Jacobs Journal of Neurology and Neuroscience

Change in Mood and Functional Outcomes in the Year following Subarachnoid Haemorrhage and Comparison to Matched Controls

*Suzanne Barker-Collo
Department Of Psychology, The University Of Auckland, Auckland, New Zealand

*Corresponding Author:
Suzanne Barker-Collo
Department Of Psychology, The University Of Auckland, Auckland, New Zealand
Email:s.barker-collo@auckland.ac.nz

Published on: 2018-09-04

Abstract

Subarachnoid Haemorrhage (SAH) research rarely examines psychological outcomes, particularly in relation to functional recovery (e.g., Health Related quality of life HRQoL). This study describes mood and functional outcomes in the first year postSAH, compared to matched controls, and examined factors related to mood and function at 12-months. Thirty individuals with SAH and 29 age, gender and ethnicity matched controls participated. SAH-participants were assessed at 28-days, 6- and 12-months post-SAH on the Hospital Anxiety Depression Scale(HADS), General Health Questinonaire-28(GHQ-28), Short Form36(SF-36), modified Rankin Scale(mRS), and Barthel Index (BI). Despite good disability outcomes (mRS≤2; BI≥90) at each assessment, SAH participants exceeded cut-off on the GHQ-28 at 28-days, but not 6- or 12-months. At 6- and 12-months the SAH group scored significantly higher than controls on the HADS and GHQ-28, was significantly more disabled (mRS but not BI), and had significantly poorer HRQoL. From 28-days to 6-months, HADS depression scores and GHQ-28 somatic symptoms and social dysfunction scores reduced significantly while HADS anxiety and GHQ-28 total score did not change (p>.05). No significant changes were found for mood or HRQoL from 6- to 12-months (p>.05). Age, ethnicity, education, and SAH severity were not related to 12-month HRQoL (p>.05), while female gender, clipping, having previous stroke history, and worse overall mood were significantly related. Mood and HRQoL outcomes should be repeatedly assessed post-SAH. The current findings indicated that SAH survivors who have had a previous stroke and/or underwent surgical clipping during acute SAH intervention had worse emotional and physical HRQoL outcomes compared to those survivors who had not.

Keywords

Subarachnoid Haemorrhage; Mood; Quality Of Life; Matched Comparison

Introduction

Subarachnoid haemorrhage(SAH) accounts for approximately only 5% of strokes [1], yet occurs at a young age leading to lengthy burden. SAH outcomes research has rarely examined psychological outcomes, despite their prevalence and substantial contribution to recovery [2], and potentially to functional outcomes.

Mood Post-SAH

Studies show increased rates of post-stroke depression (PSD) and anxiety (PSA) following SAH compared to controls [3]. Studies reporting mood outcomes have often used rare SAH cases and/or samples whose characteristics predict favourable outcome (e.g., no complications [4, 5]). Reported rates of emotional outcomes also vary widely post-SAH with depression rates ranging from 5% to 50%, and anxiety from 27 to 54% [6, 7]. Frequency of psychological outcomes vary over time, ranging from 14% to 64% (depression) and 16 to 52% (anxiety) at 3-months [3, 8, 9]; and up to 33% (depression) at 12-months [7]. Differing rates may also be attributed to differing samples, time frames, definitions and measures [10]. Of interest here is whether mood outcomes have an independent impact on wider functional outcomes post-SAH.

Impact of Mood on Functional Outcomes

Functional outcomes (e.g., disability, health related quality of life[HRQoL]) are associated with PSD 12-months postSAH, with depressed patients demonstrating significantly more disability, handicap, institutionalisation, poorer HRQoL, reduced return to pre-stroke employment, poorer social cognition, and fewer social activities [7, 11-13]. More severe PSD is linked to more severe functional disability after stroke [14, 15], and remission of PSD significanlty improves performance of daily activities and HRQoL post-stroke [7, 14]. While the above studies link PSD to functional outcomes postischemic or general stroke; studies of this relationship postSAH are few, as are those examining post-SAH anxiety.

This goals of this study were to (1) describes PSD, PSA, and functional outcomes across the first year post-SAH, (2) to compares mood and functional outcomes of SAH at 6 and 12-months post-SAH to those of a group of age, gender and ethnicity matched stroke-free controls; and (3) to explore the relationship of demographic (e.g., age, gender), SAH characteristics (e.g., severity, surgical intervention), and concurrent mood with 12-month HRQoL outcomes. The sample was sources from a population-based incidence and outcomes study, the Auckland Regional Community Outcomes of Stroke study (ARCOS-IV).

