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Published in: Journal of Cardiovascular Magnetic Resonance 1/2020

Open Access 01-12-2020 | Arterial Occlusive Disease | Research

Carotid geometry is an independent predictor of wall thickness – a 3D cardiovascular magnetic resonance study in patients with high cardiovascular risk

Authors: Christoph Strecker, Axel Joachim Krafft, Lilli Kaufhold, Markus Hüllebrandt, Susanne Weber, Ute Ludwig, Martin Wolkewitz, Anja Hennemuth, Jürgen Hennig, Andreas Harloff

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2020

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Abstract

Background

The posterior wall of the proximal internal carotid artery (ICA) is the predilection site for the development of stenosis. To optimally prevent stroke, identification of new risk factors for plaque progression is of high interest. Therefore, we studied the impact of carotid geometry and wall shear stress on cardiovascular magnetic resonance (CMR)-depicted wall thickness in the ICA of patients with high cardiovascular disease risk.

Methods

One hundred twenty-one consecutive patients ≥50 years with hypertension, ≥1 additional cardiovascular risk factor and ICA plaque ≥1.5 mm thickness and < 50% stenosis were prospectively included. High-resolution 3D-multi-contrast (time of flight, T1, T2, proton density) and 4D flow CMR were performed for the assessment of morphological (bifurcation angle, ICA/common carotid artery (CCA) diameter ratio, tortuosity, and wall thickness) and hemodynamic parameters (absolute/systolic wall shear stress (WSS), oscillatory shear index (OSI)) in 242 carotid bifurcations.

Results

We found lower absolute/systolic WSS, higher OSI and increased wall thickness in the posterior compared to the anterior wall of the ICA bulb (p < 0.001), whereas this correlation disappeared in ≥10% stenosis. Higher carotid tortuosity (regression coefficient = 0.764; p < 0.001) and lower ICA/CCA diameter ratio (regression coefficient = − 0.302; p < 0.001) were independent predictors of increased wall thickness even after adjustment for cardiovascular risk factors. This association was not found for bifurcation angle, WSS or OSI in multivariate regression analysis.

