Interpretation of European clinical practice guidelines for oligometastatic esophagogastric cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

 DUAN Xiaofeng , WANG Shangren , YUE Jie , JIANG Hongjing

Department of Minimally Invasive Esophageal Surgery, Key Laboratory of Cancer Prevention and Therapy, National Clinical Research Center for Cancer, Tianjin Medical University Cancer Hospital and Institute, Tianjin, 300060, P. R.China;

Corresponding author：

DUAN Xiaofeng, Email: xduan@tmu.edu.cn

Keywords：

Esophageal cancer; oligometastasis; guldeline interpretation

DOI：

10.7507/1007-4848.202412075

Video：

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In recent years, with the clinical application of minimally invasive surgical techniques and comprehensive perioperative treatment, the survival rate of locally advanced esophageal cancer has significantly improved. However, the treatment of metastatic esophagogastric cancer still relies mainly on systemic therapy, and immunotherapy combined with chemotherapy has become a first-line treatment option, prolonging the survival of patients with metastatic esophagal cancer. Oligometastatic esophagal cancer is expected to bring survival benefits through systemic therapy combined with local treatment. The 2024 European clinical practice guidelines for oligometastatic esophageal and gastric cancer have been officially released, which standardize the definition, diagnosis, and treatment of oligometastatic esophageal cancer for further prospective studies. The author interprets this guideline, especially by reviewing the clinical evidence of oligometastatic esophageal squamous cell carcinoma, to provide reference for the diagnosis and treatment of oligometastatic esophageal cancer in China.

