Computational fluid dynamics modeling of symptomatic intracranial atherosclerosis may predict risk of stroke recurrence

Xinyi Leng, Fabien Scalzo, Hing Lung Ip, Mark Johnson, Albert K Fong, Florence S Y Fan, Xiangyan Chen, Yannie O Y Soo, Zhongrong Miao, Liping Liu, Edward Feldmann, Thomas W H Leung, David S Liebeskind, Ka Sing Wong, Xinyi Leng, Fabien Scalzo, Hing Lung Ip, Mark Johnson, Albert K Fong, Florence S Y Fan, Xiangyan Chen, Yannie O Y Soo, Zhongrong Miao, Liping Liu, Edward Feldmann, Thomas W H Leung, David S Liebeskind, Ka Sing Wong

Abstract

Background: Patients with symptomatic intracranial atherosclerosis (ICAS) of ≥ 70% luminal stenosis are at high risk of stroke recurrence. We aimed to evaluate the relationships between hemodynamics of ICAS revealed by computational fluid dynamics (CFD) models and risk of stroke recurrence in this patient subset.

Methods: Patients with a symptomatic ICAS lesion of 70-99% luminal stenosis were screened and enrolled in this study. CFD models were reconstructed based on baseline computed tomographic angiography (CTA) source images, to reveal hemodynamics of the qualifying symptomatic ICAS lesions. Change of pressures across a lesion was represented by the ratio of post- and pre-stenotic pressures. Change of shear strain rates (SSR) across a lesion was represented by the ratio of SSRs at the stenotic throat and proximal normal vessel segment, similar for the change of flow velocities. Patients were followed up for 1 year.

Results: Overall, 32 patients (median age 65; 59.4% males) were recruited. The median pressure, SSR and velocity ratios for the ICAS lesions were 0.40 (-2.46-0.79), 4.5 (2.2-20.6), and 7.4 (5.2-12.5), respectively. SSR ratio (hazard ratio [HR] 1.027; 95% confidence interval [CI], 1.004-1.051; P = 0.023) and velocity ratio (HR 1.029; 95% CI, 1.002-1.056; P = 0.035) were significantly related to recurrent territorial ischemic stroke within 1 year by univariate Cox regression, respectively with the c-statistics of 0.776 (95% CI, 0.594-0.903; P = 0.014) and 0.776 (95% CI, 0.594-0.903; P = 0.002) in receiver operating characteristic analysis.

Conclusions: Hemodynamics of ICAS on CFD models reconstructed from routinely obtained CTA images may predict subsequent stroke recurrence in patients with a symptomatic ICAS lesion of 70-99% luminal stenosis.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Evaluation of computational fluid dynamics…
Figure 1. Evaluation of computational fluid dynamics model of an atherosclerotic lesion of left middle cerebral artery.
A: Post- and pre-stenotic pressures were measured using spherical volumes-of-interest (VOI, double arrows) at the first anatomically normal diameters distal (VOI 1) and proximal (VOI 2) to the lesion, respectively. The pressure ratio was calculated by dividing the mean pressure at VOI 1 by the mean pressure at VOI 2. B: Shear strain rates (SSR) were respectively measured at the stenotic throat (cut-plane 1) and at the first anatomically normal diameter (cut-plane 2) proximal to the lesion, by using cut-planes perpendicular to the direction of blood flow (arrow). The SSR ratio was calculated by dividing the SSR averaged over cut-plane 1 by the SSR averaged over cut-plane 2. C: Velocities were similarly measured (arrow) as with the SSRs, and the velocity ratio was similarly calculated as with the SSR ratio.
Figure 2. Kaplan-Meier curves for the cumulative…
Figure 2. Kaplan-Meier curves for the cumulative probabilities of recurrent ischemic stroke in the territory (SIT) of the stenotic artery within 1 year after ictus, according to the shear strain rate (SSR) ratio (≥ or
Intracranial atherosclerotic lesions with a SSR ratio of ≥ median may relate to a higher risk of SIT, compared with lesions with a SSR ratio of

Figure 3. Kaplan-Meier curves for the cumulative…

Figure 3. Kaplan-Meier curves for the cumulative probabilities of recurrent ischemic stroke in the territory…

Figure 3. Kaplan-Meier curves for the cumulative probabilities of recurrent ischemic stroke in the territory (SIT) of the stenotic artery within 1 year after ictus, according to the velocity ratio (≥ or
Intracranial atherosclerotic lesions with a velocity ratio of ≥ median may relate to a higher risk of SIT, compared with lesions with a velocity ratio of

