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Original research
Efficacy of endovascular surgery for ruptured aneurysms with vasospasm of the parent artery
  1. Akira Kurata,
  2. Sachio Suzuki,
  3. Kazuhisa Iwamoto,
  4. Madoka Inukai,
  5. Kuniaki Nakahara,
  6. Kimitoshi Satou,
  7. June Niki,
  8. Makoto Sasaki,
  9. Kiyotaka Fujii,
  10. Shiichi Kan,
  11. Takao Kitahara
  1. Department of Neurosurgery, Kitasato University School of Medicine, Kanagawa, Japan
  1. Correspondence to Dr Akira Kurata, Department of Neurosurgery, Kitasato University School of Medicine, 1-15-1, Minamaku, Sagamihara, Kanagawa, Japan; akirak{at}med.kitasato-u.ac.jp

Abstract

Introduction In the presence of vasospasm it is recommended that surgical clipping for a ruptured aneurysm should be delayed until it disappears, but this may be associated with re-rupture of the aneurysm resulting in a poor outcome. The indications for endovascular coil embolization in such cases are discussed.

Methods Since November 2002, endovascular coil embolization has been used in 18 consecutive patients with ruptured aneurysm with vasospasm of the parent artery ranging from 2 to 28 days (mean 9 days) after the initial subarachnoid hemorrhage. After successful obliteration of the aneurysm, a microcatheter preceded by a guidewire was introduced into the peripheral vessels with vasospasm of the A2 or M2 portions in order to release the vasospasm mechanically.

Results Endovascular procedures were performed successfully in all but one of the cases (94%), resulting in complete occlusion in 14 of 17 patients and mild dilation of the vasospasm in all 17 patients without technical complications or re-rupture of the aneurysm. In the one case of failure because of a tortuous artery, surgical clipping was performed after disappearance of the vasospasm. Cerebral infarction occurred in four patients, but only one correlated with the distribution of catheterization and the neurological deficits had completely disappeared 3 months after the onset.

Conclusion Catheterization of parent vessels in cases of vasospasm is safe for coiling and also mechanically releases vasospasm. Vasospasm of M2 and A2 segments can be treated with microcatheterization only.

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Introduction

Vasospasm appears most frequently 3–15 days after subarachnoid hemorrhage (SAH) and can severely impair cerebral blood flow and even cause cerebral infarcts.1 Surgical clipping during the period of vasospasm should therefore be avoided, particularly in cases with higher Hunt and Hess grades,2 and surgery is therefore recommended earlier3 or later,4–6 before or after the vasospasm period. However, Alaraj et al7 recently reported that patients with SAH with vasospasm treated with endovascular coiling showed no difference in outcome from those treated with surgical clipping. They suggested that surgical clipping and endovascular intervention were equally valid alternatives for the treatment of ruptured aneurysms in patients with existing symptomatic vasospasm.

Wikholm et al8 reported that endovascular surgery itself did not affect the occurrence of vasospasm in patients treated on days 3–14 after the onset of SAH. Murayama et al9 also found that endovascular surgery in patients with acute aneurysmal SAH did not impact on cerebral vasospasm unfavorably compared with conventional surgery (clipping and cisternal drainage). Endovascular coil embolization is a relatively gentle intra-arterial approach, and endovascular treatment combined with balloon angioplasty and/or papaverine infusioin for ruptured aneurysms with vasospasm has been reported to be safe and effective.10–12 However, to our knowledge, endovascular surgery followed by percutaneous transluminal angioplasty with only catheterization of vasospasm has not previously been evaluated. We present the results of a case series of patients who underwent treatment with catheterization alone for vasospasm.

