Research ajog.

org

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 intra-
ventricular 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.

T here is growing evidence that

enhanced placental transfusion by
delaying umbilical cord clamping (DCC)
enterocolitis (NEC).1-6 Recently, the
American College of Obstetricians and
Gynecologists (ACOG) published a
widely, mainly because of the concern
of a delay in initiating resuscitation
in this vulnerable population.8 Fur-
in very preterm infants may improve committee opinion that supported DCC thermore, there is uncertainty regarding
hemodynamic stability after birth and in preterm infants, with the possibility the magnitude of published benefits
decrease the incidence of major neo- for a nearly 50% reduction in IVH.7 in very preterm infants because previ-
natal morbidities, such as intraventric- However, the practice of DCC in pre- ous trials were limited by small sample
ular hemorrhage (IVH) and necrotizing term infants has not been adopted sizes, wide variability in the technique,
and inconsistent reporting of factors
that may have contributed to clinical
From the Division of Neonatology, Department of Pediatrics (Drs Chiruvolu and Tolia), and outcomes.9,10
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
We recently implemented a DCC
Health Care System (Ms Qin), Dallas, and Department of Medical Education, Texas A&M Health quality improvement (QI) process in
Science Center College of Medicine, Bryan (Dr Conant), TX. very preterm infants at a large delivery
Received April 4, 2015; revised May 21, 2015; accepted July 13, 2015. hospital. The objective of this cohort
Financial support for the statistical analysis was provided by Baylor Scott & White Nursing study was to evaluate the clinical conse-
Research Council. quences of a protocol-driven DCC
The authors report no conflict of interest. implementation in singleton infants
Corresponding author: Arpitha Chiruvolu, MD. Arpitha.Chiruvolu@baylorhealth.edu who were born at
32 weeks’ gestation.
0002-9378/$36.00  ª 2015 Elsevier Inc. All rights reserved.  http://dx.doi.org/10.1016/j.ajog.2015.07.016 We hypothesized that DCC would not
compromise initial resuscitation and

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would be associated with a significant
decrease in early red blood cell trans- FIGURE
fusions and IVH compared with a his- Distribution of the cohorts
toric cohort.

M ATERIALS AND M ETHODS

On average, our level III Neonatal
Intensive Care Unit cares for approxi-
mately 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 re-
striction, 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 retro-
spective data were extracted from
maternal and neonatal electronic medi-
cal records. The prospective study period During the retrospective study period, 88 (69%) singleton infants were eligible to receive DCC
was 1 year, from Aug.19, 2013, to Aug. (historic cohort). During the prospective study period, 60 (63%) singleton infants received DCC
18, 2014. The study period for the his- (DCC cohort). Different exclusion criteria are shown in the figure.
toric cohort was also 1 year, from Aug. DCC, delaying umbilical cord clamping.
19, 2012, to Aug. 18, 2013. Collected data Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.
included maternal demographics, ob-
stetric complications, any antenatal ste-
roid and magnesium use, and other of respiratory distress syndrome (RDS), severe IVH. White matter injury such as
labor and delivery variables. Neonatal surfactant therapy, therapy for patent periventricular leukomalacia and por-
data included gestational age, birth- ductus arteriosus, and incidence of cul- encephaly also were documented.
weight, sex, postdelivery data variables ture positive sepsis. We also recorded All statistical analysis was performed
such as Apgar scores, resuscitation data, major outcomes such as death, bron- with SAS Enterprise Guide software
and the infant’s temperature upon chopulmonary dysplasia (BPD), NEC (version 5.1; SAS Institute Inc, Cary,
admission to the neonatal intensive care Bell’s stage 2,12 retinopathy of prema- NC). Demographic and outcome vari-
unit. Other clinical variables included turity (ROP), and IVH. Diagnosis of ables were compared between the
treatment with phototherapy, (intensive BPD was made at 36 weeks post- DCC cohort and historic control groups
phototherapy defined as irradiance in the menstrual age if there was any oxygen with the use of the Student t test for
blue-green spectrum of at least 30 mW/ requirement.13 Any operative in- continuous variables, and c2 or Fisher
cm2 per nm),11 red blood cell trans- terventions for NEC or ROP were also exact test for categoric variables. We also
fusions, and inotropic and corticosteroid documented.14 IVH was graded 1-4 calculated odds ratios (with 95% confi-
therapy within 1 week of life. Additional based on the criteria developed by Papile dence interval) for comparisons after
outcome variables included incidence et al15 who defined grades 3 and 4 as adjustment for gestation. Death and

