Dandy (3) pioneered aneurysm surgery ROUTINE CEREBRAL ANGIOGRAPHY AFTER SURGERY FOR SACCULAR ANEURYSMS: IS IT WORTH IT?

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1 CLINICAL STUDIES ROUTINE CEREBRAL ANGIOGRAPHY AFTER SURGERY FOR SACCULAR ANEURYSMS: IS IT WORTH IT? Riku P. Kivisaari, M.D. Hospital, Helsinki, Finland Matti Porras, M.D., Ph.D. Department of Diagnostic Radiology, Helsinki University Central Hospital, Helsinki, Finland Juha Öhman, M.D., Ph.D. Hospital, Helsinki, Finland Jari Siironen, M.D., Ph.D. Hospital, Helsinki, Finland Keisuke Ishii, M.D., Ph.D. Hospital, Helsinki, Finland Juha Hernesniemi, M.D., Ph.D. Hospital, Helsinki, Finland Reprint requests: Riku Kivisaari, M.D., Hospital, Topeliuksenkatu 5, Helsinki, Finland. Received, January 7, Accepted, May 6, OBJECTIVE: The objective of this study was to determine whether an angiographically proven rate of saccular intracranial aneurysm occlusion after surgical clipping suggests that postoperative angiography should continue to be used routinely or should be supplanted by intraoperative angiography. These data also should establish a basis for comparing surgery with new endovascular methods of treatment. METHODS: During a 3.5-year period, a consecutive series of 622 patients (955 aneurysms, 808 of which were surgically clipped) who underwent postoperative angiography were studied retrospectively. This series comprised 493 ruptured and 315 unruptured aneurysms. RESULTS: Complete aneurysm closure was achieved in 88% of aneurysms, a neck remnant was discovered in 9%, and a fundus remnant was revealed in 3%. Of 493 ruptured aneurysms, 86% were completely occluded. Of 315 unruptured aneurysms, 91% were completely occluded. The results for clipping of complex aneurysms, i.e., posterior circulation or large to giant aneurysms, were significantly inferior to those for small and anterior circulation aneurysms. In one-third of the large and giant aneurysms, a part of the base was left intentionally because of calcifications or strong wall or to prevent occlusion of any branches. In the series, a significant 5% complication rate of major vessel occlusion was detected. CONCLUSION: Our retrospective analysis revealed that ruptured, posterior circulation, and large/giant aneurysms are more prone to incomplete clipping. Therefore, these aneurysms require postoperative if not intraoperative evaluation with angiography. Many clippings of anterior circulation aneurysms experience unexpected failures, which suggests that intraoperative angiography could be beneficial. This series, which has no selection bias, can be used as a basis to compare the results of other series reporting surgical or endovascular treatment. KEY WORDS: Angiography, Intracranial aneurysm, Subarachnoid hemorrhage, Surgery Neurosurgery 55: , 2004 DOI: /01.NEU Dandy (3) pioneered aneurysm surgery by clipping the base of the aneurysm, and Yaşargil (32) introduced the systemic use of microsurgery to cure these fatal sacs. When an aneurysm is clipped, the base of the aneurysm is closed, and the walls are apposed for a continuous endothelial lining. If the clip is perfectly positioned, this completely occludes the aneurysm and leaves the parent vessels intact. The complete closure of the base of an intracranial aneurysm is crucial for the prevention of rebleeding of a ruptured aneurysm or the subsequent growth and rupture of an unruptured aneurysm (4, 9, 12, 14, 15, 26). During the past 10 years, endovascular therapy with coils has been used increasingly to occlude aneurysms (21, 31). In experienced hands, aneurysms can be clipped or coiled with low morbidity and mortality rates and a high short-term success rate (7, 10, 12, 31, 32). At many centers, control angiograms are seldom performed. The difficulty in predicting the presence of a residual or unclipped aneurysm suggests that all patients should undergo intra- or postoperative catheter angiography, even if the aneurysm is opened and/or coagulated, which is how we regularly handle aneurysms after clipping (1, 19, 24, 30). Angiography is a reliable method to evaluate the completeness of the closure of an aneurysm, NEUROSURGERY VOLUME 55 NUMBER 5 NOVEMBER