Conclusions

High carotid tortuosity and low ICA diameter were independent predictors for wall thickness of the ICA bulb in this cross-sectional study, whereas this association was not present for WSS or OSI. Thus, consideration of geometric parameters of the carotid bifurcation could be helpful to identify patients at increased risk of carotid plaque generation. However, this association and the potential benefit of WSS measurement need to be further explored in a longitudinal study.
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Literature
1.
go back to reference Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1998;339(20):1415–25.PubMed Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1998;339(20):1415–25.PubMed
2.
go back to reference Selwaness M, van den Bouwhuijsen Q, van Onkelen RS, Hofman A, Franco OH, van der Lugt A, et al. Atherosclerotic plaque in the left carotid artery is more vulnerable than in the right. Stroke. 2014;45(11):3226–30.PubMed Selwaness M, van den Bouwhuijsen Q, van Onkelen RS, Hofman A, Franco OH, van der Lugt A, et al. Atherosclerotic plaque in the left carotid artery is more vulnerable than in the right. Stroke. 2014;45(11):3226–30.PubMed
3.
go back to reference Morbiducci U, Kok AM, Kwak BR, Stone PH, Steinman DA, Wentzel JJ. Atherosclerosis at arterial bifurcations: evidence for the role of haemodynamics and geometry. Thromb Haemost. 2016;115(3):484–92.PubMed Morbiducci U, Kok AM, Kwak BR, Stone PH, Steinman DA, Wentzel JJ. Atherosclerosis at arterial bifurcations: evidence for the role of haemodynamics and geometry. Thromb Haemost. 2016;115(3):484–92.PubMed
4.
go back to reference Sitzer M, Puac D, Buehler A, Steckel DA, von Kegler S, Markus HS, et al. Internal carotid artery angle of origin: a novel risk factor for early carotid atherosclerosis. Stroke. 2003;34(4):950–5.PubMed Sitzer M, Puac D, Buehler A, Steckel DA, von Kegler S, Markus HS, et al. Internal carotid artery angle of origin: a novel risk factor for early carotid atherosclerosis. Stroke. 2003;34(4):950–5.PubMed
5.
go back to reference Stensland-Bugge E, Bønaa KH, Joakimsen O, Njølstad I. Sex differences in the relationship of risk factors to subclinical carotid atherosclerosis measured 15 years later: the Tromsø study. Stroke. 2000;31(3):574–81.PubMed Stensland-Bugge E, Bønaa KH, Joakimsen O, Njølstad I. Sex differences in the relationship of risk factors to subclinical carotid atherosclerosis measured 15 years later: the Tromsø study. Stroke. 2000;31(3):574–81.PubMed
6.
go back to reference Wagenknecht LE, Langefeld CD, Freedman BI, Carr JJ, Bowden DW. A comparison of risk factors for calcified atherosclerotic plaque in the coronary, carotid, and abdominal aortic arteries: the diabetes heart study. Am J Epidemiol. 2007;166(3):340–7.PubMedPubMedCentral Wagenknecht LE, Langefeld CD, Freedman BI, Carr JJ, Bowden DW. A comparison of risk factors for calcified atherosclerotic plaque in the coronary, carotid, and abdominal aortic arteries: the diabetes heart study. Am J Epidemiol. 2007;166(3):340–7.PubMedPubMedCentral
7.
go back to reference Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. Jama. 1999;282(21):2035–42.PubMed Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. Jama. 1999;282(21):2035–42.PubMed
8.
go back to reference Markl M, Wegent F, Zech T, Bauer S, Strecker C, Schumacher M, et al. In vivo wall shear stress distribution in the carotid artery: effect of bifurcation geometry, internal carotid artery stenosis, and recanalization therapy. Circ Cardiovasc Imaging. 2010;3(6):647–55.PubMed Markl M, Wegent F, Zech T, Bauer S, Strecker C, Schumacher M, et al. In vivo wall shear stress distribution in the carotid artery: effect of bifurcation geometry, internal carotid artery stenosis, and recanalization therapy. Circ Cardiovasc Imaging. 2010;3(6):647–55.PubMed
9.
go back to reference Cecchi E, Giglioli C, Valente S, Lazzeri C, Gensini GF, Abbate R, et al. Role of hemodynamic shear stress in cardiovascular disease. Atherosclerosis. 2011;214(2):249–56.PubMed Cecchi E, Giglioli C, Valente S, Lazzeri C, Gensini GF, Abbate R, et al. Role of hemodynamic shear stress in cardiovascular disease. Atherosclerosis. 2011;214(2):249–56.PubMed
