Assessment of right ventricular systolic function in patients with hypertrophic cardiomyopathy by layer-specific speckle tracking echocardiography

Introduction

Hypertrophic cardiomyopathy (HCM) is a common genetic disorder characterized by unexplained left ventricular (LV) hypertrophy in the absence of identifiable secondary causes (1,2). Advances in clinical and molecular genetic research, particularly in family pedigree screening and precise cardiac imaging, suggest that HCM is commonly a global disease with an incidence rate of 1/200 (3). The clinical presentation of HCM varies widely, ranging from asymptomatic cases to those complicated by progressive heart failure (HF), recurrent arrhythmias, or sudden cardiac death (SCD) (4). For decades, research efforts have refined risk stratification for HCM and identified key risk factors for SCD (1). However, as most risk factors had been primarily based on the LV, the clinical significance of right ventricular (RV) parameters in HCM remains incompletely understood (5,6). The RV is susceptible to elevated filling pressures transmitted by the hypertrophied LV. Previous research has demonstrated that impaired RV systolic function is significantly associated with worsening myocardial function in HCM patients and is correlated with poor LV systolic function (7,8).

Recent evidence demonstrates that increased RV wall thickness (RVWT) is associated with a higher incidence of arrhythmias and dyspnea (9,10). RV enlargement and dysfunction negatively affected the prognosis of HCM, being associated with nearly two-fold higher all-cause mortality during long-term follow-up (11). Cardiac magnetic resonance (CMR) has emerged as the gold standard for assessing RV function due to high accuracy and reproducibility (12). The CMR study of Mushtaq et al. demonstrated that HCM could also influence RV function. The RV stroke volume index is the strongest predictor of ventricular arrhythmia, HF, and adverse cardiac events, including death (13). However, the application of CMR might be limited in hemodynamically unstable patients or those with certain cardiac implantable electronic devices (14,15). Consequently, echocardiography remains an essential noninvasive method to assess cardiac function in these populations (16). Despite this, most HCM patients showed preserved RV function by conventional echocardiographic parameters, which often failed to identify early subclinical RV myocardial deformation (17). It should be noted that reduced RV myocardial strain could be detected prior to any observable decline in RV ejection fraction (RVEF) (18).

Two-dimensional speckle tracking echocardiography (2D-STE) is a relatively advanced technique for evaluating myocardial deformation and offers several benefits over conventional echocardiography, as it is less dependent on insonation angle and cardiac load while providing greater accuracy and reproducibility. There were some studies concerning 2D-STE parameters and RV function (19). Chang et al. demonstrated that patients with adverse cardiovascular events (ACEs) exhibited decreased tricuspid annular plane systolic excursion (TAPSE) and RV strains. It has been reported that RV function indexed by TAPSE or RV strains could predict future ACE and contribute to risk stratification in HCM patients (20). Thus, RV strain analysis serves as an effective method for assessing mechanical alterations in RV myocardium, with results comparable to those obtained by CMR (21). The RV wall consisted of three layers: the inner longitudinal myocardium, the middle circumferential myocardium, and the outer oblique myocardium. While previous studies treated the RV wall as a single entity in the assessment of RV function, neglecting the layer structures of RV wall. The layer-specific strain (LSS) developed on the basis of 2D-STE, allowed for quantitative assessment of altered myocardial mechanics across the endocardial, middle, and epicardial layers (22,23). In HCM patients, focal myocardial fibrosis and intramural coronary artery disease can lead to injury within specific myocardial layers (24). Therefore, the evaluation of subclinical alterations in myocardial mechanics across all three layers in HCM patients can be effectively performed using LSS.

For the first time, this study was conducted to assess RV function across the three myocardial layers using the 2D-STE and its derived LSS techniques in HCM patients with or without RV wall thickening, which focused on identifying early sensitive markers of RV dysfunction in HCM patients. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1593/rc).

Methods

Study population

From September 2021 to March 2024, a total of 102 HCM patients (HCMs) were enrolled in The People’s Hospital of Liaoning Province. The diagnostic of HCM was based on the criteria established by the American College of Cardiology/European Society of Cardiology, which require echocardiographic evidence of LV wall thickness (LVWT) at the end of diastole ≥15 or ≥13 mm in the presence of a confirmed HCM diagnosis in a first-degree relative, provided that no other cardiac or systemic diseases could explain the observed hypertrophy (25). The exclusion criteria were as follows: myocardial hypertrophy secondary to hypertension, aortic stenosis or other causes; severe arrhythmia; and a LV ejection fraction (LVEF) of less than 50%. In this study, the HCMs were divided into two groups according to RVWT. The HCMs with RV hypertrophy (RVH) were diagnosed as RVWT >5 mm. While the HCMs without RVH were diagnosed as RVWT ≤5 mm. Fifty healthy controls (HCs) were included with a similar age and sex distribution, who had no evidence or family history of HCM, hypertension, diabetes mellitus (DM), or any other disease. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of The People’s Hospital of Liaoning Province [No. (2023) K020] and informed consent was taken from all the patients.

