Factors related to morbidity and maternal and perinatal outcomes of umbilical cord torsion.

Introduction

Umbilical cord coiling has been described as Wharton’s jelly-covered umbilical vessels that spiral 360° because of fetal movement, with active or passive torsion of the embryo and various umbilical vascular growth rates, fetal hemodynamic forces, and arrangements of muscular fibers in the umbilical arterial wall.[1] The umbilical vessels are protected against pressure by the buffering effect of the tissue and coiled nature of the umbilical cord.[2] In one study in China, torsion of the umbilical cord was defined as more than 11 coils.[3] Coiling can restrict blood flow in the umbilical vessels, resulting in umbilical cord thrombogenesis, fetal growth restriction, or intrauterine fetal death. The arteries coil around the vein, causing artery pulsation and longitudinal distortion of the cord. This creates a relative negative pressure in the vein, which then helps increase blood flow from the placenta to the fetus.[4] Physiological twists are considered to involve 12 coils, and they make the umbilical cord flexible and strong, providing resistance to external forces. The umbilical coiling index (UCI) was defined by Strong et al.[5] in 1994 as the total number of complete coils per centimeter of the total length of the umbilical cord. In the present study, we evaluated the independent risk factors affecting torsion of the umbilical cord, identified the relationship between torsion of the umbilical cord and maternal and perinatal outcomes, analyzed the clinical value of the UCI in predicting fetal distress, and provided a clinical reference for prenatal diagnosis of umbilical cord torsion and prevention of fetal distress.

Methods

Study design and patients

This retrospective study was performed at the Fujian Provincial Maternity and Children’s Hospital. Antenatal women with a singleton pregnancy who went into labor from 1 January 2016 to 31 December 2016 were included. We excluded women with multifetal gestation, stillbirths, and fetuses with congenital malformation. Torsion of the umbilical cord was defined as ≥12 coils according to a Chinese perinatology study.[2] As previously described, the UCI was defined as the number of complete coils per centimeter of umbilical cord length.[3]

Data collection

The patients were divided into two groups: those with and without torsion of the umbilical cord. Antepartum data, labor parameters, and neonatal outcomes were collected. The antepartum data included maternal age, parity (primiparous or multiparous), premature rupture of membranes, gestational diabetes, hypertension during gestation, intrauterine growth restriction, polyhydramnios, oligohydramnios, prior cesarean delivery, and placenta previa. The labor parameters included gestational age at delivery, fetal heart rate abnormalities during labor, meconium staining of amniotic fluid, length of the umbilical and nuchal cord, fetal distress, and mode of delivery. After delivery, the length of the umbilical cord was measured and the number of complete coils was counted. The UCI was calculated by dividing the total number of coils by the total length of the umbilical cord in centimeters. The neonatal outcomes included the sex of the newborn, birth weight, Apgar scores, admission to the neonatal intensive care unit, and small for gestational age.

Statistical analysis

SPSS version 22.0 software (IBM Corp., Armonk, NY, USA) was used for the statistical analyses. Quantitative data are expressed as mean ± standard deviation, and qualitative data are presented as ratios. The statistical significance of differences between the two groups was assessed using the independent-samples t test, chi square test, and Fisher’s exact test. A logistic regression analysis was used to select the main variables related to umbilical cord torsion. A multivariable logistic regression analysis was applied to identify independent risk factors for torsion. The results are reported as odds ratios (ORs) and 95% confidence intervals (CIs). A p-value of <0.05 was regarded as statistically significant. A receiver operating characteristic curve was plotted to select the proper cut-off value of the UCI to predict fetal distress.

Results

Patients

This study included a total of 845 pregnant women (433 primiparas and 412 multiparas). Their age ranged from 16 to 45 years, and the gestational age at the time of delivery ranged from 29.57 to 41.71 weeks. The mean UCI was 0.3671 ± 0.11 coils/cm.

