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Quantitative Hemodynamic Analysis Of Brain Aneurysm At Different Locations

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1. ORIGINAL Quantitative Hemodynamic Analysis of Brain RESEARCH Aneurysms at Different Locations A. Chien BACKGROUND AND PURPOSE: Studies have shown that the occurrence…
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  • 1. ORIGINAL Quantitative Hemodynamic Analysis of Brain RESEARCH Aneurysms at Different Locations A. Chien BACKGROUND AND PURPOSE: Studies have shown that the occurrence of brain aneurysms and risk of M.A. Castro rupture vary between locations. However, the reason that aneurysms at different branches of the cerebral arteries have different clinical presentations is not clear. Because research has indicated that S. Tateshima aneurysm hemodynamics may be one of the important factors related to aneurysm growth and J. Sayre rupture, our aim was to analyze and compare the flow parameters in aneurysms at different locations. J. Cebral MATERIALS AND METHODS: A total of 24 patient-specific aneurysm models were constructed by using F. Vinuela ˜ 3D rotational angiographic data for the hemodynamic simulation. Previously developed computational fluid dynamics software was applied to each aneurysm to simulate the blood-flow properties. Hemo- dynamic data at peak pulsatile flow were recorded, and wall shear stress (WSS) and flow rate in the aneurysms and parent arteries were quantitatively compared. To validate our method, a comparison with a previously reported technique was also performed. RESULTS: WSS and flow rate in the aneurysms at the peak of the cardiac cycle were found to differ in magnitude between different locations. Multiple comparisons among locations showed higher WSS and flow rate in middle cerebral artery aneurysms and lower WSS and flow rate in basilar artery and anterior communicating artery aneurysms. CONCLUSIONS: We observed changes in hemodynamic values that may be related to aneurysm location. Further study of aneurysm locations with a large number of cases is needed to test this hypothesis. B rain aneurysm rupture is one cause of subarachnoid hem- orrhage and results in substantial rates of morbidity and mortality. Autopsy studies have reported that intracranial an- ing, realistic aneurysm geometry and vascular structure can be incorporated into simulations to perform patient-specific he- modynamic analysis. This type of image-based hemodynamic INTERVENTIONAL ORIGINAL RESEARCH eurysms are common lesions and certain locations tend to research has shown that ruptured aneurysms tend to have a have a higher rate of incidence.1 Recent international studies more complicated flow pattern.14,17 Using a longitudinal data have reported that some aneurysm locations have a higher risk base, a recent hemodynamic study of aneurysm growth also of rupture than others.2-4 Because little is known about the reported that aneurysms are more likely to grow in regions of cause of brain aneurysms or the process by which they grow low wall shear stress (WSS).18 Although studies have suggested and rupture, studies of how anatomic location may affect that aneurysms at different locations tend to differ geometri- brain aneurysms can help further understand this disease.5 cally and clinically,1-4 to our knowledge, whether aneurysms at Vascular geometry, branching angles, and surrounding an- different locations have different hemodynamic properties has atomic structures, the features used to identify and specify an not yet been reported. The aim of this study was to examine aneurysm, have previously been studied to find their relation- the hemodynamic parameters in aneurysms at different ships with the natural history of aneurysms.6-8 Analyzing dif- locations. ferences in parent artery geometry revealed that aneurysms with a large caliber of the proximal artery tended to rupture at Materials and Methods a larger size.6 Bifurcations beyond the circle of Willis approx- imated optimality principles, unlike those within the circle of Data Collection and Imaging Technique Willis.7 Moreover, the perianeurysmal environment has been Twenty-four aneurysms from 4 of the common locations in cerebral suggested to influence aneurysm shape and risk of rupture, arteries (anterior communicating artery [AcomA], middle cerebral especially for locations with unbalanced contact constraint.8 artery [MCA], internal carotid artery [ICA], basilar artery [BA]) were Intra-aneurysmal hemodynamic characteristics are also selected from the University of California, Los Angeles interventional believed to be an important factor for aneurysm growth and neuroradiology data base from November 2007 to June 2008. 