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Original research
Is a high initial World Federation of Neurosurgery (WFNS) grade really associated with a poor clinical outcome in elderly patients with ruptured intracranial aneurysms treated with coiling?
  1. Christina Iosif1,
  2. Federico Di Maria1,
  3. Nader Sourour1,
  4. Vincent Degos2,
  5. Fabrice Bonneville3,
  6. Alessandra Biondi4,
  7. Betty Jean5,
  8. Chantal Colonne6,
  9. Aurelien Nouet6,
  10. Jacques Chiras1,
  11. Frédéric Clarençon1
  1. 1Department of Neuroradiology, Pitié-Salpêtrière University Hospital, Paris, France
  2. 2Department of Anaesthesiology, Pitié-Salpêtrière University Hospital Paris, France
  3. 3Department of Neuroradiology, University Hospital of Toulouse, France
  4. 4Department of Neuroradiology, University Hospital of Besançon, France
  5. 5Department of Neuroradiology, University Hospital of Clermont-Ferrand, France
  6. 6Department of Neurosurgery, Pitié-Salpêtrière University Hospital, Paris, France
  1. Correspondence to Dr Christina Iosif, Department of Neuroradiology, Pitié-Salpêtrière University Hospital, 47 Bd de l'Hôpital, Paris 75013, France; christina.iosif{at}gmail.com

Abstract

Background Coiling of ruptured intracranial aneurysms in elderly patients remains debatable in terms of technical feasibility and clinical outcome.

Aims In this observational cohort study we aimed to assess the technical feasibility, complication profile and clinical outcomes of elderly patients with subarachnoid hemorrhage (SAH) treated with endovascular therapy.

Methods The study included 59 consecutive patients (47 women) aged ≥70 years (mean age 76 years, range 71–84) admitted to our institution with SAH from January 2002 to July 2011. The patients were treated for 66 aneurysms (regular coiling: n=62 (94%), balloon-assisted technique: n=2 (3%), stent and coil technique: n=2 (3%)). World Federation of Neurosurgery (WFNS) grade at admission was 1 in 13 patients, 2 in 23 patients, 3 in 8 patients, 4 in 11 patients and 5 in 4 patients. We analysed data by univariate and multivariate statistical analyses with an emphasis on the initial clinical situation, complications and clinical outcome.

Results The technical success rate was 98% with a procedure-related deficit rate of 10% and procedure-related death rate of 5%. The Glasgow Outcome Scale score at 6 months was 1 in 15 patients (25.4%), 2 in 8 patients (13.6%), 3 in 14 patients (23.7%), 4 in 11 patients (18.6%) and 5 in 11 patients (18.6%). Patients admitted with a high initial WFNS grade did not differ statistically in terms of clinical outcome. The final clinical outcome was not significantly correlated with age, initial Fisher score or procedure-related complications.

Conclusions Endovascular treatment of elderly patients with ruptured cerebral aneurysms is feasible, safe and beneficial regardless of the presenting WFNS score.

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Background

Over the past two decades the endovascular treatment of ruptured intracranial aneurysms has been shown to be effective in reducing the morbidity and mortality of aneurysmal subarachnoid hemorrhage (SAH).1 ,2 However, embolization of elderly patients (age ≥70 years) with aneurysmal SAH remains questionable as advanced age may hamper the clinical outcome, especially in patients admitted with a poor World Federation of Neurosurgery (WFNS) grade.3 Moreover, in elderly patients, comorbidities such as cardiac or pulmonary failure can contribute to complications during the period in the ICU and consequently increase the morbidity and mortality rates. Furthermore, these patients often have tortuous vessels and atherosclerotic lesions resulting in additional technical difficulties regarding endovascular treatment and may be responsible for higher rates of thromboembolic complications.4

Despite the above mentioned limitations for the treatment of elderly patients with ruptured aneurysms, some considerations can be made in favor of the treatment of such patients. Over the last few decades an increase in life expectancy has led to an increase in the percentage of individuals aged ≥70 years with active social and personal roles. In Western countries, patients aged ≥70 years now represent 12% of the general population.5 ,6 As aneurysms tend to rupture more as age progresses, the number of elderly patients who will be admitted with aneurysmal SAH is likely to increase in the future.

