386
Participation of Atrial Specialized Conduction
Pathways in Atrial Flutter
GUSTAVO PASTELIN, RAFAEL MENDEZ, AND GORDON K. MOE
SUMMARY The circus movement theory of flutter has been supported by numerous theoretical, experimental,
and clinical studies, but there has been little consideration of the possible participation of the specialized conduction
pathways of the atria. In the present work we have studied experimental atrial flutter in relation to the behavior of
these pathways, in response to elevated potassium and to surgical interruption. Application of trains of ttimuli at
frequencies appropriate to Induce a self-sustained flutter revealed that (1) flutter can be more easily induced by
stimuli applied to the left atrial insertion of Bachmann's bundle than to the body of the right atrium, (2) flutter can
be initiated by appropriate trains of stimuli without the creation of an artificial obstacle, and (3) flutter exhibits the
same characteristic behavior, with or without artificial obstacles. Doses of potassium that elevate the plasma
concentration to 9.5 mM/liter cause total inactivation of atrial myocardium without suppressing flutter waves as
recorded from the vicinity of the intemodal pathways. Section of the middle internodal pathway reduces the
frequency of experimental flutter, section of both the middle and posterior pathways prevents the establishment of
flutter. The results suggest that the specialized intemodal pathways play an important role in the genesis and
maintenance of circus movement flutter.
SINCE THE circus movement theory of atrial flutter was
proposed by Lewis et al.,1 there have been many theoretical, experimental, and clinical studies in support of the
concept. Among the relevant theoretical studies are those
of Wiener and Rosenblueth,1 Rytand,3 and Stibitz and
Rytand,4 all of whom, in accord with Lewis et al.,5 made
the simplifying assumption that the propagation of impulses in the atria occurred at the same velocity in all
directions, and selected as the primary condition of mathematical analysis a model with homogeneous properties.
Using such a model, Wiener and Rosenblueth demonstrated the necessity for an obstacle around which an
impulse could circulate; circulation could be permanent
provided the perimeter of the obstacle exceeded the
wavelength of the impulse (defined as the distance travelled during a period of time equal to the refractory
period). Initiation of the flutter process can be explained
by assuming asymmetric recovery of excitability in a zone
that includes the perimeter of the obstacle; introduction
of a second impulse during the phase of asymmetric
excitability then could initiate the one-way conduction
that is essential for the self-sustained circus movement.
Most of the published experimental studies, in accord
with this hypothesis, suggest that the natural obstacle
provided by the caval orifices might suffice,6"6 but some
investigators, estimating that the perimeter of the natural
obstacles would be too small, enlarged the potential circuit
path by crushing an area of atrial tissue adjacent to the
natural openings. Rosenblueth and Garcia Ramos6 exFrom the Institute Nacional de Cflrdiologia, Mexico, Distrito Federal;
the Department of Pharmacology, SUNY Upstate Medical Center,
Syracuse, New York, and the Masonic Medical Research Laboratory,
Utica, New York.
Supported in part by National Institute! of Health Grant HL 15759 to
Dr. G. K. Moe. Dr. Pastelin was an OUen Memorial Fellow, Masonic
Medical Research Laboratory, 1973.
Address for reprints: Dr. G.K. Moe, Masonic Medical Research
Laboratory, Utica, New York 13503.
Received December 3, 1976; accepted for publication October 17,
1977.
tended the margin of the inferior caval orifice, a method
widely adopted in subsequent studies, and were able to
show that the excitation wave in their experimental flutter
did indeed sequentially activate the tissue around the
obstacle.
Pharmacological evidence reported by Mendez et al.'°
supports the circus movement character of flutter induced
by the Rosenblueth and Garcia Ramos technique. Antiarrhythmic agents that increase the wavelength of the excitatory process suppress the flutter; others, like potassium,
that are effective in overcoming an aconitine-induced
tachyarrhythmia, reduce the wavelength and fail to abolish
the circus movement flutter. Clinical confirmation reported by Cardenas et al." suggests that many cases of
atrial flutter in man are of circus movement origin.
Indirect evidence has also been published by Decherd et
al.12 and by Cabrera and Sodi Pallares,13 who found that
the electrical axis of the atria undergoes a 360° shift with
each flutter wave. More recent studies with intracavitary
electrodes14'15 and with vectorcardiographic and ultrasonic techniques16 support the hypothesis.
These many studies provide a solid basis for the circus
movement theory of flutter, but few have considered the
possible role of specialized conduction pathways within
the atria, although the functional significance of oriented
bundles was considered years ago by Eysterand Meek.17-'"
The three internodal pathways19-M and the interatrial
band described by Bachmann11 probably determine the
sequence of atrial activation in a number of species,
including man.""" Struck by the orientation of the internodal pathways, James19 called attention to the possibility
of their participation in circus movement flutter. In some
respects the physiological characteristics of atrial specialized fibers resemble those of the ventricular Purkinje
tissue: more rapid depolarization during "phase O," faster
conduction velocity, a plateau during phase 2, and a
greater capacity to undergo spontaneous pacemaker activity than the "ordinary" atrial muscle fibers.""30 Of great
SPECIALIZED CONDUCTION IN ATRIAL FLUTTER/Pastelin el al.
significance is their relatively high resistance to elevated
external postassium concentration.29"^
The internodal pathways form closed loops between the
sinoatrial (SA) and atrioventricular (AV) nodes; as preferential pathways, they could play a role in the genesis
and maintenance of atrial flutter.'9 To test this hypothesis,
we have examined the possibility of producing circus
movement flutter by applying rapidly repetitive stimuli to
the left atrium, on the assumption that the junction of
Bachmann's bundle with the anterior internodal pathway
would provide an asymmetric input into the right atrial
internodal complex. We have also studied the effects of
increasing the plasma potassium concentration on established flutter. Because the loops formed by the three
internodal pathways provide three potential circuits of
different perimeters, we studied the influence of surgical
section of the middle and posterior pathways on the
initiation, frequency, and persistence of flutter.
Methods
Young dogs of both sexes, weighing between 10 and 15
kg, were anesthetized with sodium pentobarbital, 35 mg/
kg, administered intravenously. Under artificial respiration, the chest was opened in the midline and the heart
was suspended in a pericardia! cradle attached to the
edges of the split sternum.
Electrograms were recorded by means of an ink-writing
polygraph (Grass p-7) or an Electronics for Medicine
photographic oscillograph. Three pairs of direct leads
were attached to the atrial epicardial surface (Fig. 1); one
was positioned over the middle internodal pathway near
its junction with the SA node (site 8), one was placed over
FIGURE 1 Schematic drawing of the heart as seen from the right
anterosuperior aspect: (1) sinus node, (2) AV node, (3) superior
vena cava, (4) inferior vena cava, (5) right atrial appendage, (6)
left atrial appendage, (7) anterior internodal pathway, (8) middle
internodal pathway (site of electrode placement), (9) posterior
pathway, (10) site of recording electrodes over middle pathway,
(II) anterior margin of right auricle, (12) site of section of anterior
pathway, (13) Bachmann's bundle and site of stimulation, (14)
site of crushing of Bachmann's bundle, (15) site of section of the
middle pathway, (16) recording site on right ventricle, (17) site of
stimulation and recording on the body of the right atrium, (18) site
of crushing lesion used by Rosenblueth and Garcia Ramos, (19)
site of section of the posterior internodal pathway, and (20)
coronary sinus.
387
the middle pathway at its passage between the caval
orifices (site 10), and the third was attached to the
anterior margin of the right atrial appendage (site I 1). A
fourth channel was used to display a modified lead 2
electrocardiogram, recorded between the superior vena
cava and the left hind leg, a lead that enhances the P
waves. The distances between atrial recording sites 8 and
10 averaged about 20 mm, and between 8 and 11, 35 mm.
Electrode terminals (Grass E2B) were separated by 0.51.0 mm and were inserted at a depth of 0.5-1.0 mm in the
atrial wall at the specified points. The recording sites were
chosen to be representative of events near one ot the
internodal pathways, in comparison with activity recorded
from atrial myocardium. These limited sites do not, of
course, permit a map of atrial excitation sequence during
flutter, nor was it our objective to record such a map.
