APADEM-NH: Apathy Scale Validation in Dementia Patients

A Novel Rating Scale for the Measurement of
Apathy in Institutionalized Persons with
Dementia: The APADEM-NH
Luis Agüera-Ortiz, M.D., Ph.D., Nuria Gil-Ruiz, Ph.D., Isabel Cruz-Orduña, Ph.D.,
Isabel Ramos-García, M.D., Ricardo S. Osorio, M.D., Meritxell Valentí-Soler, M.D.,
Javier Olazarán-Rodriguez, M.D., Ph.D., Jos!
e L. Dobato-Ayuso, M.D., Ph.D.,
Krista Lanctôt, Ph.D., Pablo Martínez-Martín, M.D., Ph.D.
Objective: Apathy is one of the most frequent symptoms of dementia, still needing
better measurement methods. The objective of this study was to validate a new scale for
apathy in institutionalized persons with dementia (APADEM-NH). Methods: The scale
includes 26 items distributed in three dimensions: Deficit of Thinking and SelfGenerated behaviors (DT): 13 items, Emotional Blunting (EB): 7 items, and Cognitive Inertia (CI): 6 items. The sample included 100 institutionalized patients (90%
female) with probable Alzheimer disease (AD) (57%), possible AD (13%), AD þ
cerebral vascular disease (17%), Lewy body dementia (11%), and Parkinson associated to dementia (2%), covering all stages of dementia severity according to the
Global Deterioration Scale and Clinical Dementia Rating. Additional assessments
were the Apathy Inventory, Neuropsychiatric Inventory, Cornell Scale for Depression,
and the tested scale. Re-test and inter-rater reliability were carried out in 50 patients.
Results: All subscales lacked relevant floor and ceiling effects (<15%). Internal
consistency for each dimension was (Cronbach’s a): DT ¼ 0.88, EB ¼ 0.83, CI ¼ 0.88;
item-total correlations were >0.40; and item homogeneity 0.36e0.51. Testeretest
reliability for the items was kW ¼ 0.48e0.92; for the subscales, intraclass correlation
coefficient (ICC) ¼ 0.80e0.88; and for the total score, ICC ¼ 0.90. Inter-rater reliability reached kW values of 0.84e1.00; subscales ICC, 0.97e0.99, and total score ICC,
0.99. Standard error of measurement for total score was 6.41 and internal validity
ranged from rS ¼ 0.69e0.80. Conclusions: APADEM-NH proved to be feasible, reliable, and valid for apathy assessment in institutionalized patients suffering mild to
severe dementia, discerning well between apathy and depression. (Am J Geriatr
Psychiatry 2015; 23:149e159)
Received October 18, 2012; revised January 27, 2013; accepted January 31, 2013. From the Alzheimer Disease Research Unit, CIEN Foundation, Carlos III Institute of Health, Alzheimer Center Reina Sofia Foundation (LA-O, NG-R, IC-O, IRG, MV-S, JO-R, JLD-A, PM-M), Madrid,
Spain Centro de Investigación Biom!edica en Red de Salud Mental, CIBERSAM (LA-O), Madrid, Spain; Center for Brain Health, NYU Langone
Medical Center, NYU School of Medicine (RSO), New York, NY; Sunnybrook Health Sciences Centre (KL), Toronto, Canada; and the Centro
de Investigación Biom!edica en Red sobre Enfermedades Neurodegenerativas, CIBERNED (PM-M), Madrid, Spain. Send correspondence and
reprint requests to Luis Agüera-Ortiz, M.D., Ph.D., Alzheimer Disease Research Unit, CIEN Foundation, Valderrebollo, 5 28031- Madrid,
Spain. e-mail: [email protected]
Supplemental digital content is available for this article in the HTML and PDF versions of this article on the journal’s Web site (www.
ajgponline.org).
! 2015 American Association for Geriatric Psychiatry
http://dx.doi.org/10.1016/j.jagp.2013.01.079
Am J Geriatr Psychiatry 23:2, February 2015
149
Validation of the APADEM-NH Apathy Scale
Key Words: Apathy, dementia, rating scale, institutionalized persons, validation study,
psychometrics
A
pathy is commonly defined as a persistent
deficit of motivation, feelings, emotions, and/or
interests that leads to a significant reduction in selfgenerated behaviors aimed at a goal.1 The term is
frequently associated with other concepts, such as
indifference, lack of motivation, and procrastination,
and can refer to cognitive, affective, or behavioral
symptoms. Apathy can be confounded by other
symptoms, such as depression, anxiety, agitation,
irritability, or motor slowing, making the assessment
of this syndrome challenging.
A recent international consensus has proposed new
diagnostic criteria for the apathy syndrome to be
applied in clinical practice.2 The development of these
new criteria is a step forward toward a more standardized diagnosis. Apathy is one of the most frequent
neuropsychiatric symptoms of dementia, particularly
in Alzheimer disease (AD), where the prevalence of
apathy is around 55% (even 75% in some studies) both
in the community and in nursing homes.3e6 Studies
using the Neuropsychiatric Inventory (NPI)7 identified apathy as one of the most common and prominent
symptoms associated with dementia, especially in
nursing homes, where its prevalence tends to increase
with time and placement in such institutions can be
partially predicted by the symptom.8,9
Apathy is a major obstacle in dealing with the
demented patient, both in clinical practice and in daily
care. Patients with dementia encounter severe difficulties in performing or being involved individually
in the activities of daily living and may have limited
access to nonpharmacological therapies. With limited
pharmacologic10 and nonpharmacologic11 interventions for apathy, caregivers may be frequently faced
with a lack of the resources needed to motivate
patients and to improve the symptom. The lack of
adequate treatment and support affects the quality of
life of many patients. As a result, apathy is a major
challenge for professionals assisting this population.
