British Journal of Obstetrics and Gynaecology January, 1977. Vol84. pp 44-47.
EFFECTS OF SPONTANEOUS AND ARTIFICIAL MEMBRANE RUPTURE IN LABOUR UPON FETAL HEART RATE BY
S. ALADJEM, Professor AND
T. MILLER, Assistant Professor Department of Obstetrics and Gynecology, The Abraham Lincoln School of Medicine, University of Illinois at the Medical Center, Chicago, Illinois 60612
Summary This study reports the effects of spontaneous rupture of membranes and artificial rupture of membranes on fetal heart rate patterns during labour in 87 normal and 25 complicated pregnancies. The incidence of early deceleration patterns following membrane rupture was 6.25 per cent during the first 15 minutes and 1.78 per cent after 45 minutes, regardless of whether the pregnancy was normal or complicated. It is concluded that rupture of membranes does not significantly increase the incidence of early deceleration patterns. However, the occurrence of other heart rate alterations such as late decelerations, loss of beat-to-beat variability, changes in base line and tachycardia, need to be investigated further in larger collaborative studies.
RECENTpublications suggested that amniotomy adversely affects fetal homeostasis, facilitating uneven compression and deformation of the head, the occlusion of umbilical vessels, and the appearance of early decelerations (Type 1 dips) (Althabe et al, 1969; Caldeyro-Barcia, 1974). Nonetheless, it seemed that the perinatal effects of amniotomy needed to be elucidated and so we studied the effects of amniotomy upon the fetal heart rate (FHR) pattern in both normal and complicated pregnancies.
artificially in labour was made by the attending physician on obstetric considerations. All patients were monitored using Hewlett-Packard Equipment (Model Nos 8020-A Fetal Monitor; 15 180-A Ultrasound Amplifier; HP5 154-A Ultrasound Amplifier and Oscilloscope 15139A). Patients with technically unsatisfactory external recordings, or those in whom the relation between FHR alterations and uterine activity was not clear, were not included in the study. In most cases a spiral fetal scalp electrode was applied after the membranes were ruptured. A FHR between 120 to 160 beats per minute without changes during contractions and with good beat-to-beat variability (more than 5 beats per minute) was considered to be normal. A transient fall of the FHR greater than 10 beats/minute, synchronous with the uterine contraction, with a rate not below 100 beats/ minute at the peak of the uterine contraction was considered to represent an early deceleration.
METHODS We studied 112 patients from the Obstetrical Service of the University of Illinois Hospital; 87 patients had an uncomplicated term pregnancy and 25 had a complicated pregnancy (Table I). Only patients with intact membranes on admission in labour were included in the study. The decision to await spontaneous rupture of membranes or to ruptnre the membranes 44
MEMBRANE RUPTURE AND FETAL HEART RATE
TABLE I Distribution of patients Normal term pregnancy 87 Urinary oestriol less than 10 mg/24 hours Diabetes insulin 4 Chronic hypertension dependent Glomerulonephritis 2 Third trimester bleeding Prolonged pregnancy 3 Pyelonephritis more than 42 weeks l’re-eclampsia 4 Gastroenteritis Proteinuria more than Renal glycosuria 1 0 . 5 g/24 hours Anaemia, haemoglobin 3 Abruptio placentae less than 10 g/dl
five minutes ; infant’s birth weight; route of delivery; head measurements and the presence or absence of caput and moulding. 1
1 1 1 2 1
1
