Operative Nuances
The “Squeezing Maneuver” in Microsurgical Clipping of Intracranial Aneurysms Assisted by Indocyanine Green Videoangiography BACKGROUND: Indocyanine green videoangiography (ICGV) is becoming routine in intracranial aneurysm surgery to assess intraoperatively both sac obliteration and vessel patency after clipping. However, ICGV-derived data have been reported to be misleading at times. We recently noted that a simple intraoperative maneuver, the “squeezing maneuver,” allows the detection of deceptive ICGV data on aneurysm exclusion and allows potential clip repositioning. The squeezing maneuver is based on a gentle pinch of the dome of a clipped aneurysm when ICGV documents its apparent exclusion. OBJECTIVE: To present the surgical findings and the clinical outcome of this squeezing maneuver. METHODS: Data from 23 consecutive patients affected by intracranial aneurysms who underwent the squeezing maneuver were analyzed retrospectively. The clip was repositioned in all cases when the dyeing of the sac was visualized after the maneuver. RESULTS: In 22% of patients, after an initial ICGV showing the aneurysm exclusion after clipping, the squeezing maneuver caused the prompt dyeing of the sac; in all cases, the clip was consequently repositioned. A calcification/atheroma of the wall/neck was predictive of a positive maneuver (P = .001). The aneurysm exclusion rate at postoperative radiological findings was 100%. CONCLUSION: With the limits of our small series, the squeezing maneuver appears helpful in the intraoperative detection of misleading ICGV data, mostly when dealing with aneurysms with atheromatic and calcified walls.
Alessandro Della Puppa, MD* Oriela Rustemi, MD* Marta Rossetto, MD* Giorgio Gioffre`, MD* Marina Munari, MD‡ Fady T. Charbel, MD§ Renato Scienza, MD* *Department of Neurosurgery and ‡Department of Anaesthesiology, Padua University Hospital, Padua, Italy; §Department of Neurosurgery, University of Illinois at Chicago, Chicago, Illinois Correspondence: Alessandro Della Puppa, MD, Department of Neurosurgery, Padua University Hospital, Azienda Ospedaliera di Padova, Via Giustiniani, 2-35128, Padova, Italy. E-mail: alessandro.dellapuppa@ sanita.padova.it
KEY WORDS: Cerebral aneurysm, Clipping, Indocyanine green videoangiography, Squeezing maneuver Received, December 20, 2013. Accepted, February 12, 2014. Published Online, March 3, 2014. Copyright © 2014 by the Congress of Neurological Surgeons.
Operative Neurosurgery 10:208–213, 2014
I
ndocyanine green (ICG) videoangiography (ICGV) is now used routinely in neurosurgery to assist in vascular and occasionally oncological surgery. As far as aneurysm surgery is concerned, it represents a remarkable tool to verify both sac obliteration1-3 and vessel patency after microsurgical clipping.4,5 The actual obliteration rate of ICGV-monitored clipped aneurysms is about 90% to 100% compared with digital subtraction angiography (DSA) control.1-4,6-13 Nevertheless, it is not uncommon to observe an intraoperative ICGV-assisted obliteration of an aneurysm after clipping and the apparently slack dome to be still filling after aneurysm sac opening.13,14 The ABBREVIATIONS: DSA, digital subtraction angiography; ICG, indocyanine green; ICGV, indocyanine green videoangiography
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DOI: 10.1227/NEU.0000000000000334
identification of these “false negatives” at an intraoperative stage could allow a prompt clip repositioning to achieve the final and secure exclusion of all aneurysms. The direct dome opening or puncture after clipping may maximize the intraoperative detection of such false negatives. However, a calcified sac, atheromas, thickwalled vessels, and broad-neck aneurysms might not leave enough tissue to control the potential bleeding after sac incision, thus making the dome opening unsafe. From these findings, some authors suggested the use of intraoperative DSA.5,15,16 After an initial ICGV showing a complete occlusion of aneurysm, we have observed that a rather simple maneuver done with bipolar or Cushing bayonet forceps to test the aneurysm slackness allows assessment of the actual aneurysm obliteration under the same ICG injection and allows potential clip repositioning.
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ICGV FALSE-NEGATIVE CLIPPED ANEURYSMS
METHODS The Squeezing Maneuver The squeezing maneuver is based on a gentle pinch of the dome of a clipped aneurysm after ICGV has documented its apparent exclusion. The maneuver is carried out during the same ICG injection to confirm the actual exclusion of the dome. It is called positive when, after an initial ICGV shows the aneurysm exclusion, a gentle pinch of the slack aneurysm dome with a bipolar or Cushing bayonet forceps under ICGV visualization causes the prompt dyeing of the sac, suggesting that the aneurysm is still filling up (Figure 1). Conversely, the maneuver is called negative when, after pinching of the clipped dome, the sac does not fill up (Figure 2). Subsequent opening of the sac can confirm whether a flow is still filling the aneurysm. The purpose of the maneuver is to detect a potential deceptively excluded aneurysm, as previously shown by ICGV. The consequence is the opportunity to readjust the clip, allowing complete exclusion of the sac during the same procedure.
was performed after the ICGV showed no aneurysm remnants after clipping. Patients underwent a distinct surgical strategy based on the outcome of the maneuver. Indeed, when the maneuver was positive and the sac was promptly filled by the dye, the aneurysm was always secured by placing an additional clip or alternatively by repositioning the same clip. When the maneuver was negative and the sac did not fill up when the clipped dome was pinched, the clip was not repositioned. To verify the ICGV findings after the maneuver, the dome opening was always carried out when deemed safe and feasible by the surgeon. All patients underwent the assessment of sac exclusion both intraoperatively through ICGV and postoperatively with a computed tomographic angiography scan (or magnetic resonance angiography when computed tomographic angiography was not feasible). Patient and aneurysm features were correlated to the maneuver outcomes: patient age and aneurysm size, bleeding history of the aneurysm, atheromas of the neck or dome, and dome-to-neck ratio. To assess the role of this approach in the final aneurysm exclusion rate, the postoperative radiological findings were analyzed by an expert neuroradiologist blinded to intraoperative data and surgical strategy.
