ETHICS/EDUCATION
Delayed cord clamping
Savvas Argyridis
Abstract
Timing of cord clamping is believed to greatly affect placental transfu-
sion rate and therefore neonatal and infant circulation. Delayed cord
clamping of 30e60 seconds after birth, in combination with neonatal
position at the level of placenta, respirations and uterine contractility
increase haemoglobin and lower iron deficiency rate in both term
and preterm infants. In preterm neonates, there is evidence on
increased cardiovascular stability and a possible reduction of intraven-
tricular haemorrhage and necrotising enterocolitis as well as need of
blood transfusion. Adverse neonatal effects include increase of jaun-
dice requiring phototherapy, without any adverse maternal effects re-
ported, such as postpartum haemorrhage or anaemia. A possible
adverse effect is the reduction of total nucleated cells during umbilical
cord blood collection. Long term neurodevelopment has been
assessed in term neonates, and a possible improvement of fine-
motor and social domains in four years of life has been reported.
Cord milking is an alternative technique to delayed cord clamping
and as studies show, infant outcomes are at least comparable to
delayed clamping. Delayed cord clamping of 30e60 seconds is there-
fore recommended, in both term and preterm neonates, provided there
are no contra-indications and phototherapy facilities are available.
Keywords cord milking; delayed cord clamping; early cord clamping;
placental transfusion
Introduction
One of the most important aspects of intrapartum care is the
provision of adequate arterial oxygen to meet the demands of the
neonatal circulation. This is achieved by increased placental
transfusion, the transfer of placental blood to the neonate within
the first few minutes of life. Approximately a third of the blood
volume circulating in the fetomaternal unit, is contained in the
placenta. Various methods are in use to enhance blood trans-
fusion; they include delayed cord clamping, cord milking, posi-
tioning of the neonate at the level or below the placenta,
stimulation of neonatal respiration and enhancing uterine con-
tractions prior to cord clamping. Early studies suggest that
delayed cord clamping, either alone or in combination with other
techniques, results in 50% higher neonatal blood volume than
early clamping. About 80 ml (range 51e163 ml) of blood are
transfused in the first 5 minutes of life, if the cord is left intact,
which contributes to 20% of the total infant blood volume.
Technique and factors that affect placental transfusion
Delayed cord clamping requires delay in clamping for at least 30e
60 seconds in both term and preterm neonates, provided there is
Savvas Argyridis MD MSc PhD is a Consultant Obstetrician and
Gynaecologist, Archbishop Makarios III Hospital, University of
Nicosia, Cyprus. Conflicts of interest: none.
OBSTETRICS, GYNAECOLOGY AND REPRODUCTIVE MEDICINE --:-
Please cite this article in press as: Argyridis S, Delayed cord clamping, Obstetrics, Gynaecology and Reproductive Medicine (2017), http://
dx.doi.org/10.1016/j.ogrm.2017.08.003
no neonatal or maternal contraindications such as respiratory
depression or postpartum haemorrhage. Several time limits have
been assessed, ranging from 30 seconds to 5 minutes. Early
studies, suggest that the increase in neonatal blood volume is
proportional to the time delayed in both term and preterm neo-
nates. Venous and arterial blood flow occurs for longer period
than previously expected, as about 57% of venous flow occurs in
4:34 minutes and 43% of arterial flow in 5:16 minutes after birth.
Factors that may affect placental transfusion include neonatal
position, respirations and uterine contractions. Regarding
neonatal position, it is suggested that it should be at or below the
level of the placenta as the gravity effect expedites placental
transfusion to completion on 30 seconds while if the neonate is
placed on the maternal abdomen it will take twice as much time
to transfuse the same blood volume. Newer studies have refuted
this practice as they suggest that neonatal position does not affect
transfused blood volume. Uterine contractility is believed to be a
major determinant of blood flow, as the initial contraction that
expels the fetus contributes 25% and the following contractions
contribute to 50% of blood volume transfused. Spontaneous
breathing and respirations are responsible for negative intratho-
racic pressure and increased gradient between placental vessels
and feral right atrium, which in turn increase placental trans-
fusion. Umbilical arteries constrict approximately 45 seconds
after the onset of respirations but the umbilical vein remains
patent, which facilitates transfusion. Breathing movement is
more important in caesarean section deliveries, since uterine
contractility is absent. There are studies that assessed whether
positive pressure ventilation may enhance placental perfusion
but there is no statistically significant benefit compared to
spontaneous respirations.
Effects in term neonates
Placental transfer has been estimated at about 80 ml in 60 sec-
onds and at 100 ml in 180 seconds following delivery, while the
circulating blood volume between neonates and placenta is
80%e20% in 60 seconds and 87%e13% at time that pulsations
end. A randomised controlled trial that assessed placental re-
sidual blood volume following early and late clamping,
concluded that there is approximately 39.5% lower blood vol-
ume in the delayed group. A Cochrane review of 15 clinical trials
that included 3911 mothers and term neonates, compared the
maternal and neonatal outcomes of early (<60 seconds) and late
(>60 seconds) clamping. Results show that neonates in the early
clamping group had significantly lower haemoglobin level at
birth (mean difference 2.17 g/dL) and at 3e6 months of life,
infants from the early clamping group had significantly higher
risk of iron deficiency (RR, 2.65; 95% CI, 1.04e6.73). There was
no significant difference between the two groups regarding Apgar
score less than 7 in 5 minutes or neonatal mortality. The rate of
jaundice requiring phototherapy was significantly higher in the
late clamping group (4.36% compared to 2.74%), but overall
jaundice rate and polycythaemia was not significantly different
between the two groups. Maternal outcomes measured (severe
postpartum haemorrhage, use of uterotonics, blood loss) were
similar and were not affected by the cord clamping technique
implemented. With access to phototherapy it is suggested that
delayed cord clamping is of proven benefit compared to early
1 Ó 2017 Elsevier Ltd. All rights reserved.
 ETHICS/EDUCATION