To date, the scientific literature has emphasized two
apathy models. Marin0 s model12 defines apathy as a
“motivation reduction, not justified by an altered level
150
of consciousness, cognitive impairment, or emotional
distress.” This motivation decrease must be persistent
over time. The author identifies three dimensions of
apathy: a decrease or reduction of emotional response
(emotional numbing), a decrease or reduction of
cognitive activity directed to a specific purpose or goal,
and a decrease or reduction of behavior directed to
a specific purpose or goal. This definition has been key
to the conceptualization of apathy as a distinct
syndrome. Nevertheless, it has been criticized by some,
concerning the subjectivity of its main concept: motivation is an imprecise and non-homogenous psychological concept that is difficult to operationalize.
Levy and Dubois’s model1 defines apathy as
a “quantitative reduction of voluntary self-generated
and purposeful behavior.” In this model, the symptoms of apathy must be always noticeable and
measurable. Moreover, there must be a distinct
contrast between the profound alteration of selfgenerated behavior and the appearance of purposeful behavior after external stimulation, which may
remain relatively preserved. This means that apathy
can be reduced at least partially after external stimulation of different intensity. Levy and Dubois
propose three dimensions of apathy: Emotional
Blunting, Cognitive Inertia, and Deficit of Thinking
and Self-Generated Behaviors.
The most commonly used specific scales for apathy
assessment are the Structured Clinical Interview for
Apathy,13 the Apathy Evaluation Scale,14,15 the
Apathy Scale,16 the Apathy Inventory (AI),17 the
Dementia Apathy Interview and Rating,18 and the
Lille Apathy Rating Scale.19 These assessments are
mostly based on Marin0 s model, which is centralized
around a lack of motivation. The application of the
most frequent apathy rating scales offers advantages
and disadvantages (Table 1). In institutionalized
patients with advanced dementia, the existing apathy
rating scales frequently show marked ceiling effects
(i.e., scoring at or near the maximum indicating highest degrees of apathy), making such an assessment
nondiscriminatory or useless in these populations.
Am J Geriatr Psychiatry 23:2, February 2015
Am J Geriatr Psychiatry 23:2, February 2015
Low correlation
with depression
and anxiety
measurements:
PANSSedepression
and PANSSeanxiety
subscales.
Discriminant
Validity
Long application
20 min.
Low correlation
between AES-10
and NPI-depression
subscale (r ¼ 0.09).
High correlation
between AES-10
and other Apathy
measures
AES (r ¼ 0.97) and
NPI-a (r ¼ 0.62).
High correlation
between Apathy scores
and an independent
clinician0 s blind
assessment of
Apathy on
Likert-like scale.
Low correlation
with depression
subscale of the
Consortium to
Establish a
Registry for
Alzheimer Disease
behavior Rating
Scale for dementia.
(r ¼ 0.08).
Creation and
validation for
specific population
(dementia).
r ¼ 1.00
56 days for
the second
interview
r ¼ 0.85
a ¼ 0.89-0.94
NO
Dementia Apathy
Interview
and Rating (DAIR)
AI score discriminate
controls from
patients based on
Apathy symptoms.
The item “Lack
of interest”
does not show good
discriminant properties.
Correlation between
the Items lack
of initiative
(r ¼ 0.23) and
lack of interest
(r ¼ 0.66) with
NPI-Apathy subscale.
Not assessed.
No studies.
r ¼ 0.99
Time not reported
for the second
interview
r ¼ 0.96
a ¼ 0.84
NO
Apathy
Inventory
(AI)
NPI-NHa susceptible to
halo effect and high ceiling
effect in severe stages.
A change of 4 points or more is
needed for estimating a
significant change in Apathy
symptoms, specially
in extreme scores.
NPI-NH time application : 30 min.
Not assessed for Apathy
subscale.
For NPI-a: r ¼ 0.74
Time not reported for the
second interview.
NPI-NHa; 0.71 and 72 hours
interval.
NPI-a; -r ¼ 0.98 for
frequency and
0.89 for severity.
Not assessed for NPI-NHa.
High correlation with
AES, AS-10NH (r ¼ 0.50
and r ¼ 0.61) and
AI (r ¼ 0.66)
Not assessed for NPI-NHa.
a ¼ 0.87e0.88 (NPI)
a ¼ 0.67 (NPI-NH)
YES (NPI-NH version)
Neuropsychiatry
Inventory (NPI)
(Apathy subscale NPI-a)
Creation and
validation
for specific
population
(Parkinson
disease).
Low correlation
with depression
measurements:
MADRS.
High correlation
with AES
(r ¼ 0.87).
ICC ¼ 0.98
4 months for
the second
interview
r ¼ 0.95
a ¼ 0.80
NO
Lille Apathy
Rating Scale
(LARS)
Notes: a: Cronbach’s a; r: Spearman correlation coefficient; ICC: intra-class correlation coefficient; PANSS: Positive and Negative Syndrome Scale; MADRS: Montgomery Asberg
Depression Rating Scale; NPI-NHa: NPI-NH apathy item.
Long application:
at least 10e20 min
for trained interviewer.
Time shorter
for short version.
High correlation
with other Apathy
measures: NPI-a,
the LARS and
PANSS-negative
symptom subscale.
