Blood flow stagnation after treatment of a giant internal carotid artery aneurysm: a computed fluid dynamics analysis

doi:10.21203/rs.3.rs-1348097/v1

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Blood flow stagnation after treatment of a giant internal carotid artery aneurysm: a computed fluid dynamics analysis

https://doi.org/10.21203/rs.3.rs-1348097/v1

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Balloon test occlusion (BTO) is an angiographic test to evaluate ischemic tolerance after permanent occlusion of an internal carotid artery (ICA). BTO can simulate ischemia caused by parent artery occlusion and can be used to select a suitable bypass surgery using specific criteria. On the other hand, a postoperative thrombus can form despite proper case selection, optimal radiological evaluation, and an appropriate surgical strategy. Postoperative ischemic complications related to perforating branches are clinically significant. This simulation study aimed to analyze postoperative flow characteristics and elucidate the cause of ischemic complications related to the perforating branch using computational fluid dynamics (CFD). An unexpected postoperative thrombus formation related to the perforating branch occurred after treating a giant aneurysm in the cavernous portion of the ICA in a patient. Three-dimensional digital subtraction angiography was used to acquire flow data and set up the CFD simulation. The flow simulations were performed at various bypass flow rates. The CFD analysis indicated flow stagnation in the ICA only when surgical treatment using a low-flow bypass graft was performed. Thrombus formation may lead to ischemic complications related to the perforating branch, such as the anterior choroidal artery. BTO did not reflect the influence of bypass blood flow. Therefore, recognizing that blood flow stagnation may occur and comprehensively deciding on the surgical strategy by CFD analysis can be helpful to prevent ischemic complications in patients with giant aneurysms.

Treatment for large or giant aneurysms in the cavernous portion of the internal carotid artery (ICA) remains challenging. Although recent advances in endovascular therapy could provide less invasive treatment for intracranial aneurysms, they do not always offer good outcomes, especially for large or giant ICA aneurysms. Parent artery occlusion (PAO) can lead to intra-aneurysmal thrombosis. However, PAO may occasionally require reconstructive bypass surgery, such as low-flow bypass with a superficial temporal artery (STA)–middle cerebral artery (MCA) bypass or high-flow bypass with a radial artery/saphenous vein graft. A preoperative balloon test occlusion (BTO) of the parent artery is commonly performed to assess the appropriate bypass surgery for each patient. The BTO can simulate the ischemic condition caused by PAO and facilitate the selection of the bypass surgery method using specific criteria. In our institute, we select each treatment based on BTO results.

A postoperative thrombus can form despite proper case selection, optimal radiological evaluation, and an appropriate surgical strategy. Postoperative ischemic complications related to the perforating branches are clinically significant. We recently experienced unfavorable outcomes, such as an unexpected postoperative thrombus formation related to the perforating branch, after treating a giant aneurysm in the cavernous portion of the ICA.

Computational fluid dynamics (CFD) has been used in clinical practice to obtain precise patient-specific hemodynamic parameters, including 3D-velocity, streamline, and particle tracking. This study aimed to analyze postoperative flow characteristics using CFD and elucidate intracranial thrombus formation mechanisms.

Analysis of patient flow data

Figure 4 depicts streamlines color-coded based on their origin. In the posterior–anterior view, the green line indicates blood flow from the left ICA, the red line indicates bypass flow from the STA, and the blue line indicates blood flow from the BA. Without any bypass, the retrograde blood flow of the ICA C8 segment was demonstrated through the posterior communicating artery (Pcom) (Fig. 4a). With a very low bypass flow rate of 25 ml/min, the blood flow of the ICA C8 segment was similar to that in the absence of bypass flows (Fig. 4b). Blood flow stagnation was observed with a low-flow bypass (bypass flow rates = 45 and 50 ml/min) (Fig. 4c and d). With high-flow bypass (bypass flow rates = 75 and 100 ml/min), the anterograde blood flow of the ICA C8 segment was observed (Fig. 4e–f). Consequently, no streamlines were observed in the ICA C8 segment when the bypass flow rate was approximately 50 ml/min, indicating that the flow was stagnant in this segment.

The quantitative blood flow analysis is illustrated in Fig. 5. When the bypass flow rate was approximately 50 ml/min, the blood flow was almost zero in the ICA C8 segment, Acom, and Pcom.

