Psychometric Properties of an Abbreviated

Version of the Apathy Evaluation Scale for

Parkinson Disease (AES-12PD)
Yuliya Stankevich, M.Sc., Ulrike Lueken, Ph.D., Monika Balzer-Geldsetzer, Ph.D.,
€
Richard Dodel, M.D., Susanne Graber-Sultan, Ph.D., Daniela Berg, M.D.,
€
Inga Liepelt-Scarfone, Ph.D., Rudiger Hilker-Roggendorf, M.D., Elke Kalbe, Ph.D.,
€
Oliver Kaut, M.D., Brit Mollenhauer, M.D., Kathrin Reetz, M.D., Eva Schaffer, M.D.,
€ B. Schulz, M.D., Annika Spottke, M.D., Karsten Witt, M.D.,
Nele Schmidt, Ph.D., Jorg
Katharina Linse, Ph.D., Alexander Storch, M.D., Oliver Riedel, Ph.D.

Background: Apathy is a frequent symptom in Parkinson’s disease (PD), substan-

tially aggravating the course of PD. Regarding the accumulating evidence of the key
role of apathy in PD, time-efficient assessments are useful for fostering progress in
research and treatment. The Apathy Evaluation Scale (AES) is widely used for the
assessment of apathy across different nosologies. Objective: To facilitate the applica-
tion of the AES in PD, we reduced the AES to two-thirds its length and validated this
abbreviated version. Design: Data sets of 339 PD patients of the DEMPARK/LAND-
SCAPE study without dementia and depression were randomly split into two sam-
ples. Data of sample 1 were used to develop a brief version of the AES (AES-12PD). A
cross-validation was conducted in sample 2 and in a subsample of 42 PD patients
with comorbid dementia and depressive symptomatology. Receiver operating charac-
teristic analysis was applied to determine the optimal cutoff of the AES-12PD as an
indicator of apathy. Results: The AES-12PD featured high internal consistency that

Received December 4, 2017; revised May 23, 2018; accepted June 4, 2018. From the Institute of Clinical Psychology and Psychotherapy, Depart-
ment of Psychology, Technische Universit€at Dresden, Dresden, Germany; Department of Psychiatry, Psychosomatics, and Psychotherapy,
Center of Mental Health, University Hospital of W€ urzburg, W€urzburg, Germany; Department of Psychology, Humboldt-Universit€at zu Berlin,
Berlin; Department of Neurology, Phillips University Marburg, Marburg, Germany; Chair of Geriatrics, University Hospital Essen, Geriatric
Centre Haus Berge, Contilia GmbH, Essen, Germany; Department of Neurology, Goethe University Frankfurt, Frankfurt; Department of Neu-
rodegenerative Diseases, Hertie Institute for Clinical Brain Research, Universit€at T€
ubingen, and German Center for Neurodegenerative Dis-
eases (DZNE), T€ ubingen, Germany; Department of Neurology, University Hospital Campus Kiel, Kiel, Germany; Department of Medical
Psychology | Neuropsychology and Gender Studies & Center for Neuropsychological Diagnostics and Intervention (CeNDI), University Hos-
pital Cologne, Cologne; Department of Neurology, University Hospital Bonn, and German Center for Neurodegenerative Diseases (DZNE),
Bonn, Germany; Paracelsus-Elena-Klinik, Kassel, Germany; Klinik f€ ur Neurologie, Universit€atsmedizin G€ ottingen, G€
ottingen, Germany;
Department of Neurology, RWTH Aachen University, Aachen, Germany; JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging,
Forschungszentrum J€ ulich GmbH and RWTH Aachen University, Aachen, Germany; Department of Neurology, Carl von Ossietzky Univer-
sity Oldenburg, Oldenburg, Germany; Division of Neurodegenerative Diseases, Department of Neurology, Technische Universit€at Dresden,
Dresden, Germany; Department of Neurology, University of Rostock, and German Center for Neurodegenerative Diseases (DZNE) Rostock/
Greifswald, Rostock, Germany; and the Department of Clinical Epidemiology, Leibniz Institute for Prevention Research and Epidemiology
BIPS GmbH, Bremen, Germany. Send correspondence and reprint requests to Yuliya Stankevich, M.Sc., Institute of Clinical Psychology and
Psychotherapy, Technische Universit€at Dresden, Chemnitzer Strasse 46, 01187 Dresden, Germany. e-mail: yuliya.stankevich@tu-dresden.de
© 2018 American Association for Geriatric Psychiatry. Published by Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.jagp.2018.06.012

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Psychometric Properties of an Abbreviated Version of the Apathy Evaluation Scale

was better compared to the AES. The abbreviated scale was well differentiated from
motor impairment and cognitive deficits. The AES-12PD cutoff of 27/28 was the opti-
mal cutoff for apathy in PD patients without dementia and depression. The cutoff of
25/26 indicated apathy in PD patients with comorbid dementia and depression.
Conclusion: Results confirm a high internal consistency and good discriminant
validity of the AES-12PD. The AES-12PD represents a reliable tool for the efficient
assessment of apathy that can be applied in PD patients with and without dementia
and depression. (Am J Geriatr Psychiatry 2018; 26:1079 1090)
Key Words: Apathy, Parkinson disease, Apathy Evaluation Scale, psychometric
properties, neuropsychiatric symptoms
Highlights
 We developed and validated a brief version of the Apathy Evaluation Scale (AES-
12PD) in a sample of 170 Parkinson’s disease (PD) patients without dementia and
depression
 The AES-12PD featured high internal consistency and good discriminant validity con-
sistent with the full-length AES
 The validation in a subsample of 42 PD patients with comorbid dementia and depres-
sive symptomatology confirmed good psychometric properties of the AES-12PD
 The optimal AES-12PD cut-off score for apathy in PD patients without dementia and
depression was 27/28
 In PD patients with comorbid dementia and depression we recommend the cut-off
25/26 of the AES-12PD as indicator of apathy

