Microsurgical management of large and giant paraclinoid aneurysms

2.1. Patient characteristics 

We treated 51 patients with a total of 59 aneurysms (Table 1), constituting 9% of the 560 patients with cerebral aneurysms treated in the same time period at our institution. Patients comprised 33 women (65%) and 18 men (35%). Their mean age was 54.5 (range 19-73) years.

Table 1. Distribution and size of paraclinoid aneurysms

	Location	Size
		15-25mm	>25mm
	Carotid cave	2	0	2 (3.92%)
	Ophthalmic	17	21	38 (74.51%)
	Superior hypophyseal	3	4	7 (13.73%)
	Posterior carotid wall	2	2	4 (7.84%)
	Total	24 (47.06%)	27 (52.94%)	51 (100%)

2.2. Clinical presentation 

Thirty-seven patients (73%) had ruptured aneurysms. Thirty patients (81%) were in good clinical condition (Hunt and Hess grades I and II) before the operation (Table 2). Seventeen patients (33%) presented with impairments of visual acuity or visual field deficit, three (6%) had oculomotor nerve palsies, one (2%) had ischemic infarction, and six (12%) had chronic headaches (Table 3). One aneurysm was found incidentally.

Table 2. Hunt and Hess scores for patients with subarachnoid hemorrhage (n = 37)

	Hunt and Hess Grade	No. of patients
	1	18
	2	12
	3	5
	4	2
	5	0

Table 3. Clinical symptoms

	Symptoms	No. of patients
	Oculomotor palsy	3
	Chronic Headache	6
	Ischemic infarction	1
	Visual disturbance	17

2.3. Size of aneurysms 

Twenty-four patients (47%) had large aneurysms (largest diameter 15-24 mm); the remaining 27 patients (53%) had giant aneurysms (25 mm or larger).

2.4. Radiological investigations 

All 51 patients underwent computed tomography (CT) and DSA examinations preoperatively. After the operation, all patients underwent CT scan to exclude surgical complications. Postoperative DSA was performed to detect residual aneurysm after clipping and CTA was performed to follow-up the residual aneurysm.

Preoperative CT findings were as follows: 37 patients (73%) with acute subarachnoid hemorrhage, 4 patients (8%) with a calcified aneurysm, 4 patients (8%) with an accompanying hydrocephalus, and one patient (2%) with a preexisting ischemic infarction. Twenty-nine patients (57%) needed additional magnetic resonance imaging examinations before the operation, revealing 12 thrombotic aneurysms (24%).

Preoperative DSA detected 59 aneurysms in 51 patients; the eight associated aneurysms were located as follows: two contralateral ophthalmic aneurysms, three PComA aneurysms, one proximal anterior cerebral artery aneurysm, one anterior communicating artery aneurysm, and one middle cerebral artery (MCA) bifurcation aneurysm. All of these patients underwent balloon test occlusion (BTO) or Matas test with provoked hypotension. Blood pressure was 30 mmHg lower than normal levels and maintained for 30 minutes. Fourteen of the 51 patients could not tolerate the test.

We have classified the paraclinoid aneurysms as follows: 38 ophthalmic aneurysms (75%), 7 superior hypophyseal aneurysms (14%), 4 posterior carotid wall aneurysms (8%), and 2 carotid cave aneurysms (4%).

2.5. Surgical technique 

A routine pterional-transsylvian craniotomy was combined with exposure of the cervical ICA. The ACP, the roof of the optic nerve canal, and the optic strut were removed intradurally by a diamond drill. The optic nerve sheath was also opened for satisfactory visualization of the proximal side of the aneurysm's neck [22]. If necessary, the distal dural ring was opened, allowing mobilization of the ICA. Sometimes, even the proximal dural ring was opened along the ICA and the wall of the aneurysm, extending into the cavernous sinus for better visualization of the aneurysm. When dissecting the aneurysm, the cervical ICA was intermittently occluded to prevent intraoperative rupture of the aneurysm. After satisfactory dissection of the aneurysm base, the cervical ICA was closed simultaneously with the distal ICA, making the aneurysm softer and decompressing it. This short trapping was used to clip the aneurysm, and the parent artery was reconstructed simultaneously. Multiple, strong, long clips were frequently used. In aneurysms with wall calcifications or a thrombus inside the aneurysm, endoaneurysmectomy was performed for total or partial removal of the calcifications or the thrombus.

