DOI QR코드

DOI QR Code

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

  • Heo, Suk Hee (Department of Radiology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School) ;
  • Shin, Sang Soo (Department of Radiology, Chonnam National University Hospital, Chonnam National University Medical School) ;
  • Kim, Jin Woong (Department of Radiology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School) ;
  • Lim, Hyo Soon (Department of Radiology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School) ;
  • Jeong, Yong Yeon (Department of Radiology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School) ;
  • Kang, Woo Dae (Department of Obstetrics and Gynecology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School) ;
  • Kim, Seok Mo (Department of Obstetrics and Gynecology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School) ;
  • Kang, Heoung Keun (Department of Radiology, Chonnam National University Hwasun Hospital, Chonnam National University Medical School)
  • Received : 2012.12.18
  • Accepted : 2013.04.24
  • Published : 2013.07.01

Abstract

Objective: To evaluate the value of apparent diffusion coefficient (ADC) histogram analysis for predicting tumor recurrence in patients with uterine cervical cancer treated with chemoradiation therapy (CRT). Materials and Methods: Our institutional review board approved this retrospective study and waived informed consent from each patient. Forty-two patients (mean age, 56 ${\pm}$ 14 years) with biopsy-proven uterine cervical squamous cell carcinoma who underwent both pre-treatment pelvic magnetic resonance imaging with a 3.0 T magnetic resonance scanner and concurrent CRT were included. All patients were followed-up for more than 6 months (mean, 36.4 ${\pm}$ 11.9 months; range 9.0-52.8 months) after completion of CRT. Baseline ADC parameters (mean ADC, 25th percentile, 50th percentile, and 75th percentile ADC values) of tumors were calculated and compared between the recurrence and no recurrence groups. Results: In the recurrence group, the mean ADC and 75th percentile ADC values of tumors were significantly higher than those of the no recurrence group (p = 0.043 and p = 0.008, respectively). In multivariate analysis, the 75th percentile ADC value of tumors was a significant predictor for tumor recurrence (p = 0.009; hazard ratio, 1.319). When the cut-off value of the 75th percentile ADC ($0.936{\times}10^{-3}mm^2/sec$) was used, the overall recurrence free survival rate above the cut-off value was significantly lower than that below the cut-off value (51.9% vs. 91.7%, p = 0.003, log-rank test). Conclusion: Pre-CRT ADC histogram analysis may serve as a biomarker for predicting tumor recurrence in patients with uterine cervical cancer treated with CRT.

