Early esophageal cancer: Endoscopic resection or surgical resection?_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LI Shan , CHEN Lin , ZHANG Yuhang , GUO Linjie , ZHANG Qiongying ,  HU Bing

Digestive Endoscopy Center, West China Hospital, Sichuan University, Chengdu, 610041, P.R.China;

Corresponding author：

HU Bing, Email: hubingnj@163.com

Keywords：

Early esophageal cancer; endoscopic resection; surgical resection; complication

DOI：

10.7507/1007-4848.202004053

Video：

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Abstract Full text Figures/Tables Video References Cited by

Endoscopic resection and surgical resection are the two major therapeutic methods for early esophageal cancer. Endoscopic resection is safe and minimally invasive, but lymph node dissection can not be performed. Although surgery provides a rather thorough resection of the lesions and affected lymph nodes, surgical trauma brings certain negative impact on patients' long-term life quality. A comprehensive assessment of the patient's general condition, the risk of diseased lymph node metastasis, and the risk of the treatment itself is an important measure to optimize treatment decisions and formulate personalized treatment plans.

Citation： LI Shan, CHEN Lin, ZHANG Yuhang, GUO Linjie, ZHANG Qiongying, HU Bing. Early esophageal cancer: Endoscopic resection or surgical resection?. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2020, 27(10): 1223-1227. doi: 10.7507/1007-4848.202004053 Copy

1.	赫捷, 邵康. 中国食管癌流行病学现状、诊疗现状及未来对策. 中国癌症杂志, 2011, 21(7): 501-504.
2.	Pennathur A, Gibson MK, Jobe BA, et al. Oesophageal carcinoma. Lancet, 2013, 381(9864): 400-412.
3.	中华医学会消化内镜学分会, 中华医学会消化病学分会, 中华医学会消化病学分会消化病理学组. 中国早期食管鳞状细胞癌及癌前病变筛查与诊治共识 (2015 年, 北京). 中华消化内镜杂志, 2016, 33(1): 3-18.
4.	The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc, 2003, 58(6 Suppl): S3-S43.
5.	李苗, 曾晓清, 谭黎杰, 等. 浅表食管癌术后患者的生存及预后分析. 中华医学杂志, 2016, 96(6): 460-463.
6.	艾波, 廖永德, 付向宁, 等. 全胸腔镜下食管胃胸内吻合术治疗中下段食管癌的技术探讨. 中国微创外科杂志, 2013, 13(5): 394-397.
7.	马荣, 弓磊, 尚晓滨, 等. 腔镜食管癌根治术与开放三切口食管癌根治术的疗效对比. 中华消化外科杂志, 2018, 17(8): 804-809.
8.	张楷悦, 王璐, 修艳丽, 等. 不同外科治疗方案在 T1b 期食管癌患者中的疗效对比. 中国医药科学, 2019, 9(15): 247-250.
9.	Campos JH. An update on robotic thoracic surgery and anesthesia. Curr Opin Anaesthesiol, 2010, 23(1): 1-6.
10.	张含露, 陈龙奇, 耿英才, 等. 机器人辅助食管癌根治手术的应用. 中国胸心血管外科临床杂志, 2019, 26(3): 206-210.
11.	Bergman JJ, Zhang YM, He S, et al. Outcomes from a prospective trial of endoscopic radiofrequency ablation of early squamous cell neoplasia of the esophagus. Gastrointest Endosc, 2011, 74(6): 1181-1190.
12.	He S, Bergman J, Zhang Y, et al. Endoscopic radiofrequency ablation for early esophageal squamous cell neoplasia: Report of safety and effectiveness from a large prospective trial. Endoscopy, 2015, 47(5): 398-408.
13.	di Pietro M, Canto MI, Fitzgerald RC. Endoscopic management of early adenocarcinoma and squamous cell carcinoma of the esophagus: Screening, diagnosis, and therapy. Gastroenterology, 2018, 154(2): 421-436.
14.	Pouw RE, van Vilsteren FG, Peters FP, et al. Randomized trial on endoscopic resection-cap versus multiband mucosectomy for piecemeal endoscopic resection of early Barrett's neoplasia. Gastrointest Endosc, 2011, 74(1): 35-43.
15.	吕昆明, 令狐恩强. 早期和浅表性食管鳞状细胞癌内镜治疗现状. 中华腔镜外科杂志 (电子版), 2019, 12(3): 185-188.
16.	Ono S, Fujishiro M, Koike K. Endoscopic submucosal dissection for superficial esophageal neoplasms. World J Gastrointest Endosc, 2012, 4(5): 162-166.
17.	Takahashi H, Arimura Y, Masao H, et al. Endoscopic submucosal dissection is superior to conventional endoscopic resection as a curative treatment for early squamous cell carcinoma of the esophagus (with video). Gastrointest Endosc, 2010, 72(2): 255-264.
18.	令狐恩强. 消化内镜隧道技术专家共识 (2017, 北京) 解读. 中华胃肠内镜电子杂志, 2017, 4(4): 159-161.
19.	Zhang W, Zhai Y, Chai N, et al. Endoscopic submucosal tunnel dissection and endoscopic submucosal dissection for large superficial esophageal squamous cell neoplasm: Efficacy and safety study to guide future practice. Surg Endosc, 2018, 32(6): 2814-2821.
20.	翟亚奇, 令狐恩强, 李惠凯, 等. 内镜下隧道式与常规黏膜剥离术治疗食管大面积浅表性肿瘤的对比研究. 南方医科大学学报, 2014, 34(1): 36-40.
21.	Ohashi S, Miyamoto S, Kikuchi O, et al. Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology, 2015, 149(7): 1700-1715.
22.	费翔, 王新宇, 卢琪珏, 等. T1 期食管鳞癌淋巴结转移及预后危险因素分析. 中国胸心血管外科临床杂志, 2020. [Epub ahead of print].
23.	Yamashina T, Ishihara R, Nagai K, et al. Long-term outcome and metastatic risk after endoscopic resection of superficial esophageal squamous cell carcinoma. Am J Gastroenterol, 2013, 108(4): 544-551.
24.	Kitagawa Y, Uno T, Oyama T, et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: Part 1. Esophagus, 2019, 16(1): 1-24.
25.	Ishikawa H, Sakurai H, Tamaki Y, et al. Radiation therapy alone for stageⅠ (UICC T1N0M0) squamous cell carcinoma of the esophagus: indications for surgery or combined chemoradiotherapy. J Gastroenterol Hepatol, 2006, 21(8): 1290-1296.
26.	Eguchi T, Nakanishi Y, Shimoda T, et al. Histopathological criteria for additional treatment after endoscopic mucosal resection for esophageal cancer: analysis of 464 surgically resected cases. Mod Pathol, 2006, 19(3): 475-480.
27.	Katada C, Muto M, Momma K, et al. Clinical outcome after endoscopic mucosal resection for esophageal squamous cell carcinoma invading the muscularis mucosae—A multicenter retrospective cohort study. Endoscopy, 2007, 39(9): 779-783.
