How Does Right Atrial Function Differ? A Speckle‐Tracking Echocardiographic Comparison of Fetuses With Left Ventricular Outflow Tract Obstruction Versus Those With Significant Tricuspid Regurgitation

ABSTRACT

Purpose

To evaluate the feasibility of two‐dimensional speckle tracking echocardiography (2D‐STE) for quantitatively assessing right atrial global longitudinal strain (RAGLS) in normal fetuses, and to compare RAGLS among normal fetuses, fetuses with left ventricular outflow tract obstruction (LVOTO), and those with moderate‐to‐severe tricuspid regurgitation (TR).

Methods

A total of 32 fetuses with LVOTO, 25 with moderate‐to‐severe TR, and 100 normal fetuses were enrolled. RAGLS was compared among the three groups, and its correlations with gestational age (GA) and other echocardiographic parameters were analyzed. Inter‐ and intra‐observer repeatability was assessed using intraclass correlation coefficients (ICC) and Bland‐Altman analysis.

Results

RAGLS differed significantly among the three groups (p < 0.01). The RAGLS values in both the TR and LVOTO groups were significantly lower than those in the control group (both p < 0.01), whereas the LVOTO group exhibited significantly higher RAGLS compared to the TR group (p < 0.05). In the control group, RAGLS was negatively correlated with GA (r = −0.47, p < 0.01). However, in the TR or LVOTO groups, RAGLS showed no significant correlation with GA or other measured parameters (all p > 0.05). The inter‐ and intra‐observer repeatability of RAGLS measurements was good (ICC > 0.75).

Conclusion

The right atrial reservoir function is impaired in fetuses with TR and those with LVOTO. RAGLS may serve as a sensitive indicator for quantitatively evaluating RA dysfunction in fetal cardiac anomalies.

This study systematically compared the differences in right atrial global longitudinal strain (RAGLS) among normal fetuses, fetuses with left ventricular outflow tract obstruction (LVOTO), and fetuses with moderate‐to‐severe tricuspid regurgitation (TR) for the first time.

There was a more significant decrease in RAGLS within the moderate‐to‐severe TR group as compared with the LVOTO group.

Abbreviations

2D‐STE

two‐dimensional speckle tracking echocardiography

AO

systolic aortic annular diameter

AS

aortic stenosis

BPD

biparietal diameter

CoA

coarctation of the aortic arch

FHR

fetal heart rate

FL

femur length

GA

gestational age

HLHS

hypoplastic left heart syndrome

IAA

interruption of the aortic arch

ICC

intraclass correlation coefficients

LVOTO

left ventricular outflow tract obstruction

PA

systolic pulmonary annular diameter

PA/AO

pulmonary‐to‐aortic diameter ratio

RAESA

RA end‐systolic area

RAESD

RA end‐systolic transverse dimension

RAESL

RA end‐systolic longitudinal dimension

RAGLS

right atrial global longitudinal strain

RVEDD

right ventricular end‐diastolic transverse dimension

TAPSE

tricuspid annular plane systolic excursion

TR

tricuspid regurgitation

1. Introduction

Two‐dimensional speckle tracking echocardiography (2D‐STE) is an angle‐independent technique for evaluating myocardial mechanics [1, 2]. Specialized software is used to track the spatial movement of myocardial tissue by measuring its deformation. This method yields strain parameters that allow quantitative assessment of myocardial function. Currently, 2D‐STE is widely applied in studies of fetal ventricular function [3, 4, 5]. However, research on fetal atrial function, particularly right atrial function under pathological conditions, remains limited.

The unique shunting through the foramen ovale during fetal life and the dominant role of the right ventricle in cardiac output make the right atrium particularly important in fetal circulation. The right atrium undergoes three phases during the cardiac cycle: reservoir, conduit, and contraction phases. During the reservoir phase, atrial function reflects atrial compliance and ventricular diastolic function [6, 7, 8]. Studies on adult atrial function have indicated that atrial functional changes usually precede ventricular dysfunction [9]. Therefore, early detection of fetal atrial dysfunction is clinically important. This study focused on right atrial global longitudinal strain (RAGLS), which represents the reservoir function of the right atrium.

