Screening for Cognitive Dysfunction in Corticobasal Syndrome: Utility of Addenbrooke s Cognitive Examination
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1 Original Research Article DOI: / Accepted: March 8, 2011 Published online: April 8, 2011 Screening for Cognitive Dysfunction in Corticobasal Syndrome: Utility of Addenbrooke s Cognitive Examination Robert Mathew a, c Thomas H. Bak b John R. Hodges a, d a Neuroscience Research Australia (Previously Prince of Wales Medical Research Institute), Sydney, N.S.W., Australia; b School of Psychology, Edinburgh University, Edinburgh, UK; c Department of Neurology, Government Medical College, Trivandrum, India; d University of New South Wales, Sydney, N.S.W., Australia Key Words Addenbrooke s Cognitive Examination Addenbrooke s Cognitive Examination-Revised Corticobasal degeneration Corticobasal syndrome Pro g re ssi ve aphasia in CBS. Using a cutoff of 88/89 out of 100, 90% of CBS and 82.6% of PNFA patients were impaired. At this cutoff of 88/89, ACE-R in CBS had sensitivity and specificity values of 91 and 98%, respectively. Copyright 2011 S. Karger AG, Basel Abstract Introduction: The motor features of corticobasal syndrome (CBS) are well recognized but the fact that many, if not all, affected patients develop cognitive impairment is still underrecognized. The dementia of CBS overlaps most with a language variant of frontotemporal dementia: progressive nonfluent aphasia (PNFA). The aim of this study was to determine the usefulness of Addenbrooke s Cognitive Examination-Revised (ACE-R) in the evaluation of CBS and to document similarities and differences between CBS and PNFA. Materials and Methods: Patients with well-defined CBS or PNFA from two tertiary referral centers were selected along with matched controls. Results: Twenty-one patients with CBS, 23 patients with PNFA and 47 age- and educationmatched controls were included. Both CBS and PNFA groups showed substantial impairment on the ACE-R (f = , p! 0.001) and were significantly impaired in all domains (p! 0.001). The only significant difference between CBS and PNFA was in the visuospatial domain (p! 0.009), being worse Introduction Corticobasal syndrome (CBS) is a syndromic label used to describe patients presenting with extrapyramidal rigidity, dystonia, apraxia and alien limb phenomenon together with cognitive features, notably aphasia and frontal executive dysfunction. Although initially described as a predominantly motor syndrome, an increasing number of cases in whom cognitive involvement predominates have been reported [1 7]. As a result, CBS is now regarded as a complex disorder which affects motor and cognitive function although the relative importance of these two major features remains controversial. Progressive nonfluent aphasia (PNFA), a variant of frontotemporal dementia (FTD) characterized by disturbances in the motor aspect of language production and a variable degree of agrammatism but sparing semantics, overlaps considerably at a clinical and pathological level with CBS [8 10]. Both CBS and PNFA are associated with a range Fax karger@karger.ch S. Karger AG, Basel /11/ $38.00/0 Accessible online at: Prof. John R. Hodges Neuroscience Research Australia (Previously Prince of Wales Medical Research Institute) Barker Street, Randwick, NSW 2031 (Australia) Tel , neura.edu.au
2 of pathologies notably FTD with tau-positive inclusions and Alzheimer s disease [6, 10]. Assessment of patients with potential CBS in the clinic should involve both motor and cognitive evaluation, yet the utility of screening instruments is uncertain. Although a number of studies have explored cognition and language in CBS using detailed neuropsychologic batteries, there is clearly a need for assessment tools that are brief but useful [2 4, 7, 11]. The Mini-Mental State Examination (MMSE), which has been widely used for the screening of dementia, has the advantage of brevity and ease of administration, but lacks sensitivity to frontal, linguistic, and early amnestic deficits. Addenbrooke s Cognitive Examination (ACE) and its revision (ACE-R) are cognitive screening tests that incorporate the MMSE with expanded memory, language and visuospatial components, plus a test of verbal fluency [12, 13]. The ACE and ACE-R are able to detect early-stage dementia [12, 14] and have been shown to distinguish between FTD and Alzheimer s disease, although this is not a universal finding [15, 16]. Of relevance to the present study the ACE appears appropriate for the detection and monitoring of progressive aphasia syndromes and is sensitive to impairment in