Key Words : aneurysms·in situ·bypass·graft·extracranial-intracranial·suture.

Introduction

Most intracranial aneurysms can be managed with microsurgical clipping or endovascular coiling, but a subset of aneurysms with complex anatomy or fusiform/dolichoectatic morphology may require an alternative approach involving revascularization.4)6)9) Extracranial-intracranial bypass has been a crucial component of neurosurgery for complex intracranial aneurysms4)6)8-9) ; however, when the donor and recipient arteries are in close proximity to each other, intracranial-intracranial bypass can be very useful, especially for the distal MCA, ACA and posterior inferior cerebellar artery (PICA).3)5)8) In addition, aneurysms arising from the dorsal wall of the ICA, known as the BBA, rupture easily during surgical manipulation, resulting in an arterial wall defect in the ICA.2)7)10) In such situations, we performed direct suture of the arterial tear on the BBA, followed by a clip reinforcement technique and circumferential wrapping with a silastic sheet.2)10) We report our clinical experience using vascular reconstruction techniques without an extracranial arterial stump for the treatment of complex intracranial aneurysms.

Material and Methods

A total of 27 patients underwent cerebral revascularization for the management of intracranial aneurysms at our hospital between 1996 and 2008. Fourteen patients underwent bypass surgery with arterial pedicles, such as the superficial temporal artery or occipital artery, and six patients underwent bypass surgery with a saphenous vein interposition graft. In situ bypass was performed in five patients, and direct neck sutures were performed secondary to the wrapping-clipping method in two patients. Vascular reconstruction techniques without an extracranial arterial stump included in situ bypass of end-to-side anastomosis or end-to-end reanastomosis of the parent artery after aneurysm excision in five cases and direct neck sutures with the wrapping-clipping method in two cases. The medical records, images, and operative records of seven patients were retrospectively reviewed. Patient outcome was assessed according to the Glasgow Outcome Scale (GOS).

Results

The patients were four men and three women, with a mean age of 38.14 years. Only one patient had an incidental aneurysm, and the other six patients presented with subarachnoid hemorrhage (SAH), the severity of which was Hunt-Hess (H-H) grade III in three patients, IV in one patient and V in two patients. The Fisher computed tomography grade was III in two patients and IV in four patients.

Five aneurysms were fusiform and located in the ACA in two patients, MCA in two patients and anterior tempeoral artery (ATA) in one patient. One case of ACA aneurysm was traumatic. They were treated with in situ bypass followed by aneurysm excision, including end-to-side reanastomosis in two MCA aneurysms and one ACA aneurysm and end-to-end reanastomosis in the other ACA and ATA aneurysm. In one case of distal MCA fusiform aneurysm, superficial temporal artery (STA)-MCA end-to-end bypass and MCA-MCA end-to-side bypass were performed simultaneously. The other two aneurysms were BBAs located on the dorsal ICA. They were managed using direct suture secondary to clip reinforcement and circumferential wrapping with a silastic sheet.

The follow-up periods ranged from 3 to 35 months. Postoperative or follow-up angiography revealed complete obliteration of the aneurysm in five patients, a patent graft in four patients and delayed graft occlusion due to granuloma formation in one patient with BBA. However, all patients who underwent follow-up angiography had an excellent outcome (GOS score 5). Two patients did not undergo postoperative angiography due to unfavorable neurologic outcomes: one patient was in a vegetative state, and one patient died. The poor outcomes were related to the initial injury after SAH, the preoperative clinical condition was H-H grade V in both patients. The patient data are summarized in Table 1.

Case Illustration

Patient 1 (ACA)

This 46-year-old woman presented with a history of headache lasting approximately 9 months. CT scan revealed an irregular, round, calcified, hyperdense lesion, along the genu of the corpus callosum and no hemorrhagic lesion (Fig. 1A). Cerebral angiography revealed a giant serpentine aneurysm arising from the right proximal A2 segment (Fig. 1B, C, D).

The bifrontal interhemispheric approach was performed to expose the proximal and distal portion of the aneurysm. To reconstruct the cerebral flow in the right distal ACA after aneurysm trapping, we considered A3-A3 side-to-side anastomosis or end-to-side anastomosis and A2-A3 end-to-end anastomosis using the STA interpositional graft. After considering these surgical options, we decided to perform A3-A3 end-to-side anastomosis because it was the simplest option. Postoperatively, the patient awoke without any neurological deficits. A subsequent three-dimensional CT angiography showed good filling of the distal right ACA through the left ACA (Fig. 1E), which was confirmed by cerebral angiography obtained 10 days later (Fig. 1F).

