, Volume 61, Issue 2, pp 195–205 | Cite as

Single-stage planning for total cure of grade III–V brain arteriovenous malformations by embolization alone or in combination with microsurgical resection

  • Naci KocerEmail author
  • Sedat Giray Kandemirli
  • Reza Dashti
  • Osman Kizilkilic
  • Hakan Hanimoglu
  • Galip Zihni Sanus
  • Yusuf Tunali
  • Ercan Tureci
  • Civan Islak
  • Mehmet Yasar Kaynar
Interventional Neuroradiology



There are no established guidelines for treatment of Spetzler–Martin grade III–V brain arteriovenous malformations (bAVMs). The purpose of this study is to report our institutional experience in total obliteration/eradication of grade III–V bAVMs by single-stage planning of embolization combined with microsurgical resection when necessary.


All patients harboring Spetzler–Martin (S–M) grade III–V bAVMs treated with single-stage planning between January 2006 and January 2018 were retrospectively reviewed. This treatment paradigm is applicable only to surgically accessible bAVMs and does not include deep-seated bAVMs. Indications for treatment, clinical presentation, imaging characteristics, and treatment outcomes were analyzed. Outcomes were assessed based on modified Rankin Scale.


A total of 31 patients were identified. Seventeen patients (54.8%) presented with hemorrhage, 10 (32.3%) with seizures, 3 (9.7%) with headaches, and 1 (3.2%) with progressive neurological deficit. Based on S–M grading system, 25 patients (80.6%) harbored grade III bAVM, 5 patients had grade IV bAVMs (16.1%), and 1 patient (3.2%) had a grade V bAVM. There were no treatment-related complications in 24/31 (77.4%) patients. Of the total of seven patients with complications, four patients had clinical deterioration. The long-term (> 6-month), non-disabling morbidity (mRS ≤ 2) rate was 6.5%. The long-term, disabling morbidity rate was 3.2% with a mortality of 3.2%. Complete angiographic obliteration was achieved in 30/31 (96.8%) patients.


Single-stage treatment strategy can be considered as an alternative to multistage embolization prior to surgery in grade III–V bAVMs. In this study, a high rate of total obliteration with relatively low rates of permanent morbidity and mortality was achieved.


Arteriovenous malformation Microsurgical resection Embolization Multimodality treatment Single-stage treatment 


Compliance with ethical standards


No funding was received for this study.

Conflict of Interest

NK consults and proctors for MicroVention, Inc and Medtronic, Inc. CI consults and proctors for Medtronic, Inc.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

Supplementary material

234_2018_2140_Fig3_ESM.png (2.5 mb)
Fig. 1

A 67-year-old male with progressive right hemiparesis, aphasia and swallowing difficulty due to extensive venous reflux from an unruptured left fronto-parietal grade V bAVM. The patient had initially presented with seizures 37 years back and had undergone unsuccessful microsurgical bAVM resection. The patient clinically deteriorated over the last 6 months. The patient was planned to undergo single combined embolization and surgical treatment. a-b) Coronal T2-weighted MRI (in the year 1996) shows a left parietal AVM with a corticoventricular nidus. Digital subtraction angiogram (in the year 1996) shows a mixed fistulous and plexiform nidus with perinidal angiogenesis and venous drainage into deep and superficial venous system. c-e) Cranial computed tomography (in the year 2013) shows a craniotomy defect with surgical metallic artifacts. There is effacement of left parietal sulci. T2W and T1W MRI show prominent posterior fossa veins and extensive deep white matter hyperintensities. An enlarged venous aneurysm is projecting into right lateral ventricle (arrow). f-g) DSA prior to embolization (in the year 2013) shows a progressively enlarged corticoventricular nidus involving almost the entire parietal and posterior frontal region with an enlarged venous aneurysm projecting into right lateral ventricle. h) Cerebral DSA in venous phase shows enlargement of posterior fossa veins with prolonged circulation time. i-m) The posterior, superior and inferior components of the nidus were embolized with Onyx® through multiple dural and pial arterial feeders (arrows). A small residual anterior component was spared intentionally to avoid post-embolization perinidal hemorrhage. Also note the venous stagnation of the entire hemispheric venous system. n-o) Immediately after surgical resection, control DSA anteroposterior and lateral projections show complete elimination of the bAVM. p-r) MRI brain at one-month follow up shows regressing post-operative changes with thrombosed intra-ventricular venous aneurysm. On the 3rd year follow-up, patient had only one episode of seizure but had no other fresh neurological deficit. His speech and swallowing improved, while his right hemiparesis persisted (JPG 1026 kb)

234_2018_2140_MOESM1_ESM.tif (10.8 mb)
High resolution image (TIF 11087 kb)
234_2018_2140_Fig4_ESM.png (2.2 mb)
Fig. 2

A 20-year-old female presented with seizures due to an unruptured right temporal grade III bAVM. a-c) Cerebral DSA shows a moderate 2.5x4cms sized bAVM supplied by enlarged temporal branches of right middle cerebral artery. The bAVM had a mixed fistulous and plexiform nidus located in cortical-subcortical region with a multiple venous drainage pattern. Note the 3x3cm sized venous aneurysm in the draining vein of Trolard. d-e) 3D roadmap with overlaying technology, thin section algorithm and automatic motion compensation were used for microcatheter navigation and final positioning (arrow indicates venous aneurysm). f-h) Post-embolization anteroposterior and lateral internal carotid artery angiograms depict complete obliteration of AVM nidus with no early venous drainage. However, there are multiple regions of perinidal vascular structures with stagnant flow. i-k Right temporal parenchymal hemorrhage is seen adjacent to embolized nidus with intraventricular hemorrhage in the immediate post-embolization non-contrast CT. The patient underwent surgical bAVM resection and hematoma evacuation. Post surgical CT shows hematoma evacuation and nidus resection. l-o) Immediate post-treatment DSA shows total elimination of the nidus and perinidal stagnant vessels. p-t) 6-month follow-up MRI and 12-month follow-up DSA show gliotic right temporal changes, normalization of the pial vessels with no recurrence of bAVM (PNG 2240 kb)

234_2018_2140_MOESM2_ESM.tif (9.4 mb)
High resolution image (TIF 9661 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Naci Kocer
    • 1
    Email author
  • Sedat Giray Kandemirli
    • 1
  • Reza Dashti
    • 2
  • Osman Kizilkilic
    • 1
  • Hakan Hanimoglu
    • 3
  • Galip Zihni Sanus
    • 3
  • Yusuf Tunali
    • 4
  • Ercan Tureci
    • 4
  • Civan Islak
    • 1
  • Mehmet Yasar Kaynar
    • 3
  1. 1.Division of Neuroradiology, Department of Radiology, Cerrahpasa Medical FacultyIstanbul UniversityIstanbulTurkey
  2. 2.Department of NeurosurgeryUniversity of Illinois at ChicagoChicagoUSA
  3. 3.Department of Neurosurgery, Cerrahpasa Medical FacultyIstanbul UniversityIstanbulTurkey
  4. 4.Department of Anesthesiology and Reanimation, Cerrahpasa Medical FacultyIstanbul UniversityIstanbulTurkey

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