Prognostic significance of extranodal extension in gastric cancer, esophageal cancer and gastroesophageal junction cancer: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

LEI Yuying ¹ , ZHAO Qiongrui ² ,  SUN Zhe ¹

1. Department of Surgical Oncology, First Affiliated Hospital of China Medical University, Shenyang, 110000, P.R.China;
2. Evidence-Based Medicine Center, First Affiliated Hospital of China Medical University, Shenyang, 110000, P.R.China;

Corresponding?author：

SUN Zhe, Email: sunzheyida@163.com

Keywords：

Gastric cancer; Esophageal cancer; Gastroesophageal cancer; Extranodal extension; Prognosis; Meta-analysis

DOI：

10.7507/1672-2531.201609069

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Objective To systematically review the prognostic significance of extranodal extension in gastric cancer, esophageal cancer and gastroesophageal junction cancer. Methods We searched EMbase, The Cochrane Library (Issue 9, 2016), PubMed, CBM, CNKI, VIP and WanFang Data databases from inception to August 2016, to collect cohort studies about the prognostic significance of extranodal extension. Two reviewers independently screened literature, extracted data and evaluated the risk of bias of included studies. Then, meta-analysis was performed by using RevMan 5.2 software. Results A total of 16 studies involving 9 445 participants were included. The results of meta-analysis showed that for gastric cancer patients, the overall survival (OS) (HR=1.71, 95%CI 1.49 to 2.00,P<0.000 01), disease free survival (DFS) (HR=1.39, 95%CI 1.12 to 1.73,P=0.003) and cancer specific survival (HR=1.52, 95%CI 1.18 to 1.96,P=0.001) in ENE(+) group were lower than ENE(–) group. For esophageal cancer and gastroesophageal junction cancer patients, the overall survival (OS) (HR=1.84, 95%CI 1.49 to 2.27,P<0.000 01), disease free survival (DFS) (HR=2.18, 95%CI 1.70 to 2.81,P<0.000 01) and cancer specific survival (HR=1.73, 95%CI 1.19 to 2.52,P=0.004) in ENE(+) group were lower than ENE(–) group. Conclusion Current evidence indicates that ENE(+) was correlated with a poor prognosis in gastric cancer, esophageal cancer and gastroesophageal junction cancer patients. Due to the quantity and quality limitations of included studies, more high quality cohort studies are needed to verify the above conclusions.

Citation： LEI Yuying, ZHAO Qiongrui, SUN Zhe. Prognostic significance of extranodal extension in gastric cancer, esophageal cancer and gastroesophageal junction cancer: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2017, 17(4): 402-408. doi: 10.7507/1672-2531.201609069 Copy

