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Computed tomography angiography in detection and characterization of ruptured anterior cerebral artery aneurysms at uncommon location for emergent surgical clipping
Journal of Clinical Imaging 30 (2006) 87 – 93
Computed tomography angiography in detection and characterization of ruptured anterior cerebral artery aneurysms at uncommon location for emergent surgical clipping Chia-yuen Chena, Shu-Chiang Hsieha, Wai-Man Choia, Pei-yeh Chiangb, Jerry Chin-Wei Chiena, Wing P. Chana,c,4 a
Department of Radiology, Taipei Medical University –Municipal Wan Fang Hospital, 111 Hsing-Long Road, Section 3, Taipei 116, Taiwan, ROC Department of Neurosurgery, Taipei Medical University –Municipal Wan Fang Hospital, 111 Hsing-Long Road, Section 3, Taipei 116, Taiwan, ROC c Department of Radiology, School of Medicine, Taipei Medical University, 250 Wu-Hsing Street, Taipei 110, Taiwan, ROC
b
Received 10 August 2005; received in revised form 7 September 2005; accepted 7 September 2005
Abstract Introduction: Cerebral subarachnoid hemorrhage may result from rupture of saccular aneurysms at uncommon location [excluding the anterior communicating artery (ACOM)] of the anterior cerebral artery (ACA). The purpose of this study was to evaluate the usefulness of helical computed tomography angiography (CTA) in detection and characterization of intracranial aneurysms at such uncommon locations before emergent surgical clipping. Materials and methods: Between 1998 and 2003, records for 50 consecutive patients who underwent emergent surgical clipping for intracranial aneurysms were reviewed. Eighteen of these patients had aneurysms in the ACA. After those patients with unequivocal ACOM aneurysms were excluded, eight patients with eight aneurysms in an uncommon location of the ACA were recruited to this study. Plain computed tomography (CT) and CTA were performed in eight patients, and digital subtraction angiographies were done in three patients. Each aneurysm was evaluated for the detection, quantification, and characterization of the aneurysms with 2D multiplanar reformatted and 3D volume-rendering techniques. Results: There were two small aneurysms arising from the A1 segment, one from the A2 segment, two at the junction of triplicated ACAs, two at the junction of A2 and A3 segments, and one at the junction of A2 and A3 segments of the azygos ACA. The average diameter of the aneurysmal sac was 4.44 mm (range, 2.7–7.0 mm), and the aneurysmal neck averaged 2.59 mm (range, 1.2–3.5 mm) in size. The smallest aneurysm measured 2.21.82.7 mm (neck, 1.2 mm) in the A1 segment of the left ACA. Three patients had intracerebral hematoma, seven had intraventricular hemorrhage, and three had acute hydrocephalus. Conclusion: Aneurysms in uncommon locations of ACAs exhibited characteristic features. Rupture of these aneurysms can cause intracerebral hematoma, intraventricular hemorrhage, and/or acute hydrocephalus. Noninvasive CTA can reliably detect and characterize intracranial aneurysms at such uncommon location for planning of emergent surgical intervention. D 2006 Elsevier Inc. All rights reserved. Keywords: Aneurysm; Anterior cerebral artery; CT angiography, subarachnoid hemorrhage
1. Introduction
4 Corresponding author. Department of Radiology, Taipei Medical University–Municipal Wan Fang Hospital, 111, Hsing-Long Road, Section 3, Taipei 116, Taiwan, ROC. Tel.: +886 2 2930 7930x1300; fax: +886 2 2931 6809. E-mail address: [email protected] (W.P. Chan). 0899-7071/06/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.clinimag.2005.09.022
The subarachnoid hemorrhage (SAH) due to ruptured aneurysm accounted for 2.1% of stroke patients and the reported surgical mortality rates ranged from 7.7% to 12.5% of patients in Taiwan [1]. Selective intraarterial digital subtraction angiography (DSA) has been used as a diagnostic standard for the detection and characterization
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Table 1 Plain CT findings of eight patients with aneurysms in uncommon location of ACA Case
Age/sex
Location of aneurysm
ICH
IVH
Hydrocephalus
Midline shifting
SAH
1
64/F
No
I–IV
Mild
No
Left BA= left SY= IHF N MCAF = QGP
2
73/F
No
No
Left BA= left MCAF N left SY= left AM
41/F
Bilateral lateral horns I–III
Mild
3
Mild
No
IHF N SYN MCAF = BA= QGP
4 5
49/M 55/F
Minimal Moderate
No No
IHF N BA= MCAF = SY IHF N BA= SY N MCAF = QGP
68/M
I–IV
Severe
No
IHF N BA
7
70/F
No Bilateral frontal lobe Bilateral frontal lobe No
No I–IV
6
I–IV
Mild
No
IHF N SY= MCAF N BA
8
59/M
A1 segment of the left ACA A1 segment of the left ACA Four aneurysms including the left A2 segment Triplicated ACA Two aneurysms including triplicated ACA Junction of A2 and A3 segment of the left ACA Junction of A2 and A3 segment of the right ACA Junction of A2 and A3 segment of azygos ACA
Bilateral frontal lobe
I–IV
Moderate
No
IHF N BA= MCAF = SY= QGP
No
ICH, intracerebral hematoma; IVH, intraventricular hemorrhage; BA, basal cistern; SY, sylvian fissure; MCAF, middle cerebral artery fissure; IHF, interhemispheric fissure; QGP, quadrigeminal plate cistern; AM, ambient cistern.
of intracranial aneurysms, with false-negative rate of detection 5% to 10% [2]. Obtaining less than optimal projection with angiographic equipment may limit detection of some intracranial aneurysms [3,4] or measurement of the aneurysmal neck relating to the parent artery, impairing selection of the treatment method [3,4]. Other disadvantages of DSA include the invasiveness of arterial puncture and intraarterial catheter manipulation, and that it is a time-consuming procedure and that the devices are expensive. Helical computed tomography angiography (CTA) is a new noninvasive volumetric imaging technique. By using optimized acquisition and postprocessing protocols, the sensitivity of CTA in the detection of very small (b 5 mm) cerebral aneurysms is higher than that of DSA, with equal specificity and higher interoperator reliability [4]. Imaging acquisition of CTA requires only 1 min or less, thereby benefiting high-risk patients.