apathy in PD has been associated with increased

TAGEDH1INTRODUCTIONTAGEDN
A pathy is one of the most frequent neuropsychi-
atric symptoms in Parkinson disease (PD),
characterized by a loss of motivation and reduction
of goal-directed behavior, cognition, and emotional
expression.1 Apathy already occurs in early stages of
PD but increases with disease progression.2 A recent
meta-analysis reported the pooled prevalence of apa-
thy in 40% of PD patients, with concomitant depres-
sion present in 57% of apathetic patients.3 In a
prospective longitudinal study over 18 months with
89 mild PD patients, apathy was present in 43% of
PD patients, and it was predicted by male gender,
lower educational level, higher symptoms of depres-
sion, and more severe functional disability.4 Further-
more, in almost half of apathetic patients (23%), no
concomitant depression or cognitive impairment was
present, suggesting apathy as a separate syndrome in
PD.3 Consistent with the results reported by Den
Brok et al.,3 other studies have also suggested that
depression,5 cognitive deficits,6 poor health related
quality of life,2,7,8 and increased caregiver distress.9,10
Thus, the assessment of apathy in daily routine care
is essential for early detection and treatment of
apathy and requires appropriate and time-efficient
instruments. In the present study, we aimed to
develop and evaluate a brief version of the Apathy
Evaluation Scale (AES), adapted for PD, that would
facilitate its use as an assessment tool.
Psychometric properties of the available apathy
scales in PD were assessed in a review of the Move-
ment Disorder Society.11 The Apathy Scale12 and item
4 of the Unified Parkinson's Disease Rating Scale
(UPDRS)13 were classified as “recommended” scales.
The AES,14 the Lille Apathy Rating Scale,15 and sec-
tion seven of the Neuropsychiatric Inventory16 were
classified as “suggested” scales for assessment of
severity of apathetic symptoms in PD. A study in
untreated, drug-naive PD patients reported satisfac-
tory psychometric properties of the self-rating AES.17
A recent study by our group18 of 582 PD patients
with and without depression and dementia suggested

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the AES as a valid instrument for PD, advancing the
available evidence regarding the applicability of the
AES in PD.
The AES14 (German version: Lueken et al.19) has
been widely used for the assessment of apathy in vari-
ous patient groups.20 The scale consists of 18 items
assessing apathetic symptoms on a behavioral, cogni-
tive, and emotional level. The AES is available as a self-
rating, an informant rating, or a clinical interview.
To foster the assessment of apathy for PD in
research and clinical routine, we reduced the AES to
two-thirds of its original length and evaluated the
brief version of the self-rating AES (AES-12PD) using
the data of PD patients without dementia and depres-
sion based on the previously used sample.18 The
resultant reduction of one-third of the assessment
time (seen when applying the abbreviated AES-
12PD) can be a relevant time factor, especially in large
patient samples. We also report the psychometric
properties of the AES-12PD for PD patients with
comorbid dementia and signs of clinically relevant
depression (PD-DD). We provide a cutoff for the
AES-12PD as an indicator for the presence of apathy.
TAGEDH1METHODSTAGEDN
Patient Recruitment
AES data were collected within the German DEM-
PARK/LANDSCAPE project, a multicenter prospec-
tive longitudinal cohort study across 6 years with
annual examinations. A detailed description of the
study procedure is provided elsewhere.21 For the
present analysis, only data from the baseline assess-
ment were used. The recruitment of patients and
baseline assessment started in November 2009 and
were finished in February 2012. Patients were
included in the study after giving their written
informed consent. The study protocol was approved
by the Philipps University Marburg Ethics Committee
(approval 178/07) and by the local ethics committees
of the participating centers.
The diagnosis of PD was stated according to the U.
K. Parkinson's Disease Society Brain Bank clinical
diagnostic criteria.22 Following the neuropsychologi-
cal assessment, PD patients were allocated to one of
three subgroups: cognitively intact PD patients (PD),
PD patients with mild cognitive impairment (PD-
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Stankevich et al.
MCI), and PD patients with dementia (PD-D). MCI
was stated according to Petersen et al.,23 as the Move-
ment Disorder Society criteria for PD24 had not been
published at the setup of the study. Dementia was
diagnosed by a clinician's rating according to the diag-
nostic criteria.25,26 Patients with evidence or diagnosis
of atypical Parkinson syndromes (e.g., multiple sys-
tem atrophy, progressive supranuclear palsy, cortical-
basal degeneration) were not included in the study. A
cutoff score of 5 or higher on the short form of the
Geriatric Depression Scale (GDS)27 was used to indi-
cate clinically significant depressive symptomatology.
To avoid the confounding effects of comorbid con-
ditions, the sample of cognitively intact and PD
patients with MCI, all without dementia and depres-
sion, was chosen for the development of the brief
AES (Fig. 1). The eligible sample of 339 patients was
randomly split into two halves in order to establish
psychometric characteristics and develop the brief
AES in sample 1, and then to cross-validate it in sam-
ple 2 and in a subsample of 42 PD patients with
comorbid dementia and depression (PD-DD). The
PD-DD sample was initially composed of 68
demented PD patients who were excluded previously
during the selection of sample 1 and sample 2 (Fig. 1).
Of these 68 demented patients, 26 nondepressed
patients (GDS score <5) were excluded, resulting in
the final PD-DD sample, comprising 42 PD patients.
Procedure and Materials
Baseline assessment was a single evaluation, and
patients were tested on their regular antiparkinson
medication. Patients underwent a comprehensive
standardized neurologic examination and neuropsy-
chological testing. The UPDRS13 was applied for the
assessment of behavioral, cognitive, affective, and
motor symptoms. The global cognitive status was
assessed with the Mini-Mental State Examination
(MMSE)28 and the Parkinson Neuropsychometric
Dementia Assessment (PANDA).29 In both instru-
ments, lower scores indicate greater cognitive impair-
ment. Depression was screened with the short version
of the GDS,27 containing 15 items. Higher scores on
the GDS indicate higher depressive symptoms.
Apathy was evaluated with the German version
(Lueken et al.19) of the self-rating form of the AES,14 com-
prising 18 items; the answers were recorded by clinical
psychologists. The AES score ranges between 18 and 72.
1081
Psychometric Properties of an Abbreviated Version of the Apathy Evaluation Scale