Twenty-four experiments, divided in four groups of six,
were performed (six additional experiments were used to
assess questions raised by the first groups). The first group
was used to assess the efficacy of stimuli applied to the left
atrium near the distal portion of Bachmann's bundle,
compared with similar trains of stimuli applied to the body
of the right atrium (site 17). The stimuli, obtained from a
Grass S-8 stimulator, were delivered at frequencies of 8,
10 and 15 Hz, in trains lasting 1, 2, 4, 6, 8, and 10
seconds. Stimuli were applied through bipolar electrodes
at 0.5-msec duration, and 10% above the diastolic threshold intensity. The characteristics of the resulting flutters,
at all combinations of stimulus frequency and duration,
were compared, following which the obstacle formed by
the inferior vena cava was enlarged by crushing adjacent
atrial tissue, and the influence of the site of stimulation
was again assessed. The site of the crush, as in the
experiments of Rosenblueth and Garcia Ramos," is indicated in Figure 1 by the solid line at position 18. The
resulting lesion was about 20 mm in length and 10 mm in
breadth, encompassing the full thickness of the atrial wall
and the adjacent vena cava. Postmortem examination in
three experiments confirmed that the lesion included the
posterior internodal pathway (9 in Fig. 1).
In the second group of experiments, flutter was again
initiated by stimulation of the intact atria. After an
observation period of 30 minutes, a bolus of KG, 10 mg/
kg, was injected into the superior vena cava. Blood
samples for potassium analysis by flame photometry were
drawn from the brachiocephalic artery before, during, and
each minute for 5 minutes after the injection. Electrograms were recorded at a paper speed of 100 mm/sec
during the whole period.
In the third set of experiments, KC1 was administered
during a stable flutter by continuous intracaval infusion at
a rate of 10 mg/kg per minute. Blood samples were drawn
at intervals of 1 minute for 5 minutes. As before, the
electrograms were recorded continuously before, during,
and after the KC1 infusion.
In the last series, flutter was again initiated in the intact
atria, and the effect of a rapid injection of KC1 (10 mg/kg)
was noted. Thirty minutes later, when the plasma [K] had
returned to normal, the middle internodal pathway was
sectioned by cutting through the bridge of atrial tissue
between the caval orifices (15 in Fig. 1) and immediately
CIRCULATION RESEARCH
388
suturing the incision. Flutter was again initiated, and the
electrocardiographic characteristics were compared with
those recorded prior to the intervention. The effect of KG
was again observed, and after an additional recovery
period of 30 minutes, the posterior tract was sectioned at
the point of its passage between the inferior vena cava and
the atrioventricular sulcus (site 19). Following this final
intervention, attempts to reinitiate flutter were made.
Additional experiments were done to test the effect of
elevated plasma [K] on conduction velocity at a stimulation frequency of 7 Hz and to test the effect of section of
Bachmann's bundle.
Results
Influence of the Site of Stimulation
Stimulation of the left atrium proved to be much more
effective than stimulation of the right atrium in initiating
flutter in the intact atria (Fig. 2).
In the six experiments represented in Figure 2, stimuli
were applied at a frequency of 8 Hz in part A, 10 Hz in B,
and 15 Hz in C. Open columns indicate the success rate
for stimuli applied to the left atrium (Bachmann's bundle),
solid columns for right atrium. In no case did stimulation
of the body of the right atrium at 8 Hz result in flutter,
even with 10 seconds of stimulation, while left atrial
stimulation succeeded in one dog at the briefest duration
and in 50% at 8 and 10 seconds. The discrepancy is
evident also at the higher stimulus frequencies (Fig. 2, B
and C). Right atrial stimulation was 100% successful only
at the longest duration (10 seconds) and the two highest
frequencies, whereas left atrial stimulation was 100%
successful in 9 of the 18 possible combinations.
At the lower and upper extremes of the stimulus
patterns (low frequency, brief duration; high frequency,
long duration), the test procedure does not discriminate
between right and left atrial stimulation. With these two
extremes eliminated, the data are summarized as a 2 x 2
table in Table 1, which indicates the success rate for right
and left atrial stimulation with trains of 1, 2, 4, and 6
seconds at frequencies of 10 and 15 Hz. The exact
probability, according to Fisher's bilateral test for 2 x 2
tables, is 4.028 x 10"10.
