Abstract
The present case of a patient with acute myocarditis with preserved left ventricular (LV) ejection fraction at the acute stage illustrates the obvious impairment of circumferential and rotational deformation, which can be documented by speckle tracking echocardiography. Thus, qualitative patterns of LV twist, radial strain, and circumferential layer strain, might be a new approach to detect acute myocarditis. The early diagnosis of acute myocarditis by echocardiography is important because of the considerable risk of cardiovascular morbidity as documented by the occurrence of an acute myocardial infarction presumably induced by inflammatory process in this case.
<Learning objective: The compound of myocardial deformations caused by left ventricular subendomyocardial and subepimyocardial fibers may be a crucial diagnostic target in cardiac diseases. The predominant involvement of viral myocarditis of the outer myocardial layers might induce impairment of circumferential and rotational deformation, which can potentially serve as a new diagnostic key by echocardiography. In contrast, left ventricular ejection fraction and longitudinal deformation are often observed within normal ranges in patients with acute myocarditis. Acute myocardial infarction as a major cardiac event in acute stage of myocarditis causes completely different deformation patterns, mainly by the predominant involvement of the inner myocardial layers inducing severe pathologies of territorial longitudinal deformation. Patients with suspected acute myocarditis and abnormal findings of circumferential and rotational deformation should undergo additional diagnostic procedures as cardiac magnetic resonance and myocardial biopsy to confirm the diagnosis.>
Keywords: Myocarditis, Acute myocardial infarction layered-specific strain, Rotation rate, Echocardiography
Introduction
The echocardiographic detection of acute myocarditis (AM) and its differentiation from other cardiomyopathies remains challenging [1], [2], [3]. Altered left ventricular (LV) myocardial velocities, impaired longitudinal and circumferential strain as well as twist and untwisting were previously described in AM patients with reduced, preserved, as well as normal LV ejection fraction [4], [5], [6], [7], [8], [9], [10]. Layered-specific strain makes it possible to account for etiopathology of myocardial lesions by studying regional myocardial function [11], [12], [13], [14], [15]. However, the layer strain-analysis method is limited by several methodological factors [16]. Differences in deformation parameters between patients with and without AM are discussed to be suitable for accurate diagnostics [5], [6], [7], [8], [9], [10]. Deformation analysis presumably provides options to detect AM in a qualitative manner due to the improvement in echocardiographic image quality and postprocessing techniques. The normal curves of deformation and alterations during pathological conditions of radial and circumferential strain as well as of rotation and rotations rate are illustrated in a schematic drawing (Fig. 1). The course of circumferential strain curves corresponds to those of longitudinal strain. Normal radial and circumferential strain and rotation curves of a representative echocardiographic documentation are presented for better understanding in a normal case before illustrating pathological conditions (Fig. 2).
Fig. 1.
Schematic drawing of global radial strain (GRS), regional circumferential strain (RCS), rotation, and rotation rate during normal conditions (above). The normal ranges are indicated by key values at the ordinates. Global deformation curves are black, regional deformation curves are colored. Pathological conditions are illustrated by qualitative changes of the curves in the second row of the scheme: post-systolic shortening of GRS (maximum after end-systole during diastole, e.g. for apical GRS in blue); no radial deformation of GRS, (no increase during systole, e.g. for basal GRS in magenta); akinesis of RCS (no deformation during systole in the basal posterior and lateral segments colored in magenta and green); biphasic rotation during systole (net-effect of basal and apical rotation = twist) and diastolic undulation of the rotation rate during early diastole (net-effect of basal and apical rotation = untwisting). IVRT, isovolumic relaxation time.
Fig. 2.
Physiological normal deformation of the apex and the base: apical 2D-parasternal short-axis view during diastole (a) and systole (b) documenting counter-clockwise rotation by 2D speckle tracking echocardiography; basal 2D-parasternal short-axis view during diastole (c) and systole (d) documenting clockwise rotation; line graphs of regional radial strain of the apical (e) and the basal segment (f). Radial strain in the basal segments showed minimal post-systolic shortening (dotted arrow); 2D-parasternal short-axis views presenting segmental values of apical (g,h) and basal (i,j) subendomyocardial (g,i), and subepimyocardial (h,j) circumferential strain and the corresponding segmental strain graphs and color-M-Modes; line graphs of apical rotation (blue) and basal rotation (magenta) as well as twist (white) (k) and the corresponding line graphs of rotation rate (l).
Currently cardiac magnetic resonance (CMR) is considered as the primary non-invasive diagnostic tool of choice for AM in routine practice [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], [13], [14], [15], [16], [17]. In patients with high contagiousness and high pathogenicity, echocardiography becomes important due to its overall availability by portable devices and the fast and easy image acquisition procedures.
