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The influence of scalp sampling on the cesarean section rate for fetal distress
FETUS,PLACENTA, ANDNEWBORN
The influence bf scalp sampling on the cesarean section rate for fetal distress RICHARD EDWARD Los Angeles,
W.
ZALAR,
JR.,
J. QUILLIGAN,
M.D.
M.D.
Calz;fornia
One%y&r’s obstetric experience at Los Angeles County-University of Southern California Medical Center was reviewed and, compared with previous years. The incidence of cesarean section for fetal distress is @V and h&s remained constant over the past 7 years. Periodic changes and decreased Mseline variability of the fetal heart rate accounted for 39% of the diagnoses of fetal distress in this group. Scalp &mpling clarifi&d the diagnosis of fetal distress and prevented unnecessary ceaarean section. Compromised p&natal outcome in the >2,500 gram weight group was confined to those who were monitored, had indications for monitoring, or had identifiable prospective risk factors, with rare exceptions. (AM. J. OBSTET. GYNECOL. 135:239, 1979.)
THERE HAS BEEN a significant increase in the cesarean section rate in the past two decades. In the 1950s cesarean section rates of 5% to 7% were unusual. Today many institutions report a cesarean section rate of 15% or greater. Some of this increase has been attributed to the introduction of continuous fetal heart rate monitoring. Haverkamp and colleagues,’ in a study of high-risk patients, reported a cesarean section rate for fetal distress that was 7.4% in the patient managed by continuous fetal heart rate monitoring as opposed to a 1.2% cesarean section rate for fetal distress in patients managed by auscultation of the fetal heart. Renou and associates2 found no significant increase in cesarean sections in a monitored group of high-risk
From the Women’s Hospital, Los Angeles County-University of Southern California Center. Received for publication Revired Accepted
October October
May
Medical
15, 1978.
17, 1978. 19, 1978.
Reprint requests: Dr. E. J. Quilligan, Women’s Hospital, 1240 N. Mission Rd., Los Angeles, California 90033. 0002-9378/79/180239+08$00.80/O
0
1979
The
C. V. Mosby
Co.
patients compared to control nonmonitored patients. One major difference in the two studies was the use of fetal scalp sampling which was utilized in the Renou study while it was not in the Have& management plan. The Department of Obstetrics and Gynecology at Los Angeles County-University of Southern California (LAC-USC) Medical Center has used both continuous fetal heart rate monitoring and fetal scalp blood sampling in the management of high-risk patients for the past 6 to 7 years. We felt it would be useful to look at the indications for cesarean section and how they might be modified by fetal scalp blood sampling in our own population. One year’s experience (1976) was reviewed in order to: (1) define the contribution of the category fetal distress to the cesarean section rate and to see if this increase was concomitant with an increased use of continuous fetal heart rate monitoring, (2) itemize the types of fetal distress, (3) assess how fetal scalp blood sampling may modify obstetric management and interpretation of fetal heart rate monitor records, and (4) determine the immediate outcome in the group of infants who underwent fetal scalp blood sampling. 239
240
Zalar
and Quilligan
September Am. J. Obstet.
Table 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16.
I. Indications
for fetal monitoring
Induction or augmentation of labor Pregnancy-induced hypertension Meconium-stained amniotic fluid Postmaturity Estimated fetal weight less than 2,500 grams (intrauterine growth retardation or prematurity) Maternal medical problem (especially diabetes mellitus, hypertension. rheumatic heart disease, hemoglobinopathy, systemic lupus erythematosus, hyperthyroidism) Abnormal presentation Third-trimester vaginal bleeding Chorioamnionitis Ausctiltated abnormalities of the fetal heart rate Previous uterine surgery Elderly primigravid patient Positive contraction stress test Falling or low estriol levels Previous stillbirth Rhesus sensitization
Material and m#hods In 1976 there were 13,612 live births (13,780 total deliveries) at LAC-USC Medical Center and fetal monitoring was done in 4,978 labors (360/1,000 live births). The rate of fetal monitoring was iritially lOO/ 1,006 live births in the last quarter of 1969 but increased rapidly to its current level where it has been since late 1h72.3 Because of the large volume, not all patients could be monitored, and those considered to be at increased risk received priority. The indications for fetal monitoring in order of frequency appear in Table I. The fetal monitoring records were interpreted by the resident staff, and when there was suspicion of fetal distress in the first stage of labor, the patient became a “candidate for fetal scalp sampling,” which was usually performed. A sample of maternal venous blood collected without stasis was also collected for pH. The interpretation of the fetal scalp sampling results followed these guidelines if maternal pH was normal: (1) if greater than 7.25. the labor was observed; (2) if between 7.20 and 7.25, the sample was repeated within 30 minutes; (3) if less than 7.20, the sample was immediately repeated and the patient was moved to the cesarean section room, where the fetal scalp sampling result was awaited while the patient was prepared for surgery. If the low value was confirmed, a cesarean section was performed. If not, and if the value was again greater than 7.25, the labor was observed. In some instances cesarean section was performed for a persistently downward pH trend or without repeating the fetal scalp sampling. In others the clinician may have foregone fetal scalp sampling altogether on the basis of the clinical setting (e.g., classical pattern, early labor, extremely high-risk or “premium” pregnancy). The primary indications for cesarean section were
15. 1979 Gymecol.
retrieved from the weekly 1976 obstetric statistics and were compared with similar data compiled by Hibbard.’ In some instances there was more than one indication, but the one which led to delivery specifically by cesarean section was considered rhe primary indication (e.g., breech plus dystocia = dystocia). Information regarding the course of labor and its management was obtained from the logbook of the fetal intensive care unit, the microfilm records of the fetal monitor tracings, the logbook of the blood gas laboratory, and the maternal hospital charts. Information regarding the perinatal outcome in the >2,500 gram weight group was obtained from the perinatal mortality statistics, the delivery room logbook, and the neonatal hospital charts. Perinatal deaihs and morbidity were defined as follows: (I) intrapartum fetal dea&--fetal heart tones documented in the labor area and subsequently lost; (2) neonatal death-death in the first 28 days of life; (3) low Apgar score-5 minute Apgar score less than 7.
