Journal of Perinatology (2015) 35, 919–923

© 2015 Nature America, Inc. All rights reserved 0743-8346/15

www.nature.com/jp

ORIGINAL ARTICLE
The association between umbilical cord abnormalities and
the development of non-reassuring fetal heart rate leading
to emergent cesarean deliveries
E Weiner1, N Fainstein1, L Schreiber2, R Sagiv1, J Bar1 and M Kovo1

OBJECTIVE: To study the contribution of umbilical cord (UC) abnormalities in emergent cesarean deliveries (ECDs) for non-
reassuring fetal heart rate (NRFHR) and to explore their association with placental histopathology and neonatal outcome.
STUDY DESIGN: Data from 530 ECDs for NRFHR were reviewed for the occurrence of UC abnormalities. Those included the
presence of UC entanglements, the number and location of loops, true knots and short cord ( o50 cm). Multiple UC entanglements
were defined as ⩾ 2 UC loops. Results were compared with 530 vaginal deliveries (VD group) matched for maternal age, parity and
gestational age. Additionally, we compared neonatal outcome and placental histopathology in cases of ECDs with a single vs
multiple UC entanglements. Neonatal outcome consisted of low Apgar score (⩽7 at 5 min), cord blood pH ⩽ 7.1 and composite
neonatal outcome that was defined as one or more of respiratory distress, necrotizing enterocolitis, sepsis, transfusion, ventilation,
seizure, hypoxic-ischemic encephalopathy, phototherapy or death. Placental lesions were classified as: lesions related to maternal
vascular supply, lesions related to fetal vascular supply (consistent with fetal thrombo-occlusive disease), and maternal and fetal
inflammatory responses.
RESULTS: UC entanglements, true knots and short cords were all more common in the ECD group compared with the VD group,
Po 0.001, P = 0.002, P = 0.004, respectively. The rate of one loop entanglement did not differ between the groups. The rate of
multiple UC entanglements was higher in the ECD group compared with the VD group, 20.6% vs 6.4%, respectively, Po 0.001. ECDs
with multiple compared with single UC entanglement had higher rate of adverse neonatal outcome, P = 0.031, and more placental
fetal vascular lesions 19.3% vs 8.1%, P = 0.027, respectively.
CONCLUSION: Multiple UC entanglements, true knots and short cords were more common in ECDs for NRFHR, suggesting their
role in the development of fetal placental vascular lesions and adverse neonatal outcome.
Journal of Perinatology (2015) 35, 919–923; doi:10.1038/jp.2015.102; published online 20 August 2015

INTRODUCTION Most of the studies lack information about the number of

Non-reassuring fetal heart rate (NRFHR) monitoring during labor is
one of the major indications for immediate delivery by performing
an emergent cesarean delivery (ECD) worldwide.1,2
Several umbilical cord (UC) abnormalities have been associated
with the development of NRFHR and adverse perinatal outcome.
Such UC abnormalities include cord entanglements, hypercoiling,
true knots, strictures and short cords.3 Multiple mechanisms may
lead to the development of NRFHR in association with placental
pathology and UC abnormalities and macroscopic and
microscopic changes.4,5 Notably, UC abnormalities occur also in
uneventful normal vaginal deliveries.
The association of nuchal cord (cord around neonatal neck) and
pregnancy outcome has been studied thoroughly, suggesting an
increased risk for induction of labor, slow progress of labor, fetal
distress, shoulder dystocia, meconium, low Apgar scores and
higher rate of instrumental and CDs.6–14 On the other hand, others
found no association between the presence of nuchal cord and
adverse neonatal outcome or labor complications.15–17
Furthermore, in a very large study including 420 000 pregnancies
with nuchal cord, lower rate of CDs and lower perinatal mortality
was observed, compared with deliveries without nuchal cord.18
UC loops entangled, sites of entanglements other than the fetal
neck and other cord abnormalities. We aimed to fill this gap and
to study the association of different UC abnormalities, in particular
UC entanglements with respect to site and the number of cord
loops in pregnancies complicated with ECD. Additionally,
we aimed to study the association between single vs multiple
UC entanglements in cases of NRFHR requiring ECD with
pregnancy outcome and placental histopathology. We
categorized placental lesions into those that are associated with
maternal vascular circulation, changes in the fetal vascular supply
(thrombo-occlusive disease) and inflammatory lesions of maternal
and fetal origin.19
MATERIALS AND METHODS
The medical records of all women who underwent ECD for NRFHR between
37 and 42 weeks of gestation at the labor ward of Edith Wolfson Medical
Center, Holon, Israel from January 2009 to June 2013 were reviewed. Fetal
heart rate monitor tracings were interpreted by the obstetrical staff
according to the American College of Obstetrics and Gynecology
guidelines.20

