Factors That Predict the Usefulness of Intraoperative Angiography. Intracranial Aneurysm: Anatomic MATERIALS AND METHODS

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1 Cohn P. Derdeyn, MD #{149}Christopher J. Moran, MD #{149}DeWitte T. Cross III, MD Eric W. Sherburn, MD #{149}Ralph G. Dacey, Jr, MD Intracranial Aneurysm: Anatomic Factors That Predict the Usefulness of Intraoperative Angiography PURPOSE: To correlate the size and location of intracranial aneurysm with the need to reposition the aneurysm clip after intraoperative angiography. MATERIALS AND METHODS: In 199 consecutive patients with 234 clipped intracranial aneurysms, 273 intraoperative angiographic studies were retrospectively reviewed. Aneurysm size and location, determined with preoperative angiographic and surgical reports, were correlated with the frequency of clip repositioning because of parent- or branch-vessel compromise or unexpected residual aneurysm. RESULTS: Findings from intraoperalive angiograms resulted in clip repositioning in 46 of 273 (16.8%) studies. Clip repositioning was statistically significantly less frequent with aneurysms of the posterior communicating (three of 52 [5.7%] studies) and anterior choroidal (none of 12 studies) arteries. High rates of clip repositioning were found in aneurysms of the superior hypophyseal artery (seven of 18 [38.9%1 studies), supenor cerebellar artery (three of five [60.0%] studies), and bifurcation of the internal carotid artery (three of nine [33.3%] aneurysms). In 98 conventional follow-up angiographic studies, seven (7%) false-negative cases with unsuspected aneurysm neck remnant were found. CONCLUSION: The rate of clip repositioning in aneurysms of the postenor communicating or anterior choroidal arteries was less than that at other locations (P <.05). Intraoperative angiography may not be necessary when aneurysms are at these two locations. I NTRAOPERATWE angiography after clipping of intracranial aneurysms is an established, useful procedure (1-4). The advantages of intraoperative angiography, compared with those of conventional postoperative studies, are all related to timing. Despite limitations inherent in intraopemative angiography, information gained with this technique can lead to modifications at initial surgery that prevent complications or obviate the need for a second operation. Modifications may involve the adjustment of an aneurysm clip because of parentor branch-vessel compromise or filling of residual aneurysm. The yield (ie, relative frequency of abnormal studies that lead to changes in the surgical approach) of intraoperative angiography, however, is rebatively low. In a recent report (4) of the largest series of which we are aware (100 intraoperative angiographic studies after aneurysm clipping), a 12% frequency of clip repositioning or other changes in therapy due to angiographic findings was reported. This rate of revision is similar to that reported in other series (1-3). The yield of intraopemative angiography could be improved if the technique were performed only in patients in whom an abnormal study was likely to be obtained. The purpose of this study was to determine if such a group of patients could be identified preoperativeby on the basis of aneurysm size and location. Index terms: Aneurysm, intracranial, #{149} Angiography, intraoperative, Radiology 1997; 205: MATERIALS AND METHODS After the clipping of 234 aneurysms in 199 patients between January 1994 and December 1996, 273 consecutive intraoperative angiograms were obtained. Two factors account for the difference between the number of aneurysms and the number of angiographic studies. First, repeated angiographic studies after clip repositioning were considered separately from the initial angiographic results during the same surgical procedure. Second, in patients with multiple clipped aneurysms, each angiogmaphic examination of a treated aneurysm was considered a separate study. This series of patients did not include those who were treated for a dissecting aneurysm (n = 4) or those who underwent emergent intraoperative angiography in the operating room before craniotomy (n = 4). Also not included in this series were patients whose aneurysms were treated with surgical techniques (eg, trapping or proximal ligation) other than clipping of the aneurysm neck. One patient underwent surgical exploration without clipping. During the 3-year study period, six patients underwent craniotomy and surgical clipping without follow-up intraoperative angiography. A 5-F femoral sheath was placed during preoperative diagnostic angiography or while the patient was in the operating room (usually after the administration of anesthesia and before surgery). While not in use, the sheath was continuously flushed with hepaminized saline at arterial pressure. A radiolucent operating table (Skytron, Grand Rapids, Mich) and carbon-fiber head holder (Mayfield radiolucent skull clamp; Ohio Medical, Cincinnati) were used in all patients. The femoral 1 From the Section of Neuroradiolog Mallinckrodt Institute of Radiology (C.P.D., C.J.M., D.T.C.); and the Department of Neurology and Neurosurgery (Neurological Surgery) (E.W.S., R.G.D.), Washington University School of Medicine, Kingshighway Blvd, St Louis, MO ;. Received April 23, 1997; revision requested June 13; revision received June 24; accepted July 8. Address reprint requests to C.P.D. C.P.D. supported by a grant from the RSNA/Siemens Medical Systems Research and Education Fund. C RSNA,