Materials and methods

From November 2002 to November 2010, 253 patients with ruptured saccular aneurysms were treated by endovascular surgery in our department. In our institution, immediately after the diagnosis of SAH all patients undergo sedation with continuous intravenous administration of 1% propofol in a dose of 4–10 mg/kg/h. For cerebral aneurysms with existing vasospasm, direct clipping surgery is avoided, with endovascular surgery being preferred. Our strategy has always been to embolize aneurysms as soon as possible after SAH, even in patients with existing vasospasm. There are surgical indications for endovascular coil embolization, even in a patient who is grade V on the Hunt and Hess (H&H) scale but with evidence of brainstem function. After endovascular obliteration of the aneurysm, intravenous hexahydro-1-(5-isoquinoline sulfonyl) H-1,4-diazepine hydrochloride (fasudil hydrochloride) (Eril; Asahi Kasei Pharma Corporation and Eisai Co Ltd, Tokyo, Japan), 30 mg diluted with 100 ml physiological saline/h, is given three times a day for 14 days as a vasodilating agent for vasospasm in patients with or without clinical symptoms. Intravenous administration of fasudil hydrochloride is standard vasodilating therapy for vasospasm in Japan and its use has previously been reported in detail elsewhere.13 14

Eighteen consecutive patients (9 men, 9 women) with vasospasm underwent endovascular coil embolization during the period of vasospasm (range 2–28 days, mean 9 days, after the initial SAH). A summary of the clinical characteristics of the patients with ruptured aneurysm with vasospasm is shown in table 1. The outcome was defined by the Glasgow Outcome Scale 3 months after onset. The vessel diameter was measured with reference to the diameter of the catheter inserted into the parent artery The degree of cerebral vasospasm was classified as severe if there was >50% narrowing compared with the initial or follow-up angiography in the chronic period, moderate if there was 50% narrowing and mild if there was <50% narrowing.15 Vasospasm was also classified as diffuse if more than one vascular territory was affected and localized if only the vascular territory of the ruptured aneurysm was affected. Symptomatic vasospasm was defined as worsening of the conscious state or development of new neurological symptoms or signs not found to be due to any other causes (eg, hydrocephalus, electrolyte disturbance or infection). All endovascular surgery was performed with an SL-10 microcatheter (Stryker Co, MI, USA) preceded by an Agility 10 soft-tip guidewire (Codman, Inc., MA, USA). In all cases these were introduced into the spasm vessels gently and slowly under maximum magnification using the road mapping function of digital subtraction angiography. After successful obliteration of the aneurysm, a microcatheter preceded by a guidewire was introduced into the peripheral vessels with remaining vasospasm at the A2 or M2 portions in order to release the vasospasm mechanically. In patients in whom severe vasospasm remained in other and/or more peripheral vascular territories, a total dose of 40 mg papaverine hydrochloride was administered into one arterial territory to reduce the vasospasm. Angiographic improvement in the cerebral vasospasm was assessed as the degree of residual stenosis (mild, moderate and severe), which was the same as the pretreatment classification.

Table 1

Clinical characteristics of ruptured aneurysms with vasospasm

Results

Five patients had aneurysms of the middle cerebral artery (MCA), 11 of the anterior cerebral artery (ACA) and two had aneurysms of the vertebral artery. Eight patients experienced only a single episode of SAH and 10 had re-rupture of the aneurysm before treatment. Endovascular surgery was performed at days 2–28 (mean day 10). The reasons for the delay in treatment of >3 days after the hemorrhage were delayed admission in 11 patients (cases 1–3, 8, 9, 12, 14–18), delayed diagnosis in 2 (cases 5 and 11), additional coil embolization in 2 (cases 4 and 13) and uncontrollable intracerebral pressure of grade V on the H&H scale in 2 (cases 6 and 10). H&H grades on admission were I–III in 13 cases, IV in 3 and V in 2 cases. Symptomatic vasospasm was seen in 8 cases and non-symptomatic vasospasm in 6. The remaining 4 cases were undetermined because of poor grade (2 cases grade IV; 2 cases grade V) and sedation. The distribution of the vasospasm was local in 8 cases and diffuse in 10 (table 1).