FIGURE 1. Recruitment of eligible patients in sample 1 and sample 2 for development and validation of the AES brief version.

Higher scores indicate greater apathy, and a score greater
than 38 indicates clinically relevant apathy.30,31 Levo-
dopa equivalent daily doses (LEDDs) were computed
according to Tomlinson et al.32
Analyses of Missing Data
As shown in Figure 1, 83 PD patients with miss-
ing or incomplete AES data and 77 patients with
missing GDS data, representing 24.06% of the orig-
inal sample, were excluded. Comparison of the
completers with the excluded patients by means of
Mann-Whitney U tests showed that the excluded
patients were significantly older (median: 71.00
versus 69.00 years; U = 34.465, p = 0.005) and
showed a tendency to a higher disease duration
(median: 6.42 versus 5.42 years; U = 35.700,
p = 0.101). There were no differences in sex, dopa-
minergic medication, or motor and cognitive
impairment.
Statistical Analyses
The total sample of 339 PD patients was randomly
split into two samples by means of random sampling
of cases. The samples were tested with Mann-
Whitney U tests or x2 tests in order to be similar in
clinical and demographic characteristics, i.e., gender,
disease duration, Hoehn and Yahr stage, AES, and
MMSE score. The data were tested for normal distri-
bution with the Shapiro-Wilk test. The assumption of
normal distribution was not confirmed in sample 1
and sample 2. In the PD-DD subsample, UPDRS I
item 4, UPDRS III, GDS, and LEDD score were not
normally distributed. Differences in demographic,
clinical, and neuropsychological characteristics were
examined with Mann-Whitney U tests or x2 tests. The
data of sample 1 were used to evaluate the psycho-
metric characteristics of the AES. Item difficulty, cor-
rected item-total correlations, and squared multiple
correlation (SMC) coefficients as correlations of each
item (target variable) with the remaining items (pre-
dictor variables) were calculated for each item of the
AES. Spearman rank correlation coefficients were cal-
culated for each item of the AES with the measures of
construct validity (convergent validity: item 4 of the
UPDRS I, assessing motivation; discriminant validity:
UPDRS III score assessing motor impairment, MMSE
and PANDA scores assessing cognitive impairment).
Items that yielded unfavorable characteristics, such
as low corrected item-total correlation, low SMC
and/or small effect correlations with the criterion of

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 Stankevich et al.

convergent validity, were excluded iteratively. After

rejection of one item, corrected item-total correlation
and SMC were calculated for the remaining items in
an iterative way. For the brief AES, internal consis-
tency (Cronbach’s alpha) and Spearman rank correla-
tions with the AES and with the measures of
construct validity were calculated and compared
with the corresponding measures of the AES. This
procedure was repeated in sample 2 and in the PD-
DD subsample. Fisher’s z test was conducted to test
for significant differences in correlations obtained in
sample 1 and sample 2. All Spearman correlations
underwent Bonferroni correction. We report
Cohen’s33 effect size of correlations as small (<0.3),
medium (0.3 0.5), and large (>0.5). Diagnostic accu-
racy of the brief AES-12PD was evaluated with the
receiver operating characteristic (ROC) analysis and
the area under the curve (AUC). Here, the original
AES (cutoff: 38/3917,18) was used as predictor in esti-
mation of sensitivity, specificity, and the optimal cut-
off score of the brief AES-12PD. Statistical analyses
were conducted with SPSS Statistics 23.0 (IBM,
Armonk, NY), and statistical significance alpha was
set to 0.05 for all analyses.
TAGEDH1RESULTSTAGEDN
Sample Characteristics
Demographic, clinical, and behavioral characteris-
tics of the samples are presented in Table 1. Sample 1
and sample 2 did not differ in demographic, behav-
ioral, or clinical measures considered. For demo-
graphic and clinical features in the PD-DD subsample,
see Table, Supplemental Digital Content 1.
Item Selection
Table 2 summarizes psychometric characteristics
of the original AES. After exclusion of one item, cor-
rected item-total correlations and SMCs were com-
puted in an iterative way for the remaining items and
are reflected in the text below. Item six (“S/he puts
little effort into anything”) featured the lowest cor-
rected item-total correlation and the lowest SMC, sug-
gesting a low association with other items of the AES.
It also displayed a rather low mean value, indicating
a low item difficulty. Item six showed a small effect
correlation with UPDRS I item 4 (for correlations of

