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RESEARCH ARTICLE
Extreme umbilical cord lengths, cord knot and
entanglement: Risk factors and risk of adverse
outcomes, a population-based study
Lorentz Erland Linde
1☯
, Svein Rasmussen
1,2☯
, Jo
¨rg Kessler
1
, Cathrine Ebbing
1
*
1Department of Obstetrics and Gynecology, Haukeland University Hospital, Bergen, Norway, 2Department
of Clinical Science, University of Bergen, Bergen, Norway
☯These authors contributed equally to this work.
*Cathrine.ebbing@helse-bergen.no
Abstract
Objectives
To determine risk factors for short and long umbilical cord, entanglement and knot. Explore
their associated risks of adverse maternal and perinatal outcome, including risk of recur-
rence in a subsequent pregnancy. To provide population based gestational age and sex and
parity specific reference ranges for cord length.
Design
Population based registry study.
Setting
Medical Birth Registry of Norway 1999–2013.
Population
All singleton births (gestational age>22weeks<45 weeks) (n = 856 300).
Methods
Descriptive statistics and odds ratios of risk factors for extreme cord length and adverse out-
comes based on logistic regression adjusted for confounders.
Main outcome measures
Short or long cord (<10
th
or >90
th
percentile), cord knot and entanglement, adverse preg-
nancy outcomes including perinatal and intrauterine death.
Results
Increasing parity, maternal height and body mass index, and diabetes were associated with
increased risk of a long cord. Large placental and birth weight, and fetal male sex were fac-
tors for a long cord, which again was associated with a doubled risk of intrauterine and
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 1 / 20
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OPEN ACCESS
Citation: Linde LE, Rasmussen S, Kessler J,
Ebbing C (2018) Extreme umbilical cord lengths,
cord knot and entanglement: Risk factors and risk
of adverse outcomes, a population-based study.
PLoS ONE 13(3): e0194814. https://doi.org/
10.1371/journal.pone.0194814
Editor: Sari Helena Ra¨isa¨nen, Helsingin Yliopisto,
FINLAND
Received: January 14, 2018
Accepted: March 9, 2018
Published: March 27, 2018
Copyright: ©2018 Linde et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: The data underlying
this study belong to the Medical Birth Registry of
Norway and the Norwegian Institute of Public
Health. Interested researchers must apply for
approval from the Regional Committee for Medical
Research Ethics using the following link: https://
helseforskning.etikkom.no/page/forside?
_ikbLanguageCode=us. After receiving approval,
data access can be requested here: https://www.
fhi.no/en/more/research–access-to-data/. The
authors did not have special access privileges.
perinatal death, and increased risk of adverse neonatal outcome. Anomalous cord insertion,
female sex, and a small placenta were associated with a short cord, which was associated
with increased risk of fetal malformations, placental complications, caesarean delivery, non-
cephalic presentation, perinatal and intrauterine death. At term, cord knot was associated
with a quadrupled risk of perinatal death. The combination of a cord knot and entanglement
had a more than additive effect to the association to perinatal death. There was a more than
doubled risk of recurrence of a long or short cord, knot and entanglement in a subsequent
pregnancy of the same woman.
Conclusion
Cord length is influenced both by maternal and fetal factors, and there is increased risk of
recurrence. Extreme cord length, entanglement and cord knot are associated with increased
risk of adverse outcomes including perinatal death. We provide population based reference
ranges for umbilical cord length.
Introduction
A normal umbilical cord is of obvious importance for a normal fetal development. It has been
estimated that about 10% of intrauterine deaths in the USA may be attributable to umbilical
cord complications, and these complications are associated with clinically significant placental
pathology [1]. Lately there has been an increased awareness of placental and cord abnormali-
ties and their associated risk of adverse outcome for the mother and the newborn [2–4]. In
case studies excessive long cords have been associated with cord entanglements, emergency
deliveries and fetal thrombotic vasculopathy in the placenta, fetal death and increased risk of
neurological complications [5,6]. A short cord has been associated with increased risk of fetal
malformations, fetal distress and possibly placental abruption [7–9]. Although anomalous
cord length is associated with adverse outcome [5,9], normal cord length is poorly defined in
many studies, and population based studies and reference ranges are lacking. Also studies on
risk factors and outcome of cord entanglement and knots are scarce, and population studies
are yet to be performed. Therefore, the aims of the present study was 1: to determine risk fac-
tors for long and short umbilical cord, cord knots and entanglements, 2: to study the associated
risks of adverse outcome of pregnancies with abnormal cord length, cord knot and entangle-
ment in the Norwegian population, 3: to study the risk of recurrence of abnormal cord length,
cord knot and entanglement in a subsequent pregnancy of the same woman, and 4: to provide
population based gestational age, sex and parity specific charts for umbilical cord length.
Methods
We performed a population-based register study of all singleton births in Norway with gesta-
tional age >21 weeks and <45 weeks during the period 1999–2013 (n= 856 300) using data
from the Medical Birth Register of Norway (MBRN). The attending midwife or physician per-
formed the examinations of the neonate, placenta, membranes and cord, and entered the
requested information into a registration form shortly after delivery. Information regarding
the umbilical cord has been specified since 1999 using tick boxes named: “normal, marginal,
velamentous, vessel anomalies, entanglement (around the neck or other body parts) and cord
knot”. The length of the umbilical cord was measured in centimetres. Placenta with cord and
Umbilical cord length, knots and entanglement and associated risks
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 2 / 20
Funding: Cathrine Ebbing was supported
financially by the Western Norway Regional Health
Authority (Post doctoral grant no 911581). The
funders had no role in study design, data collection
and analysis, decision to publish, or preparation of
the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
Abbreviations: aOR, adjusted Odds Ratio; ART,
Assisted reproductive technology; CI, Confidence
interval; MBRN, Medical birth registry of Norway;
OR, Odds Ratio.
membranes attached were weighed in grams. To construct empirical percentiles of cord length
for the population we included cord lengths from 1 to 290 cm (n= 797 096). The attending
midwife or physician also clinically estimated the amount of amniotic fluid (poly- or oligohy-
dramnios) and postpartum bleeding volume. Preterm pre labour rupture of the membranes
(PPROM) was defined as rupture of the membranes <37 weeks of gestation and >24 hours
before birth (yes/no). Gestational age was based on ultrasound dating in the first half of preg-
nancy when available (in 97.0% of the cases) or the mother’s last menstrual period. Preterm
birth was defined as birth before gestational week 37. Parity was defined as the number of pre-
vious deliveries. From 2006 maternal weight and height from the pregnancy file has been
included in the register. Body mass index was available for 37.2% of the pregnancies from 2006
(n= 174 337 of 468 321 possible).
Pregnancies conceived by assisted reproductive technology (ART) have been notified in the
register on voluntary basis from 1988 and compulsory basis since 2001 (n= 16 810). The diag-
nosis of abruption of the placenta and placenta previa was done by the clinician.
All neonates were examined by a physician who recorded any malformation at birth or at
the neonatal care unit. Severe malformations were defined by specific Q diagnoses in the Inter-
national Classification of Diseases (10
th
revision) system (see supporting information). Trans-
ferral to neonatal intensive care unit was registered.