Convergent
validity
NOTES
ICC ¼ 0.94
r ¼ 0.81(AES-14)
a ¼ 0.92
(AS-10-NH)
1 week for the
second interview
r ¼ 0.90 (AES-14)
a ¼ 0.86e0.94
25 days for the
second
interview
r ¼ 0.76e0.94
YES, Only for AS10 items (AS-10-NH
version)
Apathy Scale (AS)
(AS-7, AS-14, AS-10)
YES (AES-short
version)
Iterrater
reliability
Validation
in nursing
home (NH)
inpatients
Internal
Consistency
Testeretest
reliability
Apathy
Evaluation
Scale (AES)
TABLE 1. Psychometric Properties of the Most Frequently Used Apathy Scales
Agüera-Ortiz et al.
151
Validation of the APADEM-NH Apathy Scale
The APADEM-NH (APAthy in DEMentia, Nursing
Home) scale was specifically designed to measure
apathy in institutionalized patients with neurodegenerative dementia by considering the special
characteristics of the most severe stages of the illness
and the distinctiveness of the institutional environment such as group-living or professional caregiving.
The scale responds to the need of a measurement
instrument to overcome the limitations of the existing
apathy scales, especially the “ceiling” effects.
The main objective of the present study was to
develop and test a scale for assessing apathy in institutionalized patients with dementia in all severity
stages, even the most severe.
METHODS
Patients
The APADEM-NH was applied to a sample of institutionalized patients with a diagnosis of dementia
based on the Spanish version of DSM-IV-TR criteria.20
Patients in all stages of dementia severity according to
the Global Deterioration Scale (GDS) and Clinical
Dementia Rating (CDR) were included. All patients
were institutionalized at the Alzheimer Center Reina
Sofia Foundation at the time of the study, with
a generic diagnosis of “neurodegenerative dementia”
at entry. All subjects and/or their legal representatives signed the informed consent for the study, which
was approved by the institutional Ethics Committee.
Assessments
The APADEM-NH is a shortened version of the
APADEM-NH-66 rating scale, which was created to
assess apathy in institutionalized dementia patients.
Data about the design and the validation process of
the preliminary longer version of the scale are available elsewhere.21 An item reduction process was performed on the APADEM-NH-66, by factor analysis
techniques and expert criteria, and resulted in the
shorter, 26-item version used in this study: the
APADEM-NH. Details of the process of item reduction have also been published22 but not the validation
and psychometric characteristics of the final 26-item
version that constitute the core of the present work.
The original Spanish version has undergone the usual
translation, back-translation, and approval process
152
TABLE 2. Characteristics of the Sample (N [ 100)
%
Sex
Female
Male
Age groups, years
#74
75e84
$85
Education
Illiterate
Incomplete primary education
Primary education
Secondary education
Superior
Diagnosis etiologies
Probable AD
Possible AD
AD with CVD
Lewy Bodies Dementia
Parkinson associated to dementia
CDR global
1 Mild
2 Moderate
3 Severe
GDS
4 Mild
5 Moderate
6 Moderately severe
7 Severe
90
10
6
44
50
13
19
62
4
2
57
13
17
11
2
4
26
70
4
21
33
42
Notes: AD: Alzheimers disease; CVD: cerebro-vascular disease;
CDR: clinical dementia rating; GDS: Global Dementia Scale.
and resulted in the items appearing in Appendix 1
(available online).
The scale consists of 26 items, distributed across
the three dimensions of apathy described by Levy
and Dubois: Deficit of Thinking and Self-Generated
behaviors (DT): 13 items, Emotional Blunting (EB):
7 items, and Cognitive Inertia (CI): 6 items.
The APADEM-NH assesses the patient’s state of
apathy through an interview with a professional
TABLE 3. Score Distribution of the Applied Rating Scales
Apathy Inventory
Neuropsychiatric
Inventory
Apathy item
Depression item
Cornell scale for
depression in dementia
Observed Theoretical
range
range
Mean
SD
16.05
11.08
0e36
0e36
3.22
1.47
6.65
3.89
2.96
5.27
0e12
0e12
0e24
0e12
0e12
0e38
Notes: SD: standard deviation.
Am J Geriatr Psychiatry 23:2, February 2015
Agüera-Ortiz et al.
caregiver who has a good level of knowledge (e.g.,
caring for the patient on a regular basis) of the
cognitive and functional status of the patient. Each
item is scored from 0 to 3, depending on the severity
measured by the intensity of stimulation needed to
perform a specific task or elicit a response: 0 ¼ No
Apathy (spontaneous emotion or action), 1 ¼ Mild
Apathy (action or emotion needs some kind of stimulation), 2 ¼ Moderate Apathy (action or emotion
obtained only with intense stimulation), and 3 ¼
Severe Apathy (not responding to any intervention).
In addition to APADEM-NH, patients’ psychopathology and severity of illness was measured, using
the validated Spanish versions of the following
instruments: GDS;23 CDR;24 The Apathy and Depression items of the Neuropsychiatric Inventory-Nursing
Home (NPI-NH);7,25 Cornell Scale of Depression in
Dementia (CSDD);26,27 and the AI.17 Four experienced
psychiatrists and psychologists who were blind to the
patients’ clinical data and the other rating scales
applied the APADEM-NH independently.
Re-test and inter-rater reliability evaluations were
carried out in 50 patients.
Data Analysis
Descriptive statistics were used for demographic,
medical history, and assessment data of the sample.
Inter-observer and testeretest reliability were performed on 50% of the sample (N ¼ 50). The following
psychometric attributes of the APADEM-NH scale
were analyzed.