1
Department of Obstetrics and Gynecology, Edith Wolfson Medical Center, affiliated with Sackler Faculty of Medicine, Tel Aviv University, Holon, Israel and 2Department of
Pathology, Edith Wolfson Medical Center, affiliated with Sackler Faculty of Medicine, Tel Aviv University, Holon, Israel. Correspondence: Dr E Weiner, Department of Obstetrics and
Gynecology, Edith Wolfson Medical Center, affiliated with Sackler Faculty of Medicine, Tel Aviv University, P.O. Box 5, Holon 58100, Israel.
E-mail: masolbarak@gmail.com
Received 24 March 2015; revised 8 July 2015; accepted 9 July 2015; published online 20 August 2015
 Contribution of UC abnormalities in ECD for NRFHR
E Weiner et al
920
Excluded from the study were patients with additional indications for
ECD such as abnormal progress in labor, patients with evidence of fetal or
neonatal malformations, multiple pregnancies, preterm labor (o 37 weeks
of gestation), non-vertex presentation or cases with missing data. The
control group included patients who underwent normal vaginal deliveries
at the same time period matched for maternal age, gestational age and
parity.
As part of our departmental protocol, documenting UC abnormalities
observed during cesarean or vaginal deliveries by the obstetrics staff is
included in every delivery report. UC abnormalities included: cord
entanglements loops around neck (nuchal cord loop), trunk or limb, as
well as the number of loops, true knots and short UCs ( o50 cm). Multiple
UC entanglements were defined as ⩾ 2 loops of the UC around neonatal
neck, trunk or limb.
Data collection
The clinical data for the present study were collected from the patients’
medical and surgical files and included demographic and labor
characteristics: age, gravidity and parity, body mass index, pregestational
diabetes mellitus, gestational diabetes mellitus (A1 and A2), preeclampsia,
trial of labor after cesarean section (TOLAC) attempt, gestational age at
delivery, oligohydramnious (amniotic fluid index o5 cm), the presence of
intrapartum fever 438 °C, and meconium. Gestational age was confirmed
by first-trimester ultrasonography.
The following information was collected from the neonatal records:
Apgar scores, cord blood pH, sepsis (positive blood or cerebrospinal fluid
culture), need for blood transfusion, need for phototherapy, respiratory
distress syndrome, need for mechanical ventilation, necrotizing
enterocolitis, intraventricular hemorrhage, hypoxic ischemic encephalo-
pathy, seizures, and death. Birth weight percentile for gestational age was
assigned using the updated Israeli growth charts.21 Fetal growth restriction
(FGR) was defined as actual birth weight o 10th% for gestational age.
For the purpose of the study, we compared the prevalence and types of
UC abnormalities between ECD and normal vaginal deliveries (controls).
Additionally, we compared pregnancy characteristics, neonatal outcome
and placental histopathology in cases of ECDs with a single UC
entanglement (nuchal or body or limb) vs multiple UC entanglements.
Approval for the study was obtained from the Local Ethics Committee.
Placental examination
As part of departmental protocol, in every case of ECD placentas are sent
to histopathology evaluation. Placental pathology examinations were
performed using a standard protocol, described by us in previous
studies.22,23 Briefly, after fixation in formalin and removal of the
membranes and cord, the placentas were weighed. For each placenta, at
least five tissue samples were embedded in paraffin blocks for microscopic
assessment. All examinations were done by a single pathologist (LS).
number of coils by the length of the cord in centimeters. Hypercoiling was
diagnosed in cases of umbilical coiling index 40.3 coils cm− 1.24
Statistics
Continuous variables were calculated as mean ± s.d. or median and range,
as appropriate. Categorical variables were calculated as rate (%).
Continuous parameters were analyzed by Student’s t-test and categorical
variables by chi-square test or by Fisher exact test, as appropriate.
A P-value of o0.05 was considered statistically significant. Data were
analyzed with the SPSS software, version 15.0 (SPSS, Chicago, IL, USA).
Composite neonatal outcome was defined as ⩾ 1 of the following
complications: Apgar scores ⩽ 7 in 5 min, cord blood pH ⩽ 7.1, sepsis, blood
transfusion, phototherapy, respiratory distress syndrome, transient
tachypnea of the newborn, mechanical ventilation, intraventricular
hemorrhage, seizures, hypoxic–ischemic encephalopathy, necrotizing
enterocolitis, or death.
Composite placental maternal vascular supply lesions was defined as the
presence of ⩾ 1 maternal vascular supply abnormalities and composite
placental fetal vascular supply lesions was defined as the presence of ⩾ 1
fetal vascular supply abnormalities.
To identify independent risk factors for ECD, a multivariate stepwise
forward logistic regression analysis was performed. Preeclampsia, FGR and
TOLAC attempts served as independent variables.
RESULTS
During the study time period, 4507 CDs were performed out of
20 366 deliveries (CD rate of 22.1%). Of them, 530 ECD (ECD group)
were performed owing to NRFHR, as the only indication. Normal
matched VD (VD group) served as controls.
At the time of decision to perform an ECD, 494/530 (93.2%)
of the FHR tracings were interpreted as category 2 tracings and
36/530 (6.8%) as category 3 tracings according to the guidelines of
the American College of Obstetrics and Gynecology.20
Maternal and delivery characteristics are summarized in Table 1.
There were no between-group differences in maternal age,
gestational age at delivery, maternal body mass index, rate of
diabetes, oligohydramnious, intrapartum fever or meconium.
Higher rate of preeclampsia, FGR and TOLAC attempts
were observed in the ECD group compared with controls
(P = 0.003, P o0.001, Po 0.001 respectively).
Table 2 presents the different UC abnormalities observed in the
study groups. UC entanglements were the most common cord
abnormality observed in both groups. UC entanglements were
significantly more common in the ECD group compared with the

