Assessing myocardial hyperemia in acute myocarditis with 3T contrast-enhanced whole-heart magnetic resonance imaging: a feasibility study

Introduction

Patients with acute chest pain and elevated troponin levels may have acute myocarditis. Myocarditis has been reported to be associated with life-threatening arrhythmia, sudden cardiac death, and dilated cardiomyopathy (1,2) and is typically caused by viral infection (3). This disorder manifests through a spectrum of clinical features, such as angina-equivalent chest pain, paroxysmal palpitations, malignant arrhythmia, decompensated cardiac dysfunction, and even sudden cardiac death, often mimicking the phenotypic expression of common cardiovascular pathologies (4). Studies have identified several factors associated with a poorer outcome in myocarditis, such as clinical manifestations, the type of virus involved, consistency with Lake Louis Criteria (LLC) diagnosis, the value of extracellular volume (ECV), and the identification of late gadolinium enhancement (LGE) with a specific anteroseptal distribution pattern (5-9). Therefore, the early and accurate diagnosis of myocarditis is crucial for devising a tailored therapeutic strategy for reducing adverse clinical outcomes and improving prognosis. Although recognized as the gold-standard diagnostic tool for myocarditis, endomyocardial biopsy (EMB) is seldom applied in routine clinical practice due to its invasive nature and the potential for inadequate tissue sampling, which may compromise diagnostic accuracy (10).

Cardiac magnetic resonance (CMR) has emerged as an effective tool for the detection of myocarditis due to its unique ability of multiparametric tissue characterization. The LLC constitute the widely accepted diagnostic protocol for myocarditis, first established in 2009 (11) and subsequently updated in 2018 (12). CMR and its various modalities can diagnose different conditions; for instance, myocardial edema can be detected by T2-weighted spin echo, hyperemia by T1-weighted spin-echo, and necrosis by LGE (11). Early gadolinium enhancement (EGE) assessment is the most controversial and generally considered the least robust of the three LLC (11). A significant limitation of the EGE ratio (EGER) technique with the T1-fast spin-echo (T1-FSE) pulse sequence is the potential degradation of image quality, which may render the results nondiagnostic due to motion-induced artifacts. Moreover, myositis affecting skeletal muscle signal intensity can result in the potential misdiagnosis of a normal EGER. In 2014, Perfetti et al. (13) demonstrated the feasibility of using the contrast-enhanced steady-state free precession (ceSSFP) technique (administered shortly after gadolinium injection) to evaluate myocardial hyperemia in cases of acute myocarditis. However, this approach fails to detect myocardial hyperemia in 23% of patients. As reported by Zarka et al. (14), subepicardial hyperemia on perfusion MRI has diagnostic value for acute myocarditis. Palmisano et al. (15) proposed an early T1-mapping technique (acquired 2 min after contrast agent injection) for the detection of myocardial hyperemia and found the early T1 shortening had outstanding performance in diagnosing acute myocarditis. However, the mapping technique has several limitations; these include the dependence of normal mapping values on the specific CMR sequence, algorithm, or field strength used; the absence of standardized cutoff values for diagnosing myocarditis; and a spatial resolution that is inferior to that of LGE imaging (16-18).

A 3-Tesla (T) contrast-enhanced whole-heart magnetic resonance imaging (CE WH-MRI) protocol with a fast low-angle shot (FLASH) sequence was developed to enable the detection of coronary artery stenosis within a 10-min examination duration. Several pioneering studies have demonstrated the clinical diagnostic value of CE WH-MRI and reported encouraging results (19-21). The CE-FLASH, a three-dimensional (3D) T1-weighted gradient-echo sequence, employs centric k-space filling to ensure preferential acquisition of central k-space data during the critical early phase following contrast injection. This approach optimizes temporal resolution while maintaining robust image contrast. Therefore, we hypothesized that CE WH-MRI can enable the detection of myocardial hyperemia-associated imaging features in patients with acute myocarditis. Thus far, no study has been conducted to specifically examine the use of CE WH-MRI in detecting myocardial hyperemia in patients with acute myocarditis. Therefore, the aim of this study was to evaluate the potential of CE WH-MRI as a novel approach for diagnosing acute myocarditis. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-2293/rc).

