Distinctive flow pattern of wall shear stress and oscillatory shear index: similarity and dissimilarity in ruptured and unruptured cerebral aneurysm blebs

Clinical article

View More View Less
  • 1 Departments of Neurosurgery and
  • 2 Radiology, Aomori Prefectural Central Hospital, Aomori, Japan
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

Object

The difference in the hemodynamics of wall shear stress (WSS) and oscillatory shear index (OSI) between ruptured and unruptured aneurysms is not well understood. The authors investigated the hemodynamic similarities and dissimilarities in ruptured and thin-walled unruptured aneurysm blebs.

Methods

Magnetic resonance imaging–based fluid dynamics analysis was used to calculate WSS and OSI, and hemodynamic and intraoperative findings were compared. The authors also compared ruptured and unruptured thin-walled blebs for the magnitude of WSS and OSI.

Results

Intraoperatively, 13 ruptured and 139 thin-walled unruptured aneurysm blebs were identified. Twelve of the ruptured (92.3%) and 124 of the unruptured blebs (89.2%) manifested low WSS and high OSI. The degree of WSS was significantly lower in ruptured (0.49 ± 0.12 Pa) than in unruptured (0.64 ± 0.15 Pa; p < 0.01) blebs.

Conclusions

Ruptured and unruptured blebs shared a distinctive pattern of low WSS and high OSI. The degree of WSS at the rupture site was significantly lower than in the unruptured thin-walled blebs.

Abbreviations used in this paper:ACA = anterior cerebral artery; ACoA = anterior communicating artery; CFD = computational fluid dynamics; ICA = internal carotid artery; MCA = middle cerebral artery; MRA = MR angiography; OSI = oscillatory shear index; SAH = subarachnoid hemorrhage; WSS = wall shear stress.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Address correspondence to: Tomohiro Kawaguchi, M.D., Ph.D., Department of Neurosurgery, Aomori Prefectural Central Hospital, 2-1-1 Higashitsukurimichi, Aomori 030-8553, Japan. email: kawaguchi@nsg.med.tohoku.ac.jp.

Please include this information when citing this paper: published online August 24, 2012; DOI: 10.3171/2012.7.JNS111991.

  • 1

    Ahn S, , Shin D, , Tateshima S, , Tanishita K, , Vinuela F, & Sinha S: Fluid-induced wall shear stress in anthropomorphic brain aneurysm models: MR phase-contrast study at 3 T. J Magn Reson Imaging 25:11201130, 2007

    • Search Google Scholar
    • Export Citation
  • 2

    Bammer R, , Hope TA, , Aksoy M, & Alley MT: Time-resolved 3D quantitative flow MRI of the major intracranial vessels: initial experience and comparative evaluation at 1.5T and 3.0T in combination with parallel imaging. Magn Reson Med 57:127140, 2007

    • Search Google Scholar
    • Export Citation
  • 3

    Beck J, , Rohde S, , el Beltagy M, , Zimmermann M, , Berkefeld J, & Seifert V, : Difference in configuration of ruptured and unruptured intracranial aneurysms determined by biplanar digital subtraction angiography. Acta Neurochir (Wien) 145:861865, 2003

    • Search Google Scholar
    • Export Citation
  • 4

    Canstein C, , Cachot P, , Faust A, , Stalder AF, , Bock J, & Frydrychowicz A, : 3D MR flow analysis in realistic rapid-prototyping model systems of the thoracic aorta: comparison with in vivo data and computational fluid dynamics in identical vessel geometries. Magn Reson Med 59:535546, 2008

    • Search Google Scholar
    • Export Citation
  • 5

    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 26:25502559, 2005

    • Search Google Scholar
    • Export Citation
  • 6

    Cheng CP, , Parker D, & Taylor CA: Quantification of wall shear stress in large blood vessels using Lagrangian interpolation functions with cine phase-contrast magnetic resonance imaging. Ann Biomed Eng 30:10201032, 2002

    • Search Google Scholar
    • Export Citation
  • 7

    Chien A, , Tateshima S, , Castro M, , Sayre J, , Cebral J, & Viñuela F: Patient-specific flow analysis of brain aneurysms at a single location: comparison of hemodynamic characteristics in small aneurysms. Med Biol Eng Comput 46:11131120, 2008

