Abstract
The influence of aneurysm size on the outcomes of endovascular management (EM) for aneurysmal subarachnoid hemorrhages (aSAH) is poorly understood. To evaluate the outcomes of EM for ruptured large cerebral aneurysms, we retrospectively analyzed the medical records of patients with aSAH that were treated with coiling between 2013 and 2020 and compared the differences in outcomes depending on aneurysm size. A total of 469 patients with aSAH were included; 73 patients had aneurysms measuring ≥10 mm in diameter (group L), and 396 had aneurysms measuring <10 mm in diameter (group S). The median age; the percentage of patients that were classified as World Federation of Neurological Surgeons grade 1, 2, or 3; and the frequency of intracerebral hemorrhages differed significantly between group L and group S (p = 0.0105, p = 0.0075, and p = 0.0458, respectively). There were no significant differences in the frequencies of periprocedural hemorrhagic or ischemic events. Conversely, rebleeding after the initial treatment was significantly more common in group L than in group S (6.8% vs. 2.0%; p = 0.0372). The frequency of a modified Rankin Scale score of 0-2 at discharge was significantly lower (p = 0.0012) and the mortality rate was significantly higher (p = 0.0023) in group L than in group S. After propensity-score matching, there were no significant differences in complications and outcomes between the two groups. Rebleeding was more common in large aneurysm cases. However, propensity-score matching indicated that the outcomes of EM for aSAH may not be affected markedly by aneurysm size.
Keywords: large aneurysm, subarachnoid hemorrhage, coil embolization
Introduction
The International Subarachnoid Aneurysm Trial (ISAT) was the first trial to show the effectiveness of coil embolization (CE) for ruptured cerebral aneurysms.1) However, 92% of the aneurysms in the ISAT measured <10 mm in diameter. The outcomes of CE for an aneurysmal subarachnoid hemorrhage (aSAH) may be worse in patients with large aneurysms than in patients with small aneurysms because recurrence and rebleeding are more common in patients with large aneurysms.2-6) To the best of our knowledge, few previous studies have compared the clinical characteristics and treatment outcomes of small and large aneurysms, and how the size of a ruptured cerebral aneurysm affects its outcomes is poorly understood. The purpose of this study is to evaluate the clinical characteristics and treatment outcomes of CE for large aneurysms and compare them with those of CE for small aneurysms performed in the same period.
Materials and Methods
Patient population
This was an institutional review board (IRB)-approved, retrospective multicenter cohort study conducted at six institutions in Japan. It was based on the medical records of patients with aSAH who underwent endovascular management (EM) between January 2013 and April 2020 (Tsukuba University IRB: #H30-137). Opt-out consent was employed, and the requirement to obtain informed consent was waived by IRB.
We classified aneurysm locations as follows: A1, the anterior communicating artery, and the distal anterior cerebral artery (dACA) were classified as the ACA; the basilar artery (BA) trunk, basilar-superior cerebellar artery, and BA bifurcation were classified as the BA; and the vertebral artery (VA) trunk and VA-posterior inferior cerebellar artery were classified as the VA. Internal carotid artery (ICA) aneurysms were classified into posterior communicating artery, distal ICA (ICA-anterior choroidal artery and the ICA bifurcation), and proximal ICA (ICA-cavernous and ICA-paraclinoid) aneurysms.
All procedures were performed under general anesthesia. During the procedure, heparin was administered to control the activated clotting time at 200 s. The degree of aneurysm occlusion after the initial CE was defined as follows: the total exclusion of the aneurysm from the circulation was classified as complete occlusion (CO), limited residual filling at the junction with the parent vessel was classified as a neck remnant (NR), and residual filling within the coil interstices or at the aneurysm's perimeter was classified as body filling (BF). Periprocedural hemorrhagic events included intraprocedural aneurysmal perforation, blood vessel perforation, enlargement of the intracranial hemorrhage after the procedure, and a new intracerebral hemorrhage (ICH) that appeared after the procedure. Ischemic events included all cerebral infarctions due to coil migration, thrombus formation, or vasospasm that occurred during the procedure and delayed cerebral ischemia (DCI) with or without symptoms. DCI was defined as cerebral ischemia that was detected by magnetic resonance imaging within 14 days after the procedure. Postdischarge aneurysm evaluation was performed by MR angiography or digital subtraction angiography within 3 months of initial treatment. If signs of recurrence were seen at that time, retreatment was considered. Retreatment included CE or clipping of the treated aneurysm.
