British Journal of Neurosurgery, October 2014; 28(5): 658–662 © 2014 The Neurosurgical Foundation ISSN: 0268-8697 print / ISSN 1360-046X online DOI: 10.3109/02688697.2014.889811
ORIGINAL ARTICLE
False-negative indocyanine green videoangiography among complex unruptured middle cerebral artery aneurysms: The importance of further aneurysm inspection Charles Kulwin & Aaron A. Cohen-Gadol Department of Neurological Surgery, Goodman Campbell Brain and Spine, Indiana University, Indianapolis, IN, USA
of these goals are confounded by the discrepancy between the outer and inner vessel wall topologic discrepancies; this difference increases with vessel wall thickness.1 In the presence of significant vessel wall atherosclerosis, clip blades that externally appear to occlude only the aneurysm neck may internally occlude the parent vessel lumen, or conversely, clip blades that externally appear to leave a remnant may in fact result in complete occlusion. To evaluate internal aneurysm and vessel lumen topology, a variety of intraoperative adjuncts are available, including microdoppler ultrasound,2 digital subtraction angiography (DSA),3 and indocyanine green videoangiography (ICG-VA).4 Drawbacks to DSA include invasiveness and morbidity, logistic difficulties, and significant resource requirements.5 ICG-VA negates these factors, requiring only near-infrared imaging integration within the operative microscope and the intravenous access already in place for the procedure. Although concordance rates between ICG-VA and DSA are very high,6–8 DSA remains the gold standard. The ability to visualize local small perforators is more pronounced with ICG-VA.9 A false-negative ICG-VA study may result in suboptimal clip placement, exposing the patient to further hemorrhage risk and/or postoperative stroke due to aneurysm remnant or branching or perforating vessel occlusion. In a technically adequate study, ICG-VA may be limited by field-of-view limitations, which may be more common among aneurysms of the anterior communicating artery complex.6,10 An undescribed risk for a false-negative ICG-VA study is an atherosclerotic aneurysm or decreased flow within the dome. In this study, we describe our experience with cases of middle cerebral artery (MCA) aneurysms with false-negative ICG-VA studies requiring clip adjustment for optimal surgical treatment.
Abstract Successful surgical treatment of cerebral aneurysms requires complete occlusion of the aneurysm lumen while maintaining patency of the adjacent branching and perforating arteries. Intraoperative flow assessment allows aneurysm clip repositioning in the event these requirements are not met, avoiding the risk of postoperative rehemorrhage or infarction. A number of modalities have been proposed for primarily intraoperative qualitative blood flow assessment, including microdoppler ultrasonography, intraoperative digital subtraction angiography (DSA), and more recently noninvasive fluorescent angiography including indocyanine green (ICG) fluorescent imaging. Puncture of the aneurysm dome to exclude aneurysm sac filling may also assess the efficacy of clip placement. Although a high concordance between ICG and DSA has been reported, there remains an important subset of aneurysms for which negative ICG study may erroneously suggest aneurysm occlusion. A high-risk situation for such a false-negative study is an atherosclerotic middle cerebral artery (MCA) aneurysm in which vessel wall plaque interferes with the ICG signal. Furthermore, a decreased flow within the aneurysm may not allow enough emission light for detection under the current technology. In this report, we describe our experience with cases of MCA aneurysms with false-negative ICG-VA studies requiring clip adjustment for optimal surgical treatment and discuss two illustrative cases of MCA aneurysms with intraoperative fluorescence studies that were falsely negative, requiring puncture of the aneurysm to correctly identify incomplete aneurysm occlusion. Keywords: aneurysm; false negative; indocyanine green; microsurgical clipping
Introduction
Case 1
Cerebral aneurysm treatment centers on the prevention of future aneurysmal hemorrhage. Protection from hemorrhage is accomplished when the aneurysm lumen is fully occluded, no longer exposed to arterial flow. During microsurgery, both
A 33-year-old woman presented with an incidentally discovered right MCA aneurysm during a work-up for headaches. Pre-operative arteriogram demonstrated a 10-mm
