Research

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OBSTETRICS

Effect of delayed cord clamping on very

preterm infants
Arpitha Chiruvolu, MD; Veeral N. Tolia, MD; Huanying Qin, MS; Genna Leal Stone, BSN, MBA;
Diana Rich, BSN; Rhoda J. Conant, MD; Robert W. Inzer, MD
OBJECTIVE: Despite significant proposed benefits, delayed umbilical

cord clamping (DCC) is not practiced widely in preterm infants largely

because of the question of feasibility of the procedure and uncertainty
regarding the magnitude of the reported benefits, especially intraventricular hemorrhage (IVH) vs the adverse consequences of delaying
the neonatal resuscitation. The objective of this study was to determine
whether implementation of the protocol-driven DCC process in our
institution would reduce the incidence of IVH in very preterm infants
without adverse consequences.
STUDY DESIGN: We implemented a quality improvement process for
DCC the started in August 2013 in infants born at
32 weeks
gestational age. Eligible infants were left attached to the placenta for 45
seconds after birth. Neonatal process and outcome data were collected
until discharge. We compared infants who received DCC who were born
between August 2013 and August 2014 with a historic cohort of infants
who were born between August 2012 and August 2013, who were
eligible to receive DCC, but whose cord was clamped immediately after
birth, because they were born before the protocol implementation.
RESULTS: DCC was performed on all the 60 eligible infants; 88
infants were identified as historic control subjects. Gestational

age, birthweight, and other demographic variables were similar

between both groups. There were no differences in Apgar scores
or admission temperature, but significantly fewer infants in the
DCC cohort were intubated in delivery room, had respiratory
distress syndrome, or received red blood cell transfusions in the
first week of life compared with the historic cohort. A significant
reduction was noted in the incidence of IVH in the DCC cohort
compared with the historic control group (18.3% vs 35.2%).
After adjustment for gestational age, an association was found
between the incidence of IVH and DCC with IVH was significantly
lower in the DCC cohort compared with the historic cohort; an
odds ratio of 0.36 (95% confidence interval, 0.15e0.84; P <
.05). There were no significant differences in deaths and other
major morbidities.
CONCLUSION: DCC, as performed in our institution, was associated
with significant reduction in IVH and early red blood cell transfusions.
DCC in very preterm infants appears to be safe, feasible, and effective
with no adverse consequences.

Key words: delaying umbilical cord clamping, intraventricular

hemorrhage, very preterm infant

Cite this article as: Chiruvolu A, Tolia VN, Qin H, et al. Effect of delayed cord clamping on very preterm infants. Am J Obstet Gynecol 2015;213:676.e1-7.

here is growing evidence that

enhanced placental transfusion by
delaying umbilical cord clamping (DCC)
in very preterm infants may improve
hemodynamic stability after birth and
decrease the incidence of major neonatal morbidities, such as intraventricular hemorrhage (IVH) and necrotizing

enterocolitis (NEC).1-6 Recently, the

American College of Obstetricians and
Gynecologists (ACOG) published a
committee opinion that supported DCC
in preterm infants, with the possibility
for a nearly 50% reduction in IVH.7
However, the practice of DCC in preterm infants has not been adopted

From the Division of Neonatology, Department of Pediatrics (Drs Chiruvolu and Tolia), and
Departments of Nursing (Ms Stone and Ms Rich) and Obstetrics and Gynecology (Dr Inzer), Baylor
University Medical Center, and Department of Quantitative Health Sciences, Baylor Scott & White
Health Care System (Ms Qin), Dallas, and Department of Medical Education, Texas A&M Health
Science Center College of Medicine, Bryan (Dr Conant), TX.
Received April 4, 2015; revised May 21, 2015; accepted July 13, 2015.
Financial support for the statistical analysis was provided by Baylor Scott & White Nursing
Research Council.
The authors report no conict of interest.
Corresponding author: Arpitha Chiruvolu, MD. Arpitha.Chiruvolu@baylorhealth.edu
0002-9378/$36.00  2015 Elsevier Inc. All rights reserved.  http://dx.doi.org/10.1016/j.ajog.2015.07.016

676.e1 American Journal of Obstetrics & Gynecology NOVEMBER 2015

widely, mainly because of the concern

of a delay in initiating resuscitation
in this vulnerable population.8 Furthermore, there is uncertainty regarding
the magnitude of published benets
in very preterm infants because previous trials were limited by small sample
sizes, wide variability in the technique,
and inconsistent reporting of factors
that may have contributed to clinical
outcomes.9,10
We recently implemented a DCC
quality improvement (QI) process in
very preterm infants at a large delivery
hospital. The objective of this cohort
study was to evaluate the clinical consequences of a protocol-driven DCC
implementation in singleton infants
who were born at
32 weeks gestation.
We hypothesized that DCC would not
compromise initial resuscitation and

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would be associated with a signicant
decrease in early red blood cell transfusions and IVH compared with a historic cohort.

