The impact of the invisible
Buunk, Anne Marie
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from
it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date:
2019
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Buunk, A. M. (2019). The impact of the invisible: Cognitive deficits, behavioral changes, and fatigue after
subarachnoid hemorrhage. Rijksuniversiteit Groningen.
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 63PDF page: 63PDF page: 63PDF page: 63
4
Cognitive deficits after aneurysmal and
angiographically negative subarachnoid
hemorrhage: memory, attention, executive
functioning, and emotion recognition
Anne M. Buunk1
Rob J. M. Groen2
Wencke S. Veenstra1,2
Jan D. M. Metzemaekers2
Johannes H. van der Hoeven3
J. Marc C. van Dijk2
Jacoba M. Spikman4
1 Department of Neuropsychology, University of Groningen,
University Medical Center Groningen, the Netherlands
2 Department of Neurosurgery, University of Groningen, University Medical Center
Groningen, the Netherlands
3 Department of Neurology, University of Groningen, University Medical Center
Groningen, the Netherlands
4 Department of Neuropsychology, University of Groningen, the Netherlands
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 64PDF page: 64PDF page: 64PDF page: 64
64
Abstract
Objective. Our aim was to investigate cognitive outcome in patients with aneurysmal and angiographically negative subarachnoid hemorrhage (aSAH and anSAH), by comparing them to healthy controls and to each other. Besides investigating cognitive functions as memory and attention, we focused on higher-order prefrontal functions, namely executive functioning (EF) and emotion recognition.
Methods. Patients and healthy controls were assessed with tests measuring memory (15 Words Test, Digit Span), attention and processing speed (Trail Making Test A and B), EF (Zoo Map, Letter Fluency, Dysexecutive Questionnaire) and emotion recognition (Facial Expressions of Emotion Stimuli and Tests). Between-group comparisons of test performances were made.
Results. Patients with aSAH scored significantly lower than healthy controls on measures of memory, processing speed, and attention, but anSAH patients did not. In the higher-order prefrontal functions (EF and emotion recognition), aSAH patients were clearly impaired when compared to healthy controls. However, anSAH patients did not perform significantly better than aSAH patients on the majority of the tests.
Conclusions. In the subacute phase after SAH, cognitive functions, including the higher-order prefrontal functions EF and emotion recognition, were clearly impaired in aSAH patients. Patients with anSAH did not perform better than aSAH patients, which indicates that these functions may also be affected to some extent in anSAH patients. Considering the importance of these higher-order prefrontal functions for daily life functioning, and following the results of our present study, tests that measure emotion recognition and EF should be part of the standard neuropsychological assessment after SAH.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 65PDF page: 65PDF page: 65PDF page: 65
4
65
Introduction
Idiopathic aneurysmal subarachnoid hemorrhage (aSAH) is a severe condition, with many patients having an unfavorable neurological and neurocognitive outcome (Egge et al., 2005; Quinn et al., 2014). In approximately 15% of all patients with SAH no structural cause for the hemorrhage can be detected (Boswell, Thorell, Gogela, Lyden, & Surdell, 2013). Such cases of idiopathic SAH are typed as angiographically negative SAH (anSAH). Unlike aSAH, anSAH is regarded a more benign disorder, considering the relatively good recovery and the low number of neurological complications reported (Rinkel et al., 1991; Ruelle, Lasio, Boccardo, Gottlieb, & Severi, 1985). However, previous studies mainly focused on neurological outcomes, but there is some evidence for suboptimal neurocognitive and daily life functioning in the long-term in anSAH patients (Canhao, Ferro, Pinto, Melo, & Campos, 1995; Germano et al., 1998).
In aSAH patients, cognitive deficits are frequently found, with attention, processing speed, memory and executive functioning (EF) as the most often affected domains (Al-Khindi, Macdonald, & Schweizer, 2010; Hutter, Gilsbach, & Kreitschmann, 1994). Furthermore, a wide range of complaints is described, in particular mood disturbances and fatigue (Al-Khindi et al., 2010; Kutlubaev, Barugh, & Mead, 2012; Passier et al., 2010; Passier, Post, et al., 2011; Visser-Meily, Rhebergen, Rinkel, van Zandvoort, & Post, 2009). These sequelae can affect daily life functioning negatively; for instance, reported percentages of patients returning to work are lower than 50 (Passier, Visser-Meily, Rinkel, Lindeman, & Post, 2011; Rinkel & Algra, 2011). Higher-order prefrontal functions like EF and social cognition (SC) are crucial for adapting behavior to complex situations and hence for daily life functioning (Radice-Neumann, Zupan, Babbage, & Willer, 2007; Spikman, Milders, et al., 2013). In other patient groups, for instance patients with traumatic brain injury (TBI), clear relations have been found between EF deficits and impaired daily life functioning (Bottari, Dassa, Rainville, & Dutil, 2009). However, to date the extent to which deficits in EF and SC influence return to pre-SAH activities has not been studied. Moreover, SC has hardly been investigated in patients after (a)SAH. SC refers specifically to the ability to perceive and understand socially relevant information (Adolphs, 2001); a crucial component of SC is the recognition of the facial expression of emotions (Blair, 2003; Bornhofen & McDonald, 2008). Deficits in emotion recognition have been found to be an important predictor of behavioral problems after TBI (Babbage et al., 2011; Bornhofen & McDonald, 2008; Spikman, Milders, et al.,
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 66PDF page: 66PDF page: 66PDF page: 66
66
2013); consequently, this might also be the case in patients with (a)SAH. Unlike in aSAH, no clear evidence has been found for cognitive impairments after anSAH. Some authors found evidence for slightly lower scores considering divided attention, mental flexibility, memory and fluency (Boerboom, Heijenbrok-Kal, Khajeh, van Kooten, & Ribbers, 2014; Hutter et al., 1994; Sonesson, Saveland, Ljunggren, & Brandt, 1989), but others reported cognitive functions to be in the normal range (Germano et al., 1998; Krajewski et al., 2014). In contrast, persistent complaints have been consistently found in anSAH patients, for instance regarding irritability, depression, fatigue and cognitive functioning (Alfieri et al., 2008; Canhao et al., 1995; Marquardt, Niebauer, Schick, & Lorenz, 2000). Also, return to work percentages range from 15% to 57%, equalling those of aSAH patients (Alfieri, Gazzeri, Pircher, Unterhuber, & Schwarz, 2011; Canhao et al., 1995). Possibly, deficits in higher-order prefrontal functions contribute to negative outcome and persisting complaints after anSAH. However, EF has barely been investigated after anSAH, and, similar to aSAH, to date there are no studies that focused on SC.
Only few studies have evaluated cognitive consequences in both anSAH and aSAH patients but these yielded no consensus regarding the differences in neurocognitive outcome when these two groups were compared to each other. Some authors found that cognitive functioning was impaired to a similar extent in both groups (Hutter et al., 1994; Krajewski et al., 2014), others found a trend towards fewer deficits in anSAH patients (Mukerji et al., 2010), but relatively small subgroups were investigated or patients were compared on a limited range of general cognitive tests. We deem it worthwhile to directly compare cognitive profiles of anSAH patients to those of aSAH patients, which might be helpful in finding explanations for the fact that a part of this group has persistent complaints and problems in daily life functioning.
