3D bone subtraction CT angiography for the evaluation of intracranial aneurysms: a comparison study with 2D bone subtraction CT angiography and conventional non-subtracted CT angiography

Abstract

Background

Bone subtraction computed tomography angiography (BSCTA) is better able to facilitate the detection of intracranial aneurysms adjacent to bone structures compared to conventional non-subtracted CTA (CNSCTA). However, the comparison of the diagnostic accuracy of three-dimensional (3D) and two-dimensional (2D) BSCTA and conventional CTA in evaluating intracranial aneurysms remains unclear.

Purpose

To evaluate whether 3D BSCTA has a superior diagnostic accuracy to those of 2D BSCTA and CNSCTA in a single center with the same instrument.

Material and Methods

Sixty-three patients received 3D BSCTA, 2D BSCTA, and NSCTA for the detection and treatment planning of suspected intracranial aneurysms. The angiography readouts were reviewed by two independent radiologists. The sensitivity of CTA in detecting aneurysm was analyzed on a per-aneurysm and per-patient basis, using 3D digital subtraction angiography (DSA) and surgical findings as the gold standard. The potential of endovascular treatment or surgical clipping was also assessed based on information provided by the CTA.

Results

A total of 66 aneurysms were detected in 54 patients. The overall sensitivity, specificity, positive, and negative predictive values of 3D BSCTA were all 100%, and these values for 2D BSCTA were 98.1%, 100%, 100%, and 90%, respectively. The total sensitivity, specificity, positive, and negative predictive values of CNSCTA were 94.4%, 100%, 100%, and 75%, respectively. Finally, 100%, 98.1%, and 85.2% patients received appropriate treatment decisions after 3D BSCTA, 2D BSCTA, and CNSCTA imaging, respectively.

Conclusion

3D BSCTA has a higher sensitivity for the detection of small aneurysms and aneurysms adjacent to bone compared to 2D BSCTA or CNSCTA, which were still able to obtain sufficient information for the detection of intracranial aneurysms and therapeutic decision-making.

Keywords

Intracranial aneurysms computed tomography angiography bone subtraction digital subtraction angiography spontaneous subarachnoid hemorrhage

Introduction

Overall, 80–90% of spontaneous subarachnoid hemorrhages (SAH) are caused by the rupture of an intracranial aneurysm (1,2). Early identification and immediate therapy of impending ruptured aneurysms is generally advocated to reduce the mortality and morbidity (3). Digital subtraction angiography (DSA) is the current gold standard for the detection of intracranial aneurysms (4). However, DSA is an invasive examination (5), that must be carried out by experienced experts. With the rapid improvements in multi-detector computed tomography (MDCT) technology, computed tomography angiography (CTA), a relatively non-invasive diagnostic tool, has been widely applied in the neurovascular imaging of intracranial aneurysms (6). In previous reports, multi-detector conventional non-subtracted CTA (CNSCTA) has shown a favorable diagnostic performance for the detection of intracranial aneurysms (7,8). Nevertheless, the detection of aneurysms at the level of the skull base still remains challenging (9). This problem can be solved by applying bone subtraction CTA (BSCTA) technique to remove the bone signal from the raw data (5,9 –12). Although traditional BSCTA (two-dimensional [2D] BSCTA) has been widely used in a variety of clinical settings (9,13), there are still some limitation such as misregistration due to patients’ motions during scanning, although non-rigid registration techniques have been proposed to overcome this difficulty (14). Recently, a new subtraction software (three-dimensional [3D] BSCTA Tool) designed by Neusoft has been introduced for 3D registration and subtraction and has proven to be a fast and efficient BSCTA technique. To the best of our knowledge, no previous studies have been published about the comparison of diagnostic accuracy (sensitivity, specificity, positive, and negative predictive values) between 3D and 2D BSCTA and CNSCTA to evaluate cerebral aneurysms.

The purpose of this study was to compare the diagnostic performance of 3D and 2D BSCTA with CNSCTA for the detection and characterization of intracranial aneurysms, and to evaluate the value of these tools in indicating treatment.