1.	Qi L, Sun M, Liu W et al. Global esophageal cancer epidemiology in 2022 and predictions for 2050: A comprehensive analysis and projections based on GLOBOCAN data. Chin Med J (Engl), 2024, 137(24): 3108-3116.
2.	Yang H, Wang F, Hallemeier CL et al. Oesophageal cancer. Lancet, 2024, 404(10466): 1991-2005.
3.	Kroese TE, Christ SM, van Rossum PSN et al. Incidence and survival of patients with oligometastatic esophagogastric cancer: A multicenter cohort study. Radiother Oncol, 2022, 173 269-276.
4.	Elliott JA, Markar SR, Klevebro F et al. An international multicenter study exploring whether surveillance after esophageal cancer surgery impacts oncological and quality of life outcomes (ENSURE). Ann Surg, 2023, 277(5): e1035-e1044.
5.	Hellman S, Weichselbaum RR. Oligometastases. J Clin Oncol, 1995, 13(1): 8-10.
6.	van Hootegem SJM, de Pasqual CA, Giacopuzzi S et al. Outcomes after surgical treatment of oesophagogastric cancer with synchronous liver metastases: A multicentre retrospective cohort study. Cancers (Basel), 2024, 16(4): 797.
7.	Kroese TE, Bronzwaer S, van Rossum PSN et al. European clinical practice guidelines for the definition, diagnosis, and treatment of oligometastatic esophagogastric cancer (OMEC-4). Eur J Cancer, 2024, 204: 114062.
8.	Kroese TE, van Rossum PSN, Nilsson M et al. Study protocol for the oligometastatic esophagogastric cancer (OMEC) project: A multidisciplinary European consensus project on the definition and treatment for oligometastatic esophagogastric cancer. Eur J Surg Oncol, 2023, 49(1): 21-28.
9.	Kroese TE, van Laarhoven HWM, Nilsson M et al. Definition of oligometastatic esophagogastric cancer and impact of local oligometastasis-directed treatment: A systematic review and meta-analysis. Eur J Cancer, 2022, 166: 254-269.
10.	Kroese TE, van Hillegersberg R, Schoppmann S et al. Definitions and treatment of oligometastatic oesophagogastric cancer according to multidisciplinary tumour boards in Europe. Eur J Cancer, 2022, 164: 18-29.
11.	Kroese TE, van Laarhoven HWM, Schoppman SF et al. Definition, diagnosis and treatment of oligometastatic oesophagogastric cancer: A Delphi consensus study in Europe. Eur J Cancer, 2023, 185: 28-39.
12.	Matsumoto C, Iwatsuki M, Morinaga T et al. The relationship between the treatment course and prognosis of oligometastasis after esophageal squamous cell carcinoma resection. Surg Today, 2024, 54(8): 927-934.
13.	Rice TW, Ishwaran H, Hofstetter WL et al. Recommendations for pathologic staging (pTNM) of cancer of the esophagus and esophagogastric junction for the 8th edition AJCC/UICC staging manuals. Dis Esophagus, 2016, 29(8): 897-905.
14.	Mine S, Tanaka K, Kawachi H et al. Japanese classification of esophageal cancer, 12th edition: Part I. Esophagus, 2024, 21(3): 179-215.
15.	Liu Q, Chen J, Lin Y et al. Systemic therapy with or without local intervention for oligometastatic oesophageal squamous cell carcinoma (ESO-Shanghai 13): An open-label, randomised, phase 2 trial. Lancet Gastroenterol Hepatol, 2024, 9(1): 45-55.
16.	Ichikawa H, Kosugi S, Nakagawa S et al. Operative treatment for metachronous pulmonary metastasis from esophageal carcinoma. Surg, 2011, 149(2): 164-170.
17.	Shiono S, Kawamura M, Sato T et al. Disease-free interval length correlates to prognosis of patients who underwent metastasectomy for esophageal lung metastases. J Thorac Oncol, 2008, 3(9): 1046-1049.