Methods

Potential SAH participants included all hospitalised and nonhospitalised adult patients in the Auckland region during the 12-months from February 28, 2011 to March 1st 2012. Of 86 SAH cases located, 14(16%) died prior to notification. Of the remaining 72, 31 cases met inclusion criteria (i.e., ≥16 years, resident in Auckland region, gave consent to followup). One participant was lost to follow-up. Of the 30 SAH participants 9(30%) had experienced previous stroke. Most SAH participants had undergone surgical clipping (57%, n=17), compared to endovascular coiling (27%, n=8). Neither procedure was recorded for 5(17%) participants.

Sensitivity analyses compared the SAH sample (n = 30) with SAH survivors who did not participate (n=42). The groups did not differ significantly in terms of age, gender, or stroke severity (Glasgow Coma Scale; p>0.05), they did differ in ethnicity (χ2 (1)=6.58, p=.01), with more participants selfidentifying as European.

Control participants were recruited from the Auckland region and matched to the SAH sample on age (within 2 years), gender and ethnicity. Individuals were excluded if they had another neurological condition or known cognitive disability. One control participant could not be found to match a SAH participant, thus there were 29 control participants.

Measures

Psychological measures were administered at baseline (within 2-weeks of SAH), 28-days, 6- and 12-month post-SAH. Control participants were assessed once.

Mood was assessed using the Hospital Anxiety and Depression Scale (HADS[16]) and General Health Questionnaire 28 (GHQ-28[17]). The HADS has 14 items with seven items each for anxiety and depression (e.g., “I feel tense or wound up”), excluding somatic symptoms which could be endorsed due to physical rather than psychological state[16]. Each item has four possible responses (e.g., “0=Not at all”, “1=From time to time, occasionally”, “2=A lot of the time”, “3=Most of the time”). Individuals are asked how they have felt in the past week. Subscale scores may indicating normal(0-7), mild(8-10), moderate(11-14), or severe(15-21) anxiety or depression. The GHQ-28 has 28 items across four subscales: somatic symptoms, anxiety and insomnia, social dysfunction, and severe depression. Each item has four possible responses (e.g., 0=Not at all, 1=No more than usual, 2=Rather more than usual, 3=Much more than usual). Participants indicate if their psychological health has differed from usual over the past few weeks. Total scores range from 0 to 84 with high scores indicating poorer health and wellbeing. A cut-off score of 24 is used to indicate psychological disorder[17, 18].

The Modified Rankin Scale(mRS[19]) evaluates disability post-stroke[20] across 7 categories ranging from grade 0=”no symptoms” at all, to 5=”severe disability”, with grade 6=”death”. Stroke research suggests good outcome be defined as mRS ≤2, and poor outcome as ≥3[21].

The Barthel Index(BI[22]) assesses performance on ten activities of daily living associated with personal care and mobility. A maximum score of 100 indicates full independence; whilst 0 indicates a bed ridden state. Research suggests that the BI cut-off score be determined in relation to mRS cut-off score used (e.g., if ‘good’ on mRS≤2, BI≥90 is appropriate[23]).

The Short Form 36(SF-36[24]) is the most widely used measure of HRQoL[25]. It comprises 36 multiple choice items in eight areas of HRQoL: physical functioning(PH); role limitations due to physical health problems(RP); social functioning(SF); bodily pain(BP); general mental health(MH); role limitations due to emotional health(RE); vitality, energy and fatigue(VT); and general health perceptions(GH). There are a variety of response formats (e.g., yes/no; three to six category responses). The SF36 also yields two summary scores; the Mental Component Summary(MCS) score, derived from the SF, VT, RE and MH scales, and the Physical Component Summary(PCS) score, derived from the PH, RP, BP and GH scales. These summary scores have a mean of 50 and SD of 10. Scale and summary scores >1 SD below the mean indicate poor HRQoL[26]. 

Procedure

Ethical approval was obtained from the Northern X Regional Ethics Committee and University of Auckland Human Participants Ethics Committee. SAH-cases were drawn from the Auckland Region Community Stroke(ARCOS-IV) study, a prospective population-based stroke incidence and outcomes study in Auckland, New Zealand[27].

The control group included healthy participants from the general community residing in the Auckland region who were matched to the SAH group on age, gender and ethnicity. Potential controls were recruited via posted advertisement in community centres, churches, and medical service cites throughout the Auckland region. Potential control participants were matched to SAH participants and checked for exclusion criteria. All assessments for both groups were completed by trained research nurses, taking approximately 90 minutes at the participant’s usual place of residence.

