A STUDY OF SUBSTANCES WHICH ALTER INTRAVENTRICULAR CONDUCTION IN THE ISOLATED DOG HEART. Received for publication December 7, 1956
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1 A STUDY OF SUBSTANCES WHICH ALTER INTRAVENTRICULAR CONDUCTION IN THE ISOLATED DOG HEART HENRY H. SWAIN AND CHARLES L. WEIDNER2 Department of Pharmacology, University of Michigan Medical School, Ann A rbor Received for publication December 7, 1956 The transmission of the cardiac impulse to the various parts of the ventricles involves both the regular myocardial fibers and the specialized or so-called Purkinje network. When the ventricles are driven electrically and conduction times are measured to several epicardial electrodes, it is possible to estimate the conduction velocities in these two conductile tissues. Thus Lewis and Rothschild (1915) demonstrated that conduction between electrodes close to the site of stimulation is relatively slow. They assumed that an impulse arising at the epicardium would have to travel a certain distance through the slowly conducting myocardial fibers before it could reach and utilize the more rapidly conducting Purkinje fibers. Therefore transmission for short. distances along the epicardial surface of the heart would involve only the slow system, and conduction times to near-by electrodes would reflect this slow conduction velocity. They estimated that the regular myocardial fibers in the dog ventricle conduct at a rate of 300 to 500 mm./sec. When these investigators drove the ventricle at a greater distance from the recording electrodes, they noted that the iritraelectrode conduction time became much shorter. This, they believed, reflected the conduction time in the Purkinje network between their electrodes. Their estimate of Purkinje conduction velocity was 3000 to 5000 mm./sec. Moe and Mendez (1951) used a somewhat similar technique to demonstrate that strophanthin K in toxic doses slows Purkinje conduction at a time when myocardial conduction is not significantly altered. They related this preferential effect of strophanthin K on the high-speed system to the ability of the drug to induce ventricular fibrillation. Many investigators have measured the effects of drugs upon ventricular conduction velocity, but in the main, they have not differentiated between effects on myocardial conduction and effects on Purkinje conduction. Because some agents alter conduction in the two systems to different degrees or even in different directions, it seemed germane to observe both the myocardial and Purkinje effects of conduction-altering substances. 1 This investigation was supported in part by a grant from the Michigan Heart Association and in part by Grant H-2466 from the National Institutes of Health, Public Health Service. 2 Summer Research Fellow, National Fund for Medical Education, June-August, 1955, Medical Student Research Fellow, United States Public Health Service, Grant % FG-l54, December 1955-May
2 138 SWAIN AND WEIDNER FIG. 1. Circuit diagram. Stimulator with stimulus isolation unit (SIU) drives right ventricle through bipolar clip electrode. Synchronization lead (SYNC) connects stimulator to oscilloscope (SCOPE). A common ground connects stimulator, oscilloscope, and the metal tracheal cannula (TRACH. CAN.) of the heart-lung preparation. Alligator clips fastened to the epicardium are connected to a terminal block. The Y-input lead connects one recording electrode at a time to the oscilloscope. Sketch at right shows the square-wave stimulus artifact, upward and downward defiections, and at far right, the beginning of the T-wave. Conduction time (CT.) is measured in milliseconds. METHODS. The dog heart-lung preparation was employed in these studies. Subject dogs weighed between 8 and 12 kgm. and were anesthetized with intravenous sodium pentobarbital, 30 mgm./kgm. Donor dogs received no general anesthetic agent but were exsanguinated from an arterial cut-down performed under local procaine anesthesia. The blood of both subject and donor dogs was rendered non-coagulable with Mepesulfate,3 20 mgm./kgm. After the pericardium was opened, a bipolar clip electrode was fixed onto the epicardial surface of the right ventricle toward its apical end, as shown in figure 1. This bipolar electrode was driven by a Grass (Model 3-C) square-wave stimulator through a stimulus isolation unit (5113). Occasionally the parameters of stimulation were changed for specific reasons as mentioned, but unless otherwise stated the heart was driven at a rate of 192 beats per minute with 20 volt square-wave shocks 1 millisecond in duration. After the stimulating electrode was affixed to the heart, the S-A node was crushed in a large hemostat to slow the spontaneous rate of the heart. Local electrograms were obtained from a row of seven small alligator clips placed as indicated in figure 1. Wires were passed from the alligator clips to a terminal block, and Mepesulfate Roche is the registered trade mark of Hoffmann-LaRoche Inc. for the sodium salt of sulfated polygalacturonic acid methyl ester methyl glycoside.
