Microsurgical Relations between Internal Carotid Artery–Posterior Communicating Artery (ICA-PComA) Segment Aneurysms and Skull Base: An Anatomoclinical Study

Abstract

Purpose The study of the clinical, anatomic, imaging, and microsurgical characteristics of the aneurysms of the internal carotid-posterior communicating artery (ICA-PComA) segment and their relationships with the skull base structures.

Methods The anatomic relationships of PComA with neurovascular elements and skull base structures were studied in cadavers. The clinical, imaging, and microsurgical findings of 84 microsurgically treated ICA-PComA aneurysms compiled in a prospective database were reviewed.

Results The most important anatomic relations of the PComA and ICA-PComA aneurysms are with the oculomotor nerve around the oculomotor triangle that forms the roof of the cavernous sinus. Aneurysms of the ICA-PComA are classified according to the orientation of the aneurysmal sac in infratentorial, supratentorial, and tentorial. Infratentorial aneurysms frequently present with subarachnoid hemorrhage (SAH) and oculomotor nerve paralysis. They have relations with skull base structures that often make it necessary to totally or partially resect the anterior clinoid process (6.7%) or anterior petroclinoid dural fold (15%). Supratentorial aneurysms course with SAH and without oculomotor nerve involvement, but they often are associated with intracranial hematoma.

Conclusion ICA-PComA aneurysms have complex anatomic relations. The orientation of the aneurysmal fundus induces relevant differences in the anatomic relations, clinical presentation, and microsurgical approach to ICA-PComA aneurysms.

Introduction

Internal carotid-posterior communicating artery aneurysms (ICA-PComA aneurysms) are lesions that arise around the origin of the posterior communicating artery from the internal carotid artery. Although ICA-PComA aneurysms account for more than 20% of all intracranial saccular aneurysms nowadays, the neurosurgical interest on these lesions based on their high incidence has declined due to the indication for endovascular coiling treatment for most of them. Some ICA-PComA aneurysms are easily visualized and clipped by using a standard pterional microsurgical approach. However, ICA-PComA aneurysms possess complex and variable anatomical relationships, making a microsurgical approach hazardous and dangerous in some cases. Aneurysms of the ICA-PComA develop in the carotid cistern, and they are—or may be—intimately related to relevant neural and vascular elements. Moreover, similar to what happens in ICA paraclinoid aneurysms, ICA-PComA aneurysms may also be closely related to some skull base structures, specifically the anterior clinoid process (ACP), posterior clinoid process (PCP) or dorsum sellae, and dural folds that extend between the clinoid processes, sphenoid bone, and petrous apex. These anatomic relations vary and should be familiar to any neurosurgeon working in this area. The objective of this study has been to review the anatomic relationships of ICA-PComA aneurysms with the skull base. The first part was a cadaveric dissection study of the region where ICA-PComA aneurysms arise and grow. The second part was a clinical study of imaging techniques and microsurgical findings from a series of patients with ICA-PComA aneurysms treated using microsurgical techniques.

Methods

Anatomic Study

Ten sides of five heads were used in the anatomic study. The arterial vessels were injected with red silicone. To minimize the distortion of the anatomic elements, the carotid cistern was approached from above after eliminating the cerebral peduncles and sectioning the ICA just above the bifurcation. Some brains were studied from their basal face after the skull was removed. The specimens were studied and dissected using microsurgical techniques and a Zeiss Pico microscope (Carl Zeiss Corp., Oberkochen, Germany).

Clinical Study

A consecutive series of aneurysms of the ICA-PComA that were operated on by the first author was reviewed. All the aneurysms were clipped via a pterional approach using standard microsurgical techniques. Each case had been included in a prospective file opened at the time of patient admission and closed 1 year after hospital discharge. Each record included numerous data on the demographic and clinical parameters, imaging and microsurgical findings, follow-up, and images with diagrams of the most relevant intraoperative findings, photographs, and video recordings. The demographic, clinical, and imaging data retrieved for the study included age, gender, degree of subarachnoid hemorrhage (SAH) at admission according to the scale of the World Federation of Neurological Surgeons (WFNS),¹ preoperative or postoperative paresis and/or paralysis of the oculomotor nerve, SAH Fisher grade² and, as applicable, location of the intracranial hematoma at admission, total number of aneurysms diagnosed and, finally, the association of a fetal type PComA on the same side of the operated lesion. In every case, the orientation of the aneurysmal sac dilation was determined exactly. The lesions were grouped according to the main direction of the aneurysmal sac projection determined in the coronal plane using the straight anteroposterior angiography projection or three-dimensional reconstructions of computed tomography (CT) or magnetic resonance imaging (MRI) angiography. The anatomic relations of the aneurysm with neurovascular and the skull base structures were established by reviewing the drawings, photographs, and videos made during surgery.