Methods and instruments

General information

The general clinical data were collected, including age, sex, body mass index (BMI), smoker, drinker, hypertension, DM, hyperlipidemia, and β-blockers. A standardized questionnaire was administered to each subject to document symptoms and history, including chest pain, syncope, New York Heart Association (NYHA) grade, sudden family history of death and arrhythmia.

Echocardiographic parameters

All individuals were in sinus rhythm at the time of echocardiographic examination. Echocardiographic cine loops were acquired, measured, and analyzed by two experienced ultrasonographers using GE Vivid E9 color Doppler ultrasound system (GE Vingmed, Horten, Norway). This involved a phased array probe with a frequency range of 2.0–4.0 MHz, a scanning depth of 15–18 cm, a frame rate exceeding 50 frames/s, and with simultaneous electrocardiogram monitoring.

The conventional echocardiographic parameters included LVWT measured from the parasternal long and axis views. Linear measurement of RVWT (either by M-mode or 2DE) was performed at end-diastole, below the tricuspid annulus at a distance approximating the length of the anterior tricuspid leaflet, when it is fully open and parallel to the RV free wall. Trabeculae, papillary muscles, and epicardial fat should be excluded. Zoomed imaging with focus on the RV mid-wall and respiratory maneuvers may improve endocardial border definition (19). Early diastolic mitral flow velocity (E) was measured by pulse doppler from the apical four-chamber view, and TAPSE was measured by M-mode ultrasound from the apical four-chamber view. The LV end-diastolic volume (LVEDV), LV end-systolic volume (LVESV), and LVEF were measured by the Simpson method. The RV fractional area change (RVFAC) was calculated as the difference between end-diastolic and end-systolic RV area divided by the end-diastolic RV area.

Tissue Doppler imaging (TDI) was used to measure the early diastolic velocity of mitral annular septal and lateral wall (E'). The average E' and the E/E' were calculated. Additionally, measurements were taken for the RV isovolumic contraction time (ICT), isovolumic relaxation time (IRT), and RV ejection time (ET). The RV Tei index was calculated using the formula, Tei index = (ICT + IRT)/ET. The systolic velocity of the tricuspid annulus (RV S') was obtained in the view that achieved parallel alignment of the Doppler beam with the RV free wall.

In 2D-STE, conventional cine loops of apical four-, three-, and two-chamber views, as well as cine loops of the apical four-chamber view for RV strain analysis, were captured and stored for five cardiac cycles in each subject at the end of expiration. The data were subsequently analyzed offline using EchoPAC software (EchoPAC version 113.0, GE Vingmed). STE is an angle-independent technique that enables evaluation of RV systolic function by tracking the displacement of speckles in the myocardium frame-by-frame. After drawing the outline of both endocardial and epicardial boundaries at the end of the T-wave, a region of interest (ROI) representing the LV and RV wall was obtained. The ROI was automatically divided into three myocardial layers and six segments by the software. Then, longitudinal strain (LS) curves were then generated for each myocardial layer. General parameters were obtained, including LV global LS (LVGLS), RVGLS, and LS of the RV free wall strain (RVFWS). RVGLS was calculated by averaging local strains along the entire right ventricle. The LSS parameters of RV were also obtained, including endocardial, mid-myocardial, and epicardial RVGLS and RVFWS (RVGLSendo, RVGLSmid, RVGLSepi, RVFWSendo, RVFWSmid, and RVFWSepi).

Statistical analysis

Data were analyzed by SPSS Statistics V26.0 (IBM Corp., Armonk, USA). Categorical variables were expressed as frequency and percentage [n (%)]. Continuous variables that followed a normal distribution were expressed as mean ± standard deviation (SD), while non-normally distributed data were expressed as medians and ranges. Between-group differences among the three groups were compared using one-way analysis of variance (ANOVA), followed by least significant difference (LSD) post-hoc test, and the Kruskal-Wallis test as appropriate. Categorical variables were compared using the Chi-squared (χ²) test or Fisher’s exact test. Pearson and Spearman correlation analyses were conducted to assess the correlations between RV parameters and conventional echocardiographic parameters or clinical factors. To identify significant independent correlations while excluding confounding factors such as age, gender, and hypertension, variables with P values less than 0.05 from the univariate analysis were included in the multivariate model. A P value less than 0.05 was considered statistically significant.