Placental lesions
Categorization of placental lesions was described by us in previous Table 1. Maternal and delivery characteristics in the ECD group
studies,22,23 and it is based according to the criteria that were adopted by compared with the normal VD (control) group
the Society for Pediatric Pathology.19 Briefly, maternal vascular supply
abnormalities included: lesions resulting from loss of integrity of the Characteristic ECD group VD group P-value
maternal circulation, that is, placental, marginal and retro-placental
hemorrhages, vascular lesions related to maternal underperfusion (acute n = 530 n = 530
atherosis and mural hypertrophy), and villous changes related to maternal
underperfusion (increased syncytial knots, villous agglutination, increased Maternal age (years) 29.7 ± 5.1 30.1 ± 5.2 0.206
intervillous fibrin deposition and villous infarcts). Fetal vascular supply Gestational age (weeks) 39.0 ± 2.4 39.1 ± 2.5 0.506
abnormalities included findings consistent with fetal thrombo-occlusive BMI (kg m − 2) 24.7 ± 5.4 24.1 ± 4.8 0.056
disease: vascular lesions (thrombosis of the chorionic plate and stem Diabetes mellitus 28 (5.3) 22 (4.2) 0.469
villous vessels) and villous changes (hypovascular, fibrotic and avascular Preeclampsia 43 (8.1) 20 (3.8) 0.003
villi). Placental findings consistent with chorioamnionitis were defined by Oligohydramnious 32 (6.0) 19 (3.6) 0.084
the presence of an inflammatory neutrophil infiltrate at ⩾ 2 sites on the TOLAC attempts 42 (7.9) 14 (2.6) o0.001
chorionic plate and extraplacental membrane. The maternal inflammatory FGRo10th percentile 99 (18.6) 48 (9.1) o0.001
response was divided into three stages: early, acute subchorionitis Intrapartum fever 438 °C 22 (4.2) 13 (2.5) 0.168
(stage 1); intermediate acute chorioamnionitis (stage 2); and late, severe Meconium 107 (20.1) 89 (16.8) 0.178
chorioamnionitis (stage 3). The fetal inflammatory response was also
Abbreviations: BMI, body mass index; ECD, emergent cesarean delivery;
divided into three stages: early, umbilical phlebitis (stage 1); intermediate,
FGR, fetal growth restriction; TOLAC, trial of labor after cesarean delivery;
umbilical arteritis (stage 2); and concentric umbilical perivasculitis VD, normal vaginal delivery. All data are shown as number (%) or
(necrotizing funisitis, stage 3). mean ± s.d. Diabetes mellitus: include pregestational and gestational
Abnormal cord insertion was defined as either velamentous or marginal diabetes (GDMA1 and A2).
insertion. Umbilical coiling index was calculated by dividing the total

Journal of Perinatology (2015), 919 – 923 © 2015 Nature America, Inc.

 Contribution of UC abnormalities in ECD for NRFHR
E Weiner et al
921
Table 2. Umbilical cord abnormalities in the ECD group and in the Table 3. Maternal and delivery characteristics in ECDs with single vs
control group multiple umbilical cord entanglements

Umbilical cord abnormalities ECD group VD group P-value Single UC Multiple UC P-value
entanglement entanglements
n = 530 n = 530
n = 99 n = 109
Umbilical cord entanglements 208 (39.2) 117 (22.1) o0.001
Maternal age (years) 29.6 ± 5.2 29.7 ± 5.2 0.89
Single UC entanglement 99 (18.7) 83 (15.7) 0.221 Gestational age 39.6 ± 1.32 39.9 ± 1.12 0.077
Nuchal loop 65 (12.3) 68 (12.8) 0.853 (weeks)
UC around limb 16 (3) 6 (1.1) 0.051 Nulliparity 58 (58.6) 64 (58.7) 1
UC around trunk 18 (3.4) 9 (1.7) 0.117 BMI (kg m −2) 24.6 ± 5.2 24.8 ± 5.3 0.784
Diabetes mellitus 6 (6.1) 3 (2.8) 0.314
Multiple UC entanglements 109 (20.6) 34 (6.4) o0.001 Preeclampsia 10 (10.1) 6 (5.5) 0.298
Nuchal loops 81 (15.3) 31 (5.8) o0.001 Oligohydramnions 9 (9.1) 3 (2.8) 0.072
UC loops around limb 16 (3) 1 (0.2) o0.001 TOLAC attempts 12 (12.1) 12 (11.0) 0.831
UC loops around trunk 12 (2.3) 2 (0.4) 0.01 Active labor 45 (45.5) 57 (52.2) 0.334
FGRo10th percentile 21 (21.2) 19 (17.4) 0.597
True knot 18 (3.4) 4 (0.8) 0.004 Intrapartum fever 3 (3.0) 5 (4.6) 0.502
Short cord o50 cm 17 (3.2) 4 (0.8) 0.006 438 °C
Meconium 33 (33.3) 36 (33.0) 1
Abbreviations: ECD, emergent cesarean delivery; UC, umbilical cord; VD,
normal vaginal delivery. All data are shown as number (%). Abbreviations: BMI, body mass index; ECD, emergent cesarean delivery;
FGR, fetal growth restriction; TOLAC, trial of labor after cesarean delivery;
UC, umbilical cord. Diabetes mellitus: include pre-gestational and gesta-
tional diabetes (GDMA1 and A2). All data are shown as number (%) or
VD group, 39.2% vs 22.1%, respectively, P o 0.001. The rate of mean ± s.d.
single UC entanglement did not differ between the ECD and the
VD groups, 18.7% vs 15.7%, respectively, P = 0.221. The most
common site of single UC entanglement was neonatal neck
(12.3% vs 12.8% in the ECD compared with the VD group, Table 4. Immediate neonatal outcome in ECDs with single vs multiple
respectively, P = 0.853). The rate of single UC loop at other umbilical cord entanglements
neonatal sites, such as neonatal limb or trunk, did not differ
between the groups. Single UC Multiple UC P-value
The rate of multiple UC entanglements was significantly higher entanglement entanglements
in the ECD group compared with the VD group, 20.6% vs 6.4%,
respectively, P o0.001. n = 99 n = 109
Multiple UC entanglements around neonatal neck, limb or trunk
were all more common in the ECD group compared with the Neonatal weight (g) 3158 ± 484 3272 ± 411 0.067
VD group, P o 0.001, P o 0.001, P = 0.01, respectively. With respect Neonatal 5.34 ± 1.9 5.91 ± 2.2 0.047
to other UC abnormalities: ECD group compared with the VD hospitalization (days)
group had higher rate of true knots, 3.4% vs 0.8%, respectively, Umbilical cord 3 (3) 6 (5.5) 0.502
P = 0.004, and short cords, 3.2% vs 0.8%, respectively, P = 0.006. pH ⩽ 7.1
5-min Apgar 1 (1) 2 (1.8) 1
By using multivariate stepwise forward logistic regression score ⩽ 7
analysis, ECD was found to be independently associated with Respiratory 4 (4) 8 (7.3) 0.38
total UC entanglements (odds ratio (OR) = 1.6, 95% confidence morbiditya
interval (CI) = 1.2 to 1.8, P = 0.008), multiple UC entanglements Cerebral morbidityb 0 0 1
(OR = 2.9, 95% CI = 2.1 to 3.9, P = 0.012), true knot (OR = 2.7, 95% Neonatal sepsis 0 1 (0.9) 1
CI = 1.4 to 3.2, P = 0.007) and short cord (OR = 2.6, 95% CI = 1.9 to Necrotizing 0 0 1
3.6, P = 0.004). enterocolitis
Out of the 530 ECDs, UC entanglements were observed in 208 Blood transfusions 0 1 (0.9) 1
cases (39.2%). Cases were divided into those with single vs Phototherapy 3 (3) 6 (5.5) 0.502
Neonatal death 0 0 1
multiple UC entanglements. Table 3 presents maternal and Composite adverse 9 (9.1) 22 (29.3) 0.031
delivery characteristics in ECDs with single UC entanglement vs neonatal outcome
multiple UC entanglements. There were no between-group
differences in maternal age, gestational age at delivery, maternal Abbreviations: ECD, emergent cesarean delivery; UC, umbilical cord. All data
body mass index, nulliparity, rate of pregnancy complications as are shown as number (%) or mean ± s.d. aRespiratory morbidity included
the presence of respiratory distress syndrome or transient tachypnea
diabetes, preeclampsia and FGR, rate of oligohydramnions,
of the newborn or mechanical ventilation or need for respiratory support.
intrapartum fever or meconium. Neonatal outcome parameters b
Cerebral morbidity included the presence of intraventricular hemorrhage
of cases with single loop vs multiple UC loops are summarized in or seizures or hypoxic–ischemic encephalopathy.
Table 4. Neonatal hospitalization was longer in the multiple
UC entanglements vs single UC entanglement group,
5.91 ± 2.2 days vs 5.34 ± 1.9 days, respectively, P = 0.047. Compo-
site adverse neonatal outcome was higher in the multiple UC UC entanglements vs single UC loop group, 438 ± 104 vs
entanglements vs single UC entanglement group, 29.3% vs 9.1%, 468 ± 102 g, respectively, P = 0.037. Higher rate of fetal vascular
respectively, P = 0.031. supply lesions (composite) was observed in the multiple UC
Table 5 presents the rate of different placental lesions in the entanglements group compared with the single UC entanglement
group with single UC entanglement vs multiple UC entanglements group, 19.3% vs 8.1%, respectively, P = 0.027. There was no
group. Placenta weights were significantly lower in the multiple difference in the rate of abnormal cord insertion, hypercoiling

