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Correlation Between the Aneurysm Morphometry and Severity of Subarachnoid Hemorrhage in the Posterior Cerebral Circulation
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Correlation Between the Aneurysm Morphometry and Severity of Subarachnoid Hemorrhage in the Posterior Cerebral Circulation Tomasz Tykocki1 and Bogusław Kostkiewicz2
Key words Aneurysm - Fisher revised scale - Morphometry - SAH - WFNS scale -
Abbreviations and Acronyms FRS: Fisher revised scale IA: intracranial aneurysm SAH: Subarachnoid hemorrhage SR: Size ratio WFNS: World Federation of Neurosurgical Societies WSS: Wall shear stress From the 1Department of Neurosurgery, Institute of Psychiatry and Neurology; and 2Department of Neurosurgery, Central Clinical Hospital Ministry of Interior, Warsaw, Poland To whom correspondence should be addressed: Tomasz Tykocki, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6:1100-1105. http://dx.doi.org/10.1016/j.wneu.2014.07.007 Supplementary digital content available online. Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION The dilemma concerning the optimal treatment of unruptured intracranial aneurysms (IAs) raises many controversies. The predictors of the risk of aneurysm rupture, estimated by presuming that morphometric absolute dimensions of aneurysmal complex are sufficient to definitely postulate the aneurysmal rupture risk, are not necessarily reliable. Conclusions from the International Study of Unruptured Intracranial Aneurysms, a classic study aimed to assess the natural history of unruptured aneurysms, has constituted that the aneurysm size alone correlates independently with the risk of rupture (8). On the contrary, however, other studies have emphasized different findings, raising the greater incidents of subarachnoid hemorrhage (SAH) from small aneurysms (11, 21). To improve the decision making in clinical practice, there
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- OBJECTIVE:
The aim of the study was to examine the correlation between various morphometric factors of the posterior circulation aneurysms and the severity of neurologic status and radiologic extent of subarachnoid hemorrhage.
- METHODS:
A total of 105 patients with ruptured posterior circulation aneurysms (IAs) were retrospectively analyzed in the study. The neurologic status was graded in World Federation of Neurosurgical Societies (WFNS) scale and radiological severity of subarachnoid hemorrhage was assessed in Fisher revised scale (FRS). All patients were qualified for 3-dimensional digital subtraction angiography. The following morphometric measurements were taken: dome size, dome-to-neck ratio, neck size, parent artery size; size ratio (SR), neck-to-parent artery ratio, inflow angle, and diameters of posterior circulation arteries. The univariate and the multiple regression models were used for all independent variables. The significant predictors were compared between ruptured and unruptured IAs.
- RESULTS:
Univariate regression analysis revealed that inflow angle influenced grading in WFNS and that FRS grades were positively correlated with SR, dome-toneck ratio, and inflow angle. The multiple regression model confirmed that inflow angle is an independent factor influencing WFNS scale. FRS is affected by 2 factors: SR and inflow angle. SR was more strongly correlated with FRS (r [ 0.403) than with inflow angle (r [ 284). The comparison of inflow angle and SR in ruptured and unruptured IAs showed a significant difference between means, 125.18 21.86 versus 103.86 17.7 degrees and 2.48 0.46 versus 1.91 0.45, respectively. The cut off points were 115.9 degrees for inflow angle and 2.31 for SR.
- CONCLUSION:
Inflow angle and SR were found to be correlated with grading in FRS, and WFNS scale was correlated with inflow angle.
was an expectation for establishing other unequivocal factors affecting the likelihood of aneurysm rupture. Different morphologic parameters such as size ratio (SR), aspect ratio, inflow angle, undulation index, ellipticity index, and nonsphericity index are believed to contribute significantly in determining the risk of aneurysm rupture (1, 5, 16, 20, 23). The impact of SR in the morphometric-based extrapolation of SAH probability has been proven in several studies (5, 16, 20). SR, defined as the ratio of aneurysm maximal size divided by the average parent vessel diameter based on 2-dimensional angiographic data, is a simple arithmetic formula sufficient to be routinely applied in the daily practice (16).
The impact of the morphologic features of the aneurysm on the clinical course and severity of bleeding after SAH, however, still remains unexplored. In this study, the authors decided to examine the correlation between various morphometric factors of the posterior circulation IAs and commonly applied scales: The Fisher revised scale (FRS) and World Federation of Neurological Surgeons (WFNS) Scale. The study was based on the population of posterior cerebral circulation IAs. METHODS A total of 105 patients (62 women and 43 men) with ruptured posterior circulation aneurysms who were diagnosed and
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treated between 2008 and 2012 at Central Clinical Hospital Ministry of Interior in Warsaw were retrospectively analyzed in the study. The patients’ neurologic status was based on the retrospective analysis of the medical records. All patients were evaluated with the WFNS scale at the time of admission to the Department of Neurosurgery. The severity of SAH was assessed with the FRS based on computed tomography (CT) imaging (Table 1), which had been performed within 24 hours from the onset of SAH symptoms. Grade 0 in FRS was interpreted as no SAH on CT but present in the cerebrospinal fluid test. The following morphometric measurements of the aneurysmal complex (independent variables) were taken: aneurysm dome size, neck size, parent artery size, dome-to-neck ratio, SR (¼ maximum aneurysm dome size, defined as the largest distance between any 2 points on the aneurysm dome surface /vessel diameter), neck-to-parent artery ratio, and inflow angle (Figure 1 and Figure 2 A,B). In the aneurysm involving more than one parent vessel, the mean diameter from all vessels was included. In addition the measurements of posterior circulation arteries were collected: diameters of posterior cerebral right and left arteries at P1 region (precommunicating segment), diameters of right and left vertebral arteries below the level of basilar artery, and the maximum diameter of basilar artery. Demographic and medical history data were obtained from medical records. All demographic factors, including age, sex, smoking history, and hypertension also
ANEURYSM MORPHOMETRY AND SEVERITY OF SAH
source, cross-platform, software system for 3-dimensional computer graphics, the Visualization Toolkit libraries (http:// www.vtk.org/). All angiographies within SAH group were obtained emergently within 48 hours from the admission to the hospital, and before the onset of vasospasm. Size measurements were performed by 2 neurosurgeons in a blinded fashion with respect to the rupture status of the aneurysms. The intraclass correlation coefficient for 2 raters was 0.90.
Figure 1. Schematic drawing presenting the morphometric parameters. d indicates the maximal aneurysm dome size; h indicates the aneurysm dome depth; n the neck size; a is the parent artery diameter; a the inflow angle; F the blood flow direction. The size ratio is determined by d/n.
were tested in stepwise regression models as potentially influencing on the morphometric results.
