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. Author manuscript; available in PMC: 2021 Aug 23.
Published in final edited form as: Radiology. 2018 Feb 5;287(3):808–815. doi: 10.1148/radiol.2017171568

Perivascular Epicardial Fat Stranding at Coronary CT Angiography: A Marker of Acute Plaque Rupture and Spontaneous Coronary Artery Dissection

Sandeep Hedgire, Vinit Baliyan, Evan J Zucker, Daniel O Bittner, Pedro V Staziaki, Richard A P Takx, Jan-Erik Scholtz, Nandini Meyersohn, Udo Hoffmann, Brian Ghoshhajra
PMCID: PMC8382040  NIHMSID: NIHMS1058389  PMID: 29401041

Abstract

Purpose:

To evaluate the frequency and implications of perivascular fat stranding on coronary computed tomography (CT) angiograms obtained for suspected acute coronary syndrome (ACS).

Materials and Methods:

This retrospective registry study was approved by the institutional review board. The authors reviewed the medical records and images of 1403 consecutive patients (796 men, 607 women; mean age, 52.8 years) who underwent coronary CT angiography at the emergency department from February 2012 to March 2016. Fat attenuation, length and number of circumferential quadrants of the affected segment, and attenuation values in the unaffected epicardial and subcutaneous fat were measured. “Cases” were defined as patients with perivascular fat stranding. Patients with significant stenosis but without fat stranding were considered control subjects. Baseline imaging characteristics, ACS frequency, and results of subsequent downstream testing were compared between cases and control subjects by using two-sample t, Mann-Whitney U, and Fisher tests.

Results:

Perivascular fat stranding was seen in 11 subjects, nine with atherosclerotic lesions and two with spontaneous coronary artery dissections, with a mean fat stranding length of 19.2 mm and circumferential extent averaging 2.9 quadrants. The mean attenuation of perivascular fat stranding, normal epicardial fat, and normal subcutaneous fat was 17, −93.2, and −109.3 HU, respectively (P < .001). Significant differences (P < .05) between cases and control subjects included lower Agatston score, presence of wall motion abnormality, and initial elevation of serum troponin level. ACS frequency was 45.4% in cases and 3.8% in control subjects (P = .001).

Conclusion:

Recognition of perivascular fat stranding may be a helpful additional predictor of culprit lesion and marker of risk for ACS in patients with significant stenosis or spontaneous coronary artery dissection.

Adipose tissue between the myocardium and the visceral pericardium surrounds the epicardial course of the coronary arteries (1). Normal epicardial fat has homogeneous low attenuation (−45 to −195 HU) at computed tomography (CT) (2). At coronary CT angiography, well-opacified normal coronary artery walls have a distinct interface with the epicardial fat. Fat stranding is a CT finding of an abnormally increased attenuation in fat tissue, as a manifestation of edema or inflammatory and/or neoplastic infiltration, and was first described with abdominopelvic CT (3). Perivascular fat stranding is a well-known predictor of high risk in aortic aneurysms and is considered one of the earliest signs of impending rupture (4). The interaction between the perivascular fat and/or adipose tissue and blood vessels is an evolving concept, with animal models showing the role of proinflammatory adipocytokines in the progression of atherosclerotic disease. In their animal models, Takaoka et al (5) demonstrated migration of inflammatory cells into the perivascular fat in response to endovascular injury.

Low-to-intermediate risk patients suspected of having acute coronary syndrome (ACS) benefit from triage by means of coronary CT angiography in the emergency department to exclude hemodynamically significant stenosis (6). Rupture of atherosclerotic plaques underlies many cases of ACS, and plaque inflammation is a marker of plaque instability and vulnerability (7), as a result of the complex interplay of proinflammatory molecules and T cells, mast cells, and macrophages (8). Given that perivascular fat stranding is a CT sign of inflammation, it could potentially serve as an “imaging biomarker” of high-risk or ruptured plaques. The purpose of this study was to evaluate the frequency and implications of perivascular fat stranding at coronary CT angiography in patients suspected of having ACS.