Feasibility and acceptability. Quality of data was
considered satisfactory if more than 90% of
TABLE 4. Data Quality and Acceptability Parameters of the Scale
Domain/Item
D1. Deficit of Thinking
Item 1
Item 2
Item 3
Item 4
Item 5
Item 6
Item 7
Item 8
Item 9
Item 10
Item 11
Item 12
Item 13
Total Deficit of Thinking
D2. Emotional Blunting
Item 14
Item 15
Item 16
Item 17
Item 18
Item 19
Item 20
Total Emotional Blunting
D3. Cognitive Inertia
Item 21
Item 22
Item 23
Item 24
Item 25
Item 26
Total Cognitive Inertia
APADEM-NH
Total
Fully
computable (%)
Mean
Median
SD
Min.
Max.
Skewness
Floor
effect (%)
Ceiling
effect (%)
100
100
100
99
100
100
97
98
97
97
93
94
95
89
0.32
0.72
0.63
1.03
0.69
0.83
1.98
1.37
1.51
2.30
1.79
1.88
2.26
16.90
0.00
0.00
0.00
0.00
0.00
0.00
2.00
0.00
1.00
3.00
3.00
3.00
3.00
16.00
0.78
1.12
1.11
1.32
1.25
1.29
0.96
1.45
1.41
1.17
1.39
1.28
1.11
9.87
0
0
0
0
0
0
0
0
0
0
0
0
0
0
3
3
3
3
3
3
3
3
3
3
3
3
3
38
2.4
1.23
1.37
0.68
1.3
1.02
%0.39
0.18
%0.01
%1.24
%0.39
%0.47
%1.1
0.26
83.0
65.0
73.0
57.6
76.0
68.0
6.2
51.0
42.3
16.5
33.3
23.4
12.6
1.1
4.0
15.0
13.0
27.3
22.0
24.0
38.1
41.8
44.3
71.1
54.8
52.1
65.3
2.2
99
99
100
97
99
96
93
88
1.01
1
0.5
1.07
1.41
1.33
1.36
7.27
1.00
0.00
0.00
0.00
1.00
0.50
1.00
6.00
0.97
1.35
1.09
1.34
1.41
1.42
1.41
6.17
0
0
0
0
0
0
0
0
3
3
3
3
3
3
3
21
0.72
0.7
1.78
0.62
0.12
0.22
0.16
0.68
35.4
62.6
82.0
56.7
45.5
50.0
48.4
10.2
11.1
28.3
14.0
29.9
40.4
38.5
37.6
2.3
92
93
89
94
92
91
83
1.75
1.11
1.55
1.54
1.87
1.22
8.36
2.00
1.00
2.00
2.00
3.00
1.00
7.00
1.26
1.25
1.27
1.38
1.4
1.12
5.84
0
0
0
0
0
0
0
3
3
3
3
3
3
18
%0.34
0.52
%0.15
%0.08
%0.51
0.37
0.15
27.2
48.4
34.8
40.4
32.6
35.2
8.4
42.4
23.7
32.6
41.5
57.6
18.7
6.0
74
30.95
27.50
20.28
0
74
0.49
1.3
1.3
Notes: SD: standard deviation; Min: minimum; Max: maximum
Am J Geriatr Psychiatry 23:2, February 2015
153
Validation of the APADEM-NH Apathy Scale
APADEM-NH data were fully computable.28,29 The
difference between mean and median (arbitrary
limit, 10% of the maximum possible score),30 floor
and ceiling effects (maximum acceptable for both,
15%),31 and the skewness (limits: %1 to þ1) was
calculated.32
Internal consistency and reliability. Internal consistency was tested using the Cronbach’s coefficient
(criterion value $0.70),33 item-total correlation (criterion
value $0.40),34 and item homogeneity (criterion
value $0.30).35 Item reproducibility was tested by
weighted k (quadratic weights). For total scores of the
domains and the scale, intraclass correlation coefficient
(ICC, one-way random effects for testeretest and twoway random effects for inter-rater reliability) was
used. For satisfactory reliability, a threshold value
greater than or equal to 0.70 was considered.36,37
Construct validity. When examining correlations
with APADEM-NH and on the basis of previous
studies,22 we a priori hypothesized a strong association (rS >0.50) with the AI and the NPI-Apathy
item, a moderate correlation (rS: 0.35e0.50) with
dementia severity (CDR, GDS), and a low association
(rS <0.35) with depression measurements (Cornell
Depression Scale and NPI-depression item).38
Internal validity was determined on the basis of
intercorrelations of APADEM-NH domains (standard, rS: 0.30e0.70).39 The Spearman correlation
coefficient was used because assumptions required
to use parametric tests were not met. Known-groups
validity was explored on the grouping of patients by
dementia severity levels based on GDS and CDR
scores, using the Kruskal-Wallis test for group
comparisons.
Precision. Standard error of measurement (SEM),
based on the ICC as reliability index, was calculated
for each APADEM-NH domain and the total
score.31
Table 2. Descriptive statistics of the applied measures
are shown in Table 3.
Feasibility and Acceptability
The data were fully computable for 74% of the
sample, with 3.7% (96/2,600) missing item values:
2.3% for DT; 2.4% for EB; and 8.2% for CI. Missing
data were predominantly due to the impossibility of
assigning an item’s score to a particular patient
because of severe mobility reduction, aphasia, or
important sensorial deficits. In addition, some
missing data were due to non-observed items (lack of
information about the item by the caregiver interviewed). Imputation was not carried out for missing
data. Patients with and without missing data were
comparable, with no statistically significant differences in age, education, sex, diagnosis, CDR, GDS,
or AI.
Distribution of APADEM scores, data quality, and
acceptability parameters are shown in Table 4. For all
subscales and total score, floor and ceiling effects
were lower than 15% (Fig. 1) and skewness was
within the limit values. The mean application time
was 9.6 minutes.