Even though surgical treatment can be a valuable option,7–9 poor general condition of elderly patients may represent a limitation for this treatment choice. The improvement of endovascular devices, especially conformable guiding catheters, has reduced the risk of embolization in elderly patients with tortuous and atheromatous vessels,10 thus adding importance to endovascular procedures in everyday clinical practice.

We present our experience with coil embolization in patients aged ≥70 years admitted for a ruptured intracranial aneurysm, giving emphasis to the clinical outcome of patients presenting with a poor initial WFNS grade.

Methods

We retrospectively reviewed our database of 1024 consecutive patients admitted to our institution with aneurysmal SAH from January 2002 to July 2011. Among these patients, 87 were aged ≥70 years and, of these, 59 were treated by endovascular means and were included in the study (figure 1). No patients were excluded from treatment on the basis of age or high WFNS score.

Figure 1

Flow chart summarising the demographic characteristics of the patients involved in the study. GOS, Glasgow Outcome Scale; Pts, patients; SAH, subarachnoid hemorrhage; Tx, treatment.

We extracted the personal, clinical and imaging data from the database and cross-checked them with the electronic database of our ICU. All the angiographic data were reviewed in consensus by two interventional neuroradiologists (CI and FC).

Endovascular procedures

All embolisation procedures were performed in a biplane angiosuite (Axiom Artis; Siemens, Erlangen, Germany).

Patients were treated under general anesthesia and the preferred access was femoral whenever possible. We used a straightforward strategy favoring regular coiling over balloon remodeling and stent-assisted coiling, which were performed only if judged to be the only option.

A bolus of heparin (50 IU/kg) was usually administered after the placement of the first coil and effective anticoagulation was maintained throughout the whole procedure (activated clot time objective 2–3 times baseline). Total exclusion, neck remnant or persistent filling of the aneurysm were evaluated by control digital subtraction angiography (DSA). The immediate angiographic result was categorized according to the Roy and Raymond classification as follows: complete occlusion, residual neck or residual circulating aneurysm.11 ,12

Evaluation of procedure difficulties

All difficulties with the procedures were documented prospectively by the operator and were included in the written report. They were also re-evaluated retrospectively by two interventional neuroradiologists (CI and FC) who revised the angiograms for the purposes of the study.

Our classification of the procedure difficulties concerned the presence or absence of marked vessel tortuosities, kinking or stenosis of parent vessels, atheromatous changes of parent vessels, the presence of anatomic variations that were causing additional difficulty and a wide aneurysm neck.

Complications

Complications were classified into two main categories: per-procedural complications, which occurred during or immediately after the procedure, and post-procedural complications. Per-procedural complications included spontaneous per-procedural rebleeding, perforation and thrombosis. Post-procedural complications included the following three main subcategories:

  1. Delayed procedure-related complications (ischemic stroke related to the procedure, re-rupture of treated aneurysm).

  2. Delayed complications related to the aneurysmal SAH (hydrocephalus, non-ischemic vasospasm, ischemic vasospasm).

  3. Complications unrelated either to the procedure or to the haemorrhage (pulmonary embolism, myocardial infarction, other irrelevant to the aneurysm rupture conditions).

Clinical and imaging follow-up

Clinical outcome was evaluated at 6 months by intensive care neurovascular anesthesiologists and was documented by means of the Glasgow Outcome Scale (GOS).13–15

Imaging follow-up was performed in 28/44 patients (64%) who survived during the follow-up period (mean=9±16 months, median 12, range 3–60). Patients were followed either exclusively by DSA (9/28, 32%) or by alternating DSA and three-dimensional time of flight MR angiography (MRA) (8/28, 28%) with a 3T MRI system (Siemens Healthcare, Erlangen, Germany). It is noteworthy that 11/28 patients (40%) were followed exclusively by MRA, given the fact that MRA is much safer in certain patient groups and the value of the method is nowadays comparable to DSA for coiled aneurysms.16 ,17 The classification used was the abovementioned Roy and Raymond scale.11 ,12

Statistical analysis

The sample was statistically analyzed by descriptive statistics after verifying normality by the De Agostino–Pearson test for normal distribution.

Two groups of patients were subsequently identified according to good or poor clinical outcome (good outcome was defined as GOS 4 and 5; poor as GOS 1, 2 and 3). The variables tested were Fisher grade, initial WFNS, technical difficulty, per-procedural complications, post-procedural complications, age, delay from SAH to treatment and aneurysm size.

