Epicardial fat volume assessment and strain analysis by cardiac magnetic resonance: a novel method for evaluating microcirculation dysfunction after myocardial infarction

Introduction

Acute ST-segment elevation myocardial infarction (STEMI) is a severe type of coronary heart disease, primarily due to coronary artery obstruction leading to acute ischemic necrosis of the myocardium. Despite a decline in STEMI with the improvement in medical standards and lifestyle, it remains a significant public health issue worldwide, especially in developing countries. Prevention and early intervention are key to reducing the incidence of STEMI and improving prognosis.

The goal of STEMI treatment is to restore myocardial perfusion as quickly as possible, save the myocardium, and prevent infarct expansion. Current reperfusion therapies mainly involve percutaneous coronary intervention (PCI) or thrombolysis. However, after the culprit vessel is reopened, microcirculation reperfusion cannot be fully guaranteed, leading to areas of no reflow in the myocardial ischemic region, known as microvascular obstruction (MVO). MVO can be seen in patients with acute myocardial infarction (AMI) after coronary artery occlusion reperfusion (1), some patients with acute extensive myocardial ischemia, and those with late MVO (2). Its characteristic is the damage and dysfunction of the myocardial microvascular system, with no reflow phenomenon in the infarct area (3), ultimately leading to reduced tissue perfusion and the formation of an infarct zone, mainly extending from the endocardium to the epicardium (4,5). Cardiac magnetic resonance (CMR) imaging is the gold standard for MVO assessment, with MVO appearing as low signal areas within the late gadolinium enhanced (LGE) myocardial region (6). Cardiac imaging plays a crucial role in the diagnosis and treatment process of MVO. Contrast-enhanced steady-state free precession (CE-SSFP) technology combines LGE and steady-state free precession, accurately quantifying MVO, while CMR imaging has a unique ability to extensively analyze cardiac deformation, volume, myocardial morphology, and tissue composition, with increasing evidence of its importance for prognosis and superiority over currently used clinical parameters (7).

Epicardial adipose tissue (EAT) serves as a fat storage reservoir in the heart and plays an important role in cardiac lipid metabolism, deposited between the myocardium and the visceral layer of the pericardium, covering more than 60% of the heart surface and accounting for about 20% of heart weight (8). Studies have found that EAT has potential roles in the progression of ventricular structural changes, functional pathophysiological changes, and clinical evolution in the context of AMI (9-11). Ultrasound is the simplest, convenient, and highly safe method for measuring EAT, directly detecting the thickness of EAT at the right ventricular free wall to assess the overall distribution of EAT in the heart. Although this method is non-invasive, fast, and relatively inexpensive, it has many obvious limitations. Ultrasound finds it difficult to differentiate EAT or pericardial fat and may be affected by the operator’s technique and many other factors. Compared to ultrasound, spiral computed tomography (CT) not only accurately measures the thickness of EAT at each level but also has the advantage of repeatable operation. After certain post-processing on the computer, the overall epicardial fat volume (EFV) can be obtained. However, coronary CT angiography (CTA) examination must be completed with intravenous injection of iodinated contrast agents and emits certain radiation to the human body.

Magnetic resonance imaging (MRI) is a non-invasive, non-ionizing radiation, high soft tissue resolution technique, with significant advantages in the quantitative measurement of fat in some visceral organs. At the same time, CMR can meticulously depict cardiac structure and function and provide more accurate and quantitative assessments of ventricular volume, myocardial mass, and cardiac function. Myocardial strain measures the spatial vectors in the longitudinal, axial, and radial predefined directions during the entire cardiac cycle using an internal coordinate system aligned with the three axes of the heart. Longitudinal strain (LS) refers to longitudinal shortening, radial strain (RS) refers to radial thickening, and circumferential strain (CS) refers to circumferential rotation (12). Myocardial strain can be divided into global myocardial strain and segmental myocardial strain, usually referring to the 17-segment division of the left ventricle by the American Heart Association. Previous studies have shown that myocardial strain has a high diagnostic efficiency for early changes in the heart. After AMI, myocardial contractile function is impaired, and animal experiments and clinical studies have confirmed significant changes in myocardial strain after AMI. Animal experiments have found that global CS (GCS) is significantly reduced on both early 9±2 days and late 33±10 days after myocardial infarction compared to before infarction, and studies have shown that the myocardial strain in the remote area of myocardial infarction decreases after the occurrence of heart failure compared to before the occurrence of heart failure, with global LS (GLS) being a more sensitive parameter for assessing local myocardial dysfunction (13).

