In intracranial neurosurgery, few procedures

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1 Vascular: Aneurysm Optimal Clip Application and Intraoperative Angiography for Intracranial Aneurysms T.C. Origitano, M.D., Ph.D.,* Karin Schwartz, M.D.,* Douglas Anderson, M.D.,* Behrooz Azar-Kia, M.D., and O. Howard Reichman, M.D., FACS* Departments of *Neurological Surgery, Physiology, and Radiology, Section of Neuroradiology, Loyola University Medical Center, Maywood, Illinois Origitano TC, Schwartz K, Anderson D, Azar-Kia B, Reichman OH. Optimal clip application and intraoperative angiography for intracranial aneurysms. Surg Neurol. Address reprint requests to: Dr. T.C. Origitano, Associate Professor, Department of Neurological Surgery, Loyola University Medical Center, 2160 South First Avenue, Maywood, IL Received June 9, 1997; accepted September 25, BACKGROUND The actual incidence of residual aneurysm after clipping is unknown. The natural history of residual aneurysm can be regrowth and hemorrhage. Intraoperative angiography offers a cost-effective, safe interdiction to the problem of residual aneurysm and parent vessel stenosis. METHODS/RESULTS Forty consecutive patients harboring 54 aneurysms underwent 42 operative procedures to clip 52 aneurysms, during which 220 intraoperative angiographic runs were performed. Ninety-three percent of the procedures were performed on patients with acute subarachnoid hemorrhage. There were 4 giant ( 2.5 cm, 4/52 8%, all anterior circulation), 21 large ( cm, 21/52 40%, 16/ 21 76% anterior circulation, 6/21 28% posterior circulation), and 27 small ( 1.0 cm, 27/52-52%, 22/27 81% anterior circulation, 5/27 18% posterior circulation) aneurysms. Intraoperative angiography led to clip adjustment in 18/52 34% of aneurysms (4/18 22% for parent artery stenosis, 8/18 44% for residual aneurysm and 6/18 33% for both). Of the 18 adjustments made, 16 88% were made on giant or large aneurysms and two were small (one was a complex anterior communicating and one was a vertebral junction aneurysm). Follow-up angiography was performed on 26/42 62% of operative cases. Postoperative angiography confirmed intraoperative angiography in all cases. Two complications occurred during 220 angiographic runs: one embolic stroke and one incident of equipment failure. CONCLUSION A grading scale was applied to test the relationship between anatomical site and size as they relate to the necessity for clip adjustment for complete aneurysm obliteration and/or parent artery compromise. Significance was related to site (basilar bifurcation, anterior communicating, middle cerebral bifurcation, and ophthalmic) and size ( 1.0 cm), both as independent and codependent variables. An analysis of the cost-effectiveness of intraoperative angiography was demonstrated by Elsevier Science Inc. KEY WORDS Aneurysm grading scale, intracranial aneurysm, intraoperative angiography, parent vessel stenosis, suboptimal clip position. In intracranial neurosurgery, few procedures promise the possibility of complete cure. Obliteration of an intracranial aneurysm by clip ligation carries with it the greatest potential and expectation for such an outcome. Literature values for residual aneurysm after clip ligation range from % with a range for parent vessel occlusion being % [4 8,10 15,16]. The true scope of suboptimal clip placement is unknown because the overwhelming majority of operated aneurysms are not followed up with angiography. The complications of suboptimal clip placement are legend: regrowth of the aneurysm with subsequent hemorrhage, mass effect, and/or stroke with parent artery occlusion [4 10,15,16]. Location (deep, midline, complex) and size (large/giant) may be important factors in successful clip application [3,11 14]. Intraoperative angiography provides a means to assess and intervene in suboptimal clip placement and/or confirm optimal clip placement. This opportunity for direct assessment can be life-saving for the patient and gratifying for the surgeon. Patients and Methods Forty consecutive patients (24 females, age years; 16 males, age years; mean SD) harboring 54 aneurysms underwent 42 operative procedures to clip 52 aneurysms (Table 1) by Elsevier Science Inc /99/$ see front matter 655 Avenue of the Americas, New York, NY PII S (97)

2 1 Demographics of Intraoperative Angiographic Cases PT SEX AGE ACUTE SAH LOCATION OF ANEURYSM SIZE MODIFIED CLIP APPLICATION INTRA-OPERATIVE ANGIOGRAPHY PARENT ARTERY STENOSIS RESIDUAL ANEURYSM BOTH COMPLICATION F/U POST-OP ANGIOGRAPHY 1 M 65 yes (L) MCA giant yes none not performed 2 F 35 yes A Comm small no none confirmed 3 M 75 yes (R) MCA giant yes none confirmed 4 F 67 yes (R) SCA small no none not performed 5 F 47 yes (L) ophthalmic large yes none confirmed no (R) P Comm small no none confirmed 6 F 54 yes basilar tip large yes none confirmed no (R) MCA large yes none confirmed 7 F 51 yes (R) SCA small no none confirmed 8 F 46 yes (R) MCA trifurcation n 1 large yes none confirmed (R) MCA (M 1 )n 2 small 9 M 29 yes A Comm small yes none confirmed 10 F 55 yes (R) MCA large yes none confirmed 11 M 37 no (L) ophthalmic large no none not performed 12 F 51 yes (L) P Comm small no none not performed 13 M 39 yes basilar bifurcation large yes none confirmed 14 F 68 yes (R) P Comm small no embolization not performed 15 F 58 yes (L) MCA small (L) P Comm small no none confirmed (L) ophthalmic small (R) ICA bifurcation large no not performed 16 F 46 yes A Comm small no none confirmed 17 M 56 yes (R) P Comm large no none not performed 18 M 37 yes (R) MCA large no none not performed 19 M 32 yes VB junction small yes none confirmed 20 M 86 yes (R) P Comm small no none not performed 21 F 53 yes A Comm small no none not performed 22 M 49 yes (R) MCA large not operated (L) MCA large yes none confirmed 23 F 48 no (L) ophthalmic small no none not performed 24 M 58 yes A Comm large yes (R) MCA large yes none confirmed basilar bifurcation large no 25 F 48 yes A Comm large yes none not performed 26 M 43 yes basilar bifurcation large yes none confirmed 27 F 56 yes basilar bifiurcation large yes none not performed (L) MCA small not operated 28 F 49 yes A Comm small no none not performed ICA large no 118 Surg Neurol Origitano et al