Tricuspid regurgitation(TR) is the most common cardiac valve regurgitation during fetal life. Isolated mild TR is often physiological and usually has no clinical implications, whereas moderate‐to‐severe TR is frequently associated with structural cardiac anomalies. The prognosis depends not only on the severity of regurgitation but also on associated cardiac abnormalities [10, 11]. Excessive right ventricular pressure or volume overload directly causes TR, which subsequently increases right atrial volume and pressure. This direct hemodynamic effect initiates a detrimental cycle.

Left ventricular outflow tract obstruction (LVOTO) is another significant category of fetal congenital heart anomalies. It includes isolated aortic stenosis (AS), coarctation of the aortic arch (CoA), interruption of the aortic arch (IAA), and hypoplastic left heart syndrome (HLHS) [12]. Traditionally, these conditions have been considered primarily left‐heart pathologies. Their effects on the right heart, particularly the functional changes in the right atrium, are often overlooked. In fetuses with LVOTO, increased left ventricular afterload may affect right ventricular size and pressure through the foramen ovale. These compensatory changes can trigger early structural and functional remodeling of the right atrium.

This study aims to investigate the feasibility of quantifying fetal RAGLS in the second to third trimester using 2D‐STE. To our knowledge, this is the first comparative analysis of RAGLS among normal fetuses, fetuses with LVOTO, and those with moderate‐to‐severe TR. Employing 2D‐STE, this study explored its utility and mechanistic basis for evaluating right atrial function in fetuses under diverse pathophysiological conditions.

2. Methods

2.1. Study Population

A retrospective study design was employed. Pregnant women who underwent fetal echocardiography at the Department of Ultrasound & Echocardiography, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China, were enrolled.

A total of 32 fetuses with LVOTO were identified by echocardiography, including 17 cases with CoA, 10 with IAA, 4 with HLHS, and 1 with isolated AS. Maternal age ranged from 21 to 38 years (mean 29.1 ± 4.8 years), and GA ranged from 19 to 37 weeks (mean 25.8 ± 4.5 weeks). Among these, 16 cases (50%) had concomitant ventricular septal defects.

Additionally, 25 cases of moderate‐to‐severe TR were identified by echocardiography. The etiologies varied, with right ventricular pressure overload being most common (20 cases). This included 18 cases of pulmonary artery stenosis or atresia and 2 cases with premature ductus arteriosus contraction. Other etiologies were 1 case of restricted foramen ovale with right ventricular volume overload, 3 cases of tricuspid valve disease (2 cases of Ebstein's anomaly and 1 case of tricuspid valve hypoplasia), and 1 case associated with a redundant foramen ovale flap. Maternal age ranged from 23 to 40 years (mean 30.1 ± 4.2 years), and GA ranged from 17 to 38 weeks (mean 27.2 ± 5.2 weeks).

The control group consisted of 100 singleton fetuses with normal echocardiography. Maternal age ranged from 20 to 40 years (mean 29.8 ± 3.9 years), and GA ranged from 20 to 39 weeks (mean 25.8 ± 3.9 weeks).

This study was approved by the hospital ethics committee. All enrolled pregnant women subsequently reviewed and provided written informed consent for the fetal echocardiography examination.

2.2. Inclusion Criteria and Exclusion Criteria

Inclusion criteria were as follows: singleton pregnancy, ultrasound‐estimated GA consistent with the last menstrual period (difference <2 weeks), absence of maternal cardiovascular disease, endocrine disorders, or other significant diseases, and echocardiographic images clearly showing the endocardial surface. Inclusion criteria for the LVOTO group were one or more of the following: (1) abnormal pulmonary‐to‐aortic diameter ratio (PA/AO >1.4); (2) thickened aortic valve with increased echogenicity and restricted opening, possibly accompanied by post‐stenotic ascending aorta dilatation and color Doppler showing accelerated or sparse blood flow at the aortic valve; (3) significantly narrowed ascending aorta or aortic arch (Figure 1), with color Doppler revealing indistinct or retrograde flow; (4) abnormal left‐to‐right ventricular size ratio with left ventricular hypoplasia. The inclusion criterion for the TR group was moderate‐to‐severe regurgitation. Qualitative criteria typically involve detecting abnormal blood flow signals and spectra in the right atrium during systole on the four‐chamber view (Figure 2). The severity of TR is graded semi‐quantitatively as mild (narrow jet, ≤ half the atrial length), moderate (narrow jet, > half the atrial length), or severe (wide jet, > half the atrial length) [13]. Control group fetuses exhibited no abnormalities in cardiac structure, function, or significant valvular regurgitation.

