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Predictive factors for pre-intervention rebleeding in aneurysmal subarachnoid haemorrhage: a systematic review and meta-analysis

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Abstract

Rebleeding before intervention is a devastating complication of aneurysmal subarachnoid haemorrhage (aSAH). It often occurs early and is associated with poor outcomes. We present a systematic review and meta-analysis to identify potential predictors of rebleeding in aSAH. A database search identified studies detailing the occurrence of pre-intervention rebleeding in aSAH, and 809 studies were screened. The association between rebleeding and a variety of demographic, clinical, and radiological factors was examined using random effects meta-analyses. Fifty-six studies totalling 33,268 patients were included. Rebleeding occurred in 3,223/33,268 patients (11.1%, 95%CI 9.4–13), with risk decreasing by approximately 0.2% per year since 1981. Systolic blood pressure (SBP) during admission was higher in patients who rebled compared with those who did not (MD 7.4 mmHg, 95%CI 2.2 – 12.7), with increased risk in cohorts with SBP > 160 mmHg (RR 2.12, 95%CI 1.35–3.34), but not SBP > 140 mmHg. WFNS Grades IV–V (RR 2.05, 95%CI 1.13–3.74) and Hunt-Hess grades III–V (RR 2.12, 95%CI 1.38–3.28) were strongly associated with rebleeding. Fisher grades IV (RR 2.24, 95%CI 1.45–3.49) and III–IV (RR 2.05, 95%CI 1.17–3.6) were also associated with an increased risk. Awareness of potential risk factors for rebleeding is important when assessing patients with aSAH to ensure timely management in high-risk cases. Increased SBP during admission, especially > 160 mmHg, poorer clinical grades, and higher radiological grades are associated with an increased risk. These results may also aid in designing future studies assessing interventions aimed at reducing the risk of rebleeding.

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Supplementary digital content is available which details the search string used to identify articles that were considered for inclusion. All extracted data is available within the full texts of referenced articles.

References

  1. Robbert M, Hoogmoed J, van Straaten HA, Coert BA, Peter Vandertop W, Verbaan D (2014) Time intervals from aneurysmal subarachnoid hemorrhage to treatment and factors contributing to delay. J Neurol 261(3):473–479. https://doi.org/10.1007/s00415-013-7218-2

    Article  PubMed  Google Scholar 

  2. Lovelock CE, Rinkel GJ, Rothwell PM (2010) Time trends in outcome of subarachnoid hemorrhage: population-based study and systematic review. Neurology 74(19):1494–1501. https://doi.org/10.1212/WNL.0b013e3181dd42b3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Steiner T, Juvela S, Unterberg A, Jung C, Forsting M, Rinkel G, European Stroke O (2013) European stroke organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovasc Dis 35(2):93–112. https://doi.org/10.1159/000346087

    Article  PubMed  Google Scholar 

  4. Sweeney K, Silver N, Javadpour M (2016) Subarachnoid haemorrhage (spontaneous aneurysmal). BMJ Clin Evid 17;2016:1213

  5. Nicholson P, O’Hare A, Power S, Looby S, Javadpour M, Thornton J, Brennan P (2019) Decreasing incidence of subarachnoid hemorrhage. J Neurointerv Surg 11(3):320–322. https://doi.org/10.1136/neurintsurg-2018-014038

    Article  PubMed  Google Scholar 

  6. Huang J, Van Gelder JM (2002) The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis. Neurosurgery 51(5):1101–1105. https://doi.org/10.1097/00006123-200211000-00001. (discussion 1105-1107)

    Article  PubMed  Google Scholar 

  7. Nieuwkamp DJ, Setz LE, Algra A, Linn FHH, de Rooij NK, Rinkel GJE (2009) Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. The Lancet Neurology 8(7):635–642. https://doi.org/10.1016/s1474-4422(09)70126-7

    Article  PubMed  Google Scholar 

  8. Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, Hoh BL, Kirkness CJ, Naidech AM, Ogilvy CS, Patel AB, Thompson BG, Vespa P, American Heart Association Stroke C, Council on Cardiovascular R, Intervention, Council on Cardiovascular N, Council on Cardiovascular S, Anesthesia, Council on Clinical C (2012) Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43(6):1711–1737. https://doi.org/10.1161/STR.0b013e3182587839

