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Am J Physiol Heart Circ Physiol 309: H1094 –H1096, 2015;
doi:10.1152/ajpheart.00483.2015.
Letter to the Editor
Letter to the Editor: Atrioventricular plane displacement is not the sole
mechanism of atrial and ventricular refill
Per M. Arvidsson,1 Marcus Carlsson,1 Sándor J. Kovács,2 and Håkan Arheden1
1
Department of Clinical Physiology, Lund University, and Lund University Hospital, Lund, Sweden; and 2Cardiovascular
Biophysics Laboratory, Cardiovascular Division, Washington University School of Medicine, Saint Louis, Missouri
Address for reprint requests and other correspondence: H. Arheden, Dept. of
Clinical Physiology, Lund Univ., 22185 Lund, Sweden (e-mail: hakan.
[email protected]).
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aging and have found numbers of 5-11% (4, 8). Total heart
volume diminishes during systole and recovers during diastole,
indicating that venous return to the heart is not temporally
matched to ventricular ejection (26, 29, 32). Furthermore,
THVV was found to increase and AVPD decreased during
moderate intensity supine exercise (30). For perfect constantvolume pumping, atrial filling must be matched to ventricular
ejection, but the atrial reservoir only houses 40 – 60% of the
ventricular stroke volumes (19, 20). The remaining blood, the
conduit fraction, is drawn from the veins through the atria
during the early rapid filling phase, seen in pulmonary venous
flow profiles as the D wave whose volume corresponds to the
total heart volume recovery during early diastole (5). The D
wave gives rise to the “crescent effect” as seen on cardiac MRI
(32), and its existence proves that the ventricular stroke volume
is not fully compensated by the pulmonary vein S wave; if
venous return to the heart was entirely balanced and driven by
AVPD, there would be no D wave. On average, 70% of atrial
filling occurs during systole, again incompatible with perfectly
constant-volume pumping (29). Furthermore, healthy volunteers display a 2- to 3-mm cardiac center of volume variation,
indicating that the heart shifts position over the cardiac cycle
(10). And, finally, the existence of cardiac ballistography, i.e.,
measurement of total body motion due to cardiac pumping,
demonstrates that the ejection and filling momentums of the
heart do not fully cancel each other out (28). Therefore, the
heart is not a perfectly balanced, self-reciprocating pump, nor
is it a perfect constant-volume pump. Rather, the contents of
the pericardial sac can be more accurately described as a
near-constant volume pump that changes by ⬃8% over the
cardiac cycle.
The importance of momentum conservation. Arutunyan next
concludes that “venous return to the chambers of the heart is a
momentum-driven process that is powered by ventricular contraction” and elucidates that “once forcefully accelerated, the
columns of blood in the veins will inertially continue to flow
toward the heart until the momentums of the columns are
negated by a mechanical or higher pressure barrier.”
Momentum has been suggested to contribute to ventricular
function in various ways. Noble (25) demonstrated in 1968 that
momentum contributes to ventricular ejection in dogs, and
Kilner et al. (21) postulated that momentum conservation in
organized, swirling blood flow within the heart might contribute to optimize cardiac function. This would benefit diastolic
filling, with the greatest potential benefit during exercise when
diastole is markedly shortened. In atrial blood, kinetic energy
(KE), a measure closely connected to momentum, is determined in part by AVPD during systole, but a negligible amount
of KE “spills over” from systole to diastole in the left atrium
[Arvidsson et al. (3), Figs. 3 and 6A]. Data from the same
article support that for the right heart, blood momentum may
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WE HAVE READ WITH GREAT INTEREST the recent Perspective by
Arutunyan (2), titled “Atrioventricular plane displacement is
the sole mechanism of atrial and ventricular refill,” in which
the author revisited important, and perhaps not well-known,
aspects of cardiac pumping physiology in an attempt to uncover a “universal” explanation for how cardiac filling is
achieved. There is a considerable body of evidence showing
that atrioventricular (AV) plane displacement (AVPD) is not
the sole mechanism of atrial and ventricular refill. The explanation proposed in the recent Perspective would therefore
benefit from contextualization with the existing data.
Arutunyan approaches the problem of cardiac filling from
four main perspectives: 1) constant-volume pumping, 2) the
importance of momentum conservation, 3) atrial contraction,
and 4) pressure gradients. We will address these accordingly.
