European Jourtml of Obstetrics & Gynecoiogv and Reproducrioe Biology, 40 (1991) 119- 122 0 1991 Elsevier Science Publishers B.V. 06i8-2243//$03.50
119
EUROBS 01135
The effect of maternal exercise on fetal umbilical artery waveforms N.M. Rafla and J.M. Beazely The Royal Liverpool Hospital, Prescot street, Liverpool, UK. Accepted for publication 31 October 1990
Summary
Twenty-one nulliparous women in the last trimester of pregnancy gave their informed verbal consent to undergo an acute exercise test. Fetal umbilical artery velocimetry waveforms were measured to monitor the effect of exercise on fetal umbilical artery blood flow. The mean gestational age was 32 weeks (range 28-37 weeks). The mean exercise intensity was 71% of submaximal exercise (range 67-74s). Maternal heart rate rose significantly (P < 0.001) from a mean of 83 to 138 beats per min. Following moderate exercise, the systolic over the diastolic ratio (S/D) decreased significantly (P c 0.001) after 2 and 20 min. This indicates a decrease in umbilical blood flow resistance and an improved placental circulation following exercise in healthy women. We conclude that maternal exercise does not appear to be harmful to the mother or her fetus at this level of exercise intensity in healthy individuals. Exercise; Doppler; Fetal blood flow
Introduction
In humans the effect of maternal exercise on fetal arterial blood flow using non-invasive techniques has only recently become possible. Previously, Morris et al. in 1956 [12] using a radioactive saline injected into maternal arteries, measured uterine blood flow during exercise. Investigations undertaken on humans showed that exercise is neither harmful to the mother nor her fetus [13,16] Jovanovic et al. in 1985 [7] on exercising 6 women in the third trimester using a bicycle ergometer found that 60-70s of submaxi-
Correspondence: Mr. N.M. Rafla, Consultant Obstetrician and Gynaecologist, Kent and Cantebury Hospital, Cantebury, Kent, CT1 3NG, U.K.
ma1 exercise does not appear to be harmful to the fetus. More recently, Kupla et al. in 1987 [lo] studied the effect of aerobic exercise at 75% of maximal heart rate on 141 pregnant women during the first and third trimester of pregnancy and found no associated increase in neonatal morbidity or obstetric complications. The aim of this study was to study the effect of maternal exercise on fetal blood flow, using a new, safe and non-invasive approach. Patients and Methods
The investigation was conducted on 21 healthy primigravidae in their third trimester of pregnancy. All patients gave their verbal informed consent to the study which was approved by the local ethical committee.
120
All patients abstained from smoking, coffee, alcohol and medications for at least 24 h prior to the test [4,6,8]. Iron supplements were permitted. The duration of each patient’s pregnancy was confirmed by an early ultrasound scan. The birth weight of each of the babies was appropriate for its gestational age. Prior to the test and during the recording of the umbilical artery velocimetry waveforms, the subjects rested in a semi-Fowler position with the head of the bed raised 30 degrees. The test was divided into three periods; a baseline control period of rest lasting 15 min; an exercise period lasting 5 min, during which the pregnant women exercised on an upright bicycle ergometer; and a recovery period lasting 30 min. Non-weight bearing exercise was the method of choice for exercise testing in pregnancy. Pedalling was at a constant 60 cycles per min and the ergometer work load was increased stepwise each min, until the patient achieved 70% of her submaximal exercise. Maximal heart rate was estimated by subtracting the subject’s age from 220
PI* To obtain a baseline control value, umbilical artery velocimetry waveforms were measured during the end of the rest period. Following exercise, measurement were made at intervals of 2,5 and 20 min. To record umbilical artery velocimetry waveforms, a linear array scanning model, SAL-50 A Toshiba 2.4 MHz, connected to a pulsed-Doppler unit, model SDL-OlA Toshiba with 3.5 MHz probe was used. Once a satisfactory velocimetry waveforms image was obtained, it was freeze-framed. The cursor was then moved, and the systolic ‘peak to diastolic ‘trough’ was calculated. All the measurements were obtained by the same observer (N.M. Rafla) to eliminate inter-observer error, which could possibly be up to 168, while Intraobserver error has been shown previously to be 6% by Bracero in 1986 [2]. Intraobserver error in this study was 6.3% [17].
