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Umbilical Hypercoiling in 2nd- and 3rd-
Trimester Intrauterine Fetal Death
ANNEMIEK C. DUTMAN AND PETER G.J. NIKKELS
*
Department of Pathology, University Medical Center Utrecht, Utrecht, The Netherlands
Received October 8, 2013; accepted October 25, 2014; published online October 31, 2014.
ABSTRACT
Cases of unexplained intrauterine fetal death (IUFD) can
be reduced by full placental examination, with or without
autopsy. Determination of the umbilical coiling index
(UCI) is considered to be a part of full placental
examination. Umbilical hypercoiling (UCI above 0.30
coils/cm) is associated with IUFD. In a large retrospective
study, we found an incidence of 18% umbilical
hypercoiling in IUFD. We explored the association
between umbilical hypercoiling and 2nd- and 3rd-
trimester IUFD in 77 cases. There was a significant
negative correlation between the UCI and gestational age
of IUFD (P,0.001). More severe cases of hypercoiling
were observed in the categories of IUFD at a younger age
and with a longer duration. Signs of fetal thrombosis were
significantly more present in IUFDs with umbilical
hypercoiling. An umbilical cord stricture and hypercoil-
ing seem to be significantly more common in IUFD. The
severity of hypercoiling was of no influence on the
presence or absence of an umbilical cord stricture.
Furthermore, there was no significant difference in signs
of cardiac failure between the groups of IUFD with and
without umbilical hypercoiling. Our findings may be
explained by the theory that hypercoiling leads to a
disturbed fetal-placental circulation. Therefore, determi-
nation of the UCI should be part of the routine placental
examination of cases of IUFD.
Key words: fetal death, flow, hypercoiling, placenta,
umbilical coiling index, umbilical cord
INTRODUCTION
By examination of the placenta, separately or in
combination with postmortem examination of the fetus,
many cases of fetal death can be explained. However,
up to 31% of cases of intrauterine fetal death (IUFD)
remain unexplained, in spite of full examination of the
placenta and fetus [1,2]. Horn and colleagues [3]
documented 15.2% unexplained IUFD because of an
unavailable placenta for autopsy. Other reasons were
insufficient clinical data or severe maceration. Full
placental investigations reduce the proportion of unex-
plained stillbirths, compared to those without placental
examination [4].
Umbilical cord abnormalities are numerous, ranging
from false knots, which have no clinical significance, to
abnormalities that may lead to fetal death [5]. Abnormal
coiling—especially hypercoiling—of the umbilical cord
is associated with IUFD [6,7]. Coiling of the umbilical
cord arteries is an intrinsic anatomical feature of the
umbilical cord and unlike twists or torsion cannot be
undone [8]. Hypercoiling was noted earlier in a case
report [9] that documented 2 cases of IUFD (stillborn at
35 and 40 weeks of gestation) caused by an extremely
large number of coils of the umbilical cord as the only
abnormal pathological finding. Three cases of hypercoil-
ing were found in a study of early IUFD [10]. De Laat and
colleagues [11] confirmed the association between fetal
death and umbilical hypercoiling, next to a placental
maturation defect.
Little has been written on a possible correlation of a
long umbilical cord and preterm IUFD. An excessively
long umbilical cord (ELUC), defined as an umbilical cord
of a full-term pregnancy with a length of more than 70 cm,
showed a non–statistically significant association with
fetal death [12]. In a few studies, umbilical cord stricture
at the fetal side has been described as a cause of IUFD,
with or without hypercoiling [6,10,13,14]. In conclusion,
little is known about umbilical cord abnormalities and
IUFD.