Materials and Methods

Patient Population

In this institutional review board–approved, Health Insurance Portability and Accountability Act–compliant retrospective study, we reviewed medical records and images from 1403 patients (796 men and 607 women) who underwent coronary CT angiography in our hospital’s emergency department from February 2012 to March 2016. Clinical exclusion and inclusion criteria have been previously described in a published registry (9). Briefly, coronary CT angiography is part of routine clinical care of patients presenting to our emergency department with chest pain. The patients are screened for relative contraindications to imaging, which include previous revascularization or known coronary artery disease, electrocardiographic changes suggestive of myocardial ischemia, positive serum biomarker levels suggestive of high risk of myocardial infarction, impaired renal function (estimated glomerular filtration rate <60 mL/min/1.73 m2), and previous anaphylactoid reaction to iodinated contrast media. Patients with relative contraindications were permitted to undergo coronary CT angiography only after consultation with a cardiologist (Fig 1).

Figure 1:

Figure 1:

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Flowchart with inclusion and exclusion criteria and distribution of stenosis per Coronary Artery Disease Reporting and Data System (CAD-RADS). Chart shows distribution of degree of stenosis, cases with perivascular fat stranding, and control subjects without perivascular fat stranding. CTA = CT angiography, eCG = electrocardiography, eGFR = estimated glomerular filtration rate.

Image Acquisition and Analysis

The coronary CT angiographic studies, including qualitative functional assessment, were performed with either a second- or third-generation dual-source scanner (Somatom Definition Flash or Somatom Force; Siemens Healthineers, Forchheim, Germany) according to our institution’s protocol, which has previously been described in detail (10). “Cases” were defined as patients with perivascular fat stranding; a control cohort was identified from within the study population with an equivalent degree of luminal stenosis but without associated fat stranding. After definition of the study cohort, images were jointly reviewed by two radiologists blinded to history and findings at subsequent downstream testing in consensus (V.B. and S.H., with 3 and 10 years of experience, respectively, and both with subspecialty fellowship training in cardiac CT) for the presence of perivascular fat stranding in the cohort with a mild or higher degree of coronary artery disease. The presence and absence of fat standing was assessed on multiplanar reformatted coronary CT angiograms free of any motion artifacts and without mimickers such as myocardial bridging and accompanying veins. The degree of stenosis was graded according to the Coronary Artery Disease Reporting and Data System (CAD-RADS) (11). The reviewers were allowed to modify the window width and window level, and all CT angiograms were reviewed on a three-dimensional postprocessing workstation (v.4.4.11; TeraRecon, Foster City, Calif). Perivascular fat stranding was defined as irregular obscuration of epicardial fat adjacent to a coronary artery wall in the setting of mild or greater stenosis. When present, high-risk plaque features (12) were also evaluated to avoid false-positive findings, especially in the setting of the napkin ring sign and positive remodeling, which can lead to caliber change of the vessel, although both findings are observed with a preserved fat plane between epicardial fat and the coronary artery. Positive remodeling was assessed on multiplanar reformatted images with a threshold of 1.1 (ratio of plaque to normal reference segment diameter). The napkin ring sign was defined as peripheral ringlike noncalcified plaque with high attenuation. Calcified plaque less than 3 mm in diameter, length of calcium less than 1.5 times that of the coronary artery, and width less than two-thirds of the coronary artery diameter was considered as spotty calcium. Low-attenuation plaque was defined as plaque with a CT attenuation of less than 30 HU. In the absence of atherosclerotic plaques, the images were also evaluated for the presence of other obstructive coronary arterial abnormalities such as spontaneous coronary artery dissection (SCAD). When fat stranding was detected, it was quantified by measuring the attenuation within the involved fat, the length of the vascular segment affected, and the number of circumferential quadrants of the affected segment. For comparison, Hounsfield unit values of the adjacent unaffected epicardial fat and subcutaneous fat were measured by placing a region of interest of equivalent size. Associated findings, including degree of stenosis by the plaque associated with fat stranding, overall and pervessel Agatston score, and presence of wall motion abnormalities, were also recorded. Confounding imaging findings like myocardial bridging were also recorded. Qualitative functional assessment was performed by using multiplanar reformatted cine images at a 50-msec interval of the entire cardiac cycle in standard cardiac imaging planes such as two-, three-, and four-chamber views and the short-axis plane. Clinical diagnosis of ACS was assessed by reviewing the medical records, including all subsequent test results, including those of invasive coronary angiography (when performed). The demographic characteristics, body mass index, coronary risk factors, presence of regional wall motion abnormalities, and troponin levels were compared between the two groups.

