Assessment of Left Atrial Function in Normal Fetuses Using Speckle Tracking Analysis: Implications for Diastolic Function

doi:10.21203/rs.3.rs-3247188/v1

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Assessment of Left Atrial Function in Normal Fetuses Using Speckle Tracking Analysis: Implications for Diastolic Function

https://doi.org/10.21203/rs.3.rs-3247188/v1

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Introduction:

Fetal echocardiography is a valuable diagnostic tool for evaluating the structure and function of the fetal heart. However, assessing fetal left atrial (LA) function in various phases remains challenging, and the relationship between fetal LA and diastolic function is unknown. We used two-dimensional speckle-tracking echocardiography (2D-STE) to assess LA function in healthy fetuses in different stages and evaluated the relationship between fetal LA function and diastolic function.

Materials and methods

This single-center prospective study included 225 healthy women with normal singleton pregnancies. At three gestational ages, 23–24 weeks, 32–33 weeks, and 36–37 weeks, 2D-STE was performed to obtain the LA strain and strain rate in the reservoir, conduit, and contraction phases. Parameters of left ventricular (LV) diastolic function, including global longitudinal early peak LV strain rate, global longitudinal late peak LV strain rate, diastolic strain rate e/a ratio, and mitral Doppler inflow pattern E/A ratio were measured and correlated with LA strain parameters.

Results

Of the 225 cases, 198 (88%) were included in the analysis. Compared with measurements in the second trimester, during the third trimester, both LA strain and strain rate were lower during the reservoir and contraction phases, while the LA strain was more significant during the conduit phase (all p < 0.05). The LA strain and strain rate in the contraction phase showed a significant correlation with the parameters of LV diastolic function.

Conclusions

Our study findings suggest that LA contraction function correlates strongly with LV diastolic function in fetuses. Thus, monitoring changes in atrial function throughout gestation can be valuable for assessing fetal cardiac maturation and identifying abnormal fetal cardiac position.

fetal echocardiography

left atrium

left ventricle

strain

diastolic function

The left atrium plays a key role in regulating ventricular filling and cardiac output. However, only a few studies have focused on characterizing fetal left atrial (LA) function [1–3]. Furthermore, the relationship between LA function and diastolic function has only been investigated in adults, and in this population, LA function in each phase was shown to contribute to LV diastolic function [4, 5]. Notably, the anatomy and physiology of the fetal myocardium and circulation differ from those of the newborn and the adult, and the role of LA phase function in fetal myocardial development and its relationship with diastolic function remain poorly understood.

In recent years, two-dimensional speckle-tracking echocardiography (2D-STE) has been increasingly used for evaluating both left ventricular (LV) and right ventricular (RV) deformation in the fetus [1, 6]. Changes in strain parameters reflect the maturity of the fetal myocardium and the degree of cardiac dysfunction under pathological conditions. The assessment of LA function is a crucial aspect of evaluating global cardiac function. However, data on parameters that reflect fetal LA myocardial deformation are limited, and our understanding of fetal LA changes and their relationship with fetal myocardial diastolic function remains incomplete [7]. Moreover, variability in image acquisition protocols, frame rates, and software from different vendors leads to divergent strain values, highlighting the need for further research to enrich the available data and provide evidence for the key role of measuring LA strain parameters in the evaluation of fetal cardiac function [5].

The purpose of this study was to characterize LA function in different phases in healthy fetuses and investigate associations between parameters of LS function and parameters of fetal myocardial diastolic function using speckle tracking analysis at different gestational ages.

Participants

For this single-center, prospective study, a total of 225 healthy, non-smoking women with a normal singleton pregnancies who were undergoing routine obstetric examinations from November 2020 to November 2021 at Beijing Chaoyang Hospital, affiliated with Capital Medical University were invited to enroll. Gestational age (in weeks) was determined by the last menstrual period and fetal crown-rump length measured by ultrasonography in the first trimester. The exclusion criteria included unacceptable visualization of the fetal heart, maternal chronic disease or obstetric complications, and fetal malformations. According to the results of routine postnatal examinations, all 225 women gave birth to a healthy infant. The study was granted approval by the ethics committee Beijing Chaoyang Hospital, and all cases provided written informed consent for study participation.