Statistical analysis
To detect the features of clinical characteristics and outcomes of patients with large aneurysms, we compared the clinical factors between patients whose aneurysms measured ≥10 mm in diameter and those whose aneurysms measured <10 mm in diameter. To find out the clinical factors that influenced the clinical outcomes of patients with aSAH, univariate and multivariate logistic regression analyses were performed. The variables that exhibited significance in the univariate analyses were included in the multivariate analysis. In addition, to reduce the differences in characteristics, except for aneurysm diameter, between the two groups that might have affected outcomes, a case-matched study was conducted.
For baseline variables, summary statistics are presented (frequencies and percentages for categorical data and medians and interquartile ranges (IQR) for continuous data). Fisher's exact test was used for analyzing categorical data, and the Wilcoxon rank-sum test was used for analyzing continuous data. Patient selection for the case-matched study was performed by employing the propensity-score matching method with a Greedy 5-to-1 Digit-Matching algorithm for clinical factors.
All comparisons were planned, and all tests were two-sided. P-values of <0.05 were considered statistically significant. All statistical analyses were performed using JMP (Japanese version 12 for Windows; SAS Institute Inc., Cary, NC, USA).
Results
A total of 605 consecutive patients with SAH were identified. After excluding 51 patients whose SAH were caused by dissection, 27 patients with fusiform aneurysms, 8 patients who were treated using PAO, 13 patients who were treated >14 days after onset, 1 patient with an arteriovenous malformation-related aneurysm, and 36 patients in whom detailed information was not obtained, 469 patients were included in this study (Fig. 1). Of the 469 patients, 165 did not undergo a CT scan at >30 days after the initial procedure. Thus, 304 patients underwent repeated CT scans, including at least one at >30 days after the initial procedure. They were included in the calculation of the frequency of rebleeding at >30 days after the initial procedure. Postdischarge aneurysm evaluation was performed in 258 patients (55.0%).
Fig. 1.
Schematic drawing of the patient selection method.
Table 1 summarizes the clinical characteristics of all patients and the two groups. Patients whose aneurysms had a maximum diameter of ≥10 mm were placed in group L (large, 73 patients), and those whose aneurysms had a maximum diameter of <10 mm were included in group S (small, 396 patients). The median age was significantly higher in group L than in group S (71.0 vs. 65.0, p = 0.0105). The proportion of patients with WFNS grade 1, 2, or 3 at admission was significantly lower in group L than in group S (57.5% vs. 73.5%, p = 0.0075). There were no patients with giant aneurysms (>25 mm). The dome/neck ratio (2.00 vs. 1.47) and aspect ratio (1.50 vs. 1.34) were significantly higher in group L than in group S (p < 0.0001 and p = 0.0105, respectively). Blebs, ICH, and intra-aneurysmal thromboses were significantly more common in group L than in group S (p = 0.0176, p = 0.0458, and p = 0.0107, respectively). Adjunctive techniques were used more frequently in group L than in group S (79.5% vs. 55.3%, p < 0.0001).
Table 1.
