Ultrasound Obstet Gynecol 2015; 45: 358–362 Published online 29 January 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.14742

How to . . . . Practical advice on imaging-based techniques and investigations with accompanying slides and videoclips online

How to measure cervical length K. O. KAGAN* and J. SONEK†‡ *Department of Obstetrics and Gynaecology, University of Tubingen, Tubingen, Germany; †Fetal Medicine Foundation USA, Dayton, OH, ¨ ¨ USA; ‡Division of Maternal Fetal Medicine, Wright State University, Dayton, OH, USA

BACKGROUND Cervical-length measurement using transvaginal sonography (TVS) is an essential part of assessing the risk of preterm delivery. At mid-gestation, it provides a useful method with which to predict the likelihood of subsequent preterm birth in asymptomatic women. In women who present with threatened spontaneous preterm labor, TVS measurement of cervical length can help to distinguish between ‘true’ and ‘false’ spontaneous preterm labor. Additionally, there is some evidence that measurement of the cervix at the 11+0 to 13+6-week scan can help to establish the risk of preterm birth1,2 . To et al.3 reported on cervical-length measurement between 22 and 24 weeks’ gestation in 39 000 women with a singleton pregnancy. The cervical length was found to be distributed normally, with a mean length of 36 mm. In about 1% of the women, the length was 15 mm or less. This cut-off is generally used to define the high-risk group in interventional studies4 . In most studies focusing on asymptomatic twin pregnancies at 20 to 24 weeks, a cut-off of 25 mm is applied5 . Celik et al.6 used cervical-length measurements obtained between 20 and 24 weeks’ gestation, along with maternal history, in more than 58 000 women to create computed risk models for preterm delivery. They compared patients who delivered before 28 weeks, between 28 and 30 weeks, between 31 and 33 weeks, and between 34 and 36 weeks’ gestation. For a 10% false-positive rate, the sensitivities were 81%, 59%, 53% and 29%, respectively. In a Health Technology Assessment report, Honest et al.7 summarized the results of five studies that used cervical-length measurements between 20 and 24 weeks, with cut-offs of 20–30 mm, to predict preterm birth before 34 weeks’ gestation. The resultant positive likelihood ratios ranged from 2.3 for 30 mm to 7.6 for 20 mm.

It has been shown that only 15% of symptomatic patients presenting with preterm contractions will actually deliver within the next 7 days8 . Cervical length can be used to distinguish between ‘true’ and ‘false’ labor. Sotiriadis et al.9 summarized six studies, including about 1800 women, that assessed the risk for preterm delivery within 1 week, based on cervical length at the time of admission. With a cut-off of 15 mm, the sensitivity was about 60% for a false-positive rate of about 10%. The respective positive and negative likelihood ratios were 5.7 and 0.5. With cut-offs of 20 and 25 mm, the sensitivities increased to 75% and 80%, but at the expense of false-positive rates of 20% and 30%, respectively. Recent work10 has shown that cervical length at 11–13 weeks’ gestation, in combination with maternal history, can detect about half of the pregnancies that result in preterm delivery before 34 weeks, for a false-positive rate of 10%. However, the difference between the median cervical length of the normal group and that of the preterm-birth group was only 5 mm (32.5 mm vs 27.5 mm)10 , which raises doubts as to whether this technique can be used for general screening.

PRACTICAL POINTS There are essentially four methods that can be used to evaluate the uterine cervix: digital examination, transabdominal ultrasound, transperineal ultrasound (TPS) and TVS. It is the digital examination that provides the most comprehensive evaluation of the cervix, assessing dilatation, position, consistency and length. However, this examination suffers from being subjective. It is limited especially in its ability to establish accurately the cervical length. It also cannot detect reproducibly any changes at the internal cervical os and the upper portion of the cervical canal. Ultrasound, with its ability to penetrate the

¨ Correspondence to: Prof. K. O. Kagan, University of Tuebingen, Calwerstrasse 7, 72076 Tubingen, Germany (e-mail: [email protected])

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identify the internal, as well as the external, cervical ora. The external os is identified as the point at which the anterior and posterior lips of the cervix come together. Identification of the location of the internal os can be more challenging. In order to do so, the cervical mucosa must be identified. This is usually hypoechoic, with respect to the surrounding stroma, though occasionally it can be slightly hyperechoic. A thin line of demarcation between the stroma and the cervical mucosa can generally be identified on ultrasound. The point at which the cervical mucosa ends is considered to be the internal cervical os. Of note, the mucosa of the lower uterine segment is much thinner than is the cervical mucosa and is usually difficult to identify on ultrasound (Figure 4). Figure 1 Transvaginal ultrasound image of a normal cervix, showing the most commonly used method of cervical length measurement (double-headed arrow). In a curved cervix, the length is underestimated with a straight line. If the cervix is curved and the straight-line cervical length measurement is short, measurement obtained in two or more segments provides a more accurate estimation of length14 . However, in patients with a pathologically short cervix, the cervical canal will be straight and this adjustment in measurement technique is unnecessary.

cervical tissue and display its anatomy, makes an ideal modality with which to address both of these issues. Both TVS and TPS are performed with the patient in a dorsal lithotomy position. In order for the measurement to be accurate and reproducible, the following factors need to be taken into account (Figure 1 and Videoclip S1): Maternal bladder should be essentially empty The patient having a full bladder can increase artificially the cervical length. To et al.11 showed that the mean difference between cervical length measured when the patient’s bladder is empty and that measured when the bladder is full is about 4 mm. In addition, a full bladder can obscure the presence of cervical funneling by compressing the two halves of the funnel together (Figure 2). A longitudinal view of the cervix should be obtained The cervix should be measured along its longitudinal axis, which may be different from the patient’s longitudinal axis. The cervical canal, in most cases, is a fairly thin line. It may have a thin layer of hypoechoic contents. This is true especially in the third trimester. In all likelihood, it represents accumulation of mucus, and needs to be differentiated from a thin cervical funnel. This is best done by delineating the course of the fetal membranes: if they are not prolapsing into the cervical canal and are located at the level of the internal cervical os, the presence of a true funnel is unlikely (Figure 3). The cervical canal and surrounding cervical mucosa need to be identified In order to avoid inclusion of the isthmus into the cervical-length measurement, care must be taken to

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Magnification of the ultrasound image needs to be appropriate The image should be magnified sufficiently so that the morphology of the cervix is easily identifiable. The cervix should occupy approximately 50–75% of the image. Pressure from the probe on the cervix should be as little as possible If excessive pressure is applied on the cervix by the probe, the cervix appears artificially to be longer and the presence of a funnel will be obscured. Generally, in order to identify the relevant structures, it is helpful to put some pressure on the cervix initially. However, subsequently this should be reduced to the minimum that is required in order to view the cervix adequately (Videoclip S2). Duration of the examination should be 3–5 min The cervix is not a static structure and the length can vary, for example due to uterine contractions or to different positions of the patient (Videoclip S3). Therefore, sufficient time should be allowed for the examination to detect these changes. It may be helpful to press manually on the uterus or to ask the patient to push downwards to assess the cervical stability. Some even suggest that during the examination the patient stands, with the ultrasound probe inside the vagina. Several (at least three) measurements should be obtained during the course of the examination and the shortest measurement should be used for counseling. Calipers should be placed correctly Cervical measurement is obtained by placing calipers at the external and the internal ora (Figure 1). In 95% of cases, the difference between two measurements obtained by the same sonographer or by two different sonographers is about 4 mm12 . If there is funneling, the caliper should be placed at the apex of the funnel. If the cervix exceeds 25 mm in length, it will be curved in more than 50% of cases13 . The standard method of measurement, using a

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27mm

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Figure 2 Transvaginal ultrasound measurement of cervical length in the same patient, with a full bladder (a) and with an empty bladder (b).

Figure 3 Transvaginal ultrasound image of a cervix with accumulation of mucus. Amniotic membranes are indicated (arrow), showing that funneling is not present.

Figure 4 Transvaginal ultrasound image of a cervix, showing cervical mucosa as a homogeneous and hypoechoic structure compared to the surrounding stroma.

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd.

Figure 5 Transvaginal ultrasound image of a short cervix with funneling.

Figure 6 Transvaginal ultrasound image of amniotic fluid sludge (arrow).

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Figure 7 Transvaginal ultrasound Doppler image of vasa previa (a) and gray-scale image of placenta previa (b).

Figure 8 Transperineal (a) and transabdominal (b) ultrasound images of the cervix in the same patient. The cervical canal is indicated (arrows).

straight line between the internal and the external ora, will underestimate the cervical length in these cases. However, this is of little clinical significance as these patients are at low risk regardless of the exact measurement. In the high-risk group of patients with a cervical length < 16 mm, the cervix will always be a straight line. In the first trimester, the difference in cervical length between patients who are at risk for preterm birth and those who are not is extremely small; therefore, it would seem appropriate to correct for cervical curvature by obtaining the measurement either in segments or by tracing the canal14 .

logistic regression analysis that includes both funneling and cervical length, funneling has been shown not to be an independent risk factor for spontaneous preterm delivery17 . • Amniotic fluid sludge can be found as echogenic aggregates close to the internal os or within a funnel. This appears to be associated with microbial invasion of the amniotic cavity18,19 . Sludge is an independent risk factor for spontaneous preterm delivery, preterm rupture of membranes and histological chorioamnionitis in asymptomatic patients at high risk for spontaneous preterm delivery (Figure 6, Videoclip S4). • Vasa previa, placenta previa or low-lying placenta can be diagnosed20 (Figure 7).

Identification of additional significant findings at the time of the cervical scan

Other approaches

• Funneling, defined as protrusion of the amniotic membranes into the cervical canal, is considered by some as an additional risk factor for preterm delivery (Figure 5). Various criteria for the diagnosis of true funneling have been published15,16 . However, using a

In general, the cervix should be assessed by TVS. In cases in which this should be avoided, such as in those with preterm prelabor rupture of membranes, the cervical length can be measured by TPS: the transducer is placed on the perineum and rotated until the complete cervical

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canal and the internal and external ora can be identified. The placement of the probe is further away from the cervix than it is on TVS; therefore, there is a reduction in the detail in which the cervix is seen. In 95% of cases, the difference between TVS and TPS measurements is within ± 5 mm21 . Assessment of cervical length by TAS can be used as an initial evaluation but it should be borne in mind that, especially in cases with a short cervix, this modality tends to overestimate the true cervical length. Therefore, a proper risk assessment should be based on a TVS or TPS measurement (Figure 8).

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REFERENCES 1. Kagan KO, To M, Tsoi E, Nicolaides KH. Preterm birth: the value of sonographic measurement of cervical length. BJOG 2006; 113 (Suppl): 52–56. 2. Sonek J, Shellhaas C. Cervical sonography: a review. Ultrasound Obstet Gynecol 1998; 11: 71–78. 3. To MS, Skentou CA, Royston P, Yu CKH, Nicolaides KH. Prediction of patient-specific risk of early preterm delivery using maternal history and sonographic measurement of cervical length: a population-based prospective study. Ultrasound Obstet Gynecol 2006; 27: 362–367. 4. Fonseca EB, Celik E, Parra M, Singh M, Nicolaides KH, Fetal Medicine Foundation Second Trimester Screening Group. Progesterone and the risk of preterm birth among women with a short cervix. N Engl J Med 2007; 357: 462–469. 5. Conde-Agudelo A, Romero R, Hassan SS, Yeo, L. Transvaginal sonographic cervical length for the prediction of spontaneous preterm birth in twin pregnancies: a systematic review and meta-analysis. Am J Obstet Gyneco. 2010; 203: 128.e1–12. 6. Celik E, To M, Gajewska K, Smith GCS, Nicolaides KH, On behalf of the Fetal Medicine Foundation Second Trimester Screening Group. Cervical length and obstetric history predict spontaneous preterm birth: development and validation of a model to provide individualized risk assessment. Ultrasound Obstet Gynecol 2008; 31: 549–554. 7. Honest H, Forbes CA, Dur´ee KH, Norman G, Duffy SB, Tsourapas A, Roberts TE, Barton PM, Jowett SM, Hyde CJ, Khan KS. Screening to prevent spontaneous preterm birth: systematic reviews of accuracy and effectiveness literature with economic modelling. Health Technol Assess 2009; 13: 1–627. 8. Kenyon SL, Taylor DJ, Tarnow-Mordi W. Broad-spectrum antibiotics for spontaneous preterm labour: the ORACLE II randomised trial. Lancet 2001; 357(9261): 989–994. 9. Sotiriadis A, Papatheodorou S, Kavvadias A, Makrydimas G. Transvaginal cervical length measurement for prediction of

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preterm birth in women with threatened preterm labor: a meta-analysis. Ultrasound Obstet Gynecol 2010; 35: 54–64. Greco E, Gupta R, Syngelaki A, Poon LCY, Nicolaides KH. First-Trimester Screening for Spontaneous Preterm Delivery with Maternal Characteristics and Cervical Length. Fetal Diagn Ther 2012; 31: 154–161. To MS, Skentou C, Cicero S, Nicolaides KH. Cervical assessment at the routine 23-weeks’ scan: problems with transabdominal sonography. Ultrasound Obstet Gynecol 2000; 15: 292–296. Heath VC, Southall TR, Souka AP, Novakov A, Nicolaides KH. Cervical length at 23 weeks of gestation: relation to demographic characteristics and previous obstetric history. Ultrasound Obstet Gynecol 1998; 12: 304–311. To MS, Skentou C, Chan C, Zagaliki A, Nicolaides KH. Cervical assessment at the routine 23-week scan: standardizing techniques. Ultrasound Obstet Gynecol 2001; 17: 217–219. Retzke JD, Sonek JD, Lehmann J, Yazdi B, Kagan KO. Comparison of three methods of cervical measurement in the first trimester: single-line, two-line, and tracing. Prenat Diagn 2013. Rust OA, Atlas RO, Kimmel S, Roberts WE, Hess LW. Does the presence of a funnel increase the risk of adverse perinatal outcome in a patient with a short cervix? Am J Obstet Gynecol 2005; 192: 1060–1066. Grimes-Dennis J, Berghella V. Cervical length and prediction of preterm delivery. Current Opinion Obstet Gynecol 2007; 19: 191–195. Owen J, Yost N, Berghella V, Thom E, Swain M, Dildy GA, Miodovnik M, Langer O, Sibai B, McNellis D, National Institute of Child Health and Human Development, Maternal-Fetal Medicine Units Network. Mid-trimester endovaginal sonography in women at high risk for spontaneous preterm birth. JAMA 2001; 286: 1340–1348. Kusanovic JP, Espinoza J, Romero R, Gonc¸alves LF, Nien JK, Soto E, Khalek N, Camacho N, Hendler I, Mittal P, Friel LA, Gotsch F, Erez O, Than NG, Mazaki-Tovi S, Schoen ML, Hassan SS. Clinical significance of the presence of amniotic fluid ‘‘sludge’’ in asymptomatic patients at high risk for spontaneous preterm delivery. Ultrasound Obstet Gynecol 2007; 30: 706–714. Espinoza J, Gon alves LF, Romero R, Nien JK, Stites S, Kim YM, Hassan S, Gomez R, Yoon BH, Chaiworapongsa T, Lee W, Mazor M. The prevalence and clinical significance of amniotic fluid sludge in patients with preterm labor and intact membranes. Ultrasound Obstet Gynecol 2005; 25: 346–352. Oyelese Y, Smulian JC. Placenta previa, placenta accreta, and vasa previa. Obstet Gynecol 2006; 107: 927–941. Cicero S, Skentou C, Souka A, To MS, Nicolaides KH. Cervical length at 22–24 weeks of gestation: comparison of transvaginal and transperineal-translabial ultrasonography. Ultrasound Obstet Gynecol 2001; 17: 335–340.

Slides summarizing practical points, with accompanying illustrations and videoclips, are provided as supporting information online.

Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd.

Ultrasound Obstet Gynecol 2015; 45: 358–362.

How to measure cervical length.

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