Internal Consistency and Reliability
Table 5 displays data on internal consistency and
reproducibility of the APADEM-NH Subscales and
total score. In summary, Cronbach’s a coefficients
FIGURE 1. Histogram showing the distribution of the
APADEM total scores (oberved range: 0e74
points).
RESULTS
Description of the Sample
A total of 100 institutionalized patients with the
diagnosis of dementia covering all stages of the
disease severity were included. Mean age (&SD) was
84.8 & 6.4 (range: 58e97) years; 90% women. Selected
demographic and clinical variables are presented in
154
Am J Geriatr Psychiatry 23:2, February 2015
Agüera-Ortiz et al.
TABLE 5. Reliability of the APADEM-NH
Domain/Item
Internal consistencya
Testeretest Reliabilityc
Inter-rater reliabilityc
0.46
0.61
0.62
0.43
0.56
0.52
0.60
0.68
0.64
0.59
0.58
0.56
0.66
(0.88)b
0.84
0.48
0.92
0.81
0.77
0.54
0.70
0.81
0.70
0.79
0.69
0.69
0.49
[0.88]d (0.84e0.89)
0.96
0.89
0.93
0.84
0.95
0.99
0.88
0.98
0.97
0.95
0.92
0.93
0.93
[0.99]d (0.98e0.99)
0.59
0.59
0.61
0.47
0.64
0.64
0.62
(0.83)b
0.76
0.58
0.49
0.64
0.67
0.82
0.67
[0.82]d (0.80e0.91)
0.98
0.99
1.00
0.99
0.99
0.99
0.96
[0.99]d (0.99e0.99)
0.71
0.70
0.72
0.72
0.61
0.57
(0.86)b
0.78
0.69
0.52
0.55
0.70
0.78
[0.80]d (0.72e0.80)
0.94
0.96
0.90
0.96
0.95
0.96
[0.97]d (0.94e0.98)
—
0.90d (0.88e0.92)
0.99 (0.98e0.99)
D1. Deficit of Thinking
Item 1
Item 2
Item 3
Item 4
Item 5
Item 6
Item 7
Item 8
Item 9
Item 10
Item 11
Item 12
Item 13
Total Deficit of Thinking
D2. Emotional Blunting
Item 14
Item 15
Item 16
Item 17
Item 18
Item 19
Item 20
Total Emotional Blunting
D3. Cognitive Inertia
Item 21
Item 22
Item 23
Item 24
Item 25
Item 26
Total Cognitive Inertia
APADEM-NH
Total
a
Item-total correlation.
Cronbach’s a index.
c
Weighted k (quadratic weights).
d
Intraclass correlation coefficient (95% confidence interval).
b
ranged from 0.83 (EB) to 0.88 (DT) and the item-total
corrected correlations reached values from 0.43 to
0.72. Item homogeneity values were: DT, 0.36; EB,
0.39; and CI, 0.51. Mean time elapsed between test
and retest was 13.76 & 4.53 (range: 7e25) days.
Regarding item testeretest reliability, the k index
reached values from 0.48 (Item 2) to 0.92 (Item 3). For
domains, the ICC ranged between 0.80 (CI domain)
and 0.88 (DT domain). Concerning the inter-rater
reliability, k reached values between 0.84 (Item 4)
and 1.00 (Item 16) and for domains, the ICC ranged
from 0.97 (CI domain) to 0.99 (EB domain). ICC
values greater than or equal to 0.90 were found for
the APADEM-NH total score for both modalities of
reliability.
Am J Geriatr Psychiatry 23:2, February 2015
Construct Validity and Precision
The APADEM-NH total score showed low to
moderate correlation coefficients with apathy scales
(AI, rS ¼ 0.33, p ¼ 0.004; NPIa, rS ¼ 0.31, p ¼ 0.008);
high correlation with CDR and GDS (rS $0.50;
p <0.0001); and no correlation with depression scales
(NPId, rS ¼ e0.003; CSDD, rS ¼ 0.10; both, nonsignificant) (Table 6). The correlation coefficients
among the APADEM-NH subscales ranged from 0.69
to 0.80 (all, p <0.0001). APADEM-NH total score
increased significantly with dementia severity level
and discriminated between patients grouped by GDS
(Kruskal-Wallis test: c2 ¼ 27.83; df ¼ 3; p <0.0001)
and CDR (Kruskal-Wallis test: c2 ¼ 17.826, df ¼ 2;
155
Validation of the APADEM-NH Apathy Scale
TABLE 6. Correlation Between APADEM-NH and Other
Measuresa
Convergent
validity
AI
NPIa
NPId
CSDD
CDR
GDS
Deficit of
Thinking
(N [ 89)
Emotional
Blunting
(N [ 88)
Cognitive
Inertia
(N [ 83)
Total
(N [ 74)
0.46
0.27
0.05
0.16
0.49
0.61
0.31
0.10
%0.14
%0.001
0.40
0.49
0.24
0.31
%0.06
0.03
0.47
0.60
0.33
0.31
%0.003
0.10
0.51
0.63
Notes: AI: Apathy Inventory; NPI: Neuropsychiatric Inventory;
NPIa: NPI Apathy Item; NPId: NPI Depression Item; CSDD:
Cornell Scale for Depression in Dementia; CDR: Clinical Dementia
Rating. GDS: Global Dementia Scale.
a
Spearman rank correlation coefficients (not significant if
rS <0.24 to p <0.0001 if rS >0.45).
p <0.0001) severity levels. SEM ranged from 2.61 (CI
domain) to 3.42 (DT domain) for the domains and
was 6.41 for the total score.
