Computational fluid dynamics analysis on recurrence of simple coiling intracranial aneurysms with remnant neck
- Xilong Yu†1,
- Gang Lu†1,
- Shengzhang Wang2Email author,
- Lei Huang1,
- Liang Ge1,
- Jun Wan3,
- Ruoyu Di1,
- Yeqing Jiang1 and
- Xiaolong Zhang1Email author
© The Author(s) 2016
Received: 21 February 2016
Accepted: 26 August 2016
Published: 18 October 2016
Hemodynamic factors are considered to play an important role in the initiation and recurrence of cerebral aneurysms. However, hemodynamic characteristics leading to the recurrence of aneurysms is not well recognized. This study analyzes the hemodynamics of simple-coiling and remnant-neck aneurysms, and discusses the impact of hemodynamic factors on the recurrence of cerebral aneurysms.
This study selected three simple-coiled and remnant-neck aneurysms with at least once angiographic follow-up. The follow-up was conducted by 3D rotational DSA and the 3D reconstruction of the vessel. The aneurysms located on ophthalmic segment of ICA, including one recurrent case and two stable cases. We used a porous medium model to simulate and analyze the hemodynamics of aneurysms.
For the recanalized aneurysm, in the immediate post-operative period, the WSS at the remnant neck decreased, low blood flow velocity and stagnant regions were found in the aneurysm sac. In the first follow-up, compared to immediately post-operative, at the residual neck, the WSS was higher, the flow impingement was stronger. In the sac, the stagnation area decreased and its contour limit shrank into the aneurysm. However, in the second follow-up, compared to the previous follow-up, at the remnant neck, the WSS was lower, the flow impingement weaker, while in the sac the stagnant region expanded.
Aneurysm recurrence could occur in two phases: early coil compaction resulting from blood flow impingement and later vessel remodeling due to hemodynamic effects.
KeywordsCerebral aneurysm Remnant neck Recanalization Computational fluid dynamics Embolization
Endovascular embolization has been widely used as a safe and effective treatment method for intracranial aneurysms. However, the residual neck of intracranial aneurysms can easily relapse after coil embolization . Recurrence is usually influenced by multiple factors, and the pathogenesis is still unclear [2–4]. It is a significant clinical problem, waiting to be addressed by the advancement of endovascular techniques. With the rapid development of hydromechanics and numerical simulation of computational fluid dynamics and its close connection with clinical work, more and more studies increasingly suggest that intracranial aneurysm hemodynamic parameters may be related to recurrence of aneurysms after coil embolization [5–13]. As aneurysm remnant may still carry a small risk of rupture , it is important to study the underlying mechanisms of aneurysm recurrence after coiling. So it is important to study the underlying recurrence mechanism of the remnant-neck aneurysms treated with simple coiling.
Meanwhile, recently most hydrodynamic research only simulates the hemodynamic characteristics of the vessel and the aneurysm remnant-neck after coil embolization [15, 16]. However, these studies did not consider the percolation in the coils after embolization, and hence the conclusion is different with the actual situation.
Our study used a porous medium model to simulate the hydrodynamics of three aneurysms with a remnant-neck after coil embolization. We used the porous medium to simulate the coiled aneurysm, and pure fluid to simulate the parent artery, then calculated and simulated the blood flow with CFD. This study analyzed the hemodynamic changes in the pre-operative, the immediate post-operative period and for the two follow-up periods in order to discuss the hemodynamic mechanism of aneurysm recurrence.
Clinical and image data
Cerebral aneurysm and coil embolization modeling
Where N is the number of coils released into the aneurysm, Vc, i is the volume of ith coil, and Van is the total volume of the aneurysm.
Numerical simulation of blood flow was conducted under corresponding state. The streamlines, the distributions of the wall shear stress (WSS) and the velocity contours of aneurysms were acquired.
