Introduction
Distal anterior cerebral artery (DACA) aneurysms are located distal to the anterior communicating artery (AComA) on the A2-A5 segments of the anterior cerebral artery (ACA).12) Aneurysms rarely occur in the DACA and account for approximately 5% of all intracranial aneurysms. Most of them arise at the bifurcation formed by the origin of the callosomarginal artery (CMA) from the pericallosal artery.3)14)24)26) The clinical features of these aneurysms are unusual, including subarachnoid hemorrhage (SAH) with intracerebral hematoma (ICH), multiplicity and association with vascular anomalies such as azygous ACA.6) Moreover, these aneurysms lead to some unique operative difficulties, including a narrow surgical field, the need to secure the bridging veins, orientation of the pericallosal artery, broad-necked small aneurysms and dense adhesion of the aneurysms to the cingulate gyri. These difficulties could cause premature rupture of the aneurysm before the vascular anatomy is identified.24)
In this report, we present detailed angiographic findings and treatment outcomes of 33 patients diagnosed with DACA aneurysms.
Materials and Methods
Thirty-three patients with DACA aneurysms underwent surgery or endovascular treatment at our institution between September 1992 and January 2010. We performed a review of the clinical and radiologic records of all patients with DACA aneurysms.
Clinical data included initial Hunt and Hess grade (H-H Gr.), Fisher grade, the time interval between ictus and surgical clipping (or coil embolization) and modified Rankin Scale (mRS) at discharge. Radiologic data included aneurysm location, size, association with any ACA anomaly or other congenital vascular anomaly and presence of multiple aneurysms.
The anatomic location of the DACA aneurysm is described by Fischer's division of the ACA into five segments: A1-A5 (Fig. 1).4)27) The A3 segment is subdivided into three segments based on location of the genu (A3A), infracallosal (A3I) and supracallosal (A3S).
Of the 33 patients, 29 were surgically treated and four patients received endovascular treatment. For the surgically treated group, we performed unilateral craniotomy and approached the aneurysm via an interhemispheric route in all cases. Unruptured aneurysms in patients with multiple aneurysms were treated in a second scheduled operation. In the endovascular treatment group, 1 patient was treated by stent-assisted coil embolization (Fig. 3) and the other patients were treated by the two-catheter technique.
The radiographic outcomes of the surgical treatment were assessed by postoperative computed tomography angiography (CTA) and/or digital subtraction angiography (DSA) 1-2 weeks after the operation. The outcomes of the endovascular treatment were assessed by immediate post-embolization angiography. Follow-up magnetic resonance angiography (MRA) was inspected for aneurysmal recanalization 6 months postoperatively.
mRS was used to assess the clinical outcomes for all patients at the time of discharge and at 6 months post-operatively.
Results
1. Clinical characteristics
We identified 33 patients (3.1%) with 35 DACA aneurysms from 1106 surgically treated aneurysm patients. There were 19 women (57%) and 14 men (43%) and the mean age was 53.8 years (Table 1). Twenty-four patients had ruptured aneurysms and nine had unruptured aneurysms.In the ruptured cases, 22 patients were categorized as good grade (H-H Gr. I–III) and 2 patients were rated as H-H Gr. IV (Table 2). We performed early surgical clipping (or coil embolization) within 72 hours after ictus to prevent rebleeding and aggressively managed vasospasm (Table 3). Sixteen (67%) of the 24 ruptured cases scored a Fisher grade III and IV SAH, with as many as 7 (29%) having an ICH (Fisher grade IV) on CT scan. Eight patients scored Fisher grades I and II.
2. Radiologic characteristics
In patients with ruptured aneurysms, SAH was diagnosed based on the findings from CT scans and ICH was identified in seven of the 24 (29%) patients.
All patients underwent DSA and 35 DACA aneurysms were identified in 33 patients. Of these 2 patients had 2 DACA aneurysms. The distribution of the aneurysms along the DACA is shown in Table 4.
Eighteen aneurysms (51%) arose from the origin of the callosomarginal artery, 14 (40%) arose from the frontopolar branch, 2 (6%) arose from the orbitofrontal artery and 1 (3%) arose from the distal pericallosal (A4) area. According to Fischer's division, the aneurysms were distributed as follows: 5 aneurysms were located in A2, 28 in A3 and 2 in A4. We further divided the A3 segment according to its relationship with the genu of the corpus callosum (GCC) into A3S (superior), A3A (anterior) and A3I (inferior). This demonstrated that most of the 28 A3 aneurysms were located in the A3A segment. Table 5 presents the distribution of the 35 DACA aneurysms according to their anatomic location. The A3 segment was the most frequent location in agreement with the findings of other studies. Anterior A3 was the most frequent location in relation to the GCC.