M ATERIALS

AND

Research

FIGURE

Distribution of the cohorts

M ETHODS

On average, our level III Neonatal

Intensive Care Unit cares for approximately 200 very preterm inborn infants
every year. The previous routine clinical
practice was to clamp the umbilical cord
immediately after the birth. The DCC
QI process was implemented starting
August 2013. All infants born at
32
weeks gestation were eligible for DCC,
unless they met the following exclusion
criteria: severe maternal illness that
prompted immediate delivery, placental
causes (abruption or previa) or fetal
causes (multiple gestation, major
congenital anomalies, severe growth restriction, or hydrops fetalis). After birth,
the infant was left unstimulated,
attached at or slightly below the level of
placenta for 45 seconds. The cord was
then clamped and cut, and the neonatal
team initiated resuscitation efforts.
Apgar timing was initiated at the time
of birth when the infant was delivered
completely.
With approval by the institutional
review board, prospective and retrospective data were extracted from
maternal and neonatal electronic medical records. The prospective study period
was 1 year, from Aug.19, 2013, to Aug.
18, 2014. The study period for the historic cohort was also 1 year, from Aug.
19, 2012, to Aug. 18, 2013. Collected data
included maternal demographics, obstetric complications, any antenatal steroid and magnesium use, and other
labor and delivery variables. Neonatal
data included gestational age, birthweight, sex, postdelivery data variables
such as Apgar scores, resuscitation data,
and the infants temperature upon
admission to the neonatal intensive care
unit. Other clinical variables included
treatment with phototherapy, (intensive
phototherapy dened as irradiance in the
blue-green spectrum of at least 30 mW/
cm2 per nm),11 red blood cell transfusions, and inotropic and corticosteroid
therapy within 1 week of life. Additional
outcome variables included incidence

During the retrospective study period, 88 (69%) singleton infants were eligible to receive DCC
(historic cohort). During the prospective study period, 60 (63%) singleton infants received DCC
(DCC cohort). Different exclusion criteria are shown in the figure.
DCC, delaying umbilical cord clamping.
Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.

of respiratory distress syndrome (RDS),

surfactant therapy, therapy for patent
ductus arteriosus, and incidence of culture positive sepsis. We also recorded
major outcomes such as death, bronchopulmonary dysplasia (BPD), NEC
Bells stage 2,12 retinopathy of prematurity (ROP), and IVH. Diagnosis of
BPD was made at 36 weeks postmenstrual age if there was any oxygen
requirement.13 Any operative interventions for NEC or ROP were also
documented.14 IVH was graded 1-4
based on the criteria developed by Papile
et al15 who dened grades 3 and 4 as

severe IVH. White matter injury such as

periventricular leukomalacia and porencephaly also were documented.
All statistical analysis was performed
with SAS Enterprise Guide software
(version 5.1; SAS Institute Inc, Cary,
NC). Demographic and outcome variables were compared between the
DCC cohort and historic control groups
with the use of the Student t test for
continuous variables, and c2 or Fisher
exact test for categoric variables. We also
calculated odds ratios (with 95% condence interval) for comparisons after
adjustment for gestation. Death and

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other major outcomes were also reported after stratication for gestational
age. A probability value < .05 was
considered to be the threshold of statistical signicance.

R ESULTS
During the prospective study period,
after implementation of DCC protocol,
157 infants were born at
32 weeks
gestation. After excluding multiple
gestation infants, 96 singleton infants
were included in analysis. DCC was
performed on all of the 60 eligible infants
per prespecied protocol (DCC cohort).
During the retrospective study period,
158 infants were born at
32 weeks
gestation, of which 127 were singletons.
Among them, 88 infants would have
been eligible to receive DCC (historic
cohort). All of these infants received
immediate umbilical cord clamping after
birth. The Figure shows the distribution
of both cohorts, including exclusion
criteria.
There were no signicant differences
in maternal characteristics (Table 1).
Articial reproductive therapy and cesarean delivery numbers were not
different between the groups. Similarly,
there were no differences in other maternal variables such as chorioamnionitis, gestational hypertension or diabetes
mellitus, preeclampsia, or poly- or oligohydramnios. Overall antenatal steroid
administration and maternal magnesium exposure were similar between the
groups. However, there was a signicantly higher incidence of rupture of
membranes at >18 hours before birth
in the historic cohort (17.1% vs 5%).
There were no signicant differences
in baseline neonatal characteristics between the groups (Table 1). Mean gestational age was 27.9  2.8 weeks in
the historic cohort compared with
27.9  2.4 weeks in the DCC cohort;
mean birthweight was 1155  399 g in
the historic cohort compared with
1173  362 g in the DCC cohort. Male
infants represented 53% in both groups.
There were no signicant differences
in 1- and 5-minute Apgar scores or admission temperature. However, signicantly fewer infants in the DCC cohort
were intubated in the delivery room

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TABLE 1

Maternal and neonatal characteristics and resuscitation data

Cohort

Variable
a

Maternal age, y

Historic
(n [ 88)

Delaying
umbilical
cord clamping
(n [ 60)

28.9  7.2

27.6  6.2

Maternal race, n (%)

P value
.27
.7

White

27 (30)

19 (32)

Black

43 (49)

25 (42)

Hispanic

18 (21)

16 (26)

Other

1 (1.1)

1 (1.7)

.77

Antenatal steroids, n (%)

84 (95.4)

56 (93.3)

.96

Maternal magnesium, n (%)

82 (93.1)

56 (93.3)

.95

Cesarean delivery, n (%)

58 (65.9)

39 (65)

.92

Chorioamnionitis, n (%)

9 (10.2)

9 (15)

.51

29 (32.9)

17 (28.3)

.63

5 (5.7)

1 (1.7)

.4

3 (5)

.04

Artificial reproductive technique, n (%)

Pregnancy-induced hypertension/
preeclampsia/eclampsia/hemolysis,
elevated liver enzymes, and low
platelet count syndrome, n (%)
Poly-/oligohydramnios
Prolonged rupture of membranes
>18 hours

15 (17.1)

27.9  2.4

.86

1155.1  399 1173.5  362

27.9  2.8

.78

Gestation, wka
Birthweight, ga
Male, n (%)

47 (53.4)

32 (53.3)

.99

1 minute

5 (1-9)

6 (1-9)

.2

5 minutes

7 (1-9)

8 (3-10)

.19

97.6  1.6

98.2  1

.47

46 (62.2)

11 (18.3)

< .0001

Chest compressions

1 (1.1)

2 (3.3)

.56

Epinephrine

2 (2.3)

.52

Packed red blood cells

1 (1.1)

1.00

Apgar score, n

Admission temperature, degrees Fa

Events in the delivery room, n (%)
Intubation

Data are given as mean  SD; b Data given as median (range).

Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.

compared with the historic cohort

(18.3% vs 62.2%).
Red blood cell transfusion need in
the rst week of life was signicantly
lower in the DCC cohort compared with
the historic cohort (13.3% vs 33%), although the use of pressor support or
corticosteroids was not different (Table 2).

676.e3 American Journal of Obstetrics & Gynecology NOVEMBER 2015

Phototherapy in rst week of life was

signicantly higher in the DCC cohort,
but none of the infants in either groups
received intensive phototherapy or exchange transfusion. Incidence of RDS
and surfactant administration was significantly lower in the DCC cohort. A signicant reduction was noted in the

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Research

TABLE 2

Comparison of neonatal outcomes

Cohort, n (%)
Variable

Historic
(n [ 88)

Pressor need in first week

15 (17)

Steroid need in first week

Packed red blood cell transfusion in first week
Phototherapy in first week

Respiratory distress syndromea

Surfactant administration

0.69 (0.22e2.19)

3 (5)

3.77 (0.47e30.27)

8 (13.3)

0.11 (0.03e0.41)

72 (81.8)

56 (93.3)

5.25 (1.11e24.85)

58 (65.9)

26 (43.3)

0.18 (0.07e0.50)

29 (33)

30 (34.1)

Patent ductus arteriosus treated

Odds ratio adjusted for

gestation (95% confidence
interval)

7 (11.7)

2 (2.3)
a

Delaying umbilical
cord clamping (n [ 60)

20 (23.7)

3 (5)

0.04 (0.01e0.19)

14 (23.3)

1.06 (0.40e2.76)

Death

10 (11.4)

4 (6.7)

0.78 (0.19e3.25)

Intraventricular hemorrhagea (grades 1-4)

31 (35.2)

11 (18.3)

0.36 (0.15e0.84)

Severe intraventricular hemorrhage (grades 3,4)

10 (11.4)

5 (8.3)

0.80 (0.23e2.76)

4 (4.5)

2 (3.3)

0.78 (0.13e4.74)

Bronchopulmonary dysplasia

17 (19.3)

10 (16.7)

0.62 (0.20e1.95)

Retinopathy of prematurity

Periventricular leukomalacia or porencephaly

20 (22.7)

14 (23.3)

0.80 (0.28e2.32)

Surgical retinopathy of prematurity

4 (5.1)

1 (1.7)

0.29 (0.03e2.96)

Necrotizing enterocolitis

4 (4.5)

5 (8.3)

2.46 (0.56e10.88)

Surgical necrotizing enterocolitis

3 (3.4)

4 (6.7)

2.31 (0.47e11.46)

14 (15.9)

11 (18.3)

1.54 (0.56e4.24)

Culture-positive sepsis
a

P value < .05.

Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.

incidence of IVH in the DCC cohort

compared with the historic cohort
(18.3% vs 35.2%). After adjustment for
gestational age, an association was found
between the incidence of IVH and
DCC, with IVH signicantly lower in the
DCC cohort compared with the historic
cohort with an odds ratio of 0.36 (95%
condence interval, 0.15e0.84; P < .05).
Severe IVH or white matter injury was

not different between both groups. The

distribution of IVH grades by cohort is
shown in Table 3. There was no signicant
difference in mortality or other major
morbidity rates (Table 2). Length of hospital stay was similar between both
groups.
Death and other major outcomes
were also stratied based on 3 gestation
groups: 23-26 6/7 weeks, 27-29 6/7

TABLE 3

Distribution of intraventricular hemorrhage by grade

weeks, and 30-32 weeks (Table 4). DCC

cohort in the 23-26 6/7 weeks and 27-29
6/7 weeks gestation groups had signicantly lower need for early red blood
cell transfusion compared with the historic cohort of similar gestation group.
The incidences of IVH and BPD were
signicantly lower in DCC cohort compared with historic cohort of the 23-26
6/7 weeks gestation group. There was
no signicant difference in mortality or
other major morbidity rates between
similar gestation groups.

Cohort, n (%)
Grade of hemorrhage

Historic
(n [ 88)

Delaying umbilical
cord clamping (n [ 60)

12 (14)

4 (7)

9 (10)

2 (3)

6 (7)

2 (3)

4 (5)

3 (5)

Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.

C OMMENT
In a recent survey among the members
of ACOG and the Collaborative Ambulatory Research Network, the majority
of the respondents indicated that their
hospital does not have an umbilical cord
clamping policy.16 Our study demonstrates that implementation of the DCC
process with standardized protocol in

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very preterm infants is feasible and

effective with improved outcomes.
Many obstetricians and neonatologists share the same concern regarding
DCC in the very preterm infants, which
are adverse outcomes that result from
delaying the resuscitation in this
vulnerable group.16-20 We found that,
despite delaying resuscitation briey,
Apgar scores, other resuscitation variables, and mean admission temperature
were not different between the DCC
and historic control groups. Additionally, a signicantly lower number of infants in the DCC cohort were intubated
in the delivery room. More infants were
breathing spontaneously after DCC,
which contributes to the success of
nonmechanical ventilation. This supports the general hypothesis that DCC
at birth decreases the need for resuscitation by promoting a more physiologic
transition to extrauterine life.21,22 Our
observed reduction in the incidence
of RDS and surfactant administration
adds evidence to the recommendation
of DCC for decreased incidence and
severity of RDS.23,24
Importantly, our study demonstrated
a signicant reduction in the incidence
of IVH in very preterm infants who
received DCC compared with historic
control group. The clinical consequences
of this reduction are valuable, given the
recent evidence that even isolated lower
grades of IVH (grades 1 and 2) are associated independently with a higher risk
of neurosensory impairment compared
with no IVH.25 However, incidence of
severe IVH (grades 3 and 4) or white
matter injury, which is associated with
higher rates of developmental delay and
cerebral palsy, was not signicantly
different between the 2 groups (perhaps
because of the lack of sufcient power to
detect these rare outcomes). These results
are consistent with a recent metaanalysis
of very preterm infants (12 studies; 531
infants).9 Our study also demonstrated
that signicantly fewer very preterm infants received early red blood cell transfusions in the DCC group compared with
historic control group. This nding is also
important, given evidence that early
blood transfusion in very preterm infants
is associated with an increased risk of

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TABLE 4

Stratification of outcomes based on gestation

Cohort, n/N (%)

Variable
Packed red blood cell
transfusion in first week

Intraventricular hemorrhage
(grades 1-4)

Gestation,
wkDd

Historic
a

23/27 (88.5)

27e296/7a

5/28 (17.9)

0/21

30e32

1/33 (3)

0/18

23e266/7

23e266/7

27e296/7
30e32
Severe intraventricular
hemorrhage (grades 3,4)

Bronchopulmonary dysplasia

Retinopathy of prematurity

Necrotizing enterocolitis

Death

Delaying
umbilical cord
clamping

20/27 (74)

4/21 (19)

10/28 (35.7)

7/21 (33.3)

1/33 (3)

23e266/7

8/21 (38.1)

10/27 (37)

0/18
4/21 (19)

27e296/7

0/28

0/21

30e32

0/33

0/18

23e266/7

15/27 (55.6)

7/21 (33.3)

27e296/7

2/28 (7.1)

3/21 (14.2)

30e32

0/33

0/18

23e266/7

15/27 (55.6)

10/21 (47.6)

27e296/7

5/28 (17.9)

4/21 (19)

30e32

0/33

0/18

23e266/7

4/27 (14.8)

4/21 (19)

27e296/7

0/28

1/21 (4.8)

30e32

0/33

0/18

23e266/7

10/27 (35.7)

4/21 (19)

27e296/7

0/28

0/21

30e32

0/33

0/18

P value < .05, for comparison between cohorts.

Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.

developmental delay, IVH, and NEC.26

The persistence of these benecial effects of DCC in the higher risk subgroup
of infants born at <27 weeks gestation
supports recent evidence of more hemodynamic stability and lower rates of
morbidities with enhanced placental
transfusion in extremely low gestational
age neonates.27
There are several factors that contributed to the high rate of compliance
with DCC in our institution. First, the
process was developed with substantial
interprofessional coordination between
the departments of obstetrics and neonatology that resulted in standardized

676.e5 American Journal of Obstetrics & Gynecology NOVEMBER 2015

protocol and narrow eligibility criteria to

overcome perceived barriers. In addition, the extensive implementation plan
included staff education, simulation exercises, and interim monitoring. Finally,
this intervention was incorporated into
our Golden Hour protocol that has objectives and processes for very preterm
infant care in the delivery room that we
have used successfully in our practice
>10 years.28
However, as highlighted in the ACOG
committee statement, there continues
to be substantial gaps in knowledge
regarding optimal duration and technique of umbilical cord clamping.7 We

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chose to delay umbilical cord clamping
by 45 seconds, because we believed the
very preterm infant would receive
enough placental transfusion by that
time.29 We placed the baby at or below
the level of the placenta as feasible.
Because most of the preterm deliveries in
our institution were cesarean sections, it
was a challenge getting the baby truly
below the level of the placenta. Because
good evidence is emerging in more
mature infants, the optimal timing and
positioning in a very preterm infant still
must be explored.30 A large percentage of
deliveries did not receive DCC because
of our predened narrow eligibility
criteria. The question of DCC being
benecial or harmful in these higher risk
excluded infants (such as multiple gestations, growth restricted, and other
vulnerable preterm groups) must be
explored carefully in the future. We were
aware of the different approaches reported in the literature like umbilical
cord milking and mobile trolley use that
may minimize delay in resuscitation.31,32
They are promising alternatives, but we
believe additional studies are needed to
determine fully the safety of these procedures and the impact on short- and
long-term outcomes.
As a prospective cohort study with a
historic control cohort comparison, this
study has several limitations. This study
reports observational data of a QI process from a single center. Thus, conclusions from this study are limited to
associations. Confounding of the results
by other changes in practice is also a risk.
However, our practice did not change
much during the study period other
than more widespread use of nonmechanical ventilation in very preterm infants. This might have had some impact
on our lower intubation and surfactant
administration rates. The radiologists
reading the cranial ultrasound scans
were not blinded formally, but they were
not aware of the implementation of
DCC. There is also the question of
generalizability because the data reported are from a single center. Despite
these limitations, we believe it is
important to share our observations,
which more likely reect the real world
clinical practice and address some of the

concerns that are impeding the widespread practice of DCC in preterm infants.33-35
In conclusion, we have implemented
DCC QI process successfully in a large
delivery hospital. DCC, as performed in
our institution, was associated with a
signicant reduction in IVH and early
red blood cell transfusions. DCC in
very preterm infants appears to be safe,
feasible, and effective with no adverse
consequences. Further clinical studies are
needed to optimize the timing and technique of DCC and to report the impact
of this potentially valuable procedure
on long-term neurodevelopmental outcomes of the very preterm infants.
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