Patients and Surgical Strategy Data from 23 patients affected by intracranial aneurysms who underwent microsurgical clipping with the assistance of ICGV associated with the squeezing maneuver at our department between May and October 2013 were analyzed retrospectively. In all cases, the maneuver
RESULTS A total of 23 patients were enrolled in the study (Table 1). Median age was 60 years. Eleven patients presented with a ruptured
FIGURE 1. A female 56-year-old patient affected by a bilobated middle cerebral artery aneurysm (A). The initial indocyanine green videoangiography (ICGV) shows occlusion of both aneurysm sacs (B), but the bipolar clipping of the slack domes fills them with dye under ICGV visualization (C). Because little tissue is left in the aneurysm dome, a direct sac opening is not deemed safe. Indeed, the lack of space at the dome would not allow a second clip to be placed without removing the first, making potential bleeding difficult to control (D).
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FIGURE 2. A female 39-year-old patient affected by a middle cerebral artery aneurysm (A). The initial indocyanine green videoangiography (ICGV) shows aneurysm sac occlusion (B), and the bipolar clipping of the slack domes does not fill it with dye under ICGV visualization (C). The direct sac opening confirms aneurysm exclusion (D).
TABLE 1. Clinical and Surgical Features
Variables Investigated Postoperative computed tomographic angiography findings No remnant Remnant Atheromas Yes No Presentation Ruptured Unruptured Size, mm ,10 .10 Dome-to-neck ratio .2 ,2 Median age, y
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Total (n = 57), n
Group I (Squeezing) (n = 23), n
55 2
23 0
14 43
6 17
30 27
11 12
30 27
10 13
37 20 62
18 5 60
and 12 with an unruptured aneurysm. The aneurysm was at the middle cerebral artery level in 15 patients, at the anterior cerebral artery level in 6 patients, and at the internal carotid artery level in 2 patients. An atheromatous wall or neck was present in 6 patients. The aneurysm size was ,10 mm in 10 patients, whereas the dometo-neck ratio was .2 in 18 cases. Computed tomographic angiography was performed in 21 patients, and magnetic resonance angiography was done in 2 patients for different reasons (iodate contrast allergy in 1 patient and artifacts resulting from previous embolization in the other). Intraoperative data are summarized in Table 2. The maneuver was positive in 5 (22%) and negative in 18 (78%) of the 23 patients. The mean time at which the maneuver was performed was 14 seconds (range, 10-22 seconds). Actually, we waited and observed the aneurysm for .60 seconds after ICGV in all cases, as is usually done to assess the completeness of clipping. Indeed, the rational of the maneuver was not to replace the usual observation but to add a novel test to the usual aneurysm observation alone after ICGV. However, we performed the maneuver early, during the arterial phase, assuming that it could be the best moment to test the clip capacity; in fact, in no case did we detect an aneurysm filling over time after a negative maneuver. We performed the dome opening in 19 of 23 patients: 4 of 5 patients with a positive maneuver and 15 of 18 patients with
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ICGV FALSE-NEGATIVE CLIPPED ANEURYSMS
TABLE 2. Clinical and Surgical Features of Patients Who Underwent the Squeezing Maneuvera
Variables Postoperative computed tomographic angiography findings No remnant Remnant Atheromas Yes No Presentation Ruptured Unruptured Size, mm ,10 .10 Dome-to-neck ratio .2 ,2 Median age, y
Squeezing Negative, P n Value
Total, n
Squeezing Positive, n
23
5
18
23 0
5 0
18 0
—
6 17
5 0
1 17
.001
11 12
2 3
9 9
.99
10 13
2 3
8 10
.99
18 5 60
4 1 59
14 4 61
.99
a
Positive: aneurysms that fill with dye after the maneuver. Negative: aneurysms that do not fill with dye after the maneuver.
a negative maneuver. Among patients in whom the maneuver caused the prompt dyeing of the sac, all opened domes were found bleeding (4 of 4, 100%); conversely, in 1 patient, the dome incision was not feasible for the insufficient tissue remaining after additional clip positioning. Among patients in whom the maneuver did not cause the dyeing of the sac, in 1 case (of 15), the dome was found to be bleeding (7%). In all 5 cases with a positive maneuver, either the clip was repositioned or an additional clip was placed on the aneurysm neck. The strategy thus determined a rate of clip repositioning of 22%. A calcification/atheroma of the wall or neck was predictive of a positive maneuver (P = .001), whereas bleeding history, aneurysm size, and neck-dome ratio were not. With regard to the exclusion rate outcomes, no cases of remnants were reported at the radiological evaluation.
