Human fetal breathing activity during electively induced labor at term BKYAN
Human fetal breathing movements were measured during the first stage of electively induced labor in 20 healthy term pregnancies. Fetuses made breathing movements 25.6% of the time during a 1 hour control period and breathing decreased significantly to 8.3% during latent-phase labor and further decreased to 0.8% during active labor (P < 0.001). Patterns of increased fetal breathing activity accompanied by increased gross fetal body movements and increased fetal heart rate variability for periods of 20 to 60 minutes out of every 1 .O to 1.5 hours were observed, and the intermittent patterns of increased body movement and heart rate variability continued throughout the first stage of labor despite the decrease in fetal breathing activity during latent- and active-phase labor. It will be important to account for rest activity patterns when interpreting variability of heart rate during labor. The absence of fetal breathing activity during electively induced labor at term is not a clinical indicator of fetal ill health. (AM. J. OBSTET. GYNECOL. 133:247, 1979.)
FETAL BREATHING movements may be an indicator of fetal health during human pregnancy.’ Human fetuses make episodic, rapid, irregular breathing movcments about 30% of the time when observed with real-time ultrasonic scanners.2m” Patterns in fetal breathing activity have been described and factors such as time of day, relationship to maternal meals, maternal glucose concentrations, cigarette smoking, and administration of drugs to mothers have been shown to affect fetal breathing activity.‘. :j. z. 6 A decrease in human fetal breathing activity within 72 hours of spontaneous labor at term was reported by Boddy,” using an A-scan ultrasound technique. He also reported a decrease in fetal breathing activity during normal labor. If fetal breathing movements are to become a useful indicator of fetal health it will be important to document biologic patterns and factors normally influencing fetal breathing activity. The purpose of this stud!
0 1979 The C. V. Mosby
was to define the range of fetal breathing activity during electively induced labor at term, with the use of a real-time ultrasonic scanner, and to determine factors which might influence fetal breathing activity during labor.
Methods Patients. Informed consent was obtained from 20 pregnant women admitted to the hospital at 38 to 42 weeks’ gestational age for elective induction of labor at term. Eighteen patients were considered in good health. One patient had mild pre-eclampsia and another patient, with a past history of chronic hypertension, had been treated with methyldopa throughout pregnancy. Eleven women were pregnant for the first time and the remaining nine had been delivered of 12 term pregnancies. Fetal outcome confirmed gestational age and the good health of fetuses studied (Table I). Fetus No. 16 was a breech presentation and all others were vertex. None of the fetuses developed fetal distress during labor. Patient No. 8. who had a failed Syntocinon induction, was delivered by cesarean section for cephalopelvic disproportion after a second Svntocinon infusion. All other fetuses were delivered vaginally. Experimental design. All studies began between 07:OO and 14:00 hours. Patients were studied for a 1 hour control period prior to induction of labor and then at intervals throughout the first stage of labot
Table Pt. No.
1 2 3 4 5
9 10 11 12 13
I. Clinical Gd. age (4
Umbilical PO, (mm 43
41 48 41 39 26 47-
7.31 7.32 7.31 7.31 7.43 7.24
20.3 24 20
-5.5 -2 -5.8 -6.2 -5.5 -7.5 -
16.7 19.6 12 19 16.2
7.29 7.32 7.32
20 16.7 17
7.39 7.27 7.23
18.5 14.3 10.6
7.28 0.07 0.02
17.7 3.3 0.78
9 10 10 9 109
19 15 23 20 18
$ 270 480
4,240 2,860 2,880 2,540
54 43.5 42 33 33.5 30.5 32 26
41% 41 38
42 40% 39%
.4pgar (score) (5 min)
Duration jirst stage of labor (min) 3,800 3,770 4,600 2,980 3,360 4,290 3,350
data of fetal outcome
170 255 105 405 375 270 285
40 41% 42 40 39 41% 42
42 40 41 40 42
90 1090 180 345 360 235
2 10 240 360
Mean SD SEM
3,210 3.040 3,350 3,350 3,050 2,750 3,070 3,150 2,650
9 Y 8 Y 9 Y 8
21 20.5 28.3 15 43
- 13.0 -6
-15 -10 -11.8 -6 -8 -8 -5 --11.6 -15.6 -8.4 3.8 0.93
*Mild pre-eclampsia. t Chronic hypertension. f Cesarean section. (Fig. 1). Labor was induced by artificial rupture of membranes in 14 patients and Syntocinon infusion in five. Patient No. 16, with a breech presentation, had spontaneous onset of labor. No sedative or analgesic medication was used during the study. Continuous epidural infusions were used for pain relief during labor in 17 patients. Three patients required no pain relief. Patients were instructed to fast from midnight the day before the study and were given a clear fluid diet ad libitum during the study period. A continuous infusion of 3.3% dextrose and 0.3% sodium chloride at 125 ml/hour was given during the entire study period. Free-flowing venous blood was sampled at intervals throughout the study period and piaced in tubes containing 14 mg of potassium oxaloacetate and 17.5 mg of sodium fluoride. At the end of each study. plasma was analyzed as a batch b) the Hoffman method of ferricyanide reduction in an AutoAnalyzer Model I. The coefficient of variation for the assay was 1% Samples of venous blood were taken at intervals for determination of blood gas and pH. Samples were collected in heparinized syringes and transported on ice to a laboratorv for immediate analysis.* *Model BMS 3 Mk 2, Blood Microsystem, Radiometer Corporation, Copenhagen, Denmark.
Patients were monitored when possible with an intra-amniotic pressure catheter and fetal scalp clip after rupture of the membranes. The pressure catheter was hydraulically coupled to a strain-gauge pressure transducer* and the signal, after amplification with a low-level DC preamplifier and a driver amplifier, was recorded on a polygraph chart rec0rder.t The electrocardiogram, after amplification with an EEG preamplifier and a driver amplifier, was recorded on a polygraph chart rec0rder.t In addition, a pen recording of instantaneous heart rate was obtained after amplification with a tachograph preamplifier and driver amplifier.? Analysis of fetal breathing movements. Observations of fetuses were made with an ADR real-time ultrasonic scanner.3 The transducer operated at a frequency of 3.5 MHz with an average intensity of 0.045 mW/cm2 and was held by a device developed in our laboratory. Images present on the display screen were viewed on an 11 inch video monitor. Individual fetal breathing movements were identified on the video monitor and coded on a chart re*Model P23, Statham Strain Gauge Pressure Transducer, Statham Instruments, Inc., Oxnard, California. tGrass Instruments, Quincy, Massachusetts. *Model 2130, Advanced Diagnostic Research Corp., Tempe, Arizona.
Fetal breathing during induced labor
1 CONTROL PERIOD
‘. t 0
PRELAiENT LATENT ACTIVE PHASE OF ~ABOUR ,‘. ,,. .. ” ,. TIME
’ ‘. ,,. :.
: . :
.;::, .5. .. .,
t ARM or SYNTDCINCN
Fig. ing and the into
ACTIVE PHASE LABOUR
LATENT PHASE LABOUR
2. Mean percentage time spent breathing (? SEM) durcontrol period, prelatent-phase labor, latent-phase labot-, active-phase labor. Five patients were not studied during 1 hour control period and several patients went directly latent- or active-phase labor following induction.
previously described and validated.” rate of successive fetal breathing sured
of a technique
The instantaneous movements was mea-
bv a second event marker.
on a chart
Fig. 3. Percentage time spent breathing and percentage time spent making gross body movements of fetus No. 14 were plotted in 15 minute intervals. During the control period and prelatent-phase labor, episodes of breathing activitv occurred during episodes of increased gross fetal hody movements. During latent- and active-phase labor episodes of gross fetal body movements continued every 60 to 90 minutes. but fetal breathing movements were absent.