2 sheath was draped to allow access during angiography. Care was taken to avoid placement of radiopaque materials over the patient s head, neck, and chest. The operating room table was positioned to allow space for the bedside angiographic unit. Selective catheter placement of the desired vessel was performed in standard fashion with the 5-F arterial sheath immediately before angiography. Manual injections were performed. Three views of each lesion were routinely obtained, including anterior, lateral, and oblique projections, and attempts were made to duplicate usefiil preoperative views. In many patients, the neurosurgical head-holding device prevented predse duplication ofstandard views. A bedside digital subtraction unit (OEC Diasonics, Salt Lake City Utah) that consisted of a C-arm fluoroscope, a digital image processor and storage unit, and a video monitor was used in all cases. This unit allows performance of routine fluoroscopy and real-time digital subtraction angiography. The recorded images could be reviewed at different speeds and frameby-frame. Permanent hard-copy images were made for the radiologic file with a photographic unit. The preoperative diagnostic studies were available in the operating room for comparison in all cases. All studies were interpreted by the attending neuroradiobogist (C.P.D., C.J.M., D.T.C.), and results were discussed with the neurosurgeon (R.G.D.). The femorab sheath was removed in either the recovery room or the intensive care unit, which allowed routine observation by the nursing staff of the puncture site and lower extremity. The medical records, including surgical and radiographic reports, were reviewed in all patients. Information gathered included (a) information about the intraoperative or postoperative complications possibly attributable to angiography or surgery, (b) the recorded findings of the intraoperative studies, and (c) the sungeon s notes about intraoperative decisions made on the basis of the angiographic results. Preoperative and intraoperative angiograms and surgical reports were reviewed to determine aneurysm size and location. Measured diameters of aneurysms of the anterior circulation were corrected for magnification with the method described by Zubillaga and coworkers (5). With this method, the actual diameter ofthe internal carotid artery proximal to the bifurcation is assumed to be 3.4 mm. A proximal basilar artery diameter of 3.3mm was used in cases of aneurysm of the postenor circulation (5). Aneurysm size was graded as follows: small (diameter < 10 mm), large (diameter, mm), and giant (diameter > 25 mm). Statistical anabysis was performed with the x2 test, with statistically significant differences inferred at the P <.05 level. Aneurysm location was categorized by using established conventions. Internal carotid artery aneurysms were named for the nearest branch vessel of origin (eg, superior hypophyseal artery aneurysms) even if the vessel was not visible on angiograms. At our institution, postoperative angiography is generally reserved for patients Table I Revision of Oip Placement according to Aneurysm Location Frequency of Frequency of No. of No. of Revisions No. of No. of Revisions Arterial Location Studies Revisions (%)* Aneurysms Revisions (%)* All sites (±4.5) (±4.2) Middle cerebral (±10.6) (±10.3) Anterior communicaring (±9.8) (±9.2) Posterior communicating (±6.3)t (±6.6) Ophthalmic (±13.7) (± 13.1) Superior hypophyseal (±22.8)t (±26.5)t Pericallosal (±22.8) (±22.8) Basilar tip (±13.4) (±14.5) Anterior choroidal (±25.0) (±27.3) Bifurcation of internal carotid artery (±24.5) (±30.7)t Superior cerebellar (±42.9) (±53.3)t Posterior inferior cerebellar (±75.0) (±75.0) Posterior cerebral (±53.3) (±53.3) Anterior cerebral (Al segment) (±0.0) Vertebrobasilar junction (±0.0) Anterior inferior cerebellar I (±0.0) * Numbers in parentheses are 95% confidence level t Rate of revision was statically significantly different than the overall rate (P <.05). who do not respond to medical treatment for vasospasm and who are candidates for endovascular treatment. These postoperative studies were reviewed, and findings were correlated with those from the intraoperative study to assess accuracy with intraoperative angiograms. RESULTS Aneurysm clips were repositioned on the basis of intraoperative angiographic findings from 46 of 273 (16.8% ± 4.5 [mean ± 95% confidence level]) studies of 234 aneurysms (Table 1). The repositioning rate per aneurysm was lower (30 of 234 [12.8% ± 4.2] aneurysms) than the 16.8% rate per angiographic study. The 46 intraoperative angiograms with findings that bed to revision of clip placement were penformed in 30 cases of aneurysm. Two on more revisions were necessary in 10 of