European Journal of Radiology 81 (2012) e123e125

Contents lists available at ScienceDirect

European Journal of Radiology

journal homepage: www.elsevier.com/locate/ejrad

The effect of nuchal cord on nuchal fold thickness measured in the second trimester
Esra zkavukcu , Nuray Halilo lu g
Ankara University School of Medicine, Turkey

a r t i c l e

i n f o

a b s t r a c t
Purpose: To nd out whether nuchal cord causes an effect on the nuchal skin fold thickness (NFT) measurements, or not. Patients and methods: A total of 242 fetuses with normal outcomes that had undergone detailed second trimester US scan between 18 and 24 weeks of gestation were included in the study. NFT measurements were made on axial cranial US images passing through the cerebellum and cavum septi pellucidum. To detect nuchal cord, color Doppler imaging was performed on the axial views of the fetal neck. To investigate the differences in NFT measurements of the fetuses with or without nuchal cord, statistical analysis was performed using MannWhitney test. P < 0.05 was considered statistically signicant. Results: The study group was divided into two groups: nuchal cord (+) (n: 26) and nuchal cord () (n: 216) fetuses. Mean NFT measurements were 4.66 0.64 mm and 4.36 0.79 mm for nuchal cord (+) and nuchal cord () fetuses, respectively. Median NFT measurement for nuchal cord (+) fetuses was 4.6 mm, whereas it was 4.4 mm for nuchal cord () fetuses. Statistically signicant difference was denoted between two groups, in terms of NFT measurements (P = 0.049). Conclusion: NFT measurements of fetuses with nuchal cord are higher than the NFT measurements of fetuses without nuchal cord. One can conclude that the nuchal cord (+) fetuses with no other anomalies but increased NFT should be re-scanned to see if the increased NFT resolves in the absence of nuchal cord. 2011 Elsevier Ireland Ltd. All rights reserved.

Article history: Received 30 November 2010 Accepted 28 December 2010 Keywords: Nuchal cord Nuchal skin fold thickness Ultrasound

1. Introduction Nuchal cord or so-called cord around neck is a frequent incidental nding during pregnancy [13]. The term nuchal cord infers to the umbilical cord that encircles the fetal neck. Its incidence is controversial, probably depending on the gestational age [1] and the ultrasound (US) method used (2D vs. 3D) [3]. Nuchal cord is generally accepted as a benign nding [2]. The aim of this study was to nd out whether this benign condition, i.e. nuchal cord causes an effect on the nuchal skin fold thickness (NFT) measured in the second trimester of the pregnancy, or not. 2. Patients and methods Study group consisted of 242 pregnant women who referred to the radiology department for detailed second trimester US scan

Corresponding author at: Ankara niversitesi Tp Fakltesi Cebeci Hastanesi, Radyoloji Blm, 06100, Dikimevi, Ankara, Turkey. Tel.: +90 312 5956781. E-mail addresses: eozkavukcu@gmail.com (E. zkavukcu), nurayunsal2@hotmail.com (N. Halilo lu). g 0720-048X/$ see front matter 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2010.12.090

between November 2009 and February 2010. All US examinations were performed between 18 and 24 weeks of gestation, by the same observer. Only singleton pregnancies were included in the study. Fetuses with enlarged NFT, or major congenital anomalies were not enrolled in the study either. Fetuses with normal US scans, and normal physical examinations right after birth were accepted as normal and included in the study. All US examinations were performed using a SSA 770A ultrasound system (Toshiba, Tokyo, Japan) with a 3.5 MHz curvilinear transducer. During US scan, NFT measurements were made on axial cranial US images passing through the cerebellum and cavum septi pellucidum. NFT was measured from the outside of the external table of the occipital bone to the outer edge of outlying skin. To increase the accuracy of the measurement, NFT was measured at least two times. Then, the optimum images with the measurements were reviewed and the maximum NFT measurement was recorded as the nal one. During all US scans, special attention was paid for the presence of nuchal cord. An umbilical cord completely encircling the fetal neck was accepted as nuchal cord. To detect nuchal cord, color Doppler or dynamic ow imaging were performed on the axial views of the fetal neck. Once nuchal cord was conrmed, NFT was always measured above the level of nuchal cord (Fig. 1).

e124

E. zkavukcu, N. Halilo lu / European Journal of Radiology 81 (2012) e123e125 g

To investigate the differences in NFT measurements of the fetuses with or without nuchal cord, statistical analysis was performed with SPSS version 15.0 (SPSS Inc., Chicago, IL, USA) using MannWhitney test. P < 0.05 was considered statistically signicant. 3. Results Among all fetuses enrolled in the study (n: 242), 26 fetuses with nuchal cord were detected (10.74%). The study group was divided into two groups: nuchal cord (+) (n: 26) and nuchal cord () (n: 216) fetuses. All nuchal cord (+) fetuses had a single loop around their neck, except the two fetuses that had double loops. NFT measurements ranged between 3.56 mm and 2.36 mm, in nuchal cord (+) and nuchal cord () fetuses, respectively. Mean NFT measurements were 4.66 0.64 mm and 4.36 0.79 mm for nuchal cord (+) and nuchal cord () fetuses, respectively. Median NFT measurement for nuchal cord (+) fetuses was 4.6 mm, whereas it was 4.4 mm for nuchal cord () fetuses. Using MannWhitney test, statistically signicant difference was denoted between nuchal cord (+) and nuchal cord () groups, in terms of NFT measurements (P = 0.049). 4. Discussion Thanks to the improvement in US machines and the widespread usage of US, the antenatal detection rate of nuchal cord is increasing progressively. However, the detection of nuchal cord by US scans can cause anxiety in both the expectant mother and the doctor [2]. Despite the older studies which demonstrated associations between nuchal cord and maternal or neonatal morbidity, recent studies showed that the nuchal cord is not associated with adverse perinatal outcome and fetal compromise [1,2]. Thus, informing the patient about this probably negligible US nding is still debatable [2]. Although the antenatal incidence of nuchal cord is controversial, one well-known factor inuencing its incidence is the gestational age [1]. Clapp et al., showed an incidence of nuchal cord ranging between 12 and 37%, rising with advancing gestational age [1]. Another possible major factor that may inuence the incidence of nuchal cord is the method used for the US scan [3]. For example, in their study group consisting of fetuses between 10 and 14 weeks of gestational age, Schaefer et al. reported a nuchal cord incidence of 8% using two dimensional US [4], whereas Tepper et al, reported a much higher incidence between 13 and 16 weeks [3]. We used two-dimensional US, combined with color Doppler imaging, and our study group consisted of fetuses between 18 and 24 weeks of gestational age. Considering the US method we used and the gestational age of our patients, the incidence of nuchal cord (10.74%) that we found is quite consistent with the previous reports. In our opinion, realizing the presence of a nuchal cord during routine twodimensional US scanning is not that easy, unless special attention is paid and color Doppler imaging is used. Nuchal cord can lead to an increase in the nuchal translucency (NT) and NFT measurements, in the rst and second trimesters of the pregnancy, respectively [47]. Nuchal cord can cause indentation of the fetal skin, in this way it can cause displacement of the uid in the fetal neck leading to alteration of the NT measurement [5]. Other possible mechanisms that might explain the increased NT measurements of nuchal cord (+) fetuses are the alterations in the lymphatic drainage and transient heart failure due to umbilical cord compression [6]. Maymon et al. claimed that the nuchal cord could be the cause of the transient increased NT thickness in their two cases, with no other fetal anatomical or chromosomal anomalies [6]. Schaefer et al. and Scheier et al. both investigated the impor-

Fig. 1. (ac) Sagittal (a) and axial (b) plane color Doppler US views of a fetus with a gestational age of 22 weeks and 4 days show the double loop nuchal cord around the fetal neck (arrows). On the axial transcerebellar US view (c) of the same patient passing through the cavum septum pellucidum and thalami, nuchal skin fold thickness is measured as 5.6 mm (arrowheads).

E. zkavukcu, N. Halilo lu / European Journal of Radiology 81 (2012) e123e125 g

e125

tance of nuchal cord in the measurement of NT in rst trimester [4,5]. Schaefer et al. pointed out that if the umbilical cord is measured together with NT, this adds a mean of 0.8 mm to the actual NT measurement. Therefore, the nuchal cord should not be included in NT measurements, so as not to lead a false-positive diagnosis and unnecessary invasive testing [4]. On the other hand, Scheier et al. claim that the nuchal cord causes unpredictable changes in the NT measurement and true NT cannot be predicted accurately when the NT is measured in the presence of a nuchal cord [5]. They suggest repeating the US scan after a few hours, to measure the true NT in the absence of nuchal cord [5]. In this study, we did not repeat the examination to see if the NFT measurement changes when the nuchal cord is gone. In fact, it would truly be wise to repeat the examination in the fetuses with enlarged NT or NFT accompanied by nuchal cord. Lee et al., studied the effects of gestational age, cephalic index, fetal presentation, and nuchal cord on NFT measurements. They formulated a regression equation on the basis of these variables, to calculate the actual NFT. They showed that the fetuses with nuchal cord has a mean NFT of 5.92 (1.03), whereas fetuses without nuchal cord has a mean NFT of 4.85 (1.29), with a P value of 0.0001 [7]. This statistical difference is quite higher than the difference we found in our study. Our US scans were done by a single, experienced observer, and although nuchal cord can increase NFT measurements, we do not think that this effect is that strong. 5. Conclusions NFT measurement is an important US parameter in the antenatal diagnosis of Down syndrome. The presence of nuchal cord might lead to an increased NFT. Considering that the nuchal cord is a quite

frequent US nding, for the fetuses with increased NFT measurements, color Doppler imaging of the fetal neck should be done, in order to exclude nuchal cord. Although fetuses with increased NFT measurements were not enrolled in this study, one can conclude that in the presence of nuchal cord, fetuses with no other anomalies but increased NFT measurements should be re-scanned to see if the increased NFT resolves in the absence of nuchal cord. This might reduce the false-positive screening results that lead to unnecessary invasive testing. Conict of interest There are no conict of interests. References
[1] Clapp 3rd JF, Stepanchak W, Hashimoto K, Ehrenberg H, Lopez B. The natural history of antenatal nuchal cords. Am J Obstet Gynecol 2003;189(2):488 93. [2] Sheiner E, Abramowicz JS, Levy A, Silberstein T, Mazor M, Hershkovitz R. Nuchal cord is not associated with adverse perinatal outcome. Arch Gynecol Obstet 2006;274(2):813. [3] Tepper R, Kidron D, Aviram R, Markovitch O, Hershkovitz R. High incidence of cord entanglement during early pregnancy detected by three-dimensional sonography. Am J Perinatol 2009;26(5):37982. [4] Schaefer M, Laurichesse-Delmas H, Ville Y. The effect of nuchal cord on nuchal translucency measurement at 1014 weeks. Ultrasound Obstet Gynecol 1998;11(4):2713. [5] Scheier M, Egle D, Himmel I, et al. Impact of nuchal cord on measurement of fetal nuchal translucency thickness. Ultrasound Obstet Gynecol 2007;30(2):197 200. [6] Maymon R, Herman A, Dreazen E, Tovbin Y, Bukovsky I, Weinraub Z. Can nuchal cord cause transient increased nuchal translucency thickness? Hum Reprod 1999;14(2):5569 [Erratum in: Hum Reprod 1999;14(4):1140]. [7] Lee PR, Won HS, Chung JY, Shin HJ, Kim A. The variables affecting nuchal skin-fold thickness in mid-trimester. Prenat Diagn 2003;23(1):604.