Serial Contrast-Enhanced Cardiac Magnetic Resonance Imaging Demonstrates Regression of Hyperenhancement Within the Coronary Artery Wall in Patients After Acute Myocardial Infarction
Tareq Ibrahim, MD*,
Markus R. Makowski, MD ,
Antanas Jankauskas, MD,
David Maintz, MD ,
Martin Karch, MD*,
Sylvia Schachoff, RT,
Warren J. Manning, MD ,
Albert Schömig, MD*,
Markus Schwaiger, MD,
Rene M. Botnar, PhD,*
* Deutsches Herzzentrum München and 1. Medizinische Klinik des Klinikums Rechts der Isar, Technische Universität München, München, Germany
Nuklearmedizinische Klinik und Poliklinik der Technischen Universität München, München, Germany
Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts
Radiologische Klinik, Universität Münster, Münster, Germany
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Abstract
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Objectives: Our aim was to determine whether serial contrast-enhanced cardiac magnetic resonance (CE-CMR) is useful for the characterization of tissue signal changes within the coronary vessel wall in patients after acute myocardial infarction (AMI).
Background: Inflammation plays a key role in the development of AMI. CE-CMR of the vessel wall has been found useful for the characterization of inflammatory tissue signal changes in patients with carotid artery stenosis, giant cell arteritis, or Takayasu's arteritis; however, it has never been serially performed in the coronary artery wall in patients with acute and chronic myocardial infarction using a gadolinium-based contrast medium and compared with systemic markers of inflammation.
Methods: CE-CMR using a T1-weighted 3-dimensional gradient echo inversion recovery sequence of the coronary artery wall and 0.2 mmol/kg of gadolinium-diethylenetriaminepentaacetic acid was performed in 10 patients with AMI 6 days and 3 months after coronary intervention and in 9 subjects without coronary artery disease on invasive coronary angiography. Contrast-to-noise ratio (CNR) within the coronary artery wall was quantified in comparison with blood signal.
Results: Patients with AMI demonstrated a significantly increased coronary vessel wall enhancement 6 days after infarction compared with normal subjects (CNR 7.8 ± 4.4 vs. 5.3 ± 3.2, p < 0.001). Three months after infarction, CNR decreased to 6.5 ± 4.7 (p < 0.03). This decrease paralleled declines in C-reactive protein. Angiographically normal segments showed no contrast changes, but CNR significantly decreased in stenotic segments, from 10.9 ± 3.8 to 6.8 ± 5.0 (p < 0.002), resulting in a reduction of enhanced segments from 70% to 25% (p < 0.01).
Conclusions: Serial CE-CMR identified changes in spatial extent and intensity of coronary contrast enhancement in patients after AMI. This technique may be useful for the characterization of transient coronary tissue signal changes, which may represent edema or inflammation during the post-infarction phase. In addition, CE-CMR may offer the potential for visualization of inflammatory activity in atherosclerosis associated with acute coronary syndromes.
Key Words: cardiac magnetic resonance • late enhancement • coronary artery • acute myocardial infarction
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Abbreviations and Acronyms
| | ACS = acute coronary syndromes | | AMI = acute myocardial infarction | | CAD = coronary artery disease | | CE-CMR = contrast-enhanced cardiac magnetic resonance | | CRP = C-reactive protein | | LCA = left coronary artery | | LCX = left circumflex artery | | SI = signal intensity |
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Atherosclerotic cardiovascular disease is the leading cause of mortality and morbidity in developed countries (1). Inflammation plays a key role in the initiation, progression, and complication of atherosclerosis (2) and is closely linked to coronary plaque rupture, the underlying pathogenesis of acute coronary syndromes (ACS) (3). Growing evidence suggests that the decisive factor determining plaque vulnerability is plaque composition and inflammatory activity rather than the degree of luminal narrowing (4). Angiography often underestimates the true burden of disease and does not provide any information with regard to plaque activity. In addition, high-risk plaques of the coronary arteries are often associated with positive lumen preserving remodeling (5) and, therefore, a priori detection by X-ray angiography or scintigraphic techniques is ambiguous.
