Early Human Development 91 (2015) 407–411

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Effect of delayed cord clamping (DCC) on breathing and transition at birth in very preterm infants Elizabeth Nevill a, Michael P. Meyer a,b,⁎ a b

Neonatal Unit, Kidz First, Middlemore Hospital, Otahuhu, Private Bag 93311, Auckland, New Zealand Department of Paediatrics, University of Auckland, Private Bag 92019, Auckland 1142, New Zealand

a r t i c l e

i n f o

Article history: Received 12 January 2015 Received in revised form 16 April 2015 Accepted 29 April 2015 Available online xxxx Keywords: Delayed cord clamping Preterm infants Outcomes Neonatal transition Resuscitation

a b s t r a c t Background: The effects of delayed cord clamping (DCC) on transition in preterm infants are important as this procedure is becoming increasingly recommended. The aim of this study was to compare the effects of DCC with an historical cohort. Method: In this observational study, outcomes for infants ≤29 weeks were compared with a group born before the introduction of DCC. The intended intervention was DCC for 40 s. Primary outcomes were the need for resuscitation and intubation in infants undergoing DCC, whilst taking note of their breathing during the procedure. Neonatal morbidities were analysed, including the association between breathing during DCC and outcome. Results: There were 62 infants in the DCC group, and 62 who received immediate cord clamping (ICC). Maternal and infant characteristics including gestational age (p = 0.76) and birth weight (p = 0.74) between groups were not significantly different. 70% of the DCC group breathed regularly at birth. Comparing the DCC and ICC groups, there was no significant difference in 1 min and 5 min Apgar scores or in the number requiring intubation at birth (p = 0.88). Likewise, admission temperatures were similar (p = 0.57). There was a significant increase in the rate of chronic lung disease in the DCC group (p = 0.013). When comparing the infants who breathed during DCC with the non-breathers; the non-breathing group was more likely to be intubated (p = 0.01), have chronic lung disease (p = 0.02), and severe intraventricular haemorrhage (p = 0.02). Conclusion: DCC in these very preterm infants was well tolerated and the majority established spontaneous respiration whilst DCC was occurring. Infants who did not breathe during DCC had worse outcomes. © 2015 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Delayed cord clamping (DCC) and the effects this has on transition at birth in preterm infants are important as this procedure is becoming increasingly recommended [1–6]. Recent investigations support DCC as a safe and achievable practice for preterm infants [7–9]. Individual studies and a meta-analysis reported fewer blood transfusions, less intraventricular haemorrhage (IVH) and a reduction in the risk for necrotising enterocolitis (NEC) but increased serum bilirubin levels following DCC [7,8,10–12]. Other benefits such as a reduction of late onset sepsis [13], and improved cerebral blood flow and oxygenation [14–19] have likewise been reported. Recent attention has focused on the haemodynamic effects of an intact placental bed whilst the transitional circulation shifts from a high to a low pulmonary resistance. Better understanding of the physiology at this important time may help explain the observations of increased haemodynamic stability following DCC in preterm infants ⁎ Corresponding author. Tel.: +64 9 2760000; fax: +64 9 2760091. E-mail addresses: [email protected] (E. Nevill), [email protected] (M.P. Meyer).

http://dx.doi.org/10.1016/j.earlhumdev.2015.04.013 0378-3782/© 2015 Elsevier Ireland Ltd. All rights reserved.

[15,16]. Animal work has demonstrated the importance of establishing ventilation before cutting the cord, allowing for a smoother transition in cerebral blood flow [18]. DCC was introduced as a standard practice in our institution, on the basis of existing evidence from meta-analysis [5]. We carried out an audit to describe the condition and the breathing effort of very preterm infants during the procedure, the resuscitation measures they received and their neonatal outcomes compared to a historical cohort. DCC — delayed cord clamping, ICC — immediate cord clamping, NEC — necrotizing enterocolitis, CLD — chronic lung disease, and IVH — intraventricular haemorrhage. 2. Method We introduced a neonatal guideline to facilitate 40 s of DCC as standard practice for all infants born ≤34 weeks. We commenced our study 6 months after introduction of DCC to allow for a period of adaption. In addition, 15 patients, part of a previous report examining blood flow to the upper body [16] were excluded so to avoid duplication. During the study period from November 2011 to October 2012, inborn infants ≤ 29 weeks were eligible for inclusion. The historical


E. Nevill, M.P. Meyer / Early Human Development 91 (2015) 407–411

p value

using Mann–Whitey U whilst categorical variables were compared using Pearson chi-square. Binary logistic regression with severe IVH as an outcome and covariates of delivery mode, birth weight, gestation, gender, and presence of breathing during DCC was carried out.