CONCLUSIONS
This study refers to the validation of the first rating
scale specifically designed for assessment of apathy
in institutionalized patients with dementia by
neurodegenerative disease. The scale items were built
after an extensive period of observation of the
behaviors of the demented patients living in our
nursing home/research facility and a selection
process of the most relevant ones by statistical means
that has been described elsewhere.22
Despite its prevalence, and probably due to its
undisruptive nature, apathy in dementia has received
little attention and the development of a measurement for the presence and severity of apathy in
institutionalized patients has subsequently been
neglected. Nevertheless, apathy causes most of the
functional disability linked to dementia.6,40 To date,
several scales have been published for the evaluation
of apathy. Despite the existence of these published
scales, their application to persons with dementia,
especially those at the most advanced stages or those
who are institutionalized, proves to be frequently
disappointing. In these circumstances, the briefer
scales have limited practical value for clinical practice
or research, because of an excessive ceiling effect,
where most patients receive the maximum score.
Excessive floor or ceiling effects are problematic as
156
they heavily imbalance the sensitivity and responsiveness of the instrument.
Dementia imposes its own characteristics to the
apathy syndrome, making it different from other
common causes of apathy, like depression or
schizophrenia, where cognitive impairment does not
play such a significant role. Thus, general scales that
measure apathy independently of the underlying
condition are of limited value in dementia patients.41
Our aim was to create a new specific instrument for
dementia, rather than adapting an existing general
scale. The conceptual framework used for the design
of the new scale was the one described by Levy and
Dubois, because the three dimensions that it is based
on are easier to measure and transport to a rating
scale than the concept of motivation used in existing
general scales, which is a concept difficult to measure
in practice objectively.
The APADEM-NH is a scale applied by a rater
who collects information from a caregiver with
optimal knowledge of the patient. The characteristics
of dementia populations make a self-rated instrument unfeasible. The informant should not be a relative, even in the case of daily visits, in order to avoid
subjective and emotionally biased responses that
could interfere with the assessment. The scoring
system reflects the theoretical frame chosen and is
based on the degree of stimulation needed to elicit
the response.
Acceptability of the scale was satisfactory in all
dimensions. Scores covering the whole possible range
of scoring, without a significant skew in the distribution, were obtained in the three subscores and in
the total APADEM-NH score. Missing data corresponded mainly to the subscale CI (8.2%), but still
remained under the 10% limit.28,29 Despite nonimputation of data, 74% of the observations were
fully computable. A clear strength of the scale,
specifically intended in its design, is the absence of
floor and ceiling effects in the three dimensions. This
absence allows for a potentially adequate measurement of the different levels of intensity of the
construct and responsiveness.
The internal consistency of the APADEM-NH
subscales was satisfactory, with all coefficients above
the threshold values. The testeretest reliability analysis also demonstrated that responses to APADEMNH questions were stable over short intervals, with
73.1% of the items, the three subscores, and the total
Am J Geriatr Psychiatry 23:2, February 2015
Agüera-Ortiz et al.
score reaching values well above the 0.70 standard
level. The inter-rater reliability was optimal. The
APADEM-NH total score, therefore, possesses
a satisfactory stability and reproducibility (Table 5).
Concerning the hypothesized associations for
construct validity, a lowemoderate correlation was
found between the APADEM-NH and the two other
apathy measurements applied. This might be due to
the fact that the three-item AI and the apathy item of
the NPI-NH are much shorter scales with known
ceiling effects and different scoring methods. Correlation between the APADEM-NH and the depression
measurements was negligible. Apathy and depression are psychopathologically related, with a certain
degree of apathy frequently being observed in
depressive episodes. Nevertheless, it is possible to
find apathy without depression, and this can be
the case in many neuropsychiatric diseases, including dementia.42 The low correlation between the
APADEM-NH ratings and those of depression are in
favor of the APADEM-NH’s capacity to measure
apathy independent of the possible interference by
depressive symptoms present in some patients.
Severity of apathy correlates with severity of
dementia in many studies14,43 and our results confirmed that assumption. The APADEM-NH total score
increased significantly with dementia severity and
discriminated between patients grouped by GDS and
CDR levels.
The SEM, an index of precision, represents the
minimal detectable change and remains relatively
constant across samples. In this study, the APADEMNH domains and the total score showed SEM values
lower than one-half of SD of the respective subscale
scores, which is a putative criterion indicative of
adequate precision.44
The APADEM-NH scale can help apply Robert
et al.’s new Criteria for Apathy in clinical practice.2,45
In fact, the three Apathy dimensions of the
APADEM-NH scale correspond well with the three
domains that are part of Criterion B of Robert’s
Diagnostic Criteria (APADEM-NH’s “Deficit of
Thinking and Self Generated Behaviors” with Robert’s Criterion “Behavior”, “Emotional Blunting”
with Robert’s Criterion “Emotions,” and “Cognitive
Inertia” with Robert’s Criterion “Cognition”). In
addition, Robert’s criteria differentiate between selfinitiated and environment-stimulated behaviors,
and cognitions and emotions. Both are part of the
Am J Geriatr Psychiatry 23:2, February 2015
three Criteria B of the diagnostic criteria set. Spontaneous presence versus environmental stimulation is
in the core of the APADEM-NH scale as it is the basis
of the scoring system and complies with the new
Apathy Diagnostic Criteria.
Some limitations of the study must be considered.
First, the composition of our sample comprised
a majority of women. Although a more sex-equal
sample might have been more desirable, our study
composition reflects the reality of most nursing
homes with patients in advanced stages of dementia
and our population is consistent with other studies8
also conducted in nursing homes. This being stated,
there was no scale item that reflects a sex-oriented
activity or emotion, thus minimizing the impact of
sex in the scale results. Nevertheless, due to the
particular composition of the sample, no assertion
can be done with respect to sex differences in the
apathy measurements of the scale or apathy itself.
