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Urgent Cesarean Delivery for Fetal Bradycardia

Leung, Tak Yeung MRCOG, MD; Chung, Pui Wah MBChB; Rogers, Michael Scott FRCOG, MD; Sahota, Daljit Singh PhD; Lao, Terence Tzu-Hsi FRCOG, MD; Hung Chung, Tony Kwok FRCOG, MD

doi: 10.1097/AOG.0b013e3181bc6e15
Original Research

OBJECTIVE: To estimate whether fetal bradycardia-to-delivery interval or decision-to-delivery interval was related to cord arterial pH according to different causes of fetal distress.

METHODS: Women who delivered singleton neonates by urgent cesarean delivery because of intrapartum fetal bradycardia were retrospectively categorized into three groups according to the cause of fetal bradycardia: 1) Irreversible; 2) Potentially Reversible; and 3) Unknown (no identifiable cause). Comparisons were made between groups in regard to pH, bradycardia-to-delivery interval, and decision-to-delivery interval. Correlation analyses between pH and both intervals were then performed for different groups.

RESULTS: Of 235 cases, 39, 22, and 174 were respectively categorized into the Irreversible group, Potentially Reversible group, and Unknown group. The median pH was lower in the Irreversible group (7.094; interquartile range [IQR] 6.991–7.216) than in Potentially Reversible group (7.162; IQR 7.064–7.251) or Unknown group (7.210; IQR 7.161–7.255) (P<.001). The Irreversible group's median bradycardia-to-delivery interval was 5 minutes shorter than those of the other two groups (11 compared with 16.5 and 16 minutes, respectively; P<.001), whereas its median decision-to-delivery interval was 1 minute shorter (10 compared with 11.5 and 11 minutes, respectively; P=.001). In the Irreversible group, pH decreased with the bradycardia-to-delivery interval (Spearman's ρ=–0.354; P=.027) at a rate of 0.011 per minute. Cord arterial pH did not correlate with the bradycardia-to-delivery interval in the Potentially Reversible and Unknown groups. In neither group did pH correlate with decision-to-delivery interval.

CONCLUSION: Cord arterial pH deteriorates with bradycardia-to-delivery interval when the underlying cause of fetal distress is irreversible, but not so otherwise.


Cord arterial pH deteriorates with fetal bradycardia-to-delivery interval.

From the Department of Obstetrics and Gynecology, the Chinese University of Hong Kong, Hong Kong, China.

Corresponding author: Dr. Tak Yeung Leung, Department of Obstetrics and Gynecology, Prince of Wales Hospital, Shatin, Hong Kong, China SAR; e-mail:

Financial Disclosure The authors did not report any potential conflicts of interest.

The auditable standard of delivering fetuses within 30 minutes after a diagnosis of fetal distress remains one of the most controversial issues in obstetrics. Yet this 30-minute rule for decision-to-delivery interval has become a medical–legal benchmark for adequacy of obstetric care.1 Although many national professional associations such as the American College of Obstetricians and Gynecologists recommend this 30-minute rule,2–4 the existing scientific evidence to support such recommendations is weak. On the other hand, there are many reports showing that a longer delivery interval did not necessarily correlate with a poorer perinatal outcome, even if the fetal monitoring showed ominous findings.5–9 Some reports even demonstrated a better cord arterial pH when the delivery interval became longer.6,10

Such paradoxical results can be partly explained by the fact that the current method of diagnosing fetal distress is so nonspecific that many false-positive cases actually had a good outcome regardless of the time of delivery.11 In addition, these results might also be related partly to the design of those studies. Firstly, all of those studies did not analyze the fetal outcomes in regard to the causes of fetal distress, which are well-known to be heterogeneous with various degree of severity.6–10 The adverse effects of more severe cases could be masked by the less severe cases. It was also possible that selection bias might have existed, because clinicians tended to deliver those fetuses with severe distress more promptly than the less severe cases. Secondly, those studies only focused on the decision-to-delivery interval, instead of the bradycardia-to-delivery interval, which should be a more relevant reflection of fetal compromise and therefore should be more likely to be correlated with fetal outcome. Therefore, the aim of our study was to estimate whether bradycardia-to-delivery interval or decision-to-delivery interval was related to adverse perinatal outcome after extremely urgent or crash cesarean delivery for different causes of fetal distress.

