Can the Efficacy of Indocyanine Green Videoangiography in Cerebral Arterio-Venous Malformations Surgery Be Further Improved? To the Editor: We read with great interest the article “Indocyanine Green Angiography in the Surgical Management of Cerebral Arteriovenous Malformations: Lessons Learned in 130 Consecutive Cases” published in the June issue of Operative Neurosurgery.1 The authors present a large case series—in fact, the largest published in the literature so far—in which indocyanine green videoangiography (ICG-VA) was applied in arteriovenous malformation (AVM) surgery. We think this is a key article for all surgeons involved in this fascinating field. Zaidi et al1 clearly highlighted both the advantages and drawbacks of this intraoperative imaging modality, now established worldwide. In particular, they emphasized that ICG-VA remains an adjunctive tool, its main application being “creating a plan of attack for superficially located AVMs.” Interestingly, comparing a cohort of 56 patients operated on with the assistance of ICG-VA with a second cohort of 74 patients who were not, the authors showed that the use of ICG-VA neither statistically reduced the incidence of residual disease nor improved the clinical outcome of patients. Furthermore, it did not prove reliable in detecting residual disease and is less useful in deep-seated lesions. With the limits of our little experience compared with that of Zaidi et al, we completely agree with the authors that ICG-VA cannot substitute for digital subtraction angiography in AVM surgery. However, we would like to highlight the potential integration of ICG-VA within a multimodal approach to reduce some of the limits of such technique. Over the last 2 years, we have used ICG-VA in combination with additional intraoperative tools in a multimodal strategy in 27 patients undergoing cerebral AVM resection. In particular, ICG-VA was used to address 2 specific issues frequently arising during AVM surgery. The first issue is whether ICG-VA can improve the “identification and preservation of en passage vessels resulting in improved clinical outcomes.” This is a remarkable concern when handling an en passage vessel in proximity of motor/ eloquent areas. As stated by the authors, ICG-VA “should be not used as an isolated imaging modality to identify en passage vessels.” Indeed, the flow through the vessel is really quick at times, and ICG-VA can have difficulty detecting the en passage vessel itself. In addition, the en passage vessel is usually tenaciously attached to the malformation, and ICG-VA may not be able to discriminate the artery from the nidus. Furthermore, its complete surgical dissection can be challenging and unsafe, leading to AVM injury. With regard to these specific issues, we combined ICG-VA with both neurophysiological

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monitoring and the occlusion test of the presumed en passage vessel. Whenever ICG-VA identified a large feeder that appeared to go further than the malformation to feed functional areas, it was clipped (Figure), and the AVM resection was carried out in a different site for some time (usually 20 minutes). If the motor evoked potential (MEP) or somatosensory evoked potential (SSEP) remained stable, the vessel could be cut at the site of the clip, and the AVM dissection and resection went on through this plane under neurophysiological monitoring. If an MEP/SSEP amplitude decrease was recorded, the vessel was preserved and the clip removed. The occlusion test was used in 10 of the 23 cases. An MEP decrease was detected in 2 cases; the clip was thus removed, and the dissection proceeded closer to the nidus. No morbidity related to the occlusion test was observed. The second issue is that the evaluation of flow change through the draining veins during resection is crucial because the AVM venous drainage should be interrupted only at the very final stage of dissection to prevent bleeding from the AVM and to avoid an incomplete resection of the nidus. The optimal stage at which the draining vein should be sectioned is when the blood through the vessel is entirely venous, meaning that all arterial feeders to the AVM have been interrupted. This can be detected by watching the drainage getting bluer under high magnification or by checking how quickly the vein fills over time after ICG injection. However, both methods are not accurate enough. ICG-VA cannot provide a quantitative assessment of flow variations. In addition, careful monitoring of such variations often requires a repeated assessment, not available through ICG-VA alone. For this purpose, we used the Microvascular Ultrasonic Flow Probe (Charbel Micro-Flowprobe; Transonic Systems, Inc, Ithaca, New York) to assess blood flow through the draining vein previously identified by ICG-VA (Figure). This tool enables the surgeon to repeatedly assess the flow safely until a complete lack of flow allows safe section of the drainage and complete resection of the AVM. We used this approach in 16 patients, and no residual malformations were detected at immediate postoperative digital subtraction angiography. In conclusion, both of these issues represent crucial stages of AVM resection, and in both cases, ICG-VA alone was, in our experience, not accurate enough to assist in the decision-making process. In both situations, a multimodal approach combining ICG-VA with different techniques may improve the safety and enhance the effectiveness of ICG-VA–assisted resection of AVMs. The actual efficacy of such multimodal approach can be assessed only if shared with and used by other neurosurgeons.

