Early detection of right atrial dysfunction in patients with hypertrophic cardiomyopathy using cardiac magnetic resonance feature tracking

Introduction

Hypertrophic cardiomyopathy (HCM) is a common type of inherited primary cardiomyopathy with an estimated prevalence of 1:200–1:500 (1). Although a considerable number of patients with HCM exhibit a benign clinical trajectory and remain asymptomatic (2), sudden cardiac death can occur as the first manifestation of HCM in asymptomatic patients, particularly in young students and athletes (3,4). HCM is distinctly characterized by features such as disorganized myocyte structure, crypt-like invaginations, asymmetric left ventricular (LV) wall thickening, myocardial fibrosis, and mitral valve distortion (5). These abnormalities may reduce LV compliance and increase LV end-diastolic pressure (6), ultimately resulting in atrial dilation and dysfunction through ventricular-atrial coupling. However, previous studies in patients with HCM have primarily focused on biventricular and left atrial (LA) morphology and function (7-10), with the right atrium (RA) garnering limited attention.

This is a particularly noticeable oversight given that RA is being increasingly recognized as more than a passive filling chamber, and it has been discovered that it plays a pivotal role in modulating ventricular filling through three phasic functions (11): (I) reservoir function, which reserves blood from the systemic venous during ventricular systole and atrial diastole; (II) conduit function, which serves as a pathway for passive blood flow into the ventricle during early ventricular diastole; (III) booster pump function, which actively propels blood into the right ventricle (RV) in late ventricular diastole. Despite the physiological importance of the RA, the prevalence of RA enlargement (RAE) and its implications for RA function in patients with HCM have not been sufficiently investigated.

Cardiac magnetic resonance (CMR) is recognized as the reference standard for assessing cardiac structure and function (12). CMR feature tracking (CMR-FT), a novel, noninvasive method, evaluates myocardial mechanics through the postprocessing of standard CMR cine images, thereby obviating the need for specialized acquisition sequences (13). This technique can identify abnormal myocardial motion by tracking changes in deformation parameters, such as myocardial strain, strain rate (SR), torsion, and desynchrony (3,12), which are considered more sensitive indicators of cardiac function than ejection fraction. At present, deformation parameters have demonstrated value in the diagnosis and prognostic prediction of various cardiovascular conditions, such as hypertension, ischemic and nonischemic cardiomyopathy, heart failure, and pulmonary hypertension (12,14-16). However, there remains a lack of studies on the application of CMR-FT for early RA dysfunction in patients with HCM.

Therefore, this study aimed to investigate whether early RA dysfunction in patients with HCM, both with and without RAE, could be detected by CMR-FT. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2871/rc).

Methods

Study population

This study was approved by the ethics committee of The First Affiliated Hospital of Zhejiang Chinese Medical University (No. 2022-KLS-207-01) and the ethics committee waived the requirement for participant consent due to its retrospective nature. All participating institutions were informed and agreed to the study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. From June 2023 to July 2024, a total of 155 consecutive patients with HCM who underwent CMR examinations at The First Affiliated Hospital of Zhejiang Chinese Medical University, The Second Affiliated Hospital of Zhejiang University School of Medicine, and Chinese Medical Hospital of Yiwu were included. HCM was defined as LV wall thickness on CMR images ≥15 mm, or ≥13 mm in patients with a known family history of HCM (17,18). The exclusion criteria were as follows: (I) history of coronary artery disease, myocardial infarction, or myocarditis; (II) history of septal myectomy or alcoholic septal ablation; (III) myocardial hypertrophy due to other causes such as hypertensive cardiomyopathy, cardiac amyloidosis, valvular disease, and Fabry disease; and (IV) quality of image hindering the assessment of RA deformation parameters. Ultimately, a total of 143 patients with HCM were included and further divided into two groups: the RAE group (n=25) and the non-RAE group (n=118) (Figure 1). RAE was defined as an RA maximum volume index (RAVmaxi) >53.1 mL/m² for men or >48.8 mL/m² for women (19). Additionally, 70 age- and gender-matched healthy individuals without hypertension, diabetes, or overt cardiovascular disease were included as the healthy control group.

Figure 1 The flow chart of the current study. HCM, hypertrophic cardiomyopathy; RAE, right atrial enlargement.

