The critical role of hemodynamics in the development of cerebral vascular disease

A review

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Atherosclerosis and intracranial saccular aneurysms predictably localize in areas with complex arterial geometries such as bifurcations and curvatures. These sites are characterized by unique hemodynamic conditions that possibly influence the risk for these disorders. One hemodynamic parameter in particular has emerged as a key regulator of vascular biology—wall shear stress (WSS). Variations in geometry can change the distribution and magnitude of WSS, thus influencing the risk for vascular disorders. Computer simulations conducted using patient-specific data have suggested that departures from normal levels of WSS lead to aneurysm formation and progression. In addition, multiple studies indicate that disturbed flow and low WSS predispose patients to extracranial atherosclerosis, and particularly to carotid artery disease. Conversely, in the case of intracranial atherosclerosis, more studies are needed to provide a firm link between hemodynamics and atherogenesis. The recognition of WSS as an important factor in cerebral vascular disease may help to identify individuals at risk and guide treatment options.

Abbreviations used in this paper: BA = basilar artery; CA = carotid artery; CFD = computational fluid dynamics; ECA = external CA; eNOS = endothelial nitric oxide synthase; ICA = internal CA; iNOS = inducible NO synthase; ISA = intracranial saccular aneurysm; MAPK = mitogen-activated protein kinase; MCA = middle cerebral artery; NF-κB = nuclear factor–kappa B; VA = vertebral artery; WSS = wall shear stress.
Article Information

Contributor Notes

Address correspondence to: Bauer E. Sumpio, M.D., Ph.D., Department of Vascular Surgery, Yale University School of Medicine, 333 Cedar Street, BB 204, New Haven, Connecticut 06520. email: Bauer.sumpio@yale.edu.Please include this information when citing this paper: published online November 27, 2009; DOI: 10.3171/2009.10.JNS09759.
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References
  • 1

    Alnaes MSIsaksen JMardal KARomner BMorgan MKIngebrigtsen T: Computation of hemodynamics in the circle of Willis. Stroke 38:250025052007

    • Search Google Scholar
    • Export Citation
  • 2

    Arnal JFDinh-Xuan ATPueyo MDarblade BRami J: Endothelium-derived nitric oxide and vascular physiology and pathology. Cell Mol Life Sci 55:107810871999

    • Search Google Scholar
    • Export Citation
  • 3

    Atlas SW: Magnetic resonance imaging of intracranial aneurysms. Neuroimaging Clin N Am 7:7097201997

  • 4

    Azuma NDuzgun SAIkeda MKito HAkasaka NSasajima T: Endothelial cell response to different mechanical forces. J Vasc Surg 32:7897942000

    • Search Google Scholar
    • Export Citation
  • 5

    Ballermann BJDardik AEng ELiu A: Shear stress and the endothelium. Kidney Int Suppl 67:S100S1081998

  • 6

    Balligand JLFeron ODessy C: eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev 89:4815342009

    • Search Google Scholar
    • Export Citation
  • 7

    Bauer RSheehan SMeyer JS: Arteriographic study of cerebrovascular disease. II. Cerebral symptoms due to kinking, tortuosity, and compression of carotid and vertebral arteries in the neck. Arch Neurol 4:1191311961

    • Search Google Scholar
    • Export Citation
  • 8

    Bergh NUlfhammer EKarlsson LJern S: Effects of two complex hemodynamic stimulation profiles on hemostatic genes in a vessel-like environment. Endothelium 15:2312382008

    • Search Google Scholar
    • Export Citation
  • 9

    Berk BC: Atheroprotective signaling mechanisms activated by steady laminar flow in endothelial cells. Circulation 117:108210892008

  • 10

    Bilguvar KYasuno KNiemelä MRuigrok YMvon Und Zu Fraunberg Mvan Duijn CM: Susceptibility loci for intracranial aneurysm in European and Japanese populations. Nat Genet 40:147214772008

    • Search Google Scholar
    • Export Citation
  • 11

    Bonneville FSourour NBiondi A: Intracranial aneurysms: an overview. Neuroimaging Clin N Am 16::371382vii2006

  • 12

    Bor ASVelthuis BKMajoie CBRinkel GJ: Configuration of intracranial arteries and development of aneurysms: a follow-up study. Neurology 70:7007052008

