INTERNATIONAL JOURNAL OF GERIATRIC PSYCHIATRY

Int. J. Geriat. Psychiatry 14, 10191030 (1999)

DECREASED AWARENESS OF COGNITIVE

DEFICITS IN PATIENTS WITH MILD
DEMENTIA OF THE ALZHEIMER TYPE
CHRISTIAN DEROUESNE 1*, STEPHANIE THIBAULT 1, SAMIRA LAGHA-PIERUCCI 1, VERONIQUE BAUDOUIN-MADEC 1,
1

DANIEL ANCRI 2 AND LUCETTE LACOMBLEZ 3

Department of Neurology, Groupe Hospitalier Pitie-Salpetriere, Paris, France

2
Department of Nuclear Medicine, Groupe Hospitalier Pitie-Salpetriere, Paris, France
3Department of Neurology and Department of Pharmacology, Groupe Hospitalier Pitie-Salpetriere, Paris, France

ABSTRACT
Objective. To study the unawareness of cognitive decits in patients with mild dementia of Alzheimer type (DAT).
Design. Retrospective study. We surveyed the medical records of outpatients meeting the NINCDSADRDA
criteria for probable DAT who were able to complete the Cognitive Diculties Scale (CDS) and had a close informant
relative (IR) who could complete the family form of the same questionnaire.
Setting. A department of neurology in a general teaching hospital.
Subjects. Eighty-eight patients, aged 73.2+8.6 years with a mean MMSE score of 22.5+3.2. Fifty-two of the
88 patients had a follow-up examination after a mean interval of 21 months.
Methods. Awareness of cognitive decits was mainly assessed as the dierence between the scores on the CDS
completed by the IR and the patient (Index of Unawareness, IU). Two secondary assessments of unawareness were
performed: (1) an assessment by the clinician on the basis of the patient's answers to questions probing the awareness
of memory decits; (2) an evaluation by the IR of the frequency of behavioural manifestations of unawareness in
everyday life. SPECT was performed in 78 patients to study the relationship between unawareness and the topography
of perfusion decits.
Results. Awareness of the cognitive decits varied greatly between patients, according to the assessment method
used and the stage of progression of the disease. Most patients with mild DAT were cognitively aware of their
cognitive decits but failed to appraise their severity and their consequences in everyday life. Decreased awareness was
positively correlated with age and perfusion decits in the frontal regions and negatively with the anxious
symptomatology. However, the main correlate of unawareness was apathy.
Conclusion. The nature of unawareness of cognitive decits appeared to be more dimensional than categorical. In
patients with mild dementia, decreased awareness appeared to be more related to aective disturbances, especially to
emotional decit or apathy, than to cognitive decits. Copyright # 1999 John Wiley & Sons, Ltd.
KEY WORDS Alzheimer's

disease; unawareness; anosognosia; apathy; aective disturbances

Over the past few years, there has been a growing

interest in unawareness of cognitive decits in
patients with Alzheimer's disease (Mullen et al.,
1996; Starkstein et al., 1996; Agnew and Morris,
1998). However, conicting results have been
obtained regarding both the frequency of unawareness in these patients and its relationship with the
severity of cognitive decits, depression or frontal
*Correspondence to: Professor C. Derouesne, Department of
Neurology, Hopital de la Salpetriere, 47 Boulevard de l'Hopital,
75651 Paris Cedex 13, France. Tel: (33) 01 42 16 18 12. Fax: (33)
01 44 24 52 46. Email: cherou@cybercable.fr
CCC 08856230/99/12101912$17.50
Copyright # 1999 John Wiley & Sons, Ltd.

lobe dysfunction. The divergent ndings may be

due to the dierences between the size of the
samples and their heterogeneity and inclusion of
patients with dementia of varying severity
(Anderson and Tranel, 1989; DeBettignies et al.,
1990; Verhey et al., 1993). The lack of standardized
assessment procedures to evaluate the impaired
awareness of cognitive decits (McGlynn and
Schacter, 1989; Markova and Berrios, 1992;
Migliorelli et al., 1995) is a further source of
confusion.
Unawareness of cognitive decits in patients
with mild dementia of Alzheimer type (DAT) may
Received 1 February 1999
Accepted 24 May 1999

1020

C. DEROUESNE, S. THIBAULT, S. LAGHA-PIERUCCI ET AL.

result in delaying diagnosis, a failure to initiate

therapy and conict with the caregivers. The aim of
the present study was to explore the unawareness of
cognitive decits in patients with mild DAT and to
assess its relationships with cognitive and aective
status and topography of cerebral perfusion
decits.
SUBJECTS AND METHODS
We reviewed the medical les of consecutive
demented outpatients examined in a neurological
department at a university teaching hospital
between 1990 and 1992. Patients were included in
the study if (1) they met the NINCDSADRDA
criteria for probable DAT (McKhann et al. 1984);
(2) they had mild dementia dened by an MMSE
score 5 18 and the capacity to complete autoquestionnaires; and (3) they had a close informant
relative (IR), usually a spouse, who was able to
complete questionnaires.
Diagnosis was supported by (a) an extensive
neuropsychological examination including the
Coloured Progressive Matrices (Raven, 1965),
the Wechsler Memory Scale (Wechsler, 1955), the
WAIS similarities (Wechsler, 1972), the Boston
Diagnostic Aphasia Examination (Goodglass and
Kaplan, 1972) a verbal categorical uency test, a
standardized praxis examination and research of
behavioural signs of frontal lobe dysfunction
including impulsivity, perseverations (Luria,
1966), utilization and imitation behaviours
(Lhermitte et al., 1986); (b) CT scan or magnetic
resonance imaging ndings; and (c) blood tests to
rule out other diagnoses.
Assessment of unawareness
Unawareness of cognitive decits was assessed
mainly by the comparison of ratings from the
patient and from the caregiver on the French
version of the Cognitive Diculties Scale (CDS)
(McNair and Kahn, 1983; Derouesne et al., 1993).
This scale is a 37-item self-rated questionnaire
which requires subjects to indicate on a 5-point
scale ( from 0 never to 4 most of the time)
how often they experience particular diculties in
everyday life (eg `do you nd it dicult to
remember usual phone numbers?'). The IRs
completed the family form of the CDS, which
includes questions identical to the questions on the
self-rating CDS but worded in such a way as to
Copyright # 1999 John Wiley & Sons, Ltd.