Results

Demographic and clinical characteristics among the three groups

This study enrolled 102 HCMs and 50 HCs, of which 57 HCMs with RVH and 45 HCMs without RVH. There were no significant differences in age, sex, BMI, smokers, drinkers, and DM among the three groups (all P>0.05). The HCMs with or without RVH had more proportion of hypertension, DM, dyslipidemia, and β-blockers, in comparison with the HCs (all P<0.05). Moreover, there were more individuals experiencing chest pain, fainting, sudden family death, and arrhythmia than the HCs (all P<0.05). The NYHA grade was higher in the HCMs with or without RVH compared to that in the HCs (all P<0.05) (Table 1).

LV echocardiographic parameters among the three groups

There were significant differences of LV mass index (LVMI), LVEDV index (LVEDVi), LVESV index (LVESVi), septal E', lateral E', mean E', E/E', and LVGLS among the three groups (all P<0.05). The HCMs with or without RVH exhibited significantly higher LVMI, LVEDVi, LVESVi, and E/E', and significantly lower septal E', lateral E', mean E', and absolute values of LVGLS, compared to the HCs (all P<0.05). Moreover, the HCMs with RVH showed significantly lower absolute values of LVGLS than the HCMs without RVH (P<0.05) (Table 2).

RV echocardiographic parameters among the three groups

Significant differences in RVWT, Tei index, TAPSE, RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, and RVFWSepi were found among the three groups (all P<0.05). Compared with HCs, HCMs with or without RVH demonstrated a significantly higher Tei index, and significantly lower TAPSE, as well as lower absolute values of RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, and RVFWSepi (all P<0.05) (Figure 1). Furthermore, the HCMs with RVH had significantly lower TAPSE, absolute values of RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, and RVFWSepi than the HCMs without RVH (all P<0.05) (Figure 2, Table 3).

Figure 1 RV LSS among the HCs, HCMs with RVH, and HCMs without RVH. (A) LSS in the HCs; (B) LSS in the HCMs without RVH; (C) LSS in the HCMs with RVH. AVC, aortic valve closure; endo, endocardial; epi, epicardial; GS, global strain; HC, healthy control; HCM, hypertrophic cardiomyopathy; LSS, layer-specific strain; RV, right ventricular; RVH, right ventricular hypertrophy.

Figure 2 RV layer-specific RVGLS and RVFWS among the HCs, HCMs with RVH, and HCMs without RVH. (A) RV layer-specific RVGLS among the HCs, HCMs with RVH, and HCMs without RVH; (B) RV layer-specific RVFWS among the HCs, HCMs with RVH, and HCMs without RVH. The plots represented the distributions of RV strains in each group and solid lines indicated means. *, P<0.05; **, P<0.01; ***, P<0.001. HC, healthy control; HCM, hypertrophic cardiomyopathy; RV, right ventricular; RVFWS, right ventricular free wall strain; RVGLS, right ventricular global longitudinal strain; RVH, right ventricular hypertrophy.

Correlations between RV dysfunction and echocardiographic factors in the HCMs

We evaluated the echocardiographic factors associated with RV dysfunction, as measured by TAPSE, RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, and RVFWSepi in the HCMs. The results showed negative correlations between LVESVi and RVGLS, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, and RVFWSepi (all P<0.05). Positive correlations were observed between LVGLS and TAPSE, RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, and RVFWSepi (all P<0.05). Additionally, RVWT showed positive correlations with parameters of RV dysfunction (all P<0.05) (Table 4).

Correlations between RV dysfunction and clinical factors in the HCMs

We further evaluated the clinical factors associated with the RV dysfunction, measured by TAPSE, RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, and RVFWSepi in the HCMs. The results demonstrated positive correlations between Chest pain or NYHA grade, and RVGLS, RVGLSendo, RVGLSmid, and RVGLSepi, as well as positive correlations between arrhythmia, and RVGLS, RVGLSendo, RVGLSmid, RVGLSepi, RVFWS, RVFWSendo, RVFWSmid, or RVFWSepi (all P<0.05) (Table 5).

Discussion

This study contributes to the limited data utilizing RV LSS analysis to comprehensively evaluate the RV systolic function in HCM patients with RVH, HCM patients without RVH, and HCs. Our study revealed several key findings: (I) significant differences in RVGLS and RVFWS were observed across all three myocardial layers among the groups; (II) RV systolic function was most impaired in HCM patients with RVH, followed by HCM patients without RVH; and (III) several echocardiographic and clinical factors were associated with RV dysfunction, including LVESVi, LVGLS, RVWT, chest pain, NYHA grade, and arrhythmia.