Statistical Analysis

Results were analyzed with a statistical software (version 17.2; Medcalc, Ostend Belgium). Continuous parametric variables are expressed as means ± standard deviations. Categorical variables are expressed as frequencies and percentages. The independent sample t test was used for comparing calcium scores between the two groups, the Mann-Whitney U test for comparing Hounsfield unit and body mass index, and the Fisher exact test for comparing regional wall motion abnormality, elevated troponin level at presentation, frequency of ACS, and traditional high-risk plaque features. P values were two-sided, and P < .05 was considered indicative of a statistically significant difference.

Results

The mean age of the study population was 52.8 years ± 10.9 (95% confidence interval [CI]: 52.23 years, 53.37 years), and the mean body mass index was 29.2 kg/m2 6 6.1 (95% CI: 28.88 kg/ m2, 29.52 kg/m2). Coronary CT angiography showed no coronary artery stenosis (CAD-RADS 0) in 656 of the 1403 subjects (46.8%), minimal or mild stenosis (CAD-RADS 1–2) in 528 (37.6%), moderate stenosis (CAD-RADS 3) in 96 (6.8%), severe stenosis (CAD-RADS 4) in 99 (7.0%), and occlusion (CAD-RADS 5) in 24 (1.7%). In subjects with minimal or mild stenosis (CAD-RADS 1–2), no perivascular fat stranding was identified (Fig 1). In the 219 subjects with a moderate or higher degree of luminal stenosis (CAD-RADS 3–5), perivascular fat stranding was identified in 12 vascular segments of 11 patients (5.0%)—nine men and two women with a mean age of 49.7 years ± 16.6 (95% CI: 38.5 years, 60.8 years) (Table E1 [online]). One hundred twenty subjects had features of vulnerable plaque (CAD-RADS modifier V), two coexisting with the fat stranding in the case group (spotty calcium and positive remodeling in one case each) and 118 in the control group (spotty calcium in 110 subjects, positive remodeling in two, napkin ring sign in three, and low-attenuation plaque in six) with two features coexisting in three control subjects. The mean Hounsfield unit value in the affected segment was 17 HU (95% CI: 2.6 HU, 31.4 HU) (mean region of interest size: 2.86 mm2 ± 1.37) in comparison with control Hounsfield unit value of −93.2 HU (95% CI: −111 HU, −75.3 HU) and −109.3 HU (95% CI: −120.6 HU, −98 HU) in the unaffected epicardial and subcutaneous fat, respectively (P < .001, Mann-Whitney test). Of the 11 cases with perivascular fat stranding, nine had atherosclerotic plaques and two had SCAD (Figs 2, 3). One patient with dissection had two distinct segments of perivascular fat stranding within the same vessel. No cases of SCAD were seen in the control group. Both cases of SCAD were verified with subspecialty cardiology consultation and confirmed by an independent adjudicator. In all 12 segments, perivascular fat stranding was associated with the lesion causing significant stenosis (moderate in three, severe in two, and occlusive in seven cases). Of the 12 segments with perivascular fat stranding, 10 were in the right coronary artery and two were in the left anterior descending artery (LAD). Two of the 11 cases (18.2%) and 34 of the 208 control subjects (16.3%) had myocardial bridging of the LAD. The segment of perivascular fat stranding did not have an overlap with the bridged segments of the LAD. The mean length of the affected segment was 19.19 mm ± 34.87 (95% CI: 0 mm, 39.19 mm; range: 2.38–129 mm; median: 9.7 mm), and an average of 2.9 quadrants were involved (out of four).