refer to the patient's cognitive abilities (Derouesne

et al., 1995). We dened as the Index of Unawareness (IU) the dierence between CDS ratings by the
IR and by the patient according to the formula:
IU IR's CDS score patient's CDS score, such
that the greater the positive score, the more severe
the unawareness.
Two secondary assessments of unawareness were
performed: (1) an overall clinical assessment was
made by the investigator after a few questions (such
as `What are the problems you are here for?' `How
good do you estimate your memory to be?'), using
a three-point scale: no anosognosia, mild anosognosia, severe anosognosia (Reed et al., 1993;
Sevush and Leve, 1993; Lopex et al., 1994).
Patients were considered as being aware of their
memory decits if they gave memory disturbances
as the motive in taking medical advice, mildly
unaware if they did not but eventually admitted
decline when questioned about their memory, and
severely unaware if they denied any memory decit
(Anderson and Tranel, 1989); (2) an evaluation of
the behavioural aspects of unawareness in everyday
life using three questions from a Psychobehavioural Questionnaire (PBQ), a 44-item questionnaire
derived from the BEHAVE-AD (Reisberg et al.,
1987) and the Depressive Mood Scale (Jouvent
et al., 1988). This questionnaire was rated by the IR
assessing the frequency of the patient's behaviour
and mood disturbances on a seven-point scale
( from 0 never to 6 most of the time). Three
questions on this questionnaire were specically
designed to assess the frequency of behavioural
aspects of unawareness: `Does it happen that he
(she) denies being ill?' `Do you nd him (her) being
abnormally optimistic about his (her) decits?'
`Does he (she) hide his (her) diculties behind a
joking, facetious mood?'. An Index of Behavioural
Aspects of Unawareness (IBAU) was calculated by
summing the scores on these three questions (score
from 0, no unawareness, to 18, permanent unawareness).
The severity of the disease was assessed by the
score on the Mini-Mental State Examination
(MMSE) (Folstein et al., 1975), the duration of
the disease and the score on the Activities of Daily
Living-scale (ADL) completed by the IR. This
ADL scale is derived from the Physical SelfMaintenance Scale and the Instrumental Activities
of Daily Living scale (Lawton and Brody, 1969)
and from the ADL scale of Katz and Lyerly (1963)
for social activities (score from 21 normal
activities to 84 total loss of autonomy).
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

1021

UNAWARENESS AND ALZHEIMER'S DISEASE

Aective status was assessed: (1) by the IR using

the PBQ. A principal component analysis of this
scale showed four factors: apathy (including eight
items: withdrawal into oneself, indierence to
surroundings, decreased everyday life activities,
slowing in everyday life activities, anhedonia,
indierence to usual incentives and to sexual
interests, and decreased emotional expressivity),
emotional incontinence (bursts or crying, anxiety,
hypersensitivity to emotional stimuli, changes of
mood, sadness), irritability (bursts of anger,
aggressiveness, impulsivity) and psychosis (hallucinations, delusions); (2) by the patient him(her)self,
using the Zung Self-Rating Scales for Depression
(ZD) and Anxiety (ZA) (Zung, 1965, 1971).
Single photon emission computed
tomography, SPECT
SPECT examination was included in this study if
it was performed within the 30 days following the
clinical examination. SPECT was performed using
123
I N-isopropyl-p-iodoamphetamine (IMP) as a
tracer. Tomographic acquisition was performed
30 minutes after injection of a 34 mCi bolus of
IMP while the patient was in the supine position
with eyes closed and ears unplugged. Imaging was
carried out with a gamma rotating camera (General Electric 400 TxlC), provided with a collimator
of medium energy; 3608 data were collected,
recording 64 views of 25 seconds each, on a
128  128 matrix. On each slice ( pixel size 3 mm),
12 regions of interest were positioned in frontal,
temporal and parietal regions. For each region, the
relative tracer activity in the slice was measured as
the number of counts per pixel and is expressed as a
proportion of the activity in the slice as a whole and
compared to those of a normal control population.
The results were considered as abnormal when the
dierence between patients and controls was
greater than two standard deviations. They were
summed and expressed according to three overall
regions of interest ( frontal, parietotemporal and
frontotemporoparietal) and hemispheric perfusion
decits ( predominant in the right or the left
hemisphere, or without asymmetry).
Follow-up
Patients were included in the follow-up study if
their medical records contained at least a second
examination with the CDS lled in by the patient
and the same IR as at the rst examination.
Copyright # 1999 John Wiley & Sons, Ltd.

Statistical analysis
Comparisons between qualitative and quantitative variables were performed with bilateral
unpaired t-test (or paired t-test for repeated
measures in the follow-up study) and ANOVA.
Quantitative variables were compared using Pearson's correlation coecient and simple or multiple
regression (backward stepwise analysis). When
there was doubt concerning the normality of the
distribution, parametric and non-parametric tests
were performed (Mann-Whitney, Wilcoxon, Kruskall Wallis and Spearman rank correlation). When
no discrepancies were found between the two
methods, the results of parametric tests are
presented for simplicity. For comparison of
qualitative variables, contingency tables and
Fisher's exact test were performed (Statview15.0).
The level of statistical signicance was p 0.05.
RESULTS
Sample characteristics
Eighty-eight patients were included in the study,
36 men (41%) and 52 women (59%). The mean age
of the patients was 73.2+8.6 years (range
5187 years). The educational level was low
(5 years or fewer) in 39 patients (44%), medium
(611 years) in 27 (31%) and high (12 years or
more) in 22 (25%). The mean duration of the
disease was 2.9+1.8 years (range 18 years).
Twenty of the patients (23%) had an early onset
(65 years old and younger) and 68 (77%) a late
onset disease. The results of the cognitive and
aective assessments are shown in Table 1.
Unawareness of cognitive decits
Index of unawareness. The mean CDS score
was 60.7+22.6 (range 7114) according to the
patients and 76.9+22.5 (range 13136) according
to the IRs (t87 5.6; p 0.0001). The mean IU
was 16.2+26.9 (range 70 to 87). The distribution of the IU was close to a normal distribution
(Fig. 1). The IU was negative in 23% of the
patients, ie the patients reported more diculties
than the IRs, but the dierence was only signicant
(IU 5 10) for 10 patients (11%). The most
frequent and the rarest types of complaints are
shown in Table 2.
Secondary assessments of unawareness. Sixtyeight patients (77%) complained of a memory
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

1022

C. DEROUESNE, S. THIBAULT, S. LAGHA-PIERUCCI ET AL.

Table 1. Cognitive and aective assessments in the crosssectional study and in the follow-up study. ADL,
Activities of Daily Living; PBQ, Psychobehavioural
Questionnaire; ZD and ZA, Zung's Depression and
Anxiety Self-Rating scales; Em decit, emotional decit;
IU, Index of Unawareness; IBAU, Index of Behavioural
Aspects of Unawareness. Mean+SD (range)
Cross-sectional
study
N 88
MMSE
CDS P
CDS IR
IU
IBAU
ADL
PBQ
Em decit
ZD
ZA

22.5+3.2
(18, 27)
60.7+22.6
(7, 114)
76.9+22.5
(13, 136)
16.1+26.9
(70, 87)
4.0+3.9
(0, 18)
31.7+13.3
(959)
70.4+41.3
(4, 201)
20.3+12.7
(0, 32)
50.1+8.7
(29, 71)
41.0+7.2
(29, 61)

Follow-up study
N 52
1st exam.
2nd exam.
22.9+3.5
(18, 27)
61.0+20.1
(19, 111)
79.4+23.1
(22, 136)
18.3+27.6
(50, 87)
4.0+3.4
(014)
(31.8+13.5)
(9, 58)
(68.4+38.9)
(4, 201)
19.4+12.2
(0, 32)
48.2+9.6
(29, 64)
44.4+7.8
(29, 61)