2 KIVISAARI ET AL. but it is not completely without complications, especially in elderly patients or if performed by less-experienced practitioners (1, 22, 30). We conducted this study because of the high incidence (16 20 per 100,000 persons per year) of subarachnoid hemorrhage (SAH) in Finland (9, 11, 27, 28), our defined catchment area comprising 2 million people. As our institution is the only neurosurgical center, there is no referral bias, and we have extensive experience with more than 10,000 patients with cerebral aneurysms. Until recently, routine intra-arterial angiography was performed during the early postoperative period for all patients who underwent aneurysm clipping at our institution; subsequently, computed tomographic angiography replaced digital subtraction angiography (DSA). As many neurosurgical centers do not perform postoperative controls, we analyzed the completeness of the closure of intracranial aneurysms treated by experienced surgeons. This analysis also should establish a basis for comparing surgery with endovascular therapy and the results of intraoperative angiography. PATIENTS AND METHODS Patients Helsinki is the only neurosurgical unit serving a population of 2 million in Southern Finland. There are no admission biases, because all of the patients, including those in poor condition or moribund, are admitted. Of 932 patients with SAH or an unruptured saccular intracerebral aneurysm treated at our hospital between August 1, 1998, and December 31, 2001, a consecutive series of 622 patients (41% men, 59% women; age range, yr) was studied retrospectively. Excluded were 32 patients with fusiform aneurysm, 103 patients who had nonaneurysmal SAH, and 44 patients who underwent endovascular treatment or surgery other than clipping (e.g., trapping or bypass). In addition, 77 patients with no control digital subtraction angiogram were excluded. The reasons for not performing control DSA included severe calcifications at the aortic arch and its branches, a complication in obtaining the diagnostic digital subtraction angiogram, or perfect visualization of the anatomy at operation. All patients with saccular aneurysm were treated, with the exception of 54 moribund or rapidly deteriorating or extremely old ( 85 yr) patients. Patients with large hematomas also were treated. The aneurysms were operated on by 12 surgeons; the senior author (JH) performed most of the aneurysm operations (68%). The 622 patients presented with 955 aneurysms. Of these, 808 aneurysms were clipped, and the results were monitored postoperatively by angiography. A total of 121 patients (19%) had no history of SAH, i.e., they had incidental aneurysms. A total of 493 of the aneurysms (61%) were ruptured causing SAH; 315 (39%) of the 808 aneurysms were unruptured. The demographic features of the patients with SAH are listed in Table 1, and those of the patients without SAH are listed in Table 2. TABLE 1. Patients with subarachnoid hemorrhage operated on for ruptured aneurysms a Clinical characteristics No. of patients (%) Sex Male 210 (43%) Female 283 (57%) Age (yr) Average 53 Range Patients with multiple aneurysms 152 (31%) WFNS grade (42%) 2 89 (18%) 3 27 (5%) 4 84 (17%) 5 85 (17%) Aneurysm location ICA 98 (20%) MCA 143 (29%) AComA 174 (35%) Peric 31 (6%) VBA 47 (10%) Aneurysm size Small ( 7 mm) 218 (44%) Medium (7 14 mm) 238 (48%) Large (15 24 mm) 20 (4%) Giant ( 24 mm) 4 (1%) NA 13 (3%) Timing of surgery 24 h 288 (58%) 72 h 400 (81%) 3 10 d 63 (13%) 10 d 30 (6%) GOS score (at 3 mo) GR 229 (46%) MD 100 (20%) SD 94 (19%) VS 20 (4%) Dead 50 (10%) a WFNS, World Federation of Neurosurgical Societies scale (2); ICA, internal carotid artery; MCA, middle cerebral artery; AComA, anterior communicating artery; Peric, pericallosal artery; VBA, vertebrobasilar arteries; NA, not available; GOS, Glasgow Outcome Scale (13); GR, good recovery; MD, moderate disability; SD, severe disability; VS, vegetative state VOLUME 55 NUMBER 5 NOVEMBER

3 CEREBRAL ANGIOGRAPHY AFTER SURGERY FOR SACCULAR ANEURYSMS TABLE 2. Patients without subarachnoid hemorrhage operated on for unruptured aneurysms a Clinical characteristics No. of patients Sex Male 81 (36%) Female 141 (64%) Total 222 (100%) Incidental 121 Age (yr) Average 52 Range Multiple aneurysms 144 (65%) Aneurysm location ICA 64 (20%) MCA 163 (51%) AComA 44 (14%) Peric 14 (4%) VBA 30 (9%) Total 315 (100%) Aneurysm size Small ( 7 mm) 215 (68%) Medium (7 14 mm) 78 (25%) Large (15 24 mm) 8 (3%) Giant ( 24 mm) 7 (2%) NA 7 (2%) Total 315 (100%) GOS score (incidental at 3 mo) GR 98 (81%) MD 13 (11%) SD 7 (6%) VS 1 (1%) Dead 2 (2%) Total 121 (100%) of any major artery or branch or perforator. The closure of the aneurysm was considered incomplete if even a small neck remnant ( 1 mm) or fundus of the aneurysm was reliably visible (Figs. 1 3). Incomplete closures were divided into two categories: 1) neck remnant only; and 2) residual filling of the fundus of the aneurysm. The size of the aneurysm was approximated in millimeters by comparison with the intracavernous part of the internal carotid artery (5 mm) and the middle part of the