Are hemodynamics responsible for inflammatory changes in venous vessel walls? A quantitative study of wall-enhancing intracranial arteriovenous malformation draining veins

Janneck Stahl Research Campus STIMULATE, University of Magdeburg, Germany;
Departments of Fluid Dynamics and Technical Flows and

Search for other papers by Janneck Stahl in
Current site
Google Scholar
PubMed
Close
 MSc
,
Laura Stone McGuire Department of Neurosurgery, University of Illinois, Chicago, Illinois; and

Search for other papers by Laura Stone McGuire in
Current site
Google Scholar
PubMed
Close
 MD
,
Mark Rizko Department of Neurosurgery, University of Illinois, Chicago, Illinois; and

Search for other papers by Mark Rizko in
Current site
Google Scholar
PubMed
Close
 MD
,
Sylvia Saalfeld Research Campus STIMULATE, University of Magdeburg, Germany;
Department of Computer Science and Automation, Ilmenau University of Technology, Ilmenau, Germany

Search for other papers by Sylvia Saalfeld in
Current site
Google Scholar
PubMed
Close
 PhD
,
Philipp Berg Research Campus STIMULATE, University of Magdeburg, Germany;
Medical Engineering, University of Magdeburg, Germany;

Search for other papers by Philipp Berg in
Current site
Google Scholar
PubMed
Close
 PhD
, and
Ali Alaraj Department of Neurosurgery, University of Illinois, Chicago, Illinois; and

Search for other papers by Ali Alaraj in
Current site
Google Scholar
PubMed
Close
 MD
Restricted access

Purchase Now

USD  $45.00

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

USD  $536.00

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

USD  $636.00
USD  $45.00
USD  $536.00
USD  $636.00
Print or Print + Online Sign in

OBJECTIVE

Signal enhancement of vascular walls on vessel wall MRI might be a biomarker for inflammation. It has been theorized that contrast enhancement on vessel wall imaging (VWI) in draining veins of intracranial arteriovenous malformations (AVMs) may be associated with disease progression and development of venous stenosis. The aim of this study was to investigate the relationship between vessel wall enhancement and hemodynamic stressors along AVM draining veins.

METHODS

Eight AVM patients with 15 draining veins visualized on VWI were included. Based on MR venography data, patient-specific 3D surface models of the venous anatomy distal to the nidus were segmented. The enhanced vascular wall regions were manually extracted and mapped onto the venous surface models after registration of image data. Using image-based blood flow simulations applying patient-specific boundary conditions based on phase-contrast quantitative MR angiography, hemodynamics were investigated in the enhanced vasculature. For the shear-related parameters, time-averaged wall shear stress (TAWSS), oscillatory shear index (OSI), and relative residence time (RRT) were calculated. Velocity, oscillatory velocity index (OVI), and vorticity were extracted for the intraluminal flow-related hemodynamics.

RESULTS

Visual observations demonstrated overlap of enhancement with local lower shear stresses resulting from decreased velocities. Thus, higher RRT values were measured in the enhanced areas. Furthermore, nonenhancing draining veins showed on average slightly higher flow velocities and TAWSS. Significant decreases of 55% (p = 0.03) for TAWSS and of 24% (p = 0.03) for vorticity were identified in enhanced areas compared with near distal and proximal domains. Velocity magnitude in the enhanced region showed a nonsignificant decrease of 14% (p = 0.06). Furthermore, increases were present in the OSI (32%, p = 0.3), RRT (25%, p = 0.15), and OVI (26%, p = 0.3) in enhanced vessel sections, although the differences were not significant.

CONCLUSIONS

This novel multimodal investigation of hemodynamics in AVM draining veins allows for precise prediction of occurring shear- and flow-related phenomena in enhanced vessel walls. These findings may suggest low shear to be a local predisposing factor for venous stenosis in AVMs.

ABBREVIATIONS

AVM = arteriovenous malformation; IA = intracranial aneurysm; MRV = MR venography; OSI = oscillatory shear index; OVI = oscillatory velocity index; QMRA = quantitative MR angiography; RRT = relative residence time; TAWSS = time-averaged WSS; VWI = vessel wall imaging; WSS = wall shear stress.
  • Collapse
  • Expand
  • 1

    Asif K, Leschke J, Lazzaro MA. Cerebral arteriovenous malformation diagnosis and management. Semin Neurol. 2013;33(5):468475.

  • 2

    Ozpinar A, Mendez G, Abla AA. Epidemiology, genetics, pathophysiology, and prognostic classifications of cerebral arteriovenous malformations. Handb Clin Neurol. 2017;143:513.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Choi JH, Mast H, Sciacca RR, et al. Clinical outcome after first and recurrent hemorrhage in patients with untreated brain arteriovenous malformation. Stroke. 2006;37(5):12431247.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Can A, Gross BA, Du R. The natural history of cerebral arteriovenous malformations. Handb Clin Neurol. 2017;143:1524.

  • 5

    Shaligram SS, Winkler E, Cooke D, Su H. Risk factors for hemorrhage of brain arteriovenous malformation. CNS Neurosci Ther. 2019;25(10):10851095.