3 Advantages of Intraoperative Angiography Surg Neurol Demographics of Intraoperative Angiographic Cases (continued) INTRA-OPERATIVE ANGIOGRAPHY F/U POST-OP ANGIOGRAPHY COMPLICATION RESIDUAL ANEURYSM BOTH PARENT ARTERY STENOSIS MODIFIED CLIP APPLICATION ACUTE SAH LOCATION OF ANEURYSM SIZE PT SEX AGE 29 F 55 yes (L) P Comm large no none confirmed 30 M 50 yes (R) posterior cerebral large no none confirmed 31 M 38 yes (L) ICA giant yes none confirmed 32 M 47 yes (L) MCA small no none confirmed A Comm small no 33 F 54 yes A Comm small no equipment failure failure (L) MCA small no none confirmed 34 F 58 no (L) ophthalmic giant yes none confirmed 35 F 59 yes (R) P Comm small no none confirmed 36 F 69 yes A Comm small no none not performed 37 F 35 yes (L) ICA bifurcation small no none confirmed 38 M 40 yes A Comm large no none confirmed 39 F 46 yes SCA small no none not performed 40 F 33 yes mid basilar small no none not performed Two-hundred and twenty intraoperative angiographic runs were performed on the 52 aneurysms. Acute subarachnoid hemorrhage was associated with 92.5% of the cases. At our institution, patients with aneurysmal subarachnoid hemorrhage (Grade IV or better without significant medical comorbidity) are operated within 24 hours of admission. Four-vessel cerebral angiography is performed at the time of admission (unless admission is between 2200 and 0500, in which case it is delayed to 0600 the next day). Our intraoperative angiographic protocol consisted of femoral artery access followed by placement of a heparinized angiographic catheter into the appropriate parent artery (carotid or vertebral) while in the angiographic suite with subsequent transfer to the operating room. The heparin drip through the catheter was maintained continuously via an infusion pump (1000 u/500 cc NS, 3 5 cc/ hour). Two patients had both anterior and posterior circulation aneurysms that necessitated bilateral femoral access for intraoperative evaluation. At the completion of the diagnostic study, the parent vessel best visualizing the aneurysm is cannulated with a heparinized catheter and the patient is transported directly to the operating room (heparin drip infusion 1000 u/500 cc NS, 3 5 cc/hour). If the operating room cannot be sequentially entered after angiography, the femoral access catheter is covered with a sterile dressing and the patient is returned to the angiography suite for parent artery catheterization before surgery. Once in the operating room, two basic plans are followed depending on the surgeon s discretion. PLAN ONE The intraoperative digital fluoroscope is positioned at the head of the patient and a series of angiographic runs are made to optimize aneurysm visualization. The fluoroscope is draped into the field. This plan has the advantage of on-demand, instantaneous angiogram. Its disadvantages are limitation in number of views that can be taken and restrictions of movement around the fluoroscope by the surgeon and assistant. PLAN TWO Initial fluoroscopy is performed to reproduce the orientation of the skull to the X-ray beam, which demonstrated the best view of the aneurysm in the angiography suite. The fluoroscope is then positioned directly behind the surgeon and moved into place at the time of clipping. A preclipping examination is then obtained, the clip placed, and confirmation angiography performed.

4 120 Surg Neurol Origitano et al 2 Proposed Aneurysm Grading Scale Size Site Small 0 Ophthalmic 1 Large 1 MCA trifurcation 1 Giant 2 A Comm 1 Basilar bifurcation 1 Other 0 Score Simple 1 Complex 2 In either plan, multiple views of each aneurysm are taken by rotating the patient, fluoroscope, or both. Only when, in two separate views, the aneurysm is demonstrated to be obliterated and all associated vessels accounted for is clip placement deemed optimal. Once optimal clip placement is confirmed, the angiographic catheter is pulled. The femoral introducer catheter is removed in the recovery room. Twenty-four patients who underwent 26/42 procedures (62%), harboring 35 aneurysms, underwent postoperative angiograms at 7 10 days postoperatively as part of a second study. To validate the observations that size and location may play a role in optimal clip placement, a grading scale was developed (Table 2). Efficacy of the scale in predicting the need for clip modification was then tested. Univariate analyses were conducted using the t-test and one-way analysis of variance for continuous variables. The Chi square test and, as appropriate, the Fisher s exact test were used for categorical measures. Multivariate analyses were conducted using logistic regression techniques with full models and stepwise procedures. For all tests a two-sided alpha level of 0.05 was considered statistically significant. Results Clip modification was prompted by intraoperative angiography in 18/52 cases (34%). The reasons for clip modification were: residual aneurysm 8/18, 44%; parent vessel stenosis only 4/18, 22%; and both residual aneurysm and parent vessel stenosis 6/18, 33%. We experienced two complications, one technical and one clinical. The technical complication was an equipment failure that resulted in a 5-cc contrast injection without image capture. This was corrected and a confirmatory angiogram was subsequently obtained. A single embolic complication occurred during the 42 procedures/220 angiographic runs (2.3%/ 0.4%, respectively). This occurred in a patient who was discovered to have significant cervical carotid atherosclerotic disease. Average intraoperative catheter time (insertion in angiographic suite to removal in operating room) was minutes. Interestingly, the case in which the embolization occurred had only 157 minutes of catheter time. All of the 26 postoperative angiograms (100%) confirmed intraoperative findings. Univariate and multivariate analysis of the occurrence of clip modification based on aneurysm size, cerebral circulation (Table 3), anatomical site (Table 4), and patient age and sex were performed. The univariate analysis of independent variables demonstrated that the rate of clip modification was similar for males (53%) and females (30%) (p 0.08). A significant association was detected between gender and