Cardiac magnetic resonance (CMR) has shown great promise for noninvasive imaging and characterization of the coronary atherosclerotic plaque (6). Native coronary CMR vessel wall imaging has provided assessment of arterial remodeling in patients with coronary artery disease (CAD) (7–9), but widespread use of this technique is limited by long scan times and the need for high spatial resolution.
Contrast-enhanced CMR (CE-CMR) using extracellular gadolinium contrast agents represents an alternative imaging approach that may offer morphological as well as functional assessment of atherosclerotic plaque formation. This technique is flow insensitive and relatively fast and therefore potentially more robust than noncontrast-enhanced CMR vessel wall imaging. Furthermore, the imaging task is reduced to detect the presence or absence of contrast uptake, thereby lowering spatial resolution requirements. CE-CMR has been found useful for the characterization of fibrous plaque tissue and neovascularization in patients with advanced carotid artery stenosis (10–13). Preliminary data in patients with stable CAD have demonstrated that CE-CMR provides selective plaque visualization in the major coronary arteries in comparison to multidetector computed tomography (14,15).
Because extracellular contrast agents are nonspecific, this technique also allows for the characterization of acute inflammation within the vessel wall, as has been demonstrated in giant cell arteritis or Takayasu's arteritis (16,17). Whether coronary enhancement may also reflect an inflammatory component is not known, as ACS patients have not been examined.
In this study, we sought to evaluate coronary CE-CMR vessel wall imaging in patients with acute myocardial infarction (AMI). To assess potential changes of atherosclerotic plaque signal, CE-CMR was serially performed during the post-infarct phase.
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Methods
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Study populations.
We prospectively enrolled 10 patients (9 men, age 56.5 ± 4.9 years) with AMI with an onset of symptoms <48 h. Diagnosis of AMI was based on the presence of acute chest pain lasting for at least 20 min, characteristic electrocardiographic changes (ST-segment elevation or depression) as well as elevation of troponin T. All patients underwent successful percutaneous coronary intervention with stenting (drug-eluting stent) of the infarct-related artery on the day of admission. To be included, patients had to be hemodynamically stable and to have no contraindication to CMR. All patients were examined twice by CMR, 6 ± 3 days and 93 ± 40 days after reperfusion. During this period, no patient had clinical evidence of recurrent myocardial infarction, and all received medical therapy consisting of aspirin, clopidogrel, beta-blocker, angiotensin-converting enzyme inhibitor, and statins. Nine subjects (5 men, age 61.7 ± 9.5 years) without angiographically detectable CAD served as controls. CMR in the control group was performed 3 ± 2 days after elective X-ray coronary angiography. The study protocol was reviewed and approved by the local ethics committee for clinical investigations. Written informed consent was obtained before inclusion in the study.
Image acquisition.
All subjects were scanned in the supine position on a 1.5-T magnetic resonance scanner (Gyroscan Achieva, Philips Medical Systems, Best, the Netherlands) with a 5-element cardiac synergy coil and an advanced cardiovascular software package (R11, Philips Medical Systems).
Before imaging, 0.2 mmol/kg of gadolinium-diethylenetriaminepentaacetic acid (DTPA) (Magnevist, Bayer-Schering, Berlin, Germany) was administered intravenously using a bolus injection. Coronary CMR of the right and left system was then performed using a previously described free-breathing navigator-gated and corrected electrocardiography-triggered 3-dimensional (3D) balanced steady-state free precession coronary CMR sequence (18). Imaging parameters included field of view = 320 x 320 mm, matrix = 256 x 256, acquired in-plane resolution = 1.25 x 1.25 mm, reconstructed slice thickness = 1.5 mm (acquired: 3 mm), acquisition window = 80 to 100 ms, repetition time/echo time = 4.2 ms/2.1 ms, flip angle = 110°, startup cycles = 5, and number of slices = 24. Immediately after coronary lumen imaging, CE-CMR coronary artery wall imaging (targeted slab acquisition) was performed using a T1-weighted 3D gradient echo inversion recovery sequence (3D IR TFE) (19,20). Because of scout scans, including coronary lumen scans, the time delay between contrast injection and CE-CMR was approximately 30 to 40 min. Imaging parameters, including imaging plane and voxel size, were identical to the coronary CMR sequence, except for TR/TE = 6.1/1.9 ms, flip angle = 30°, and a nonselective inversion radiofrequency pulse instead of T2 preparation for magnetization preparation. The patient-specific inversion time (range 250 to 280 ms) was adjusted to null blood (using a region of interest to determine the most accurate value) using a Look Locker sequence. Owing to time constraints, only post-contrast imaging was performed. However, previous studies showed no enhancement before contrast injection in healthy subjects (15).
