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Obstetrics and Gynegology2022№8
Magnetic resonance imaging in the...

Magnetic resonance imaging in the initial staging of cervical cancer: updating the 2021 ESUR guidelines

DOI
https://dx.doi.org/10.18565/aig.2022.8.36-46

Solopova A.E., Ukraintsev N.I., Rubtsova N.A.

1) Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of the Russian Federation, Moscow, Russia; 2) A.S. Loginov Moscow Clinical Research and Practical Center, Moscow Healthcare Department, Moscow, Russia; 3) Р.A. Herzen Moscow Oncology Research Institute, Branch, National Medical Radiology Research Center, Ministry of Health of the Russian Federation, Moscow, Russia
The paper presents the European Society for Urogenital Radiology (ESUR) guidelines for the radiodiagnosis
of cervical cancer (CC) and current concepts in its primary staging, by taking into account the main characteristics of the tumor and the possibilities of treating CC. Objective of this review – to systematize relevant scientific data on the possibilities and prospects for developing medical imaging techniques in CC. The ESUR guidelines standardize and promote the higher efficiency of using radiodiagnostic techniques for CC. The updated ESUR guidelines consider into account all the changes given in the FIGO classification in accordance of the 2009/2018 revisions and the 8th edition of the Timor-Node-Metastasis (TNM) staging system. In accordance with the updated FIGO system, the paper shows a significant role and place of MRI in CC before, during, and after antitumor treatment. Clinical assessment of the neoplasm is the basis of the FIGO classification as before. Modern instrumental diagnosis makes it possible to increase the objectivity of estimating the prevalence of the tumor process in the preoperative stage. This enables radiodiagnostic techniques to be used as an additional tool in clinical staging. The ESUR clarifies the criteria for primary staging and for planning anticancer therapy. The paper considers clinical cases with an emphasis on MRI staging criteria, evaluation of the efficiency of treatment and prognosis, diagnosis of recurrent CC. The review highlights the possibilities for the development of medical imaging, which are aimed at using hybrid methods for imaging and radiomics in the staging of advanced CC.
Conclusion: The current scientific data on urogenital radiology are of particular interest for radiation diagnosis and gynecologic oncology and serve as the basis for clinical application.

Keywords

cervical cancer
magnetic resonance imaging
MRI
MRI assessment system
diffusion-weighted imaging
neoplasm staging
neoplasm recurrence
Full text (in Russian)