Pre-operatively, part of the blood flow entered the aneurysm sac from the distal side of the neck and formed a large and complex vortex inside aneurysm. In the Immediate post-operative period, there was still some minor blood flow in the aneurysm, which entered the aneurysm from the distal side of the remnant neck, but the blood flow in the aneurysm was less than the untreated aneurysm. In the two follow-ups, compared to the immediate post-operative period, the blood flow in the aneurysm had no obvious change, there was still some slight blood flow in the aneurysm. But for recanalized case 1, high velocity and dense streamlines could be demonstrated by the enlargement of the remnant neck. Luo B et al.  assumed, after partial occlusion, that the blood inflow did not enter the aneurysm sac. They used a model of the parent artery for hemodynamic analysis after coil embolization, which was equivalent to directly deleting the aneurysm and did not correspond to the actual blood flow situation. In this study, we used a porous media model to simulate the blood flow in the aneurysm, and more accurately simulated the blood flow.
Distributions of the wall shear stress
Magnitude of Wall Shear Stress (Pa) and velocity (m/s)
The velocity contours on the longitudinal section
Pre-operatively, the blood flow velocity was rapid in the sac, and no stagnation region was formed in the recanalized and stable aneurysms. In the immediate post-operative period, the velocity became lower in most of the aneurysm sac, and then formed a stagnant region. While for the recanalized case, an obvious flow impingement region could be observed in a wide area at the remnant neck. In the first follow-up, for the recanalized case, the flow impingement was stronger than the immediate post-operative period, the impingement region was wide, while the stagnation area in the aneurysm was reduced; for stable cases, the velocity had no obvious change (Table 1). In the second follow-up, the flow impingement in the recanalized case became weaker than in the first follow-up.
Recently, hemodynamic research mainly simulated the blood flow characteristics of the remnant neck without considering the coils . However, even when an aneurysm was completely embolized, the packing density might be only 25–35 % . Though the aneurysm displayed no contrast material, in the immediate post-operative period, blood flow percolation could still occur in the aneurysm pouch. Therefore their method did not accord with the actual situation. Our study used a porous medium model as the equivalent of the coils , and combined with the reconstruction of the parent artery to simulate the hemodynamic characteristics of the aneurysm obtaining a more accurate result. Meanwhile, the porous model required the uniformity of the simulation material. In this study, in the immediate post-operative period, the velocity of the blood flow surrounding the coils was high, so that no thrombosis was formed in the aneurysm. As the material in the aneurysm approximated homogeneous distribution, it was reasonable to model the aneurysm with the porous medium. In the two follow-ups, significant thrombosis formed in the aneurysm, resulting in a change of porosity, so that the porous medium may not very accurately model the blood flow, while there was also percolation in the aneurysm. So the porous medium simulation largely replicated the blood flow situation, and the hemodynamic results were relatively accurate.
Sluzewski M  et al. demonstrated that coil compaction, resulting from high blood flow impingement, was an important factor in aneurysm recurrence. Some studies had also found that hemodynamic factors, such as high WSS and velocity, were highly related to aneurysm recurrence [16, 20]. In this study, for recanalized case, in the immediate post-operative period, the form of the aneurysm had no obvious change. However, a sizeable blood stagnation region was formed in the sac, and the WSS on the remnant neck decreased. In the first follow-up, the remnant neck area had no obvious change, the WSS on the remnant neck was higher than the immediate post-operative period, the flow impingement was stronger, while the impingement region was wide, and the blood stagnation region decreased. In the second follow-up, the remnant neck of the aneurysm enlarged, the aneurysm recurred, and while the WSS was lower on the remnant neck and aneurysm sac than the previous follow-up, the blood stagnation region became larger. For the recanalized case the WSS and velocity underwent dynamic changes during the aneurysm recurrence process after embolization, which influenced the progress of the aneurysm outcome. In conclusion this aneurysm recurrence process can be divided into two phases: in the first phase (from the immediate post-operative period to the first follow-up) the aneurysm did not recur, the coils experienced only minor compaction, resulting in local high blood flow velocity and a decrease in the blood stagnation area, the WSS on the remnant neck increased. In the second phase (from the first follow-up to the second follow-up) high WSS on the remnant neck resulted in the regrowth of the remnant neck and aneurysm recurrence.