DISCUSSION The Issue of Misleading ICGV Data in Aneurysm Surgery The intraoperative occurrence of an aneurysm that looks apparently excluded (slack) but is not actually obliterated is not uncommon.14 To the best of our knowledge, the first 2 cases in the literature of aneurysms with ICGV evidence of complete obliteration, which after dome opening showed continuous bleeding, were reported by Mery et al.14 Another report indicates a 3.6% rate of false-negative ICGV-documented obliterated aneurysms, with persistent flow within the aneurysm after dome
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puncture.13 The authors found no morphological explanations that might have contributed to the failure of ICG in demonstrating persistent residual flow. Gruber et al8 described a case in which the postclipping manipulation of the sac of a fusiform anterior cerebral artery aneurysm, after initial negative ICGV and intraoperative DSA findings, revealed that the aneurysm was still filling from the superior anterior cerebral artery, as a further ICGV confirmed. Subsequent trapping of the superior anterior cerebral artery resulted in aneurysm occlusion. In a comment on that article, Raabe postulated that puncturing the aneurysm is the most reliable way to confirm its exclusion from circulation.8 However, in some cases, the amount of tissue of the aneurysm dome left after clipping may not be enough to allow a safe dome incision; furthermore, in cases with calcified walls or important atheromas, the sac opening is not feasible. Significance of the Squeezing Maneuver Our study presents a simple, safe, cheap, and fast maneuver to detect intraoperatively deceptive ICGV data on aneurysm exclusion after microsurgical clipping. This maneuver is simple and cheap because only a bipolar or bayonet forceps is needed. It is safe because, in all 23 cases, we did not detect aneurysm or brain damage, and no clips were displaced during the maneuver. It is fast because it takes only a few seconds through ICGV. Actually, the main question concerns the value and the role of the maneuver in the current microsurgical clipping practice. Indeed, some might argue that the issue being studied does not need a solution because a filling aneurysm after the maneuver could still potentially undergo spontaneous thrombosis. However, so far, ICGV has been reported to have a sensibility inferior to that of DSA as far as the obliteration assessment of clipped aneurysms is concerned.1-4,6-13 A recent study comparing ICGV and intraoperative DSA found a 14% rate of ICGV failure in detecting aneurysm exclusion.17 Could the patients with a falsely excluded clipped aneurysm at ICGV be detected, at least in part, by this maneuver? The 100% aneurysm exclusion rate achieved through the high clip repositioning rate (22%) reported in our study might be an answer. On the other hand, the high rate of nonexcluded aneurysm detected by the maneuver could mean that not only unsecured aneurysms but also aneurysms prone to rehabilitation over time are detected by the squeezing, which puts to test the mechanical strength of the clip. Further studies are needed to assess this issue. The main limitation of this study is that the data are retrospective and the application of the squeezing maneuver is not randomized, with consequent potential bias that may increase the actual impact of the maneuver. Indeed, in all cases, the maneuver was performed only when safe to carry out. In addition, we must emphasize that the gold standard to assess complete aneurysm occlusion and preservation of flow in the involved vessels remains DSA. This represents an additional bias of our study. Another remarkable issue concerns the safety of the maneuver. Indeed, we should bear in mind that this maneuver could be safe only in rather experienced hands because putting extra stress on an already stretched wall of a partly clipped aneurysm,
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DELLA PUPPA ET AL
especially at the neck region, might lead in less experienced hands to a serious tear close to the vessel. In addition, there is the possibility that partly clotted blood or calcified fragments may be pushed into the vessel lumen, potentially causing microembolism, if the maneuver is not performed gently. However, in our experience, no cases of stroke were clinically or radiologically detected. Our data show that the maneuver is highly recommended when the aneurysm presents an atheroma or a calcific wall; actually, the intraoperative exclusion assessment of this subgroup of aneurysms after clipping is challenging, and intraoperative DSA has been already suggested for this purpose.5,15,16 In our study, the maneuver outcomes were confirmed, whenever possible, by dome opening. In 80% of patients with a positive maneuver, the dome was opened, and in all cases, it was found to be actively bleeding. Conversely, 7% of patients had a bleeding aneurysm at dome opening after the sac did not fill up after the pinching of the clipped aneurysm, which means that a negative maneuver is not enough to warrant the exclusion of the aneurysm. Larger studies are needed to validate the clinical impact of our strategy.
CONCLUSION The intraoperative ICGV remains a very useful tool in aneurysm surgery. Squeezing the clipped aneurysm dome with bipolar/ Cushing bayonet forceps is a simple maneuver that controls the reliability of ICGV-assisted obliteration, especially in selected cases. This maneuver allows detection of deceptive ICGV data (false negatives) intraoperatively and clip repositioning or placement of an additional clip in the same surgical session. Disclosure The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. 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(1):132-139. 2. Raabe A, Nakaji P, Beck J, et al. Prospective evaluation of surgical microscopeintegrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg. 2005;103:982-989. 3. Wang S, Liu L, Zhao Y, Zhang D, Yang M, Zhao J. Evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. Neurosurg Rev. 2010;34(2):209-215. 4. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative nearinfrared indocyanine green videoangiography. Neurosurgery. 2008;62(6 suppl 3): 1300-1310. 5. Snyder LA, Sperzler RF. Current indications for green angiography. World Neurosurg. 2011;76(5):405-406. 6. Dashti R, Laakso A, Niemelä M, Porras M, Hernesniemi J. Microscope-integrated near-infrared indocyanine green videoangiography during surgery of intracranial aneurysms: the Helsinki experience. Surg Neurol. 2009;71(5):543-550. 7. Fischer G, Stadie A, Oertel JM. Near-infrared indocyanine green videoangiography versus microvascular Doppler sonography in aneurysm surgery. Acta Neurochir (Wien). 2010;152(9):1519-1525. 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(3):657-673; discussion 673.
