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The electrocardiogram in the newborn period. I. the normal infant
FETAL
AND
NEONATAL
M E D I C I N E inch.rer. Behrman,Editor
The electrocardiogram in the newborn period I The normal infant Alois R. Hastreiter, M.D., * and Jose B. Abella, M.D. CHICAGO,
ILL.
I N T E g P R ] g T A T I O iN" o f the electrocardiogram (ECG) in the neonatal period is more difficult than at any other age because of the rapid perinatal hemodynamic changes and the wide overlap of normal and abnormal findings. Adequate analysis of the tracings requires a well-standardized recording technique (size and position of electrodes and calibration). Normal standards reported for this age group also vary because they are based on data obtained with different types of recorders (photographic, directwriter, and jet-writer)? "33 Information is particularly scarce for some of the leads frequently used in newborn infants and younger children (V4R, VaR, and VT). In addition, data are often grouped together over relatively wide periods of time (e.g., 0 to 24 hours, 2 to 7 days, or 8 to 30 days). Finally, in evaluating the ECG, there is no general agreement about how to take into consideration various age and growth factors (chronologic age, gestational age, weight, state of nutrition, and anemia) and perinatal factors that affect the circulation (placental transfusion, persistent arteriovenous shunt through the ductus arterious, and hypoxia).
From the University of Illinois Hospital. Supported in part by the University o[ Illinois Foundation, Goodenberger Medical Research, No. 2-44-33-66-3-14. ~Repr~nt address: Department o~ Pedhztrles, University o] Illinois Hospital, 840 S. Wood St., Chicago, Ill. 60612.
Vol. 78, No. I, pp. 146-I56
The purpose of this review is threefold: (1) to describe the normal ECG of the newborn infant and its evolution during the neonatal period (Tables I to V), (2) to correlate the electrocardiographic changes with the perinatal physiologic events, and (3) to review the electrocardiographic abnormalities in this age group (Part I I ) . The normal electrocardiographic characteristics of premature and postmature newborn infants are also briefly described. VECTORCARDIOGRAPHIC APPROACH TO THE SCALAR ELECTROCARDIOGRAM During depolarization and repolarization of a single myocardial cell, the electrical forces produced at any given instant can be represented by a single equivalent dipole or mean vector which expresses the total effect of all elementary dipole forces. According to the "equivalent dipole" concept of electrocardiography, the electrical activity of the heart, as manifested at the body surface, can also be represented at any given instant by a single equivalent dipole or its corresponding mean vector. The process of depolarization and repolarization is much more complex in the heart muscle than in the single muscle cell; e.g., atrial excitation spreads radially throug the atria at a uniform speed, and the Purkinje system provides the
Volume 78 Number 1
ventricles with a specialized conduction path. However, ventricular depolarization and repolarization may be simplified by visualizing a segment of ventricular wall as if it consisted of a single muscle fiber extended from endocardium to epicardium; the resulting electrical forces produced by activation of the ventricular wall are directed outward, perpendicular to the epicardial surface. The electrical forces produced during activation of different portions of the heart follow a certain course in time and vary widely in direction, electrical sense, and magnitude. The balance between opposing forces determines the electrical field of the heart at a given instant (at the body surface) and can be visualized as a single equivalent dipole or mean instantaneous spatial vector. The purpose of the ECG (and vectorcardiogram) is to provide information concerning the orientation and magnitude of the instantaneous cardiac spatial vectors. The changing projections of these vectors on a given plane plotted against time results in a "vector loop"; recording these vectors on a given lead axis produces the familiar P, QRS, and T deflections, which reflect the sequence of atrial depolarization and ventricular depolarization and repolarization. Rather than just analyzing the various configurations of conventional scalar ECG patterns as such, one should view them as sequential projections of the spatial vector; the latter is much easier to describe and memorize. An approximate reconstruction of the sequential changes of the spatial vector projected on a plane ("vector loop") can be made from analysis of 2 scalar leads in the same plane (preferably perpendicular). Thus, the events projected on the frontal plane can be reconstructed by a combination of standard leads I and aVF and events in the horizontal plane by precordial leads V2 and V6. The events in space can be reconstructed by a synthesis of the two planes. The cardiac spatial vector is equal to the vectorial sum of its projection on the transverse (x axis, leads I or V6), vertical (y axis, lead aVF), and sagittal axis
Electrocardiogram in normal neonate
14 7
(z axis, lead V2). This subject is reviewed in detail elsewhere. 2, 5, 7, s CIRCULATORY ADAPTATIONS IN THE NEWBORN PERIOD
The thickness of the ventricular and atrial walls and the size of these chambers are determined by the work that they do in carrying a volume of blood and overcoming the resistance to ejection of this blood. The right and left ventricles have the same pressure in utero, but the resistance offered by the semicollapsed lungs to pulmonary blood flow is higher than the systemic resistance (right ventricular "pressure work" is greater). Before birth the low-resistance placenta (which receives about 55 per cent of the combined ventricular output) is part of the systemic circulation, the systemic small muscular arteries have less muscle mass than the pulmonary arteries, 3~ the left ventricle is smaller than the right, as and there is a large blood flow from pulmonary artery to aorta through the ductus arteriosus. Pulmonary vasoconstriction is also an important contributing factor in elevating the pulmonary vascular resistance. At birth, removal of the placenta results in a marked increase of the systemic vascular resistance; the first breath causes a decrease in pulmonary vasoconstriction and a drop of the pulmonary vascular resistance. Therefore, shortly after birth systemic and pulmonary resistances are similar. The pulmonary vascular resistance continues to fall, and within a few hours after birth the flow through the ductus arteriosus reverses and then disappears. There is also a large increase in pulmonary venous return to the left atrium and ventricle. By the end of the first day of life the pulmonary artery pressure is reduced to about one half that of the systemic, and by 2 weeks of age it is close to that of adults. Pulmonary vasoconstriction may be increased by hypoxemia and acidemia, which are more frequent in low-birth-weight and immature infants. The arteriovenous shunt through the ductus arteriosus also may be larger and persist longer in this group. The amount of placental transfusion at birth which is
14 8
Hastreiter and Abella
The Journal of Pediatrics January 1971
T a b l e I. H e a r t r a t e , P R i n t e r v a l , P - w a v e d u r a t i o n , Q R S a m p l i t u d e i n l e a d I I of m a t u r e n e w b o r n i n f a n t s ~
Age
t Minimum Heart rate
0 - 24 hr. 1- 7 days 8 - 30 days
[
5%
I
Mean
94 100 115
85 100 115
duration, and P-wave
[
95%
119 133 163
I Maximum
145 175 190
[
I45 175 190
s.D. 16.1 22.3 19.9
PR interval 0 - 24 hr. 1- 7 days 8 - 30 days
0.07 0.05 0.07
0.07 0.07 0.07
0.10 0.09 0.09
0.12 0.12 0.11
0.13 0.13 0.13
0.012 0.014 0.010
0.040 0.038 0.040
0.051 0.046 0.048
0.065 0.061 0.057
0.075 0.065 0.065
0.066 0.066 0.064
0.05 0.04 0.04
0.065 0.056 0.057
0.084 0.079 0.073
0.09 0.08 0.08
0.010 0.010 0.009
1.5 1.6 1.6
2.3 2.5 2.4
2.6 2.8 2.7
0.50 0.51 0.48
P-wave duration 0 - 24 hr. 1- 7 days 8 - 30 days
0.040 0.035 0.040
QRS duration 0 - 24 hr. 1- 7 days 8 - 30 days
0.05 0.04 0.04
P-wave amplitude in I f 0 - 24 hr. 1 - 7 days 8 - 30 days
0 0.5 0.5
0.8 0.8 0.8
~Data from Ziegler 1 (photographic records), fifth and nlnety-fifth percentiles recalculated by Liebman. ~
T a b l e I I . M e a n f r o n t a l , Q R S , a n d T axes i n m a t u r e n e w b o r n i n f a n t s ~
Q RS axis (frontal plane)
T axis (frontal plane)
Minimum
5%
Mean
95%
mum
Minimum
0 - 2 4 hr.
60
60
135
180
180
-20
I-
7 days
60
80
125
160
180
-40
8 - 3 0 days
0
60
110
160
180
-20
0
Age
Maxi-
Mean
95%
Maximum
0
70
140
180
-40
25
80
100
35
60
120
5%
eData from Liebman. ~
T a b l e I I I . A m p l i t u d e s of R a n d S w a v e s i n p r e c o r d i a l l e a d s ~
S wave
R wal)e
Age
Minimum
5%
Mean
95%
30 hr. 1 too.
3.5 3.0
4.0 3.3
8.6 6.3
14.2 8.5
30 hr. 1 too.
5.0 4.0
4.3 3.3
11.9 11.1
21.0 18.7
30 hr. 1 mo.
2.0 3.8
3.I 3.8
9.4 15.0
16.6 24.2
30 hr. 1 too.
1.5 1.0
1.5 1.0
5.4 10.8
tl.3 16.2
MiniMaximum mum Amplitudes in V~R 15.0 12.0
0.0 0.0
Maxi-
5%
Mean
95%
0.2 0.8
3.8 1.8
13.0 4.6
12.0 9.0
1.1 0.0
9.7 6.1
19.1 15.0
26.0 15.0
2.4 2.8
9.5 8.3
18.5 16.3
22.0 30.0
1.0 0.0
5.6 4.8
13.8 9.5
20.0 18.0
mum
Amplitudes in V1 30.0 20.0
0.0 0.0
Amplitudes in Vs 20.0 30.0
0.5 0.0
Amplitudes in Vs 15.0 22.0
0.2 0.0
~Data from Namin ~, a (direct writer), fifth and ninety-fifth percentiles recalculated by L i e b m a n )
Volume 78 Number 1
Electrocardiogram in normal neonate
149
T a b l e I V . A m p l i t u d e s of R a n d S w a v e s i n p r e c o r d i a l l e a d s ~ R 733aue
Age
Minimum
5%
S waue
Mean
95%
Maximum
Minimum
S.D.
