Journal of the Korean Society of Radiology (대한영상의학회지)

The Korean Society of Radiology (대한영상의학회)
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Response Prediction after Neoadjuvant Chemotherapy for Colon Cancer Using CT Tumor Regression Grade: A Preliminary Study

대장암 환자의 수술 전 항암화학요법의 반응을 CT 종양퇴행등급을 이용한 반응 예측: 예비 연구

  • Hwan Ju Je (Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • Seung Hyun Cho (Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • Hyun Seok Oh (Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • An Na Seo (Department of Pathology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • Byung Geon Park (Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • So Mi Lee (Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • See Hyung Kim (Department of Radiology, Kyungpook National University Hospital, School of Medicine, Kyungpook National University) ;
  • Gab Chul Kim (Department of Radiology, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University) ;
  • Hunkyu Ryeom (Department of Radiology, Kyungpook National University Hospital, School of Medicine, Kyungpook National University) ;
  • Gyu-Seog Choi (Department of Colorectal Cancer Centre, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University)
  • 제환주 (경북대학교 의과대학 칠곡경북대학교병원 영상의학과) ;
  • 조승현 (경북대학교 의과대학 칠곡경북대학교병원 영상의학과) ;
  • 오현석 (경북대학교 의과대학 칠곡경북대학교병원 영상의학과) ;
  • 서안나 (경북대학교 의과대학 칠곡경북대학교병원 병리학과) ;
  • 박병건 (경북대학교 의과대학 칠곡경북대학교병원 영상의학과) ;
  • 이소미 (경북대학교 의과대학 칠곡경북대학교병원 영상의학과) ;
  • 김시형 (경북대학교 의과대학 경북대학교병원 영상의학과) ;
  • 김갑철 (경북대학교 의과대학 칠곡경북대학교병원 영상의학과) ;
  • 염헌규 (경북대학교 의과대학 경북대학교병원 영상의학과) ;
  • 최규석 (경북대학교 의과대학 칠곡경북대학교병원 대장항문외과)
  • Received : 2022.08.30
  • Accepted : 2023.02.06
  • Published : 2023.09.01
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Abstract

Purpose To investigate whether CT-based tumor regression grade (ctTRG) can be used to predict the response to neoadjuvant chemotherapy (NAC) in colon cancer. Materials and Methods A total of 53 patients were enrolled. Two radiologists independently assessed the ctTRG using the length, thickness, layer pattern, and luminal and extraluminal appearance of the tumor. Changes in tumor volume were also analyzed using the 3D Slicer software. We evaluated the association between pathologic TRG (pTRG) and ctTRG. Patients with Rödel's TRG of 2, 3, or 4 were classified as responders. In terms of predicting responder and pathologic complete remission (pCR), receiver operating characteristic was compared between ctTRG and tumor volume change. Results There was a moderate correlation between ctTRG and pTRG (ρ = -0.540, p < 0.001), and the interobserver agreement was substantial (weighted κ = 0.672). In the prediction of responder, there was no significant difference between ctTRG and volumetry (Az = 0.749, criterion: ctTRG ≤ 3 for ctTRG, Az = 0.794, criterion: ≤ -27.1% for volume, p = 0.53). Moreover, there was no significant difference between the two methods in predicting pCR (p = 0.447). Conclusion ctTRG might predict the response to NAC in colon cancer. The diagnostic performance of ctTRG was comparable to that of CT volumetry.

목적 대장암 환자에서 선행화학요법(neoadjuvant chemotherapy; 이하 NAC)의 반응을 CT를 이용한 종양퇴행등급(CT-based tumor regression grade; 이하 ctTRG)으로 예측할 수 있는지를 알아보고자 한 연구이다. 대상과 방법 총 53명을 대상으로 NAC 전후 종양의 길이, 두께, 장벽의 패턴과 모양으로 ctTRG를 정하고 부피도 측정했다. 병리 종양퇴행등급(pathologic TRG; 이하 pTRG)을 반응 평가의 기준으로 ctTRG와 연관성을 평가했다. Rödel's TRG 2, 3 그리고 4를 반응군으로 분류하였다. ctTRG와 부피변화로 반응군 및 병리완전퇴행(pathologic complete remission; 이하 pCR)을 예측하는 성능을 비교하였다. 결과 ctTRG와 pTRG는 moderate의 연관성을 보였다(ρ = -0.540). 관찰자간 신뢰도는 substantial으로 보였다(weighted κ = 0.672). 반응군을 예측하는데 ctTRG와 volume 변화의 성능은 유의미한 차이를 보이지 않았다(ctTRG의 Az = 0.749, 반응기준: ctTRG ≤ 3, volume 변화의 Az = 0.794, 반응기준: ≤ -27.1%, p = 0.53). pCR을 예측하는 두 방법 간의 성능도 차이가 없었다(p = 0.447). 결론 ctTRG는 대장암에 NAC 후 반응을 예측할 수 있었고, 그 성능은 종양부피변화 방법과 차이가 없었다.

