Metastasis rate of intraperitoneal lymph nodes in Siewert type Ⅱ/Ⅲ adenocarcinoma of esophagogastric junction: a meta-analysis and systematic evaluation_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

DU Shuxiang ¹ , ZHANG Lulu ¹ , WANG Tao ¹ , LIANG Yanxu ² , YANG Jingshu ² , ZHANG Wei ³ ,  WU Gang ³

1. Department of Gastrointestinal Surgery, People’s Hospital of Zhengzhou University, Zhengzhou 450003, P. R. China;
2. Department of Gastrointestinal Surgery, People’s Hospital of Henan University, Kaifeng, Henan 475000, P. R. China;
3. Department of Gastrointestinal Surgery, Henan Provincial People’s Hospital, Zhengzhou 450003, P. R. China;

Corresponding author：

WU Gang, Email: wugang006123@163.com

Keywords：

adenocarcinoma of gastroesophageal junction; lymph node metastasis; risk factor; meta-analysis

DOI：

10.7507/1007-9424.202204019

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Objective To analyze rate of intraperitoneal lymph node metastasis (LNM) in Siewert type Ⅱ/Ⅲ adenocarcinoma of esophagogastric junction (AEG) so as to determine optimal extent of lymph node dissection. Methods A systematic and comprehensive search of PubMed, Medline, and Cochrane Library databases for study reports on LNM in patients with Siewert type Ⅱ/Ⅲ AEG was performed. The retrieval time ranged from database establishment to October 1, 2021. The pooled LNM rate was analyzed for each lymph node group. In addition, the influencing factors of LNM in AEG were analyzed. Results After screening, a total of 22 relevant studies were included, with a total of 3 934 cases. For the patients with Siewert type Ⅱ/Ⅲ AEG, the LNM rates of No.1, 2, 1&2, 3, 7 lymph nodes were ≥20%, LNM rates of No.4, 9, 11 (11p+11d), 11p, 16 lymph nodes were 10%–20%, LNM rates of No.4sa, 8a, 10, 11d lymph nodes were 5%–10%, the rest were <5%. For the patients with Siewert type Ⅱ AEG, the LNM rates of No.1, 2, 1&2, 3, 7 lymph nodes were ≥20%, LNM rates of No.4, 9, 11 (11p+11d), 11p lymph nodes were 10%–20%, LNM rates of No.8a, 10 lymph nodes were 5%–10%, and the rest were <5%. For the patients with Siewert type Ⅲ AEG, the LNM rates of No.1, 2, 1&2, 3, 4, 7 lymph nodes were ≥20%, LNM rate of No.11p lymph nodes was 10%–20%, LNM rates of No.4sa, 4sb, 4d, 8a, 9, 10, 11(11p+11d), 11d lymph nodes were 5%–10%, and the rest were <5%. No matter Siewert Ⅱ and (or) Ⅲ AEG patients, the rates of LNM in No.5, 6, and 12a lymph nodes were <5%. The tumor diameter ≥2 cm and higher T stage (T2–T4) increased the probability of LNM in AEG (P<0.05). Conclusions The results of this meta-analysis combined with the literature suggest that in clinical practice, No.10 lymph node dissection is not necessary for Siewert Ⅱ and Siewert Ⅲ AEG patients with tumor length diameter <2 cm and T1 of tumor invasion. No matter Siewert Ⅱ or Ⅲ AEG, as long as the tumor length diameter <2 cm and T1 of tumor invasion, the distal perigastric lymph nodes (No.4d, 5, 6) may not be dissected; Siewert type Ⅱ or Ⅲ AEG patients don’t need to clean No.12a lymph nodes.

Citation： DU Shuxiang, ZHANG Lulu, WANG Tao, LIANG Yanxu, YANG Jingshu, ZHANG Wei, WU Gang. Metastasis rate of intraperitoneal lymph nodes in Siewert type Ⅱ/Ⅲ adenocarcinoma of esophagogastric junction: a meta-analysis and systematic evaluation. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(11): 1495-1502. doi: 10.7507/1007-9424.202204019 Copy

1.	Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Abate D, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol, 2019, 5(12): 1749-1768.
2.	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.
3.	Goto H, Tokunaga M, Miki Y, et al. The optimal extent of lymph node dissection for adenocarcinoma of the esophagogastric junction differs between Siewert type Ⅱ and Siewert type Ⅲ patients. Gastric Cancer, 2014, 18(2): 375-381.
4.	Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg, 1998, 85(11): 1457-1459.
5.	徐泽宽, 王林俊, 李铮. 食管胃结合部腺癌淋巴结清扫策略. 中华消化外科杂志, 2021, 20(6): 631-634.
6.	Zhang X, He XD, Zhang YC, et al. Characteristics of lymph node (No. 5 and No. 6) metastasis and significance of lymph node dissection in Siewert type Ⅱ esophagogastric junction adenocarcinoma (AEG): No. 5 and No. 6 lymph node metastases of AEG and clearance. Medicine (Baltimore), 2021, 100(35): e27106. doi: 10.1097/MD.0000000000027106.
7.	Zheng Z, Shang Y, Xu R, et al. Risk factors and prognosis in patients with adenocarcinoma of esophagogastric junction with lymph node metastasis of Siewert Ⅱ/Ⅲ. Int J Clin Exp Pathol, 2020, 13(5): 1262-1269.
8.	Han WH, Eom BW, Yoon HM, et al. The optimal extent of lymph node dissection in gastroesophageal junctional cancer: retrospective case control study. BMC Cancer, 2019, 19(1): 719. doi: 10.1186/s12885-019-5922-8.
9.	Sato Y, Katai H, Ito M, et al. Can proximal gastrectomy be justified for advanced adenocarcinoma of the esophagogastric junction? J Gastric Cancer, 2018, 18(4): 339-347.
10.	Liu JF, Jiang T, Shi ZH, et al. Prognostic significance of the location of metastatic lymph nodes in patients with adenocarcinoma of the oesophagogastric junction. ANZ J Surg, 2018, 88(3): 218-222.
11.	Duan X, Shang X, Tang P, et al. Lymph node dissection for Siewert Ⅱ esophagogastric junction adenocarcinoma: a retrospective study of 136 cases. ANZ J Surg, 2018, 88(4): E264-E267.
12.	Zheng Z, Yin J, Wu HW, et al. Explored risk factors for lymph node metastasis with Siewert Ⅱ/Ⅲ adenocarcinoma of the gastroesophageal junction. Anticancer Res, 2017, 37(8): 4605-4610.
13.	Wang JB, Lin MQ, Li P, et al. The prognostic relevance of parapyloric lymph node metastasis in Siewert type Ⅱ/Ⅲ adenocarcinoma of the esophagogastric junction. Eur J Surg Oncol, 2017, 43(12): 2333-2340.
14.	Suh YS, Lee KG, Oh SY, et al. Recurrence pattern and lymph node metastasis of adenocarcinoma at the esophagogastric junction. Ann Surg Oncol, 2017, 24(12): 3631-3639.
15.	Hosoda K, Yamashita K, Moriya H, et al. Optimal treatment for Siewert type Ⅱ and Ⅲ adenocarcinoma of the esophagogastric junction: a retrospective cohort study with long-term follow-up. World J Gastroenterol, 2017, 23(15): 2723-2730.
16.	Matsuda T, Kurokawa Y, Yoshikawa T, et al. Clinicopathological characteristics and prognostic factors of patients with Siewert type Ⅱ esophagogastric junction carcinoma: a retrospective multicenter study. World J Surg, 2016, 40(7): 1672-1679.
17.	Peng J, Wang WP, Yuan Y, et al. Optimal extent of lymph node dissection for Siewert type Ⅱ esophagogastric junction adenocarcinoma. Ann Thorac Surg, 2015, 100(1): 263-269.
18.	Yabusaki H, Nashimoto A, Matsuki A, et al. Comparison of the surgical treatment strategies for Siewert type Ⅱ squamous cell carcinoma in the same area as esophagogastric junction carcinoma: data from a single Japanese high-volume cancer center. Surg Today, 2014, 44(8): 1522-1528.
19.	Ito H, Inoue H, Odaka N, et al. Comparison of clinicopathological characteristics in the patients with cardiac cancer with or without esophagogastric junctional invasion: a single-center retrospective cohort study. Int J Surg Oncol, 2013, 2013: 189459. doi: 10.1155/2013/189459.
