Distinctive flow pattern of wall shear stress and oscillatory shear index: similarity and dissimilarity in ruptured and unruptured cerebral aneurysm blebs

Clinical article

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Object

The difference in the hemodynamics of wall shear stress (WSS) and oscillatory shear index (OSI) between ruptured and unruptured aneurysms is not well understood. The authors investigated the hemodynamic similarities and dissimilarities in ruptured and thin-walled unruptured aneurysm blebs.

Methods

Magnetic resonance imaging–based fluid dynamics analysis was used to calculate WSS and OSI, and hemodynamic and intraoperative findings were compared. The authors also compared ruptured and unruptured thin-walled blebs for the magnitude of WSS and OSI.

Results

Intraoperatively, 13 ruptured and 139 thin-walled unruptured aneurysm blebs were identified. Twelve of the ruptured (92.3%) and 124 of the unruptured blebs (89.2%) manifested low WSS and high OSI. The degree of WSS was significantly lower in ruptured (0.49 ± 0.12 Pa) than in unruptured (0.64 ± 0.15 Pa; p < 0.01) blebs.

Conclusions

Ruptured and unruptured blebs shared a distinctive pattern of low WSS and high OSI. The degree of WSS at the rupture site was significantly lower than in the unruptured thin-walled blebs.

Abbreviations used in this paper:ACA = anterior cerebral artery; ACoA = anterior communicating artery; CFD = computational fluid dynamics; ICA = internal carotid artery; MCA = middle cerebral artery; MRA = MR angiography; OSI = oscillatory shear index; SAH = subarachnoid hemorrhage; WSS = wall shear stress.

Abstract

Object

The difference in the hemodynamics of wall shear stress (WSS) and oscillatory shear index (OSI) between ruptured and unruptured aneurysms is not well understood. The authors investigated the hemodynamic similarities and dissimilarities in ruptured and thin-walled unruptured aneurysm blebs.

Methods

Magnetic resonance imaging–based fluid dynamics analysis was used to calculate WSS and OSI, and hemodynamic and intraoperative findings were compared. The authors also compared ruptured and unruptured thin-walled blebs for the magnitude of WSS and OSI.

Results

Intraoperatively, 13 ruptured and 139 thin-walled unruptured aneurysm blebs were identified. Twelve of the ruptured (92.3%) and 124 of the unruptured blebs (89.2%) manifested low WSS and high OSI. The degree of WSS was significantly lower in ruptured (0.49 ± 0.12 Pa) than in unruptured (0.64 ± 0.15 Pa; p < 0.01) blebs.

Conclusions

Ruptured and unruptured blebs shared a distinctive pattern of low WSS and high OSI. The degree of WSS at the rupture site was significantly lower than in the unruptured thin-walled blebs.

The hemodynamics of intracranial aneurysms, including WSS and OSI, are thought to play an important role in the initiation, growth, and rupture of these lesions.5,7,14,20,24,25,28,32,39,40,42,43 Wall shear stress is a tangential frictional force induced by viscous blood moving across the vascular wall surface. In vivo, blood under pulsation flows in the vasculature, and knowledge of the vascular 3D geometry and velocity fields is necessary to understand the spatial distribution of WSS and flow structure. Shearing forces oscillate with the cardiac cycle, and the OSI indicates the extent of such fluctuations.14

Although WSS is known to regulate endothelial cell function and is thought to play a role in the progression of atherosclerosis,8,9,28 its contribution to aneurysm rupture is not well understood. Given that the highest degree of shear stress has been recorded at the aneurysm bleb, an association between high WSS and aneurysm rupture has been proposed.12,27,44 Alternatively, Shojima et al.,39 who found that the degree of WSS was significantly lower in the dome and bleb of ruptured than in unruptured aneurysms, attributed rupture to low WSS. Others16–18,47 have also identified low WSS and high OSI as important factors contributing to aneurysm rupture.