both semantic dementia and PNFA [17, 18]. The ACE has also been applied to patients with parkinsonism syndromes [12, 19, 20]. The original ACE appears useful in CBS, but the revised version, which allows analysis of the pattern across domains, has not been applied to a substantial cohort of well-defined CBS patients [19, 20] and importantly there has been no direct comparison of CBS and PNFA. The aim of this study was to determine the usefulness of ACE in the evaluation of CBS, and to explore appropriate cutoffs for detecting cognitive impairment. A second aim was to document similarities and differences between CBS and PNFA, and a third aim was to confirm previous reports regarding the profile of cognitive deficits in CBS. Materials and Methods The databases of two tertiary referral centers for cognitive and movement disorders were searched (FRONTIER, Frontotemporal Dementia Research Group in Sydney and DMC, Disorders of Movement and Cognition Clinic, Cambridge, UK) for cases assessed since the introduction of the ACE-R. All patients were assessed by one of two experienced neurologists (J.R.H. and T.H.B.) and underwent neurological examination, neuroimaging (CT or MRI) and standard neuropsychological assessments, and were followed up, whenever possible, until death. The diagnosis of CBS was made according to the criteria of Shelley et al. [5] and Bak and Hodges [21]. The diagnosis of PNFA was made according to the international consensus criteria for subtype of FTD [22, 23], on the basis of impaired motor speech and/ or agrammatism with distorted hesitant and aprosodic speech output but sparing of semantics. The details of some of these patients have been described previously [18]. Matched healthy controls were selected from the FRONTIER database. The ACE-R surveys key aspects of cognition without the use of specialized test equipment and compares five subscales: Attention and Orientation, Memory, Fluency, Language and Visuospatial. It takes an average of 15 min to complete [12, 13]. It is freely available in 15 languages with 7 more in development (see website S t a t i s t i c s SPSS software for Windows version 18 was used. One-way ANOVA was used to compare mean scores between various groups. For uniformity ACE-R scores were converted to percentage of maximum score. The receiver operating characteristic (ROC) curve was used to explore the ability in diagnosing the disease at the time of presentation of various criteria. Likelihood ratio was calculated from the sensitivity and specificity values. One-sample t test was used to compare ACE-R subscores within each group. R e s u l t s Twenty-one patients with CBS (age years), 23 patients with PNFA (age years) and 47 age- and education-matched controls (age years) were included in the study. The mean duration of illness of patients with CBS was 4 (SD 4.0) years and PNFA 1.7 (SD 0.9) years ( table 1 ). Both CBS and PNFA groups showed substantial impairment on the ACE-R. One-way ANOVAs revealed significant group effects for both the total score and subscores (f = , p! 0.001). Post hoc pairwise comparisons between groups showed that the CBS as well as the PNFA group were significantly impaired versus controls in all domains (p! 0.001). The only significant difference between CBS and PNFA was in the visuospatial subscore with the CBS group performing more poorly than the PNFA group (p! 0.009). The magnitude of impairment across domains on the ACE-R is illustrated in figure 1. It can be seen that the most impaired domain in CBS was verbal fluency followed by visuospatial function and memory. Attention and orientation was the least involved. The profile in PNFA is essentially the same with the exception of visuospatial function. Two methods were used to explore the sensitivity and specificity of the ACE-R in CBS. Using a cutoff score of 88/89, representing two standard deviations below the controls mean composite score, which also corresponds ACE-R in Corticobasal Syndrome 255
