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Abstract
Purpose: The purpose of this study is to report mid- and long-term clinical and angiographic results of coiling of basilar tip aneurysms.
Materials and Methods: Between January 1995 and August 2006, 154 basilar tip aneurysms were coiled. A total of 114 (74%) had ruptured and 40 (26%) were unruptured. There were 42 men and 112 women taking part in this study, with a mean age of 50.5 years (median, 50; range, 25–73 years). The mean aneurysm size was 11.1 mm (median, 10; range, 2–30 mm) and 71 (46%) were large or giant. Of 154 aneurysms, 40 (26%) were primarily coiled with a supporting device.
Results: Initial occlusion was (near) complete in 144 (94%) and incomplete in 10 (6%) aneurysms. The combined procedural mortality and morbidity was 3.8% (6 of 154, 95% CI 1.4–8.3%). The mean clinical follow-up of 144 surviving patients was 53 months (range, 3–144 months; 637 patient-years). The annual incidence rate for recurrent haemorrhage was 0.3% (2 in 637 patient years, 95% CI 0.04–1.1%). During angiographic follow-up of mean 34 months (range, 6–122 months) in 138 patients (96%), 27 basilar tip aneurysms (17.5%) re-opened over time and were additionally coiled. Of these, 11 repeatedly re-opened and were repeatedly coiled. An aneurysm size of median >10 mm was the only significant predictor for re-treatment at follow-up (OR 7.0, 95% CI 2.5–19.7).
Conclusion: Coiling of basilar tip aneurysms is safe and effective in preventing recurrent haemorrhage. Follow-up angiography is mandatory to timely detection of re-opening, especially in large and giant aneurysms.
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Since the introduction of detachable coils in the early 1990s, endovascular treatment of basilar tip aneurysms has rapidly replaced surgery for these lesions. Surgical approaches for basilar tip aneurysms are more challenging than for aneurysms at other locations, as these aneurysms are deeply located, confined in the narrow interpeduncular fossa in close proximity to the midbrain, and surrounded by important perforating arteries. As a consequence, surgery is associated with substantial morbidity.1–3 In several previous studies, the safety and effectiveness of coiling of basilar tip aneurysms has been established, in addition to the safety and effectiveness of large aneurysms and for patients in poor clinical grades.4–12
In this study, we report our experience in coiling of 154 consecutive patients with basilar tip aneurysms over a 12-year-period, with emphasis on recurrent haemorrhage and re-treatment at mid- and long-term follow-up.
MATERIALS AND METHODS
This observational study was compliant with institutional privacy policy. The Institutional Review Board gave exempt status for approval and informed consent.
Patients
Between January 1995 and July 2006, 1839 aneurysms were treated in our institution and 911 of these were selectively occluded with detachable coils. Patients with treated aneurysms were prospectively entered in a database that included various patient and aneurysm characteristics. In addition, clinical and angiographic follow-up results were prospectively collected and entered in the database at regular intervals. Since the beginning of the study period, endovascular treatment was the therapy of choice for posterior circulation aneurysms and only 7 of 314 posterior circulation aneurysms were treated surgically. One hundred and fifty-four aneurysms in 154 consecutive patients were located on the basilar tip and all were coiled. Thus, the frequency of basilar tip aneurysms was 8.4% (154 of 1839) of all treated intracranial aneurysms and 49% (154 of 314) of treated posterior circulation aneurysms. Of 154 basilar tip aneurysms, 114 had ruptured (74%) and 40 had not (26%). Of 40 unruptured aneurysms, 19 were incidentally found on imaging unrelated to presenting symptoms, 18 were additional to another ruptured aneurysm and 3 presented with symptoms of mass effect on the brain stem.