The aim of our study was to explore whether there is
an association between umbilical hypercoiling and 2nd-
and 3rd-trimester IUFD. We hypothesized that severity of
umbilical hypercoiling may be negatively correlated to
the gestational age of the stillborns. Our hypothesis was
based on the paper of Kaplan and colleagues [15]. They
developed a computational model for blood flow in the
coiled umbilical artery. In this paper it was demonstrated
that increased coiling is associated with a higher driving
pressure to perfuse the umbilical cord vessels and pla-
centa, with consequently an increased fetal cardiac work-
load. We compared signs of cardiac failure (hypertrophy
*Corresponding author, e-mail: p.g.j.nikkels@umcutrecht.nl
Pediatric and Developmental Pathology 18, 10–16, 2015
DOI: 10.2350/13-10-1390-OA.1
ª2015 Society for Pediatric Pathology
and ventricular dilatation) and signs of fetal thrombosis
between groups of unexplained IUFD with or without
umbilical hypercoiling. In cases of hypercoiling, the
distribution of the umbilical coiling index (UCI) was
studied between groups with presence or absence of an
umbilical cord stricture and between groups with a long
or no long umbilical cord. Furthermore, we studied the
presence of an umbilical cord stricture between groups of
IUFDs with or without umbilical hypercoiling.
METHODS
This retrospective study was conducted from January 1,
2000, to July 1, 2013, at the Department of Pathology of
the University Medical Center Utrecht, a tertiary referral
center in the Netherlands. All placentas of cases of IUFD
were examined, with and without postmortem examina-
tion of the fetus. Cases of postpartum-deceased neonates
and terminations of pregnancy were excluded. The UCI
was part of the routine examination of the placentas and
was studied in fresh, unfixed placentas. The UCI was
calculated as the number of coils divided by the length of
the cord [16]. Using references values from van Dijk and
colleagues [17], we defined hypocoiling as less than 0.07
coils/cm and hypercoiling as more than 0.30 coils/cm.
Cases of IUFD of the 2nd and 3rd trimester with
umbilical hypercoiling in the report (n577) were
extracted from a total of 417 2nd- and 3rd-trimester
IUFDs. The IUFDs were classified according to the Tulip
classification [18]. The gestational age (in weeks) at the
time of delivery of the stillborns was based on the last
menstrual period or 1st-trimester ultrasound. The duration
of the IUFD was determined by the severity of maceration
at postmortem examination of the fetus and placenta,
based on the data from Genest and colleagues [19–21].
The cases with umbilical hypercoiling were divided into 4
categories of IUFD and defined as (1) up to 1 day, (2) 2–
7 days, (3) 8–14 days, and (4) more than 14 days. The
following data were retrieved from the pathology
application forms: maternal age at delivery, parity,
placental abruption, preterm rupture of membranes, and
presence of diabetes or preeclampsia. Data collected
about the fetus and placenta included the gender,
maturation of the fetus, weight of the fetus, weight of
the heart, cardiac ventricular dilatation, chromosomal
abnormalities, congenital malformations, twinship, length
of the umbilical cord, UCI, umbilical cord stricture at the
fetal side, single umbilical artery, fetal thrombosis (FTV),
and velamentous cord insertion. Signs of FTV were
defined as ‘‘mild’’ (uniformly avascular villi or villous
stromal-vascular karyorrhexis [more than 2 foci/5–15
affected villi per slide] 6fetal vessel lesions) or
‘‘severe’’ (uniformly avascular villi or villous stromal-
vascular karyorrhexis [more than 2 foci/average of 15 or
more affected villi per slide] 6fetal vessel lesions) [22].
Fetal hearts were defined as hypertrophic when the
weight of the heart was above the mean plus 1 standard
deviation (SD) [23]. The umbilical cord strictures were
not documented in all cases and therefore postmortem
photos were reviewed (n5319). Ninety-eight postmor-
tem photos were not available because the cases were
revisions from other hospitals (n517) or former cases
from our own institute without photo documentation (n5
81). Excessively long umbilical cords were defined as
those umbilical cords measuring approximately 2 SD
above the mean for full-term pregnancies [12]. Umbilical
cords from 20 to 42 weeks of gestational age with a length
measuring 2 SD above the mean and lengths of
gestational ages 14–20 weeks above the 95th percentile
were defined as long cords [24,25]. All other umbilical
cord lengths were defined as no long cord. Short cords
were defined in a similar manner as long cords, with
lengths measuring 2 SD below the mean and below the
5th percentile [24,25]. Cases without internal postmortem
examination of the fetus resulted in an incomplete data
collection.
The data were analyzed using IBM SPSS Statistics
(IBM, Armonk, NY, USA), version 20. Pearson correla-
tion was used to determine the associations between
gestational age and the UCI and between gestational age
and the length of the umbilical cord. We used the chi-
square, Mann-Whitney, and Kruskal-Wallis tests for
statistical comparisons. Pvalues of 0.05 were consid-
ered to indicate statistically significant differences.
RESULTS
In this study 77 cases of IUFD with umbilical hypercoil-
ing (18%) were extracted from a total of 417 cases of
IUFD. The 77 cases of IUFD with hypercoiling were all
classified as unknown according to the Tulip classifica-
tion. The causes of IUFD of all cases (n5417) are shown
in Table 1. In cases of IUFD without umbilical hypercoil-
ing, the mean gestational age (SD) was 24.7 (8.4) weeks
and the mean maternal age (SD) was 31.6 (5.5) years.
Baseline and outcome characteristics of the 77 cases of
IUFD with umbilical hypercoiling are summarized in
Table 2. The mean gestational age (SD) was 22.6 (6.7)
weeks and the mean UCI (SD) was 0.73 (0.43) coils/cm.
Table 1. Causes of intrauterine fetal death according
to the Tulip classification
Frequency %
Congenital anomaly (1) 63 15.1
Placenta (2)
Placental bed pathology (2.1) 78 18.7
Placental pathology (2.2) 47 11.3
Umbilical cord complication (2.3) 9 2.2
Not otherwise specified (2.4) 31 7.4
Infection (4) 36 8.6
Other (5)
Trauma (5.3) 3 0.7
Unknown (6) 150 36.0
Total 417 100
UMBILICAL HYPERCOILING IN FETAL DEATH 11
There was a negative, strong, and significant correlation
between the UCI and gestational age at delivery in weeks
(r520.515, r
2
526.5%, P,0.001) (Fig. 1). A
determination coefficient r
2
between 25% and 50% means
a strong association according to Pearson correlation. A
similar correlation was found when we corrected the
gestational age at time of delivery (in weeks) with the
duration of the IUFD. These are estimated gestational
ages when the IUFD has occurred (data not shown).
Furthermore, we did not find a UCI above 1.00 coils/cm
at a gestational age of 23 weeks or more. Four categories
of IUFD were defined: (1) up to 1 day, (2) 2–7 days, (3)
8–14 days, and (4) more than 14 days. More severe cases
of umbilical hypercoiling were seen in the categories of
IUFD with a longer duration (P50.002) (Fig. 2). The
umbilical cord stricture was studied from postmortem
photos in 319 cases. From these 319 cases, 32 cases were
not assessable, mainly because of an umbilical cord
removed very close to the fetus. The other 98 cases
without photo documentation were revisions from other
hospitals (n517) and former cases from our own
institute (n581). An umbilical cord stricture was present
in 24 of the 235 assessable cases without hypercoiling. In
the assessable cases with hypercoiling (n552), 18 cases
showed presence of an umbilical cord stricture (Fig. 3).
The presence of an umbilical cord stricture in IUFDs with
hypercoiling was significantly more common as com-
pared with IUFDs without hypercoiling (P,0.001). In
the cases with hypercoiling, no significant difference of
the UCI was found between the presence and absence of
an umbilical cord stricture (P50.507). As would be
expected there was a strong and significant correlation
between the length of the umbilical cord and gestational
age at delivery in weeks (r50.594, r
2
535.3%, P,
0.001; Fig. 4). The mean length of the umbilical cord was
in 2nd trimester 34.1 cm (n560) and in 3rd trimester
55.0 cm (n516). There was no significant difference in
length distribution across the different categories of IUFD
(P50.343). The distribution of the UCI was the same
across groups with long or no long cords (P50.217).