3D rupture.9-16 With the help of advancements in medical imag- rotational angiographic (3DRA) images (Integris; Philips Medical Systems, Best, the Netherlands) obtained before aneurysm emboliza- Received December 5, 2008; accepted after revision March 1, 2009. tion were collected and transferred to an Integris workstation (Philips From the Division of Interventional Neuroradiology (A.C., S.T., F.V.), David Geffen School of Medicine, University of California Los Angeles, Los Angeles, Calif; Department of Compu- Medical Systems) for 3D voxel generation. The Table summarizes the tational Sciences (M.A.C., J.C.), George Mason University, Fairfax, Va; and Department of details of the cases. Biostatistics (J.S.), School of Public Health, University of California Los Angeles, Los Angeles, Calif. Hemodynamic Modeling of Aneurysms Paper previously presented in part at: Annual Meeting of Society of Neurointerventional The computational model for each aneurysm was reconstructed by Surgery, July 28 –August 1, 2008; Lake Tahoe, Calif. using patient-specific computational fluid dynamics simulation Please address correspondence to Aichi Chien, PhD, Division of Interventional Neuroradi- ology, David Geffen School of Medicine at UCLA, 10833 LeConte Ave, Box 951721, Los software developed by George Mason University.14,15,17,19-25 All Angeles, CA 90095; e-mail: [email protected] 3DRA images were denoised and later segmented by using a region- DOI 10.3174/ajnr.A1600 growing algorithm.14,15,20,24 A volumetric model generated by a 3D AJNR Am J Neuroradiol 30:1507–12 Sep 2009 www.ajnr.org 1507
  • 2. Summary of aneurysm cases* Characteristics Group 1 Group 2 Group 3 Group 4 Summary Age (year) Mean 65.2 64.2 51.3 57.3 59.5 Range 48–81 42–79 24–70 47–70 24–81 Sex (No. of patients) Female 5 5 6 3 19 Male 1 1 0 3 5 Unruptured-ruptured aneurysms (No. of patients) 4–2 4–2 4–2 4–2 16–8 Total No. of aneurysms 6 6 6 6 24 Largest diameter of aneurysm (mm) Mean 5.2 6.25 7.2 11.0 7.4 Range 3.6–8.2 5.1–8.1 5–8 6–15 3.6–15 Diameter of aneurysm neck (mm) Mean 3.5 3.7 4.4 7.17 4.7 Range 2.3–6.5 3.3–4 2.7–7 4–14.6 2.3–14.6 Size of aneurysm (No. of patients) 7 mm 5 4 2 1 12 7–12 mm 1 2 4 2 9 13–24 mm 0 0 0 3 3 Diameter of parent artery vessel lumen (mm) Mean 2.1 2.2 3.9 3.4 2.9 Range 1.3–3.2 1.6–2.7 3.4–5.3 2.7–4.4 1.3–4.4 * Groups 1, 2, 3, and 4 are aneurysms located at the AComA, MCA, ICA, and BA, respectively. advancing front technique was used to define the geometry of the the parent artery— crossing at the proximal end of the aneurysm, the computational domain. To have the same inflow settings for all the center of the aneurysm, and the distal end of the aneurysm. For an- aneurysm simulations, aneurysms located at the anterior circulation eurysms located at multi-avenue terminals or bifurcations, 1 region were all modeled from the ICA cavernous segment, and aneurysms crossed the proximal point of the bifurcation at the main artery and located at posterior circulation were all modeled from the BA 2 regions crossed the arteries at the distal end of the aneurysm. segment. Although the 6-region method reduces the complexity of hemo- Previously reported pulsatile flow profiles for the ICA and BA dynamic results, its consistency with hemodynamic data collected measured from a healthy subject by using phase-contrast MR imag- from the entire aneurysm dome and parent artery needed to be eval- ing (Signa 1.5T scanner; GE Healthcare, Waukesha, Wis) were im- uated. Due to the complexity of the data-analysis process, few studies posed as the inflow for the computational fluid dynamics mod- have detailed the collection of hemodynamic data from the entire els.14,21,26 The flow profiles were prescribed by using the Womersley aneurysm dome and parent artery. However, one relatively recent solution for the fully developed pulsatile flow in a rigid straight report by Shojima et al13 extracted data from the entire aneurysm tube13-15,27 and were scaled according to the cross-sectional area of dome and MCA to study MCA aneurysms. We reproduced their ap- the inflow vessels for each model.28 Assuming that all the distal vas- proach and compared results collected from the entire dome and cular beds have similar total resistance to flow, traction-free boundary parent artery with the 6-region method. Because the method of conditions with the same pressure level were applied to all the model Shojima et al13 was only applicable to study WSS in MCA aneurysms, outlets. Blood flow was modeled as an incompressible Newtonian 10 MCA aneurysms from the University of California, Los Angeles fluid. The governing equations were the unsteady Navier-Stokes interventional neuroradiology data base (from November 2007 to equations in 3D. The blood attenuation was 1.0 g/cm3 and the viscos- June 2008) were selected for the method comparison. ity was 0.04 poise. Vessel walls were assumed rigid, and no-slip boundary conditions were applied at the walls. Numeric solutions of Statistical Methods the Navier-Stokes equations were obtained by using a fully implicit Results were expressed as mean value and SD. Repeated measure- finite-element formulation. Two cardiac cycles were computed by ments and analysis of variance were used. Multivariate tests and mul- using 100 steps per cycle, and all the results presented corresponded to tiple comparisons between location groups were performed to see the the second cardiac cycle.13-15,27 Details of the simulation