TABLE 1. Demographic, Clinical, and Neuropsychological Characteristics of Sample 1 and Sample 2

Sample 1 (N = 170) Sample 2 (N = 169) U/x2 (df) p value
Demographic data
Male [n (%)] 119 (70) 119 (70.41) 0.007 (1) 0.934
Age [years] 68.00 68.00 14.839 0.599
Parkinson status
Disease duration [years] 5.42 4.75 15.138 0.211
LEDD [mg] 615.00 609.00 14.312 0.541
Hoehn and Yahr stage [n (%)]
Stage 1 32 (18.94) 31 (18.34)
Stage 2 94 (55.62) 94 (55.62)
Stage 3 36 (21.30) 38 (22.49) 0.161 (4) 0.997
Stage 4 6 (3.55) 5 (2.96)
Stage 5 1 (0.59) 1 (0.59)
UPDRS I item 4: motivation 0.00 0.00 13.531 0.738
UPDRS III score 19.00 20.00 12.877 0.775
Neuropsychological/neuropsychiatric
characteristics
MMSE score 29.00 29.00 13.730 0.467
PANDA score 24.00 24.00 13.898 0.604
GDS score 2.00 2.00 12.981 0.117
MCI [n (%)] 86 (50.59) 82 (48.52) 0.145 (1) 0.703
AES full length [18 items] 27.00 27.00 14.064 0.738
AES-12PD 17.00 18.00 14.054 0.729
AES cutoff 38/39 [n (%)] 13 (7.65) 15 (8.88) 0.169 (1) 0.681

Notes: Data are medians except where noted. Disease duration available for 168 (sample 1)/167 (sample 2); Hoehn and Yahr available for 169
(sample 1); UPDRS I item 4 available for 165 (sample 1)/167 (sample 2); UPDRS III available for 159 (sample 1)/165 (sample 2). GDS used is the
short form. df: degrees of freedom; U: Mann-Whitney U test.

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Psychometric Properties of an Abbreviated Version of the Apathy Evaluation Scale

TABLE 2. Initial Psychometric Characteristics of the AES in Sample 1

Corrected item-total Squared Multiple
Item Mean SD correlations Correlation
1. S/he is interested in things. 1.41 0.571 0.536 0.373
2. S/he gets things done during the day. 1.42 0.583 0.587 0.472
3. Getting things started on her/his own is important to her/him. 1.51 0.673 0.569 0.455
4. S/he is interested in having new experiences. 1.61 0.723 0.634 0.561
5. S/he is interested in learning new things. 1.76 0.809 0.568 0.463
6. S/he puts little effort into anything. 1.32 0.658 0.166 0.143
7. S/he approaches life with intensity. 1.81 0.699 0.546 0.370
8. Seeing a job through to the end is important to her/him. 1.39 0.636 0.630 0.493
9. S/he spends time doing things that interest her/him. 1.39 0.579 0.591 0.456
10. Someone has to tell her/him what to do each day. 1.31 0.705 0.223 0.152
11. S/he is less concerned about her/his problems than s/he should be. 1.72 0.844 0.313 0.235
12. S/he has friends. 1.58 0.840 0.449 0.600
13. Getting together with friends is important to her/him. 1.52 0.723 0.548 0.625
14. When something good happens, s/he gets excited. 1.48 0.690 0.559 0.454
15. S/he has an accurate understanding of her/his problems. 1.80 0.804 0.520 0.403
16. Getting things done during the day is important to her/him. 1.51 0.637 0.668 0.543
17. S/he has initiative. 1.60 0.683 0.743 0.700
18. S/he has motivation. 1.62 0.670 0.714 0.691

Notes: N = 170. SD: standard deviation.

