(Chest. 2000;117:1118-1123.)
© 2000
American College of Chest Physicians
Atrial Function During Cardiac Arrest Caused by Ventricular Fibrillation*
Andrej Pernat, MD;
Max Harry Weil, MD, PhD, Master FCCP;
Shijie Sun, MD;
Wanchun Tang, MD, FCCP;
Hitoshi Yamaguchi, MD and
Joe Bisera, MSEE
*
From the Institute of Critical Care Medicine (Drs. Pernat, Weil, Sun, Tang, and Yamaguchi, and Mr. Bisera), Palm Springs, CA; and The University of Southern California School of Medicine (Drs. Weil, Sun, and Tang, and Mr. Bisera), Los Angeles, CA.
Address correspondence to: Max Harry Weil, MD, PhD, Master FCCP, Institute of Critical Care Medicine, 1695 North Sunrise Way, Bldg #3, Palm Springs, CA 92262-5309; e-mail: Weilm{at}aol.com
 |
Abstract
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Objectives: To report observations on preserved regular
atrial electrical and mechanical systole during ventricular
fibrillation (VF) and to quantitate blood flow generated by atrial
contractions in this setting.
Methods: In 10 rats,
right atrial pressure pulses were continuously recorded before and for
an interval of 8 min after inducing VF. In 3 isolated, perfused rat
hearts, epicardial right atrial electrograms were recorded after
inducing VF. In 15 pigs, transesophageal echo-Doppler measurements were
obtained with pulsed and color-Doppler visualization of flow across the
mitral valve after onset of VF.
Results: In each rat,
regular right atrial pressure pulses were documented during VF. These
persisted over an average interval of 7.5 min. In isolated, perfused
hearts, right atrial contractions were accompanied by regular atrial
depolarizations. In pigs, regular atrial contractions generated atrial
stroke volumes of approximately 12 mL, or 25% of prearrest values
during the first minute after onset of VF, but those declined to
approximately 6 mL after 10 min of untreated cardiac arrest. Blood flow
from the left atrium into the left ventricle failed to advance
significantly into the systemic circuit. During atrial diastole, we
observed reversal of flow into the left atrium.
Conclusions: Atrial contractions are preserved during the
initial 8 min or more after cardiac arrest due to VF. Substantial
forward flow into the left ventricle failed to advance through the
outflow tract but regurgitated into the atrium during atrial
diastole.
Key Words: atrial pressure • cardiac arrest • resuscitation • transesophageal echo-Doppler • ventricular fibrillation
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Introduction
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Sudden
cardiac death in patients is most frequently caused by spontaneous
onset of ventricular fibrillation (VF). The fibrillating ventricles
fail to maintain coordinated mechanical function, accounting for
cardiac arrest, in which pulsatile blood flow to
the pulmonary and systemic circuits stops.1
However, such may not apply to the atria. A report by Garrey 2
in 1914 on fibrillation of the heart referred to
observations, which demonstrated that fibrillations of the atria are
not transmitted to the ventricles, and fibrillations of the ventricles
are not transmitted to the atria. Subsequent electrophysiological
studies in dogs and humans documented that regular atrial
depolarizations occasionally persisted during VF.3
4
Persistent atrial activity was observed after ventricular cardioplegia
during open heart surgery.5
Regular atrial
contractions were also observed with transesophageal echocardiographic
visualization, after brief intervals of VF induced in the
electrophysiology laboratory.6
In two human subjects,
Benchimol et al7
used a Doppler flowmeter positioned in
the aorta and in the dorsalis pedis artery. Pulsations during VF were
attributed by these investigators to atrial contractions, producing
forward propulsions of blood.
We sought to extend observations on atrial functions during VF,
especially their hemodynamic effect, in experimental settings of
cardiac arrest due to VF that remained untreated for intervals of 8
min or greater. Accordingly, we examined intact rats,
isolated perfused rat hearts, and intact pigs for initial confirmation
of pulsatile atrial activity during VF; and, subsequently, we
quantitated the amount and direction of blood flow produced by atrial
contractions.