achieved (range 67-741. Maternal heart rate increased significantly (P < O.OOl), from a mean of 84 beats per min at rest (range, 80-100) to a mean of 137 beats per min (range 130-1471. The results obtained after the exercise were compared with the baseline values, and the significance of changes observed was established using a paired t-test. Measurement of umbilical artery waveforms revealed a significant decrease (P -c 0.001) in the S/D ‘value following the period of exercise. Table I shows that the mean S/D ratio was 2.6 (0.33) at rest, 2.22 (0.33) after 2 min, and 2.36 (0.42) 20 min after exercise has ceased. This also was statistically significant (P -c 0.04). However, the decrease in the S/D ratio after 5 min was not statistically significant. See Fig. 1 for graphical display of these changes. In one of the patients the fetus showed no changes in umbilical artery velocimetry after the exercise, and the S/D ratio remained constant throughout. In another patient the S/D ratio increased by 12% following exercise, and returned to the pre-exercise level after 30 min. In the latter patient a fetal bradycardia of 90 beats per min was observed immediately following exercise but recovered within 2 min. (See Discussion). The increase in fetal heart rate following exercise was thnbilml artery blood flw
Results At
Within 5 min of exercise on a bicycle ergometer, a mean of 71% of submaximal exercise was
rert
5
mins
a
Fig. 1. The mean S/D ratios showed significant decrease following 2 and 20 min of recovery from exercise.
121 TABLE
I
The S/D
ratio before and after exercise for each woman.
At
2 sins
rest
5 mlns
20 m1ns
1
2.0
1.9
1.8
1.6
2
2.0
1.9
2.4
2.3
3
2.7
2.7
2.7
2.7
4
2.5
1.7
3.0
2.5
5
2.0
1.9
1.9
2.5
6
2.3
2.6
2.3
3.0
7
2.8
2.6
2.0
3.4
8
2.8
2.2
2.5
2.7
9
2.7
2.4
3.4
1.9
10
2.3
1.9
1.9
2.2
11
2.7
2.3
3.1
2.0
12
3.1
2.1
2.3
2.3
13
2.6
2.5
2.9
2.5
14
3.1
2.6
3.0
1.8
15
2.7
2.6
2.4
2.4
16
2.9
1.9
1.6
1.6
17
2.3
1.7
2.0
2.1
18
3.0
2.7
2.7
2.6
19
2.8
2.5
2.7
2.2
20
2.9
2.0
2.0
2.3
21
2.7
2.0
2.4
2.8
T.
2.6
X=
2.22
S
2.43
D
2.36
SD.
0.33
SD =
0.33
0 =
0.47
D-
0.42
tix*
54.9
IX * 46.7
x = 51
I=
49.6
not statistically sjgnificant and returned to normal within the 20 min of rest. Discussion The flow velocity is influenced by the ejection systolic pulse, arterial wall compliance, blood stream inertia and downstream peripheral resistance. If peripheral resistance is large then the pressure pulse wave travelling down the arterial tree is highly reflected and there is little flow into the capillary bed; hence diastolic velocity is small and the ratio of peak systolic to end diastolic flow is large [20]. Low resistance, however, allows onward travel of the pressure wave with little alteration and large diastolic flow results as in this study.
