Generic placeholder image

Current Neurovascular Research

Editor-in-Chief

ISSN (Print): 1567-2026
ISSN (Online): 1875-5739

Research Article

Association of Rebleeding and Delayed Cerebral Ischemia with Long-term Mortality Among 1-year Survivors After Aneurysmal Subarachnoid Hemorrhage

Author(s): Xing Wang, Yu Zhang, Weelic Chong, Yang Hai, Peng Wang, Haidong Deng, Chao You and Fang Fang*

Volume 19, Issue 3, 2022

Published on: 07 October, 2022

Page: [282 - 292] Pages: 11

DOI: 10.2174/1567202619666220822105510

Price: $65

Open Access Journals Promotions 2
conference banner
Abstract

Background and Objective: The potential impact of rebleeding and Delayed Cerebral Ischemia (DCI) on long-term survival in patients with aneurysmal subarachnoid hemorrhage (aSAH) remained unclear. This study aimed to investigate whether DCI and rebleeding increase the risk of long-term all-cause mortality in patients with aSAH who survived the follow-up period of one year.

Methods: We retrospectively collected data on patients with atraumatic aSAH who were still alive 12 months after aSAH occurrence between December 2013 and June 2019 from the electronic health system. Patients were then classified by the occurrence of rebleeding or DCI during hospitalization. Death records were obtained from an administrative database, the Chinese Household Registration Administration System, until April 20, 2021. Multivariable Cox proportional hazards models were used to compare overall survival in different groups. Sensitivity analysis was performed with propensity-score matching (PSM).

Results: A total of 2,607 patients were alive one year after aSAH. The crude annual death rate from any cause among patients who had rebleeding (7.2 per 100 person-years) and patients who had DCI (3.7 per 100 person-years) during hospitalization was higher than that of patients with neither event (2.1 per 100 person-years). Multivariate analysis showed that rebleeding is an independent risk factor for long-term mortality (adjusted hazard ratio (aHR), 2.37; 95% confidence interval (CI), 1.47- 3.81). DCI was an independent prognostic factor of poorer overall survival (aHR, 2.09; 95% CI, 1.54-2.84).

Conclusion: Amongst patients alive one year after aSAH, rebleeding and DCI during hospitalization were independently associated with higher rates of long-term mortality.

Keywords: Aneurysmal subarachnoid hemorrhage, rebleeding, delayed cerebral ischemia, mortality, intracranial aneurysm, survival analysis.