Cerebral SAH may result from rupture of saccular aneurysm of anterior cerebral artery (ACA), which is commonly originated from anterior communicating artery (ACOM). Only 0.88% of all intracranial aneurysms have been reported to have originated from the A1 segment and 5.3% from the distal ACA [5,6]. Anterior cerebral artery aneurysm in such uncommon locations is usually associated with multiple aneurysms and vascular anomalies and may exhibit a similar appearance to ACOM aneurysm rupture on plain computed tomography (CT) [5,6]. The surgical approach of these aneurysms is different from those of the other anterior circulation aneurysms [6]. Previous CTA studies have reported only 14 aneurysms at such uncommon locations in a total of 545 intracranial aneurysms [4,7 – 16]. The purpose of this study was to evaluate the usefulness of plain CT and helical CTA in detection and characterization of intracranial aneurysms at such uncommon location before emergent surgical clipping.
Table 2 Computed tomography angiographic findings of eight patients with aneurysms in uncommon location of ACA Case
Location of aneurysm
CTA
Sac size (mm)
Neck size (mm)
Cal/thom
DSA
Surgery
Surgical approach
1
A1 segment of the left ACA
Positive
3.12.0
3.5
No
Positive
Clip
Left pterional
2
A1 segment of the left ACA
Positive
2.72.2
1.2
No
Positive
Clip
Left pterional
3
Left A2 segment
Positive
6.14.9
3.2
No
N/A
Clip
Left pterional
4
Triplicated ACA
Positive
3.53.3
2.5
No
N/A
Clip
Left pterional
5
Triplicated ACA
Positive
7.04.6
2.5
No
N/A
Clip
Right pterional
6
Junction of A2–3 segment of the left ACA Junction of A2–3 segment of the right ACA Junction of A2–3 segment of azygos ACA
Positive
6.04.0
2
No
N/A
Clip
Interhemispheric
Positive
2.92.2
3.3
No
Positive
Clip
Interhemispheric
Positive
4.24.0
2.5
No
N/A
Clip
Interhemispheric
7 8
Cal/thom, calcification/thrombus; N/A, not available
Status at follow-up Alive, after 27 months Alive, after 24 months Expired, after 1 month Alive, after 40 months Alive, after 5 months Alive, after 26 months Alive, after 10 months Alive, after 23 months
C.-y. Chen et al. / Journal of Clinical Imaging 30 (2006) 87 – 93
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2. Materials and methods 2.1. Patients Between 1998 and 2003, the records of 50 consecutive patients who underwent emergency aneurysm clipping for intracranial aneurysms were reviewed. Eighteen of them had aneurysms that occurred in the ACA. After exclusion of those patients with typical ACOM aneurysms, eight aneurysms at uncommon location of the ACA were recruited in this study. Plain CT and CTA were performed in all eight patients, and DSA was done in three patients. Plain CT and CTA images were reviewed without knowledge of DSA or surgical reports by a single experienced
Fig. 2. Case 3: Patient with a saccular aneurysm originating from A2 segment of the left ACA, in addition to a saccular aneurysm at ACOM and the other two at other locations (not shown). (A) Sagittal view, 2D multiplanar reformatted CTA image shows a saccular aneurysm with wide neck originating from A2 segment of the left ACA (arrow). (B) Threedimensional anteroposterior projection CTA image with lateral angulation shows a wide-based aneurysm from the A2 segment of the left ACA (arrow) and a bilobulated saccular aneurysm from ACOM (arrowhead). One branch of A2 segment originating from the proximal neck of aneurysm is well seen.
Fig. 1. Case 2: Patient with a small saccular aneurysm originating from A1 segment of the left ACA. (A) Midarterial phase anteroposterior projection DSA image shows a small saccular aneurysm at the proximal portion of the A1 segment of the left ACA (arrow). (B) Three-dimensional anteroposterior projection CTA image with caudal angulation shows a 2.7-mm aneurysm sac (arrow) in superior and medial direction with narrow neck. One small lenticulostriate artery from the aneurysm neck is well seen (arrowhead).
neuroradiologist (C.Y.C). Digital subtraction angiography images were read with CTA images by the same radiologist to see if DSA provided information additional to that of the CTA. Parameters for interpretation included detection, quantification, and characterization of ACA aneurysms at uncommon locations. Only aneurysms, defined as a saccular outpouching from a parent artery having a clearly definable sac and neck, were recruited in this study. Aneurysmal dilatations, defined as abnormal outpouching of an arterial wall but without a definable neck, were not considered as aneurysms. Infundibula, defined as a pyramidal dilatation at the origin of a vessel with an artery arising from the apex, were excluded.
