Short-term outcomes of neoadjuvant immunotherapy combined with minimally invasive McKeown esophagectomy for locally advanced thoracic esophageal squamous cell carcinoma: A retrospective cohort study_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WU Hanran , LIU Changqing , SUN Xiaohui , TIAN Jieyong , MEI Xinyu , XU Meiqing ,  XIE Mingran

Department of Thoracic Surgery, The First Affiliated Hospital of University of Science and Technology of China, Hefei, 230001, P. R. China;

Corresponding author：

XIE Mingran, Email: xiemingran@hotmail.com

Keywords：

Esophageal neoplasms; thoracoscopes; esophagectomy; cervical anastomosis; neoadjuvant therapy

DOI：

10.7507/1007-4848.202305038

Video：

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Objective To investigate the feasibility, safety, and short-term efficacy of minimally invasive McKeown esophagectomy (MIME) in patients with locally advanced thoracic esophageal squamous cell carcinoma (TESCC) after neoadjuvant immunotherapy. Methods The clinical data of the patients with locally advanced TESCC in the First Affiliated Hospital of University of Science and Technology of China from July 2022 to March 2023 were restrospectively analyzed. They were divided into a neoadjuvant immunotherapy (NI) group and a non-neoadjuvant immunotherapy (NNI) group according to different preoperative neoadjuvant therapy. The perioperative clinical data and 3-month follow-up data were compared between the two groups. Results A total of 47 patients were collected, including 31 males and 16 females with a mean age of (67.57±7.64) years. There were 29 patients in the NI group and 18 patients in the NNI group. There were no statistical differences in baseline data, perioperative complications, short-term complications, surgical time, intraoperative bleeding, postoperative adjuvant therapy, metastasis/recurrence within 3 months, R0 resection rate, postoperative pathological staging decline, or College of American Pathologists (CAP) tumor regression grade between the two groups (P＞0.05). Conclusion Neoadjuvant immunotherapy combined with minimally invasive McKeown esophagectomy can be safely and effectively performed for patients with locally advanced TESCC without increasing operation time, intraoperative blood loss and perioperative complications.