Methods

Study population

This retrospective, cross-sectional study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments and was approved by the Fujian Medical University Union Hospital (No. 2019-KJCX030). Written informed consent was obtained from all participants. We reviewed the clinical database of 54 patients admitted to Fujian Medical University Union Hospital between May 2020 to March 2024 with clinically suspected acute myocarditis. The diagnostic guidelines established by the European Society of Cardiology (ESC) were applied in this study (22). CMR is considered to constitute diagnostic evidence of myocarditis when (I) at least one T2-based criterion (indicating myocardial edema) and (II) at least one T1-based criterion (reflecting either hyperemia/capillary leakage or fibrosis) are met (12). The inclusion criteria for patients in this study were: (I) new onset of symptoms and signs suggestive of myocarditis; (II) elevated necrosis biomarkers; (III) a history of recent viral infection; and (IV) a lack of coronary artery disease (CAD). Meanwhile, the exclusion criteria were as follows: (I) a history of myocardial infarction; (II) contraindications to cardiac magnetic resonance imaging (MRI); (III) atrial fibrillation or obvious arrhythmia; and (IV) renal insufficiency (estimated glomerular filtration rate assessed by creatinine clearance <60 mL/min/1.73 m²). All enrolled patients underwent CMR imaging at the acute phase after symptoms’ onset. The control group comprised 43 healthy individuals and outpatients who had been referred due to nonspecific thoracic pain. Importantly, none of the participants in the control group exhibited any structural abnormalities as detected on CMR imaging. Outpatients had no documented history of cardiac disease, exhibited no recognized cardiovascular risk factors, and had outcomes of electrocardiogram (ECG) and echocardiographic assessment within the normal range. The abdominal belt was wrapped tightly in patients with an irregular breath pattern to reduce the abdominal movement during magnetic resonance (MR) scan. This study was approved by the institutional review board and local ethics committee. The flowchart of patient enrollment is provided in Figure 1.

Figure 1 Flowchart of patient enrollment. b-SSFP, balanced steady-state free precession; CE WH-MRI, contrast-enhanced whole heart magnetic resonance imaging; ECG, electrocardiogram; LGE, late gadolinium enhancement; LLC, Lake Louis Criteria; T2-STIR, T2-weighted short tau inversion recovery.

CMR protocol

Cardiac MRI was performed with a whole-body 3T MR system (MAGNETOM Prisma, Siemens Healthineers, Erlangen, Germany) with an 18-channel body matrix coil combined with a 32-channel spine matrix coil. The R-wave acquired from a wireless vectorcardiogram was used to trigger the data acquisition. The CMR acquisition protocol for the myocarditis group and healthy control group is described below.

Myocardial edema was evaluated under a breath-hold with a black-blood, T2-weighted short tau inversion recovery (T2-STIR) sequence acquired in four-chamber long-axis and short-axis orientations covering the entire left ventricular (LV) myocardium before contrast medium was administered. Assessment of myocardial edema was performed under a breath-hold with a black-blood T2-STIR sequence, acquired in four-chamber long-axis and short-axis planes to encompass the full left LV myocardium prior to contrast agent administration. Breath-hold balanced steady-state free precession (b-SSFP) cine sequences were used to assess cardiac function, with acquisitions performed in short-axis, two-chamber, and four-chamber planes in accordance with a standardized protocol. Native T1 mapping, postcontrast T1 mapping, and T2 mapping were performed under motion-corrected Look-Locker inversion recovery. Both T1 and T2 mapping were acquired in three short-axis slices (basal, midventricular, and apical).

Inflammation-related myocardial hyperemia-weighted signal detection was conducted with a prospective navigator-gated, ECG-triggered, fat-suppressed, inversion recovery-prepared, segmented 3D FLASH sequence. Contrast enhancement was achieved via slow infusion of gadobenate dimeglumine (0.2 mmol/kg body weight) at 0.3 mL/s, which was followed by a 15-mL saline flush at the same infusion rate. Data acquisition commenced 60 seconds postcontrast initiation. Imaging parameters included repetition time =320 ms, echo time =1.4 ms, flip angle =20°, matrix size =256×256, field of view =220×330 mm², voxel resolution =0.65×0.65×0.9 mm³, readout bandwidth =610 Hz/pixel, and parallel imaging acceleration factor =2. Background tissue suppression was performed with a nonselective inversion recovery pulse [inversion time (TI) =200 ms]. Finally, myocardial necrosis assessment was performed with LGE imaging, acquired via a 2D phase-sensitive inversion-recovery (PSIR) gradient-echo sequence following gadolinium-based contrast agent administration (10–15 min’ postinjection). Images were obtained in four-chamber, two-chamber, and short-axis orientations to ensure comprehensive coverage of the LV myocardium. The TI was optimized in order to nullify the signal from the normal myocardium (TI =250–400 ms, decided by the TI scout).

Image analysis

All CMR examinations were performed by the same operator. All CMR studies were analyzed offline with a dedicated workstation (Syngo.via, Siemens Healthineers). Images were analyzed in consensus by two cardiovascular radiologists with 10 and 20 years of CMR experience in a random order. Functional analysis, including LV end-diastolic volume (LVEDV), LV ejection fraction (LVEF), and LV mass index (LVMI) was conducted. In T2-STIR images, edema was considered positive when the ratio of the signal intensity of the myocardium to that of the skeletal muscle was greater than 1.9 (11). Native T1 value, T2 value, and ECV were measured with postprocessing software. Endocardial and epicardial contours were manually drawn on the apical, midventricular, and basal short-axis images, and the average values were calculated to obtain the mean global native T1 value, T2 value, and ECV (23). LGE was assessed through visual confirmation of a nonischemic pattern of distribution (i.e., subepicardial or midmyocardial enhancement). The CE WH-MRI was also visually assessed for the presence of myocardial hyperintense areas in multiplanar reformations of any orientation. The segment of myocardium with high signal intensity was deemed positive. Furthermore, when hyperintense areas in the LGE and CE WH-MRI images were doubtfully or reliably interpreted by the two observers, this was regarded as inconclusive or definite, respectively. The LV myocardium was divided into 17 segments according to the American Heart Association (AHA) consensus, which allowed us to evaluate the presence of a hyperemia-weighted pattern or LGE. The definite hyperintense myocardial areas of CE WH-MRI-reconstructed images and LGE images at the same level were first identified visually on the short-axis orientation.

Statistical analysis

Continuous variables are presented as the mean ± standard deviation and were tested first with the Kolmogorov-Smirnov test for normality and then with the Levene test for variance homogeneity. For normally distributed data, the independent-samples t-test was used for statistical comparisons. A paired Mann-Whitney test was used for data, which was not normally distributed. Count data are expressed as percentages and as the median and interquartile range, and comparisons between groups were completed with the χ² test or Mann-Whitney test.

The statistical analysis was conducted with SPSS 26.0 software (IBM Corp., Armonk, NY, USA). A two-sided P value <0.05 was considered to indicate statistical significance.

Results

Forty-three participants were enrolled according to the inclusion criteria. Baseline features of the myocarditis cohort are summarized in Tables 1,2. Among patients with myocarditis, the most common clinical manifestation was chest pain (37/43, 86.05%), while fever (28/43, 65.12%) was relatively less common. All patients had increased troponin levels (43/43, 100%), and ECG abnormalities were found in 24 of 43 (55.81%) patients. Invasive coronary angiography (ICA) was performed in 37.21% of the patients, and coronary computed tomography angiography was performed in 32.56% of the patients, which ruled out significant CAD. The remaining 30.23% of the patients younger than 30 years old did not undergo coronary artery angiography due to low suspicion of CAD risk. Forty-three healthy control participants with normal results on cardiac MRI were enrolled. Healthy participants were similar to the patients with myocarditis in terms of age (39.69±11.49 vs. 43.01±17.94 years; P=0.353), sex (25 males vs. 26 males; P=0.826), and BMI (23.57±2.79 vs. 22.45±3.0 kg/m²; P=0.077), with no statistical differences.

Cardiac MRI was performed at a median of 7 days [interquartile range (IQR), 5–11 days] from the onset of clinical symptoms. The average acquisition time of CE WH-MRI was 8.2±1.3 min. The mean heart rate during CE WH-MRI was 74±9 beat/min, and the average navigator acceptance rate was 37.1%±5.2%. There was no statistical difference in the LVEF between patients with myocarditis (median 62%, IQR 55.5–66%) and healthy controls (median 60%, IQR 59–65%) (P=0.091). Myocardial edema in T2-STIR images was found in 30 of the 43 (69.77%) patients with myocarditis. Hyperintense regions in the myocardium on CE WH-MRI images were evident in most of the patients with myocarditis (95.35%). LGE was detected in 29 of 43 (67.44%) patients and was mostly subepicardial and midwall but not subendocardial, which was roughly consistent with the T2-STIR findings. The enhancement pattern in patients with myocarditis was mostly focal but less diffused. The CE WH-MRI sequence identified 322 myocardial segments with involvement, while the 2D LGE images indicated 210 segments as being involved (Figure 2). A subset of 112 segments remained inconclusive or undetected by the LGE method. The confirmed hyperenhanced regions of LGE were all found by CE WH-MRI. A representative example is shown in Figure 3.