28.	Tanaka T, Matono S, Mori N, et al. T1 squamous cell carcinoma of the esophagus: long-term outcomes and prognostic factors after esophagectomy. Ann Surg Oncol, 2014, 21(3): 932-938.
29.	Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy, 2015, 47(9): 829-854.
30.	Sun F, Yuan P, Chen T, et al. Efficacy and complication of endoscopic submucosal dissection for superficial esophageal carcinoma: a systematic review and meta-analysis. J Cardiothorac Surg, 2014, 9: 78.
31.	Pech O, May A, Manner H, et al. Long-term efficacy and safety of endoscopic resection for patients with mucosal adenocarcinoma of the esophagus. Gastroenterology, 2014, 146(3): 652-660.
32.	Ono S, Fujishiro M, Niimi K, et al. Predictors of postoperative stricture after esophageal endoscopic submucosal dissection for superficial squamous cell neoplasms. Endoscopy, 2009, 41(8): 661-665.
33.	Shi Q, Ju H, Yao LQ, et al. Risk factors for postoperative stricture after endoscopic submucosal dissection for superficial esophageal carcinoma. Endoscopy, 2014, 46(8): 640-644.
34.	Funakawa K, Uto H, Sasaki F, et al. Effect of endoscopic submucosal dissection for superficial esophageal neoplasms and risk factors for postoperative stricture. Medicine (Baltimore), 2015, 94(1): e373.
35.	唐健, 刘枫, 陈洁, 等. 大范围早期食管癌内镜粘膜下剥离术后发生难治性狭窄的危险因素分析. 中华消化内镜杂志, 2017, 34(6): 11-14.
36.	Yu JP, Liu YJ, Tao YL, et al. Prevention of esophageal stricture after endoscopic submucosal dissection: a systematic review. World J Surg, 2015, 39(12): 2955-2964.
37.	Hanada M, Kanetaka K, Hidaka S, et al. Effect of early mobilization on postoperative pulmonary complications in patients undergoing video-assisted thoracoscopic surgery on the esophagus. Esophagus, 2018, 15(2): 69-74.
38.	Atkins BZ, Shah AS, Hutcheson KA, et al. Reducing hospital morbidity and mortality following esophagectomy. Ann Thorac Surg, 2004, 78(4): 1170-1176.
39.	Bailey SH, Bull DA, Harpole DH, et al. Outcomes after esophagectomy: a ten-year prospective cohort. Ann Thorac Surg, 2003, 75(1): 217-222.
40.	Buise M, Van Bommel J, Mehra M, et al. Pulmonary morbidity following esophagectomy is decreased after introduction of a multimodal anesthetic regimen. Acta Anaesthesiol Belg, 2008, 59(4): 257-261.
41.	Derogar M, Orsini N, Sadr-Azodi O, et al. Influence of major postoperative complications on health-related quality of life among long-term survivors of esophageal cancer surgery. J Clin Oncol, 2012, 30(14): 1615-1619.
42.	Wormuth JK, Heitmiller RF. Esophageal conduit necrosis. Thorac Surg Clin, 2006, 16(1): 11-22.
43.	Biere SS, Maas KW, Cuesta MA, et al. Cervical or thoracic anastomosis after esophagectomy for cancer: a systematic review and meta-analysis. Dig Surg, 2011, 28(1): 29-35.
44.	Kim RH, Takabe K. Methods of esophagogastric anastomoses following esophagectomy for cancer: A systematic review. J Surg Oncol, 2010, 101(6): 527-533.
45.	Veeramootoo D, Parameswaran R, Krishnadas R, et al. Classification and early recognition of gastric conduit failure after minimally invasive esophagectomy. Surg Endosc, 2009, 23(9): 2110-2116.
46.	Gockel I, Kneist W, Keilmann A, et al. Recurrent laryngeal nerve paralysis (RLNP) following esophagectomy for carcinoma. Eur J Surg Oncol, 2005, 31(3): 277-281.
47.	Wright CD, Zeitels SM. Recurrent laryngeal nerve injuries after esophagectomy. Thorac Surg Clin, 2006, 16(1): 23-33.
48.	Pertl L, Zacherl J, Mancusi G, et al. High risk of unilateral recurrent laryngeal nerve paralysis after esophagectomy using cervical anastomosis. Eur Arch Otorhinolaryngol, 2011, 268(11): 1605-1610.
49.	Schild HH, Strassburg CP, Welz A, et al. Treatment options in patients with chylotho rax. Dtsch Arztebl Int, 2019, 110(48): 819-826.
50.	Breaux JR, Marks C. Chylothorax causing reversible T-cell depletion. J Trauma, 1988, 28(5): 705-707.
51.	Skouras V, Kalomenidis I. Chylothorax: diagnostic approach. Curr Opin Pulm Med, 2010, 16(4): 387-393.

1. 赫捷, 邵康. 中国食管癌流行病学现状、诊疗现状及未来对策. 中国癌症杂志, 2011, 21(7): 501-504.
2. Pennathur A, Gibson MK, Jobe BA, et al. Oesophageal carcinoma. Lancet, 2013, 381(9864): 400-412.
3. 中华医学会消化内镜学分会, 中华医学会消化病学分会, 中华医学会消化病学分会消化病理学组. 中国早期食管鳞状细胞癌及癌前病变筛查与诊治共识 (2015 年, 北京). 中华消化内镜杂志, 2016, 33(1): 3-18.
4. The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc, 2003, 58(6 Suppl): S3-S43.
5. 李苗, 曾晓清, 谭黎杰, 等. 浅表食管癌术后患者的生存及预后分析. 中华医学杂志, 2016, 96(6): 460-463.
6. 艾波, 廖永德, 付向宁, 等. 全胸腔镜下食管胃胸内吻合术治疗中下段食管癌的技术探讨. 中国微创外科杂志, 2013, 13(5): 394-397.
7. 马荣, 弓磊, 尚晓滨, 等. 腔镜食管癌根治术与开放三切口食管癌根治术的疗效对比. 中华消化外科杂志, 2018, 17(8): 804-809.
8. 张楷悦, 王璐, 修艳丽, 等. 不同外科治疗方案在 T1b 期食管癌患者中的疗效对比. 中国医药科学, 2019, 9(15): 247-250.
9. Campos JH. An update on robotic thoracic surgery and anesthesia. Curr Opin Anaesthesiol, 2010, 23(1): 1-6.
10. 张含露, 陈龙奇, 耿英才, 等. 机器人辅助食管癌根治手术的应用. 中国胸心血管外科临床杂志, 2019, 26(3): 206-210.
11. Bergman JJ, Zhang YM, He S, et al. Outcomes from a prospective trial of endoscopic radiofrequency ablation of early squamous cell neoplasia of the esophagus. Gastrointest Endosc, 2011, 74(6): 1181-1190.
12. He S, Bergman J, Zhang Y, et al. Endoscopic radiofrequency ablation for early esophageal squamous cell neoplasia: Report of safety and effectiveness from a large prospective trial. Endoscopy, 2015, 47(5): 398-408.
13. di Pietro M, Canto MI, Fitzgerald RC. Endoscopic management of early adenocarcinoma and squamous cell carcinoma of the esophagus: Screening, diagnosis, and therapy. Gastroenterology, 2018, 154(2): 421-436.
14. Pouw RE, van Vilsteren FG, Peters FP, et al. Randomized trial on endoscopic resection-cap versus multiband mucosectomy for piecemeal endoscopic resection of early Barrett's neoplasia. Gastrointest Endosc, 2011, 74(1): 35-43.
15. 吕昆明, 令狐恩强. 早期和浅表性食管鳞状细胞癌内镜治疗现状. 中华腔镜外科杂志 (电子版), 2019, 12(3): 185-188.
16. Ono S, Fujishiro M, Koike K. Endoscopic submucosal dissection for superficial esophageal neoplasms. World J Gastrointest Endosc, 2012, 4(5): 162-166.
17. Takahashi H, Arimura Y, Masao H, et al. Endoscopic submucosal dissection is superior to conventional endoscopic resection as a curative treatment for early squamous cell carcinoma of the esophagus (with video). Gastrointest Endosc, 2010, 72(2): 255-264.
18. 令狐恩强. 消化内镜隧道技术专家共识 (2017, 北京) 解读. 中华胃肠内镜电子杂志, 2017, 4(4): 159-161.
19. Zhang W, Zhai Y, Chai N, et al. Endoscopic submucosal tunnel dissection and endoscopic submucosal dissection for large superficial esophageal squamous cell neoplasm: Efficacy and safety study to guide future practice. Surg Endosc, 2018, 32(6): 2814-2821.
20. 翟亚奇, 令狐恩强, 李惠凯, 等. 内镜下隧道式与常规黏膜剥离术治疗食管大面积浅表性肿瘤的对比研究. 南方医科大学学报, 2014, 34(1): 36-40.
21. Ohashi S, Miyamoto S, Kikuchi O, et al. Recent advances from basic and clinical studies of esophageal squamous cell carcinoma. Gastroenterology, 2015, 149(7): 1700-1715.
22. 费翔, 王新宇, 卢琪珏, 等. T1 期食管鳞癌淋巴结转移及预后危险因素分析. 中国胸心血管外科临床杂志, 2020. [Epub ahead of print].
23. Yamashina T, Ishihara R, Nagai K, et al. Long-term outcome and metastatic risk after endoscopic resection of superficial esophageal squamous cell carcinoma. Am J Gastroenterol, 2013, 108(4): 544-551.
24. Kitagawa Y, Uno T, Oyama T, et al. Esophageal cancer practice guidelines 2017 edited by the Japan Esophageal Society: Part 1. Esophagus, 2019, 16(1): 1-24.
25. Ishikawa H, Sakurai H, Tamaki Y, et al. Radiation therapy alone for stageⅠ (UICC T1N0M0) squamous cell carcinoma of the esophagus: indications for surgery or combined chemoradiotherapy. J Gastroenterol Hepatol, 2006, 21(8): 1290-1296.
26. Eguchi T, Nakanishi Y, Shimoda T, et al. Histopathological criteria for additional treatment after endoscopic mucosal resection for esophageal cancer: analysis of 464 surgically resected cases. Mod Pathol, 2006, 19(3): 475-480.
27. Katada C, Muto M, Momma K, et al. Clinical outcome after endoscopic mucosal resection for esophageal squamous cell carcinoma invading the muscularis mucosae—A multicenter retrospective cohort study. Endoscopy, 2007, 39(9): 779-783.
28. Tanaka T, Matono S, Mori N, et al. T1 squamous cell carcinoma of the esophagus: long-term outcomes and prognostic factors after esophagectomy. Ann Surg Oncol, 2014, 21(3): 932-938.
29. Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, et al. Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy, 2015, 47(9): 829-854.
30. Sun F, Yuan P, Chen T, et al. Efficacy and complication of endoscopic submucosal dissection for superficial esophageal carcinoma: a systematic review and meta-analysis. J Cardiothorac Surg, 2014, 9: 78.
31. Pech O, May A, Manner H, et al. Long-term efficacy and safety of endoscopic resection for patients with mucosal adenocarcinoma of the esophagus. Gastroenterology, 2014, 146(3): 652-660.
32. Ono S, Fujishiro M, Niimi K, et al. Predictors of postoperative stricture after esophageal endoscopic submucosal dissection for superficial squamous cell neoplasms. Endoscopy, 2009, 41(8): 661-665.
33. Shi Q, Ju H, Yao LQ, et al. Risk factors for postoperative stricture after endoscopic submucosal dissection for superficial esophageal carcinoma. Endoscopy, 2014, 46(8): 640-644.
34. Funakawa K, Uto H, Sasaki F, et al. Effect of endoscopic submucosal dissection for superficial esophageal neoplasms and risk factors for postoperative stricture. Medicine (Baltimore), 2015, 94(1): e373.
35. 唐健, 刘枫, 陈洁, 等. 大范围早期食管癌内镜粘膜下剥离术后发生难治性狭窄的危险因素分析. 中华消化内镜杂志, 2017, 34(6): 11-14.
36. Yu JP, Liu YJ, Tao YL, et al. Prevention of esophageal stricture after endoscopic submucosal dissection: a systematic review. World J Surg, 2015, 39(12): 2955-2964.
37. Hanada M, Kanetaka K, Hidaka S, et al. Effect of early mobilization on postoperative pulmonary complications in patients undergoing video-assisted thoracoscopic surgery on the esophagus. Esophagus, 2018, 15(2): 69-74.
38. Atkins BZ, Shah AS, Hutcheson KA, et al. Reducing hospital morbidity and mortality following esophagectomy. Ann Thorac Surg, 2004, 78(4): 1170-1176.
39. Bailey SH, Bull DA, Harpole DH, et al. Outcomes after esophagectomy: a ten-year prospective cohort. Ann Thorac Surg, 2003, 75(1): 217-222.
40. Buise M, Van Bommel J, Mehra M, et al. Pulmonary morbidity following esophagectomy is decreased after introduction of a multimodal anesthetic regimen. Acta Anaesthesiol Belg, 2008, 59(4): 257-261.
41. Derogar M, Orsini N, Sadr-Azodi O, et al. Influence of major postoperative complications on health-related quality of life among long-term survivors of esophageal cancer surgery. J Clin Oncol, 2012, 30(14): 1615-1619.
42. Wormuth JK, Heitmiller RF. Esophageal conduit necrosis. Thorac Surg Clin, 2006, 16(1): 11-22.
43. Biere SS, Maas KW, Cuesta MA, et al. Cervical or thoracic anastomosis after esophagectomy for cancer: a systematic review and meta-analysis. Dig Surg, 2011, 28(1): 29-35.
44. Kim RH, Takabe K. Methods of esophagogastric anastomoses following esophagectomy for cancer: A systematic review. J Surg Oncol, 2010, 101(6): 527-533.
45. Veeramootoo D, Parameswaran R, Krishnadas R, et al. Classification and early recognition of gastric conduit failure after minimally invasive esophagectomy. Surg Endosc, 2009, 23(9): 2110-2116.
46. Gockel I, Kneist W, Keilmann A, et al. Recurrent laryngeal nerve paralysis (RLNP) following esophagectomy for carcinoma. Eur J Surg Oncol, 2005, 31(3): 277-281.
47. Wright CD, Zeitels SM. Recurrent laryngeal nerve injuries after esophagectomy. Thorac Surg Clin, 2006, 16(1): 23-33.
48. Pertl L, Zacherl J, Mancusi G, et al. High risk of unilateral recurrent laryngeal nerve paralysis after esophagectomy using cervical anastomosis. Eur Arch Otorhinolaryngol, 2011, 268(11): 1605-1610.
49. Schild HH, Strassburg CP, Welz A, et al. Treatment options in patients with chylotho rax. Dtsch Arztebl Int, 2019, 110(48): 819-826.
50. Breaux JR, Marks C. Chylothorax causing reversible T-cell depletion. J Trauma, 1988, 28(5): 705-707.
51. Skouras V, Kalomenidis I. Chylothorax: diagnostic approach. Curr Opin Pulm Med, 2010, 16(4): 387-393.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Early esophageal cancer: Endoscopic resection or surgical resection?

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