The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
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Approaches and considerations in the endoscopic treatment of T1 colorectal cancer

  • Yunho Jung (Division of Gastroenterology, Department of Medicine, Soonchunhyang University College of Medicine)
  • Received : 2023.11.11
  • Accepted : 2023.12.27
  • Published : 2024.07.01
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Abstract

The detection of early colorectal cancer (CRC) is increasing through the implementation of screening programs. This increased detection enhances the likelihood of minimally invasive surgery and significantly lowers the risk of recurrence, thereby improving patient survival and reducing mortality rates. T1 CRC, the earliest stage, is treated endoscopically in cases with a low risk of lymph node metastasis (LNM). The advantages of endoscopic treatment compared with surgery include minimal invasiveness and limited tissue disruption, which reduce morbidity and mortality, preserve bowel function to avoid colectomy, accelerate recovery, and improve cost-effectiveness. However, T1 CRC has a risk of LNM. Thus, selection of the appropriate treatment between endoscopic treatment and surgery, while avoiding overtreatment, is challenging considering the potential for complete resection, LNM, and recurrence risk.

Keywords

Acknowledgement

This work was supported by the Soonchunhyang University Research Fund.

References

  1. Shaukat A, Kaltenbach T, Dominitz JA, et al. Endoscopic recognition and management strategies for malignant colorectal polyps: recommendations of the US Multi-Society Task Force on colorectal cancer. Am J Gastroenterol 2020;115:1751-1767. 
  2. Weiser MR. AJCC 8th edition: colorectal cancer. Ann Surg Oncol 2018;25:1454-1455. 
  3. Japanese Society for Cancer of the Colon and Rectum. Japanese classification of colorectal, appendiceal, and anal carcinoma: the 3d english edition [secondary publication]. J Anus Rectum Colon 2019;3:175-195. 
  4. Yeh JH, Tseng CH, Huang RY, et al. Long-term outcomes of primary endoscopic resection vs surgery for T1 colorectal cancer: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 2020;18:2813-2823.e5. 
  5. Backes Y, Moss A, Reitsma JB, Siersema PD, Moons LM. Narrow band imaging, magnifying chromoendoscopy, and gross morphological features for the optical diagnosis of T1 colorectal cancer and deep submucosal invasion: a systematic review and meta-analysis. Am J Gastroenterol 2017;112:54-64. 
  6. Saraiva S, Rosa I, Fonseca R, Pereira AD. Colorectal malignant polyps: a modern approach. Ann Gastroenterol 2022;35:17-27. 
  7. Pickhardt PJ, Hain KS, Kim DH, Hassan C. Low rates of cancer or high-grade dysplasia in colorectal polyps collected from computed tomography colonography screening. Clin Gastroenterol Hepatol 2010;8:610-615. 
  8. Kudo S, Kashida H, Tamura T, et al. Colonoscopic diagnosis and management of nonpolypoid early colorectal cancer. World J Surg 2000;24:1081-1090. 
  9. Bogie RMM, Veldman MHJ, Snijders LARS, et al. Endoscopic subtypes of colorectal laterally spreading tumors (LSTs) and the risk of submucosal invasion: a meta-analysis. Endoscopy 2018;50:263-282. 
  10. Kaltenbach T, Anderson JC, Burke CA, et al. Endoscopic removal of colorectal lesions-recommendations by the US Multi-Society Task Force on colorectal cancer. Gastroenterology 2020;158:1095-1129. 
  11. Ferlitsch M, Moss A, Hassan C, et al. Colorectal polypectomy and endoscopic mucosal resection (EMR): European Society of Gastrointestinal Endoscopy (ESGE) Clinical Guideline. Endoscopy 2017;49:270-297. 
  12. Park W, Kim B, Park SJ, et al. Conventional endoscopic features are not sufficient to differentiate small, early colorectal cancer. World J Gastroenterol 2014;20:6586-6593. 
  13. Ikehara H, Saito Y, Matsuda T, Uraoka T, Murakami Y. Diagnosis of depth of invasion for early colorectal cancer using magnifying colonoscopy. J Gastroenterol Hepatol 2010;25:905-912. 
  14. Bugajski M, Kaminski MF, Orlowska J, et al. Suspicious macroscopic features of small malignant colorectal polyps. Scand J Gastroenterol 2015;50:1261-1267. 
  15. Puig I, Lopez-Ceron M, Arnau A, et al. Accuracy of the narrow-band imaging international colorectal endoscopic classification system in identification of deep invasion in colorectal polyps. Gastroenterology 2019;156:75-87. 
  16. Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 1993;25:455-461. 
