Right ventricular end-systolic remodeling index on cardiac magnetic resonance imaging: comparison with other functional markers in patients with chronic thromboembolic pulmonary hypertension

Introduction

Chronic pulmonary thromboembolism (CTE) (1-3) results from incomplete lysis of acute pulmonary embolism with the subsequent organizationof residual thrombus. It may lead to pulmonary arterial pressure, pulmonary vascular resistance, and right heart dysfunction, which is called chronic thromboembolic pulmonary hypertension (CTEPH). The right ventricle and pulmonary vasculature are integrally related, and measures of right ventricular afterload, stress, and functional adaptation provide important prognostic information for patients with pulmonary hypertension (PH) (4). This is also extremely important for patients with CTEPH.

Echocardiography is the tool most widely available for monitoring the ventricular function of patients with PH. Amsallem et al. (5) reported that the right ventricular end-systolic remodeling index (RVESRI) measured on the right ventricular apical 4-chamber echocardiographic view strongly predicted outcomes in pulmonary arterial hypertension (PAH). However, the technique has several limitations that limit the accurate evaluation of right ventricular performance, especially operator experience dependence and patient-dependent echo windows. Due to the high spatial resolution and the independence of the doctor’s experience, cardiac magnetic resonance imaging (CMR) can show the anatomical complexity of the right ventricle and quantify ventricular function, blood flow, myocardial perfusion, and fibrosis (6-8). So far, the application of RVESRI measured on CMR in the assessment of CTEPH has not been investigated. Thus, the current objective was to assess the reproducibility of RVESRI measured with CMR to determine whether RVESRI correlates with other CMR functional parameters and hemodynamics measured with right heart catheterization (RHC) in patients with CTEPH.

Methods

Study design

This study was registered at the Chinese Clinical Trials Registry Center (http://www.chictr.org/en/; registration number ChiCTR-OCH-14004929) and was approved by our institutional review board (IRB No. 2017-24). The study was conducted following the Declaration of Helsinki (as revised in 2013), and all patients signed informed consents. We retrospectively included 64 patients (45±14 years, 37 males), including 46 patients with CTEPH and 18 with CTE from January 2017 to January 2020. All patients who underwent RHC and CMR within 1 week in our hospital were included. CTEPH was diagnosed by tissue pathology from pulmonary endarterectomy, characteristic findings on CT pulmonary angiography or ventilation-perfusion scintigraphy, and elevated pulmonary arterial pressure and pulmonary vascular resistance measured with RHC. CTE was diagnosed by a prior history of acute pulmonary embolism, characteristic findings on CT pulmonary angiography or ventilation-perfusion scintigraphy, and normal pulmonary arterial pressure and pulmonary vascular resistance measured with RHC. The flowchart of this study is shown in Figure 1.

Figure 1 The flowchart of the study. CTEPH, chronic thromboembolic pulmonary hypertension; CTE, chronic pulmonary thromboembolism; CMR, cardiac magnetic resonance imaging; RHC, right heart catheterization.

CMR

All patients underwent CMR on a 1.5 Tesla clinical MR scanner (MAGNETOM Area, Siemens Healthcare, Erlangen, Germany) with an 18-channel phased-array surface coil. All images were acquired with retrospective electrocardiographic gating in the end-expiratory breath hold. Standard contiguous short-axis slices covering both ventricles from base to apex and long-axis 4-chamber cine images were acquired with the balanced steady-state free precession sequence. The typical acquisition parameters included repetition time/echo time 34.5/1.1 ms, flip angle 50–60°, slice thickness 6 mm, in-plane spatial resolution 1.8×1.8 mm², temporal resolution 40 ms, and 25 reconstructed cardiac phases.

CMR analysis

RVESRI is the ratio of the lateral free wall length to septal wall height in the end-systolic phase (5) and was independently measured on the long-axis 4-chamber cine image of CMR (Figure 2) by 2 residents with 5 years of experience on the picture archiving and communication system. After one month, the measurement of RVESRI was repeated by one resident. Moreover, the right ventricular eccentricity index (RVEI) (9) was also calculated on short-axis cine images at the mid ventricular level of the right ventricle in the end systole by one resident with 4 years of experience.

Figure 2 Measurement of right ventricular end-systolic remodeling index (RVESRI) on the 4-chamber cine image of cardiac magnetic resonance imaging (CMR) in end systole. RVESRI was the ratio of end-systolic lateral free wall length (red line) to interventricular septal height (blue line).

