True esophagogastric junction adenocarcinoma: background of its definition and current surgical trends

  • Tsutomu Kumamoto
  • Yasunori Kurahashi
  • Hirotaka Niwa
  • Yasutaka Nakanishi
  • Koichi Okumura
  • Rie Ozawa
  • Yoshinori Ishida
  • Hisashi ShinoharaEmail author
Review Article


The definition of true esophagogastric junction (EGJ) adenocarcinoma and its surgical treatment are debatable. We review the basis for the current definition and the Japanese surgical strategy in managing true EGJ adenocarcinoma. The Siewert classification is a well-known anatomical classification system for EGJ adenocarcinomas: type II tumors in the region 1 cm above and 2 cm below the EGJ are described as “true carcinoma of the cardia”. Coincidentally, this range matches gastric cardiac gland distribution. Conversely, Nishi’s classification is generally used to describe EGJ carcinomas, defined as tumors with the center located within 2 cm above and 2 cm below the EGJ, regardless of their histological subtype. This range coincides with the extent of the lower esophageal sphincter combined with gastric cardiac gland distribution. The current Japanese surgical strategy focuses on the tumor range from the EGJ to the esophagus and stomach. According to previous studies, the strategy can be roughly classified into three types. The optimal surgical procedure for true EGJ adenocarcinoma is controversial. However, an ongoing Japanese nationwide prospective trial will help confirm the appropriate standard surgery, including the optimal extent of lymph node dissection.


Esophagogastric junction adenocarcinoma Gastroesophageal junction adenocarcinoma Siewert classification Surgery 



This work was supported in part by JSPS KAKENHI (Grant number 16H05399).

Compliance with ethical standards

Conflict of interest

We have no conflicts of interest to declare.


