Placenta 34 (2013) 583e588

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Placenta
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Gross patterns of umbilical cord coiling: Correlations with placental

histology and stillbirth
L.M. Ernst a, *, L. Minturn a, M.H. Huang a, E. Curry a, E.J. Su b
a
Northwestern University Feinberg School of Medicine, Department of Pathology, Chicago, IL, USA
b
Northwestern University Feinberg School of Medicine, Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Chicago, IL, USA

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: The purpose of this study was to dene gross patterns of umbilical cord hypercoiling and
Accepted 5 April 2013 determine correlations with histological features in the placenta and/or perinatal outcomes such as
stillbirth.
Keywords: Methods: Gross images of placentas with hypercoiled umbilical cords (>3 coils/10 cm) were assigned a
Avascular villi major umbilical coiling pattern and the direction (right or left) of the coiling. Denitions of 4 gross coiling
Fetal thrombotic vasculopathy
patterns were established: undulating, rope, segmented, and linked, each with progressively deeper
Hypercoiling
indentations in cord diameter. Outcome variables obtained from placental pathology reports and
Stillbirth
Umbilical coiling index
maternal medical records included histological abnormalities indicative of signicant chronic fetal
vascular obstruction, such as fetal vascular thrombi, avascular villi, villous stromal-vascular karyorrhexis,
and fetal thrombotic vasculopathy, and stillbirth.
Results: 318 placentas/umbilical cords met inclusion criteria. The rope pattern was the most common
(52%), followed by the undulating (26%), segmented (19%) and linked (3%) patterns. The segmented and
linked gross coiling patterns were signicantly correlated with histologic evidence of chronic fetal
vascular obstruction and stillbirth, when compared with the ropeand undulating patterns. Cords with
right twists were also signicantly correlated with histologic evidence of chronic fetal vascular
obstruction and stillbirth when compared with cords with left twists. The number of cord coils per 10 cm
did not correlate with any of the outcome variables.
Conclusions: Among hypercoiled umbilical cords, specic gross patterns of coiling can be recognized, and
patterns with the most signicant indentation or pinching of the cord diameter are associated with
histological evidence of chronic fetal vascular obstruction and stillbirth.
2013 Elsevier Ltd. All rights reserved.

1. Introduction between 6 and 21% of pregnancies [2,3]. Pregnancies with hyper-

The umbilical cord is the vital link between the fetus and
placenta which carries oxygenated blood to the fetus via the um-
bilical vein and removes deoxygenated blood via the umbilical ar-
teries. One of the most characteristic gross features of the umbilical
cord is its helical coiling pattern. On average, the umbilical cord has
about one coil every 5 cm as dened by the Umbilical Coiling Index
(UCI) [1]. Hypercoiled umbilical cords with a coiling index greater
than 0.3 coils/cm are not uncommon, with incidence reported
Abbreviations: UCI, umbilical coiling index; FTV, fetal thrombotic vasculopathy.
* Corresponding author. Northwestern University Feinberg School of Medicine,
Department of Pathology, Olson Pavilion 2-461, 710 N. Fairbanks Court, Chicago, IL
60611, USA. Tel.: 1 312 926 4069; fax: 1 312 926 9830.
E-mail address: linda-ernst@northwestern.edu (L.M. Ernst).
coiled umbilical cords have increased incidence of pregnancy
complications [2e4], and adverse outcomes, such as fetal
demise [3].
Due to the relatively high incidence of umbilical cord hyper-
coiling and to personal, clinical observations that not all hyper-
coiled cords are associated with evidence of fetal vascular
obstruction and/or poor outcome, we hypothesized that beyond
the number of coils in the umbilical cord, other specic gross fea-
tures of the hypercoiled umbilical cord may contribute to delete-
rious effects on the fetus. In other words, UCI alone may not be
entirely informative about the potential of the umbilical cord
anatomy to contribute to an adverse outcome. To our knowledge,
the gross patterns of umbilical cord hypercoiling and their effect on
fetal outcome have not been well-studied. The purpose of the
present study was to dene and describe the gross patterns of
umbilical cord hypercoiling and to determine if there are any