In addition to the initial impact caused by the hemorrhage, several secondary clinical characteristics are purported to play a role in neurocognitive outcome, such as bleeding pattern on CT (in anSAH) (Alfieri et al., 2011; Canovas, Gil, Jato, de Miquel, & Rubio, 2012), site of the aneurysm (in aSAH) (Hutter, Kreitschmann-Andermahr, & Gilsbach, 2001; Manning, Pierot, & Dufour, 2005; Mayer et al., 2002), treatment modality (surgical clipping or endovascular obliteration of the aneurysm [coiling] in aSAH) (Hutter et al., 2001; Mukerji et al., 2010), and the presence of hydrocephalus (Dombovy, Drew-Cates, & Serdans, 1998; Stienen et al., 2014) or vasospasm (Richardson, 1991). Evidence for the exact roles of these factors is conflicting and their precise relationship with
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 67PDF page: 67PDF page: 67PDF page: 67
4
67
cognitive outcome is unclear.
The aim of the present study is twofold. First, to investigate to which extent both anSAH and aSAH patients are cognitively impaired, by comparing them to healthy controls and to each other. Because of the high rates of emotional, cognitive, and physical complaints previously found after anSAH, we hypothesize that cognitive outcome is not only impaired in aSAH patients, but also in anSAH patients. Secondly, we focused mainly on deficits in higher-order prefrontal functions, in addition to testing for deficits in memory, attention, and processing speed. Deficits in EF have not been studied extensively in anSAH patients before and deficits in SC have not been studied in patients with SAH at all. Considering behavioral problems after SAH found in previous studies, we expect higher-order prefrontal functions to be impaired in SAH patients. Lastly, the impact of aneurysm location, posthemorrhagic hydrocephalus, vasospasm and treatment modality of the aneurysm (only in aSAH) will be taken into account.
Methods
All nontraumatic SAH patients admitted to the University Medical Center Groningen (UMCG) in the period from 2010 to 2013 were eligible for inclusion in this study. Exclusion criteria were age younger than 18 years, serious co-morbidity and insufficient proficiency of the Dutch language. The diagnosis of SAH was established by means of a computed tomography (CT) scan on admission and the presence (aSAH) or absence (anSAH) of a symptomatic intracranial aneurysm or vascular anomaly was evaluated using CT angiography (CTA) and/or digital subtraction angiography (DSA). AnSAH was defined as a CT-confirmed idiopathic SAH with a negative CTA and DSA. Information on demographic data (age, sex), clinical condition at admission (World Federation of Neurological Surgeons; Teasdale et al., 1988), and presence of post-hemorrhagic hydrocephalus was collected. Acute symptomatic hydrocephalus was initially treated with (temporary) external lumbar drainage (ELD) or external ventricular drainage (EVD). If symptomatic hydrocephalus persisted beyond the acute post-hemorrhage stage, external drainage was terminated and definitive internal ventriculoperitoneal (VP) shunting was performed. Patients were assessed with Transcranial Doppler sonography (TCD) exams to evaluate and monitor flow dynamics/vasospasm over time in the first two weeks after bleeding.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 68PDF page: 68PDF page: 68PDF page: 68
68
Vasospasm were diagnosed using norm values of Ringelstein et al. (1990) with a Lindegaard ratio (Lindegaard, Nornes, Bakke, Sorteberg, & Nakstad, 1989) of greater than 3 as indicative for vasospasm.
Approximately six months post-SAH, patients underwent neuropsychological assessment. Three matched (gender, age, educational level) non-overlapping healthy control groups were created based on material from previous studies in which specific test batteries were used and were recruited by means of an advertisement in a local newspaper. Control participants were excluded if they had histories of head injury or other neurological conditions, psychiatric disorders or substance abuse (information obtained per participant’s report). Approval from the Medical Ethical Committee of the UMCG has been obtained. All participants gave written consent and were treated according to the Declaration of Helsinki.
Measurement instruments
Memory, attention, and processing speed
The 15 Words Test (15WT), a Dutch version of the Rey Auditory Verbal Learning Test (Deelman, Brouwer, van Zomeren, & Saan, 1980), measures verbal memory. The score is the total words recalled in 5 trials, with a maximum of 75 and 15 for Immediate Recall (IR) and Delayed Recall (DR) respectively. Working memory was assessed with the Digit Span of the Wechsler Adult Intelligence Scale (WAIS) (Stinissen, Willems, Coetsier, & Hulsman, 1970). The score is the total strings repeated, with a maximum of 30.
The Trail Making Test (TMT) (Reitan & Wolfson, 1985) measures psychomotor speed and attention. The scores are the time (in seconds) needed to complete part A (psychomotor speed) and part B (switching attention).
Executive functioning
The Zoo Map test measures planning ability (Wilson, Alderman, Burgess, Emslie, & Evans, 1996) and has a maximum score of 16. The Dutch version of the Controlled Oral Word Association Test (Benton & Hamsher, 1976), Letter Fluency, measures verbal fluency and divergent thinking. The total score is the number of accurately produced words in three minutes.
The Dysexecutive Questionnaire, including a version to be filled in by a close other (DEX and DEX-Proxy; Wilson et al., 1996), measures executive
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 69PDF page: 69PDF page: 69PDF page: 69
4
69
impairments in daily life. This questionnaire has a maximum score of 80, whereby a total score above 27 points indicates dysexecutive problems (Spikman, Milders, et al., 2013).
Emotion recognition
Recognition of facial expressions of emotion was investigated with the Facial Expressions of Emotion Stimuli and Tests (FEEST; Young, Perrett, Calder, Sprengelmeyer, & Ekman, 2002). Sixty faces expressing the primary emotions Fear, Happiness, Disgust, Anger, Sadness or Surprise are presented to the participant with a maximum score of 60.
Statistical analysis
Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) version 22.0 . Educational level was recorded with the Dutch classification system (Verhage, 1964), ranging from 1 (no primary school) to 7 (university), which was dichotomized as low (1-4) and high (5-7). Test performances were examined in contrast to normative data as used in clinical practice and performances below the tenth percentile or a cut-off score in case of the FEEST and Zoo Map, were considered to be impaired (Lezak, Howieson, Loring, Hannay, & Fischer, 2004). Neuropsychological test scores were checked for normal distribution by using quantile-quantile (Q-Q) plots, nonparametric alternatives were applied in case of not-normally distributed scores. Mean scores (M) on the different tests were compared between anSAH, aSAH and healthy controls, using Mann-Whitney U and independent t-tests. Effect sizes (Cohen’s d) were calculated for all between-group comparisons. The overall alpha level (p) was set at 0.05 and in case of multiple comparisons, Bonferroni Holm corrections were used (Holm, 1979).