Material and Methods

This study was approved by the ethical committee of the Second Affiliated Hospital of Soochow University. Informed consent documents were obtained from all patients or their legal representatives. A total of 63 consecutive patients with suspected intracranial aneurysms (35 men, 28 women; mean age, 51 years; age range, 17–88 years) who were examined with non-contrast-enhanced cranial CT and followed by conventional CTA were enrolled in this study. Among these 63 patients, 50 presented with acute non-traumatic SAH. The remaining 13 patients had severe headaches as the only symptom, suggestive of the presence of an aneurysm. All involved patients underwent DSA or surgery later.

Imaging protocols

All enrolled patients were examined with a 64-row multi-detector CT system (GE LightSpeed VCT; GE Healthcare, Milwaukee, WI, USA). The head was fixed during CT scanning to prevent motion artifacts. For BSCTA, we added a non-contrast-enhanced CT (NECT) before following the CNSCTA protocol regularly used in clinical settings. The CT parameters were as follows: 100 KV tube voltage, 300 mAs; 0.5-s rotation time; 64 × 0.625 mm section collimation; 0.625-mm reconstruction interval; pitch, 0.983; matrix, 512 × 512; field of view, 18–24 cm. The CT scan included the area from the first cervical vertebra up to the cranial vault. In total, 70 mL of a contrast agent (Ultravist, 370 mg iodine/mL; Bayer Schering Pharma AG, Berlin, Germany) was injected into the antecubital vein through an 18-gauge needle (Missouri CT injector XD 2001; Ulrich Medical Technic, Ulm, Germany) at a rate of 5 mL/s, followed by 30 mL of normal saline. A test bolus method was used to determine the imaging delay for each patient.

The reconstructed axial images were sent to a GE workstation (Advantage Windows 4.3; GE Healthcare, Milwaukee, WI, USA) and a Neusoft workstation (Neusoft, Shenyang, China) for bone subtraction (BS). Bone removal was performed by subtraction of the NECT data from the CNSCTA data using dedicated software (3D BS of Neusoft’s BSCTA Tool and 2D BS of GE’s Add/Sub). The principle of the Add/Sub software was that the two datasets (NECT and conventional CTA) were registered in a 2D way by the subtraction of the NECT data from the conventional CTA data, slice by slice, at which point the subtracted isotropic datasets were reformatted into 3D volume rendering (VR) and maximum intensity projection (MIP) images for further review. The principles of the BSCTA Tool software was that the two datasets were registered and subtracted in a 3D way to selectively eliminate bones and soft tissues from the conventional CTA datasets, leaving only contrast-enhanced vessels for further evaluation (15). The technical details were also reported in IEEE, 2010, Chengdu, China. In our study, Neusoft’s BSCTA tool transformed 3D subtracted isotropic data into 2D data, which were then transferred to the GE workstation for 3D reconstruction.

DSA of both common carotid arteries, the internal carotid arteries, and the vertebral arteries was selectively performed in all patients via femoral catheterization by the Seldinger technique with a plane DSA unit (AlluraXper FD20; Philips, Best, The Netherlands). 3D DSA views including anteroposterior, lateral, and oblique projections were obtained and additional views were acquired at the discretion of the angiographer.

Image interpretation

All CT angiograms were randomized for interpretation. Two experienced radiologists blinded to the DSA results evaluated the CT angiograms (MIP and VR image) and the source image. The DSA results were analyzed by an experienced interventional radiologist. The radiologists evaluated the size, shape, and location of each aneurysm, as well as its relationship with the parent artery and adjacent structures. The maximal sac diameter, neck size, and location were also recorded. The visualization of the aneurysms was classified into three categories: (i) precise visualization, in which the shape of the aneurysm was clearly depicted; (ii) ambiguous or partial visualization, in which the anatomy of the aneurysm was obscured by adjacent bones or vessels; and (iii) poor visualization, in which the shape of the aneurysm could not be identified. The possibility of endovascular treatment or surgical clipping of aneurysms was also assessed, given the individual characteristics of the aneurysm provided by CT angiograms alone. The quality of both 3D and 2D BSCTA images was grouped into three levels. The images with top image quality visualized only vascular structures without any disturbance of bony structures; the images with medial image quality were also adequate for diagnosis but contained some bone remnants; and the images with poor image quality presented large bony remnants, causing problems in the further evaluation of the aneurysms (6).