PATIENT SELECTION All patients were qualified for diagnostic 3-dimensional rotational angiography by a team of doctors consisting of a neurosurgeon, neuroradiologist, and an anesthesiologist. Three-dimensional reconstruction was performed by the use of an open-
Statistical Analysis All the results were statistically analyzed using the computer software MedCalc 12.7; (Ostend, Belgium). Statistical significance was assumed for P < 0.05. The continuous data were expressed as means standard deviation. One-way analysis of variance was used to test for morphometric differences among FRS and WFNS groups. The univariate regression analysis was first used to test all the independent variables as potentially influencing on the grading in WFNS scale and FRS. Then the significant factors were tested in the stepwise multiple regression model. After the predictors had been defined, authors compared them between ruptured and unruptured IAs. The unruptured IAs were retrospectively obtained from the same
Table 1. Fisher Revised Scale Grade 0
No SAH or IVH
Grade I
Minimal/thin SAH, no IVH in either lateral ventricle
Grade II
Minimal/thin SAH, with IVH in both lateral ventricles
Grade III
Dense SAH,* no IVH in either lateral ventricle
Grade IV
Dense SAH,* with IVH in both lateral ventricles
SAH, subarachnoid hemorrhage; IVH, intraventricular hemorrhage. *Completely filling 1 cistern or fissure.
Figure 2. Three-dimensional rotational angiography of basilar tip aneurysm in coronal (A) and sagittal (B) view, presenting the concept of measurement performed in the study. d, maximal aneurysm dome size; h, aneurysm dome depth; n, neck size; a, inflow angle; a, parent artery diameter; p1, diameter of precommunicating segment of the posterior cerebral artery; B, diameter of basilar artery trunk; and V, diameter of vertebral artery.
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database, the same time period, and their morphometric characteristics were defined in the same way as for ruptured IAs. There were 86 unruptured IAs. The interactive dot diagrams were created to compare the morphometric factors between ruptured and unruptured IAs and to calculate the cut off values. RESULTS A population sample of 105 patients with ruptured IAs underwent a retrospective analysis. The grading distribution in WFNS scale was: I (21; 20%); II (23; 21.9%); III (27; 25.7%); IV (18; 17.1%); V (16; 15.2%) (Table 2), and in FRS, grade 0 (7; 6.7%), I (30; 28.6%), II (28; 26.7%), III (23; 21.9%), IV (17; 16.2%) (Table 3). Univariate regression analysis revealed that inflow angle influenced WFNS grade (P ¼ 0.045) and that FRS grades were positively correlated with SR, dome-toneck ratio, and inflow angle. The increasing values of SR and inflow angle predicted the growth of grading in the FRS (Figure 3 A,B). The multiple stepwise regression model confirmed that inflow angle was a sole independent factor influencing WFNS scale; the strength of
ANEURYSM MORPHOMETRY AND SEVERITY OF SAH
this relationship was moderate (correlation coefficient r ¼ 0.37) (Figure 4). A 1-grade increase in WFNS scale was associated with the growth of inflow angle by 5.9 degrees above 109.6 degrees. FRS is affected by a combination of 2 factors: SR and inflow angle. Dome-toneck ratio was eliminated during the analysis. For every 1-grade increase in FRS, SR is expected to be higher by 0.2 above 2 and inflow angle to increase by 4.5 degrees above 110.6 degrees; however, SR was more strongly correlated with FRS (r ¼ 0.403) than with inflow angle (r ¼ 284). The comparison of inflow angle and SR in ruptured and unruptured groups showed a significant difference between mean results, 125.18 21.86 versus 103.86 17.7 degrees (P < 0.05) and 2.48 0.46 versus 1.91 0.45 (P < 0.05) respectively (Figure 5). Detailed results of the analysis of variance comparison of the inflow angle and SR in both scales are presented in Tables S1, S2, and S3. In further comparison of these 2 predictors against the demographic factors (age, sex, smoking and hypertension), we did not find any significant differences (Figure 5). Inflow angle and SR were tested against the rupture criterion by the use of
interactive dot diagram. The values of cutoff points were 115.9 degrees (inflow angle) (Figure 6A) and 2.31 (SR) (Figure 6B). DISCUSSION Controversy and ambiguity regarding the treatment of unruptured aneurysms is still present despite the fact that this issue has been repeatedly taken in the literature and clinical trials. The conclusion of the International Study of Unruptured Intracranial Aneurysms study, in which the investigators highlight the key role of the absolute aneurysm size in predicting of SAH has been criticized (8). Epidemiologic data show that the majority of ruptured aneurysms (about 80%) are less than 10 mm (11, 21). On the basis of these data, it could be definitively assumed that smaller aneurysms rupture more often. However, based on recent reports, SR was introduced and proven to be a significant predictor of IA rupture (5, 16, 20). The concept of this ratio takes into account the relationship between the parent vessel and the aneurysm dome, which is more akin to the anatomy and circulation of the aneurysmal complex.
Table 2. Morphometric Results of the Aneurysms in WFNS Scale WFNS Scale I
Basilar artery, mm
N
Mean
21
4.99
II
III
SD
N
Mean
SD
N
Mean
1.42
23
5.32
1.99
27
4.61
IV SD
N
Mean
1.25
18
4.54
V SD
N
Mean
0.43
16
5.58
SD 0.83
Dome/neck
21
2.75
0.98
23
3.18
0.88
27
2.50
0.54
18
3.36
0.81
16
3.45
1.06
Inflow angle, degrees
21
109.16
21.82
23
113.83
5.39
27
121.30
21.35
18
126.45
33.87
16
129.23
24.45
Dome size, mm
21
10.79
4.46
23
11.36
4.06
27
10.35
2.84
18
10.67
0.31
16
12.18
2.64
Neck size, mm
21
3.16
2.96
23
3.93
1.82
27
4.13
0.23
18
4.34
0.47
16
5.57
1.47
Neck/parent artery
21
1.04
0.39
23
0.80
0.14
27
0.91
0.08
18
0.82
0.09
16
0.95
0.11
P1 right, mm
21
3.13
0.89
23
3.56
0.91
27
2.89
1.54
18
2.47
0.90
16
3.17
0.63
P1 left, mm
21
3.01
1.04
23
3.20
1.14
27
3.01
1.41
18
2.20
1.15
16
3.14
0.52
Parent artery, mm
21
5.11
2.14
23
4.85
1.78
27
4.58
0.65
18
2.93
0.91
16
5.95
2.00
Size ratio
21
2.18
0.80
23
2.51
0.74
27
2.24
0.30
18
2.78
0.97
16
2.91
0.94
Vertebral artery right, mm
21
3.84
1.14
23
4.22
1.38
27
3.83
1.03
18
3.01
0.16
16
4.02
0.43
Vertebral artery left, mm
21
3.94
1.18
23
4.30
1.85
27
3.90
1.27
18
3.89
0.16
16
4.47
0.37
WFNS, World Federation of Neurosurgical Societies; SD, standard deviation; P1, precommunicating segment of the posterior cerebral artery.
