Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage

doi:10.1016/S1474-4422(11)70017-5

The Lancet Neurology

Volume 10, Issue 4, April 2011, Pages 349-356

https://doi.org/10.1016/S1474-4422(11)70017-5 Get rights and content

Summary

More and more patients survive aneurysmal subarachnoid haemorrhage (aSAH), with case fatality decreasing by 17% in absolute terms over the past three decades and incidence remaining relatively stable at nine per 100 000 patient-years. The mean age at which aSAH occurs is reasonably young at 55 years, and people of this age in the general population have a good life expectancy. However, there are few data for life expectancy after aSAH, and the risks of late recurrent aSAH and other vascular diseases are unclear. The course of associated long-term physical and cognitive deficits after aSAH is not well established, leading to questions about potential outcomes to quality of life and working capacity, as well as best clinical practices.

Introduction

Subarachnoid haemorrhage from a ruptured aneurysm is a subset of stroke that occurs at a relatively young age compared with other stroke subtypes. The incidence is around nine cases per 100 000 person-years, which has decreased little during the past four decades.¹ However, the chance of a patient surviving an aneurysmal subarachnoid haemorrhage (aSAH) has increased by 17% over the past three decades and is around 65%.2, 3, 4, 5 The reduction in fatality is remarkable because about 12% of patients who have a subarachnoid haemorrhage die immediately.⁶ Thus, a third of those who die from subarachnoid haemorrhage are not admitted to hospital and do not benefit from improved diagnostics and treatment methods. Most patients who survive the initial weeks are functionally independent.³ As the mean age of occurrence is around 55 years, the question is whether patients who survive an aSAH have an equivalent life expectancy to that of healthy people of this age in the general population, which in the Netherlands is around another 30 years.⁷

Because aneurysms are not congenital as was previously assumed but instead develop during life,⁸ patients who survive the initial weeks might be at risk of development of new aneurysms and new episodes of aSAH. Furthermore, because hypertension and smoking are major risk factors for aSAH,⁹ patients who survive the initial weeks might have a higher than normal risk of cardiovascular diseases. Equally, functional independence is not the only important outcome: many patients who are functionally independent have cognitive dysfunction in the initial phase after aSAH. Here, we review data for life expectancy and the risk of new episodes of aSAH and other cardiovascular diseases for patients who survived an aSAH. We also describe the long-term course of residual physical and cognitive deficits, detail implications for quality of life and working capacity from an individual and societal perspective, and discuss the implications for clinical practice and future research.

Section snippets

Risk of late recurrent aSAH, death, and cardiovascular diseases

Until the end of the 20th century, the prevailing perception of outcomes of patients who survived an aSAH was that the disorder was fixed by closure of the aneurysm (and verification that there were no other unruptured aneurysms). This notion has been overruled by evidence that aneurysms are not a one-off event, but rather a chronic disease. The table summarises data from long-term follow-up studies on the occurrence of new aSAHs after appropriate closure of the ruptured aneurysm that caused

Residual deficits after aSAH

Although several population-based studies have described case fatality rates of aSAH, only a few have also described the proportion of patients who regain independence for activities of daily life. Estimates of independence (modified Rankin scale score of 0–3 dependent on the study) varied between 36% and 55% at assessments 1–12 months after aSAH;³ however, there were too few data to establish whether this proportion changed during the preceding decades.

Clinical condition at admission is one of

Effect on society

Although aSAHs account for only 5% of strokes, their effect on society is substantial because of the young age at which they occur and the poor outcomes they lead to. In the last decades of the 20th century, the proportion of years of potential life lost from subarachnoid haemorrhage was similar to that of ischaemic stroke and intracerebral haemorrhage.⁵⁴ In the first years of the 21st century, the mean hospital charge in the USA for aSAH was more than US$65 000 per patient.⁵⁵ The total cost to

Multidisciplinary outpatient clinics

Although most patients who recover from aSAH are well informed about their event and about the type of treatment they received, a third with non-treated additional aneurysms are not aware of having one or more unsecured aneurysms.⁵⁸ Moreover, most patients interviewed about the information that they were given expressed a need for more and improved information.⁵⁹ The same study⁵⁹ also reported that in most instances the information about the aSAH was given to the patient in the absence of their