Image analysis.
CE-CMR and X-ray coronary angiography were compared according to an 8-segment model (Fig. 1). For CE-CMR, multiplanar reformatted images were analyzed by a blinded observer (A.J.) who was unaware of the patient's clinical and X-ray angiographic data. Segments with stents (metallic artifacts) and distal to stents (local field disturbance and Faraday shielding effect with inadequate blood nulling) were excluded from analysis. A contour was manually drawn in the ascending aorta to determine blood signal intensity (SI), and coronary wall SI was assessed in each segment and quantified with the use of dedicated post-processing software (21). Contrast enhancement within coronary or aortic vessel wall segments was defined as the contrast-to-noise ratio (CNR) between coronary or aortic wall signal (SIwall) and aortic blood signal: CNR = (SIwall – SIblood)/noise. Noise was determined in a region of interest placed ventrally to the patient's chest wall.
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Figure 1 Segmental Model for Comparison of Coronary Contrast-Enhanced Cardiac Magnetic Resonance and X-Ray Coronary Angiography
The coronary vessel tree was subdivided into 8 segments. For segment identification, segments were pre-defined according to distance from coronary origin. The right coronary artery (RCA) was analyzed in 3 segments (1, 2, and 3), the left coronary artery (LCA) within the left main artery (5), the left anterior descending (6 and 7), and the circumflex artery (11 and 13).
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The X-ray coronary angiography was performed using standard techniques with multiple projections. Coronary angiograms were evaluated by 2 experienced cardiologists (T.I. and M.K.) who were blinded to clinical data and CMR results. The presence of lumen narrowing was classified visually by consensus on a segment-by-segment basis using the following scheme: 0 = none, 1 = 1% to 24%, 2 = 25% to 50%, and 3 = >50% stenosis. Coronary artery stenosis was defined by a segment score of  2. Suppression of coronary blood signal facilitated good delineation of the enhancing coronary vessel wall segments. To highlight the anatomic relationship between contrast enhancement and morphology, images were fused in a way similar to positron emission tomography/computed tomography (Figs. 2D, 2H, and 2L).
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Figure 2 CMR Findings
Control population: data are shown from a 52-year-old subject with a normal right coronary artery (RCA) on (A) X-ray angiography and (B) coronary magnetic resonance angiography (MRA) without contrast uptake on (C) contrast-enhanced cardiac magnetic resonance (CE-CMR). To highlight the anatomic relationship between contrast enhancement and morphology, images were fused in a way similar to positron emission tomography/computed tomography (D). Data are shown from a 56-year-old patient with anterior myocardial infarction and luminal irregularities (arrow) of the RCA on X-ray angiography (E). Coronary MRA (F) 10 days after acute myocardial infarction (AMI) confirms this finding; and CE-CMR (G, H) revealed diffuse strong contrast enhancement (white arrow) in the corresponding vessel segments. Note the excellent suppression of blood signal (dotted white arrows). Data are shown from the left coronary artery system of the same patient with a stent in the proximal left anterior descending artery (LAD) on (I) X-ray angiography and (J) corresponding coronary MRA, demonstrating a signal void at the location of the stent (arrow). On CE-CMR, focal enhancement (K, L) can be observed proximal to the stent and in the proximal left circumflex artery (LCX) (dotted arrows). LV = left ventricle.
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Statistical analysis.
For statistical analysis, SPSS software (SPSS version 12.0, SPSS Inc., Chicago, Illinois) was used. Results are expressed as mean ± SD. An unpaired Student t test was applied for the comparison of continuous variables between subjects without and patients with CAD. For serial assessment of CNR in patients with CAD, the paired Student t test was used. The Kruskal-Wallis test was used for the correlation of CNR according to severity of coronary stenosis. Categorical variables were compared by Fisher exact test. Receiver-operating characteristic (ROC) analysis was performed in AMI patients at baseline to define the threshold for increased coronary contrast enhancement (CNR) by CE-CMR according to the presence of coronary artery stenosis (25%) on X-ray angiography. All tests were 2-sided, and a value of p < 0.05 was considered to indicate statistical significance.