Once induced, the frequency of the flutter was the same
, B
VOL. 42, No. 3, MARCH
1978
TABLE 1 Incidence of Flutter Resulting from Stimulation
of Right vs. Left Atria with Trains of 1, 2, 4, and 6
Seconds at Frequencies of 10 and 15 Hz
Left
Right
Flutter
No flutter
43
13
5
35
whether stimulation was applied to the left or to the right
atrium, and the frequency was not influenced by crushing
tissue adjacent to the inferior vena cava according to the
technique of Rosenblueth and Garcia Ramos 6 (Table 2).
The greater ease of inducing flutter by left atrial stimulation, apparent in Figure 2, was not influenced by the
crushing lesion. In all cases, the flutter persisted until
interrupted by a brief burst of rapid stimulation or other
intervention.
In three ancillary experiments, crushing lesions were
made across the interatrial band. Left atrial stimulation
was still effective in inducing flutter in two of these. This
result was not unexpected, as the localized interruption
would not prevent a bypass and reentry of the specialized
tissue beyond the incision. In the third experiment, stimulation on the left atrial side of the lesion was no longer
successful, but stimulation of the region of Bachmann's
bundle on the right side of the lesion was still effective.
Efects of Potassium, Single Bolus
Abrupt elevation of plasma [K] during atrial flutter
suppressed electrical activity in atrial muscle (as recorded
from the margin of the right atrial appendage), but flutter
activity persisted for a brief time in electrograms recorded
in proximity to the specialized fibers (Fig. 3). In each of
the panels of Figure 3, the two upper traces were recorded
from the region of the middle internodal pathway near the
sinus node and between the two caval orifices, respectively
(sites 8 and 10 in Fig. 1). The third trace displays activity
from the atrial myocardium (site 11), and the fourth is the
electrocardiogram derived from superior vena cava and
left hind leg. Between panels A and B, flutter at a
frequency of 8 Hz was established by a brief train of
stimuli. All atrial records show the same frequency, also
evident in the ECG, in which 2:1 AV block is apparent.
The alternating configuration of the electrograms in the
atrial records indicates that the flutter was near the
maximum frequency permitted by the limiting refractory
TABLE 2
Frequency of Atrial Flutter According to Its
Type
Experiment
no.
FIGURE 2 Incidence of flutter induced by stimulation of left and
right atria. Abscissas: duration of stimulus train in seconds at
frequencies of 8, 10, and 15 Hz in A, B, and C, respectively.
Ordinates: number of episodes of flutter in six experiments. Solid
bars: stimuli applied to right atrium; open bars; stimulation of
Bachmann's bundle via left atrium.
1
2
3
4
5
6
Intact atria
| Rosenblueth technique
Produced by Stimulus In:
R.A
L.A.
R.A.
L.A.
(Hz)
(Hz)
(Hz)
(Hz)
8.0
8.2
8.0
9.5
8.9
8.9
8.0
8.6
8.0
9.5
8.6
9.0
R.A. = right atrium; L.A. = left atrium.
8.0
8.6
8.3
9.4
7.8
8.6
8.3
9.8
8.7
8.6
SPECIALIZED CONDUCTION IN ATR1AL FLUTTER/Pastelin et al.
—-
H»
I
I
I'
I "
•**
I
^*-
v, -v.
Isec
FIGURE 3 Initiation of flutter and its persistence in specialized
alrial tissue (upper two traces in each panel) after inactivation of
alrial myocardial activity (3rd trace) by single bolus of KCl.
Further explanation in text.
period of the tissue in the circuit pathway. In panel C,
recorded 11 seconds after the bolus of KCl, the atrial
frequency was retarded to 6.7 Hz, and activity at that
frequency appeared in both of the upper traces. The
electrograms recorded from the region of the middle
pathway at this stage are more variable, in spite of the
slower frequency, as a result of the K-induced slowing of
conduction (see below). Activity in the atrial muscle was
reduced to approximately half the flutter frequency, but
flutter with 2:1 AV block was still apparent in the
electrocardiogram. Panel D, recorded 2 seconds later,
shows the last three flutter waves recorded near the
middle pathway and a complete absence of electrical
activity in the ordinary myocardium. Upon restoration of
sinus rhythm (last half of panel D), the ECG showed
ventricular complexes without P waves, presumptive evidence for a sinoventricular rhythm. Activity was still
present in the region of the middle pathway, but the total
mass of participating atrial tissue was obviously too small
to generate manifest P waves, even in the modified lead 2
recording. Plasma K concentration reached 8 mM/liter in
the 1st minute and returned to normal within the following
5 minutes. Similar events were consistently observed in all
six experiments of this series.