Keywords

References

  1. Waggoner SE. Cervical cancer. Lancet 2003;361:2217-2225 https://doi.org/10.1016/S0140-6736(03)13778-6
  2. Peters WA 3rd, Liu PY, Barrett RJ 2nd, Stock RJ, Monk BJ, Berek JS, et al. Concurrent chemotherapy and pelvic radiation therapy compared with pelvic radiation therapy alone as adjuvant therapy after radical surgery in high-risk early-stage cancer of the cervix. J Clin Oncol 2000;18:1606-1613
  3. Thomas GM. Improved treatment for cervical cancer--concurrent chemotherapy and radiotherapy. N Engl J Med 1999;340:1198-1200 https://doi.org/10.1056/NEJM199904153401509
  4. Kastritis E, Bamias A, Efstathiou E, Gika D, Bozas G, Zorzou P, et al. The outcome of advanced or recurrent non-squamous carcinoma of the uterine cervix after platinum-based combination chemotherapy. Gynecol Oncol 2005;99:376-382 https://doi.org/10.1016/j.ygyno.2005.06.024
  5. Thoeny HC, Ross BD. Predicting and monitoring cancer treatment response with diffusion-weighted MRI. J Magn Reson Imaging 2010;32:2-16 https://doi.org/10.1002/jmri.22167
  6. Heo SH, Jeong YY, Shin SS, Kim JW, Lim HS, Lee JH, et al. Apparent diffusion coefficient value of diffusion-weighted imaging for hepatocellular carcinoma: correlation with the histologic differentiation and the expression of vascular endothelial growth factor. Korean J Radiol 2010;11:295-303 https://doi.org/10.3348/kjr.2010.11.3.295
  7. Lyng H, Haraldseth O, Rofstad EK. Measurement of cell density and necrotic fraction in human melanoma xenografts by diffusion weighted magnetic resonance imaging. Magn Reson Med 2000;43:828-836 https://doi.org/10.1002/1522-2594(200006)43:6<828::AID-MRM8>3.0.CO;2-P
  8. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 2007;188:1622-1635 https://doi.org/10.2214/AJR.06.1403
  9. Harry VN, Semple SI, Parkin DE, Gilbert FJ. Use of new imaging techniques to predict tumour response to therapy. Lancet Oncol 2010;11:92-102 https://doi.org/10.1016/S1470-2045(09)70190-1
  10. Kyriazi S, Collins DJ, Messiou C, Pennert K, Davidson RL, Giles SL, et al. Metastatic ovarian and primary peritoneal cancer: assessing chemotherapy response with diffusion-weighted MR imaging--value of histogram analysis of apparent diffusion coefficients. Radiology 2011;261:182-192 https://doi.org/10.1148/radiol.11110577
  11. Charles-Edwards EM, Messiou C, Morgan VA, De Silva SS, McWhinney NA, Katesmark M, et al. Diffusion-weighted imaging in cervical cancer with an endovaginal technique: potential value for improving tumor detection in stage Ia and Ib1 disease. Radiology 2008;249:541-550 https://doi.org/10.1148/radiol.2491072165
  12. Harry VN, Semple SI, Gilbert FJ, Parkin DE. Diffusion-weighted magnetic resonance imaging in the early detection of response to chemoradiation in cervical cancer. Gynecol Oncol 2008;111:213-220 https://doi.org/10.1016/j.ygyno.2008.07.048
  13. Kim HS, Kim CK, Park BK, Huh SJ, Kim B. Evaluation of therapeutic response to concurrent chemoradiotherapy in patients with cervical cancer using diffusion-weighted MR imaging. J Magn Reson Imaging 2013;37:187-193 https://doi.org/10.1002/jmri.23804
  14. Liu Y, Bai R, Sun H, Liu H, Wang D. Diffusion-weighted magnetic resonance imaging of uterine cervical cancer. J Comput Assist Tomogr 2009;33:858-862 https://doi.org/10.1097/RCT.0b013e31819e93af
  15. Liu Y, Bai R, Sun H, Liu H, Zhao X, Li Y. Diffusion-weighted imaging in predicting and monitoring the response of uterine cervical cancer to combined chemoradiation. Clin Radiol 2009;64:1067-1074 https://doi.org/10.1016/j.crad.2009.07.010
  16. McVeigh PZ, Syed AM, Milosevic M, Fyles A, Haider MA. Diffusion-weighted MRI in cervical cancer. Eur Radiol 2008;18:1058-1064 https://doi.org/10.1007/s00330-007-0843-3
  17. Naganawa S, Sato C, Kumada H, Ishigaki T, Miura S, Takizawa O. Apparent diffusion coefficient in cervical cancer of the uterus: comparison with the normal uterine cervix. Eur Radiol 2005;15:71-78 https://doi.org/10.1007/s00330-004-2529-4
