J Neurol Surg A Cent Eur Neurosurg 2018; 79(02): 108-115
DOI: 10.1055/s-0037-1603634
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Morphological Effect on Wall Shear Stress in Intracranial Aneurysms

Tian-Lun Qiu
1   Department of Neurosurgery, Shaoxing People's Hospital, Shaoxing, China
,
Guo-Liang Jin
1   Department of Neurosurgery, Shaoxing People's Hospital, Shaoxing, China
,
Wu-Qiao Bao
1   Department of Neurosurgery, Shaoxing People's Hospital, Shaoxing, China
,
Hai-Tao Lu
2   Department of Neurosurgery, Chongming Branch of Shanghai Xinghua Hospital, Shanghai, China
› Author Affiliations
Further Information

Publication History

20 December 2016

05 April 2017

Publication Date:
12 July 2017 (online)

Abstract

Background and Study Aims Both high and low wall shear stress (WSS) play important roles in the development and rupture of intracranial aneurysms (IAs). This study aimed to determine the morphological factors that affect WSS in the IA and the parent artery.

Material and Methods We studied a total of 66 IAs with three-dimensional imaging. Computational fluid dynamics (CFD) models were constructed and used to characterize the hemodynamics quantitatively. Aneurysms were grouped according to the mean neck width. The associations among hemodynamics and morphology were analyzed.

Results Aspect ratio was correlated to lowest WSS (r = − 0.576), aneurysm-to-parent vessel (A-P) WSS ratio (r = − 0.500), and lowest-parent vessel (L-P) WSS ratio (r = − 0.575). Height-to-width ratio and height were correlated to WSS. Mean aneurysm WSS (p = 0.023), lowest WSS (p < 0.0001), highest-to-lowest WSS ratio (p = 0.004), L-P WSS ratio (p < 0.0001), highest-parent vessel (H-P) WSS ratio (p = 0.008), A-P WSS ratio (p < 0.001), and height (p < 0.001) were different between the two groups of aneurysms that were divided by the relationship between the diameters of the aneurysms and the necks. Multivariable analysis showed that the lowest WSS (p = 0.028) and A-P WSS ratio (p = 0.001) were independently associated with neck width.

Conclusion Morphological characteristics are associated with IA and parent vessel WSS. Aneurysms with different neck widths have different hemodynamics. These results could help in understanding the progression of IA and in building predictive models for IA rupture.

 
  • References

  • 1 Connolly Jr ES, Rabinstein AA, Carhuapoma JR. , et al; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2012; 43 (06) 1711-1737
  • 2 Suarez JI, Tarr RW, Selman WR. Aneurysmal subarachnoid hemorrhage. N Engl J Med 2006; 354 (04) 387-396
  • 3 Cebral JR, Meng H. Counterpoint: realizing the clinical utility of computational fluid dynamics—closing the gap. AJNR Am J Neuroradiol 2012; 33 (03) 396-398
  • 4 Jou LD, Wong G, Dispensa B. , et al. Correlation between lumenal geometry changes and hemodynamics in fusiform intracranial aneurysms. AJNR Am J Neuroradiol 2005; 26 (09) 2357-2363
  • 5 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 (02) E429-E430 ; author reply E429–E430
  • 6 Sugiyama S, Meng H, Funamoto K. , et al. Hemodynamic analysis of growing intracranial aneurysms arising from a posterior inferior cerebellar artery. World Neurosurg 2012; 78 (05) 462-468
  • 7 Xiang J, Natarajan SK, Tremmel M. , et al. Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 2011; 42 (01) 144-152
  • 8 Cebral JR, Mut F, Weir J, Putman C. Quantitative characterization of the hemodynamic environment in ruptured and unruptured brain aneurysms. AJNR Am J Neuroradiol 2011; 32 (01) 145-151
  • 9 Shojima M, Oshima M, Takagi K. , et al. Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 2004; 35 (11) 2500-2505
  • 10 Jou LD, Lee DH, Morsi H, Mawad ME. Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 2008; 29 (09) 1761-1767
  • 11 Xiang J, Tutino VM, Snyder KV, Meng H. CFD: computational fluid dynamics or confounding factor dissemination? The role of hemodynamics in intracranial aneurysm rupture risk assessment. AJNR Am J Neuroradiol 2014; 35 (10) 1849-1857
  • 12 Tremmel M, Dhar S, Levy EI, Mocco J, Meng H. Influence of intracranial aneurysm-to-parent vessel size ratio on hemodynamics and implication for rupture: results from a virtual experimental study. Neurosurgery 2009; 64 (04) 622-630 ; discussion 630–631
  • 13 Tateshima S, Tanishita K, Omura H, Villablanca JP, Vinuela F. Intra-aneurysmal hemodynamics during the growth of an unruptured aneurysm: in vitro study using longitudinal CT angiogram database. AJNR Am J Neuroradiol 2007; 28 (04) 622-627
  • 14 Millán RD, Dempere-Marco L, Pozo JM, Cebral JR, Frangi AF. Morphological characterization of intracranial aneurysms using 3-D moment invariants. IEEE Trans Med Imaging 2007; 26 (09) 1270-1282
  • 15 Tateshima S, Chien A, Sayre J, Cebral J, Viñuela F. The effect of aneurysm geometry on the intra-aneurysmal flow condition. Neuroradiology 2010; 52 (12) 1135-1141
  • 16 Moyle KR, Antiga L, Steinman DA. Inlet conditions for image-based CFD models of the carotid bifurcation: is it reasonable to assume fully developed flow?. J Biomech Eng 2006; 128 (03) 371-379
  • 17 Shaffer N, Loth F. CFD challenge: modeling blood flow dynamics in a cerebral aneurysm using Fluent. Paper presented at: ASME 2012 Summer Bioengineering Conference; June 20–23, 2012; Fajardo, Puerto Rico
  • 18 Irie K, Anzai H, Kojima M. , et al. Computational fluid dynamic analysis following recurrence of cerebral aneurysm after coil embolization. Asian J Neurosurg 2012; 7 (03) 109-115
  • 19 Cebral JR, Castro MA, Burgess JE, Pergolizzi RS, Sheridan MJ, Putman CM. Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models. AJNR Am J Neuroradiol 2005; 26 (10) 2550-2559
  • 20 Schnell S, Ansari SA, Vakil P. , et al. Three-dimensional hemodynamics in intracranial aneurysms: influence of size and morphology. J Magn Reson Imaging 2014; 39 (01) 120-131
  • 21 Long Y, Yu H, Zhuo Z. , et al. A geometric scaling model for assessing the impact of aneurysm size ratio on hemodynamic characteristics. Biomed Eng Online 2014; 13: 17
  • 22 LaMack JA, Friedman MH. Individual and combined effects of shear stress magnitude and spatial gradient on endothelial cell gene expression. Am J Physiol Heart Circ Physiol 2007; 293 (05) H2853-H2859
  • 23 Wang Z, Kolega J, Hoi Y. , et al. Molecular alterations associated with aneurysmal remodeling are localized in the high hemodynamic stress region of a created carotid bifurcation. Neurosurgery 2009; 65 (01) 169-177 ; discussion 177–178
  • 24 Boussel L, Rayz V, McCulloch C. , et al. Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke 2008; 39 (11) 2997-3002
  • 25 Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999; 282 (21) 2035-2042
  • 26 Kaiser D, Freyberg MA, Friedl P. Lack of hemodynamic forces triggers apoptosis in vascular endothelial cells. Biochem Biophys Res Commun 1997; 231 (03) 586-590
  • 27 Singh PK, Marzo A, Howard B. , et al. Effects of smoking and hypertension on wall shear stress and oscillatory shear index at the site of intracranial aneurysm formation. Clin Neurol Neurosurg 2010; 112 (04) 306-313
  • 28 Torii R, Oshima M, Kobayashi T. , et al. Fluid-structure interaction modelling of a patient-specific cerebral aneurysm: influence of structural modelling. Comput Mech 2008; 43: 151-159
  • 29 Maurits NM, Loots GE, Veldman AE. The influence of vessel wall elasticity and peripheral resistance on the carotid artery flow wave form: a CFD model compared to in vivo ultrasound measurements. J Biomech 2007; 40 (02) 427-436
  • 30 Steinman DA, Milner JS, Norley CJ, Lownie SP, Holdsworth DW. Image-based computational simulation of flow dynamics in a giant intracranial aneurysm. AJNR Am J Neuroradiol 2003; 24 (04) 559-566
  • 31 Dempere-Marco L, Oubel E, Castro M. , et al. CFD analysis incorporating the influence of wall motion: application to intracranial aneurysms. Med Image Comput Comput Assist Interv 2006; 9 (Pt 2): 438-445
  • 32 Sforza DM, Löhner R, Putman C, Cebral J. Hemodynamic analysis of intracranial aneurysms with moving parent arteries: basilar tip aneurysms. Int J Numer Methods Biomed Eng 2010; 26 (10) 1219-1227
  • 33 Fisher C, Rossmann JS. Effect of non-newtonian behavior on hemodynamics of cerebral aneurysms. J Biomech Eng 2009; 131 (09) 091004
  • 34 Xiang J, Tremmel M, Kolega J, Levy EI, Natarajan SK, Meng H. Newtonian viscosity model could overestimate wall shear stress in intracranial aneurysm domes and underestimate rupture risk. J Neurointerv Surg 2012; 4 (05) 351-357
  • 35 Castro MA, Ahumada Olivares MC, Putman CM, Cebral JR. Unsteady wall shear stress analysis from image-based computational fluid dynamic aneurysm models under Newtonian and Casson rheological models. Med Biol Eng Comput 2014; 52 (10) 827-839
  • 36 Lee SW, Steinman DA. On the relative importance of rheology for image-based CFD models of the carotid bifurcation. J Biomech Eng 2007; 129 (02) 273-278
  • 37 Marzo A, Singh P, Larrabide I. , et al. Computational hemodynamics in cerebral aneurysms: the effects of modeled versus measured boundary conditions. Ann Biomed Eng 2011; 39 (02) 884-896
  • 38 Steinman DA, Taylor CA. Flow imaging and computing: large artery hemodynamics. Ann Biomed Eng 2005; 33 (12) 1704-1709
  • 39 Cebral JR, Castro MA, Appanaboyina S, Putman CM, Millan D, Frangi AF. Efficient pipeline for image-based patient-specific analysis of cerebral aneurysm hemodynamics: technique and sensitivity. IEEE Trans Med Imaging 2005; 24 (04) 457-467
  • 40 Rahman M, Ogilvy CS, Zipfel GJ. , et al. Unruptured cerebral aneurysms do not shrink when they rupture: multicenter collaborative aneurysm study group. Neurosurgery 2011; 68 (01) 155-160 ; discussion 160–161
  • 41 Asari S, Ohmoto T. Natural history and risk factors of unruptured cerebral aneurysms. Clin Neurol Neurosurg 1993; 95 (03) 205-214
  • 42 Zhang Y, Takao H, Murayama Y, Qian Y. Propose a wall shear stress divergence to estimate the risks of intracranial aneurysm rupture. Sci World J 2013; 2013: 508131
  • 43 Sen Y, Qian Y, Avolio A, Morgan M. Image segmentation methods for intracranial aneurysm haemodynamic research. J Biomech 2014; 47 (05) 1014-1019
  • 44 Qian Y, Takao H, Umezu M, Murayama Y. Risk analysis of unruptured aneurysms using computational fluid dynamics technology: preliminary results. AJNR Am J Neuroradiol 2011; 32 (10) 1948-1955
  • 45 Venugopal P, Valentino D, Schmitt H, Villablanca JP, Viñuela F, Duckwiler G. Sensitivity of patient-specific numerical simulation of cerebal aneurysm hemodynamics to inflow boundary conditions. J Neurosurg 2007; 106 (06) 1051-1060