(Circulation. 1996;94:1125-1130.)
© 1996 American Heart Association, Inc.
Articles |
Percutaneous Multielectrode Endocardial Mapping During Ventricular Tachycardia in the Swine Model
the Neufeld Cardiac Research Institute, Tel Aviv University, Israel (M.E., D.O., Z.V., Z.R.); the Department of Medicine, University of California, San Francisco (A.P.F., M.C., M.M.S., M.D.L.); the Department of Medicine, Thomas Jefferson University Hospital, Philadelphia, Pa (M.F.S., S.H., A.J.G.); and EP Technologies, Sunnyvale, Calif (J.G.W., T.K., D.K.S.).
Correspondence to Michael Eldar, MD, Neufeld Cardiac Research Institute, Sheba Medical Center, Tel Hashomer 52621, Israel.
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Abstract |
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Background Identification of critical areas within the ventricular tachycardia circuit is a prerequisite for catheter ablation. Currently, mapping during ventricular tachycardia, usually performed with standard catheters, is difficult and time-consuming and can be used only in patients with hemodynamically stable tachycardia.
Methods and Results A total of 43 pigs underwent closed-chest induction of myocardial infarction. A basket-shaped catheter carrying 64 electrodes was deployed in the left ventricle during normal sinus rhythm. Unipolar pacing at 3 mA was successful in 78% of the basket catheter electrodes, demonstrating good electrode-tissue contact. Hemodynamic and echocardiographic measurements did not reveal any significant interference with myocardial or valvular function during or after catheter deployment. One hundred eighteen episodes of monomorphic ventricular tachycardia were induced in 28 pigs through right ventricular stimulation, 81 of which were mapped and analyzed. Ventricular tachycardia mapping was rapid, requiring only several beats and <10 seconds to complete. Presystolic potentials, a possible target for ablation, were identified in 58% of the tachycardia episodes mapped. Pathological examination revealed only minor valvular and endocardial catheter–induced lesions immediately after mapping and none a month later.
Conclusions The multielectrode catheter enables rapid and safe percutaneous endocardial mapping of ventricular tachycardia in the swine model. Exploration of the clinical potential of the multielectrode catheter seems warranted.
Key Words: mapping • tachycardia • catheter
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Introduction |
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Nonpharmacological treatment of sustained ventricular tachycardia (VT), by either surgical subendocardial resection or catheter ablation, requires recording of endocardial electrograms during the arrhythmia from multiple ventricular sites.1 2 3 4 5 6 7 Both custom-made and commercial mapping systems are available for simultaneous, multielectrode epicardial8 9 10 and endocardial11 12 13 ventricular mapping during open-chest surgery. In contrast, percutaneous catheter mapping techniques usually use a conventional catheter carrying a relatively small number of electrodes that is sequentially moved around the endocardium during VT.14 15 16 17 18 This method is time-consuming and limited to the mapping of patients with hemodynamically stable sustained monomorphic VT that lasts for a relatively long time. Methods that allow simultaneous recording from multiple endocardial sites could shorten the mapping procedure and enable mapping of VT that lasts only a short time or is hemodynamically unstable.
We describe in this article a multielectrode basket-shaped catheter that was used for endocardial left ventricular recording in a pig model of post–myocardial infarction, sustained, monomorphic VT.
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Methods |
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Animal Preparation
Experiments were performed at three centers (the Neufeld Cardiac Research Institute, Tel Aviv, Israel; the University of California at San Francisco; and Thomas Jefferson University Hospital, Philadelphia, Pa) with a common protocol. Female domestic German Landrace pigs (n=43) weighing between 25 and 35 kg were studied (Fig 1
). Each pig underwent a closed-chest induction of myocardial infarction under general anesthesia.19 Briefly, the pig was premedicated with droperidol (0.1 mg/kg IM), pethidine (2 mg/kg IM), and diazepam (0.5 mg/kg IV) and anesthetized with thiopental sodium (10 and 12 mg/kg IV) and halothane (1.5% to 2.5%) delivered through a breathing system. By use of a standard Seldinger technique, a 2.5- or 3.0-mm angioplasty balloon catheter was placed in the middle left anterior descending coronary artery. The balloon was inflated, and 100 µL agarose gel beads (75 to 150 µm) was injected through the lumen of the angioplasty catheter into the coronary artery. The balloon was deflated 30 seconds later, and the pig was allowed to recover for 3 hours under general anesthesia. The pigs were sent to a farm to recover and were returned 2 to 6 weeks later for induction of VT. The procedures followed were in accordance with institutional guidelines.
