Definition, classification, and staging for adenocarcinoma of esophagogastric junction: updates in controversies_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIU Kai ¹ , ZHANG Weihan ¹ ,  CHEN Xinzu ^1,2

1. Department of Gastrointestinal Surgery & Laboratory of Gastric Cancer, West China Hospital, Sichuan University, Chengdu 610041,P. R. China;
2. Department of General Surgery, West China Longquan Hospital, Sichuan University, Chengdu 610100, P. R. China;

Corresponding author：

CHEN Xinzu, Email: chenxinzu@scu.edu.cn

Keywords：

adenocarcinoma of esophagogastric junction; WHO definition; TNM stage; diagnostic laparoscopy

DOI：

10.7507/1007-9424.201907029

Video：

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Objectives To summarize the latest advances about definition, classification, and TNM stage of adenocarcinoma of esophagogastric junction (AEG).Method The available guidelines, consensuses, international conference proceedings, and clinical studies were reviewed and summarized.Results The AEG trended to be an independent entity of malignant tumor at the special location. The previous misunderstanding of AEG definitions from the WHO needed to be corrected and unified in China. The Siewert classification was still a practical clinical approach to guiding treatment strategy, while the new draft of JGCA classification needed to be evaluated and verified in the clinical practice. By contrast, the 8th edition AJCC/UICC classification was relatively controversial in the guiding treatment strategies, mainly due to the staging system, surgical approach, and extent of lymphadenectomy of Siewert Ⅱ type AEG. Based on the available research results, the TNM staging system of the 8th edition of gastric cancer tended to be more reasonable for the Siewert Ⅱ and Ⅲ types AEG.Conclusion With increasing incidence of AEG, more experimental and clinical studies on AEG are ongoing, and it is expected to have more optimized classification and exclusive staging system for AEG in future.

Citation： LIU Kai, ZHANG Weihan, CHEN Xinzu. Definition, classification, and staging for adenocarcinoma of esophagogastric junction: updates in controversies. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(9): 1040-1045. doi: 10.7507/1007-9424.201907029 Copy