[1]
Stegmayr B, Eriksson M, Asplund K. Declining mortality from subarachnoid hemorrhage: Changes in incidence and case fatality from 1985 through 2000. Stroke 2004; 35(9): 2059-63.
[http://dx.doi.org/10.1161/01.STR.0000138451.07853.b6] [PMID: 15272133]
[2]
Truelsen T, Bonita R, Duncan J, Anderson NE, Mee E. Changes in subarachnoid hemorrhage mortality, incidence, and case fatality in New Zealand between 1981-1983 and 1991-1993. Stroke 1998; 29(11): 2298-303.
[http://dx.doi.org/10.1161/01.STR.29.11.2298] [PMID: 9804637]
[3]
Shea AM, Reed SD, Curtis LH, Alexander MJ, Villani JJ, Schulman KA. Characteristics of nontraumatic subarachnoid hemorrhage in the United States in 2003. Neurosurgery 2007; 61(6): 1131-8.
[http://dx.doi.org/10.1227/01.neu.0000306090.30517.ae] [PMID: 18162891]
[4]
Nieuwkamp DJ, Setz LE, Algra A, Linn FHH, de Rooij NK, Rinkel GJE. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: A meta-analysis. Lancet Neurol 2009; 8(7): 635-42.
[http://dx.doi.org/10.1016/S1474-4422(09)70126-7] [PMID: 19501022]
[5]
Broderick JP, Brott TG, Duldner JE, Tomsick T, Leach A. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 1994; 25(7): 1342-7.
[http://dx.doi.org/10.1161/01.STR.25.7.1342] [PMID: 8023347]
[6]
Solenski NJ, Haley ECJ Jr, Kassell NF, et al. Medical complications of aneurysmal subarachnoid hemorrhage. Crit Care Med 1995; 23(6): 1007-17.
[http://dx.doi.org/10.1097/00003246-199506000-00004] [PMID: 7774210]
[7]
van Donkelaar CE, Bakker NA, Veeger NJGM, et al. Predictive factors for rebleeding after aneurysmal subarachnoid hemorrhage. Stroke 2015; 46(8): 2100-6.
[http://dx.doi.org/10.1161/STROKEAHA.115.010037] [PMID: 26069261]
[8]
Larsen CC, Astrup J. Rebleeding after aneurysmal subarachnoid hemorrhage: A literature review. World Neurosurg 2013; 79(2): 307-12.
[http://dx.doi.org/10.1016/j.wneu.2012.06.023] [PMID: 22722033]
[9]
Tanno Y, Homma M, Oinuma M, Kodama N, Ymamoto T. Rebleeding from ruptured intracranial aneurysms in North Eastern Province of Japan. A cooperative study. J Neurol Sci 2007; 258(1-2): 11-6.
[http://dx.doi.org/10.1016/j.jns.2007.01.074] [PMID: 17512010]
[10]
Zhao B, fan Y, Xiong Y, et al. Aneurysm rebleeding after poor-grade aneurysmal subarachnoid hemorrhage: Predictors and impact on clinical outcomes. J Neurol Sci 2016; 371(15): 62-6.
[http://dx.doi.org/10.1016/j.jns.2016.10.020] [PMID: 27871451]
[11]
Lord AS, Fernandez L, Schmidt JM, et al. Effect of rebleeding on the course and incidence of vasospasm after subarachnoid hemorrhage. Neurology 2012; 78(1): 31-7.
[http://dx.doi.org/10.1212/WNL.0b013e31823ed0a4] [PMID: 22170890]
[12]
Naidech AM, Janjua N, Kreiter KT, et al. Predictors and impact of aneurysm rebleeding after subarachnoid hemorrhage. Arch Neurol 2005; 62(3): 410-6.
[http://dx.doi.org/10.1001/archneur.62.3.410] [PMID: 15767506]
[13]
Williamson CA, Sheehan KM, Tipirneni R, et al. The association between spontaneous hyperventilation, delayed cerebral ischemia, and poor neurological outcome in patients with subarachnoid hemorrhage. Neurocrit Care 2015; 23(3): 330-8.
[http://dx.doi.org/10.1007/s12028-015-0138-5] [PMID: 25846710]
[14]
Roos YBWEM, de Haan RJ, Beenen LF, Groen RJ, Albrecht KW, Vermeulen M. Complications and outcome in patients with aneurysmal subarachnoid haemorrhage: A prospective hospital based cohort study in The Netherlands. J Neurol Neurosurg Psychiatry 2000; 68(3): 337-41.
[http://dx.doi.org/10.1136/jnnp.68.3.337] [PMID: 10675216]
[15]
Huhtakangas J, Lehto H, Seppä K, et al. Long-term excess mortality after aneurysmal subarachnoid hemorrhage. Stroke 2015; 46(7): 1813-8.
[http://dx.doi.org/10.1161/STROKEAHA.115.009288] [PMID: 26045602]
[16]
Rinkel GJE, Algra A. Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol 2011; 10(4): 349-56.
[http://dx.doi.org/10.1016/S1474-4422(11)70017-5] [PMID: 21435599]
[17]
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for reporting observational studies. Lancet 2007; 370(9596): 1453-7.
[http://dx.doi.org/10.1016/S0140-6736(07)61602-X] [PMID: 18064739]
[18]
Vergouwen MDI, Vermeulen M, van Gijn J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: Proposal of a multidisciplinary research group. Stroke 2010; 41(10): 2391-5.
[http://dx.doi.org/10.1161/STROKEAHA.110.589275] [PMID: 20798370]
[19]
Geraghty JR, Testai FD. Delayed cerebral ischemia after subarachnoid hemorrhage: Beyond vasospasm and towards a multifactorial pathophysiology. Curr Atheroscler Rep 2017; 19(12): 50.
[http://dx.doi.org/10.1007/s11883-017-0690-x] [PMID: 29063300]
[20]
Pegoli M, Mandrekar J, Rabinstein AA, Lanzino G. Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 2015; 122(2): 414-8.
[http://dx.doi.org/10.3171/2014.10.JNS14290] [PMID: 25495745]
[21]
Rosengart AJ, Schultheiss KE, Tolentino J, Macdonald RL. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 2007; 38(8): 2315-21.
