Does lymph node ratio (metastasis/total lymph node count) affect survival and prognosis in gastric cancer?

Ramazan Topcu; İbrahim T. Şahiner; Murat Kendirci; Murathan Erkent; İsmail Sezikli; Mehmet B. Tutan

doi:10.15537/smj.2022.43.2.20210464

References

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1. Bray F,
2. Ferlay J,
3. 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: 394–424.
OpenUrl CrossRef PubMed
2.↵
1. Zhang YX,
2. Yang K.
Significance of nodal dissection and nodal positivity in gastric cancer. Transl Gastroenterol Hepatol 2020; 5: 17.
OpenUrl
3.↵
1. Pan S,
2. Wang P,
3. Xing Y,
4. Li K,
5. Wang Z,
6. Xu H, et al.
Retrieved lymph nodes from different anatomic groups in gastric cancer: a proposed optimal number, comparison with other nodal classification strategies and its impact on prognosis. Cancer Commun 2019; 39:49
OpenUrl
4.↵
1. Eshuis WJ,
2. van Barge Henegouwen MI,
3. Draaisma WA,
4. Gisbert SS.
Compliance to D2 lymphadenectomy in laparoscopic gastrectomy. Updates Surg 2018; 70: 197–205.
OpenUrl
5.
1. Zhang N,
2. Bai H,
3. Deng J,
4. Wang W,
5. Sun Z,
6. Wang Z, et al.
Impact of examined lymph node count on staging and long-term survival of patients with node-negative stage III gastric cancer: a retrospective study using a Chinese multi-institutional registry with Surveillance, Epidemiology, and End Results (SEER) data validation. Ann Transl Med 2020; 8: 1075–1091.
OpenUrl
6.↵
1. Kinami S,
2. Ohnishi T,
3. Nakamura N,
4. Jiang ZY,
5. Miyata T,
6. Fujita H, et al.
Efficacy of the fat-dissociation method for nodal harvesting in gastric cancer. World J Gastrointest Surg 2020; 12: 277–286.
OpenUrl
7.↵
1. Baiocchi GL,
2. Molfino S,
3. Molteni B,
4. Quarti, Arcangli G,
5. Manenti S, et al.
Fluorescence-guided lymphadenectomy in gastric cancer: a prospective western series. Updates Surg 2020; 72: 761–772.
OpenUrl
8.↵
1. Nakamura K,
2. Ueyama T,
3. Yao T,
4. XuanV ZX,
5. Ambe K,
6. Adachi Y, et al.
Pathology and prognosis of gastric carcinoma. Findings in 10,000 patients who underwent primary gastrectomy. Cancer 1992; 70: 1030–1037.
OpenUrl CrossRef PubMed Web of Science
9.↵
1. Lu J,
2. Zheng CH,
3. Cao LL,
4. Li P,
5. Xie JW,
6. Wang JB, et al.
The effectiveness of the 8th American Joint Committee on Cancer TNM classification in the prognosis evaluation of gastric cancer patients: A comparative study between the 7th and 8th editions. Eur J Surg Oncol 2017; 43: 2349–2356.
OpenUrl
10.↵
1. Biondi A,
2. D’Ugo D,
3. Cananzi FC,
4. Papa V,
5. Borasi A,
6. Sicoli F, et al.
Does a minimum number of 16 retrieved nodes affect survival in curatively resected gastric cancer? Eur J Surg Oncol 2015; 41:779–786.
OpenUrl
11.↵
1. Lee YC,
2. Yang PJ,
3. Zhong Y,
4. Clancy TE,
5. Lin MT,
6. Wang J.
Lymph node ratio-based staging system outperforms the seventh AJCC system for gastric cancer: Validation analysis with National Taiwan University Hospital Cancer Registry. Am J Clin Oncol 2017; 40: 35–41.
OpenUrl CrossRef PubMed
12.↵
1. Xu J,
2. Bian YH,
3. Jin X,
4. Cao H.
Prognostic assessment of different metastatic lymph node staging methods for gastric cancer after D2 resection. World J Gastroenterol 2013; 19: 1975–1983.
OpenUrl
13.↵
1. Tóth D,
2. Bíró A,
3. Varga Z,
4. Török M,
5. Árkosy P.
Comparison of different lymph node staging systems in prognosis of gastric cancer: A bi-institutional study from Hungary. Chin J Cancer Res 2017; 29: 323–332.
OpenUrl
14.↵
1. Marchet A,
2. Mocellin S,
3. Ambrosi A,
4. Morgagni P,
5. Garcea D,
6. Marrelli D, et al.
The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients. Ann Surg 2007; 245: 543–552.
OpenUrl CrossRef PubMed Web of Science
15.↵
1. Turhan VB,