Long (>90
th
gestational age, sex and parity (0 and 1+) specific empirical percentile) or
short (<10
th
empirical percentile) umbilical cord, umbilical cord knot or entanglement were
considered as outcome measures, as well as exposures. Placenta previa, abruption of the pla-
centa, preeclampsia, caesarean delivery, non-cephalic presentation, low Apgar score at 5 min-
utes, transferal to neonatal intensive care unit (NICU), malformations, birth weight- and
placental weight (empirical gestational, sex and parity specific percentiles), intrauterine and
perinatal death were considered as outcomes of these (cord) exposures.
Variables were included in the model according to their potential influence on the risk esti-
mates: parity, maternal and paternal age, neonatal sex, maternal BMI on the first prenatal visit,
maternal height, cigarette smoking at the beginning of pregnancy, maternal medical condi-
tions, anomalous cord insertion site on the placenta, conception by ART, small or large birth
weight and placental weight for gestational age based on empirical percentiles for the popula-
tion (birthweight <10
th
or >90
th
percentile, SGA and LGA), and low or high placental weight
(<10
th
or >90
th
percentile).
In order to study trend we categorized the study period in 5-year intervals (1999–2003,
2004–2008, and 2009–2013).
The Regional Committee for Medical and Health Research Ethics West (REK Vest)
approved the study protocol (approval no. REC West 2011/949) and waived the need for writ-
ten informed consent from the participants due to the data being analysed anonymously.
The data are reported in accordance with the STROBE guidelines (https://www.strobe-
statement.org).
Statistics
Odds ratios (ORs) and 95% confidence intervals (95%CI) for short and long umbilical cord,
cord knot and cord entanglement were estimated using Generalized Estimating Equations
analyses, with adjustments for possible confounding factors. We analysed the data with the
population stratified for gestational age at birth in weeks: 22–27, 28–36, 37–41, 42+, or in pre-
term (gestational age below 37 weeks) and term (37 weeks) births. In order to calculate ORs
for a repeat long or short cord length, cord knot and entanglement in the subsequent preg-
nancy, data from the first and second births of each woman were linked using national
Umbilical cord length, knots and entanglement and associated risks
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 3 / 20
identification numbers. Differences within the population were assessed by chi-squared test,
and p<0.05 was defined significant.
We calculated gestational age (weeks), parity (0, 1+) and sex specific empirical umbilical
cord length percentiles, but in analyses where fetal sex and/ or parity was included in the
model, gestational age specific percentiles (not specific for sex or parity) for cord length were
used. Below 29 weeks linear regression within strata of whole gestational age weeks, with
umbilical cord length as outcome and gender and parity (0, 1+) as independent variables,
revealed non-significant influence of sex and parity. Thus, the percentile tables were made sex
and parity specific for gestational age above 28 weeks only. The percentiles were smoothed by
Kernel smoothing (SigmaPlot version 13.0 (Systat Software, San Jose, CA)). Statistical Package
for the Social Sciences for Windows (version 24; SPSS, Chicago IL, USA) was used for the sta-
tistical analyses.
Results
Descriptive information of the study population according to properties of the cord (long or
short cord, cord knot and entanglement) is shown in Table 1.
Including maternal age and parity in the models did not significantly influence the associa-
tions (Tables 2and 3). Therefore only unadjusted ORs are given in the tables, and exceptions
are specified in the text. In the tables we report only significant findings.
What influences the length of the cord? There was an overall slight reduction in the risk
of a long cord during the study period (Table 2).
Maternal parity and BMI significantly increased the risk of developing a long cord in a
dose-response pattern (Table 2, Figs 1and 2).
Adjusting for maternal age did not change the effects of parity on the risk of a long cord,
which implies that parity and not maternal age influence the risk of a long cord. Paternal age
had no effect on the risk of an extreme cord length (data not shown). Girls had a lower risk of
developing a long cord, cord knots and entanglements than boys (Table 2). Sex differences in
cord length were significant after gestational week 28 (Fig 3, and S1 Table).
The effect of daily maternal smoking at the beginning of pregnancy was weak, but showed a
tendency to significantly reduce the risk of having a short cord and increase the risk of cord
knot and entanglement (Table 2). The risk of a long cord correlated positively to maternal
height and BMI at the beginning of pregnancy (Fig 2 and Table 2). Maternal diabetes, particu-
larly pre gestational diabetes mellitus, increased the risk of a long cord (Table 2). For pre
gestational diabetes this effect was not significantly altered by including maternal age, parity
and BMI in the model, while for gestational diabetes the effect was weaker when BMI was
included (adjusted OR (aOR) 1.29, 95%CI 1.17–1.42). Chronic hypertension before pregnancy
increased the risk of a long cord and reduced the risk of a short cord (Tables 1and 2). These
findings persisted after including maternal age and parity in the model, but the effects were no
longer significant when maternal BMI was included in the model (aOR 1.10, 95%CI 0.91–
1.33). Other maternal chronic conditions like asthma, rheumatoid arthritis and epilepsy did
not influence the risk of extreme cord length (data not shown). When analyzing the term and
preterm group separately, the associations with long or short cord, entanglements, and polyhy-
dramnios did not differ significantly (data not shown).
Conception by ART increased the risk of having a short, but not a long cord. However, the
effect almost was abolished when we adjusted for maternal age and parity (aOR 1.09, 95%CI
1.04–1.15).
Placental weight was significantly associated with cord length (Table 2). There was no effect
of including maternal age and parity, BMI or diabetes in the model. The relationship to birth
Umbilical cord length, knots and entanglement and associated risks
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Table 1. Maternal and pregnancy characteristics for pregnancies with long or short (>90th percentile or <10th percentile) umbilical cord, cord knot and entangle-
ment in the population of singleton births in Norway 1999–2013.