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Table 3. Morphometric Results of the Aneurysms Using the Fisher Revised Scale Fisher Revised Scale 0 N
Mean
Basilar artery, mm
7
Dome/neck
I
II SD
N
Mean
4.62
1.62
28
2.70
1.02
28
III
SD
N
Mean
4.29
1.25
30
7
2.74
0.66
30
Inflow angle, degrees
7
108.86
17.70
30
115.8
20.3
28
117.1
26.7
23
Dome size, mm
7
7.89
2.75
30
11.8
4.8
28
12.2
4.3
23
Neck size, mm
7
2.09
1.38
30
3.28
28
1.52
23
3.24
IV
SD
N
Mean
SD
N
Mean
5.22
2.38
23
4.96
1.01
17
5.37
0.74
2.85
0.41
23
3.65
0.16
17
3.52
1.07
123.5
6.3
17
128.7
18.9
11.1
2.8
17
12.3
2.9
0.87
17
4.52
3.05
4.59
SD
1.72
Neck/parent artery
7
0.51
0.09
30
0.93
0.21
28
0.88
0.17
23
0.86
0.07
17
1.11
0.56
P1 right, mm
7
2.33
0.86
30
2.96
0.65
28
3.10
1.27
23
2.71
0.94
17
3.88
0.78
P1 left, mm
7
2.42
0.87
30
2.76
0.69
28
2.78
1.07
23
2.43
1.07
17
3.87
1.17
Parent artery, mm
7
4.06
1.52
30
4.15
2.06
28
5.29
1.21
23
4.49
1.01
17
4.81
2.37
Size ratio
7
1.89
0.46
30
2.34
0.63
28
2.46
0.40
23
2.77
0.29
17
2.94
1.18
Vertebral artery right, mm
7
2.91
0.68
30
3.77
1.19
28
3.93
1.36
23
3.20
0.87
17
4.23
0.62
Vertebral artery left, mm
7
2.83
0.71
30
3.71
1.06
28
4.06
1.95
23
3.31
0.99
17
4.57
1.07
SD, standard deviation; P1, precommunicating segment of the posterior cerebral artery.
In this study, authors decided to investigate the impact of SR on the neurologic status and severity of SAH on CT imaging. It was found that inflow angle affected both the WFNS scale and FRS; however, the correlation coefficient in these cases was less than 0.4 showing a very weak relationship. Other morphometric factors investigated in the study, including diameters of the aneurysm parent arteries in the posterior circulation, did not appear to be significant. Nikolic et al. (13) reported
the average value of the angle in ruptured aneurysms of 139.22 degrees and in unruptured 101.73 the last value was significantly smaller. Dhar et al. (5) found that 81.8% of all unruptured IAs had aneurysm angles less than 112 degrees. According to Suga at al. (18), the greatest risk of rupture occurs at an angle of 160170 degrees and the rarest risk of rupture at an angle of 80130 degrees. Inflow angle is a significant discriminant of rupture status in aneurysms and is
Figure 3. Box-and-whisker plots showing the distribution of inflow angle (A) and size ratio (B) in Fisher revised scale grades. The middle horizontal line represents the median and the central box indicates the values from the lower to upper quartile (2575 percentile) whiskers extend from the minimum to the maximum. The means for every grade are connected by a dotted line. Error bars represent one standard deviation.
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associated with significantly greater peak velocities (increasing 80-fold from 0.004 m/s at 60 to 0.32 m/s at 140 ) and kinetic energy (increased 20-fold from 9.2 109 J at 60 to 1.8 107 J at 140 ) transmission to the dome (1). Greater inflow angle led to a 7.2-fold increase of wall shear stress (WSS) and spatial gradient increasing 5.6-fold. To summarize, the greater inflow angle results in more direct flow into the aneurysm dome and more often a parallel axis of the aneurysm relative to the parent vessel in ruptured aneurysms (2, 17, 19). These altered blood flow parameters within the aneurysm complex may trigger a neurodegenerative cascade originating from epithelial dysfunction and proinflammatory signal pathways are activated (3, 15, 22). The importance of SR ratio is emphasized in many studies. Xiang et al. (23) showed that for a unit increase in the SR of an IA, the odds of IA rupture increased by 2.96. SR was also inversely correlated with low WSS (23), defined as the areas of the aneurysm wall exposed to a WSS below 10% of the mean parent arterial WSS and then normalized by the dome area (9). More complex flow patterns with multiple vortices were observed among
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Figure 4. Box-and-whisker plot showing the distribution of inflow angle in World Federation of Neurosurgical Societies scale grades. The middle horizontal line represents the median and the central box indicates the values from the lower to upper quartile (2575 percentile) whiskers extend from the minimum to the maximum. The means for every grade are connected by a dotted line. Error bars represent one standard deviation.
ruptured aneurysms with the prevalence of more than 60%, and unruptured aneurysms presented simple flow patterns with a single vortex in 75% (23). Low wall shear stress and high oscillatory shear index (measurement of the directional change of WSS during the cardiac
ANEURYSM MORPHOMETRY AND SEVERITY OF SAH
cycle) (6) represent blood flow associated conditions significantly correlated with the risk of rupture (23). Miura et al. (12) reported in 106 patient-specific geometries of the middle cerebral artery aneurysms that WSS may be the most reliable parameter characterizing the rupture status of middle cerebral artery aneurysms. The fluid relative residence time (10), which indicates the time of residence the molecules spent at endothelium, is longer among the ruptured aneurysms (23). The WFNS scale is used commonly to predict the clinical outcome after SAH. The WFNS scale is based on the Glasgow Coma Scale, and although finally accepted by the experts consensus, it has not been formally validated (7). However, the Hunt and Hess scale has a poor interobserver agreement, and the WFNS scale was chosen in this study because of its better predictive value. We also used the FRS proposed by Claassen et al. (4) to assess the correlation between the amount of blood seen on CT and the risk of developing clinical vasospasm and delayed neurological deficits. The FRS does not differentiate the type and severity of intraventricular
hemorrhage and the correlation with the thin or thick SAH (14). There are no studies presenting the purely morphometric data for the SAH grading in RFS and WFNS scales. Therefore, authors could not methodologically refer the data from this study to other reports; however, it is worth mentioning that the multiprofile morphologic variables of the aneurysm complex were intensively explored in the literature. Conclusions from many well-designed studies allow us to repeatedly determine the predictors of the risk of aneurysm rupture. Therefore, in this study, we tested the morphologic factors that might be potential predictors of the aneurysm risk rupture in the prediction of radiological severity of SAH. The results showed that SR and inflow angle determine the extent of bleeding on the FRS. Less significant predictive strength was found for the WFNS scale, where only the angle proved to be of statistical significance. The interpretation of these data might be that any anatomical predictor of the aneurysm complex reflects more the conditions of blood flow and possibly the extent and
Figure 5. Forest plots comparing mean results of size ratio and inflow angle in unruptured and ruptured aneurysms, in demographic factors: sex, history of hypertension, and smoking.