All size measurements are presented in Table 6. The size of the aneurysms ranged from 2~14 mm and these were divided into small (<6 mm), medium (6~10 mm), large (11~25 mm) and giant (>25 mm). The mean size of the 35 aneurysms was 4.2 mm. Thirty (85%) of the aneurysms were <6 mm in diameter and giant aneurysms were not detected.
The presence of additional aneurysms or other vascular anomalies was also determined by angiography. Multiple aneurysms were detected in 9 patients (27%) and of these, 8 patients had one additional aneurysm and 1 patient had 2 additional aneurysms; in all, 10 aneurysms were identified. The locations of the associated aneurysms were the middle cerebral artery (MCA; n=5), pericallosal artery (n=2), anterior communicating artery (n=1), vertebral artery (n=1) and basilar tip (n=1).
Association with vascular anomalies was noted in 6 patients (18%). In five patients, aneurysms were associated with congenital DACA anomalies (four azygous ACA, one bihemispheric ACA); 1 patient was diagnosed with Moyamoya disease (Table 7).
3. Surgical outcomes
All of the patients with ruptured aneurysms underwent early surgery or endovascular treatment within 72 hours of onset to avoid the risk of rebleeding. Clipping was successfully performed in 28 of the 29 patients who underwent surgery and aneurysm wrapping was carried out in the remaining patient. The four patients who underwent endovascular treatment were successfully treated by coil embolization. There were no cases of residual sac or parent artery occlusion.
No patient suffered premature rupture during the dissection of the aneurysm or the coiling procedure. In patients with multiple aneurysms, 4 unruptured MCA aneurysms were clipped during the second operation; clipping was performed for two patients who had other pericallosal aneurysms in the same operative field (Fig. 4). Furthermore, one basilar tip aneurysm was coiled. All coil-treated aneurysms in the patients with multiple aneurysms were simultaneously coiled (MCA, AComA and vertebral artery dissection; Fig. 5).
Outcomes at discharge were as follows: the mRS scores were 0, 1, 2, 3 and 4 for 8, 12, 4, 5 and 1 patient(s), respectively. One patient died from sepsis due to infective colitis. One patient who underwent surgery complained of urinary incontinence and the other one patient in whom coiling was performed experienced mild motor weakness; however, all these symptoms were transient. Of the two patients who had an unfavorable outcome (mRS 5), one had sepsis related to pneumonia and the other had a cerebral infarction related to vasospasm, despite their preoperative status of H-H Gr. II.
Among the seven patients who had ICH, two patients had a poor H-H grade (lower than grade 3). The diameter of the ICH ranged from 1-3.2 cm. In the two patients with H-H Gr. IV who had SAH with ICH, the patient presenting the largest diameter had an unfavorable outcome (mRS 4).
Favorable outcomes (mRS < 4) were observed in 29 of the 33 patients (Table 2) and no mortality or morbidity was directly related to the aneurysmal surgery or coiling. There was no change in the clinical outcomes at the 6-month follow-up evaluation.
Discussion
DACA aneurysms are infrequent, accounting for 2.1-9.2% (average, 5%) of all intracranial aneurysms reported.2)6)8)14)16)18)24)26)30)31)33) The incidence of DACA aneurysms in our study was 2%, less than the average incidence reported previously. Most studies, including ours, involved females.
The anatomic course of the ACA is described by Fischer's division of the ACA into five segments: A1-A5 (Fig. 1).4)27) The A1 segment is the section between the bifurcation of the internal carotid artery and the AComA. The A2 segment extends from the AComA to the region between the rostrum and GCC. The A3 segment curves around the GCC and ends at the rostral section of the corpus callosum body. The A4 and A5 segments follow the superior surface of the body of the corpus callosum with a virtual plane of division at the level of the coronary suture. Furthermore, the ACA is divided into a proximal (segment A1) and distal part (segments A2-5) also known as the pericallosal artery.5)9)19)22)29)32)
A3 aneurysms can be further divided into three groups with the GCC as the anatomic landmark for this division (Fig. 2).13) Aneurysms at each of these locations require a modified microsurgical approach: (1) inferior A3 aneurysms are located in the proximal part of the A3 segment inferior to the GCC, (2) anterior A3 aneurysms are located in the central part of the A3 segment anterior to the GCC and (3) superior A3 aneurysms are located in the distal part of the A3 segment superior to the GCC.13) In our study, 28 aneurysms (80%) were located in A3 segment and most were located in the A3A segment.
