinson’s Disease Rating Scale, SD standard deviation

Fig. 1 Study design; PD

Parkinson’s disease, PDD

Parkinson’s disease dementia,

MDS Movement Disorders

Society

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obtained via the reference list established according to

MDS criteria, i.e. the exhaustive cognitive assessment

(Table 5).

MDS checklist performance for the diagnosis of PDD

compared with the MDS exhaustive evaluation:

All the patients who met the diagnostic criteria for PDD

according to the MDS checklist had an MMSE score of

\26 (A1 group), while all the remaining subjects (A2 and

B groups) had an MMSE score C26. The application of the

MDS checklist resulted in a diagnosis of dementia in 20

patients, i.e. in 50 % of the study population. No between-

group difference was found for the characteristics exam-

ined, and no readjustment for age or educational level was

required. The extremely low p-values for the CDR scale

and the MMSE, the seven backwards test and the verbal

fluency test were explained by the fact that these were

selection criteria. Variables such as the global score on the

MDRS, the MDRS memory test, the ROCF and the 16-item

free and cued recall test were the most determinant in

differentiating between the MDS checklist-positive group

(A1 group) and the other PDD subjects with an MMSE

C26 (A2 group) based on the results of the MDS

exhaustive cognitive assessment. The specificity of the

checklist compared with that of the exhaustive evaluation

was 1, and its sensitivity amounted to 0.645. The accuracy

was 0.725, with a 95 % CI (0.561, 0.854), positive pre-

dictive value (PPV) of 1, negative predictive value (NPV)

0.450, and prevalence 0.775.

The characteristics of the patients who fulfilled either

the checklist criteria or those of the exhaustive evaluation

recommended by the MDS were compared. The compari-

son between the checklist–positive dementia group

(n = 20) or the A1 group and the PDD subgroup with an

MMSE C26 identified via the exhaustive assessment

(n = 11) or the A2 group showed that the item, orientation

in space, scored on the MMSE was significantly associated

with the diagnosis of PDD via the checklist, with a p value

of 0.0033.

Discussion

To the authors’ knowledge, this is the first study to apply the

MDS criteria for the diagnosis of PDD to a patient popu-

lation of such an advanced age using a detailed method of

cognitive assessment. This was a monocentric cross-

Table 3 Comparison of results of cognitive tests in PDD and PD dementia-free patients according to the MDS exhaustive cognitive assessment

(mean and SD)

N A Group N = 31 A1 group N = 20 A2 group N = 11 B group N = 9 p-value

Mean (SD) Mean (SD) Mean (SD) Mean (SD) A/B A1/A2

MMSE global score/30 23.7 (3.3) 22 (2.8) 26.9 (0.7) 27.3 (1.1) 0.001 \0.001

Seven backwards 0/5 3.5 (1.5) 2.8 (1.5) 4.8 (0.4) 4.6 (0.5) NS \0.001

Temporal orientation0/5 3.8 (1.2) 3.5 (1.3) 4.5 (0.7) 4.8 (0.4) 0.02 0.04

Spatial orientation 0/5 4.4 (0.8) 4.1 (0.8) 4.9 (0.3) 4.7 (0.5) NS 0.003

3-word recall 0/3 1.5 (1.4) 1.4 (1.7) 1.7 (0.9) 2 (1.0) NS NS

Pentagons 0/1 0.8 (1.4) 0.8 (1.8) 0.8 (0.4) 0.9 (0.3) NS NS

Word fluency score 120 s 7.7 (3) 7 (2.9) 8.9 (2.9) 10.8 (3.9) 0.02 NS

MDRS global score 0/144 110.5 (13.7) 109.9 (11.2) 111.17 (18.0) 130.1 (5.6) \0.001 NS

Attention 0/37 34.1 (2.9) 34.1 (2.3) 34 (3.9) 35.9 (1.2) 0.03 NS

Initiation 0/37 25.6 (5.1) 26.1 (5.0) 24.8 (5.4) 32 (3.6) 0.002 NS

Construction 0/6 4.6 (1.3) 4.6 (1.1) 4.6 (1.6) 5.7 (0.5) 0.01 NS

Memory 0/25 14.5 (5.5) 12.9 (4.5) 17.2 (6.3) 18.8 (4.0) 0.01 NS

FRCST-IR IR score 0/48 12.2 (2.4) 12.2 (2.8) 12.1 (1.6) 14.6 (2.2) 0.004 NS

3-FR score0/48 13.8 (6.9) 13.1 (8.0) 15.1 (3.9) 22.9 (5.6) 0.003 NS

3-TR score0/48 33.3 (10.4) 31.2 (11.8) 37 (6.0) 43.3 (3.4) 0.004 NS

ROCF score 0/36 16.3 (7.4) 15.7 (7.7) 17.4 (6.9) 27.2 (6.6) 0.002 NS

PASAT* 7.9 (8.9) 9.7 (10.1) 4.6 (5.2) 16.9 (12.8) 0.04 NS

A group Movement Disorders Society (MDS) exhaustive assessment-determined PDD, A1 group MDS exhaustive assessment-determined PDD

and eight-item checklist positive for PDD, A2 group MDS exhaustive assessment-determined PDD and 8-item checklist \8, B group MDS

exhaustive assessment-determined PD dementia-free, PDD Parkinson’s disease dementia, MDRS Mattis Dementia Rating Scale, FCSRT-IR

Grober & Buschke’s Free and Cued Selective Reminding Test with Immediate Recall (French version), IR immediate recall, FR free recall, TR

total recall from the FRCST, ROCF Rey–Osterreith Complex Figure test, PASAT-4 s Paced Auditory Serial Addition Test with an interval of 4 s

between each number, * total number of correct responses/60, SD standard deviation

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sectional study that for the most part recruited PD patients

from the urban community in Strasbourg, an average-sized

city. The relatively low number of patients included who

had PDD may be explained in two ways: on the one hand, it

has been reported that 6.9 % of persons living in the urban

community of Strasbourg are over 75 years old, and that

14 % of this elderly population have dementia [34]; as PDD

has been reported to account for 3–4 % of cases of dementia

[5], an estimation may be made that around 130 subjects

who are over 75 years of age are likely to have PDD. On the

other hand, if the number of subjects included in the various

studies on the diagnosis of PD-associated cognitive disor-

ders is so low, it could also well be due to the selection

criteria used and the feasibility of carrying out a detailed

Table 4 Comparison of results of cognitive tests in PDD and PD dementia-free patients according to the MDS exhaustive cognitive assessment

(median and range)

N A group N = 31 A1 group N = 20 A2 group N = 11 B group N = 9 p-value

Median (range) Median (range) Median (range) Median (range) A/B A1/A2

MMSE global score/30 24 (16–28) 23 (16–25) 27 (26–28) 27 (26–29) 0.001 \0.001

Seven backwards 0/5 4 (1–5) 3 (1–5) 5 (4–5) 5 (4–5) NS \0.001

Temporal orientation 0/5 4 (1–5) 3.5 (1–5) 5 (3–5) 5 (4–5) 0.02 0.04

Spatial orientation 0/5 5 (3–5) 4 (3–5) 5 (4–5) 5 (4–5) NS 0.003

3-word recall 0/3 1 (0–3) 1 (0–3) 2 (0–3) 2 (0–3) NS NS

Pentagons 0/1 1 (0–1) 0.5 (0–1) 1(0–1) 1 (0–1) NS NS

Word fluency score 120 s 8 (3–15) 7.5 (3–13) 8 (6–15) 11 (4–18) 0.02 NS

MDRS global score 0/144 113 (60–131) 112 (85–131) 116 (60–123) 131 (121–137) \0.001 NS

