Introduction

Transitional internal carotid artery (ICA) aneurysms incorporate the cavernous, clinoidal, and supraclinoidal segments of the ICA as portions of the neck of the aneurysm. In this chapter, we review the natural history, clinical course, our series, and surgical techniques/nuances for the treatment of these aneurysms.

Pure cavernous ICA aneurysms are a separate category of aneurysms, which do not extend beyond the dural ring of the ICA. In general, in the neurosurgical literature these aneurysms are considered benign, even in larger sizes.¹ However, in our experience it is possible that when these aneurysms get significantly large in size, they can cause rupture through the middle fossa dura, causing hemorrhage and potential mortality (Figure 23–1).

Figure 23–1 A, A 55-year-old presented with new onset diplopia. T1 axial MRI shows cavernous sinus aneurysm. B, Digital subtraction angiogram (DSA) showing a giant cavernous ICA aneurysm (does not extend into the supraclinoidal segment). Following balloon test occlusion in hospital, the patient had an acute headache, and became fixed and dilated. The patient subsequently died within 2 hours. C, Autopsy revealed a rupture through the middle fossa dura into the temporal lobe.

Natural history of transitional segment of ICA aneurysms

Unruptured intracranial aneurysms are being diagnosed more often than in the past and these lesions pose management problems. The first series of giant aneurysms was presented in 1969 by Morley and Barr, who described giant aneurysms as >2.5 cm.² Giant aneurysms are relatively rare, comprising between 5% and 7% of aneurysms³ in most series. Giant aneurysms have a female predominance with ratios as high as 3:1 in some series⁴ and most commonly present in the middle decades. Giant aneurysms are most frequently located on the ICA, specifically, involving the paraclinoid segment 21% of the time.⁵

The natural history of giant aneurysms is one of a poor prognosis. Some have compared the fate of unruptured giant aneurysms to that of subarachnoid hemorrhage (SAH).⁶ Patients often present with symptoms consistent with SAH or mass effect. The Italian cooperative study has shown a 28% mortality rate for untreated giant aneurysms compared to a 14% mortality rate for patients who received treatment.⁷ In the same series, morbidity was seen in 48% of cases due to expansion. Giant aneurysms, not unlike other aneurysms, continue to enlarge over time. Expansion is thought to be from growth of the lumen or thrombus formation within the sac. This progressive enlargement often causes symptoms of mass effect.⁸

Historically, it was thought that giant aneurysms were less prone to rupture; however, contemporary evidence suggests that this is inaccurate. Drake found that 62 of 174 cases did rupture.⁹ Aneurysms sized ≥25 mm had a relative risk of rupture of 59% compared to aneurysms <10 mm.¹⁰ Giant aneurysms had a 6% rupture rate in the first year compared to <1% for aneurysms <10 mm.¹⁰ Patients with a giant aneurysm, but without previous SAH, were at a significantly increased risk for rupture based on size. The rupture rate was not dependent on the location of the aneurysm; all anterior circulation giant aneurysms were at increased risk of rupture.³ Risk factors for aneurysm rupture include hypertension, current or former tobacco use, alcohol use greater than five drinks per day, and use of oral contraceptives.¹⁰ It was thought that partially or completely thrombosed aneurysms would be less likely to rupture, thus not requiring treatment; however, in Drake’s large series, this was not the case.⁹

The ISUIA (International Study of Unruptured Intracranial Aneurysms Investigators) trial has shown that un-ruptured aneurysms overall do not pose the risk they once were thought to; and that treating aneurysms, specifically small ones, puts the patient at more risk than surveillance. However, this advice should not be applied to the special case of giant aneurysms, where “the natural history is ominous.”⁶ Morley and Barr’s original series demonstrated similar findings, with an 80% mortality rate for untreated aneurysms. Other studies have shown high 1-year mortality rates.¹¹ Peerless et al. found that 85% of patients with giant intracranial aneurysms were dead at 5 years.¹² Additionally, the ISUIA II found that the cumulative rupture rates for anterior circulation giant aneurysms with no previous history of SAH were 40%. Patients who present with SAH are at increased risk of mortality compared to patients without SAH.¹³ We present a case of a ruptured giant aneurysm without previous history of SAH 6 months after initial diagnosis (Figure 23–2).