Summary of the clinical characteristics of 469 patients in whom aneurysmal SAH was treated with interventional radiology
| Total | Group L | Group S | P-value | |
|---|---|---|---|---|
| No. of patients | 469 | 73 | 396 | |
| Age, years | ||||
| Median | 67.0 | 71.0 | 65.0 | 0.0105 |
| IQR | 54.0-77.0 | 58.0-81.5 | 52.0-75.0 | |
| Sex, female | 337 (71.9%) | 57 (78.1%) | 280 (70.7%) | 0.2568 |
| WFNS grade 1-3 | 333 (71.0%) | 42 (57.5%) | 291 (73.5%) | 0.0075 |
| mRS score before onset, 0-2 | 454 (97.0%) | 69 (94.5%) | 385 (97.5%) | 0.2496 |
| Location of ruptured AN, anterior | 379 (80.8%) | 52 (71.2%) | 327 (82.6%) | 0.0343 |
| ACA | 160 (34.1%) | 12 (16.4%) | 148 (37.4%) | |
| Pcom | 131 (27.9%) | 26 (35.6%) | 105 (26.5%) | |
| Distal ICA | 29 (6.2%) | 3 (4.1%) | 26 (6.6%) | |
| Proximal ICA | 17 (3.6%) | 2 (2.7%) | 15 (3.8%) | |
| MCA | 39 (8.3%) | 9 (12.3%) | 30 (7.6%) | |
| BA | 62 (13.2%) | 17 (23.3%) | 45 (11.4%) | |
| VA | 31 (6.6%) | 4 (5.5%) | 27 (6.8%) | |
| AN maximum size, mm | ||||
| Median | 5.7 | 12.0 | 5.2 | |
| IQR | 4.0-7.8 | 11.0-13.9 | 3.7-6.8 | |
| Dome/neck ratio | ||||
| Median | 1.54 | 2.00 | 1.47 | <0.0001 |
| IQR | 1.23-2.06 | 1.50-2.67 | 1.21-1.99 | |
| Aspect ratio | ||||
| Median | 1.36 | 1.50 | 1.34 | 0.0105 |
| IQR | 0.92-1.81 | 1.03-2.25 | 0.87-1.77 | |
| Bleb, yes | 331 (70.6%) | 60 (82.2%) | 271 (68.4%) | 0.0176 |
| ICH, yes | 55 (11.8%) | 14 (19.2%) | 41 (10.4%) | 0.0458 |
| IVH, yes | 139 (29.6%) | 27 (37.0%) | 112 (28.3%) | 0.1626 |
| Intra-aneurysmal thrombosis | 10 (2.1%) | 5 (6.8%) | 5 (1.3%) | 0.0107 |
| Adjunctive technique, yes | 277 (59.1%) | 58 (79.5%) | 219 (55.3%) | <0.0001 |
| Balloon | 245 (52.2%) | 43 (58.9%) | 202 (51.0%) | |
| Double catheter | 44 (9.4%) | 23 (31.5%) | 21 (5.3%) | |
| Stent | 23 (4.9%) | 5 (6.8%) | 18 (4.5%) | |
| Follow-up period, median (days) | 60.5 (25.8-551.0) | 60 (23-415.5) | 61 (26.5-567.5) | 0.7106 |
ACA, anterior cerebral artery; AN, aneurysm; BA, basilar artery; ICA, internal cerebral artery; ICH, intracerebral hemorrhage; IQR, interquartile range; IVH, intraventricular hemorrhage; MCA, middle cerebral artery; mRS, Modified Rankin Scale; Pcom, posterior communicating artery; SAH, subarachnoid hemorrhage; VA, vertebral artery; WFNS, World Federation of Neurosurgical Societies
The patients' outcomes are summarized in Table 2. The proportion of CO cases was significantly lower in group L than in group S (15.1% vs. 33.6%, p = 0.0014). There were no significant differences between the two groups in the frequencies of periprocedural hemorrhagic events (p = 0.7837) or ischemic events (p = 0.5617). The total incidence of rebleeding after treatment was significantly higher in group L than in group S (6.8% vs. 2.0%, p = 0.0372). There were two patients in group L and seven patients in group S who experienced rebleeding within 30 days of treatment, and this was not significantly different (p = 0.6359). Conversely, three patients in group L and one patient in group S experienced rebleeding after >30 days, and the difference between the groups was significant (p = 0.0177). A patient in group S experienced rebleeding at 96 days after the initial treatment, and three patients in group L experienced rebleeding at 230, 1194, and 1366 days after the initial treatment. Aneurysm evaluation was possible in a total of five rebleeding patients (two patients in group S and three patients in group L). In two patients in group S, the aneurysm BF was seen after initial treatment and rebleeding occurred within 30 days without increasing of blood flow into the aneurysm. Conversely, in three patients in group L, NR was present after initial treatment and rebleeding occurred after more than 30 days with progression of NR. The percentage of patients who required retreatment for aneurysms did not differ significantly between the groups (p = 0.1062). Twenty-three patients were treated with CE, and six patients were treated with clipping. The median interval between the first and second procedures was 369.5 days in group L and 105 days in group S. It was significantly longer in group L (p = 0.0146).
Table 2.