Results
In a 2-year period, 203 SAH patients were admitted to the UMCG. Of these patients, 15 died in the hospital. Of the remaining 188 patients, 69 patients were approached but declined to participate or did not participate because their clinical outcomes did not allow for a detailed neuropsychological evaluation. Therefore, 119 SAH patients (90 aSAH, 29 anSAH) were included in this study. Demographic and SAH characteristics are shown in Table 1.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 70PDF page: 70PDF page: 70PDF page: 70
70
Table 1. Characteristics of SAH patients
Characteristic aSAH (n = 90) anSAH (n = 29) Sex, number of women 62 (68.9%) 15 (51.7%) Mean age at time of the SAH, years 53.1 53.6 Time since SAH, months, mean (range) 5.2 (3-8) 4.8 (2-12) Educational level Low (1-4) 34 (37.8%) 9 (31%) High (5-7) 56 (62.2%) 20 (69%) WFNS Low (1-3) 72 (80%) 28 (96.6%) High (4-5) 18 (20%) 1 (3.4%) Hydrocephalus ELD/EVD 65 (72.2%) 11 (37.9%)
VP shunt (after ELD/EVD) 17 (18.9%) 2 (6.9%) Vasospasm on TCD Yes 67 (74.4%) 10 (34.5%) No 23 (25.6%) 19 (65.5%) Treatment aSAH Clipping 22 (24.4%) Coiling 66 (73.3%) None 2 (2.2%) Aneurysm location a Anterior 69 (76.7%) Posterior 21 (23.3%)
Note. SAH, subarachnoid hemorrhage; aSAH, aneurysmal subarachnoid hemorrhage; anSAH, angiographically negative subarachnoid hemorrhage; WFNS, World Federation of Neurological Surgeons; ELD, external lumbar drainage; EVD, external ventricular drainage; VP shunt, ventriculoperitoneal shunt; TCD, Transcranial Doppler sonography. a Aneurysm localization, divided in anterior circulation (aneurysms originating from the anterior cerebral artery, anterior communicating artery, middle cerebral artery or internal carotid artery) and posterior circulation (aneurysms originating from the posterior communicating artery or vertebrobasilar artery system).
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 71PDF page: 71PDF page: 71PDF page: 71
4
71 Comparison of aSAH patients, anSAH patients and healthy controls
Table 2 shows demographic data for the control groups 1 (15WT), 2 (Zoo Map, TMT, Digit Span and Letter Fluency) and 3 (FEEST). These three control groups were each separately compared with the patient group; statistical testing revealed no significant differences between each of the control groups and patients (all ps > 0.05).
Table 2. Characteristics of healthy controls
Characteristic Control Group 1 (n = 97) a Control Group 2 (n = 77) b Control Group 3 (n = 101) c Sex, number of women 55 (56.7%) 48 (62.3%) 67 (67.3%) Mean age, years, mean (SD) 49.6 (18.16) 56.1 (10.47) 52.2 (9.40) Educational level
Low (1-4) 43 (44.3%) 13 (16.9%) 25 (24.8%) High (5-7) 54 (55.7%) 64 (83.1%) 76 (75.2%) a Group 1: 15 Words Test; b Group 2: Zoo Map, Digit Span, Trail Making Test, Letter Fluency; c Group 3: Facial Expressions of Emotion: Stimuli and Tests.
Memory, attention, speed and executive functions
Table 3 shows results of Mann-Whitney tests or t-tests for differences in mean scores on tests for memory, speed/attention and EF of both patient groups and healthy controls as well as the percentages of patients who were impaired on these tests. Patients with aSAH scored significantly lower than healthy controls on all measures, effect sizes were moderate to large (Cohen’s d between 0.42 and 0.90). Patients with anSAH did not score significantly lower than healthy controls, effect sizes were low (Cohen’s d < 0.50). However, anSAH patients neither differed significantly from aSAH patients on most measures, except for the TMT-B and Letter Fluency. Effect sizes of the differences between anSAH and aSAH patients were low to moderate (Cohen’s d between 0.22 and 0.56).
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 72PDF page: 72PDF page: 72PDF page: 72
72
Table 3.
Performance on neuropsychological tests and comparisons between aSAH patients, anSAH patients and healthy controls
Measure aSAH anSAH Controls aSAH anSAH Controls aSAH vs controls anSAH vs controls anSAH vs aSAH % impaired % impaired % impaired M(SD) M(SD) M(SD) T/U P d a T/U p d a T/U p d a Memory 15WT IR 54.5* 41.4 27.8 38.28 (10.29) 41.69 (12.19) 43.36 (10.89) -3.25 0.001* * 0.47 -0.71 0.48 0.15 1.48 0.14 0.32 15WT DR 13.6 3.4 9.3 7.74 (2.98) 8.79 (2.76) 9.25 (3.26) -3.27 0.001* * 0.49 -0.68 0.49 0.15 1.68 0.10 0.36 Digit Span 25* 7.4 5.2 12.85 (2.96) 14.33 (3.39) 14.58 (2.73) -3.89 0.000 ** 0.61 -0.39 0.70 0.09 2.20 0.03 0.49
Attention, speed TMT-A
16.3* 3.4 5.2 40 (16.26) 32.07 (13.57) 34.14 (11.21) 2581 0.02 ** 0.42 933 0.19 0.18 822 0.006 0.51 TMT-B 16.5 3.4 6.5 98.91 (53.20) 72.59 (49.32) 76.71 (35.12) 2401.5 0.003 ** 0.49 929.5 0.19 0.11 753.5 0.002 ** 0.51
Executive Functions Zoo Map
41.4* 31 4 6.55 (6.02) 7.86 (6.26) 9.83 (5.18) -3.70 0.000 ** 0.58 -1.64 0.10 0.36 1.01 0.32 0.22 Letter Fluency 21.5* 7.7 6.3 30.19 (10.70) 36.07 (10.21) 39.57 (10.17) -5.36 0.000 ** 0.90 -1.53 0.13 0.35 2.58 0.01 ** 0.56 Note. Mann-Whitney tests were used to compare results of the Trail Making Test (TMT). aSAH, aneurysmal subarachnoid hemorrhage; anSAH, angiographically negative subarachnoid hemorrhage; t, statistic of independent t-test; U, statistic of Mann-Whitney test; 15WT
IR, 15 Words Test Immediate Recall; 15WT DR, 15 Words Test Delayed Recall. a Cohen’s d, effect size. * significant
difference in percentages impaired between the patient group (anSAH or aSAH) and control group using a χ 2 test (p < 0.05).
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 73PDF page: 73PDF page: 73PDF page: 73
4
73
Dysexecutive problems (DEX-score > 27) were reported by 26.1% of aSAH and 17.2% of anSAH patients, proxy ratings were 19.5% (aSAH) and 13.8% (anSAH). No significant differences were found between DEX total scores of both groups (t(115) = -1.92, p > 0.05) but proxies of aSAH patients reported significantly more dysexecutive problems than proxies of anSAH patients (t(113) = -2.35, p < 0.05). DEX and DEX-Proxy scores did not differ significantly in the anSAH group (t(55) = 0.84, p > 0.05) and the aSAH group (t(173) = 0.64, p > 0.05).
