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Hemodynamics and Rupture of Terminal Cerebral Aneurysms

Rationale and Objectives

The objective of this study was to investigate the relationship between hemodynamics patterns and aneurysmal rupture in cerebral aneurysms of the same morphology regardless their location. Particularly, terminal aneurysms in both the anterior and posterior circulation were studied.

Materials and Methods

A total of 42 patient-specific vascular models were constructed from three-dimensional rotational angiography images. All patients had terminal aneurysms at different arteries: a) middle cerebral; b) anterior communicating; c) internal carotid (terminus); d) internal carotid–posterior communicating; e) basilar; or f) anterior cerebral. Hemodynamics information (intra-aneurysmal velocity and wall shear stress distributions) was derived from image-based computational fluid dynamics models with realistic patient-specific anatomies.

Results

The group of aneurysms with an inflow jet that splits in two secondary jets, one of which enters the aneurysm before reaching one of the daughter vessels (type B), had the highest peak wall shear stress (WSS) and the highest rupture rate. The peak WSS averaged over each flow type showed a higher value in the ruptured group. The average peak WSS in the ruptured group (all types) was 188 dyn/cm 2 (compared to 118 dyn/cm 2 for the unruptured).

Conclusions

This finding is in agreement with a previous work in which only anterior communicating artery aneurysms were investigated. The significance of these findings is that, if they are statistically confirmed with larger number of cases, flow types could be directly observed during angiographic examinations and linked to WSS categories that may help evaluate which aneurysms are more likely to rupture.

It is widely believed that the initiation, growth, and ultimately rupture of cerebral aneurysms is related to the interaction between hemodynamic forces with the arterial wall biology resulting in a focalized weakening of the wall. For example, anterior communicating artery (AcoA) aneurysms can be experimentally produced in hypertensive rats by unilaterally ligation of the common carotid artery , suggesting a causative relationship between increased flow and aneurysm formation. The flow dynamics of cerebral aneurysms have been studied in numerous experimental models and clinical studies to investigate the role of hemodynamics in their initiation, growth, and rupture . Although this work has characterized the complexity of intra-aneurysmal hemodynamics, the studies have largely focused on idealized aneurysm geometries or surgically created aneurysms in animals. Each of these approaches has had significant limitations in connecting the hemodynamic factors studied with clinical events. Recently, computational fluid dynamics studies have tried to replicate the exact anatomy of specific patients and investigate connections between hemodynamic variables and aneurysm rupture . In this study, a further analysis of the relationship between hemodynamic characteristics and aneurysm rupture is carried out using image-based, patient-specific computational models. In our previous study of anterior communicating artery aneurysms, we found a possible association between both the flow pattern and the high wall shear stress with rupture . Given that most aneurysms had a flow pattern compatible with a terminal location, that single morphological type (terminal aneurysms) is investigated in this work.

Material and methods

Patients and Images

A total of 42 consecutive terminal cerebral aneurysms were selected from our database for this study. Patients referred to the interventional neuroradiological service of the Inova Fairfax Hospital (Virginia) between 2003 and 2005, and diagnosed with cerebral aneurysms by conventional catheter angiograms and three-dimensional rotational angiography were considered. Rotational angiography images were obtained during a 180° rotation and imaging at 15 frames per second for a total of 8 seconds, by using an Integris system (Philips Medical Systems, Best, The Netherlands). The corresponding 120 projection images were reconstructed into a three-dimensional data set of 128 × 128 × 128 voxels covering a field of view of 54.02 mm on a dedicated Philips workstation. The selected aneurysms occurred at the bifurcation apex of a single inflow vessel subdivided into two branches of roughly the same diameter. This study included terminal cerebral aneurysms at different locations: 22 in the AcoA, 9 in the middle cerebral artery, 5 in the basilar artery, 3 in the internal carotid artery terminus, 2 at the internal carotid artery–posterior communicating artery bifurcation, and 1 in the anterior cerebral artery (anterior cerebral artery-pericallosa). In this sample, there were 25 ruptured aneurysms (59%) and 17 unruptured aneurysms (41%). Patient characteristics are included in Table 1 . Examples of terminal cerebral aneurysms at different locations are shown in Figure 1 . The rotational angiography images were obtained during a 180° rotation and imaging at 15 frames per second for a total of 8 seconds, using a Phillips Integris System. The corresponding 120 projection images were reconstructed into three-dimensional datasets of 256 × 256 × 256 voxels covering a field of view of 54.02 mm on a dedicated Phillips workstation. The voxel data were exported to a PC for patient-specific computational modeling.

Table 1

Patient Characteristics

Gender No. % Location No. Male 18 42% Acom bilateral 11 Female 24 58% Acom unilateral 11 Ruptured MCA bifurcation 9 Yes 25 59% BA tip 5 No 17 41% Pcom 2 Age ICA terminus 3 Min 35 ACA-pericallose 1 Max 88 Mean 56 Total 42

Acom: anterior communicating artery; MCA: middle cerebral artery; BA: basilar artery; Pcom: posterior communicating artery; ICA: internal carotid artery; ACA: anterior cerebral artery.

Figure 1, Examples of terminal cerebral aneurysms at different locations.

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Patient-Specific Models

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Hemodynamics Characterization

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Figure 2, Classification of flow patterns according to the parent artery flow splitting characteristics.

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Figure 3, Examples of cerebral aneurysm flow classifications using color-coded streamlines.

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Results

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Table 2

Number and Percentage of Ruptured (R) and Unruptured (UR) Aneurysms in each Flow Type

Type R % UR % Total A 6 50% 6 50% 12 B 15 68% 7 32% 22 C 2 33% 4 67% 6 Total 23 58% 17 42% 40

In these results, the two ruptured aneurysms with a pathological reduction of the lumen proximal to the aneurysms and a consequent extremely elevated wall shear stress were excluded.

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Table 3

Maximum Wall Shear Stress Averaged over Flow Type for Ruptured (R) and Unruptured (UR) Aneurysms

Type R Range UR Range A 89 35–200 68 10–150 B 226 50–600 175 10–570 C 165 160–170 93 10–40 Mean 188 35–600 118 10–570

In these results, the two ruptured aneurysms with a pathological reduction of the lumen proximal to the aneurysms and a consequent extremely elevated wall shear stress were excluded. If they were included, the average wall shear stress of the ruptured group would be 271 dyn/cm 2 .

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Figure 4, Peak wall shear stress distributions in ruptured and unruptured aneurysms of each flow type. Maximum scale values for ruptured aneurysms are: 200, 450, and 150 dyn/cm 2 for flow types A, B, and C, respectively (upper row) . Maximum scale values for unruptured aneurysms are: 150, 35, and 10 dyn/cm 2 for flow types A, B, and C, respectively (lower row) .

Figure 5, Flow patterns for ruptured and unruptured aneurysms of each type. Different flow types tend to produce different levels of wall shear stress on the aneurysm (the WSS distributions corresponding to these aneurysms are shown in Figure 4 ). Maximum scale values for ruptured aneurysms are: 200, 450, and 150 cm/sec for flow types A, B, and C, respectively (upper row) . Maximum scale value for unruptured aneurysms is 100 cm/sec for all flow types (upper row) . Maximum scale values for unruptured aneurysms are 40, 25, and 40 cm/sec for flow types A, B, and C, respectively (lower row) .

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Conclusion

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