Image acquisition and analysis

All imaging examinations were performed by an experienced fetal sonographer (more than 3 years of experience) using the Philips EPIQ 7C ultrasound system with C5-1 probes. Ultrasound data were collected only once for each case at one of the following time points: 23–24 weeks of pregnancy, 32–33 weeks of pregnancy, and 36–37 weeks of pregnancy. For offline analysis, the sonographer saved a four-chamber fetal heart view with either an acceptable apical or basal view that clearly showed the atrial endocardial border with a frame rate exceeding 100 frames per second (fps). Two examiners conducted offline image analysis using the QLAB 13.0 software (Philips Healthcare, The Netherlands).

The cardiac cycle was defined mechanically rather than by an electrocardiography (ECG): one frame prior to mitral valve closure and ending at the next frame immediately prior to mitral valve closure were examined as a single cardiac cycle. For analysis, three consecutive cardiac cycles were chosen. The area of interest for the left atrium was traced from the endocardial boundary of the mitral annulus and extrapolated along the opening of the pulmonary vein and/or the left atrial appendage to the endocardial boundary of the left atrium on the side of the mitral annulus, set to fit the width of the LA wall (0.1 cm), including the whole of the atrial wall with pulmonary veins and the foramen ovale. Examples of the LA strain and LA strain rate curve are shown in Fig. 1. The software automatically tracked the area of interest, and the examiners visually inspected the tracking results to ensure the accuracy of the software for endometrial tracking. Before reapplying the tracking algorithm, any necessary changes were made to the area of interest.

The following parameters were measured: LA strain during reservoir phase (LASr), LA strain during conduit phase (LAScd), LA strain during contraction phase (LASct), LA peak strain rate during reservoir phase (pLASRr), LA peak strain rate during conduit phase (pLASRcd), LA peak strain rate during contraction phase (pLASRct), global longitudinal early peak LV strain rate (LSr-LVe), global longitudinal late peak LV strain rate (LSr-LVa), and mitral Doppler inflow pattern E/A ratios.

The LA strain and strain rate were displayed for manual measurements. Atrial contraction initiation was defined as the start of the second downslope following the peak strain during heart diastasis in the absence of the fetal ECG. A Case was excluded if the strain during the contraction phase could not be seen on the strain curve.

Statistical analysis

Data for continous variables are expressed as mean and standard deviation (SD), or median and interquartile range. Categorical data are expressed as absolute values and percentages. The Kolmogorov–Smirnov test was used to test for data normality, and comparisons of continuous variables between different gestational ages was performed using univariate analysis of variance or Welch analysis of variance according to the results of the variance homogeneity test. The least significant difference (LSD) test or Games–Howell test was used for comparisons between two groups, and the chi-square test was used for comparisons of categorical variables. Correlations between the diastolic functional parameters and LA phasic functional parameters were assessed by calculating Spearman’s rank correlation coefficients. The intraobserver consistency and interobserver consistency of LA strain parameters were evaluated in 15 randomly selected cycles 4 weeks after the first measurement, based on calculated intraclass correlation coefficients (ICCs). All analyses were two-sided, and statistical significance was defined as P < 0.05. SPSS version 23.0 software (IBM SPSS Statistics, v23) and MedCalc 15.6 software (MedCalc Software) were used for statistical analysis.

Case characteristics and strain values

Of the recruited 225 women, 8 were excluded due to unsatisfactory tracking performance, and 19 because the initiation of LA contraction could not be identified. Thus, the final sample included in the statistical analysis consisted of 198 pregnant women (88% of total) who were subdivided into three gestational age groups: 23–24 weeks (n = 67), 32–33 weeks (n = 68), and 36–37 weeks (n = 63). The clinical characteristics and conventional echocardiographic parameters of the 198 singleton pregnancies are presented in Table 1.

Table 1

Demographic and conventional echocardiographic parameters of 198 singleton pregnancies evaluated at different gestational ages
Variables	22–24 weeks (n = 67)	31–33 weeks (n = 68)	36–37 weeks (n = 63)	P value
Maternal age (years)	29.75 ± 3.43	29.73 ± 3.27	30.98 ± 3.68	0.065
Gestational age at delivery (weeks)	39.33 ± 1.09	39.25 ± 1.14	38.93 ± 1.36	0.133
Birth weight (g)	3335.96 ± 366.25	3333.12 ± 403.62	3430.56 ± 398.88	0.274
Frame rate (fps)	115.28 ± 7.86	114.51 ± 6.90	115.24 ± 7.26	0.794
LVd (mm)	8.54 ± 0.47	12.33 ± 0.57	14.68 ± 0.68	< 0.001
RVd (mm)	8.61 ± 0.34	12.42 ± 0.66	15.21 ± 0.74	< 0.001
LAd (mm)	9.01 ± 0.56	12.12 ± 0.67	14.31 ± 0.61	< 0.001
RAd (mm)	8.98 ± 0.57	12.93 ± 0.64	15.27 ± 0.68	< 0.001
Values are mean ± standard deviation
LVd, transverse diameter of left ventricle in four-chamber view; RVd, transverse diameter of right ventricle in four-chamber view;
Lad, transverse diameter of left atrium in four-chamber view atrium; Rad, transverse diameter of right atrium in four-chamber view

LA strain and strain rate in fetuses of different gestational ages

The strain and strain rate parameters of LA phasic function are compared among fetuses of three different gestational ages in Table 2. Statistical differences in LASr, LAScd, LASct, pLASRr, and pLASRct were observed among the three age groups (all P < 0.05). LASr was lower at 32–33 weeks and 36–37 weeks than at 21–24 weeks (both P < 0.05), whereas no difference was observed between the LASr values at 32–33 weeks and 36–37 weeks (P > 0.05). LAScd did not differ significantly between 23–24 and 32–33 weeks (P > 0.05), but LAScd was higher at 36–37 weeks than at 23–24 and 32–33 weeks (all P < 0.05). From pairwise comparisons, LASct decreased with increasing gestational age, with statistical differences between each pair of groups (all P < 0.05). pLASRr and pLASRct were lower in the third trimester (32–33 weeks and 36–37 weeks) than at 23–24 weeks (both P < 0.05), with no significant difference found between the two third trimester time points (P > 0.05). pLASRcd showed no statistically significant difference among the time points (P = 0.076).

Table 2

LA functional and diastolic parameters among fetuses at different gestational ages
Variables	22–24 weeks (n = 67)	31–33 weeks (n = 68)	36–37 weeks (n = 63)	P value
LASr (%)	32.43 ± 4.36	28.85 ± 6.01^*	28.23 ± 4.93^*	< 0.001
pLASRr (sec^− 1)	5.61 ± 1.16	4.89 ± 1.20^*	4.61 ± 1.09^*	< 0.001
LAScd (%)	12.71 ± 2.97	12.98 ± 3.33	14.71 ± 3.90^*†	0.001
pLASRcd (sec^− 1)	5.00 ± 1.47	4.53 ± 1.41	4.75 ± 1.34	0.155
LASct (%)	19.74 ± 3.39	15.85 ± 3.94^*	13.48 ± 3.49^*†	< 0.001
pLASRct (sec^− 1)	8.78 ± 1.97	7.20 ± 1.99^*	6.80 ± 2.11^*	< 0.001
Mitral E/A ratio	0.62 ± 0.08	0.68 ± 0.14^*	0.74 ± 0.16^*†	< 0.001
LSr-LVe (%)	1.87 ± 0.87	2.63 ± 0.71^*	2.91 ± 0.74^*†	< 0.001
LSr-LVa (%)	3.90 ± 0.63	2.93 ± 0.55^*	2.95 ± 0.67^*	< 0.001
LSr-LV e/a	0.49 ± 0.22	0.91 ± 0.25^*	1.00 ± 0.23^*†	< 0.001
Values are mean ± standard deviation
LASr, strain during reservoir phase; pLASRr, peak strain rate during reservoir phase; LAScd, strain during conduit phase; pLASRcd, peak strain rate during conduit phase; LASct, strain during contraction phase; pLASRct, peak strain rate during contraction phase;LSr-LVe, global longitudinal early peak left ventricular strain rate; LSr-LVa, global longitudinal late peak left ventricular strain rate