    Article  PubMed  Google Scholar 

  9. Tang C, Zhang TS, Zhou LF (2014) Risk factors for rebleeding of aneurysmal subarachnoid hemorrhage: a meta-analysis. PLoS ONE 9(6):e99536. https://doi.org/10.1371/journal.pone.0099536

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Alfotih GT, Li F, Xu X, Zhang S (2014) Risk factors for re-bleeding of aneurysmal subarachnoid hemorrhage: meta-analysis of observational studies. Neurol Neurochir Pol 48(5):346–355. https://doi.org/10.1016/j.pjnns.2014.08.002

    Article  PubMed  Google Scholar 

  11. Tanno Y, Homma M, Oinuma M, Kodama N, Ymamoto T (2007) Rebleeding from ruptured intracranial aneurysms in North Eastern Province of Japan. A cooperative study J Neurol Sci 258(1–2):11–16. https://doi.org/10.1016/j.jns.2007.01.074

    Article  PubMed  Google Scholar 

  12. Choudhry A, Murray D, Corr P, Nolan D, Coffey D, MacNally S, O’Hare A, Power S, Crockett M, Thornton J, Rawluk D, Brennan P, Javadpour M (2022) Timing of treatment of aneurysmal subarachnoid haemorrhage: are the goals set in international guidelines achievable? Ir J Med Sci 191(1):401–406. https://doi.org/10.1007/s11845-021-02542-1

    Article  PubMed  Google Scholar 

  13. Inagawa T, Kamiya K, Ogasawara H, Yano T (1987) Rebleeding of ruptured intracranial aneurysms in the acute stage. Surg Neurol 28(2):93–99

    PubMed  CAS  Google Scholar 

  14. Juvela S (1989) Rebleeding from ruptured intracranial aneurysms. Surg Neurol 32(5):323–326

    PubMed  CAS  Google Scholar 

  15. Richardson AE, Jane JA, Payne PM (1964) Assessment of the natural history of anterior communicating aneurysms. J Neurosurg 21:266–274. https://doi.org/10.3171/jns.1964.21.4.0266

    Article  PubMed  CAS  Google Scholar 

  16. Ando T, Sakai N, Yamada H, Iwai T, Nishimura Y, Hirata T, Funakoshi T, Takada M (1989) Analysis of reruptured cerebral aneurysms and the prophylactic effects of barbiturate therapy on the early stage. Neurol Res 11(4):245–248

    PubMed  CAS  Google Scholar 

  17. White P, Gregson B, McColl E, Brennan P, Steel A, Watts P, Wood R, Bowes C, Javadpour M, Weston A, Mitra D (2021) Emergent aneurysm treatment compared with treatment on neurological improvement in patients with ruptured poor-grade aneurysmal subarachnoid haemorrhage: the TOPSAT2 RCT In Efficacy and Mechanism Evaluation. Southampton (UK). https://doi.org/10.3310/eme08080

    Article  PubMed Central  Google Scholar 

  18. Sorteberg A, Romundstad L, Sorteberg W (2021) Timelines and rebleeds in patients admitted into neurosurgical care for aneurysmal subarachnoid haemorrhage. Acta Neurochir (Wien) 163(3):771–781

    PubMed  Google Scholar 

  19. Lamb JN, Crocker M, Tait MJ, Anthony Bell B, Papadopoulos MC (2011) Delays in treating patients with good grade subarachnoid haemorrhage in London. Br J Neurosurg 25(2):243–248. https://doi.org/10.3109/02688697.2010.544787

    Article  PubMed  Google Scholar 

  20. Post R, Germans MR, Tjerkstra MA, Vergouwen MDI, Jellema K, Koot RW, Kruyt ND, Willems PWA, Wolfs JFC, de Beer FC, Kieft H, Nanda D, van der Pol B, Roks G, de Beer F, Halkes PHA, Reichman LJA, Brouwers P, van den Berg-Vos RM, Kwa VIH, van der Ree TC, Bronner I, van de Vlekkert J, Bienfait HP, Boogaarts HD, Klijn CJM, van den Berg R, Coert BA, Horn J, Majoie C, Rinkel GJE, Roos Y, Vandertop WP, Verbaan D (2021) Ultra-early tranexamic acid after subarachnoid haemorrhage (ULTRA): a randomised controlled trial. Lancet (London, England) 397(10269):112–118

    PubMed  CAS  Google Scholar 

  21. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A (2016) Rayyan-a web and mobile app for systematic reviews. Syst Rev 5(1):210. https://doi.org/10.1186/s13643-016-0384-4

    Article  PubMed  PubMed Central  Google Scholar 

  22. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hrobjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lin L, Chu H (2020) Meta-analysis of proportions using generalized linear mixed models. Epidemiology 31(5):713–717. https://doi.org/10.1097/EDE.0000000000001232

    Article  PubMed  PubMed Central  Google Scholar 

  24. Turner RM, Omar RZ, Yang M, Goldstein H, Thompson SG (2000) A multilevel model framework for meta-analysis of clinical trials with binary outcomes. Stat Med 19(24):3417–3432. https://doi.org/10.1002/1097-0258(20001230)19:24%3c3417::Aid-sim614%3e3.0.Co;2-l

    Article  PubMed  CAS  Google Scholar 

  25. Rhodes KM, Turner RM, Higgins JP (2015) Predictive distributions were developed for the extent of heterogeneity in meta-analyses of continuous outcome data. J Clin Epidemiol 68(1):52–60. https://doi.org/10.1016/j.jclinepi.2014.08.012

    Article  PubMed  PubMed Central  Google Scholar 

  26. Turner RM, Jackson D, Wei Y, Thompson SG, Higgins JP (2015) Predictive distributions for between-study heterogeneity and simple methods for their application in Bayesian meta-analysis. Stat Med 34(6):984–998. https://doi.org/10.1002/sim.6381

    Article  PubMed  Google Scholar 

  27. R Core Development Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  28. Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L (2008) Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol 61(10):991–996. https://doi.org/10.1016/j.jclinepi.2007.11.010

    Article  PubMed  Google Scholar 

  29. Wasserstein RL, Lazar NA (2016) The ASA statement on p-values: context, process, and purpose. Am Stat 70(2):129–133. https://doi.org/10.1080/00031305.2016.1154108

    Article  Google Scholar 

  30. GA Wells, B Shea, D O'Connell, J Peterson, V Welch, M Losos, Tugwell P (2004) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. The Ottawa Hospital. Accessed 6th of January 2020

  31. Guyatt GH, Oxman AD, Vist GE, Kunz R, Falck-Ytter Y, Alonso-Coello P, Schunemann HJ, Group GW (2008) GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 336(7650):924–926. https://doi.org/10.1136/bmj.39489.470347.AD

    Article  PubMed  PubMed Central  Google Scholar 

  32. Torner JC, Kassell NF, Wallace RB, Adams HP Jr (1981) Preoperative prognostic factors for rebleeding and survival in aneurysm patients receiving antifibrinolytic therapy: report of the cooperative aneurysm study. Neurosurgery 9(5):506–513

    PubMed  CAS  Google Scholar 

  33. Kassell NF, Torner JC (1983) Size of intracranial aneurysms. Neurosurgery 12(3):291–297

    PubMed  CAS  Google Scholar 

  34. Aoyagi N, Hayakawa I (1984) Analysis of 223 ruptured intracranial aneurysms with special reference to rerupture. Surg Neurol 21(5):445–452

    PubMed  CAS  Google Scholar 

  35. Hijdra A, van Gijn J, Nagelkerke NJ, Vermeulen M, van Crevel H (1988) Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke 19(10):1250–1256

    PubMed  CAS  Google Scholar 

  36. Paré L, Delfino R, Leblanc R (1992) The relationship of ventricular drainage to aneurysmal rebleeding. J Neurosurg 76(3):422–427

    PubMed  Google Scholar 

  37. Tokuda Y, Inagawa T, Katoh Y, Kumano K, Ohbayashi N, Yoshioka H (1995) Intracerebral hematoma in patients with ruptured cerebral aneurysms. Surg Neurol 43(3):272–277

    PubMed  CAS  Google Scholar 

  38. Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Koike T, Tanaka R (1996) Ultra-early rebleeding in spontaneous subarachnoid hemorrhage. J Neurosurg 84(1):35–42

    PubMed  CAS  Google Scholar 

  39. Gruber A, Dietrich W, Czech T, Richling B (1997) Recurrent aneurysmal subarachnoid haemorrhage: bleeding pattern and incidence of posthaemorrhagic ischaemic infarction. Br J Neurosurg 11(2):121–126

    PubMed  CAS  Google Scholar 

  40. Kawai K, Nagashima H, Narita K, Nakagomi T, Nakayama H, Tamura A, Sano K (1997) Efficacy and risk of ventricular drainage in cases of grade V subarachnoid hemorrhage. Neurol Res 19(6):649–653

