Cardiac Magnetic Resonance in Rheumatology to Detect Cardiac Involvement Since Early and Pre-clinical Stages of the Autoimmune Diseases: A Narrative Review

Abstract

Autoimmune diseases (ADs) encompass multisystem disorders, and cardiovascular involvement is a well-known feature of autoimmune and inflammatory rheumatic conditions. Unfortunately, subclinical and early cardiovascular involvement remains clinically silent and often undetected, despite its well-documented impact on patient management and prognostication with an even more significant effect on severe and future MACE events as the disease progresses. Cardiac magnetic resonance imaging (MRI), today, commands a unique position of supremacy versus its competition in cardiac assessment and is the gold standard for the non-invasive evaluation of cardiac function, structure, morphology, tissue characterization, and flow with the capability of evaluating biventricular function; myocardium for edema, ischemia, fibrosis, infarction; valves for thickening, large masses; pericardial inflammation, pericardial effusions, and tamponade; cardiac cavities for thrombosis; conduction related abnormalities and features of microvascular and large vessel involvement. As precise and early detection of cardiovascular involvement plays a critical role in improving the outcome of rheumatic and autoimmune conditions, our review aims to highlight the evolving role of CMR in systemic lupus erythematosus (SLE), antiphospholipid syndrome (APS), rheumatoid arthritis (RA), systemic sclerosis (SSc), limited sclerosis (LSc), adult-onset Still's disease (AOSD), polymyositis (PM), dermatomyositis (DM), eosinophilic granulomatosis with polyangiitis (EGPA) (formerly Churg-Strauss syndrome), and DRESS syndrome (DS). It draws attention to the need for concerted, systematic global interdisciplinary research to improve future outcomes in autoimmune-related rheumatic conditions with multiorgan, multisystem, and cardiovascular involvement.

Keywords: antiphospholipid; autoimmune disease; cardiac MRI; fibrosis; late gadolinium enhancement; lupus; rheumatoid arthritis; thrombosis.

Figure 1

Algorithm of representative rheumatological disorders. This figure shows an algorithm created using the published literature that includes most rheumatological disorders. The algorithm is divided into six big categories as systemic and localized (both with autoantibodies), one group secondary to hypersensitivity, another large group of diseases of unknown etiology (with or without autoantibodies) which mainly involve spondyloarthropathies and vasculitides (34), one group of genetic origin and finally a group of other sub-groups of disorders such as those related to neoplasias, infectious and metabolic diseases. By looking at the algorithm, it is comprehensive that one general review paper could not go into detail for each component. Therefore, we chose to describe the most frequent diseases with known cardiovascular involvement from the systemic with autoantibodies groups, such as those underlined ones—one representative illness of the group of spondyloarthropathies and one from the group of vasculitides. Finally, one infrequent, maybe underdiagnosed disease such as the DRESS syndrome from the group of diseases secondary to hypersensitivity. SLE, systemic lupus erythematosus; APS, antiphospholipid syndrome; SSc, systemic sclerosis; RA, rheumatoid arthritis; DM, diabetes mellitus; TA, Takayasu arteritis; GCA, giant cell arteritis; PAN, polyarteritis nodosa; KD, Kawasaki disease; ANCA AAV, Antineutrophil cytoplasmic antibody (ANCA)-associated vasculitis (AVV); MPA, microscopic polyangiitis; EGPA, eosinophilic granulomatosis with polyangiitis (formerly Churg-Strauss syndrome); GPA, granulomaotsis with polyangiitis (Wegener's); SVV, small vessel vasculitis; CV, cryoglobulinemic vasculitis; IgAV, IgA vasculitis (Henoch-Schönlein); HUV, hypocomplementemic urticarial vasculitis (anti-C1q vasculitis); CS, Cogan's syndrome; BS, Behcet's syndrome.