Attention 0/37 35 (23–37) 35 (29–37) 35 (23–37) 36 (34–37) 0.03 NS

Initiation 0/37 26 (12–36) 25.5 (18–36) 26 (12–33) 32 (25–36) 0.002 NS

Construction 5 (1–6) 5 (2–6) 5 (1–6) 6 (5–6) 0.01 NS

Memory 0/25 15 (6–22) 12.5 (6–20) 16 (6–25) 20 (11–22) 0.01 NS

FRCST-IR IR score 0/48 13 (5–16) 13 (5–16) 13 (8–14) 15 (9–16) 0.004 NS

3-FR score0/48 14 (0–30) 13 (0–30) 15 (8–21) 23 (14–30) 0.003 NS

3-TR score0/48 35 (6–48) 34 (6–47) 35 (30–48) 44 (37–47) 0.004 NS

ROCF score 0/36 18 (0–31) 16 (0–31) 19 (1–25) 28 (17–36) 0.002 NS

PASAT * 7 (0–40) 8.5 (0–40) 2 (0–14) 14 (2–38) 0.04 NS

A group Movement Disorders Society (MDS) exhaustive assessment-determined PDD, A1 group MDS exhaustive assessment-determined PDD

and checklist 8 items positive for PDD, A2 group MDS exhaustive assessment-determined PDD and 8-item checklist \8, B group MDS

exhaustive assessment-determined PDD-free, PDD Parkinson’s disease dementia, MDRS Mattis Dementia Rating Scale, FCSRT-IR Grober &

Buschke’s Free and Cued Selective Reminding Test with Immediate Recall (French version), IR immediate recall, FR free recall, TR total recall

from the FRCST, ROCF Rey–Osterreith Complex Figure test, PASAT-4 s Paced Auditory Serial Addition Test with an interval of 4 s between

each number, * total number of correct responses/60

Table 5 Discriminant validity of the investigated cognitive assessment scales for the diagnosis of PDD

MDRS score 0/144 FCSRT-IR 3-FR

score 0/48

ROCF score 0/36

Cut-off point B120 B123 B132 B22 B21

AUC (95 %) 0.959 B123 B132 0.855 0.839

Sensitivity 0.806 0.935 1.000 0.839 0.903

Specificity 1.000 0.778 0.444 0.778 0.778

PPV 1.000 0.935 0.861 0.929 0.933

NPV 0.600 0.778 1.000 0.778 0.700

Incidence of detection 0.625 0.775 0.900 0.700 0.750

Accuracy 0.85 0.9 0.875 0.825 0.875

95 % CI 0.702–0.943 0.763–0.972 0.732–0.958 0.672–0.927 0.732–0.958

PDD Parkinson’s disease dementia, AUC area under the curve, CI confidence interval, PPV positive predictive value, NPV negative predictive

value, MDRS Mattis Dementia Rating Scale, FCSRT-IR Grober and Buschke’s Free and Cued Selective Reminding Test with Immediate Recall

(French version), 3-FR 3 Free Recalls, ROCF Rey–Osterreith Complex Figure test

J Neurol

123

cognitive examination in this specific, i.e. very elderly

patient population. This view is corroborated by the studies

of Riedel et al. [35] (GEPAD) and Balzer-Geldsetzer et al.

[36] (DEMPARK). The first study found that 229 patients

had PDD, i.e. 29 % of the PD population investigated

diagnosis of dementia established by an MMSE score B24,

global clinical impression and DSM IV criteria, whereas in

the latter study the number of patients diagnosed with PDD

amounted to just 78, i.e. 13.1 % of the 604 PD patients who

had been selected on the basis of a detailed cognitive

examination carried out within the same urban community,

but one which was much larger than that examined in the

present work.

The relative utility of the checklist has been confirmed

in the present study for the diagnosis of PDD in an elderly

PD population although it has its limitations as a screening

instrument. However, there is a widespread need for a brief

yet reliable diagnostic method to help diagnose PDD

patients who are at a relatively advanced stage of their

disease. Not only would a short method be simpler and thus

more feasible to apply, but as these attention disorders will

continue to worsen in this elderly PDD population it will

become increasingly more difficult for them to be capable

of undergoing an in-depth neuropsychological assessment.