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9. Imizu S, Kato Y, Sangli A, Oguri D, Sano H. Assessment of incomplete clipping of aneurysms intraoperatively by a nearinfrared indocyanine green-video angiography (Niicg-Va) integrated microscope. Minim Invasive Neurosurg. 2008;51:199-203. 10. Jing Z, Ou S, Ban Y, Tong Z, Wang Y. Intraoperative assessment of anterior circulation aneurysms using the indocyanine green video angiography technique. J Clin Neurosci. 2010;17(1):26-28. 11. Li J, Lan Z, He M, You C. Assessment of microscope-integrated indocyanine green angiography during intracranial aneurysm surgery: a retrospective study of 120 patients. Neurol India. 2009;57:453-459. 12. Ma CY, Shi JX, Wang HD, Hang CH, Cheng HL, Wu W. Intraoperative indocyanine green angiography in intracranial aneurysm surgery: microsurgical clipping and revascularization. Clin Neurol Neurosurg. 2009;111(10):840-846. 13. Özgiray E, Aktüre 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(7):870-878. 14. Mery FJ, Amin-Hanjani S, Charbel FT. Is an angiographically obliterated aneurysm always secure? Neurosurgery. 2008;62(4):979-982. 15. Chiang VL, Gaillouud P, Murphy KJ, Rigamonti D, Tamargo RJ. Routine intraoperative angiography during aneurysm surgery. J Neurosurg. 2002;96(6): 988-992. 16. Tang G, Cawley CM, Dion JE, Barrow DL. Intraoperative angiography during aneurysm surgery: a prospective evaluation of efficacy. J Neurosurg. 2002;96(6): 993-999. 17. Washington CW, Zipfel GJ, Chicoine MR, et al. Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg. 2013;118(2):420-427.
COMMENTS
I
ndocyanine green (ICG) videoangiography represents a relatively new technique that provides additional information on the perfusion physiology and occlusion rate of cerebral aneurysms. The technique is considered to be very helpful by many vascular neurosurgeons and represents a particularly valuable tool for all who do not proceed with intraoperative digital subtraction angiography in the operating room. The technique is very sensitive, and the number of intraoperative applications of the technique within 1 surgical procedure is limited. Thus, observations that, after aneurysm clipping, remnants of fluorescence dye mimic persistent aneurysm perfusion are not rare. In the present article, the authors report their experience with squeezing the aneurysm sac after clipping under ICG angiography. They suggest that ICG videoangiography is misleading in some cases; in particular, a falsepositive impression of complete occlusion of the aneurysm sac is stated to be frequent. Based on this background, a series of 23 aneurysm clippings is reported in which a positive squeezing maneuver was demonstrated in 80% of the incomplete clipped aneurysms (4 of 5). The study is well written and well illustrated. I think that the idea of squeezing the aneurysm sac after clipping to evaluate the aneurysm occlusion is a nice idea. The technique appeals by its easy performance and its availability. However, I personally—not having ever done the squeezing maneuver in any ICG aneurysm clipping—think of squeezing the aneurysm and causing its rupture. What now? Will I be able to clip the aneurysm in the same safe way I would have done it without the rupture? In addition, the study is based on just 5 cases of incomplete aneurysm clipping. Thus, more experience is needed before a definite decision on the value of this simple technique for aneurysm clipping can be made. Joachim Oertel Mainz, Germany
T
his is an interesting article reporting a technique for verifying aneurysm occlusion after indocyanine green (ICG) angiography. I
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ICGV FALSE-NEGATIVE CLIPPED ANEURYSMS
am convinced that it is clinically useful, but how useful remains unanswered. Technically, the detection of residual filling after incomplete clipping requires “late” images. This is opposite of the detection of branch stenosis/occlusion in which the early inflow images at the time of dye arrival are most important. To diagnose potential residual filling of the aneurysm, I usually wait 60 seconds after the first arterial filling to ensure that the aneurysm remains completely dark. If the diagnosis of complete occlusion is made before this time, it may be false negative. There have been reports of bleeding after dome puncture in aneurysms in which ICG showed complete occlusion, but there is no information on how long the aneurysm was inspected after ICG angiography. In this report, the squeezing test was performed after a mean of 14 seconds; in Figure 1B, the image confirms complete occlusion even after 3.7 seconds. Thus, I assume that some of the aneurysms might have shown late filling after 60 seconds. If the aneurysm remains completely dark 60 seconds after ICG arrival, the consequence of any microleakage remains questionable. I personally do not open the sac routinely (except in unclear cases), and I have never seen residual filling of the aneurysm sac in such cases in a postoperative angiogram, provided that the wall of the aneurysm was calcified and the aneurysm was not thrombosed. Nonetheless, the
OPERATIVE NEUROSURGERY
technique of gently squeezing the aneurysm will force some outflow of blood and then inflow of dye in incompletely clipped aneurysms, and vascular neurosurgeons should know this technique. Andreas Raabe Bern, Switzerland
T
his is a very important article describing a problem that has probably been encountered by many vascular neurosurgeons and that might have been considered a rare event. In fact, mechanical manipulation of a clipped aneurysm under indocyanine green (ICG) videoangiography resulted in residual aneurysm filling in 21.7% of the cases in this retrospective analysis. The authors identified atheromatous plaques in the neck area as a possible reason, indicating that the squeezing maneuver described will result in visible ICG inflow into the aneurysm sac in the presence of mechanically suboptimal clip closure. This can be considered an advantage of ICG videoangiography over digital subtraction angiography because a mechanical challenge to the mechanical strength of the clip is usually not possible during a digital subtraction angiography run. Andreas Gruber Vienna, Austria
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The “Squeezing Maneuver” in Microsurgical Clipping of Intracranial Aneurysms Assisted by Indocyanine Green Videoangiography BACKGROUND: Indocyanine green videoangiography (ICGV) is becoming routine in intracranial aneurysm surgery to assess intraoperatively both sac obliteration and vessel patency after clipping. However, ICGV-derived data have been reported to be misleading at times. We recently noted that a simple intraoperative maneuver, the “squeezing maneuver,” allows the detection of deceptive ICGV data on aneurysm exclusion and allows potential clip repositioning. The squeezing maneuver is based on a gentle pinch of the dome of a clipped aneurysm when ICGV documents its apparent exclusion. OBJECTIVE: To present the surgical findings and the clinical outcome of this squeezing maneuver. METHODS: Data from 23 consecutive patients affected by intracranial aneurysms who underwent the squeezing maneuver were analyzed retrospectively. The clip was repositioned in all cases when the dyeing of the sac was visualized after the maneuver. RESULTS: In 22% of patients, after an initial ICGV showing the aneurysm exclusion after clipping, the squeezing maneuver caused the prompt dyeing of the sac; in all cases, the clip was consequently repositioned. A calcification/atheroma of the wall/neck was predictive of a positive maneuver (P = .001). The aneurysm exclusion rate at postoperative radiological findings was 100%. CONCLUSION: With the limits of our small series, the squeezing maneuver appears helpful in the intraoperative detection of misleading ICGV data, mostly when dealing with aneurysms with atheromatic and calcified walls.