Results

Table 1 summarises sample characteristics of the SAH and control groups. The groups did not differ significantly across the demographic characteristics.

Table 1. Demographic characteristics.

Overall performance of SAH group

Table 2 presents performance of the SAH groups across outcomes at each assessment. All group means were within the “normal” rang (≤7) on HADS subscales at each assessment. The mean SAH-group GHQ-28 exceeded the cut-off at 28-days, suggesting poor psychological wellbeing.GHQ-28 scores fell below cut-off level at all other assessments. The SAH group also had good disability outcomes (mRS≤2; BI≥90) at each assessment.

Table 2. Performance of SAH and control groups and group comparisons across measures.

Table 3 presents the proportion of SAH group scores at 6- and 12-months and control group scores that exceeded cut-offs across measures. As seen in table 3, on the HADS post-SAH anxiety was found in 39% of participants at 6-months and 32% at 12-months; whilst depression was recorded in 18% and 16% of SAH-survivors, respectively. On the GHQ-28 36% of participants had total scores indicating distress at both 6 and 12 months.

The proportion of SAH survivors at 6 and 12 months with poor functional outcomes (BI and MRS) was relatively small, remaining below 10%. In terms of HRQoL, the proportion meeting or exceeding cut-offs for poor physical and mental function was low at 6 months (4.35% and 13.04%, respectively), with the proportions increasing to 12 months (24% and 20%, respectively).

Table 3. Proportion of SAH and control group scores exceeding cut-offs across mood and functional measures.

Comparison of SAH group to Controls

As seen in Table 2, at 6-months the SAH group scored significantly higher than controls on both the HADS and GHQ28. At 12-months SAH participants continued to produce significantly higher scores on HADS depression and GHQ28 somatic symptoms subscales. In regards to proportions exceeding HADS and GHQ-28 cut-offs for psychological difficulties, a significantly greater proportions of SAH participants produced scores exceeding cut-offs on the HADS and GHQ-28 at 6- and 12-months as compared to controls; with proportion of SAH participants scoring above cut-offs being similar at 6- and 12-months.

At 6- and 12-months the SAH group was significantly more disabled on mRS than controls. However, BI scores did not differ significantly between the groups at either 6- or 12-months. The SAH group scored significantly lower than controls on all SF-36 scales except the GH scale at 6-months. At 12-months, the SAH group scored significantly worse than controls on all SF-36 summary scores and scales.

A small proportion of SAH participants had poor disability outcomes. However, more SAH group scores at 6- and 12-months had poor HRQoL on SF-36 summary scores and scales. While <5% of controls had poor HRQoL on RP, VT, SF and RE scales only; SAH group proportions were significantly higher on the MCS, and all SF-36 scales at 6- and 12-months.

Table 4. Within-subject change over time for SAH participants’ mood and functional outcomes.

At 12-months, significantly more SAH participants had poor HRQoL across all SF-36 scores.

Change over time

Table 4 shows SAH-group change over time across measures. From 28-days to 6-months, HADS total and depression scores reduced significantly over time, as did GHQ-28 somatic symptoms and social dysfunction. HADS anxiety and GHQ28 total scores did not change significantly. No significant changes were found for mood from 6- to 12-months post-SAH.

Table 5. Correlations between mood and HRQoL at 12-months.

Disability (mRS and BI) reduced significantly from 28-days to 6-months, but did not change significantly from 6- to 12-months. On the SF-36 only PCS improved significantly from 28-days to 6-months, as did PH and RP scales. There were no significant HRQoL changes from 6- to 12-months.

Relationships to 12-month HRQoL

In the following analysis, due to small group size, intervention was dichotomized into clipping versus coiling, with the 5 participants who underwent neither being excluded. Age at time of SAH, ethnicity, education and SAH severity were not significantly related to 12-month HRQoL(p>0.05). Females had significantly lower HRQoL BP scores than males at 12-months(F[1,23]=5.22, p=0.03). SAH survivors who underwent clipping produced significantly lower PCS (F[1,23]=9.54, p=0.01), and MCS summary scores (F[1,23]=4.67, p=0.04), and PH(F[1,23]=6.12, p=0.02), RP(F[1,23]=5.41, p=0.03), BP (F[1,23]=6.22, p=0.02), GH(F[1,23]=7.29, p=0.01) and VT(F[1,23]=6.92, p=0.02) subscale scores at 12-months compared to those who underwent coiling.