2. Ünsal A,
3. Gök HF,
4. Öztürk B,
5. Öztürk D,
6. Simsek GG, et al.
Predictive value of preoperative neutrophil-lymphocyte and platelet-lymphocyte ratio in determining the stage of colon tumors. Cureus 2021; 13: e18381.
OpenUrl
16.↵
1. Chen S,
2. Rao H,
3. Liu J,
4. Geng Q,
5. Guo J,
6. Kong P, et al.
Lymph nodes ratio based nomogram predicts survival of resectable gastric cancer regardless of the number of examined lymph nodes. Oncotarget 2017; 8: 45585–45596.
OpenUrl
17.↵
1. Agnes A,
2. Biondi A,
3. Cananzi FM,
4. Rausei S,
5. Reddavid R,
6. Laterza V, et al.
Ratio-based staging systems are better than the 7th and 8th editions of the TNM in stratifying the prognosis of gastric cancer patients: A multicenter retrospective study. J Surg Oncol 2019; 119: 948–957.
OpenUrl
18.↵
1. Huang CM,
2. Lin BJ,
3. Lu HS,
4. Zhang XF,
5. Li P,
6. Xie JW.
Prognostic impact of metastatic lymph node ratio in advanced gastric cancer from cardia and fundus. World J Gastroenterol 2008; 21; 14: 4383–4388.
OpenUrl
19.↵
1. Know Sj, Kim GS
, Prognostic significance of lymph node metastasis in advanced carsinoma of the stomach. Br J Surg 1996; 83: 1600–1603.
OpenUrl PubMed
20.↵
1. Siewert JR,
2. Böttcher K,
3. Stein HJ,
4. Roder JD.
Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg 1998; 228: 449–461.
OpenUrl CrossRef PubMed Web of Science
21.↵
1. Hou Y,
2. Wang X,
3. Chen J.
Prognostic significance of metastatic lymph node ratio: the lymph node ratio could be a prognostic indicator for patients with gastric cancer. World J Surg Onc 2018; 16: 198.
OpenUrl
22.↵
1. Nelen SD,
2. van Steenbergen LN,
3. Dassen AE,
4. van der Wurff AA,
5. Lemmens VE,
6. Bosscha K, et al.
The lymph node ratio as a prognostic factor for gastric cancer. Acta Oncol 2013; 52: 1751–1759.
OpenUrl
23.↵
1. Jiang Zhu, Zhao Xue,
2. Shumei Zhang, et al.
Integrated analysis of the prognostic role of the lymph node ratio in node-positive gastric cancer: A meta-analysis. International Journal of Surgery 2018; 57: 76–83.
OpenUrl
24.↵
1. Wang W,
2. Sun Z,
3. Deng JY,
4. Qi XL,
5. Feng XY,
6. Fang C, et al.
A novel nomogram individually predicting disease-specific survival after D2 gastrectomy for advanced gastric cancer. Cancer Commun (Lond) 2018; 38: 23.
OpenUrl
25.↵
1. Gu P,
2. Deng J,
3. Sun Z,
4. Wang Z,
5. Wang W,
6. Liang H, et al.
Superiority of log odds of positive lymph nodes (LODDS) for prognostic prediction after gastric cancer surgery: a multi-institutional analysis of 7620 patients in China. Surg Today 2021; 51: 101–110.
OpenUrl PubMed
26.
1. Wang XQ,
2. Bao M,
3. Zhang C.
Prognostic value of different lymph node staging methods for node-positive cardia gastric cancer: a register-based retrospective cohort study. BMJ Open 2021; 11: e050378.
OpenUrl
27.↵
1. Xu Z,
2. Jing J,
3. Ma G.
Development and validation of prognostic nomogram based on log odds of positive lymph nodes for patients with gastric signet ring cell carcinoma. Chin J Cancer Res 2020; 32: 778–793.
OpenUrl
28.↵
1. Chen YR,
2. Wang MQ,
3. Li YT,
4. Li P,
5. Ouyang SS,
6. Xu HW, et al.
Prognostic performance of different lymph node classification systems in young gastric cancer. J Gastrointest Oncol 2021: 1285–1300.
29.↵
1. Cao H,
2. Tang Z,
3. Yu Z,
4. Wang Q,
5. Li Z,
6. Lu Q, et al.
Comparison of the 8th union for international cancer control lymph node staging system for gastric cancer with two other lymph node staging systems. Oncol Lett 2019; 17: 1299–1305.
OpenUrl
30.↵
1. Kong SH.
Lymph node ratio system for N staging of gastric cancer: challenging for universal application but useful for the prognostic prediction of individual patients. J Gastric Cancer 2021; 21: 1–3.
OpenUrl