Image acquisition

All CMR scans were performed on 1.5-T MR scanners (Signa HD Excite, GE HealthCare, Chicago, IL, USA; MAGNETOM Avanto, Siemens Healthineers, Erlangen, Germany) or 3.0-T MR scanners (Discovery MR750 and Signa Premier, GE HealthCare) with a phased-array surface coil at three centers. Short-axis cine images covering the entire LV and RV from the base to the apex were acquired with a retrospective electrocardiogram-gated and balanced steady-state free precession sequence. Three long-axis slices (two-, three-, and four-chamber views) were also acquired. The respective imaging parameters for the Discovery MR750, Signa Premier, Signa HD Excite, and MAGNETOM Avanto scanners were as follows: repetition time (TR) =3.2 ms, echo time (TE) =1.4 ms, field of view (FOV) =340×340 mm², slice thickness =8 mm, and phases per cardiac cycle =20–30; TR=2.9 ms, TE =1.1 ms, FOV =340×340 mm², slice thickness =8 mm, and phases per cardiac cycle =30; TR=3.5 ms, TE =1.5 ms, FOV =360×360 mm², slice thickness =8 mm, and phases per cardiac cycle =20–25; and TR=2.6 ms, TE =1.1 ms, FOV =340×276 mm², slice thickness =8 mm, and phases per cardiac cycle =25.

Image analysis

Image analysis was performed on cine images using dedicated software (cvi42 version 5.14.2; Circle Cardiovascular Imaging, Calgary, AB, Canada) by an experienced researcher [W.L., with >5 years of experience in cardiac MR imaging (MRI)] who was blinded to clinical information. LV and RV function and volumes, including the biventricular end-diastolic volume index (EDVi), end-systolic volume index (ESVi), stroke volume index (SVi), ejection fraction (EF), and cardiac index (CI), along with LV mass, were quantified from short-axis cine images. Biventricular strain parameters, including LV and RV global radial, circumferential, and longitudinal strain, were obtained on short-axis and long-axis cine images using CMR-FT (17). RA volumes and function were quantified from a four-chamber view according to the single area-length method (20). The RAVmaxi, RA pre-atrial contraction volume index (RAVpaci), and RA minimum volume index (RAVmini) were assessed at RV systole, RV diastole before RA contraction, and late RV diastole after RA contraction, respectively (21). Total RA emptying fraction (RAEF total; corresponding to RA reservoir function), passive RAEF (corresponding to RA conduit function), and active RAEF (RAEF booster; corresponding to RA contractile booster pump function) were calculated according to the following equations (22):

RAEFtotal=(RAVmaxi−RAVmini)RAVmaxi×100[1]

RAEFpassive=(RAVmaxi− RAVpaci)RAVmaxi×100[2]

RAEFbooster=(RAVpaci− RAVmini)RAVpaci×100[3]

RA feature tracking

RA feature tracking strain analysis was performed using dedicated software (cvi42 version 5.14.2) by an experienced researcher (W.L., with >5 years of experience in cardiac MRI) who was blinded to the clinical information. RA endocardial and epicardial borders were automatically traced and manually adjusted if the atrial wall was not properly followed, with LV end-diastole serving as the phase of reference in the four-chamber view (15). The superior vena cava and RA appendage were excluded from RA endocardial contours (15). Subsequently, RA strain and strain rate (SR) parameters were analyzed according to strain-time and SR-time curves (20): reservoir strain (εs), conduit strain (εe), booster strain (εa), and the corresponding SR, including the peak positive SR (SRs), the peak early negative SR (SRe), and the peak late negative SR (SRa).

Reproducibility

To evaluate the interobserver reproducibility of the RA deformation parameters, 20 cases (20 patients with HCM) were randomly selected and analyzed by two independent observers (W.L. and Y.G., with >5 years of experience in cardiac MRI). For intraobserver reproducibility, the same 20 patients were analyzed by the first author (W.L.) for a second time with a time interval of >1 month.

Statistical analysis

Continuous variables with a normal distribution are expressed as the mean ± standard deviation (SD), while nonnormally distributed variables are presented as the median and interquartile range. Meanwhile, categorical variables are expressed as frequencies and percentages. Comparisons between two groups were performed with the Student’s t-test, Mann-Whitney test, or Chi-square test as appropriate. Comparisons between three groups were conducted using one-way analysis of variance (ANOVA) with post-hoc least significant difference tests or Chi-square test as appropriate. The associations of right ventricular ejection fraction (RVEF) and RAEF with RA strain parameters were evaluated using Pearson correlation analysis, and a correlation coefficient (r) was obtained. Correlation strength was defined as weak for |r| values between 0.20 and 0.39, moderate for those between 0.40 and 0.59, and strong for those ≥0.60 (23). Intra- and interobserver reproducibility analysis was performed using intraclass correlation coefficients (ICCs) and Bland-Altman plots. An ICC >0.75 was considered to indicate excellent reproducibility, 0.40–0.75 good, and <0.40 poor (24). All statistical analyses were conducted via SPSS version 29.0.1.0 (IBM Corp., Armonk, NY, USA) and GraphPad Prism version 10.2.3 (GraphPad Software, Insight Partners, New York, NY, USA). A P value <0.05 was considered to indicate statistical significance.