Constant-volume pumping. The concept of constant-volume
pumping has interested readers of this journal since its first
edition in 1898 (24). Arutunyan first concludes that “ventricular contractions cause circulation of the blood by pumping
blood into arteries and simultaneously pulling it from large
veins. Ejection and pulling momentums of the blood act as
counterbalances, negate each other, and provide spatial stability to the heart during contraction.” In other words, the heart is
described as a constant-volume, self-reciprocating pump that
balances output with filling. As the ventricles contract, the AV
plane moves longitudinally toward the apex, as first described
by Leonardo da Vinci in the 15th century (31). Longitudinal
pumping is mediated through AVPD and is quantified as the
product of AVPD and epicardial short-axis area (23). Given
that both the epicardial apex (residing within the spatially fixed
pericardial sac) and the back of the atria (anchored in the
mediastinum by pulmonary veins) of the heart remain stationary, ventricular contraction shortens the long-axis dimension of
the chamber by displacing the valve planes toward the apex
and by necessity must lead to a reciprocal enlargement of the
atria by aspiration of extracardiac blood. Perfectly balanced
inflows and outflows would result in a perfectly constantvolume heart, as first postulated by Hamilton and Rompf (16)
in 1932, an appealing concept since no work is wasted moving
extracardiac tissues. This view, however, is only an approximation in light of the existing data.
Initial investigations by Hoffman and Ritman (18) supported
the idea, finding an average total heart volume variation
(THVV) of 2.7% in dogs. The authors state, “the combined
atrial filling appears to approximate the volume ejected by the
combined right and left ventricles” (18). Later studies have
investigated THVV in humans using magnetic resonance im-
Letter to the Editor
LETTER TO THE EDITOR
encompassing move would transfer blood from the atrium into
the ventricle without accelerating any blood. However, studies
on intracardiac KE and the acceleration feature of the Doppler
A wave demonstrate that encompassing of blood is only a
partial explanation. KE manifesting as transmitral flow increases during atrial contraction (Doppler A wave), indicating
that external work is being performed on the blood. This
manifests as transient fluid acceleration, the Doppler A wave,
rather than the blood remaining stationary in space and only
being encompassed by tissue sliding over it (3, 9, 13, 14). Thus
atrial contraction acts both by sliding past the blood and
accelerating it.
Venous pressure and AVPD. Arutunyan writes, “For example, 5–7 mm pressure difference between venules and veins
provides a slow flow of blood toward the heart. But a subtle
pressure difference between the large veins and the heart
chambers, as qualitative estimates show, is not sufficient for
filling the ventricle within a diastole.” This hypothesis can be
rejected on the basis of previous in vivo experiments, which
demonstrated sufficient LV filling in dogs occurring with a
peak pressure gradient from left atrium to LV of 2.8 ⫾ 0.3
mmHg (12). Furthermore, Arutunyan remarks, “the systolic
pressure gradient powers blood circulation up to the large veins
close to the heart, but the beat-to-beat transfer of blood to atria
and ventricle occurs via a forceful, AVPD-driven suction,
pull-up process that is powered by ventricular systole.” Pulsatile flow is present in the veins of the legs and contains
waveforms related to both respiration and heart frequency (1),
suggesting that venous flow is affected by both venous pressure
and AVPD even in distal parts of the vasculature.
In conclusion, AVPD is clearly an important and a definite
major contributor to cardiac filling. Substantial data from the
literature, however, suggest that the heart fills through a combination of AV plane reciprocity, diastolic recoil, venous
pressure, and momentum conservation with significant differences between the systemic and pulmonary circulations. Together, these mechanisms make the heart a near-constant volume pump, but the notion of a universal explanation for cardiac
filling based solely on AVPD lacks support in available data.
DISCLOSURES
No conflicts of interest, financial or otherwise, are declared by the author(s).
AUTHOR CONTRIBUTIONS
P.M.A. drafted manuscript; P.M.A., C.M., S.J.K., and H.A. edited and
revised manuscript; P.M.A., C.M., S.J.K., and H.A. approved final version of
manuscript.
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AJP-Heart Circ Physiol • doi:10.1152/ajpheart.00483.2015 • www.ajpheart.org
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Furthermore, Arutunyan states that “During the contraction,
atrial push of blood into ventricles occur via the pull-up of the
ventricular edges. ѧ During this process, in essence, the contracting edges of atria slide back over the blood.” Such an
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Letter to the Editor
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LETTER TO THE EDITOR