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A triplication of ACA was defined as three branches arising from ACOM, including bilateral A2 segments of the ACA and an unusual branch of ACOM (or known as accessory ACA) distributed to one or to both hemispheres. Hydrocephalus was defined as a ventricular enlargement with rounded dilation of the superior-lateral portion of the frontal horns and temporal horn. Acute hydrocephalus was defined as a hydrocephalus associated with periventricular
hypodensity due to transependymal CSF resorption and/or intraventricular hemorrhagic clot in central lumen of the dilated ventricles. 2.2. Helical CTA All CTA examinations were performed using a helical technique on either one of the two CT scanners (Hi-Speed CT/I and Hi-Speed CT/FX, General Electric, Milwaukee, WI). All patients were positioned supine, with head immobilization achieved with adhesive tape. The delayed scanning time was 18 s. The helical technique included a pitch of 1.0 to 1.5 of 1-mm section collimation, 0.5-mm reconstruction interval, and a coverage from the level of 1 cm below sella floor to the upper margin of sylvian fissure. The average acquisition time was 60 s. Other imaging parameters included a matrix of 512512, a 150-mm field of view, 120 kV, and 260 to 290 mA. The administration of 100 ml nonionic contrast medium (Ultravist 300 I mg/ml, Schering) was injected by an intravenous route through a 20-gauge antecubital angiocatheter using a power injector at a rate of 3 cc/s. 2.3. Image processing Postprocessing of CTA images was performed using commercially available software in an independent workstation (Advantage Workstation version 4.0, General Electric). Three-dimensional perspective volume-rendered images, 3D thick slab and gray scale 2D single section, and thick slab multiplanar reformatted 2D images were evaluated. Single section 2D and thick slab 3D multiplanar reformatted images were used for detection and quantification of the aneurysmal sac and neck, and used for the determination of the presence, location, and extent of mural calcification and intraluminal thrombi with respect to the aneurysmal neck. Volume-rendered 3D images were used for the detection of intracranial aneurysm, the characterization of arterial branching patterns at the neck, the depiction of the position and spatial orientation of the aneurysmal neck and sac, and the depiction of the relationship of the aneurysm to local and regional bone anatomy.
Fig. 3. Case 5: Patient with a saccular aneurysm originating from triplicated ACA, in addition to other aneurysms at other locations (not shown). (A) Nonenhanced CT image shows dense intracerebral hematoma at the left frontal lobe, diffusely dense SAH in interhemispheric fissure, basal cistern, and bilateral sylvian fissure with localized hematoma formation (arrow). Intraventricular hemorrhage and hydrocephalus are noted. (B) Sagittal view, multiplanar reformatted CTA image shows an elongated aneurysm in superior and anterior direction from the junction of bilateral A1 segments (arrow). Three branches distal to ACOM are noted. Note the ability of CTA to visualize aneurysm in the setting of acute severe SAH with local dense hematoma. (C) Three-dimensional anteroposterior projection CTA image with lateral and caudal angulation shows the aneurysm sac (arrow) and the trifurcation (bilateral A2 segments and accessory ACA) arising from aneurysm neck (arrowheads).
C.-y. Chen et al. / Journal of Clinical Imaging 30 (2006) 87 – 93
The size of each aneurysm was measured in maximum projection of aneurysmal sac in 3D images. If more than one aneurysm was detected, the aneurysm that caused SAH (on the basis of the blood distribution as shown on unenhanced CT images) was selected for analysis in this study. 2.4. Digital subtraction angiography Digital subtraction angiography images were obtained in patients who underwent selective three- or four-vessel angiograms on frontal, lateral, and oblique projections. The CT angiograms were available to the angiographer as a reference guide for possible extra DSA projections.
91
Three patients received DSA within 24 h after CTA. In comparing DSA with CTA, there was no additional for any of the three patients. Microsurgery was performed in all patients in the acute stage; for seven of eight patients, it was performed within 48 h of their visit to our emergency department. All aneurysms were confirmed during operation. All patients were successfully treated by surgical clipping: three via interhemispheric approach and five via pterional approach.
3. Results There were eight patients (five women and three men) who presented with intracranial aneurysms in uncommon location of the ACA. Their age ranged from 41 to 73 years old (mean, 60 years old). All patients were sent to the emergency room with chief complaints of severe headache or loss of consciousness. Table 1 summarizes the patients’ data and plain CT findings. The emergent plain CT scan revealed an SAH in all patients, with the most increased density area in interhemispheric fissure in six patients and the unilateral basal cistern in two patients, relating to the location of ruptured aneurysms. Localized intracranial hemorrhage was seen in the bilateral frontal lobes of three patients. Seven of eight patients had intraventricular hemorrhage, and all eight patients suffered from various degrees of hydrocephalus; three patients had acute hydrocephalus. No patients had a mass effect causing midline shifting. Of the eight patients, two patients had multiple aneurysms (Table 1). Case 3 had four intracranial aneurysms, respectively, in the left A2 segment of the ACA, the ACOM, the junction of M1 and M2 segments of the left middle cerebral artery, and the cavernous portion of the right intracranial artery. Case 5 had two intracranial aneurysms, respectively, in a triplicated ACA and the junction of M1 and M2 segments of the right middle cerebral artery. All eight aneurysms were detected preoperatively by CTA, and all were confirmed at surgery and/or DSA (Table 2). There were two small aneurysms arising from A1 segment of the ACA (Fig. 1), one from the A2 segment (Fig. 2), two at the junction of triplication of the ACA (Fig. 3), two at the junction of A2 and A3 segments, and one at the junction of A2 and A3 segments of azygos ACA (Fig. 4). The average maximal diameter of the aneurysmal sac was 4.44 mm (range, 2.7–7.0 mm). The size of the aneurysmal neck averaged 2.59 mm (range, 1.2–3.5 mm). The smallest aneurysm measured 2.21.82.7 mm, with a neck measured 1.2 mm (Fig. 2), located in the A1 segment of the left ACA. Neither mural thrombus nor wall calcification was noted in any aneurysms.
Fig. 4. Case 8: Patient with a saccular aneurysm originating at the distal tip of azygos ACA. (A) Axial view, multiplanar reformatted CTA image shows azygos ACA and aneurysm in its distal end (arrow). Two cortical arteries arising from the distal portion of azygos ACA are seen. (B) Threedimensional anteroposterior projection CTA image with lateral angulation shows aneurysm sac, azygos ACA as a single A2 segment (small arrows), and paired A3 segments.