10.
go back to reference Lee SW, Antiga L, Spence JD, Steinman DA. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke. 2008;39(8):2341–7.PubMed Lee SW, Antiga L, Spence JD, Steinman DA. Geometry of the carotid bifurcation predicts its exposure to disturbed flow. Stroke. 2008;39(8):2341–7.PubMed
11.
go back to reference Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113(23):2744–53.PubMed Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113(23):2744–53.PubMed
12.
go back to reference van Bochove GS, Straathof R, Krams R, Nicolay K, Strijkers GJ. MRI-determined carotid artery flow velocities and wall shear stress in a mouse model of vulnerable and stable atherosclerotic plaque. Magma. 2010;23(2):77–84.PubMed van Bochove GS, Straathof R, Krams R, Nicolay K, Strijkers GJ. MRI-determined carotid artery flow velocities and wall shear stress in a mouse model of vulnerable and stable atherosclerotic plaque. Magma. 2010;23(2):77–84.PubMed
13.
go back to reference Tuenter A, Selwaness M, Arias Lorza A, Schuurbiers JCH, Speelman L, Cibis M, et al. High shear stress relates to intraplaque haemorrhage in asymptomatic carotid plaques. Atherosclerosis. 2016;251:348–54.PubMed Tuenter A, Selwaness M, Arias Lorza A, Schuurbiers JCH, Speelman L, Cibis M, et al. High shear stress relates to intraplaque haemorrhage in asymptomatic carotid plaques. Atherosclerosis. 2016;251:348–54.PubMed
14.
go back to reference Groen HC, Gijsen FJ, van der Lugt A, Ferguson MS, Hatsukami TS, van der Steen AF, et al. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke. 2007;38(8):2379–81.PubMed Groen HC, Gijsen FJ, van der Lugt A, Ferguson MS, Hatsukami TS, van der Steen AF, et al. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke. 2007;38(8):2379–81.PubMed
15.
go back to reference Phan TG, Beare RJ, Jolley D, Das G, Ren M, Wong K, et al. Carotid artery anatomy and geometry as risk factors for carotid atherosclerotic disease. Stroke. 2012;43(6):1596–601.PubMed Phan TG, Beare RJ, Jolley D, Das G, Ren M, Wong K, et al. Carotid artery anatomy and geometry as risk factors for carotid atherosclerotic disease. Stroke. 2012;43(6):1596–601.PubMed
16.
go back to reference Bijari PB, Wasserman BA, Steinman DA. Carotid bifurcation geometry is an independent predictor of early wall thickening at the carotid bulb. Stroke. 2014;45(2):473–8.PubMed Bijari PB, Wasserman BA, Steinman DA. Carotid bifurcation geometry is an independent predictor of early wall thickening at the carotid bulb. Stroke. 2014;45(2):473–8.PubMed
17.
go back to reference Cibis M, Potters WV, Selwaness M, Gijsen FJ, Franco OH, Arias Lorza AM, et al. Relation between wall shear stress and carotid artery wall thickening MRI versus CFD. J Biomech. 2016;49(5):735–41.PubMed Cibis M, Potters WV, Selwaness M, Gijsen FJ, Franco OH, Arias Lorza AM, et al. Relation between wall shear stress and carotid artery wall thickening MRI versus CFD. J Biomech. 2016;49(5):735–41.PubMed
18.
go back to reference von Reutern GM, Goertler MW, Bornstein NM, Del Sette M, Evans DH, Hetzel A, et al. Grading carotid stenosis using ultrasonic methods. Stroke. 2012;43(3):916–21. von Reutern GM, Goertler MW, Bornstein NM, Del Sette M, Evans DH, Hetzel A, et al. Grading carotid stenosis using ultrasonic methods. Stroke. 2012;43(3):916–21.
19.
go back to reference Jung B, Stalder AF, Bauer S, Markl M. On the undersampling strategies to accelerate time-resolved 3D imaging using k-t-GRAPPA. Magn Reson Med. 2011;66(4):966–75.PubMed Jung B, Stalder AF, Bauer S, Markl M. On the undersampling strategies to accelerate time-resolved 3D imaging using k-t-GRAPPA. Magn Reson Med. 2011;66(4):966–75.PubMed
20.
go back to reference Bauer S, Markl M, Foll D, Russe M, Stankovic Z, Jung B. K-t GRAPPA accelerated phase contrast MRI: improved assessment of blood flow and 3-directional myocardial motion during breath-hold. J Magn Reson Imaging. 2013;38(5):1054–62.PubMed Bauer S, Markl M, Foll D, Russe M, Stankovic Z, Jung B. K-t GRAPPA accelerated phase contrast MRI: improved assessment of blood flow and 3-directional myocardial motion during breath-hold. J Magn Reson Imaging. 2013;38(5):1054–62.PubMed
