Magnetic resonance imaging in the planning and monitoring of the treatment of cervical cancer

DOI

https://dx.doi.org/10.18565/aig.2023.253

Solopova A.E., Bendzhenova B.B.
1) Academician V.I. Kulakov National Medical Research Centre for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia, Moscow, Russia; 2) Botkin City Clinical Hospital, Moscow Healthcare Department, Moscow, Russia

Cervical cancer remains one of the leading causes of cancer morbidity and mortality among the female population worldwide. The prognosis as well as the choice of therapy depends on the initial assessment of the extent of the tumor spread. The latter is mainly determined with the use of methods of radiologic diagnostics: magnetic resonance imaging (MRI), positron emission tomography and multispiral computed tomography. These methods also play one of the leading roles in assessing the treatment response. The updated classification of the International Federation of Gynecology and Obstetrics (FIGO, 2018) recognizes the value of imaging in cervical cancer, in particular MRI, before, during and after antitumor treatment. The development of medical imaging and the search for new biomarkers will increase the prognostic value in assessing the response to therapy, identifying residual tumors and relapse of the disease.
This review presents the relevant information on the possibilities and limitations, the place of MRI in the complex diagnostic algorithm at the stage of primary assessment of the tumor process, the choice of tactics and analysis of the effectiveness of cervical cancer treatment. Different data bases, including PubMed/MEDLINE, eLibrary, Scopus, NCCN, ESUR, ACR, were searched. We analyzed the studies results on the use of noninvasive imaging techniques at the stage of primary diagnosis, assessing the effectiveness of treatment and its prognosis in patients with cervical cancer. The diagnostic opportunities and limitations of MRI in the cervical cancer diagnosis are summarized in our review. Due to the high soft tissue contrast, MRI is the method of choice in assessing the response to therapy, predicting treatment and further monitoring.
Conclusion: Noninvasive imaging plays a leading role in the primary diagnosis of cervical cancer. Further research is needed to overcome the difficulties of staging, monitoring the response to therapy and detecting relapse of the disease.

Authors’ contributions: Solopova A.E. – developing the concept of the study; Solopova A.E., Bendzhenova B.B. – collecting and analyzing sources, writing, editing the text of the article.
Conflicts of interest: Authors declare lack of the possible conflicts of interests.
Funding: The study was carried out as a part of the Russian Science Foundation grant “Development of technology for objective assessment of the potential of tumor progression in cervical cancer for proposing new approaches to investigate individual pathogenetic mechanisms of therapeutic resistance by using quantitative imaging methods, a search for signs of therapeutic effectiveness based on mathematical modeling of real-life clinical data” (No. 23-25-00445 dated of 24.01.2023).
For citation: Solopova A.E., Bendzhenova B.B. Magnetic resonance imaging
in the planning and monitoring of the treatment of cervical cancer.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2023; (12): 47-58 (in Russian)
https://dx.doi.org/10.18565/aig.2023.253

cervical cancer

magnetic resonance imaging

treatment effectiveness

prognosis of response to therapy

Full text (in Russian)

Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021:71:209-49. https://dx.doi.org/10.3322/caac.21660.
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.
Berek J.S., Matsuo K., Grubbs B.H., Gaffney D.K., Lee S.I., Kilcoyne A. et al. Multidisciplinary perspectives on newly revised 2018 FIGO staging of cancer of the cervix uteri. J. Gynecol. Oncol. 2019; 30(2): e40. https://dx.doi.org/10.3802/jgo.2019.30.e40.
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.
Shrestha P., Poudyal B., Yadollahi S., Wright D.E., Gregory A.V., Warner J.D. et al. A systematic review on the use of artificial intelligence in gynecologic imaging - Background, state of the art, and future directions. Gynecol. Oncol. 2022;166(3): 596-605. https://dx.doi.org/10.1016/j.ygyno.2022.07.024.
Epstein E., Testa A., Gaurilcikas A., Di Legge A., Ameye L., Atstupenaite V. et al. Early-stage cervical cancer: tumor delineation by magnetic resonance imaging and ultrasound - a European multicenter trial. Gynecol. Oncol. 2013; 128(3): 449-53. https://dx.doi.org/10.1016/j.ygyno.2012.09.025
Testa A.C., Di Legge A., De Blasis I., Moruzzi M.C., Bonatti M., Collarino A. et al. Imaging techniques for the evaluation of cervical cancer. Best Pract. Res. Clin. Obstet. Gynaecol. 2014; 28(5): 741-68. https://dx.doi.org/10.1016/j.bpobgyn.2014.04.009.
Lee S.I., Catalano O.A., Dehdashti F. Evaluation of gynecologic cancer with MR imaging, 18F-FDG PET/CT, and PET/MR imaging. J. Nucl. Med. 2015; 56(3): 436-43. https://dx.doi.org/10.2967/jnumed.114.145011.
Cibula D., Pötter R., Planchamp F., Avall-Lundqvist E., Fischerova D., Haie Meder C. et al. The European Society of Gynaecological Oncology/European Society for Radiotherapy and Oncology/European Society of Pathology Guidelines for the Management of Patients With Cervical Cancer. Int. J. Gynecol. Cancer. 2018; 28(4): 641-55. https://dx.doi.org/10.1097/IGC.0000000000001216.
Sharma D.N., Thulkar S., Goyal S., Shukla N.K., Kumar S., Rath G.K. et al. Revisiting the role of computerized tomographic scan and cystoscopy for detecting bladder invasion in the revised FIGO staging system for carcinoma of the uterine cervix. Int. J. Gynecol. Cancer. 2010; 20(3): 368-72.https://dx.doi.org/10.1111/IGC.0b013e3181d02d2d.
Meva J., Chaudhary R.K., Bhaduri D., Bhatia M., Hatti S., Ba R. Lacunae in International Federation of Gynecology and Obstetrics (FIGO) classification for cervical carcinoma: observational study using TNM classification as comparator. Int. J. Gynecol. Cancer. 2013; 23(6):1071-7. https://dx.doi.org/10.1097/IGC.0b013e31829783c4.
Gee M.S., Atri M., Bandos A.I., Mannel R.S., Gold M.A., Lee S.I. Identification of distant metastatic disease in uterine cervical and endometrial cancers with FDG PET/CT: Analysis from the ACRIN 6671/GOG 0233 multicenter trial. Radiology. 2018; 287(1): 176-84. https://dx.doi.org/10.1148/radiol.2017170963.
Balcacer P., Shergill A., Litkouhi B. MRI of cervical cancer with a surgical perspective: staging, prognostic implications and pitfalls. Abdom. Radiol. (NY). 2019; 44(7): 2557-71. https://dx.doi.org/10.1007/s00261-019-01984-7.
Hou B., Xiang S.F., Yao G.D., Yang S.J., Wang Y.F., Zhang Y.X.,Wang J.W. Diagnostic significance of diffusion-weighted MRI in patients with cervical cancer: a meta-analysis. Tumour Biol. 2014; 35(12):11761-9.https://dx.doi.org/10.1007/s13277-014-2290-5.
Csutak C., Ordeanu C., Nagy V.M., Pop D.C., Bolboaca S.D., Badea R. et al. A prospective study of the value of pre- and post-treatment magnetic resonance imaging examinations for advanced cervical cancer. Clujul. Med. 2016; 89(3): 410-8. https://dx.doi.org/10.15386/cjmed-558.
Bleker S.M., Bipat S., Spijkerboer A.M., van der Velden J., Stoker J., Kenter G.G. The negative predictive value of clinical examination with or without anesthesia versus magnetic resonance imaging for parametrial infiltration in cervical cancer stages IB1 to IIA. Int. J. Gynecol. Cancer. 2013; 23(1):193-8.https://dx.doi.org/10.1097/IGC.0b013e31827a4ad8.
Sarabhai T., Schaarschmidt B.M., Wetter A., Kirchner J., Aktas B., Forsting M. et al. Comparison of 18F-FDG PET/MRI and MRI for pre-therapeutic tumor staging of patients with primary cancer of the uterine cervix. Eur. J. Nucl. Med. Mol. Imaging. 2018; 45(1):67-76. https://dx.doi.org/10.1007/s00259-017-3809-y.
Haldorsen I.S., Lura N., Blaakær J., Fischerova D., Werner H.M.J. What Is the Role of Imaging at Primary Diagnostic Work-Up in Uterine Cervical Cancer? Curr. Oncol. Rep. 2019; 21(9): 77. https://dx.doi.org/10.1007/s11912-019-0824-0.
Patel-Lippmann K., Robbins J.B., Barroilhet L., Anderson B., Sadowski E.A., Boyum J. MR Imaging of cervical cancer. Magn. Reson. Imaging Clin. N. Am. 2017;25(3):635-49. https://dx.doi.org/10.1016/j.mric.2017.03.007.
Woo S., Atun R., Ward Z.J., Scott A.M., Hricak H., Vargas H.A. Diagnostic performance of conventional and advanced imaging modalities for assessing newly diagnosed cervical cancer: systematic review and meta-analysis. Eur. Radiol. 2020;30(10):5560-77. https://dx.doi.org/10.1007/s00330-020-06909-3.
Xiao M., Yan B., Li Y., Lu J., Qiang J. Diagnostic performance of MR imaging in evaluating prognostic factors in patients with cervical cancer: a meta-analysis. Eur. Radiol. 2020;30(3):1405-18. https://dx.doi.org/10.1007/s00330-019-06461-9.
Woo S., Suh C.H., Kim S.Y., Cho J.Y., Kim S.H. Magnetic resonance imaging for detection of parametrial invasion in cervical cancer: An updated systematic review and meta-analysis of the literature between 2012 and 2016. Eur. Radiol. 2018;28(2):530-41. https://dx.doi.org/10.1007/s00330-017-4958-x.
Sala E., Rockall A.G., Freeman S.J., Mitchell D.G., Reinhold C. The added role of MR imaging in treatment stratification of patients with gynecologic malignancies: what the radiologist needs to know. Radiology. 2013; 266(3): 717-40. https://dx.doi.org/10.1148/radiol.12120315.
Leblanc E., Narducci F., Frumovitz M., Lesoin A., Castelain B., Baranzelli M.C. et al. Therapeutic value of pretherapeutic extraperitoneal laparoscopic staging of locally advanced cervical carcinoma. Gynecol. Oncol. 2007;105(2): 304-11. https://dx.doi.org/10.1016/j.ygyno.2006.12.012.
McMahon C.J., Rofsky N.M., Pedrosa I. Lymphatic metastases from pelvic tumors: anatomic classification, characterization, and staging. Radiology. 2010; 254(1): 31-46. https://dx.doi.org/10.1148/radiol.2541090361.
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.
Lucia F., Visvikis D., Desseroit M.C., Miranda O., Malhaire J.P., Robin P. et al. Prediction of outcome using pretreatment 18F-FDG PET/CT and MRI radiomics in locally advanced cervical cancer treated with chemoradiotherapy. Eur. J. Nucl. Med. Mol. Imaging. 2018; 45(5): 768-86.https://dx.doi.org/10.1007/s00259-017-3898-7.
Bae J.M., Kim C.K., Park J.J., Park B.K. Can diffusion-weighted magnetic resonance imaging predict tumor recurrence of uterine cervical cancer after concurrent chemoradiotherapy? Abdom. Radiol. (NY). 2016; 41(8):1604-10. https://dx.doi.org/10.1007/s00261-016-0730-y.
Chino J., Annunziata C.M., Beriwal S., Bradfield L., Erickson B.A., Fields E.C. et al. The ASTRO clinical practice guidelines in cervical cancer: Optimizing radiation therapy for improved outcomes. Gynecol. Oncol. 2020; 159(3): 607-10. https://dx.doi.org/10.1016/j.ygyno.2020.09.015.
Оводенко Д.Л., Хабас Г.Н., Макарова А.С., Шешко П.Л., Санникова М.В., Пирогова М.С., Голицына Ю.С., Мамедов Ш.Я., Григорьев В.Ю., Ашрафян Л.А. Лапароскопическая радикальная гистерэктомия при раке шейки матки стадий Ia2–IIb. Акушерство и гинекология. 2018; 4: 104-7. [Ovodenko D.L., Khabas G.N., Makarova A.S., Sheshko P.L., Sannikova M.V., Pirogova M.S., Golitsyna Yu.S., Mamedov Sh.Ya., Grigoryev V.Yu., Ashrafyan L.A. Laparoscopic radical hysterectomy for Stages IA2 and IB cervical cancer. Obstetrics and Gynecology. 2018; (4): 101-7. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.4.101-107.
