Relationships between myocardial activity and potentials on the ventricular surfaces

Journal of Electrocardiology Vol. 30 Supplement

Relationships B e t w e e n Myocardial Activity and Potentials on the Ventricular Surfaces

Bruno Taccardi MD, PhD, Bonnie B. Punske, PhD, Robert L. Lux, PhD, Robert MacLeod, PhD, Philip R. Ershler, PhD, Theodore J. Dustman, and Nicole Ingebrigtsen

The electrical activity of the heart can be studied in h u m a n patients by recording electrical signals from the surface of the body, from the epicardial surface at surgery, and from the endocardial surface during catheterization. Among body surface recordings, body surface potential maps (BSPMs) provide more information than can be obtained from the 12-lead electrocardiogram (ECG) (1). However, BSPMs offer only a limited capability of resolving multiple intracardiac events, because the potential at every point on the body surface is a weighted sum of contributions from electrical sources distributed throughout heart. In addition, the conducting volume interposed between the heart and the body surface has an irregular shape and nonhomogeneous conductivity. As a result, BSPMs are smoothed and distorted reflections of intracardiac and epicardial potential distributions. Thus at present, visual inspection and statistical analysis of BSPMs do not enable us to reconstruct the three-dimensional sequence of epicardial and intracardiac events with a sufficient degree of certainty. A far greater a m o u n t of information on the electrical activity of the heart can be obtained by recording electrical signals directly from the epicardial and/or endocardiaI surface, as is discussed in greater detail below. However, both epicardial and endocardial mapping suffer from a n u m b e r of limitations, one of which is invasiveness. Epicardial mapping requires open-chest surgery. Endocardial mapping involves lengthy catheterization sessions, or introduction into the ventricular cavities of multielec-

From the Nora Eccles Harrison Cardiovascular Research and Training Institute, Utah University of Utah, Salt Lake City.

Supported by National Institutes of Health Grant R01 HL43276-08 and by awards from the Nora Eccles Treadwell Foundation and the Richard A. and Nora Eccles Harrison Pund for Cardiovascular Research. Reprint requests: Bruno Taccardi, MD, PhD, Cardiovascu]ar Research and Training Institute, CVRTI,The University of Utah, Building 500, Salt Lake City, UT 84112. ©1998 Churchill Livingstone ® 0022-0736/300S-0001 $5.00/0

trode arrays that require cardiopulmonary bypass (2). However, recently introduced basket catheters obviate the need for cardiopulmonary bypass. Also, recent advances in solving the inverse problem of electrocardiography make it possible to compute epicardial potentials noninvasively from body surface ECGs albeit at the cost of some loss of resolution and accuracy (3). Similarly, endocardial potentials and isochrones can be inversely computed from multielectrode noncontact probes introduced into the ventricular cavities (4). Another limitation is the difficulty of inferring intramural events, which applies to both epicardial and endocardial maps. As stated by Gulrajani et al. (5) "...the primary intracardiac sources cannot be uniquely determined from surface measurements as long as the active region is inaccessible, since the electric field that they generate outside any closed surface enclosing them may be duplicated by equivalent single- or double-layer sources on the closed surface itself." This problem was considered as long ago as 1853 by Helmholtz (6) and in 1982 by Yamashita {7). However, the indeterminacy of the inverse problem {in terms of intracardiac electric sources) can be removed, at least in principle, if we know the distribution of fiber directions and the electrical properties of the fibers (eg the conductivity tensors) in the entire heart (8). In accordance with this theoretical prediction, recent studies with experimental animals (9) and numerical simulations (10, 11) have shown that epicardial and endocardial potential distributions and excitation time maps convey a great deal of information about intramural events, if the maps are interpreted in the light of present day knowledge of fiber architecture, anisotropic propagation, and electric properties of the current generators associated with excitation and recovery. In this report we discuss the electrophysiologic information that can be obtained from epicardial and endocardial electric signals, and we also address the problem of extracting intramural information from surface measurements. To study the relationships between surface and intramural events, it is necessary to examine both

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Journal of Electrocardiology Vol. 30 Supplement

surface and intramural signals obtained from experimental animals and mathematical models.

Materials and Methods Epicardial Mapping In addition to studying epicardial maps published by other investigators, we recorded epicardial maps by applying Nylon socks, carrying 64-1,200 electrodes, to the ventricular surface of exposed or isolated dog hearts. Electrograms were recorded in banks of 256 or 512 signals at a time during atrial drive or ventricular pacing from as m a n y as 90 epicardial or intramural sites in the same animal. Equipotential contour maps and excitation time maps were obtained by using special software developed at our institution. i

Intramural and Endocardial Mapping isolated dog hearts were suspended in a warm chamber or in an electrolytic tank. In some experiments, the right ventricular wall was surgically removed to expose the interventricular septum. From 50 to 150 intramural needles, each of which carried 10 electrodes along its shaft, were inserted into the left and right ventricular free walls or into the left wall and septum. Electrograms from the needle electrodes were used to compute potential distributions and excitation times on the epicardial surface, in the thickness of the wall, and on the endocardium. Intracavitary activity was also recorded by inserting noncontact cylindrical probes carrying 50-100 electrodes into the right or left ventricular cavity.

Results In this section we discuss the electrophysiologic information yielded by epicardiaI and endocardial maps as obtained by us and by other investigators. Epicardial excitation time maps show whether the epicardiaI spread of excitation is normal or abnormal. In 1979, W y n d h a m et al. (12) recorded epicardial excitation time maps in 11 h u m a n subjects without conduction disturbances. In a typical case, the maps showed the location and time of occurrence of three epicardial breakthrough sites (two on the right ventricle), which could not be inferred from body surface recordings. In five subjects with left bundle branch block (13), excitation propagated slowly on the left ventricle, where no epicardial breakthroughs were observed. In experimental animals, high-resolution electrode arrays made it possible to describe epicardial excitation in greater details. Thus, Arisi et al. (I4) detected up to 35 epicardial breakthrough sites in canine hearts during normal propagation by using 1,124 epicardial electrodes. The same group (15) showed that during epicardial pacing, epicardiaI maps exhibited a clear-cut sep-

aration between a "primary" area, where excitation propagated through working myocardium as a continuous wave spreading from the pacing site, and a "secondary" area, where excitation arrived through the intervention of the Pnrkinje network. Unpublished data from this laboratory show that regional conduction disturbances, experimentally produced by locally inactivating the conduction system, can be localized with great accuracy by means of epicardial maps. In 5-day old experimental myocardial infarctions, Berbari et al (16) recorded QS-shaped unipolar electrograms from the infarcted area, with local spikes revealing delayed epicardial conduction in some regions. Importantly, epicardial reentry pathways in ventricular tachycardias were clearly revealed by epicardial excitation time maps (17). Endocardial maps have also been used to demonstrate the normal or abnormal spread of excitation in the left or right ventricular endocardium (18) and the site of preexcitation in the Wolff-Parkinson-White syndrome. Recent work by Osswald et al. (19) showed that during sustained m o n o m o r p h i c ventricular tachycardia, reentry can often be observed in both epicardial and endocardial excitation time maps. In these cases, the intramural depth of the exit site was assessed by comparing the earliest activation time in epicardial and endocardiaI maps. Reentry was deemed to be epicardial w h e n the earliest epicardial activation was at least l0 ms earlier than the earliest endocardial activation, and vice versa. If the endocardial and the epicardial earliest excitation times differed by less than 10 ms, intramural reentry was assumed. In case of septal reentry, similar criteria were applied by Boineau et al. (2) to endocardial maps recorded from both sides of the interventricular septum. However, there are cases in which epicardial and/or endocardiaI electrograms, excitation time maps, and potential maps recorded during normal sinus rhythm do not reveal intramural abnormalities (eg, localized necrosis). In an experimental study by Watabe et aI. (20), small nontransmural necroses were induced by applying laser energy or by injecting small amounts of formalin in the left ventricular wall in i3 dogs. In several cases of deep necrosis, epicardial electrograms, excitation time maps and potential maps recorded during sinus r h y t h m did not show clear-cut abnormalities. However, previous studies based on the analysis of epicardial potentials during paced beats (9) provided a tool for revealing an otherwise silent intramural necrosis. In those studies, epicardial potential maps recorded from normal hearts during epicardial, intramural, or endocardial stimulation showed characteristic patterns, which made it possible to Iocalize the site and depth of pacing, and also revealed whether excitation was spreading in an epicardiaI to endocardial direction or vice versa. Owing to the anisotropic electrical conductivity of the heart muscle, conduction velocity is faster along fibers than across fibers (21). As a consequence, an excitation wave front elidted by point stimulation assumes an approximately eIIipsoidal shape, with the major axis aligned with the local fiber direction. Also, because of anisotropy, the