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One patient (Case 3) expired 1 month after surgical clipping due to postoperative ischemic insult and uncontrollable brain swelling. The other seven patients were discharged with stable clinical condition; clinical followup for 5 to 40 months (mean, 22.1 months) revealed no complications.
4. Discussion Cerebral SAH due to ruptured aneurysms often results in poor prognosis. Most of the patients die of rebleeding in additional to the initial intracranial hemorrhage [17]. Rebleeding can be prevented by early neurosurgical intervention. In our hospital, CTA has been employed as a first-line imaging modality in screening patients with SAH possibly caused by ruptured aneurysm. When ruptured aneurysm was detected in CTA, surgical clipping was performed to minimize rebleeding. Digital subtraction angiography was requested only for uncertainty about the presence of aneurysms. Our results indicated that CTA could be used to substitute DSA in screening patients with SAH and suspected ruptured intracranial aneurysms; a similar conclusion has been made by Velthuis et al. [18]. Digital subtraction angiography images provided no additional information compared with CTA. Computed tomography angiography can demonstrate the aneurysmal neck and relationship between the aneurysm and the parent artery even better than DSA. Van der Jagt et al. [19] suggested that the parenchymal cerebral hematoma was an excellent predictor for the site of a ruptured aneurysm. The next most useful predictor was blood distribution on CT in patients with a ruptured ACA aneurysm or ACOM aneurysm, with sensitivity of 0.79, specificity of 0.97, and positive predictive value of 0.90. In our study, frontal lobe hematoma and interhemispheric SAH correlated with distal ACA aneurysms, and SAH in the unilateral basal cistern correlated with A1 aneurysm. In this study, the associated hematoma or dense SAH did not affect the diagnosis of CTA when its acquisition was properly optimized, which was suggested by previous authors [4,9,13,15]. The incidence of the distal ACA saccular aneurysms (usually between pericallosal and callosomarginal arteries) is about 1.5% to 9% of all intracranial aneurysms [6,20,21]. Aneurysms in the proximal (A1) segment of ACA are even rare, with incidence of 0.88% to 3.4% [5,22,23]. In this study, CTA could demonstrate these small aneurysms in unusual locations well, and it provided enough information for emergent surgical clipping. Vascular anomalies are common findings in distal ACA, including azygos ACA, bihemispheric ACA, and triplicated ACA [24]. Among these anomalies, the most characteristic feature associated with aneurysm is azygos ACA, about 10% of the surgical cases. Three aneurysms of this study associated with vascular anomaly: one with azygos A2
segment and two with triplicated ACA. However, a triplicated ACA associated with an aneurysm has seldom been reported [25,26]. Better than conventional DSA in a given angle, CTA could show both the aneurysm and vascular anomaly in one time and could project in proper angle as a map for emergent surgical approach. The incidence of multiple aneurysms is approximately one fifth of the aneurysmal cases [27]. A high incidence (35 –44.7%) of multiple aneurysms presents frequently in coexistence with an A1 aneurysm or distal ACA aneurysm [5,20]. In patients of multiple aneurysms where an ACA is presented, there is a high incidence of rupture of that aneurysm [5]. It was proved again in two patients of our study. There are several limitations in the present study. First, a retrospective study based on the patients’ received operation may have selection bias. Second, comparison of DSA and CTA was not completed because DSA studies were limited. However, surgical findings enabled the diagnosis to be confirmed. In conclusion, the ACA aneurysms at uncommon location are usually small, with multiplicity and vascular anomaly, and associated with complex vascular structures wrapping around the aneurysms. All ruptured aneurysms at such uncommon location can be detected with certainty on CTA, and surgical intervention can usually be performed with only CTA as preoperative guidance. A high-quality CTA images can well show the body and neck of an aneurysm and adjacent complex vascular anatomy. Noninvasive CTA can be reliable in detection and characterization of intracranial aneurysms at such uncommon location for planning of emergent surgical intervention.
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C.-y. Chen et al. / Journal of Clinical Imaging 30 (2006) 87 – 93 [9] Lenhart M, Bretschneider T, Gmeinwieser J, et al. Cerebral CT angiography in the diagnosis of acute subarachnoid hemorrhage. Acta Radiol 1997;38:791 – 6. [10] Ogawa T, Okudera T, Noguchi K, et al. Cerebral aneurysms: evaluation with three-dimensional CT angiography. AJNR Am J Neuroradiol 1996;17:447 – 54. [11] Imakita S, Onishi Y, Hashimoto T, et al. Subtraction CT angiography with controlled-orbit helical scanning for detection of intracranial aneurysms. AJNR Am J Neuroradiol 1998;19:291 – 5. [12] Anderson GB, Findlay JM, Steinke DE, et al. Experience with computed tomographic angiography for the detection of intracranial aneurysms in the setting of acute subarachnoid hemorrhage. Neurosurgery 1997;41:522 – 8. [13] Kogori Y, Takahashi M, Katada K, et al. Intracranial aneurysms: detection with three-dimensional CT angiography with volume rendering — comparison with conventional angiographic and surgical findings. Radiology 1999;211:497 – 506. [14] Velthuis BK, Rinkel GJE, Ramos LMP, et al. Subarachnoid hemorrhage: aneurysm detection and preoperative evaluation with CT angiography. Radiology 1998;208:423 – 30. [15] Schwartz RB, Tice HM, Hooten SM, et al. Evaluation of cerebral aneurysms with helical CT: correlation with conventional angiography and MR angiography. Radiology 1994;192:717 – 22. [16] Harrison MJ, Johnson BA, Gardner GM, Welling BG. Preliminary results on the management of unruptured intracranial aneurysms with magnetic resonance angiography and computed tomographic angiography. Neurosurgery 1997;40:947 – 57. [17] Broderick JP, Brott TG, Duldner JE, et al. Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 1994;25:1342 – 7.
