Research progress in neoadjuvant therapy for locally advanced rectal cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LIU Yuqing ^1,2 , MAO Xiaoxiao ³ , RAN Xinxin ³ , CAO Xiaoman ³ , WANG Xiaodong ¹ ,  ZHAO Yaqin ⁴

1. Division of Gastrointestinal Surgery, Department of General Surgery，West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. West China School of Nursing, Sichuan University, Chengdu 610041, P. R. China;
3. West China School of Medicine, Sichuan University, Chengdu 610041, P. R. China;
4. Cancer Center, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

ZHAO Yaqin, Email: zhaoyaqin@wchscu.cn

Keywords：

locally advanced rectal cancer; neoadjuvant therapy; total neoadjuvant treatment; neoadjuvant target/immune therapy

DOI：

10.7507/1007-9424.202303073

Video：

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Objective To analyze the advantages and disadvantages of various neoadjuvant therapy , provide reference for clinical diagnosis and treatment, and provide direction for further research and exploration. Method The recent domestic and international medical databases (PubMed, EMBASE, Cochrane Library, VIP database, CNKI, WanFang database, etc.) were searched and the relevant literature on neoadjuvant therapy for locally advanced rectal cancer (LARC) were reviewed. Results Neoadjuvant therapy could decrease tumor staging, increase anal reserving rate, and reduce local recurrence rate, but it does not significantly reduce the rates of distant metastasis and lateral lymph node metastasis, nor does it improve long-term survival. More and more optimization neoadjuvant therapy had emerged. Molecular targeted drugs and immunotherapy were being attempted for clinical using, combined with research on emerging biomarkers, to improve the therapeutic efficacy of LARC patients, reduce treatment related side effects, and improve patient survival benefits. Conclusions Neoadjuvant therapy is the standard treatment strategy for LARC, and the exploration of neoadjuvant treatment models is expected to further improve treatment effectiveness, reduce toxic side effects, and improve survival prognosis. By combining tumor molecular biology indicators to identify and screen beneficiaries, it is expected to become an important direction for future research.

Citation： LIU Yuqing, MAO Xiaoxiao, RAN Xinxin, CAO Xiaoman, WANG Xiaodong, ZHAO Yaqin. Research progress in neoadjuvant therapy for locally advanced rectal cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(7): 882-888. doi: 10.7507/1007-9424.202303073 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.	刘宗超, 李哲轩, 张阳, 等. 2020全球癌症统计报告解读. 肿瘤综合治疗电子杂志, 2021, 7(2): 1-14.
3.	中国临床肿瘤学会(CSCO)结直肠癌专家委员会. 可切除的进展期结直肠癌围手术期治疗专家共识(2019). 中华胃肠外科杂志, 2019, 22(8): 701-710.
4.	Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med, 2004, 351(17): 1731-1740.
5.	Bahadoer RR, Dijkstra EA, van Etten B, et al. Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial. Lancet Oncol, 2021, 22(1): 29-42.
6.	Conroy T, Bosset JF, Etienne PL, et al. Neoadjuvant chemotherapy with FOLFIRINOX and preoperative chemoradiotherapy for patients with locally advanced rectal cancer (UNICANCER-PRODIGE 23): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol, 2021, 22(5): 702-715.
7.	Fernandez-Martos C, Brown G, Estevan R, et al. Preoperative chemotherapy in patients with intermediate-risk rectal adenocarcinoma selected by high-resolution magnetic resonance imaging: the GEMCAD 0801 phaseⅡ multicenter trial. Oncologist, 2014, 19(10): 1042-1043.
8.	AlGizawy SM, Essa HH, Ahmed BM. Chemotherapy alone for patients with stageⅡ/Ⅲ rectal cancer undergoing radical surgery. Oncologist, 2015, 20(7): 752-757.