As a parameter that has emerged in recent years to evaluate the overall and local movement and function of the myocardium, myocardial strain is increasingly widely used in non-invasive assessment of the heart. CMR, with its high resolution and one-stop non-invasive assessment of the heart, is currently recognized as the gold standard for quantitative evaluation of changes in cardiac tissue function after myocardial infarction (14).

Therefore, this study uses CMR to explore the degree of impairment of myocardial strain in myocardial infarction of different degrees and its impact on local left ventricular function, and to quantitatively analyze EFV, discuss the relationship with MVO, and provide a basis for early clinical evaluation and treatment. We present this article in accordance with the STARD reporting checklist (available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-359/rc).

Methods

General data and grouping

STEMI patients who were admitted to The First Affiliated Hospital of Bengbu Medical University from June 2022 to December 2023 were included in this retrospective study. Inclusion criteria: (I) diagnosed with STEMI according to the diagnostic criteria of the European Society of Cardiology (15); (II) first-time myocardial infarction, successfully treated with PCI; and (III) first CMR examination with image quality meeting the requirements. Exclusion criteria: (I) history of myocardial infarction; (II) history of PCI or coronary artery bypass grafting; and (III) contraindications for LGE-CMR examination (such as claustrophobia, etc.). After exclusion, a total of 80 STEMI patients were enrolled. Finally, 56 STEMI patients were included. The flow diagram refers to Figure 1. All patients underwent CMR examination within 6.1±2.2 days after PCI. The absence of low signal areas in the magnetic resonance (MR) delayed enhancement high signal infarcted myocardium was defined as the non-MVO (NMVO) group, and the presence of low signal areas in the MR delayed enhancement high signal infarcted myocardium was defined as the MVO group. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study received approval from the Ethics Committee of The First Affiliated Hospital of Bengbu Medical University (No. 2023YJS287). Patient informed consent was exempted given the retrospective nature of the study.

Figure 1 Flow diagram of patient selection. STEMI, ST-segment elevation myocardial infarction; MRI, magnetic resonance imaging; MVO, microvascular obstruction; NMVO, non-microvascular obstruction.

Research methods

CMR examination

All patients using the Siemens MAGNETOM Avanto 1.5-T magnetic resonance scanner (Siemens, Earlangen, Germany) equipped in the Radiology Department of The First Affiliated Hospital of Bengbu Medical University. The main scanning sequences included: ventricular short-axis, two-chamber, three-chamber, and four-chamber heart views with balanced steady-state free precession (bSSFP) cine imaging, triple inversion recovery (IR) sequence ventricular short-axis, and LGE. The parameters for the cine sequence were set as follows: repetition time (TR) 2.84 ms, echo time (TE) 1.25 ms, flip angle 180°, slice thickness 6.0 mm, resolution 1.4 mm × 1.8 mm. The LGE used an electrocardiogram (ECG)-triggered inversion recovery fast gradient echo sequence, with gadolinium-diethylene triamine pentaacetate (Gd-DTPA) contrast agent injected intravenously at a dose of 0.15 mmol/kg, starting the scan 10–30 minutes after the delay, with the following parameters: TR 904 ms, TE 1.98 ms, flip angle 20°, slice thickness 6.0 mm, resolution 1.4 mm × 1.9 mm.

Image processing

The images were uploaded to the CVi42 software platform (Circle Cardiovascular Imaging, Calgary, Canada) for post-processing, and all images were independently analyzed by two radiologists with over 5 years of experience in cardiac radiology. The observer performing the strain analysis was blinded to the baseline CMR parameters and advanced tissue characterization. Using the software’s built-in analysis functions, the endocardial and epicardial boundaries of the left ventricle at the end of systole and diastole in the two-, three-, and four-chamber heart views of the long-axis, and the basal, papillary muscle, and apical segments of the short-axis were manually outlined using a semi-automatic method. The papillary muscle was included in the ventricular cavity; the CMR software divided the left ventricular endocardium into 48 characteristic points and automatically tracked the endocardial and epicardial boundaries, calculating cardiac function parameters and myocardial strain indicators. The observer analyzed all CMR short-axis images using dedicated post-processing software (CVi42), Cardiac adipose tissue was quantified on all short-axis slices (base to apex) in end-diastolic phase, After the delineation was completed, the software automatically calculated the EFV, as shown in Figure 2. MVO, identifiable as a no-reflow area within the myocardial infarction characterized by a hypointense signal in the delayed enhancement images, is depicted in Figure 3.

