Left ventricular rotational abnormalities in adult patients with congenital heart disease late after Fontan procedure: detailed analysis from the CSONGRAD Registry and MAGYAR-Path Study

Introduction

In the last decades, a trend can be observed that, due to more appropriate diagnostic and treatment procedures, a large number of patients with congenital heart diseases (CHDs) live into adulthood. The Fontan procedure (FP) has been introduced in 1971 as a cavopulmonary connection and is used in children with univentricular heart (UH) as a surgical palliation diverting blood flow from the caval veins to the pulmonary artery (1). Since the original description, several modifications have been introduced and have spread allowing the FP to be used in several CHDs over complex situations, for instance not only in the absence of a heart valve [mitral/tricuspid atresia (TA)], but also in the presence of an abnormality of a heart chamber [hypoplastic left heart syndrome/hypoplastic right heart syndrome (HRHS)] (1-4).

The left ventricle (LV) is the central engine of the heart, it is made up of muscle bands located endocardially and epicardially, perpendicular to each other, that is muscle fibers running obliquely (5-9). However, these fibers not only contract/relax during the cardiac cycle, but have a spatial rotational mechanics as well meaning that the LV apex rotates in counterclockwise direction, while the LV base rotates in clockwise direction resulting in a towel-wringing-like motion called LV twist in systole (5-9). The newly developed three-dimensional (3D) speckle tracking echocardiography (3DSTE) is a proven suitable and validated method to quantify LV rotations and consequent LV twist (10-13). Since little information is available on the cardiac mechanics of FP-operated patients, the present study aimed to determine 3DSTE-derived basal and apical LV rotations in adult patients with CHD mainly affecting the right heart late after FP (14). We present this article in accordance with the STROBE reporting checklist (available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-503/rc).

Methods

Patient population

The present study comprised 15 CHD patients late after FP with a mean age of 32.6±8.0 years (5 males). Two patients had bidirectional Glenn procedure (BDGP) as the only and final procedure. In case of modified Kreutzer procedure (MKP; 3 patients), only BDGP was performed previously. Five out of 8 patients following total cavopulmonary connection (TCPC) had previous BDGP, while 3 subjects had TCPC at first. The essence of the MKP is that the systemo-pulmonary connection is created with wide base between the right atrial (RA) appendage and the pulmonic trunc. In case of traditional FP, the shunt is created between the free wall of the RA and the pulmonary artery. Clinical data originate from the CSONGRAD Registry [Registry of C(S)ONGenital caRdiAc Disease patients at the University of Szeged], which has been created to summarize clinical variables and parameters of all CHD patients treated and followed-up at the Departments of Pediatrics, Cardiology and Heart Surgery at the University of Szeged, Hungary since 1961 (15). All subjects were involved in the study and followed-up, who were alive and willing to participate in this study. Their results were compared to a group of 25 age- and gender-matched healthy individuals (mean age: 33.4±11.9 years, 8 males). They had no known disorder, pathological condition, used any drug, were obese or athlete, which could affect the results, and their laboratory, electrocardiographic (ECG) and echocardiographic results proved to be normal. In all CHD patients and healthy individuals, a complete two-dimensional (2D) Doppler echocardiography and 3DSTE were performed according to recent guidelines and practices. This retrospective cohort study is part of the Motion Analysis of the heart and Great vessels bY three-dimensionAl speckle-tRacking echocardiography in Pathological cases (MAGYAR-Path) Study, which aimed to assess disease-specific 3DSTE-derived features of abnormalities in cardiac mechanics in certain CHDs (‘Magyar’ means ‘Hungarian’ in Hungarian language). The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Institutional and Regional Human Biomedical Research Committee of University of Szeged approved the study on a registration number 71/2011, and informed consent was given by all participants.

2D Doppler echocardiography

All healthy subjects and CHD patients late after FP underwent a complete 2D Doppler echocardiographic assessment, which included measurement of left atrial and LV dimensions and measurement of LV ejection fraction (EF) according to the Simpson’s method. During all examinations, a Toshiba Artida^TM echocardiography tool (Toshiba Medical Systems, Tokyo, Japan) attached to a PST-30BT (1–5 MHz) phased-array transducer was used. Valvular regurgitation and stenosis were detected and quantified in accordance with recent guidelines (16).