  17. Kudo SE, Takemura O, Ohtsuka K. Flat and depressed types of early colorectal cancers: from East to West. Gastrointest Endosc Clin N Am 2008;18:581-593, xi. 
  18. Ishigaki T, Kudo SE, Miyachi H, et al. Treatment policy for colonic laterally spreading tumors based on each clinicopathologic feature of 4 subtypes: actual status of pseudo-depressed type. Gastrointest Endosc 2020;92:1083-1094.e6. 
  19. Russo P, Barbeiro S, Awadie H, Libanio D, Dinis-Ribeiro M, Bourke M. Management of colorectal laterally spreading tumors: a systematic review and meta-analysis. Endosc Int Open 2019;7:E239-E259. 
  20. Yamada M, Saito Y, Sakamoto T, et al. Endoscopic predictors of deep submucosal invasion in colorectal laterally spreading tumors. Endoscopy 2016;48:456-464. 
  21. Saito Y, Ono A, Garcia VAJ, et al. Diagnosis and treatment of colorectal tumors: differences between Japan and the West and future prospects. DEN Open 2021;2:e66. 
  22. Nagai M, Suzuki S, Minato Y, et al. Detecting colorectal lesions with image-enhanced endoscopy: an updated review from clinical trials. Clin Endosc 2023;56:553-562. 
  23. Lee HH, Lee BI. Image-enhanced endoscopy in lower gastrointestinal diseases: present and future. Clin Endosc 2018;51:534-540. 
  24. Tanaka S, Sano Y. Aim to unify the narrow band imaging (NBI) magnifying classification for colorectal tumors: current status in Japan from a summary of the consensus symposium in the 79th Annual Meeting of the Japan Gastroenterological Endoscopy Society. Dig Endosc 2011;23 Suppl 1:131-139. 
  25. Tanaka S, Hayashi N, Oka S, Chayama K. Endoscopic assessment of colorectal cancer with superficial or deep submucosal invasion using magnifying colonoscopy. Clin Endosc 2013;46:138-146. 
  26. Sumimoto K, Tanaka S, Shigita K, et al. Clinical impact and characteristics of the narrow-band imaging magnifying endoscopic classification of colorectal tumors proposed by the Japan NBI Expert Team. Gastrointest Endosc 2017;85:816-821. 
  27. Sumimoto K, Tanaka S, Shigita K, et al. Diagnostic performance of Japan NBI Expert Team classification for differentiation among noninvasive, superficially invasive, and deeply invasive colorectal neoplasia. Gastrointest Endosc 2017;86:700-709. 
  28. Kudo S, Tamura S, Nakajima T, Yamano H, Kusaka H, Watanabe H. Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc 1996;44:8-14. 
  29. Bianco MA, Rotondano G, Marmo R, et al. Predictive value of magnification chromoendoscopy for diagnosing invasive neoplasia in nonpolypoid colorectal lesions and stratifying patients for endoscopic resection or surgery. Endoscopy 2006;38:470-476. 
  30. Tanaka S, Kaltenbach T, Chayama K, Soetikno R. High-magnification colonoscopy (with videos). Gastrointest Endosc 2006;64:604-613. 
  31. Kanao H, Tanaka S, Oka S, et al. Clinical significance of type V(I) pit pattern subclassification in determining the depth of invasion of colorectal neoplasms. World J Gastroenterol 2008;14:211-217. 
  32. Li JW, Wang LM, Ichimasa K, Lin KW, Ngu JC, Ang TL. Use of artificial intelligence in the management of T1 colorectal cancer: a new tool in the arsenal or is deep learning out of its depth? Clin Endosc 2024;57:24-35. 
  33. Park EY, Baek DH, Lee MW, Kim GH, Park DY, Song GA. Long-term outcomes of T1 colorectal cancer after endoscopic resection. J Clin Med 2020;9:2451. 
  34. Lopez A, Bouvier AM, Jooste V, et al. Outcomes following polypectomy for malignant colorectal polyps are similar to those following surgery in the general population. Gut 2019;68:111-117. 
  35. Cooper GS, Xu F, Barnholtz Sloan JS, Koroukian SM, Schluchter MD. Management of malignant colonic polyps: a population-based analysis of colonoscopic polypectomy versus surgery. Cancer 2012;118:651-659. 
  36. ASGE Technology Committee, Hwang JH, Konda V, et al. Endoscopic mucosal resection. Gastrointest Endosc 2015;82:215-226. 
  37. Hashiguchi Y, Muro K, Saito Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 2020;25:1-42. 
  38. Pohl H, Srivastava A, Bensen SP, et al. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. Gastroenterology 2013;144:74-80.e1. 
  39. Yamashina T, Uedo N, Akasaka T, et al. Comparison of underwater vs conventional endoscopic mucosal resection of intermediate-size colorectal polyps. Gastroenterology 2019;157:451-461.e2. 
  40. Jung Y, Hwangbo Y, Cho YS, et al. Is colorectal endoscopic submucosal dissection safe and effective for 15-19-mm tumors? Int J Colorectal Dis 2023;38:206. 
  41. Tanaka S, Kashida H, Saito Y, et al. Japan Gastroenterological Endoscopy Society guidelines for colorectal endoscopic submucosal dissection/endoscopic mucosal resection. Dig Endosc 2020;32:219-239. 
  42. Jideh B, Bourke MJ. How to perform wide-field endoscopic mucosal resection and follow-up examinations. Gastrointest Endosc Clin N Am 2019;29:629-646. 
  43. Saito Y, Sakamoto T, Fukunaga S, Nakajima T, Kiriyama S, Matsuda T. Endoscopic submucosal dissection (ESD) for colorectal tumors. Dig Endosc 2009;21 Suppl 1:S7-S12. 
  44. Belderbos TD, Leenders M, Moons LM, Siersema PD. Local recurrence after endoscopic mucosal resection of nonpedunculated colorectal lesions: systematic review and meta-analysis. Endoscopy 2014;46:388-402. 
  45. Komeda Y, Watanabe T, Sakurai T, et al. Risk factors for local recurrence and appropriate surveillance interval after endoscopic resection. World J Gastroenterol 2019;25:1502-1512. 
  46. Sekiguchi M, Matsuda T, Hotta K, Saito Y. Post-polypectomy surveillance: the present and the future. Clin Endosc 2022;55:489-495. 
  47. Kim SY, Kwak MS, Yoon SM, et al. Korean guidelines for postpolypectomy colonoscopic surveillance: 2022 revised edition. Clin Endosc 2022;55:703-725. 
  48. Binmoeller KF, Weilert F, Shah J, Bhat Y, Kane S. "Underwater" EMR without submucosal injection for large sessile colorectal polyps (with video). Gastrointest Endosc 2012;75:1086-1091. 
  49. Nett A, Binmoeller K. Underwater endoscopic mucosal resection. Gastrointest Endosc Clin N Am 2019;29:659-673. 
  50. Zhang Z, Xia Y, Cui H, et al. Underwater versus conventional endoscopic mucosal resection for small size non-pedunculated colorectal polyps: a randomized controlled trial : (UEMR vs. CEMR for small size non-pedunculated colorectal polyps). BMC Gastroenterol 2020;20:311. 
  51. Yen AW, Leung JW, Wilson MD, Leung FW. Underwater versus conventional endoscopic resection of nondiminutive nonpedunculated colorectal lesions: a prospective randomized controlled trial (with video). Gastrointest Endosc 2020;91:643-654.e2. 
  52. Inoue T, Nakagawa K, Yamasaki Y, et al. Underwater endoscopic mucosal resection versus endoscopic submucosal dissection for 20-30 mm colorectal polyps. J Gastroenterol Hepatol 2021;36:2549-2557. 
  53. Nagl S, Ebigbo A, Goelder SK, et al. Underwater vs conventional endoscopic mucosal resection of large sessile or flat colorectal polyps: a prospective randomized controlled trial. Gastroenterology 2021;161:1460-1474.e1. 
  54. Chien H, Imai K, Hotta K, et al. Tip-in EMR for R0 resection for a large flat colonic tumor. Gastrointest Endosc 2016;84:743. 
  55. Jacques J, Legros R, Charissoux A, et al. Anchoring the snare tip by means of a small incision facilitates en bloc endoscopic mucosal resection and increases the specimen size. Endoscopy 2017;49(S 01):E39-E41. 
  56. Sato Y, Ozawa SI, Yasuda H, et al. Tip-in endoscopic mucosal resection for large colorectal sessile polyps. Surg Endosc 2021;35:1820-1826. 
  57. Pioche M, Wallenhorst T, Lepetit H, et al. Endoscopic mucosal resection with anchoring of the snare tip: multicenter retrospective evaluation of effectiveness and safety. Endosc Int Open 2019;7:E1496-E1502. 
  58. Imai K, Hotta K, Ito S, et al. Tip-in endoscopic mucosal resection for 15- to 25-mm colorectal adenomas: a single-center, randomized controlled trial (STAR Trial). Am J Gastroenterol 2021;116:1398-1405. 
