Perspectives Commentary on: The Utility and Limitations of Intraoperative Near-Infrared Indocyanine Green Videoangiography in Aneurysm Surgery by Sharma et al. pp. E607-E613.
Juha Hernesniemi, M.D., Ph.D. Professor and Chairman Department of Neurosurgery Helsinki University Central Hospital
Intraoperative Assessment of a Quality of Microneurosurgical Clipping: Role of Indocyanine Green Videoangiography Reza Dashti1 and Juha Hernesniemi2
D
espite recent technical and technological advancements in the microneurosurgical management of intracranial aneurysms, neck residuals or inadvertent occlusion of adjacent vessels can alter the efficacy and safety of treatment. Postoperative unexpected findings are not infrequent, even in experienced hands. On the basis of our experience, in a consecutive series of 622 patients with 808 clipped aneurysms, postoperative angiography revealed neck remnants in 9%, dome residuals in 3%, and major vessel occlusion in 5% of cases (4). Regrowth or rebleeding of a partially clipped aneurysm can have significant impact on patient outcomes. Similarly, ischemic consequences of inadvertent occlusion of a vessel during clipping may be irreversible and devastating. Detection of such findings in postoperative imaging studies necessitate redo surgeries with questionable outcomes and can increase the duration and costs of treatment significantly. Intraoperative assessment of quality of clipping and immediate replacement of clip(s) may have great impact on the efficacy and safety of treatment.
Among the different techniques of intraoperative assessment of clipping, conventional angiogram is considered the gold standard. However, cost-effectiveness, limited availability, length of procedure, and safety concerns have limited its routine application. In addition, resolution of an intraoperative angiogram is not enough to assess the patency of perforating branches in majority of cases. Microvascular Doppler is used widely during aneurysm surgery. This is a rather cost-effective and available method; however, nonquantitative measurement, limited ability to detect
Key words - Aneurysm - Indocyanine green - Near-infrared - Surgery - Videoangiography
Abbreviations and Acronyms DSA: Digital subtraction angiography ICG-VA: Indocyanine green video angiography
WORLD NEUROSURGERY 82 [5]: e589-e590, NOVEMBER 2014
residual filling of an aneurysm, and inability to assess the patency of perforating branches are major disadvantages. Ultrasonic perivascular microprobe has the great advantage of quantitative measurement of blood flow in the parent and branching vessels (1); however, evaluation of perforating branches is not possible. After its introduction by Raabe et al. (6), microscope-integrated indocyanine green video angiography (ICG-VA) has been used with increasing popularity for the treatment of cerebrovascular lesions. This technique is based on detection of indocyanine green (ICG) dye fluorescence, which is injected intravenously, by an infrared camera mounted on operating microscope. An angiographic image with arterial, capillary, and venous phases is obtained in real time, and recorded loops are repeatable. A dose of 0.2 0.5 mg/kg with maximum daily dose limit of 5 mg/kg is recommended (6). ICG-VA is a noninvasive, safe, practical, and cost-effective way of intraoperative assessment of blood flow (2, 3, 5, 6). One of the unique features of ICG-VA is to create high-resolution images obtained under the magnification of an operating microscope. Immediate real-time assessment of patency of parent, branching, and, in particular, perforating arteries is a major advantage of ICG-VA compared with other available techniques. Additionally, ICG-VA can detect residual filling and remnants of a clipped aneurysm. Immediate correction of an improperly placed clip prevents ischemic and hemorrhagic complications of surgery to a great extent. Other applications of ICG-VA in neurosurgery include surgery of brain and spinal cord
From the 1Department of Neurosurgery, University of Illinois at Chicago, Chicago, Illinois, USA; and 2Department of Neurosurgery, Helsinki University Central Hospital, Helsinki, Finland To whom correspondence should be addressed: Prof. Juha Hernesniemi, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 5:e589-e590. http://dx.doi.org/10.1016/j.wneu.2014.08.060
www.WORLDNEUROSURGERY.org
e589
PERSPECTIVES
arteriovenous malformations and fistulas, bypass and revascularization procedures, surgery of hypervascular tumors, evaluation of cortical perfusion, and preservation of venous flow particularly during retraction and surgical manipulations.
residual filling. Interpretation of findings of ICG-VA is of paramount importance, and the learning curve is rather steep. In case of partially or completely occluded vessels, a retrograde flow via collaterals can be confusing.
To date, few clinical studies with large sample size demonstrated acceptable efficacy and sensitivity of ICG-VA both in detection of aneurysms remnants and also inadvertent vessel compromise (2, 3, 5-8). In 2009 we published a series of 239 aneurysms in 190 patients who underwent operation (2). We compared the results of intraoperative ICG-VA with postoperative computed tomography angiography and/or digitally subtracted angiography. Unexpected neck remnants were detected in approximately 6% of aneurysms. Similarly, unexpected aneurysm residuals were detected in approximately 6% of aneurysms. Residuals were noted more frequently in deepsited locations, with the anterior communicating complex being the most common. On the basis of our published and unpublished experience, deep location of aneurysm in the operative filed, aneurysm and vessel wall calcifications, intramural thrombi, and large or giant aneurysm size are among important factors responsible for unexpected findings on ICG-VA. Furthermore, arachnoid adhesions and the presence of blood, cottonoids, and similar materials in the operative field can have a major impact on quality of obtained images.
In this issue of WORLD NEUROSURGERY, Sharma et al. have presented a retrospective study included a series of 112 consecutive patients with 126 aneurysms underwent ICG-VA during microneurosurgical clipping between 2008 and 2013. This was a single-surgeon series with the aim of elimination of interobserver differences of ICG-VA results. No other methods of intraoperative assessment of blood flow were applied in this series. The results of intraoperative ICG-VA were compared with the results of postoperative DSA, which were obtained on postoperative day 1 5. According to results of this study, ICG-VA resulted in intraoperative replacement of the clip in 10 patients (8%). Furthermore, discordance between ICG-VA and postoperative digital subtraction angiography (DSA) was observed in 4% of cases. The location of the aneurysm on ophthalmic segment of ICA was reported to increase the likelihood of discordance between the results. On the basis of their results, Sharma et al. supported routine use of ICG-VA during aneurysm surgery. However, they concluded that the technique is not adequate for assessment of clipping in ICA-ophthalmic segment aneurysms. The use of intraoperative angiogram in this subgroup of aneurysms was recommended.
ICG-VA has technical and practical limitations. This technique cannot be used to provide quantitative measurement of flow. Difficulty to assess that part of aneurysm base obscured in the operative field is a major limitation of technique. The quality of obtained ICG-VA images can be greatly operator/observer dependent. Visualization of inadequately dissected vessels or aneurysms hidden behind thickened arachnoid bands increases the risk of false findings. Injection of an inadequate dose of ICG or repeating a study in intervals shorter than half-life of ICG also may cause a false impression of vessel patency. Additionally, remnants of ICG in the dome of a perfectly clipped aneurysm may be considered as
The authors should be commended for their work. This study has some limitations that are honestly discussed by authors. The greater likelihood of unexpected results for ophthalmic aneurysms could be the result of uneven distribution of aneurysm locations in this series. Based on our experience, we agree with the utility of intraoperative DSA for all large, giant, and complex aneurysms with calcified walls and/or intramural thrombi. Furthermore, we recommend application of other noninvasive methods of intraoperative blood flow assessment to augment the findings of ICG-VA. Similarly, immediate postoperative DSA should be considered for all aneurysms with questionable intraoperative assessments.
REFERENCES 1. Charbel FT, Hoffman WE, Misra M, Hannigan K, Ausman JI: Role of a perivascular ultrasonic microflow probe in aneurysm surgery. Neurol Med Chir (Tokyo) 38(Suppl):35-38, 1998. 2. Dashti R, Laakso A, Niemela M, Porras M, Hernesniemi J: Microscope-integrated nearinfrared indocyanine green videoangiography during surgery of intracranial aneurysms: the Helsinki experience. Surg Neurol 71:543-550; discussion 550, 2009. 3. Hardesty DA, Thind H, Zabramski JM, Spetzler RF, Nakaji P: Safety, efficacy, and cost of intraoperative indocyanine green angiography compared to intraoperative catheter angiography in cerebral aneurysm surgery. J Clin Neurosci 21:1377-1382, 2014.
e590
www.SCIENCEDIRECT.com
4. Kivisaari RP, Porras M, Ohman J, Siironen J, Ishii K, Hernesniemi J: Routine cerebral angiography after surgery for saccular aneurysms: is it worth it? Neurosurgery 55:1015-1024, 2004. 5. Ozgiray E, Akture E, Patel N, Baggott C, Bozkurt M, Niemann D, Baskaya MK: How reliable and accurate is indocyanine green video angiography in the evaluation of aneurysm obliteration? Clin Neurol Neurosurg 115:870-878, 2013. 6. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V: Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52: 132-139; discussion 139, 2003. 7. Scerrati A, Della Pepa GM, Conforti G, Sabatino G, Puca A, Albanese A, Maira G, Marchese E, Esposito G: Indocyanine green video-angiography in neurosurgery: a glance beyond vascular applications. Clin Neurol Neurosurg 124C:106-113, 2014.
8. Washington CW, Zipfel GJ, Chicoine MR, Derdeyn CP, Rich KM, Moran CP, Cross DT, Dacey RG Jr: Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg 118:420-427, 2013.
Citation: World Neurosurg. (2014) 82, 5:e589-e590. http://dx.doi.org/10.1016/j.wneu.2014.08.060 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Published by Elsevier Inc.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.08.060
Juha Hernesniemi, M.D., Ph.D. Professor and Chairman Department of Neurosurgery Helsinki University Central Hospital
Intraoperative Assessment of a Quality of Microneurosurgical Clipping: Role of Indocyanine Green Videoangiography Reza Dashti1 and Juha Hernesniemi2
D
espite recent technical and technological advancements in the microneurosurgical management of intracranial aneurysms, neck residuals or inadvertent occlusion of adjacent vessels can alter the efficacy and safety of treatment. Postoperative unexpected findings are not infrequent, even in experienced hands. On the basis of our experience, in a consecutive series of 622 patients with 808 clipped aneurysms, postoperative angiography revealed neck remnants in 9%, dome residuals in 3%, and major vessel occlusion in 5% of cases (4). Regrowth or rebleeding of a partially clipped aneurysm can have significant impact on patient outcomes. Similarly, ischemic consequences of inadvertent occlusion of a vessel during clipping may be irreversible and devastating. Detection of such findings in postoperative imaging studies necessitate redo surgeries with questionable outcomes and can increase the duration and costs of treatment significantly. Intraoperative assessment of quality of clipping and immediate replacement of clip(s) may have great impact on the efficacy and safety of treatment.
Among the different techniques of intraoperative assessment of clipping, conventional angiogram is considered the gold standard. However, cost-effectiveness, limited availability, length of procedure, and safety concerns have limited its routine application. In addition, resolution of an intraoperative angiogram is not enough to assess the patency of perforating branches in majority of cases. Microvascular Doppler is used widely during aneurysm surgery. This is a rather cost-effective and available method; however, nonquantitative measurement, limited ability to detect
Key words - Aneurysm - Indocyanine green - Near-infrared - Surgery - Videoangiography
Abbreviations and Acronyms DSA: Digital subtraction angiography ICG-VA: Indocyanine green video angiography
WORLD NEUROSURGERY 82 [5]: e589-e590, NOVEMBER 2014
residual filling of an aneurysm, and inability to assess the patency of perforating branches are major disadvantages. Ultrasonic perivascular microprobe has the great advantage of quantitative measurement of blood flow in the parent and branching vessels (1); however, evaluation of perforating branches is not possible. After its introduction by Raabe et al. (6), microscope-integrated indocyanine green video angiography (ICG-VA) has been used with increasing popularity for the treatment of cerebrovascular lesions. This technique is based on detection of indocyanine green (ICG) dye fluorescence, which is injected intravenously, by an infrared camera mounted on operating microscope. An angiographic image with arterial, capillary, and venous phases is obtained in real time, and recorded loops are repeatable. A dose of 0.2 0.5 mg/kg with maximum daily dose limit of 5 mg/kg is recommended (6). ICG-VA is a noninvasive, safe, practical, and cost-effective way of intraoperative assessment of blood flow (2, 3, 5, 6). One of the unique features of ICG-VA is to create high-resolution images obtained under the magnification of an operating microscope. Immediate real-time assessment of patency of parent, branching, and, in particular, perforating arteries is a major advantage of ICG-VA compared with other available techniques. Additionally, ICG-VA can detect residual filling and remnants of a clipped aneurysm. Immediate correction of an improperly placed clip prevents ischemic and hemorrhagic complications of surgery to a great extent. Other applications of ICG-VA in neurosurgery include surgery of brain and spinal cord
From the 1Department of Neurosurgery, University of Illinois at Chicago, Chicago, Illinois, USA; and 2Department of Neurosurgery, Helsinki University Central Hospital, Helsinki, Finland To whom correspondence should be addressed: Prof. Juha Hernesniemi, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 5:e589-e590. http://dx.doi.org/10.1016/j.wneu.2014.08.060
www.WORLDNEUROSURGERY.org
e589
PERSPECTIVES
arteriovenous malformations and fistulas, bypass and revascularization procedures, surgery of hypervascular tumors, evaluation of cortical perfusion, and preservation of venous flow particularly during retraction and surgical manipulations.
residual filling. Interpretation of findings of ICG-VA is of paramount importance, and the learning curve is rather steep. In case of partially or completely occluded vessels, a retrograde flow via collaterals can be confusing.
To date, few clinical studies with large sample size demonstrated acceptable efficacy and sensitivity of ICG-VA both in detection of aneurysms remnants and also inadvertent vessel compromise (2, 3, 5-8). In 2009 we published a series of 239 aneurysms in 190 patients who underwent operation (2). We compared the results of intraoperative ICG-VA with postoperative computed tomography angiography and/or digitally subtracted angiography. Unexpected neck remnants were detected in approximately 6% of aneurysms. Similarly, unexpected aneurysm residuals were detected in approximately 6% of aneurysms. Residuals were noted more frequently in deepsited locations, with the anterior communicating complex being the most common. On the basis of our published and unpublished experience, deep location of aneurysm in the operative filed, aneurysm and vessel wall calcifications, intramural thrombi, and large or giant aneurysm size are among important factors responsible for unexpected findings on ICG-VA. Furthermore, arachnoid adhesions and the presence of blood, cottonoids, and similar materials in the operative field can have a major impact on quality of obtained images.
In this issue of WORLD NEUROSURGERY, Sharma et al. have presented a retrospective study included a series of 112 consecutive patients with 126 aneurysms underwent ICG-VA during microneurosurgical clipping between 2008 and 2013. This was a single-surgeon series with the aim of elimination of interobserver differences of ICG-VA results. No other methods of intraoperative assessment of blood flow were applied in this series. The results of intraoperative ICG-VA were compared with the results of postoperative DSA, which were obtained on postoperative day 1 5. According to results of this study, ICG-VA resulted in intraoperative replacement of the clip in 10 patients (8%). Furthermore, discordance between ICG-VA and postoperative digital subtraction angiography (DSA) was observed in 4% of cases. The location of the aneurysm on ophthalmic segment of ICA was reported to increase the likelihood of discordance between the results. On the basis of their results, Sharma et al. supported routine use of ICG-VA during aneurysm surgery. However, they concluded that the technique is not adequate for assessment of clipping in ICA-ophthalmic segment aneurysms. The use of intraoperative angiogram in this subgroup of aneurysms was recommended.
ICG-VA has technical and practical limitations. This technique cannot be used to provide quantitative measurement of flow. Difficulty to assess that part of aneurysm base obscured in the operative field is a major limitation of technique. The quality of obtained ICG-VA images can be greatly operator/observer dependent. Visualization of inadequately dissected vessels or aneurysms hidden behind thickened arachnoid bands increases the risk of false findings. Injection of an inadequate dose of ICG or repeating a study in intervals shorter than half-life of ICG also may cause a false impression of vessel patency. Additionally, remnants of ICG in the dome of a perfectly clipped aneurysm may be considered as
The authors should be commended for their work. This study has some limitations that are honestly discussed by authors. The greater likelihood of unexpected results for ophthalmic aneurysms could be the result of uneven distribution of aneurysm locations in this series. Based on our experience, we agree with the utility of intraoperative DSA for all large, giant, and complex aneurysms with calcified walls and/or intramural thrombi. Furthermore, we recommend application of other noninvasive methods of intraoperative blood flow assessment to augment the findings of ICG-VA. Similarly, immediate postoperative DSA should be considered for all aneurysms with questionable intraoperative assessments.
REFERENCES 1. Charbel FT, Hoffman WE, Misra M, Hannigan K, Ausman JI: Role of a perivascular ultrasonic microflow probe in aneurysm surgery. Neurol Med Chir (Tokyo) 38(Suppl):35-38, 1998. 2. Dashti R, Laakso A, Niemela M, Porras M, Hernesniemi J: Microscope-integrated nearinfrared indocyanine green videoangiography during surgery of intracranial aneurysms: the Helsinki experience. Surg Neurol 71:543-550; discussion 550, 2009. 3. Hardesty DA, Thind H, Zabramski JM, Spetzler RF, Nakaji P: Safety, efficacy, and cost of intraoperative indocyanine green angiography compared to intraoperative catheter angiography in cerebral aneurysm surgery. J Clin Neurosci 21:1377-1382, 2014.
e590
www.SCIENCEDIRECT.com
4. Kivisaari RP, Porras M, Ohman J, Siironen J, Ishii K, Hernesniemi J: Routine cerebral angiography after surgery for saccular aneurysms: is it worth it? Neurosurgery 55:1015-1024, 2004. 5. Ozgiray E, Akture E, Patel N, Baggott C, Bozkurt M, Niemann D, Baskaya MK: How reliable and accurate is indocyanine green video angiography in the evaluation of aneurysm obliteration? Clin Neurol Neurosurg 115:870-878, 2013. 6. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V: Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52: 132-139; discussion 139, 2003. 7. Scerrati A, Della Pepa GM, Conforti G, Sabatino G, Puca A, Albanese A, Maira G, Marchese E, Esposito G: Indocyanine green video-angiography in neurosurgery: a glance beyond vascular applications. Clin Neurol Neurosurg 124C:106-113, 2014.
8. Washington CW, Zipfel GJ, Chicoine MR, Derdeyn CP, Rich KM, Moran CP, Cross DT, Dacey RG Jr: Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg 118:420-427, 2013.
Citation: World Neurosurg. (2014) 82, 5:e589-e590. http://dx.doi.org/10.1016/j.wneu.2014.08.060 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Published by Elsevier Inc.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2014.08.060