LV strain and diastolic function

The LV diastolic strain rate and mitral valve E/A values of fetuses at different gestational ages are presented in Table 2. The mitral E/A ratio, LSr-LVe, and LSr-LV e/a values at 32–33 weeks and 36–37 weeks were higher than those at 23–24 weeks (all P < 0.05), with no differences in these values observed between 32–33 weeks and 36–37 weeks (P > 0.05). LSr-LVa levels were lower in the third trimester than in the second trimester (P < 0.05).

Correlations between LA strain and strain rate parameters and LV diastolic function

The results of correlation analyses between LA strain and strain rate parameters and LV diastolic strain rate, the ratio of LSr-LVe to LSr-LVa, and mitral valve E/A values are presented in Table 3. The strain and strain rate parameters representing the function of the LA reservoir and contraction phases (LASr, pLASRr, LASct, pLASRct) showed significant negative correlations with the mitral E/A ratio and LSr-LV e/a. LASct had the strongest correlation with LV diastolic function parameters, including the mitral E/A ratio, LSr-LVe, LSr-LVa, and LSr-LV e/a, with correlation coefficients of -0.56, -0.31, 0.37, and − 0.48, respectively (Fig. 2).

Table 3

Correlation between LA functional and LV diastolic parameters
	Mitral E/A ratio		LSr-LVe		LSr-LVa		LSr-LV e/a
Variables	r	P	r	P	r	P	r	P
LASr	-0.41	< 0.001	-0.098	0.167	0.32	< 0.001	-0.27	< 0.001
LAScd	0.05	0.501	0.22	0.002	-0.03	0.635	0.20	0.004
LASct	-0.56	< 0.001	-0.31	< 0.001	0.37	< 0.001	-0.48	< 0.001
pLASRr	-0.33	< 0.001	-0.07	0.319	-0.26	< 0.001	-0.22	0.002
pLASRcd	-0.07	0.322	0.13	0.060	0.17	0.016	0.013	0.851
pLASRct	-0.43	< 0.001	-0.16	0.020	0.42	< 0.001	-0.37	< 0.001
LASr: strain during reservoir phase; pLASRr, peak strain rate during reservoir phase; LAScd, strain during conduit phase; pLASRcd, peak strain rate during conduit phase; LASct, strain during contraction phase; pLASRct, peak strain rate during contraction phase; LSr-LVe, global longitudinal early peak left ventricular strain rate; LSr-LVa, global longitudinal late peak left ventricular strain rate

Intra- and interobserver variability of fetal LA strain measurements

Upon analysis of intraobserver and interobserver variability in the same cardiac cycle, the ICCs showed good-to-excellent intra- and interobserver agreement for fetal LA strain and strain rate indices (ICC values = 0.8–0.9; Table 4).

Table 4

Intraobserver and interobserver concordance
	Intraobserver		Interobserver
Variables	ICC	95%CL	ICC	95%CL
LASr	0.919	0.782–0.972	0.903	0.739–0.966
LAScd	0.897	0.728–0.964	0.848	0.616–0.946
LASct	0.886	0.693–0.960	0.876	0.672–0.957
pLASRr	0.881	0.606–0.962	0.864	0.651–0.952
pLASRcd	0.907	0.753–0.968	0.816	0.532–0.934
pLASRct	0.862	0.639–0.952	0.855	0.630–0.949
ICC, intraclass correlation coefficient; CL, confidence limit; LASr, strain during reservoir phase; pLASRr, peak strain rate during reservoir phase; LAScd, strain during conduit phase; pLASRcd, peak strain rate during conduit phase; LASct, strain during contraction phase; pLASRct, peak strain rate during contraction phase.

