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ORIGINAL RESEARCH |
From the Departments of 1Obstetrics, Julius Center for Health Sciences, 2Primary Care, and 3Pathology, University Medical Center Utrecht, Utrecht, the Netherlands; and 4Department of Obstetrics and Gynaecology, St. Elisabeth Hospital Tilburg, Tilburg, the Netherlands.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: Umbilical cords and hospital records of 885 patients were studied in a cross-sectional study design. The umbilical coiling index was determined as the number of complete coils divided by the length of the cord in centimeters, blinded for pregnancy outcome. Obstetric history and pregnancy outcome of each patient were obtained from hospital records, blinded for the umbilical coiling index. Odds ratios and their 95% confidence intervals were calculated to evaluate associations between undercoiling and overcoiling and adverse pregnancy outcome, using multiple logistic regression.
RESULTS: Undercoiling (umbilical coiling index below the 10th percentile, using references values from uncomplicated pregnancies) was associated with fetal death (odds ratio [OR] 3.35, 95% confidence interval [CI] 1.48–7.63), spontaneous preterm delivery (OR 2.16, 95% CI 1.34–3.48), trisomies (OR 5.79, 95% CI 2.07–16.24), low Apgar score at 5 minutes (OR 3.14, 95% CI 1.47–6.70), velamentous cord insertion (OR 3.00, 95% CI 1.16–7.76), single umbilical artery (OR 3.68, 95% CI 1.26–10.79), and dextral coiling (OR 1.80, 95% CI 1.02–3.17). Overcoiling (umbilical coiling index above the 90th percentile) was associated with asphyxia (OR 4.16, 95% CI 1.30–13.36), umbilical arterial pH < 7.05 (OR 2.91, 95% CI 1.05–8.09), small for gestational age infants (OR 2.10, 95% CI 1.01–4.36), trisomies (OR 9.26, 95% CI 2.84–30.2), single umbilical artery (OR 8.25, 95% CI 2.60–26.12), and sinistral coiling (OR 4.30, 95% CI 1.52–12.2).
CONCLUSION: Undercoiling and overcoiling of the umbilical cord are associated with increased risk for adverse perinatal outcome.
LEVEL OF EVIDENCE: II-3
Several studies have addressed the correlations between abnormal cord coiling and adverse pregnancy outcome. They all show an increase in adverse pregnancy outcome when there is abnormal cord coiling. However, the results are equivocal in several respects. Whereas some studies showed significant correlations between abnormal cord coiling and preterm delivery, fetal death, fetal growth restriction, fetal chromosomal or structural abnormalities, operative delivery for fetal distress, and meconium staining of amniotic fluid, others did not. Confounding factors, such as considerably varying reference values, no blinding procedures, and not performing multivariate analyses may be the reasons behind these conflicting results.11
The aim of our study was to estimate the correlation between umbilical cord coiling and adverse pregnancy outcome, with adequate blinding procedures, use of reference values from exclusively uncomplicated pregnancies, and multivariate analysis of the results.
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MATERIALS AND METHODS |
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Clinical indications for histologic examination of the placenta were fetal death, fetal growth restriction, fetal asphyxia, structural or chromosomal abnormalities of the infant, preterm delivery, signs of intrauterine infection, preeclampsia, gestational diabetes mellitus, and macroscopic abnormalities of the placenta. Referral for placental examination was independent of umbilical cord coiling status.
The placentas were examined by 1 or 2 of the authors (M.dL., P.N.), who were blinded to patient characteristics and pregnancy outcome. All specimens were unfixed. The length of the cord was measured and the number of complete (360°) helices of the umbilical vessels was counted. The umbilical coiling index was calculated as the number of coils divided by the cord length in centimeters, as introduced by Strong et al.7 Measurement of the umbilical coiling index is demonstrated in Figure 1. One of the authors (M.dL.) also reported the direction of cord coiling (sinistral, dextral, or mixed). The coiling pattern was defined as being sinistral if the course of the umbilical helix was from right to left, ie, counterclockwise. A number of unselected cords (n = 190) were examined independently by both authors to evaluate the interobserver agreement for the umbilical coiling index.
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As in previous studies, the umbilical coiling index was classified as undercoiled if the coiling index was smaller than the 10th percentile, normocoiled if the umbilical coiling index was between the 10th and 90th percentile, or overcoiled if the umbilical coiling index was above the 90th percentile.6–8,10 Undercoiling was defined as less than 0.07 coils/cm and overcoiling as more than 0.30 coils/cm. These cutoffs were derived from an earlier study of the umbilical coiling index in normal pregnancies in our institution, designed and executed to provide reference values for cord coiling.12
We estimated possible associations with a range of clinical outcomes and with placental histologic findings. A form was completed for each subject, detailing the medical and obstetric history. The investigator completing these forms was blinded to the coiling index. The following data were collected: gestational age at delivery, parity, maternal age, maternal race, obstetric history, Apgar scores, fetal blood gasses, meconium staining of the amniotic fluid, sex and birth weight of the neonate, preterm delivery, instrumental delivery for fetal distress, small for dates infants, large for dates infants, trisomies, anatomic abnormalities in absence of trisomy, fetal death, neonatal death within 28 days of delivery, termination of pregnancy, preeclampsia, use of medication, substance abuse, and neonatal events.
