Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Prognostic Value of Tumor Regression Grade on MR in Rectal Cancer: A Large-Scale, Single-Center Experience

  • Heera Yoen (Department of Radiology, Seoul National University Hospital) ;
  • Hye Eun Park (Department of Pathology, Seoul National University Hospital) ;
  • Se Hyung Kim (Department of Radiology, Seoul National University Hospital) ;
  • Jeong Hee Yoon (Department of Radiology, Seoul National University Hospital) ;
  • Bo Yun Hur (Department of Radiology, Healthcare System Gangnam Center, Seoul National University Hospital) ;
  • Jae Seok Bae (Department of Radiology, Seoul National University Hospital) ;
  • Jung Ho Kim (Department of Pathology, Seoul National University Hospital) ;
  • Hyeon Jeong Oh (Department of Pathology, Seoul National University Hospital) ;
  • Joon Koo Han (Department of Radiology, Seoul National University Hospital)
  • Received : 2019.10.25
  • Accepted : 2020.03.12
  • Published : 2020.09.01
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Abstract

Objective: To determine the prognostic value of MRI-based tumor regression grading (mrTRG) in rectal cancer compared with pathological tumor regression grading (pTRG), and to assess the effect of diffusion-weighted imaging (DWI) on interobserver agreement for evaluating mrTRG. Materials and Methods: Between 2007 and 2016, we retrospectively enrolled 321 patients (male:female = 208:113; mean age, 60.2 years) with rectal cancer who underwent both pre-chemoradiotherapy (CRT) and post-CRT MRI. Two radiologists independently determined mrTRG using a 5-point grading system with and without DWI in a one-month interval. Two pathologists graded pTRG using a 5-point grading system in consensus. Kaplan-Meier estimation and Cox-proportional hazard models were used for survival analysis. Cohen's kappa analysis was used to determine interobserver agreement. Results: According to mrTRG on MRI with DWI, there were 6 mrTRG 1, 48 mrTRG 2, 109 mrTRG 3, 152 mrTRG 4, and 6 mrTRG 5. By pTRG, there were 7 pTRG 1, 59 pTRG 2, 180 pTRG 3, 73 pTRG 4, and 2 pTRG 5. A 5-year overall survival (OS) was significantly different according to the 5-point grading mrTRG (p = 0.024) and pTRG (p = 0.038). The 5-year disease-free survival (DFS) was significantly different among the five mrTRG groups (p = 0.039), but not among the five pTRG groups (p = 0.072). OS and DFS were significantly different according to post-CRT MR variables: extramural venous invasion after CRT (hazard ratio = 2.259 for OS, hazard ratio = 5.011 for DFS) and extramesorectal lymph node (hazard ratio = 2.610 for DFS). For mrTRG, k value between the two radiologists was 0.309 (fair agreement) without DWI and slightly improved to 0.376 with DWI. Conclusion: mrTRG may predict OS and DFS comparably or even better compared to pTRG. The addition of DWI on T2-weighted MRI may improve interobserver agreement on mrTRG.

Keywords

Acknowledgement

This research was supported by the Basic Science Research Program of the National Research Foundation of Korea [NRF] funded by the Ministry of Science, ICT & Future Planning (NRF-2019R1F1A1060131) and from the Seoul National University Hospital Research Fund No. 04-2020-2010.

References

  1. Kapiteijn E, Marijnen CA, Nagtegaal ID, Putter H, Steup WH, Wiggers T, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 2001;345:638-646 https://doi.org/10.1056/NEJMoa010580
  2. Capirci C, Valentini V, Cionini L, De Paoli A, Rodel C, GlynneJones R, et al. Prognostic value of pathologic complete response after neoadjuvant therapy in locally advanced rectal cancer: long-term analysis of 566 ypCR patients. Int J Radiat Oncol Biol Phys 2008;72:99-107 https://doi.org/10.1016/j.ijrobp.2007.12.019
  3. Park IJ, You YN, Agarwal A, Skibber JM, Rodriguez-Bigas MA, Eng C, et al. Neoadjuvant treatment response as an early response indicator for patients with rectal cancer. J Clin Oncol 2012;30:1770-1776 https://doi.org/10.1200/JCO.2011.39.7901
  4. Rodel C, Martus P, Papadoupolos T, Fuzesi L, Klimpfinger M, Fietkau R, et al. Prognostic significance of tumor regression after preoperative chemoradiotherapy for rectal cancer. J Clin Oncol 2005;23:8688-8696 https://doi.org/10.1200/JCO.2005.02.1329
  5. Maas M, Nelemans PJ, Valentini V, Das P, Rodel C, Kuo LJ, et al. Long-term outcome in patients with a pathological complete response after chemoradiation for rectal cancer: a pooled analysis of individual patient data. Lancet Oncol 2010;11:835-844 https://doi.org/10.1016/S1470-2045(10)70172-8
  6. Dworak O, Keilholz L, Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy. Int J Colorectal Dis 1997;12:19-23 https://doi.org/10.1007/s003840050072
  7. Wheeler JM, Warren BF, Mortensen NJ, Ekanyaka N, Kulacoglu H, Jones AC, et al. Quantification of histologic regression of rectal cancer after irradiation: a proposal for a modified staging system. Dis Colon Rectum 2002;45:1051-1056 https://doi.org/10.1007/s10350-004-6359-x
  8. Vecchio FM, Valentini V, Minsky BD, Padula GD, Venkatraman ES, Balducci M, et al. The relationship of pathologic tumor regression grade (TRG) and outcomes after preoperative therapy in rectal cancer. Int J Radiat Oncol Biol Phys 2005;62:752-760 https://doi.org/10.1016/j.ijrobp.2004.11.017
  9. Seo N, Kim H, Cho MS, Lim JS. Response assessment with MRI after chemoradiotherapy in rectal cancer: current evidences. Korean J Radiol 2019;20:1003-1018 https://doi.org/10.3348/kjr.2018.0611
  10. Patel UB, Brown G, Rutten H, West N, Sebag-Montefiore D, Glynne-Jones R, et al. Comparison of magnetic resonance imaging and histopathological response to chemoradiotherapy in locally advanced rectal cancer. Ann Surg Oncol 2012;19:2842-2852 https://doi.org/10.1245/s10434-012-2309-3
  11. Kim YH, Kim DY, Kim TH, Jung KH, Chang HJ, Jeong SY, et al. Usefulness of magnetic resonance volumetric evaluation in predicting response to preoperative concurrent chemoradiotherapy in patients with resectable rectal cancer. Int J Radiat Oncol Biol Phys 2005;62:761-768 https://doi.org/10.1016/j.ijrobp.2004.11.005
  12. Kang JH, Kim YC, Kim H, Kim YW, Hur H, Kim JS, et al. Tumor volume changes assessed by three-dimensional magnetic resonance volumetry in rectal cancer patients after preoperative chemoradiation: the impact of the volume reduction ratio on the prediction of pathologic complete response. Int J Radiat Oncol Biol Phys 2010;76:1018-1025 https://doi.org/10.1016/j.ijrobp.2009.03.066
  13. Yeo SG, Kim DY, Park JW, Oh JH, Kim SY, Chang HJ, et al. Tumor volume reduction rate after preoperative chemoradiotherapy as a prognostic factor in locally advanced rectal cancer. Int J Radiat Oncol Biol Phys 2012;82:e193-e199 https://doi.org/10.1016/j.ijrobp.2011.03.022
  14. Xiao J, Tan Y, Li W, Gong J, Zhou Z, Huang Y, et al. Tumor volume reduction rate is superior to RECIST for predicting the pathological response of rectal cancer treated with neoadjuvant chemoradiation: results from a prospective study. Oncol Lett 2015;9:2680-2686 https://doi.org/10.3892/ol.2015.3101
  15. Patel UB, Taylor F, Blomqvist L, George C, Evans H, Tekkis P, et al. Magnetic resonance imaging-detected tumor response for locally advanced rectal cancer predicts survival outcomes: MERCURY experience. J Clin Oncol 2011;29:3753-3760 https://doi.org/10.1200/JCO.2011.34.9068
  16. Salerno G, Chandler I, Wotherspoon A, Thomas K, Moran B, Brown G. Sites of surgical wasting in the abdominoperineal specimen. Br J Surg 2008;95:1147-1154 https://doi.org/10.1002/bjs.6231
  17. Siddiqui MR, Gormly KL, Bhoday J, Balyansikova S, Battersby NJ, Chand M, et al. Interobserver agreement of radiologists assessing the response of rectal cancers to preoperative chemoradiation using the MRI tumour regression grading (mrTRG). Clin Radiol 2016;71:854-862 https://doi.org/10.1016/j.crad.2016.05.005
  18. Sclafani F, Brown G, Cunningham D, Wotherspoon A, Mendes LST, Balyasnikova S, et al. Comparison between MRI and pathology in the assessment of tumour regression grade in rectal cancer. Br J Cancer 2017;117:1478-1485 https://doi.org/10.1038/bjc.2017.320
  19. Kim SH, Lee JM, Hong SH, Kim GH, Lee JY, Han JK, et al. Locally advanced rectal cancer: added value of diffusion-weighted MR imaging in the evaluation of tumor response to neoadjuvant chemo- and radiation therapy. Radiology 2009;253:116-125 https://doi.org/10.1148/radiol.2532090027
  20. Elmi A, Hedgire SS, Covarrubias D, Abtahi SM, Hahn PF, Harisinghani M. Apparent diffusion coefficient as a non-invasive predictor of treatment response and recurrence in locally advanced rectal cancer. Clin Radiol 2013;68:e524-e531 https://doi.org/10.1016/j.crad.2013.05.094
  21. Moon SJ, Cho SH, Kim GC, Kim WH, Kim HJ, Shin KM, et al. Complementary value of pre-treatment apparent diffusion coefficient in rectal cancer for predicting tumor recurrence. Abdom Radiol (NY) 2016;41:1237-1244 https://doi.org/10.1007/s00261-016-0648-4
  22. Sassen S, de Booij M, Sosef M, Berendsen R, Lammering G, Clarijs R, et al. Locally advanced rectal cancer: is diffusion weighted MRI helpful for the identification of complete responders (ypT0N0) after neoadjuvant chemoradiation therapy? Eur Radiol 2013;23:3440-3449 https://doi.org/10.1007/s00330-013-2956-1
  23. Quirke P, Durdey P, Dixon MF, Williams NS. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 1986;2:996-999 https://doi.org/10.1016/S0140-6736(86)92612-7
  24. Quirke P, Dixon MF. The prediction of local recurrence in rectal adenocarcinoma by histopathological examination. Int J Colorectal Dis 1988;3:127-131 https://doi.org/10.1007/BF01645318
  25. Mandard AM, Dalibard F, Mandard JC, Marnay J, Henry-Amar M, Petiot JF, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer 1994;73:2680-2686 https://doi.org/10.1002/1097-0142(19940601)73:11<2680::AID-CNCR2820731105>3.0.CO;2-C
  26. Willett CG, Badizadegan K, Ancukiewicz M, Shellito PC. Prognostic factors in stage T3N0 rectal cancer: do all patients require postoperative pelvic irradiation and chemotherapy? Dis Colon Rectum 1999;42:167-173 https://doi.org/10.1007/BF02237122
  27. Lee SY, Kim CH, Kim YJ, Kim HR. Oncologic outcomes according to the treatment strategy in radiologic complete responders after neoadjuvant chemoradiation for rectal cancer. Oncology 2015;89:311-318 https://doi.org/10.1159/000439279
  28. Jang JK, Lee JL, Park SH, Park HJ, Park IJ, Kim JH, et al. Magnetic resonance tumour regression grade and pathological correlates in patients with rectal cancer. Br J Surg 2018;105:1671-1679 https://doi.org/10.1002/bjs.10898
  29. Chetty R, Gill P, Govender D, Bateman A, Chang HJ, Deshpande V, et al. International study group on rectal cancer regression grading: interobserver variability with commonly used regression grading systems. Hum Pathol 2012;43:1917-1923 https://doi.org/10.1016/j.humpath.2012.01.020
  30. Lee ES, Kim MJ, Park SC, Hur BY, Hyun JH, Chang HJ, et al. Magnetic resonance imaging-detected extramural venous invasion in rectal cancer before and after preoperative chemoradiotherapy: diagnostic performance and prognostic significance. Eur Radiol 2018;28:496-505 https://doi.org/10.1007/s00330-017-4978-6