Acceleration of Sinus Rhythm
During Slow-rate Atrial Pacing
RALPH HABERL, M.D., GERHARD STEINBECK, M.D.,
AND
BERNDT LUDERITZ, M.D.
SUMMARY We evaluated the effects of slow-rate atrial pacing on impulse formation of the sinus node in
13 isolated rabbit right atria using the microelectrode technique. After the spread of activation was mapped
to determine true sinoatrial conduction time (SACT) (38 ± 16 msec [ ± SD]), the atrium was paced for eight
beats at constant intervals slightly shorter than spontaneous cycle length in steps of 10 msec. In all
preparations, slow-rate atrial pacing failed to capture the pacemaker center, but shortened action potential
duration because of electrotonic interaction between atrium and sinus node. The resulting acceleration of
impulse formation of dominant fibers ceased instantaneously when atrial pacing was terminated.
Estimation of SACT by constant pacing 5 beats/min faster than sinus rhythm seriously underestimated
the true values (p < 0.05), because sinus node acceleration prevented capture of dominant pacemaker fibers
in 10 of 13 preparations. At pacing rates 10 beats/min faster than sinus rhythm, capture did not occur in
eight of 13 experiments; at pacing rates 20 beats/min faster, the pacemaker center was captured in all
preparations.
This study describes sinus node acceleration as a consistent and hitherto unknown finding during slowrate stimulation of the atrium. This phenomenon accounts for the failure of the constant atrial pacing
technique to determine SACT accurately in man.
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
IN 1973, Strauss and co-workers proposed premature
atrial stimulation as an indirect measure of sinoatrial
conduction time (SACT) in man. I Subsequent experimental studies have shown several inherent inadequacies of this technique.2 3 Using constant atrial pacing at
rates slightly faster than sinus rhythm, Narula et al.4
found a simpler and quicker approach for measuring
SACT. Data obtained by constant atrial pacing have
been used to characterize sinus node function in man5-7
and also have been compared for validation with the
results of independent method of direct extracellular
direct-current recordings of sinus node activity.8
Testing the Narula technique in an experimental microelectrode study, we consistently found an acceleration of sinus node automaticity during slow-rate atrial
drive. In this report, we describe the electrophysiologic mechanism of this acceleration and the resulting
pitfalls when SACT calculation is performed by this
technique.
achieve a pH of 7.35 ± 0.05 and temperature was
maintained at 37 + 0. 1°C.
A pair of Teflon-coated silver wires was placed on
the midportion of crista terminalis to record a bipolar
electrogram; a second pair of electrodes was positioned on the atrial appendage to stimulate the preparation. A programmable stimulator (Arrhythmia Investigation System Type 4279, Digitimer LTD) provided
single stimuli with variable prematurity after every
tenth spontaneous beat of sinus origin or a train of
stimuli with variable pacing intervals and duration of
pacing. Stimuli were constant 2-msec voltage pulses,
twice threshold.
Transmembrane potentials were recorded with glass
microelectrodes filled with 3M KCI (resistance 10-20
Mfl). All signals were displayed on a storage oscilloscope (Tektronix 5103N), stored on magnetic tape
(Ampex PR 2200, tape speed 15 inches/sec) and recorded on a Minograf 804 (Siemens) for detailed analysis.
All preparations beat spontaneously.
The pacemaker site was identified by extensive
mapping of the endocardial sinus node area using 4060 intracellular impalements as previously described.3
Dominant pacemaker fibers exhibit marked phase 4
depolarization, a smooth transition between phase 4
and phase 0 of the action potential, and the longest
latency between activity of the cell and the atrium.
After a stable impalement of a dominant pacemaker
fiber had been achieved, the preparation was paced for
a train, started at random, or eight beats at a constant
interval 10 msec shorter than spontaneous cycle
length. This pacing run was performed four times,
interposed with intervals of 20 spontaneous cycles.
Then, the pacing interval was shortened further in
steps of 10 msec. These steps equalled a change of
pacing rate of 2.3-4.7 beats/min.
Methods
Young rabbits that weighed 1.5-2.5 kg were killed
by a blow on the neck. The hearts were rapidly excised
and dissected in cool Tyrode's solution. The right atrium was isolated from the remaining part of the heart
and pinned with its endocardial surface uppermost in a
tissue bath, which was perfused with oxygenated Tyrode's solution at 50 ml/min.
The composition of the modified Tyrode's solution
was (in mM): NaCl, 130; KCI, 4.7; CaCl2, 2.5; MgCl2,
2.6; NaHCO3, 24.9; NaH2PO4, 1.3; glucose, 11. The
solution was bubbled with 95% 02 and 5% CO2 to
From the Medizinische Klinik I der Universitat Miinchen, Klinikum
Grosshadern, Munich, West Germany.
Supported by the Deutsche Forschungsgemeinschaft.
Address for correspondence: Gerhard Steinbeck, M.D., Medizinische Klinik I der Universitat Munchen, Klinikum Grosshadem, Marchioninistrasse 15, D-8000 Miunchen 70, West Germany.
Received October 13, 1982; revision accepted March 4, 1983.
Circulation 67, No. 6, 1983.
Data Analysis
SACT was defined as the time between the activation of a dominant pacemaker fiber and atrial activa1368
ACCELERATION OF SINUS RHYTHM/Haberl et al.
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
pacemaker fiber (upper trace) and the surface electrogram of crista terminalis (lower trace) during spontaneous rhythm. The spontaneous cycle length is 455
msec and the true SACT 58 msec. Although the preparation was paced at an interval of 440 msec (panel B),
activation of the fiber still precedes the' activation of
the atrium by 10 msec, and phase 4 depolarization
merges smoothly into phase 0 depolarization. Thus,
the atrial impulses do not capture the pacemaker fi'ber.
Nevertheless, sinus node impulse formation is accelerated due to a shortening of action potential duration
from 194 msec to 176 msec.
In panel'C, the pacing interval is 410 msec. The
transition from phase 4 to phase 0 depolarization is
more marked, but still gradual, indicating that the fiber
continues to discharge spontaneously. The action potential duration is shortened to 154 msec, which leads
to a further decrease of sinus node cycle length. The
atrial deflection precedes activation of the pacemaker
fiber by 32 msec, but the impulses fail to capture the
pacemaker center. At a pacing interval of 380 msec
(panel D), a sharp transition from phase 4 to phase 0
depolarization occurs, indicating that the fiber'is prematurely discharged by the paced atrial beats. Atriosinus conduction time is 44 msec. Thus, sinus node
capture in this preparation does not occur until the
pacing interval is 75 msec shorter than spontaneous
cycle length.
In figure 2, the transmembrane potential of a dominant pacemaker fiber during spontaneous rhythm at a
cycle length of 455 msec (broken) and during atrial
pacing with an interval of 410 msec (solid) is superimposed. During stimulation, phase 4 depolarization of
the fiber continues to merge gradually into action potential upstroke. Nevertheless, the transmembrane potential is influenced by the atrial impulses. Phase 0
depolarization and repolarization are speeded up; as a
consequence, the duration of the action potential is
shortened.
In all 13 experiments, the atrial stimuli failed to
capture the dominant pacemaker fibers when the pacing cycle closely approached the spontaneous cycle
length. During noncapture, the'action potential dura-
tion. We defined the moment of activation as the 50%
amplitude of the transmembrane potential of a fiber
during phase 0 depolarization and the intrinsic deflection of the surface electrogram.
The action potential duration was measured from the
moment of activation of a fiber to the time at which
repolarization was 90% complete. In each preparation,
we determined the slowest pacing rate that led to a
sharp transition between phase 4 and phase 0 depolarization of the dominant sinus node fiber; this we defined as sinus node' capture.
Sinus node recovery time (SNRT) after a train of
constant atrial pacing was measured as the interval
between the last paced atrial electrogram and the first
spontaneous atrial electrogram of sinus origin.
To compare data from several experiments with different basic cycle lengths, we calculated the corrected
recovery time (CSNRT) as sinus node recovery time
minus spontaneous cycle length before stimulation.
Corrected recovery time of dominant pacemaker fibers
was measured from phase 0 depolarization after the
last paced atrial beat to phase 0 depolarization of the
first spontaneous sinus node action potential.