Citation： WU Hanran, LIU Changqing, SUN Xiaohui, TIAN Jieyong, MEI Xinyu, XU Meiqing, XIE Mingran. Short-term outcomes of neoadjuvant immunotherapy combined with minimally invasive McKeown esophagectomy for locally advanced thoracic esophageal squamous cell carcinoma: A retrospective cohort study. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(12): 1767-1774. doi: 10.7507/1007-4848.202305038 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.	Eyck BM, van Lanschot JJB, Hulshof MCCM, et al. Ten-year outcome of neoadjuvant chemoradiotherapy plus surgery for esophageal cancer: The randomized controlled CROSS trial. J Clin Oncol, 2021, 39(18): 1995-2004.
3.	Yang H, Liu H, Chen Y, et al. Long-term efficacy of neoadjuvant chemoradiotherapy plus surgery for the treatment of locally advanced esophageal squamous cell carcinoma: The NEOCRTEC5010 randomized clinical trial. JAMA Surg, 2021, 156(8): 721-729.
4.	Kelly RJ, Ajani JA, Kuzdzal J, et al. Adjuvant nivolumab in resected esophageal or gastroesophageal junction cancer. N Engl J Med, 2021, 384(13): 1191-1203.
5.	Kumagai K, Rouvelas I, Tsai JA, et al. Meta-analysis of postoperative morbidity and perioperative mortality in patients receiving neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal and gastro-oesophageal junctional cancers. Br J Surg, 2014, 101(4): 321-338.
6.	Donohoe CL, Reynolds JV. Neoadjuvant treatment of locally advanced esophageal and junctional cancer: The evidence-base, current key questions and clinical trials. J Thorac Dis, 2017, 9(Suppl 8): S697-S704.
7.	Amin MB, Edge S, Grene FL, et al. AJCC Cancer Stating Manual. 8^th ed. New York: Springer, 2017.
8.	College of American Pathologists. Cancer protocol templates. URL: https//www. cap. org/protocols-and-guidelines/cancer-reporting-tools/cancer-protocol-templates. Accessed on June 11, 2022.
9.	刘勤, 雷彩鹏, 范俊利, 等. 新辅助放化疗与新辅助化疗后手术治疗食管癌的疗效比较. 食管疾病, 2022, 4(4): 265-268.Liu Q, Lei CP, Fan JL, et al. Cmoparison of curative effects of neoadjuvant chemoradiotherapy and neoadjuvant chemotherapy in the surgical treatment of esophageal cancer. J Esophag Dis, 2022, 4(4): 265-268.
10.	李红远. 可切除局部晚期食管癌新辅助治疗临床对照分析. 河南大学, 2019.Li HY. Controlled clinical study of preoperative neoadjuvant therapy in local advanced resectable esophageal cancer. Henan University, 2019.
11.	李京沛. 新辅助免疫联合同步化疗治疗可手术切除食管鳞癌的有效性和安全性研究. 广州医科大学, 2022.Li JP. Efficacy and safety of neoadjuvant immunotherapy plus chemotherapy in subjects with resectable esophageal squamous cell carcinoma. Guangzhou Medical University, 2022.
12.	宋春涛, 于永洋, 高振等. 局部晚期食管癌免疫治疗的现状及前景. 实用肿瘤杂志, 2023, 38(2): 195-201.Song CT, Yu YY, Gao Z, et al. Current situation and prospect of immunotherapy for locally advanced esophageal cancer. J Pract Oncol, 2023, 38(2): 195-201.
13.	王晨, 张沛刚, 马秉灵. 新辅助化疗联合胸腹腔镜手术治疗Ⅲa期和Ⅲb期食管鳞癌的疗效观察. 中国医学装备, 2022, 19(5): 129-132.Wang C, Zhang PG, Ma BL. Observantion of curative effect of neoadjuvant chemotherapy combined with thoracic laparoscopic surgery in treating esophageral squamous cell carcinoma at stage Ⅲa and Ⅲb. China Med Equip, 2022, 19(5): 129-132.
14.	Liu J, Li J, Lin W, et al. Neoadjuvant camrelizumab plus chemotherapy for resectable, locally advanced esophageal squamous cell carcinoma (NIC-ESCC2019): A multicenter, phase 2 study. Int J Cancer, 2022, 151(1): 128-137.
15.	Duan H, Wang T, Luo Z, et al. A multicenter single-arm trial of sintilimab in combination with chemotherapy for neoadjuvant treatment of resectable esophageal cancer (SIN-ICE study). Ann Transl Med, 2021, 9(22): 1700.
16.	Liu J, Yang Y, Liu Z, et al. Multicenter, single-arm, phase Ⅱ trial of camrelizumab and chemotherapy as neoadjuvant treatment for locally advanced esophageal squamous cell carcinoma. J Immunother Cancer, 2022, 10(3): e004291.