Figure 23–2 A, A patient was diagnosed with this aneurysm at an outside institution and was recommend conservative treatment. B, Patient was transferred to our institution 6 months after initial diagnosis with acute SAH and IVH, and underwent an angiogram. C, During angiography, the aneurysm reruptured (see extravagation of blood). D, Postangiography CT scan showing blood completely filling the lateral ventricles. The patient subsequently expired.

The Dilemma of Deliberate ICA Occlusion

Traditional neurosurgical literature and practice have held a liberal view of ICA occlusion for the treatment of giant ICA aneurysms. Historically, this has been accompanied by a relatively high risk of stroke following the ICA occlusion (Table 23–1). With recent improvements in the balloon test occlusion (BTO) paradigms, the risk is smaller but clearly not absent.

Table 23–1 ICA Sacrifice.

Source	Surgery	Outcomes
Sahs and Locksley, 196914	ICA ligation	Stroke 30% Mortality 20.7%
Roski et al., 198115	ICA ligation	TIA 16.6% Stroke 16.6% SAH 5.5% Mortality 5.5%
Linskey et al., 199416	Intravascular ICA occlusion	Stroke 12.9% Mortality 3.2%
Larson et al., 199517	Intravascular ICA occlusion	TIA 10.9% Stroke 3.6% SAH 3.6% Mortality 5.4%

ICA, internal carotid artery; SAH, subarachnoid hemorrhage; TIA, transient ischemic attack.

For the treatment of carotid occlusive disease, traditional neurosurgical literature and practice have strongly recommended preservation of the ICA. High-grade stenosis (i.e., 99% stenosis) is considered a relative neurosurgical emergency, requiring an endarterectomy or stenting. It is interesting that most patients who present with cervical carotid occlusive disease are usually older and generally have multiple medical comorbidities; yet performing a procedure to open the carotid artery has remained standard practice. Most cervical carotid occlusive disease symptomatology is due to embolic disease rather than hemodynamic compromise. Therefore, in the majority of cervical carotid occlusive disease, a deliberate occlusion of the ICA, in the opinion of the senior author, could be performed with a relatively low risk of morbidity, and most likely less risk of morbidity and mortality, when compared to carotid endarterectomy or stenting. However, this would be considered a complete departure from our current standards of care (Figure 23–3).

Figure 23–3 ICA sacrifice versus ICA preservation.

On the other hand, patients with giant ICA aneurysms are usually younger and have relatively less medical comorbidities when compared to patients with cervical carotid occlusive disease. Yet, in these cases, it is considered acceptable in neurosurgical practice to sacrifice the ICA. Long-term effects of deliberate carotid occlusion are not well studied. The risks of forming additional aneurysms, developing hemodynamic ischemic disease, and developing potential cognitive disorders have to be taken into account when this decision is made.

Therefore, it has been the practice of the senior author (SIA) to preserve flow to the hemisphere in the treatment of giant aneurysms, especially in younger patients.

Experience at St. Louis University Hospital in Treatment of Giant ICA Aneurysms

We performed a retrospective review of 55 consecutive patients treated at St. Louis University Hospital from June 1999 to June 2007. All 55 patients had transitional ICA aneurysms. The mean aneurysm size was 34.7 mm (range 25 to 70 mm). The mean age was 46 years (range 30 to 64 years). The mean follow-up period was 34.7 months (range 1 to 76 months). The objectives of this study were to assess the use of high-flow EC-IC bypass for the treatment of giant transitional ICA aneurysms, delineate surgical mortality and morbidity, and determine the long-term efficacy of the treatment and functional outcomes of these patients. The presenting symptoms were cranial neuropathy (42%), headache or incidental finding (40%), and SAH (18%) (Figure 23–4). The World Federation of Neurological Surgeons (WFNS) grade was 0 in 81%, 1 in 15%, 2 in 2%, and 3 in 2% (Figure 23–5). All 55 patients underwent a high-flow EC-IC bypass procedure.