Emotion recognition
Table 4 shows the results of t-tests for differences in means on the total FEEST score and the six subcale scores of both patient groups and healthy controls as well as the percentages of patients with impaired performances. Patients with aSAH had significantly lower total scores as well as lower Anger and Disgust subscale scores compared to healthy controls, with moderate effect sizes (Cohen’s d > 0.50). Patients with anSAH did not differ significantly from healthy controls and neither from aSAH patients on any of the measures. Effect sizes were low (Cohen’s d < 0.50) for differences between anSAH and aSAH patients and low to moderate (Cohen’s d between 0.09 and 0.71) for differences between anSAH patients and controls.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 74PDF page: 74PDF page: 74PDF page: 74
74
Table 4.
Performance on the FEEST and comparisons between aSAH patients, anSAH patients and healthy controls.
Measure aSAH anSAH Controls aSAH anSAH Controls aSAH vs control anSAH vs control anSAH vs aSAH % impaired % impaired % impaired M(SD) M(SD) M(SD) T p d a T p d a T p d a Total 30* 17.2* 5 45.64 (6.76) 46.21 (6.63) 48.85 (3.91) -3.94 0.000 ** 0.63 -2.05 0.048 0.57 0.39 0.69 0.09 Anger 6.7 10.3* 1 7.55 (2.02) 7.38 (1.99) 8.46 (1.37) -3.57 0.000 ** 0.54 -2.73 0.01 0.71 -0.40 0.69 0.09 Disgust 16.7 13.8 11.9 7.13 (2.17) 7.72 (2.04) 8.29 (1.78) -4.03 0.000* * 0.59 -1.45 0.15 0.31 1.29 0.20 0.28 Fear 16.7 20.7 11.9 5.51 (2.19) 5.52 (2.64) 6.11 (2.25) -1.87 0.06 0.27 -1.20 0.23 0.25 0.02 0.98 0.00 Happiness 1.1 0 1 9.84 (0.40) 9.90 (0.31) 9.85 (0.43) -0.15 0.89 0.02 0.52 0.60 0.12 0.67 0.51 0.16 Sadness 25.6* 20.7 11.9 6.69 (2.13) 7.03 (2.24) 7.19 (1.76) -1.79 0.08 0.26 -0.34 0.74 0.09 0.76 0.45 0.16 Surprise 2.2 3.4 3 8.80 (1.34) 8.66 (1.32) 8.99 (1.23) -1.03 0.31 0.15 -1.27 0.21 0.21 -0.50 0.62 0.11 Note
: aSAH, aneurysmal subarachnoid hemorrhage; anSAH, angiographically negative subarachnoid hemorrhage;
t = statistic of independent
t test; FEEST, Facial Expressions of Emotion: Stimuli and Tests. a Cohen’s d, effect size. * significant difference in percentages impaired between the patient group (anSAH or aSAH) and control group using a χ2 test (
p <
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 75PDF page: 75PDF page: 75PDF page: 75
4
75 Cognitive performances related to differences in secondary clinical characteristics
Hydrocephalus
SAH patients (both anSAH and aSAH) with a VP shunt for hydrocephalus performed significantly worse on the 15WT IR (t(115) = 3.64, p < 0.05), 15WT DR (t(115) = 3.86, p < 0.05), Zoo Map (t(114) = 2.22, p < 0.05), Letter Fluency (t(110) = 2.50, p < 0.01), and FEEST total score (t(116) = 2.24, p < 0.05) than patients without a VP shunt. DEX proxy scores of patients with a VP shunt were significantly higher than those of patients without a VP shunt (t(113) = -2.72, p < 0.05), meaning proxies of patients with a VP shunt reported more executive impairments.
Vasospasm
No significant differences between cognitive outcome of SAH patients (both aSAH and anSAH) with and without vasospasm on TCD were found (all ps > 0.05).
Treatment
Patients after surgical clipping performed significantly worse on the Zoo Map, compared to patients after coiling of the aneurysm (t(85) = 2.13, p < 0.05). No significant differences were found between clipped and coiled patients on all other cognitive measures (all ps > 0.05).
Aneurysm location
No significant differences were found between patients with anterior and posterior aneurysms (all ps > 0.05).
Discussion
In the present study, we found aSAH patients to be impaired on a broad range of cognitive measures, including higher-order prefrontal functions. Although anSAH patients did not perform significantly worse than healthy controls on these measures, they also did not perform significantly better than aSAH patients, indicating suboptimal functioning. In particular we investigated higher-order prefrontal functions, i.e. social cognition and executive functioning, because of
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 76PDF page: 76PDF page: 76PDF page: 76
76
their important role in functioning in daily life. As far as we know, this is the first study that investigated emotion recognition after aSAH. As such, this also is the first study that reports serious impairment in this domain. Again, although emotion recognition of anSAH patients was not impaired when compared to healthy controls, we found clear indications of a trend towards emotion recognition impairments after anSAH.
In aSAH patients, we found deficits in memory, attention and processing speed, similar to previous studies (Al-Khindi et al., 2010; Rinkel & Algra, 2011). Also, executive deficits after SAH have been found before, but we were the first to demonstrate these deficits using a test (the Zoo Map) which has been found to have high ecological validity, that is having a high predictive value for daily life functioning (Josman et al., 2014; Norris & Tate, 2000). Authors who reported executive deficits post-SAH previously used more standard tests focusing on specific aspects of EF, for instance switching and flexibility (Kreiter et al., 2002; Manning et al., 2005; Martinaud et al., 2009) or investigated only a subgroup of clipped aSAH patients (Uchikawa et al., 2014). In addition, we extended our research by also investigating self- and other-reported executive problems. We found that proxies of aSAH patients reported significantly more dysexecutive problems than proxies of anSAH patients, while the two patient groups did not differ in their self-ratings. Possibly, self-ratings reflect the actual problems of patients less accurately than proxy-ratings in the more severely injured aSAH patients. A discrepancy between proxies’ and patients’ ratings is interpreted as indicative for impaired self-awareness in moderate to severe TBI patients (Spikman, Milders, et al., 2013). Also, in stroke patients, who are similar to SAH patients, the method of discrepancy ratings has been successfully used to rate awareness (Langer & Samuels, 2008; Nurmi Laihosalo & Jehkonen, 2014).
Although scores on cognitive tests of anSAH patients were lower than those of healthy controls, the differences were not significant. At the same time, overall cognitive performance of anSAH patients was not significantly better when compared to aSAH patients. In most cases, the means of anSAH patients were between those of healthy controls and aSAH patients. Moreover, effect sizes of the non-significant differences between anSAH and aSAH patients were moderately large, indicating a trend towards impairment in the anSAH patient group. These findings provide more insight in neurocognitive outcome after (an) SAH; cognitive functions are clearly affected in aSAH patients, and apparently not optimal in anSAH patients. In addition, almost one fifth of the anSAH patients had serious dysexecutive complaints. This profile of mild cognitive deficits with
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 77PDF page: 77PDF page: 77PDF page: 77
4
77
serious complaints in a part of the patient group bears some resemblance to what is found in patients with mild traumatic brain injury (mTBI) (Stulemeijer, Vos, Bleijenberg, & van der Werf, 2007). Results from fMRI studies suggested that mTBI patients need to use additional resources to keep cognitive functioning at a normal level (Smits et al., 2009), causing mental fatigue and a high rate of (cognitive) complaints (van der Horn, Liemburg, Aleman, Spikman, & Naalt, 2015). Possibly, a similar mechanism might explain the discrepancy between relatively intact cognition and severe subjective complaints and impaired daily life functioning after anSAH.