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This was a retrospective study conducted in a university tertiary referral obstetric unit after obtaining approval from the Chinese University of Hong Kong—New Territories East Cluster Clinical ethics committee. The total number of births during 2005–2008 was 26,028. The study unit had a standard intrapartum management protocol that included 1) the use of routine continuous cardiotocograph monitoring, 2) that interpretation of cardiotocograph followed the Royal College of Obstetricians and Gynaecologists guideline,12 3) that extremely urgent cesarean delivery should be prepared when there was persistent fetal bradycardia (less than 110 beats per minute) for 3 minutes, and should be decided when it lasted for 5 minutes without sign of recovery, or when the fetal bradycardia was associated with irreversible conditions such as placental abruption or cord prolapse, and 4) clear documentation in the medical notes of the timing of all major events, including the time of various examinations, onset of bradycardia, decision for an intervention, transferal to operating theater, start of operation, uterine incision, and delivery. The definition of extremely urgent cesarean delivery used in the study unit was equivalent to the grade 1 of the Royal College of Obstetricians and Gynaecologists classification of “urgency” of emergency cesarean delivery.12 For this group of cesarean deliveries, the protocol aimed at a decision-to-delivery interval within 15 minutes. On-site 24-hour emergency anesthetic support was available. There were two operating theaters inside the labor ward, so that transfer of the patients from the delivery room to the operation theater could be accomplished within a few minutes.

Women who delivered their neonates by extremely urgent cesarean delivery because of fetal distress during the study period were identified from the hospital Obstetric Specialty Clinical Information System, which is a clinical database recording maternity and perinatal outcome information for all women delivering at the university unit.13 Antenatal data, such as age, weight, height, and previous obstetric history, were collected during each visit. Perinatal outcomes including mode of delivery, indication for operative delivery, birth weight, cord arterial blood gas, and perinatal complications were collected at time of delivery.

The medical notes of all eligible cases identified from the Obstetric Specialty Clinical Information System were retrieved as well and reviewed for the bradycardia-to-delivery interval, decision-to-delivery interval, and umbilical cord arterial blood gas, which are all routinely recorded. Other information stated in Obstetric Specialty Clinical Information System was also cross-checked for any error. Multiple pregnancies and pregnancies with fetal abnormalities were excluded for analysis.

The causes of fetal bradycardia were reviewed, and the cases were categorized into three different groups according to the cause of fetal distress: 1) Irreversible; 2) Potentially Reversible; and 3) Unknown (no identifiable cause) (Table 1). Comparisons were made between groups with regard to cord pH and base excess levels, bradycardia-to-delivery interval, decision-to-delivery interval, gestational age, and birth weight using Kruskal-Wallis test for continuous variables followed by post-hoc Dunn test and χ2 test for categorical variables. Correlation analysis between cord pH and both bradycardia-to-delivery interval and decision-to-delivery interval were then performed for different groups using the Spearman test. All statistical tests were performed using a commercially available statistical package (Statistical Package for the Social Science for Windows 16.0, SPSS Inc., Chicago, IL).

Table 1

Table 1

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During the study period, 236 women with a singleton pregnancy underwent extremely urgent cesarean delivery, which accounted for 5.7% of all emergency cesarean deliveries and 0.9% of all deliveries in the study unit. The median maternal age was 30 years (interquartile range [IQR] 25–34) and 182 of them (77.1%) were nulliparous. The median gestation at delivery was 39 6/7 (IQR 38 5/7 to 40 6/7), and the median birth weight was 3,160 g (IQR 2,825–3,424 g). The median cord arterial pH was 7.196 (IQR 7.120–7.250). The cord arterial pH was less than 7 in 20 cases (8.5%). Overall, 51.7% had an arterial pH less than 7.2 at delivery. The median bradycardia-to-delivery interval and decision-to-delivery intervals were 16 minutes (IQR 14–18 minutes) and 11 minutes (IQR 10–13 minutes), respectively. All the neonates were delivered within 19 minutes, and 213 (90.3%) operations were performed under general anesthesia, whereas the rest were under regional anesthesia. There were no major maternal postoperative complications or neonatal complications, except a case of perinatal death resulting from acute maternal ketoacidosis, which was excluded from further analysis because ketoacidosis itself might affect cord pH and base excess levels.

Identifiable causes for the occurrence of fetal bradycardia are listed in Table 1 and included placental abruption (nine cases including one case with eclampsia; 3.8%), cord prolapse (21 cases; 8.9%), severe preeclampsia (three cases excluding coexisting abruption; 1.3%), and failed instrumental delivery (six cases; 2.5%). They (39 cases; 16.6%) were categorized into the Irreversible group. Another 22 cases (9.4%) who had potentially reversible causes were categorized into the Potentially Reversible group, which included hypotension after epidural anesthesia (five cases; 2.1%), external cephalic version (four cases excluding coexisting abruption; 1.7%), and iatrogenic uterine hyperstimulation (13 cases; 5.6%). However, no causes could be identified in the remaining 174 cases (74.0%), although some of them had risk factors such as loose cord around fetal neck (20 cases), meconium stained liquor (48 cases), birth weight less than fifth centile (13 cases), and they were categorized into the Unknown group.

Table 2 shows the comparison of the basic maternal demographic and selected perinatal outcomes and delivery intervals among the three groups. The median cord arterial pH was significantly lower in the Irreversible group (7.094; IQR 6.991–7.216) when compared with the Potentially Reversible group (7.162; IQR 7.064–7.251) and Unknown group (7.210; IQR 7.161–7.255) (P<.05), although there was no difference between the Potentially Reversible group and the Unknown group. The proportion of neonates with cord pH less than 7 was also significantly higher in the Irreversible group in comparison with those in the two other groups (25.6% compared with 4.5% and 4.6%, respectively; P<.05). Cord base excess was also lower in the Irreversible and Potentially Reversible groups when compared with the Unknown group (–10.0 compared with –9.5 compared with –6.3, respectively).

Table 2

Table 2

The median bradycardia-to-delivery interval was 5 to 5.5 minutes shorter in the Irreversible group (11 minutes; IQR 9–16) than in other two groups (Potentially Reversible group 16.5 minutes; IQR 14–18.3; Unknown group 16 minutes IQR 14–19; P<.05). The median decision-to-delivery interval of the Irreversible group was just 1 to 1.5 minutes shorter than the other two groups (10 minutes compared with 11.5 minutes compared with 11 minutes respectively; P=.002).

Table 3 shows the result of the correlation analysis between cord arterial pH and base excess with bradycardia-to-delivery interval and decision-to-delivery interval. When correlation analysis was performed for the whole cohort of 235 patients, no relationship was found between pH and base excess with either bradycardia-to-delivery interval or decision-to-delivery interval. However, subgroup analysis revealed that cord arterial pH was significantly inversely correlated with bradycardia-to-delivery interval in the Irreversible group (Spearman's =–0.354; P=.027), but not in the other two groups, whereas cord arterial pH was not correlated with decision-to-delivery interval in any of the three groups. The rate of drop of pH with bradycardia-to-delivery interval in the Irreversible group estimated by liner regression analysis was 0.011 per minute (95% confidence interval 0.003–0.020). The changes of pH with bradycardia-to-delivery interval in the different groups are shown in Figure 1. Similarly, cord arterial base excess deteriorated significantly with bradycardia-to-delivery interval (Spearman's ρ=–0.406; P=.011) but not decision-to-delivery interval in the Irreversible group, but not so in either the Potentially Reversible or Unknown groups.

Table 3

Table 3



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The results of this study have several important implications. Firstly, our result has clearly shown that where the underlying cause of fetal distress was irreversible, the cord arterial pH deteriorates rapidly starting from the onset of fetal bradycardia. Therefore, in such a situation, immediate delivery is essential to minimize the risk of irreversible fetal brain damage due to hypoxia. On the other hand, among those cases in which the cause was either potentially reversible or not identifiable, there was no significant relationship between the cord arterial pH and the delivery interval, and the cord pH was in general relatively better, with only 4% to 5% chance of being lower than 7 (compared with 26.8% in the Irreversible group). Thus, accurate clinical judgement is as critical as speed for proper management in these situations. Every effort must be made to look for irreversible conditions which require prompt delivery.