Statistical analysis

Statistical analysis was performed using Statistical Product and Service Solutions (SPSS, version 17.0; IBM, Armonk, NY, USA). DSA and surgical findings were considered as the reference standard for the evaluation of cerebral aneurysms. The sensitivity of 3D, 2D BSCTA, and CNSCTA in detecting aneurysms on a per-aneurysm, per-patient basis, as well as their overall sensitivity, specificity, positive predictive value, and negative predictive value were calculated. Kappa statistics were used to quantify inter-reader variability in detecting aneurysms on a per-patient and per-aneurysm basis. Kappa values less than 0.20 were interpreted as poor agreement; 0.21–0.40, as fair; 0.41–0.60, as moderate; 0.61–0.80, as good; and 0.81–1.00, as very good agreement. P values less than 0.05 were considered statistically significant.

Results

Image quality of 3D and 2D BSCTA

No obvious adverse effects or complications were found after CTA and DSA examination in any patient. All of the 3D and 2D BSCTA images were of diagnostic quality. The image quality of 3D and 2D BSCTA was optimal in 60 of 63 (95.2%) and 57 of 63 (90.5%) of the patients, respectively. For three patients, 3D BSCTA was rated at the top level and 2D BSCTA was rated at the medial level due to incomplete bone removals after mild head motion during the imaging process. In three patients, both 3D and 2D BSCTA were rated at the medial level due to severe head motion.

Accuracy of detection of aneurysms

Out of the 63 patients, aneurysms were not found in nine; 54 patients had a total of 66 aneurysms (Table 1). A single aneurysm was detected in 45 patients (83.3%), and multiple aneurysms were detected in nine patients (16.7%). Six patients (11.1%) had two aneurysms, and three patients (5.6%) had three aneurysms. According to 3D and 2D BSCTA, the average maximal aneurysm sac diameter was 4.2 mm (range, 1.5–15.7 mm) and 4.1 mm (range, 1.4–15.6 mm), respectively, whereas the average neck size of the aneurysm was 2.8 mm (range, 0.9–8.5 mm) and 2.9 mm (range, 0.9–8.6 mm), respectively.

Table 1.

Aneurysm detection: location and size of 66 aneurysms based on 3D DSA or surgical findings.

Aneurysm location	Aneurysm size (mm)
Aneurysm location	<3	3–5	>5	Total
Posterior cerebral artery	0	1	0	1
Anterior cerebral artery	4	0	1	5
Middle cerebral artery	5	2	0	7
Anterior communicating artery	6	3	1	10
Posterior communicating artery	2	5	6	13
Internal carotid artery	10	6	4	20
Vertebral artery	2	0	1	3
Basilar artery	4	1	2	7
Total	33	18	15	66

In the per-patient basis analysis, both radiologists identified all aneurysms in all patients (100%) by 3D BSCTA. In the 54 patients with aneurysms, 65 aneurysms were detected in 53 patients (98.1%) with 2D BSCTA. One aneurysm located at the left communicating (C7) segment of the internal carotid artery (ICA) was missed due to incomplete bone removal produced by mild head motion during the imaging process (Fig. 1). Analysis on a per-aneurysm basis, revealed a sensitivity of 3D BSCTA of 100%, whereas the sensitivity of 2D BSCTA was 98.5%. Analysis on a per-patient basis, showed a sensitivity of 3D BSCTA at 100% and a sensitivity of 2D BSCTA at 98.1%. Inter-reader agreement on a per-patient (k = 0.960, P < 0.05) and per-aneurysm basis (κ = 0.964, P < 0.05) between two independent radiologists was satisfactory. The overall sensitivity, speciﬁcity, positive, and negative predictive values of 3D BSCTA were 100%, with the corresponding values of 2D BSCTA being 98.1%, 100%, 100%, and 90%, respectively. However, there were no significant differences between 3D and 2D BSCTA regarding sensitivity, speciﬁcity, and positive or negative predictive values for the aneurysm.

