Skip to main content
Top
Published in: Surgery Today 9/2021

01-09-2021 | Computed Tomography | Original Article

Prediction of the tumor response and survival based on computed tomography in esophageal squamous cell carcinoma after trimodality therapy

Authors: Ryosuke Hirohata, Yoichi Hamai, Manabu Emi, Tomoaki Kurokawa, Toru Yoshikawa, Manato Ohsawa, Kazuki Tadokoro, Morihito Okada

Published in: Surgery Today | Issue 9/2021

Login to get access

Abstract

Purpose

Predicting the response to neoadjuvant chemoradiotherapy (NCRT) and the prognosis of esophageal squamous cell carcinoma (ESCC) is challenging. This study evaluated the potential of a preoperative computed tomography (CT) analysis for predicting the pathological response and survival of patients with ESCC who received trimodality therapy.

Methods

A total of 119 patients with cT3 or T4 ESCC who underwent surgery following NCRT between 2007 and 2019 were assessed. The CT-based parameters were measured with enhanced CT preoperatively, prior to and during treatment. Associations between these parameters and the pathologic response, as well as the prognosis, were examined.

Results

Pretreatment maximum CT value (p = 0.009), pretreatment mean CT value (p = 0.022), preoperative whole tumor volume (WTV, p = 0.003), preoperative largest cross section (LCS, p = 0.002), ΔLCS (pretreatment to preoperative, p = 0.004), ΔWTV (pretreatment to preoperative, p = 0.012), and Δmean CT value (pretreatment to preoperative, p = 0.012) of the primary lesion were significantly associated with a good pathological response. A Cox-regression analysis of recurrence-free survival (RFS) and overall survival (OS) showed that preoperative LCS was an independent CT-based predictor. RFS and OS were significantly higher at the optimal cut-off value of the preoperative LCS (p = 0.036 and p = 0.016, respectively).