Outcomes

We compared the antepartum data, labor parameters, and neonatal outcomes between patients with and without umbilical cord torsion, and these data are summarized in Table 1. A maternal age of ≥35 years was significantly more prevalent in patients with than without torsion (53.7% vs. 46.3%, respectively; p = 0.017). The mean length of the umbilical cord was significantly longer in patients with than without torsion (64.03 ± 14.13 vs. 58.12 ± 11.90 cm, respectively; p = 0.000). The mean neonatal weight was significantly lower in patients with than without torsion (3194.71 ± 529.50 vs. 3279.77 ± 449.36 g, respectively; p = 0.018). Multiparous pregnancy and gestational diabetes were not significantly associated with torsion of the umbilical cord.

Table 1.

Antepartum data, labor parameters, and neonatal outcomes.

Characteristics	No umbilical cord torsion	Umbilical cord torsion	χ2	p-value
Maternal age of ≥35 years	50 (46.3)	58 (53.7)	5.734	0.017
Maternal weight, kg	67.95 ± 8.00	69.47 ± 32.86	0.686*	0.493
Parity
Primiparous	168 (38.8)	265 (61.2)	3.619	0.057
Multiparous	134 (32.5)	278 (67.5)
Premature rupture of membranes	77 (38.9)	121 (61.1)	0.958	0.328
Gestational diabetes	34 (28.3)	86 (71.7)	3.614	0.057
Hypertension during gestation	19 (43.2)	25 (56.8)	1.049	0.306
Intrauterine growth restriction	6 (27.3)	16 (72.7)	0.748	0.387
Oligohydramnios	15 (50.0)	15 (50.0)	2.659	0.103
Polyhydramnios	0 (0.0)	6 (100.0)	2.009	0.156
Prior cesarean delivery	43 (36.4)	75 (63.6)	0.018	0.893
Placenta previa	5 (35.7)	9 (64.3)	0.893	1.000
Amniotic fluid index	13.12 ± 9.27	13.67 ± 4.13	1.131*	0.259
Length of umbilical cord, cm	58.12 ± 11.90	64.03 ± 14.13	6.175*	0.000
Gestational age at delivery of ≥37 weeks	290 (36.8)	498 (63.2)	3.372	0.066
Longer length of umbilical cord	4 (19.0)	17 (81.0)	2.677	0.102
Number of nuchal cords
One loop	54 (30.9)	121 (69.1)	–	0.357
Two loops	14 (43.8)	18 (56.3)
Three loops	1 (20.0)	4 (80.0)
Four loops	0 (0.0)	1 (100.0)
Sex of newborn
Male	156 (35.0)	290 (65.0)	–	0.685
Female	148 (37.0)	252 (63.0)
Birth weight, g	3,279.77 ± 449.36	3,194.71 ± 529.50	2.367*	0.018

Data are shown as mean ± standard deviation or n (%). Fisher’s exact probability method was used. *Independent-samples t-test was used.

In the multivariable logistic regression analysis, multiparous pregnancy (OR, 1.638; 95% CI, 1.199–2.239; p = 0.002) and a longer umbilical cord (OR, 1.041; 95% CI, 1.027–1.054; p = 0.000) were independent risk factors for torsion of the umbilical cord (Table 2).

Table 2.

Multivariable logistic regression analysis of factors associated with umbilical cord torsion.

Characteristics	Regression coefficient	Standard error	Wald statistic	p-value	OR (95% CI)
Maternal age of ≥35 years	−0.842	0.233	13.005	0.000	0.431 (0.273–0.681)
Parity (primiparous or multiparous)	0.494	0.159	9.586	0.002	1.638 (1.199–2.239)
Gestational diabetes	0.397	0.229	3.013	0.083	1.488 (0.950–2.329)
Gestation age at delivery of ≥37 weeks	−0.446	0.364	1.502	0.220	0.640 (0.313–1.307)
Length of umbilical cord	0.040	0.006	37.683	0.000	1.041 (1.027–1.054)
Birth weight	−0.385 × 10−3	0.000	4.683	0.030	1.000 (0.999–1.000)

OR, odds ratio; CI, confidence interval.