Figure 4. Receiver operating characteristic curves for…

Figure 4. Receiver operating characteristic curves for shear strain rate ratio (left) and velocity ratio…

Figure 4. Receiver operating characteristic curves for shear strain rate ratio (left) and velocity ratio (right) to predict recurrent ischemic stroke in the territory of the qualifying artery.
SIT indicates recurrent ischemic stroke in the territory of the qualifying artery; AUC, area under curve.
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References
Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, Hertzberg VS, et al. (2005) Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med 352: 1305–1316. - PubMed Kasner SE, Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, et al. (2006) Predictors of ischemic stroke in the territory of a symptomatic intracranial arterial stenosis. Circulation 113: 555–563. - PubMed Chimowitz MI, Lynn MJ, Derdeyn CP, Turan TN, Fiorella D, et al. (2011) Stenting versus aggressive medical therapy for intracranial arterial stenosis. N Engl J Med 365: 993–1003. - PMC - PubMed Derdeyn CP, Chimowitz MI, Lynn MJ, Fiorella D, Turan TN, et al. (2014) Aggressive medical treatment with or without stenting in high-risk patients with intracranial artery stenosis (SAMMPRIS): the final results of a randomised trial. Lancet 383: 333–341. - PMC - PubMed Furie KL, Kasner SE, Adams RJ, Albers GW, Bush RL, et al. (2011) Guidelines for the prevention of stroke in patients with stroke or transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42: 227–276. - PubMed
Show all 28 references
Publication types
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
MeSH terms
Intracranial Arteriosclerosis / complications*
Intracranial Arteriosclerosis / physiopathology*
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Figure 3. Kaplan-Meier curves for the cumulative…
Figure 3. Kaplan-Meier curves for the cumulative probabilities of recurrent ischemic stroke in the territory (SIT) of the stenotic artery within 1 year after ictus, according to the velocity ratio (≥ or
Intracranial atherosclerotic lesions with a velocity ratio of ≥ median may relate to a higher risk of SIT, compared with lesions with a velocity ratio of

Figure 4. Receiver operating characteristic curves for…

Figure 4. Receiver operating characteristic curves for shear strain rate ratio (left) and velocity ratio…

Figure 4. Receiver operating characteristic curves for shear strain rate ratio (left) and velocity ratio (right) to predict recurrent ischemic stroke in the territory of the qualifying artery.
SIT indicates recurrent ischemic stroke in the territory of the qualifying artery; AUC, area under curve.
Figure 4. Receiver operating characteristic curves for…
Figure 4. Receiver operating characteristic curves for shear strain rate ratio (left) and velocity ratio (right) to predict recurrent ischemic stroke in the territory of the qualifying artery.
SIT indicates recurrent ischemic stroke in the territory of the qualifying artery; AUC, area under curve.