Conclusions

CT-based parameters are thus considered to be valuable predictors of the tumor response and survival after trimodality therapy for ESCC.
Appendix
Available only for authorised users
Literature
1.
go back to reference Sjoquist KM, Burmeister BH, Smithers BM, Zalcberg JR, Sumes RJ, Barbour A, et al. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. Lancet Oncol. 2011;12:681–92.CrossRef Sjoquist KM, Burmeister BH, Smithers BM, Zalcberg JR, Sumes RJ, Barbour A, et al. Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis. Lancet Oncol. 2011;12:681–92.CrossRef
2.
go back to reference van Hagen P, Hulshof MC, van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366:2074–84.CrossRef van Hagen P, Hulshof MC, van Lanschot JJ, Steyerberg EW, van Berge Henegouwen MI, Wijnhoven BP, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366:2074–84.CrossRef
3.
go back to reference Donahue JM, Nichols FC, Li Z, Schomas DA, Allen MS, Cassici SD, et al. Complete pathologic response after neoadjuvant chemoradiotherapy for esophageal cancer is associated with enhanced survival. Ann Thorac Surg. 2009;87:392–9.CrossRef Donahue JM, Nichols FC, Li Z, Schomas DA, Allen MS, Cassici SD, et al. Complete pathologic response after neoadjuvant chemoradiotherapy for esophageal cancer is associated with enhanced survival. Ann Thorac Surg. 2009;87:392–9.CrossRef
4.
go back to reference Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG 9907). Ann Surg Oncol. 2012;19:68–74.CrossRef Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG 9907). Ann Surg Oncol. 2012;19:68–74.CrossRef
5.
go back to reference Nakamura K, Kato K, Igaki H, Ito Y, Mizusawa J, Ando N, et al. Three-arm phase III trial comparing cisplatin plus 5-FU (CF) versus docetaxel, cisplatin plus 5-FU (DCF) versus radiotherapy with CF (CF-RT) as preoperative therapy for locally advanced esophageal cancer (JCOG 1109, NExT study). Jpn J Clin Oncol. 2013;43:752–5.CrossRef Nakamura K, Kato K, Igaki H, Ito Y, Mizusawa J, Ando N, et al. Three-arm phase III trial comparing cisplatin plus 5-FU (CF) versus docetaxel, cisplatin plus 5-FU (DCF) versus radiotherapy with CF (CF-RT) as preoperative therapy for locally advanced esophageal cancer (JCOG 1109, NExT study). Jpn J Clin Oncol. 2013;43:752–5.CrossRef
6.
go back to reference van Hagen P, Hulshof MC, van Lanschot JJ, Steterberg EW, van Berge Henegouwen MI, Wijnhoven BP, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366:2074–84.CrossRef van Hagen P, Hulshof MC, van Lanschot JJ, Steterberg EW, van Berge Henegouwen MI, Wijnhoven BP, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med. 2012;366:2074–84.CrossRef
7.
go back to reference Ajani JA, D’Amico TA, Bentrem DJ, Chao J, Corvera C, Das P, et al. Esophageal and esophagogastric junction cancers, version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2019;17:855–83.CrossRef Ajani JA, D’Amico TA, Bentrem DJ, Chao J, Corvera C, Das P, et al. Esophageal and esophagogastric junction cancers, version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2019;17:855–83.CrossRef
8.
go back to reference Berger AC, Farma J, Scott WJ, Freedman G, Weiner L, Cheng JD, et al. Complete response to neoadjuvant chemoradiotherapy in esophageal carcinoma is associated with significantly improved survival. J Clin Oncol. 2005;23:4330–7.CrossRef Berger AC, Farma J, Scott WJ, Freedman G, Weiner L, Cheng JD, et al. Complete response to neoadjuvant chemoradiotherapy in esophageal carcinoma is associated with significantly improved survival. J Clin Oncol. 2005;23:4330–7.CrossRef
9.
go back to reference Hamai Y, Hihara J, Emi M, Furukawa T, Murakami Y, Nishibuchi I, et al. Evaluation of prognostic factors for esophageal squamous cell carcinoma treated with neoadjuvant chemoradiotherapy followed by surgery. World J Surg. 2018;42:1496–505.CrossRef Hamai Y, Hihara J, Emi M, Furukawa T, Murakami Y, Nishibuchi I, et al. Evaluation of prognostic factors for esophageal squamous cell carcinoma treated with neoadjuvant chemoradiotherapy followed by surgery. World J Surg. 2018;42:1496–505.CrossRef