3DSTE

In all cases, 3DSTE was performed after the 2D echocardiographic examination. For this the same Toshiba Artida^TM echocardiographic device was used, but the transducer was replaced by a 3D capable PST-25SX matrix-array transducer. 3DSTE was performed in 2 steps (10-13). Firstly, 3D echocardiographic datasets were acquired digitally the subjects/patients being in left lateral decubitus position by the 3D-capable transducer from the apical window. For optimal images, 6 subvolumes were acquired using ECG-gating during a single breath-hold. The subvolumes were stitched together by the software automatically to create a complete full volume 3D echocardiographic dataset.

As a second phase, offline data analysis was performed at a later date using the vendor-provided 3D Wall Motion Tracking software version 2.7 (Ultra Extend, Toshiba Medical Systems, Tokyo, Japan). The aim of this analysis was the creation of a virtual 3D cast of the LV, on which volumes and rotational parameters of the LV could be calculated respecting the cardiac cycle. Optimal typical apical longitudinal views and basal, midventricular and apical cross-sectional planes were selected and mitral annular-LV edges were defined together with the endocardial surface of the LV apex, then a sequential analysis helped the creation of the 3D virtual LV model (Figure 1). The following features of the LV rotational mechanics have been determined: clockwise basal LV rotation (in degrees), counterclockwise apical LV rotation (in degrees), LV twist (net difference of LV apical and basal rotations in degrees) and time-to-peak LV twist (in milliseconds) were calculated (17-19). When basal and apical LV rotations were in the same clockwise or counterclockwise direction, LV ‘rigid body rotation’ (RBR) were present and LV twist could not be calculated, only the difference between LV apical and basal rotations called the LV apico-basal gradient could be determined (20).

Figure 1 3D speckle-tracking assessment of LV apical and basal rotations from an LV focused view in a patient. Apical four-chamber (A) and two-chamber views (B) and basal (C₁), midventricular (C₂) and apical (C₃) short-axis views are demonstrated, that can be automatically extracted from the acquired 3D echocardiographic database. (D) 3D model of the LV, while (E) LV volumetric parameters and ejection fraction. (F) Apical and basal LV rotations. Yellow arrow represents counterclockwise LV apical rotation, while dashed yellow arrow represents clockwise basal LV rotation. 2D, two-dimensional; 3D, three-dimensional; EDV, end-diastolic volume; EF, ejection fraction; ESV, end-systolic volume; LA, left atrial; LV, left ventricular; RA, right atrial; RV, right ventricular.

Statistical analysis

Both continuous and categorical variables are presented as mean ± standard deviation or number/percent format, as appropriate. P<0.05 was considered to be statistically significant. Student’s t-test, Mann-Whitney-Wilcoxon test, one-way analysis of variance (ANOVA) and Fischer’s exact test were used where appropriate. Pearson’s correlation coefficients were calculated for numerical correlations. MedCalc software (Medcalc, Mariakerke, Belgium) was used during statistical analyses.

Results

Clinical and demographic data

The FP groups of CHD patients proved to be inhomogeneous regarding the type of the procedure and the ventricular anatomy (Tables 1,2). Regarding the type of the procedure, BDGP, MKP and TCPC were performed as final palliative procedures in 2, 3 and 8 patients, respectively. Regarding the ventricular anatomy of CHD, HRHS, a condition in case of which the right ventricle is too small or do not function properly, UH in case of which the patient has a single ventricle or a rudimentary, non-functional right ventricle and TA were present in 3, 5 and 5 patients, respectively. Distribution of procedures and diagnoses is presented in Table 2. At the time of the first procedure, the average age was 8.5±5.3 years in the FP patients, while 22.8±6.2 years elapsed between the procedure and the 3DSTE in these patients.

LV dimensions

Although aggregated data did not show differences between FP patients and healthy controls, subgroup analyses confirmed differences. With 2D echocardiography, regarding the procedure, MKP patients have tendentiously larger LV end-diastolic diameter (EDD) with thicker LV walls compared to the other groups. Regarding the ventricular anatomy, UH patients have tendentiously larger LV-EDD with thicker LV walls compared to the other groups. Results of detailed analysis are presented in Table 3. None of the FP patients and matched healthy controls showed larger than grade 1 valvular regurgitation or had valvular stenosis on any valves.

