Korean Journal of Cerebrovascular Surgery 2004;6(2):137-143.
Published online September 1, 2004.
Clinical Value of Computed Tomographic Angiography: Our Prospective Clinical Trial.
Cha, Ki Yong , Kim, Tae Hong , Kwon, Soon Chan , Shin, Hyung Shik , Hwang, Yong Soon , Park, Sang Keun
Department of Neurosurgery, Sanggye Paik Hospital, Inje University, Seoul, Korea. skpark@sanggyepaik.co.kr
Abstract
OBJECTIVE
S: Computed tomographic angiography (CTA) to diagnose intracranial aneurysms in patients with spontaneous subarachnoid hemorrhage (SAH) has been well documented and widely accepted. In this study, it was assessed whether aneurysm surgery can be performed in aneurysm patients by using CTA regardless of their status. METHODS: To assess the clinical value of CTA, we treated patients with SAH using it as the primary means of diagnosis. During the period between August 2001 and May 2003, a consecutive series of 82 cases of ruptured cerebral aneurysms were evaluated via both CTA and postoperative transfemoral cerebral angiography(TFCA), and we investigated the detectability of cerebral aneurysms. In cases of vague CTA findings, we performed TFCA preoperatively. We correlated the CTA results with operative findings and preoperative TFCA, when performed. RESULTS: In 82 patients, 100 aneurysms (96 aneurysms via CTA, 1 aneurysm via TFCA, 3 aneurysms via operation) were disclosed. The size of aneurysms detected by CTA ranged from 1.95 mm to 19.4 mm. Aneurysms that were not found via TFCA were detected by CTA in two patients. Three additional small multiple aneurysms that could not be confirmed via CTA were found through operation. No previously undiscovered aneurysms were found via postoperative TFCA. Corresponding to the operative findings, the sensitivity of CTA was 96%. CONCLUSION: According to our results, we hold that CTA is the first choice among diagnostic methods for the treatment of SAH.
Key Words: Computed Tomographic Angiography (CTA), Aneurysm, Transfemoral cerebral angiography (TFCA), Subarachnoid Hemorrhage (SAH)

Introduction


  
A large number of factors can contribute to spontaneous subarachnoid hemorrhage(SAH). Depending on such factors, a wide range of effects as well as methods for treatment exist. The most common cause is the rupturing of an intracranial aneurysm. When this occurs, two popular methods of treatment are to clip the neck of intracranial aneurysm directly or to perform endovascular surgery to occlude the aneurysm.5)24) The most accurate procedure performed not only to extract detailed data on the aneurysm's location, direction, size, shape and circulation, but to decide such initial treatment is Transfemoral Cerebral Angiography(TFCA). However, limits to this practice are invasiveness, the extensive time it takes for the completion of the procedure, thus ruling out its performance in cases where excessive hematoma gives cause for immediate emergency operation.20)25) Recently, the software and hardware technology for 3-D Computed Tomographic Angiography(CTA) has undergone amazing development and is thus once again receiving spotlight as a valuable tool for diagnosing aneurysms. However, in practice, its use as an initial diagnostic method has exposed lower-than-expected reliability, and thus CTA is commonly employed on a selective basis. Hence, the purpose of this study was to perform CTA on patients with ruptured intracranial aneurysms, regardless of their clinical status and history, and use the analysis of results as a basis for evaluating the feasibility and accuracy, as well as limitations, of using CTA as a determinant for subsequent operative measures.

Materials and Methods

1. Subjects 
  
This study was conducted from August 2001 to May 2003 to study a total of 100 intracranial aneurysm cases from which 82 patients were diagnosed via CTA after SAH. Subject patients evidenced neurological status of Hunt-Hess(H-H) grade 0-V and, barring certain cases that were transferred for endovascular treatment, all were subjected to operative measures to treat the aneurysms. During the first six months of the study, both CTA and preoperative TFCA were carried out. During the remaining six months, only CTA was used for diagnosis. If an intracranial aneurysm was observed via CTA, surgery was directly performed without the use of any other previous diagnosis method. Subsequently, as the patient reached an appropriate level of stability, TFCA was performed to examine the postoperative status and look for any other signs of diseased blood vessels. In cases where the diagnosis via CTA was excessively unclear, TFCA was performed to supplement the diagnosis. 