References

  1. Каприн А.Д., Старинский В.В., Шахзадова А.О., ред. Состояние онкологической помощи населению России в 2020 году. М.: МНИОИ им. П.А. Герцена – филиал ФГБУ «НМИРЦ» Минздрава России; 2021. 239с. [Kaprin A.D., Starinsky V.V., Shakhzadova A.O., ed. The state of oncological care to the population of Russia in 2020. Moscow: P.A. Herzen Institute of Oncology – branch of the Federal State Budgetary Institution "NMIRC" of the Ministry of Health of Russia; 2021. (in Russian)].
  2. Bhatla N., Aoki D., Sharma D.N., Sankaranarayanan R. Cancer of the cervix uteri. Int. J. Gynaecol. Obstet. 2018; 143(Suppl. 2): 22-36. https://dx.doi.org/10.1002/ijgo.12611.
  3. Manganaro L., Lakhman Y., Bharwani N., Gui B., Gigli S., Vinci V. et al. Staging, recurrence and follow-up of uterine cervical cancer using MRI: updated Guidelines of the European Society of Urogenital Radiology after revised FIGO staging 2018. Eur. Radiol. 2021; 31(10): 7802-16. https://dx.doi.org/10.1007/s00330-020-07632-9.
  4. Bentivegna E., Maulard A., Pautier P., Chargari C., Gouy S., Morice P. Fertility results and pregnancy outcomes after conservative treatment of cervical cancer: a systematic review of the literature. Fertil. Steril. 2016; 106(5): 1195-211.e5. https://dx.doi.org/10.1016/j.fertnstert.2016.06.032.
  5. Koh W.J., Abu-Rustum N.R., Bean S., Bradley K., Campos S.M., Cho K.R. et al. Cervical Cancer, Version 3. 2019, NCCN Clinical Practice Guidelines in Oncology. J. Natl. Compr. Canc. Netw. 2019; 17(1): 64-84. https://dx.doi.org/10.6004/jnccn.2019.0001.
  6. Marth C., Landoni F., Mahner S., McCormack M., Gonzalez-Martin A., Colombo N. Cervical cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2017; 28(Suppl. 4): iv72-iv83.https://dx.doi.org/10.1093/annonc/mdx220.
  7. Bhatla N., Berek J.S., Cuello Fredes M., Denny L.A., Grenman S., Karunaratne K. et al. Revised FIGO staging for carcinoma of the cervix uteri. Int. J. Gynaecol. Obstet. 2019; 145(1): 129-35. https://dx.doi.org/10.1002/ijgo.12749.
  8. Lee S.I., Atri M. 2018 FIGO staging system for uterine cervical cancer: enter cross-sectional imaging. Radiology. 2019; 292(1): 15-24. https://dx.doi.org/10.1148/radiol.2019190088.
  9. Hori M., Kim T., Onishi H., Ueguchi T., Tatsumi M., Nakamoto A. et al. Uterine tumors: comparison of 3D versus 2D T2-weighted turbo spin-echo MR imaging at 3.0 T-initial experience. Radiology. 2011; 258(1): 154-63. https://dx.doi.org/10.1148/radiol.10100866.
  10. Park J.J., Kim C.K., Park S.Y., Park B.K. Parametrial invasion in cervical cancer: fused T2-weighted imaging and high-b-value diffusion-weighted imaging with background body signal suppression at 3 T. Radiology. 2015; 274(3): 734-41. https://dx.doi.org/10.1148/radiol.14140920.
  11. Moribata Y., Kido A., Fujimoto K., Himoto Y., Kurata Y., Shitano F. et al. Feasibility of computed diffusion weighted imaging and optimization of b-value in cervical cancer. Magn. Reson. Med. Sci. 2017; 16(1): 66-72.https://dx.doi.org/10.2463/mrms.mp.2015-0161.
  12. Hricak H., Gatsonis C., Chi D.S., Amendola M.A., Brandt K., Schwartz L.H. et al. Role of imaging in pretreatment evaluation of early invasive cervical cancer: results of the intergroup study American College of Radiology Imaging Network 6651-Gynecologic Oncology Group 183. J. Clin. Oncol. 2005; 23(36): 9329-37. https://dx.doi.org/10.1200/JCO.2005.02.0354.
  13. Liu B., Gao S., Li S. A comprehensive comparison of CT, MRI, positron emission tomography or positron emission tomography/CT, and diffusion weighted imaging-MRI for detecting the lymph nodes metastases in patients with cervical cancer: a meta-analysis based on 67 studies. Gynecol. Obstet. Invest. 2017; 82(3): 209-22. https://dx.doi.org/10.1159/000456006.
  14. Woo S., Moon M.H., Cho J.Y., Kim S.H., Kim S.Y. Diagnostic performance of MRI for assessing parametrial invasion in cervical cancer: a head-to-head comparison between oblique and true axial T2-weighted images. Korean J. Radiol. 2019; 20(3): 378-84. https://dx.doi.org/10.3348/kjr.2018.0248.
  15. Lakhman Y., Akin O., Park K.J., Sarasohn D.M., Zheng J., Goldman D.A. et al. Stage IB1 cervical cancer: role of preoperative MR imaging in selection of patients for fertility-sparing radical trachelectomy. Radiology. 2013; 269(1): 149-58. https://dx.doi.org/10.1148/radiol.13121746.
  16. Downey K., Attygalle A.D., Morgan V.A., Giles S.L., MacDonald A., Davis M. et al. Comparison of optimised endovaginal vs external array coil T2-weighted and diffusion-weighted imaging techniques for detecting suspected early stage (IA/IB1) uterine cervical cancer. Eur. Radiol. 2016; 26(4): 941-50.https://dx.doi.org/10.1007/s00330-015-3899-5.
  17. McEvoy S.H., Nougaret S., Abu-Rustum N.R., Vargas H.A., Sadowski E.A., Menias C.O. et al. Fertility sparing for young patients with gynecologic cancer: how MRI can guide patient selection prior to conservative management. Abdom. Radiol. (NY). 2017; 42(10): 2488-512. https://dx.doi.org/10.1007/s00261-017-1179-3.
