Progress of neoadjuvant immunotherapy in the treatment of locally advanced resectable esophageal carcinoma_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

HUANG Junjun ¹ , SUN Jiuhe ² , ZHANG Shifa ² , LIU Hongfeng ² , SONG Ru ² , WANG Qian ¹ , CHEN Liji ¹ ,  CAI Haibo ²

1. Clinical Medical School of Jining, Jining, 272000, Shandong, P. R. China;
2. Department of Thoracic Surgery, Jining No.1 People's Hospital, Jining, 272000, Shandong, P. R. China;

Corresponding author：

CAI Haibo, Email: 13518670801@163.com

Keywords：

Neoadjuvant immunotherapy; locally advanced resectable esophageal carcinoma; review

DOI：

10.7507/1007-4848.202211040

Video：

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Surgery is the preferred treatment for resectable esophageal cancer, but in locally advanced esophageal cancer, the effect of surgery alone is not ideal, so surgery-based comprehensive treatment is the best option. Neoadjuvant therapy has become a standard treatment in the treatment of locally advanced resectable esophageal cancer. Neoadjuvant therapy includes neoadjuvant chemotherapy, radiochemotherapy, immunotherapy, targeted therapy, etc. With the significant efficacy and acceptable toxicity of immunotherapy in the first-line and second-line treatment of advanced esophageal cancer, neoadjuvant immunotherapy has become a research hotspot of locally advanced resectable esophageal cancer. This article reviews the latest research progress and some limitations of neoadjuvant immunotherapy in locally advanced resectable esophageal cancer.