On the other hand, cesarean delivery may sometimes be avoidable in potentially reversible conditions with correct and decisive management, such as acute tocolysis for uterine hyperstimulation14 and vasopressors to treat hypotension associated with regional anesthesia.15 In the case of fetal bradycardia after external cephalic version, it usually lasts less than 1 minute without immediate fetal danger.16 It could be due to cord compression or vagal stimulation secondary to the application of excessive force on the fetal head by the operator during version.17,18 However, bradycardia could sometimes last longer after external cephalic version and in such a situation, placental abruption could not be excluded with certainty. In cases without an identifiable cause, the overall cord arterial pH was satisfactory and it did not deteriorate rapidly with time. Therefore, our protocol used during the study period that required a decision for cesarean delivery after 3 to 5 minutes might have been too strict. To minimize the need for extremely urgent cesarean delivery, it is possible to monitor for the recovery of fetal bradycardia to beyond 5 minutes and to proceed to cesarean delivery only when there is still no evidence of recovery. Alternatively, the persistence of fetal bradycardia could be reconfirmed in the operating theater just before the incision.

Secondly, the rate of cord arterial pH deterioration in the Irreversible group of 0.011 per minute was more rapid when compared with other conditions. For example, it was 2.4-fold faster than that of the second twin after the vaginal delivery of the first twin (approximately 0.0046 per minute).19 The chance of the second twin's cord arterial pH being below 7 is minimal when the second twin is delivered within 15 minutes after the birth of the first twin, 5.9% if within 16–30 minutes, and 27% if more than 30 minutes.20 However, in the Irreversible group, the chance was 20.7% (6 of 29) if the bradycardia-to-delivery interval was within 15 minutes, and 40% (4 of 10) if the bradycardia-to-delivery interval was between 16 and 30 minutes. Since a twin-to-twin delivery interval of 30 minutes is a commonly acceptable standard,21,22 it is thus reasonable to set bradycardia-to-delivery interval a time limit of 30 minutes or less with irreversible cause, and the decision-to-delivery interval limit should be even shorter.

The median bradycardia-to-delivery interval in the Irreversible group was 5 to 5.5 minutes shorter than the other two groups, but there was only a 1- to 1.5-minute difference in decision-to-delivery interval. These results indicated that when the clinical condition was deemed severe and irreversible, the attending clinicians decided for cesarean delivery earlier in response to fetal bradycardia. On the other hand, when the cause of fetal bradycardia was clinically not obvious or potentially reversible, the clinicians tended to look for signs of recovery before deciding on cesarean delivery. However, once cesarean delivery was decided, the action to delivery was very rapid in all groups, because the difference in decision-to-delivery interval is only 1 minute between groups. This clearly explains why if analysis was not stratified by the underlying causes, it could result in a misleading interpretation that a longer decision-to-delivery interval did not lead to a poorer outcome or even gave a better outcome compared with those with a short decision-to-delivery interval.

Our result demonstrated clearly that a short decision-to-delivery interval is possible in a well-organized unit with experienced staff. We were able to achieve 100% delivery within 20 minutes of the decision-to-delivery interval, with a median value of 10 minutes. However, this process was extremely stressful, and has potential risks if there is inadequate training or staffing. To make this possible, almost all women undergoing extremely urgent cesarean delivery had a general anesthesia, which in general carries a higher complication rate than regional anesthesia. Therefore, the understanding that speedy delivery is probably only useful in reducing adverse fetal outcome in those cases with irreversible causes would enable the clinician to make a more logical decision based on the actual clinical situation.

Finally, all professional bodies audit the clinicians' response time by the interval starting from the decision time for cesarean delivery to delivery time, instead of starting from onset of fetal distress. One of the possible reasons is that the onset time of fetal distress, or abnormal heart rate tracing, is often difficult to define unless it presents as fetal bradycardia. However, our study has shown that the length of bradycardia-to-delivery interval, rather than the decision-to-delivery interval, correlated significantly with the deterioration of cord arterial pH. Whereas the decision-to-delivery interval only measures the capacity of a clinical team or a unit to arrange an urgent or emergency cesarean delivery, which is mainly influenced by the facilities and staff availability,23 bradycardia-to-delivery interval also measures the performance of a team or unit in fetal monitoring, interpretation, and decision making processes. Therefore, we suggest that bradycardia-to-delivery interval should be included as an additional measure because it may help to explain some cases of otherwise inexplicable adverse perinatal outcome despite a short decision-to-delivery interval. However, whether the bradycardia-to-delivery interval could be adopted as part of the clinical governance of the standard of practice remains to be proven in prospective studies in the future.

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© 2009 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved.