Elsevier

World Neurosurgery

Volume 101, May 2017, Pages 26-32
World Neurosurgery

Original Article
Target Embolization of Associated Aneurysms in Ruptured Arteriovenous Malformations

https://doi.org/10.1016/j.wneu.2017.01.081Get rights and content

Objectives

The purpose of this study was to examine the safety and efficacy of target embolization of aneurysms associated with ruptured brain arteriovenous malformations (BAVMs).

Methods

Ruptured BAVM patients who underwent endovascular treatment at our institution from January 2011 to December 2015 were retrospectively reviewed. Patients were divided into aneurysm (AN) and nonaneurysm (non-AN) groups on the basis of the existence of BAVM-associated aneurysms or not. Demographics, angiographic characteristics, complications, and clinical outcomes were compared between 2 groups. Complication risk factors were analyzed for all objects. Patient outcomes were assessed with modified Rankin Scale (mRS).

Results

A total of 129 (male = 53) patients were included. In 31 (24.0%) patients, 33 aneurysms were observed, including 16 intranidal and 17 flow-related aneurysms. Of the 166 sessions of embolization performed, there were 13 (10.1% of patients, 7.8% per session) complications in all, including 2 hemorrhagic, 8 transient ischemic, and 3 permanent ischemic types. There was no statistical difference in terms of complication incidence rate between groups. A total of 12 patients (9.3% of patients, 3.3% per person-year) experienced postoperative hemorrhage during follow-up (mean = 3.4 years). The yearly postoperative hemorrhage incidence rate was 3.4% in the non-AN group and 2.0% in AN group. Excellent or good outcomes (mRS ≤ 2) were observed in 103 (91.2%) patients. Unfavorable outcomes (mRS ≥ 3) as a direct result of embolization remained in no patients.

Conclusions

Target embolization of aneurysms associated with ruptured BAVMs could significantly decrease postoperative rehemorrhage without increasing complications.

Introduction

Intracranial hemorrhage (ICH) secondary to brain arteriovenous malformations (BAVMs) carries significant morbidity and mortality.1, 2 Initial hemorrhage presentation is the most important indicator for subsequent hemorrhage for BAVM patients. The overall yearly hemorrhage risk of ruptured BAVMs ranges from 2.55%–17.8%, higher than that (2.1%–4.12%) of unruptured BAVMs.3, 4, 5, 6 Aneurysms associated with BAVMs portend a high risk of hemorrhage or rehemorrhage. The risk of hemorrhage in BAVM patients with associated aneurysms was reported to be 7% per year, which is higher than the 3% risk of hemorrhage for patients without aneurysms.3, 7, 8 Studies have proved that target embolization of associated aneurysms may decrease the hemorrhage rate and improve clinical outcome for unruptured BAVMs.9 However, for ruptured BAVMs, whether target embolization of associated aneurysms will be safe and efficient is not well known. In order to evaluate the safety and efficacy of target embolization, we compared the complication incidence rate and rehemorrhage incidence rate between ruptured BAVMs with and without associated aneurysms.

Section snippets

Patients

This study was approved by the ethics committee of Beijing Tiantan Hospital. All patients signed informed consent. A series of 336 consecutive BAVM patients from January 2011 to December 2015 at Beijng Tiantan Hospital were retrospectively reviewed. Patients who presented with intracerebral hemorrhage (ICH) caused by BAVM or associated aneurysms and underwent endovascular embolization were included. Patients who underwent surgery resection before or after embolization were excluded.

ICH is

Statistical Analysis

All statistical analyses were conducted by using SPSS 18.0 (Chicago, IL, USA). Patients' characteristics were described with frequencies for categorical variables and mean ± standard deviation for continuous variables. Categorical variables were compared using Fisher exact test or the Pearson χ2 test. Continuous variables were compared between groups using student's t test. Univariate and multivariate logistic analyses were done to assess risk factors of complications. P < 0.05 was considered

Demographic and Angiographic Characteristics

A total of 129 (male = 53, 41.1%) patients met the inclusion criteria (Table 1). Age ranged from 5–65 years old (mean ± standard deviation: 26.9 ± 13.3 years old). The period of time from initial hemorrhage presentation to endovascular treatment ranged from 1–160 days (median = 42 days). The location of BAVM is cortical in 70 (54.3%) patients, deep in 40 (31.0%), infratentorial in 19 (14.7%), and eloquent in 59 (45.7%) patients. As for the maximum diameter of the nidus, 87 (67.4%) patients are

Endovascular Treatment

During the treatment period, 129 patients underwent a total of 166 (1.29 ± 0.5 sessions per patient) embolization sessions, 95 (73.6%) patients underwent 1 session, 31 (24.0%) underwent 2 sessions, and 3 (2.3%) underwent 3 or more sessions. A total of 208 pedicles (1.6 ± 0.8 pedicles per patient) were embolized. Twenty-nine (93.5%) aneurysms were occluded (Figure 2). Two were not embolized because of inaccessibility of microcatheters. Two patients were treated for associated aneurysm with coils

Complications

Thirteen complications (10.1% of patients, 7.8% per session) occurred in this series. Of the 13 patients, 2 were hemorrhagic and 11 were ischemic (Table 2). Of the 11 (8.5% per patient, 6.6% per session) ischemic complications, 8 (6.2% per patient, 4.8% per session) were transient and 3 (2.3% per patient, 1.8% per session) were permanent. Complications are not statistically significant (P > 0.05) between the AN group and non-AN group.

Risks Factors Related to Complications

In univariate and multivariate analysis (Table 3), there was a higher rate of procedural complications in BAVMs with 3 or more pedicles occluded at 1 session (P = 0.037, odds ratio = 2.798, 95% confidence interval = 1.304–6.002). A coexisting aneurysm is not an indicator of procedural complications.

Follow-Up

Outcomes were recorded through in-person (25 patients, 22.1%) or structured telephone interviews (88 patients, 77.9%). The follow-up period ranges from 1–5 years. A total of 290 (mean = 3.4) person-years' follow-up were completed for non-AN group and 99 (mean = 3.7) person-years for AN-group (total 389 person-years, mean = 3.4). Sixteen (12.4%) patients are failed to show at follow-up, including 12 (12.2%) patients in the AN group and 4 (12.9%) in the non-AN group, leaving 113 to be calculated

Clinical Outcomes

In all, 10 (annual hemorrhage rate: 10/290 = 0.034) patients in the non-AN group and 2 (annual hemorrhage rate: 2/99 = 0.020) patients in the AN group experienced postoperative hemorrhage. The overall annual hemorrhage rate after embolization was 3.1% (12/389 = 0.031). Excellent or good outcomes (mRS = 0–2) were observed in 103 (91.2%) patients. Seven (6.2%) had persistent moderate (mRS = 3) deficits, 2 had a significant deficit (1.8%, mRS > 3) due to hemorrhage, and 1 patient (0.9%) died of

Discussion

Several previous studies have reported that the endovascular procedural-related complication rate is 0%–18% and the mortality rate is 0%–4%.11, 12, 13, 14, 15, 16, 17 Clinical complications include hemorrhagic and ischemic events. The hemorrhagic complication rate after BAVM embolization was reported to be approximately 3%–15% per patient and 1%–2% per procedure.11, 18, 19 Hemorrhagic complications may be caused by vessel perforation during catheterization, BAVM rupture, intranidal aneurysm

Conclusions

Target embolization of aneurysms associated with ruptured BAVMs could significantly decrease the rehemorrhage incidence rate without increasing the complication rate.

References (29)

  • X. Lv et al.

    Endovascular treatment of cerebral aneurysms associated with arteriovenous malformations

    Eur J Radiol

    (2012)
  • X. Lv et al.

    Complication risk of endovascular embolization for cerebral arteriovenous malformation

    Eur J Radiol

    (2011)
  • S.L. Ondra et al.

    The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment

    J Neurosurg

    (1990)
  • F. Signorelli et al.

    Ruptured brain arteriovenous malformations associated with aneurysms: safety and efficacy of selective embolization in the acute phase of hemorrhage

    Neuroradiology

    (2014)
  • R.D. Brown et al.

    The natural history of unruptured intracranial arteriovenous malformations

    J Neurosurg

    (1988)
  • R.D. Brown et al.

    Incidence and prevalence of intracranial vascular malformations in Olmsted County, Minnesota, 1965 to 1992

    Neurology

    (1996)
  • L. da Costa et al.

    The natural history and predictive features of hemorrhage from brain arteriovenous malformations

    Stroke

    (2009)
  • R.A. Gabriel et al.

    Ten-year detection rate of brain arteriovenous malformations in a large, multiethnic, defined population

    Stroke

    (2010)
  • M. Westphal et al.

    Clinical significance of pedicle aneurysms on feeding vessels, especially those located in infratentorial arteriovenous malformations

    J Neurosurg

    (2000)
  • H. Xiaochuan et al.

    Targeted embolization reduces hemorrhage complications in partially embolized cerebral AVM combined with gamma knife surgery

    Interv Neuroradiol

    (2015)
  • M.V. Jayaraman et al.

    Neurologic complications of arteriovenous malformation embolization using liquid embolic agents

    AJNR Am J Neuroradiol

    (2008)
  • C.J. Ledezma et al.

    Complications of cerebral arteriovenous malformation embolization: multivariate analysis of predictive factors

    Neurosurgery

    (2006)
  • C.S. Haw et al.

    Complications of embolization of arteriovenous malformations of the brain

    J Neurosurg

    (2006)
  • J. van Beijnum et al.

    Treatment of brain arteriovenous malformations: a systematic review and meta-analysis

    JAMA

    (2011)
  • Cited by (12)

    • Clinical Characteristics and Multimodality Therapy Outcomes in 304 Pediatric Patients with Cerebral Arteriovenous Malformations

      2022, World Neurosurgery
      Citation Excerpt :

      They suggested that the best candidates for stereotactic radiosurgery are pediatric patients with smaller-volume AVMs in critical brain regions. Recently, multimodality therapy has been advocated to improve clinical and radiographic outcomes.28-33 Blauwblomme et al. found that immediate surgery or curative embolization should be used in patients with ruptured AVMs with risk factors for re-hemorrhage, such as associated aneurysms and deep venous drainage, while radiosurgery may be more suited for patients without these features.34

    • Risk Factors of Brain Arteriovenous Malformation Embolization as Adjunctive Therapy: Single-Center 10-Year Experience

      2022, World Neurosurgery
      Citation Excerpt :

      However, at the same time, it has been reported that more embolic material injection can lead to hemorrhagic complication.23 Minimal embolization limited to the dangerous component, such as AVM-related aneurysm or fistulous component, is called target (or targeted) embolization.24-26 At our institution, since ARUBA, therapeutic intervention with SRS for AVMs has been increasing, especially in unruptured AVMs.

    View all citing articles on Scopus

    Conflict of interest statement: This work was supported by the Beijing Municipal Health Bureau, Special Research Project of Capital Health Development, China (grant 2016-1-1075). The authors declare they have no conflict of interests.

    Yong Sun and Hengwei Jin contributed equally to this work.

    View full text