Paraclinoid Carotid Aneurysms: Surgical Management, Complications, and Outcome Based on a New Classification Scheme

ABSTRACT

The site of origin, projection, and relationship of aneurysms arising from the ophthalmic segment of the internal carotid artery (ICA) to adjacent structures are heterogeneous. Based on a retrospective analysis of 61 patients with aneurysms in this location, we developed a simple numerical classification system to guide surgical planning. We used angiographic findings to categorize the aneurysms. We followed the nomenclature of the carotid segments by Bouthillier et al (Neurosurgery 1996;38:425–432), C4 being the intracavernous ICA, C5 the clinoidal segment, and C6 the ophthalmic segment of the ICA. The aneurysms were divided into four major types: Types Ia and Ib projected superiorly and arose from the dorsal surface of C6. Type Ia was related to the ophthalmic artery. Type Ib aneurysms were sessile and had no branch relations. Type II aneurysms were related to the ventral wall of the C6 segment without any branch relation. Type IIIa variant arose from medial wall of the C6 segment and was related to the superior hypophyseal artery. Type IIIb arose from the medial wall of the C5 segment below the dural reflection without any branch relation. Large type IV aneurysms arose from the C5 and C6 segments, widening the distal dural ring. Patients' postoperative status and visual and overall outcomes were analyzed. Ultimately, this classification helped us to plan operative approaches and clip selection.

The complex anatomy of the paraclinoid internal carotid artery (ICA) makes the surgical management of aneurysms arising from this segment difficult. The key features of successful surgical treatment of these lesions include establishing control of the proximal artery, adequate exposure of the aneurysm neck, and successful obliteration of the aneurysm with minimal manipulation of the optic nerve.¹ Accurate preoperative assessment of the origin of these lesions is critical for determining the surgical approach. We reviewed 61 patients with paraclinoid aneurysms who were treated surgically and discuss the surgical technique, complications, and outcome, based on a new practical numerical classification scheme.

MATERIALS AND METHODS

In this study we used Bouthillier and associates' nomenclature² of the carotid segments, C4 being the intracavernous ICA, C5 the clinoidal segment, and C6 the ophthalmic segment of the ICA. We reviewed our operative experience with 61 paraclinoid ICA aneurysms treated in 49 females (mean age, 50.6 years) and 12 males (mean age, 46 years) between 1994 and 1999 at the Detroit Medical Center. We obtained patients' clinical information from their charts and reviewed their arteriograms. Each patient underwent cerebral angiography to determine the size, shape, and exact configuration of his or her aneurysm. Preoperative management and surgical technique were similar to that described elsewhere.³

Initial Management

Patients with symptoms of subarachnoid hemorrhage (SAH) were admitted to the intensive care unit. Their clinical condition was classified according to the Hunt and Hess grading system. Systemic arterial pressure, central venous pressure, and pulmonary arterial and wedge pressures were monitored. Cardiac output, cardiac index, and systemic vascular resistance were optimized for each patient. All patients received phenytoin and nimodipine.

Preoperative Radiological Evaluation

The extent of hemorrhage was graded on computed tomography (CT) scans according to the Fisher classification system.⁴ The presence or absence of hydrocephalus was noted. A ventriculostomy was performed only if impaired consciousness was associated with the hydrocephalus. Most patients underwent thin–section CT of the clinoidal region with bone windows to determine whether calcification was present within the aneurysm wall and ICA, or if there was any evidence of erosion of the clinoid process.

Cerebral Angiography

Cerebral angiography permitted the direction of projection and size of the aneurysm to be assessed. Based on this information, aneurysms were classified into one of the four types (Table 1). Types Ia, Ib, II, and IV were best visualized on lateral projections (Figs. 1, 2, 3, 4); type III was best visualized on anteroposterior and submentovertical projections. Type Ia aneurysms arose from the superior ophthalmic segment of the ICA and were related to the ophthalmic artery. They were either medial or lateral to the optic nerve and projected superiorly. Type Ib aneurysms arose from the superior ophthalmic segment of the ICA, had no branch relations, projected superiorly, and were lateral to the optic nerve. Type II aneurysms arose from the ventral ophthalmic segment of the ICA and had no branch relations. The dome often projected inferiorly into the cavernous sinus roof. Type IIIa aneurysms arose from the medial ophthalmic segment of the ICA and were related to the superior hypophyseal artery. They projected medially over the dorsum sella. Type IIIb aneurysms arose from the medial clinoidal segment of the ICA, below the dural reflection. They were related to superior hypophyseal artery yet were infradiaphragmatic and projected medially. Type IV aneurysms were often large and involved the ventral clinoidal and ophthalmic segment of the ICA. They had no branch relations and widened the distal dural ring.