FIGURE 1.

Fetal Long‐Axis View of the Aortic Arch. The image shows a significant Coarctation at the aortic arch (arrow). AAO, ascending aorta; DAO, descending aorta; CoA, coarctation of the Aorta).

FIGURE 2.

Severe Tricuspid Regurgitation (TR) in a Fetus: Four‐Chamber View on Color Doppler Flow Imaging. Asterisk indicates TR jet; LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle.

Exclusion criteria included fetal chromosomal abnormalities, extracardiac malformations, or suboptimal image quality caused by thick maternal abdominal walls, unfavorable fetal positioning, or frequent fetal movement. Fetuses with complex cardiac malformations that were difficult to classify were also excluded. Additionally, pregnant women with gestational diabetes or gestational hypertension were excluded.

2.3. Equipment and Methods

Fetal echocardiography was performed using Philips IE33 and GE Voluson E10 ultrasonography systems equipped with S8‐3 (3–8 MHz) and C9‐2 (2–9 MHz) probes.

Pregnant women were positioned laterally or supine during routine fetal echocardiography. An experienced specialist captured dynamic images of the fetal apical four‐chamber view, storing at least three cardiac cycles in DICOM format. Image quality was optimized by adjusting depth, width, and imaging gain. Frame rates were set above 80 frames per second to ensure sufficient temporal resolution for speckle tracking analysis.

All measurements were performed by a senior fetal echocardiography specialist. Each fetus routinely underwent measurements of fetal heart rate (FHR), biparietal diameter (BPD), femur length (FL), systolic aortic annular diameter (AO), systolic pulmonary annular diameter (PA), pulmonary‐to‐aortic diameter ratio (PA/AO), RA end‐systolic longitudinal dimension (RAESL), RA end‐systolic transverse dimension (RAESD), RA end‐systolic area (RAESA), right ventricular end‐diastolic transverse dimension (RVEDD), and tricuspid annular plane systolic excursion (TAPSE) measured by free‐angle M‐mode.

Stored images of the four‐chamber view were imported into the TOMTEC‐ARENA offline analysis workstation (TOMTEC Imaging Systems GmbH, Unterschleissheim, Germany) for processing. A second attending physician, who was blinded to the patient groups, performed the analyses. Due to the absence of fetal electrocardiography, cardiac cycles were identified using M‐mode echocardiographic curves (Figure 3a). The zero‐strain reference point was defined as the end‐diastole of the right ventricle, characterized by the imminent closure of the tricuspid valve. The right atrial endocardial border was manually traced according to the 2018 European Association of Cardiovascular Imaging/American Society of Echocardiography guidelines. Tracings encompassed the interatrial septum, lateral wall, and contralateral tricuspid annulus (Figure 3b). Dedicated software automatically tracked endocardial boundaries throughout the cardiac cycle, with manual correction of inaccurate segments as necessary. The software generated a strain curve for the cardiac cycle (Figure 3c). The peak of the curve represented RAGLS, expressed as an absolute value reflecting right atrial reserve function. TAPSE was measured using free‐angle M‐mode, with the sampling line positioned at the tricuspid annulus‐right ventricular free‐wall junction, parallel to the interventricular septum and perpendicular to the annulus. Maximum annular displacement from end‐systole to end‐diastole represented TAPSE.

FIGURE 3.

Right atrial strain analysis. (a) M‐mode echocardiography identifies cardiac cycles (b) Four‐chamber view of the fetal heart with myocardial border tracking of the right atrium. (c) Atrial global longitudinal systolic strain measurement within 1 cardiac cycle.

To assess measurement reliability, inter‐ and intra‐observer repeatability of RAGLS was evaluated. A second observer randomly selected 40 cases (21 controls, 10 LVOTO, 9 TR) and independently performed RAGLS measurements. Three weeks later, the first observer repeated measurements for these same cases.

