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 Table of Contents  
ORIGINAL RESEARCH
Year : 2022  |  Volume : 6  |  Issue : 2  |  Page : 100-107

Echocardiographic Assessment of Right Ventricular Systolic Function in Postoperative Tetralogy of Fallot Patients with Special Emphasis on Right Ventricular-Global Longitudinal Strain


Department of Pediatric Cardiology, Fortis Escorts Heart Institute, New Delhi, India

Date of Submission11-Nov-2021
Date of Acceptance21-Dec-2021
Date of Web Publication23-Feb-2022

Correspondence Address:
Dr. Mohammad Moaaz Kidwai
Flat No – G3, Ground Floor, Alhamd Gulmohar Suites, New Sir Syed Nagar, Aligarh - 202 002, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiae.jiae_60_21

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  Abstract 


Background: Limitations of echocardiography have long been known for the assessment of right ventricular (RV) systolic function in postoperative tetralogy of Fallot (TOF) patients. In this study, we evaluated the role of RV-global longitudinal strain (GLS) for the assessment of RV systolic function. Materials and Methods: It was a single institution prospective observational study of ninety postoperative TOF patients. Detailed 2-dimensional echocardiography along with RV-GLS using speckle tracing imaging was done at baseline and after 1 year. The children were divided into three groups based on duration since total correction, i.e., group A (6 months to 5 years), group B (6–10 years), and group C (>10 years) to assess the differences in RV systolic function. Furthermore, correlation of RV-GLS with RV-fractional area change (FAC), tricuspid annular plane systolic excursion, and tricuspid valve tissue Doppler imaging s' velocity was done. Results: In group A patients, a statistically significant increase in RV systolic function was seen over a period of 1 year. However, in group B and C patients, no significant change was seen. There was a strong positive correlation of RV-GLS only with RV-FAC during the first follow-up (r = 0.41, P < 0.01) and second follow-up periods (r = 0.67, P < 0.01). Conclusion: RV-GLS has a strong positive correlation with RV-FAC, and it detects preclinical regional myocardial dysfunction even when the RV-FAC is normal and thus must be included in the evaluation of postoperative TOF children.

Keywords: Global longitudinal strain-global longitudinal strain, right ventricular systolic function, tetralogy of Fallot


How to cite this article:
Kidwai MM, Azad S, Radhakrishnan S, Garg A, Yadav S, Kumar A. Echocardiographic Assessment of Right Ventricular Systolic Function in Postoperative Tetralogy of Fallot Patients with Special Emphasis on Right Ventricular-Global Longitudinal Strain. J Indian Acad Echocardiogr Cardiovasc Imaging 2022;6:100-7

How to cite this URL:
Kidwai MM, Azad S, Radhakrishnan S, Garg A, Yadav S, Kumar A. Echocardiographic Assessment of Right Ventricular Systolic Function in Postoperative Tetralogy of Fallot Patients with Special Emphasis on Right Ventricular-Global Longitudinal Strain. J Indian Acad Echocardiogr Cardiovasc Imaging [serial online] 2022 [cited 2022 Oct 3];6:100-7. Available from: https://jiaecho.org/text.asp?2022/6/2/100/338245