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Characteristics of the Multielectrode Basket Catheter
The catheter (EP Technologies) consists of an 8F flexible, 110-cm-long shaft carrying eight 7-cm-long nitinol superelastic splines in the shape of a basket (Fig 2). These splines are collapsible so that they can fit inside a specially designed guiding sheath for introduction into the heart. When released from the guiding sheath, the splines expand and conform to the shape of the cardiac chamber during both systole and diastole owing to the elasticity of the nitinol material. Each spline has 8 electrodes (a total of 32 bipolar pairs per basket) that are individually connected to insulated thin electric wires. Two splines carry 1 and 2 additional electrodes, respectively, on their proximal parts to allow identification and orientation of the splines of the deployed catheter.
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Catheter Introduction
To introduce the catheter, an 11F introducer was initially placed into the femoral artery by use of the standard Seldinger technique. Then a specially designed 11F 100-cm-long guiding sheath was inserted through the introducer and advanced into the left ventricle over a 0.32-in guide wire and a 7F pigtail catheter. The guide wire and pigtail catheter were then withdrawn. The collapsed basket catheter was advanced past the distal end of the sheath, which was then pulled back into the ascending aorta, allowing expansion of the preshaped basket inside the left ventricle. This procedure lasted <5 minutes in all pigs. Heparin sulfate (100 to 110 IU/kg IV) was administered and was followed by 60 to 70 IU·kg-1·h-1, and the guiding catheter was irrigated with 200 IU/h heparin throughout the procedure.
Measurements During Basket Deployment
Sinus Rhythm
Intracardiac electrograms were recorded during sinus rhythm after deployment of the basket catheter. Two centers (University of California and Thomas Jefferson University Hospital) used Bard LabSystem (Bard Electrophysiology) to acquire signals from each of 32 bipolar pairs of electrodes. Surface 12-lead ECGs also were recorded. The LabSystem software permitted simultaneous acquisition of all 32 bipolar electrograms along with a 12-lead ECG. The third center (Neufeld Cardiac Research Institute) used a custom-designed recording system. The electrograms were digitized at 1 kHz with an analog-to-digital board with a 12-bit resolution and recorded directly to a disk on a 486 personal computer (Hyondai, 90 Pro) with custom software. All 32 bipolar electrograms were recorded simultaneously for 8 seconds. A simultaneous surface ECG was not recorded because of software limitations.
Unipolar pacing was performed from each of the 64 electrodes at 3 and 10 mA to evaluate electrode-tissue contact. Pacing was performed by a custom-made switch box that allows rapid pacing and recording from each electrode.
The hemodynamic effects of the expanded basket were evaluated by measurement of left ventricular and aortic pressures (n=9) and right ventricular pressure (n=5) before and after catheter deployment. The catheter was left in the ventricle for 0.5 to 7 hours.
Ten pigs underwent transthoracic Doppler echocardiographic study (Hewlett Packard). During predeployment study, the parasternal long- and short-axis views were measured. During catheter deployment, two-dimensional echocardiogram allowed visual evaluation of the basket's conformity to the ventricular shape and its effects on ventricular contraction. Pulsed and color Doppler echocardiograms were used to assess aortic and mitral valvular function. In three pigs, a standard 8F, 4-mm, deflectable-tip radiofrequency ablation catheter (EP Technologies) was introduced into the left ventricle through the aortic valve after deployment of the basket catheter. The catheter was deflected in various directions inside the ventricle for several minutes and then was used to randomly deliver radiofrequency energy (20 to 50 J for 15 to 60 seconds) to the inferior and anterior walls of the ventricle.
Analysis of Electrogram Morphology
The electrograms obtained from the multielectrode basket catheter were analyzed in five pigs before acute myocardial infarction (control) and five of the pigs that returned 4 to 6 weeks later for induction of VT (after myocardial infarction). Electrograms were obtained simultaneously from each of 32 bipolar pairs of electrodes during sinus rhythm after introduction of the basket catheter. The electrograms were recorded for a minimum of 5 seconds, filtered at 30 to 500 Hz at a fixed gain of 5 mV/cm, and stored on an EPLabsystem (BARD Electrophysiology). Measurements were obtained with electronic calipers at a display speed of 200 mm/s. The following measurements were obtained for each electrogram: peak noise (in microvolts), peak amplitude (in millivolts), signal duration (in milliseconds), and amplitude/duration (in millivolts per second).