In this study, the parameters of fetal LA function were measured with 2D speckle-tracking echocardiography. The 2D speckle-tracking technology can be used to obtain the LA strain curve and to divide LA function into three phases within the cardiac cycle, providing measurements of reservoir strain, conduit strain, and contraction strain in adults and children [8–9]. The present study shows that LA function in the fetus also can be divided into three phases, with 88% of cases in this study having a similar LA strain curve that identified three corresponding LA phase strain values. In the third trimester, the LA reservoir strain parameters decreased, and LASct and pLASRct also decreased with increasing gestational age. In contrast, LAScd was higher at 36–37 weeks than at 23–24 weeks and 32–33 weeks. These results indicate that with fetal development, the reservoir function and pump function decrease, and the conduit function increases. We also identified a correlation between LA phase function and LV diastolic function during fetal development, and the strongest correlation was observed between parameters of LA pump function and LV diastolic function.

The left atrium stores pulmonary venous blood and energy in the form of pressure during ventricular systole. Moreover, the left atrium acts as a conduit for pulmonary venous blood to flow into the left ventricle in early diastole, and in late diastole, it contracts to maintain LV filling. The LA blood mainly comes from the right atrium through the foramen ovale with a small amount coming from the pulmonary veins in fetuses [10]. Although the source of LA blood flow in fetuses differs from that in adults, there are still three phases: the reservoir phase, conduit phase, and contraction phase, which are the same as in adults. Another aspect that differs from adults is that LV filling seems to be more dependent on atrial contraction [11, 12], and, thus greater attention has been paid to the role of the atrium in fetal heart development.

The fetal LV myocardium has fewer myofibrils, shows a more random arrangement, and is not yet fully elongated, especially in early pregnancy [13]. The internal structures of fetal myocytes (including the energy-producing mitochondria and the sarcoplasmic reticulum that regulates calciumions) are immature, resulting in the fetal myocytes having less active tone, elevated resting tone, and lower relaxation capacity and compliance than mature myocytes. During this time, LV filling is mostly completed by contraction of the left atrium. As the LV myocardium continues to mature, the diastolic function also increases [14]. Tissue Doppler measurements of e' at the LV, right ventricular, and septal annuli increase faster than a' with increasing gestational age [15]. The mitral E/A in fetuses is similar to that in older adults and also increases with gestational age, indicating altered flow patterns [16]. As LV diastolic function matures, blood in the left atrium decreases, lowering preload and resulting in a reduction in LASr and pLASRr, as illustrated by the results of the present study. We also observed that LAScd decreased in the third trimester, which may have been caused by the fetal hemodynamics. Left and right ventricular afterload are mostly determined by placental and fetal cerebrovascular resistance, respectively. The placental vascular resistance and fetal cerebrovascular resistance both decrease in the third trimester after reaching their peak levels in the second trimester [17, 18].

Our study also found a negative correlation between LA systolic and LV diastolic parameters. This indicates that with the increase of LV myocardial relaxation, the demand for LA contraction decreases during the LV diastole. Our analysis also revealed a weak positive correlation between LAScd and LSr-LVe in this study. Many studies in adults have shown that LA conduit function directly reflects LV function at the early diastolic period. Based on findings that reduced LV diastolic function and LA conduit function correlate linearly, the increase in conduit flow may reflect an increase in suction acting on the LV side [19][20]. Compared with those in adults, fetal LA hemodynamics and function are more complex, with differences including foramen ovale opening and lack of pulmonary vein blood flow [21]. Also, functional changes in the fetal heart are influenced by the resistance of fetal cerebral and placental blood vessels. This complex relationship may explain why the correlation coefficient between fetal LA phase function and diastolic function parameters was not higher.

In comparison to previous studies, the techniques used in study offer greater feasibility, and the results suggest that a higher frame rate may be required to identify changes in the fetal left atrium. Joao et al. reported the identification of contraction strain in 67% of 53 normal fetal LA strain curves and that a high frame rate aided the identification of the curve’s starting point of LA contraction [22]. Although some studies have shown that a higher frame rate leads to reduced strain values [23–24], higher frame rates can provide adequate temporal resolution, especially for the rapid fetal heart rate.

The present study has several limitations. First, the sample size was a relatively small and recruited from a single-center. Thus, larger prospective, multi-center studies are needed. Additionally, the software applied in this study was not a specialized LA analysis software program. Instead, the 2D speckle-tracking echocardiographic software used in this study was designed for ventricles and based on ‘‘normal’’ LV myocardial mechanics [25]. Because fetal ECG is not possible, this study used the strain curve to judge the left atrium functional phases. Also, the region of interest included the entrance of the pulmonary vein and the foramen ovale, and therefore, the influence of the valve activity of the foramen ovale could not be ruled out. However, in a previous study, no significant difference was found among strain values of corresponding segments with or without the foramen ovale [22].

Compared with that observed in the second trimester, fetal LA reservoir function and contraction function decreased in the third trimester, while conduit function increased. The strain parameters of the LA contraction phase were closely related to parameters of LV diastolic function. Characterization of the changes in normal atrial function with gestational age can provide a foundation for evaluating fetal cardiac maturation and detecting abnormal fetal cardiac function.

LASr Left atrial strain during reservoir phase

pLASRr Left atrial peak strain rate during reservoir phase

LAScd Left atrial strain during conduit phase

pLASRcd Left atrial peak strain rate during conduit phase

LASct Left atrial strain during contraction phase

pLASRct Left atrial peak strain rate during contraction phase

LSr-LVe global longitudinal early peak left ventricular strain rate

LSr-LVa global longitudinal late peak left ventricular strain rate

LVd transverse diameter of left ventricle in four-chamber view

RVd transverse diameter of right ventricle in four-chamber view;

LAd transverse diameter of left atrium in four-chamber view atrium

RAd transverse diameter of right atrium in four-chamber view

Ethical approval was obtained from the ethics review board of Beijing Chaoyang hospital ethics committee (NO.2020-department-34). All participants provided witten informed consent before performance.

Competing interests

None.

Funding

This study was funded by the Beijing Key Specialists in Major Epidemic Prevention and Control. Dr. Xiuzhang Lu is in charge of the funding, and he is the corresponding author of this manuscript.

Consent to Publication statement

Not applicable

Availability of data and materials

The datasets of the current study are not publicly available due to the restrictions by the Beijing Chaoyang Hospital. The authors used this dataset under an agreement with the Beijing Chaoyang Hospital for the present study. The data are available from the corresponding author on reasonable request.

Acknowledgements

Not applicable

Authors’ contributions

Dr. Xiaoguang Ye and Xiuzhang Lu conceived and designed the study. Dr. Lanlan Sun , Dr. Xiaoguang Ye and Dr. Qizhe Cai participated in the acquisition of data. Dr. Weiwei Zhu and Xueyan Ding analyzed and statisticed the data. Dr. Yidan Li and Qizhe Cai gave advice on methodology. Dr. Xiaoguang Ye drafted the manuscript. Dr. Yidan Li proofread the manuscript. All authors have read and approved the final version of the manuscript for submission.

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Assessment of Left Atrial Function in Normal Fetuses Using Speckle Tracking Analysis: Implications for Diastolic Function

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Abstract

Introduction:

Materials and methods

Results

Conclusions

Figures

Introduction

METHODS

Participants

Image acquisition and analysis

Statistical analysis

Results

Case characteristics and strain values

LA strain and strain rate in fetuses of different gestational ages

LV strain and diastolic function

Correlations between LA strain and strain rate parameters and LV diastolic function

Intra- and interobserver variability of fetal LA strain measurements

Discussion

Conclusion

Abbreviations

Declarations

References

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