A Review of Metastasis-Directed Therapy in Oligometastatic Gastrointestinal Cancers
Main Article Content
Abstract
This review provides an overview of the current understanding regarding the role of metastasis-directed therapy (MDT) in patients with oligometastatic gastrointestinal cancers. A review of clinical data was conducted to describe patient outcomes associated with the use of local therapy alone or in combination with systemic therapy to gastrointestinal oligometastases. Included cancers were esophagus, liver, pancreas, colorectal, and anal canal. Radiotherapy was the most common MDT employed across studies although surgical resection and transarterial ablation were also used.
Present data suggest that local therapies should be considered in the treatment of oligometastatic gastrointestinal malignancies for appropriate patients. MDT may be associated with improved overall survival, progression-free survival, particularly for esophageal and colorectal cancers. Enhanced disease control has also been seen for hepatocellular and pancreatic cancers with limited adverse events.
The data highlight the increasing impact of locoregional management of oligometastatic disease through multiple treatment modalities. Targeted approaches involving radiotherapy and surgical resection can enhance clinical response to systemic therapy and improve patient outcomes. Future randomized clinical trials will further establish the role of MDT in patients with oligometastatic GI cancers.
Keywords:
Metastasis-Directed Therapy (MDT), Oligometastatic Gastrointestinal Cancers, Local Therapy, Radiotherapy, Surgical Resection, Systemic Therapy, Patient Outcomes
Article Details
How to Cite
DIPKO, Kawika et al.
A Review of Metastasis-Directed Therapy in Oligometastatic Gastrointestinal Cancers.
Medical Research Archives, [S.l.], v. 12, n. 7, july 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5629>. Date accessed: 21 dec. 2024.
doi: https://doi.org/10.18103/mra.v12i7.5629.
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. Cancer statistics, 2023 - Siegel - 2023 - CA: A Cancer Journal for Clinicians - Wiley Online Library. Accessed April 24, 2024. https://acsjournals.onlinelibrary.wiley.com/doi/10.3322/caac.21763
2. SEER*Explorer Application. National Cancer Institute: Surveillance, Epidemiology, and End Results Program. Published April 17, 2024. Accessed April 24, 2024. https://seer.cancer.gov/statistics-network/explorer/application.html?site=18&data_type=1&graph_type=4&compareBy=sex&chk_sex_1=1&chk_sex_3=3&chk_sex_2=2&race=1&age_range=1&advopt_precision=1&advopt_show_count=on&hdn_view=0
3. Siegel RL, Wagle NS, Cercek A, Smith RA, Jemal A. Colorectal cancer statistics, 2023. CA: A Cancer Journal for Clinicians. 2023;73(3):233-254. doi:10.3 322/caac.21772
4. Correa RJM, Salama JK, Milano MT, Palma DA. Stereotactic Body Radiotherapy for Oligometastasis: Opportunities for Biology to Guide Clinical Management. The Cancer Journal. 2016;22(4):247. doi:10.1097/PPO.0000000000000202
5. Guckenberger M, Lievens Y, Bouma AB, et al. Characterisation and classification of oligometastatic disease: a European Society for Radiotherapy and Oncology and European Organisation for Research and Treatment of Cancer consensus recommendation. The Lancet Oncology. 2020;21(1):e18-e28. doi:10.1016/S1470 -2045(19)30718-1
6. Lievens Y, Guckenberger M, Gomez D, et al. Defining oligometastatic disease from a radiation oncology perspective: An ESTRO-ASTRO consensus document. Radiother Oncol. 2020;148: 157-166. doi:10.1016/j.radonc.2020.04.003
7. Palma DA, Olson R, Harrow S, et al. Stereotactic ablative radiotherapy versus standard of care palliative treatment in patients with oligometastatic cancers (SABR-COMET): a randomised, phase 2, open-label trial. The Lancet. 2019;393(10185):2051 -2058. doi:10.1016/S0140-6736(18)32487-5
8. Tsai CJ, Yang JT, Guttmann DM, et al. Final Analysis of Consolidative Use of Radiotherapy to Block (CURB) Oligoprogression Trial - A Randomized Study of Stereotactic Body Radiotherapy for Oligoprogressive Metastatic Lung and Breast Cancers. International Journal of Radiation Oncology*Biology*Physics. 2022;114(5): 1061. doi:10.1016/j.ijrobp.2022.09.008
9. Deek MP, Taparra K, Phillips R, et al. Metastasis-directed Therapy Prolongs Efficacy of Systemic Therapy and Improves Clinical Outcomes in Oligoprogressive Castration-resistant Prostate Cancer. European Urology Oncology. 2021;4(3):44 7-455. doi:10.1016/j.euo.2020.05.004
10. Stephen Paget. The Distribution of Secondary Growths in Cancer of the Breast. The Lancet. 1889;1:571-573.
11. Fisher B. Laboratory and Clinical Research in Breast Cancer—A Personal Adventure: The David A. Karnofsky Memorial Lecture1. Cancer Research. 1980;40(11):3863-3874.
