Download The Sequence of Retrograde Atrial Activation in the Canine Heart

The Sequence of Retrograde Atrial Activation in the Canine
Heart
CORRELATION WITH POSITIVE AND NEGATIVE RETROGRADE P WAVES
By Albert L. Waldo, Kari J. Vitikainen, and Brian F. Hoffman
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ABSTRACT
The relationship of P-wave polarity and morphology in leads II, III, and aVF to the
sequence of atrial activation was studied in the canine heart when the atria were paced
from the region of the sinus node or the posterior-inferior left atrium and when retrograde
activation of the atria occurred with right ventricular epicardial pacing. Deeply negative P
waves in leads II, III, and aVF which occurred when the posterior-inferior left atrium was
paced were associated with true retrograde activation of the atria. Positive P waves
recorded in leads II, III, and aVF during retrograde atrial capture with right ventricular
pacing were associated with rapid retrograde spread of the impulse in the interatrial
septum to the region of Bachmann's bundle from which site the impulse spread to
depolarize significant portions of both atria in a manner similar to that demonstrated
during pacing from the region of the sinus node. When the atria were paced from a site just
anterior to the coronary sinus ostium, positive P waves recorded in leads II, III, and aVF
were associated with early activation in the vicinity of Bachmann's bundle and later
activation of the posterior-inferior left atrium. When the atria were paced from a site just
posterior to the coronary sinus ostium, negative P waves in leads II, III, and aVF were
associated with early activation of the posterior-inferior left atrium and later activation in
the vicinity of Bachmann's bundle. It was concluded that the time of arrival of the
impulse at Bachmann's bundle relative to that at the posterior left atrium and the
direction of spread of the impulse from and within Bachmann's bundle are critical in
determining P-wave polarity and morphology.
• Previous reports from this (1-4) and other (5-8)
laboratories and scattered clinical reports (9-14)
disagree with the classic concept that the "retrograde" P waves produced during ventricular, atrioventricular (AV) junctional, and low atrial
rhythms are necessarily negative in electrocardiogram (ECG) leads II, III and aVF. One report (8)
has correlated the sequence of activation of portions of the right atrial appendage, the left atrial
appendage, and the free wall of the right atrium
with P-wave polarity in standard ECG leads during
the retrograde atrial capture which occurred with
right ventricular epicardial pacing. With the exception of this paper, we are unaware of any
previous studies which have correlated P-wave
From the Department of Pharmacology, College of Physicians and Surgeons of Columbia University, New York, New
York 10032.
This investigation was supported in part by U. S. Public
Health Service Grants HL12738 and HL11.310 from the National Heart and Lung Institute.
Dr. Waldo is the Otto G. Storm Established Investigator of
the American Heart Association. His present address is Department of Medicine, University of Alabama Medical Center,
Birmingham, Alabama 35294.
Please address reprint requests to Albert L. Waldo, M.D.,
UAB Medical Center—LHR 339, University Station, Birmingham, Alabama 35294.
Received October 24, 1974. Accepted for publication April 29,
1975.
156
polarity and morphology in standard ECG leads
during ectopic atrial rhythms with a map of the
sequence of atrial activation.
The present report describes a series of studies
performed on the canine heart which correlate
P-wave polarity and morphology with the origin
and the time course of atrial epicardial and endocardial activation during ectopic atrial rhythms.
Ectopic pacing sites were selected which produced
either a negative retrograde P wave (3, 4) or a
positive retrograde P wave (1, 8) in ECG leads II,
III, and aVF. The sequences of atrial activation
during rhythms produced when these ectopic sites
were paced were then compared with each other as
well as with that demonstrated when the atria were
paced from a site close to the sinus node.
Methods
STUDIES OF P-WAVE POLARITY AND MORPHOLOGY
Twenty-seven healthy adult mongrel dogs weighing
18-25 kg were studied. The dogs were anesthetized with
sodium pentobarbital (30 mg/kg, iv) and ventilated with
room air using a Harvard respirator. Each dog was
placed on its left side, and a right thoracotomy through
the fifth intercostal space was performed. A pericardiotomy was performed and a pericardial cradle created.
Using previously described techniques (1, 4), electrodes
were placed at selected sites which included (Fig. 1) the
region of the sinus node (SN), the portion of Bachmann's
Circulation Research, Vol. 37, August 1975
157
SEQUENCE OF ATRIAL ACTIVATION
LAS
on photographic paper at recording speeds of 50, 100, and
200 mm/sec.
