Acta Obstet Gynecol Scand 58: 197-201, 1979

FETAL BREATHING MOVEMENTS AND MATERNAL EXERCISE Karel Margal, Olof Lofgren and Gerhard Gennser From ihe Deparimeni of Obssreirics and Gynecology, Allmdnna Sjukhusei, University of Lund, Malrnd, Sweden

Abstract. Earlier statements that fetal breathing movements

(FBM) are sensitive to changes in the fetal homeostasis prompted the study of the effect of maternal exercise on FBM and fetal heart rate. Forty women in the last trimester of gestation were subjected to a work load (80 W)for 5 min on a bed ergometer cycle; in 30 of them FBM were recorded by A-mode ultrasound, and in 10, the fetal heart rate was monitored by continuous ultrasound. Maternal blood pressure, pulse rate, blood pH and pC02, and transcutaneous PO, were also followed. The FBM showed a transient marked increase in incidence immediately after the end of the exercise. No changes in basal level or in baseline variability of the fetal heart rate were found in the recovery period after work. Some possible causes of the observed FBM alterations are discussed. The findings imply that, after this particular form of stress, FBM are a more sensitive indicator of the physiological state of the fetus than the fetal heart rate.

Our knowledge of whether maternal physical activity affects the human fetus in normal gestation is at present incomplete. Only few clinically normal pregnant women subjected to exercise tests have shown any changes in the fetal heart rate (14, 16, 24, 26, 27). It has been suggested that measurements of fetal breathing movements (FBM) in man provide a more sensitive indication of fetal physiological state than does fetal heart rate (FHR) (5). This concept has been supported by some observations on a&als (19,23) but was recently doubted in a study on sheep (29). The present investigation in uncomplicated human pregnancy studies the effect of a defined maternal work load on the FBM compared with that on the FHR.

MATERIAL AND METHODS Two groups of pregnant women participated in the study after giving their informed consent. All had singleton pregnancies with the fetal head in pelvic inlet. Group I. The effect of maternal exercise on FBM was examined in 30 women in the 30th-42nd (median 35th) gestational week. The pregnancy was normal in all respects in 27 women. two had mild cholestasis of pregnancy. and one

showed ABO-isoimmunization. The maternal age ranged from 19-38 (median 25.5) years; 19 of the women were nulliparae. Two women were subsequently delivered by elective cesarean section (indications: elderly primigravida; longstanding sterility). the rest by the vaginal route. Four were delivered by a low vacuum extraction - two because of acute fetal distress, the other two because of a prolonged second stage of labor. Group 11. In the second group of ten pregnant women, FHR was monitored in relation to maternal exercise, as, for technical reasons, FHR could not be continuously measured in Group I at the same time as the FBM. The maternal ages ranged from 18- 30 (median 25) years and the gestational ages from 32-37 (median 34) weeks; eight of the women were nulliparae. All ten women had an uneventful pregnancy and all were delivered vaginally at term. Low vacuum extraction had to be used at two deliveries because of acute fetal distress. All the women of both groups gave birth to clinically healthy infants. All the infants had Apgar score 2 7 . One was born before the end of the 36th week of pregnancy; all infants were appropriate for the gestational age according to the Swedish standards for singletons (28). One woman was delivered one day after the investigation; all the others had an interval greater than two days to delivery. All the women except one tolerated the work test without distress. The only exception was a woman with a normal pregnancy who was not included in the study group because measurement could not be carried out. She responded with painful, hypertonic uterine contractions and extreme tachycardia. This response lasted for 10 minutes; she subsequently delivered a healthy infant. The investigation was performed during the morning with the women in a semi-recumbent position. The work load, equivalent to 80 W,was achieved by exercise on a bed-type bicycle ergometer. Calibration of the cycle ergometer was controlled by measuring the oxygen uptake at steady state in two male volunteers when pedalling on three different occasions (mean oxygen uptake: 1 420 ml/min). The women were exposed to the work load for 5 min after a 30-minute control period. Recording continued for another 30 min after the exercise ended. FBM were monitored in Group I continuously by a modified A-mode echoscope (Ekoline 20, Smith Kline) as originally described by Boddy and Robinson (2). The records were evaluated according to the method given by Parmelee et 01. (22). The entire record was divided into 20-second pe riods and the FBM for each period were classified in one of four patterns - regular, irregular, periodic and apneic. The Acta Ohtet Gynccol Scand S8 (1979)


K . Marfal et al.

rnW 20 10





finger tips for 30 sec in a warm water bath. Maternal pH and pC0, in capillary blood were estimated by conventional electrodes (Instrumentation Laboratory Inc., Boston, Ma., USA). The maternal transcutaneous PO, (Tc-PO,) was measured in 14 women of Group I by a Radiometer TCM 1 unit. TcPO, (mm Hg) and energy supply to the electrode (mw), necessary to keep a constant temperature (44.5" C), were continuously recorded. The Tc-p02 electrode was Clark type, modified according to Huch (15). With this device, the correlation between arterial PO, and Tc-PO, in adults, measured at the electrode temperature of 44.5" C (within 0.1" C)was found to be highly significant (r = 0.95). The mean difference between arterial PO, and Tc-pO, was 16.5 mm Hg (SD f 11.9) (LOfgren. 1977 - to be published). The electrode was attached to the skin in the subclavicular area with a double-adhesive tape. After a stabilization time of about 15 min, the recording was begun. The records were evaluated manually - the mean of Tc-pO, values and ofrelative levels in energy supply were calculated for every 5-minute period. Statistical evaluation was made by Student's t-test based on intra-individual differencies and by correlation analysis.


m m Hg

- 10




30 rnin

Fig. I. Maternal transcutaneous PO, (Tc-pod and the rela-

tive energy supply to the Tc-PO, electrode during the exercise test. (14 of the women in Group I; Means f SEM for 5minute periods). The shaded area depicts the exercise period (0-5 min). The energy supply values for each woman are related to the zero point at the start of the exercise.

percentage of time for which each of the FBM patterns was present was calculated for every 5-minute period. All records were analysed by one of the authors (K.M). Maternal breathing was monitored by a thermistor applied to one nostril for identification of any artifacts in the FBM records caused by transmitted maternal respiratory movements. The echoscope used for the FBM measurements could not simultaneously record the FHR. Therefore the FHR in Group I was counted visually on the echoscope screen every second minute. In Group 11, the instantaneous FHR was followed continuously before and after the exercise by an ultrasonic Doppler cardiometer (Fetasonde 2100, Roche). (Accuracy of the cardiotachometer is reported by the manufacturer to be *2.5 per cent of full scale). The FHR traces were analysed manually for mean basal rate and baseline variability for every 5-minute period. During the exercise, the measurements of FBM and FHR could not be carried out as maternal movements dislocated the ultrasonic transducers being attached to the maternal abdomen. Maternal brachial blood pressure was measured every fifth minute. The results are presented as the mean arterial pressure calculated according to the formula (8): mean arterial pressure=

[systolic + 2 (diastolic pressure)]

Maternal heart rate was monitored continuously via conventional ECG chest electrodes. In 20 consecutive tests in Group I maternal capillary blood was sampled on three occasions: 10 min before the load, immediately after, and 15 min after the end of the load. The capillary blood was arterialized by dipping the Acta Obstet Gynecol &and 58 (1979)

RESULTS Group I. The pregnant women responded to the work load with a significant rise in heart rate. The maternal tachycardia was maximum during the exercise and persisted for the next 25 minutes. There was also an elevation in maternal mean arterial pressure, but this persisted only during the work (Table I). The maternal Tc-PO, was stable in the control period; it rose during the exercise to reach the maximum level in the first 5 min after the end of the exercise (p < 0.001) (Fig. 1). Thereafter, Tc-PO, declined slowly and reached the control level 30 min after the exer-

Table I. Maternal heart rate (beats per min) and maternal mean arterial pressure (mm Hg) during the exercise test. (Group I; exercise period 0 - 5 min, n = 30). Min from start _______~






_________~~ ~

A. Maternal heart rate beatshin, mean 88 SEM f 0.7 Sign of diff t P 8. Mat. art. pressure mm Hg, mean 87 SEM 0.7 Sign of diff t P




131 98 95 4.3 f 2.9 2.2 10.728 4.456 4.760 < 0.001 < 0.001 < 0.001



106 91 f 1.7 1.8 11.164 1.871 < 0.001 n.s.


87 i 1.6



Fetal breathing movements DH

The changes in pH, pC02, Tc-pO2, and the energy supply between the control period and the period immediately after the end of exercise did not correlate with the changes in the incidence of irregular FBM (r = 0.22, r = 0.01, r = 0.45, andr = 0.50, respective-

PCO2 rnrn H g





ly). 60 . 7L5







735 30 -

V 7 3c I





The work caused no perceptible change in the FHR when intermittently recorded. The mean FHR before and immediately after the exercise was 140 f 0.4 and 140 1.3 beats per min, respectively. Group 11. The maternal circulatory response to the exercise was similar to that of the women in Group I. The maternal heart rate rose significantly from 83 to 139 beats per rnin during the exercise and returned successively to the control levels after 20 min. The mean arterial pressure of the women increased transiently from 86 to 106 mm Hg. No significant difference in the basal level of the FHR or its baseline variability was detectable between the pre- and post-exercise continuous recordings (Table 11).





20 rnin

Fig. 2. Values of pH and pC0, in maternal capillary blood before and after the exercise test in 19 of the women in Group I. (Exercise period 0 - 5 min).

cise. The corresponding energy supply to the Tc-pO2 electrode increased to a maximum during the maternal exercise (p < 0.001) and returned to the control level 10 min later (Fig. 1). Mean pH of the arterialized capillary blood in the control period was 7.45 f 0.01 ( * SEM) (Fig. 2). Immediately after the exercise, pH had fallen significantly (p < 0.001) to 7.41 rf: 0.01 and returned 15 rnin later to the control level (7.44 rt 0.01). The mean capillary pC02 in the control period was 33.5 f 0.6 mm Hg. A slight non-significant increase occurred at the end of the maternal exercise (34.6 i 0.7 mm Hg); 15 min later, the pC02 level had decreased to 32.1 rt 0.7 mm Hg (Fig. 2). The pattern of FBM was marked altered by the work test. The exercise period was immediately followed by a profound reduction of the relative incidence of apnea (p < 0.001) and of periodic breathing (p < 0.001) and by an increase in the incidence of irregular breathing (p < 0.001) compared with that of the control period. The alteration of the fetal breathing patterns subsided gradually and had disappeared 15 rnin after the exercise (Fig. 3). No difference in fetal response was noted between primi- and multigravidae; nor between two women who were more than 35 years of age and the entire group.

DISCUSSION The present study demonstrated a pronounced transient increase in the incidence of FBM after a short period of moderate maternal exercise. The incidence of FBM in the control period was in good agreement with that in earlier reports on normal pregnancy (12, 18). The marked acute effect of moderate exercise on

Table 11. Fetal heart rate (beats per min) measured continuously before and qfter exercise. (Group II; exercise period 0 -5 min, n = 10). FHR could not be registered during the exercise for technical reasons (see text). Min from start Parameter





A. Fetal heart rate Baseline level, mean 139 f SEM f 3.2 Sign of diff: t

138 f 2.7 0.689

139 f 2.7 0.495

140 f 2.6



0.909 n.s.



15 1.3 0.263

16 1.3 0.780





B. Fetal heart rate Baseline variability, mean 15 f SEM f 0.8 Sign of diff: t


15 f 1.0


Acta Obstet Gynecol Scand 58 (1979)