2.4. Statistical Analysis

Data analysis was performed using SPSS 30.0 software. Sample size was estimated using PASS 15, setting effect size at 0.25, power at 0.95, and α = 0.05. With 100 controls, the minimum required case group size was calculated as 16, and the actual case group size met this requirement. Normality of continuous data was tested; normally distributed data were expressed as mean ± SD, while non‐normally distributed data were reported as M (Q1, Q3). Comparisons among groups utilized one‐way ANOVA or Kruskal–Wallis H tests based on data distribution. Spearman's rank correlation analysis examined relationships between RAGLS, GA, and echocardiographic parameters. Correlation coefficients (r) of <0.3, 0.3–0.6, and >0.6 indicated weak, moderate, and strong correlations, respectively. Reliability was evaluated using ICC, with values <0.40 indicating poor reliability, 0.40–0.75 fair reliability, and >0.75 good reliability. Reliability was also assessed using Bland‐Altman analysis. A two‐tailed p < 0.05 indicated statistical significance.

3. Results

A total of 157 fetuses were analyzed, divided into a control group (n = 100), an LVOTO group (n = 32), and a TR group (n = 25). No statistically significant differences existed among the groups regarding maternal age, GA, FHR, BPD, FL, or RVEDD (all p > 0.05). This indicated comparable baseline characteristics among the three groups.

Significant differences in cardiac structural and functional parameters were observed among the groups (all p < 0.05). Detailed data are shown in Table 1.

TABLE 1.

Baseline clinical characteristics of the study population

Parameter	Control group (n = 100)	LVOTO group (n = 32)	TR group (n = 25)	p value
Maternal & Obstetric
Maternal age (years)	29.8 ± 3.9	29.1 ± 4.8	30.1 ± 4.2	0.61
Gestational age (weeks)	25.8 ± 3.9	25.8 ± 4.5	27.2 ± 5.2	0.34
Fetal growth
Biparietal diameter, BPD (mm)	63.4 ± 11.3	62.3 ± 12.8	67.7 ± 13.0	0.17
Femur length, FL (mm)	46.2 ± 7.9	45.8 ± 11.2	48.9 ± 11.2	0.41
Cardiac dimensions & Function
Fetal heart rate, FHR (bpm)	146.5 ± 10.1	141.4 ± 7.8	143.8 ± 10.6	0.15
Aortic annulus, AO (mm)	3.8 (3.5, 4.8)	3.1(2.3, 4.1)*	4.5(3.9, 5.0)*†	<0.001
Pulmonary annulus, PA (mm)	4.9 (4.5, 6.0)	5.6 (4.9, 6.4)*	4.3(3.4, 5.7)*†	<0.05
PA/AO ratio	1.3(1.2, 1.3)	1.8(1.4, 2.2)*	0.9 (0.8, 1.3)*†	<0.001
RA end‐systolic length, RAESL (mm)	9.9(9.0, 11.4)	10.7(8.8, 14.4)	15.0(12.9, 18.9)*†	<0.001
RA end‐systolic diameter, RAESD (mm)	10.8 ± 2.6	11.1 ± 3.2	14.2 ± 3.2*†	<0.001
RA end‐systolic area, RAESA (cm2)	1.0 (0.7, 1.4)	0.9 (0.8, 1.5)	1.5(1.2, 2.4)*†	<0.001
RV end‐diastolic diameter, RVEDD (mm)	9.5 (7.9, 11.9)	9.8 (8.0, 12.3)	9.9(7.7, 13.4)	0.70
Tricuspid annular plane systolic excursion, TAPSE(mm)	6.9 ± 0.9	5.6 ± 1.4*	5.8 ± 1.5*	<0.001
Right strial global longitudinal strain, RAGLS (%)	36.4 ± 5.4	32.6 ± 6.7*	22.4 ± 5.5*†	<0.001

Abbreviations: LVOTO, left ventricular outflow tract obstruction; TR, tricuspid regurgitation; RA, right atrium; RV, right ventricle.