  1. 1.
    Devesa SS, Blot WJ, Fraumeni JF Jr. Changing patterns in the incidence of esophageal and gastric carcinoma in the United States. Cancer. 1998;83:2049–53.CrossRefGoogle Scholar
  2. 2.
    Bollschweiler E, Wolfgarten E, Gutschow C, Holscher AH. Demographic variations in the rising incidence of esophageal adenocarcinoma in white males. Cancer. 2001;92:549–55.CrossRefGoogle Scholar
  3. 3.
    Buas MF, Vaughan TL. Epidemiology and risk factors for gastroesophageal junction tumors: understanding the rising incidence of this disease. Semin Radiat Oncol. 2013;23:3–9.CrossRefGoogle Scholar
  4. 4.
    Chow WH, Blaser MJ, Blot WJ, Gammon MD, Vaughan TL, Risch HA. An inverse relation between cagA+strains of helicobacter pylori infection and risk of esophageal and gastric cardia adenocarcinoma. Cancer Res. 1998;58:588–90.Google Scholar
  5. 5.
    Lagergren J, Bergstrom R, Lindgren A, Nyren O. Symptomatic gastroesophageal reflux as a risk factor for esophageal adenocarcinoma. N Engl J Med. 1999;340:825–31.CrossRefGoogle Scholar
  6. 6.
    O’Doherty MG, Freedman ND, Hollenbeck AR, Schatzkin A, Abnet CC. A prospective cohort study of obesity and risk of oesophageal and gastric adenocarcinoma in the NIH-AAPR Diet and Health Study. Gut. 2012;61:1261–8.CrossRefGoogle Scholar
  7. 7.
    Siewert JR, Stein HJ. Carcinoma of the gastroesophageal junction—classification, pathology and extent of resection. Dis Esophagus. 1996;9:173–82.CrossRefGoogle Scholar
  8. 8.
    Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg. 1998;85:1457–9.CrossRefGoogle Scholar
  9. 9.
    Nishi M, Noumura H, Kajisa T, Aiko T, Kaneko Y, Kawaji T, et al. Surgical problem of carcinoma in the esophagogastric junction (In Japanese with English abstract). Stomach Intest. 1978;13:1497–507.Google Scholar
  10. 10.
    Japanese classification of gastric cancer, 3rd English ed. Japanese Gastric Cancer Association; 2011.Google Scholar
  11. 11.
    Japanese classification of esophageal cancer, 11th ed. Tokyo: Japan Esophageal Society; 2015.Google Scholar
  12. 12.
    Siewert JR, Feith M, Werner M, Stein HJ. Adenocarcinoma of the esophagogastric junction: results of surgical therapy based on anatomical/topographic classification in 1,002 consecutive patients. Ann Surg. 2000;3:353–61.CrossRefGoogle Scholar
  13. 13.
    Grotenhuis BA, Wijnhoven BP, van Marison R, van Dekken H, Hop WC, Tilanus HW, et al. The sentinel node concept in adenocarcinoma of the distal esophagus and gastroesophageal junction. J Thorac Cardiovasc Surg. 2009;138:608–12.CrossRefGoogle Scholar
  14. 14.
    Hasegawa S, Yoshikawa T. Adenocarcinoma of the esophagogastric junction: incidence, characteristics, and treatment strategies. Gastric Cancer. 2010;13:63–73.CrossRefGoogle Scholar
  15. 15.
    Mariette C, Piessen G, Briez N, Gronnier C, Triboulet JP. Oesophagogastric junction adenocarcinoma: which therapeutic approach? Lancet Oncol. 2011;12:296–305.CrossRefGoogle Scholar
  16. 16.
    Haverkamp L, Seesing MFJ, Ruurda JP, Boone J, Hillegersberg R. Worldwide trends in surgical techniques in the treatment of esophageal and gastroesophageal junction cancer. Dis Esophagus. 2017;30:1–7.Google Scholar
  17. 17.
    Brown AM, Giugliano DN, Berger AC, Pucci MJ, Palazzo F. Surgical approaches to adenocarcinoma of the gastroesophageal junction: the Siewert II conundrum. Langenbecks Auch Surg. 2017;402:1153–8.CrossRefGoogle Scholar
  18. 18.
    Giacopuzzi S, Bencivenga M, Weindelmayer J, Verlato G, de Manzoni G. Western strategy for EGJ carcinoma. Gastric Cancer. 2017;20:S60–S6868.CrossRefGoogle Scholar
  19. 19.
    Feith M, Stein HJ, Siewert JR. Adenocarcinoma of the esophagogastric junction: surgical therapy based on 1602 consecutive resected patients. Surg Oncol Clin N Am. 2006;15:751–64.CrossRefGoogle Scholar
  20. 20.
    Sasako M, Sano T, Yamamoto S, Sairenji M, Arai K, Kinoshita T, et al. Left thoracoabdominal approach versus abdominal-transhiatal approach for gastric cancer of the cardia or sub cardia: a randomized controlled trial. Lancet Oncol. 2006;7:644–51.CrossRefGoogle Scholar
  21. 21.
    Omloo JM, Lagrade SM, Hulscher JB, Reitsma JB, Fockens P, van Dekken H, et al. Extended transthoracic resection compared within limited transhiatal resection for adenocarcinoma of the mid/distal esophagus: five-year survival of a randomized clinical trial. Ann Surg. 2007;246:992–1000.CrossRefGoogle Scholar
  22. 22.
    Misumi A, Murakami K, Harada K, Baba K, Akagi M. Definition of carcinoma of the gastric cardia. Langenbecks Arch Chir. 1989;374:221–6.CrossRefGoogle Scholar
  23. 23.
    Bonavina L, Evander A, Demeester TR, Walther B, Cheng AC, et al. Length of the distal esophageal sphincter and competency of the cardia. Am J Surg. 1986;151:25–34.CrossRefGoogle Scholar
  24. 24.
    Byrne PJ, Stuart RC, Lawlor P, Walsh TN, Hennessy TP. A new technique for measuring lower oesophageal sphincter competence in patients. Ir J Med Sci. 1993;162:351–4.CrossRefGoogle Scholar
  25. 25.
    De Carvalho CAF. Sur l’angio-architecture veineuse de la zone de transition oesophago-gastrique et son interpretation fonctionnelle [in French with English and German abstract]. Acta Anat. 1966;64:125–62.CrossRefGoogle Scholar
  26. 26.
    Sato T, Lato Y, Matsuura M, Ganger M. Significance of palisading longitudinal esophagus vessels: Identification of the true esophagogastric junction has histopathological and oncological considerations. Dig Dis Sci. 2010;55:3095–101.CrossRefGoogle Scholar