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13. Nikolic I, Tasic G, Bogosavljevic V, Nestorovic B, Jovanovic V, Kojic Z, Djoric I, Djurovic B: Predictable morphometric parameters for rupture of intracranial aneurysms—a series of 142 operated aneurysms. Turk Neurosurg 22:420-426, 2012. 14. Oliveira AMP, Paiva WS, Figueiredo EG de, Oliveira HA, Teixeira MJ: Fisher revised scale for assessment of prognosis in patients with subarachnoid hemorrhage. Arq Neuropsiquiatr 69:910-913, 2011.
Figure 6. Interactive dot diagram presenting the comparison of size ratio (A) and inflow angle (B) in unruptured and ruptured aneurysms. In the graph, the data of the positive and negative groups are displayed as dots on two vertical axes. A horizontal line indicates the cut-off point with the best separation (minimal false and false positive results) between the 2 groups.
severity of bleeding (FRS) than the evaluation of the clinical status (WFNS scale), which does not have to be proportionally dependent on the severity of the bleeding.
CONCLUSION Grading in the FRS positively correlates with the inflow angle and SR of the posterior circulation aneurysms. Thus, these 2 morphometric predictors might be supportive to anticipate the extent and severity of SAH based on CT imaging in this location. The evaluation of neurologic status after SAH via us of the WFNS scale was weakly correlated only with the inflow angle. Morphologic predictors reflect the hemodynamic conditions and flow pattern in the aneurysmal complex and illustrate very different clinical and radiological consequences after the aneurysm rupture. Comparison of the inflow angle and SR between ruptured and unruptured aneurysms in posterior circulation showed, that both of these factors are significantly higher in ruptured aneurysms. The cut of value for inflow angle was 115.9 degrees and for SR 2.31. REFERENCES 1. Baharoglu MI, Schirmer CM, Hoit DA, Gao B-L, Malek AM: Aneurysm inflow-angle as a discriminant for rupture in sidewall cerebral aneurysms: morphometric and computational fluid dynamic analysis. Stroke J Cereb Circ 41:1423-1430, 2010. 2. Cebral JR, Castro MA, Burgess JE, Pergolizzi RS, Sheridan MJ, Putman CM: Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models. AJNR Am J Neuroradiol 26: 2550-2559, 2005.
3. Chiu J-J, Chen C-N, Lee P-L, Yang CT, Chuang HS, Chien S, Usami S: Analysis of the effect of disturbed flow on monocytic adhesion to endothelial cells. J Biomech 36:1883-1895, 2003. 4. Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, Connolly ES, Mayer SA: Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke J Cereb Circ 32:2012-2020, 2001. 5. Dhar S, Tremmel M, Mocco J, Kim M, Yamamoto J, Siddiqui AH, Hopkins LN, Meng H: Morphology parameters for intracranial aneurysm rupture risk assessment. Neurosurgery 63:185-196, 2008. 6. He X, Ku DN: Pulsatile flow in the human left coronary artery bifurcation: average conditions. J Biomech Eng 118:74-82, 1996. 7. Van Heuven AW, Dorhout Mees SM, Algra A, Rinkel GJE: Validation of a prognostic subarachnoid hemorrhage grading scale derived directly from the Glasgow Coma Scale. Stroke J Cereb Circ 39:1347-1348, 2008. 8. International Study of Unruptured Intracranial Aneurysms Investigators: Unruptured intracranial aneurysms—risk of rupture and risks of surgical intervention. N Engl J Med 339:1725-1733, 1998. 9. Jou L-D, Lee DH, Morsi H, Mawad ME: Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 29:1761-1767, 2008. 10. Lee S-W, Antiga L, Steinman DA: Correlations among indicators of disturbed flow at the normal carotid bifurcation. J Biomech Eng 131:061013, 2009. 11. Maslehaty H, Ngando H, Meila D, Brassel F, Scholz M, Petridis AK: Estimated low risk of rupture of small-sized unruptured intracranial aneurysms (UIAs) in relation to intracranial aneurysms in patients with subarachnoid haemorrhage. Acta Neurochir (Wien) 155:1095-1100, 2013. 12. Miura Y, Ishida F, Umeda Y, Tanemura H, Suzuki H, Matsushima S, Shimosaka S, Taki W: Low wall shear stress is independently associated with the rupture status of middle cerebral artery aneurysms. Stroke J Cereb Circ 44:519-521, 2013.