For estimation of SACT by constant atrial pacing,
the atrial return cycle after a train of eight consecutive
stimuli was measured and divided by two (undirectional SACT). For calculation of SACT by premature
atrial stimulation, the postextrasystolic cycles of the
atrium A23 were plotted as a function of the curtailed
cycle A1A2. SACT tsition was calculated from A2A3 at
transition from compensatory to noncompensatory 'return cycles and SACT50% from A2A3 after a curtailed
cycle that was 50% of spontaneous cycle length.
Statistical evaluation was by linear regression analysis and Wilcoxon matched-pairs, signed-rank tests.
Results
Acceleration of Sinus Rate
In 13 experiments, various pacing rates slightly faster than sinus rhythm were applied with a microelectrode impaled in a dominant pacemaker fiber. Figure 1
depicts a representative experiment.
Panel A shows the transmembrane potential of a
-0
-0
I
;~ ~ 154
194
~ ~
410 ms
455 ms
-o
-0
II
176~
16
-
440 ms
l.
~~
25mV
146
--
380ms
1369
~
FIGURE 1. Acceleration of sinus rate during
atrial pacing. The transmembrane potential of
a dominant pacemakerfiber is shown together
with the surface ECG during spontaneous
rhythm (A) and during slow-rate atrial drive
with diferent pacing intervals (B, C and D).
The spontaneous cycle length is 455 msec and
true SACT 58 msec. At pacing intervals of 440
msec (B) and 410 msec (C), the fiber continues
to discharge spontaneously (smooth transition
from phase 4 to phase 0 depolarization, phase
4 unchanged). Nevertheless, the action potential duration is shortened to 176 msec and 154
At a pacing interval of 380
transition between phase 4
and phase 0 depolarization indicates capture
of the fiber by the atrial impulse.
msec, respectively.
msec (D), a sharp
VOL 67, No 6, JUNE 1983
CIRCULATION
1370
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
FIGURE 2. Superposition of the transmembrane potential of a
dominant pacemaker fiber during spontaneous rhythm (broken
recording, cycle length 455 msec) and the same fiber during
slow-rate atrial drive (solid recording, pacing interval 410
msec), which does not prematurely discharge the sinus node.
The fiber is the same as infigure 1. During stimulation, phase 0
depolarization and repolarization are accelerated and the action potential amplitude and the maximal diastolic potential are
slightly increased.
tion of pacemaker fiber was shortened, the maximal
degree of shortening varying from preparation to preparation. Prolongation of the stimulation period in eight
experiments up to 60 seconds did not alter the phenomenon of sinus node acceleration.
Table 1 lists complete data from 13 experiments.
Preparations 1-7 exhibited a long SACT (> 30 msec)
and preparations 8-13 exhibited a short SACT (s- 30
msec) during spontaneous rhythm. The length of true
SACT is positively correlated to action potential duration of dominant pacemaker fibers (r = 0.854, p <
0.01). Also, the pacing rate necessary to capture the
pacemaker center is positively correlated to action potential duration (r - 0.859, p < 0.01) and true SACT
(r - 0.843, p < 0.01). Thus, the longer the action
potential duration during spontaneous rhythm, the
more pronounced the shortening of action potential
duration and the extent of sinus node acceleration during atrial pacing. In preparations with a long SACT
(nos. 1-7), capture of dominant pacemaker fibers occurred only at pacing rates at least 14 + 3 beats/min
faster than spontaneous rhythm (range 12-20 beats/
min). In preparations with a rather short SACT (nos.
8-13), capture occurred at pacing rates 6 + 3 beats!
min faster than sinus rhythm (range 2-9 beats/min)
(table 1).
Sinus node acceleration during atrial pacing developed independent of the prematurity of the first paced
beat, as long as the spontaneous cycle and the pacing
cycle differed enough to influence the sinus node at all.