Note: *p < 0.05 compared with the control group; †p < 0.05 compared with the LVOTO group. Variables meeting normality were expressed as Mean ± SD, while non‐normally distributed variables were presented as M (Q1, Q3)

Among routine echocardiographic parameters, the AO was significantly smaller in the LVOTO group compared to the control and TR groups. Conversely, AO was enlarged in the TR group. The PA/AO ratio was significantly decreased in the TR group and significantly increased in the LVOTO group. This finding reflected distinct hemodynamic changes associated with the two types of congenital heart disease. The RAESL, RAESD, and RAESA in the TR group were significantly larger than in the other two groups, reflecting severe RA volume overload. Although RAESL and RAESD were larger in the LVOTO group compared to controls, the difference was not statistically significant.

Regarding fetal RA function, significant differences in RAGLS among the three groups were observed (Figure 4). In both case groups, RAGLS values were significantly lower than in the control group (p < 0.05). Additionally, fetuses with moderate‐to‐severe TR had significantly lower RAGLS than those in the LVOTO group (p < 0.001). Furthermore, both case groups exhibited significantly lower TAPSE compared to controls (p < 0.05), indicating right ventricular systolic dysfunction in both groups.

FIGURE 4.

Violin plots of RAGLS for the control, LVOTO, and TR groups, with intergroup comparisons.

In the control group, RAGLS showed a moderate negative correlation with GA (r = −0.47, p < 0.01), as shown in Figure 5a. The linear regression equation was Y = 53.15 − 0.65X, R ² = 0.22, p < 0.01. RAGLS also showed moderate negative correlations with BPD, FL, AO, PA, RAESL, RAESD, RAESA, and RVEDD (all p < 0.01). In both the LVOTO and moderate‐to‐severe TR groups, RAGLS had no significant correlation with GA, routine cardiac structural parameters, or TAPSE (all p > 0.05; Table 2). In the LVOTO group, the regression of RAGLS on GA yielded a non‐significant equation: Y = 33.42 − 0.032X (R ² = 0.0004, p = 0.9; Figure 5b). Similarly, in the moderate‐to‐severe TR group, the association was also non‐significant (Y = 15.85 + 0.242X, R ² = 0.03, p = 0.3; Figure 5c).

FIGURE 5.

Scatter plot and linear regression analysis of RAGLS and gestational age in the control group, LVOTO group, and TR group.

TABLE 2.

Correlation between RAGLS and other variable

Parameter	Control Group		LVOTO Group		TR Group
	r	p value	r	p value	r	p value
Maternal Age (years)	−0.12	0.25	−0.02	0.36	−0.21	0.31
Gestational Age (weeks)	−0.47	<0.001	0.02	0.91	0.18	0.40
Biparietal Diameter, BPD (mm)	−0.50	<0.001	0.04	0.82	0.17	0.43
Femur Length, FL (mm)	−0.46	<0.001	0.02	0.93	0.12	0.56
Fetal Heart Rate, FHR (bpm)	0.03	0.79	−0.11	0.57	0.01	0.96
Aortic Annulus, AO (mm)	−0.39	<0.001	0.09	0.65	0.02	0.93
Pulmonary Annulus, PA (mm)	−0.44	<0.001	0.25	0.18	0.21	0.33
PA/AO Ratio	0.03	0.78	0.05	0.78	0.12	0.58
RA End‐Systolic Length, RAESL (mm)	−0.45	<0.001	0.06	0.74	0.10	0.65
RA End‐Systolic Diameter, RAESD (mm)	−0.36	<0.001	0.06	0.75	0.07	0.76
RA End‐Systolic Area, RAESA (cm2)	−0.43	<0.001	0.06	0.75	0.05	0.80
RV End‐Diastolic Diameter, RVEDD (mm)	−0.32	<0.001	0.12	0.54	0.12	0.56
Tricuspid Annular Plane Systolic Excursion, TAPSE(mm)	0.09	0.37	0.22	0.23	0.09	0.67

Abbreviations: LVOTO, left ventricular outflow tract obstruction; RA, right atrium; RAGLS, right atrial global longitudinal strain; RV, right ventricle; TR, tricuspid regurgitation.

