R. J. Athey et al.
Age and Ageing 2005; 34: 268–273
doi:10.1093/ageing/afi098
 The Author 2005. Published by Oxford University Press on behalf of the British Geriatrics Society.
All rights reserved. For Permissions, please email: [email protected]
Cognitive assessment of a representative
community population with Parkinson’s
disease (PD) using the Cambridge Cognitive
Assessment–Revised (CAMCOG-R)
RICHARD J. ATHEY, ROBERT W. PORTER, RICHARD W. WALKER
Parkinson’s Disease Department, North Tyneside General Hospital, Rake Lane, North Shields, Tyne & Wear NE29 8NH, UK
Address correspondence to: R. J. Athey. Tel: (+44) 191 258 4404; fax: (+44) 191 293 2709; Email: [email protected]
Abstract
Background: cognitive decline is well recognised in Parkinson’s disease (PD) but the best cognitive assessment tool for use
in such patients remains unclear. The 30-point Mini-Mental State Examination (MMSE), while quick and straightforward to use,
fails to cover a full range of cognitive domains and is recognised to have a ceiling effect. The Cambridge Cognitive Assessment–
Revised (CAMCOG-R) is a cognitive screening tool allowing the assessment of a number of different domains of cognition.
It has not previously been used specifically on PD subjects.
Methods: a prevalent community population of 135 PD patients were assessed cognitively using the MMSE. Those scoring 25
or above on the MMSE were subsequently further assessed using CAMCOG-R. Demographic and disease factors including
disease duration, symptom severity, anxiety, depression and the presence of hallucinations were recorded for each participant.
Results: 31/135 (23%) demonstrated cognitive impairment on the MMSE (score <25). Ninety-four of the remaining group
(10 were excluded) achieved a median total CAMCOG-R score of 89/104. The results were widely distributed. The subjects
scored particularly highly in the cognitive domains of orientation, comprehension and perception but relatively poorly at
memory and abstract thinking. Significantly poorer scores (P < 0.05) were seen throughout the cognitive domains with
increasing age, increasing PD symptom severity and increasing disease duration, but not with the presence of anxiety, depression or hallucinations in the subjects.
Discussion: CAMCOG-R was found to be a viable and useful cognitive screening tool for use in PD. A wide range of
cognitive ability was demonstrated in subjects who had been assessed previously by the MMSE as not having significant cognitive impairment. The group performed worse in certain cognitive domains than others and those who were older, with
more severe PD symptoms and with symptoms for longer, scored less well.
Keywords: Parkinson’s disease, cognitive impairment, dementia, CAMCOG-R, elderly
Introduction
Cognitive decline is well recognised over time in Parkinson’s
disease (PD) and can be associated with Alzheimer’s
disease, vascular dementia or Lewy-body disease. Studies
have reported the frequency of dementia in PD to vary
from 8% [1] to 81% [2]. Various factors have been shown
to predict the future development of dementia in PD
patients, including older age [3], older age at diagnosis [3]
and longer duration of disease [4]. Cognitive impairment
is associated in such patients with shorter life expectancy
[5], and is known to contribute significantly towards
268
caregiver distress [6]. An accurate and relatively rapid
cognitive screening tool for use in such patients would be
useful.
Previous UK-based PD prevalence studies found frequencies of cognitive impairment varying between 18.5%
[7] using a Mini-Mental State Examination (MMSE) [8]
cut-off of 24 or less and 41% [9] using a cut-off of 25 or
less. A third study [10] described cognitive impairment in
28% of their population using the Aberdeen minimental
test. A recent Norwegian study followed a population of
PD patients, initially cognitively intact, for 8 years assessing
cognitive function at regular intervals [11]. At the end of
Cognitive screening in PD with CAMCOG-R
this period, 78% had developed cognitive impairment by
DSM III criteria with hallucinations before the onset of
cognitive decline and an akinetic-rigid form of PD as risk
factors for its subsequent development.
PD patients are frequently affected by depression and
motor deficits, which can make the assessment of cognition
difficult [12]. Several different methods of cognitive assessment have been considered in such patients.
It is desirable that any cognitive examination should be relatively brief. The MMSE is a relatively quick and straightforward
assessment of cognitive function and has been used previously in the cognitive assessment of PD patients [13]. A
decline of 1.3 MMSE points over 28 months has been demonstrated in ‘normal’ elderly individuals [14] and 3 points
annually in subjects with Alzheimer’s disease [15]. The
MMSE has, however, been shown to demonstrate a ceiling
effect in some studies with a large proportion of the subjects, felt to have a wide range of cognitive abilities, all scoring relatively highly [16]. The MMSE remains a relatively
crude tool and fails to cover a full range of cognitive
domains, particularly global and executive function. MMSE
scores have shown poor inter-examiner reliability and often
do not reflect subjective assessment.