Included in this study were 42 men and 112 women, with a mean age of 50.5 years (median, 50; range, 25–73 years). Clinical grading according to the Hunt and Hess scale (HH) at the time of treatment in 114 patients with a ruptured basilar tip aneurysm was: HH I-II 68 patients, HH III 25 patients and HH IV-V 21 patients. Timing of treatment after subarachnoid haemorrhage (SAH) was 0–3 days in 43 patients, between 4 and 14 days in 53 patients, and ⩾14 days in 18 patients. Mean aneurysm size was 11.1 mm (median, 10; range, 2–30 mm). There were 83 small aneurysms (⩽10 mm), 61 large aneurysms (11–24 mm) and 10 giant aneurysms (⩾25 mm). Of 154 patients, 21 had 25 additional aneurysms at other locations coiled in the same session as for the basilar tip aneurysm.
Coiling procedure
Coiling of aneurysms was performed on a biplane angiographic unit (Integris BN 3000; Philips Medical Systems, Best, The Netherlands) with the patient under general anaesthesia. Prior to coiling or after placement of the first coil, a bolus of 2500 U heparin was administered intra-arterially, followed by drip infusion of 1000 U of heparin per 500 ml infusion fluid during the intervention. Heparin was continued intravenously or subcutaneously for 48 hours after the procedure, followed by 80 mg aspirin daily and orally for 3 months. For procedures with stent placement, patients were preloaded with antiplatelet medication (clopidogrel 75 mg and aspirin 80 mg daily). Coiling was performed with Guglielmi Detachable Coils (GDCs; Boston Scientific, Fremont, CA) or TruFill DCS/Orbit coils (Cordis, Miami, FL). Some large aneurysms were coiled with 50 cm long mechanically detachable coils (Detach 18; Cook Inc, Copenhagen, Denmark). The aim of coiling was to obtain a dense packing of the aneurysm, until not one additional coil could be placed.
In the occurrence of aneurysm perforation during coiling, heparin was reversed instantly and coiling was continued until the bleeding stopped. When thromboembolic complications occurred, usually a selective bolus injection of 100 000–250 000 units of urokinase alone was administered in the involved vessel; however, in the last 4 years, the urokinase was followed by intravenous infusion of a glycoprotein IIb/IIIa antagonist (tirofiban (Aggrastat); Merck & Co., Inc., Whitehouse Station, NJ, USA) for 24–48 hours.13 14 Initial angiographic results of coiling were classified as (near)complete occlusion and incomplete occlusion. Aneurysm occlusion was determined in consensus during a weekly joint meeting of two neurosurgeons, two neurologists and two neuroradiologists.
Supporting devices
Of 154 basilar tip aneurysms, 40 wide-necked aneurysms (26%) were primarily coiled with the aid of a supporting device. A wide neck was defined as a dome-to-neck ratio ⩽1 or when the origin of one or both posterior cerebral arteries was incorporated into the base of the aneurysm. Twenty-six were primarily coiled with a temporary supporting balloon. During the study period, several occlusion balloons were used for this purpose:15 Balt no I balloon glued onto a Magic 1.8 micro catheter (Balt, Montmorency, France); Endeavour non-detachable balloon (Boston Scientific); Solstice Balloon Occlusion System (Medtronic MIS, Sunnyvale, CA); Sentry 15 mm balloon (Boston Scientific); and HyperForm balloon (EV3, Irvine, CA).
Another 13 wide-necked basilar tip aneurysms were coiled with the aid of a TriSpan supporting device (Boston Scientific) and one incidental basilar tip aneurysm was coiled after placement of a stent (Neuroform; Boston Scientific).
Procedural complications
Procedural complications (aneurysm rupture or thromboembolic) of coiling leading to death or neurological disability at the time of hospital discharge were prospectively recorded in our database during the weekly joint meeting. For comatose patients, thromboembolic complications were considered to have caused neurological deficit if this was either clinically evident or if there were infarctions on subsequent CT scans in the territory of the involved vessel. Procedural rupture in comatose patients who subsequently died was considered to be procedural mortality.