Figure 2 Short-axis MR slices for different levels (basal to apical). (A) Not sketch level, step by step (B-H) sketch different levels of short-axis after MRI slices. Red line: myocardial intima; green line: pericardial; light green line: EAT. MR, magnetic resonance; MRI, magnetic resonance imaging; EAT, epicardial adipose tissue.

Figure 3 A 58-year-old male with an acute anterior myocardial infarction following PCI shows a hypointense area (red arrow) on delayed enhancement. PCI, percutaneous coronary intervention.

Statistical analysis

We used the Shapiro-Wilk and Kolmogorov-Smirnov tests to examine the normal distribution. Quantitative variables of data conforming to the normal distribution and non-normal distribution were represented by mean ± standard deviation and median [range or interquartile range (IQR)], respectively, while qualitative variable data were represented by n (%). The Mann-Whitney U test (Chi-squared test) was used to compare continuous variable datasets and non-parametric data. The two independent sample t-tests were used for comparison between the MVO group and the NMVO group. The results of the count data were represented by the number of cases or the percentage of the total, and the group comparison was made using the Chi-squared test. Univariate and multivariate logistic regression analyses were used to determine the independent predictive factors for MVO, with variables with P values <0.10 in the univariate analysis being included in the multivariate model. The predictive value of the EFV indicator for MVO was evaluated using the area under the receiver operating characteristic (ROC) curve (AUC). Cardiac function and myocardial strain parameters were analyzed using Pearson’s correlation analysis, with correlation coefficients of 0.8–1.0 being extremely strong, 0.6–0.7 being strong, 0.4–0.5 being moderate, 0.2–0.3 being weak, and 0.0–0.1 being extremely weak or no correlation. All analyses were performed using SPSS 26 (IBM, Chicago, IL, USA), Medcalc 20.0 (Medcalc, Ostend, Belgium), and GraphPad Prism (Prism 9 for Windows, San Diego, CA, USA). A two-tailed P value <0.05 was considered statistically significant.

Results

Comparison of clinical data of patients

A retrospective study was conducted on 56 patients who underwent PCI diagnosed with acute STEMI by coronary angiography at The First Affiliated Hospital of Bengbu Medical University from June 2022 to December 2023. There were 42 male patients (accounting for 75%) with an average age of 59.84±12.37 years. There were no significant differences in age, male gender, body surface area (BSA), underlying diseases, left ventricular end-diastolic volume, left ventricular end-systolic volume, and left ventricular end-diastolic diameter between the two groups (P>0.05). However, the left ventricular ejection fraction in the MVO group was significantly lower than that in the NMVO group (P=0.001), and the heart rate in the MVO group was higher than that in the NMVO group. As shown in Table 1.

Diagnostic efficacy of EFV, myocardial strain, and combined analysis for MVO

The GLS, global RS (GRS), and GCS in the MVO group were all significantly lower than those in the NMVO group (P<0.001); the EFV in the MVO group was higher than that in the NMVO group (P<0.001). The ROC curve analysis showed that among the three, the best diagnostic efficacy was for GLS (AUC: 0.929; sensitivity: 90.90%; specificity: 94.12%), with a Youden index of 0.85. EFV predicted MVO (AUC: 0.856; sensitivity: 77.27%; specificity: 91.18%); as shown in Tables 2,3.

Correlation between EFV and global myocardial strain parameters of the left ventricle

First, the EFV was normalized using BSA to obtain the normalized EFV (EFVnormalized). A scatter plot of EFVnormalized and global myocardial strain parameters of the left ventricle for 22 patients in the MVO group was drawn, as shown in Figure 4. Pearson correlation analysis showed that GRS (r=−0.38, P=0.08) and GLS (r=0.26, P=0.63) had a weak correlation with EFV, while the correlation between GCS (r=0.11, P=0.24) with EFV was weaker and not statistically significant.