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15. Passerini AG, Polacek DC, Shi C, Francesco NM, Manduchi E, Grant GR, Pritchard WF, Powell S, Chang GY, Stoeckert CJ Jr, Davies PF: Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc Natl Acad Sci U S A 101:2482-2487, 2004. 16. Rahman M, Smietana J, Hauck E, Hoh B, Hopkins N, Siddiqui A, Levy EI, Meng H, Mocco J: Size ratio correlates with intracranial aneurysm rupture status: a prospective study. Stroke J Cereb Circ 41:916-920, 2010. 17. Shojima M, Oshima M, Takagi K, Torii R, Hayakawa M, Katada K, Morita A, Kirino T: Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke J Cereb Circ 35:2500-2505, 2004. 18. Suga M, Yamamoto Y, Sunami N, Yoshida H, Kawasaki S, Akamune A, Inoue T: Natural course of asymptomatic unruptured aneurysms without operation. Analysis of the various radiological findings. Clin Neurol Neurosurg 99 (Suppl 1); 41-41, 1997. 19. Szikora I, Paal G, Ugron A, Nasztanovics F, Marosfoi M, Berentei Z, Kulcsar Z, Lee W, Bojtar I, Nyary I: Impact of aneurysmal geometry on intraaneurysmal flow: a computerized flow simulation study. Neuroradiology 50:411-421, 2008. 20. Tremmel M, Dhar S, Levy EI, Mocco J, Meng H: Influence of intracranial aneurysm-to-parent vessel size ratio on hemodynamics and implication for rupture: results from a virtual experimental study. Neurosurgery 64:622-630, 2009. 21. UCAS Japan Investigators: The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 366:2474-2482, 2012. 22. Ujiie H, Tamano Y, Sasaki K, Hori T: Is the aspect ratio a reliable index for predicting the rupture of a saccular aneurysm? Neurosurgery 48:495-502, 2001. 23. Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, Siddiqui AH, Levy EI, Meng H: Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke J Cereb Circ 42:144-152, 2011. Received 16 January 2014; accepted 3 July 2014; published online 5 July 2014 Citation: World Neurosurg. (2014) 82, 6:1100-1105. http://dx.doi.org/10.1016/j.wneu.2014.07.007 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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Correlation Between the Aneurysm Morphometry and Severity of Subarachnoid Hemorrhage in the Posterior Cerebral Circulation Tomasz Tykocki1 and Bogusław Kostkiewicz2
Key words Aneurysm - Fisher revised scale - Morphometry - SAH - WFNS scale -
Abbreviations and Acronyms FRS: Fisher revised scale IA: intracranial aneurysm SAH: Subarachnoid hemorrhage SR: Size ratio WFNS: World Federation of Neurosurgical Societies WSS: Wall shear stress From the 1Department of Neurosurgery, Institute of Psychiatry and Neurology; and 2Department of Neurosurgery, Central Clinical Hospital Ministry of Interior, Warsaw, Poland To whom correspondence should be addressed: Tomasz Tykocki, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2014) 82, 6:1100-1105. http://dx.doi.org/10.1016/j.wneu.2014.07.007 Supplementary digital content available online. Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
INTRODUCTION The dilemma concerning the optimal treatment of unruptured intracranial aneurysms (IAs) raises many controversies. The predictors of the risk of aneurysm rupture, estimated by presuming that morphometric absolute dimensions of aneurysmal complex are sufficient to definitely postulate the aneurysmal rupture risk, are not necessarily reliable. Conclusions from the International Study of Unruptured Intracranial Aneurysms, a classic study aimed to assess the natural history of unruptured aneurysms, has constituted that the aneurysm size alone correlates independently with the risk of rupture (8). On the contrary, however, other studies have emphasized different findings, raising the greater incidents of subarachnoid hemorrhage (SAH) from small aneurysms (11, 21). To improve the decision making in clinical practice, there
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- OBJECTIVE:
The aim of the study was to examine the correlation between various morphometric factors of the posterior circulation aneurysms and the severity of neurologic status and radiologic extent of subarachnoid hemorrhage.
- METHODS:
A total of 105 patients with ruptured posterior circulation aneurysms (IAs) were retrospectively analyzed in the study. The neurologic status was graded in World Federation of Neurosurgical Societies (WFNS) scale and radiological severity of subarachnoid hemorrhage was assessed in Fisher revised scale (FRS). All patients were qualified for 3-dimensional digital subtraction angiography. The following morphometric measurements were taken: dome size, dome-to-neck ratio, neck size, parent artery size; size ratio (SR), neck-to-parent artery ratio, inflow angle, and diameters of posterior circulation arteries. The univariate and the multiple regression models were used for all independent variables. The significant predictors were compared between ruptured and unruptured IAs.
- RESULTS:
Univariate regression analysis revealed that inflow angle influenced grading in WFNS and that FRS grades were positively correlated with SR, dome-toneck ratio, and inflow angle. The multiple regression model confirmed that inflow angle is an independent factor influencing WFNS scale. FRS is affected by 2 factors: SR and inflow angle. SR was more strongly correlated with FRS (r [ 0.403) than with inflow angle (r [ 284). The comparison of inflow angle and SR in ruptured and unruptured IAs showed a significant difference between means, 125.18 21.86 versus 103.86 17.7 degrees and 2.48 0.46 versus 1.91 0.45, respectively. The cut off points were 115.9 degrees for inflow angle and 2.31 for SR.
- CONCLUSION:
Inflow angle and SR were found to be correlated with grading in FRS, and WFNS scale was correlated with inflow angle.
was an expectation for establishing other unequivocal factors affecting the likelihood of aneurysm rupture. Different morphologic parameters such as size ratio (SR), aspect ratio, inflow angle, undulation index, ellipticity index, and nonsphericity index are believed to contribute significantly in determining the risk of aneurysm rupture (1, 5, 16, 20, 23). The impact of SR in the morphometric-based extrapolation of SAH probability has been proven in several studies (5, 16, 20). SR, defined as the ratio of aneurysm maximal size divided by the average parent vessel diameter based on 2-dimensional angiographic data, is a simple arithmetic formula sufficient to be routinely applied in the daily practice (16).
The impact of the morphologic features of the aneurysm on the clinical course and severity of bleeding after SAH, however, still remains unexplored. In this study, the authors decided to examine the correlation between various morphometric factors of the posterior circulation IAs and commonly applied scales: The Fisher revised scale (FRS) and World Federation of Neurological Surgeons (WFNS) Scale. The study was based on the population of posterior cerebral circulation IAs. METHODS A total of 105 patients (62 women and 43 men) with ruptured posterior circulation aneurysms who were diagnosed and
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treated between 2008 and 2012 at Central Clinical Hospital Ministry of Interior in Warsaw were retrospectively analyzed in the study. The patients’ neurologic status was based on the retrospective analysis of the medical records. All patients were evaluated with the WFNS scale at the time of admission to the Department of Neurosurgery. The severity of SAH was assessed with the FRS based on computed tomography (CT) imaging (Table 1), which had been performed within 24 hours from the onset of SAH symptoms. Grade 0 in FRS was interpreted as no SAH on CT but present in the cerebrospinal fluid test. The following morphometric measurements of the aneurysmal complex (independent variables) were taken: aneurysm dome size, neck size, parent artery size, dome-to-neck ratio, SR (¼ maximum aneurysm dome size, defined as the largest distance between any 2 points on the aneurysm dome surface /vessel diameter), neck-to-parent artery ratio, and inflow angle (Figure 1 and Figure 2 A,B). In the aneurysm involving more than one parent vessel, the mean diameter from all vessels was included. In addition the measurements of posterior circulation arteries were collected: diameters of posterior cerebral right and left arteries at P1 region (precommunicating segment), diameters of right and left vertebral arteries below the level of basilar artery, and the maximum diameter of basilar artery. Demographic and medical history data were obtained from medical records. All demographic factors, including age, sex, smoking history, and hypertension also
ANEURYSM MORPHOMETRY AND SEVERITY OF SAH
source, cross-platform, software system for 3-dimensional computer graphics, the Visualization Toolkit libraries (http:// www.vtk.org/). All angiographies within SAH group were obtained emergently within 48 hours from the admission to the hospital, and before the onset of vasospasm. Size measurements were performed by 2 neurosurgeons in a blinded fashion with respect to the rupture status of the aneurysms. The intraclass correlation coefficient for 2 raters was 0.90.