Several conclusions may be drawn from this set of
experiments. First, activity may be recorded from the
vicinity of the internodal pathways at a time when areas of
atrial myocardium are inexcitable. Second, the frequency
of the flutter movement diminishes as the concentration
of K in the plasma increases. Third, conduction in the
flutter pathway becomes compromised, as indicated by
389
the varying configuration of electrograms recorded in the
region of the internodal pathway.
It is known that elevated [K], beyond about 7 HIM, will
depress conduction in cardiac tissues even at "normal"
frequencies of stimulation, but accessory experiments
were conducted to assess the effect of elevated K on
conduction at a driving frequency comparable to the
flutter frequency. In three experiments, conduction intervals were measured between sites 8 and 10, as representative of conduction in the specialized pathways, and
between 5 and 11 (Fig. 1), as representative of conduction
in atrial muscle. Stimuli were applied at a site close to site
8, at a frequency of 7 Hz, as KCl was infused at a rate of
7.0 mg/kg per minute. The data are listed in Table 3 as
apparent velocities (i.e., interelectrode distance divided
by the time interval) as a function of plasma K concentration. In the control condition (K = 4.25 ITIM), the
apparent velocity was approximately 60% faster in the
region of the middle internodal pathway than in the
direction of the path in atrial myocardium. As the K
concentration increased, conduction was depressed in
both routes; 2:1 block appeared in the atrial muscle at K
= 8.9 mM, and total block at an average of about lOmin.
At this level, conduction velocity as estimated in the
internodal pathway was depressed to a degree compatible
with the observed depression of frequency of the flutter
movement recorded following K injection in the series of
experiments represented by Figure 3. The last two rows of
figures in the table were recorded during recovery from K
infusion.
Potassium Infusion
When potassium was injected as a bolus, as in Figure 3,
dissociation between the specialized pathways and the
atrial myocardium was limited to a very brief period just
prior to arrest of the flutter, and precise estimation of the
plasma [K] at the critical moment could not be achieved;
accordingly, six additional experiments were conducted in
which KCl was infused at a rate of 10 mg/kg per minute.
In three of these, the flutter was induced by left atrial
stimulation in intact atria; in the other three, the method
TABLE 3 Effect of Elevated [KJ on Conduction at
Driving Frequency of 7 Hz
Plasma K+
Apparent conduction velocity (m/sec)
(mM/l'ter)
Middle pathway
4 25
5.05
6.05
6.65
1.3
1.1
1.1
1.1
1.1
1.0
0.8
0.7
0.5
1.1
8.2
8.9
9.7
10.5
11 8
9.8
6.8
1.0
Atrial myocardium
0.7
0.7
0.6
0.6
0.6
0.5 (2:1 block)
0.4 (2:1-4:1 block)
Total block
Total block
0.4
0.5
The figures represent the average of three experiments. The
lower two rows were recorded during recovery from infusion of
KCl.
CIRCULATION RESEARCH
390
of Rosenblueth and Garcia Ramos was used. In the first
two experiments with intact atria, the flutter ceased within
a few seconds after electrical activity in the atrial myocardium was suppressed. In the third experiment, the infusion
of KG was stopped at the first sign of inactivation of the
atrial muscle. Examples of the record obtained from this
experiment are shown in Figure 4. In each panel the upper
tracing was recorded from the intercaval portion of the
middle pathway, the second tracing from the right atrial
appendage, and the lower trace from the modified lead 2.
As in Figure 3, panel A was recorded during sinus rhythm
and panel B after initiation of flutter at 8.7 Hz, again with
2:1 AV block. Panel C was obtained 80 seconds after the
KC1 infusion was begun. Flutter frequency had diminished
to 7.3 Hz, with considerable irregularity of the configuration of the electrograms, and some degree of block was
apparent in the myocardial record. Plasma [K] at that
time had risen from 3.5 to 7.5 mM/liter, and the infusion
was stopped. Five seconds later (panel D) the atrial
electrogram was completely silent, but activity continued
at a frequency of about 6 Hz in the middle pathway, as
shown in the upper tracing. At that time, the plasma [K]
had reached 9 mM/liter. Suppression of atrial myocardial
activity, with continuing activity in the vicinity of the
middle pathway, persisted until plasma [K] dropped below
7.0 mM/liter. Recovery of activity in the muscle is shown
in panel E, recorded 2 minutes after the end of the
infusion. Recovery to the initial flutter pattern in all leads
was complete within the following 2 minutes.