Correspondence: Aaron A. Cohen-Gadol, MD, MSc, Department of Neurological Surgery, Goodman Campbell Brain and Spine, Indiana University School of Medicine, 355 W. 16th St, Suite 5100, Indianapolis, IN 46202, USA. Tel: ⫹ 317-362-8760. Fax: ⫹ 317-924-8472. E-mail: [email protected] Received for publication 7 November 2013; accepted 26 January 2014
658
False-negative indocyanine green videoangiography 659 broad-based aneurysm at the M1 bifurcation pointing inferolaterally (Fig. 1a). After a frontotemporal craniotomy and dissection of the M1 and M2 branches, including the aneurysm neck and dome, no significant evidence of calcification or atherosclerosis was encountered along the vascular tree upon careful intraoperative inspection (Fig. 1b). One curved titanium clip was placed to completely occlude the aneurysm neck while maintaining parent vessel patency under temporary M1 occlusion and burst suppression. The clip blades spanned the entire neck of the aneurysm (Fig. 1c). ICG-VA and fluorescein angiography were subsequently performed. Both fluorescent modalities demonstrated good M1 and M2 patency with no fluorescent signal detectable within the aneurysm sac (Fig. 1d). To confirm successful aneurysm occlusion, the dome of the aneurysm was directly punctured, revealing steady arterial filling of the aneurysm dome (Fig. 1e). A second slightly longer and curved aneurysm clip was then positioned to prevent further filling of the aneurysm sac. Postoperative DSA revealed no aneurysm filling, neck remnant, or vessel stenosis. The patient was discharged home on the second postoperative day with no complication.
Case 2 A 63-year-old woman was diagnosed with an incidentally discovered right MCA aneurysm on a pre-operative DSA that demonstrated a 16-mm inferiorly pointing aneurysm
incorporating the base of both M2 trunks (Fig. 2a). Intraoperative microdissection disclosed a moderately patchy atherosclerotic aneurysm neck and dome (Fig. 2b). A curved clip was applied onto the aneurysm neck to occlude the aneurysm sac. Two additional reinforcing clips, including a shorter straight clip and a longer fenestrated clip, were also applied because of the evidence of atherosclerosis within the neck of the aneurysm (Fig. 2c). ICG-VA clearly demonstrated parent vessel patency and no fluorescent signal within the aneurysm dome (Fig. 2d). At this point, the dome of the aneurysm was directly punctured, revealing highly pressurized arterial bleeding (Fig. 2e). Under temporary proximal vascular occlusion, the final two clips were repositioned and no further bleeding was noted. Postoperative DSA showed no aneurysm filling, neck remnant, or vessel stenosis. The patient awoke at her preoperative baseline and was subsequently discharged after resolution of exacerbation of chronic obstructive pulmonary disease, on the 7th postoperative day.
Discussion Published concordance rates for ICG-VA and DSA are generally ⬎ 90%.6–8 However, some studies advocate using these two modalities in combination rather than in isolation.10,11 In most series,7,8,10 ICG-VA incongruity is related to vessel stenosis/occlusion or aneurysmal neck remnant
Fig. 1. Pre-operative arteriogram demonstrated a 10-mm broad-based aneurysm at the M1 bifurcation pointing inferolaterally (a). No significant evidence of calcification or atherosclerosis was encountered along the vascular tree upon careful intraoperative inspection (b). One curved clip was placed across the neck of the aneurysm, spanning its entire neck (c). Both fluorescent modalities (fluorescein VA-left upper corner and ICG-VA-Right lower corner) demonstrated good M1 and M2 patency with no fluorescent signal detectable within the aneurysm sac (d). To confirm successful aneurysm occlusion, the dome of the aneurysm was directly punctured, revealing steady arterial filling of the aneurysm dome (e).
660
C. Kulwin & A. A. Cohen-Gadol
Fig. 2. Pre-operative DSA which demonstrated a 16-mm inferiorly pointing aneurysm incorporating the base of both M2 trunks (a). Intraoperative microdissection disclosed a moderately patchy atherosclerotic aneurysm neck and dome (b). Three clips, including a shorter straight clip and a longer fenestrated clip, were also applied because of evidence of atherosclerosis within the neck of the aneurysm (c). ICG-VA clearly demonstrated parent vessel patency and no fluorescent signal within the aneurysm dome (d). The dome of the aneurysm was then directly punctured, revealing highly pressurized arterial bleeding (e).