Citation： HUANG Junjun, SUN Jiuhe, ZHANG Shifa, LIU Hongfeng, SONG Ru, WANG Qian, CHEN Liji, CAI Haibo. Progress of neoadjuvant immunotherapy in the treatment of locally advanced resectable esophageal carcinoma. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(7): 1058-1065. doi: 10.7507/1007-4848.202211040 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.	Zeng H, Chen W, Zheng R, et al. Changing cancer survival in China during 2003-15: A pooled analysis of 17 population-based cancer registries. Lancet Glob Health, 2018, 6(5): e555-e567.
3.	Short MW, Burgers KG, FRY VT. Esophageal cancer. Am Fam Physician, 2017, 95(1): 22-28.
4.	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.
5.	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.
6.	van Hagen P, Hulshof MC, van Lanschot JJ, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med, 2012, 366(22): 2074-2084.
7.	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.
8.	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.
9.	Yang H, Liu H, Chen Y, et al. Neoadjuvant chemoradiotherapy followed by surgery versus surgery alone for locally advanced squamous cell carcinoma of the esophagus (NEOCRTEC5010): A phaseⅢ multicenter, randomized, open-label clinical trial. J Clin Oncol, 2018, 36(27): 2796-2803.
10.	Mariette C, Dahan L, Mornex F, et al. Surgery alone versus chemoradiotherapy followed by surgery for stageⅠ and Ⅱ esophageal cancer: Final analysis of randomized controlled phase III trial FFCD 9901. J Clin Oncol, 2014, 32(23): 2416-2422.
11.	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.
12.	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.
13.	Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: A common denominator approach to cancer therapy. Cancer Cell, 2015, 27(4): 450-461.
14.	Gotwals P, Cameron S, Cipolletta D, et al. Prospects for combining targeted and conventional cancer therapy with immunotherapy. Nat Rev Cancer, 2017, 17(5): 286-301.
15.	Khan M, Arooj S, Wang H. Soluble B7-CD28 family inhibitory immune checkpoint proteins and anti-cancer immunotherapy. Front Immunol, 2021, 12: 651634.
16.	Bluestone JA, St Clair EW, Turka LA. CTLA4Ig: Bridging the basic immunology with clinical application. Immunity, 2006, 24(3): 233-238.
17.	Weber J. Ipilimumab: Controversies in its development, utility and autoimmune adverse events. Cancer Immunol Immunother, 2009, 58(5): 823-830.
18.	乌日罕, 呼群, 马强, 等. PD-1和PD-L1在肿瘤免疫逃逸中的作用机制及临床意义. 现代肿瘤医学, 2019, 27(9): 1635-1638.
19.	Moujaess E, Haddad FG, Eid R, et al. The emerging use of immune checkpoint blockade in the adjuvant setting for solid tumors: A review. Immunotherapy, 2019, 11(16): 1409-1422.
20.	Rong L, Liu Y, Hui Z, et al. PD-L1 expression and its clinicopathological correlation in advanced esophageal squamous cell carcinoma in a Chinese population. Diagn Pathol, 2019, 14(1): 6.
21.	Huang J, Xu J, Chen Y, et al. Camrelizumab versus investigator's choice of chemotherapy as second-line therapy for advanced or metastatic oesophageal squamous cell carcinoma (ESCORT): A multicentre, randomised, open-label, phase 3 study. Lancet Oncol, 2020, 21(6): 832-842.
22.	Kato K, Cho BC, Takahashi M, et al. Nivolumab versus chemotherapy in patients with advanced oesophageal squamous cell carcinoma refractory or intolerant to previous chemotherapy (ATTRACTION-3): A multicentre, randomised, open-label, phase 3 trial. Lancet Oncol, 2019, 20(11): 1506-1517.
