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ORIGINAL ARTICLE
Year : 2011  |  Volume : 59  |  Issue : 6  |  Page : 829-832

Preliminary evaluation of the role of surgical microscope-integrated intraoperative FLOW 800 colored indocyanine fluorescence angiography in arteriovenous malformation surgery


1 Department of Neurosurgery, Fujita Health University, Kutsukake-cho, Toyoake, Aichi, Japan
2 Department of Neurosurgery, Seth GS Medical College and King Edward Memorial Hospital, Parel, Mumbai, India

Date of Submission06-Aug-2011
Date of Decision30-Aug-2011
Date of Acceptance02-Sep-2011
Date of Web Publication2-Jan-2012

Correspondence Address:
Yoko Kato
Department of Neurosurgery, Fujita Health University, 1-98 Dengakubakubo, Kutsukakecho, Toyoake, Aichi- 470-1192
Japan
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DOI: 10.4103/0028-3886.91359

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 » Abstract 

Objective: To discuss the role of FLOW 800 innovative software for analytical color visualization and objective evaluation of fluorescence videos obtained by microscope-integrated intraoperative indocyanine green (ICG) fluorescence angiography in arteriovenous malformations (AVM) surgery. Materials and Methods: Microscope-integrated intraoperative FLOW 800 was used and evaluated in three consecutive AVM surgeries over a period of two months. The role of FLOW 800 to distinguish feeding arteries from arterialized veins and other arteries was evaluated. Its advantages and limitations over conventional intraoperative ICG angiography were evaluated. Results: This software was found to be useful in identifying arterial feeders, arterialized veins and other arteries in all the three patients and it gives additional information on the status of AVM before and after clipping suspected feeders which is sometimes difficult to interpret on conventional ICG angiography. Conclusion: Flow 800 is a reliable and useful addition to microscope-integrated color ICG video angiography. Although its role is limited in deep-seated AVMs, if properly dissected and exposed it can give useful information which can be easily interpretable and reproducible.


Keywords: Arteriovenous malformations, FLOW 800, indocyanine green, intraoperative angiography


How to cite this article:
Kato Y, Jhawar SS, Oda J, Watabe T, Oguri D, Sano H, Hirose Y. Preliminary evaluation of the role of surgical microscope-integrated intraoperative FLOW 800 colored indocyanine fluorescence angiography in arteriovenous malformation surgery. Neurol India 2011;59:829-32

How to cite this URL:
Kato Y, Jhawar SS, Oda J, Watabe T, Oguri D, Sano H, Hirose Y. Preliminary evaluation of the role of surgical microscope-integrated intraoperative FLOW 800 colored indocyanine fluorescence angiography in arteriovenous malformation surgery. Neurol India [serial online] 2011 [cited 2014 Sep 20];59:829-32. Available from: http://www.neurologyindia.com/text.asp?2011/59/6/829/91359



 » Introduction Top


Despite recent advances in the fields of embolization and radio surgery, complete surgical extirpation remains the mainstay of the treatment (cure) for arteriovenous malformations (AVMs). The vascular architecture of AVMs is usually very complex involving tortuous feeding arteries, abnormal vascular nidus and draining veins. The role of intraoperative digital subtraction angiography (DSA) in AVM surgery is well established. [1],[2],[3],[4],[5],[6] Intraoperative DSA is reported to have a significant effect on surgical procedure in 7-34% of cases. [1],[2],[5],[6] Intraoperative DSA is technically demanding, expensive, invasive, requires additional time and manpower and has a potential for vascular or neurological injury. [5] These limitations of intraoperative DSA led to development of various noninvasive intraoperative modalities such as Doppler ultrasound imaging, three-dimensional ultrasound angiography and indocyanine green (ICG) fluorescence angiography. [5],[7],[8],[9],[10],[11] ICG fluorescence has proven to be most attractive due its microscopic integration, real-time high-resolution imaging, and ability to differentiate arteries from arterialized veins.