We were the first to investigate emotion recognition, an important aspect of SC, after SAH and found that this was significantly impaired in aSAH patients. Although we did not find significant differences in emotion recognition between anSAH patients and healthy controls, also no significant differences were found between anSAH and aSAH patients. Moreover, a significantly higher percentage of anSAH patients was impaired (i.e. performance below the tenth percentile) when compared to control subjects. These latter findings combined with moderate to high effect sizes indicate that deficits in emotion recognition can be found after anSAH. Deficits in emotion recognition have been extensively demonstrated in patients who sustained a TBI and for this patient group several authors reported a positive correlation between emotion recognition deficits and the presence of social behavioral changes (Milders, Ietswaart, Crawford, & Currie, 2008; Spikman, Milders, et al., 2013). Consequently, it seems reasonable to assume that emotion recognition is crucial for adequate social functioning after SAH as it is in TBI. This warrants further research on SC after SAH.
It has been stated before that prefrontal brain areas play an important role both in emotion recognition and in social behavior (Adolphs, 2001; Zald & Andreotti, 2010). Hence, it seems likely that impaired emotion recognition in SAH patients is related to structural defects in the prefrontal cortex. However, we found no relation between emotion recognition and the location of the aneurysm (if present) or the method of treatment (if performed). This lack of findings may be related to the fact that SAH is a complex disease, with a high risk of secondary ischemic deficits after the initial bleeding, that can occur in vascular territories remote from the site of the symptomatic aneurysm. As such, aneurysm site is not a predictor for the brain area in which secondary ischemic deficits becomes manifest. Also, choice of treatment depends on several factors, such as initial clinical condition, patient comorbidities, aneurysm size, aneurysm shape, and location of the aneurysm (Fraser et al., 2011; Jaja et al., 2015). Therefore, the
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 78PDF page: 78PDF page: 78PDF page: 78
78
reported differences between clipped and coiled patients have to be interpreted with caution, because the groups may also differ with regard to other factors. In the current study, SAH patients with a VP shunt for hydrocephalus scored significantly lower on measures of memory, EF, and emotion recognition than patients without permanent shunt. Although an association between chronic hydrocephalus and neuropsychological deficits has been suggested by several authors (Stienen et al., 2014, 2015), it remained unclear which cognitive domains are most severely affected.
Some limitations of our study have to be taken into account. First, only those patients who were able to undergo extensive neuropsychological testing were investigated; our results may not be applicable to more severely impaired SAH patients. Secondly, we investigated cognitive functioning in the subacute phase (i.e. around 6 months) after SAH. Although this is generally considered to be a clinically relevant phase to evaluate patients (Zweifel-Zehnder et al., 2015), cognitive functioning might change in the following months. Lastly, due to the relatively small number of anSAH patients, a lack of statistical power could be an explanation for the absence of significant differences in cognitive outcome between anSAH patients on the one hand and aSAH patients and healthy controls on the other hand. Effect sizes of these non-significant results were moderately large, indicating that a larger sample of anSAH patients would possibly have resulted in different findings.
In conclusion, our study shows a high rate of cognitive impairments in aSAH patients, including deficits in higher-order prefrontal functions, that is EF and emotion recognition. Although anSAH patients did not perform significantly worse than healthy controls, also only few significant differences were found when their results were compared to those of aSAH patients. Hence, neurocognitive performance in anSAH patients appears to be affected as well, albeit to a lesser extent. Importantly, we were the first to investigate emotion recognition, and found this to be clearly impaired after aSAH. Again, although anSAH patients did not differ significantly from healthy controls on emotion recognition, almost one-fifth was impaired when compared to norm scores and they did not perform better than aSAH patients. Ergo, this indicates that emotion recognition in anSAH patients is at a suboptimal level.
SC and EF are crucial for daily life functioning as was found in a range of studies in patients with moderate to severe TBI (Hanks, Rapport, Millis, & Deshpande, 1999; Novack, Bush, Meythaler, & Canupp, 2001; Spikman, Boelen, et al., 2013). In these studies, emotion recognition deficits were related
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 79PDF page: 79PDF page: 79PDF page: 79
4
79
to impaired social relationships and behavioral problems (Radice-Neumann et al., 2007; Spikman, Milders, et al., 2013), and EF deficits were associated with reduced daily functioning. Despite the relevance for daily life functioning, these higher-order prefrontal functions are not assessed routinely after SAH. However, it is likely that suboptimal higher-order prefrontal functioning affects SAH patients’ ability to meet the demands of the environment, resulting in the high amount of emotional, physical and cognitive complaints previously found after anSAH (Marquardt et al., 2000; Sonesson et al., 1989) and impaired daily functioning after aSAH (Vilkki, Juvela, Malmivaara, Siironen, & Hernesniemi, 2012). We strongly recommend for clinical practice to perform a comprehensive neuropsychological assessment post-SAH, and to incorporate measures for EF and SC into the series of tests. Considering the relationship between SC deficits and impaired psychosocial functioning as well as behavioral problems after stroke (Blonder, Pettigrew, & Kryscio, 2012; Bornstein & Poon, 2012) and TBI (Milders et al., 2008; Spikman, Milders, et al., 2013; Ubukata et al., 2014), SC is an important topic which requires further study in SAH patients. Timely detection of specific (social) cognitive deficits helps to decide whether early treatment is necessary and to tailor such treatment to individual needs. This will enhance the chance of successful social and vocational reintegration.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 80PDF page: 80PDF page: 80PDF page: 80
80
References
Adolphs, R. (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11(2), 231–239. https://doi.org/S0959-4388(00)00202-6 [pii]
Al-Khindi, T., Macdonald, R. L., & Schweizer, T. A. (2010). Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke; a Journal of Cerebral Circulation, 41(8), e519-36. https://doi.org/10.1161/STROKEAHA.110.581975; 10.1161/STROKEAHA.110.581975
Alfieri, A., Gazzeri, R., Pircher, M., Unterhuber, V., & Schwarz, A. (2011). A prospective long-term study of return to work after nontraumatic nonaneurysmal subarachnoid hemorrhage. Journal of Clinical Neuroscience : Official Journal of the Neurosurgical Society of Australasia, 18(11), 1478–1480. https://doi.org/10.1016/j. jocn.2011.02.036 [doi]
Alfieri, A., Unterhuber, V., Pircher, M., Schwarz, A., Gazzeri, R., Reinert, M., & Widmer, H. R. (2008). Psychosocial and neurocognitive performance after spontaneous nonaneurysmal subarachnoid hemorrhage related to the APOE-epsilon4 genotype: a prospective 5-year follow-up study. Journal of Neurosurgery, 109(6), 1019–1026. https://doi.org/10.3171/JNS.2008.109.12.1019 [doi]
Babbage, D. R., Yim, J., Zupan, B., Neumann, D., Tomita, M. R., & Willer, B. (2011). Meta-analysis of facial affect recognition difficulties after traumatic brain injury. Neuropsychology, 25(3), 277–285. https://doi.org/10.1037/a0021908 [doi]
Benton, A. L., & Hamsher, K. (1976). Multilingual aphasia examination (2nd ed.). Iowa City: AJA Associates.
