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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References

Background:

Acute myocarditis (AM) may occasionally have an infarct-like presentation. The aim of the present study was to investigate the relation between electrocardiographic (ECG) findings in this group of patients and myocardial damage assessed by cardiac magnetic resonance imaging (MRI) with the late gadolinium enhancement (LGE) technique.

Hypothesis:

Myocardial damage may be associated with ECG changes in infarct-like AM.

Methods:

Forty-one consecutive patients (36 males; mean age, 36 ± 12 years) with diagnosis of AM according to cardiac MRI Lake Louise criteria and infarct-like presentation were included. The relation between site of ST-segment elevation (STE), sum of STE (sumSTE), time to normalization of STE, and development of negative T wave with the extent of LGE (expressed as % of left ventricular mass [%LV LGE]), was evaluated.

Results:

Most (80%) patients presented with inferolateral STE; mean sumSTE was 5 ± 3 mm. Normalization of STE occurred within 24 hours in 20 (49%) patients. Development of negative T wave occurred in 28 (68%) patients. Cardiac MRI showed LGE in all patients; mean %LV LGE was 9.6 ± 7.2%. Topographic agreement between site of STE and LGE was 68%. At multivariate analysis, sumSTE (β = 0.42, P < 0.001), normalization of STE >24 hours (β = 0.39, P < 0.001), and development of negative T wave (β = 0.49, P < 0.001) were independently related to %LV LGE.

Conclusions:

Analysis of the site of STE underestimates the extent of myocardial injury among patients with infarct-like myocarditis. However, some ECG features (ie, sumSTE, normalization of STE >24 hours, and development of negative T wave) may help to identify patients with larger areas of myocardial damage.

The authors have no funding, financial relationships, or conflicts of interest to disclose.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References

The clinical presentation of acute myocarditis (AM) is highly variable, ranging from subclinical disease to fulminant heart failure, cardiogenic shock, and death.1 In a subset of patients, AM may have an infarct-like presentation, with chest pain, ST-segment elevation (STE) on electrocardiogram (ECG), and elevated troponin (Tn) levels.2–5 Cardiac magnetic resonance imaging (cMRI) has recently emerged as a valuable tool for the diagnostic workup of these patients, due to its ability to in vivo identify myocardial inflammatory involvement and myocardial injury.6 By accurately diagnosing the underlying cause of clinical presentation, cMRI may indeed facilitate appropriate treatment and follow-up.7,8

In the setting of STE myocardial infarction (STEMI), previous cMRI studies have demonstrated a relation between some ECG features (including the sum of total STE [sumSTE], ST-segment resolution, residual STE, and the number of Q waves) with infarct size and extent of myocardium salvaged by reperfusion therapies.9–14 Conversely, scarce data are available regarding the clinical meaning of ECG changes in the setting of infarct-like myocarditis; accordingly, the purpose of this study was to explore the relation between the ECG findings in this group of patients and the extent of myocardial damage, as assessed by cMRI.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References

Patient Population

A total of 41 consecutive previously healthy patients acutely admitted to our institution because of acute-onset chest pain and STE on ECG, and with subsequent cMRI findings consistent with AM according to the Lake Louise criteria, were included in the study.6 All patients had evidence of elevated Tn levels during hospitalization. Coronary artery lesions were ruled out by emergent coronary angiography in 24 (59%) patients. The remaining 17 (41%) patients did not undergo coronary angiography because they were considered by the treating cardiologist as having a very low pretest probability of coronary artery disease (due to young age, absence of wall-motion abnormalities on transthoracic echocardiography, or presence of obvious gastrointestinal or respiratory infection).

Twelve-Lead Electrocardiogram Acquisition Protocol and Analysis

A standard 12-lead ECG was recorded in each patient upon admission, at 12 hours, and every 24 hours thereafter until hospital discharge, at a paper speed of 25 mm/s and an amplification of 10 mm/mV. Electrocardiographic data were evaluated by an observer who was unaware of clinical data and cMRI results. The isoelectric line was defined as the level of the preceding TP segment. The following ECG parameters were determined: (1) site of STE (A. anterolateral for STE in leads V1 through V4, I, aVL ± V5, and V6; B. inferolateral for STE in leads II, III, aVF ± V5, and V6; C. diffuse)15; (2) sum of STE (sumSTE), which was measured 20 ms after the J point in every lead, as previously described15; (3) time to normalization of STE, defined as no residual STE ≥0.1 mV in any of the 12 leads15; (4) development of pathologic Q wave, defined as an initial negative deflection of the QRS complex >30 ms in duration and >0.1 mV, if it was preceded by STE in the same lead on the ECG at diagnosis, and with exclusion of aVR16; and (5) development of negative T wave. T waves were considered negative when the negative amplitude was ≥0.1 mV.17