References

    1. Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, Hertzberg VS, et al. (2005) Comparison of warfarin and aspirin for symptomatic intracranial arterial stenosis. N Engl J Med 352: 1305–1316.
    1. Kasner SE, Chimowitz MI, Lynn MJ, Howlett-Smith H, Stern BJ, et al. (2006) Predictors of ischemic stroke in the territory of a symptomatic intracranial arterial stenosis. Circulation 113: 555–563.
    1. Chimowitz MI, Lynn MJ, Derdeyn CP, Turan TN, Fiorella D, et al. (2011) Stenting versus aggressive medical therapy for intracranial arterial stenosis. N Engl J Med 365: 993–1003.
    1. Derdeyn CP, Chimowitz MI, Lynn MJ, Fiorella D, Turan TN, et al. (2014) Aggressive medical treatment with or without stenting in high-risk patients with intracranial artery stenosis (SAMMPRIS): the final results of a randomised trial. Lancet 383: 333–341.
    1. Furie KL, Kasner SE, Adams RJ, Albers GW, Bush RL, et al. (2011) Guidelines for the prevention of stroke in patients with stroke or transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42: 227–276.
    1. Bodle JD, Feldmann E, Swartz RH, Rumboldt Z, Brown T, et al. (2013) High-resolution magnetic resonance imaging: an emerging tool for evaluating intracranial arterial disease. Stroke 44: 287–292.
    1. Donahue MJ, Strother MK, Hendrikse J (2012) Novel MRI approaches for assessing cerebral hemodynamics in ischemic cerebrovascular disease. Stroke 43: 903–915.
    1. Liebeskind DS, Cotsonis GA, Saver JL, Lynn MJ, Turan TN, et al. (2011) Collaterals dramatically alter stroke risk in intracranial atherosclerosis. Ann Neurol 69: 963–974.
    1. Tonino PA, De Bruyne B, Pijls NH, Siebert U, Ikeno F, et al. (2009) Fractional flow reserve versus angiography for guiding percutaneous coronary intervention. N Engl J Med 360: 213–224.
    1. Taylor CA, Fonte TA, Min JK (2013) Computational fluid dynamics applied to cardiac computed tomography for noninvasive quantification of fractional flow reserve. Scientific basis. J Am Coll Cardiol 61: 2233–2241.
    1. Leng X, Scalzo F, Fong A, Johnson M, Ip HL, et al. (2013) Computational fluid dynamics of computed tomography angiography to detect the hemodynamic impact of intracranial atherosclerosis. Cerebrovasc Dis 36: P48.
    1. De Bruyne B, Sarma J (2008) Fractional flow reserve: a review. Heart 94: 949–959.
    1. Schirmer CM, Malek AM (2007) Prediction of complex flow patterns in intracranial atherosclerotic disease using computational fluid dynamics. Neurosurgery 61: 842–852.
    1. Ruggeri ZM, Orje JN, Habermann R, Federici AB, Reininger AJ (2006) Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 108: 1903–1910.
    1. Maxwell MJ, Westein E, Nesbitt WS, Giuliano S, Dopheide SM, et al. (2007) Identification of a 2-stage platelet aggregation process mediating shear-dependent thrombus formation. Blood 109: 566–576.
    1. Nesbitt WS, Westein E, Tovar-Lopez FJ, Tolouei E, Mitchell A, et al. (2009) A shear gradient-dependent platelet aggregation mechanism drives thrombus formation. Nat Med 15: 665–673.
    1. Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Stone PH, et al. (2007) Risk stratification of individual coronary lesions using local endothelial shear stress: a new paradigm for managing coronary artery disease. Curr Opin Cardiol 22: 552–564.
    1. Wentzel JJ, Chatzizisis YS, Gijsen FJH, Giannoglou GD, Feldman CL, et al. (2012) Endothelial shear stress in the evolution of coronary atherosclerotic plaque and vascular remodelling: current understanding and remaining questions. Cardiovasc Res 96: 234–243.
    1. Antiga L, Piccinelli M, Botti L, Ene-Iordache B, Remuzzi A, et al. (2008) An image-based modeling framework for patient-specific computational hemodynamics. Med Biol Eng Comput 46: 1097–1112.
    1. Suh DC, Ko YB, Park ST, Yoon K, Lim OK, et al. (2011) Computational flow dynamics of the severe M1 stenosis before and after stenting. Neurointervention 6: 13–16.
    1. Sorimachi T, Morita K, Ito Y, Fujii Y (2011) Blood pressure measurement in the artery proximal and distal to an intra-arterial embolus during thrombolytic therapy. J Neurointerv Surg 3: 43–46.
    1. Batchelor GK (1967) An introduction to fluid dynamics. Cambridge: Cambridge University Press.
    1. Jung JM, Kang DW, Yu KH, Koo JS, Lee JH, et al. (2012) Predictors of recurrent stroke in patients with symptomatic intracranial arterial stenosis. Stroke 43: 2785–2787.
    1. Leng X, Wong KS, Liebeskind DS (2014) Evaluating intracranial atherosclerosis rather than intracranial stenosis. Stroke 45: 645–651.
    1. Kwon SU, Hong KS, Kang DW, Park JM, Lee JH, et al. (2011) Efficacy and safety of combination antiplatelet therapies in patients with symptomatic intracranial atherosclerotic stenosis. Stroke 42: 2883–2890.
    1. Scalzo F, Hao Q, Walczak AM, Hu X, Hoi Y, et al.. (2010) Computational hemodynamics in intracranial vessels reconstructed from biplane angiograms. In: Bebis G, Boyle R, Parvin B, Koracin D, Chung R, et al..., editors. Advances in Visual Computing, Part III: Springer Berlin Heidelberg. 359–367.
    1. Liebeskind DS, Feldmann E (2013) Fractional flow in cerebrovascular disorders. Interv Neurol 1: 87–99.
    1. van Laar PJ, van der Grond J, Hendrikse J (2008) Brain perfusion territory imaging: Methods and clinical applications of selective arterial spin-labeling MR imaging. Radiology 246: 354–364.

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