size of aneurysm, with males tending to have larger aneurysms than females (p 0.004). Age did not demonstrate any significant differences in the rate of clip adjustment (p 0.52) and did not seem to be associated with size or location (p 0.32)/(p 0.60), respectively. Large and giant aneurysms are more prone to errant clip placement (16/25; 64% of total events). This is in comparison to 2/27 (7%) for small aneurysms. There was a significant increase in the rate of clip adjustment with increasing aneurysm size (7% small, 57% large, 100% giant) (p 0.001). Interestingly, location (anterior versus posterior circulating) was not a significant indicator. There was no difference in the rate of adjustment for anterior circulating (34%) as compared with posterior circulating (36%) aneurysms. Aneurysms located at anatomical sites with multiple inflow and distal outflow vessels, midline, deep (anterior communicating, middle cerebral basilar bifurcation), and ophthalmic lesions, because of their complicated relationship to the optic nerve and anterior clinoid process, had a highly significant association with clip modification (p 0.006). Multivariate analysis confirmed the combination of size (large or giant) (p 0.001) and site (middle cerebral artery, anterior communicating, ophthalmic, basilar bifurcation) (p 0.02) constituting 15/18 (83%) of the suboptimal clip applications to be highly significant (p ). Analysis of the proposed grading scale demonstrated statistical significant with a p ; however, this grading, based on this data set, would be predicted to have a 7.7% false positive and false negative rate. These findings may reflect the sample size.

5 Advantages of Intraoperative Angiography Surg Neurol Aneurysms by Size and Location ANTERIOR CIRCULATION NO. SUB N 41 N 52 CLIP ADJUSTMENT STENOSIS RESIDUAL BOTH S SPECIFIC SIZE SUB N 41 N 52 Small 22 54% 42% % 2% 2% Large 15 36% 29% % 22% 17% Giant 4 10% 8% % 10% 7% Subtotal POSTERIOR CIRCULATION NO. SUB N 11 N 52 CLIP ADJUSTMENT STENOSIS RESIDUAL BOTH S SPECIFIC SIZE SUB N 41 N 52 Small 5 45% 10% % 9% 2% Large 6 55% 11% % 27% 6% Giant Subtotal Total Total Clip Adjustment N 18 Discussion Complete obliteration of an intracranial aneurysm with preservation of associated inflow and egress vessels carries an expectation of cure. The actual incidence of residual aneurysm or parent vessel occlusion is unknown in that routine intraoperative or postoperative angiography is not performed on the majority of operated intracranial aneurysms. Clearly, regrowth and hemorrhage can and do occur after incomplete obliteration resulting in a suboptimal outcome. As early as 1967, Drake reported on the hazards of incomplete treatment [5]. In a study of 70 cases in which postoperative angiography was performed, 45/70 (64%) demonstrated complete obliteration, 12/70 (17%) had small resid- 4 Aneurysms by Anatomic Site ANTERIOR CIRCULATION NO. SUB N 41 N 52 CLIP ADJUSTMENT STENOSIS RESIDUAL BOTH S SPECIFIC SIZE SUB N 13 N 18 Ophthalmic 5 12% 9% % 15% 11% P Comm 8 19% 15% ICA 4 10% 7% % 8% 5.5% A Comm 11 27% 21% % 23% 16% MCA 13 31% 25% % 54% 39% Subtotal % 13/41 (32%) POSTERIOR CIRCULATION NO. SUB N 11 N 52 CLIP ADJUSTMENT STENOSIS RESIDUAL BOTH S SPECIFIC SIZE SUB N 5 N 18 Basilar 5 45% 9% % 80% 22% bifurcation Posterior 1 9% 2% cerebral Superior 3 27% 6% cerebellar Mid-basilar 1 9% 2% VB junction 1 9% 2% % 20% 5.5% Subtotal % 5/11 (45%) Total 52 18

6 122 Surg Neurol Origitano et al ual, and 13/70 (17%) had whole or large residual aneurysms. Rebleeding occurred in 4/12 (33%) with small residual, resulting in three deaths and 7/13 (54%) with large residual, resulting in six deaths. Rebleeding occurred up to 11.5 years after initial incomplete treatment. Sato and Suzuki reported 11 residual aneurysms of 303, which had been clipped/ ligated (3.6%) with a 14.3% mortality rate [15]. Drake and Allcock reported 43 of 329 (13%) who underwent postoperative angiography demonstrated incomplete obliteration, with 12/43 experiencing rebleeding (28%) [4]. Drake further reported on a series of 115 re-operations [6]. The reasons for reoperation were rebleeding in 24/115 (21%) and mass effect in 17/115 (15%). Feuerberg reported residual aneurysm in 27/715 patients (3.8%) [8]. One rehemorrhage occurred within a mean follow-up of 8 years. Lin reported 19 patients with known residual neck, 15/19 (79%) had recurrent hemorrhage, 2/19 (10%) had mass effect with an interval of 4 20 years before second presentation; 5/17 (29%) died, and 2/17 (12%) had a poor outcome [10]. Giannotta recently reported 19 patients with residual aneurysm; 5/19 presented with rebleed (26%), and 6/19 (32%) with mass effect, with an average time interval from treatment to recurrent hemorrhage or mass effect of 10.5 and 9.75 years, respectively [9]. These studies demonstrate that the incidence of residual aneurysms is in the range of 3 18% [4 10,15]. These results occur in the hands of some of the most experienced and skilled aneurysm surgeons. The consequences of these residuals are frequently not benign. MacDonald reported on 66 patients having 78 cerebral aneurysms who underwent controlled postoperative angiograms [12]. Unexpected residual aneurysms were seen in 3/78 (4%); three additional aneurysms were noted to be completely unclipped. Nine unexpected major vessel occlusions were noted, resulting in six strokes and two deaths. Rauzzino reported on 228 consecutive patients harboring 313 intracerebral aneurysms who underwent postoperative selective angiography [14]. Thirteen cases of residual aneurysm (4.2%) and one case of major vessel occlusion (0.32%) were found. Additionally, three cases of incidental aneurysms not identified on the preoperative angiograms were found. Residual aneurysms led to rehemorrhage in three and mass effect in one within 2 years of their primary procedure. In both studies new onset of neurologic deficit postoperatively was correlated with major vessel occlusion found on postoperative angiography. In light of their results, both authors recommended prompt reoperation for residual aneurysms and suggested intraoperative angiography for detection of major vessel occlusion [12,14]. Intraoperative angiography offers a number of advantages