21.0+3.5**
(16, 27)
61.0+19.1 NS
(25, 110)
89.7+25.3***
(30, 143)
30.3+28.3***
(30, 96)
5.0+4.5*
(017)
41.5+12.2***
(21, 67)
84.3+49.5**
(4, 202)
23.8+14.2***
(0, 33)
47.6+9.6 NS
(29, 68)
40.9+9.1*
(26, 65)

* p 5 0.5; ** p 5 0.01; *** p 5 0.001; statistical signicance of

the dierence between the rst and the second, follow-up,
examination.

decit as the presenting symptom. The other

20 patients (23%) had a dierent presenting
symptom but they admitted suering memory
decits when specically asked about the functioning of their memory (mild anosognosia). None of
the patients explicitly denied his (her) memory
disturbances (severe anosognosia).
Denial of illness was reported `often or most of
the time' by 27% of the IRs, `sometimes' by 33%
and `never' by 40%. However, the mean IBAU was
low, 4.0+3.9 (range 018).
Relationships between the various assessments of
unawareness. The IU did not dier between the
patients with mild anosognosia and those without
(16.3+31.8 vs 16.1+25.5; t86 0.03; p 0.98).
The IU was moderately correlated with the IBAU
(r 0.33; p 0.002).
Copyright # 1999 John Wiley & Sons, Ltd.

Fig. 1. Distribution of the Index of Unawareness at the rst

(IU 1st) and second, follow-up, examination (IU 2nd)

For simplicity and to reduce the amount of

statistical comparison, only the IU is considered in
the subsequent analysis.
Unawareness and general characteristics of
the patients
The IU was not related to sex (males m 18.9+
27.3; females m 14.2+26.7; t86 0.8; p 0.42)
or educational level (F(2.85) 0.36; p 0.70). IU
was weakly correlated with age (r 0.22;
p 0.04) and was higher in patients with late
onset than in those with early onset disease
(19.9+26.1 vs 4.4+26.9; t86 2.3; p 0.02).
Unawareness and severity of the disease
No correlation was found between IU and
disease duration (rho 0.10; p 0.50). IU was
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

UNAWARENESS AND ALZHEIMER'S DISEASE

weakly correlated with the MMSE score

(rho 0.21; p 0.05) and the ADL score
(rho 0.27; p 0.01).
Unawareness and cognitive status
There was no relationship between IU and scores
on the Raven's Progressive Matrices, the Wechsler
Memory Scale, verbal uency, or the WAIS
similarities (correlation between IU and all of
these measures: r 5 0.10; p 4 0.50).
Patients with mild anosognosia had more
frequent clinical signs of frontal lobe dysfunction
than patients without (32% vs 16%; Fisher's exact
test, p 0.05). However, no statistically signicant
dierence in IU was observed between the patients
who presented one or more behavioural signs of
frontal lobe dysfunction and those who did not
(17.6+27.9 vs 13.7+27.7; t86 0.6; p 0.55).
Unawareness and aective status
A backward stepwise analysis was performed
with IU as the dependent variable and age, scores
on the MMSE, ADL, ZD and ZA, overall PBQ
score and each of the four PBQ factor scores
as covariates. Three independent variables
explained 38% of the variance (F(9.53) 2.8;
p 0.009): the PBQ subscore of emotional decit
(standard coecient 0.35), the ZA score (standard coecient 0.30) and age (standard
coecient 0.24).
Unawareness and cerebral regional perfusion decits
SPECT was available for 78 patients. These
patients did not dier from those for whom no
SPECT imaging data were available regarding age,
sex, educational level and severity of the disease or
aective status.
In seven cases, no cerebral perfusion decit was
found. In 27 patients (38%) the perfusion decit
was predominant in the parietotemporal regions, in
22 (31%) in the frontal regions and in 22 (31%) it
was equally distributed in the frontotemporoparietal regions. The decit was predominant in
the left hemisphere in 29 patients (41%), in the
right hemisphere in 17 (24%) and no interhemispheric asymmetry was found in 25 patients (35%).
IU was signicantly lower in patients with a pure
temporoparietal decit than in patients with a
predominant frontal lobe decit or with a frontotemporoparietal decit (respectively 6.0+29.4,
17.2+33.0 and 25.5+23.3; F(2.68) 3.6;
Copyright # 1999 John Wiley & Sons, Ltd.

1023

p 0.03). IU tended to be higher in the patients

with a predominant right hemisphere decit
(25.6+27.2) than in those with a predominant
left hemisphere decit (12.1+28.0) and in those
with no interhemispheric asymmetry (12.6), but the
dierences were not statistically signicant
(F(2.68) 1.7; p 0.20).
Follow-up
For 52 of the 88 patients, the medical records
available contained at least one follow-up examination after a mean interval of 20.9+15.9 months
(range 373 months). This group of patients did not
dier signicantly from the 36 who did not meet the
criteria for the follow-up study as concerns general
characteristics, disease duration and severity of
cognitive decits at the rst examination. Only 41 of
the 52 patients completed the ZD and ZA scales at
the second examination. All clinical parameters
showed a progression of the disease since the rst
assessment (Table 1). The ZD and ZA scores were
lower than at the rst examination but the
emotional decit score was signicantly higher
(24+14 vs 19+12; t39 3.5; p 0.001).
Index of unawareness. The mean U was signicantly higher at the second examination than at the
rst (30.3+29.3 vs 16.1+20.9; t51 4.1;
p 0.0001) but the IU had decreased by 10 points
or more in four patients (8%). These four patients
had a signicantly higher IU than the other
patients at the rst examination (IU1 51.8+
29.4 vs IU2 15.5+25.8; t51 2.7; p 0.01). The
distribution of the IU remained about normal.
The most frequent and rarest types of complaints
at the second evaluation are shown in Table 3. The
agreement between the patients and IRs for the
items scored as the most frequent and the rarest
was not as good as at the rst examination.
Unawareness and general characteristics. As at
the rst examination, there were no relationships
between IU and sex or educational level. The IU
remained correlated with age (r 0.32; p 0.02)
and was higher in patients with late onset disease
than in those with early onset disease (34.7+27.2
vs 15.8+28.3; t50 2.11; p 0.04).
Unawareness and severity of the disease. The IU
was not correlated with the MMSE score
(rho 0.2; p 0.16) but remained correlated
with the ADL score (rho 0.37; p 0.008) at the
second examination.
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

1024

C. DEROUESNE, S. THIBAULT, S. LAGHA-PIERUCCI ET AL.

Table 2. The most frequent and the rarest complaints

reported by the patients and the informant relatives
(IRs) at the rst examination. The brackets indicate
items classied as the rarest complaints by the patients
and not by the IRs, or vice versa
Items