Measurements During VT
VT Induction
Induction of VT was attempted 2 to 6 weeks after the myocardial infarction.19 A 6F electrode catheter was inserted percutaneously and positioned in the right ventricular apex. Pacing and programmed electric stimulation were performed from the right ventricular apex or bipolar pair of electrodes on the basket catheter. VT induction was obtained with either overdrive pacing at rates of 240 to 360 per minute or programmed stimulation with one to four premature beats. Because induced VT rates were generally considerably faster than the usual human VT rates, antiarrhythmic drugs were used in 15 pigs to slow the VT. Either procainamide 20 mg/kg (n=12) or amiodarone (n=3) in consecutive doses of 3 mg/kg every 10 minutes (up to 15 mg/kg) was administered intravenously before VT induction.
Sustained monomorphic VT was defined as tachycardia of ventricular origin lasting >30 seconds and having a single morphology in all ECG leads. Activation maps from the basket catheter were acquired for all induced episodes of VT.
Presystolic activity was defined as any endocardial electric activity preceding the beginning of the earliest surface ECG. Reset by bipolar pacing from different electrode pairs on the basket catheter during stable VT was attempted in 10 pigs.
Morphological Evaluation
At the end of the final study, the basket catheter was withdrawn and all but 6 pigs were killed. The basket catheter was inspected for mechanical dysfunction (eg, spline dislodgement). In 12 pigs, the hearts were excised and examined for evidence of catheter-induced trauma. Six pigs were killed and examined 4 weeks later to evaluate possible permanent myocardial or valvular damage.
Statistical Analysis
Mean±SD was calculated for continuous variables. The parameters measured before and after deployment were compared by use of the paired two-tailed t test, with significance defined as P<.05.
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Results |
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Forty-three pigs underwent myocardial infarction induction. A total of 15 pigs were excluded because of either death (n=6) or the inability to induce or completely map VT (n=9).
Sinus Rhythm
Electrode-Tissue Contact
Unipolar ventricular pacing at 3 mA from each of the basket catheter electrodes was performed in 27 pigs during sinus rhythm. Ventricular capture, indicating electrode-tissue contact, was achieved in 78±15% (mean±SD) of the electrodes. Ventricular capture at 10 mA was evident in an additional 13±7% of the electrodes. Failure to capture occurred primarily in electrodes located below the aortic valve.
Hemodynamic, Echocardiographic, and Morphological Evaluation
The systolic left ventricular, mean aortic, and right ventricular pressures were not affected significantly during basket deployment (Table 1). Fluoroscopy and echocardiography revealed stable contact of the basket with the ventricular wall with no apparent impairment of wall motion by visual inspection (Fig 3). This was confirmed by measurements of left ventricular fractional shortening and systolic and diastolic dimensions before and during catheter deployment (Table 1). No significant aortic or mitral valve dysfunction (insufficiency or obstruction) could be detected, although a mild degree of either may have been missed owing to difficulties in obtaining optimal echocardiographic views. The basket catheter remained intact even after prolonged procedures. During simultaneous deployment of the basket and the ablation catheters, no interference with the ablation catheter movement was observed, and no harm to the basket was noted after radiofrequency energy delivery.
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Inspection of the hearts in 12 pigs at the end of the procedure revealed minor hemorrhages on the superior aspect of the aortic cusps in 8 pigs and on the septal cusp of the mitral valve in 3 pigs. Small (maximal diameter, 5 mm) and superficial (depth <2 mm) subendocardial hemorrhages were noted in the left ventricular apex in 10 pigs. In the 3 pigs in which radiofrequency application was attempted, typical lesions (n=11) were detected, consisting of round burns 0.5 to 1.0 cm in diameter and 0.5 to 0.9 cm in depth. In the 6 pigs killed 4 weeks after the procedure, no endocardial or valvular hemorrhages were observed.
Analysis of Electrogram Morphology
Two electrograms in the control group and only one electrogram in the post–myocardial infarction group could not be analyzed because of poor signal quality. Therefore, a total of 158 control electrograms and 159 post–myocardial infarction electrograms were available for analysis. In the control group, 135 of 158 electrodes (85%) demonstrated contact (ability to pace at 10 mA). The mean signal amplitude was higher in electrodes demonstrating contact compared with electrodes showing no contact (2.3±2.1 versus 1.3±1.3 mV, respectively; P<.05). No significant differences were found in peak noise (33.1±10.1 versus 28.7±7.0 µV) or signal duration (49.4±7.5 versus 50.0±8.3 ms) in electrodes making contact compared with those not making contact, respectively.
Peak noise was significantly lower in the post–myocardial infarction group compared with controls (24.6±10.2 versus 32.5±9.2 µV, P<.001; Table 2). The peak amplitude of the recorded electrogram also was lower in the post–myocardial infarction group (1.7±1.5 versus 2.1±2.0 mV, P=.04). The amplitude/signal duration tended to be lower in the post–myocardial infarction group but did not reach statistical significance (0.03±0.03 versus 0.04±0.04, P=.09).
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Ventricular Tachycardia
One or more episodes of sustained monomorphic VT were induced in 28 pigs with the multielectrode catheter deployed within the left ventricle. Overall, 118 episodes of sustained monomorphic VT were induced during one to four consecutive induction trials. Of these, 69 were induced before (baseline) and 49 after the administration of antiarrhythmic drugs. VT lasted from 12 seconds to 34 minutes. The VT cycle length at baseline was relatively rapid, ranging between 150 and 243 ms (mean, 185±37 ms). After intravenous administration of either procainamide or amiodarone, the VT cycle length was prolonged by 25 to 90 ms to a mean of 216±41 ms (P<.001). In 20 pigs, a 12-lead ECG was recorded during 55 episodes of monomorphic VT, of which 34 had left bundle-branch block and 21 had right bundle-branch block morphology.
Complete activation recordings from 32 bipolar sites during sinus rhythm and during VT took <10 seconds for acquisition and generally provided good-quality electrograms (Fig 4). Endocardial mapping with the multielectrode basket catheter was analyzed during 81 induced episodes of sustained or nonsustained monomorphic VT (40 at baseline and 41 after antiarrhythmic drug administration). Because of the inability to record simultaneous intracardiac and surface electrograms by the custom-made computer software (see "Methods''), presystolic activity could not be defined in 37 episodes of VT in 5 pigs.
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Of the 81 VT episodes that were successfully mapped in 19 pigs, presystolic electrograms were recorded during 47 episodes (58%). Twenty-two episodes (47%) were at baseline, and 25 (53%) were after drug administration (P=NS). The earliest presystolic activity was recorded 10 to 46 ms (27.6±13.2 ms) before the QRS complex. In an additional 5 episodes of VT (6%), the earliest activation occurred simultaneously with the beginning of the surface QRS complex.
VT reset was demonstrated in four pigs with single ventricular premature depolarizations that were delivered from a bipolar pair of electrodes on the basket catheter. A reset plot could not be constructed owing to the short cycle lengths of the VT.
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Discussion |
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The present study demonstrates for the first time the feasibility of percutaneous left ventricular mapping in a pig model by use of a basket-shaped multielectrode catheter. The catheter could be deployed safely in the left ventricle without significantly damaging intracardiac structures or causing hemodynamic compromise. Furthermore, the catheter provided stable simultaneous multielectrode endocardial recordings and enabled activation map acquisition during VT within several seconds.
Current Mapping Techniques
Identification of critical areas within the VT circuit seems to be the single most important factor limiting the efficacy of VT ablation.20 Current nonsurgical mapping techniques use a single roving catheter carrying a limited number of electrodes and requiring repositioning to multiple ventricular sites during the arrhythmia.14 15 16 17 18 Difficulties in mapping arise for several reasons. First, tachycardia may terminate spontaneously or as a result of catheter-induced premature beats. Not infrequently, several inductions are needed during a mapping procedure. Second, restimulation may induce new forms of VT or episodes of polymorphic VT or ventricular fibrillation. The chances of obtaining complete and accurate maps of two or more VT circuits are small. Third, the induced VT may be hemodynamically unstable, preventing complete mapping. Finally, inducible nonsustained episodes may be too short to be completely mapped. The basket catheter provides a comprehensive activation map within several beats. It may therefore significantly shorten the mapping procedure and allow mapping of rapid or unstable VT.
Previous Experience
Experience with percutaneous multielectrode catheter mapping of sustained arrhythmia has been very limited. Jenkins et al21 described a basket catheter (Webster Laboratories, Inc) similar to the one described here that was used for endocardial atrial mapping during sinus rhythm and atrial tachycardia in sheep and pigs. Differences between catheters include a smaller number of electrodes (25 bipoles) and a pull-string mechanism to achieve optimal tissue contact. Jenkins et al could get adequate signals from >95% of the electrode pairs, although some were ventricular owing to protrusion of one or two splines through the tricuspid valve. The authors felt that the basket may ultimately assist in the understanding and ablation of complicated atrial arrhythmias. Recently, Davis et al22 inserted up to five decapolar catheters into the left ventricle to simultaneously record 50 left ventricular unipolar signals in 22 patients with inducible sustained VT. Both retrograde aortic and atrial transseptal approaches were used. Fourteen (64%) of the patients had either multiple (>2) configurations or hemodynamically unstable VTs, which probably would not have been successfully mapped by conventional roving catheter technique. Of 22 arrhythmogenic areas subsequently confirmed at operative mapping, 21 were correctly identified during the multicatheter mapping procedure. Presystolic signals were detected in 68% of the patients during (at least one) VT. Limitations of this method include a long procedure time and the risks of multiple arterial and transseptal punctures. Of the four major complications (18%), two were directly related to the transseptal punctures. In contrast, we were able to deploy the catheter by the retrograde aortic technique in <5 minutes in all pigs without significant complications.
Basket Catheter
The multielectrode basket catheter has been developed to solve some of the problems that limit VT mapping by the roving catheter technique. The specially designed introduction system allows full deployment of the basket within a few minutes of the femoral artery cannulation. Because this is a flexible 8F catheter, it could conceivably be introduced by atrial transseptal puncture when necessary, eg, in patients with tortuous aorta and prosthetic aortic valve.
The deployed catheter conformed to the left ventricular geometry, and echocardiographic and hemodynamic examinations failed to reveal significant interference with ventricular function. Moreover, there was no evidence of aortic or mitral valve obstruction or regurgitation during the introduction and deployment and after the retraction of the catheter. Although minor valvular and subendocardial hemorrhages were noted immediately after the mapping procedure, none was present 4 weeks later.
Pacing studies revealed good tissue contact in 
78% of the electrodes and fair contact in an additional 13%. Failure to achieve contact occurred mostly in the proximal spline electrodes situated under the aortic valve, probably because of the less-than-ideal conformity of the basket to the ventricular geometry in this region. Failure to pace additional electrodes may reflect infarct-related elevated threshold, causing overestimation of the number of sites with poor or no contact.
The mapping procedure is relatively fast, the quality of the endocardial electrograms with conventional filtering is good, and the signals during VT showed little change over time (Fig 4
). Only 3 of 320 analyzed signals were of poor quality. Whether this was the result of poor contact, recording over scar tissue, problems with basket design, or another reason is difficult to ascertain in this closed-chest preparation. The signal-to-noise ratio was high (>500:1) for control and post–myocardial infarction pigs, attesting to the high quality of the recording. The peak signal amplitude was lower in the post–myocardial infarction than the control pigs, which was responsible for a tendency toward lower signal-amplitude-to-duration ratio. This may reflect the lower amount of viable tissue that generates smaller electric signals or poor electrode tissue contact, maybe secondary to localized ventricular contraction abnormalities after infarction.
Choosing the appropriate target site for catheter ablation of VT may be possible with this system. Activation mapping detected presystolic electrograms in 58% of the induced VTs. The inability to record presystolic potentials in all VT episodes may be due to an incomplete map or nonendocardial origin of the VT.23 24 25 Presystolic activity was not as early as that usually considered significant in human postinfarction VT (at least 50 ms before the QRS).26 However, the VT rate in this pig model was generally faster than the human VT rate and may have contributed to shorter presystolic activity. In addition, only one map was recorded and analyzed for each induced episode of VT, and earlier activity may have been missed as a result of incomplete mapping.