    PubMed  CAS  Google Scholar 

  41. Ohkuma H, Tsurutani H, Suzuki S (2001) Incidence and significance of early aneurysmal rebleeding before neurosurgical or neurological management. Stroke, vol 32, 5 edn., United States

  42. Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE (2002) Immediate administration of tranexamic acid and reduced incidence of early rebleeding after aneurysmal subarachnoid hemorrhage: a prospective randomized study. J Neurosurg 97(4):771–778

    PubMed  CAS  Google Scholar 

  43. McIver JI, Friedman JA, Wijdicks EF, Piepgras DG, Pichelmann MA, Toussaint LG 3rd, McClelland RL, Nichols DA, Atkinson JL (2002) Preoperative ventriculostomy and rebleeding after aneurysmal subarachnoid hemorrhage. J Neurosurg 97(5):1042–1044

    PubMed  Google Scholar 

  44. Naidech AM, Janjua N, Kreiter KT, Ostapkovich ND, Fitzsimmons BF, Parra A, Commichau C, Connolly ES, Mayer SA (2005) Predictors and impact of aneurysm rebleeding after subarachnoid hemorrhage. Arch Neurol 62(3):410–416

    PubMed  Google Scholar 

  45. Beck J, Raabe A, Szelenyi A, Berkefeld J, Gerlach R, Setzer M, Seifert V (2006) Sentinel headache and the risk of rebleeding after aneurysmal subarachnoid hemorrhage. Stroke, vol 37, 11 edn., United States

  46. Kitsuta Y, Suzuki N, Sugiyama M, Yamamoto I (2006) Changes in level of consciousness and association with hyperglycemia as tool for predicting and preventing re-bleeding after spontaneous subarachnoid hemorrhage. Prehosp Disaster Med 21(3):190–195

    PubMed  Google Scholar 

  47. Machiel Pleizier C, Algra A, Velthuis BK, Rinkel GJ (2006) Relation between size of aneurysms and risk of rebleeding in patients with subarachnoid haemorrhage. Acta Neurochir (Wien) 148(12):1277–1279 (discussion 1279-1280)

    PubMed  CAS  Google Scholar 

  48. Hellingman CA, van den Bergh WM, Beijer IS, van Dijk GW, Algra A, van Gijn J, Rinkel GJ (2007) Risk of rebleeding after treatment of acute hydrocephalus in patients with aneurysmal subarachnoid hemorrhage. Stroke 38(1):96–99

    PubMed  Google Scholar 

  49. Cha KC, Kim JH, Kang HI, Moon BG, Lee SJ, Kim JS (2010) Aneurysmal rebleeding : factors associated with clinical outcome in the rebleeding patients. J Korean Neurosurg Soc 47(2):119–123

    PubMed  PubMed Central  Google Scholar 

  50. Inagawa T (2010) Size of ruptured intracranial saccular aneurysms in patients in Izumo City Japan. World Neurosurg 73(2):84–92 (discussion e11)

    PubMed  Google Scholar 

  51. Guo LM, Zhou HY, Xu JW, Wang Y, Qiu YM, Jiang JY (2011) Risk factors related to aneurysmal rebleeding. World Neurosurg 76(3):292–298 (discussion 253-294)

    PubMed  Google Scholar 

  52. van den Berg R, Foumani M, Schröder RD, Peerdeman SM, Horn J, Bipat S, Vandertop WP (2011) Predictors of outcome in World Federation of Neurologic Surgeons grade V aneurysmal subarachnoid hemorrhage patients. Crit Care Med 39(12):2722–2727

    PubMed  Google Scholar 

  53. Cong W, Zhongxin Z, Tiangui L, Zhang Y, Min H, Chao Y (2012) Risk factors for rebleeding of aneurysmal subarachnoid hemorrhage based on the analysis of on-admission information. Turk Neurosurg 22(6):675–681

    PubMed  Google Scholar 

  54. Lord AS, Fernandez L, Schmidt JM, Mayer SA, Claassen J, Lee K, Connolly ES, Badjatia N (2012) Effect of rebleeding on the course and incidence of vasospasm after subarachnoid hemorrhage. Neurology 78(1):31–37. https://doi.org/10.1212/WNL.0b013e31823ed0a4

  55. Wu TC, Tsui YK, Chen TY, Lin CJ, Wu TC, Tzeng WS (2012) Rebleeding of aneurysmal subarachnoid hemorrhage in computed tomography angiography: risk factor, rebleeding pattern, and outcome analysis. J Comput Assist Tomogr 36(1):103–108