0143-4004/$ e see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.placenta.2013.04.002
584 L.M. Ernst et al. / Placenta 34 (2013) 583e588
specic coiling patterns that correlate with evidence of chronic
fetal vascular obstruction in the placenta and/or stillbirth.
2. Methods
Placentas are submitted to the Pathology Department at Northwestern Memo-
rial Hospital/Prentice Womens Hospital based on criteria established by a multi-
disciplinary group of clinicians. Criteria are based on College of American Pathologist
guidelines [5] and include: gross abnormality of the placenta, stillbirth, intrauterine
growth restriction, preterm delivery less that 34 weeks gestation, severe pre-
eclampsia, clinical suspicion of infection or abruption, maternal malignancy, and
compromised clinical course of the neonate. As part of the routine examination of
placentas at our institution, all placentas received in pathology are photographed,
and the umbilical cord coils are counted and recorded as the number of 360 coils
per 10 cm segment. A diagnosis of hypercoiled umbilical cord was made based on
the gross description indicating that the umbilical cord had more than three coils
per 10 cm segment. After institutional review board approval, we searched the
pathology database between January 2009 and December 2010 for placentas with a
diagnosis of hypercoiled umbilical cord. Gross digital images of all singleton cases
were collected and examined. Placental images which did not include the umbilical
cord or where the umbilical cord was partially obscured or too short for analysis
(<10 cm) were excluded. Based on previous observations by the authors, a priori
denitions of the gross patterns of coiling were established. Coiling was divided into
4 major patterns: undulating, rope, segmented, and linked patterns (Fig. 1). The
undulating pattern was dened as a cord with a serpentine or loose S-shape to the
coils without signicant indentations between the coils. The rope pattern was
characterized by relatively tight coils but with a generally preserved/straight
external surface to the cord, similar to the appearance of a rope. The segmented
umbilical cord showed coils with indentations involving <50% of the diameter of the
cord between each coil, and the linked pattern displayed deeper indentations (>50%
of the cord diameter) between each coil (Fig. 2).
Gross photographs of placenta and umbilical cord were then reviewed by the
authors blinded to any clinical or other pathologic data. For each case, a major
umbilical coiling pattern and the direction, counterclockwise (left) or clockwise
(right), of the coiling was assigned. If a second, minor coiling pattern (involving less
than 50% of the cord length) was present, that pattern was also recorded. Cord
insertion was recorded and considered abnormal if marginal or velamentous.
Placental pathology reports nalized by a single pathologist (LE) were reviewed for
all cases.
Routine histologic sampling included at least two sections of umbilical cord, at
least one section of the membrane roll, three sections of the parenchyma with
maternal surface, and two full-thickness sections of parenchyma. Histologic ab-
normalities indicative of signicant chronic fetal vascular obstruction such as cho-
rionic or stem villous vascular thrombi, avascular villi, and villous stromal-vascular
karyorrhexis were recorded. Criteria for the histologic lesions was based upon
denitions created by the Society for Pediatric Pathology, perinatal section, fetal
vascular obstruction nosology committee [6]. Fetal vessel thrombi were dened by
the presence of occlusive or non-occlusive blood clots in chorionic or stem villous
vessels. The blood clots were characterized histologically by brin strands and
adherence to the endothelium. Avascular villi were dened as any focus of terminal
villi showing a total loss of villous capillaries with bland hyaline brosis of the
villous stroma. Villous stromal-vascular karyorrhexis was dened as terminal villi
showing karyorrhexis of fetal cells within the villous and capillary degenerative
Fig. 1. Schematic representation of the four gross umbilical cord coiling patterns.
changes. A diagnosis of severe fetal vascular obstruction, consistent with fetal
thrombotic vasculopathy (FTV) was recorded in cases with >15 avascular villi per
slide  fetal thrombi [6]. Clinical pregnancy data such as maternal age, gravidity,
parity, maternal medical complications, and gestational age was obtained from re-
view of the maternal medical record. The immediate outcome of the pregnancy, live
birth or stillbirth, was recorded.
All data were entered into a coded database to protect patient condentiality.
Umbilical cord coiling patterns were correlated with gross and histologic placental
characteristics and outcome using Chi-square analysis for categorical variables and
students t-test or one way analysis of variance (ANOVA) for continuous variables. All
statistical analyses were performed using IBM SPSS Statistics, version 20. P-
value < 0.05 was considered to indicate statistically signicant correlations.
3. Results
Our search of the Surgical Pathology database at Northwestern
Memorial Hospital/Prentice Womens Hospital returned 392
placental cases with hypercoiled umbilical cords. A total of 74 cases
were excluded based on the above exclusion criteria, leaving 318
cases qualifying for analysis. The gestational age of the patients
ranged from 19 weeks to 42 completed weeks of gestation with a
mean of 37.3  4.0 weeks. The remaining clinical characteristics of
these 318 pregnancies are shown in Table 1.
The most common umbilical cord coiling pattern identied was
the rope pattern which was seen in 164 cases or 52% of the um-
bilical cords analyzed. The second most common pattern was the
undulating pattern seen in 82 cases or 26% of the total group. The
segmented and linked patterns were less common, with 60 cases
showing the segmented pattern, and only 12 cases with the linked
pattern. See Table 2. There was no signicant difference in the
average UCI or number of coils per 10 cm length of cord between
the rope, segmented, and linked patterns. However, cords with the
undulating pattern had signicantly fewer coils per 10 cm segment
of cord. Abnormal umbilical cord insertion, either marginal or
velamentous, was seen in all coiling groups, and there was no
signicant difference in frequency of abnormal cord insertion
among the groups. See Table 2.
Stillbirth was identied in 18 cases and occurred across all cord
coiling groups, but was by far most frequently associated with the
linked pattern of coiling, occurring in nearly half (5/12, 42%) of
cases showing that coiling pattern. In addition, 56% of the stillbirths
had either the segmented or linked pattern of umbilical cord coil-
ing. FTV was present in 7/18 (39%) of the placentas associated with
stillbirth, but 12/18 (67%) showed some element of fetal vascular
obstructive pathology in the form of fetal vascular thrombi or
avascular villi. Therefore, only one third of the stillbirths were not
 L.M. Ernst et al. / Placenta 34 (2013) 583e588 585

