DCC-ET-Caesar: Feasibility and safety of delayed cord clamping with ex-utero transfusion in elective caesarean deliveries – A pilot study

Introduction

Delayed cord clamping (DCC) and placental transfusion techniques have been associated with improved neonatal outcomes, including enhanced haemodynamic stability and increased haemoglobin levels.^1,2 Physiologically based cord clamping (PCC) is a method of umbilical cord management that delays clamping until the newborn’s lungs have aerated, pulmonary gas exchange has begun, and pulmonary blood flow has increased. This approach ensures a smoother cardiovascular transition at birth by maintaining placental circulation until the neonate establishes independent respiration. It is particularly helpful as it helps the neonate in adjusting to the extra-uterine environment.^1,2 It has been mainly studied in pre-term neonates where, while receiving support, including for those needing resuscitation, the umbilical cord is clamped only after the baby is stabilized. ³ Delayed umbilical cord clamping (DCC) has been widely advocated for its benefits in improving neonatal iron stores and reducing anaemia in infancy. ⁴ While multiple studies support physiologically based cord clamping methods in pre-term births needing stabilization, limited data exist on its feasibility and safety in elective caesarean sections. The optimal timing of clamping, particularly after complete cessation of blood flow as confirmed by Doppler ultrasonography, warrants investigation. This pilot study, the DCC-ET-Caesar Study, evaluates the feasibility and safety of DCC after Doppler-confirmed cessation of umbilical blood flow in term elective caesarean deliveries. Should the technique prove feasible and safe, a randomized controlled trial would be essential to evaluate the impact of this approach on clinical outcomes.

Methods

This was a prospective, single-arm pilot feasibility study conducted to evaluate the safety, feasibility, and preliminary outcomes of physiology-guided delayed cord clamping with ex-utero transfusion (DCC-ET) in term elective cesarean deliveries. Additionally, an exploratory comparison was made with a historical cohort of neonates delivered via elective cesarean section at the same institution, where a time-based delayed cord clamping protocol (approximately 60 seconds) was routinely practiced. The primary outcome was the feasibility of the DCC-ET protocol, defined by successful completion of the procedure without protocol deviation, the ability to perform continuous Doppler monitoring throughout, the absence of maternal or neonatal complications directly related to the procedure, and the acceptability of the technique by the clinical team. Secondary outcomes included neonatal haemoglobin and haematocrit levels at 48–72 hours of life, residual placental blood volume (RPBV), neonatal temperature at initial assessment, cord separation time, and maternal and neonatal adverse outcomes such as postpartum haemorrhage, need for neonatal resuscitation beyond initial stimulation, hypothermia, and NICU admissions.

Ethical approval from the institutional Ethical Committee was taken, vide reference no. AIIMS/BBN/IEC/MAY/2024/431-R. The study was registered in the Clinical Trial Registry of India, ref no. CTRI/2024/07/070137 [Registered on: 07/07/2024]. Eligible participants included women undergoing elective caesarean sections at ≥37 weeks’ gestation with singleton pregnancies. Exclusion criteria included multiple gestation, fetuses with prenatally detected major or minor anomalies, and emergency caesarean deliveries. The technique of delayed cord clamping utilized in this study, that is, delayed cord clamping with ex-utero transfusion (DCC-ET), is a modification of the method used by Welsh et al ⁵ and Landau et al. ⁶ After the delivery of the baby, a thorough inspection of the uterine incision was done to check for any bleeding sinuses or lacerations, or any extensions in the incision that needed immediate repair. All the bleeding points were duly secured, without prioritizing rapid cord clamping. All mothers received oxytocin (10 IU) administered intravenously immediately after the delivery of the anterior shoulder, as per standard clinical protocol for active management of the third stage of labour. The placenta was allowed to separate on its own, and when the signs of placental separation were evident, controlled cord traction was done to complete the placental removal. The newborn was handed over to the neonatal resuscitation team, still attached to the placenta through the umbilical cord. The placenta was kept at least 30 cm above higher level of the baby, to complete the process of placental transfusion. Due care was taken for routine care and continuous assessment of babies. Also, care was taken to avoid trauma to the placenta or cord insertion site of the newborn. Umbilical blood flow was assessed using colour Doppler and pulsed-wave Doppler ultrasound at an arbitrary fixed point approximately 10 cm from the neonatal cord insertion. Both umbilical arterial and venous flows were individually interrogated and identified based on their characteristic pulsatile (arterial) and continuous (venous) waveforms. The procedure involved intermittent Doppler assessments until complete cessation of either arterial or venous flow was confirmed. While arterial and venous flow presence or absence was recorded, the direction of flow (towards or away from the placenta) was not specifically monitored in this study (Figures 1 and 2). The umbilical cord was clamped only after complete cessation of arterial or venous flow at this point. The time interval between the uterine incision, delivery of the baby, clamping of the cord, and delivery of the placenta was measured with the help of stop stopwatch by a separate nursing team who were not involved in the study, and the duration of cord clamping was recorded by them. This timing commenced from the delivery of the last part of the fetus until the first clamp was applied to the cord.OPEN IN VIEWER