Frequency
Patients
IRs
N 88 N 88

Most frequent types of complaints

(% of items rated 4 very often)
Need for a written list when doing errands
Diculty in nding where things have
been put down
Diculty in retrieving usual phone
numbers
Forgetting the day of the month
Rarest types of complaints
(% of items rated 0 never)
Diculty in putting a key into a lock
Diculty in manipulating buttons or zips
Forgetting to button or zip clothing
Forgetting to pay bills, record
cheques, . . .
Diculty in sewing, mending, making
more repairs

31
19

56
53

18

50

17

34

79
70
59
58

51
71
54
(29)

(48)

32

Unawareness and aective status. A backward

stepwise analysis was performed with the IU as the
dependent variable and age, MMS, ADL, overall
PBQ score and each of the four PBQ factor scores
as covariates. The only predictor of the IU was the
subscore of emotional decit, explaining 48% of
the variance (F(1.46) 31.4; p 0.0001).
DISCUSSION
Our patients had early dementia but they met the
NINCDSADRDA for probable Alzheimer's
disease and neuropsychological examination and
follow-up indicates that they were clearly distinct
from elderly people with only age-related cognitive
changes.
The issue of assessment of anosognosia
In the literature, unawareness of decits has been
assessed by three main methods: (1) The patient
carer discrepancy judgements on questionnaires
assessing cognitive disturbances or activity in
everyday life. We used this method to dene an
Index of Unawareness, IU, as the patientrater
Copyright # 1999 John Wiley & Sons, Ltd.

Table 3. The most frequent and the rarest complaints

reported by the patients and the informant relatives
(IRs) at the second examination. The brackets indicate
items classied as the most frequent complaints (or the
rarest complaints) by the patients and not by the IRs, or
vice versa
Items

Frequency
Patients
IRs
N 52 N 52

Most frequent types of complaints

(% of items rated 4-very often)
Need for a written list when doing errands
Forgetting the day of the month
Forgetting the day of the week
Diculty in retrieving usual phone
numbers
Diculty in nding where things have
been put down
Forgetting appointments, dates, meetings
Rarest types of complaints
(% of items rated 0 never)
Diculty in manipulating buttons or zips
Forgetting the names of people after
being introduced
Diculty in putting a key into a lock
Forgetting to button or zip clothing
Forgetting to pay bills, record
cheques, . . .
Diculty in manipulating tools, scissors,
corkscrew, . . .

23
21
18
(14)

64
(46)
(45)
63

16

57

(4)

57

70
63

48
(9)

57
52
52

48
39
(23)

(48)

25

discrepancy on the scores on the Cognitive

Diculties Scale (McNair and Kahn, 1983).
Using the IU, some degree of unawareness of
cognitive decits was found in 76% of patients.
This percentage is close to that found by Reed et al.
(1993) (81%) but below that (93%) reported in the
study of Verhey et al. (1993). One interesting result
of our study is the normal distribution of the IU,
showing: (a) the great variability of unawareness
among the patients, resulting in a large SD; (b) that
it is dicult to draw a clear distinction between
anosognosic and non-anosognosic patients, therefore the dimensional (quantitative) more than the
categorical nature of unawareness. This method
has been criticized because it has been shown that
patients tend to under-report memory disturbances
compared to normal subjects (Ballard et al., 1991;
Feehan et al., 1991); on the other hand, the
caregiver's perception of the level of patient's
functioning was shown to be dependent on the
level of the caregiver's burden and depression more
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

UNAWARENESS AND ALZHEIMER'S DISEASE

than on the severity of the disease and could

underestimate
the
patient's
performance
(DeBettignies et al., 1990; Mangone et al., 1991).
However, in our study, the patients had higher
scores on the CDS than non-demented elderly
subjects examined in a previous study (mean score
60.1+23.1 vs 45.5+21.4; t90 6.19; p 0.0001)
(Derouesne et al., 1993), results in agreement with
other studies (DeBettignies et al., 1990; Ballard
et al., 1991; Reed et al., 1993). Negative IU scores
were linked to anxious symptomatology in the
patient but also to underestimation of patients'
disturbances by some caregivers. (2) The inability
to correctly report a memory decit following
direct questioning as rated by the experimenter
(Lopez et al., 1994). In that way, we rated unawareness according to the nature of the presenting
symptom and the global assessment by the patient
of the functioning of his memory. We found 23%
of patients with mild unawareness, a result close to
that of Migliorelli et al. (1995), but no patient with
severe unawareness, contrary to the results of Reed
et al. (1993) and Verhey et al. (1993), who found
respectively 28% and 18% of severe anosognosia.
The absence of severe anosognosia in our study is
in agreement with the low scores of unawareness using the two other methods and can be
explained by the inclusion criteria, which limited
the study to patients with mild dementia. (3) The
presence of impaired judgement of performance on
memory tests (Pappas et al., 1992) was not assessed
in the present study, but (4) we used a third
additional assessment method, based on the rating
by the caregiver of behavioural manifestations of
unawareness in everyday life. The presence
of unawareness behaviour was noted in 75% of
patients but the mean Behavioural Index of
Unawareness, BIU, was low, indicating that
unawareness behaviour was only occasional in the
great majority of the patients.
The comparison of the results from the three
assessment methods showed that: (1) the presence
and severity of unawareness diered according to
the assessment method; (2) there was no close
relationship between the results of the various
methods, which underlies the complexity of
unawareness and the need for a more specic
assessment tool for studying unawareness in
patients with AD.
However, two conclusions can be drawn from
our results: (a) there is a great between-patients
variability of unawareness; (b) in the early stage of
AD, unawareness remained moderate.
Copyright # 1999 John Wiley & Sons, Ltd.

1025

Unawareness of cognitive decits and

general characteristics
We did not nd any relationship between
unawareness and sex or educational level, consistent with the ndings of most previous studies
(DeBettignies et al., 1990; Lopez et al., 1994;
Nargeot et al., 1994; Reed et al., 1993). We found a
slight positive correlation between unawareness
and age, in contrast to the negative correlation
found by others (Migliorelli et al., 1995; Verhey
et al., 1993).
Unawareness and severity of the disease
Most studies showed a negative relationship
between unawareness of cognitive decits and
severity of the disease assessed by the MMSE
(McDaniel et al., 1995; Migliorelli et al., 1995;
Lopez et al., 1994; Starkstein et al., 1996; Sultzer
et al., 1992), but others did not (DeBettignies et al.,
1990; Feher et al., 1991; Kotler-Cope and Camp,
1995; Nargeot et al., 1994; Reed et al., 1993;
Verhey et al., 1993). In our study, there was a
negative correlation between the severity of the
unawareness at the rst examination but not at the
follow-up examination. A relationship between
unawareness and a global assessment of the
severity of the disease, such as the Global
Deterioration Scale, was found in some studies
(Feehan et al., 1991; Verhey et al., 1993; Lopez
et al., 1994) but not in others (Feher et al., 1991;
Sevush and Leve, 1993). No relationship between
unawareness of cognitive decits and disease
duration was found in our study, as in all studies
except two (Migliorelli et al., 1995; Starkstein et al.,
1996). This negative result is easily explained by the
diculty of determining the onset of the disease.
We found a relationship between unawareness and
impairment in everyday life activity, assessed by the
ADL scale, on the rst and second examination in
agreement with the study of Migliorelli et al.
(1995). At the follow-up examination, the frequency and severity of unawareness were higher
than at the rst examination, as in most studies
which show that unawareness increases with the
progression of the disease (McDaniel et al., 1995;
Reisberg et al., 1985). However, about 10% of our
patients showed a lesser degree of unawareness at
the second examination, a result similar to that
found in the CERAD study (McDaniel et al.,
1995). This result may be explained by the
phenomenon of regression towards the mean,
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