Figure 4 GRS, GCS, GLS, and EFV linear relationship. EFVnormalized, the EFV was normalized using BSA to obtain the normalized EFV. EFV, epicardial fat volume; BSA, body surface area; GRS, global radial strain; GCS, global circumferential strain; GLS, global longitudinal strain.

ROC curves for predicting MVO using EFV, myocardial strain, and combined diagnosis

The ROC of the combined analysis predicted MVO [AUC: 0.945; 95% confidence interval (CI): 0.850–0.988; sensitivity 95.45%; specificity 91.59%]; the AUC value and sensitivity were higher than those of single diagnosis, as shown in Figure 5.

Figure 5 ROC curve of combined analysis of CMR parameters and EFV in the diagnosis of microcirculatory disturbance in STEMI patients after PCI. EFV, epicardial fat volume; GCS, global circumferential strain; GLS, global longitudinal strain; GRS, global radial strain; ROC, receiver operating characteristic; CMR, cardiac magnetic resonance; STEMI, ST-segment elevation myocardial infarction; PCI, percutaneous coronary intervention.

Independent predictive parameters for MVO based on multivariate logistic regression analysis

In multivariate logistic regression, GLS [odds ratio (OR) =1.910; 95% CI: 1.137–3.206; P=0.01] and EFV (OR =1.077; 95% CI: 1.013–1.144; P=0.02) were independent predictive factors for MVO, as shown in Table 4 and Figure 6.

Figure 6 Multivariate logistic regression analysis to identify the risk factors associated with the occurrence of MVO in patients with STEMI. *, GLS and EFV were independent predictive factors for MVO. GRS, global radial strain; GCS, global circumferential strain; GLS, global longitudinal strain; EFV, epicardial fat volume; LVEF, left ventricular ejection fraction; HR, heart rate; CI, confidence interval; MVO, microvascular obstruction; STEMI, ST-segment elevation myocardial infarction.

Correlation between MVO and EFV, left ventricular global myocardial strain parameters

Spearman correlation analysis showed that EFV (r=0.602, P<0.001), GLS (r=0.726, P<0.001), GCS (r=0.457, P<0.001) was significantly positively correlated with postoperative myocardial infarction with mcrocirculation obstruction, while GRS (r=−0.486, P<0.001) were negatively correlated with postoperative myocardial infarction with mcrocirculation obstruction, as shown in Table 5.

Discussion

Studies have shown that the volume of EAT is associated with an increased incidence of cardiovascular disease (CVD) (16). However, there is limited research on its impact on MVO after myocardial infarction. Additionally, they all analyze the relationship between MVO and EFV with myocardial strain separately. Therefore, this study constructs a combined model of EFV and myocardial strain to enhance the diagnostic performance for MVO. Meanwhile, this study primarily explored the correlation between EFV and MVO and left ventricular myocardial strain in patients after AMI who underwent PCI. In the study, we used CMR and tissue tracking technology to quantify left ventricular myocardial function. When measuring EFV, CMR was used for quantitative measurement of EFV, rather than cardiac CT volume measurement or echocardiographic local thickness measurement. The final analysis results showed that after myocardial infarction, the MVO group had more EFV content and greater reduction in GLS, GRS, and GCS compared to the NMVO group. Multivariate regression analysis indicated that GLS and EFV are independent influencing factors for MVO after myocardial infarction.

EAT is deposited in the fat layer between the pericardium and myocardium, closely contacting the myocardium, and there is no fascial tissue between them (17). It has a mechanical protective effect on the heart and can directly transport fatty acids to the myocardium, serving as an energy source for the myocardium (18). EAT also participates in the synthesis, production, and secretion of various bioactive molecules (19,20), and is the main source of a large number of free fatty acids and bioactive molecules (such as adiponectin, leptin, and inflammatory cytokines). However, excessive secretion of fatty acids by EAT exceeds the myocardial oxidation capacity, leading to the accumulation of intermediates such as ceramides, which in turn leads to myocardial cell apoptosis and fibrosis (21,22). An increase in EFV increases the secretion of pro-inflammatory adipokines (leptin, mucin, interleukin-1β, interleukin-6, and antibodies), directly causing an increase in paracrine effects leading to inflammation and fibrosis in adjacent myocardium (23,24). Additionally, the protective or harmful effects of EAT on coronary arteries and myocardial cells mainly depend on the relationship between EAT and the microenvironment (20,25). In patients who undergo PCI after AMI, factors such as cytotoxic factors, inflammatory reactions, and vasoconstriction, as well as microthrombi caused by atherosclerotic debris in the distal lumen, platelet plugging, and cellular edema after reperfusion, can lead to MVO (26,27). After the acute phase, MVO gradually fibroses during the formation of myocardial scar tissue. Therefore, an increase in EFV in such patients indicates the occurrence of MVO, suggesting a more severe degree of myocardial infarction (28,29). In this study, the MVO group had more EFV content than the NMVO group. Based on the EFV content, a prediction model for myocardial infarction with combined MVO was constructed, with an AUC value of 0.856, a sensitivity of 77.27%, and a specificity of 91.18%.

Due to the highly complex functional changes in acute STEMI, it is particularly important to comprehensively assess left ventricular function in the early stages after STEMI (30). CMR strain technology can well diagnose and assess the early stages of ischemic myocardial dysfunction that are not easily detected by conventional diagnostic methods (31). This study showed that the LVEF, GLS, GRS, and GCS in the MVO group were lower than those in the NMVO group. GLS has a significantly higher diagnostic efficacy for MVO after PCI in STEMI patients than GCS and GRS, which is consistent with previous studies (32). In the studies by Cherian et al. and Zhang et al., GLS was proven to be a strong predictor of left ventricular remodeling and adverse events (such as congestive heart failure and death) (23,33). This may be because the irreversible myocardial ischemia caused by STEMI first affects the longitudinal myocardial fibers of the subendocardium, thereby affecting the longitudinal myocardial contraction represented by GLS (33).

In this study, correlation analysis showed that EFV, GLS, and GCS were significantly positively correlated with postoperative myocardial infarction combined with MVO; while GRS, were negatively correlated with postoperative myocardial infarction combined with MVO. The diagnostic sensitivity and AUC value of myocardial strain parameters (GLS, GRS, GCS) combined with EFV volume in MVO after PCI in STEMI patients were higher than those of single diagnosis. In the analysis of the correlation between EFV and global myocardial strain parameters of the left ventricle, it was found that GRS and GLS had a weak correlation with EFV, and an extremely weak correlation with GCS. This indicates that the changes in cardiac function after myocardial infarction cannot be predicted by a single condition alone; it is necessary to combine clinical symptoms, routine blood indicators such as N-terminal pro-brain natriuretic peptide (NT-proBNP), and other indicators for joint analysis. CMR, as a non-invasive, radiation-free imaging method, can provide various quantitative indicators (myocardial strain capacity, infarct area size, microcirculation resistance index, etc.), all of which are important parameters for evaluating the patient’s cardiac function status (34-36).

Limitations

Due to the small sample size of this experiment and only studying the overall strain parameters, and the lack of detailed classification and treatment of the infarct area combined with intramyocardial hemorrhage (IMH), further research and expansion of the sample size are still needed. Secondly, this study found that EFV is an independent determinant of MVO, indicating that to some extent, an increase in EFV content is a partial cause of the occurrence of MVO and left ventricular myocardial dysfunction and reduced myocardial strain, but the specific mechanism still needs further research.

Conclusions

In summary, through CMR imaging, a close correlation between EFV and MVO can be found, which can serve as an important functional imaging parameter for acute myocardial pathological changes in patients with acute STEMI. Combined with GLS, GRS, GCS, and clinical-related indicators, it can provide prognosis assessment and treatment strategies for clinical practice.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist. Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-359/rc

Data Sharing Statement: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-359/dss

Peer Review File: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-359/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-359/coif). M.L. is a current employee of Siemens Healthineers Ltd., Shanghai. The other 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. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study received approval from the Ethics Committee of The First Affiliated Hospital of Bengbu Medical University (No. 2023YJS287). Patient informed consent was exempted given the retrospective nature of the study.

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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