the p wave andp-r interval

The P Wave and P-R Interval

Effects of the Site of Origin of Atrial Depolarization

By ALBERT L. WALDO, M.D., KARI J. VITIXAINEN, M.D., GFBAuR A. KAIsEIR, M.D.,

JAMES R. MALM, M.D., AND BRIAN F. HOFFMAN, M.D.

SUMMARYThe atria of 37 patients were paced from selected sites during cardiac surgery. When

the atria were paced from endocardial sites low in the right atrium, the P waves inECG leads II, III, and aVF were shown to be either negative, biphasic, or positive,depending on the site paced. When the endocardial sites were paced, the P-R intervalswere, almost without exception, less than 0.12 sec. When those endocardial sitesclosest to the A-V junction were paced, the P-R intervals were always less than 0.12sec. When the atria were paced, from the epicardial sites, the P-R intervals were

always greater than 0.12 sec. Negative P waves in ECG leads II, III, and aVF were

recorded when the atria were paced from the postero-inferior left atrium and the caudalright atrium. The P-R interval did not always reflect the initial period of atrialactivation because an isoelectric interval, generally of 0.01 to 0.025 sec, was frequentlypresent between the onset of atrial stimulation and the first clear evidence of theP wave in the ECG. The implications of these results are discussed.

Additional Indexing Words:Low atrial rhythm A-V junctional rhytAtrial pacing

HE ELECTROCARDIOGRAPHIC di-agnosis of several atrial arrhythmias

depends strongly on the polarity and mor-phology of the P wave and duration of the P-R or R-P interval. Such arrhythmias include A-V junctional or A-V nodal rhythms, coronarysinus rhythms, coronary nodal rhythms, andleft atrial rhythms.1-8 A knowledge of relation-ships between the site of origin of atrial

From the Departments of Pharmacology andSurgery, College of Physicians and Surgeons, Colum-bia University, and the Surgical Service, ThePresbyterian Hospital, New York, New York.

This work was supported in part by Research GrantHE 12738 from the National Heart and Lung Insti-tute, U. S. Public Health Service. Work was carriedout during Dr. Waldo's tenure of a John PolachekMedical Research Fellowship and Dr. Vitikainen'ssurgical traineeship from the National Institute ofGeneral Medical Sciences, National Institutes ofHealth.

Received March 30, 1970; revision accepted forpublication June 22, 1970.

Circulation, Volume XLII, October 1970

thm Specialized atrial conduction

depolarization and the resulting sequence ofatrial activation is central to the understand-ing of these arrhythmias and the P wavesassociated with them. Scherf and Cohen havethoroughly reviewed this aspect of electrocar-diographic interpretation.' 9

Lewis'0 and others,"-14 as a result of studieson the canine heart, accepted the premise thatexcitation of the atria spreads radially and atuniform velocity from its site of origin. Mostinterpretations of clinical electrocardiogramsmake the same assumption. In terms of thishypothesis, activation of the atria by animpulse originating at a site near the A-Vnode should result in negative P waves inleads II, III, and aVF. However, reports fromthis laboratory'5 16 and those of others'7-26have provided evidence that this need not betrue. Recently, Spach and associates26 demon-strated that when the atria of the canine heartwere paced from a site near the coronarysinus, retrograde activation of the atria wasnot radial. In studies on the canine heart,

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P WAVE AND P-R INTERVAL

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Moore and associates15 found that activationof the atria resulting either from retrogradeconduction of an impulse through the A-Vnode or from stimulation of the lowerinteratrial septum resulted in P waves whichwere predominantly positive in leads II, III,and aVF. More recently, we have shown"6that, in man, retrograde activation of the atriaby an impulse initiated in the specializedconduction system distal to the N region ofthe A-V node can result in P waves which arebiphasic (-, +) or positive (+) in leads II,III, and aVF.

Because our results were in disagreementwith the conclusions resulting from mostclinical and experimental studies'10-4 27-30 andbecause there have been few detailed studieson relationships between site of origin of animpulse in the human atria and the polarityand morphology of the P wave, we haveconducted a systematic investigation of thechanges in polarity and morphology of the Pwave which occur when the atria of thehuman heart are paced from selected epicar-dial and endocardial sites.

MethodsAll patients were studied during cardiac

surgery. The experimental protocol varied some-what for each patient and was determined by thenature and requirements of the surgical proce-dure. A summary of pertinent clinical data on the37 patients studied is provided in table 1. Theages of the patients studied ranged from 5 to 66years, the mean age being 19 years. The atria of23 patients had no congenital defects. Fourteenpatients with atrial septal defects of the secun-dum type are included because we assumed thata defect limited to the region of the fossa ovaliswould not interfere with the sequence of atrialactivation.31' 32 In the preoperative ECGs, cardi-ac rhythm, polarity, and morphology of the Pwaves and P-R intervals were within normallimits for each patient. All but 12 patientsreceived small amounts of atropine or scopola-mine (table 1) at least 2Y2 hours prior to thestudy. P-R intervals recorded in the operatingroom prior to thoracotomy were comparable tothose recorded at a similar heart rate prior tosurgery.An acrylic plaque containing five silver elec-

trodes'6' 33 was sutured to the right atrialepicardium of each patient to provide a clearrecord of atrial activity at all times during theCirculation, Volume XLII, October 1970

surgical procedure and to permit atrial pacing tosuppress arrhythmias or to provide a supraven-tricular rhythm.'16 34 One pair of electrodes in theplaque was used only to record a bipolar atrialelectrogram; another pair was used either torecord a second electrogram or to stimulate. Thefifth electrode contact served as a spare. A probe,containing three silver electrodes, was used eitherfor bipolar stimulation or to record bipolarelectrograms from selected sites on the atria orventricles. Use of such an electrode to locate thebundle of His and other parts of the specializedconducting system has been described previous-ly.35' 36 All leads in contact with the heart wereisolated from ground and the recording instru-ments by isolation transformers. During periods ofdata collection, body temperature, measured fromthe retrocardiac portion of the esophagus or fromthe rectum, varied from patient to patient asdetermined by the requirements of the surgicalprocedure; the range was 34 to 37 C.