We report another valuable addition to this well-established intraoperative imaging modality. FLOW 800 is an analytical color visualization map and objective evaluation of fluorescence videos obtained by microscope-integrated intraoperative ICG angiography. This map employs colors to instantly identify the direction and sequence of blood flow and is also presented as an intensity diagram with graphical representation. Red represents the initial blood inflow, followed by a gradient color scale for subsequent blood flow sequences giving the temporal relation of blood flow dynamics in a single map.


 » Materials and Methods Top


Technique details

All operations were performed with near infrared video camera and FLOW 800 software-integrated operating microscope (Carl Zeiss Co., Germany). Briefly, the camera records a real-time un-intensified image from the operating microscope through an optical filter that allows only fluorescence in the ICG emission wavelength. The dye is administrated at the surgeon's request and vessel fluorescence appears in 3 to 12 sec and clears within 10 min, allowing for additional injections. After this angiographic video is played and within 30 to 40 sec FLOW 800 map is produced which is displayed on a monitor. In all cases, ICG angiography with FLOW 800 was performed after opening the dura at initial exposure before resection of AVM, after clipping of the suspected feeders, once or twice during the resection after division of feeders as required and once at the completion of excision of the AVM.

Patients

Case 1: An 11-year-old male child presented with headache followed by sudden onset weakness of right-sided limbs. Neurological examination revealed right hemiplegia (Grade 2-3/5 motor power). Cranial computerized tomography (CT) scan showed an acute hematoma on the medial side of the frontal lobe. DSA revealed a Spetzlar Martin Grade II AVM along the medial frontal inter-hemispheric surface fed by branches from the anterior cerebral artery and draining into the superior sagittal sinus [Figure 1]a. The patient underwent right frontoparietal craniotomy with inter-hemispheric approach. An ICG angiography with FLOW 800 study was done on opening the dura before any dissection which showed large vein on medial surface but no nidus [Figure 1]b and c. After inter-gyral dissection another ICG angiography and FLOW 800 study was done to identify the feeders to the AVM [Figure 1]d-f. This made identification of feeders and veins easy and nidus was excised completely. After complete excision of the nidus another study was performed to document the completeness of excision and rule out any residual nidus [Figure 1]g and h. Patient improved in weakness, motor power 4/5 on discharge.
Figure 1: (a) Preoperative anterioposterior (AP) and lateral DSA of case 1 showing a frontal AVM along the medial inter-hemispheric surface supplied by feeders from the anterior and middle cerebral artery branches. (b) Operative photograph showing large draining vein. No major feeders seen on the surface. (c) corresponding FLOW 800 picture. (d) Post-dissection intraoperative photograph showing suspicious feeders. (e), (f) ICG angiogram after dissection and corresponding FLOW 800 showing feeders as bright red and early draining vein as yellow. (g),(h) Post-excision intraoperative photograph and ICG angiogram confirming the total excision

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Case 2: A large right parietal convexity Spetzlar Martin Grade IV AVM was detected incidentally on magnetic resonance imaging (MRI) in a 56-year-old asymptomatic male. He also had an incidental internal carotid artery and posterior communicating artery junction aneurysm. A DSA was performed which showed feeders to the AVM arising from the middle cerebral artery, anterior cerebral artery, posterior cerebral artery, and lateral posterior choroidal artery and draining into the superior sagittal sinus, and deep venous system [Figure 2]. Coiling of the aneurysm was done. The patient underwent three sessions of embolization over eight months. After the third session he developed a sudden-onset left-sided weakness (Grade 0/5 motor power). Cranial CT scan showed a large hematoma in the right parietal lobe with mass effect. A right frontoparietal decompressive craniectomy with hematoma evacuation was done. The patient subsequently underwent AVM surgery six months after the onset of sudden-onset hemiplegia. After exposure of the AVM, an ICG angiography with FLOW 800 study was done showing dilated tortuous vessels. FLOW 800 maps showed arteries as red and arterialized veins as orange or yellow, and normal veins are seen as violet [Figure 3]a-c. A standard resection of the AVM was performed by carefully identifying all the feeders with the aid of microscope-integrated ICG angiography and FLOW 800. Additional injections of ICG and FLOW 800 studies were done after clipping and disconnecting major feeders [Figure 3]d, e. A total excision of AVM was possible without difficulty. There was no residual nidus on final injection of ICG and FLOW 800 study done at the end of the resection of the AVM [Figure 3]f and g. Th epostoperative period was uneventful and there was no improvement in motor power at the two-month follow-up. Postoperative DSA confirmed total excision of the AVM.
Figure 2: Preoperative DSA of Case 2. (a) Right common carotid AP angiogram showing right parietal convexity AVM receiving feeders from the middle cerebral and anterior cerebral artery. An incidental aneurysm also noted at the internal carotid and posterior communicating artery junction. (b) Right lateral vertebral angiogram showing supply from the posterior cerebral artery. Note feeders from the lateral posterior choroidal artery (arrow). (c) Right common carotid AP angiograph after embolization showing diminished feeders from the middle cerebral artery and anterior cerebral artery. (d) Right vertebral AP angiograph post embolization showing deep feeders from the posterior cerebral artery and lateral posterior choroidal artery