  Introduction Top


Postoperative follow-up of tetralogy of Fallot (TOF) patients is mainly done by transthoracic echocardiography with the focus on the assessment of right ventricular (RV) systolic function as RV dysfunction is strongly associated with poor prognosis in these patients.[1] Assessment of RV systolic function is done using RV fractional area change (RV-FAC), tricuspid annular plane systolic excursion (TAPSE), and tricuspid valve tissue Doppler s' velocity (TV-TDI s' velocity). However, none of these are free from limitations. The measurement of RV ejection fraction (EF) using two-dimensional echocardiography is not feasible as the analysis models make certain geometric assumptions which are not applicable to the complex-shaped RV.[2] In postoperative TOF patients, the RV geometry becomes even more complex due to the abnormal volume loading conditions, residual stenosis, presence of fibrosis, and scarring, which make these geometrical assumptions even less accurate when we compare it with cardiac magnetic resonance imaging (MRI) derived RV-EF.[3] Currently, cardiac MRI is the gold standard technique for the assessment of biventricular size and systolic function.[4] RV-global longitudinal strain (RV-GLS) is a relatively new parameter and has been shown to correlate best with cardiac MRI among the various surrogate parameters of RV systolic function.[5] RV-GLS detects subclinical changes in function and predicts adverse outcomes in adults with heart failure.[6] Postoperative TOF patients have shown low RV-GLS despite normal cardiac MRI-derived RV-EF.[7] Despite its potential benefits, RV-GLS is not being used in daily clinical practice to assess RV systolic function in postoperative TOF patients. In addition, the trend of RV systolic function as the postoperative time increases has not been studied using RV-GLS. Thus, the purpose of this study was to assess RV systolic function in postoperative TOF patients, with special emphasis on RV-GLS and to study the changes in the same over a period of 1 year.


  Materials and Methods Top


Ethics

The study was undertaken after ethical clearance from the institute's ethical committee. The purpose and design of the study were explained to the patients or the consenting family members. The parents or consenting family members were informed that they could withdraw from the study at any time without having reasons for the same. The confidentiality of information obtained was maintained and revealed only to the doctor/auditor involved in the study and to regulatory authorities. The study was conducted on ethical guidelines for Biomedical Research on human subjects given by Central Ethical Committee on human research, New Delhi, in addition to principles enunciated in the “Declaration of Helsinki.”

Design of study and participants

It was a single-center prospective, observational study, in which eligible patients were included from the outpatient department.

Aims and objectives

  • To assess the role of RV-GLS in the assessment of RV systolic function in postoperative TOF patients
  • To evaluate the correlation of RV-GLS with RV-FAC, TAPSE, and TV-TDI s' velocity
  • To assess the trend of RV systolic function over a period of 1 year
  • To evaluate the effect of severe pulmonary regurgitation (PR) on RV systolic function.


Inclusion criteria

Postoperative TOF patients <18 years old who had undergone total correction surgery at least 6 months ago were included in the study. All the surgeries were done by the same surgeon and the type of surgery included both those with and without transannular patch (TAP). None of the patients had DiGeorge syndrome.

Exclusion criteria

TOF patients with associated significant atrioventricular valve regurgitation or any systemic condition which could affect the cardiac function.

Echocardiographic evaluation

  • Clinical variables were recorded (patient's age, weight, height, and duration of the postoperative follow-up)
  • The degree of PR was measured and graded as mild, moderate, and severe depending on the origin of the diastolic backflow in the parasternal short-axis view[8]
  • RV-FAC was measured using RV-focused apical four-chamber view. In the pediatric age group, the American Society of Echocardiography in 2005[9] described the normal range for RV-FAC, and a value of <32% was taken as suggestive of RV systolic dysfunction
  • TAPSE was measured using M-mode echocardiography. Normative values are available for the pediatric population age wise[10]
  • TV-TDI s' velocity was measured by recording the peak systolic velocity at the lateral tricuspid valve annulus using TDI. It was measured at end-expiration and/or the average of ≥5 consecutive beats was taken. Normative TV-TDI s' velocity data for the pediatric age group have been published[11]
  • RV-GLS: There are two types of RV-GLS measurements. They are- RV-GLS total and RV-GLS free wall. RV-GLS total includes the strain value of the ventricular septum added to RV-GLS free wall. The exclusion of the interventricular septum in RV-GLS free wall is based on the consideration that it reflects both right and left systolic function. However, systolic interventricular dependence greatly contributes to RV longitudinal shortening. In fact, a muscle fiber continuity exists between the right and left ventricle (LV), and this evidence represents the anatomic basis of RV free wall traction secondary to LV contraction. It is seen that RV-GLS free wall and RV-GLS total can be similarly used to stratify patient prognosis, although RV-GLS total seems to have a slightly greater prognostic power.[12] In this study, RV-GLS total was measured. Frame rate was kept between 60 and 90/min, and RV-focused apical four-chamber view was used. The machine used was PHILIPS EPIQ 7 machine, and software was QLAB (LV strain software). Because the RV has a different anatomy and physiology from the LV, validation studies are needed to use the LV software for the analysis of RV-GLS. In a study which analyzed intraoperative RV strain using LV-specific strain software commonly available on the echo machine (Phillips Qlab Chamber Motion Quantification, version 10.7 Phillips Medical Systems, Andover), it was seen that RV-GLS correlated with offline RV strain measurements using RV-specific strain software (Epsilon Echo Insight, version 2.2.6.2230, Ann Arbor).[13] Furthermore, in a study done by Gao et al., in 2018, the RV-GLS was analyzed in a vendor-neutral platform. This study showed that it was feasible to assess RV strain across multiple platforms in a reproducible and reliable fashion.[14] In a meta-analysis, the normal mean values for RV-GLS total in the pediatric population were − 23.56% to − 31.90% (mean: −28.20%; 95% confidence interval [CI], −31.52% to −24.88%), so a value of <−23.5% was taken as RV systolic dysfunction.[15]