Table 1.

Classification of Paraclinoid Aneurysms

	Carotid		Branch
Type	Segment	Surface	Relation	Comments
Ia	C6	Superior	Ophthalmic	Medial or lateral to ON
Ib	C6	Superior	None	Lateral to ON
II	C6	Ventral	None	Dome projects into CS roof
IIIa	C6	Medial	SHA	Carotid cave aneurysm projects over DS
IIIb	C5	Medial	SHA	Transitional aneurysm infradiaphragmatic
IV	C5, C6	Ventral	None	Giant aneurysm extends between C5 and C6 segmentsWidens distal dural ring

CS, cavernous sinus; DS, diaphragma sella; ON, optic nerve, SHA, superior hypophyseal artery

Figure 1.

Types Ia and Ib variants arise from the dorsal surface of the C6 segment of the carotid artery seen here on a lateral projection. Type Ia aneurysms are closely related to the ophthalmic artery (OA) origin. Type Ib aneurysms have no branch relation and are often sessile. Type II variants arise from the ventral surface of the C6 segment without any branch relation. Type III aneurysms project medially.

Figure 2.

Anteroposterior view of the carotid arteries. Types IIIa and IIIb aneurysms (supra– and infradiaphragmatic types) are closely related to the superior hypophyseal artery (SHA) origin. They arise on the medial surface of C5 and C6 segments. DS, diaphragma sella.

Figure 3.

Type IV aneurysms are large broad–based aneurysms extending from the distal C4 segment to the proximal C6 segment. They widen the distal dural ring.

Figure 4.

Typical angiographic pictures of each type of aneurysm. Types I (A), II (B), and IV (D) are best visualized on lateral angiographic projections and type III (C) on anteroposterior projections.

Balloon Test Occlusion and Single Photon Emission CT

Patients harboring large or giant aneurysms, especially a type IV variant or an aneurysm with extensive calcification, underwent balloon test occlusion (BTO) with systemic hypotension and single photon emission CT (SPECT) to evaluate the patient's tolerance for carotid occlusion as a definitive therapy and to assess the need for a bypass procedure. If a patient tolerated the test occlusion clinically and SPECT revealed no perfusion defects, permanent balloon occlusion of the ICA and trapping of the aneurysm were offered as definitive therapy. Patients who failed the BTO or who had significant perfusion defects on SPECT received a vascular bypass. If the superficial temporal artery (STA) was greater than 1.5 mm in diameter, an STA–to–M2 segment of the middle cerebral artery (MCA) bypass was performed; if the STA was less than 1.5 mm, a venous bypass graft was placed from the cervical ICA to the M2 segment of the MCA.

Magnetic Resonance Imaging and Magnetic Resonance Angiography

Magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) helped determine the exact dimensions of aneurysms filled with thrombus. Coronal MRI and MRA of the sellar area helped differentiate type IIIa from IIIb, that is, the supra– and infradiaphragmatic variants of paraclinoid aneurysms. This knowledge was helpful in planning the extent of diaphragmatic division needed to expose the aneurysm adequately. The infradiaphragmatic variant was visualized only after the diaphragm sella was divided around the superior surface of the dome of the aneurysm.

Timing of Surgery

Surgery was delayed for patients classified as Hunt and Hess grade V and for those with multiple systemic problems (e.g., sepsis or aspiration pneumonia) until their clinical grade or general condition improved. Those classified as Hunt and Hess grades I to IV underwent surgery within 24 hours of admission.

Operative Procedure

In all cases, an ipsilateral pterional craniotomy with orbital osteotomy and anterior clinoidectomy³ was performed. The neck was included in the sterile operative field. The angle of the mandible and the anterior margin of the sternocleidomastoid muscle were marked after sterile preparation so that the carotid artery could be compressed digitally or exposed for proximal control, trapping, or a venous bypass procedure. Proximal control was attained by exposing the ICA at one of three sites: the cervical carotid artery if the aneurysm was large and encroached on the cavernous sinus; the cavernous carotid; or the clinoidal segment of the ICA.