    PubMed  Google Scholar 

  56. Yin C, Ruan J, Jiang L, Zhou S, Sun X (2012) The relationship between rebleeding after spontaneous SAH and APOE polymorphisms in a Chinese population. Int J Neurosci 122(8):472–476

    PubMed  CAS  Google Scholar 

  57. De Marchis GM, Lantigua H, Schmidt JM, Lord AS, Velander AJ, Fernandez A, Falo MC, Agarwal S, Connolly ES Jr, Claassen J, Mayer SA (2014) Impact of premorbid hypertension on haemorrhage severity and aneurysm rebleeding risk after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry 85(1):56–59

    PubMed  Google Scholar 

  58. Davies BM, Chung KH, Dulhanty L, Galea J, Patel HC (2015) Pre-protection re-haemorrhage following aneurysmal subarachnoid haemorrhage: where are we now? Clin Neurol Neurosurg 135:22–26

    PubMed  Google Scholar 

  59. Jaja BN, Lingsma H, Schweizer TA, Thorpe KE, Steyerberg EW, Macdonald RL (2015) Prognostic value of premorbid hypertension and neurological status in aneurysmal subarachnoid hemorrhage: pooled analyses of individual patient data in the SAHIT repository. J Neurosurg 122(3):644–652

    PubMed  Google Scholar 

  60. Oheda M, Inamasu J, Moriya S, Kumai T, Kawazoe Y, Nakae S, Kato Y, Hirose Y (2015) Early rebleeding in patients with subarachnoid haemorrhage under intensive blood pressure management. J Clin Neurosci 22(8):1338–1342

    PubMed  Google Scholar 

  61. van Donkelaar CE, Bakker NA, Veeger NJ, Uyttenboogaart M, Metzemaekers JD, Luijckx GJ, Groen RJ, van Dijk JM (2015) Predictive factors for rebleeding after aneurysmal subarachnoid hemorrhage: rebleeding aneurysmal subarachnoid hemorrhage study. Stroke 46(8):2100–2106

    PubMed  Google Scholar 

  62. Wilson TJ, Saadeh Y, Stetler WR Jr, Pandey AS, Gemmete JJ, Chaudhary N, Thompson BG, Fletcher JJ (2015) Transfer time to a high-volume center for patients with subarachnoid hemorrhage does not affect outcomes. J Stroke Cerebrovasc Dis 24(2):416–423

    PubMed  Google Scholar 

  63. Lin QS, Ping C, Lin YX, Lin ZY, Yu LH, Dai LS, Kang DZ (2016) Systolic blood pressure variability is a novel risk factor for rebleeding in acute subarachnoid hemorrhage: a case-control study. Medicine 95(11):e3028

    PubMed  PubMed Central  Google Scholar 

  64. Solanki C, Pandey P, Rao KV (2016) Predictors of aneurysmal rebleed before definitive surgical or endovascular management. Acta Neurochir (Wien) 158(6):1037–1044

    PubMed  Google Scholar 

  65. Suwatcharangkoon S, Meyers E, Falo C, Schmidt JM, Agarwal S, Claassen J, Mayer SA (2016) Loss of consciousness at onset of subarachnoid hemorrhage as an important marker of early brain injury. JAMA Neurol 73(1):28–35

    PubMed  Google Scholar 

  66. Zhao B, Fan Y, Xiong Y, Yin R, Zheng K, Li Z, Tan X, Yang H, Zhong M (2016) Aneurysm rebleeding after poor-grade aneurysmal subarachnoid hemorrhage: predictors and impact on clinical outcomes. J Neurol Sci 371:62–66

    PubMed  Google Scholar 

  67. Malekpour M, Kulwin C, Bohnstedt BN, Radmand G, Sethia R, Mendenhall SK, Weyhenmeyer J, Hendricks BK, Leipzig T, Payner TD, Shah MV, Scott J, DeNardo A, Sahlein D, Cohen-Gadol AA (2017) Effect of short-term ε-aminocaproic acid treatment on patients undergoing endovascular coil embolization following aneurysmal subarachnoid hemorrhage. J Neurosurg 126(5):1606–1613