CONTROL PRELATENT PERIOD PHASE LABOUR
250 fetal re-
Measurements of time during which fetuses made breathing movements did not include episodes of apnea or gross fetal body movements. Apnea was defined as the absence for 6 seconds or more
fetal breathing did not include
gross fetal body movements. Gross fetal body mol-ements were identified as fetal activity sufficient to 1)1-event recognition of fetal breathing movements. Mean fetal respirator) rates were derived from measurements of rate made every 30 seconds during fetal breathing episodes. Portions of records which could not be analyzed due to technical failure or patient interruption
as fail time.
in the time
February Am. J. Obstet.
Richardson, Natale, and Patrick
t T 180 Fig.
1. 1979 Gynecol.
4 180 minutes
labor during a time of increased gross fetal body movement and increased fetal breathing activity. At this time uterine activity was minimal. Arrows indicate gross fetal body movements. induction
surements of fetal breathing movements, gross fetal body movements, and apnea were calculated for each of the following time intervals: Control period. A 1 hour period of observation immediately prior to the induction of labor. Prrlatent-phase labor. The period of observation from induction of labor until the onset of regular uterine activity as determined subjectively by the patient or objectively by intra-amniotic pressure catheters. Latent-phnx labor. The period of observation time from onset of regular uterine contractions until active-phase labor as determined by the Friedman curve.’ Act&-phase labor. The period of observation beginning with the onset of active labor delined by the Friedman curve until full dilatation of the uterine cervix. Results presented represent grouped means and standard error of the means for each observation period. Significance was determined by the use of a t test for small samples with variances not assumed to be equal as described by Bailey,’ with confidence limits based on Student’s t distribution. Results Continous observation of fetal chest and abdominal wall echoes with the real-time scanner resulted in rec-
ognition of fetal breathing movements and gross fetal body movements as previously described by Patrick and associates.4 Human fetal breathing movements, both during the control period of observation and after initiation of labor, were episodic and chest wall movement during individual fetal breaths was variable in amplitude. The mean rate of fetal breathing movements during episodes of breathing was 47 breaths/ minute and was not significantly different during breathing episodes in the control period or those following induction of labor. The mean percentage time spent breathing during the 1 hour control period of observation was 25.6% t 5.1% (range 1.3% to 71.4%‘) (Fig. 2). During the prelatent phase of labor, the mean percentage time spent breathing was 13.7% rt 3.8’%, which was not significantly different from the control hour. The mean time spent breathing during the latent phase of labor was 8.3% + 2.3%. which was significantly less than during the control period prior to induction (P < 0.01). During active labor fetuses made breathing movements 0.8% 2 0.4% of the time, which was significantly less than both the control period (P < 0.001) and the latent phase of labor (I’ < 0.01). Gross fetal body movements observed consisted of fetal rolling movements, fetal stretching movements,
Fetal breathing during induced labor
TIME (minutes) t
T 210 Fig. 5. Chart recording of patient demonstrates that there was very fetal body movements.
No. 4 taken 30 minutes following record shown in Fig. 4, which little fetal heart rate variability during a time of absence of gross
TIME (minutes) l-300 Fig. 6. Chart recording of patient No. 4 taken 90 minutes following record shown in Fig. 5 taken during active labor. Heart rate variability was increased during a time of increased gross fetal body movements despite the absence of fetal breathing activity. Arrows indicate gross fetal body movements.
February 1, 1979 Am. J. Ohstet. Gynecol.
Richardson, Natale, and Pakick
Table II. Epidural spent breathing
Before or without efidural anesthesia
Latent-phase labor Active-phase labor
8.7 t 2.4
N = 15 2.2 2 1.0 N = IO P < 0.0.5
Table III. Syntocinon breathing
Latent-phase labor Active-phase labor
1.8 2 1.5 N=3
P < 0.05
O.lti 2 0.1 N= 16 NS
7.2 k 2.9
N= to 1.3 _f 0.8 N= to NS
Table IV. Ruptured time spent breathing
Latent-phase labor Active-phase labor
Before or without Syntocinon
18.4 * 9.2 N=4
1.0 ? 0.6 N=?J NS
(1.1; z 08.1 NS P < 0.05
5.5 2 1.8 N= 14 0.8 t 0.4
N= 18 P < 0.05
and isolated movements of fetal extremities. These three types of gross fetal movement occurred both during the control period of’ observation and after induction of labor. The mean percentage time spent making gross fetal body movements during the control period was 8.3!1( ? 1.5%‘. This was not significantly different during prelatent-phase labor (6.OY i- 2.1 ‘P) or during latent-phase labor (.?.3CV ? 1.65i;). During active labor. fetuses made gross body movements 2.9% i 0.7% ot the time, and this was significantly less than during the control period of observation (P < 0.01). Hiccough-like movements as described previously b) Patrick and associates4 were observed in LOUI. fetuses. I‘hese movements were readil?- distinguished from typical fetal breathing movements h!, rapid large inward and outward movement of fetal chest wall echoes. The mean length of hiccough episodes ~caj 9.8 minutes (range 1.1 to 6.7 minutes). Episodes of hiccoughs were observed during the control pex-iod and during latentphase labor.
Analysis of fetal breathing activity in some patients revealed that during the control period of observation and during labor a periodic pattern of breathing activity became apparent. This was characterized by an increase in fetal breathing activity accompanied by increased gross fetal body movements for periods of 20 to 60 minutes out of every I .O to 1.5 hours of observation time (Fig. n). As labor progressed, there was a decrease in the total amount of fetal breathing activit). but the occurrence of breathing activity maintained a periodic pattern. During well-established labor, onl) fetal apnea esisted. A similar pattern occurred in gross tttal body tnovetnents; however, this pattern of periodic increase in gross fetal body movements was maintained throughout active labor. Fetal heart rate \,ariability also followed a pattern in some patients. Heart rate variability was usually increased during observation periods in which increased fetal breathing activity and gross fetal body movements were observed. During episodes of gross fetal body movement the fetal heart rate was often seen to inclease. During times of decreased or absent fetal breathing activitv and absence of gross fetal hod) movement, fetal heart rate variability was diminished. Chart recordings of fetal breathing movements, gross fetal body tnox~etnents. intra-amniotic pressure, and fetal heart rate in fetus No. ,I are presented in Figs. -l to 6. Fig. -I illustrates that during early label-. with minimal uterine activity. significant fetal heart rate variabilit) occurred during a time of increased fetal breathing activity and gross fetal body movements. Fig. 5 illustrates that 30 minutes later in the same fetus, during a time of absence of fetal breathing movements and gross fetal hod! movements, there was very little fetal heart rate variability. Fig. 6 illustrates, in the same fetus 90 minutes later, that during active labor fetal heart rate variability was increased during a time of increased gross fetal boil> movements despite the absence of fetal breathing activity. Occasional heart rate changes best described as variable decelerations” occurred in patients Nos. 3, 6. 13, and 19 during the last 20 to 40 minutes of first-stage labor. Patients Nos. 9 and 18 both had early and variable heart rate decelerations during the last 50 to 60 minutes of first-stage labor. No fetal breathing activity was observed during these decelerations. During this study no late fetal heart Iate decelerations were recorded. There was no statistically significant change in maternal glucose values throughout the study. Mean maternal venous plasma glucose concentrations were 79.2 2 3.1 mg/lOO ml during the control hour, 95.0 ? 7.3 mg/lOO ml during prelatent-phase labor, 90.1 ?