In our study, for recurrent case 1, it was stable in the 6-month follow-up, but had recanalized in the 18-month follow up. For recurrent case 2, it recurred in the first follow-up on seventh month after procedure. Therefore, the different interval in different patients between the first follow-up and the second follow-up may induce much influence on the results. And it is necessary to conduct long-term follow-up for remnant-neck aneurysms. In clinical practice, the hemodynamic features of the intracranial aneurysms can also provide some references for the treatment and follow-up of the intracranial aneurysms.
The porous medium model also has some limitations, in the immediate post-operative period, the velocity of the blood flow surrounding the coils was high, so that thrombosis was difficult to be formed in the aneurysm. It is relatively reasonable to model the aneurysm with the porous medium. However, in the two follow-ups, significant thrombosis formed in the aneurysm, resulting in a gradual decrease of porosity, we could not accurately describe the thrombosis and calculate the porosity, but we gave a rough estimate of the porosity of the follow-up. Simultaneously this model represented blood flow in the aneurysm sac after coil embolization, it might be more reasonable than the previous method which directly deleted the aneurysm.
This aneurysm recurrence did not result solely from pure coil compaction or vessel reconstruction caused by hemodynamic change, but was rather the result of these two factors working in concert in two stages. In the first phase, high velocity blood flow impingement on the coils resulted in coil compaction, and the aneurysm did not noticeably recur, while hemodynamic parameters significantly changed. In the second phase, the coils were stable, while high WSS for a long period at the remnant neck resulted in vessel reconstruction leading to aneurysm recurrence.
Computational fluid dynamics
Digital subtraction angiography
Intracranial carotid artery
Wall shear stress
We gratefully acknowledge John Bominghan for English review.
This work is supported by the National Science Foundation of China (grant81371308) and the health and family planning in shanghai city committee projects (grant 20134088).
Availability of data and material
All relevant data of this manuscript can be freely available. And all of the data is linked in https://drive.google.com/open?id=0BwCpEKrOvwY1NU9scm8xdklPRGc.
XL Y carried out aneurysmal model reconstruction and CFD calculation, and drafted the manuscript; GL carried out aneurysmal model reconstruction and CFD calculation; SZ W carried out critical revision of the manuscript for important intellectual content.; LH analyzed and interpreted the data; LG analyzed and interpreted the data; JW acquired the data; RY D carried out aneurysmal model reconstruction; YQ J carried out aneurysmal model reconstruction; XL Z conceived and designed the research, analyzed and interpreted the data, and handled funding and supervision. All authors read and approved the final manuscript.
XL Y: M.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China.
GL: PH.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China.
SZ W: M.D, Department of Mechanics and Engineering Science, Fudan University, Shanghai 200433, China
LH: M.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China
LG: M.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China.
JW: M.D, Department of radiology, Jing’an District Centre Hospital, Shanghai 200040, China.
RY D, M.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China.
YQ J, M.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China.
XL Z, PH.D, Department of Radiology, Huashan Hospital Affiliated to Fudan University, Shanghai 200040, China.
The authors declare that they have no competing interests.
Consent for publication
All of the individual person’s data in the manuscript has been consented to publish which was obtained from the person in this study.
Ethics approval and consent to participate
This study on ethics has been approved and consented by the Medical Ethics Committee of Huashan Hospital.
National Nature Science Foundation of China (Grant No. 81371308)
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Nohra C, Cory D. Long-term catheter angiography after aneurysm coil therapy: results of 209 patients and predictors of delayed recurrence and retreatment. J Neurosurg. 2014;121:1102–6.View ArticleGoogle Scholar
- Kai Y, Hamada J, Kuratsu J, et al. Evaluation of the stability of small ruptured aneurysms with a small neck after embolization with Guglielmi detachable coils: Correlation between coil packing ratio and coil compaction. Neurosurgery. 2005;56:785–92.View ArticlePubMedGoogle Scholar
- Jin S-C, Kwon O-K, Park H, et al. Simple coiling using single or multiple catheters without balloons or stents in middle cerebral artery bifurcation aneurysms. Neuroradiology. 2013;55:321–6.View ArticlePubMedGoogle Scholar
- Gallas S, Pasco A, Cottier JP, et al. A multicenter study of 705 ruptured intracranial aneurysms treated with guglielmi detachable coils. AJNR Am J Neuroradiol. 2005;26:1723–31.PubMedGoogle Scholar
- Shengzhang Wang*, Jialiang Chen, Xiaolong Zhang, et al. Non-newtonian computational hemodynamics in two patient-specific cerebral aneurysms with daughter saccules. J Hydrodynamics. 2010;22:639–646.