Figure 2

(A) CMR findings in SLE—(A) from an arrhythmic perspective. A panel figure demonstrates the array of findings from a comprehensive CMR study in SLE from an arrhythmia perspective. (A.a) Shows normal global and regional right and left ventricular functions in SSFP sequence still cine images in short-axis views at the mid-ventricular level in end-diastole (A.a.1) and end-systole (A.a.2) LVEF 66% and RVEF 63%. (A.b) T2-W STIR sequence in short-axis view projection at a mid-ventricular level demonstrating mildly increased signal intensity in the anterior, anteroseptal, and inferoseptal segments (arrow) with a myocardial/skeletal muscle ratio of 2.8 and (A.f) a color-coded T2 mapping (native T2 value of 48 ms) consistent with myocardial edema. (A.c) Stress CMR with FPP T1-W sequence with adenosine infusion at 140 mcg/kg/min over 6 minutes shows a subendocardial ring perfusion defect (arrowheads) consistent with subendocardial ischemia due to endothelial dysfunction and probably microvascular disease (no obstructive coronary artery disease in CCTA). (A.d.1) LGE PSIR sequence. (A.d.1–3) short-axis views at basal (A.d.1), mid (A.d.2) and apical (A.d.3) levels, and long-axis views in 4-chambers (A.d.4,6) and 3-chambers (A.d.5) projections. The arrows in these images show areas of focal fibrosis in the subepicardium in the inferior segments in (A.d.1–3) from the base to the apex. (A.d.4,5) shows areas of midventricular LGE in basal anteroseptal and inferoseptal segments (arrows) and subepicardial enhancement in mid and apical inferolateral segments (arrow). (A.d.6) A zoomed image of the 4-chambers view showing LGE suggestive of LA fibrosis (arrow). (A.h) A polygraphic trace of an EP study showing atrial fibrillation successfully ablated. (A.e.1–3) SSFP sequence still cine images in long-axis views, showing in a 3-chambers view an isointense, small nodule, in the ventricular side of the mitral valve suggestive of Libman-Sacks endocarditis (arrow) (confirmed by echo) (A.e.1), in a 2-chambers view, a mildly thickened mitral valve (A.e.2) and in a color-coded 4-chambers (A.e.3) the presence of tricuspid regurgitation (arrow). (A.g) An SSFP sequence still cine images in true axial view showing bilateral pleural effusion (asterisks). SLE, systemic lupus erythematosus; CMR, cardiovascular magnetic resonance; SSFP, steady-state free precession; LVEF%, left ventricular ejection fraction; RVEF%, right ventricular ejection fraction; T2-W STIR, T2-weighted short-tau inversion recovery; FPP, first-pass perfusion; T1-W, T1-weighted; CCTA, invasive coronary angiography; LGE, late gadolinium enhancement; PSIR, phase-sensitive inversion recovery; LA, contrast enhancement magnetic resonance angiography; EP, electrophysiology. (B) CMR findings in SLE—(B), from a thrombotic perspective. A panel figure demonstrates the array of findings from a comprehensive CMR study in a 1.5 T scanner of SLE from a coronary thrombosis perspective. (B.a.1–4) SSFP sequence still cine images in short-axis views at mid to apical ventricular level in end-diastole (A.a.1) and end-systole (A.a.2) and long-axis 3-chambers view, in end-diastole (B.a.3) and end-systole (B.a.4) that shows in (A.a.1) the loss of continuity of the LV anterior segment (yellow arrow), with normal thickening of the remaining segments (B.a.2) surrounded by a large pericardial effusion (black asterixis), that exhibits hemodynamic compromise as the diastolic collapse of the LA [yellow arrow in (B.a.3,4)]. LVEF 42% and RVEF 65%. (B.b,c) Show the tissue characterization findings. (B.b.1) T1-W sequence in long-axis view demonstrating a wide-necked outpouching of the LV anterior wall with the apparent loss of myocardial continuity with a thinned out, fibrosed muscle surrounding the cavity consistent with true aneurysm (yellow arrow) with tissue within the aneurysmal cavity of two different intensities (yellow asterisks) suggestive of thrombus. (B.b.2) T2-W STIR sequence in long-axis view confirming the findings of T1-W sequences (yellow arrow) with the evident different signal intensity of the tissue components inside the aneurysmal cavity (black asterixis) suggestive of two varying ages of the thrombus, recent and old, and slow-flowing blood. (B.c) LGE PSIR sequence. (B.d.1) Long-axis 3-chambers view showing loss of myocardial continuity, a large cavity surrounded by scarred myocardium (green arrow) with a large thrombus on its endocardial aspect (white asterisks), pericardial enhancement (orange arrow), and a large pericardial effusion (yellow double asterisks) that are confirmed on the corresponding short-axis view (B.c.2). (B.c.3) A long TI LGE-PSIR long-axis 3-chambers view confirming previous data and showing the new thrombus component (yellow asterisks). (B.d.1) An invasive angiography demonstrating a total occlusion of the proximal LAD (arrow) and the invasive ventriculography (B.d.2) Showing a large leak of contrast media at an anterior mid-ventricular level impossible to differentiate aneurysm from pseudoaneurysm. (B.e.1) Open heart surgery showing the intact LV wall covered by the pericardium consistent with a true aneurysm (arrow) which was successfully resected (B.e.2), and surgery confirmed CMR findings, a ventricular aneurysm (B.e.2.a,b), a transmural scar (B.e.2.e) and a large thrombus (B.e.2.c) composed of two different aged thrombi (B.e.2.d). H.E. stain histology confirmed the presence of a large scar with no evidence of atherosclerosis (B.f.1). Based on the inflammatory component of the pericardium, suspicion of autoimmune instead of atherosclerotic etiology was suspected and confirmed by the finding of ANA with a homogeneous pattern in the pericardial effusion (B.g.1) and peripheral blood of a fine speckled pattern (B.g.2). SLE, systemic lupus erythematosus; CMR, cardiovascular magnetic resonance; SSFP, steady-state free precession; LVEF%, left ventricular ejection fraction; RVEF%, right ventricular ejection fraction; LV, left ventricle; LA, left atrium; T2-W STIR, T2-weighted short-tau inversion recovery; FPP, first-pass perfusion; T1-W, T1-weighted; ICA, invasive coronary angiography; LGE, late gadolinium enhancement; PSIR, phase-sensitive inversion recovery; TI, time to inversion; LAD, left anterior descending artery; H.E., hematoxylin and eosin.