Seven of these studies initially were performed using
sterile techniques (1). These dogs were permitted to
recover and were then restudied 1-2 weeks later under
sodium pentobarbital anesthesia while they were lying
on their left side; thus, P-wave polarity and morphology
were compared with the chest open and closed in the
same dog. During normal and ectopic rhythms, P-wave
polarity always was identical, and P-wave morphology,
although never completely identical, was quite similar
under both conditions, confirming previous observations
(1,3,8).
STUDIES OF THE SEQUENCE OF ATRIAL ACTIVATION
PLA
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LAA
FIGURE 1
Sketches of four views of the canine atria. A: View of the free
wall of the right atrium. B: View of the right side of the
interatrial septum and A V junction visualized after the free wall
of the right atrium and part of the right ventricle have been cut
away. C: View of Bachmann's bundle and both atrial appendages as well as a portion of the left atrium. D: View of the
inferior aspects of both atria. The fixed electrode recording sites
include the region of the sinus node (SN), the right atrial
appendage (RAA), the low atrial septum in the region of the A V
node (LAS), Bachmann's bundle (BB), the left atrial appendage
(LAA), the posterior-inferior left atrium (PLA), and the right
ventricular epicardium (RV). During the studies of sequence of
atrial activation, fixed electrodes were placed only at the SN,
PLA, and RV sites. The black dots represent the points at which
electrograms were recorded during atrial activation when the
atria were paced from the SN, PLA, and RV sites. Pacing sites
anterior and posterior to the coronary sinus ostium (CSO) are
identified by two small arrows; the A arrow is the posterior site
and the B arrow is the anterior site. SVC = superior vena cava,
IVC = inferior vena cava, PV = pulmonary veins, RA = right
atrium, LA = left atrium, RV = right ventricle, LV = left
ventricle, CS = coronary sinus, and TV = tricuspid valve.
bundle (BB) overlying the interatrial septum, the right
atrial appendage (RAA), the left atrial appendage
(LAA), the posterior-inferior left atrium (PLA), the free
wall of the right ventricle (RV), and, in 14 studies, the
low atrial septum in the region of the AV node (LAS).
During spontaneous sinus rhythms and during atrial
rhythms produced during bipolar threshold pacing
through the SN electrode, the PLA electrode, and the RV
electrode, standard bipolar and augmented unipolar
ECGs and atrial electrograms from each electrode site
were monitored simultaneously on a DR-8 Electronicsfor-Medicine switched-beam oscilloscope and recorded
Circulation Research, Vol. 37, August 1975
Preparation of the Study (Perfused) Heart.—Studies
were performed on 13 isolated canine hearts perfused
with arterial blood from a donor (support) dog. The
donor dogs weighed 30-40 kg. The study heart was
obtained from dogs which weighed 18-25 kg. After the
study dog's heart had been exposed, electrodes were
sutured to the SN, PLA, and RV sites. Modifying
previously described techniques (15), the study heart was
isolated intact, and perfusion with arterial blood from
the donor dog was initiated. The isolated heart was then
placed in a blood-filled bath. Using standard techniques,
the perfused blood and the bath were maintained at
37°C. Using a roller pump, the venous blood, which
drained directly into the bath, was returned to the donor
dog through a defoaming reservoir. During the periods of
data collection, the ventricles remained immersed in the
bath, and blood from the bath was gently poured over the
atria at appropriate intervals to prevent any drying of the
atrial tissue.
In three additional experiments, the study heart was
exposed through a right thoracotomy, and the heart was
then perfused in situ. This in situ study allowed the
recording of standard ECGs in the study dog during the
experiment. In these studies, electrodes were placed at
the same epicardial sites used in the studies of P-wave
polarity and morphology. Conduction in the study heart,
checked periodically by pacing through each fixed electrode with threshold stimuli and then measuring the
conduction time to the other fixed electrodes, remained
constant throughout each study. After completion of all
epicardial mapping studies, a right atriotomy was performed to permit endocardial mapping. The right atriotomy incision was placed 5 mm from the margin of fat in
the AV groove and extended no closer than 1 cm to the
crista terminalis.
Mapping the Sequence of Atrial Activation.—Grid
maps were drawn on Polaroid photographs of several
views of the isolated heart, providing accurate identification of mapping sites both during each study and for the
permanent record. The grid sites were not always equidistant from one another but were generally separated by
5 mm, i.e., the diameter of the electrode probe (2, 3)
utilized to record bipolar electrograms from each of the
sites. Figure 1 shows drawings of four views of the canine
atria with the grid sites superimposed. The sequence of
atrial activation was mapped during threshold pacing
from each fixed electrode (SN, PLA, and RV). During
bipolar threshold pacing from the PLA site, the SN site,
and the RV site, conduction times from each pacing site
to each grid site were measured directly from the
WALDO. VITIKAINEN, HOFFMAN
158
oscilloscope grid of a Tektronix 502 dual-beam oscilloscope whose sweep was triggered from thejiacing stimulus at a sweep speed of 1 mm/sec. When the RV site was
paced, the oscilloscope was triggered after a suitable
delay which allowed for retrograde conduction of the
impulse through the AV node to the atria, and the
electrogram recorded from the SN electrode was used as
a time reference. Also, during ventricular pacing, the
earliest point of activation of the atria was considered
zero time. In the three studies in which the study heart
was perfused in situ, utilizing the electrode probe to
deliver bipolar threshold stimuli, the atria were also
paced from sites just anterior and posterior to the
coronary sinus ostium (Fig. 1C); ECGs and electrograms
were recorded as described for studies of P-wave polarity
and morphology. For all studies, ECGs were recorded at
a band pass between 0.1 and 200 Hz and electrograms at
a band pass between 12 and 200 Hz.
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Results
PACING FROM THE REGION OF THE SINUS NODE
This portion of the study largely confirms the
results of previous studies in which the sequence of
atrial activation during sinus rhythm has been
mapped either partially (8, 16-20) or completely
(21). The P waves in ECG leads II, III, and aVF
were always positive.
Figure 2 illustrates the sequence of activation in
a representative study in which the atria were
paced from the region of the sinus node. For this
and other such figures, the sequence of atrial
activation is illustrated by isochronous lines drawn
at 5-msec intervals. The activation front in the free
wall of the right atrium (Fig. 2A) spread inferiorly
down the sulcus terminalis and anteriorly along the
pectinate muscles. Most of the left atrium was
depolarized through a wave front from Bachmann's
bundle (Fig. 2C). However, the posterior-inferior
region (PLA) consistently was activated relatively
late by a wave front which seemed to come from the
lower interatrial septum (Fig. 2D). Thus, the
direction of spread of activation in the left atrium
with the exception of the left atrial appendage was
basically directed inferiorly.
The wave front in the AV junction consistently
D
FIGURE 2
Maps of the sequence of atrial activation in a representative study when the atria were paced from the
electrode in the region of the sinus node (SN). Isochronous lines are drawn at 5-msec intervals.
Abbreviations are the same as they are in Figure 1.
Circulation Research, Vol. 37, August 1975
159
SEQUENCE OF ATRIAL ACTIVATION
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FIGURE 3
Maps of the sequence of atrial activation in a representative study when the atria were paced from the
posterior-inferior left atrial electrode site (PLA). Isochronous lines are drawn at 5-msec intervals.
Abbreviations are the same as they are in Figure I.
advanced to the coronary sinus ostium, suggesting
that a wave front from the posterior internodal
pathway does not contribute to activation of the
AV node when the atria are paced from the SN site.
This direct observation is consistent with previously published indirect observations in the dog (4)
and in man (22) which suggested that normally the
main route of conduction between the sinus node
and AV node is via the anterior internodal pathway. These data conflict with the observations of
Goodman et al. (21), who suggested that activation
of the AV node occurs via the posterior internodal
pathway, and with the data of Spach et al. (23),
who described simultaneous activation of the AV
nodal region from an anterior and a posterior wave
front.
PACING FROM THE POSTERIOR-INFERIOR LEFT ATRIUM
As we (3, 4) and others (24-26) have previously
described, the P waves in ECG leads II, III, and
aVF were always deeply negative when the PLA
site was paced. As illustrated in the representative
Circulation Research, Vol. 37, August 1975
example shown in Figure 3, when the atria were
paced from the PLA site, the interatrial septum,
the right atrial free wall, and the left atrium were
depolarized by retrograde wave fronts. Therefore,
except for the tips of the left and right atrial
appendages, the atria were depolarized in a sequence opposite to that which occurred during the
paced sinus rhythm. Thus, negative P waves in
leads II, III, and aVF can be correlated with true
retrograde activation of the atria. The left atrial
portion of Bachmann's bundle was depolarized
simultaneously throughout its length (Fig. 3C),
thereby explaining previous observations (4) in
which discrete lesions in Bachmann's bundle did
not alter the polarity, morphology, or duration of
the P wave when the atria were paced from the
PLA site.
PACING THROUGH THE RIGHT VENTRICULAR ELECTRODE WITH
RETROGRADE CAPTURE OF THE ATRIA
As Moore et al. (1, 8) have previously described,
the P waves in ECG leads II, III, and aVF were
160
WALDO. VITIKAINEN, HOFFMAN
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D
FIGURE 4
Maps of the sequence of atrial activation in a representative study when the atria were paced from the
right ventricular epicardial electrode site (RV). Isochronous lines are drawn at 5-msec intervals.
Abbreviations are the same as they are in Figure 1.
consistently positive with retrograde atrial capture
during ventricular pacing. A representative study
of the sequence of atrial activation during retrograde atrial capture with pacing from the right
ventricle is illustrated in Figure 4. The depolarization wave front spread quickly up the interatrial
septum, consistently emerging superiorly very
early (within 15 msec in this example) at Bachmann's bundle (Fig. 4C). Having reached this site,
the activation front proceeded along Bachmann's
bundle to depolarize a considerable portion of the
left atrium in a manner similar to that which
occurred during the paced sinus rhythm and
clearly opposite to that which occurred during the
rhythm produced by pacing at the PLA site. In
addition, an activation front proceeded from Bachmann's bundle toward the sinus node and spread to
depolarize a significant portion of the upper right
atrium (Fig. 4A and C) in a manner similar to that
which occurred during paced sinus rhythm. The
caudal aspects of both atria consistently were
activated by retrograde wavefronts (Fig. 4D), the
right atrial wave front being primarily in the region
of the posterior internodal pathway (27-29). Also
present in some studies and illustrated in Figure 4A
was a third contribution to right atrial epicardial
activation which corresponded in location to the
anatomical locus of the middle internodal pathway
(27-29).
As can be extrapolated from these data on the
sequence of atrial activation during ventricular
pacing with retrograde atrial capture, the critical
factor in determining P-wave polarity seems to be
the relatively rapid spread of the impulse to the
region of Bachmann's bundle from which point it
can be spread inferiorly over significant portions of
both atria. Cancellation of early wave fronts also
may be important.
PACING FROM SITES IN PROXIMITY TO THE CORONARY SINUS
OSTIUM
When the atria were paced from site B just anterior to the coronary sinus ostium (Fig. IB) P
Circulation Research, Vol. 37, August 1975
SEQUENCE OF ATRIAL ACTIVATION
161
occurred during sinus rhythm. When this group
paced the posterior site in proximity to the coronary sinus ostium, the sequence of atrial activation
was almost identical to that which occurred when
the atria were activated from the PLA site in the
present study, i.e., there was complete retrograde
activation of the atria without any inferiorly directed wave fronts.
Discussion
RELATIONSHIP OF THE SEQUENCE OF ATRIAL ACTIVATION TO
P-WAVE POLARITY AND MORPHOLOGY
FIGURE 5
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A: P wave recorded in lead II when the atria were paced from
the posterior coronary sinus ostial site (see Fig. IB). B: P wave
recorded in lead II when the atria were paced from the anterior
coronary sinus ostial site (see Fig. IB). The relative times of
arrival of the impulse at the various atrial recording sites have
been superimposed on each P wave. STIM = stimulus, PLA =
posterior-inferior left atrium, LAS = low atrial septum, BB =
Bachmann's bundle, SN = sinus node, and LAA = left atrial
appendage.
waves were positive in ECG leads II, III, and aVF
(1) (Fig. 5B). As illustrated by the relative sequence of activation of the atrial sites from which
electrograms were recorded (Fig. 5B), the impulse
arrived relatively early at the BB site particularly
in comparison with its arrival at the PLA site. Data
from a previous study (4) in which positive P waves
in leads II, III, and aVF were produced when the
atria were paced from a LAS site also were associated with relatively early activation of a BB site
and significantly later activation of a PLA site.
Thus, the positive P waves in leads II, III, and aVF
during "retrograde" activation of the atria seem to
be consistently associated with early activation of
Bachmann's bundle and relatively later activation
of the posterior-inferior left atrium.
When the atria were paced from site A just
posterior to the coronary sinus ostium (Fig. IB), P
waves in leads II, III, and aVF were negative (Fig.