20.	Hasegawa S, Yoshikawa T, Rino Y, et al. Priority of lymph node dissection for Siewert type Ⅱ/Ⅲ adenocarcinoma of the esophagogastric junction. Ann Surg Oncol, 2013, 20(13): 4252-4259.
21.	Fujitani K, Miyashiro I, Mikata S, et al. Pattern of abdominal nodal spread and optimal abdominal lymphadenectomy for advanced Siewert type Ⅱ adenocarcinoma of the cardia: results of a multicenter study. Gastric Cancer, 2013, 16(3): 301-308.
22.	Nakamura M, Iwahashi M, Nakamori M, et al. Lower mediastinal lymph node metastasis is an independent survival factor of Siewert type Ⅱ and Ⅲ adenocarcinomas in the gastroesophageal junction. Am Surg, 2012, 78(5): 567-573.
23.	Yamashita H, Katai H, Morita S, et al. Optimal extent of lymph node dissection for Siewert type Ⅱ esophagogastric junction carcinoma. Ann Surg, 2011, 254(2): 274-280.
24.	Fang WL, Wu CW, Chen JH, et al. Esophagogastric junction adenocarcinoma according to Siewert classification in Taiwan. Ann Surg Oncol, 2009, 16(12): 3237-3244.
25.	Yonemura Y, Kojima N, Kawamura T, et al. Treatment results of adenocarcinoma of the gastroesophageal junction. Hepatogastroenterology, 2008, 55(82-83): 475-481.
26.	Meier I, Merkel S, Papadopoulos T, et al. Adenocarcinoma of the esophagogastric junction: the pattern of metastatic lymph node dissemination as a rationale for elective lymphatic target volume definition. Int J Radiat Oncol Biol Phys, 2008, 70(5): 1408-1417.
27.	Ichikura T, Ogawa T, Kawabata T, et al. Is adenocarcinoma of the gastric cardia a distinct entity independent of subcardial carcinoma? World J Surg, 2003, 27(3): 334-338.
28.	Kurokawa Y, Takeuchi H, Doki Y, et al. Mapping of lymph node metastasis from esophagogastric junction tumors: a prospective nationwide multicenter study. Ann Surg, 2021, 274(1): 120-127.
29.	Munn Z, Moola S, Lisy K, et al. Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int J Evid Based Healthc, 2015, 13(3): 147-153.
30.	Sasako M, Sano T, Yamamoto S, et al. Left thoracoabdominal approach versus abdominal-transhiatal approach for gastric cancer of the cardia or subcardia: a randomised controlled trial. Lancet Oncol, 2006, 7(8): 644-651.
31.	Mönig SP, Collet PH, Baldus SE, et al. Splenectomy in proximal gastric cancer: frequency of lymph node metastasis to the splenic hilus. J Surg Oncol, 2001, 76(2): 89-92.
32.	Sano T, Sasako M, Mizusawa J, et al. Randomized controlled trial to evaluate splenectomy in total gastrectomy for proximal gastric carcinoma. Ann Surg, 2017, 265(2): 277-283.
33.	Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer, 2021, 24(1): 1-21.
34.	林密, 吕陈彬, 郑朝辉, 等. 脾门淋巴结清扫在肿瘤长径≥4 cm的Siewert Ⅱ型和Ⅲ型食管胃结合部腺癌中的应用价值. 中华消化外科杂志, 2016, 15(11): 1055-1061.
35.	Sasako M, McCulloch P, Kinoshita T, et al. New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg, 1995, 82(3): 346-351.
36.	Yamashita H, Seto Y, Sano T, et al. Results of a nation-wide retrospective study of lymphadenectomy for esophagogastric junction carcinoma. Gastric Cancer, 2017, 20(Suppl 1): 69-83.
37.	Cao H, Ooi M, Yu Z, et al. Should pyloric lymph nodes be dissected for Siewert type Ⅱ and Ⅲ adenocarcinoma of the esophagogastric junctions: experience from a high-volume center in China. J Gastrointest Surg, 2019, 23(2): 256-263.
38.	Mine S, Sano T, Hiki N, et al. Lymphadenectomy around the left renal vein in Siewert type Ⅱ adenocarcinoma of the oesophagogastric junction. Br J Surg, 2013, 100(2): 261-266.
39.	Yoshikawa T, Takeuchi H, Hasegawa S, et al. Theoretical therapeutic impact of lymph node dissection on adenocarcinoma and squamous cell carcinoma of the esophagogastric junction. Gastric Cancer, 2016, 19(1): 143-149.

1. Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Abate D, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol, 2019, 5(12): 1749-1768.
2. 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.
3. Goto H, Tokunaga M, Miki Y, et al. The optimal extent of lymph node dissection for adenocarcinoma of the esophagogastric junction differs between Siewert type Ⅱ and Siewert type Ⅲ patients. Gastric Cancer, 2014, 18(2): 375-381.
4. Siewert JR, Stein HJ. Classification of adenocarcinoma of the oesophagogastric junction. Br J Surg, 1998, 85(11): 1457-1459.
5. 徐泽宽, 王林俊, 李铮. 食管胃结合部腺癌淋巴结清扫策略. 中华消化外科杂志, 2021, 20(6): 631-634.
6. Zhang X, He XD, Zhang YC, et al. Characteristics of lymph node (No. 5 and No. 6) metastasis and significance of lymph node dissection in Siewert type Ⅱ esophagogastric junction adenocarcinoma (AEG): No. 5 and No. 6 lymph node metastases of AEG and clearance. Medicine (Baltimore), 2021, 100(35): e27106. doi: 10.1097/MD.0000000000027106.
7. Zheng Z, Shang Y, Xu R, et al. Risk factors and prognosis in patients with adenocarcinoma of esophagogastric junction with lymph node metastasis of Siewert Ⅱ/Ⅲ. Int J Clin Exp Pathol, 2020, 13(5): 1262-1269.
8. Han WH, Eom BW, Yoon HM, et al. The optimal extent of lymph node dissection in gastroesophageal junctional cancer: retrospective case control study. BMC Cancer, 2019, 19(1): 719. doi: 10.1186/s12885-019-5922-8.
9. Sato Y, Katai H, Ito M, et al. Can proximal gastrectomy be justified for advanced adenocarcinoma of the esophagogastric junction? J Gastric Cancer, 2018, 18(4): 339-347.
10. Liu JF, Jiang T, Shi ZH, et al. Prognostic significance of the location of metastatic lymph nodes in patients with adenocarcinoma of the oesophagogastric junction. ANZ J Surg, 2018, 88(3): 218-222.
11. Duan X, Shang X, Tang P, et al. Lymph node dissection for Siewert Ⅱ esophagogastric junction adenocarcinoma: a retrospective study of 136 cases. ANZ J Surg, 2018, 88(4): E264-E267.
12. Zheng Z, Yin J, Wu HW, et al. Explored risk factors for lymph node metastasis with Siewert Ⅱ/Ⅲ adenocarcinoma of the gastroesophageal junction. Anticancer Res, 2017, 37(8): 4605-4610.
13. Wang JB, Lin MQ, Li P, et al. The prognostic relevance of parapyloric lymph node metastasis in Siewert type Ⅱ/Ⅲ adenocarcinoma of the esophagogastric junction. Eur J Surg Oncol, 2017, 43(12): 2333-2340.
14. Suh YS, Lee KG, Oh SY, et al. Recurrence pattern and lymph node metastasis of adenocarcinoma at the esophagogastric junction. Ann Surg Oncol, 2017, 24(12): 3631-3639.
15. Hosoda K, Yamashita K, Moriya H, et al. Optimal treatment for Siewert type Ⅱ and Ⅲ adenocarcinoma of the esophagogastric junction: a retrospective cohort study with long-term follow-up. World J Gastroenterol, 2017, 23(15): 2723-2730.
16. Matsuda T, Kurokawa Y, Yoshikawa T, et al. Clinicopathological characteristics and prognostic factors of patients with Siewert type Ⅱ esophagogastric junction carcinoma: a retrospective multicenter study. World J Surg, 2016, 40(7): 1672-1679.
17. Peng J, Wang WP, Yuan Y, et al. Optimal extent of lymph node dissection for Siewert type Ⅱ esophagogastric junction adenocarcinoma. Ann Thorac Surg, 2015, 100(1): 263-269.
18. Yabusaki H, Nashimoto A, Matsuki A, et al. Comparison of the surgical treatment strategies for Siewert type Ⅱ squamous cell carcinoma in the same area as esophagogastric junction carcinoma: data from a single Japanese high-volume cancer center. Surg Today, 2014, 44(8): 1522-1528.
19. Ito H, Inoue H, Odaka N, et al. Comparison of clinicopathological characteristics in the patients with cardiac cancer with or without esophagogastric junctional invasion: a single-center retrospective cohort study. Int J Surg Oncol, 2013, 2013: 189459. doi: 10.1155/2013/189459.
