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Original Article

Electronic Fetal Monitoring and Neonatal Outcomes


when a Nuchal Cord Is Present at Delivery
Ebony B. Carter, MD, MPH1 Cheryl S. Chu, MD1 Zach Thompson, BS1 Methodius G. Tuuli, MD, MPH1
George A. Macones, MD, MSCE1 Alison G. Cahill, MD, MSCI1

1 Division of Maternal-Fetal Medicine, Department of Obstetrics and Address for correspondence Ebony B. Carter, MD, MPH, Division of
Gynecology, Washington University School of Medicine, St. Louis, Missouri Maternal-Fetal Medicine, Department of Obstetrics and Gynecology,
Washington University School of Medicine, 660 South Euclid Avenue,
Am J Perinatol Maternity Building, 5th Floor, Campus Box 8064, St. Louis, MO 63110
(e-mail: cartere@wustl.edu).

Abstract Objective To determine the association between nuchal cord, electronic fetal
monitoring parameters, and adverse neonatal outcomes.
Study Design This was a prospective cohort study of 8,580 singleton pregnancies.
Electronic fetal monitoring was interpreted, and patients with a nuchal cord at delivery

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were compared with those without. The primary outcome was a composite neonatal
morbidity index. Logistic regression was used to adjust for confounders.
Result Of 8,580 patients, 2,071 (24.14%) had a nuchal cord. There was no difference
Keywords in the risk of neonatal composite morbidity in patients with or without a nuchal cord
► nuchal cord (8.69 vs. 8.86%; p ¼ 0.81). Nuchal cord was associated with category II fetal heart
► neonatal morbidity tracing and operative vaginal delivery (OVD) (6.4 vs. 4.3%; p < 0.01).
► electronic fetal Conclusion Nuchal cord is associated with category II electronic fetal monitoring
monitoring parameters, which may drive increased rates of OVD. However, there is no significant
► fetal heart rate association with neonatal morbidity.

There is continued debate regarding the clinical significance We studied the association between EFM, NC, and neo-
of a nuchal cord (NC) at the time of delivery. Multiple prior natal outcomes among women laboring at term with single-
studies have concluded that there is no risk of neonatal ton pregnancies to estimate whether the presence of an NC at
morbidity associated with an NC.1–5 However, other studies the time of delivery was associated with nonreassuring EFM
have reported an increased risk of certain neonatal outcomes parameters and adverse neonatal outcomes. We hypothe-
including decreased birthweight,7,8 shoulder dystocia,6,7 sized that women with NC would be more likely to have
Apgar score < 7,9–14 neonatal intensive care unit (NICU) category II EFM characteristics, such as variable decelera-
admissions,7,10,11 need for respiratory resuscitation,10 and tions, than women without NC but both groups would have
fetal distress.13,14 This uncertainty leads to frustration for similar neonatal outcomes.
providers and patients who often believe that an NC at the
time of birth is associated with poor neonatal outcomes.15
Materials and Methods
Additionally, despite its ubiquitous use, intrapartum elec-
tronic fetal monitoring (EFM) and its association with NC and This was a planned secondary analysis of a prospective
neonatal outcomes have not been widely studied. Earlier cohort study of 8,580 women with consecutive singleton
reports have generally been in disagreement and have not pregnancies in labor at or beyond 370/7 weeks.20 The
systematically examined specific EFM parameters;1,8,10,13,16–19 primary purpose of the cohort was to examine the relation-
thus, there is a need to further assess the risk of neonatal ship between intrapartum EFM and perinatal outcomes.
morbidity in the setting of both NC and EFM parameters. The study was approved by the Washington University

received Copyright © by Thieme Medical DOI https://doi.org/


August 3, 2018 Publishers, Inc., 333 Seventh Avenue, 10.1055/s-0039-1679866.
accepted after revision New York, NY 10001, USA. ISSN 0735-1631.
January 12, 2019 Tel: +1(212) 584-4662.
Electronic Fetal Monitoring and Neonatal Outcomes Carter et al.