2. Three-Dimensional CTA procedural methodology 
   The CTA instrument employed a Somatome volume zoom (Siemens, Erlangen, Germany). Ion-free contrast media Ultravist 370(Schering AG, Berlin, Germany) was used in one phase intravenous injection of 3 cc per second with Minimum 18G angio catheters to prep for the CTA procedure. The imaging scope consisted of an area ranging from the orbitomeatal line to a parallel line 50 mm above. Depending on interpretation of the initial computed tomography(CT), the imaging could be set to include an area below the orbitomeatal line as well. In any given case, the imaging commenced after 18-20 seconds of administering the contrast material intravenously. Imaging was performed in intervals of 1.25 mm with an overlap of 0.25 mm. Hence, the finished imaging product revealed a total of 70 cross-sectional photographs at 1mm intervals. The complete scan time lasted on average 9-10 seconds. The approximate location of any intra-cranial aneurysm was found via the MIP(Maximum Intensity Projection) method and examination of the resulting axial, coronal, and sagittal cross-sectional images. Then, using the SSD(Shaded Surface Display) method, the lower image limits were set to 130-150 H.U.(Hounsfield Units), and all images were reorganized factoring out soft tissue to produce a final three-dimensional image. After reorganizing the image, radiologists and neurosurgeons were consulted to observe the intra-cranial blood vessels from various angles and refine the image around any aneurysm to reflect the correlation with surrounding bone tissue and blood vessels. Subsequently, the optimal surgical view was found, thus leading to the extraction of surrounding bone tissue to provide a focused image of the aneurysm. The time required to complete this entire process was on average 10-15 minutes. 

3. Operative measures
  
To administer endovascular treatment, excluding two cases, craniotomies were performed. In two cases in which the aneurysm was located in the posterior inferior cerebellar artery (PICA), we used the far lateral transcondylar approach. Also, as for the five cases in which the aneurysm was found in the distal anterior cerebral artery(ACA), surgery was performed using the interhemispheric approach. These cases aside, the remainder received operative procedures using the pterional approach. Surgical views confirmed the middle cerebral artery, anterior cerebral artery, internal carotid artery, posterior communicating artery, and anterior choroidal artery on the same in addition to the basilar artery and the opposite-side internal carotid artery as well as the A1 and A2 parts of the anterior cerebral artery. Among the multiple aneurysm patients, one exhibited an extremely small basilar aneurysm and then it has been followed up. Another small basilar aneurysm was also found and it was treated via muscle wrapping. In two cases where an aneurysm was found in the superior cerebellar artery, muscle wrapping was performed in one case, and clipping was done in the other. During surgery, the accuracy of the preoperative aneurysm diagnosis was assessed. In addition, following surgery and excluding those aged and/or other disease-suffering patients for whom TFCA would pose certain risks, patients were subjected to TFCA to check for the possibility of lesions in other blood vessels. 

Results

1. Patient statistics
  
Among the 82 intra-cranial patients, 31 were male, and the remaining 51 were female. By age group, the highest number, 61 cases, was found among patients from 40-60 years old, with one case of a patient in the twenties, and 13 cases of patients in their thirties. The average patient age was 53.5 years. In terms of preoperative neurological status, 77 patients registered an H-H grade of II
~IV, two registered 0, another two registered I, and one registered V. Initial CT records show a Fisher grade of II-III in 54 cases, and 14 cases each for the grades I and IV(Table 1).

2. Aneurysm statistics 
   Among the 100 aneurysms that were found, the highest number, 34, were located in the anterior communicating artery, followed by 28 in the middle cerebral artery, 16 in the posterior communicating artery, 7 in the carotid artery, 5 in the distal anterior cerebral artery, 3 in the basal artery, 2 in the superior cerebellar artery, 2 in the posterior inferior cerebellar artery, 1 in the A1 part of the anterior communicating artery, 1 in the ophthalmic artery, and 1 in the anterior choroidal artery(Table 2). There were three cases of previously undiscovered aneurysms found during surgery. The size of these aneurysms was in the microbleb level, and in terms of location, one was found in the middle cerebral artery(M1), and the remaining two found in the posterior communicating artery. 
   Via CTA, the smallest diagnosed aneurysm was 1.95 mm in size, and the largest was 19.5 mm. Statistics by aneurysm size showed that 16 were 3 mm or less, 77 were 3-10 mm, and 7 were 10-25 mm(Table 2). Among the studied patients, 79 suffered from ruptured aneurysms, and the remaining three experienced the unruptured. In terms of aneurysm form, with the exception of one being fusiform, the remainder was all of the saccular type. Sixty-nine of the patients had single aneurysm, while thirteen had multiple aneurysms more than two.

