Vortex ring behavior provides the epigenetic blueprint for the human heart

Abstract

The laws of fluid dynamics govern vortex ring formation and precede cardiac development by billions of years, suggesting that diastolic vortex ring formation is instrumental in defining the shape of the heart. Using novel and validated magnetic resonance imaging measurements, we show that the healthy left ventricle moves in tandem with the expanding vortex ring, indicating that cardiac form and function is epigenetically optimized to accommodate vortex ring formation for volume pumping. Healthy hearts demonstrate a strong coupling between vortex and cardiac volumes (R(2) = 0.83), but this optimized phenotype is lost in heart failure, suggesting restoration of normal vortex ring dynamics as a new, and possibly important consideration for individualized heart failure treatment. Vortex ring volume was unrelated to early rapid filling (E-wave) velocity in patients and controls. Characteristics of vortex-wall interaction provide unique physiologic and mechanistic information about cardiac diastolic function that may be applied to guide the design and implantation of prosthetic valves, and have potential clinical utility as therapeutic targets for tailored medicine or measures of cardiac health.

Figure 1. Possible anatomical arrangements for intracardiac vortex ring generation.

(a) Vortex rings are formed by pulsatile flow through an aperture, such as flow from the left atrium (LA) to the LV through the mitral orifice. A large left ventricle can accommodate the full size of the vortex ring it generates, but the vortex cannot rinse the distant ventricular wall and prevent mural thrombus formation. Furthermore, large ventricles are poor suction pumps and have high wall tension which causes energy waste. (b) If the chamber is too small it cannot accommodate full vortex ring formation, and is therefore incompatible with efficient filling. (c) An optimized left ventricle enables energy-efficient filling by matching endocardial expansion to vortex ring expansion and formation, thereby facilitating rinsing at low pressure, and maintenance of low wall tension.

Figure 2. Flow patterns by Lagrangian Coherent Structures.

(a) The black water of the Rio Negro meets the muddy water of the Rio Solimoẽs outside Manaus, Brazil. The border separating flows of different origins (colored line) is, by definition, a Lagrangian Coherent Structure (LCS). The LCS persists for several kilometers and grows increasingly uneven and complex as eddies contribute to mixing of the two flows. Image modified from an original by NASA Earth Observatory, with permission. (b) Water tank experiment with LCS analysis of vortex rings. As water is injected from a nozzle into a tank, a symmetrical vortex ring forms (left), detaches and evolves (middle), then gradually breaks down into more complex flow patterns (right). (c) LCS showing vortex ring formation during filling of the LV. Healthy control (top), patient with ischemic cardiomyopathy (middle), and non-ischemic dilated cardiomyopathy (bottom). After the formative phase, the vortex ring evolved close to the endocardial border (red dotted line) in the control, gaining additional complexity compared to the water tank model. In the patients, vortex ring formation occurred without an obvious connection to the endocardium, and the vortex ring moved along the inferior LV wall towards the apex. LV, left ventricle; RV, right ventricle; LA, left atrium; Ao, aorta; *, vortex core.

Figure 3

(a) Short-axis midventricular slice showing cardiac anatomy. Arrowheads indicate the position of papillary muscles. (b) Corresponding LCS image. The vortex ring adapts to intracavitary structures, causing an irregular appearance. (c) LCS superimposed over anatomy. The yellow line shows the manual delineations of the vortex ring boundary. LV, left ventricle; RV, right ventricle.

Figure 4. Measurements of vortex ring parameters.

(a) Volume-time curves of one control and one patient. Vortex ring development was initially similar between patients and controls. In the patient, however, the vortex ring continued to grow independently of LV volume, leading to additional entrainment of ventricular blood. (b) Distance between vortex ring surface (LCS) and endocardium of the left ventricle (mean ± SD). In controls, the vortex ring boundary was in close proximity to the endocardium after the initial growth phase. The dilated ventricle displayed continuous evolution of the vortex ring throughout diastole. (c) Vortex ring volume at end-diastole was linearly correlated to LV end-diastolic volume in controls, and filled on average 53% of the ventricle. This implies that LV chamber size and motion are tuned to accommodate the vortex ring in healthy hearts regardless of total heart size. Conversely, patients demonstrate a loss of optimized vortex-wall interaction. (d) The ratio between peak vortex ring diameter and inlet orifice diameter in controls and patients was lower in controls, a consequence of the elongated shape of the vortex ring at rest. The ratios in patients were more scattered, consistent with lower remaining filling reserve.