Figure 2:

Figure 2:

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A, Curved planar reformatted coronary CT angiogram in 22-year-old man with acute chest pain following exercise, mildly elevated troponin level, and suspected coronary anomaly. Coronary CT angiogram reveals multifocal dissection of proximal through distal dominant right coronary artery, with occlusion of the distal segment, with, B, corresponding colorized image demonstrating perivascular fat stranding with indistinct interface between coronary artery and epicardial fat (arrow). C, Curved planar reformatted coronary CT angiogram in 52-year-old woman with chest pressure and multiple cardiac risk factors. Curved planar reformatted image and, D, colorized image illustrate severe stenosis and subtotal occlusion of proximal right coronary artery with surrounding fat stranding (arrows).

Figure 3:

Figure 3:

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A–D, Curved planar reformatted coronary CT angiograms show perivascular fat stranding (arrows) with spontaneous coronary artery dissection in, A, 22-year-old man and hemodynamically significant coronary atherosclerosis in, B, 73-year-old woman, C, 73-year-old man, and, D, 37-year-old man. E, Oblique axial and, F, coronal coronary CT angiograms in 39-year-old man demonstrate great cardiac vein (arrow), a common mimicker in assessment of perivascular fat stranding. Note distinct margin and underlying normal circumflex coronary artery (without stenosis or plaque).

The Table highlights key differences between the cases and control subjects. The control cohort was composed of 208 subjects (147 men and 61 women; mean age, 60.35 years ± 10.85 [95% CI: 58.85 years, 61.85 years]). The mean body mass index was comparable between the two groups (cases: 29.36 kg/m2 ± 6.4 [95% CI: 25.06 kg/m2, 33.66 kg/m2]; control subjects: 29.47 kg/m2 ± 5.09 [95% CI: 28.75 kg/m2, 30.19 kg/m2]). The mean age of cases (49.7 years ± 16.5; interquartile range, 53–66.5 years) was lower than that of the control subjects (60.3 years ± 10.8; interquartile range, 38.7–61.5 years) (P = .031, Mann-Whitney test). The mean Agatston score was 209 ± 254 (95% CI: 39, 379) in cases with perivascular fat stranding and 482 ± 786 (95% CI: 370, 592) in control subjects (P = .008, t test). The percentile scores of the two groups (per the Multi-Ethnic Study of Atherosclerosis normative database for healthy populations adjusted for age, sex, and race [13]) were not significantly different (median percentiles: 73 for cases vs 79 for control subjects; P = .21, Mann-Whitney test). Seven of the 11 cases (63.6%) had a corresponding regional wall motion abnormality, compared with 38 of the 208 control subjects (18.2%) (P = .0017, Fisher test). An elevated troponin level was noted at presentation in three cases with perivascular fat stranding (P < .001, Fisher test) compared with two of the 208 control subjects. The frequency of ACS was 45.4% in cases and 3.8% in control subjects.

Key Differences between Cases and Control Subjects

Characteristic Cases (n = 11)* Control Subjects (n = 208)* P Value
Mean age (y) 49.7 ± 16.5 60.3 ± 10.8 .031
Mean BMI (kg/m2) 29.36 ± 6.4 29.47 ± 5.09 .95
Mean calcium score 209 ± 254 482 ± 786 .008
Regional wall motion abnormality 7 (63.6) 38 (18.2) .0017
Elevated troponin level at presentation 3 (27.3) 2 (0.1) .001
ACS 5 (45.4) 8 (3.8) .001
Traditional high-risk plaque features 2 (18.2) 118 (56.7) .02
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Note.—ACS = acute coronary syndrome, BMI = body mass index.

*

Except where indicated, data are numbers of subjects, with percentages in parentheses.

The frequency of occlusive disease was greater in cases with fat stranding (54.5%, six of 11 cases) than in control subjects (8.6%, 18 of 208 subjects). The Fisher tests for wall motion abnormality and troponin level were repeated for the subgroups having occlusive disease as the worst lesion. A regional wall motion abnormality was seen in six of seven cases with perivascular fat stranding (85.7%) and four of 24 control subjects (16.7%) (P = .006).