In the three experiments in which the caval orifice was
B
-'v^\A t
VOL. 42, No. 3, MARCH 1978
extended by crushing, the KCl infusion was stopped at the
first sign of inactivation of the atrial muscle. In each of
these the sequence of events was similar to that in Figure
4. The results from one of these are graphed in Figure 5.
KCl was infused for 75 seconds beginning at time 0. The
flutter frequency, initially 500/min, dropped progressively
to 170/min, but was still maintained in the region of the
internodal pathway (open circles) while atrial muscle
(crosses) was completely inactive. Plasma [K] reached a
peak value of 9.3 mM/liter (triangles); when it had fallen
to 7.6 at the 3rd minute, the flutter frequency began to
increase, and activity returned in the atrial muscle. During
the subsequent 5 minutes, both the [K] and the flutter
frequency approached the initial conditions. The principal
conclusion of these experiments is that, while activity in
atrial muscle was completely suppressed, activity (although slower and irregular in contour) persisted in the
region of the internodal pathway, and that the initial
flutter frequency was resumed when the elevated K receded.
Influence of Section of the Internodal Pathways
In six experiments, the middle internodal pathway was
sectioned between the venae cavae (site 15, Fig. 1).
Invariably, this intervention reduced the flutter frequency
(Fig. 6). In the example shown in the figure, electrograms
were recorded from the middle internodal pathway near
the SA node and at its intercaval passage (upper two
traces; 8 and 10, respectively, in Figure 1), from atrial
muscle of the right atrial appendage (3rd trace), and from
the epicardial surface of the ventricle. Panel A was
recorded during sinus rhythm, and B was recorded 30
minutes after flutter had been established at a frequency
of 8 Hz. At this frequency, alternating configuration and
cycle lengths occurred in all three atrial records. Between
B and C, a rapid injection of KCl, as in previous experiments, caused the development of 2:1 block between the
specialized tissue and atrial muscle (last half of panel C),
progressing to complete block in D. Soon after, the flutter
was replaced by sinus rhythm. When plasma [K] had
returned to its original level, the middle pathway was
sectioned, and flutter was reestablished, but at a frequency
10
700
-
600
£j 500
0.
« 400
X
2 MO
ZOO
5 2
100
4
3
0
FIGURE 4 Persistence of flutter throughout a brief infusion of
KCl. Records from specialized tracts, upper traces; atrial myocardium, middle traces; modified lead 2, lower traces. Further description in text.
1
£
3
4
5
MINUTES
FIGURE 5 Frequency of flutter in specialized atrial fibers (circles)
and in atrial muscle (crosses) in relation to changes in plasma
potassium concentration (triangles).
SPECIALIZED CONDUCTION IN ATR1AL FLUTTER/Pastelin el al.
391
contrary.17"30 The nonhomogeneous nature of intra-atrial
conduction forms the basis of our experimental approach.
Influence of the Site of Stimulation
I SEC
FIGURE 6 Frequency of flutter induced before (panel B) and after
section of the middle trad (panel E), and response to bolus
injections of KCl (C, D, and F). Upper two traces recorded from
specialized tracts; third trace from atrial muscle; bottom trace from
the epicardial surface of the right ventricle Further explanation in
text.
of 7 Hz (panel E). At the slower frequency, all of the
atrial electrograms recorded regular rhythmic activity.
Again, KCl injection terminated activity in the atrial
muscle, while flutter waves persisted in the region of the
middle pathway (panel F). In panels D and F, it is clear
that the persistent activity in the upper two traces is
flutter, not fibrillation. In each panel, however, the frequency was reduced at the higher potassium concentrations.
Following recovery from elevated plasma [K], two
additional surgical interventions were made. The anterior
pathway was cut near the sinus node (site 12) and the
posterior pathway where it passed between the inferior
vena cava and the AV groove (site 19). Both incisions
were scalpel cuts of about 10 mm in length, immediately
sutured. Following these procedures, it was no longer
possible to induce a persistent flutter.
When the initial flutter frequency in the intact atria is
high, the electrograms are often irregular in contour. In
one experiment, illustrated in Figure 7, it was impossible
to induce a stable flutter before surgical intervention.
Brief periods of irregular activity at a variable frequency
of 7.3-7.6 Hz, and lasting less than 2 minutes, followed
repeated attempts (Fig. 7, panel B). With the objective of
increasing the potential path length, the intercaval portion
of the middle pathway was crushed. A stable flutter at a
frequency of 6.3 Hz followed the first burst of stimuli
applied to the left atrium (panel C) and persisted for 30
minutes until terminated by an injection of quinidine.
Discussion
The results described above provide one more piece of
evidence in support of the circus movement theory proposed by Lewis,1 but there are some important differences
between results of these studies and the many previous
reports. In earlier studies, in accord with the concepts of
Lewis et al.B the atrial myocardium was considered as a
physiologically homogeneous system, despite accumulating physiological and anatomic evidence to the
The very significantly greater ease with which stimulation of the left atrium can induce flutter, compared with
the right, can be explained in terms of the physiological
properties and anatomic relations of Bachmann's bundle.
The interatrial band and a branch of the anterior pathway
share a common origin, and they run a parallel course to
their divergence at the level of the interatrial septum.19-20
Bachmann's bundle continues along the superior aspect of
the left atrium, giving rise to branches that are distributed
to the appendage and body of the left atrium.21 Given the
greater conduction velocity of the bundle, an impulse
initiated in the left atrium should be conducted quickly to
the junction of Bachmann's bundle and the anterior
pathway, a site at which the necessary asymmetry postulated by Wiener and Rosenblueth1 might permit the
initiation of one-way conduction. This would be less likely
to occur for impulses initiated in the body of the right
atrium.
The frequency of flutter induced in the intact atria, and
that produced in the same heart after a crushing lesion
adjacent to the inferior vena cava, were invariably the
same. This suggests that the circuit pathway could not
have been limited to the natural obstacle of the caval
orifice, for enlargement of that obstacle should have
diminished the flutter frequency. Admittedly, the observation of identical frequencies does not deny the possibility of another loop not involving the inferior vena cava,
A—V-A—V
KAAAAAAAAAAs
1 sec
FIGURE 7 "Stabilization" of flutter following interruption of the
middle pathway. Upper trace in each panel, electrogram recorded
from the right auricle (Fig. 1, site II), lower trace, right ventricle.
A: sinus rhythm; B: irregular and nonpersisten; atrial activity
shortly after an attempt to induce stable flutter (frequency, about
7.5 Hz); C: stable flutter at 6.3 Hz after the atrial tissue was
crushed between the venae cavae (site 15).
392
CIRCULATION RESEARCH
but it is wholly compatible with the trajectory provided by
circuits involving the specialized fibers.
The emphasis on internodal pathways as "loops" providing a preferential circuit pathway does not, of course,
imply that the internodal bands are insulated from the
ordinary atrial muscle with which they are intermingled. If
a bundle of fibers with a higher conduction velocity is
enmeshed in an otherwise homogeneous matrix, the
"wake" of a wavefront will describe an angle with the axis
of propagation that depends on the relative velocities; the
transit time of a loop will still be determined by the
intrinsic velocity in the "specialized" bundle.
VOL. 42, No. 3, MARCH
1978
velocity, for it is quite possible that a "short circuit"
through atrial muscle within the specialized loop provides
a somewhat briefer cycle at normal [K] but is suppressed
at the higher concentrations, forcing the flutter wave to
traverse a longer pathway composed solely of specialized
fibers. Nevertheless, the apparent depression of conduction shown in Table 3 (at [K] = 10 niM) is approximately
equivalent to the observed reduction in flutter frequency.
The remaining possibility, that the flutter is the expression of a rapidly firing ectopic focus, is incompatible with
the demonstrated action of elevated potassium on the
abnormal pacemaker activity generated by aconitine' MM
or digitalis.3"
Elevated Potassium Concentrations
The effect of elevated [K] provides the strongest evidence for the participation of the specialized circuits,
namely, the persistence of flutter waves in electrograms
recorded from the vicinity of the internodal pathways at a
time when no activity could be recorded from the atrial
myocardium. The greater resistance of the specialized
fibers to potassium is perhaps the strongest physiological
evidence for their fundamental difference from atrial
muscle.1*""3*
Block between the specialized fibers and atrial muscle
induced by increased [K] is enhanced by rapid driving
rates.31 The high frequency of flutter must in itself increase
the chance of block and, thus, facilitate demonstration of
the persistence of flutter after cessation of atrial myocardial activity.