The endovascular procedure was successful in all but one of the cases, resulting in complete occlusion of the aneurysm in 14 of 17 patients and mild dilation of the vasospasm in all 17 (table 2). In one patient (case 11), endovascular surgery failed because of tortuous parent vessels and clipping surgery was performed after the vasospasm had resolved. Before endovascular surgery the degree of vasospasm was mild in 2 cases, moderate in 9 and severe in 7 cases; after endovascular surgery all but one (case 11) showed mild dilation. No complications relating to the technique were encountered. The success rate with endovascular surgery for ruptured aneurysms with vasospasm of parent arteries was 94% (17/18). In two patients (cases 3 and 8) with severe vasospasm remaining in the bilateral peripheral territory of the ACA, 40 mg papaverine hydrochloride was administered into the ACA to reduce the vasospasm. The preictal neurological condition in case 3 who was bedridden was already poor because of multiple symptomatic old infarctions in the bilateral basal ganglia. Case 8 showed acutely progressive disturbance of consciousness immediately after admission. Brain edema with slight midline shift was already evident on the CT scan before treatment. Intra-arterial papaverine solution, 40 mg/10 ml (0.4%), was administered into the A1 portion in both patients; intra-arterial vasodilator therapy was not used in the other 15 patients. Cerebral infarction occurred in 4 cases (cases 1, 5, 6 and 8), but only one (case 5) had a new episode in the area correlating with the distribution of catheterization and the neurological deficit had completely disappeared 3 months after the onset. In two other patients (cases 1 and 6) infarction occurred in different sites. The remaining patient (case 8) already had brain edema with midline shift on the CT scan and transient anisocoria before treatment. Newly developed infarction after endovascular surgery was therefore seen in three patients (cases 1, 5 and 6). The Glasgow Outcome Scale showed a good recovery in 11 of the 12 patients successfully treated by endovascular surgery with H&H grades I–III on admission, but one patient (case 3) remained in a vegetative state. Two of the patients with H&H grade IV (cases 5 and 13) had a good recovery but the other patient (case 8) died as a result of primary brain damage. Of the two patients with H&H grade V, one (case 6) remained in a vegetative state due to primary damage and the other (case 10) died as a result of sepsis.

Table 2

Results of treatments and outcome

Representative case reports

Case 5

A 32-year-old man presented with headache and vomiting and was admitted to our institution immediately after the onset. SAH was evident on the CT scan which suggested an aneurysmal rupture of the ACA, but this could not be confirmed by angiography (figure 1A). The next day re-rupture occurred, resulting in aggravation of unconsciousness (H&H grade II–IV). A second angiography 7 days after the first again failed to delineate the aneurysm, but a third angiography after 17 days showed an aneurysm at the right A1–A2 junction with vasospasm located in the terminal portion of the right internal carotid artery, ACA (A1–A2 portion) and MCA (M1 portion) (figure1B). Endovascular surgery was recommended. An Excelsior SL-10 microcatheter preceded by an Agility 10 soft-tip guidewire was successfully introduced into the aneurysm which was completely obliterated, followed by catheterization into the peripheral ACA (A2 portion) and M1 portion (figure 1C).

Figure 1

Case 5. (A) Right carotid angiogram showing no aneurysm. (B) Right carotid angiogram showing an aneurysm in the right anterior carotid artery (ACA) with vasospasm involving the right internal carotid artery (arrow), ACA (double arrows) and middle carotid artery (MCA) (asterisk). (C) Right carotid angiogram after embolization and catheterization into the peripheral ACA (A2 portion) and MCA (M1 portion) showing complete obliteration of the aneurysm and mild dilation of the treated spasm: terminal portion of internal carotid artery (arrow), A1 (double arrows), MCA (asterisk).

Case 15

A 54-year-old man developed sudden onset of headache and vomiting and 4 days later became disorientated with aphasia and right hemiparesis. Five days later he was admitted to our institution with H&H grade II. A CT scan on admission showed no remarkable SAH but magnetic resonance FLAIR images showed SAH in the left sylvian fissure. A three-dimensional CT scan showed an aneurysm in the left MCA with vasospasm around the arteries. A perfusion CT scan showed decreased cerebral blood flow and mean transit time in the left cerebral hemisphere. Angiography demonstrated an aneurysm in the left MCA with vasospasm involving the left MCA, ACA and terminal portion of the internal carotid artery (figure 2A). Endovascular surgery was recommended. An Excelsior SL-10 microcatheter preceded by an Agility 10 soft-tip guidewire was successfully introduced into the aneurysm which was completely obliterated, followed by catheterization into the peripheral ACA (A2 portion) and MCA (M2 portion) to dilate the vasospasm (figure 2B). One day after treatment the right hemiparesis improved. A perfusion CT scan showed improvement of cerebral blood flow in the left cerebral hemisphere and mean transit time. No brain infarction occurred and the subsequent clinical course was uneventful. Fourteen days after admission the patient was discharged without neurological symptoms.

