Radiology
Neuroradiology Menno Sluzewski, MD, PhD Willem Jan van Rooij, MD, PhD Gabrie¨l J. E. Rinkel, MD, PhD Douwe Wijnalda, MD
Index terms: Aneurysm, cerebral, 17.73 Brain, hemorrhage, 17.434 Published online 10.1148/radiol.2273020656 Radiology 2003; 227:720 –724 Abbreviations: SAH ⫽ subarachnoid hemorrhage HH ⫽ Hunt and Hess score GOS ⫽ Glasgow Outcome Scale
Endovascular Treatment of Ruptured Intracranial Aneurysms with Detachable Coils: Long-term Clinical and Serial Angiographic Results1 PURPOSE: To evaluate the stability of aneurysm occlusion over time, the need for additional treatments, and the long-term clinical outcome of patients, with emphasis on late recurrences of bleeding. MATERIALS AND METHODS: The records of 160 patients with aneurysmal subarachnoid hemorrhage who were treated with coils were retrospectively reviewed. Follow-up angiography was performed 6 and 18 months after coil placement, and the results were classified as complete, near complete, and incomplete occlusion.
1
From the Departments of Radiology (M.S., W.J.v.R.) and Neurosurgery (D.W.), St Elisabeth Ziekenhuis, Hilvarenbeekseweg 60, 5022 GC Tilburg, the Netherlands; and Department of Neurology, University Medical Centre, Utrecht, the Netherlands (G.J.E.R.). Received June 4, 2002; revision requested July 30; final revision received September 27; accepted November 4. G.J.E.R. supported in part by grant D98.014 from the Netherlands Heart Foundation. Address correspondence to M.S. (e-mail:
[email protected]).
RESULTS: Six (4%) of the 160 patients experienced procedural mortality or dependency. After a mean follow-up of 36 months, 134 (84%) patients had a good outcome. Outcome was independent of aneurysm size and location and timing of treatment. Reopening of the aneurysm occurred exclusively during the first 6 months after coil placement, mainly in aneurysms larger than 15 mm. Between 6 and 18 months, no change in aneurysm occlusion was observed. Additional coil placement was performed in 15 (9%) patients. After this second coil placement, nine (7%) aneurysms were still incompletely occluded. Additional therapy was performed in eight (5%) patients. Two recurrences of bleeding were observed in two incompletely occluded large aneurysms. No recurrences of bleeding occurred in patients with completely or near completely occluded aneurysms. CONCLUSION: Coil placement is an effective and safe treatment strategy for patients with aneurysmal subarachnoid hemorrhage. If aneurysm occlusion is sufficient at 6 months, the yield of further follow-up angiography is very low. ©
Author contributions: Guarantors of integrity of entire study, M.S., W.J.v.R.; study concepts, all authors; study design, M.S., W.J.v.R., G.J.E.R.; literature research, M.S., W.J.v.R.; clinical studies, M.S., W.J.v.R., D.W.; data acquisition, M.S., W.J.v.R.; data analysis/ interpretation, all authors; statistical analysis, G.J.E.R.; manuscript preparation, M.S., W.J.v.R.; manuscript definition of intellectual content, all authors; manuscript editing, M.S., W.J.v.R.; manuscript revision/review, G.J.E.R., D.W.; manuscript final version approval, all authors. ©
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Endovascular occlusion of intracranial aneurysms with detachable coils has been employed in thousands of patients since its introduction in the early 1990s, and in many centers it equals placement of a neurosurgical clip as the first treatment option (1,2). Endovascular treatment with coils is effective for prevention of early recurrences of bleeding, and this technique has a low risk of procedural complications (3). Despite the widespread use of detachable coils, data on long-term management and outcome are scarce. Main concerns with this treatment are the fate of patients with an aneurysm that is initially not completely occluded and the possibility of reopening of the aneurysm lumen over time. These are concerns because they expose the patient to the risk of a recurrent hemorrhage. The purpose of our study was to evaluate the stability of aneurysm occlusion over time, the need for additional treatments, and long-term clinical outcome with emphasis on late recurrences of bleeding.