  18. Raithatha A., Papadopoulou I., Stewart V., Barwick T.D., Rockall A.G., Bharwani N. Cervical cancer staging: a resident’s primer: women’s imaging. Radiographics. 2016; 36(3): 933-4. https://dx.doi.org/10.1148/rg.2016150173.
  19. Qi Y.F., He Y.L., Lin C.Y., Wang X.Q., Zhou H.L., Yuan L. et al. Diffusion-weighted imaging of cervical cancer: feasibility of ultra-high b-value at 3T. Eur. J. Radiol. 2020; 124: 108779. https://dx.doi.org/10.1016/j.ejrad.2019.108779.
  20. Jalaguier-Coudray A., Villard-Mahjoub R., Delouche A., Delarbre B., Lambaudie E., Houvenaeghel G. et al. Value of dynamic contrast-enhanced and diffusion-weighted MR imaging in the detection of pathologic complete response in cervical cancer after neoadjuvant therapy: a retrospective observational study. Radiology. 2017; 284(2): 432-42. https://dx.doi.org/10.1148/radiol.2017161299.
  21. Vincens E., Balleyguier C., Rey A., Uzan C., Zareski E., Gouy S. et al. Accuracy of magnetic resonance imaging in predicting residual disease in patients treated for stage IB2/II cervical carcinoma with chemoradiation therapy: correlation of radiologic findings with surgicopathologic results. Cancer. 2008; 113(8): 2158-65. https://dx.doi.org/10.1002/cncr.23817.
  22. Schreuder S.M., Lensing R., Stoker J., Bipat S. Monitoring treatment response in patients undergoing chemoradiotherapy for locally advanced uterine cervical cancer by additional diffusion-weighted imaging: a systematic review. J. Magn. Reson. Imaging. 2015; 42(3): 572-94. https://dx.doi.org/10.1002/jmri.24784.
  23. Onal C., Reyhan M., Guler O.C., Yapar A.F. Treatment outcomes of patients with cervical cancer with complete metabolic responses after definitive chemoradiotherapy. Eur. J. Nucl. Med. Mol. Imaging. 2014; 41(7): 1336-42. https://dx.doi.org/10.1007/s00259-014-2719-5.
  24. Grigsby P.W., Siegel B.A., Dehdashti F., Rader J., Zoberi I. et al. Posttherapy [18F] fluorodeoxyglucose positron emission tomography in carcinoma of the cervix: response and outcome. J. Clin. Oncol. 2004; 22(11): 2167-71. https://dx.doi.org/10.1200/JCO.2004.09.035.
  25. Ho J.C., Allen P.K., Bhosale P.R., Rauch G.M., Fuller C.D., Mohamed A.S. et al. Diffusion-weighted magnetic resonance imaging as a predictor of outcome in cervical cancer after chemoradiation. Int. J. Radiat. Oncol. Biol. Phys. 2017; 97(3): 546-53. https://dx.doi.org/10.1016/j.ijrobp.2016.11.015.
  26. Gladwish A., Milosevic M., Fyles A., Xie J., Halankar J., Metser U. et al. Association of apparent diffusion coefficient with disease recurrence in patients with locally advanced cervical cancer treated with radical chemotherapy and radiation therapy. Radiology. 2016; 279(1): 158-66. https://dx.doi.org/10.1148/radiol.2015150400.
  27. Onal C., Erbay G., Guler O.C. Treatment response evaluation using the mean apparent diffusion coefficient in cervical cancer patients treated with definitive chemoradiotherapy. J. Magn. Reson. Imaging. 2016; 44(4):1010-9.https://dx.doi.org/10.1002/jmri.25215.
  28. Zhou W., Yang X., Dai Y., Wu Q., He G., Yin G. Survey of cervical cancer survivors regarding quality of life and sexual function. J. Cancer Res. Ther. 2016; 12(2): 938-44. https://dx.doi.org/10.4103/0973-1482.175427.
  29. Himoto Y., Kido A., Fujimoto K., Daido S., Kiguchi K., Shitano F. et al. MR imaging-based evaluation of morphological changes in the uterus and ovaries of patients following neoadjuvant chemotherapy for cervical cancer. Magn. Reson. Med. Sci. 2015; 14(1): 65-72. https://dx.doi.org/10.2463/mrms.2014-0025.
  30. Heo S.H., Shin S.S., Kim J.W., Lim H.S., Jeong Y.Y., Kang W.D. et al. Pre-treatment diffusion-weighted MR imaging for predicting tumor recurrence in uterine cervical cancer treated with concurrent chemoradiation: value of histogram analysis of apparent diffusion coefficients. Korean J. Radiol. 2013; 14(4): 616-25. https://dx.doi.org/10.3348/kjr.2013.14.4.616.
  31. Nakamura K., Kajitani S., Joja I., Haruma T., Fukushima C., Kusumoto T. et al. The posttreatment mean apparent diffusion coefficient of primary tumor is superior to pretreatment ADCmean of primary tumor as a predictor of prognosis with cervical cancer. Cancer Med. 2013; 2(4): 519-25. https://dx.doi.org/10.1002/cam4.100.
  32. Signorelli M., Guerra L., Montanelli L., Crivellaro C., Buda A., Dell'Anna T. et al. Preoperative staging of cervical cancer: is 18-FDG-PET/ CT really effective in patients with early stage disease? Gynecol. Oncol. 2011; 123(2): 236-40.https://dx.doi.org/10.1016/j.ygyno.2011.07.096.
  33. Li Z., Li H., Wang S., Dong D., Yin F., Chen A. et al. MR-based radiomics nomogram of cervical cancer in prediction of the lymph-vascular space invasion preoperatively. J. Magn. Reson. Imaging. 2019; 49(5): 1420-6. https://dx.doi.org/10.1002/jmri.26531.
