Quantification of carotid plaque lipid content with magnetic resonance T2 mapping in patients undergoing carotid endarterectomy

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Abstract

Background and purpose

Techniques to stratify subgroups of patients with asymptomatic carotid artery disease are urgently needed to guide decisions on optimal treatment. Reliance on estimates of % luminal stenosis has not been effective, perhaps because that approach entirely disregards potentially important information on the pathological process in the wall of the artery.

Methods

Since plaque lipid is a key determinant of plaque behaviour we used a newly validated, high-sensitivity T2-mapping MR technique for a systematic survey of the quantity and distribution of plaque lipid in patients undergoing endarterectomy. Lipid percentage was quantified in 50 carotid endarterectomy patients. Lipid distribution was tested, using two imaging indices (contribution of the largest lipid deposit towards total lipid (LLD %) and a newly-developed LAI ‘lipid aggregation index’).

Results

The bifurcation contained maximal lipid volume. Lipid percentage was higher in symptomatic vs. asymptomatic patients with degree of stenosis (DS ≥ 50%) and in the total cohort (P = 0.013 and P = 0.005, respectively). Both LLD % and LAI was higher in symptomatic patients (P = 0.028 and P = 0.018, respectively), suggesting that for a given plaque lipid volume, coalesced deposits were more likely to be associated with symptomatic events. There was no correlation between plaque volume or lipid content and degree of luminal stenosis measured on ultrasound duplex (r = -0.09, P = 0.53 and r = -0.05, P = 0.75), respectively. However, there was a strong correlation in lipid between left and right carotid arteries (r = 0.5, P <0.0001, respectively).

Conclusions

Plaque lipid content and distribution is associated with symptomatic status of the carotid plaque. Importantly, plaque lipid content was not related to the degree of luminal stenosis assessed by ultrasound. Determination of plaque lipid content may prove useful for stratification of asymptomatic patients, including selection of optimal invasive treatments.

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Most cited references 19

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Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial.

A. Halliday, A. Mansfield, J. Marro … (2004)

Among patients with substantial carotid artery narrowing but no recent neurological symptom (stroke or transient ischaemia), the balance of surgical risks and long-term benefits from carotid endarterectomy (CEA) was unclear. During 1993-2003, 3120 asymptomatic patients with substantial carotid narrowing were randomised equally between immediate CEA (half got CEA by 1 month, 88% by 1 year) and indefinite deferral of any CEA (only 4% per year got CEA) and were followed for up to 5 years (mean 3.4 years). Kaplan-Meier analyses of 5-year risks are by allocated treatment. The risk of stroke or death within 30 days of CEA was 3.1% (95% CI 2.3-4.1). Comparing all patients allocated immediate CEA versus all allocated deferral, but excluding such perioperative events, the 5-year stroke risks were 3.8% versus 11% (gain 7.2% [95% CI 5.0-9.4], p<0.0001). This gain chiefly involved carotid territory ischaemic strokes (2.7% vs 9.5%; gain 6.8% [4.8-8.8], p<0.0001), of which half were disabling or fatal (1.6% vs 5.3%; gain 3.7% [2.1-5.2], p<0.0001), as were half the perioperative strokes. Combining the perioperative events and the non-perioperative strokes, net 5-year risks were 6.4% versus 11.8% for all strokes (net gain 5.4% [3.0-7.8], p<0.0001), 3.5% versus 6.1% for fatal or disabling strokes (net gain 2.5% [0.8-4.3], p=0.004), and 2.1% versus 4.2% just for fatal strokes (net gain 2.1% [0.6-3.6], p=0.006). Subgroup-specific analyses found no significant heterogeneity in the perioperative hazards or (apart from the importance of cholesterol) in the long-term postoperative benefits. These benefits were separately significant for males and females; for those with about 70%, 80%, and 90% carotid artery narrowing on ultrasound; and for those younger than 65 and 65-74 years of age (though not for older patients, half of whom die within 5 years from unrelated causes). Full compliance with allocation to immediate CEA or deferral would, in expectation, have produced slightly bigger differences in the numbers operated on, and hence in the net 5-year benefits. The 10-year benefits are not yet known. In asymptomatic patients younger than 75 years of age with carotid diameter reduction about 70% or more on ultrasound (many of whom were on aspirin, antihypertensive, and, in recent years, statin therapy), immediate CEA halved the net 5-year stroke risk from about 12% to about 6% (including the 3% perioperative hazard). Half this 5-year benefit involved disabling or fatal strokes. But, outside trials, inappropriate selection of patients or poor surgery could obviate such benefits.

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Endarterectomy for asymptomatic carotid artery stenosis. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study.

JF Toole, M Goldstein, JR Marler … (1995)

To determine whether the addition of carotid endarterectomy to aggressive medical management can reduce the incidence of cerebral infarction in patients with asymptomatic carotid artery stenosis. Prospective, randomized, multicenter trial. Thirty-nine clinical sites across the United States and Canada. Between December 1987 and December 1993, a total of 1662 patients with asymptomatic carotid artery stenosis of 60% or greater reduction in diameter were randomized; follow-up data are available on 1659. At baseline, recognized risk factors for stroke were similar between the two treatment groups. Daily aspirin administration and medical risk factor management for all patients; carotid endarterectomy for patients randomized to receive surgery. Initially, transient ischemic attack or cerebral infarction occurring in the distribution of the study artery and any transient ischemic attack, stroke, or death occurring in the perioperative period. In March 1993, the primary outcome measures were changed to cerebral infarction occurring in the distribution of the study artery or any stroke or death occurring in the perioperative period. After a median follow-up of 2.7 years, with 4657 patient-years of observation, the aggregate risk over 5 years for ipsilateral stroke and any perioperative stroke or death was estimated to be 5.1% for surgical patients and 11.0% for patients treated medically (aggregate risk reduction of 53% [95% confidence interval, 22% to 72%]). Patients with asymptomatic carotid artery stenosis of 60% or greater reduction in diameter and whose general health makes them good candidates for elective surgery will have a reduced 5-year risk of ipsilateral stroke if carotid endarterectomy performed with less than 3% perioperative morbidity and mortality is added to aggressive management of modifiable risk factors.