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Figure 3: (a) Operative exposure of the right parietal AVM in Case 2. (b) ICG angiographic findings at late arterial phase with early venous filling showing multiple dilated tortuous vessels. (c) Corresponding FLOW 800 image showing color gradient of various vessels helping in identification of the main feeders on the surface (arrows). (d), (e) ICG angiogram after clipping of main feeders and corresponding FLOW 800 image demonstrating color change due to slowing of blood. (f), (g) Post-excision ICG angiogram showing total excision of AVM and corresponding FLOW 800 image

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Case 3: A 50-year-old male presented with sudden-onset behavioral disturbances with irrelevant talking and left-sided weakness. On neurological examination, patient was disorientated to time, place and person and was having impaired higher mental functions and left hemiparesis (Grade 4/5 motor power). Cranial CT scan showed acute intra-parenchymal hematoma in the right posterior, frontal and temporal regions [Figure 4]a. Three-dimensional CT-angiography and DSA revealed an abnormal vasculature area in the region of clot and confirmed the lesion to be Spetzlar Martin Grade II AVM [Figure 4]b and c. Patient underwent emergency clot evacuation followed by elective excision of AVM. A right frontoparietal craniotomy was done [Figure 4]d-f. AVM was identified in the wall of the clot cavity after meticulous dissection with the aid of intraoperative ICG angiography and FLOW 800 [Figure 4]g-i. A total excision of AVM was achieved and confirmed with intraoperative FLOW 800 and ICG angiography [Figure 4]j-l. Postoperatively patient improved in weakness and higher mental functions.
Figure 4: (a) Computerized tomography (CT) scan of Case 3 showing acute hematoma in the right posterior frontal lobe. (b) DSA showing small AVM displaced due to clot. (c) Three-dimensional CT angiogram of the same patient. (d), (e), (f) Intraoperative photograph showing operative exposure and corresponding ICG angiogram with FLOW 800 picture showing no obvious feeders or AVM. (g) Post-dissection intraoperative photograph showing AVM in the wall of the clot cavity. (h), (i) Intraoperative ICG angiogram and corresponding FLOW 800 confirmed the location of the AVM along the wall of the clot cavity. (j) Intraoperative photograph showing complete excision. (k), (l) Post-excision ICG angiogram and FLOW 800 pictures confirming the total excision

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 » Discussion Top


An AVM is a collection of tangled blood vessels where high-pressure blood in distorted abnormal arteries flows directly into large draining veins without the presence of an intervening network of capillaries. Intraoperative DSA has a well-established role and is the gold standard in complex AVM surgery. [4],[5],[6],[11] But it has many disadvantages as described above. Recently, Raabe et al., [12] described a neurosurgical technique for ICG video angiography in which a fluorescent camera is integrated in the microscope to assess intraoperative blood flow in various neurovascular conditions like aneurysm, spinal and cranial dural fistula. The same group later demonstrated the efficacy of microscope-integrated ICG fluorescence angiography in aneurysm surgery and concluded that the modality is an efficient and useful tool for these procedures. [13] Later, the role of ICG angiography was evaluated by the same group in AVM surgery and was found to be a useful tool which can support intraoperative DSA but cannot replace it. [5]