23.	Shen L, Kato K, Kim SB, et al. Tislelizumab versus chemotherapy as second-line treatment for advanced or metastatic esophageal squamous cell carcinoma (RATIONALE-302): A randomized phase Ⅲ study. J Clin Oncol, 2022, 40(26): 3065-3076.
24.	Kojima T, Shah MA, Muro K, et al. Randomized Phase Ⅲ keynote-181 study of pembrolizumab versus chemotherapy in advanced esophageal cancer. J Clin Oncol, 2020, 38(35): 4138-4148.
25.	Luo H, Lu J, Bai Y, et al. Effect of camrelizumab vs placebo added to chemotherapy on survival and progression-free survival in patients with advanced or metastatic esophageal squamous cell carcinoma: the escort-1st randomized clinical trial. JAMA, 2021, 326(10): 916-925.
26.	Doki Y, Ajani JA, Kato K, et al. Nivolumab combination therapy in advanced esophageal squamous-cell carcinoma. N Engl J Med, 2022, 386(5): 449-462.
27.	Sun JM, Shen L, Shah MA, et al. Pembrolizumab plus chemotherapy versus chemotherapy alone for first-line treatment of advanced oesophageal cancer (KEYNOTE-590): A randomised, placebo-controlled, phase 3 study. Lancet, 2021, 398(10302): 759-771.
28.	Wang ZX, Cui C, Yao J, et al. Toripalimab plus chemotherapy in treatment-naïve, advanced esophageal squamous cell carcinoma (JUPITER-06): A multi-center phase 3 trial. Cancer Cell, 2022, 40(3): 277-288.
29.	Lu Z, Wang J, Shu Y, et al. Sintilimab versus placebo in combination with chemotherapy as first line treatment for locally advanced or metastatic oesophageal squamous cell carcinoma (ORIENT-15): Multicentre, randomised, double blind, phase 3 trial. BMJ, 2022, 377: e068714.
30.	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.
31.	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.
32.	Li Z, Liu J, Zhang M, et al. A PhaseⅡ 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.
33.	Yang P, Zhou X, Yang X, et al. Neoadjuvant camrelizumab plus chemotherapy in treating locally advanced esophageal squamous cell carcinoma patients: A pilot study. World J Surg Oncol, 2021, 19(1): 333.
34.	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.
35.	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.
36.	Shang X, Zhao G, Liang F, et al. Safety and effectiveness of pembrolizumab combined with paclitaxel and cisplatin as neoadjuvant therapy followed by surgery for locally advanced resectable (stage Ⅲ) esophageal squamous cell carcinoma: A study protocol for a prospective, single-arm, single-center, open-label, phase-Ⅱ trial (Keystone-001). Ann Transl Med, 2022, 10(4): 229.
37.	He W, Leng X, Mao T, et al. Toripalimab plus paclitaxel and carboplatin as neoadjuvant therapy in locally advanced resectable esophageal squamous cell carcinoma. Oncologist, 2022, 27(1): e18-e28.
38.	Gao L, Lu J, Zhang P, et al. Toripalimab combined with docetaxel and cisplatin neoadjuvant therapy for locally advanced esophageal squamous cell carcinoma: A single-center, single-arm clinical trial (ESONICT-2). J Gastrointest Oncol, 2022, 13(2): 478-487.
39.	Yan X, Duan H, Ni Y, et al. Tislelizumab combined with chemotherapy as neoadjuvant therapy for surgically resectable esophageal cancer: A prospective, single-arm, phaseⅡ study (TD-NICE). Int J Surg, 2022, 103: 106680.
40.	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.
