European Journal of Obstetrics & Gynecology and Reproductive Biology 123 (2005) 188192 www.elsevier.

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Nuchal cord detected by ultrasound at term is associated with mode of delivery and perinatal outcome
E. Assimakopoulos a,*, M. Zafrakas a, P. Garmiris b, D.G. Goulis a, A.P. Athanasiadis a, K. Dragoumis a, J. Bontis a
a

1st Department of Obstetrics and Gynaecology, Aristotle University of Thessaloniki, Papageorgiou General Hospital, D. Gounari 8, 54621 Thessaloniki, Greece b Department of Obstetrics and Gynaecology, General District Hospital of Chalkidiki, Polygyros, Greece Received 3 December 2003; received in revised form 8 January 2005; accepted 26 February 2005

Abstract Objectives: To evaluate the clinical relevance of nuchal cord in normal, vertex, singleton pregnancies at term, and its effect on mode of delivery and perinatal outcome. Study design: Prospective study with 352 normal, singleton pregnancies, with fetuses in the vertex presentation, examined with real-time ultrasound at 3739 weeks. Health care workers at labour and delivery blinded to previous detection of nuchal cord. Results: Fetuses of nulliparous women with a nuchal cord were more likely to be delivered with operative vaginal or caesarean delivery (n = 153, p < 0.0001). This was not the case with higher parity (n = 199, p = 0.07). There was no difference between nuchal cord (n = 144) and control groups (n = 208) in amniotic uid quantity at 3739 weeks ( p = 0.554) or intrapartum CTG ( p = 0.9). On the other hand, nuchal cord group had lower Apgar scores at 1 and 5 min ( p = 0.001 and 0.027 respectively); this difference remained signicant when adjusted for birth weight ( p = 0.001 and 0.016), but disappeared when adjusted for mode of delivery ( p = 0.048 and 0.319). Conclusions: Nuchal cord in normal pregnancies at term is associated with increased rate of operative vaginal and caesarean delivery in nulliparae. The presence of a nuchal cord results in slightly lower Apgar scores at 1 and 5 min, mainly as a consequence of higher operative delivery rates. # 2005 Elsevier Ireland Ltd. All rights reserved.
Keywords: Nuchal cord; Normal pregnancies; Mode of delivery; Perinatal outcome

1. Introduction Loops of umbilical cord around the neck are common and the incidence of entanglement of the umbilical cord around the neck has been reported to be between 15.8 and 30% [1,2]. The incidence of single, double, triple and quadruple nuchal cord(s) at delivery has been reported to be 10.6, 2.5, 0.5 and 0.1%, respectively [3,4]. Coiling around the neck accounts for 7080% of all cord complications noticed at delivery [5]. Nuchal cords have been reported as early as the rst trimester [6], but they are generally rare before midgestation because the cord at that
* Corresponding author. Tel.: +30 2310 279292. E-mail address: mpontis@auth.gr (E. Assimakopoulos).

time is shorter than the body. The frequency of nuchal cords increases linearly from 20 weeks gestation onwards, regardless of whether the entanglement involves a single or multiple loops; after 38 weeks the frequency increases steeply [79]. It has been reported that nuchal cords, diagnosed prenatally with ultrasonographic imaging, may resolve spontaneously, especially before 36 weeks gestation [10]. The clinical signicance of a nuchal cord is controversial. Although in many cases it does not seem to do any harm, it has been reported to be associated with an increased risk of variable decelerations in both the rst and second stages of labour, acidemia, signicantly higher incidences of low 1 min Apgar score, meconium-stained amniotic uid, emergency caesarean section, need for neonatal resuscita-

0301-2115/$ see front matter # 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejogrb.2005.02.026

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tion and admission to the neonatal intensive care unit, and possibly, perinatal death [1114]. We conducted a prospective study in normal, singleton pregnancies, in the vertex presentation, at 3739 weeks gestation, in order to evaluate the clinical relevance of a nuchal cord and to determine whether the presence of a nuchal cord detected by two-dimensional ultrasound could predict the mode of delivery and perinatal outcome.