wsults The primary indications for, the numbers of, and the rates of cesarean se&o? for 1970, 1974, and 1976 are shown in Table II. The total rate has increased slightly, but the increase is almost entirely explained by a change in the approach to breech presentation which is included under malpresentation. The rate of cesarean section for abruptio placentae appears to have fallen, but in the review of 197.6 some patients with that diagnosis underwent cesarean section for fetal distress and thus were included under the latter category. There was no change in the rate of cesarean section for fetal distress during this time. Types of fetal distress are listed in Table III. One hundred thirty-four of 1,O 19 ( 13%) primary cesarean sections were performed for fetal distress. Ninety-two of these were based on changes in the fetal heart rate. Forty-three cesarean sections were done on the basis of late decelerations only. The percentage of infants delivered by cesarean section for fetal distress is about 1% of the total deliveries. Two hundred ninety-eight patients were candidates for fetal scalp sampling; however, in 40 patients the scalp sampling was not performed, in eight due to inability to obtain the sample and in 32 it was elected not to sample. Thus 258 patients underwent fetal scalp sampling for the indications listed in Table IV. This is an incidence of 5.2% of the labors monitored or 1.2% of the total deliveries. The most common indication was the diagnosis or suspicion of late decelerations, accounting for 61% of the total. Although it was performed, fetal scalp sampling for prolonged deceleration or bradycardia ultimately played no role in the
influence of scalp sampling on cesarean section rate
Volume Number
135 2
Table
II. Indications
for cesarean
section
1970* (Total No. of deliveries = 9,775)
Indication
No.
Cesarean section: Repeat Primary Malpresentation Dystocia Fetal distress Placenta previa Abruptio placentae Miscellaneous
928 314 614 134 322 91 37 15 15
*Adapted
Table
from
% Deliveries
1974* (TotaZ No. of deliven’es = 11,584)
70 Primary
9.49 3.21 6.28 1.37 3.30 0.93 0.38 0.15 0.15
1,055 353 702 262 238 130 43 17 12
21.8 52.4 14.8 ;:: 2.4
Antepartum Positive contraction stress test plus unfavorable cervix Severe Rh isoimmunization Intrapartum Prolapsed cord Heart rate changes Bradycardia Prior late decelerations Prior variable decelerations No prior change Late decelerations Abnormal scalp sample Variable decelerations Abnormal scalp sample Decreased baseline variabifity and abnormal scalp sample
counted
when
score
%
No.
identified.
% Primary
10.65 3.26 7.39 2.72 3.09 0.97 0.46 0.06 0.09
36.8 41.8 13.2 6.3 0.8 1.2
1,468 449 1,019 375 426 134 64 8 12
7.1 2.4 1.7
1
3
2
26 74 42 26
15 59
23 43 23 9 3 1
47 53 10 33 1
as <7
baseline
variability
it occurs
Forty-one
only one of these had an low Apgar score at birth. variability, the pregnancy and there was meconium In the total group there
with
9 26 12 3 2 7 11 i 0 1
at 5 minutes
is known
late
28 28 31 30 33
*Some
Table Case No.
251 20 22 0 100
to be sig-
deceleration,’
no periodic
but
change
No. of patients
patients
Birth
weight (gm)
rate
18 18 3 3 21
had multiple
V. Intrapartum
258 158 73
indications.
deaths >2,500 Fetal monitoring
:
3,050 4,010
No No
3
3,270
No
grams Cause of death
Unrecognized breech Previous cesarean section in labor Lethal congenital heart malformation
in all
it
in the absence of any periodic cases of decreased variability had
IV. Scalp samples-Indications*
Total (patients) Late decelerations Decreased baseline heart variatiility Variable decelerations Frolonged decelerations Bradycardia Tachycardia Miscellaneous
%
5
22 92 39 10 6
was classified
may rarely be significant changes. Seventy-three were
% Deliveries
Indication
to deliver by cesarean section. The fetal scalp done for decreased baseline variability acfor 28% of the total and deserves special
Decreased
No.
37.3 33.9 18.5
Low Apgar scwe
attention. nificant
% Primaly
9.11 3.05 6.06 2.26 2.06 1.12 0.37 0.15 0.10
Tabie
No.
Types
judgment sampling
1976 (Total No. of deliveries = 13,780)
L. Hibbard.4
Patients
Apgar
% Deliveries
No.
III. Types of fetal distress
Low groups.
241
and
abnormal scalp blood pH and In addition to the decreased was postdate (>42 weeks) staining of the amniotic fluid. were seven other instances of
the “symptom triad” listed above. All seven infants had a normal scalp blood pH and normal 5 minute Apgar scores at delivery. This syndrome has been previously described.6 The pathophysiology is unknown, but it is postulated that fetal metabolic acidosis acts on the central nervous system’ or directly on the myocardium’ to produce the decrease in baseline variability. The outcome of the labors in which fetal scalp sampling was performed is seen in Fig. 1. A total of 10.4% (271258) of the labors progressed rapidly and obstetric management played little or no role in these vaginai deliveries. In six of these 27 patients, the scalp pH was C7.25, and the one low Apgar score tias found in this group. Another 10% of the labors were terminated on the basis of the fetal heart rate pattern and fetal scalp sampling result; 19% of the infants in this group had
242
Zalar and Quilligan
September Am. J. Obsat.
15. 1979 Gyecol.
CANDIDATES C/S Z” FHR PATTERN
UNABLE T O SS
-----j
ELECTED NOT T O SS
6 CJ
1
11)
ABNORMAL PH
NORMAL PH
C/S 2’= FURTHER CHANGE IN FHA PATTERN
LATES
(1) $k
ABRUPT10 PLACENTAE
PROLONGED DECELERATION VAGINAL SPONTANEOUS
A
DELIVERY OPERATJVE VACUUM EXTRACTION1
FETAL DISTRESS
FAILURE OF DESCENT IOYSTOCIAI
Fig. 1. Outcome of labors in which fetal scalp sampling was performed. Numbers in parentheses are numbers of low 5 minute Apgar scores.
low Apgar scores. Five percent (11 of 205) of those remaining were later delivered by cesarean section for feta1 distress, based on worsening patterns or prolonged deceleration. It is noteworthy that 74% (2201298) of the candidates, 85% of those undergoing fetal scalp sampling (220/258) and 95% .( 194/205) of those with a normal scalp pH and an observable labor, were nit delivered by cesarean section for fetal distress. Approximately 25% of those delivered by cesarean section for fetal distress had low Apgar scores (20/78), but these accounted for only 65% (20/3 1) of ,a11the low Apgar scores. It is of interest to consider some of the others individually. One cesarean section was done for abruptio placentae and a falling hematocrit and resulted in a low Apgar score, explained by a low umbilical cord pH:AII three low Apgar scores in the cesarean section for dystocia group were associated with clinical chorioamnionitis; in one case the cord pH was normal, and asphyxia was excluded as the etiology. The three low Apgar scores in the spontaneous vaginal delivery group are not well explained, although clinical chorio-
amnionitis (2/3), significant delay between the time of the fetal scalp sampling and delivery (2/3), and severe cord compression patterns just prior to delivery (l/3) may have been contributory. The results in those patients who underwent fetal scalp sampling for late decelerations are seen in Fig. 2. Of 178 candidates only 47 (26%) had cesarean sections for fetal distress and the total cesarean section rate in this group was 39% (70/178). Table V shows the intrapartum deaths in the >2,500 gram weight group. Case 1 was misdiagnosed as a cephalic presentation by a first-year house officer and by the time the error was recognized the fetal heart tones were lost. Case 2 was that of a 28-year-old secundigravid patient admitted for repeat cesarean section in early labor with an unengaged vertex, a cervix dilated to one fingertip, and intact membranes. The history and physical examination were unremarkable. External monitoring was not done. Fetal heart tones were last heard immediately prior to the abdominal preparation for surgery, and when the uterus was entered.