Figure 2

Case 15. (A) Left carotid angiogram showing an aneurysm in the left middle carotid artery (MCA) with vasospasm involving the terminal portion of the left internal carotid artery, anterior carotid artery (ACA) (arrow) and MCA (double arrows). (B) Left carotid angiogram after embolization and catheterization into the peripheral ACA (A2 portion) and MCA (M2 portion) showing complete obliteration of the aneurysm and mild dilation of the treated spasm: ACA (arrow), MCA (double arrows).

Discussion

To our knowledge, there have been no reports evaluating the effects of catheterization alone on vasospasm after SAH. In the present series, most of the patients were treated without intra-arterial vasodilator therapy, generally with a good outcome. Wanke et al16 first reported two cases with ruptured aneurysms successfully treated by coil embolization via vasospasm followed by intra-arterial vasodilator therapy. They mentioned that vasospasm might still be significant after aneurysm embolization. Following intra-arterial vasodilator therapy using papaverine hydrochloride, marked dilation of the vasospasm was achieved but this obscured any effects of catheterization alone on the vasospasm. In a few of our cases the vasospasm showed mild dilation after catheterization, and in one case infarction occurred within the distribution field of the catheterized vasospasm. In the present series the success rate for treating aneurysms by catheterization via vasospasm was 94%, a little better than the 88% reported by Hope et al.17 In their series, however, catheterization via vasospasm was undetermined. With vasospasm of the parent artery, endovascular coil embolization allows satisfactory obliteration of aneurysms without aggravation of the vasospasm. In our series 8 of 18 aneurysms were defined as having severe vasospasm of the parent artery according to the criteria proposed by Kassel et al.1 However, introduction of a microcatheter preceded by a micro-guidewire into the vasospasm could be successfully performed. After embolization 14 of 17 patients had complete obliteration of the aneurysm; the remaining three were incomplete (neck remnant). In this relatively small series, the clinical outcomes were good recovery in 13 patients, moderately disabled in 1, vegetative state in 2 and 2 patients died. Eleven of 13 patients with H&H grades I–III showed good recovery and 2 of 3 patients with H&H grade IV also showed good recovery.

Morizane et al10 and Murayama et al11 reported successful endovascular surgery combined with balloon angioplasty and/or intra-arterial papaverine infusion for ruptured aneurysms with symptomatic severe vasospasm. In the series described by Murayama et al,11 complete occlusion was achieved in eight patients, a small neck remnant in three and incomplete in one. The clinical outcomes were good recovery in six patients, moderately disabled in two, severely disabled in three and one patient died. All but two of seven patients with H&H grades II–III showed a good recovery and one of four with H&H grade IV also had a good recovery. These results were almost the same as ours, but somewhat less positive.

Technical considerations

A vasodilating agent was not injected before introduction of the microcatheter into the vasospasm in our series because of the danger of re-rupturing the aneurysm. Care is needed in introducing the microcatheter into the severe vasospasm following the micro-guidewire, and it should then be advanced to the distal branches beyond the aneurysm, pulled back to decrease the tension and then introduced into the aneurysm. Direct introduction of the microcatheter may injure the aneurysm because of the tension and forcing the microcatheter to pass the narrowed part. We used a small-caliber microcatheter and a soft guidewire. The outer diameter of the tip of the microcatheter was 1.7 F, which is the smallest size available to introduce the 10 types of platinum coils. The micro-guidewire has a small caliber of 0.010 inches. The small diameter is essential for introduction into the aneurysm via the vasospasm.