Clinical and angiographic follow-up
Patients that survived the hospital admission period were scheduled for clinical follow-up in the outpatient clinic at 6 weeks and for angiographic follow-up at 6 and 18 months. Results of angiographic follow-up were classified in the same way as the initial post-embolisation occlusion. Incomplete occlusion at any point in time was considered to be an indication for further therapy, unless clinical or anatomical factors dictated otherwise. Clinical follow-up was assessed according to the Glasgow Outcome Scale (GOS) at every outpatient clinic visit and at every admission for follow-up angiography. Results and consequences of clinical and angiographic follow-up were discussed in the weekly joint meeting. When appropriate, during the meeting a decision was made for the need for additional treatment or extended angiographic or MRA follow-up. When additional treatment was performed, the result was evaluated in the weekly meeting and angiographic follow -up was scheduled at 6 months. Clinical follow-up of patients who refused or were unable to undergo follow-up angiography was assessed by contacting the family physician by telephone or in writing at various follow-up intervals. Of 154 patients, 85 were included in a previous mid-term clinical follow-up study conducted in January 2005.16
Statistical analysis
For patients that survived the hospital admission period, (re)bleeding after coiling was calculated as an incidence rate with corresponding 95% confidence intervals (CIs) for all aneurysms, for ruptured aneurysms and for unruptured aneurysms.
For all 154 basilar tip aneurysms, odds ratios (ORs) for the chance of re-treatment at follow-up were calculated for the following possible predictors: aneurysm size > median size (10 mm), ruptured aneurysms, use of a supporting device and initial incomplete aneurysm occlusion.
Statistical analysis was performed using univariate logistic regression for dependent and multivariate logistic regression for independent risk factors.
Mean size of basilar tip aneurysms that re-opened over time and were additionally coiled was compared with mean size of aneurysms that were stable at follow-up using the t-test.
The complication rate of first coiling was compared with the complication rate of additional coiling using the Chi square test.
RESULTS
Initial angiographic occlusion and complications
Initial angiographic occlusion of 154 basilar tip aneurysms was complete or near-complete in 144 (94%) and incomplete in 10 (6%) aneurysms. Complications occurred in 6 patients, leading to death in 5 (procedural mortality 5 of 154 (3.2%), 95% CI 1.1–7.4%) and to permanent neurological deficit in 1 patient (procedural morbidity 1 of 154 (0.6%), 95% CI 0.0–3.5%). Complications leading to mortality consisted of: 2 procedural aneurysm ruptures, 2 inadvertent (partial) occlusions and thrombosis of a posterior cerebral artery by malpositioned coils protruding from the neck ; and 1 rupture of a superior cerebellar artery branch by the guide wire during positioning of a supporting balloon. One inadvertent posterior cerebral artery occlusion led to permanent morbidity.
Clinical follow-up and re-bleeding rate
Clinical follow-up was available for all 154 patients. Of 40 patients with unruptured basilar tip aneurysms, 2 died of procedural complications; the remaining 38 patients were neurologically intact. Of 114 patients with ruptured basilar tip aneurysms, 8 patients died during hospital admission, 3 after procedural complications and 5 of direct impact of SAH or diffuse vasospasm. Two patients died before the 6 months’ follow-up interval: one patient died of brain abscess after ventricular drainage 3 months after coiling and the other patient died 4 months after incomplete coiling of a 30 mm basilar tip aneurysm of recurrent haemorrhage. The GOS score at 6 months’ follow-up for the remaining 112 patients was GOS 1 in 101 patients (90%), GOS 2 in 6 patients (5%) and GOS 3 in 5 patients (5%).
The mean clinical follow-up beyond the 6 months’ interval of all 142 surviving patients was 53 months (median, 49.5; range, 3–144 months; 637 patient-years). Five patients died of unrelated causes (pneumonia, 2; pulmonary embolism, 1; disseminated cancer, 2). Two other patients, who initially presented with symptoms of a mass effect on the brain stem, died of aggravation of symptoms 14 and 24 months after coiling of the basilar tip aneurysm. As well as the patient who died of recurrent haemorrhage 4 months after coiling, one other patient (who had refused 6 months’ follow-up angiography) experienced a recurrent haemorrhage 12 months after coiling. The annual incidence rate for re-bleeding was 0.3% (2 in 637 patient-years; 95% CI 0.04–1.1%) for all aneurysms, 0.4% for ruptured aneurysms (2 in 513 patient-years; 95% CI 0.05–1.4%) and 0.0% for unruptured aneurysms (0 in 124 patient-years; 97.5% CI 0.0–2.4%).
