Korean Journal of Cerebrovascular Surgery 2007;9(2):87-93.
Published online June 1, 2007.
Angiographic Characteristics of the Intracranial Saccular Aneurysms to Predict the Rupture.
Park, Soon Don , Won, Yu Sam , Kwon, Young Joon , Yang, Jae Young , Choi, Chun Sik
Department of Neurosurgery, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea. yusam.won@Samsung.com
Abstract
OBJECTIVE
During the last two decades, detection of unruptured intracranial aneurysms has increased because of the improving diagnostic methods, but the management of unruptured intracranial aneurysm is still controversial. We analyzed the angiographic characteristics to compare ruptured aneurysms with unruptured aneurysms. METHODS: The patients were retrospectively selected for this study based on the availability of angiograms and a clear diagnosis of an unruptured or ruptured aneurysm. One hundred sixty nine patients with 209 aneurysms were included in the study. Sixty-one patients harbored only unruptured lesions, 85 only ruptured lesions and 27 had both ruptured and unruptured lesions. RESULTS: The mean age of all the patients was 55.3 years, and it was 53.34 years for those with ruptured aneurysms. It was found that 42.0% of the ruptured aneurysms were on the anterior communicating artery, compared with 10.3% of the unruptured aneurysms. None of the ophthalmic artery aneurysms were ruptured. The mean dome size, depth and aspect ratio of the ruptured aneurysms, except for the neck size, were significantly larger than that of the unruptured aneurysms, but the mean neck size of the ruptured and unruptured aneurysms showed no significant difference. A daughter sac was present in 7.2% of the unruptured aneurysms and in 17.0% of the ruptured aneurysms. CONCLUSION: We suggest that the morphologic features and location of aneurysms should be considered when making decisions regarding whether to treat unruptured aneurysms.
Key Words: Ruptured aneurysm, Unruptured aneurysm, Aspect ratio, Anterior communicating artery aneurysm

Introduction


  
Despite recent improvement in surgical and medical management of aneurysmal subarachnoid hemorrhage (SAH), the overall mortality rate in this disease is high (approximately 40
~50%).6)7)13) The high mortality and morbidity rates are attributed mainly to brain damage caused by a severe initial hemorrhage, early rebleeding, and delayed cerebral ischemia. 
   Because of the development of increasing advanced methods for intracranial vascular imaging and the increased attention of health, screening test (MR or CT angiography) became more popular and the identification of unruptured intracranial aneurysm is becoming more common. Most intracranial aneurysm do not rupture, so their identification creates a serious dilemma for neurosurgeons with regard to whether to treat on patients with incidentally discovered unruptured aneurysms, because a rupture of such an aneurysm can lead to catastrophic results. Therefore, the decision to perform preventive treatment for an unruptured aneurysm must be based on a prediction of which aneurysms are most likely to develop a rupture. 
   To find the differences between the angiographic features of the ruptured aneurysm and the unruptured aneurysm, we analyzed the angiographic characteristics between the ruptured aneurysms with the unruptured aneurysms. 

Materials and Methods 

Patient population 
   From October 2002 to December 2006, 169 patients with aneurysmal SAH or unruptured aneurysm were admitted to our hospital. Patients for this study were based on the availability of angiograms and a clear diagnosis of an unruptured or ruptured aneurysm. Patient age and sex, and the location of the aneurysm were also recorded. The sex distribution in these patients was 35.4% male and 64.6% female. The mean age of the patients was 56.3 years and the median age was 55 years. The number of aneurysms per patient were one in 138, two in 26, and three in 5 patients. In patients with multiple aneurysms, the aneurysm that ruptured was determined using standard radiological and clinical methods such as the following: the pattern of blood on a computerized tomography scan; the relative size, site, and loculations on an angiogram; and the operative findings. 

Statistical analysis 
   A spreadsheet with statistical functions (Microsoft Excel; Microsoft Corp., Redmond, WA) was used for preliminary calculations; all other analysis were performed using a statistical software package (SPSS for Windows version 10.0 : SPSS INC., Chicago, IL). Categorical variables were compared by Fisher exact test. Continuous variables were compared among groups by using Student's t-test. Bivariate association of continuous variables was tested by Pearson correlation coefficients.
   To compare the utility of aneurysm size, depth, and aspect ratio more fully for discriminating between ruptured and unruptured aneurysm, we performed an ROC(Receiver Operation Characteristic) analysis. The ROC analysis is commonly used when evaluating diagnostic tests. The ROC curve is used to plot the tradeoff between sensitivity and specificity, and the closer the curve is to the upper left-hand corner of the plot the better the discrimination. 

