EXPERIMENTAL STUDIES
Double component action potentials in the posterior approach to the atrioventricular node: do they reflect activation delay in the slow pathway?
Jacques M. T. de Bakker, PhDa*  ,
Peter Loh, MDa* ,
M.élèze Hocini, MDa* ,
Bernard Thibault, MDa* and
Michiel J. Janse, MDa*
a Department of Experimental Cardiology, Academic Medical Center, Amsterdam, The Netherlands
* Interuniversity Cardiology Institute of the Netherlands, Utrecht, The Netherlands
Heart Lung Institute, University of Utrecht, Utrecht, The Netherlands
Manuscript received January 26, 1998;
revised manuscript received March 2, 1999,
accepted April 9, 1999.
Reprint requests and correspondence: Dr. Jacques M.T. de Bakker, Department of Experimental Cardiology, Academic Medical Center, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands
j.m.debakker{at}amc.uva.nl
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Abstract
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OBJECTIVES
The aim of the study was to elucidate the mechanism of double component action potentials in the posterior approach to the atrioventricular (AV) junctional area.
BACKGROUND
Double component action potentials are often associated with activation delay and therefore might be a marker of the location of the so-called slow pathway.
METHODS
The AV junction was scanned for double component action potentials in Langendorff perfused pig and dog hearts, using conventional microelectrode recordings. Characteristics of these action potentials were investigated during basic and premature stimulation and cooling of the anterior approach to the node.
RESULTS
During basic stimulation, double component action potentials were recorded in 19 out of 20 hearts. In 74% of these cases, the second component occurred before the His deflection. During premature stimulation this percentage was 50%, while delay between the two components always increased. In 80% of the cases, the amplitude of the two components became <20 mV during progressive shortening of the coupling interval. The first component was generated by activation in superficial layers, the second one by activation in deeper layers. Cooling of the anterior region revealed that the second component was caused by activation arriving from the anterior region.
CONCLUSIONS
Double component action potentials in the posterior approach to the AV node are generated by the asynchronous arrival of wave fronts in different, weakly coupled layers or by the summation of asynchronously arriving wave fronts. They are not always associated with activation delay in the slow pathway.
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Abbreviations and Acronyms
| | AV | = atrioventricular | | CS | = coronary sinus | | DAM | = Diacetyl monoxime | | IU | = international units | | IM | = intramuscular | | IV | = intravenous | M | = mega Ohm |
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Double component action potentials point to asynchronous depolarization and reflect activation delay between adjacent sites. These action potentials are often associated with discontinuities in cardiac structure and have been recorded at sites where a mismatch exists between current demand and current supply. This happens at isthmus sites (1,2) or regions where activation fronts curve (3). Transfer of activation via inexcitable gaps or a coupling too weak for active conduction also give rise to double component action potentials (4,5). They may also result from the asynchronous arrival of activation fronts at a point where anyone of these wave fronts alone would be blocked (5).
Double component action potentials are a common finding in the atrioventricular (AV) junctional area, including the posterior approach to the node, the presumed location of the so-called slow pathway (6–9). Because their occurrence is often associated with activation delay, it is challenging to find out if double component action potentials point to activation delay in the slow pathway. The purpose of this study was to characterize the double component action potentials in the posterior approach to the AV node and to delineate the underlying mechanism.
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Methods
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Measurements were carried out in isolated, Langendorff-perfused dog and pig hearts conformed to the guiding principles of the American Physiological Society and according to the following protocol. During basic stimulation from either a posterior or an anterior site, the AV junctional area was scanned with a microelectrode for double component action potentials. These are defined as action potentials revealing a distinct change in the upstroke velocity, indicating electrotonic interaction between two cells. Diacetyl monoxime (DAM) was added to the perfusate to dampen cardiac contractions. Whenever double component action potentials were recorded, or if the action potential revealed a rounded tip, suggestive of double, closely-coupled components, premature stimulation was applied. Recording sites yielding double component action potentials were tagged with a fine needle for histologic investigation.
Preparation of the hearts.
