Short-term efficacy of minimally invasive esophagectomy combined with three-field versus two-field lymphadenectomy for 257 patients with esophageal squamous cell carcinoma: A retrospective cohort study_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

SUN Zengfeng ¹ , LIU Junqiang ² , FAN Boshi ² , SONG Weian ² , YUE Caiying ² , DI Shouying ² , ZHAO Jiahua ² , ZHOU Shaohua ² , DONG Hai ² , WANG Jusi ² , CHEN Siyu ² ,  GONG Taiqian ^1,2

1. The Second Clinical College of Southern Medical University, Guangzhou, 510080, P. R. China;
2. Department of Thoracic Surgery, Sixth Medical Center, Chinese People’s Liberation Army General Hospital, Beijing, 100089, P. R. China;

Corresponding author：

GONG Taiqian, Email: gongtq_thoracic@163.com

Keywords：

Esophageal squamous cell carcinoma; minimally invasive esophagectomy; three-field lymphadenectomy; two-field lymphadenectomy

DOI：

10.7507/1007-4848.202208021

Video：

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Objective To explore the safety of minimally invasive esophagectomy (MIE) with three-field lymphadenectomy (3-FL) for esophageal squamous cell carcinoma (ESCC) by comparing the short-term outcomes between the 3-FL and the two-field lymphadenectomy (2-FL) in MIE. Methods The clinical data of patients with ESCC who underwent minimally invasive McKeown esophagectomy in our hospital from July 2015 to March 2022 were collected retrospectively. Patients were divided into a 3-FL group and a 2-FL group according to lymph node dissection method. And the clinical outcomes and postoperative complications were compared between the two groups. Results A total of 257 patients with ESCC were included in this study. There were 211 males and 46 females with an average age of 62.2±8.1 years. There were 109 patients in the 3-FL group and 148 patients in the 2-FL group. The operation time of the 3-FL group was about 20 minutes longer than that of the 2-FL group (P<0.001). There was no statistical difference between the two groups in the intraoperatve blood loss (P=0.376). More lymph nodes (P<0.001) and also more positive lymph nodes (P=0.003) were obtained in the 3-FL group than in the 2-FL group, and there was a statistical difference in the pathological N stage between the two groups (P<0.001). But there was no statistical difference in the incidence of anastomotic leak (P=0.667), chyle leak (P=0.421), recurrent laryngeal nerve injury (P=0.081), pulmonary complications (P=0.601), pneumonia (P=0.061), cardiac complications (P=0.383), overall complications (P=0.147) or Clavien-Dindo grading (P=0.152) between the two groups. Conclusion MIE 3-FL can improve the efficiency of lymph node dissection and the accuracy of tumor lymph node staging, but it does not increase the postoperative complications, which is worthy of clinical application.

Citation： SUN Zengfeng, LIU Junqiang, FAN Boshi, SONG Weian, YUE Caiying, DI Shouying, ZHAO Jiahua, ZHOU Shaohua, DONG Hai, WANG Jusi, CHEN Siyu, GONG Taiqian. Short-term efficacy of minimally invasive esophagectomy combined with three-field versus two-field lymphadenectomy for 257 patients with esophageal squamous cell carcinoma: A retrospective cohort study. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(4): 556-561. doi: 10.7507/1007-4848.202208021 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Sohda M, Kuwano H. Current status and future prospects for esophageal cancer treatment. Ann Thorac Cardiovasc Surg, 2017, 23(1): 1-11.
3.	Wang WP, Ni PZ, Yang YS, et al. The role and prognostic significance of aortopulmonary, anterior mediastinal, and tracheobronchial lymph nodes in esophageal cancer: Update of the eighth-edition TNM staging system (2018). Ann Surg Oncol, 2019, 26(4): 1005-1011.
4.	Lerut T, Nafteux P, Moons J, et al. Three-field lymphadenectomy for carcinoma of the esophagus and gastroesophageal junction in 174 R0 resections: Impact on staging, disease-free survival, and outcome: A plea for adaptation of TNM classification in upper-half esophageal carcinoma. Ann Surg, 2004, 240(6): 962-972.
5.	Kato H, Watanabe H, Tachimori Y, et al. Evaluation of neck lymph node dissection for thoracic esophageal carcinoma. Ann Thorac Surg, 1991, 51(6): 931-935.
6.	Song WA, Fan BS, Di SY, et al. Three-field lymphadenectomy in minimally invasive esophagectomy for squamous cell carcinoma. Ann Thorac Surg, 2021, 112(3): 928-934.
7.	Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅠ. Esophagus, 2017, 14(1): 1-36.
8.	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.
9.	Low DE, Alderson D, Cecconello I, et al. International consensus on standardization of data collection for complications associated with esophagectomy: Esophagectomy Complications Consensus Group (ECCG). Ann Surg, 2015, 262(2): 286-294.
10.	Charlson ME, Carrozzino D, Guidi J, et al. Charlson Comorbidity Index: A critical review of clinimetric properties. Psychother Psychosom, 2022, 91(1): 8-35.
11.	Biere SS, van Berge Henegouwen MI, Maas KW, et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: A multicentre, open-label, randomised controlled trial. Lancet, 2012, 379(9829): 1887-1892.
12.	Mariette C, Markar SR, Dabakuyo-Yonli TS, et al. Hybrid minimally invasive esophagectomy for esophageal Cancer. N Engl J Med, 2019, 380(2): 152-162.
13.	Shim YM, Kim HK, Kim K. Comparison of survival and recurrence pattern between two-field and three-field lymph node dissections for upper thoracic esophageal squamous cell carcinoma. J Thorac Oncol, 2010, 5(5): 707-712.
14.	Koterazawa Y, Oshikiri T, Takiguchi G, et al. Prophylactic cervical lymph node dissection in thoracoscopic esophagectomy for esophageal cancer increases postoperative complications and does not improve survival. Ann Surg Oncol, 2019, 26(9): 2899-2904.
15.	陈茂辉. 胸腔镜下胸段食管鳞癌2.5野淋巴结清扫术与3野淋巴结清扫术对比. 福建医科大学, 2020.
16.	Bona D, Lombardo F, Matsushima K, et al. Three-field versus two-field lymphadenectomy for esophageal squamous cell carcinoma: A long-term survival meta-analysis. Surgery, 2022, 171(4): 940-947.
17.	Ye T, Sun Y, Zhang Y, et al. Three-field or two-field resection for thoracic esophageal cancer: A meta-analysis. Ann Thorac Surg, 2013, 96(6): 1933-1941.
18.	Ma GW, Situ DR, Ma QL, et al. Three-field vs. two-field lymph node dissection for esophageal cancer: A meta-analysis. World J Gastroenterol, 2014, 20(47): 18022-18030.
19.	Wang J, Yang Y, Shafiulla Shaik M, et al. Three-field versus two-field lymphadenectomy for esophageal squamous cell carcinoma: A meta-analysis. J Surg Res, 2020, 255: 195-204.
20.	Li B, Hu H, Zhang Y, et al. Three-field versus two-field lymphadenectomy in transthoracic oesophagectomy for oesophageal squamous cell carcinoma: Short-term outcomes of a randomized clinical trial. Br J Surg, 2020, 107(6): 647-654.
21.	Nishihira T, Hirayama K, Mori S. A prospective randomized trial of extended cervical and superior mediastinal lymphadenectomy for carcinoma of the thoracic esophagus. Am J Surg, 1998, 175(1): 47-51.
22.	Peng X, Chen Y, Nassor Juma A, et al. Comparison of short-term outcomes between minimally invasive McKeown esophagectomy and Ivor-Lewis esophagectomy for esophageal cancer. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2017, 42(5): 546-552.
23.	Deng J, Su Q, Ren Z, et al. Comparison of short-term outcomes between minimally invasive McKeown and Ivor Lewis esophagectomy for esophageal or junctional cancer: A systematic review and meta-analysis. Onco Targets Ther, 2018, 11: 6057-6069.
24.	Seesing MFJ, Gisbertz SS, Goense L, et al. A propensity score matched analysis of open versus minimally invasive transthoracic esophagectomy in the netherlands. Ann Surg, 2017, 266(5): 839-846.
25.	郑晓东, 张卫民, 侯建彬. 食管癌喉返神经旁淋巴结预测锁骨上淋巴结转移的临床分析. 中国胸心血管外科临床杂志, 2020, 27(3): 297-302.
26.	黄可南, 丁新宇, 陈子豪, 等. 裸眼3D胸腔镜与2D胸腔镜在微创食管癌根治术中的临床对比研究. 中国胸心血管外科临床杂志, 2020, 27(4): 441-445.
27.	张树亮, 郑斌, 陈椿, 等. 食管2.5野之上纵隔超胸顶下颈部淋巴结清扫的应用. 中华胸心血管外科杂志, 2020, 36(6): 373-376.
28.	卢建国, 刘扬, 谷城威, 等. 新辅助化疗联合腔镜手术治疗Ⅲ期食管鳞癌患者临床疗效. 临床心身疾病杂志, 2022, 28(3): 130-132.
29.	Mota FC, Cecconello I, Takeda FR, et al. Neoadjuvant therapy or upfront surgery? A systematic review and meta-analysis of T2N0 esophageal cancer treatment options. Int J Surg, 2018, 54(Pt A): 176-181.
30.	Kidane B, Korst RJ, Weksler B, et al. Neoadjuvant therapy vs. upfront surgery for clinical T2N0 esophageal cancer: A systematic review. Ann Thorac Surg, 2019, 108(3): 935-944.
31.	Isono K, Sato H, Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology, 1991, 48(5): 411-420.
32.	Yamashita K, Makino T, Yamasaki M, et al. Comparison of short-term outcomes between 2- and 3-field lymph node dissection for esophageal cancer. Dis Esophagus, 2017, 30(11): 1-8.
33.	Fan N, Yang H, Zheng J, et al. Comparison of short- and long-term outcomes between 3-field and modern 2-field lymph node dissections for thoracic oesophageal squamous cell carcinoma: A propensity score matching analysis. Interact Cardiovasc Thorac Surg, 2019, 29(3): 434-441.

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Sohda M, Kuwano H. Current status and future prospects for esophageal cancer treatment. Ann Thorac Cardiovasc Surg, 2017, 23(1): 1-11.
3. Wang WP, Ni PZ, Yang YS, et al. The role and prognostic significance of aortopulmonary, anterior mediastinal, and tracheobronchial lymph nodes in esophageal cancer: Update of the eighth-edition TNM staging system (2018). Ann Surg Oncol, 2019, 26(4): 1005-1011.
4. Lerut T, Nafteux P, Moons J, et al. Three-field lymphadenectomy for carcinoma of the esophagus and gastroesophageal junction in 174 R0 resections: Impact on staging, disease-free survival, and outcome: A plea for adaptation of TNM classification in upper-half esophageal carcinoma. Ann Surg, 2004, 240(6): 962-972.
5. Kato H, Watanabe H, Tachimori Y, et al. Evaluation of neck lymph node dissection for thoracic esophageal carcinoma. Ann Thorac Surg, 1991, 51(6): 931-935.
6. Song WA, Fan BS, Di SY, et al. Three-field lymphadenectomy in minimally invasive esophagectomy for squamous cell carcinoma. Ann Thorac Surg, 2021, 112(3): 928-934.
7. Japan Esophageal Society. Japanese classification of esophageal cancer, 11th edition: PartⅠ. Esophagus, 2017, 14(1): 1-36.
8. 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.
9. Low DE, Alderson D, Cecconello I, et al. International consensus on standardization of data collection for complications associated with esophagectomy: Esophagectomy Complications Consensus Group (ECCG). Ann Surg, 2015, 262(2): 286-294.
10. Charlson ME, Carrozzino D, Guidi J, et al. Charlson Comorbidity Index: A critical review of clinimetric properties. Psychother Psychosom, 2022, 91(1): 8-35.
11. Biere SS, van Berge Henegouwen MI, Maas KW, et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: A multicentre, open-label, randomised controlled trial. Lancet, 2012, 379(9829): 1887-1892.
12. Mariette C, Markar SR, Dabakuyo-Yonli TS, et al. Hybrid minimally invasive esophagectomy for esophageal Cancer. N Engl J Med, 2019, 380(2): 152-162.
13. Shim YM, Kim HK, Kim K. Comparison of survival and recurrence pattern between two-field and three-field lymph node dissections for upper thoracic esophageal squamous cell carcinoma. J Thorac Oncol, 2010, 5(5): 707-712.
14. Koterazawa Y, Oshikiri T, Takiguchi G, et al. Prophylactic cervical lymph node dissection in thoracoscopic esophagectomy for esophageal cancer increases postoperative complications and does not improve survival. Ann Surg Oncol, 2019, 26(9): 2899-2904.
15. 陈茂辉. 胸腔镜下胸段食管鳞癌2.5野淋巴结清扫术与3野淋巴结清扫术对比. 福建医科大学, 2020.
16. Bona D, Lombardo F, Matsushima K, et al. Three-field versus two-field lymphadenectomy for esophageal squamous cell carcinoma: A long-term survival meta-analysis. Surgery, 2022, 171(4): 940-947.
17. Ye T, Sun Y, Zhang Y, et al. Three-field or two-field resection for thoracic esophageal cancer: A meta-analysis. Ann Thorac Surg, 2013, 96(6): 1933-1941.
18. Ma GW, Situ DR, Ma QL, et al. Three-field vs. two-field lymph node dissection for esophageal cancer: A meta-analysis. World J Gastroenterol, 2014, 20(47): 18022-18030.
19. Wang J, Yang Y, Shafiulla Shaik M, et al. Three-field versus two-field lymphadenectomy for esophageal squamous cell carcinoma: A meta-analysis. J Surg Res, 2020, 255: 195-204.
20. Li B, Hu H, Zhang Y, et al. Three-field versus two-field lymphadenectomy in transthoracic oesophagectomy for oesophageal squamous cell carcinoma: Short-term outcomes of a randomized clinical trial. Br J Surg, 2020, 107(6): 647-654.
21. Nishihira T, Hirayama K, Mori S. A prospective randomized trial of extended cervical and superior mediastinal lymphadenectomy for carcinoma of the thoracic esophagus. Am J Surg, 1998, 175(1): 47-51.
22. Peng X, Chen Y, Nassor Juma A, et al. Comparison of short-term outcomes between minimally invasive McKeown esophagectomy and Ivor-Lewis esophagectomy for esophageal cancer. Zhong Nan Da Xue Xue Bao Yi Xue Ban, 2017, 42(5): 546-552.
23. Deng J, Su Q, Ren Z, et al. Comparison of short-term outcomes between minimally invasive McKeown and Ivor Lewis esophagectomy for esophageal or junctional cancer: A systematic review and meta-analysis. Onco Targets Ther, 2018, 11: 6057-6069.
24. Seesing MFJ, Gisbertz SS, Goense L, et al. A propensity score matched analysis of open versus minimally invasive transthoracic esophagectomy in the netherlands. Ann Surg, 2017, 266(5): 839-846.
25. 郑晓东, 张卫民, 侯建彬. 食管癌喉返神经旁淋巴结预测锁骨上淋巴结转移的临床分析. 中国胸心血管外科临床杂志, 2020, 27(3): 297-302.
26. 黄可南, 丁新宇, 陈子豪, 等. 裸眼3D胸腔镜与2D胸腔镜在微创食管癌根治术中的临床对比研究. 中国胸心血管外科临床杂志, 2020, 27(4): 441-445.
27. 张树亮, 郑斌, 陈椿, 等. 食管2.5野之上纵隔超胸顶下颈部淋巴结清扫的应用. 中华胸心血管外科杂志, 2020, 36(6): 373-376.
28. 卢建国, 刘扬, 谷城威, 等. 新辅助化疗联合腔镜手术治疗Ⅲ期食管鳞癌患者临床疗效. 临床心身疾病杂志, 2022, 28(3): 130-132.
29. Mota FC, Cecconello I, Takeda FR, et al. Neoadjuvant therapy or upfront surgery? A systematic review and meta-analysis of T2N0 esophageal cancer treatment options. Int J Surg, 2018, 54(Pt A): 176-181.
30. Kidane B, Korst RJ, Weksler B, et al. Neoadjuvant therapy vs. upfront surgery for clinical T2N0 esophageal cancer: A systematic review. Ann Thorac Surg, 2019, 108(3): 935-944.
31. Isono K, Sato H, Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology, 1991, 48(5): 411-420.
32. Yamashita K, Makino T, Yamasaki M, et al. Comparison of short-term outcomes between 2- and 3-field lymph node dissection for esophageal cancer. Dis Esophagus, 2017, 30(11): 1-8.
33. Fan N, Yang H, Zheng J, et al. Comparison of short- and long-term outcomes between 3-field and modern 2-field lymph node dissections for thoracic oesophageal squamous cell carcinoma: A propensity score matching analysis. Interact Cardiovasc Thorac Surg, 2019, 29(3): 434-441.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Short-term efficacy of minimally invasive esophagectomy combined with three-field versus two-field lymphadenectomy for 257 patients with esophageal squamous cell carcinoma: A retrospective cohort study

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