Alessandro Della Puppa, MD* Oriela Rustemi, MD* Marta Rossetto, MD* Giorgio Gioffre`, MD* Marina Munari, MD‡ Fady T. Charbel, MD§ Renato Scienza, MD* *Department of Neurosurgery and ‡Department of Anaesthesiology, Padua University Hospital, Padua, Italy; §Department of Neurosurgery, University of Illinois at Chicago, Chicago, Illinois Correspondence: Alessandro Della Puppa, MD, Department of Neurosurgery, Padua University Hospital, Azienda Ospedaliera di Padova, Via Giustiniani, 2-35128, Padova, Italy. E-mail: alessandro.dellapuppa@ sanita.padova.it
KEY WORDS: Cerebral aneurysm, Clipping, Indocyanine green videoangiography, Squeezing maneuver Received, December 20, 2013. Accepted, February 12, 2014. Published Online, March 3, 2014. Copyright © 2014 by the Congress of Neurological Surgeons.
Operative Neurosurgery 10:208–213, 2014
I
ndocyanine green (ICG) videoangiography (ICGV) is now used routinely in neurosurgery to assist in vascular and occasionally oncological surgery. As far as aneurysm surgery is concerned, it represents a remarkable tool to verify both sac obliteration1-3 and vessel patency after microsurgical clipping.4,5 The actual obliteration rate of ICGV-monitored clipped aneurysms is about 90% to 100% compared with digital subtraction angiography (DSA) control.1-4,6-13 Nevertheless, it is not uncommon to observe an intraoperative ICGV-assisted obliteration of an aneurysm after clipping and the apparently slack dome to be still filling after aneurysm sac opening.13,14 The ABBREVIATIONS: DSA, digital subtraction angiography; ICG, indocyanine green; ICGV, indocyanine green videoangiography
208 | VOLUME 10 | NUMBER 2 | JUNE 2014
DOI: 10.1227/NEU.0000000000000334
identification of these “false negatives” at an intraoperative stage could allow a prompt clip repositioning to achieve the final and secure exclusion of all aneurysms. The direct dome opening or puncture after clipping may maximize the intraoperative detection of such false negatives. However, a calcified sac, atheromas, thickwalled vessels, and broad-neck aneurysms might not leave enough tissue to control the potential bleeding after sac incision, thus making the dome opening unsafe. From these findings, some authors suggested the use of intraoperative DSA.5,15,16 After an initial ICGV showing a complete occlusion of aneurysm, we have observed that a rather simple maneuver done with bipolar or Cushing bayonet forceps to test the aneurysm slackness allows assessment of the actual aneurysm obliteration under the same ICG injection and allows potential clip repositioning.
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ICGV FALSE-NEGATIVE CLIPPED ANEURYSMS
METHODS The Squeezing Maneuver The squeezing maneuver is based on a gentle pinch of the dome of a clipped aneurysm after ICGV has documented its apparent exclusion. The maneuver is carried out during the same ICG injection to confirm the actual exclusion of the dome. It is called positive when, after an initial ICGV shows the aneurysm exclusion, a gentle pinch of the slack aneurysm dome with a bipolar or Cushing bayonet forceps under ICGV visualization causes the prompt dyeing of the sac, suggesting that the aneurysm is still filling up (Figure 1). Conversely, the maneuver is called negative when, after pinching of the clipped dome, the sac does not fill up (Figure 2). Subsequent opening of the sac can confirm whether a flow is still filling the aneurysm. The purpose of the maneuver is to detect a potential deceptively excluded aneurysm, as previously shown by ICGV. The consequence is the opportunity to readjust the clip, allowing complete exclusion of the sac during the same procedure.
was performed after the ICGV showed no aneurysm remnants after clipping. Patients underwent a distinct surgical strategy based on the outcome of the maneuver. Indeed, when the maneuver was positive and the sac was promptly filled by the dye, the aneurysm was always secured by placing an additional clip or alternatively by repositioning the same clip. When the maneuver was negative and the sac did not fill up when the clipped dome was pinched, the clip was not repositioned. To verify the ICGV findings after the maneuver, the dome opening was always carried out when deemed safe and feasible by the surgeon. All patients underwent the assessment of sac exclusion both intraoperatively through ICGV and postoperatively with a computed tomographic angiography scan (or magnetic resonance angiography when computed tomographic angiography was not feasible). Patient and aneurysm features were correlated to the maneuver outcomes: patient age and aneurysm size, bleeding history of the aneurysm, atheromas of the neck or dome, and dome-to-neck ratio. To assess the role of this approach in the final aneurysm exclusion rate, the postoperative radiological findings were analyzed by an expert neuroradiologist blinded to intraoperative data and surgical strategy.