12. Weichselbaum RR, Hellman S. Oligometastases revisited. Nat Rev Clin Oncol. 2011;8(6):378-382. doi:10.1038/nrclinonc.2011.44
13. Norton L, Massagué J. Is cancer a disease of self-seeding? Nat Med. 2006;12(8):875-878. doi:10.1038/nm0806-875
14. Kim MY, Oskarsson T, Acharyya S, et al. Tumor Self-Seeding by Circulating Cancer Cells. Cell. 2009;139(7):1315-1326. doi:10.1016/j.cell.2009.11.025
15. Khodarev NN, Pitroda SP, Weichselbaum RR. microRNAs and oligometastasis. Aging (Albany NY). 2015;7(3):146-147.
16. Lussier YA, Xing HR, Salama JK, et al. MicroRNA Expression Characterizes Oligometastasis(es). PLOS ONE. 2011;6(12):e28650. doi:10.1371/journ al.pone.0028650
17. Uppal A, Ferguson MK, Posner MC, Hellman S, Khodarev NN, Weichselbaum RR. Towards a molecular basis of oligometastatic disease: potential role of micro-RNAs. Clin Exp Metastasis. 2014;31(6):735-748. doi:10.1007/s10585-014-9664-3
18. Statistics for Esophageal Cancer | Esophageal Cancer Stats | American Cancer Society. Accessed April 22, 2024. https://www.cancer.org/cancer/types/esophagus-cancer/about/key-statistics.html
19. 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. The Lancet. 2021;398(10302):759-771. doi:10.101 6/S0140-6736(21)01234-4
20. Obermannová R, Alsina M, Cervantes A, et al. Oesophageal cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up☆. Annals of Oncology. 2022;33(10):992-1004. doi:10.1016/j.annonc.2022.07.003
21. 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. doi:10.21037/jtd.2019.03.10
22. Li J, Wen Y, Xiang Z, et al. Radical radiotherapy for metachronous oligometastasis after initial treatment of esophageal cancer. Radiotherapy and Oncology. 2021;154:201-206. doi:10.1016/j.radon c.2020.09.042
23. Liu Q, Zhu Z, Chen Y, et al. Phase 2 Study of Stereotactic Body Radiation Therapy for Patients with Oligometastatic Esophageal Squamous Cell Carcinoma. International Journal of Radiation Oncology*Biology*Physics. 2020;108(3):707-715. doi:10.1016/j.ijrobp.2020.05.003
24. 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. doi:10.1016/S2468-1253(23)00316-3
25. 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. JCO. 2021;39(18):1995-2004. doi:10.1200/JCO.2 0.03614
26. Nataliya Uboha. Trial Spotlight: Nataliya Uboha on the EA2183 Trial for Esophageal and Gastric Adenocarcinoma. News from the ECOG-ACRIN Cancer Research Group. Published February 24, 2022. Accessed April 22, 2024. https://blog-ecog-acrin.org/trial-spotlight-nataliya-uboha-on-the-ea2183-trial-for-esophageal-and-gastric-adenocarcinoma/
27. Gordan JD, Kennedy EB, Abou-Alfa GK, et al. Systemic Therapy for Advanced Hepatocellular Carcinoma: ASCO Guideline Update. JCO. Published online March 19, 2024:JCO.23.02745. doi:10.1200/JCO.23.02745
28. Finn Richard S., Qin Shukui, Ikeda Masafumi, et al. Atezolizumab plus Bevacizumab in Unresectable Hepatocellular Carcinoma. New England Journal of Medicine. 2020;382(20):1894-1905. doi:10.1056/NEJMoa1915745
29. Sangro B, Chan S, Kelley R, et al. SO-15 Four-year overall survival update from the phase 3 HIMALAYA study of tremelimumab plus durvalumab in unresectable hepatocellular carcinoma. Annals of Oncology. 2023;34:S168. doi:10.1016/j.annonc.2023.04.487
30. Qin S, Kudo M, Meyer T, et al. Tislelizumab vs Sorafenib as First-Line Treatment for Unresectable Hepatocellular Carcinoma: A Phase 3 Randomized Clinical Trial. JAMA Oncology. 2023;9(12):1651-1659. doi:10.1001/jamaoncol.2023.4003
31. Kim K, Kim TH, Kim TH, Seong J. Efficacy of Local Therapy for Oligometastatic Hepatocellular Carcinoma: A Propensity Score Matched Analysis. Journal of Hepatocellular Carcinoma. Published online February 11, 2021. Accessed April 22, 2024. https://www.tandfonline.com/doi/abs/10.2147/JHC.S290197
32. Jo IY, Park HC, Kim ES, et al. Stereotactic ablative radiotherapy for pulmonary oligometastases from primary hepatocellular carcinoma: a multicenter and retrospective analysis (KROG 17-08). Japanese Journal of Clinical Oncology. 2022;52(6):616-622. doi:10.1093/jjco/hyac028
33. Kim S, Lee J, Rim CH. Local Treatment of Hepatocellular Carcinoma with Oligometastases: A Systematic Review and Meta-Analysis. Cancers. 2023;15(13):3467. doi:10.3390/cancers15133467