For type Ia aneurysms, the optic canal sheath was incised longitudinally and the carotid artery was displaced laterally. With large aneurysms, proximal control was achieved by exposing the cavernous or clinoidal segment of the ICA. Most type Ia aneurysms projected superiorly and could be clipped with a 45–degree angled clip (Fig. 5).

Figure 5.

Diagrams illustrating the type of clip used to treat each type of aneurysm.

Type Ib aneurysms were broad based and sessile and therefore were difficult to obliterate. Mobilization of the carotid artery with circumferential division of the distal dural ring followed by proximal and distal temporary clipping slackened the segment of the carotid enough to allow satisfactory placement of the clip.

To facilitate gentle medial retraction of type II aneurysms, the optic nerve sheath was incised longitudinally. The distal dural ring along the floor of the optic canal was incised, and the cavernous segment was mobilized laterally for proximal control. Typically, a right–angled fenestrated clip was used (Fig. 5).

Preoperatively, it was usually difficult to determine whether a type III aneurysm was projecting above or below the diaphragma sella. To view the supradiaphragmatic variant, the optic nerve sheath was incised and the optic nerve was gently retracted medially. Proximal control was achieved in large aneurysms by exposing the cavernous–carotid segment. The supradiaphragmatic variant aneurysm was usually clipped with a 90–degree angled fenestrated clip applied from a lateral direction. Because the infradiaphragmatic variant was usually under the diaphragm, it was not visualized despite lateral displacement of the ophthalmic segment of the ICA. In these situations, the distal dural ring was incised circumferentially around the carotid artery and extended medially across the diaphragma sella, leaving a cuff of the dura attached to the periphery of the aneurysm. The roof of the cavernous sinus was exposed during this process. The pituitary gland was identified medial to the aneurysm. A 90–degree curved fenestrated clip (placed encircling the ICA) effectively obliterated the aneurysm.

For type IV aneurysms, the optic nerve sheath was incised and the nerve was retracted medially. The medial dura was incised along the roof of the cavernous sinus medial to the oculomotor nerve, and the nerve was retracted laterally. The distal dural ring, which often had been widened by the large aneurysm along with the dura on the roof of the cavernous sinus, was incised around the aneurysm. After the clinoidal and ophthalmic segments were mobilized, a temporary clip was placed on the cavernous and ophthalmic segments to trap the aneurysm. A right–angled fenestrated clip typically was used to encircle the carotid artery (Fig. 5). Often, multiple serial clips were needed to obliterate the entire length of the aneurysm neck. The aneurysm was collapsed with a 25–gauge needle and the first clip was removed. Temporary clips were removed after patency of the carotid artery was restored and the aneurysm was obliterated.

RESULTS

Type Ia aneurysms were most common (43 %), followed by type IIIa (21 %), type IIIb (11 %), type II (11 %), type Ib (8 %), and type IV aneurysms (6 %). Eighteen (28 %) patients suffered multiple vascular anomalies, including additional aneurysms or arteriovenous malformations (AVMs). Fifty–five percent of the aneurysms were small (< 1 cm), 40 % were large (1 to 2.5 cm), and 5 % were giant (> 2.5 cm). Common presenting symptoms included headaches (almost all patients), SAH (23 %), and visual changes (20 %). Of the 61 patients, 58 underwent successful surgical clipping of their aneurysms and 3 underwent bypass procedures. The latter three had either giant or unclippable (fusiform) aneurysms.

Complications and Outcomes

Three patients died. Two patients had presented with Hunt and Hess grade IV SAH. The third patient, who had a giant aneurysm, developed cerebral infarction and ultimately died. Overall, 57 patients (93 %) had a good long–term outcome (i.e., Glasgow Outcome Scale score of 4 to 5 at 6 months).

Of 35 patients who had preoperative and postoperative visual assessment at 6 months, 28 patients (80 %) had no change in their visual status, 3 patients' visual acuity decreased after surgery, and 2 patients' field defects worsened. Three patients, two of whom harbored type III aneurysms, developed ipsilateral visual loss with light perception only. In seven patients, transient third nerve palsy developed and resolved 6 months after surgery. No particular variant was associated with a specific postoperative visual complication (Table 2).

