Expansive arterial remodeling of the carotid arteries and its effect on atherosclerotic plaque composition and vulnerability: an in-vivo black-blood 3T CMR study in symptomatic stroke patients | springermedicine.com

Springer Medicine

Top

Journal of Cardiovascular Magnetic Resonance

Published in:

Open Access 01-12-2016 | Research

Expansive arterial remodeling of the carotid arteries and its effect on atherosclerotic plaque composition and vulnerability: an in-vivo black-blood 3T CMR study in symptomatic stroke patients

Authors: Tobias Saam, Maximilian Habs, Martin Buchholz, Andreas Schindler, Anna Bayer-Karpinska, Clemens C. Cyran, Chun Yuan, Maximilian Reiser, Andreas Helck

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

Login to get access

Abstract

Background

Based on intravascular ultrasound of the coronary arteries expansive arterial remodeling is supposed to be a feature of the vulnerable atheroslerotic plaque. However, till now little is known regarding the clinical impact of expansive remodeling of carotid lesions. Therefore, we sought to evaluate the correlation of expansive arterial remodeling of the carotid arteries with atherosclerotic plaque composition and vulnerability using in-vivo Cardiovascular Magnetic Resonance (CMR).

Methods

One hundred eleven symptomatic patients (74 male/71.8 ± 10.3y) with acute unilateral ischemic stroke and carotid plaques of at least 2 mm thickness were included. All patients received a dedicated multi-sequence black-blood carotid CMR (3Tesla) of the proximal internal carotid arteries (ICA). Measurements of lumen, wall, outer wall, hemorrhage, calcification and necrotic core were determined. Each vessel-segment was classified according to American Heart Association (AHA) criteria for vulnerable plaque. A modified remodeling index (mRI) was established by dividing the average outer vessel area of the ICA segments by the lumen area measured on TOF images in a not affected reference segment at the distal ipsilateral ICA. Correlations of mRI and clinical symptoms as well as plaque morphology/vessel dimensions were evaluated.

Results

Seventy-eight percent (157/202) of all internal carotid arteries showed atherosclerotic disease with AHA Lesion-Type (LT) III or higher. The mRI of the ICA was significantly different in normal artery segments (AHA LT I; mRI 1.9) compared to atherosclerotic segments (AHA LT III-VII; mRI 2.5; p < 0.0001). Between AHA LT III-VII there was no significant difference of mRI. Significant correlations (p < 0.05) of the mRI with lumen-area (LA), wall-area (WA), vessel-area (VA) and wall-thickness (WT), necrotic-core area (NC), and ulcer-area were observed. With respect to clinical presentation (symptomatic/asymptomatic side) and luminal narrowing (stenotic/non-stenotic) no relevant correlations or significant differences regarding the mRI were found.

Conclusion

Expansive arterial remodeling exists in the ICA. However, no significant association between expansive arterial remodeling, stroke symptoms, complicated AHA VI plaque, and luminal stenosis could be established. Hence, results of our study suggest that expansive arterial remodeling is not a very practical marker for plaque vulnerability in the carotid arteries.

1.

Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ. Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med. 1987;316:1371–5.CrossRefPubMed

2.

Pasterkamp G, Schoneveld AH, van der Wal AC, Haudenschild CC, Clarijs RJ, Becker AE, et al. Relation of arterial geometry to luminal narrowing and histologic markers for plaque vulnerability: the remodeling paradox. J Am Coll Cardiol. 1998;32(3):655–62.CrossRefPubMed

3.

Smits PC, Pasterkamp G, de Jaegere PP, de Feyter PJ, Borst C. Angioscopic complex lesions are predominantly compensatory enlarged: an angioscopy and intracoronary ultrasound study. Cardiovasc Res. 1999;41(2):458–64.CrossRefPubMed

4.

Schoenhagen P, Ziada KM, Kapadia SR, Crowe TD, Nissen SE, Tuzcu EM. Extent and direction of arterial remodeling in stable versus unstable coronary syndromes : an intravascular ultrasound study. Circulation. 2000;101(6):598–603.CrossRefPubMed

5.

Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, et al. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364(3):226–35.CrossRefPubMed

6.

Pasterkamp G, Schoneveld AH, van Wolferen W, Hillen B, Clarijs RJ, Haudenschild CC, et al. The impact of atherosclerotic arterial remodeling on percentage of luminal stenosis varies widely within the arterial system. A postmortem study. Arterioscler Thromb Vasc Biol. 1997;17(11):3057–63.CrossRefPubMed

7.

Galis ZS, Johnson C, Godin D, Magid R, Shipley JM, Senior RM, et al. Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ Res. 2002;91:852–9.CrossRefPubMed

8.

Ivan E, Khatri JJ, Johnson C, Magid R, Godin D, Nandi S, et al. Expansive arterial remodelling is associated with increased neointimal macrophage foam cell content: the murine mode macrophage-rich carotid artery lesions. Circulation. 2002;105:2686–91.CrossRefPubMed

9.

Dalager S, Paaske WP, Kristensen IB, Laurberg JM, Falk E. Artery-related differences in atherosclerosis expression: implications for atherogenesis and dynamics in intima-media thickness. Stroke. 2007;38(10):2698–705.CrossRefPubMed

10.

Mohiaddin RH, Burman ED, Prasad SK, Varghese A, Tan RS, Collins SA, et al. Glagov remodeling of the atherosclerotic aorta demonstrated by cardiovascular magnetic resonance: the CORDA asymptomatic subject plaque assessment research (CASPAR) project. J Cardiovasc Magn Reson. 2004;6(2):517–25.CrossRefPubMed

11.

Yuan C, Kerwin WS, Yarnykh VL, Cai J, Saam T, Chu B, et al. MRI of atherosclerosis in clinical trials. NMR Biomed. 2006;19(6):636–54.CrossRefPubMed

12.

Qian D, Bottomley PA. High-resolution intravascular magnetic resonance quantification of atherosclerotic plaque at 3T. J Cardiovasc Magn Reson. 2012;14:20.CrossRefPubMedPubMedCentral

13.

Cai JM, Hatsukami TS, Ferguson MS, Small R, Polissar NL, Yuan C. Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation. 2002;106(11):1368–73.CrossRefPubMed

14.

Kamenskiy AV, Pipinos II, Carson JS, MacTaggart JN, Baxter BT. Age and disease-related geometric and structural remodeling of the carotid artery. J Vasc Surg. 2015;62(6):1521–8.CrossRefPubMed

15.

Thomas JB, Antiga L, Che SL, Milner JS, Steinman DA, Spence JD, et al. Variation in the carotid bifurcation geometry of young versus older adults: implications for geometric risk of atherosclerosis. Stroke. 2005;36(11):2450–6.CrossRefPubMed

16.

Saam T, Raya JG, Cyran CC, Bochmann K, Meimarakis G, Dietrich O, et al. High resolution carotid blackblood 3T MR with parallel imaging and dedicated 4-channel surface coils. J Cardiovasc Magn Reson. 2009;11(1):41.CrossRefPubMedPubMedCentral

17.

Naghavi M, Libby P, Falk E, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies—part I. Circulation. 2003;108:1664–72.CrossRefPubMed

18.

Naghavi M, Libby P, Falk E, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies—part II. Circulation. 2003;108:1772–8.CrossRefPubMed

19.

Ku DN, Giddens DP, Zarins CK, Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis. 1985;5(3):293–302.CrossRefPubMed

20.

Zarins CK, Giddens DP, Bharadvaj BK, Sottiurai VS, Mabon RF, Glagov S. Carotid bifurcation atherosclerosis. Quantitative correlation of plaque localization with flow velocity profiles and wall shear stress. Circ Res. 1983;53(4):502–14.CrossRefPubMed

21.

Samady H, Eshtehardi P, McDaniel MC, Suo J, Dhawan SS, Maynard C, et al. Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease. Circulation. 2011;124(7):779–88.CrossRefPubMed

22.

Groen HC, Gijsen FJ, van der Lugt A, Ferguson MS, Hatsukami TS, van der Stehen AW, et al. Plaque rupture in the carotid artery is localized at the high shear stress region: a case report. Stroke. 2007;38:2379–81.CrossRefPubMed

23.

Bianda N, Di Valentino M, Périat D, Segatto JM, Oberson M, Moccetti M, et al. Progression of human carotid and femoral atherosclerosis: a prospective follow-up study by magnetic resonance vessel wall imaging. Eur Heart J. 2012;33(2):230–7.CrossRefPubMed

24.

Hayashi K, Mani V, Nemade A, Aguiar S, Postley JE, Fuster V, et al. Variations in atherosclerosis and remodeling patterns in aorta and carotids. J Cardiovasc Magn Reson. 2010;12:10.CrossRefPubMedPubMedCentral

25.

Hardie AD, Kramer CM, Raghavan P, Baskurt E, Nandalur KR. The impact of expansive arterial remodeling on clinical presentation in carotid artery disease: a multidetector CT angiography study. AJNR Am J Neuroradiol. 2007;28(6):1067–70.CrossRefPubMedPubMedCentral

26.

Miura T, Matsukawa N, Sakurai K, Katano H, Ueki Y, Okita K, et al. Plaque vulnerability in internal carotid arteries with positive remodeling. Cerebrovasc Dis Extra. 2011;1(1):54–65.CrossRefPubMedPubMedCentral

27.

Saam T, Cai J, Ma L, Cai YQ, Ferguson MS, Polissar NL, et al. Comparison of symptomatic and asymptomatic atherosclerotic carotid plaque features with in vivo MR imaging. Radiology. 2006;240(2):464–72.CrossRefPubMedPubMedCentral

28.

Yoshida K, Fukumitsu R, Kurosaki Y, Funaki T, Kikuchi T, Takahashi JC, et al. The association between expansive arterial remodeling detected by high-resolution MRI in carotid artery stenosis and clinical presentation. J Neurosurg. 2015;13:1–7.

29.

Grimm JM, Schindler A, Freilinger T, Cyran CC, Bamberg F, Yuan C, et al. Comparison of symptomatic and asymptomatic atherosclerotic carotid plaques using parallel imaging and 3T black-blood in vivo CMR. J Cardiovasc Magn Reson. 2013;15:44.CrossRefPubMedPubMedCentral

30.

Inaba S, Mintz GS, Farhat NZ, Fajadet J, Dudek D, Marzocchi A, et al. Impact of positive and negative lesion site remodeling on clinical outcomes: insights from PROSPECT. JACC Cardiovasc Imaging. 2014;7(1):70–8.CrossRefPubMed

Title: Expansive arterial remodeling of the carotid arteries and its effect on atherosclerotic plaque composition and vulnerability: an in-vivo black-blood 3T CMR study in symptomatic stroke patients
Authors: Tobias Saam
Maximilian Habs
Martin Buchholz
Andreas Schindler
Anna Bayer-Karpinska
Clemens C. Cyran
Chun Yuan
Maximilian Reiser
Andreas Helck
Publication date: 01-12-2016
Publisher: BioMed Central
Published in: Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI: https://doi.org/10.1186/s12968-016-0229-2

Home
Congress Coverage
Clinical Collections
- Advances in Alzheimer’s
About Springer Medicine
Key Specialties