Predictive factors for clinical outcome were statistically analyzed by the creation of 2×2 tables for OR and the Fisher exact test calculation for dichotomous variables. Continuous variables (age) were compared using the Mann–Whitney test.

The two groups were statistically compared by logistic regression (after a Hosmel and Lemeshaw test) in order to determine parameters that could be related to good or poor outcome using one-way MANOVA.

The statistical analysis was performed with MedCalc statistical electronic software (Medcalc software, Mariakerke, Belgium). The level of statistical significance was p≤0.05.

Results

Of the 66 aneurysms found in our sample, 64 (97%) were successfully embolized. We failed to embolize two aneurysms (3% treatment failure) owing to technical difficulties. Large neck and vascular tortuosities were the main vascular difficulties encountered in this series of patients.

Patient demographics

The sample population consisted of 59 patients (47 women, 12 men) of mean±SD age 76±3.82 years (range 71–84). SAH was confirmed by plain CT in all but one case in whom lumbar puncture was performed to confirm the diagnosis.

Clinical and imaging presentation

The initial WFNS grade was 1 in 13 patients (22.0%), 2 in 23 patients (39%), 3 in 8 patients (13.6%), 4 in 11 patients (18.6%) and 5 in 4 patients (6.8%). Fisher grade at the presentation CT scan was 1 in 1 patient (1.7%), 2 in 8 patients (13.6%), 3 in 7 patients (11.9%) and 4 in 43 patients (72.9%). Thus, 15 patients (25%) presented with a high WFNS score (grade 4 and 5) and about 73% had a high Fisher grade (grade 4). These WFNS scores represent the clinical situation before embolization; after embolization the WFNS scores were unchanged in 51 of the 59 patients (86.4%).

Aneurysm characteristics

We identified 66 aneurysms in our sample population, all of which presented with a maximum diameter up to 15 mm (mean±SD 5.7±2.6 mm, range 2–14). The mean ± SD neck diameter was 2.74±1.36 mm (median 2.40). Fifteen of the 66 aneurysms (22.7%) had a large neck, defined as >4 mm or a dome-to-neck ratio of <2. Fifty-six of the aneurysms (85%) were located in the anterior vascular system and 10 (15%) were located in the vertebrobasilar system. The most frequent localization was the anterior communicating artery (ACom, 27/66 aneurysms, 40.9%) followed by the posterior communicating artery (10/66 aneurysms, 15.2%).

Procedures

Thirty-nine patients (66.1%) were treated within the first 24 h after the haemorrhage, eight patients (13.6%) were treated between 24 and 48 h, four patients (6.8%) received treatment between 48 and 72 h and the remaining eight patients (13.6%) were treated after the first 72 h.

In four patients multiple aneurysms were coiled (two embolized aneurysms in three patients, three aneurysms in one patient), all of them in the same session in the early acute phase.

All patients were treated under general anesthesia. The femoral approach was used in all but one case (58/59, 98%). In the remaining case (1/59, 2%) a direct carotid artery puncture was chosen after unsuccessful embolization attempts via the femoral approach due to the tortuosity of the major vessels.

We used a standard 6 Fr sheath whenever possible with a 6 Fr Envoy guiding catheter (Cordis, Warren, New Jersey, USA). In cases with major stenosis at the origin of the internal carotid artery, the guiding catheter was left below the stenosis. In all other arterial vascular tortuosities we used a long sheath (6 Fr Destination; Terumo Medical Corporation, Somerset, New Jersey, USA) that was navigated in the distal segment of the common carotid artery followed by a flexible guiding catheter (Fargo; Balt, Montmorency, France) or Neuron (Penumbra, Alameda, California, USA) to bypass the tortuosities.

A balloon remodeling technique was used in two of the 66 aneurysms (3%). In two cases a stenting technique was performed in the acute phase. The first case was a ‘bail out’ stenting due to coil protrusion in the parent artery by means of a Neuroform-3 stent of 4.5/20 mm (Stryker Neurovascular, Fremont, California, USA). In the second case a stent-assisted coiling technique was performed with the aid of two Enterprise stents (Cordis Neurovascular, Miami Lakes, Florida, USA), 4.5/28 mm and 4.5/22 mm, respectively. In both cases dual antiplatelet therapy was started during the procedure (250 mg acetylsalicylic acid intravenously and six doses of clopidogrel 75 mg in the nasogastric catheter). Aspirin was continued orally for the following 6 months and clopidogrel for the following 3 months.