Results

Anatomic Study

Vascular Relations

The PComA emerges from the ICA at approximately half the distance between its origin and its bifurcation. The PComA originates on the posterior wall of the ICA, generally at a point where the artery turns slightly in lateral and superior direction. The PComA passes backward and medially and slightly above and medial to the oculomotor nerve before merging with the posterior cerebral artery (PCA). In our study we found two PComAs of fetal type (defined as arteries with a diameter equal to or greater than the ipsilateral P1 segment of the PCA). These arteries were unilateral and had a more superior but also lateral path with respect to the oculomotor nerve (Fig. 1D).

Figure 1.

Microsurgical anatomy of the relationships of the posterior communicating artery (PComA). (A) Anatomic view of the standard pterional approach, with a long supraclinoid internal carotid artery (ICA). The oculomotor nerve is visible under the carotid artery as it goes toward the cavernous sinus, and the PComA remains hidden behind the ICA. (B) Anatomic view of the pterional approach in a more posterior direction. The entrance of the oculomotor nerve in the cavernous sinus through the oculomotor triangle is visible. The PComA is visualized behind the ICA as it goes toward the P1 segment of the posterior cerebral artery. (C) Posterolateral anatomic view of the relations of the PComA with the structures of the skull base and oculomotor nerve. The ICA is short and the PComA is of fetal type. The dissector separates the anterior petroclinoid fold to show the entrance of the oculomotor nerve in the oculomotor triangle. (D) Posterolateral anatomic view of the relations of the PComA with the structures of the skull base and oculomotor nerve. The ICA is very short, the ACA is hypoplastic, and the PComA is of fetal type with an infundibular implantation. The PComA is easily visualized. PComA originates practically at the level of the tip of the anterior clinoid process. The relations of the PComA with the oculomotor triangle and oculomotor nerve are visible. ACA, anterior cerebral artery; AchA, anterior choroidal artery; ACP, anterior clinoid process; APCF, anterior petroclinoid fold; ICA, internal carotid artery; IIn, optic nerve; IIIn, oculomotor nerve; IIIv, third ventricle; MCA, middle cerebral artery; PComA, posterior communicating artery; temporal lobe, anteromedial aspect of the temporal lobe; uncus, uncus of the temporal lobe.

Neural Relations

The main neural relations of the PComA are with the oculomotor nerve and the medial aspect of the temporal lobe (uncus). The oculomotor nerve emerges from the cerebral peduncle in the depth of the interpeduncular fossa (Figs. 1C and 1D). The nerve passes below the PCA and over the superior cerebellar artery and then takes an anterior, lateral, and slightly downward direction, occupying an inferomedial position in relation to the uncus and a lateral position with respect to the PComA. The nerve is lodged in the oculomotor cistern and enters the cavernous sinus through its roof (oculomotor triangle), lateral to the posterior clinoid process and medial to the anterior petroclinoid fold (APCF), a band of dura mater that extends from the edge of the tentorium to the ACP (Fig. 1B). The oculomotor nerve enters through the dura mater at a variable distance from the point where the ICA exits through the dural ring (mean: 5 mm; range: 2 to 7 mm). The PComA is also related to the medial part of the temporal lobe; specifically, the uncus. However, we did not find any PComA in direct contact with any part of the uncus.

Skull Base, Dura, and Arachnoid Relations

The PComA crosses the carotid cistern and the external arachnoid aspect of the lower wall of the carotid cistern and it is related to the skull base, specifically to the dura mater that covers the posterior clinoid process and cavernous sinus. The oculomotor nerve is contained in the oculomotor cistern, which houses it from the point where it leaves the cerebral peduncle to the point where it enters the roof of the cavernous sinus in the oculomotor triangle (Fig. 1). The oculomotor triangle of the cavernous sinus lies between the dural folds formed between the anterior and posterior clinoid processes (interclinoid fold) and between the anterior and posterior clinoid processes and the petrosal apex (anterior and posterior petroclinoid folds). In this area, the limit between the supratentorial and infratentorial spaces is marked by the ACP and the APCF.