    • Search Google Scholar
    • Export Citation
  • 8

    Giddens DP, , Zarins CK, & Glagov S: The role of fluid mechanics in the localization and detection of atherosclerosis. J Biomech Eng 115:4B 588594, 1993

    • Search Google Scholar
    • Export Citation
  • 9

    Gimbrone MA Jr, , Nagel T, & Topper JN: Biomechanical activation: an emerging paradigm in endothelial adhesion biology. J Clin Invest 99:18091813, 1997

    • Search Google Scholar
    • Export Citation
  • 10

    Glor FP, , Ariff B, , Hughes AD, , Crowe LA, , Verdonck PR, & Barratt DC, : Image-based carotid flow reconstruction: a comparison between MRI and ultrasound. Physiol Meas 25:14951509, 2004

    • Search Google Scholar
    • Export Citation
  • 11

    Glor FP, , Long Q, , Hughes AD, , Augst AD, , Ariff B, & Thom SA, : Reproducibility study of magnetic resonance image-based computational fluid dynamics prediction of carotid bifurcation flow. Ann Biomed Eng 31:142151, 2003

    • Search Google Scholar
    • Export Citation
  • 12

    Hassan T, , Ezura M, , Timofeev EV, , Tominaga T, , Saito T, & Takahashi A, : Computational simulation of therapeutic parent artery occlusion to treat giant vertebrobasilar aneurysm. AJNR Am J Neuroradiol 25:6368, 2004

    • Search Google Scholar
    • Export Citation
  • 13

    Hayakawa M, , Katada K, , Anno H, , Imizu S, , Hayashi J, & Irie K, : CT angiography with electrocardiographically gated reconstruction for visualizing pulsation of intracranial aneurysms: identification of aneurysmal protuberance presumably associated with wall thinning. AJNR Am J Neuroradiol 26:13661369, 2005

    • Search Google Scholar
    • Export Citation
  • 14

    He X, & Ku DN: Pulsatile flow in the human left coronary artery bifurcation: average conditions. J Biomech Eng 118:7482, 1996

  • 15

    Hollnagel DI, , Summers PE, , Kollias SS, & Poulikakos D: Laser Doppler velocimetry (LDV) and 3D phase-contrast magnetic resonance angiography (PC-MRA) velocity measurements: validation in an anatomically accurate cerebral artery aneurysm model with steady flow. J Magn Reson Imaging 26:14931505, 2007

    • Search Google Scholar
    • Export Citation
  • 16

    Isoda H, , Hirano M, , Takeda H, , Kosugi T, , Alley MT, & Markl M, : Visualization of hemodynamics in a silicon aneurysm model using time-resolved, 3D, phase-contrast MRI. AJNR Am J Neuroradiol 27:11191122, 2006

    • Search Google Scholar
    • Export Citation
  • 17

    Isoda H, , Ohkura Y, , Kosugi T, , Hirano M, , Alley MT, & Bammer R, : Comparison of hemodynamics of intracranial aneurysms between MR fluid dynamics using 3D cine phase-contrast MRI and MR-based computational fluid dynamics. Neuroradiology 52:913920, 2010

    • Search Google Scholar
    • Export Citation
  • 18

    Isoda H, , Ohkura Y, , Kosugi T, , Hirano M, , Takeda H, & Hiramatsu H, : In vivo hemodynamic analysis of intracranial aneurysms obtained by magnetic resonance fluid dynamics (MRFD) based on time-resolved three-dimensional phase-contrast MRI. Neuroradiology 52:921928, 2010

    • Search Google Scholar
    • Export Citation
  • 19

    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 29:17611767, 2008

    • Search Google Scholar
    • Export Citation
  • 20

    Jou LD, , Wong G, , Dispensa B, , Lawton MT, , Higashida RT, & Young WL, : Correlation between lumenal geometry changes and hemodynamics in fusiform intracranial aneurysms. AJNR Am J Neuroradiol 26:23572363, 2005

    • Search Google Scholar
    • Export Citation
  • 21

    Karmonik C, , Klucznik R, & Benndorf G: Comparison of velocity patterns in an AComA aneurysm measured with 2D phase contrast MRI and simulated with CFD. Technol Health Care 16:119128, 2008