17.	聂洪鑫, 杨思豪, 刘洪刚, 等. 围术期食管癌术后食管胃吻合口瘘的危险因素及预测模型的建立. 中国胸心血管外科临床杂志, 2023, 30(4): 586-592.Nie HX, Yang SH, Liu HG, et al. Risk factors and prediction model of perioperative esophagogastric anastomotic leakage after esophageal cancer surgery. Chin J Clin Thorac Cardiovasc Surg, 2023, 30(4): 586-592.
18.	曹春平, 董梦圆, 王金菊. 食管癌患者切除术后并发急性呼吸衰竭的危险因素. 实用癌症杂志, 2023, 38(1): 136-138.Cao CP, Dong MY, Wang JJ. Risk factors of acute respiratory failure after resection of esophageal cancer. Pract J Cancer, 2023, 38(1): 136-138.
19.	Jin Z, Zhang J, Chen D, et al. Neoadjuvant chemoradiotherapy, chemotherapy, and radiotherapy do not significantly increase the incidence of anastomotic leakage after esophageal cancer surgery: A meta-analysis. Dis Esophagus, 2022, 35(9): doab089.
20.	肖林林, 秦建军, 王军. 食管癌新辅助治疗后cCR患者的疗效评价. 中华肿瘤防治杂志, 2020, 27(16): 1350-1356.Xiao LL, Qin JJ, Wang J. A systemic review of evaluation for complete clinical response after chemo (radio) therapy in patients with esophageal carcinoma. Chin J Cancer Prev Treat, 2020, 27(16): 1350-1356.
21.	李文华. 食管癌新辅助化疗后病理缓解患者的临床特点及预后. 郑州大学, 2021.Li WH. Clinical characteristics and prognosis of patients with pathological response after neoadjuvant chemotherapy for esophageal cancer. Zhengzhou University, 2021.
22.	王希龙, 修家伟, 李旭, 等. 卡瑞利珠单抗联合白蛋白紫杉醇+顺铂化疗用于局部晚期食管癌术前新辅助治疗临床效果观察. 临床军医杂志, 2022, 50(8): 806-809, 813.Wang XL, Xiu JW, Li X, et al. Clinical study of carrelizumab combined with albumin-bound paclitaxel and cisplatin in preoperative neoadjuvant therapy for locally advanced esophageal cancer. Clin J Med Offic, 2022, 50(8): 806-809, 813.
23.	Yamamoto S, Kato K, Daiko H, et al. Feasibility study of nivolumab as neoadjuvant chemotherapy for locally esophageal carcinoma: FRONTiER (JCOG1804E). Future Oncol, 2020, 16(19): 1351-1357.
24.	Duan H, Shao C, Pan M, et al. Neoadjuvant pembrolizumab and chemotherapy in resectable esophageal cancer: An open-label, single-arm study (PEN-ICE). Front Immunol, 2022, 13: 849984.
25.	Yan X, Duan H, Ni Y, et al. Tislelizumab combined with chemotherapy as neoadjuvant therapy for surgically resectable esophageal cancer: A prospective, single-arm, phase Ⅱ study (TD-NICE). Int J Surg, 2022, 103: 106680.
26.	Yang W, Xing X, Yeung SJ, et al. Neoadjuvant programmed cell death 1 blockade combined with chemotherapy for resectable esophageal squamous cell carcinoma. J Immunother Cancer, 2022, 10(1): e003497.
27.	Li Z, Liu J, Zhang M, et al. A phase Ⅱ study of neoadjuvant immunotherapy combined with chemotherapy (camrelizumab plus albumin paclitaxel and carboplatin) in resectable thoracic esophageal squamous cell cancer (NICE Study): Interim results. J Clin Oncol, 2021, 39(Suppl 15): 4060.
28.	周思呈. 两种新辅助治疗模式对于局部晚期食管癌预后影响的meta分析. 广州医科大学, 2021.Zhou SC. Meta analysis of prognostic effects of two neoadjuvant treatment models on local advanced esophageal carcinoma. Guangzhou Medical University, 2021.
29.	Ando N, Kato H, Igaki H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol, 2012, 19(1): 68-74.
30.	Mariette C, Dahan L, Mornex F, et al. Surgery alone versus chemoradiotherapy followed by surgery for stage Ⅰand Ⅱ esophageal cancer: Final analysis of randomized controlled phase Ⅲ trial FFCD 9901. J Clin Oncol, 2014, 32(23): 2416-2422.
31.	Gronnier C, Tréchot B, Duhamel A, et al. Impact of neoadjuvant chemoradiotherapy on postoperative outcomes after esophageal cancer resection: Results of a European multicenter study. Ann Surg, 2014, 260(5): 764-770.
32.	黄俊俊, 孙久贺, 张士法, 等. 新辅助免疫治疗在局部晚期可切除食管癌治疗中的应用进展. 中国胸心血管外科临床杂志, 2024, 31(7): 1058-1065.Huang JJ, Sun JH, Zhang SF, et al. Progress of neoadjuvant immunotherapy in the treatment of locally advanced resectable esophageal carcinoma. Chin J Clin Thorac Cardiovasc Surg, 2024, 31(7): 1058-1065.