Byrne et al18 found that patients treated by endovascular surgery within 6 days of SAH had a better outcome than those treated later, so the intervention should be performed as soon as possible after presentation. On the other hand, it is recommended that surgical clipping during the period of vasospasm (days 4–10 after SAH) should be undertaken with caution because of the possibility of aggravating latent cerebral ischemia, especially in the presence of significant cerebral vasospasm determined either by angiography or by cerebral blood flow studies. Wanke et al12 described two patients with aneurysms successfully treated with coils followed by intra-arterial infusion of papaverine to treat vasospasm as a one-stage procedure. However, the beneficial effects of an intra-arterial infusion of papaverine solution are transient and repeated treatment sessions are often necessary. Furthermore, the intra-arterial infusion of papaverine is not always effective for vasospasm after SAH. Discrepancies between angiographic and clinical findings have been reported by many authors,15 19 20 and only about 50% of patients with angiographic improvement show clinical improvement.20 21 Jin et al22 reported paradoxical effects such as a vasoconstrictor response to papaverine at the microvascular level. Aggravated microvascular vasospasm may explain the common observation of a lack of correlation between angiographic and clinical benefit. Clyde et al23 reported paradoxical aggravation of vasospasm in the distal MCA and the ACA territories during intra-arterial papaverine treatment. One explanation for the discrepancy is that papaverine may only exert transient effects. Another possible mechanism is stealing cerebral blood flow from the affected vascular area.

In our series only two patients received intra-arterial vasodilator therapy. In one the involved territory did not develop infarction while, in the other, extensive ischemic changes suspected but not confirmed on the pretreatment CT scan resulted in massive infarction. This patient presumably sustained irreversible ischemic injury prior to papaverine treatment.

Nimodipine is a calcium antagonist that reduces the influx of calcium into smooth muscle cells, thereby reducing vascular muscle contraction. Prophylactic intravenous nimodipine is widely used as a vasodilating agent for vasospasm in patients with SAH, with intra-arterial infusion being used for severe vasospasm refractory to intravenous nimodipine.24 However, the long-term efficacy of intra-arterial nimodipine has yet to be assessed.25 The efficacy of intra-arterial verapamil for the treatment of vasospasm has recently been reported.26 27 Unfortunately, neither nimodipine nor verapamil are available in Japan so fasudil hydrochloride hydrate, usually administered intravenously after obliteration of the ruptured aneurysm, is mainly used as a prophylactic vasodilating agent in patients with SAH. Fasudil hydrochloride is a potent vasodilator that inhibits rho-kinase which causes phosphorylation of the myosin-binding subunit of the myosin phosphatase complex leading to the inactivation of myosin phosphatase.13 A prospective double-blind study has shown that intravenous administration of fasudil hydrochloride significantly reduces the incidence of both symptomatic and asymptomatic vasospasm after SAH.14 In our series, intravenous infusion of fasudil hydrochloride hydrate was started immediately after obliteration of the aneurysm and appeared to be effective in 14 of the 18 patients. The fact that brain infarction occurred in the other four patients suggests that conventional medical therapy might not have been sufficient. For massive vasospasm not treatable by a microcatheter, intra-arterial28 and/or intrathecal29 approaches using medical vasodilators may be needed to facilitate additional treatment. Vasospasm after SAH may occur due to extravascular stimulation by various kinds of chemical mediators in blood degradation products, but these are poorly defined. Open surgery will aggravate such vasospasm as a result of extravascular stimulation. On the other hand, catheterization without open surgery will produce intravascular mechanical mild dilation of vasospasm.

Balloon angioplasty itself can achieve persistent dilation of vasospasm,30 31 but it is only appropriate for comparatively large vessels at the A1 or M1 levels.12 A microcatheter preceded by a micro-guidewire can be advanced to more distal portions such as A2, M2 or even more distally for dilation of vasospasm. The tension produced by a microcather preceded by a micro-guidewire while advancing it to the targeted vessels will dilate vasospasm. In our series of patients all vasospasm showed mild dilation after introduction of the catheter, with cerebral infarction in only one case. The advantage of angioplasty using a microcatheter is its feasibility for peripheral vasospasm not accessible to balloon angioplasty.

From this relatively small series of cases we conclude that coil embolization via vasospasm is a safe and effective treatment for aneurysms. Data are now needed in a larger number of cases to confirm the indications for endovascular surgery in the treatment of aneurysms with vasospasm.

Acknowledgments

We thank Dr Malcolm Moore for editing the scientific English in the manuscript.

References

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Footnotes

  • Competing interests None.

  • Patient consent Obtained.

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

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