Cervical strain elastography: pattern analysis and cervical sliding sign in preterm and control pregnancies
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Bianca Debring
, Mareike Möllers
Abstract
Objectives
The aim of this study was to assess the value of cervical strain elastography and Cervical Sliding Sign (CSS) for predicting spontaneous preterm birth (sPTB).
Methods
In our case-control study we performed an elastographic assessment of the cervix in 82 cases of preterm birth (preterm group) and 451 control pregnancies (control group) between the 20th and 37th week of gestation. We divided the anterior cervical lip first into two (“Intern2”, “Extern2”) and into three sectors (“Intern3”, “Middle3”, “Extern3”). The tissue deformation pattern after local compression with an ultrasound probe was recorded. We distinguished between an irregularly distributed (“Spotting”) and homogeneous pattern presentation. Additionally, the presence of a sliding of the anterior against the posterior cervical lip (positive CSS) during compression was evaluated. A logistic regression analysis and the Akaike Information Criterion (AIC) were used to estimate the probability of sPTB and to select a prediction model.
Results
Spotting and positive CSS occurred more frequently in the preterm group compared to control group (97.8 vs. 2.2%, p<0.001; 26.8 vs. 4.2%, p<0.001; respectively). The model with the parameters week of gestation at ultrasound examination, Intern3, Middle3 and CSS was calculated as the highest quality model for predicting sPTB. The AUC (Area Under the Curve) was higher for this parameter combination compared to cervical length (CL) (0.926 vs. 0.729).
Conclusions
Cervical strain elastography pattern analysis may be useful for the prediction of sPTB, as the combination of Spotting analysis and CSS is superior to CL measurement alone.
Acknowledgments
We thank everyone who voluntarily dedicated their time and effort.
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Research funding: None declared.
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Author contributions: B. Debring: data collection, data management, data analysis, manuscript writing. M. Möllers: data collection, manuscript editing. H.A. Köster: scientific consulting, manuscript editing. R. Kwiecien: statistics, manuscript editing. J. Braun: data collection, manuscript editing. K. Oelmeier: data collection, manuscript editing. W. Klockenbusch: data collection, manuscript editing. R. Schmitz: project construction, data collection, manuscript revision. All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
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Competing interests: Authors state no conflict of interest.
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Informed consent: Informed consent was obtained from all individual participants included in the study.
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Ethical approval: The study was designed according to the Declaration of Helsinki and was approved by the Institutional Ethics Board (2010-256-f-S and 2015-649-f-S).
References
1. Slattery, MM, Morrison, JJ. Preterm delivery. Lancet 2002;360:1489–97. https://doi.org/10.1016/s0140-6736(02)11476-0.Suche in Google Scholar
2. Beck, S, Wojdyla, D, Say, L, Betran, AP, Merialdi, M, Requejo, JH, et al.. The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ 2010;88:31–8. https://doi.org/10.2471/blt.08.062554.Suche in Google Scholar PubMed PubMed Central