Clinical Study

A total of 84 patients were included in the series, 68 women (71.4%) and 16 men (28.6%). Mean age at the time of surgery was 54.2 ± 14.9 years. At admission, the WFNS grade of the patients was as follows: grade 0 in 18 (21.4%); grade 1 in 33 (39.4%); grade 2 in 10 (11.9%); grade 3 in 6 (7.1%); grade 4 in 10 (11.9%); and grade 5 in 7 (8.3%). Oculomotor nerve deficit was present at the time of surgery in 11 patients and developed in the postoperative period in 6 patients. SAH on the CT at admission was of the following Fisher's grades: grade 0 in 24 patients (28.6%); grade 1 in 11 (13.1%); grade 2 in 12 (14.3%); grade 3 in 13 (15.4%); and grade 4 in 24 (28.6%). Fourteen patients had an intracranial hematoma associated with SAH at admission. The location of the hematomas was as follows: eight in the temporal lobe; two in the frontal lobe; two in the subdural space; and two with combined subdural and ipsilateral temporal lobe hematomas. The number of aneurysms diagnosed with the different study techniques ranged from one to three per patient (two aneurysms in 14 patients and three aneurysms in three patients). Imaging studies showed a fetal type PComA on the same side of the aneurysm in 31 cases (36.9%).

The orientation of the aneurysmal fundus was identified in the coronal plane using imaging studies. The most frequent projection of the aneurysms was inferior (43 cases, 51.1%), followed by the inferolateral (18 cases, 21.4%) and lateral directions (15 cases, 17.9%). Less frequent directions of the aneurysmal projection on the coronal plane were superolateral (four cases), superior (three cases), and inferomedial (two cases). None of the aneurysms had a medial or superomedial direction. As mentioned, the supratentorial or infratentorial position of the dome of each aneurysm was determined at surgery in relation to the tentorial plane formed by the ACP and APCF (Fig. 2). The aneurysmal fundus was infratentorial in 60 cases (71.4%) and supratentorial in 22 cases (26.2%). The location of the aneurysmal dome was considered strictly tentorial in the remaining two cases (2.4%). At surgery, the axial relationships of the infratentorial aneurysms were studied analyzing the position of the neck along the tentorial incisura by the necessity to remove part of the ACP or of the APCF to visualize the proximal part of the aneurysmal neck to have enough room to place the anterior blade of the clip. Total or partial intradural clinoidectomy had to be performed in four patients (6.7%) because of the very proximal location of the aneurysm. In nine patients (15%) a partial resection of the petroclinoid fold was sufficient due to the more distal location of the aneurysm.

Figure 2.

ICA-PComA segment aneurysms. (A) Microsurgical photography of a right supratentorial internal carotid artery-posterior communicating artery (ICA-PComA) aneurysm (>) buried in the temporal lobe (TL) after dissection of the medial aspect of the entire traject of the internal carotid artery. (B) Microsurgical photograph of an left infratentorial ICA-PComA aneurysm (<), which is hidden under the anterior petroclinoid fold (APCF) but posterior to the anterior clinoid process (ACP).

Overall, the most frequent lesion found at surgery in our series was an aneurysm with an infratentorial orientation. Actually, a total 60 patients in the series (71.4%) had infratentorial aneurysms. Almost all of them had an inferior, inferolateral, or lateral projection of the sac on the coronal plane. Twenty-five cases were associated with a fetal type PComA (41.7%). Sixteen patients (26.7%) in this group developed oculomotor nerve deficits before or after surgery, and in only one case was it definitive. It was a patient with a large and partially thrombosed infratentorial aneurysm, with preoperative paresis worsened after surgery due to the severing of the oculomotor nerve during the dissection of the aneurysmatic sac. Forty-five patients (80%) had SAH and six patients (10%) had associated temporal, subdural, or subdural and temporal intracranial hematoma. Supratentorial aneurysms were identified at surgery in 26.2% of cases (22 patients), most of which had a lateral, superolateral, or superior projection on the coronal plane. Only in six patients was the supratentorial aneurysm associated with a fetal type PComA (27.3%). Fifteen patients (77.3%) presented with SAH and only one patient (4.5%) had oculomotor nerve paralysis. Eight patients (36.4%) had associated intracranial hematoma: in six patients with laterally projecting aneurysms the hematoma was temporal or subdural, and in the remaining two cases with superiorly projected aneurysms, the hematoma was into the frontal lobe. The variables were statistically analyzed for group differences using Chi-2 and Wilcoxon tests, and statistical significance was determined at p ≤ 0.05. The infratentorial group showed a significant number of cases with preoperative and/or postoperative oculomotor paresis or paralysis (p < 0.05) and low-grade SAH (WHNS grades 1 and 2) (p < 0.05) and the supratentorial group showed a significant number of intracranial hematomas (p < 0.001). The distribution of the projections of the aneurismal sac in coronal plane is also statistically different when both groups are compared (p < 0.001).