Figure 1. Schematic drawing presenting the morphometric parameters. d indicates the maximal aneurysm dome size; h indicates the aneurysm dome depth; n the neck size; a is the parent artery diameter; a the inflow angle; F the blood flow direction. The size ratio is determined by d/n.
were tested in stepwise regression models as potentially influencing on the morphometric results.
PATIENT SELECTION All patients were qualified for diagnostic 3-dimensional rotational angiography by a team of doctors consisting of a neurosurgeon, neuroradiologist, and an anesthesiologist. Three-dimensional reconstruction was performed by the use of an open-
Statistical Analysis All the results were statistically analyzed using the computer software MedCalc 12.7; (Ostend, Belgium). Statistical significance was assumed for P < 0.05. The continuous data were expressed as means standard deviation. One-way analysis of variance was used to test for morphometric differences among FRS and WFNS groups. The univariate regression analysis was first used to test all the independent variables as potentially influencing on the grading in WFNS scale and FRS. Then the significant factors were tested in the stepwise multiple regression model. After the predictors had been defined, authors compared them between ruptured and unruptured IAs. The unruptured IAs were retrospectively obtained from the same
Table 1. Fisher Revised Scale Grade 0
No SAH or IVH
Grade I
Minimal/thin SAH, no IVH in either lateral ventricle
Grade II
Minimal/thin SAH, with IVH in both lateral ventricles
Grade III
Dense SAH,* no IVH in either lateral ventricle
Grade IV
Dense SAH,* with IVH in both lateral ventricles
SAH, subarachnoid hemorrhage; IVH, intraventricular hemorrhage. *Completely filling 1 cistern or fissure.
Figure 2. Three-dimensional rotational angiography of basilar tip aneurysm in coronal (A) and sagittal (B) view, presenting the concept of measurement performed in the study. d, maximal aneurysm dome size; h, aneurysm dome depth; n, neck size; a, inflow angle; a, parent artery diameter; p1, diameter of precommunicating segment of the posterior cerebral artery; B, diameter of basilar artery trunk; and V, diameter of vertebral artery.
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database, the same time period, and their morphometric characteristics were defined in the same way as for ruptured IAs. There were 86 unruptured IAs. The interactive dot diagrams were created to compare the morphometric factors between ruptured and unruptured IAs and to calculate the cut off values. RESULTS A population sample of 105 patients with ruptured IAs underwent a retrospective analysis. The grading distribution in WFNS scale was: I (21; 20%); II (23; 21.9%); III (27; 25.7%); IV (18; 17.1%); V (16; 15.2%) (Table 2), and in FRS, grade 0 (7; 6.7%), I (30; 28.6%), II (28; 26.7%), III (23; 21.9%), IV (17; 16.2%) (Table 3). Univariate regression analysis revealed that inflow angle influenced WFNS grade (P ¼ 0.045) and that FRS grades were positively correlated with SR, dome-toneck ratio, and inflow angle. The increasing values of SR and inflow angle predicted the growth of grading in the FRS (Figure 3 A,B). The multiple stepwise regression model confirmed that inflow angle was a sole independent factor influencing WFNS scale; the strength of
ANEURYSM MORPHOMETRY AND SEVERITY OF SAH
this relationship was moderate (correlation coefficient r ¼ 0.37) (Figure 4). A 1-grade increase in WFNS scale was associated with the growth of inflow angle by 5.9 degrees above 109.6 degrees. FRS is affected by a combination of 2 factors: SR and inflow angle. Dome-toneck ratio was eliminated during the analysis. For every 1-grade increase in FRS, SR is expected to be higher by 0.2 above 2 and inflow angle to increase by 4.5 degrees above 110.6 degrees; however, SR was more strongly correlated with FRS (r ¼ 0.403) than with inflow angle (r ¼ 284). The comparison of inflow angle and SR in ruptured and unruptured groups showed a significant difference between mean results, 125.18 21.86 versus 103.86 17.7 degrees (P < 0.05) and 2.48 0.46 versus 1.91 0.45 (P < 0.05) respectively (Figure 5). Detailed results of the analysis of variance comparison of the inflow angle and SR in both scales are presented in Tables S1, S2, and S3. In further comparison of these 2 predictors against the demographic factors (age, sex, smoking and hypertension), we did not find any significant differences (Figure 5). Inflow angle and SR were tested against the rupture criterion by the use of
interactive dot diagram. The values of cutoff points were 115.9 degrees (inflow angle) (Figure 6A) and 2.31 (SR) (Figure 6B). DISCUSSION Controversy and ambiguity regarding the treatment of unruptured aneurysms is still present despite the fact that this issue has been repeatedly taken in the literature and clinical trials. The conclusion of the International Study of Unruptured Intracranial Aneurysms study, in which the investigators highlight the key role of the absolute aneurysm size in predicting of SAH has been criticized (8). Epidemiologic data show that the majority of ruptured aneurysms (about 80%) are less than 10 mm (11, 21). On the basis of these data, it could be definitively assumed that smaller aneurysms rupture more often. However, based on recent reports, SR was introduced and proven to be a significant predictor of IA rupture (5, 16, 20). The concept of this ratio takes into account the relationship between the parent vessel and the aneurysm dome, which is more akin to the anatomy and circulation of the aneurysmal complex.
