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.	劉勤, 雷彩鵬, 范俊利, 等. 新輔助放化療與新輔助化療后手術治療食管癌的療效比較. 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.	李紅遠. 可切除局部晚期食管癌新輔助治療臨床對照分析. 河南大學, 2019.Li HY. Controlled clinical study of preoperative neoadjuvant therapy in local advanced resectable esophageal cancer. Henan University, 2019.
11.	李京沛. 新輔助免疫聯合同步化療治療可手術切除食管鱗癌的有效性和安全性研究. 廣州醫科大學, 2022.Li JP. Efficacy and safety of neoadjuvant immunotherapy plus chemotherapy in subjects with resectable esophageal squamous cell carcinoma. Guangzhou Medical University, 2022.
12.	宋春濤, 于永洋, 高振等. 局部晚期食管癌免疫治療的現狀及前景. 實用腫瘤雜志, 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, 張沛剛, 馬秉靈. 新輔助化療聯合胸腹腔鏡手術治療Ⅲa期和Ⅲb期食管鱗癌的療效觀察. 中國醫學裝備, 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.	聶洪鑫, 楊思豪, 劉洪剛, 等. 圍術期食管癌術后食管胃吻合口瘺的危險因素及預測模型的建立. 中國胸心血管外科臨床雜志, 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, 董夢圓, 王金菊. 食管癌患者切除術后并發急性呼吸衰竭的危險因素. 實用癌癥雜志, 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, 秦建軍, 王軍. 食管癌新輔助治療后cCR患者的療效評價. 中華腫瘤防治雜志, 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.	李文華. 食管癌新輔助化療后病理緩解患者的臨床特點及預后. 鄭州大學, 2021.Li WH. Clinical characteristics and prognosis of patients with pathological response after neoadjuvant chemotherapy for esophageal cancer. Zhengzhou University, 2021.
22.	王希龍, 修家偉, 李旭, 等. 卡瑞利珠單抗聯合白蛋白紫杉醇+順鉑化療用于局部晚期食管癌術前新輔助治療臨床效果觀察. 臨床軍醫雜志, 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. 兩種新輔助治療模式對于局部晚期食管癌預后影響的meta分析. 廣州醫科大學, 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.	黃俊俊, 孫久賀, 張士法, 等. 新輔助免疫治療在局部晚期可切除食管癌治療中的應用進展. 中國胸心血管外科臨床雜志, 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. 劉勤, 雷彩鵬, 范俊利, 等. 新輔助放化療與新輔助化療后手術治療食管癌的療效比較. 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. 李紅遠. 可切除局部晚期食管癌新輔助治療臨床對照分析. 河南大學, 2019.Li HY. Controlled clinical study of preoperative neoadjuvant therapy in local advanced resectable esophageal cancer. Henan University, 2019.
11. 李京沛. 新輔助免疫聯合同步化療治療可手術切除食管鱗癌的有效性和安全性研究. 廣州醫科大學, 2022.Li JP. Efficacy and safety of neoadjuvant immunotherapy plus chemotherapy in subjects with resectable esophageal squamous cell carcinoma. Guangzhou Medical University, 2022.
12. 宋春濤, 于永洋, 高振等. 局部晚期食管癌免疫治療的現狀及前景. 實用腫瘤雜志, 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, 張沛剛, 馬秉靈. 新輔助化療聯合胸腹腔鏡手術治療Ⅲa期和Ⅲb期食管鱗癌的療效觀察. 中國醫學裝備, 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. 聶洪鑫, 楊思豪, 劉洪剛, 等. 圍術期食管癌術后食管胃吻合口瘺的危險因素及預測模型的建立. 中國胸心血管外科臨床雜志, 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, 董夢圓, 王金菊. 食管癌患者切除術后并發急性呼吸衰竭的危險因素. 實用癌癥雜志, 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, 秦建軍, 王軍. 食管癌新輔助治療后cCR患者的療效評價. 中華腫瘤防治雜志, 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. 李文華. 食管癌新輔助化療后病理緩解患者的臨床特點及預后. 鄭州大學, 2021.Li WH. Clinical characteristics and prognosis of patients with pathological response after neoadjuvant chemotherapy for esophageal cancer. Zhengzhou University, 2021.
22. 王希龍, 修家偉, 李旭, 等. 卡瑞利珠單抗聯合白蛋白紫杉醇+順鉑化療用于局部晚期食管癌術前新輔助治療臨床效果觀察. 臨床軍醫雜志, 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. 兩種新輔助治療模式對于局部晚期食管癌預后影響的meta分析. 廣州醫科大學, 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. 黃俊俊, 孫久賀, 張士法, 等. 新輔助免疫治療在局部晚期可切除食管癌治療中的應用進展. 中國胸心血管外科臨床雜志, 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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