OPEN IN VIEWER

Figure 2.

The technique of DCC-ET used for the current study. (a) Waiting for the spontaneous placental separation f/b controlled cord traction, the neonate was handed over to the neonatal resuscitation team still attached to the placenta; (b) weighing the placenta, immediately after its delivery; (c), (d) placental transfusion and its assessment by Doppler; (e) the ultrasound machine equipped with Doppler used for the present study; (f) clamping of the cord by neonatology team, after Doppler-confirmed cessation of blood flow in umbilical cord; (g) weighing the placenta after cord clamping and completion of placental transfusion; (h) and (i) measurement of residual placental blood volume (RPBV).

The placenta was weighed twice, once immediately after spontaneous detachment and once after cord clamping following ex-utero transfusion. To minimize the inclusion of maternal blood in the measurement, the placenta was gently rinsed with sterile saline to remove excess blood clots and allowed to drain for approximately 30 seconds on a sterile, non-absorbent surface. During ex-utero transfusion, the placenta was held using sterile, rigid, non-absorbent trays to prevent fluid transfer to any cloth or gauze. Care was taken to avoid compression or trauma to the placenta that might artificially displace blood. Both measurements were taken using the same calibrated digital scale. Residual placental blood volume was measured immediately after cord clamping and placental separation. The placenta was placed in a sterile kidney tray, and residual blood was allowed to drain passively without applying external pressure. The collected blood was then measured using a sterile syringe to ensure precise volume estimation (Figure 2). This measurement was completed within 5 minutes of cord clamping to minimize clot formation and ensure accuracy. Cord separation time was recorded based on follow-up telephone interviews with the mothers, who were asked to report the day on which the umbilical cord stump spontaneously detached. This data point was collected to evaluate whether the technique of delayed cord clamping with ex-utero transfusion had any impact on the timing of cord detachment, which may have clinical relevance for neonatal care and infection monitoring. Neonatal parameters, including Apgar scores and vitals, were recorded. The decision of admission to the NICU was made by neonatology consultant as per unit policy. Neonatal axillary temperature was measured using a calibrated digital thermometer within the first 10 minutes after delivery, immediately following initial neonatal assessment by the resuscitation team. According to our institutional protocol, neonatal hypothermia is defined as an axillary temperature less than 36.5°C, in line with the World Health Organization (WHO) classification. Maternal parameters, such as estimated blood loss and postpartum complications, were also assessed by a separate obstetric team who did not involve in the study.

Feasibility in this study was defined by the following parameters ¹ : successful completion of the delayed cord clamping with ex-utero transfusion (DCC-ET) procedure without interruption or protocol deviation ² ; the ability to perform umbilical blood flow monitoring using Doppler throughout the procedure without significant technical difficulty ³ ; the absence of maternal or neonatal adverse events directly related to the procedure, such as cord rupture, uterine atony, or neonatal haemodynamic instability; and ⁴ acceptability of the protocol by the clinical team, assessed informally through staff feedback regarding the ease of implementation and integration into routine caesarean workflows.

Statistical analysis was performed using SPSS version 21 software (SPSS Inc., Chicago, IL, USA). Continuous variables were tested for normality using the Shapiro-Wilk test and presented as mean with standard deviation for normally distributed data or median with interquartile range for non-normally distributed data. Descriptive statistics were used to summarize maternal, neonatal, and placental characteristics. For comparison, we utilized a historical cohort of term elective caesarean deliveries conducted at our centre over the preceding 12 months. In this cohort, standard time-based delayed cord clamping (approximately 60 seconds) was practiced without ex-utero transfusion. Comparison between the study cohort and the historical cohort was conducted using the independent samples t-test for normally distributed continuous variables and the Mann-Whitney U test for non-normally distributed variables. Categorical variables were compared using the Chi-square test or Fisher’s exact test as appropriate. A p-value of less than 0.05 was considered statistically significant, and 95% confidence intervals were reported where applicable.

Results

A total of 44 participants were recruited after taking informed consent. The procedure could be completed in 40 out of these, as two patients were excluded, due to extension of the uterine incision, causing excessive bleeding intra-operatively; for two patients, we had to abandon the procedure, because of non-availability of ultrasound machine, making Doppler assessment difficult. The socio-demographic details of the included patients are mentioned in Table 1. The mean time to cord clamping was significantly longer in the DCC-ET group (6.60 ± 1.91 minutes vs 1.33 ± 0.28 minutes; p = 0.001). The mean total surgical time from skin incision to closure was 66.73 ± 6.91 minutes in DCC-ET group, comparable between groups (p = 0.568). There was no significant difference in the weight of the placenta immediately after delivery (p = 0.087), but the weight of the placenta after cord clamping was significantly lower in the DCC-ET group (407.75 ± 67.65 g vs 491.25 ± 51.20 g; p = 0.001), reflecting reduced residual placental blood volume (RPBV) (11.40 ± 2.56 mL vs 45.91 ± 13.01 mL; p = 0.001). The mean time taken for the physiological separation of umbilical cord was 2.95 ± 0.68 days.

OPEN IN VIEWER

Table 1.

The socio-demographic profile of the participants included in the present study.

Parameter	DCC-ET Caesar group (n = 40) Mean ± SD	DCC at 1-minute group (n = 40) Mean ± SD	p value
Age	26.60 ± 4.04 years	26.50 ± 4.17	0.914
Maternal height (cm)	149 ± 5	156 ± 4.6	0.001
Maternal weight (kg)	79.70 ± 6.09	75.78 ± 5.08	0.160
Maternal BMI (kg/m2)	35.89 ± 3.69	32.02 ± 5.24	0.001
Weight of the baby in kg	2.99 ± 0.32	2.96 ± 0.34	0.488
Length of the baby in cm	50.88 ± 1.64	50.13 ± 1.62	0.078
Head circumference of the baby in cm	33.13 ± 1.44	32.75 ± 1.46	0.266

Neonatal cord separation occurred earlier in the DCC-ET group (2.95 ± 0.68 days vs 4.43 ± 0.78 days; p = 0.001). Apgar scores at 1 minute were similar, while Apgar scores at 5 minutes were slightly higher in the DCC-ET group (p = 0.036). Neonatal haemoglobin at 48–72 hours was comparable between groups (p = 0.838), but neonatal haematocrit was significantly higher in the DCC-ET group (61.25 ± 2.39% vs 55.81 ± 5.41%; p = 0.001). There were no cases of neonatal hypothermia or infants with Apgar scores less than 4 at 1 or 5 minutes in either group. Phototherapy requirements were minimal and not significantly different between groups (Table 2). No significant postpartum haemorrhage or maternal complications was observed. In the DCC-ET group, the mean maternal blood loss during cesarean was significantly lower compared to the 1-minute DCC group (415.48 ± 36.64 mL vs 323 ± 88.24 mL; p = 0.001). Postoperative maternal haemoglobin and haematocrit were significantly better preserved in the DCC-ET group (Hb: 11.18 ± 1.26 g/dL vs 10.12 ± 1.03 g/dL; HCT: 32.75 ± 1.17% vs 29.93 ± 2.03%; p = 0.001 for both), with less drop in haemoglobin from preoperative to postoperative day 1 (0.72 ± 0.36 g/dL vs 1.31 ± 0.60 g/dL; p = 0.001).

OPEN IN VIEWER

Table 2.

Post-delivery maternal and neonatal parameters.

	DCC-ET group				DCC at 1 minute			p value
	Mean	SD	Median	IQR	Mean	SD	Z
Maternal parameters
Amount of blood loss in CS (ml)	415.48	36.64	415	390–450	323	88.24	−6.122	0.001
Weight of placenta after delivery (g)	451.03	101.09	450	360–510	448.87	52.8	−5.567	0.087
Weight of the placenta after clamping of umbilical cord (g)	407.75	67.65	410	350–450	491.25	51.20	−5.240	0.001
Residual blood volume in the placenta (ml)	11.40	2.56	11	9–13	45.91	13.01	16.456	0.001
Time from uterine incision to uterine closure (minutes)	6.12	1.81	6	4.625–7.4125	11.60	2.53	11.127	0.001
Total surgical time (minutes)	66.73	6.91	67.5	60–72	65.85	6.73	−0.574	0.568
Preoperative Hb	11.92	1.34	11.7	10.975–13.05	11.42	1.06	−1.833	0.071
Preoperative HCT	33.55	0.85	33.6	32.825–34.175	31.96	2.88	−3.340	0.001
Postoperative Hb (at 24 hours post-op)	11.18	1.26	10.9	10.05–12.1	10.12	1.03	−4.121	0.001
Postoperative HCT (at 24 hours post-op)	32.75	1.17	32.75	32.2–33.375	29.93	2.03	−7.617	0.001
Change in maternal Hb from pre-op to post-op day 1	0.72	0.36	0.7	0.5–0.9	1.31	0.60	5.267	0.001
Neonatal parameters
Time from birth of baby to cord clamp (minutes)	6.60	1.91	7	5–8	1.33	0.28	−17.317	0.001
Physiological separation of umbilical cord baby (days)	2.95	0.68	3	3–3	4.43	0.78	9.024	0.001
Apgar score at 1 min/10	8.80	0.56	9	8–9	8.80	0.56	0.000	1.000
Apgar score at 5 min/10	9.75	0.44	10	9.25–10	9.50	0.60	−2.130	0.036
Neonatal peripheral venous Hb (48–72 hours)	19.52	2.28	19.3	18.2–21.1	19.41	2.62	−0.205	0.838
Haematocrit peripheral venous (48–72 hours)	61.25	2.39	60.8	59.425–63.025	55.81	5.41	−5.092	0.001
How long was phototherapy required (days)	0.28	0.72	0	0–0	0.25	0.78	−0.150	0.881
Neonatal hypothermia	None	—	—	None	—	—	—	—
Number of infants with Apgar score less than 4 at 1 and 5 minutes	None	—	—	None	—	—	—	—

In terms of its feasibility, we found that DCC-ET until complete cessation of umbilical cord blood flow, as confirmed by Doppler, is a feasible approach. No maternal or neonatal adverse events were noted in relation to the procedure. Specifically, no cases of cord rupture, uterine atony requiring additional intervention, or neonatal haemodynamic instability were observed. Monitoring via Doppler was practical and provided an objective assessment of cord circulation status. No significant adverse maternal or neonatal outcomes were observed with this approach. Neonates exhibited stable transitional circulation, with no increased incidence of polycythaemia, hyperbilirubinemia requiring treatment, or haemodynamic instability. Maternal outcomes, including postpartum haemorrhage rates, were comparable to standard DCC protocols. Overall, this method of DCC appears to be both feasible and safe, warranting further large-scale studies to validate its clinical benefits.