Long cord
(>90th
percentile)
Short cord
(<10th
percentile)
Cord knot Cord
entanglement
Characteristics total n % p-value n % p-value total n % p-value n % p-value
Maternal age (years) <20 17649 1341 7.60 <0.001 1637 9.28 <0.001 19168 181 0.94 <0.001 4164 21.72 <0.001
20–24 117980 9315 7.90 10977 9.30 126936 1238 0.98 27225 21.45
25–29 259300 21138 8.15 23517 9.07 278348 3158 1.13 58546 21.03
30–34 263366 23375 8.88 22285 8.46 282562 4050 1.43 57663 20.41
35–39 117707 11644 9.89 9107 7.74 126499 2180 1.72 25033 19.79
40 + 21029 2246 10.68 1679 7.98 22714 463 2.04 4320 19.02
Total 797031 69059 8.66 69202 8.68 856227 11270 1.32 176951 20.67
Parity 0 331108 23861 7.21 <0.001 35451 10.71 <0.001 354902 3038 0.86 <0.001 70258 19.80 <0.001
1 285462 24740 8.67 22598 7.92 306427 4210 1.37 64334 20.99
2 127640 14018 10.98 8115 6.36 137557 2680 1.95 30119 21.90
3 35832 4379 12.22 2063 5.76 38875 888 2.28 8303 21.36
4+ 17054 2064 12.10 984 5.77 18539 455 2.45 3943 21.27
Total 797096 69062 8.66 69211 8.68 856300 11271 1.32 176957 20.67
Fetal gender Boy 409410 40353 9.86 <0.001 30470 7.44 <0.001 439407 6907 1.57 <0.001 95408 21.71 <0.001
Girl 387654 28705 7.40 38732 9.99 416631 4364 1.05 81543 19.57
ART No 781178 69162 8.85 NS 67998 8.70 <0.001 839490 11097 1.32 0.0012 173798 20.70 <0.001
Yes 15886 1437 9.05 1563 9.84 16810 174 1.04 3159 18.79
BMI at the beginning of
pregnancy
<18.5 6949 407 5.86 <0.001 765 11.01 <0.001 7215 63 0.87 <0.001 1567 21.72 NS
18.5–24.9 102781 7966 7.75 9787 9.52 106680 1145 1.07 23810 22.32
25–29.9 37733 3880 10.28 2935 7.78 39196 520 1.33 8900 22.71
>30 20430 2619 12.82 1364 6.68 21246 328 1.54 4844 22.80
Total 167893 14872 8.86 14851 8.85 174337 2056 1.18 39121 22.44
Smoking No 562309 50364 8.96 <0.001 48772 8.67 <0.001 599743 7923 1.32 <0.001 129881 21.66 <0.001
Sometimes 12949 1235 9.54 1034 7.99 14004 181 1.29 2990 21.35
Daily 94397 8613 9.12 7764 8.22 103122 1578 1.53 24332 23.60
Not
answered
127409 10387 8.15 11991 9.41 139431 1589 1.14 19754 14.17
Maternal height (cm) <150 818 41 5.01 <0.001 55 6.72 <0.001 849 4 0.47 <0.001 159 18.73 <0.001
150–159 20432 1441 7.05 1140 5.58 21287 199 0.93 4598 21.60
160–169 96836 8050 8.31 4204 4.34 100653 1146 1.14 22771 22.62
170–179 60492 6044 9.99 2122 3.51 62756 825 1.31 14213 22.65
180+ 4492 562 12.51 141 3.14 4642 65 1.40 1061 22.86
Pre gestational diabetes
mellitus
No 791627 69807 8.82 <0.001 69287 8.75 <0.001 850402 11165 1.31 0.0011 176046 20.70 <0.001
yes 5437 792 14.57 274 5.04 5898 106 1.80 911 15.45
Gestational diabetes mellitus No 786161 69169 8.80 <0.001 68926 8.77 <0.001 844856 11063 1.31 <0.001 174636 20.67 NS
Yes 10903 1430 13.12 635 5.82 11444 208 1.82 2321 20.28
Pre-existing hypertension No 792749 70142 8.85 <0.001 33030 4.17 NS 851518 11180 1.31 <0.001 175953 20.66 NS
Yes 4315 457 10.59 167 3.87 4782 91 1.90 1004 21.00
Marginal cord insertion No 751043 66684 8.88 0.006 30873 4.11 <0.001 807183 10699 1.33 0.0024 164075 20.33 <0.001
Yes 46021 3915 8.51 2324 5.05 49117 572 1.16 12882 26.23
Velamentous cord insertion No 785000 69546 8.86 NS 32393 4.13 <0.001 843315 11149 1.32 <0.001 173729 20.60 <0.001
Yes 12064 1053 8.73 804 6.66 12985 122 0.94 3228 24.86
Placental weight<10th
percentile
No 718903 67385 9.37 <0.001 56142 7.81 <0.001 753533 10297 1.37 <0.001 157099 20.85 NS
Yes 71597 2561 3.58 12661 17.68 75705 683 0.90 15629 20.64
(Continued)
Umbilical cord length, knots and entanglement and associated risks
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weight was similar; birth weight >90
th
percentile was associated with a doubled risk of having
a long cord and reduced risk of having a short cord (Table 2). This was not changed by includ-
ing maternal diabetes in the model, however, including maternal BMI slightly attenuated the
association (aOR 1.66 95%CI 1.58–1.74). Birthweight <10
th
percentile was associated with
reduced risk of a long cord and a doubled risk of a short cord. We tested for co-linearity
between placental weight and cord length. Condition Index was low, suggesting that co-linear-
ity is not a concern.
We found a weak positive effect of both poly- and oligohydramnios on the risk of a long
cord. This effect persisted after adjustment for maternal age and parity, but when analyzed for
the term and preterm group separately, the effect was no longer significant in the preterm
group.
Risks associated with short or long cord. Tables 3and 4show the risks of adverse out-
comes associated with the presence of a short or long cord.
A short cord was associated with a 40% increased risk of the neonate having a major mal-
formation (Table 3, and in S1 List of malformation diagnoses). Fetuses and newborns with a
short cord carried increased risk of intrauterine and perinatal death also after including mal-
formations in the model (Table 3). In stratified analyses based on gestational age (term or pre-
term) this risk was confined to preterm births (aOR of intrauterine death 1.85, 95%CI 1.60–
2.14). Also, in preterm births a short cord was associated with an increased risk of a low 5 min-
utes Apgar score and transferal to intensive care unit (aOR 1.53, 95%CI 1.39–1.68, and 1.30,
95%CI 1.21–1.40, respectively).
Table 1. (Continued)
Long cord
(>90th
percentile)
Short cord
(<10th
percentile)
Cord knot Cord
entanglement
Characteristics total n % p-value n % p-value total n % p-value n % p-value
Placental weight>90th
percentile
No 714228 56521 7.91 <0.001 65594 9.18 <0.001 749473 9457 1.26 <0.001 156705 20.91 <0.001
Yes 76272 13425 17.60 3209 4.21 79765 1523 1.91 16023 20.09
Birth weight<10th percentile No 718181 65525 9.12 <0.001 57658 8.03 <0.001 771324 10113 1.31 NS 156844 20.33 <0.001
Yes 78449 5039 6.42 11842 15.10 84164 1151 1.37 20005 23.77
Birth weight>90th percentile No 718427 59503 8.28 <0.001 65772 9.16 <0.001 771107 10026 1.30 <0.001 162763 21.11 <0.001
Yes 78203 11061 14.14 3728 4.77 84381 1238 1.47 14086 16.69
Year of birth 1999–2003 246159 22503 9.14 <0.001 21019 8.54 <0.001 277673 4146 1.49 <0.001 63255 22.78 <0.001
2009–2013 265475 23231 8.75 22866 8.61 282466 3778 1.34 54541 19.31
2009–2013 285430 24865 8.71 25676 9.00 296161 3347 1.13 59161 19.98
Gestational age at birth (weeks) 22–27 2538 216 8.51 0.002 200 7.88 0.007 3320 41 1.23 <0.001 232 6.99 <0.001
28–36 39943 3663 9.17 3316 8.30 43459 652 1.50 6463 14.87
37–41 701315 61819 8.81 61416 8.76 751904 9900 1.32 157056 20.89
42+ 53268 4901 9.20 4629 8.69 57617 678 1.18 13206 22.92
Oligohydramnios No 774296 68320 8.82 <0.001 67267 8.69 <0.001 832171 10922 1.31 NS 171056 20.56 <0.001
Yes 22768 2279 10.01 2294 10.08 24129 349 1.45 5901 24.46
Polihydramnios No 788851 69714 8.84 <0.001 68880 8.73 NS 847568 11103 1.31 <0.001 175166 20.67 NS
Yes 8213 885 10.78 681 8.29 8732 168 1.92 1791 20.51
Malformations No 761515 67761 8.90 <0.001 65435 8.59 <0.001 818253 10756 1.31 <0.001 170217 20.80 <0.001
Yes 35549 2838 7.98 4126 11.61 38047 515 1.35 6740 17.71
ART; assisted reproductive technology, BMI: Body mass index,
https://doi.org/10.1371/journal.pone.0194814.t001
Umbilical cord length, knots and entanglement and associated risks
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Table 2. Odds ratios of a long cord (>90
th
percentile), short cord (<10
th
percentile), cord knot and entanglement according to maternal and pregnancy characteris-
tics in singletons in Norway 1999–2013.