Fig. 2. Placental images representing the four gross umbilical cord coiling patterns. A. Undulating pattern, B. Rope pattern, C. Segmented pattern, D. Linked pattern.

associated with histologic evidence of fetal vascular obstruction.
Umbilical cords with the linked pattern were associated with the
highest frequency of lesions associated with chronic fetal vascular
ow obstruction such as fetal vascular thrombi, avascular villi,
villous stromal-vascular karyorrhexis, and FTV, followed closely by
the segmented pattern. See Table 2.
Since the linked and segmented patterns both showed some
degree of umbilical cord indentation, while the undulating and
rope patterns did not, we dichotomized the four patterns into two
broader presentations of cord coiling: segmented linked and
the rope undulating categories. These two categories were
reanalyzed for the same outcome variables. The
segmented linked patterns of umbilical cord coiling showed
signicant correlations with fetal thrombi, avascular villi, villous
stromal-vascular karyorrhexis, fetal thrombotic vasculopathy, and
stillbirth when compared with the rope and undulating patterns.
See Table 3.
257 of the cords presented with a left-handed twist while 61 of
them presented with a right-handed twist. Right-handed coiling
correlated with a higher percentage of the histologic markers of
chronic fetal vascular obstruction (fetal thrombi, avascular villi,
villous stromal-vascular karyorrhexis, and FTV) and stillbirth than
left coiling. See Table 4. There were no signicant differences in the
incidence of abnormal cord insertion between the two coiling di-
rections. The spectrum of gross coiling patterns also differed
signicantly between cords that coiled to the right versus the left.
See Fig. 3. The most common coiling pattern in left hypercoiled
cords was the rope pattern (60%), while only 15% of the right
hypercoiled cords displayed the rope pattern. In contrast, the
segmented pattern was most frequent in right hypercoiled cords

Table 1
Clinical characteristics of pregnancies for placentas studied.