Medical School Human Research Protection Office (IRB ID as a decrease in FHR from the baseline of 15 bpm, lasting
#201102438). between 2 and 10 minutes. The characteristics of EFM
This secondary analysis compared patients with a neona- patterns were defined and compared using the Eunice
tal NC at the time of delivery with those without. NC was Kennedy Shriver National Institute of Child Health and
diagnosed at birth and was defined as the umbilical cord Human Development 3-tier category system.27
wrapped 360 degrees or more around the fetal neck. Exclu- Data analysis was performed with descriptive and bivari-
sion criteria included unknown NC status, major fetal anom- ate statistics using an unpaired Student’s t-test or Mann–
aly, scheduled cesarean delivery without labor, failure to Whitney U test for continuous variables and using a chi-
reach the second stage with pushing, and gestational age square or Fisher’s exact test for categorical variables, as
< 37 weeks. Trained research staff collected detailed data appropriate. The Kolmogorov–Smirnov test was used to
from participant’s medical records. test the normal distribution of continuous variables. Rates
The primary outcome of the study was composite neona- of the primary and secondary outcomes were estimated
tal morbidity, defined as one or more of the following events: within groups. Multivariable logistic regression models for
neonatal death before hospital discharge, seizure(s), the primary and secondary outcomes were developed to
hypoxic–ischemic encephalopathy, need for hypothermic adjust for potential confounders. Covariates that were asso-
treatment, respiratory morbidity, hypotension requiring ciated with the presence of NC in bivariable analyses were
vasopressor therapy, and suspected sepsis. A diagnosis of included in the initial model and were removed sequentially
hypoxic–ischemic encephalopathy required moderate-to- with the use of a backward stepwise approach. Covariates
severe neonatal encephalopathy, defined by the National that were considered in the model included advanced mater-
Institute of Child Health and Human Development criteria,21 nal age (AMA; maternal age  35), Black race, obesity (body

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or seizure activity) in the setting of an abnormal umbilical mass index  30), diabetes, hypertension, history of previous
artery cord gas (pH < 7.0 or base deficit more than 16), 5- cesarean delivery, and oxytocin use. Final models included
minute Apgar score < 5, or need for respiratory support at black race and oxytocin use and were tested using the
10 minutes of life. Respiratory morbidity included need for Hosmer–Lemeshow goodness-of-fit test. We explored spe-
ventilator support or respiratory distress diagnosed clini- cific features within the category II FHR patterns to identify
cally by nasal flaring, subcostal/intercostal retractions, and whether NC in the setting of specific features conferred risk.
need for supplemental oxygen to main oxygen saturation All statistical analyses were performed using STATA software
> 95%. Secondary outcomes included components of the (version 10.0 [special edition], StataCorp, College Station, TX).
composite as well as NICU admission, umbilical artery cord
pH < 7, and 5-minute Apgar score < 7.
Results
Gestational age was calculated based on the woman’s first
ultrasound examination in the pregnancy and last menstrual Among 8,580 patients meeting the inclusion criteria, 2,071
period.22 A woman was considered to have diabetes mellitus women (24.14%) had an NC at the time of delivery. Women
if she had a diagnosis of type 1/type 2 in the medical record or with an NC at delivery were more likely to be white and of
gestational diabetes mellitus based on the National Diabetes AMA and were less likely to have a prior cesarean delivery
Group criteria.23 A hypertensive disorder in pregnancy was (►Table 1).
defined as chronic hypertension, gestational hypertension, There was no significant difference in the risk of the
or preeclampsia.24 Maternal and neonatal demographic data primary outcome of neonatal composite morbidity (adjusted
obtained from the medical record included type of labor odds ratio [aOR]: 0.99; 95% confidence interval [CI]: 0.83–
(spontaneous or induced), oxytocin use, mode of delivery 1.18) (►Table 2). There were also no differences in the
(vaginal, cesarean, operative vaginal), use of regional components of the composite with the exception of sei-
anesthesia, neonatal birth weight, and maternal complica- zure(s), which was associated with a higher risk (aOR: 2.62;
tions. Maternal complications were classified as those during 95% CI: 1.03–6.68) in neonates with an NC. All infants with
delivery (shoulder dystocia, fever, retained placenta, and seizures underwent magnetic resonance imaging (MRI) of
other) or postpartum (wound infection, fever, transfusion, the head, and the results were normal in 3/8 neonates with
hemorrhage, endomyometritis). Small for gestational age NC versus 5/10 neonates without NC. Rates of NICU admis-
was defined as birth weight < 10th percentile based on sion, arterial cord pH < 7, and low 5-minute Apgar score < 7
the Alexander growth curve reference.25 were also similar between groups (►Table 2). With regard to
Obstetric research nurses, formally trained to system- labor characteristics, patients with NC were more likely to
atically review EFM patterns using the National Institute of receive oxytocin (aOR 1.15; 95% CI: 1.04–1.28) and have an
Child Health and Human Development criteria,26 were operative vaginal delivery (OVD) (6.4 vs. 4.3%; p < 0.01; aOR
blinded to all clinical data and extracted EFM patterns in 1.47; 95% CI: 1.18–1.81) and less likely to deliver by cesarean
the 120 minutes prior to delivery. These patterns were (13.4 vs. 18.1%; p < 0.01; aOR 0.73; 95% CI: 0.63–0.84)
categorized according to fetal heart rate (FHR) baseline, (►Table 3). The most common indication for both cesarean
variability, number of accelerations, and number/type of section and OVD was nonreassuring fetal status.
decelerations.27 Decelerations were considered repetitive if We further examined the FHR characteristics in the
they occurred with 50% of uterine contractions in any 30 minutes prior to delivery. The presence of an NC was
20-minute window. Prolonged decelerations were defined associated with a significant increase in repetitive late