the AES items with measures of construct validity, see
Table, Supplemental Digital Content 2). Due to these
characteristics, item six was rejected.
Item 10 (“Someone has to tell her/him what to do
each day”) had the lowest item difficulty of all items
indicated by the low mean value, and it featured the
lowest corrected item-total correlation (r = 0.204),
accompanied by the lowest SMC (r2 = 0.118). More-
over, item 10 displayed a very low correlation with
UPDRS I item 4. The results imply that item 10 was
less appropriate for the assessment of apathy in the
present sample, and it was rejected.
Item 11 (“S/he is less concerned about her/his
problems than s/he should be”) featured the lowest
corrected item-total correlation (r = 0.291) and the
lowest SMC (r2 = 0.216) of the remaining 16 AES
items as well as a small effect association with UPDRS
I item 4. Due to these unfavorable characteristics, item
11 was rejected.
Of the remaining 15 items, item 12 (“S/he has
friends”) yielded the lowest corrected item-total cor-
relation (r = 0.468), although it had a quite normal
SMC (r2 = 0.597). Furthermore, item 12 featured a
small effect association with UPDRS I item 4, suggest-
ing that it was less suited as part of the scale, and
item 12 was therefore omitted.
Following the rejection of item 12, item 13 (“Get-
ting together with friends is important to her/him”)
showed the lowest SMC (r2 = 0.349) of the remaining
items, suggesting that item 13 was less congruent
with the scale. Item 13 showed a small effect associa-
tion with UPDRS I item 4. Due to these characteris-
tics, item 13 appeared to be less suited for the
assessment of apathy in the present sample, and it
was rejected.
Item 15 (“S/he has an accurate understanding of
her/his problems”) showed a low SMC (r2 = 0.387),
pointing to a rather weak consistency with the
remaining AES items. Item 15 had a rather high mean
value in comparison to other items, suggesting a high
item difficulty. Furthermore, item 15 featured a small
effect association with UPRDS I item four; therefore,
item 15 was rejected.
The remaining AES items featured good psycho-
metric properties. The final AES brief version, com-
prising 12 items, was maintained.
Cross-Validation in Sample 2 and PD-DD
Subsample
The AES-12PD was evaluated in sample 1, includ-
ing for internal consistency (Cronbach's alpha), corre-
lations between full-length and abbreviated version,
and correlations with the measures of construct valid-
ity. To confirm the results, this procedure was
repeated in sample 2. The results are summarized in
Table 3 (see Table, Supplemental Digital Content 3
for item characteristics of the AES in sample 2).
Psychometric properties of the AES and the AES-
12PD in the PD-DD subsample are presented in

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 Stankevich et al.

TABLE 3. Psychometric Characteristicsa of the Full-Length AES (18 items) and the AES Brief Version (AES-12PD) in Sample 1 and
Sample 2

Sample 1 (N = 170) Sample 2 (N = 169)

AES AES-12PD AES AES-12PD z score p value
Correlation with AES-18 1.000 0.949 1.000 0.954 -0.48 0.631
Internal consistency (Cronbach’s alpha) 0.889 0.901 0.897 0.921 -1.08 0.280
Convergent validity
UPDRS I item 4: motivation 0.307 0.339 0.192 0.197 1.4 0.162
Discriminant validity
UPDRS III (motor symptoms) 0.121 0.120 0.077 0.072 0.44 0.656
LEDD 0.211 0.203 -0.037 -0.038 2.23 0.026
MMSE -0.127 -0.137 -0.186 -0.159 0.21 0.834
PANDA -0.199 -0.205 -0.196 -0.137 -0.64 0.522

Notes: Fisher’s z test was applied to test correlation coefficients of the AES-12PD obtained in sample 1 and sample 2; p Bonferroni corrected:
0.05/7 = 0.007. Significant results are presented in bold.
a
Psychometric characteristics were computed as Spearman rank correlation coefficients (sample 1: degrees of freedom = 168, sample 2: degrees
of freedom = 167).

Table 4. The AES-12PD showed a high correlation with In the PD-DD subsample, the AES yielded a small
the AES in both samples and in the PD-DD subsample. effect correlation, and the AES-12PD showed a
In sample 1, the AES-12PD showed high internal con- medium effect correlation with UPDRS I item 4.
sistency, which was higher than the internal consis-
tency of the AES. Similar results with slightly higher
internal consistencies for the AES-12PD were obtained Discriminant Validity
in sample 2 and in the PD-DD subsample. The AES-12PD and the AES featured similar levels of
correlation with the criteria of discriminant validity in
both samples (Table 3). Low associations of the AES-
Convergent Validity 12PD and the AES with the UPDRS III as well as with
The AES-12PD showed a medium effect positive the MMSE score were observed in both samples. Corre-
correlation with UPDRS I item 4 in sample 1, which lations with the PANDA score were somewhat higher,
was higher compared to the AES. In sample 2, both albeit at a low level, in sample 1 as compared to sample
the AES-12PD and the AES exhibited small effect cor- 2. Fisher's z test showed a significant difference in corre-
relations with UPDRS I item 4. lation coefficients of the AES-12PD with dopaminergic
medication (LEDD) in sample 1 and sample 2.
TABLE 4. Psychometric Characteristicsa of the Full-Length In the PD-DD subsample, the AES-12PD and the AES
AES and the AES Brief Version (AES-12PD) in a Sub- showed small effect correlations with the UPDRS III, the
sample of PD Patients with Dementia and Depres- LEDD, and the MMSE and PANDA scores as well as
sion (N = 42)
medium effect correlations with the GDS score (Table 4).
AES AES-12PD
Correlation with AES-18 1.000 0.926
Internal consistency (Cronbach’s alpha) 0.896 0.913
Convergent validity
Receiver Operating Characteristic Analysis
UPDRS I item 4: motivation 0.245 0.281
Discriminant validity The receiver operating characteristic curve was calcu-
UPDRS III (motor symptoms) 0.031 -0.017 lated for the AES-12PD (range: 12 48) from the original
LEDD 0.079 0.056 AES (range: 18 72; cutoff: 38/39) for combined sample
GDS 0.381 0.355
MMSE -0.085 -0.148 1 and sample 2 (N = 339) and separately for the PD-DD
PANDA 0.005 0.008 subsample (N = 42). The AUC in the combined sample
was 0.996 (confidence interval 0.991 1.000; p <0.001).
Notes: Significant results are presented in bold; p Bonferroni cor-
rected: 0.05/8 = 0.006. In the PD-DD subsample, the AUC was 0.931 (confi-
a
Psychometric characteristics were computed as Spearman rank dence interval 0.856 1.000; p <0.001). The cutoff of 25/
correlation coefficients (degrees of freedom = 40).
26 showed in both the combined sample and in the PD-