27 (23–32)



33 (53) 22 (35) 7 (11) 46 (74) 13 (21) 11 (18) 12 (19) 38 (61) 14 (22) 11 (18) 33 (53) 34 (55) 27 (25–29) 1000 (796–1306) 8 (13)

0.59 0.33 0.79 0.70 0.83 0.65 0.07 0.71 0.16 0.62 0.05 0.78 0.76 0.74 0.20

Table 1 Maternal and infant characteristics for preterm infants receiving either delayed or immediate cord clamping. Data are shown as median (IQR) or number (%). Delayed cord clamping n = 62 Maternal age 25.5 (21–32) (years) Antenatal steroids Completed 37 (59) Incomplete course 16 (26) None 9 (14) Preterm labour 44 (71) PROM 14 (22) PIH 13 (21) APH 5 (8) Antibiotics in labour 40 (64) Chorioamnionitis 21 (34) Twins 8 (13) Caesarean section 21 (34) Male 36 (58) Gestation (weeks) 28 (25–29) Birth Weight (g) 985 (813–1310) IUGR 2 (3)

Immediate cord clamping n = 62

PROM: preterm rupture of membranes N24 h. PIH: pregnancy induced hypertension. APH: antepartum haemorrhage. Chorioamnionitis: based on placental histology. IUGR: birth weight b10% percentile.

cohort was born in the period January 2008 to December 2009 before the introduction of DCC. Cord milking or stripping was not routinely carried out but was allowed based on the judgement of the medical team [1,20–22]. Milking the umbilical cord involved actively milking blood in the cord towards the infant, three to four times [4,6, 21], whilst cord stripping involved clamping the cord approximately 20 cm from the umbilicus, unravelling the vessels and stripping the blood in the cord towards the infant [20]. This observational study was planned for infants exposed to the implemented DCC guideline we described above. Infants in the study group were observed so that their breathing could be described but did not receive intervention to initiate or support spontaneous breathing during the procedure. Infants born by caesarean section and vaginal birth were included. The attending neonatal team requested and timed the DCC using the Apgar score timer. The obstetric team provided supportive information and clamped the cord. Infants were positioned at the level of the introitus on the bed for vaginal deliveries; and on maternal thighs at caesarean section deliveries. Thermal wrap was used in all cases. The neonatal resuscitation team leader observed the infant's breathing effort and later completed the birth record. After 40 s, infants were transferred to the radiant warmer for transition and stabilisation. Resuscitation measures were based on ILCOR guidelines [3]. Infants were transferred to the neonatal unit on a radiant warmer, equipped with an uninterrupted power supply. Axillary admission temperatures were obtained as per study centre guidelines. One of the authors (MM) collected data from the attending team member who observed the infants' breathing status during the intervention. Time to first gasp and time to established breathing as well as the timing of cord clamping was recorded in the birth summary for both groups. This study met ethical guidelines as an audit activity and received institutional approval. Statistics Primary data analysis was carried out on the basis of the cohorts in which the infants were born (although not all infants in the DCC cohort received the intervention). The IBM SPSS Statistics 19 programme was used for analysis. Non-parametric data was analysed

Sixty-two infants were eligible for the study during the period DCC was performed. In addition, by chance, there were also 62 infants in the historical control cohort who received immediate cord clamping (ICC). Forty-six (74%) infants in the study group actually received DCC. The reasons for the 16 (26%) infants not receiving the intervention included late calls to the attending team, delivery in other parts of the hospital than delivery suite, one case each of placental abruption and cord prolapse and a set of twins delivered by emergency caesarean section (the procedure was not contraindicated in this case but was not done). Six infants received longer than 40 s DCC (5 received 45 s whilst one received 60 s). Two infants received less than the planned 40 s DCC (1 received 25 s and one 30 s). In 7 infants cord milking or stripping was performed. Maternal and infant characteristics are shown in Table 1 below. Patient characteristics between the groups were similar, we did however observe a higher proportion of caesarean section deliveries in the ICC group (p = 0.05); the reasons for which are not clear. Table 2 shows outcomes during transition. There were no significant differences between the groups for breathing at birth or during the procedure, the need for positive pressure ventilation or intubation in the delivery room. Likewise Apgar scores at 1 and 5 min and admission temperatures as well as base deficit on admission to the unit were similar. Neonatal outcomes are shown in Table 3. Of note, the receipt of phototherapy was not significantly higher in the DCC group. Day one haemoglobin levels in the DCC group were significantly higher (p = 0.01). We observed an increase in chronic lung disease (defined as the need for respiratory support or oxygen at 36 weeks corrected gestational age) in the DCC group; however there was no difference between the groups in the percentage discharged home on oxygen. Physiologic testing for bronchopulmonary dysplasia [23] was not carried out. When we evaluated breathing during DCC we found that of the 46 infants that received DCC, 34 infants breathed, whilst 12 did not breathe (Table 4). Maternal data for the infants who breathed compared to the infants who did not breathe were similar. In particular, there were no significant differences (p N 0.05) in percentages of women with preterm labour, prolonged rupture of membranes, pregnancy induced hypertension, antepartum haemorrhage, antenatal growth restriction or, antibiotics received in labour. Chorioamnionitis rates

Table 2 Events during transition in preterm infants receiving either delayed or immediate cord clamping. Data are shown as median (IQR) or number (%). Delayed cord clamping n = 62 Breathed at birth / during the 43 (69) procedure Apgar score 1 min 5 (4–6) Apgar score 5 min 7 (6–9) Need for positive pressure 29 (47) ventilation Intubation in delivery room 19 (31) Admission temperature, °C 36.75 (36.4–36.9) Worst base deficit on admission −2.5 (−6.2–0.0)

Immediate cord clamping n = 62

p value

42 (67)


5 (3–6) 8 (6–9) 38 (61)

0.98 0.52 0.45

15 (24) 36.85 (36.3–37.1) −1.0 (−6.0–0.0)

0.55 0.43 0.27

E. Nevill, M.P. Meyer / Early Human Development 91 (2015) 407–411 Table 3 Neonatal outcomes in preterm infants receiving either delayed or immediate cord clamping. Data shown as median (IQR) or number (%) CLD: chronic lung disease: respiratory support or oxygen at 36 weeks. Delayed cord clamping n = 62 Haemoglobin day 1 g/L Phototherapy Age at first blood transfusion (days) Blood transfusion Number of blood transfusions Surfactant Ventilated days CPAP days CLD Home oxygen NEC ROP stage 3 LOS IVH PDA treated Death

Immediate cord clamping n = 62

p value

164.00 (146.5–182.7) 154.00 (138.5–166.0) 0.01 56 (90) 49 (80) 0.10 15 (4–23) 10 (2–24) 0.08 23 (37) 0 (0–1) 29 (47) 1 (0–3.5) 37.5 (10.7–53.7) 20 (32) 3 (4.8) 2 (3.2) 4 (6.5) 13 (21) 12 (19) 20 (32) 12 (19)

33 (53) 1 (0–2) 24 (39) 0.9 (0–6.2) 27.5 (6.7–47.2) 9 (14) 3 (4.8) 7 (11) 6 (9.6) 19 (30) 13 (21) 19 (31) 11 (18)

0.05 0.70 0.37 0.13 0.12 0.02 1.000 0.09 0.51 0.22 1.00 0.85 0.82

NEC: necrotising enterocolitis Bell stage 2 or more. ROP: retinopathy of prematurity treated with laser therapy. LOS: late onset sepsis (N48 h of age). IVH: intraventricular haemorrhage. PDA: patent ductus arteriosus treated.

