IOS Press The prognostic value of neuropsychological ...Hemorrhage (PAASH) scale, were obtained from the prospectively collected database of the UMC Utrecht. A highly similar control

Behavioural Neurology 23 (2010) 173–175 173DOI 10.3233/BEN-2010-0287IOS Press

The prognostic value of neuropsychologicalexamination after SAH

J.F. Penninxa,b, J.M.A. Visser-Meilyc, P.E.C.A. Passierc, G.J.E. Rinkelb, M.W. Postc

M.J.E. Van Zandvoorta,b

aPsychological Laboratory, Heimholtz Institute, Utrecht University, The NetherlandsbRudolf Magnus Institute of Neuroscience, Department of Neurology and Neurosurgery, University Medical CentreUtrecht, Utrecht, The NetherlandscRudolf Magnus Institute of Neuroscience and Centre of Excellence for Rehabilitation Medicine, UniversityMedical Centre Utrecht and De Hoogstraat, Utrecht, The Netherlands

1. Introduction

Cognitive impairments are well known conse-quences of subarachnoid hemorrhage (SAH) [7]. In50–60 % of the SAH survivors mild to severe cogni-tive dysfunctions have been reported [5,10]. Moreover,from the SAH survivors with a good neurological out-come (no physical disabilities) 30% remain cognitiveimpaired in the long term [10].

Memory appeared most frequently impaired [3,6].However, evidence for more diffuse deficits, such asreduced psychomotor speed and decreased sustainedattention, have been reported [7]. A recent review un-derlines the heterogeneity of the cognitive sequels af-ter SAH and points towards memory, executive func-tioning and language as most frequently impaired [1].Therefore, a clear-cut profile of the cognitive sequelsof SAH is still lacking, and so far no predictors for longterm cognitive functioning have been reported. Never-theless, the majority of SAH patients experience cog-nitive complaints of influence on their quality of life,stressing the need for more knowledge in this area tooptimise care in the long term. The aims of the presentstudy are (a) to describe the course of cognitive func-tioning at three months and 1 year post SAH and (b) tosearch for sensitive predictors for cognitive functioningin the long term.

2. Methods

2.1. SAH patients and procedure

At our SAH-outpatient clinic a concise cognitive ex-amination is administered within 3 months after a SAHfrom a rupturedaneurysm (baseline measurement). For53 randomly assigned patients an extended evaluationtook place at 12 to 18 months post onset. Patientgroup included 42 women (79%), with mean age of54.4 (11.8) range of 32 to 85. Data on demograph-ics and clinical condition, assessed by means of thePrognosis on Admission of Aneurysmal SubarachnoidHemorrhage (PAASH) scale, were obtained from theprospectively collected database of the UMC Utrecht.A highly similar control group was assembled as ref-erence sample consisting of 62 subjects all seen twicefor neuropsychological examination. Both baseline (9tasks) and follow-up (16 tasks) examination coveredsix major cognitive domains consisting of verbal andnonverbal neuropsychological tasks: Verbal and Non-verbal Memory, Attention, Executive functioning, Vi-suoconstruction and Perception, and Speed of Process-ing.

2.2. Statistical analyses

The PAASH was dichotomized resulting in good(PAASH 6 I) or reduced (PAASH>I) clinical condi-tion. The raw test scores on the individual neuropsy-

ISSN 0953-4180/10/$27.50 2010 – IOS Press and the authors. All rights reserved

174 J.F. Penninx et al. / The prognostic value of neuropsychological examination after SAH

Fig. 1. ROC curve. Prognostic validity of neuropsychological tasks on cognitive functioning in the long term.

chological tasks were transformed into z-scores basedon the reference sample. Subsequently, we averagedz-scores of individual tasks into domain scores. Forclassification of impairment, either at task or domainlevel, z-score< −1.5 was used. In addition, a sumscore for overall cognitive integrity was composed bythe mean z-score of all assessed tasks. This measurewas dichotomised as z-score> −0.5 representing cog-nitively favourable outcome, and z-score6 − 0.5 aspointing toward the presence of cognitive problems thatcan hamper daily life [4].

Receiver-operator characteristic (ROC curves) wereused to search for the best predictors for cognitive in-tegrity in the long term amongst the neuropsychologicaltasks and the PAASH.

3. Results

At baseline, 20 of the 53 patients (38%) presentedwith a cognitive impairment in one or more domains.Deficits appeared as expected in a heterogeneous pat-tern with most deficits in the domains of verbal andnonverbal memory and visuoconstruction. Notably, inalmost 1 out every 2 patients (45%) these impairmentsappeared persistent as compared to the same test bat-tery at follow-up. Inspection of the recovery courseshowed that the domain Attention and Nonverbal mem-

ory demonstrated the largest recovery, whereas impair-ments in Visuoconstruction and Visuoperception re-mained over time.