Future directions

Secondary prevention of cardiovascular diseases after clinically manifest atherosclerotic disease is broadly accepted and has, apart from recommendations to adapt lifestyle, three key principles: blood pressure reduction, lipid lowering, and antithrombotic treatment. As previously mentioned, patients have an increased risk of vascular disease after aSAH; however there are no data for effectiveness of secondary prevention. Such data are needed before secondary prevention can be implemented,

Conclusions

Previous studies13, 20, 21 have shown that life expectancy is reduced for patients who survived aSAH. These patients have a higher risk of aSAH in their remaining life than do the general population (panel), but because the absolute risk is still low, screening for new aneurysms is in general not cost effective after aSAH. Furthermore, the risk of cardiovascular diseases apart from aSAH is higher in patients who have had aSAH than it is in the general population. Consequently, life expectancy

Search strategy and selection criteria

References for this Review were retrieved from a prospectively built database of references collected between Jan 1, 2000, and Jan 19, 2011, by unrestricted PubMed searches with the terms “subarachnoid hemorrhage”, “aneurysm”, “arteriovenous malformation”, “perimesencephalic”, “subarachnoid haemorrhage”, OR “aneurysm*”. References were also identified by searching the PubMed database with the terms “hearing loss” or “deafness”; “blindness” or “loss of vision”; or “costs”, in combination

References (76)

DJ Nieuwkamp et al.
Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis
Lancet Neurol
(2009)
VL Feigin et al.
Worldwide stroke incidence and early case fatality reported in 56 population-based studies: a systematic review
Lancet Neurol
(2009)
AJ Molyneux et al.
Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up
Lancet Neurol
(2009)
P Greebe et al.
Long-term outcome of patients discharged to a nursing home after aneurysmal subarachnoid hemorrhage
Arch Phys Med Rehabil
(2010)
PM Bossuyt et al.
Screening families for intracranial aneurysms: Anxiety, perceived risk, and informed choice
Prev Med
(2005)
GJE Rinkel
Intracranial aneurysm screening: indications and advice for practice
Lancet Neurol
(2005)
NK de Rooij et al.
Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends
J Neurol Neurosurg Psychiatry
(2007)
H Koffijberg et al.
Subarachnoid haemorrhage in Sweden 1987–2002: regional incidence and case fatality rates
J Neurol Neurosurg Psychiatry
(2008)
CE Lovelock et al.
Time trends in outcome of subarachnoid hemorrhage. Population-based study and systematic review
Neurology
(2010)
J Huang et al.
The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis
Neurosurgery
(2002)

Remaining (healthy) life expectancy

GJE Rinkel et al.

Prevalence and risk of rupture of intracranial aneurysms: a systematic review

(2006)

JD Schaafsma et al.

Long-term recurrent subarachnoid hemorrhage after adequate coiling versus clipping of ruptured intracranial aneurysms

Stroke

(2009)

DS Choi et al.

Neurology

(2006)

P Bendel et al.

MR imaging of the brain 1 year after aneurysmal subarachnoid hemorrhage: randomized study comparing surgical with endovascular treatment

Radiology

(2008)

P Bendel et al.

Brain atrophy and neuropsychological outcome after treatment of ruptured anterior cerebral artery aneurysms: a voxel-based morphometric study

Neuroradiology

(2009)

Cited by (361)