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[18] Velthuis BK, Leeuwen MSV, Witkamp TD, et al. Computerized tomography angiography in patients with subarachnoid hemorrhage: from aneurysm detection to treatment without conventional angiography. J Neurosurg 1999;91:761 – 7. [19] Van der Jagt M, Hasan D, Bijvoet HW, et al. Validity of prediction of the site of ruptured intracranial aneurysms with CT. Neurology 1999;52:34–9. [20] Inci S, Erbengi A, Ozgen T. Aneurysms of the distal anterior cerebral artery. Surg Neurol 1998;50:130 – 40. [21] Miyazawa N, Nukui H, Yagi S, et al. Statistical analysis of factors affecting the outcome of patients with ruptured distal anterior cerebral artery aneurysms. Acta Neurochir 2000;142:1241 – 6. [22] Hino A, Fujimoto M, Iwamoto Y, et al. Surgery of proximal anterior cerebral artery aneurysms. Acta Neurochir 2002;144:1291 – 6. [23] Wakabayashi T, Tamaki N, Yamashita H, et al. Angiographic classification of aneurysms of the horizontal segment of the anterior cerebral artery. Surg Neurol 1985;24:31 – 4. [24] Baptista AG. Studies of the arteries of the brain II The anterior cerebral artery: some anatomic features and their clinical implications. Neurology 1963;13:825 – 35. [25] Shimosegawa Y, Takahashi A, Onuma T. Ruptured cerebral aneurysm of the median artery of the corpus callosum (accessory anterior cerebral artery): case report. No Shinkei Geka 1985;13:579 – 83. [26] Kaido T, Nakase H, Goda K, et al. Value of 3D CTA in association with accessory anterior cerebral artery with ruptured anterior communicating artery aneurysm. Acta Neurochir 2003;145:157 – 8. [27] Mount LA, Brisman R. Treatment of multiple aneurysms—symptomatic and asymptomatic. Clin Neurosurg 1974;21:166 – 70.
Computed tomography angiography in detection and characterization of ruptured anterior cerebral artery aneurysms at uncommon location for emergent surgical clipping Chia-yuen Chena, Shu-Chiang Hsieha, Wai-Man Choia, Pei-yeh Chiangb, Jerry Chin-Wei Chiena, Wing P. Chana,c,4 a
Department of Radiology, Taipei Medical University –Municipal Wan Fang Hospital, 111 Hsing-Long Road, Section 3, Taipei 116, Taiwan, ROC Department of Neurosurgery, Taipei Medical University –Municipal Wan Fang Hospital, 111 Hsing-Long Road, Section 3, Taipei 116, Taiwan, ROC c Department of Radiology, School of Medicine, Taipei Medical University, 250 Wu-Hsing Street, Taipei 110, Taiwan, ROC
b
Received 10 August 2005; received in revised form 7 September 2005; accepted 7 September 2005
Abstract Introduction: Cerebral subarachnoid hemorrhage may result from rupture of saccular aneurysms at uncommon location [excluding the anterior communicating artery (ACOM)] of the anterior cerebral artery (ACA). The purpose of this study was to evaluate the usefulness of helical computed tomography angiography (CTA) in detection and characterization of intracranial aneurysms at such uncommon locations before emergent surgical clipping. Materials and methods: Between 1998 and 2003, records for 50 consecutive patients who underwent emergent surgical clipping for intracranial aneurysms were reviewed. Eighteen of these patients had aneurysms in the ACA. After those patients with unequivocal ACOM aneurysms were excluded, eight patients with eight aneurysms in an uncommon location of the ACA were recruited to this study. Plain computed tomography (CT) and CTA were performed in eight patients, and digital subtraction angiographies were done in three patients. Each aneurysm was evaluated for the detection, quantification, and characterization of the aneurysms with 2D multiplanar reformatted and 3D volume-rendering techniques. Results: There were two small aneurysms arising from the A1 segment, one from the A2 segment, two at the junction of triplicated ACAs, two at the junction of A2 and A3 segments, and one at the junction of A2 and A3 segments of the azygos ACA. The average diameter of the aneurysmal sac was 4.44 mm (range, 2.7–7.0 mm), and the aneurysmal neck averaged 2.59 mm (range, 1.2–3.5 mm) in size. The smallest aneurysm measured 2.21.82.7 mm (neck, 1.2 mm) in the A1 segment of the left ACA. Three patients had intracerebral hematoma, seven had intraventricular hemorrhage, and three had acute hydrocephalus. Conclusion: Aneurysms in uncommon locations of ACAs exhibited characteristic features. Rupture of these aneurysms can cause intracerebral hematoma, intraventricular hemorrhage, and/or acute hydrocephalus. Noninvasive CTA can reliably detect and characterize intracranial aneurysms at such uncommon location for planning of emergent surgical intervention. D 2006 Elsevier Inc. All rights reserved. Keywords: Aneurysm; Anterior cerebral artery; CT angiography, subarachnoid hemorrhage
1. Introduction
4 Corresponding author. Department of Radiology, Taipei Medical University–Municipal Wan Fang Hospital, 111, Hsing-Long Road, Section 3, Taipei 116, Taiwan, ROC. Tel.: +886 2 2930 7930x1300; fax: +886 2 2931 6809. E-mail address: [email protected] (W.P. Chan). 0899-7071/06/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.clinimag.2005.09.022
The subarachnoid hemorrhage (SAH) due to ruptured aneurysm accounted for 2.1% of stroke patients and the reported surgical mortality rates ranged from 7.7% to 12.5% of patients in Taiwan [1]. Selective intraarterial digital subtraction angiography (DSA) has been used as a diagnostic standard for the detection and characterization
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Table 1 Plain CT findings of eight patients with aneurysms in uncommon location of ACA Case
Age/sex
Location of aneurysm
ICH
IVH
Hydrocephalus
Midline shifting
SAH
1
64/F
No
I–IV
Mild
No
Left BA= left SY= IHF N MCAF = QGP
2
73/F
No
No
Left BA= left MCAF N left SY= left AM
41/F
Bilateral lateral horns I–III
Mild
3
Mild
No
IHF N SYN MCAF = BA= QGP
4 5
49/M 55/F
Minimal Moderate
No No
IHF N BA= MCAF = SY IHF N BA= SY N MCAF = QGP
68/M
I–IV
Severe
No
IHF N BA
7
70/F
No Bilateral frontal lobe Bilateral frontal lobe No
No I–IV
6
I–IV
Mild
No
IHF N SY= MCAF N BA
8
59/M
A1 segment of the left ACA A1 segment of the left ACA Four aneurysms including the left A2 segment Triplicated ACA Two aneurysms including triplicated ACA Junction of A2 and A3 segment of the left ACA Junction of A2 and A3 segment of the right ACA Junction of A2 and A3 segment of azygos ACA
Bilateral frontal lobe
I–IV
Moderate
No
IHF N BA= MCAF = SY= QGP
No
ICH, intracerebral hematoma; IVH, intraventricular hemorrhage; BA, basal cistern; SY, sylvian fissure; MCAF, middle cerebral artery fissure; IHF, interhemispheric fissure; QGP, quadrigeminal plate cistern; AM, ambient cistern.