Figure 2 Bull’s eye maps for the spatial distribution of the prevalence of (A) CE WH-MRI and (B) LGE by segment. CE WH-MRI, contrast-enhanced whole-heart magnetic resonance imaging; LGE, late gadolinium enhancement.

Figure 3 A 27-year-old male patient with acute myocarditis presenting with fever and chest pain. (A,C) CE WH-MRI and (B,D) LGE images on a short-axis and four-chamber long-axis views at the same largest slice location showed multiple hyperintensities in the left ventricular wall (black arrows: the interventricular septum; white arrows: the left ventricular lateral wall). (E) CE WH-MRI-reconstructed volume rendering image provided an overview of myocardial damage in the heart. CE WH-MRI, contrast-enhanced whole-heart magnetic resonance imaging; LGE, late gadolinium enhancement.

Discussion

In this study, the mean acquisition time of CE WH-MRI was 8 min. Using 3D k-space data acquired with a centric ordering scheme along the phase-encoding direction, we conducted CE-FLASH data acquisition in the initial minutes, which was crucial for determining image contrast. The remaining acquisition time was primarily dedicated to capturing the anatomical details of the image. In other words, the CE WH-MRI acquired the central k-space data precisely during the early vascular phase. To the best of our knowledge, myocardial hyperemia is considered to be increased vascular permeability and blood flow leading to the increased uptake of contrast agents during acute inflammation; this phase lasts for the first minutes (2–3 min) after gadolinium administration. Thus, the acquisition time is a key factor for assessing myocardial hyperemia. LGE can reflect myocarditis-related necrosis 4–5 min following the injection. Therefore, the CE WH-MRI provides temporal information that captures early hyperemia (as reflected by central k-space data) and late myocardial necrosis, as identified by LGE. In fact, myocardial hyperemia and necrosis may manifest in the same myocardial injury segments but represent distinct pathophysiological phenomenon. Therefore, LGE images and CE WH-MRI images can be combined to produce the hyperenhancement of damaged regions in myocarditis-related tissue. In summary, we believe that CE WH-MRI likely reflects the myocardial hyperemia-weighted pattern in acute myocarditis.

Our study is novel in that it used CE WH-MRI to evaluate acute myocarditis. The findings of our study indicate that CE WH-MRI outperforms LGE imaging in detecting a broader range of segmental myocardial involvement and facilitates the direct assessment of nonischemic distribution patterns within the myocardium. The key determinants of this outcome can be summarized as follows. First, the CE WH-MRI images obtained with the FLASH sequence demonstrated superior spatial resolution, characterized by a threefold reduction in voxel size compared as to the T2-STIR and LGE imaging modalities. Such a high resolution translated into an improved visibility of small myocardial injuries and a clear distinction between a subendocardial and a subepicardial primary location of the injury, thus leading to a higher rate of definite myocardial lesions. Previous studies have demonstrated the value of LGE imaging in the diagnosis of myocardial infarction and myocarditis (24,25). Nevertheless, we found high rates of negative or inconclusive results after the standard LGE imaging. The limited spatial resolution of CMR may lead to a failure in the detection of the small regions of necrotic myocytes associated with early phases of inflammation (26). Thus, smaller lesions in the myocardium causing a negative or uncertain diagnosis remains a major challenge in clinical cardiology. In 2020, Lintingre et al. (27) proposed a high-resolution LGE (voxel size 1.25 mm × 1.25 mm × 2.5 mm) imaging method for the diagnosis of myocardial infarction using a free-breathing method as an alternative strategy, which improved diagnostic confidence. However, this method had a relatively lower resolution in the through-plane direction as compared to the CE-FLASH sequence and had a longer overall exam duration. Similarly, in our study, CE WH-MRI was able to uncover or confirm small myocardial lesions, especially those located at the apex of the heart. Therefore, the advantage of enhanced spatial resolution provided by the CE-FLASH sequence at 3T is significant. Furthermore, since the gadolinium contrast agent is administered intravenously and only distributes to the extracellular space, LGE is unable to detect intracellular edema in the early stages of myocarditis (28). Moreover, the increased accumulation of gadolinium in CE WH-MRI may be caused by myocardial hyperemia in the early washout phase and necrosis in the later washout phase. In addition, 2D techniques, such as T2-STIR and 2D-LGE, are typically carried out in an alternating manner within one or multiple adjacent acquisitions, which can lead to misalignment or obscuration of anatomical structures if there is inconsistent breath-holding. Conversely, the 3D FLASH pulse sequence allows for the acquisition of thinner slices without any gaps between them, facilitating multiplanar reformation in any desired projection and providing a unique overview of cardiac anatomy. Additionally, CE WH-MRI performed during free breathing is especially beneficial for patients who have difficulty adhering to breath-hold instructions.