Fig. 1.

A 68-year-old man with an aneurysm in the left C7 segment of the internal carotid artery.One aneurysm located at the left communicating (C7) segment of the internal carotid artery (arrow) was missed due to incomplete bone removal produced by a mild head motion with 2D BSCTA VR (a) and MIP images (c). 3D BSCTA VR (b) and MIP images (d) clearly showed the left C7 internal carotid artery aneurysm (arrow) with optimal image quality and no bone remnants. DSA (e) showed the left C7 segment of the internal carotid artery aneurysm (arrow).

Among the 54 patients with aneurysms, CNSCTA detected 62 out of 66 aneurysms in 52 patients. The average maximal aneurysm sac diameter was 4.0 mm (range, 1.3–15.4 mm), and the average neck size was 3.0 mm (range, 0.9–8.6 mm). Four aneurysms were omitted including two aneurysms less than 3 mm in maximal diameter. In one patient with SAH, the M1 segment of the left middle cerebral artery aneurysm was missed during the preliminary reading. Further analysis of the images revealed that CNSCTA only visualized part of the missed aneurysm. All four of the overlooked aneurysms that were not detected by either reader were adjacent to the skull base; three were located at the clinoid (C5) section of the ICA (Fig. 2) and the last, at the left ophthalmic (C6) section of the ICA (Fig. 3). On a per-aneurysm basis, the sensitivity of CNSCTA was 93.9%. On the basis of per-patient, the sensitivity of CNSCTA was 96.3%. The total sensitivity, speciﬁcity, positive, and negative predictive values of CNSCTA were 94.4%, 100%, 100%, and 75%, respectively. Both 3D and 2D BSCTA had significant differences from CNSCTA (P < 0.05).

Fig. 2.

CNSCTA failed to detect three aneurysms in a 77-year-old woman with SAH. The three aneurysms were surgically treated based on 2D and 3D BSCTA results. CNSCTA VR (a) and MIP images (d) failed to detect the three C5 internal carotid artery aneurysms because of overlying bones. Despite some bone remnants remaining at the skull base, 2D BSCTA VR (b) and MIP images (e) depicted the three aneurysms (arrows). 3D BSCTA VR (c) and MIP images (f) clearly showed the three C5 internal carotid artery aneurysms (arrows) due to optimal image quality when no bone remnant and only arteries were present.

Fig. 3.

CNSCTA failed to detect one aneurysm in a 73-year-old woman with SAH. Conventional CTA VR (a) and MIP images (e) failed to detect the left C6 segment of the internal carotid artery aneurysm because of overlying bones. 2D BSCTA VR (b) and MIP images (f) clearly depicted the aneurysm (arrow) due to their optimal image quality. 3D BSCTA VR (c) and MIP images (g) clearly showed the left C6 segment of the internal carotid artery aneurysm (arrow) because of their optimal image quality. The aneurysm (arrow) was also clearly shown using DSA (d). Endovascular coiling treatment (h) was then performed according to the results of the 2D and 3D BSCTA.

Pretreatment evaluation and treatment outcome of the aneurysms

The display of the aneurysms was precisely visualized in all patients with 3D BSCTA. The exhibition of the aneurysms was precisely visualized in 53 of 54 patients, although the last exhibition allowed for an ambiguous or partial visualization at 2D BSCTA. As for the CNSCTA, 46 of 54 patients’ aneurysms were precisely visualized. Six of these had partial or ambiguous visualization, and another two showed poor visualization. In all cases, appropriate treatment decisions could be easily made with 3D BSCTA images. For 98.1% of patients (53 of the 54), appropriate treatment decisions could be made based on 2D BSCTA images. Overall, 85.2% (46 out of 54) patients received appropriate treatment decision after CNSCTA. Under the 3D BSCTA assessments, 34 patients were eligible for endovascular coiling (Fig. 3), 18 for surgical clipping, and two for conservative treatment. After the treatment, 61 aneurysms in 52 patients were successfully treated by surgical clipping or endovascular coiling, which in accordance with the pretreatment assessments based on 3D BSCTA. Five small non-liability aneurysms in patients with multiple aneurysms had no indications for coiling or clipping and thus were not treated.