- Lu G, Zhang XL, Geng DY, et al. Influence of hemodynamic factor on rupture of intracranial aneurysm: patient-specific 3d mirror aneurysms model computational fluid dynamics simulation. AJNR Am J Neuroradiol. 2011;32:1255–61.View ArticlePubMedGoogle Scholar
- Chatziprodromou I, Tricoli A, Poulikakos D, Ventikos Y. Haemodynamics and wall remodelling of a growing cerebral aneurysm: a computational model. J Biomech. 2007;40:412–26.View ArticlePubMedGoogle Scholar
- Low M, Perktold K, Raunig R. Hemodynamics in rigid and distensible saccular aneurysms: a numerical study of pulsatile flow characteristics. Biorheology. 1993;30:287–98.PubMedGoogle Scholar
- Jou LD, Wong G, Dispensa B, et al. Correlation between luminal geometry changes and hemodynamics in fusiform intracranial aneurysms. AJNR Am J Neuroradiol. 2005;26:2357–63.PubMedGoogle Scholar
- Acevedo-Bolton G, Jou LD, Dispensa BP, et al. Estimating the hemodynamic impact of interventional treatments of aneurysms: numerical simulation with experimental validation: technical case report. Neurosurgery. 2006;59:E429–30.View ArticlePubMedGoogle Scholar
- Sugiyama SI, Meng H, Funamoto K, et al. Hemodynamic analysis of growing intracranial aneurysms arising from a posterior inferior cerebellar artery. World Neurosurg. 2012;78:462–68.View ArticlePubMedGoogle Scholar
- Shojima M, Oshima M, Takagi K, et al. Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of20 middle cerebral artery aneurysms. Stroke. 2004;35:2500–5.View ArticlePubMedGoogle Scholar
- Ford MD, Nikolov HN, Milner JS, et al. Piv-measured versus CFD-predicted flow dynamics in anatomically realistic cerebral aneurysm models. J Biomech Eng. 2008;130:210–15.View ArticleGoogle Scholar
- Sluzewski M, Rooij W, Slob M, et al. Relation between aneurysm volume, packing and compaction in 145 cerebral aneurysms treated with coils. Radiology. 2004;231:653–8.View ArticlePubMedGoogle Scholar
- Hasan DM, Nadareyshvili AI, Hoppe AL, et al. Cerebral aneurysm sac growth as the etiology of recurrence after successful coil embolization. Stroke. 2012;43:86–868.View ArticleGoogle Scholar
- Luo B, Yang X, Wang S, et al. High shear stress and flow velocity in partially occluded aneurysms prone to recanalization. Stroke. 2011;42:745–53.View ArticlePubMedGoogle Scholar
- Kakalis NMP, Mitsos AP, Byrne JV, et al. The haemodynamics of endovascular aneurysm treatment: A computational modeling approach for estimating the influence of multiple coil deployment. IEEE Transmed Imaging. 2008;27:814–24.View ArticleGoogle Scholar
- Choi DS, Kim MC, Terbrugge KG, et al. Clinical and angiographic long-term follow-up of completely coiled intracranial aneurysms using endovascular technique. J Neurosurg. 2010;112:575–81.View ArticlePubMedGoogle Scholar
- Mitsos AP, Kakalis NMP, Ventikos YP, et al. Haemodynamic simulation of aneurysm coiling in an anatomically accurate computational fluid dynamics model: Technical note. Neuroradiology. 2008;50:341–7.View ArticlePubMedGoogle Scholar
- Keiko I, Hitomi A, Naomi H, et al. Computational fluid dynamic analysis following recurrence of cerebral aneurysm after coil embolization. AJNS. 2012;7:109–15.Google Scholar