American Journal of Perinatology


Electronic Fetal Monitoring and Neonatal Outcomes Carter et al.

Table 1 Comparison of baseline characteristics in the presence decelerations (aOR: 1.45; 95% CI: 1.12–1.87), repetitive
or absence of a nuchal cord variable decelerations (aOR: 1.41; 95% CI: 1.27–1.58), and
overall category II tracings (aOR: 1.53; 95% CI: 1.38–1.70)
Nuchal cord, No nuchal cord, p-Value (►Table 4).
N ¼ 2,071 N ¼ 6,509
Among patients with an OVD, those with an NC were more
Maternal age 25 (21–31) 25 (21–30) <0.01
than twice as likely (aOR: 2.40; 95% CI: 1.14–5.02) to have
median (IQR)
repetitive late decelerations, but the rates of repetitive
AMA (35 years) 223 (10.77) 541 (8.31) 0.01
variable decelerations were similar in the presence or
Race
absence of an NC (►Table 5).
Black 1,265 (61.08) 4,300 (66.06) <0.01
White 524 (25.30) 1,417 (21.77)
Discussion
Latino/Hispanic 161 (7.77) 452 (6.94)
Asian 7 (0.34) 22 (0.34) Our study demonstrates that NC at delivery is common and
Native American 85 (4.10) 233 (3.58)
associated with category II EFM parameters and higher rates
of OVD in infants at or beyond 37 weeks. However, there is no
Other 14 (0.68) 38 (0.58)
significant association between NC and neonatal morbidity;
Unknown 15 (0.72) 47 (0.72)
thus, reassurance can be provided to parents when NC is
Obese 1,141 (55.09) 3,586 (55.09) 0.99 diagnosed and there is likely no utility for NC screening.
Asthma 281 (13.57) 896 (13.77) 0.85 Previous literature has shown opposing results regarding
Diabetes 85 (4.10) 272 (4.18) 0.90 the significance of an NC. In some reports, presence of an NC