Dynamic changes of systemic inflammation response index and systemic immune-inflammation index are associated with delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage
2024, Journal of Stroke and Cerebrovascular Diseases
Delayed cerebral ischemia (DCI) is a factor contributing to poor outcome of aneurysmal subarachnoid hemorrhage (aSAH). Serial inflammatory response is known to affect the occurrence of DCI. The aim of this study was to evaluate associations of dynamic changes of various inflammatory markers with occurrence of DCI after aSAH.
A total of 279 patients with interventional treatment for aSAH were enrolled, and dichotomized according to the occurrence of DCI. Various inflammatory markers, including systemic immune-inflammation index (SII), systemic inflammation response index (SIRI), and their dynamic changes were analyzed at four different time points. Receiver operating characteristic (ROC) curve analysis with area under the curve (AUC) and univariate, multivariate Cox regression analyses with hazard ratio (HR) and 95 % confidence interval (CI) were performed to identify predictors for DCI.
Differences of SII and SIRI values between DCI (+) and DCI (-) group were significantly higher at 5-7 days than at other time points (P < 0.001 and P < 0.001, respectively). SII and SIRI had higher predicting values for DCI occurrence than other inflammatory markers (AUC: 0.862, 95 % CI: 0.786–0.928; P < 0.001 and AUC: 0.851, 95 % CI: 0.769–0.913; P < 0.001, respectively). SII at 5–7 days (HR: 1.74, 95 % CI: 1.38–3.22, P = 0.020) and SIRI at 5–7 days (HR: 1.62, 95 % CI: 1.28–2.84, P = 0.035) were associated with occurrence of DCI.
Dynamic changes of SII and SII might be predictors of DCI occurrence in patients with aSAH.
Pan-immune-inflammation value predict delayed cerebral ischemia in patients with aneurysmal subarachnoid hemorrhage
2024, Journal of Clinical Neuroscience
Inflammatory reaction and immune dysregulation are known as components contributing to delayed cerebral ischemia (DCI) in patients with following aneurysmal subarachnoid hemorrhage (aSAH). The objective of this study was to investigate the role of pan-immune-inflammation value (PIV) as a novel comprehensive inflammatory marker in predicting the DCI development following aSAH. A total of 1028 participants with aSAH were enrolled. There were 296 patients with DCI and 732 patients without DCI. Various inflammatory markers were analyzed using peripheral blood sample obtained at admission. Receiver operating characteristic (ROC) analysis was performed to identify the optimal cutoff value of PIV for distinguishing DCI. Multivariate analysis was used to determine independent predictors for DCI. Mean PIV was significantly higher in the DCI (+) group than in the DCI (-) group (437.6 ± 214.7 vs 242.1 ± 154.7, P = 0.007). In ROC analysis, the optimal cutoff value of PIV was 356.7 for predicting DCI (area under the curve [AUC] 0.772, 95 % confidence interval [CI] 0.718–0.816; P < 0.001). Multivariate analysis showed that high Hunt-Hess grade (odds ratio [OR] 1.70, 95 % CI 1.38–2.22; P = 0.007), thick SAH (OR 1.82, 95 % CI 1.44–2.32; P = 0.005), and elevated PIV (≥356.7) (OR 1.42, 95 % CI 1.10–1.74; P = 0.013) were independent predictors of DCI after aSAH. PIV is a potent predictor of DCI in patients with aSAH. Elevated PIV is associated with more DCI development. Thus, PIV has predictive value for DCI development.
Health-related quality of life of patients with aneurysmal subarachnoid hemorrhage who were classified as having “good outcomes”
2024, Journal of Clinical Neuroscience
This study aimed to understand the health-related quality of life (HRQoL) of patients with aneurysmal subarachnoid hemorrhage (aSAH) classified as having “good outcomes” and determine associated sociodemographic, psychological, and clinical factors.
Participants were 86 patients with aSAH with modified Rankin Scale (mRS) scores of 0–2 in our hospital between February 2003 and April 2014. Participants completed self-report questionnaires examining sociodemographic characteristics and the following self-rating scales: the hospital anxiety and depression scale, Pittsburgh sleep quality index, and EuroQoL-5 Dimension Index (EQ-5D). Further, we retrospectively reviewed clinical data from medical records and radiologic images. Average EQ-5D scores for each variable were compared using Student’s t-test and analysis of variance. Correlations between EQ-5D and continuous variables were examined using Pearson correlation analysis. Factors associated with EQ-5D were then examined using univariate and stepwise multivariate analyses through simple and multiple regression.
The mean age of the 86 participants was 56.87 ± 10.28 years (range: 29–79 years), while the mean EQ-5D value was 0.738 ± 0.169. There were 54 women (62.8 %) and 33 men (37.2 %). The participants had depressive symptoms (30.2 %), anxiety (10.5 %), and sleep problems (51.2 %). Regarding sociodemographic variables, educational level (p = 0.017) and monthly income (p = 0.037) were positively correlated with HRQoL. Depressive symptoms (r = −0.505, p < 0.001), anxiety (r = −0.498, p < 0.001), sleep problems (r = −0.265, p = 017), and mRS (r = −0.352, p = 0.001) were negatively correlated with HRQoL. Depressive symptoms, diabetes mellitus, and past psychiatric history explained 48.8 % of the variance in HRQoL in good outcome aSAH according to stepwise multiple regression analysis.