Results

Baseline characteristics

The baseline characteristics of the study population are summarized in Table 1. Among the 143 patients with HCM, 25 (17.5%) patients exhibited RA dilation. There was no significant difference in age, gender, diastolic blood pressure, or fasting blood glucose between the healthy control group, the HCM non-RAE group, and the HCM RAE group (all P values >0.05). Compared with the control group, both HCM groups (RAE and non-RAE) had significantly higher systolic blood pressure (both P values <0.05). Additionally, the HCM non-RAE group had a significantly higher body mass index, body surface area, diastolic blood pressure, and heart rate than did the control group (all P values <0.05). A total of 13 patients with HCM had atrial fibrillation, with 11 in the HCM non-RAE group and 2 in the HCM RAE group. There was no statistically significant difference in atrial fibrillation incidence between the two HCM groups (P value =0.835).

Biventricular conventional parameters

The comparative analysis of biventricular structure and function parameters is shown in Table 2. Significant differences in all biventricular conventional parameters were found between the healthy control group, the HCM non-RAE group, and the HCM RAE group (all P values <0.05). Both the HCM groups (RAE and non-RAE) demonstrated significantly higher LV end-diastolic volume index (LVEDVi), LV end-systolic volume index (LVESVi), LV stroke volume index (LVSVi), LV cardiac index (LVCI), and LV mass values, along with lower LVEF, RVEF, and biventricular strain when compared to the control group (all P values <0.05); however, no significant differences were observed between the two HCM groups (all P values >0.05). Moreover, compared with the HCM non-RAE group, the HCM RAE group exhibited significantly higher RV end-diastolic volume index (RVEDVi), RV end-systolic volume index (RVESVi), RV stroke volume index (RVSVi), and RV cardiac index (RVCI) values (all P values <0.05).

RA volumetric and deformation parameters

The comparisons of RA volumetric and deformation parameters between the three groups are shown in Table 3 and Figure 2. The HCM RAE group had significantly greater RAVmaxi, RAVpaci, and RAVmini values than did both the healthy control group and the HCM non-RAE group (all P values <0.05), while there were no significant differences between the healthy control group and the HCM non-RAE group (all P values >0.05). As for RAEF, both the HCM RAE and non-RAE groups exhibited significantly lower RAEF booster values as compared to the healthy control group (both P values <0.05), while there was no difference in the RAEF total or RAEF passive between the three groups (all P values >0.05).

Figure 2 Comparisons of RA deformation parameters between healthy controls, the HCM non-RAE group, and the HCM RAE group. *, P<0.05 compared to healthy controls. εa, booster strain; εe, conduit strain; εs, reservoir strain; HCM, hypertrophic cardiomyopathy; RA, right atrial; RAE, right atrial enlargement; SRa, peak late negative strain rate; SRe, peak early negative strain rate; SRs, peak positive strain rate.

RA deformation parameters, including RA εs, εe, εa, SRs, SRe, and SRa, were significantly reduced in both the HCM groups (RAE and non-RAE) as compared to the healthy control group (all P values <0.05). There was no difference in any RA strain parameters between the HCM RAE group and the HCM non-RAE group (all P values >0.05). Examples of RA strain and SR measurements in the healthy control group and both HCM groups are presented in Figure 3.

Figure 3 Representative cases of RA strain and strain rate between healthy controls (A-C), the HCM non-RAE group (D-F), and the HCM RAE group (G-I), respectively. RA endocardial (red) and epicardial (green) borders were automatically traced with left ventricle end-diastole serving as the phase of reference in the four-chamber view. The length and direction of the lines represent the magnitude and orientation of myocardial deformation throughout the cardiac cycle. εa, booster strain; εe, conduit strain; εs, reservoir strain; HCM, hypertrophic cardiomyopathy; RA, right atrial; RAE, right atrial enlargement; SRa, peak late negative strain rate; SRe, peak early negative strain rate; SRs, peak positive strain rate.