  18. 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;127:478-483 https://doi.org/10.1016/j.ygyno.2012.07.123
  19. Somoye G, Harry V, Semple S, Plataniotis G, Scott N, Gilbert FJ, et al. 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;22:2319-2327 https://doi.org/10.1007/s00330-012-2496-0
  20. Kang H, Lee HY, Lee KS, Kim JH. Imaging-based tumor treatment response evaluation: review of conventional, new, and emerging concepts. Korean J Radiol 2012;13:371-390 https://doi.org/10.3348/kjr.2012.13.4.371
  21. Payne GS, Schmidt M, Morgan VA, Giles S, Bridges J, Ind T, et al. Evaluation of magnetic resonance diffusion and spectroscopy measurements as predictive biomarkers in stage 1 cervical cancer. Gynecol Oncol 2010;116:246-252 https://doi.org/10.1016/j.ygyno.2009.09.044
  22. Koh DM, Scurr E, Collins D, Kanber B, Norman A, Leach MO, et al. Predicting response of colorectal hepatic metastasis: value of pretreatment apparent diffusion coefficients. AJR Am J Roentgenol 2007;188:1001-1008 https://doi.org/10.2214/AJR.06.0601
  23. Park SH, Moon WK, Cho N, Song IC, Chang JM, Park IA, et al. Diffusion-weighted MR imaging: pretreatment prediction of response to neoadjuvant chemotherapy in patients with breast cancer. Radiology 2010;257:56-63 https://doi.org/10.1148/radiol.10092021
  24. Dzik-Jurasz A, Domenig C, George M, Wolber J, Padhani A, Brown G, et al. Diffusion MRI for prediction of response of rectal cancer to chemoradiation. Lancet 2002;360:307-308 https://doi.org/10.1016/S0140-6736(02)09520-X
  25. Zhang Y, Chen JY, Xie CM, Mo YX, Liu XW, Liu Y, et al. Diffusion-weighted magnetic resonance imaging for prediction of response of advanced cervical cancer to chemoradiation. J Comput Assist Tomogr 2011;35:102-107 https://doi.org/10.1097/RCT.0b013e3181f6528b
  26. Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, et al. Usefulness of diffusion-weighted MRI with echoplanar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 1999;9:53-60 https://doi.org/10.1002/(SICI)1522-2586(199901)9:1<53::AID-JMRI7>3.0.CO;2-2
  27. Higano S, Yun X, Kumabe T, Watanabe M, Mugikura S, Umetsu A, et al. Malignant astrocytic tumors: clinical importance of apparent diffusion coefficient in prediction of grade and prognosis. Radiology 2006;241:839-846 https://doi.org/10.1148/radiol.2413051276
  28. Murakami R, Hirai T, Sugahara T, Fukuoka H, Toya R, Nishimura S, et al. Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one- versus twoparameter pilot method. Radiology 2009;251:838-845 https://doi.org/10.1148/radiol.2513080899
  29. Pope WB, Kim HJ, Huo J, Alger J, Brown MS, Gjertson D, et al. Recurrent glioblastoma multiforme: ADC histogram analysis predicts response to bevacizumab treatment. Radiology 2009;252:182-189 https://doi.org/10.1148/radiol.2521081534
  30. Barajas RF Jr, Rubenstein JL, Chang JS, Hwang J, Cha S. Diffusion-weighted MR imaging derived apparent diffusion coefficient is predictive of clinical outcome in primary central nervous system lymphoma. AJNR Am J Neuroradiol 2010;31:60-66 https://doi.org/10.3174/ajnr.A1750
  31. Harrison LB, Chadha M, Hill RJ, Hu K, Shasha D. Impact of tumor hypoxia and anemia on radiation therapy outcomes. Oncologist 2002;7:492-508 https://doi.org/10.1634/theoncologist.7-6-492
  32. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 2007;26:225-239 https://doi.org/10.1007/s10555-007-9055-1
  33. DeVries AF, Kremser C, Hein PA, Griebel J, Krezcy A, Ofner D, et al. Tumor microcirculation and diffusion predict therapy outcome for primary rectal carcinoma. Int J Radiat Oncol Biol Phys 2003;56:958-965 https://doi.org/10.1016/S0360-3016(03)00208-6
  34. Lambregts DM, Beets GL, Maas M, Curvo-Semedo L, Kessels AG, Thywissen T, et al. Tumour ADC measurements in rectal cancer: effect of ROI methods on ADC values and interobserver variability. Eur Radiol 2011;21:2567-2574 https://doi.org/10.1007/s00330-011-2220-5
  35. Schaefer PW, Grant PE, Gonzalez RG. Diffusion-weighted MR imaging of the brain. Radiology 2000;217:331-345 https://doi.org/10.1148/radiology.217.2.r00nv24331