MATERIALS AND METHODS Patients From January 1995 to January 2000, 163 consecutive patients with subarachnoid hemorrhage (SAH) were referred for treatment of a ruptured aneurysm with coils. During the
Radiology
same period, 75 patients with an unruptured aneurysm underwent coil placement. Meanwhile, 45 patients with an aneurysm underwent parent vessel balloon occlusion, and 658 underwent surgery. The assignment of patients to methods of treatment was made in a joint meeting of neurosurgeons, neurologists, and interventional neuroradiologists. During the study period, the indication for coil placement gradually changed from “high surgical risk” aneurysms to all aneurysms amenable for coil placement, and as a consequence, the proportion of aneurysms treated endovascularly rose from 29 (15%) of 191 in 1995 to 82 (57%) of 143 in 1999. Among the 163 patients who underwent endovascular coil placement, the procedure failed in three patients, each with one aneurysm. The aneurysm was successfully treated with clip placement in two of these patients; however, clip placement failed in the third patient, who died 3 months later of a recurrence of bleeding. Thus, the study group consisted of 160 patients. The baseline characteristics of these patients and aneurysms are listed in Table 1. Our Institutional Review Board did not require its approval or patient informed consent for this study.
Methods Coil placement procedure.—Coil placement was performed with use of general anesthesia and systemic administration of heparin. Intravenously or subcutaneously administered heparin (Fragmin; Pharmacia, Woerden, Netherlands) was continued for 48 hours after the procedure, followed by orally administered aspirin (Ascal; Viatris, Diemen, Netherlands) for 3 months. Coil placement was performed with Guglielmi detachable coils (GDC-10 and/or 18; Target Therapeutics, Freemont, Calif), and some, mainly large, aneurysms were treated with mechanically detachable coils (Detach 18; Cook, Copenhagen, Denmark). The aim of coil placement was to pack the aneurysm as densely as possible, until not one more coil could be placed. Clinical outcome.—We (M.S., W.J.v.R., D.W. by consensus) reviewed all relevant clinical and imaging data of the 160 consecutive patients who underwent successful coil placement. Clinical follow-up was assessed according to the Glasgow Outcome Scale (GOS) (5) at every admission for follow-up angiography and at every visit to the outpatient clinic. Beginning in October 2001, all patients who Volume 227
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did not undergo follow-up angiography or visit the outpatient clinic in the previous 2 months were contacted by telephone and read a standard questionnaire designed to identify any change in the clinical condition of the patient since the last visit. For patients with less than good clinical outcomes (GOS 1–3), an effort was made to determine the cause of the disabling neurologic deficit or death, in particular whether this was related to the procedure, the disease, or other factors. Angiographic outcome.—Aneurysm occlusion after coil placement was assessed on the initial postembolization angiogram, as well as on follow-up angiograms, and was defined as complete (98%–100% occlusion), near complete (90%–98% occlusion), and incomplete (⬍90% occlusion). Incomplete occlusion at any point in time was considered an indication for further therapy. Follow-up angiography was scheduled at 6 and 18 months after coil placement. Analysis of angiographic aneurysm occlusion included five stages. (a) Initial aneurysm occlusion was assessed in all 160 patients. (b) The angiograms of the patients who underwent 6-month follow-up angiography were compared with the initial images after occlusion, with an emphasis on the change of the aneurysm occlusion during the first 6 months. The mean sizes of the aneurysms that reopened and the aneurysms that were stable were calculated. Also, the proportion of aneurysms smaller than 15 mm versus those 15 mm or larger that reopened was calculated. (c) The 18-month follow-up angiograms (when available) were compared with the 6-month follow-up angiograms to detect possible late changes in aneurysm occlusion. (d) After the 6-month follow-up angiogram was analyzed, the angiographic results of the patients who underwent coil placement twice were analyzed separately. (e) The final angiographic results were exclusively assessed for those patients who underwent follow-up angiography at least once after initial or second coil placement.