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Materials and Methods
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All animals received humane care in compliance with the
Principles of Laboratory Animal Care, as formulated by the National
Society for Medical Research. Our facility is fully accredited by the
Association for Assessment and Accreditation of Laboratory Animal Care
International.
Rat
In Vivo: A well established model of cardiac
arrest in the rat was used.8
Ten male Sprague-Dawley
breeder rats, weighing between 450 and 550 g, were fasted
overnight, except for free access to water. Anesthesia was induced by
intraperitoneal injection of 45 mg/kg sodium pentobarbital. The trachea
was intubated with a 14-gauge cannula (Quick-Cath, Vicra Division;
Travenol Laboratory; Dallas, TX) by methods previously
described.8
For measurement of left ventricular pressure,
a 0.965 mm polyethylene catheter (Intramedic PE50; Becton Dickinson;
Sparks, MD) was advanced retrograde into the left ventricle from the
right carotid artery. A second polyethylene catheter was advanced into
the right ventricle from the left external jugular vein. The right
ventricular catheter was then slowly withdrawn into the right atrium,
guided by pressure monitoring. For measurements of aortic pressure, a
third polyethylene catheter was advanced through the left femoral
artery into the descending thoracic aorta. A 3.5-F bipolar pacing
electrode was advanced from the right external jugular vein into the
right ventricle for inducing VF. A conventional scalar lead II ECG was
recorded with the aid of needle electrodes.
Animals were mechanically ventilated with a tidal volume of 6.5 mL/kg
weight and at a frequency of 100 breaths/min, using a
volume-controlled ventilator of our own design.8
End-tidal
PCO2 was monitored with an infrared
CO2 analyzer (End-Tid IL200;
Instrumentation Laboratories; Lexington, MA). Tidal volume was
subsequently adjusted to yield an end-tidal
PCO2 of between 35 and 40 mm Hg.
Isolated, Perfused Rat Heart:
Three rats were anesthetized
and mechanically ventilated, as described above. A thoracotomy was
performed, and the heart was rapidly cooled by flooding the thoracic
cavity with iced saline solution. The heart was immediately harvested
by the Langendorf method, as previously exercised by our group, except
that both atria were excised together with the
ventricles.9
10
Special care was taken not to damage the
right atrium. The aorta was then incised at a site 8 mm distal to the
aortic valve, and a blunt 18-gauge needle was advanced proximally, for
a distance of 4 mm. Retrograde perfusion was then begun at a rate of 10
mL/min, and constant flow was maintained by a roller pump (AIP 1100;
CCMI; Los Angeles, CA).11
12
The perfusate was a
modified Krebs-Henseleit solution containing 118 mmol/l NaCl; 4.7
mmol/l KCl; 2.52 mmol/L CaCl2; 1.2 mmol/L
MgSO4; 25.0 mmol/L NaHCO3; 1.2 mmol/L
KH2PO4; 0.4 mmol/L Na2EDTA; 5.5
mmol/L glucose. A gas mixture of oxygen (95%) and
CO2 (5%) was bubbled through a vented
reservoir containing the perfusate. The heart was then removed from the
thorax. It was immediately suspended in a humidified glass
chamber. The electrocardiogram of the atria and ventricles was then
recorded. The negative electrode of the ventricular electrocardiogram
was at the root of the aorta, and the positive electrode was at
the apex. The negative electrode of the right atrial electrocardiogram
was also at the root of the aorta and the positive electrode on the
lateral wall of the right atrium, immediately distal to its junction
with the superior vena cava. A 3.5-F bipolar pacing electrode was
advanced from the detached inferior vena cava into the right ventricle.
Perfusate temperature was initially established at 24°C and gradually
increased to 37°C over an interval of 20 min with an externally
heated water jacket.
Porcine Model:
An established model of cardiac arrest and
resuscitation in the domestic pig was used. The preparation has been
extensively exercised by our group.13
14
Fifteen male pigs
weighing 40–45 kg were investigated. After the animals were
anesthetized, initially by IM injection of 20 mg/kg ketamine and
finally by 30 mg/kg of sodium pentobarbital, mechanical ventilation was
established. An 8-F catheter (USCI Model 6523–8F; CR Bard Inc;
Billerica, MA) was advanced from the right femoral artery into the
thoracic aorta. A 7.5-F balloon-tipped thermodilution pulmonary artery
catheter (Abbott Critical Care; North Chicago, IL) was then advanced
through the right femoral vein into the pulmonary artery. A 5-F pacing
electrode (I-NBIH; USCI; Bard Inc) was advanced through the right
cephalic vein into the right ventricle. A prototype single-plane 5 MHz
transesophageal echo-Doppler probe (Hewlett-Packard; Andover, MA), 6 mm
in diameter, was advanced from the mouth into the esophagus, and an
appropriate window was established for long-axis visualization of the
left atrium and ventricle.
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Experimental Procedures and Measurements
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Rat
In Vivo: After baseline hemodynamic
measurements were obtained, VF was induced by delivering a 0.5-mA AC
current to the right ventricular endocardium. The current was then
reduced to 0.2 mA and continued for 3 min to preclude spontaneous
reversion of VF.8
Mechanical ventilation was discontinued
after arterial pressure decreased to closing pressures and VF was
confirmed by ECG. VF was untreated for 8 min, after which precordial
compression was begun, with a precordial compressor of our own design, 8
and continued for 8 min. Right atrial, left ventricular,
and aortic pressures were recorded continuously with the aid of
pressure transducers (Transpac; Abbott Critical Care Systems; North
Chicago, IL), together with lead II of the ECG. The data
were recorded on a PC-based data acquisition system supported by CODAS
software (DATAQ Instruments; Akron, OH).
Isolated Perfused Rat Heart:
Both whole heart and right
atrial electrocardiograms were continuously recorded using conventional
ECG amplifiers (Model 7010; Marquette; Milwaukee, WI). Ventricular
fibrillation was induced by delivering a 0.12-mA AC current to the
right ventricular endocardium, and current flow was also continued for
3 min. Immediately after VF appeared, perfusion was stopped. At the end
of 10 min, perfusion was resumed at a rate of 4 mL/min for 2 min, and
10 mL/min for an additional 3 min. At the end of this 5-min interval,
which represented a total duration of 15 min of VF, the heart was
successfully defibrillated in each instance with a direct current
countershock delivered between the apex and cardiac base. All data were
recorded and stored on the digital acquisition system.
Porcine Model:
After baseline measurements had been
obtained, VF was induced with a 2-mA AC current delivered to the right
ventricular endocardium. Mechanical ventilation was stopped after the
onset of VF. VF was untreated for 10 min. Defibrillation was then
attempted with a 200-J precordial countershock, followed by two
additional shocks of 300 J and 360 J, as needed. If such failed to
restore the regular rhythm, precordial compression by a mechanical
compressor (Thumper, Model 1000; MI Instruments; Grand Rapids, MI) at a
rate of 80 beats/min was started for 60 s, and then another
sequence of up to three shocks was delivered. This sequence was
repeated for up to 15 min. Each animal was successfully resuscitated.
Echocardiographic-Doppler measurements were obtained with the aid of a
Hewlett-Packard Sonos 2500 system (Andover, MA) and a 5 MHz prototype
single plane transesophageal probe. For measurement of transmitral
flow, the sample volume of the pulsed Doppler was positioned at the
level of the mitral valve leaflets, and the ultrasound beam was
adjusted to be parallel with left ventricular inflow. Using algorithms
described by Lewis et al,15
transmitral flow velocity
signals were digitized on-screen for measurement of maximal flow
velocities, transmitral velocity time integrals, and
transmitral blood flow. The volume of blood propelled into the left
ventricle by each atrial contraction was computed from the total
transmitral flow divided by the number of atrial contractions over the
same minute. The direction of transmitral flow was identified by pulsed
Doppler and color Doppler flow imaging. For estimation of aortic
transvalvular flow, comparable methods were used, except that the
pulsed Doppler was positioned at a site immediately distal to the
aortic valve. Flow across the mitral valve was measured and recorded at
1-min intervals. The number of atrial contractions during each minute
was calculated from the measured time interval between the two peaks of
the pulsed Doppler transmitral flow signals and was confirmed by
counting echocardiographically visualized atrial contractions.