1026

C. DEROUESNE, S. THIBAULT, S. LAGHA-PIERUCCI ET AL.

because the patients who showed such a decrease of

unawareness at the second examination had very
high IU at the rst examination.
Taken globally, these results suggest that there is
a link between unawareness and the severity of the
disease, but that this link is not a direct one.
Unawareness of cognitive decits cannot be considered as the result of a general judgement decit.
The absence of a general judgement decit is also
supported by (1) the analysis of the most frequent
and rarest type of complaints in our study, which
showed that the complaints varied according to
dierent cognitive activities, and (2) the results of
studies which showed that AD patients, unaware of
their memory decit, were accurate in assessing the
memory of their relatives (Anderson and Tranel,
1989; McGlynn and Kaszniak, 1991; Vasterling
et al., 1995).
Unawareness and cognitive performance
No relationship was found between unawareness
and any of the neuropsychological test results in
our study, nor in most studies (DeBettignies et al.,
1990; Feher et al., 1991; Nargeot et al., 1994; Reed
et al., 1993; Verhey et al., 1993). However, some
studies showed a negative correlation between
unawareness and the Verbal IQ (Starkstein et al.,
1993), the Object Naming Test (Sevush and Leve,
1993), and the Buschke Selective Reminding Test
and the Token Test (Migliorelli et al., 1995;
Starkstein et al., 1996).
A direct link between unawareness and memory
decits has been suggested in some studies which
showed a relationship between unawareness and
severity of memory decits (Green et al., 1993;
Dalla Barba et al., 1995). However, severe amnesic
patients were reported to present normal awareness
of their decits (Duyckaerts et al., 1995) and no
relationship was found between unawareness and
memory performance in our study, as in most
studies (Correa et al., 1996; DeBettignies et al.,
1990; Feher et al., 1991; McGlynn and Kaszniak,
1991; Michon et al., 1994; Nargeot et al., 1994;
Reed et al., 1993; Verhey et al., 1993). Impairment
of episodic memory may be considered as a
maintenance factor in unawareness, but not as a
factor responsible for it (Agnew and Morris, 1998).
We did not nd statistically signicant dierence
in IU between the patients who presented one or
more clinical signs of frontal lobe dysfunction and
those who did not (17.6+27.9 vs 13.7+27.7;
t86 0.6; p 0.55), in contrast to various studies
Copyright # 1999 John Wiley & Sons, Ltd.

which showed a close relationship between unawareness and frontal lobe dysfunction documented by neuropsychological testing (Nargeot et al.,
1994; Mangone et al., 1991; Reed et al., 1993;
Damasio, 1994; Kotler-Cope and Camp, 1995).
This discrepancy might be explained by the lack of
sensitivity for frontal disturbances of our clinical
examination compared to neuropsychological
testing of frontal functions.
Unawareness of cognitive decits and
aective status
Numerous reports showed a close relationship
between cognitive complaints and aective symptomatology in cognitively normal and demented
people (Derouesne et al., 1989; Feher et al., 1991;
Grut et al., 1993; Jorm et al., 1994; McGlone et al.,
1990; Migliorelli et al., 1995; O'Connor et al., 1990;
Sevush and Leve, 1993). However, other studies
failed to show a relationship between unawareness
and the severity of depressive symptomatology in
AD (DeBettignies et al., 1990; Kotler-Cope and
Camp, 1995; Lopez et al., 1994; Mangone et al.,
1991; Ott et al., 1996; Starkstein et al., 1995;
Verhey et al., 1993). In our study, unawareness was
negatively correlated with anxious symptomatology but not with depressive symptomatology rated
by the patients.
One of the most interesting results of our study is
that the main correlate of unawareness was apathy.
The positive relationship with apathy and the
negative correlation with anxious symptomatology
remained at the follow-up study. Apathy is dened
as a lack of motivation associated with an
emotional decit (Marin, 1991). Emotional decit
has been found to be a major dimension of aective
disturbances in DAT patients (Bungener et al.,
1996) and is frequently mistaken for depression.
Two recent studies have stressed the relationship
between unawareness and apathy in AD (Ott et al.,
1996; Starkstein et al., 1996). This relationship may
be explained, in the early stage of the disease, by
the pathological changes in amygdaloid nuclei
found to be associated with early clinical symptoms
in DAT (Braak and Braak, 1991).
Unawareness of cognitive decits and topography of
cerebral perfusion decits
Although the most characteristic topography of
cerebral perfusion or metabolic decits in DAT is a
bilateral temporoparietal decit, some studies
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

UNAWARENESS AND ALZHEIMER'S DISEASE

report that perfusion decits are not constant in

mild DAT and have a heterogeneous topography
(Celsis et al., 1987; Haxby et al., 1990; Waldemar
et al., 1997). We, like others, found a relationship
between the severity of unawareness and frontal
cerebral perfusion decits (Reed et al., 1993;
Starkstein et al., 1995). Unawareness of cognitive
decits has also been associated with cerebral
perfusion decits in the right hemisphere in
SPECT studies (Reed et al., 1993; Sevush and
Leve, 1993; Starkstein et al., 1995). In our study,
IU was higher in patients with predominant right
hemispheric perfusion decits than in patients with
left hemispheric or bihemispheric decits, but the
dierence was not statistically signicant. The
relationship between unawareness and right hemispheric perfusion decit may be explained by the
dominant role currently attributed to the right
hemisphere in processing emotional information
(Blonder et al., 1991).
Heterogeneity of unawareness of cognitive decits
Unawareness should no longer be considered as
a single entity (Schacter, 1991; Feinberg, 1997;
Agnew and Morris, 1998). The heterogeneity of
unawareness of cognitive decits in AD is evidenced by (1) the presence of dissociation between
(a) unawareness of cognitive decits and unawareness of behavioural problems (Starkstein et al.,
1996); (b) unawareness of memory decits and of
everyday life activities or behavioural disturbances
(Green et al., 1993; Vasterling et al., 1995);
(c) unawareness for recent and distant memories
(Starkstein et al., 1995); (d) anxiety and irritability,
on the one hand, and depressive symptomatology
on the other (Correa et al., 1996); and (e) various
cognitive tasks (Dalla Barba et al., 1995; McGlynn
and Schacter, 1989) and (2) the diversity of
correlates. Numerous explanations have been proposed: lack of feedback regarding memory loss,
decit in self-monitoring (Auchus et al., 1994;
Correa et al., 1996; Grut et al., 1993; McGlone
et al., 1990; Reed et al., 1993) and diculty in
emotional anticipatory responses in frontal
patients (Damasio, 1994). Agnew and Morris
(1998) proposed the only cognitive model of
unawareness of memory decits. According to
this model, derived from the general model of
Schacter (1991), the contents of episodic and
semantic memory are continually being revised
in the light of new incoming information. A
mnemonic comparator located within the central
Copyright # 1999 John Wiley & Sons, Ltd.