Patient 4 (MCA)

A 22-year-old man presented in a comatose state. Computerized tomography revealed intracerebral hemorrhage in the left frontal lobe, intraventricular hemorrhage in all ventricles with severe mass effect and an incidental arachnoid cyst in the right middle fossa (Fig. 2A). No significant vascular lesion was observed on three-dimensional CTA (Fig. 2B). A wide left frontotemporal craniotomy was performed for decompression. During careful removal of the hematoma, a heavily thrombosed and fusiform M2 aneurysm, approximately 25mm sized, and two distal M3 branches arising from the dome of the aneurysm were found (Fig. 2 C, D). One branch of the distal M3 was reimplanted into another M2, and the other was anastomosed with STA (Fig. 2E). The aneurysm was excised.

The patient remained in a vegetative state postoperatively because of the initial injury. Postoperative CT angiography showed good patency of bypass (Fig. 2F).

Patient 6 (ICA BBA)

This case, which has been reported elsewhere, is included for the sake of completeness (2). A 30-year-old man suffered a sudden-onset headache and vomiting. His condition was graded as H-H Grade III. Cerebral angiography indicated a blister-like aneurysm (Fig. 3A). Surgery was performed two days after the onset of symptoms. The cervical ICA was exposed for proximal control in case of premature rupture. The aneurysm was exposed on the C2 segment of the ICA. It had no relation to any of the carotid branches, and its wall seemed to be very thin (Fig. 3B). Massive arterial bleeding occurred during removal of the local blood clot and aneurysmal neck dissection. We tried to repair the wall with 8-0 nylon sutures (Fig. 3C). Finally, the sutured vessel wall was wrapped with a transparent silicone sheet (Medical grade silicone sheet; size#20-05; Bioplexus Corporation, USA), and a curved Sugita clip was applied parallel to the arterial wall to prevent the regrowth of the aneurysm (Fig. 3D). The clipped wall was secured with a beam sheet and fibrin glue. The total time for the temporary clipping was approximately 20 minutes.

The postoperative course was uneventful. However, the patient deteriorated on postoperative day 4. Angiography performed 5 days after surgery demonstrated severe vasospasm of the left ACA and MCA. Angioplasty was performed with intra-arterial papaverine, and the vasospasm improved. Repeat CT scans revealed cerebral infarction of the left frontal and temporal lobe. The patient recovered gradually and was discharged with mild hemiparesis on the right side. Follow-up angiography obtained 9 months later demonstrated total occlusion of the left ICA just distal to the ophthalmic artery and collateral opacification of the left MCA by the left P-com (Fig. 3E). However, there was no symptom of the delayed occlusion.

Discussion

Intracranial aneurysms can be treated optimally by either microsurgical clipping or endovascular coiling. Endovascular and microsurgical clip reconstruction techniques may be impossible in certain situations, such as giant or fusiform aneurysms which may incorporate the parent artery or adjacent arterial branches from the aneurysm base, as calcification or atherosclerotic thickening can make clipping hazardous. Under such situations, parent vessel occlusion or trapping may be necessary and cerebral revascularization must be considered to augment the blood flow if the patient� collateral circulation is insufficient to supply vascular territories distal to the occlusion.

The selection of the type of revascularization procedures depends on the demand of blood flow through the bypass and the anatomy of the vessels associated with the lesion. With the exception of high-flow bypass, the most commonly used vascular donor is a pedicle arterial graft, such as the superficial temporal artery or occipital artery. However, certain situations are amenable to in situ bypass if the blood flow does not demand high flow. In situ bypass requires that the donor and recipient arteries lie parallel and in close proximity to one another. It is advantageous as it is a less invasive intracranial technique, less vulnerable to injury or occlusion, does not require harvesting of an extracranial arterial graft, requires one suture line, involves a short bypass distance, and the diameter between the donor and recipient arteries is well-matched.5)8)