Patients with good outcome aSAH had low EQ-5D values, which were negatively correlated with depressive symptoms, anxiety, and sleep problems. In addition, HRQoL in good outcome aSAH is associated with depressive symptoms, diabetes mellitus, and past psychiatric disease history. Depressive symptoms, anxiety, and sleep problems are frequent in patients with good outcome aSAH, and mediation of these factors may help improve HRQoL.
Role of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) in autophagy activation following subarachnoid hemorrhage
2024, Experimental Neurology
Early brain injury (EBI) refers to a severe brain injury that occurs within hours to days after subarachnoid hemorrhage (SAH). Neuronal damage in EBI is considered a key factor leading to poor prognosis. Currently, our understanding of the mechanisms of neuronal damage, such as neuronal autophagy, is still incomplete. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is a key enzyme in metabolism and plays an important role in autophagy. Based on this, this study will further explore the regulation of autophagy by GAPDH after SAH, which may provide a new treatment strategy for improving the prognosis of SAH patients.
The rat SAH model was established by endovascular puncturing, and the trend of autophagy in hippocampal neurons at different time points was discussed. Additionally, an in vitro SAH model was created using the oxygenated hemoglobin and hippocampal neuronal HT22 cell line. Through siRNA and overexpression adenovirus techniques, we further investigated the relationship between the key enzyme GAPDH and autophagy in the in vitro SAH model.
We observed significant neuronal damage in the hippocampus 24 h after SAH, and the proteomics showed significant enrichment of autophagy-related pathways at this time point. Further studies showed that the expression of LC3 and Beclin1 peaked at 24 h, and the nuclear translocation of GAPDH occurred simultaneously with SAH-induced neuronal autophagy. Our in vitro SAH model confirmed the role of GAPDH in regulating the level of autophagy in HT22 cells. Knockdown of GAPDH significantly reduced the level of autophagy, while overexpression of GAPDH increased the level of autophagy.
This study shows the trend of autophagy in hippocampal neurons after SAH, and reveals the regulatory role of GAPDH in SAH-induced autophagy. However, further studies are needed to reveal the exact mechanism of GAPDH in the nuclear translocation regulation of autophagy and validate in animal models.
Depression screening in patients with aneurysmal subarachnoid haemorrhage and their caregivers: A systematic review
2023, Australian Critical Care
Depression commonly occurs after aneurysmal subarachnoid haemorrhage (aSAH) which can negatively impact patients and their caregivers. Identification and validation of depression screening instruments specifically for patients with aSAH and their caregivers has not been performed.
The objectives of this study were to identify the common depression screening tools in patients with aSAH and their caregivers and to determine if they are validated for use in these populations.
Medical Subject Headings and keyword search terms were used in five electronic databases to identify randomised controlled, quasi-experimental and observational studies published between 1 January 2010 and 26 June 2022. Screening, data extraction and study quality assessments were conducted by two independent reviewers.
Of the 3440 identified studies, 61 met inclusion, with 2 of 61 (3%) RCTs, 2 of 61 (3%) quasi-experimental, and 57 of 61 (93%) observational studies included. The majority of studies (58/61 [95%]) reported patient-only depression screening, 1 of 61 (2%) reported both patients' and caregivers' depression screening, and 2 of 61 (3%) reported caregiver-only depression screening. Nine depression screening instruments were identified. The Beck Depression Inventory-II (BDI-II) was the most commonly used (13/59; 22%), followed by the Hospital Anxiety and Depression Scale (HADS) (12/59; 20%). In the ischaemic stroke population, the BDI-II was reported to have excellent sensitivity (0.85) and specificity (0.75); the HADS was also found to have good sensitivity (0.62) and specificity (0.83) in the ischaemic stroke population. Only two depression screening instruments for caregivers were identified: HADS and Goldberg Depression Scale. Both were found to have good sensitivity (>0.80) and specificity (>0.80) in the general population.
The BDI-II and HADS were the most commonly used depression screening instruments in patients with aSAH. Neither of these instruments has been specifically validated in an aSAH population. None of the nine depression instruments were validated for patients with aSAH. Due to an insufficient number of studies in caregivers' population, validity was unable to be determined.
Neurosurgical clipping versus endovascular coiling for patients with ruptured anterior circulation aneurysms: A systematic review and meta-analysis
2024, Neurosurgical Review

View all citing articles on Scopus

View full text

ReviewLong-term outcomes of patients with aneurysmal subarachnoid haemorrhage

Summary

Introduction

Section snippets

Risk of late recurrent aSAH, death, and cardiovascular diseases

Residual deficits after aSAH

Effect on society

Multidisciplinary outpatient clinics

Future directions

Conclusions

Search strategy and selection criteria

Lancet Neurol

Lancet Neurol

Lancet Neurol

Arch Phys Med Rehabil

Prev Med

Lancet Neurol

Incidence of subarachnoid haemorrhage: a systematic review with emphasis on region, age, gender and time trends

J Neurol Neurosurg Psychiatry

Subarachnoid haemorrhage in Sweden 1987–2002: regional incidence and case fatality rates

J Neurol Neurosurg Psychiatry

Time trends in outcome of subarachnoid hemorrhage. Population-based study and systematic review

Neurology

The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis

Neurosurgery

Remaining (healthy) life expectancy

Prevalence and risk of rupture of intracranial aneurysms: a systematic review

Stroke

Attributable risk of common and rare determinants of subarachnoid hemorrhage

Stroke

Risk of recurrent subarachnoid hemorrhage after complete obliteration of cerebral aneurysms

Stroke

Incidence of recurrent subarachnoid subarachnoid hemorrhage after clipping for ruptured intracranial aneurysms

Stroke

Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment

Stroke

Long-term recurrent subarachnoid hemorrhage after adequate coiling versus clipping of ruptured intracranial aneurysms

Stroke

Clinical and angiographic long-term follow-up of completely coiled intracranial aneurysms using endovascular technique

J Neurosurg

Epidemiology of aneurysmal subarachnoid hemorrhage in Australia and New Zealand: incidence and case fatality from the Australasian Cooperative Research on Subarachnoid Hemorrhage Study (ACROSS)

Stroke

New detected aneurysms on follow-up screening in patients with previously clipped intracranial aneurysms: comparison with DSA or CTA at time of the SAH

Stroke

Follow-up screening after subarachnoid haemorrhage: frequency and determinants of new aneurysms and enlargement of existing aneurysms

Brain

Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies

Stroke

Evidence for excess long-term mortality after treated subarachnoid hemorrhage

Stroke

Long-term mortality and vascular event risk after aneurysmal subarachnoid haemorrhage

J Neurol Neurosurg Psychiatry

Excess mortality and cardiovascular events in patients surviving subarachnoid hemorrhage: a nationwide study in Sweden

Stroke

Validation of a prognostic subarachnoid hemorrhage grading scale derived directly from the Glasgow Coma Scale

Stroke

Cognitive functioning and health-related quality of life 1 year after aneurysmal subarachnoid hemorrhage in preoperative comatose patients (Hunt and Hess Grade V patients)

Neurosurgery

Independent living following a ‘do not resuscitate’ order after subarachnoid haemorrhage

Disabil Rehabil

Global and domain-specific cognitive impairment and outcome after subarachnoid hemorrhage

Neurology

Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage

Stroke

Prevalence and determinants of cognitive complaints after aneurysmal subarachnoid hemorrhage

Cerebrovasc Dis

Cognitive outcome after aneurysmal subarachnoid hemorrhage: time course of recovery and relationship to clinical, radiological, and management parameters

Neurosurgery

Recovery of cognitive function after surgery for aneurysmal subarachnoid hemorrhage

Stroke

Health outcomes 1 year after subarachnoid hemorrhage. An international population-based study

Neurology

Improved cognitive outcomes with endovascular coiling of ruptured intracranial aneurysms: neuropsychological outcomes from the International Subarachnoid Aneurysm Trial (ISAT)

Stroke

Subarachnoid hemorrhage is followed by temporomesial volume loss: MRI volumetric study

Neurology

MR imaging of the brain 1 year after aneurysmal subarachnoid hemorrhage: randomized study comparing surgical with endovascular treatment

Radiology

Brain atrophy and neuropsychological outcome after treatment of ruptured anterior cerebral artery aneurysms: a voxel-based morphometric study

Neuroradiology

Review
Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage