Introduction

In children with dilated cardiomyopathy, left ventricular twist–untwist mechanics may serve as useful tools for quantifying systolic and diastolic function. The aim of this study was to explore rotational parameters in paediatric dilated cardiomyopathy, since such studies in this population are lacking. We hypothesised that dilated cardiomyopathy patients would exhibit altered rotational mechanics (decreased apical and basal rotations and twist) and may present with reversed apical rotation. ^{Reference Kanzaki, Nakatani, Yamada, Urayama, Miyatake and Kitakaze1}

This study was a cross-sectional, single-centre prospective study and included 23 patients with dilated cardiomyopathy between 10 months and 18 years. These were compared with 10 age-and sex matched controls. The cause of dilated cardiomyopathy was heterogeneous, which included idiopathic dilated cardiomyopathy (31%), Duchenne muscular dystrophy (26%), myocarditis (13%), vascular causes (ischaemia or anomalous origin of coronary arteries) (17%), and other causes (13%). The average ejection fraction was 41%. Patients continued their regular medications. Eighty-seven percent were taking angiotensin-converting enzyme inhibitors/angiotensin II receptor antagonists, 74% beta-blockers, 9% digoxin, and 65% diuretics. None had intracardiac defibrillators or pacemakers. Additionally, a follow-up of only clinical outcomes for the same cohort of dilated cardiomyopathy patients was conducted after a mean follow-up period of 6 years.

Echocardiographic images of the cardiac apex and base were acquired and processed using two-dimensional speckle-tracking. Measurements of rotational mechanics (apical rotation, basal rotation, twist, torsion, and untwist) were obtained. During systole, two rotational patterns were identified in patients with dilated cardiomyopathy. In the first group, 10 patients presented with preserved counterclockwise (positive value) apical rotation but with a significant decrease in all peak parameters, including apical, basal rotation, twist, and torsion (Figure 1( a ) and supplemental table), compared to controls. They also manifested a much lower peak untwist rate (Figure 2( a ) and supplemental table). A second group of 13 patients (57% of dilated cardiomyopathy cohort) exhibited reverse apical rotation, a clockwise (negative value) rotation of both the apex and the base (Figure 1( b )). This replaces the usual wringing motion of the left ventricle with a roller-pump-like motion. These results were not comparable to controls.

Figure 1.

( a ) Graph comparing apical and basal rotation of a representative DCM patient (non-reverse apical rotation) and age-and sex-matched control. The rotational parameters are greatly decreased in the DCM patient. ( b ) Graphical representation of apical rotation, basal rotation, and twist of a representative DCM patient with reverse apical rotation (RAR). The apex rotation is negative, as is the basal rotation. AVC: Aortic valve closure. MVO: Mitral valve opening.

Figure 1. Long description

Two line graphs depict rotational parameters in children with dilated cardiomyopathy. Panel A shows a comparison of apical and basal rotation between a representative DCM patient and an age-and sex-matched control. The x-axis represents time in milliseconds, and the y-axis represents rotation in degrees. The graph includes four lines: apex control in blue, base control in red, apex DCM in yellow, and base DCM in orange. The DCM patient exhibits greatly decreased rotational parameters compared to the control. Panel B illustrates apical rotation, basal rotation, and twist of a representative DCM patient with reverse apical rotation. The x-axis represents time in milliseconds, and the y-axis represents rotation in degrees. The graph includes three lines: apex in blue, base in orange, and twist in gray. The apex rotation is negative, as is the basal rotation. Key events such as aortic valve closure and mitral valve opening are marked on the graphs.

Figure 2.

( a ) Comparison of twist and untwist rates in a representative DCM patient and age-and sex-matched control. The twist velocities are lower in the DCM group. AVC = aortic valve closure indicating 100% of systole. ( b ) Torsion/RDi loop of a representative DCM patient and age-and sex-matched control. The blue arrow indicates the change in the slope of the systolic limb in DCM. The area of the DCM loop is significantly smaller, which can be interpreted as a lower amount of stored potential energy compared to controls. AVC = Aortic valve closure, ED = End-diastole.