Cardiac Magnetic Resonance Imaging Acquisition Protocol

Cardiac MRI studies were performed using a 1.5-T scanner (MAGNETOM Avanto; Siemens, Erlangen, Germany) at 8.5 ± 5.2 days after admission; 34 (83%) patients underwent a cMRI study within 14 days. All studies were performed using dedicated cardiac software, a phased-array surface receiver coil, and vectorcardiogram triggering. Three standard cine long-axis slices and a stack of contiguous cine short-axis slices (slice thickness, 8 mm) from the atrioventricular ring to the apex were acquired using a steady-state free-precession pulse sequence. Breath-hold T2-weighted short-TI inversion-recovery fast spin-echo pulse sequence in the same long-axis and short-axis plane of cine images was utilized to assess the presence of myocardial edema. The late gadolinium enhancement (LGE) images were acquired in the same views as used for cine images 10 minutes after intravenous injection of 0.1 mmol/kg gadolinium-based contrast agent (Omniscan; GE Healthcare, Princeton, NJ) using a phase-sensitive inversion-recovery gradient-echo sequence, individually adjusting TI to optimize nulling of apparently normal myocardium.

Cardiac Magnetic Resonance Imaging Data Analysis

All cMRI studies were analyzed offline using dedicated software (Argus software, Siemens; and Segment 1.9, Medviso AB, Lund, Sweden) by an experienced observer blinded to clinical and ECG data. Biventricular volumes and function, and left ventricular (LV) mass were measured using standard volumetric techniques from the cine short-axis images.18 Volume and mass measurements were indexed to body surface area. Global myocardial edema was assessed by normalized signal intensity quantification in T2-weighted images, with manually traced endocardial and epicardial contours of the entire visible myocardium and skeletal muscle in the same slice. Myocardial signal intensity was divided by the signal intensity (SI) of skeletal muscle; a ratio ≥2 was considered indicative of global myocardial edema.6 Focal areas of high SI in T2 images (those with SI ≥2 SD above the mean SI of the normal myocardium) were considered to demarcate regional myocardial edema6; only areas of ≥10 adjacent pixels with high SI were considered relevant.6 Images were visually assessed for the presence and distribution of LGE areas (indicative of myocardial necrosis) for each LV myocardial segment using the 17-segment cardiac model.19 In addition, the spatial extent of these lesions was automatically quantified from the short-axis LGE images according to a previously described method and expressed as percentage of the LV mass (%LV LGE).20 Briefly, the endocardial and epicardial borders were traced manually with exclusion of the papillary muscles. The LGE myocardium was then defined using a computer algorithm that compensates for partial volume effects by weighting pixels according to their SI; manual adjustments were made when the computer algorithm was obviously wrong.20

Cardiac MRI findings were considered consistent with AM when both regional or global myocardial edema and ≥1 focal lesion of myocardial necrosis with nonischemic regional distribution were present.6

Statistical Analysis

Continues variables are expressed as mean and SD. Categorical data are presented as absolute numbers and percentages. Differences in continuous variables were assessed using the Student t test or the Mann-Whitney U test, when appropriate. The χ2 square test or Fisher exact test, when appropriate, were computed to assess differences in categorical variables.

Topographic agreement between site of LGE and site of STE was calculated as follows: (N° of LV segments with LGE predicted by the site of STE / N° of LV segments with LGE) × 100. Anterolateral STE was considered as a predictor of LGE in the anterior interventricular septum, anterior wall, anterolateral wall, and apex; inferolateral STE elevation was considered as a predictor of LGE in the inferolateral wall, inferior wall, and inferior interventricular septum.

Linear regression analyses were performed to evaluate the relation between peak C-reactive protein (CRP) and peak cardiac TnI with %LV LGE.

Univariate and multivariate linear regression analysis (with an automatic stepwise selection procedure with backward elimination) was performed to evaluate the relationship between %LV LGE and the following variables: clinical risk factors, flu-like symptoms, left ventricular ejection fraction (LVEF), and ECG parameters. Only variables with P value <0.1 at univariate analysis were entered as covariates in the multivariate model. A 2-tailed P value <0.05 was considered statistically significant. Statistical analysis was performed using SPSS software, version 20 (SPSS Inc., Chicago, IL).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References

Clinical, Electrocardiographic, and Cardiac Magnetic Resonance Imaging Data

Clinical and ECG characteristics of the study population are summarized in Table 1. Mean age was 36 ± 12 years; 36 (88%) patients were male. Prevalence of coronary risk factors was very low. Peak cardiac TnI value was 11 ± 10 ng/mL (normal value, ≤0.04 ng/mL). Most (80%) patients presented with inferolateral STE; mean sumSTE was 5 ± 3 mm. ST-segment elevation regressed during hospitalization in all patients; normalization of STE occurred within 24 hours in 20 (49%) patients. Development of pathologic Q wave was not observed in any patients, whereas development of negative T wave occurred in 28 (68%) patients during hospitalization.

Table 1. Clinical and ECG Characteristics of the Study Population
CharacteristicN = 41
  1. Abbreviations: CAD, coronary artery disease; CRP, C-reactive protein; DM, diabetes mellitus; ECG, electrocardiographic; SD, standard deviation; STE, ST-segment elevation; TnI, troponin I.

  2. Data are expressed as mean ± SD and n (%).

Age (y) 36 ± 12
Male sex36 (88)
Family history of CAD7 (17)
Hypertension5 (12)
Dyslipidemia2 (5)
DM2 (5)
Active or previous smoking10 (24)
Flu-like symptoms (recent or current)34 (83)
Peak cardiac TnI (ng/mL)11 ± 10
Peak CRP (mg/L)75 ± 69
Site of STE 
 Anterolateral5 (12)
 Inferolateral33 (81)
 Diffuse3 (7)
SumSTE (mm)5 ± 3
Normalization of STE >24 h20 (49)
Development of pathologic Q wave0 (0)
Development of negative T wave28 (68)

Cardiac MRI characteristics are summarized in Table 2. Mean LV end-diastolic volume index (LVEDVI) and mean LVEF were 73 ± 11 mL/m2 and 65 ± 7%, respectively. The mean number of LV segments with myocardial edema per patient was 6.3 ± 3.5; the mean global T2 ratio was 1.98 ± 0.30. The mean number of LV segments with LGE per patient was 5.6 ± 3.4, and the mean %LV LGE was 9.6 ± 7.2%. Overall, a total of 232 (33%) LV segments showed LGE. Late gadolinium enhancement had a patchy pattern, with midmyocardial or subepicardial distribution in 49 (21%) and 183 (79%) LV segments, respectively. As shown in Figure 1, LGE was most commonly located in the anterolateral wall (n = 81, 35%), inferior wall (n = 56, 24%), and inferolateral wall (n = 43, 19%); LGE was less frequently located in the anterior wall (n = 24, 10%), interventricular septum (n = 21, 9%), and apex (n = 7, 3%).

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Figure 1. Distribution of LV segments with LGE in the overall study population (A), and among patients with inferolateral, anterolateral, and diffuse STE (B, C, and D, respectively). As shown in (A), LGE was most commonly located in the anterolateral wall, inferior wall, and inferolateral wall. As shown in (B) and (C), LGE was not infrequently observed in LV segments other than predicted by site of STE; topographic agreement between the site of LGE and site of STE was 46% (B) among patients presenting with inferolateral STE and 59% (C) among patients with anterolateral STE. Among patients with diffuse STE (D), LGE was observed in both anterolateral and inferolateral LV segments. Overall topographic agreement between the site of LGE and site of STE was 68%. Abbreviations: LGE, late gadolinium enhancement; LV, left ventricular; STE, ST-segment elevation.

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Table 2. Cardiac MRI Characteristics of the Study Population
  1. Abbreviations: LGE, late gadolinium enhancement; LV, left ventricular; LVEDVI, left ventricular end-diastolic volume index; LVEF, left ventricular ejection fraction; LVESVI, left ventricular end-systolic volume index; LVMI, left ventricular mass index; MRI, magnetic resonance imaging; RVEDVI, right ventricular end-diastolic volume index; RVEF, right ventricular ejection fraction; RVESVI, right ventricular end-systolic volume index; SD, standard deviation; WMSI, wall motion score index.

  2. Data are expressed as mean ± SD and n (%).

LVEDVI (mL/m2)73 ± 11
LVESVI (mL/m2)26 ± 8
LVEF (%)65 ± 7
LVMI (g/m2)62 ± 10
Wall-motion abnormalities9 (22%)
WMSI1.05 ± 0.17
RVEDVI (mL/m2)70 ± 11
RVESVI (mL/m2)24 ± 7
RVEF (%)66 ± 7
LV segments with myocardial edema, n6 ± 3
T2 ratio1.98 ± 0.30
LV segments with LGE, n5.6 ± 3.4
LV LGE, %9.6 ± 7.2

Peak CRP was not significantly related to %LV LGE (β = 0.12, P = 0.45). Conversely, peak cardiac TnI was significantly related to %LV LGE (β = 0.83, P < 0.001).

Relation Between Electrocardiogram and Late Gadolinium Enhancement

Late gadolinium enhancement was not infrequently observed in LV segments other than predicted by site of STE (Figure 1); topographic agreement between the site of LGE and site of STE was 59% among patients presenting with anterolateral STE and 46% among patients with inferolateral STE. Late gadolinium enhancement was observed in both anterolateral and inferolateral LV segments among patients with diffuse STE. Overall topographic agreement between site of LGE and site of STE was 68% (Figure 1). Figure 2 shows LGE images of a patient with diffuse STE and cMRI findings consistent with AM.

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Figure 2. Contrast-enhanced inversion-recovery gradient-echo images of a patient with infarct-like myocarditis presenting with diffuse STE. (A) 4-chamber view, (B) 2-chamber view, (C) 3-chamber view, and (D) mid–short-axis view. Patchy LGE with midmyocardial and subepicardial distribution involving the inferior, anterior, anterolateral, and inferolateral wall was observed. Abbreviations: LGE, late gadolinium enhancement; STE, ST-segment elevation.

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A significant relation was found between sumSTE and %LV LGE (β = 0.69, P < 0.001). Patients having anterolateral or diffuse STE had higher %LV LGE compared with the patients with inferolateral ST-segment elevation (17 ± 8% vs 8 ± 6%, P = 0.012). In addition, patients showing normalization of STE >24 hours from clinical presentation had higher %LV LGE compared with the remaining patients (14 ± 7% vs 5 ± 4%, P < 0.001). Similarly, patients showing ECG evolution to T-wave inversion had higher %LV LGE compared with patients with normalized ECG (12 ± 7% vs 4 ± 3%, P < 0.001).

Table 3 shows the results of the univariate and multivariate linear regression analysis performed to determine the independent correlates of %LV LGE. At multivariate analysis, sumSTE (β = 0.42, P < 0.001), normalization of STE >24h (β = 0.39, P < 0.001), and development of negative T wave (β = 0.49, P < 0.001) were independently related to %LV LGE.

Table 3. Univariate and Multivariate Regression Analyses to Determine the Independent Correlates of LGE Expressed as Percentage of the LV Mass
 UnivariateMultivariate
βP ValueβPValue
  1. Abbreviations: CAD, coronary artery disease; DM, diabetes mellitus; LGE, late gadolinium enhancement; LV, left ventricular; LVEF, left ventricular ejection fraction; STE, ST-segment elevation.

  2. R2 square of the model selected at multivariate analysis was 0.73.

Age0.0360.82  
Male sex0.340.032
Family history of CAD0.160.31  
Hypertension0.0540.74  
Dyslipidemia−0.210.18  
DM0.140.36  
Active or previous smoking0.220.17  
Flu-like symptoms (recent or current)0.200.21  
LVEF−0.0180.91  
Anterolateral or diffuse STE0.53<0.001
SumSTE0.69<0.0010.42<0.001
Normalization of STE >24 hours0.63<0.0010.39<0.001
Development of negative T wave0.53<0.0010.49<0.001

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References

The results of the present study can be summarized as follows. First, ECG underestimates the extent of myocardial injury among patients with infarct-like myocarditis; overall topographic agreement between the site of LGE and site of STE was only 68% in the present study. Second, some ECG parameters, including sumSTE, normalization of STE >24 hours, and development of negative T wave, are significantly and independently related to the extent of myocardial damage.