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Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST)

(1998)

Our objective was to assess the risks and benefits of carotid endarterectomy, primarily in terms of stroke prevention, in patients with recently symptomatic carotid stenosis. This multicentre, randomised controlled trial enrolled 3024 patients. We enrolled men and women of any age, with some degree of carotid stenosis, who within the previous 6 months had had at least one transient or mild symptomatic ischaemic vascular event in the distribution of one or both carotid arteries. Between 1981 and 1994, we allocated 1811 (60%) patients to surgery and 1213 (40%) to control (surgery to be avoided for as long as possible). Follow-up was until the end of 1995 (mean 6.1 years), and the main analyses were by intention to treat. The overall outcome (major stroke or death) occurred in 669 (37.0%) surgery-group patients and 442 (36.5%) control-group patients. The risk of major stroke or death complicating surgery (7.0%) did not vary substantially with severity of stenosis. On the other hand, the risk of major ischaemic stroke ipsilateral to the unoperated symptomatic carotid artery increased with severity of stenosis, particularly above about 70-80% of the original luminal diameter, but only for 2-3 years after randomisation. On average, the immediate risk of surgery was worth trading off against the long-term risk of stroke without surgery when the stenosis was greater than about 80% diameter; the Kaplan-Meier estimate of the frequency of a major stroke or death at 3 years was 26.5% for the control group and 14.9% for the surgery group, an absolute benefit from surgery of 11.6%. However, consideration of variations in risk with age and sex modified this simple rule based on stenosis severity. We present a graphical procedure that should improve the selection of patients for surgery. Carotid endarterectomy is indicated for most patients with a recent non-disabling carotid-territory ischaemic event when the symptomatic stenosis is greater than about 80%. Age and sex should also be taken into account in decisions on whether to operate.

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Author and article information

Contributors

Mohammad Alkhalil:

ORCID: http://orcid.org/0000-0002-3088-8878

Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing

Luca Biasiolli: Role: Data curationRole: InvestigationRole: SoftwareRole: Writing – review & editing

Joshua T. Chai: Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing

Francesca Galassi: Role: Data curationRole: SoftwareRole: Writing – review & editing

Linqing Li: Role: Data curationRole: SoftwareRole: Writing – review & editing

Christopher Darby: Role: ResourcesRole: Writing – review & editing

Alison Halliday: Role: ResourcesRole: Writing – review & editing

Linda Hands: Role: ResourcesRole: Writing – review & editing

Timothy Magee: Role: ResourcesRole: Writing – review & editing

Jeremy Perkins: Role: ResourcesRole: Writing – review & editing

Ed Sideso: Role: ResourcesRole: Writing – review & editing

Peter Jezzard: Role: Data curationRole: SoftwareRole: Writing – review & editing

Matthew D. Robson: Role: Data curationRole: SoftwareRole: Writing – review & editing

Ashok Handa: Role: InvestigationRole: ResourcesRole: Writing – review & editing

Robin P. Choudhury: Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing

Christina A. Bursill: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 26 July 2017

Publication date Collection: 2017

Volume: 12

Issue: 7

Electronic Location Identifier: e0181668

Affiliations

[1 ] Acute Vascular Imaging Centre, Radcliffe Department of Medicine, University of Oxford, Oxford, United Kingdom

[2 ] FMRIB Centre, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

[3 ] Nuffield Department of Surgical Sciences, University of Oxford, Oxford, United Kingdom

Heart Research Institute, AUSTRALIA

Author notes

Competing Interests: Professor Choudhury has received honoraria from Amgen; Sanofi; ISIS pharmaceuticals; Merck, Astra Zeneca, Boehringer Ingelheim, GlaxoSmithKline, Regneron, and research funding from Novartis, Merck and the NovoNordisk Foundation. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

* E-mail: robin.choudhury@ 123456cardiov.ox.ac.uk

Author information

Mohammad Alkhalil http://orcid.org/0000-0002-3088-8878

Article

Publisher ID: PONE-D-17-16240

DOI: 10.1371/journal.pone.0181668

PMC ID: 5528883

PubMed ID: 28746385

SO-VID: 8d21d227-089f-4a69-b50b-9ce6d3129599

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 27 April 2017

Date accepted : 5 July 2017

Page count

Figures: 5, Tables: 1, Pages: 12

Funding

Funded by: funder-id http://dx.doi.org/10.13039/501100000274, British Heart Foundation;

Award ID: PG/11/120/29302 & PG/15/74/31747

Funded by: funder-id http://dx.doi.org/10.13039/501100000272, National Institute for Health Research;

Funded by: funder-id http://dx.doi.org/10.13039/501100000377, Dunhill Medical Trust;

This work was supported from BHF (grant PG/11/120/29302 & PG/15/74/31747), the NIHR Oxford Biomedical Research Centre, and the Dunhill Medical Trust. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Quantification of carotid plaque lipid content with magnetic resonance T2 mapping in patients undergoing carotid endarterectomy

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Abstract

Background and purpose

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Results

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PLOS: COVID-19 pandemic

Most cited references 19

Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial.

Endarterectomy for asymptomatic carotid artery stenosis. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study.

Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST)

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