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cating the uterus during the test and transmitted to the fetus are one possible mechanism. Boddy (6) rea cently reported that palpation of the uterus decreased 4! the FBM in man, whereas, on the other hand, tactile stimulation to fetuses of small laboratory animals (7) and painful irritation to lamb fetuses (25) evoked FBM. The fetal response might be influenced by the activation of the adrenergic nervous system (1 1) and the pituitary-adrenal axis (1) occurring during physical strain. Thus, in monkeys (20)and in sheep (23)infusion of catecholamines increased FBM, and plasma levels of ACTH in the latter species have been shown to be inversely related to the incidence of FBM (4). Adaptation of the maternal circulation to exercise manifested by tachycardia and increased blood pressure might affect the placental perfusion by a redistribution of blood flow. It is in this context relevant to recall one of the few studies of uterine circulation performed on conscious pregnant women. Morris et a1 (21) reported that, after a decrease during the course of maternal work, an increase in total uterine blood flow above the control level occurred during the first five min after exercise. But these investiga-30 -IS 0 IS 30 min tors could not differentiate between changes in myoFig. 3. Distribution of fetal breathing movement patterns metrial and placental blood perfusion. A subsequent during the exercise test in 30 pregnant women. (Group I; study on pregnant ewes has shown that a shift of Means f SEM for 5-minute periods). The shaded area de- blood flow from the uterine wall to the placenta was picts the exercise period (0 - 5 min). present immediately after maternal exercise (9).Such circulatory adaptions to work are possibly uncoupled FBM in normal pregnancies is of importance in view by an altered acid-base balance or changes in blood of the fact that the work load did not affect either the gas tensions. The cycling exercise caused a fall in mabasal level or the baseline variability of FHR. The ternal blood pH, whereas the pCOz was virtually unpresent results agree well with the reports by Hon and changed at the end of the exercise period. At this Wohlgemuth (14)and Stembera (27) which demon- point, the oxygenation measured as Tc-pOz had strated no, or only slight, FHR changes after step-test reached its highest level. It has been demonstrated in uncomplicated pregnancies. However, Pomerance that mild hypercapnia, with or without concomitant et al(24) showed that in 9 per cent of normal preg- hyperoxemia, decreased the porcine uterine vascular nant women, a reduction in FHR of more than 16 resistance (13), and isolated increase of the C02 tenbeats per minute followed a bicycle ergometer test at sion in fetal blood stimulated to increased FBM in a load level similar to ours. The present fiidings con- sheep (3). It is also of some interest to note, in view of firm the greater reactivity to various stimuli of FBM the observation that in sheep the presence of the FBM compared with FHR. This has also been demon- is associated with a certain pattern of the fetal electrostrated in human fetuses after maternal smoking (12) corticogram (lo), that induced acidosis caused a deor in chronic distress (5). Similar results were re- creased over-all amplitude and a disappearance of ported from experiments on Rhesus monkeys (19) fast rhytms in the electrocorticogram of fetal lambs and sheep (23).Thus, an abnormal pattern of FBM in (17). lambs for 30 hours before intrauterine death was acIt is not possible from the data available in the companied by normal FHR (23). present study to clarify the mechanism(s) responsible Clearly, several factors might play a part in media- for the transient alteration of the FBM. However, ting the alteration of the FBM. The mechanical this work showed that moderate exercise in normal stimuli from the maternal muscular movements dislo- gestation is a more powerful stimulus to the fetal

5 i

oi time lor

Aeta Obstet Gynecol &and SB (1979)

Fetal breathing movements breathing system than t o the cardiac centers. The observation suggests that, in some situations, the monitoring of FBM might constitute an investigative clinical method for supervision of the fetus with a higher resolution power than hitherto offered by the study of the FHR.

14. Hon, E.H. & Wohlgemuth, R.: The electronic evalua-


16. ACKNOWLEDGEMENTS The authors thank Mrs. Eva Eriksson, Miss Ann Thuring, and Mr. Arne Bjuvholt for expert technical help. We are grateful to colleagues from the Department of Clinical Physiology, University of Lund, Allmilnna Sjukhuset, MalmO for laboratory analysis and valuable discussions. Supported by grants from the Swedish Medical Research Council (B77-17x445 17-03), the Swedish Tobacco Company and the Medical Faculty of the University of Lund. REFERENCES 1. Bellet, S., Roman, L. & Barham, F.: Effect of physical exercise on adrenocortical secretion. Metabolism 18:484, 1969. 2. Boddy, K. & Robinson, J.S.: External method for detection of fetal breathing in utero. Lancet 2:1231,1971. 3. Boddy, K., Dawes, G.S., Fisher, R., Pinter, S. & Robinson, J.S.: Foetal respiratory movements, electrocortical and cardiovascular responses to hypoxaemia and hypercapnia in sheep. J Physiol243.599, 1974. 4. Boddy, K.,Jones, C. & Robinson, J.: Correlations between plasma ACTH concentrations and breathing movements in foetal sheep. Nature 250375, 1974. 5. Boddy. K. & Dawes, G.S.: Fetal breathing. Brit Med Bull 31.9, 1975. 6. Boddy, K.:Fetal circulation and breathing movements. In Fetal physiology and medicine (eds R.W. Beard, P.W. Nathanielsz), pp. 302-328. W.B. Saunders Comp. Ltd, London, 1976. 7. Bonar, B.E., Blumenfeld, C.M. & Fenning, C.: Studies of fetal respiratory movements. I. Historical and present day observations. Am J Dis Child 55:1, 1938. 8. Burton, A.C.: Physiology and Biophysics of the circulation, p. 86. Year Book Medical Publishers Inc., Chicago, 1%5. 9. Curet, L.B., Orr. J.A., Rankin, J.H.G. &Ungerer, T.: Effect of exercise on cardiac output and distribution of uterine blood flow in pregnant ewes. J Appl Physiol 40:725, 1976. 10. Dawes. G.S., Fox, H.E., Leduc, B.M., Lagins, G.C. & Richards, R.T.: Respiratory movements and rapid eye movement sleep in the foetal lamb. J Physiol220:119, 1972. 11. Euler, U.S. von & Hellner, S.:Excretion of noradrenaline and adrenaline in muscular work. Acta Physiol Scand 26:183, 1952. 12. Gennser, G., MarW K. & Brantmark, B.: Maternal smoking and fetal breathing movements. Am J Obstet Gynecol I23:861, 1975. 13. Hanka, R., Lawn, L., Mills, I.H., Prior, D.C. & Tweeddale, P.: The effects of maternal hypercapnia on foetal oxygenation and uterine blood flow in the pig. J Physiol247:447, 1975.