Volume 135 Number
Influence of scalp sampling on cesarean section rate
243
2
C/S 20FHR
PATTERN
CANDIDATES
I
SCALP-SAMPLED
-
ELECTED NOT T O SS
UNABLE T O SS
m
1
lo) m C/S 20 FHR PATTERN + SS I 23
15’
I?
- RAPID
El 18
15)
1 C/S 20 FURTHER CHANGE IN FHR PATTERN
A
4
2
2
C/S 2O OTHER INDICATION
(1)
(1) DYSTOCIA
PROLONGED DECELERATION
SPONTANEOUS
I
OBSERVED
-
1 67
111
(21
(1)
LATES
PROGRESS
VAGINAL
DELIVERY
A
(1)
ABRUPT10 PLACENTAE
OPERATIVE
A
19
7
101
FETAL DISTRESS
(2)
12
i2)
FAILURE OF DESCENT 0YSTOCIA)
Fig. 2. Results in patients undergoing fetal scalp sampling for late decelerations. Numbers in parentheses are numbers of low 5 minute Apgar scores.
thick meconium and a nuchal cord were encountered. The infant was a fresh stillborn and efforts at resuscitation failed. Both patients had risk factors when considered prospectively, and both had indications for fetal monitoring or obstetric intervention. There were no intrapartum deaths in the >2,500 gram weight group who underwent fetal monitoring. In fact there was none in the >I,500 gram weight group undergoing fetal monitoring. Table VI showsthe neonatal deaths in the >2,500 gram weight group. In this group only the deaths from intrapartum asphyxia would have been influenced by intrapartum fetal monitoring. In those casesof death associatedwith abruptio placentae, all patients were admitted to the labor area with vaginal bleeding and fetal bradycardia and underwent immediate cesarean section. Those deaths from meconium aspiration also must be considered asphyxial and potentially preventable by fetal monitoring. Four of the five labors were monitored, and in three of those four delivery wasperformed becauseof fetal distress.In one of these three,
intervention wastardy and the opportunity to enhance the chance of neonatal survival may have been missed. The one unmonitored patient was admitted late in labor and progressedrapidly to vaginal delivery before fetal monitoring could be instituted. The low 5 minute Apgar scoresin the >2,500 gram weight group are shown in Fig. 3. The incidence was 7/ 1,000live births. In 3 1 of 90, delivery wasperformed becauseof fetal distress,and 20 of these 31 underwent fetal monitoring. Only 18 patients were unmonitored, not delivered becauseof fetal distress, and not delivered by cesareansection. The attendant risk factors in 14 of these 18 who did not have a midpelvic operative vaginal delivery (i.e., vacuum extraction or midforceps) are shownin Table VII, demonstrating that only five of 90 low Apgar scores are poorly explained or unexplained. Thus 85 of the 90 infants with low Apgar scores prospectively had identifiable risk factors, had indications for fetal monitoring, or were delivered hecauseof fetal distress.It is of interest that of 58 patients who underwent fetal monitoring and were delivered of
244
Table
Zalar and Quilligan
VI. Neonatal
Clinicopathologic
September Am. J. Obstet.
deaths in infants
correlations
weighing
Birth weight kWJ
Apgar scores
Mode d&q
3,860 3,600 3,000 3,000 3,500
a/9 l/7 l/l 3/a l/2
2,630 3,450 3,040
>2,500
grams (No. = 30)
monitoring
Delivered for fetal distress
Scalp sample
Vaginal CS CS CS cs
No Yes Yes Yes Yes
No No Yes Yes Yes
Yes Yes Yes No
l/O o/o/2 o/o/4
cs cs cs
No No No
Yes Yes Yes
Bradycardia on admission Bradycardia on admission
4,780 5,100 3,470 3,240
618 719 6110 l/2
Vaginal Vaginal Vaginal cs
No No No Yes
No No No No
No
Fractured humerus Neonatal cystic hygroma Failed midforceps delivery
2.780
216
cs
No
No
2,770
819
cs
Yes
No
No
Piacenta previa, maternal pheochromocytoma Sepsis(?)
Fetal
of
13, 1979 Gynecol.
Comments
Lethal congenital malformation (No. = 16) Meconium aspbation (No. = 5):
Case 1 Case 2 Case 3 Case 4 Case 5 Abruptio
placentae
(No.
Case 2
CS: Cesarean section; RDS: respiratory distress; NEC: necrotizing VII.
Attendant Risk
Bradycardia
= 3):
Case 1 Case 2 Case 3 Sepsis(No. = 3): Case 1 Case 2 Case 3 Trauma (1) RDS ? NEC (2) Case 1
Table
Late intervention
risk factors to Fig. 3
factors (Total
= 14)
No.
Congenital malformation Second twin Meconium-stained amniotic fluid (rapid progress of labor) Breech presentation Abruptio placentae Amniotic fluid embolism Hydramnios (5 1) (rapid progress of labor) Total Analgesic Unexplained Chart available Total
infants with low 5 minute Apgar delivered vaginally or abdominally tress (Fig. 3).
