Clinical outcomes of procedures combining endovascular embolization with a direct surgical approach in a hybrid operating room for the treatment of refractory dural arteriovenous fistulas
- Department of Neurosurgery, Jikei University, Tokyo, Japan.
- Department of Advanced Therapies Innovation, Siemens Healthcare K.K., Tokyo, Japan.
Naoki Kato, Department of Neurosurgery, Jikei University, Tokyo, Japan.
DOI:10.25259/SNI_486_2021Copyright: © 2021 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Naoki Kato1, Toshihiro Ishibashi1, Fumiaki Maruyama1, Katharina Otani2, Shota Kakizaki1, Gota Nagayama1, Ayako Ikemura1, Shunsuke Hataoka1, Issei Kan1, Tomonobu Kodama1, Yuichi Murayama1. Clinical outcomes of procedures combining endovascular embolization with a direct surgical approach in a hybrid operating room for the treatment of refractory dural arteriovenous fistulas. 30-Aug-2021;12:439
How to cite this URL: Naoki Kato1, Toshihiro Ishibashi1, Fumiaki Maruyama1, Katharina Otani2, Shota Kakizaki1, Gota Nagayama1, Ayako Ikemura1, Shunsuke Hataoka1, Issei Kan1, Tomonobu Kodama1, Yuichi Murayama1. Clinical outcomes of procedures combining endovascular embolization with a direct surgical approach in a hybrid operating room for the treatment of refractory dural arteriovenous fistulas. 30-Aug-2021;12:439. Available from: https://surgicalneurologyint.com/?post_type=surgicalint_articles&p=11070
Background: We reviewed the clinical outcomes of a procedure that combines endovascular embolization and a direct surgical approach in a hybrid operating room (OR) for the treatment of refractory dural arteriovenous fistulas (dAVFs).
Methods: All patients with intracranial dAVFs who underwent a procedure combining endovascular embolization and direct surgical approach with biplane angiography or a robotic C-arm system in a hybrid OR between February 2004 and June 2020 were considered. Borden grading, occlusion rate, pre-and post-operative modified Rankin Scale (mRS) scores, and complications were retrospectively investigated. The pre-and postoperative mRS scores were compared using the Wilcoxon signed-ranks test.
Results: We evaluated 14 arteriovenous fistulas (AVFs) in consecutive 13 patients. Of these, ten AVFs were previously treated with endovascular embolization, ten were located in the transverse-sigmoid sinus, and four in the cortical vein. The Borden grade was II in two AVFs and III in 12 AVFs. Immediate occlusion of the AVF was achieved in 13 AVFs, and gradual occlusion was observed in one case. The median preoperative mRS was 1 (0–3), whereas the median postoperative mRS was 0 (0–1) which indicated marked improvement (P = 0.006). Complications including postoperative transient visual disturbance and intraprocedural extravasation were observed in only two cases.
Conclusion: The combination of endovascular embolization and direct surgical approach in a hybrid OR could achieve sufficient occlusion of refractory AVFs with acceptable complication rates and improved symptoms.
Keywords: Angiography, Arteriovenous fistula, Hybrid operating room, Robotic C-arm
Dural arteriovenous fistulas (dAVFs) are usually treated with an endovascular approach, including transarterial embolization (TAE) or transvenous embolization (TVE).[
This study was approved by the institutional review board (IRB) of the university hospital (reference # 29-228 ). Informed consent for treatment and image acquisition in the hybrid OR was obtained from each patient. As per IRB’s request, we posted a notice describing the study and gave the patients the opportunity to refuse participation. The IRB waived the requirement for specific informed consent for this study because the data were obtained from routine workflow and investigated retrospectively. We reviewed data for all patients treated for AVFs at our institution between February 2004 and June 2020 and selected those patients treated by a procedure combining endovascular embolization and a direct surgical approach.