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Keywords

[1] 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: 394–424.
OpenUrl CrossRef PubMed

[2] Bray F,

[3] Ferlay J,

[4] Soerjomataram I, et al.

[5] 2.↵
Zhang YX,
Yang K.
Significance of nodal dissection and nodal positivity in gastric cancer. Transl Gastroenterol Hepatol 2020; 5: 17.
OpenUrl

[6] Zhang YX,

[7] Yang K.

[8] 3.↵
Pan S,
Wang P,
Xing Y,
Li K,
Wang Z,
Xu H, et al.
Retrieved lymph nodes from different anatomic groups in gastric cancer: a proposed optimal number, comparison with other nodal classification strategies and its impact on prognosis. Cancer Commun 2019; 39:49
OpenUrl

[9] Pan S,

[10] Wang P,

[11] Xing Y,

[12] Li K,

[13] Wang Z,

[14] Xu H, et al.

[15] 4.↵
Eshuis WJ,
van Barge Henegouwen MI,
Draaisma WA,
Gisbert SS.
Compliance to D2 lymphadenectomy in laparoscopic gastrectomy. Updates Surg 2018; 70: 197–205.
OpenUrl

[16] Eshuis WJ,

[17] van Barge Henegouwen MI,

[18] Draaisma WA,

[19] Gisbert SS.

[20] 5.
Zhang N,
Bai H,
Deng J,
Wang W,
Sun Z,
Wang Z, et al.
Impact of examined lymph node count on staging and long-term survival of patients with node-negative stage III gastric cancer: a retrospective study using a Chinese multi-institutional registry with Surveillance, Epidemiology, and End Results (SEER) data validation. Ann Transl Med 2020; 8: 1075–1091.
OpenUrl

[21] Zhang N,

[22] Bai H,

[23] Deng J,

[24] Wang W,

[25] Sun Z,

[26] Wang Z, et al.

[27] 6.↵
Kinami S,
Ohnishi T,
Nakamura N,
Jiang ZY,
Miyata T,
Fujita H, et al.
Efficacy of the fat-dissociation method for nodal harvesting in gastric cancer. World J Gastrointest Surg 2020; 12: 277–286.
OpenUrl

[28] Kinami S,

[29] Ohnishi T,

[30] Nakamura N,

[31] Jiang ZY,

[32] Miyata T,

[33] Fujita H, et al.

[34] 7.↵
Baiocchi GL,
Molfino S,
Molteni B,
Quarti, Arcangli G,
Manenti S, et al.
Fluorescence-guided lymphadenectomy in gastric cancer: a prospective western series. Updates Surg 2020; 72: 761–772.
OpenUrl

[35] Baiocchi GL,

[36] Molfino S,

[37] Molteni B,

[38] Quarti, Arcangli G,

[39] Manenti S, et al.

[40] 8.↵
Nakamura K,
Ueyama T,
Yao T,
XuanV ZX,
Ambe K,
Adachi Y, et al.
Pathology and prognosis of gastric carcinoma. Findings in 10,000 patients who underwent primary gastrectomy. Cancer 1992; 70: 1030–1037.
OpenUrl CrossRef PubMed Web of Science

[41] Nakamura K,

[42] Ueyama T,

[43] Yao T,

[44] XuanV ZX,

[45] Ambe K,

[46] Adachi Y, et al.

[47] 9.↵
Lu J,
Zheng CH,
Cao LL,
Li P,
Xie JW,
Wang JB, et al.
The effectiveness of the 8th American Joint Committee on Cancer TNM classification in the prognosis evaluation of gastric cancer patients: A comparative study between the 7th and 8th editions. Eur J Surg Oncol 2017; 43: 2349–2356.
OpenUrl

[48] Lu J,

[49] Zheng CH,

[50] Cao LL,

[51] Li P,

[52] Xie JW,

[53] Wang JB, et al.