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2.	Ferlay J, Soerjomataram I, Dikshit R,et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer, 2015, 136(5): E359-86.
3.	Sobin LH, Gospodarowic MK, Wittekind C,et al. TNM classification of malignant tumours. 7th ed. International Union Against Cancer (UICC), New York: Wiley. 2009.
4.	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.
5.	Stitzenberg KB, Meyer AA, Stern SL,et al. Extracapsular Extension of the Sentinel Lymph Node Metastasis: A Predictor of Nonsentinel Node Tumor Burden. Ann Surg, 2003, 237(5): 607-613.
6.	Veronese N, Nottegar A, Pea A,et al. Prognostic impact and implications of extracapsular lymph node involvement in colorectal cancer: a systematic review with meta-analysis. Ann Oncol, 2016, 27: 42-48.
7.	Edge S, Byrd D, Compton C. AJCC cancer staging manual. 7th edition New York. Springer. 2010.
8.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
9.	文進, 李幼平. Meta 分析中效應尺度指標的選擇. 中國循證醫學雜志, 2007, 7(8): 606-613.
10.	Higgins JP, Thompson SG, Deeks JJ,et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327: 557-560.
11.	丹王, 翟俊霞, 牟振云, 等. Meta 分析中的異質性及其處理方法. 中國循證醫學雜志, 2009, 9(10): 1115-1118.
12.	Peters JL, Sutton AJ, Jones DR,et al. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol, 2008, 61(10): 991-996.
13.	Etoh T, Sasako M, Ishikawa K,et al. Extranodal metastasis is an indicator of poor prognosis in patients with gastric carcinoma. Br J Surg, 2006, 93(3): 369-373.
14.	Lagarde SM, ten Kate FJ, de Boer DJ,et al. Extracapsular lymph node involvement in node positive patients with adenocarcinoma of the distal esophagus or gastroesophageal junction. Am J Surg Pathol, 2006, 30(2): 171-176.
15.	Choi WH, Kim S, Shen J,et al. Prognostic significance of perinodal extension in gastric cancer. J Surg Oncol, 2007, 95(7): 540-545.
16.	Tanabe T, Kanda T, Kosugi S,et al. Extranodal spreading of esophageal squamous cell carcinoma: clinicopathological characteristics and prognostic impact. World J Surg, 2007, 31(11): 2192-2198.
17.	王曉娜, 丁學偉, 張李, 等. 淋巴結外軟組織陽性胃癌預后相關分析. 中華胃腸外科雜志, 2007, 10(5): 436-439.
18.	Alakus H, Holscher AH, Grass G,et al. Extracapsular lymph node spread: a new prognostic factor in gastric cancer. Cancer, 2010, 116(2): 309-315.
19.	Nakamura K, Ogoshi K, Makuuchi H. Subclassification of extranodal involvement in gastric cancer patients. Hepato-Gastroenterology, 2010, 57(101): 968-974.
20.	Tapia EO, Villaseca HM, Araya OJ,et al. Prognostic value of extracapsular lymph node involvement among patients with gastric cancer. Rev Med Chile, 2011, 139: 992-997.
21.	Wang W, Li Y, Zhang Y,et al. Incorporation of extranodal metastasis of gastric carcinoma into the 7th edition UICC TNM staging system. PLoS One, 2011, 6(6): e19557.
22.	Sun Z, Wang ZN, Xu YY,et al. Prognostic significance of tumor deposits in gastric cancer patients who underwent radical surgery. Surgery, 2012, 151(6): 871-881.
23.	D'Annoville T, D'Journo XB, Loundou A,et al. Prognostic impact of the extracapsular lymph node involvement on disease-free survival according to the 7th edition of American Joint Committee on Cancer Staging System. Eur J Cardiothorac Surg, 2013, 44(3): e207-211.
24.	Zhang HD, Tang P, Duan XF,et al. Extranodal metastasis is a powerful prognostic factor in patients with adenocarcinoma of the esophagogastric junction. J Surg Oncol, 2013, 108(8): 542-549.
25.	張洪典, 唐鵬, 段曉峰, 等. 賁門癌淋巴結外軟組織轉移的臨床病理特征及預后分析. 中華外科雜志, 2013, 51(10): 882-886.
26.	Jiang N, Deng JY, Ding XW,et al. Node-extranodal soft tissue stage based on extranodal metastasis is associated with poor prognosis of patients with gastric cancer. J Surg Res, 2014, 192(1): 90-97.
27.	Lee IS, Park YS, Ryu MH,et al. Impact of extranodal extension on prognosis in lymph node-positive gastric cancer. Br J Surg, 2014, 101(12): 1576-1584.
28.	Nafteux P, Lerut T, de Hertogh G,et al. Can extracapsular lymph node involvement be a tool to fine-tune pN1 for adenocarcinoma of the oesophagus and gastro-oesophageal junction in the Union Internationale contre le Cancer (UICC) TNM 7th edition?dagger. Eur J Cardiothorac Surg, 2014, 45(6): 1001-1010.
29.	Cm BD. Quantitative analysis of the extent of extracapsular invasion and its prognostic significance: a prospective study of 170 cases of carcinoma of the larynx and hypopharynx. Head Neck, 1998, 20(1): 16-21.
30.	Ishida T, Tateishi M, Kaneko S,et al. Surgical treatment of patients with non-small-cell lung cancer and mediastinal lymph node involvement. J Surg Oncol, 1990, 43(3): 161-166.
31.	Ahn TS, Kim HS, Jeong CW,et al. Extracapsular Extension of Pelvic Lymph Node Metastasis is an Independent Prognostic Factor in Bladder Cancer: A Systematic Review and Meta-analysis. Ann Surg Oncol, 2015, 22: 3745-3750.
32.	Pecorelli S. Revised FIGO staging for carcinoma of the vulva, cervix, and endometrium. Int J Gynaecol Obstet, 2009, 105(2): 103-104.
33.	Nottegar A, Veronese N, Senthil M,et al. Extra-nodal extension of sentinel lymph node metastasis is a marker of poor prognosis in breast cancer patients: A systematic review and an exploratory meta-analysis. Eur J Surg Oncol, 2016, 42(7): 919-925.
34.	Griebling TL, Ozkutlu D, See WA,et al. Prognostic implications of extracapsular extension of lymph node metastases in prostate cancer. Mod Pathol, 1997, 10(8): 804-809.

1. ?Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin, 2012, 62(1): 10-29.
2. Ferlay J, Soerjomataram I, Dikshit R,et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer, 2015, 136(5): E359-86.
3. Sobin LH, Gospodarowic MK, Wittekind C,et al. TNM classification of malignant tumours. 7th ed. International Union Against Cancer (UICC), New York: Wiley. 2009.
4. 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.
5. Stitzenberg KB, Meyer AA, Stern SL,et al. Extracapsular Extension of the Sentinel Lymph Node Metastasis: A Predictor of Nonsentinel Node Tumor Burden. Ann Surg, 2003, 237(5): 607-613.
6. Veronese N, Nottegar A, Pea A,et al. Prognostic impact and implications of extracapsular lymph node involvement in colorectal cancer: a systematic review with meta-analysis. Ann Oncol, 2016, 27: 42-48.
7. Edge S, Byrd D, Compton C. AJCC cancer staging manual. 7th edition New York. Springer. 2010.
8. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
9. 文進, 李幼平. Meta 分析中效應尺度指標的選擇. 中國循證醫學雜志, 2007, 7(8): 606-613.
10. Higgins JP, Thompson SG, Deeks JJ,et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327: 557-560.
11. 丹王, 翟俊霞, 牟振云, 等. Meta 分析中的異質性及其處理方法. 中國循證醫學雜志, 2009, 9(10): 1115-1118.
12. Peters JL, Sutton AJ, Jones DR,et al. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol, 2008, 61(10): 991-996.
13. Etoh T, Sasako M, Ishikawa K,et al. Extranodal metastasis is an indicator of poor prognosis in patients with gastric carcinoma. Br J Surg, 2006, 93(3): 369-373.
14. Lagarde SM, ten Kate FJ, de Boer DJ,et al. Extracapsular lymph node involvement in node positive patients with adenocarcinoma of the distal esophagus or gastroesophageal junction. Am J Surg Pathol, 2006, 30(2): 171-176.
15. Choi WH, Kim S, Shen J,et al. Prognostic significance of perinodal extension in gastric cancer. J Surg Oncol, 2007, 95(7): 540-545.
16. Tanabe T, Kanda T, Kosugi S,et al. Extranodal spreading of esophageal squamous cell carcinoma: clinicopathological characteristics and prognostic impact. World J Surg, 2007, 31(11): 2192-2198.
17. 王曉娜, 丁學偉, 張李, 等. 淋巴結外軟組織陽性胃癌預后相關分析. 中華胃腸外科雜志, 2007, 10(5): 436-439.
18. Alakus H, Holscher AH, Grass G,et al. Extracapsular lymph node spread: a new prognostic factor in gastric cancer. Cancer, 2010, 116(2): 309-315.
19. Nakamura K, Ogoshi K, Makuuchi H. Subclassification of extranodal involvement in gastric cancer patients. Hepato-Gastroenterology, 2010, 57(101): 968-974.
20. Tapia EO, Villaseca HM, Araya OJ,et al. Prognostic value of extracapsular lymph node involvement among patients with gastric cancer. Rev Med Chile, 2011, 139: 992-997.
21. Wang W, Li Y, Zhang Y,et al. Incorporation of extranodal metastasis of gastric carcinoma into the 7th edition UICC TNM staging system. PLoS One, 2011, 6(6): e19557.