When an aneurysm is saccular, it can be decompressed and dissected by using the retrograde suction method [2]. The aneurysm is trapped first by occluding the proximal carotid artery at the neck and the intracranial ICA distal to the aneurysm. The aneurysm is then aspirated through a needle inserted into the cervical ICA. Direct puncture of the aneurysm is another method to decompress the saccular aneurysm. However, when using this technique, the proximal and distal segments of the aneurysm must be temporarily occluded. These temporary clips and alternative suction in the narrow field will hinder clip placement and adjustment. Moreover, if the aneurysm is not completely obliterated, retrograde blood from the ophthalmic artery or the PComA will flow into the aneurysm sac; bleeding from the puncture orifice can be catastrophic. For this reason, we prefer cervical ICA retrograde suction.

In seven unclippable aneurysms (14%), the collateral flow was found to be insufficient in preoperative tests, and consequently, an extra-intracranial bypass using a saphenous vein graft followed by trapping was performed. One patient (2%) with sufficient collateral circulation had a proximal Hunterian ligation. The microsurgical steps were as follows: 1) the cervical ICA and its branches were prepared; 2) the pterional craniotomy was performed and the M2 segment exposed; 3) the saphenous vein was harvested; 4) the extracarotid artery and the inferior trunk of the M2 segment were revascularized using the saphenous vein graft in an end-to-side fashion; and 5) the aneurysm was trapped.

As all patients had temporary occlusion of the ICA during the surgery, intra-operative EEG and SSEP monitoring were routinely performed. As soon as changes were seen in electrophysiological monitoring (six patients), the blood flow was immediately restored. The surgery was continued after the electrophysiological monitoring normalized. No ischemic signs were observed in the follow-up in any of these patients. Occlusion was limited to 10 minutes even if no obvious changes occurred during electrophysiological monitoring.

Intraoperatively, MDU was used to assess blood flow in parent and branch arteries. Recently, intraoperative ICG videoangiography was introduced and has been used to evaluate complete obliteration of the aneurysm and patency of arteries, even of perforating arteries. Clips in 12 patients were readjusted when Doppler and/or intraoperative ICG videoangiography detected insufficient blood flow in the parent vessel, branches, or perforating arteries. Intraoperative DSA was not used, but postoperative DSA was performed to confirm complete obliteration of aneurysms or patency of the bypass graft. A Storz rigid endoscope with a 30° angle of view was used mainly in ICA posterior wall aneurysms (in 3 of 4 patients) when the PComA, choroidal artery, or one of the distal cerebral or perforating arteries was hidden behind the aneurysm dome. Before and after clipping, the endoscope was also used to assess or verify the exact position of the clip(s) [18], [26].

3.1. Surgical mortality and morbidity 

Two (4%) of the 51 patients died during the postoperative follow-up. One was a 65-year-old woman who presented with a giant paraclinoid aneurysm harboring severe calcification and an intra-aneurysmal thrombus. After the aneurysm was incised and the calcification and thrombus evacuated, the parent artery could not be reconstructed despite repeated clip readjustment. We discovered that the proximal ICA was thrombosed, and consequently, (in this desperate situation) a STA-MCA bypass was performed to supply distal blood flow. At the end of the operation, the bone flap was discharged to decrease intracranial pressure. The patient died one week later due to brain infarction. The other patient was a 56-year-old woman with an ophthalmic aneurysm who died two weeks after the operation due to brain infarction, probably caused by an embolism released from the wall of the cervical carotid artery.