Since the umbilical arteries carry fetal blood to the placenta, umbilical artery waveform studies provide an indirect assessment of placental blood flow. Alterations in velocity are caused primarily by changes in resistance [21]. The S/D ratio examines the placental role in resistance to fetal umbilical artery velocity. A decrease in the S/D ratio of the umbilical artery waveform suggests a decrease in resistance and an increase in the fetal blood flow, as demonstrated by Trudinger and his colleagues in 1985 [21]. The relationship between exercise and placental resistance by measuring umbilical artery waveforms, to our knowledge, has not been previously tested in humans using this non-invasive technique, and at this level of exercise. However, Pijpers and his associates in 1984 [15] using mild exercise of 30% submaximal exercise, did not observe significant effect on fetal blood flow. In our study the intensity of exercise was 71% of submaximal exercise. Our findings are in agreement with previous animal studies, Dhindsa et al. in 1978 [3] found significant decrease in placental vascular resistance when he exercised five pregnant goats. Orr et al. in 1972 [14] measured the effect of exercise on uterine and iliac blood flow, using Doppler ultrasound on pregnant sheep and a found slight increase in uterine blood flow, and concluded that exercise is not hazardous to the fetus. In measuring the response to exercise, a history of previous exercise is important. Athletes have a different reference range from the rest of the population as shown by Rafla and Rumley [18,19]. In pregnancy it may be similar, and therefore the response to exercise may be different in the two groups. This may explain the results in the two patients mentioned above. In one of these, who was a highly trained athlete, the S/D ratio increased following exercise, and a transient fetal bradycardia was observed immediately following exercise. This athlete had to exercise harder to reach 70% of submaximal value, and the S/D ratio increased by 12%. In the second patient, who provided a history of regular jogging before and during pregnancy, no change in umbilical artery waveforms following exercise was observed. Mires et al. in 1987 [ll] demonstrated that the
122
S/D ratio decreases when fetal heart rate accelerates. Kofinas and his colleagues in 1989 [9] found that it is unnecessary to correct umbilical artery velocity waveforms for fetal heart rate. In our study the changes in fetal heart rates were not statistically significant and did not influence the significance of the effect of exercise on fetal blood flow. From this study it is concluded that exercise in pregnancy is not harmful to the fetus in healthy subjects and may improve placental circulation by decreasing placental vascular resistance. Healthy pregnant women who wish to exercise during pregnancy should not be discouraged. References Artal R, Wiswell RA, Exercise in pregnancy. Baltimore: Williams and Wilkins, 1986. Bracero L, Schulman H, Fleischer A, Farmakides G, Rochelson B. Umbilical artery velocimetry in diabetes and pregnancy. Obstet Gynaecol 1986;68:654-658. Dhindsa DS, Metcalfe J, Hummels DH. Responses to exercise in the pregnant pigmy goat. Respir Phys 1978;32: 299-311. Eriskine RLA, Ritchie JWK. The effect of maternal consumption of alcohol on human umbilical artery blood flow. Am J Obstet Gynecol 1986;154:318-21. Eriksen PS, Marsal K, Circulatory changes in the fetal aorta after maternal smoking. Br J Obstet Gynaecol 1987;94:301-305. Jouppila P, Kirkinen P, Eik-Nes S. Acute effect of maternal smoking on the human fetal blood flow. Br J Obstet Gynaecol1983;90:7-10. Jovanovic L, Kessler A, Peterson CM. Human maternal and fetal response to graded exercise. J Appl Physiol 1985; 58:1719-1722. Kirkinen P, Jouppila P, Koivula A, Vuori J, Puukka M. The effect of caffeine on placental and fetal blood flow in human pregnancy. Am J Obstet Gynecol1983;147:939-943.
