RICHARD J. ATHEY, ROBERT W. PORTER, RICHARD W. WALKER. Abstract. Introduction. R. J. Athey et al.

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1 R. J. Athey et al. Age and Ageing 2005; 34: doi: /ageing/afi098 The Author Published by Oxford University Press on behalf of the British Geriatrics Society. All rights reserved. For Permissions, please 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) ; fax: (+44) ; richardathey@doctors.org.uk 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 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 268

2 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 (CAM- DEX) 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 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 CAM- COG 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. Cognitive screening in PD with CAMCOG-R 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 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 CAM- COG-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

3 R. J. Athey et al. Results 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. Total CAMCOG-R scores The median total CAMCOG-R score obtained by the 94 participants was 89/104 (range ). The scores were widely distributed but the majority scored in the range of A figure showing the distribution of the total CAMCOG-R scores can be found in the supplementary data on the journal website ( 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 < MMSE Statistical significance P = 0.01 P < P = 0.10 P <0.001 P = 0.03 Table 2. Demographic and clinical characteristics of the 94 subjects for CAMCOG-R Previous hallucinations Disease duration No. in group Age Hoehn and Yahr (years) HAD ANX HAD DEP Formed Minor None Total (51 85) 2.0 (1 5) 6.1 (1 28) 5.4 (0 15) 5.1 (0 13) Male (51 85) 1.9 (1 5) 5.7 (1 17) 4.4 (0 13) 4.9 (0 12) Female (59 84) 2.1 (1 5) 6.5 (1 28) 6.4 (0 15) 5.3 (0 13) 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 [26] (n = 11,009) Orientation 10 9 (5 10) 10 (4 10) 10 (4 10) 10 Comprehension 9 8 (5 9) 9 (7 9) 8 (5 9) 8 Expression (7 21) 18 (13 21) 18 (7 21) 18 Memory (14 26) 23 (15 26) 22 (14 26) 22 Attention and calculation 9 7 (3 9) 7 (3 9) 7 (3 9) 7 Praxis 12 9 (6 12) 10 (4 12) 9 (4 12) 11 Abstract thinking 8 6 (3 8) 6 (5 8) 6 (3 8) 6 Perception 8 a 7 (4 8) 7 (4 8) 7 (4 8) 7 Total 104 a * 89 (49 102) 90 (67 100) 89 (49 102) 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

4 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 CAM- COG-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 /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 Pearson correlation (r) Sig. (2-tailed) P = P <0.001 P <0.001 Comprehension Pearson correlation (r) Sig. (2-tailed) P = P P <0.001 Expression Pearson correlation (r) Sig. (2-tailed) P P P <0.001 Memory Pearson correlation (r) Sig. (2-tailed) P = P P Attention and calculation Pearson correlation (r) Sig. (2-tailed) P = P P Praxis Pearson correlation (r) Sig. (2-tailed) P P <0.001 P <0.001 Abstract thinking Pearson correlation (r) Sig. (2-tailed) P = P P Perception Pearson correlation (r) Sig. (2-tailed) P <0.001 P P <

5 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. 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