Prognostic analysis of pT1b esophageal squamous cell carcinoma after open or minimally invasive esophagectomy_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LIU Lin ^1,2 , ZHANG Yong ¹ ,  WANG Xiaolin ² ,  SHU Yusheng ²

1. Department of Thoracic Surgery, Second Affiliated Hospital of Dalian Medical University, Dalian, 116044, P.R.China;
2. Department of Thoracic Surgery, Northern Jiangsu People’s Hospital, Yangzhou, 255001, Jiangsu, P.R.China;

Corresponding author：

WANG Xiaolin, Email: wangxiaolinyz@163.com; SHU Yusheng, Email: Shuyusheng65@163.com

Keywords：

Esophageal cancer; squamous cell carcinoma; stage T1b; prognosis; surgery

DOI：

10.7507/1007-4848.202004056

Video：

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Objective To compare the short-term and long-term effects of minimally invasive esophagectomy (MIE) and traditional open esophagectomy (OE) in patients with stage T1b esophageal squamous cell carcinoma (ESCC).Methods We retrospectively analyzed the clinical pathology data of 162 patients undergoing thoracic surgery at Northern Jiangsu People's Hospital from 2015 to 2018 whose pathological diagnosis was stage pT1b ESCC. According to the surgical approach, they were divided into MIE group and OE group. There were 55 males and 21 females in the OE group, with an average age of 63.3±5.6 years, and 60 males and 26 females in the MIE group, with an average age of 64.7±6.1 years. The preoperative, intraoperative and postoperative data of the two groups were compared and followed up. Survival data were compared using Kaplan-Meier and log-rank tests between the two groups, and Cox proportional hazard regression models were used to analyze prognostic factors.Results Compared with the OE group, the intraoperative bleeding volume of the MIE group was less (119.8±70.0 mL vs. 210.5±136.2 mL, P<0.001), and the lymph nodes dissected during the operation were more (19.1±7.4 vs. 13.8±5.9, P<0.001), the rate of postoperative pulmonary infections was lower (9.3% vs. 21.1%, P=0.036), but the operation time was longer (240.0±52.4 min vs. 179.5±35.7 min, P<0.001). Twenty-one patients had lymph node metastasis, and the lymph node metastasis rate was 13.0%. At the end of the follow-up, 19 patients died, and the overall survival (OS) at 1 year, 3 years, and 5 years after operation were 97.5%, 88.8% and 82.9%, respectively; 31 patients had recurrence and metastasis, and the disease-free survival (DFS) rate at 1 year, 3 years, and 5 years after operation was 95.1%, 80.9% and 75.6%. There was no significant difference in OS and DFS between the two groups. Multivariate Cox regression analysis of OS found that lymph node metastasis, anastomotic fistula and chylothorax were independent risk factors for OS. Multivariate Cox regression analysis of DFS found that lymph node metastasis, anastomotic fistula, chylothorax, and vascular cancer thrombus were independent risk factors for OS.Conclusion MIE can achieve the same long-term effects as OE, with less intraoperative bleeding, more lymph nodes dissected, and lower incidence of postoperative pulmonary infections, but it takes longer operation time.

Citation： LIU Lin, ZHANG Yong, WANG Xiaolin, SHU Yusheng. Prognostic analysis of pT1b esophageal squamous cell carcinoma after open or minimally invasive esophagectomy. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2021, 28(2): 225-232. doi: 10.7507/1007-4848.202004056 Copy