34. Gerum S, Heinz C, Belka C, et al. Stereotactic body radiation therapy (SBRT) in patients with hepatocellular carcinoma and oligometastatic liver disease. Radiat Oncol. 2018;13(1):100. doi:10.11 86/s13014-018-1048-4
35. Kim TH, Nam TK, Yoon SM, Kim TH, Choi YM, Seong J. Stereotactic Ablative Radiotherapy for Oligometastatic Hepatocellular Carcinoma: A Multi-Institutional Retrospective Study (KROG 20-04). Cancers. 2022;14(23):5848. doi:10.3390/cance rs14235848
36. Choi SH, Lee B min, Kim J, Kim DY, Seong J. Efficacy of Stereotactic Ablative Radiotherapy in Patients with Oligometastatic Hepatocellular Carcinoma: A Phase II Study. Journal of Hepatology. 2024;0(0). doi:10.1016/j.jhep.2024.03.003
37. Chen YX, Yang P, Du SS, et al. Stereotactic body radiotherapy combined with sintilimab in patients with recurrent or oligometastatic hepatocellular carcinoma: A phase II clinical trial. World J Gastroenterol. 2023;29(24):3871-3882. doi:10.3748/wjg.v29.i24.3871
38. Stereotactic Ablative Radiotherapy for Oligometastatic Hepatocellular Carcinoma | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT05173610
39. Phase 2 Study of SBRT Plus Tislelizumab and Regorafenib in Unresectable or Oligometastatic HCC | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT05917431
40. Pancreatic Cancer Treatment (PDQ®) - NCI. Published February 2, 2024. Accessed April 22, 2024. https://www.cancer.gov/types/pancreatic/hp/pancreatic-treatment-pdq
41. Jiang Y, Sohal DPS. Pancreatic Adenocarcinoma Management. JCO Oncol Pract. 2023;19(1):19-32. doi:10.1200/OP.22.00328
42. Thierry Conroy, Francoise Desseigne, Marc Ychou, et al. FOLFIRINOX versus Gemcitabine for Metastatic Pancreatic Cancer | New England Journal of Medicine. The New England Journal of Medicine. 2011;364(19):1817-1825. doi:10.1056/N EJMoa1011923
43. Turpin A, Neuzillet C, Colle E, et al. Therapeutic advances in metastatic pancreatic cancer: a focus on targeted therapies. Ther Adv Med Oncol. 2022;14:17588359221118019. doi:10. 1177/17588359221118019
44. Yang J, Zhang J, Lui W, et al. Patients with hepatic oligometastatic pancreatic body/tail ductal adenocarcinoma may benefit from synchronous resection. HPB. 2020;22(1):91-101. doi:10.1016/j.h pb.2019.05.015
45. Breton C, Meyer A, Malka D, et al. Local treatment of pancreatic cancer metastases: A multicenter French study of the AGEO group. Clinics and Research in Hepatology and Gastroenterology. 2021;45(6):101607. doi:10.1016 /j.clinre.2020.101607
46. Ludmir EB, Sherry AD, Fellman BM, et al. Addition of metastasis-directed therapy to standard-of-care systemic therapy for oligometastatic pancreatic ductal adenocarcinoma (EXTEND): Results of a multicenter, randomized phase II trial. JCO. 2024;42(3_suppl):603-603. doi:10.1200/JCO.2024.42.3_suppl.603
47. Simultaneous Resection of Pancreatic Cancer and Liver Oligometastasis After Induction Chemotherapy | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT03398291?tab=table
48. Chemotherapy and Surgical Resection in Patients With Hepatic Oligometastatic Adenocarcinoma of the Pancreas | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT04617457?tab=results
49. Surgery and Thermal Hepatic Ablation Combined With Chemotherapy in Hepatic Oligometastatic Pancreatic Cancer (HOPE-1). Accessed April 24, 2024. https://classic.clinicaltrials.gov/ct2/show/study/NCT05611359
50. Surgery for Liver Metastases From PDAC | ClinicalTrials.gov. Accessed April 24, 2024. https://clinicaltrials.gov/study/NCT05271110
51. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer Statistics, 2021. CA A Cancer J Clin. 2021;71(1):7-33. doi:10.3322/caac.21654
52. Väyrynen V, Wirta EV, Seppälä T, et al. Incidence and management of patients with colorectal cancer and synchronous and metachronous colorectal metastases: a population-based study. BJS Open. 2020;4(4):685-692. doi:10.1002/bjs5.50299
53. Welch JP, Donaldson GA. The clinical correlation of an autopsy study of recurrent colorectal cancer. Ann Surg. 1979;189(4):496-502. doi:10.1097/00000658-197904000-00027
54. Ikoma N, You YN, Bednarski BK, et al. Impact of Recurrence and Salvage Surgery on Survival After Multidisciplinary Treatment of Rectal Cancer. JCO. 2017;35(23):2631-2638. doi:10.1200/JCO.20 16.72.1464