VT reset by pacing of electrodes on the basket catheter was induced during some episodes of VT. The induction of VT by premature ventricular depolarizations and overdrive pacing, the reset phenomenon, and the ability to terminate the VT through pacing19 seem to favor reentry with an excitable gap as the mechanism of at least some of the VT episodes. Further investigation into the mechanism of VT and optimizing the target site for ablation in this model should be possible with additional methods, such as pace mapping and concealed entrainment.18 27 If an adequate target electrogram is not identified, the basket can be collapsed and redeployed after some rotation inside the sheath. Ablation of arrhythmogenic areas based on these findings was not attempted in this study. However, an ablation catheter was codeployed and could be easily maneuvered inside the ventricle, and radiofrequency energy delivery caused typical endomyocardial burn lesions and did not harm the basket catheter.
Study Limitations
The present prototype of the basket catheter carries 32 bipolar electrodes. This may not be adequate for fine-scale mapping of VT, and withdrawal of the catheter into the sheath and redeployment(s) may be required to achieve a complete map. No pigs developed ventricular aneurysm after induction of myocardial infarction. It is not known whether the basket design allows adequate mapping of aneurysms. In addition, mapping of VT episodes arising in basal areas and below the aortic valve may be difficult.
No systematic effort was made to study the mechanism of the VT and to confirm the accuracy of mapping by maneuvers, such as concealed entrainment of the VT or successful ablation. It would be desirable to ablate from the electrode(s) recording the most favorable electrogram; however, the basket electrodes are too small to allow efficient energy delivery. Although an additional standard ablation catheter can be safely manipulated with the basket catheter deployed inside the ventricle, it may be difficult to identify and engage the desired site.
The catheter diameter mandates the use of a relatively large sheath (11F). The retrograde aortic approach may be difficult or impossible because of tortuous aorta or aortic stenosis, mainly in elderly patients with coronary artery disease. The feasibility of transseptal approach was not examined in this study.
The number of catheter deployments and the length of deployment may affect the incidence of complications (such as cusp and subendocardial hemorrhage). These issues were not addressed in the present study.
Conclusions
We have developed a new catheter that allows relatively fast and safe simultaneous multielectrode mapping of the left ventricle during induced VT. Exploration of the clinical application of this catheter seems warranted.
Received December 8, 1995; revision received February 13, 1996; accepted March 13, 1996.
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References |
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A. Kadish, J. Hauck, B. Pederson, G. Beatty, and C. Gornick Mapping of Atrial Activation With a Noncontact, Multielectrode Catheter in Dogs Circulation, April 13, 1999; 99(14): 1906 - 1913. [Abstract] [Full Text] [PDF]
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C. C. Gornick, S. W. Adler, B. Pederson, J. Hauck, J. Budd, and J. Schweitzer Validation of a New Noncontact Catheter System for Electroanatomic Mapping of Left Ventricular Endocardium Circulation, February 16, 1999; 99(6): 829 - 835. [Abstract] [Full Text] [PDF]
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J. L. R. M. Smeets, S. A. Ben-Haim, L.-M. Rodriguez, C. Timmermans, and H. J. J. Wellens New Method for Nonfluoroscopic Endocardial Mapping in Humans : Accuracy Assessment and First Clinical Results Circulation, June 23, 1998; 97(24): 2426 - 2432. [Abstract] [Full Text] [PDF]
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T. Nitta, R. B. Schuessler, M. Mitsuno, C. K. Rokkas, F. Isobe, C. S. Cronin, J. L. Cox, and J. P. Boineau Return Cycle Mapping After Entrainment of Ventricular Tachycardia Circulation, March 31, 1998; 97(12): 1164 - 1175. [Abstract] [Full Text] [PDF]
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D. S. Khoury, K. L. Berrier, S. M. Badruddin, and W. A. Zoghbi Three-Dimensional Electrophysiological Imaging of the Intact Canine Left Ventricle Using a Noncontact Multielectrode Cavitary Probe: Study of Sinus, Paced, and Spontaneous Premature Beats Circulation, February 3, 1998; 97(4): 399 - 409. [Abstract] [Full Text] [PDF]
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M. Eldar, D. G. Ohad, J. J. Goldberger, Z. Rotstein, S. Hsu, D. K. Swanson, and A. J. Greenspon Transcutaneous Multielectrode Basket Catheter for Endocardial Mapping and Ablation of Ventricular Tachycardia in the Pig Circulation, October 7, 1997; 96(7): 2430 - 2437. [Abstract] [Full Text]
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