20. Hasegawa S, Yoshikawa T, Rino Y, et al. Priority of lymph node dissection for Siewert type Ⅱ/Ⅲ adenocarcinoma of the esophagogastric junction. Ann Surg Oncol, 2013, 20(13): 4252-4259.
21. Fujitani K, Miyashiro I, Mikata S, et al. Pattern of abdominal nodal spread and optimal abdominal lymphadenectomy for advanced Siewert type Ⅱ adenocarcinoma of the cardia: results of a multicenter study. Gastric Cancer, 2013, 16(3): 301-308.
22. Nakamura M, Iwahashi M, Nakamori M, et al. Lower mediastinal lymph node metastasis is an independent survival factor of Siewert type Ⅱ and Ⅲ adenocarcinomas in the gastroesophageal junction. Am Surg, 2012, 78(5): 567-573.
23. Yamashita H, Katai H, Morita S, et al. Optimal extent of lymph node dissection for Siewert type Ⅱ esophagogastric junction carcinoma. Ann Surg, 2011, 254(2): 274-280.
24. Fang WL, Wu CW, Chen JH, et al. Esophagogastric junction adenocarcinoma according to Siewert classification in Taiwan. Ann Surg Oncol, 2009, 16(12): 3237-3244.
25. Yonemura Y, Kojima N, Kawamura T, et al. Treatment results of adenocarcinoma of the gastroesophageal junction. Hepatogastroenterology, 2008, 55(82-83): 475-481.
26. Meier I, Merkel S, Papadopoulos T, et al. Adenocarcinoma of the esophagogastric junction: the pattern of metastatic lymph node dissemination as a rationale for elective lymphatic target volume definition. Int J Radiat Oncol Biol Phys, 2008, 70(5): 1408-1417.
27. Ichikura T, Ogawa T, Kawabata T, et al. Is adenocarcinoma of the gastric cardia a distinct entity independent of subcardial carcinoma? World J Surg, 2003, 27(3): 334-338.
28. Kurokawa Y, Takeuchi H, Doki Y, et al. Mapping of lymph node metastasis from esophagogastric junction tumors: a prospective nationwide multicenter study. Ann Surg, 2021, 274(1): 120-127.
29. Munn Z, Moola S, Lisy K, et al. Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int J Evid Based Healthc, 2015, 13(3): 147-153.
30. Sasako M, Sano T, Yamamoto S, et al. Left thoracoabdominal approach versus abdominal-transhiatal approach for gastric cancer of the cardia or subcardia: a randomised controlled trial. Lancet Oncol, 2006, 7(8): 644-651.
31. Mönig SP, Collet PH, Baldus SE, et al. Splenectomy in proximal gastric cancer: frequency of lymph node metastasis to the splenic hilus. J Surg Oncol, 2001, 76(2): 89-92.
32. Sano T, Sasako M, Mizusawa J, et al. Randomized controlled trial to evaluate splenectomy in total gastrectomy for proximal gastric carcinoma. Ann Surg, 2017, 265(2): 277-283.
33. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer, 2021, 24(1): 1-21.
34. 林密, 吕陈彬, 郑朝辉, 等. 脾门淋巴结清扫在肿瘤长径≥4 cm的Siewert Ⅱ型和Ⅲ型食管胃结合部腺癌中的应用价值. 中华消化外科杂志, 2016, 15(11): 1055-1061.
35. Sasako M, McCulloch P, Kinoshita T, et al. New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg, 1995, 82(3): 346-351.
36. Yamashita H, Seto Y, Sano T, et al. Results of a nation-wide retrospective study of lymphadenectomy for esophagogastric junction carcinoma. Gastric Cancer, 2017, 20(Suppl 1): 69-83.
37. Cao H, Ooi M, Yu Z, et al. Should pyloric lymph nodes be dissected for Siewert type Ⅱ and Ⅲ adenocarcinoma of the esophagogastric junctions: experience from a high-volume center in China. J Gastrointest Surg, 2019, 23(2): 256-263.
38. Mine S, Sano T, Hiki N, et al. Lymphadenectomy around the left renal vein in Siewert type Ⅱ adenocarcinoma of the oesophagogastric junction. Br J Surg, 2013, 100(2): 261-266.
39. Yoshikawa T, Takeuchi H, Hasegawa S, et al. Theoretical therapeutic impact of lymph node dissection on adenocarcinoma and squamous cell carcinoma of the esophagogastric junction. Gastric Cancer, 2016, 19(1): 143-149.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Metastasis rate of intraperitoneal lymph nodes in Siewert type Ⅱ/Ⅲ adenocarcinoma of esophagogastric junction: a meta-analysis and systematic evaluation

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