  27. 27.
    Maselli R, Inoue H, Ikeda H, Onimaru M, Yosida A, Santi EG, et al. Microvasculature of the esophagus and gastroesophageal junction: lesson learned from submucosal endoscopy. World J Gastrointest Endosc. 2016;16:690–6.CrossRefGoogle Scholar
  28. 28.
    Mine S, Sano T, Hiki N, Yamada K, Nunobe S, Yamaguchi T. Lymphadenectomy around the left renal vein in Siewert type II adenocarcinoma of the oesophagogastric junction. Br J Surg. 2013;100:261–6.CrossRefGoogle Scholar
  29. 29.
    Pedrazzani C, de Manzoni G, Marrelli D, Giacopuzzi S, Corso G, Minicozzi AM, et al. Lymph node involvement in advanced gastroesophageal junction adenocarcinoma. J Thorac Cardiovasc Surg. 2007;134:378–85.CrossRefGoogle Scholar
  30. 30.
    Yamashita H, Katai H, Morita S, Saka M, Taniguchi H, Fukagawa T. Optimal extent of lymph node dissection for Siewert type II esophagogastric junction carcinoma. Ann Surg. 2011;254:274–80.CrossRefGoogle Scholar
  31. 31.
    Grotenhuis BA, Wijnhoven BP, Poley JW, Hermans JJ, Biermann K, Spaander MC, et al. Preoperative assessment of tumor location and station-specific lymph node status in patients with adenocarcinoma of the gastroesophageal junction. World J Surg. 2013;37:147–55.CrossRefGoogle Scholar
  32. 32.
    Kurokawa Y, Hiki N, Yoshikawa T, Kishi K, Ito Y, Ohi M, et al. Theoretical therapeutic impact of lymph node dissection on adenocarcinoma of the esophagogastric junction. Surgery. 2015;157:551–5.CrossRefGoogle Scholar
  33. 33.
    Hosokawa Y, Kinoshita T, Konishi M, Takahashi S, Gotohda N, Kato Y, 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;19:677–83.CrossRefGoogle Scholar
  34. 34.
    Koyanagi K, Kato F, Kanamori J, Daiko H, Ozawa S, Tachimori Y. Clinical significance of esophageal invasion length for the prediction of mediastinal lymph node metastasis in Siewert type II adenocarcinoma: a retrospective single-institution study. Ann Gastroenterol Surg. 2018;2:187–96.CrossRefGoogle Scholar
  35. 35.
    Yamashita H, Seto Y, Sano T, Makuuchi H, Ando N, Sasako M, et al. Results of a nation-wide retrospective study of lymphadenectomy for esophagogastric junction carcinoma. Gastric Cancer. 2017;20:S69–83.CrossRefGoogle Scholar
  36. 36.
    Fujitani K, Miyashiro I, Mikata S, Tamura S, Imamura H, Hara J, et al. Pattern of nodal spread and optimal abdominal lymphadenectomy for advanced Siewert type II adenocarcinoma of the cardia: results of a multicenter study. Gastric Cancer. 2013;16:301–8.CrossRefGoogle Scholar
  37. 37.
    Yoshikawa T, Takeuchi H, Hasegawa S, Nozaki I, Kishi K, Ito S, et al. Theoretical therapeutic impact of lymph node dissection on adenocarcinoma and squamous cell carcinoma of the esophagogastric junction. Gastric Cancer. 2016;19:143–9.CrossRefGoogle Scholar
  38. 38.
    Mine S, Kurokawa Y, Takeuchi H, Kishi K, Ito Y, Ohi M, et al. Distribution of involved abdominal lymph nodes is correlated with the distance from the esophagogastric junction to the distal end of the tumor in Siewert type II tumors. Eur J Surg Oncol. 2015;41:1348–53.CrossRefGoogle Scholar
  39. 39.
    Haruta S, Shinohara H, Hosogi H, Ohkura Y, Kobayashi N, Mizuno A, et al. Proximal gastrectomy with exclusion of no. 3b lesser curvature lymph node dissection could not be indicated for patients with advanced upper-third gastric cancer. Gastric Cancer. 2017;20:528–35.CrossRefGoogle Scholar
  40. 40.
    Sano T, Sasako M, Mizusawa J, Yamamoto S, Katai H, Yoshikawa T, et al. Randomized controlled trial to evaluate splenectomy in total gastrectomy for proximal gastric carcinoma. Ann Surg. 2017;265:277–83.CrossRefGoogle Scholar
  41. 41.
    Brierley JD, Gospodarowicz MK, Wittekind C. TNM classification of malignant tumours. 8th ed. Hoboken: Wiley-Blackwell; 2017.Google Scholar
  42. 42.
    Tsujinaka T, Sasako M, Yamamoto S, Sano T, Kurokawa Y, Nashimoto A, et al. Influence of overweight on surgical complication for gastric cancer: results from a randomized control trial comparing D2 and extended para-aortic D3 lymphadenectomy (JCOG9501). Ann Surg Oncol. 2007;14:355–61.CrossRefGoogle Scholar
  43. 43.
    Mine S, Sano T, Hiki N, Yamada K, Kosuga T, Nunobe S, et al. Proximal margin length with transhiatal gastrectomy for Siewert type II and III adenocarcinomas of the oesophagogastric junction. Br J Surg. 2013;100:1050–4.CrossRefGoogle Scholar
  44. 44.
    Barbour AP, Rizk NP, Gonen M, Tang L, Bains MS, Rusch VW, et al. Adenocarcinoma of the gastroesophageal junction: influence of esophageal resection margin and operative approach on outcome. Ann Surg. 2007;246:1–8.CrossRefGoogle Scholar
  45. 45.
    Ito H, Clancy TE, Osteen RT, Swanson RS, Bueno R, Sugarbaker DJ, et al. Adenocarcinoma of the gastric cardia: what is the optimal surgical approach? J Am Coll Surg. 2004;199:880–6.CrossRefGoogle Scholar
  46. 46.
    Casson AG, Darnton SJ, Subramanian S, Hiller L. What is the optimal distal resection margin for esophageal carcinoma? Ann Thorac Surg. 2000;69:205–9.CrossRefGoogle Scholar
  47. 47.
    Reed CE. Technique of open Ivor Lewis esophagectomy. Oper Tech Thorac Cardiovasc Surg. 2009;14:160–75.CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Department of SurgeryHyogo College of MedicineNishinomiyaJapan

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