5%
Mean
95%
Maximum
S.D.
0-24 hr. 1- 7 days 8-30 days
5.5 5.5 2.5
7.0 9.0 4.2
14.8 18.2 11.4
20.0 27.4 19.8
20.5 29.5 26.5
Amplitudes in V1 3.75 0 5.44 1.5 4.97 0
2.5 4.6 2.5
9.3 10.4 5.0
27.0 18.8 12.8
28.5 25.5 18.5
7.99 4.70 3.73
0-24 hr. 1- 7 days 8-30 days
11.5 8.5 5.5
13.0 11.7 6.8
20.1 19.9 17.5
28.1 31.1 29.0
29.5 32.5 32.5
Amplitudes in V~ 3.81 5.0 5.89 5.0 6.48 1.0
9.0 9.3 4.2
20.3 20.2 14.0
33.8 34.1 25.7
37.0 37.0 29.0
6.73 7.26 6.24
0-24 hr. 1- 7 days 8-30 days
12.0 4.0 0.0
12.7 8.8 8.3
18.8 18.1 18.8
26.7 30.0 33.8
28.0 40.0 36.0
Amplitudes in V~ 4.12 10.0 12.0 6.55 0 2.6 7.50 2.0 4.2
25.0 17.1 12.4
32.0 33.0 20.0
38.0 38.0 26.0
6.05 8.37 5.47
0-24 hr. 1- 7 days 8-30 days
8.0 4.0 4.0
9.0 4.9 3.3
17.4 18.8 15.9
26.0 33.1 33.3
32.0 36.0 36.0
Amplitudes in V~ 5.97 2 7.24 0 7.82 0
4.0 3.4 3.1
21.8 13.2 6.8
36.0 27.7 16.3
42.0 30.0 18.0
9.08 8.11 5.05
0-24 hr. 1- 7 days 8-30 days
0.0 0.0 0.0
4.0 3.4 3.5
10.2 10.7 11.9
18.0 19.3 27.0
24.0 28.0 36.0
Amplitudes in V5 5.44 0 5.54 0 7.28 0
0.0 3.6 2.7
11.9 6.8 4.8
24.0 16.2 12.3
31.5 19.5 13.5
6.87 4.73 3.50
0-24 hr. 1- 7 days 8-30 days
0 0 0
2.3 2.2 1.7
3.3 5.1 6.7
7.0 13.1 20.5
7.5 16.5 25.5
Amplitudes in V~ 2.10 0 3.97 0 4.82 0
1.6 0.8 0.6
4.5 3.3 2.0
10.3 9.9 9.0
14.0 14.0 10.0
2.78 2.99 2.46
0-24 hr. 1- 7 days 8-30 days
-0 0
. 0.5 1.0
.
. 7.5 6.5
Amplitudes in A V R . . . . 1.80 3.0 3.7 1.39 5.0 5.6
. 7.9 10.1
. 13.9 14.6
15.0 15.0
3.11 2.81
0-24 hr. 1- 7 days 8-30 days
-0 0
. 0.5 1.2
.
. 6.5 7.5
Amplitudes in A V L . . . . 1.04 0 1.4 1.48 0 2.2
. 5.2 5.3
. 9.7 8.9
13.0 13.0
2.48 2.10
0-24 hr. 1- 7 days 8-30 days
-1.0 1.0
. 1.9 1.4
.
. 13.0 15.0
Amplitudes in A V F . . . . 2.43 0 0.6 3.39 0 0.6
. 0.7 0.6
. 3.1 3.8
3.5 5.5
1.10 1.20
. 2.8 2.0
. 6.4 4.0
. 1.7 2.2
. 3.3 5.8
. 5.4 6.1
. 10.5 12.4
"~Data from Zieglerx (photographic records), fifth and ninety-fifth percentiles recalculated by Liebman.5
T a b l e V . A m p l i t u d e o f T w a v e s i n p r e c o r d i a l l e a d s V~ to V6 ~ V~
Age 0-24 hr. 1- 7 days 8-30 days
Vs
Mean
95%
Maximum
.4.3 4.4 5.3
72 7.7 8.1
8.5 8.5 8.5
"~Data from Liebman.5
S.D.
Mean
95%
0.95 1.39 1.49
3.3 4.9 5.3
6.8 7.3 7.5
V,
Maximum
S.D.
Mean
95%
mum
S.D.
7.5 7.5 10.5
1.62 1.44 1.50
2.4 2.9 3.5
3.9 4.2 5.3
4.5 4.5 7.5
0.63 0.67 1.01
maxi-
150
Hastreiter and Abella
related to early or Iate clamping of the umbilical cord (with or without stripping) may affect the blood volume, cardiac output, and the pressures in the cardiac chambers for several hours or days after birth. The higher cardiac output associated with anemia in the premature infant probably adds to the work of both ventricles. The changes in right and left ventricular weights occurring perinatally are as follows 3s : At 30 weeks' gestation the left ventricle is thicker than the right (average weight ratio 1.15:1), at 32 to 35 weeks' they are equal, and at about 36 weeks' the average newborn value of 1.3:1 (favoring the right ventricle) is attained. Following birth, the left ventricular wall rapidly increases in thickness. At one month the left ventricle is heavier than the right, and by 6 months the ratio is about 2:1 in favor of the left ventricle. The adult ratio is 2.5:1. ELECTROCARDIOGRAPHIC VECTORS IN THE NEWBORN INFANT
QRS vector. The newborn infant's right ventricular dominance is well known, but the degree of dominance is variable, resulting in a wide spread of normal values. The mean spatial QRS vector during the first 2 weeks of llfe is oriented to the right, anteriorly and inferiorly. It gradually rotates leftward and inferiorly; at the end of the first month it points predominantly inferlorly, anteriorly, and slightly to the right. In the adult it is oriented inferiorly, posterio'rly, and to the left and has a considerably greater magnitude. Thus, the newborn infant's ECG exhibits prominent and prolonged anterior forces resulting in a tall and broad R wave in the right chest leads and often a deep S wave in the left chest leads. The leftward vector in the newborn infant is small; consequently the R wave in the left precordium has low amplitude initially but increases rapidly in the first few months. The posterior vector, although variable, is frequently small in the newborn period and appears late. Thus, the S wave in leads V1 and V2 is small. By 2 years of age the posterior vector predominates.
The ]ournal o[ Pediatrics ]anuar7 1971
The init{al or septal vector may be to the left in the newborn period (less so in the premature infant). Rarely this may result in a qR complex in lead V~R or even in V1 and absent or small Q waves in the left chest leads. With aging, the initial vector extends further to the right, and the Q wave increases in the left precordium. The initial vector can be very superior in infancy and childhood, causing a prominent Q wave in lead aVF which gradually decreases throughout childhood. The terminal rightward force is prominent in the newborn infant and gradually decreases over months to years. This explains the deep S wave in the left chest leads, which decreases with age. The terminal vector tends to become more superior and is important in evaluating left-axis deviation. The newborn infant's ECG almost invariably demonstrates clockwise rotation in the frontal plane and usually (but less often) also in the horizontal plane. The horizontal plane changes rapidly; if this vector is not counterclockwise by 3 months of age, right ventricular hypertrophy can usually be diagnosed. The frontal plane only gradually changes its inscription with aging so that in older childhood the vector loop usually can be inscribed in either direction. The clockwise or counterclockwise direction of depolarization is reflected in the scalar leads by the ventricular activation time (time from the onset of the QRS complex to the peak of the R wave); a ventricular activation time shorter in lead V6 than in lead V2 indicates clockwise rotation and the opposite pattern counterclockwise rotation. The QRS patterns in the chest leads were classified by Alimurung and associates 36 into: (1) adult R / S progression--the S wave has higher amplitude than the R wave in the right chest leads and smaller than the R wave in the left chest leads, (2) partial reversal of the R / S progression--the R-wave amplitude is higher than that of the S wave in both right and left chest leads, and (3) complete reversal of R / S progression--the R wave is larger than the S wave in the right and smaller than the S wave in the left chest leads. The newborn infant has
Volume 78 Number 1
Electrocardiogram in normal neonate
either complete (50 per cent) or partial reversal (50 per cent) but no adult progression (with rare exceptions) of the R / S ratio. By one month of age complete reversal disappears and adult R / S progression is common. A pure R wave in lead V1 is rare and a qR wave only exceptionally seen in newborn infants. T vector. Dramatic changes occur in the T vector following birth. Within the first 5 minutes following birth this vector is oriented to the left, anteriorly and minimally inferiorly; by 1 to 6 hours it has shifted much more inferiorly and to the right. Over the next several days the vector rotates markedly to the left and eventually becomes oriented to the left and posteriorly. In our own series, during the first 24 hours the T vector was still oriented to the left, anteriorly and inferiorly; at 2 to 7 days it was oriented to the left, posteriorly and inferiorly. These changes of the T vector explain the upright T wave in lead V1 and the negative or flat T wave in lead V6 in the early neonatal period.