Authors of clinical studies have suggested blebs as the areas at increased risk of rupture,3,41,45 and Hayakawa et al.13 reported that aneurysm blebs are thin-walled and subject to a stronger pulsatile force than other parts of the aneurysm. Cebral et al.5 described an association between high WSS and the development of new blebs; however, little is known about factors that result in the rupture of preexisting blebs.

In the present study we used MRI in a 4D fluid dynamics analysis of ruptured and unruptured aneurysms to clarify the hemodynamics near aneurysm blebs. We showed a distinctive flow pattern around the blebs and report our comparative findings on ruptured and unruptured thin-walled blebs.

Methods

Study Population

Our cohort included 125 patients with 150 saccular aneurysms (13 ruptured, 137 unruptured) treated at our hospital between November 2008 and December 2010. Patients with SAH due to aneurysm rupture underwent surgery within 48 hours of their hemorrhage. Some of these cases have been reported elsewhere.22,23 Informed consent was obtained from the patients or their legal representatives at the time of admission and before contrast-enhanced CT studies. We excluded patients with cerebral artery dissection, aneurysms smaller than 3 mm, and aneurysms on the anterior wall of the internal carotid artery, because of limited spatial resolution on MR images and because the mechanism of cerebral artery dissection might be different from saccular aneurysm formation. Patients with SAH who had a poor clinical grade (Hunt and Kosnik Grade V) were also excluded because of poor vital signs.

Data Collection and Analysis

On admission, all patients underwent neurological examination by neurosurgeons; head CT, MRI, MRA, and digital subtraction angiography studies were subsequently performed. Magnetic resonance imaging–based fluid dynamics analysis was conducted before surgery. Radiologists blinded to the status of the aneurysms (ruptured or unruptured) evaluated results of the fluid dynamics studies. They identified the blebs as regions of interest and quantified the WSS and OSI values. The bleb surface was defined as the area outside the ostium on a plane between the bleb and the aneurysm dome.13,19,35 Surgery was performed and 3 neurosurgeons reviewed video recordings of the operations. They were blinded to results of the fluid dynamics analysis to ensure objective evaluation of the thin-walled blebs and rupture sites. We entered patient age and sex, aneurysm site, aneurysm geometric information, WSS, OSI, Hunt and Kosnik grade, treatment, and intraoperative findings (including rupture site and location of thin-walled blebs) on a computer and analyzed the data retrospectively.

Fluid Dynamics Analysis

We subjected the parent artery, aneurysm, and arterial branches distal to the aneurysm to preoperative MRI-based 4D fluid dynamics analysis. Magnetic resonance imaging and flow dynamics data were obtained using the 2D fastcard phase-contrast method on a 1.5-T MRI unit (Signa, General Electric Medical Systems) combined with electrocardiography gating. This method yields 3D voxel data.2,6,17,18,29,31 Imaging parameters were as follows: repetition time, 17.5 msec; echo time, 7.7 msec; FOV, 180 mm; matrix, 256 × 256; velocity encoding, 30–100 cm/second; scanning time, 15–20 minutes; and gating with electrocardiography, 20 phases. Details have been described elsewhere.17,18

For 3D time-of-flight MRA, imaging parameters were as follows: repetition time, 25 msec; echo time, 6.9 msec; FOV, 180 mm; and scanning time, 2 minutes. Acquired data were used to determine the boundary of the inner wall of cerebral aneurysms. The region of interest around the aneurysm was selected based on fluid dynamics and MRA findings. The vascular structures were segmented based on 3D MRA data sets using the region growing method,38 and vascular shapes were created with the marching cubes method.26

Three-dimensional flow information was interpolated at a spatial resolution of 0.5 × 0.5 × 0.5 mm using the 3D data sets obtained on MRI-based fluid dynamics analysis. We set several planes traversing the aneurysm and the parent arteries and generated a 3D streamline using the Runge-Kutta method.37 Data that included velocity components for x, y, and z directions and time yielded 4D flow information.16