2. Study design The study population comprised 352 normal singleton pregnancies, which were studied prospectively. There were 153 nulliparae (43.5%), 127 primiparae (36.1%), 54 parae-II (15.3%) and 18 women of higher parity. All pregnant women received antepartum care and subsequently delivered at the Department of Obstetrics and Gynaecology of the General District Hospital of Chalkidiki, at Polygyros, Greece. Fetal presentation was vertex in all 352 pregnancies. Gestational age was estimated from the rst day of the last menstrual period. Women with history of previous caesarean section or uterine surgery were excluded, as well as women with medical problems in the current pregnancy, in particular diabetes mellitus, hypertension, cardiac disease, renal disease, and women under any sort of medication or drugs. All women were examined by ultrasound at 38 1 weeks gestation by the same operator (PG). A real-time ultrasonographic device (SCANNER 900, Pie Data Medical, Holland) was used. The presence or absence of a nuchal cord was documented sonographically. The amniotic uid quantity was estimated with measurement of the length of

the maximum vertical pocket of amniotic uid without limbs or umbilical cord. A maximum vertical pocket of amniotic uid between 3 and 8 cm was considered normal, whereas for values above 8 cm and below 3 cm the amniotic uid quantity was considered increased and decreased respectively. The presence of a nuchal cord was determined by real-time ultrasound as follows: the ultrasound transducer was placed parallel to the longitudinal axis of the fetal neck and the presence of a nuchal cord was visualised as a single or as multiple coils around the fetal neck, according to the number of cord entanglements. In Fig. 1 a representative picture of nuchal cord detection by real-time ultrasound is presented. Ultrasound examination at 38 1 weeks was preceded by history and typical clinical evaluation, including assessment of Bishop score and NST. All women delivered at the Department for Obstetrics and Gynaecology of the General District Hospital of Chalkidiki, under supervision of health care providers routinely working for the Department. These providers were blinded to the ultrasonographic ndings documented at 38 1 weeks. Patients and their relatives were blinded to sonographic ndings as well. Intrapartum routine care included electronic FHR monitoring. Women were followed-up in respect to the following parameters: mode of delivery (normal or operative vaginal or caesarean section), intrapartum CTG, and Apgar scores at 1 and 5 min. There were no neonates with congenital malformations or genetic disorders. All antenatal and postnatal data were entered into an electronic database (Microsoft Access1 1997). Data were described as mean and standard error of the mean (SEM). In order to compare nuchal cord and non-nuchal cord groups t-test was used for numerical and x2 or Fishers exact test for

Fig. 1. A representative picture showing detection of nuchal cord with real-time ultrasound device.

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E. Assimakopoulos et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 123 (2005) 188192 Table 2 Amniotic uid quantity according to presence of nuchal cord Amniotic uid quantity Normal (38 cm) Increased (>8 cm) Decreased (<3 cm) Total
a

categorical parameters. The ANCOVA test was used for analysis of co-variate parameters. A p value of less than 0.05 was considered statistically signicant. SPSS for Windows1 version 11 (SPSS Inc., Illinois, USA) was used for statistical analysis.

NC (%)a 122 (84.7) 2 (1.4) 20 (13.9) 144

Non-NC (%) 173 (83.2) 1 (0.5) 34 (16.3) 208

Total 295 3 54 352

3. Results Nuchal cord was detected by two-dimensional ultrasound at 38 1 weeks gestation in 144 out of 352 pregnancies. The mode of delivery was as follows: normal vaginal delivery in 275, operative vaginal delivery in 59 and caesarean section in 18 cases. Standard indications for operative vaginal and caesarean delivery were used. Detection of a nuchal cord was not used as an indication for operative delivery, since health care providers at labour were blinded to the ultrasonographic ndings documented at 38 1 weeks. There was a signicant difference between nuchal cord and non-nuchal cord groups regarding the mode of delivery, with operative vaginal delivery and caesarean section being more common in the nuchal cord group (x2-test, p < 0.0001). In a further sub-analysis, this difference remained signicant for nulliparae (n = 153, x2-test, p < 0.0001), but not for parous women (n = 199, x2-test, p = 0.07). The mode of delivery of fetuses according to presence of nuchal cord and parity is presented in Table 1. No signicant difference was found between the amniotic uid quantity, measured prenatally at 38 1 weeks, and the presence of a nuchal cord (x2-test, p = 0.554), (Table 2). There was also no difference between the nuchal cord and non-nuchal cord groups in respect to intrapartum CTG (x2test, p = 0.9), (Table 3). There were statistically differences between nuchal cord and non-nuchal cord groups in respect to Apgar scores at 1 min (7.9 0.1 versus 8.3 0.1, t-test, p = 0.001) and 5 min (9.2 0.1 versus 9.5 0.1, p = 0.027), and birth weight (3456.5 33.4 versus 3360.5 29.5, p = 0.034). After correction of Apgar scores at 1 and 5 min for birth weight, the difference between nuchal and non-nuchal cord
Table 1 Mode of delivery, according to parity and presence of nuchal cord Mode of delivery Parae 0 NC (%) a NVD OVD CS Total cases 23 (25.0) 27 (58.7) 11 (73.3) 61 (39.9) Non-NC (%) 69 (75.0) 19 (41.3) 4 (26.7) 92 (60.1) Parae 1 NC (%)b 43 (37.1) 6 (66.7) 1 (50.0) 50 (39.4) Non-NC (%) 73 (62.9) 3 (33.3) 1 (50.0) 77 (60.6)

NC vs. non-NC: x2-test, p = 0.55, NC = nuchal cord.

Table 3 Intrapartum CTG, according to presence of nuchal cord Intrapartum CTG Reassuring Non-reassuring Total
a

NC (%) a 124 (86.1) 20 (13.9) 144

Non-NC (%) 178 (85.6) 30 (14.4) 208

Total 302 50 352

NC vs. non-NC: x2-test, p = 0.90, NC: nuchal cord.

groups remained signicant (Apgar score at 1 min: 7.9 0.1 versus 8.3 0.1, ANCOVA, p = 0.001, Apgar score at 5 min 9.2 0.1 versus 9.5 0.1, p = 0.016). On the other hand, after correction of Apgar scores at 1 and 5 min for mode of delivery, the difference between nuchal and nonnuchal cord groups remained marginally signicant for Apgar score at 1 min (8.0 0.1 versus 8.2 0.1, ANCOVA, p = 0.048), and disappeared for Apgar score at 5 min (9.3 0.1 versus 9.4 0.1, p = 0.319). Conrmation of the presence of nuchal cord was made after delivery. There were 23 false positives and 21 false negatives results. Thus, detection of nuchal cord with twodimensional ultrasound had a sensitivity of 85% and a specicity of 89%.

4. Discussion The clinical signicance of a nuchal cord is controversial. Variable tightness of the nuchal cord [15], cords wrapped around the neck in a locked fashion or not [16], and multiple cord entanglements around the fetal neck [17] may be contributors to this controversy. It has been suggested that

Parae 2 NC (%) c 23 (44.2) 2 (100.0) 1 (100.0) 26 (47.3) Non-NC (%) 29 (55.8) 0 (0.0) 0 (0.0) 29 (52.7)

Parae > 2 NC (%) d 6 (40.0) 1 (50.0) 0 () 7 (41.2) Non-NC (%) 9 (60.0) 1 (50.0) 0 () 10 (58.8)

Totale

275 59 18 352

NC vs. non-NC: x2-test, NC: nuchal cord, NVD: normal vaginal delivery, OVD: operative vaginal delivery, CS: caesarean section. a p = 0.0001. b p = 0.21. c p = 0.17. d p = 0.04. e p = 0.0001.

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a moderately tight cord around the neck would impair cephalic venous blood ow only, whereas a very tight would compromise the umbilical circulation and produce systemic hypoxia, hypercapnia, and acidemia [18]. Sonographic detection of a nuchal cord was rstly reported in 1982 [5]. With two-dimensional ultrasound a high degree of suspicion is required in order not to miss the presence of a nuchal cord, even with the application of highresolution sonographic imaging. This is due to the sonolucent nature of the umbilical vessels [19]. In cases in which the diagnosis is uncertain, colour Doppler ultrasound or Doppler ow velocimetry can assist in conrming the diagnosis [13,15,20]. Furthermore, Doppler ow velocimetry may reveal abnormal waveforms of umbilical vessels in fetuses with a nuchal cord [20]. Thus, Doppler ow velocimetry of the umbilical vessels may be useful in the evaluation of fetuses with sonographic diagnosis of nuchal cord, and conversely, a nuchal cord should be considered as part of the differential diagnosis of abnormal Doppler velocimetry of the umbilical vessels [20]. Though the subjective assessment of the ease of visualization of a nuchal cord seems to be better with threedimensional sonography, 3D-imaging does not seem to provide more useful diagnostic information compared to two-dimensional or colour Doppler ultrasound for detecting nuchal cord in utero [21]. In the present study, the presence of a nuchal cord was detected prenatally, in normal, singleton cephalic fetuses at 3739 weeks gestation with the use of two-dimensional ultrasound. We found that fetuses with a nuchal cord were more likely to be delivered with operative vaginal delivery or caesarean section rather than normal vaginal delivery. In a further sub-analysis, this association was found only in nulliparous women, but not in women who had at least one previous delivery; this could be due to differences in the physiology of labour and delivery. Our results are generally in agreement with those of two previous studies [13,17]. Both studies included only singleton, cephalic fetuses from uncomplicated pregnancies at term. Jauniaux et al. [13] examined the antenatal, intrapartum, and neonatal records of 2650 neonates and found a signicantly higher incidence of emergency caesarean section in the nuchal cord group compared to controls. Larson et al. [17] examined the records of 8565 deliveries and found that the presence of multiple nuchal cord entanglements was associated with a greater need for operative vaginal delivery but not for caesarean section. It should be noted, that women in these two studies were not stratied, according to parity, the presence of nuchal cords was diagnosed postnatally, and that both studies were retrospective, while our study was conducted prospectively in a blind fashion. The tightness of the umbilical cord around the fetal neck could play a role in causing fetal distress, and the quantity of amniotic uid could theoretically inuence the tightness of the nuchal cord. We did not nd however any association between the presence of a nuchal cord and the amniotic uid

quantity. Strong et al. [22] demonstrated that, among 70 women delivering infants with nuchal cords, there were signicantly increased incidences of meconium-stained amniotic uid and of non-reassuring CTG-patterns in those patients who had intrapartum oligohydramnios. However, only normal pregnancies and no pregnancies with oligohydramnios were included in our study, and our study design did not include intrapartum estimation of amniotic uid quantity. We did not nd any association between the presence of a nuchal cord and a non-reassuring intrapartum CTG. Our results are in agreement with those of a previous study [15]; Qin et al. [15], studied prospectively 180 uncomplicated pregnancies in the vertex presentation during labour, and reported no signicant differences in pregnancy outcome in respect to evidence of fetal distress between the nuchal and non-nuchal cord groups. On the other hand, an increased risk of non-reassuring CTG-patterns [14,17,23,24], umbilical artery acidemia [23], and meconium-stained amniotic uid [1315] in the presence of a nuchal cord were found in previous studies; these studies were however based on postnatal and retrospective data. We also found that the presence of a nuchal cord was associated with low Apgar scores at 1 and 5 min. This association was also found after correction for birth weight, but was only marginally signicant for Apgar score at 1 min, and disappeared for Apgar score at 5 min after correction for mode of delivery. Our results are generally in agreement with those of the following studies: Rhoades et al. [14] found a signicantly higher incidence of low Apgar score at 5 min in the nuchal cord group. Both Jauniaux et al. [13] and Larson et al. [17] found a signicantly higher incidence of low Apgar score at 1 min but not at 5 min in the nuchal cord groups compared with controls. In the former study [13], a higher incidence of need for neonatal resuscitation, and admission to the neonatal intensive care unit was found in the nuchal cord group, while in the latter [17] higher incidence of low umbilical artery pH was reported in the presence of multiple cord entanglements. Our results together with those of previous studies suggest that sonographic identication of nuchal cord may be an important observation during third trimester sonography. However, no denitive conclusions can be drawn concerning the optimal management of this clinical condition. This is not only due to the heterogeneity in reporting results concerning the mode of delivery and the perinatal outcome, but also due to the variability in studydesign and methods used in the diagnosis of nuchal cords. Future prospective studies using common methods and clinical end-points could lead to more rm conclusions. Though many would probably prefer not to verify the presence of a nuchal cord and not to inform the patient in order to avoid anxiety, others suggest that the presence of a nuchal cord should become an integral part of third trimester ultrasound, and that in such cases the patient should be guided to monitor fetal movements [19]. Such recommendations are very reasonable but caution is needed in order not