HCM primarily affects the LV, particularly the interventricular septum, resulting in characteristic asymmetric LV hypertrophy (26). LV wall involvement is common, and in some cases, the RV wall may also be affected (10). Typically, the LVEF remains normal in HCM patients, with fewer than 15% showing reduced LVEF until later stages of life (27). In fact, impairment of RV function often precedes the decline in LVEF (28). The histopathological changes in the hypertrophic myocardium of LV and RV are similar in HCM patients. The hypertrophy of RV wall can lead to increased stiffness and reduced compliance, resulting in RV systolic dysfunction (29). Doesch et al. reported that the presence of RV systolic dysfunction in HCM patients increases the risk of HF-related mortality by 1.6-fold (30).

RV involvement in HCM patients encompasses both structural and functional alterations of the RV. According to the 2015 American Society of Echocardiography (ASE)/European Association of Cardiovascular Imaging (EACVI) recommendations, RVH was defined as a RVWT greater than 5 mm at end-diastole (31). McKenna et al. classified RVH based on wall thickness into mild (5–8 mm), moderate (9–12 mm) and severe (>12 mm) hypertrophy (9). The risk of cardiovascular mortality over a decade is elevated in HCM patients with moderate to severe RVH (10). Nagata et al. indicated that HCM patients with RVH on CMR images have a greater incidence of cardiovascular events than non-RVH patients (32). Long-term RV systolic dysfunction can lead to increased RV filling pressures and RV enlargement, which are closely associated with reduced exercise capacity and elevated risk of pulmonary embolism in HCM patients (30). While accurate assessment of RV function is of great clinical value, it has historically posed challenges. Unlike the LV with regular morphology, the RV possesses a complex structure comprising inflow tract, trabeculated apical portion, and outflow tract, making EF less suitable for evaluating the RV systolic function.

In this study, the RV function of HCM patients was assessed using 2D-STE and LSS, including RVGLS, RVFWS, and their strains of the endocardial, mid-myocardial, and epicardial layers. The findings indicated that the RV systolic function of HCM patients was reduced to varying extents, particularly in those with RVH. Significant differences in RVGLS and RVFWS were observed across all three myocardial layers among HCM patients. This can be attributed to the crucial role of the interventricular septum in the performance of both RV and LV (33). Normal septal function is essential for optimal electromechanical coupling, systolic function, and diastolic function of both ventricles (34). The shared septum resulted in ventricular interdependence. Furthermore, the RV is composed of longitudinal and oblique helical myocardial fibers responsible for longitudinal shortening and lengthening, which account for over 80% of RV systolic ejection (33). Roşca et al. also assessed the parameters of RV function in HCM patients through echocardiographic strains and found a correlation between impaired RV function and increased RVWT in these patients (10). In addition, Maron et al. demonstrated that RV dysfunction in HCM patients with or without RVH associated with LVGLS (26), which aligned with our findings. Although previous studies have investigated RV systolic ejection, there is still limited information available regarding the use of LSS to assess RV systolic function in HCM patients. Our findings suggest that impaired RV LSS may primarily affect RV longitudinal systolic function (35).

The clinical course of HCM is characterized by extreme heterogeneity, with unpredictable development of HF and arrhythmia, and with sudden death as the most feared complication (10). In this study, there were negative correlations between chest pain or NYHA grade, and RVGLS, RVGLSmid, or RVGLSepi, and negative correlations between arrhythmia, and RVFWS, RVFWSmid, or RVFWSepi, which supported previous reports, suggesting that the measures for assessing RV systolic dysfunction, such as RVGLS, RVGLSmid, RVGLSepi, RVFWS, RVFWSmid, and RVFWSepi, could serve as indicators of increased risk for chest pain, NYHA grade, and arrhythmias (7), ultimately aiding in better risk stratification for HCM patients.

There were several limitations in this study. First, this study was conducted at a single center, because HCM is not a very common disease, the study sample size was relatively small, particularly for several clinical factors, that cause positive P values for Pearson correlation effect sizes are very small, meanwhile, it is also quite suitable for LSD. Second, the study duration was brief without follow-up. There were no prognostic parameters. Further studies on the prognostic significance of RV function were necessary. Third, the study lacked animal or molecular experiments, which should be addressed in future research.

Conclusions

In summary, for the first time, our study revealed that the RV systolic function decreased significantly in HCM patients with or without RVH, characterized by decreased RVGLS and RVFWS for all three myocardial layers, especially the endocardial layer. The decrease was the most significant in the HCM patients with RVH. Layer-specific strains of RVGLS and RVFWS may be associated with increased risk for chest pain, NYHA grade, and arrhythmias.

Acknowledgments

The authors thanked all the participants for their cooperation and are grateful for the support of Department of Ultrasound, The People’s Hospital of Liaoning Province.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1593/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1593/dss

Funding: This work was supported by the National Natural Science Foundation of China (No. 82371982 to D.S.) and the Xingliao Talents Program of Liaoning Province (No. XLYC2412072 to D.S.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1593/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. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of The People’s Hospital of Liaoning Province [No. (2023) K020] and informed consent was taken from all the 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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