    PubMed  CAS  Google Scholar 

  68. Wang J, Alotaibi NM, Akbar MA, Ayling OG, Ibrahim GM, Macdonald RL (2017) Loss of consciousness at onset of aneurysmal subarachnoid hemorrhage is associated with functional outcomes in good-grade patients. World Neurosurg 98:308–313

    PubMed  Google Scholar 

  69. Darkwah Oppong M, Gumus M, Pierscianek D, Herten A, Kneist A, Wrede K, Barthel L, Forsting M, Sure U, Jabbarli R (2018) Aneurysm rebleeding before therapy: a predictable disaster? J Neurosurg 1–8. https://doi.org/10.3171/2018.7.JNS181119

  70. Nemoto M, Masuda H, Sakaeyama Y, Okonogi S, Node Y, Ueda K, Ando S, Kondo K, Harada N, Sugo N (2018) Clinical Characteristics of Subarachnoid Hemorrhage with an Intracerebral Hematoma and Prognostic Factors. J Stroke Cerebrovasc Dis 27(5):1160–1166. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.11.034

  71. van Lieshout JH, Pumplün I, Fischer I, Kamp MA, Cornelius JF, Steiger HJ, Boogaarts HD, Petridis AK, Beseoglu K (2018) Volume of cerebrospinal fluid drainage as a predictor for pretreatment aneurysmal rebleeding. J Neurosurg 128(6):1778–1784

    PubMed  Google Scholar 

  72. He Q, Zhou Y, Liu C, Zhang X, Huang N, Wang F, Liu G, Cheng Y, Xie Z (2019) Thromboelastography with platelet mapping detects platelet dysfunction in patients with aneurysmal subarachnoid hemorrhage with rebleeding. Neuropsychiatr Dis Treat 15:3443–3451

    PubMed  PubMed Central  CAS  Google Scholar 

  73. Horie N, Sato S, Kaminogo M, Morofuji Y, Izumo T, Anda T, Matsuo T (2019) Impact of perioperative aneurysm rebleeding after subarachnoid hemorrhage. J Neurosurg 1–10. https://doi.org/10.3171/2019.6.JNS19704

  74. Koopman I, Greving JP, van der Schaaf IC, van der Zwan A, Rinkel GJ, Vergouwen MD (2019) Aneurysm characteristics and risk of rebleeding after subarachnoid haemorrhage. Eur Stroke J 4(2):153–159

    PubMed  Google Scholar 

  75. Tack RW, Vergouwen MD, van der Schaaf I, van der Zwan A, Rinkel GJ, Lindgren AE (2019) Preventable poor outcome from rebleeding by emergency aneurysm occlusion in patients with aneurysmal subarachnoid haemorrhage. Eur Stroke J 4(3):240–246

    PubMed  PubMed Central  Google Scholar 

  76. Zheng J, Xu R, Guo Z, Sun X (2019) Small ruptured intracranial aneurysms: the risk of massive bleeding and rebleeding. Neurol Res 41(4):312–318

    PubMed  Google Scholar 

  77. Lu VM, Graffeo CS, Perry A, Carlstrom LP, Casabella AM, Wijdicks EFM, Lanzino G, Rabinstein AA (2020) Subarachnoid hemorrhage rebleeding in the first 24 h is associated with external ventricular drain placement and higher grade on presentation: cohort study. J Clin Neurosci 81:180–185

    PubMed  Google Scholar 

  78. Rehman S, Chandra RV, Zhou K, Tan D, Lai L, Asadi H, Froelich J, Thani N, Nichols L, Blizzard L, Smith K, Thrift AG, Stirling C, Callisaya ML, Breslin M, Reeves MJ, Gall S (2020) Sex differences in aneurysmal subarachnoid haemorrhage (aSAH): aneurysm characteristics, neurological complications, and outcome. Acta Neurochir (Wien) 162(9):2271–2282

    PubMed  Google Scholar 

  79. Wang JY, Zhang XT, Wang JQ, Wang CY, Zheng WL, Pan ZM, Xu ZB, Li XY, Zhang YB (2020) Admission neutrophil-lymphocyte ratio predicts rebleeding following aneurismal subarachnoid hemorrhage. World Neurosurg 138:e317–e322

    PubMed  Google Scholar 

  80. Kaneko J, Tagami T, Tanaka C, Kuwamoto K, Sato S, Shibata A, Kudo S, Kitahashi A, Kuno M, Yokobori S, Unemoto K (2021) Ultra-early induction of general anesthesia for reducing rebleeding rates in patients with aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis 30(8):105926