With 3DSTE, regarding the procedure, only MKP patients showed normal LV-EF due to increased LV end-diastolic volume (EDV), other groups showed mildly reduced LV-EF. With 3DSTE, regarding the ventricular anatomy, UH patients had the largest LV-EDV, but no differences were detected in mildly reduced LV-EF between the subgroups (Table 4).

LV rotational mechanics

Out of 15 FP patients, 2 subjects showed LV-RBR, one with clockwise LV-RBR (LV-cRBR) and one with counterclockwise LV-RBR (LV-ccRBR). The remaining 13 FP cases showed normally directed LV rotational mechanics. Data of these patient groups were managed separately.

LV-RBR

The LV-cRBR patient had HPRV who underwent BDGP, while the counterclockwise patient proved to have BDGP-corrected TA. 3DSTE-derived basal and apical LV rotations of the LV-cRBR patient proved to be 2.0 and 2.4 degrees with normal LV-EDV (90 mL), LV-ESV (36 mL), interventricular septum (IVS) (10 mm), LV posterior wall (PW) (10 mm) and LV-EF (60%). Basal and apical LV rotations of the LV-ccRBR patient proved to be −3.5 and −4.4 with normal LV-EDV (108 mL), LV-ESV (39 mL), IVS (8 mm), LV-PW (8 mm) and LV-EF (64%).

Normally directed LV rotational mechanics

On group level, FP patients had preserved basal LV rotation and reduced apical LV rotation resulting in tendentiously reduced LV twist compared to the controls. However, regarding the procedure, BDGP patients had larger basal LV rotation with preserved apical LV rotation resulting in increased LV twist compared to the controls. MKP and TCPC patients had preserved basal LV rotation and reduced apical LV rotation resulting in reduced LV twist compared to the controls. Regarding the ventricular anatomy, HRHS patients had larger basal LV rotation with preserved apical LV rotation resulting in increased LV twist compared to the controls. UH and TA patients had preserved basal LV rotation and reduced apical LV rotation resulting in reduced LV twist compared to the controls (Table 5).

Correlations

No linear correlation was seen between LV twist and LV-EF between the subgroups. No correlation was seen between LV apical rotation and LV-EF either.

Intra- and interobserver variability analysis

Intraobserver ICCs were 0.83, 0.82 and 0.84 for basal and apical LV rotations and LV twist, respectively. Interobserver ICCs proved to be 0.84, 0.83, and 0.84 for the same parameters, respectively.

Discussion

Although CHD patients represent a small proportion of all cardiology patients, their appropriate care and management are essential. The fact that the CHD patient group includes rare and diverse diseases, and that several invasive procedures have been used even within the same patient group in recent decades making the analysis of these patients more difficult. Moreover, some patients underwent several procedures including a palliation first and a definitive intervention at a later date. The FP is one of the palliative methods used for decades in CHD patients with a single functional ventricle (1-4).

Not only the invasive treatment procedures, but also the diagnostic possibilities have improved a lot in the meantime. New non-invasive imaging techniques such as 3DSTE have become widespread. 3DSTE combines the advantages of modern echocardiographic techniques: it is suitable for quantifying spatial wall movements with parameters like strains and rotations with the help of virtual 3D casts approaching reality. 3DSTE makes quantification of LV rotations together with volumes respecting the cardiac cycle possible in a non-invasive manner within a short time from a single 3D echocardiographic data acquisition by creating a virtual 3D model of the LV (10-13). The method is validated (21-23), normal reference values are published (17). The 3DSTE-derived LV-EF is known to be lower than that of by 2D echocardiography due to differences in the assessment of LV volumes respecting the cardiac cycle, as it has been found in this study (24).

Although limited clinical information is available, better understanding LV rotational mechanics in certain CHD group of patients could theoretically help in their diagnosis and treatment. In the present study, rare disorders with a limited number of cases late after FP were investigated. It could be stated that on a group level, LV-EF is reduced and is associated with tendentiously lower LV twist due to reduced apical LV rotation. However, differences between CHD patients varied based on the ventricular anatomy and on the procedure performed as well. Moreover, it could be assumed, that there is an effect of ventricular interaction between diagnosis groups. Presumably, the decreased LV-EDV in the HRHS and TA patients are due to a right ventricular cavity contributing to cardiac output. It is unclear what effect this may have on LV rotational function from a purely mechanical standpoint.