Blair, R. J. (2003). Facial expressions, their communicatory functions and neuro-cognitive substrates. Philosophical Transactions of the Royal Society of London.Series B, Biological Sciences, 358(1431), 561–572. https://doi.org/10.1098/rstb.2002.1220 [doi]
Blonder, L. X., Pettigrew, L. C., & Kryscio, R. J. (2012). Emotion recognition and marital satisfaction in stroke. Journal of Clinical and Experimental Neuropsychology, 34(6), 634–642. https://doi.org/10.1080/13803395.2012.667069 [doi]
Boerboom, W., Heijenbrok-Kal, M. H., Khajeh, L., van Kooten, F., & Ribbers, G. M. (2014). Differences in cognitive and emotional outcomes between patients with perimesencephalic and aneurysmal subarachnoid haemorrhage. Journal of Rehabilitation Medicine : Official Journal of the UEMS European Board of Physical and Rehabilitation Medicine, 46(1), 28–32. https://doi.org/10.2340/16501977-1236 [doi]
Bornhofen, C., & McDonald, S. (2008). Emotion perception deficits following traumatic brain injury: a review of the evidence and rationale for intervention. Journal of the International Neuropsychological Society : JINS, 14(4), 511–525. https://doi. org/10.1017/S1355617708080703 [doi]
Bornstein, N., & Poon, W. S. (2012). Accelerated recovery from acute brain injuries: clinical efficacy of neurotrophic treatment in stroke and traumatic brain injuries. Drugs of Today (Barcelona, Spain : 1998), 48 Suppl A, 43–61. https://doi.org/10.1358/
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 81PDF page: 81PDF page: 81PDF page: 81
4
81 dot.2012.48(Suppl.A).1739723 [doi]
Boswell, S., Thorell, W., Gogela, S., Lyden, E., & Surdell, D. (2013). Angiogram-negative subarachnoid hemorrhage: outcomes data and review of the literature. Journal of Stroke and Cerebrovascular Diseases : The Official Journal of National Stroke Association, 22(6), 750–757. https://doi.org/10.1016/j. jstrokecerebrovasdis.2012.02.001 [doi]
Bottari, C., Dassa, C., Rainville, C., & Dutil, E. (2009). The criterion-related validity of the IADL Profile with measures of executive functions, indices of trauma severity and sociodemographic characteristics. Brain Injury, 23(4), 322–335. https://doi. org/10.1080/02699050902788436 [doi]
Canhao, P., Ferro, J. M., Pinto, A. N., Melo, T. P., & Campos, J. G. (1995). Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms. Acta Neurochirurgica, 132(1–3), 14–19.
Canovas, D., Gil, A., Jato, M., de Miquel, M., & Rubio, F. (2012). Clinical outcome of spontaneous non-aneurysmal subarachnoid hemorrhage in 108 patients. European Journal of Neurology : The Official Journal of the European Federation of Neurological Societies, 19(3), 457–461. https://doi.org/10.1111/j.1468-1331.2011.03542.x [doi] Deelman, B. G., Brouwer, W. H., van Zomeren, A. H., & Saan, R. J. (1980). Functiestoornissen
na trauma capitis. In A. Jennekens-Schinkel, J. J. Diamant, H. F. A. Diesfeldt, & R. Haaxma (Eds.), Neuropsychologie in Nederland. Van Loghum Slaterus.
Dombovy, M. L., Drew-Cates, J., & Serdans, R. (1998). Recovery and rehabilitation following subarachnoid haemorrhage: Part II. Long-term follow-up. Brain Injury, 12(10), 887–894.
Egge, A., Waterloo, K., Sjoholm, H., Ingebrigtsen, T., Forsdahl, S., Jacobsen, E. A., & Romner, B. (2005). Outcome 1 year after aneurysmal subarachnoid hemorrhage: relation between cognitive performance and neuroimaging. Acta Neurologica Scandinavica, 112(2), 76–80. https://doi.org/ANE449 [pii]
Fraser, J. F., Smith, M. J., Patsalides, A., Riina, H. A., Gobin, Y. P., & Stieg, P. E. (2011). Principles in case-based aneurysm treatment: approaching complex lesions excluded by International Subarachnoid Aneurysm Trial (ISAT) criteria. World Neurosurgery, 75(3–4), 462–475. https://doi.org/10.1016/j.wneu.2010.10.014 [doi] Germano, A., Caruso, G., Caffo, M., Cacciola, F., Belvedere, M., Tisano, A., … Tomasello,
F. (1998). Does subarachnoid blood extravasation per se induce long-term neuropsychological and cognitive alterations? Acta Neurochirurgica, 140(8), 802– 805.
Hanks, R. A., Rapport, L. J., Millis, S. R., & Deshpande, S. A. (1999). Measures of executive functioning as predictors of functional ability and social integration in a rehabilitation sample. Archives of Physical Medicine and Rehabilitation, 80(9), 1030–1037. https://doi.org/S0003-9993(99)90056-4 [pii]
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65–70.
Hutter, B. O., Gilsbach, J. M., & Kreitschmann, I. (1994). Is there a difference in cognitive deficits after aneurysmal subarachnoid haemorrhage and subarachnoid
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 82PDF page: 82PDF page: 82PDF page: 82
82
haemorrhage of unknown origin? Acta Neurochirurgica, 127(3–4), 129–135. Hutter, B. O., Kreitschmann-Andermahr, I., & Gilsbach, J. M. (2001). Health-related quality
of life after aneurysmal subarachnoid hemorrhage: impacts of bleeding severity, computerized tomography findings, surgery, vasospasm, and neurological grade. Journal of Neurosurgery, 94(2), 241–251. https://doi.org/10.3171/ jns.2001.94.2.0241
Jaja, B. N., Lingsma, H., Steyerberg, E. W., Schweizer, T. A., Thorpe, K. E., Macdonald, R. L., & investigators, on behalf of S. (2015). Neuroimaging characteristics of ruptured aneurysm as predictors of outcome after aneurysmal subarachnoid hemorrhage: pooled analyses of the SAHIT cohort. Journal of Neurosurgery, 1–9. https://doi. org/10.3171/2015.4.JNS142753 [doi]
Josman, N., Kizony, R., Hof, E., Goldenberg, K., Weiss, P. L., & Klinger, E. (2014). Using the virtual action planning-supermarket for evaluating executive functions in people with stroke. Journal of Stroke and Cerebrovascular Diseases : The Official Journal of National Stroke Association, 23(5), 879–887. https://doi.org/10.1016/j. jstrokecerebrovasdis.2013.07.013 [doi]
Krajewski, K., Dombek, S., Martens, T., Koppen, J., Westphal, M., & Regelsberger, J. (2014). Neuropsychological assessments in patients with aneurysmal subarachnoid hemorrhage, perimesencephalic SAH, and incidental aneurysms. Neurosurgical Review, 37(1), 55–62. https://doi.org/10.1007/s10143-013-0489-3 [doi]
Kreiter, K. T., Copeland, D., Bernardini, G. L., Bates, J. E., Peery, S., Claassen, J., … Mayer, S. A. (2002). Predictors of cognitive dysfunction after subarachnoid hemorrhage. Stroke; a Journal of Cerebral Circulation, 33(1), 200–208.