    PubMed  Google Scholar 

  81. Liu Q, Yang Y, Yang J, Li M, Yang S, Wang N, Wu J, Jiang P, Wang S (2021) Rebleeding of ruptured intracranial aneurysm after admission: a multidimensional nomogram model to risk assessment. Front Aging Neurosci 13:692615

    PubMed  PubMed Central  Google Scholar 

  82. Sebök M, Hostettler IC, Keller E, Rautalin IM, Coert BA, Vandertop WP, Post R, Sardeha A, Tjerkstra MA, Regli L, Verbaan D, Germans MR (2021) Prehemorrhage antiplatelet use in aneurysmal subarachnoid hemorrhage and impact on clinical outcome. Int J Stroke:17474930211035647

  83. Park J, Woo H, Kang DH, Kim YS, Kim MY, Shin IH, Kwak SG (2015) Formal protocol for emergency treatment of ruptured intracranial aneurysms to reduce in-hospital rebleeding and improve clinical outcomes. J Neurosurg 122(2):383–391. https://doi.org/10.3171/2014.9.JNS131784

    Article  PubMed  Google Scholar 

  84. Sorteberg A, Bredmose PP, Hansen AE, Sorteberg W (2019) The path from ictus to neurosurgery: chronology and transport logistics of patients with aneurysmal subarachnoid haemorrhage in the South-Eastern Norway Health Region. Acta Neurochir (Wien) 161(8):1497–1506. https://doi.org/10.1007/s00701-019-03971-9

    Article  PubMed  Google Scholar 

  85. Nieuwkamp DJ, Rinkel GJ, Silva R, Greebe P, Schokking DA, Ferro JM (2006) Subarachnoid haemorrhage in patients > or = 75 years: clinical course, treatment and outcome. J Neurol Neurosurg Psychiatry 77(8):933–937. https://doi.org/10.1136/jnnp.2005.084350

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  86. Ohkuma H, Shimamura N, Naraoka M, Katagai T (2017) Aneurysmal subarachnoid hemorrhage in the elderly over age 75: a systematic review. Neurol Med Chir (Tokyo) 57(11):575–583. https://doi.org/10.2176/nmc.ra.2017-0057

    Article  PubMed  Google Scholar 

  87. Zheng J, Sun X, Zhang X (2020) Influence of age-related complications on clinical outcome in patients with small ruptured cerebral aneurysms. Front Neurol 11:131. https://doi.org/10.3389/fneur.2020.00131

    Article  PubMed  PubMed Central  Google Scholar 

  88. Turan N, Heider RA, Zaharieva D, Ahmad FU, Barrow DL, Pradilla G (2016) Sex differences in the formation of intracranial aneurysms and incidence and outcome of subarachnoid hemorrhage: review of experimental and human studies. Transl Stroke Res 7(1):12–19. https://doi.org/10.1007/s12975-015-0434-6

    Article  PubMed  Google Scholar 

  89. Cras TY, Bos D, Ikram MA, Vergouwen MDI, Dippel DWJ, Voortman T, Adams HHH, Vernooij MW, Roozenbeek B (2020) Determinants of the presence and size of intracranial aneurysms in the general population: the rotterdam study. Stroke 51(7):2103–2110. https://doi.org/10.1161/STROKEAHA.120.029296

    Article  PubMed  PubMed Central  Google Scholar 

  90. Kongable GL, Lanzino G, Germanson TP, Truskowski LL, Alves WM, Torner JC, Kassell NF (1996) Gender-related differences in aneurysmal subarachnoid hemorrhage. J Neurosurg 84(1):43–48. https://doi.org/10.3171/jns.1996.84.1.0043

    Article  PubMed  CAS  Google Scholar 

  91. Wang YX, He J, Zhang L, Li Y, Zhao L, Liu H, Yang L, Zeng XJ, Yang J, Peng GM, Ahuja A, Yang ZH (2016) A higher aneurysmal subarachnoid hemorrhage incidence in women prior to menopause: a retrospective analysis of 4,895 cases from eight hospitals in China. Quant Imaging Med Surg 6(2):151–156. https://doi.org/10.21037/qims.2016.01.06

    Article  PubMed  PubMed Central  Google Scholar 

  92. Teo M, Guilfoyle MR, Turner C, Kirkpatrick PJ, Collaborators S (2017) What factors determine treatment outcome in aneurysmal subarachnoid hemorrhage in the modern era? A Post Hoc STASH Analysis. World Neurosurg 105:270–281. https://doi.org/10.1016/j.wneu.2017.05.005