clamping. A Cochrane update, has concluded that the need for
phototherapy is significantly increased in the delayed clamping
group (RR 0.59, 95% CI 0.38e0.92) as the mean haemoglobin
levels has a mean weighted difference of 2.17 g/dl between the
two groups. A study that assessed arterial and venous umbilical
cord gases, bicarbonate, base excess and lactate between early
and delayed cord clamping, concluded that there is an increase of
lactate and PaCO2 as well as a decrease of PaO2, bicarbonate and
base excess in the delayed clamping group.
Long term neurodevelopment was assessed in delayed
clamping infants and children. A randomized controlled trial
evaluated 382 infants at 1 and 4 years and reported that although
there is no significant difference in 12 months, there is signifi-
cantly better fine-motor and social domains at 4 years, following
delayed cord clamping.
assists lung expansion that helps to initiate breathing; especially
in preterm neonates born via caesarean section. Another trial
that assessed milking prior to clamping in preterm neonates re-
ported improvement of haemodynamic stability as measured by
mean blood pressure and the initial haematocrit. The need for
red cell transfusion was lower. A randomized trial that compared
the two techniques in term infants, reported that there is no
significant difference in ferritin and haemoglobin six weeks
postpartum.
Delayed cord clamping and umbilical cord blood collection
If delayed cord clamping is performed and cord blood collection
follows there seems to be a reduction in mean volume and the
total nucleated cells collected, compared with early clamping and
immediate blood collection.

Effects in preterm neonates

Conclusions
In preterm neonates, there are concerns regarding the possible
Delayed cord clamping for about 30e60 seconds seem to be
beneficial effects of delayed clamping. A Cochrane review of 15
beneficial for both term and preterm infants, and should be
studies that assessed 738 neonates between 24 and 36 weeks,
recommended, except in the presence of neonatal or maternal
concluded that although there is a trend towards reduction in the
indications that require immediate cord clamping. Delayed cord
intraventricular haemorrhage and necrotising enterocolitis rate
clamping in term infants, increases haemoglobin and ferritin for
in the delayed cord clamping group, the data were inadequate to
the first months of life, with possible neurodevelopmental benefit
show a statistically significant result. A significant increase of 15
later in life. Jaundice requiring phototherapy is increased if
mmol/L in the mean bilirubin rate between the two groups has
delayed clamping is practiced, therefore phototherapy equipment
also been found. Another review of 12 studies which included
should be available. Preterm infants may also be benefited by
531 neonates with an average gestation of 28 weeks, concluded
delayed cord clamping, as studies show that there is improve-
that there is a significant reduction in intraventricular haemor-
ment of neonatal circulation and haemoglobin as well as reduc-
rhage (RR 0.62), mortality (RR 0.42) and blood transfusion (RR
tion in need for transfusion. There is reduction in the incidence of
0.75), but no difference in delivery room intubation or peak
intraventricular haemorrhage and better long term outcome.
serum bilirubin in the delayed clamping group. Animal studies
There has been no increase in adverse maternal outcome such as
have suggested that there is a benefit in apnoeic preterm neo-
increased risk of postpartum haemorrhage. A
nates as delayed clamping increases pulmonary blood flow and
maintains a stable cardiac output. A trial that assessed rate of late
onset sepsis in preterm neonates with delayed cord clamping did FURTHER READING
not find a significant difference compared to early clamping. American College of Obstetricians and Gynaecologists. Delayed um-
bilical cord clamping after birth. Committee Opinion No. 684.
Comparison between delayed cord clamping to cord Obstet Gynecol 2017; 129: e5e10.
milking Farrar D, Airey R, Law GR, Tuffnell D, Cattle B, Duley L. Measuring
placental transfusion for term births weighing babies with cord
Cord milking is an alternate technique to delayed cord clamping
intact. BJOG 2011; 118: 70e5.
that has been known to increase placental transfusion. The
Katheria AC, Truong G, Cousins L, et al. Umbilical cord milking versus
proposed technique involves four milking movements toward the
delayed cord clamping in preterm infants. Pediatrics 2015; 136:
neonate with a speed of 20 cm/2 seconds prior or after cord
61e9.
clamping. A meta-analysis of seven trials that included 501 in-
McDonald SJ, Middleton P, Dowswell T, Morris PS. Effect of timing of
fants concluded that cord milking, increases haemoglobin in
umbilical cord clamping of term infants on maternal and neonatal
term neonates for the first 48 hours of life and reduces incidence
outcomes. Cochrane Database Syst Rev 2013. Issue 7. Art. No.:
of intraventricular haemorrhage in preterm infants. A study that
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compared delayed cord clamping to cord milking in preterm
Rabe H, Diaz-Rosselle JL, Duley L, Dowswell T. Effect of timing of
neonates, concluded that in the cord milking group, there is
umbilical cord clamping and other strategies to influence placental
increased haemoglobin, blood pressure and urine output
transfusion at preterm birth on maternal and infant outcomes.
compared to the delayed clamping group. The same study also
Cochrane Database Syst Rev 2012. Issue 8. Art. No.:CD003248.
reported that there is improvement of pulmonary blood flow that

OBSTETRICS, GYNAECOLOGY AND REPRODUCTIVE MEDICINE --:- 2 Ó 2017 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Argyridis S, Delayed cord clamping, Obstetrics, Gynaecology and Reproductive Medicine (2017), http://
dx.doi.org/10.1016/j.ogrm.2017.08.003