Alternative cognitive screening methods have been
considered, one of which is the Cambridge Cognitive
Assessment (CAMCOG). Created in 1986, CAMCOG is a
107-point complete cognitive assessment and forms part of
the Cambridge Mental Disorders of the Elderly (CAMDEX) assessment [17]. With CAMCOG, eight different
domains of cognitive function can be assessed and compared. Overall scores of less than 80 have been suggested as
a cut-off for dementia [18]. It has been shown to have a
greater sensitivity and specificity for diagnosing dementia
than the MMSE [19].
When used on a group of ‘normal’ elderly individuals, all
of whom had previously scored 29–30 on the MMSE, the
CAMCOG results showed a wider spread, eliminating the
ceiling effect characteristic of the MMSE [20]. CAMCOG
was shown, therefore, to differentiate between individuals
even at high levels of performance. The maximum CAMCOG score is achieved only rarely if ever. Annual decline of
1.6 CAMCOG points has been shown in ‘normal’ individuals
including decline across every cognitive domain [21].
The only published study to use CAMCOG specifically
in PD patients [16] compared its sensitivity and specificity
for the detection of dementia with the MMSE. CAMCOG
had a sensitivity of 95% and a specificity of 94%, while the
MMSE had a sensitivity and specificity of 98% and 77%,
respectively. Poorer performance was seen using CAMCOG
in the demented group in all of the different CAMCOG
cognitive domains.
In 1999 a ‘revised’ version of CAMCOG was published.
CAMCOG-R [22] now includes questions updated to be
more relevant to the present day. To date there is little
published literature regarding this test. We chose to use
CAMCOG-R in this study as the most up-to-date version of
CAMCOG available. To our knowledge there is no evidence of CAMCOG-R ever having been used before specifically on PD subjects.
In performing this study our aims were firstly to ascertain the viability of CAMCOG-R as a cognitive assessment
tool for use in a community-based, prevalent population of
PD subjects. We wanted to determine whether CAMCOG-R
could detect cognitive impairment in subjects previously
screened using the MMSE as not being significantly cognitively impaired. We hoped to ascertain whether CAMCOG-R
could demonstrate weak and strong domains of cognitive
function in the subjects and, finally, to determine the
relationship of cognitive function to sex, age, disease severity, disease duration, and the presence of hallucinations and
depressive symptoms.
Methods
The two cognitive screening tests utilised in this study were
the MMSE and the CAMCOG-R. This study was carried
out as part of a larger study looking at the prevalence of
idiopathic PD in an area of North Tyneside in the UK with
a population of 108,597 [23]. Cases were sourced from local
hospital and general practitioner records. A variety of
demographic and disease-related information, including a
MMSE, was obtained from each participant by way of a
semi-structured interview.
Those subjects screened by a MMSE of 25–30 as not
having significant cognitive impairment were invited to take
part in this subsequent study in which they were further
cognitively assessed using CAMCOG-R. The eight CAMCOG-R domains are orientation (assessed by testing time
and place), comprehension (multi-stage commands and
questions), expression (naming objects and fluency), memory (recall and recognition of objects, general knowledge),
attention and calculation (serial sevens, counting backwards
and calculations), praxis (copying shapes, drawing a clock
and writing an envelope to dictation), abstract thinking
(similarities between objects) and perception (recognition of
famous people and objects from unusual angles). Only
subjects under the care of the North Tyneside Parkinson’s
disease service were included.
The age, sex, Hoehn and Yahr disability rating score
[24], duration of PD symptoms, Hospital Anxiety and
Depression (HAD) scores for anxiety and depression [25]
and the incidence of previous hallucinations were noted for
each participant. The correlation between these demographic and disease-related variables and the CAMCOG-R
scores was assessed using an ANOVA multiple regression
analysis and Pearson biphasic correlation coefficients.
Ethical approval for this study was granted by the Newcastle and North Tyneside Ethics Committee. The subjects
were visited in their own homes between March and
December 2003 and informed written consent was obtained
from each. In each case CAMCOG-R was completed by the
same examiner, the whole process taking around 30 minutes.
Scores were calculated for each participant for each of the
eight CAMCOG-R domains and for the total CAMCOG-R
score.
The initial prevalence study [23] was funded by Northumbria Healthcare NHS Trust. No funding was required
for this subsequent study.