Table 2. Morphometric Results of the Aneurysms in WFNS Scale WFNS Scale I
Basilar artery, mm
N
Mean
21
4.99
II
III
SD
N
Mean
SD
N
Mean
1.42
23
5.32
1.99
27
4.61
IV SD
N
Mean
1.25
18
4.54
V SD
N
Mean
0.43
16
5.58
SD 0.83
Dome/neck
21
2.75
0.98
23
3.18
0.88
27
2.50
0.54
18
3.36
0.81
16
3.45
1.06
Inflow angle, degrees
21
109.16
21.82
23
113.83
5.39
27
121.30
21.35
18
126.45
33.87
16
129.23
24.45
Dome size, mm
21
10.79
4.46
23
11.36
4.06
27
10.35
2.84
18
10.67
0.31
16
12.18
2.64
Neck size, mm
21
3.16
2.96
23
3.93
1.82
27
4.13
0.23
18
4.34
0.47
16
5.57
1.47
Neck/parent artery
21
1.04
0.39
23
0.80
0.14
27
0.91
0.08
18
0.82
0.09
16
0.95
0.11
P1 right, mm
21
3.13
0.89
23
3.56
0.91
27
2.89
1.54
18
2.47
0.90
16
3.17
0.63
P1 left, mm
21
3.01
1.04
23
3.20
1.14
27
3.01
1.41
18
2.20
1.15
16
3.14
0.52
Parent artery, mm
21
5.11
2.14
23
4.85
1.78
27
4.58
0.65
18
2.93
0.91
16
5.95
2.00
Size ratio
21
2.18
0.80
23
2.51
0.74
27
2.24
0.30
18
2.78
0.97
16
2.91
0.94
Vertebral artery right, mm
21
3.84
1.14
23
4.22
1.38
27
3.83
1.03
18
3.01
0.16
16
4.02
0.43
Vertebral artery left, mm
21
3.94
1.18
23
4.30
1.85
27
3.90
1.27
18
3.89
0.16
16
4.47
0.37
WFNS, World Federation of Neurosurgical Societies; SD, standard deviation; P1, precommunicating segment of the posterior cerebral artery.
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Table 3. Morphometric Results of the Aneurysms Using the Fisher Revised Scale Fisher Revised Scale 0 N
Mean
Basilar artery, mm
7
Dome/neck
I
II SD
N
Mean
4.62
1.62
28
2.70
1.02
28
III
SD
N
Mean
4.29
1.25
30
7
2.74
0.66
30
Inflow angle, degrees
7
108.86
17.70
30
115.8
20.3
28
117.1
26.7
23
Dome size, mm
7
7.89
2.75
30
11.8
4.8
28
12.2
4.3
23
Neck size, mm
7
2.09
1.38
30
3.28
28
1.52
23
3.24
IV
SD
N
Mean
SD
N
Mean
5.22
2.38
23
4.96
1.01
17
5.37
0.74
2.85
0.41
23
3.65
0.16
17
3.52
1.07
123.5
6.3
17
128.7
18.9
11.1
2.8
17
12.3
2.9
0.87
17
4.52
3.05
4.59
SD
1.72
Neck/parent artery
7
0.51
0.09
30
0.93
0.21
28
0.88
0.17
23
0.86
0.07
17
1.11
0.56
P1 right, mm
7
2.33
0.86
30
2.96
0.65
28
3.10
1.27
23
2.71
0.94
17
3.88
0.78
P1 left, mm
7
2.42
0.87
30
2.76
0.69
28
2.78
1.07
23
2.43
1.07
17
3.87
1.17
Parent artery, mm
7
4.06
1.52
30
4.15
2.06
28
5.29
1.21
23
4.49
1.01
17
4.81
2.37
Size ratio
7
1.89
0.46
30
2.34
0.63
28
2.46
0.40
23
2.77
0.29
17
2.94
1.18
Vertebral artery right, mm
7
2.91
0.68
30
3.77
1.19
28
3.93
1.36
23
3.20
0.87
17
4.23
0.62
Vertebral artery left, mm
7
2.83
0.71
30
3.71
1.06
28
4.06
1.95
23
3.31
0.99
17
4.57
1.07
SD, standard deviation; P1, precommunicating segment of the posterior cerebral artery.
In this study, authors decided to investigate the impact of SR on the neurologic status and severity of SAH on CT imaging. It was found that inflow angle affected both the WFNS scale and FRS; however, the correlation coefficient in these cases was less than 0.4 showing a very weak relationship. Other morphometric factors investigated in the study, including diameters of the aneurysm parent arteries in the posterior circulation, did not appear to be significant. Nikolic et al. (13) reported
the average value of the angle in ruptured aneurysms of 139.22 degrees and in unruptured 101.73 the last value was significantly smaller. Dhar et al. (5) found that 81.8% of all unruptured IAs had aneurysm angles less than 112 degrees. According to Suga at al. (18), the greatest risk of rupture occurs at an angle of 160170 degrees and the rarest risk of rupture at an angle of 80130 degrees. Inflow angle is a significant discriminant of rupture status in aneurysms and is
Figure 3. Box-and-whisker plots showing the distribution of inflow angle (A) and size ratio (B) in Fisher revised scale grades. The middle horizontal line represents the median and the central box indicates the values from the lower to upper quartile (2575 percentile) whiskers extend from the minimum to the maximum. The means for every grade are connected by a dotted line. Error bars represent one standard deviation.
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associated with significantly greater peak velocities (increasing 80-fold from 0.004 m/s at 60 to 0.32 m/s at 140 ) and kinetic energy (increased 20-fold from 9.2 109 J at 60 to 1.8 107 J at 140 ) transmission to the dome (1). Greater inflow angle led to a 7.2-fold increase of wall shear stress (WSS) and spatial gradient increasing 5.6-fold. To summarize, the greater inflow angle results in more direct flow into the aneurysm dome and more often a parallel axis of the aneurysm relative to the parent vessel in ruptured aneurysms (2, 17, 19). These altered blood flow parameters within the aneurysm complex may trigger a neurodegenerative cascade originating from epithelial dysfunction and proinflammatory signal pathways are activated (3, 15, 22). The importance of SR ratio is emphasized in many studies. Xiang et al. (23) showed that for a unit increase in the SR of an IA, the odds of IA rupture increased by 2.96. SR was also inversely correlated with low WSS (23), defined as the areas of the aneurysm wall exposed to a WSS below 10% of the mean parent arterial WSS and then normalized by the dome area (9). More complex flow patterns with multiple vortices were observed among
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Figure 4. Box-and-whisker plot showing the distribution of inflow angle in World Federation of Neurosurgical Societies scale grades. The middle horizontal line represents the median and the central box indicates the values from the lower to upper quartile (2575 percentile) whiskers extend from the minimum to the maximum. The means for every grade are connected by a dotted line. Error bars represent one standard deviation.