Second, not all items of the scale could be
completed for all patients in the sample. As explained
before, in the most advanced stages of dementia,
some activities or emotions cannot be scored due to
mobility reduction, aphasia, or sensory deficits. The
scale items related to these situations were reduced to
a minimum in the design phase, but some of those
participants susceptible to influence of the mentioned
factors are unavoidable and remain. Finally, a validation and comparative analysis by diagnostic
subgroups would be very interesting and has been
planned for future studies.
In conclusion, the APADEM-NH psychometric
attributes are satisfactory, allowing the assessment of
the fundamental apathy dimensions in a rapid,
comprehensive, reliable, and valid way. Nursing
home assessment of apathy is crucial for care planning. The APADEM-NH not only offers a general
measurement of the symptom through all severity
degrees but also adds separate measurement of its
three dimensions. This can certainly help to personalize treatment plans and design better-tailored
specialized care. Recent data suggest that apathy
dimensions evolve differently as dementia progresses46 and treatment response may be different for
each dimension.47
Further steps in the development of the scale will
include the calculation of clinically meaningful cutoff
points and the study of its capacity to measure
change after therapeutic interventions. A thorough
157
Validation of the APADEM-NH Apathy Scale
and systematic measurement of apathy in institutionalized persons with dementia should help to gain
insight into the origins of apathy, improve the quality
of care for patients with dementia, and spur research
on this frequently forgotten syndrome.
The authors would like to thank Megan Cummings
and Tyler Gumb from the NYU Langone Medical Center
for their help in revising the English version of the
manuscript.
The authors declare no conflict of interest. All work
was performed as one of the research projects of the regular
research programs of the Alzheimer Disease Research
Unit, CIEN Foundation, with public funding of the Carlos
III Institute of Health, Madrid, Spain, which provided all
material and professional resources.
References
1. Levy R, Dubois B: Apathy and the functional anatomy of the
prefrontal cortex-basal ganglia circuits. Cereb Cortex 2006; 16:
916e928
2. Robert P, Onyike CU, Leentjens AF, et al: Proposed diagnostic
criteria for apathy in Alzheimer’s disease and other neuropsychiatric disorders. Eur Psychiatry 2009; 24:98e104
3. Landes AM, Sperry SD, Strauss ME: Apathy in Alzheimer’s disease.
J Am Geriatr Soc 2001; 49:1700e1707
4. Zuidema S, Koopmans R, Verhey F: Prevalence and predictors of
neuropsychiatric symptoms in cognitively impaired nursing
home patients. J Geriatr Psychiatry Neurol 2007; 20:41e49
5. Garcia-Alberca JM, Pablo Lara J, Gonzalez-Baron S, et al: [Prevalence and comorbidity of neuropsychiatric symptoms in Alzheimer’s disease]. Actas Esp Psiquiatr 2008; 36:265e270
6. Onyike CU, Sheppard JM, Tschanz JT, et al: Epidemiology of
apathy in older adults: the Cache County Study. Am J Geriatr
Psychiatry 2007; 15:365e375
7. Cummings JL, Mega M, Gray K, et al: The Neuropsychiatric
Inventory: comprehensive assessment of psychopathology in
dementia. Neurology 1994; 44:2308e2314
8. Wetzels RB, Zuidema SU, de Jonghe JF, et al: Course of neuropsychiatric symptoms in residents with dementia in nursing homes
over a 2-year period. Am J Geriatr Psychiatry 2010; 18:1054e1065
9. Tun SM, Murman DL, Long HL, et al: Predictive validity of
neuropsychiatric subgroups on nursing home placement and
survival in patients with Alzheimer disease. Am J Geriatr Psychiatry 2007; 15:314e327
10. Berman K, Brodaty H, Withall A, et al: Pharmacologic treatment
of apathy in dementia. Am J Geriatr Psychiatry 2012; 20:104e122
11. Brodaty H, Burns K: Nonpharmacological management of apathy
in dementia: a systematic review. Am J Geriatr Psychiatry 2012;
20:549e564
12. Marin RS: Differential diagnosis and classification of apathy. Am J
Psychiatry 1990; 147:22e30
13. Starkstein SE, Ingram L, Garau ML, et al: On the overlap between
apathy and depression in dementia. J Neurol Neurosurg Psychiatry 2005; 76:1070e1074
14. Marin RS, Biedrzycki RC, Firinciogullari S: Reliability and validity
of the Apathy Evaluation Scale. Psychiatry Res 1991; 38:143e162
15. Lueken U, Seidl U, Volker L, et al: Development of a short version of
the Apathy Evaluation Scale specifically adapted for demented
nursing home residents. Am J Geriatr Psychiatry 2007; 15:376e385
16. Starkstein SE, Mayberg HS, Preziosi TJ, et al: Reliability, validity,
and clinical correlates of apathy in Parkinson’s disease.