In this regard, reports have been published in the literature

on the diagnostic method proposed by Emre et al. and

Dubois et al. [10, 11], and several other studies have also

investigated the sensitivity and specificity of the checklist

for the diagnosis of PDD.

Using an in-depth neuropsychological examination as

reference, Barton et al.’s study [37] classified 15 subjects

out of 91 PD patients as suffering from PDD (mean age:

66.3 ± 9.7 years). It should, however, be mentioned that

these authors had expressly not respected definite cut-off

values for the cognitive assessment, and that the specificity

amounted to 1. The sensitivity of the checklist was only

46 %, with a prevalence of 7.7 %. The study by Riedel et al.

[35] on the assessment of PD-associated disorders with an

MMSE of B24 also showed a sensitivity of only 50 %.

In Di Battista et al.’s study [38] using the DSM IV cri-

teria for the diagnosis of PDD as reference, the checklist

was validated with a sensitivity of 78 % and a specificity of

95.5 % for a 12 % prevalence of PDD in 76 subjects (mean

age: 69.3 ± 8.5 years), i.e. nine cases of PDD (mean age:

77 ± 5.4 years) with a PPV of 70 %, an NPV of 97 %, and

an accuracy of 93.4 %. Nine cases of PDD were determined

using the checklist and seven cases of PDD with the DSM

IV criteria. The latter study is the only one in which the

checklist overestimated the diagnosis of PDD. In fact, use of

the checklist tends to result in an underestimation of the

number of PDD cases rather than the opposite. It has been

suggested that the sensitivity of the checklist could be

improved upon if depression, apathy, hallucinations and

delusions were to be considered characteristics in support of

a diagnosis of PDD [37, 39]; moreover, the results of the

present study did not reveal any significant differences in

this regard: all the patients in fact had at least one psychi-

atric disorder at inclusion in this study. Thus, it was not the

lack of data on psychiatric or behavioral disorders that

declassified patients likely to have PDD. In the present

study, the PDD patients classified by the checklist (A1

group) were at a stage of dementia in which temporo-spatial

orientation disorders had developed. As regards the MMSE

orientation subtest, among the patients with PDD (A group),

the A2 group was found to be better oriented in time and

space than the A1 group, with a significant difference of

0.04 and 0.003 respectively. Also of note, as regards the

MMSE orientation subtest the dementia-free PD patients (B

group) were better temporally oriented than the 31 PDD

subjects (A group), with a significant difference of 0.02. In

fact, the diagnosis of PDD is strongly linked to the devel-

opment of disorientation [35]; at this point, it is suggested

that the checklist could include a temporal orientation item

to determine the progressive impairment of temporo-spatial

perception, as was observed in the present study. It can be

considered that the cognitive deficits determined via the

eight-item checklist tended to be more severe in PD

patients: however, the latter was not sufficiently sensitive

for the diagnosis of PDD because 11 out of the 31 patients

with at least two cognitive domains impaired were excluded

using this method. Attention disorders were therefore

determined by the item, disorientation on the MMSE, which

characterizes the advanced stages of PDD.