3. Unique characteristics and accuracy level of CTA 
   During surgery, the 96 aneurysms diagnosed via preoperative CTA were confirmed, as well as the one aneurysm that was not discovered via preoperative CTA and thus required TFCA for detection. A total of three aneurysms that were not discovered prior to operation were found during surgery. One of the three escaped preoperative detection via CTA as well as TFCA. The other two represented non-hemorrhaging aneurysms that were not discovered via CTA and had not been subjected to TFCA. In contrast, there were a total of three cases of aneurysms that were not shown via TFCA, but were diagnosed via CTA the following day and were thus confirmed through surgery. Hence, the correct diagnosis rate of CTA was measured at 96%. 

4. CTA-Related complications 
   Although there were three cases in which the venipuncture sites were close to the rupture sites and thus leakage of the contrast media presented possible danger, they were all detected early, and thus any possible complications were avoided. In addition, there were no cases of other possible complications such as rebleeding and any of those related to evaluation procedures including vasospasms, air embolisms, infections, hematomas, etc.

5. Postoperative results 
   From a neurological standpoint, postoperative results showed 52 cases as "good", 13 as "fair", 10 as "poor", and 7 resulting in "death". Factors found leading to the cases ending in death showed four cases due to vasospasms, two due to septic shock, and the last due to acute myocardial infarction.

Discussion

   For the diagnosis of SAH and other cerebrovascular diseases, the most common and widely used method is TFCA.1)2)5)7)17)19)20)28)31) Not only does TFCA offer the most accurate cerebrovascular imaging, its diagnostic value is made even higher by the fact that it yields much information on collateral circulation and hemodynamics. However, there is a higher risk for complications including a rebleeding of the aneurysm during the procedure(especially within the first six hours) due to the prolonged period of time that it takes for completion. In addition, due to the risk of other complications such as cerebral infarctions following air embolisms and possible kidney damage or hemorrhaging, the procedure is not recommended for patients suffering from other disorders such as renal disease or bleeding tendency and the elderly.20)25)28) Furthermore, to obtain suitable surgical views, the patient can be exposed to larger levels of contrast media and radiation. The probability of complications occurring from TFCA differs according to various expert opinions. However, the generally accepted probability is approximately 0.25-1%, with the rate being higher for elderly patients.16)17)20)24) On another hand, Velthuis et al.29) have stated the probability for false negative value from TFCA to be 5-10%, and Grandin et al.7) put the rate at 6%.
  
Two methods that present relatively less risk for complications and are also non-invasive are magnetic resonance angiography(MRA) and CTA. Recent developments in MRA technology have resulted in higher diagnosis rates for intracranial aneurysms with Ogawa et al. stating the sensitivity at 91-94%. However, with MRA, the accuracy of diagnosis varies with the size of the aneurysm, and one weakness that is inherent is the notable falloff in accuracy for aneurysms smaller than 3 mm. The sensitivity of 1.5T MRA imaging is 79-93% for aneurysms of 3 mm or higher, and the corresponding diagnostic specificity is 92-100%. However, when the aneurysm is less than 3 mm in size, the diagnostic rate falls to around 60%.14)20) Statistics from a study of aneurysm diagnosis via MRA performed by Grandin et al.7) on a sample of 140 patients revealed overall sensitivity of 91-94% and specificity of 100%, with 80-88% sensitivity for aneurysms of 5mm or less in size. In another study by Korogi et al.,8) the sensitivity for aneurysms of 5mm or less in size was reported at only 63%. Indeed, many experts consider the aneurysm size of 5mm in diameter to be a critical point.12)14)15) Some drawbacks to MRA are the prolonged length of time required as well as the drop in accuracy if the patient makes any slight movements during the procedure. In addition, if the clinical status is poor and/or the various instruments are required, the monitoring of patients may be difficult. Also, in recurred patients, the diagnosis rate drops substantially for any aneurysms located in the proximity of the clip area of the previous aneurysm surgery, and accurate diagnosis is much more difficult to achieve with turbulent aneurysms and/or when the blood flow is very slow. Due to all these factors, the use of MRA is limited.7)20)23)27)
  