Discussion

Our study demonstrated that 3D BSCTA has a better diagnostic performance than 2D BSCTA and CNSCTA in the detection and evaluation of intracranial aneurysms. 3D BSCTA also shows a better performance in sensitivity than 2D BSCTA, making 3D BSCTA less likely to omit intracranial aneurysms. Compared with 2D/3D BSCTA, a lower sensitivity was found for CNSCTA in detecting intracranial aneurysms, especially for the small aneurysms or aneurysms adjacent to the bone.

The rapid technological development of MDCT scanners has resulted in great improvements in the imaging quality of CTA and in the detection rate of intracranial aneurysms (5,10,16). CTA is now a routine examination that has become fully integrated into the imaging and treatment decision-making process for patients with SAH. Compared with DSA, CTA is a non-invasive, easily applicable, fast, and cost-effective imaging modality for the evaluation of intracranial aneurysms. However, small aneurysms may be overlooked by radiologists with CNSCTA because they are usually mistaken for vascular infundibular, tight vascular loops, or hidden by the overlying bone structures (6,17 –19). Despite this fact, the CNSCTA showed sufficient diagnostic ability to visualize aneurysms located at the anterior cerebral artery, middle cerebral artery or anterior communicating artery. In interpreting aneurysms with a diameter less than 3 mm that were located at the skull base, four aneurysms were missed by radiologists with CNSCTA because of the difficulty in separating the vessels from the bone. One aneurysm located at the M1 segment of the left middle cerebral artery aneurysm was also missed by radiologists due to poor visualization of CNSCTA.

To reduce the risk of missing aneurysms close to the central skull base, various subtraction methods and postprocessing algorithms have previously been proposed (9,10,12,20 –28). Manual bone removal was time consuming and user dependent (20). Threshold-based “region-grow” algorithms often failed to separate the vessels at the base of skull (21). In a study of 36 patients, Imakita et al. (24) reported that the usefulness of subtraction CTA with controlled-orbit helical scanning for detecting aneurysms adjacent to bone was superior to that CNSCTA. In a study of 27 patients with 29 intracranial aneurysms, Tomandl et al. (12) reported that seven aneurysms out of 13 aneurysms located at the ICA were not or only partially visible on CNSCTA, whereas all of the aneurysms were optimally visualized on BSCTA. Other studies (6,26,27,29) have also found that BSCTA can improve the delineation of the vasculature and increase the detection rate of intracranial aneurysms closely adjacent to bony structures by comparison with CNSCTA. However, no comparison of the diagnostic performances 3D, 2D BSCTA, and CNSCTA has been reported yet.

For the first time, our results demonstrated that 3D BSCTA has superior image quality and sensitivity in detecting aneurysms, compared to 2D BSCTA or CNSCTA. Different subtraction methods and post processing algorithms may account for this conclusion. Image postprocessing algorithms often reduce the amount of information originally presented in the raw data (27), and because 3D BSCTA registers in a 3D way, more raw data may be retained than by a 2D BSCTA. 3D BSCTA could also avoid the artifacts produced by mild head motions, eliminating the junction vessel wall when the CT attenuation value of the targeted arteries approximates the adjacent bone. In our study, one aneurysm located at the left communicating segment of the ICA was missed by readers on 2D BSCTA due to artifacts from incomplete bone removals produced by mild head motions during the imaging process; however, the aneurysm was clearly found on 3D BSCTA.