1027

The study of 88 patients with early Alzheimer's disease showed that:

. Decreased awareness of cognitive decits was
present in most patients but remained of
moderate severity. However, the presence and
severity of unawareness varied according to
the assessment methods
. Unawareness should be considered according
more to a dimensional than a categorical
perspective
. The cognitive diculties rated by the patients
as the most frequent and the rarest were
similar to those rated by the caregivers and
cognitively normal elderly subjects
. The main correlate of unawareness was
apathy, suggesting that, in this stage of the
disease, decreased awareness is more related
to aective than to cognitive disturbances
executive system of the short-term memory compares the memory performance with the state of the
memory function held in a personal knowledge
base (PBK). When the comparator detects a
mismatch between the incoming information in
term of ability and the PBK, the PBK is updated
via inputs of episodic to semantic memory. Three
types of anosognosia could be distinguished: (1) in
mnemonic anosognosia, the mismatch between the
performance and the state of memory function is
perceived but not encoded in the semantic memory.
There is an immediate perception of the memory
failure but no encoding/updating of the memory
decit as a whole in the PBK. However, some
implicit knowledge of the comparator output may
result in denying a memory impairment but
avoiding certain behavioural tasks that rely on
intact memory functioning; (2) executive anosognosia is related to a decit in the comparator
functioning. The error is perceived and experienced
but there is no signal indicating failure as an
unusual event. These patients may attempt to
process the contradictory failure experience by
confabulations; (3) primary anosognosia, where
there is no awareness of an error despite a signal
from the comparator demonstrating such. The
error is perceived and experienced only through
implicit knowledge (Agnew and Morris, 1998).
This type of anosognosia results in unawareness of
other cognitive domains and of dementia as a
whole. The knowledge of a memory problem but
its underestimation by our patients suggests a
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

1028

C. DEROUESNE, S. THIBAULT, S. LAGHA-PIERUCCI ET AL.

decit in updating the PBK which might also

explain the similarity between the type of complaints in normal elderly people and in patients
with AD. The patients report the same diculties
they experienced before the onset of the disease and
which are encoded in the PBK. However, this
explanation does not t with their awareness of a
global memory dysfunction or with the decrease of
similarity between the patients' and caregivers'
ratings at the follow-up examination. Moreover,
it does not explain the main relationship with
apathy and the negative correlation with anxious
symptomatology. Babinski (1914), in his seminal
paper, described patients who were aware of their
decits but remained indierent to them. He
distinguished these patients from anosognosia
and coined the term of anosodiaphoria to describe
them, which underlined that some unawareness of
decits could be related to aective mechanisms.
Our ndings suggest that, in the early stage of
Alzheimer's disease, emotional decit related to
lesions in amygdaloid nuclei may play a major role
in the decreased awareness of cognitive decits by
the patients.
CONCLUSION
Several conclusions can be drawn from our study:
(1) unawareness of cognitive decits seems to be
frequent but of moderate severity in patients with
early DAT. Most patients seemed to be cognitively
aware of their decits but they failed to accurately
evaluate their severity and their consequences in
everyday life; (2) the severity of unawareness
greatly varied between the patients but also
between various cognitive domains explored.
There was no strong correlation between the
subjective estimation of the memory decits and
the behavioural manifestations of unawareness;
(3) unawareness of cognitive decits seems to be
better correlated with emotional disturbances than
with the severity of the cognitive decits at this
stage of progression of the disease; (4) the main
relationship was with apathy; (5) unawareness of
cognitive decits and its behavioural consequences
should not be considered as a single entity, present
or absent, but as a process or a continuum of
thinking and feeling, which cannot be separated
either from the psychopathology of the disorder
itself or from the specicity of cognitive tasks
(Schacter, 1990, 1991; Kern et al., 1992; Bahro et al.,
1995; Feinberg, 1997; Agnew and Morris, 1998).
Copyright # 1999 John Wiley & Sons, Ltd.

The relationship between unawareness of cognitive decits and apathy seems to be the strongest
relationship in early DAT, but this needs to be
conrmed by a prospective study using more objective methods to assess unawareness and apathy.
Nevertheless, apathy is not the only correlate of
unawareness. It is likely that various dierent neuropsychological and aective mechanisms can underlie unawareness at dierent stages of the disease.
REFERENCES
Agnew, S. K. and Morris, R. G. (1998) The heterogeneity of anosognosia for memory impairment in
Alzheimer's disease: A review of the literature and a
proposed model. Aging Ment. Health 2, 719.
Anderson, S. W. and Tranel, D. (1989) Awareness of
disease states following cerebral infarction, dementia,
and head trauma: Standardized assessment. Clin.
Neuropsychologist 3, 327339.
Auchus, A. P., Goldstein, F. C., Green, J. and Green,
R. C. (1994) Unawareness of cognitive impairments in
Alzheimer's disease. Neuropsychiat. Neuropsychol.
Behav. Neurol. 7, 2529.
Babinski, J. (1914) Contribution a l'etude des troubles
mentaux dans l'hemiplegie organique. Rev. Neurol.
(Paris) 22, 845848.
Bahro, M., Siber, E. and Sunderland, T. (1995) How do
patients with Alzheimer's disease cope with their
illness? A clinical experience report. J. Am. Geriatr.
Soc. 43, 4146.
Ballard, C. G., Chithiramohan, R. N., Handy, S.,
Bannister, C., Davis, R. and Todd, N. B. (1991)
Information reliability in dementia suerers. Int. J.
Geriatr. Psychiat. 6, 313316.
Blonder, L. X., Bowers, D. and Heilman, K. M. (1991)
The role of the right hemisphere in emotional communication. Brain 114, 11151127.
Braak, H. and Braak, E. (1991) Neuropathological
staging of Alzheimer's-related changes. Acta Neuropathol. 82, 239259.
Bungener, C., Jouvent, R. and Derouesne, C. (1996)
Aective disturbances in Alzheimer's disease. J. Am.
Geriatr. Soc. 44, 10661071.
Celsis, P., Agniel, A., Puel, M., Rascol, A. and MarcVergnes, J. P. (1987) Focal cerebral hypoperfusion and
selective cognitive decit in dementia of the Alzheimer
type. J. Neurol. Neurosurg. Psychiat. 50, 16021612.
Correa, D. D., Graves, R. E. and Costa, L. (1996)
Awareness of memory decit in Alzheimer's disease
patients and memory-impaired older adults. Aging
Neuropsychol. Cognition 3, 215228.
Craig, A. H., Cummings, J. L., Fairbanks, L., Itti, L.,
Miller, B. L., Li, J. and Mena, I. (1996) Cerebral blood
ow correlates of apathy in Alzheimer disease. Arch.
Neurol. 11, 116120.
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

UNAWARENESS AND ALZHEIMER'S DISEASE

Dalla Barba, G., Parlato, V., Iavarone, A. and Boller, F.