Patients and Surgical Strategy Data from 23 patients affected by intracranial aneurysms who underwent microsurgical clipping with the assistance of ICGV associated with the squeezing maneuver at our department between May and October 2013 were analyzed retrospectively. In all cases, the maneuver
RESULTS A total of 23 patients were enrolled in the study (Table 1). Median age was 60 years. Eleven patients presented with a ruptured
FIGURE 1. A female 56-year-old patient affected by a bilobated middle cerebral artery aneurysm (A). The initial indocyanine green videoangiography (ICGV) shows occlusion of both aneurysm sacs (B), but the bipolar clipping of the slack domes fills them with dye under ICGV visualization (C). Because little tissue is left in the aneurysm dome, a direct sac opening is not deemed safe. Indeed, the lack of space at the dome would not allow a second clip to be placed without removing the first, making potential bleeding difficult to control (D).
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FIGURE 2. A female 39-year-old patient affected by a middle cerebral artery aneurysm (A). The initial indocyanine green videoangiography (ICGV) shows aneurysm sac occlusion (B), and the bipolar clipping of the slack domes does not fill it with dye under ICGV visualization (C). The direct sac opening confirms aneurysm exclusion (D).
TABLE 1. Clinical and Surgical Features
Variables Investigated Postoperative computed tomographic angiography findings No remnant Remnant Atheromas Yes No Presentation Ruptured Unruptured Size, mm ,10 .10 Dome-to-neck ratio .2 ,2 Median age, y
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Total (n = 57), n
Group I (Squeezing) (n = 23), n
55 2
23 0
14 43
6 17
30 27
11 12
30 27
10 13
37 20 62
18 5 60
and 12 with an unruptured aneurysm. The aneurysm was at the middle cerebral artery level in 15 patients, at the anterior cerebral artery level in 6 patients, and at the internal carotid artery level in 2 patients. An atheromatous wall or neck was present in 6 patients. The aneurysm size was ,10 mm in 10 patients, whereas the dometo-neck ratio was .2 in 18 cases. Computed tomographic angiography was performed in 21 patients, and magnetic resonance angiography was done in 2 patients for different reasons (iodate contrast allergy in 1 patient and artifacts resulting from previous embolization in the other). Intraoperative data are summarized in Table 2. The maneuver was positive in 5 (22%) and negative in 18 (78%) of the 23 patients. The mean time at which the maneuver was performed was 14 seconds (range, 10-22 seconds). Actually, we waited and observed the aneurysm for .60 seconds after ICGV in all cases, as is usually done to assess the completeness of clipping. Indeed, the rational of the maneuver was not to replace the usual observation but to add a novel test to the usual aneurysm observation alone after ICGV. However, we performed the maneuver early, during the arterial phase, assuming that it could be the best moment to test the clip capacity; in fact, in no case did we detect an aneurysm filling over time after a negative maneuver. We performed the dome opening in 19 of 23 patients: 4 of 5 patients with a positive maneuver and 15 of 18 patients with
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ICGV FALSE-NEGATIVE CLIPPED ANEURYSMS
TABLE 2. Clinical and Surgical Features of Patients Who Underwent the Squeezing Maneuvera
Variables Postoperative computed tomographic angiography findings No remnant Remnant Atheromas Yes No Presentation Ruptured Unruptured Size, mm ,10 .10 Dome-to-neck ratio .2 ,2 Median age, y
Squeezing Negative, P n Value
Total, n
Squeezing Positive, n
23
5
18
23 0
5 0
18 0
—
6 17
5 0
1 17
.001
11 12
2 3
9 9
.99
10 13
2 3
8 10
.99
18 5 60
4 1 59
14 4 61
.99
a
Positive: aneurysms that fill with dye after the maneuver. Negative: aneurysms that do not fill with dye after the maneuver.
a negative maneuver. Among patients in whom the maneuver caused the prompt dyeing of the sac, all opened domes were found bleeding (4 of 4, 100%); conversely, in 1 patient, the dome incision was not feasible for the insufficient tissue remaining after additional clip positioning. Among patients in whom the maneuver did not cause the dyeing of the sac, in 1 case (of 15), the dome was found to be bleeding (7%). In all 5 cases with a positive maneuver, either the clip was repositioned or an additional clip was placed on the aneurysm neck. The strategy thus determined a rate of clip repositioning of 22%. A calcification/atheroma of the wall or neck was predictive of a positive maneuver (P = .001), whereas bleeding history, aneurysm size, and neck-dome ratio were not. With regard to the exclusion rate outcomes, no cases of remnants were reported at the radiological evaluation.