In the control group, inter‐observer ICC value was 0.82, and intra‐observer ICC value was 0.80. In the case groups, inter‐observer ICC value was 0.83, and intra‐observer ICC value was 0.91. All ICC values exceeded 0.75, indicating excellent reliability and reproducibility of 2D‐STE measurements of fetal RAGLS. Bland‐Altman plots for intra‐observer and inter‐observer reliability are presented in Figures 6 and 7.

FIGURE 6.

Bland‐Altman plots for intraobservor reliability for measurements of RAGLS with mean and 95% limits of agreement (dotted horizontal lines).

FIGURE 7.

Bland‐Altman plots for interobservor reliability for measurements of RAGLS with mean and 95% limits of agreement (dotted horizontal lines).

4. Discussion

RAGLS is defined as the rate of change in endocardial length from the end of atrial systole to peak diastole, calculated as (end‐systolic length − end‐diastolic length)/end‐diastolic length [14]. This parameter corresponds to the atrial filling phase during ventricular systole and appears as a characteristic peak on the strain curve, indicating the reserve function of the right atrium. The precise contribution of the right atrium to right ventricular filling and cardiac output remains incompletely elucidated. This contribution might be influenced by ventricular diastolic characteristics and function. Nevertheless, the interdependence between atrial and ventricular function is widely recognized. TAPSE is conventionally used as a sensitive indicator of right ventricular systolic function in adults [15, 16]. Studies addressing the relationship between TAPSE and fetal right atrial function remain limited. Because the right atrial reservoir phase coincides with right ventricular systole, TAPSE was used in this study as a reference parameter to explore potential associations between right ventricular systolic function and right atrial reserve function.

The average RAGLS in the control group was (36.4% ± 5.4%). Devore et al. [14] reported that the RAGLS in normal fetuses was approximately (35.86% ± 13.3%), a value close to the mean obtained in the present study, albeit with greater variability. This discrepancy may be attributable to their larger sample size (200 cases) and differences in analytical methods. A negative correlation between RAGLS and GA indicated decreasing fetal right atrial reservoir function with advancing pregnancy. RAGLS also showed negative correlations with multiple growth and cardiac parameters, including BPD, FL, AO, PA, RAESL, RAESD, RAESA, and RVEDD. These findings reflected the intrinsic association of RAGLS with increasing GA. Possible explanations for these findings include the following two points. First, the gradual maturation of right ventricular myocardium improves compliance and diastolic function. Consequently, blood from the right atrium more easily enters the right ventricle during diastole, reducing right atrial volume load and diminishing its reserve capacity [17, 18]. Second, placental vascular resistance, the main determinant of fetal right ventricular afterload, continues to decrease during late pregnancy [19]. The reduction in right ventricular afterload enhances cardiac output and atrial emptying. Furthermore, the fetal foramen ovale differs from the adult structure, acting as a conduit that directs most inferior vena cava blood directly into the left heart [20] With advancing GA, left ventricular diastolic function improves and cerebral vascular resistance decreases [21], lowering left ventricular afterload and promoting left atrial emptying. This accelerates right atrium emptying via the foramen ovale. These combined effects result in decreased right atrial reserve function.

In the control group, RAGLS negatively correlated with GA, reflecting normal physiological maturation of the fetal cardiovascular system. In a study of 101 normal fetuses, Meister et al. similarly confirmed a significant negative correlation between RAGLS and gestational age, which is consistent with our findings [22]. In fetuses with TR or LVOTO, right atrial function impairment disrupted this developmental correlation. RAGLS showed no significant correlation with measured growth and cardiac parameters (BPD, FL, AO, PA, RAESL, RAESD, RAESA, and RVEDD), indicating the pathophysiological effects had masked the physiological trajectory. This disruption suggested the right atrial compensatory capacity had reached its limit under abnormal hemodynamic loading. Thus, right atrial function no longer followed the established developmental pattern. In this study, no significant correlation was observed between RAGLS and TAPSE in either the control or case groups. However, both RAGLS and TAPSE significantly differed between case and control groups. These findings implied that reduced right ventricular systolic function might impair right atrial reserve function. The underlying mechanisms of this association warrant further investigation.