statistical difference in their heart rates2 PR interval. T h e average 'PR interval at birth is 0.096 seconds; it increases to 0.100 after several minutes to hours and then declines to a low of 0.095 seconds at approximately 1 to 3 weeks of age. 1~ It gradually increases to reach 0.110 seconds at the end of the first year and 0.150 seconds in adult life. Hypervolemia secondary to delayed clamping a n d / o r vigorous stripping of the umbilical cord appears to lengthen the PR interval (average 0.124 seconds at birth)a2; this interval declines at 4 to 5 days of age to reach a level comparable to that of infants with early clamping of the cord. There is no statistically significant difference between the duration of the PR interval in premature and in full-term infants, a~ 2~ Duration o[ the P wave. Walsh 12 observed a duration of 0.060 seconds at birth in infants with early clamped cords versus 0.082 in those with stripped cords. Following birth it declines to a low value of about 0.050 which is maintained during the first month of life. PR segment. The average value of the PR segment is relatively constant throughout childhood, ranging from 0.050 to 0.065 seconds. According to Burch and DePasquale, ~ it averages 0.054 seconds in the first week of life and reaches the lowest value of 0.044 seconds at 3 to 6 months of life. Q R S interval. The duration of the QRS complex increases gradually throughout childhood. At birth it averages 0.065 seconds; it falls to about 0.055 seconds at the end of the first week and gradually increases to reach 0 . 0 6 8 seconds at 12 months; the adult value is 0.080. Ventricular activation time. At birth ventricular activation time in lead Va averages 0.018; it falls to 0.016 at 3 to 5 days of age and climbs to a maximum of 0.024 at 3 to 6 months. The adult level, averaging 0.020 seconds in lead V1, is reached at the end of the first year. During the first day of life, the average value is 0.019 in lead V6; at one month of age it is 0.023 and at one year 0.031 (Ziegler, 1 photographic method). Burch and De-
THE NORMAL SCALAR ELECTROCARDIOGRAM A N D ITS E V O L U T I O N IN THE NEWBORN PERIOD
T h e study of the normal electrocardiogram of the newborn infant will be divided into: (1) the time relationships or intervals, (2) the axes, and (3) the amplitudes in the various leads. Pursuing a vectorial approach for analysis of the ECG, these parameters will be studied in the frontal plane (standard leads) and in the horizontal projection (precordial leads). Intervals (Table I). Heart rate. At birth the average heart rate is 140 beats per minute. It drops to slightly less than 120 during the first several hours and then rises gradually to attain a maximum average rate of 160 at 1 to 3 months of age? 5 Premature infants have a slightly higher heart rate than full-term infants for the corresponding postnatal agel~ when premature and full-term infants of similar weight but different postnatal ages are compared, there is no
15 1
152
Hastreiter and AbeUa
Pasquale, 6 using the direct writing method, obtained slightly higher values for the ventricular activation time in lead V1 and lower values in lead V6. The ventricular activation time in lead V~ is lower in premature infants than in full-tei~l infants of comparable age. The same occurs when premature infants who have attained full-term size are compared to mature infants of similar weight2 There is controversy in the literature concerning the importance of the ventricular activation time. ~ QT interval. At birth the Q T interval is relatively long (0.296 seconds); the lowest value is reached at about 3 weeks (0.240 seconds). It then increases to a value of 0.260 to 0.270 seconds at one year and 0.370 in early adulthood. The corrected Q T interval or QT index (QTe) remains remarkably constant throughout childhood; the average value is 0.400 seconds. However, significant changes occur during the neonatal p eriod15: The average value at birth is 0.400 seconds; it then rises to a peak of 0.420 during the first 24 hours and declines rapidly to about 0.405 to 0.410 at the end of the second day and to 0.385 at one month (lowest value). The stable adult value is reached at the end of the second month. Walsh a~- describes a higher value of the QTe for infants with late clamping or stripping of the cord--0.440, compared to those with early clamped cord, 0.405. There is considerable disagreement in the literature as to the value of the QTo measurement. Axes (Table II). These will be described in the frontal and horizontal planes. P-wave axis (frontal). It averages +60 degrees at birth and declines to +54 degrees toward the end of the first month. In later childhood and adulthood it remains relatively constant at about +50 degrees. P-wave axis (horizontal). The P wave remains stationary at +50 degrees throughout the first month? ~ The average adult level is +5 degrees. QRS axis (frontal). The mean frontal QRS axis remains relatively constant throughout childhood and adulthood (average value +60 degrees), with the excep-
The ]ournal o[ Pediatrics January 1971
tion of the first 6 months of life. The average value during the first day of life is about +I35 degrees, at 1 week 130 degrees, at 3 weeks 105 degrees, at 5 weeks 90 degrees, and at the end of the second month 75 degrees. In premature infants the mean frontal QRS axis has a significantly lower value than in full-term infants up until the end of the second week? ~ The initial frontal QRS vector is approximately 0 degrees at birth and becomes gradually more superiorly oriented reaching -20 degrees at the end of the first month. The final frontal QRS vector is +170 degrees on the first day of life and subsequently remains relatively stationary throughout the first month of life, average value +165 degrees? ~ QRS axis (horizontal). This mean QRS axis has an average value of +130 during the first day of life, decreases gradually to about 110 degrees at the end of the first week, and remains stationary throughout the first month. It then gradually decreases with age toward normal adult value of -10 degrees. The initial and final QRS vectors in the horizontal plane maintain a relatively constant value of +70 degrees and +245 degrees throughout the first month of life? ~ The corresponding adult values are +50 degrees and -80 degrees. T-wave axis (fro.ntal). Marked changes of this axis occur during the newborn period. According to Hair and Gasu121 the frontal T-wave axis is +7 degrees from 1 to 5 minutes after birth, then shifts to +115 degrees at 2 to 4 hours after birth; this is followed by a gradual return to approximately the previous level (+10 degrees) during the ensuing 2 to 7 days. From the first week to the beginning of the third month of life the frontal T-wave axis gradually increases to reach a maximum of +60 degrees. T-wave axis (horizontal). This axis shifts from +67 degrees immediately after birth to +130 in the following 2 to 6 hours and then rotates back to about -10 degrees at 3 days and -28 degrees at 7 days of age. The axis remains at this level throughout the first month.
Volume 78 Number 1
Electrocardiogram in normal neonate
Amplitudes. Changes in amplitude of various ECG parameters with age in the newborn period are shown in Tables III to V. A brief description of this evolution follows. P-wave amplitude (frontal). The evolution of the P wave is best studied in lead II '~, lz: From birth it decreases to a low point at about 2 days of age and later gradually rises. P-wave amplitude (horizontal). In lead V~ the P wave rises slightly during the first few weeks or months; it then declines gradually and starts rising again at several months of age and finally stabilizes at about 4 years. In lead V6 the P wave remains relatively stable throughout childhood. Q-wave amplitude (frontal). The most interesting feature in the newborn period is perhaps the definite increase in depth of the Q wave in all leads (except aVL) following birth. It reaches a maximal depth at several months of age and then gradually declines in amplitude. Q-wave amplitude (horizontal). In the newborn infant a Q wave is only exceptionally present in leads V4R to V2; the incidence is higher the further the lead is to the left of the precordium. This incidence of Q wave is lower at birth than in the subsequent days and weeks. The incidence expressed in per cent is as follows:
Following birth there is an initial decline in the amplitude of the R wave in most precordial leads with a slow subsequent rise to adult levels; in the right chest leads VaR to V1 the reduction continues until adulthood. The S wave increases in depth following birth in all precordial leads except VsR. and V4R. A maximal depth is reached at about the second day and is followed by a gradual rise over the remaining 1 to 2 months. Lead V4R has a relatively constant amplitude throughout this period. These changes result in the relatively constant magnitude of R + S but a more prominent negative component (deeper S wave) hnmediately following birth.
I Birth Adult
v: 0 0-5
I
I 8 40
v: 60 80-90
I
v= 73 90-100
R- and S-wave amplitudes (frontal) (Table IV). After birth there is a reduction in the amplitude of the R wave in all standard leads. This is followed by a gradual rise over the next few months except in lead aVR, which remains stationary. There is also an initial decrease in the amplitude of the S wave during the first 1 or 2 months in all standard leads. As a consequence the magnitude of R + S is much smaller at birth than in the subsequent months.
R- and S-wave amplitudes (horizontal).
15 3
T-wave amplitude (frontal) (Table V). The amplitude of the T wave in the standard leads tends to change considerably during the first month of life and then remains at a relatively stable level. T-wave amplitude (horizontal). In the horizontal plane the incidence of a positive T wave in the right precordium and a negative or flat T wave in the left precordium are important because of the marked changes involving the T vector in tile early days after birth. At birth the incidence of upright T waves in lead V1 is about 70 per cent. There is a gradual decline over the next several days, so that by the fifth day the average incidence reaches 0. At the time of birth over 60 per cent of the T waves in lead V6 are upright; this declines to less than 10 per cent during the first day with a rise to about 50 per cent by the end of the first day to 100 per cent by the fourth day. This same phenomenon is reflected in the amplitude of the T wave in leads V1 and V6. ELECTROCARDIOGRAM PREMATURE INFANTS
OF
In premature infants the right ventricle to left ventricle weight ratio and the muscle mass of the small muscular arteries in the lungs is less than in full-term infants. There is, therefore, less right ventricular dominance in premature infants. The question of whether or not the premature infant's ECG presents characteristic
1 54
Hastreiter and AbeIla
features different from those of mature newborn infants is not answered despite a number of comprehensive studies. 4, 9, ~0, 24, 27 In part this is because the premature newborn infant's ECG shows even more variability than that of the full-term infant. However, some differences do exist and these are particularly apparent in the first week of life. The most striking features are as follows: (1) There is generally lower voltage of the R, S, and T wave, particularly in the standard limb leads. This is best appreciated in the first week of life. Despite the lower voltage, the R / S ratio is generally higher in both the right and left chest leads. The P-wave amplitude may also be lower than in full-term newborn infants but occasional premature babies may have tall and peaked P waves. (2) There is less right ventricular dominance in the tracings from premature infant than from mature newborn infants. This observation is more striking in the Frank vectorcardiogram than in the conventional scalar ECG4; it shouts a more rapid evolution toward left ventricular dominance, e.g., counterclockwise rotation in the horizontal plane occurs early, between 24 and 72 hours of age? In the conventional electrocardiogram, this is manifested by fewer upright T waves in lead V~ than in full-term newborn infants (there is also a significant difference in this regard between smaller and larger premature newborn infants), a higher incidence of deep Q waves in lead V~, and the mean QRS and T vectors may be more leftward in the frontal plane. (3) A longer Q T interval has been described in premature infants than in full-term infants, although Walsh describes a shortened, scooped-out ST segment. (4) ST deviations are more common in premature infants; they usually consist of ST depression in the right chest leads. This distinction between premature and full-term infants may not be significant. A study comparing premature and mature infants of similar weight 9 (average ages 1.5 to 3 months and 5.5 days, respectively) also revealed a tendency toward relative left ventricular dominance for the premature
The Journal of Pediatrics ]anuary 1971
group: the mean frontal QRS axis lay significantly more to the left; the ventricular activation time in V1 was less; the R wave was significantly taller in V6 and smaller in V4R and V~, while the S wave was smaller in both V~ and V6. In addition, the T wave was taller in V6 and the durations of the QRS and Q T intervals were lower. These findings may be partially explained on the basis of the difference in age between the two groups. ELECTROCARDIOGRAM POSTMATURE INFANTS
OF
A recent study of 40 postmature infants 29 described an elevated R / S ratio or a pure Rwave pattern in the right precordial leads. Thus, there was a tendency toward more right ventricular dominance than in mature newborn infants. Other statistically different observations in the postmature infants included a higher than normal amplitude of R in V4R (but not in V3R or V1) and an absent R wave or an R wave less than 1 mm. in height in lead I. HEMODYNAMIC CORRELATES IN THE NEWBORN
Emmanouilides and associates 1~ studied the pulmonary artery pressures and pulmonary-systemic pressure ratios and the persistence of a left-to-right shunt through the ductus arteriosus in 28 newborn infants, ages 1 to 27 hours; these observations were correlated with the ECG. They concluded that postnatal hemodynamic changes are reflected in the ECG of the normal newborn infant. Upright T waves in the right chest leads were associated with significantly higher pulmonary artery pressures than were found in patients with a negative T wave. The majority of infants with negative T waves in V~ were under 10 hours of age and had left-to-right shunts through the ductus arteriosus. An R / S ratio of less than 1 in the right precordial leads was observed only in infants with left-to-right shunts through the ductus arteriosus; an R / S ratio of more than 1 was associated with lower pulmonaryto-systemic pressure ratios. There was no
Volume 78
Number
1
correlation between the a m p l i t u d e R or S waves in the p r e c o r d i a l leads a n d the hemod y n a m i c p a r a m e t e r s investigated. E F F E C T OF E A R L Y C L A M P I N G VERSUS STRIPPING OF T H E C O R D
W a l s h ' s 12 recent study indicates t h a t newborn infants w i t h h y p e r v o l e m i a secondary to stripping of the umbilical cord at delivery have e l e c t r o c a r d i o g r a p h i c differences from infants whose cord is c l a m p e d early. T h e former infants have increased a m p l i t u d e a n d d u r a t i o n of the P wave, increased d u r a t i o n of the P R a n d Q T intervals, lower a m p l i t u d e of the R waves, lower R / S ratios in b o t h right- a n d left-sided chest leads, a n d delayed inversion of T waves in lead V1. These findings m a y be related to a delay in fall of the p u l m o n a r y artery pressure a n d closure of the ductus arteriosus. REFERENCES
1. Ziegler, R. F.: Electrocardiographic studies in normal infants and children, Springfield, Ill., 1951, Charles C Thomas, Publisher. 2. Namin, E. P.: Pediatric electrocardiography and vectorcardiography, in Gasul, B. M., Arcilla, R. A., and Lev, M., editors: Heart disease in children: Diagnosis and treatment, Philadelphia, 1966, J. B. Lippincott Company, pp. 69-120. 3. Namin, E. P., and Miller, R. A.: The normal electrocardiogram and vectorcardiogram in children, in CasseIs, D. E., and Ziegler, R. F., editors: Electrocardiography in infants and children, New York, 1966, Grune & Stratton, Inc., pp. 99-115. 4. Liebman, J.: The normal electrocardiogram in newborns and infants (a critical review), in Cassels, D. E., and Ziegler, R. F., editors: Electrocardiography in infants and children, New York, 1966, Grune & Stratton, Inc., pp. 79-98. 5. Liebman, J.: Electrocardiography, in Moss, A. J., and Adams, F. H., editors: Heart disease in infants, children, and adolescents, Baltimore, 1968, The Williams & Wilkins Company, pp. t83-231. 6. Butch, G. E., and DePasquale, N. P.: Electrocardiography in the diagnosis of congenital heart disease, New York, 1967, Lea & Febiger, Inc. 7. Massie, E., and Walsh, T. J.: Clinical vectorcardiography and electrocardiography, Chicago, 1960, Year Book Medical Publlshers, Inc. 8. Lamb, L. E.: Electrocardiography and vectorcardiography: Instrumentation, fundamentals,
Electrocardiogram in normal neonate
9.
10.
i1. 12.
13. 14. 15. 16.
17.
18. 19. 20. 2I.
22.
23. 24. 25.
26.
27.
15 5
and clinical applications, Philadelphia, 1965, W. B. Saunders Company. Walsh, S. Z.: Comparative study of electrocardiograms of healthy premature and fullterm infants of similar weight, Amer. Heart J. 68: 183, 1964. Costa, A. F., Faul, B. C., Ledbetter, M. K., and Oalmon, M. C.: The electrocardiogram of the premature infant, Amer. Heart J. 67: 4, 1964. Datey, K. K., and Bharucha, P. E.: Electrocardiographic changes in the first week of life, Brit. Heart J. 92:175, 1960. Walsh, S. Z.: Early clamping versus stripping of cord: Comparative study of electrocardiogram in neonatal period, Brit. Heart J. 31: 122, 1969. Stern, L., and Lind, J.: Neonatal T wave patterns, Acta Paediat. 49: 329, 1960. Walsh, S. Z.: The S-T segment and T wave during the first week of life, Brit. Heart J. 26: 679, 1964. Walsh, S. Z.: EIectroeardiographic intervals during the first week of life, Amer. Heart J. 66: 36, 1963. Sutin, G. J., and Schrire, V.: The electrocardiogram in the first two days of life. An interracial study, Amer. Heart J. 67: 749, 1964. Emmanouilides, G. C., Moss, A. J., and Adams, F. H.: The electrocardiogram in normal newborn infants: Correlation with hemodynamic observations, J. P~DIAT. 67: 578, 1965. Kessel, I.: The electrocardiogram on the first day of life, Brit. Heart J. 15: 430, 1953. Scott, O., and Franklin, D.: The electrocardiogram in the normal infant, Brit. Heart J. 25: 441, 1963. Walsh, S. Z.: P wave duration and P-R interval during first week of life, Brit. Heart J. 25: 42, 1963. Halt, G., and Gasul, B. M.: The evolution and significance of T wave changes in the normal newborn during first seven days of life, Amer. J. Cardiol. 12: 494, 1963. Tazawa, H., and Yoshimoto, C.: Electrocardiographic potential distributions in newhorn infants from 12 hours to 8 days after birth, Amer. Heart J. 78: 292, 1969. Michaelsson, M.: Electrocardiographic studies in the healthy newborn, Acta Paediat. 48: (Suppl. 117), 108, 1959. Levine, O. R., and Griffiths, S. P.: Electrocardiographic findings in healthy premature infants, Pediatrics 30: 361, 1962. Rothfeld, E. L., Wachtel, F. W., Karlen, W. S., and Bernstein, A. : The evolution of the vectorcardiogram and electrocardiogram of the normal infant. I. The normal newborn, Amer. J. Cardioh 5: 439, 1960. WachteI, F. W., RothfeId, E. L., Karlen, W. S., and Bernstein, A.: The evolution of the vectorcardiogram and electrocardiogram of the normal infant. II. Transition toward adult patterns, Amer. J. Cardiol. 5: 450, 1960. Walsh, S. Z.: Evolution of the electrocardio-
156
28. 29.
30.
31.
Hastreiter and AbeUa
gram of healthy premature infants during the first year of life, Acta Paediat. (Suppl.) 145: 1, 1963. Hubsher, J. A.: The electrocardiogram of the premature infant, Amer. Heart J. 61: 467, 1961. Ackerman, B. D., Sperling, D. R., and O'Loughlin, B. J.: Electrocardiographic observations in postmature infants, J. PED~AT. 76: 399, 1970. Namin, E. P., Arcilla, R. A., D'Cruz, I. A., and Gasul, B. M.: Evolution of the Frank vectoreardiogram in normal infants, Amer. J. Cardiol. 13: 757, 1964. DePasquale, N. P., and Burch, G. E.: A study of the ventrlcular gradient in normal infants and chiIdren, Amer. J. Cardiol. 25: 464, 1960.
The Journal of Pediatrics January 1971
32. Walsh, S. Z.: The electrocardiogram during the first week of life, Brit. Heart J. 25: 784, 1963. 33. DePasquale, N. P., and Burch, G. E.: The eleetrocardiogram, ventrlcular gradient and spatial veetorcardiogram during the first week of life, Amer. J. Cardiol. 12: 482, 1963. 34. Naeye, R. L.: Arterial changes during the perinatal period, Arch. Path. 71: 191, 1961. 35. Emery, J. L., and MacDonald, A. M.: The weight of the ventricles in the later weeks of intrauterine life, Brit. Heart J. 22: 563, 1960. 36. Alimurung, M. M., Joseph, L. G., Nadas, A. S., and Massell, B. F.: The unipolar precordial and extremity electrocardiogram in normal infants and children, Circulation 4: 420, 1951.