55. Ottaiano A, Caraglia M, Di Mauro A, et al. Evolution of Mutational Landscape and Tumor Immune-Microenvironment in Liver Oligo-Metastatic Colorectal Cancer. Cancers. 2020;12(10 ):3073. doi:10.3390/cancers12103073
56. Ottaiano A, Circelli L, Lombardi A, et al. Genetic trajectory and immune microenvironment of lung-specific oligometastatic colorectal cancer. Cell Death Dis. 2020;11(4):1-11. doi:10.1038/s414 19-020-2480-6
57. Pitroda SP, Khodarev NN, Huang L, et al. Integrated molecular subtyping defines a curable oligometastatic state in colorectal liver metastasis. Nat Commun. 2018;9(1):1793. doi:10.1038/s41467 -018-04278-6
58. Morris VK, Kennedy EB, Baxter NN, et al. Treatment of Metastatic Colorectal Cancer: ASCO Guideline. J Clin Oncol. 2023;41(3):678-700. doi:10.1200/JCO.22.01690
59. Mohammad WM, Balaa FK. Surgical Management of Colorectal Liver Metastases. Clin Colon Rectal Surg. 2009;22(4):225-232. doi:10.105 5/s-0029-1242462
60. Benjamin Goodman, Edward Mannina, Sandra Althouse, Mary Maluccio, Higinia Cardenes. Long-term safety and efficacy of stereotactic body radiation therapy for hepatic oligometastases - ScienceDirect. Practical Radiation Oncology. 2016; 6(2):86-95.doi:doi.org/10.1016/j.prro.2015.10.011
61. Kobiela J, Spychalski P, Marvaso G, et al. Ablative stereotactic radiotherapy for oligometastatic colorectal cancer: Systematic review. Critical Reviews in Oncology/Hematology. 2018;129:91-101. doi:10.1016/j.critrevonc.2018.06.005
62. Jung J, Song SY, Kim JH, et al. Clinical efficacy of stereotactic ablative radiotherapy for lung metastases arising from colorectal cancer. Radiation Oncology. 2015;10(1):238. doi:10.1186/ s13014-015-0546-x
63. Kinj R, Bondiau PY, François E, et al. Radiosensitivity of Colon and Rectal Lung Oligometastasis Treated With Stereotactic Ablative Radiotherapy. Clin Colorectal Cancer. 2017;16(3):e211-e220. doi:10.1016/j.clcc.2016.08.003
64. Jingu K, Matsuo Y, Onishi H, et al. Dose Escalation Improves Outcome in Stereotactic Body Radiotherapy for Pulmonary Oligometastases from Colorectal Cancer. Anticancer Res. 2017;37(5):270 9-2713. doi:10.21873/anticanres.11621
65. Hong TS, Wo JY, Borger DR, et al. Phase II Study of Proton-Based Stereotactic Body Radiation Therapy for Liver Metastases: Importance of Tumor Genotype. JNCI: Journal of the National Cancer Institute. 2017;109(9):djx031. doi:10.1093/jnci/djx031
66. Vogl TJ, Marko C, Langenbach MC, et al. Transarterial chemoembolization of colorectal cancer liver metastasis: improved tumor response by DSM-TACE versus conventional TACE, a prospective, randomized, single-center trial. Eur Radiol. 2021;31(4):2242-2251. doi:10.1007/s00330 -020-07253-2
67. Fiorentini G, Aliberti C, Tilli M, et al. Intra-arterial infusion of irinotecan-loaded drug-eluting beads (DEBIRI) versus intravenous therapy (FOLFIRI) for hepatic metastases from colorectal cancer: final results of a phase III study. Anticancer Res. 2012;32(4):1387-1395.
68. Osterlund P, Salminen T, Soveri LM, et al. Repeated centralized multidisciplinary team assessment of resectability, clinical behavior, and outcomes in 1086 Finnish metastatic colorectal cancer patients (RAXO): A nationwide prospective intervention study. The Lancet Regional Health - Europe. 2021;3:100049. doi:10.1016/j.lanepe.202 1.100049
69. Ruers T, Punt C, Van Coevorden F, et al. Radiofrequency ablation combined with systemic treatment versus systemic treatment alone in patients with non-resectable colorectal liver metastases: a randomized EORTC Intergroup phase II study (EORTC 40004). Annals of Oncology. 2012;23(10):2619-2626. doi:10.1093/annonc/mds053
70. Ruers T, Van Coevorden F, Punt CJA, et al. Local Treatment of Unresectable Colorectal Liver Metastases: Results of a Randomized Phase II Trial. JNCI: Journal of the National Cancer Institute. 2017;109(9):djx015. doi:10.1093/jnci/djx015
71. Hitchcock KE, Miller ED, Shi Q, et al. Alliance for Clinical Trials in Oncology (Alliance) trial A022101/NRG-GI009: A pragmatic randomized phase III trial evaluating total ablative therapy for patients with limited metastatic colorectal cancer: evaluating radiation, ablation, and surgery (ERASur). Published online December 23, 2023. doi:10.21203/rs.3.rs-3773522/v1