9.	Koike J, Funahashi K, Yoshimatsu K, et al. Efficacy and safety of neoadjuvant chemotherapy with oxaliplatin, 5-fluorouracil, and levofolinate for T3 or T4 stageⅡ/Ⅲ rectal cancer: the FACT trial. Cancer Chemother Pharmacol, 2017, 79(3): 519-525.
10.	Smith CA, Kachnic LA. Evolving treatment paradigm in the treatment of locally advanced rectal cancer. J Natl Compr Canc Netw, 2018, 16(7): 909-915.
11.	Gérard A, Buyse M, Nordlinger B, et al. Preoperative radiotherapy as adjuvant treatment in rectal cancer. Final results of a randomized study of the European Organization for Research and Treatment of Cancer (EORTC). Ann Surg, 1988, 208(5): 606-614.
12.	Swedish Rectal Cancer Trial, Cedermark B, Dahlberg M, et al. Improved survival with preoperative radiotherapy in resectable rectal cancer. N Engl J Med, 1997, 336(14): 980-987.
13.	Bruheim K, Guren MG, Skovlund E, et al. Late side effects and quality of life after radiotherapy for rectal cancer. Int J Radiat Oncol Biol Phys, 2010, 76(4): 1005-1011.
14.	Heriot AG, Tekkis PP, Fazio VW, et al. Adjuvant radiotherapy is associated with increased sexual dysfunction in male patients undergoing resection for rectal cancer: a predictive model. Ann Surg, 2005, 242(4): 502-511.
15.	Rahbari NN, Elbers H, Askoxylakis V, et al. Neoadjuvant radiotherapy for rectal cancer: meta-analysis of randomized controlled trials. Ann Surg Oncol, 2013, 20(13): 4169-4182.
16.	Sauer R, Liersch T, Merkel S, et al. Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: results of the German CAO/ARO/AIO-94 randomized phase Ⅲ trial after a median follow-up of 11 years. J Clin Oncol, 2012, 30(16): 1926-1933.
17.	Gérard JP, Conroy T, Bonnetain F, et al. Preoperative radiotherapy with or without concurrent fluorouracil and leucovorin in T3-4 rectal cancers: results of FFCD 9203. J Clin Oncol, 2006, 24(28): 4620-4625.
18.	Duzova M, Basaran H, Inan G, et al. Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: Outcomes of survival, toxicity, sphincter preserving and prognostic factors. Transpl Immunol, 2021, 69: 101489. doi: 10.1016/j.trim.2021.101489.
19.	Bujko K, Nowacki MP, Nasierowska-Guttmejer A, et al. Long-term results of a randomized trial comparing preoperative short-course radiotherapy with preoperative conventionally fractionated chemoradiation for rectal cancer. Br J Surg, 2006, 93(10): 1215-1223.
20.	Ngan SY, Burmeister B, Fisher RJ, et al. Randomized trial of short-course radiotherapy versus long-course chemoradiation comparing rates of local recurrence in patients with T3 rectal cancer: Trans-Tasman Radiation Oncology Group trial 01. 04. J Clin Oncol, 2012, 30(31): 3827-3833.
21.	Erlandsson J, Holm T, Pettersson D, et al. Optimal fractionation of preoperative radiotherapy and timing to surgery for rectal cancer (Stockholm Ⅲ): a multicentre, randomised, non-blinded, phase 3, non-inferiority trial. Lancet Oncol, 2017, 18(3): 336-346.
22.	肖巍魏, 陈功. 全程新辅助治疗: 局部进展期直肠癌的术前治疗新策略. 中国普外基础与临床杂志, 2017, 24(11): 1311-1315.
23.	Fernandez-Martos C, Garcia-Albeniz X, Pericay C, et al. Chemoradiation, surgery and adjuvant chemotherapy versus induction chemotherapy followed by chemoradiation and surgery: long-term results of the Spanish GCR-3 phaseⅡ randomized trial†. Ann Oncol, 2015, 26(8): 1722-1728.