Querleu D., Morrow C.P. Classification of radical hysterectomy. Lancet Oncol. 2008; 9(3): 297-303. https://dx.doi.org/10.1016/S1470-2045(08)70074-3.
Cibula D., Pötter R., Planchamp F., Avall-Lundqvist E., Fischerova D., Haie Meder C. et al. The European Society of Gynaecological Oncology/European Society for Radiotherapy and Oncology/European Society of Pathology Guidelines for the management of patients with cervical cancer. Int. J. Gynecol. Cancer. 2018; 28(4): 641-55. https://dx.doi.org/10.1097/IGC.0000000000001216.
Silvestris E., Paradiso A.V., Minoia C., Daniele A., Cormio G., Tinelli R. et al. Fertility preservation techniques in cervical carcinoma. Medicine (Baltimore). 2022; 101(17): e29163. https://dx.doi.org/10.1097/MD.0000000000029163.
Nie H., Bu F., Xu J., Li T., Huang J. 29 immune-related genes pairs signature predict the prognosis of cervical cancer patients. Sci. Rep. 2020; 10(1):14152. https://dx.doi.org/10.1038/s41598-020-70500-5.
Paik E.S., Lim M.C., Kim M.H., Kim Y.H., Song E.S., Seong S.J. et al. Prognostic model for survival and recurrence in patients with early-stage cervical cancer: A Korean Gynecologic Oncology Group Study (KGOG 1028). Cancer Res. Treat. 2020;52(1):320-33. https://dx.doi.org/10.4143/crt.2019.124.
Солопова А.Е., Украинцев Н.И., Рубцова Н.А. Магнитно-резонансная томография в первичном стадировании и мониторинге рака шейки матки: обновление рекомендаций ESUR (2021). Акушерство и гинекология. 2022; 8: 36-46. [Solopova A.E., Ukraintsev N.I., Rubtsova N.A. Magnetic resonance imaging in the initial staging of cervical cancer: updating the 2021 ESUR guidelines. Obstetrics and Gynecology. 2022; (8): 36-46 (in Russian)].https://dx.doi.org/10.18565/aig.2022.8.36-46.
Kamimori T., Sakamoto K., Fujiwara K., Umayahara K., Sugiyama Y., Utsugi K. et al. Parametrial involvement in FIGO stage IB1 cervical carcinoma diagnostic impact of tumor diameter in preoperative magnetic resonance imaging. Int. J. Gynecol. Cancer. 2011; 21(2): 349-54.
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.
Lu H., Wu Y., Liu X., Huang H., Jiang H., Zhu C. et al. The role of dynamic contrast-enhanced magnetic resonance imaging in predicting treatment response for cervical cancer treated with concurrent chemoradiotherapy. Cancer Manag. Res. 2021; 13: 6065-78. https://dx.doi.org/10.2147/CMAR.S314289.
Jung E.J., Byun J.M., Kim Y.N., Lee K.B., Sung M.S., Kim K.T., Jeong D.H. Cervical adenocarcinoma has a poorer prognosis and a higher propensity for distant recurrence than squamous cell carcinoma. Int. J. Gynecol. Cancer. 2017; 27(6): 1228-36. https://dx.doi.org/10.1097/IGC.0000000000001009.
de Foucher T., Hennebert C., Dabi Y., Ouldamer L., Lavoué V., Dion L. et al. Recurrence pattern of cervical cancer based on the platinum sensitivity concept: a multi-institutional study from the FRANCOGYN Group. J. Clin. Med. 2020; 9(11): 3646. https://dx.doi.org/10.3390/jcm9113646.

Received 08.11.2023

Accepted 12.12.2023

Alina E. Solopova, Dr. Med. Sci., Leading Researcher, Radiology Department, Academician V.I. Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia; Professor, Department of Obstetrics, Gynecology and Perinatal Medicine, Sechenov University, Ministry of Health of Russia, dr.solopova@mail.ru, https://orcid.org/0000-0003-4768-115X, Scopus Author ID: 24460923200. Researcher ID: P-8659-2015, 117997, Russia, Moscow, Ac. Oparin str., 4.
Bova B. Bendzhenova, MD, obstetrician-gynecologist, Gynecological Department, Botkin City Clinical Hospital, https://orcid.org/0000-0003-4768-115X,
125284, Russia, Moscow, 2nd Botkinsky pr., 5.
Corresponding author: Alina E. Solopova, dr.solopova@mail.ru

Magnetic resonance imaging in the planning and monitoring of the treatment of cervical cancer

Solopova A.E., Bendzhenova B.B.

Keywords

References

About the Authors

Similar Articles