over conventional postoperative angiography. Primarily, it allows for interdiction of improper clip placement, which would have led to parent artery compromise, residual aneurysm, or worse, both. Martin reported on 51 patients with 57 large and giant aneurysms (anterior communicating artery, middle cerebral, vertebrobasilar, and multiple aneurysms) undergoing intraoperative angiography [11]. Selective arterial catheterization occurred in the operating room. Average time required for intraoperative angiography was minutes. In five cases (5/57, 8.8%) aneurysm clip repositioning was required (residual aneurysm, 2; parent vessel compromise, 3). Postoperative angiography was performed in 22 cases. There were two false negatives. One clip appeared to have moved secondarily between the intraoperative and postoperative angiograms. In the second case, residual neck was hidden behind superimposed vessels. Because of the small size of the residual aneurysm, the patient was followed. A recurrent hemorrhage occurred 1 year later. Complications directly related to intraoperative angiography in this series (105 procedures for aneurysm and AVM) were one cerebral embolus (AVM case), one foot embolus (AVM case), and one femoral artery occlusion (aneurysm case) that spontaneously reopened. No cerebral infarctions from unrecognized arterial occlusions occurred. Barrow presented a series of 64 intraoperative angiographic procedures for intracerebral aneurysm [1]. Femoral catheterization occurred in preoperative holding. Selective arterial catheterization occurred in the operating room. Seven patients had operative interdiction based on intraoperative angiography (two angiograms demonstrated unclippable aneurysms requiring bypass, one a compromised parent vessel, two residual aneurysms, and one showed parent artery kinking; in the final case, angiogram showed good collateral after trapping of the aneurysm, making bypass unnecessary). Seventeen patients in the aneurysm series underwent postoperative angiography. One false negative was found. Complications included one distal embolus and one late aortic dissection (patient had a total of four angiographic procedures). Derdeyn reported 66 intraoperative studies on 63 patients undergoing aneurysm clipping [3]. Again, intraoperative angiography was used for complex or giant aneurysms. Femoral access sheaths were placed before surgery. Selective catheterization of the desired artery was performed immediately before angiography. Multiple views were obtained of each lesion. Intraoperative angiography led to five

7 Advantages of Intraoperative Angiography Surg Neurol Institutional Costs for Major Expenses in Aneurysm Care TREATMENT HOSPITAL SURGEON/ PHYSICIAN Unruptured aneurysm $26,000 $8,000 Ruptured aneurysm $92,000 $8,000 Conventional four-vessel $1,467 $2,780 angiogram Selective single vessel $847 $2,085 angiogram Intraoperative angiogram $2,215 $1,810 clinically significant changes in surgical management (three for unsuspected secondary aneurysms, two for branch occlusion). One embolic complication was associated with intraoperative angiography for aneurysms (1.5%). Conventional postoperative angiography was performed on 25 of the 66 aneurysm patients (primarily for vasospasm). False negatives were observed in 3/25 cases (12%). Two were unexpected residuals and one resulted from clip migration. What is the actual incidence of suboptimal clip application leading to residual aneurysm and/or parent vessel compromise following intracranial aneurysm surgery? The fact is that it is unknown. This is in the face of the great scrutiny being applied to the endovascular treatment of intracranial aneurysms where multiple repeat angiography is demanded to demonstrate efficacy. Pooling literature values from studies on intraoperative and postoperative angiography (constituting 1,329 cases), the necessity for clip adjustment ranges from 4 to 21% [1 3,8,11,12,14]. It has been observed by the majority of these authors that size (large or giant), 6 Overall Cost Analysis A. Cost of intraoperative angiography (42 procedures on 52 aneurysms) B. Cost of postoperative angiography (42 procedures on 52 aneurysms) C. Cost of re-operation if all aneurysms were found unruptured after routine post-operative angiogram (in our series, 18 patients would require reoperation) D. Additional overall cost of management by routine postoperative angiography and reoperation (B C) E. Cost of re-operation on eight patients who would potentially rehemorrhage from suboptimal clip placement should no postoperative or intraoperative angiography be performed $169,050 $152,204 $612,000 $764,204 $833,576 location (deep, midline), and anatomical complexity (multiple inflow and outflow vessels, proximity to optic nerve/clinoid process) seem to influence clip application [1,11,12,14]. Our overall rate of clip adjustment of 33% seems high. When adjusted for size, our rate compares favorably with the published literature, especially considering the number of aneurysms in the large/ giant category (46%) [1,3,8,11 14]. A second factor that has to be considered is human nature. The ability to check clip application to attain the perfect post-clipping angiogram may increase clip manipulation. Application of the proposed aneurysm grading scale permits selection of those aneurysms most likely to benefit from intraoperative angiography. Complex aneurysms (score, 2), either by distinction of overall size or specific site, have a statistically significant higher risk of clip malplacement. As an example, posterior communicating artery aneurysms, unless giant in size, are probably safe to clip without intraoperative angiography, whereas large, anterior communicating artery aneurysms or basilar bifurcation aneurysms would benefit. Today, benefit is not only defined in terms of clinical outcome but also in terms of cost analysis. Listed in Table 5 are major institutional costs for a ruptured and unruptured aneurysm. The major difference in expenses is hospital cost, related to additional length of stay associated with post-bleed pathology. Assuming that mean of rehemorrhage rate for suboptimally clipped aneurysms is 42% [4 9,15] in our series, eight patients ( ) could