24.	Benson AB, Venook AP, Al-Hawary MM, et al. Rectal cancer, version 2. 2022, NCCN clinical practice guidelines in oncology . J Natl Compr Canc Netw, 2022, 20(10): 1139-1167.
25.	Deng Y, Chi P, Lan P, et al. Modified FOLFOX6 with or without radiation versus fluorouracil and leucovorin with radiation in neoadjuvant treatment of locally advanced rectal cancer: initial results of the Chinese FOWARC multicenter, open-label, randomized three-arm phase Ⅲ trial. J Clin Oncol, 2016, 34(27): 3300-3307.
26.	Weiser MR, Fichera A, Schrag D, et al. Progress in the PROSPECT trial: precision treatment for rectal cancer? Bull Am Coll Surg, 2015, 100(4): 51-52.
27.	Wang J, Fan J, Li C, et al. The impact of chemotherapy completion on the efficacy of irinotecan in the preoperative chemoradiotherapy of locally advanced rectal cancer: An expanded analysis of the cinclare phase Ⅲ trial. Clin Colorectal Cancer, 2020, 19(2): e58-e69. doi: 10.1016/j.clcc.2020.01.004.
28.	Sobrero AF, Maurel J, Fehrenbacher L, et al. EPIC: phase Ⅲ trial of cetuximab plus irinotecan after fluoropyrimidine and oxaliplatin failure in patients with metastatic colorectal cancer. J Clin Oncol, 2008, 26(14): 2311-2319.
29.	Dewdney A, Cunningham D, Tabernero J, et al. Multicenter randomized phaseⅡclinical trial comparing neoadjuvant oxaliplatin, capecitabine, and preoperative radiotherapy with or without cetuximab followed by total mesorectal excision in patients with high-risk rectal cancer (EXPERT-C). J Clin Oncol, 2012, 30(14): 1620-1627.
30.	Willett CG, Boucher Y, Duda DG, et al. Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J Clin Oncol, 2005, 23(31): 8136-8139.
31.	Willett CG, Boucher Y, di Tomaso E, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med, 2004, 10(2): 145-147.
32.	Chua YJ, Barbachano Y, Cunningham D, et al. Neoadjuvant capecitabine and oxaliplatin before chemoradiotherapy and total mesorectal excision in MRI-defined poor-risk rectal cancer: a phase 2 trial. Lancet Oncol, 2010, 11(3): 241-248.
33.	Grem JL. Sequencing of treatment in advanced unresectable colorectal cancer. J Natl Compr Canc Netw, 2013, 11 Suppl 4: S28-S37.
34.	Maeda K, Shibutani M, Otani H, et al. Neoadjuvant radiotherapy with capecitabine plus bevacizumab for locally advanced lower rectal cancer: results of a single-institute phaseⅡ study. Anticancer Res, 2018, 38(7): 4193-4197.
35.	Ludford K, Ho WJ, Thomas JV, et al. Neoadjuvant pembrolizumab in localized microsatellite instability high/deficient mismatch repair solid tumors. J Clin Oncol, 2023, 41(12): 2181-2190.
36.	Trojan J, Stintzing S, Haase O, et al. Complete pathological response after neoadjuvant short-course immunotherapy with ipilimumab and nivolumab in locally advanced MSI-H/dMMR rectal cancer. Oncologist, 2021, 26(12): e2110-e2114. doi: 10.1002/onco.13955.
37.	Shamseddine A, Zeidan YH, El Husseini Z, et al. Efficacy and safety-in analysis of short-course radiation followed by mFOLFOX-6 plus avelumab for locally advanced rectal adenocarcinoma. Radiat Oncol, 2020, 15(1): 233. doi: 10.1186/s13014-020-01673-6.