Figure 3

CMR findings in APS. A figure demonstrates the array of findings from a comprehensive CMR study at a 1.5 Tesla scanner of APS. (a) SSFP sequence still cine images in short-axis view at the mid-ventricular level in end-diastole (a.1) and end-systole (a.2) show normal global and regional right and left ventricular functions, LVEF 63% and RVEF 56%. (b) T2-W STIR sequence in short-axis view at a mid-ventricular level shows mildly increased signal intensity in the anterior and anteroseptal segments (arrow) with a myocardial/skeletal muscle ratio of 3.6 suggestive of myocardial edema. (c) Stress CMR with FPP T1-W sequence with adenosine infusion at 140 mcg/kg/min over 6 mins showing a subendocardial circumferential perfusion defect (arrowheads) consistent with subendocardial ischemia due to endothelial dysfunction and probably to a microvascular disease (no obstructive coronary artery disease demonstrated in ICA). (d) LGE PSIR sequence. (d.1–3) short-axis views at basal (d.1), mid (d.2), and apical (d.3) levels, and long-axis views in 4-chambers (d.4) and 3-chambers (d.5) projections. The arrows in these images demonstrate areas of focal fibrosis as mid-wall LGE in the anteroseptal segment in (d.1,d.2,d.4); and in the subepicardium of the inferior segment from the base to the apex. (d.5) Shows aortic root and ascending aorta dilatation confirmed by the CE-MRA in (g) and the coronal view in SSFP still cine image (f), where it also demonstrates the presence of aortic regurgitation (arrow). (e) Zoomed still cine images in SSFP sequence of the mitral valve (e.1) and a fused asymmetric bicuspid aortic valve (e.3) Showing in a 4-chambers view a small isointense nodule in the ventricular side of the mitral valve, suggestive of Libman-Sacks endocarditis (arrow) and in the LVOT [arrow in (e.2)] (confirmed by echo), and mild thickening of the fused coronary bicuspid cusp [arrow in (e.3)]. Additionally, images (h.1–3) Show a thrombus within the portal vein and its main branches; in (h.1), a venous phase of the CE-MRA shows a contrast defect within the portal vein (arrow) consistent with a thrombus. T1-W axial view of the liver (h.2) shows a hyperintense structure within the portal system (arrow), and a T2-W STIR view of the liver (h.3) shows hypointense masses within the main portal branches (arrow) consistent with thrombus. CMR, cardiovascular magnetic resonance; SSFP, steady-state free precession; LVEF%, left ventricular ejection fraction; RVEF%, right ventricular ejection fraction; T2-W STIR, T2-weighted short-tau inversion recovery; FPP, first-pass perfusion; T1-W, T1-weighted; ICA, invasive coronary angiography; LGE, late gadolinium enhancement; PSIR, phase-sensitive inversion recovery; CE-MRA, contrast enhancement magnetic resonance angiography; LVOT, left ventricular outflow tract.