Data Analysis For the chance of less than good outcome, we calculated relative risks with corresponding 95% CIs for the following factors: age greater than median age, poor clinical condition at the time of treatment (HH IV–V), procedure-related complications, aneurysm size of 15 mm or larger, and aneurysm location in the posterior circulation. For patients in whom aneurysm occlusion decreased between the initial
TABLE 1 Baseline Characteristics of 160 Patients with Aneurysmal SAH
Baseline Characteristic Sex Women Men Timing of treatment Early (0–3 d) Intermediate (4–10 d) Late (11–30 d) Delayed (31–60 d) Clinical condition at time of treatment Good (HH I–II) Moderate (HH III) Poor (HH IV–V) Location of ruptured aneurysm Carotid artery Middle cerebral artery Anterior communicating or cerebral artery Posterior circulation Size of aneurysm (mm) ⱕ10 11–25 ⱖ25 ⬍15 ⱖ15
No. of Patients (n ⫽ 160) 110 (69) 50 (31) 27 (17) 57 (36) 57 (36) 19 (12) 106 (66) 33 (21) 20 (12) 35 (22) 15 (9) 41 (26) 69 (43) 97 (61) 57 (36) 6 (4) 125 (78) 35 (22)
Note.—Median age of patients was 50 years with a range of 26 –78 years. Numbers in parentheses are percentages. HH ⫽ Hunt and Hess score.
postembolization angiogram and the first follow-up angiogram at 6 months, we calculated relative risks with corresponding 95% CIs for the following factors: age greater than median age, poor clinical condition at the time of treatment (HH IV–V), aneurysm size of 15 mm or larger, and aneurysm location in the posterior circulation. We calculated the annual risk of recurrence of bleeding (number of recurrences of bleedings divided by patient follow-up years) for all 160 patients, for patients with an incompletely occluded aneurysm at some stage, and for patients with a completely or near completely occluded aneurysm at initial postembolization angiography and all follow-up angiography.
RESULTS Clinical Results All 160 patients were clinically observed. After a mean follow-up period of 37.1 months (median, 36 months) totalling 496 patient years, 18 patients died (GOS 1), seven patients became dependent (GOS 3), and 135 patients had a good outcome (GOS 4 and 5). The reaRuptured Intracranial Aneurysms
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TABLE 2 Causes of Less than Good Outcome after a Mean Follow-up of 37.1 Months in 160 Patients Cause
GOS 1
GOS 3
Procedure related Disease related Unrelated to treatment Recurrence of bleeding
5 6 6 1
1 4 1 1
18
7
Total
TABLE 3 Relative Risk Factors of Dependency and Death Risk Factors
Relative Risk 95% CI
Age ⬎ median Poor condition (HH IV–V) Procedural complications Aneurysm size ⱖ 15 mm Posterior circulation Early treatment (⬍ 4 d)
1.8 4.1 3.4 1.2 0.6 0.9
0.8, 3.8 1.9, 8.6 1.6, 7.3 0.5, 3.0 0.3, 1.3 0.8, 1.2
constructed, and bilateral vertebral balloon occlusion was performed (6). Six months later, this patient had a fatal recurrence of bleeding from this aneurysm, as confirmed at autopsy. The second patient, a 73-year-old woman, had SAH from a 15-mm basilar tip. The aneurysm was treated with coil placement, which resulted in near complete occlusion. She fully recovered and declined follow-up angiography. One year later, she had a recurrence of bleeding, and angiography showed the aneurysm to have reopened 50% due to resolution of intraluminal thrombus that was not appreciated on the initial angiogram. In retrospect, this intraluminal thrombus could have been suspected from the displacement of the thalamoperforating arteries. This patient underwent coil placement a second time with complete occlusion that was stable at 6-month follow-up angiography. She became dependent (GOS 3).