Parameter

Age Average 32.15 SD 6.0 Range 17e50

Race White 186 Black 51 Hispanic 40 Asian 18 Unknown 23
Gravity Median 2 Range 1e10
Parity Median 0 Range 0e8
Gestational age Average 37.3 SD 4.0 Range 19e42
Cigarettes Yes 6 No 312
Alcohol Yes 1 No 317
Drugs (THC only) Yes 2 No 316
Steroids Yes 41 No 277
Chronic hypertension Yes 13 No 305
Gestational hypertension Yes 9 No 309
Preeclampsia Mild 8 Severe 19 Superimposed 7 No 284
Pre-gestational diabetes Yes 5 No 313
Gestational diabetes Yes 11 No 307
Labor Yes 264 No 54
Route of delivery NSVD 162 Assisted vaginal 27 Cesarean section 129
Birth weight Average 2878.29 SD 845.8 Missing 1
Placental weight Average 421.23 SD 122.11
Sex Female 140 Male 177 Ambiguous 1

NSVD Normal Spontaneous Vaginal Delivery, SD standard deviation, THC Tetrahydrocannabinol.

586 L.M. Ernst et al. / Placenta 34 (2013) 583e588

Table 2
Frequency and associations of coiling patterns.

Coiling Frequency Abnormal cord # of coils per 10 cm Fetal thrombi Avascular villi Villous stromal-vascular Fetal thrombotic Stillbirth
pattern N (%) insertion N (%) mean SD N (%) N (%) N (%) karyorrhexis N (%) vasculopathy N (%) N (%)

Undulating 82 (26) 14 (17) 4.64  1.05 20 (24) 14 (17) 5 (6) 6 (7) 5 (6)
Rope 164 (52) 28 (17) 5.34  1.7 28 (17) 25 (15) 2 (1) 8 (5) 3 (2)
Segmented 60 (19) 10 (17) 5.43  1.5 19 (32) 19 (32) 5 (8) 8 (13) 5 (8)
Linked 12 (3) 1 (8) 5.50  1.5 6 (50) 5 (42) 2 (17) 3 (25) 5 (42)
P-value 0.963** 0.003^ 0.013* 0.009* 0.005** 0.027** 0.000**

For categorical variables: Pearson Chi-square* or Fishers exact**: For continuous variable: One way ANOVA^.

Table 3
Correlations of dichotomized coiling patterns.

Coiling Frequency Abnormal cord Fetal thrombi Avascular villi Villous stromal-vascular Fetal thrombotic Stillbirth
pattern N (%) insertion N (%) N (%) N (%) karyorrhexis N (%) vasculopathy N (%) N (%)

Undulating Rope 246 (77) 42 (17) 48 (20) 39 (16) 7 (3) 14 (6) 8 (3)
Segmented Linked 72 (23) 11 (16) 25 (35) 24 (33) 7 (10) 11 (15) 10 (14)
P-value NS 0.007 0.001 0.012 0.008 0.001