72. Anal Cancer Treatment (PDQ®) - NCI. Published January 26, 2024. Accessed April 24, 2024. https://www.cancer.gov/types/anal/hp/anal-treatment-pdq
73. Rao S, Sclafani F, Eng C, et al. International Rare Cancers Initiative Multicenter Randomized Phase II Trial of Cisplatin and Fluorouracil Versus Carboplatin and Paclitaxel in Advanced Anal Cancer: InterAAct. JCO. 2020;38(22):2510-2518. doi:10.1200/JCO.19.03266
74. Sclafani F, Hesselberg G, Thompson SR, et al. Multimodality treatment of oligometastatic anal squamous cell carcinoma: A case series and literature review. Journal of Surgical Oncology. 2019;119(4):489-496. doi:10.1002/jso.25320
75. Eng C, Chang GJ, You YN, et al. The role of systemic chemotherapy and multidisciplinary management in improving the overall survival of patients with metastatic squamous cell carcinoma of the anal canal. Oncotarget. 2014;5(22):11133-11142. doi:10.18632/oncotarget.2563
76. Chakrani Z, Hristidis V, Reyngold M, et al. Definitive Intent Locoregional IMRT In Oligometastatic Anal Squamous Cell Carcinoma. International Journal of Radiation Oncology, Biology, Physics. 2020;108(3):e615. doi:10.1016/j.ij robp.2020.07.1866
2. SEER*Explorer Application. National Cancer Institute: Surveillance, Epidemiology, and End Results Program. Published April 17, 2024. Accessed April 24, 2024. https://seer.cancer.gov/statistics-network/explorer/application.html?site=18&data_type=1&graph_type=4&compareBy=sex&chk_sex_1=1&chk_sex_3=3&chk_sex_2=2&race=1&age_range=1&advopt_precision=1&advopt_show_count=on&hdn_view=0
3. Siegel RL, Wagle NS, Cercek A, Smith RA, Jemal A. Colorectal cancer statistics, 2023. CA: A Cancer Journal for Clinicians. 2023;73(3):233-254. doi:10.3 322/caac.21772
4. Correa RJM, Salama JK, Milano MT, Palma DA. Stereotactic Body Radiotherapy for Oligometastasis: Opportunities for Biology to Guide Clinical Management. The Cancer Journal. 2016;22(4):247. doi:10.1097/PPO.0000000000000202
5. Guckenberger M, Lievens Y, Bouma AB, et al. Characterisation and classification of oligometastatic disease: a European Society for Radiotherapy and Oncology and European Organisation for Research and Treatment of Cancer consensus recommendation. The Lancet Oncology. 2020;21(1):e18-e28. doi:10.1016/S1470 -2045(19)30718-1
6. Lievens Y, Guckenberger M, Gomez D, et al. Defining oligometastatic disease from a radiation oncology perspective: An ESTRO-ASTRO consensus document. Radiother Oncol. 2020;148: 157-166. doi:10.1016/j.radonc.2020.04.003
7. Palma DA, Olson R, Harrow S, et al. Stereotactic ablative radiotherapy versus standard of care palliative treatment in patients with oligometastatic cancers (SABR-COMET): a randomised, phase 2, open-label trial. The Lancet. 2019;393(10185):2051 -2058. doi:10.1016/S0140-6736(18)32487-5
8. Tsai CJ, Yang JT, Guttmann DM, et al. Final Analysis of Consolidative Use of Radiotherapy to Block (CURB) Oligoprogression Trial - A Randomized Study of Stereotactic Body Radiotherapy for Oligoprogressive Metastatic Lung and Breast Cancers. International Journal of Radiation Oncology*Biology*Physics. 2022;114(5): 1061. doi:10.1016/j.ijrobp.2022.09.008
9. Deek MP, Taparra K, Phillips R, et al. Metastasis-directed Therapy Prolongs Efficacy of Systemic Therapy and Improves Clinical Outcomes in Oligoprogressive Castration-resistant Prostate Cancer. European Urology Oncology. 2021;4(3):44 7-455. doi:10.1016/j.euo.2020.05.004
10. Stephen Paget. The Distribution of Secondary Growths in Cancer of the Breast. The Lancet. 1889;1:571-573.
11. Fisher B. Laboratory and Clinical Research in Breast Cancer—A Personal Adventure: The David A. Karnofsky Memorial Lecture1. Cancer Research. 1980;40(11):3863-3874.
12. Weichselbaum RR, Hellman S. Oligometastases revisited. Nat Rev Clin Oncol. 2011;8(6):378-382. doi:10.1038/nrclinonc.2011.44
13. Norton L, Massagué J. Is cancer a disease of self-seeding? Nat Med. 2006;12(8):875-878. doi:10.1038/nm0806-875
14. Kim MY, Oskarsson T, Acharyya S, et al. Tumor Self-Seeding by Circulating Cancer Cells. Cell. 2009;139(7):1315-1326. doi:10.1016/j.cell.2009.11.025