Angiographic Results
sons for less than good clinical outcome in the 25 patients are summarized in Table 2. Five patients died of procedurerelated complications (procedural rupture, n ⫽ 2; thromboembolic event, n ⫽ 3), and one patient became dependent after a thromboembolic complication (procedure-related complication rate leading to mortality or dependency: 4%, 95% CI: 1.4%, 8%). Six patients died of sequelae of SAH; the clinical grade at the time of treatment was HH I–II in one patient and HH IV–V in five patients. Six patients died of unrelated causes, including surgery for another aneurysm (n ⫽ 2), brain abscess (n ⫽ 1), cardiac arrest (n ⫽ 1), renal cell carcinoma (n ⫽ 1), and pneumonia (n ⫽ 1). One patient became dependent after undergoing treatment of another aneurysm with coil placement. The relative risk factors for dependency or death are summarized in Table 3. Two patients had a recurrent SAH from the aneurysm that was treated with coil placement during the follow-up period that resulted in an annual recurrence of bleeding rate of 2/496 patient years ⫽ 0.4% (95% CI: 0.1%, 1.5%). The first patient, a 52-year-old man, had SAH from a 28-mm basilar tip aneurysm that occurred in 1995. Coil placement was incomplete (approximately 50% occlusion) due to failure of electrolytic detachment of additional coils after insertion of 11 coils. A bypass from the external carotid artery to the posterior cerebral artery was 722
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Initial results after coil placement.—Immediate postembolization angiography in 160 patients with 160 aneurysms showed the following results: complete aneurysm occlusion in 113 (71%) patients, near complete occlusion in 35 (22%) patients, and incomplete occlusion in 12 (8%) patients. Results at 6-month follow-up.—At 6-month follow-up, 15 of 160 patients had died. Five patients had received additional therapy for the same aneurysm after coil placement (surgery, n ⫽ 4; parent vessel balloon occlusion, n ⫽ 1). Of the remaining 140 patients, 14 declined follow-up angiography (6-month angiographic follow-up rate, 126 [90%] of 140). The initial results in these 14 patients were complete occlusion in 12, near complete occlusion in one, and incomplete occlusion in one. The initial angiographic results and the results after 6 months (mean, 6.5 months; median, 6 months) in the 126 patients are summarized in Table 4. In 88 (70%) patients, the occlusion was stable; in 31 (25%) patients, the occlusion decreased; and in seven (6%) patients, the occlusion increased. The mean size of aneurysms that reopened was 14.7 mm (median, 14 mm). The mean size of aneurysms that were stable or improved was 9.2 mm (median, 8 mm). The proportion of aneurysms 15 mm or larger that reopened was 15 (52%) of 29, versus 16 (16%) of 97 aneurysms less than 15 mm. The relative risk factors for decrease in aneurysm occlusion between the initial postembolization angio-
gram and the first follow-up angiogram at 6 months are listed in Table 5. Results at 18-month follow-up.—Of the 126 patients with a follow-up angiogram at 6 months, 125 survived the 18-month follow-up interval. One patient died of cardiac disease. At 18-month follow-up, 14 patients received additional therapy for the same aneurysm (13, second coil placement; one, clip placement). Of the remaining 111 patients, 21 declined 18month follow-up angiography (18month angiographic follow-up rate, 90 [72%] of 125). The results of 6-month angiography in the 21 patients who declined 18-month follow-up angiography were complete occlusion, n ⫽ 17; near complete occlusion, n ⫽ 3; and incomplete occlusion, n ⫽ 1. Ninety patients underwent coil placement once as a sole therapy and underwent angiography at 6-months and 18months. The results at 18 months were complete occlusion in 58, near complete occlusion in 27, and incomplete occlusion in 5. None of these 90 aneurysms showed any change in occlusion between 6-month and 18-month follow-up angiography. Results at extended follow-up.