RV functional metrics were measured on the short-axis and long-axial 4-chamber cine images with the commercial software, CardiacFunction, on SyngoVia workstation (Siemens Healthcare, Erlangen, Germany) by a resident with 4 years ofexperience. Right and left ventricular epicardial and endocardial surfaces were traced from the contiguous short-axis cine images. End-diastole and end-systole, respectively were defined as the first cine phase of the R-wave triggered acquisition or the largest volume and the smallest cavity area. From the end-diastolic and end-systolic volumes, right ventricular and left ventricular end-diastolic and end-systolic volumes/body surface area (RVEDVI, RVESVI, LVEDVI, LVESVI), right ventricular and left ventricular ejection fractions (RVEF and LVEF, respectively), cardiac output (CO), and right ventricular myocardial mass index (RVMI) were calculated.

Moreover, RV strain including right ventricular global longitudinal strain (RVGLS), circumferential strain (RVGCS), and radial strain (RVGRS) was analyzed from cine images in the 4-chamber view and short-axial views using CVI⁴² (Version 5.11, Circle Cardiovascular Imaging Inc., Calgary, Alberta, Canada) by a resident with 4 years of experience.

Hemodynamics

Hemodynamics were evaluated with RHC. Venous access was obtained by inserting an introducer into the internal jugular vein. A Swan-Ganz standard thermodilution pulmonary artery catheter was placed at the right inferior pulmonary artery. The metrics included diastolic pulmonary arterial pressure (DPAP), systolic pulmonary arterial pressure (SPAP), mean pulmonary arterial pressure (MPAP), right atrial pressure (RAP), pulmonary capillary wedge pressure (PCWP), and pulmonary vascular resistance (PVR). CO was determined using the Fick method.

Statistical analysis

Statistical analysis was performed using SPSS 22 (Chicago, IL, USA) and MedCalc statistical software (version15.6.1, Ostend, Belgium). Data are expressed as mean ± standard deviation (SD) or median with interquartile range (IQR). Bland-Altman plots and the intraclass correlation coefficient (ICC) for RVESRI were calculated for the intra- and inter-observer agreement. The differences in RV functional parameters, including RVESRI between CTEPH and CTE, were compared with the nonparametric Mann-Whitney U test. Spearman’s rank test was used to evaluate correlations between RVESRI and other RV functional parameters, plasma biomarkers, and hemodynamic metrics. A receiver operating characteristic (ROC) curve was used to analyzethe area under the curve (AUC) of the ROC curve and measure cut-off values of RVESRI, RVEI, the diameter of the main pulmonary artery (MPA), and the ratio of the MPA and ascending aorta diameter (MPA/AAo) in predicting MPAP ≥25 mmHg. Statistical comparisons of ROC curves were analyzed with the DeLong test (MedCalc statistical software). A P value <0.05 was considered statistically significant.

Results

Baseline characteristics

The demographic, clinical, and hemodynamic-derived information of all patients are shown in Table 1. There were no differences among CTEPH and CTE patients concerning age, sex, body mass index (BMI), systolic blood pressure (SBP), and diastolic blood pressure (DBP). A total of 19 patients (29.7%) were classified as World Health Organization (WHO) functional class I, 26 (40.6%) patients as WHO class II, patients 16 (25.0%) as WHO class III, and 3 (4.6%) patients as WHO class IV. Table 2 showed there was a significant difference between the RVESRI and other CMR functional metrics in patients with CTEPH and CTE, except for RVGRS, RVGCS, LVESVI, and LVEF.

Reproducibility of RVESRI measurements

A Bland-Altman plot (Figure 3A) of the RVESRI measurements from the 2 observers showed that the bias (difference between the means) was 0 and the 95% limits of agreement were between −0.12 and 0.11. A Bland-Altman plot (Figure 3B) of RVESRI measurements repeated by one observer showed that the bias (difference between the means) was 0 and the 95% limits of agreement were between −0.13 and 0.13. The ICC for intra-observer reproducibility was 0.96 [95% confidence interval (CI), 0.93–0.97] for RVESRI. The ICC for inter-observer reproducibility was 0.99 (95% CI, 0.98–0.99) for RVESRI.

Figure 3 Reproducibility of right ventricular end-systolic remodeling index (RVESRI) measurements by Bland-Altman plots. (A) Measurements of RVESRI by 2 independent observers and (B) measurements of RVESRI twice by one observer.