41.	Zhang Z, Hong ZN, Xie S, et al. Neoadjuvant sintilimab plus chemotherapy for locally advanced esophageal squamous cell carcinoma: A single-arm, single-center, phase 2 trial (ESONICT-1). Ann Transl Med, 2021, 9(21): 1623.
42.	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.
43.	Yamamoto S, Kato K, Daiko H, Kojima T, et al. FRONTiER: A feasibility trial of nivolumab with neoadjuvant CF or DCF therapy for locally advanced esophageal carcinoma (JCOG1804E)—The short-term results of cohort A and B. J Clin Oncol, 2021, 39(Suppl 3): 202.
44.	Matsuda S, Yamamoto S, Kato K, et al. FRONTiER: A feasibility trial of nivolumab with neoadjuvant CF or DCF, FLOT therapy for locally advanced esophageal carcinoma (JCOG1804E)—Short-term results for cohorts C and D. J Clin Oncol, 2022, 40(Suppl 4): 286-286.
45.	Jing SW, Zhai C, Zhang W, et al. Comparison of neoadjuvant immunotherapy plus chemotherapy versus chemotherapy alone for patients with locally advanced esophageal squamous cell carcinoma: A propensity score matching. Front Immunol, 2022, 13: 970534.
46.	Xiao X, Yang YS, Zeng XX, et al. The comparisons of neoadjuvant chemoimmunotherapy versus chemoradiotherapy for oesophageal squamous cancer. Eur J Cardiothorac Surg, 2022, 62(1): ezac341.
47.	Zhang W, Yan C, Gao X, et al. Safety and feasibility of radiotherapy plus camrelizumab for locally advanced esophageal squamous cell carcinoma. Oncologist, 2021, 26(7): e1110-e1124.
48.	Li C, Zhao S, Zheng Y, et al. Preoperative pembrolizumab combined with chemoradiotherapy for oesophageal squamous cell carcinoma (PALACE-1). Eur J Cancer, 2021, 144: 232-241.
49.	Hong MH, Kim H, Park SY, et al. A phase Ⅱ trial of preoperative chemoradiotherapy and pembrolizumab for locally advanced esophageal squamous cell carcinoma (ESCC). JCO, 2019, 37(15 Suppl): 4027.
50.	Shah MA, Almhanna K, Iqbal S, et al. Multicenter, randomized phaseⅡ study of neoadjuvant pembrolizumab plus chemotherapy and chemoradiotherapy in esophageal adenocarcinoma (EAC). J Clin Oncol, 2021, 39(15_Suppl): 4005.
51.	van den Ende T, de Clercq NC, van Berge Henegouwen MI, et al. Neoadjuvant chemoradiotherapy combined with atezolizumab for resectable esophageal adenocarcinoma: A single-arm phaseⅡ feasibility trial (perfect). Clin Cancer Res, 2021, 27(12): 3351-3359.
52.	Xu X, Sun Z, Zhang Y, et al. Neoadjuvant chemoradiotherapy combined with perioperative toripalimab in locally advanced esophageal cancer. J Clin Oncol, 2022, 40(Suppl16): e16065.
53.	Jiang N, Jiang M, Zhu XZ, et al. SCALE-1: Safety and efficacy of short course neoadjuvant chemo-radiotherapy plus toripalimab for locally advanced resectable squamous cell carcinoma of esophagus. J Clin Oncol, 2022, 40(16_Suppl): 4063.
54.	Joseph KR, Nicole SK, Valsamo A, et al. Neoadjuvant nivolumab plus concurrent chemoradiation in stage Ⅱ/Ⅲ esophageal/gastroesophageal junction cancer. J Clin Oncol, 2019, 37(4_suppl): 142.
55.	Bauer L, Lang K. Randomized phase Ⅱ study of PET response-adapted combined multimodal therapy for esophageal cancer: Results of the CALGB 80803 (Alliance) trial. Strahlenther Onkol, 2022, 198(3): 322-324.
56.	Ku GY, Wu AJC, Sihag S, et al. Durvalumab (D) and PET-directed chemoradiation (CRT) after induction FOLFOX for esophageal adenocarcinoma. J Clin Oncol, 2021, 39(3_Suppl): 2264.

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. Zeng H, Chen W, Zheng R, et al. Changing cancer survival in China during 2003-15: A pooled analysis of 17 population-based cancer registries. Lancet Glob Health, 2018, 6(5): e555-e567.
3. Short MW, Burgers KG, FRY VT. Esophageal cancer. Am Fam Physician, 2017, 95(1): 22-28.
4. 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.
5. 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.
6. van Hagen P, Hulshof MC, van Lanschot JJ, et al. Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med, 2012, 366(22): 2074-2084.
7. 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.
8. 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.
9. Yang H, Liu H, Chen Y, et al. Neoadjuvant chemoradiotherapy followed by surgery versus surgery alone for locally advanced squamous cell carcinoma of the esophagus (NEOCRTEC5010): A phaseⅢ multicenter, randomized, open-label clinical trial. J Clin Oncol, 2018, 36(27): 2796-2803.
10. Mariette C, Dahan L, Mornex F, et al. Surgery alone versus chemoradiotherapy followed by surgery for stageⅠ and Ⅱ esophageal cancer: Final analysis of randomized controlled phase III trial FFCD 9901. J Clin Oncol, 2014, 32(23): 2416-2422.
11. 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.
12. 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.
13. Topalian SL, Drake CG, Pardoll DM. Immune checkpoint blockade: A common denominator approach to cancer therapy. Cancer Cell, 2015, 27(4): 450-461.
14. Gotwals P, Cameron S, Cipolletta D, et al. Prospects for combining targeted and conventional cancer therapy with immunotherapy. Nat Rev Cancer, 2017, 17(5): 286-301.
15. Khan M, Arooj S, Wang H. Soluble B7-CD28 family inhibitory immune checkpoint proteins and anti-cancer immunotherapy. Front Immunol, 2021, 12: 651634.
16. Bluestone JA, St Clair EW, Turka LA. CTLA4Ig: Bridging the basic immunology with clinical application. Immunity, 2006, 24(3): 233-238.
17. Weber J. Ipilimumab: Controversies in its development, utility and autoimmune adverse events. Cancer Immunol Immunother, 2009, 58(5): 823-830.
18. 乌日罕, 呼群, 马强, 等. PD-1和PD-L1在肿瘤免疫逃逸中的作用机制及临床意义. 现代肿瘤医学, 2019, 27(9): 1635-1638.
19. Moujaess E, Haddad FG, Eid R, et al. The emerging use of immune checkpoint blockade in the adjuvant setting for solid tumors: A review. Immunotherapy, 2019, 11(16): 1409-1422.
20. Rong L, Liu Y, Hui Z, et al. PD-L1 expression and its clinicopathological correlation in advanced esophageal squamous cell carcinoma in a Chinese population. Diagn Pathol, 2019, 14(1): 6.
21. Huang J, Xu J, Chen Y, et al. Camrelizumab versus investigator's choice of chemotherapy as second-line therapy for advanced or metastatic oesophageal squamous cell carcinoma (ESCORT): A multicentre, randomised, open-label, phase 3 study. Lancet Oncol, 2020, 21(6): 832-842.
22. Kato K, Cho BC, Takahashi M, et al. Nivolumab versus chemotherapy in patients with advanced oesophageal squamous cell carcinoma refractory or intolerant to previous chemotherapy (ATTRACTION-3): A multicentre, randomised, open-label, phase 3 trial. Lancet Oncol, 2019, 20(11): 1506-1517.
23. Shen L, Kato K, Kim SB, et al. Tislelizumab versus chemotherapy as second-line treatment for advanced or metastatic esophageal squamous cell carcinoma (RATIONALE-302): A randomized phase Ⅲ study. J Clin Oncol, 2022, 40(26): 3065-3076.
24. Kojima T, Shah MA, Muro K, et al. Randomized Phase Ⅲ keynote-181 study of pembrolizumab versus chemotherapy in advanced esophageal cancer. J Clin Oncol, 2020, 38(35): 4138-4148.
25. Luo H, Lu J, Bai Y, et al. Effect of camrelizumab vs placebo added to chemotherapy on survival and progression-free survival in patients with advanced or metastatic esophageal squamous cell carcinoma: the escort-1st randomized clinical trial. JAMA, 2021, 326(10): 916-925.
26. Doki Y, Ajani JA, Kato K, et al. Nivolumab combination therapy in advanced esophageal squamous-cell carcinoma. N Engl J Med, 2022, 386(5): 449-462.
27. Sun JM, Shen L, Shah MA, et al. Pembrolizumab plus chemotherapy versus chemotherapy alone for first-line treatment of advanced oesophageal cancer (KEYNOTE-590): A randomised, placebo-controlled, phase 3 study. Lancet, 2021, 398(10302): 759-771.
28. Wang ZX, Cui C, Yao J, et al. Toripalimab plus chemotherapy in treatment-naïve, advanced esophageal squamous cell carcinoma (JUPITER-06): A multi-center phase 3 trial. Cancer Cell, 2022, 40(3): 277-288.
29. Lu Z, Wang J, Shu Y, et al. Sintilimab versus placebo in combination with chemotherapy as first line treatment for locally advanced or metastatic oesophageal squamous cell carcinoma (ORIENT-15): Multicentre, randomised, double blind, phase 3 trial. BMJ, 2022, 377: e068714.
30. 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.
31. 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.
32. Li Z, Liu J, Zhang M, et al. A PhaseⅡ 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.
33. Yang P, Zhou X, Yang X, et al. Neoadjuvant camrelizumab plus chemotherapy in treating locally advanced esophageal squamous cell carcinoma patients: A pilot study. World J Surg Oncol, 2021, 19(1): 333.
34. 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.
35. 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.
36. Shang X, Zhao G, Liang F, et al. Safety and effectiveness of pembrolizumab combined with paclitaxel and cisplatin as neoadjuvant therapy followed by surgery for locally advanced resectable (stage Ⅲ) esophageal squamous cell carcinoma: A study protocol for a prospective, single-arm, single-center, open-label, phase-Ⅱ trial (Keystone-001). Ann Transl Med, 2022, 10(4): 229.
37. He W, Leng X, Mao T, et al. Toripalimab plus paclitaxel and carboplatin as neoadjuvant therapy in locally advanced resectable esophageal squamous cell carcinoma. Oncologist, 2022, 27(1): e18-e28.
38. Gao L, Lu J, Zhang P, et al. Toripalimab combined with docetaxel and cisplatin neoadjuvant therapy for locally advanced esophageal squamous cell carcinoma: A single-center, single-arm clinical trial (ESONICT-2). J Gastrointest Oncol, 2022, 13(2): 478-487.
39. Yan X, Duan H, Ni Y, et al. Tislelizumab combined with chemotherapy as neoadjuvant therapy for surgically resectable esophageal cancer: A prospective, single-arm, phaseⅡ study (TD-NICE). Int J Surg, 2022, 103: 106680.
40. 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.
41. Zhang Z, Hong ZN, Xie S, et al. Neoadjuvant sintilimab plus chemotherapy for locally advanced esophageal squamous cell carcinoma: A single-arm, single-center, phase 2 trial (ESONICT-1). Ann Transl Med, 2021, 9(21): 1623.
42. 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.
43. Yamamoto S, Kato K, Daiko H, Kojima T, et al. FRONTiER: A feasibility trial of nivolumab with neoadjuvant CF or DCF therapy for locally advanced esophageal carcinoma (JCOG1804E)—The short-term results of cohort A and B. J Clin Oncol, 2021, 39(Suppl 3): 202.
44. Matsuda S, Yamamoto S, Kato K, et al. FRONTiER: A feasibility trial of nivolumab with neoadjuvant CF or DCF, FLOT therapy for locally advanced esophageal carcinoma (JCOG1804E)—Short-term results for cohorts C and D. J Clin Oncol, 2022, 40(Suppl 4): 286-286.
45. Jing SW, Zhai C, Zhang W, et al. Comparison of neoadjuvant immunotherapy plus chemotherapy versus chemotherapy alone for patients with locally advanced esophageal squamous cell carcinoma: A propensity score matching. Front Immunol, 2022, 13: 970534.
46. Xiao X, Yang YS, Zeng XX, et al. The comparisons of neoadjuvant chemoimmunotherapy versus chemoradiotherapy for oesophageal squamous cancer. Eur J Cardiothorac Surg, 2022, 62(1): ezac341.
47. Zhang W, Yan C, Gao X, et al. Safety and feasibility of radiotherapy plus camrelizumab for locally advanced esophageal squamous cell carcinoma. Oncologist, 2021, 26(7): e1110-e1124.
48. Li C, Zhao S, Zheng Y, et al. Preoperative pembrolizumab combined with chemoradiotherapy for oesophageal squamous cell carcinoma (PALACE-1). Eur J Cancer, 2021, 144: 232-241.
49. Hong MH, Kim H, Park SY, et al. A phase Ⅱ trial of preoperative chemoradiotherapy and pembrolizumab for locally advanced esophageal squamous cell carcinoma (ESCC). JCO, 2019, 37(15 Suppl): 4027.
50. Shah MA, Almhanna K, Iqbal S, et al. Multicenter, randomized phaseⅡ study of neoadjuvant pembrolizumab plus chemotherapy and chemoradiotherapy in esophageal adenocarcinoma (EAC). J Clin Oncol, 2021, 39(15_Suppl): 4005.
51. van den Ende T, de Clercq NC, van Berge Henegouwen MI, et al. Neoadjuvant chemoradiotherapy combined with atezolizumab for resectable esophageal adenocarcinoma: A single-arm phaseⅡ feasibility trial (perfect). Clin Cancer Res, 2021, 27(12): 3351-3359.
52. Xu X, Sun Z, Zhang Y, et al. Neoadjuvant chemoradiotherapy combined with perioperative toripalimab in locally advanced esophageal cancer. J Clin Oncol, 2022, 40(Suppl16): e16065.
53. Jiang N, Jiang M, Zhu XZ, et al. SCALE-1: Safety and efficacy of short course neoadjuvant chemo-radiotherapy plus toripalimab for locally advanced resectable squamous cell carcinoma of esophagus. J Clin Oncol, 2022, 40(16_Suppl): 4063.
54. Joseph KR, Nicole SK, Valsamo A, et al. Neoadjuvant nivolumab plus concurrent chemoradiation in stage Ⅱ/Ⅲ esophageal/gastroesophageal junction cancer. J Clin Oncol, 2019, 37(4_suppl): 142.
55. Bauer L, Lang K. Randomized phase Ⅱ study of PET response-adapted combined multimodal therapy for esophageal cancer: Results of the CALGB 80803 (Alliance) trial. Strahlenther Onkol, 2022, 198(3): 322-324.
56. Ku GY, Wu AJC, Sihag S, et al. Durvalumab (D) and PET-directed chemoradiation (CRT) after induction FOLFOX for esophageal adenocarcinoma. J Clin Oncol, 2021, 39(3_Suppl): 2264.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Progress of neoadjuvant immunotherapy in the treatment of locally advanced resectable esophageal carcinoma

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