38.	Yuichiro Tsukada, Hideaki Bando, Koji Inamori, et al. Survival outcomes and functional results of VOLTAGE-A: Preoperative chemoradiotherapy (CRT) and consolidation nivolumab (nivo) in patients (pts) with both microsatellite stable (MSS) and microsatellite instability–high (MSI-H) locally advanced rectal cancer (LARC). J Clin Oncol, 2023, 41(Suppl 4): 108.Yuichiro Tsukada, Hideaki Bando, Koji Inamori, et al. Survival outcomes and functional results of VOLTAGE-A: Preoperative chemoradiotherapy (CRT) and consolidation nivolumab (nivo) in patients (pts) with both microsatellite stable (MSS) and microsatellite instability–high (MSI-H) locally advanced rectal cancer (LARC). J Clin Oncol, 2023, 41(Suppl 4): 108.
39.	DAI S, WANG F, SHEN Y, et al. Efficacy and safety of neoadjuvant preoperative short-course radiation followed by envafolimab plus CAPEOX in microsatellite stable (MSS)/mismatch repair proficient (pMMR) locally advanced rectal cancer. J Clin Oncol, 2023, 41(Suppl 4): 134.DAI S, WANG F, SHEN Y, et al. Efficacy and safety of neoadjuvant preoperative short-course radiation followed by envafolimab plus CAPEOX in microsatellite stable (MSS)/mismatch repair proficient (pMMR) locally advanced rectal cancer. J Clin Oncol, 2023, 41(Suppl 4): 134.
40.	Verschoor YL, Lambregts DMJ, Berg JVD, et al. Radiotherapy, atezolizumab, and bevacizumab in rectal cancers with the aim of organ preservation: The TARZAN study. J Clin Oncol, 2023, 41(Suppl 4): 158.Verschoor YL, Lambregts DMJ, Berg JVD, et al. Radiotherapy, atezolizumab, and bevacizumab in rectal cancers with the aim of organ preservation: The TARZAN study. J Clin Oncol, 2023, 41(Suppl 4): 158.
41.	George TJ, Yothers G, Rahma OE, et al. Long-term results from NRG-GI002: A phaseⅡ clinical trial platform using total neoadjuvant therapy (TNT) in locally advanced rectal cancer (LARC). Journal of Clinical Oncology, 2023, 41(Suppl 4): 7.George TJ, Yothers G, Rahma OE, et al. Long-term results from NRG-GI002: A phaseⅡ clinical trial platform using total neoadjuvant therapy (TNT) in locally advanced rectal cancer (LARC). Journal of Clinical Oncology, 2023, 41(Suppl 4): 7.
42.	Wang Y, Shen L, Wan J, et al. Short-course radiotherapy combined with CAPOX and toripalimab for the total neoadjuvant therapy of locally advanced rectal cancer: a randomized, prospective, multicentre, double-arm, phaseⅡ trial (TORCH). BMC Cancer, 2022, 22(1): 274. doi: 10.1186/s12885-022-09348-z.
43.	Yang Z, Zhang X, Zhang J, et al. Rationale and design of a prospective, multicenter, phaseⅡ clinical trial of safety and efficacy evaluation of long course neoadjuvant chemoradiotherapy plus tislelizumab followed by total mesorectal excision for locally advanced rectal cancer (NCRT-PD1-LARC trial). BMC Cancer, 2022, 22(1): 462. doi: 10.1186/s12885-022-09554-9.

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. 刘宗超, 李哲轩, 张阳, 等. 2020全球癌症统计报告解读. 肿瘤综合治疗电子杂志, 2021, 7(2): 1-14.
3. 中国临床肿瘤学会(CSCO)结直肠癌专家委员会. 可切除的进展期结直肠癌围手术期治疗专家共识(2019). 中华胃肠外科杂志, 2019, 22(8): 701-710.
4. Sauer R, Becker H, Hohenberger W, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med, 2004, 351(17): 1731-1740.
5. Bahadoer RR, Dijkstra EA, van Etten B, et al. Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial. Lancet Oncol, 2021, 22(1): 29-42.
6. Conroy T, Bosset JF, Etienne PL, et al. Neoadjuvant chemotherapy with FOLFIRINOX and preoperative chemoradiotherapy for patients with locally advanced rectal cancer (UNICANCER-PRODIGE 23): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol, 2021, 22(5): 702-715.
7. Fernandez-Martos C, Brown G, Estevan R, et al. Preoperative chemotherapy in patients with intermediate-risk rectal adenocarcinoma selected by high-resolution magnetic resonance imaging: the GEMCAD 0801 phaseⅡ multicenter trial. Oncologist, 2014, 19(10): 1042-1043.
8. AlGizawy SM, Essa HH, Ahmed BM. Chemotherapy alone for patients with stageⅡ/Ⅲ rectal cancer undergoing radical surgery. Oncologist, 2015, 20(7): 752-757.
9. Koike J, Funahashi K, Yoshimatsu K, et al. Efficacy and safety of neoadjuvant chemotherapy with oxaliplatin, 5-fluorouracil, and levofolinate for T3 or T4 stageⅡ/Ⅲ rectal cancer: the FACT trial. Cancer Chemother Pharmacol, 2017, 79(3): 519-525.
10. Smith CA, Kachnic LA. Evolving treatment paradigm in the treatment of locally advanced rectal cancer. J Natl Compr Canc Netw, 2018, 16(7): 909-915.
11. Gérard A, Buyse M, Nordlinger B, et al. Preoperative radiotherapy as adjuvant treatment in rectal cancer. Final results of a randomized study of the European Organization for Research and Treatment of Cancer (EORTC). Ann Surg, 1988, 208(5): 606-614.
12. Swedish Rectal Cancer Trial, Cedermark B, Dahlberg M, et al. Improved survival with preoperative radiotherapy in resectable rectal cancer. N Engl J Med, 1997, 336(14): 980-987.
13. Bruheim K, Guren MG, Skovlund E, et al. Late side effects and quality of life after radiotherapy for rectal cancer. Int J Radiat Oncol Biol Phys, 2010, 76(4): 1005-1011.
14. Heriot AG, Tekkis PP, Fazio VW, et al. Adjuvant radiotherapy is associated with increased sexual dysfunction in male patients undergoing resection for rectal cancer: a predictive model. Ann Surg, 2005, 242(4): 502-511.
15. Rahbari NN, Elbers H, Askoxylakis V, et al. Neoadjuvant radiotherapy for rectal cancer: meta-analysis of randomized controlled trials. Ann Surg Oncol, 2013, 20(13): 4169-4182.
16. Sauer R, Liersch T, Merkel S, et al. Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: results of the German CAO/ARO/AIO-94 randomized phase Ⅲ trial after a median follow-up of 11 years. J Clin Oncol, 2012, 30(16): 1926-1933.
17. Gérard JP, Conroy T, Bonnetain F, et al. Preoperative radiotherapy with or without concurrent fluorouracil and leucovorin in T3-4 rectal cancers: results of FFCD 9203. J Clin Oncol, 2006, 24(28): 4620-4625.
18. Duzova M, Basaran H, Inan G, et al. Preoperative versus postoperative chemoradiotherapy for locally advanced rectal cancer: Outcomes of survival, toxicity, sphincter preserving and prognostic factors. Transpl Immunol, 2021, 69: 101489. doi: 10.1016/j.trim.2021.101489.
19. Bujko K, Nowacki MP, Nasierowska-Guttmejer A, et al. Long-term results of a randomized trial comparing preoperative short-course radiotherapy with preoperative conventionally fractionated chemoradiation for rectal cancer. Br J Surg, 2006, 93(10): 1215-1223.
20. Ngan SY, Burmeister B, Fisher RJ, et al. Randomized trial of short-course radiotherapy versus long-course chemoradiation comparing rates of local recurrence in patients with T3 rectal cancer: Trans-Tasman Radiation Oncology Group trial 01. 04. J Clin Oncol, 2012, 30(31): 3827-3833.