Figure 6a depicts the mean PRT for a specific area. The mean PRT was stable and small, except when the bypass flow rate was approximately 50 ml/min (Fig. 6b), indicating that the particles washed out smoothly and had minimal flow stagnation. By contrast, the PRT increased gradually when the bypass flow rate was approximately 50 ml/min, indicating that the risk of thrombus formation increased. Online resources 1–6 reveal the still particle tracking images. The particles were color-coded according to PRT, and those with a large PRT were observed in the case of a bypass flow rate of approximately 50 ml/min, in which the particles were trapped in stagnation and exhibited to-and-fro motions.

In the CFD analysis using the data of postoperative thrombus formation in a patient with a giant aneurysm in the cavernous portion of the ICA, flow stagnation was observed in the ICA C8 segment only when surgical treatment using a low-flow bypass graft was performed. This flow stagnation may have caused the thrombus formation in our case.

Two types of ischemic complications have been reported after surgery for ICA aneurysms with occlusion. One is related to the occlusion of the perforating branch, such as the anterior choroidal artery. Murakami et al. have reported no significant difference in the risk of ischemic complications related to the perforating branch between PAO and any bypass [6]. Hence, ischemic complications related to the perforating branch may be due to mechanisms other than hemodynamic hypoperfusion. The other factor is related to thromboembolic events as most ischemic complications result from surgical procedures.

BTO alone or other CBF studies have performed standard care in the preoperative assessment of patients who require ICA ligation for ICA aneurysms. The sensitivity of BTO can be increased by combining it with CBF studies such as SPECT, PET, and xenon-enhanced CT and stump pressure measurements [7]. Nevertheless, postoperative ischemic complications may occur in approximately 10–20% of patients who pass BTO with the hypotensive challenge [8–10].

BTO cannot consider the effect of bypass blood flow after ICA ligation for ICA aneurysm surgery; therefore, it does not faithfully express postoperative hemodynamics. Postoperative cerebral infarction in the anterior choroidal artery region, a perforating branch, may be a false negative in BTO. As for the ischemia mechanism in our case, stagnation due to the bypass blood flow collision may have been the cause.

Stagnation of blood flow has been reported in cardiovascular surgery. Aortic valve bypass surgery is an alternative to aortic valve replacement in high-risk patients with aortic stenosis. Aortic thrombus is severe and may be caused by blood flow stagnation arising from competition between the antegrade and retrograde flows. Kawahito et al. confirmed flow stagnation in the aorta by CFD analysis [11].

Blood flow stagnation in cerebrovascular surgery has not been previously reported.

This study’s results are based only on the anatomical data of a specific patient. Hence, the results may differ depending on each blood vessel's branch angle and blood vessel diameter; therefore, analyzing each case is necessary.

Postoperative ischemic complications related to the perforating branch are clinically significant in patients with giant aneurysms of the cavernous portion of the ICA. The CFD analysis revealed that flow stagnation occurred only in the ICA C8 segment when surgical treatment using a low-flow bypass graft was performed. Thrombus formation may lead to ischemic complications related to the perforating branch, such as the anterior choroidal artery. Therefore, recognizing that blood flow stagnation may occur and comprehensively deciding on the surgical strategy by CFD analysis can be helpful to prevent ischemic complications in patients with giant aneurysms.

Study design

This simulation study analyzed blood flow stagnation in the ICA in these case scenarios (bypass blood flow rates of 0, 25, 45, 50, 75, and 100 ml/min) based on a patient's preoperative condition data.

This study was approved by the institutional review board of Nagoya University Graduate School of Medicine (approval number: 2016 − 0437). All procedures performed were in accordance with the ethical standards of the Declaration of Helsinki. All experiments were performed in accordance with relevant named guidelines and regulations and informed concent was obtained from the patient’s families.

Operative strategy

Our institute’s policy is essentially based on BTO with a hypotensive challenge (Fig. 1) [1]. In cases in which retrograde dome filling from collateral flow was observed during BTO, a parent artery occlusion (PAO) was conducted. Otherwise, proximal ICA ligation of the cervical portion was performed with no retrograde dome filling from the collateral flow during BTO. Treatment for contralateral CCA was based on the second BTO’s results. A high-flow bypass with PAO was administered if a patient exhibited a neurologic deficit during a 20-minute BTO. An STA–MCA bypass with PAO was performed in patients who demonstrated neurologic deficits during a BTO test within a 15-minute hypotensive challenge. Without bypass, PAO was performed in patients who did not demonstrate neurologic deficits during the BTO test within 15 min of a hypotensive challenge.