7.4 mg/lOO ml during latent-phase labor, and 85.0 ? 4.6 mgi100 ml during active-phase labor. The mean umbilical cord venous plasma glucose concentration was 76.8 + 5.0 mgi100 ml. Mean maternal venous blood Pco? during the control period of observation was 28.2 ? 1.5 mm Hg and this was not significantly different from the mean venous blood Pco2 of 27.6 ? 1.3 mm Hg observed during active labor. Mean maternal venous blood pH was 7.43 i- 0.01 during the control period of observation and was unchanged during the active phase of labor. Epidural anesthesia for relief of pain was necessarily a function of increase in uterine activity (Table II). Although there was a significant decrease in fetal breathing activit!, during latent-phase labor before administration of an anesthetic or without epidural anesthesia, as compared to after epidural anesthesia, this was likely explained by an associated increase in uterine activity during the latent phase of labor. Only three patients required epidural anesthesia during the latent phase of labor, and in these patients the percentage time spent breathing before epidural anesthesia during the latent phase was 1.2% + 1.08,. After epidural anesthesia in these same patients the percentage time spent breathing was 1.8% * 1.5%. Furthermore, when noting only observation periods prior to or without epidural anesthesia, there was a significant decrease in fetal breathing activity during the active phase of labor despite the lack of an epidural analgesia. These data suggested that epidural analgesia was not, by itself, responsible for decreased amounts of fetal breathing activity observed during labor. Administration of Syntocinon had no apparent direct effect on fetal breathing activity. Fetal breathing activity did not change significantly during either latent- or active-phase labor before or without Syntocinon as compared to after Syntocinon (Table III). Patient No. 8, who had a failed Syntocinon induction, had fetal breathing activity which averaged 13.4% over a 3 hour observation period while receiving up to 20 mU of Syntocinon per minute. Artificial rupture of membranes also did not appear to directly influence fetal breathing activity. The mean percentage time spent breathing did not change significantly during either latent- or active-phase labor before ruptured membranes as compared to after rupture of membranes (Table IV).
Comment This study demonstrated that fetal breathing activity changed significantly during electively induced labor at term. Fetuses made breathing movements 25.6% ? 5.1% of the time during the 1 hour control period and
breathing decreased significantly to 8.3% * 2.3% during the latent phase of labor (P < 0.01) and further decreased to 0.8% * 0.4% during active-phase labor (P < 0.001). These data suggested that the decrease in fetal breathing activity which occurred during labor was in some way related to an increase in uterine activity or to the progress of labor. The percentage of time spent making gross fetal body movements also decreased during labor. Gross fetal body movement decreased from 8.3% ? 1.5% during the 1 hour control period to 2.9% * 0.7%’ during active-phase labor (P < 0.0 1). However, gross fetal body movement during latent-phase labor did not differ significantly from that observed during the control period or the active phase of labor. These data suggested that the decrease in gross fetal body movements measured might also in some way be related to increase in uterine activity or to the progress of labor. Successive periods of increased fetal breathing activity and increased gross fetal body movements were separated by periods of decreased fetal breathing activity and decreased gross fetal body movements. These may have represented fetal rest activity patterns in utero. Patrick, Natale, and Richardson” reported periods of increased fetal breathing movement and increased gross fetal body movement lasting 20 to 60 minutes and occurring every 1.0 to 1.5 hours in 24 hour observations of pregnant women at 34 to 35 weeks’ gestational age. These authors suggested that this activity might be related to changes in fetal rest activity states. In the present study, periodic increases in gross fetal body movements continued throughout labor, although fetal breathing activity, which usually occurred during these times of increased fetal body movement, was virtually abolished during active labor. This suggested that the decrease of fetal breathing activity observed during active labor could not be explained by alterations in fetal rest activity patterns. Heart rate variability increased during periods of increased fetal breathing activity and increased gross fetal body movements. Dalton, Dawes, and Patrick”’ reported an increase in heart rate variability during breathing episodes in chronic fetal lamb preparations which occurred during low-voltage rapid electrocortical activity consistent with rapid eye movement (active) sleep. Throughout the present study successive periods of increased heart rate variability, during episodes of increased gross fetal body movement, were separated by periods of absence of heart rate variability during periods of decreased fetal body movement. Therefore fetal heart rate variability was directly related to fetal rest activity patterns. The intermittent changes in heart rate variability associated with fetal activity continued