Clinical outcome

At the 6-month clinical follow-up the GOS score was 1 in 15 patients (25.4%), 2 in 8 patients (13.6%), 3 in 14 patients (23.7%), 4 in 11 patients (18.6%) and 5 in 11 patients (18.6%) (table 1). Overall, at 6 months 22 patients (37.2%) had a good clinical outcome and 15 patients (25.4%) had died.

Table 1

Clinical outcome of patients at 6-month follow-up

Of  the 15 patients admitted with a high initial WFNS score, 3 (20%) had a favorable evolution (GOS 4 or 5) and, of the 44 patients admitted with a low initial WFNS score, 18 (41%) had a favorable evolution. The difference between the two groups was not statistically significant (Fisher exact test, p=0.18), which means that, for this study population, both favorable and unfavorable initial clinical grades evolved similarly when treated by endovascular means. The final clinical outcome did not show a statistically significant correlation with age, initial Fisher score or procedure-related complications.

Angiographic outcome

The initial angiographic result was complete occlusion in 34 (53%) of the treated aneurysms, residual neck was observed in 24 (37.5%) aneurysms and residual aneurysm in 6 (9.5%). Final follow-up was undertaken in 34/49 (70%) of the coiled aneurysms in the patients who survived during the follow-up period, of which 17 (50.0%) showed complete occlusion, 14 (40.0%) had a residual circulating neck and 3 (9%) were still circulating.

The retreatment rate was 5% (3 patients) during the follow-up period with a mean ± SD delay of 3.2 ± 2.2  months (median 3). Initially a fourth patient was planned for retreatment but, on the day of the intervention, the aneurysm was no longer circulating.

Postoperative and procedure-related complications

There were no complications during the procedure in 46 patients (78%), spontaneous per-procedural rebleeding occurred in 2 patients (3.4%), perforation during the procedure occurred in 4 (6.8%) and thromboembolic complications were observed during the procedure in 7 cases (11.9%). No complications were reported for the retreatment coiling procedures.

Coiling was continued successfully in all cases and thromboembolic complications were successfully resolved during the procedure. Nevertheless, in four of the seven patients (6.8%) who presented with per-procedural thrombus an ischemic complication occurred later during the post-procedural period.

During the postoperative period 33 patients (55.9%) were free of complications. Hydrocephalus developed in 12 patients (20.3%). Six patients (10.1%) developed vasospasm which was effectively resolved with chemical dilation (intra-arterial nimodipine±milrinone), in another eight patients (13.7%) ischemic stroke due to vasospasm was inevitable, although systemic and intra-arterial chemical vasodilation as well as mechanical balloon vasodilation were performed in two cases.

In 4/59 cases (6.7%), although a procedure-related complication was initially reported, no deficit was found at 6 months. Procedure-related neurological deficit was permanent in 10% of cases (six patients in our sample) and 3/59 patients (5%) died of procedure-related causes. Overall, the symptomatic procedure-related rate of complications was 15% (9/59 patients) (table 2).

Table 2

Clinical outcome in relation to procedure-related complications

Rebleeding occurred in two patients (3.4%) during the whole post-treatment follow-up period and was fatal in one case. The first case was a patient with an ACom aneurysm implanted mainly on the left A1–ACom segment which was coiled at day 10 due to unstable clinical conditions, with severe vasospasm of the left A1 and A2 segments, in which we considered a coil that would not bulge in order to avoid vasospasm-related ischemic complications. The second case was a patient who was treated on day 35 with stent-assisted coiling for a vertebral junction aneurysm for which a complementary coil was programmed some days following the first intervention. However, on the initial angiogram during the second intervention the residual aneurysm was found to be spontaneously occluded so we did not proceed with the additional treatment. The patient was receiving dual antiplatelet therapy with aspirin and clopidogrel for 3 months following the procedure when he rebled. He survived with a GOS score of 3 at 6 months (initial WFNS grade 2).

Discussion

‘Elderly’ is a controversial term in medicine since no real consensus exists on age cut-off. In this study we chose a cut-off of 70 years,9 taking into account the increase in life span throughout the last decades as well as the improvement in the quality of life of older people who nowadays remain socially active until the age of ≥70 years.