The persisting activity in the area of the internodal
pathway often became irregular in the presence of elevated [K], but the basic frequency is still readily estimated.
The irregular contour might resemble "fibrillation," but it
is almost surely not fibrillation for the following reasons.
(1) Fibrillation, even when all of the atrial tissue mass is
available, can be induced and sustained in the normal dog
heart only when gross dispersion of atrial refractory
periods is induced by vagal stimulation.33 When so induced, the frequency, when it can be measured at all, is
considerably greater than that of circus movement flutter.
(2) When fibrillation terminates (with cessation of vagal
stimulation), it is almost invariably followed by resumption of sinus rhythm. In the experiments described here,
the frequency of recorded activity diminished gradually as
the potassium concentration increased, and increased
gradually as the potassium level receded. (3) Fibrillation,
defined in a mechanistic sense (i.e., not merely irregular
contours of extracellular electrical records), cannot be
maintained in a narrow channel; this probably accounts
for experimental and clinical observations of dissimilar
rhythms in the two atria.
Elevation of plasma [K] to levels that suppressed activity in atrial muscle often terminated the flutter (Fig. 3 and
Fig. 6D), and invariably decreased the frequency. Extracellular [K] levels that suppress activity in atrial muscle
will reduce the conduction velocity in the specialized
fibers; the fundamental difference between the tissues is a
quantitative one, not qualitative (Table 3). It is not,
however, justified to say that a reduction of 60% in the
frequency represents a 60% reduction of conduction
Section of the Internodal Tracts
The three internodal pathways have different lengths,
providing three possible loops of different circumferences
(anteromedial, anteroposterior, posteromedial). If we assume that the conduction velocity is the same in each,
then the flutter must circulate at a frequency determined
by the shortest loop. Anatomically, the shortest loop is
that provided by the anterior and medial bundles, and this
is probably the circuit pathway whether flutter is established in the intact atria, or following the technique of
Rosenblueth and Garcia Ramos. The crushing lesion at
site 18 interrupts the posterior pathway but does not alter
the flutter frequency (Table 2). When the medial pathway
is sectioned, the only remaining option is the loop formed
by the anterior and posterior bundles, which must necessitate a lower flutter frequency. This was the invariable
result. Persistence of the slower flutter in the presence of
elevated potassium (Fig. 6) again attests to the participation of the specialized fibers, as does the failure to
establish a stable flutter after section of the anterior and
posterior tracts.
Are Obstacles Needed?
Although there are anatomic obstacles present within
the postulated loops (venae cavae, membranous septum),
it should be apparent that such obstacles are not a
prerequisite. The "obstacle" can be a functional one,
determined by the duration of refractoriness relative to
the conduction velocity. This was apparent in a mathematical model of atrial fibrillation37 and was recently elegantly
demonstrated in isolated rabbit atrial tissue by Allessie et
a]3K.
39
Finally, we note the analogy between the topography of
the circuits19-20 and the trajectory of the flutter waves
recorded in man.14"16
Conclusions
These studies, based on different premises than previous investigations of circus movement flutter, permit the
following conclusions. (1) The internodal pathways form
loops through which flutter waves may circulate. (2) The
greater conduction velocity in the loops of specialized
tissue than in atrial muscle makes a flutter movement
possible without the necessity for a physical obstacle. (3)
The insertion of Bachmann's bundle into the loops via its
SPECIALIZED CONDUCTION IN ATRIAL FLUTTER/Pastelin et al.
junction with the anterior pathway facilitates the initiation
of flutter by impulses initiated in the left atrium. (4) The
greater resistance of the specialized fibers to hyperkalemia
suggests the need to examine possible differences in the
response to other substances, with the objective of improving our understanding of the mechanism of action of
antiarrhythmic agents in the treatment of flutter.
17.
18.
19.
Acknowledgments
We thank Dr. Emilio Kabela for the use of his laboratory facilities at
the Upftate Medical Center, and Dr. J. J. Mandoki for his assistance in
the statistical analysis
20.
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