Wall shear stress and OSI were calculated on a personal computer. Wall shear stress is defined as the product of fluid viscosity and shearing velocity of the neighboring vascular wall.17,18,28 For our calculations we used 0.0038 Pa × second as the viscosity of blood.17,18 The OSI is the nondimensional parameter; it ranged from 0 to 0.5 and indicated the magnitude of WSS fluctuations during a cardiac cycle. It is defined as follows:

article image
where WSSi represents the instantaneous WSS vectors, and τ the cycle duration.14 Details can be found elsewhere.17,18

For segmentation, creation of vascular models, and calculations of WSS and OSI, we used commercially available software (Flova, R'Tech Co. Ltd.).17,18

Wall shear stress ranging between 1.0 and 7.0 Pa in the arterial vascular network is considered normal in human arteries,28,32,49 and the physiological level of OSI to maintain endothelial function has been reported to be under 0.20.10,11 Consequently, we defined low WSS and high OSI values as < 1.0 Pa and > 0.20, respectively.

Intraoperative Findings

All 13 ruptured aneurysms were surgically treated within 48 hours of SAH onset. The aneurysm neck was clipped, and the aneurysms were totally exposed to ensure that clipping was complete. The site covered by a clot or fibrin net was defined as the rupture point. In some cases we had histological confirmation of the rupture site. We also clipped the neck of unruptured aneurysms. Intraoperative evidence of blood flow through the aneurysm wall indicated a thin-walled region.

Statistical Analysis

The quantitative values of the time-averaged WSS and OSI values for each bleb were recorded and evaluated. Differences were analyzed with the Student t-test, and differences of p ≤ 0.05 were considered significant.

Results

Clinical Characteristics

Of the 150 saccular aneurysms, 13 were ruptured and 137 were unruptured. Several unruptured aneurysms had multiple blebs, and thus 139 blebs were analyzed. As shown in Table 1, the aneurysms tended to be located in the anterior circulation (MCA, ICA, ACA, and ACoA). They ranged in size from 3.1 to 11.2 mm (mean 5.3 mm).

TABLE 1:

Summary of clinical characteristics in 125 patients with 150 aneurysms*

ParameterRuptured CasesUnruptured Cases
no. of patients13112
age in yrs
 mean63.266.1
 range44–7734–81
M/F1:1235:77
no. of aneurysms13137
aneurysm site
 MCA666
 ICA142
 ACoA417
 ACA09
 VA/BA23
size (diameter) in mm
 mean5.94.7
 range3.9–11.23.1–8.8

* BA = basilar artery; VA = vertebral artery.

Distinctive Flow Pattern at Ruptured Blebs

We performed MRI-based fluid dynamics analysis of ruptured aneurysms at the time of admission, and hemodynamic data were analyzed preoperatively. Patients underwent open surgery for aneurysm clipping, and the actual rupture point was identified. Of the 13 ruptured blebs, 12 (92.3%) manifested low WSS and high OSI values preoperatively. In the remaining bleb, WSS was low (0.54 Pa) and OSI was not high (0.18; Table 2).

TABLE 2:

Summary of flow characteristics at ruptured blebs and unruptured thin-walled blebs

Flow PatternNo./Total (% of total)
Ruptured BlebsThin-Walled Blebs
low WSS/high OSI12/13 (92.3)124/139 (89.2)
low WSS/non-high OSI1/13 (7.7)10/139 (7.2)
non-low WSS/high OSI4/139 (2.9)
non-low WSS/non-high OSI1/139 (0.7)

Distinctive Flow Pattern of Unruptured Thin-Walled Blebs

Unruptured aneurysms were subjected to MRI-based fluid dynamics analysis, and hemodynamic data were analyzed preoperatively. At open surgery, 139 blebs were thin-walled, and 124 (89.2%) had low WSS and high OSI preoperatively. Low WSS and non-high OSI were demonstrated in 10 (7.2%) of the 139 blebs, and non-low WSS and high OSI were demonstrated in 4 (2.9%). Only 1 bleb (0.7%) was found to have non-low WSS and non-high OSI (Table 2).