(based on placental histology) were similar between groups. The median gestational age between the groups (p = 0.48) was likewise not significantly different. A significant proportion of the infants in the non-breathing group required intubation in the delivery room (*p = 0.006) and had lower 1 min Apgar scores (p b 0.001). They were more likely to be male, had lower day 1 haemoglobin levels, and were more likely to develop chronic lung disease and severe IVH. Binary logistic regression with severe IVH as an outcome indicated that the only significant factor was whether or not the infant breathed during the procedure. In a secondary analysis we compared the outcomes for the 7 infants that received cord milking and stripping with the DCC cohort 46 (74%) that actually received DCC and found no significant differences between the groups for Apgar scores at 1 min (p = 0.14) and 5 min (p = 0.90), receiving a blood transfusion (p = 0.8), all grades of IVH (p = 0.21), CLD (p = 0.56), home oxygen (p = 0.56), ROP stage 3 (p = 0.50), NEC (p = 0.55), or type and duration of respiratory support received. 3. Discussion The implementation of delayed cord clamping in this group of preterm infants appeared to be well accepted amongst medical and nursing staff. In the initial stages we found frequent case evaluations to discuss practical aspects around transition to be important. We noted that the procedure was unlikely to be undertaken if neonatal staff were not in attendance to plan the procedure beforehand. Our results indicated that the majority of very preterm infants breathed during DCC and that there was no adverse effect of DCC on the need for resuscitation or intubation in the delivery room. Apgar scores, admission temperatures and base deficits were not significantly different between groups, suggesting that the procedure was well tolerated. (In 7 infants cord milking or stripping was carried out, which allowed earlier attention to resuscitation.) In a small randomised controlled trial where delayed cord clamping was compared with immediate clamping in infants 24–27 weeks, Oh et al. [11] recorded similar events during transition to those we have described. In addition, in a meta-analysis, there were no significant differences in Apgar


scores in preterm infants subject to immediate or delayed cord clamping [12]. Apart from this, there is a paucity of literature describing breathing status or resuscitation measures in preterm infants receiving either DCC or cord milking [4,22]. Haemoglobin levels on day one for the infants receiving DCC were significantly increased; suggesting transfusion occurred [11]. Fewer infants in our study received blood transfusions after DCC, similar to published reports [12]. Avoiding blood transfusions [10] along with improved tissue perfusion following DCC have been implicated in the prevention of necrotizing enterocolitis (NEC) [12,13,24]. In addition to transfusion-limiting practices, we introduced probiotics and lactoferrin in 2011 as prophylaxis against NEC [25,26]. The observed trend towards a reduction in NEC in our DCC cohort could therefore be related to other changes in practice. We found an increase in chronic lung disease following introduction of DCC, the reasons for which are unclear. Results from randomised trials comparing ICC and DCC have not confirmed this finding, and a meta-analysis has shown a trend towards a reduction in the incidence of chronic lung disease [12]. Red blood cell transfusion criteria remained consistent for both our study groups, so this is unlikely to have been responsible. Another potential confounding factor in our study was the change from the routine use of erythropoietin in the time period ICC was performed to selected use for our DCC group [27]. An observational study has linked cessation of erythropoietin use to increased chronic lung disease [27,28]. Other neonatal outcomes including late onset sepsis, retinopathy of prematurity and death in our study cohort were similar in the two groups. A small number of studies have reported on these outcomes and no significant differences were noted [12]. The infants who did not breathe during DCC (although a relatively small subgroup with a higher proportion of males) had worse outcomes (Table 4). This could be because they suffered some form of insult such as hypoxia during delivery or because the fact that they were not breathing affected their transition and subsequent outcomes. There

Table 4 Data for breathing infants compared to infants who did not breathe during delayed cord clamping. Data are shown as median (IQR) or number (%). Breathing n = 34 Antenatal Steroids: Completed Incomplete course None Caesarean section birth Male Gestation weeks Birth weight (g) IUGR (birth weight b10% percentile) Twins Apgar score, 1 min Apgar score, 5 min Intubation at delivery Worst BD on admission Haemoglobin day 1 g/L Surfactant Ventilated days CPAP days CLD Inotropes for hypotension Treated PDA IVH Grades 1 & 2 IVH Grades 3 & 4 IVH all grades Death

Not breathing n = 12

21 (62) 10 (29) 3 (9) 12 (35) 14 (41) 28 (25–29) 1005 (887–1341) 2 (5.8)

8 (67) 4 (33) 0 4 (33) 10 (83) 26.5 (25–29) 819 (726–1250) 1 (8)