22. Sun Z, Wang ZN, Xu YY,et al. Prognostic significance of tumor deposits in gastric cancer patients who underwent radical surgery. Surgery, 2012, 151(6): 871-881.
23. D'Annoville T, D'Journo XB, Loundou A,et al. Prognostic impact of the extracapsular lymph node involvement on disease-free survival according to the 7th edition of American Joint Committee on Cancer Staging System. Eur J Cardiothorac Surg, 2013, 44(3): e207-211.
24. Zhang HD, Tang P, Duan XF,et al. Extranodal metastasis is a powerful prognostic factor in patients with adenocarcinoma of the esophagogastric junction. J Surg Oncol, 2013, 108(8): 542-549.
25. 張洪典, 唐鵬, 段曉峰, 等. 賁門癌淋巴結外軟組織轉移的臨床病理特征及預后分析. 中華外科雜志, 2013, 51(10): 882-886.
26. Jiang N, Deng JY, Ding XW,et al. Node-extranodal soft tissue stage based on extranodal metastasis is associated with poor prognosis of patients with gastric cancer. J Surg Res, 2014, 192(1): 90-97.
27. Lee IS, Park YS, Ryu MH,et al. Impact of extranodal extension on prognosis in lymph node-positive gastric cancer. Br J Surg, 2014, 101(12): 1576-1584.
28. Nafteux P, Lerut T, de Hertogh G,et al. Can extracapsular lymph node involvement be a tool to fine-tune pN1 for adenocarcinoma of the oesophagus and gastro-oesophageal junction in the Union Internationale contre le Cancer (UICC) TNM 7th edition?dagger. Eur J Cardiothorac Surg, 2014, 45(6): 1001-1010.
29. Cm BD. Quantitative analysis of the extent of extracapsular invasion and its prognostic significance: a prospective study of 170 cases of carcinoma of the larynx and hypopharynx. Head Neck, 1998, 20(1): 16-21.
30. Ishida T, Tateishi M, Kaneko S,et al. Surgical treatment of patients with non-small-cell lung cancer and mediastinal lymph node involvement. J Surg Oncol, 1990, 43(3): 161-166.
31. Ahn TS, Kim HS, Jeong CW,et al. Extracapsular Extension of Pelvic Lymph Node Metastasis is an Independent Prognostic Factor in Bladder Cancer: A Systematic Review and Meta-analysis. Ann Surg Oncol, 2015, 22: 3745-3750.
32. Pecorelli S. Revised FIGO staging for carcinoma of the vulva, cervix, and endometrium. Int J Gynaecol Obstet, 2009, 105(2): 103-104.
33. Nottegar A, Veronese N, Senthil M,et al. Extra-nodal extension of sentinel lymph node metastasis is a marker of poor prognosis in breast cancer patients: A systematic review and an exploratory meta-analysis. Eur J Surg Oncol, 2016, 42(7): 919-925.
34. Griebling TL, Ozkutlu D, See WA,et al. Prognostic implications of extracapsular extension of lymph node metastases in prostate cancer. Mod Pathol, 1997, 10(8): 804-809.

Chinese Journal of Evidence-Based Medicine

Prognostic significance of extranodal extension in gastric cancer, esophageal cancer and gastroesophageal junction cancer: a meta-analysis

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