The dilemma whether or not to treat intracranial aneurysm rupture in atheromatous patients with tortuous vessels and multiple medications is common in everyday practice. The number of patients with contraindications to surgery is not negligible and endovascular approaches may provide a good alternative.

There is now sufficient evidence for the effectiveness of endovascular treatment as far as the risk of rebleeding is concerned in the acute phase of aneurysm rupture.1 ,18 Additionally, there is growing evidence that the endovascular approach is safer in terms of morbidity and mortality than microsurgical clipping for ruptured aneurysms.1 ,19

We found that endovascular treatment was feasible in almost all cases (97%). This result is concordant with the data of previously published series on this topic where it ranges from 92% to 96%.3 ,20 ,21 Although higher than the complication rate reported in the literature for overall endovascular treatment of ruptured intracranial aneurysms (mean 9%, range 2.8–28.6%, in a meta-analysis of 14 studies22), the procedure-related complications recorded in our study (23.7%, 13.6% symptomatic) were within the range of previously published series on endovascular coiling of ruptured intracranial aneurysms in elderly patients (19–22%).3 ,23

Procedure-related mortality in our series (5%) was in all cases related to thromboembolic complications and, although high, was comparable with the other studies on the same topic (range 2–19.5%).3 ,20 The clinical outcome was good (GOS=4 or 5), independently of the initial WFNS score, in 37.2% of the cases. These results are lower than some of the published series in the literature (40–68%).3 ,20 ,21 ,23 This result may be explained by the fact that, in our study, more patients with a poor clinical grade were included than in some other series3 and, in some series, patients aged between 60 and 70 years were also included.23

One strength of our series is that, unlike some previously published studies,3 ,20 it involved only patients with ruptured aneurysms. Moreover, the proportion of patients with a high WFNS grade was high in our series (15/59, 25.4%) compared with some other large series on the same topic.3

In patients with good initial clinical status (WFNS grade 1–3), GOS was good (4 or 5) in 41% of cases whereas a good clinical outcome was reported in 20% of patients admitted with a poor clinical grade (WFNS 4 or 5). However, this difference was not statistically significant (p=0.18). A possible reason why this study failed to demonstrate a statistically significant result on this matter may be lack of power due to the small sample size. Thus, a prospective study with a larger number of patients, probably multicenter, is necessary to obtain sufficient evidence.

Overall, our results tend to show that clinical outcome is not significantly dependent on the initial clinical grade. These results are different from those of previously published series on the topic in which a poor initial clinical grade was significantly associated with a poor clinical outcome.3 ,20 ,23 ,24

In our series, a satisfactory immediate angiographic result (ie, complete aneurysm occlusion or residual neck) was achieved in 90.5% of the cases. On angiographic follow-up the results remained stable or improved in most cases (79.5%); in 5% of cases retreatment of a recanalization was performed during the follow-up period without complication. These results are within the range of previously published series on this topic.20

Although evidence exists in the literature in favor of significant long-term recanalization rates with coiling,11 in elderly patients this is not as important as in young patients. It is noteworthy that two patients who experienced rebleeding were classified in the post-procedural evaluation as having a small residual neck or an aneurysm still circulating but with complete occlusion on angiography 3 days after coiling.

In our series the patients who rebled were either receiving dual antiplatelet therapy or had a satisfactory angiographic outcome. On the other hand, patients with incomplete angiographic occlusion (ie, residual circulating aneurysm) did not rebleed and the angiographic outcome was stable during the follow-up period.

The limitations of our study are the absence of a control cohort (patients aged <70 years) for comparison, as well as the fact that this is a single-centre and retrospective cohort with a limited number of patients. Furthermore, the decade over which the patients were recruited has seen the development of endovascular technology and procedural complications rates may be lower with the current generation devices.

Nevertheless, until a prospective double-blind study is published, we think that our experience may be helpful when dealing with the dilemma of whether or not to treat elderly patients who should not be seen as hopeless cases but as individuals who could benefit from a treatment which is feasible, despite the added difficulties of this age group.

Conclusions

Although technical difficulties may be more frequent than in younger patients, endovascular treatment of ruptured intracranial aneurysms in patients aged ≥70 years is feasible and beneficial with an acceptable symptomatic complication rate. Advancing age does not seem to hinder the clinical benefit of early endovascular treatment in these cases, even in cases with high initial WFNS and Fisher grades.

References

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Footnotes

  • Contributors All authors contributed significantly to the study.

  • Competing interests None.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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