2 1 2 1 1 1 1 9 2 : 5
scores, only 20 were because of fetal dis-
Comment The data from this review show that the incidence of cesarean section for fetal distress in this institution is low and has remained low over the last 7 years. Fetal scalp sampling prevented unnecessary cesarean section when the fetal heart rate tracing suggested fetal distress. The incidence of cesarean section has risen slightly during the period of observation, explained almost entirely by a change in the attitude toward
enterocolitis. breech presentation. Kubli’O has had a similar experience. The evidence in this study corroborates some of the findings previously reported regarding fetal monitoring. Intrapartum fetal death, with a previously expected incidence at term of 1 to 2/1,000,3* 9 may be virtually eliminated. 3, 8 Continuous fetal heart monitoring, even with the assistance of scalp sampling in this study, “overpredicts” neonatal depression based on the 5 minute Apgar score.“, ‘I Although false positive results are more desirable than false negative ones in this setting, it is significant that while about 25% of those infants of all weight groups who were delivered because of fetal distress had low 5 minute Apgar scores only about 35% of those t.erm infants who were monitored and had low Apgar scores were delivered because of fetal distress. These findings suggest that the methodology or the local practices of diagnosing fetal distress on the fetal monitor need further refinement and/or that the majority of the remaining neonatal depression at term is not hypoxic in origin (e.g., trauma secondary to dystocia, infection, airway obstruction secondary to meconium, congenital malformation). One must question, however, the 5 minute Apgar score as an end point, since even in the group delivered because of fetal acidosis the low Apgar score rate was only 22%. We may also have some cases of low Phs in which delivery is not required since in some instances the low pH may be on the basis of an elevated Pcoz alone
Volume Number
135 2
Influence
NO FM
A5
VAGINAL
50
FETAL DISTRESS
NO FM
FM
El-
19
31
NO
FM
of scalp
sampling
on cesarean
section
rate
245
FM
DELIVERY
F”LOTHER
1
(6)
I
WITH RISK FACTORS
DELIVERED FOR FETAL DISTRESS
A
18
4
DYSTOCIA (OPERATIVE MIDPELVIC DELIVERY1
14
OTHER ISEE TABLE
VII )
Fig. 3. Low 5 minute Apgar scores in the >72,500 gram weight group. Numbers in parentheses are numbers of babies in whom scalp sampling was done. rather than metabolic acidosis. This can be eliminated only by measuring Pco2 or a Pcoz specimen equilibrated at 40 mm Hg. The cases of asphyxial neonatal deaths aIf had identifiable risk factors and indications for fetal monitoring or immediate delivery when considered prospectively, and in most instances a cesarean section was performed for the indication of fetal distress. The results of this study suggest that in the >2,500 gram infant the current application of fetal heart rate monitoring and scalp sampling has greater impact on the prediction and prevention of intrapartum death than neonatal death or neonatal depression. It has been amply shown that continuous fetal monitoring benefits the premature infant,3, 21-23 especially in the 1,000 to 1,500 gram weight group,3 and consequently premature infants were not studied separately in this report. There is only indirect evidence that fetal monitoring alters the perinatal mortality rate of the >1,500 gram weight group. Paul and Hon3 showed that intrapartum and neonatal mortality rates were not significantly different, contrary to expectations, in monitored and unmonitored patients during the first 3 years of fetal monitoring at this institution. While the conclusions of that study are undoubtedly still true, the
current review of compromised perinatal outcome in the same institution shows that some high-risk patients were included in the unmonitored group. It also shows that compromised perinatal outcome in the >2,500 gram weight group, with rare exceptions, was limited to the group selected for fetal monitoring and high-risk patients remaining in the unmonitored group. The high-risk concept has been developed over the past decade. rz. I3 Lilieng reported from the Collaborative Perinatal Study that term intrapartum fetal death in the absence of risk factors was exceedingly rare-less than l/25,000 in that study. Hobel and colleagues13 stressed the use of intrapartum as well as antepartum criteria of high risk, and two important conclusions may be drawn from their study. First, the patient with a normal pregnancy and an abnormal labor was actually at slightly greater risk for a poor outcome than was the patient with an abnormal pregnancy and a normal labor, emphasizing the need to continue high-risk screening in the intrapartum period. Second, a very low-risk group may be identified by exclusion, which in this study experienced no perinatal deaths other than that caused by lethal congenital malformation. The data of the present study support the selection of candidates for fetal intensive care by the liberal use of such
246
Zalar
and Quilligan
September 15, 1979 Am. J. Obstet. Gynerol.
high-risk criteria in a setting where immediate intervention is possible. The question of yield is inevitably raised by this report. Only about one-third of all intrapartum patients underwent continuous fetal heart rate monitoring, yet those infants with compromised perinatal outcomes were almost universally monitored, had indications for monitoring, or had identifiable prospective risk factors.
The yield of monitoring the remaining two thirds of our population would appear to be small, i.e., about 5% of the infants with low Apgar scores in the >2,500 gram weight group were possibly without risk factors. Until further studies have been performed one couid utilize this type of information in making a rational choice as to the use of monitors when limited numbers of instruments are available.
REFERENCES
1. Haverkamp, A. D., Thompson, E. E., McFee, J. G., and Cetrulo, C.: The evaluation of continuous fetal heart rate monitoring in high-risk pregnancy, AM. J. OBSTET. GYNECOL.
125:310,
8.
1976.
2. Renou, P., Chang, A., Anderson, trolled trial of fetal intensive
I., and Wood, C.: Concare, AM. J. OBSTET.
9.
3. Paul, R. H., and Hon, E. H.: Clinical fetal monitoring. V. Effect on perinatal outcome, AM. J. OBSTET. GYNECOL.
10.
GYNECOL.
1 l&529,
126~470,
1976.
1974.
4. Hibbard, L. T.: Changing trends in cesarean section, AM. J.OBSTET.GYNECOL. 125:798, 1976. 5. Paul, R. H., Suidan, A. K., Yeh, S-Y, Schifrin, B. S., and Hon, E. H.: Clinical fetal monitoring. VII. The evaluation and significance of intrapartum baseline fetal heart rate variability, AM. J. OBSTET. GYNECOL. 123:206, 1975. 6. Cibils, L. A.: Clinical significance of fetal heart rate patterns during labor. I. Baseline patterns, AM. J. OBSTET. GyNECOL. 125:290, 1976. 7. Mann, L. I.. Solomon, G., Carmichael, A., and Duchin, S.:
11.
12. 13.
The effect of metabolic acidosis on fetal brain function and metabolism, AM. J. OBSTET. GYNECOL. 111:353, I97 1. Shenker, L., Post, R. C., and Seiler, J. S.: Routine electronic monitoring of fetal heart rate and uterine activity during labor, Obstet. Gynecol. 46: 185, 1975. L&en, A. A.: Term intrapartum fetal death, AM. J. OBSTET.GYNECOL. 107:595, 1970. Kubli, F. W.: Influence of labor on fetal acid-base balance, Clin. Obstet. Gynecol. 11:168, 1968. Low, J. A., Pancham, S. R., Worthington, D., and Boston, R. W.: Clinical characteristics of pregnancies complicated by intrapartum fetal asphyxia, AM. J. OBSTET. CYNECOL. 121:452, 1975. Goodwin, J. W., Dunne, J. T., and Thomas, B. W.: Antepartum identification of the fetus at risk, Can. Med. Assoc. J. 101:458, 1969. Hobel, C. J., Hyvarinen. M. A., Okada, D. M., and Oh, W.: Prenatal and intrapartum high-risk screening. I. Prediction of the high-risk neonate, AM. J. OBSTET. GYNEcoL. 117:1, 1973.
