- Department of Neurosurgery, Saitama Medical Center, Saitama Medical University, 1981 Kamoda, Kawagoe, Saitama 350-8550, Japan
Department of Neurosurgery, Saitama Medical Center, Saitama Medical University, 1981 Kamoda, Kawagoe, Saitama 350-8550, Japan
DOI:10.4103/2152-7806.157445Copyright: © 2015 Oya S. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
How to cite this article: Oya S, Nejo T, Fujisawa N, Tsuchiya T, Indo M, Nakamura T, Matsui T. Usefulness of repetitive intraoperative indocyanine green-based videoangiography to confirm complete obliteration of micro-arteriovenous malformations. Surg Neurol Int 21-May-2015;6:85
How to cite this URL: Oya S, Nejo T, Fujisawa N, Tsuchiya T, Indo M, Nakamura T, Matsui T. Usefulness of repetitive intraoperative indocyanine green-based videoangiography to confirm complete obliteration of micro-arteriovenous malformations. Surg Neurol Int 21-May-2015;6:85. Available from: http://surgicalneurologyint.com/surgicalint_articles/usefulness-repetitive-intraoperative-indocyanine-green%e2%80%91based/
Background:It is difficult to intraoperatively confirm the total disappearance of arteriovenous (AV) shunts during surgery for microarteriovenous malformations (micro-AVMs), especially when the nidus is extremely small or diffuse on preoperative angiography. Although intraoperative angiography is effective for evaluating residual shunts, procedure-related risks raise important concerns. The purpose of this study was to assess the usefulness of intraoperative indocyanine green-based videoangiography (ICG–VA) to determine complete disappearance of micro-AVMs during surgery.
Methods:We retrospectively analyzed eight patients with ruptured micro-AVMs who were treated using craniotomy with ICG–VA at our institution.
Results:Two patients underwent emergency partial evacuation of hematoma and external decompression before the diagnostic angiography. While three patients had a nidus smaller than 1 cm, five patients had only early draining veins without an appreciable nidus. The draining veins were superficial in six cases and deep in two cases. The average interval from onset to surgery was 33 days (range, 2–57). ICG–VA was repetitively conducted until disappearance of the AV shunt was confirmed. No residual AV shunt was observed on postoperative radiological examinations. In all cases, the diagnosis of AVM was confirmed from the results of postoperative pathological examination.
Conclusions:ICG–VA could detect early draining veins more clearly in situ than diagnostic angiography. Although it is not as effective for visualizing lesions with deep draining veins, repetitive ICG–VA was safe and effective for confirming the disappearance of AV shunts with superficial drainage.
Keywords: Arteriovenous malformation, hematoma, indocyanine green-based videoangiography, microarteriovenous malformation
Since Margolis emphasized small cerebrovascular malformations as an important cause of intracerebral hemorrhage (ICH),[
Patients, diagnosis, and treatment strategies
This study was approved by the Saitama Medical Center Institutional Review Board (No. 954). Between January 2011 and April 2014, 19 patients with AVM were treated at the Saitama Medical Center: There were 2 cases of unruptured AVM and 17 of ruptured AVM. In the present study, micro-AVM was angiographically defined as an AVM with a nidus smaller than 1 cm or as an early draining vein without an angiographically appreciable nidus.[
Our policy regarding the treatment of ICH in young patients or atypically located hypertensive ICH is to investigate the pathology of the hemorrhage using angiography as well as 3D-CT angiography and magnetic resonance (MR) imaging. When the patients’ condition is critical because of the mass effect of the hematoma, emergency partial evacuation of the hematoma and external decompression are conducted before the angiography. Because a small nidus may not be visible even on angiograms recorded in the acute phase of hemorrhage, we carefully examined digital subtraction angiography images, especially for cases of lobar hemorrhage in young patients with no history of hypertension. If the result of the initial angiography performed immediately after onset is negative, angiography is repeated 4–6 weeks after hematoma onset. To delineate the early draining vein clearly on angiography, we obtain images with a short serial duration (12 shots per second) and a double dose of contrast medium. Patients diagnosed with micro-AVMs were scheduled for craniotomy and resection of superficial micro-AVMs.
Surgical technique and intraoperative ICG–VA
The patient's head was fixed in a 3-pin Mayfield headholder. The Stealth Navigation system (Medtronic, Surgical Navigation Technologies, Louisville, CO) was set up to confirm the location of the small nidus in the operative field. After standard craniotomy was performed to create ample space for surgery, ICG–VA was routinely conducted, and early draining veins were visualized. To compare early draining veins and normally irrigating veins, it was important to adequately expose the cortex. ICG dye diluted to 2.5 mg/mL was injected intravenously as a bolus (0.1 mg/kg of ICG dye, followed by 20 mL of saline). Vessels were visualized using surgical microscopes integrated with a video camera (OPMI PENTERO with INFRARED 800 microscope [Carl Zeiss, Oberkochen, Germany] or M720 OH5 [Leica Microsystems, Heerbrugg, Switzerland]). ICG–VA was performed to confirm the disappearance of the early draining vein when complete shunt obliteration was suspected. If the targeted early draining vein was still visualized on angiography, exploration of the small nidus remaining on the hematoma walls was continued. The ICG–VA was repeated until all the veins around the hematoma could be visualized in the normal venous phase. Postoperative angiography or MR imaging was performed 1–2 weeks after the surgery to confirm total obliteration of AV shunts.