Angiographic examination 
   The anteroposterior, mediolateral, and oblique views were routinely recorded. The maximum longitudinal diameter between the aneurysmal neck and dome, the maximum transverse diameter of the dome, and the maximum transverse diameter of the neck were recorded. The aspect ratio 1 was calculated from the dome size divided by the neck width and the aspect ratio 2 from the depth divided by the neck width (Fig. 1). 
   Lobulation was divided into unilobular, multilobular, which was defined as irregular appearance or one or more additional blebs with neck wider than the largest diameter of bleb. A daughter sac was defined as a second aneurysmal sac/bleb arising from the actual aneurysmal sac with a neck smaller than the largest diameter of the daughter aneurysm. 

Results 

   We identified 209 aneurysms with available size information including 97 unruptured and 112 ruptured lesions. The mean age of the patients harboring the ruptured and unruptured aneurysms was 53.3 years and 57.6 years, respectively. Table 1 shows the number of lesions at each of th several locations studied. It was found that 42.0% of the ruptured aneurysms were on anterior communicating artery, compared with 10.3% of the unruptured aneurysms. None of the ophthalmic artery aneurysms were ruptured. Twenty four unruptured aneurysms (24.7%) were on the middle cerebral artery. The mean size at each location shows no statistical significance excluding the pericallosal artery. 
   In Table 2, the mean values of dome size, depth, neck width, aspect ratio 1, and aspect ratio 2 of aneurysms at the ruptured and unruptured groups are shown. We analyzed the mean values using the independent sample t-test at the ruptured and unruptured groups. The difference between two groups for the mean dome, depth, aspect ratio 1, and aspect ratio 2 were statistically significant. The difference in neck width in two groups was not found to be significant (p = 0.297). It is important to note that in 67% of patients with multiple aneurysms, the aneurysms with highest aspect ratio had ruptured. 
   The dome size and depth did not increase significantly with increasing patient age, although the depth and neck size increased with increasing dome size at both groups (Fig. 2). 
   Thirteen unruptured aneurysms (13.7%) showed a multilobular appearance compared with 27 ruptured aneurysms (24.1%). A daughter sac was present in 7.2%(7/97) of unruptured aneurysms and in 17.0% of ruptured aneurysms (19/112). It showed the statistical significance (Table 3). 
   The results of the ROC analysis are depicted in Fig. 3. The area under the ROC curve for the dome size, depth, aspect ratio 1, and aspect ratio 2 is 0.66 (95% CI 0.58-0.74), 0.67 (95% CI 0.59-0.75), 0.73 (95% CI 0.66-0.80), and 0.73 (95% CI 0.66-0.79), respectively. This result shows that each index has the similar predictive capability and statistical significance, but is not ideal. 