3 Table 1. C omparison of performances on the ACE-R in CBS, PNFA and controls (mean 8 SD) CBS (n = 21) PNFA (n = 23) Control (n = 47) CBS vs. control CBS vs. NFA PNFA vs. control Age, years NS NS NS Sex male, % Education, years NS NS NS MMSE total <0.001 NS <0.001 ACE-R total <0.001 NS <0.001 Subscores Attention and concentration <0.001 NS <0.001 Memory <0.001 NS <0.001 Fluency <0.001 NS <0.001 Language <0.001 NS <0.001 Visuospatial < <0.001 A ll subscores are shown as percentages of maximum. NS = Not significant at p < 0.05 (one-way ANOVA) Attention Memory Fluency CBS Language Visuospatial ACE-R total PNFA Controls Fig. 1. Graph showing the ACE-R subscores and total score. The subscores as well as ACE-R total score are expressed as percentage of maximum score. to the previously recommended upper level cutoff for use in a clinic population, 19 CBS (90%) and 19 PNFA (83%) patients scored below normal. Second, sensitivity and specificity values of the ACE-R for detecting cognitive dysfunction at various cutoff scores were determined and ROC was constructed. For CBS patients versus controls, the area under the curve was 0.99 and asymptotic significance! 0.001, thereby indicating excellent test utility. A cutoff value of 88/89 produced a sensitivity of 91% and a specificity of 98%, while at a cutoff score of 82/83 sensitivity was 71% and specificity was 100%. The corresponding values for PNFA were 91 and 94% (for cutoff of 88/89) and 83 and 100%, (for a cutoff of 82/83). Table 2 shows the sensitivity and specificity at various cutoff values of ACE-R for CBS and PNFA. Likelihood ratios were calculated for several cutoff scores based on the sensitivity and specificity values. With descending cutoffs from 92 to 85 (being the lower limit, i.e. 92 = 92/93) the likelihood ratio rose from 7.8 to 40.8 ( table 2 ), which means that a score of 85 is 40 times more likely to come from a patient with CBS than from a control subject. The corresponding likelihood ratio scores for PNFA were 7.5 at a cutoff of 92/93 and 43.5 at 88/89. In differentiating CBS from PNFA, the utility was poor as evidenced by an area under the curve of 0.5 and asymptotic significance of 0.6. Discussion This study, the first to compare directly CBS and PNFA, has confirmed equivalent levels of cognitive dysfunction in those overlapping disorders. Using a cutoff of 88/89, the ACE-R detected cognitive dysfunction in 90% of the CBS patients (sensitivity 91%, specificity 98% and likelihood ratio of 40). The subscore profile ACE-R was very similar in CBS and PNFA, except for poorer visuospatial function in CBS. As discussed above, the CBS syndrome is now conceptualized as a mixed motor and cognitive disorder. The cognitive impairment in CBS includes language, frontal executive functions and memory abilities [2 4, 7, 11]. The 256 Mathew /Bak /Hodges
4 Table 2. Likelihood ratios, sensitivity and specificity values at various ACE-R cutoff scores for CBS and PNFA versus controls ACE-R score CBS vs. controls P NFA vs. controls sensitivity, % specificity, % likelihood ratio sensitivity, % specificity, % likelihood ratio * * * Lik elihood ratio cannot be calculated as 1 specificity is 0 (marked with an asterisk). predominant form of language impairment in CBS fits within the umbrella of nonfluent aphasia with a marked reduction in speech fluency with deficits in grammar and motor speech. The prevalence of aphasia in CBS varies across studies and depends to a large extent upon selection criteria and the sophistication of the language assessment undertaken [2, 24]. In this study the vast majority of the patients (90%) had cognitive impairment based upon the ACE-R, which adds to the increasing evidence of cognitive impairment in CBS [3, 7]. Predictably, verbal fluency was the domain most affected in keeping with prior reports [2, 24], although the dementia was generalized with impairment in all areas including visuospatial function. The latter discriminated CBS from PNFA. The ACE, though initially devised as a screening instrument for Alzheimer s disease and FTD, has recently been shown to be useful in parkinsonian and progressive aphasic syndromes with an annual rate of change of 10 points per year in both PNFA and semantic dementia [18]. It is remarkable that patients presenting with an isolated language disorder, PNFA, and those with a syndrome originally conceptualized as a movement disorder sparing cognition, CBS, actually performed at a similar level on the ACE-R, further adding to evidence of overlap between these disorders that share the same range of underlying neuropathologies [6, 25]. The most notable difference was on the visuospatial component of the ACE-R. This domain includes copying of a pentagon and cube plus drawing a clock face, which may be compounded by impaired manual dexterity and, in addition, has two tests which are perceptually based (dot counting and fragmented letters) unaffected by apraxia. In summary, the ACE-R is sensitive to cognitive dysfunction in CBS with a very high level of impairment comparable to that found in patients with PNFA. Acknowledgment We thank David Foxe and Michael Hornberger for statistical and database help. Disclosure Statement Financial disclosure related