Sixteen short umbilical cords were present in the group
with no long cords. There were only 4 cases of full-term
Figure 2. Box plots for the umbilical coiling index (UCI) in
categories of intrauterine fetal death. IUFD indicates
intrauterine fetal death.
Table 2. Baseline and outcome characteristics of
intrauterine fetal death with umbilical hypercoiling
Characteristics
Mean ±SD
or n(%)
Maternal age (years), n577 33.5 64.7
Parity
Nulliparous 12 (15.6)
Parous 48 (62.3)
Not documented 17 (22.1)
Preeclampsia 0
Diabetes 3 (3.9)
Preterm rupture of membranes 1 (1.3)
Placental abruption 2 (2.6)
Post mortem examination of the fetus 64 (83.1)
Gender of the infant
Male 37 (48.1)
Female 27 (35.1)
Not documented 13 (16.9)
Maturation of the fetus (weeks), n564 19.8 67.1
Weight of the fetus (g), n560 446.3 6721.1
Chromosomal abnormalities 4 (5.2)
Not documented 10 (13.0)
Congenital malformations 15 (19.5)
Not documented 13 (16.9)
Twinship 5 (6.5)
Single umbilical artery 1 (1.3)
Fetal thrombosis 14 (18.2)
Velamentous cord insertion 2 (2.6)
Length of the umbilical cord (cm), n576 34.9 618.8
Figure 1. Scatterplot of the umbilical coiling index (UCI)
against gestational age in weeks of cases of 2nd- and 3rd-
trimester intrauterine fetal death with hypercoiling. Cases
with a UCI more than 1.00 coils/cm are present only under
the gestational age of 23 weeks.
12 A.C. DUTMAN AND P.G.J. NIKKELS
Figure 3. Cases of fetal death with hypercoiling and presence or absence of an umbilical cord stricture. A. Fetal death at
22 weeks with a striking example of hypercoiling (umbilical coiling index 51.80 coils/cm) and without an umbilical cord
stricture. B. Fetal death at 24 weeks with an umbilical cord stricture. C. Fetal death at 27 weeks without an umbilical cord
stricture. D. Fetal death at 40 weeks with an umbilical cord stricture.
UMBILICAL HYPERCOILING IN FETAL DEATH 13
pregnancies (37 weeks) in our cases of IUFD with
hypercoiling, and no ELUCs were present in this small
group, according to the definition of Baergen and
colleagues [12]. There was no significant difference in
presence of cardiac hypertrophy or ventricular dilatation
between the groups of IUFD with and without umbilical
hypercoiling (P 50.573; P50.581; Table 3). There
were signs of FTV in 18.2% of IUFDs with hypercoil-
ing (Table 2). Cases of IUFD without hypercoiling
showed FTV in 2.9% (n510). Fetal thrombosis (mild
plus severe) was strongly significantly more common
in IUFDs with umbilical hypercoiling (P ,0.001)
(Table 4).
DISCUSSION
In this study the incidence of umbilical hypercoiling in
IUFD was 18%. We have found a negative linear
correlation between the UCI and IUFD. Higher UCIs
were found at younger gestational ages (Fig. 1). Our
study confirms the association between fetal death and
umbilical hypercoiling, as was found in previous studies
[6,7,11,13]. Furthermore, a UCI of more than 1.00 coils/
cm was only observed in cases less than 23 weeks of
gestational age. Higher UCIs were associated with IUFDs
at a younger gestational age with more severe maceration;
a possible explanation might be that early IUFDs are
likely to be detected later. First, in younger pregnancies
mothers experience no fetal movements yet. Secondly, in
the Netherlands no structural ultrasound is provided until
a gestational age of 20–22 weeks. Therefore, early IUFD
can be present longer before detection by ultrasound.
Coiling is an intrinsic feature of the umbilical cord,
and coils cannot be undone like twists or torsion [8].
Little is known about the effect of abnormal coiling on the
umbilical cord blood flow and the mode of fetal death,
although a cardiovascular disturbance seems most likely.
It could be due to acute or chronic cardiac failure or a
disturbed fetal-placental blood flow. In a study by
Predanic and colleagues [26] it was shown that increased
coiling was associated with increased venous flow and
decreased arterial resistance. In another study it was
demonstrated that overcoiled cords were associated with a
reduced forward venous flow [27]. The arteries coil
around the vein and hypercoiling may make the arteries
compress the vein, leading to a hampered venous flow
from the placenta to the fetus, as was discussed in studies
by Nakai and colleagues [28,29]. It was suggested that
coiling may be beneficial for venous and arterial flow to a
certain point but further increased coiling may be
detrimental for blood flow [30]. Kaplan and colleagues
[15] developed a computational model of steady blood
flow through a coiled structure resembling an umbilical
artery. They showed that the driving pressure for a given
blood flow rate is increasing as the number of coils in the
cord structure increases. The driving pressure decreases
when spacing between the coils increases. The total
number of coils has no influence on the maximal values
of wall shear stress (WSS). However, when the distance
between the coils is smaller, the maximal WSS is
significantly larger. Kaplan and colleagues simulated a
case with hypercoiling (UCI 50.66 coils/cm), which may
represent cases that may lead to IUFD. This simulation
showed a higher inlet pressure to drive the arterial blood
flow and significantly larger maximal WSS, which may
have an adverse effect on the development of the fetal
cardiovascular system. And furthermore, an increased
WSS may damage endothelial cells, which may lead to
thrombus formation [31]. In comparison with our study,
FTV was associated with hypercoiling in cases of IUFD
[6,7,13]. We found signs of FTV in 18.2% of the cases
with umbilical hypercoiling and in 2.9% in the non-
overcoiled cords (Tables 2,4), a comparable percentage
(16 of 76 [21%]) to that found by de Laat and colleagues
[7]. The presence of FTV in these cases was usually not
Figure 4. Scatterplot of the length of the umbilical cord
against gestational age in weeks of cases of 2nd- and 3rd-
trimester intrauterine fetal death with hypercoiling.
Table 3. Signs of cardiac failure in cases of intrauterine fetal death with or without umbilical hypercoiling
Without hypercoiling With hypercoiling Total
Cardiac hypertrophy No 219 44 263
Yes (%) 9 (3.9) 1 (2.2) 10
Total 228 45 273
Ventricular dilatation No 211 45 256
Yes (%) 20 (8.7) 3 (6.3) 23
Total 231 48 279
14 A.C. DUTMAN AND P.G.J. NIKKELS
comprehensive enough to explain the IUFD. Even in the
severe cases, loss of placental villi was not above 30% of
the total parenchyma. We hypothesized that umbilical
hypercoiling may cause an increased fetal cardiac
workload and that it reduces both venous and arterial
blood flow. Kaplan and colleagues showed that a higher
driving pressure for the umbilical arterial blood flow is
needed for the same placental perfusion as the coiling
index increases. This may lead to a higher fetal cardiac
workload and may support one of our findings that higher
umbilical hypercoiling is associated with earlier IUFD
and this may be due to earlier fetal cardiac overload.
However, signs of cardiac failure (i.e., hypertrophy or
dilatation) were not significantly more present in cases of
IUFD with umbilical hypercoiling. However, it is not
known if the very young fetal heart responds in a similar
manner as an adult heart to an increase in workload. The
fetal myocardial cells are not the same as adult
myocardial cells; the presence and distribution of cell
junctions changes during development [32,33]. Myocar-
dial passive stiffness decreases with development of the
fetus. In other terms, myocardial compliance increases
with development [34]. Maybe the fetal heart responds in
a different way to cardiac overload. The association
between umbilical hypercoiling and thrombosis may be
explained by the larger values of WSS, possible damage
of the endothelium, and stasis of the blood flow.
Furthermore, a reduction in the venous blood flow due
to umbilical hypercoiling may result in hypoxemia in the
fetus. In conclusion, it is suggested that umbilical
hypercoiling is associated with a disturbance in the
fetal-placental circulation and may cause IUFD.
