Ultra-early endovascular embolization of ruptured cerebral aneurysm and the increased risk of hematoma growth unrelated to aneurysmal rebleeding

Clinical article

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Object

Hematoma growth unrelated to aneurysmal rebleeding is recognized as a somewhat common complication following endovascular embolization of ruptured aneurysms, but it is scarcely studied. The aim of this study is to elucidate the possible risk factors for this phenomenon.

Methods

Included in this study were 101 consecutive patients with subarachnoid hemorrhage (SAH) who underwent endovascular embolization for saccular aneurysms at the authors' institution within 72 hours of symptom onset. All endovascular procedures were conducted under intraprocedural systemic anticoagulation. Age, sex, hypertension, type 2 diabetes, preoperative antiplatelet or anticoagulation use, neurological grade, Fisher grade, location and size of the aneurysm, grade of aneurysm occlusion, and timing of the endovascular procedure were retrospectively analyzed to determine the risk factors for hematoma growth unrelated to aneurysmal rebleeding. To determine the clinical significance of this complication, the authors also investigated the risk factors for poor clinical outcome (modified Rankin Scale Scores 3–6 at 30 days after onset).

Results

This series included 32 men (31.7%) and 69 women (68.3%) with a mean age ± SD of 65.5 ± 14.0 years. The mean time from onset to endovascular procedure was 12.1 ± 14.0 hours. After the procedure, hematoma growth unrelated to aneurysmal rebleeding occurred in 14 patients (13.9%), 10 of whom required surgical removal of the hematoma and/or ventriculostomy to control intracranial pressure. All 14 patients had an anterior circulation aneurysm and had Fisher Grade 3 or 4 SAH. Ultra-early embolization (conducted within 6 hours after onset), female sex, history of hypertension, and poor neurological grade (World Federation of Neurosurgical Societies Grades IV and V) were significant risk factors for hematoma growth (p < 0.05 for all, univariate logistic analysis). In multivariate analysis, ultra-early embolization (OR 18.0 [95% CI 3.26–338], p < 0.001) and female sex (OR 9.83 [95% CI 1.73–187], p = 0.007) were independent risk factors for this phenomenon. Anterior circulation aneurysms and Fisher Grade 3 or 4 SAH were also revealed to be significant risk factors (p = 0.02 for each, chi-square test). Furthermore, hematoma growth without aneurysmal rebleeding was determined as an independent risk factor for poor clinical outcome by multivariate logistic analysis (OR 11.8 [95% CI 2.31–87.1], p = 0.002).

Conclusions

Ultra-early endovascular embolization for ruptured cerebral aneurysms under systemic anticoagulation increases the risk of growth of hematomas unrelated to aneurysmal rebleeding. It is important to recognize the risk of this complication and to either reduce the amount of heparin or to refer the patient for direct clipping if appropriate.

Abbreviations used in this paper:ICA = internal carotid artery; ICH = intracerebral hematoma; MCA = middle cerebral artery; mRS = modified Rankin Scale; SAH = subarachnoid hemorrhage; WFNS = World Federation of Neurosurgical Societies.

Article Information

Address correspondence to: Shinichi Yoshimura, M.D., Ph.D., Department of Neurosurgery, Gifu University Graduate School of Medicine, 1-1 Yanagido, Gifu-city, Gifu, Japan 501-1194. email: s-yoshi@gifu-u.ac.jp.

Please include this information when citing this paper: published online December 14, 2012; DOI: 10.3171/2012.11.JNS12610.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Images obtained in a 79-year-old woman who suffered SAH classified as Grade IV according to the WFNS scale. A: Computed tomography scan obtained on admission, revealing Fisher Grade 3 SAH with a left sylvian hematoma. B: Preoperative left carotid angiogram showing the saccular aneurysm at the ICA. Immediate coil embolization was performed 2.5 hours after onset under general anesthesia with systemic anticoagulation. C: Postoperative left carotid angiogram obtained after embolization, showing the successful obliteration of the aneurysm with little observed residual flow. D: Computed tomography scan obtained immediately after embolization (first follow-up CT). The left sylvian hematoma is slightly enlarged. E: Computed tomography scan obtained 10 hours after onset (second follow-up CT). Remarkable enlargement of the sylvian hematoma is observed, although the patient did not exhibit clinical signs of aneurysmal rebleeding. This patient underwent surgical hematoma removal, and the mRS score was 5 at 30 days after onset.

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    Images obtained in a 57-year-old woman who suffered SAH that was classified as WFNS Grade V. A: Computed tomography scan obtained on admission, revealing Fisher Grade 3 SAH with a dense focal hematoma on the left cingulate sulcus. B: Preoperative right carotid angiogram showing the saccular aneurysm at the anterior communicating artery. Immediate coil embolization was performed 4 hours after onset under general anesthesia with systemic anticoagulation. C: Postoperative right carotid angiogram obtained after embolization, showing complete obliteration of the aneurysm. D: Computed tomography scan obtained immediately after embolization (first follow-up CT). No significant enlargement of the hematoma is observed. E: Computed tomography scan obtained 26 hours after onset (second follow-up CT), revealing that enlargement of the left cingulate hematoma extended intraparenchymally, although the patient did not exhibit clinical signs of aneurysmal rebleeding. Interestingly, the enlarged hematoma was remote from the embolized aneurysm. This patient was treated conservatively, and her mRS score was 4 at 30 days after onset.