An asynchronous fall in FHR, greater than 10 beats per minute, with a lag-time or recoverytime of 30 seconds or more was considered to represent a late deceleration pattern. Transient falls in FHR greater than 10 beats per minute of variable shape and onset were considered to represent variable decelerations. These criteria follow generally the nomenclature proposed by Hon and Quilligan (1967). Based on these criteria, there were no differences between the compared ECG or ultrasound tracings on this study. FHR patterns recorded between 0 to 15 minutes and 16 to 45 minutes after rupture of the membranes were compared with tracings obtained 30 minutes before rupture of the membranes. The presence of FHR alteration was noted regardless of duration or persistence. Clinical variables other than FHR patterns studied in all patients were : presence or absence of meconium; cervical dilatation at the time of rupture of membranes; station of presenting part at the time of rupture of membranes; interval between delivery and rupture of membranes; infant’s Apgar score at birth at one and
RESULTS VariabIes other than FHR patterns There were no significant differences in the two groups of patients for any of the other clinical variables studied whether early deceleration patterns were present or not. At the time of spontaneous membrane rupture the cervix was between 5 and 9 cm dilated in 75 per cent of patients; in 2 3 . 3 per cent it was less than 4 cm, and in only 2 . 7 per cent had it reached full dilatation. In no patient were membranes intact at the time of delivery. Effects of rupture of membranes on FHR pattern Rupture of membranes, whether spontaneous or artificial, in normal or complicated pregnancies had no effect upon fetal heart rate pattern in 75 per cent of patients, while some changes occurred in 25 per cent (Table 11). During the first 15 minutes after rupture of membranes early deceleration patterns were noted in nine patients ; the early decelerations were thought to be drug-related in two patients as they coincided with the administration of a paracervical block and persisted for over 30 minutes. The total corrected incidence of early decelerations probably attributable to rupture of membranes was therefore 6 . 2 5 per cent (7 out of 112). Tachycardia appeared in 2 - 7 per cent (3/112), loss of beat-to-beat variability in 1 . 8 per cent (2/112), and change in the baseline and variable decelerations in 0 . 9 per cent (1/112) of patients. At 16 to 45 minutes after rupture of the
TABLEI1 Effects of rupture of membranes on fetal heart rate (FHR)pattern in the first 45 minutes FHR No change 84/112=75
%
Pregnancy
Rupture of membranes
No.
Per cent
Uncomplicated
Spontaneous Artificial Spontaneous Artificial Spontaneous Artificial Spontaneous Artificial
14/23 50164 415 16/20 9/23 14/64 115 4/20
60.8 78.1 80 80 39.2 21.9 20 20
64/87= 73.6 %
Complicated
20125 =80 %
Change
Uncomplicated
28/112=25%
23/87=26.4
%
Complicated 5/25 =20
%
45
46
ALADJEM A N D MlLLER
TABLE111 Fetal heart raie changes afrer rupture of membranes in 112 patients 0 to 15 minutes
16 to 45 minutes
No.
Per cent
No.
Per cent
Early decelerations Late decelerations Variable decelerations Loss of beat-to-beat variability ( < 5 beat/minute) Tachycardia (>160 beats/rninute) Change of base line
7 1 2 3
6.25
2 2 2 1 3 2
1.78 1.78 1.78 0 .8 9 2.7
membranes, early, variable, and late decelerations were each present in 1.8 per cent of patients (2/112) tachycardia in 2.7 per cent (3/112), loss of beat-to-beat variability in 0 . 9 per cent (l/ll2), and change in the baseline in 1 a 8 per cent (2/112) (Table 111).
et al, 1963), may be a composite physiological reflex under vagal control. Animal experiments have also indicated that pressure on the fetal head is accompanied by a decrease in the carotid blood flow, a decrease in the cerebral oxygenation, and an increase in the arterial blood pressure (Mann et al, 1972; Paul et al, 1964). Electroencephalographic changes were also noted (Garcia-Austt, 1969; Mann et al, 1972), but not all authors recorded alterations of the fetal heart rate (Mann el al, 1972; Pearse and Bliese, 1968; Reynolds and Paul, 1955). The reduction in the oxygen consumption by the brain during early decelerations may be a risk to the fetal brain and subtle subclinical changes may result (Windle, 1970). Because hypoxia has been shown to be the cause of 55 per cent of all perinatal deaths (Butler and Bonham, 1963), the untimely rupture of membranes during early labour is of great concern. Caldeyro-Barcia (1974) points out that 34 per cent of spontaneous membrane ruptures occur at full dilatation and 20 per cent at the time of delivery, with 66 per cent of patients having intact membranes at the end of the first stage of labour. This has not been the finding in our study nor in larger studies which have reported a 45 per cent incidence of spontaneous membrane rupture before the onset of labour (Niswander and Gordon, 1972). It would therefore seem unlikely that rupture of membranes before or during the first stage of labour is unphysiological. Caldeyro-Barcia (1974) reported a 34 per cent incidence of caput and a 44 per cent incidence of disalignment of fetal skull bones with early
DISCUSSION At term, the uterus and its contents may be thought of as a closed hydraulic system wherein any increase in pressure will affect all of its components equally (Reynolds and Paul, 1955). The pressure upon the fetal head is thought to be higher than in the amniotic fluid, being maximal at the largest circumference of the head (Bore11 and Fernstrom, 1958;Lindgren, 1972). Mechanical models have indicated that such forces are necessary if the fetal head is to descend through the birth canal (Rydberg, 1954). Considering that the usual range of intrauterine pressures may reach values between 100 and 130 mm Hg during bearing down in the second stage of labour, the pressure on the fetal head could reach 200 mm Hg (Turnbull, 1959). Moulding during descent may be favoured by the rupture of membranes in early labour, thus increasing the risks of traumatic lesions (Caldeyro-Barcia, 1974; Amiel-Tison, 1973; Fedric and Butler, 1971) as well as the risk of transient fetal acidosis (Lumley and Wood, I97 l), the incidence of early decelerations (Althabe et al, 1969; CaldeyroBarcia, 1974), and the risk of cord occlusion when a nuchal encirclement is present (CaldeyroBarcia, 1974). The vagal reflex theory attempts to explain the mechanism of early deceleration. This pattern which is inhibited by atropine (Mendez-Bauer
1
0.89 1.78 2.7 0.89
1.78
MEMBRANE RUPTURE AND FETAL HEART RATE
rupture of membranes, as opposed to 5 per cent and 35 per cent respectively when membranes were intact at delivery; patients with cephalopelvic disproportion were not included. In our series there were four patients with moulding, all associated with cephalopelvic disproportion necessitating Caesarean section ; there were three patients with caput formation and no disalignments. Head measurements were all within the normal range and the timing of membrane rupture thus did not seem to influence the state of the fetal head. Caldeyro-Barcia (1 974) indicated that the incidence of early decelerations (Type I dips) rose in patients with an unengaged fetal head from 4.49 per cent with intact membranes to 15.6 per cent with ruptured membranes, whereas when the head was engaged, the incidence rose from 9 per cent with late amniotomy to 45 per cent with early amniotomy. In our study 75 per cent of patients showed no FHR alterations with either spontaneous or artificial membrane rupture and the corrected incidence of early decelerations during the first 15 minutes after rupture was 6.25 per cent (7/112). The timing of rupture of membranes, cervical dilatation, the level of the presenting part, the time to delivery, the route of delivery and the fetal weight, had no influence on these changes or on the fetal Apgar score at birth. Furthermore, the presence of risk factors during pregnancy did not influence the incidence of early decelerations. Thus we cannot support the contention that rupture of membranes significantly increased the number of early deceleration patterns. However, we did detect other alterations of the FHR such as tachycardia, late deceleration, change in baseline, and loss of beat-to-beat variability. The number of patients was too small to evaluate such alterations and further enquiries seem warranted. REFERENCES Althabe, O., Aramburu, G., Schwarcz, R. L., and Caldeyro-Barcia, R. (1969) : In Perinatal Factors Aflecting Human Development. Pan-American Health Organization Scientific Publication No. 185, Washington, DC, p 143.
47
Amiel-Tison, C. (1973): Current Problems in Pediatrics, 3, 3. Borell, U., and Fernstrom, I. (1958): GeburtshiIfe und Frauenheilkunde, 18, 1156. Butler, N. R., and Bonham, D. G., (1963): Perinatal Mortfility, E. & S . Livinsgtone, Edinburgh, p 203. Caldeyro-Barcia, R. (1974) : Modern Perinatal Medicine. Edited by L. Gluck. Year Book Publishers, Chicago, p 431. Fedric, J., and Butler, N. R. (1971): Biologica neonatorum, 18, 321. Garcia-Austt, E. (1969) : In Perinatal Factors Affecting Human Development. Pan-American Health Organization Scientific Publication, No. 185, Washington, DC, p 127. Hon, E. H., and Quilligan, E. J. (1967): Connecticut Medicine, 33,779. Lindgren, I,. (1972) : Acta obstetricia et gynecologica Scandinavica, 51,37. Lumley, J., and Wood, C. (1971): Australian and New Zealand Journal of Obstetrics and Gynaecology, 11, 221. Mann, L., Carmichael, A., and Duchin, S. (1972): Obstetrics and Gynecology, 39, 721. Mendez-Bauer, C., Poseiro, J., Arellano, H. G., Zambrana, M. A., and Caldeyro-Barcia, R. (1963): American Journal of Obstetrics and Gynecology, 85, 1033. Niswander, K., and Gordon, M. (1972): Collaborative Perinatal Study of the National Institute of Neurological Diseases and Stroke, W. B. Saunders, Philadelphia, p 427. Paul, W. M., Quilligan, E. J., and MacLachlan, T. (1964): American Journal of Obstetrics and Gynaecology, 90, 824. Pearse, W. H., and Bliese, K. A. (1968): Obstetrics and Gynecology, 32, 254. Reynolds, S. R. M., and Paul, W. M. (1955): Bulletin of the Johns Hopkins Hospital, 97,383. Rydberg, E. (1954): The Mechanism of Labour, 1st Edition. Charles C. Thomas, Springfield, Illinois, P 6. Turnbull, A. (1959): In Oxygen Supply to the Human Foetus. Blackwell Scientific Publications, Oxford, p 129. Windle, W. (1 970) : In Year Book of Obstetrics and Gynecology. Greenhill, Year Book Medical Publishers, Chicago, p 238.
EFFECTS OF SPONTANEOUS AND ARTIFICIAL MEMBRANE RUPTURE IN LABOUR UPON FETAL HEART RATE BY
S. ALADJEM, Professor AND
T. MILLER, Assistant Professor Department of Obstetrics and Gynecology, The Abraham Lincoln School of Medicine, University of Illinois at the Medical Center, Chicago, Illinois 60612
Summary This study reports the effects of spontaneous rupture of membranes and artificial rupture of membranes on fetal heart rate patterns during labour in 87 normal and 25 complicated pregnancies. The incidence of early deceleration patterns following membrane rupture was 6.25 per cent during the first 15 minutes and 1.78 per cent after 45 minutes, regardless of whether the pregnancy was normal or complicated. It is concluded that rupture of membranes does not significantly increase the incidence of early deceleration patterns. However, the occurrence of other heart rate alterations such as late decelerations, loss of beat-to-beat variability, changes in base line and tachycardia, need to be investigated further in larger collaborative studies.
RECENTpublications suggested that amniotomy adversely affects fetal homeostasis, facilitating uneven compression and deformation of the head, the occlusion of umbilical vessels, and the appearance of early decelerations (Type 1 dips) (Althabe et al, 1969; Caldeyro-Barcia, 1974). Nonetheless, it seemed that the perinatal effects of amniotomy needed to be elucidated and so we studied the effects of amniotomy upon the fetal heart rate (FHR) pattern in both normal and complicated pregnancies.
artificially in labour was made by the attending physician on obstetric considerations. All patients were monitored using Hewlett-Packard Equipment (Model Nos 8020-A Fetal Monitor; 15 180-A Ultrasound Amplifier; HP5 154-A Ultrasound Amplifier and Oscilloscope 15139A). Patients with technically unsatisfactory external recordings, or those in whom the relation between FHR alterations and uterine activity was not clear, were not included in the study. In most cases a spiral fetal scalp electrode was applied after the membranes were ruptured. A FHR between 120 to 160 beats per minute without changes during contractions and with good beat-to-beat variability (more than 5 beats per minute) was considered to be normal. A transient fall of the FHR greater than 10 beats/minute, synchronous with the uterine contraction, with a rate not below 100 beats/ minute at the peak of the uterine contraction was considered to represent an early deceleration.
METHODS We studied 112 patients from the Obstetrical Service of the University of Illinois Hospital; 87 patients had an uncomplicated term pregnancy and 25 had a complicated pregnancy (Table I). Only patients with intact membranes on admission in labour were included in the study. The decision to await spontaneous rupture of membranes or to ruptnre the membranes 44
MEMBRANE RUPTURE AND FETAL HEART RATE
TABLE I Distribution of patients Normal term pregnancy 87 Urinary oestriol less than 10 mg/24 hours Diabetes insulin 4 Chronic hypertension dependent Glomerulonephritis 2 Third trimester bleeding Prolonged pregnancy 3 Pyelonephritis more than 42 weeks l’re-eclampsia 4 Gastroenteritis Proteinuria more than Renal glycosuria 1 0 . 5 g/24 hours Anaemia, haemoglobin 3 Abruptio placentae less than 10 g/dl
five minutes ; infant’s birth weight; route of delivery; head measurements and the presence or absence of caput and moulding. 1
1 1 1 2 1
1
An asynchronous fall in FHR, greater than 10 beats per minute, with a lag-time or recoverytime of 30 seconds or more was considered to represent a late deceleration pattern. Transient falls in FHR greater than 10 beats per minute of variable shape and onset were considered to represent variable decelerations. These criteria follow generally the nomenclature proposed by Hon and Quilligan (1967). Based on these criteria, there were no differences between the compared ECG or ultrasound tracings on this study. FHR patterns recorded between 0 to 15 minutes and 16 to 45 minutes after rupture of the membranes were compared with tracings obtained 30 minutes before rupture of the membranes. The presence of FHR alteration was noted regardless of duration or persistence. Clinical variables other than FHR patterns studied in all patients were : presence or absence of meconium; cervical dilatation at the time of rupture of membranes; station of presenting part at the time of rupture of membranes; interval between delivery and rupture of membranes; infant’s Apgar score at birth at one and
RESULTS VariabIes other than FHR patterns There were no significant differences in the two groups of patients for any of the other clinical variables studied whether early deceleration patterns were present or not. At the time of spontaneous membrane rupture the cervix was between 5 and 9 cm dilated in 75 per cent of patients; in 2 3 . 3 per cent it was less than 4 cm, and in only 2 . 7 per cent had it reached full dilatation. In no patient were membranes intact at the time of delivery. Effects of rupture of membranes on FHR pattern Rupture of membranes, whether spontaneous or artificial, in normal or complicated pregnancies had no effect upon fetal heart rate pattern in 75 per cent of patients, while some changes occurred in 25 per cent (Table 11). During the first 15 minutes after rupture of membranes early deceleration patterns were noted in nine patients ; the early decelerations were thought to be drug-related in two patients as they coincided with the administration of a paracervical block and persisted for over 30 minutes. The total corrected incidence of early decelerations probably attributable to rupture of membranes was therefore 6 . 2 5 per cent (7 out of 112). Tachycardia appeared in 2 - 7 per cent (3/112), loss of beat-to-beat variability in 1 . 8 per cent (2/112), and change in the baseline and variable decelerations in 0 . 9 per cent (1/112) of patients. At 16 to 45 minutes after rupture of the
TABLEI1 Effects of rupture of membranes on fetal heart rate (FHR)pattern in the first 45 minutes FHR No change 84/112=75
%
Pregnancy
Rupture of membranes
No.