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(6): 394-424.
2.	Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
3.	Li KK, Wang YJ, Liu XH, et al. The effect of postoperative complications on survival of patients after minimally invasive esophagectomy for esophageal cancer. Surg Endosc, 2017, 31(9): 3475-3482.
4.	Ajani JA, D'Amico TA, Bentrem DJ, et al. Esophageal and esophagogastric junction cancers, version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2019, 17(7): 855-883.
5.	McK Manson J, Beasley WD. A personal perspective on controversies in the surgical management of oesophageal cancer. Ann R Coll Surg Engl, 2014, 96(8): 575-578.
6.	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.
7.	Qi X, Li M, Zhao S, et al. Prevalence of metastasis in T1b esophageal squamous cell carcinoma: a retrospective analysis of 258 Chinese patients. J Thorac Dis, 2016, 8(5): 966-976.
8.	方文涛. 通过食管癌TNM新分期(第八版)解读2017年NCCN食管鳞癌诊疗指南. 中华胃肠外科杂志, 2017, 20(10): 1122-1126.
9.	Rice TW, Chen LQ, Hofstetter WL, et al. Worldwide esophageal cancer collaboration: pathologic staging data. Dis Esophagus, 2016, 29(7): 724-733.
10.	Rice TW, Gress DM, Patil DT, et al. Cancer of the esophagus and esophagogastric junction-major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin, 2017, 67(4): 304-317.
11.	Dubecz A, Kern M, Solymosi N, et al. Predictors of lymph node metastasis in surgically resected T1 esophageal cancer. Ann Thorac Surg, 2015, 99(6): 1879-1885.
12.	郝曙光, 李志刚, 方文涛, 等. T1b期食管癌手术方式的选择. 中华胃肠外科杂志, 2015, 18(9): 885-888.
13.	Yibulayin W, Abulizi S, Lv H, et al. Minimally invasive oesophagectomy versus open esophagectomy for resectable esophageal cancer: A meta-analysis. World J Surg Oncol, 2016, 14(1): 304.
14.	Mu JW, Gao SG, Xue Q, et al. Updated experiences with minimally invasive McKeown esophagectomy for esophageal cancer. World J Gastroenterol, 2015, 21(45): 12873-12881.
15.	孙超, 石维平, 吕小夏, 等. 三切口食管癌切除术:胸腔镜与开放手术的术后并发症分析. 中华腔镜外科杂志(电子版), 2016, 9(6): 354-357.
16.	Lin M, Shen Y, Feng M, et al. Minimally invasive esophagectomy: Chinese experiences. J Vis Surg, 2016, 2: 134.
17.	方文涛, 陈文虎. 食管癌手术治疗原则和淋巴结清扫. 中国癌症杂志, 2011, 21(7): 522-527.
18.	茅腾, 方文涛, 谷志涛, 等. 腔镜微创与开放食管癌根治术围手术期并发症和淋巴结清扫的比较研究. 中华胃肠外科杂志, 2012, 15(9): 922-925.
19.	Guo W, Zou YB, Ma Z, et al. One surgeon's learning curve for video-assisted thoracoscopic esophagectomy for esophageal cancer with the patient in lateral position: how many cases are needed to reach competence? Surg Endosc, 2013, 27(4): 1346-1352.
20.	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.
21.	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.
22.	王文凭, 何松林, 杨玉赏, 等. 食管癌微创外科手术的现状与思考. 中国胸心血管外科临床杂志, 2018, 25(4): 338-344.
23.	Li B, Yang Y, Sun Y, et al. Minimally invasive esophagectomy for esophageal squamous cell carcinoma—Shanghai Chest Hospital experience. J Thorac Dis, 2018, 10(6): 3800-3807.
24.	Lv L, Hu W, Ren Y, et al. Minimally invasive esophagectomy versus open esophagectomy for esophageal cancer: A meta-analysis. Onco Targets Ther, 2016, 9: 6751-6762.
25.	Kauppi J, Räsänen J, Sihvo E, et al. Open versus minimally invasive esophagectomy: Clinical outcomes for locally advanced esophageal adenocarcinoma. Surg Endosc, 2015, 29(9): 2614-2619.
26.	Takeuchi H, Miyata H, Gotoh M, et al. A risk model for esophagectomy using data of 5354 patients included in a Japanese nationwide web-based database. Ann Surg, 2014, 260(2): 259-266.
27.	Kim DU, Lee JH, Min BH, et al. Risk factors of lymph node metastasis in T1 esophageal squamous cell carcinoma. J Gastroenterol Hepatol, 2008, 23(4): 619-625.
28.	段晓峰, 尚晓滨, 唐鹏, 等. T1期食管癌淋巴结转移的预后因素分析. 中华外科杂志, 2017, 55(9): 690-695.
29.	Straatman J, van der Wielen N, Cuesta MA, et al. Minimally invasive versus open esophageal resection: three-year follow-up of the previously reported randomized controlled trial: the TIME trial. Ann Surg, 2017, 266(2): 232-236.
30.	Wang H, Feng M, Tan L, et al. Comparison of the short-term quality of life in patients with esophageal cancer after subtotal esophagectomy via video-assisted thoracoscopic or open surgery. Dis Esophagus, 2010, 23(5): 408-414.
31.	Rutegård M, Lagergren P, Rouvelas I, et al. Intrathoracic anastomotic leakage and mortality after esophageal cancer resection: A population-based study. Ann Surg Oncol, 2012, 19(1): 99-103.
32.	Kofoed SC, Calatayud D, Jensen LS, et al. Intrathoracic anastomotic leakage after gastroesophageal cancer resection is associated with reduced long-term survival. World J Surg, 2014, 38(1): 114-119.
33.	Kofoed SC, Calatayud D, Jensen LS, et al. Intrathoracic anastomotic leakage after gastroesophageal cancer resection is associated with increased risk of recurrence. J Thorac Cardiovasc Surg, 2015, 150(1): 42-48.
34.	van der Schaaf M, Johar A, Wijnhoven B, et al. Extent of lymph node removal during esophageal cancer surgery and survival. J Natl Cancer Inst, 2015, 107(5): djv043.
35.	Hölscher AH, Bollschweiler E, Schröder W, et al. Prognostic impact of upper, middle, and lower third mucosal or submucosal infiltration in early esophageal cancer. Ann Surg, 2011, 254(5): 802-807.
36.	Mu JW, Gao SG, Xue Q, et al. Comparison of short-term outcomes and three year survival between total minimally invasive McKeown and dual-incision esophagectomy. Thorac Cancer, 2017, 8(2): 80-87.
37.	Li H, Zhang Y, Cai H, et al. Pattern of lymph node metastases in patients with squamous cell carcinoma of the thoracic esophagus who underwent three-field lymphadenectomy. Eur Surg Res, 2007, 39(1): 1-6.
38.	彭凯明, 林济红, 余绍斌, 等. pT1胸段食管鳞癌根治术后复发转移的危险因素分析. 临床外科杂志, 2018, 26(9): 657-661.
39.	Tachezy M, Tiebel AK, Gebauer F, et al. Prognostic impact of perineural, blood and lymph vessel invasion for esophageal cancer. Histol Histopathol, 2014, 29(11): 1467-1475.