Figure 4

CMR findings in AR. A panel figure demonstrates varying findings from a comprehensive CMR study at a 3.0 Tesla scanner of RA with PH and arrhythmias. (a) SSFP sequence still cine images in short-axis view at the mid-ventricular level in end-diastole (a.1) and in end-systole (a.2) show normal global and regional left ventricular functions, mass, and wall thickness, LVEF 64% and moderately reduced systolic global RV function with global hypokinesia and mild hypertrophy (RV mass index 95 g/m²), RVEF 44%. (b.1) T2-W STIR sequence in short-axis view at a mid-ventricular level showing mildly increased signal intensity in the anterior, anteroseptal, and inferoseptal segments (arrow) with a myocardial/skeletal muscle ratio of 2.4 suggesting mild myocardial edema. (b.2) T1 mapping with a native T1 of 1,212 ms (normal), (b.3) T2 mapping with a T2 time of 42 msec (upper limit of normal) and (b.4) the ECV map corresponding to an elevated 52%. (c) LGE PSIR sequence. (c.1–3) Short-axis views at basal (c.1), mid (c.2), and apical (c.3) levels, and long-axis views in four-chambers (c.4) and three-chambers (c.5) projections. The arrows in these images show areas of focal fibrosis as midventricular LGE in the anteroseptal segment in (c.1,2) and the subepicardium of the anterior segment in (c.1) and subepicardial in the inferior segment in (c.2). (c.4) Shows LGE on the upper RA wall (arrow) and both-sided pleura (asterisks). (c.5) Shows mid-wall LGE on the anteroseptal segment. Pericardial LGE is shown in (c.1–3,5) (arrowheads), consistent with pericardial inflammation in the absence of pericardial effusion. (d) Zoomed still cine image in SSFP sequence of the aortic valve showing cusps thickening (arrow) with a mildly reduced valvular area (1.57 cm²). (e.1–3) SSFP sequence still cine images in long-axis 4-chambers view (e.1) showing RV enlargement (asterisks), (e.2) true axial view at great vessels level showing a mildly enlarged PA (asterisks) confirmed in the corresponding coronal view (e.3). (f) Zoom LGE PSIR image of the descending aorta showing wall artery enhancement (arrows). (g) SSFP sequence still cine images in the true axial view show an isointense tissue between the aortic root and the LA, probably of a granulomatous origin (arrow). CMR, cardiovascular magnetic resonance; RA, rheumatoid arthritis; SSFP, steady-state free precession; LVEF%, left ventricular ejection fraction; RVEF%, right ventricular ejection fraction; T2-W STIR, T2-weighted short-tau inversion recovery; ECV, extracellular volume; T1-W, T1-weighted; LGE, late gadolinium enhancement; PSIR, phase-sensitive inversion recovery; PA, pulmonary artery; LA, left atrium.

Figure 5

CMR findings in SSc. A panel figure demonstrates varying findings by a comprehensive CMR study at 1.5 Tesla scanner of SS. (a) SSFP sequence still cine images in short-axis view at the mid-ventricular level in end-diastole (a.1) and end-systole (a.2) shows normal global and regional functions of both ventricles, LVEF 57% and RVEF 56%. (b.1) T2-W STIR sequence in short-axis view at the mid-ventricular level of normal myocardium and myocardial/skeletal muscle ratio. (b.2) T1 mapping with a native T1 of 998 ms (mildly increase) and a calculated ECV of 32% (mildly increase). (c.1–5) LGE PSIR sequence. (c.1–3) Short-axis views at basal (c.1), mid (c.2), and apical (c.3) levels, and long-axis views in 4-chambers (c.4) and 3-chambers (c.5). The arrowheads in these images show areas of focal fibrosis as mid-wall LGE of the anteroseptal segment in (c.1) and the subepicardium of the inferior segment in (c.1–3) in the basal and mid anterolateral segments in (c.4) and subendocardial in the LV apex in (c.5). In addition, the same set of images shows LGE of the pericardium without effusion (arrow), suggestive of pericardial inflammation. CMR, cardiovascular magnetic resonance; SS, systemic sclerosis; SSFP, steady-state free precession; LVEF%, left ventricular ejection fraction; RVEF%, right ventricular ejection fraction; T2-W STIR, T2-weighted short-tau inversion recovery; ECV, extracellular volume; LGE, late gadolinium enhancement; PSIR, phase-sensitive inversion recovery.

Figure 6

CMR findings in DS. A panel figure demonstrates varying findings from a comprehensive CMR study at a 1.5 Tesla scanner of DS. (a) SSFP sequence still cine images in short-axis view at the mid-ventricular level in end-diastole (a.1) and end-systole (a.2) show normal global and regional functions of the left ventricle, LVEF 63% and mildly reduce systolic global RV function and mild global hypokinesia RVEF 45%. (a.3) In a coronal view showing the mild pericardial effusion surrounding the heart (asterisks). (b) T2-W STIR sequence in short-axis view at a mid-ventricular level showing increased signal intensity in the septal segments (arrow) with a myocardial/skeletal muscle ratio of 2.3, suggesting mild myocardial edema. (c.1–5) LGE PSIR sequence. (c.1–3) Short axis views at basal (c.1), mid (c.2), and apical (c.3) levels, and long-axis views in four-chambers (c.4) and three-chambers (c.5). The arrows in these images show areas of focal fibrosis as midventricular LGE of the anteroseptal and inferior segments in (c.1) and in the subepicardium of the inferior segment in (c.2,3). (c.1) Shows mild pericardial effusion (asterisks) and trivial pericardial enhancement (arrow), suggesting minimal pericardial inflammation. CMR, cardiovascular magnetic resonance; DS, DRESS syndrome; SSFP, steady-state free precession; LVEF%, left ventricular ejection fraction; RVEF%, right ventricular ejection fraction; T2-W STIR, T2-weighted short-tau inversion recovery; LGE, late gadolinium enhancement; PSIR, phase-sensitive inversion recovery.