Eight of the 11 cases with perivascular fat stranding underwent invasive coronary angiography, which showed severe stenosis in four cases and occlusion in four. In six cases, the severity was in full agreement with findings at CT angiography. In the remaining two cases, one stenosis was upgraded to occlusion from severe with invasive coronary angiography and one stenosis was downgraded to severe from occlusion. No cardiovascular mortality was observed in 155 subjects (eight cases and 147 control subjects) who completed a follow-up of 120 days after the initial event.

Discussion

In this study, we investigated the frequency and clinical implications of an imaging finding, perivascular epicardial fat stranding, at coronary CT angiography performed for suspected ACS. We found a prevalence of 5% in subjects with moderate or higher grades of stenosis (CAD-RADS 3–5) or SCAD. Fat stranding was found to be significantly associated with high-risk clinical features, including elevated troponin level at baseline and regional ventricular wall motion abnormality. These findings suggest that fat stranding is a potential imaging risk indicator of high-risk or ruptured plaques. In addition, fat stranding was seen in relatively younger patients with a lower Agatston score, predominantly along the proximal right coronary artery, as well as in patients with SCAD.

Rupture of vulnerable plaques is thought to be the cause of ACS, which is responsible for approximately 75% of coronary thrombi that lead to myocardial infarction and/or death (14–16). Vulnerable plaques that tend to rupture are generally large, with a large lipid core, inflammatory cell infiltration (7,17), neovascularity (16), and intraplaque hemorrhage (18). Although atherosclerosis is an intimal disease, inflammation beyond the intima has been described in patients with ACS (19). This inflammation beyond the intima, even though clearly reported in the pathology literature, has, to our knowledge, not been described in imaging with CT angiography in patients presenting to the emergency department with acute chest pain.

SCAD results from a nontraumatic, non-iatrogenic tear in the intimal layer of an artery leading to the intrusion of blood within the layers of an arterial wall or rupture of vasa vasorum (20). At coronary CT angiography, SCAD may demonstrate intramural hematoma, dissection flap, and coronary stenosis (21). Involvement of the media and adventitial extension have been described in arterial dissections (22,23). Kohchi et al (24), in an autopsy study, described adventitial inflammation associated with atherosclerotic plaques in patients with unstable angina. Moreno et al (25) found that intimomedial interface changes, medial inflammation, and fibrosis are associated with disrupted plaques. Adventitial inflammation has been suggested as a marker of plaque vulnerability (25,26). Litovsky et al (27) studied the superparamagnetic iron oxide uptake in macrophages associated with atherosclerotic plaques. They reported that nanoparticles are taken up not only by the plaque macrophages but also by macrophages in periadventitial fat and suggested that adventitia and periadventitial fat behave as a single physiologic unit in the inflammatory process (28). Perivascular fat plays an important role in the development of vascular inflammation and coronary atherosclerosis through bidirectional communication with the vessel wall at a cellular level (29). Recently, the average attenuation of the fat surrounding the coronary vessel was shown to be increased in patients imaged during the acute phase of myocardial infraction, likely owing to accumulation of inflammatory cells in the perivascular space, a pattern different than fat attenuation in patients with stable plaques (30).

In our study, a corresponding regional wall motion abnormality was present in 63% of patients with fat stranding (compared with 18% of control subjects); similarly, an elevated troponin level was seen at baseline in 27.3% of patients with perivascular fat stranding (compared with <1% of control subjects). The prevalence of occlusive disease was higher in patients with fat stranding than in control subjects. The number of high-risk plaques in the control group was higher than that in the case group, which suggests that the finding of fat stranding is a marker of acuity and high risk. The association of fat stranding with regional wall motion abnormalities and elevated troponin level suggests an underlying high-risk and/or ruptured atherosclerotic plaque resulting in myocardial ischemia or infarction.

The lower mean calcium score in cases than in control subjects could be attributable to a lower mean age or the inclusion of subjects with SCAD, who tend to have no calcified or noncalcified plaque in addition to being younger with a distinct risk profile that frequently includes extracoronary vascular abnormalities such as medial fibroplasia and/or fibromuscular dysplasia.