The patient characteristics and outcomes are summarized in [
Six patients showed complete recovery (modified Rankin Scale [mRS] 0), while two experienced moderate neurological deficits rated as mRS 2 and 3). The deficits were attributed to initial damage due to the hemorrhage and were not considered surgical complication. The average duration of follow-up was 5.2 months (range, 1.2–15.5). The disappearance of the AV shunt was postoperatively confirmed on angiography in seven cases and on MR images in one case.
A 43-year-old male with no past medical history woke up one day with a severe headache, nausea, and subjective visual disturbance. On admission, neurological examination showed slight disturbance of consciousness and homonymous hemianopia on the left side. An emergency CT scan showed a 5.3 × 2.2 × 3.8 cm-sized ICH in the right parietal lobe [
(a) CT scan at admission showing an intracerebral hemorrhage in the right parietal lobe. (b) A left internal carotid angiogram on admission showing no definitive vascular abnormality. (c) A time-of-flight MR image showing a small but abnormally dilated vein (arrow) near the hematoma. (d) A left internal carotid angiogram repeated in 2 weeks clearly showing the early draining vein (arrowhead) near the hematoma
(a) A photograph showing cortical arteries and veins around the hematoma. (b) Initial ICG–VA showing an early draining vein (arrow) (c) ICG–VA in the late venous phase showing the hematoma cavity as a dark area (*). (d) A photograph showing that the evacuation was almost complete. (e) Second ICG–VA showing the disappearance of the early draining vein (arrowhead). However, another early draining vein (arrowhead) is visible near the hematoma cavity. (f) Final ICG–VA confirming the complete disappearance of all drainers. (g) Postoperative angiogram showing no residual nidus (arrowhead)
In the present study, we examined the usefulness and limitations of ICG–VA during surgical treatment for micro-AVMs. We highlighted some diagnostic and operative tips specific for micro-AVMs and not large AVMs. Our technique using ICG–VA seem especially useful for intraoperative confirmation of complete AV shunt obliteration.
Problems related to the preoperative diagnosis of micro-AVMs and the importance of in situ evaluation of early venous drainage using ICG–VA
Despite their small size, micro-AVM can cause large hematomas, leading to serious neurological impairments.[
Effectiveness of ICG–VA in confirming total obliteration of AV shunts for micro-AVMs or diffuse AVMs
Localization of the nidus and drainer is of paramount importance in micro-AVM surgery in order to ensure complete AV shunt obliteration,[
In most cases of compact AVMs with a medium-to-large nidus, surgeons are usually able to find the lesion easily and ensure complete obliteration of AV shunts by visual confirmation of changes in the color of the drainer. This empirical judgment can be rationally reinforced by intraoperative angiography, which may also help improve the obliteration rate.[
To our knowledge, the clinical significance of intraoperative angiography for micro-AVMs has not been discussed previously, but given the preoperative difficulties in lesion delineation, its effectiveness would probably be limited. Identification of residual AV shunt after surgical resection is critical because partial resection of AVMs may increase the risk of hemorrhage.[
Takagi et al. described the case of a 2-year-old patient with a diffuse AVM.[
(a) CT scan at admission showing an intracerebral hematoma in the left frontoparietal region. (b) A left internal carotid angiogram at admission showing no abnormal findings that could explain the hemorrhage. (c) A CT scan captured 8 years after the initial episode showing hematoma recurrence at the same location as that when the patient first presented with disturbed consciousness. (d) A left internal carotid angiogram showing a diffuse AVM
If the early draining vein had been detected on ICG–VA in situ during the evacuation surgery, we could have followed the vein and rigorously searched for hidden AV shunts. Zaidi et al. recently reported that the significance of intraoperative ICG–VA alone did not improve the identification of residual nidus and clinical outcome based on the data of 56 patients with AVM treated using ICG.[
Limitations of ICG–VA
There are some limitations regarding the use of ICG–VA. Deep-seated lesions are not visualized on ICG–VA.[
ICG–VA is a powerful tool for in situ localization of AV shunts of micro-AVMs with superficial drainage. It is also extremely useful for confirming complete obliteration of AV shunts for such micro-AVMs. We believe that repetitive ICG–VA contributes to reducing the chances of residual AV shunts, especially micro-AVMs.
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