In Dujardin et al.’s study [40] involving 41 PDD patients

(mean age: 73.95 ± 5.27 years) out of a total PD patient

population of 188 subjects (mean age: 69.10 ± 8.68 years),

validity was based on an adaptation of the MDS checklist

which included a five-word test, the Pill questionnaire and

an assessment of specific behavioral disorders—halluci-

nations, depression and motivational state. The shortened

approach developed by Dujardin et al. was compared with

an in-depth neuropsychological examination as recom-

mended by the MDS, and showed a sensitivity of 65.85 %

(95 % CI = 49.41–79.92 %) and a specificity of 94.56 %

(95 % CI = 89.56–97.62 %). An MMSE score B26, ver-

bal fluency B7, the five-word recall test, the score on the

Pill questionnaire and age C70 years showed improved

sensitivity at 85.37 % (95 % CI = 76.69–89.25 %) with-

out overly reducing specificity at 83.67 % (95 %

CI = 76.69–89.25 %). In the present study, this threshold

of B26 only permitted five patients to be reclassified in the

group of dementia patients instead of the 11 PDD subjects

diagnosed via the exhaustive assessment, taking into

account the fact that the five-word test was not used in the

MDS checklist in the present study. Moreover, two out of

these five patients were not classified as demented by the

J Neurol

123

exhaustive list. Hoops et al.’s study [41] investigated the

validity of the Montreal Cognitive Assessment test [42]

and the MMSE for the detection of mild cognitive

impairment (MCI) and PDD. These authors showed an

optimal cut-off point of between 24 and 25 for the diag-

nosis of PDD via the MMSE, with a sensitivity of 29 %,

specificity of 99 %, PPV of 83 %, NPV of 88 %. In the

present study, the MDS checklist displayed a better sensi-

tivity for an optimal specificity of 1, with an MMSE of

\26. In Biundo et al.’s study [43], the cut-off score, in

agreement with the MDS criteria for differentiation

between PDD and PD without the presence of cognitive

impairment, had a value of\25.9 for 15 PDD patients with

an average age of 70.3 years (±7.6 years) out of 104

consecutive PD patients, with a PPV of 80 %. With a

sensitivity of 0.645 for the checklist results, the present

study showed that it had a fairly low capacity for detecting

patients suffering from PDD when they had an MMSE

score of C26.

This study proposes that the evaluation of the cognitive

domains be based on the MDS exhaustive reference method

or gold standard. The choice of subtests with the 3-FRs

seemed to be of interest for the diagnosis of dementia,

whatever its etiology [44], while the memory subtest, which

explores visual memory, verbal recall and fluctuating

attention, displayed an excellent capacity to establish a

diagnosis of dementia [28]. The utility of the Rey–Osterrieth

Complex Figure for the exploration of visuo-constructive

capacities was confirmed for its use in the assessment of PD-

associated cognitive disorders [43]. In the present study, the

choice of at least one abnormal test result out of two for

classifying a cognitive domain as being impaired rather than

two abnormal test results can be explained by the fact that it is

thereby possible to avoid underestimating the number of

domains that have been impaired, all the more as the tests

used to assess a domain have been specifically adapted to the

assessment of states of dementia. The choice of two abnor-

mal test results out of three for classifying the executive

function cognitive domain as impaired is explained by the

fact that as the PASAT has frequently failed to adequately

assess dementia, it is thereby possible to avoid overesti-

mating executive dysfunction. This approach permitted 31

patients to be classified as having PDD, and for nine patients

to be considered dementia-free, although the latter group

nevertheless experienced problems regarding ADL. How-

ever, it is commonly known that PD-associated cognitive

impairment has a progressively negative effect on PD

patients’ capacity to deal with ADL, even in the absence of

dementia [23]. As regards the PDD-free group, the criteria

for the assessment of mild cognitive impairment (MCI),

which were not applied in the present study, would have

allowed cognitive impairment to be classified between MCI

and normal. In a predominantly PD patient population,

around 10 % of patients have been found to progress from

the non-demented to the demented stage each year [45].

This study also attempted to establish optimal cut-off

values for the diagnosis of PDD using other cognitive tests.