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Chronic hypertension 95 (4.59) 310 (4.76) 0.76 has been associated with poor neonatal outcomes including
Hypertensive 414 (19.99) 1,317 (20.23) 0.81 unexplained quadriplegia,28 fetal distress, birth asphyxia,
disorder during and neonatal death.29 Several small retrospective studies
pregnancy found NC to be associated with increased rates of nonreas-
Medical or 678 (32.74) 2,118 (32.54) 0.87 suring FHR patterns (variable decelerations, fetal bradycar-
antepartum
complication
dia), meconium-stained amniotic fluid, operative delivery,
and acidic umbilical artery pH.1,8,10,13,16–18 In general, how-
Prior cesarean 158 (7.63) 603 (9.26) 0.02
section ever, the majority of previous studies have found no increase
Prior preterm birth 180 (8.69) 611 (9.39) 0.34
in the risk of neonatal morbidity associated with NC at
delivery.3,7
Nulliparity 891 (43.02) 2,780 (42.71) 0.80
The results of this study are in agreement with the
Alcohol use 27 (1.30) 63 (0.97) 0.19
suggestion that there is no significant risk of neonatal
Tobacco use 286 (13.81) 883 (13.57) 0.78 morbidity when an NC is present at delivery. Furthermore,
Drug use 229 (11.06) 762 (11.71) 0.42 in contrast to many earlier studies, our large study did not
find any significant association with neonatal death, cord
Abbreviations: AMA, advanced maternal age; IQR, interquartile range.
Note: Data are presented as n (%) unless otherwise noted. Values in bold acidosis, birth weight, low Apgar score, NICU admission, or
denote statistical significance (p < 0.05). respiratory morbidity.

Table 2 Comparison of neonatal outcomes in the presence or absence of a nuchal cord

Nuchal cord, No nuchal cord, p-Value OR aORa


N ¼ 2,071 N ¼ 6,509
Neonatal composite morbidity 180 (8.69) 577(8.86) 0.81 0.98 (0.82–1.17) 0.99 (0.83–1.18)
Neonatal death 2 (0.10) 2 (0.03) 0.23 3.14 (0.44–22.34) 3.34 (0.47–23.88)
Seizure 8 (0.39) 10 (0.15) 0.04 2.52 (0.99–6.39) 2.62 (1.03–6.68)
Hypoxic–ischemic encephalopathy 2 (0.10) 14 (0.22) 0.39 0.45 (0.10, 1.98) 0.43 (0.10, 1.92)
Need for hypothermic treatment 9 (0.43) 33 (0.51) 0.68 0.86 (0.41–1.79) 0.84 (0.40–1.75)
Respiratory morbidity 90 (4.35) 242 (3.72) 0.20 1.17 (0.92–1.51) 1.20 (0.94–1.54)
Hypotension requiring treatment 2 (0.10) 4 (0.06) 0.60 1.57 (0.29–8.59) 1.54 (0.28–8.47)
Suspected sepsis 144 (6.95) 483 (7.42) 0.48 0.93 (0.77–1.13) 0.94 (0.78–1.15)
NICU admission 33 (1.59) 99 (1.52) 0.83 1.05 (0.71–1.56) 1.04 (0.70–1.54)
Arterial cord pH < 7 6 (0.29) 19 (0.29) 1 0.99 (0.40–2.49) 0.95 (0.38–2.39)
5-minute Apgar < 7 57 (2.75) 151 (2.32) 0.27 1.19 (0.88–1.62) 1.22 (0.90–1.67)

Abbreviations: aOR, adjusted odds ratio; NICU, neonatal intensive care unit; OR, odds ratio.
Note: Data are presented as n (%). Values in bold denote statistical significance (p < 0.05)
a
Adjusted for maternal age, black race, and prior cesarean section.

American Journal of Perinatology


Electronic Fetal Monitoring and Neonatal Outcomes Carter et al.

Table 3 Comparison of pregnancy outcomes in the presence or absence of a nuchal cord

Nuchal cord, No nuchal cord, p-Value OR aORa


N ¼ 2,071 N ¼ 6,509
Gestational age (weeks)
Early term (37–38.6) 719 (34.72) 2,332 (35.83) 0.23 Reference Reference
Term (39–40.6) 1,185 (57.22) 1.06 (0.96–1.19) 1.05 0.94–1.17)
Late term (41) 167 (8.06) 3,597 (55.26) 0.93 (0.77–1.13) 0.91 (0.75–1.11)
580 (8.91)
Oxytocin use 1,437 (69.39) 4,309 (66.20) <0.01 1.16 (1.04–1.29) 1.15 (1.04–1.28)
Epidural 1,861 (89.86) 5,822 (89.45) 0.59 1.05 (0.89–1.23) 1.09 (0.93–1.29)
Small for gestational age 318 (15.35) 929 (14.27) 0.22 1.09 (0.95–1.25) 1.13 (0.99–1.30)
Induction of labor 937 (45.24) 2,850 (43.79) 0.24 1.06 (0.96–1.17) 1.05 (0.95–1.16)
Indication for delivery
Non-reassuring fetal status 289 (13.95) 894 (13.73) 0.80 1.01 (0.88–1.18) 1.05 (0.91–1.21)
Mode of delivery
Spontaneous vaginal delivery 1,660 (80.15) 5,045 (77.51) <0.01 Reference Reference

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Operative vaginal delivery 133 (6.42) 279 (4.29) 1.45 (1.16–1.79) 1.47 (1.18–1.81)
Cesarean delivery 278 (13.42) 1,181 (18.14) 0.71 (0.61–0.82) 0.73 (0.63–0.84)
Meconium 462 (22.31) 1,351 (20.76) 0.13 1.10 (0.97–1.24) 1.11 (0.98–1.25)

Abbreviations: aOR, adjusted odds ratio; OR, odds ratio.


Note: Data are presented as n (%). Values in bold denote statistical significance (p < 0.05).
a
Adjusted for maternal age, black race, and prior cesarean section.

Table 4 Fetal heart rate characteristics in 30 minutes prior to delivery in the presence or absence of a nuchal cord

Nuchal cord, No nuchal cord, p-Value OR aORa


N ¼ 2,071 N ¼ 6,509
Baseline
> 160 66 (3.19) 210 (3.23) 0.93 0.99 (0.75–1.31) 0.97 (0.73–1.29)
< 110 3 (0.14) 17 (0.26) 0.44 0.55 (0.16–1.89) 0.56 (0.16–1.91)
Variability
Moderate variability 1,016 (49.06) 2,931 (45.03) <0.01 1.18 (1.06–1.30) 1.16 (1.05–1.28)
Marked variability 2 (0.10) 9 (0.14) >0.99 0.70 (0.15–3.23) 0.75 (0.16–3.46)
Absent variability 0 1 (0.02) >0.99 – –
Accelerations/decelerations
Repetitive late decelerations 91 (4.40) 193 (2.97) <0.01 1.45 (1.13–1.88) 1.45 (1.12–1.87)
Repetitive variable decelerations 696 (33.61) 1,671 (25.67) <0.01 1.42 (1.27–1.58) 1.41 (1.27–1.58)
Repetitive prolonged decelerations 43 (2.08) 109 (1.67) 0.31 1.20 (0.84–1.72) 1.20 (0.84–1.71)
Category
1 35 (1.69) 185 (2.84) <0.01 0.59 (0.41–0.85) 0.58 (0.40–0.83)
2 1,410 (68.08) 3,772 (57.95) <0.01 1.54 (1.39–1.72) 1.53 (1.38–1.70)
3 0 1 (0.02) >0.99 – –

Abbreviations: aOR, adjusted odds ratio; OR, odds ratio.


Note: Data are presented as n (%). Values in bold denote statistical significance (p < 0.05).
a
Adjusted for maternal age, black race, and prior cesarean section.

A unique component of this study is the inclusion of EFM between NC and abnormal EFM parameters.30 In contrast,
data and its relation to neonatal morbidity. Few prior studies Sheiner et al reported that nonreassuring EFM patterns are
have evaluated the characteristics of EFM that are associated associated with NC.3 Our study found significant associations
with NC at delivery. Peregrine et al found no association with NC and category II EFM parameters. However, the lack of

American Journal of Perinatology


Electronic Fetal Monitoring and Neonatal Outcomes Carter et al.

Table 5 Fetal heart rate characteristics in 30 minutes prior to delivery in the presence or absence of a nuchal cord among patients
with an operative vaginal delivery

Nuchal cord, No nuchal cord, p-Value OR aORa


N ¼ 133 N ¼ 279
Repetitive late decelerations 16 (12.03) 15 (5.38) 0.02 2.40 (1.16–5.02) 2.40 (1.14–5.02)
Repetitive variable decelerations 47 (35.34) 78 (27.96) 0.14 1.40 (0.90–2.19) 1.42 (0.91–2.22)

Abbreviations: aOR, adjusted odds ratio; OR, odds ratio.


Note: Data are presented as n (%). Values in bold denote statistical significance (p < 0.05).
a
Adjusted for maternal age, black race, and prior cesarean section.

significant neonatal outcomes and interventions associated The use of a composite outcome may be viewed as a
with an NC calls into question whether its association with limitation of this study. However, we believe that the use of
nonreassuring FHR patterns is clinically relevant. Our results a composite was necessary because the individual components
suggest that the higher rates of OVD in the NC group were in of the composite are rare complications. In addition, the
response to category II EFM. Therefore, it is possible that this neonatal outcomes that were considered as part of the com-
intervention improved the rates of neonatal morbidity in the posite are more clinically meaningful than more commonly
NC group. occurring surrogate measures of morbidity, such as low Apgar
Multiple factors support the validity of our study. Pro- score, but they are short term, and we are unable to comment

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spective interpretation of FHR tracings by nurses who are on any long-term sequelae of NC at the time of delivery.
blinded to clinical outcome is a major strength. Additionally, In summary, NC at delivery is associated with category II
to the best of our knowledge, this is the largest prospective EFM parameters, which likely influences provider behaviors
study to date of patients with an NC at delivery. Our EFM and increases the likelihood for OVD. Fortunately, concerning
analysis was limited to the final 30 minutes prior to delivery EFM patterns do not translate into fetal compromise—either
since the impact of an NC is most likely to be experienced because the NC is innocuous or clinical practice patterns
during the second stage of labor with the descent of the fetus. cause providers to intervene before fetal compromise occurs
Limiting our patient population to women reaching in the second stage. Either way, parents and providers alike
the second stage and the final 30 minutes of monitoring can be reassured that there is no significant association
helped us discriminate between variables most likely caused between NC and short-term neonatal morbidity within the
by an NC versus other sources. context of current obstetric practice patterns.
Given the large sample size and small amount of missing
data, due to our prospective study design, findings can be Funding
applied widely and support the generalizability of our This study is supported by the National Institute of Child
findings. Health and Human Development (NICHD) grant number
Despite strengths, this study has some potential limita- R01H061619–04 (PI: Alison Cahill). Dr. Carter was sup-
tions to be considered when evaluating our results. As with ported by a National Institutes of Health T32 training
all cohort studies, confounding is a concern. We used appro- grant (5T32HD055172–05) and the Robert Wood Johnson
priate statistical techniques to adjust for confounders, but Foundation #74250. The contents of this publication are
there is a possibility of residual confounding by unmeasured solely the responsibility of the authors and do not neces-
factors. For example, the presence of nuchal is not routinely sarily represent the official view of the Robert Wood
noted on ultrasound reports at our institution. However, we Johnson Foundation.
do not know whether clinicians managing labor had knowl-
edge regarding the presence of an NC by bedside ultrasound Conflict of Interest
prior to delivery and, if so, whether this knowledge altered None declared.
management. It is also possible that neonatal outcomes were
similar between groups because there was a higher level of
intervention, such as OVD in the NC group in response to
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American Journal of Perinatology

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