Discussion

Aneurysms of the intracranial ICA usually are classified on the basis of the main branch of the ICA around which they originate. Aneurysms that develop around the origin of the PComA are known as aneurysms of the ICA-PComA segment, or ICA-PComA aneurysms. In our experience, the aneurysmal fundus orientation is particularly important when considering the anatomic and microsurgical relations of the aneurysm. In the case of aneurysms of the ICA-PComA segment, this subject has been taken into account by some authors. Yasargil recognized five categories of ICA-PComA aneurysms according to the orientation of the aneurysmal fundus: anterolateral, superolateral, superior posterolateral (supratentorial), inferior posterolateral (infratentorial), and inferior posteromedial.³ More often, only two subtypes are considered, grouping them by their supratentorial or infratentorial projection of the dome.⁴ Supratentorial aneurysms are related to the temporal uncus and infratentorial aneurysms to the oculomotor nerve. Nevertheless, the orientation of the aneurysmal fundus on the axial plane along the incisural plane must also be considered, since it has relevant microsurgical implications.

Anatomic Relations of ICA-PComA Aneurysms with the Skull Base

Our anatomic study showed that aneurysms that originated in the ICA-PComA segment may be related to many structures because they develop in the carotid cistern. The anatomic relations of the PComA and of the ICA-PComA segment aneurysms have been studied in detail by Rhoton^5,6 and Inaoue et al.⁷ Nevertheless, in our study we placed special emphasis on the relationships of infratentorial aneurysms of the ICA-PComA with the skull base. An important point is the relation between PComA and the oculomotor triangle, where the oculomotor nerve passes through the roof of the cavernous sinus and enters the sinus. It is interesting that these anatomic relations cannot usually be appreciated in the standard pterional microsurgical approach when dealing with these aneurysms or other local pathology, nor can they be detected in most anatomic studies. Only the approach used in our dissection strategy affords a more posterolateral view that clearly reveals the intimate relations between the point where the PComA emerges from the ICA and where the oculomotor nerve enters the cavernous sinus (Fig. 1). Although the PComA is lodged in the carotid cistern and the oculomotor nerve in the oculomotor cistern, the nerve may be compressed at this point by an ICA-PComA aneurysm when it reaches more than 4 to 5 mm.⁸ The adult type PComA has a more medial direction than the fetal type PComA, which has a larger caliber and more lateral location, closer to the oculomotor nerve. Consequently, aneurysms associated with fetal type PComA can compress the oculomotor nerve more easily. When infratentorial aneurysms of the ICA-PComA originate proximally, the relations of the aneurysm with the skull base are with the ACP and APCF and the aneurysm may be hidden underneath these structures. The length of the ICA is therefore a critical point, as it determines where the PComA originates on the axial plane (Fig. 1). On a short ICA, an aneurysm of the ICA-PComA is more likely to be related to the ACP. In contrast, on a long ICA the artery occupies a more lateral and superior position in the carotid cistern, the origin of the PComA is more superior and any aneurysm that may develop is more likely to project supratentorially. Some of these relations can be adequately demonstrated in preoperative imaging studies, especially with three-dimensional reconstruction of CT angiography, where bone structures can be assessed. During the microsurgical procedures for ICA-PComA aneurysms, clipping a high percentage of infratentorial aneurysms requires total or partial resection of these skull base structures.^{9,10,11,12,13} Kim et al,¹⁰ in a series of 117 aneurysms, resected the ACP in 4.3% and the APCF in 6.8% of cases. These authors indicated that the ACP must be resected when the distance between the proximal side of the aneurysmal dilation and the tip of the ACP is less than 5 to 6 mm or the ACP is large enough to obscure the proximal portion of the aneurysmal dilation. Park et al¹² had to perform anterior clinoidectomy in 6.4% of a series of 94 ICA-PComA aneurysms. They concluded that the distance between the aneurysm and ACP and the tortuosity of the ICA have predictive value for the need for anterior clinoidectomy. In our experience, resection of ACP or the APCF was necessary, respectively, in 6.7% and 15% of infratentorial aneurysms, corresponding to a total of 15.5% of aneurysms in our series. Intradural clinoidectomy is highly recommended in neurovascular surgery to avoid an uncontrollable rupture of the aneurysm. Moreover, in our series, the convenience to resect the ACP or the APCF was decided always intraoperatively based in the microsurgical findings and therefore it was done intradurally. For clinoidectomy usually it was enough a partial resection of the ACP just to place the proximal blade of the clip or to gain room to assure the proximal control of the ACI and in any of our cases the proximal ring was opened.

Conclusion

Aneurysms of the ICA-PComA segment have complex anatomic relations. Their anatomic relations with skull base structures such as the oculomotor triangle, ACP, and APCF are especially relevant. In a percentage of cases, achieving safe clipping of the aneurysm or proximal control of the ICA requires total or partial resection of the ACP or APCF. However, only some of these relations can be known from preoperative imaging studies, and the surgeon must be well versed in the microsurgical anatomy of the area to perform safe clipping.