Furthermore, CE WH-MRI images were obtained following the administration of gadolinium, prior to the acquisition of LGE images. In theory, LGE data acquisition commences 10–15 min after the injection of contrast media, meaning that CE WH-MRI does not add any extra time to the procedure. Additionally, unlike breath-hold T2-STIR and LGE imaging, CE WH-MRI permits free breathing throughout the MR examination, thus avoiding any discomfort to the patient.

Due to the variety of clinical presentations, especially with ST elevation in the ECG, the clinical diagnosis of acute myocarditis should exclude CAD through the use of ICA or computed tomography coronary angiography. However, they have the disadvantages of high costs, invasiveness, and ionizing radiation in clinical practice. CE WH-MRI at 3T has emerged as a promising noninvasive imaging modality for the assessment of coronary artery stenoses and has shown excellent results in previous studies (20,21). In 2020, Sun et al. (21) demonstrated that CE WH-MRI and dual-source computed tomography coronary angiography have similar diagnostic accuracies. Thus, CE WH-MRI is regarded as a valuable imaging method for identifying significant coronary artery stenosis, offering an additional advantage for the noninvasive and radiation-free diagnosis of myocarditis. In this retrospective study, the CE WH-MRI accurately identified 2 patients with significant coronary stenosis and myocardial infarction. The CE WH-MRI and ICA images are shown in Figure 4.

Figure 4 A 60-year-old female patient presenting with chest pain, absence of fever, and ECG with ST segment elevation. Short-axis and four-chamber long-axis CE WH-MRI images. (A,C) Increased signal (arrows) in the midventricular region. (B,D) Short-axis and four-chamber long-axis LGE images were considered negative. MIP images (E) of CE WH-MRI showed a normal RCA, LAD, and LCX. CE WH-MRI, contrast-enhanced whole-heart magnetic resonance imaging; ECG, electrocardiogram; LAD, left anterior descending artery; LCX, left circumflex artery; LGE, late gadolinium enhancement; MIP, maximum intensity projection; RCA, right coronary artery.

Certain limitations to this study should be mentioned. First, we employed a retrospective, single-center design with a very small sample size. A prospective larger sample size would further provide more robust results. Second, the diagnosis of myocarditis was performed only by the summation of clinical and CMR findings, and EMB was not performed. Third, CE WH-MRI may not isolate hyperemia and necrosis due to its longer acquisition time. Finally, a limitation of the CE WH-MRI is its susceptibility to irregular breathing patterns, which led to image degradation in this study.

Conclusions

This study established the viability of CE WH-MRI in identifying myocardial hyperemia-weighted patterns among patients with acute myocarditis. Additionally, with the combination of quantitative CMR and established LLC parameters, CE WH-MRI can provide additive value for enhancing the accuracy of diagnosing acute myocarditis.

Acknowledgments

The authors would like to thank the members of cardiac magnetic resonance team at Fujian Medical University Union Hospital for their exceptional collaboration, rigorous quality control of the imaging procedures. And portions of this work were previously presented at the 2021 Annual Meeting of the International Society for Magnetic Resonance in Medicine (ISMRM).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-2293/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-24-2293/dss

Funding: This study was supported by the Joint Funds for the Innovation of Science and Technology, Fujian Province (No. 2019Y9095).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-2293/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments and study was approved by the Fujian Medical University Union Hospital (No. 2019-KJCX030). Written informed consent was obtained from all individual participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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