Table 2.

Pre– and Postoperative Findings on Visual Examination in 35 Patients and Correlation with Type of Aneurysm

Patient No.	Aneurysm Type	Preoperative Visual Exam	Postoperative Visual Exam
1	Ia	Normal	Decreased visual acuity
2	IIIa	Normal	No change
3	II	Normal	Transient CN III palsy
4	II	Normal	No change
5	IV	Normal	Transient CN III palsy
6	IIIa	CN III, IV palsies	No change
7	IIIb	Decreased visual acuity	Ipsilateral light perception only
8	IIIa	Decreased visual acuity	Ipsilateral light perception only
9	IV	Normal	No change
10	IIIa	Normal	No change
11	Ia	Normal	No change
12	Ia	Normal	Transient CN III palsy
13	II	Normal	No change
14	Ia	Normal	No change
15	Ia	Normal	Decreased visual acuity, ipsilateral inferior nasal field defect, transient CN III palsy
16	IIIa	Normal	No change
17	Ia	Normal	No change
18	Ia	Normal	Ipsilateral light perception only
19	Ib	Normal	No change
20	Ia	Normal	No change
21	IIIb	Normal	Decreased visual acuity, ipsilateral nasal field defect
22	Ia	Normal	No change
23	IIIb	Ipsilateral peripheral visual field defect	No change
24	Ia	Normal	Transient CN III palsy
25	Ia	Normal	No change
26	IIIa	Normal	No change
27	IIIb	Normal	Transient CN III palsy
28	Ia	Normal	No change
29	IIIb	Normal	No change
30	Ia	Ipsilateral inferior nasal quadrantanopsia	No change in visual field, transient CN III palsy
31	IIIa	Normal	No change
32	Ia	Normal	No change
33	Ia	Normal	No change
34	Ia	Contralateral homonomous hemianopsia, decreased visual acuity	No change
35	II	Normal	No change

CN, cranial nerve

DISCUSSION

Classification of Paraclinoid Aneurysms

Paraclinoid aneurysms often fail to follow the classic teachings about aneurysmal development, branch vessel origin, or hemodynamic origin. Multiple classification systems of these lesions have been proposed (Table 3).^{1, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20} The earliest report on carotid–ophthalmic aneurysms as a distinct entity written in 1968 by Drake et al offered no classification scheme.²¹ Kothandaram et al proposed the first classification scheme in 1971.¹¹ Based on intraoperative observations, they classified carotid–ophthalmic aneurysms into three groups according to their relationship with the optic chiasm: subchiasmal, suprachiasmal, and parachiasmal. In 1976, Almeida et al. classified their experience with carotid–ophthalmic aneurysms into two groups, again based on the relation between the aneurysm and optic chiasm: latero–optochiasmatic and sub–optochiasmatic.¹⁵ Also in 1976, Thurel et al. added two other groups: suprachiasmal and global types.²²

Table 3.

Proposed Classification Compared with Previous Classification Schemes for Paraclinoid Aneurysms

Author (year)	Classification Scheme	Basis of Classification
Kothandaram et al11	SubchiasmalSuprachiasmalParaclinoid	Intraoperative findings
Almeida et al15	Latero–optochiasmaticSuboptochiasmatic	Angiographic findings
Thurel et al22	SuprachiasmalGlobal	Intraoperative findings
Day8	Ophthalmic arterySuperior hypophyseal (paraclinoid)Superior hypophyseal (suprasellar)	Angiographic findings
Al–Rodhan et al7	SupraophthalmicOphthalmicInfraophthalmicTransitionalCavernous	Angiographic and intraoperative findings
Batjer et al2	Carotid–ophthalmicSuperior hypophysealProximal posterior carotid	Angiographic findings
Kumon et al6	SubchiasmaticLateral chiasmaticSuprachiasmaticCarotid caveParaclinoid	Angiographic findings
De Jesus et al5	ClinoidOphthalmicSuperior hypophysealPosterior paraclinoid	Angiographic findings
Barami et al (current study)	Ophthalmic artery (Ia)Dorsal ICA (Ib)Ventral ICA (II)Supradiaphragmatic (IIIa)Infradiaphragmatic (IIIb)Clinoid segment of ICA (IV)	Angiographic findings

ICA, internal carotid artery.