Figure 23–4 Percentage of patients initially presenting with headache, cranial neuropathy, and SAH.

Figure 23–5 Initial WFNS grade at presentation.

Surgical technique

Craniotomy: A skull base approach, usually a cranio-orbital or a cranio-orbital-zygomatic access, is usually needed. We prefer a single-piece craniotomy, which entails an osteotomy of the orbital roof and lateral margins. A high-speed drill is used to thin the zygomatic arch posteriorly, which allows the radial artery to lie without kinking at the zygomatic area (Figure 23–6A).

Figure 23–6 A, Operative photograph shows simultaneous planning for the craniotomy, cervical incision, and radial artery harvest. B, Operative photograph shows exposure of the radial artery with superficial marking. C, Trans-sylvian preparation for anastomosis. M3 recipient branch with temporary clips. Radial artery donor graft is shown. D, Completed anastomosis is shown. E, Anastomosis of the radial graft to the ECA in the neck and temporary clips on ECA are shown. ECA, external carotid artery.

(From Abdulrauf SI: Extracranial-to-intracranial bypass using radial artery grafting for complex skull base tumors: technical note, Skull Base 2005;15:207-213, with permission.)

Exposure of the carotid artery in the neck: A standard incision anterior to the sternocleidomastoid muscle to expose the common, external, and internal carotid arteries (CCA, ECA, and ICA) is used. Vessel loops are applied around the CCA, ECA, and ICA. We recommend the use of the ECA as the site for the proximal anastomosis.

Radial artery harvest: The critical aspect of radial artery harvest is the length of the graft, which can be limiting. Obtaining maximal length is critical during this harvest. The senior author prefers to personally mark the superficial wall of the radial artery with a marking pen prior to removal of the graft. This step is crucial to avoid rotation during the tunneling (Figure 23–6B). Once the graft is harvested, it is placed in a heparinized saline solution.

Tunneling the graft: The graft is tunneled using a pediatric chest tube. The marked surface of the graft is kept most superficial.

Intracranial anastomosis: We also start the patient on aspirin (81 mg) daily for 3 days prior to surgery. Intraoperative continuous electroencephalography (EEG), somatosensory-evoked potential (SSEP), and motor-evoked potentials are monitored. The site of the anastomosis is determined based on several factors: intended revascularization territory, size of donor and recipient vessels, length of the graft, and location of the aneurysm. Mild hypothermia is used. EEG burst suppression using pentobarbital is maintained during the temporary clipping period. A color background is placed behind the recipient vessel. Temporary clips are applied (Figure 23–6C). An arteriotomy is made using an arachnoid knife. The arteriotomy is extended using a microscissors to the width of the donor vessel lumen. The lumen of the donor vessel is expanded by “fish-mouthing” the opening. We used 9-0 nylon for M2 and M3 vessels and 8-0 nylon for the supraclinoidal ICA. We prefer a running suture technique and performing the “back” wall (i.e., the more difficult anastomosis) first, followed by the front wall (Figure 23–6D). When the anastomosis is completed, retrograde flow is confirmed in the graft followed by positioning of a temporary clip on the graft just distal to the anastomosis.

Cervical carotid anastomosis: The graft length is cut to expose an area of the ECA where the proximal anastomosis is planned. Yasargil long temporary clips can be used for the ECA anastomosis. Similar technique of “back” wall and “front” wall can be utilized as described previously for the intracranial anastomosis. For this part, 7-0 prolene can be used (Figure 23–6E).

Graft inspection: Pulsatility of the graft is not enough to confirm graft potency. Micro-Doppler (Mizuho America, Inc., Beverly, MA) can be used. We now use ICG microscope-based angiography routinely for these cases. If the latter technology is not available, intraoperative angiography, in our opinion, is critical before parent vessel occlusion is performed. Flow probe technology (Transonic Systems, Inc., Ithaca, NY) has allowed us to estimate the amount of flow (cubic centimeter per minute) within the graft.