3 (8.8) 5 (5–6) 8 (6–9) 10 (29) −2.5 (−7.2–0.0) 165 (151–183) 14 (41) 0.45 (0–2) 40.5 (14.2–52.2) 10 (29) 7 (21) 13 (38) 4 (12) 2 (6) 6 (18) 4 (12)

1 (8) 4 (2–4) 6 (5–7) 9 (75) −3.5 (−6.7–0.0) 144 (137–181) 7 (58) 1 (1–9) 45 (25.7–67) 7 (58) 2 (17) 4 (33) 1 (8) 4 (33) 5 (41) 3 (25)

CLD: chronic lung disease: respiratory support or oxygen at 36 weeks. IVH: intraventricular haemorrhage. PDA: patent ductus arteriosus treated.

p value 0.77 0.82 0.08 1.00 0.02 0.48 0.22 0.77 0.16 b0.001 0.092 0.006 0.98 0.003 0.32 0.05 0.46 0.02 0.77 0.77 0.75 0.02 0.1 0.3


E. Nevill, M.P. Meyer / Early Human Development 91 (2015) 407–411

was no evidence of preceding hypoxia in terms of antenatal events and peripartum heart rate monitoring and cord gas base deficits on admission were similar in both groups (p = 0.98). In addition, there were no significant differences in maternal characteristics between the groups, including the use of antenatal steroids (our rates for completed steroids are similar to those of Australia New Zealand Neonatal Network (ANZNN) overall, although figures for any antenatal steroid received are somewhat lower [29]). Ersdal and colleagues studied a large cohort of term and preterm infants and noted that the probability of death or admission to the newborn nursery was greatly reduced in infants who established respiration prior to cord clamping [2]. In their study logistic regression indicated that the length of time of spontaneous respiration before cord clamping was a major indicator of outcome. They found little evidence that birth asphyxia played a role in these infants' outcomes. Whilst other studies do not appear to have described the breathing pattern of preterm infants undergoing DCC, there is evidence from animal studies of the importance of ventilation prior to cord clamping. In a study of preterm lambs, animals that were ventilated first (as compared to a group where the cord was clamped prior to establishing ventilation) had a more stable cardiovascular transition [18]. This resulted in less fluctuation in carotid artery flow and pressure in the ventilated first group, potentially allowing more stable cerebral perfusion. Avoiding fluctuations in cerebral perfusion is especially important in preterm infants, partly because of limited auto regulation of cerebral blood flow. It has been found that a period of decreased cerebral perfusion in the first 12–24 h after birth followed by reperfusion is associated with IVH [30]. Using flow in the superior vena cava as a proxy for cerebral blood flow, it has been shown that low flow in the first 24 h predisposes to IVH [30]. DCC is associated with a reduction in the number of preterm infants with low superior vena cava flow [16,17,22]. These circulatory improvements may help explain the reduction in IVH as a consequence of DCC noted in some randomised trials [13,31]. Whilst we did not find an overall reduction in the incidence of IVH with DCC, our findings indicate that establishing respiration in conjunction with DCC is important. As such our data provides clinical support for the findings from the lamb study noted above. The observational nature of our current study results in a number of limitations. There were changes in practice between the groups as noted above. In addition 26% of our study group did not receive the DCC intervention. Comparing outcomes for breathers with the non-breathers resulted in groups with small numbers and as such the findings should be interpreted with caution. Our preliminary observations require confirmation with larger groups. 4. Conclusion Overall the comparison of DCC and ICC groups showed that delayed cord clamping was well tolerated during transition in very preterm infants. The majority of patients breathed during DCC with no effect overall on the need for resuscitation and intubation. The association between DCC and CLD has not been noted before and may reflect other changes in neonatal practice. Infants who did not breathe during DCC appeared to have worse outcomes including an increase in severe IVH, which may relate to reduced cardiovascular stability. This clinical audit provides support for the application of DCC into clinical practice, indicating that it is well tolerated in the majority of early gestation infants. Further research is needed for those infants who fail to breathe during transition and DCC. Conflict of interest The authors declare that they have no conflict of interest.

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Effect of delayed cord clamping (DCC) on breathing and transition at birth in very preterm infants.

The effects of delayed cord clamping (DCC) on transition in preterm infants are important as this procedure is becoming increasingly recommended. The ...
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