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FIGURE. Representative case of multimodal flow assessment approach in a 64-year-old male patient. A, preoperative digital subtraction angiography showing a right frontoparietal unruptured arteriovenous malformation (AVM) with a transit artery to the motor area. B, functional magnetic resonance imaging (MRI; motor task) showing the functional areas located in close proximity to the malformation. C, AVM exposure through an interhemispheric approach and indocyanine green videoangiography (ICG-VA) to plan the surgical strategy (plan of attack) that cannot discriminate between feeding arteries and transit arteries. D, temporary clip occlusion of a feeding artery (artery 1) under motor evoked potentials (MEPs). E, MEPs decrease detection after 7 minutes. The clip is promptly removed, and artery 1 is preserved and sharply dissected by the nidus. F, a second feeding artery (artery 2) is temporary occluded with a clip under MEP monitoring. G, flow assessment with the Micro-Flowprobe of the transit artery distally to the nidus. The flow is not reduced after the temporary clipping; thus, the artery can be safely sectioned (H). I, no flow detection at the final assessment with the Micro-Flowprobe of venous drainage is the sign of a complete AVM deafferentation. J, final ICG-VA. Neither early venous injection nor residual nidus is detected. The preserved transit artery is still injected by ICG. K, postoperative digital subtraction angiography and (L) MRI performed 48 hours after surgery show neither residual AVM nor strokes. The transit artery is still visible.


VOLUME 75 | NUMBER 6 | DECEMBER 2014 | E733

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Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

Alessandro Della Puppa, MD* Renato Scienza, MD* Oriela Rustemi, MD‡ Giorgio Gioffré, MD‡ *Department of Neurosurgery Padua University Hospital Padua, Italy ‡Department of Neuroscience University Hospital of Padova Padua, Italy 1. Zaidi HA, Abla AA, Nakaji P, Chowdhry SA, Albuquerque FC, Spetzler RF. Indocyanine green angiography in the surgical management of cerebral arteriovenous malformations: lessons learned in 130 consecutive cases. Neurosurgery. 2014;10(suppl 2):246-251.

by difficulties related to operator inexperience with this modality, difficulty in interpreting data, particularly with higher flow lesions, and disruption of work flow during the resection, especially when using the intraoperative microscope. In addition, the Doppler probe can only be used when the draining vein is superficial and accessible to the probe and is not valuable for deep-seated lesions. One additional tool not mentioned by Della Puppa et al is the FLOW 800 imaging software (Carl Zeiss Surgical, Oberkochen, Germany), which provides color-coded overview maps of time to half maximal peak. This may provide a more efficient method for identifying flow via the primary draining vein using indocyanine green angiography, but this tool is again limited to superficially located draining veins.1 We believe that outside of the numerous adjunctive tools available to assist the surgeon during resection of these complex lesions, the most important element to achieving acceptable clinical outcomes is the surgeon's thorough understanding of the relevant surgical anatomy and experience with this complex surgical entity. Disclosure


In Reply: Can the Efficacy of Indocyanine Green Videoangiography in Cerebral Arteriovenous Malformations Surgery Be Further Improved? We thank Della Puppa et al for their generous and well-written comments, and we agree that a multimodal approach is necessary to achieve acceptable clinical outcomes when resecting a cerebral arteriovenous malformation (AVM). Nevertheless, it is important to be aware of the limits of each intraoperative diagnostic tool. For example, Della Puppa et al provide an excellent method for identifying an en passage vessel during resection of an AVM using temporary clip occlusion followed by close electrophysiological monitoring. Although this is one viable alternative, we would like to emphasize that it is only applicable in a very small subset of cases when the en passage vessel in question is feeding the primary motorsensory strip. Often, a redundant vascular supply to these functional regions can buffer any electrophysiological changes. Furthermore, this method is not particularly useful when en passage vessels are supplying the visual or language areas because these structures are not directly assessed during standard intraoperative electrophysiological monitoring. Surgeons should be highly cognizant of these limitations when interpreting the results of a temporary vessel occlusion test. The editorial also advocates the use of the Ultrasonic Flow Probe (Charbel Micro Flowprobe; Transonic Systems, Inc, Ithaca, New York) to assess the amount of residual flow through the draining vein and gain a sense of how much the nidus has been disconnected during the course of the resection. We agree with the authors that this is an important intraoperative tool that should be used in select cases, but, as alluded to in our original article, Doppler probes are often fraught

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The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

Hasan A. Zaidi, MD Robert F. Spetzler, MD Division of Neurological Surgery Barrow Neurological Institute St. Joseph's Hospital and Medical Center Phoenix, Arizona 1. Scerrati A, Della Pepa GM, Conforti G, et al. Indocyanine green video-angiography in neurosurgery: a glance beyond vascular applications. Clin Neurol Neurosurg. 2014;124C:106-113. 10.1227/NEU.0000000000000532

iPod Touch-Assisted Instrumentation of the Spine: Is It Accurate and Reliable? To the Editor: With great interest, we have read the article by Jost et al “iPod Touch-Assisted Instrumentation of the Spine: A Technical Report” in Operative Neurosurgery.1 The authors explored a new method to use an iPod touch application to measure and intraoperatively determine the angles that were used to assist with screw implantation. We agree that the accelerometer- or gyroscope-based applications with handheld devices or smartphones are simple and helpful to measure angles.2-4 However, we cannot replicate the author's method, and we doubt if this method is accurate and reliable. The authors measured the lateromedial angulation on preoperative images and reproduced in the operative field with the iPod touch. However, with the application they used (Angle, Smudge Apps,

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Can the efficacy of indocyanine green videoangiography in cerebral arterio-venous malformations surgery be further improved?

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