5A). These negative P waves were associated with
early activation of the PLA site and relatively later
activation of the BB site (Fig. 5A).
Goodman et al. (21) paced the canine atria from
similar sites in proximity to the coronary sinus
ostium and studied the sequence of atrial activation, but they did not record any ECGs. When this
group paced the site anterior to the coronary sinus
ostium, the wave front spread rapidly up the
interatrial septum to Bachmann's bundle and from
there it spread inferiorly over significant portions of
both atria in a manner similar to that which
Circulation Research, Vol. 37, August 1975
Data from the present study and, by extrapolation, combined data from the present study and the
study of Goodman et al. (21) clearly demonstrate
that for the canine heart the positive retrograde P
waves in ECG leads II, III, and aVF result from
rapid spread of the wave of excitation up the
interatrial septum to Bachmann's bundle from
which point it then spreads inferiorly over a significant portion of both atria in a manner similar to
that which occurs during spontaneous sinus
rhythm. This finding confirms previous hypotheses
(3, 4, 7, 10). Furthermore, the relative time of
arrival of the impulse at Bachmann's bundle compared with that at the posterior-inferior left atrium
and the direction of spread of the impulse in and
from Bachmann's bundle play a critical role in
determining P-wave polarity and morphology. Relatively early activation of Bachmann's bundle
compared with the posterior-inferior left atrium
permits excitation to spread inferiorly from Bachmann's bundle to depolarize significant portions of
both atria, thereby producing positive P waves in
leads II, III, and aVF. When activation of the
posterior-inferior left atrium is relatively early
during the sequence of atrial activation and activation of Bachmann's bundle is relatively later during the sequence of atrial activation, excitation
from the posterior-inferior left atrium spreads as a
retrograde wave front over much if not all of the left
atrium, thereby preventing the occurrence of any
significant inferiorly directed wave front from
Bachmann's bundle. The result is negative P waves
in leads II, III, and aVF.
There is some evidence in patients that the
preceding explanation for the positive retrograde P
wave probably holds true for the human heart as
well. In studies of the P wave produced by pacing
the atria in the region of the AV node in patients
with ostium primum atrial septal defects, only
negative retrograde P waves in leads II, III, and
aVF have been produced (22); however, in patients
with ostium secundum or sinus venosus atrial
septal defects or with intact atrial septa, positive
162
WALDO. VITIKAIIMEN. HOFFMAN
retrograde P waves in the same ECG leads have
been produced (3, 22). Thus, it is evident that the
critical location of the ostium primum lesion in the
atrial septum precludes the possibility of retrograde activation of the atria in the previously
described manner; moreover, these data suggest
that the sequence of atrial activation during the
inscription of the positive retrograde P wave in
man is quite similar to that demonstrated for the
canine heart.
SPECIALIZED ATRIAL CONDUCTION
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Data from the present study are consistent with
the considerable body of evidence (30) which demonstrates the presence and supports the functional
significance of specialized atrial pathways. However, no discrete, functionally isolated pathways of
rapid conduction in the atria equivalent to those
which can be demonstrated for the His bundle or
the bundle branches were identified in the present
study. As conduction in the former pathways
normally occurs simultaneously with conduction in
working atrial muscle, there is no way to distinguish qualitatively between electrograms recorded
from the specialized atrial pathways and those
recorded from working atrial muscle. In contradistinction, it is only the fact that conduction in the
His bundle and bundle branches normally occurs
during the isoelectric portion of the P-R interval
(when simultaneous conduction in any other cardiac tissue normally does not occur) which permits
electrophysiological identification of the His bundle and the bundle branches when electrograms are
recorded from the whole heart. It should be noted
that several studies have concluded that there are
no functionally significant specialized atrial pathways but rather that there are preferential atrial
pathways (16, 21, 23). The major objection seems
to be primarily with the term specialized. However,
for the data presented in this paper, the semantic
difference between specialized and preferential
atrial pathways seems relatively unimportant.
Acknowledgment
The authors would like to express their appreciation to Dr.
Thomas N. James for his critical review of this manuscript.
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The sequence of retrograde atrial activation in the canine heart. Correlation with positive
and negative retrograde P waves.
A L Waldo, K J Vitikainen and B F Hoffman
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Circ Res. 1975;37:156-163
doi: 10.1161/01.RES.37.2.156
Circulation Research is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1975 American Heart Association, Inc. All rights reserved.
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