The results of our study suggest that BSCTA especially 3D BSCTA could help in preoperative decision-making such as in consideration of surgical clipping versus endovascular coiling. In previous reports, therapeutic decisions could be made based on sufficient information provided by the CTA (6). Westerlaan et al. (30) demonstrated that CTA should be used as the initial diagnostic modality in the selection of patients for the surgical or endovascular treatment of ruptured intracranial aneurysms. Another study reported that a correct treatment decision was made for 97.7% of patients based on the information provided by CTA alone. Recently, Li et al. (6) found that correct treatment decision could be made for 98.4% and 85.9%, respectively, based on the information provided by subtraction CTA and CNSCTA images alone. With the aid of 3D reconstruction in unlimited projections, the neck of aneurysm, vessel branching, and vascular spatial relationships can be clearly visualized on 3D BSCTA. Therefore, 3D BSCTA provides precise information regarding the aneurysm’s anatomy and facilitates important treatment decisions, such as the placement of a surgical clip versus the use of an endovascular coil. Certain reconstruction algorithms, such as 3D VR and MIP images provided more useful anatomic information for the aneurysm.

There are some limitations of our study. First, compared with CNSCTA, BSCTA might require an increase in the radiation dose, due to the acquisition of the additional unenhanced preliminary mask. However, the radiation dose is still less than that required for DSA. Second, there were no significant differences between 3D and 2D BSCTA regarding sensitivity, speciﬁcity, and positive or negative predictive values for the aneurysm. The relative smaller sample size may partly account for this. Besides, the new subtraction software (BSCTA Tool) used for 3D BSCTA is still in the stages of maturing and consummating, although its 3D display should be fully capacitated in the near future. The feasibility of the BSCTA Tool software has been proved in our previous studies (20,21), and it has the potential for wide application as a new subtraction software.

In conclusion, our study demonstrates 3D BSCTA, with the merit of registering and subtracting in 3D, has higher sensitivity for the detection of intracranial aneurysms with small size and near the skull base than 2D BSCTA or CNSCTA. 3D BSCTA could provide sufficient information equivalent to that obtained with 3D DSA for the detection of intracranial aneurysms and in further therapeutic decision-making.

Footnotes

Acknowledgements

The authors thank Qing Lan, Qing Zhu and Yuyuan Ma for therapeutic decision-making of intracranial aneurysms. We especially thank Wei Zhang, Fang Qiao, Xinyu Hu, Kai Zhao, Shengjun Wang, Bin Kang, Yan Huang and Wen Liu for their important contributions.

References

Kirkpatrick

. Subarachnoid haemorrhage and intracranial aneurysms: what neurologists need to know. J Neurol Neurosurg Psychiatry 2002; 73: 28–33.

Van Gijn

Rinkel

. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 2001; 124: 249–278.

Milhorat

. Timing of aneurysm surgery in subarachnoid hemorrhage: a systematic review of the literature. Neurosurgery 2002; 51: 525–525.

Zhang

L-J

S-Y

Poon

. Automatic bone removal dual-energy CT angiography for the evaluation of intracranial aneurysms. J Comput Assist Tomogr 2010; 34: 816–824.

Lell

Anders

Klotz

. Clinical evaluation of bone-subtraction CT angiography (BSCTA) in head and neck imaging. Eur Radiol 2006; 16: 889–897.

. Subtraction CT angiography for evaluation of intracranial aneurysms: comparison with conventional CT angiography. Eur Radiol 2009; 19: 2261–2267.

Wintermark

Uske

Chalaron

. Multislice computerized tomography angiography in the evaluation of intracranial aneurysms: a comparison with intraarterial digital subtraction angiography. J Neurosurg 2003; 98: 828–836.

Tipper

. Detection and evaluation of intracranial aneurysms with 16-row multislice CT angiography. Clin Radiol 2005; 60: 565–572.

Venema

Hulsmans

FJH

den Heeten

. CT angiography of the circle of Willis and intracranial internal carotid arteries: maximum intensity projection with matched mask bone elimination—feasibility study. Radiology 2001; 218: 893–898.

10.

Jayakrishnan

White

Aitken

. Subtraction helical CT angiography of intra- and extracranial vessels: technical considerations and preliminary experience. Am J Neuroradiol 2003; 24: 451–455.

11.

Sakamoto

Kiura

Shibukawa

. Subtracted 3D CT angiography for evaluation of internal carotid artery aneurysms: comparison with conventional digital subtraction angiography. Am J Neuroradiol 2006; 27: 1332–1337.