Angiographic follow-up
Of 144 patients that survived the hospital admission period, 2 died before the 6-month follow-up interval and 5 patients refused to follow angiography. The remaining 137 patients all had angiography at 6 months and the 1 patient with a recurrent haemorrhage at 12 months had a follow-up angiogram at the time of re-bleeding. Thus, follow-up angiography was available in 138 patients for a total of 296 angiograms: 55 patients had 1 follow-up angiogram; 39 patients had 2; 25 patients had 3; and 19 patients had 4–8 follow-up angiograms. The mean duration of angiographic follow-up was 34 months (median, 21.5; range, 6–122 months).
Additional treatments and risk factors
During follow-up, 27 basilar tip aneurysms (17.5%) re-opened over time and were additionally coiled. Of these 27 aneurysms, 11 repeatedly re-opened and were repeatedly coiled: 6 aneurysms were coiled 3 times, 3 aneurysms 4 times, 1 aneurysm 5 times, and 1 aneurysm 6 times. Four aneurysms were additionally coiled after placement of a stent (Enterprise; Cordis Neurovascular, Miami Lakes, FL) (fig. 1) and four aneurysms were repeatedly coiled with the aid of a supporting balloon. All 46 additional coilings were without complications (0%; 97.5% CI 0.0–6.3%). The complication rate of 3.8% of first coiling did not differ significantly from the complication rate of 0% of the additional coiling (Chi square, p = 0.40).
Aneurysm re-opening over time was by compaction (fig. 1) or migration of coils into intraluminal thrombus in 24 of 27 aneurysms. The mean interval between the first and second coiling was 17 months (median, 12; range, 5–100 months). One small basilar tip aneurysm that was initially completely occluded showed gradual growth over a period of almost 9 years and was finally additionally treated after placement of a stent (fig. 2). Two very large aneurysms that were repeatedly coiled showed late regrowth of the aneurysm at the base near the inflow zone, which was apparent at 89 and 130 months after first coiling (76 and 95 months after last coiling, respectively). Altogether, in 154 patients, 225 coil treatments were performed (145 primary coilings, 25 additional aneurysms and 46 repeated coilings).
The mean size of 17.0 mm of 27 basilar tip aneurysms that re-opened over time and were additionally coiled was significantly larger than the mean size of 9.9 mm of 127 aneurysms that were coiled once (t-test, p<0.0001). Of 27 additionally treated aneurysms, 22 were large or giant.
Aneurysm size > median 10 mm was the only significant predictor for re-treatment at follow-up (table 1).
DISCUSSION
In this study, we found that coiling of basilar tip aneurysms is associated with low morbidity and adequately protects against recurrent or primary haemorrhage. During clinical follow-up of all 144 surviving patients and angiographic follow-up of 138 patients (96%) up to 12 years, re-opening needing additional coiling occurred in 27 aneurysms (17.5%). Of these 27 aneurysms, 11 (7%) repeatedly re-opened and were repeatedly coiled up to six times. The only significant predictor for re-opening and re-treatment was large aneurysm size. The high re-treatment rate of 17.5% is in concordance with other studies concerning basilar tip aneurysms5 6 11 12 and may be explained by the fact that many basilar tip aneurysms had a wide neck and almost half of the aneurysms were of large or giant size.5 In many patients with large or giant basilar tip aneurysms, coiling may be considered to be a staged treatment with ongoing follow-up. Our findings indicate that basilar tip aneurysms that re-open over time and need to be coiled for a second time, should be followed with angiography or MRA at regular intervals (1–3 years), even when aneurysm occlusion is stable during some years.