Eight New Yorkshire pigs, 6 to 8 weeks old, weighing 18 to 25 kg and 12 mongrel dogs, 2 to 4 years old, weighing 20 to 30 kg were used. Animals were premedicated with azaperon (12 mg/kg intramuscular [IM]) and atropine (500 mg IM), then anaesthetized with sodium pentobarbital (35 mg/kg intravenous [IV]) and metomidaat (5 mg/kg IV). After endotracheal intubation, animals were ventilated with room air, and heparin (5,000 IU IV) was given. One liter Tyrode’s solution was infused via a peripheral vein. A midline sternotomy was performed, and a large-bore needle was inserted into the cranial vein for the collection of 1 to 2 l blood/Tyrode’s solution mixture, which was later used to perfuse the heart. The heart was excised and rinsed in cold Tyrode’s solution. The aortic root was cannulated and perfused with a Langendorff apparatus as described previously (10). Perfusion was at constant pressure (60 cm H2O); flow ranged between 60 and 150 ml/min. The temperature of the heart was maintained at 37°C (within 1°C) by warming the perfusate and by partially surrounding the heart with a heating jacket.
A Y-shaped incision was made in the superior vena cava and anterolateral wall of the right atrium to expose Koch’s triangle. Bipolar pacing and recording electrodes were positioned: - on the anterior region, 1 cm above the tendon of Todaro,
- on the posterior region, 1 cm posterior from the ostium of the coronary sinus, and
- on the right ventricular wall.
Stimulation was done at a basic cycle length of 600 or 500 ms (in one case, at 450 ms). Stimulus strength was 2 times threshold and pulsewidth was 1 ms. Extracellular signals were amplified 500 times and bandpass-filtered between 0.1 and 500 Hz. Electrograms were displayed on a four-channel oscilloscope (Tektronix 2214) and recorded on an eight-channel digital recorder (DTR 1801, Biologic).
Intracellular recordings.
Microelectrode recordings were made using conventional techniques. Tip-resistances of the microelectrode ranged from 15 to 30 mega Ohm (M). The reference electrode was placed close to the microelectrode. Because it is not possible to achieve stable microelectrode impalements in blood-perfused mammalian hearts because of the vigorous cardiac contractions, 1 to 2 g of DAM was added to the perfusate to dampen cardiac contraction. Diacetyl monoxime in the concentration of 10 to 20 mmol/l has a marked negatively inotropic effect but has little effect on the action potential. The effects of DAM on AV conduction have been described previously (11).
Cooling the anterior region.
In three hearts, the anterior region was cooled at the site where the atrial exit was located during retrograde conduction. The cooling probe consisted of a stainless steel tube with a diameter of 3 mm and a length of 10 cm. The tube was closed at the end in contact with the myocardium. A second, open-ended tube 10 cm long and 2 mm in diameter was inserted into the first tube, to a point 1 cm from its lower end. The probe was cooled by pumping ice-water through the inner tube. The coolant was retrieved via the mantel between the inner and outer tube at a rate of 100 ml/min. In this way, the tip of the probe could be cooled to a temperature of 4°C. The probe was mounted in a micromanipulator for accurate positioning.
Histologic investigations.
Histologic studies were performed on three hearts. In these hearts, pins with a diameter of 0.3 mm were impaled at sites revealing double component action potentials during basic stimulation. From the areas including the tagged sites, sections were made perpendicular to the tricuspid valve annulus. Sections were stained with sirius red and elastic van Gieson stains and examined by light microscopy.
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Results
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Double component action potentials.
Action potentials with double components were recorded from 80 sites in 19 of the 20 hearts. Cells revealing double component action potentials had the following characteristics: resting membrane potentials ranging from –56 to –91 mV (mean –74 mV), maximal upstroke velocity ranging from 20 to 180 V/s (mean 91 V/s) and action potential amplitude ranging from 56 to 112 V/s (mean 76 mV). These action potentials were preferentially recorded in the area between the CS orifice and the tricuspid valve annulus almost up to the middle of the triangle of Koch (the posterior approach to the AV node). In 18 hearts, they appeared both during basic and premature stimulation but in one heart during premature stimulation alone. During basic stimulation, delay between the two components could be as large as 60 ms, but it could increase to 150 ms after premature stimulation.
Premature stimulation.
Whenever double component action potentials were present during basic stimulation, delay between the two components increased after premature stimulation (Fig. 1). The tracing in the middle shows action potentials with double upstrokes evoked during basic stimulation (S1) and after an early coupled stimulus (S2). Stimulation was performed from a posterior site. Progressive shortening of the S1 to S2 interval yielded action potentials with increasing delay between the two components (lower tracings in Fig. 1). Delay between the premature stimulus and the upstroke of the first component remained almost unchanged.