    • Search Google Scholar
    • Export Citation
  • 22

    Kawaguchi T, , Kanamori M, , Takazawa H, , Omodaka S, , Yonezawa S, & Maeda N, : [Flow dynamics analysis in patients with a ruptured middle cerebral artery aneurysm. A case report.]. No Shinkei Geka 39:281286, 2011. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 23

    Kawaguchi T, , Nishimura S, , Kanamori M, , Hori E, , Shibahara I, & Yonezawa S, : MRI-based flow dynamics analysis in patients with cerebral aneurysm. Jpn J Neurosurg (Tokyo) 19:412418, 2010

    • Search Google Scholar
    • Export Citation
  • 24

    Kayembe KN, , Sasahara M, & Hazama F: Cerebral aneurysms and variations in the circle of Willis. Stroke 15:846850, 1984

  • 25

    Keynton RS, , Evancho MM, , Sims RL, , Rodway NV, , Gobin A, & Rittgers SE: Intimal hyperplasia and wall shear in arterial bypass graft distal anastomoses: an in vivo model study. J Biomech Eng 123:464473, 2001

    • Search Google Scholar
    • Export Citation
  • 26

    Lorensen WE, & Cline HE: Marching cubes: A high resolution 3D surface construction algorithm. Comput Graph 21:163169, 1987

  • 27

    Lotz J, , Döker R, , Noeske R, , Schüttert M, , Felix R, & Galanski M, : In vitro validation of phase-contrast flow measurements at 3 T in comparison to 1.5 T: precision, accuracy, and signal-to-noise ratios. J Magn Reson Imaging 21:604610, 2005

    • Search Google Scholar
    • Export Citation
  • 28

    Malek AM, , Alper SL, & Izumo S: Hemodynamic shear stress and its role in atherosclerosis. JAMA 282:20352042, 1999

  • 29

    Markl M, , Chan FP, , Alley MT, , Wedding KL, , Draney MT, & Elkins CJ, : Time-resolved three-dimensional phase-contrast MRI. J Magn Reson Imaging 17:499506, 2003

    • Search Google Scholar
    • Export Citation
  • 30

    Marshall I, , Zhao S, , Papathanasopoulou P, , Hoskins P, & Xu Y: MRI and CFD studies of pulsatile flow in healthy and stenosed carotid bifurcation models. J Biomech 37:679687, 2004

    • Search Google Scholar
    • Export Citation
  • 31

    Masaryk AM, , Frayne R, , Unal O, , Krupinski E, & Strother CM: In vitro and in vivo comparison of three MR measurement methods for calculating vascular shear stress in the internal carotid artery. AJNR Am J Neuroradiol 20:237245, 1999

    • Search Google Scholar
    • Export Citation
  • 32

    Meng H, , Wang Z, , Hoi Y, , Gao L, , Metaxa E, & Swartz DD, : Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke 38:19241931, 2007

    • Search Google Scholar
    • Export Citation
  • 33

    Mizoi K, , Yoshimoto T, & Nagamine Y: Types of unruptured cerebral aneurysms reviewed from operation video-recordings. Acta Neurochir (Wien) 138:965969, 1996

    • Search Google Scholar
    • Export Citation
  • 34

    Moore JA, , Steinman DA, , Holdsworth DW, & Ethier CR: Accuracy of computational hemodynamics in complex arterial geometries reconstructed from magnetic resonance imaging. Ann Biomed Eng 27:3241, 1999

    • Search Google Scholar
    • Export Citation
  • 35

    Nakase H, , Aketa S, , Sakaki T, , Nakamura M, & Aoyama N: Detection of a newly-developed thin-walled out pouching (“bleb”) in an unruptured intracranial aneurysm by computed tomographic angiography. Acta Neurochir (Wien) 140:517518, 1998

    • Search Google Scholar
    • Export Citation
  • 36

    Papathanasopoulou P, , Zhao S, , Köhler U, , Robertson MB, , Long Q, & Hoskins P, : MRI measurement of time-resolved wall shear stress vectors in a carotid bifurcation model, and comparison with CFD predictions. J Magn Reson Imaging 17:153162, 2003