(1995) Anosognosia, intrusions and `frontal' functions
in Alzheimer's disease and depression. Neuropsychologia 33, 247259.
Damasio, A. R. (1994) Descartes's Error. Emotion,
Reason, and the Human Brain. Putnam's, New York.
DeBettignies, B. H., Mahurin, R. K. and Pirozzolo, F. J.
(1990) Insight for impairment in independent living
skills in Alzheimer's disease and multi-infarct dementia. J. Clin. Exp. Neuropsychol. 12, 355363.
Derouesne, C., Alperovitch, A., Arvay, N., Migeon, P.,
Moulin, F., Vollant, M., Rapin, J. R. and LePoncin,
M. (1989) Memory complaints in elderly. A study of
367 community dwelling individuals from 50 to 80
year old. In Memory and aging, (C. Derouesne, D.
Guez and J. P. Porier, eds). Arch. Gerontol. Geriatr.
Suppl. 1, 151164.
Derouesne, C., Dealberto, M. J., Boyer, P., Lubin, S.,
Sauron, B., Piette, F., Kohler, F. and Alperovitch, A.
(1993) An empirical evaluation of the `Cognitive
Diculties Scale' to assess memory complaints in
general practice. Int. J. Geriatr. Psychiat. 8, 599607.
Derouesne, C., Guigot, J. and Chatellier, G. (1995) A
caregiver form of the `Cognitive Diculties Scale' for
assessment of functional impairment in daily life in
Alzheimer's disease. In Treating Alzheimer's Disease
and Other Dementias (M. Bergener and S. I. Finkel,
eds). Springer, New York, 318328.
Duyckaerts, C., Derouesne, C., Signoret, J. L., Gray, F.,
Escourolle, R. and Castaigne, P. (1985) Bilateral and
limited amygdalohippocampal lesions causing a pure
amnesic syndrome. Ann. Neurol. 18, 314319.
Feehan, M., Knight, R. G. and Partridge, F. M. (1991)
Cognitive complaint and test performance in elderly
patients suering depression or dementia. Int. J.
Geriatr. Psychiat. 6, 287294.
Feher, E. P., Mahurin, R. K., Inbody, S. B., Crook, T. H.
and Pirozzolo, F. J. (1991) Anosognosia in Alzheimer's disease. Neuropsychiat. Neuropsychol. Behav.
Neurol. 4, 136146.
Feinberg, T. E. (1997) Anosognosia and confabulation.
In Behavioural Neurology and Neuropsychology (T. E.
Feinberg and M. T. Farah, eds). McGraw-Hill, New
York, 369390.
Folstein, M. F., Folstein, S. E. and McHugh, P. R. (1975)
`Mini-Mental State': A practical method for grading
the cognitive state of patients for clinician. J. Psychiat.
Res. 12, 189198.
Goodglass, H. and Kaplan, E. (1972) Assessment of
Aphasia and Related Disorders. Lea and Febiger,
Philadelphia.
Green, J., Goldstein, F. C., Sirockman, B. E. and Green,
R. C. (1993) Variable awareness of decits in
Alzheimer's disease. Neuropsychiat. Neuropsychol.
Behav. Neurol. 6, 159165.
Grut, M., Jorm, A. F., Fratiglioni, L., Forsell, Y.,
Viitanen, M. and Windblat, B. (1993) Memory
complaints of elderly people in a population survey:
Copyright # 1999 John Wiley & Sons, Ltd.

1029

Variation according to dementia stage and depression.

J. Am. Geriatr. Soc. 41, 12951300.
Haxby, J. V., Grady, C. L., Koss, E., Horwitz, B.,
Heston, L., Schapiro, M., Friedland, R. P. and
Rapoport, S. I. (1990) Longitudinal study of cerebral
metabolic asymmetries and associated neuropsychological patterns in early dementia of the Alzheimer
type. Arch. Neurol. 47, 753760.
Jorm, A. F., Christensen, H., Henderson, A. S., Korten,
A. E., Mackinnon, A. J. and Scott, R. (1994)
Complaints of memory decline in the elderly: A
comparison of reports by subjects and informants in
a community survey. Psychol. Med. 24, 365374.
Jouvent, R., Vintreau, C., Montreuil, M., Carton, S. and
Widlocher, D. (1988) La clinique polydimensionnelle
de l'humeur depressive: Nouvelle version de l'echelle
EHD. Psychiat. Psychobiol. 3, 245253.
Katz, M. M. and Lyerly, S. B. (1963) Methods for
measuring DATjustment and social behavior in the
community: I. Rationale, description, discriminative
validity and scale development. Psychol. Rep. 13,
503535.
Kern, R. S., van Gorp, W. G., Cummings, J. L., Brown,
W. S. and Osato, S. S. (1992) Confabulation in
Alzheimer's disease. Brain Cognition 19, 172182.
Kotler-Cope, S. and Camp, C. J. (1995) Anosognosia in
Alzheimer disease. Alz. Dis. Assoc. Disord. 9, 5256.
Lawton, M. P. and Brody, E. M. (1969) Assessment of
older people: Self-maintaining and instrumental activities of daily living. Gerontologist 9, 179186.
Lhermitte, F., Pillon, B. and Serdaru, M. (1986) Human
autonomy and the frontal lobes. Ann. Neurol. 1,
326334.
Lopez, O. L., Becker, J. T., Somsak, D., Dew, M. A. and
DeKosky, S. T. (1994) Awareness of cognitive decits
and anosognosia in probable Alzheimer's disease. Eur.
Neurol. 34, 277282.
Luria, A. R. (1966) Higher Cortical Functions in Man.
Basic Books, New York.
Mangone, C. A., Hier, D. B., Gorelik, P. B., Ganellen,
R. J., Langenberg, R. J., Boarman, R. and Dollear,
W. C. (1991) Impaired insight in Alzheimer's disease.
J. Geriatr. Psychiat. Neurol. 4, 189193.
Marin, R. S. (1991) Apathy: A neuropsychiatric syndrome. J. Neuropsychiat. 243254.
Markova, I. S. and Berrios, G. E. (1992) The assessment
of insight in clinical psychiatry: A new scale. Acta
Psychiatr. Scand. 86, 159164.
McDaniel, K. D., Edland, S. D., Heyman, A. and
CERDAT clinical investigators (1995) Relationship
between the level of insight and severity of dementia in
Alzheimer's disease. Alz. Dis. Assoc. Disord. 9,
101104.
McGlone, J., Gupta, S., Humphrey, D., Oppenheimer,
S., Mirsen, T. and Evans, D. R. (1990) Screening for
early dementia using memory complaints from
patients and relatives. Arch. Neurol. 47, 11891193.
Int. J. Geriat. Psychiatry 14, 10191030 (1999)

