Intercaval Block in Normal Canine Hearts
Role of the Terminal Crest
Ruediger Becker, MD; Alexander Bauer, MD; Stephan Metz, MD; Ralf Kinscherf, PhD;
Julia C. Senges, MD; Kirsten D. Schreiner, MD; Frederik Voss, MD;
Wolfgang Kuebler, MD, FACC; Wolfgang Schoels, MD
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Background—The intriguing monotony in the occurrence of intercaval conduction block during typical atrial flutter
suggests an anatomic or electrophysiological predisposition for conduction abnormalities.
Methods and Results—To determine the location of and potential electrophysiological basis for conduction block in the
terminal crest region, a high-density patch electrode (10⫻10 bipoles) was placed on the terminal crest and on the
adjacent pectinate muscle region in 10 healthy foxhounds. With a multiplexer mapping system, local activation patterns
were reconstructed during constant pacing (S1S1⫽200 ms) and introduction of up to 2 extrastimuli (S2, S3). Furthermore,
effective refractory periods were determined across the patch. If evident through online analysis, the epicardial location
of conduction block was marked for postmortem verification of its endocardial projection. Marked directional
differences in activation were found in the terminal crest region, with fast conduction parallel to and slow conduction
perpendicular to the intercaval axis (1.1⫾0.4 versus 0.5⫾0.2 m/s, P⬍0.01). In the pectinate muscle region, however,
conduction velocities were similar in both directions (0.5⫾0.3 versus 0.6⫾0.2 m/s, P⫽NS). Refractory patterns were
relatively homogeneous in both regions, with local refractory gradients not ⬎30 ms. During S3 stimulation, conduction
block parallel to the terminal crest was inducible in 40% of the dogs compared with 0% in the pectinate muscle region.
Conclusions—Even in normal hearts, inducible intercaval block is a relatively common finding. Anisotropic conduction
properties would not explain conduction block parallel to the intercaval axis in the terminal crest region, and obviously,
refractory gradients do not seem to play a role either. Thus, the change in fiber direction associated with the terminal
crest/pectinate muscle junction might form the anatomic/electrophysiological basis for intercaval conduction block.
(Circulation. 2001;103:2521-2526.)
Key Words: atrial flutter 䡲 atrium 䡲 conduction 䡲 electrophysiology 䡲 mapping
T
he intriguing monotony in the occurrence of intercaval
conduction block during typical atrial flutter seems to
indicate either an anatomic or an electrophysiological predisposition for conduction abnormalities. Experimental1–5 and
clinical studies6 –14 suggest that the terminal crest (TC) forms
the anatomic substrate underlying intercaval conduction
block. The well-known anisotropic conduction properties of
the TC would readily explain conduction block perpendicular
to but not parallel to the intercaval axis because of a reduced
safety factor for propagation longitudinal to the fiber direction.15 Studies in isolated atrial preparations seem to indicate
that conduction delay and block from the TC to the pectinate
muscle region result from anatomic determinants such as
collagenous septa16 and/or inhomogeneities in the distribution
of gap junctions.17,18 Alternatively, electrophysiological determinants such as refractory gradients might play a role,
although not apparent in in vitro preparations.2 On the basis
of the hypothesis that the TC forms the anatomic substrate for
functional conduction block across the intercaval region,
conduction and refractory properties in the intercaval component of the TC and its ramifications into the right atrial
appendage were studied in normal dogs to determine the
anatomic location of and the potential electrophysiological
basis for intercaval conduction block.
Methods
All animal experiments conformed to the “Position of the American
Heart Association on Research Animal Use” adopted November 11,
1984.
Model Preparation
Ten healthy foxhounds (31⫾6 kg body weight) were anesthetized
with intravenous pentobarbital (0.5 mg/kg), intubated, and ventilated
with nitrous oxide and oxygen (70%/30%). ECG leads I, II, and III
were continuously monitored on a VR 12 recorder (Electronics for
Medicine). The heart was exposed through an extended midsternal
approach, and the pericardium was removed. During all experiments,
body temperature was adjusted to 37°C with a heating lamp.
Received November 8, 2000; revision received January 12, 2001; accepted January 19, 2001.
From the University of Heidelberg, Department of Cardiology, and the Department of Anatomy III (S.M., R.K.), Heidelberg, Germany.
Correspondence to Ruediger Becker, MD, University of Heidelberg/Department of Cardiology, Bergheimer Str 58, 69115 Heidelberg, Germany. E-mail
[email protected]
© 2001 American Heart Association, Inc.
Circulation is available at http://www.circulationaha.org
2521
2522
Circulation
May 22, 2001
TABLE 1.
Conduction and Refractory Parameters
TC Region
Pectinate Muscle
Region
P*
CTpara(ms)/CVpara(m/s)
16⫾8/1.1⫾0.4
34⫾20/0.5⫾0.3
⬍0.05
CTperp(ms)/CVperp(m/s)
33⫾12/0.5⫾0.2
28⫾8/0.6⫾0.2
NS
⬍0.01
NS
ERP, ms
104⫾10
108⫾12
⬍0.01
ERPgrad, ms
10⫾8
9⫾8
NS
P*
CVpara indicates conduction velocity parallel to the intercaval axis; CVperp,
conduction velocity perpendicular to the intercaval axis; and ERPgrad, local
gradients of the ERPs.
*Student’s t test for unpaired data.
S2 and S3 stimulation (S2/S3⫽ERP⫹10 ms) from the anterior margin
of the patch for the TC and pectinate muscle region, respectively. If
conduction block was evident, the epicardial location of block was
marked with 2 needles at both edges of the patch for postmortem
analysis of its endocardial projection.
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Histology
Figure 1. Lateral view on right atrial wall. Position 1, multielectrode in TC region; position 2, multielectrode in pectinate muscle region. SVC indicates superior vena cava; RAA, right atrial
appendage; IVC, inferior vena cava; and ⫹, pacing site.
Mapping Technique
For high-resolution mapping of the in situ canine lateral right atrial
wall, a custom-designed, square patch containing 10⫻10 bipoles
(interelectrode distance, 1.5 mm) was sutured epicardially on the
intercaval component of the TC (Figure 1, position 1) and on the
adjacent pectinate muscle region (Figure 1, position 2). A Biotronik
UHS 20 stimulator (Biotronik GmbH&Co KG) was used for pacing
and determination of effective refractory periods (ERPs). Mapping
data were simultaneously processed through a 256-channel multiplexer and recorded on videotape for offline digitization and computer analysis (bandwidth, 20 to 500 Hz; sampling rate, 1000 Hz).
The mapping system used was developed at the University of
Limburg (Maastricht, the Netherlands).19 At each recording site,
local activation time (AT) was determined automatically on the basis
of the maximal first derivative as in comparable previous studies.1,20
Each marking was reviewed and manually revised if necessary. In
multiphasic signals lacking a sharp intrinsic deflection, the peak of
the major deflection was chosen as the moment of activation. ATs
were calculated relative to the pacing artifact. From these ATs, 2D
isochronal activation maps were constructed manually at 10-ms
intervals. As detailed previously, conduction block was assumed if
the AT of adjacent electrode sites differed by ⱖ40 ms and if local
electrograms in respective regions showed characteristic double
potentials.1,20 Areas of slow conduction were defined as areas of
crowded isochrones comprising ⱖ3 consecutive electrode sites, with
adjacent electrode sites separated by ⱖ1 isochronal line.1,20
Study Protocol
In the TC and in the pectinate muscle region, the following protocol
was applied. First, activation patterns were determined, and conduction times (CTs) for the TC and pectinate muscle region were
calculated during constant pacing from the superior (parallel to
intercaval axis) and posterior (perpendicular to intercaval axis)
margins of the patch, respectively, at a cycle length of 200 ms
(Figure 1). Second, local ERPs were measured along a line of 10
adjacent electrodes across the center of the patch perpendicular to the
intercaval axis. After 8 basic stimuli at twice the diastolic threshold
(S1), an extrastimulus (S2) was introduced, decreasing the S1S2
coupling interval in steps of 10 ms. The ERP was defined as the
maximum S1S2 interval that failed to evoke a propagated atrial
response. Third, activation patterns were reconstructed online during
After atriotomy, specimens containing the intercaval component of
the TC, together with the transition to the sinus venarum (SV)
(posteriorly) and the pectinate muscles (anteriorly), were fixed in 4%
paraformaldehyde (24 hours at 4°C) and rinsed in 10 mmol/L PBS (3
times over 24 hours at 4°C), followed by conventional alcohol
dehydration and methacrylate embedding according to the user
instructions for Kulzer Histo-Technique (Heraeus Kulzer). Sections
(7 ␮m) were cut parallel to the epicardial surface toward the
endocardium on a microtome (Leica) and routinely stained either
with hematoxylin-eosin or azan.
Photographs were taken with a Zeiss-Axiomat camera on Agfapan
25 professional film (Agfa-Gaevert). The photographs were
mounted, and the regions of interest, particularly the transition of the
TC to the SV and to the pectinate muscles, were analyzed.
Statistical Analysis
Data are presented as mean⫾SD. Comparative statistics were performed by use of Student’s t test for paired and unpaired data. A
value of P⬍0.05 was considered statistically significant.
Results
Conduction Properties During S1 Stimulation
In the TC region, marked directional differences in CT/
conduction velocity were found, with significantly faster
conduction parallel to compared with perpendicular to the
intercaval axis. In the adjacent pectinate muscle region,
however, no statistically significant directional differences in
CT were encountered, although there was a tendency toward
faster conduction perpendicular to the intercaval axis. The
data are summarized in Table 1. In Figure 2, typical activation patterns from both regions have been selected, displaying
very fast conduction along the TC (Figure 2A) compared with
relatively slower propagation perpendicular to the intercaval
axis in the TC region (Figure 2B) and in the pectinate muscle
region, where similar activation patterns and CTs were
evident almost independently of the direction of impulse
propagation.
Effects of S2 and S3 Stimulation on Conduction
Perpendicular to the Intercaval Axis
Compared with S1 stimulation, conduction perpendicular to
the intercaval axis was significantly delayed during S2 stim-
Becker et al
High-Resolution Mapping of Terminal Crest Region
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Figure 2. Activation patterns during S1 stimulation. A, TC region;
B, pectinate muscle region; top, propagation parallel to intercaval axis; bottom, propagation perpendicular to intercaval axis.
SVC indicates superior vena cava; CT, CT across patch; IVC,
inferior vena cava; -u-, pacing site. See text for further details.
ulation in both the TC and the pectinate muscle region (Table
2). However, no evidence of conduction block was found in
any dog. During S3 stimulation, conduction perpendicular to
the intercaval axis was further delayed compared with S2
stimulation (Table 2), but no complete conduction block
occurred in the pectinate muscle region. In the TC region,
however, S3 stimulation induced lines of conduction block
parallel to the intercaval axis in 4 of 10 dogs (P⬍0.05 versus
pectinate muscle region). As a result, S3 stimulation more
markedly prolonged CTs in the TC than in the pectinate
muscle region (Table 2). In dogs exhibiting conduction block
at S3 stimulation, CT perpendicular to the intercaval axis at S1
stimulation was significantly longer than in dogs without
conduction block (36⫾7 versus 24⫾2 ms, P⬍0.05). In Figure
3, typical examples of activation patterns are displayed that
were obtained during extrastimulation in the TC (Figure 3A)
and in the pectinate muscle region (Figure 3B) and are
complemented by original electrogram tracings. In the pectinate muscle region (Figure 3B), conduction spread centrifugally and homogeneously from the pacing site at the anterior
edge toward the posterior edge of the patch and toward both
TABLE 2. Conduction Times Perpendicular to the Intercaval
Axis During S1, S2, and S3 Stimulation
CT S1, ms
CT S2, ms
CT S3, ms
TC region
33⫾12
60⫾17*
78⫾18†
Pectinate muscle region
28⫾8
54⫾12*
60⫾15‡
*P⬍0.001 vs CT S1; †P⬍0.01 vs S2; ‡P⬍0.05 vs S2 (Student’s t test for
paired data).
2523
Figure 3. Activation patterns during S3 stimulation in TC (A) and
pectinate muscle region (B) (dog 6). Conduction block is represented by heavy solid lines. E5 through E95 are electrode numbers. See text for further details. Abbreviations as in Figure 2,
plus EG indicates electrograms.
sides, with the CT across the patch delayed to a greater extent
during S3 compared with S2 stimulation (65 versus 54 ms).
Activation patterns were otherwise very similar. In the TC
region (Figure 3A), conduction was more markedly delayed
during S2 stimulation, particularly in the central part of the
multielectrode; however, no complete conduction block occurred. With the introduction of a second extrastimulus (S3),
a line of conduction block was encountered separating the
third from the fourth row of electrodes on the superior and the
fourth from the fifth row of electrodes on the inferior margin
of the patch, respectively. The direction of activation in the
area distal to the block was changed markedly, displaying a
pattern consistent with 2 colliding wavefronts entering
through both sides of the patch. Postmortem examination
revealed that the epicardial line of block exactly matched the
endocardial location of the TC (Figure 4). This was true for
all dogs exhibiting complete conduction block.
In a subgroup of dogs (n⫽5), extrastimulation was performed from both the anterior and posterior margins of the
multielectrode (distance between anterior and posterior pacing sites and TC, 4.5 to 9 mm and 3 to 6 mm, respectively).
In 2 of those dogs, complete conduction block across the TC
was inducible. In both of them, the location of the block was
independent of the site of pacing, as illustrated in Figure 5.
Refractory Patterns Across the Intercaval Axis
Refractory patterns were relatively homogeneous both in the
TC and in the pectinate muscle region. Local ERP gradients
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May 22, 2001
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Figure 5. Activation maps obtained during S2 and S3 stimulation
in dog 2. Left, Pacing from posterior margin of patch; right, pacing from anterior margin of patch; top, S2 stimulation; bottom,
S3 stimulation. Line of block (heavy solid line in bottom maps)
remains in same location regardless of pacing site. Abbreviations as in Figure 2.
Figure 4. Endocardial view of TC region of dog 6. Endocardial
projection of line of block shown in Figure 3 exactly matches
course of TC, as indicated by 2 needles marked by arrows. SUP
indicates superior; INF, inferior.
did not exceed 30 ms in both areas, with no obvious
differences in the frequency or distribution of peak gradients.
Mean refractory gradients did not differ either (Table 1).
However, mean ERP was slightly longer in the pectinate
muscle compared with the TC region (Table 1). Even in areas
with proven conduction block during S3 stimulation, there
was no systematic decrease or increase in local refractoriness,
and no significant refractory gradients could be observed.
Histology
To elucidate the role of regional ultrastructure for the occurrence of conduction block, arrangement and continuity of
muscle bundles, as well as distribution and amount of
connective tissue, were analyzed in multiple sections of the
TC and its transition to the pectinate muscles and to the SV.
Sections were obtained in steps of ⬇100 ␮m from epicardial
to endocardial layers. A representative example is depicted in
Figure 6. Histological findings in a dog with (dog 6) and a
dog without (dog 10) conduction block are shown for
comparison. In both animals, the TC consisted of a broad
band of parallel muscle bundles. Within these bundles, the
muscle cells were closely packed, and branches of smaller
bundles were ramified toward the pectinate muscle region
and toward the SV. In both dogs, the muscle bundles
continued from the TC to the pectinate muscles over a
thickness of ⬇1000 ␮m. No obvious differences were observed between both dogs in terms of arrangement and
continuity of muscle cells at the ramification area between the
TC and pectinate muscles. Both gradual changes in fiber
direction with longitudinally contacting muscle cells and
abrupt changes with orthogonally contacting muscle cells
were found in each dog (Figure 6A and C). The transition
between the TC and the SV was not as regular as the
transition between pectinate muscles and the TC; however,
continuous connections between the muscle fibers were
always present (Figure 6B and D); the muscle bundles were
less tightly arranged, and the amount of connective tissue was
increased considerably. Generally, no clear boundary between the TC and SV was seen in both animals (Figure 6B
and D). Within the connective tissue, the muscle cells were
connected in a netlike manner. In summary, obvious histological differences potentially explaining the occurrence of
conduction block could not be demonstrated. This was true
not only for the arrangement of muscle bundles in the TC and
its transition toward both the pectinate muscles and the SV
but also for the arrangement and amount of connective tissue.