Kutlubaev, M. A., Barugh, A. J., & Mead, G. E. (2012). Fatigue after subarachnoid haemorrhage: a systematic review. Journal of Psychosomatic Research, 72(4), 305–310. https://doi.org/10.1016/j.jpsychores.2011.12.008; 10.1016/j. jpsychores.2011.12.008
Langer, K. G., & Samuels, M. C. (2008). Unawareness of disability in CVA: a comparison study with musculoskeletal patients. Cognitive and Behavioral Neurology : Official Journal of the Society for Behavioral and Cognitive Neurology, 21(4), 206–213. https://doi.org/10.1097/WNN.0b013e3181864a4b [doi]
Lezak, M. D., Howieson, D. B., Loring, D. W., Hannay, H. J., & Fischer, J. S. (2004). Neuropsychological Assessment (4th ed.). New York: Oxford University Press. Lindegaard, K. F., Nornes, H., Bakke, S. J., Sorteberg, W., & Nakstad, P. (1989). Cerebral
vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochirurgica, 100(1–2), 12–24.
Manning, L., Pierot, L., & Dufour, A. (2005). Anterior and non-anterior ruptured aneurysms: memory and frontal lobe function performance following coiling. European Journal of Neurology : The Official Journal of the European Federation of Neurological Societies, 12(6), 466–474. https://doi.org/10.1111/j.1468-1331.2005.01012.x Marquardt, G., Niebauer, T., Schick, U., & Lorenz, R. (2000). Long term follow up
after perimesencephalic subarachnoid haemorrhage. Journal of Neurology, Neurosurgery, and Psychiatry, 69(1), 127–130.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 83PDF page: 83PDF page: 83PDF page: 83
4
83 Martinaud, O., Perin, B., Gerardin, E., Proust, F., Bioux, S., Gars, D. L., … Godefroy,
O. (2009). Anatomy of executive deficit following ruptured anterior communicating artery aneurysm. European Journal of Neurology : The Official Journal of the European Federation of Neurological Societies, 16(5), 595–601. https://doi. org/10.1111/j.1468-1331.2009.02546.x [doi]
Mayer, S. A., Kreiter, K. T., Copeland, D., Bernardini, G. L., Bates, J. E., Peery, S., … Connolly Jr, E. S. (2002). Global and domain-specific cognitive impairment and outcome after subarachnoid hemorrhage. Neurology, 59(11), 1750–1758.
Milders, M., Ietswaart, M., Crawford, J. R., & Currie, D. (2008). Social behavior following traumatic brain injury and its association with emotion recognition, understanding of intentions, and cognitive flexibility. Journal of the International Neuropsychological Society : JINS, 14(2), 318–326. https://doi.org/10.1017/S1355617708080351 [doi] Mukerji, N., Holliman, D., Baisch, S., Noble, A., Schenk, T., & Nath, F. (2010).
Neuropsychologic impact of treatment modalities in subarachnoid hemorrhage: clipping is no different from coiling. World Neurosurgery, 74(1), 129–138. https:// doi.org/10.1016/j.wneu.2010.05.009 [doi]
Norris, G., & Tate, G. L. (2000). The behavioural assessment of the dysexecutive syndrome (BADS): Ecological, concurrent and construct validity. Neuropsycholical Rehabilitation, 10, 33–45.
Novack, T. A., Bush, B. A., Meythaler, J. M., & Canupp, K. (2001). Outcome after traumatic brain injury: pathway analysis of contributions from premorbid, injury severity, and recovery variables. Archives of Physical Medicine and Rehabilitation, 82(3), 300– 305. https://doi.org/S0003-9993(01)94036-5 [pii]
Nurmi Laihosalo, M. E., & Jehkonen, M. (2014). Assessing anosognosias after stroke: a review of the methods used and developed over the past 35 years. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior, 61, 43–63. https://doi.org/10.1016/j.cortex.2014.04.008 [doi]
Passier, P. E., Post, M. W., van Zandvoort, M. J., Rinkel, G. J., Lindeman, E., & Visser-Meily, J. M. (2011). Predicting fatigue 1 year after aneurysmal subarachnoid hemorrhage. Journal of Neurology, 258(6), 1091–1097. https://doi.org/10.1007/ s00415-010-5891-y [doi]
Passier, P. E., Visser-Meily, J. M., Rinkel, G. J., Lindeman, E., & Post, M. W. (2011). Life satisfaction and return to work after aneurysmal subarachnoid hemorrhage. Journal of Stroke and Cerebrovascular Diseases : The Official Journal of National Stroke Association, 20(4), 324–329. https://doi.org/10.1016/j. jstrokecerebrovasdis.2010.02.001; 10.1016/j.jstrokecerebrovasdis.2010.02.001 Passier, P. E., Visser-Meily, J. M., van Zandvoort, M. J., Post, M. W., Rinkel, G. J., &
van Heugten, C. (2010). Prevalence and determinants of cognitive complaints after aneurysmal subarachnoid hemorrhage. Cerebrovascular Diseases (Basel, Switzerland), 29(6), 557–563. https://doi.org/10.1159/000306642; 10.1159/000306642
Quinn, A. C., Bhargava, D., Al-Tamimi, Y. Z., Clark, M. J., Ross, S. A., & Tennant, A. (2014). Self-perceived health status following aneurysmal subarachnoid haemorrhage:
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 84PDF page: 84PDF page: 84PDF page: 84
84
a cohort study. BMJ Open, 4(4), e003932-2013-003932. https://doi.org/10.1136/ bmjopen-2013-003932 [doi]
Radice-Neumann, D., Zupan, B., Babbage, D. R., & Willer, B. (2007). Overview of impaired facial affect recognition in persons with traumatic brain injury. Brain Injury, 21(8), 807–816. https://doi.org/781125439 [pii]
Reitan, R. M., & Wolfson, D. (1985). The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. Neuropsychology Press.
Richardson, J. T. (1991). Cognitive performance following rupture and repair of intracranial aneurysm. Acta Neurologica Scandinavica, 83(2), 110–122.