Umbilical cord stricture and hypercoiling as a cause
of IUFD has been described in a few studies [6,13].
Several case reports have been published on fetal death
resulting from umbilical cord stricture, mainly caused by
loss of Wharton jelly and replacement by fibrosis
[10,14,35]. Stricture of the umbilical cord may be
associated with torsion [10,35]. In one case report of
IUFD it was suggested that hypercoiling of the umbilical
cord led to torsion without a stricture or abnormality of
the Wharton jelly [9]. In fetal death, umbilical hypercoil-
ing was reported with or without a stricture [6,10,13].
Peng and colleagues [13] found 19% (26 of 139) of fetal
death cases to have umbilical cord stricture, hypercoiling,
or a combination of both. Of those cases, 54% (14 of 26)
had an umbilical cord stricture with hypercoiling.
According to a similar calculation, our cases (in total
287 assessable cases: 52 with hypercoiling and 235
without hypercoiling) showed an umbilical cord stricture
with hypercoiling in 24% (18 of 76; stricture with
hypercoiling n518, only stricture n524, only
hypercoiling n534). Furthermore, Peng and colleagues
reported an incidence of 14% umbilical cord stricture
with or without hypercoiling in cases of fetal death. We
showed a similar incidence of 15% (42 of 287) umbilical
cord stricture in our assessable cases with or without
hypercoiling. According to our study, an umbilical cord
stricture and hypercoiling seem to be significantly more
common in fetal death. The IUFDs with hypercoiling
showed an umbilical cord stricture in 35% of cases [18 of
52]. Machin and colleagues [6] reported an incidence of
13% of fetal death associated with umbilical cord stricture
in the presence of hypercoiling. We found that severity of
hypercoiling was of no influence on the presence or
absence of an umbilical cord stricture.
As expected, we found a highly significant correlation
between the length of the umbilical cord and gestational age
at the time of delivery in weeks. A variety of authors found
cord lengths to grow linearly. As was suggested by
Leonardo da Vinci, the umbilical cord at any gestational
age has usually the same length as the fetus [5]. In our study,
no definite conclusion could be made about the association
between UCI and cord length. The umbilical cord was not
always submitted completely to pathology and therefore
there is uncertainty about the total length of the umbilical
cord. Maybe ‘‘short cords’’ were not short and perhaps there
were ELUCs present in our study group. In cases of IUFD
with hypercoiling, there were 46 cases with an umbilical
cord defined as no long cord (including 16 short cords) and
30 cases with an umbilical cord defined as a long cord.
There was no significant difference in the distribution of the
UCI between these 2 groups. Also, there were no significant
differences in length of the umbilical cord between the 4
categories of IUFD. Excessively long umbilical cords have
an association with fetal death [12]. We found no ELUCs in
our small group of full-term IUFDs with umbilical
hypercoiling. Excessively long umbilical cords were defined
as those umbilical cords measuring approximately 2 SD
above the mean for full-term pregnancies.
In summary, we found a negative correlation between
UCI and gestational age. A higher UCI was associated
with an IUFD at younger age. We hypothesized that
umbilical hypercoiling leads to a reduction of umbilical
cord blood flow and increased fetal cardiac workload.
Consequently, umbilical hypercoiling may be associated
with a disturbance of the fetal-placental circulation and
this may be a possible explanation for IUFD. If
hypercoiling is accepted as cause of death in the Tulip
classification the ‘‘unknown’’ group decreases from 36%
to 17.5% and the ‘‘umbilical cord complication’’ group
increases from 2.2% to 20.6%. Therefore we recommend
Table 4. Fetal thrombosis (FTV) in cases of
intrauterine fetal death with or without umbilical
hypercoiling
Without
hypercoiling
With
hypercoiling Total
FTV
Mild 9 7 16
Severe 1 7 8
Total (%) 10 (2.9) 14 (18.2) 24
No FTV 330 63 393
Total 340 77 417
UMBILICAL HYPERCOILING IN FETAL DEATH 15
that determination of the UCI should be part of the routine
examination of the placentas of cases of IUFD.
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