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Psychometric Properties of an Abbreviated Version of the Apathy Evaluation Scale

TABLE 5. Results of the Receiver Operating Characteristic Analysis and the Area Under the Curve
Combined sample 1 and sample 2
Cutoff 22.5 23.5 24.5 25.5* 26.5 27.5 28.5
Sensitivity 1 1 1 0.964 0.893 0.893 0.821
Specificity 0.836 0.9 0.923 0.961 0.99 1 1
PPV 0.354 0.475 0.538 0.692 0.893 1 1
NPV 1 1 1 0.997 0.99 0.99 0.984
Subsample PD-DD
Cutoff 22.5 23.5 24.5 25.5* 26.5 27.5 28.5
Sensitivity 1 0.960 0.960 0.960 0.840 0.720 0.600
Specificity 0.412 0.412 0.706 0.824 0.824 0.882 1
PPV 0.714 0.706 0.828 0.889 0.875 0.900 1
NPV 1 0.875 0.923 0.933 0.778 0.682 0.630

Notes: Recommended cutoffs as indicators of apathy are presented in bold. Sensitivity, specificity, positive and negative predictive values of the
AES-12PD based on the AES cutoff of 38/39 in combined sample 1 and sample 2 (N = 339) and in subsample PD-DD (N = 42)
*The highest sum of sensitivity and specificity.

DD subsample the highest sum of sensitivity and speci-
ficity (Table 5). In the combined sample, using the cutoff
of 25/26 of the AES-12PD, 27 of 28 patients who were
apathetic according to the AES were correctly diag-
nosed by the AES-12PD, 1 patient missed the diagnosis,
and 299 of 311 were correctly identified as not having
apathy. However, 12 patients were misclassified as apa-
thetic, leading to a reduced positive predictive value
(PPV). The cutoff of 27/28 yielded the highest specific-
ity and PPV at the cost of somewhat lower sensitivity
(25 of 27 apathetic patients were correctly diagnosed; 3
patients missed the diagnosis). Therefore, we suggest
the cutoff of 27/28 as the optimal indicator of apathy in
PD patients without dementia and depression. In the
PD-DD subsample, using the cutoff of 25/26 for the
AES-12PD, 24 of 25 patients were correctly diagnosed
as apathetic, 1 patient missed the diagnosis, 3 patients
were misclassified as apathetic, and 14 of 17 patients
were correctly identified as not having apathy. The cut-
off of 25/26 showed high sensitivity and NPV together
with high specificity and PPV above 0.8. Higher cutoffs
were associated with elevated specificity and PPV but a
considerable reduction in sensitivity and NPV. There-
fore, we suggest a cutoff of 25/26 as an indicator of apa-
thy in PD patients with comorbid dementia and
depression.
TAGEDH1CONCLUSIONSTAGEDN
Although apathy assessment scales have been vali-
dated for PD, clinical routine and large-scale scientific
studies involving multiple assessment time points
need brief, valid, and efficient assessment tools.
Moreover, in the presence of substantial apathetic
symptoms, PD patients are even more easily
exhaustible, and brief questionnaires can provide a
considerable reduction of distress. In the present psy-
chometric study, we reduced the AES and evaluated
the brief version of the AES-12PD, specifically
adapted for PD. The main results are as follows: 1)
the AES-12PD showed high internal consistency com-
parable with the full-length AES; 2) apathy was suc-
cessfully differentiated from motor impairment and
cognitive deficits; 3) the cross-validation within sam-
ple 2 and the PD-DD subsample confirmed good
agreement of the psychometric properties of the AES-
12PD with the results in sample 1; and 4) in PD
patients without dementia and depression, a cutoff of
27/28 for the AES-12PD demonstrated high diagnos-
tic agreement with the AES. In patients with comor-
bid dementia and depression, the optimal AES-12PD
cutoff for apathy was 25/26.
Within the psychometric evaluation of the AES in
sample 1, six items were removed. Lueken et al.18
recently reported a three-factorial solution of the origi-
nal AES in PD, which is largely consistent with the
results of Marin et al.14 and Santangelo et al.17 Accord-
ing to these results, the AES items assessing friendship
(items 12 and 13) and the inverted items (items 6, 10,
and 11) do not load on the main factor of apathy, sug-
gesting that they may be rather influenced by other
factors. In the present sample, item 6, item 10, and
item 11 yielded low correlations with UPDRS I item 4
and with the AES. These aspects—lack of effort,
dependency on others, and lack of concern about one's
own problems—may be more pronounced and more
frequent in PD patients experiencing higher