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Figure 1 Upper tracing: extracellular recording from the His bundle region. Middle tracing: action potentials with a double upstroke recorded in the posterior aspect of the AV node during basic stimulation (S1) with a cycle length of 500 ms followed by an early coupled stimulus (S2). The heart was stimulated from a posterior site. Lower tracings: Action potentials recorded after a premature stimulus with a coupling interval of 1) 310, 2) 290 and 3) 280 ms, respectively. Delay between the first and the second component of the action potential increased and the amplitude of the second component decreased with prematurity. Delay between the stimulus and the first upstroke remained virtually the same. Activation evoked after the extra of 280 ms was blocked toward His. This presents a rather exceptional case. Inset: schematic drawing of the AV junctional area, showing the recording site. A = atrial deflection; CFB = central fibrous body; CS = orifice of coronary sinus; H = His deflection; ME = microelectrode; TT = Tendon of Todaro; TVA = tricuspid valve annulus; V = ventricular deflection.
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The amplitude of the action potentials decreased with increasing prematurity of the extra stimulus. A coupling interval of 280 ms (tracing 3) resulted in an intracellular complex exhibiting two humps with amplitudes of 20 and 25 mV. Such low amplitude complexes (<25 mV) that are unlikely to participate in conduction were elicited after early coupled stimuli at 13 of 16 sites, despite the observation that activation conducted toward His.
Superficially versus deeply located cells.
Double component action potentials could be recorded both in cells located directly beneath the endocardium (superficially located cells) and cells from deeper layers. An example is presented in Fig. 2. The action potential recorded from a cell located in the superficial layer had a low upstroke velocity (tracing marked superficial). A small dip 110 ms after stimulus S1 (bold arrow in first complex) suggested the presence of a second component. The latter was more easily distinguished after premature stimulation (arrow in second complex).
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Figure 2 Upper tracing: extracellular electrogram from the His bundle region. Lower tracings are action potentials recorded from the same endocardial site after the last basic stimulus (S1) and an early coupled stimulus (S2). The tracing marked superficial shows the action potential from a cell located in a superficial layer (directly beneath the endocardium). The tracing marked deep shows the action potential from a cell located at a deeper level. Both tracings show double components during basic stimulation (S1), but the notch in the superficial tracing (bold arrow) becomes more distinct after the premature stimulus (S2). The main (first) component of the action potentials of the superficial tracing has a low upstroke velocity. The timing corresponds with the first, low amplitude deflection of the action potentials from the deeper tracing (open arrow). The main (second) component of the deeper tracing has a high amplitude and fast upstroke velocity. The timing corresponds with the notches marked by the bold arrow in the superficial tracing. The inset shows the endocardial location of the microelectrode. The dips following the bold arrows are artifacts caused by the reference of the microelectrode. Abbreviations as in Figure 1.
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The action potential recorded from a deeper-located cell at the same endocardial location also revealed two components (tracing marked deep in Fig. 2). The first one (open arrow) had a low amplitude and a low upstroke velocity and its timing corresponded with the main upstroke of the action potential recorded from the superficially located cell. This deflection, too, became more pronounced after premature stimulation. The main (second) upstroke of the action potential recorded from the cell located in a deeper layer was fast. The timing of this deflection corresponded with the dip in the action potential derived from the superficially located cell.
Histologic investigation.
Figure 3 shows the histology of an area in the posterior approach to the AV node where the microelectrode registered double component action potentials. The site where the microelectrode penetrated the endocardium is indicated by an arrow. The subendocardial layers, which harbored the tip of the microelectrode, revealed small myocardial bundles (dark areas) separated by fibrous tissue (white areas). Cells in these bundles often had the morphologic characteristics of transitional cells; they were deprived of cross striation. This is compatible with the observations made by McGuire and Truex (11,12).
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Figure 3 Section from the area beneath the endocardial site where the microelectrode from Fig. 2 was impaled. The section was cut perpendicular to the tricuspid valve annulus. The arrow indicates the insertion site. The area consists of strands of myocardial cells widely separated by connective tissue (light areas). Most cells are deprived of cross striation, indicative of transitional cells. A = atrium; E = endocardium; V = ventricle. Scale 0.5 mm.
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Anterior versus posterior stimulation.
During basic stimulation a change in the site of stimulation from posterior to anterior affected the configuration of the double component action potentials only marginally. Differences were more pronounced during premature stimulation. The delay between the two components of the action potentials was always less during stimulation from a posterior site. The effectiveness of posterior stimulation was always greater than that of anterior stimulation, evidenced by conduction block toward His occurring at shorter coupling intervals of the premature stimulus.