ROC-analyses in search for sensitive predictors forlong term cognitive functioning, represented as the di-chotomised sum score of all tasks of the extended testbattery, demonstrated that clinical condition (PAASH)had only limited non-significant predictive value; opti-mal cut-off PAASH: 1,5/6 with a corresponding sensi-tivity/specificity 17/59. The Rey-Osterrieth ComplexFigure appeared to be the most sensitive predictor forlong term cognitive functioning (AUC= 0.93; 95% CI:0.86–1.00,p < 0.0001). The optimal cut-off score of30,5/36 yielded a sensitivity/specificity rate of 96/65,indicative for a highly sensitive measurement [2].

4. Discussion

On the whole, our patients, showed both relativelygood clinical and cognitive outcome in line with ear-lier findings. However, our study included selective-ly patients who visited outpatient clinics within threemonths post SAH, so these comprise the SAH survivorswith expected good outcome. It is the more importantto note that, the profile at baseline reflected a hetero-geneous pattern of impairments across individuals anddomains. This heterogeneity was in line with the lit-

J.F. Penninx et al. / The prognostic value of neuropsychological examination after SAH 175

erature [1]. Unexpected was that in almost half of theinitially cognitive impaired patients (45%) deficits re-mained present over time, with impairments in visuo-construction and perception as most persistent. More-over, in search for a predictor for cognitive integrity inthe long term, the Rey-Osterrieth complex figure copyemerged surprisingly as the most sensitive predictor.

Although the suggestion of this study could be that aSAH leads towards impairments in the visuoperceptionand construction, impairments are relatively mild andon group level do not resemble focal impairments invisual perception. The heterogeneity of the profile atbaseline resembles the diffuse effects of a SAH on thecognitive functioning. We interpret our findings as adecrease in cognitive integrity, which is more affectedat baseline as reflected in a heterogeneous profile. Inthe long term patients recover, however a substantialpart of the SAH survivors with seemingly good out-come, present with persistent cognitive impairments.The Rey-Osterrieth complex figure copy appeared tobe able to significantly predict cognitive integrity evenat a subtle level of dysfunction. From earlier researchwe know that the majority of the SAH patients expe-rience cognitive complaints in the long term affectingtheir quality of life [1]. We suggest that these cognitivecomplaints might reflect the experienced decrease incognitive integrity as can be predicted by neuropsycho-logical evaluation within three months post SAH.

References

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[2] H. Blake, M. McKinney, K. Treece, E. Lee and N.B. Lincoln,An evaluation of screening measures for cognitive impairmentafter stroke,Age and Ageing31 (2002), 451–456.

[3] M.L. Hackett, M.A. Hons and C.S. Anderson, Health out-comes 1 year after subarachnoid hemorrhage,Neurology55(2000), 658–662.

[4] M.D. Lezak, D.B. Howieson and D.W. Loring,Neuropsycho-logical Assessment, (4th ed.), New York: Oxford UniversityPress (2004).

[5] W.T. Longstret, L.M. Nelson, T.D. Koepsell and G. van Belle,Clinical course of spontaneous subarachnoid hemorrhage: apopulation-based study in King County, Washington,Neurol-ogy43 (1993), 712–718.

[6] S.A. Mayer, K.T. Kreiter, M.A. Copeland, G.L. Bernardini,J.E. Bates, S. Peery, J. Claassen, Y.E. Du and E.S. Connolly,Global and domain- specific cognitive impairment and out-come after subarachnoid hemorrhage,Neurology59 (2002),1750–1758.

[7] J.A. Odgen, E.W.M.B. Mee and M.M.A. Henning, A prospec-tive study of impairment of cognition and memory and recov-ery after subarachnoid hemorrhage,Neurosurgery33 (1993),572–587.

[8] P.E.C.A. Passier, J.M.A. Visser-Meily, M.J.E. van Zandvoort,M.W.M. Post, G.J.E. Rinkel and C. van Heugten, Prevalenceand determinants of cognitive complaints after aneurismalsub-arachnoid hemorrhage,Cerebrovascular Diseases29 (2010),557–563.

[9] R.B. Scott, F. Eccles, A.J. Molyneux, R.S.C. Kerr, P.M. Roth-well and K. Carpenter, Improved Cognitive Outcomes WithEndovascular Coiling of Ruptured Intracranial Aneurysms:Neuropsychological Outcomes From the International Sub-arachnoid Aneurysm Trial (ISAT),Stroke41 (2010), 1743–1747.

[10] J.I. Suarez, Timing of neuropscyological outcome measuresin patients with subarachnoid hemorrhage,Stroke28 (2007),1724–1725.

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IOS Press The prognostic value of neuropsychological ...Hemorrhage (PAASH) scale, were obtained from the prospectively collected database of the UMC Utrecht. A highly similar control