10.
go back to reference Tepper J, Krasna MJ, Niedzwiecki D, Hollis D, Reed CE, Goldberg R, et al. Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol. 2008;26:1086–92.CrossRef Tepper J, Krasna MJ, Niedzwiecki D, Hollis D, Reed CE, Goldberg R, et al. Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. J Clin Oncol. 2008;26:1086–92.CrossRef
11.
go back to reference Reynolds JV, Muldoon C, Hollywood D, Ravi N, Rowley S, O’Byrne K, et al. Long-term outcomes following neoadjuvant chemoradiotherapy for esophageal cancer. Ann Surg. 2007;245:707–16.CrossRef Reynolds JV, Muldoon C, Hollywood D, Ravi N, Rowley S, O’Byrne K, et al. Long-term outcomes following neoadjuvant chemoradiotherapy for esophageal cancer. Ann Surg. 2007;245:707–16.CrossRef
12.
go back to reference Shapiro J, van Lanschot JJB, Hulshof M, van Hegen P, van Berge HMI, Wijnhoven BPL, et al. Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial. Lancet Oncol. 2015;16:1090–8.CrossRef Shapiro J, van Lanschot JJB, Hulshof M, van Hegen P, van Berge HMI, Wijnhoven BPL, et al. Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): long-term results of a randomised controlled trial. Lancet Oncol. 2015;16:1090–8.CrossRef
13.
go back to reference Hamai Y, Hihara J, Emi M, Furukawa T, Murakami Y, Nishibuchi I, et al. Preoperative prediction of a pathologic complete response of esophageal squamous cell carcinoma to neoadjuvant chemoradiotherapy. Surgery. 2018;164:40–8.CrossRef Hamai Y, Hihara J, Emi M, Furukawa T, Murakami Y, Nishibuchi I, et al. Preoperative prediction of a pathologic complete response of esophageal squamous cell carcinoma to neoadjuvant chemoradiotherapy. Surgery. 2018;164:40–8.CrossRef
14.
go back to reference Ohsawa M, Hamai Y, Emi M, Takaoki F, Ibuki Y, Tokmoaki K, et al. Tumor response in esophageal squamous cell carcinoma treated with neoadjuvant chemotherapy followed by surgery. Anticancer Res. 2020;40:1153–60.CrossRef Ohsawa M, Hamai Y, Emi M, Takaoki F, Ibuki Y, Tokmoaki K, et al. Tumor response in esophageal squamous cell carcinoma treated with neoadjuvant chemotherapy followed by surgery. Anticancer Res. 2020;40:1153–60.CrossRef
15.
go back to reference Hamai Y, Hihara J, Taomoto J, Yamakita I, Ibuki Y, Okada M, et al. Effects of neoadjuvant chemoradiotherapy on postoperative morbidity and mortality associated with esophageal cancer. Dis Esophagus. 2015;28:358–64.CrossRef Hamai Y, Hihara J, Taomoto J, Yamakita I, Ibuki Y, Okada M, et al. Effects of neoadjuvant chemoradiotherapy on postoperative morbidity and mortality associated with esophageal cancer. Dis Esophagus. 2015;28:358–64.CrossRef
16.
go back to reference Hamai Y, Hihara J, Emi M, Murakami Y, Kenjo M, Nagata Y, et al. Results of neoadjuvant chemoradiotherapy with docetaxel and 5-fluorouracil followed by esophagectomy to treat locally advanced esophageal cancer. Ann Thorac Surg. 2015;99:1887–93.CrossRef Hamai Y, Hihara J, Emi M, Murakami Y, Kenjo M, Nagata Y, et al. Results of neoadjuvant chemoradiotherapy with docetaxel and 5-fluorouracil followed by esophagectomy to treat locally advanced esophageal cancer. Ann Thorac Surg. 2015;99:1887–93.CrossRef
17.
go back to reference Emi M, Hihara J, Hamai Y, Aoki Y, Okada M, Kenjo M, et al. Neoadjuvant chemoradiotherapy with docetaxel, cisplatin, and 5-fluorouracil for esophageal cancer. Cancer Chemother Pharmacol. 2012;69:1499–505.CrossRef Emi M, Hihara J, Hamai Y, Aoki Y, Okada M, Kenjo M, et al. Neoadjuvant chemoradiotherapy with docetaxel, cisplatin, and 5-fluorouracil for esophageal cancer. Cancer Chemother Pharmacol. 2012;69:1499–505.CrossRef
18.
go back to reference Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: part II and III. Esophagus. 2017;14:37–65.CrossRef Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: part II and III. Esophagus. 2017;14:37–65.CrossRef
19.
go back to reference Agrawal N, Jiao Y, Bettegowda C, Hutfless SM, Wang Y, David S, et al. Comparative genomic analysis of esophageal adenocarcinoma and squamous cell carcinoma. Cancer Discov. 2012;2:899–905.CrossRef Agrawal N, Jiao Y, Bettegowda C, Hutfless SM, Wang Y, David S, et al. Comparative genomic analysis of esophageal adenocarcinoma and squamous cell carcinoma. Cancer Discov. 2012;2:899–905.CrossRef
20.
go back to reference Ohashi S, Miyamoto S, Kikuchi O, Kikuchi O, Goto T, Amanuma Y, et al. Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology. 2015;149:1700–15.CrossRef Ohashi S, Miyamoto S, Kikuchi O, Kikuchi O, Goto T, Amanuma Y, et al. Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology. 2015;149:1700–15.CrossRef
21.
go back to reference Sepesi B, Schmidt HE, Lada M, Correa AM, Walsh GL, Mehran RJ, et al. Survival in patients with esophageal adenocarcinoma undergoing trimodality therapy is independent of regional lymph node location. Ann Thorac Surg. 2016;101:1075–80.CrossRef Sepesi B, Schmidt HE, Lada M, Correa AM, Walsh GL, Mehran RJ, et al. Survival in patients with esophageal adenocarcinoma undergoing trimodality therapy is independent of regional lymph node location. Ann Thorac Surg. 2016;101:1075–80.CrossRef
22.
go back to reference Chen WH, Huang YL, Chao YK, Yeh CJ, Cheng HK, Tseng CK, et al. Prognostic significance of lymphovascular invasion in patients with esophageal squamous cell carcinoma treated with neoadjuvant chemoradiotherapy. Ann Surg Oncol. 2015;22:338–43.CrossRef Chen WH, Huang YL, Chao YK, Yeh CJ, Cheng HK, Tseng CK, et al. Prognostic significance of lymphovascular invasion in patients with esophageal squamous cell carcinoma treated with neoadjuvant chemoradiotherapy. Ann Surg Oncol. 2015;22:338–43.CrossRef
23.
go back to reference Heneghan HM, Donohoe C, Elliot J, Ahmed Z, Malik V, Ravi N, et al. Can CT-PET and endoscopic assessment post-neoadjuvant chemoradiotherapy predict residual disease in esophageal cancer? Ann Surg. 2016;264:831–8.CrossRef Heneghan HM, Donohoe C, Elliot J, Ahmed Z, Malik V, Ravi N, et al. Can CT-PET and endoscopic assessment post-neoadjuvant chemoradiotherapy predict residual disease in esophageal cancer? Ann Surg. 2016;264:831–8.CrossRef
24.
go back to reference Eyck BM, Onstenk BD, Noordman BJ, Bieboer D, Spaander MCW, Valkema R, et al. Accuracy of detecting residual disease after neoadjuvant chemoradiotherapy for esophageal cancer: a systematic review and meta-analysis. Ann Surg. 2020;271:245–56.CrossRef Eyck BM, Onstenk BD, Noordman BJ, Bieboer D, Spaander MCW, Valkema R, et al. Accuracy of detecting residual disease after neoadjuvant chemoradiotherapy for esophageal cancer: a systematic review and meta-analysis. Ann Surg. 2020;271:245–56.CrossRef
25.
go back to reference Hamai Y, Hihara J, Emi M, Furukawa T, Yamakita I, Kurokawa T, et al. Ability of fluorine-18 fluorodeoxyglucose positron emission tomography to predict outcomes of neoadjuvant chemoradiotherapy followed by surgical treatment for esophageal squamous cell carcinoma. Ann Thorac Surg. 2016;102:1132–9.CrossRef Hamai Y, Hihara J, Emi M, Furukawa T, Yamakita I, Kurokawa T, et al. Ability of fluorine-18 fluorodeoxyglucose positron emission tomography to predict outcomes of neoadjuvant chemoradiotherapy followed by surgical treatment for esophageal squamous cell carcinoma. Ann Thorac Surg. 2016;102:1132–9.CrossRef
26.
go back to reference Hamai Y, Emi M, Ibuki Y, Murakami Y, Nishibuchi I, Nagata Y, et al. Predictions of pathological features and recurrence based on FDG-PET findings of esophageal squamous cell carcinoma after trimodal therapy. Ann Surg Oncol. 2020;27:4422–30.CrossRef Hamai Y, Emi M, Ibuki Y, Murakami Y, Nishibuchi I, Nagata Y, et al. Predictions of pathological features and recurrence based on FDG-PET findings of esophageal squamous cell carcinoma after trimodal therapy. Ann Surg Oncol. 2020;27:4422–30.CrossRef
27.
go back to reference Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.CrossRef Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.CrossRef
28.