—A third follow-up angiogram was obtained in 13 patients (median, 39 months; range, 24 –55 months), and a fourth follow-up angiogram was obtained in four patients (median, 44 months; range, 40–73 months). The occlusions were stable compared with the occlusions seen on the 6-month and 18-month follow-up angiograms. Regrowth of aneurysms was not observed. Results of aneurysms treated with more than one coil placement.—The occlusion status of the 15 aneurysms (9%) that were treated with coil placement more than once are summarized in Table 6. The decision to perform a second coil placement was made in 13 patients after 6-month follow-up angiography and in two patients after 18-month follow-up angiography. The mean size of these 15 aneurysms was 20.1 mm (median, 20 mm). One patient underwent coil placement a third and fourth time, and a complete occlusion was the final result. Five of these 15 patients underwent extended angiographic follow-up at 22, 24, 25, 31, and 54 months. None of their aneurysms showed any change in occlusion in comparison to the 6-month follow-up angiogram obtained after second coil placement. Final Results.—Final occlusion was exclusively assessed for the 126 patients with at least one 6-month follow-up angiogram after initial or second coil placeSluzewski et al
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ment. The mean angiographic follow-up period was 20.3 months (median, 19 months; range, 5–73 months), totaling 213 patient years (Table 7). Three of nine patients with an incomplete occlusion at last follow-up underwent successful surgery. In six patients, no further therapy was offered because of unfavorable anatomy of the aneurysm (n ⫽ 3) or because the patient was older than 70 years (n ⫽ 3). Second coil placement was required in 12 (41%) of 29 aneurysms greater than or equal to 15 mm and in three (3%) of 97 aneurysms less than 15 mm. Results after additional therapy other than second coil placement.—During the follow-up period, eight (5%) of 160 patients received additional therapy other than second coil placement for the same aneurysm. Seven patients underwent surgery, and one patient underwent parent vessel balloon occlusion. Four patients underwent placement of a clip within 3 weeks of the initial coil placement. One patient underwent clip placement after the first follow-up angiograms were obtained at 6 months, and two patients underwent clip placement after the 6-month follow-up angiograms were obtained after the second coil placement. One parent vessel balloon occlusion was performed 1 month after initial coil placement. Relation between angiographic results and recurrence of bleeding.—There were 28 patients with an incompletely occluded aneurysm at some stage. Two of these 28 patients experienced a recurrent SAH during a mean follow-up period of 36 months totaling 83 patient years (recurrence of bleeding rate 2 (2.4%) of 83, 95% CI: 0.3, 8.4%). There were 105 patients with a completely or near completely occluded aneurysm at initial postembolization and all follow-up angiography. In these 105 patients, no recurrences of bleeding occurred during a mean follow-up period of 41.2 months, totaling 362 patient years (recurrence of bleeding rate 0%; 95% CI: 0%, 1%).
DISCUSSION We found that coil placement was an effective and safe treatment strategy for patients with an aneurysmal SAH who underwent coil placement as an initial treatment. Although 15 (9%) of 160 patients underwent a second coil placement, the aneurysm was completely or near completely occluded in 117 (93%) of the 126 patients. Additional coil placeVolume 227
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TABLE 4 Initial Results and Changes at 6-month Follow-up Angiography in 126 Patients Initial Angiography 6-Month Angiography
Complete Occlusion
Near Complete Occlusion
Incomplete Occlusion
Total
Complete occlusion Near complete occlusion Incomplete occlusion
68 15 6
6 16 10
1 0 4
75 (59) 31 (25) 20 (16)
89 (71)
32 (25)
5 (4)
126 (100)
Total
Note.—Numbers in parentheses are percentages.