Outcome Condition Long cord (>90
th
percentile)
Short cord(<10
th
percentile)
Cord knot Cord entanglement
Exposure OR 95%CI OR 95%CI OR 95%CI OR 95%CI
Parity 0 reference
1 1.22 1.20 1.24 0.72 0.80 0.73 1.61 1.54 1.69 1.07 1.06 1.09
2 1.59 1.55 1.62 0.57 0.55 0.58 2.30 2.18 2.43 1.13 1.12 1.15
3 1.79 1.73 1.86 0.51 0.49 0.53 2.71 2.51 2.92 1.09 1.07 1.13
4+ 1.77 1.69 1.86 0.51 0.48 0.55 2.91 2.64 3.22 1.09 1.06 1.13
Maternal age (years) <20 reference
20–24 NS NS NS NS
25–29 1.08 1.02 1.14 NS 1.20 1.04 1.40 0.96 0.93 0.99
30–34 1.18 1.12 1.25 0.90 0.86 0.95 1.53 1.31 1.77 0.92 0.89 0.96
35–39 1.34 1.26 1.42 0.82 0.78 0.87 1.84 1.58 2.14 0.89 0.86 0.92
40 + 1.45 1.35 1.56 0.85 0.79 0.91 2.18 1.84 2.59 0.85 0.81 0.89
Fetal gender Boy reference
Girl 0.73 0.72 0.74 1.38 1.36 1.40 0.66 0.64 0.69 0.88 0.87 0.89
ART Yes NS 1.14 1.09 1.21 0.78 0.67 0.91 0.89 0.85 0.92
BMI <18.5 reference
18.5–24.9 1.35 1.22 1.50 0.85 0.79 0.92 NS NS
25–29.9 1.84 1.66 2.05 0.68 0.63 0.74 1.53 1.17 1.98 1.06 1.00 1.13
>30 2.36 2.12 2.63 0.58 0.53 0.63 1.78 1.36 2.33 1.06 1.00 1.14
Smoking at the beginning of pregnancy no reference
sometimes 1.07 1.01 1.14 0.91 0.86 0.97 NS NS
daily 1.02 1.00 1.05 0.94 0.92 0.97 1.16 1.10 1.23 1.12 1.11 1.15
na 0.90 0.88 0.92 1.09 1.07 1.12 0.84 0.79 0.98 0.57 0.56 0.58
Maternal height (cm) 160–169 reference
<150 0.59 0.43 0.81 1.60 1.31 1.96 NS 0.79 0.66 0,94
150–159 0.82 0.78 0.87 1.25 1.19 1.31 0.82 0.70 0.95 0.94 0.91 0.98
170–179 1.24 1.20 1.28 0.87 0.82 0.79 1.16 1.06 1.27 NS
180+ 1.51 1.38 1.66 0.72 0.64 0.81 NS NS
Pre-gestational diabetes mellitus yes 1.76 1.63 1.90 0.55 0.49 0.62 1.38 1.13 1.67 0.70 0.65 0.75
Gestational diabetes mellitus Yes 1.56 1.48 1.66 0.64 0.59 0.70 1.40 1.21 1.60 NS
Pre-existing hypertension Yes 1.22 1.11 1.35 0.86 0.77 0.97 1.46 1.18 1.80 NS
Marginal cord insertion Yes 0.95 0.92 0.99 1.20 1.16 1.23 0.88 0.81 0.95 1.39 1.37 1.42
Velamentous cord insertion Yes NS 1.49 1.41 1.57 0.71 0.59 0.85 1.28 1.22 1.33
Placental weight<10th percentile Yes 0.36 0.34 0.37 2.54 2.48 2.59 0.66 0.61 0.71 NS
Placental weight>90th percentile Yes 2.49 2.44 2.54 0.43 0.42 0.45 1.52 1.44 1.61 0.95 0.93 0.97
Birth weight<10th percentile Yes 0.68 0.66 0.70 2.04 1.99 2.08 NS 1.22 1.20 1.24
Birth weight>90th percentile Yes 1.82 1.79 1.86 0.50 0.48 0.51 1.13 1.07 1.20 0.75 0.73 0.76
Year of birth 1999–2003 reference
2009–2013 0.95 0.93 0.97 NS 0.89 0.86 0.94 0.81 0.80 0.82
2009–2013 0.95 0.93 0.97 1.06 1.04 1.08 0.75 0.72 0.79 0.85 0.84 0.86
Gestational age at birth (weeks) 22–27 reference
28–36 NS NS NS 2.33 2.03 2.66
37–41 NS NS NS 3.51 3.07 4.02
(Continued)
Umbilical cord length, knots and entanglement and associated risks
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Table 2. (Continued)
Outcome Condition Long cord (>90
th
percentile)
Short cord(<10
th
percentile)
Cord knot Cord entanglement
Exposure OR 95%CI OR 95%CI OR 95%CI OR 95%CI
42+ NS NS NS 3.96 3.46 4.53
Oligohydramnios Yes 1.15 1.10 1.20 1.18 1.13 1.23 NS 1.25 1.21 1.29
Polyhydramnios Yes 1.25 1.16 1.34 NS 1.48 1.27 1.72 NS
ART; assisted reproductive technology, BMI: Body mass index, OR; Odds ratio, CI; Confidence Interval, NS; non-significant
https://doi.org/10.1371/journal.pone.0194814.t002
Table 3. Odds ratios of adverse pregnancy outcomes in pregnancies with a short umbilical cord (<10th sex and parity specific percentile) in the population of sin-
gleton births in Norway 1999–2013.
Exposure Outcome
Cord <10th percentile Condition Yes (n) Total (n) % OR 95% CI
No Malformation 31456 727885 4.32
Yes 4100 69211 5.92 1.40 1.35 1.44
No Placenta previa 2023 727885 0.28
Yes 275 69211 0.40 1.50 1.33 1.70
No Abruptio placentae 2479 727885 0.34
Yes 366 69211 0.53 1.54 1.38 1.72
No Post partum haemorrhage 117369 727503 16.08
Yes 11757 69211 16.99 1.03 1.00 1.05
No Manual removal of the placenta 9859 727885 1.35
Yes 1260 69211 1.82 1.30 1.23 1.38
No Preeclampsia 25250 727885 3.47
Yes 2253 69211 3.26 0.85 0.82 0.89
No PPROM
¥
6203 727885 0.85
Yes 357 69211 0.52 0.65 0.58 0.72
No Preterm birth 39223 727885 5.39
Yes 3287 69211 4.75 0.85 0.82 0.89
No Transverse lie 2100 727885 0.29
Yes 227 69211 0.33 1.20 1.05 1.37
No Breech position 24290 727885 3.34
Yes 4091 69211 5.91 1.74 1.68 1.80
No Emergency caesarean 63155 727885 8.68
Yes 9961 69211 14.39 1.65 1.61 1.68
No Caesarean delivery 104329 727885 14.33
Yes 15787 69211 22.81 1.73 1.70 1.77
No Perinatal death 3332 727885 0.46
Yes 465 69211 0.67 1.50 1.36 1.65
No Intrauterine death 2539 727885 0.35
Yes 325 69211 0.47 1.37 1.22 1.53
No NICU55866 727885 7.68
Yes 5847 69211 8.45 1.10 1.07 1.13
No 5 minute Apgar score <7 19201 727885 2.64
Yes 2186 69211 3.16 1.15 1.10 1.21
¥
Preterm pre labor rupture of the membranes
Transferral to neonatal intensive care unit
OR; Odds ratio, CI; Confidence Interval
https://doi.org/10.1371/journal.pone.0194814.t003
Umbilical cord length, knots and entanglement and associated risks
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Pregnancies with a short cord exhibited increased risk of non-cephalic presentation, in
both term and preterm births. Short cord was also associated with increased risk of emergency
and all-cause caesarean delivery (Table 3), (in stratified analyses in both term and preterm
births). Pregnancies with a short cord also carried an increased risk of placental complications
like placenta previa, placental abruption and the need of manual removal of the placenta after
birth (Table 3). The associated risk of placental abruption (Table 3) was observed particularly
in term births (OR 1.98 (95%CI 1.72–2.73), but was also significant in preterm births (OR
1.35, (95%CI 1.12–1.62). We observed a reduced risk of PPROM and preterm birth when the
cord was short. This was also the case for spontaneous preterm birth (data not shown).
On the other hand, pregnancies with a long cord carried a slightly reduced risk for several
of the adverse outcomes including malformations, placental abruption, placenta previa, non-
cephalic presentation and emergency caesarean delivery (Table 4). A slight increase in the risk
of preeclampsia, PPROM, intrauterine and perinatal death, low 5 minute Apgar score, and
transferal to NICU was observed in pregnancies with a long cord (Table 4).
What influences the risk of entanglement? The occurrence of umbilical cord entangle-
ment at birth was 20.7% (Table 1). The occurrence declined during the study period (Table 2)
and increased with gestational age (Tables 1and 2). In analyses stratified for gestational age
weeks (22–27, 28–36, 37–41, 42+) the risk of entanglement significantly increased if the umbil-
ical cord length was >90th percentile, and correspondingly reduced for cord length <10th
percentile in all gestational age groups (OR 2.9–3.1, and OR 0.65–0.22, respectively). In gesta-
tional age groups >27 weeks, when cord length was found to differ between the sexes, female
Fig 1. Odds ratios of a long umbilical cord (>90
th
percentile) on parity, vertical bars represent 95% confidence interval.
https://doi.org/10.1371/journal.pone.0194814.g001
Umbilical cord length, knots and entanglement and associated risks
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fetuses exhibited a significantly lower risk than male fetuses of entanglement (OR 0.86–0.88,
95% CI 0.82–0.91). Including a long or short cord and maternal age and parity in the model
did not change this.
Birth weight was significantly associated with entanglements. In SGA (<10th percentile)
we found a 22% increased risk for entanglement, and a reduced risk was observed for LGA
(>90
th
percentile). This association was also observed for all groups >27 weeks when we strati-
fied the population according to gestational age. Co-linearity of birth weight and cord length
was tested and was not present. After adjustments ART pregnancies carried a slightly lower
risk of entanglement. We further explored whether anomalous cord insertion influenced the
risk of entanglement. Velamentous and marginal cord insertions were significantly associated
with increased risk of entanglement (Table 2). This was present in both preterm and term
births (data not shown). Including, maternal age and parity, cord length and neonatal sex to
the model did not change these.
While polyhydramnios was not associated with entanglement, oligohydramnios was associ-
ated with increased risk of entanglement (OR 1.25, 95%CI 1.21–1.29). Analyzing term and pre
term births separately, this association remained significant in the term birth group (OR 1.28,
95%CI 1.24–1.32), whereas the risk of entanglement was reduced in the preterm birth group
with oligohydramnios (OR 0.82, 95%CI 0.64–0.96).
Risks associated with cord entanglement. In the analyses of associated risks in pregnan-
cies with entanglement at birth results of adjustments for maternal age and parity or other pos-
sible confounders are specified in the text when they significantly influenced the association.
Births with entanglement carried an increased risk of low 5 minutes Apgar score, intrauterine
Fig 2. Odds ratios of a long umbilical cord (>90
th
percentile) on maternal body mass index, vertical bars
represent 95% confidence interval.
https://doi.org/10.1371/journal.pone.0194814.g002
Umbilical cord length, knots and entanglement and associated risks
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and perinatal death. However, these risks were confined to term births in analyses stratified
based on gestational age (Table 5).
The associated risks for placental complications, preterm and caesarean birth and non-
cephalic position, were reduced in births with cord entanglement (Table 5).
What influences the risk of cord knots? The occurrence of cord knot in the total popula-
tion was 1.32% (Table 1), and the trend was declining during the study period (Table 2). The
occurrence did not vary significantly with gestational age at birth (Table 2). Cord knot
occurred more often in male than in female fetuses (Tables 1and 2). Parity significantly
increased the risk of cord knot (Table 2).
The strongest risk factor for cord knot was a long umbilical cord (OR 8.42, 95%CI 8.10–
8.76). Adding parity and fetal sex to the model did not significantly change this. In pregnancies
with a short cord the risk of a knot was markedly reduced (aOR 0.11, 95%CI 0.09–0.13). The
risk of a cord knot was increased in polyhydramnios, and adding a long cord to the model sig-
nificantly reduced the effect of polyhydramnios. Further including maternal age, parity, and
neonatal sex, the effect of polyhydramnios on the risk of cord knot disappeared. Also
Fig 3. Sex specific percentiles for umbilical cord length based on singleton births in Norway 1999–2013.
https://doi.org/10.1371/journal.pone.0194814.g003
Umbilical cord length, knots and entanglement and associated risks
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pregnancies with maternal diabetes, and preexisting hypertension (Table 2) were associated
with increased risk of cord knot. But also the effect of pre-gestational diabetes on the risk of
cord knot disappeared when a long cord was included in the model.