All patients who underwent a combined surgical procedure were treated in a hybrid OR equipped with a biplane digital subtraction angiography (DSA) or a robotic C-arm system (Artis dBA, Artis Zee, Artis Q, Artis zeego, and ARTIS pheno; Siemens Healthcare GmbH, Forchheim, Germany) under general anesthesia. The patients were positioned in the supine or prone position, and diagnostic DSA was performed following fixation of the patient’s head. After craniotomy on the shunt point or draining vein of the AVF, the dura mater was opened to expose a sufficient area for safe catheterization of the microcatheter. The microcatheter was directly inserted into the draining vein using microsurgical techniques under a microscope with an integrated indocyanine green (ICG) videoangiography (Zeiss OPMI Pentero 900, Carl Zeiss Meditec, Oberkochern, Germany). A virtual three-dimensional (3D) DSA road map was obtained from the post-processing of DSA performed before craniotomy (Syngo 3D Roadmap, Siemens Healthcare GmbH, Forchheim, Germany) to facilitate the navigation of the microcatheter. Subsequently, the microcatheter was delivered to a vessel neighboring the shunt point using intraoperative live DSA or a virtual 3D DSA road map. After adequate delivery of the microcatheter, detachable coils were placed to occlude the shunt flow. As per the requirement, liquid embolic agents, such as n-butyl-2-cyanoacrylate (NBCA) (Histoacryl; B. Braun - AESCULAP, Tokyo, Japan) or ethylene vinyl alcohol copolymer (EVOH) (Onyx; Medtronic, Minneapolis, Minnesota, USA), were injected under careful inspection through the continuous acquisition of fluoroscopy. After confirmation of the shunt occlusion, the skull and the scalp incisions were closed. Thereafter, postoperative DSA was conducted under general anesthesia before extubation to verify complete occlusion of the dAVF.
For this case series, the disappearance of the AVFs during the procedure was reviewed from the operative records. Data on age, sex, preoperative symptoms, location of the AVF, Borden classification, presence of previous treatment, modified Rankin Scale (mRS), and postoperative course were retrieved from the patients’ medical records retrospectively.
Patients were followed-up using magnetic resonance imaging (MRI) the next day, and subsequently 3, 6, and 12 months post-embolization, followed by every other year. Additionally, DSA was performed 6 or 12 months after treatment. Complete occlusion of the AVF was defined as the disappearance of a high-intensity signal around the treated shunt point by the time of flight on MRI or the disappearance of shunt flow on postoperative DSA. Complications related to treatment were defined as events that occurred during the procedure or during the hospitalization period.
The preoperative and postoperative mRS scores were compared using the Wilcoxon signed-rank test. All analyses were performed using statistical software (StatView version 5.0, SAS institute, North Carolina, USA).
We reviewed 174 AVF procedures. Of these, 150 procedures were endovascular embolizations, and nine were only direct surgeries. The remaining 14 procedures (13 patients; 10 male; and 3 female) met the inclusion criteria for the combined procedures and the median age was 61 (range 43–81 years). Of these, 10 AVFs were previously treated 1–5 times (median, 1.0). Preoperative mRS was 0 in two AVFs, 1 in six AVFs, 2 in five AVFs, and 3 in one AVF. Ten AVFs were located in the transverse-sigmoid sinus and four in the cortical vein. The Borden grade was II in two AVFs and III in 12 AVFs. Nine of the 14 craniotomy locations were temporo-occipital. The agents used for embolization were coil, EVOH, NBCA, or a combination of these. Immediate occlusion of the AVF was achieved in 13 AVFs, where a gradual occlusion, 4 months after the treatment, was observed in one AVF. [
The mRS scores improved from a median preoperative mRS score of 1 to a median postoperative mRS of 0 (P = 0.006) [
A patient with a left convexity dAVF was previously treated with endovascular embolization of the middle meningeal arteries and occipital arteries using EVOH and could not be occluded. During the procedure combining endovascular embolization and direct surgical approach, intraoperative DSA acquisitions were conducted using the robotic C-arm setup. The obtained images indicated that the residual AVF was fed by the middle cerebral artery and draining vein [
Illustrative case 1 demonstrating setup and exposure of arteriovenous fistula (AVF). (a) Digital subtraction angiography showing an AVF fed by the middle cerebral artery and draining vein into the superior sagittal sinus (arrow). (b) A photograph showing position of a robotic C-arm (arrowheads), and a microscope (arrow). (c) Intraoperative photo of microscope showing the exposed AVF. (d) Color-coded map of indocyanine green videoangiography reveals increased velocity of blood flow in the arterialized draining vein of the AVF.