These findings are partially in agreement with previous results. In a retrospective analysis of cardiac magnetic resonance imaging study of 329 FP patients, abnormal torsional mechanics were found to be associated with death or need for heart transplantation (14). In another study, single LV and RV exhibited preserved torsion due to preserved or increased apical rotation (25). LV rotational abnormalities were found in other CHDs like in repaired tetralogy of Fallot (rTOF) (18,26,27) and in corrected dextro-transposition of the great arteries (dTGA) after atrial/arterial switch operation (19,28). LV-RBR was found to be present in some CHDs as well like in rTOF (18,26,27), dTGA (19), Ebstein’s anomaly (29), HRHS (30) and UH (31). In contrast, global LV torsion and twist were preserved in patients after successful coarctation repair (32). In the present study, only 2 out of 15 FP patients showed LV-RBR (13%), which is higher compared to the healthy population (6%) (20).

Limitation section

These are the most important study-related limitations:

• Both 2D Doppler echocardiography and 3DSTE were performed in all subjects. It is known that 2D echo-derived image quality is still superior compared to that of 3DSTE, which can be considered as the most important technical limitation of the presented findings (10-13).
• Limited number of CHD patients late after FP were included in the present study due to the rarity of these disorders. It was not possible to involve more patients, all subjects from the CSONGRAD Registry, who are alive and willing to participate have been included (15).
• In addition, within the last few decades the pre-natal echocardiographic diagnosis of CHDs has made substantial progresses, there has been a dramatic decrease in birth incidence of UH patients most probably due to a corresponding increase in potential termination of pregnancy as demonstrated in a population-based study from 1977 to 2009 in Denmark (33). In a large single-center cohort with a 99% follow-up rate, the 20-year estimate for survival with intact Fontan circulation is 74%. Although early perioperative mortality has improved over time, late survival after FP has not changed appreciably during the past 2 decades (34). Further studies on a younger cohort could have resulted in more significant differences, but the above mentioned limitations make it difficult to enroll further patients in our study.
• Moreover, the patient group was not homogenous regarding the ventricular anatomy and the procedure. Therefore, statistical analysis between subgroups could not be performed, only tendencies could be detected.
• BDGP was performed in case of all CHD patients as the first intervention, but in most cases, treatment was completed with TCPC or MKP later. In the present study, the BDGP group consisted of patients in case of whom BDGP was the final operation and no TCPC or MKP was performed in these patients.
• Due to technically difficulties of echocardiographic assessment, traditional 2D echocardiographic parameters could not be measured in 2 UH patients.
• Although LV strain could have been measured from the same 3D echocardiographic dataset, their demonstration and analysis should have exceeded the possible framework and accordingly could be the topic of a further scientific work (10-13).
• It was not aimed to validate 3DSTE-derived LV rotational parameters due to their validated nature (21-23).
• No hemodynamic assessment was performed in case of our patients following the surgery.

Conclusions

In FP patients with CHD mainly affecting the right heart, on a group level, impaired LV-EF is associated with tendentiously lower LV twist due to reduced apical LV rotation, but characteristics of LV functional and rotational mechanics show substantial differences depending on the ventricular anatomy of CHD and the procedure performed.

Acknowledgments

None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editor (Harald Kaemmerer) for the series “Current Management Aspects in Adult Congenital Heart Disease (ACHD): Part VI” published in Cardiovascular Diagnosis and Therapy. The article has undergone external peer review.

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-503/rc

Data Sharing Statement: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-503/dss

Peer Review File: Available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-503/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://cdt.amegroups.com/article/view/10.21037/cdt-24-503/coif). The series “Current Management Aspects in Adult Congenital Heart Disease (ACHD): Part VI” was commissioned by the editorial office without any funding or sponsorship. The authors have no other 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 and Regional Human Biomedical Research Committee of University of Szeged, Hungary (No. 71/2011) and informed consent was taken from all individual participants.

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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