The ROC curve showed a clear relationship between PDD

diagnosis and the MDRS score. However, a circularity bias

was present as the global score on the MDRS rating scale,

the construction score and the memory score were included

in the diagnostic criteria on the reference list. At this point,

it should also be recalled that the values were expressed in

pc (the reference was in percentiles such as \10 pc), and

the threshold values of previous studies did not serve as a

basis in the present case for differentiating between normal

and demented patients. The MDRS explored the executive

functions and contributed to establishing the diagnosis of

PDD. The results of the MDRS in the present study were

fairly similar to those previously published in the literature,

but with slight differences. Mean values of 109.5 ± 11.2

(A1 group) versus 110.5 ± 13.7 (A group) were found,

whereas in Llebaria et al.’s study [28] which investigated a

younger and less educated patient population

(77.6 ± 5 years; 6.4 ± 4 years in PDD patients), the mean

value for subjects classified as having PDD amounted to

105 ± 14.30. Using the CDR scale and the DSM IV cri-

teria as diagnostic reference tools, a diagnostic cut-off

value of 123 for the MDRS was proposed by these authors.

This value corresponded to a sensitivity of 92.65 % and a

specificity of 91.4 %, a PPV of 83.3 %, and an NPV of

96.4 %. In Martinez-Martin et al.’s study [46], the diag-

nostic criteria for PDD in a population of 85 PDD patients

(mean age: 71.9 ± 6.3 years) based on the CDR scale and

the DSM IV criteria were found to be less sensitive than

those proposed by the MDS. Using the MDS in-depth

neuropsychological examination as a basis for reference

which did not include the MDRS to avoid a circularity bias,

an optimal cut-off value of B132 on the MDRS scale has

been proposed by Matteau et al. [47] for the diagnosis of

PDD (n = 6; mean age: 73.5 ± 7.7 years), with a sensi-

tivity of 1 and a specificity of 1. In the latter study, the

neuropsychological examination was better adapted to a

diagnosis of MCI rather than to that of PDD, and classified

as PDD patients all subjects who presented with a depen-

dent state. The cut-off point of 132 in the present study

showed a sensitivity of 1 with a low specificity; the cut-off

point of 120 appears to correspond to a discriminatory

value for the diagnosis of PDD, and that of 132 to a dis-

criminatory value for the screening of PDD. The use of the

checklist criteria could suffice for the diagnosis of severe

PDD, and that of the MDRS for the diagnosis of PDD in

patients who do not fulfill the checklist conditions. How-

ever, the difficulty lies in determining which persons

actually have disease and who remain undiagnosed among

the group classified as PDD-free for an MMSE score of

J Neurol

123

between 26 and 30. The distribution of values in the dif-

ferent cognitive assessment tests is of prime importance for

an exploration of the four cognitive domains. In Dujardin

et al.’s study [40], the distribution of values on the MDRS

scale ranged from 95 to 138, and in the FCSRT test from 0

to 27 for FR and from 10 to 48 for TR in the PDD group.

Similar results were found in the present study. These

findings underline the importance of carrying out a full

exploration of the four cognitive domains. The authors,

therefore, propose a more specifically adapted approach for

the diagnosis of PDD in elderly PD patients who display

symptoms indicative of a diagnosis of PDD such as

depressive mood, apathy and hallucinations [36] (Fig. 2).

Conclusion

Establishing a diagnosis of PDD is particularly important at

any stage of dementia, as it has a major influence on the

type of treatment to be subsequently administered and on

the appropriate medical care to be given to these patients.

In the case of suspected PD-associated dementia, the MDS

checklist criteria appear to be well adapted for elderly

patients with an MMSE score of \26; however, for sub-

jects with an MMSE score between 26 and 30, and in

particular in the case of alterations in spatial orientation

determined via the MMSE, a more exhaustive assessment

is required and should in particular include a MDRS score

with a cut-off value of 132. More specifically, the

exhaustive assessment should be focused on executive

functions, FR tests for the investigation of memory

impairment, and the reproduction of the ROCF for the

evaluation of visuo-constructive capacity.

Acknowledgments We would like to thank Marilyn Schreier-Au-

doire for her assistance in translating and copy-editing this article.

Conflicts of interest On behalf of all the authors, the corresponding

author states that there is no conflict of interest to report.

Ethical standard This study was approved by the ethics committee

of Strasbourg University Hospital and was performed in accordance

with the ethical standards laid down in the 1964 Declaration of

Helsinki and its later amendments.

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