    • Search Google Scholar
    • Export Citation
  • 13

    Boussel LRayz VMcCulloch CMartin AAcevedo-Bolton GLawton M: Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke 39:299730022008

    • Search Google Scholar
    • Export Citation
  • 14

    Brooks ARLelkes PIRubanyi GM: Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol Genomics 9:27412002

    • Search Google Scholar
    • Export Citation
  • 15

    Canham PBFinlay HM: Morphometry of medial gaps of human brain artery branches. Stroke 35:115311572004

  • 16

    Castro MAPutman CMCebral JR: Computational fluid dynamics modeling of intracranial aneurysms: effects of parent artery segmentation on intra-aneurysmal hemodynamics. AJNR Am J Neuroradiol 27:170317092006

    • Search Google Scholar
    • Export Citation
  • 17

    Cebral JRCastro MABurgess JEPergolizzi RSSheridan MJPutman CM: Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models. AJNR Am J Neuroradiol 26:255025592005

    • Search Google Scholar
    • Export Citation
  • 18

    Cebral JRCastro MASoto OLöhner RAlperin N: Blood-flow models of the circle of Willis from magnetic resonance data. J Eng Math 47:3693862003

    • Search Google Scholar
    • Export Citation
  • 19

    Chachisvilis MZhang YLFrangos JA: G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci U S A 103:15463154682006

    • Search Google Scholar
    • Export Citation
  • 20

    Chatzizisis YSCoskun AUJonas MEdelman ERFeldman CLStone PH: Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J Am Coll Cardiol 49:237923932007

    • Search Google Scholar
    • Export Citation
  • 21

    Cheng CHelderman FTempel DSegers DHierck BPoelmann R: Large variations in absolute wall shear stress levels within one species and between species. Atherosclerosis 195:2252352007

    • Search Google Scholar
    • Export Citation
  • 22

    Cheng Cvan Haperen Rde Waard Mvan Damme LCTempel DHanemaaijer L: Shear stress affects the intracellular distribution of eNOS: direct demonstration by a novel in vivo technique. Blood 106:369136982005

    • Search Google Scholar
    • Export Citation
  • 23

    Chien ATateshima SCastro MSayre JCebral JViñuela F: Patient-specific flow analysis of brain aneurysms at a single location: comparison of hemodynamic characteristics in small aneurysms. Med Biol Eng Comput 46:111311202008

    • Search Google Scholar
    • Export Citation
  • 24

    Chow CLOng AC: Autosomal dominant polycystic kidney disease. Clin Med 9:2782832009

  • 25

    Dardik AChen LFrattini JAsada HAziz FKudo FA: Differential effects of orbital and laminar shear stress on endothelial cells. J Vasc Surg 41:8698802005

    • Search Google Scholar
    • Export Citation
  • 26

    Dardik ALiu ABallermann BJ: Chronic in vitro shear stress stimulates endothelial cell retention on prosthetic vascular grafts and reduces subsequent in vivo neointimal thickness. J Vasc Surg 29:1571671999

    • Search Google Scholar
    • Export Citation
  • 27

    Dardik AYamashita AAziz FAsada HSumpio BE: Shear stress-stimulated endothelial cells induce smooth muscle cell chemotaxis via platelet-derived growth factor-BB and interleukin-1alpha. J Vasc Surg 41:3213312005

    • Search Google Scholar
    • Export Citation
  • 28

    De Keulenaer GWChappell DCIshizaka NNerem RMAlexander RWGriendling KK: Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: role of a superoxide-producing NADH oxidase. Circ Res 82:109411011998

    • Search Google Scholar
    • Export Citation
  • 29

    de Paepe Avan Landegem Wde Keyser Fde Reuck J: Association of multiple intracranial aneurysms and collagen type III deficiency. Clin Neurol Neurosurg 90:53561988

    • Search Google Scholar
    • Export Citation
  • 30

    DeBakey MELawrie GMGlaeser DH: Patterns of atherosclerosis and their surgical significance. Ann Surg 201:1151311985

  • 31

    Du WMills ISumpio BE: Cyclic strain causes heterogeneous induction of transcription factors, AP-1, CRE binding protein and NF-kB, in endothelial cells: species and vascular bed diversity. J Biomech 28:148514911995