Determination of SACT
In 13 experiments, we compared true SACT, determined by intracellular "mapping," and estimated
SACT, determined by premature atrial stimulation and
constant atrial pacing (table 1). Premature atrial stimulation underestimates true SACT when estimation is
based on an atrial return cycle at transition from compensatory to noncompensatory pause (transition method).2 Estimated SACT derived from the length of
A2A3 after a curtailed cycle of 50% of A,A, tends to
overestimate true values. For constant atrial pacing,
TABLE 1. Electrophysiologic Data from 13 Experiments
Experiment
1
2
3
4
Cycle
length
(msec)
458
(msec)
67
455
515
500
460
470
510
475
408
390
370
402
362
58
44
50
38
44
55
28
28
23
20
16
24
SACT
APD
(msec)
170
192
176
190
160
148
180
164
142
124
116
100
122
153+30
Estimation of SACT
Constant pacing
5 bpm >
10 bpm > 20 bpm >
Premature stimulation
sinus rhythm
sinus rhythm
"Transition" 50% of AIA,
(msec)
(msec)
(msec)
(msec)
(msec)
50
10
20
72
36
43
36
15
5
6
37
17
7
31
13
8
45
25
9
34
15
10
52
22
11
29
16
12
28
12
13
40+13
20± 11
Mean ±SD
444±52
38± 16
*p < 0.05 vs true SACT.
Abbreviations: SACT = sinoatrial conduction time; APD = action potential duration.
39
13
36
22
18
32
15
20
18
22
18
17
15
22±8*
52
20
38
30
22
40
23
23
45
31
29
20
24
31+10
57
29
42
35
28
43
28
24
35
32
32
24
25
33±9
Capture
bpm >
sinus
rhythm
12
20
11
16
11
12
13
7
8
4
2
4
9
10±5
ACCELERATION OF SINUS RHYTHM/Haberl et al.
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
estimation of SACT depends on atrial pacing rate.
At stimulation rates only 5 beats/min faster than
sinus rhythm, true SACT was underestimated in 10 of
13 experiments, whereas in three experinents (nos.
10, 11 and 12), all with SACTs < 30 msec, est'imation
of SACT is correct. The pacemaker center in these
preparations is already captured at this slow pacing' rate
bec'ause they show little sinus node acceleration.
At stimulation rates 10 beats/min faster than sinus
rhythm, estimated values of SACT increased in general, in four preparations (nos. 9-12), all with a short
SACT (< 30 msec), leading to an overestimation.
However, in seven preparations with a long SACT (>
30 msec), the true values are still underestimated. All
of the latter preparations showed marked sinus node
acceleration, and the dominant pacemaker fibers were
not captured by the atrial impulses.
Pacing'at 20 beats/min faster causes a further increase in estimated SACT; the mean value (33 ± 9
msec) closely approaches true SACT. In single experiments, however, marked deviations from true SACT
are observed, ranging from an underestimation of 50%
(experiment 2) to an overestimation of 60% (experiment 11).
How sinus node acceleration during drive affects
estimation of SACT is illustrated in figure 3. The two
beats on the left are the last during a train of constant
atrial pacing (interval 410 msec), followed by two
spontaneous beats of sinus origin. The atrial return
cycle A2A3 after cessation of drive, subtracted by the
basic cycle (455 msec) and divided by two, gives an
estimated SACT of 24 msec; the true SACT, however,
is 58 msec. As explanation for this underestimation the
microelectrode recording shows that the atrial impulses fail to capture the pacemaker fiber (smooth transition from phase 4 to phase 0 depolarization). Furthermore, the sinus node return cycle S2S3 is reduced to
412 msec with respect to the basic cycle of 455 msec,
caused by an acceleration of both phase 0 depolarization and repolarization of the paced beat. Thus, sinus
node acceleration accounts for the serious underestimation of SACT at slow-rate atrial pacing.
In 12 experiments, we determined the relationship
between cycle length of atrial drive and CSNRT, as
a2
410
a2
t
502
a3
455
1371
shown in figure 4. Panel A includes six experiments
with true SACT > 30 msec. CSNRT (A2A3-A A )
increases continuously when the pacing cycle is shortened. Instead, the corrected recovery time of dominant
fibers (S2S3'-SS,) becomes negative (that is, the return cycle S2S3 after drive is shorter than spontaneous
cycle length) due to a shortening of action potential
duration. The maximum decrease- of 27 + 20 msec is
reached when the atrial cycle is curtailed by 50 msec,
coinciding with capture of the pacemaker center. Further curtailment slightly prolongs the CSNRT. Panel B
includes six experiments with true SACT < 30 msec.