Electrocardiography in Infarct-Like Myocarditis and Relation to Myocardial Damage

Several studies have previously shown that a subset of AM patients may have an infarct-like presentation, with chest pain, elevated Tn levels, and ECG findings suggestive of STEMI.2–5 This pattern of clinical presentation has been related to parvovirus B19 infection of the endothelial cells of myocardial vessels, causing endothelial dysfunction and coronary vasospasm, migration of inflammatory cells into the myocardial interstitium, and subsequent myocyte damage.21,22

Cardiac MRI with the LGE technique has emerged as an important tool for the diagnostic workup of these patients, noninvasively distinguishing AM from ischemic injury and other nonischemic conditions with infarct-like presentation, such as Takotsubo cardiomyopathy.7 Following a myocardial infarction, LGE with subendocardial or transmural pattern is typical.7 Among patients with AM, LGE is typically epicardial, in the mid-wall, or patchy.7 Among patients with Takotsubo cardiomyopathy, which is characterized by a typical pattern of LV dysfunction, significant LGE is conversely usually absent.23,24

Electrocardiographic repolarization changes in infarct-like myocarditis have been described5,25,26; STE, attributed to epicardial inflammatory injury, is followed by gradual ST-segment normalization and subsequent variable occurrence of T-wave inversion, attributed to epicardial damage. Finally, the ECG normalizes, with resolution of T-wave abnormalities; of note, development of Q wave is rarely observed. Recent cMRI studies have extensively investigated the relation between repolarization changes observed in STEMI and infarct size and extent of myocardium salvaged by reperfusion therapies.9–14 Conversely, little is known about the clinical meaning of repolarization changes in the setting of infarct-like myocarditis. Karjalainen and Heikkila evaluated the relation between the amount of myocardial damage, assessed as peak creatine kinase MB value, and ECG changes in 18 young men with infarct-like myocarditis. They observed that the peak creatine kinase MB value was significantly higher in patients with conspicuous STE and with subsequent T-wave inversion.27 More recently, Deluigi et al28 and Di Bella et al29 evaluated the relation between the site of repolarization abnormalities and location of myocardial injury assessed by cardiac MRI in patients with AM (including 20 and 46 patients with infarct-like myocarditis, respectively); both groups found a weak correlation between ECG leads showing repolarization abnormalities and location of LGE. The results of the present study, which used cMRI as a reference technique for the evaluation of myocardial damage, confirm and extend these previous observations. First, we observed that the site of STE is not a perfect predictor of the region of myocardial injury among both groups of patients presenting with anterolateral or inferolateral STE; topographic agreement between the site of LGE and the site of STE was only 59% and 46%, respectively. Second, the amount of STE (sumSTE), late normalization of STE (ie, >24 hours), and development of negative T wave were found to be significantly and independently related to the extent of LGE, suggesting that these ECG indexes could be used for a fast bedside estimation of the extent of myocardial damage in this group of patients. This finding is novel in the setting of infarct-like myocarditis and parallels recent cMRI observations in the setting of STEMI, which documented a relation between sumSTE and the extent of myocardial injury and between ST-segment resolution and improvement of myocardial damage owing to reperfusion.9–14 Interestingly, Naruse and colleagues recently observed a relation between time to ECG normalization and LGE among patients with Takotsubo cardiomyopathy as well.30 Third, none of the patients included in the present study developed pathologic Q waves. Moon et al have shown that the presence of Q wave in ischemic heart disease is mainly related to the extent of infarct size and, secondarily, to its transmural extent31; accordingly, the scattered nature and the absence of transmurality of myocardial damage in AM may explain the lack of development of Q waves in this group of patients.

Study Limitations

This study has some limitations that should be acknowledged. First, the study population was relatively small; however this reflects the low incidence of the disease.5 Second, endomyocardial biopsy, which is considered the gold standard for the diagnosis of myocarditis,32 was not performed; however, all included patients had cMRI findings consistent with AM, in agreement with current criteria.6 Moreover, according to current guidelines, endomyocardial biopsy is not indicated in patients with suspected AM presenting without heart failure symptoms and preserved LV systolic function.33

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References

Among patients with infarct-like myocarditis, analysis of the site of STE underestimates the extent of myocardial injury. However, some ECG features, such as sumSTE, normalization of STE >24 hours, and development of negative T wave, may help to identify patients with larger areas of myocardial damage.

References

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  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. References
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