269
R. J. Athey et al.
Results
Total CAMCOG-R scores
Cognitive assessment of the prevalent population
using the MMSE
The initial study [23] identified 161 subjects with PD, of
whom 135 agreed to be assessed cognitively with the
MMSE. Using a cut-off of less than 25, 31 out of 135 (23%)
were found to have evidence of dementia. Demographic
and disease characteristics of the groups with and without
evidence of dementia by the MMSE are shown in Table 1.
There was no significant difference in the frequency of
cognitive impairment between the sexes with 13/64 (21%)
of the males and 18/71 (25%) of the female subjects affected.
Further cognitive assessment of the group screened
by MMSE as cognitively intact, using CAMCOG-R
Of the 104 subjects with a MMSE of 25 or above, 10 were
excluded because they had either died, declined to participate
or were outside the care of the North Tyneside PD service,
leaving a total of 94 participants who underwent assessment
with CAMCOG-R. Demographic and clinical characteristics
of these 94 subjects are shown in Table 2.
The median total CAMCOG-R score obtained by the 94
participants was 89/104 (range 49–102). The scores were
widely distributed but the majority scored in the range of
80–100. A figure showing the distribution of the total
CAMCOG-R scores can be found in the supplementary
data on the journal website (www.ageing.oupjournals.org).
Fifteen participants scored less than 80 at CAMCOG-R.
These 15 participants had previously scored a mean MMSE
of 26.8 (range 25–29) whereas the remaining 79, who scored
80 or more at CAMCOG-R, had previously achieved a
mean MMSE of 28.4 (range 26–30).
Results for the individual CAMCOG-R cognitive
domains
Results for each of the eight CAMCOG-R cognitive
domains and the total CAMCOG-R score for the group,
divided into male and female subgroups, are shown in Table 3.
A comparison is also shown with the results from a study in
which CAMCOG was performed on a large group of ‘normal’
elderly individuals [26]. Differences in the scores obtained
between the sexes were not of statistical significance.
Table 1. Comparison of patients with and without evidence of dementia using the MMSE (n = 135)
No. in group
Mean age (years)
Mean age at onset (years)
Disease duration (years)
Hoehn Yahr
UPDRS
. . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . .. . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
MMSE <25
MMSE 25–30
Statistical significance
31
104
78.5
73.6
P = 0.01
72.5
68.2
P < 0.001
6.0
5.4
P = 0.10
2.8
2.1
P < 0.001
42.5
28.6
P = 0.03
Table 2. Demographic and clinical characteristics of the 94 subjects for CAMCOG-R
Previous hallucinations
No. in group
Age
Hoehn and Yahr
Disease duration
(years)
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
HAD ANX
HAD DEP
Formed
Minor
None
. . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . .. . . . . . . . . . . . . . . . . . . . .
Total
Male
Female
94
45
49
74.6 (51–85)
74.0 (51–85)
75.2 (59–84)
2.0 (1–5)
1.9 (1–5)
2.1 (1–5)
6.1 (1–28)
5.7 (1–17)
6.5 (1–28)
5.4 (0–15)
4.4 (0–13)
6.4 (0–15)
5.1 (0–13)
4.9 (0–12)
5.3 (0–13)
15
6
9
33
16
17
46
23
23
NB: Figures are quoted as the mean with the range for each group shown in parentheses. HAD ANX = HAD anxiety score; HAD DEP = HAD depression score.
The figures for hallucinations are given as the number of subjects in each group.
Table 3. The CAMCOG-R scoring system and scores for the individual CAMCOG-R domains compared by the gender of
the subjects and compared to recent CAMCOG ‘normative data’
Domain
Maximum
possible score
Male (n = 45)
Female (n = 49)
Total (n = 94)
Williams et al.
2003 [26]
(n = 11,009)
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . .
Orientation
Comprehension
Expression
Memory
Attention and calculation
Praxis
Abstract thinking
Perception
Total
10
9
21
27
9
12
8
8a
104a*
9 (5–10)
8 (5–9)
17 (7–21)
21 (14–26)
7 (3–9)
9 (6–12)
6 (3–8)
7 (4–8)
89 (49–102)
10 (4–10)
9 (7–9)
18 (13–21)
23 (15–26)
7 (3–9)
10 (4–12)
6 (5–8)
7 (4–8)
90 (67–100)
10 (4–10)
8 (5–9)
18 (7–21)
22 (14–26)
7 (3–9)
9 (4–12)
6 (3–8)
7 (4–8)
89 (49–102)
10
8
18
22
7
11
6
7
88
Results are given as the median with the range in parentheses.
a
For the purpose of this study the subjects were interviewed in their own homes, not infrequently alone. As suggested by the CAMCOG-R authors, the question
asking the patient to recognise two individual people was omitted. Therefore in this study the total possible score was 104. The CAMCOG-R total normally scores
out of 105 and perception out of 9.
270
Cognitive screening in PD with CAMCOG-R
Correlation between the CAMCOG-R results and
the disease characteristics of the participants
The ANOVA multiple regression analysis revealed a statistically significant correlation between the total CAMCOG-R
score and the increasing age of the participants (P = 0.011)
and their increasing disease severity (by Hoehn and Yahr
score) (P = 0.001) but not with increasing disease duration.
Pearson correlation coefficients were used to assess the
relationship between the above disease variables and each
CAMCOG-R domain. The results are shown in Table 4. Note
that the correlation coefficients are uniformly negative, indicating that as the variables increase cognitive performance
gets worse. Given statistical significance at a P-value of 0.05
or less, the domains with a significant correlation are highlighted in bold. No significant correlation was found between
anxiety, depression or the incidence of hallucinations with
any of the CAMCOG-R domains or the overall CAMCOG-R
score.
Discussion
Cognitive impairment is known to be a relatively common
disease-related complication in PD [1, 2] but its assessment
is not straightforward. We found CAMCOG-R to be a viable
and useful cognitive screening tool for use with such subjects
in their own homes, taking around 30 minutes to complete.
To our knowledge this is the first published use of CAMCOG-R on a community population and there is only one
previous study using CAMCOG, the earlier version of
CAMCOG-R, specifically on PD patients [16].
Twenty-three per cent of the prevalent population in
this study had evidence of dementia as defined by a MMSE
score of less than 25 out of 30. This figure is not dissimilar
to that obtained in previous UK prevalence studies [7, 9].
The mean age of the subjects assessed with CAMCOG-R
was 74.6 years with the female participants being slightly
older and having a slightly longer duration of PD symptoms.
CAMCOG has been shown to have a high specificity
and sensitivity for predicting dementia in PD subjects [16]
and a score of less than 80 has been used before as a cut-off
for cognitive impairment [18].The majority of subjects
achieved an overall CAMCOG-R score in the range of
80-100/104 but 15 (a further 11% of the prevalent population) scored lower than 80, suggesting evidence of dementia
not previously picked up by the MMSE (although this 15 had
achieved ‘low-normal’ MMSE scores). While CAMCOG
and CAMCOG-R differ only very marginally, a diagnostic
CAMCOG-R score for dementia has yet to be suggested.
Some of the activities involved in completing
CAMCOG-R involve a strong emphasis on writing, copying
and drawing skills, which may discriminate unfairly against
PD subjects. PD patients are characteristically subject to
‘good and bad days’ and it was felt that several subjects,
including one who scored only 49/104 overall, were assessed
on days when they were not performing as well as they
might otherwise have done.
The PD subjects in this study scored highly in the cognitive domains of orientation, comprehension and perception, but relatively poorly at expression, memory and praxis,
and particularly poorly at abstract thinking, a domain that
every subject seemed to find difficult regardless of age or
other factors. Abstract thinking, a useful neuropsychological test, is assessed in CAMCOG-R using similar questions
to those in the Wechsler adult intelligence scale [27]. These
are of sufficient difficulty that a fair proportion of ‘normal’
individuals would not be expected to get them all correct.
The questions used in orientation have been noted previously to be reasonably straightforward even for most ‘normal’
individuals [26]. The domain of memory has previously
shown the greatest variation in scores obtained [26], an
effect again reproduced in this study.
Normative values have been suggested for CAMCOG
although unfortunately not for CAMCOG-R. The two tests
are very similar and can be considered comparable. Williams
Table 4. Correlation between the eight CAMCOG-R domains with the age, disease duration and disease severity of the
subjects
Domain (n = 94)
Age
Disease duration
(years)
Disease severity
(Hoehn and Yahr)
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . .
Orientation
Comprehension
Expression
Memory
Attention and calculation
Praxis
Abstract thinking
Perception
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
Pearson correlation (r)
Sig. (2-tailed)
−0.105
P = 0.313
−0.175
P = 0.091
−0.246
P ⫽ 0.022
−0.159
P = 0.126
−0.129
P = 0.217
−0.226
P ⫽ 0.029
−0.092
P = 0.378
−0.367
P < 0.001
−0.356
P < 0.001
−0.207
P ⫽ 0.046
−0.279
P ⫽ 0.006
−0.275
P ⫽ 0.007
−0.301
P ⫽ 0.003
−0.476
P < 0.001
−0.128
P ⫽ 0.219
−0.341
P ⫽ 0.001
−0.358
P < 0.001
−0.167
P < 0.001
−0.368
P < 0.001
−0.344
P ⫽ 0.001
−0.294
P ⫽ 0.004
−0.438
P < 0.001
−0.171
P ⫽ 0.100
−0.385
P < 0.001
271
R. J. Athey et al.
et al. [26] performed CAMCOG on a group of 11,009
individuals aged 65 and upwards with a wide range of comorbidities and from a variety of socio-economic backgrounds, who had previously been assessed using methods
other than CAMCOG as having a wide range of cognitive
ability. Even given the limitations in comparing two different
but similar tests, we noted that the performance of the PD
population was almost identical to that of the control study
population across all domains. This seems to imply that the
level of cognitive function is similar in this selected PD
population to that of the general population.
The PD population scored less well in the domain of
praxis. This is assessed in CAMCOG-R using writing and
drawing skills, and probably reflects the higher incidence of
motor impairment in these patients. It has previously been
shown that subjects with Lewy-body disease can be expected
to achieve lower scores in the domain of praxis than those
with Alzheimer’s or vascular dementia but better scores at
memory testing [28]. The participants in this study performed poorly in both these areas.
When looking at the results for the PD population in
more detail, significant correlation was seen using ANOVA,
which corrects for the effects of the other variables,
between poorer total CAMCOG-R scores and the increasing
age and increasing disease severity of the subjects but not
with increasing disease duration. It could be argued that
increasing disease severity and duration in PD subjects represent a common process. The ANOVA suggests that much
of the variability demonstrated in CAMCOG-R scores in
PD is due to the increasing severity of symptoms rather
than their duration.
The majority of the CAMCOG-R domains correlate
significantly using Pearson correlations with both PD symptom duration and symptom severity in the subjects. This
implies that poorer cognitive performance across many
areas of cognition can be demonstrated with CAMCOG-R
as PD progresses over time and as its symptoms become
more severe. While cognitive decline in PD is not, in itself, a
new finding it is interesting to observe how the CAMCOG-R
domain scores are all seen to decline with the progression of
PD. This gives weight to the viability of CAMCOG-R as a
cognitive screening tool for such subjects. The increasing
age of the participants correlated significantly with poorer
performance only in the domains of expression, praxis and
perception however.
PD patients are commonly subject to depression [12] and
depression has been shown to be commoner in those PD
patients with dementia [29], but no significant relationship
was seen between any of the CAMCOG-R scores and the
presence of anxiety symptoms, depressive symptoms and the
incidence of halluinations in the subjects in this study. While
CAMCOG scores have previously been found to be vulnerable to the effects of depression [30], no evidence was found
here of depression or hallucinations, common in PD, exerting any influence on the CAMCOG-R scores. One might
well expect PD patients with hallucinations to perform worse
in cognitive testing but this was not demonstrated here.
It is already known that cognition declines over time in
PD subjects [11]. Doctors and other healthcare professionals
272
providing a service to PD patients should expect about one
quarter of their patients to have evidence of cognitive
impairment. CAMCOG-R was found to be a useful and
reasonably straightforward assessment tool for use in such
patients. While less sophisticated than the DSM criteria for
diagnosing dementia, it is likely to be far more practical in a
clinic situation. A wide range of cognitive ability was
revealed in a PD population who had all scored 25 or above
at the MMSE. We were able to demonstrate that PD subjects
perform worse in certain areas of cognition than others.
Participants who were older and who had more severe PD
symptoms and symptoms for longer tended to have significantly worse scores, these effects being reproduced across
the majority of the cognitive domains. The scores obtained
were not dissimilar to those expected of normal elderly individuals except for poorer performance in the domain of
praxis. Our population was only assessed on one occasion
but longitudinal studies looking at cognitive performance
over time in PD subjects using CAMCOG-R would be
helpful.
Key points
• 23% of the prevalent PD population showed evidence of
cognitive impairment using the MMSE. A further 11%
showed evidence of cognitive impairment using CAMCOG-R.
• CAMCOG-R can be used to demonstrate a considerable
range of cognitive ability in PD subjects previously
screened as cognitively intact using the MMSE.
• Weak and strong domains of cognitive function were
demonstrated.
• Scores obtained for the PD population closely matched
those expected of ‘normal’ elderly subjects.
• Significantly poorer performance is seen across the
CAMCOG-R scores with increasing age, increasing
symptom severity and increasing disease duration of the
participants but not with the presence of anxiety, depression or hallucinations.
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Received 29 August 2004; accepted in revised form 4 January 2005
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