15. Khodarev NN, Pitroda SP, Weichselbaum RR. microRNAs and oligometastasis. Aging (Albany NY). 2015;7(3):146-147.
16. Lussier YA, Xing HR, Salama JK, et al. MicroRNA Expression Characterizes Oligometastasis(es). PLOS ONE. 2011;6(12):e28650. doi:10.1371/journ al.pone.0028650
17. Uppal A, Ferguson MK, Posner MC, Hellman S, Khodarev NN, Weichselbaum RR. Towards a molecular basis of oligometastatic disease: potential role of micro-RNAs. Clin Exp Metastasis. 2014;31(6):735-748. doi:10.1007/s10585-014-9664-3
18. Statistics for Esophageal Cancer | Esophageal Cancer Stats | American Cancer Society. Accessed April 22, 2024. https://www.cancer.org/cancer/types/esophagus-cancer/about/key-statistics.html
19. 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. The Lancet. 2021;398(10302):759-771. doi:10.101 6/S0140-6736(21)01234-4
20. Obermannová R, Alsina M, Cervantes A, et al. Oesophageal cancer: ESMO Clinical Practice Guideline for diagnosis, treatment and follow-up☆. Annals of Oncology. 2022;33(10):992-1004. doi:10.1016/j.annonc.2022.07.003
21. 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. doi:10.21037/jtd.2019.03.10
22. Li J, Wen Y, Xiang Z, et al. Radical radiotherapy for metachronous oligometastasis after initial treatment of esophageal cancer. Radiotherapy and Oncology. 2021;154:201-206. doi:10.1016/j.radon c.2020.09.042
23. Liu Q, Zhu Z, Chen Y, et al. Phase 2 Study of Stereotactic Body Radiation Therapy for Patients with Oligometastatic Esophageal Squamous Cell Carcinoma. International Journal of Radiation Oncology*Biology*Physics. 2020;108(3):707-715. doi:10.1016/j.ijrobp.2020.05.003
24. 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. doi:10.1016/S2468-1253(23)00316-3
25. 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. JCO. 2021;39(18):1995-2004. doi:10.1200/JCO.2 0.03614
26. Nataliya Uboha. Trial Spotlight: Nataliya Uboha on the EA2183 Trial for Esophageal and Gastric Adenocarcinoma. News from the ECOG-ACRIN Cancer Research Group. Published February 24, 2022. Accessed April 22, 2024. https://blog-ecog-acrin.org/trial-spotlight-nataliya-uboha-on-the-ea2183-trial-for-esophageal-and-gastric-adenocarcinoma/
27. Gordan JD, Kennedy EB, Abou-Alfa GK, et al. Systemic Therapy for Advanced Hepatocellular Carcinoma: ASCO Guideline Update. JCO. Published online March 19, 2024:JCO.23.02745. doi:10.1200/JCO.23.02745
28. Finn Richard S., Qin Shukui, Ikeda Masafumi, et al. Atezolizumab plus Bevacizumab in Unresectable Hepatocellular Carcinoma. New England Journal of Medicine. 2020;382(20):1894-1905. doi:10.1056/NEJMoa1915745
29. Sangro B, Chan S, Kelley R, et al. SO-15 Four-year overall survival update from the phase 3 HIMALAYA study of tremelimumab plus durvalumab in unresectable hepatocellular carcinoma. Annals of Oncology. 2023;34:S168. doi:10.1016/j.annonc.2023.04.487
30. Qin S, Kudo M, Meyer T, et al. Tislelizumab vs Sorafenib as First-Line Treatment for Unresectable Hepatocellular Carcinoma: A Phase 3 Randomized Clinical Trial. JAMA Oncology. 2023;9(12):1651-1659. doi:10.1001/jamaoncol.2023.4003
31. Kim K, Kim TH, Kim TH, Seong J. Efficacy of Local Therapy for Oligometastatic Hepatocellular Carcinoma: A Propensity Score Matched Analysis. Journal of Hepatocellular Carcinoma. Published online February 11, 2021. Accessed April 22, 2024. https://www.tandfonline.com/doi/abs/10.2147/JHC.S290197
32. Jo IY, Park HC, Kim ES, et al. Stereotactic ablative radiotherapy for pulmonary oligometastases from primary hepatocellular carcinoma: a multicenter and retrospective analysis (KROG 17-08). Japanese Journal of Clinical Oncology. 2022;52(6):616-622. doi:10.1093/jjco/hyac028
33. Kim S, Lee J, Rim CH. Local Treatment of Hepatocellular Carcinoma with Oligometastases: A Systematic Review and Meta-Analysis. Cancers. 2023;15(13):3467. doi:10.3390/cancers15133467
34. Gerum S, Heinz C, Belka C, et al. Stereotactic body radiation therapy (SBRT) in patients with hepatocellular carcinoma and oligometastatic liver disease. Radiat Oncol. 2018;13(1):100. doi:10.11 86/s13014-018-1048-4
35. Kim TH, Nam TK, Yoon SM, Kim TH, Choi YM, Seong J. Stereotactic Ablative Radiotherapy for Oligometastatic Hepatocellular Carcinoma: A Multi-Institutional Retrospective Study (KROG 20-04). Cancers. 2022;14(23):5848. doi:10.3390/cance rs14235848
36. Choi SH, Lee B min, Kim J, Kim DY, Seong J. Efficacy of Stereotactic Ablative Radiotherapy in Patients with Oligometastatic Hepatocellular Carcinoma: A Phase II Study. Journal of Hepatology. 2024;0(0). doi:10.1016/j.jhep.2024.03.003