[http://dx.doi.org/10.1161/STROKEAHA.107.484360] [PMID: 17569871]
[22]
Marbacher S, Remonda L, Soleman J, et al. Outcome after in-hospital rebleeding of rupture of intracranial aneurysms. J Neurol Surg A Cent Eur Neurosurg 2016; 77(3): 207-21.
[http://dx.doi.org/10.1055/s-0035-1570007] [PMID: 26807617]
[23]
Darkwah Oppong M, Gümüs M, Pierscianek D, et al. Aneurysm rebleeding before therapy: A predictable disaster? J Neurosurg 2019; 131(5): 1473-80.
[http://dx.doi.org/10.3171/2018.7.JNS181119] [PMID: 30952125]
[24]
Horie N, Sato S, Kaminogo M, et al. Impact of perioperative aneurysm rebleeding after subarachnoid hemorrhage. J Neurosurg 2020; 133(5): 1401-10.
[http://dx.doi.org/10.3171/2019.6.JNS19704] [PMID: 31518984]
[25]
Eagles ME, Tso MK, Macdonald RL. Cognitive impairment, functional outcome, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. World Neurosurg 2019; 124: e558-62.
[http://dx.doi.org/10.1016/j.wneu.2018.12.152] [PMID: 30639483]
[26]
Al-Khindi T, Macdonald RL, Schweizer TA. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 2010; 41(8): e519-36.
[http://dx.doi.org/10.1161/STROKEAHA.110.581975] [PMID: 20595669]
[27]
Benke T, Köylü B, Delazer M, Trinka E, Kemmler G. Cholinergic treatment of amnesia following basal forebrain lesion due to aneurysm rupture - an open-label pilot study. Eur J Neurol 2005; 12(10): 791-6.
[http://dx.doi.org/10.1111/j.1468-1331.2005.01063.x] [PMID: 16190917]
[28]
Wong GKC, Lam SW, Wong A, et al. Early MoCA-assessed cognitive impairment after aneurysmal subarachnoid hemorrhage and relationship to 1-year functional outcome. Transl Stroke Res 2014; 5(2): 286-91.
[http://dx.doi.org/10.1007/s12975-013-0284-z] [PMID: 24323708]
[29]
Gerner ST, Reichl J, Custal C, et al. Long-term complications and influence on outcome in patients surviving spontaneous subarachnoid hemorrhage. Cerebrovasc Dis 2020; 49(3): 307-15.
[http://dx.doi.org/10.1159/000508577] [PMID: 32623428]
[30]
Rücker V, Heuschmann PU, O’Flaherty M, et al. Twenty-year time trends in long-term case-fatality and recurrence rates after ischemic stroke stratified by etiology. Stroke 2020; 51(9): 2778-85.
[http://dx.doi.org/10.1161/STROKEAHA.120.029972] [PMID: 32811383]
[31]
Hill MD, Silver FL, Austin PC, Tu JV. Rate of stroke recurrence in patients with primary intracerebral hemorrhage. Stroke 2000; 31(1): 123-7.
[http://dx.doi.org/10.1161/01.STR.31.1.123] [PMID: 10625726]
[32]
Connolly ES Jr, Rabinstein AA, Carhuapoma JR, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: A guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke 2012; 43(6): 1711-37.
[http://dx.doi.org/10.1161/STR.0b013e3182587839] [PMID: 22556195]
[33]
Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G. European stroke organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis 2013; 35(2): 93-112.
[http://dx.doi.org/10.1159/000346087] [PMID: 23406828]
[34]
Baharoglu MI, Germans MR, Rinkel GJE, et al. Antifibrinolytic therapy for aneurysmal subarachnoid haemorrhage. Cochrane Libr 2013; 2013(9): CD001245.
[http://dx.doi.org/10.1002/14651858.CD001245.pub2] [PMID: 23990381]
[35]
Post R, Germans MR, Coert BA, Rinkel GJE, Vandertop WP, Verbaan D. Update of the ULtra-early TRranexamic Acid after Subarachnoid Hemorrhage (ULTRA) trial: Statistical analysis plan. Trials 2020; 21(1): 199.
[http://dx.doi.org/10.1186/s13063-020-4118-5] [PMID: 32070395]
[36]
Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet 2017; 389(10069): 655-66.
[http://dx.doi.org/10.1016/S0140-6736(16)30668-7] [PMID: 27637674]
[37]
Boogaarts HD, van Lieshout JH, van Amerongen MJ, et al. Aneurysm diameter as a risk factor for pretreatment rebleeding: A meta-analysis. J Neurosurg 2015; 122(4): 921-8.
[http://dx.doi.org/10.3171/2014.12.JNS14931] [PMID: 25658785]
[38]
Yang L, Li M, Zhan Y, et al. The impact of ischemic stroke on gray and white matter injury correlated with motor and cognitive impairments in permanent MCAO Rats: A multimodal MRI-based study. Front Neurol 2022; 13: 834329.
[http://dx.doi.org/10.3389/fneur.2022.834329] [PMID: 35309583]
[39]
Tang T, Hu L, Liu Y, et al. Sex-associated differences in neurovascular dysfunction during ischemic stroke. Front Mol Neurosci 2022; 15: 860959.
[http://dx.doi.org/10.3389/fnmol.2022.860959] [PMID: 35431804]
[40]
Gasbarrino K, Di Iorio D, Daskalopoulou SS. Importance of sex and gender in ischaemic stroke and carotid atherosclerotic disease. Eur Heart J 2022; 43(6): 460-73.
[http://dx.doi.org/10.1093/eurheartj/ehab756] [PMID: 34849703]
[41]
van Dam-Nolen DHK, van Egmond NCM, Dilba K, et al. Sex differences in plaque composition and morphology among symptomatic patients with mild-to-moderate carotid artery stenosis. Stroke 2022; 53(2): 370-8.
[http://dx.doi.org/10.1161/STROKEAHA.121.036564] [PMID: 34983237]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy