Review Arch Argent Pediatr 2017;115(2):188-194 / 188

Timing of umbilical cord clamping of

term infants
José María Ceriani Cernadas, M.D.a,b

ABSTRACT time to newborn infant (NBI) care, is

For at least over 200 years, multiple controversies
considered the father of neonatology.
have arisen around the timing of umbilical
cord clamping. In the past decades, early cord In 1875, Budin published an article
clamping (within the first 15 seconds) had markedly discussing the right timing for cord
prevailed. Only in the 21st century, randomized clamping. 2 In 1975, this article was
controlled trials have demonstrated the benefits
commented in Pediatrics under a
of delayed cord clamping (at 2-3 minutes).
Delayed cord clamping has been practiced in suggestive title: “100 years on, and still
obstetrics based on the recommendations made no answer.” 3 Nothing had changed
by scientific societies and in systematic reviews, after so many years.
which have provided solid evidence to support
In the second half of the 20th century,
this practice in term infants.
This review describes the most relevant factors immediate cord clamping became
supporting the use of delayed cord clamping in the generalized practice in Western
term infants. It points out the essential role played countries. Several studies done in a
by physiological mechanisms which, undoubtedly,
small number of patients and published
allow us to understand the benefits of delayed cord
clamping and advise us to wait for what nature has in the 1960s and 1970s 4-8 strongly
established. Other relevant aspects supporting supported immediate cord clamping
delayed cord clamping are also described here. but there was no evidence to endorse
Key words: clamping, umbilical cord, placental
this practice.
transfusion, neonatal transition, iron deficiency.
Only in this century, well-designed
http://dx.doi.org/10.5546/aap.2017.eng.188 studies have been published that have
settled some of the disputes. The
current evidence is solid enough
To cite: Ceriani Cernadas JM. Timing of umbilical
cord clamping of term infants. Arch Argent Pediatr to confirm the undeniable benefits
2017;115(2):188-194. of delayed cord clamping for term
infants (TIs).9-11
To understand the basis of such
assertion, the main factors involved
INTRODUCTION in delayed cord clamping of TIs are
Since the mid-18 th century, the described below.
a. Division of timing of umbilical cord clamping has
Neonatology and
Teaching Institute of
been, and still is, focus of controversy. Physiological aspects
Hospital Italiano de Erasmus Darwin, a distinguished Physiological mechanisms play an
Buenos Aires. physician and the grandfather of essential role in the outcomes observed
b. Council of Publications
of the Argentine
the famous Charles, wrote a book when the cord is clamped not earlier
Society of Pediatrics. published in 1801,1 where he points than 1 minute after birth. For this
out his concern on this aspect: “Another reason, it is critical to know the
E-mail address: precise action of these mechanisms to
thing very injurious to the child is the
José María Ceriani
Cernadas, M.D.: tying and cutting of the navel-string too understand their effects on NBIs.
jose.ceriani@ soon; which should always be left till the
hospitalitaliano.org.ar child has not only repeatedly breathed, Placental transfusion
but till all pulsation in the cord ceases. As This is the transfer of blood from
Funding:
None. otherwise the child is much weaker than it the placenta to the infant. It is a very
ought to be; a part of the blood being left in important physiological mechanism
Conflict of interest: the placenta, which ought to have been in and the basis to understand the
None. differences in cord clamping timing
the child.”
Received: 10-11-2016 Pierre Budin, a renowned French and its effects on the infant. At
Accepted: 10-14-2016 obstetrician who also devoted his 1 minute, NBIs receive 80 mL of
 Timing of umbilical cord clamping of term infants / 189

blood; at 2-3 minutes, 100 mL; accounting for when clamping was delayed at least until after
approximately 30-35 mL/kg, volume that is 75% the first breath, cardiovascular function improved
higher than with early clamping. markedly based on the increased pulmonary
blood flow in the NBI and the resulting cerebral
Iron supply during placental transfusion hemodynamic stability in the key moments of
At birth, TIs have a 75 mg/kg iron (Fe) store; postnatal transition. In addition, these results
with delayed cord clamping and placental indicated that delaying cord clamping until
transfusion, TIs receive an additional 40 mg of Fe after the onset of ventilation led to a better NBI
at 1 minute and 50 mg at 3 minutes (Figure 1). This adaptation, one of the most significant benefits of
way, TIs have a body iron store of 115-125 mg/ delayed cord clamping.
kg, which is enough to prevent iron deficiency in Knowing these mechanisms indicates that if
the first 6 months of life, and probably until they a baby is cyanotic at birth, the cord should not
turn 1 year old. be clamped immediately, a very common but
In a study conducted in our setting,12 blood inappropriate practice. Early cord clamping will
ferritin levels at 6 months old were significantly only worsen the infant’s clinical status because
higher among infants whose cord was clamped at it causes a noticeable restriction of cardiac
3 minutes versus during the first seconds. Other output and therefore increases hypoxia. An
authors have described similar results.13-23 increased cardiac output is essential to counteract
Such effect is very important for the future the effects of hypoxemia; for this reason, limiting
of children considering that iron deficiency in or preventing the rise in cardiac output exposes
the early stages may be harmful to the central the baby to hypoxia-ischemia.
nervous system and result in neurocognitive A study conducted in Africa in an
disorders. In addition, iron deficiency is the main extensive cohort of 15 563 NBIs28 reviewed the
cause of anemia, a severe condition in developing relationship between cord clamping timing and
countries, although less serious in developed the spontaneous onset of breath and infants’
countries.24-26 clinical course in the first 24 hours of life.
Results showed that the risk of death or post-
First breath and timing of cord clamping discharge readmission was higher when the
Several studies have demonstrated that cord cord was clamped before the first breath and
clamping timing is greatly relevant for the time that such risk decreased by approximately 20%
of the first breath and for other major aspects of per every additional 10 seconds lapsed until cord
the physiological adaptation to extrauterine life. clamping.
In a research conducted in sheep, Bhatt et al.27 Several update articles have reasserted the
studied the influence of delayed cord clamping on benefits of delayed cord clamping over immediate
ventilation and on cardiovascular and cerebral clamping and explored the different aspects that may
hemodynamic stability. Their results showed that explain the importance of beneficial mechanisms.29-30

Figure 1. Iron supply through the umbilical cord

Milligrams of iron received based on the time of cord clamping

60
50
mg of Fe+

40 mg of Fe
30
20
10
0
0 30 60 90 120 150 180
Time in seconds
Source: Usher, Yao and Lind.
190 / Arch Argent Pediatr 2017;115(2):188-194 / Review

Hooper et al. 31 emphasize that immediate neither justified nor supported by any study
clamping results in a considerable limitation of demonstrating that delayed cord clamping is
venous return in the absence of breathing, thus detrimental to the recovery of an infant with
reducing cardiac output, which remains very asphyxia. On the contrary, there is a growing
low until the infant starts breathing. When this trend of encouraging resuscitation of TIs while
occurs, lung aeration causes a particular increase leaving the cord unclamped.35,36 The rationale
in pulmonary circulation, which in turn rapidly for this is similar to what has been described
boosts cardiac output, which is reflected by the above, given that, also in this case, physiological
clear increase in the infant’s heart rate. It is worth mechanisms play a critical role in the prevention
noting that, during fetal life, the source of left of cardiac output reduction.
ventricular preload is the blood flow from the For this reason, the systematic clamping of the
placenta; this is replicated at birth while the blood umbilical cord before attempting resuscitation
from the placenta flows through the umbilical is inadequate because, once again, it means
cord to the infant. not being aware of the physiological concepts
Once again, a big mistake is made when a NBI related to neonatal transition. As indicated
has apnea and cord clamping is hurried because, above, clamping should be delayed enough time,
in the presence of a restricted cardiac output, the until at least after the first breath, and the same
infant will remain cyanotic and have a reduced approach may be applied in the case resuscitation
brain circulation. is required.
This aspect reaffirms that cardiac output is This aspect was assessed many years ago
the most important physiological mechanism in an experimental study conducted in rhesus
and is necessary to prevent hypoxia-ischemia monkeys.37 For the study, a model was created
in the blood flow to the brain. This may only be to cause moderate depression at birth, and
achieved by leaving the cord unclamped until it was observed that if the cord was clamped
placental transfusion is completed. Thus, preload immediately, it resulted in marked bradycardia
and cardiac output restriction will be prevented accompanied by irregular breathing, panting, and
and the infant will have a more stable blood flow subsequent apnea.
during adaptation. Clinical studies have endorsed the potential
Recent publications have emphatically benefits of placental transfusion in the
underlined the importance of knowing and resuscitation of TIs, 35,36 but scarce data have
implementing physiological mechanisms in the been published in the very small preterm infant
approach to cord clamping timing in clinical population.
practice.32,33 However, a recent study conducted by
Undoubtedly, the generalized Kaempf et al. 38 provided interesting results
recommendation of immediate cord clamping after comparing the clinical course of 77 very
–in place for several decades and based on no low birth weight (VLBW) preterm newborn
sound evidence– has inflicted countless damage infants and 172 low birth weight (LBW) preterm
on NBIs. To a great extent, this was the result of newborn infants. They were all born at less than
being unaware that placental transfusion provided 35 weeks of gestation and cord clamping was
an adequate volume loading that prevented a delayed until 45 seconds, and were compared to
low cardiac output; this indicates that health the same number of historical controls born in
care providers did not know the physiological the immediately previous period and subjected
processes involved in blood flow from the to early cord clamping. The Apgar score at 1
placenta to the infant. minute was higher among VLBW preterm infants
In another recent article, Niermeyer approaches subjected to delayed cord clamping (7 versus 5,
an extremely important aspect with great p < 0.001). Also, there was a remarkable reduction
implications for everyday practice, and that is the in the number of NBIs who required supplemental
relationship between cord clamping timing and oxygen and ventilation at birth.
the need to resuscitate the infant.34 However, most likely, and for the time being,
Obstetricians and neonatologists agree on we may not recommend the systematic use of
delayed cord clamping only if the NBI does not delayed cord clamping for all TIs who require
require resuscitation. Once it is determined that resuscitation. Nonetheless, it may become part
a NBI does require resuscitation, the umbilical of the practice based on its high chances of being
cord is clamped immediately. However, this is beneficial taking into account that the foundation
 Timing of umbilical cord clamping of term infants / 191

for delayed cord clamping lies in physiological In addition, umbilical cord blood contains
mechanisms, which are the safest alternative. a number of hematopoietic stem cells large
enough to be used for transplantation in children,
Stem cells and placental transfusion adolescents, and adults,41 a firmly rising hope.42,43
The presence of stem cells in blood from the
placenta is another highly relevant aspect because Other aspects to be taken into consideration in
it plays a critical role, not only for infants but also relation to umbilical cord clamping timing
for children and adults.
The number of stem cells is significantly Plasma bilirubin levels
higher in extremely preterm infants than in TIs. Studies conducted in the 1970s found that
This has been demonstrated by Haneline et al.,39 infants undergoing delayed cord clamping had
who also observed that the number of stem cells higher bilirubinemia values. 5 An increase in
contained in the umbilical cord blood was higher the indication for phototherapy has also been
than in older children and even higher than in described, but it is not unanimous; even though,
the adult bone marrow. As per these findings, a systematic review of clinical trials found that the
the number of stem cells in extremely preterm indication for phototherapy was lower (at the cut-
infants would be at its highest level than at any off point) among infants with early clamping.44
other time in human life. In our study,9 no differences were observed
In this physiological process, stem cells play between groups in terms of bilirubin levels and
multiple protective roles during fetal life and the indication for phototherapy (Table 1).
when the baby is born. In NBIs, the most important
functions of these cells include mechanisms that Anemia at birth and between 24 and 48 hours
regulate the growth and development of different The presence of early anemia observed in
organs (especially the central nervous system), our study9 was significantly higher among NBIs
an anti-inflammatory action, and the reduction with early cord clamping (Table 2). The presence
of several diseases, such as respiratory distress of anemia at birth is detrimental because it
syndrome, anemia, sepsis, intraventricular means iron stores will become insufficient in the
hemorrhage, and periventricular leukomalacia. short run, thus increasing the presence of iron
There are other disorders, such as retinopathy deficiency anemia, together with its potential
of prematurity and necrotizing enterocolitis, for risks.
which their function has not been confirmed yet.40 It is worth noting that a subsequent subgroup
Even though, at full term, the number of analysis –done after our study was published–
stem cells decreases, the amount provided with showed that all NBIs with anemia (hematocrit
delayed cord clamping is more than enough, which < 45%) at 24 and 48 hours had been born by
is not the case with early clamping; and this is yet C-section and had undergone early cord
another sound argument against this practice. clamping. 45 This information takes on special

Table 1. Plasma bilirubin levels between 36 and 48 hours

Treatment Blood bilirubin at 36-48 hours
N Missing Min. Max. Mean SD Median Q25 Q75
Immediate clamping 91 2 1 17.4 7.39 3.08 7.3 5.6 9
Clamping at 1 minute 85 6 1 18.9 7.58 3.04 7.7 6.1 9
Clamping at 3 minutes 90 2 1 14.6 6.99 2.98 7.2 5.0 9

Outcome measure Immediate clamping Clamping at 1 min Clamping at 3 min

n/N (%) n/N (%) n/N (%)
Bilirubin at 36-48 hours
higher than 16 mg/dL 2/91 (2.20) 1/85 (1.18) 0/90 (0.0)

SD: Standard deviation.

Ceriani Cernadas JM, Carroli G, et al. Pediatrics 2006;117:e779-e786
192 / Arch Argent Pediatr 2017;115(2):188-194 / Review

relevance due to the extremely high number of that cord clamping timing has on long-term
C-sections performed at present, and reconfirms neurodevelopment, both in term and preterm
that delayed cord clamping should be the infants. Recently published randomized studies
approach used in the case of a C-section. have assessed neurodevelopment at 1 year old47
and at 4 years old,48 in the same cohort of term
Oxidative stress infants with early cord clamping (within the
It is known that free radicals cause different first 10 seconds) versus delayed cord clamping
types of damage in certain situations, for example, (at 3 minutes). No differences were observed in
at the time of delivery, when oxidative stress is the assessment at 1 year old, although boys with
confirmed in the mother, and especially in the delayed clamping tended to show better results.
NBI. Among other factors, the sudden change The assessment at 4 years old is the first clinical
from the uterine environment with physiological research on neurodevelopment in the preschool
hypoxia to the abrupt increase in partial pressure population. No overall differences were found
of oxygen (pO2) at birth may likely release free in the Wechsler Preschool and Primary Scale
radicals that are highly toxic to the infant. To of Intelligence (WPPSI-III), although boys with
avoid tissue damage, antioxidant systems should delayed cord clamping obtained a significantly
come into play during the first minutes after birth higher score than those with early cord clamping
to reduce the harmful effects of oxidative stress. in the processing speed quotient, and they also
Until recently, these mechanisms were not obtained better scores and showed a significant
considered related to umbilical cord clamping differences in the movement tests, the fine motor
timing. In 2014, Pediatrics 46 published the first area and the personal-social area of the Ages and
study that assessed the impact of early clamping Stages Questionnaire (ASQ).
(at 10 seconds) versus delayed clamping (at It is worth noting that such better results
2 minutes) on oxidative stress. Several inflammatory were observed in children at a very low risk
parameters were measured in healthy TIs who from a highly developed country (Sweden).
had been born from healthy mothers, by vaginal This is worthy of consideration given that
delivery, and who had an Apgar score at 1 and beneficial effects of delayed cord clamping on
5 minutes ≥ 7. Results were conclusive and neurodevelopment may have a greater impact
demonstrated that all protective elements measured on vulnerable populations from a low social class
in the study (erythrocyte catalase, superoxide and with a low education level. Although another
dismutase, tumor necrosis factor receptor 2, etc.) study has been recently published,49 new trials are
were significantly higher among NBIs with delayed required to examine long-term effects of delayed
cord clamping. cord clamping.
Although future randomized studies are
required, a very interesting research ground is Final remarks
charted that will provide important elements Based on every aspect pointed out in this
when deciding on the timing of cord clamping. article, and the sound evidence supporting them,
there is no doubt that delayed cord clamping
Long-term neurodevelopment should be the standard of care for infants born at
Only a few studies have assessed the impact term or close to term.

Table 2. Central hematocrit in the first 48 hours

Early clamping Clamping at 1 min Clamping at 3 min
n= 90 n= 90 n= 92
Hematocrit at 6 h < 45% (n%)¹ 8 (8.9) 1 (1.1) 0 (0.0)
Hematocrit at 24-48 h < 45% (n%)² 15 (16.9) 2 (2.3) 3 (3.3)
¹ Clamping at 1 minute versus early clamping: RR 0.3 (95% CI: 0.02-0.8), P < 0.034.
¹ Clamping at 3 minutes versus early clamping: RR 0.06 (95% CI: 0.006-0.6), P < 0.003.
² Clamping at 1 minute versus early clamping: RR 0.13 (95% CI: 0.035-0.50), P < 0.0014.
² Clamping at 3 minutes versus early clamping: RR 0.20 (95% CI: 0.06-0.61), P < 0.0027.
Ceriani Cernadas JM, Carroli G, et al. Pediatrics 2006;117:e779-e786.
 Timing of umbilical cord clamping of term infants / 193

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