Our strict clinical and angiographic follow-up strategy with additional treatment when necessary and possible was effective in preventing recurrent haemorrhage in ruptured aneurysms or primary haemorrhage in unruptured aneurysms. Only 2 patients experienced recurrent haemorrhage during follow-up and, in both patients, this could probably have been prevented. In one patient, treated in 1995, failure of electrolytic detachment of coils precluded adequate occlusion of a 30 mm aneurysm. This flaw of early GDC design has been overcome in later years. The other patient refused 6 months’ follow-up angiography and had a recurrent haemorrhage 12 months after coiling. Angiography at that time showed a 50% re-opening and enlargement of the aneurysm. It is likely that this re-opening would have been present at 6 months, and additional coiling should then have been performed. Our annual incidence of recurrent haemorrhage of 0.3% is lower than that reported in other studies. In a meta-analysis by Lozier et al.11 concerning 221 eligible patients with basilar tip aneurysms, the annual incidence of recurrent haemorrhage was 0.7%. Henkes et al.12 reported 11 recurrent haemorrhages after coiling in a series of 317 patients with incomplete angiographic and clinical follow-up.
When giant basilar tip aneurysms present with symptoms of a mass effect on the brain stem, coiling seems not to be effective: 2 of 3 patients in this study died of progressive brain-stem dysfunction 14 and 24 months after complete occlusion with coils and the other patient died of a procedural complication. Although different treatment strategies for these aneurysms, such as single or double vertebral artery occlusion and (bypass) surgery were considered, these therapies were not judged to be feasible.
Although many wide-necked basilar tip aneurysms can be adequately occluded with coils without a supporting device, in 40 of 154 aneurysms (26%) with wide necks that incorporated the ostia of posterior cerebral arteries, primary coiling was performed with the aid of a supportive balloon, TriSpan or stent. Also, many additional coilings were performed with these devices.
As well as procedural rupture, thromboembolic occlusion of one or two posterior cerebral arteries by protrusion of coil loops from the neck at the end of the procedure was the most serious complication leading to mortality in three patients and to morbidity in one patient. Despite formation of an adequate basket over the neck of the aneurysm with the first coils, with insertion of additional coils, the coil mesh may slowly expand with protrusion into the parent posterior cerebral arteries, resulting in flow restriction and thrombosis. The use of a supporting balloon to protect the neck does not always prevent this complication. A possible solution is placement of a stent. During most of the study period, intracranial stents were not yet available and only one patient was primarily coiled after stent placement. At the end of the study period, a new stent system became available and this stent proved to be easy to handle and valuable in re-treating re-opened wide-necked basilar tip aneurysms.17 However, a drawback of stent placement in acutely ruptured aneurysms is the required antiplatelet medication. This medication is preferably preloaded several days before stent placement and, as patients may not be responding to both clopidogrel and aspirin, verification of response is recommended. To overcome this drawback in patients with acutely ruptured aneurysms, another possible solution to prevent occlusion of the parent artery is leaving the neck wide open at initial treatment, followed by stent placement and complete occlusion at a later stage (compaction usually occurs within the first 6 months).
This study is a single-centre experience, with basilar tip aneurysms treated with coiling. Since the introduction of coiling in our hospital in 1994, no basilar tip aneurysm has been operated on. Thus, effectively, all treated basilar tip aneurysms are included in the study. For the most part of the study period, our institution has been a tertiary referral centre for the endovascular treatment of aneurysms (especially basilar tip aneurysms) for the whole country. For this reason, basilar tip aneurysms may have been over-represented in our patient population.
CONCLUSION
Coiling of basilar tip aneurysms is safe and effective in preventing recurrent or primary haemorrhage. Follow-up angiography is mandatory to timely detection of re-opening, especially in large and giant aneurysms. Various supporting devices (balloons, stents, TriSpan) are available to coil wide-necked basilar tip aneurysms successfully.
REFERENCES
Footnotes
Competing interests: None declared.