9 Kofinas AD, Espeland M, Swain M, Penry M, Nelson L. Correcting umbilical artery flow velocity waveforms for fetal heart rate is unnecessary. Am J Obstet Gynecol. 1989;160:704-707. exercise in 10 Kupla PJ, White BM, Visscher R. Aerobic pregnancy. Am J Obstet Gynecol 1987;156:1395-1403. 11 Mires G, Dempster J, Pataf NB, Crawford JW. The effect of fetal heart rate on umbilical artery flow velocity waveforms. Br J Obstet Gynaecol. 1987;94:665-669. 12 Morris N, Osbom SB, Wright HP, Hart A. Effective uterine blood flow during exercise in normal and pre-eclamptic pregnancies. Lancet 1956;i:481-485. 13 Morton MJ, Paul MS, Campos GR, Hart MV, Metcalfe J. Exercise dynamics in late gestation: effect of physical training. Am J Obstet Gynecol. 1985;152:91-97. 14 Orr J, Ungerer T, Will J, Wemicke K, Curet LB. Effect of exercise stress on carotid, uterine and iliac blood flow in pregnant and non-pregnant ewes. Am J Obstet Gynecol 1972;114:213-217. 15 Pijpers L, Wladimiroff JW, McGhie J. Effect of short-term maternal exercise on maternal and fetal cardiovascular dynamics. Br J Obstet Gynaecol 1984;91:1081-1086. 16 Pomerance JJ, Gluck L, Lynch VA. Physical fitness in pregnancy: its effect on pregnancy outcome. Am J Obstet Gynecol 1974;119:867-876. 17 Rafla NM. The effect of maternal exercise on fetal and maternal blood flow in healthy and unhealthy women. Thesis submitted to the university of Liverpool, 1990. 18 Rafla N, Rumley AG. Clinical and biochemical changes during ninety hours of continuous basketball. Stand. J Sports Sci 1987;9:15-19. 19 Rumley AG, Rafla N. Serum enzyme changes during ninety hours of continuous basketball. Stand J Sports Sci 1983;5:45-49. 20 Schulman H, Fleischer A, Stem W, Farmakides G, Jagani N, Blattner P. Umbilical velocity wave ratios in human pregnancy. Am J Obstet Gynecol 1984;148:985-990. 21 Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins L. Fetal umbilical artery velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol 1985;92:23-30.
119
EUROBS 01135
The effect of maternal exercise on fetal umbilical artery waveforms N.M. Rafla and J.M. Beazely The Royal Liverpool Hospital, Prescot street, Liverpool, UK. Accepted for publication 31 October 1990
Summary
Twenty-one nulliparous women in the last trimester of pregnancy gave their informed verbal consent to undergo an acute exercise test. Fetal umbilical artery velocimetry waveforms were measured to monitor the effect of exercise on fetal umbilical artery blood flow. The mean gestational age was 32 weeks (range 28-37 weeks). The mean exercise intensity was 71% of submaximal exercise (range 67-74s). Maternal heart rate rose significantly (P < 0.001) from a mean of 83 to 138 beats per min. Following moderate exercise, the systolic over the diastolic ratio (S/D) decreased significantly (P c 0.001) after 2 and 20 min. This indicates a decrease in umbilical blood flow resistance and an improved placental circulation following exercise in healthy women. We conclude that maternal exercise does not appear to be harmful to the mother or her fetus at this level of exercise intensity in healthy individuals. Exercise; Doppler; Fetal blood flow
Introduction
In humans the effect of maternal exercise on fetal arterial blood flow using non-invasive techniques has only recently become possible. Previously, Morris et al. in 1956 [12] using a radioactive saline injected into maternal arteries, measured uterine blood flow during exercise. Investigations undertaken on humans showed that exercise is neither harmful to the mother nor her fetus [13,16] Jovanovic et al. in 1985 [7] on exercising 6 women in the third trimester using a bicycle ergometer found that 60-70s of submaxi-
Correspondence: Mr. N.M. Rafla, Consultant Obstetrician and Gynaecologist, Kent and Cantebury Hospital, Cantebury, Kent, CT1 3NG, U.K.
ma1 exercise does not appear to be harmful to the fetus. More recently, Kupla et al. in 1987 [lo] studied the effect of aerobic exercise at 75% of maximal heart rate on 141 pregnant women during the first and third trimester of pregnancy and found no associated increase in neonatal morbidity or obstetric complications. The aim of this study was to study the effect of maternal exercise on fetal blood flow, using a new, safe and non-invasive approach. Patients and Methods
The investigation was conducted on 21 healthy primigravidae in their third trimester of pregnancy. All patients gave their verbal informed consent to the study which was approved by the local ethical committee.