Illustrative case 1 demonstrating step-by-step occlusion of the arteriovenous fistula (AVF). (a) Intraoperative photo of microscope showing the draining vein occluded by a microvascular clip (arrow). (b) Intraoperative digital subtraction angiography (DSA) after occlusion of the main draining vein disclosed residual shunts and other multiple draining veins which cannot be recognized on preoperative DSA (arrowheads). (c) The cast of ethylene vinyl alcohol copolymer (EVOH) injected via microcatheter is visible under the microscope (arrow) and (d) intraoperative DSA (arrow). (e) Complete occlusion of the AVF is confirmed by indocyanine green videoangiography after the EVOH injection and (f) repeated intraoperative DSA.
A patient with a dAVF of the right latero-cavernous sinus was previously treated with endovascular embolization in another institute and failed to be occluded [
Illustrative case 2 demonstrating exposure of arteriovenous fistula (AVF) and its step-by-step occlusion. (a) Dural AVF is disclosed by magnetic resonance angiography (MRA) (arrow) and (b) digital subtraction angiography (DSA). (c) After fixation of the patient’s head, intraoperative DSA by a robotic C-arm is performed to a create virtual three-dimensional (3D) DSA road map for following catheter delivery. (d) After craniotomy, a distal access catheter (DAC) is introduced in an arterialized draining vein (arrowheads). (e) A microcatheter is advanced through the DAC and detachable coils are placed in the venous pouch neighboring the shunt point under the guidance of a virtual 3D DSA road map (arrow). (f) Complete occlusion of the AVF is verified by postoperative MRA.
In this case series, we reviewed the clinical outcomes of procedures combining endovascular embolization with a direct surgical approach for the treatment of refractory intracranial dAVFs having complex structures. With the combined procedure, we achieved improvement in all cases and curative treatment in most cases. With the aid of the hybrid OR, both endovascular embolization and microsurgery were conducted in a single session in the same room. Although complications were observed, the morbidities were transient or asymptomatic. No case of mortality was observed.
At present, dAVFs are majorly treated with endovascular embolization including TVE or TAE.[
However, this technique has some drawbacks. Bleeding can occur from abnormal vessels within the skull or skin surrounding the AVFs,[
In this technique, we used virtual guidance of 3D DSA road map images acquired by a biplane or robotic angiographic C-arm system to evaluate the live images of AVFs.[
Intraoperative ICG and fluorescein videoangiography are also established modalities to evaluate AVF structure or confirm sufficient occlusion of the shunt points, though they have some shortcomings.[
Procedures combining endovascular embolization with a direct surgical approach can only be performed in a hybrid OR, which requires a substantial monetary investment. As the costs of a hybrid OR depend on its utilization rate, it is difficult to assess the cost-effectiveness of isolated procedures.[
Our study had some limitations. Only a few cases from a single center were included in the study. In future, studies with larger numbers of patients are needed to validate this technique.
The combination of craniotomy and endovascular embolization in a hybrid OR resulted in a good occlusion rate of the AVFs, even in cases where the endovascular access was obliterated by previous embolization or the draining vessels were cortical veins. Although the study involved a small patient population, the outcome was favorable, and the complication rate was low. This technique can be an effective modality for the treatment of refractory intracranial AVFs.
Institutional Review Board (IRB) permission obtained for the study.
Siemens Healthcare K.K.
This study was partially supported by a research grant (ID C00221026) from Siemens Healthcare K.K. Katharina Otani is an employee of Siemens Healthcare K.K.
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