Patients were studied while in the supineposition. Pacing was performed from sites on theatrial epicardium prior to atriotomy for cannula-tion of the cavae and initiation of cardiopulmo-nary bypass. Endocardial sites were paced duringthe period of cardiopulmonary bypass. Theatriotomy extended from the tip of the right atrialappendage toward the inferior vena cava to apoint 1 to 2 cm onto the lateral free wall of theright atrium. This incision avoided the sino-atrial(SA) node and the atrial internodal tracts.31' 32Furthermore, the atriotomy itself did not modifythe polarity or morphology of the P waves in thestandard and augmented ECG leads when theatria were paced from the SA nodal region.The five epicardial pacing sites are shown in

figure 1. The PLA site is that portion of thepostero-inferior left atrium which lies just abovethe coronary sinus, below the right inferiorpulmonary vein, and just posteromedial to theinferior vena cava. The CRA site is the portion ofthe caudal right atrium just anterolateral to thejunction of the inferior vena cava with the rightatrium. In some patients, the epicardial aspect ofthe coronary sinus just as it enters the rightatrium also served as a pacing site (CS epi). TheCST site is the caudal portion of the sulcusterminalis, and the MST site is its mid-portion.The SA site is near the head of the SA node.The endocardial pacing sites are shown in

figure 2. During the period when the endocardialsites were paced, vacuum suction from adependent portion of the right atrial endocardiumnear the coronary sinus ostium permitted readyvisualization of the endocardial pacing sites. Site1 is the roof of the coronary sinus ostium. Site 2lies on the dorsal lip of the coronary sinus (theeustachean ridge), and site 3 is just within the

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Figure 1

Postero-inferior aspect of the human heart showingthe epicardial sites on the left and right atria fromwhich the atria were paced. Abbreviations of sites:PLA =postero-inferior left atrium: CRA = caudalright atrium; CST __ caudal sulcies terminalis; MST -mid-sulcus terminalis; SA = sinoatrial node area; CSepi - epicardial aspect of the coronary sinus as itenters right atrial cavity. Abbreviations of anatomy:SVC = superior vena cava; Ao = aorta; PA -pul-monary artery; PV pulmonary veins; LA leftatrium; RA = right atrium; CS = coronary sinus;IVC -_ inferior vena cava; LV - left ventricle; RV=right ventricle.

coronary sinus ostium. Site 4 is on the ven-tral lipof the coronary sinus ostium, and site 5 isimmediately medial to the ostium. Sites 6 and 7are parallel to the atrioventricular groove and 4 to5 mm medial to site 5; sites 8 and 9 are parallel tothe atrioventricular groove and 4 to 5 mm medialto sites 6 and 7; and sites 10 and 11 are parallelto the atrioventricular groove and medial to sites8 and 9. All epicardial and endocardial sites werenot always paced in each patient.The atria were paced at a rate slightly in excess

of the spontaneous rate. Stimuli were provided bya Medtronic 1187 special digital thresholdstimulator37 anid delivered through a stimulusisolator. Bipolar electrograms and simultaneousstandard bipolar and augmented unipolar ECGleads were monitored on an eight channelElectronics for Medicine switched beam oscillo-scope and recorded on photographic papermoving at speeds of 50 to 200 mm/sec. ECGrecordings were calibrated at 2 cm/mv. ECG leadII was recorded for all patients. Only 18 patients,however, had all of the standard andaugmented ECG leads recorded. Six patients hadfive leads recorded, 11 had three leads, two hadtwo leads, and one patient had only one lead.Measurement of all intervals was made from the

records with a vernier measuring device havingan accuracy of -+- 2 msec at the slowest recordingspeed used.

In many of these patients, bipolar wireelectrodes were implanted in the atria at the endof the cardiac surgical proceduire and brought outthrough the chest wall for use during thepostoperative period as an aid in diagnosis andtherapy.38," This enabled us to evaluate theeffect of the open chest on P-wave polarity andmorphology in 10 patients in whom the bipolarxvire electrodes had been implanted at a site usedto pace the atria during surgery. In these patients,on the first postoperative day, the atria werepaced through the implanted electrodes and the Pvaves which resulted were compared to thoserecorded during surgery.

Results

Relationship Between the Site of Origin of theImpulse and P-Wave Polarity and Morphology

When the atria were paced from theepicardial and endocardial sites shown infigures 1 and 2, a consistent spectrum ofchanges in P-wave polarity and morphologyresulted. P waves in leads II, III, and aVF

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Right atrial endocardium of the human heart showingthe endocardial sites (1 to 11) from which the atriawere paced. Abbreviations: F=-foramen ovale;CS - coronary sinus oriface; TV =posterior leafletof the tricuspid valve; Ao aorta; PA = pulmonaryartery; RAA = right atrial appendage; SCV = superiorvena cava; IVC = inferior vena cava.


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P WAVE AND P-R INTERVAL 659

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Figure 3(A and B) P waves recorded from patient 31 when the atria were paced from the epicardial sites.A stimulus artifact (S) precedes each P wave. A tinw line appears in the record from eachsite. aVL was not recorded for this patient when sites CRA, CST and MST were paced.PLA = posterior left atrium; CRA = caudal right atrium; CST = caudal sulcus terminalis;MST = mid-sulcus terminalis; SA = sinoatrial nodal area. Paper speed is 50 mm/sec.


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Figure 4

The P waves recorded in ECG lead II for patient 20, when the atria were paced from endo-cardial sites on either side of (sites 4 and 10) and from sites within this patient's endocardialtransition zone (sites 5, 7, and 9). S represents the stimulus artifact. A time line appears inthe records from sites 4, 7, and 9. Paper speed is 50 mm/sec.

