Multiparameter magnetic resonance imaging in the diagnosis of cancer of the cervix uteri

Cancer of the cervix uteri (CCU) ranks third in the incidence of malignancies in women. The choice of CCU treatment mainly depends on the extent of the tumor process, i.e. the stage of the disease. Determining the stage of CCU is based on the clinical classification of the International Federation of Gynecology and Obstetrics (FIGO) (2009) and has a number of substantial limitations in evaluating parametrial invasion, tumor spread to the pelvic wall, and involvement of regional lymph nodes and in determining the true tumor sizes. Magnetic resonance imaging (MRI) is now the method of choice in staging invasive CCU.
Multiparameter MRI will be able to enhance the efficiency of diagnosing microinvasive CCU as well (FIGO 2009), to plan surgical and/or chemoradiation treatment, to evaluate its efficiency, and to diagnose locally recurrent CCU.

cancer of the cervix uteri, International Federation of Gynecology and Obstetrics, magnetic resonance imaging, diffusion-weighted magnetic resonance images, measured diffusion coefficient, dynamic contrast-enhanced magnetic resonance imaging, positron emission tomography

1. Chissov V.I., Starinskiy V.V., Petrova G.V. Status of cancer care in Russia in 2010. Moscow; 2011 (in Russian).

2. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin. 2013; 63 (1): 11–30.

3. Axel’ E.M. Statistic of malignance gynecologic tumors. Onkoginekologiya. 2012 (1): 18–23 (in Russian).

4. Trufanov V.G., Panov V.O. Handbook of radiation diagnostic in gynecology. St. Petersburg: ELBI-SPb; 2008: 590–2, 616 (in Russian).

5. Davydov M.I., Kuznetsov V.V., Nechushkina M.V. Lections of oncogynecology. Moscow: MEDpressinform; 2009: 20–1, 33 (in Russian).

6. Paliychuk O.V., Polishchuk L.Z. The role of infection in etiology and pathogenesis of cervical intraepithelial neoplasms and cervical cancer. Reproduktivnoe zdorov’e zhenshchiny. 2007; 32 (3): 10–6 (in Russian).

7. Polonskaya N.Yu., Yurasova I.V., Sokol’skaya T.Yu. Benefits and efficacy of standardization of cythology methods in gynecology. Klinicheskaya laboratornaya diagnostika. 2004; 1 (11): 47–50 (in Russian).

8. Hopman A.H., Smedts F., Dignef W., Ummelen M., Sonke G., Mravunac M., Vooijs G.P., Speel E.J., Ramaekers F.C. Transition of highgrade cervical intraepithelial neoplasia to micro-invasive carcinoma is characterized by integration of HPV 16/18 and numerical chromosome abnormalities. J. Pathol. 2004; 202 (1): 23–33.

9. Petsuksiri J., Jaishuen A., Pattaranutaporn P., Chansilpa Y. Advanced imaging applications for locally advanced cervical cancer. Asian Pacific. J. Cancer Prevention. 2012; 13 (5): 1713–8.

10. Makarov I.O., Ovsyannikova T.V., Shemanaeva T.V., Borovkova E.I., Kulikov I.A., Guriev T.D. 3D US in normal and abnormal cervix. Akusherstvo, ginekologiya i reproduktsiya. 2013; 7 (2): 23–6 (in Russian).

11. Adamyan L.V., Demidov V.N., Gus A.I., Obel’chak I.S. Handbook of radiation diagnostic and therapy in obstetrics and gynecology. Moscow: GEOTAR-Media; 2012 (in Russian).

12. Rogozhin V.I. MRT in gynecologic practice. Russian eltctronic journal of radiology. 2012; 2 (3): 27–40 (in Russian).

13. Pecorelli S. Revised FIGO staging for carcinoma of the vulva, cervix, and endometrium. Int. J. Gynaecol. Obstet. 2009; 105 (2): 103–4.

14. Liyanage S.H., Roberts C.A., Rockall A.G. MRI and PET scans for primary staging and detection of cervical cancer recurrence. Womens Health (Lond Engl). 2010; 6 (2): 251–69.

15. Kim H.S., Kim C.K., Park B.K., Huh S.J., Kim B. Evaluation of therapeutic response to concurrent chemoradiotherapy in patients with cervical cancer using diffusionweighted MR imaging. J. Magn. Reson. Imaging. 2013; 37 (1): 187–93.

16. Freeman S.J., Aly A.M., Kataoka M.Y., Addley H.C., Reinhold C., Sala E. The revised FIGO staging system for uterine malignancies: implications for MR imaging. Radiographics. 2012; 32 (6): 1805–27.

17. Kraljevic Z., Viskovic K., Ledinsky M., Zadravec D., Grbavac I., Bilandzija M. et al. Primary uterine cervical cancer: correlation of preoperative magnetic resonance imaging and clinical staging (FIGO) with histopathology findings. Coll. Antropol. 2013; 37 (2): 561–8.