120
All patients abstained from smoking, coffee, alcohol and medications for at least 24 h prior to the test [4,6,8]. Iron supplements were permitted. The duration of each patient’s pregnancy was confirmed by an early ultrasound scan. The birth weight of each of the babies was appropriate for its gestational age. Prior to the test and during the recording of the umbilical artery velocimetry waveforms, the subjects rested in a semi-Fowler position with the head of the bed raised 30 degrees. The test was divided into three periods; a baseline control period of rest lasting 15 min; an exercise period lasting 5 min, during which the pregnant women exercised on an upright bicycle ergometer; and a recovery period lasting 30 min. Non-weight bearing exercise was the method of choice for exercise testing in pregnancy. Pedalling was at a constant 60 cycles per min and the ergometer work load was increased stepwise each min, until the patient achieved 70% of her submaximal exercise. Maximal heart rate was estimated by subtracting the subject’s age from 220
PI* To obtain a baseline control value, umbilical artery velocimetry waveforms were measured during the end of the rest period. Following exercise, measurement were made at intervals of 2,5 and 20 min. To record umbilical artery velocimetry waveforms, a linear array scanning model, SAL-50 A Toshiba 2.4 MHz, connected to a pulsed-Doppler unit, model SDL-OlA Toshiba with 3.5 MHz probe was used. Once a satisfactory velocimetry waveforms image was obtained, it was freeze-framed. The cursor was then moved, and the systolic ‘peak to diastolic ‘trough’ was calculated. All the measurements were obtained by the same observer (N.M. Rafla) to eliminate inter-observer error, which could possibly be up to 168, while Intraobserver error has been shown previously to be 6% by Bracero in 1986 [2]. Intraobserver error in this study was 6.3% [17].
achieved (range 67-741. Maternal heart rate increased significantly (P < O.OOl), from a mean of 84 beats per min at rest (range, 80-100) to a mean of 137 beats per min (range 130-1471. The results obtained after the exercise were compared with the baseline values, and the significance of changes observed was established using a paired t-test. Measurement of umbilical artery waveforms revealed a significant decrease (P -c 0.001) in the S/D ‘value following the period of exercise. Table I shows that the mean S/D ratio was 2.6 (0.33) at rest, 2.22 (0.33) after 2 min, and 2.36 (0.42) 20 min after exercise has ceased. This also was statistically significant (P -c 0.04). However, the decrease in the S/D ratio after 5 min was not statistically significant. See Fig. 1 for graphical display of these changes. In one of the patients the fetus showed no changes in umbilical artery velocimetry after the exercise, and the S/D ratio remained constant throughout. In another patient the S/D ratio increased by 12% following exercise, and returned to the pre-exercise level after 30 min. In the latter patient a fetal bradycardia of 90 beats per min was observed immediately following exercise but recovered within 2 min. (See Discussion). The increase in fetal heart rate following exercise was thnbilml artery blood flw
Results At
Within 5 min of exercise on a bicycle ergometer, a mean of 71% of submaximal exercise was
rert
5
mins
a
Fig. 1. The mean S/D ratios showed significant decrease following 2 and 20 min of recovery from exercise.
121 TABLE
I
The S/D
ratio before and after exercise for each woman.
At
2 sins
rest
5 mlns
20 m1ns
1
2.0
1.9
1.8
1.6
2
2.0
1.9
2.4
2.3
3
2.7
2.7
2.7
2.7
4
2.5
1.7
3.0
2.5
5
2.0
1.9
1.9
2.5
6
2.3
2.6
2.3
3.0
7
2.8
2.6
2.0
3.4
8
2.8
2.2
2.5
2.7
9
2.7
2.4
3.4
1.9
10
2.3
1.9
1.9
2.2
11
2.7
2.3
3.1
2.0
12
3.1
2.1
2.3
2.3
13
2.6
2.5
2.9
2.5
14
3.1
2.6
3.0
1.8
15
2.7
2.6
2.4
2.4
16
2.9
1.9
1.6
1.6
17
2.3
1.7
2.0
2.1
18
3.0
2.7
2.7
2.6
19
2.8
2.5
2.7
2.2
20
2.9
2.0
2.0
2.3
21
2.7
2.0
2.4
2.8
T.
2.6
X=
2.22
S
2.43
D
2.36
SD.
0.33
SD =
0.33
0 =
0.47
D-
0.42
tix*
54.9
IX * 46.7
x = 51
I=
49.6
not statistically sjgnificant and returned to normal within the 20 min of rest. Discussion The flow velocity is influenced by the ejection systolic pulse, arterial wall compliance, blood stream inertia and downstream peripheral resistance. If peripheral resistance is large then the pressure pulse wave travelling down the arterial tree is highly reflected and there is little flow into the capillary bed; hence diastolic velocity is small and the ratio of peak systolic to end diastolic flow is large [20]. Low resistance, however, allows onward travel of the pressure wave with little alteration and large diastolic flow results as in this study.
Since the umbilical arteries carry fetal blood to the placenta, umbilical artery waveform studies provide an indirect assessment of placental blood flow. Alterations in velocity are caused primarily by changes in resistance [21]. The S/D ratio examines the placental role in resistance to fetal umbilical artery velocity. A decrease in the S/D ratio of the umbilical artery waveform suggests a decrease in resistance and an increase in the fetal blood flow, as demonstrated by Trudinger and his colleagues in 1985 [21]. The relationship between exercise and placental resistance by measuring umbilical artery waveforms, to our knowledge, has not been previously tested in humans using this non-invasive technique, and at this level of exercise. However, Pijpers and his associates in 1984 [15] using mild exercise of 30% submaximal exercise, did not observe significant effect on fetal blood flow. In our study the intensity of exercise was 71% of submaximal exercise. Our findings are in agreement with previous animal studies, Dhindsa et al. in 1978 [3] found significant decrease in placental vascular resistance when he exercised five pregnant goats. Orr et al. in 1972 [14] measured the effect of exercise on uterine and iliac blood flow, using Doppler ultrasound on pregnant sheep and a found slight increase in uterine blood flow, and concluded that exercise is not hazardous to the fetus. In measuring the response to exercise, a history of previous exercise is important. Athletes have a different reference range from the rest of the population as shown by Rafla and Rumley [18,19]. In pregnancy it may be similar, and therefore the response to exercise may be different in the two groups. This may explain the results in the two patients mentioned above. In one of these, who was a highly trained athlete, the S/D ratio increased following exercise, and a transient fetal bradycardia was observed immediately following exercise. This athlete had to exercise harder to reach 70% of submaximal value, and the S/D ratio increased by 12%. In the second patient, who provided a history of regular jogging before and during pregnancy, no change in umbilical artery waveforms following exercise was observed. Mires et al. in 1987 [ll] demonstrated that the
122