ment was needed mainly in aneurysms of 15 mm or larger. After additional clip placement in seven (4%) of 160 patients and parent vessel balloon occlusion in one (1%) of 160 patients, six patients still had an incompletely occluded aneurysm. There were no complications of additional treatments. We found no benefit of 18-month follow-up angiography in patients with completely or near completely occluded aneurysms at 6 months. Change in the occlusion rate between 6 and 18 months and at extended follow-up did not occur. In two other long-term follow-up studies (7,8), four late changes in aneurysm occlusion were observed in 482 aneurysms, which resulted in one recurrence of bleeding. Two additional late recanalizations, albeit anecdotal, have been reported after a stable result at 6-month and 12-month follow-up angiography, indicating that late reopening can occur (9,10); in our view, however, it is questionable whether this very low rate of late recurrence warrants long-term angiographic follow-up in all patients with a completely occluded aneurysm after 6 months. After initial coil placement, a substantial proportion of aneurysms show a change in the occlusion rate during the first 6 months, with aneurysm size greater than or equal to 15 mm being a strong risk factor for decreased occlusion. About one of four aneurysms has or will develop a neck remnant, but the clinical relevance is likely to be low since we did not observe any recurrences of bleeding from these nearly completely occluded aneurysms. This is in concordance with results of other studies, in which recurrences of bleeding have been exclusively reported from incompletely occluded aneurysms (6,11–15). About one of eight aneurysms either is or will become incompletely occluded. Since these aneurysms may bleed again,
TABLE 5 Relative Risk Factors of Decrease in Aneurysm Occlusion in the First 6 Months after Coil Placement Risk Factors Age ⬎ median Poor condition (HH IV–V) Aneurysm size ⱖ 15 mm Posterior circulation
Relative Risk 95% CI 1.5 1.1 3.4 0.8
0.8, 2.8 0.4, 3.1 2.0, 5.9 0.4, 1.5
additional endovascular or surgical therapy is indicated. The complication rate in this series was low and comparable to that of other studies (3). Long-term clinical outcome was good in 135 (84%) of our 160 patients and independent of timing of coil placement after SAH and size and location of the aneurysm, as confirmed in previous studies (7,13,15–17). This contrasts with surgical clip placement, where outcome is negatively affected by a higher complication rate from early treatment, large aneurysm size, and aneurysm location in the posterior circulation (18 – 20). The need for angiographic follow-up in all patients treated with coil placement and the need for additional treatment in some patients are obvious disadvantages of this procedure. After surgery, angiography is not routinely performed because it is assumed that the clip was placed successfully; however, several studies have shown that if postoperative angiography was performed, 4%–26% of the aneurysms would have a neck remnant (21,22). Our retrospective study has several inherent shortcomings in data collected. Advantages of the study design are the long-term follow-up and the high proportion of patients with serial angiographic follow-up. Because our study is treatment based, our results do not apply to patients with SAH in general. ComparRuptured Intracranial Aneurysms
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TABLE 6 Angiographic Results of 15 Patients that Underwent Coil Placement More than Once
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12. Time of Angiography
Complete Occlusion
Near Complete Occlusion
Incomplete Occlusion
Total
Initial 6-mo follow-up After second coil placement (mean, 9 mo) 6 mo after second coil placement
4 0 8 5 (6)
9 1 6 6
2 14 1 4 (3)
15 15 15 15
13.
Note.—Data in parentheses include the result of third and fourth coil placement in one patient. 14.
TABLE 7 Final Occlusion Status in 126 Patients Final Occlusion Status Complete Near complete Incomplete
No. of Patients 81 (64) 36 (29) 9 (7)
Note.—Numbers in parentheses are percentages.
ison of our study with neurosurgical studies of patients with SAH is not valid because of variances in clinical grading, timing of treatment, aneurysm location, and outcome assessment. Direct comparisons are ideally made with randomized trials, but such trials can be performed only in patients with aneurysms that are suitable for placement of either a clip or a coil. Many patients with aneurysmal SAH are poor candidates for surgery either because of their poor clinical condition or because the physician anticipates technical problems during surgery. Randomized trials will therefore include only a minority of patients with SAH (23); hence, large observational studies with prospective data collection will also be needed to compare these techniques properly. We conclude that coil placement is an effective and safe treatment strategy for patients with aneurysmal SAH. Although one of eight aneurysms is or will become incompletely occluded, this can be adequately managed with additional coil placement or surgery. If aneurysm occlusion is sufficient at 6 months, the benefit of further follow-up angiography is very low.
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