Parent vessel occlusion: Once the preceding steps, including intraoperative angiography, have documented flow in the graft, we then advocate parent vessel occlusion during the same surgical procedure, rather than delayed (staged) occlusion. In our opinion, the risk of graft occlusion would be high if competitive flow in the parent vessel were allowed to continue. We occlude the ICA at the level of the bifurcation in the cervical area and just distal to the giant aneurysm in the supra-clinoidal portion of the ICA. The distal occlusion must be performed proximal to the anterior choroidal and dominant posterior communicating arteries.¹⁸

Results of Giant Aneurysm Series

The outcome of this series shows that 50 patients (91%) had a Modified Rankin Scale (mRS) of 0 to 1, two patients (3.5%) had a mRS of 2 to 3, and three patients (5.5%) had a mRS of 4 to 5. Fifty-one patients (93%) had a Glasgow Outcome Scale (GOS) of 5, two patients (3.5%) had a GOS of 3 to 4, and two (3.5%), a GOS of 1 to 2. At discharge from the hospital, 49 (89%) of the patients went home, four (7%) went to rehabilitation facilities, and two patients (4%) went to nursing homes (Figure 23–7).

Figure 23–7 A total of 92.7% of patients had good GOS, 90.9% had none to no significant disability, and 89.1% went home. Only one patient died, which accounts for the 1.8% mortality.

Acute graft occlusion occurred in four patients (7.3%), and late graft occlusion in four (7.3%). The main complication/morbidity was reflected in our cerebrovascular accident (CVA) rate, which occurred in four patients (7.3%). Two patients had CVA secondary to acute graft occlusion, and two had CVA secondary to microsurgical manipulation of calcified aneurysms. Aneurysm recurrence was seen in only one patient (Figure 23–8). Mortality occurred in one patient from a pulmonary embolus at home 5 weeks postoperatively.

Figure 23–8 A, Fusiform aneurysm (involves the entire wall) of the lateral ICA segment. Patient failed BTO within 60 seconds. B, Immediate postoperative angiogram showing graft with nonsymptomatic vasospasm. C, Six-month follow-up showing end-to-end bypass (patient is asymptomatic.) D, One-year follow-up showing progression of disease into the distal ICA. E, Lateral view ICA injection showing the progression. F, Lateral view vertebral artery injection showing new formation of aneurysm in distal ICA. G, ICA injection following endovascular coiling of the aneurysm through the posterior communicating artery (PCA). H, Vertebral artery injection following endovascular coiling through the PCA. I, CCA injection following coiling showing the bypass as well as complete resolution of the aneurysm. J, At 1-year follow-up, patient is asymptomatic and aneurysm is completely treated.

Options for treatment of giant ica aneurysms

Traditional treatment of giant aneurysms was direct microsurgical clipping. This continues to be a feasible option in certain cases. However, the risk of direct clipping of giant aneurysms is not low. Our review of major series of direct clipping of giant ICA aneurysms revealed a fair to poor outcome in approximately 18% of the patients. In these same series, the mortality rate was 11% (Table 23–2). Endovascular treatment of giant aneurysms also poses certain challenges. In our review of major series of coiling, stent plus coiling of giant aneurysms reveals that approximately 42% of the aneurysms are completely occluded by the treatment. Thirty-seven percent of the aneurysms recanalize. Major morbidity occurred in approximately 21% of the patients. Mortality occurred in 15% of the patients (Table 23–3).

EC-IC bypass for giant aneurysms in the major published series shows relatively better outcomes than direct microsurgical clipping or endovascular treatment. Based on our review of these major series, excellent to good outcome was achieved on average in 84% of the patients. Significant morbidity was seen on average in 11% of the patients. Mortality was seen on average in 5% of the patients (Table 23–4).