    • Search Google Scholar
    • Export Citation
  • 32

    Eftekhar BDadmehr MAnsari SGhodsi MNazparvar BKetabchi E: Are the distributions of variations of circle of Willis different in different populations? Results of an anatomical study and review of literature. BMC Neurol 6:222006

    • Search Google Scholar
    • Export Citation
  • 33

    Eng EBallermann BJ: Diminished NF-kappaB activation and PDGF-B expression in glomerular endothelial cells subjected to chronic shear stress. Microvasc Res 65:1371442003

    • Search Google Scholar
    • Export Citation
  • 34

    Finlay HMWhittaker PCanham PB: Collagen organization in the branching region of human brain arteries. Stroke 29:159516011998

  • 35

    Fisher CMGore IOkabe NWhite PD: Calcification of the carotid siphon. Circulation 32:5385481965

  • 36

    Fisher MFieman S: Geometric factors of the bifurcation in carotid atherogenesis. Stroke 21:2672711990

  • 37

    Foutrakis GNYonas HSclabassi RJ: Finite element methods in the simulation and analysis of intracranial blood flow. Neurol Res 19:1741861997

    • Search Google Scholar
    • Export Citation
  • 38

    Foutrakis GNYonas HSclabassi RJ: Saccular aneurysm formation in curved and bifurcating arteries. AJNR Am J Neuroradiol 20:130913171999

    • Search Google Scholar
    • Export Citation
  • 39

    Frangos SGGahtan VSumpio B: Localization of atherosclerosis: role of hemodynamics. Arch Surg 134:114211491999

  • 40

    Frösen JPiippo APaetau AKangasniemi MNiemelä MHernesniemi J: Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: histological analysis of 24 unruptured and 42 ruptured cases. Stroke 35:228722932004

    • Search Google Scholar
    • Export Citation
  • 41

    Fukuda SHashimoto NNaritomi HNagata INozaki KKondo S: Prevention of rat cerebral aneurysm formation by inhibition of nitric oxide synthase. Circulation 101:253225382000

    • Search Google Scholar
    • Export Citation
  • 42

    Gao LHoi YSwartz DDKolega JSiddiqui AMeng H: Nascent aneurysm formation at the basilar terminus induced by hemodynamics. Stroke 39:208520902008

    • Search Google Scholar
    • Export Citation
  • 43

    Gaucher CDevaux CBoura CLacolley PStoltz JFMenu P: In vitro impact of physiological shear stress on endothelial cells gene expression profile. Clin Hemorheol Microcirc 37:991072007

    • Search Google Scholar
    • Export Citation
  • 44

    Glagov SZarins CGiddens DPKu DN: Hemodynamics and atherosclerosis. Insights and perspectives gained from studies of human arteries. Arch Pathol Lab Med 112:101810311988

    • Search Google Scholar
    • Export Citation
  • 45

    Gosling RGNewman DLBowden NLTwinn KW: The area ration of normal aortic junctions. Aortic configuration and pulse-wave reflection. Br J Radiol 44:8508531971

    • Search Google Scholar
    • Export Citation
  • 46

    Grond-Ginsbach CSchnippering HHausser IWeber RWerner ISteiner HH: Ultrastructural connective tissue aberrations in patients with intracranial aneurysms. Stroke 33:219221962002

    • Search Google Scholar
    • Export Citation
  • 47

    Hassan TTimofeev EVSaito TShimizu HEzura MMatsumoto Y: A proposed parent vessel geometry-based categorization of saccular intracranial aneurysms: computational flow dynamics analysis of the risk factors for lesion rupture. J Neurosurg 103:6626802005

    • Search Google Scholar
    • Export Citation
  • 48

    Hobson RW IIWilson SEVeith FJ: Vascular Surgery: Principles and Practice ed 3New YorkMarcel Dekker2004

  • 49

    Hoi YMeng HWoodward SHBendok BRHanel RAGuterman LR: Effects of arterial geometry on aneurysm growth: three-dimensional computational fluid dynamics study. J Neurosurg 101:6766812004

    • Search Google Scholar
    • Export Citation
  • 50

    Hoi YWoodward SHKim MTaulbee DBMeng H: Validation of CFD simulations of cerebral aneurysms with implication of geometric variations. J Biomech Eng 128:8448512006