References

  • 1

    Drake CG: Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale. J Neurosurg 68:9859861988. (Letter)

  • 2

    Egashira YYoshimura SFunatsu NTanaka YYamada KEnomoto Y: Continuous growth of remote intracerebral haematoma following angiographically successful endovascular embolisation of ruptured cerebral aneurysms. J Clin Neurosci 19:1701732012

  • 3

    Fisher CMKistler JPDavis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:191980

  • 4

    Fujii YTakeuchi SSasaki OMinakawa TKoike TTanaka R: Ultra-early rebleeding in spontaneous subarachnoid hemorrhage. J Neurosurg 84:35421996

  • 5

    Higashi YSanada MSasaki SNakagawa KGoto CMatsuura H: Effect of estrogen replacement therapy on endothelial function in peripheral resistance arteries in normotensive and hypertensive postmenopausal women. Hypertension 37:6516572001

  • 6

    Jartti PIsokangas JMKarttunen AJartti AHaapea MKoskelainen T: Early rebleeding after coiling of ruptured intracranial aneurysms. Acta Radiol 51:104310492010

  • 7

    Johnston SCDowd CFHigashida RTLawton MTDuckwiler GRGress DR: Predictors of rehemorrhage after treatment of ruptured intracranial aneurysms: the Cerebral Aneurysm Rerupture After Treatment (CARAT) study. Stroke 39:1201252008

  • 8

    Kremer CGroden CHansen HCGrzyska UZeumer H: Outcome after endovascular treatment of Hunt and Hess grade IV or V aneurysms: comparison of anterior versus posterior circulation. Stroke 30:261726221999

  • 9

    Kusumi MYamada MKitahara TEndo MKan SIida H: Rerupture of cerebral aneurysms during angiography—a retrospective study of 13 patients with subarachnoid hemorrhage. Acta Neurochir (Wien) 147:8318372005

  • 10

    Melake MSYamamoto MYoshida KOishi HArai HElwan M: A retrospective clinical and angiographic study of the coiling outcome of ruptured intracranial aneurysms. J Clin Neurosci 17:3283332010

  • 11

    Molyneux AKerr RStratton ISandercock PClarke MShrimpton J: International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:126712742002

  • 12

    Naidech AMJanjua NKreiter KTOstapkovich NDFitzsimmons BFParra A: Predictors and impact of aneurysm rebleeding after subarachnoid hemorrhage. Arch Neurol 62:4104162005

  • 13

    Niemann DBWills ADMaartens NFKerr RSByrne JVMolyneux AJ: Treatment of intracerebral hematomas caused by aneurysm rupture: coil placement followed by clot evacuation. J Neurosurg 99:8438472003

  • 14

    Raymond JGuilbert FWeill AGeorganos SAJuravsky LLambert A: Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke 34:139814032003

  • 15

    Shin YSKim SYKim SHAhn YHYoon SHCho KH: One-stage embolization in patients with acutely ruptured poor-grade aneurysm. Surg Neurol 63:1491552005

  • 16

    Sluzewski Mvan Rooij WJ: Early rebleeding after coiling of ruptured cerebral aneurysms: incidence, morbidity, and risk factors. AJNR Am J Neuroradiol 26:173917432005

  • 17

    Suzuki SJahan RDuckwiler GRFrazee JMartin NViñuela F: Contribution of endovascular therapy to the management of poor-grade aneurysmal subarachnoid hemorrhage: clinical and angiographic outcomes. J Neurosurg 105:6646702006

  • 18

    Tanikawa R: [Less invasive cistemal approach and removal of subarachnoid hematoma for the treatment of ruptured cerebral aneurysms.]. No Shinkei Geka 35:17242007. (Jpn)

  • 19

    Tsuang FYSu ICChen JYLee JELai DMTu YK: Hyperacute cerebral aneurysm rerupture during CT angiography. Clinical article. J Neurosurg 116:124412502012

  • 20

    Tsuda K: Statins and gender-related difference in endothelial function in cerebral small vessel disease. Stroke 40:e5432009

  • 21

    van Asch CJOudendijk JFRinkel GJKlijn CJ: Early intracerebral hematoma expansion after aneurysmal rupture. Stroke 41:259225952010

  • 22

    Weir RUMarcellus MLDo HMSteinberg GKMarks MP: Aneurysmal subarachnoid hemorrhage in patients with Hunt and Hess grade 4 or 5: treatment using the Guglielmi detachable coil system. AJNR Am J Neuroradiol 24:5855902003

  • 23

    Willinsky RAPeltz Jda Costa LAgid RFarb RIter-Brugge KG: Clinical and angiographic follow-up of ruptured intracranial aneurysms treated with endovascular embolization. AJNR Am J Neuroradiol 30:103510402009

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