21.
go back to reference Wehrum T, Kams M, Schroeder L, Drexl J, Hennemuth A, Harloff A. Accelerated analysis of three-dimensional blood flow of the thoracic aorta in stroke patients. Int J Cardiovasc Imaging. 2014;30(8):1571–7.PubMed Wehrum T, Kams M, Schroeder L, Drexl J, Hennemuth A, Harloff A. Accelerated analysis of three-dimensional blood flow of the thoracic aorta in stroke patients. Int J Cardiovasc Imaging. 2014;30(8):1571–7.PubMed
22.
go back to reference Friedman MH, Deters OJ, Mark FF, Bargeron CB, Hutchins GM. Arterial geometry affects hemodynamics. A potential risk factor for athersoclerosis. Atherosclerosis. 1983;46(2):225–31.PubMed Friedman MH, Deters OJ, Mark FF, Bargeron CB, Hutchins GM. Arterial geometry affects hemodynamics. A potential risk factor for athersoclerosis. Atherosclerosis. 1983;46(2):225–31.PubMed
23.
go back to reference Friedman MH, Deters OJ, Bargeron CB, Hutchins GM, Mark FF. Shear-dependent thickening of the human arterial intima. Atherosclerosis. 1986;60(2):161–71.PubMed Friedman MH, Deters OJ, Bargeron CB, Hutchins GM, Mark FF. Shear-dependent thickening of the human arterial intima. Atherosclerosis. 1986;60(2):161–71.PubMed
24.
go back to reference Gallo D, Bijari PB, Morbiducci U, Qiao Y, Xie YJ, Etesami M, et al. Segment-specific associations between local haemodynamic and imaging markers of early atherosclerosis at the carotid artery: an in vivo human study. J R Soc Interface. 2018;15(147):20180352.PubMedPubMedCentral Gallo D, Bijari PB, Morbiducci U, Qiao Y, Xie YJ, Etesami M, et al. Segment-specific associations between local haemodynamic and imaging markers of early atherosclerosis at the carotid artery: an in vivo human study. J R Soc Interface. 2018;15(147):20180352.PubMedPubMedCentral
25.
go back to reference Harloff A, Berg S, Barker AJ, Schollhorn J, Schumacher M, Weiller C, et al. Wall shear stress distribution at the carotid bifurcation: influence of eversion carotid endarterectomy. Eur Radiol. 2013;23(12):3361–9.PubMed Harloff A, Berg S, Barker AJ, Schollhorn J, Schumacher M, Weiller C, et al. Wall shear stress distribution at the carotid bifurcation: influence of eversion carotid endarterectomy. Eur Radiol. 2013;23(12):3361–9.PubMed
27.
go back to reference Brown AJ, Teng Z, Calvert PA, Rajani NK, Hennessy O, Nerlekar N, et al. Plaque structural stress estimations improve prediction of future major adverse cardiovascular events after intracoronary imaging. Circ Cardiovasc Imaging. 2016;9(6):e004172.PubMed Brown AJ, Teng Z, Calvert PA, Rajani NK, Hennessy O, Nerlekar N, et al. Plaque structural stress estimations improve prediction of future major adverse cardiovascular events after intracoronary imaging. Circ Cardiovasc Imaging. 2016;9(6):e004172.PubMed
28.
go back to reference Eshtehardi P, Brown AJ, Bhargava A, Costopoulos C, Hung OY, Corban MT, et al. High wall shear stress and high-risk plaque: an emerging concept. Int J Cardiovasc Imaging. 2017;33(7):1089–99.PubMedPubMedCentral Eshtehardi P, Brown AJ, Bhargava A, Costopoulos C, Hung OY, Corban MT, et al. High wall shear stress and high-risk plaque: an emerging concept. Int J Cardiovasc Imaging. 2017;33(7):1089–99.PubMedPubMedCentral
29.
go back to reference Smedby O, Bergstrand L. Tortuosity and atherosclerosis in the femoral artery: what is cause and what is effect? Ann Biomed Eng. 1996;24(4):474–80.PubMed Smedby O, Bergstrand L. Tortuosity and atherosclerosis in the femoral artery: what is cause and what is effect? Ann Biomed Eng. 1996;24(4):474–80.PubMed
30.
go back to reference Augst AD, Ariff B, Mc GTSA, Xu XY, Hughes AD. Analysis of complex flow and the relationship between blood pressure, wall shear stress, and intima-media thickness in the human carotid artery. Am J Physiol Heart Circ Physiol. 2007;293(2):H1031–7.PubMed Augst AD, Ariff B, Mc GTSA, Xu XY, Hughes AD. Analysis of complex flow and the relationship between blood pressure, wall shear stress, and intima-media thickness in the human carotid artery. Am J Physiol Heart Circ Physiol. 2007;293(2):H1031–7.PubMed