Summary of P-wave Polarity for all Endocardial Pacing Sites

Polarity Sites1 2 3 4 5 6 7 8 9 10 11

+ 0 0 0 0 0 0 1 2 27 -15.0 100-10

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All numbers are expressed in per cent and indicate the percentage of time the P waves inECG leads II, III, and aVF were either positive (+), biphasic (- +), or negative (-) on

pacing from right atrial endocardial sites 1 to 11. Shaded areas indicate an incidence of50% or more.

always were negative when the atria were

paced from the PLA and CRA (fig. 3A).When the atria were paced from the CST, theP waves in leads IL, III, and aVF were

predominantly negative although they tended

to be flat (fig. 3A). When the atria were

paced from the MST, the P waves in leads II,III and aVF were predominantly positivealthough they tended to be flat (fig. 3B).When the atria were paced from the SA, the P


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Figure 6P waves recorded in all standard and augmented leads from patient 17 when the atria werepaced from right atrial endocardial sites 2, 7, and 11. The P waves in leads II, III, and aVFhave been enlarged five times and appear beside the complete record. Stim identifies thestimulus artifact delivered through the pacing electrode. SA identifies the bipolar electrogramrecorded from the region of the sinoatrial node. A time line appears in the record fromsite 11. Paper speed is 50 mm/sec.

waves in leads II, III, and aVF always werepositive (fig. 3B).When the atria were paced from sites

around the coronary sinus ostium (endocar-dial sites 1 to 4), the P waves in leads II, III,and aVF almost always were negative. Medialto the coronary sinus ostium, there was atransition zone which generally extended fromendocardial site 7 through site 9 and oftenincluded sites 5 and 6. Stimulation within thiszone resulted in P waves in leads II, III, andaVF which were biphasic (-, +). Stimulationat sites medial to the transition zone (endo-cardial sites 10 and 11) resulted in P waves inleads II, III, and aVF which were franklyCirculation, Volume XLII, October 1970

positive. Figure 4 shows for lead II the changein P-wave polarity and morphology when theatria of patient 20 were paced from sites oneither side of and from within the transitionzone. When the atria were paced from sites inthe transition zone closest to the coronarysinus ostium (for example, site 5 in patient20), the positive portion of the biphasic Pwave in leads II, III, and aVE was small andthe major portion of the P wave was negative.When the atria were paced from sites withinthe transition zone but farther from (that is,medial to) the coronary sinus ostium (forexample, sites 6 to 9 in patient 20), thepositive portion of the biphasic P wave in

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WALDO ET AL.

leads II, III, and aVF became larger and thenegative portion smaller. Medial to thetransition zone (sites 10 and 11) the P wave

was positive. The location and extent of thisendocardial transition zone varied somewhatfrom patient to patient. Figure 5 summarizesin percentage form the P-wave polarity inleads II, III, and aVF for all endocardialpacing sites. In relation to figure 5, it mustagain be noted that although lead II was

recorded from each patient, leads III and aVFwere not always recorded simultaneously. Forsome patients lead II was recorded only withlead aVF; for others, only with lead III, andfor some, with neither lead III nor aVF.

Figure 6 demonstrates the spectrum of Pwaves recorded from patient 17 in all thestandard and augmented leads when the atriawere paced from three of the endocardial

Suprathreshold

Threshold

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Figure 7

The P waves recorded in lead II from patient 20when right atrial endocardial site 9 was paced. Inpanel A the stimuli were suprathreshold. During an

interval of 34 beats, between the end of panel A andthe beginning of panel B, the stimulus strength was

lowered, becoming threshold for the first two beats inpanel B and subthreshold for the third beat in panelB. Note that when the stimulus strength becomessubthreshold, atrial capture is lost. S indicates thestimulus artifact. Time lines are at intervals of I sec;

paper speed is 50 mm/sec.

sites. It again illustrates the negative P wavesin leads II, III, and aVF recorded when theatria were paced from sites around thecoronary ostium (site 2), the biphasic P wavesrecorded in leads II, III, and aVF when theatria were paced from within the endocardialtransition zone (site 7), and the positive Pwaves recorded in the same leads when theatria were paced from sites medial to thetransition zone (site 11). Careful examinationof the P waves recorded when the atria werepaced from endocardial site 7 suggests thatthe P waves in lead III and probably in leadaVF are triphasic (+, -, +) while the P wavein lead II is biphasic (-, +). In three otherpatients, the polarity and morphology of the Pwaves recorded in lead III or aVF or bothleads were somewhat different from the Pwave in lead II when the atria were pacedfrom some but not all of the endocardialtransition zone sites. However, the point offigure 6, as well as figures 4 and 5, is that the Pwaves in ECG leads II, III, and aVF are notsolely negative when the atria are activatedfrom endocardial sites low in the right atrium.Depending on the site paced, P waves in theseleads may be biphasic (-, +) or positive.Furthermore, it must be emphasized that thedistance from endocardial site 5 to sites 10 and11 was only 1.5 cm. Thus, the changes in Pwave polarity and morphology which werecorded occurred when the atria were pacedfrom endocardial sites separated only by shortdistances.

Stimulus strength also had an effect on theP wave at some endocardial sites. The polarityand morphology of the P wave differed forsuprathreshold and threshold stimuli. Figure 7illustrates for endocardial site 9 in patient 20the change in P-wave polarity and morphol-ogy in lead II that occurred when the stimulusstrength was decreased from suprathreshold tojust threshold. Note that the biphasic (-, +)P wave has a prominent initial negativedeflection during suprathreshold pacing, butwhen the stimulus was just threshold, the Pwave, while still biphasic, is almost entirelypositive.


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OPEN CHEST

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Figure 8

Standard and augmented ECG leads recorded frompatient 37 when the atria were paced through the im-planted wire electrodes from the same site (CRA) atthe same rate in the operating room when the chestwas open and during the first postoperative day.(The P-R intervals are 0.15 sec and the S-P intervalsare 20 msec in each instance. See also the sectionon the P-R interval in "Results"). S represents thestimulus artifact. Time lines are at 1 sec intervals.Paper speed is 50 mm/sec.

Comparison of P-Wave Polarity and MorphologyWhen the Chest Was Open and Closed

The same atrial site was paced in theoperating room and during the immediatepostoperative period in 10 patients and therecorded ECGs compared. In all instances,when such comparisons were made, thepolarity of the P waves in leads II, III, andaVF was identical, and the morphology of theP waves in leads II, III, and aVF, althoughnever identical, was similar. This confirms

the observations of Moore and associates'5and Spach and co-workers.26 Figure 8 illus-trates for patient 37 the polarity and morphol-ogy of the P waves in the standard andaugmented ECG leads recorded when theatria were paced through the same wireelectrodes at the same rate both in theoperating room when the chest was open (leftpanel) and during the first postoperative day(right panel). Note that the P waves in leadsII, III, and aVF are identical in polarity andsimilar in morphology. We have thereforeconcluded that the open chest did notsignificantly affect our data.The P-R Interval*While this study was initially designed to

examine P-wave polarity and morphologywhen the heart was paced from selected atrialsites, it soon became evident that the studiesalso provided important data regarding the P-R interval. As demonstrated in figure 3A andB and summarized in table 2, when the atriawere paced from the selected epicardial sites,the P-R interval was always greater than 0.12sec.t When the endocardial sites were paced,

*The P-R interval was measured from the earliestinscription of the P wave in any of the simultaneouslyrecorded ECG leads to the earliest inscription of theQRS complex in any of the simultaneously recordedECO leads.

tIn two of seven patients in whom site CS epi waspaced, intervals of 0.117 sec and 0.109 sec wererecorded. The proximity of this site to the endocardialsites of the coronary sinus ostium ( 1 to 4) mayexplain the short P-R interval in these two instances( cf. ). The range of P-R intervals for this site was 0.109to 0.144 sec, the mean being 0.130 sec. The P wavesin ECG leads II, III, and a VF were always negativewhen this site was paced.

Table 2

Summary of P-R Intervals Recorded When Epicardial Atrial Sites Were Paced

P-R intervals% 0.12 sec % less than Range Mean

Epicardial site or more 0.12 sec (sec) (sec)

PLA 100 0 0.143 - 0.189 0.165CRA 100 0 0.151 - 0.172 0.146CST 100 0 0.168 - 0.213 0.185MST 100 0 0.140 - 0.198 0.172SA 100 0 0.131 - 0.208 0.159

Abbreviations: Defined in text and legend for figure 1.


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Table 3

Summary of P-R Intervals Recorded When Endocardial Atrial Sites Were PacedP-R intervals

%7c 0.12 sec % less than Range MeanEndocardial site or more 0.12 sec (sec) (see)

1 9 91 0.098 - 0.125 0.1012 9 91 0.092 - 0.120 0.1083 17 83 0.089 - 0.127 0.0984 0 100 0.077 - 0.113 0.090

0 100 0.080 - 0.119 0.0906 0 100 0.073 - 0.112 0.0987 0 100 0.089 - 0.119 0.1048 0 100 0.083 -0.113 0.1009 12 88 0.098 - 0.124 0.10810 14 86 0.088 - 0.125 0.10411 25 75 0.094 - 0.126 0.107

the P-R intervals were, almost without excep-

tion, less than 0.12 sec (table 3). Pacing fromendocardial sites closest to the A-V junction,sites 4 to 8, always resulted in P-R intervals ofless than 0.12 sec. P-R intervals as short as

0.073 sec were recorded when pacing from site6, and P-R intervals shorter than 0.099 sec

were often recorded when pacing from allendocardial sites. The mean P-R interval foreach endocardial pacing site was short andranged from 0.090 to 0.108 sec. In the fewinstances in which the P-R intervals were

greater than 0.12 sec, they did not exceed0.127 sec (table 3).These data clearly show that P-R intervals

of less than 0.12 sec can result from initiationof impulses in the right atrium. In evaluatingthese data, it should be noted that severalhours prior to surgery most patients receivedatropine or scopolamine (table 1), both ofwhich can decrease atrioventricular conduc-tion time.40 However, in the doses adminis-tered, these drugs probably did not significant-ly affect the P-R intervals recorded when theatria were paced. Evidence for this isprovided by the fact that the P-R intervalsrecorded in the operating room prior tothoracotomy were comparable to those re-

corded at a similar heart rate prior to surgery

and prior to administration of preanestheticmedication. Also, the P-R intervals recordedfrom patients who had received neither ofthese drugs also were less than 0.12 sec when

the atria were paced from all endocardial

sites, except for a P-R interval of 0.12 sec,recorded in one patient when endocardial site1 was paced.

In further consideration of factors tendingto affect the P-R interval, it must be noted thatmany of the patients were studied at tempera-tures lower than 37 C (table 1). This would, ifanything, prolong atrioventricular conductiontime.41 Also, pacing the heart at a rate slightlyfaster than the spontaneous rate would, ifanything, prolong atrioventricular conductiontime.42 Thus, the P-R intervals recorded inthese studies may, if anything, be slightly

Table 4

Summary of Data Pertaining to S-P Interval

Range MeanSites % present (msec) (msec)

EpicardialPLA 56 0-16 7CRA 100 12-32 23CST 100 10-40 23MST 100 12-40 22SA 50 0-20 9

Endocardial1 82 0-56 212 93 0-46 203 93 0-31 184 92 0-59 285 87 0-32 196 70 0-35 157 55 0-31 88 88 042 239 57 0-32 1110 86 0-47 2111 67 0-51 23


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Stim

SA

I

aVr

aVL

aVf

l ~ ~~~~~~~~~~ l--- w -tftm - - - I

UO

4-

Figure 9An S-P interval of 20 msec was recorded when pacingthe atria from endocardial site 2 in patient 17. Aline has been drawn through the stimulus artifact todemonstrate the 20-msec isoelectric interval betweenthe stimulus artifact and the onset of the P wave.

Stim identifies the stimulus artifact, and SA identifiesthe bipolar electrogram recorded from the region ofthe sino-atrial node. A time line appears through theP wave of the second beat on this record. Paperspeed is 50 mm/sec.

prolonged because of the low temperature anda pacing rate faster than the spontaneousrate.One important interval remains to be

discussed. Frequently, there was an interval(S-P interval) between the time of stimulationof the atrium and the first clear evidence of


the inscription of the P wave (table 4 and fig.9). This interval, when present, was generallybetween 0.01 and 0.025 sec although it wasonce as long as 0.059 sec. Thus, in manyinstances, the beginning of the P wave doesnot necessarily coincide with the beginning ofatrial activation. This observation clearlyreflects on the utility of rigid criteria for the P-R interval in determining the site of origin ofatrial activity.

DiscussionOur results suggest that it may be necessary

to reevaluate the criteria employed for thediagnosis of certain arrhythmias (such as A-Vnodal rhythm, coronary nodal rhythm, andcoronary sinus rhythm) since the identifica-tion of these rhythms depends primarily onthe polarity and morphology of the P waveand the duration of the P-R interval.