    • Search Google Scholar
    • Export Citation
  • 51

    Hoogstraten HWKootstra JGHillen BKrijger JKWensing PJ: Numerical simulation of blood flow in an artery with two successive bends. J Biomech 29:107510831996

    • Search Google Scholar
    • Export Citation
  • 52

    Horikoshi TAkiyama IYamagata ZSugita MNukui H: Magnetic resonance angiographic evidence of sex-linked variations in the circle of Willis and the occurrence of cerebral aneurysms. J Neurosurg 96:6977032002

    • Search Google Scholar
    • Export Citation
  • 53

    Humphrey JDTaylor CA: Intracranial and abdominal aortic aneurysms: similarities, differences, and need for a new class of computational models. Annu Rev Biomed Eng 10:2212462008

    • Search Google Scholar
    • Export Citation
  • 54

    Ingebrigtsen TMorgan MKFaulder KIngebrigtsen LSparr TSchirmer H: Bifurcation geometry and the presence of cerebral artery aneurysms. J Neurosurg 101:1081132004

    • Search Google Scholar
    • Export Citation
  • 55

    Isaksen JGBazilevs YKvamsdal TZhang YKaspersen JHWaterloo K: Determination of wall tension in cerebral artery aneurysms by numerical simulation. Stroke 39:317231782008

    • Search Google Scholar
    • Export Citation
  • 56

    Kaazempur-Mofrad MRIsasi AGYounis HFChan RCHinton DPSukhova G: Characterization of the atherosclerotic carotid bifurcation using MRI, finite element modeling, and histology. Ann Biomed Eng 32:9329462004

    • Search Google Scholar
    • Export Citation
  • 57

    Kadohama TAkasaka NNishimura KHoshino YSasajima TSumpio BE: p38 Mitogen-activated protein kinase activation in endothelial cell is implicated in cell alignment and elongation induced by fluid shear stress. Endothelium 13:43502006

    • Search Google Scholar
    • Export Citation
  • 58

    Kapoor KSingh BDewan LI: Variations in the configuration of the circle of Willis. Anat Sci Int 83:961062008

  • 59

    Karino TGoldsmith HL: Particle flow behavior in models of branching vessels. II. Effects of branching angle and diameter ratio on flow patterns. Biorheology 22:871041985

    • Search Google Scholar
    • Export Citation
  • 60

    Kasuya HShimizu TNakaya KSasahara AHori TTakakura K: Angeles between A1 and A2 segments of the anterior cerebral artery visualized by three-dimensional computed tomographic angiography and association of anterior communicating artery aneurysms. Neurosurgery 45:89941999

    • Search Google Scholar
    • Export Citation
  • 61

    Kayembe KNSasahara MHazama F: Cerebral aneurysms and variations in the circle of Willis. Stroke 15:8468501984

  • 62

    Kilic TSohrabifar MKurtkaya OYildirim OElmaci IGünel M: Expression of structural proteins and angiogenic factors in normal arterial and unruptured and ruptured aneurysm walls. Neurosurgery 57:99710072005

    • Search Google Scholar
    • Export Citation
  • 63

    Kissela BMSauerbeck LWoo DKhoury JCarrozzella JPancioli A: Subarachnoid hemorrhage: a preventable disease with a heritable component. Stroke 33:132113262002

    • Search Google Scholar
    • Export Citation
  • 64

    Kleinstreuer C: Biofluid Dynamics: Principles and Selected Applications Boca Raton, FLCRC Press2006

  • 65

    Kondo SHashimoto NKikuchi HHazama FNagata IKataoka H: Apoptosis of medial smooth muscle cells in the development of saccular cerebral aneurysms in rats. Stroke 29:1811891998

    • Search Google Scholar
    • Export Citation
  • 66

    Kondo SHashimoto NKikuchi HHazama FNagata IKataoka H: Cerebral aneurysms arising at nonbranching sites. An experimental Study. Stroke 28:3984041997

    • Search Google Scholar
    • Export Citation
  • 67

    Korenaga RAndo JKosaki KIsshiki MTakada YKamiya A: Negative transcriptional regulation of the VCAM-1 gene by fluid shear stress in murine endothelial cells. Am J Physiol 273:C1506C15151997