Correlation of RVESRI with RV functional metrics and plasma biomarkers

As shown in Table 3, RVESRI positively correlated with RVEDVI, RVESVI, RVMI, and RVGLS, while RVESRI negatively correlated with RVEI, RVEF, and RVCO in the total patients and CTEPH patients. RVESRI did not correlate with RVGRS or RVCRS. Figure 4 shows that RVESRI positively correlated with plasma N-terminal pro-brain natriuretic peptide (NT-proBNP) (r=0.85, P<0.001) and negatively correlated with six-minute walk distance (6MWD) (r=−0.79, P<0.001). RVESRI also correlated with cardiac troponin T (r=0.53, P<0.001) but did not correlate with D-dimer (r=0.06, P=0.65) or creatine kinase isoenzyme (r=0.16, P=0.23). Furthermore, in patients with CTEPH, RVESRI positively correlated with plasma NT-proBNP (r=0.75, P<0.001) and negatively correlated with 6MWD (r=−0.50, P=0.001).

Figure 4 Correlation analysis of the right ventricular end-systolic remodeling index (RVESRI) with plasma N-terminal pro-brain natriuretic peptide (NT-proBNP) and 6-minute walk distance (6MWD). (A) RVESRI positively correlated with plasma NT-proBNP (r=0.85, P<0.001). (B) RVESRI negatively correlated with 6MWD (r=−0.79, P<0.001).

Correlations of RVESRI with hemodynamics

Figure 5 shows that RVESRI positively correlated with RAP (r=0.64, P<0.001), MPAP (r=0.65, P<0.001), and PVR (r=0.69, P<0.001), while there was a negative correlation between RVESRI and CO (r=−0.64, P<0.001) in all patients. RVESRI did not correlate with PCWP (r=0.20, P=0.139). In patients with CTEPH, RVESRI positively correlated with MPAP (r=0.33, P=0.01) and PVR (r=0.42, P=0.003), while RVESRI was negatively correlated with CO (r=−0.52, P<0.001). RVESRI in patients with CTEPH did not correlate with RAP (r=0.24, P=0.053) or PCWP (r=0.16, P=0.211). Furthermore, Figure 6 shows the ROCs of RVESRI, RVEI, RVMI, MPA, and MPA/AAo in predicting MPAP ≥25 mmHg. Table 4 indicates that the AUC of RVESRI was comparable to RVEI and was more than RVMI, MPA, and MPA/AAo ratio. RVESRI >1.35 (optimal ROC cutoff) had a sensitivity of 97.8% and a specificity of 83.3% for predicting MPAP ≥25 mmHg, with an AUC of 0.96±0.02 (95% CI, 0.926–1.000).

Figure 5 Correlation analysis of right ventricular end-systolic remodeling index (RVESRI) with hemodynamics. (A) RVESRI positively correlated with right atrial pressure (RAP) (r=0.64, P<0.001). (B) RVESRI positively correlated with mean pulmonary arterial pressure (MPAP) (r=0.65, P<0.001). (C) RVESRI positively correlated with pulmonary vascular resistance (PVR) (r=0.69, P<0.001). (D) RVESRI negatively correlated with cardiac output (CO) (r=−0.64, P<0.001).

Figure 6 Performance of right ventricular end-systolic remodeling index (RVESRI), right ventricular eccentricity index (RVEI), right ventricular myocardial mass index (RVMI), the diameter of the main pulmonary artery (MPA), and the ratio of the MPA and ascending aorta diameter (MPA/AAo) for the prediction of mean pulmonary artery pressure ≥25 mmHg as indicated by receiver operating characteristic curves.

Discussion

There are 3 main findings in the current study: (I) RVESRI measured by CMR has the advantage of simplicity and reproducibility without the need for the special post-processing software; (II) increased RVESRI closely correlates with other RV ventricular remodeling and dysfunctional metrics; (III) increased RVESRI correlates with elevated pulmonary arterial pressure and afterload, while RVESRI >1.35 has a sensitivity of 97.83% and specificity of 83.33% in predicting MPAP ≥25 mmHg.

CTEPH is a potentially curable PH disease and can be treated by pulmonary endarterectomy or pulmonary balloon angioplasty. CMR studies have emphasized the predictive value of RVEF and RV end-diastolic and end-systolic volumes (10-12). The anatomical complexity of the right ventricle made the measurement of RVEF on CMR more time-consuming and complicated than the left ventricle. Amsallem et al. (5) proposed that RVESRI has the advantage of scaling using the same dimension and being less influenced by obesity. Since 4-chamber cine images on CMR can clearly demonstrate the temporal changes of the ventricular walls and chambers, our results indicated that the measurement of RVESRI on CMR is simple and reproducible.