AND
NEONATAL
M E D I C I N E inch.rer. Behrman,Editor
The electrocardiogram in the newborn period I The normal infant Alois R. Hastreiter, M.D., * and Jose B. Abella, M.D. CHICAGO,
ILL.
I N T E g P R ] g T A T I O iN" o f the electrocardiogram (ECG) in the neonatal period is more difficult than at any other age because of the rapid perinatal hemodynamic changes and the wide overlap of normal and abnormal findings. Adequate analysis of the tracings requires a well-standardized recording technique (size and position of electrodes and calibration). Normal standards reported for this age group also vary because they are based on data obtained with different types of recorders (photographic, directwriter, and jet-writer)? "33 Information is particularly scarce for some of the leads frequently used in newborn infants and younger children (V4R, VaR, and VT). In addition, data are often grouped together over relatively wide periods of time (e.g., 0 to 24 hours, 2 to 7 days, or 8 to 30 days). Finally, in evaluating the ECG, there is no general agreement about how to take into consideration various age and growth factors (chronologic age, gestational age, weight, state of nutrition, and anemia) and perinatal factors that affect the circulation (placental transfusion, persistent arteriovenous shunt through the ductus arterious, and hypoxia).
From the University of Illinois Hospital. Supported in part by the University o[ Illinois Foundation, Goodenberger Medical Research, No. 2-44-33-66-3-14. ~Repr~nt address: Department o~ Pedhztrles, University o] Illinois Hospital, 840 S. Wood St., Chicago, Ill. 60612.
Vol. 78, No. I, pp. 146-I56
The purpose of this review is threefold: (1) to describe the normal ECG of the newborn infant and its evolution during the neonatal period (Tables I to V), (2) to correlate the electrocardiographic changes with the perinatal physiologic events, and (3) to review the electrocardiographic abnormalities in this age group (Part I I ) . The normal electrocardiographic characteristics of premature and postmature newborn infants are also briefly described. VECTORCARDIOGRAPHIC APPROACH TO THE SCALAR ELECTROCARDIOGRAM During depolarization and repolarization of a single myocardial cell, the electrical forces produced at any given instant can be represented by a single equivalent dipole or mean vector which expresses the total effect of all elementary dipole forces. According to the "equivalent dipole" concept of electrocardiography, the electrical activity of the heart, as manifested at the body surface, can also be represented at any given instant by a single equivalent dipole or its corresponding mean vector. The process of depolarization and repolarization is much more complex in the heart muscle than in the single muscle cell; e.g., atrial excitation spreads radially throug the atria at a uniform speed, and the Purkinje system provides the
Volume 78 Number 1
ventricles with a specialized conduction path. However, ventricular depolarization and repolarization may be simplified by visualizing a segment of ventricular wall as if it consisted of a single muscle fiber extended from endocardium to epicardium; the resulting electrical forces produced by activation of the ventricular wall are directed outward, perpendicular to the epicardial surface. The electrical forces produced during activation of different portions of the heart follow a certain course in time and vary widely in direction, electrical sense, and magnitude. The balance between opposing forces determines the electrical field of the heart at a given instant (at the body surface) and can be visualized as a single equivalent dipole or mean instantaneous spatial vector. The purpose of the ECG (and vectorcardiogram) is to provide information concerning the orientation and magnitude of the instantaneous cardiac spatial vectors. The changing projections of these vectors on a given plane plotted against time results in a "vector loop"; recording these vectors on a given lead axis produces the familiar P, QRS, and T deflections, which reflect the sequence of atrial depolarization and ventricular depolarization and repolarization. Rather than just analyzing the various configurations of conventional scalar ECG patterns as such, one should view them as sequential projections of the spatial vector; the latter is much easier to describe and memorize. An approximate reconstruction of the sequential changes of the spatial vector projected on a plane ("vector loop") can be made from analysis of 2 scalar leads in the same plane (preferably perpendicular). Thus, the events projected on the frontal plane can be reconstructed by a combination of standard leads I and aVF and events in the horizontal plane by precordial leads V2 and V6. The events in space can be reconstructed by a synthesis of the two planes. The cardiac spatial vector is equal to the vectorial sum of its projection on the transverse (x axis, leads I or V6), vertical (y axis, lead aVF), and sagittal axis
Electrocardiogram in normal neonate
14 7
(z axis, lead V2). This subject is reviewed in detail elsewhere. 2, 5, 7, s CIRCULATORY ADAPTATIONS IN THE NEWBORN PERIOD
The thickness of the ventricular and atrial walls and the size of these chambers are determined by the work that they do in carrying a volume of blood and overcoming the resistance to ejection of this blood. The right and left ventricles have the same pressure in utero, but the resistance offered by the semicollapsed lungs to pulmonary blood flow is higher than the systemic resistance (right ventricular "pressure work" is greater). Before birth the low-resistance placenta (which receives about 55 per cent of the combined ventricular output) is part of the systemic circulation, the systemic small muscular arteries have less muscle mass than the pulmonary arteries, 3~ the left ventricle is smaller than the right, as and there is a large blood flow from pulmonary artery to aorta through the ductus arteriosus. Pulmonary vasoconstriction is also an important contributing factor in elevating the pulmonary vascular resistance. At birth, removal of the placenta results in a marked increase of the systemic vascular resistance; the first breath causes a decrease in pulmonary vasoconstriction and a drop of the pulmonary vascular resistance. Therefore, shortly after birth systemic and pulmonary resistances are similar. The pulmonary vascular resistance continues to fall, and within a few hours after birth the flow through the ductus arteriosus reverses and then disappears. There is also a large increase in pulmonary venous return to the left atrium and ventricle. By the end of the first day of life the pulmonary artery pressure is reduced to about one half that of the systemic, and by 2 weeks of age it is close to that of adults. Pulmonary vasoconstriction may be increased by hypoxemia and acidemia, which are more frequent in low-birth-weight and immature infants. The arteriovenous shunt through the ductus arteriosus also may be larger and persist longer in this group. The amount of placental transfusion at birth which is
14 8
Hastreiter and Abella
The Journal of Pediatrics January 1971
T a b l e I. H e a r t r a t e , P R i n t e r v a l , P - w a v e d u r a t i o n , Q R S a m p l i t u d e i n l e a d I I of m a t u r e n e w b o r n i n f a n t s ~
Age
t Minimum Heart rate
0 - 24 hr. 1- 7 days 8 - 30 days
[
5%
I
Mean
94 100 115
85 100 115
duration, and P-wave
[
95%
119 133 163
I Maximum
145 175 190
[
I45 175 190
s.D. 16.1 22.3 19.9
PR interval 0 - 24 hr. 1- 7 days 8 - 30 days
0.07 0.05 0.07
0.07 0.07 0.07
0.10 0.09 0.09
0.12 0.12 0.11
0.13 0.13 0.13
0.012 0.014 0.010
0.040 0.038 0.040
0.051 0.046 0.048
0.065 0.061 0.057
0.075 0.065 0.065
0.066 0.066 0.064
0.05 0.04 0.04
0.065 0.056 0.057
0.084 0.079 0.073
0.09 0.08 0.08
0.010 0.010 0.009
1.5 1.6 1.6
2.3 2.5 2.4
2.6 2.8 2.7
0.50 0.51 0.48
P-wave duration 0 - 24 hr. 1- 7 days 8 - 30 days
0.040 0.035 0.040
QRS duration 0 - 24 hr. 1- 7 days 8 - 30 days
0.05 0.04 0.04
P-wave amplitude in I f 0 - 24 hr. 1 - 7 days 8 - 30 days
0 0.5 0.5
0.8 0.8 0.8
~Data from Ziegler 1 (photographic records), fifth and nlnety-fifth percentiles recalculated by Liebman. ~
T a b l e I I . M e a n f r o n t a l , Q R S , a n d T axes i n m a t u r e n e w b o r n i n f a n t s ~
Q RS axis (frontal plane)
T axis (frontal plane)
Minimum
5%
Mean
95%
mum
Minimum
0 - 2 4 hr.
60
60
135
180
180
-20
I-
7 days
60
80
125
160
180
-40
8 - 3 0 days
0
60
110
160
180
-20
0
Age
Maxi-
Mean
95%
Maximum
0
70
140
180
-40
25
80
100
35
60
120
5%
eData from Liebman. ~
T a b l e I I I . A m p l i t u d e s of R a n d S w a v e s i n p r e c o r d i a l l e a d s ~
S wave
R wal)e
Age
Minimum
5%
Mean
95%
30 hr. 1 too.
3.5 3.0
4.0 3.3
8.6 6.3
14.2 8.5
30 hr. 1 too.
5.0 4.0
4.3 3.3
11.9 11.1
21.0 18.7
30 hr. 1 mo.
2.0 3.8
3.I 3.8
9.4 15.0
16.6 24.2
30 hr. 1 too.
1.5 1.0
1.5 1.0
5.4 10.8
tl.3 16.2
MiniMaximum mum Amplitudes in V~R 15.0 12.0
0.0 0.0
Maxi-
5%
Mean
95%
0.2 0.8
3.8 1.8
13.0 4.6
12.0 9.0
1.1 0.0
9.7 6.1
19.1 15.0
26.0 15.0
2.4 2.8
9.5 8.3
18.5 16.3
22.0 30.0
1.0 0.0
5.6 4.8
13.8 9.5
20.0 18.0
mum
Amplitudes in V1 30.0 20.0
0.0 0.0
Amplitudes in Vs 20.0 30.0
0.5 0.0
Amplitudes in Vs 15.0 22.0
0.2 0.0
~Data from Namin ~, a (direct writer), fifth and ninety-fifth percentiles recalculated by L i e b m a n )
Volume 78 Number 1
Electrocardiogram in normal neonate
149
T a b l e I V . A m p l i t u d e s of R a n d S w a v e s i n p r e c o r d i a l l e a d s ~ R 733aue
Age
Minimum
5%
S waue
Mean
95%
Maximum
Minimum
S.D.