Upper Nodal Rhythm

In the absence of conduction defects, anelectrocardiogram showing a P-R interval ofless than 0.12 sec and negative P waves inleads II, III, and aVF usually is thought torepresent upper nodal rhythm with retrogradeactivation of the atria.2-5 If these criteria wereemployed, the records we have obtained whenthe atria were paced from the vicinity of thecoronary sinus ostium would be classified asupper nodal rhythm. Our data clearly showthat negative P waves in leads II, III, and aVFand P-R intervals of less than 0.12 sec and asshort as 0.077 sec can result from impulsesinitiated in the right atrium.

Coronary Nodal RhythmThis rhythm is characterized by positive P

waves in leads I and II and a P-R intervalbetween 0.10 and 0.02 sec.6 7 We haverecorded short P-R intervals, positive P wavesin lead II, and positive or biphasic (-, +) Pwaves in lead I when the atria were pacedfrom endocardial sites 10 and 11 and some-times from sites 7, 8, and 9. While we neverhave recorded P-R intervals less than 0.083 secwhile pacing from these sites, our evidencesuggests that some spontaneous arrhythmiasidentified as coronary nodal rhythm may

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result from initiation of activity at one of theseendocardial sites.

Coronary Sinus RhythmA P-R interval of 0.12 sec or more, in

association with a negative P wave in leads II,III, and aVF, usually is thought to representeither a rhythm originating in the coronarysinus1 3-5 or an A-V junctional rhythm withretrograde capture of the atria and markedlydelayed conduction to the ventricles.'1- Wehave shown that if atrial activity is initiated atappropriate sites in left atiium (PLA) andright atrium (CRA), the electrocardiogramshows a P-R interval greater than 0.12 sec andnegative P waves in leads II, III, and aVF. Todesignate all such tracings as coronary sinusrhythm clearly is incorrect.Our findings are in agreement with results

obtained from studies on the canine heartwhen stimuli were applied to the same partsof the atria.10 43 44 Also, others have paced thehuman heart through catheters placed withinthe coronary sinus and recorded negative Pwaves in leads II, III, and aVF and P-Rintervals of 0.12 sec or more.45-50 It seemslikely that in these studies the atria actuallywere activated from the PLA. As shown infigure 1, most of the coronary sinus liesadjacent to the left atrium, and, as shown infigure 2, only its ostium is within the rightatrium. Because of these anatomic relation-ships, any catheter advanced into the coronarysinus necessarily lies adjacent to the PLA. Itreasonably follows that, when pacing the atriathrough such a catheter, the impulse isinitiated in the region of site PLA. Harris andassociates51 paced the PLA through a catheterinserted in the left atrium and recordednegative P waves in leads II, III, and aVF andP-R intervals of more than 0.12 sec. Prinz-metal and co-workers,29 also produced nega-tive P waves in the same leads by mechanicalstimulation of the human heart at right andleft atrial sites comparable to PLA and CRA;their results differ from ours, however, in thatthey recorded P-R intervals shorter than 0.12sec.

Lower Nodal RhythmWe have previously described the polarity

and morphology of the P wave duringretrograde capture of the atria in somerhythms initiated at sites in or distal to theNH region of the A-V node.'6 In that study,we found retrograde P waves to be primarilybiphasic in the standard and augmented leads.In leads II, III, and aVF the retrograde Pwave was most often largely negative with alate, small positive component, much as wehave demonstrated in this study for stimula-tion of sites in the endocardial transition zoneclose to the coronary sinus ostium. Ourimpression, based on a review of a large seriesof ECGs demonstrating A-V junctionalrhythm, confirms the observation of Puech24that the P waves in leads II, III, and aVF areoften negative but may, in fact, be biphasic(-, + ). It should be noted that the positivecomponent of this biphasic type of P wavemay often be masked within the T wave,resulting in a P wave in II, III, and aVF whichappears as a completely negative deflection.'6Also, the initial negative portion of the P wavein leads II, III, and aVF may be maskedwithin the preceding QRS complex during A-V junctional rhythm with retrograde atrialcapture, resulting in a P wave which appearsto be positive in II, III, and aVF.'6

A-V Junctional and Low Atrial RhythmsWe have previously defined an A-V junc-

tional rhythm as a rhythm initiated by apacemaker located somewhere between theNH region of the A-V node and thebifurcation of the bundle of His.16 None of theresults presented here appear to requiremodification of this definition. Also, recordsobtained by the use of catheter electrodes torecord from the His bundle52 have provideddata which are in agreement with thisdefinition and with the earlier conclusion ofHoffman and Cranefield53 that automatic cellsare found in the NH region of the A-V nodeand in the His bundle but not in the AN or Nregions of the node. We suggest, therefore,that the term "A-V junctional rhythm" should


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be employed to describe what formerly hasbeen called lower nodal rhythm.Our data show that the electrocardiographic

patterns thought to be characteristic of uppernodal rhythm can result from activation of theatria in the vicinity of the coronary sinusostium. This finding is consistent with theconclusions of Hoffman and Cranefield53 thatcells in the AN region of the A-V node do notshow automaticity. Although Watanabe andDreifus54 concluded that impulses might beinitiated in the AN region of the A-V node,their data consisted of several instances ofprimary negativity recorded from this region.However, as Erlanger55 pointed out, therecording of primary negativity in a unipolarlead identifies not the pacemaker but only thepart of the atrium first activated by apacemaker. Primary negativity recorded byWatanabe and Dreifus from the vicinity ofthe AN region thus may result from automaticfiring of a pacemaker located in the region ofthe coronary sinus. This interpretation wasalso suggested by others.52

It has been postulated that coronary nodalrhythm is initiated by a pacemaker in a regionnear the tail of the SA node.6 7 However, thisexplanation does not seem likely since ourdata consistently showed that when the atriawere paced from an epicardial site near thetail of the SA node (MST), the P-R intervalwas always greater than 0.12 sec. If the termCcoronary nodal rhythm" implies that thepacemaker is located in the vicinity of thecoronary sinus,6' 7 our data are in cleardisagreement with this electrocardiographicinterpretation. We never have recorded posi-tive P waves in lead II when the atria werepaced from this site.Our findings also conflict with the usual

criteria employed for the diagnosis of coro-nary sinus rhythm. We have found negative Pwaves in leads II, III, and aVF and P-Rintervals greater than 0.12 sec associated withactivity initiated low in the right and left atria(CRA and PLA) .Our data, obtained by simulation of hearts

in which there were no known conductiondefects, suggest that it probably is reasonableCirculation, Volume XLII, October 1970

to designate these three rhythms (uppernodal, coronary nodal, and coronary sinus) aslow atrial rhythms, in keeping with thesuggestion of Pick and Langendorf56 until aprecise identification of the mechanism re-sponsible for each has been provided.

P-R Interval

Our findings also suggest that anotherassumption employed in electrocardiographicinterpretations should be reevaluated. If thereis no reason to think that atrioventriculartransmission time has changed, it usually isassumed that differences in the P-R intervalreflect changes in the site of origin of the atrialimpulse or, in unusual circumstances, changesin conduction time throughout atrial muscle.Our findings indicate that differences in P-Rinterval need not provide an accurate indica-tion of the time lapse between initiation of theimpulse and its arrival at the A-V junction. Aswe have shown, and others have shownpreviously,12' 15, 57 there may be an isoelectricinterval between the time of activation of theatrium and the first clear evidence of a P wavein the body surface leads. Thus, the initialinscription of the P wave does not necessarilyprovide any indication of the time of initiationof the atrial impulse or the anatomic site ofimpulse initiation. Unless one assumes that thephenomena we have described would notoccur when the atria are activated by intrinsicpacemakers, it seems reasonable to concludethat the beginning of the P wave provides, atbest, only an imprecise index of the time atwhich a spontaneous impulse is initiated in theatrium. Furthermore, it seems likely that inthe presence of inflammatory or degenerativedisease, or perhaps after administration ofcertain drugs, the phenomena which we havedescribed would assume greater importance.A short P-R interval, thus, may reflect in partthe fact that the initial spread of activity fromits site of origin does not generate arecognizable contribution to the electrocardio-gram and that changes in P-R interval mayresult, not from change in the location of thepacemaker, but rather from changes in thetime required for the impulse to activate a

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sufficient segment of atrial muscle to cause avisible deflection in the ECG.P-Wave Polarity

We have shown that the P wave in leads II,III, and aVF is not always negative when theatria are activated from sites low in the rightatrium. The P wave may be biphasic (-, +)or positive. It is difficult to explain thesefindings on the basis of the Lewis thesis'0 thatspread of excitation in the atria is radial. Ifthis were so, initiation of atrial activation atsites low in the right atrium should alwaysresult in negative P waves in leads II, III, andaVF. Our results would be better explained ifspecialized atrial pathways or internodaltracts31' 32 play a role in determining thesequence of atrial activation.The likelihood of functionally significant

specialized pathways in the atria was firstemphasized by Eyster and Meek.58 60 Manyanatomic studies31' 32, 61-65 have demonstratedat least three such tracts, the anterior(AINT), middle (MINT), and posterior(PINT) internodal tracts. Furthermore,James31 demonstrated that a branch of theanterior tract extends to the left atrium inBachmann's bundle (the interatrial band).Evidence for specialized fibers in Bachmann'sbundle received physiologic support from thework of Wagner and associates66 and Childersand co-workers.67 Also, Vassalle and Hoff-man68 and Holsinger and associates69 havedemonstrated by physiologic technics theprobable existence of specialized paths be-tween the SA and A-V nodes.

It is reasonable to' suppose that thesepathways are important in determining thesequence of activation in the atria. They,therefore, must play an important role indetermining the polarity and morphology ofthe P wave. This becomes even more likelywhen one considers the finding that changingthe pacing site by only several millimeters inthe endocardial transition zone usually resultsin significant change in P-wave polarity andmorphology. The AINT, MINT, and PINT, asthey approach and enter the A-V node,probably run close to most of the endocardialpacing sites.31' 32 It is not difficult, then, to

modify the hypothesis of Danielopolu andProca19 and Brumlik25 and suppose that animpulse can rapidly spread retrograde, proba-bly through one or more of the internodaltracts, to Bachmann's bundle and the regionof the SA node and from there can depolarizesignificant areas of both atria in a sequencesimilar to that which occurs during so-callednormal sinus rhythm. The important point isthat under these conditions a significantportion of the left atrium and some of theright atrium would be depolarized in a"normal" sequence. This is consistent with thedata recently presented by Spach and asso-ciates26 and would explain the positive Pwaves in leads II, III, and aVF which arerecorded when the atria are activated fromsome of the right atrial endocardial pacingsites.No specialized pathways have been de-

scribed in the PLA region30' 31 which, whenstimulated, results in negative P waves inleads II, III, and aVF. Excitation of thisregion, therefore, could result in radial spreadand truly retrograde activation. Negative Pwaves in leads II, III, and aVF thus would beexpected when this area is paced.Data which would permit a complete

explanation, in terms of the sequence ofactivation, for the negative P waves producedin leads II, III, and aVF when the rightatrium is paced are not yet available. Also,there is no ready explanation for the biphasic-, + ) P waves recorded in leads II, III,

and aVF when the atria are paced from siteswithin the transition zone on the right atrialendocardium. It is clear, however, that thecloser the endocardial pacing sites are to theposterior left atrium, or conversely, the fartherthese sites are from the point where the AINTapproaches the A-V node, the greater thenegative portion and the smaller the positiveportion of the P wave. When the atria arepaced from the lips of the coronary sinusostium, the P wave is almost always totallynegative. This implies that if the impulsereaches the posterior left atrium quickly andbegins to depolarize the left atrium inretrograde fashion before the activity reaches


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Bachmann's bundle via the AINT, much ofthe P wave in leads II, III, and aVF will benegative. The longer it takes for activity toreach the posterior left atrium relative to itsarrival at Bachmann's bundle, the greater thepositive portion of the P wave. We havepreviously demonstrated70 in canine heartsthat a negative P wave in leads II, III, and aaVF is most consistently associated with earlyactivation of the postero-inferor region of theleft atrium (PLA). In this regard, it is worthsuggesting that, when stimuli are applied tothe caudal portion of the right atrial epicar-dium, the impulse spreads rapidly to theposterior left atrium, with subsequent retro-grade radial activation of the left atrium.Furthermore, it is reasonable to assume thatan impulse initiated at this site would notspread rapidly to Bachmann's bundle, andfurthermore that it would depolarize the rightatrium in a retrograde, as opposed to a"normal ,' fashion resulting in negative Pwaves in leads II, III, and aVF.

AcknowledgmentThe authors would like to express their appreciation

to Dr. M. Irene Ferrer for her valuable comments andcriticisms.