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. Eyck BM, van Lanschot JJB, Hulshof MCCM, et al. Ten-year outcome of neoadjuvant chemoradiotherapy plus surgery for esophageal cancer: The randomized controlled CROSS trial. J Clin Oncol, 2021, 39(18): 1995-2004.
3. Yang H, Liu H, Chen Y, et al. Long-term efficacy of neoadjuvant chemoradiotherapy plus surgery for the treatment of locally advanced esophageal squamous cell carcinoma: The NEOCRTEC5010 randomized clinical trial. JAMA Surg, 2021, 156(8): 721-729.
4. Kelly RJ, Ajani JA, Kuzdzal J, et al. Adjuvant nivolumab in resected esophageal or gastroesophageal junction cancer. N Engl J Med, 2021, 384(13): 1191-1203.
5. Kumagai K, Rouvelas I, Tsai JA, et al. Meta-analysis of postoperative morbidity and perioperative mortality in patients receiving neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal and gastro-oesophageal junctional cancers. Br J Surg, 2014, 101(4): 321-338.
6. Donohoe CL, Reynolds JV. Neoadjuvant treatment of locally advanced esophageal and junctional cancer: The evidence-base, current key questions and clinical trials. J Thorac Dis, 2017, 9(Suppl 8): S697-S704.
7. Amin MB, Edge S, Grene FL, et al. AJCC Cancer Stating Manual. 8^th ed. New York: Springer, 2017.
8. College of American Pathologists. Cancer protocol templates. URL: https//www. cap. org/protocols-and-guidelines/cancer-reporting-tools/cancer-protocol-templates. Accessed on June 11, 2022.
9. 刘勤, 雷彩鹏, 范俊利, 等. 新辅助放化疗与新辅助化疗后手术治疗食管癌的疗效比较. 食管疾病, 2022, 4(4): 265-268.Liu Q, Lei CP, Fan JL, et al. Cmoparison of curative effects of neoadjuvant chemoradiotherapy and neoadjuvant chemotherapy in the surgical treatment of esophageal cancer. J Esophag Dis, 2022, 4(4): 265-268.
10. 李红远. 可切除局部晚期食管癌新辅助治疗临床对照分析. 河南大学, 2019.Li HY. Controlled clinical study of preoperative neoadjuvant therapy in local advanced resectable esophageal cancer. Henan University, 2019.
11. 李京沛. 新辅助免疫联合同步化疗治疗可手术切除食管鳞癌的有效性和安全性研究. 广州医科大学, 2022.Li JP. Efficacy and safety of neoadjuvant immunotherapy plus chemotherapy in subjects with resectable esophageal squamous cell carcinoma. Guangzhou Medical University, 2022.
12. 宋春涛, 于永洋, 高振等. 局部晚期食管癌免疫治疗的现状及前景. 实用肿瘤杂志, 2023, 38(2): 195-201.Song CT, Yu YY, Gao Z, et al. Current situation and prospect of immunotherapy for locally advanced esophageal cancer. J Pract Oncol, 2023, 38(2): 195-201.
13. 王晨, 张沛刚, 马秉灵. 新辅助化疗联合胸腹腔镜手术治疗Ⅲa期和Ⅲb期食管鳞癌的疗效观察. 中国医学装备, 2022, 19(5): 129-132.Wang C, Zhang PG, Ma BL. Observantion of curative effect of neoadjuvant chemotherapy combined with thoracic laparoscopic surgery in treating esophageral squamous cell carcinoma at stage Ⅲa and Ⅲb. China Med Equip, 2022, 19(5): 129-132.
14. Liu J, Li J, Lin W, et al. Neoadjuvant camrelizumab plus chemotherapy for resectable, locally advanced esophageal squamous cell carcinoma (NIC-ESCC2019): A multicenter, phase 2 study. Int J Cancer, 2022, 151(1): 128-137.
15. Duan H, Wang T, Luo Z, et al. A multicenter single-arm trial of sintilimab in combination with chemotherapy for neoadjuvant treatment of resectable esophageal cancer (SIN-ICE study). Ann Transl Med, 2021, 9(22): 1700.
16. Liu J, Yang Y, Liu Z, et al. Multicenter, single-arm, phase Ⅱ trial of camrelizumab and chemotherapy as neoadjuvant treatment for locally advanced esophageal squamous cell carcinoma. J Immunother Cancer, 2022, 10(3): e004291.
17. 聂洪鑫, 杨思豪, 刘洪刚, 等. 围术期食管癌术后食管胃吻合口瘘的危险因素及预测模型的建立. 中国胸心血管外科临床杂志, 2023, 30(4): 586-592.Nie HX, Yang SH, Liu HG, et al. Risk factors and prediction model of perioperative esophagogastric anastomotic leakage after esophageal cancer surgery. Chin J Clin Thorac Cardiovasc Surg, 2023, 30(4): 586-592.