ruptured aneurysms with the prevalence of more than 60%, and unruptured aneurysms presented simple flow patterns with a single vortex in 75% (23). Low wall shear stress and high oscillatory shear index (measurement of the directional change of WSS during the cardiac
ANEURYSM MORPHOMETRY AND SEVERITY OF SAH
cycle) (6) represent blood flow associated conditions significantly correlated with the risk of rupture (23). Miura et al. (12) reported in 106 patient-specific geometries of the middle cerebral artery aneurysms that WSS may be the most reliable parameter characterizing the rupture status of middle cerebral artery aneurysms. The fluid relative residence time (10), which indicates the time of residence the molecules spent at endothelium, is longer among the ruptured aneurysms (23). The WFNS scale is used commonly to predict the clinical outcome after SAH. The WFNS scale is based on the Glasgow Coma Scale, and although finally accepted by the experts consensus, it has not been formally validated (7). However, the Hunt and Hess scale has a poor interobserver agreement, and the WFNS scale was chosen in this study because of its better predictive value. We also used the FRS proposed by Claassen et al. (4) to assess the correlation between the amount of blood seen on CT and the risk of developing clinical vasospasm and delayed neurological deficits. The FRS does not differentiate the type and severity of intraventricular
hemorrhage and the correlation with the thin or thick SAH (14). There are no studies presenting the purely morphometric data for the SAH grading in RFS and WFNS scales. Therefore, authors could not methodologically refer the data from this study to other reports; however, it is worth mentioning that the multiprofile morphologic variables of the aneurysm complex were intensively explored in the literature. Conclusions from many well-designed studies allow us to repeatedly determine the predictors of the risk of aneurysm rupture. Therefore, in this study, we tested the morphologic factors that might be potential predictors of the aneurysm risk rupture in the prediction of radiological severity of SAH. The results showed that SR and inflow angle determine the extent of bleeding on the FRS. Less significant predictive strength was found for the WFNS scale, where only the angle proved to be of statistical significance. The interpretation of these data might be that any anatomical predictor of the aneurysm complex reflects more the conditions of blood flow and possibly the extent and
Figure 5. Forest plots comparing mean results of size ratio and inflow angle in unruptured and ruptured aneurysms, in demographic factors: sex, history of hypertension, and smoking.
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13. Nikolic I, Tasic G, Bogosavljevic V, Nestorovic B, Jovanovic V, Kojic Z, Djoric I, Djurovic B: Predictable morphometric parameters for rupture of intracranial aneurysms—a series of 142 operated aneurysms. Turk Neurosurg 22:420-426, 2012. 14. Oliveira AMP, Paiva WS, Figueiredo EG de, Oliveira HA, Teixeira MJ: Fisher revised scale for assessment of prognosis in patients with subarachnoid hemorrhage. Arq Neuropsiquiatr 69:910-913, 2011.
Figure 6. Interactive dot diagram presenting the comparison of size ratio (A) and inflow angle (B) in unruptured and ruptured aneurysms. In the graph, the data of the positive and negative groups are displayed as dots on two vertical axes. A horizontal line indicates the cut-off point with the best separation (minimal false and false positive results) between the 2 groups.
severity of bleeding (FRS) than the evaluation of the clinical status (WFNS scale), which does not have to be proportionally dependent on the severity of the bleeding.
CONCLUSION Grading in the FRS positively correlates with the inflow angle and SR of the posterior circulation aneurysms. Thus, these 2 morphometric predictors might be supportive to anticipate the extent and severity of SAH based on CT imaging in this location. The evaluation of neurologic status after SAH via us of the WFNS scale was weakly correlated only with the inflow angle. Morphologic predictors reflect the hemodynamic conditions and flow pattern in the aneurysmal complex and illustrate very different clinical and radiological consequences after the aneurysm rupture. Comparison of the inflow angle and SR between ruptured and unruptured aneurysms in posterior circulation showed, that both of these factors are significantly higher in ruptured aneurysms. The cut of value for inflow angle was 115.9 degrees and for SR 2.31. REFERENCES 1. Baharoglu MI, Schirmer CM, Hoit DA, Gao B-L, Malek AM: Aneurysm inflow-angle as a discriminant for rupture in sidewall cerebral aneurysms: morphometric and computational fluid dynamic analysis. Stroke J Cereb Circ 41:1423-1430, 2010. 2. Cebral JR, Castro MA, Burgess JE, Pergolizzi RS, Sheridan MJ, Putman CM: Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models. AJNR Am J Neuroradiol 26: 2550-2559, 2005.
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15. Passerini AG, Polacek DC, Shi C, Francesco NM, Manduchi E, Grant GR, Pritchard WF, Powell S, Chang GY, Stoeckert CJ Jr, Davies PF: Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc Natl Acad Sci U S A 101:2482-2487, 2004. 16. Rahman M, Smietana J, Hauck E, Hoh B, Hopkins N, Siddiqui A, Levy EI, Meng H, Mocco J: Size ratio correlates with intracranial aneurysm rupture status: a prospective study. Stroke J Cereb Circ 41:916-920, 2010. 17. Shojima M, Oshima M, Takagi K, Torii R, Hayakawa M, Katada K, Morita A, Kirino T: Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke J Cereb Circ 35:2500-2505, 2004. 18. Suga M, Yamamoto Y, Sunami N, Yoshida H, Kawasaki S, Akamune A, Inoue T: Natural course of asymptomatic unruptured aneurysms without operation. Analysis of the various radiological findings. Clin Neurol Neurosurg 99 (Suppl 1); 41-41, 1997. 19. Szikora I, Paal G, Ugron A, Nasztanovics F, Marosfoi M, Berentei Z, Kulcsar Z, Lee W, Bojtar I, Nyary I: Impact of aneurysmal geometry on intraaneurysmal flow: a computerized flow simulation study. Neuroradiology 50:411-421, 2008. 20. Tremmel M, Dhar S, Levy EI, Mocco J, Meng H: Influence of intracranial aneurysm-to-parent vessel size ratio on hemodynamics and implication for rupture: results from a virtual experimental study. Neurosurgery 64:622-630, 2009. 21. UCAS Japan Investigators: The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med 366:2474-2482, 2012. 22. Ujiie H, Tamano Y, Sasaki K, Hori T: Is the aspect ratio a reliable index for predicting the rupture of a saccular aneurysm? Neurosurgery 48:495-502, 2001. 23. Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, Siddiqui AH, Levy EI, Meng H: Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke J Cereb Circ 42:144-152, 2011. Received 16 January 2014; accepted 3 July 2014; published online 5 July 2014 Citation: World Neurosurg. (2014) 82, 6:1100-1105. http://dx.doi.org/10.1016/j.wneu.2014.07.007 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2014 Elsevier Inc. All rights reserved.
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TOMASZ TYKOCKI AND BOGUSŁAW KOSTKIEWICZ