Parity was defined as the number of previous pregnancies of at least 20 weeks gestational age. Gestational age at delivery was calculated by the best estimate according to menstrual history or first trimester ultrasonography or both. Preterm delivery was defined as a delivery before 37 completed weeks of gestation. A low Apgar score was defined as a score less than 7. Small for dates infants and large for dates infants were defined as having a birth weight below the 10th percentile or above the 90th percentile, respectively, for the Dutch population.13 Meconium staining of amniotic fluid included the presence of any degree of meconium in the amniotic fluid noticed during delivery.
The placenta and umbilical cord were examined for placental weight, umbilical cord length, number of umbilical coils, and insertion of the umbilical cord. For clinical reasons placentas were examined microscopically for signs of chorioamnionitis, funiculitis umbilicalis, chronic hypoxia or ischemia, accelerated or delayed maturation of the placenta, and thrombosis of the fetal placental vessels. Chronic fetal hypoxia or ischemia was defined as an increase in nucleated red blood cells in the fetal circulation of the placental villi.14 Accelerated or delayed maturation of the placenta was scored using the criteria of Benirschke and Kaufmann.14 Chorioamnionitis was defined as inflammatory reaction with infiltration of polymorphonuclear leukocytes in the membranes or chorionic plate. Thrombosis was defined as thrombosis in fetal vessels (arteries as well as veins) of the chorionic plate or groups of more than 5 avascular fibrotic villi without inflammation or iron depositions.
The data were analyzed using the Statistical Package for the Social Sciences 11.5 (SPSS Inc, Chicago, IL). Differences between continuous variables were tested by the Student t test for independent samples. Spearman correlation was used to examine the relation of maternal age, gestational age, birth weight, and birth percentile on the umbilical coiling index. Interobserver agreement on the ascertainment to the undercoiling, normocoiling, or overcoiling group was evaluated by Cohen's 
. We calculated odds ratios and their 95% confidence intervals using logistic regression analysis to evaluate the strength of associations between undercoiling and overcoiling and adverse pregnancy outcome. Multiple regression analysis was used to correct for possible confounding variables. The model used 2 dummy variables, with an umbilical coiling index between the 10th and 90th percentiles as the reference. Linear regression was used to evaluate differences in mean umbilical coiling index between the groups with a different umbilical coiling pattern (sinistral, dextral, and mixed), again using dummy variables. A value of P < .05 was considered to indicate statistically significant differences.
Sample size consideration a priori showed that 312 cases and 468 controls would be needed for this study to have a power of 90% to detect odds ratios of 2 or larger at the 2-tailed .05 level of significance, with a case–control ratio of 1:1.5 and with a 10% frequency of both undercoiling and overcoiling in the control population.15
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RESULTS |
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The associations between undercoiling and overcoiling and adverse outcome are summarized in Table 2. Undercoiling was associated with fetal death, spontaneous preterm delivery, trisomies, low Apgar score at 5 minutes, velamentous cord insertion, and presence of a single umbilical artery. Overcoiling was associated with asphyxia, low arterial pH in umbilical artery at birth, small for gestational age neonates, trisomies, and presence of a single umbilical artery. There was a nonsignificant trend toward more fetal deaths in pregnancies with overcoiled cords.
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We found a small but significant inverse relation between umbilical coiling index and birth weight percentile (r –0.08, P = .02). Adjustment of all associations for nulliparous compared with parous women (because their difference in mean umbilical coiling index almost reached statistical significance) for single umbilical artery or for velamentous insertion of the cord did not substantially alter the magnitude of the associations.
There were no significant relations between undercoiling or overcoiling and racial differences, maternal medication, structural abnormalities of the fetus in the absence of trisomy, preterm rupture of membranes, operative delivery for fetal distress, cord entanglement, meconium staining of amniotic fluid, chorioamnionitis, thrombosis of fetal placental vessels, placental abruption, or placental maturation. There were no significant linear or U-shaped relations between umbilical coiling index and arterial pH (r 0.00), venous pH (r 0.03), arterial base deficit (r 0.01), and venous base deficit (r 0.03). U-shaped relations were excluded by evaluations of deviations from linear fits.
The observed incidence of sinistrally coiled cords was 70.7% and of dextrally coiled cords was 16.5%; the remainder of umbilical cords had a mixed coiling direction pattern. The mean umbilical coiling index was 0.18 coils/cm in sinistrally coiled cords, 0.14 coils/cm in dextrally coiled cords, and 0.12 coils/cm in cords with a mixed coiling pattern. The differences in means were tested using linear regression. The difference in means between sinistral coiling and dextral or mixed coiling was statistically significant (P < .001), the difference in means between dextral and mixed coiling did not reach statistical significance (P = .13). Overcoiling occurred more often in sinistrally coiled cords, and undercoiling occurred more often in dextrally coiled cords (Table 2). In cords with a mixed coiling pattern, overcoiling did not occur at all. The results of the reproducibility study showed the value on the ascertainment to the overcoiling, normocoiling, and undercoiling subgroups was 0.63.
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DISCUSSION |
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Measuring the umbilical coiling index is not always easy, especially in cords with a very irregular coiling pattern, and especially when blood has been drained from the cord. We found that the statistic for categorical classification indicated only modest agreement. It seemed to be predominantly due to disagreement on cases with an umbilical coiling index just under or above the 10th percentile. Because reproducibility between observers was not excellent, the magnitude of the true relationships between undercoiling and adverse outcome may have been underestimated in our study. Another possible limitation of our study, and of most other studies to date as well, is that we were unable to study the part of the umbilical cord that remained attached to the neonate. The density of umbilical coiling is often a little higher near the fetal end than near the placental end,1 and the length of umbilical cord remaining attached to the neonate may vary depending on the condition of the newborn. This potential bias, however, is likely to have weakened rather than strengthened the relations we found between overcoiling on the one hand and small for gestational age infants, fetal death, low umbilical arterial pH, and asphyxia on the other.
Our mean umbilical coiling index was slightly lower than the mean umbilical coiling index in several other studies,7,8,10 which may have been due to differences between study protocols. We studied unclamped cords. If the cord is clamped at both sides, the umbilical coiling index is slightly overestimated as compared with the umbilical coiling index in the same, unclamped cord.
Because both overcoiling and undercoiling of the umbilical cord are associated with adverse pregnancy outcome, there seems to be a window of optimal coiling. Why is the degree of coiling of the umbilical cord of importance to the well-being of the fetus? One obvious benefit of a coiled cord is its enhanced capacity to withstand kinking, compression and torsion, which can be demonstrated in a telephone receiver cord. The coils may make the cord more resistant to kinking and compression, but under a tight encirclement force (as in nuchal cords), the opposite occurs. In an experiment by Georgiou et al17 in which venous perfusion was measured in cords subjected to a standardized tight encirclement force, a significant inverse relationship was found between coiling index and the minimum weight required to occlude venous perfusion.
So undercoiling may give way to kinking and compression, whereas overcoiling may give way to occlusion in cases with cord entanglement. This may help to explain the association with low Apgar score in undercoiled cords, and with low arterial pH and asphyxia in overcoiled cords.
Another mechanism that may explain why umbilical coiling is beneficial has been proposed by Reynolds.18,19 The close association between the umbilical arteries and vein raise the possibility of a dynamic interaction between these vessels. The fetal blood flows through the umbilical vein, pumped by slight but definitive decreases and increases in venous pressure, caused by adjacent arterial pressure pulses. The arterial coils around the vein along the length provide multiple variations of pressure in an additive fashion, so if the number of coils increases, the effect is larger. This is supported by a study by Degani et al20 who found a linear relationship between the coiling index and venous flow. In cases with overcoiling the effect of the arterial pressure pulses may be opposed by increased turbulence in the vessels and compression of the vein.
The higher incidence of preterm delivery may have another cause. Preterm delivery seems to be associated with chorioamnionitis. Although we did not find a significant association with chorioamnionitis in our present study, it was found in a previous study of a selected population with adverse pregnancy outcome.6 The authors proposed that in undercoiled cords the stroma may be less turgid than in normal cords.6 This property of the stroma may be related to the strength of the chorionic and amniotic membranes and to the susceptibility to intrauterine infection and therefore preterm delivery.
Undercoiling or overcoiling occurs more often in cords with other abnormalities, such as single umbilical artery and velamentous insertion, which are also associated with adverse pregnancy outcome.21,22 Despite all associations we found, it was intriguing to find that even with extremely undercoiled and overcoiled cords, some mothers gave birth to a healthy infant after an uneventful pregnancy. Because both undercoiling and overcoiling are associated with adverse pregnancy outcome, we recommend that determination of the umbilical coiling index be included as a routine part of placental pathologic examination. Furthermore, an attractive hypothesis is that antenatal detection of cord abnormalities with ultrasonography may be helpful in selecting cases in which strict fetal monitoring is warranted, antenatally as well as intrapartum. If the umbilical coiling index can be measured reliably in utero by ultrasound, then it might be a promising prognostic marker for adverse pregnancy outcome. This deserves to be tested in further studies.
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Footnotes |
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doi:10.1097/01.AOG.0000209197.84185.15
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REFERENCES |
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20. Degani S, Lewinsky RM, Berger H, Spiegel D. Sonographic estimation of umbilical coiling index and correlation with Doppler flow characteristics. Obstet Gynecol 1995;86:990–3.[Abstract]
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