S/D ratio decreases when fetal heart rate accelerates. Kofinas and his colleagues in 1989 [9] found that it is unnecessary to correct umbilical artery velocity waveforms for fetal heart rate. In our study the changes in fetal heart rates were not statistically significant and did not influence the significance of the effect of exercise on fetal blood flow. From this study it is concluded that exercise in pregnancy is not harmful to the fetus in healthy subjects and may improve placental circulation by decreasing placental vascular resistance. Healthy pregnant women who wish to exercise during pregnancy should not be discouraged. References Artal R, Wiswell RA, Exercise in pregnancy. Baltimore: Williams and Wilkins, 1986. Bracero L, Schulman H, Fleischer A, Farmakides G, Rochelson B. Umbilical artery velocimetry in diabetes and pregnancy. Obstet Gynaecol 1986;68:654-658. Dhindsa DS, Metcalfe J, Hummels DH. Responses to exercise in the pregnant pigmy goat. Respir Phys 1978;32: 299-311. Eriskine RLA, Ritchie JWK. The effect of maternal consumption of alcohol on human umbilical artery blood flow. Am J Obstet Gynecol 1986;154:318-21. Eriksen PS, Marsal K, Circulatory changes in the fetal aorta after maternal smoking. Br J Obstet Gynaecol 1987;94:301-305. Jouppila P, Kirkinen P, Eik-Nes S. Acute effect of maternal smoking on the human fetal blood flow. Br J Obstet Gynaecol1983;90:7-10. Jovanovic L, Kessler A, Peterson CM. Human maternal and fetal response to graded exercise. J Appl Physiol 1985; 58:1719-1722. Kirkinen P, Jouppila P, Koivula A, Vuori J, Puukka M. The effect of caffeine on placental and fetal blood flow in human pregnancy. Am J Obstet Gynecol1983;147:939-943.
9 Kofinas AD, Espeland M, Swain M, Penry M, Nelson L. Correcting umbilical artery flow velocity waveforms for fetal heart rate is unnecessary. Am J Obstet Gynecol. 1989;160:704-707. exercise in 10 Kupla PJ, White BM, Visscher R. Aerobic pregnancy. Am J Obstet Gynecol 1987;156:1395-1403. 11 Mires G, Dempster J, Pataf NB, Crawford JW. The effect of fetal heart rate on umbilical artery flow velocity waveforms. Br J Obstet Gynaecol. 1987;94:665-669. 12 Morris N, Osbom SB, Wright HP, Hart A. Effective uterine blood flow during exercise in normal and pre-eclamptic pregnancies. Lancet 1956;i:481-485. 13 Morton MJ, Paul MS, Campos GR, Hart MV, Metcalfe J. Exercise dynamics in late gestation: effect of physical training. Am J Obstet Gynecol. 1985;152:91-97. 14 Orr J, Ungerer T, Will J, Wemicke K, Curet LB. Effect of exercise stress on carotid, uterine and iliac blood flow in pregnant and non-pregnant ewes. Am J Obstet Gynecol 1972;114:213-217. 15 Pijpers L, Wladimiroff JW, McGhie J. Effect of short-term maternal exercise on maternal and fetal cardiovascular dynamics. Br J Obstet Gynaecol 1984;91:1081-1086. 16 Pomerance JJ, Gluck L, Lynch VA. Physical fitness in pregnancy: its effect on pregnancy outcome. Am J Obstet Gynecol 1974;119:867-876. 17 Rafla NM. The effect of maternal exercise on fetal and maternal blood flow in healthy and unhealthy women. Thesis submitted to the university of Liverpool, 1990. 18 Rafla N, Rumley AG. Clinical and biochemical changes during ninety hours of continuous basketball. Stand. J Sports Sci 1987;9:15-19. 19 Rumley AG, Rafla N. Serum enzyme changes during ninety hours of continuous basketball. Stand J Sports Sci 1983;5:45-49. 20 Schulman H, Fleischer A, Stem W, Farmakides G, Jagani N, Blattner P. Umbilical velocity wave ratios in human pregnancy. Am J Obstet Gynecol 1984;148:985-990. 21 Trudinger BJ, Giles WB, Cook CM, Bombardieri J, Collins L. Fetal umbilical artery velocity waveforms and placental resistance: clinical significance. Br J Obstet Gynaecol 1985;92:23-30.