In most instances (10 of 12 segments), fat stranding was seen along the right coronary artery and in proximal segments. Various factors could contribute to this trend. First, it could be related to the distribution of fat in the epicardium. The right coronary artery has more surrounding fat compared with other coronary arteries and runs perpendicular to the axial acquisition in its mid segment, whereas the smaller distal branches have minimal surrounding perivascular fat (31). Second, myocardial bridging of LAD segments would limit the detection of fat stranding owing to the absence of surrounding fat (and rather in these bridged segments, surrounding muscle tissue). Finally, the circumflex coronary artery and LAD have comparatively less fat around them and have accompanying veins tracking along them, which might limit the ability to detect this finding; their more horizontal course (particularly in the proximal LAD and obtuse marginal branches) may make the fat stranding less apparent upon review of axial images (noting that our research interpretations were performed as a three-dimensional multiplanar workstation review in an effort to avoid this limitation).

The prevalence of fat stranding was found to be very low (5%) in patients with moderate or higher stenosis grades or SCAD. Fat stranding is likely associated with high-risk and/or ruptured plaques, and conventionally high-risk patients are subjected to early invasive coronary angiography instead of initial coronary CT angiography (6), which might explain the low frequency of this finding in our study cohort. We speculate that this may change as the proportion of disease shifts upon availability of high-sensitivity troponin (32).

This study has some limitations. The small number of cases with perivascular fat stranding and the retrospective design are the most important limitations of this study. Motion artifacts were common distractors while evaluating images for the presence of fat stranding. Review of multiple phases of the cardiac cycle at 20-msec intervals per our institution’s protocol was useful to differentiate between motion artifact and true stranding (10). Bridged segments of vessels, especially the LAD, could not be assessed because these segments lack surrounding epicardial fat, although atherosclerotic plaques tend to be in the segment proximal to the bridge itself but can of course occur in segments with myocardial bridges (33). Last, it would be more interesting to compare the calcium within the individual plaques to evaluate the association of this finding with lipid-rich versus calcified plaques, as lipid-rich plaques are considered more vulnerable (12). This is a limitation of this study as calcium scores compared are overall scores, including all possible lesions for a particular subject.

In conclusion, perivascular epicardial fat stranding has the potential to improve the diagnostic sensitivity of coronary CT angiography and alert the physician to a higher-risk patient or a nonatherosclerotic cause of stenosis (ie, SCAD). Perivascular fat stranding was seen in 5% of low-to-intermediate pretest risk patients found to have moderate or higher degrees of stenosis (CAD-RADS 3–5) and was seen less commonly along with the classic high-risk plaque features (vulnerable plaque, CAD-RADS modifier V). Recognition of perivascular fat stranding may be helpful in identifying the culprit lesion, SCAD, and patients at elevated risk for ACS.

Supplementary Material

Table E1

Abbreviations:

ACS

acute coronary syndrome

CAD-RADS

Coronary Artery Disease Reporting and Data System

CI

confidence interval

LAD

left anterior descending artery

SCAD

spontaneous coronary artery dissection

Footnotes

Conflicts of interest are listed at the end of this article.

Disclosures of Conflicts of Interest: S.H. disclosed no relevant relationships. V.B. disclosed no relevant relationships. E.J.Z. disclosed no relevant relationships. D.O.B. disclosed no relevant relationships. P.V.S. disclosed no relevant relationships. R.A.P.T. disclosed no relevant relationships. J.E.S. disclosed no relevant relationships. N.M. disclosed no relevant relationships. U.H. Activities related to the present article: disclosed no relevant relationships. Activities not related to the present article: received grants for research support from MedImmune, Kowa, Siemens Healthcare, and HeartFlow. Other relationships: disclosed no relevant relationships. B.G. Activities related to the present article: received a grant from Siemens Healthcare. Activities not related to the present article: received consulting fees from Siemens Healthcare and Medtronic. Other relationships: disclosed no relevant relationships.

Online supplemental material is available for this article.

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Supplementary Materials

Table E1
NIHMS1058389-supplement-Table_E1.pdf (106.7KB, pdf)

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