Values for WSS and OSI at Ruptured and Unruptured Thin-Walled Blebs

We calculated the mean ± standard deviation of the WSS and OSI values (Table 3). The time-averaged WSS on thin-walled blebs of unruptured aneurysms was low (0.64 ± 0.15 Pa); at the point of aneurysm rupture it was significantly lower (0.49 ± 0.12 Pa; p < 0.01). On the other hand, the OSI was not significantly different for ruptured and unruptured thin-walled blebs (0.38 ± 0.070 vs 0.34 ± 0.17, respectively).

TABLE 3:

Comparison of WSS and OSI at the ruptured bleb wall and in thin-walled unruptured blebs*

ParameterRuptured BlebsThin-Walled Blebs
time-averaged WSS (Pa)0.49 ± 0.120.64 ± 0.15
OSI0.38 ± 0.0700.34 ± 0.17

* Values are expressed as the means ± standard deviation.

† p < 0.01, compared with time-averaged WSS on thin-walled unruptured blebs.

Illustrative Cases

Case 1: Ruptured Aneurysm

This 74-year-old woman experienced sudden-onset headache and loss of consciousness. A head CT scan demonstrated SAH. At admission, her Glasgow Coma Scale score was 11 (E3V4M4). Digital subtraction angiography demonstrated an irregular aneurysm on the ACoA with a bleb at the apex (Fig. 1A). The left A1 portion was hypoplastic or aplastic; it was not visualized on a left internal carotid arteriogram. Magnetic resonance imaging–based fluid dynamics analysis revealed that WSS was lower on the bleb (0.41 Pa) than in the surrounding area (Fig. 1B). The OSI on the bleb was 0.31, higher than in the surrounding area. The aneurysm neck was clipped on the day of admission. Intraoperatively, the bleb was covered with a clot and fibrin net (Fig. 1C). Histological evidence of degenerative changes identified the bleb as the rupture point (Fig. 1D).

Fig. 1.
Fig. 1.

Case 1. Images obtained in a 74-year-old woman with a ruptured ACoA aneurysm. Digital subtraction angiogram (A) revealing an irregular aneurysm measuring 11.2 mm in diameter and a bleb at its apex (arrow). Magnetic resonance imaging–based fluid dynamics analysis (B) showing that at 0.41 Pa, WSS was lower than in the surrounding area (left; arrow). The OSI on the bleb was 0.31, higher than in the surrounding area (right; arrow). The aneurysm neck was clipped on the day of admission. Intraoperative photograph (C) showing that the bleb was covered with a clot and fibrin net (arrow). Histological studies confirmed the bleb as the site of rupture. Photomicrographs (D) revealing an absent intimal layer and internal elastic lamina along with degenerative changes around the rupture point. EVG = elastica van Gieson.

Case 2: Unruptured Aneurysm

This 70-year-old woman was admitted for preoperative study. Digital subtraction angiography demonstrated an irregular 10-mm unruptured aneurysm with 3 blebs on the right MCA bifurcation (Fig. 2A). Magnetic resonance imaging–based fluid dynamics analysis showed that WSS at all 3 blebs (Fig. 2B) was below normal values (0.91, 0.97, and 0.72 Pa). The OSI of 1 bleb was high (0.37), and for the other 2 blebs was 0.02 and 0.08. At surgery the aneurysm was totally exposed, and the bleb manifesting low WSS and high OSI was confirmed as thin-walled (Fig. 2C).

Fig. 2.
Fig. 2.

Case 2. Images obtained in a 70-year-old woman with an unruptured aneurysm. Digital subtraction angiogram (A) revealing an irregular 10-mm aneurysm harboring multiple blebs on the right MCA bifurcation (arrows and arrowhead each indicate a bleb). Magnetic resonance imaging–based fluid dynamics analysis (B) showing that all 3 blebs (left; solid arrow, arrowhead, and open arrow) were exposed to low WSS (0.72, 0.91, and 0.97 Pa, respectively). The OSI mapping indicated a high OSI (0.37) for 1 of the blebs (right; open arrow); the other 2 blebs (right; solid arrow and arrowhead) had a low OSI (0.02 and 0.08, respectively). Intraoperative photograph (C) showing a totally exposed aneurysm. The bleb with low WSS and high OSI was confirmed to be thin-walled (open arrow; solid arrow and arrowhead each indicate a bleb). The aneurysm neck was clipped, and the patient was discharged 8 days after surgery without neurological deficits. M1 = M1 segment; M2 = M2 segment.