1.	Chen XZ, Liu Y, Wang R, et al. Improvement of cancer control in mainland China: epidemiological profiles during the 2004-10 National Cancer Prevention and Control Program. Lancet, 2016, 388(Suppl 1): S40.
2.	Wang R, Chen XZ. High mortality from hepatic, gastric and esophageal cancers in mainland China: 40 years of experience and development. Clin Res Hepatol Gastroenterol, 2014, 38(6): 751-756.
3.	Powell J, McConkey CC. The rising trend in oesophageal adenocarcinoma and gastric cardia. Eur J Cancer Prev, 1992, 1(3): 265-269.
4.	Colquhoun A, Arnold M, Ferlay J, et al. Global patterns of cardia and non-cardia gastric cancer incidence in 2012. Gut, 2015, 64(12): 1881-1888.
5.	Liu K, Yang K, Zhang W, et al. Changes of esophagogastric junctional adenocarcinoma and gastroesophageal reflux disease among surgical patients during 1988–2012: a single-institution, high-volume experience in China. Ann Surg, 2016, 263(1): 88-95.
6.	Jankowski JA, Perry I, Harrison RF. Gastro-oesophageal cancer: death at the junction. BMJ, 2000, 321(7259): 463-464.
7.	Gertler R, Stein HJ, Loos M, et al. How to classify adenocarcinomas of the esophagogastric junction: as esophageal or gastric cancer? Am J Surg Pathol, 2011, 35(10): 1512-1522.
8.	Takeuchi H, Kitagawa Y. Adenocarcinoma of the esophagogastric junction: territory of the esophagus or stomach, or an independent region? Ann Surg Oncol, 2013, 20(3): 705-706.
9.	胡建昆, 陈心足. 重视胃癌不同分型分期的治疗和预后. 中国普外基础与临床杂志, 2014, 21(1): 1-6.
10.	国际食管疾病学会中国分会(CSDE)食管胃结合部疾病跨界联盟, 中国医师协会内镜医师分会腹腔镜外科专业委员会, 中国医师协会外科医师分会上消化道外科医师专业委员会, 等. 食管胃结合部腺癌外科治疗中国专家共识(2018年版). 中华胃肠外科杂志, 2018, 21(9): 961-975.
11.	袁勇, 陈心足, 胡建昆, 等. 食管胃结合部腺癌外科治疗中国专家共识(2018年版)解读. 中华胃肠外科杂志, 2019, 22(2): 101-106.
12.	Liu K, Zhang W, Chen X, et al. Comparison on clinicopathological features and prognosis between esophagogastric junctional adenocarcinoma (Siewert Ⅱ/Ⅲ types) and distal gastric adenocarcinoma: retrospective cohort study, a single institution, high volume experience in China. Medicine (Baltimore), 2015, 94(34): e1386.
13.	Hamilton SR, Aaltonen LA (Eds.). World Health Organization Classification of Tumours. Pathology and genetics of tumours of the digestive system. Lyon: International Agency for Research on Cancer (IARC) Press, 2000.
14.	Amin MB, Edge S, Greene FL, et al. AJCC cancer staging manual (8th Ed.). New York: Springer, 2017: 185-202.
15.	Rice TW, Ishwaran H, Hofstetter WL, et al. Recommendations for pathologic staging (pTNM) of cancer of the esophagus and esophagogastric junction for the 8th edition AJCC/UICC staging manuals. Dis Esophagus, 2016, 29(8): 897-905.
16.	Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg, 2017, 6(2): 119-130.
17.	National Comprehensive Cancer Network. Esophageal and esophagogastric junction cancers. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®). 2018 (Version 1). www.nccn.org.
18.	Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg, 1998, 85(11): 1457-1459.
19.	Rüdiger Siewert J, Feith M, Werner M, et al. Adenocarcinoma of the esophagogastric junction: results of surgical therapy based on anatomical/topographic classification in 1 002 consecutive patients. Ann Surg, 2000, 232(3): 353-361.
20.	Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer, 2017, 20(1): 1-19.
21.	Giacopuzzi S, Bencivenga M, Weindelmayer J, et al. Western strategy for EGJ carcinoma. Gastric Cancer, 2017, 20(Suppl 1): 60-68.
22.	Kurokawa Y, Sasako M, Doki Y. Treatment approaches to esophagogastric junction tumors. Dig Surg, 2013, 30(2): 169-173.
23.	Reeh M, Mina S, Bockhorn M, et al. Staging and outcome depending on surgical treatment in adenocarcinomas of the oesophagogastric junction. Br J Surg, 2012, 99(10): 1406-1414.
24.	Hosokawa Y, Kinoshita T, Konishi M, et al. Clinicopathological features and prognostic factors of adenocarcinoma of the esophagogastric junction according to Siewert classification: experiences at a single institution in Japan. Ann Surg Oncol, 2012, 19(2): 677-683.
25.	Zhang W, Chen X, Liu K, et al. Comparison of survival outcomes between transthoracic and transabdominal surgical approaches in patients with Siewert-Ⅱ/Ⅲ esophagogastric junction adenocarcinoma: a single-institution retrospective cohort study. Chin J Cancer Res, 2016, 28(4): 413-422.
26.	杨世界, 袁勇, 李睿哲, 等. Siewert Ⅱ型食管胃结合部腺癌经胸与经腹入路手术的预后比较—胸外科与胃肠外科联合数据分析. 中华胃肠外科杂志, 2019, 22(2): 132-142.
27.	National Comprehensive Cancer Network. Gastric Cancer. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines^®). 2018 (Version 1). www.nccn.org.
28.	D’Journo XB. Clinical implication of the innovations of the 8(th) edition of the TNM classification for esophageal and esophago-gastric cancer. J Thorac Dis, 2018, 10(Suppl 22): S2671-S2681.
29.	Amin MB, Greene FL, Edge SB, et al. The eighth edition AJCC cancer staging manual: Continuing to build a bridge from a population-based to a more " personalized” approach to cancer staging. CA Cancer J Clin, 2017, 67(2): 93-99.
30.	Huang Q, Shi J, Feng A, et al. Gastric cardiac carcinomas involving the esophagus are more adequately staged as gastric cancers by the 7th edition of the American Joint Commission on Cancer Staging System. Mod Pathol, 2011, 24(1): 138-146.
31.	Hasegawa S, Yoshikawa T, Aoyama T, et al. Esophagus or stomach? The seventh TNM classification for Siewert type Ⅱ/Ⅲ junctional adenocarcinoma. Ann Surg Oncol, 2013, 20(3): 773-779.
32.	Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol, 2010, 17(6): 1471-1474.
33.	Sobin LH, Gospodarowicz M, Wittekind C. TNM classification of malignant tumours. 7th ed. New York: Wiley, 2009: 66-72.
34.	Suh YS, Han DS, Kong SH, et al. Should adenocarcinoma of the esophagogastric junction be classified as esophageal cancer? A comparative analysis according to the seventh AJCC TNM classification. Ann Surg, 2012, 255(5): 908-915.
35.	In H, Solsky I, Palis B, et al. Validation of the 8th edition of the AJCC TNM staging system for gastric cancer using the national cancer database. Ann Surg Oncol, 2017, 24(12): 3683-3691.
36.	Liu K, Feng F, Chen XZ, et al. Comparison between gastric and esophageal classification system among adenocarcinomas of esophagogastric junction according to AJCC 8th edition: a retrospective observational study from two high-volume institutions in China. Gastric Cancer, 2019, 22(3): 506-517.
37.	Rice TW, Apperson-Hansen C, DiPaola LM, et al. Worldwide Esophageal Cancer Collaboration: clinical staging data. Dis Esophagus, 2016, 29(7): 707-714.
38.	Rice TW, Ishwaran H, Ferguson MK, et al. Cancer of the esopha-gus and esophagogastric junction: an eighth edition staging primer. J Thorac Oncol, 2017, 12(1): 36-42.
39.	Liu K, Chen XZ, Zhang WH, et al. " Four-Step Procedure” of laparoscopic exploration for gastric cancer in West China Hospital: a retrospective observational analysis from a high-volume institution in China. Surg Endosc, 2019, 33(5): 1674-1682.
40.	陈心足, 刘凯, 张维汉, 等. 胃癌腹腔镜探查. 中华胃肠外科杂志, 2018, 21(5): 497.

