Abstract
Background
This study aimed to analyze age-related changes in shear wave speed (SWS) of the normal uterine cervix.
Methods
We studied 362 women with a normal singleton pregnancy at 12–35 weeks’ gestation. The SWS of the cervix was measured using transvaginal ultrasonography at the internal os region of the anterior cervix (IOA), posterior cervix (IOP) and cervical canal (IOC), and at the external os region of the anterior cervix (EOA), posterior cervix (EOP) and cervical canal (EOC). The following parameters were analyzed: (1) time trend of SWS of the individual sampling points, (2) comparison of SWS in the internal cervical region and SWS in the external cervical region, and (3) comparison of SWS between the internal and external cervical regions. Statistical analyses were performed using mixed-effects models.
Results
The SWS of IOP decreased in bilinear regression, with a critical change in the rate at 22 weeks, whereas the SWS of the remaining points decreased linearly. The estimated values of SWS of IOP at 84, 154 and 251 days were higher than those of IOA and IOC (P<0.001). The estimated values of SWS of IOP at 84 and 154 days were higher than those of EOP (P<0.001). Significant differences between IOP and EOP were shown until 244 days (P<0.05). The estimated value of SWS of IOC at 84 days was higher than that of EOC (P<0.001). Significant differences between IOC and EOC were shown until 210 days (P<0.05).
Conclusion
The SWS of the uterine cervix in pregnancy decreases with advancing gestation. The SWS of IOP had the highest value among the sampling points with unique characteristics.
Acknowledgments
We thank Ellen Knapp, PhD, from the Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript. This study was supported in part by the Grant-in-Aid for Scientific Research (C) (JP18K09306).
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. 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;42:159–69.10.1515/jpm-2013-0277Search in Google Scholar PubMed PubMed Central
2. 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;43:657–66.10.1515/jpm-2014-0382Search in Google Scholar PubMed PubMed Central
3. Hwang HS, Sohn IS, Kwon HS. Imaging analysis of cervical elastography for prediction of successful induction of labor at term. J Ultrasound Med 2013;32:937–46.10.7863/ultra.32.6.937Search in Google Scholar PubMed
4. Pereira S, Frick AP, Poon LC, Zamprakou A, Nicolaides KH. Successful induction of labor: prediction by preinduction cervical length, angle of progression and cervical elastography. Ultrasound Obstet Gynecol 2014;44:468–75.10.1002/uog.13411Search in Google Scholar PubMed
5. Carlson LC, Romero ST, Palmeri ML, Muñoz Del Rio A, Esplin SM, Rotemberg VM, et al. Changes in shear wave speed pre- and post-induction of labor: a feasibility study. Ultrasound Obstet Gynecol 2015;46:93–8.10.1002/uog.14663Search in Google Scholar PubMed PubMed Central
6. Molina FS, Gómez LF, Florido J, Padilla MC, Nicolaides KH. Quantification of cervical elastography: a reproducibility study. Ultrasound Obstet Gynecol 2012;39:685–9.10.1002/uog.11067Search in Google Scholar PubMed
7. Nightingale K. Acoustic radiation force impulse (ARFI) imaging: a review. Curr Med Imaging Rev 2011;7:328–39.10.2174/157340511798038657Search in Google Scholar PubMed PubMed Central
8. Ferraioli G, Tinelli C, Zicchetti M, Above E, Poma G, Di Gregorio M, et al. Reproducibility of real-time shear wave elastography in the evaluation of liver elasticity. Eur J Radiol 2012;81:3102–6.10.1016/j.ejrad.2012.05.030Search in Google Scholar PubMed
9. Carlson LC, Feltovich H, Palmeri ML, Dahl JJ, Munoz del Rio A, Hall TJ. Estimation of shear wave speed in the human uterine cervix. Ultrasound Obstet Gynecol 2014;43:452–8.10.1002/uog.12555Search in Google Scholar PubMed PubMed Central
10. Hernandez-Andrade E, Aurioles-Garibay A, Garcia M, Korzeniewski SJ, Schwartz AG, Ahn H, et al. Effect of depth on shear-wave elastography estimated in the internal and external cervical os during pregnancy. J Perinat Med 2014;42:549–57.10.1515/jpm-2014-0073Search in Google Scholar PubMed PubMed Central
11. 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;41:2789–97.10.1016/j.ultrasmedbio.2015.06.020Search in Google Scholar PubMed
12. Peralta L, Molina FS, Melchor J, Gómez LF, Massó P, Florido J, et al. Transient elastography to assess the cervical ripening during pregnancy: a preliminary study. Ultraschall Med 2017;38:395–402.10.1055/s-0035-1553325Search in Google Scholar PubMed
13. Ono T, Katsura D, Yamada K, Hayashi K, Ishiko A, Tsuji S, et al. Use of ultrasound shear-wave elastography to evaluate change in cervical stiffness during pregnancy. J Obstet Gynaecol Res 2017;43:1405–10.10.1111/jog.13379Search in Google Scholar PubMed
14. Brown H, Prescott B. Applied mixed models in medicine. 3rd ed. Chichester: John Wiley & Sons; 2015.10.1002/9781118778210Search in Google Scholar
15. Naumova EN, Must A, Laird NM. Tutorial in biostatistics: evaluating the impact of ‘critical periods’ in longitudinal studies of growth using piecewise mixed effects models. Int J Epidemiol 2001;30:1332–41.10.1093/ije/30.6.1332Search in Google Scholar PubMed
16. Frulio N, Trillaud H. Ultrasound elastography in liver. Diagn Interv Imaging 2013;94:515–34.10.1016/j.diii.2013.02.005Search in Google Scholar PubMed
17. Myers KM, Socrate S, Paskaleva A, House M. A study of the anisotropy and tension/compression behavior of human cervical tissue. J Biomech Eng 2010;132:021003.10.1115/1.3197847Search in Google Scholar PubMed
18. Yang L, Yuan J, Wang Q, Wu G, Guo WQ, Wang WW, et al. Reliability analysis of acoustic radiation force impulse ultrasound imaging with virtual touch tissue quantification: ex vivo ox liver. Ultrasound Q 2015;31:59–62.10.1097/RUQ.0000000000000070Search in Google Scholar PubMed
19. Chang S, Kim MJ, Kim J, Lee MJ. Variability of shear wave velocity using different frequencies in acoustic radiation force impulse (ARFI) elastography: a phantom and normal liver study. Ultraschall Med 2013;34:260–5.10.1055/s-0032-1313008Search in Google Scholar PubMed
20. Garra BS. Elastography: history, principles, and technique comparison. Abdom Imaging 2015;40:680–97.10.1007/s00261-014-0305-8Search in Google Scholar PubMed
21. U.S. Department of Health and Human Services Food and Drug Administration Center for Devices and Radiological Health. Information for Manufacturers Seeking Marketing Clearance of Diagnostic Ultrasound Systems and Transducers. 2008.Search in Google Scholar
22. Shiina T, Nightingale KR, Palmeri ML, Hall TJ, Bamber JC, Barr RG, et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 1: basic principles and terminology. Ultrasound Med Biol 2015;41:1126–47.10.1016/j.ultrasmedbio.2015.03.009Search in Google Scholar PubMed
23. Palmeri ML, Nightingale KR. On the thermal effects associated with radiation force imaging of soft tissue. IEEE Trans Ultrason Ferroelectr Freq Control 2004;51:551–65.10.1109/TUFFC.2004.1320828Search in Google Scholar
24. Tabaru M, Yoshikawa H, Azuma T, Asami R, Hashiba K. Experimental study on temperature rise of acoustic radiation force elastography. J Med Ultrason 2012;39:137–46.10.1063/1.4749345Search in Google Scholar
25. Liu Y, Herman BA, Soneson JE, Harris GR. Thermal safety simulations of transient temperature rise during acoustic radiation force-based ultrasound elastography. Ultrasound Med Biol 2014;40:1001–14.10.1016/j.ultrasmedbio.2013.11.015Search in Google Scholar PubMed
26. Fatemi M, Alizad A, Greenleaf JF. Characteristics of the audio sound generated by ultrasound imaging systems. J Acoust Soc Am 2005;117:1448–55.10.1121/1.1852856Search in Google Scholar PubMed
27. Stratmeyer ME, Greenleaf JF, Dalecki D, Salvesen KA. Fetal ultrasound: mechanical effects. J Ultrasound Med 2008;27:597–605.10.7863/jum.2008.27.4.597Search in Google Scholar PubMed
28. Oxlund BS, Ørtoft G, Brüel A, Danielsen CC, Bor P, Oxlund H, et al. Collagen concentration and biomechanical properties of samples from the lower uterine cervix in relation to age and parity in non-pregnant women. Reprod Biol Endocrinol 2010;8:82.10.1186/1477-7827-8-82Search in Google Scholar PubMed PubMed Central
29. Wojcinski S, Brandhorst K, Sadigh G, Hillemanns P, Degenhardt F. Acoustic radiation force impulse imaging with virtual touch tissue quantification: measurements of normal breast tissue and dependence on the degree of pre-compression. Ultrasound Med Biol 2013;39:2226–32.10.1016/j.ultrasmedbio.2013.06.014Search in Google Scholar PubMed
30. Myers KM, Hendon CP, Gan Y, Yao W, Yoshida K, Fernandez M, et al. A continuous fiber distribution material model for human cervical tissue. J Biomech 2015;48:1533–40.10.1016/j.jbiomech.2015.02.060Search in Google Scholar PubMed PubMed Central
31. House M, Kaplan DL, Socrate S. Relationships between mechanical properties and extracellular matrix constituents of the cervical stoma during pregnancy. Semin Perinatol 2009;33:300–7.10.1053/j.semperi.2009.06.002Search in Google Scholar PubMed PubMed Central
32. Gress VS, Glawion EN, Schmidberger J, Kratzer W. Comparison of liver shear wave elastography measurements using Siemens Acuson S3000, GE LOGIQ E9, Philips EPIQ7 and Toshiba Aplio 500 (Software Versions 5.0 and 6.0) in Healthy Volunteers. Ultraschall Med 2018. doi: 10.1055/a-0651-0542. [Epub ahead of print]10.1055/a-0651-0542Search in Google Scholar
33. Uldbjerg N, Ekman G, Malmström A, Olsson K, Ulmsten U. Ripening of the human uterine cervix related to changes in collagen, glycosaminoglycans, and collagenolytic activity. Am J Obstet Gynecol 1983;147:662–6.10.1016/0002-9378(83)90446-5Search in Google Scholar
34. Guzman ER, Mellon C, Vintzileos AM, Ananth CV, Walters C, Gipson K. Longitudinal assessment of endocervical canal length between 15 and 24 weeks’ gestation in women at risk for pregnancy loss or preterm birth. Obstet Gynecol 1998;92:31–7.10.1016/S0029-7844(98)00120-3Search in Google Scholar
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