    • Search Google Scholar
    • Export Citation
  • 68

    Krex DKönig IRZiegler ASchackert HKSchackert G: Extended single nucleotide polymorphism and haplotype analysis of the elastin gene in Caucasians with intracranial aneurysms provides evidence for racially/ethnically based differences. Cerebrovasc Dis 18:1041102004

    • Search Google Scholar
    • Export Citation
  • 69

    Ku DN: Blood flow in arteries. Annu Rev Fluid Mech 29:3994341997

  • 70

    Ku DNGiddens DPZarins CKGlagov S: Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5:2933021985

    • Search Google Scholar
    • Export Citation
  • 71

    Kuivaniemi HProckop DJWu YMadhatheri SLKleinert CEarley JJ: Exclusion of mutations in the gene for type III collagen (COL3A1) as a common cause of intracranial aneurysms or cervical artery dissections: results from sequence analysis of the coding sequences of type III collagen from 55 unrelated patients. Neurology 43:265226581993

    • Search Google Scholar
    • Export Citation
  • 72

    Lee RM: Morphology of cerebral arteries. Pharmacol Ther 66:1491731995

  • 73

    Lee SWAntiga LSpence JDSteinman DA: Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke 39:234123472008

    • Search Google Scholar
    • Export Citation
  • 74

    Li YSHaga JHChien S: Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38:194919712005

  • 75

    Libby PGeng YJAikawa MSchoenbeck UMach FClinton SK: Macrophages and atherosclerotic plaque stability. Curr Opin Lipidol 7:3303351996

    • Search Google Scholar
    • Export Citation
  • 76

    Lin MCAlmus-Jacobs FChen HHParry GCMackman NShyy JY: Shear stress induction of the tissue factor gene. J Clin Invest 99:7377441997

    • Search Google Scholar
    • Export Citation
  • 77

    Lum RMWiley LMBarakat AI: Influence of different forms of fluid shear stress on vascular endothelial TGF-beta1 mRNA expression. Int J Mol Med 5:6356412000

    • Search Google Scholar
    • Export Citation
  • 78

    Malek AIzumo S: Physiological fluid shear stress causes downregulation of endothelin-1 mRNA in bovine aortic endothelium. Am J Physiol 263:C389C3961992

    • Search Google Scholar
    • Export Citation
  • 79

    Malek AMJiang LLee ISessa WCIzumo SAlper SL: Induction of nitric oxide synthase mRNA by shear stress requires intracellular calcium and G-protein signals and is modulated by PI 3 kinase. Biochem Biophys Res Commun 254:2312421999

    • Search Google Scholar
    • Export Citation
  • 80

    Marshall IZhao SPapathanasopoulou PHoskins PXu Y: MRI and CFD studies of pulsatile flow in healthy and stenosed carotid bifurcation models. J Biomech 37:6796872004

    • Search Google Scholar
    • Export Citation
  • 81

    Masuda HZhuang YJSingh TMKawamura KMurakami MZarins CK: Adaptive remodeling of internal elastic lamina and endothelial lining during flow-induced arterial enlargement. Arterioscler Thromb Vasc Biol 19:229823071999

    • Search Google Scholar
    • Export Citation
  • 82

    Meng HSwartz DDWang ZHoi YKolega JMetaxa EM: A model system for mapping vascular responses to complex hemodynamics at arterial bifurcations in vivo. Neurosurgery 59:109411012006

    • Search Google Scholar
    • Export Citation
  • 83

    Meng HWang ZHoi YGao LMetaxa ESwartz DD: Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke 38:192419312007

    • Search Google Scholar
    • Export Citation
  • 84

    Metaxa EMeng HKaluvala SRSzymanski MPPaluch RAKolega J: Nitric oxide-dependent stimulation of endothelial cell proliferation by sustained high flow. Am J Physiol Heart Circ Physiol 295:H736H7422008

    • Search Google Scholar
    • Export Citation
  • 85

    Mohan SHamuro MSorescu GPKoyoma KSprague EAJo H: IκBα-dependent regulation of low-shear flow-induced NF-κB activity: role of nitric oxide. Am J Physiol Cell Physiol 284:C1039C10472003

    • Search Google Scholar
    • Export Citation
  • 86

    Mohan SMohan NSprague EA: Differential activation of NF-kappa B in human aortic endothelial cells conditioned to specific flow environments. Am J Physiol 273:C572C5781997