    • Search Google Scholar
    • Export Citation
  • 37

    Press WH, , Teukolsky SA, , Vetterling WT, & Flannery BP: Numerical Recipes in C: The Art of Scientific Computing ed 2 Cambridge, Cambridge University Press, 1992

    • Search Google Scholar
    • Export Citation
  • 38

    Shimai H, , Yokota H, , Nakamura S, & Himeno R, Extraction from biological volume data of a region of interest with nonuniform intensity. Sumi K: Optomechatronic Machine Vision Proceedings of SPIE Bellingham, WA, SPIE, 2005. 6051:605115, (Abstract)

    • Search Google Scholar
    • Export Citation
  • 39

    Shojima M, , Oshima M, , Takagi K, , Torii R, , Hayakawa M, & Katada K, : Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 35:25002505, 2004

    • Search Google Scholar
    • Export Citation
  • 40

    Steiger HJ: Pathophysiology of development and rupture of cerebral aneurysms. Acta Neurochir Suppl (Wien) 48:157, 1990

  • 41

    Suga M, , Yamamoto Y, , Sunami N, , Abe T, & Kondo A: [Growth of asymptomatic unruptured aneurysms in follow-up study: report of three cases.]. No Shinkei Geka 31:303308, 2003. (Jpn)

    • Search Google Scholar
    • Export Citation
  • 42

    Tateshima S, , Chien A, , Sayre J, , Cebral J, & Viñuela F: The effect of aneurysm geometry on the intra-aneurysmal flow condition. Neuroradiology 52:11351141, 2010

    • Search Google Scholar
    • Export Citation
  • 43

    Tateshima S, , Murayama Y, , Villablanca JP, , Morino T, , Nomura K, & Tanishita K, : In vitro measurement of fluid-induced wall shear stress in unruptured cerebral aneurysms harboring blebs. Stroke 34:187192, 2003

    • Search Google Scholar
    • Export Citation
  • 44

    Tateshima S, , Murayama Y, , Villablanca JP, , Morino T, , Takahashi H, & Yamauchi T, : Intraaneurysmal flow dynamics study featuring an acrylic aneurysm model manufactured using a computerized tomography angiogram as a mold. J Neurosurg 95:10201027, 2001

    • Search Google Scholar
    • Export Citation
  • 45

    Tsukahara T, , Murakami N, , Sakurai Y, , Yonekura M, , Takahashi T, & Inoue T, : Treatment of unruptured cerebral aneurysms; a multi-center study at Japanese national hospitals. Acta Neurochir Suppl 94:7785, 2005

    • Search Google Scholar
    • Export Citation
  • 46

    Wetzel S, , Meckel S, , Frydrychowicz A, , Bonati L, , Radue EW, & Scheffler K, : In vivo assessment and visualization of intracranial arterial hemodynamics with flow-sensitized 4D MR imaging at 3T. AJNR Am J Neuroradiol 28:433438, 2007

    • Search Google Scholar
    • Export Citation
  • 47

    Xiang J, , Natarajan SK, , Tremmel M, , Ma D, , Mocco J, & Hopkins LN, : Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 42:144152, 2011

    • Search Google Scholar
    • Export Citation
  • 48

    Yamashita S, , Isoda H, , Hirano M, , Takeda H, , Inagawa S, & Takehara Y, : Visualization of hemodynamics in intracranial arteries using time-resolved three-dimensional phase-contrast MRI. J Magn Reson Imaging 25:473478, 2007

    • Search Google Scholar
    • Export Citation
  • 49

    Zeng Z, , Kallmes DF, , Durka MJ, , Ding Y, , Lewis D, & Kadirvel R, : Sensitivity of CFD based hemodynamic results in rabbit aneurysm models to idealizations in surrounding vasculature. J Biomech Eng 132:091009, 2010

    • Search Google Scholar
    • Export Citation
  • 50

    Zhao SZ, , Papathanasopoulou P, , Long Q, , Marshall I, & Xu XY: Comparative study of magnetic resonance imaging and image-based computational fluid dynamics for quantification of pulsatile flow in a carotid bifurcation phantom. Ann Biomed Eng 31:962971, 2003

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 775 273 39
Full Text Views 316 48 6
PDF Downloads 213 29 5
EPUB Downloads 0 0 0