18. 曹春平, 董梦圆, 王金菊. 食管癌患者切除术后并发急性呼吸衰竭的危险因素. 实用癌症杂志, 2023, 38(1): 136-138.Cao CP, Dong MY, Wang JJ. Risk factors of acute respiratory failure after resection of esophageal cancer. Pract J Cancer, 2023, 38(1): 136-138.
19. Jin Z, Zhang J, Chen D, et al. Neoadjuvant chemoradiotherapy, chemotherapy, and radiotherapy do not significantly increase the incidence of anastomotic leakage after esophageal cancer surgery: A meta-analysis. Dis Esophagus, 2022, 35(9): doab089.
20. 肖林林, 秦建军, 王军. 食管癌新辅助治疗后cCR患者的疗效评价. 中华肿瘤防治杂志, 2020, 27(16): 1350-1356.Xiao LL, Qin JJ, Wang J. A systemic review of evaluation for complete clinical response after chemo (radio) therapy in patients with esophageal carcinoma. Chin J Cancer Prev Treat, 2020, 27(16): 1350-1356.
21. 李文华. 食管癌新辅助化疗后病理缓解患者的临床特点及预后. 郑州大学, 2021.Li WH. Clinical characteristics and prognosis of patients with pathological response after neoadjuvant chemotherapy for esophageal cancer. Zhengzhou University, 2021.
22. 王希龙, 修家伟, 李旭, 等. 卡瑞利珠单抗联合白蛋白紫杉醇+顺铂化疗用于局部晚期食管癌术前新辅助治疗临床效果观察. 临床军医杂志, 2022, 50(8): 806-809, 813.Wang XL, Xiu JW, Li X, et al. Clinical study of carrelizumab combined with albumin-bound paclitaxel and cisplatin in preoperative neoadjuvant therapy for locally advanced esophageal cancer. Clin J Med Offic, 2022, 50(8): 806-809, 813.
23. Yamamoto S, Kato K, Daiko H, et al. Feasibility study of nivolumab as neoadjuvant chemotherapy for locally esophageal carcinoma: FRONTiER (JCOG1804E). Future Oncol, 2020, 16(19): 1351-1357.
24. Duan H, Shao C, Pan M, et al. Neoadjuvant pembrolizumab and chemotherapy in resectable esophageal cancer: An open-label, single-arm study (PEN-ICE). Front Immunol, 2022, 13: 849984.
25. Yan X, Duan H, Ni Y, et al. Tislelizumab combined with chemotherapy as neoadjuvant therapy for surgically resectable esophageal cancer: A prospective, single-arm, phase Ⅱ study (TD-NICE). Int J Surg, 2022, 103: 106680.
26. Yang W, Xing X, Yeung SJ, et al. Neoadjuvant programmed cell death 1 blockade combined with chemotherapy for resectable esophageal squamous cell carcinoma. J Immunother Cancer, 2022, 10(1): e003497.
27. Li Z, Liu J, Zhang M, et al. A phase Ⅱ study of neoadjuvant immunotherapy combined with chemotherapy (camrelizumab plus albumin paclitaxel and carboplatin) in resectable thoracic esophageal squamous cell cancer (NICE Study): Interim results. J Clin Oncol, 2021, 39(Suppl 15): 4060.
28. 周思呈. 两种新辅助治疗模式对于局部晚期食管癌预后影响的meta分析. 广州医科大学, 2021.Zhou SC. Meta analysis of prognostic effects of two neoadjuvant treatment models on local advanced esophageal carcinoma. Guangzhou Medical University, 2021.
29. Ando N, Kato H, Igaki H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol, 2012, 19(1): 68-74.
30. Mariette C, Dahan L, Mornex F, et al. Surgery alone versus chemoradiotherapy followed by surgery for stage Ⅰand Ⅱ esophageal cancer: Final analysis of randomized controlled phase Ⅲ trial FFCD 9901. J Clin Oncol, 2014, 32(23): 2416-2422.
31. Gronnier C, Tréchot B, Duhamel A, et al. Impact of neoadjuvant chemoradiotherapy on postoperative outcomes after esophageal cancer resection: Results of a European multicenter study. Ann Surg, 2014, 260(5): 764-770.
32. 黄俊俊, 孙久贺, 张士法, 等. 新辅助免疫治疗在局部晚期可切除食管癌治疗中的应用进展. 中国胸心血管外科临床杂志, 2024, 31(7): 1058-1065.Huang JJ, Sun JH, Zhang SF, et al. Progress of neoadjuvant immunotherapy in the treatment of locally advanced resectable esophageal carcinoma. Chin J Clin Thorac Cardiovasc Surg, 2024, 31(7): 1058-1065.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Short-term outcomes of neoadjuvant immunotherapy combined with minimally invasive McKeown esophagectomy for locally advanced thoracic esophageal squamous cell carcinoma: A retrospective cohort study

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