Per cent
Uncomplicated
Spontaneous Artificial Spontaneous Artificial Spontaneous Artificial Spontaneous Artificial
14/23 50164 415 16/20 9/23 14/64 115 4/20
60.8 78.1 80 80 39.2 21.9 20 20
64/87= 73.6 %
Complicated
20125 =80 %
Change
Uncomplicated
28/112=25%
23/87=26.4
%
Complicated 5/25 =20
%
45
46
ALADJEM A N D MlLLER
TABLE111 Fetal heart raie changes afrer rupture of membranes in 112 patients 0 to 15 minutes
16 to 45 minutes
No.
Per cent
No.
Per cent
Early decelerations Late decelerations Variable decelerations Loss of beat-to-beat variability ( < 5 beat/minute) Tachycardia (>160 beats/rninute) Change of base line
7 1 2 3
6.25
2 2 2 1 3 2
1.78 1.78 1.78 0 .8 9 2.7
membranes, early, variable, and late decelerations were each present in 1.8 per cent of patients (2/112) tachycardia in 2.7 per cent (3/112), loss of beat-to-beat variability in 0 . 9 per cent (l/ll2), and change in the baseline in 1 a 8 per cent (2/112) (Table 111).
et al, 1963), may be a composite physiological reflex under vagal control. Animal experiments have also indicated that pressure on the fetal head is accompanied by a decrease in the carotid blood flow, a decrease in the cerebral oxygenation, and an increase in the arterial blood pressure (Mann et al, 1972; Paul et al, 1964). Electroencephalographic changes were also noted (Garcia-Austt, 1969; Mann et al, 1972), but not all authors recorded alterations of the fetal heart rate (Mann el al, 1972; Pearse and Bliese, 1968; Reynolds and Paul, 1955). The reduction in the oxygen consumption by the brain during early decelerations may be a risk to the fetal brain and subtle subclinical changes may result (Windle, 1970). Because hypoxia has been shown to be the cause of 55 per cent of all perinatal deaths (Butler and Bonham, 1963), the untimely rupture of membranes during early labour is of great concern. Caldeyro-Barcia (1974) points out that 34 per cent of spontaneous membrane ruptures occur at full dilatation and 20 per cent at the time of delivery, with 66 per cent of patients having intact membranes at the end of the first stage of labour. This has not been the finding in our study nor in larger studies which have reported a 45 per cent incidence of spontaneous membrane rupture before the onset of labour (Niswander and Gordon, 1972). It would therefore seem unlikely that rupture of membranes before or during the first stage of labour is unphysiological. Caldeyro-Barcia (1974) reported a 34 per cent incidence of caput and a 44 per cent incidence of disalignment of fetal skull bones with early
DISCUSSION At term, the uterus and its contents may be thought of as a closed hydraulic system wherein any increase in pressure will affect all of its components equally (Reynolds and Paul, 1955). The pressure upon the fetal head is thought to be higher than in the amniotic fluid, being maximal at the largest circumference of the head (Bore11 and Fernstrom, 1958;Lindgren, 1972). Mechanical models have indicated that such forces are necessary if the fetal head is to descend through the birth canal (Rydberg, 1954). Considering that the usual range of intrauterine pressures may reach values between 100 and 130 mm Hg during bearing down in the second stage of labour, the pressure on the fetal head could reach 200 mm Hg (Turnbull, 1959). Moulding during descent may be favoured by the rupture of membranes in early labour, thus increasing the risks of traumatic lesions (Caldeyro-Barcia, 1974; Amiel-Tison, 1973; Fedric and Butler, 1971) as well as the risk of transient fetal acidosis (Lumley and Wood, I97 l), the incidence of early decelerations (Althabe et al, 1969; CaldeyroBarcia, 1974), and the risk of cord occlusion when a nuchal encirclement is present (CaldeyroBarcia, 1974). The vagal reflex theory attempts to explain the mechanism of early deceleration. This pattern which is inhibited by atropine (Mendez-Bauer
1
0.89 1.78 2.7 0.89
1.78
MEMBRANE RUPTURE AND FETAL HEART RATE