Review after 1 year

Detailed echocardiography as done in the first follow-up was done after 1 year.

All the patients were divided into three groups based on the duration since total correction for analysis of outcomes and RV function as follows:

  • Group A: 6 months–5 years
  • Group B: 6–10 years
  • Group C: >10 years.


To study the effect of degree of PR on RV systolic function, the patients were divided into two groups, i.e., those with severe PR and those with mild to moderate PR.

Statistical methods

Descriptive statistics for categorical variables were reported as frequency and percentage, whereas continuous variables were reported as mean and standard deviations. Comparisons between the echocardiographic parameters measured 1 year apart were carried out using paired t-test. For the statistical comparison between the three groups, ANOVA test was applied. For the comparison of RV function between patients with severe PR and mild-to-moderate PR, unpaired t-test was used. Pearson correlation coefficient was used to assess the correlation of RV-GLS with RV-FAC, TAPSE, and TV-TDI s' velocity. P < 0.05 was considered statistically significant.


  Results Top


Patient characteristics

In this study, a total of 103 patients were enrolled who underwent total correction for TOF and met the inclusion criteria during the first follow-up. Only ninety patients came for the second follow-up, so ninety patients were analyzed. Out of these ninety patients, 71 were male (78.8%) and 19 (21.2%) were female [Table 1]. The mean age at total correction was 3.06 ± 2.94 years with the minimum age being 5 months and maximum being 15 years [Table 1]. A total of 4 (4.4%) patients underwent a total correction in the adolescent age group. TAP was needed in 57 (63.3%) patients [Table 1].
Table 1: Demographics of the patient population

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Right ventricular systolic dysfunction at the two follow-up visits

The total number of patients with RV systolic dysfunction was 8.9% when RV-FAC was used and this proportion was significantly higher when other parameters were used as shown in [Table 2]. The mean RV-GLS was −23.01% ± −3.03% and −23.21% ± −3.29% at the two follow-up visits, respectively, as shown in [Table 3].
Table 2: Total number of patients with right ventricular systolic dysfunction parameter-wise

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Table 3: Right ventricular systolic function at the first and second follow-up

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Impact of the degree of pulmonary regurgitation on right ventricular systolic function

As shown in [Table 4], patients with severe PR had worse RV systolic function as compared to those with mild-to-moderate PR at both the follow-up visits. These differences were statistically significant when using RV-FAC (P = 0.01 and < 0.01) and RV-GLS (P = 0.02 and 0.03) but not using TAPSE and TV-TDI s' velocity.
Table 4: Impact of degree of pulmonary regurgitation on right ventricular systolic function

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Group wise analysis of patients

Group A comprised 34 (38.0%) patients whose time since total correction was 6 months to 5 years [Table 1]. Of them 4 (11.8%) patients underwent total correction at adolescent age. The mean age was 4.92 ± 4.9 years and 5.86 ± 4.0 years at the first and second follow-up visits, respectively, as shown in [Table 5]. There was a statistically significant increase in RV systolic function over a period of 1 year in group A patients as shown in [Table 5].
Table 5: Characteristics of patients in Group A at the first and second follow-up