Relation with the His deflection.
The first upstroke of the double component action potential always occurred before the His deflection. The upstroke of the second deflection, however, ensued after His in 16 out of 62 impalements (26%) during basic stimulation and in 8 of 16 impalements (50%) after premature stimulation. This suggested that activation generating that second component did not participate in AV conduction in these cases.
Cooling of the anterior exit site.
In three hearts we cooled the anterior region at the site that proved to be the atrial-exit during retrograde conduction. Microelectrodes were impaled in the posterior approach to the AV node. The distance between the cooling probe and the site where the microelectrode was impaled ranged from 0.5 to 1 cm. A decrease in temperature resulted in an increase of the delay between the stimulus artifact and the second component of the double component action potential (Fig. 4, upper tracings). The interval between the stimulus and the upstroke of the first component did not change. The delay increased with decreasing temperature.
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Figure 4 Tracings are intracellular recordings made during cooling of the anterior area of the AV junction (Panel A). This area was the atrial exit during retrograde conduction. Recordings were made during posterior stimulation at three instants during the cooling procedure: 1) baseline, no cooling, 2) 30 s of cooling, 3) 60 s of cooling. A double component is present during baseline (tracing 1). Delay between the first and second components of the action potential increases with cooling. Delay between the stimulus and the first component remains the same. The inset shows the location of the cooling probe and the recording electrode. The distance between the center of the cooling probe and the endocardial site where the microelectrode was impaled was 5 mm. The tracing, marked His, shows the extracellular electrogram from a site overlying the bundle of His and was made 90 s after starting the cooling procedure (Panel B). At this level of cooling Wenckebach periodicity occurred. The lower tracing (ME) shows the microelectrode recording in the posterior region. Note that the two components do not change with the Wenckebach periodicity. Abbreviations as in Figure 1.
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During cooling, increasing the stimulation frequency resulted in Wenckebach periodicity of the AV conduction (Fig. 4, His tracing). In contrast, Wenckebach periodicity did not occur in the double component action potentials (ME tracing).
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Discussion
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The classical concept of AV conduction suggests that the anatomical substrate consists of two pathways (slow and fast) within the AV junctional area, each with different conduction velocities and refractory periods (13–15). The demonstration of discontinuous conduction-time curves in human and dog hearts and the results of radiofrequency catheter ablation for treatment of AV junctional tachycardias have been accepted as evidence for this concept (14–19). There is no evidence that anatomically delineated dual pathways exist within the atrioventricular nodal area (20).
Many studies support the supposition that the slow pathway is located in the posterior approach of the AV node (14,21–24). Because analysis of human and animal hearts fails to reveal anatomical evidence for these pathways, it islikely that they are functionally determined. Some intrinsic factors have been proposed to affect conduction of the impulse through the node. These include automaticity, fiber direction and geometry, anisotropy, ionic currents, summation and inhomogeneous conduction (25,26). The specific relationship between these factors and AV nodal conduction has, however, never been established.
Double component action potentials are associated with activation delay between adjacent sites and are often recorded in the posterior approach to the AV node. Therefore, they could serve as an indicator for the location of the slow pathway.
Action potentials with double components.
Double component action potentials may be caused by (Fig. 5): - activation at discontinuities: This is the case when there is electrotonic impulse transmission over an inexcitable or high resistance gap (panel a), which has been described in depressed Purkinje and myocardial fibers (4). Transmission of activation at isthmus sites, where a small bundle inserts into a large bundle, also gives rise to double component action potentials (panel b). At the isthmus the large bundle represents a high load for the relatively weak wave front generated by the small bundle (1), which results in activation delay. If propagation occurs at the discontinuity, at least one of the deflections in the action potentials will reach threshold (panel c). In case of activation block, only single deflections remain (panel d).
- asynchronous arrival of activation: A weak coupling between bundles through which activation propagates asynchronously (panel e) and summation of asynchronously arriving activation fronts at a point where any single wave front would be blocked (panel f) may also give rise to double component action potentials (panel g). In these instances, however, both components may become subthreshold (panel h).
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Figure 5 Schematic drawings illustrating how double component action potentials may arise. An activation front (arrows) that passes a discontinuity, being a high resistance gap (panel a), or a site with impedance mismatch (panel b) generates double component action potentials at sites before (1) and after (2) the discontinuity (panel c). Because this process is active, at least one of the components has a large (suprathreshold) amplitude. When activation blocks at the discontinuity, only one deflection remains (panel d). A weak coupling between bundles (panel e) or summation of activation in branching structures (panel f) also gives rise to double component action potentials. When the wave fronts (arrows) are propagating in these structures, the configuration of the generated action potentials is similar to those that arise at high resistance gaps or sites with a load mismatch. When, however, wave fronts are dying, double component action potentials with subthreshold amplitudes may arise (panel h). 1 and 2 indicate recording sites.