1. Chen XZ, Liu Y, Wang R, et al. Improvement of cancer control in mainland China: epidemiological profiles during the 2004-10 National Cancer Prevention and Control Program. Lancet, 2016, 388(Suppl 1): S40.
2. Wang R, Chen XZ. High mortality from hepatic, gastric and esophageal cancers in mainland China: 40 years of experience and development. Clin Res Hepatol Gastroenterol, 2014, 38(6): 751-756.
3. Powell J, McConkey CC. The rising trend in oesophageal adenocarcinoma and gastric cardia. Eur J Cancer Prev, 1992, 1(3): 265-269.
4. Colquhoun A, Arnold M, Ferlay J, et al. Global patterns of cardia and non-cardia gastric cancer incidence in 2012. Gut, 2015, 64(12): 1881-1888.
5. Liu K, Yang K, Zhang W, et al. Changes of esophagogastric junctional adenocarcinoma and gastroesophageal reflux disease among surgical patients during 1988–2012: a single-institution, high-volume experience in China. Ann Surg, 2016, 263(1): 88-95.
6. Jankowski JA, Perry I, Harrison RF. Gastro-oesophageal cancer: death at the junction. BMJ, 2000, 321(7259): 463-464.
7. Gertler R, Stein HJ, Loos M, et al. How to classify adenocarcinomas of the esophagogastric junction: as esophageal or gastric cancer? Am J Surg Pathol, 2011, 35(10): 1512-1522.
8. Takeuchi H, Kitagawa Y. Adenocarcinoma of the esophagogastric junction: territory of the esophagus or stomach, or an independent region? Ann Surg Oncol, 2013, 20(3): 705-706.
9. 胡建昆, 陈心足. 重视胃癌不同分型分期的治疗和预后. 中国普外基础与临床杂志, 2014, 21(1): 1-6.
10. 国际食管疾病学会中国分会(CSDE)食管胃结合部疾病跨界联盟, 中国医师协会内镜医师分会腹腔镜外科专业委员会, 中国医师协会外科医师分会上消化道外科医师专业委员会, 等. 食管胃结合部腺癌外科治疗中国专家共识(2018年版). 中华胃肠外科杂志, 2018, 21(9): 961-975.
11. 袁勇, 陈心足, 胡建昆, 等. 食管胃结合部腺癌外科治疗中国专家共识(2018年版)解读. 中华胃肠外科杂志, 2019, 22(2): 101-106.
12. Liu K, Zhang W, Chen X, et al. Comparison on clinicopathological features and prognosis between esophagogastric junctional adenocarcinoma (Siewert Ⅱ/Ⅲ types) and distal gastric adenocarcinoma: retrospective cohort study, a single institution, high volume experience in China. Medicine (Baltimore), 2015, 94(34): e1386.
13. Hamilton SR, Aaltonen LA (Eds.). World Health Organization Classification of Tumours. Pathology and genetics of tumours of the digestive system. Lyon: International Agency for Research on Cancer (IARC) Press, 2000.
14. Amin MB, Edge S, Greene FL, et al. AJCC cancer staging manual (8th Ed.). New York: Springer, 2017: 185-202.
15. Rice TW, Ishwaran H, Hofstetter WL, et al. Recommendations for pathologic staging (pTNM) of cancer of the esophagus and esophagogastric junction for the 8th edition AJCC/UICC staging manuals. Dis Esophagus, 2016, 29(8): 897-905.
16. Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg, 2017, 6(2): 119-130.
17. National Comprehensive Cancer Network. Esophageal and esophagogastric junction cancers. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines®). 2018 (Version 1). www.nccn.org.
18. Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg, 1998, 85(11): 1457-1459.
19. Rüdiger Siewert J, Feith M, Werner M, et al. Adenocarcinoma of the esophagogastric junction: results of surgical therapy based on anatomical/topographic classification in 1 002 consecutive patients. Ann Surg, 2000, 232(3): 353-361.
20. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer, 2017, 20(1): 1-19.
21. Giacopuzzi S, Bencivenga M, Weindelmayer J, et al. Western strategy for EGJ carcinoma. Gastric Cancer, 2017, 20(Suppl 1): 60-68.
22. Kurokawa Y, Sasako M, Doki Y. Treatment approaches to esophagogastric junction tumors. Dig Surg, 2013, 30(2): 169-173.
23. Reeh M, Mina S, Bockhorn M, et al. Staging and outcome depending on surgical treatment in adenocarcinomas of the oesophagogastric junction. Br J Surg, 2012, 99(10): 1406-1414.
24. Hosokawa Y, Kinoshita T, Konishi M, et al. Clinicopathological features and prognostic factors of adenocarcinoma of the esophagogastric junction according to Siewert classification: experiences at a single institution in Japan. Ann Surg Oncol, 2012, 19(2): 677-683.
25. Zhang W, Chen X, Liu K, et al. Comparison of survival outcomes between transthoracic and transabdominal surgical approaches in patients with Siewert-Ⅱ/Ⅲ esophagogastric junction adenocarcinoma: a single-institution retrospective cohort study. Chin J Cancer Res, 2016, 28(4): 413-422.
26. 杨世界, 袁勇, 李睿哲, 等. Siewert Ⅱ型食管胃结合部腺癌经胸与经腹入路手术的预后比较—胸外科与胃肠外科联合数据分析. 中华胃肠外科杂志, 2019, 22(2): 132-142.
27. National Comprehensive Cancer Network. Gastric Cancer. NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines^®). 2018 (Version 1). www.nccn.org.
28. D’Journo XB. Clinical implication of the innovations of the 8(th) edition of the TNM classification for esophageal and esophago-gastric cancer. J Thorac Dis, 2018, 10(Suppl 22): S2671-S2681.
29. Amin MB, Greene FL, Edge SB, et al. The eighth edition AJCC cancer staging manual: Continuing to build a bridge from a population-based to a more " personalized” approach to cancer staging. CA Cancer J Clin, 2017, 67(2): 93-99.
30. Huang Q, Shi J, Feng A, et al. Gastric cardiac carcinomas involving the esophagus are more adequately staged as gastric cancers by the 7th edition of the American Joint Commission on Cancer Staging System. Mod Pathol, 2011, 24(1): 138-146.
31. Hasegawa S, Yoshikawa T, Aoyama T, et al. Esophagus or stomach? The seventh TNM classification for Siewert type Ⅱ/Ⅲ junctional adenocarcinoma. Ann Surg Oncol, 2013, 20(3): 773-779.
32. Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol, 2010, 17(6): 1471-1474.
33. Sobin LH, Gospodarowicz M, Wittekind C. TNM classification of malignant tumours. 7th ed. New York: Wiley, 2009: 66-72.
34. Suh YS, Han DS, Kong SH, et al. Should adenocarcinoma of the esophagogastric junction be classified as esophageal cancer? A comparative analysis according to the seventh AJCC TNM classification. Ann Surg, 2012, 255(5): 908-915.
35. In H, Solsky I, Palis B, et al. Validation of the 8th edition of the AJCC TNM staging system for gastric cancer using the national cancer database. Ann Surg Oncol, 2017, 24(12): 3683-3691.
36. Liu K, Feng F, Chen XZ, et al. Comparison between gastric and esophageal classification system among adenocarcinomas of esophagogastric junction according to AJCC 8th edition: a retrospective observational study from two high-volume institutions in China. Gastric Cancer, 2019, 22(3): 506-517.
37. Rice TW, Apperson-Hansen C, DiPaola LM, et al. Worldwide Esophageal Cancer Collaboration: clinical staging data. Dis Esophagus, 2016, 29(7): 707-714.
38. Rice TW, Ishwaran H, Ferguson MK, et al. Cancer of the esopha-gus and esophagogastric junction: an eighth edition staging primer. J Thorac Oncol, 2017, 12(1): 36-42.
39. Liu K, Chen XZ, Zhang WH, et al. " Four-Step Procedure” of laparoscopic exploration for gastric cancer in West China Hospital: a retrospective observational analysis from a high-volume institution in China. Surg Endosc, 2019, 33(5): 1674-1682.
40. 陈心足, 刘凯, 张维汉, 等. 胃癌腹腔镜探查. 中华胃肠外科杂志, 2018, 21(5): 497.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Definition, classification, and staging for adenocarcinoma of esophagogastric junction: updates in controversies

Abstract Full text Figures/Tables Video References Cited by

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