    Article  PubMed  Google Scholar 

  93. McGurgan IJ, Clarke R, Lacey B, Kong XL, Chen Z, Chen Y, Guo Y, Bian Z, Li L, Lewington S, China Kadoorie Biobank C (2018) Blood pressure and risk of subarachnoid hemorrhage in China. Stroke: STROKEAHA118022239. https://doi.org/10.1161/STROKEAHA.118.022239

  94. Andreasen TH, Bartek J Jr, Andresen M, Springborg JB, Romner B (2013) Modifiable risk factors for aneurysmal subarachnoid hemorrhage. Stroke 44(12):3607–3612. https://doi.org/10.1161/STROKEAHA.113.001575

    Article  PubMed  Google Scholar 

  95. Feigin VL, Rinkel GJ, Lawes CM, Algra A, Bennett DA, van Gijn J, Anderson CS (2005) Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies. Stroke 36(12):2773–2780. https://doi.org/10.1161/01.STR.0000190838.02954.e8

    Article  PubMed  Google Scholar 

  96. Backes D, Rinkel GJE, Greving JP, Velthuis BK, Murayama Y, Takao H, Ishibashi T, Igase M, terBrugge KG, Agid R, Jaaskelainen JE, Lindgren AE, Koivisto T, von Und Zu, Fraunberg M, Matsubara S, Moroi J, Wong GKC, Abrigo JM, Igase K, Matsumoto K, Wermer MJH, van Walderveen MAA, Algra A, Vergouwen MDI (2017) ELAPSS score for prediction of risk of growth of unruptured intracranial aneurysms. Neurology 88(17):1600–1606. https://doi.org/10.1212/WNL.0000000000003865

    Article  PubMed  Google Scholar 

  97. Greving JP, Wermer MJH, Brown RD, Morita A, Juvela S, Yonekura M, Ishibashi T, Torner JC, Nakayama T, Rinkel GJE, Algra A (2014) Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol 13(1):59–66. https://doi.org/10.1016/s1474-4422(13)70263-1

    Article  PubMed  Google Scholar 

  98. Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6(1):1–9. https://doi.org/10.1227/00006123-198001000-00001

    Article  PubMed  CAS  Google Scholar 

  99. Frontera JA, Claassen J, Schmidt JM, Wartenberg KE, Temes R, Connolly ES Jr, MacDonald RL, Mayer SA (2006) Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery 59(1):21–27. https://doi.org/10.1227/01.NEU.0000218821.34014.1B. (discussion 21-27)

    Article  PubMed  Google Scholar 

  100. Kramer AH, Hehir M, Nathan B, Gress D, Dumont AS, Kassell NF, Bleck TP (2008) A comparison of 3 radiographic scales for the prediction of delayed ischemia and prognosis following subarachnoid hemorrhage. J Neurosurg 109(2):199–207. https://doi.org/10.3171/JNS/2008/109/8/0199

    Article  PubMed  Google Scholar 

  101. van der Steen WE, Leemans EL, van den Berg R, Roos Y, Marquering HA, Verbaan D, Majoie C (2019) Radiological scales predicting delayed cerebral ischemia in subarachnoid hemorrhage: systematic review and meta-analysis. Neuroradiology 61(3):247–256. https://doi.org/10.1007/s00234-019-02161-9

    Article  PubMed  Google Scholar 

  102. Komiyama M (2019) Misunderstanding of Fisher’s grouping system for computed tomography evaluation of aneurysmal subarachnoid haemorrhage. Interv Neuroradiol 25(6):653–654. https://doi.org/10.1177/1591019919856511

    Article  PubMed  PubMed Central  Google Scholar 

  103. Kienzler J, Marbacher S, Remonda L, Soleman J, Ai Schlaeppi J, Leupold U, Fandino J (2016) Outcome after in-hospital rebleeding of rupture of intracranial aneurysms. J Neurol Surg A Cent Eur Neurosurg 77(3):207–221. https://doi.org/10.1055/s-0035-1570007

    Article  PubMed  Google Scholar 

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Doherty, R.J., Henry, J., Brennan, D. et al. Predictive factors for pre-intervention rebleeding in aneurysmal subarachnoid haemorrhage: a systematic review and meta-analysis. Neurosurg Rev 46, 24 (2023). https://doi.org/10.1007/s10143-022-01930-0

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