12.

Tomandl

Hammen

Klotz

. Bone-subtraction CT angiography for the evaluation of intracranial aneurysms. Am J Neuroradiol 2006; 27: 55–59.

13.

Majoie

van Straten

Venema

. Multisection CT venography of the dural sinuses and cerebral veins by using matched mask bone elimination. Am J Neuroradiol 2004; 25: 787–791.

14.

Loeckx

Coudyzer

Maes

. Nonrigid registration for subtraction CT angiography applied to the carotids and cranial arteries. Acad Radiol 2007; 14: 1562–1576.

15.

Ramasundara

Mitchell

Dowling

. Bone subtraction CT angiography for the detection of intracranial aneurysms. J Med Imaging Radiat Oncol 2010; 6: 1754–1985.

16.

El Khaldi

Pernter

Ferro

. Detection of cerebral aneurysms in nontraumatic subarachnoid haemorrhage: role of multislice CT angiography in 130 consecutive patients. La Radiol Med 2007; 112: 123–137.

17.

Westerlaan

van Dijk

Jansen-van der Weide

. Intracranial aneurysms in patients with subarachnoid hemorrhage: CT angiography as a primary examination tool for diagnosis—systematic review and meta-analysis. Radiology 2011; 258: 134–145.

18.

Agid

Lee

Willinsky

. Acute subarachnoid hemorrhage: using 64-slice multidetector CT angiography to “triage” patients’ treatment. Neuroradiology 2006; 48: 787–794.

19.

McKinney

Palmer

Truwit

. Detection of aneurysms by 64-section multidetector CT angiography in patients acutely suspected of having an intracranial aneurysm and comparison with digital subtraction and 3D rotational angiography. Am J Neuroradiol 2008; 29: 594–602.

20.

Schwartz

Tice

Hooten

. Evaluation of cerebral aneurysms with helical CT: correlation with conventional angiography and MR angiography. Radiology 1994; 192: 717–722.

21.

Lell

Anders

Uder

. New techniques in CT angiography. Radiographics 2006; 26: 45–62.

22.

Jayaraman

Mayo-Smith

Tung

. Detection of intracranial aneurysms: multi-detector row CT angiography compared with DSA. Radiology 2004; 230: 510–518.

23.

Romijn

van Andel

Van Walderveen

. Diagnostic accuracy of CT angiography with matched mask bone elimination for detection of intracranial aneurysms: comparison with digital subtraction angiography and 3D rotational angiography. Am J Neuroradiol 2008; 29: 134–139.

24.

Imakita

Onishi

Hashimoto

. Subtraction CT angiography with controlled-orbit helical scanning for detection of intracranial aneurysms. Am J Neuroradiol 1998; 19: 291–295.

25.

Sarikaya

Deniz

. Unregistered subtracted CT angiography for the visualization of intracranial arteries at or near the skull base: preliminary experience. Diagn Interv Radiol 2007; 13: 105–108.

26.

Lell

Ruehm

Kramer

. Cranial computed tomography angiography with automated bone subtraction: a feasibility study. Invest Radiol 2009; 44: 38–43.

27.

Morhard

Fink

Becker

. Value of automatic bone subtraction in cranial CT angiography: comparison of bone-subtracted vs. standard CT angiography in 100 patients. Eur Radiol 2008; 18: 974–982.

28.

Tomura

Otani

Sakuma

. Three-dimensional bone-free computed tomographic angiography of aneurysms near the skull base using a new bone-removal application. Jpn J Radiol 2009; 27: 31–36.

29.

Hwang

Kwak

Han

. Detection of intracranial aneurysms using three-dimensional multidetector-row CT angiography: is bone subtraction necessary? Eur J Radiol 2011; 79: 18–23.

30.

Westerlaan

van Dijk

Jansen-van der Weide

. Intracranial aneurysms in patients with subarachnoid hemorrhage: CT angiography as a primary examination tool for diagnosis—systematic review and meta-analysis. Radiology 2011; 258: 134–145.