Discussion 

   Unruptured aneurysms are becoming an increasingly important neurosurgical problem because of the advent of innovation in diagnostic technology. To manage patients with unruptured aneurysms rationally, we must know the natural history of these lesions. We must also use a reliable index to predict aneurysmal rupture. Although aneurysm size is theoretically and empirically an important predictor for the occurrence of SAHs, the critical size for a rupture remains controversial. The recently published prospective part of The International Study of Unruptured Intracranial Aneurysms (ISUIA; patient enrollment in 61 centers between 1991 and 1998) reported that overall incidence of aneurysm rupture was 0.8% ; relative risk for rupture of vertebrobasilar aneurysms was 2.3 as compared with other aneurysms ; a limit of aneurysms for very low risk for rupture in patients without a prior SAH was below 7 mm. Some authors reported that unruptured aneurysms may affect from 2 to 10% of the general population2)11)12)16)24) and whereas the incidence of SAH is relatively low, with an annual rupture rate of approximately 1 to 2% per year.8)11)18)28)29) Therefore, the decision to perform preventive surgery for an unruptured aneurysms must be based on a prediction of which aneurysms are most likely to develop a rupture. So, identifying reliable indicators of risk for rupture of an intact lesion could vastly improve clinical management of intracranial aneurysm. Aneurysm size is a well-recognized risk factor in predicting aneurysm rupture. However, there is little consensus regarding a threshold value at which to treat these aneurysm.9)20)22) In our study, aneurysm size(dome size), depth, and aspect ratio 1 & 2 were statistically significant. Although the existence of a magic threshold in index for the risk of rupture is not proven, it shows probability of rupture increase with the increase of morphological index. 
   Black and German4) investigated the relationship between aneurysm size and neck width with a venous pouch graft model. The characteristic of the neck and size of the aneurysm has a definite relationship to the velocity of blood flow into and out of the aneurysm. The area of the neck is a factor in limiting blood flow into and out of the aneurysm. Within the aneurysm, velocity of blood is inversely proportional to the aneurysm's volume. Thus, the larger the aneurysm in proportion to the aneurysm neck, the more sluggish the blood flow will be and the longer the blood will remain within the aneurysm. Roach17) studied the relationship between the neck size and aneurysmal thrombosis and rupture with a canine tail artery aneurysm model. She caused aneurysms to obstruct the tail artery in variable lengths. She found that short aneurysms were unaltered after 2 weeks, medium-size aneurysms ruptured, and long ones thrombosed. Thus, the aspect ratio should be a good parameter by which to express the intra-aneurysmal flow condition. Bryce et al.27) suggested that aspect ratio (dome/neck ratio) might be useful index. Ujiie and colleague23)25)26) hypothesized that flow stagnation might precipitate aneurysm rupture. Such condition is more likely to occur in aneurysm having a long depth in relation to a small orifice. In our analysis, although the aspect ratio is not a ideal index, the rupture and the aspect ratio showed a positive correlation. 
   In virtually all major surgical series of ruptured aneurysms, the ACoA site is the most common, but in all the major series of unruptured aneurysms it is the least. Weir et al.27) reported that aneurysms of ACoA had a increased tendency to rupture at smaller sizes relative to MCA site. Clark study5) showed that the internal carotid artery was the most common site for unruptured aneurysms (38%). Aneurysms located in the posterior circulation had an overall annual bleed rate of 1.8%. This compared with 0.49% for the anterior circulation. The bleed rate from aneurysms of the posterior communicating artery (0.46%) was similar to that of the rest of the anterior circulation. In our study, ACoA had the higher percentage of ruptured aneurysms than other sites. Our study shows there are 47 AcoA ruptured aneurysms (42.0%) and the mean size is not larger than the unruptured aneurysm. We suggest that incidentally found aneurysms of ACoA need aggressive treatment despite of the small size. 
   Other factors, such as the morphology of the aneurysm, is an important risk factor in predicting aneurysm rupture. Raghavan et al.15) reported that they quantified the size and shape indices of intracranial aneurysms by using threedimensional computerized tomography angiography models of the brain vasculature and quantified shape was more effective than size in discriminating between ruptured and unruptured aneurysms. Sakamoto et al.21) reported that irregularities of the aneurysmal wall and the existence of a daughter aneurysm attached to the main aneurysm had a tendency to rupture. Asari and Ohmoto1) investigated the factors for predicting subsequent ruptures in a series 54 patients with 72 unruptured cerebral aneurysms during a mean follow up period of 44 months. The authors found that the shape (multilobular) and location of the aneurysm and the presence of hypertension were the most important factors for predicting a subsequent rupture. In our study, there was a significant difference in lobulation and presence of daughter sac. 
   To reach a decision regarding the treatment of an asymptomatic unruptured aneurysm, other contributing factors such as the patient's age and average number of years of life remaining for different age groups, the patient's history of smoking and familial aneurysms, an association with autosomal dominant polycystic kidney disease, and aneurysm morphology, especially loculation (daughter aneurysms), should be taken into account.14) A Finnish study showed that the prevalence of intracranial aneurysms among the familial cases was 10 times higher than the rate found in the average population.19) Of the patients with familial aneurysms that ruptured, 60% were 50 years of age or younger.10) 
   The limitation of this study include its retrospective nature, subjective bias in determining aneurysm dimension, and the special patient population resulting from the selection and referral bias. A common limitation in using aneurysm shape as predictor of aneurysm rupture is the use of 2D angiographic data for determining and calculating shape feature such as aspect ratio. Standard cerebral angiographic projections are 2D images. Cerebral aneurysm are often asymmetrical structures that do not allow for simple extrapolation of 3D morphology from 2D data. Thus the measurements of geometric features can vary with the angiographic projection used, resulting in multiple findings for the same aneurysm. This phenomenon may partially explain the contradictory findings of different reports in regard to the effect of aspect ratio and risk of aneurysm rupture.3)26) Another potential source of bias is that a relatively large percentage of patients harbored multiple aneurysm and in patients with multiple aneurysms, it is not always possible to identify with certainty which aneurysm has ruptured. 

Conclusion 

   This study shows that aneurysms on ACoA site and aneurysms having lobulation and daughter sac were found much more in ruptured group. The difference between two groups for the mean dome size, depth, aspect ratio 1, and aspect ratio 2 were statistically significant, but each index is not ideal for the prediction of aneurysm rupture. Although there is not optimal predictor to rupture, we suggest that small unruptured aneurysms with lobulation/daughter sac or high aspect ratio should be treated. 


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