Digital subtraction angiography

Three-dimensional digital subtraction angiography (3D-DSA) was performed by femoral catheterization using the Seldinger technique with a biplane DSA unit with rotational capabilities (Axiom Artis dTA; Siemens Healthcare, Erlangen, Germany). Typically, 4–10 ml of nonionic contrast medium (Iopamidol, 300 mg of iodine per ml; Teva Takeda Pharma, Nagoya, Japan) was used per acquisition. The spatial resolution was 0.32 × 0.32 mm. Standard anteroposterior and lateral DSA images were obtained with the catheter in the four significant arteries (the common carotid arteries and vertebral arteries). The single 3D rotational angiographic acquisition is typically performed to evaluate aneurysm shape and surrounding blood vessels. Images were reconstructed using a 256 × 256 matrix. Rotational angiographic data were transferred to an independent workstation (Syngo Workplace; Siemens Healthcare, Erlangen, Germany) to generate 3D reformatted images. 3D-DSA data were immediately sent to an adjacent 3D workstation (Siemens Medical Solutions, Erlangen, Germany). An experienced endovascular staff reviewer evaluated the conventional DSA and discussed the operative strategy with the surgical intervention staff.

The CFD model

Postoperative blood flow characteristics were evaluated by CFD analysis. The vascular geometry was reconstructed from the 3D-DSA images, and the surface was smoothed using a 3D slicer, which is an image-computing platform (ver. 4.10.2, The Slicer Community, Harvard, USA). Five layers of prism meshes were created near the vessel wall, and the remaining geometry was filled with polyhedral meshes. The total number of meshes was approximately 600,000. Blood was treated as an incompressible Newtonian fluid with a density of 1,060 kg/m³ and viscosity of 0.004 Pa∙s.

Flow simulation in the 3D domain of the vascular geometry obtained from the 3D-DSA images was conducted using scFlow (MSC software, Japan). The flow was assumed steady. A no-slip condition was applied to the wall, and the vessel wall was assumed to be rigid.

Bypass surgery of the left MCA with clipping of the left ICA was simulated by providing inflow to the left MCA. Previous reports have revealed low-flow bypass grafts, such as the STA permit 15–50 ml/min flow velocity [2–4]. High-flow bypass grafts, such as a radial artery or saphenous vein graft, have flow rates of 50–150 ml/min [2, 5]. Flow simulations were implemented at various intracranial blood flows of the bypass graft (bypass blood flow of 0, 25, 45, 50, 75, and 100 ml/min). Based on the patient's own DSA data, inflows of 235, 5, and 114 ml/min were administered to the right ICA, basilar artery (BA), and left ophthalmic artery, respectively. These blood flow velocities were obtained from the patients’ data. A 0D blood flow model was assigned to the rest of the blood vessels, numerically coupled with blood flow in a 3D domain.

For comparison, ICA clipping without bypass surgery was also simulated. The boundary condition was the same as in the cases with bypass surgery, except for the left MCA. In this case, the 0D blood flow model was assigned to the left MCA instead of defining the flow rate.

Particle residence time

The particle residence time (PRT) was calculated for the quantitative evaluation of particle tracking. The trajectories of massless and volumeless particles were calculated using the predictor–corrector method considering the flow velocity fields.

Patient

A 64-year-old woman visited an ophthalmologist for diplopia for one month. She was referred to our department for abductor nerve palsy. Brain magnetic resonance imaging revealed a 25-mm left giant ICA cavernous segment aneurysm. A 3D-DSA was performed (Fig. 2); the left common carotid artery angiography (CCAG) suggested a left giant ICA cavernous segment aneurysm. The right CCAG with a left ICA balloon occlusion indicated adequate perfusion of the contralateral MCA territory via the anterior communicating artery (Acom). Left external carotid artery angiography with left ICA balloon occlusion indicated retrograde blood flow to the aneurysm via the left ophthalmic artery. No neurological deficit was observed with left BTO, although aphasia occurred during the BTO test with a hypotensive challenge. Computed tomography (CT) perfusion imaging during the BTO test indicated no change in cerebral blood flow (CBF), a slight increase in cerebral blood volume (CBV), and an extension of mean transit time. This CT perfusion image suggested that peripheral arterial dilation led to preserving the left CBF.