Discussion

This study explores the feasibility and safety of delayed cord clamping with ex-utero transfusion (DCC-ET) after physiologic placental separation and complete cessation of umbilical cord blood flow, as confirmed by Doppler. In this study, we used a two-phase approach to delayed cord clamping. The first phase involved standard delayed cord clamping with the placenta still attached to the uterus while the newborn remained in utero or was handed over to the neonatal team with the cord intact. The second phase, ex-utero transfusion, was initiated after placental separation and delivery. The placenta was elevated approximately 30 cm above the neonate to facilitate continued placental transfusion until cessation of umbilical blood flow was confirmed by Doppler. The rationale for combining both phases was to maximize placental transfusion time while allowing adequate opportunity for surgical inspection and haemostasis, which is critical during caesarean deliveries. We believe this combined method may offer additional advantages by ensuring a longer and potentially more complete placental transfusion compared to either method alone. However, this pilot study was not designed to compare the efficacy of the combined method against standard delayed cord clamping or ex-utero transfusion in isolation. Future randomized controlled trials are planned to directly assess and compare these approaches.

Traditional DCC practices recommend waiting for a fixed duration (typically 30–60 seconds to a few minutes),^7–13 whereas this approach individualizes clamping based on objective haemodynamic parameters, potentially optimizing neonatal transitional circulation. Our findings suggest that waiting for complete cessation of blood flow, rather than relying on a predefined time frame, is a feasible and safe strategy. The use of Doppler ultrasonography provided a clear, non-invasive method to confirm cessation, allowing a standardized approach to determining the ideal clamping time. While this method required additional monitoring, it did not introduce significant delays that would interfere with standard delivery room practices. The variation in time until blood flow cessation across neonates highlights the individual nature of placental transfusion, reinforcing the need for a physiologic, rather than time-based, approach.^14–16 Although the interquartile range for the present study was 5–8 minutes, in one neonate we found that flow was still evident till 11 minutes and 30 seconds. The potential benefits of enhanced neonatal iron stores and improved haematological parameters support further investigation through larger randomized trials. The approach of DCC-ET allows for an uninterrupted placental transfusion, ensuring the baby receives the full benefit of its residual blood supply.

In our hospital, the recorded rates of neonatal adverse outcomes (including the need for resuscitation beyond initial stimulation, neonatal intensive care unit [NICU] admission, and hypothermia) following standard elective caesarean sections with time-based DCC are approximately 5% for NICU admissions, 2% for need for advanced resuscitation, and 4% for neonatal hypothermia. Maternal adverse outcomes (such as postpartum haemorrhage, surgical site infection, and uterine atony) occur in approximately 3–4 % of elective caesarean deliveries. In our study cohort using delayed cord clamping with ex-utero transfusion (DCC-ET), there were no observed increases in these adverse outcomes compared to the hospital’s routine rates. No significant maternal or neonatal complications were observed with this strategy. Neonates tolerated the extended DCC period well, with no increased incidence of adverse outcomes such as polycythaemia or hyperbilirubinemia requiring phototherapy. Haemodynamic stability was maintained, suggesting that allowing complete cessation of cord blood flow does not impose risks of over-transfusion. Maternal safety was also preserved, with no observed increase in postpartum haemorrhage rates compared to conventional DCC protocols. In corroboration with few studies, this reassures that waiting for physiologic cessation of blood flow does not prolong the third stage of labour to a clinically concerning extent.^17,18

Conclusion

The present pilot study demonstrates that delayed cord clamping with ex-utero transfusion (DCC-ET) is a feasible and safe procedure during elective caesarean deliveries. The protocol was successfully implemented in majority of cases, with no increase in maternal or neonatal complications and acceptable integration into routine clinical practice. Doppler assessment of umbilical blood flow provided a practical method to individualize cord clamping timing, although variability in time to flow cessation between participants highlighted the need for a physiology-guided, rather than time-based, approach. Further randomized controlled trials are required to compare this combined method with standard delayed cord clamping and isolated ex-utero transfusion to better understand potential additional benefits and to refine best practices for neonatal transition.