basilar artery (3 mm). RESULTS FIGURE 1. Digital subtraction angiograms of a 58-year-old man. A, ruptured aneurysm of the basilar artery, World Federation of Neurosurgical Societies Grade 1. The patient underwent surgery on Day 2. B, to save a small perforator, a small neck remnant was left at operation. The patient died secondary to rebleeding 10 days after the operation. Complete closure of aneurysm was achieved in 711 (88%) of the 808 aneurysms (Table 3). Approximately two-thirds (59) of the 97 incomplete closures were unexpected, and one-third (38) of the incomplete closures were planned to save a major vessel, because of calcifications, or owing to a thick aneurysm wall. The frequency of unexpected incom- a ICA, internal carotid artery; MCA, middle cerebral artery; AComA, anterior communicating artery; Peric, pericallosal artery; VBA, vertebrobasilar arteries; NA, not available; GOS, Glasgow Outcome Scale (13); GR, good recovery; MD, moderate disability; SD, severe disability; VS, vegetative state. Angiography Patients were assessed preoperatively by use of computed tomographic angiography or catheter DSA; both carotid arteries and at least one vertebral artery were assessed. Postoperative DSA was performed with an Integris V3000 ( matrix; Philips Medical Systems, Best, The Netherlands), within 24 hours after the operation. At least four different projections per vessel were obtained. All angiographic studies were analyzed by an experienced neuroradiologist (MP) who has assessed nearly 10,000 intracranial aneurysms. The analysis focused on: 1) the completeness of the closure of the aneurysm; and 2) the occlusion FIGURE 2. Computed tomographic (A) and digital subtraction (B) angiograms of a 57-year-old woman. A, unruptured giant aneurysm of the left middle cerebral artery bifurcation. Only part of the aneurysm is filled with contrast medium. Immediately after the operation, the patient experienced slight hemiparesis, which subsided. B, complete closure of the aneurysm. NEUROSURGERY VOLUME 55 NUMBER 5 NOVEMBER

4 KIVISAARI ET AL. FIGURE 3. Digital subtraction angiograms of a 43-year-old man. A, ruptured aneurysm of the anterior communicating artery and unruptured aneurysm of the right middle cerebral artery bifurcation, World Federation of Neurosurgical Societies Grade 1. The patient underwent surgery on Day 2. B, control digital subtraction angiogram showing the fundus of the middle cerebral artery bifurcation aneurysm still filling. The aneurysm of the anterior communicating artery is completely unclipped. The aneurysm sacs were not resected and coagulated, as is now our standard method. C, after reoperation, the middle cerebral artery bifurcation aneurysm is completely occluded, but part of the aneurysm sac of the anterior communicating artery aneurysm remains unclipped (arrow). plete closure was extremely high at the following locations: anterior communicating artery (84% of all incomplete closures were unexpected), internal carotid artery (73% of all incomplete closures were unexpected), and pericallosal arteries (71% of all incomplete closures were unexpected) (Table 4). Of the 493 ruptured aneurysms, 424 (86%) were completely occluded, and 46 of the 69 incomplete closures were unexpected. Of the 94 unruptured aneurysms that were operated on during the same operation with a ruptured aneurysm, 83 (88%) were completely occluded, and 6 of the 11 incomplete closures were unexpected. A total of 221 unruptured aneurysms were in patients without SAH or after a 2- to 3-month recovery period after SAH. Of the 221 aneurysms, 204 (92%) were completely occluded, and 7 of the 17 incomplete closures were unexpected. Overall, there were 315 unruptured aneurysms, of which 287 (91%) were completely occluded. The difference in the number of completely closed aneurysms between ruptured and all unruptured aneurysms is significant (P 0.003, 2 test) (Table 3). Neither the World Federation of Neurosurgical Societies grade (2) at admission of the patients with SAH or the timing of surgery influenced the success rate of complete closure (Table 5). The closure percentage (expected and unexpected) of the ruptured vertebrobasilar aneurysms (74%) was significantly lower than that of ruptured middle cerebral, carotid, or anterior communicating artery aneurysms. In addition, the closure percentage of the ruptured aneurysms of the middle cerebral artery (92%) was significantly higher than that of ruptured pericallosal or anterior communicating artery aneurysms, whereas other differences were not statistically significant. The unruptured vertebrobasilar aneurysms also were significantly less often completely