References1. SCHERF D, COHEN J: The Atrioventricular Node

and Selected Cardiac Arrhythmias. New York,Grune & Stratton, Inc., 1964, pp 47-105

2. KATZ LN, PICK A: Clinical Electrocardiography:Part I. The Arrhythmias. Philadelphia, Lea &Febiger, 1956, pp 100-104

3. FRIEDBERG CK: Diseases of the Heart. Philadel-phia, W. B. Saunders Co., 1966, pp 489-491

4. BELLET S: Clinical Disorders of the Heart Beat.Philadelphia, Lea & Febiger, 1963, pp 386-391

5. LANGENDORF R, SIMON AJ, KATZ LN: A-V blockin A-V nodal rhythm. Amer Heart J 27: 209,1944

6. EYRING EJ, SPODICK DH: Coronary nodalrhythm. Amer J Cardiol 5: 781, 1960

7. BIx HH: The electrocardiographic pattern ofinitial stimulation in the left auricle: A studywith a report of unusual arrhythmias originat-ing in the left auricle. Sinai Hosp J(Baltimore) 2: 37, 1953

8. MIROWSKI M: Left atrial rhythm: Diagnosticcriteria and differentiation from nodal arrhyth-mias. Amer J Cardiol 17: 203, 1966

Circulation, Volume XLIl, October 1970

9. SCHERF D, COHEN J: op. cit. reference 1, pp 21-22

10. LEWIs T: The Mechanism and Graphic Registra-tion of the Heart Beat, ed 3. London, Show &Sons, 1925, pp 83-88

1 1. BRENDEL W, RAULE WV, TRAUTWEIN W: DieLeitungsgeschwindigkeit und Erregungsaus-breitung in den Vorhdfen den Hundes. ArchGes Physiol 253: 106, 1950

12. PUECH P, ESCLARISSAT M, SODI-POLLARES D, ETAL: Normal auricular activation in the dog'sheart. Amer Heart J 47: 174, 1954

13. SCHER-AM: Excitation of the heart. In Handbookof Physiology, Section 2, Circulation, vol 1,edited by WF Hamilton, P Dow. Washington,D. C. American Physiological Society, 1962, p293

14. SCHAEFER H, HAAS HG: Electrocardiography. InHandbook of Physiology, op. cit., p 349

15. MOORE EN, JOMAIN SL, STUCKEY JH, ET AL:

Studies on ectopic atrial rhythms in dogs. AmerJ Cardiol 19: 676, 1967

16. WALDo AL, VITIKAINEN KJ, HARRIS PD, ET AL:The mechanism of synchronization in iso-rhythmic A-V dissociation: Some observationson the morphology and polarity of the P waveduring retrograde capture of the atria. Circula-tion 38: 880, 1968

17. GALLAVARDIN L, DuFOUR P, PETZETAKAS: Auto-matisme ventriculaire intermittant spontane ouprovoque par la compression oculaire etl'injection d'atropine dans les bradycardiestotales. Arch Mal Coeur 7: 1, 1914

18. GALLAVARDIN L, VEIL P.: Sur un cas debradycardie permanente a 40: Rythme nodalavec P positif ou dere-glage auriculoventricu-laire. Arch Mal Coeur 21: 210, 1928

19. DANIELOPOLU D, PROCA AG: Recherches sur lerhythme atrioventriculaire chez l'homme. ArchMal Coeur 19: 217, 225, 1926

20. SCHERF D, SHOOKHOFF C: Reitzleitungsstoerun-gen im Bundel. Wien Arch Inn Med 10: 97,1925

21. BORMAN MC, MEEK WJ: Coronary sinusrhythms: Rhythm subsequent to destruction byradon of the sino-auricular nodes in dogs. ArchIntern Med 47: 957, 1931

22. JOURDAN F, FROMENT R, GALLAVARDIN L, ET AL:

Trois observations de rhythme nodal experi-mental chronique par ablation chirurgicale dunoerd sinusal. Arch Mal Coeur 38: 197,1945

23. DRESSLER W, ROESSLER H: Premature beats inatrioventricular rhythm. Amer Heart J 51: 261,1956

24. PUECH P: L'activite Electrique AuriculaireNormale et Pathologique. Paris, Masson et Cie,1956, p 219; 212-213

25. BRUMLIK JV: The sinoatrial node, the atrioven-

669



ownloaded from


WALDO ET AL.

tricular node, and atrial dysrhythmias. InAdvances in Electrocardiography, edited byCK Kossmann. New York, Grune & Stratton,Inc., 1958, pp. 260-267

26. SPACH MS, KONG TD, BARR RC, ET AL:

Electrical potentical distribution surroundingthe atria during depolarization and repolariza-tion in the dog. Circulation Research 24: 857,1969

27. RUSKIN A, MCKINLEY WF, DECHARD CM:Studies of the A-V node: IV. A clinical studyof A-V nodal rhythm. Texas Rep Biol Med 3:86, 1945

28. SCHERF D: Ueber den atrioventriculaeren Rhyth-mus. Z Ges Exp Med 78: 511, 1931

29. PRINZMETAL M, CORDAY E, BRILL IC, ET AL: TheAuricular Arrhythmias. Springfield, Illinois,Charles C Thomas, Publisher, 1952, pp 36-64;73-97

30. SCHERF D, BLUMENFELD S, YILDEZ M: Experi-mental studies on A-V nodal rhythm followingsuppression of activity of the sinus node. AmerJ Cardiol 10: 234, 1962

31. JAMES TN: The connecting pathways betweenthe sinus node and A-V node and between theright and the left atrium in the human heart.Amer Heart J 66: 498, 1963

32. MERIDETH J, TITUS JL: The anatomic connec-

tions between the sinus and A-V node.Circulation 37: 566, 1968

33. STUCKEY JH, HOFFMAN BF, SASKENA CP, ET AL:

Electrode identification of the conductionsystem during open heart surgery. Surg Forum9: 202, 1957

34. KAISER GA, WALDo AL, BEACH PM, ET AL: Animproved electrophysiologic technique to iden-tify the cardiac conduction system at surgery.