  34. Tian X., Sun C., Liu Z., Li W., Duan H., Wang L. et al. Prediction of response to preoperative neoadjuvant chemotherapy in locally advanced cervical cancer using multicenter CT-based radiomic analysis. Front. Oncol. 2020; 10: 77. https://dx.doi.org/10.3389/fonc.2020.00077.
  35. Lucia F., Visvikis D., Vallières M., Desseroit M.C., Miranda O., Robin P. et al. External validation of a combined PET and MRI radiomics model for prediction of recurrence in cervical cancer patients treated with chemoradiotherapy. Eur. J. Nucl. Med. Mol. Imaging. 2019; 46(4): 864-77. https://dx.doi.org/10.1007/s00259-018-4231-9.
  36. Jin X., Ai Y., Zhang J., Zhu H., Jin J., Teng Y. et al. Noninvasive prediction of lymph node status for patients with early-stage cervical cancer based on radiomics features from ultrasound images. Eur. Radiol. 2020; 30(7): 4117-24. https://dx.doi.org/10.1007/s00330-020-06692-1.
  37. Schernberg A., Reuze S., Orlhac F., Buvat I., Dercle L., Sun R. et al. A score combining baseline neutrophilia and primary tumor SUVpeak measured from FDG PET is associated with outcome in locally advanced cervical cancer. Eur. J. Nucl. Med. Mol. Imaging. 2018; 45(2): 187-95. https://dx.doi.org/10.1007/s00259-017-3824-z.
  38. Wang T., Gao T., Yang J., Yan X.., Wang Y, Zhou X. et al. Preoperative prediction of pelvic lymph nodes metastasis in early-stage cervical cancer using radiomics nomogram developed based on T2-weighted MRI and diffusion-weighted imaging. Eur. J. Radiol. 2019; 114: 128-35. https://dx.doi.org/10.1016/j.ejrad.2019.01.003.
  39. Lin Y.C., Lin C.H., Lu H.Y., Chiang H.J., Wang H.K., Huang Y.T. et al. Deep learning for fully automated tumor segmentation and extraction of magnetic resonance radiomics features in cervical cancer. Eur. Radiol. 2020; 30(3):1297-305. https://dx.doi.org/10.1007/s00330-019-06467-3.
  40. Liu Y., Zhang Y., Cheng R., Liu S., Qu F., Yin X. et al. Radiomics analysis of apparent diffusion coefficient in cervical cancer: a preliminary study on histological grade evaluation. J. Magn. Reson. Imaging. 2019; 49(1): 280-90. https://dx.doi.org/10.1002/jmri.26192.
  41. Zwanenburg A., Vallières M., Abdalah M.A., Aerts H.J.W.L., Andrearczyk V., Apte A. et al. The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology. 2020; 295(2): 328-38. https://dx.doi.org/10.1148/radiol.2020191145.
  42. Li K., Sun H., Lu Z., Xin J., Zhang L., Guo Y. et al. Value of [18F]FDG PET radiomic features and VEGF expression in predicting pelvic lymphatic metastasis and their potential relationship in early-stage cervical squamous cell carcinoma. Eur. J. Radiol. 2018; 106: 160-6. https://dx.doi.org/10.1016/j.ejrad.2018.07.024.
  43. Hou L., Zhou W., Ren J., Du X., Xin L., Zhao X. et al. Radiomics analysis of multiparametric MRI for the preoperative prediction of lymph node metastasis in cervical cancer. Front. Oncol. 2020; 10: 1393. https://dx.doi.org/10.3389/fonc.2020.01393.
  44. Wang T., Gao T., Guo H., Wang Y., Zhou X., Tian J. et al. Preoperative prediction of parametrial invasion in early-stage cervical cancer with MRI-based radiomics nomogram. Eur. Radiol. 2020; 30(6): 3585-93. https://dx.doi.org/10.1007/s00330-019-06655-1.
  45. Cai M., Yao F., Ding J., Zheng R., Huang X., Yang Y. et al. MRI radiomic features: a potential biomarker for progression-free survival prediction of patients with locally advanced cervical cancer undergoing surgery. Front. Oncol. 2021; 11: 749114. https://dx.doi.org/10.3389/fonc.2021.749114.
  46. Autorino R., Gui B., Panza G., Boldrini L., Cusumano D., Russo L. et al. Radiomics-based prediction of two-year clinical outcome in locally advanced cervical cancer patients undergoing neoadjuvant chemoradiotherapy. Radiol. Med. 2022; 127(5): 498-506. https://dx.doi.org/10.1007/s11547-022-01482-9.
  47. Kim K.E., Kim C.K. Magnetic resonance imaging-based texture analysis for the prediction of postoperative clinical outcome in uterine cervical cancer. Abdom. Radiol. (NY). 2022; 47(1): 352-61. https://dx.doi.org/10.1007/s00261-021-03288-1.
  48. Liu B., Sun Z., Xu Z.L., Zhao H.L., Wen D.D., Li Y.A. et al. Predicting disease-free survival with multiparametric MRI-derived radiomic signature in cervical cancer patients underwent CCRT. Front. Oncol. 2022; 11: 812993.https://dx.doi.org/10.3389/fonc.2021.812993.
  49. Ikushima H., Haga A., Ando K., Kato S., Kaneyasu Y., Uno T. et al. Prediction of out-of-field recurrence after chemoradiotherapy for cervical cancer using a combination model of clinical parameters and magnetic resonance imaging radiomics: a multi-institutional study of the Japanese Radiation Oncology Study Group. J. Radiat. Res. 2022; 63(1): 98-106. https://dx.doi.org/10.1093/jrr/rrab104.
  50. Zhou Y., Gu H.L., Zhang X.L., Tian ZF., Xu X.Q., Tang W.W. Multiparametric magnetic resonance imaging-derived radiomics for the prediction of disease-free survival in early-stage squamous cervical cancer. Eur. Radiol. 2022; 32(4): 2540-51. https://dx.doi.org/10.1007/s00330-021-08326-6.

Received 13.07.2022

Accepted 08.08.2022

About the Authors

Alina E. Solopova, MD, PhD, Associate Professor, Leading Researcher, Department of Radiology, Academician V.I. Kulakov National Medical Research Center for Obstetrics,
Gynecology and Perinatology, a_solopova@oparina4.ru, https://orcid.org/0000-0003-4768-115X, 117997, Russia, Moscow, Academician Oparin str., 4.
Nikita I. Ukraintsev, MD, resident doctor, Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department, ukraincev.nikita@mail.ru,
111123, Russia, Moscow, Shosse Entuziastov, 86.
Natalia A. Rubtsova, Dr. Med. Sci., Professor, Head of the Department of Radiology, P.A. Hertsen Moscow Oncological Center, rna17@yandex.ru,
125284, Russia, Moscow, 2nd Botkinsky pr., 3.

Authors' contributions: Solopova A.E. – analysis of sources, writing the article, selection of images; Ukraintsev N.I. – analysis of current literature, writing the article, selection of images; Rubtsova N.A. – peer-reviewing and editing the text of the article, assistance in adapting the recommendations.
Conflicts of interest: The authors declare that there are no conflicts of interest regarding this publication.
Funding: The investigation has not been sponsored.
For citation: Solopova A.E., Ukraintsev N.I., Rubtsova N.A. Magnetic resonance imaging in the initial staging of cervical cancer: updating the 2021 ESUR guidelines.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2022; 8: 36-46 (in Russian)
https://dx.doi.org/10.18565/aig.2022.8.36-46

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