© 2015 Nature America, Inc. Journal of Perinatology (2015), 919 – 923

 Contribution of UC abnormalities in ECD for NRFHR
E Weiner et al
922
Table 5. Placental histopathology lesions in emergent cesarean delivery group with single vs multiple umbilical cord entanglements

Single UC entanglement Multiple UC entanglements P-value

n = 99 n = 109

Placental weight (g) 468 ± 102 438 ± 104 0.037

Placental weight o10% 11 (11.1) 16 (14.7) 0.537
Hypercoiled cord 12 (12.1) 16 (14.7) 0.686
Abnormal cord insertion 13 (13.1) 19 (17.4) 0.444

Maternal vascular supply lesions

Placental hemorrhage 2 (2) 5 (4.6) 0.449
Vascular lesions related to maternal under-perfusion 3 (3) 8 (7.3) 0.220
Villous changes related to maternal under-perfusion 36 (36.3) 30 (27.5) 0.182
Composite maternal vascular supply lesions 41 (41.4) 43 (39.4) 0.779

Fetal vascular supply lesions

Vascular lesions consistent with FTOD 2 (2) 8 (7.3) 0.105
Villous lesions consistent with FTOD 6 (6.1) 13 (11.9) 0.156
Composite fetal vascular supply lesions 8 (8.1) 21 (19.3) 0.027

Inflammatory lesions
MIR stages 1–3 24 (24.2) 21 (19.5) 0.404
FIR stages 1–3 7 (7.1) 6 (5.5) 0.776
Abbreviations: ECD, emergent cesarean delivery; FIR, fetal inflammatory response; FTOD, fetal thrombo-occlusive disease; MIR, maternal inflammatory
response; UC, umbilical cord. Continuous variables are presented as mean ± s.d. and categorical variables as n (%).

cord, maternal vascular supply lesions and placental inflammatory
lesions between the groups.
DISCUSSION
The present study demonstrates a significant high rate of UC
abnormalities in patients who underwent emergent CD owing to
NRFHR, compared with normal vaginal deliveries. The most
common UC abnormality was nuchal cord entanglements.
However, we found that only multiple UC entanglements and
not a single loop entanglement were associated with ECD. These
findings are in concordance with previous studies demonstrating
an association of gross cord abnormalities with intrapartum
complications, FGR and stillbirth.6–10,25–27 However, the exact
relation between cord abnormalities or entanglements and their
effect on delivery and pregnancy outcome is still controversial.18
Multiple cord loops are reported in 0.3% to 3.8% of deliveries;4
nevertheless, the current study demonstrate a much higher
rate of multiple UC entanglements in patients who undergo ECD
(20.6%), suggesting its role in the development of NRFHR. UC
entanglements can cause alterations in cord blood flow.28 These
alterations can be caused either from direct compression or from
stretch during fetal descent, which lead to transient cessation of
cord blood flow, which will be expressed as NRFHR monitor. Other
possible mechanism by which multiple UC entanglements could
affect neonatal outcome is through their influence on the
placenta.
Following the same line, we found that, in pregnancies
complicated with ECD, owing to NRFHR, the presence of multiple
UC entanglements was associated with higher rate of composite
adverse neonatal outcome, as compared with those with a single
UC loop. Additionally, we evaluated placental histology findings in
all ECD owing to NRFHR and demonstrated that cases with
multiple UC entanglements had lower placental weights and
higher rate of fetal vascular supply lesions, specifically, lesions
consistent with fetal thrombo-occlusive disease. Fetal vascular
obstructive lesions are probably the result of stasis, hyper-
coagulability and vascular damage within the fetal circulation of
the placenta.29 Redline4 studied UC abnormalities and placental
lesions in 125 neurological impaired infants, demonstrating that
UC entanglements and cord abnormalities are significantly
increased in placentas with fetal thrombotic vasculopathy, thus
directly contributing to the development of this placental lesion.
Saleemuddin et al.5 demonstrated that placentas with fetal
thrombotic vasculopathy were associated with higher rate of
pregnancy complications, such as stillbirth, FGR, oligohydram-
nious and fetal cardiac abnormalities. Our findings point to the
association between multiple cord entanglements and the
development of fetal vascular supply lesions, suggesting an
indirect evidence for the presence of compromised UC blood flow,
leading to NRFHR and impaired neonatal outcome. Still, despite
these observations, the impact of screening for UC entanglements
prior to labor, by Doppler ultrasound on pregnancy and neonatal
outcome, is contradictive.8,30,31
The present study is unique in several aspects; there are other
publications on the association of UC abnormalities and NRFHR.
Yet, to the best of our knowledge, we are the first to compare
neonatal outcome and placental histopathology in cases of single
vs multiple UC entanglements. Second, we applied placental
histopathology criteria that were validated and adopted by the
Society of Pediatrics Pathology19 and analyze placentas in terms of
maternal and fetal vascular supply and maternal and fetal
inflammatory responses.
We are aware of the limitations of our study: (1) Because of its
retrospective design, clinical follow-up was limited. Only early
neonatal complications could be recorded and analyzed; (2)
Histological evaluation of the cord and placentas were available
only for the ECD. Placentas from normal VD are not routinely sent
to histology evaluation; (3) The term NRFHR monitor is subject to
considerable variations of interpretation among maternal–fetal
medicine specialists. There is a wide spectrum of abnormal FHR
patterns, especially in category 2 tracings, not necessarily
suggesting fetal compromise;32–34 (4) Unintended bias by the
obstetrician attempting to identify an etiology for NRFHR may
have occurred, leading to a more detailed documentation of UC
gross abnormalities in the ECD group compared with cases of
normal deliveries; (5) Antenatal management probably cannot be
directly deduced from the present study.

Journal of Perinatology (2015), 919 – 923 © 2015 Nature America, Inc.


In conclusion, UC abnormalities and mostly multiple UC
entanglements are associated with the development of NRFHR
and adverse neonatal outcome. The mechanisms that participate
in the development of fetal hypoxia leading to NRFHR involve
placental and UC macroscopic and microscopic abnormalities.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
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