Association of RVEF and RAEF with RA deformation parameters

The correlation between RVEF, RAEF, and RA deformation parameters in patients with HCM is outlined in Table 4. Simple linear regression analysis revealed weak-to-moderate correlations between RVEF and RA deformation parameters (εs and RVEF: r=0.56, P<0.001; εe and RVEF: r=0.48, P<0.001; εa and RVEF: r=0.42, P<0.001; SRs and RVEF: r=0.42, P<0.001; SRe and RVEF: r=−0.39, P<0.001; SRa and RVEF: r=−0.40, P<0.001) (Figure 4). Additionally, RA deformation parameters were moderately to strongly correlated with RAEFs for RA reservoir, conduit, and booster pump function in all patients with HCM (εs and RAEF total: r=0.60, P<0.001; εe and RAEF passive: r=0.67, P<0.001; εa and RAEF booster: r=0.62, P<0.001; SRs and RAEF total: r=0.56, P<0.001; SRe and RAEF passive: r=−0.57, P<0.001; SRa and RAEF booster: r=−0.52, P<0.001).

Figure 4 Association of RVEF with RA εs (A), εe (B), and εa (C) in hypertrophic cardiomyopathy patients. The blue line represents the linear regressions and the red line represents 95% confidence intervals. εa, booster strain; εe, conduit strain; εs, reservoir strain; RA, right atrial; RVEF, right ventricular ejection fraction.

Interobserver and intraobserver variability

Interobserver and intraobserver reproducibility analysis for all the RA deformation parameters are presented in Table 5 and Figures S1,S2. The reproducibility indices of RA deformation parameters were excellent, with all ICCs >0.75 and narrow limits of agreement in the Bland-Altman plots.

Discussion

In this study, we used the CMR-FT technique to comprehensively assess RA phasic function in HCM patients with and without RAE. The principal findings of our study are as follows: (I) Compared with healthy controls, both the HCM groups (RAE and non-RAE) exhibited lower RA reservoir, conduit, and booster strain and SR, suggesting that RA function may be already impaired even in the presence of normal RA volumes in patients with HCM. (II) The RA deformation parameters were significantly lower in all patients with HCM (both RAE and non-RAE) as compared to the healthy control group, while RAEF total and RAEF passive were similar, which indicates that RA strain and SR derived from CMR-FT may be more sensitive indicators of early RA dysfunction in patients with HCM than RAEF. (III) The RA deformation parameters were closely associated with RVEF and RAEF metrics in this population.

RA dysfunction before RA enlargement

Although LA enlargement has been established as a sensitive indicator for filling pressures and poor prognosis (25,26), there is a paucity of research on the prevalence and clinical significance of RAE in HCM. A previous CMR-FT study by Mazurkiewicz et al. (6), which included 55 children with HCM and 20 healthy controls, found that both RA minimal volume and volume immediately before contraction were significantly greater in children with HCM than in the controls. However, the authors did not report on the prevalence of RAE in the pediatric HCM population. In our study, we observed that 17.5% of patients with HCM exhibited RAE, which was consistent with an echocardiography study conducted by Limongelli et al. (27). To our knowledge, our work is the first of its kind to examine the prevalence of RAE in patients with HCM using CMR, and the findings may offer in-depth insight into the pathophysiology of HCM.

Several studies have reported on the impairment of RA function in patients with HCM; however, their findings have been relatively inconsistent (6,28-30). Specifically, several CMR-FT and speckle tracking echocardiography (STE) studies observed lower RA reservoir strain and conduit strain, but comparable RA booster strain, in patients with HCM as compared to healthy controls (28,29). In contrast, a comparative study found no significant differences in RA reservoir, conduit, or booster strain between patients with HCM and controls (30). In our study, we found that patients with HCM and RAE exhibited impaired RA reservoir and conduit and booster function as evidenced by declines in RA εs, εe, εa, SRs, SRe, and SRa values. This observation was consistent with a previous CMR-FT study conducted on children with HCM (6). We speculate that the discrepancies between studies may be attributed to variations in sample size, disease severity, and progression. Notably, our investigation revealed that patients with HCM with non-RAE also had lower RA deformation parameters compared to healthy controls, suggesting that RA function may be compromised even when normal RA volumes are present in patients with HCM.