The influence bf scalp sampling on the cesarean section rate for fetal distress RICHARD EDWARD Los Angeles,
W.
ZALAR,
JR.,
J. QUILLIGAN,
M.D.
M.D.
Calz;fornia
One%y&r’s obstetric experience at Los Angeles County-University of Southern California Medical Center was reviewed and, compared with previous years. The incidence of cesarean section for fetal distress is @V and h&s remained constant over the past 7 years. Periodic changes and decreased Mseline variability of the fetal heart rate accounted for 39% of the diagnoses of fetal distress in this group. Scalp &mpling clarifi&d the diagnosis of fetal distress and prevented unnecessary ceaarean section. Compromised p&natal outcome in the >2,500 gram weight group was confined to those who were monitored, had indications for monitoring, or had identifiable prospective risk factors, with rare exceptions. (AM. J. OBSTET. GYNECOL. 135:239, 1979.)
THERE HAS BEEN a significant increase in the cesarean section rate in the past two decades. In the 1950s cesarean section rates of 5% to 7% were unusual. Today many institutions report a cesarean section rate of 15% or greater. Some of this increase has been attributed to the introduction of continuous fetal heart rate monitoring. Haverkamp and colleagues,’ in a study of high-risk patients, reported a cesarean section rate for fetal distress that was 7.4% in the patient managed by continuous fetal heart rate monitoring as opposed to a 1.2% cesarean section rate for fetal distress in patients managed by auscultation of the fetal heart. Renou and associates2 found no significant increase in cesarean sections in a monitored group of high-risk
From the Women’s Hospital, Los Angeles County-University of Southern California Center. Received for publication Revired Accepted
October October
May
Medical
15, 1978.
17, 1978. 19, 1978.
Reprint requests: Dr. E. J. Quilligan, Women’s Hospital, 1240 N. Mission Rd., Los Angeles, California 90033. 0002-9378/79/180239+08$00.80/O
0
1979
The
C. V. Mosby
Co.
patients compared to control nonmonitored patients. One major difference in the two studies was the use of fetal scalp sampling which was utilized in the Renou study while it was not in the Have& management plan. The Department of Obstetrics and Gynecology at Los Angeles County-University of Southern California (LAC-USC) Medical Center has used both continuous fetal heart rate monitoring and fetal scalp blood sampling in the management of high-risk patients for the past 6 to 7 years. We felt it would be useful to look at the indications for cesarean section and how they might be modified by fetal scalp blood sampling in our own population. One year’s experience (1976) was reviewed in order to: (1) define the contribution of the category fetal distress to the cesarean section rate and to see if this increase was concomitant with an increased use of continuous fetal heart rate monitoring, (2) itemize the types of fetal distress, (3) assess how fetal scalp blood sampling may modify obstetric management and interpretation of fetal heart rate monitor records, and (4) determine the immediate outcome in the group of infants who underwent fetal scalp blood sampling. 239
240
Zalar
and Quilligan
September Am. J. Obstet.
Table 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16.
I. Indications
for fetal monitoring
Induction or augmentation of labor Pregnancy-induced hypertension Meconium-stained amniotic fluid Postmaturity Estimated fetal weight less than 2,500 grams (intrauterine growth retardation or prematurity) Maternal medical problem (especially diabetes mellitus, hypertension. rheumatic heart disease, hemoglobinopathy, systemic lupus erythematosus, hyperthyroidism) Abnormal presentation Third-trimester vaginal bleeding Chorioamnionitis Ausctiltated abnormalities of the fetal heart rate Previous uterine surgery Elderly primigravid patient Positive contraction stress test Falling or low estriol levels Previous stillbirth Rhesus sensitization
Material and m#hods In 1976 there were 13,612 live births (13,780 total deliveries) at LAC-USC Medical Center and fetal monitoring was done in 4,978 labors (360/1,000 live births). The rate of fetal monitoring was iritially lOO/ 1,006 live births in the last quarter of 1969 but increased rapidly to its current level where it has been since late 1h72.3 Because of the large volume, not all patients could be monitored, and those considered to be at increased risk received priority. The indications for fetal monitoring in order of frequency appear in Table I. The fetal monitoring records were interpreted by the resident staff, and when there was suspicion of fetal distress in the first stage of labor, the patient became a “candidate for fetal scalp sampling,” which was usually performed. A sample of maternal venous blood collected without stasis was also collected for pH. The interpretation of the fetal scalp sampling results followed these guidelines if maternal pH was normal: (1) if greater than 7.25. the labor was observed; (2) if between 7.20 and 7.25, the sample was repeated within 30 minutes; (3) if less than 7.20, the sample was immediately repeated and the patient was moved to the cesarean section room, where the fetal scalp sampling result was awaited while the patient was prepared for surgery. If the low value was confirmed, a cesarean section was performed. If not, and if the value was again greater than 7.25, the labor was observed. In some instances cesarean section was performed for a persistently downward pH trend or without repeating the fetal scalp sampling. In others the clinician may have foregone fetal scalp sampling altogether on the basis of the clinical setting (e.g., classical pattern, early labor, extremely high-risk or “premium” pregnancy). The primary indications for cesarean section were
15. 1979 Gymecol.
retrieved from the weekly 1976 obstetric statistics and were compared with similar data compiled by Hibbard.’ In some instances there was more than one indication, but the one which led to delivery specifically by cesarean section was considered rhe primary indication (e.g., breech plus dystocia = dystocia). Information regarding the course of labor and its management was obtained from the logbook of the fetal intensive care unit, the microfilm records of the fetal monitor tracings, the logbook of the blood gas laboratory, and the maternal hospital charts. Information regarding the perinatal outcome in the >2,500 gram weight group was obtained from the perinatal mortality statistics, the delivery room logbook, and the neonatal hospital charts. Perinatal deaihs and morbidity were defined as follows: (I) intrapartum fetal dea&--fetal heart tones documented in the labor area and subsequently lost; (2) neonatal death-death in the first 28 days of life; (3) low Apgar score-5 minute Apgar score less than 7.
wsults The primary indications for, the numbers of, and the rates of cesarean se&o? for 1970, 1974, and 1976 are shown in Table II. The total rate has increased slightly, but the increase is almost entirely explained by a change in the approach to breech presentation which is included under malpresentation. The rate of cesarean section for abruptio placentae appears to have fallen, but in the review of 197.6 some patients with that diagnosis underwent cesarean section for fetal distress and thus were included under the latter category. There was no change in the rate of cesarean section for fetal distress during this time. Types of fetal distress are listed in Table III. One hundred thirty-four of 1,O 19 ( 13%) primary cesarean sections were performed for fetal distress. Ninety-two of these were based on changes in the fetal heart rate. Forty-three cesarean sections were done on the basis of late decelerations only. The percentage of infants delivered by cesarean section for fetal distress is about 1% of the total deliveries. Two hundred ninety-eight patients were candidates for fetal scalp sampling; however, in 40 patients the scalp sampling was not performed, in eight due to inability to obtain the sample and in 32 it was elected not to sample. Thus 258 patients underwent fetal scalp sampling for the indications listed in Table IV. This is an incidence of 5.2% of the labors monitored or 1.2% of the total deliveries. The most common indication was the diagnosis or suspicion of late decelerations, accounting for 61% of the total. Although it was performed, fetal scalp sampling for prolonged deceleration or bradycardia ultimately played no role in the
influence of scalp sampling on cesarean section rate
Volume Number
135 2
Table
II. Indications
for cesarean
section
1970* (Total No. of deliveries = 9,775)
Indication
No.