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Results
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Rat In Vivo
Right atrial pressure pulses were observed in each of 10 animals
during VF. The atrial pressure complexes persisted for
7.4 ± 0.9 min (mean ± SD), indicating that effective atrial
mechanical function persisted during this time interval. A
representative tracing is shown in Figure 1
. In addition to atrial pressure pulses, minute ventricular pressure
pulses provided additional evidence that atrial contractions produced
forward flow (Fig 2 ). These small ventricular pressure pulses were documented in each of
the 10 animals.
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Figure 1. Recordings of ECG and right atrial pressure (RA)
during the 2nd, 4th, 6th, and 8th min of VF in the rat. The 2-min
recording demonstrates artifacts produced by a continuous 0.2-mA
current delivered to the endocardium of the right ventricle to maintain
VF. Subsequent ECG recordings document VF. Atrial pressure pulses
diminished in amplitude over 8 min.
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Isolated, Perfused Rat Heart
Regular atrial contractions were visually confirmed in each of the
isolated, perfused heart preparations. These were associated with
regular atrial depolarizations (Fig 3
).
Porcine Model
Echocardiographic mitral valve opening and closing were documented
in each of 15 animals. After the onset of VF, we observed irregular
oscillatory movements of the mitral valve, accompanied by irregular
jets of transmitral flow registered by pulsed Doppler. Within an
interval of 1 min, prominent atrial contractions appeared with regular
mitral valve opening and closing. Color Doppler and pulsed Doppler
recordings documented forward blood flow from the left atrium to the
left ventricle during each atrial contraction, as shown in Figure 4 . Atrial contractions began as early as 7 s and as late as 85
s after onset of VF; mean time to appearance of atrial contraction was
36 ± 26 s. The changes in transmitral flow velocity, atrial stroke
volume, and the frequency of atrial contractions are shown in Figure 5
. There was a progressive decrease in both transmitral flow velocity and
atrial stroke volumes, together with the frequency of atrial
contractions over the 10-min observation interval. Atrial stroke volume
of 12.1 ± 2.6 mL, observed at the end of the first minute of VF,
represented 25% of the 51.1 ± 11.4 mL baseline stroke volume. The
maximal average atrial stroke volume was 15.1 ± 5.6 mL, and this
represented 28% of the baseline stroke volume. However, with both
pulsed and color Doppler measurements documented, forward flow into the
left ventricle produced by atrial contractions was followed by reversal
of flow from the ventricle to the atrium (Fig 4)
. Consequently, no
significant forward blood flow extended past the outflow of the left
ventricle and the aortic valve (Fig 6
).
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Figure 4. A color Doppler recording of transmitral blood
flow during cardiac arrest (not shown) demonstrated that blood flow
generated by atrial contraction was from the atrium into the ventricle.
This was followed by reversal of flow at the level of the mitral valve.
Pulsed Doppler recording of transmitral flow during VF is shown in this
figure. Regularly repeating jets of forward flow follow atrial
contractions. Regurgitant flow during atrial diastole is demonstrated
by pulses below the baseline.
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Figure 5. Transmitral maximal flow velocity, the atrial
stroke volume, and the frequency of atrial contractions during the
initial 10 min after the onset of VF in pigs during cardiac arrest.
Transmitral flow, generated by atrial contractions, and the frequency
of atrial contractions decreased over the 10-min interval.
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Figure 6. Pulsed Doppler recording of transaortic
blood flow during VF in the pig. Quantitatively insignificant but
regular Doppler pulses were detected, indicating that no significant
net blood flow was generated across the aortic valve during atrial
contractions.
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Discussion
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In each of the three models investigated, regular electrical and
mechanical atrial activity were preserved during cardiac arrest caused
by VF. In studies on intact rats and isolated, perfused rat hearts, we
demonstrated that atrial functions persist for at least 8 min after the
onset of VF. Small right ventricular pressure pulses, demonstrated
during VF in the rats, indicated propulsion of blood from the atria to
the ventricles after atrial contraction. The hemodynamic effects of
atrial contractions during cardiac arrest were then further evaluated
in pigs, using transesophageal echo-Doppler methodologies. We observed
mitral valve opening after atrial contraction, and both pulsed and
color Doppler confirmed that atrial contractions generated blood flow
from the atrium into the ventricle.
Regular electrical activity of the atria during VF was previously
described. However, these observations were made in surgical settings
that included hypothermia and hyperkalemic
cardioplegia.5
16
17
18
The presence of contractions was
also documented after diagnostic studies in the electrophysiology
laboratory after very brief intervals of VF.3
4
19
Damato
et al19
investigated dogs during the first minute of VF.
Initially, retrograde atria activation was observed after inducing VF,
and this was followed by regular anterograde depolarizations after 1
minute. These earlier observations also applied to the porcine model in
which regular atrial contractions and mitral valve opening and closing
appeared after an interval of approximately 30 s after VF was
induced.
The present studies advance these earlier observations to the extent
that mechanical function of atrial contractions are characterized. The
mechanical contribution of atrial contraction to normal cardiac
function was first described in the 17th century by William
Harvey.20
He observed regular gushes of blood from a cut
in the apex of the heart after ventricular contractions ceased but
atrial contractions persisted. In 1965, Nakano and
Mercer21
observed regular and forceful atrial contractions
for as long as 30 min after the onset of VF. More recently, De Piccoli
et al6
noted regular mitral and aortic valve motion,
together with transmitral blood flow, during brief intervals of VF
induced for testing purposes in the clinical electrophysiology
laboratory. They attributed their observations to preserved atrial
contractions during the necessarily brief interval of 20 s before
defibrillation. Our observations extended over a prolonged time
interval after onset of cardiac arrest. Atrial contractions persisted
for 10 min or more. Significant volumes were ejected by the atria, but
forward propulsion of blood from the atrium to the left ventricle
failed to advance blood flow through the aortic valve. Color Doppler
measurements demonstrated that atrial contractions propelled blood from
the atrium into the inflow of the left ventricle. However, flow
reversed during atrial diastole through a partially open mitral valve.
A ventriculo-atrial pressure gradient after atrial contraction had been
identified by Sarnoff et al, 22
the same gradient that
normally accounted for mitral valve closure before normal ventricular
contraction.
During sinus rhythm, atrial contraction contributes between 20 and 35%
of the output of the left side of the heart.23
24
25
26
27
The
largest atrial stroke volume during VF, observed in our study,
represented approximately 28% of baseline ventricular stroke volume.
However, this blood flow did not advance past the aortic valve.
Nevertheless, the atrial contractions were sufficiently forceful to
propagate an arterial pressure pulse, as described by Benchimol et
al7
and also as observed by us in the aorta of both rats
and pigs during ventricular fibrillation.
It was previously demonstrated in patients during pulseless electrical
activity, that when sinoatrial activity was preserved, or when
sinoatrial activity was restored during resuscitation, there was
greater success of resuscitation and survival.28
29
In the
absence of effective increases in systemic blood flow generated by
atrial contraction, the persistence of sinoatrial activity and its
prediction of successful resuscitation is more likely due to better
perfusion generated by precordial compression and attenuation of
myocardial ischemia.
In summary, our investigations confirmed that regular
atrial systole persists during the initial 10 min of cardiac arrest
caused by VF. Stroke volumes generated by the left atrium during VF
represented up to 28% of ventricular stroke volume before inducing
cardiac arrest. However, this transmitral flow failed to advance into
the systemic circuit and regurgitated into the atrium, but accounted
for transmission of pressure pulses into the arterial circuit.
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Footnotes
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Abbreviation: VF =
ventricular fibrillation
This work was supported in part by Grant HL 54322 from the Heart, Lung,
and Blood Institute of the National Institutes of Health, Bethesda, MD,
and by Laerdal Foundation for Acute Medicine Inc., Stavanger, Norway.
Received for publication March 23, 1999.
Accepted for publication September 8, 1999.
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Abstract
Introduction