settings have relationship of hemodynamic properties and locations. The sign been previously described.14,15,17,19-25 test30 was used for the method comparison. The Spearman rank cor- relation was used to find the relationship between vessel dimensions Quantitative Hemodynamic Analysis and Validation and hemodynamic values. The statistical significance level was set Method at .05. After the hemodynamic simulation, for each aneurysm, the blood- flow rate and WSS at the peak of the cardiac cycle were collected both Results from the aneurysm and the parent artery. We applied a previously developed technique to perform quantitative analyses by using a pre- Hemodynamic Properties in Aneurysms defined 6-region method.29 Hemodynamic data were collected from The representative hemodynamic properties of brain aneu- 3 equal sections in the aneurysm dome, with regions defined crossing rysms from different locations are shown in Fig 2. Patient- the aneurysm dome at the level of the aneurysm neck, middle, and top specific aneurysm models were reconstructed based on the (Fig 1). Likewise, data in the vessel were recorded from 3 regions of 3DRA images (Fig 2, top row). The instantaneous streamlines 1508 Chien AJNR 30 Sep 2009 www.ajnr.org
  • 3. Fig 1. Schematic representations of regions for hemodynamic data analysis. A, Regions in the arteries of terminal or bifurcation aneurysms. B, Regions in the arteries of sidewall aneurysms. C, Regions in the aneurysm dome. D and E, Application to patient-specific aneurysm models are shown for a bifurcation aneurysm (D) and a sidewall aneurysm (E ). Fig 2. Representative hemodynamic results for AcomA (A and B), MCA (C and D ), ICA (E and F ), and BA (G and H ) aneurysms. Top row is the 3DRA images obtained for each aneurysm during the clinical procedure. A diversity of aneurysms and complicated arterial structures can be observed. The middle row (flow pattern) and the bottom row (WSS) are the hemodynamic results obtained from the simulation. Flow pattern and WSS show differences among aneurysms, and each one has a unique pattern in the arteries and the aneurysms. WSS is in pascal units. at the peak of systole, recorded from the trajectory of the in- we calculated the WSS and flow rate from different regions of stantaneous 3D velocity field,29 show the flow pattern in aneurysms. The average WSS in the aneurysms, parent arter- the aneurysms (Fig 2, the second row). The third row is the ies, and the entire aneurysm area (both aneurysm and parent distribution of WSS for each aneurysm. As previously shown, artery regions) is shown in Fig 3. WSS was found to differ the patient-specific hemodynamic simulation allowed us to among locations in aneurysms (P .01) and in parent arteries study flow properties in various aneurysms; however, the re- (P .009). Multiple comparisons showed that the BA aneu- sults yielded from the simulation can be complicated and dif- rysms had the lowest average WSS, lower than AcomA (P ficult to compare, especially when studies include a variety of .009), ICA (P .001), and MCA (P .001) aneurysms. WSS aneurysms. in AcomA aneurysms was lower than that in MCA aneurysms For quantitative comparison of hemodynamic properties, (P .001). AJNR Am J Neuroradiol 30:1507–12 Sep 2009 www.ajnr.org 1509
  • 4. Fig 3. WSS in aneurysms at each location. Note the average WSS in arteries and aneurysms and the average WSS in the entire aneurysm area. Fig 4. Flow rates in aneurysms at different locations. Note the average flow in arteries and aneurysms and the average flow velocity in the entire aneurysm area. The average blood-flow rate calculated for the aneurysms, shapes and complicated vascular structures. In this study, we parent arteries, and the entire aneurysm area is shown in Fig 4. quantitatively analyzed hemodynamic data in aneurysms and We found the trend of flow rate in the parent arteries (P found that there were hemodynamic differences among aneu- .001) and aneurysms (P .071) also differed among loca- rysms at different locations. Many causes may produce differ- tions. Aneurysms at the BA had the lowest average flow rate, ences in aneurysmal hemodynamic values among locations: and multiple comparisons showed that the flow rate in BA aneurysm geometry, vessel geometry, parent artery size and aneurysms was lower than that in AcomA (P .018), ICA curvature, or blood flow rates. From this study, we were not (P .001), and MCA (P .001) aneurysms. Flow in AcomA able to determine the reason for such hemodynamic differ- aneurysms was slower than that in MCA (P .001) and ICA ences because of the small number of cases. Furthermore, (P .05) aneurysms. many other factors affecting aneurysms were not considered, including aneurysm size, patient age and sex, and population. Technique Validation Studies incorporating those groups with more cases are also Figure 5 shows the average WSS in 10 MCA aneurysms ob- important to find out how hemodynamic changes among lo- tained by the present method, which collected data from 6 cations are associated with these parameters. regions, and by the method