31.
go back to reference Tang D, Yang C, Canton G, Wu Z, Hatsukami T, Yuan C. Correlations between carotid plaque progression and mechanical stresses change sign over time: a patient follow up study using MRI and 3D FSI models. Biomed Eng Online. 2013;12:105.PubMedPubMedCentral Tang D, Yang C, Canton G, Wu Z, Hatsukami T, Yuan C. Correlations between carotid plaque progression and mechanical stresses change sign over time: a patient follow up study using MRI and 3D FSI models. Biomed Eng Online. 2013;12:105.PubMedPubMedCentral
32.
go back to reference van Ooij P, Cibis M, Rowland EM, Vernooij MW, van der Lugt A, Weinberg PD, et al. Spatial correlations between MRI-derived wall shear stress and vessel wall thickness in the carotid bifurcation. Eur Radiol Exp. 2018;2(1):27.PubMedPubMedCentral van Ooij P, Cibis M, Rowland EM, Vernooij MW, van der Lugt A, Weinberg PD, et al. Spatial correlations between MRI-derived wall shear stress and vessel wall thickness in the carotid bifurcation. Eur Radiol Exp. 2018;2(1):27.PubMedPubMedCentral
33.
go back to reference Carallo C, Tripolino C, De Franceschi MS, Irace C, Xu XY, Gnasso A. Carotid endothelial shear stress reduction with aging is associated with plaque development in twelve years. Atherosclerosis. 2016;251:63–9.PubMed Carallo C, Tripolino C, De Franceschi MS, Irace C, Xu XY, Gnasso A. Carotid endothelial shear stress reduction with aging is associated with plaque development in twelve years. Atherosclerosis. 2016;251:63–9.PubMed
34.
go back to reference Zhang B, Gu J, Qian M, Niu L, Zhou H, Ghista D. Correlation between quantitative analysis of wall shear stress and intima-media thickness in atherosclerosis development in carotid arteries. Biomed Eng Online. 2017;16(1):137.PubMedPubMedCentral Zhang B, Gu J, Qian M, Niu L, Zhou H, Ghista D. Correlation between quantitative analysis of wall shear stress and intima-media thickness in atherosclerosis development in carotid arteries. Biomed Eng Online. 2017;16(1):137.PubMedPubMedCentral
35.
go back to reference Harloff A, Zech T, Frydrychowicz A, Schumacher M, Schollhorn J, Hennig J, et al. Carotid intima-media thickness and distensibility measured by MRI at 3 T versus high-resolution ultrasound. Eur Radiol. 2009;19(6):1470–9.PubMed Harloff A, Zech T, Frydrychowicz A, Schumacher M, Schollhorn J, Hennig J, et al. Carotid intima-media thickness and distensibility measured by MRI at 3 T versus high-resolution ultrasound. Eur Radiol. 2009;19(6):1470–9.PubMed
36.
go back to reference Alizadeh Dehnavi R, Doornbos J, Tamsma JT, Stuber M, Putter H, van der Geest RJ, et al. Assessment of the carotid artery by MRI at 3T: a study on reproducibility. J Magn Reson Imaging. 2007;25(5):1035–43.PubMed Alizadeh Dehnavi R, Doornbos J, Tamsma JT, Stuber M, Putter H, van der Geest RJ, et al. Assessment of the carotid artery by MRI at 3T: a study on reproducibility. J Magn Reson Imaging. 2007;25(5):1035–43.PubMed
37.
go back to reference Neuhaus E, Weiss K, Bastkowski R, Koopmann J, Maintz D, Giese D. Accelerated aortic 4D flow cardiovascular magnetic resonance using compressed sensing: applicability, validation and clinical integration. J Cardiovasc Magn Reson. 2019;21(1):65.PubMedPubMedCentral Neuhaus E, Weiss K, Bastkowski R, Koopmann J, Maintz D, Giese D. Accelerated aortic 4D flow cardiovascular magnetic resonance using compressed sensing: applicability, validation and clinical integration. J Cardiovasc Magn Reson. 2019;21(1):65.PubMedPubMedCentral
Metadata
Title
Carotid geometry is an independent predictor of wall thickness – a 3D cardiovascular magnetic resonance study in patients with high cardiovascular risk
Authors
Christoph Strecker
Axel Joachim Krafft
Lilli Kaufhold
Markus Hüllebrandt
Susanne Weber
Ute Ludwig
Martin Wolkewitz
Anja Hennemuth
Jürgen Hennig
Andreas Harloff
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2020
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-020-00657-5

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