Due to the direct impact of moderate‐to‐severe TR on the right atrium, fetuses with TR exhibited the lowest RAGLS values. Meister et al. [22]. reported a case of pulmonary atresia with TR, in which the RAGLS was only 20.65%, markedly lower than that of the control group, suggesting impaired right atrial function in fetuses with TR—a finding that also aligns with the results of the present study. RAGLS primarily reflects the passive filling capacity of the right atrium during ventricular systole. TR causes right atrial volume overload, reducing the intrinsic deformation capacity of atrial myocardium. Severe blood regurgitation into the right atrium causes acute or chronic atrial dilatation, indicated by significant increases in RAESL, RAESD, and RAESA. This finding mirrors observations in adults with severe TR, where right atrial dilatation and dysfunction predict poor prognosis [23, 24]. Prolonged overload can trigger atrial remodeling, including myocardial fibrosis. This remodeling directly reduces atrial compliance and relaxation, resulting in decreased strain. Additionally, reduced TAPSE in case groups indicated impaired right ventricular systolic function. Right ventricular contraction provides the primary force expanding the right atrial wall during systole. Reduced right ventricular function implies diminished stretching force on the right atrium, increasing residual right ventricular blood volume at end‐systole and elevating end‐diastolic pressure. The combined effects of increased preload and reduced stretching force significantly impaired right atrial reserve function in fetuses with moderate‐to‐severe TR.

This study demonstrated that fetal RAGLS in the LVOTO group was significantly lower than in controls. Increased pressure load on the left heart is the primary consequence of LVOTO, which includes conditions such as AS, CoA, IAA, and HLHS [25, 26]. Right atrial function is affected through an indirect mechanism, reflecting strong interdependence within fetal circulation. In normal fetuses, oxygenated blood shunts from the right atrium to the left atrium through the foramen ovale. However, significantly elevated left atrial pressure limits or reverses this shunt in severe LVOTO. Consequently, blood destined for the left heart accumulates in the right heart system, increasing right ventricular volume load [27]. The right heart responds by increasing stroke volume as compensation. Although this volume increase is less pronounced than in severe TR, it sufficiently challenges right atrial compensatory capacity. The fetus may also raise systemic vascular resistance through neurohumoral regulation, further elevating right ventricular afterload. Increased afterload subsequently transmits to the right atrium, restricting diastolic expansion and impairing right atrial function. Notably, to date, no dedicated studies have been conducted on right atrial function in fetuses with LVOTO. Existing evidence [28] is primarily derived from a fetal sheep model of acute obstruction, which suggested that right ventricular function remains relatively stable without compensatory changes under acute left ventricular outflow obstruction. This indirectly implies that the right atrium may also exhibit no significant functional compensation or impairment. This conclusion is inconsistent with our findings. We speculate that the main reason for this discrepancy is that the fetal sheep model represents acute experimental obstruction, whereas the LVOTO fetuses in our study experienced chronic, progressive alterations in left heart hemodynamics during intrauterine development. The sustained obstruction of the left heart system, through abnormal foramen ovale flow, exerts progressive effects on the structure and function of both the left and right hearts, ultimately leading to reduced right atrial global strain. This mechanism warrants further investigation and validation in future studies.

The degree of RAGLS impairment in the LVOTO group was milder compared with the moderate‐to‐severe TR group. This indicated distinct pathophysiological mechanisms between the two conditions. TR imposes a direct and severe volume load on the right atrium, whereas LVOTO indirectly affects right atrial function through combined volume and pressure loads. The observed difference in severity suggests that RAGLS could distinguish between different hemodynamic load abnormalities.

In this study, the TR group exhibited significantly increased values of RAESL, RAESD, and RAESA, which aligns with the characteristic findings of right atrial enlargement due to volume overload. Research on right atrial strain in adults has shown that atrial enlargement leads to a reduction in reservoir function [29]. The findings from this fetal study demonstrate results consistent with those observed in adults. Compared to the LVOTO and control groups, the TR group had a significantly larger AO diameter. This is most likely because the increased right atrial volume overload causes more blood to be shunted into the left heart through the foramen ovale, increasing the left heart volume load. However, the PA diameter of the TR group was significantly smaller than that of the other two groups. This is because TR causes a portion of blood to flow back into the right atrium during right ventricular systole, rather than being entirely ejected forward into the PA. Consequently, PA perfusion decreases, restricting its development and resulting in smaller dimensions. Forward aortic flow is greatly reduced in the LVOTO group due to ineffective left ventricular blood ejection into the aorta. Sonographically, this reduced flow causes the aortic to underdevelop, which manifests as a smaller AO or even an aortic interruption. At the same time, an elevated left heart pressure load may cause a reversal of flow across the foramen ovale, which could raise the right heart volume load and cause PA enlargement. These two opposing patterns of great vessel morphology clearly illustrate the compensatory interaction between the left and right hearts within the fetal circulation.