these 30 aneurysms. Findings from an initial study that bed to clip repositioning were, therefore, associated with a statistically significantly higher nate of subsequent revision of clip placement (10 of 30 [33.3% ± 16.9] aneurysms). The frequency of clip repositioning was statistically significantly higher than average for aneurysms in the superior hypophyseal and superior cemebelbar arteries. The frequency of clip repositioning was statistically significantly higher for aneurysms at the bifurcation of the internal carotid amtemy compared with the frequency for all clipped aneurysms, but not when the number of studies performed was considered. High rates of clip reposihoning that did not reach statistical significance were also seen for aneumysms in the middle cerebral artery and pericallosal artery. The rate of clip repositioning was also statistically significantly more frequent for large aneurysms (Table 2). The mate of clip repositioning was statistically significantly lower than average for aneurysms in the postenon communicating artery and in the anterior choroidal artery. If these two similar and adjacent locations along the posterior wall of the supraclinoid internal carotid artery proximal to the bifurcation are considered together, the revision rate was even smaller (three of 64 [4.7% ± 5.1%] angiograms and three of 60 [4.8% ± 5.3%] aneurysms) and achieved statistical significance for all aneurysms, as well as for total studies. The reasons for clip repositioning could be grouped into two categories: (a) parent- or branch-vessel compromise and (b) residual aneurysm. The category of residual aneurysm encompassed three situations: persistent filling of the sac, filling of a neck remnant, or filling of an uncipped adjacent lobe or of a second aneurysm. The relative frequency of these two findings 336 Radiology November 1997

3 .4 a. Table 2 Revision of Clip Placement according to Aneurysm Size No. of No. of Frequency of No. of No. of Frequency of Size Studies Revisions Revisions (%)* Aneurysms Revisions Revisions (%)* All sizes (±4.5) (±4.2) Small (±4.6) (±4.2) Large (±20.1)t (±19.8)t Giant (±29.8) (±35.1) * Numbers in parentheses are 95% confidence level. t Rate of revision was statistically significantly different than the overall rate (P <.05). Table 3 Reasons for Revision of Clip Placement according to Aneurysm Location Vessel Residual Vessel Residual No. of Compromise Aneurysm No. of Compromise Aneurysm Arterial Location Studies (%) (%) Aneurysms (%) (%) Allsites Middlecerebral Anterior communicating Posterior communicating Ophthalmic Superior hypophyseal Pericallosal Superior cerebellar Basilartip Bifurcation of the internal carotid Posterior cerebral Figure 1. Unexpected filling of residual aneurysm at the superior hypophyseal artery after initial clip placement. (a) Oblique lateral intraoperative angiogram demonstrates residual filling of the aneurysm sac (arrow). On the basis of this information, the jaws of the aneurysm clip we re opened, and the clip was extended anteriorly. A subtraction artifact (arrowhead) of the fenestrated aneurysm clip overlies the supraclinoid carotid artery. (b) Same view from the repeated intraoperative angiogram demonstrates no filling of the aneurysm and no compromise of internal carotid artery flow. Arrowhead = subtraction artifact due to the presence of the clip. for each aneurysm location is shown in Table 3. For internal carotid artery aneurysms above the dunal ring but proximal to the bifurcation, all repositionings were undertaken because of residual aneurysm. At the superior hypophyseal location, three of 11 aneurysms continued to fill after initial clipping (Fig 1). In two of these three b. aneurysms, multiple surgical adjustments were needed to exclude the aneurysm from the circulation. All antenor communicating artery aneurysms that needed clip revision were for mesidual aneurysm, as well. At the tnfurcation of the middle cerebral artery, most revisions were necessary to improve parent-or branch-vessel flow (abnormal findings from 11 of 14 intraopenative angiogmams led to repositioning) (Fig 2). p Conventional angiography was penformed in 98 of the 234 cases of clipped aneurysms. Unexpected residual aneurysm was noted in seven (7% false-negative rate) cases. One of the seven falsenegative studies is shown in Figure 3. No unexpected parent- or branch-vessel compromise was seen. No complications were observed after intraoperative angiography. DISCUSSION The goal of surgery in cases of aneurysm is to exclude the aneurysm from the circulatory system without compromising flow through parent or branch vessels. The frequency of incomplete aneurysm obliteration is not known. Feuerberg et al (6) found mesidual aneurysm in one of 27 (4%) treated intracranial aneurysms. Clipped aneurysms with small (1-2 mm in length) neck remnants have been shown to enlarge and bleed (6-8). Branch-vessel occlusion caused by an aneurysm clip may also complicate surgery. After the clipping of 78 consecutive aneurysms, MacDonald et al (9) reported nine unexpected majorvessel occlusions on postoperative angiognams obtained urgently or routinely. Six of these occlusions resulted in disability due to infarct. In addition, residual aneurysm was seen in six patients. Three of these six patients with residual aneurysm underwent repeated surgery. The frequency of these undesired events was 19.2% (15 of 78 aneurysms)and was similar to the rate of clip repositioning observed in our large series and to that reported by other investigators (1-4). The data from our investigation suggest that certain aneurysm bocations and sizes are associated with particular rates of clip replacement after intraopenative angiognaphy. A low rate of clip repositioning after intnaopenative angiography was observed with aneurysms at the relalively easily exposed and well-visualized supraclinoid segment of the internal carotid artery. A change in clip placement was not necessary in any of the 12 aneurysms of the anterior choroidal artery. Revision of clip placement was necessary in only three of the 50 aneurysms of the posterior communicating artery. These findings contrast with those of Alexander et al (4). In their study of 100 craniotomies, clip repositioning was necessary in five of 27 aneurysms of the posterior communicating artery. Not all patients in their series, however, underwent intmaoperative angiography; among patients who did not undergo intraoperative angiognaphy were six patients Volume 205 #{149} Number 2 Radiology #{149} 337

4 with aneurysms of the posterior communicating artery. High frequencies of unexpected residual aneurysm that necessitated clip manipulation were observed at the superior hypophyseal artery, at the bifurcation of the internal carotid antery, and at the superior cerebellar artery. Aneurysms arising from the superior hypophyseal artery can be difficult to risualize; these aneurysms are close to the cavernous sinus and the relatively fixed position of the internal carotid artery at the durab ring, which makes exposure of the aneurysm neck challenging. All revisions of clip placement in aneurysms of the superior hypophyseal artery were performed for residual filling of the aneurysm sac (Fig 1). Adequate exposure of aneurysms of the superior cerebellan artery and of the bifurcation of the internal carotid artery may also be difficult. Parent- or branch-vessel compromise was a frequent finding after clipping of aneurysms of the middle cerebral artery. Aneurysms at this location often involve origins of branch vessels, and complete obliteration of the aneurysm may be difficult without compromising parent- on branch-yessel flow. Large aneurysms were associated with higher rates of clip repositioning. This finding is not surprising because visualization of parent and branch vessels can be more difficult with larger aneurysms. Giant aneurysms were not associated with high rates of revision, but only six of these lesions were included in this series. Alexander et al (4) found a statistically significantly higher frequency of clip repositioning in the 11 giant aneurysms they studied. No complications attributable to intraoperative angiography were encountered in this retrospective review. Derdeyn et ab (3) noted one possible embolic complication in 87 transfemoral catheter placements at intraoperative angiography. Alexander et al (4) reported one possible embolic complication in 100 transfemoral studies. The working conditions in the operating room are different from those in the angiography suite, and the apparent improvement in the complication rate of Alexander et al may reflect the benefit of experience. The resolution on intraoperative angiograms is not as high as that on conventional angiograms. Small yessels such as the anterior choroidab antery and perforating vessels often are not visualized on intraoperative angiograms. In addition, the head holder can limit the angles at which angio- a. Figure 2. Unexpected branch-vessel occlusion after clipping of a complex aneurysm of the middle cerebral artery. (a) Anteropostenor preoperative angiogram of the right internal carotid artery shows a large, lobulated aneurysm (arrow) at the trifurcation. An intracerebral hematoma was present with mass effect. Narrowing of the Ml and Al segments of the proximal middle cerebral and anterior cerebral arteries was consistent with vasospasm. (b) Oblique anteroposterior initial intraoperative angiogram obtained after clipping demonstrates no filling of the aneurysm or of the previously visualized branches of the middle cerebral artery. Arrow = subtraction artifact due to the presence of the aneurysm clip. (c) Angiogram acquired after the clip was repositioned shows restoration of flow to the branch. Of necessity, the residual aneurysm (arrow) was left in place. graphic projections are obtained. Conyentional angiography in a dedicated angiography suite offers biplane capability, which doubles the number of views obtained with each injection and provides higher resolution and greaten flexibility with regard to projections. Despite the limitations of intraoperative angiography, however, diagnostic information regarding parent- and branch-vessel patency and the status of the clipped aneurysm is usually obtained. The radiologist performing these studies must be thoroughly familiar with the preoperative cerebral angiogmam to ensure that intraoperative images will optimally provide clinically relevant infonmation. An unexpected residual aneurysm neck was identified on seven of the 98 (7()/()) postoperative angiognams in this series; note that no vessel occlusions were found. In general, the false-negative results obtained in cases of small r b.,1 C. I 4 I... - neck remnants were often attributable to limited resolution and limited availability of angiographic projections with the current intraopenative angiogmaphic equipment (Fig 3). The actual rate of false-negative findings from intraopemative angiography in cases of an unsuspected residual aneurysm cannot be determined from our data because only those patients suspected of having vasospasm Undenwent conventional angiography after surgery. Our 7% nate is similar to that found in other studies of this technique. Martin et al (1) noted three false-negative intraopemative studies in their series with angiognaphic foblow-up in 62 patients. Two residual aneurysm sacs were overlooked, and a small residual nidus of an anteniovenous malformation was overlooked in a third case. In the series of Barrow et al (2), one residual aneurysm sac was noted in 17 postoperative studies after aneurysm clipping. With subsequent angiography, Derdeyn et al (3) observed two unexpected, small residual aneurysms (false-negative studies) on 25 studies of aneurysms. While intraopenative angiogmaphy cleanly offers several advantages in,. 338 Radiology November 1997

5 a. b. C. t_. choroidal arteries is low, and intraopenative angiognaphy may not be necessary, in these cases. #{149} I Jfr. d. e. Figure 3. False-negative intraoperative angiogram. (a) Preoperative angiogram shows a large internal carotid artery aneurysm at the ophthalmic level. (b) On the anteroposterior intraoperative angiogram, no definite residual aneurysm filling is depicted, and the study was considered to he normal. (c) A similar view from the postoperative angiogram shows definite residual lateral filling (arrow) of the aneurysm beneath the clips. (d) Findings on the lateral intraoperative angiogram are unremarkable and are similar those on (e) the postoperative lateral angiogram. the surgical treatment of aneurysms, this procedure also has some limitations. First, intraoperative angiography necessitates more operating-room time (average of 45 minutes [3]) and consequently increases cost. Second, intraoperative angiography is associated with a small risk of angiographic complications. Third, intraoperative angiographic equipment does not pro- ide the resolution available with equipment in modem angiography suites. The magnitude of the rate of false-negative intraopenative angiograms in cases of aneurysm neck remnant and the subsequent effect of this rate on outcome are unknown. Finally, the information gained with intnaopenative angiognaphy may not result in improved outcome. For example, despite identification of an abnormality such as branch-vessel occlusion and rapid surgical correction, an infarct may still occur (3). The data from this study demonstrate that different aneurysm diameters and locations are associated with different rates of clip repositioning after intraoperative angiogmaphy. The yield of intraoperative angiognaphy is high in cases of large aneurysms and of aneurysms of the superior hypophyseal artery, superior cerebellan artery, and bifurcation of the internal carotid artery. The need for intraopenative angiography should be anticipated in these situations. The rate of clip repositioning in aneurysms of the posterior communicating and anterior References D Martin NA, Bentson J, Vinucla F, et al. Intraoperative digital subtraction angiography and the surgical treatment of intracranial aneurysms and vascular malformations. J Ne urosurg 1990; 73: Barrow DL, Boyer KL, Joseph GJ. lntraoperative angiography in the management of neurovascular disorders. Neurosurgery, 1992; 30: /. 3. Derdeyn CP. Moran CJ, Cross DT, Grubb RL, Dacey RG. lntraoperative digital subtraction angiography: a review of 112 consecutive cxaminations. AJNR 1995; 16: Alexander TD, Macdonald RL, Weir B, Kowalczuk A. Intraoperative angiography in aneurysm surgery: a prospective study of 100 craniotomies. Neurosurgery 1996; 39: Zubillaga AF, Guglielmi G, Vinuela F, Duckwiler GR. Endovascular occlusion of intracranial aneurysms with electrically detachable coils: correlation of aneurysm neck size and treatment results. AJNR 1994; 15: Feuerberg I, Lindquist C, Lindqvist M, Steiner L. Natural history of postoperative aneurysm rests. J Neurosurg 1987; 66: Drake CG, Vanderlinden RG. The late consequences of incomplete surgical treatment of cerebral aneurysms. J Neurosurg 1967; 27: Lin T, Fox AJ, Drake CG. Regrowth of aneurysm sacs from residual neck following aneurysm clipping. J Neurosurg 1989; 70: MacDonald R, Wallace M, Kestle J. Role of angiography following aneurysm surgery. Neurosurg 1993; 79: Volume 205 #{149} Number 2 Radiology #{149} 339