Coiling was not significantly related to most HRQoL domains(p>0.05), with the exception of VT(F[1,23]=4.57, p=0.04) with those undergoing coiling scoring significantly better at 12-months than those who underwent clipping.

SAH survivors with previous stroke scored significantly worse on the MCS (F[1,23]=5.30, p=0.03) and contributing domain scores (i.e., VT:F[1,23]=5.32, p=0.03; SF:F[1,23]=5.30, p=0.03; MH:F[1,23]=4.62, p=0.04), at 12-months compared to those who no previous stroke. Previous stroke was also significantly related to a lower PH domain score(F[1,23]=11.07, p=0.00).

Table 5 presents correlations between 12-month psychological and functional outcomes. Due to the large number of correlations p

Discussion

Overall performance

Consistent with the literature[3], while both SAH and control groups averaged “normal” psychological outcomes, SAH survivors had significantly more depression, somatic symptoms, and overall distress than controls at 6- and 12-months post-SAH. A significantly larger proportion of SAH participants also reported anxiety, depression, and overall emotional distress at these time points- indeed 36% of SAH survivors reported poor overall psychological wellbeing (GHQ28) at 12-month which is consistent with other populationbased SAH studies[28].

The proportion of SAH participants reporting clinical range depression here (18% and 16% at 6- and 12-months, respectively) is at the lower end of the range in the literature[6, 12, 17], likely due to different sampling and measures used[11]. That SAH participants reported significantly more depressive symptoms than controls on HADS but not GHQ-28 is likely as HADS assesses general depressive symptomatology, while GHQ-28 reflects more severe hopelessness, self-harm, and suicidal ideation. Similar findings are reported for late outcomes post-SAH[29].

SAH participants did not differ significantly from controls on mean HADS anxiety despite previous research demonstrating anxiety is common post-SAH[6, 8]. However, SAH participants were significantly more likely to report anxiety in the clinical range at 6- and 12-months than controls, demonstrating that average score comparisons may mask between-group clinical differences- twice as many SAH participants were classified anxious compared to depressed at 6- and 12-months (HADS). The proportion of SAH participants experiencing clinical range anxiety in this study was within the upper end of the range reported in the literature [3, 6, 8].

The SAH group had ‘good’ disability outcomes, but were significantly more disabled than controls. While the literature is reasonably conclusive that stroke and SAH survivors experience considerable disability and handicap compared to control samples[30, 31], our findings are consistent with a comprehensive review[6] where only 4-12% of SAH survivors experienced disability. 

The current study suggests SAH survivors had significantly reduced HRQoL and were significantly more likely to report HRQoL in the impaired range across all domains at 6- and 12-months compared to controls. Hackett and Anderson[28] found SAH survivors reported significantly reduced HRQoL at 12-months in role limitations due to physical functioning only. Our findings are more comparable to others[26], who concluded that at least 20% of their SAH-sample was impaired on each HRQoL domain. While Hackett and Anderson’s[28] sample was population-based, comparison to population norms rather than matched controls likely contributed to differing results.

Change over time

Though the SAH group had poorer psychological outcomes compared to controls, significant improvements were evident from 28-days to 6-months post-SAH. Though the literature is sparse, generally improved psychological functioning throughout the first 12-months is reported[3, 7]. Consistent with the literature the SAH group’s anxiety outcomes did not change significantly over time[3]. This is concerning as many SAH participants reported anxiety in the clinical range. 

Significantly improved HRQoL in the year post-SAH has been documented using a hospital-based sample[32]. However, stable or even deteriorating HRQoL in specific domains (e.g., recreational activities, energy) has been reported in the first 12-months post-SAH[6]. This is more consistent with the current findings, where most HRQoL outcomes did not change. Hop and colleagues[33] report similar findings post-SAH, with physical functioning and related role limitations remaining significantly impaired.

Relationships to functional outcomes

Our findings are consistent with the literature with age, gender, ethnicity and education not significantly related to 12-month HRQoL post-SAH in this study[34]. Those who underwent clipping had significantly worse physical HRQoL outcomes 12-months post-SAH than those who underwent coiling; while undergoing coiling was also associated with significantly better vitality than undergoing clipping in the current study. Research demonstrates an association between clipping and reduced disability [35], though using hospital based selected samples (e.g., aneurysmal SAH[36]). It should be noted here that the decision to clip versus coil was made based upon clinical criteria and judgement. It is therefore possible that some other factors that was present in those who underwent clipping resulted in reduced physical HRQoL. Clipping versus coiling has not previously been related to HRQoL outcomes [6]; and the findings here suggest that coiling has better HRQoL outcomes.