37. Chen YX, Yang P, Du SS, et al. Stereotactic body radiotherapy combined with sintilimab in patients with recurrent or oligometastatic hepatocellular carcinoma: A phase II clinical trial. World J Gastroenterol. 2023;29(24):3871-3882. doi:10.3748/wjg.v29.i24.3871
38. Stereotactic Ablative Radiotherapy for Oligometastatic Hepatocellular Carcinoma | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT05173610
39. Phase 2 Study of SBRT Plus Tislelizumab and Regorafenib in Unresectable or Oligometastatic HCC | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT05917431
40. Pancreatic Cancer Treatment (PDQ®) - NCI. Published February 2, 2024. Accessed April 22, 2024. https://www.cancer.gov/types/pancreatic/hp/pancreatic-treatment-pdq
41. Jiang Y, Sohal DPS. Pancreatic Adenocarcinoma Management. JCO Oncol Pract. 2023;19(1):19-32. doi:10.1200/OP.22.00328
42. Thierry Conroy, Francoise Desseigne, Marc Ychou, et al. FOLFIRINOX versus Gemcitabine for Metastatic Pancreatic Cancer | New England Journal of Medicine. The New England Journal of Medicine. 2011;364(19):1817-1825. doi:10.1056/N EJMoa1011923
43. Turpin A, Neuzillet C, Colle E, et al. Therapeutic advances in metastatic pancreatic cancer: a focus on targeted therapies. Ther Adv Med Oncol. 2022;14:17588359221118019. doi:10. 1177/17588359221118019
44. Yang J, Zhang J, Lui W, et al. Patients with hepatic oligometastatic pancreatic body/tail ductal adenocarcinoma may benefit from synchronous resection. HPB. 2020;22(1):91-101. doi:10.1016/j.h pb.2019.05.015
45. Breton C, Meyer A, Malka D, et al. Local treatment of pancreatic cancer metastases: A multicenter French study of the AGEO group. Clinics and Research in Hepatology and Gastroenterology. 2021;45(6):101607. doi:10.1016 /j.clinre.2020.101607
46. Ludmir EB, Sherry AD, Fellman BM, et al. Addition of metastasis-directed therapy to standard-of-care systemic therapy for oligometastatic pancreatic ductal adenocarcinoma (EXTEND): Results of a multicenter, randomized phase II trial. JCO. 2024;42(3_suppl):603-603. doi:10.1200/JCO.2024.42.3_suppl.603
47. Simultaneous Resection of Pancreatic Cancer and Liver Oligometastasis After Induction Chemotherapy | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT03398291?tab=table
48. Chemotherapy and Surgical Resection in Patients With Hepatic Oligometastatic Adenocarcinoma of the Pancreas | ClinicalTrials.gov. Accessed April 23, 2024. https://www.clinicaltrials.gov/study/NCT04617457?tab=results
49. Surgery and Thermal Hepatic Ablation Combined With Chemotherapy in Hepatic Oligometastatic Pancreatic Cancer (HOPE-1). Accessed April 24, 2024. https://classic.clinicaltrials.gov/ct2/show/study/NCT05611359
50. Surgery for Liver Metastases From PDAC | ClinicalTrials.gov. Accessed April 24, 2024. https://clinicaltrials.gov/study/NCT05271110
51. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer Statistics, 2021. CA A Cancer J Clin. 2021;71(1):7-33. doi:10.3322/caac.21654
52. Väyrynen V, Wirta EV, Seppälä T, et al. Incidence and management of patients with colorectal cancer and synchronous and metachronous colorectal metastases: a population-based study. BJS Open. 2020;4(4):685-692. doi:10.1002/bjs5.50299
53. Welch JP, Donaldson GA. The clinical correlation of an autopsy study of recurrent colorectal cancer. Ann Surg. 1979;189(4):496-502. doi:10.1097/00000658-197904000-00027
54. Ikoma N, You YN, Bednarski BK, et al. Impact of Recurrence and Salvage Surgery on Survival After Multidisciplinary Treatment of Rectal Cancer. JCO. 2017;35(23):2631-2638. doi:10.1200/JCO.20 16.72.1464
55. Ottaiano A, Caraglia M, Di Mauro A, et al. Evolution of Mutational Landscape and Tumor Immune-Microenvironment in Liver Oligo-Metastatic Colorectal Cancer. Cancers. 2020;12(10 ):3073. doi:10.3390/cancers12103073
56. Ottaiano A, Circelli L, Lombardi A, et al. Genetic trajectory and immune microenvironment of lung-specific oligometastatic colorectal cancer. Cell Death Dis. 2020;11(4):1-11. doi:10.1038/s414 19-020-2480-6
57. Pitroda SP, Khodarev NN, Huang L, et al. Integrated molecular subtyping defines a curable oligometastatic state in colorectal liver metastasis. Nat Commun. 2018;9(1):1793. doi:10.1038/s41467 -018-04278-6
58. Morris VK, Kennedy EB, Baxter NN, et al. Treatment of Metastatic Colorectal Cancer: ASCO Guideline. J Clin Oncol. 2023;41(3):678-700. doi:10.1200/JCO.22.01690
59. Mohammad WM, Balaa FK. Surgical Management of Colorectal Liver Metastases. Clin Colon Rectal Surg. 2009;22(4):225-232. doi:10.105 5/s-0029-1242462