Cesarean section: Repeat Primary Malpresentation Dystocia Fetal distress Placenta previa Abruptio placentae Miscellaneous
928 314 614 134 322 91 37 15 15
*Adapted
Table
from
% Deliveries
1974* (TotaZ No. of deliven’es = 11,584)
70 Primary
9.49 3.21 6.28 1.37 3.30 0.93 0.38 0.15 0.15
1,055 353 702 262 238 130 43 17 12
21.8 52.4 14.8 ;:: 2.4
Antepartum Positive contraction stress test plus unfavorable cervix Severe Rh isoimmunization Intrapartum Prolapsed cord Heart rate changes Bradycardia Prior late decelerations Prior variable decelerations No prior change Late decelerations Abnormal scalp sample Variable decelerations Abnormal scalp sample Decreased baseline variabifity and abnormal scalp sample
counted
when
score
%
No.
identified.
% Primary
10.65 3.26 7.39 2.72 3.09 0.97 0.46 0.06 0.09
36.8 41.8 13.2 6.3 0.8 1.2
1,468 449 1,019 375 426 134 64 8 12
7.1 2.4 1.7
1
3
2
26 74 42 26
15 59
23 43 23 9 3 1
47 53 10 33 1
as <7
baseline
variability
it occurs
Forty-one
only one of these had an low Apgar score at birth. variability, the pregnancy and there was meconium In the total group there
with
9 26 12 3 2 7 11 i 0 1
at 5 minutes
is known
late
28 28 31 30 33
*Some
Table Case No.
251 20 22 0 100
to be sig-
deceleration,’
no periodic
but
change
No. of patients
patients
Birth
weight (gm)
rate
18 18 3 3 21
had multiple
V. Intrapartum
258 158 73
indications.
deaths >2,500 Fetal monitoring
:
3,050 4,010
No No
3
3,270
No
grams Cause of death
Unrecognized breech Previous cesarean section in labor Lethal congenital heart malformation
in all
it
in the absence of any periodic cases of decreased variability had
IV. Scalp samples-Indications*
Total (patients) Late decelerations Decreased baseline heart variatiility Variable decelerations Frolonged decelerations Bradycardia Tachycardia Miscellaneous
%
5
22 92 39 10 6
was classified
may rarely be significant changes. Seventy-three were
% Deliveries
Indication
to deliver by cesarean section. The fetal scalp done for decreased baseline variability acfor 28% of the total and deserves special
Decreased
No.
37.3 33.9 18.5
Low Apgar scwe
attention. nificant
% Primaly
9.11 3.05 6.06 2.26 2.06 1.12 0.37 0.15 0.10
Tabie
No.
Types
judgment sampling
1976 (Total No. of deliveries = 13,780)
L. Hibbard.4
Patients
Apgar
% Deliveries
No.
III. Types of fetal distress
Low groups.
241
and
abnormal scalp blood pH and In addition to the decreased was postdate (>42 weeks) staining of the amniotic fluid. were seven other instances of
the “symptom triad” listed above. All seven infants had a normal scalp blood pH and normal 5 minute Apgar scores at delivery. This syndrome has been previously described.6 The pathophysiology is unknown, but it is postulated that fetal metabolic acidosis acts on the central nervous system’ or directly on the myocardium’ to produce the decrease in baseline variability. The outcome of the labors in which fetal scalp sampling was performed is seen in Fig. 1. A total of 10.4% (271258) of the labors progressed rapidly and obstetric management played little or no role in these vaginai deliveries. In six of these 27 patients, the scalp pH was C7.25, and the one low Apgar score tias found in this group. Another 10% of the labors were terminated on the basis of the fetal heart rate pattern and fetal scalp sampling result; 19% of the infants in this group had
242
Zalar and Quilligan
September Am. J. Obsat.
15. 1979 Gyecol.
CANDIDATES C/S Z” FHR PATTERN
UNABLE T O SS
-----j
ELECTED NOT T O SS
6 CJ
1
11)
ABNORMAL PH
NORMAL PH
C/S 2’= FURTHER CHANGE IN FHA PATTERN
LATES
(1) $k
ABRUPT10 PLACENTAE
PROLONGED DECELERATION VAGINAL SPONTANEOUS
A
DELIVERY OPERATJVE VACUUM EXTRACTION1
FETAL DISTRESS
FAILURE OF DESCENT IOYSTOCIAI
Fig. 1. Outcome of labors in which fetal scalp sampling was performed. Numbers in parentheses are numbers of low 5 minute Apgar scores.
low Apgar scores. Five percent (11 of 205) of those remaining were later delivered by cesarean section for feta1 distress, based on worsening patterns or prolonged deceleration. It is noteworthy that 74% (2201298) of the candidates, 85% of those undergoing fetal scalp sampling (220/258) and 95% .( 194/205) of those with a normal scalp pH and an observable labor, were nit delivered by cesarean section for fetal distress. Approximately 25% of those delivered by cesarean section for fetal distress had low Apgar scores (20/78), but these accounted for only 65% (20/3 1) of ,a11the low Apgar scores. It is of interest to consider some of the others individually. One cesarean section was done for abruptio placentae and a falling hematocrit and resulted in a low Apgar score, explained by a low umbilical cord pH:AII three low Apgar scores in the cesarean section for dystocia group were associated with clinical chorioamnionitis; in one case the cord pH was normal, and asphyxia was excluded as the etiology. The three low Apgar scores in the spontaneous vaginal delivery group are not well explained, although clinical chorio-
amnionitis (2/3), significant delay between the time of the fetal scalp sampling and delivery (2/3), and severe cord compression patterns just prior to delivery (l/3) may have been contributory. The results in those patients who underwent fetal scalp sampling for late decelerations are seen in Fig. 2. Of 178 candidates only 47 (26%) had cesarean sections for fetal distress and the total cesarean section rate in this group was 39% (70/178). Table V shows the intrapartum deaths in the >2,500 gram weight group. Case 1 was misdiagnosed as a cephalic presentation by a first-year house officer and by the time the error was recognized the fetal heart tones were lost. Case 2 was that of a 28-year-old secundigravid patient admitted for repeat cesarean section in early labor with an unengaged vertex, a cervix dilated to one fingertip, and intact membranes. The history and physical examination were unremarkable. External monitoring was not done. Fetal heart tones were last heard immediately prior to the abdominal preparation for surgery, and when the uterus was entered.