More and more studies (13-15) have applied CMR in the evaluation of PH and have identified a range of valuable metrics, among which RVEF is an important prognostic factor for PH. In patients with CTEPH, RVESRI correlated with RVEDVI, RVESVI, and RVEF, indicating that RVESRI is the functional marker of RV systolic performance. In pediatric PAH, RVESRI is a useful marker in assessing right ventricular remodeling and dilation (16). With the elevation of right ventricular afterload, ventricular adaptive remodeling gradually progresses to maladaptive remodeling, which manifests as right ventricular wall hypertrophy and dilation. Progressive right ventricular remodeling in PAH is associated with a parallel decline in transversal and longitudinal shortening until a floor effect is reached for longitudinal shortening. Subsequently, the further reduction of right ventricular function is due to progressive leftward septal displacement and the increased RVESRI. Thus, ventricular strain can identify regional and global dysfunction. Some studies (17-19) showed that RVGLS was a remodeling marker and one of the strongest predictors of outcome in PH, and RVGLS, including right ventricular free wall and interventricular septum, showed a better correlation with RVEF by CMR. Recently, the utility of three-dimensional right ventricular strain was reported to be more accurate than two-dimensional strain in CTEPH (20). However, measurement depends on special post-processing software. In the current study, RVGLS was reduced in patients with CTEPH, and RVESRI was correlated with RVGLS and RVEF.

Moreover, CMR-derived RVEI (9) appears to have useful diagnostic and prognostic value in PAH, and provides incremental value to the risk stratification strategy. There was a significant negative correlation between RVESRI and RVEI. Moreover, the AUCs of RVESRI and RVEI in predicting mPAP ≥25 mmHg were comparable. These findings indicate that RVESRI on CMR is a remodeling marker like RVEI, which is easy to measure, and could provide a prognostic assessment of patients with CTEPH.

In terms of circulating blood biomarkers, BNP and NT-proBNP have been predictive of PH patients’ outcomes (21,22). Clinical studies of PAH have used the change in 6MWD as a clinical end point (23). RVESRI was positively associated with NT-proBNP and negatively associated with 6MWD, which indicated that it could be a prognostic marker. RHC is considered the gold standard for the diagnosis of PH and the assessment of hemodynamic severity. However, frequent or serial invasive testing is not practical. RVESRI correlated with RAP, PAP, PVR, and CO measured with RHC. Dilatation of the MPA is a common characteristic of PAH, and the identification of PA dilation on CT or MR of the chest performed to assess patients with nonspecific cardiorespiratory symptoms may raise the possibility of PH (24-27). Thus, we compared RVESRI, MPA, and MPA/AAo ratio in predicting PH, and the ROC curve indicated that RVESRI >1.35 had a higher sensitivity, specificity, and AUC value in identifying mPAP ≥25 mmHg compared to MPA and MPA/AAo ratio. However, in total patients and CTEPH patients, RVESRI moderately (r=0.65) and weakly (r=0.33) correlated with MPAP respectively, indicating that even though RVESRI might be a good parameter for predicting increased MPAP, it does not necessarily have to be accurate in estimating the MPAP value. Based on the present observations, RVESRI can be used to identify CTEPH patients from CTE patients and assess RV afterload (e.g., pulmonary pressure, PVR), stress (e.g., strain, NT-proBNP), and functional adaptation (e.g., RVEF, RVESVI) for patients with CTEPH.

Limitations

It should be noted that there are several limitations in our current study. As a retrospective study, we included patients with confirmed CTEPH and CTE. However, most patients were excluded because they had no CMR or a longer time interval of CMR and RHC, and only a small number of patients at a single center were included. This led to the drastic difference in the hemodynamic parameters of the CTE vs. CTEPH groups which was the important limitation of this study. Therefore, future studies with larger numbers of patients are required to determine the actual utility of RVESRI for the evaluation of CTEPH. Predictors of perioperative mortality in patients with operable CTEPH are useful in planning treatment, and whether RVESRI is a prognostic parameter needs to be determined. Our study only included certain CTEPH patients, a subgroup of PH, and whether these findings can be extrapolated to other groups of PH patients such as those with PH due to lung diseases and/or hypoxia or PH due to left heart disease need further research in the future.

Conclusions

In our study, RVESRI can be easily and reproducibly assessed on cine images of CMR, which are acquired in virtually all patients undergoing CMR. Moreover, CMR-derived RVESRI may assist in evaluating CTEPH.

Acknowledgments

Funding: This work was supported by the National Natural Science Foundation of China (Grant No. 81871328), Beijing Nature Science Foundation (Grant No. 7182149), Youth Talents project of Chinese Academy of Medical Science (Grant No. 2018RC320013), and Beijing Science and Technology Commission Pharmaceutical and Technology Innovation Project (Grant No. Z181100001918034).

Footnote

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://dx.doi.org/10.21037/qims-21-385). 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. The study was approved by the ethics committee of China-Japan Friendship Hospital (IRB No.2017-24), and was performed following the latest version of the Declaration of Helsinki (as revised in 2013) for Medical Research involving human subjects. Informed consent was obtained from all patients.

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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