In 1990 Day classified his series of paraclinoid aneurysms into three groups: ophthalmic artery aneurysms, superior hypophyseal–paraclinoid aneurysms, and superior hypophyseal–suprasellar aneurysms.⁸ In 1993 Al–Rodhan and associates classified paraclinoid aneurysms into five groups based on angiographic and intraoperative observations: supraophthalmic, ophthalmic, infraophthalmic/supracavernous, transitional, and cavernous.⁷ They further classified the lesions based on the position of the neck and dome of the aneurysm. In 1994, Batjer et al classified carotid–ophthalmic aneurysms into three groups: ophthalmic artery, superior hypophyseal artery, and proximal posterior wall of ICA.¹ In 1997 Fries et al added “partially intracavernous aneurysms” to Batjer's classification.²³ That year Kumon et al classified paraclinoid aneurysms into five groups: subchiasmatic, lateral chiasmatic, suprachiasmatic, carotid cave, and paraclinoid.⁶ Most recently, in 1999, De Jesus et al classified carotid–ophthalmic aneurysms into four groups: clinoid, ophthalmic, superior hypophyseal, and posterior paraclinoid.⁵

We found that most classification schemes were too broad or impractical to allow preoperative planning. We therefore classified these lesions based on their angiographic appearance. Specifically, we grouped them based on the relation of the neck of the aneurysm to the ICA segment of origin and on the direction that the aneurysm projected. Dividing these aneurysms into the discrete subtypes identified several important features that we believe are critical for preoperative planning and choice of clip selection: the relationship of the aneurysm to the branching vessels and perforators, optic nerve, falciform ligament, oculomotor nerve, diaphragma sella, dural rings, anterior clinoid, and cavernous sinus.^{8, 24, 25, 26, 27, 28}

Technical Considerations

Although the contralateral and interhemispheric approaches have been described before for the treatment of paraclinoid lesions,²³ we used the ipsilateral pterional craniotomy with orbital osteotomy in all cases. Review of our series identified several pitfalls that deserve special attention.

During clipping of type Ia aneurysms a carotid segment could be so ectatic that the neck of the aneurysm was medial to the optic nerve. In these instances, the tuberculum sella was drilled medial to the optic nerve. After drilling, the optic nerve was retracted laterally and the clip was applied from its medial aspect. During clipping of type Ib aneurysms, a portion of the parent vessel was occasionally included in the clip blades. The base was very friable and might have been avulsed when the clip blades were approximated.

When some type II aneurysms were clipped, a second fenestrated clip was placed parallel to the first one to occlude the neck and completely obliterate the aneurysm. If the aneurysm projected deeply into the cavernous sinus, the dura of the roof of the cavernous sinus that encircled the aneurysm prevented the clip blades from approximating each other. In these situations, dura forming the roof of the cavernous sinus was incised circumferentially around the waist of the aneurysm, allowing the clip blades to close and occlude the neck of the aneurysm.

Type IV aneurysms (especially in elderly patients) may contain significant calcification in the vessel wall. Attempts to clip a heavily calcified aneurysm can be dangerous because of the risks of avulsion of the aneurysm, embolic phenomena with ischemic complications, or the inability to obliterate the aneurysm. If a calcified aneurysm is encountered and if the patient has no SAH, the procedure can be terminated or a bypass procedure performed, followed by endovascular balloon occlusion of the ICA.³

The anterior clinoid process and optic strut can be pneumatized and must be recognized while drilling. The sinus communication must be obliterated before closure. A small fat graft obtained from deep temporal fat or the abdomen is secured with fibrin glue. The frontal sinus entry should always be identified and managed appropriately. The sphenoid sinus and the posterior ethmoid sinuses also may be opened during clinoidectomy and should be recognized and obliterated.

Patency of the carotid artery is easily evaluated with microDoppler ultrasonography after aneurysm obliteration. In large and complex aneurysms, intraoperative angiography is performed.

Finally, optic nerve injury is one of the most common complications after surgical treatment of paraclinoid aneurysms. Caution must be exercised when the optic canal is unroofed. The dura overlying the optic canal must not be disrupted. Moreover, the pial vessels of the optic nerve must not be disrupted while the dura is incised. Retraction of the optic nerve must be brief and minimal. Before incising the dura on the distal dural ring and the floor of the optic canal, the ophthalmic artery must be identified to avoid its inadvertent injury.