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Results
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Patient characteristics.
Clinical and angiographic characteristics of the study populations are summarized in Table 1. In patients with AMI, infarct was located in the anterior (n = 4), inferior (n = 4), and lateral (n = 2) wall. Eighty percent showed ST-segment elevation at presentation, and 90% were classified according to Killip class 1 criteria; 1 patient met Killip class 2 criteria. During AMI, inflammatory markers were significantly increased compared with subjects without CAD (Table 1). Although C-reactive protein (CRP) levels at baseline were elevated in 9 of 10 infarct patients, all except 1 patient showed normal levels at follow-up.
CE-CMR analysis.
CMR scans were successfully performed in all subjects. In controls, contrast enhancement within the coronary vessel wall was assessable in 71 of 72 (98.6%) of the segments. The distal part of the right coronary artery (segment 3) was not visible on CE-CMR in 1 subject. In patients with AMI, 20% (16 of 80) of the segments could not be analyzed by CE-CMR. The most common reason was the presence of implanted stents (15 of 80), and in 1 patient, the distal right coronary artery segment was not detectable.
Baseline CE-CMR in AMI patients.
Six days after AMI, the strength of coronary contrast enhancement as defined by the CNR averaged over all segments was 7.8 ± 4.4 and was significantly higher compared with normal subjects (5.3 ± 3.2, p < 0.001) (Figs. 2 and 3). Coronary contrast enhancement significantly correlated with the angiographic severity of lumen narrowing (p < 0.001). Coronary segments with stenosis had a significantly increased CNR compared with nonstenotic segments (CNR 10.9 ± 3.8 vs. 6.4 ± 3.9, p < 0.001). Based on an ROC curve analysis, a CNR threshold of 9.7 (hyperenhancement) was determined for detection of stenotic coronary segments by CE-CMR (area under the curve 0.81, sensitivity 70%, specificity 86%). This threshold was used to distinguish between stenotic and nonstenotic segments. For the descending aortic vessel wall, a mean CNR of 12.2 ± 5.0 was measured.
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Figure 3 Contrast-to-Noise Ratio at Baseline and Follow-Up
Comparison of the average contrast-enhanced cardiac magnetic resonance contrast enhancement within the coronary artery wall in patients 6 days (baseline) and 3 months (follow-up) after acute myocardial infarction (AMI) as well as in subjects without coronary artery disease (CAD).
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Follow-up CE-CMR in AMI patients.
Three months after AMI, coronary CNR was 6.5 ± 4.7, and was reduced as compared with 6-day data (p < 0.03) (Figs. 4 and 5). Although CNR did not change in angiographically normal segments between the acute and chronic phase of infarction, stenotic segments revealed a significant decrease in signal intensity (CNR 6.8 ± 5.0 vs. 10.9 ± 3.8, p < 0.002) and spatial extent of hyperenhanced segments (25% vs. 70%, p < 0.01) (Fig. 5). For the descending aortic vessel wall, a mean CNR of 10.3 ± 6.4 was measured, which was not significantly different from the acute post-infarct phase.
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Figure 4 Time Course of Coronary Enhancement
Infarct population: data are shown from a 55-year old patient with lateral AMI (troponin T 7.3 ng/ml). To highlight the relationship between contrast enhancement and morphology, images were fused. (A) Coronary MRA of the left coronary system shows a stent artifact within the LCX. (A, E) CE-CMR 10 days after AMI displays diffuse contrast uptake within the proximal LAD and LCX as well as in the ascending and descending aorta. The C-reactive protein (CRP) at that time was 3.7 mg/dl. (B, F) Follow-up CE-CMR 3 months after AMI displays a marked decrease of hyperenhancement within the ascending and descending aorta, the LCX, and to a lesser degree, within the LAD while CRP returned to normal levels. (C) Coronary MRA of a 62-year-old patient with inferolateral infarction (troponin T 2.0 ng/ml) shows a luminal stenosis within the proximal LAD (arrow) that corresponds to a 50% stenosis on X-ray angiography. (C, G) CE-MRA 5 days after infarction revealed contrast uptake within the entire proximal LAD (CRP 3.5 mg/dl). (D, H) Four months after AMI, coronary enhancement was markedly reduced within the proximal LAD while the stenotic region still showed some enhancement (arrows). CRP levels were normal at the follow-up scan. Abbreviations as in Figure 2.