FLOW 800 is a further extension of ICG video angiography, which gives a real-time high-resolution colored visual map of vascular blood flow dynamics in the operative field thus enabling better differentiation of the feeding arteries, normal cortical arteries and draining veins. Information from the infrared video sequences is compiled into visual maps clearly presented at a glance. The real benefit of this technique according to our preliminary observation is its easy interpretation, reproducibility, real-time identification of feeding arteries and side to side comparison of the flow dynamics of AVM before and after clipping, giving the added margin of safety. Conventional ICG depends upon the rate of filling of the vessels to differentiate between arteries and veins, which is difficult to interpret, especially if repeated injections are given over a small interval of time. [5] In this scenario, FLOW 800 gives a different color to different rates of flow in vessels thus making interpretation very easy and more useful. The pinpoint analysis of areas of confusion or doubt on ICG angiography gives graphical information of flow over time, which is another advantage over conventional ICG angiography. Sometimes in AVM surgery, clipping of feeders is required and ICG is repeated before and after clipping to see changes in vascularity of AVMs. in such cases there may be residual ICG giving false-positive findings. So in such situations an intensity diagram is more useful, giving variation of flow over time and helps in differentiating feeders from normal vessels. Apart from this, the technique is safe, inexpensive, quick, and requires no additional human or hardware resources in the operation room. Similar to ICG, multiple injections can be performed without any risk to the patient or operation theatre staff.

FLOW 800 has a few limitations similar to ICG angiography. It is also a surface imaging modality with limited penetration. Its role is limited in deep-seated AVMs in the initial stages of operation but here also if the AVM can be exposed by meticulous dissection, useful information can be obtained. As seen in the first patient it allowed identification of deep feeders in the inter-hemispheric fissure which were not seen on the surface. Similarly, in the third patient we found FLOW 800 more useful compared to conventional ICG in identifying the location of the AVM nidus in the wall of the clot cavity after meticulous exposure.

 
 » References Top

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2.Bauer BL. Intraoperative angiography in cerebral aneurysm and AV-malformation. Neurosurg Rev 1984;7:209-17.  Back to cited text no. 2
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3.Derdeyn CP, Moran CJ, Cross DT, Grubb RL Jr, Dacey RG Jr. Intraoperative digital subtraction angiography: a review of 112 consecutive examinations. AJNR Am J Neuroradiol 1995;16:307-18.  Back to cited text no. 3
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4.Hashimoto H, Iida J, Hironaka Y, Sakaki T. Surgical management of cerebral arteriovenous malformations with intraoperative digital subtraction angiography. J Clin Neurosci 2000;7[Suppl 1]:33-5.  Back to cited text no. 4
    
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6.Vitaz TW, Gaskill-Shipley M, Tomsick T, Tew JM Jr. Utility, safety, and accuracy of intraoperative angiography in the surgical treatment of aneurysms and arteriovenous malformations. AJNR Am J Neuroradiol 1999;20:1457-61.  Back to cited text no. 6
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7.Black KL, Rubin JM, Chandler WF, McGillicuddy JE. Intraoperative colour flow Doppler imaging of AVM's and aneurysms. J Neurosurg 1988;68:635-9.  Back to cited text no. 7
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8.Dempsey RJ, Moftakhar R, Pozniak M. Intraoperative doppler to measure cerebrovascular resistance as a guide to complete resection of arteriovenous malformations. Neurosurgery 2004;55:155-61.  Back to cited text no. 8
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9.Mathiesen T, Peredo I, Edner G, Kihlström L, Svensson M, Ulfarsson E, et al. Neuronavigation for arteriovenous malformation surgery by intraoperative three-dimensional ultrasound angiography. Neurosurgery 2007;60[4 Suppl 2]:345-51.  Back to cited text no. 9
    
10.Wang Y, Wang Y, Wang Y, Taniguchi N, Chen XC. Intraoperative real-time contrast-enhanced ultrasound angiography: A new adjunct in the surgical treatment of arteriovenous malformations. J Neurosurg 2007;107: 959-64.  Back to cited text no. 10
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

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