We present a case that demonstrates a presumably easy qualitative approach of using two-dimensional speckle tracking echocardiography to detect AM in patients with preserved LV function. The acute course of the AM showed a serious complication, which 1) demonstrates the need for close monitoring of AM patients and 2) clearly highlights the easy differentiation between pathologies of rotational deformation due to the involvement of the outer myocardial layers by AM and of longitudinal deformation due to the predominant involvement of territorial inner layers by ischemia in the same patient.
Case report
A 38-year-old woman presented with chest pain and dyspnoea in the emergency unit. She had symptoms of lower respiratory tract infection. Electrocardiography was normal. Myocardial enzymes were elevated (creatine kinase-MB 2.98 mmol/l, troponin-T 142 mmol/l). Coronary angiogram was normal at the day of hospital admission. CMR imaging confirmed the diagnosis of AM, affecting the LV free wall, fulfilling all Lake Louise criteria [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], [13], [14], [15], [16], [17]. T1- and T2-mapping were not performed at this time in the clinical routine. Echocardiography showed normal LV-function. Applying 2D speckle-tracking echocardiography, normal global longitudinal strain (-19 %) was observed. However, regional circumferential strain was affected in the LV-free wall resulting in obviously pathological regional circumferential layer strain, pathological basal radial strain, and consecutive chaotic shapes of the rotation, and rotation rate (Fig. 3). The pathological findings of CMR - predominantly edema and hyperemia - and deformation imaging were mainly located in the lateral LV segments. A transmural involvement of the AM by edema formation can be assumed in the basal posterolateral segments (Fig. 3 i,j,m,n), a non-transmural subepimyocardial involvement by bland subepicardial late enhancement in the apical posterolateral segments (Fig. 3 h,o).
Fig. 3.
Pathological rotation of the base in acute myocarditis: apical 2D-parasternal short-axis view during diastole (a) and systole (b) documenting physiological counter-clockwise rotation by 2D speckle tracking echocardiography; basal 2D-parasternal short-axis view during diastole (c) and systole (d) documenting lack of clockwise rotation; line graphs of regional radial deformation of the apical segment with minimal post-systolic shortening (dotted arrow - e) and pathological radial deformation of the basal segment (white arrow - f). 2D-parasternal short-axis views presenting segmental sub-endomyocardial and subepimyocardial circumferential strain values (g-j) including segmental strain graphs and color-M-Modes; pathological deformation is documented in the apical inferior and posterolateral as well as in the basal posterolateral segments (colored arrows); line graphs of apical rotation (blue) and basal rotation (magenta) as well as twist (white) (k) and the corresponding line graphs of rotation rate (l) documenting pathophysiological twist (biphasic curve during systole - white arrows) and untwisting (undulation during diastole - white arrows). Cardiac magnetic resonance imaging documents formation of edema in T2STIR-sequences predominantly in the inferior and lateral regions (white arrows in basal sectional plane - m and apical sectional plane - n) and mid and subepimyocardial delayed enhancement in PSIR sequences predominantly in the lateral segments (white arrows - o).
Fourteen days after diagnosis of AM re-admission to hospital occurred because of acute anterior myocardial infarction due to a thrombus formation in the proximal left anterior descending artery. Despite acute interventional treatment residual scar formation could not be prevented as documented by the postinterventional echocardiography at hospital discharge. The acute complication of myocardial infarction within the healing period of AM documents the difficulties to interpret the deformation findings in the follow-up. The observed abnormalities were mainly due to ischemia - especially the pathological pattern of longitudinal deformation (Fig. 4 and Fig. 5) and do not allow any interpretation about time-dependent changes due to inflammation.
Fig. 4.
Coronary angiography of the left coronary artery at hospital admission with a moderate narrowing of the proximal left anterior descending artery (LAD) (a); Follow-up angiography 14 days later after acute ST-elevation myocardial infarction (STEMI) documenting acute thrombus formation (white arrow) in the proximal LAD (b). Line graphs of the pathological regional radial deformation of the apical segments (white arrow: no deformation - c) and basal segments (white arrow: wall thinning during systole - d) in the follow-up at hospital discharge. 2D-parasternal short-axis views presenting segmental sub-endomyocardial and sub-epimyocardial circumferential strain values of the apical segments (g) and of the basal segments (h) including segmental strain graphs and color-M Modes at 6-month follow-up, pathological deformation is documented in the apical inferior segment (colored arrows); illustration of the corresponding line graphs of apical rotation (blue) and basal rotation (magenta) as well as twist (white) (biphasic pattern - white arrow - i) and the corresponding line graphs of rotation rate (undulation during diastole - white arrow - j) at 6-month follow-up due to the acute STEMI and the ischemic myocardial damage significant alterations between acute stage of myocarditis and follow-up deformation could be documented.
Fig. 5.
The deformation curves and patterns of longitudinal left ventricular strain during acute myocarditis pre (a,c,e,g,i) and post myocardial infarction(b,d,f,h,j): regional longitudinal strain curves of the six segments in the long-axis view (a,b), in the 2-chamber view (c,d), and in the 4-chamber view (e,f) as well as pattern of peak systolic strain (g,h) and post systolic shortening index (i,j) are presented to document almost normal longitudinal deformation prior (dotted arrows) to acute anterior infarction and severe dyskinesis after acute myocardial infarction (colored and white arrows).
Discussion
We report a case of AM, which possibly can serve as a hypothesis to use deformation imaging - especially layer strain - for further studies. CMR often documents that the subepimyocardial fibers are primarily involved in AM. The results of a necropsy study of AM patients after sudden cardiac death also confirm these findings [18]. The outer subepimyocardial outer layers are primarily composed of the circumferential fibers. These circumferential fibers are mainly responsible for the rotational motion of the heart with the base of the heart in the clockwise direction and apex of the heart in counter-clockwise direction resulting in the torsion. If the circumferential fibers are involved in the disease process, the chaotic pattern of rotation and rotation rate curve in these patients can be explained. The reduced circumferential strain predominantly in the subepimyocardial layers as well as the concomitant pathological radial strain patterns might demonstrate that the fibers of the outer layers might be predominantly involved. Thus, deformation imaging of LV rotation is able to detect alterations of LV function due to AM. Global longitudinal function of the myocardium is reduced when there is extensive transmural or subendomyocardial myocardial damage [8]. In minor involvement of the LV wall as in the present case at the acute stage of AM, transmural damage is unlikely. The early diagnosis of AM is known to be important because of the considerable risk of cardiovascular morbidity and mortality due to AM as documented in this case by the occurrence of acute myocardial infarction in a young female. Because detection of AM by echocardiography in patients with normal LV ejection fraction is challenging - especially only in the presence of isolated unspecific clinical symptoms such as sub-febrile temperature, cough, dyspnea, and palpitations, no further diagnostic tests might be initiated to confirm the diagnosis of myocarditis. Thus, modern echocardiographic features may considerably contribute to better patient management in this diagnostic scenario - especially for the early detection of complications by ischemia-typical deformation patterns of reduced longitudinal strain. A simple qualitative approach comparing pathological strain patterns in comparison to healthy individuals can be particularly useful in these cases. If abnormal deformation patterns can be documented, further tests can be initiated to confirm the diagnosis of AM.
In addition, the echocardiographic diagnostic of AM can become more important in diseases with high contagiousness and high pathogenicity, because the disinfection of large medical devices such as CMR is time-consuming. We acknowledge that there is a considerable variability in assessment of absolute values of regional strain parameters which makes it difficult to implement this method into routine workflow [19]. Except for global values of longitudinal strain deformation imaging is not yet implemented in the clinical scenario [20]. Therefore, we are proposing a qualitative approach analyzing pattern of circumferential strain and rotation just by eye balling, which might be easier to interpret than absolute values of regional deformation. A good example of pattern assessment of regional function is apical sparing of longitudinal strain which has found wide acceptance in the imaging community [21]. In cases with other known cardiac and non-cardiac systemic comorbidities, one should be careful in interpreting the results as many comorbidities are associated with LV dysfunction with impaired strain. This is also documented by the alterations of deformation patterns caused by the myocardial infarction in the present case.
Limitations
The major challenge of parasternal 2D speckle tracking is the acquisition of robust strain and rotation data - especially in the basal LV segments. Radial and circumferential strain analysis is influenced by several methodological problems. Firstly, image quality has to be adequate. Artifacts due to pulmonary interferences and rib shadowing - especially in the lateral LV regions - and lack of transducer contact - especially in thin patients - have to be excluded. Secondly, the apical short-axis planes have to be correctly acquired within the apical third of the left ventricle, the basal short-axis views without depicting parts of the left atrial wall and/or the mitral annulus as well as the coronary sinus during systole and parts of the mitral valve during diastole. Thirdly, the tracking areas - especially for radial strain - have to be positioned exclusively into the myocardium. The integration of paracardial structures as well as parts of the mitral valve into the tracking area can produce false negative radial strain curves. The limitation of circumferential and radial strain assessment in the absence of an adequate acoustic window can possibly be solved by 3D echocardiography. Finally, this observation of pathological circumferential strain and rotation should be investigated in a larger series of patients for more compelling evidence.
Summary and conclusion
In conclusion, this case points out novel options to easily detect AM at the early stages by an easy qualitative approach to detect the impairment of circumferential subepimyocardial strain and LV rotation in the presence of preserved LV ejection fraction by speckle tracking. In addition, complications such as acute ischemic events can be detected early by characteristic deformation patterns, which might be helpful in monitoring these patients. Thus, deformation imaging should be integrated into the diagnostic algorithm in AM (Fig. 6). This case report sets the stage for diagnostic application of these parameters in a larger cohort of patients as well as to determine the prognostic importance of deformation imaging parameters in AM patients.
Fig. 6.
Diagnostic algorithm for the utility of imaging modalities in suspected acute myocarditis. ECG, electrocardiography; LV, left ventricular; MR, magnetic resonance.
Disclosure
None.
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