This study has demonstrated a spatiotemporal coupling between the left ventricular vortex ring and endocardial wall during diastole, implying that the healthy heart is tuned to accommodate vortex ring formation. Intracardiac vortex ring formation provides a stable, recurring and predictable flow phenomenon that may dictate and optimize cardiogenesis by providing endocardial shear forces. Failing, dilated hearts show dissociation between the vortex ring and endocardium, indicating the potential utility of vortex ring-derived metrics for quantification of cardiac health.

The effects of altered flow or cardiac loading conditions on cardiac development was investigated by Hove et al.5 and Sedmera et al.6, although the experimental setups did not enable the authors to distinguish which particular flow pattern was the driving force. We propose that the vortex ring is the hemodynamic blueprint for cardiac shape and that disruption of vortex ring formation leads to altered shear along the endocardial border. Blood flow is known to influence endothelial cell structure and alignment through membranous mechanotransducers7,8,9, which provides a mechanistic explanation for how vortex rings may influence ventricular dimensions by shear forces, activating cellular remodeling/growth programs until the ventricle conforms to the vortex dimensions. Indeed, congenital mitral valvular stenosis has been associated with abnormally small LVs27. Altering inflow conditions by ligation of the mitral valve annulus during cardiogenesis would enable validation of the proposed causal connection between inflow parameters and ventricular dimensions.

Vortex formation in humans is spatially more complex compared to water tank experiments14, as shown in Figs 2 and 3. The proximity to the endocardial walls means that the vortex ring will interact with and be deformed by ventricular structures. Both the asymmetry of the mitral valve apparatus and the presence of papillary muscles add to the lopsided and somewhat irregular appearance of the intracardiac vortex ring, complicating direct comparison with tank models20,28. These limitations notwithstanding, we found a very consistent ratio between the largest vortex ring diameter and mitral valve diameter in controls, but large differences between controls and some patients; and both groups showed discrepancies compared to the water tank experiments. Mitral valve area was similar between patients and controls, so an explanation for this discrepancy must reside elsewhere. It appears that the vortex ring of the healthy heart is deformed by its close proximity to the wall, so that maximum diameter is not attained and vortex ring growth is limited by ventricular dimensions, unlike in the dilated heart where the vortex ring can continue to grow throughout diastole, even after termination of the E-wave (Fig. 4a). At rest, therefore, the mitral valve is not fully utilized for vortex ring generation in the healthy heart. Instead, there may be a “reserve capacity” for vortex ring formation, which would allow for sustained energy-efficient mass transfer during demand for higher cardiac output. Given the close coupling between vortex ring border and left ventricular wall, the only way to significantly increase the diameter of the vortex ring during exercise is to increase the radius of the left ventricle – a phenomenon previously observed using both echocardiography29 and MRI30. Such an arrangement keeps wall tension low during extended periods of rest, while preserving the capability to quickly increase cardiac output when necessary.

Cardiac remodeling is typically triggered during periods of stress, such as physical exertion or a pathological increase in cardiac load. Therefore, vortex-wall interaction during exercise is of potential interest for remodeling mechanics. Conversely, the ratio between vortex ring and mitral annular diameter may be a key factor in cardiac suction-pump efficiency during exercise; if the vortex formation capacity is nearly fully utilized at rest (high ratio), LV filling is likely to be a limiting factor for exercise tolerance. Hence the fluid dynamics of the failing heart resides closer to the limit for how large a vortex can be formed. We predict that the ratio in healthy hearts will increase during vigorous exercise, reflecting the optimized relationship between dynamic valve and flow properties and chamber size.

Vortex-wall interaction may be an important consideration for the long-term performance of prosthetic valves; if the implanted valve is too small in relation to the LV or its valve leaflet orientation alters inflow direction relative to normal, it may substantially impair optimal vortex generation. Therefore, the opportunity exists for prosthetic valve implants to be tuned to the dimensions of the left ventricle in the exercise state, to ensure optimal vortex ring formation under conditions where it matters most.

The narrow physiological range of vortex ring size relative to chamber size (Fig. 4c) implies this ratio has potential to serve as an index of diastolic function. Currently, 4D PC-MR is the only imaging modality that allows for accurate LCS computations of the complex flow field within the human left ventricle. LCS are inherently insensitive to image noise and developments in graphical processing unit technology are rapidly shrinking computational times, increasing clinical availability. Although echo-determined VFR now includes diastolic chamber properties22, future studies should investigate whether vortex-ventricle coupling is further quantifiable by readily available clinical tools, e.g. transthoracic ultrasound with microbubbles15 or fully noninvasive Doppler technique31 and whether new indexes can augment or replace current clinical diastolic function parameters. For echocardiographic studies of vortex ring LCS, a two-dimensional approach may render significantly different results with small variations in placement of the acoustic beam due to the irregular appearance of the vortex ring and these inconsistencies should be meticulously evaluated. For example, assuming a linearly tapering vortex ring, as recently presented32, is not consistent with our observations. Detailed study of the spatial localization of the vortex ring in relation to the endocardium may hold further information than given here, especially in patients with pathologically altered ventricular geometry.

From an evolutionary standpoint, matching endocardial wall movement to vortex growth implies optimization of the suction pump attribute of the LV. Because maintenance of cardiac output is a prime evolutionary directive for survival, the optimization of LV size and motion to accommodate the largest possible vortex is accompanied by numerous biological advantages. Vortex formation converts and preserves linear momentum as angular momentum13,33 and thereby prevents fluid kinetic energy from being converted into increased pressure24. Energy-wise, an optimal vortex is therefore one that contains all the inflowing blood without formation of a trailing jet. In terms of energy expenditures, systolic stroke work far exceeds blood flow, so vortex energetics are likely of small importance for global systolic function34. However, it has recently been shown that the kinetic energy of the diastolic vortex ring is significantly altered in heart failure35, implying that altered vortex ring dynamics may be a factor in the development of diastolic dysfunction and elevated filling pressures. A large vortex ring relative to the chamber size will also distribute inflow energy throughout the entire ventricle, which minimizes endocardial stasis of blood and thereby prevents thrombus formation. In contrast, a small vortex ring relative to chamber endocardial dimensions will interact less with the ventricular blood, provide a lower degree of mixing of the blood and hence increase the risk for thrombosis. Thus, any rinsing effect is likely to be diminished in hearts with vortex-wall dissociation. In most patients, the vortex ring moved along the inferior and lateral wall, typically dissolving near the apex. This flow pattern has been connected to increased risk for thrombus formation10, as the anterior wall is not exposed to fast-moving blood.

In conclusion, we have shown that the spatiotemporal behavior of the healthy left ventricle is optimized to accommodate the formation of an evolving diastolic vortex ring. Diastolic vortex ring features and dynamics are consistent across a wide size range of healthy hearts but significantly disturbed in heart failure, which increases our understanding of how fluid dynamics is coupled to and governs cardiac shape and function. Vortex ring parameters carry implications for exercise physiology, cardiac surgery and design and implantation of prosthetic valves. Future studies should investigate vortex ring dynamics during exercise and examine the clinical utility of vortex ring-derived metrics. The vortex ring behavior of the right ventricle also merits further characterization16,24,36.