  59. Takada K, Hotta K, Imai K, et al. Tip-in EMR as an alternative to endoscopic submucosal dissection for 20- to 30-mm nonpedunculated colorectal neoplasms. Gastrointest Endosc 2022;96:849-856.e3. 
  60. Yang DH, Kwak MS, Park SH, et al. Endoscopic mucosal resection with circumferential mucosal incision for colorectal neoplasms: comparison with endoscopic submucosal dissection and between two endoscopists with different experiences. Clin Endosc 2017;50:379-387. 
  61. Lee EJ, Lee JB, Lee SH, Youk EG. Endoscopic treatment of large colorectal tumors: comparison of endoscopic mucosal resection, endoscopic mucosal resection-precutting, and endoscopic submucosal dissection. Surg Endosc 2012;26:2220-2230. 
  62. Yoshida N, Inoue K, Dohi O, et al. Efficacy of precutting endoscopic mucosal resection with full or partial circumferential incision using a snare tip for difficult colorectal lesions. Endoscopy 2019;51:871-876. 
  63. Fuccio L, Hassan C, Ponchon T, et al. Clinical outcomes after endoscopic submucosal dissection for colorectal neoplasia: a systematic review and meta-analysis. Gastrointest Endosc 2017;86:74-86.e17. 
  64. Yoshida N, Naito Y, Yasuda R, et al. The efficacy of the pocket-creation method for cases with severe fibrosis in colorectal endoscopic submucosal dissection. Endosc Int Open 2018;6:E975-E983. 
  65. Faller J, Jacques J, Oung B, et al. Endoscopic submucosal dissection with double clip and rubber band traction for residual or locally recurrent colonic lesions after previous endoscopic mucosal resection. Endoscopy 2020;52:383-388. 
  66. Ide D, Ohya TR, Ishioka M, et al. Efficacy of the pocket-creation method with a traction device in endoscopic submucosal dissection for residual or recurrent colorectal lesions. Clin Endosc 2022;55:655-664. 
  67. Yang DH. Combination of endoscopic submucosal dissection techniques, a practical solution for difficult cases. Clin Endosc 2022;55:626-627. 
  68. Ma MX, Bourke MJ. Endoscopic submucosal dissection in the West: current status and future directions. Dig Endosc 2018;30:310-320. 
  69. Rashid MU, Alomari M, Afraz S, Erim T. EMR and ESD: indications, techniques and results. Surg Oncol 2022;43:101742. 
  70. Fujiya M, Tanaka K, Dokoshi T, et al. Efficacy and adverse events of EMR and endoscopic submucosal dissection for the treatment of colon neoplasms: a meta-analysis of studies comparing EMR and endoscopic submucosal dissection. Gastrointest Endosc 2015;81:583-595. 
  71. Gweon TG, Yang DH. Management of complications related to colorectal endoscopic submucosal dissection. Clin Endosc 2023;56:423-432. 
  72. Zwager LW, Bastiaansen BAJ, van der Spek BW, et al. Endoscopic full-thickness resection of T1 colorectal cancers: a retrospective analysis from a multicenter Dutch eFTR registry. Endoscopy 2022;54:475-485. 
  73. Dolan RD, Bazarbashi AN, McCarty TR, Thompson CC, Aihara H. Endoscopic full-thickness resection of colorectal lesions: a systematic review and meta-analysis. Gastrointest Endosc 2022;95:216-224.e18. 
  74. Park CH, Yang DH, Kim JW, et al. Clinical practice guideline for endoscopic resection of early gastrointestinal cancer. Clin Endosc 2020;53:142-166. 
  75. Lugli A, Kirsch R, Ajioka Y, et al. Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016. Mod Pathol 2017;30:1299-1311. 
  76. Glynne-Jones R, Wyrwicz L, Tiret E, et al. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2018;29(Suppl 4):iv263. 
  77. Ciocalteu A, Gheonea DI, Saftoiu A, Streba L, Dragoescu NA, Tenea-Cojan TS. Current strategies for malignant pedunculated colorectal polyps. World J Gastrointest Oncol 2018;10:465-475. 
  78. Ichimasa K, Kudo SE, Miyachi H, et al. Current problems and perspectives of pathological risk factors for lymph node metastasis in T1 colorectal cancer: systematic review. Dig Endosc 2022;34:901-912. 
  79. Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology 1985;89:328-336. 
  80. Kitajima K, Fujimori T, Fujii S, et al. Correlations between lymph node metastasis and depth of submucosal invasion in submucosal invasive colorectal carcinoma: a Japanese collaborative study. J Gastroenterol 2004;39:534-543. 