3. Frey, HA, Klebanoff, MA. The epidemiology, etiology, and costs of preterm birth. Semin Fetal Neonatal Med 2016;21:68–73. https://doi.org/10.1016/j.siny.2015.12.011.Suche in Google Scholar PubMed
4. Petrou, S. Health economic aspects of late preterm and early term birth. Semin Fetal Neonatal Med 2019;24:18–26. https://doi.org/10.1016/j.siny.2018.09.004.Suche in Google Scholar PubMed
5. Iams, JD. Clinical practice. Prevention of preterm parturition. N Engl J Med 2014;370:254–61. https://doi.org/10.1056/nejmcp1103640.Suche in Google Scholar
6. Ville, Y, Rozenberg, P. Predictors of preterm birth. Best Pract Res Clin Obstet Gynaecol 2018;52:23–32. https://doi.org/10.1016/j.bpobgyn.2018.05.002.Suche in Google Scholar PubMed
7. Winkler, M, Rath, W. Changes in the cervical extracellular matrix during pregnancy and parturition. J Perinat Med 1999;27:45–60. https://doi.org/10.1515/jpm.1999.006.Suche in Google Scholar
8. Vink, J, Feltovich, H. Cervical etiology of spontaneous preterm birth. Semin Fetal Neonatal Med 2016;21:106–12. https://doi.org/10.1016/j.siny.2015.12.009.Suche in Google Scholar PubMed PubMed Central
9. Volpe, N, Schera, GBL, Dall’Asta, A, Di Pasquo, E, Ghi, T, Frusca, T. Cervical sliding sign: new sonographic marker to predict impending preterm delivery in women with uterine contractions. Ultrasound Obstet Gynecol 2019;54:557–8. https://doi.org/10.1002/uog.20395.Suche in Google Scholar PubMed
10. Palmeri, ML, Feltovich, H, Homyk, AD, Carlson, LC, Hall, T. Evaluating the feasibility of acoustic radiation force impulse shear wave elasticity imaging of the uterine cervix with an intracavity array: a simulation study. IEEE Trans Ultrason Ferroelectr Freq Control 2013;60:2053–64. https://doi.org/10.1109/tuffc.2013.2796.Suche in Google Scholar PubMed PubMed Central
11. Oturina, V, Hammer, K, Möllers, M, Braun, J, Falkenberg, MK, de Murcia, KO, et al.. Assessment of cervical elastography strain pattern and its association with preterm birth. J Perinat Med 2017;45:925–32. https://doi.org/10.1515/jpm-2016-0375.Suche in Google Scholar PubMed
12. Gesthuysen, A, Hammer, K, Möllers, M, Braun, J, de Murcia, KO, Falkenberg, MK, et al.. Evaluation of cervical elastography strain pattern to predict preterm birth. Ultraschall der Med 2020;41:397–403. https://doi.org/10.1055/a-0865-1711.Suche in Google Scholar PubMed
13. Köbbing, K, Fruscalzo, A, Hammer, K, Möllers, M, Falkenberg, M, Kwiecien, R, et al.. Quantitative elastography of the uterine cervix as a predictor of preterm delivery. J Perinatol 2014;34:774–80. https://doi.org/10.1038/jp.2014.87.Suche in Google Scholar PubMed
14. Hernandez-Andrade, E, Romero, R, Korzeniewski, SJ, Ahn, H, Aurioles-Garibay, A, Garcia, M, et al.. Cervical strain determined by ultrasound elastography and its association with spontaneous preterm delivery. J Perinat Med 2014;42:159–69. https://doi.org/10.1515/jpm-2013-0277.Suche in Google Scholar PubMed PubMed Central
15. Hernandez-Andrade, E, Garcia, M, Ahn, H, Korzeniewski, SJ, Saker, H, Yeo, L, et al.. Strain at the internal cervical os assessed with quasi-static elastography is associated with the risk of spontaneous preterm delivery at ≤34 weeks of gestation. J Perinat Med 2015;43:657–66. https://doi.org/10.1515/jpm-2014-0382.Suche in Google Scholar PubMed PubMed Central
16. Landis, JR, Koch, GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159–74. https://doi.org/10.2307/2529310.Suche in Google Scholar