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The observation that delay between the two components increases after premature stimulation argues in favor of the concept that double component action potentials are caused by activation arriving at discontinuities. This, however, does not fit in with the observation that in virtually all cases the amplitudes of both components become <20 mV with increasing prematurity. The latter favors the concept of asynchronous propagation of activation in poorly coupled sheets or bundles of transitional cells or the asynchronous arrival of converging wave fronts. In such cases premature stimulation may give rise to increased delay of the second component as well.
Relation with slow pathway conduction.
Arguments in favor of the hypothesis that double component action potentials in the posterior approach to the AV node reflect activation delay related to AV nodal transmission are: 1) in 74% of the cases the second component preceded the His bundle deflection during basic stimulation and in 50% during premature stimulation, and 2) with premature stimulation, delay of the second component and delay of the His bundle potential increased more or less equally.
However, in 26% of the cases during basic stimulation and in 50% of those during premature stimulation, the second component occurred after the His bundle potential. In such cases, the double component action potential probably belonged to a dead-end pathway and did not contribute to antegrade conduction to the His bundle. In our view this argues against the notion that these potentials arise in the slow pathway, which is supposed to ensure atrium–His conduction of premature impulses that are blocked in the fast pathway. In these cases, the double components could still be due to the asynchronous arrival of converging wave fronts in a dead-end pathway or the asynchronous arrival of wave fronts in different weakly coupled layers. Arguments for the latter possibility are provided by the experiments in which posterior and anterior approaches to the AV node were cooled. Cooling of the posterior area hardly affected the timing of the two components, whereas cooling of the anterior area delayed the second component, suggesting influence of deeper layers. A third explanation for a second component occurring later than the His bundle potential could be (concealed) reentry. We cannot prove this, because atrial echo beats were never observed.
Coupling between superficially and deeply located cells.
There was a major difference in the origin of the two components in the action potentials. The earliest component was recorded from cells directly beneath the endocardium, whereas late components were always generated by depolarization of cells in deeper layers. Histologic investigations carried out at sites with double component action potentials revealed a subendocardial zone of mainly transitional cells. Although light microscopy did not reveal sharply demarcated layers, it showed clusters of cells and single strands interspersed with connective tissue. This architecture may represent the layered structure, in which small strands serve as the weak coupling between larger cell clusters. McGuire et al. (27) have shown that there is a discrepancy between histologic and electrophysiologic characteristics in the AV junction, which was explained by differences in connexin 43 content in superficial and deeper layers. Because connexin 43 determines the coupling between cells, these differences in its distribution may also well account for variations in coupling strengths and create preferential pathways.
Limitations of the study.
Atrioventricular conduction in dog and pig hearts shows many characteristics comparable to those in human hearts. Slow potentials and slow pathway potentials have been described in human as well as animal hearts (11,21,22,28) and ventricular echo beats can be induced in nearly all dog hearts. Although discontinuous AV nodal conduction curves are a rare finding in animal hearts, dual pathway physiology can often be proved. In all of our experiments, conduction curves were smooth, which may indicate that the architecture of the animal hearts differs from that of human hearts, especially those with AV nodal reentry tachycardias. Another problem, because of the lack of discontinuous conduction curves, was our inability to indicate at which coupling interval slow pathway conduction started. In patients with a smooth conduction curve, Sheahan et al. (29) found an increase in the atrium–His (AH) delay beyond 70 ms, at which point they presume slow pathway conduction begins. In our study we found that, at short coupling intervals of the premature stimuli, the AH interval increased by more than 70 ms in most cases. Although we cannot be sure that AV characteristics in the human heart and those in the animal hearts we studied are comparable, in light of Sheahan’s data, it seems conceivable that slow pathway conduction was present at short coupling intervals.
Recordings were made both from superficial and deeper layers, but it has been shown that the maximum-depth of impalements in the AV junctional area of rabbit hearts is no more than a few hundred micrometers (30). Therefore, we have no information from deeper layers that might constitute the slow pathway.
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Footnotes
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This study was partly funded by the Dutch Heart Foundation (Grant 94.137).
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Abstract
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