The study by Howley et al. [30]. demonstrated that fetuses with severe TR exhibited right atrial enlargement and functional impairment, as reflected by significantly reduced right atrial emptying fraction, filling fraction, and reservoir function. Their findings confirmed that right atrial dysfunction is a contributing factor to adverse fetal outcomes, including an increased risk of hydrops fetalis and intrauterine death. For fetuses with moderate‐to‐severe TR, such as those with Ebstein anomaly or tricuspid valve dysplasia, the primary clinical value of RAGLS lies in identifying high‐risk subgroups and predicting perinatal outcomes. A marked reduction in RAGLS should be regarded as an independent and strong predictor of poor prognosis. This finding carries several clinical implications: closer fetal surveillance and more frequent follow‐up visits are warranted, with careful monitoring for signs of hydrops; and delivery timing should be optimized to avoid urgent situations at term. For fetuses with LVOTO, RAGLS may serve as an indirect marker of the hemodynamic burden imposed by left heart impairment and the severity of the disease. It helps assess whether the relatively unaffected right ventricle possesses sufficient functional reserve to sustain a single‐ventricle circulation. Incorporating RAGLS into the routine fetal echocardiographic evaluation has the potential to meaningfully improve the precision of clinical management for both conditions.

This study confirmed that under strict image‐quality control and standardized post‐processing protocols, 2D‐STE reliably quantified fetal right atrial strain with excellent reproducibility (ICC > 0.75). The angle‐independent characteristic of 2D‐STE offers potential advantages over traditional Doppler techniques when evaluating morphologically irregular fetal atria. This study had a small sample size, was retrospective, and was single‐center. Larger sample sizes and a prospective, multicenter design should be the norm for future studies. Furthermore, measurement errors could be introduced if adult cardiac software is used. One crucial area for future research was the establishment of direct correlations between fetal RAGLS values and neonatal outcomes, which was not possible due to the lack of postnatal follow‐up.

5. Conclusion

This study systematically compared RAGLS among normal fetuses, fetuses with moderate‐to‐severe TR, and fetuses with LVOTO for the first time. The results confirmed that 2D‐STE was a reliable and reproducible method for evaluating fetal right atrial function. RAGLS provided a novel quantitative reference for assessing fetal right atrial dysfunction. Both moderate‐to‐severe TR and LVOTO significantly impaired RA reserve function, with TR resulting in greater impairment. Future research should focus on increasing sample sizes, developing fetal‐specific analytical software, and conducting neonatal follow‐up studies.

Funding

National Key Research and Development Program of China (2023YFC2705700); Zhejiang University Science and Technology Research Institute General Horizontal Project (School Collaboration‐2021‐KYY‐518053‐0055)

Ethics Statement

This study was approved by the Ethics Committee of Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China (Approval No. 20200210–78). All procedures were performed in accordance with the ethical standards of the institutional and national research committee and with the Declaration of Helsinki.

Consent

Written informed consent was obtained from all individual participants included in the study.

Conflicts of Interest

The authors declare no conflicts of interest.

Yang Y., Zhou L., Mao Y., et al. “How Does Right Atrial Function Differ? A Speckle‐Tracking Echocardiographic Comparison of Fetuses With Left Ventricular Outflow Tract Obstruction Versus Those With Significant Tricuspid Regurgitation.” Echocardiography 43, no. 5 (2026): e70499. 10.1111/echo.70499

Data Availability Statement

Data described in the manuscript will be made available upon request and being approved by the Ethical Committee of the author's institute, with a signed data access agreement. To access these data, one should contact zbwcjp@zju.edu.cn via email.