CTA differs compared to MRA as well as conventional angiography in that it can be performed fairly quickly to yield the selected results. Thus, to date, it has been used on a limited basis to provide quick and essential diagnostic information in cases that demand immediate operation such as for patients with large hematomas resulting from ruptured aneurysms.2)19) Although when compared to TFCA, CTA offers the benefits of being faster to complete, less invasive, less exposing to radiation, and cheaper, it does not facilitate the discrimination of arteries and veins as well as offer any information on collateral circulation and hemodynamics.1)3)20) Moreover, CTA can be notably less accurate in finding very small aneurysms or those located in atypical areas such as the cavernous sinus or infraclinoid as well as aneurysms that are in close proximity to the clipped area from any previous aneurysm surgery. Using CTA as a substitute for conventional angiography can therefore pose a number of problems. Barring emergency situations, the use of TFCA is most frequently recommended.1)2)6)13) In contrast, Zouaoui et al.31) and Reiger et al.23) reported that results from CTA and conventional angiography were not significantly different, and thus CTA was a viable substitute for conventional angiography. Furthermore, Velthuis et al.28) asserted that preoperative TFCA was not necessary for the diagnosis of aneurysms. In 1996, Hsiang et al.13) purported the effectiveness of CTA, citing numerous cases in which early-stage aneurysms were spotted via CTA and treated after escaping diagnosis via conventional angiography. In this study as well, three cases were recorded in which aneurysms were discovered via CTA on the following day after these aneurysms had avoided detection via TFCA. In Korea, Chun et al.5) emphasized the value of three-dimensional CTA in the early operative treatment of serious intracranial aneurysm patients and asserted the feasibility of substituting conventional angiography with CTA. The diagnostic sensitivity of CTA is commonly reported as 96-100%20) but has shown variance in a number of studies:Hashimoto et al.9) 77-97%, Chen et al.4) 96.8%, Hope et al.11) 90% sensitivity and 50% specificity, Ogawa et al.22) 77% sensitivity and 87% specificity, Vieco et al.30) 97% sensitivity and 100% specificity, Alberico et al.1) 96% sensitivity and 100% specificity, and Hsiang et al.13) 95% sensitivity and 83% specificity. In the study performed by Matsumoto et al.,20) 100% sensitivity was reported with not one case of false positive results. Such results speak to the assertion that CTA does not have any significant weaknesses when compared to MRA and TFCA. In 2004, Hoh et al.10) performed a study of 223 aneurysm patients, subjecting them to both CTA and TFCA, to find that the diagnostic sensitivity of both methods were the same, and thus purported that the lone use of CTA was absolutely feasible. In this study, the diagnostic accuracy of CTA proved to be 96%, and among the total of 100 aneurysms, the three that were not discovered prior to surgery but were confirmed during operation were of particularly small size.
  
Previously considered as limited by technology, the diagnosis of aneurysms in such nether regions of the cranium such as the occiput and cranial base is becoming increasingly feasible, especially due to the rapid development of related software as well as spiral-computed tomography. In addition, with it being possible to obtain three-dimensional images from desired angles that clearly show the surrounding bony structure and correlation with such solid masses, it has become easier to plan the surgical procedure prior to operation.4)8) In this study, when signs of an aneurysm were present after examining the circulation results from initial CT, CTA was done with parameters reset to the inferior regions of the orbitomeatal line. In this way, aneurysms in the posterior inferior cerebella artery(Fig. 1) were found. Aneurysms located in the ophthalmic artery(Fig. 2) were found through the manipulation of three-dimensional imaging and examination of vessels and bony structure from various angles. In addition, Tampieri et al.26)27) pointed out that in cases where thrombus exists within an aneurysm and thus makes it virtually impossible to inject contrast media, CTA allowed for easy viewing of the aneurysm and its correlation with surrounding blood vessels to facilitate proper diagnosis.
   The diagnostic accuracy rate of CTA varies by the size of the aneurysm. Such variance can be seen in a number of studies such as that done by Alberico et al.

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