Low placental weight was associated with reduced risk of knot (Table 2), whereas a large
placenta was not associated with increased risk of a knot when we included a long cord to the
model. In pregnancies after ART we found no difference in the risk of cord knot compared
with the rest of the population.
Table 4. Odds ratios of adverse pregnancy outcomes in pregnancies with a long umbilical cord (>90th sex and parity specific percentile) in the population of single-
ton births in Norway 1999–2013.
Exposure Outcome
Cord>90th percentile Condition Yes(n) Total (n) % OR 95% CI
No Malformation 32698 728034 4.49
yes 2858 69062 4.14 0.89 0.85 0.92
No Placenta previa 2171 728034 0.30
Yes 127 69062 0.18 0.58 0.48 0.69
No Abruptio placentae 2679 726465 0.37
Yes 165 70599 0.23 0.63 0.54 0.74
No Post-partum haemorrhage
§
117376 728034 16.12
Yes 11450 69062 16.58 1.04 1.02 1.07
No Manual removal of the placenta 10280 728034 1.41
Yes 839 69062 1.21 0.84 0.78 0.90
No Preeclampsia 24881 728034 3.42
Yes 2622 69062 3.80 1.16 1.12 1.21
No PPROM
¥
5838 728034 0.80
Yes 722 69062 1.05 1.26 1.17 1.36
No Pre-term birth 65105 754586 8.63
Yes 3957 42510 9.31 1.09 1.05 1.12
No Transverse lie 2139 728034 0.29
Yes 188 69062 0.27 0.83 0.71 0.97
No Breech position 26856 728034 3.69
Yes 1525 69062 2.21 0.62 0.59 0.65
No Emergency caesarean 68379 728034 9.39
Yes 4737 69062 6.86 0.71 0.69 0.74
No Caesarean delivery 113013 728034 15.52
yes 7103 69062 10.28 0.62 0.60 0.64
No Perinatal death 3225 728034 0.44
Yes 572 69062 0.83 1.83 1.67 2.00
No Intrauterine death 2363 728034 0.32
Yes 501 69062 0.73 2.21 2.01 2.44
No NICU55735 728034 7.66
Yes 5978 69062 8.66 1.11 1.08 1.14
No 5 minute Apgar score<7 66814 775709 8.61
Yes 2248 21387 10.51 1.25 1.19 1.30
¥
Pre-term pre labour rupture of the membranes
Transferral to neonatal intensive care unit
§
Post-partum haemorrhage >500mL
OR; Odds ratio, CI; Confidence Interval
https://doi.org/10.1371/journal.pone.0194814.t004
Umbilical cord length, knots and entanglement and associated risks
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 12 / 20
Table 5. Odds ratios of adverse pregnancy outcomes in pregnancies with cord entanglement in the population of singleton births in Norway 1999–2013.
Exposure Outcome
Entanglement Condition Yes (n) Total (n) % OR 95%CI
No Malformation 31307 679343 4.61
Yes 6740 176957 3.81 0.82 0.80 0.84
No Placenta previa 2208 679343 0.33
Yes 266 176957 0.15 0.46 0.41 0.52
No Abruptio placentae 2803 679343 0.41
Yes 358 176957 0.20 0.49 0.44 0.55
No Post-partum haemorrhage
§
112507 679343 16.56
Yes 25165 176957 14.22 0.84 0.82 0.85
No Manual removal of the placenta 10303 679343 1.52
Yes 2306 176957 1.30 0.86 0.82 0.90
No Preeclampsia 23870 679343 3.51
Yes 5746 176957 3.25 0.92 0.90 0.95
No PPROM
¥
5937 679343 0.87
Yes 1227 176957 0.69 0.79 0.74 0.84
No Pre-term birth 40084 679343 5.90
Yes 6695 176957 3.78 0.63 0.61 0.64
No Transverse lie 2320 679343 0.34
Yes 228 176957 0.13 0.38 0.33 0.43
No Breech position 28135 679343 4.14
Yes 2577 176957 1.46 0.34 0.33 0.36
No Emergency caesarean 68937 679343 10.15
Yes 9880 176957 5.58 0.52 0.51 0.54
No Caesarean delivery 114749 679343 16.89
Yes 14127 176957 7.98 0.43 0.42 0.44
No Perinatal death term 1161 639259 0.18
Yes 530 170262 0.31 1.72 1.55 1.90
No Perinatal death pre-term 2414 40084 6.02
Yes 370 6695 5.53 NS
No Intrauterine death term 862 639259 0.13
Yes 437 170262 0.26 1.94 1.73 2.18
No Intrauterine death preterm 1778 40084 4.44
Yes 326 6695 4.87 NS
No NICUterm 33252 639259 5.20
Yes 9258 170262 5.44 1.04 1.02 1.07
No NICUpre-term 21603 40084 53.89
Yes 3135 6695 46.83 0.75 0.72 0.79
No 5 minute Apgar score<7 term 12484 639259 1.95
Yes 4621 170262 2.71 1.40 1.35 1.45
No 5 minute Apgar score<7 pre-term 5606 40084 13.99
Yes 773 6695 11.55 0.80 0.74 0.87
¥
Preterm pre labor rupture of the membranes
Transferral to neonatal intensive care unit
§
Post partum haemorrhage >500mL
OR; Odds ratio, CI; Confidence Interval
https://doi.org/10.1371/journal.pone.0194814.t005
Umbilical cord length, knots and entanglement and associated risks
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Risks associated with cord knot. In the analyses of associated risks in pregnancies with a
cord knot at birth adjustments for maternal age and parity did not significantly influence the
associations. In the total population cord knot increased the risk of perinatal death (OR 2.65,
95%CI 2.25–3.11). When we stratified the population for gestational age at birth, OR of perina-
tal death was more than quadrupled at term, and increased by 65% in the preterm group
(Table 6).
Also the risk of intrauterine death and low 5 minutes Apgar score was increased in both
term and preterm births with a cord knot (Table 6), whereas the risk of transferal to NICU was
increased in the term birth group (Table 6).
Combined knot and entanglement. The combination of cord entanglement and knot
occurred in 3698 births (0.43%). The occurrence of the combination did not vary significantly
between gestational age groups (data not shown), and decreased during the study period,
(0.49% in 1999–2003, and 0.37% in 2009–2013), OR 0.75 (95%CI 0.70–0.82). For the total pop-
ulation the risk of perinatal death with combined cord entanglement and knot was increased
OR 5.1 (95%CI 4.16–6.27). For gestational age 37–41 and 28–36 weeks the effect of the combi-
nation of cord entanglement and knot was more than additive with aORs of perinatal death
9.77 (95%CI 7.57–12.60) and 5.90 (95%CI 3.92–8.87), respectively. Interaction terms between
knot and entanglement in the models were significant. Adding birthweight below the 10
th
per-
centile to the model did not significantly change these results. There was no significant associ-
ated increased risk of perinatal death in births <28 and >41 weeks in births with combined
cord knot and entanglement.