RA strain was superior to RAEF in detecting early RA dysfunction

Myocardial strain has emerged as a sensitive indicator for detecting early, subtle alterations in cardiac function across various cardiovascular diseases. There is growing amount evidence suggesting that LV global longitudinal strain is significantly impaired in patients with heart failure with preserved EF (31,32). Moreover, a CMR-FT study reported that biventricular strain may serve as an early biomarker of HCM in individuals at risk (17). Recently, Zheng et al. identified RA strain as an independent indicator for adverse cardiac events in patients with arrhythmogenic RV cardiomyopathy, incremental to conventional predictors (33). In our study, we found that the RA deformation parameters were all significantly lower in both the RAE and non-RAE HCM groups as compared to the healthy group, while there were no differences observed in RAEF total or RAEF passive. These findings suggest that RA strain and SR may be more sensitive than RAEF in identifying early RA dysfunction in HCM. Furthermore, the RA deformation measurements from CMR-FT exhibited good intra- and interobserver reproducibility in patients with HCM, which was consistent with several previous studies (28,34). Overall, our findings underscore the potential of RA strain and SR derived from CMR-FT as sensitive markers for the early detection of RA dysfunction in patients with HCM.

Associations of RVEF and RAEF with RA deformation parameters

Several studies (7,9) have demonstrated that RV dysfunction is associated with adverse clinical outcomes in patients with HCM. Impaired RV function, including reduced RVEF and RV strain, has been linked to an increased risk of heart failure progression, arrhythmic events, and overall cardiovascular morbidity and mortality. In this study, we observed significant correlations between RVEF and RA deformation parameters, including RA εs, εe, εa, SRs, SRe, and SRa, in patients with HCM. This may be attributable to a number of mechanisms: (I) According to the Frank-Starling mechanism (35), LV systolic and diastolic dysfunction-particularly in the presence of asymmetric LV wall thickening-exacerbates RV overload. This overload impairs RV diastolic function and worsens functional tricuspid regurgitation, which in turn, contributes to RAE and RA dysfunction, ultimately leading to decreased cardiac output. (II) The performance of the right heart is contingent upon effective atrial-ventricular coupling (36). The mechanism involving the temporal coordination between the atrium and ventricle, which relies upon the delayed conduction properties of the atrioventricular node, ensures that the ventricles have sufficient time to fill with blood following atrial contraction. RA dysfunction and decreased compliance may reduce the efficiency of RV output by affecting ventricular filling and systolic contraction. Moreover, we found that RA deformation parameters were closely associated with RAEFs for atrial reservoir, conduit, and booster pump function, which was consistent with several previous studies (20,37).

Limitations

This study involved several limitations which should be addressed. First, we employed a retrospective design with a relatively limited sample size, which might have introduced potential selection bias. Second, the prevalence of RAE in patients with HCM was not high, resulting in an imbalanced distribution of sample sizes across the three groups. Third, we did not conduct direct comparisons with STE due to its unavailability at the time of the CMR examination. However, other research has identified a significant correlation between the atrial strain parameters measured by STE and those obtained through CMR-FT (38,39). Finally, due to the short duration of patient enrollment, which began in 2023, there were insufficient follow-up data; thus, the prognostic value of RA strain within this cohort should be investigated in future research.

Conclusions

Patients with HCM exhibited impaired RA reservoir, conduit, and booster pump function even with normal RA volumes. CMR-FT-derived RA strain and SR may serve as more sensitive indicators of early RA functional impairment compared to traditional RAEF metrics. These findings suggest the potential of CMR-FT to enhance the evaluation of RA myocardial mechanics, providing valuable insights into the early alterations in RA phasic function in patients with HCM. However, further validation is needed to fully understand its clinical utility.

Acknowledgments

Preliminary results of this work were presented at the Chinese Congress of Radiology in 2024 (Abstract #PO-3160).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2871/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2871/dss

Funding: This study received funding by the National Natural Science Foundation of China (No. 81971600, to M.X.), the “Pioneer” and “Leading Goose” R&D Program of Zhejiang (No. 2022C03046, to M.X.), and the Talent Cultivation Program for Outstanding Innovative Individuals at Zhejiang Chinese Medical University (No. 2024YJSBJ002, to Y.G.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2871/coif). Y.G. has received funding support from the Talent Cultivation Program for Outstanding Innovative Individuals at Zhejiang Chinese Medical University (No. 2024YJSBJ002). M.X. has received funding support by the National Natural Science Foundation of China (No. 81971600) and the “Pioneer” and “Leading Goose” R&D Program of Zhejiang (No. 2022C03046). 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. This study was approved by the ethics committee of The First Affiliated Hospital of Zhejiang Chinese Medical University (No. 2022-KLS-207-01) and the ethics committee waived the requirement for participant consent due to its retrospective nature. All participating institutions were informed and agreed to the study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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