Outcomes of 469 patients in whom aneurysmal SAH was treated with interventional radiology
| Total | Group L | Group S | P-value | |
|---|---|---|---|---|
| Result of occlusion | ||||
| BF | 150 (32.0%) | 35 (47.9%) | 115 (29.0%) | |
| NR | 175 (37.3%) | 27 (37.0%) | 148 (37.4%) | |
| CO | 144 (30.7%) | 11 (15.1%) | 133 (33.6%) | 0.0014 |
| Periprocedural hemorrhagic events | 27 (5.8%) | 3 (4.1%) | 24 (6.1%) | 0.7837 |
| Ischemic events | 57 (12.2%) | 7 (9.6%) | 50 (12.6%) | 0.5617 |
| Rebleeding after procedure | 13 (2.8%) | 5 (6.8%) | 8 (2.0%) | 0.0372 |
| within 30 days | 9 (1.9%) | 2 (2.7%) | 7 (1.8%) | 0.6359 |
| later than 30 days | 4/304 (1.3%) | 3/53 (5.7%) | 1/251 (0.4%) | 0.0177 |
| Cranial nerve palsy | 3 (0.6%) | 0 | 3 (0.8%) | 1.0000 |
| Retreatment for aneurysm | 29 (6.2%) | 8 (11.0%) | 21 (5.3%) | 0.1062 |
| Time between 1st and 2nd treatments (days) | 192 (29-370) | 369.5 (215.0-691.0) | 105.0 (18.0-287.0) | 0.0146 |
| mRS score @ discharge | ||||
| 0-2 | 263 (56.1%) | 28 (38.4%) | 235 (59.3%) | 0.0012 |
| 3-5 | 165 (35.2%) | 31 (42.5%) | 134 (33.8%) | |
| 6 | 41 (8.7%) | 14 (19.2%) | 27 (6.8%) | 0.0023 |
BF, body filling; CO, complete occlusion; mRS, Modified Rankin Scale; NR, neck remnant; SAH, subarachnoid hemorrhage
The proportion of patients that had an mRS score of 0-2 at discharge was significantly lower in group L than in group S (38.4% vs. 59.3%, p = 0.0012) and that of patients with an mRS score of 6 at discharge was significantly higher in group L than in group S (19.2% vs. 6.8%, p = 0.0023). In the multivariate analyses (Table 3), the independent risk factors for poor outcomes were found to be higher age (odds ratio [OR]: 162.62, p < 0.0001), a poor WFNS grade (OR: 8.73, p < 0.0001), ICH (OR: 4.66, p = 0.0001), IVH (OR: 2.97, p < 0.0001), periprocedural hemorrhagic or ischemic events (OR: 3.55, p < 0.0001), and rebleeding within 30 days (OR: 64.19, p = 0.0003). Aneurysm size was not associated with poor outcomes (p = 0.1849).
Table 3.
Results of the univariate and multivariate analyses of the risk factors associated with poor outcomes in patients with aneurysmal subarachnoid hemorrhages
| Outcome at discharge | Univariate | Multivariate | ||||
|---|---|---|---|---|---|---|
| mRS score:
0-2 (good) |
mRS score:
3-6 (poor) |
OR (95% CI) | P-value | OR (95% CI) | P-value | |
| No. of patients | 263 | 206 | ||||
| Age, median (IQR) | 61 (48-69) | 73 (63-82) | 68.09 (24.17-203.65) | <0.0001 | 162.62 (42.26-692.42) | <0.0001 |
| WFNS grade 4-5 | 31 (11.8%) | 105 (51.0%) | 7.78 (4.95-12.53) | <0.0001 | 8.73 (4.89-16.14) | <0.0001 |
| Location of ruptured AN, anterior | 211 (80.2%) | 168 (81.6%) | 1.09 (0.69-1.74) | 0.7173 | ||
| AN maximum size, ≥10 mm | 28 (10.6%) | 45 (21.8%) | 2.35 (1.41-3.95) | 0.0009 | 1.60 (0.80-3.23) | 0.1849 |
| Bleb | 184 (70.0%) | 147 (71.4%) | 1.07 (0.72-1.60) | 0.7416 | ||
| ICH | 12 (4.6%) | 43 (20.9%) | 5.50 (2.90-11.19) | <0.0001 | 4.66 (2.09-10.99) | 0.0001 |
| IVH | 40 (15.2%) | 99 (48.1%) | 5.16 (3.37-8.03) | <0.0001 | 2.97 (1.73-5.15) | <0.0001 |
| Intra-aneurysmal thrombosis | 3 (1.1%) | 7 (3.4%) | 3.05 (0.84-14.28) | 0.0924 | ||
| Result of occlusion, NR or BF | 171 (65.0%) | 154 (74.8%) | 1.59 (1.07-2.40) | 0.0225 | 1.54 (0.89-2.70) | 0.1241 |
| Periprocedural hemorrhagic or ischemic events | 30 (11.4%) | 51 (25.2%) | 2.56 (1.57-4.23) | 0.0002 | 3.55 (1.89-6.83) | <0.0001 |
| Rebleeding within 30 days | 1 (0.4%) | 8 (3.9%) | 10.59 (1.92-197.16) | 0.0042 | 64.19 (6.04-1565.68) | 0.0003 |
AN, aneurysm; BF, body filling; CI, confidence interval; ICH, intracerebral hemorrhage; IQR, interquartile range; IVH, intraventricular hemorrhage; NR, neck remnant; OR, odds ratio; WFNS, World Federation of Neurosurgical Societies
Studies of a case-matched subset
To calculate propensity score, age, WFNS grade, the presence/absence of an ICH, and the presence/absence of an IVH were used, all of which had p-values < 0.05. After all of the propensity-score matches had been performed, we compared baseline characteristics between the two groups. Ultimately, 146 patients (73 in each group) were selected. The p-values after matching were over 0.05 for all clinical factors, except the geometric indices: aneurysm size and dome/neck ratio (Supplemental Table 1).
The ratio of CO was also significantly lower in group L than in group S after case-matching (15.1% vs. 39.7%, p = 0.0014). Conversely, the ratios of periprocedural hemorrhagic events, ischemic events, rebleeding, retreatment, mRS 0-2, and mRS 6 were not significantly different (Supplemental Table 2).
Discussion
In this study, the clinical outcomes of CE for aSAH were significantly worse in patients with large aneurysms than in those with small aneurysms. The proportion of patients with mRS scores of 0-2 at discharge was significantly lower and the mortality rate was significantly higher in group L than in group S. However, clinical characteristics, such as age, the WFNS grade, the presence/absence of ICH, and the presence/absence of IVH, which may strongly influence outcomes, differed significantly between the two groups. Multivariate logistic regression analysis revealed that higher age, a poor WFNS grade, ICH, IVH, periprocedural hemorrhagic or ischemic events, and rebleeding were associated with unfavorable outcomes, but aneurysm size was not. Furthermore, after propensity-score matching, both incidence of mRS 0-2 and mortality rate did not differ significantly between the two groups. A previous study reported that aneurysm size affected the outcomes of surgical clipping.7) Conversely, the influence of aneurysm size on the outcomes of EM is controversial. In the ISAT, age, the WFNS grade, and aneurysm location were found to be associated with outcomes, but aneurysm size was not.1) Similarly, a prospective cohort study of EM for unruptured giant aneurysms reported that aneurysm size was not associated with mortality rate.8) Conversely, a retrospective study of 334 cases of EM for large or giant aneurysms, which included both ruptured and unruptured aneurysms, reported that a larger aneurysm size was one of the negative independent predictors of favorable outcomes.3) Our case-matched study indicates that the outcomes of EM for aSAH may not be affected markedly by aneurysm size, at least in the short-term, if the aneurysm measures <25 mm in diameter.
The occurrence of periprocedural hemorrhagic or ischemic events is a predictor of unfavorable outcomes, but there were no significant differences in the incidence rates of these events between the two groups in this study. Hemorrhagic complications occurred in 4.1% of cases, and ischemic events occurred in 9.6% of cases in group L. Previous studies of EM for aSAH reported that the frequency of complications was 10.9%-13.1%.9-11) This frequency was not so different from that seen in our group L. Accordingly, the influence of aneurysm size on the occurrence of periprocedural hemorrhagic or ischemic events after EM might be low. These may be because there is not much difference in the difficulty of the procedure depending on the size of the aneurysm, unlike clipping.