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impairment due to primary disorder. Items dealing
with friendship (items 12 and 13) and assessing insight
(item 15) were also less suited as part of the brief AES.
As stated above, items on friendship were found not
to be part of the general apathy factor.17,18 Availability
of friends and degree of impairment—but not neces-
sarily apathy—are some of the factors to be considered
in relation to the construct of friendship.34
We found low to moderate convergent validity for
the AES and the AES-12PD using item 4 of the
UPDRS I. As a single item, it does not differentiate
multiple facets of apathy. Therefore, we strongly rec-
ommend using more elaborate measures, such as the
recently proposed diagnostic criteria for apathy.35
Previous psychometric studies did, however, confirm
good general convergent validity of the AES in PD
and various patient groups beyond PD.14,19,36
The AES-12PD featured, in sample 1 and sample 2,
high internal consistencies that were actually better
than those of the AES. Small effect correlations of the
AES-12PD and the AES with the UPDRS III, MMSE,
and PANDA suggest good discrimination of apathy
from motor impairment and cognitive deficits. These
results are consistent with findings reported in recent
studies.17,18
Psychometric properties of the AES-12PD in PD
patients with dementia and depression were compa-
rable with the results obtained in sample 1 and sam-
ple 2, showing that the scale maintains its favorable
psychometric properties even in patients with pro-
nounced neuropsychiatric symptoms. The AES-12PD
featured high internal consistency, low convergent
validity, and good discriminant validity regarding
cognitive (dys)function. However, a medium effect
correlation of apathy with depression, which did not
reach statistical significance, still indicates a certain
overlap of apathy and depression symptoms in this
group. This finding is in line with recent evidence
considering apathy and depression to be frequent
comorbid conditions in PD.2,8,31 However, other stud-
ies have also suggested that apathy and depression
are dissociable constructs in PD.3,37 40 Future studies
should aim to disentangle these syndromes, particu-
larly in patients with neuropsychiatric comorbidities,
to find reliable markers for differentiation.
The ROC yielded the optimal AES-12PD cutoff of
27/28 as an indicator of apathy in PD patients with-
out dementia and depression. The detection of apathy
with this cutoff demonstrated a high accord with the
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Stankevich et al.
AES, confirming its value as a diagnostic tool. In PD
patients with comorbid dementia and depression, the
optimal cutoff for apathy was 25/26, albeit with
lower specificity and positive predictive value. Fur-
ther studies are needed to provide more insight into
the optimal apathy score in the presence of neuropsy-
chiatric comorbidities within clinical samples.
Some methodological limitations need to be men-
tioned. Due to missing or incomplete AES and GDS
data, about a quarter (24%) of the original sample was
excluded from the present analyses. The excluded
patients were older and showed a tendency to a higher
disease duration compared to the completers. For con-
struct validity, item 4 of the UPDRS I was applied,
which showed low correlations with the AES and
AES-12PD. A more accurate evaluation of convergent
validity would have been provided by application of
an additional apathy scale or the diagnostic criteria for
apathy.35 In the present study, the diagnostic criteria
for apathy and an additional apathy scale were not
applied, representing a limitation of the study design.
Only a small sample of PD patients with comorbid
dementia and depression was available for the evalua-
tion of the AES-12PD and the optimal cutoff in this
group. Furthermore, prior to the application of the
AES-12PD in PD patients with comorbid conditions,
estimation of dementia and depressive symptomatol-
ogy is required. A further limitation concerns the
application of the self-rating AES in patients with
dementia, depression, and/or cognitive deficits who
are likely to develop impaired awareness. In these
cases, the assessment should be accompanied by addi-
tional evaluations (e.g., interviewer rating).
The AES is a widely used scale for the assessment of
apathy in PD. In the present study, we aimed to make
the AES a more time-efficient apathy screening. How-
ever, recent theoretical frameworks41 emphasize that
apathy is a multidimensional construct in PD that may
arise from dysfunctions in several domains (cognitive,
emotional, and behavioral). The identification of these
dysfunctions may contribute considerably to the devel-
opment of optimal treatment strategies. The differen-
tial assessment of apathy can be targeted with
multidimensional apathy scales, e.g., the Lille Apathy
Rating Scale, and will likely impact future apathy
assessment.
We here provided the construction of and psycho-
metric properties for an abbreviated version of the
AES, the AES-12PD. When applying the abbreviated
1087
Psychometric Properties of an Abbreviated Version of the Apathy Evaluation Scale
AES-12PD, the assessment time was reduced to one-
third as compared to the original AES. The results sug-
gest that the AES-12PD is a reliable tool for the assess-
ment of apathy in PD patients with and without
comorbid dementia and depression. This self-rating
instrument may reduce time and effort considerably,
especially in the context of repeated administration
and large patient samples.
TAGEDH1CONFLICTS OF INTEREST AND SOURCE
OF FUNDINGTAGEDN