  81. Nivatvongs S, Rojanasakul A, Reiman HM, et al. The risk of lymph node metastasis in colorectal polyps with invasive adenocarcinoma. Dis Colon Rectum 1991;34:323-328. 
  82. Cooper HS, Deppisch LM, Gourley WK, et al. Endoscopically removed malignant colorectal polyps: clinicopathologic correlations. Gastroenterology 1995;108:1657-1665. 
  83. ASGE Standards of Practice Committee, Fisher DA, Shergill AK, et al. Role of endoscopy in the staging and management of colorectal cancer. Gastrointest Endosc 2013;78:8-12. 
  84. Oh JR, Park B, Lee S, et al. Nomogram development and external validation for predicting the risk of lymph node metastasis in T1 colorectal cancer. Cancer Res Treat 2019;51:1275-1284. 
  85. Ha RK, Han KS, Sohn DK, et al. Histopathologic risk factors for lymph node metastasis in patients with T1 colorectal cancer. Ann Surg Treat Res 2017;93:266-271. 
  86. Zwager LW, Bastiaansen BAJ, Montazeri NSM, et al. Deep submucosal invasion is not an independent risk factor for lymph node metastasis in T1 colorectal cancer: a meta-analysis. Gastroenterology 2022;163:174-189. 
  87. Kouyama Y, Kudo SE, Miyachi H, et al. Practical problems of measuring depth of submucosal invasion in T1 colorectal carcinomas. Int J Colorectal Dis 2016;31:137-146. 
  88. Miyachi H, Kudo SE, Ichimasa K, et al. Management of T1 colorectal cancers after endoscopic treatment based on the risk stratification of lymph node metastasis. J Gastroenterol Hepatol 2016;31:1126-1132. 
  89. Butte JM, Tang P, Gonen M, et al. Rate of residual disease after complete endoscopic resection of malignant colonic polyp. Dis Colon Rectum 2012;55:122-127. 
  90. Bujanda L, Cosme A, Gil I, Arenas-Mirave JI. Malignant colorectal polyps. World J Gastroenterol 2010;16:3103-3111. 
  91. Gijsbers KM, van der Schee L, van Veen T, et al. Impact of ≥ 0.1-mm free resection margins on local intramural residual cancer after local excision of T1 colorectal cancer. Endosc Int Open 2022;10:E282-E290. 
  92. Toyoshima N, Abe S, Saito Y. In addition to free deep margins, R0 resection should be required for T1 colorectal cancers to inform further surgical resection. Endosc Int Open 2022;10:E291-E292. 
  93. Ito T, Eishi Y, Kobayashi D, Akashi T, Koike M, Ohashi K. A risk stratification for nodal metastasis in T1 colorectal cancer after successful therapeutic endoscopy. Gastrointest Endosc 2022;96:131-134. 
  94. Dang H, Dekkers N, le Cessie S, et al. Risk and time pattern of recurrences after local endoscopic resection of T1 colorectal cancer: a meta-analysis. Clin Gastroenterol Hepatol 2022;20:e298-e314. 
  95. Park EY, Baek DH, Song GA, Kim GH, Lee BE, Park DY. Long-term outcomes of endoscopically resected laterally spreading tumors with a positive histological lateral margin. Surg Endosc 2020;34:3999-4010. 
  96. Sakamoto T, Matsuda T, Otake Y, Nakajima T, Saito Y. Predictive factors of local recurrence after endoscopic piecemeal mucosal resection. J Gastroenterol 2012;47:635-640. 
  97. National Health Commission of the People's Republic of China; Society of Oncology, Chinese Medical Association. National Health Commission guidelines for diagnosis and treatment of colorectal cancer 2023 in China (English version). Chin J Cancer Res 2023;35:197-232. 
  98. Bartel MJ, Brahmbhatt BS, Wallace MB. Management of colorectal T1 carcinoma treated by endoscopic resection from the Western perspective. Dig Endosc 2016;28:330-341. 
  99. Iguchi K, Mushiake H, Aoyama T, et al. Additional surgical resection after endoscopic resection for patients with high-risk T1 colorectal cancer. In Vivo 2019;33:1243-1248. 
  100. Oh EH, Kim N, Hwang SW, et al. Comparison of long-term recurrence-free survival between primary surgery and endoscopic resection followed by secondary surgery in T1 colorectal cancer. Gastrointest Endosc 2021;94:394-404. 
  101. Joo HJ, Seok JU, Kim BC, et al. Effects of prior endoscopic resection on recurrence in patients with T1 colorectal cancer who underwent radical surgery. Int J Colorectal Dis 2023;38:167.