1030

C. DEROUESNE, S. THIBAULT, S. LAGHA-PIERUCCI ET AL.

McGlynn, S. M. and Kaszniak, A. W. (1991) When

metacognition fails: Impaired awareness of decit in
Alzheimer's disease. J. Cog. Neurosci. 3, 183189.
McGlynn, S. M. and Schacter, D. L. (1989) Unawareness
of decits in neuropsychological syndromes. J. Clin.
Exp. Neuropsychol. 1, 143205.
McKhann, G., Drachman, D., Folstein, M., Katzman,
R., Price, D. and Stadlan (1984) Clinical diagnosis of
Alzheimer's disease: Report of the NINCDS
ADRDA Work Group under the auspices of
Department of Health and Human Services Task
Force on Alzheimer's disease. Neurology 34, 939944.
McNair, D. M. and Kahn, R. J. (1983) Self-assessment
of cognitive decits. In Assessment in Geriatric Psychopharmacology (T. Crook, S. Ferris and R. Bartus, eds).
Mark Powley, New Canaan (Conn), 119136.
Michon, A., Deweer, B., Pillon, B. and Dubois, B. (1994)
Relation of anosognosia to frontal lobe dysfunction in
Alzheimer's disease. J. Neurol. Neurosurg. Psychiat.
57, 805809.
Migliorelli, R., Teson, R., Sabe, L., Petracca, G.,
Petracchi, M., Leiguardia, R. and Starkstein, S. E.
(1995) Anosognosia in Alzheimer's disease: A study of
associated factors. J. Neurosci. 7, 338344.
Mullen, R., Howard, R., David, A. and Levy, R. (1996)
Insight in Alzheimer's disease. Int. J. Geriatr. Psychiat.
11, 645652.
Nargeot, M. C., Touchon, J. and Van der Linden, M.
(1994) Auto-evaluation des troubles mnesiques dans la
maladie d'Alzheimer: Heterogeneite de l'anosognosie.
In Actualites sur la Maladie d'Alzheimer et les
Syndromes Apparentes (M. Poncet, B. Michel and A.
Nieoullon, eds). Solal, Marseille, 209214.
O'Connor, D. W., Pollitt, P. A. and Roth, M. (1990)
Coexisting depression and dementia in a community
survey. Int. Psychogeriat. 2, 4554.
Ott, B. R., Noto, R. B. and Fogel, B. S. (1996) Apathy
and loss of insight in Alzheimer's disease. J. Neuropsychiat. Clin. Neurosci. 8, 4146.
Pappas, B. A., Sunderland, T., Weingartner, H. M.,
Vitello, B., Martinson, H. and Putnam, K. (1992)
Alzheimer's disease and feeling-of-knowing for knowledge and episodic memory. J. Gerontol. 47, 150164.
Raven, J. C. (1965) Guide to Using the Coloured Progressive Matrices. Lewis, London.
Reed, B. R., Jagust, W. J. and Coulter, L. (1993)
Anosognosia in Alzheimer's disease: Relationship to
depression, cognitive function, and cerebral perfusion.
J. Clin. Exp. Neuropsychol. 15, 231244.
Reisberg, B., Borenstein, J., Salob, S. P., Ferris, S. H.,
Franssen, E. and Georgotas, A. (1987) Behavioral
symptoms in Alzheimer's disease: Phenomenology and
treatment. J. Clin. Psychiat. 48, suppl., 915.
Reisberg, B., Ferris, S. H., de Leon, M. J. and Crook, T.
(1982) The Global Deterioration Scale for assessment
of primary degenerative dementia. Am. J. Psychiat.
139, 11361139.
Copyright # 1999 John Wiley & Sons, Ltd.

Reisberg, B., Gordon, B. and McCarthy, M. (1985)

Insight and denial accompanying progressive cognitive
decline in normal aging and Alzheimer's disease. In
Geriatric Psychiatry: Ethical and Legal Issues (B.
Stanley, ed.). American Psychiatric Press, Washington,
DC, 1939.
Schacter, D. L. (1990) Toward a cognitive neuropsychology of unawareness. J. Clin. Exp. Neuropsychol. 10,
155178.
Schacter, D. L. (1991) Unawareness of decit and
unawareness of knowledge in patients with memory
disorders. In Awareness of Decit After Brain Injury.
Clinical and Theoretical Issues (G. P. Prigratano and
D. L. Schacter, eds). Oxford University Press, New
York, 127151.
Sevush, S. and Leve, N. (1993) Denial of memory decit
in Alzheimer's disease. Am. J. Psychiat. 150, 748751.
Starkstein, S. E., Fedoro, J. P., Price, T. R., Leiguarda,
R. and Robinson, R. G. (1993) Neuropsychological
decits in patients with anosognosia. Neuropsychiat.
Neuropsychol. Behav. Neurol. 6, 4348.
Starkstein, S. E., Sabe, L., Chemerinski, E., Jason, L.
and Leiguardia, R. (1996) Two domains of
anosognosia in Alzheimer's disease. J. Neurol. Neurosurg. Psychiat. 61, 485490.
Starkstein, S. E., Sabe, L., Garcia Cuerva, A., Kuzis, G.
and Leiguardia, R. (1997) Anosognosia and procedural learning in Alzheimer's disease. Neuropsychiat.
Neuropsychol. Behav. Neurol. 10, 96101.
Starkstein, S. E., Vazquez, S., Migliorelli, R., Teson, A.,
Sabe, L. and Leiguardia, R. (1995) A single-photon
emission computed tomographic study of anosognosia
in Alzheimer's disease. Arch. Neurol. 52, 415420.
Sultzer, D. L., Levin, H. S., Mahler, M. E., High, W. M.
and Cummings, J. F. (1992) Assessment of cognitive,
psychiatric, and behavioral disturbances in patients
with dementia: The Neurobehavioral Rating Scale. J.
Am. Geriatr. Soc. 40, 549555.
Vasterling, J. J., Seltzer, B., Foss, J. W. and Vanderbrook, V. (1995) Unawareness of decit in Alzheimer's
disease. Domain-specic dierences and disease correlates. Neuropsychiat. Neuropsychol. Behav. Neurol. 8,
2632.
Verhey, F. J., Rozendael, N., Ponds, R. H. M. and Jolles,
J. (1993) Dementia, awareness and depression. Int. J.
Geriatr. Psychiat. 8, 851856.
Waldemar, G., Hgh, P. and Paulson, O. B. (1997)
Functional brain imaging with single-photon emission
computed tomography in the diagnosis of Alzheimer's
disease. Int. Psychogeriat. 9, Suppl. 1, 223227.
Wechsler, D. (1972) WAIS-R Manual. Psychological
Corporation, New York.
Wechsler, D. and Stone, C. P. (1973) Manual: Wechsler
Memory Scale. Psychological Corporation, New York.
Zung, W. W. K. (1965) A self-assessing depression scale.
Arch. Gen. Psychiat. 12, 6370.
Zung, W. W. K. (1971) A self-rating instrument for
anxiety disorders. Psychosomatics 12, 371379.
Int. J. Geriat. Psychiatry 14, 10191030 (1999)