Technical nuances in high-flow ec-ic bypass surgery

Importance of Atypical Appearance of Giant Aneurysms

Irregular appearance of the wall, or the pattern of more than one sac, indicates partial calcification or thrombosis. The appearance of the aneurysm on cerebral angiography is a critical factor in decision making regarding treatment. In the experience of the senior author, complex aneurysms, including those with irregular appearance of the wall, outpouching within the dome, or the presence of calcification, may carry a higher risk with direct clipping. Partial thrombosis of the aneurysm may show a smaller aneurysm on angiography when compared to the MRI. Partially thrombosed aneurysms also carry a risk of embolic complications during microsurgical clipping or endovascular coiling (Figure 23–9).

Figure 23–9 Importance of the atypical appearance of giant aneurysms: Irregular appearance of the wall, or the pattern of more than one sac should indicate partial calcification or thrombosis. A, DSA of partially thrombosed giant ICA aneurysm. B, DSA angiogram of partially calcified and partially thrombosed giant ICA aneurysm. C, DSA of a partially thrombosed and partially calcified ICA aneurysm.

Aneurysm size: The size of the aneurysm, although a critical factor when considering direct microsurgical clipping or endovascular coiling, is not an equally important factor when considering EC-IC bypass. In our opinion, for significantly large aneurysms, EC-IC bypass would be the least risky procedure (Figure 23–10).

Figure 23–10 Treatment of a 9-cm “mega-giant” aneurysm using EC-IC bypass. A, CT of a 51-year-old female presenting with speech difficulties and hemiparesis. B, Lateral view of DSA showing aneurysm. C, Anteroposterior view showing aneurysm. D, Contralateral DSA shows no flow through anterior communicating artery (ACA). E, Intraoperative angiogram showing radial artery to MCA bypass. F, Postoperative angiogram. G, Postoperative DSA showing bypass and clip reconstruction of the aneurysm and the preservation of the PCA.

EC-IC bypass for giant cavernous segment ICA aneurysm: The location of the aneurysm is an important factor when making decisions regarding treatment. Endovascular stenting plus coiling or EC-IC bypass are potential treatments of a giant cavernous segment aneurysm. Direct surgical clipping should not be considered in these cases, as it would almost certainly lead to ophthalmoplegia (Figure 23–11).

Figure 23–11 EC-IC bypass for giant cavernous segment ICA aneurysm. A, Axial T1+gad showing cavernous aneurysm in 45-year-old female presenting with ophthalmoplegia. B, Sagittal T1+ gad. C, DCA of giant aneurysm. D, Intraoperative angiogram of ICA radial artery graft. E, Postoperative angiogram showing radial graft and occlusion of the cavernous aneurysm.

End-to-side versus end-to-end proximal anastomosis: For the proximal anastomosis, both end-to-end or end-to-side are options. The senior author prefers the use of the ECA as the donor vessel. This avoids temporary occlusion of the ICA during the procedure. The advantage of end-to-end anastomosis is, presumably, more vigorous flow into the graft. The disadvantage of end-to-end anastomosis is potential occlusion of ophthalmic-based collaterals into the surpraclinoidal carotid artery. End-to-side anastomosis, therefore, is a reasonable option, and it is an easier anastomosis to make in comparison to end-to-end (end-to-end may create a size mismatch that may in certain occasions be difficult to compensate for) (Figure 23–12).

Figure 23–12 A, End-to-side radial artery graft to the ECA. B, End-to-end radial artery graft to the ECA.

Competitive flow: It is important to recognize that during intraoperative angiography, the graft may only supply a single division of the recipient territory (i.e., a single M2 division). This should not be a concerning sign. In general, this is due to the fact that there is significant competitive flow coming through the ACA from the contralateral side, which is protective, and the surgeon should not change the strategy during the case (Figure 23–13).

Figure 23–13 Intraoperative angiogram of an ECA to MCA radial artery bypass showing flow into a single MCA division.

Radial artery graft enlargement over time as graft adapts to blood flow demands: The diameter size of the graft as seen during intraoperative catheter or ICG is not concerning as long as there is no occlusion or specific area of stenosis. In our experience, the graft will expand in diameter over time to accommodate for blood flow demand (Figure 23–14).