    • Search Google Scholar
    • Export Citation
  • 87

    Motomiya MKarino T: Flow patterns in the human carotid artery bifurcation. Stroke 15:50561984

  • 88

    Nagel TResnick NAtkinson WJDewey CF JrGimbrone MA Jr: Shear stress selectively upregulates intercellular adhesion molecule-1 expression in cultured human vascular endothelial cells. J Clin Invest 94:8858911994

    • Search Google Scholar
    • Export Citation
  • 89

    Nahed BVBydon MOzturk AKBilguvar KBayrakli FGunel M: Genetics of intracranial aneurysms. Neurosurgery 60:2132262007

  • 90

    Nguyen KTClark CDChancellor TJPapavassiliou DV: Carotid geometry effects on blood flow and on risk for vascular disease. J Biomech 41:11192008

    • Search Google Scholar
    • Export Citation
  • 91

    Oluwole BODu WMills ISumpio BE: Gene regulation by mechanical forces. Endothelium 5:85931997

  • 92

    Onda HKasuya HYoneyama TTakakura KHori TTakeda J: Genomewide-linkage and haplotype-association studies map intracranial aneurysm to chromosome 7q11. Am J Hum Genet 69:8048192001

    • Search Google Scholar
    • Export Citation
  • 93

    Osawa MMasuda MKusano KFujiwara K: Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule?. J Cell Biol 158:7737852002

    • Search Google Scholar
    • Export Citation
  • 94

    Osborn AG: Diagnostic Cerebral Angiography ed 2PhiladelphiaLippincott Williams & Wilkins1999

  • 95

    Oshima MKobayashi TTakagi K: Biosimulation and visualization: effect of cerebrovascular geometry on hemodynamics. Ann N Y Acad Sci 972:3373442002

    • Search Google Scholar
    • Export Citation
  • 96

    Oshima MTorii RKobayashi TTaniguchi NTakagi K: Finite element simulation of blood flow in the cerebral artery. Comput Methods Appl Mech Eng 191:6616712001

    • Search Google Scholar
    • Export Citation
  • 97

    Oyre SRinggaard SKozerke SPaaske WPErlandsen MBoesiger P: Accurate noninvasive quantitation of blood flow, cross-sectional lumen vessel area and wall shear stress by three-dimensional paraboloid modeling of magnetic resonance imaging velocity data. J Am Coll Cardiol 32:1281341998

    • Search Google Scholar
    • Export Citation
  • 98

    Painter PREdén PBengtsson HU: Pulsatile blood flow, shear force, energy dissipation and Murray's Law. Theor Biol Med Model 3:312006

    • Search Google Scholar
    • Export Citation
  • 99

    Prado CMRamos SGAlves-Filho JCElias J JrCunha FQRossi MA: Turbulent flow/low wall shear stress and stretch differentially affect aorta remodeling in rats. J Hypertens 24:5035152006

    • Search Google Scholar
    • Export Citation
  • 100

    Raghavan MLMa BHarbaugh RE: Quantified aneurysm shape and rupture risk. J Neurosurg 102:3553622005

  • 101

    Ravensbergen JKrijger JKHillen BHoogstraten HW: The influence of the angle of confluence on the flow in a vertebrobasilar junction model. J Biomech 29:2812991996

    • Search Google Scholar
    • Export Citation
  • 102

    Ravensbergen JKrijger JKVerdaasdonk ALHillen BHoogstraten HW: The influence of the blunting of the apex on the flow in a vertebro-basilar junction model. J Biomech Eng 119:1952051997

    • Search Google Scholar
    • Export Citation
  • 103

    Ravensbergen JRavensbergen JWKrijger JKHillen BHoogstraten HW: Localizing role of hemodynamics in atherosclerosis in several human vertebrobasilar junction geometries. Arterioscler Thromb Vasc Biol 18:7087161998

    • Search Google Scholar
    • Export Citation
  • 104

    Rhoton AL Jr: Aneurysms. Neurosurgery 51:4 SupplS121S1582002

  • 105

    Rhoton AL Jr: The cerebrum. Anatomy Neurosurgery 61:1 Suppl371192007

  • 106

    Riedel MRafflenbeul WLichtlen P: Ovarian sex steroids and atherosclerosis. Clin Investig 71:4064121993