to research covered in this article (12 months): nil. Full financial disclosure for the previous 12 months: nil. J.R.H. is supported by an Australian Research Council Federation Fellowship. References 1 Rebeiz JJ, Kolodny EH, Richardson EP Jr: Corticodentatonigral degeneration with neuronal achromasia. Arch Neurol 1968; 18: Graham NL, Bak T, Patterson K, Hodges JR: Language function and dysfunction in corticobasal degeneration. Neurology 2003; 61: Graham NL, Bak TH, Hodges JR: Corticobasal degeneration as a cognitive disorder. Mov Disord 2003; 18: Mathuranath PS, Xuereb JH, Bak T, Hodges JR: Corticobasal ganglionic degeneration and/or frontotemporal dementia? A report of two overlap cases and review of literature. J Neurol Neurosurg Psychiatry 2000; 68: Shelley BP, Hodges JR, Kipps CM, Xuereb JH, Bak TH: Is the pathology of corticobasal syndrome predictable in life? Mov Disord 2009; 24: Kertesz A, Martinez-Lage P, Davidson W, Munoz DG: The corticobasal degeneration syndrome overlaps progressive aphasia and frontotemporal dementia. Neurology 2000; 55: ACE-R in Corticobasal Syndrome 257
5 7 Kertesz A, McMonagle P: Behavior and cognition in corticobasal degeneration and progressive supranuclear palsy. J Neurol Sci 2010; 289: Hodges JR, Patterson K: Nonfluent progressive aphasia and semantic dementia: a comparative neuropsychological study. J Int Neuropsychol Soc 1996; 2: Hodges JR, Patterson K, Oxbury S, Funnell E: Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain 1992; 115: Knibb JA, Xuereb JH, Patterson K, Hodges JR: Clinical and pathological characterization of progressive aphasia. Ann Neurol 2006; 59: Grimes DA, Lang AE, Bergeron CB: Dementia as the most common presentation of cortical-basal ganglionic degeneration. Neurology 1999; 53: Mathuranath PS, Nestor PJ, Berrios GE, Rakowicz W, Hodges JR: A brief cognitive test battery to differentiate Alzheimer s disease and frontotemporal dementia. Neurology 2000; 55: Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR: The Addenbrooke s Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 2006; 21: Jeyapaul P, Kerwick S: Addenbrooke s Cognitive Examination as a better discriminator of cognitive impairment than the Mini- Mental State Examination in patients with dementia. Int Psychogeriatr 2008; 20: Larner AJ: Addenbrooke s Cognitive Examination (ACE) for the diagnosis and differential diagnosis of dementia. Clin Neurol Neurosurg 2007; 109: Bier JC, Ventura M, Donckels V, Van Eyll E, Claes T, Slama H, Fery P, Vokaer M, Pandolfo M: Is the Addenbrooke s cognitive examination effective to detect frontotemporal dementia? J Neurol 2004; 251: Davies RR, Dawson K, Mioshi E, Erzinclioglu S, Hodges JR: Differentiation of semantic dementia and Alzheimer s disease using the Addenbrooke s Cognitive Examination (ACE). Int J Geriatr Psychiatry 2008; 23: Leyton CE, Hornberger M, Mioshi E, Hodges JR: Application of Addenbrooke s Cognitive Examination to Diagnosis and Monitoring of Progressive Primary Aphasia. Dement Geriatr Cogn Disord 2010; 29: Bak TH, Crawford LM, Hearn VC, Mathuranath PS, Hodges JR: Subcortical dementia revisited: similarities and differences in cognitive function between progressive supranuclear palsy (PSP), corticobasal degeneration (CBD) and multiple system atrophy (MSA). Neurocase 2005; 11: Bak TH, Rogers TT, Crawford LM, Hearn VC, Mathuranath PS, Hodges JR: Cognitive bedside assessment in atypical parkinsonian syndromes. J Neurol Neurosurg Psychiatry 2005; 76: Bak TH, Hodges JR: Corticobasal degeneration: clinical aspects; in Duyckaerts C, Litvan I (eds): Handbook of Clinical Neurology. Amsterdam, Elsevier, 2008, vol 89, pp McKhann GM, Albert MS, Grossman M, Miller B, Dickson D, Trojanowski JQ: Clinical and pathological diagnosis of frontotemporal dementia: report of the Work Group on Frontotemporal Dementia and Pick s Disease. Arch Neurol 2001; 58: Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, Freedman M, Kertesz A, Robert PH, Albert M, Boone K, Miller BL, Cummings J, Benson DF: Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1998; 51: Murray R, Neumann M, Forman MS, Farmer J, Massimo L, Rice A, Miller BL, Johnson JK, Clark CM, Hurtig HI, Gorno-Tempini ML, Lee VMY, Trojanowski JQ, Grossman M: Cognitive and motor assessment in autopsy-proven corticobasal degeneration. Neurology 2007; 68: Gorno-Tempini ML, Murray RC, Rankin KP, Weiner MW, Miller BL: Clinical, cognitive and anatomical evolution from nonfluent progressive aphasia to corticobasal syndrome: a case report. Neurocase 2004; 10: Mathew /Bak /Hodges
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