Figure 23–14 A, Lateral three-dimensional DSA reconstruction of a giant ICA transitional segment aneurysm. B, Anteroposterior three-dimensional DSA reconstruction of a giant ICA transitional segment aneurysm. C, Intraoperative angiogram showing the bypass and deliberate occlusion of the ICA. D, At 1-year follow-up, DSA showing increased diameter of the graft.

Intraoperative failure of graft: In most situations where the graft is not visible during intraoperative angiography, technical failure is assumed, and the anastomosis, as well as the tunneling, should be reinvestigated. In patients who have passed the BTO, it is possible to have such significant competitive flow that the resistance in the graft cannot match the higher contralateral flow and the graft is not necessary. It is important to look at every step of the procedure to ensure that there is no technical failure before making any other decisions. If no technical failures are found and no changes in the patient’s motor and sensory evoked potentials are detected, it is reasonable to leave the graft in place. In certain circumstances, the graft may enlarge over time if demand is placed on it. While in other situations, the graft would be occluded without any neurological symptoms based on the fact that competitive flow was significantly strong and the graft was not needed to start with (Figure 23–15).

Figure 23–15 A, Three-dimensional DSA reconstruction of complex ICA partial thrombosed aneurysm. B, Intraoperative failure to establish flow with no change in SSEPs and motor-evoked potentials C, Immediate postoperative reconstruction showing graft is patent but small diameter. D, Immediate postoperative CTA showing small diameter graft. E, At 3-month follow-up, CTA reconstruction showing the expanded graft diameter.

Creation of a new posterior communicating artery: EC-IC bypass surgery is an intellectual exercise given the complexity of the aneurysm. In certain situations, an intraposition graft may be needed. In some cases, an IC-IC bypass may be more appropriate than an EC-IC bypass. In other cases, the creation of a new ACA or PCA (using an interposition graft) may aid in the treatment of the specific aneurysm, whether it is microsurgical or endovascular (Figure 23–16).

Figure 23–16 A, Patient with a third SAH following previous endovascular coiling. B, Anteroposterior DSA showing the coil embedded in the L P1 segment C, A/P DSA L ICA showing new P-Com artery. D, Vertebral artery DSA showing PCA flow completely dependant on the P1. E, ECA to PCA bypass postoperative DSA showing graft. F, Postoperative DSA showing flow to the PCA. G, Postoperative lateral view showing a PCA to radial artery graft showing PCA flow completely coming through the graft.

Length of the graft and risk of occlusion: The length of the graft is also an important aspect. Unneeded length may lead to kinking in the cervical or cranial areas and could be a risk factor for graft occlusion. This aspect has to be well studied during the operation, as this is an important variable in achieving success in EC-IC bypass surgery (Figure 23–17).

Figure 23–17 A. DSA of the R CCA showing a radial artery bypass for a giant aneurysm. The graft redundancy in the cervical area may be risky from a kinking standpoint as shown in this case. B. DSA of the R CCA showing a radial artery bypass for a giant aneurysm with ideal length of the graft that would minimize the risk of kinking.

Distal anastomosis size mismatch: From a technical standpoint of the distal anastomosis, it is important to match the size of the donor and recipient arteries. In our opinion a significant size mismatch could have a higher risk of turbulent flow and subsequent thrombosis at the anastomosis site (Figure 23–18).

Figure 23–18 A. DSA angiogram of a radial artery bypass to the MCA showing ideal size match. B. DSA angiogram of a radial artery bypass to the MCA showing significant size mismatch.

Conclusion

Giant intracranial aneurysms carry a high risk of morbidity and mortality. They are among the highest-risk disease processes within the field of neurosurgery. These aneurysms are potentially curable. Advances in microsurgical clipping, endovascular treatments, and EC-IC bypass have all contributed to decreasing the morbidity of these treatment modalities.

Evolving techniques in EC-IC bypass have documented a measurable decrease in the morbidity of treating these complex lesions. Minimally invasive EC-IC bypass techniques currently being developed will add to the armamentarium that will lead to less morbidity while achieving a cure.