DACA aneurysms are more frequently associated with intraparenchymal hemorrhage than the aneurysms at the other sites, with an average of 46.2% and up to 73%.14)32) The small pericallosal cistern and the close relationship of these aneurysms with the adjacent cerebral cortex could be plausible causes for the ICH.28) Miyazawa et al.18) carried out multiple logistic regression analysis in a large series of patients with ruptured distal ACA aneurysms and reported that the most significant factors affecting outcome were the clinical grade just before operation and the timing of the operation. They also found that ICH with a diameter >3 cm and a poor preoperative grade lead to poor outcomes. Oshiro et al.20) documented that ICH appears to have negative implications not only because of poor preoperative status but also the close apposition of the frontal lobe and the corpus callosum to the aneurysm and the limited subarachnoid space adjacent to these aneurysms. In our series, seven patients (29%) had ICH, of which two scored poor H-H grades (lower than grade 3) and a patient who had the largest ICH diameter evolved to an poor outcome (mRS 4). These results are in accordance with those of previous studies.18)20)
Many authors have indicated an increased incidence of multiple aneurysms in patients with DACA aneurysms. Steven et al. found that 10 major reports induding the present report described 43% of 400 patients had one or more additional intracranial aneurysms. The most frequent site was the middle cerebral artery (42%), followed by the internal carotid artery (24%). Additional DACA aneurysms were identified in 16% of patients.3)6)7)20)24-26)28)31)32) In our series, nine patients (27%) had multiple aneurysms, with the middle cerebral artery bifurcation aneurysm being the most frequently identified type (56%).
In general, aneurysms at the DACA are rather smaller than those at other sites.3)6)7)19) In our series, 20 of 24 (84%) ruptured aneurysms were small (diameter, <6 mm); moreover, small aneurysms (ruptured and unruptured) were found in 30 of 33 (86%) cases. In contrast, large aneurysms were found in only two of 33 (5%) cases. The low incidence of large DACA aneurysms can be explained by the tendency of DACA aneurysms to rupture before they turn large or gigantic.6) In the current study, most of the DACA aneurysms (94%) measured <10 mm in diameter. We achieved acceptable clinical outcomes with aggressive treatment. Therefore, DACA aneurysms require active treatment, even if they have been incidentally discovered and measure <10 mm in diameter.
Yasargil12)31) described the following special features of DACA aneurysms: (1) reduction in the operative space in the interhemispheric space and pericallosal cistern; (2) dense adhesion between the cingulate gyri making the separation and location of the aneurysm difficult; (3) sclerotic wall and broad base of the aneurysm; (4) origin of the branching arteries at the neck and attachment of the dome to the opposite pericallosal artery; (5) difficult preoperative decision on the parent A3; (6) attachment or embedding of the dome in the pial layer of the cingulate gyrus; (7) location of the aneurysm at the bifurcation of an azygous pericallosal artery. Additional difficulties during the surgery for DACA aneurysms include preservation of the bridging vein, frontal expansive ICH, small size of the aneurysm making correct clip placement difficult and difficult proximal control.15) Projection of the aneurysmal dome toward the surgeon and broad-based sclerotic aneurysms make establishment of proximal control very difficult, especially in case of the infracallosal type of DACA aneurysm at the origin of the callosomarginal artery.8) Previously, several authors recommended an anterior interhemispheric approach or a bifrontal basal anterior interhemispheric approach to safely achieve proximal control.1)11)21)
In this study, all patients were operated on by unilateral craniotomy and a right-side interhemispheric approach, and good outcomes were obtained. To select the shortest route, we measured the position of the aneurysm in relation to the exterior of the cranium to obtain exact head positioning and bone flap placement. In cases of inferior A3 and A2 aneurysms, we performed a more basal interhemispheric exposure to achieve proximal control safely. We believe that the unilateral approach is less invasive, rapid and allows sufficient exposure of the DACA, even in the case of an infracallosal aneurysm (A2, A3I), compared to a bifrontal basal anterior interhemispheric approach.
The number of endovascular options has increased as coiling technology continues to advance. However, early attempts to apply such treatments were unsuccessful, because of the distal location and the inability to control microcatheters during aneurysm catheterization. One study suggested a coiling success rate of only 25% (two of eight patients).23) Since then, smaller microcatheters and shapeable microwires have allowed interventionalists to access these lesions.17) The availability of balloon and stent assistance has increased the endovascular options for wide-necked lesions.
In our series, four patients were successfully treated by coiling. There was no evidence to indicate superiority of coiling over surgical clipping. There are few reports concerning studies on endovascular treatment, especially of DACA aneurysms. Our study thus sheds new light on this area, although it has a limitation in the form of the small number of patients.
Conclusion
DACA aneurysms have a tendency to rupture before turning large or reaching a gigantic size. Microsurgical clipping is a safe and effective treatment method and endovascular treatment can be an alternative treatment strategy for DACA aneurysms. We emphasize that DACA aneurysms should be treated positively even if they are <10 mm in diameter and operating early can reduce the rate of rebleeding.
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