As in panel A, CSNRT increased continuously when
the pacing cycle was decreased. In contrast to panel A,
however', the CSNRT of dominant fibers increased.
The preparations exhibit less sinus node acceleration
and, hence, are captured earlier during atrial drive and
consequently develop a more pronounced depression
of phase 4 depolarization.
Discussion
Electrotonic Interaction Between Atrium and Sinus Node
During atrial stimulation, the impulse propagates
retrogradely from the atrium into the sinus node.
Therefore, compared with spontaneous rhythm, depolarization and repolarization start earlier in fibers at
the border of the sinus node than in fibers of the pacemaker center. Since sinus node tissue is electrically
coupled,9' 10 different levels of transmembrane potentials at a given time will cause a current flow between
cells tending to minimize these differences. Because of
this electrotonic interaction, repolarization of dominant pacemaker fibers is accelerated compared with
spontaneous rhythm.2 Also, a premature ectopic atrial
beat penetrating the pacemaker area without capturing
it nonetheless shortens action potential duration of
dominant pacemaker fibers to that these fibers come to
next spontaneous discharge earlier than expected; electrotonic interaction between the atrium and the sinus
node during premature atrial stimulation explains why
transition from compensatory to noncompensatory
atrial return cycles does not indicate capture of the
pacemaker center.2' 3
During constant atrial pacing, exertion of an electro-
a4
FIGURE 3. Consequences of sinus node accelerationfor estimation of sinoatrial conduction time (SACT). The transmembrane potential of a dominant pacemaker,fiber (same as in
figures 1 and 2) is recorded together with the
crista terminalis electrogram. The basic cycle
length is 455 msec and true SACT 58 msec.
After a period of atrial drive (A2A2) thatfails to
capture the fiber (pacing interval 410 msec),
the atrial return cycle A2A3 amounts to 502
msec. Subtraction of the basic cycle and division by two leads to a unidirectional SACT of
only 24 msec. Phase 4 depolarization and
SACT after drive (S3A3) are not affected (S3S4
= S1S1 = A1A,).
CIRCULATION
1372
VOL 67, No 6, JUNE 1983
phase 4 to 0 depolarization becomes sharp, indicating
capture of dominant pacemaker fibers (fig. 1). The
degree of sinus rate acceleration varied from
maximal
100
to preparation (table 1). It appears that the
preparation
[-I
longer the true SACT, the longer the action potential
so
Atrium
duration during spontaneous rhythm, the more the
60
I
electrotonic interaction presumably occurs because of
,I
time difference of repolarization between fibers of
the
40
the border and pacemaker center, all of which leads to
20
a marked acceleration of rate, and vice versa (compare
8-13 isin surrounded
if a
table 1). Thus,
1-7 with
experiments
P
by very
location
u
certain pacemaker
9
~~~~~~~~Pacemaker Fiber
slowly conducting tissue (long SACT, long action po-20I IT T T
tential duration), the acceleration of rate will be most
I
l T T
pronounced.
1 1 1 1 1 1
-401
In 1965, Lange'2 described a temporary acceleration
60] 0____________________________________
10 20 30 40 50 60 70 80 90 160
within the sinoatrial pacemaker of the in situ dog heart
Curtailment [msec]
A
after cessation of slow-rate atrial drive. Lange also
"the ability of an intrinsic pacemaker to continnoted
Corrected Recovery Timne
when
SACTn<30
ue
actionwasandattempted."
even to accelerate
120
:6 msec
Pharmacologic
extrinsic drive
slowcompetitive
100
studies in this paper suggest that this acceleration is
J J
[mec]
due to release of catecholamines from tissue storage by
electrical stimulation. This mechanism of acceleration
T T I | 1
Atrium
60
is different from our topic: Electrotonic interaction
T
leads to acceleration up to the rate of imposed drive,
40
Pacemaker Fiber
I
but never above it, and the prior rate resumes upon
of drive.
20
20
~~~~~~~~~~~~cessation
The synchronization of pacemakers we report in this
0
1 1 1 1
study is strikingly similar to the increase of atrial flutter rate in man during atrial pacing - entrainment. 13 In
both instances, the intrinsic rhythm speeds up exactly
-20
to the rate of imposed drive, and resumes its original
-40rate upon termination of drive. It has been speculated
that a reentrant atrial rhythm might similarly be accel0 10 20 3'0 40 50' 60 70 80 90 100
erated by atrial pacing, 13' 14 which might better explain
Curtailment [msec]
of the atrial flutter waves.
the unchanged configuration
on
Ioe
phaenomn
of
ac elatrio during (anaso
FIGURE 4. Corrected recovery time as a function of the pacthe
of
so,
(and also
phenomenon
afafter)
ing interval expressed as curtailment (basic cycle minus pacing
of
can
heart
be
due to
the
stimulatnon
interval). Filled circles represent the mean of corrected recov-.. ~~~both electracal
an automatic and a reentrant mechanism.
ery time of the atrium + 1 SD (A2A3-A1A1); open circles indicate
the mean of corrected recovery time of a dominant pacemaker
Calculation of SACT by Atrial Pacing
fiber - 1 SD (S2S3-S1SI)- SACT = sinoatrial conduction time.
Because of electrotonic interaction, spontaneous sinus rhythm speeds up to the rate of imposed atrial
tonic influence by the atrial wave, which either closely
drive, until, with further increase of pacing rate, shortapproaches or captures the pacemaker center, can he
ening of action potential duration can no longer counexpected to occur with every beat. In a previous experterbalance the shortened cycle of atrial drive, leading
imental microelectrode study comparing true SACT
to capture of dominant sinus node fibers. Thus, capture
with SACT estimated by constant atrial pacing, the
of the pacemaker area by atrial pacing at rates slightly
sinus rate accelerated during atrial pacing at a rate 5
above sinus rhythm as the major prerequisite of the
beats/min faster than spontaneous rhythm in a minority
validity of the method4 is not met. This event explains
of experiments; its mechanism remained unclear.'1
the serious underestimation of true SACT when a pacOur study is the first to describe acceleration of
ing rate 5 beats/min faster than sinus rhythm is chosen
sinus rhythm due to electrotonic interaction without
(table 1). Most likely it accounts for rather low values
capture of the pacemaker as a consistent finding during
of SACT reported in man when a rate approximately 3
slow-rate atrial pacing. Most of the increase of sinus
beats/min faster than sinus rhythm was chosen for
rate is caused by acceleration of repolarization; howevmeasurement.'5 Narula and co-workers used a pacing
rate 7 + 3 beats/min faster than sinus rhythm (range 2er, with somewhat higher pacing rates, there is also
some acceleration of the process of phase 0 depolariza11 beats/min) and recommended a drive rate of 10
beats/min faster.4 Our study showed that with variabiltion, until with even higher pacing rates transition from
Corrected Recovery Timfe
120
SACT >30msec
n:6
II I I I I
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
accelerathon durtng
I
A
A
A A
ACCELERATION OF SINUS RHYTHM/Haberl et al.
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
ity from one experiment to another, seven of 13 preparations were not captured by a pacing rate 10 beats/
min faster (table 1). This variability is expected to
increase when diseased sinus node function in man is
studied. One may argue that a pacing rate 10 beats/min
faster than sinus rhythm represents a more rapid rate
for overdrive at a spontaneous heart rate of 70 beats/
min in man, compared to a spontaneous rate of 135
beats/min in the isolated rabbit heart. One might also
speculate that with slower heart rates in man, the action potential duration of sinus node cells would be
longer, disparity of repolarization between border and
dominant pacemaker fibers during atrial drive larger
and, hence, acceleration more pronounced. Sinus node
acceleration in man cannot be predicted quantitatively,
but we expect from our study that this phenomenon in
man might prevent sinus node capture at pacing rates
commonly used to estimate SACT.
The premature atrial stimulation and constant atrial
pacing methods showed further inadequacies, such as
shortening of action potential duration of captured
sinus node cells,2 differences between SACT and atriosinus conduction time,2' 3, 16 depression of diastolic
depolarization and pacemaker shifts after stimulation,'7' '8 as previously described.'" Thus, although
constant atrial pacing is simpler and quicker to perform
than the premature atrial stimulation procedure, it does
not improve our ability to determine sinoatrial conduction time accurately in man.
Acknowledgment
We gratefully acknowledge careful review of the manuscript by Dr.
M.A. Allessie and the skillful technical assistance of Regine Pulter and
Elisabeth Nowak.
References
1. Strauss HC, Saroff AL, Bigger JT Jr, Giardina EGV: Premature
atrial stimulation as a key to the understanding of sinoatrial conduction in man. Circulation 47: 86, 1973
1373
2. Miller HC, Strauss HC: Measurement of sinoatrial conduction time
by premature atrial stimulation in the rabbit. Circ Res 35: 935,
1974
3. Steinbeck G, Allessie MA, Bonke FIM, Lammers WJEP: Sinus
node response to premature atrial stimulation in the rabbit studied
with multiple microelectrode impalements. Circ Res 43: 695, 1978
4. Narula OS, Shanba N, Vasquez M, Towne WD, Linhart JW: A
new method for measurement of sinoatrial conduction time. Circulation 58: 706, 1978
5. Gomes JAC, Kang PS, El-Sherif N: Effects of digitalis on the
human sick sinus node after pharmacologic autonomic blockade.
Am J Cardiol 48: 783, 1981
6. Kang PS, Gomes JAC, El-Sherif N: Differential effects of functional autonomic blockade on the variables of sinus nodal automaticity in sick sinus syndrome. Am J Cardiol 49: 273, 1982
7. Alboni P, Malcame C, Pedroni P, Masoni A, Narula OS: Electrophysiology of normal sinus node with and without autonomic
blockade. Circulation 65: 1236, 1982
8. Rakovec P, Jakopin J, Rode P, Kenda MF, Horvat M: Clinical
comparison of indirectly and directly determined sinoatrial conduction time. Am Heart J 102: 292, 1981
9. Bonke FIM: Electrotonic spread in the sinoatrial node of the rabbit
heart. Pfluegers Arch 339: 17, 1973
10. Seyama I: Characteristics of the rectifying properties of the sinoatrial node cell of the rabbit. J Physiol (Lond) 255: 379, 1976
11. Grant AO, Kirkorian G, Benditt DG, Strauss HC: The estimation
of sinoatrial conduction time in rabbit heart by the constant atrial
pacing technique. Circulation 60: 597, 1979
12. Lange G: Action of driving stimuli from intrinsic and extrinsic
sources on in situ cardiac pacemaker tissues. Circ Res 17: 449,
1965
13. Waldo AL, MacLean WAH, Karp RB, Kouchoukos NT, James
TN: Entrainment and interruption of atrial flutter with atrial pacing.
Circulation 56: 737, 1977
14. Watson RM, Josephson ME: Atrial flutter. I. Electrophysiologic
substrates and modes of initiation and termination. Am J Cardiol
45: 732, 1980
15. Breithardt G, Seipel L: Comparative study of two methods of
estimating sinoatrial conduction time in man. Am J Cardiol 42:
965, 1978
16. Steinbeck G, Haberl R, Luderitz B: Effects of atrial pacing on atriosinus conduction and overdrive suppression in the isolated rabbit
sinus node. Circ Res 46: 859, 1980
17. Bonke FIM, Bouman LN, van Rijn HE: Change of cardiac rhythm
in the rabbit after an atrial premature beat. Circ Res 24: 533, 1969
18. Steinbeck G, Luderitz B: Sinoatrial pacemaker shift following
atrial stimulation in man. Circulation 56: 402, 1977
Acceleration of sinus rhythm during slow-rate atrial pacing.
R Haberl, G Steinbeck and B Luderitz
Downloaded from http://circ.ahajournals.org/ by guest on June 17, 2017
Circulation. 1983;67:1368-1373
doi: 10.1161/01.CIR.67.6.1368
Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1983 American Heart Association, Inc. All rights reserved.
Print ISSN: 0009-7322. Online ISSN: 1524-4539
The online version of this article, along with updated information and services, is located on
the World Wide Web at:
http://circ.ahajournals.org/content/67/6/1368
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally
published in Circulation can be obtained via RightsLink, a service of the Copyright Clearance Center, not the
Editorial Office. Once the online version of the published article for which permission is being requested is
located, click Request Permissions in the middle column of the Web page under Services. Further
information about this process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Circulation is online at:
http://circ.ahajournals.org//subscriptions/