Case 3: Unruptured Aneurysm With Subsequent Rupture

This 48-year-old woman was admitted for preoperative study. Digital subtraction angiography demonstrated a 6-mm unruptured aneurysm on the right MCA bifurcation (Fig. 3A). The aneurysm had a bleb at the apex and another at the neck. Magnetic resonance imaging–based fluid dynamics analysis showed that WSS was low at both blebs (0.67 and 0.48 Pa; Fig. 3B). The OSI was low for the neck bleb (0.091) and high for the bleb at the apex (0.29). Surgery was scheduled for the following month; however, on the day of hospital discharge, the patient reported a sudden-onset headache. A head CT scan showed SAH, and she underwent emergency surgery. Intraoperative findings showed the apical bleb as the rupture site (Fig. 3C); the bleb at the neck was intact.

Fig. 3.
Fig. 3.

Case 3. Images obtained in a 48-year-old woman with an unruptured aneurysm. Digital subtraction angiogram (A) revealing a 6-mm aneurysm on the right MCA bifurcation. Blebs were detected at the aneurysm apex (open arrow) and around the neck (solid arrow). Magnetic resonance imaging–based fluid dynamics analysis (B) showed that WSS was low at both blebs (left; 0.67 Pa [solid arrow] and 0.48 Pa [open arrow]). The OSI was low at the bleb around the aneurysm neck (right; 0.091 [solid arrow]) and high at the bleb at the apex (right; 0.29 [open arrow]). Surgery was scheduled for the following month; however, on the day of hospital discharge, the patient reported a sudden-onset headache. Computed tomography revealed SAH, and she underwent emergency surgery. Intraoperative photographs (C) showing rupture of the bleb at the aneurysm apex (left; open arrow) and an intact bleb around the neck (right; solid arrow). She underwent aneurysm neck clipping and was discharged 18 days after surgery without neurological deficits.

Discussion

We found that low WSS and high OSI are characteristics of ruptured blebs and thin-walled blebs of unruptured aneurysms and that WSS at the rupture site is much lower than at the thin-walled bleb of unruptured aneurysms. Xiang et al.47 measured hemodynamic parameters including the wall pressure of both ruptured and unruptured aneurysms. Their multivariate logistic regression analysis showed that WSS and OSI are the only statistically significant variables between ruptured and unruptured aneurysms. They quantified the WSS and OSI of the entire aneurysm wall but did not study specific areas of the aneurysms. In contrast, we focused on the WSS and OSI of the bleb, which is thought to be the area at highest risk for rupture.3,41,45

We documented the flow characteristics, that is, low WSS and high OSI, of the aneurysm rupture site and of unruptured thin-walled blebs. While low WSS and high OSI are equivocal indicators of a high bleb rupture risk and although they cannot be considered causative factors in bleb rupture, Case 3 in our study is particularly interesting. The patient in that case was found to harbor blebs at the aneurysm neck and apex, and fluid dynamics analysis showed low WSS (0.48 Pa) and high OSI (0.29) at the apical bleb. One day after undergoing these studies she suffered an aneurysm rupture and underwent emergency surgery. Intraoperative findings confirmed that the rupture site was the bleb at the tip of the aneurysm. While other such cases must be documented and analyzed, we suggest that our case illustrates the natural history of a cerebral aneurysm.