17. Iams, JD, Goldenberg, RL, Meis, PJ, Mercer, BM, Moawad, A, Das, A, et al.. The length of the cervix and the risk of spontaneous premature delivery. N Engl J Med 1996;334:567–72. https://doi.org/10.1056/nejm199602293340904.Suche in Google Scholar PubMed
18. Berger, R, Abele, H, Bahlmann, F, Bedei, I, Doubek, K, Felderhoff-Müser, U, et al.. Prevention and therapy of preterm birth. Guideline of the DGGG, OEGGG and SGGG (S2k level, AWMF registry number 015/025, february 2019) – part 1 with recommendations on the epidemiology, etiology, prediction, primary and secondary prevention of preterm birth. Z Geburtshilfe Neonatol 2019;223:304–16. https://doi.org/10.1055/a-0979-1028.Suche in Google Scholar PubMed
19. Berghella, V, Saccone, G. Cervical assessment by ultrasound for preventing preterm delivery. Cochrane Database Syst Rev 2015;9:CD007235.Suche in Google Scholar
20. Word, RA, Li, XH, Hnat, M, Carrick, K. Dynamics of cervical remodeling during pregnancy and parturition: mechanisms and current concepts. Semin Reprod Med 2007;25:69–79. https://doi.org/10.1055/s-2006-956777.Suche in Google Scholar PubMed
21. Timmons, B, Akins, M, Mahendroo, M. Cervical remodeling during pregnancy and parturition. Trends Endocrinol Metab 2010;21:353–61. https://doi.org/10.1016/j.tem.2010.01.011.Suche in Google Scholar PubMed PubMed Central
22. House, M, Kaplan, DL, Socrate, S. Relationships between mechanical properties and extracellular matrix constituents of the cervical stroma during pregnancy. Semin Perinatol 2009;33:300–7. https://doi.org/10.1053/j.semperi.2009.06.002.Suche in Google Scholar PubMed PubMed Central
23. Feltovich, H, Hall, TJ, Berghella, V. Beyond cervical length: emerging technologies for assessing the pregnant cervix. Am J Obstet Gynecol 2012;207:345–54. https://doi.org/10.1016/j.ajog.2012.05.015.Suche in Google Scholar PubMed PubMed Central
24. Fruscalzo, A, Mazza, E, Feltovich, H, Schmitz, R. Cervical elastography during pregnancy: a critical review of current approaches with a focus on controversies and limitations. J Med Ultrason 2016;43:493–504. https://doi.org/10.1007/s10396-016-0723-z.Suche in Google Scholar PubMed
25. Yamaguchi, S, Kamei, Y, Kozuma, S, Taketani, Y. Tissue elastography imaging of the uterine cervix during pregnancy. J Med Ultrason 2007;34:209–10. https://doi.org/10.1007/s10396-007-0150-2.Suche in Google Scholar PubMed
26. Fuchs, T, Pomorski, M, Zimmer, M. Quantitative cervical elastography in pregnancy. Ultrasound Obstet Gynecol 2013;41:712. https://doi.org/10.1002/uog.12474.Suche in Google Scholar PubMed
27. Hernandez-Andrade, E, Hassan, SS, Ahn, H, Korzeniewski, SJ, Yeo, L, Chaiworapongsa, T, et al.. Evaluation of cervical stiffness during pregnancy using semiquantitative ultrasound elastography. Ultrasound Obstet Gynecol 2013;41:152–61. https://doi.org/10.1002/uog.12344.Suche in Google Scholar PubMed PubMed Central
28. Fruscalzo, A, Schmitz, R. Quantitative cervical elastography in pregnancy. Ultrasound Obstet Gynecol 2012;40:612. https://doi.org/10.1002/uog.12320.Suche in Google Scholar PubMed
29. Fruscalzo, A, Schmitz, R, Klockenbusch, W, Steinhard, J. Reliability of cervix elastography in the late first and second trimester of pregnancy. Ultraschall der Med 2012;33:E101–7. https://doi.org/10.1055/s-0031-1299330.Suche in Google Scholar PubMed
30. Fruscalzo, A, Steinhard, J, Londero, AP, Fröhlich, C, Bijnens, B, Klockenbusch, W, et al.. Reliability of quantitative elastography of the uterine cervix in at-term pregnancies. J Perinat Med 2013;41:421–7. https://doi.org/10.1515/jpm-2012-0180.Suche in Google Scholar PubMed
31. Fruscalzo, A, Londero, AP, Fröhlich, C, Möllmann, U, Schmitz, R. Quantitative elastography for cervical stiffness assessment during pregnancy. BioMed Res Int 2014;2014:826535. https://doi.org/10.1155/2014/826535.Suche in Google Scholar PubMed PubMed Central
32. Molina, FS, Gómez, LF, Florido, J, Padilla, MC, Nicolaides, KH. Quantification of cervical elastography: a reproducibility study. Ultrasound Obstet Gynecol 2012;39:685–9. https://doi.org/10.1002/uog.11067.Suche in Google Scholar PubMed
33. Fruscalzo, A, Londero, AP, Schmitz, R. Quantitative cervical elastography during pregnancy: influence of setting features on strain calculation. J Med Ultrason 2015;42:387–94. https://doi.org/10.1007/s10396-015-0619-3.Suche in Google Scholar PubMed
34. Wozniak, S, Czuczwar, P, Szkodziak, P, Milart, P, Wozniakowska, E, Paszkowski, T. Elastography in predicting preterm delivery in asymptomatic, low-risk women: a prospective observational study. BMC Pregnancy Childbirth 2014;14:238. https://doi.org/10.1186/1471-2393-14-238.Suche in Google Scholar PubMed PubMed Central
35. Sabiani, L, Haumonte, JB, Loundou, A, Caro, AS, Brunet, J, Cocallemen, JF, et al.. Cervical HI-RTE elastography and pregnancy outcome: a prospective study. Eur J Obstet Gynecol Reprod Biol 2015;186:80–4. https://doi.org/10.1016/j.ejogrb.2015.01.016.Suche in Google Scholar PubMed
36. Jiang, L, Peng, L, Rong, M, Liu, X, Pang, Q, Li, H, et al.. Nomogram incorporating multimodal transvaginal ultrasound assessment at 20 to 24 Weeks’ gestation for predicting spontaneous preterm delivery in low-risk women. Int J Womens Health 2022;14:323–31. https://doi.org/10.2147/ijwh.s356167.Suche in Google Scholar
37. von Schöning, D, Fischer, T, von Tucher, E, Slowinski, T, Weichert, A, Henrich, W, et al.. Cervical sonoelastography for improving prediction of preterm birth compared with cervical length measurement and fetal fibronectin test. J Perinat Med 2015;43:531–6. https://doi.org/10.1515/jpm-2014-0356.Suche in Google Scholar PubMed
38. O’Hara, S, Zelesco, M, Sun, Z. Shear wave elastography on the uterine cervix: technical development for the transvaginal approach. J Ultrasound Med 2019;38:1049–60. https://doi.org/10.1002/jum.14793.Suche in Google Scholar PubMed
39. Peralta, L, Mourier, E, Richard, C, Charpigny, G, Larcher, T, Aït-Belkacem, D, et al.. Vivo evaluation of cervical stiffness evolution during induced ripening using shear wave elastography, histology and 2 photon excitation microscopy: insight from an animal model. PLoS One 2015;10:e0133377. https://doi.org/10.1371/journal.pone.0133377.Suche in Google Scholar PubMed PubMed Central
40. Carlson, LC, Romero, ST, Palmeri, ML, Del Rio, AM, Esplin, SM, Rotemberg, VM, et al.. Changes in shear wave speed pre- and post-induction of labor: a feasibility study. Ultrasound Obstet Gynecol 2015;46:93–8. https://doi.org/10.1002/uog.14663.Suche in Google Scholar PubMed PubMed Central
41. Muller, M, Aït-Belkacem, D, Hessabi, M, Gennisson, JL, Grangé, G, Goffinet, F, et al.. Assessment of the cervix in pregnant women using shear wave elastography: a feasibility study. Ultrasound Med Biol 2015;41:2789–97. https://doi.org/10.1016/j.ultrasmedbio.2015.06.020.Suche in Google Scholar PubMed
42. Hernandez-Andrade, E, Maymon, E, Luewan, S, Bhatti, G, Mehrmohammadi, M, Erez, O, et al.. A soft cervix, categorized by shear-wave elastography, in women with short or with normal cervical length at 18–24 weeks is associated with a higher prevalence of spontaneous preterm delivery. J Perinat Med 2018;46:489–501. https://doi.org/10.1515/jpm-2018-0062.Suche in Google Scholar PubMed PubMed Central
43. Suthasmalee, S, Moungmaithong, S. Cervical shear wave elastography as a predictor of preterm delivery during 18–24 weeks of pregnancy. J Obstet Gynaecol Res 2019;45:2158–68. https://doi.org/10.1111/jog.14094.Suche in Google Scholar PubMed
44. Yang, X, Ding, Y, Mei, J, Xiong, W, Wang, J, Huang, Z, et al.. Second-Trimester cervical shear wave elastography combined with cervical length for the prediction of spontaneous preterm birth. Ultrasound Med Biol 2022;48:820–29.10.1016/j.ultrasmedbio.2022.01.003Suche in Google Scholar PubMed
45. Park, HS, Kwon, H, Kwak, DW, Kim, MY, Seol, HJ, Hong, JS, et al.. Addition of cervical elastography may increase preterm delivery prediction performance in pregnant women with short cervix: a prospective study. J Korean Med 2019;34:e68. https://doi.org/10.3346/jkms.2019.34.e68.Suche in Google Scholar PubMed PubMed Central
46. Nazzaro, G, Saccone, G, Miranda, M, Crocetto, F, Zullo, F, Locci, M. Cervical elastography using E-cervix for prediction of preterm birth in singleton pregnancies with threatened preterm labor. J Matern Fetal Neonatal Med 2020;24:1–6.10.1080/14767058.2020.1716721Suche in Google Scholar PubMed
47. Zhang, L, Zheng, Q, Xie, H, Du, L, Wu, L, Lin, M. Quantitative cervical elastography: a new approach of cervical insufficiency prediction. Arch Gynecol Obstet 2020;301:207–15. https://doi.org/10.1007/s00404-019-05377-5.Suche in Google Scholar PubMed
48. Seol, HJ, Sung, JH, Seong, WJ, Kim, HM, Park, HS, Kwon, H, et al.. Standardization of measurement of cervical elastography, its reproducibility, and analysis of baseline clinical factors affecting elastographic parameters. Obstet Gynecol Sci 2020;63:42–54. https://doi.org/10.5468/ogs.2020.63.1.42.Suche in Google Scholar PubMed PubMed Central
49. Patberg, ET, Wells, M, Vahanian, SA, Zavala, J, Bhattacharya, S, Richmond, D, et al.. Use of cervical elastography at 18 to 22 weeks’ gestation in the prediction of spontaneous preterm birth. Am J Obstet Gynecol 2021;225:525.e1–9. https://doi.org/10.1016/j.ajog.2021.05.017.Suche in Google Scholar PubMed
50. Thomsen, CR, Jensen, MSS, Leonhard, AK, Mortensen, TØ, Bor, P, Sandager, P, et al.. A force-measuring device combined with ultrasound-based elastography for assessment of the uterine cervix. Acta Obstet Gynecol Scand 2022;101:241–7. https://doi.org/10.1111/aogs.14309.Suche in Google Scholar PubMed PubMed Central
© 2022 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Editorial
- A Celebration of Professor Joachim Dudenhausen
- Reviews
- Gestational complications associated with SARS-CoV-2 infection in pregnant women during 2020–2021: systematic review of longitudinal studies
- Eclampsia a preventable tragedy: an African overview
- Original Articles – Obstetrics
- How do bicornuate uteri alter pregnancy, intra-partum and neonatal risks? A population based study of more than three million deliveries and more than 6000 bicornuate uteri
- Maternal urogenital infection and fetal heart functional assessment – what is the missing link?
- Knowledge and attitudes of pregnant women on maternal immunization against COVID-19 in Croatia
- Retrospective review of GCT cutoff value based on pre-pregnancy BMI class in patients with GDM
- Cervical strain elastography: pattern analysis and cervical sliding sign in preterm and control pregnancies
- Maternal race/ethnicity impacts the success rates of external cephalic version (ECV) in the United States
- Fetal adrenal gland size and umbilical artery Doppler in growth-restricted fetuses
- Counseling pregnant women on calcium: effects on calcium intake
- Relationship among anogenital distance, adrenal gland volume, and penile length and width at 22–36 weeks of pregnancy
- Intra-amniotic inflammation in the mid-trimester of pregnancy is a risk factor for neuropsychological disorders in childhood
- Genetic amniocentesis using atraumatic 29 gauge needle in patients having a chorioamniotic separation
- YouTube as a source of patient information on external cephalic version
- Midwives’ personal and professional attitudes towards women’s delivery choices, interventions and neonatal care
- Maternal serum midkine level in fetal growth restriction: a case-control study
- Original Articles – Neonates
- Interventions for reducing late-onset sepsis in neonates: an umbrella review
- Maternal knowledge of recommendations for safe infant sleep and intentions for implementation – a cross sectional analysis of data from the KUNO-Kids birth cohort study
- Short Communication
- Lysophosphatidylcholine acyltransferase 1 protein is present in maternal blood in the third trimester and is upregulated by antenatal corticosteroids
- Letters to the Editor
- Peripartum hysterectomy at a tertiary university perinatal center – retrospective analysis of the 25-year period
- Neonate, infected mother and monkeypox: the present concern
Artikel in diesem Heft
- Frontmatter
- Editorial
- A Celebration of Professor Joachim Dudenhausen
- Reviews
- Gestational complications associated with SARS-CoV-2 infection in pregnant women during 2020–2021: systematic review of longitudinal studies
- Eclampsia a preventable tragedy: an African overview
- Original Articles – Obstetrics
- How do bicornuate uteri alter pregnancy, intra-partum and neonatal risks? A population based study of more than three million deliveries and more than 6000 bicornuate uteri
- Maternal urogenital infection and fetal heart functional assessment – what is the missing link?
- Knowledge and attitudes of pregnant women on maternal immunization against COVID-19 in Croatia
- Retrospective review of GCT cutoff value based on pre-pregnancy BMI class in patients with GDM
- Cervical strain elastography: pattern analysis and cervical sliding sign in preterm and control pregnancies
- Maternal race/ethnicity impacts the success rates of external cephalic version (ECV) in the United States
- Fetal adrenal gland size and umbilical artery Doppler in growth-restricted fetuses
- Counseling pregnant women on calcium: effects on calcium intake
- Relationship among anogenital distance, adrenal gland volume, and penile length and width at 22–36 weeks of pregnancy
- Intra-amniotic inflammation in the mid-trimester of pregnancy is a risk factor for neuropsychological disorders in childhood
- Genetic amniocentesis using atraumatic 29 gauge needle in patients having a chorioamniotic separation
- YouTube as a source of patient information on external cephalic version
- Midwives’ personal and professional attitudes towards women’s delivery choices, interventions and neonatal care
- Maternal serum midkine level in fetal growth restriction: a case-control study
- Original Articles – Neonates
- Interventions for reducing late-onset sepsis in neonates: an umbrella review
- Maternal knowledge of recommendations for safe infant sleep and intentions for implementation – a cross sectional analysis of data from the KUNO-Kids birth cohort study
- Short Communication
- Lysophosphatidylcholine acyltransferase 1 protein is present in maternal blood in the third trimester and is upregulated by antenatal corticosteroids
- Letters to the Editor
- Peripartum hysterectomy at a tertiary university perinatal center – retrospective analysis of the 25-year period
- Neonate, infected mother and monkeypox: the present concern