21. Erlandsson J, Holm T, Pettersson D, et al. Optimal fractionation of preoperative radiotherapy and timing to surgery for rectal cancer (Stockholm Ⅲ): a multicentre, randomised, non-blinded, phase 3, non-inferiority trial. Lancet Oncol, 2017, 18(3): 336-346.
22. 肖巍魏, 陈功. 全程新辅助治疗: 局部进展期直肠癌的术前治疗新策略. 中国普外基础与临床杂志, 2017, 24(11): 1311-1315.
23. Fernandez-Martos C, Garcia-Albeniz X, Pericay C, et al. Chemoradiation, surgery and adjuvant chemotherapy versus induction chemotherapy followed by chemoradiation and surgery: long-term results of the Spanish GCR-3 phaseⅡ randomized trial†. Ann Oncol, 2015, 26(8): 1722-1728.
24. Benson AB, Venook AP, Al-Hawary MM, et al. Rectal cancer, version 2. 2022, NCCN clinical practice guidelines in oncology . J Natl Compr Canc Netw, 2022, 20(10): 1139-1167.
25. Deng Y, Chi P, Lan P, et al. Modified FOLFOX6 with or without radiation versus fluorouracil and leucovorin with radiation in neoadjuvant treatment of locally advanced rectal cancer: initial results of the Chinese FOWARC multicenter, open-label, randomized three-arm phase Ⅲ trial. J Clin Oncol, 2016, 34(27): 3300-3307.
26. Weiser MR, Fichera A, Schrag D, et al. Progress in the PROSPECT trial: precision treatment for rectal cancer? Bull Am Coll Surg, 2015, 100(4): 51-52.
27. Wang J, Fan J, Li C, et al. The impact of chemotherapy completion on the efficacy of irinotecan in the preoperative chemoradiotherapy of locally advanced rectal cancer: An expanded analysis of the cinclare phase Ⅲ trial. Clin Colorectal Cancer, 2020, 19(2): e58-e69. doi: 10.1016/j.clcc.2020.01.004.
28. Sobrero AF, Maurel J, Fehrenbacher L, et al. EPIC: phase Ⅲ trial of cetuximab plus irinotecan after fluoropyrimidine and oxaliplatin failure in patients with metastatic colorectal cancer. J Clin Oncol, 2008, 26(14): 2311-2319.
29. Dewdney A, Cunningham D, Tabernero J, et al. Multicenter randomized phaseⅡclinical trial comparing neoadjuvant oxaliplatin, capecitabine, and preoperative radiotherapy with or without cetuximab followed by total mesorectal excision in patients with high-risk rectal cancer (EXPERT-C). J Clin Oncol, 2012, 30(14): 1620-1627.
30. Willett CG, Boucher Y, Duda DG, et al. Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J Clin Oncol, 2005, 23(31): 8136-8139.
31. Willett CG, Boucher Y, di Tomaso E, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med, 2004, 10(2): 145-147.
32. Chua YJ, Barbachano Y, Cunningham D, et al. Neoadjuvant capecitabine and oxaliplatin before chemoradiotherapy and total mesorectal excision in MRI-defined poor-risk rectal cancer: a phase 2 trial. Lancet Oncol, 2010, 11(3): 241-248.
33. Grem JL. Sequencing of treatment in advanced unresectable colorectal cancer. J Natl Compr Canc Netw, 2013, 11 Suppl 4: S28-S37.
34. Maeda K, Shibutani M, Otani H, et al. Neoadjuvant radiotherapy with capecitabine plus bevacizumab for locally advanced lower rectal cancer: results of a single-institute phaseⅡ study. Anticancer Res, 2018, 38(7): 4193-4197.
35. Ludford K, Ho WJ, Thomas JV, et al. Neoadjuvant pembrolizumab in localized microsatellite instability high/deficient mismatch repair solid tumors. J Clin Oncol, 2023, 41(12): 2181-2190.