Arch Surg. In press

35. STUCKEY JH, HOFFMAN BF, AMER NS, ET AL:

Localization of bundle of His with a surfaceelectrode during cardiotomy. Surg Forum 10:551, 1960

36. STUCKEY JH, HOFFMAN BF: Prevention of injuryto the specialized conduction system. ArchSurg 85: 224, 1962

37. HARMIS PD, KAISEK GA, BOWMAN FO, ET AL:

The use of a digital readout unit for rapiddetermination of myocardial stimulation thres-holds. Surgery 65: 10, 1969

38. HARRIS PD, SINGER DH, MALM JR, ET AL:

Chronically implanted cardiac electrodes fordiagnostic therapeutic and investigational use

in man. J Thorac Surg 54: 191, 196739. WALDO AL, Ross, SM, KAISER GA: The

epicardial electrogram in the diagnosis ofcardiac arrhythmias in the postoperative peri-od. Geriatrics. In press

40. GOLDBERG LI: Pharmacology of cardiovasculardrugs. In The Heart, edited by JW Hurst, RB

Logue. New York, McGraw-Hill Book Co.,1966, p 153

41. BROOKS C MCC, HOFFMAN BF, SUCKLING EE, ETAL: Excitability of the Heart. New York, Grune& Stratton, Inc., 1955, p 178

42. LISTER JW, STERN E, KoSOWSKY BD, ET AL:Atrioventricular conduction in man: Effect ofrate, exercise, isoproterenol and atropine on theP-R interval. Amer J Cardiol 16: 516. 1965

43. LEwis T: Galvanometric curves yielded bycardiac beats generated in various areas of theauricular musculature: The pacemaker of theheart. Heart 2: 23, 1910

44. ROGEL S, MiRowsKi M: Experimental left atrialrhythm. Israel J Med Sci 2: 352, 1966

42. LISTER JW, STERN E, KoSOWSKY BD, ET AL:Coronary sinus catheterization for studyingcoronary blood flow and myocardial metabo-lism. Amer J Physiol 152: 340, 1948

46. LEVINE HD, GOODALE WT: Studies in intracar-diac electrocardiography in man: IV. Potentialvariations in the coronary venous system.Circulation 2: 48, 1950

47. GIRARD G, LATOUR H, PUECH P: Le'lectrocar-diographie du sinus coronaire: 2e partie. Etudeelectrocardiographique endocavitaire des dys-rythmies du sinus coronaire chez l'homme.Arch Mal Coeur 47: 1008, 1954

48. LANCASTER JF, LEONARD JJ, LEON DF, ET AL:The experimental production of coronary sinusrhythm in man. Amer Heart J 70: 89, 1965

49. LAU SH, COHEN SI, STEIN E, ET AL: P wavesand P loops in coronary sinus and left atrialrhythms. Amer Heart J 79: 201, 1970

50. LEON DF, LANCASTER JF, SHAVER JA, ET AL:Right atrial ectopic rhythms: Experimentalproduction in man. Amer J Cardiol 25: 6,1970

51. HARRIs BC, SHAVER JA, GRAY S III, ET AL: Leftatrial rhythm: Experimental production inman. Circulation 37: 1000, 1968

52. DAMATO AN, LAU SH: His bundle rhythm.Circulation 40: 527, 1969

53. HOFFMAN BF, CRANEFIELD PF: The physiologi-cal basis of cardiac arrhythmias. Amer J Med37: 670, 1964

54. WATANABE Y, DRE1FUS LS: Sites of impulseformation within the atrioventricular junctionof the rabbit. Circulation Research 22: 717,1968

55. ERLANGER J: The localization of impulse initia-tion and conduction in the heart. Arch InternMed 2: 334, 1913

56. PICK A, LANGENDORF R: Recent advances in thedifferential diagnosis of A-V junctional ar-rhythmias. Amer Heart J 76: 553, 1968

57. WEDD AM, STRouD WD: The spread of theexcitation wave related to the standard


670



ownloaded from



electrocardiogram in the dog's heart. Heart 9:15, 1921-22

58. EYSTER JAE, MEEK WJ: Experiments on theorigin and propagation of the impulse in theheart: The point of primary negativity in themammalian heart and the spread of negativityto other regions. Heart 5: 119, 1913-14

59. EYSTIR JAE, MEEK WJ: Experiments on theorigin and conduction of the cardiac impulse:VI. Conduction of the excitation from the SAnode to the right auricle and AV node. ArchIntern Med 18: 775, 1916

60. EYSTER JAE, MEEK WJ: Experiments on theorigin and conduction of the heart beat: IX.Sinoventricular conduction. Amer J Physiol61: 130, 1922

61. WENCKEBACH KF: Beitrage zur Kenntnis dermenschlichen Herztatigkeit. Arch Anat Physiol1-2: 1, 1907

62. WENCKEBACH KF: Beitrage zur Kenntnis dermenschlichen Herztatigkeit. Arch Anat Physiol3: 53, 1908

63. THOREL C: Vorlaufige Mitteilung uber einebesondere Muskel verbindung zwischen der

Cava superiur und dem Hisschen Bundel.Munchen Med Wschr 56: 2159, 1909

64. THOREL C: Uber den Aufbau des Sinusknoteusund seine Verbindung mit der Cava superiurund den Wenckebachschen Bundeln. MunchenMed Wschr 57: 183, 1910

65. BACHMANN G: The inter-auricular time interval.Amer J Physiol 41: 309, 1916

66. WAGNER ML, LAZZARA R, WEIss RM, ET AL:

Specialized conducting fibers in the interatrialband. Circulation Research 18: 502, 1966

67. CHILDERS RW, MERIDETH J, MOE GK: Super-normality in Bachmann's bundle: An in vivoand in vitro study. Circulation Research 22:363, 1961

68. VASSALLE M, HOFFMAN BF: Spread of sinusactivation during potassium administration.Circulation Research 17: 285, 1965

69. HOLSINGER JW JR, WALLACE AG, SEALY WC:The identification and surgical significance ofthe atrial internodal conduction tracts. AnnSurg 167: 447, 1968

70. VITIKAINEN KJ, WALDO AL, HARIMS PD, ET AL:Significance of P wave inversion. Amer JCardiol 19: 154, 1967


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MALM and BRIAN F. HOFFMANALBERT L. WALDO, KARI J. VITIKAINEN, GERARD A. KAISER, JAMES R.

DepolarizationThe P Wave and P-R Interval: Effects of the Site of Origin of Atrial

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