Surgical procedure

The patient was in supine, and her head was rotated toward the right side at approximately 30°. A left frontotemporal craniotomy was performed followed by cervical ICA ligation and a double STA–MCA bypass surgery. Intraoperative indocyanine green video angiography revealed good bypass flow. Sensory-evoked potential and motor-evoked potential monitorings were normal during the surgery.

Postoperative course

After the operation, the patient woke up with good consciousness. The patient was transferred to the intensive care unit with no remarkable neurological deficits. Approximately 12 h postoperatively, contralateral hemiplegia, hemianesthesia, and homonymous hemianopsia occurred with occlusion of the anterior choroidal artery. Brain magnetic resonance angiography revealed an acute thrombus formation at the C8 segment of the ICA with good bypass patency (Fig. 3). Despite systemic anticoagulation and antiplatelet therapy, the thrombus formation progressed. On postoperative day 4, the patient died of hemorrhagic cerebral infarction.

Acknowledgments:

We would like to thank Editage (www.editage.com) for English language editing.

Authors’ contributions

- Substantial contributions to conception and design: SM, YA, MS, SO, TI, RS

- Acquisition and analysis and interpretation of data: SM, YA, KU, MS, SO, MNi, TI

- Computed fluid dynamics analysis: RT, MNa

- Drafting a significant portion of the manuscript or figures: SM, RT, MNa

- Supervisor: RS

Data availability

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

Declarations

Funding:

No funds, grants, or other support was received.

Competing interests:

The authors have no competing interests to declare that are relevant to the content of this article.

Ethics approval:

All procedures performed were in accordance with the ethical standards of the Declaration of Helsinki. This study was approved by the institutional review board of Nagoya University Graduate School of Medicine (approval number: 2016-0437).

Consent to participate:

All experiments were performed in accordance with relevant named guidelines and regulations and informed concent was obtained from the patient’s families.

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No competing interests reported.

Video1.mov
Video 1Postoperative blood flow characteristics (bypass flow rate=0ml/min) using PRT. This situation was imitated parent artery occlusion without any bypass vessels. Under this situation, there was no stagnation around the left ICA C8 segment.
Video2.mov
Video 2Postoperative blood flow characteristics (bypass flow rate=25 ml/min) using PRT. This situation imitated parent artery occlusion with very low-flow bypass vessels. Under this situation, stagnation was slight around the left ICA C8 segment.
Video3.mov
Video 3Postoperative blood flow characteristics (bypass flow rate=45 ml/min) using PRT. This situation imitated parent artery occlusion with low-flow bypass vessels, such as the superficial temporal artery. Under this situation, stagnation was present around the left ICA C8 segment.
Video4.mov
Video 4Postoperative blood flow characteristics (bypass flow rate=50 ml/min) using PRT. This situation imitated parent artery occlusion with low-flow bypass vessels, such as the superficial temporal artery. Under this situation, stagnation was present around the left ICA C8 segment.
Video5.mov
Video 5Postoperative blood flow characteristics (bypass flow rate=75 ml/min) using PRT. This situation imitated parent artery occlusion with high-flow bypass vessels, such as the radial artery. Under this situation, no stagnation was observed around the left ICA C8 segment.
Video6.mov
Video 6Postoperative blood flow characteristics (bypass flow rate=100 ml/min) using PRT. This situation imitated parent artery occlusion with high-low flow bypass vessels, such as the saphenous vein. Under this situation, no stagnation was observed around the left ICA C8 segment.

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You are reading this latest preprint version

Blood flow stagnation after treatment of a giant internal carotid artery aneurysm: a computed fluid dynamics analysis

Status:

Version 1

Abstract

Figures

Introduction

Results

Analysis of patient flow data

Discussion

Conclusion

Methods

Study design

Operative strategy

Digital subtraction angiography

The CFD model

Particle residence time

Patient

Surgical procedure

Postoperative course

Declarations

Acknowledgments:

Authors’ contributions

Data availability

Declarations

Funding:

Competing interests:

Ethics approval:

Consent to participate:

References

Additional Declarations

Supplementary Files

Status:

Version 1