3 INTRAVENTRICULAR CONDUCTION 139 from there each electrode was connected in turn to the Y-input of a cathode ray oscilloscope. The circuit was completed by grounding the oscilloscope to the metal tracheal cannula of the heart-lung preparation. The sweep of the oscilloscope was triggered by the Grass stimulator, and the X-amplitude was adjusted so that the one-tenth inch horizontal scale division was equal to 4 msec. With such a sweep speed, the entire depolarization complex can be observed on the oscilloscope at one time, and the arrival of the propagated impulse at a given electrode can be timed to 1 msec. Although only one recording electrode is in the circuit at any one time, readings from all seven can be obtained in less than half a minute. The typical unipolar electrogram as sketched in figure 1 includes a stimulus artifact at the left, an upward deflection, a downward deflection, an isoelectric segment, and, off the screen to the right, an upright T wave. The time of arrival of the propagated impulse at the recording electrode was taken as that point between the upward and downward deflections where the tracing crosses the base-line. Early in an experiment local injury caused by the clip electrodes is manifested by an elevation of the S-T segment. This local effect disappears within ten to fifteen minutes, and control readings are not taken until the S-T segment has returned to the base-line. Distances from the stimulating electrode to the several recording electrodes were measured with a pair of dividers and a millimeter ruler. Repeat measurements on the beating heart check within 2 mm. Conduction times to the several recording electrodes were plotted against the distances of these electrodes from the stimulating electrode. Control readings consistently form two straight lines. Readings from electrodes within the first 20 to 25mm. determine a line with a slope corresponding to a conduction velocity of 450 to 650 mm./sec. Readings from more distant electrodes determine a second line with a slope corresponding to a conduction veloc - ity of 1500 to 4000 mm./sec. The former is assumed to be a reflection of myocardial conduc. tion velocity and the latter a reflection of Purkinje conduction velocity. With this preparation we can measure changes in myocardial and Purkinje conduction velocities. In addition we can see an indication of any marked increase in automaticity which may be induced by the agents studied. After the S-A node was crushed the hearts had spontaneous rates in the range of 100 to 120 beats per minute. Such hearts will follow electrical stimulation of the ventricle at rates of 130 to 160 beats per minute without the appearance of spontaneous beats. Since our preparations were driven at the rate of 192 beats per minute, spontaneous beats rarely were seen under control conditions. However, certain substances in addition to their effects upon conduction increase the automaticity of the heart to the point that the usual driving frequency will no longer maintain control. Under these circumstances increasing the driving frequency to 220 to 250 beats per minute may eliminate spontaneous beats. By noting the driving frequency required to suppress spontaneous beats, we have a rough indication of the automaticity of the heart. The preparation is quite stable, after the first fifteen minutes during which the local injury effects are disappearing. If no drugs are given and temperature is constant, no conduction time changes of more than 2 msec. are observed during the next hour. RESULTS. Effects of the parameters of stimulation. Voltage: The threshold for ventricular driving was found to be between 2 and 6 volts in the various preparations. At these lower voltages there appears to be an appreciable latency between the application of the stimulus and the initiation of a propagated response, as indicated by an intercept on the X-axis of the conduction graphs (see figure 2). With increasing voltage, the curve is shifted to the left and shows an intercept on the Y-axis. This suggests that the shocks of greater intensity are capable of initiating a propagated impulse at some small distance removed from the stimulating electrode. A stimulus of 20 volts was employed routinely because at this value small voltage changes have little effect upon conduction times.
4 140 SWAIN AND WEIDNER 50 C.;). VOLTAGE CONDUCTION TIME-MSEC. FIG. 2. Effect of variation of voltage. Slope of left hand portion of each curve is myocardial conduction velocity. Greater slope at. right is Purkinje conduction velocity. Dotted extrapolation of 3 V curve intercepts X-axis, indicating a latency between application of minimal stimulus and initiation of propagated impulse. Dotted extrapolation of 30 V curve intercepts Y-axis, indicating that at higher voltage, propagated impulse is started several millimeters away from stimulating electrode. Duration: Shocks of less than 0.1 msec. duration were found to be -ineffective for driving the ventricle. Variation of shock duration from 0.1 to 20 msec. pro duced no change in conduction times to the several recording electrodes. A shock of 1 msec. duration was used in these studies. Frequency: Conduction times were found to be constant though the heart rate was varied from 120 to 250 beats per minute. This agrees with the findings of Lewis and Rothschild (1915). At very high rates of stimulation the cardiac output is markedly decreased, as would be expected. The effect of temperature. As would be expected, conduction velocities are a function of temperature. The circulating blood can be cooled to about 30#{176} C., and this procedure slows both myocardial and Purkinje conduction, as shown in figure 3. Below 30#{176} C. the cardiac output of the preparation is so low that there is no necessary relationship between the temperature of the blood in the inflow cannula (where we measure it) and the temperature of the blood in contact with the heart. Elevating the blood temperature to 42#{176} C. produces a corresponding increase in the two conduction velocities. Since conduction is temperature-sensitive, results were discarded when the temperature of the circulating blood changed as much as 0.5#{176} C. between control and experimental observations. Effects of cations. The chloride salts of sodium, calcium, and magnesium prolong intraventricular conduction times. The doses requlred for this effect are large and the myocardial and Purkinje systems are both depressed. With sufficiently large doses of any of these three salts, the ventricles may fibrillate. On the estimate that our average heart-lung preparation has 500 ml. of circulating
5 INTRAVENTRICULAR CONDUCTION C. 40,.. #{149} TEMPERATURE CONDUCTION TIME- MSEC. FIG. 3. Effect. of blood temperature on myocardial and Purkinje conduction velocities. 50 U). #{149}/ 40 i//c 1 30 /11,7 II 0 II,! i/ri 20 _ $0 POTASSIUM CONDUCTION TJME-MSEC. FIG. 4. Effect of potassium chloride on conduction. Addition of 100 mgm. of KCI (approximately 2.6 meq./l. of K ion) shortened conduct.ion times to all electrodes. A total of 175 mgm. (approximately 4.5 meq./l.) added prolonged conduction times moderately, and further addition of 25 mgm. slowed conduction markedly. The 200 mgm. total dose is approximately 5.2 meq./l. added to the preparation. plasma, we calculate that an additional 70 meq./1. of sodium ion will prolong conduction times markedly, and when 340 meq./l. is added the ventricles fibrillate. The addition of 11 meq./l. of calcium ion produces a conspicuous prolongation of conduction times and 40 meq./l. added causes fibrillation. Doses of magnesium are approximately the same, 10 meq./1. added to prolong conduction times and 36 meq./l. to produce fibrillation. Potassium chloride produces a biphasic effect upon intraventricular conduction, as shown in figure 4. When 2.5 to 3.0 meq./l. are added, conduction times are shortened to all electrodes. Further additions of potassium ion then prolong
6 142 SWAIN AND WEIDNER 50 U) -J 40 I Iii C.) z 10 U) BARIUM CONDUCTION TIME- MSEC. FIG. 5. Effect of barium acetate. Addition of 90 mgm. (approximately 0.6 meq./l of Ba ion) prolonged conduction times slightly. Further addition had little effect upon conduction times but produced a marked increase in automaticity in the heart. Ventricular fibrillation followed a total dose of 240 mgm. of barium acetate (approximately 2.0 meq./l.). conduction times so that after the addition of 6 to 7 meq./l. conduction is slowed markedly, and when 10 to 12 meq./l. have been added, the preparation usually fibrifiates. These calculated values for potassium ion agree well with the measurements of Winkler et at. (1938). Barium ion will cause ventricular fibrillation, but it has little effect upon conduction times. A dose of 90 mgm. of barium acetate, which is calculated to give a plasma level of approximately 0.6 meq./l. of barium ion, prolongs conduction times by the small amount shown in figure 5. Conduction times remain essentially constant from that point until the ventricles fibrillate at approximately 2 meq./l. The more striking effect of barium ion is to increase the automaticity of the heart. This action of the ion necessitates increasing the driving frequency of the stimulator to maintain control of the heart rate. Prior to ventricular fibrillation from barium, the heart may show a spontaneous rate faster than 250 beats per minute. Effects of epinephrine, levarterenol, and acetyicholine. Myocardial and Purkinje conduction are not altered by infusions of epinephrine at rates which shorten markedly the conduction time through the A-V system from right auricular appendage to epicardium of the right ventricle. When epinephrine is infused into the inflow cannula at a rate of 0.5 microgm. per minute for five minutes, A-V conduction time is decreased by about 10 per cent. Epinephrine infusions at 3.0 microgm. per minute decrease A-V conduction time by as much as 40 per cent, and more rapid infusions have no further effect upon auricle-to-ventricle conduction time. These values agree with the observations of Krayer et al. (1951). Only at far higher rates of epinephrine infusion is there a change in the intraventricular conduction times. At 80 microgm. per minute we frequently see
7 INTRAVENTRICULAR CONDUCTION OQO FIG. 6. Levarterenol infusion. 0 NOR-EPINEPHRINE CONDUCTION TIME-MSEC. ON indicates conduction times after six minutes of infusion of a 1:25,000 solution of levarterenol at a rate of 2 ml. per minute. OFF indicates conduction times 10 minutes after infusion was stopped. small changes, but even these changes are not consistent from experiment to experiment. Levarterenol shares with epinephrine this lack of conspicuous effect upon intraventricular conduction. Very high rates of infusion may alter conduction slightly. Figure 6 shows the effect of infusion of 80 microgm. per minute of levarterenol. During infusion, conduction times were somewhat prolonged; after the infusion was stopped, conduction times became somewhat shorter than control. Both epinephrine and levarterenol caused an increase in automaticity of the heart which occasionally necessitated an increase in the driving frequency to maintain control. Acetyicholine had little or no effect upon intraventricular conduction when infused at rates as high as 2 mgm. per minute. Effects of ouabain and quinidine. Ouabain exerts qualitatively different effects upon the two conduction systems. It slows Purkinje conduction at a time when myocardial conduction is unchanged or actually speeded. The onset of action of ouabain is slow, so the usual procedure was to administer a single dose of the drug to the preparation. Changes in conduction time were recorded at intervals during the period while the drug was exerting a progressively greater effect. Figure 7 shows the conduction values 13 and 28 minutes after a dose of 100 microgm. of the glycoside. In some experiments, just prior to ventricular fibrillation the values for the seven conduction times fall on a single straight line, suggesting that the Purkinje system is no longer conducting impulses more rapidly than is the myocardium. In ouabain experiments we see some increase in automaticity but it is not as pronounced as in experiments with barium ion, epinephrime and levarterenol.
8 144 SWAIN AND WEIDNER / OUABAIN FIG. 7. Ouabain effect CONDUCTION TIME- MSEC. Conduction times 13 and 28 minutes after a dose of 100 microgm. of ouabain are shown. Ventricular fibrillation occurred 41 minutes aft.er administration of the ouabain in this particular preparation. Osd 50 0 Cl) 7 /*, / 40 0 QUINIDINE CONDUCTION TIME- MSEC. FIG. 8. Quinidine effect. Successive doses of 10, 5, and 5 mgm. of quinidine sulfate were administered at 10-minute intervals. Quinidine sulfate, shown in figure 8, slows conduction in both systems. Veratrine, protoveratrine, and andromedotoxin. A dose of 750 microgm. of verat.rine causes a conspicuous slowing of Purkinje conduction, while the myocardial conduction in the ventricle is normal or moderately accelerated. Protoveratrime differs from veratrine in some of its actions but has somewhat similar effects upon intraventricular conduction. A dose of 40 microgm. of protoeratrine is sufficient. to slow Purkinje and speed myocardial conduction. Aft.er 75 t.o 100
9 INTRAVENTRICULAR CONDUCTION 145 microgm. of protoveratrine, the Purkinje slowing is profound. Similar in action to protoveratrine is andromedotoxin, a non-nitrogenous substance from Rhododendron maximum (Moran et al., 1954). Andromedotoxin4 in doses of 300 to 500 microgm. slows Purkinje conduction without depressing myocardial conduction. Thus veratrine, protoveratrine, and andromedotoxin share with ouabain the ability to differentially depress Purkinje conduction in the ventricle of the dog heart-lung preparation. All four substances are able to induce ventricular fibrillation in the preparation when administered in microgram quantities. DIsCussIoN. Interpretation of conduction graphs. When large changes in the slopes representing the two conduction systems are seen (as with changes in ternperature or following administration of quinidine) or when the two slopes are altered in opposite directions (as seen after ouabain administration), conclusions are easy to draw. On the other hand, when individual conduction times are changed by only a few milliseconds, it may be difficult to pin-point the site of change. Conduction to a more distant electrode involves at least three variable components. First is the instantaneous conduction from the stimulating electrode to the point where the propagated