[54] 10.↵
Biondi A,
D’Ugo D,
Cananzi FC,
Papa V,
Borasi A,
Sicoli F, et al.
Does a minimum number of 16 retrieved nodes affect survival in curatively resected gastric cancer? Eur J Surg Oncol 2015; 41:779–786.
OpenUrl

[55] Biondi A,

[56] D’Ugo D,

[57] Cananzi FC,

[58] Papa V,

[59] Borasi A,

[60] Sicoli F, et al.

[61] 11.↵
Lee YC,
Yang PJ,
Zhong Y,
Clancy TE,
Lin MT,
Wang J.
Lymph node ratio-based staging system outperforms the seventh AJCC system for gastric cancer: Validation analysis with National Taiwan University Hospital Cancer Registry. Am J Clin Oncol 2017; 40: 35–41.
OpenUrl CrossRef PubMed

[62] Lee YC,

[63] Yang PJ,

[64] Zhong Y,

[65] Clancy TE,

[66] Lin MT,

[67] Wang J.

[68] 12.↵
Xu J,
Bian YH,
Jin X,
Cao H.
Prognostic assessment of different metastatic lymph node staging methods for gastric cancer after D2 resection. World J Gastroenterol 2013; 19: 1975–1983.
OpenUrl

[69] Xu J,

[70] Bian YH,

[71] Jin X,

[72] Cao H.

[73] 13.↵
Tóth D,
Bíró A,
Varga Z,
Török M,
Árkosy P.
Comparison of different lymph node staging systems in prognosis of gastric cancer: A bi-institutional study from Hungary. Chin J Cancer Res 2017; 29: 323–332.
OpenUrl

[74] Tóth D,

[75] Bíró A,

[76] Varga Z,

[77] Török M,

[78] Árkosy P.

[79] 14.↵
Marchet A,
Mocellin S,
Ambrosi A,
Morgagni P,
Garcea D,
Marrelli D, et al.
The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients. Ann Surg 2007; 245: 543–552.
OpenUrl CrossRef PubMed Web of Science

[80] Marchet A,

[81] Mocellin S,

[82] Ambrosi A,

[83] Morgagni P,

[84] Garcea D,

[85] Marrelli D, et al.

[86] 15.↵
Turhan VB,
Ünsal A,
Gök HF,
Öztürk B,
Öztürk D,
Simsek GG, et al.
Predictive value of preoperative neutrophil-lymphocyte and platelet-lymphocyte ratio in determining the stage of colon tumors. Cureus 2021; 13: e18381.
OpenUrl

[87] Turhan VB,

[88] Ünsal A,

[89] Gök HF,

[90] Öztürk B,

[91] Öztürk D,

[92] Simsek GG, et al.

[93] 16.↵
Chen S,
Rao H,
Liu J,
Geng Q,
Guo J,
Kong P, et al.
Lymph nodes ratio based nomogram predicts survival of resectable gastric cancer regardless of the number of examined lymph nodes. Oncotarget 2017; 8: 45585–45596.
OpenUrl

[94] Chen S,

[95] Rao H,

[96] Liu J,

[97] Geng Q,

[98] Guo J,

[99] Kong P, et al.

[100] 17.↵
Agnes A,
Biondi A,
Cananzi FM,
Rausei S,
Reddavid R,
Laterza V, et al.
Ratio-based staging systems are better than the 7th and 8th editions of the TNM in stratifying the prognosis of gastric cancer patients: A multicenter retrospective study. J Surg Oncol 2019; 119: 948–957.
OpenUrl

[101] Agnes A,

[102] Biondi A,

[103] Cananzi FM,

[104] Rausei S,

[105] Reddavid R,

[106] Laterza V, et al.

[107] 18.↵
Huang CM,
Lin BJ,
Lu HS,
Zhang XF,
Li P,
Xie JW.
Prognostic impact of metastatic lymph node ratio in advanced gastric cancer from cardia and fundus. World J Gastroenterol 2008; 21; 14: 4383–4388.
OpenUrl

[108] Huang CM,

[109] Lin BJ,

[110] Lu HS,

[111] Zhang XF,

[112] Li P,

[113] Xie JW.