Although MRI-based fluid dynamics analysis is less invasive and less time-consuming2,16–18,29,46,48 than CFD studies and facilitates the acquisition of in vivo hemodynamics data,2,29,38,48 concerns have been raised with regard to its accuracy. The spatial and temporal resolutions of MRI-based fluid dynamics analysis are lower than those of CFD;17,18 however, comparative studies have revealed a good correlation between the results of CFD and MRI-based fluid dynamics analysis using 2D or 3D cine phase-contrast imaging.1,4,15,21,29,30,34,36,50 According to Isoda et al.,17 there is good correlation between fluid dynamics data for intracranial aneurysms obtained via MRI-based fluid dynamics analysis and that obtained via CFD. The use of 3-T scanners with higher magnetic fields and a high signal-to-noise ratio may yield more precise results.27

Our study has some limitations. Although we demonstrated that ruptured and unruptured blebs share a distinctive pattern of low WSS and high OSI, we cannot conclude that these factors cause aneurysm rupture. Moreover, we cannot exclude the possibility that rupture affected intraaneurysmal blood flow. As we have no data on the fluid dynamics before and after aneurysm rupture in individual patients, we do not know whether and/or how it contributed to rupture. In this study, we defined regions through which blood flow could be observed as thin-walled blebs.33 Three neurosurgeons blinded to the results of the fluid dynamics analysis reviewed intraoperative video recordings to avoid bias and to minimize subjective errors. Despite these efforts, our intraoperative assessment of the wall thickness of unruptured aneurysms may be incorrect.

Conclusions

The present study demonstrated both similarities and dissimilarities with respect to the fluid dynamics of ruptured and unruptured thin-walled blebs. Low WSS and high OSI are components of their common distinctive flow pattern. Note, however, that the WSS magnitude at ruptured blebs was significantly lower than at the unruptured thin-walled blebs. Although the clinical implications of our findings deserve consideration, our study population was relatively small, and our assessment method is not ideal for obtaining accurate WSS and OSI values. Nevertheless, 4D fluid dynamics analysis may be a valuable means of gaining a better understanding of the natural history of cerebral aneurysms. Prospective data collections and prolonged follow-up of patients with unruptured and ruptured aneurysm blebs are necessary to identify the role of WSS and OSI in the initiation, growth, and rupture of intracranial aneurysms.

Disclosure

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Kawaguchi. Acquisition of data: Kawaguchi, Sato, Maeda, Yokoyama, Midorikawa. Analysis and interpretation of data: Sato, Maeda, Yokoyama. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Kawaguchi. Statistical analysis: Kanamori, Omodaka. Administrative/technical/material support: Sato, Maeda. Study supervision: Nishimura, Kanamori, Sasaki, Nishijima.

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    Tateshima SMurayama YVillablanca JPMorino TNomura KTanishita K: In vitro measurement of fluid-induced wall shear stress in unruptured cerebral aneurysms harboring blebs. Stroke 34:1871922003

  • 44

    Tateshima SMurayama YVillablanca JPMorino TTakahashi HYamauchi T: Intraaneurysmal flow dynamics study featuring an acrylic aneurysm model manufactured using a computerized tomography angiogram as a mold. J Neurosurg 95:102010272001

  • 45

    Tsukahara TMurakami NSakurai YYonekura MTakahashi TInoue T: Treatment of unruptured cerebral aneurysms; a multi-center study at Japanese national hospitals. Acta Neurochir Suppl 94:77852005

  • 46

    Wetzel SMeckel SFrydrychowicz ABonati LRadue EWScheffler K: In vivo assessment and visualization of intracranial arterial hemodynamics with flow-sensitized 4D MR imaging at 3T. AJNR Am J Neuroradiol 28:4334382007

  • 47

    Xiang JNatarajan SKTremmel MMa DMocco JHopkins LN: Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 42:1441522011

  • 48

    Yamashita SIsoda HHirano MTakeda HInagawa STakehara Y: Visualization of hemodynamics in intracranial arteries using time-resolved three-dimensional phase-contrast MRI. J Magn Reson Imaging 25:4734782007