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Group B included 26 (28.9%) patients who underwent total correction between the past 6–10 years [Table 1]. The mean age at the first follow-up was 8.05 ± 1.34 years and was 9.05 ± 1.34 years as at the second follow-up [Table 6]. Group C included a total of 30 (30.3%) patients whose time since total correction is more than 10 [Table 1]. The mean age at the first follow-up was 14.4 ± 1.88 years and was 15.36 ± 1.92 years at the second follow-up [Table 7]. The RV-GLS, RV-FAC, TAPSE, and TV-TDI s' velocity did not show any statistically significant difference between the two follow-up visits in group B and group C patients [Table 6] and [Table 7].
Table 6: Characteristics of patients in Group B at the first and second follow-up

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Table 7: Characteristics of patients in Group C at the first and second follow-up

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Comparison of right ventricular systolic function among the three groups

It was seen that there was a statistically significant difference in RV systolic function (RV-GLS, RV-FAC, TAPSE, and TV-TDI s' velocity) among the three groups, suggesting a decline in RV systolic function as the time since total correction increased [Table 8].
Table 8: Comparison of parameters of right ventricular systolic function among the three groups

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Correlation among different measures of right ventricular systolic function

RV-GLS had the best correlation with RV-FAC with a P < 0.01, suggesting a strong positive correlation at both the follow-up visits as shown in [Table 9]. There was a weak positive correlation of RV-GLS with TAPSE and TV-TDI s' velocity [Table 9].
Table 9: Correlation of right ventricular global longitudinal strain with other parameters of systolic function

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  Discussion Top


Number of patients with right ventricular systolic dysfunction

In this prospective observational study, the number of patients with RV systolic dysfunction was very less when RV-FAC was used as compared to when TAPSE and TV-TDI s' velocity were used as shown in [Table 2]. Similar findings were seen in a study done by Nair et al., in 2013[16] in postoperative TOF patients, where all patients had normal RV systolic function when assessed by RV-FAC, but all patients had asymptomatic RV dysfunction as assessed by TV-TDI s' velocity. This is because in patients with RV hypertrophy, as in TOF patients, the radial fibers predominate over the longitudinal fibers; thus those parameters which solely measure longitudinal function (TAPSE and TV-TDI s' velocity) will show falsely low values.[17] Thus, RV-FAC (which measures both radial and longitudinal function) becomes a more reliable indicator of RV systolic function than TAPSE and TV-TDI s' velocity, both of which should be reserved for individual longitudinal follow-up.

The role of right ventricular-global longitudinal strain in the assessment of right ventricular systolic function

We found that RV-GLS was a feasible tool for the assessment of RV systolic function in postoperative TOF patients. Only seven studies could be found which used RV-GLS in postoperative TOF pediatric patients [Table 10]. Moreover, only one study done by DiLorenzo et al., 2018,[18] assessed the trend of RV-GLS in the pediatric age group. Hence, to the best of our knowledge, this is the only Indian study which analyzed RV-GLS in postoperative TOF patients and observed its trend over a period of 1 year. Furthermore, the sample size in our study was more than any previous study. The mean RV-GLS measured in the previous studies mentioned above and in our study were different since the machine and the software used were different, which could be a source of error. However, as seen in the studies done by Silverton et al., in 2019[13] and Gao et al., in 2018,[14] it is feasible to assess RV strain across multiple platforms in a reproducible and reliable fashion, even using LV specific software as was done in this study.
Table 10: Various studies which used right ventricular global longitudinal strain in postoperative tetralogy of Fallot patients

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The mean RV-GLS in our study was −23.01% ± −3.03% at the first follow-up, and it was −23.21% ± −3.29% at the second follow-up for the whole study group [Table 3]. Normal mean values for RV-GLS total range from −23.56% to − 31.90% (mean: −28.20%; 95% CI: −31.52% to −24.88%) in healthy children.[12] Thus, postoperative TOF patients have lesser mean RV-GLS values than healthy children. Similar findings were also seen in the studies done by DiLorenzo et al.[18] and Li et al.[19]

We also did a correlation analysis of RV-GLS with other parameters of systolic function. There was a strong positive correlation of RV-GLS with RV-FAC at the first follow-up (r = 0.41, P < 0.01) and second follow-up visits (r = 0.67, P < 0.01), but only a weak positive correlation of RV-GLS with TAPSE and TV-TDI s' velocity [Table 9].

Thus, we can conclude that RV-FAC and RV-GLS are the parameters which reliably quantify RV systolic function and have a good correlation with each other. However, in our study, RV-GLS showed systolic dysfunction in a significantly higher number of patients than RV-FAC as shown in [Table 2]. Thus, we hypothesize that RV-GLS detects systolic dysfunction before the RV-FAC starts to decrease. This hypothesis is supported by a study done by Scherptong et al., in 2009,[22] which showed that, although RVEF on cardiac MRI remained unchanged, echo-derived RV-GLS already decreased. They also reported that RV GLS continued to deteriorate in serial assessments despite preserved RVEF, suggesting that regional wall-motion evaluations may detect early findings of subtle RV dysfunction. Thus, RV-GLS is more sensitive to detect changes in RV performance before RV-FAC starts to decline, and it should be used for serial monitoring of RV systolic function so that timely cardiac MRI can be planned.

Impact of degree of pulmonary regurgitation on right ventricular systolic function

At both the follow-up visits, it was seen that the RV systolic function was worse in those patients who had severe PR as compared to those who had mild to moderate PR. This difference was statistically significant only with RV-FAC and RV-GLS [Table 4]. Eyskens et al., 2010[23] and Li et al., 2016[19] had similarly showed that severe PR was associated with reduced RV strain and strain rate. Thus, we can conclude that the presence of severe PR has a negative impact on RV function which was better appreciated by RV-FAC and RV-GLS in this study.

Comparison of right ventricular systolic function group wise

There was a statistically significant decline in all the parameters of RV systolic function at both the follow-up visits, as the postoperative time since total correction increased [Table 8]. This finding reflects the deleterious impact of postoperative changes on RV systolic function in these patients.

Trend of right ventricular systolic function over a period of 1 year

In group A patients, on comparing the RV systolic function between the first and second follow-up, a statistically significant increase was seen over a period of 1 year [Table 5]. However, in group B and C patients, the RV systolic function was comparable between the two follow-up visits with no statistically significant difference [Table 6] and [Table 7].

This increase in RV systolic function in the group A as compared to group B and C can be explained by the fact that the patients in group A were in the 6 months to 5 years since total correction group which is the early postoperative period for the majority of the patients. It is expected that the RV function would be low during this early post-operative period and would recover as the effect of postoperative hemodynamics wore off, which took almost 1 year in our study. This was followed by a period of slow and gradual decline in the RV systolic function.

Limitations

Our study had several limitations which merit attention. The RV systolic function as assessed by the various surrogate parameters used in this study were not compared with cardiac MRI-derived RV-EF which is the gold standard. The GLS software, that is, originally designed for LV was applied to the RV analysis in the present study. The RV-focused apical four-chamber view is echocardiographer dependent and may be a source of error. Finally, this was a single-center study, and surgical techniques could differ from center to center which might impact postoperative RV function.


  Conclusion Top


Echocardiographic assessment of RV systolic function in postoperative TOF should not be perfromed by relying on a single parameter as none is free from limitations. RV systolic function is reliably predicted by RV-GLS and RV-FAC, especially in patients with severe PR which has a negative impact on RV systolic function. TAPSE and TV-TDI s' velocity should be reserved for longitudinal follow-up. Additional benefit of RV-GLS was that it detected regional myocardial dysfunction even when the RV-FAC was normal. Thus, RV-GLS should be included in the assessment of RV systolic function in postoperative TOF patients as it detects preclinical RV dysfunction before RV-FAC starts to reduce.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10]



 

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