of intracranial aneurysms, with false-negative rate of detection 5% to 10% [2]. Obtaining less than optimal projection with angiographic equipment may limit detection of some intracranial aneurysms [3,4] or measurement of the aneurysmal neck relating to the parent artery, impairing selection of the treatment method [3,4]. Other disadvantages of DSA include the invasiveness of arterial puncture and intraarterial catheter manipulation, and that it is a time-consuming procedure and that the devices are expensive. Helical computed tomography angiography (CTA) is a new noninvasive volumetric imaging technique. By using optimized acquisition and postprocessing protocols, the sensitivity of CTA in the detection of very small (b 5 mm) cerebral aneurysms is higher than that of DSA, with equal specificity and higher interoperator reliability [4]. Imaging acquisition of CTA requires only 1 min or less, thereby benefiting high-risk patients.
Cerebral SAH may result from rupture of saccular aneurysm of anterior cerebral artery (ACA), which is commonly originated from anterior communicating artery (ACOM). Only 0.88% of all intracranial aneurysms have been reported to have originated from the A1 segment and 5.3% from the distal ACA [5,6]. Anterior cerebral artery aneurysm in such uncommon locations is usually associated with multiple aneurysms and vascular anomalies and may exhibit a similar appearance to ACOM aneurysm rupture on plain computed tomography (CT) [5,6]. The surgical approach of these aneurysms is different from those of the other anterior circulation aneurysms [6]. Previous CTA studies have reported only 14 aneurysms at such uncommon locations in a total of 545 intracranial aneurysms [4,7 – 16]. The purpose of this study was to evaluate the usefulness of plain CT and helical CTA in detection and characterization of intracranial aneurysms at such uncommon location before emergent surgical clipping.
Table 2 Computed tomography angiographic findings of eight patients with aneurysms in uncommon location of ACA Case
Location of aneurysm
CTA
Sac size (mm)
Neck size (mm)
Cal/thom
DSA
Surgery
Surgical approach
1
A1 segment of the left ACA
Positive
3.12.0
3.5
No
Positive
Clip
Left pterional
2
A1 segment of the left ACA
Positive
2.72.2
1.2
No
Positive
Clip
Left pterional
3
Left A2 segment
Positive
6.14.9
3.2
No
N/A
Clip
Left pterional
4
Triplicated ACA
Positive
3.53.3
2.5
No
N/A
Clip
Left pterional
5
Triplicated ACA
Positive
7.04.6
2.5
No
N/A
Clip
Right pterional
6
Junction of A2–3 segment of the left ACA Junction of A2–3 segment of the right ACA Junction of A2–3 segment of azygos ACA
Positive
6.04.0
2
No
N/A
Clip
Interhemispheric
Positive
2.92.2
3.3
No
Positive
Clip
Interhemispheric
Positive
4.24.0
2.5
No
N/A
Clip
Interhemispheric
7 8
Cal/thom, calcification/thrombus; N/A, not available
Status at follow-up Alive, after 27 months Alive, after 24 months Expired, after 1 month Alive, after 40 months Alive, after 5 months Alive, after 26 months Alive, after 10 months Alive, after 23 months
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2. Materials and methods 2.1. Patients Between 1998 and 2003, the records of 50 consecutive patients who underwent emergency aneurysm clipping for intracranial aneurysms were reviewed. Eighteen of them had aneurysms that occurred in the ACA. After exclusion of those patients with typical ACOM aneurysms, eight aneurysms at uncommon location of the ACA were recruited in this study. Plain CT and CTA were performed in all eight patients, and DSA was done in three patients. Plain CT and CTA images were reviewed without knowledge of DSA or surgical reports by a single experienced
Fig. 2. Case 3: Patient with a saccular aneurysm originating from A2 segment of the left ACA, in addition to a saccular aneurysm at ACOM and the other two at other locations (not shown). (A) Sagittal view, 2D multiplanar reformatted CTA image shows a saccular aneurysm with wide neck originating from A2 segment of the left ACA (arrow). (B) Threedimensional anteroposterior projection CTA image with lateral angulation shows a wide-based aneurysm from the A2 segment of the left ACA (arrow) and a bilobulated saccular aneurysm from ACOM (arrowhead). One branch of A2 segment originating from the proximal neck of aneurysm is well seen.