Prior stroke was associated with worse HRQoL outcomes postSAH, particularly emotional HRQoL. Unfortunately, previous outcome studies post-SAH use first-ever stroke samples[28] or have not examined this relationship[7]. In this study psychological outcomes were significantly related to HRQoL at 12-months post-SAH.

Limitations and Strengths

Though population-based the sample was small, and differing from the population with fewer non-Europeans. Strengths of the study include its population-based sample, comprehensive assessment, inclusion of matched controls, and examination of clinical cut-offs in addition to more typical mean comparisons.

Conclusions

The findings indicated that SAH who had a previous stroke and/or underwent surgical clipping during acute SAH intervention had worse emotional and physical HRQoL outcomes, respectively, compared those who had not. The findings suggest psychological and HRQoL outcomes should be repeatedly assessed and referred for services as part of routine follow-up and post-SAH management. 

References

1. Wiebers D, Feigin, V, Brown R. Intracerebral Haemorrhage: General Evaluation and Treatment. In: D. Wiebers VF, & R. Brown, editor. Handbook of Stroke. Philadelphia: Lippincott Williams & Wilkens.; 2006, 197-200.

2. Morris PG, Wilson JTL, Dunn L. Anxiety and depression after spontaneous subarachnoid haemorrhage. Neurosurgery. 2004, 54(1): 47-54.

3. Powell J, Kitchen N, Heslin J, Greenwood R. Psychosocial outcomes at three and nine months after good neurological recovery from aneurismal subarachnoid haemorrhage: Predictors and prognosis. J Neurol Neurosurg Psychiatry. 2002, 72(6): 772-781.

4. Germanò A, Caruso G, Caffo M, Cacciola F, Belvedere M et al. Does subarachnoid blood extravasation per se induce long-term neuropsychological and cognitive alterations? Acta Neurochirurgica. 1998, 140(8): 805-812.

5. Fontanella M, Perozzo P, Ursone R, Garbossa D, Bergui M. Neuropsychological assessment after microsurgical clipping or endovascular treatment for anterior communicating artery aneurysm. Acta Neurochirurgica. 2003,145(10): 867-872.

6. Al-Khindi T, Macdonald L, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid haemorrhage. Stroke. 2010, 41(8): e519-536.

7. Kreiter KT, Rosengart AJ, Claassen J, Fitzsimmons BF, Peery S et al. Depressed mood and quality of life after subarachnoid haemorrhage. J Neurol Sci. 2013, 335(1-2): 64-71.

8. Passier PE, Visser-Meily JM, van Zandvoort MJ, Post MW, Rinkel GJ et al . Prevalence and determinants of cognitive complaints after aneurysmal subarachnoid haemorrhage. Cerebrovasc Dis. 2010, 29(6): 557-563.

9. Hillis A, Anderson N, Sampath P, Rigamonti D. Cognitive impairments after surgical repair of ruptured and unruptured aneurysms. J Neurol Neurosurg Psychiatry. 2000, 69(5): 608- 615.

10. Hackett ML, Yapa C, Parag V, Anderson CS. Frequency of depression after stroke: A systematic review of observational studies. Stroke 2005, 36(6): 1330-1340.

11. Herrmann N, Black SE, Lawrence J, Szekely C, Szalai JP. The Sunnybrook Stroke Study: A prospective study of depressive symptoms and functional outcome. Stroke. 1998, 29(3): 618- 624.

12. Brodaty H, Withall A, Sachdev PS. Rates of depression at 3 and 15 months poststroke and their relationship with cognitive decline: The Sydney Stroke Study. Am J Geriatr Psychiatry. 2007, 15(6): 477-486.

13. Passier PE, Visser-Meily JM, Rinkel GJ, Lindeman E, Post MW. Determinants of health-related quality of life after aneurysmal subarachnoid haemorrhage: A systematic review. Qual Life Res. 2013, 22(5): 1027-1043.

14. Robinson RG. Poststroke depression: Prevalence, diagnosis, treatment, and disease progression. Biol Psychiatry. 2003, 54(3): 376-387.

15. West R, Hill K, Hewison J, Knapp P, House A. Psychological disorders after stroke are an important influence on functional outcomes: A prospective cohort study. Stroke. 2010, 41(8): 1723-1727.

16. Zigmond AS, Snaith RP. The Hospital Anxiety and Depression Scale. 67(6): 361-370. Acta Psychiatrica Scandinavica. 1983, 67: 361-370.