  • 107

    Rindt CCSteenhoven AA: Unsteady flow in a rigid 3-D model of the carotid artery bifurcation. J Biomech Eng 118:90961996

  • 108

    Rizzoni DPorteri ECastellano MBettoni GMuiesan MLTiberio G: Endothelial dysfunction in hypertension is independent from the etiology and from vascular structure. Hypertension 31:3353411998

    • Search Google Scholar
    • Export Citation
  • 109

    Ruigrok YMRinkel GJ: Genetics of intracranial aneurysms. Stroke 39:104910552008

  • 110

    Sadamasa NNozaki KHashimoto N: Disruption of gene for inducible nitric oxide synthase reduces progression of cerebral aneurysms. Stroke 34:298029842003

    • Search Google Scholar
    • Export Citation
  • 111

    Samijo SKWilligers JMBarkhuysen RKitslaar PJReneman RSBrands PJ: Wall shear stress in the human common carotid artery as function of age and gender. Cardiovasc Res 39:5155221998

    • Search Google Scholar
    • Export Citation
  • 112

    Schirmer CMMalek AM: Estimation of wall shear stress dynamic fluctuations in intracranial atherosclerotic lesions using computational fluid dynamics. Neurosurgery 63:3263352008

    • Search Google Scholar
    • Export Citation
  • 113

    Schirmer CMMalek AM: Prediction of complex flow patterns in intracranial atherosclerotic disease using computational fluid dynamics. Neurosurgery 61:8428522007

    • Search Google Scholar
    • Export Citation
  • 114

    Schulz UGRothwell PM: Major variation in carotid bifurcation anatomy: a possible risk factor for plaque development?. Stroke 32:252225292001

    • Search Google Scholar
    • Export Citation
  • 115

    Schulz UGRothwell PM: Sex differences in carotid bifurcation anatomy and the distribution of atherosclerotic plaque. Stroke 32:152515312001

    • Search Google Scholar
    • Export Citation
  • 116

    Sharma RYellowley CECivelek MAinslie KHodgson LTarbell JM: Intracellular calcium changes in rat aortic smooth muscle cells in response to fluid flow. Ann Biomed Eng 30:3713782002

    • Search Google Scholar
    • Export Citation
  • 117

    Shojima MOshima MTakagi KTorii RHayakawa MKatada K: Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 35:250025052004

    • Search Google Scholar
    • Export Citation
  • 118

    Shojima MOshima MTakagi KTorii RNagata KShirouzu I: Role of the bloodstream impacting force and the local pressure elevation in the rupture of cerebral aneurysms. Stroke 36:193319382005

    • Search Google Scholar
    • Export Citation
  • 119

    Silacci PFormentin KBouzourène KDaniel FBrunner HRHayoz D: Unidirectional and oscillatory shear stress differentially modulate NOS III gene expression. Nitric Oxide 4:47562000

    • Search Google Scholar
    • Export Citation
  • 120

    Steinman DAMilner JSNorley CJLownie SPHoldsworth DW: Image-based computational simulation of flow dynamics in a giant intracranial aneurysm. AJNR Am J Neuroradiol 24:5595662003

    • Search Google Scholar
    • Export Citation
  • 121

    Sumpio BE: Hemodynamic forces and the biology of the endothelium: signal transduction pathways in endothelial cells subjected to physical forces in vitro. J Vasc Surg 13:7447461991

    • Search Google Scholar
    • Export Citation
  • 122

    Sumpio BEYun SCordova ACHaga MZhang JKoh Y: MAPKs (ERK1/2, p38) and AKT can be phosphorylated by shear stress independently of platelet endothelial cell adhesion molecule-1 (CD31) in vascular endothelial cells. J Biol Chem 280:11185111912005

    • Search Google Scholar
    • Export Citation
  • 123

    Tateshima SMurayama YVillablanca JPMorino TNomura KTanishita K: In vitro measurement of fluid-induced wall shear stress in unruptured cerebral aneurysms harboring blebs. Stroke 34:1871922003

    • Search Google Scholar
    • Export Citation
  • 124

    Thomas JBAntiga LChe SLMilner JSSteinman DASpence JD: Variation in the carotid bifurcation geometry of young versus older adults: implications for geometric risk of atherosclerosis. Stroke 36:245024562005