As shown in Figure 1, when a UCI of >0.36 coils/cm was used as the cutoff value to predict fetal distress, the sum of the sensitivity (65.2%) and specificity (63.6%) was maximal and the area under the curve was 0.666. When the umbilical artery peak systolic to end diastolic flow velocity ratio (S/D ratio) was used to predict fetal distress, the area under the curve was 0.505.

Figure 1.

Receiver operating characteristic curve of UCI for prediction of fetal distress. UCI, umbilical coiling index; S/D, peak systolic to end diastolic flow velocity ratio.

Table 3 summarizes the relationships between torsion of the umbilical cord and the maternal and perinatal outcomes. The incidences of fetal distress (20.6% vs. 6.9%, p = 0.000), fetal heart rate abnormalities during labor (3.7% vs. 0.7%, p = 0.008), and meconium staining of amniotic fluid (21.9% vs. 14.8%, p = 0.011) were significantly higher in patients with than without umbilical cord torsion. The incidences of caesarean deliveries (33.9% vs. 28.5%, p = 0.016), instrumental vaginal deliveries (1.7% vs. 0.0%, p = 0.016), and emergency cesarean deliveries (5.2% vs. 2.0%, p = 0.023) were also significantly higher in patients with than without umbilical cord torsion.

Table 3.

Maternal and perinatal outcomes in patients with and without umbilical cord torsion.

Characteristics	No umbilical cord torsion	Umbilical cord torsion	χ2	p-value
Fetal distress	21 (6.9)	112 (20.6)	27.885	0.000
Mode of delivery
Vaginal delivery	218 (71.5)	350 (64.5)	8.248	0.016
Instrumental vaginal delivery	0 (0.0)	9 (1.7)
Cesarean delivery	87 (28.5)	184 (33.9)
Fetal heart rate abnormality during labor	2 (0.7)	20 (3.7)	7.051	0.008
Emergency cesarean delivery	6 (2.0)	28 (5.2)	5.205	0.023
Meconium staining of amniotic fluid	45 (14.8)	119 (21.9)	6.420	0.011
Low Apgar score (≤7 at 1 minute)	0 (0.0)	6 (1.1)	2.004	0.157
Neonatal intensive care unit admission	10 (3.3)	37 (6.8)	4.687	0.030
Small for gestational age	5 (1.6)	28 (5.2)	6.419	0.011

Data are shown as n (%).

Admission to the neonatal intensive care unit was significantly associated with torsion of the umbilical cord (6.8% vs. 3.3% in patients with and without torsion, respectively; p = 0.030). Small for gestational age was also significantly associated with torsion (5.2% vs. 1.6% in patients with and without torsion, respectively; p = 0.011). A low Apgar score (≤7 at 1 minute) was not significantly associated with torsion of the umbilical cord.

Discussion

The umbilical cord is a banded structure of the fetus and placenta. It also serves as an active pump mechanism in the process of venous return to the fetus.[6,7] Twists of the umbilical vessels can be observed as early as 28 days after conception and are clearly present in about 95% of fetuses beginning at 9 weeks after conception.[8,9]

In this study, our objective was to analyze the risk factors for torsion of the umbilical cord. We found that multiparous pregnancy and a longer umbilical cord were independent risk factors for umbilical cord torsion. Thus, we confirmed the findings of a previous study in which the incidences of all types of umbilical cord complications (including torsion of the umbilical and nuchal cords) increased as the umbilical cord length increased.[10] Our study data showed a strong correlation between torsion of the umbilical cord and maternal age of ≥35 years. Pergialiotis et al.[1] showed that there was a similarly strong correlation between torsion of the umbilical cord and maternal age of ≥35 years (p = 0.003). Jo et al.[6] reported similar findings; torsion of the umbilical cord was related to low or high maternal age (<20 and >35 years, respectively). In the present study, lower neonatal weight was significantly correlated with torsion of the umbilical cord. Miremberg et al.[11] found that because adequate coiling prevents the umbilical cord from compressing, torsion of the umbilical cord results in reduced fetoplacental circulation in the long term, thus restricting growth.

Mittal et al.[12] found that intrauterine growth restriction and hypercoiling were significantly related to each other. A similar correlation was reported by Patil et al.[13] Although most studies reported the association between umbilical cord torsion and preterm delivery,[14,15] none has provided a rational explanation for the underlying mechanism. Our study demonstrated a contrary result; i.e., that preterm delivery was not related to umbilical cord torsion. Torsion of the umbilical cord led to fetal distress, resulting in iatrogenic preterm labor. Whether torsion of the umbilical cord causes spontaneous preterm delivery requires further investigation.

Torsion of the umbilical cord can increase resistance of blood flow and reduce the fetal blood supply, leading to fetal distress. Coiling is not homogenous throughout the umbilical cord; some segments are more coiled than others. In the present study, the UCI was calculated postpartum, similar to most studies. We found that a UCI of >0.36 can predict fetal distress. Miremberg et al.[11] proposed that the number of coils remains constant throughout pregnancy. They stated that 30% of non-coiled umbilical cords that are detected before 20 weeks’ gestation with an ultrasound scan will become coiled during the latter half of gestation, but that previously coiled umbilical cords do not become uncoiled. Although most studies measured the UCI postpartum, prenatal prediction makes more sense from a clinical viewpoint. Sharma et al.[16] calculated the antenatal UCI as a reciprocal value of the distance between a pair of coils, measured in centimeters, from the inner edge of the arterial or venous wall to the outer edge of the next coil along the ipsilateral side of the umbilical cord using Doppler ultrasonography. The direction was from the placental end to the fetal end at 18 and 22 weeks of gestation. Mittal et al.[12] determined the UCI with transabdominal ultrasound at three different cord segments (one near the fetal insertion of the umbilical cord, one near the placental insertion, and one anywhere between the two) between 20 and 24 weeks of gestation. The mean of these three values was calculated, and the reciprocal of this value was used as the final UCI value. We concluded that the UCI can be measured antenatally with sonography during the second-trimester screening examination. A UCI of >0.3 can be used to select pregnant women for more vigilant antenatal follow-up examinations and intensify the fetal monitoring during pregnancy and labor.

Torsion of the umbilical cord can lead to adverse maternal and perinatal outcomes. Pergialiotis et al.[1] demonstrated that torsion of the umbilical cord was associated with an increased incidence of meconium staining of amniotic fluid, fetal distress, caesarean deliveries, instrumental vaginal deliveries, and fetal heart rate abnormalities. Our findings support these results. Torsion of the umbilical cord led to decreased flexibility of the umbilical cord, increased twisting, and decreased ability to withstand labor. Therefore, cord torsion increases the incidence of fetal distress and heart rate abnormalities, further increasing the incidence of caesarean and instrumental vaginal deliveries.

In this study, the incidence of meconium staining of amniotic fluid was significantly higher in patients with than without umbilical cord torsion. Intrauterine fetal hypoxia led to constriction of the fetal gastrointestinal tract, increased intestinal peristalsis, relaxation of the anal sphincter, and resultant fecal excretion; the amniotic fluid was thus polluted by feces. Ohno et al.[17] reported that patients with umbilical cord torsion showed a significant decrease in the blood flow in the umbilical vein, which resulted in restricted fetal growth and various complications during delivery. In our study, the incidence of admission to the neonatal intensive care unit and the proportion of infants that were small for gestational age were significantly higher in patients with than without umbilical cord torsion, which is consistent with the results of the study by Ohno et al.[17]

This study has some limitations that should be acknowledged. We reviewed cases from a single hospital, and because of the retrospective nature of this study, some data may have been missed. However, we comprehensively analyzed factors associated with torsion of the umbilical cord. This study is the first to explore the outcomes of torsion of the umbilical cord, a topic that deserves much more attention in this field. Continued investigation of the risk factors revealed in this study may provide insight into therapeutic drug discovery.

Conclusion

Prenatal prediction of umbilical torsion is very important because torsion can result in many adverse maternal and perinatal outcomes. The UCI is a better predictor of fetal distress than the umbilical artery S/D ratio. Torsion of the umbilical cord is not associated with perinatal asphyxia. Low birth weight of the infants with umbilical cord torsion was not measured in this study, and more attention to this topic is required in future studies.