Fig. 1. Case 2: Patient with a small saccular aneurysm originating from A1 segment of the left ACA. (A) Midarterial phase anteroposterior projection DSA image shows a small saccular aneurysm at the proximal portion of the A1 segment of the left ACA (arrow). (B) Three-dimensional anteroposterior projection CTA image with caudal angulation shows a 2.7-mm aneurysm sac (arrow) in superior and medial direction with narrow neck. One small lenticulostriate artery from the aneurysm neck is well seen (arrowhead).
neuroradiologist (C.Y.C). Digital subtraction angiography images were read with CTA images by the same radiologist to see if DSA provided information additional to that of the CTA. Parameters for interpretation included detection, quantification, and characterization of ACA aneurysms at uncommon locations. Only aneurysms, defined as a saccular outpouching from a parent artery having a clearly definable sac and neck, were recruited in this study. Aneurysmal dilatations, defined as abnormal outpouching of an arterial wall but without a definable neck, were not considered as aneurysms. Infundibula, defined as a pyramidal dilatation at the origin of a vessel with an artery arising from the apex, were excluded.
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A triplication of ACA was defined as three branches arising from ACOM, including bilateral A2 segments of the ACA and an unusual branch of ACOM (or known as accessory ACA) distributed to one or to both hemispheres. Hydrocephalus was defined as a ventricular enlargement with rounded dilation of the superior-lateral portion of the frontal horns and temporal horn. Acute hydrocephalus was defined as a hydrocephalus associated with periventricular
hypodensity due to transependymal CSF resorption and/or intraventricular hemorrhagic clot in central lumen of the dilated ventricles. 2.2. Helical CTA All CTA examinations were performed using a helical technique on either one of the two CT scanners (Hi-Speed CT/I and Hi-Speed CT/FX, General Electric, Milwaukee, WI). All patients were positioned supine, with head immobilization achieved with adhesive tape. The delayed scanning time was 18 s. The helical technique included a pitch of 1.0 to 1.5 of 1-mm section collimation, 0.5-mm reconstruction interval, and a coverage from the level of 1 cm below sella floor to the upper margin of sylvian fissure. The average acquisition time was 60 s. Other imaging parameters included a matrix of 512512, a 150-mm field of view, 120 kV, and 260 to 290 mA. The administration of 100 ml nonionic contrast medium (Ultravist 300 I mg/ml, Schering) was injected by an intravenous route through a 20-gauge antecubital angiocatheter using a power injector at a rate of 3 cc/s. 2.3. Image processing Postprocessing of CTA images was performed using commercially available software in an independent workstation (Advantage Workstation version 4.0, General Electric). Three-dimensional perspective volume-rendered images, 3D thick slab and gray scale 2D single section, and thick slab multiplanar reformatted 2D images were evaluated. Single section 2D and thick slab 3D multiplanar reformatted images were used for detection and quantification of the aneurysmal sac and neck, and used for the determination of the presence, location, and extent of mural calcification and intraluminal thrombi with respect to the aneurysmal neck. Volume-rendered 3D images were used for the detection of intracranial aneurysm, the characterization of arterial branching patterns at the neck, the depiction of the position and spatial orientation of the aneurysmal neck and sac, and the depiction of the relationship of the aneurysm to local and regional bone anatomy.
Fig. 3. Case 5: Patient with a saccular aneurysm originating from triplicated ACA, in addition to other aneurysms at other locations (not shown). (A) Nonenhanced CT image shows dense intracerebral hematoma at the left frontal lobe, diffusely dense SAH in interhemispheric fissure, basal cistern, and bilateral sylvian fissure with localized hematoma formation (arrow). Intraventricular hemorrhage and hydrocephalus are noted. (B) Sagittal view, multiplanar reformatted CTA image shows an elongated aneurysm in superior and anterior direction from the junction of bilateral A1 segments (arrow). Three branches distal to ACOM are noted. Note the ability of CTA to visualize aneurysm in the setting of acute severe SAH with local dense hematoma. (C) Three-dimensional anteroposterior projection CTA image with lateral and caudal angulation shows the aneurysm sac (arrow) and the trifurcation (bilateral A2 segments and accessory ACA) arising from aneurysm neck (arrowheads).
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The size of each aneurysm was measured in maximum projection of aneurysmal sac in 3D images. If more than one aneurysm was detected, the aneurysm that caused SAH (on the basis of the blood distribution as shown on unenhanced CT images) was selected for analysis in this study. 2.4. Digital subtraction angiography Digital subtraction angiography images were obtained in patients who underwent selective three- or four-vessel angiograms on frontal, lateral, and oblique projections. The CT angiograms were available to the angiographer as a reference guide for possible extra DSA projections.
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Three patients received DSA within 24 h after CTA. In comparing DSA with CTA, there was no additional for any of the three patients. Microsurgery was performed in all patients in the acute stage; for seven of eight patients, it was performed within 48 h of their visit to our emergency department. All aneurysms were confirmed during operation. All patients were successfully treated by surgical clipping: three via interhemispheric approach and five via pterional approach.