    • Search Google Scholar
    • Export Citation
  • 125

    Thomas JBMilner JSSteinman DA: On the influence of vessel planarity on local hemodynamics at the human carotid bifurcation. Biorheology 39:4434482002

    • Search Google Scholar
    • Export Citation
  • 126

    Thubrikar MJRobicsek F: Pressure-induced arterial wall stress and atherosclerosis. Ann Thorac Surg 59:159416031995

  • 127

    Toda MYamamoto KShimizu NObi SKumagaya SIgarashi T: Differential gene responses in endothelial cells exposed to a combination of shear stress and cyclic stretch. J Biotechnol 133:2392442008

    • Search Google Scholar
    • Export Citation
  • 128

    Topper JNCai JFalb DGimbrone MA Jr: Identification of vascular endothelial genes differentially responsive to fluid mechanical stimuli: cyclooxygenase-2, manganese superoxide dismutase, and endothelial cell nitric oxide synthase are selectively up-regulated by steady laminar shear stress. Proc Natl Acad Sci U S A 93:10417104221996

    • Search Google Scholar
    • Export Citation
  • 129

    Torres VEPirson YWiebers DO: Cerebral aneurysms. N Engl J Med 355:270327052006. (Letter)

  • 130

    van den Beld AWBots MLJanssen JAPols HALamberts SWGrobbee DE: Endogenous hormones and carotid atherosclerosis in elderly men. Am J Epidemiol 157:25312003

    • Search Google Scholar
    • Export Citation
  • 131

    von Eckardstein A: Risk factors for atherosclerotic vascular disease. Handb Exp Pharmacol 170711052005

  • 132

    Vouyouka AGPowell RJRicotta JChen HDudrick DJSawmiller CJ: Ambient pulsatile pressure modulates endothelial cell proliferation. J Mol Cell Cardiol 30:6096151998

    • Search Google Scholar
    • Export Citation
  • 133

    Walford GLoscalzo J: Nitric oxide in vascular biology. J Thromb Haemost 1:211221182003

  • 134

    Wang ZKolega JHoi YGao LSwartz DDLevy EI: Molecular alterations associated with aneurysmal remodeling are localized in the high hemodynamic stress region of a created carotid bifurcation. Neurosurgery 65:1691782009

    • Search Google Scholar
    • Export Citation
  • 135

    Weir B: Unruptured intracranial aneurysms: a review. J Neurosurg 96:3422002

  • 136

    Wetzel SMeckel SFrydrychowicz ABonati LRadue EWScheffler K: In vivo assessment and visualization of intracranial arterial hemodynamics with flow-sensitized 4D MR imaging at 3T. AJNR Am J Neuroradiol 28:4334382007

    • Search Google Scholar
    • Export Citation
  • 137

    White CRFrangos JA: The shear stress of it all: the cell membrane and mechanochemical transduction. Philos Trans R Soc Lond B Biol Sci 362:145914672007

    • Search Google Scholar
    • Export Citation
  • 138

    Wityk RJLehman DKlag MCoresh JAhn HLitt B: Race and sex differences in the distribution of cerebral atherosclerosis. Stroke 27:197419801996

    • Search Google Scholar
    • Export Citation
  • 139

    Wong LK: Global burden of intracranial atherosclerosis. Int J Stroke 1:1581592006

  • 140

    Yamashita SIsoda HHirano MTakeda HInagawa STakehara Y: Visualization of hemodynamics in intracranial arteries using time-resolved three-dimensional phase-contrast MRI. J Magn Reson Imaging 25:4734782007

    • Search Google Scholar
    • Export Citation
  • 141

    Younis HFKaazempur-Mofrad MRChan RCIsasi AGHinton DPChau AH: Hemodynamics and wall mechanics in human carotid bifurcation and its consequences for atherogenesis: investigation of inter-individual variation. Biomech Model Mechanobiol 3:17322004

    • Search Google Scholar
    • Export Citation
  • 142

    Zarins CKGiddens DPBharadvaj BKSottiurai VSMabon RFGlagov S: Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res 53:5025141983

    • Search Google Scholar
    • Export Citation
  • 143

    Ziegler TBouzourène KHarrison VJBrunner HRHayoz D: Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arterioscler Thromb Vasc Biol 18:6866921998

    • Search Google Scholar
    • Export Citation
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