In general, revascularization is advisable if sacrifice of the ACA is performed within the first segment of the ACA, namely the A1 and A2.1) With ACA bypass, the STA is not long enough to reach the A3 segment. Therefore, if the surgeon wanted to use an extracranial arterial graft, a more complex bonnet bypass using interpositional graft should be done.3)8) In these circumstances, in-situ bypass is more ideal and less invasive. In distal ACAs, side-to-side anastomosis effectively prevents ischemic complications in the territory of the pericallosal artery. It has been reported that direct end-to-end anastomosis between ipsilateral A1 and A2 segments is possible only if the distance between the cut ends is less than 5 mm due to difficulties in axial mobilization of both ends.1)11) In our cases, direct end-to-side anastomosis was performed secondary to aneurysm trapping for the giant serpentine aneurysm in patient 1, and end-to-end anastomosis of the ipsilateral ACA was performed secondary to aneurysm excision for traumatic aneurysms with a relatively narrow diseased segment in patient 2. We prefer side-to-side anastomosis to end-to-end or end-to-side anastomosis because side-to-side anastomosis requires a long arteriotomy with a length that is typically three times greater than the diameter of the arteries, and it is technically more challenging to suture the back wall of the anastomosis from the inside of the lumen, and more risky to kink the afferent and efferent arteries.

Proportionately fewer MCA aneurysms were considered unclippable and unamenable to in situ bypass. At our institution, nine patients underwent bypass surgery for complex MCA aneurysms. We performed a total of seven EC-IC bypasses. STA-saphenous vein-MCA bypasses were performed in three cases: in situ bypasses, including end-to-side reimplantation of the branch was performed in three of the two cases, and primary reanastomosis was performed in one case. Unlike ACA bypass, STA to MCA branch anastomosis can be performed safely because the STA is long enough to reach the M3 or M4 segment, and it is a time-tested technique. We therefore prefer STA-MCA bypass for the treatment of complex MCA aneurysms. However, if the two branches emerge from the aneurysm, we performed in situ bypass additionally. In patient 4, STA-MCA bypass and MCA-MCA bypass were performed simultaneously for the distal MCA fusiform aneurysm. In this patient, another interesting option would be to perform a double-barrel STA to MCA bypass connecting two branches of the STA to two branches of the MCA; however, we thought that double-barrel STA has inadequate blood flow because it does not duplicate but rather divides the amount of STA flow.

In patient 5, who presented with an ATA aneurysm in the early temporal branch of the M1 segment, the authors considered several alternative methods to prevent ischemic injury during surgery including: (1) trapping followed by STA-distal ATA anastomosis; (2) excision followed by reimplantation of the distal end of the excised artery on the lateral branch of the MCA in an end-to-side fashion; and (3) excision followed by reanastomosis of the proximal and distal ends of the excised artery using the an interposition graft, such as STA or superior thyroid artery. Of these surgical options, we decided to use the third option because it is simple and because the distances of cut ends were relatively short.

Reconstruction of the parent vessel by suturing while preserving the patency of the parent artery for the BBA is a salvage technique. It can be very difficult to repair the arterial tear in the ICA because the operation field is deep and narrow during the acute stage. If complete suturing were performed, the temporary clipping time would be too long and result in a massive cerebral infarction. In our cases, we placed only three or four 8-0 nylon stitches in the ICA in order to reform the parent artery. We did not want to completely obliterate the arterial wall defect. Therefore, the temporary occlusion time could be shortened considerably. To prevent aneurysm regrowth, clip reinforcement was performed via circumferential wrapping with a transparent silicone sheet. This vascular reconstruction technique can be a useful treatment option for these fragile BBA aneurysms in cases where other options may be impossible.2) Compared with other wrapping materials such as gauze, muscle, cellulose fabric, and Gore-tex, the silicone sheet (Medical grade silicone sheet, size 20-05, Bioplexus Corporation) has the advantage that the branches around the aneurysm encircled with the sling can be seen because it is thin, flexible, and transparent. In addition, the sling can be easily tailored to incorporate perforating branches and other arteries.

Conclusion

Cerebral revascularization with an extracranial arterial graft is a safe and effective technique for the treatment of complex large or giant aneurysms, as well as unclippable fusiform aneurysms. In addition, our experience and a review of the literature indicate that vascular reconstruction without an extracranial arterial graft is also an important part of the treatment of complex intracranial aneurysms. In situ bypass is an effective alternative to extracranial-intracranial bypasses for distally located fusiform aneurysms. In addition, arterial suturing followed by clip reinforcement with circumferential wrapping is a useful technique for fragile aneurysms unsuitable to direct clipping or encircled clip placement for true ICA trunk aneurysms. Although technically challenging, this vascular reconstruction technique without an extracranial arterial graft should be considered for appropriate candidates.

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