Volume 135 Number
Influence of scalp sampling on cesarean section rate
243
2
C/S 20FHR
PATTERN
CANDIDATES
I
SCALP-SAMPLED
-
ELECTED NOT T O SS
UNABLE T O SS
m
1
lo) m C/S 20 FHR PATTERN + SS I 23
15’
I?
- RAPID
El 18
15)
1 C/S 20 FURTHER CHANGE IN FHR PATTERN
A
4
2
2
C/S 2O OTHER INDICATION
(1)
(1) DYSTOCIA
PROLONGED DECELERATION
SPONTANEOUS
I
OBSERVED
-
1 67
111
(21
(1)
LATES
PROGRESS
VAGINAL
DELIVERY
A
(1)
ABRUPT10 PLACENTAE
OPERATIVE
A
19
7
101
FETAL DISTRESS
(2)
12
i2)
FAILURE OF DESCENT 0YSTOCIA)
Fig. 2. Results in patients undergoing fetal scalp sampling for late decelerations. Numbers in parentheses are numbers of low 5 minute Apgar scores.
thick meconium and a nuchal cord were encountered. The infant was a fresh stillborn and efforts at resuscitation failed. Both patients had risk factors when considered prospectively, and both had indications for fetal monitoring or obstetric intervention. There were no intrapartum deaths in the >2,500 gram weight group who underwent fetal monitoring. In fact there was none in the >I,500 gram weight group undergoing fetal monitoring. Table VI showsthe neonatal deaths in the >2,500 gram weight group. In this group only the deaths from intrapartum asphyxia would have been influenced by intrapartum fetal monitoring. In those casesof death associatedwith abruptio placentae, all patients were admitted to the labor area with vaginal bleeding and fetal bradycardia and underwent immediate cesarean section. Those deaths from meconium aspiration also must be considered asphyxial and potentially preventable by fetal monitoring. Four of the five labors were monitored, and in three of those four delivery wasperformed becauseof fetal distress.In one of these three,
intervention wastardy and the opportunity to enhance the chance of neonatal survival may have been missed. The one unmonitored patient was admitted late in labor and progressedrapidly to vaginal delivery before fetal monitoring could be instituted. The low 5 minute Apgar scoresin the >2,500 gram weight group are shown in Fig. 3. The incidence was 7/ 1,000live births. In 3 1 of 90, delivery wasperformed becauseof fetal distress,and 20 of these 31 underwent fetal monitoring. Only 18 patients were unmonitored, not delivered becauseof fetal distress, and not delivered by cesareansection. The attendant risk factors in 14 of these 18 who did not have a midpelvic operative vaginal delivery (i.e., vacuum extraction or midforceps) are shownin Table VII, demonstrating that only five of 90 low Apgar scores are poorly explained or unexplained. Thus 85 of the 90 infants with low Apgar scores prospectively had identifiable risk factors, had indications for fetal monitoring, or were delivered hecauseof fetal distress.It is of interest that of 58 patients who underwent fetal monitoring and were delivered of
244
Table
Zalar and Quilligan
VI. Neonatal
Clinicopathologic
September Am. J. Obstet.
deaths in infants
correlations
weighing
Birth weight kWJ
Apgar scores
Mode d&q
3,860 3,600 3,000 3,000 3,500
a/9 l/7 l/l 3/a l/2
2,630 3,450 3,040
>2,500
grams (No. = 30)
monitoring
Delivered for fetal distress
Scalp sample
Vaginal CS CS CS cs
No Yes Yes Yes Yes
No No Yes Yes Yes
Yes Yes Yes No
l/O o/o/2 o/o/4
cs cs cs
No No No
Yes Yes Yes
Bradycardia on admission Bradycardia on admission
4,780 5,100 3,470 3,240
618 719 6110 l/2
Vaginal Vaginal Vaginal cs
No No No Yes
No No No No
No
Fractured humerus Neonatal cystic hygroma Failed midforceps delivery
2.780
216
cs
No
No
2,770
819
cs
Yes
No
No
Piacenta previa, maternal pheochromocytoma Sepsis(?)
Fetal
of
13, 1979 Gynecol.
Comments
Lethal congenital malformation (No. = 16) Meconium aspbation (No. = 5):
Case 1 Case 2 Case 3 Case 4 Case 5 Abruptio
placentae
(No.
Case 2
CS: Cesarean section; RDS: respiratory distress; NEC: necrotizing VII.
Attendant Risk
Bradycardia
= 3):
Case 1 Case 2 Case 3 Sepsis(No. = 3): Case 1 Case 2 Case 3 Trauma (1) RDS ? NEC (2) Case 1
Table
Late intervention
risk factors to Fig. 3
factors (Total
= 14)
No.
Congenital malformation Second twin Meconium-stained amniotic fluid (rapid progress of labor) Breech presentation Abruptio placentae Amniotic fluid embolism Hydramnios (5 1) (rapid progress of labor) Total Analgesic Unexplained Chart available Total
infants with low 5 minute Apgar delivered vaginally or abdominally tress (Fig. 3).
2 1 2 1 1 1 1 9 2 : 5
scores, only 20 were because of fetal dis-
Comment The data from this review show that the incidence of cesarean section for fetal distress in this institution is low and has remained low over the last 7 years. Fetal scalp sampling prevented unnecessary cesarean section when the fetal heart rate tracing suggested fetal distress. The incidence of cesarean section has risen slightly during the period of observation, explained almost entirely by a change in the attitude toward
enterocolitis. breech presentation. Kubli’O has had a similar experience. The evidence in this study corroborates some of the findings previously reported regarding fetal monitoring. Intrapartum fetal death, with a previously expected incidence at term of 1 to 2/1,000,3* 9 may be virtually eliminated. 3, 8 Continuous fetal heart monitoring, even with the assistance of scalp sampling in this study, “overpredicts” neonatal depression based on the 5 minute Apgar score.“, ‘I Although false positive results are more desirable than false negative ones in this setting, it is significant that while about 25% of those infants of all weight groups who were delivered because of fetal distress had low 5 minute Apgar scores only about 35% of those t.erm infants who were monitored and had low Apgar scores were delivered because of fetal distress. These findings suggest that the methodology or the local practices of diagnosing fetal distress on the fetal monitor need further refinement and/or that the majority of the remaining neonatal depression at term is not hypoxic in origin (e.g., trauma secondary to dystocia, infection, airway obstruction secondary to meconium, congenital malformation). One must question, however, the 5 minute Apgar score as an end point, since even in the group delivered because of fetal acidosis the low Apgar score rate was only 22%. We may also have some cases of low Phs in which delivery is not required since in some instances the low pH may be on the basis of an elevated Pcoz alone
Volume Number
135 2
Influence
NO FM
A5
VAGINAL
50
FETAL DISTRESS
NO FM
FM
El-
19
31
NO
FM
of scalp
sampling
on cesarean
section
rate
245
FM
DELIVERY
F”LOTHER
1
(6)
I
WITH RISK FACTORS
DELIVERED FOR FETAL DISTRESS
A
18
4
DYSTOCIA (OPERATIVE MIDPELVIC DELIVERY1
14
OTHER ISEE TABLE
VII )
Fig. 3. Low 5 minute Apgar scores in the >72,500 gram weight group. Numbers in parentheses are numbers of babies in whom scalp sampling was done. rather than metabolic acidosis. This can be eliminated only by measuring Pco2 or a Pcoz specimen equilibrated at 40 mm Hg. The cases of asphyxial neonatal deaths aIf had identifiable risk factors and indications for fetal monitoring or immediate delivery when considered prospectively, and in most instances a cesarean section was performed for the indication of fetal distress. The results of this study suggest that in the >2,500 gram infant the current application of fetal heart rate monitoring and scalp sampling has greater impact on the prediction and prevention of intrapartum death than neonatal death or neonatal depression. It has been amply shown that continuous fetal monitoring benefits the premature infant,3, 21-23 especially in the 1,000 to 1,500 gram weight group,3 and consequently premature infants were not studied separately in this report. There is only indirect evidence that fetal monitoring alters the perinatal mortality rate of the >1,500 gram weight group. Paul and Hon3 showed that intrapartum and neonatal mortality rates were not significantly different, contrary to expectations, in monitored and unmonitored patients during the first 3 years of fetal monitoring at this institution. While the conclusions of that study are undoubtedly still true, the
current review of compromised perinatal outcome in the same institution shows that some high-risk patients were included in the unmonitored group. It also shows that compromised perinatal outcome in the >2,500 gram weight group, with rare exceptions, was limited to the group selected for fetal monitoring and high-risk patients remaining in the unmonitored group. The high-risk concept has been developed over the past decade. rz. I3 Lilieng reported from the Collaborative Perinatal Study that term intrapartum fetal death in the absence of risk factors was exceedingly rare-less than l/25,000 in that study. Hobel and colleagues13 stressed the use of intrapartum as well as antepartum criteria of high risk, and two important conclusions may be drawn from their study. First, the patient with a normal pregnancy and an abnormal labor was actually at slightly greater risk for a poor outcome than was the patient with an abnormal pregnancy and a normal labor, emphasizing the need to continue high-risk screening in the intrapartum period. Second, a very low-risk group may be identified by exclusion, which in this study experienced no perinatal deaths other than that caused by lethal congenital malformation. The data of the present study support the selection of candidates for fetal intensive care by the liberal use of such
246
Zalar
and Quilligan
September 15, 1979 Am. J. Obstet. Gynerol.
high-risk criteria in a setting where immediate intervention is possible. The question of yield is inevitably raised by this report. Only about one-third of all intrapartum patients underwent continuous fetal heart rate monitoring, yet those infants with compromised perinatal outcomes were almost universally monitored, had indications for monitoring, or had identifiable prospective risk factors.
The yield of monitoring the remaining two thirds of our population would appear to be small, i.e., about 5% of the infants with low Apgar scores in the >2,500 gram weight group were possibly without risk factors. Until further studies have been performed one couid utilize this type of information in making a rational choice as to the use of monitors when limited numbers of instruments are available.
REFERENCES
1. Haverkamp, A. D., Thompson, E. E., McFee, J. G., and Cetrulo, C.: The evaluation of continuous fetal heart rate monitoring in high-risk pregnancy, AM. J. OBSTET. GYNECOL.
125:310,
8.
1976.
2. Renou, P., Chang, A., Anderson, trolled trial of fetal intensive
I., and Wood, C.: Concare, AM. J. OBSTET.
9.
3. Paul, R. H., and Hon, E. H.: Clinical fetal monitoring. V. Effect on perinatal outcome, AM. J. OBSTET. GYNECOL.
10.
GYNECOL.
1 l&529,
126~470,
1976.
1974.
4. Hibbard, L. T.: Changing trends in cesarean section, AM. J.OBSTET.GYNECOL. 125:798, 1976. 5. Paul, R. H., Suidan, A. K., Yeh, S-Y, Schifrin, B. S., and Hon, E. H.: Clinical fetal monitoring. VII. The evaluation and significance of intrapartum baseline fetal heart rate variability, AM. J. OBSTET. GYNECOL. 123:206, 1975. 6. Cibils, L. A.: Clinical significance of fetal heart rate patterns during labor. I. Baseline patterns, AM. J. OBSTET. GyNECOL. 125:290, 1976. 7. Mann, L. I.. Solomon, G., Carmichael, A., and Duchin, S.:
11.
12. 13.
The effect of metabolic acidosis on fetal brain function and metabolism, AM. J. OBSTET. GYNECOL. 111:353, I97 1. Shenker, L., Post, R. C., and Seiler, J. S.: Routine electronic monitoring of fetal heart rate and uterine activity during labor, Obstet. Gynecol. 46: 185, 1975. L&en, A. A.: Term intrapartum fetal death, AM. J. OBSTET.GYNECOL. 107:595, 1970. Kubli, F. W.: Influence of labor on fetal acid-base balance, Clin. Obstet. Gynecol. 11:168, 1968. Low, J. A., Pancham, S. R., Worthington, D., and Boston, R. W.: Clinical characteristics of pregnancies complicated by intrapartum fetal asphyxia, AM. J. OBSTET. CYNECOL. 121:452, 1975. Goodwin, J. W., Dunne, J. T., and Thomas, B. W.: Antepartum identification of the fetus at risk, Can. Med. Assoc. J. 101:458, 1969. Hobel, C. J., Hyvarinen. M. A., Okada, D. M., and Oh, W.: Prenatal and intrapartum high-risk screening. I. Prediction of the high-risk neonate, AM. J. OBSTET. GYNEcoL. 117:1, 1973.