secured (77%) than the unruptured aneurysms of the carotid (97%) and middle cerebral arteries (92%) (Table 6). The size of the aneurysm had a significant impact on closure rate (Table 6). Of the 20 large (15 24mm) ruptured aneurysms, only 12 (60%) were completely occluded, whereas 92% of the small (2 7 mm) and 84% of the medium-size (8 14 mm) unruptured aneurysms were completely occluded. Of the unruptured aneurysms, 95% of small aneurysms were completely occluded, whereas only 85% of medium, 50% of large, and 57% of giant aneurysms were completely occluded. Twentyfour (41%) of the 59 aneurysms with unexpected incomplete closure were reoperated, and 7 (12%) were treated with endovascular coiling (Fig. 4). After these treatments, four aneurysms still had neck remnants. There were 44 major vessel (or branch of major vessel) occlusions; 32 of these were unexpected. Furthermore, the frequency of unexpected major vessel occlusion was high at these locations: internal carotid artery (75%), middle cerebral artery (79%), and pericallosal arteries (83%) (Table 7). Major vessel occlusion led to reoperation in 14 patients. Two occlusions were treated with extracranial-intracranial bypass operations. In 12 occlusions, repositioning of the aneurysm clip was performed, and good angiographic results were achieved in 9 patients. Overall, control DSA lead to reoperation or coiling in 45 patients. A flowchart illustrating excluded patients and the major results of control DSA are shown in Figure 4. Despite the far greater number of large, giant, and posterior circulation aneurysms, there were fewer fundus remnants in the aneurysms operated on by the senior author (JH), with an experience of more than 2500 aneurysms treated, as compared with a group of 11 other surgeons (2.4% versus 6.1%; P ). The same comparison of neck remnants was 10.1% versus 11.7% (not significant), as giant and posterior circulation aneurysms were operated on by the senior author. Outcomes at 3 months are listed in Table 8. DISCUSSION An incompletely treated aneurysm may regrow and lead to recurrent symptoms of hemorrhage or mass effect. The rebleeding rate of aneurysms with residual necks is between 3.5 and 28%, (5 8, 12). In long-term follow-up of patients with extremely complex aneurysms as reported by Drake et al. (7), the rebleeding rate was 10%. Aneurysm regrowth has been reported to occur in 3.5 to 15% of patients (6 8). The high rebleeding rate over the long term (10 20 yr) emphasizes the importance of perfect clipping. However, aneurysms treated with perfect clip placement also may rupture or regrow with 1018 VOLUME 55 NUMBER 5 NOVEMBER

5 CEREBRAL ANGIOGRAPHY AFTER SURGERY FOR SACCULAR ANEURYSMS TABLE 3. Results of control angiograms Total closure (%) Neck remnant (%) Neck and fundus remnant (%) Major vessel occlusion (%) Total no. of aneurysms Ruptured 424 (86%) 52 (11%) 17 (3%) 30 (6%) 493 Unruptured 287 (91%) 17 (5%) 11 (3%) 14 (4%) 315 Total no. of aneurysms 711 (88%) 69 (9%) 28 (3%) 44 (5%) 808 TABLE 4. Expected and unexpected incomplete closures in control angiograms a No. (%) of incomplete closures Expected Unexpected Aneurysm location ICA 4 (27%) 11 (73%) MCA 14 (58%) 10 (42%) AComA 5 (16%) 26 (84%) Peric 2 (29%) 5 (71%) VBA 13 (65%) 7 (35%) Total 38 (39%) 59 (61%) Size of aneurysm Small ( 7 mm) 6 (21%) 22 (79%) Medium (7 14 mm) 18 (36%) 32 (64%) Large (15 24 mm) 8 (62%) 5 (38%) Giant ( 24 mm) 4 (100%) 0 (0%) NA 2 (100%) 0 (0%) Total 38 (39%) 59 (61%) a ICA, internal carotid artery; MCA, middle cerebral artery; AComA, anterior communicating artery; Peric, pericallosal artery; VBA, vertebrobasilar arteries; NA, not available. mass effect (6); this is also our long-term experience in Finland. Depending on definitions and the use of control angiograms, the reported incidence of residual neck after surgical clipping of an aneurysm ranges from 3.8 to 18% (5, 7, 8, 12, 21, 23, 24, 29, 31, 32). Despite our extensive experience, our overall results of 12% incomplete closures and 7.4% unexpected incomplete closures are within this wide range. This might be attributable to nonselection of patients for surgery but also to our strict criteria of the small neck remnants that might be considered successful surgical results in some other series. In our study, even the slightest dog ear was considered a neck remnant. Such neck remnants may not be recognized on routine control angiograms or considered as failures in other series. Furthermore, postoperative control angiography is not routinely performed in many institutions, and many surprises with partially ligated or filling aneurysms or occluded vessels remain hidden even in the most experienced neurosurgical TABLE 5. World Federation of Neurosurgical Societies grade, timing of surgery, and complete closures on control angiograms a Complete closure (%) WFNS grade (86%) 2 82 (92%) 3 23 (85%) 4 68 (81%) 5 73 (86%) Total 424 (86%) Timing of surgery 72 h 347 (87%) 3 10 d 54 (86%) 10 d 23 (77%) Total 424 (86%) a WFNS, World Federation of Neurosurgical Societies (2). hands. The few institutions that have presented excellent postoperative morphological results may not represent the average results achieved by surgery, or the criteria for aneurysm remnants are different. However, in the series by Drake et al. (7) (Drake and Peerless have a total surgical experience of 5000 aneurysm operations) of 1767 vertebrobasilar aneurysms, total obliteration was achieved in only 82.5% of aneurysms. This result is biased by the extremely difficult aneurysms in relation to site and size that were treated. In addition, in our study, the frequency of unexpected incomplete closure was extremely high at the location of the anterior communicating artery (84% unexpected of all incomplete closures), internal carotid artery (73% unexpected of all incomplete closures), and pericallosal arteries (71% unexpected of all incomplete closures). Specifically, the high frequency of unexpected closure of the anterior communicating artery was surprising. This must depend on its complicated and difficult vascular anatomy. In clipping aneurysms at these locations, intraoperative angiography may be required in addition to careful handling. In a study of timing of operation, Kassell et al. (17) reported increased tightness of the brain at early surgery. It was surprising that this finding did not result in more difficult dissection of the aneurysm. Accordingly, in our study, the timing of surgery did NEUROSURGERY VOLUME 55 NUMBER 5 NOVEMBER

6 KIVISAARI ET AL. TABLE 6. Aneurysm location and size and complete closures on control angiograms a Location and size Complete closure (%) Aneurysm location ICA 147 (91%) MCA 282 (92%) AComA 187 (86%) Peric 38 (84%) VBA 57 (74%) Total 711 (88%) Size of aneurysm Small ( 7 mm) 405 (94%) Medium (7 14 mm) 266 (84%) Large (15 24 mm) 15 (54%) Giant ( 24 mm) 7 (64%) NA 18 Total 711 (88%) a ICA, internal carotid artery; MCA, middle cerebral artery; AComA, anterior communicating artery; Peric, pericallosal artery; VBA, vertebrobasilar arteries; NA, not available. TABLE 7. Unexpected major vessel occlusions on control angiograms a No. (%) of major vessel occlusions Expected Unexpected Aneurysm location ICA 3 (25%) 9 (75%) MCA 3 (21%) 11 (79%) AComA 2 (40%) 3 (60%) Peric 1 (17%) 5 (83%) VBA 3 (43%) 4 (57%) Total 12 (27%) 32 (73%) Size of aneurysm Small ( 7 mm) 3 (17%) 15 (83%) Medium (7 14 mm) 3 (16%) 16 (84%) Large (15 24 mm) 2 (67%) 1 (33%) Giant ( 24 mm) 4 (100%) 0 (0%) Total 12 (27%) 32 (73%) a ICA, internal carotid artery; MCA, middle cerebral artery; AComA, anterior communicating artery; Peric, pericallosal artery; VBA, vertebrobasilar arteries. FIGURE 4. Flowchart summarizing the included and excluded patients, DSA results, and treatment after DSA. not affect the number of incomplete closures despite the tight conditions caused by the red and swollen brain tissue at early surgery. The most important thing in acute and early aneurysm surgery is to achieve a slack brain before beginning to clip the aneurysm(s). This can be achieved by anesthesiological means and especially by opening of the lamina terminals or frontal ventriculostomy. These maneuvers markedly reduce the need of retraction, which results in brain contusion and damage when use of brain spatulas is necessary (18). The difference of occlusion rate between unruptured and ruptured aneurysms is significant, and it might be explained by the bold dissection of unruptured aneurysms and smaller aneurysm size. In previous studies, the incidence of aneurysm neck remnants after surgery is relatively rare in the anterior circulation and in small aneurysms and much higher in the posterior circulation and midline, large, or giant aneurysms (5, 7, 29). In our study, the incidence of aneurysm neck remnants in posterior circulation aneurysms hidden deep in small gaps was significantly higher than in middle cerebral artery aneurysms, which are the most common aneurysms in Finnish series. Large aneurysms were more often left with residual neck, often intentionally so as not to occlude any branches. The reported high rates of unexpected major vessel occlusions, which also were observed in our series, harbor a great risk for the patient; many occur without symptoms, and they occur in the very best hands (7, 12, 16, 24). Those who do not obtain control angiograms do not observe the unexpected findings. At surgery, it is often difficult to predict the presence of residual aneurysm or major vessel occlusion (24). Use of mini-doppler ultrasonography has improved the situation, but many vessels are too distal to be visualized. The good results of intraoperative angiography in prevention of vessel occlusions and residual aneurysms have been well docu VOLUME 55 NUMBER 5 NOVEMBER

7 CEREBRAL ANGIOGRAPHY AFTER SURGERY FOR SACCULAR ANEURYSMS TABLE 8. Outcome according to World Federation of Neurosurgical Societies grade at 3 months a GOS score WFNS grade GR (%) MD (%) SD (%) VS (%) Dead (%) Total (73%) 36 (17%) 12 (6%) 2 (1%) 4 (2%) (48%) 19 (21%) 20 (22%) 2 (2%) 5 (6%) (26%) 7 (26%) 8 (30%) 0 (0%) 5 (19%) (21%) 26 (30%) 26 (31%) 1 (1%) 12 (14%) (7%) 12 (14%) 28 (33%) 15 (18%) 24 (28%) 85 Total 229 (46%) 100 (20%) 94 (19%) 20 (4%) 50 (10%) 493 a WFNS, World Federation of Neurosurgical Societies (2); GOS, Glasgow Outcome Scale (13); GR, good recovery; MD, moderate disability; SD, severe disability; VS, vegetative state. mented in three recent studies (1, 19, 30). Because vessel occlusion is diagnosed early, an immediate repositioning of the clip probably prevents ischemic damage to the brain. All efforts should be made during surgery to save the vessels and replace the clip; this is the golden moment for the patient and the surgeon. Small residual necks detected on a postoperative angiogram are left alone because of very difficult conditions at surgery (large and giant aneurysms), and reoperation probably would not achieve a better result. This leaves the responsibility to the experienced surgeon, who must make a judgment regarding each patient and aneurysm individually. In 7% of all patients, findings lead to reoperation or coiling. Considering the risk of both residual aneurysms and ischemic deficits caused by major vessel occlusion, virtually all patients should undergo intraoperative angiography. We have tested the value of intraoperative angiography in complex (large, giant, fusiform, and vertebrobasilar artery) aneurysms. If a simpler method were made available, intraoperative angiography should be used even in patients with uncomplicated aneurysms. Control angiography and postoperative computed tomography are recommended even when surgeons are highly experienced, as surprising findings can be observed despite the good condition of the patient. Experience slowly improves the results. The prevalence of middle cerebral artery aneurysms is typically high in the Finnish population. In addition, the femaleto-male ratio usually has been 50:50. In this series, the most common ruptured aneurysm is the anterior communicating artery aneurysm, and the number of female patients is somewhat higher than that of males. The reason for this is unknown. The study group has undergone 3 months of follow-up at our clinic. This is a short recovery period for aneurysmal SAH. For complete recovery, up to 2 years is needed, and a longer follow-up period probably would have demonstrated better results. The conclusion to be drawn from the Eastern Finland study (21, 31) and the International Subarachnoid Aneurysm Trial (25) is that only competent aneurysm surgeons should continue to perform open aneurysm surgery. In the presence of inexperience, the aneurysm should be coiled, even if the expected results are inferior to those that might be achieved via surgical clipping (20, 33). Competent aneurysm and endovascular surgeons should form neurovascular teams to discuss and tailor an individual treatment plan for each patient and ensure satisfactory results. Furthermore, today and in the future, a great amount of research effort should involve identification and treatment of aneurysms before their rupture, which will improve management results far more than any technical or medical advance. CONCLUSION Most intracranial aneurysms, ruptured or nonruptured, are treated perfectly and permanently. Even when surgeons are competent and have extensive experience with aneurysm surgery, patients should undergo postoperative DSA, as surprising findings of incomplete occlusion of the aneurysm and unplanned vessel occlusion are observed in one-sixth of patients. Because aneurysms located at the posterior circulation and large- or giant-sized aneurysms either in anterior or posterior circulation are more prone to inadequate clipping, their treatment should involve intra- and postoperative angiography. If a simpler method becomes available, intraoperative angiography should be used even in uncomplicated aneurysm cases. This series can be used as a basis to compare the results of other series reporting surgical or endovascular treatment and intraoperative angiography. REFERENCES 1. Chiang VL, Gailloud P, Murphy KJ, Rigamonti D, Tamargo RJ: Routine intraoperative angiography during aneurysm surgery. J Neurosurg 96: , NEUROSURGERY VOLUME 55 NUMBER 5 NOVEMBER

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Radiology 211: , Yaşargil MG: Microneurosurgery: Microsurgical Anatomy of the Basal Cisterns and Vessels of the Brain. Stuttgart, Georg Thieme, 1984, vol I. 33. Yaşargil MG: Reflections on the thesis Prospective outcome study of aneurysmal subarachnoid hemorrhage of Dr. Timo Koivisto. Available at: Acknowledgments This study was supported by the Maire Taponen Foundation. We thank Avula Chakrawarthi, M.D., for the preparation of the DSA studies for analysis. COMMENTS The neurosurgery group at Hospital presents a large and well-managed series of surgically treated cerebral aneurysms. More than 800 intracranial aneurysms were surgically clipped, followed by postoperative angiography. In this series, 12% of the aneurysms that were clipped were incompletely occluded. Sixty-one percent of these incomplete closures were totally unexpected on postoperative angiograms. Many of these patients were subjected to repeat operation for clip repositioning. Some patients were sent for endovascular treatment. Similarly, 44 major vessel or branch occlusions were noted on postoperative angiograms, and 32 of these occlusions were totally unexpected. Although large, giant, and complex aneurysms had significantly higher rates of residuals and vessel occlusions, it is interesting to note that many of the relatively simple anterior-circulation aneurysms also had unexpected findings on postoperative angiography. These data make a strong and convincing argument for the use of intraoperative angiography. It is likely that intraoperative angiography should be used on all aneurysm patients, because problems with clipping are sometimes unexpected, even on relatively simple aneurysms. It is often too late to prevent a stroke if there is a vessel occlusion that is picked up after surgery rather than within minutes after the clip has been placed. Similarly, the risks of taking the patient back to the operating room after a routine postoperative angiogram can be largely eliminated with the use of intraoperative angiography. For the past few years, I have used intraoperative angiography routinely on all aneurysm patients. Previously, I operated without the use of intraoperative angiography, but I believe that this technique is 1022 VOLUME 55 NUMBER 5 NOVEMBER

9 CEREBRAL ANGIOGRAPHY AFTER SURGERY FOR SACCULAR ANEURYSMS worth the small amount of inconvenience and the slight increase in time necessary to perform intraoperative studies. In retrospect, I realize that there were several intraoperative catastrophes that might have been avoided had intraoperative angiography been used. Since using intraoperative angiography, I have discovered several situations in which faulty clip placement was easily rectified. Robert A. Solomon New York, New York Kivisaari et al. provide a good contribution to the literature supporting the benefits of routine cerebral angiography after surgery for saccular aneurysm. They report a retrospective series of 622 patients with 955 aneurysms, of which 808 were surgically clipped and underwent postoperative angiography. They showed that even in very experienced hands, the frequency of unexpected incomplete closure was very high. This proves that it is worthwhile to perform a routine cerebral angiogram after clipping saccular aneurysms. They also showed, as a confirmation of what has been well established in the literature, that the size of the aneurysm had a significant impact on the closure rate. Large, complex, and giant aneurysms had a rather relevant smaller closure rate. In such cases, it is preferable to perform an intraoperative angiography. The occurrence of unexpected major vessel occlusions was also high in their series. Such occurrences can ideally be dealt with when an intraoperative angiogram is performed. However, the authors were able to reoperate on 14 patients with such unexpected major artery occlusions, in 2 by performing bypass surgery and in 12 by repositioning the clip. In total, 45 patients of the 808 were reoperated on or treated by the endovascular route because of the postoperative control angiogram. Another interesting finding of this article is that, briefly stated, experience accounts for better final results, as shown by the percentage of fundus remnant in the series of the senior author compared with those of the other 11 surgeons. After all that has been said, we must simply agree with the authors conclusion: postoperative cerebral angiography should be performed in all patients, and in the case of complex and giant aneurysms, the intraoperative angiography is mandatory. Atos Alves de Sousa Minas Gerdis, Brazil The authors present the largest series yet published on the efficacy of routine postoperative angiography for the evaluation of aneurysmal remnants. The authors carefully and methodically analyzed a variety of factors that might contribute to incomplete clipping. As noninvasive imaging methods advance and the use of intraoperative angiography becomes more common, the routine use of angiography is controversial. Our institution recently completed a prospective evaluation of intraoperative angiography as well as an evaluation of the surgeon s perceived need for angiography. We now believe that the benefits of intraoperative angiography outweigh the risks, and we have eliminated the use of routine postoperative studies. The findings from the study, designed to evaluate the surgeon s perceived need for angiography, suggested that the rate of unanticipated incomplete clipping is higher than reported. This aspect is very difficult to evaluate retrospectively. Ruth Bristol Robert F. Spetzler Phoenix, Arizona The authors present a retrospective analysis of 622 patients with cerebral aneurysms who underwent surgical clipping and postoperative angiography. Incomplete closures of aneurysms were detected in 97 patients by postoperative angiography. Thirty-eight of 97 incomplete closures were intentional, but 59 of 97 incomplete closures were unexpected. Conversely, 44 cases of major vessel occlusions were revealed by postoperative angiography, and 32 of 44 cases were unexpected. It is surprising that such a lot of unexpected findings were revealed by postoperative angiography, although experienced neurosurgeons performed clipping. It is believed that the complete closure of an aneurysm is crucial for the prevention of its subsequent growth and rupture. However, postoperative angiography recently tends to be avoided in many neurosurgical institutes. Hence, this article is considered to be important because it raises a warning against this tendency. In this article, the authors have analyzed the findings of postoperative angiography, but not intraoperative angiography, in aneurysm surgery. However, they conclude and recommend that intraoperative angiography should be used in more basic aneurysm cases, if a simpler method is available. Intraoperative angiography is considered to be very useful in aneurysm surgery, because we can detect unexpected residual aneurysms or vessel occlusions during operations. However, it has been reported that the false-negative intraoperative angiography rate is 1.1 to 8.3% (1 3). Therefore, intraoperative angiography should be conducted under ideal conditions and interpreted by experienced neurosurgeons and neuroradiologists. Hence, the continued necessity for postoperative angiography should be emphasized. Masato Hojo Nobuo Hashimoto Kyoto, Japan 1. Chiang VL, Gailloud P, Murphy KJ, Rigamonti D, Tamargo RJ: Routine intraoperative angiography during aneurysm surgery. J Neurosurg 96: , Tang G, Cawley CM, Dion JE, Barrow D: Intraoperative angiography during aneurysm surgery: A prospective evaluation of efficacy. J Neurosurg 96: , Vitaz TW, Gaskill-Shipley M, Tomsick T, Tew JM Jr: Utility, safety, and accuracy of intraoperative angiography in the surgical treatment of aneurysms and arteriovenous malformations. AJNR Am J Neuroradiol 20: , NEUROSURGERY VOLUME 55 NUMBER 5 NOVEMBER

10 KIVISAARI ET AL. The authors important conclusion is that intraoperative angiography should be performed in virtually all patients. Support for their argument can be found in the data for both ruptured and unruptured aneurysms when the majority of remnants were unexpected. Of 44 vessel occlusions, 32 were unexpected. Obviously, the demand for intraoperative angiography must be taken in the context of some associated risk to the patient associated with this procedure. In high-volume centers, however, intraoperative studies should be achievable with minimal risk and minimal extension of the operative procedure. There is little doubt that this practice should be applied to aneurysms of the anterior communicating artery complex, because 84% of residual aneurysms were unexpected in this series. H. Hunt Batjer Chicago, Illinois Thirty Systematic Color Series (oil on linen, ) by Richard Paul Lohse (courtesy of the Richard Paul Lohse Foundation, on loan to Kunsthaus, Zürich) VOLUME 55 NUMBER 5 NOVEMBER