[114] 19.↵
Know Sj, Kim GS
, Prognostic significance of lymph node metastasis in advanced carsinoma of the stomach. Br J Surg 1996; 83: 1600–1603.
OpenUrl PubMed

[115] Know Sj, Kim GS

[116] 20.↵
Siewert JR,
Böttcher K,
Stein HJ,
Roder JD.
Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg 1998; 228: 449–461.
OpenUrl CrossRef PubMed Web of Science

[117] Siewert JR,

[118] Böttcher K,

[119] Stein HJ,

[120] Roder JD.

[121] 21.↵
Hou Y,
Wang X,
Chen J.
Prognostic significance of metastatic lymph node ratio: the lymph node ratio could be a prognostic indicator for patients with gastric cancer. World J Surg Onc 2018; 16: 198.
OpenUrl

[122] Hou Y,

[123] Wang X,

[124] Chen J.

[125] 22.↵
Nelen SD,
van Steenbergen LN,
Dassen AE,
van der Wurff AA,
Lemmens VE,
Bosscha K, et al.
The lymph node ratio as a prognostic factor for gastric cancer. Acta Oncol 2013; 52: 1751–1759.
OpenUrl

[126] Nelen SD,

[127] van Steenbergen LN,

[128] Dassen AE,

[129] van der Wurff AA,

[130] Lemmens VE,

[131] Bosscha K, et al.

[132] 23.↵
Jiang Zhu, Zhao Xue,
Shumei Zhang, et al.
Integrated analysis of the prognostic role of the lymph node ratio in node-positive gastric cancer: A meta-analysis. International Journal of Surgery 2018; 57: 76–83.
OpenUrl

[133] Jiang Zhu, Zhao Xue,

[134] Shumei Zhang, et al.

[135] 24.↵
Wang W,
Sun Z,
Deng JY,
Qi XL,
Feng XY,
Fang C, et al.
A novel nomogram individually predicting disease-specific survival after D2 gastrectomy for advanced gastric cancer. Cancer Commun (Lond) 2018; 38: 23.
OpenUrl

[136] Wang W,

[137] Sun Z,

[138] Deng JY,

[139] Qi XL,

[140] Feng XY,

[141] Fang C, et al.

[142] 25.↵
Gu P,
Deng J,
Sun Z,
Wang Z,
Wang W,
Liang H, et al.
Superiority of log odds of positive lymph nodes (LODDS) for prognostic prediction after gastric cancer surgery: a multi-institutional analysis of 7620 patients in China. Surg Today 2021; 51: 101–110.
OpenUrl PubMed

[143] Gu P,

[144] Deng J,

[145] Sun Z,

[146] Wang Z,

[147] Wang W,

[148] Liang H, et al.

[149] 26.
Wang XQ,
Bao M,
Zhang C.
Prognostic value of different lymph node staging methods for node-positive cardia gastric cancer: a register-based retrospective cohort study. BMJ Open 2021; 11: e050378.
OpenUrl

[150] Wang XQ,

[151] Bao M,

[152] Zhang C.

[153] 27.↵
Xu Z,
Jing J,
Ma G.
Development and validation of prognostic nomogram based on log odds of positive lymph nodes for patients with gastric signet ring cell carcinoma. Chin J Cancer Res 2020; 32: 778–793.
OpenUrl

[154] Xu Z,

[155] Jing J,

[156] Ma G.

[157] 28.↵
Chen YR,
Wang MQ,
Li YT,
Li P,
Ouyang SS,
Xu HW, et al.
Prognostic performance of different lymph node classification systems in young gastric cancer. J Gastrointest Oncol 2021: 1285–1300.

[158] Chen YR,

[159] Wang MQ,

[160] Li YT,

[161] Li P,

[162] Ouyang SS,

[163] Xu HW, et al.

[164] 29.↵
Cao H,
Tang Z,
Yu Z,
Wang Q,
Li Z,
Lu Q, et al.
Comparison of the 8th union for international cancer control lymph node staging system for gastric cancer with two other lymph node staging systems. Oncol Lett 2019; 17: 1299–1305.
OpenUrl

[165] Cao H,

[166] Tang Z,

[167] Yu Z,

[168] Wang Q,

[169] Li Z,

[170] Lu Q, et al.

[171] 30.↵
Kong SH.
Lymph node ratio system for N staging of gastric cancer: challenging for universal application but useful for the prognostic prediction of individual patients. J Gastric Cancer 2021; 21: 1–3.
OpenUrl

[172] Kong SH.

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Does lymph node ratio (metastasis/total lymph node count) affect survival and prognosis in gastric cancer?

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