Pathologic assessment of esophageal cancer following neoadjuvant therapy_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

FENG Xijia , CHEN Xiaoyan ,  LI Hecheng

Department of Thoracic Surgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, P. R. China;

Corresponding author：

LI Hecheng, Email: lihecheng2000@hotmail.com

Keywords：

Esophageal cancer; neoadjuvant therapy; efficacy evaluation; tumor regression grading; review

DOI：

10.7507/1007-4848.202109052

Video：

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China is a country with a high incidence of esophageal cancer. Most patients are already in the locally advanced stage when first diagnosed. Preoperative neoadjuvant therapy followed by surgery has become the standard treatment mode for them. Closely related to prognosis, the evaluation of tumor response is essential. Response evaluation criteria in solid tumors is the gold standard to evaluate tumor response, but the lesions must meet the measurement standards. Tumor regression grading (TRG) systems are designed to classify regressive changes after neoadjuvant treatment based on histopathological results to reveal prognostic information. Concentrating on pathologic assessment of esophageal cancer following neoadjuvant therapy, this article reviews histopathological changes, commonly used TRG systems and current debate.

Citation： FENG Xijia, CHEN Xiaoyan, LI Hecheng. Pathologic assessment of esophageal cancer following neoadjuvant therapy. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(3): 476-482. doi: 10.7507/1007-4848.202109052 Copy

1.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2.	Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin, 2020, 70(1): 7-30.
3.	Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
4.	Feng RM, Zong YN, Cao SM, et al. Current cancer situation in China: Good or bad news from the 2018 global cancer statistics? Cancer Commun (Lond), 2019, 39(1): 22.
5.	Yang H, Liu H, Chen Y, et al. Neoadjuvant chemoradiotherapy followed by surgery versus surgery alone for locally advanced squamous cell carcinoma of the esophagus (NEOCRTEC5010): A phase Ⅲ multicenter, randomized, open-label clinical trial. J Clin Oncol, 2018, 36(27): 2796-2803.
6.	Watanabe M, Otake R, Kozuki R, et al. Recent progress in multidisciplinary treatment for patients with esophageal cancer. Surg Today, 2020, 50(1): 12-20.
7.	Shah MA, Kennedy EB, Catenacci DV, et al. Treatment of locally advanced esophageal carcinoma: ASCO guideline. J Clin Oncol, 2020, 38(23): 2677-2694.
8.	Puetz K, Bollschweiler E, Semrau R, et al. Neoadjuvant chemoradiation for patients with advanced oesophageal cancer—Which response grading system best impacts prognostic discrimination? Histopathology, 2019, 74(5): 731-743.
9.	Therasse P, Arbuck SG, Eisenhauer EA, 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(3): 205-216.
10.	Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1. 1). Eur J Cancer, 2009, 45(2): 228-247.
11.	Kurokawa Y, Shibata T, Ando N, et al. Which is the optimal response criteria for evaluating preoperative treatment in esophageal cancer: RECIST or histology? Ann Surg Oncol, 2013, 20(9): 3009-3014.
12.	Miyata H, Tanaka K, Makino T, et al. The impact of pathological tumor regression and nodal status on survival and systemic disease in patients undergoing neoadjuvant chemotherapy for esophageal squamous cell carcinoma. Ann Surg Oncol, 2018, 25(8): 2409-2417.
13.	Pai RK, Pai RK. Pathologic assessment of gastrointestinal tract and pancreatic carcinoma after neoadjuvant therapy. Mod Pathol, 2018, 31(1): 4-23.
14.	Lam AK. Esophageal squamous cell carcinoma methods and protocols: Methods and protocols. Meth Mol Biol. 2020.
15.	Tong Y, Liu D, Zhang J. Connection and distinction of tumor regression grading systems of gastrointestinal cancer. Pathol Res Pract, 2020, 216(9): 153073.
16.	Mandard AM, Dalibard F, Mandard JC, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer, 1994, 73(11): 2680-2686.
17.	Ryan R, Gibbons D, Hyland JM, et al. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology, 2005, 47(2): 141-146.
18.	Chirieac LR, Swisher SG, Correa AM, et al. Signet-ring cell or mucinous histology after preoperative chemoradiation and survival in patients with esophageal or esophagogastric junction adenocarcinoma. Clin Cancer Res, 2005, 11(6): 2229-2236.
19.	Yamasaki T, Ishii N, Okuno T, et al. A case of esophageal squamous cell carcinoma with neuroendocrine, basaloid, and ciliated glandular differentiation. Clin J Gastroenterol, 2021, 14(1): 32-38.
20.	Wang KL, Yang Q, Cleary KR, et al. The significance of neuroendocrine differentiation in adenocarcinoma of the esophagus and esophagogastric junction after preoperative chemoradiation. Cancer, 2006, 107(7): 1467-1474.
21.	Waters KM, Salimian KJ, Assarzadegan N, et al. Cell polarity (the 'four lines') distinguishes gastric dysplasia from epithelial changes in reactive gastropathy. Histopathology, 2021, 78(3): 453-458.
22.	Wu Y, Sang J, Zhou J, et al. Comparative analysis of differences between preoperative endoscopic biopsy and postoperative pathological examination for diagnosis of gastric intraepithelial neoplasia. J Int Med Res, 2021, 49(3): 300060521994929.
23.	Brien TP, Farraye FA, Odze RD. Gastric dysplasia-like epithelial atypia associated with chemoradiotherapy for esophageal cancer: A clinicopathologic and immunohistochemical study of 15 cases. Mod Pathol, 2001, 14(5): 389-396.
24.	Okuno K, Tanaka A, Yoshikawa H, et al. A new preoperative immunochemotherapy for the treatment of locally advanced esophageal cancer. Hepatogastroenterology, 1998, 45(22): 950-953.
25.	College of American Pathologists. Cancer protocol templates. URL: https://www.cap.org/protocols-and-guidelines/cancer-reporting-tools/cancer-protocol-templates. Last accessed June 11, 2021.
26.	中国临床肿瘤学会指南工作委员会. 中国临床肿瘤学会 (CSCO) 食管癌诊疗指南 2020. 北京: 人民卫生出版社, 2020.
27.	Becker K, Mueller JD, Schulmacher C, et al. Histomorphology and grading of regression in gastric carcinoma treated with neoadjuvant chemotherapy. Cancer, 2003, 98(7): 1521-1530.
28.	Schneider PM, Baldus SE, Metzger R, et al. Histomorphologic tumor regression and lymph node metastases determine prognosis following neoadjuvant radiochemotherapy for esophageal cancer: Implications for response classification. Ann Surg, 2005, 242(5): 684-692.
29.	Chirieac LR, Swisher SG, Ajani JA, et al. Posttherapy pathologic stage predicts survival in patients with esophageal carcinoma receiving preoperative chemoradiation. Cancer, 2005, 103(7): 1347-1355.
30.	Swisher SG, Hofstetter W, Wu TT, et al. Proposed revision of the esophageal cancer staging system to accommodate pathologic response (pP) following preoperative chemoradiation (CRT). Ann Surg, 2005, 241(5): 810-817.
31.	Wu TT, Chirieac LR, Abraham SC, et al. Excellent interobserver agreement on grading the extent of residual carcinoma after preoperative chemoradiation in esophageal and esophagogastric junction carcinoma: A reliable predictor for patient outcome. Am J Surg Pathol, 2007, 31(1): 58-64.
32.	Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅠ. Esophagus, 2017, 14(1): 1-36.
33.	Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer, 2011, 14(2): 101-112.
34.	Nieman DR, Peyre CG, Watson TJ, et al. Neoadjuvant treatment response in negative nodes is an important prognosticator after esophagectomy. Ann Thorac Surg, 2015, 99(1): 277-283.
35.	Castoro C, Scarpa M, Cagol M, et al. Nodal metastasis from locally advanced esophageal cancer: How neoadjuvant therapy modifies their frequency and distribution. Ann Surg Oncol, 2011, 18(13): 3743-3754.
36.	Klevebro F, Tsekrekos A, Low D, et al. Relevant issues in tumor regression grading of histopathological response to neoadjuvant treatment in adenocarcinomas of the esophagus and gastroesophageal junction. Dis Esophagus, 2020, 33(6): doaa005.
37.	Hsu PK, Yeh YC, Chien LI, et al. Clinicopathological significance of pathologic complete lymph node regression after neoadjuvant chemoradiotherapy in esophageal squamous cell carcinoma. Ann Surg Oncol, 2021, 28(4): 2048-2058.
38.	Hagi T, Makino T, Yamasaki M, et al. Pathological regression of lymph nodes better predicts long-term survival in esophageal cancer patients undergoing neoadjuvant chemotherapy followed by surgery. Ann Surg, 2022, 275(6): 1121-1129.
39.	Davies AR, Myoteri D, Zylstra J, et al. Lymph node regression and survival following neoadjuvant chemotherapy in oesophageal adenocarcinoma. Br J Surg, 2018, 105(12): 1639-1649.
40.	Groth SS, Burt BM, Farjah F, et al. Prognostic value of neoadjuvant treatment response in locally advanced esophageal adenocarcinoma. J Thorac Cardiovasc Surg, 2019, 157(4): 1682-1693.
41.	Langer R, Becker K. Tumor regression grading of gastrointestinal cancers after neoadjuvant therapy. Virchows Arch, 2018, 472(2): 175-186.
42.	Westerhoff M, Osecky M, Langer R. Varying practices in tumor regression grading of gastrointestinal carcinomas after neoadjuvant therapy: Results of an international survey. Mod Pathol, 2020, 33(4): 676-689.
43.	Saliba G, Detlefsen S, Carneiro F, et al. Tumor regression grading after neoadjuvant treatment of esophageal and gastroesophageal junction adenocarcinoma: Results of an international Delphi consensus survey. Hum Pathol, 2021, 108: 60-67.
44.	Tsekrekos A, Detlefsen S, Riddell R, et al. Histopathologic tumor regression grading in patients with gastric carcinoma submitted to neoadjuvant treatment: Results of a Delphi survey. Hum Pathol, 2019, 84: 26-34.
45.	Donohoe CL, O'Farrell NJ, Grant T, et al. Classification of pathologic response to neoadjuvant therapy in esophageal and junctional cancer: Assessment of existing measures and proposal of a novel 3-point standard. Ann Surg, 2013, 258(5): 784-792.
46.	Tomasello G, Petrelli F, Ghidini M, et al. Tumor regression grade and survival after neoadjuvant treatment in gastro-esophageal cancer: A meta-analysis of 17 published studies. Eur J Surg Oncol, 2017, 43(9): 1607-1616.
47.	Karamitopoulou E, Thies S, Zlobec I, et al. Assessment of tumor regression of esophageal adenocarcinomas after neoadjuvant chemotherapy: Comparison of 2 commonly used scoring approaches. Am J Surg Pathol, 2014, 38(11): 1551-1556.
48.	Li C, Zhao S, Zheng Y, et al. Preoperative pembrolizumab combined with chemoradiotherapy for oesophageal squamous cell carcinoma (PALACE-1). Eur J Cancer, 2021, 144: 232-241.
49.	Kato K, Shah MA, Enzinger P, et al. KEYNOTE-590: Phase Ⅲ study of first-line chemotherapy with or without pembrolizumab for advanced esophageal cancer. Future Oncol, 2019, 15(10): 1057-1066.
50.	Shen D, Chen Q, Wu J, et al. The safety and efficacy of neoadjuvant PD-1 inhibitor with chemotherapy for locally advanced esophageal squamous cell carcinoma. J Gastrointest Oncol, 2021, 12(1): 1-10.
51.	Urabe M, Ushiku T, Seto Y, et al. Pathologic response of HER2-positive gastric cancer to trastuzumab-based chemotherapy. Am J Surg Pathol, 2016, 40(10): 1326-1333.

1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin, 2020, 70(1): 7-30.
3. Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
4. Feng RM, Zong YN, Cao SM, et al. Current cancer situation in China: Good or bad news from the 2018 global cancer statistics? Cancer Commun (Lond), 2019, 39(1): 22.
5. Yang H, Liu H, Chen Y, et al. Neoadjuvant chemoradiotherapy followed by surgery versus surgery alone for locally advanced squamous cell carcinoma of the esophagus (NEOCRTEC5010): A phase Ⅲ multicenter, randomized, open-label clinical trial. J Clin Oncol, 2018, 36(27): 2796-2803.
6. Watanabe M, Otake R, Kozuki R, et al. Recent progress in multidisciplinary treatment for patients with esophageal cancer. Surg Today, 2020, 50(1): 12-20.
7. Shah MA, Kennedy EB, Catenacci DV, et al. Treatment of locally advanced esophageal carcinoma: ASCO guideline. J Clin Oncol, 2020, 38(23): 2677-2694.
8. Puetz K, Bollschweiler E, Semrau R, et al. Neoadjuvant chemoradiation for patients with advanced oesophageal cancer—Which response grading system best impacts prognostic discrimination? Histopathology, 2019, 74(5): 731-743.
9. Therasse P, Arbuck SG, Eisenhauer EA, 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(3): 205-216.
10. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1. 1). Eur J Cancer, 2009, 45(2): 228-247.
11. Kurokawa Y, Shibata T, Ando N, et al. Which is the optimal response criteria for evaluating preoperative treatment in esophageal cancer: RECIST or histology? Ann Surg Oncol, 2013, 20(9): 3009-3014.
12. Miyata H, Tanaka K, Makino T, et al. The impact of pathological tumor regression and nodal status on survival and systemic disease in patients undergoing neoadjuvant chemotherapy for esophageal squamous cell carcinoma. Ann Surg Oncol, 2018, 25(8): 2409-2417.
13. Pai RK, Pai RK. Pathologic assessment of gastrointestinal tract and pancreatic carcinoma after neoadjuvant therapy. Mod Pathol, 2018, 31(1): 4-23.
14. Lam AK. Esophageal squamous cell carcinoma methods and protocols: Methods and protocols. Meth Mol Biol. 2020.
15. Tong Y, Liu D, Zhang J. Connection and distinction of tumor regression grading systems of gastrointestinal cancer. Pathol Res Pract, 2020, 216(9): 153073.
16. Mandard AM, Dalibard F, Mandard JC, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer, 1994, 73(11): 2680-2686.
17. Ryan R, Gibbons D, Hyland JM, et al. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology, 2005, 47(2): 141-146.
18. Chirieac LR, Swisher SG, Correa AM, et al. Signet-ring cell or mucinous histology after preoperative chemoradiation and survival in patients with esophageal or esophagogastric junction adenocarcinoma. Clin Cancer Res, 2005, 11(6): 2229-2236.
19. Yamasaki T, Ishii N, Okuno T, et al. A case of esophageal squamous cell carcinoma with neuroendocrine, basaloid, and ciliated glandular differentiation. Clin J Gastroenterol, 2021, 14(1): 32-38.
20. Wang KL, Yang Q, Cleary KR, et al. The significance of neuroendocrine differentiation in adenocarcinoma of the esophagus and esophagogastric junction after preoperative chemoradiation. Cancer, 2006, 107(7): 1467-1474.
21. Waters KM, Salimian KJ, Assarzadegan N, et al. Cell polarity (the 'four lines') distinguishes gastric dysplasia from epithelial changes in reactive gastropathy. Histopathology, 2021, 78(3): 453-458.
22. Wu Y, Sang J, Zhou J, et al. Comparative analysis of differences between preoperative endoscopic biopsy and postoperative pathological examination for diagnosis of gastric intraepithelial neoplasia. J Int Med Res, 2021, 49(3): 300060521994929.
23. Brien TP, Farraye FA, Odze RD. Gastric dysplasia-like epithelial atypia associated with chemoradiotherapy for esophageal cancer: A clinicopathologic and immunohistochemical study of 15 cases. Mod Pathol, 2001, 14(5): 389-396.
24. Okuno K, Tanaka A, Yoshikawa H, et al. A new preoperative immunochemotherapy for the treatment of locally advanced esophageal cancer. Hepatogastroenterology, 1998, 45(22): 950-953.
25. College of American Pathologists. Cancer protocol templates. URL: https://www.cap.org/protocols-and-guidelines/cancer-reporting-tools/cancer-protocol-templates. Last accessed June 11, 2021.
26. 中国临床肿瘤学会指南工作委员会. 中国临床肿瘤学会 (CSCO) 食管癌诊疗指南 2020. 北京: 人民卫生出版社, 2020.
27. Becker K, Mueller JD, Schulmacher C, et al. Histomorphology and grading of regression in gastric carcinoma treated with neoadjuvant chemotherapy. Cancer, 2003, 98(7): 1521-1530.
28. Schneider PM, Baldus SE, Metzger R, et al. Histomorphologic tumor regression and lymph node metastases determine prognosis following neoadjuvant radiochemotherapy for esophageal cancer: Implications for response classification. Ann Surg, 2005, 242(5): 684-692.
29. Chirieac LR, Swisher SG, Ajani JA, et al. Posttherapy pathologic stage predicts survival in patients with esophageal carcinoma receiving preoperative chemoradiation. Cancer, 2005, 103(7): 1347-1355.
30. Swisher SG, Hofstetter W, Wu TT, et al. Proposed revision of the esophageal cancer staging system to accommodate pathologic response (pP) following preoperative chemoradiation (CRT). Ann Surg, 2005, 241(5): 810-817.
31. Wu TT, Chirieac LR, Abraham SC, et al. Excellent interobserver agreement on grading the extent of residual carcinoma after preoperative chemoradiation in esophageal and esophagogastric junction carcinoma: A reliable predictor for patient outcome. Am J Surg Pathol, 2007, 31(1): 58-64.
32. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅠ. Esophagus, 2017, 14(1): 1-36.
33. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer, 2011, 14(2): 101-112.
34. Nieman DR, Peyre CG, Watson TJ, et al. Neoadjuvant treatment response in negative nodes is an important prognosticator after esophagectomy. Ann Thorac Surg, 2015, 99(1): 277-283.
35. Castoro C, Scarpa M, Cagol M, et al. Nodal metastasis from locally advanced esophageal cancer: How neoadjuvant therapy modifies their frequency and distribution. Ann Surg Oncol, 2011, 18(13): 3743-3754.
36. Klevebro F, Tsekrekos A, Low D, et al. Relevant issues in tumor regression grading of histopathological response to neoadjuvant treatment in adenocarcinomas of the esophagus and gastroesophageal junction. Dis Esophagus, 2020, 33(6): doaa005.
37. Hsu PK, Yeh YC, Chien LI, et al. Clinicopathological significance of pathologic complete lymph node regression after neoadjuvant chemoradiotherapy in esophageal squamous cell carcinoma. Ann Surg Oncol, 2021, 28(4): 2048-2058.
38. Hagi T, Makino T, Yamasaki M, et al. Pathological regression of lymph nodes better predicts long-term survival in esophageal cancer patients undergoing neoadjuvant chemotherapy followed by surgery. Ann Surg, 2022, 275(6): 1121-1129.
39. Davies AR, Myoteri D, Zylstra J, et al. Lymph node regression and survival following neoadjuvant chemotherapy in oesophageal adenocarcinoma. Br J Surg, 2018, 105(12): 1639-1649.
40. Groth SS, Burt BM, Farjah F, et al. Prognostic value of neoadjuvant treatment response in locally advanced esophageal adenocarcinoma. J Thorac Cardiovasc Surg, 2019, 157(4): 1682-1693.
41. Langer R, Becker K. Tumor regression grading of gastrointestinal cancers after neoadjuvant therapy. Virchows Arch, 2018, 472(2): 175-186.
42. Westerhoff M, Osecky M, Langer R. Varying practices in tumor regression grading of gastrointestinal carcinomas after neoadjuvant therapy: Results of an international survey. Mod Pathol, 2020, 33(4): 676-689.
43. Saliba G, Detlefsen S, Carneiro F, et al. Tumor regression grading after neoadjuvant treatment of esophageal and gastroesophageal junction adenocarcinoma: Results of an international Delphi consensus survey. Hum Pathol, 2021, 108: 60-67.
44. Tsekrekos A, Detlefsen S, Riddell R, et al. Histopathologic tumor regression grading in patients with gastric carcinoma submitted to neoadjuvant treatment: Results of a Delphi survey. Hum Pathol, 2019, 84: 26-34.
45. Donohoe CL, O'Farrell NJ, Grant T, et al. Classification of pathologic response to neoadjuvant therapy in esophageal and junctional cancer: Assessment of existing measures and proposal of a novel 3-point standard. Ann Surg, 2013, 258(5): 784-792.
46. Tomasello G, Petrelli F, Ghidini M, et al. Tumor regression grade and survival after neoadjuvant treatment in gastro-esophageal cancer: A meta-analysis of 17 published studies. Eur J Surg Oncol, 2017, 43(9): 1607-1616.
47. Karamitopoulou E, Thies S, Zlobec I, et al. Assessment of tumor regression of esophageal adenocarcinomas after neoadjuvant chemotherapy: Comparison of 2 commonly used scoring approaches. Am J Surg Pathol, 2014, 38(11): 1551-1556.
48. Li C, Zhao S, Zheng Y, et al. Preoperative pembrolizumab combined with chemoradiotherapy for oesophageal squamous cell carcinoma (PALACE-1). Eur J Cancer, 2021, 144: 232-241.
49. Kato K, Shah MA, Enzinger P, et al. KEYNOTE-590: Phase Ⅲ study of first-line chemotherapy with or without pembrolizumab for advanced esophageal cancer. Future Oncol, 2019, 15(10): 1057-1066.
50. Shen D, Chen Q, Wu J, et al. The safety and efficacy of neoadjuvant PD-1 inhibitor with chemotherapy for locally advanced esophageal squamous cell carcinoma. J Gastrointest Oncol, 2021, 12(1): 1-10.
51. Urabe M, Ushiku T, Seto Y, et al. Pathologic response of HER2-positive gastric cancer to trastuzumab-based chemotherapy. Am J Surg Pathol, 2016, 40(10): 1326-1333.

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