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other major outcomes were also re-

ported after stratification for gestational TABLE 1
age. A probability value < .05 was Maternal and neonatal characteristics and resuscitation data
considered to be the threshold of statis- Cohort
tical significance. Delaying
umbilical
R ESULTS Historic cord clamping
During the prospective study period, Variable (n [ 88) (n [ 60) P value
after implementation of DCC protocol, Maternal age, y a
28.9  7.2 27.6  6.2 .27
157 infants were born at
32 weeks’ Maternal race, n (%) .7
gestation. After excluding multiple
White 27 (30) 19 (32)
gestation infants, 96 singleton infants
were included in analysis. DCC was Black 43 (49) 25 (42)
performed on all of the 60 eligible infants Hispanic 18 (21) 16 (26)
per prespecified protocol (DCC cohort). Other 0 0
During the retrospective study period,
158 infants were born at
32 weeks’ Artificial reproductive technique, n (%) 1 (1.1) 1 (1.7) .77
gestation, of which 127 were singletons. Antenatal steroids, n (%) 84 (95.4) 56 (93.3) .96
Among them, 88 infants would have Maternal magnesium, n (%) 82 (93.1) 56 (93.3) .95
been eligible to receive DCC (historic
Cesarean delivery, n (%) 58 (65.9) 39 (65) .92
cohort). All of these infants received
immediate umbilical cord clamping after Chorioamnionitis, n (%) 9 (10.2) 9 (15) .51
birth. The Figure shows the distribution Pregnancy-induced hypertension/ 29 (32.9) 17 (28.3) .63
of both cohorts, including exclusion preeclampsia/eclampsia/hemolysis,
criteria. elevated liver enzymes, and low
platelet count syndrome, n (%)
There were no significant differences
in maternal characteristics (Table 1). Poly-/oligohydramnios 5 (5.7) 1 (1.7) .4
Artificial reproductive therapy and ce- Prolonged rupture of membranes 15 (17.1) 3 (5) .04
sarean delivery numbers were not >18 hours
different between the groups. Similarly, Gestation, wka 27.9  2.8 27.9  2.4 .86
there were no differences in other ma-
Birthweight, ga 1155.1  399 1173.5  362 .78
ternal variables such as chorioamnioni-
tis, gestational hypertension or diabetes Male, n (%) 47 (53.4) 32 (53.3) .99
b
mellitus, preeclampsia, or poly- or oli- Apgar score, n
gohydramnios. Overall antenatal steroid 1 minute 5 (1-9) 6 (1-9) .2
administration and maternal magne-
5 minutes 7 (1-9) 8 (3-10) .19
sium exposure were similar between the
groups. However, there was a signifi- Admission temperature, degrees Fa 97.6  1.6 98.2  1 .47
cantly higher incidence of rupture of Events in the delivery room, n (%)
membranes at >18 hours before birth
Intubation 46 (62.2) 11 (18.3) < .0001
in the historic cohort (17.1% vs 5%).
There were no significant differences Chest compressions 1 (1.1) 2 (3.3) .56
in baseline neonatal characteristics be- Epinephrine 2 (2.3) 0 .52
tween the groups (Table 1). Mean ges- Packed red blood cells 1 (1.1) 0 1.00
tational age was 27.9  2.8 weeks in a
Data are given as mean  SD; b Data given as median (range).
the historic cohort compared with
Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.
27.9  2.4 weeks in the DCC cohort;
mean birthweight was 1155  399 g in
the historic cohort compared with compared with the historic cohort Phototherapy in first week of life was
1173  362 g in the DCC cohort. Male (18.3% vs 62.2%). significantly higher in the DCC cohort,
infants represented 53% in both groups. Red blood cell transfusion need in but none of the infants in either groups
There were no significant differences the first week of life was significantly received intensive phototherapy or ex-
in 1- and 5-minute Apgar scores or ad- lower in the DCC cohort compared with change transfusion. Incidence of RDS
mission temperature. However, signifi- the historic cohort (13.3% vs 33%), al- and surfactant administration was signif-
cantly fewer infants in the DCC cohort though the use of pressor support or icantly lower in the DCC cohort. A sig-
were intubated in the delivery room corticosteroids was not different (Table 2). nificant reduction was noted in the

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TABLE 2
Comparison of neonatal outcomes
Cohort, n (%) Odds ratio adjusted for
Historic Delaying umbilical gestation (95% confidence
Variable (n [ 88) cord clamping (n [ 60) interval)
Pressor need in first week 15 (17) 7 (11.7) 0.69 (0.22e2.19)
Steroid need in first week 2 (2.3) 3 (5) 3.77 (0.47e30.27)
a
Packed red blood cell transfusion in first week 29 (33) 8 (13.3) 0.11 (0.03e0.41)
a
Phototherapy in first week 72 (81.8) 56 (93.3) 5.25 (1.11e24.85)
Respiratory distress syndromea 58 (65.9) 26 (43.3) 0.18 (0.07e0.50)
a
Surfactant administration 30 (34.1) 3 (5) 0.04 (0.01e0.19)
Patent ductus arteriosus treated 20 (23.7) 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)
Periventricular leukomalacia or porencephaly 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 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)
Culture-positive sepsis 14 (15.9) 11 (18.3) 1.54 (0.56e4.24)
a
P value < .05.
Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.

incidence of IVH in the DCC cohort not different between both groups. The
compared with the historic cohort distribution of IVH grades by cohort is
(18.3% vs 35.2%). After adjustment for shown in Table 3. There was no significant
gestational age, an association was found difference in mortality or other major
between the incidence of IVH and morbidity rates (Table 2). Length of hos-
DCC, with IVH significantly lower in the pital stay was similar between both
DCC cohort compared with the historic groups.
cohort with an odds ratio of 0.36 (95% Death and other major outcomes
confidence interval, 0.15e0.84; P < .05). were also stratified based on 3 gestation
Severe IVH or white matter injury was groups: 23-26 6/7 weeks, 27-29 6/7
TABLE 3
Distribution of intraventricular hemorrhage by grade
Cohort, n (%)
Historic Delaying umbilical
Grade of hemorrhage (n [ 88) cord clamping (n [ 60)
1 12 (14) 4 (7)
2 9 (10) 2 (3)
3 6 (7) 2 (3)
4 4 (5) 3 (5)
Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.
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 signifi-
cantly lower need for early red blood
cell transfusion compared with the his-
toric cohort of similar gestation group.
The incidences of IVH and BPD were
significantly lower in DCC cohort com-
pared with historic cohort of the 23-26
6/7 weeks’ gestation group. There was
no significant difference in mortality or
other major morbidity rates between
similar gestation groups.
C OMMENT
In a recent survey among the members
of ACOG and the Collaborative Ambu-
latory Research Network, the majority
of the respondents indicated that their
hospital does not have an umbilical cord
clamping policy.16 Our study demon-
strates that implementation of the DCC
process with standardized protocol in

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very preterm infants is feasible and

effective with improved outcomes. TABLE 4
Many obstetricians and neonato- Stratification of outcomes based on gestation
logists share the same concern regarding Cohort, n/N (%)
DCC in the very preterm infants, which Delaying
are adverse outcomes that result from Gestation, umbilical cord
delaying the resuscitation in this Variable wkDd Historic clamping
vulnerable group.16-20 We found that, Packed red blood cell 23e26þ6/7 a
23/27 (88.5) 8/21 (38.1)
despite delaying resuscitation briefly, transfusion in first week
Apgar scores, other resuscitation vari- 27e29þ6/7a 5/28 (17.9) 0/21
ables, and mean admission temperature
30e32 1/33 (3) 0/18
were not different between the DCC
a
and historic control groups. Addition- Intraventricular hemorrhage 23e26þ6/7 20/27 (74) 4/21 (19)
(grades 1-4)
ally, a significantly lower number of in-
fants in the DCC cohort were intubated 27e29þ6/7 10/28 (35.7) 7/21 (33.3)
in the delivery room. More infants were 30e32 1/33 (3) 0/18
breathing spontaneously after DCC, Severe intraventricular 23e26þ6/7 10/27 (37) 4/21 (19)
which contributes to the success of hemorrhage (grades 3,4)
nonmechanical ventilation. This sup-
27e29þ6/7 0/28 0/21
ports the general hypothesis that DCC
at birth decreases the need for resusci- 30e32 0/33 0/18
a
tation by promoting a more physiologic Bronchopulmonary dysplasia 23e26þ6/7 15/27 (55.6) 7/21 (33.3)
transition to extrauterine life.21,22 Our 27e29þ6/7 2/28 (7.1) 3/21 (14.2)
observed reduction in the incidence
30e32 0/33 0/18
of RDS and surfactant administration
adds evidence to the recommendation Retinopathy of prematurity 23e26þ6/7 15/27 (55.6) 10/21 (47.6)
of DCC for decreased incidence and 27e29þ6/7 5/28 (17.9) 4/21 (19)
severity of RDS.23,24 30e32 0/33 0/18
Importantly, our study demonstrated
a significant reduction in the incidence Necrotizing enterocolitis 23e26þ6/7 4/27 (14.8) 4/21 (19)
of IVH in very preterm infants who 27e29þ6/7 0/28 1/21 (4.8)
received DCC compared with historic 30e32 0/33 0/18
control group. The clinical consequences
Death 23e26þ6/7 10/27 (35.7) 4/21 (19)
of this reduction are valuable, given the
recent evidence that even isolated lower 27e29þ6/7 0/28 0/21
grades of IVH (grades 1 and 2) are asso- 30e32 0/33 0/18
ciated independently with a higher risk a
P value < .05, for comparison between cohorts.
of neurosensory impairment compared Chiruvolu. Effect of DCC on very preterm infants. Am J Obstet Gynecol 2015.
with no IVH.25 However, incidence of
severe IVH (grades 3 and 4) or white
matter injury, which is associated with developmental delay, IVH, and NEC.26 protocol and narrow eligibility criteria to
higher rates of developmental delay and The persistence of these beneficial ef- overcome perceived barriers. In addi-
cerebral palsy, was not significantly fects of DCC in the higher risk subgroup tion, the extensive implementation plan
different between the 2 groups (perhaps of infants born at <27 weeks’ gestation included staff education, simulation ex-
because of the lack of sufficient power to supports recent evidence of more hemo- ercises, and interim monitoring. Finally,
detect these rare outcomes). These results dynamic stability and lower rates of this intervention was incorporated into
are consistent with a recent metaanalysis morbidities with enhanced placental our Golden Hour protocol that has ob-
of very preterm infants (12 studies; 531 transfusion in extremely low gestational jectives and processes for very preterm
infants).9 Our study also demonstrated age neonates.27 infant care in the delivery room that we
that significantly fewer very preterm in- There are several factors that con- have used successfully in our practice
fants received early red blood cell trans- tributed to the high rate of compliance >10 years.28
fusions in the DCC group compared with with DCC in our institution. First, the However, as highlighted in the ACOG
historic control group. This finding is also process was developed with substantial committee statement, there continues
important, given evidence that early interprofessional coordination between to be substantial gaps in knowledge
blood transfusion in very preterm infants the departments of obstetrics and neo- regarding optimal duration and tech-
is associated with an increased risk of natology that resulted in standardized nique 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 predefined narrow eligibility
criteria. The question of DCC being
beneficial or harmful in these higher risk
excluded infants (such as multiple ges-
tations, growth restricted, and other
vulnerable preterm groups) must be
explored carefully in the future. We were
aware of the different approaches re-
ported 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 pro-
cedures 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 pro-
cess from a single center. Thus, conclu-
sions 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 nonme-
chanical ventilation in very preterm in-
fants. 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 re-
ported are from a single center. Despite
these limitations, we believe it is
important to share our observations,
which more likely reflect the real world
clinical practice and address some of the
concerns that are impeding the wide-
spread practice of DCC in preterm in-
fants.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
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. Further clinical studies are
needed to optimize the timing and tech-
nique of DCC and to report the impact
of this potentially valuable procedure
on long-term neurodevelopmental out-
comes of the very preterm infants. - 991-9.
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