  • 49

    Zeng ZKallmes DFDurka MJDing YLewis DKadirvel R: Sensitivity of CFD based hemodynamic results in rabbit aneurysm models to idealizations in surrounding vasculature. J Biomech Eng 132:0910092010

  • 50

    Zhao SZPapathanasopoulou PLong QMarshall IXu XY: Comparative study of magnetic resonance imaging and image-based computational fluid dynamics for quantification of pulsatile flow in a carotid bifurcation phantom. Ann Biomed Eng 31:9629712003

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Article Information

Address correspondence to: Tomohiro Kawaguchi, M.D., Ph.D., Department of Neurosurgery, Aomori Prefectural Central Hospital, 2-1-1 Higashitsukurimichi, Aomori 030-8553, Japan. email: kawaguchi@nsg.med.tohoku.ac.jp.

Please include this information when citing this paper: published online August 24, 2012; DOI: 10.3171/2012.7.JNS111991.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Case 1. Images obtained in a 74-year-old woman with a ruptured ACoA aneurysm. Digital subtraction angiogram (A) revealing an irregular aneurysm measuring 11.2 mm in diameter and a bleb at its apex (arrow). Magnetic resonance imaging–based fluid dynamics analysis (B) showing that at 0.41 Pa, WSS was lower than in the surrounding area (left; arrow). The OSI on the bleb was 0.31, higher than in the surrounding area (right; arrow). The aneurysm neck was clipped on the day of admission. Intraoperative photograph (C) showing that the bleb was covered with a clot and fibrin net (arrow). Histological studies confirmed the bleb as the site of rupture. Photomicrographs (D) revealing an absent intimal layer and internal elastic lamina along with degenerative changes around the rupture point. EVG = elastica van Gieson.

  • View in gallery

    Case 2. Images obtained in a 70-year-old woman with an unruptured aneurysm. Digital subtraction angiogram (A) revealing an irregular 10-mm aneurysm harboring multiple blebs on the right MCA bifurcation (arrows and arrowhead each indicate a bleb). Magnetic resonance imaging–based fluid dynamics analysis (B) showing that all 3 blebs (left; solid arrow, arrowhead, and open arrow) were exposed to low WSS (0.72, 0.91, and 0.97 Pa, respectively). The OSI mapping indicated a high OSI (0.37) for 1 of the blebs (right; open arrow); the other 2 blebs (right; solid arrow and arrowhead) had a low OSI (0.02 and 0.08, respectively). Intraoperative photograph (C) showing a totally exposed aneurysm. The bleb with low WSS and high OSI was confirmed to be thin-walled (open arrow; solid arrow and arrowhead each indicate a bleb). The aneurysm neck was clipped, and the patient was discharged 8 days after surgery without neurological deficits. M1 = M1 segment; M2 = M2 segment.

  • View in gallery

    Case 3. Images obtained in a 48-year-old woman with an unruptured aneurysm. Digital subtraction angiogram (A) revealing a 6-mm aneurysm on the right MCA bifurcation. Blebs were detected at the aneurysm apex (open arrow) and around the neck (solid arrow). Magnetic resonance imaging–based fluid dynamics analysis (B) showed that WSS was low at both blebs (left; 0.67 Pa [solid arrow] and 0.48 Pa [open arrow]). The OSI was low at the bleb around the aneurysm neck (right; 0.091 [solid arrow]) and high at the bleb at the apex (right; 0.29 [open arrow]). Surgery was scheduled for the following month; however, on the day of hospital discharge, the patient reported a sudden-onset headache. Computed tomography revealed SAH, and she underwent emergency surgery. Intraoperative photographs (C) showing rupture of the bleb at the aneurysm apex (left; open arrow) and an intact bleb around the neck (right; solid arrow). She underwent aneurysm neck clipping and was discharged 18 days after surgery without neurological deficits.

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Zhao SZPapathanasopoulou PLong QMarshall IXu XY: Comparative study of magnetic resonance imaging and image-based computational fluid dynamics for quantification of pulsatile flow in a carotid bifurcation phantom. Ann Biomed Eng 31:9629712003

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