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E. Assimakopoulos et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 123 (2005) 188192 [11] Stembera ZK, Horska S. The inuence of coiling of the umbilical cord around the neck of the fetus on its gas metabolism and acidbase balance. Biol Neonate 1972;20:21425. [12] Tejani NA, Mann LI, Sanghavi M, Bhakthavathsalan A, Weiss RR. The association of umbilical cord complications and variable decelerations with acidbase ndings. Obstet Gynecol 1977;49: 15962. [13] Jauniaux E, Ramsay B, Peellaerts C, Scholler Y. Perinatal features of pregnancies complicated by nuchal cord. Am J Perinatol 1995; 12:2558. [14] Rhoades DA, Latza U, Mueller BA. Risk factors and outcomes associated with nuchal cord. A population-based study. J Reprod Med 1999;44:3945. [15] Qin Y, Wang CC, Lau TK, Rogers MS. Color ultrasonography: a useful technique in the identication of nuchal cord during labor. Ultrasound Obstet Gynecol 2000;15:4137. [16] Collins JH. Nuchal cord type A and type B. Am J Obstet Gynecol 1997;177:94. [17] Larson JD, Rayburn WF, Crosby S, Thurnau GR. Multiple nuchal cord entanglements and intrapartum complications. Am J Obstet Gynecol 1995;173:122831. [18] Arto-Medrano F. Inuence of cord around the neck on fetal acidbase balance in vigorous newborn infants. Am J Obstet Gynecol 1970;107:103543. [19] Sherer DM, Manning FA. Prenatal ultrasonographic diagnosis of nuchal cord(s): disregard, inform, monitor or intervene? Ultrasound Obstet Gynecol 1999;14:18. [20] Pilu G, Falco P, Guazzarini M, Sandri F, Bovicelli L. Sonographic demonstration of nuchal cord and abnormal umbilical artery waveform heralding fetal distress. Ultrasound Obstet Gynecol 1998;12: 1257. [21] Hanaoka U, Yanagihara T, Tanaka H, Hata T. Comparison of threedimensional, two-dimensional and color Doppler ultrasound in predicting the presence of a nuchal cord at birth. Ultrasound Obstet Gynecol 2002;19(5):4714. [22] Strong TH, Sarno A, Paul RH. Signicance of intrapartum amniotic uid volume in the presence of nuchal cords. J Reprod Med 1992;37:71820. [23] Hankins GD, Snyder RR, Hauth JC, Gilstrap 3rd LC, Hammond T. Nuchal cords and neonatal outcome. Obstet Gynecol 1987;70:68791. [24] Miser WF. Outcome of infants born with nuchal cords. J Fam Pract 1992;34:4415.

to cause unnecessary anxiety to the parents or lead to overtreatment in a condition in which no rm evidence exists. In conclusion, we found that the presence of a nuchal cord at term is related to an increased rate of operative delivery in nulliparae, but not in parous women. There was no association between the presence of a nuchal cord and amniotic uid quantity at 38 1 weeks or a non-reassuring intrapartum CTG. Apgar scores at 1 and 5 min were slightly lower in the presence of a nuchal cord, and this appeared to be largely a consequence of higher operative delivery rates in this group. References
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