go back to reference Wakatsuki K, Matsumoto S, Migita K, Ito M, Kunishige T, Nakatani M, et al. Usefulness of computed tomography density of a tumor in predicting the response of advanced esophageal cancer to preoperative chemotherapy. Surgery. 2017;162:823–35.CrossRef Wakatsuki K, Matsumoto S, Migita K, Ito M, Kunishige T, Nakatani M, et al. Usefulness of computed tomography density of a tumor in predicting the response of advanced esophageal cancer to preoperative chemotherapy. Surgery. 2017;162:823–35.CrossRef
29.
go back to reference Zhang XY, Yan WP, Sun Y, Li XT, Chen Y, Fan MY, et al. CT Signs can predict treatment response and long-term survival: a study in locally advanced esophageal cancer with preoperative chemotherapy. Ann Surg Oncol. 2015;22(Suppl 3):S1380–7.CrossRef Zhang XY, Yan WP, Sun Y, Li XT, Chen Y, Fan MY, et al. CT Signs can predict treatment response and long-term survival: a study in locally advanced esophageal cancer with preoperative chemotherapy. Ann Surg Oncol. 2015;22(Suppl 3):S1380–7.CrossRef
30.
go back to reference Ng F, Kozarski R, Ganeshan B, Goh V. Assessment of tumor heterogeneity by CT texture analysis: can the largest cross-sectional area be used as an alternative to whole tumor analysis? Eur J Radiol. 2013;82:342–8.CrossRef Ng F, Kozarski R, Ganeshan B, Goh V. Assessment of tumor heterogeneity by CT texture analysis: can the largest cross-sectional area be used as an alternative to whole tumor analysis? Eur J Radiol. 2013;82:342–8.CrossRef
31.
go back to reference Sandrasegaran K, Lin Y, Asare-Sawiri M, Taiyuni T, Tann M. CT texture analysis of pancreatic cancer. Eur Radiol. 2019;29:1067–73.CrossRef Sandrasegaran K, Lin Y, Asare-Sawiri M, Taiyuni T, Tann M. CT texture analysis of pancreatic cancer. Eur Radiol. 2019;29:1067–73.CrossRef
32.
go back to reference Ganeshan B, Goh V, Mandeville HC, Ng QS, Hoskin PJ, Miles KA. Non-small cell lung cancer: histopathologic correlates for texture parameters at CT. Radiology. 2013;266:326–36.CrossRef Ganeshan B, Goh V, Mandeville HC, Ng QS, Hoskin PJ, Miles KA. Non-small cell lung cancer: histopathologic correlates for texture parameters at CT. Radiology. 2013;266:326–36.CrossRef
33.
go back to reference Yip C, Landau D, Kozarski R, Kozarski R, Geneshan B, Thomas R, et al. Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology. 2014;270:141–8.CrossRef Yip C, Landau D, Kozarski R, Kozarski R, Geneshan B, Thomas R, et al. Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology. 2014;270:141–8.CrossRef
34.
go back to reference Swisher SG, Maish M, Erasmus JJ, Correa AM, Ajani JA, Bresalier R, et al. Utility of PET, CT, and EUS to identify pathologic responders in esophageal cancer. Ann Thorac Surg. 2004;78:1152–60.CrossRef Swisher SG, Maish M, Erasmus JJ, Correa AM, Ajani JA, Bresalier R, et al. Utility of PET, CT, and EUS to identify pathologic responders in esophageal cancer. Ann Thorac Surg. 2004;78:1152–60.CrossRef
35.
go back to reference Hayano K, Shuto K, Satoh A, Aoyagi T, Narushima K, Gunji H, et al. Tumor blood flow change measured by CT perfusion during chemoradiation therapy (CRT) for monitoring response and predicting survival in patients with esophageal cancer. Esophagus. 2014;11:72–9.CrossRef Hayano K, Shuto K, Satoh A, Aoyagi T, Narushima K, Gunji H, et al. Tumor blood flow change measured by CT perfusion during chemoradiation therapy (CRT) for monitoring response and predicting survival in patients with esophageal cancer. Esophagus. 2014;11:72–9.CrossRef
Metadata
Title
Prediction of the tumor response and survival based on computed tomography in esophageal squamous cell carcinoma after trimodality therapy
Authors
Ryosuke Hirohata
Yoichi Hamai
Manabu Emi
Tomoaki Kurokawa
Toru Yoshikawa
Manato Ohsawa
Kazuki Tadokoro
Morihito Okada
Publication date
01-09-2021
Publisher
Springer Singapore
Published in
Surgery Today / Issue 9/2021
Print ISSN: 0941-1291
Electronic ISSN: 1436-2813
DOI
https://doi.org/10.1007/s00595-021-02277-7

Other articles of this Issue 9/2021

Surgery Today 9/2021 Go to the issue