  • 6

    Alqadi M, Brunozzi D, Linninger A, Amin-Hanjani S, Charbel FT, Alaraj A. Cerebral arteriovenous malformation venous stenosis is associated with hemodynamic changes at the draining vein-venous sinus junction. Med Hypotheses. 2019;123:8688.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Young CC, Bonow RH, Barros G, Mossa-Basha M, Kim LJ, Levitt MR. Magnetic resonance vessel wall imaging in cerebrovascular diseases. Neurosurg Focus. 2019;47(6):E4.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    de Havenon A, Chung L, Park M, Mossa-Basha M. Intracranial vessel wall MRI: a review of current indications and future applications. Neurovasc Imaging. 2016;2(1):10.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Matouk CC, Mandell DM, Günel M, et al. Vessel wall magnetic resonance imaging identifies the site of rupture in patients with multiple intracranial aneurysms: proof of principle. Neurosurgery. 2013;72(3):492496.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Larsen N, von der Brelie C, Trick D, et al. Vessel wall enhancement in unruptured intracranial aneurysms: an indicator for higher risk of rupture? High-resolution MR imaging and correlated histologic findings. AJNR Am J Neuroradiol. 2018;39(9):16171621.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Swiatek VM, Neyazi B, Roa JA, et al. Aneurysm wall enhancement is associated with decreased intrasaccular IL-10 and morphological features of instability. Neurosurgery. 2021;89(4):664671.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Wu XB, Zhong JL, Wang SW, et al. Circumferential wall enhancement with contrast ratio measurement in unruptured intracranial aneurysm for aneurysm instability. Brain Behav. 2022;12(5):e2568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zhong W, Su W, Li T, et al. Aneurysm wall enhancement in unruptured intracranial aneurysms: a histopathological evaluation. J Am Heart Assoc. 2021;10(2):e018633.

  • 14

    McGuire LS, Rizko M, Brunozzi D, Charbel FT, Alaraj A. Vessel wall imaging and quantitative flow assessment in arteriovenous malformations: a feasibility study. Interv Neuroradiol. Published online December 5, 2022. doi:10.1177/15910199221143189

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Petridis AK, Dibue-Adjei M, Cornelius JF, et al. Contrast enhancement of vascular walls of intracranial high flow malformations in black blood MRI indicates high inflammatory activity. Chin Neurosurg J. 2018;4:13.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Eisenmenger LB, Junn JC, Cooke D, et al. Presence of vessel wall hyperintensity in unruptured arteriovenous malformations on vessel wall magnetic resonance imaging: pilot study of AVM vessel wall "enhancement". Front Neurosci. 2021;15:697432.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Kaneko N, Ullman H, Ali F, et al. In vitro modeling of human brain arteriovenous malformation for endovascular simulation and flow analysis. World Neurosurg. 2020;141:e873e879.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Takeda Y, Kin T, Sekine T, et al. Hemodynamic analysis of cerebral AVMs with 3D phase-contrast MR imaging. AJNR Am J Neuroradiol. 2021;42(12):21382145.

  • 19

    Alexander MD, Cooke DL, Nelson J, et al. Association between venous angioarchitectural features of sporadic brain arteriovenous malformations and intracranial hemorrhage. AJNR Am J Neuroradiol. 2015;36(5):949952.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Alaraj A, Amin-Hanjani S, Shakur SF, et al. Quantitative assessment of changes in cerebral arteriovenous malformation hemodynamics after embolization. Stroke. 2015;46(4):942947.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Guglielmi G. Analysis of the hemodynamic characteristics of brain arteriovenous malformations using electrical models: baseline settings, surgical extirpation, endovascular embolization, and surgical bypass. Neurosurgery. 2008;63(1):111.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Sheikh MAA, Shuib AS, Mohyi MHH. A review of hemodynamic parameters in cerebral aneurysm. Interdiscip Neurosurg. 2020;22:100716.

  • 23

    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):18491857.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Riccardello GJ Jr, Shastri DN, Changa AR, et al. Influence of relative residence time on side-wall aneurysm inception. Neurosurgery. 2018;83(3):574581.

  • 25

    Roberts GS, Peret A, Jonaitis EM, et al. Normative cerebral hemodynamics in middle-aged and older adults using 4D flow MRI: initial analysis of vascular aging. Radiology. 2023;307(3):e222685.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Steinman DA, Gounis MJ, Levitt MR. You’re so vein, you probably think this model’s about you: opportunities and challenges for computational fluid dynamics in cerebral venous disease. J Neurointerv Surg. 2023;15(7):621622.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Frösen J, Tulamo R, Paetau A, et al. Saccular intracranial aneurysm: pathology and mechanisms. Acta Neuropathol. 2012;123(6):773786.

  • 28

    Traub O, Berk BC. Laminar shear stress: mechanisms by which endothelial cells transduce an atheroprotective force. Arterioscler Thromb Vasc Biol. 1998;18(5):677685.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    de Castro-Afonso LH, Vanzim JR, Trivelato FP. et al. Association between draining vein diameters and intracranial arteriovenous malformation hemorrhage: a multicentric retrospective study. Neuroradiology. 2020;62(11):14971505.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Pravdivtseva MS, Gaidzik F, Berg P, et al. Pseudo-enhancement in intracranial aneurysms on black-blood MRI: effects of flow rate, spatial resolution, and additional flow suppression. J Magn Reson Imaging. 2021;54(3):888901.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Gaidzik F, Pravdivtseva M, Larsen N, Jansen O, Hövener JB, Berg P. Luminal enhancement in intracranial aneurysms: fact or feature? A quantitative multimodal flow analysis. Int J CARS. 2021;16(11):19992008.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Cornelissen BMW, Leemans EL, Slump CH, Marquering HA, Majoie CBLM, van den Berg R. Vessel wall enhancement of intracranial aneurysms: fact or artifact?. Neurosurg Focus. 2019;47(1):E18.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Voß S, Glaßer S, Hoffmann T, et al. Fluid-structure simulations of a ruptured intracranial aneurysm: constant versus patient-specific wall thickness. Comput Math Methods Med. 2016;2016:9854539.

    • PubMed
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 1980 1980 1980
Full Text Views 50 50 50
PDF Downloads 78 78 78
EPUB Downloads 0 0 0