DISCUSSION The Issue of Misleading ICGV Data in Aneurysm Surgery The intraoperative occurrence of an aneurysm that looks apparently excluded (slack) but is not actually obliterated is not uncommon.14 To the best of our knowledge, the first 2 cases in the literature of aneurysms with ICGV evidence of complete obliteration, which after dome opening showed continuous bleeding, were reported by Mery et al.14 Another report indicates a 3.6% rate of false-negative ICGV-documented obliterated aneurysms, with persistent flow within the aneurysm after dome
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puncture.13 The authors found no morphological explanations that might have contributed to the failure of ICG in demonstrating persistent residual flow. Gruber et al8 described a case in which the postclipping manipulation of the sac of a fusiform anterior cerebral artery aneurysm, after initial negative ICGV and intraoperative DSA findings, revealed that the aneurysm was still filling from the superior anterior cerebral artery, as a further ICGV confirmed. Subsequent trapping of the superior anterior cerebral artery resulted in aneurysm occlusion. In a comment on that article, Raabe postulated that puncturing the aneurysm is the most reliable way to confirm its exclusion from circulation.8 However, in some cases, the amount of tissue of the aneurysm dome left after clipping may not be enough to allow a safe dome incision; furthermore, in cases with calcified walls or important atheromas, the sac opening is not feasible. Significance of the Squeezing Maneuver Our study presents a simple, safe, cheap, and fast maneuver to detect intraoperatively deceptive ICGV data on aneurysm exclusion after microsurgical clipping. This maneuver is simple and cheap because only a bipolar or bayonet forceps is needed. It is safe because, in all 23 cases, we did not detect aneurysm or brain damage, and no clips were displaced during the maneuver. It is fast because it takes only a few seconds through ICGV. Actually, the main question concerns the value and the role of the maneuver in the current microsurgical clipping practice. Indeed, some might argue that the issue being studied does not need a solution because a filling aneurysm after the maneuver could still potentially undergo spontaneous thrombosis. However, so far, ICGV has been reported to have a sensibility inferior to that of DSA as far as the obliteration assessment of clipped aneurysms is concerned.1-4,6-13 A recent study comparing ICGV and intraoperative DSA found a 14% rate of ICGV failure in detecting aneurysm exclusion.17 Could the patients with a falsely excluded clipped aneurysm at ICGV be detected, at least in part, by this maneuver? The 100% aneurysm exclusion rate achieved through the high clip repositioning rate (22%) reported in our study might be an answer. On the other hand, the high rate of nonexcluded aneurysm detected by the maneuver could mean that not only unsecured aneurysms but also aneurysms prone to rehabilitation over time are detected by the squeezing, which puts to test the mechanical strength of the clip. Further studies are needed to assess this issue. The main limitation of this study is that the data are retrospective and the application of the squeezing maneuver is not randomized, with consequent potential bias that may increase the actual impact of the maneuver. Indeed, in all cases, the maneuver was performed only when safe to carry out. In addition, we must emphasize that the gold standard to assess complete aneurysm occlusion and preservation of flow in the involved vessels remains DSA. This represents an additional bias of our study. Another remarkable issue concerns the safety of the maneuver. Indeed, we should bear in mind that this maneuver could be safe only in rather experienced hands because putting extra stress on an already stretched wall of a partly clipped aneurysm,
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DELLA PUPPA ET AL
especially at the neck region, might lead in less experienced hands to a serious tear close to the vessel. In addition, there is the possibility that partly clotted blood or calcified fragments may be pushed into the vessel lumen, potentially causing microembolism, if the maneuver is not performed gently. However, in our experience, no cases of stroke were clinically or radiologically detected. Our data show that the maneuver is highly recommended when the aneurysm presents an atheroma or a calcific wall; actually, the intraoperative exclusion assessment of this subgroup of aneurysms after clipping is challenging, and intraoperative DSA has been already suggested for this purpose.5,15,16 In our study, the maneuver outcomes were confirmed, whenever possible, by dome opening. In 80% of patients with a positive maneuver, the dome was opened, and in all cases, it was found to be actively bleeding. Conversely, 7% of patients had a bleeding aneurysm at dome opening after the sac did not fill up after the pinching of the clipped aneurysm, which means that a negative maneuver is not enough to warrant the exclusion of the aneurysm. Larger studies are needed to validate the clinical impact of our strategy.
CONCLUSION The intraoperative ICGV remains a very useful tool in aneurysm surgery. Squeezing the clipped aneurysm dome with bipolar/ Cushing bayonet forceps is a simple maneuver that controls the reliability of ICGV-assisted obliteration, especially in selected cases. This maneuver allows detection of deceptive ICGV data (false negatives) intraoperatively and clip repositioning or placement of an additional clip in the same surgical session. Disclosure The authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article.
REFERENCES 1. 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(1):132-139. 2. Raabe A, Nakaji P, Beck J, et al. Prospective evaluation of surgical microscopeintegrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg. 2005;103:982-989. 3. Wang S, Liu L, Zhao Y, Zhang D, Yang M, Zhao J. Evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. Neurosurg Rev. 2010;34(2):209-215. 4. de Oliveira JG, Beck J, Seifert V, Teixeira MJ, Raabe A. Assessment of flow in perforating arteries during intracranial aneurysm surgery using intraoperative nearinfrared indocyanine green videoangiography. Neurosurgery. 2008;62(6 suppl 3): 1300-1310. 5. Snyder LA, Sperzler RF. Current indications for green angiography. World Neurosurg. 2011;76(5):405-406. 6. Dashti R, Laakso A, Niemelä M, Porras M, Hernesniemi J. Microscope-integrated near-infrared indocyanine green videoangiography during surgery of intracranial aneurysms: the Helsinki experience. Surg Neurol. 2009;71(5):543-550. 7. Fischer G, Stadie A, Oertel JM. Near-infrared indocyanine green videoangiography versus microvascular Doppler sonography in aneurysm surgery. Acta Neurochir (Wien). 2010;152(9):1519-1525. 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(3):657-673; discussion 673.