J Neuropsychiatry Clin Neurosci 1992; 4:134e139
17. Robert PH, Clairet S, Benoit M, et al: The apathy inventory:
assessment of apathy and awareness in Alzheimer’s disease, Parkinson’s disease and mild cognitive impairment. Int J Geriatr
Psychiatry 2002; 17:1099e1105
158
18. Strauss ME, Sperry SD: An informant-based assessment of apathy
in Alzheimer disease. Neuropsychiatry Neuropsychol Behav
Neurol 2002; 15:176e183
19. Sockeel P, Dujardin K, Devos D, et al: The Lille apathy rating scale
(LARS), a new instrument for detecting and quantifying apathy:
validation in Parkinson’s disease. J Neurol Neurosurg Psychiatry
2006; 77:579e584
20. American Psychiatric Association: DSM-IV-TR: Breviario: Criterios
diagnósticos. Barcelona, Masson, 2003
21. Agüera-Ortiz L, Gil-Ruiz N, Cruz-Orduña I, et al: Creación de una
escala de medición de la apatía en pacientes con demencia tipo
Alzheimer institucionalizados: la escala APADEM-NH-66. Psicogeriatría 2010; 4:207e219
22. Agüera-Ortiz L, Cruz-Orduña I, Ramos-García M, et al: Proceso de
creación de la escala APADEM-NH para la medición de la apatía
en pacientes con demencia institucionalizados. Psicogeriatría
2011; 3:29e36
23. Reisberg B, Ferris SH, de Leon MJ, et al: The Global Deterioration
Scale for assessment of primary degenerative dementia. Am J
Psychiatry 1982; 139:1136e1139
24. Morris JC: The Clinical Dementia Rating (CDR): current version
and scoring rules. Neurology 1993; 43:2412e2414
25. Boada M, Tarraga L, Modinos G, et al: [Neuropsychiatric
Inventory-Nursing Home version (NPI-NH): Spanish validation].
Neurologia 2005; 20:665e673
26. Alexopoulus G, Abrams R, Young R, et al: Cornell scale for
depression in dementia. Biol Psychiatry 1988:271e284
27. Pujol J, De Azpiazu P, Salamero M, et al: [Depressive symptoms in
dementia. The Cornell scale: validation of the Spanish version].
Rev Neurol 2001; 33:397e398
28. Marinus J, Visser M, van Hilten JJ, et al: Assessment of sleep and
sleepiness in Parkinson disease. Sleep 2003; 26:1049e1054
29. van der Linden FA, Kragt JJ, Klein M, et al: Psychometric evaluation of the multiple sclerosis impact scale (MSIS-29) for proxy
use. J Neurol Neurosurg Psychiatry 2005; 76:1677e1681
30. Martinez-Martin P, Rodriguez-Blazquez C, Abe K, et al: International
study on the psychometric attributes of the non-motor symptoms
scale in Parkinson disease. Neurology 2009; 73:1584e1591
31. McHorney CA, Tarlov AR: Individual-patient monitoring in clinical practice: are available health status surveys adequate? Qual
Life Res 1995; 4:293e307
32. Hays RD, Anderson R, Revicki D: Psychometric considerations in
evaluating health-related quality of life measures. Qual Life Res
1993; 2:441e449
33. Scientific Advisory Committee of the Medical Outcomes Trust:
Assessing health status and quality-of-life instruments: attributes
and review criteria. Qual Life Res 2002; 11:193e205
34. Ware JE Jr, Gandek B: Methods for testing data quality, scaling
assumptions, and reliability: the IQOLA Project approach.
Am J Geriatr Psychiatry 23:2, February 2015
Agüera-Ortiz et al.
International Quality of Life Assessment. J Clin Epidemiol 1998;
51:945e952
35. Eisen M, Ware JE Jr, Donald CA, et al: Measuring components of
children’s health status. Med Care 1979; 17:902e921
36. Chassany O, Sagnier P, Marquis P, et al: Patient-reported outcomes:
the example of health-related quality of life a European guidance
document for the improved integration of health-related quality of life
assessment in the drug regulatory process. Drug Inf J 2002:209e238
37. Terwee CB, Bot SD, de Boer MR, et al: Quality criteria were
proposed for measurement properties of health status questionnaires. J Clin Epidemiol 2007; 60:34e42
38. Juniper EF, Guyatt GH, Jaeschke R: How to develop and validate
a new quality of life instrument. In: Spilker B, ed. Quality of Life and
Pharmacoeconomics in Clinical Trials, 2nd ed. Philadelphia, PA:
Lippincott-Raven Publishers, 1996:49e56
39. Hobart J, Lamping D, Fitzpatrick R, et al: The Multiple Sclerosis
Impact Scale (MSIS-29): a new patient-based outcome measure.
Brain 2001; 124:962e973
40. Yeager CA, Hyer L: Apathy in dementia: relations with depression, functional competence, and quality of life. Psychol Rep
2008; 102:718e722
Am J Geriatr Psychiatry 23:2, February 2015
41. Clarke DE, Ko JY, Kuhl EA, et al: Are the available apathy
measures reliable and valid? A review of the psychometric
evidence. J Psychosom Res 2011; 70:73e97
42. Levy ML, Cummings JL, Fairbanks LA, et al: Apathy is not
depression. J Neuropsychiatry Clin Neurosci 1998; 10:314e319
43. Lyketsos CG, Lopez O, Jones B, et al: Prevalence of neuropsychiatric symptoms in dementia and mild cognitive impairment:
results from the cardiovascular health study. JAMA 2002; 288:
1475e1483
44. Norman GR, Sloan JA, Wyrwich KW: Interpretation of changes in
health-related quality of life: the remarkable universality of half
a standard deviation. Med Care 2003; 41:582e592
45. Mulin E, Leone E, Dujardin K, et al: Diagnostic criteria for apathy
in clinical practice. Int J Geriatr Psychiatry 2011; 26:158e165
46. Agüera-Ortiz L, Cruz-Orduna I, Ramos García I, et al: Apathy
dimensions evolve diffferently with levels of dementia severity.
Alzheimers Dement 2012; 8:622
47. Leone E, Deudon A, Bauchet M, et al: Management of apathy
in nursing homes using a teaching program for care staff:
the STIM-EHPAD study. Int J Geriatr Psychiatry 2013; 28:
383e392
159