potentially go on to rehemorrhage and/or have mass effect requiring reoperation. Table 6 applies our institutional costs as related to overall cost for treatment of our aneurysm population. Cost comparison of different treatment options (intraoperative angiography, postoperative angiography with reoperation for suboptimal clip placement, and reangiography/reoperation after rehemorrhage) are found in Table 7. Significant cost savings of approximately 80% can be found in our patient population using intraoperative angiography over both the postoperative angiography and rehemorrhage scenarios. These savings are present even if the up-front costs of the angiography unit are included as they amortize over the entire patient population. Intraoperative angiography allows for safe, costeffective interdiction leading to optimal clip application. No other treatment scenario can ensure parent vessel patency at a time when intervention is still possible. Accuracy as to residual neck is enhanced by multiple intraoperative views. Intra-

8 124 Surg Neurol Origitano et al 7 Cost Comparisons A. Intraoperative angiography $169,050 (22%) Postoperative angiography and re-operation $764,204 B. Intraoperative angiography $169,050 (20%) Rehemorrhage scenario $833,576 C. Cost of intraoperative angiographic unit $150,000 operative angiography cannot resolve perforator sacrifice or delayed clip migration. No technique available today can. Using the proposed aneurysm grading scale should influence which cases are performed that use intraoperative angiography to enhance optimal clip placement and therefore overall outcome. We thank Susan Fisher, Ph.D., for statistical support; Wink S. Fisher III, M.D., of the University of Birmingham for sharing his extensive and thought-provoking experience on postoperative angiography; and Mary Vinelli and Jill Wallock for manuscript preparation. REFERENCES 1. Barrow DL, Boyer KL, Joseph GJ. Intraoperative angiography in the management of neurovascular disorders. Neurosurg 1992;30: Bauer BL. Intraoperative angiography in cerebral aneurysm and arteriovenous malformations. Neurosurg Rev 1984;7: Derdeyn CP, Moran CJ, Cross DT, Grubb RL, Dacey RG, Jr. Intraoperative digital subtraction angiography: a review of 112 consecutive examinations. Am J Neuroradiology 1995;16: Drake CG, Allcock JM. Post-operative angiography and the slipped clip. J Neurosurg 1973;39: Drake CG, Vanderlinden RG. The late consequences of incomplete surgical treatment of cerebral aneurysms. J Neurosurg 1967;27: Drake CG, Friedman AH, Peerless SJ. Failed aneurysm surgery: re-operation in 115 cases. J Neurosurg 1984; 61: Ebina K, Suzuki M, Andoh A, Saitoh K, Iwabuchi T. Recurrence of cerebral aneurysm after initial neck slipping. Neurosurg 1982;11: Feuerberg I, Lindquist C, Lindquist M, Steiner L. Natural history of post-operative aneurysm tests. J Neurosurg 1987;66: Giannotta SL, Litofsky NS. Reoperative management of intracranial aneurysms. J Neurosurg 1995;83: Lin T, Fox AJ, Drake CG. Regrowth of aneurysmal sacs from residual neck following aneurysm clipping. J Neurosurg 1989;70: Martin NA, Bentson J, Vinuela F, Hieshima G, Reicher M, Black K, Dion J, Becker D. Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Neurosurg 1990;73: MacDonald RL, Wallace MC, Kestle JRW. Role of angiography following aneurysm surgery. J Neurosurg 1993;79: Pasquelini A, Battaglia R, Scienza R. Italian cooperative study of giant intracranial aneurysms: three modalities of treatment. Acta Neurochir Suppl 1988;42: Rauzzino M, Fisher WS. Angiography after aneurysm surgery: indicators for selective angiography [abstract]. Neurosurg 1995;37: Sato S, Suzuki J. Prognosis in cases of intracranial aneurysms after incomplete direct operations. Acta Neurochir 1971;24: Weir B. Aneurysms affecting the nervous system. Baltimore: Williams & Wilkins, COMMENTARY The authors report a series of operative procedures for intracranial aneurysms performed in conjunction with intraoperative angiography. Intraoperative angiography led to clip adjustment in 18/52 (34%) of aneurysms. According to their grading scale, the necessity for clip adjustment for complete aneurysm obliteration and/or parent artery compromise was significantly related to the site (basilar bifurcation, anterior communicating, middle cerebral bifurcation, and ophthalmic) and/or the size (large and giant) of the aneurysm. They conclude that aneurysms in these categories would benefit from intraoperative angiography. Previously, a number of neurosurgeons have stressed the benefits of intraoperative angiography in neurosurgery [1], primarily in the management of arteriovenous malformations (AVMs). We also have applied intraoperative digital subtraction angiography to the management of AVMs and aneurysms since We have used intraoperative DSA essentially only to confirm eradication of the lesion during AVM resections. In comparing the results of intraoperative DSA with those of postoperative DSA as part of a second study, we have found no residuals. The key points for success in aneurysm surgery are the complete closure of the aneurysm neck and preservation of the parent artery and all adjacent arterial branches. We usually perform aneurysm clipping without the use of intraoperative DSA because those findings do not predict the delayed postoperative events caused by clip migration, as mentioned in this article. We verify the position of