Cited by

  1. Diagnostic significance of diffusion-weighted MRI in patients with cervical cancer: a meta-analysis vol.35, pp.12, 2014, https://doi.org/10.1007/s13277-014-2290-5
  2. Pancreatic neuroendocrine tumors: correlation between histogram analysis of apparent diffusion coefficient maps and tumor grade vol.40, pp.8, 2015, https://doi.org/10.1007/s00261-015-0524-7
  3. Association of Apparent Diffusion Coefficient with Disease Recurrence in Patients with Locally Advanced Cervical Cancer Treated with Radical Chemotherapy and Radiation Therapy. vol.2015, pp.None, 2015, https://doi.org/10.1148/radiol.2015150400
  4. Current Role of Magnetic Resonance Imaging in Evaluation and Radiotherapy in Locally Advanced Carcinoma Cervix vol.14, pp.2, 2016, https://doi.org/10.1007/s40944-016-0063-3
  5. Predicting liver metastasis of gastrointestinal tract cancer by diffusion-weighted imaging of apparent diffusion coefficient values vol.22, pp.10, 2016, https://doi.org/10.3748/wjg.v22.i10.3031
  6. Diffusion weighted imaging in gynecological malignancies - present and future vol.8, pp.3, 2013, https://doi.org/10.4329/wjr.v8.i3.288
  7. Can diffusion-weighted magnetic resonance imaging predict tumor recurrence of uterine cervical cancer after concurrent chemoradiotherapy? vol.41, pp.8, 2016, https://doi.org/10.1007/s00261-016-0730-y
  8. Hypoxia in cervical cancer: from biology to imaging vol.5, pp.4, 2013, https://doi.org/10.1007/s40336-017-0238-7
  9. Predicting tumor recurrence in patients with cervical carcinoma treated with definitive chemoradiotherapy: value of quantitative histogram analysis on diffusion-weighted MR images vol.58, pp.4, 2017, https://doi.org/10.1177/0284185116656492
  10. Investigation of volumetric apparent diffusion coefficient histogram analysis for assessing complete response and clinical outcomes following pre-operative chemoradiation treatment for rectal carcinom vol.42, pp.5, 2017, https://doi.org/10.1007/s00261-016-1010-6
  11. Comparison of FDG PET metabolic tumour volume versus ADC histogram: prognostic value of tumour treatment response and survival in patients with locally advanced uterine cervical cancer vol.90, pp.1075, 2013, https://doi.org/10.1259/bjr.20170035
  12. MR Imaging for Staging of Cervical Carcinoma: Update vol.77, pp.2, 2017, https://doi.org/10.3348/jksr.2017.77.2.67
  13. Value of whole-lesion apparent diffusion coefficient (ADC) first-order statistics and texture features in clinical staging of cervical cancers vol.72, pp.11, 2013, https://doi.org/10.1016/j.crad.2017.06.115
  14. Histogram analysis of apparent diffusion coefficient for monitoring early response in patients with advanced cervical cancers undergoing concurrent chemo-radiotherapy vol.58, pp.11, 2017, https://doi.org/10.1177/0284185117694509
  15. The Value of Diffusion-Weighted Magnetic Resonance Imaging in Predicting the Efficacy of Radiation and Chemotherapy in Cervical Cancer vol.13, pp.1, 2018, https://doi.org/10.1515/biol-2018-0037
  16. Texture Analysis as Imaging Biomarker for recurrence in advanced cervical cancer treated with CCRT vol.8, pp.None, 2018, https://doi.org/10.1038/s41598-018-29838-0
  17. Prognostic model based on magnetic resonance imaging, whole-tumour apparent diffusion coefficient values and HPV genotyping for stage IB-IV cervical cancer patients following chemoradiotherapy vol.29, pp.2, 2019, https://doi.org/10.1007/s00330-018-5651-4
  18. Histogram analysis of apparent diffusion coefficient predicts response to radiofrequency ablation in hepatocellular carcinoma vol.31, pp.2, 2019, https://doi.org/10.21147/j.issn.1000-9604.2019.02.11
  19. MRI of cervical cancer with a surgical perspective: staging, prognostic implications and pitfalls vol.44, pp.7, 2013, https://doi.org/10.1007/s00261-019-01984-7
  20. Whole lesion histogram analysis of apparent diffusion coefficients on MRI predicts disease-free survival in locally advanced squamous cell cervical cancer after radical chemo-radiotherapy vol.19, pp.1, 2013, https://doi.org/10.1186/s12885-019-6344-3
  21. The usefulness of diffusion-weighted MRI in the differentiation between focal uterine endometrial soft tissue lesions vol.50, pp.1, 2019, https://doi.org/10.1186/s43055-019-0076-x
  22. Noninvasive Assessment of Liver Parenchyma Using Gray-Scale Ultrasound-Based Histogram Analysis in Patients With Chronic Hepatitis B Infection vol.36, pp.1, 2020, https://doi.org/10.1097/ruq.0000000000000438
  23. Impact of different b-value combinations on radiomics features of apparent diffusion coefficient in cervical cancer vol.61, pp.4, 2013, https://doi.org/10.1177/0284185119870157
  24. Radiomics in cervical cancer: Current applications and future potential vol.152, pp.None, 2020, https://doi.org/10.1016/j.critrevonc.2020.102985
  25. DCE‐MRI for early evaluation of therapeutic response in esophageal cancer after concurrent chemoradiotherapy and its values in predicting HIF ‐1α expr vol.10, pp.3, 2013, https://doi.org/10.1002/prm2.12049
  26. An MRI-based radiomics signature and clinical characteristics for survival prediction in early-stage cervical cancer vol.95, pp.1129, 2013, https://doi.org/10.1259/bjr.20210838