Discussion
To the best of our knowledge, this is the first high-resolution
mapping study to specifically compare directional conduction
and refractory properties in the intercaval component of the
TC and its ramifications into the right atrial appendage. Not
only were we able to confirm the markedly anisotropic
conduction properties of the TC region previously suggested
Becker et al
High-Resolution Mapping of Terminal Crest Region
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Figure 6. TC region in dog 6 with (A and B) and dog 10 without (C
and D) conduction block. A, Midmyocardial layer. At transition
between TC and pectinate muscles (PM), muscle fibers approaching TC in perpendicular direction gradually change their direction
when continuing into TC. B, Subepicardial layer. Regularly
arranged muscle cell bundles from TC spread irregularly into SV.
C, Midmyocardial layer. At transition between TC and pectinate
muscles, muscle cell bundles approaching TC in perpendicular
direction contact orthogonally. D, Midmyocardial layer. Transition
between TC and SV is gradual. Final magnification, 70-fold.
by multipolar electrode catheter recordings, but we also
demonstrated that conduction velocities perpendicular and
transverse to the intercaval axis do not differ significantly in
the adjacent pectinate muscle region, probably because of a
more complex, nonuniform anisotropic texture. Furthermore,
apart from significantly delaying conduction perpendicular to
the intercaval axis in both the TC and the pectinate muscle
region, the use of 2 extrastimuli (S2S3) induced functional
conduction blocks exactly overlying the TC in 40% of dogs.
In contrast, no evidence of complete conduction block was
ever encountered in the pectinate muscle region. With respect
to the mechanism of conduction block, refractory gradients
are unlikely to play a role, because ERPs and peak refractory
gradients did not differ significantly between both regions.
Our data confirm the hypothesis that the TC provides an
anatomic basis for rate-dependent conduction block, even in
normal canine hearts. Although histological studies failed to
demonstrate an obvious relation between the occurrence of
conduction block and both the distribution of connective
tissue and the myocardial texture in the TC or its boundaries,
the change in fiber direction at the TC/pectinate muscle
junction may still form an anatomically determined basis for
conduction abnormalities, consistent with the concept of
nonuniform anisotropy.
2525
tion delay and split potentials, suggesting that the TC forms
an anatomic substrate for functional conduction block across
the intercaval region.6 –14 Combining high-resolution mapping
with postmortem analyses in normal dogs, we could confirm
that rate-dependent conduction block epicardially coincides
with the endocardial projection of the TC and that this
phenomenon was rather common even in normal hearts
(40%). Pacing from both the anterior and posterior margins of
the multielectrode in a subgroup of dogs (n⫽5) ruled out an
additional line of block in the adjacent SV region.21 In
contrast to the TC region, no evidence of conduction block
was found in the adjacent pectinate muscle region in any dog.
The well-known anisotropic conduction properties of the TC
would readily explain conduction block perpendicular to but
not parallel to the intercaval axis because of a reduced safety
factor for propagation longitudinal to the fiber direction.15
However, experimental studies analyzing conduction properties in isolated TC preparations have elucidated that changes
in the direction of cellular connections relative to the direction of propagation predispose to unidirectional conduction
block.2,4 Specifically, branch sites of pectinate muscles from
the TC,4 particularly with acute angles,2 were suggested to
predispose to conduction block, probably because of an
increase in effective axial resistivity.4 Histology performed in
the present study did not demonstrate systematic differences
in myocardial texture at the transition between the TC and
pectinate muscles; of note, branch angles exhibited a marked
intraindividual variation through the different myocardial
layers, rendering a direct relation between the acuity of
branch angles and the occurrence of conduction block very
unlikely. However, independent of specific branch angles, the
change in fiber direction may represent an area of nonuniform
anisotropy prone to conduction block. Although this study
failed to demonstrate obvious differences in amount or
distribution of connective tissue, collagenous septa might also
play a role.16 As suggested by previous experimental findings, the predisposition of the TC for conduction block might
be related to a characteristic distribution of gap junctions;
specifically, a preponderance of end-to-end and a relative
paucity of side-to-side connections have been described that
apparently are associated with a characteristic distribution of
the channel proteins connexin 40, 43, and 45.17,18 These
findings provide an alternative explanation for transverse
conduction block across the TC.