9 Advantages of Intraoperative Angiography Surg Neurol 125 the clip by direct view; we open the cistern around the aneurysm widely, dissect the aneurysm neck from the artery and the branch vessels, and collapse the aneurysm sac by aspiration. The patency of the parent artery and perforators are checked with bidirectional ultrasonic Doppler (DVM-4200p, HDECO, Kawasaki, Japan). However, DSA is useful in the surgical treatment of large and broad-based aneurysms as well as aneurysms in deep locations where a wide operative field cannot be obtained, such as those on the proximal carotid artery and in the posterior circulation [2,3]. A wide operative field can usually be obtained by full dissection of the sylvian fissure in middle cerebral artery aneurysms. For complex anterior communicating artery aneurysms, a bifrontal interhemispheric approach will allow a wide enough surgical field, thus making intraoperative DSA necessary only occasionally. In addition to evaluating aneurysm clipping, we use intraoperative DSA for the management of large aneurysms of the proximal internal carotid artery and the vertebrobasilar artery to introduce balloon catheters for temporary occlusion, as well as retrograde suction decompression of the aneurysm. Takashi Yoshimoto, M.D. Hiroyuki Kinouchi, M.D., Ph.D. Department of Neurosurgery Tohoku University School of Medicine Sendai, Japan REFERENCES 1. Martin NA, Bentson J, Vinuela F, Hieshima G, Reicher M, Black K, Dion J, Becker D. Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Neurosurg 1990;73: Mizoi K, Takahashi A, Yoshimoto T, Fujiwara S, Koshu K. Combined endovascular and neurosurgical approach to paraclinoid internal carotid artery aneurysms. Neurosurgery 1993;33: Mizoi K, Yoshimoto Y, Takahashi A, Ogawa A. Direct clipping of basilar trunk aneurysms using temporary balloon occlusion. J Neurosurg 1994;80: This paper prospectively analyzes the positioning of the aneurysm clip according to intraoperative angiography in 40 consecutive patients harboring 54 intracranial aneurysms. The very high overall rate of clip adjustment (33%) because of parent artery stenosis, residual aneurysm, or both in this series is in part related to the large number of large and giant aneurysms (46%). This is demonstrated by the significant increase in the rate of clip adjustment with the increase in aneurysm size: 7% in small, 57% in large, and 100% in giant aneurysms. The authors do not describe what they do after clipping the aneurysm to ensure that it is completely clipped before performing intraoperative angiography; that would probably explain the most important reason for the very high rate of clip adjustment. In our service, most of the time after placing the first clip on the neck of the aneurysm, we open the aneurysm, shrink it with bipolar coagulation, and then reclip it with a smaller clip and proceed with a review of the surrounding arteries. This procedure allows better visualization and also prevents parent artery stenosis and aneurysm rests. We do not use intraoperative angiography, because it is not available in our service, but we routinely perform postoperative angiography in all aneurysm patients. In the last 1280 operated patients over the last 12 years, we had a rate of only 2.8% of residual aneurysm and/or parent artery stenosis. All of these were cases of giant aneurysms. Therefore, I conclude that the reason for the high rate of clip adjustment in the series described in this paper is that the surgeons do not follow the above-described procedures before doing the intraoperative angiography. I do recommend that intraoperative angiography be used, but only in cases of giant aneurysms in any location, particularly those in the posterior circulation where intraoperative difficulties can be expected. Atos Alves de Sousa, M.D. Neurosurgeon Belo Horizonte, Brazil I enjoyed this paper. It is well written, the arguments are rationally presented, and the information the authors provide on the technique and results, as well as a hypothetical cost analysis is, I think, quite worthwhile. Now, the problem here is that the statistics are based on very few patients, making all of the statistics a bit uncertain. As well, it is disappointing that they weren t able to do more postoperative angiograms on this small series to confirm what they think they saw in the operating room, because I have found that to be the biggest shortcoming with this technique the difficulty of being absolutely certain that one can interpret the images using a technique really identical to theirs. This is a technique I currently use in probably less than 15% of the patients I operate on; always on aneurysms that are large and complex in which I know that accurate anatomical placement of the clip is going to be difficult and visualization after the clip is in place might be impossible. S.J. Peerless, M.D. FRCSC Neurosurgeon Mercy Neuroscience Institute Miami, Florida

10 126 Surg Neurol Origitano et al This paper is a valuable addition to our knowledge in regard to the value of intraoperative angiography in the surgical management of intracranial aneurysms. The aim of intraoperative angiography is to offer the neurosurgeon security in the prevention of residual aneurysm neck or associated vascular compromise. Experienced vascular neurosurgeons are very familiar with the necessity of clip adjustment to secure satisfactory aneurysm repair and avoid parent or associated vessel stenosis. In my own practice, I always puncture the aneurysm to ensure that it is securely clipped, and then perform postoperative angiography to ensure satisfactory repair and to be certain that there is no residual neck or slipped clip. Timing postoperative angiography between days 5 and 7 after subarachnoid hemorrhage will also show whether vasospasm is present and will occasionally turn up an aneurysm not seen in the initial examination. Intraoperative angiography has a number of problems that are alluded to, but not all that well highlighted, in the article. These include (1) the ready availability of the technology, (2) the reliability of the images and their satisfactory interpretation, (3) the undoubted morbidity from either distal embolisation or arterial dissection, and (4) the technical difficulties associated with heparin infusion and accurate location of digital fluoroscopy in the operating room. For the reasons that I have pointed out, postoperative angiography remains valuable and the article has not implied its elimination from the overall management of the patients. Intraoperative angiography adds cost and morbidity to the patient and it is likely that in the future, MR angiography will replace invasive investigation altogether, thereby eliminating a significant morbidity from the overall management of intracranial aneurysms. Overall, I think this article has demonstrated that intraoperative angiography is a valuable addition to the neurosurgeon s armamentarium for dealing with giant or complex aneurysms. However, it must be performed at a centre with ready availability of appropriate technology and demonstrated low morbidity. The proposed aneurysm grading scale in this regard is rather superfluous as small; straightforward aneurysms can be repaired in the standard manner. Perforator compromise or the so-called slipped clip remain technical problems associated with operative repair of intracranial aneurysms. Michael Besser, MBBS, FRACS Neurosurgeon Westmead, Australia In the present paper, Dr. Origitano and coworkers report their experience with intraoperative angiography in aneurysm surgery. In one-third of their aneurysms, they were able to detect and promptly rectify suboptimal clipping. Thanks to this new technology, they avoided reoperation and prevented possible bleeding from residual sac and/or ischemic injury from vessel stenosis, with significant cost savings. In their hands, the technique proved to be both safe and accurate. Intraoperative verification of adequate clipping in the absence of angiography relies merely on direct inspection. The traditional manoeuvre of sac puncture and opening confirms exclusion, but does not safeguard against aneurysm remnants. The use of ultrathin (1 mm) flexible endoscopes represents a useful adjunct to the operating microscope, allowing a round the corner glance before and after clipping; in this way not only can clip position in relation to the aneurysm neck be checked, but also small perforators can be visualized and spared. Moreover, Doppler examination with microprobes of parent and adjacent vessels helps in the detection and correction of stenosis. At our institution, it is standard practice to perform postoperative angiography, especially when difficulties were encountered at surgery. Compared with our experience (15% remnants, 8% stenosis, 11% both), an incidence of 34% suboptimal clipping is definitely high, even when dealing with large or giant aneurysms. In my opinion, when an aneurysmal remnant is visualized, the decision about reoperation should be made on a case-by-case basis. Besides anatomo-surgical and patient-related variables, other important factors must be taken into consideration: although regrowth and recurrent bleeding are a constant threat, the reported risk of rupture of an aneurysm remnant is as low as 0.8% per year [1], the average interval to rehemorrhage is considerable [3], the chance of spontaneous obliteration of the residuum is not negligible [4], and an endovascular approach may represent a suitable alternative to repeat surgery in some cases of incomplete occlusion [2]. Likewise, all these factors should be considered in the evaluation of the cost-effectiveness of intraoperative angiography. Francesco Chiappetta, M.D. Reparto de Neurochirurgia Ospedale San Camillo Rome, Italy REFERENCES 1. Feuerberg I, Lindquist C, Lindquist M, Steiner L. Natural history of postoperative aneurysm rests. J Neurosurg 1987;66:30 4.

11 Advantages of Intraoperative Angiography Surg Neurol Forsting M, Albert FK, Jansen O, von Kummer R, Aschoff A, Kunze S, Sartor K. Coil placement after clipping: endovascular treatment of incompletely clipped cerebral aneurysms. Report of two cases. J Neurosurg 1996;85: Giannotta SL, Litofsky NS. Reoperative management of intracranial aneurysms. J Neurosurg 1995;83: Sato S, Suzuki J. Prognosis in cases of intracranial aneurysm after incomplete direct operations. Acta Neurochir 1971;24: Origitano et al present a series of 40 patients undergoing intraoperative angiography during aneurysm surgery. There were 52 aneurysms clipped, with a clip adjustment rate of 34%. This was because of parent artery stenosis in four cases, residual aneurysm in eight cases, and both stenosis and residual aneurysm in six cases. The authors do not state whether residual aneurysm refers to a residual neck only or to persistent filling of the aneurysm fundus. This may be an important distinction because we believe the risk of hemorrhage is greater in the latter case. The rate of clip adjustment in this report is high. In a consecutive series of 100 craniotomies for aneurysm, the clip adjustment rate was 11%, restoring flow through major arterial occlusions in 6% and completely obliterating persistently filling aneurysms in 10% [1]. Origitano and colleagues suggest a grading scale to predict cases for which intraoperative angiography may be helpful. Large or giant aneurysms and those of the anterior communicating, middle cerebral, basilar, and ophthalmic arteries were more likely to be incompletely obliterated or to be associated with inadvertent occlusion of a major vessel during clipping. Alexander et al reported that factors predictive of unexpected arterial occlusion were giant aneurysm and basilar apex location [1]. Giant aneurysm and posterior communicating artery location were predictive of unexpected residual aneurysm. Routine use of intraoperative angiography in these subgroups appears warranted, but the aneurysm surgeon should also be prepared to use the technique in any case where there is doubt about the adequacy of clipping or of arterial patency. The technique reported here requires the placement of an angiography catheter in the parent vessel (carotid or vertebral) before surgery; a slow heparin infusion is continued while the catheter is in place. The catheters were in place an average of 345 minutes. Although this technique offers the advantage of catheter placement in the angiography suite, the risk of intraarterial thrombosis is a concern. There was one thromboembolic complication in the current series. We insert the angiography catheter immediately before the intraoperative angiogram. This is made possible by placing the patient on a radiolucent operating table or a wooden extension to a standard table, allowing fluoroscopic imaging of the aorta and cranial vessels. The role of intraoperative angiography is further supported by a cost analysis based on the present series. Part of the analysis was based on an assumed 42% risk of rupture for those aneurysms where clip adjustment was required. This risk may pertain to aneurysms with persistent filling of the fundus, but is probably higher than the risk associated with small residual necks. Nevertheless, the cost analysis demonstrates a clear benefit of intraoperative angiography. Finally, we congratulate the authors on demonstrating that there is no advantage to postoperative angiography if an intraoperative angiogram is performed. Marcus Stoodley, M.D. Bryce Weir, M.D. Section of Neurosurgery University of Chicago Medical Center Chicago, Illinois REFERENCE 1. Alexander TD, Macdonald RL, Weir B, Kowalczuk A. Intraoperative angiography in cerebral aneurysm surgery: a prospective study of 100 craniotomies. Neurosurgery 1996;39:10 8. Dr. Origitano et al are to be commended for their excellent work on intraoperative angiography for intracranial aneurysms. Aneurysms located at anatomical sites with multiple inflow and distal outflow vessels, midline, deep, and ophthalmic lesions had a highly significant association with clip modification. Multivariate analysis confirmed the combination of size and site constituting 83% of the suboptimal clip applications to be highly significant. Intraoperative clip modification was prompted by this method in 34% of 52 aneurysms; the authors conclude that intraoperative angiography allows safe, cost-effective interdiction of improper clip placement leading to complete cure. Although intraoperative angiography would be the best tool to verify optimal clip application during aneurysm surgery, particularly for documentation of unexpected aneurysm remnants, this technology is not available in my practice. My methods for verifying the proper positioning of the clip during aneurysm surgery are: 1. Surgical microscopic examination with a micromirror. I use a micro-mirror, 3 mm in diameter, to visualize the under-surface of the neck of the aneurysm after clip application to detect any

12 128 Surg Neurol Origitano et al remaining aneurysm neck proximal to the clip, and to examine any perforators to ensure that they are not caught in the clip. 2. To confirm the patency of parent vessels, arterial branches, and major perforators, and to verify complete occlusion of cerebral aneurysms, I use a 1 mm, microvascular Doppler probe. I believe that this technique is a safe, instantaneous, effective, reliable, and cost-effective, as noted by Bailes et al [1]. I have used this method with great confidence in about 60 patients who have undergone aneurysm surgery in the last 6 years. However, this method cannot detect residual neck proximal to the clip. One possible difficulty in the use of intraoperative microvascular Doppler sonography would be unsteady application of the flexible probe on the target vessel in the confined space. I solved this problem with the use of a stylet obtained from a ventricular shunting system. A stylet of the ventricular catheter, which was attached to a Doppler probe with tape, made the flexible probe stiff, resulting in steady application. I think this technique is at least comparable to intraoperative angiography. 3. If there is a doubt of complete clipping, I aspirate the fundus of the aneurysm distal to the clip with a fine scalp needle attached to a low-power suction line. 4. Postoperative angiography is performed in selected cases. Although the authors have pointed out that intraoperative angiography cannot resolve perforator sacrifice, I have been utilizing intraoperative microvascular Doppler sonography to prevent unexpected perforator occlusion. I wonder whether a tiny neck remnant of the aneurysm, which may not be seen even on films taken in an angiography suite, would be visualized on intraoperative angiography. Kyu Chang Lee, M.D. Department of Neurosurgery Yonsei University College of Medicine Seoul, Korea REFERENCE 1. Bailes JE, Tantuwaya LS, Fukushima T, Schurman GW, Davis D. Intraoperative microvascular Doppler sonography in aneurysm surgery. Neurosurgery 1997;40: I view intraoperative angiography as a luxury item. I would be delighted to have intraoperative angiography performed on every case. Clearly, there can never be too much information available during complex intracranial neurovascular surgery. I use intraoperative angiography in less than 10% of my cases. I am never happy when the neuroradiologists are in the room; they add a significant amount of extra time to the operative procedure, expose the patient to some increased risk, and their jokes are usually not funny. I also believe that Dr. Origitano et al overestimate the clinical hazards related to small residual remnants of well-clipped aneurysms. I find it inconceivable to believe that a surgeon of Dr. Origitano s skill could ever expect, in his lifetime, to have to reoperate on 20% of his patients due to regrowth or rebleeding of a cerebral aneurysm. Over the last 11 years, I operated on more than 1,000 cerebral aneurysms. I have seen only 3 patients who have bled after previous aneurysm clipping. Two of them were initially clipped by other neurosurgeons without the use of postoperative angiography. The adequacy of the initial clipping remains somewhat suspect. The other case was a man with a 4-cm basilar aneurysm that could not be completely clipped. At least 30% of the aneurysm was known to have been left behind at surgery. I would suspect that the overwhelming vast majority of residual aneurysm necks that are left by experienced aneurysm surgeons without the use of intraoperative angiography represent such a low risk to the patient that the morbidity and mortality of reoperation would significantly exceed the risk of the natural history of the aneurysms if left untreated. In summary, I believe that intraoperative angiography can be useful in a few highly selected patients. The more than 2% stroke rate in Dr. Origitano s series indicates the inherent danger of applying intraoperative angiography to every aneurysm patients. The majority of aneurysm operations can be performed with less than a 2% stroke rate from traditional operative approaches. Doubling of the intraoperative event rate by using intraoperative angiography can hardly be justified. However, a case for intraoperative angiography can certainly be made for large and very complex aneurysms, especially when the possibility of an intraoperative endovascular technique such as temporary balloon occlusion can be helpful. Robert A. Solomon, M.D. Department of Neurological Surgery Columbia University New York, New York