18. Dhoot N.M., Kumar V., Shinagare A., Kataki A.C., Barmon D., Bhuyan U. Evaluation of carcinoma cervix using magnetic resonance imaging: correlation with clinical FIGO staging and impact on management. J. Med. Imaging Radiat. Oncol. 2012; 56 (1): 58–65.

19. Hricak H., Lacey C.G., Sandles L.G., Chang Y.C., Winkler M.L., Stern J.L. Invasive cervical carcinoma: comparison of MR imaging and surgical findings. Radiology. 1988; 166 (3): 623–31.

20. Lam W.W., So N.M., Yang W.T., Metreweli C. Detection of parametrial invasion in cervical carcinoma: role of short tau inversion recovery sequence. Clin. Radiol. 2000; 55 (9): 702–7.

21. Chung H.H., Kang S.B., Cho J.Y., Kim J.W., Park N.H., Song Y.S. et al. Can preoperative MRI accurately evaluate nodal and parametrial invasion in early stage cervical cancer? Jpn J. Clin. Oncol. 2007; 37 (5): 370–5.

22. Iwata S., Joja I., Okuno K., Miyagi Y., Sakaguchi Y., Kudo T., Hiraki Y. Cervical carcinoma with full-thickness stromal invasion: efficacy of dynamic MR imaging in the assessment of parametrial involvement. Radiat. Med. 2002; 20 (5): 247–55.

23. Shiraiwa M., Joja I., Asakawa T., Okuno K., Shibutani O., Akamatsu N. et al. Cervical carcinoma: efficacy of thin-section oblique axial T2- weighted images for evaluating parametrial invasion. Abdom. Imaging. 1999; 24 (5): 514–9.

24. Hawighorst H., Knapstein P.G., Weikel W., Knopp M.V., Schaeffer U., Brix G. et al. Cervical carcinoma: comparison of standard and pharmacokinetic MR imaging. Radiology. 1996; 201 (2): 531–9.

25. Rauch G.M., Kaur H., Choi H ,Ernst R.D., Klopp A.H., Boonsirikamchai P. et al. Optimization of MR imaging for pretreatment evaluation of patients with endometrial and cervical cancer. Radiographics. 2014; 34 (4): 1082–98.

26. 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.

27. Balleyguier C., Sala E., Da Cunha T., Bergman A., Brkljacic B., Danza F. et al. Staging of uterine cervical cancer with MRI: guidelines of the European Society of Urogenital Radiology. Eur. Radiol. 2011; 21 (5): 1102–10.

28. Lichy M.P., Wietek B.M., Mugler J.P., 3rd, Horger W., Menzel M.I., Anastasiadis A. et al. Magnetic resonance imaging of the body trunk using a single-slab, 3-dimensional, T2-weighted turbo-spin-echo sequence with high sampling efficiency (SPACE) for high spatial resolution imaging: initial clinical experiences. Invest. Radiol. 2005; 40 (12): 754–60.

29. Proscia N., Jaffe T.A., Neville A.M., Wang C.L., Dale B.M., Merkle E.M. MRI of the pelvis in women: 3D versus 2D T2-weighted technique. Am. J. Roentgenol. 2010; 195 (1): 254–9.

30. Bhosale P., Peungjesada S., Devine C., Balachandran A., Iyer R. Role of magnetic resonance imaging as an adjunct to clinical staging in cervical carcinoma. J. Comput. Assist. Tomogr. 2010; 34 (6): 855–64. 31. Wootton J.H., Hsu I.C., Diederich C.J. Endocervical ultrasound applicator for integrated hyperthermia and HDR brachytherapy in the treatment of locally advanced cervical carcinoma. Med. Phys. 2011; 38 (2): 598–611.

31. Aksenova S.V., Nudnov N.V., Kreynina Yu.M. Magnetic-resonance tomography as a method of diagnostic and monitoring oncogynecologic patients with vagina tumors. In: Congress RAR 2014. Moscow: Chelovek i ego zdorov’e; 2014: 70–1 (in Russian).

32. Payne G.S., Schmidt M., Morgan V.A., Giles S., Bridges J., Ind T., DeSouza N.M. Evaluation of magnetic resonance diffusion and spectroscopy measurements as predictive biomarkers in stage 1 cervical cancer. Gynecol. Oncol. 2010; 116 (2): 246–52.

33. Chen J., Zhang Y., Liang B., Yang Z. The utility of diffusion-weighted MR imaging in cervical cancer. Eur. J. Radiol. 2010; 74 (3): e101–6.

34. Levy A., Medjhoul A., Caramella C., Zareski E., Berges O., Chargari C. et al. Interest of diffusion-weighted echo-planar MR imaging and apparent diffusion coefficient mapping in gynecological malignancies: a review. J. Magn. Reson. Imaging. 2011; 33 (5): 1020–7.

35. Harry V.N., Semple S.I., Parkin D.E., Gilbert F.J. Use of new imaging techniques to predict tumour response to therapy. Lancet. Oncol. 2010; 11 (1): 92–102.