A 59-year-old woman with a clipped ophthalmic-carotid aneurysm with associated severe atherosclerotic carotid stenosis demonstrated a rebleeding with subarachnoid blood and intraventricular clot three hours after the operation. In DSA, this proved to be due to an incomplete clipping of the aneurysm. Immediate reoperation with reclipping was done, and ventricular drainage was performed. The patient was severely disabled at discharge, but continued to improve and demonstrated only mild hemiparesis at the six-month follow-up.

Six patients had transient procedure-related oculomotor nerve palsies, completely recovering within 1.5-12 months postoperatively. Visual function worsened in two patients with optic nerve distortion. One patient improved six months later and the other remained unchanged.

One patient developed postoperative cerebrospinal fluid (CSF) leakage related to pneumatization of the removed ACP. The leakage persisted even with continuous lumbar drainage and was finally repaired by using an endoscope.

The seven patients who underwent bypass, as elective procedure, had no complications.

4.1. Patient 1: Carotid Cave Aneurysm 

A 55-year-old woman presented with intermittent headache for one year; she complained of visual disturbances and double vision for one month. An aneurysm measuring 15 × 14 mm was assessed as a carotid cave aneurysm. The cervical ICA was exposed. A pterional approach with anterior clinoidectomy and removal of the roof of the optic canal and the optic strut was performed to completely expose the aneurysm base. After proximal occlusion of the cervical ICA and distal temporary clipping, the aneurysm was softer and was directly clipped. Postoperatively, the patient had a good recovery, and the preoperative visual disturbances improved in the follow-up.

Fig. 1 and Video 1.

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Fig. 1. Case 1. Illustration of a large carotid cave aneurysm. A: Preoperative anteroposterior view angiogram showing a carotid cave aneurysm. B: 3D-DSA showing a carotid cave aneurysm. C,D: Postoperative anteroposterior and lateral view angiograms showing the aneurysm completely obliterated.

4.2. Patient 2: Ophthalmic aneurysm 

A 55-year-old woman was admitted for SAH with Hunt-Hess grade II. A large ophthalmic-carotid aneurysm arose distally from the origin of the ophthalmic artery. The aneurysm was severely calcified, so it was too hard to be clipped. A saphenous vein graft high-flow bypass procedure was performed and the aneurysm was trapped. The patient had a good outcome.

Fig. 2 and Video 2.

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Fig. 2. Case 2. Illustration of a large ophthalmic-carotid aneurysm. A: CT showing SAH and severe calcification. B,C: Preoperative anteroposterior and lateral view angiogram showing an ophthalmic-carotid aneurysm. D: Intraoperative image showing a hard aneurysm that was unclippable; a bypass procedure was performed. E: Intraoperative ICG videoangiography showing a patent bypass vessel. F: Postoperative CTA showing a patent bypass vessel and a completely obliterated aneurysm.

4.3. Patient 3: Superior hypophyseal aneurysm of the ICA 

A 54-year-old woman was admitted for progressive visual disturbance over a two-month period. DSA revealed a large superior hypophyseal aneurysm. The patient underwent a left frontotemporal craniotomy, the ACP was removed, and the left cervical ICA was exposed. The optic nerve was severely distorted medially by the aneurysm. When the proximal cervical ICA and the ICA distal to the aneurysm were temporarily occluded, the aneurysm was collapsed by retrograde suction. The aneurysm was then clipped by one fenestrated clip and two long curved clips to reinforce the occlusion. Intraoperative ICG videoangiography confirmed that the aneurysm was completely obliterated and the ICA was patent. The patient had an excellent outcome, and visual disturbance improved at discharge.

Fig. 3 and Video 3.

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Fig. 3. Case 3. Illustration of a large superior hypophyseal aneurysm. A, B: Preoperative anteroposterior and lateral view angiograms showing a large superior hypophyseal aneurysm with a medially directed fundus. C: 3D-DSA showing the configuration of the aneurysm. D: Intraoperative ICG videoangiography was performed before the aneurysm was clipped. E, F: The aneurysm was clipped by one fenestrated clip and two long curved clips to reinforce the occlusion. ICG videoangiography was then performed to confirm that the aneurysm was completely obliterated and the ICA was patent. G, H: Angiograms showing that the aneurysm was completely obliterated.