Theoretically, the occurrence of conduction block across
the TC could also be related to specific refractory patterns.
Studies in isolated atrial preparations have been inconsistent
with respect to the presence of refractory gradients across the
TC.2,5 Our findings in whole animals argue against a contribution of refractory gradients to the genesis of conduction
block, at least under physiological conditions. Refractory
gradients were generally insignificant, and above all, the TC
region did not differ from the pectinate muscle region with
respect to peak and mean local refractory gradients despite
obvious differences in the propensity for conduction block.
Comparison With Other Studies
Using multipolar mapping catheters to study conduction
perpendicular to the intercaval axis in patients with atrial
flutter, previous studies have demonstrated marked conduc-
Methodological Considerations
The mapping area was limited to the intercaval component of
the TC and its ramifications into the right atrial appendage,
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May 22, 2001
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and conduction in the smooth-walled intercaval myocardium
was not analyzed. The findings presented must be considered
specific to this particular region and do not necessarily apply
to other sections of the TC.
As far as the differentiation between marked slow conduction
and conduction block is concerned, various criteria have been
extensively studied and discussed in earlier high-resolution
mapping studies.22,23 Accordingly, the criteria used in the present
study have been established and widely used in comparable
mapping studies. However, it still remains difficult to differentiate with certainty between marked slow conduction and conduction block. In anisotropic atrial preparations, minimal CTs in
the range of 0.04 to 0.12 m/s have been measured during
impulse propagation transverse to the fiber direction compared
with 1.0 to 1.3 m/s longitudinal to the fiber direction.4 Theoretically, marked slow conduction therefore might have been
misinterpreted as complete conduction block. However, independent of definitions, conduction delay as marked as this forms
a potential basis for reentrant arrhythmias and as such is
expected to exert similar functional effects.
Because of the limited size of the multielectrode used, the
length of induced conduction blocks could not be determined,
because all blocks approached or exceeded the dimensions of the
patch (ⱖ15 mm). Furthermore, the inducibility of atrial
tachyarrhythmias was not systematically studied. This could
have helped us to appreciate potential functional effects of
conduction abnormalities.
Clinical Implications
The inducibility of functional conduction block across the TC even
in normal canine atria supports the hypothesis of an anatomically
determined predisposition to conduction abnormalities, thus providing the substrate for a central obstacle in a macroreentrant circuit.
The presence of an anatomically determined substrate for reentry
might explain the occasional occurrence of (typical) atrial flutter in
healthy individuals.24,25 Although the TC obviously provides a
potential central obstacle, right atrial pathology such as pressure
load, dilatation, or fibrosis probably induces or enhances regional
conduction delay, thus potentially facilitating the occurrence of
atrial flutter in diseased atria. In the presence of an anatomically
determined substrate for conduction block, the cavotricuspid “isthmus” region remains the primary target site for therapeutic interventions such as radiofrequency ablation.26
Acknowledgments
This study was supported by a grant of the Deutsche Forschungsgemeinschaft, Bonn, Germany, within the Sonderforschungsbereich
320 Herzfunktion und ihre Regulation, University of Heidelberg,
Heidelberg, Germany. The contribution of Juergen Metz, MD,
Department of Anatomy III, University of Heidelberg, is gratefully
acknowledged. Furthermore, we are indebted to Patricia Kraft for
valuable technical assistance.
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Intercaval Block in Normal Canine Hearts: Role of the Terminal Crest
Ruediger Becker, Alexander Bauer, Stephan Metz, Ralf Kinscherf, Julia C. Senges, Kirsten D. Schreiner,
Frederik Voss, Wolfgang Kuebler and Wolfgang Schoels
Circulation. 2001;103:2521-2526
doi: 10.1161/01.CIR.103.20.2521
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