In this study, rebleeding after EM also affected treatment outcomes. The incidence of rebleeding after the initial procedure was significantly higher in group L than in group S (6.8% vs. 2.0%, p = 0.0372). In particular, the incidence rate of rebleeding within 30 days did not differ significantly between the groups (2.7% vs. 1.8%, p = 0.6359), but rebleeding after >30 days was significantly more common in group L (5.7% vs. 0.4%, p = 0.0177). In the aneurysm of patients evaluated after initial treatment, small aneurysm rebleeding tended to occur in the early phase without coil compaction, but large aneurysm rebleeding tended to occur in the chronic phase with coil compaction. In large aneurysms, the initial treatment often resulted in incomplete occlusion and coil compaction was more likely to occur. Long-term close follow-up may be needed in patients with large aneurysms, and early retreatment is recommended if an increase in blood flow into the aneurysm is observed.
In this study, adjunctive techniques were used more frequently in group L than in group S (79.5% vs. 55.3%, p < 0.0001). In particular, the balloon catheter technique was used in more than half of all cases. Conversely, the stent-assisted technique was only used in 4.9% of cases. The frequency of retreatment was higher in group L than in group S (11.0% vs. 5.3%), although the difference was not significant (p = 0.1062). In previous studies, it was reported that the frequency of retreatment increased as the aneurysm size increased.12,13) Subanalysis of the ISAT revealed that younger age, a larger aneurysm size, and incomplete occlusion were associated with retreatment.2) In the latter study, retreatment was performed in 13 (16%) of 83 patients with large aneurysms.2) Similarly, in a retrospective cohort study of 35 cases of large ICA aneurysms, 11 patients (31%) required retreatment within one year of the initial EM.11) In addition, Chalouhi et al. reported that retreatment was performed in 85 of 260 (32.7%) patients with large or giant aneurysms.3) In some studies, it was reported that the stent-assisted technique could reduce recurrence.3,14) However, a meta-analysis revealed that the periprocedural complications rate was significantly higher among patients treated with stent-assisted CE than among those treated without stent (20.2% vs. 13.1%; relative risk: 1.70; 95% confidence interval: 1.36-2.11).11) In addition, another meta-analysis revealed that 20.8% of patients with aSAH that were treated with stent-assisted CE experienced periprocedural complications.15) Accordingly, in the acute SAH period, we consider that CE without stent is better for preventing periprocedural complications. If an aneurysm cannot be completely occluded, additional treatment, such as stent-assist coiling, FD placement, or direct surgery, should be considered to reduce the risk of rebleeding after the acute period.
Limitations
The major weakness of the present study was that it was retrospective. The characteristics of the patients are considered to have a major influence on treatment selection. One approach to reducing or eliminating the effect of treatment selection bias and confounding effects is to use propensity-sore matching. Therefore, in the present investigation, a case-matched study was also conducted. Nevertheless, because this was a retrospective study, biases could not be completely eliminated.
Moreover, because this was a multicenter study, there were several differences, i.e., in treatment strategies, the timing of examinations after treatment, the imaging modalities used, and the methods used to evaluate treatment results, among the participating institutions. In addition, long-term follow-up was not carried out in many patients with mRS scores of 4-5 because they were transferred to long-term care facilities. A randomized controlled trial, including surgical treatment, is required to examine the efficacy and safety of endovascular treatment for large aneurysms.
Conclusion
The frequencies of higher age, a poor WFNS grade, and ICH were significantly higher in patients with large aneurysms than in patients with small aneurysms. The frequency of CO was significantly lower and that of rebleeding was significantly higher among the patients with large aneurysms than among those with small aneurysms. Multivariate analysis indicated that higher age, a poor WFNS grade, ICH, IVH, periprocedural hemorrhagic or ischemic events, and rebleeding were found to be significant independent predictors of unfavorable outcomes. However, aneurysm size was not associated with unfavorable outcomes. Furthermore, propensity-score matching showed that the rate of favorable outcome and mortality rate were not significantly different between the two groups. The outcomes of EM for aSAH may not be affected markedly by aneurysm size.
Conflicts of Interest Disclosure
None of the authors have any conflicts of interest.
Supplementary Material
References
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