due to a restricted field of view available to the microscope’s integrated infrared camera module. A significant depth of the surgical field can compromise excitation light reaching the aneurysm sac and ultimately affect the integrity of the emission light detected by the fluorescent module. In these two cases, however, we identified aneurysmal dome residual filling in the presence of a well visualized aneurysm and technically adequate negative ICG-VA study. In both cases, if ICG-VA results were interpreted in isolation, complete aneurysm occlusion would not have been achieved. We conducted a literature review and identified six other described cases of false-negative ICG-VA discovered upon aneurysm dome puncture12,13 (Table I). Unlike the current study, all previously reported cases involved deep operative
fields, possibly further confirming the known difficulties with field of view for ICG-VA. Of interest, there was a high rate (4 of 9, 44%) of neck atheroma in the previously reported case series. Due to these limitations, we no longer use ICG-VA for deep-seated aneurysms, including anterior communicating artery aneurysms. We reserve the use of ICG-VA for MCA aneurysms. The two cases discussed comprise 0.9% (2 of 212) of the MCA aneurysms microsurgically treated by the senior author during the past 5 years. Limitations to ICG-VA are not yet fully understood as this technology remains recently explored for intracranial surgery (first described for cerebral aneurysm surgery by Raabe et al.4 in 2003). An understanding of risk factors for an erroneous ICG-VA study is important. Unruptured, large
False-negative indocyanine green videoangiography 661 Table I. Patient data. Pt. Pt. No. Age Location 1 2 3 4 5 6 7 8
45 71 34 76 67 58 33 63
ACA(A1) Acomm PICA Acomm Acomm Acomm MCA MCA
Size
Neck Atheroma
ICG-VA
Confirmation
Source
Unknown 15 mm 6 mm 17 mm 8 mm 5 mm 10 mm 16 mm
Yes Yes No No No No No Yes
Neg Neg Neg Neg Neg Neg Neg Neg
Puncture, Repeat ICG-VA Puncture, Repeat ICG-VA Puncture Puncture Puncture Puncture Puncture Puncture
Mery13 Mery13 Ozgiray12 Ozgiray12 Ozgiray12 Ozgiray12 Current study Current study
Acomm, anterior communicating; ICG-VA, indocyanine green videoangiography; MCA, middle cerebral artery.
MCA aneurysms are frequently atherosclerotic, with a significant discordance between vessel/aneurysm lumen and external anatomy.14 Atherosclerotic aneurysms are known to carry a higher risk of operative morbidity.15 Due to the significant wall stiffness of these aneurysms, it may not be clear upon intraoperative inspection whether an aneurysm clip has fully occluded the lumen or lacks the required closing strength. Therefore, intraoperative confirmation of aneurysm occlusion is especially critical. Puncture of the aneurysm dome provides the most readily available method for confirmation of aneurysm sac exclusion. In the present series, ICG-VA demonstrated no aneurysm filling with a clear field of view to the aneurysm dome. Nonetheless, a puncture of the aneurysm dome demonstrated residual aneurysm filling. Further clip manipulation and/or additional clip placement was required to completely occlude the aneurysm. The etiology of a false-negative study may be multifactorial. The thickness of the calcified vessel wall may in part compromise the amplitude of the ICG emission signal, although in the adjacent parent high-flow atherosclerotic vessels, adequate signal was clearly present. In all our cases, clip blades were noted to be somewhat occlusive, as demonstrated by the present but somewhat compromised arterial bleeding after direct dome puncture. We hypothesize that the reduced flow in combination with thickened vessel walls may reduce the emission of ICG signal significantly, in agreement with those of Mery et al.13 This phenomenon may result in an ICG-VA study demonstrating no filling instead of reduced, but potentially clinically significant, aneurysmal filling. In our first illustrative case, the flow was significantly reduced upon direct aneurysm puncture, whereas in the second case, we encountered atherosclerosis or partial calcification along the aneurysm neck and significant arterial bleeding upon the puncture of its dome. Therefore, significant alterations in the flow within the aneurysm sac and an increased aneurysm wall thickness and opacity due to atherosclerosis/calcification are risk factors for a false-negative ICG-VA. Another possible mechanism involves small inflow within the aneurysm that creates a positive pressure within the sac, preventing further inflow. Upon puncturing the aneurysm, the pressure difference within the aneurysm sac and parent vessel increases, leading to aneurysmal filling. Finally, the natural history of a nearly-occluded aneurysm is variable.16 Although subsequent complete thrombosis may occur,17 hemorrhage or progression of angiographically visible18 or occult19 aneurysm remnant have been described.
Conclusions Intraoperative ICG-VA is a useful adjunct to surgical treatment of cerebral aneurysms, but may be limited in certain situations. Atherosclerotic MCA aneurysms may be associated with a false-negative ICG-VA in the presence of aneurysm sac filling. In addition, a decreased, but potentially clinically significant, flow within the sac may be missed by ICG-VA. Therefore, in select cases, it may be reasonable to directly confirm aneurysm occlusion after a negative ICG-VA by opening the aneurysm sac with a needle puncture. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Tanaka Y, Kobayashi S, Kyoshima K, Sugita K. Multiple clipping technique for large and giant internal carotid artery aneurysms and complications: angiographic analysis. J Neurosurg 1994;80: 635–42. 2. Siasios I, Kapsalaki EZ, Fountas KN. The role of intraoperative micro-Doppler ultrasound in verifying proper clip placement in intracranial aneurysm surgery. Neuroradiology 2012;54: 1109–18. 3. 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. Am J Neuroradiol 1999;20:1457–61. 4. 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 2003;52:132–9; discussion 139. 5. Martin NA , Bentson J, Vinuela F, et al. Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Neurosurg 1990;73: 526–33. 6. Dashti R, Laakso A , Niemela M, et al. Application of microscope integrated indocyanine green video-angiography during microneurosurgical treatment of intracranial aneurysms: a review. Acta Neurochir Suppl 2010;107:107–9. 7. Raabe A , Nakaji P, Beck J, et al. Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg 2005;103:982–9. 8. Gruber A , Dorfer C, Standhardt H, Bavinzski G, Knosp E. Prospective comparison of intraoperative vascular monitoring technologies during cerebral aneurysm surgery. Neurosurgery 2011;68:657–73; discussion 673. 9. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A . Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative near-infrared indocyanine green videoangiography. Neurosurgery 2008;62:1300–10. 10. Washington CW, Zipfel GJ, Chicoine MR, et al. Comparing indocyanine green videoangiography to the gold standard of
662
11. 12. 13. 14.
C. Kulwin & A. A. Cohen-Gadol intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg 2013;118:420–7. Moon HS, Joo SP, Seo BR, et al. Value of indocyanine green videoangiography in deciding the completeness of cerebrovascular surgery. J Korean Neurosurg Soc 2013;53:349–55. Ozgiray E, Akture E, Patel N, et al. How reliable and accurate is indocyanine green video angiography in the evaluation of aneurysm obliteration? Clin Neurol Neurosurg 2013;115:870–8. Mery FJ, Amin-Hanjani S, Charbel FT. Is an angiographically obliterated aneurysm always secure? Neurosurgery 2008;62: 979–82; discussion 982. Zhu W, Liu P, Tian Y, et al. Complex middle cerebral artery aneurysms: a new classification based on the angioarchitecture and surgical strategies. Acta Neurochir (Wien) 2013;155:1481–91.
15. Szelenyi A , Beck J, Strametz R, et al. Is the surgical repair of unruptured atherosclerotic aneurysms at a higher risk of intraoperative ischemia? Clin Neurol Neurosurg 2011;113:129–35. 16. Feuerberg I, Lindquist C, Lindqvist M, Steiner L. Natural history of postoperative aneurysm rests. J Neurosurg 1987;66:30–4. 17. Oruckaptan HH, Cekirge HS. Delayed thrombosis of a complex fusiform ICA aneurysm treated with flow reversal and partial occlusion: case report and brief review of possible mechanisms. Neuroradiology 2011;53:461–5. 18. Lin T, Fox AJ, Drake CG. Regrowth of aneurysm sacs from residual neck following aneurysm clipping. J Neurosurg 1989;70:556–60. 19. Komotar RJ, Mocco J, Lavine SD, Solomon RA . Angiographically occult, progressively expanding, giant vertebral artery aneurysm. Case report. J Neurosurg 2006;105:468–71.
Copyright of British Journal of Neurosurgery is the property of Taylor & Francis Ltd and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
ORIGINAL ARTICLE
False-negative indocyanine green videoangiography among complex unruptured middle cerebral artery aneurysms: The importance of further aneurysm inspection Charles Kulwin & Aaron A. Cohen-Gadol Department of Neurological Surgery, Goodman Campbell Brain and Spine, Indiana University, Indianapolis, IN, USA
of these goals are confounded by the discrepancy between the outer and inner vessel wall topologic discrepancies; this difference increases with vessel wall thickness.1 In the presence of significant vessel wall atherosclerosis, clip blades that externally appear to occlude only the aneurysm neck may internally occlude the parent vessel lumen, or conversely, clip blades that externally appear to leave a remnant may in fact result in complete occlusion. To evaluate internal aneurysm and vessel lumen topology, a variety of intraoperative adjuncts are available, including microdoppler ultrasound,2 digital subtraction angiography (DSA),3 and indocyanine green videoangiography (ICG-VA).4 Drawbacks to DSA include invasiveness and morbidity, logistic difficulties, and significant resource requirements.5 ICG-VA negates these factors, requiring only near-infrared imaging integration within the operative microscope and the intravenous access already in place for the procedure. Although concordance rates between ICG-VA and DSA are very high,6–8 DSA remains the gold standard. The ability to visualize local small perforators is more pronounced with ICG-VA.9 A false-negative ICG-VA study may result in suboptimal clip placement, exposing the patient to further hemorrhage risk and/or postoperative stroke due to aneurysm remnant or branching or perforating vessel occlusion. In a technically adequate study, ICG-VA may be limited by field-of-view limitations, which may be more common among aneurysms of the anterior communicating artery complex.6,10 An undescribed risk for a false-negative ICG-VA study is an atherosclerotic aneurysm or decreased flow within the dome. In this study, we describe our experience with cases of middle cerebral artery (MCA) aneurysms with false-negative ICG-VA studies requiring clip adjustment for optimal surgical treatment.
Abstract Successful surgical treatment of cerebral aneurysms requires complete occlusion of the aneurysm lumen while maintaining patency of the adjacent branching and perforating arteries. Intraoperative flow assessment allows aneurysm clip repositioning in the event these requirements are not met, avoiding the risk of postoperative rehemorrhage or infarction. A number of modalities have been proposed for primarily intraoperative qualitative blood flow assessment, including microdoppler ultrasonography, intraoperative digital subtraction angiography (DSA), and more recently noninvasive fluorescent angiography including indocyanine green (ICG) fluorescent imaging. Puncture of the aneurysm dome to exclude aneurysm sac filling may also assess the efficacy of clip placement. Although a high concordance between ICG and DSA has been reported, there remains an important subset of aneurysms for which negative ICG study may erroneously suggest aneurysm occlusion. A high-risk situation for such a false-negative study is an atherosclerotic middle cerebral artery (MCA) aneurysm in which vessel wall plaque interferes with the ICG signal. Furthermore, a decreased flow within the aneurysm may not allow enough emission light for detection under the current technology. In this report, we describe our experience with cases of MCA aneurysms with false-negative ICG-VA studies requiring clip adjustment for optimal surgical treatment and discuss two illustrative cases of MCA aneurysms with intraoperative fluorescence studies that were falsely negative, requiring puncture of the aneurysm to correctly identify incomplete aneurysm occlusion. Keywords: aneurysm; false negative; indocyanine green; microsurgical clipping
Introduction
Case 1
Cerebral aneurysm treatment centers on the prevention of future aneurysmal hemorrhage. Protection from hemorrhage is accomplished when the aneurysm lumen is fully occluded, no longer exposed to arterial flow. During microsurgery, both
A 33-year-old woman presented with an incidentally discovered right MCA aneurysm during a work-up for headaches. Pre-operative arteriogram demonstrated a 10-mm
Correspondence: Aaron A. Cohen-Gadol, MD, MSc, Department of Neurological Surgery, Goodman Campbell Brain and Spine, Indiana University School of Medicine, 355 W. 16th St, Suite 5100, Indianapolis, IN 46202, USA. Tel: ⫹ 317-362-8760. Fax: ⫹ 317-924-8472. E-mail: [email protected] Received for publication 7 November 2013; accepted 26 January 2014
658
False-negative indocyanine green videoangiography 659 broad-based aneurysm at the M1 bifurcation pointing inferolaterally (Fig. 1a). After a frontotemporal craniotomy and dissection of the M1 and M2 branches, including the aneurysm neck and dome, no significant evidence of calcification or atherosclerosis was encountered along the vascular tree upon careful intraoperative inspection (Fig. 1b). One curved titanium clip was placed to completely occlude the aneurysm neck while maintaining parent vessel patency under temporary M1 occlusion and burst suppression. The clip blades spanned the entire neck of the aneurysm (Fig. 1c). ICG-VA and fluorescein angiography were subsequently performed. Both fluorescent modalities demonstrated good M1 and M2 patency with no fluorescent signal detectable within the aneurysm sac (Fig. 1d). To confirm successful aneurysm occlusion, the dome of the aneurysm was directly punctured, revealing steady arterial filling of the aneurysm dome (Fig. 1e). A second slightly longer and curved aneurysm clip was then positioned to prevent further filling of the aneurysm sac. Postoperative DSA revealed no aneurysm filling, neck remnant, or vessel stenosis. The patient was discharged home on the second postoperative day with no complication.
Case 2 A 63-year-old woman was diagnosed with an incidentally discovered right MCA aneurysm on a pre-operative DSA that demonstrated a 16-mm inferiorly pointing aneurysm
incorporating the base of both M2 trunks (Fig. 2a). Intraoperative microdissection disclosed a moderately patchy atherosclerotic aneurysm neck and dome (Fig. 2b). A curved clip was applied onto the aneurysm neck to occlude the aneurysm sac. Two additional reinforcing clips, including a shorter straight clip and a longer fenestrated clip, were also applied because of the evidence of atherosclerosis within the neck of the aneurysm (Fig. 2c). ICG-VA clearly demonstrated parent vessel patency and no fluorescent signal within the aneurysm dome (Fig. 2d). At this point, the dome of the aneurysm was directly punctured, revealing highly pressurized arterial bleeding (Fig. 2e). Under temporary proximal vascular occlusion, the final two clips were repositioned and no further bleeding was noted. Postoperative DSA showed no aneurysm filling, neck remnant, or vessel stenosis. The patient awoke at her preoperative baseline and was subsequently discharged after resolution of exacerbation of chronic obstructive pulmonary disease, on the 7th postoperative day.
Discussion Published concordance rates for ICG-VA and DSA are generally ⬎ 90%.6–8 However, some studies advocate using these two modalities in combination rather than in isolation.10,11 In most series,7,8,10 ICG-VA incongruity is related to vessel stenosis/occlusion or aneurysmal neck remnant
Fig. 1. Pre-operative arteriogram demonstrated a 10-mm broad-based aneurysm at the M1 bifurcation pointing inferolaterally (a). No significant evidence of calcification or atherosclerosis was encountered along the vascular tree upon careful intraoperative inspection (b). One curved clip was placed across the neck of the aneurysm, spanning its entire neck (c). Both fluorescent modalities (fluorescein VA-left upper corner and ICG-VA-Right lower corner) demonstrated good M1 and M2 patency with no fluorescent signal detectable within the aneurysm sac (d). To confirm successful aneurysm occlusion, the dome of the aneurysm was directly punctured, revealing steady arterial filling of the aneurysm dome (e).
660
C. Kulwin & A. A. Cohen-Gadol
Fig. 2. Pre-operative DSA which demonstrated a 16-mm inferiorly pointing aneurysm incorporating the base of both M2 trunks (a). Intraoperative microdissection disclosed a moderately patchy atherosclerotic aneurysm neck and dome (b). Three clips, including a shorter straight clip and a longer fenestrated clip, were also applied because of evidence of atherosclerosis within the neck of the aneurysm (c). ICG-VA clearly demonstrated parent vessel patency and no fluorescent signal within the aneurysm dome (d). The dome of the aneurysm was then directly punctured, revealing highly pressurized arterial bleeding (e).
due to a restricted field of view available to the microscope’s integrated infrared camera module. A significant depth of the surgical field can compromise excitation light reaching the aneurysm sac and ultimately affect the integrity of the emission light detected by the fluorescent module. In these two cases, however, we identified aneurysmal dome residual filling in the presence of a well visualized aneurysm and technically adequate negative ICG-VA study. In both cases, if ICG-VA results were interpreted in isolation, complete aneurysm occlusion would not have been achieved. We conducted a literature review and identified six other described cases of false-negative ICG-VA discovered upon aneurysm dome puncture12,13 (Table I). Unlike the current study, all previously reported cases involved deep operative
fields, possibly further confirming the known difficulties with field of view for ICG-VA. Of interest, there was a high rate (4 of 9, 44%) of neck atheroma in the previously reported case series. Due to these limitations, we no longer use ICG-VA for deep-seated aneurysms, including anterior communicating artery aneurysms. We reserve the use of ICG-VA for MCA aneurysms. The two cases discussed comprise 0.9% (2 of 212) of the MCA aneurysms microsurgically treated by the senior author during the past 5 years. Limitations to ICG-VA are not yet fully understood as this technology remains recently explored for intracranial surgery (first described for cerebral aneurysm surgery by Raabe et al.4 in 2003). An understanding of risk factors for an erroneous ICG-VA study is important. Unruptured, large
False-negative indocyanine green videoangiography 661 Table I. Patient data. Pt. Pt. No. Age Location 1 2 3 4 5 6 7 8
45 71 34 76 67 58 33 63
ACA(A1) Acomm PICA Acomm Acomm Acomm MCA MCA
Size
Neck Atheroma
ICG-VA
Confirmation
Source
Unknown 15 mm 6 mm 17 mm 8 mm 5 mm 10 mm 16 mm
Yes Yes No No No No No Yes
Neg Neg Neg Neg Neg Neg Neg Neg
Puncture, Repeat ICG-VA Puncture, Repeat ICG-VA Puncture Puncture Puncture Puncture Puncture Puncture
Mery13 Mery13 Ozgiray12 Ozgiray12 Ozgiray12 Ozgiray12 Current study Current study
Acomm, anterior communicating; ICG-VA, indocyanine green videoangiography; MCA, middle cerebral artery.
MCA aneurysms are frequently atherosclerotic, with a significant discordance between vessel/aneurysm lumen and external anatomy.14 Atherosclerotic aneurysms are known to carry a higher risk of operative morbidity.15 Due to the significant wall stiffness of these aneurysms, it may not be clear upon intraoperative inspection whether an aneurysm clip has fully occluded the lumen or lacks the required closing strength. Therefore, intraoperative confirmation of aneurysm occlusion is especially critical. Puncture of the aneurysm dome provides the most readily available method for confirmation of aneurysm sac exclusion. In the present series, ICG-VA demonstrated no aneurysm filling with a clear field of view to the aneurysm dome. Nonetheless, a puncture of the aneurysm dome demonstrated residual aneurysm filling. Further clip manipulation and/or additional clip placement was required to completely occlude the aneurysm. The etiology of a false-negative study may be multifactorial. The thickness of the calcified vessel wall may in part compromise the amplitude of the ICG emission signal, although in the adjacent parent high-flow atherosclerotic vessels, adequate signal was clearly present. In all our cases, clip blades were noted to be somewhat occlusive, as demonstrated by the present but somewhat compromised arterial bleeding after direct dome puncture. We hypothesize that the reduced flow in combination with thickened vessel walls may reduce the emission of ICG signal significantly, in agreement with those of Mery et al.13 This phenomenon may result in an ICG-VA study demonstrating no filling instead of reduced, but potentially clinically significant, aneurysmal filling. In our first illustrative case, the flow was significantly reduced upon direct aneurysm puncture, whereas in the second case, we encountered atherosclerosis or partial calcification along the aneurysm neck and significant arterial bleeding upon the puncture of its dome. Therefore, significant alterations in the flow within the aneurysm sac and an increased aneurysm wall thickness and opacity due to atherosclerosis/calcification are risk factors for a false-negative ICG-VA. Another possible mechanism involves small inflow within the aneurysm that creates a positive pressure within the sac, preventing further inflow. Upon puncturing the aneurysm, the pressure difference within the aneurysm sac and parent vessel increases, leading to aneurysmal filling. Finally, the natural history of a nearly-occluded aneurysm is variable.16 Although subsequent complete thrombosis may occur,17 hemorrhage or progression of angiographically visible18 or occult19 aneurysm remnant have been described.
Conclusions Intraoperative ICG-VA is a useful adjunct to surgical treatment of cerebral aneurysms, but may be limited in certain situations. Atherosclerotic MCA aneurysms may be associated with a false-negative ICG-VA in the presence of aneurysm sac filling. In addition, a decreased, but potentially clinically significant, flow within the sac may be missed by ICG-VA. Therefore, in select cases, it may be reasonable to directly confirm aneurysm occlusion after a negative ICG-VA by opening the aneurysm sac with a needle puncture. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Tanaka Y, Kobayashi S, Kyoshima K, Sugita K. Multiple clipping technique for large and giant internal carotid artery aneurysms and complications: angiographic analysis. J Neurosurg 1994;80: 635–42. 2. Siasios I, Kapsalaki EZ, Fountas KN. The role of intraoperative micro-Doppler ultrasound in verifying proper clip placement in intracranial aneurysm surgery. Neuroradiology 2012;54: 1109–18. 3. 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. Am J Neuroradiol 1999;20:1457–61. 4. 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 2003;52:132–9; discussion 139. 5. Martin NA , Bentson J, Vinuela F, et al. Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Neurosurg 1990;73: 526–33. 6. Dashti R, Laakso A , Niemela M, et al. Application of microscope integrated indocyanine green video-angiography during microneurosurgical treatment of intracranial aneurysms: a review. Acta Neurochir Suppl 2010;107:107–9. 7. Raabe A , Nakaji P, Beck J, et al. Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg 2005;103:982–9. 8. Gruber A , Dorfer C, Standhardt H, Bavinzski G, Knosp E. Prospective comparison of intraoperative vascular monitoring technologies during cerebral aneurysm surgery. Neurosurgery 2011;68:657–73; discussion 673. 9. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A . Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative near-infrared indocyanine green videoangiography. Neurosurgery 2008;62:1300–10. 10. Washington CW, Zipfel GJ, Chicoine MR, et al. Comparing indocyanine green videoangiography to the gold standard of
662
11. 12. 13. 14.
C. Kulwin & A. A. Cohen-Gadol intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg 2013;118:420–7. Moon HS, Joo SP, Seo BR, et al. Value of indocyanine green videoangiography in deciding the completeness of cerebrovascular surgery. J Korean Neurosurg Soc 2013;53:349–55. Ozgiray E, Akture E, Patel N, et al. How reliable and accurate is indocyanine green video angiography in the evaluation of aneurysm obliteration? Clin Neurol Neurosurg 2013;115:870–8. Mery FJ, Amin-Hanjani S, Charbel FT. Is an angiographically obliterated aneurysm always secure? Neurosurgery 2008;62: 979–82; discussion 982. Zhu W, Liu P, Tian Y, et al. Complex middle cerebral artery aneurysms: a new classification based on the angioarchitecture and surgical strategies. Acta Neurochir (Wien) 2013;155:1481–91.
15. Szelenyi A , Beck J, Strametz R, et al. Is the surgical repair of unruptured atherosclerotic aneurysms at a higher risk of intraoperative ischemia? Clin Neurol Neurosurg 2011;113:129–35. 16. Feuerberg I, Lindquist C, Lindqvist M, Steiner L. Natural history of postoperative aneurysm rests. J Neurosurg 1987;66:30–4. 17. Oruckaptan HH, Cekirge HS. Delayed thrombosis of a complex fusiform ICA aneurysm treated with flow reversal and partial occlusion: case report and brief review of possible mechanisms. Neuroradiology 2011;53:461–5. 18. Lin T, Fox AJ, Drake CG. Regrowth of aneurysm sacs from residual neck following aneurysm clipping. J Neurosurg 1989;70:556–60. 19. Komotar RJ, Mocco J, Lavine SD, Solomon RA . Angiographically occult, progressively expanding, giant vertebral artery aneurysm. Case report. J Neurosurg 2006;105:468–71.
Copyright of British Journal of Neurosurgery is the property of Taylor & Francis Ltd and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