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Figure 5 Segmental CE-CMR Coronary Artery Wall Enhancement
Segmental contrast-enhanced cardiac magnetic resonance (CE-CMR) coronary artery wall enhancement in patients 6 days (baseline) (brown bars) and 3 months (follow-up) (orange bars) after myocardial infarction according to X-ray angiography findings. (Top) At baseline, coronary contrast enhancement significantly correlated with the angiographic severity of lumen narrowing (p < 0.001). At follow-up, a significant decrease in hyperenhancement was noted in stenosed coronary segments, while normal segments showed no changes. (Bottom) Prevalence of hyperenhancement significantly decreased in stenotic segments between baseline and follow-up CE-CMR.
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Discussion
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To the best of our knowledge, this is the first study of serial assessment of the coronary artery wall in infarct patients by CE-CMR using a gadolinium-based contrast medium. We found that in patients early after AMI, coronary wall contrast uptake is significantly increased as compared with normal subjects, and correlates with the degree of lumen narrowing by X-ray angiography. CE-CMR 3 months after AMI revealed a significant reduction of contrast uptake in stenotic segments, and the overall systemic inflammatory activity was decreased as measured by CRP. The observed CE-CMR contrast pattern during the post-infarction period may be associated with transient inflammation or edema in the pathologically altered coronary vessel wall.
CE-CMR in advanced atherosclerosis.
Atherosclerosis is a chronic inflammatory disease of the vessel wall affecting different vascular regions such as the aorta, carotid arteries, run-off vessels, and coronary arteries. It is associated with endothelial activation, intimal thickening, extracellular matrix disorganization, and accumulation of inflammatory cells (monocytes/macrophages, T cells), smooth muscle cells, and low-density lipoproteins within the arterial vessel wall (2). Gadolinium-based contrast media are nonspecific, and the underlying mechanisms leading to contrast enhancement within the atherosclerotic vessel wall are so far not fully elucidated. These agents are known to passively distribute from the intravascular to the extracellular fluid space. Contrast enhancement within atherosclerotic plaque may be due to increased wash-in, increased distribution volume, and/or decreased washout of contrast agent molecules (11). The main components of atherosclerotic plaques that may potentially contribute to contrast enhancement are the extracellular matrix (collagen, proteoglycans, elastic fibers), lipids (cholesterol, phospholipids), and inflammation (macrophages, T lymphocytes).
CE-CMR and histology studies in patients with advanced carotid atherosclerosis have shown that the enhancement pattern varies in different plaque components (10,11). Strong enhancement is particularly associated with fibrous plaque tissue whereas the necrotic core only minimally enhances (10). CE-CMR enhancement of fibrosis has been extensively described in various organ systems and is clinically commonly used to assess myocardial viability in patients with chronic CAD (22). Preliminary data in patients with stable CAD that compared CE-CMR with CT-findings have indicated that contrast enhancement occurs in fibrous-rich and calcified coronary plaques (14,15). Although these studies did not directly compare CE-CMR with histology, it is likely that the observed contrast enhancement may be related to fibrosis as has been described in atherosclerotic carotid artery tissue.
CE-CMR 6 days after AMI.
In this study, we demonstrated that patients with AMI display a significantly increased contrast enhancement of the coronary artery wall as compared with aged-matched subjects without CAD. When coronary segments were classified according to X-ray angiography, there was higher enhancement among stenotic (25%) segments, which increased with the degree of luminal stenosis. Our data are in agreement with those of previous studies in patients with stable CAD that also demonstrated progressive coronary enhancement with increasing severity of atherosclerosis (15).
CE-CMR 3 months after AMI.