I. Liepelt-Scarfone reports a grant from the German
Ministry for Education and Research (grant 01GI1008C).
J.B. Schulz reports a grant from BMBF (grant
01GI1008C). N. Schmidt reports a grant from the Federal
Ministry of Education and Research. All other authors
report no conflicts of interest related to the research covered
in the article. Data were generated within the LAND-
SCAPE study. The LANDSCAPE study is part of the
Competence Network Degenerative Dementias (KNDD),
which was funded by the German Federal Ministry of Edu-
cation and Research (grant 01GI1008C). The funding
source had no involvement in study design; collection,
analysis, and interpretation of data or in the decision to
submit the article for publication.
Full financial disclosure for the previous 36 months (out-
side the present research initiative), Y. Stankevich has been
funded by the Collaborative Research Centre 940: Volition
and Cognitive Control: Mechanisms, Modulators, Dysfunc-
tions. U. Lueken, O. Riedel, and A. Storch were principal
investigators (June 2012 May 2016) as part of the Collabo-
rative Research Centre 940: Volition and Cognitive Control:
Mechanisms, Modulators, Dysfunctions. U. Lueken is prin-
cipal investigator of the Transregional Collaborative
Research Centre 58: Fear, Anxiety, Anxiety Disorders (July
2016 June 2020). O. Riedel has also received unrestricted
educational grants from Bayer HealthCare and GlaxoS-
mithKline. R. Dodel has received grants from Abbott/Abb-
Vie and Novartis and research grants from Baxter, BMBF
(DLR), Deutsche Gesellschaft fu €r Neurologie, Deutsche
Parkinson Vereinigung, Faber-Stiftung, Internationale Par-
kinson Fonds, Michael J. Fox Foundation, UKGM, EU
Horizon 2020, AOK Gesundheitskasse Hessen, and AOK
Gesundheitskasse Sachsen und Th€ uringen. R. Dodel has
also received honoraria from the consulting/advisory board
for Abbott/AbbVie, Novartis, DZNE Deutsches Zentrum
€r neurodegenerative Erkrankungen, Lilly, Medizinische
fu
1088
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Hochschule Hannover, Pfizer, Med Update, Studienstiftung
des deutschen Volkes, Axon Neuroscience, Klinikum Fulda,
Krankenhaus der Barmherzigen Br€ uder Trier, Ono Pharma
UK Ltd., Dr. Willmar Schwabe GmbH & Co. KG, Akade-
mie f€ur medizinische Fortbildung, and Johanniter GmbH.
R. Dodel has received honoraria for authorship from Thieme
Verlag and Kohlhammer GmbH. D. Berg has received
grants and personal fees from UCB Pharma GmbH, grants
from Lundbeck, Janssen Pharmaceutica NV, Parkinson-
Fonds Deutschland gGmbH, BMWi, BMBF, Michael J. Fox
Foundation, and Novartis Pharma GmbH. D. Berg also
reports personal fees from Prexton Therapeutics, GE Health-
care, BIAL, and Bayer. I. Liepelt-Scarfone has received unre-
stricted research grants from International ParkinsonFonds
(Deutschland) GmbH (IPD) and Johnson & Johnson and
grants from the European Commission and the National
Center of Excellence in Research, University of Luxem-
bourg. R. Hilker-Roggendorf has received speaker honoraria
from Medtronic, Orion, GlaxoSmithKline, Teva, Cephalon,
Solvay, Desitin, Ipsen, Merz, Archimedes Pharma, and
Boehringer Ingelheim as well as travel funding from Med-
tronic, Allergan, and Cephalon. He has served on a scientific
advisory board for Cephalon and has received research fund-
ing from the Deutsche Parkinson Vereinigung (dPV), Bun-
desministerium f€ ur Bildung und Forschung, and Goethe-
University Frankfurt. E. Kalbe has received research grants
from the German Ministry for Education and Research
(BMBF) and honoraria from Novartis Pharma GmbH and
AbbVie Pharma GmbH. J.B. Schulz has received grants
from HEALTH-F2-2010- 242193, BMBF, GeNeMove, and
EU, EUROSCA. A. Spottke has received unrestricted edu-
cational grants from UCB. K. Witt has received grants from
the German Research Council and the German Ministry of
Education and Health and receives fees from Bayer Health-
Care, Medtronic, and BIAL. K. Reetz is partly funded by
the German Federal Ministry of Education and Research
(BMBF 01GQ1402) and has received honoraria for presen-
tations from Lilly and research grants from Pfizer, Merck,
and the Alzheimer Forschung Initiative e.V. (AFI 13812).
B. Mollenhauer has received independent research grants
from Teva Pharmaceutical Industries, Desitin, Boehringer
Ingelheim, and GE Healthcare; honoraria for consultancy
from Bayer Schering Pharma AG, Roche, AbbVie, Teva
Pharmaceutical Industries, and Biogen and for presenta-
tions from GlaxoSmithKline, Orion Pharma, and Teva
Pharmaceutical Industries; and travel costs from Teva Phar-
maceutical Industries. B. Mollenhauer is a member of the
executive steering committee of the Parkinson Progression
Marker Initiative of the Michael J. Fox Foundation for
Am J Geriatr Psychiatry 26:10, October 2018

Parkinson's Research; has received grants from BMBF, EU,
Deutsche Parkinson Vereinigung, Michael J. Fox Founda-
tion for Parkinson's Research, and Stifterverband f€
ur die
deutsche Wissenschaft; and has scientific collaborations
with Roche, Bristol-Myers Squibb, Ely Lilly, Covance, and
Biogen. N. Schmidt has received travel grants from Med-
tronic. A. Storch has received funding from the Bundesmi-
nisterium fu€r Wirtschaft und Technologie, the Deutsche
Forschungsgemeinschaft, and the Helmholtz Association.
He has received unrestricted research grants from Teva
Pharmaceutical Industries and Global Kinetics Corporation
and honoraria for presentations/advisory boards/consulta-
tions from GKC, Pfizer Ltd., Mundipharma, UCB, Gru €nen-
thal, AbbVie, Zambon, Teva, Meda Pharmaceuticals,
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