4.4. Patient 4: Posterior wall aneurysm of the ICA 

A 58-year-old woman presented with headache and visual disturbance for one month. Preoperative angiogram, CTA, and 3D-DSA showed a posterior wall aneurysm of the left ICA and an anterior communicating artery aneurysm. The patient underwent a left frontotemporal craniotomy, and the posterior wall aneurysm was clipped. The rigid endoscope (see above) confirmed that the aneurysm's neck was completely clipped and the perforators preserved. The associated anterior communicating artery aneurysm's neck was also clipped. The postoperative recovery was uneventful, and the patient had a good recovery.

Fig. 4 and Video 4.

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Fig. 4. Case 4. Illustration of a giant posterior wall aneurysm of the left ICA and an anterior communicating artery aneurysm. A: Preoperative lateral view angiogram showing a giant posterior wall aneurysm with a wide neck and an anterior communicating artery aneurysm. B: 3D-DSA showing the giant aneurysm arising from the posterior ICA wall. C: CTA showing a posterior wall aneurysm; part of the aneurysm base was covered by the ACP. D: Postoperative anteroposterior view angiogram showing the clipped aneurysm and the patent parent artery. E: The aneurysm was clipped directly and the parent artery was reconstructed.

5.1. Surgical indication 

Intracranial aneurysms cause principally clinical symptoms in three different ways: by rupturing, by compressing nearby structures, and by causing ischemia through thromboembolism. Besides rupturing, because of their critical site and size, different compression symptoms of the optic nerve and tract and other cranial nerves are common in large and giant paraclinoid aneurysms. According to Laplace's law, the aneurysm's wall tension is direct proportional to the aneurysm's diameter; the larger the aneurysm, the greater the tension on the aneurysm's wall, and the more the aneurysm is prone to rupture. In the International Study of Unruptured Intracranial Aneurysms [34], the annual rupture rate of giant aneurysms was about 6%, higher than that of smaller aneurysms. With increasing size, thrombus formation inside the aneurysm may also be increased. The presence of an intraluminal thrombus does not protect against rupture, except when the aneurysm is completely thrombosed. However, a growing thrombus can give rise to emboli distally in the carotid tree, resulting in ischemic attacks or stroke. In our institution recent rupture of the aneurysm, especially in young people, is one of the indications for acute and early surgery to prevent rebleeding. Compression syndromes and rarer embolic cases can be treated more on an elective basis, but generally the prognosis of large and giant aneurysms is so dismal that they should be treated actively.

5.2. Surgical management strategies 

When using microsurgical treatment techniques, large and giant paraclinoid aneurysms can be divided into “clippable” and “unclippable” subgroups. Irrespective of their site, soft aneurysms that do not extend deep into the cavernous sinus in our experience belong to the clippable group. Unclippable aneurysms, in turn, tend to be hard, thick-necked, and severely calcified; generally, they also extend deep into the cavernous sinus. Because of the large or giant size of these aneurysms, several different tricks not used in ordinary aneurysms must be employed to successfully occlude the aneurysm's base. Soft thin-walled aneurysms can be decompressed by retrograde suction and clipped when the aneurysm is slack [25]. A partially thrombosed aneurysm has to be opened to evacuate the thrombus mechanically or by suction, or better yet by using an ultrasonic aspirator. In a partially calcified aneurysm, endoaneurysmectomy may make the wall more malleable for clipping. When the base of the aneurysm is calcified, clipping of the aneurysm's neck should be replaced by a bypass procedure performed during the same operation or later. In these cases, preoperative collateral circulation assessment is critical for intraoperative ICA temporary occlusion, and occasionally the ICA needs to be sacrificed. Based on the result of BTO with a hypotensive provocation test [28], unclippable aneurysms can be further divided into two subgroups. Patients who tolerate BTO are treated by simple proximal ICA occlusion (Hunterian ligation), while those who do not tolerate BTO require revascularization with bypass to have their aneurysm occluded. A delayed ischemic event can occur, and for this reason, in our center, high-flow bypass is performed if the ICA must be sacrificed and low-flow bypass if the MCA is sacrificed.

If the aneurysm's neck does not extend into the cavernous sinus, the aneurysm can be directly clipped. In our series, the ophthalmic artery mainly acts as the landmark to judge the relationship between the cavernous sinus and the aneurysm neck. If the aneurysm's neck has an intimate relationship with the cavernous sinus, both direct aneurysm clipping and trapping with revascularization are planned preoperatively [15]. If the aneurysm base is partially buried deep inside the cavernous sinus, we prefer trapping of the ICA, with or without bypass. In our experience, direct clipping of the neck of aneurysms in which the base is partially intracavernous is associated with some complications (mainly incomplete obliteration and impairment of cranial nerves, especially of the oculomotor nerve) [8]. If the situation is unclear, during cranial exploration the selection of direct or indirect surgery can still be made.

5.3. Endovascular treatment of large and giant paraclinoid aneurysms 

Endovascular coiling is becoming an increasingly appealing treatment option. Several methods have been developed recently such as stenting and then coiling or filling a stented aneurysm with liquid glue to obliterate the aneurysm. Generally, if the patient is old or in poor clinical condition and if the aneurysm has no mass effect or it extends deep into the cavernous sinus, an endovascular procedure is the first treatment choice, reducing open surgery complications. However, for large or giant paraclinoid aneurysms, a densely compacted coiling is hard to achieve, and this may result in refilling of the aneurysm. Size of an aneurysm larger than 10 mm is a significant predictor factor of aneurysm recurrence and long-term angiographic follow-up is mandatory [30]. Occasionally, when the parent artery is stenosed or acutely bent, the catheter cannot reach the aneurysm. In China, the cost of endovascular treatment is five or six times higher than that of open surgery and angiographic follow-up has also an additional significant cost. The economic aspect must also be considered when selecting a treatment.

Irrespective of the location of giant aneurysms, a limitation of endovascular treatment is a reduced capability than open microsurgery to deal with the compression syndrome.

In our series, 17 patients had visual disturbances. At the six-month follow-up, visual function improved in 15 patients, remained unchanged in one patient, and worsened in one patient. Heran et al [12] reported on 17 patients with large ophthalmic aneurysms who underwent endovascular treatment, demonstrating improved vision in eight, unchanged vision in four, and worsened vision in four. Seven of their eight patients with improved vision had undergone carotid artery occlusion without continuous pulse pressure on the optic nerve. Day et al [6] reviewed 23 cases with giant ophthalmic aneurysms and preoperative vision deficits; visual function improved in 17, remained unchanged in 6, and worsened in none. Surgical treatment of paraclinoid aneurysms is an invasive and demanding treatment option, which can be performed only by experienced personnel in high-volume neurovascular centers. These patients should be centralized to a few skilled surgeons, as it is done with many other cerebrovascular lesions. Clipping the aneurysm's neck might be associated with more risks than coiling, but a permanent occlusion of the aneurysm can be achieved. Even in the best hands, there is a high recurrence rate for endovascular-treated aneurysms. Raymond et al [30] described 277 endovascular-treated aneurysms with detachable coils. Long-term follow-up angiograms revealed recurrences in up to 34% of treated aneurysms, with the most important factor associated with recurrences being size larger than 10 mm. David et al [5] reported on 135 clipped aneurysms; late follow-up angiography revealed two recurrences (1.5%). In a recent report about long-term follow-up (mean follow-up was 126 months) of a surgical series of 108 aneurysms located at the ophthalmic segment of the ICA, 93% of the aneurysms were totally clipped and 58% of them were large or giant [29]. No large endovascular series, concerning the treatment of large-giant paraclinoid aneurysms, with long-term follow-up, has been reported. In the current series 77% of the patients had a complete occlusion of the aneurysm, and in 8 patients we couldn't verify the surgical result. To ensure durability of treatment, the surgical clipping needs to be maintained.