(41%) and the linked pattern was much more likely in right
hypercoiled cords than left (15% vs 1%).
Analysis of histologic outcome variables was also performed
excluding the 18 stillborn patients to determine if these correla-
tions remained robust in the liveborn population. Statistically sig-
nicant correlations remained in the segmented and linked
patterns with fetal vascular thrombi (19/62 vs 43/238, p 0.029),
avascular villi (18/62 vs 35/238, p 0.008), but not fetal thrombotic
vasculopathy (6/52 vs 12/238, p 0.171). Right umbilical cord
coiling also remained associated with fetal vascular thrombi among
liveborns (17/54 vs 45/246, p 0.03).
4. Discussion
To our knowledge this is the rst study to dene and examine
the signicance to specic gross patterns of umbilical cord hyper-
coiling and correlate the patterns with placental histologic ndings
of chronic fetal vascular obstruction and stillbirth. Cord coiling was
recorded rst by Berengarius in the 1500s, and studied intermit-
tently through the early 1900s [7]. Edmonds did an exceptional job
of summarizing this literature in 1954 [8], describing the spirals of
the cord, setting forth an index for determining their intensity
(index of twist), and enumerating many of the vital questions
concerning gross cord patterning. However, it was not until the
early 1990s that the description and documentation of umbilical
cord coiling became a routine part of the placental examination. In
1993 Strong noted that uncoiled cords were associated with unfa-
vorable fetal outcomes such as intrauterine death, preterm de-
livery, repetitive intrapartum fetal heart rate decelerations,
operative delivery for fetal distress, meconium staining, and
anatomical-karyotypic abnormalities [9]. Then a year later, he
dened the Umbilical Coiling Index (UCI) with the normal range of
coiling as 0.1e0.3 coils/cm umbilical cord [1]. His initial study
showed that umbilical cords outside the normal range of coiling,
either hypo- or hypercoiled were associated with signicantly
greater incidence of moderate or severe variable fetal heart rate
decelerations [1].
The signicance of umbilical cord hypercoiling (>0.3 coils/cm or
>3 coils/10 cm) has continued to be examined by several authors,
and a hypercoiled umbilical cord has been found to be associated
with several adverse pregnancy outcomes including cocaine usage
and preterm delivery [4], fetal demise, fetal intolerance to labor [3],
oligohydramnios, meconium and fetal distress [2]. However, these
associations are not universally true of all hypercoiled umbilical
cords, and further examination of which particular patterns of
hypercoiling are more likely to be associated with immediate
neonatal adverse outcomes, such as stillbirth, has not been per-
formed. Our study is the rst to dene four distinct gross patterns
of umbilical cord hypercoiling in clinical placental specimens and to
show that the two patterns with the most indentation between the
coils, the segmented and linked patterns, are associated with his-
tologic evidence of chronic fetal vascular obstruction/FTV in the
placenta and stillbirth. The major implication of this nding is that
the specic coiling pattern seen in the umbilical cord may predict
the degree and/or severity of fetal blood ow restriction.
Experimental models of umbilical blood ow have been
employed to study the effects of umbilical cord coiling on blood
ow. Using a model of standardized encirclement force on the
umbilical cord, Georgiou et al. demonstrated a signicant inverse
relationship between umbilical cord coiling and minimum weight
required to occlude venous perfusion [10]. This could be inter-
preted to imply that the hypercoiled umbilical cord is associated
with decreased pressure needed to occlude the umbilical vein, and
thus could place the fetus at greater risk for a fatal cord accident. In
addition, using a computational model to study the effects of um-
bilical cord coiling on arterial blood ow, Kaplan et al. showed that
the number of coils did not have a signicant effect on wall shear
stresses, but that wider spreading of the coils reduced wall shear
stresses [11]. This is consistent with our observations that the un-
dulating pattern, with its wider spreading of coils, had less
thrombosis than the linked and segmented patterns of coiling.
Signicant, chronic umbilical cord compression or elevated wall
shear stresses can produce stasis of fetal blood ow, thrombosis in
fetal vessels, multifocal avascular villi (FTV), and ultimately fetal

Table 4
Correlation of coil twist direction and outcomes.