17. Goldberg P. Manual of the General Health Questionnaire.: NFER-Nelson: Windsor Berks; 1978.

18. Noorbala A, Bagheri Yazdi, Mohammad K. The validation of General Health Questionnaire-28 as a psychiatric screening tool. Hakim Research Journal. 2009,11(4): 47-53.

19. Bamford J, Sandercock PAG, Warlow CP, Slattery J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke. 1988, 19(5): 604-607.

20. Banks J, Marotta CA. Outcomes validity and reliability of the modified Rankin scale: implications for stroke clinical trials: a literature review and synthesis. Stroke. 2007, 38(3): 1091- 1096.

21. Sulter G, Steen C, De Keyser J. Use of the Barthel Index and Modified Rankin Scale in acute stroke trials. Stroke. 1999, 30: 1538-1541.

22. Granger C, Dewis L, Peters N, Sherwood C, Barrett J. Stroke rehabilitation: Analysis of repeated Barthel Index measures. Arch Phys Med Rehabil. 1979, 60(1): 14-17.

23. Uyttenboogaart M, Stewart RE, Vroomen PC, De Keyser J, Luijckx GJ. Optimising cutoff scores for the Barthel Index and the Modified Rankin Scale for defining outcome in acute stroke trials. Stroke. 2005, 36(9): 1984-1987.

24. Ware J, Kosinski M, Keller SD. SF-36 Physical and Mental Health Summary Scales: A Users Manual. 2nd ed. Boston, Mass: The Health Institute, New England Medical Centre; 1994.

25. de Haan EH, Nys GM, Van Zandvoort MJ. Cognitive function following stroke and vascular cognitive impairment. Curr Opin Neurol. 2006, 19(6): 559-564.

26. Katati MJ, Ramajo SS, Pérez-García M, Jofré MSM, Lopez VR et al. Description of quality of life and its predictors in patients with aneurysmal subarachnoid haemorrhage. Cerebrovasc Dis. 2007, 24(1): 66-73.

27. Krishnamurthi R, Jones A, Barber P, Barker-Collo S, McPherson K et al. Methodology of a population-based stroke and TIA incidence and outcomes study: the Auckland Regional Community Stroke Study (ARCOS IV) 2011-2012. Int J Stroke. 2014, 9(1): 140-147.

28. Hackett M, Anderson, CS. Health outcomes 1 year after subarachnoid hemorrhage: An international population-based study. The Australian Cooperative Research on Subarachnoid Hemorrhage Study Group. Neurology. 2000, 55(5): 658-662.

29. Chahal N, Barker-Collo SL, Feigin V. Cognitive and functional outcomes of 5-year subarachnoid haemorrhage survivors: Comparison to matched healthy controls. Neuroepidemiology. 2011, 37: 31-38.

30. Barker-Collo S, Feigin, V. The impact of neuropsychological deficits on functional stroke outcomes. Neuropsychol Rev. 2006, 16: 53-64.

31. Cederfeldt M, Gosman-Hedström G, Pérez CG, Sävborg M, Tarkowski E et al. Recovery in personal care related to cognitive impairment before and after stroke – A 1-year follow-up. Acta Neurol Scand. 2010, 122(6): 430-437.

32. Mocco J, Ransom ER, Komotar RJ, Sergot PB, Ostapkovich N et al. Long-term domain specific improvement following poor grade aneurysmal subarachniod hemorrhage. J Neurol. 2006, 253(10): 1278-1284.

33. Hop JW, Rinkel GJ, Algra A, van Gijn J. Quality of life in patients and partners after aneurysmal subarachnoid haemorrhage. Stroke. 1998, 29(4): 798-804.

34. Noble AJ, Schenk T. Which variables help explain the poor health-related quality of life after subarachnoid haemorrhage? A meta-analysis. Neurosurgery. 2010, 66(4): 772-783.

35. Mortimer A, Bradford C, Steinfort B, Faulder K, Asseed N et al. Short term outcomes following clipping and coiling of ruptured intracranial aneurysms: Does some of the benefit of coiling stem from less procedural impact on deranged physiology at presentation? J Neurointerv Surg. 2016. 8(2): 145-151.

36. Proust F, Martinaud O, Gérardin E, Derrey S, Levéque S et al. Quality of life and brain damage after microsurgical clip occlusion or endovascular coil embolization for ruptured anterior communicating artery aneurysms: neuropsychological assessment. J Neurosurg. 2009, 110(1): 19-29.