Recurrence. Finally, we studied the risk of recurrence of extreme cord length, knot and
entanglement in a subsequent pregnancy. In our population 289 684 women had at least two
births in the register. If the cord was long or short in the first pregnancy, the recurrence risk of
long cord or short cord in the subsequent was more than doubled (OR 2.53, (95%CI 2.42–
2.64) and OR 2.39, (95%CI 2.29–2.49), respectively). Likewise, cord knot recurred with an OR
of 2.64 (95%CI 2.29–3.06). These risks were not influenced by neonatal sex in the second preg-
nancy, whereas including long cord in the second pregnancy reduced the recurrence risk of a
cord knot to OR 1.93 (95%CI 1.52–2.44). Entanglement did also recur with an OR of 4.61
(95%CI 4.50–4.72). Including a long cord in the second birth significantly reduced this to aOR
1.20 (95%CI 1.17–1.23).
Discussion
The findings of this population based study demonstrate that sex differences in cord length are
evident after 27 weeks, that boys have longer cords than girls, and a higher risk of cord knots
and entanglement. We also identified risk factors for long and short cord and found parity was
a strong factor (Fig 1 and in S1 Table). Placental and birth weight were associated with cord
length. Both short and long cords were associated with increased risk of adverse outcome for
the fetus and the mother, also after adjustment for important confounders. We found that the
combined effect of entanglement and knot on the risk of intrauterine or perinatal death is
more than additive, and demonstrate that extreme cord length, (and to a lesser degree cord
knot or entanglement) in one pregnancy tend to recur in a subsequent pregnancy of the same
woman. We found that in our population the trend of cord knots, entanglements, and long
cords during the study period is declining.
Our reference ranges for cord length based on a nationwide registry study do not differ sig-
nificantly from those of a large Finnish hospital based study [10]. The cord length at birth
increases linearly through gestation, and continues to increase also beyond 40 weeks (Fig 3).
Georgiadis et al. [10] found a possible association of a short cord to abruption of the placenta,
Umbilical cord length, knots and entanglement and associated risks
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 14 / 20
Table 6. Odds ratios of adverse pregnancy outcomes in pregnancies with cord knot in the population of singleton births in Norway 1999–2013.
Exposure Outcome
Cord knot Condition Yes(n) Total (n) % OR 95%CI
No Malformation 37532 845029 4.44
Yes 515 11271 4.57 NS
No Placenta previa 2442 845029 0.29
Yes 32 11271 0.28 NS
No Abruptio placentae 3121 845029 0.37
Yes 40 11271 0.35 NS
No Post-partum haemorrhage
§
136027 845029 16.10
Yes 1645 11271 14.59 0.89 0.85 0.94
No Manual removal of the placenta 12435 845029 1.47
Yes 174 11271 1.54 NS
No Preeclampsia 29164 845029 3.45
Yes 452 11271 4.01 1.17 1.06 1.29
No PPROM
¥
7054 845029 0.83
Yes 110 11271 0.98 NS
No Pre-term birth 46086 845029 5.45
Yes 693 11271 6.15 1.14 1.05 1.23
No Transverse lie 2507 845029 0.30
Yes 41 11271 0.36 NS
No Breech position 30435 845029 3.60
Yes 277 11271 2.46 0.67 0.60 0.76
No Emergency caesarean 77741 845029 9.20
Yes 1076 11271 9.55 NS
No Caesarean delivery 127127 845029 15.04
Yes 1749 11271 15.52 NS
No Perinatal death term 1600 798943 0.20
Yes 91 10578 0.86 4.32 3.50 5.35
No Perinatal death pre-term 2719 46086 5.90
Yes 65 693 9.38 1.65 1.28 2.14
No Intrauterine death term 1216 798943 0.15
Yes 83 10578 0.78 5.19 4.15 6.49
No Intrauterine death pre-term 2046 46086 4.44
Yes 58 693 8.37 1.97 1.50 2.58
No NICUterm birth 41812 798943 5.23
Yes 698 10578 6.60 1.28 1.18 1.38
No NICUpre-term birth 24369 46086 52.88
Yes 369 693 53.25 NS
No 5 minute Apgar score<7 term birth 16797 798943 2.10
Yes 308 10578 2.91 1.40 1.25 1.57
No 5 minute Apgar score<7 pre-term birth 6261 46086 13.59
Yes 118 693 17.03 1.31 1.07 1.59
¥
Pre-term pre-labour rupture of the membranes
Transferral to neonatal intensive care unit
§
Post-partum haemorrhage >500mL
OR; Odds ratio, CI; Confidence Interval
NS; non-significant
https://doi.org/10.1371/journal.pone.0194814.t006
Umbilical cord length, knots and entanglement and associated risks
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and our study is large enough to confirm that a short cord is associated with a 50% increased
risk of abruption in the total population (Table 3), and a doubled risk at term. Polyhydramnios
was in our study associated with an increased risk of cord knot, which corroborates earlier
findings [4]. We find a slightly higher occurrence of cord knot (1.3% vs 1.2%), but lower asso-
ciated risks in pregnancies with a cord knot than those reported in a hospital study [11]. Both
risk factors for short cord, cord knot and associated risks of adverse outcomes including
maternal complications and stillbirth identified in our study compares well with other studies
[9,11,12]. In addition, our study finds that the risk of stillbirth in pregnancies with cord knot
and entanglement is higher in term than preterm births (Tables 5and 6). In contrast to a case-
control study [9], we find increased risk of non-cephalic position when the cord is short, and
reduced risk when the cord is long (Tables 3and 4). Further, we find an increased risk of cae-
sarean delivery in short cord pregnancies, which is in opposition to the case-control study [9].
The observed differences may be due to differences in the definition of a short cord, different
populations and study design.[1–3] Strength of the study is that it is population based, which
reduces selection bias, and its large size, which makes it possible to study exposures and out-
comes with a low incidence. The data from the MBRN also makes it possible to calculate recur-
rence risk and trend. Several of the variables in the MBRN have been validated [13–15], and
our recent study of midwives measurements, classification and notifications to the MBRN on
placenta and cord findings suggest these data are valid [16]. We consider it a strength that the
present study is comprehensive by assessing risk factors and associated risks for both a short
and a long cord, knots and entanglements in the same study.
Amniotic fluid amount was only estimated clinically at birth and was not verified by ultra-
sound. Therefore our results regarding the association between poly- and oligohydramnios
with cord length, knot and entanglement should be interpreted with caution. The only pater-
nal characteristic that was available in our study was age, and the effect of paternal age was
abolished when adjusted for maternal age or parity. We also did not have access to information
of socioeconomic or ethnic factors that may influence cord length or other outcomes or
exposures.
Because of lacking information on number of loops and of which body parts the cord was
entangled, we were unable to study whether nuchal entanglement or the number of loops
influence risks. Our study does not contain information of whether (nuchal) entanglements
were identified prenatally. A fetus may entangle or untangle during the rotational movements
during delivery. Thus, this needs to be studied in a clinical setting comparing ultrasound iden-
tification or exclusion of cord entanglement directly before delivery. A previous study of high-
risk pregnancies found that entanglement was less common in caesarean than vaginal births,
indicating that entanglement may occur during delivery [17].
Information about umbilical cord coiling or other features of umbilical cord are not avail-
able in the register. Because of practical circumstances clamping and cutting of the cord may
be performed in to stages in cesarean delivery, (clamping by the surgeon and thereafter cutting
by the midwife). Thus, a small part of the cord may be lost to measure, and we cannot entirely
rule out a systematic bias towards measuring a shorter cord when the delivery was by caesar-
ean. However, when analyzing caesarean and vaginal births separately the risks estimates did
not differ significantly. We cannot infer from our study whether cord entanglement contrib-
utes to growth restriction, or the other way around. The same applies for the association of oli-
gohydramnios and entanglement.
The identified risk factors had opposite effect on the risk of a long compared to the risk of a
short cord, which supports the biological plausibility of our findings (Tables 1and 2). Several
examples of dose-response relations in our study further lend support to this, for example the
risk of a long cord increased significantly with BMI class (Fig 1, panel B). The fact that a short
Umbilical cord length, knots and entanglement and associated risks
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 16 / 20
cord carried increased risk of placental complications and a long cord was associated with a
reduced risk for these complications (Tables 3and 4) suggest that the development of a short
cord and abnormal placentation is linked.
We provide population based empirical reference ranges (fetal sex and parity specific) for
umbilical cord length (Fig 3 and in S1 Table). However, it is important to bear in mind that
these reference ranges are based on cord length in born individuals and they may not be repre-
sentative for those still in utero.
Cord compression in knots or entanglements may reduce umbilical blood flow [18]. An
experimental study of cord compression in fetal sheep (0.6 gestation) shows that compression
of the umbilical cord alters the distribution of the umbilical and systemic blood flow [19,20]
and the fetal responses to this challenge differ with gestational age [21]. In late pregnancy less
of the fetal cardiac output is directed to the placenta [22], but the fetal demand increases,
which in turn increase the vulnerability for cord accident and obstruction of umbilical flow in
late pregnancy. This is in line with our finding that the risk of intrauterine death is quadrupled
at term when an umbilical cord knot is present and 10 times increased when the cord is both
entangled and has a knot. However, the finding that the combination of cord knot and entan-
glement was associated with increased risk of stillbirth only in the term birth group may be
due to low numbers in the pre- and post-term groups.
One may argue that it is unclear what the clinician should do with the information of the
umbilical cord length, entanglements and knots. Prenatal identification of these abnormalities
with ultrasound is hampered with low sensitivity and specificity, and the results may cause
unnecessary worries and frustration for the mother and the clinician [23,24]. However, prena-
tal identification of conditions that are associated with compressed umbilical cord are sug-
gested in the literature to be offered close follow-up [25]. The increased risk of recurrence of
cord anomalies found in this study may contribute to justify extra clinical follow-up in a preg-
nancy following one with anomalous cord or cord accidents.
Since cord anomalies are important risk factors for stillbirth the results of the present study
support that the umbilical cord and placenta should be given special attention by perinatal
pathologists in these tragic events [26].
Large-scale public health data utilized in epidemiological studies are important steps in the
way to increase the insight to the development in human (fetal) biology. Genetic and environ-
mental factors influence the development of the cord. A twin study suggests that cord length is
influenced by heritable factors, whereas their interpretation was that twisting and cord inser-
tion is strongly influenced by nongenetic factors [27]. The results from a previous study (focus-
ing on cord insertion site) and the present found that fetal sex has a strong influence, and
increased risk of recurrence of cord length and insertion suggest that genetic and persisting
environmental factors influence the development of the cord and placenta in singletons [4].
Maternal diabetes significantly influence the expression of genes in the umbilical cord and
alters the umbilical vessel phenotype, with possible long term consequences for the neonate
[28].
The fact that cord knots and entanglements occurred more often in male fetuses may be
attributable to longer cords in boys than girls. Although disputed [9], the “stretch hypothesis”
which says that tensile force is an important determinant for cord length [29] suggests that an
active fetus develop a longer cord. There have also been raised theories of male fetuses exhibit-
ing a higher level of activity in the womb [30,31]. This fits with our observation that boys had
longer cords and increased risk of entanglements and knots, also after adjusting for long cord
and parity. The differential effect of sex on cord length is supported by the finding that boys
are more active in the womb, and show larger response to vibroacoustic stimulation than girls
from 31 weeks [32–34]. Our findings of differences between girls and boys are consistent with
Umbilical cord length, knots and entanglement and associated risks
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previous findings that the placenta has sex differential features from early gestation: Sex-chro-
mosome genes are differently expressed in human male and female placentas, and male pla-
centas are more responsive to changes in maternal environment than female [35,36].
However, an ultrasound study of umbilical constriction at the abdominal wall inlet found that
the degree of constriction was positively associated with a longer cord only in female fetuses
[37].
It has been shown that fetuses in breech position had reduced body movements in response
to vibroacoustic stimulation compared with fetuses in cephalic position [38]. This is in line
with our observation that breech position was associated with reduced occurrence of a long
cord, cord knot and entanglement, and increased risk of a short cord, which further supports
the theory that fetal activity influence cord length, knots and entanglement.
Conclusions
Our population study indicates that cord length was determined by both fetal and maternal
factors in singletons, and that fetal sex and parity were important determinants. There was an
increased risk of recurrence of extreme cord length, knots and entanglement. Extreme cord
length, entanglement and particularly cord knot were associated with increased risk of adverse
outcomes including a more than doubled risk of perinatal death. The combination of cord
knot and entanglement seem to exhibit more than additive effect on the risk of perinatal death,
an almost 10 times increased risk at term. We provide population based parity and sex specific
reference ranges for umbilical cord length.
Supporting information
S1 Table. Gestational age (weeks), parity (0–1+) and sex specific empirical umbilical cord
length (cm) percentiles.
(DOCX)
S1 List. Malformation diagnoses.
(DOCX)
Acknowledgments
The authors thank the Medical Birth Registry of Norway for providing the data set.
Author Contributions
Conceptualization: Lorentz Erland Linde, Svein Rasmussen, Jo¨rg Kessler, Cathrine Ebbing.
Data curation: Svein Rasmussen.
Formal analysis: Svein Rasmussen, Cathrine Ebbing.
Funding acquisition: Cathrine Ebbing.
Investigation: Lorentz Erland Linde, Svein Rasmussen, Jo¨rg Kessler, Cathrine Ebbing.
Methodology: Lorentz Erland Linde, Svein Rasmussen, Jo¨rg Kessler, Cathrine Ebbing.
Project administration: Cathrine Ebbing.
Supervision: Svein Rasmussen.
Writing – original draft: Lorentz Erland Linde, Svein Rasmussen, Jo¨rg Kessler, Cathrine
Ebbing.
Umbilical cord length, knots and entanglement and associated risks
PLOS ONE | https://doi.org/10.1371/journal.pone.0194814 March 27, 2018 18 / 20
Writing – review & editing: Lorentz Erland Linde, Svein Rasmussen, Jo¨rg Kessler, Cathrine
Ebbing.
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