Coiling Frequency Abnormal cord Fetal thrombi Avascular villi Villous stromal-vascular Fetal thrombotic Stillbirth
pattern N (%) insertion N (%) N (%) N (%) karyorrhexis N (%) vasculopathy N (%) N (%)

Right twist 61 (19) 9 (15) 22 (36) 18 (30) 6 (10) 9 (15) 7 (12)

Left twist 257 (81) 44 (17) 51 (20) 45 (18) 8 (3) 16 (6) 11 (4)
P-value NS 0.007 0.035 0.021 0.026 0.029
 L.M. Ernst et al. / Placenta 34 (2013) 583e588
Fig. 3. Graph illustrating the spectrum of gross coiling patterns in relation to coil direction.
death. Our data support the nding that beyond the number of
coils, the gross pattern of coiling may affect the degree of fetal
blood ow restriction. Specically, our most important observation
is that the segmented and linked patterns of umbilical cord
hypercoiling are more highly associated with placental histologic
features of chronic umbilical cord obstruction and stillbirth than
the patterns with less restriction in diameter between the coils.
In general, left umbilical cord twisting is more frequent than
right umbilical cord twisting with a reported ratio of 5e7:1 [12,13],
but in our study of exclusively hypercoiled umbilical cords the ratio
is approximately 4:1, suggesting hypercoiled cords may represent
an enriched population of the right coiling pattern. Our results
show that in the setting of a hypercoiled cord, right umbilical cord
twisting is more frequently associated with histologic changes of
chronic fetal vascular obstruction and stillbirth than left umbilical
cord coiling. Baergen has also shown that long umbilical cords
frequently have right twisting [14]. Right umbilical cord twisting
may be less common in the general population because the right
umbilical artery is typically larger than the left umbilical artery, and
this discrepancy creates rotational torque to the left. Therefore,
right umbilical cord twisting may indicate a developmental ab-
normality [14]. Our results demonstrate that for the coiling patterns
with signicant indentation, and perhaps the greatest coiling tor-
que, this developmental abnormality is associated with the highest
degrees of fetal vascular obstruction and stillbirth. This is not sur-
prising, as severe fetal vascular pathology as seen in FTV has been
associated with several adverse outcomes including stillbirth [15e
19]. Our study further strengthens the link between gross umbilical
cord abnormalities and stillbirth, especially when umbilical cord
hypercoiling is associated with signicant restriction of umbilical
cord diameter between the coils.
The factors that determine umbilical cord coiling are largely
unknown, but several theories exist including fetal movement,
torsion by the embryo, differential vascular growth rates, fetal he-
modynamic forces, structure of the muscle of the umbilical vessels,
and genetic factors [7,13,14]. It is generally believed that umbilical
cord coiling is established early in gestation. Twisting of the cord
can be appreciated as early as the 9th week of gestation [4,13], and
increases only insignicantly in the third trimester [13]. Studies
demonstrating the utility of ultrasound in prenatal diagnosis of
umbilical cord coiling are conicting. For instance, Pedranic and
colleagues demonstrated a strong correlation between second
587
trimester UCI as determined by one observer and postnatal UCI,
with reliable intra-observer reproducibility [20]. Similarly, another
study that determined antenatal UCI within 24 h of delivery also
found that ultrasound UCI correlates well with UCI after birth [21].
In contrast, another study failed to show a good correlation,
although antenatal UCI measurement in this study was performed
by three separate investigators with no analysis of inter- or intra-
observer variability [22]. In addition, some studies have linked
umbilical cord coiling with umbilical arterial ow characteris-
tics [23], while others suggest that the coiling primarily correlates
with umbilical venous Doppler indices [21]. These discrepant re-
sults may be related to the methodology by which antenatal um-
bilical cord coiling is assessed, and in total, suggest that not only is a
standardized ultrasonographic technique for coiling required, but
that establishment of uniform technique in assessing gross patterns
of coiling is also necessary.
In conclusion, this is the rst study to dene four different
grossly recognizable patterns of umbilical cord hypercoiling in
clinical placental specimens and to correlate the segmented and
linked patterns (characterized by the greatest constriction of cord
diameter between the coils) with histologic evidence of chronic
fetal vascular obstruction and one of the poorest pregnancy out-
comes, stillbirth. Further studies to examine the histologic and
physical properties of the umbilical vessels in the segmented and
linked pattern of hypercoiling may shed more light on the under-
lying defect in this important developmental umbilical cord ab-
normality. Further investigation is also needed to determine if
these coiling patterns can be recognized antenatally to identify
fetuses at risk for adverse outcome.
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