18.	Hamai Y, Hihara J, Emi M et al. Treatment outcomes and prognostic factors after recurrence of esophageal squamous cell carcinoma. World J Surg, 2018, 42(7): 2190-2198.
19.	Ji J, Liu Y, Bao Y et al. Effects of local treatment in combination with systemic therapy for advanced esophageal cancer: a systematic review and meta-analysis. Adv Radiat Oncol, 2024, 9(7): 101522.
20.	Liu Q, Zhu Z, Chen Y et al. Phase 2 study of stereotactic body radiation therapy for patients with oligometastatic esophageal squamous cell carcinoma. Int J Radiat Oncol Biol Phys, 2020, 108(3): 707-715.
21.	Zhao W, Ke S, Cai X et al. Radiotherapy plus camrelizumab and irinotecan for oligometastatic esophageal squamous cell carcinoma patients after first-line immunotherapy plus chemotherapy failure: An open-label, single-arm, phase II trial. Radiother Oncol, 2023, 184: 109679.
22.	Fujitani K, Yang HK, Mizusawa J et al. Gastrectomy plus chemotherapy versus chemotherapy alone for advanced gastric cancer with a single non-curable factor (REGATTA): A phase 3, randomised controlled trial. Lancet Oncol, 2016, 17(3): 309-318.
23.	Al-Batran SE, Homann N, Pauligk C et al. Effect of neoadjuvant chemotherapy followed by surgical resection on survival in patients with limited metastatic gastric or gastroesophageal junction cancer: The AIO-FLOT3 Trial. JAMA Oncol, 2017, 3(9): 1237-1244.
24.	Liu C, Tsai PC, Chien LI et al. Esophagectomy in patients with esophageal squamous cell carcinoma and distant nodal metastasis. Dis Esophagus, 2024, 37(11): doae064.
25.	Igaue S, Nozaki R, Utsunomiya D et al. Significance of surgery for resectable m1 lymph node metastases without organ metastasis in esophageal carcinoma in the era of neoadjuvant treatment. Ann Surg Oncol, 2024, 31(3): 1525-1535.
26.	Hingorani M, Stubley H. Oligometastatic esophageal cancer cured by systemic therapy combined with radiotherapy to primary tumor and metastasis (metastasis-directed therapy)-small case series. Explor Target Antitumor Ther, 2024, 5(4): 921-930.
27.	Yamaguchi H, Fukumitsu N, Numajiri H et al. The Japanese nationwide cohort data of proton beam therapy for liver oligometastasis in esophagogastric cancer patients. J Radiat Res, 2023, 64(6): 926-932.
28.	Yamaguchi H, Kato T, Honda M et al. Proton Beam therapy for lung oligometastatic recurrence in patients with esophageal cancer. Cureus, 2023, 15(12): e50343.
29.	Li J, Wen Y, Xiang Z et al. Radical radiotherapy for metachronous oligometastasis after initial treatment of esophageal cancer. Radiother Oncol, 2021, 154: 201-206.
30.	Ohkura Y, Shindoh J, Ueno M et al. Clinicopathologic characteristics of oligometastases from esophageal cancer and long-term outcomes of resection. Ann Surg Oncol, 2020, 27(3): 651-659.
31.	Chen Y, Cheng X, Song H et al. Outcomes of concurrent chemoradiotherapy versus chemotherapy alone for esophageal squamous cell cancer patients presenting with oligometastases. J Thorac Dis, 2019, 11(4): 1536-1545.
32.	Duan Y, Qin W, Yang L et al. Safety and efficacy of concurrent or sequential radiotherapy plus (pd-1) inhibitors in oligometastatic esophageal cancer. Cancer Manag Res, 2023, 15: 55-65.
33.	Qin J, Xue L, Hao A et al. Neoadjuvant chemotherapy with or without camrelizumab in resectable esophageal squamous cell carcinoma: The randomized phase 3 ESCORT-NEO/NCCES01 trial. Nat Med, 2024, 30(9): 2549-2557.

1. Qi L, Sun M, Liu W et al. Global esophageal cancer epidemiology in 2022 and predictions for 2050: A comprehensive analysis and projections based on GLOBOCAN data. Chin Med J (Engl), 2024, 137(24): 3108-3116.
2. Yang H, Wang F, Hallemeier CL et al. Oesophageal cancer. Lancet, 2024, 404(10466): 1991-2005.
3. Kroese TE, Christ SM, van Rossum PSN et al. Incidence and survival of patients with oligometastatic esophagogastric cancer: A multicenter cohort study. Radiother Oncol, 2022, 173 269-276.
4. Elliott JA, Markar SR, Klevebro F et al. An international multicenter study exploring whether surveillance after esophageal cancer surgery impacts oncological and quality of life outcomes (ENSURE). Ann Surg, 2023, 277(5): e1035-e1044.
5. Hellman S, Weichselbaum RR. Oligometastases. J Clin Oncol, 1995, 13(1): 8-10.
6. van Hootegem SJM, de Pasqual CA, Giacopuzzi S et al. Outcomes after surgical treatment of oesophagogastric cancer with synchronous liver metastases: A multicentre retrospective cohort study. Cancers (Basel), 2024, 16(4): 797.
7. Kroese TE, Bronzwaer S, van Rossum PSN et al. European clinical practice guidelines for the definition, diagnosis, and treatment of oligometastatic esophagogastric cancer (OMEC-4). Eur J Cancer, 2024, 204: 114062.
8. Kroese TE, van Rossum PSN, Nilsson M et al. Study protocol for the oligometastatic esophagogastric cancer (OMEC) project: A multidisciplinary European consensus project on the definition and treatment for oligometastatic esophagogastric cancer. Eur J Surg Oncol, 2023, 49(1): 21-28.
9. Kroese TE, van Laarhoven HWM, Nilsson M et al. Definition of oligometastatic esophagogastric cancer and impact of local oligometastasis-directed treatment: A systematic review and meta-analysis. Eur J Cancer, 2022, 166: 254-269.
10. Kroese TE, van Hillegersberg R, Schoppmann S et al. Definitions and treatment of oligometastatic oesophagogastric cancer according to multidisciplinary tumour boards in Europe. Eur J Cancer, 2022, 164: 18-29.
11. Kroese TE, van Laarhoven HWM, Schoppman SF et al. Definition, diagnosis and treatment of oligometastatic oesophagogastric cancer: A Delphi consensus study in Europe. Eur J Cancer, 2023, 185: 28-39.
12. Matsumoto C, Iwatsuki M, Morinaga T et al. The relationship between the treatment course and prognosis of oligometastasis after esophageal squamous cell carcinoma resection. Surg Today, 2024, 54(8): 927-934.
13. Rice TW, Ishwaran H, Hofstetter WL et al. Recommendations for pathologic staging (pTNM) of cancer of the esophagus and esophagogastric junction for the 8th edition AJCC/UICC staging manuals. Dis Esophagus, 2016, 29(8): 897-905.
14. Mine S, Tanaka K, Kawachi H et al. Japanese classification of esophageal cancer, 12th edition: Part I. Esophagus, 2024, 21(3): 179-215.
15. Liu Q, Chen J, Lin Y et al. Systemic therapy with or without local intervention for oligometastatic oesophageal squamous cell carcinoma (ESO-Shanghai 13): An open-label, randomised, phase 2 trial. Lancet Gastroenterol Hepatol, 2024, 9(1): 45-55.
16. Ichikawa H, Kosugi S, Nakagawa S et al. Operative treatment for metachronous pulmonary metastasis from esophageal carcinoma. Surg, 2011, 149(2): 164-170.
17. Shiono S, Kawamura M, Sato T et al. Disease-free interval length correlates to prognosis of patients who underwent metastasectomy for esophageal lung metastases. J Thorac Oncol, 2008, 3(9): 1046-1049.
18. Hamai Y, Hihara J, Emi M et al. Treatment outcomes and prognostic factors after recurrence of esophageal squamous cell carcinoma. World J Surg, 2018, 42(7): 2190-2198.
19. Ji J, Liu Y, Bao Y et al. Effects of local treatment in combination with systemic therapy for advanced esophageal cancer: a systematic review and meta-analysis. Adv Radiat Oncol, 2024, 9(7): 101522.
20. Liu Q, Zhu Z, Chen Y et al. Phase 2 study of stereotactic body radiation therapy for patients with oligometastatic esophageal squamous cell carcinoma. Int J Radiat Oncol Biol Phys, 2020, 108(3): 707-715.
21. Zhao W, Ke S, Cai X et al. Radiotherapy plus camrelizumab and irinotecan for oligometastatic esophageal squamous cell carcinoma patients after first-line immunotherapy plus chemotherapy failure: An open-label, single-arm, phase II trial. Radiother Oncol, 2023, 184: 109679.
22. Fujitani K, Yang HK, Mizusawa J et al. Gastrectomy plus chemotherapy versus chemotherapy alone for advanced gastric cancer with a single non-curable factor (REGATTA): A phase 3, randomised controlled trial. Lancet Oncol, 2016, 17(3): 309-318.
23. Al-Batran SE, Homann N, Pauligk C et al. Effect of neoadjuvant chemotherapy followed by surgical resection on survival in patients with limited metastatic gastric or gastroesophageal junction cancer: The AIO-FLOT3 Trial. JAMA Oncol, 2017, 3(9): 1237-1244.
24. Liu C, Tsai PC, Chien LI et al. Esophagectomy in patients with esophageal squamous cell carcinoma and distant nodal metastasis. Dis Esophagus, 2024, 37(11): doae064.
25. Igaue S, Nozaki R, Utsunomiya D et al. Significance of surgery for resectable m1 lymph node metastases without organ metastasis in esophageal carcinoma in the era of neoadjuvant treatment. Ann Surg Oncol, 2024, 31(3): 1525-1535.
26. Hingorani M, Stubley H. Oligometastatic esophageal cancer cured by systemic therapy combined with radiotherapy to primary tumor and metastasis (metastasis-directed therapy)-small case series. Explor Target Antitumor Ther, 2024, 5(4): 921-930.
27. Yamaguchi H, Fukumitsu N, Numajiri H et al. The Japanese nationwide cohort data of proton beam therapy for liver oligometastasis in esophagogastric cancer patients. J Radiat Res, 2023, 64(6): 926-932.
28. Yamaguchi H, Kato T, Honda M et al. Proton Beam therapy for lung oligometastatic recurrence in patients with esophageal cancer. Cureus, 2023, 15(12): e50343.
29. Li J, Wen Y, Xiang Z et al. Radical radiotherapy for metachronous oligometastasis after initial treatment of esophageal cancer. Radiother Oncol, 2021, 154: 201-206.
30. Ohkura Y, Shindoh J, Ueno M et al. Clinicopathologic characteristics of oligometastases from esophageal cancer and long-term outcomes of resection. Ann Surg Oncol, 2020, 27(3): 651-659.
31. Chen Y, Cheng X, Song H et al. Outcomes of concurrent chemoradiotherapy versus chemotherapy alone for esophageal squamous cell cancer patients presenting with oligometastases. J Thorac Dis, 2019, 11(4): 1536-1545.
32. Duan Y, Qin W, Yang L et al. Safety and efficacy of concurrent or sequential radiotherapy plus (pd-1) inhibitors in oligometastatic esophageal cancer. Cancer Manag Res, 2023, 15: 55-65.
33. Qin J, Xue L, Hao A et al. Neoadjuvant chemotherapy with or without camrelizumab in resectable esophageal squamous cell carcinoma: The randomized phase 3 ESCORT-NEO/NCCES01 trial. Nat Med, 2024, 30(9): 2549-2557.

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