Richardson, Natale, and Patrick
up to the end of first-stage labor despite the absence of fetal breathing activity during active labor. Maternal plasma glucose concentrations are known to affect human fetal breathing activit>.“. ‘. I’ In the present study there was no significant change in maternal plasma glucose values during labor. Therefore changes in maternal glucose concentrations did not account for the decreases in fetal breathing activit! observed. Boddy” has reported that absence of fetal chest wall movements might be related to maternal hyperventilation with a consequent reduction of fetal scalp PCO, during normal spontaneous labor. In the present study, there was no significant difference in maternal venous blood pH and Pcoy during the latent or acti\:c phase of labor when compared to the control period. Ylaternal venous Pc;02 during the control period was 2X.L? + 1.S mm Hg, which was similar to that reported IJ! ‘I‘owell” for maternal venous Pw, at term during early labor. Towell also reported no change in maternal Pcol throughout the first stage of labor-. Therefore maternal hyperventilation did not account fi)r the drcrease in fetal breathing activity observed during labelin this study. The use of epidural anesthesia and Syntocinon did not seem to account fbr the decrease in fetal breathing activity observed during labor. There is a significant decrease in fetal breathing activity during active-phase labor and the data did not suggest that either epidural anesthesia or Spntocinon infusion in any way alter-et1 this observation. Artificial rupture of membranes also did not account for the significant decrease in fetal breathing activity observed as labor progressed. The mechanism for decreased fetal breathing acti\ it! with progression of labor was not clear. Bodd!, and arsoci?tes”’ . ‘ reported a decrease in fetal breathing activitv in chronic fetal lamb preparations with acute hppoxemia. Towell” has stated that oxygen saturation values in human fetal scalp blood fall during labor, although the absence of’ metabolic acidosis at deliver\-
indicated that normal fetuses \\.ere able to compensate for mild oxygen deficiencies. ‘I’herefore decrease in oxvgen saturation of fetal blood during labor might have accounted f’or the decrease in fttal breathing activity. Anothei- explanation might be the effect of esternal stimulation on the fetus bv iticreaGrig uterine activity and increasing pressure of. the pelvic wall againsl the fetal presenting part. bIannin,g” has rcported that thermal or tactile stimulation of. fetal rhesus tnonke! tacial areas induced apnea and a similarmechanism might have esplained the ohser\ations of the present stud!. Periods of increased fetal breathing movements, gross fetal hotly movements, and fetal heart rate variability occurred “0 to 60 minutes ever\’ 1 to 1.5 hours and successive episodes were separated br. periods of absence of tttal breathing movements, decreased gross fetal bocl?, movements, ancl absence of fetal heart rate variability. The apparent rest activity patterns in gross letal hod!- movement and fetal heart rate variabilit) continued throughout labor but fetal breathing activity, which was normally observed during periods of increased gross fetal body movement. was significantl) decreased as labor progressed. It will be important to account ti)r these rest activity patterns when interpreting the wriabilit! of fetal heart rate tracings during labor. The clinical significance of human fetal breathing movements is not yet clear. This study &owed a significant decrease in fetal breathing activity during electi\,ely induced labor in healthy pregnant women at term. Thcrcfot-c the absetlce of fetal hreathing activity during electively induced labor at term is not ;I clinical indicator of fetal ill health. The authol,s wish to thank Dr. P. Harding and hlrs. K. (~at~~pbell for their interest in this work and Dr. M. Binns Smith, Miss L. Carmichael, Mrs. T. Clarke, bliss M. I.. Jones, and h,fl-. 1). Miller for their excellent technical assistance.
Boddy li. and Dawes. G. S.: Frtal brrathing.
Bull. 31:3, 1975. 2. Fox, H. E., and Hohler, C. W.: Fetal evaluation by I-ealtime imaging, Clin. Obstet. Gynecol. 20:339, 1977. 3. Manning, F. A.: Fetal breathing movements as a reHection of fetal statu?, Postgrad. Med. 61: 116, 1977. 4. Patrick, J., Fetherston, W., Vick, H., and Voegelin. R.: Human fetal breathing movements and gross fetal hod\ movements at 34-33 weeks gestational agr, A&l. J. OBSTET. GYNECOI.. 130:693. 1978. i. Patrick, J., Natale. R.. and Richardson, B.: Patterns ot
T. 8. 9.
human tetal breathing activity at 34 to 35 weeks gestational age, AM. J. OBSTET. GYNECOL. 132:507. 1978. Boddy, I