60. Benjamin Goodman, Edward Mannina, Sandra Althouse, Mary Maluccio, Higinia Cardenes. Long-term safety and efficacy of stereotactic body radiation therapy for hepatic oligometastases - ScienceDirect. Practical Radiation Oncology. 2016; 6(2):86-95.doi:doi.org/10.1016/j.prro.2015.10.011
61. Kobiela J, Spychalski P, Marvaso G, et al. Ablative stereotactic radiotherapy for oligometastatic colorectal cancer: Systematic review. Critical Reviews in Oncology/Hematology. 2018;129:91-101. doi:10.1016/j.critrevonc.2018.06.005
62. Jung J, Song SY, Kim JH, et al. Clinical efficacy of stereotactic ablative radiotherapy for lung metastases arising from colorectal cancer. Radiation Oncology. 2015;10(1):238. doi:10.1186/ s13014-015-0546-x
63. Kinj R, Bondiau PY, François E, et al. Radiosensitivity of Colon and Rectal Lung Oligometastasis Treated With Stereotactic Ablative Radiotherapy. Clin Colorectal Cancer. 2017;16(3):e211-e220. doi:10.1016/j.clcc.2016.08.003
64. Jingu K, Matsuo Y, Onishi H, et al. Dose Escalation Improves Outcome in Stereotactic Body Radiotherapy for Pulmonary Oligometastases from Colorectal Cancer. Anticancer Res. 2017;37(5):270 9-2713. doi:10.21873/anticanres.11621
65. Hong TS, Wo JY, Borger DR, et al. Phase II Study of Proton-Based Stereotactic Body Radiation Therapy for Liver Metastases: Importance of Tumor Genotype. JNCI: Journal of the National Cancer Institute. 2017;109(9):djx031. doi:10.1093/jnci/djx031
66. Vogl TJ, Marko C, Langenbach MC, et al. Transarterial chemoembolization of colorectal cancer liver metastasis: improved tumor response by DSM-TACE versus conventional TACE, a prospective, randomized, single-center trial. Eur Radiol. 2021;31(4):2242-2251. doi:10.1007/s00330 -020-07253-2
67. Fiorentini G, Aliberti C, Tilli M, et al. Intra-arterial infusion of irinotecan-loaded drug-eluting beads (DEBIRI) versus intravenous therapy (FOLFIRI) for hepatic metastases from colorectal cancer: final results of a phase III study. Anticancer Res. 2012;32(4):1387-1395.
68. Osterlund P, Salminen T, Soveri LM, et al. Repeated centralized multidisciplinary team assessment of resectability, clinical behavior, and outcomes in 1086 Finnish metastatic colorectal cancer patients (RAXO): A nationwide prospective intervention study. The Lancet Regional Health - Europe. 2021;3:100049. doi:10.1016/j.lanepe.202 1.100049
69. Ruers T, Punt C, Van Coevorden F, et al. Radiofrequency ablation combined with systemic treatment versus systemic treatment alone in patients with non-resectable colorectal liver metastases: a randomized EORTC Intergroup phase II study (EORTC 40004). Annals of Oncology. 2012;23(10):2619-2626. doi:10.1093/annonc/mds053
70. Ruers T, Van Coevorden F, Punt CJA, et al. Local Treatment of Unresectable Colorectal Liver Metastases: Results of a Randomized Phase II Trial. JNCI: Journal of the National Cancer Institute. 2017;109(9):djx015. doi:10.1093/jnci/djx015
71. Hitchcock KE, Miller ED, Shi Q, et al. Alliance for Clinical Trials in Oncology (Alliance) trial A022101/NRG-GI009: A pragmatic randomized phase III trial evaluating total ablative therapy for patients with limited metastatic colorectal cancer: evaluating radiation, ablation, and surgery (ERASur). Published online December 23, 2023. doi:10.21203/rs.3.rs-3773522/v1
72. Anal Cancer Treatment (PDQ®) - NCI. Published January 26, 2024. Accessed April 24, 2024. https://www.cancer.gov/types/anal/hp/anal-treatment-pdq
73. Rao S, Sclafani F, Eng C, et al. International Rare Cancers Initiative Multicenter Randomized Phase II Trial of Cisplatin and Fluorouracil Versus Carboplatin and Paclitaxel in Advanced Anal Cancer: InterAAct. JCO. 2020;38(22):2510-2518. doi:10.1200/JCO.19.03266
74. Sclafani F, Hesselberg G, Thompson SR, et al. Multimodality treatment of oligometastatic anal squamous cell carcinoma: A case series and literature review. Journal of Surgical Oncology. 2019;119(4):489-496. doi:10.1002/jso.25320
75. Eng C, Chang GJ, You YN, et al. The role of systemic chemotherapy and multidisciplinary management in improving the overall survival of patients with metastatic squamous cell carcinoma of the anal canal. Oncotarget. 2014;5(22):11133-11142. doi:10.18632/oncotarget.2563
76. Chakrani Z, Hristidis V, Reyngold M, et al. Definitive Intent Locoregional IMRT In Oligometastatic Anal Squamous Cell Carcinoma. International Journal of Radiation Oncology, Biology, Physics. 2020;108(3):e615. doi:10.1016/j.ij robp.2020.07.1866