Ringelstein, E. B., Kahlscheuer, B., Niggemeyer, E., & Otis, S. M. (1990). Transcranial Doppler sonography: Anatomical landmarks and normal velocity values. Ultrasound in Medicine & Biology, 16, 745–761. http:// dx.doi.org/10.1016/0301-5629(90)90039-F
Rinkel, G. J., & Algra, A. (2011). Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurology, 10(4), 349–356. https://doi. org/10.1016/S1474-4422(11)70017-5; 10.1016/S1474-4422(11)70017-5
Rinkel, G. J., Wijdicks, E. F., Vermeulen, M., Hasan, D., Brouwers, P. J., & van Gijn, J. (1991). The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Annals of Neurology, 29(5), 463–468. https://doi.org/10.1002/ ana.410290503 [doi]
Ruelle, A., Lasio, G., Boccardo, M., Gottlieb, A., & Severi, P. (1985). Long-term prognosis of subarachnoid hemorrhages of unknown etiology. Journal of Neurology, 232(5), 277–279.
Smits, M., Dippel, D. W., Houston, G. C., Wielopolski, P. A., Koudstaal, P. J., Hunink, M. G., & van der Lugt, A. (2009). Postconcussion syndrome after minor head injury: brain activation of working memory and attention. Human Brain Mapping, 30(9), 2789–2803. https://doi.org/10.1002/hbm.20709 [doi]
Sonesson, B., Saveland, H., Ljunggren, B., & Brandt, L. (1989). Cognitive functioning after subarachnoid haemorrhage of unknown origin. Acta Neurologica Scandinavica, 80(5), 400–410.
Spikman, J. M., Boelen, D. H., Pijnenborg, G. H., Timmerman, M. E., van der Naalt, J., & Fasotti, L. (2013). Who benefits from treatment for executive dysfunction after brain injury? Negative effects of emotion recognition deficits. Neuropsychological Rehabilitation, 23(6), 824–845. https://doi.org/10.1080/09602011.2013.826138 [doi]
Spikman, J. M., Milders, M. V, Visser-Keizer, A. C., Westerhof-Evers, H. J., Herben-Dekker, M., & van der Naalt, J. (2013). Deficits in facial emotion recognition indicate behavioral changes and impaired self-awareness after moderate to severe traumatic brain injury. PloS One, 8(6), e65581. https://doi.org/10.1371/journal. pone.0065581; 10.1371/journal.pone.0065581
Stienen, M. N., Smoll, N. R., Weisshaupt, R., Fandino, J., Hildebrandt, G., Studerus-Germann, A., & Schatlo, B. (2014). Delayed cerebral ischemia predicts neurocognitive impairment following aneurysmal subarachnoid hemorrhage. World
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 85PDF page: 85PDF page: 85PDF page: 85
4
85 Neurosurgery. https://doi.org/S1878-8750(14)00470-7 [pii]
Stienen, M. N., Weisshaupt, R., Fandino, J., Hildebrandt, G., Studerus-Germann, A., & Schatlo, B. (2015). Characteristics of patients without neuropsychological deficits following aneurysmal subarachnoid haemorrhage. Acta Neurochirurgica. Supplement, 120, 125–129. https://doi.org/10.1007/978-3-319-04981-6_21 [doi] Stinissen, J., Willems, P. J., Coetsier, P., & Hulsman, W. L. L. (1970). Handleiding bij de
Nederlandstalige Bewerking van de Wechsler Adult Intelligence Scale (W.A.I.S.) [manual of the Dutch edition of the WAIS]. Lisse: Swets & Zeitlinger.
Stulemeijer, M., Vos, P. E., Bleijenberg, G., & van der Werf, S. P. (2007). Cognitive complaints after mild traumatic brain injury: things are not always what they seem. Journal of Psychosomatic Research, 63(6), 637–645. https://doi.org/S0022-3999(07)00295-4 [pii]
Teasdale, G. M., Drake, C. G., Hunt, W., Kassell, N., Sano, K., Pertuiset, B., & De Villiers, J. C. (1988). A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. Journal of Neurology, Neurosurgery, and Psychiatry, 51(11), 1457.
Ubukata, S., Tanemura, R., Yoshizumi, M., Sugihara, G., Murai, T., & Ueda, K. (2014). Social cognition and its relationship to functional outcomes in patients with sustained acquired brain injury. Neuropsychiatric Disease and Treatment, 10, 2061–2068. https://doi.org/10.2147/NDT.S68156 [doi]
Uchikawa, K., Inaba, M., Kagami, H., Ichimura, S., Fujiwara, T., Tsuji, T., … Liu, M. (2014). Executive dysfunction is related with decreased frontal lobe blood flow in patients with subarachnoid haemorrhage. Brain Injury : [BI], 28(1), 15–19. https://doi.org/10 .3109/02699052.2013.847209; 10.3109/02699052.2013.847209
van der Horn, H. J., Liemburg, E. J., Aleman, A., Spikman, J. M., & Naalt, J. V. (2015). Brain Networks Subserving Emotion Regulation and Adaptation after Mild Traumatic Brain Injury. Journal of Neurotrauma. https://doi.org/10.1089/neu.2015.3905 [doi] Verhage, F. (1964). Intelligentie en leeftijd: onderzoek bij Nederlanders van twaalf tot
zevenenzeventig jaar [Intelligence and age: Study on Dutch people from age 12 to 77]. Assen: Van Gorcum.
Vilkki, J., Juvela, S., Malmivaara, K., Siironen, J., & Hernesniemi, J. (2012). Predictors of work status and quality of life 9-13 years after aneurysmal subarachnoid hemorrahage. Acta Neurochirurgica, 154(8), 1437–1446. https://doi.org/10.1007/ s00701-012-1417-y; 10.1007/s00701-012-1417-y
Visser-Meily, J. M., Rhebergen, M. L., Rinkel, G. J., van Zandvoort, M. J., & Post, M. W. (2009). Long-term health-related quality of life after aneurysmal subarachnoid hemorrhage: relationship with psychological symptoms and personality characteristics. Stroke; a Journal of Cerebral Circulation, 40(4), 1526–1529. https:// doi.org/10.1161/STROKEAHA.108.531277; 10.1161/STROKEAHA.108.531277 Wilson, B. A., Alderman, N., Burgess, P. W., Emslie, H., & Evans, J. J. (1996). Behavioural
assessment of the dysexecutive syndrome. Bury St. Edmunds: Thames Valley Test Company.
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
Processed on: 18-12-2018 PDF page: 86PDF page: 86PDF page: 86PDF page: 86
86
expressions of emotion - stimuli and tests (FEEST). Bury St Edmunds, England: Thames Valley Test Company.
Zald, D. H., & Andreotti, C. (2010). Neuropsychological assessment of the orbital and ventromedial prefrontal cortex. Neuropsychologia, 48(12), 3377–3391. https://doi. org/10.1016/j.neuropsychologia.2010.08.012 [doi]
Zweifel-Zehnder, A. E., Stienen, M. N., Chicherio, C., Studerus-Germann, A., Blasi, S., Rossi, S., … group, S. S. O. S. study. (2015). Call for uniform neuropsychological assessment after aneurysmal subarachnoid hemorrhage: Swiss recommendations. Acta Neurochirurgica, 157(9), 1449–1458. https://doi.org/10.1007/s00701-015-2480-y [doi]
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018
526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk 526454-L-bw-Buunk Processed on: 18-12-2018 Processed on: 18-12-2018 Processed on: 18-12-2018