Myocardial Activity andVentricular Surface Potentials spreading wave front does not produce positive potentials in all the regions toward which it s spreading. When the stimulus is applied on the exposed epicardial surface, potential maxima and ECG R waves appear, in the early stages of propagation, only in those regions toward which excitation is spreading along fibers (9). In later stages of propagation, the excitation wave front spreads on the surface of the heart and also into the thickness of the wall. Here, the wave front encounters fibers whose direction progressively rotates counterclockwise, by approximately 120 ° on average in the left ventricle and by 70-80 ° in the right ventricle. Thus, the direction of fast propagation rotates counterclockwise from epicardium to endocardium and the intramural wave front assumes a helical shape (10,1I). Because of the abovementioned mechanism, the intramural position of the potential maxima must also rotate counterclockwise from epicardium to endocardium, thus creating a spiral region of high positive potential facing those portions of the deep wave front that move along fibers at increasing depth. The presence of the spiral positive region has been observed experimentally (22) and in numerical simulations (1 I). Interestingly, the deep rotation of the positive areas produces a far-field effect on epicardial potential, which also show two counterclockwise-rotating positive formations after epicardial pacing. The same mechanism produces a clockwise rotation of the epicardial positivity after endocardial pacing and a double rotation (both clockwise and counterclockwise) after midwall pacing (9). However, if the wave front encounters a necrotic area while it is spreading in the thickness of the wail, the corresponding positivity will be missing, as will its epicardial reflection. Therefore, we expected that the epicardial rotation of the positive areas would show a localized interruption or gap in the presence of intramural necroses. The gap in the rotating epicardial positivity was indeed observed in the experiments of Watabe et al. (20), which showed that intramural necroses can be revealed by mapping epicardial potentials during epicardiaI stimulation. The size of the gap increased with increasing size of the necrotic area, and the location of the gap rotated counterclockwise relative to the pacing site with increasing depth of the necrosis. These experiments require epicardial paring and mapping, and it m a y be difficult to apply the same procedure to h u m a n patients. However, it is interesting to note that endocardial potential distributions exhibited the same features previously observed in epicardial maps, namely, the rotation of the initial maxima as a function of intramural pacing depth and the rotation-expansion of the positive areas during later stages of intramural propagation (4). Further experimentation will be necessary to establish whether the gap in the rotating positivity associated with intramural infarctions can also be observed in endocardial maps. As stated before, these maps can be computed from ECGs recorded with noncontact intraventricular probes during a single heart beat. In a n o t h e r series of experiments, we created a superficial b u r n over a 2 - 4 cm 2 area on the left or right

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ventricular surface. In the b u r n e d area, epicardial ECGs had a QS configuration, similar to that observed in transmural myocardial infarctions. The necrosis, however, involved only a 2 - m m thick myocardial layer. This was confirmed by pacing from intramural needles inserted in the b u r n e d area. Here again, epicardial potential maps recorded during epicardial pacing revealed a continuous counterclockwise rotationexpansion of the m a x i m a in the b u r n e d area, which suggests that conduction in the underlying myocardial layers was normal.

Discussion The experimental data reported above provide only limited examples of the electrophysiologic procedures that make it possible to infer intramural activity from epicardial or endocardial data. Electrical signals recorded from the cardiac surfaces during spontaneous sinus r h y t h m convey a great deal of information and help in detecting local abnormalities of excitation and recovery. Model data by Colli-Franzone et al. (10, 11) show that the distribution of the magnitudes of the velocity vectors on the epicardial surface varies as a function of pacing depth and also suggest the location of the subendocardial Purkinje-myocardial junctions during normal sinus rhythm. In addition, excitation time maps and potential maps recorded during ventricular pacing reveal the local direction of the fibers (9,22,23), including the epicardial/ endocardial obliqueness of fiber direction (24). In summary, epicardial and endocardial maps provide significant information about intramural events, particularly if they are recorded during epicardiaI or endocardial pacing and are interpreted in light of our knowledge of fiber architecture and anisotropic electrical properties of the heart muscle.

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