rupture of membranes, as opposed to 5 per cent and 35 per cent respectively when membranes were intact at delivery; patients with cephalopelvic disproportion were not included. In our series there were four patients with moulding, all associated with cephalopelvic disproportion necessitating Caesarean section ; there were three patients with caput formation and no disalignments. Head measurements were all within the normal range and the timing of membrane rupture thus did not seem to influence the state of the fetal head. Caldeyro-Barcia (1 974) indicated that the incidence of early decelerations (Type I dips) rose in patients with an unengaged fetal head from 4.49 per cent with intact membranes to 15.6 per cent with ruptured membranes, whereas when the head was engaged, the incidence rose from 9 per cent with late amniotomy to 45 per cent with early amniotomy. In our study 75 per cent of patients showed no FHR alterations with either spontaneous or artificial membrane rupture and the corrected incidence of early decelerations during the first 15 minutes after rupture was 6.25 per cent (7/112). The timing of rupture of membranes, cervical dilatation, the level of the presenting part, the time to delivery, the route of delivery and the fetal weight, had no influence on these changes or on the fetal Apgar score at birth. Furthermore, the presence of risk factors during pregnancy did not influence the incidence of early decelerations. Thus we cannot support the contention that rupture of membranes significantly increased the number of early deceleration patterns. However, we did detect other alterations of the FHR such as tachycardia, late deceleration, change in baseline, and loss of beat-to-beat variability. The number of patients was too small to evaluate such alterations and further enquiries seem warranted. REFERENCES Althabe, O., Aramburu, G., Schwarcz, R. L., and Caldeyro-Barcia, R. (1969) : In Perinatal Factors Aflecting Human Development. Pan-American Health Organization Scientific Publication No. 185, Washington, DC, p 143.
47
Amiel-Tison, C. (1973): Current Problems in Pediatrics, 3, 3. Borell, U., and Fernstrom, I. (1958): GeburtshiIfe und Frauenheilkunde, 18, 1156. Butler, N. R., and Bonham, D. G., (1963): Perinatal Mortfility, E. & S . Livinsgtone, Edinburgh, p 203. Caldeyro-Barcia, R. (1974) : Modern Perinatal Medicine. Edited by L. Gluck. Year Book Publishers, Chicago, p 431. Fedric, J., and Butler, N. R. (1971): Biologica neonatorum, 18, 321. Garcia-Austt, E. (1969) : In Perinatal Factors Affecting Human Development. Pan-American Health Organization Scientific Publication, No. 185, Washington, DC, p 127. Hon, E. H., and Quilligan, E. J. (1967): Connecticut Medicine, 33,779. Lindgren, I,. (1972) : Acta obstetricia et gynecologica Scandinavica, 51,37. Lumley, J., and Wood, C. (1971): Australian and New Zealand Journal of Obstetrics and Gynaecology, 11, 221. Mann, L., Carmichael, A., and Duchin, S. (1972): Obstetrics and Gynecology, 39, 721. Mendez-Bauer, C., Poseiro, J., Arellano, H. G., Zambrana, M. A., and Caldeyro-Barcia, R. (1963): American Journal of Obstetrics and Gynecology, 85, 1033. Niswander, K., and Gordon, M. (1972): Collaborative Perinatal Study of the National Institute of Neurological Diseases and Stroke, W. B. Saunders, Philadelphia, p 427. Paul, W. M., Quilligan, E. J., and MacLachlan, T. (1964): American Journal of Obstetrics and Gynaecology, 90, 824. Pearse, W. H., and Bliese, K. A. (1968): Obstetrics and Gynecology, 32, 254. Reynolds, S. R. M., and Paul, W. M. (1955): Bulletin of the Johns Hopkins Hospital, 97,383. Rydberg, E. (1954): The Mechanism of Labour, 1st Edition. Charles C. Thomas, Springfield, Illinois, P 6. Turnbull, A. (1959): In Oxygen Supply to the Human Foetus. Blackwell Scientific Publications, Oxford, p 129. Windle, W. (1 970) : In Year Book of Obstetrics and Gynecology. Greenhill, Year Book Medical Publishers, Chicago, p 238.