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9. Imizu S, Kato Y, Sangli A, Oguri D, Sano H. Assessment of incomplete clipping of aneurysms intraoperatively by a nearinfrared indocyanine green-video angiography (Niicg-Va) integrated microscope. Minim Invasive Neurosurg. 2008;51:199-203. 10. Jing Z, Ou S, Ban Y, Tong Z, Wang Y. Intraoperative assessment of anterior circulation aneurysms using the indocyanine green video angiography technique. J Clin Neurosci. 2010;17(1):26-28. 11. Li J, Lan Z, He M, You C. Assessment of microscope-integrated indocyanine green angiography during intracranial aneurysm surgery: a retrospective study of 120 patients. Neurol India. 2009;57:453-459. 12. Ma CY, Shi JX, Wang HD, Hang CH, Cheng HL, Wu W. Intraoperative indocyanine green angiography in intracranial aneurysm surgery: microsurgical clipping and revascularization. Clin Neurol Neurosurg. 2009;111(10):840-846. 13. Özgiray E, Aktüre 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(7):870-878. 14. Mery FJ, Amin-Hanjani S, Charbel FT. Is an angiographically obliterated aneurysm always secure? Neurosurgery. 2008;62(4):979-982. 15. Chiang VL, Gaillouud P, Murphy KJ, Rigamonti D, Tamargo RJ. Routine intraoperative angiography during aneurysm surgery. J Neurosurg. 2002;96(6): 988-992. 16. Tang G, Cawley CM, Dion JE, Barrow DL. Intraoperative angiography during aneurysm surgery: a prospective evaluation of efficacy. J Neurosurg. 2002;96(6): 993-999. 17. Washington CW, Zipfel GJ, Chicoine MR, et al. Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg. 2013;118(2):420-427.
COMMENTS
I
ndocyanine green (ICG) videoangiography represents a relatively new technique that provides additional information on the perfusion physiology and occlusion rate of cerebral aneurysms. The technique is considered to be very helpful by many vascular neurosurgeons and represents a particularly valuable tool for all who do not proceed with intraoperative digital subtraction angiography in the operating room. The technique is very sensitive, and the number of intraoperative applications of the technique within 1 surgical procedure is limited. Thus, observations that, after aneurysm clipping, remnants of fluorescence dye mimic persistent aneurysm perfusion are not rare. In the present article, the authors report their experience with squeezing the aneurysm sac after clipping under ICG angiography. They suggest that ICG videoangiography is misleading in some cases; in particular, a falsepositive impression of complete occlusion of the aneurysm sac is stated to be frequent. Based on this background, a series of 23 aneurysm clippings is reported in which a positive squeezing maneuver was demonstrated in 80% of the incomplete clipped aneurysms (4 of 5). The study is well written and well illustrated. I think that the idea of squeezing the aneurysm sac after clipping to evaluate the aneurysm occlusion is a nice idea. The technique appeals by its easy performance and its availability. However, I personally—not having ever done the squeezing maneuver in any ICG aneurysm clipping—think of squeezing the aneurysm and causing its rupture. What now? Will I be able to clip the aneurysm in the same safe way I would have done it without the rupture? In addition, the study is based on just 5 cases of incomplete aneurysm clipping. Thus, more experience is needed before a definite decision on the value of this simple technique for aneurysm clipping can be made. Joachim Oertel Mainz, Germany
T
his is an interesting article reporting a technique for verifying aneurysm occlusion after indocyanine green (ICG) angiography. I
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ICGV FALSE-NEGATIVE CLIPPED ANEURYSMS
am convinced that it is clinically useful, but how useful remains unanswered. Technically, the detection of residual filling after incomplete clipping requires “late” images. This is opposite of the detection of branch stenosis/occlusion in which the early inflow images at the time of dye arrival are most important. To diagnose potential residual filling of the aneurysm, I usually wait 60 seconds after the first arterial filling to ensure that the aneurysm remains completely dark. If the diagnosis of complete occlusion is made before this time, it may be false negative. There have been reports of bleeding after dome puncture in aneurysms in which ICG showed complete occlusion, but there is no information on how long the aneurysm was inspected after ICG angiography. In this report, the squeezing test was performed after a mean of 14 seconds; in Figure 1B, the image confirms complete occlusion even after 3.7 seconds. Thus, I assume that some of the aneurysms might have shown late filling after 60 seconds. If the aneurysm remains completely dark 60 seconds after ICG arrival, the consequence of any microleakage remains questionable. I personally do not open the sac routinely (except in unclear cases), and I have never seen residual filling of the aneurysm sac in such cases in a postoperative angiogram, provided that the wall of the aneurysm was calcified and the aneurysm was not thrombosed. Nonetheless, the
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technique of gently squeezing the aneurysm will force some outflow of blood and then inflow of dye in incompletely clipped aneurysms, and vascular neurosurgeons should know this technique. Andreas Raabe Bern, Switzerland
T
his is a very important article describing a problem that has probably been encountered by many vascular neurosurgeons and that might have been considered a rare event. In fact, mechanical manipulation of a clipped aneurysm under indocyanine green (ICG) videoangiography resulted in residual aneurysm filling in 21.7% of the cases in this retrospective analysis. The authors identified atheromatous plaques in the neck area as a possible reason, indicating that the squeezing maneuver described will result in visible ICG inflow into the aneurysm sac in the presence of mechanically suboptimal clip closure. This can be considered an advantage of ICG videoangiography over digital subtraction angiography because a mechanical challenge to the mechanical strength of the clip is usually not possible during a digital subtraction angiography run. Andreas Gruber Vienna, Austria
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