After an average follow-up of clinical outcomes beyond 6 years, more patients from the reverse apical rotation group experienced increased incidence of arrhythmias including supraventricular tachycardia, non-sustained ventricular tachycardia, atrioventricular block and ventricular tachycardia/fibrillation (62% in reverse apical rotation versus 20 % in non-reverse apical rotation), an increased incidence of heart failure leading to hospitalisation (23% in reverse apical rotation versus 0% in non-reverse apical rotation), higher rate of intracardiac device placement (30% in reverse apical rotation versus 0% in non-reverse apical rotation), and higher incidence of death (46% in reverse apical rotation versus 10% in non-reverse apical rotation). The low number of patients in each group precluded meaningful subgroup statistical analysis.

Additionally, torsion/radial displacement-indexed loops were developed (Figure 2( b )). The slope of the systolic limb of this loop is highly linear and quite sensitive to inotropic changes, whereas the torsion/radial displacement-indexed loop itself provides composite information of coupling of systolic and diastolic events, along with simultaneous changes in left ventricle dimensions. Consequently, area enclosed by torsion/radial displacement-indexed loop has been compared with the concept of a pressure–volume loop, and area enclosed by the loop can be interpreted as a surrogate of stroke work and stored potential energy. These concepts have been described in our previous work. ^{Reference Di Maria, Caracciolo, Prashker, Sengupta and Banerjee2,Reference Montero, Numata and Kauffman3} Dilated cardiomyopathy patients showed a significant decrease in the slope and the area of the loop (Figure 2( b )).

During ventricular twisting, energy is stored in myofibres like a wound-up spring. Notomi et al. speculated that this potential energy is converted into kinetic energy during early diastole, similar to the release of a wound-up spring, resulting in higher untwist rates leading to rapid suction of blood into the left ventricle, during isovolumic relaxation. ^{Reference Notomi, Popovic and Yamada4}

As dilated cardiomyopathy progresses in adults, the helical fibres start changing into a more horizontal configuration as the heart becomes more spherical. Consequently, apical rotation begins to decrease and even reverse. ^{Reference Popescu, Beladan and Călin5} Instead of wringing during contraction, the left ventricle assumes a roller pump-like motion, which conserves potential energy less well than those patients with a more helical orientation of myofibres (Figure 2( a )).

In contrast with adults, apical rotation in children has a more dominant role in systolic function, such that apical myofibres may serve as the functional reserve or the “engine” of the left ventricle. ^{Reference Di Maria, Caracciolo, Prashker, Sengupta and Banerjee2} One of the most important findings in our study is the high incidence of reverse apical rotation in children with dilated cardiomyopathy. The lack of association between rotational pattern and left ventricular dimensions or ejection fraction suggests that these abnormalities may reflect myocardial mechanical alterations that precede or occur independently of changes detected by conventional echocardiographic parameters. Previous studies in adults indicate that there is a correlation between ventricular fibrosis and the degree of reversal of apical rotation. Those who exhibited low apical rotation presented with a greater degree of fibrosis detected by MRI. Fibrosis was even higher in those with reverse apical rotation, which may indicate a poorer prognosis. ^{Reference Karaahmet, Gürel and Tigen6}

Torsion/radial displacement-indexed loops are a graphical representation of systolic–diastolic coupling. Given that dilated cardiomyopathy patients have a decrease in the area of the loop, we speculate that there is a lower amount of stored potential energy in the myocardium of dilated cardiomyopathy patients (Figure 2( b )). Therefore, patients with dilated cardiomyopathy and, more significantly, those who exhibit reverse apical rotation, suffer from a global decrease in systolic and diastolic coupling.

Important limitations of this study are a small sample size that precluded in-depth statistical analysis and the heterogeneity of DCM patients. In previous studies from our laboratory, strong intraclass correlation coefficients for intra-and interobserver variabilities for rotational indices have been established. ^{Reference Yubbu, Kauffman and Calderon-Anyosa7–Reference Nawaytou, Montero and Yubbu9} Therefore, these were not repeated.

In conclusion, apical rotation decreases in dilated cardiomyopathy may evolve into reverse apical rotation in a subset of children. This, in turn, may result in reduced ventricular untwisting and suction. Based on previous studies in adults, changes in rotational function may potentially serve as predictors of myocardial fibrosis. Our study represents a small pilot study. Future larger studies correlating rotational mechanics with myocardial fibrosis are warranted to elucidate mechanisms underlying the associations identified herein, improve their generalisability, and strengthen their prognostic implications in paediatric patients with dilated cardiomyopathy.