Abstract

OBJECTIVE

Conventional cerebral angiography is the standard examination used to confirm aneurysm obliteration. Intraoperative indocyanine green (ICG) video angiography has recently been introduced as a valuable tool that is comparable to catheter intraoperative angiography. Intraoperative imaging evaluation is especially useful when complex aneurysm features are present, making direct clipping challenging. The aim of these angiographic evaluations is to assess parent vessel patency and to confirm lesion obliteration. However, there have been recent reports of growth or even rupture of angiographically obliterated aneurysms.

CLINICAL PRESENTATION

We report two patients in whom ICG video angiography falsely indicated that a clipped aneurysm was secure.

INTERVENTION

Both patients underwent direct clipping of unruptured aneurysms. ICG video angiography was performed, showing absence of residual filling of the sac. After incising the aneurysm dome, slow but significant dye extravasation was demonstrated. In the first patient, this occurred as a result of incomplete clipping of a wide aneurysm neck that was difficult to visualize; in the second patient, it occurred as a result of atheroma at the neck not allowing complete closure of the clip blades. This finding prompted clip readjustment and placement of an additional reinforcing clip in the two patients, respectively.

CONCLUSION

We demonstrate false indication of aneurysm obliteration by intraoperative video angiographic evaluation using ICG. It is possible that this limitation would also apply to catheter angiography. If certainty of complete exclusion of the aneurysm through opening the dome is not achieved, long-term follow-up angiographic evaluation would be strongly advised.

Direct clipping is the optimal definitive surgical treatment for an aneurysm (17,27,28). However, this approach can be challenging if there are complex features relating to aneurysm size, location, intraluminal thrombus, atheroma or calcification at the neck, involvement of branch vessels, or a wide neck (3,6,17,19,21,26,28,30).

In such cases, intraoperative assessments such as conventional catheter angiography or intraoperative indocyanine green (ICG) video angiography can be extremely useful (9,20,23,24,30). These angiographic methods help to avert parent and branch vessel occlusion and to rule out residual aneurysm opacification. The absence of angiographic filling has been the “gold standard” in confirming aneurysm obliteration. However, recent reports indicate that angiographically occult aneurysms can grow (5,13,14) or even rupture (15,29). In this article, we report two patients with aneurysms that appeared to be obliterated on ICG video angiography but were found to be unsecured intraoperatively.

CASE REPORTS

Patient 1

(see video at web site)

A 45-year-old man with no medical history was diagnosed with subarachnoid hemorrhage resulting from a ruptured left posterior communicating artery aneurysm 4 months previously. He was also found to have a left superior hypophyseal artery, a right carotid–ophthalmic, and a right anterior cerebral artery/A1 segment aneurysm. He underwent immediate successful coil embolization of the left-sided aneurysms. The right carotid–ophthalmic and A1 aneurysms were thought to be unfavorable for standard endovascular treatment as a result of a wide neck, and surgical clipping was recommended.

A standard pterional craniotomy was performed. Dissection of the sylvian fissure allowed good visualization of the aneurysms. After clipping of the right carotid–ophthalmic aneurysm, attention was brought to the A1 segment aneurysm. The wide neck was dissected and noted to be partially arising from the posterior aspect of the A1 segment. A curved Sugita clip (Mizuho America, Inc., Beverly, MA) was placed, sparing perforators of the posterior wall of the internal carotid artery. However, the tips of the clip blades could not be well visualized (Video 1). ICG video angiography was performed, using a standard central venous bolus injection of 0.5 mg/kg ICG, to rule out residual aneurysm filling and showed absence of angiographic filling of the aneurysm. However, after incising the aneurysm dome, continuous slow bleeding was demonstrated. A second round of ICG video angiography showed the dye extravasation through the unsecured aneurysm (Fig. 1; Video 1). Readjustment of the clip was performed, advancing the clip blades further across the neck and securing the aneurysm. Blood flow measurements of the A1 and M1 segments were obtained with the Ultrasonic flow probe (Transonic Systems, Inc., Ithaca, NY) and were stable from baseline. The patient's postoperative course was uneventful.

FIGURE 1.

Intraoperative and indocyanine green (ICG) video angiographic images of Patient 1 before and after clipping and opening the aneurysm dome. A, intraoperative microscopic view showing an A1 segment aneurysm. The neck partially arises from the posterior wall of the anterior cerebral artery. B, ICG video angiography showing opacification of the aneurysm sac before clipping. C, ICG video angiography showing no filling of the aneurysm sac after clipping. D, after opening the dome, continuous bleeding demonstrated that the aneurysm was not secured.

FIGURE 1.

Intraoperative and indocyanine green (ICG) video angiographic images of Patient 1 before and after clipping and opening the aneurysm dome. A, intraoperative microscopic view showing an A1 segment aneurysm. The neck partially arises from the posterior wall of the anterior cerebral artery. B, ICG video angiography showing opacification of the aneurysm sac before clipping. C, ICG video angiography showing no filling of the aneurysm sac after clipping. D, after opening the dome, continuous bleeding demonstrated that the aneurysm was not secured.