impulse is actually initiated, represented by the intercept on the Y-axis. Increased stimulating voltage or small doses of potassium ion, for instance, increase this Y-intercept. Second is the transmission of the impulse from epicardium to Purkinje system and back again through the slowly conducting myocardium. Third is the usually rapid conduction along the Purkinje system. The conduction velocities in the myocardium and in the Purkinje network may be altered, and not necessarily in the same direction. Following the administration of small doses of potassium salts, conduction times to the more distant electrodes are decreased by several milliseconds. The Y-intercept is definitely increased and velocities in the two conduction systems appear to be increased slightly. We are working so close to the limit of our measurements that the apparent increase in the two slopes may not be significant. The same situation exists for the slight prolongation of conduction times after barium ion. The conduction times are longer after the drug than they were during the control period, but one cannot say with assurance whether the change is primarily one of myocardial conduction, Purkinje conduction, or Y-intercept. When conduction in both systems is altered in the same direction we have made no attempt to quantitate the relative changes in the two components. Thus after qulnidine, for example, it is sufficient to say that both myocardial and Purkinje conduction are slowed. We could calculate percentage changes in the two slopes, but it is doubtful that such calculations would be meaningful. The relationship between conduction velocity and ventricular fibrillation. We feel that it is profitable to think of rapid intraventricular conduction as a mechanism for integrating ventricular activity and preventing ventricular fibrillation. As long as the depolarizing impulse can travel from one spot in the ventricles to any other spot in the ventricles in a time less than the effective refractory period of the ventricular muscle, there can be no more than one impulse in the tissue at. Andromedotoxin was kindly supplied by Dr. Neil C. Moran.
10 146 SWAIN AND WEIDNER a given time. However if the total conduction time becomes long with respect to the refractory period, it then becomes possible to start a second impulse before the first is extinguished. We believe that an essential criterion of fibrillation is the co-existence of more than one impulse in the ventricular muscle mass at a given instant. When conduction time becomes long with respect to refractory period, it becomes possible for the ventricles to fibrillate. Whether or not they do fibrillate will depend upon whether an impulse is initiated in the critical interval before the previous impulse is extinguished. It should make little difference in the hypothesis whether this new impulse arises from a stimulating electrode, from an ectopic focus, or from a re-entry mechanism. We believe that in our preparation the ventricular fibrillation from potassium salts is the result of profound slowing of intraventricular conduction to the point that the electrical stimulus arrives at the heart before the previous impulse has completed its journey through the myocardium. Fibrillation from barium ion, on the other hand, is more likely the consequence of the increased automaticity which supplies impulses at an increased rate at a time when conduction is slightly depressed. Fibrillation from ouabain or protoveratrine seems to be an intermediate case, combining some increase in automaticity with marked slowing of Purkinje conduction. Drugs of this latter group demonstrate the importance of the Purkinje network, for it appears that even augmented myocardial conduction is insufficient for maintaining coordination of widely separated areas in the ventricles. SUMMARY A method is described for estimating the myocardial and Purkinje conduction velocities in the right ventricle of the dog heart. The effects upon these conduction velocities of changes in the parameters of stimulation, of changes in temperature, and of the addition of several chemical substances were investigated. Ouabain, veratrine, protoveratrine and andromedotoxin share the property of depressing Purkinje conduction while leaving myocardial conduction unchanged or even augmented. All four agents can produce ventricular fibrillation in the heart-lung preparation when administered in microgram quantities. The relationship between changes in intraventricular conduction and the development of ventricular fibrillation is discussed. ACKNOWLEDGMENT. The authors would like to thank Mr. Allan Stephan who voluntarily assisted us in the surgical preparations for our experiments. REFERENCES KRAYER, 0., MANDOKI, J. J., AND MENDEZ, C.: THIS JOURNAL, 103: 412, LEwIs, T., AND ROTHSCHILD, M. A.: Phil. Trans. Royal Soc., 206 B: 181, MOE, G. K., AND MENDEZ, R.: Circulation, 4: 729, MORAN, N. C., DRESEL, P. E., PERKINS, M. E., AND RICHARDSON, A. P.: THIs JOURNAL, 110: 415, WINKLER, A. W., HOFF, H. E., AND SMITH, P. K.: Am. J. Physiol., 124: 478, 1938.
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