5%
Mean
95%
Maximum
S.D.
0-24 hr. 1- 7 days 8-30 days
5.5 5.5 2.5
7.0 9.0 4.2
14.8 18.2 11.4
20.0 27.4 19.8
20.5 29.5 26.5
Amplitudes in V1 3.75 0 5.44 1.5 4.97 0
2.5 4.6 2.5
9.3 10.4 5.0
27.0 18.8 12.8
28.5 25.5 18.5
7.99 4.70 3.73
0-24 hr. 1- 7 days 8-30 days
11.5 8.5 5.5
13.0 11.7 6.8
20.1 19.9 17.5
28.1 31.1 29.0
29.5 32.5 32.5
Amplitudes in V~ 3.81 5.0 5.89 5.0 6.48 1.0
9.0 9.3 4.2
20.3 20.2 14.0
33.8 34.1 25.7
37.0 37.0 29.0
6.73 7.26 6.24
0-24 hr. 1- 7 days 8-30 days
12.0 4.0 0.0
12.7 8.8 8.3
18.8 18.1 18.8
26.7 30.0 33.8
28.0 40.0 36.0
Amplitudes in V~ 4.12 10.0 12.0 6.55 0 2.6 7.50 2.0 4.2
25.0 17.1 12.4
32.0 33.0 20.0
38.0 38.0 26.0
6.05 8.37 5.47
0-24 hr. 1- 7 days 8-30 days
8.0 4.0 4.0
9.0 4.9 3.3
17.4 18.8 15.9
26.0 33.1 33.3
32.0 36.0 36.0
Amplitudes in V~ 5.97 2 7.24 0 7.82 0
4.0 3.4 3.1
21.8 13.2 6.8
36.0 27.7 16.3
42.0 30.0 18.0
9.08 8.11 5.05
0-24 hr. 1- 7 days 8-30 days
0.0 0.0 0.0
4.0 3.4 3.5
10.2 10.7 11.9
18.0 19.3 27.0
24.0 28.0 36.0
Amplitudes in V5 5.44 0 5.54 0 7.28 0
0.0 3.6 2.7
11.9 6.8 4.8
24.0 16.2 12.3
31.5 19.5 13.5
6.87 4.73 3.50
0-24 hr. 1- 7 days 8-30 days
0 0 0
2.3 2.2 1.7
3.3 5.1 6.7
7.0 13.1 20.5
7.5 16.5 25.5
Amplitudes in V~ 2.10 0 3.97 0 4.82 0
1.6 0.8 0.6
4.5 3.3 2.0
10.3 9.9 9.0
14.0 14.0 10.0
2.78 2.99 2.46
0-24 hr. 1- 7 days 8-30 days
-0 0
. 0.5 1.0
.
. 7.5 6.5
Amplitudes in A V R . . . . 1.80 3.0 3.7 1.39 5.0 5.6
. 7.9 10.1
. 13.9 14.6
15.0 15.0
3.11 2.81
0-24 hr. 1- 7 days 8-30 days
-0 0
. 0.5 1.2
.
. 6.5 7.5
Amplitudes in A V L . . . . 1.04 0 1.4 1.48 0 2.2
. 5.2 5.3
. 9.7 8.9
13.0 13.0
2.48 2.10
0-24 hr. 1- 7 days 8-30 days
-1.0 1.0
. 1.9 1.4
.
. 13.0 15.0
Amplitudes in A V F . . . . 2.43 0 0.6 3.39 0 0.6
. 0.7 0.6
. 3.1 3.8
3.5 5.5
1.10 1.20
. 2.8 2.0
. 6.4 4.0
. 1.7 2.2
. 3.3 5.8
. 5.4 6.1
. 10.5 12.4
"~Data from Zieglerx (photographic records), fifth and ninety-fifth percentiles recalculated by Liebman.5
T a b l e V . A m p l i t u d e o f T w a v e s i n p r e c o r d i a l l e a d s V~ to V6 ~ V~
Age 0-24 hr. 1- 7 days 8-30 days
Vs
Mean
95%
Maximum
.4.3 4.4 5.3
72 7.7 8.1
8.5 8.5 8.5
"~Data from Liebman.5
S.D.
Mean
95%
0.95 1.39 1.49
3.3 4.9 5.3
6.8 7.3 7.5
V,
Maximum
S.D.
Mean
95%
mum
S.D.
7.5 7.5 10.5
1.62 1.44 1.50
2.4 2.9 3.5
3.9 4.2 5.3
4.5 4.5 7.5
0.63 0.67 1.01
maxi-
150
Hastreiter and Abella
related to early or Iate clamping of the umbilical cord (with or without stripping) may affect the blood volume, cardiac output, and the pressures in the cardiac chambers for several hours or days after birth. The higher cardiac output associated with anemia in the premature infant probably adds to the work of both ventricles. The changes in right and left ventricular weights occurring perinatally are as follows 3s : At 30 weeks' gestation the left ventricle is thicker than the right (average weight ratio 1.15:1), at 32 to 35 weeks' they are equal, and at about 36 weeks' the average newborn value of 1.3:1 (favoring the right ventricle) is attained. Following birth, the left ventricular wall rapidly increases in thickness. At one month the left ventricle is heavier than the right, and by 6 months the ratio is about 2:1 in favor of the left ventricle. The adult ratio is 2.5:1. ELECTROCARDIOGRAPHIC VECTORS IN THE NEWBORN INFANT
QRS vector. The newborn infant's right ventricular dominance is well known, but the degree of dominance is variable, resulting in a wide spread of normal values. The mean spatial QRS vector during the first 2 weeks of llfe is oriented to the right, anteriorly and inferiorly. It gradually rotates leftward and inferiorly; at the end of the first month it points predominantly inferlorly, anteriorly, and slightly to the right. In the adult it is oriented inferiorly, posterio'rly, and to the left and has a considerably greater magnitude. Thus, the newborn infant's ECG exhibits prominent and prolonged anterior forces resulting in a tall and broad R wave in the right chest leads and often a deep S wave in the left chest leads. The leftward vector in the newborn infant is small; consequently the R wave in the left precordium has low amplitude initially but increases rapidly in the first few months. The posterior vector, although variable, is frequently small in the newborn period and appears late. Thus, the S wave in leads V1 and V2 is small. By 2 years of age the posterior vector predominates.
The ]ournal o[ Pediatrics ]anuar7 1971
The init{al or septal vector may be to the left in the newborn period (less so in the premature infant). Rarely this may result in a qR complex in lead V~R or even in V1 and absent or small Q waves in the left chest leads. With aging, the initial vector extends further to the right, and the Q wave increases in the left precordium. The initial vector can be very superior in infancy and childhood, causing a prominent Q wave in lead aVF which gradually decreases throughout childhood. The terminal rightward force is prominent in the newborn infant and gradually decreases over months to years. This explains the deep S wave in the left chest leads, which decreases with age. The terminal vector tends to become more superior and is important in evaluating left-axis deviation. The newborn infant's ECG almost invariably demonstrates clockwise rotation in the frontal plane and usually (but less often) also in the horizontal plane. The horizontal plane changes rapidly; if this vector is not counterclockwise by 3 months of age, right ventricular hypertrophy can usually be diagnosed. The frontal plane only gradually changes its inscription with aging so that in older childhood the vector loop usually can be inscribed in either direction. The clockwise or counterclockwise direction of depolarization is reflected in the scalar leads by the ventricular activation time (time from the onset of the QRS complex to the peak of the R wave); a ventricular activation time shorter in lead V6 than in lead V2 indicates clockwise rotation and the opposite pattern counterclockwise rotation. The QRS patterns in the chest leads were classified by Alimurung and associates 36 into: (1) adult R / S progression--the S wave has higher amplitude than the R wave in the right chest leads and smaller than the R wave in the left chest leads, (2) partial reversal of the R / S progression--the R-wave amplitude is higher than that of the S wave in both right and left chest leads, and (3) complete reversal of R / S progression--the R wave is larger than the S wave in the right and smaller than the S wave in the left chest leads. The newborn infant has
Volume 78 Number 1
Electrocardiogram in normal neonate
either complete (50 per cent) or partial reversal (50 per cent) but no adult progression (with rare exceptions) of the R / S ratio. By one month of age complete reversal disappears and adult R / S progression is common. A pure R wave in lead V1 is rare and a qR wave only exceptionally seen in newborn infants. T vector. Dramatic changes occur in the T vector following birth. Within the first 5 minutes following birth this vector is oriented to the left, anteriorly and minimally inferiorly; by 1 to 6 hours it has shifted much more inferiorly and to the right. Over the next several days the vector rotates markedly to the left and eventually becomes oriented to the left and posteriorly. In our own series, during the first 24 hours the T vector was still oriented to the left, anteriorly and inferiorly; at 2 to 7 days it was oriented to the left, posteriorly and inferiorly. These changes of the T vector explain the upright T wave in lead V1 and the negative or flat T wave in lead V6 in the early neonatal period.
statistical difference in their heart rates2 PR interval. T h e average 'PR interval at birth is 0.096 seconds; it increases to 0.100 after several minutes to hours and then declines to a low of 0.095 seconds at approximately 1 to 3 weeks of age. 1~ It gradually increases to reach 0.110 seconds at the end of the first year and 0.150 seconds in adult life. Hypervolemia secondary to delayed clamping a n d / o r vigorous stripping of the umbilical cord appears to lengthen the PR interval (average 0.124 seconds at birth)a2; this interval declines at 4 to 5 days of age to reach a level comparable to that of infants with early clamping of the cord. There is no statistically significant difference between the duration of the PR interval in premature and in full-term infants, a~ 2~ Duration o[ the P wave. Walsh 12 observed a duration of 0.060 seconds at birth in infants with early clamped cords versus 0.082 in those with stripped cords. Following birth it declines to a low value of about 0.050 which is maintained during the first month of life. PR segment. The average value of the PR segment is relatively constant throughout childhood, ranging from 0.050 to 0.065 seconds. According to Burch and DePasquale, ~ it averages 0.054 seconds in the first week of life and reaches the lowest value of 0.044 seconds at 3 to 6 months of life. Q R S interval. The duration of the QRS complex increases gradually throughout childhood. At birth it averages 0.065 seconds; it falls to about 0.055 seconds at the end of the first week and gradually increases to reach 0 . 0 6 8 seconds at 12 months; the adult value is 0.080. Ventricular activation time. At birth ventricular activation time in lead Va averages 0.018; it falls to 0.016 at 3 to 5 days of age and climbs to a maximum of 0.024 at 3 to 6 months. The adult level, averaging 0.020 seconds in lead V1, is reached at the end of the first year. During the first day of life, the average value is 0.019 in lead V6; at one month of age it is 0.023 and at one year 0.031 (Ziegler, 1 photographic method). Burch and De-
THE NORMAL SCALAR ELECTROCARDIOGRAM A N D ITS E V O L U T I O N IN THE NEWBORN PERIOD
T h e study of the normal electrocardiogram of the newborn infant will be divided into: (1) the time relationships or intervals, (2) the axes, and (3) the amplitudes in the various leads. Pursuing a vectorial approach for analysis of the ECG, these parameters will be studied in the frontal plane (standard leads) and in the horizontal projection (precordial leads). Intervals (Table I). Heart rate. At birth the average heart rate is 140 beats per minute. It drops to slightly less than 120 during the first several hours and then rises gradually to attain a maximum average rate of 160 at 1 to 3 months of age? 5 Premature infants have a slightly higher heart rate than full-term infants for the corresponding postnatal agel~ when premature and full-term infants of similar weight but different postnatal ages are compared, there is no
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Pasquale, 6 using the direct writing method, obtained slightly higher values for the ventricular activation time in lead V1 and lower values in lead V6. The ventricular activation time in lead V~ is lower in premature infants than in full-tei~l infants of comparable age. The same occurs when premature infants who have attained full-term size are compared to mature infants of similar weight2 There is controversy in the literature concerning the importance of the ventricular activation time. ~ QT interval. At birth the Q T interval is relatively long (0.296 seconds); the lowest value is reached at about 3 weeks (0.240 seconds). It then increases to a value of 0.260 to 0.270 seconds at one year and 0.370 in early adulthood. The corrected Q T interval or QT index (QTe) remains remarkably constant throughout childhood; the average value is 0.400 seconds. However, significant changes occur during the neonatal p eriod15: The average value at birth is 0.400 seconds; it then rises to a peak of 0.420 during the first 24 hours and declines rapidly to about 0.405 to 0.410 at the end of the second day and to 0.385 at one month (lowest value). The stable adult value is reached at the end of the second month. Walsh a~- describes a higher value of the QTe for infants with late clamping or stripping of the cord--0.440, compared to those with early clamped cord, 0.405. There is considerable disagreement in the literature as to the value of the QTo measurement. Axes (Table II). These will be described in the frontal and horizontal planes. P-wave axis (frontal). It averages +60 degrees at birth and declines to +54 degrees toward the end of the first month. In later childhood and adulthood it remains relatively constant at about +50 degrees. P-wave axis (horizontal). The P wave remains stationary at +50 degrees throughout the first month? ~ The average adult level is +5 degrees. QRS axis (frontal). The mean frontal QRS axis remains relatively constant throughout childhood and adulthood (average value +60 degrees), with the excep-
The ]ournal o[ Pediatrics January 1971
tion of the first 6 months of life. The average value during the first day of life is about +I35 degrees, at 1 week 130 degrees, at 3 weeks 105 degrees, at 5 weeks 90 degrees, and at the end of the second month 75 degrees. In premature infants the mean frontal QRS axis has a significantly lower value than in full-term infants up until the end of the second week? ~ The initial frontal QRS vector is approximately 0 degrees at birth and becomes gradually more superiorly oriented reaching -20 degrees at the end of the first month. The final frontal QRS vector is +170 degrees on the first day of life and subsequently remains relatively stationary throughout the first month of life, average value +165 degrees? ~ QRS axis (horizontal). This mean QRS axis has an average value of +130 during the first day of life, decreases gradually to about 110 degrees at the end of the first week, and remains stationary throughout the first month. It then gradually decreases with age toward normal adult value of -10 degrees. The initial and final QRS vectors in the horizontal plane maintain a relatively constant value of +70 degrees and +245 degrees throughout the first month of life? ~ The corresponding adult values are +50 degrees and -80 degrees. T-wave axis (fro.ntal). Marked changes of this axis occur during the newborn period. According to Hair and Gasu121 the frontal T-wave axis is +7 degrees from 1 to 5 minutes after birth, then shifts to +115 degrees at 2 to 4 hours after birth; this is followed by a gradual return to approximately the previous level (+10 degrees) during the ensuing 2 to 7 days. From the first week to the beginning of the third month of life the frontal T-wave axis gradually increases to reach a maximum of +60 degrees. T-wave axis (horizontal). This axis shifts from +67 degrees immediately after birth to +130 in the following 2 to 6 hours and then rotates back to about -10 degrees at 3 days and -28 degrees at 7 days of age. The axis remains at this level throughout the first month.
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Electrocardiogram in normal neonate
Amplitudes. Changes in amplitude of various ECG parameters with age in the newborn period are shown in Tables III to V. A brief description of this evolution follows. P-wave amplitude (frontal). The evolution of the P wave is best studied in lead II '~, lz: From birth it decreases to a low point at about 2 days of age and later gradually rises. P-wave amplitude (horizontal). In lead V~ the P wave rises slightly during the first few weeks or months; it then declines gradually and starts rising again at several months of age and finally stabilizes at about 4 years. In lead V6 the P wave remains relatively stable throughout childhood. Q-wave amplitude (frontal). The most interesting feature in the newborn period is perhaps the definite increase in depth of the Q wave in all leads (except aVL) following birth. It reaches a maximal depth at several months of age and then gradually declines in amplitude. Q-wave amplitude (horizontal). In the newborn infant a Q wave is only exceptionally present in leads V4R to V2; the incidence is higher the further the lead is to the left of the precordium. This incidence of Q wave is lower at birth than in the subsequent days and weeks. The incidence expressed in per cent is as follows:
Following birth there is an initial decline in the amplitude of the R wave in most precordial leads with a slow subsequent rise to adult levels; in the right chest leads VaR to V1 the reduction continues until adulthood. The S wave increases in depth following birth in all precordial leads except VsR. and V4R. A maximal depth is reached at about the second day and is followed by a gradual rise over the remaining 1 to 2 months. Lead V4R has a relatively constant amplitude throughout this period. These changes result in the relatively constant magnitude of R + S but a more prominent negative component (deeper S wave) hnmediately following birth.
I Birth Adult
v: 0 0-5
I
I 8 40
v: 60 80-90
I
v= 73 90-100
R- and S-wave amplitudes (frontal) (Table IV). After birth there is a reduction in the amplitude of the R wave in all standard leads. This is followed by a gradual rise over the next few months except in lead aVR, which remains stationary. There is also an initial decrease in the amplitude of the S wave during the first 1 or 2 months in all standard leads. As a consequence the magnitude of R + S is much smaller at birth than in the subsequent months.
R- and S-wave amplitudes (horizontal).