Patient 2

(see video at web site)

A 71-year-old woman with a long history of hypertension, hyperlipidemia, and peripheral vascular disease was found to have an incidental large 15-mm anterior communicating aneurysm. The decision was made to perform clipping. A standard pterional craniotomy was performed, and the anterior communicating aneurysm was identified, as were the bilateral A1 and A2 segments. Baseline flow measurements of these vessels were obtained. A significant amount of atheroma at the aneurysm neck was evident. Two Sugita clips were placed completely across the neck. ICG video angiography was performed using a standard central venous bolus injection of 0.5 mg/kg ICG and demonstrated absence of aneurysm filling. Then, the aneurysm dome was incised; slow but significant bleeding was evident as a result of atheroma at the neck precluding complete closure of the clip blades. A second round of ICG video angiography was performed, which demonstrated dye extravasation (Fig. 2; Video 2). Subsequently, an additional clip was placed, reinforcing the neck with a good result. Flow measurements performed after definite clipping were found to be similar to baseline. The patient's postoperative course was satisfactory.

FIGURE 2.

Intraoperative views and ICG video angiographic images showing Patient 2 after clipping previous and subsequent to opening the aneurysm dome. A, intraoperative view showing two clips across the neck of an anterior communicating artery aneurysm. B, ICG video angiography showing no filling of the aneurysm sac. C, after opening the dome, continuous bleeding demonstrated that the aneurysm was not secured. D, ICG video angiography showing dye extravasation and opacification of the aneurysm sac (yellow arrow).

FIGURE 2.

Intraoperative views and ICG video angiographic images showing Patient 2 after clipping previous and subsequent to opening the aneurysm dome. A, intraoperative view showing two clips across the neck of an anterior communicating artery aneurysm. B, ICG video angiography showing no filling of the aneurysm sac. C, after opening the dome, continuous bleeding demonstrated that the aneurysm was not secured. D, ICG video angiography showing dye extravasation and opacification of the aneurysm sac (yellow arrow).

DISCUSSION

Catheter-based angiography is the gold standard evaluation to assess complete aneurysm obliteration (9,18,24,30). Recently, ICG video angiography has emerged as a valuable intraoperative tool to reliably assess parent or branch vessel patency and to ensure nonfilling of the aneurysmal sac (23,24).

ICG video angiography results have been found to be comparable to those obtained with conventional intraoperative angiography. In a prospective study, Raabe et al. (24), found a 90% correlation with intra- and postoperative angiography. Of the remaining 10%, ICG video angiography underestimated or missed mild nonflow-limiting parent vessel stenosis in the majority; in 2.7% of the patients, the finding could have had clinical relevance underestimating a hemodynamically significant stenosis in two patients and missing a 4-mm residual neck in one. Nevertheless, incomplete occlusion and residual filling of the aneurysm sac could be clearly diagnosed, and no false-negatives were found in this series when evaluating obliteration. Regarding usefulness, in 9% of the patients, ICG video angiography provided significant information, most of which led to clip readjustment (23,24). In recent series, the accuracy of conventional intraoperative angiography ranged from 88 to 95%, with usually inconsequential false-negatives ranging from 5 to 9% (4,9,10,22,24,30). The rate of valuable additional information was similar to that of ICG video angiography (4,9,10,22,24,30). ICG video angiography has several potential advantages over conventional angiography, including a low rate of morbidity and low cost, no need for neuroendovascular surgeon availability, and the ability to provide information quickly and repeatedly as needed during surgery (23,24,31). In addition, it has enough resolution to assess patency of perforators in most cases (24).

Surgically, the optimal definitive treatment for aneurysms is direct clipping. However, there are some features that make this approach difficult. For instance, complex aneurysm characteristics relating to size, type, and location; intraluminal thrombus; atheroma or calcification at the neck; involvement of branch vessels; and a wide neck are risk factors for incomplete clipping or ischemic complications (2,3,6,7,11,12,16,17,19,21,25,28,30). Intraoperative imaging and direct vessel flow measurements can be very helpful in such cases (1,8,9,24,30).

The two cases in this report demonstrate that ICG video angiographic absence of filling of the aneurysms gave false indication that the aneurysms were secure. The probable cause was very delayed flow into the aneurysm dome resulting from incomplete clipping of a wide aneurysm neck that was difficult to visualize and atheroma at the neck precluding complete closure of the clip blades. It is possible that this limitation in visualization may also apply to catheter angiography because both techniques rely on the basic principle of intravascular dye opacification. Catheter angiography differs in that arterial pressurized (hand or mechanical) injection is used, which may more readily reveal opacification of an aneurysm sac compared with the circulating ICG dye from venous injection. However, our finding does raise the possibility that the same limitation may apply to conventional angiography. Because contemporaneous intraoperative angiography was not performed in these cases, this possibility cannot be directly confirmed.