Keywords

References

  1. Andre T, Boni C, Navarro M, Tabernero J, Hickish T, Topham C, et al. Improved overall survival with oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment in stage II or III colon cancer in the MOSAIC trial. J Clin Oncol 2009;27:3109-3116 https://doi.org/10.1200/JCO.2008.20.6771
  2. Yothers G, O'Connell MJ, Allegra CJ, Kuebler JP, Colangelo LH, Petrelli NJ, et al. Oxaliplatin as adjuvant therapy for colon cancer: updated results of NSABP C-07 trial, including survival and subset analyses. J Clin Oncol 2011;29:3768-3774 https://doi.org/10.1200/JCO.2011.36.4539
  3. Kuebler JP, Wieand HS, O'Connell MJ, Smith RE, Colangelo LH, Yothers G, et al. Oxaliplatin combined with weekly bolus fluorouracil and leucovorin as surgical adjuvant chemotherapy for stage II and III colon cancer: results from NSABP C-07. J Clin Oncol 2007;25:2198-2204 https://doi.org/10.1200/JCO.2006.08.2974
  4. Sauer R, Becker H, Hohenberger W, Rodel C, Wittekind C, Fietkau R, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med 2004;351:1731-1740 https://doi.org/10.1056/NEJMoa040694
  5. Van Cutsem E, Kohne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A, et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009;360:1408-1417 https://doi.org/10.1056/NEJMoa0805019
  6. Seymour MT, Morton D. FOxTROT: an international randomised controlled trial in 1052 patients (pts) evaluating neoadjuvant chemotherapy (NAC) for colon cancer. J Clin Oncol 2019;37:3504
  7. Conroy T, Bosset JF, Etienne PL, Rio E, Francois E, Mesgouez-Nebout N, et al. Neoadjuvant chemotherapy with FOLFIRINOX and preoperative chemoradiotherapy for patients with locally advanced rectal cancer (UNICANCER-PRODIGE 23): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol 2021;22:702-715 https://doi.org/10.1016/S1470-2045(21)00079-6
  8. Foxtrot Collaborative Group. Feasibility of preoperative chemotherapy for locally advanced, operable colon cancer: the pilot phase of a randomised controlled trial. Lancet Oncol 2012;13:1152-1160 https://doi.org/10.1016/S1470-2045(12)70348-0
  9. van der Bij GJ, Oosterling SJ, Beelen RH, Meijer S, Coffey JC, van Egmond M. The perioperative period is an underutilized window of therapeutic opportunity in patients with colorectal cancer. Ann Surg 2009;249:727-734 https://doi.org/10.1097/SLA.0b013e3181a3ddbd
  10. Bayraktar UD, Chen E, Bayraktar S, Sands LR, Marchetti F, Montero AJ, et al. Does delay of adjuvant chemotherapy impact survival in patients with resected stage II and III colon adenocarcinoma? Cancer 2011;117:2364-2370 https://doi.org/10.1002/cncr.25720
  11. Biagi JJ, Raphael MJ, Mackillop WJ, Kong W, King WD, Booth CM. Association between time to initiation of adjuvant chemotherapy and survival in colorectal cancer: a systematic review and meta-analysis. JAMA 2011;305:2335-2342 https://doi.org/10.1001/jama.2011.749
  12. Arredondo J, Gonzalez I, Baixauli J, Martinez P, Rodriguez J, Pastor C, et al. Tumor response assessment in locally advanced colon cancer after neoadjuvant chemotherapy. J Gastrointest Oncol 2014;5:104-111
  13. Mori T. A comparison of the new (planned) TNM classification and Japanese general rule for staging colorectal cancer. Cancer Invest 2010;28:387-392 https://doi.org/10.1080/07357900903287055
  14. Lambregts DMJ, Boellaard TN, Beets-Tan RGH. Response evaluation after neoadjuvant treatment for rectal cancer using modern MR imaging: a pictorial review. Insights Imaging 2019;10:15
  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. Lee SM, Kim SH, Lee JM, Im SA, Bang YJ, Kim WH, et al. Usefulness of CT volumetry for primary gastric lesions in predicting pathologic response to neoadjuvant chemotherapy in advanced gastric cancer. Abdom Imaging 2009;34:430-440 https://doi.org/10.1007/s00261-008-9420-8
  17. Arredondo J, Simo V, Castanon C, Suarez MJ, Alvarez MC. Complete pathologic response after neoadjuvant chemotherapy in locally advanced colon cancer. Cir Esp (Engl Ed) 2020;98:168-170 https://doi.org/10.1016/j.ciresp.2019.06.003
  18. Martens MH, van Heeswijk MM, van den Broek JJ, Rao SX, Vandecaveye V, Vliegen RA, et al. Prospective, multicenter validation study of magnetic resonance volumetry for response assessment after preoperative chemoradiation in rectal cancer: can the results in the literature be reproduced? Int J Radiat Oncol Biol Phys 2015;93:1005-1014 https://doi.org/10.1016/j.ijrobp.2015.09.008
  19. Choi GS. Neoadjuvant FOLFOX chemotherapy for patients with locally advanced colon cancer. Available at. https://clinicaltrials.gov/ct2/show/NCT03426904?term=gyu+seog+choi&rank=4. Accessed October 20, 2022
  20. Park H, Cho SH, Kim JE, Moon SK, Park BG, Seo AN, et al. Potential image-based criteria of neoadjuvant chemotherapy for colon cancer: multireaders' diagnostic performance. Abdom Radiol (NY) 2020;45:2997-3006 https://doi.org/10.1007/s00261-019-02243-5
  21. 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
  22. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000;92:205-216 https://doi.org/10.1093/jnci/92.3.205
  23. Therasse P, Eisenhauer EA, Verweij J. RECIST revisited: a review of validation studies on tumour assessment. Eur J Cancer 2006;42:1031-1039 https://doi.org/10.1016/j.ejca.2006.01.026
  24. Hotker AM, Tarlinton L, Mazaheri Y, Woo KM, Gonen M, Saltz LB, et al. Multiparametric MRI in the assessment of response of rectal cancer to neoadjuvant chemoradiotherapy: a comparison of morphological, volumetric and functional MRI parameters. Eur Radiol 2016;26:4303-4312 https://doi.org/10.1007/s00330-016-4283-9
  25. 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
  26. Heger U, Bader F, Lordick F, Burian M, Langer R, Dobritz M, et al. Interim endoscopy results during neoadjuvant therapy for gastric cancer correlate with histopathological response and prognosis. Gastric Cancer 2014;17:478-488 https://doi.org/10.1007/s10120-013-0296-0
  27. Smith JJ, Chow OS, Gollub MJ, Nash GM, Temple LK, Weiser MR, et al. Organ preservation in rectal adenocarcinoma: a phase II randomized controlled trial evaluating 3-year disease-free survival in patients with locally advanced rectal cancer treated with chemoradiation plus induction or consolidation chemotherapy, and total mesorectal excision or nonoperative management. BMC Cancer 2015;15:767
  28. Gollub MJ, Das JP, Bates DDB, Fuqua JL 3rd, Golia Pernicka JS, Javed-Tayyab S, et al. Rectal cancer with complete endoscopic response after neoadjuvant therapy: what is the meaning of a positive MRI? Eur Radiol 2021;31:4731-4738 https://doi.org/10.1007/s00330-020-07657-0
  29. 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
  30. Park SH, Cho SH, Choi SH, Jang JK, Kim MJ, Kim SH, et al. MRI assessment of complete response to preoperative chemoradiation therapy for rectal cancer: 2020 guide for practice from the Korean Society of Abdominal Radiology. Korean J Radiol 2020;21:812-828 https://doi.org/10.3348/kjr.2020.0483
  31. Habr-Gama A, Perez RO, Wynn G, Marks J, Kessler H, Gama-Rodrigues J. Complete clinical response after neoadjuvant chemoradiation therapy for distal rectal cancer: characterization of clinical and endoscopic findings for standardization. Dis Colon Rectum 2010;53:1692-1698 https://doi.org/10.1007/DCR.0b013e3181f42b89
  32. Nakafusa Y, Tanaka T, Tanaka M, Kitajima Y, Sato S, Miyazaki K. Comparison of multivisceral resection and standard operation for locally advanced colorectal cancer: analysis of prognostic factors for short-term and long-term outcome. Dis Colon Rectum 2004;47:2055-2063 https://doi.org/10.1007/s10350-004-0716-7