of Shojima et al,13 which found We found different hemodynamics properties according to WSS averages in the aneurysm dome and parent artery. The location. The results may not be surprising because different- average WSS in the aneurysms obtained by the present sized vessels have different flow.31 Such evidence has not yet method and by Shojima et al were 10.3 5.2 Pa and 11.7 3.6 been shown in human brain aneurysms; instead, many hemo- Pa, respectively (Fig 5A). The average WSS in the parent arter- dynamic studies have combined aneurysms in various loca- ies was 19.3 4.6 Pa and 17.4 5.9 Pa, respectively (Fig 5B). tions.14,18,32 Although this is a preliminary study and further We found that the present method and that of Shojima et al proof of this finding is needed, we think that on the basis of our yielded similar results and there was no statistical difference results, consideration of hemodynamic variation between lo- between the techniques (P .344). cations will be important for future studies. Furthermore, in our cases, no significant correlations were found between par- Discussion ent artery size and aneurysm WSS ( 0.357; P .086) and Patient-specific hemodynamic analysis enabled us to simulate flow rate ( 0.286, P .175), suggesting that due to the intra-aneurysmal flow properties for a diversity of aneurysm complexity of the brain vascular structure, using only the size 1510 Chien AJNR 30 Sep 2009 www.ajnr.org
  • 5. Limitations We compared hemodynamic properties in aneurysms among various aneurysm locations; however, even aneurysms at the same location have anatomic variations that may also affect the hemodynamic properties. Because of the limited number of cases, we were not able to compare how these anatomic differences affect aneurysm hemodynamics. Moreover, the case selection in this study was not ideal, with, for example, more large aneurysms in the BA group than in other locations. This case selection was affected by the patients’ enrollment patterns in our medical center. Although we found a statisti- cally significant difference among groups in our cases, these variations in anatomy and size were included. Further re- search with more detailed anatomic categorization and com- bining a multicenter data base would still be needed to provide thorough understanding of the association among aneurysm hemodynamics and locations and anatomic variations. Our hemodynamic study used a human pulsatile profile with inflow conditions scaled according to the patients’ inflow vessel sizes. A simulation with patient-specific inflow condi- tions will be the most ideal flow conditions to use. A recent study has shown success by using patient-specific blood-flow information collected from phase-contrast MR imaging to perform hemodynamic simulations.18 However, obtaining sufficient aneurysm cases with patients’ intracranial vessel ge- ometry and flow information is technically challenging. One of our future tasks will be collecting patient-specific inflow information to incorporate into the hemodynamic simulation to test our findings. In this study, we used the 6-region method to study hemo- dynamic properties and showed that it was a comparable and more computationally efficient approach in comparison with results collected from the entire aneurysm dome and parent artery. This data-collection method is a useful tool to reduce Fig 5. A and B, Validation study comparing the hemodynamic results by using 6 regions the amount of data and accelerate the data-collection process, (solid) and values collected from the entire dome and parent artery (method of Shojima et which is suitable for larger case numbers. However, this is just al13) (hollow) shows the average WSS in the aneurysms (A ) and the average WSS in the parent arteries (B). Note in cases 5 and 8 that both methods show the same average WSS one way to perform data analysis, and efforts to improve the in the aneurysm. analysis methods for various aneurysms are still needed to develop accurate and efficient hemodynamic analysis tools for studies including a large number of cases. In this study, we of the vessel may not be enough to understand the flow prop- analyzed the hemodynamic value at the peak of systole as our erties in aneurysms. first step to study aneurysms at different locations. Further Hemodynamic influences have important effects on vascu- study comparing the entire cardiac cycle with patient-specific lar diseases.28,33-36 WSS, caused by blood flow, is a tangential flow profiles will be needed to study whether hemodynamic force acting on the endothelial surface. Studies have shown differences among locations change during the course of the that though WSS is a small force that is insufficient to tear the cardiac cycle. vessel wall, it is an important determinant of endothelial cell The current analysis still used hemodynamic simulation function especially when WSS is low.28,34,35 Recently, studies focused on a particular segment of the artery. Because asym- evaluated the presence of endothelial cell
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