18. 19. 20.

21. 22.

23. 24. 25.



28. 29.

tion of fetal heart rate. Am J Obstet Gynecol 81:361, 1961. Huch. R., Huch, A. & Lubbers, D.W.: Transcutaneous measurement of blood PO, (tcP03 - method and application in perinatal medicine. J Perinat Med 1:183, 1973. Kuhlmann, G.. Mosler. K.H. & Schwalm, H.: Fetale Herzfrequenz und Wehenttitigkeit nach Ergometerbelastung von gesunden Schwangerenam Tragzeitende. Z Geburtsh Perinat 178279. 1974. Mann, L.I., Solomon, G., Carmichael, A. & Duchin, S.: The effect of metabolic acidosis on fetal brain function and metabolism. Am J Obstet Gynecol 111:353, 1971. Manning, F.A. & Feyerabend. C.: Cigarette smoking and fetal breathing movements. Br J Obstet Gyn 83262, 1976. Martin, C.B., Murata. Y., Petrie, R.H. & Parer, J.T.: Respiratory movements in fetal Rhesus monkeys. Am J Obstet Gynecol 119.939, 1974. Martin, C.B.: Factors affecting breathing movements in fetal rhesus monkeys. In Proceedings of the 3rd Conference on Fetal Breathing, MalmO, June 8. 1976 (eds G. Gennser, K Mar%, T. Wheeler), pp. 40-43, MalmO, 1977. Morris, N., Osborn, S.B., Wright, H.P. & Hart, A.: Effective uterine blood flow during exercise in normal and pre-eclamptic pregnancies. Lancet 2:481, 1956. Parmelee, A.H., Stern, E. & Harris, M.A.: Maturation of respiration in prematures and young infants. Neuroptidiatrie 3:294, 1972. Patrick, J.E., Dalton, K.J. & Dawes, G.S.: Breathing patterns before death in fetal lambs. Am J Obstet Gynecol 125:73, 1976. Pomerance, J.J., Gluck, L. & Lynch, V.A.: Maternal exercise as a screening test for uteroplacental insufficiency. Obstet Gynecol44.983, 1974. Scarpelli, E.M., Condorelli, S.& Cosmi, E.V.: Cutaneous stimulation and generation of breathing in the fetus. Pediat Research 11:24, 1977. Soiva. K.. Salmi, A.. GrOnroos, M. & Peltonen, T.: Physical working capacity during pregnancy and effect of physical work tests on foetal heart rate. Ann Chir Gynaecol Fenn 53:187, 1964. Stembera, Z.K.: Fetal tolerance to maternal exercise hypoxia. In Perinatal factors affecting human develop ment, Scientific Publication No. 185, pp. 105-110. Pan American Health Organization, Washington, 1%9. Sterky, 0.: Swedish standard curves for intra-uterine growth. Pediatrics 46:7, 1970. Toubas, P.L., Monset-Couchard, M., Rey, P.. Predine. J.. Verbrugge, M., Leandri, J. & Tchobroutsky. C.: Fetal breathing and adaption to maternal haemorrhage in the sheep. Am J Obstet Gynecol 127505, 1977.

Submitted for publication October 28, I977

Karel MarW Department of Obstetrics and Gynecology AllmPnna Sjukhuset S-214 01 MalmO

Fetal breathing movements and maternal exercise.

Acta Obstet Gynecol Scand 58: 197-201, 1979 FETAL BREATHING MOVEMENTS AND MATERNAL EXERCISE Karel Margal, Olof Lofgren and Gerhard Gennser From ihe D...
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