15 3
T-wave amplitude (frontal) (Table V). The amplitude of the T wave in the standard leads tends to change considerably during the first month of life and then remains at a relatively stable level. T-wave amplitude (horizontal). In the horizontal plane the incidence of a positive T wave in the right precordium and a negative or flat T wave in the left precordium are important because of the marked changes involving the T vector in tile early days after birth. At birth the incidence of upright T waves in lead V1 is about 70 per cent. There is a gradual decline over the next several days, so that by the fifth day the average incidence reaches 0. At the time of birth over 60 per cent of the T waves in lead V6 are upright; this declines to less than 10 per cent during the first day with a rise to about 50 per cent by the end of the first day to 100 per cent by the fourth day. This same phenomenon is reflected in the amplitude of the T wave in leads V1 and V6. ELECTROCARDIOGRAM PREMATURE INFANTS
OF
In premature infants the right ventricle to left ventricle weight ratio and the muscle mass of the small muscular arteries in the lungs is less than in full-term infants. There is, therefore, less right ventricular dominance in premature infants. The question of whether or not the premature infant's ECG presents characteristic
1 54
Hastreiter and AbeIla
features different from those of mature newborn infants is not answered despite a number of comprehensive studies. 4, 9, ~0, 24, 27 In part this is because the premature newborn infant's ECG shows even more variability than that of the full-term infant. However, some differences do exist and these are particularly apparent in the first week of life. The most striking features are as follows: (1) There is generally lower voltage of the R, S, and T wave, particularly in the standard limb leads. This is best appreciated in the first week of life. Despite the lower voltage, the R / S ratio is generally higher in both the right and left chest leads. The P-wave amplitude may also be lower than in full-term newborn infants but occasional premature babies may have tall and peaked P waves. (2) There is less right ventricular dominance in the tracings from premature infant than from mature newborn infants. This observation is more striking in the Frank vectorcardiogram than in the conventional scalar ECG4; it shouts a more rapid evolution toward left ventricular dominance, e.g., counterclockwise rotation in the horizontal plane occurs early, between 24 and 72 hours of age? In the conventional electrocardiogram, this is manifested by fewer upright T waves in lead V~ than in full-term newborn infants (there is also a significant difference in this regard between smaller and larger premature newborn infants), a higher incidence of deep Q waves in lead V~, and the mean QRS and T vectors may be more leftward in the frontal plane. (3) A longer Q T interval has been described in premature infants than in full-term infants, although Walsh describes a shortened, scooped-out ST segment. (4) ST deviations are more common in premature infants; they usually consist of ST depression in the right chest leads. This distinction between premature and full-term infants may not be significant. A study comparing premature and mature infants of similar weight 9 (average ages 1.5 to 3 months and 5.5 days, respectively) also revealed a tendency toward relative left ventricular dominance for the premature
The Journal of Pediatrics ]anuary 1971
group: the mean frontal QRS axis lay significantly more to the left; the ventricular activation time in V1 was less; the R wave was significantly taller in V6 and smaller in V4R and V~, while the S wave was smaller in both V~ and V6. In addition, the T wave was taller in V6 and the durations of the QRS and Q T intervals were lower. These findings may be partially explained on the basis of the difference in age between the two groups. ELECTROCARDIOGRAM POSTMATURE INFANTS
OF
A recent study of 40 postmature infants 29 described an elevated R / S ratio or a pure Rwave pattern in the right precordial leads. Thus, there was a tendency toward more right ventricular dominance than in mature newborn infants. Other statistically different observations in the postmature infants included a higher than normal amplitude of R in V4R (but not in V3R or V1) and an absent R wave or an R wave less than 1 mm. in height in lead I. HEMODYNAMIC CORRELATES IN THE NEWBORN
Emmanouilides and associates 1~ studied the pulmonary artery pressures and pulmonary-systemic pressure ratios and the persistence of a left-to-right shunt through the ductus arteriosus in 28 newborn infants, ages 1 to 27 hours; these observations were correlated with the ECG. They concluded that postnatal hemodynamic changes are reflected in the ECG of the normal newborn infant. Upright T waves in the right chest leads were associated with significantly higher pulmonary artery pressures than were found in patients with a negative T wave. The majority of infants with negative T waves in V~ were under 10 hours of age and had left-to-right shunts through the ductus arteriosus. An R / S ratio of less than 1 in the right precordial leads was observed only in infants with left-to-right shunts through the ductus arteriosus; an R / S ratio of more than 1 was associated with lower pulmonaryto-systemic pressure ratios. There was no
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correlation between the a m p l i t u d e R or S waves in the p r e c o r d i a l leads a n d the hemod y n a m i c p a r a m e t e r s investigated. E F F E C T OF E A R L Y C L A M P I N G VERSUS STRIPPING OF T H E C O R D
W a l s h ' s 12 recent study indicates t h a t newborn infants w i t h h y p e r v o l e m i a secondary to stripping of the umbilical cord at delivery have e l e c t r o c a r d i o g r a p h i c differences from infants whose cord is c l a m p e d early. T h e former infants have increased a m p l i t u d e a n d d u r a t i o n of the P wave, increased d u r a t i o n of the P R a n d Q T intervals, lower a m p l i t u d e of the R waves, lower R / S ratios in b o t h right- a n d left-sided chest leads, a n d delayed inversion of T waves in lead V1. These findings m a y be related to a delay in fall of the p u l m o n a r y artery pressure a n d closure of the ductus arteriosus. REFERENCES
1. Ziegler, R. F.: Electrocardiographic studies in normal infants and children, Springfield, Ill., 1951, Charles C Thomas, Publisher. 2. Namin, E. P.: Pediatric electrocardiography and vectorcardiography, in Gasul, B. M., Arcilla, R. A., and Lev, M., editors: Heart disease in children: Diagnosis and treatment, Philadelphia, 1966, J. B. Lippincott Company, pp. 69-120. 3. Namin, E. P., and Miller, R. A.: The normal electrocardiogram and vectorcardiogram in children, in CasseIs, D. E., and Ziegler, R. F., editors: Electrocardiography in infants and children, New York, 1966, Grune & Stratton, Inc., pp. 99-115. 4. Liebman, J.: The normal electrocardiogram in newborns and infants (a critical review), in Cassels, D. E., and Ziegler, R. F., editors: Electrocardiography in infants and children, New York, 1966, Grune & Stratton, Inc., pp. 79-98. 5. Liebman, J.: Electrocardiography, in Moss, A. J., and Adams, F. H., editors: Heart disease in infants, children, and adolescents, Baltimore, 1968, The Williams & Wilkins Company, pp. t83-231. 6. Butch, G. E., and DePasquale, N. P.: Electrocardiography in the diagnosis of congenital heart disease, New York, 1967, Lea & Febiger, Inc. 7. Massie, E., and Walsh, T. J.: Clinical vectorcardiography and electrocardiography, Chicago, 1960, Year Book Medical Publlshers, Inc. 8. Lamb, L. E.: Electrocardiography and vectorcardiography: Instrumentation, fundamentals,
Electrocardiogram in normal neonate
9.
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and clinical applications, Philadelphia, 1965, W. B. Saunders Company. Walsh, S. Z.: Comparative study of electrocardiograms of healthy premature and fullterm infants of similar weight, Amer. Heart J. 68: 183, 1964. Costa, A. F., Faul, B. C., Ledbetter, M. K., and Oalmon, M. C.: The electrocardiogram of the premature infant, Amer. Heart J. 67: 4, 1964. Datey, K. K., and Bharucha, P. E.: Electrocardiographic changes in the first week of life, Brit. Heart J. 92:175, 1960. Walsh, S. Z.: Early clamping versus stripping of cord: Comparative study of electrocardiogram in neonatal period, Brit. Heart J. 31: 122, 1969. Stern, L., and Lind, J.: Neonatal T wave patterns, Acta Paediat. 49: 329, 1960. Walsh, S. Z.: The S-T segment and T wave during the first week of life, Brit. Heart J. 26: 679, 1964. Walsh, S. Z.: EIectroeardiographic intervals during the first week of life, Amer. Heart J. 66: 36, 1963. Sutin, G. J., and Schrire, V.: The electrocardiogram in the first two days of life. An interracial study, Amer. Heart J. 67: 749, 1964. Emmanouilides, G. C., Moss, A. J., and Adams, F. H.: The electrocardiogram in normal newborn infants: Correlation with hemodynamic observations, J. P~DIAT. 67: 578, 1965. Kessel, I.: The electrocardiogram on the first day of life, Brit. Heart J. 15: 430, 1953. Scott, O., and Franklin, D.: The electrocardiogram in the normal infant, Brit. Heart J. 25: 441, 1963. Walsh, S. Z.: P wave duration and P-R interval during first week of life, Brit. Heart J. 25: 42, 1963. Halt, G., and Gasul, B. M.: The evolution and significance of T wave changes in the normal newborn during first seven days of life, Amer. J. Cardiol. 12: 494, 1963. Tazawa, H., and Yoshimoto, C.: Electrocardiographic potential distributions in newhorn infants from 12 hours to 8 days after birth, Amer. Heart J. 78: 292, 1969. Michaelsson, M.: Electrocardiographic studies in the healthy newborn, Acta Paediat. 48: (Suppl. 117), 108, 1959. Levine, O. R., and Griffiths, S. P.: Electrocardiographic findings in healthy premature infants, Pediatrics 30: 361, 1962. Rothfeld, E. L., Wachtel, F. W., Karlen, W. S., and Bernstein, A. : The evolution of the vectorcardiogram and electrocardiogram of the normal infant. I. The normal newborn, Amer. J. Cardioh 5: 439, 1960. WachteI, F. W., RothfeId, E. L., Karlen, W. S., and Bernstein, A.: The evolution of the vectorcardiogram and electrocardiogram of the normal infant. II. Transition toward adult patterns, Amer. J. Cardiol. 5: 450, 1960. Walsh, S. Z.: Evolution of the electrocardio-
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gram of healthy premature infants during the first year of life, Acta Paediat. (Suppl.) 145: 1, 1963. Hubsher, J. A.: The electrocardiogram of the premature infant, Amer. Heart J. 61: 467, 1961. Ackerman, B. D., Sperling, D. R., and O'Loughlin, B. J.: Electrocardiographic observations in postmature infants, J. PED~AT. 76: 399, 1970. Namin, E. P., Arcilla, R. A., D'Cruz, I. A., and Gasul, B. M.: Evolution of the Frank vectoreardiogram in normal infants, Amer. J. Cardiol. 13: 757, 1964. DePasquale, N. P., and Burch, G. E.: A study of the ventrlcular gradient in normal infants and chiIdren, Amer. J. Cardiol. 25: 464, 1960.
The Journal of Pediatrics January 1971
32. Walsh, S. Z.: The electrocardiogram during the first week of life, Brit. Heart J. 25: 784, 1963. 33. DePasquale, N. P., and Burch, G. E.: The eleetrocardiogram, ventrlcular gradient and spatial veetorcardiogram during the first week of life, Amer. J. Cardiol. 12: 482, 1963. 34. Naeye, R. L.: Arterial changes during the perinatal period, Arch. Path. 71: 191, 1961. 35. Emery, J. L., and MacDonald, A. M.: The weight of the ventricles in the later weeks of intrauterine life, Brit. Heart J. 22: 563, 1960. 36. Alimurung, M. M., Joseph, L. G., Nadas, A. S., and Massell, B. F.: The unipolar precordial and extremity electrocardiogram in normal infants and children, Circulation 4: 420, 1951.