36. Thoeny H.C., Ross B.D. Predicting and monitoring cancer treatment response with diffusion-weighted MRI. J. Magn. Reson. Imaging. 2010; 32 (1): 2–16.

37. Koh D.M., Collins D.J. Diffusionweighted MRI in the body: applications and challenges in oncology. Am. J. Roentgenol. 2007; 188 (6): 1622–35.

38. Somoye G., Harry V., Semple S., Plataniotis G., Scott N., Gilbert F.J., Parkin D. Early diffusion weighted magnetic resonance imaging can predict survival in women with locally advanced cancer of the cervix treated with combined chemo-radiation. Eur. Radiol. 2012; 22 (11): 2319–27.

39. Zhang Y., Chen J.Y., Xie C.M., Mo Y.X., Liu X.W., Liu Y., Wu P.H. Diffusion-weighted magnetic resonance imaging for prediction of response of advanced cervical cancer to chemoradiation. J. Comput. Assist. Tomogr. 2011; 35 (1): 102–7.

40. Nakamura K., Joja I., Nagasaka T , Fukushima C., Kusumoto T., Seki N. et al. The mean apparent diffusion coefficient value (ADCmean) on primary cervical cancer is a predictive marker for disease recurrence. Gynecol. Oncol. 2012; 127 (3): 478–83.

41. Noel P., Dube M., Plante M., St-Laurent G. Early cervical carcinoma and fertility-sparing treatment options: MR imaging as a tool in patient selection and a follow-up modality. Radiographics. 2014; 34 (4): 1099–119.

42. Hricak H.S., Swift P.S., Campos Z., Quivey J.M., Gildengorin V., Goranson H. Irradiation of the cervix uteri: value of unenhanced and contrastenhanced MR imaging. Radiology. 1993; 2 (189): 381–8.

43. He H., Bhosale P., Wei W., Ramalingam P., Iyer R. MRI is highly specific in determining primary cervical versus endometrial cancer when biopsy results are inconclusive. Clin. Radiol. 2013; 68 (11): 1107–13.

44. Ellingsen C., Hompland T., Galappathi K., Mathiesen B., Rofstad E.K. DCE-MRI of the hypoxic fraction, radioresponsiveness, and metastatic propensity of cervical carcinoma xenografts. Radiother. Oncol. 2014; 110 (2): 335–41.

45. Andersen E.K., Hole K.H., Lund K.V., Sundfor K., Kristensen G.B., Lyng H., Malinen E. Pharmacokinetic parameters derived from dynamic contrast enhanced MRI of cervical cancers predict chemoradiotherapy outcome. Radiother. Oncol. 2013; 107 (1): 117–22.

46. Halle C., Andersen E., Lando M., Aarnes E.K., Hasvold G., Holden M. et al. Hypoxia-induced gene expression in chemoradioresistant cervical cancer revealed by dynamic contrast-enhanced MRI. Cancer Res. 2012; 72 (20): 5285–95.

47. Hompland T., Ellingsen C., Rofstad E.K. Preclinical evaluation of Gd-DTPA and gadomelitol as contrast agents in DCE-MRI of cervical carcinoma interstitial fluid pressure. BMC Cancer. 2012; 12: 544.

48. Kaur H., Silverman P.M., Iyer R.B., Verschraegen C.F., Eifel P.J., Charnsangavej C. Diagnosis, staging, and surveillance of cervical carcinoma. Am. J. Roentgenol. 2003; 180 (6): 1621–31.

49. Kaur H., Choi H., You Y.N., Rauch G.M., Jensen C.T., Hou P. et al. MR imaging for preoperative evaluation of primary rectal cancer: practical considerations. Radiographics. 2012; 32 (2): 389–409.

50. Rockall A.G., Sohaib S.A., Harisinghani M.G., Babar S.A., Singh N., Jeyarajah A.R. et al. Diagnostic performance of nanoparticle-enhanced magnetic resonance imaging in the diagnosis of lymph node metastases in patients with endometrial and cervical cancer. J. Clin. Oncol. 2005; 23 (12): 2813–21.

51. Klerkx W.M., Veldhuis W.B., Spijkerboer A.M., van den Bosch M.A., Mali W.P., Heintz A.P. et al. The value of 3.0 Tesla diffusion-weighted MRI for pelvic nodal staging in patients with early stage cervical cancer. Eur. J. Cancer. 2012; 48 (18): 3414–21.

52. Shostka K.G., Pavlenko A.N., Fokina A.V., Kashina N.O., Roman L.D. Early and long-term results after pelvic exenterations of locally advanced cervical cancer. Voprosy onkologii. 2014; 60 (3): 319–22 (in Russian).

53. Padhani A.R., Liu G., Koh D.M., Chenevert T.L., Thoeny H.C., Takahara T. et al. Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia. 2009; 11 (2): 102–25.

54. Daar D.F., Bemardo M., Bernardo M.F., Choyke P.L., McKinney Y.M. et al. Prostate multiparameter MR imaging. Radiol. Technol. 2011; 6 (82): 563–8.