36. Trojan J, Stintzing S, Haase O, et al. Complete pathological response after neoadjuvant short-course immunotherapy with ipilimumab and nivolumab in locally advanced MSI-H/dMMR rectal cancer. Oncologist, 2021, 26(12): e2110-e2114. doi: 10.1002/onco.13955.
37. Shamseddine A, Zeidan YH, El Husseini Z, et al. Efficacy and safety-in analysis of short-course radiation followed by mFOLFOX-6 plus avelumab for locally advanced rectal adenocarcinoma. Radiat Oncol, 2020, 15(1): 233. doi: 10.1186/s13014-020-01673-6.
38. Yuichiro Tsukada, Hideaki Bando, Koji Inamori, et al. Survival outcomes and functional results of VOLTAGE-A: Preoperative chemoradiotherapy (CRT) and consolidation nivolumab (nivo) in patients (pts) with both microsatellite stable (MSS) and microsatellite instability–high (MSI-H) locally advanced rectal cancer (LARC). J Clin Oncol, 2023, 41(Suppl 4): 108.Yuichiro Tsukada, Hideaki Bando, Koji Inamori, et al. Survival outcomes and functional results of VOLTAGE-A: Preoperative chemoradiotherapy (CRT) and consolidation nivolumab (nivo) in patients (pts) with both microsatellite stable (MSS) and microsatellite instability–high (MSI-H) locally advanced rectal cancer (LARC). J Clin Oncol, 2023, 41(Suppl 4): 108.
39. DAI S, WANG F, SHEN Y, et al. Efficacy and safety of neoadjuvant preoperative short-course radiation followed by envafolimab plus CAPEOX in microsatellite stable (MSS)/mismatch repair proficient (pMMR) locally advanced rectal cancer. J Clin Oncol, 2023, 41(Suppl 4): 134.DAI S, WANG F, SHEN Y, et al. Efficacy and safety of neoadjuvant preoperative short-course radiation followed by envafolimab plus CAPEOX in microsatellite stable (MSS)/mismatch repair proficient (pMMR) locally advanced rectal cancer. J Clin Oncol, 2023, 41(Suppl 4): 134.
40. Verschoor YL, Lambregts DMJ, Berg JVD, et al. Radiotherapy, atezolizumab, and bevacizumab in rectal cancers with the aim of organ preservation: The TARZAN study. J Clin Oncol, 2023, 41(Suppl 4): 158.Verschoor YL, Lambregts DMJ, Berg JVD, et al. Radiotherapy, atezolizumab, and bevacizumab in rectal cancers with the aim of organ preservation: The TARZAN study. J Clin Oncol, 2023, 41(Suppl 4): 158.
41. George TJ, Yothers G, Rahma OE, et al. Long-term results from NRG-GI002: A phaseⅡ clinical trial platform using total neoadjuvant therapy (TNT) in locally advanced rectal cancer (LARC). Journal of Clinical Oncology, 2023, 41(Suppl 4): 7.George TJ, Yothers G, Rahma OE, et al. Long-term results from NRG-GI002: A phaseⅡ clinical trial platform using total neoadjuvant therapy (TNT) in locally advanced rectal cancer (LARC). Journal of Clinical Oncology, 2023, 41(Suppl 4): 7.
42. Wang Y, Shen L, Wan J, et al. Short-course radiotherapy combined with CAPOX and toripalimab for the total neoadjuvant therapy of locally advanced rectal cancer: a randomized, prospective, multicentre, double-arm, phaseⅡ trial (TORCH). BMC Cancer, 2022, 22(1): 274. doi: 10.1186/s12885-022-09348-z.
43. Yang Z, Zhang X, Zhang J, et al. Rationale and design of a prospective, multicenter, phaseⅡ clinical trial of safety and efficacy evaluation of long course neoadjuvant chemoradiotherapy plus tislelizumab followed by total mesorectal excision for locally advanced rectal cancer (NCRT-PD1-LARC trial). BMC Cancer, 2022, 22(1): 462. doi: 10.1186/s12885-022-09554-9.

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