The clinical significance of these unprotected aneurysms, if they had not been recognized, is uncertain. The flow could have been slow enough to lead the aneurysms to ultimately thrombose, but it could have also potentially led to growth or rupture. Komotar et al. (14) recently reported the growth of a giant vertebral artery aneurysm despite immediate and late angiographic evaluations confirming no filling of the lesion after hunterian occlusion. The authors stated that microrecanalization could have been the reason for the aneurysm continuing to expand. Other similar findings of growth or rupture of angiographically occult aneurysms have been described (5,13,15,29).

CONCLUSION

We demonstrate the finding of a false-negative result when assessing aneurysm obliteration by intraoperative video angiographic evaluation using ICG. In both patients, anatomic adverse factors of the aneurysm neck led to incomplete clipping.

Therefore, the absence of ICG video angiographic filling does not necessarily indicate that the aneurysm is secure. Partial incision of the aneurysm dome is suggested to completely rule out persistent flow into the aneurysm. If this is not performed, especially in technically challenging cases, long-term angiographic follow-up evaluation is advisable.

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COMMENTS

Two cases of clipping of unruptured aneurysms in which intraoperative indocyanine green (ICG) video angiography failed to show any filling of the aneurysm after clipping are reported. However, puncture of the aneurysms demonstrated continued arterial filling. We have also seen this phenomenon using conventional digital subtraction angiography intraoperatively and agree that most aneurysms should be punctured after negative angiography. In some cases, however, calcifications in the neck region prevent the clip from completely closing, and filling may continue between the clip blades. In these cases, multiple clips are usually required. When anatomical restrictions limit the use of additional clips, follow-up angiography is definitely indicated. We have seen the vast majority of these aneurysms proceed to complete thrombosis when the clip is in the correct anatomic position and is placed completely across the neck.

Robert A. Solomon

New York, New York

This case report illustrates some of the limitations of ICG video angiography in the treatment of intracranial aneurysms. The authors present two patients in whom ICG video angiography gave false-negative results. Fortunately, the aneurysms were opened intraoperatively in both patients, allowing the discovery of persistent filling. The first case was attributable to residual filling through a partially clip-occluded wide-neck aneurysm and the second case was residual filling attributable to differential wall thickness from atheroma. The authors postulate that the false-negative results resulted from very delayed flow into the aneurysm dome. ICG video angiography is another useful tool in the armamentarium of the cerebrovascular neurosurgeon, but it is not without its limits. These patients underscore the importance of understanding the limits of the diagnostic tools being used, and in occurrences such as those illustrated, further confirmatory testing may be needed. These instances remind neurosurgeons that when they are dealing with aneurysms with atheroma, a wide neck, or other morphology for which clip application may not obliterate the inflow, they need to consider additional strategies to completely obliterate the aneurysm (i.e., tandem clip techniques). Also in these instances, neurosurgeons cannot rely solely on the results of the ICG angiography and may consider other methods such as aspirating the sac to confirm aneurysm obliteration. Despite these examples, ICG video angiography has many uses in cerebrovascular neurosurgery, and like any tool in neurosurgery, it should be deployed and interpreted in the context of the clinical situation.

Dan Surdell

H. Hunt Batjer

Chicago, Illinois

In this article, the authors describe two patients in whom ICG video angiography was used to assess the degree of microsurgical reconstruction and repair of an aneurysm. In these two patients, the ICG video angiogram gave a false indication that the clipped aneurysm was secure.

Although this technology can often be very useful, this article illustrates that it can also be extremely misleading. This type of technique is extremely useful to determine whether the parent vessel is patent, and I think still has a very good role in that regard. The degree of aneurysm occlusion, however, is still in question, and in certain patients in whom aneurysm repair has been problematic intraoperatively, intraoperative or immediately postoperative angiography clearly is in order.

Robert H. Rosenwasser

Philadelphia, Pennsylvania

The authors reported two interesting examples of surgical cases in which intraoperative ICG video angiography failed to demonstrate residual filling of the sac of the aneurysm after incomplete occlusion of its neck. They concluded that incision of the dome of the aneurysm should be achieved if possible to ascertain complete absence of aneurysm filling, because both intraoperative conventional angiography and ICG video angiography may fail to confirm aneurysm obliteration.

Incising the dome of the aneurysm is a standard practice in aneurysm surgery. The article nicely illustrates the necessity of this maneuver despite negative results on ICG video angiography. Incising the dome of the aneurysm and the use of ICG video angiography are both also important procedures to improve identification and preservation of perforating arteries surrounding the aneurysm.

Juan C. Fernandez-Miranda

Aaron S. Dumont

Neal F. Kassell

Charlottesville, Virginia