3. Results There were eight patients (five women and three men) who presented with intracranial aneurysms in uncommon location of the ACA. Their age ranged from 41 to 73 years old (mean, 60 years old). All patients were sent to the emergency room with chief complaints of severe headache or loss of consciousness. Table 1 summarizes the patients’ data and plain CT findings. The emergent plain CT scan revealed an SAH in all patients, with the most increased density area in interhemispheric fissure in six patients and the unilateral basal cistern in two patients, relating to the location of ruptured aneurysms. Localized intracranial hemorrhage was seen in the bilateral frontal lobes of three patients. Seven of eight patients had intraventricular hemorrhage, and all eight patients suffered from various degrees of hydrocephalus; three patients had acute hydrocephalus. No patients had a mass effect causing midline shifting. Of the eight patients, two patients had multiple aneurysms (Table 1). Case 3 had four intracranial aneurysms, respectively, in the left A2 segment of the ACA, the ACOM, the junction of M1 and M2 segments of the left middle cerebral artery, and the cavernous portion of the right intracranial artery. Case 5 had two intracranial aneurysms, respectively, in a triplicated ACA and the junction of M1 and M2 segments of the right middle cerebral artery. All eight aneurysms were detected preoperatively by CTA, and all were confirmed at surgery and/or DSA (Table 2). There were two small aneurysms arising from A1 segment of the ACA (Fig. 1), one from the A2 segment (Fig. 2), two at the junction of triplication of the ACA (Fig. 3), two at the junction of A2 and A3 segments, and one at the junction of A2 and A3 segments of azygos ACA (Fig. 4). The average maximal diameter of the aneurysmal sac was 4.44 mm (range, 2.7–7.0 mm). The size of the aneurysmal neck averaged 2.59 mm (range, 1.2–3.5 mm). The smallest aneurysm measured 2.21.82.7 mm, with a neck measured 1.2 mm (Fig. 2), located in the A1 segment of the left ACA. Neither mural thrombus nor wall calcification was noted in any aneurysms.
Fig. 4. Case 8: Patient with a saccular aneurysm originating at the distal tip of azygos ACA. (A) Axial view, multiplanar reformatted CTA image shows azygos ACA and aneurysm in its distal end (arrow). Two cortical arteries arising from the distal portion of azygos ACA are seen. (B) Threedimensional anteroposterior projection CTA image with lateral angulation shows aneurysm sac, azygos ACA as a single A2 segment (small arrows), and paired A3 segments.
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One patient (Case 3) expired 1 month after surgical clipping due to postoperative ischemic insult and uncontrollable brain swelling. The other seven patients were discharged with stable clinical condition; clinical followup for 5 to 40 months (mean, 22.1 months) revealed no complications.
4. Discussion Cerebral SAH due to ruptured aneurysms often results in poor prognosis. Most of the patients die of rebleeding in additional to the initial intracranial hemorrhage [17]. Rebleeding can be prevented by early neurosurgical intervention. In our hospital, CTA has been employed as a first-line imaging modality in screening patients with SAH possibly caused by ruptured aneurysm. When ruptured aneurysm was detected in CTA, surgical clipping was performed to minimize rebleeding. Digital subtraction angiography was requested only for uncertainty about the presence of aneurysms. Our results indicated that CTA could be used to substitute DSA in screening patients with SAH and suspected ruptured intracranial aneurysms; a similar conclusion has been made by Velthuis et al. [18]. Digital subtraction angiography images provided no additional information compared with CTA. Computed tomography angiography can demonstrate the aneurysmal neck and relationship between the aneurysm and the parent artery even better than DSA. Van der Jagt et al. [19] suggested that the parenchymal cerebral hematoma was an excellent predictor for the site of a ruptured aneurysm. The next most useful predictor was blood distribution on CT in patients with a ruptured ACA aneurysm or ACOM aneurysm, with sensitivity of 0.79, specificity of 0.97, and positive predictive value of 0.90. In our study, frontal lobe hematoma and interhemispheric SAH correlated with distal ACA aneurysms, and SAH in the unilateral basal cistern correlated with A1 aneurysm. In this study, the associated hematoma or dense SAH did not affect the diagnosis of CTA when its acquisition was properly optimized, which was suggested by previous authors [4,9,13,15]. The incidence of the distal ACA saccular aneurysms (usually between pericallosal and callosomarginal arteries) is about 1.5% to 9% of all intracranial aneurysms [6,20,21]. Aneurysms in the proximal (A1) segment of ACA are even rare, with incidence of 0.88% to 3.4% [5,22,23]. In this study, CTA could demonstrate these small aneurysms in unusual locations well, and it provided enough information for emergent surgical clipping. Vascular anomalies are common findings in distal ACA, including azygos ACA, bihemispheric ACA, and triplicated ACA [24]. Among these anomalies, the most characteristic feature associated with aneurysm is azygos ACA, about 10% of the surgical cases. Three aneurysms of this study associated with vascular anomaly: one with azygos A2
segment and two with triplicated ACA. However, a triplicated ACA associated with an aneurysm has seldom been reported [25,26]. Better than conventional DSA in a given angle, CTA could show both the aneurysm and vascular anomaly in one time and could project in proper angle as a map for emergent surgical approach. The incidence of multiple aneurysms is approximately one fifth of the aneurysmal cases [27]. A high incidence (35 –44.7%) of multiple aneurysms presents frequently in coexistence with an A1 aneurysm or distal ACA aneurysm [5,20]. In patients of multiple aneurysms where an ACA is presented, there is a high incidence of rupture of that aneurysm [5]. It was proved again in two patients of our study. There are several limitations in the present study. First, a retrospective study based on the patients’ received operation may have selection bias. Second, comparison of DSA and CTA was not completed because DSA studies were limited. However, surgical findings enabled the diagnosis to be confirmed. In conclusion, the ACA aneurysms at uncommon location are usually small, with multiplicity and vascular anomaly, and associated with complex vascular structures wrapping around the aneurysms. All ruptured aneurysms at such uncommon location can be detected with certainty on CTA, and surgical intervention can usually be performed with only CTA as preoperative guidance. A high-quality CTA images can well show the body and neck of an aneurysm and adjacent complex vascular anatomy. Noninvasive CTA can be reliable in detection and characterization of intracranial aneurysms at such uncommon location for planning of emergent surgical intervention.
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