Probably the most interesting observation of this study was the decrease of contrast enhancement within the coronary vessel wall at the 3-month post-infarction scan, whereas no significant change of contrast enhancement was found in the aortic vessel wall. Because of the short period between both CE-CMR studies, it is not very likely that this finding is related to plaque volume regression but rather is associated with a regression of systemic inflammation.
Vessel wall enhancement by CE-CMR has been observed in various inflammatory disorders of the vascular system such as Takayasu's arteritis (17) or superficial temporal arteritis (16), and serial CE-CMR has been successfully used in other organ systems for the characterization of inflammatory activity. For instance, patients with myocarditis demonstrated a myocardial contrast enhancement in areas of acute inflammation that decreased on follow-up CE-CMR during the chronic stage of disease (23).
The increased CRP levels in our study population at baseline declined during the post-infarction period, which may further support a potential link between inflammation or edema and the CE-CMR findings. Inflammation is recognized as a major contributor to the acute manifestations of atherosclerosis (24), and elevation of inflammatory markers such as CRP is a common finding in ACS (25). However, whether CRP release in the acute setting is directly related to vascular inflammation or predominantly a response to myocardial necrosis is subject to debate (26). It, therefore, remains unclear whether the tissue signal changes measured are due to vascular inflammation or edema, or whether it is a secondary effect to AMI.
Limitations of CE-CMR.
As inflammation (16), edema (27), and fibrosis (22) are associated with hyperenhancement using extracellular contrast agents, differentiation based on the visual appearance remains difficult. Differentiation between these conditions may be potentially possible using differences in the pharmacokinetics of contrast wash-in and wash-out. For instance, early and dynamic post-contrast imaging may be helpful to characterize inflammation due to the increased permeability and wash-in (28). Further studies are warranted that account for specific timing of CMR after contrast application. Moreover, the development of new magnetic resonance contrast agents that allow the targeted imaging of plaque components associated with inflammation (29,30) or the confirmation of these findings with macrophage-targeting iron oxides (31) will give further insights in the characterization of coronary atherosclerotic lesions in the future.
Study limitations.
Patients with AMI were not imaged by CE-CMR before intervention for ethical reasons. Therefore, the underlying culprit lesion leading to infarction could not be evaluated in this study. Additionally, CE-CMR was not compared with intravascular ultrasound (IVUS), the current clinical gold standard for in vivo assessment of coronary plaque. Furthermore, it remains unclear whether the enhancement of the vessel wall observed in this study represents inflammation or edema, as no histologic specimens could be obtained.
Because of stent artifacts, the overall percentage of segments that could be evaluated by CE-CMR was reduced in patients with AMI. However, the inability of CMR in the assessment of coronary artery segments with bare-metal or drug-eluting stents is a general problem of CMR that might be solved by the use of MR lucent stents in the future (32).
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Conclusions
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In this study, we demonstrate a significant regression of coronary vessel wall enhancement in stenotic segments during the post-infarction period in patients with AMI that was paralleled by declines in CRP. Thus, serial CE-CMR may be useful for the assessment of tissue signal changes, which may represent transient coronary inflammation or edema in the post-infarction period. In addition, CE-CMR may offer the potential to visualize tissue signal changes, which potentially represent inflammatory activity or edema in atherosclerosis associated with ACS. Larger studies are now warranted to better understand the temporal and spatial change of coronary hyperenhancement by CE-CMR in patients with ACS and to understand its clinical impact.
* Reprint requests and correspondence: Rene M. Botnar, PhD, Division of Imaging Sciences, King's College London, 4th Floor, Lambeth Wing, St. Thomas' Hospital, London SE1 7EH, United Kingdom (Email: rene.botnar{at}kcl.ac.uk).
Manuscript received September 11, 2008;
revised manuscript received December 5, 2008,
accepted December 19, 2008.
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C. M. Kramer and J. Narula
Atherosclerotic Plaque Imaging: The Last Frontier for Cardiac Magnetic Resonance
J. Am. Coll. Cardiol. Img.,
July 1, 2009;
2(7):
916 - 918.
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D. Li, Z. A. Fayad, and D. A. Bluemke
Can contrast-enhanced cardiac magnetic resonance assess inflammation of the coronary wall?
J. Am. Coll. Cardiol. Img.,
May 1, 2009;
2(5):
589 - 591.
[Full Text]
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Abstract
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