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(6): 394-424.
2. Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
3. Li KK, Wang YJ, Liu XH, et al. The effect of postoperative complications on survival of patients after minimally invasive esophagectomy for esophageal cancer. Surg Endosc, 2017, 31(9): 3475-3482.
4. Ajani JA, D'Amico TA, Bentrem DJ, et al. Esophageal and esophagogastric junction cancers, version 2.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2019, 17(7): 855-883.
5. McK Manson J, Beasley WD. A personal perspective on controversies in the surgical management of oesophageal cancer. Ann R Coll Surg Engl, 2014, 96(8): 575-578.
6. 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.
7. Qi X, Li M, Zhao S, et al. Prevalence of metastasis in T1b esophageal squamous cell carcinoma: a retrospective analysis of 258 Chinese patients. J Thorac Dis, 2016, 8(5): 966-976.
8. 方文涛. 通过食管癌TNM新分期(第八版)解读2017年NCCN食管鳞癌诊疗指南. 中华胃肠外科杂志, 2017, 20(10): 1122-1126.
9. Rice TW, Chen LQ, Hofstetter WL, et al. Worldwide esophageal cancer collaboration: pathologic staging data. Dis Esophagus, 2016, 29(7): 724-733.
10. Rice TW, Gress DM, Patil DT, et al. Cancer of the esophagus and esophagogastric junction-major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin, 2017, 67(4): 304-317.
11. Dubecz A, Kern M, Solymosi N, et al. Predictors of lymph node metastasis in surgically resected T1 esophageal cancer. Ann Thorac Surg, 2015, 99(6): 1879-1885.
12. 郝曙光, 李志刚, 方文涛, 等. T1b期食管癌手术方式的选择. 中华胃肠外科杂志, 2015, 18(9): 885-888.
13. Yibulayin W, Abulizi S, Lv H, et al. Minimally invasive oesophagectomy versus open esophagectomy for resectable esophageal cancer: A meta-analysis. World J Surg Oncol, 2016, 14(1): 304.
14. Mu JW, Gao SG, Xue Q, et al. Updated experiences with minimally invasive McKeown esophagectomy for esophageal cancer. World J Gastroenterol, 2015, 21(45): 12873-12881.
15. 孙超, 石维平, 吕小夏, 等. 三切口食管癌切除术:胸腔镜与开放手术的术后并发症分析. 中华腔镜外科杂志(电子版), 2016, 9(6): 354-357.
16. Lin M, Shen Y, Feng M, et al. Minimally invasive esophagectomy: Chinese experiences. J Vis Surg, 2016, 2: 134.
17. 方文涛, 陈文虎. 食管癌手术治疗原则和淋巴结清扫. 中国癌症杂志, 2011, 21(7): 522-527.
18. 茅腾, 方文涛, 谷志涛, 等. 腔镜微创与开放食管癌根治术围手术期并发症和淋巴结清扫的比较研究. 中华胃肠外科杂志, 2012, 15(9): 922-925.
19. Guo W, Zou YB, Ma Z, et al. One surgeon's learning curve for video-assisted thoracoscopic esophagectomy for esophageal cancer with the patient in lateral position: how many cases are needed to reach competence? Surg Endosc, 2013, 27(4): 1346-1352.
20. 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.
21. 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.
22. 王文凭, 何松林, 杨玉赏, 等. 食管癌微创外科手术的现状与思考. 中国胸心血管外科临床杂志, 2018, 25(4): 338-344.
23. Li B, Yang Y, Sun Y, et al. Minimally invasive esophagectomy for esophageal squamous cell carcinoma—Shanghai Chest Hospital experience. J Thorac Dis, 2018, 10(6): 3800-3807.
24. Lv L, Hu W, Ren Y, et al. Minimally invasive esophagectomy versus open esophagectomy for esophageal cancer: A meta-analysis. Onco Targets Ther, 2016, 9: 6751-6762.
25. Kauppi J, Räsänen J, Sihvo E, et al. Open versus minimally invasive esophagectomy: Clinical outcomes for locally advanced esophageal adenocarcinoma. Surg Endosc, 2015, 29(9): 2614-2619.
26. Takeuchi H, Miyata H, Gotoh M, et al. A risk model for esophagectomy using data of 5354 patients included in a Japanese nationwide web-based database. Ann Surg, 2014, 260(2): 259-266.
27. Kim DU, Lee JH, Min BH, et al. Risk factors of lymph node metastasis in T1 esophageal squamous cell carcinoma. J Gastroenterol Hepatol, 2008, 23(4): 619-625.
28. 段晓峰, 尚晓滨, 唐鹏, 等. T1期食管癌淋巴结转移的预后因素分析. 中华外科杂志, 2017, 55(9): 690-695.
29. Straatman J, van der Wielen N, Cuesta MA, et al. Minimally invasive versus open esophageal resection: three-year follow-up of the previously reported randomized controlled trial: the TIME trial. Ann Surg, 2017, 266(2): 232-236.
30. Wang H, Feng M, Tan L, et al. Comparison of the short-term quality of life in patients with esophageal cancer after subtotal esophagectomy via video-assisted thoracoscopic or open surgery. Dis Esophagus, 2010, 23(5): 408-414.
31. Rutegård M, Lagergren P, Rouvelas I, et al. Intrathoracic anastomotic leakage and mortality after esophageal cancer resection: A population-based study. Ann Surg Oncol, 2012, 19(1): 99-103.
32. Kofoed SC, Calatayud D, Jensen LS, et al. Intrathoracic anastomotic leakage after gastroesophageal cancer resection is associated with reduced long-term survival. World J Surg, 2014, 38(1): 114-119.
33. Kofoed SC, Calatayud D, Jensen LS, et al. Intrathoracic anastomotic leakage after gastroesophageal cancer resection is associated with increased risk of recurrence. J Thorac Cardiovasc Surg, 2015, 150(1): 42-48.
34. van der Schaaf M, Johar A, Wijnhoven B, et al. Extent of lymph node removal during esophageal cancer surgery and survival. J Natl Cancer Inst, 2015, 107(5): djv043.
35. Hölscher AH, Bollschweiler E, Schröder W, et al. Prognostic impact of upper, middle, and lower third mucosal or submucosal infiltration in early esophageal cancer. Ann Surg, 2011, 254(5): 802-807.
36. Mu JW, Gao SG, Xue Q, et al. Comparison of short-term outcomes and three year survival between total minimally invasive McKeown and dual-incision esophagectomy. Thorac Cancer, 2017, 8(2): 80-87.
37. Li H, Zhang Y, Cai H, et al. Pattern of lymph node metastases in patients with squamous cell carcinoma of the thoracic esophagus who underwent three-field lymphadenectomy. Eur Surg Res, 2007, 39(1): 1-6.
38. 彭凯明, 林济红, 余绍斌, 等. pT1胸段食管鳞癌根治术后复发转移的危险因素分析. 临床外科杂志, 2018, 26(9): 657-661.
39. Tachezy M, Tiebel AK, Gebauer F, et al. Prognostic impact of perineural, blood and lymph vessel invasion for esophageal cancer. Histol Histopathol, 2014, 29(11): 1467-1475.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Prognostic analysis of pT1b esophageal squamous cell carcinoma after open or minimally invasive esophagectomy

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