Abstract
Background
The personalized treatments of T1 colorectal cancer (CRC) remains controversial. We compared the long-term outcomes of T1 CRC patients after endoscopic resection (ER) and surgery, and evaluated the risk factors for the long-term prognosis.
Methods
T1 CRCs after resection at the Cancer Hospital, Chines Academy of Medical Sciences from June 2011 to November 2021 were reviewed. High-risk factors included positive resection margin, poor differentiation, deep submucosal invasion (DSI ≥ 1000 μm), lymphovascular invasion and intermediate/high tumor budding. Comparative analyses were conducted based on three treatment methods: follow-up after ER (Group A), additional surgery after ER (Group B) and initial surgery (Group C). The primary endpoints included recurrence-free survival (RFS) and overall survival (OS). Cox proportional hazard regression models were constructed to identify risk factors for RFS and OS.
Results
A total of 528 patients were enrolled (173 patients in Group A, 102 patients in Group B, 253 patients in Group C). The 3-year RFS, 5-year RFS, 3-year OS, and 5-year OS rates were 96.7%, 94.7%, 99.1%, and 97.8%, respectively. In the absence of other high-risk factors, RFS (P = 0.321) and OS (P = 0.155) of patients with DSI after ER were not inferior to those after surgery. Multivariate analyses identified sex (HR 0.379; 95% CI 0.160–0.894), Charlson comorbidities index (CCI) (HR 3.330; 95% CI 1.571–7.062), margin (HR 8.212; 95% CI 2.325–29.006), and budding (HR 3.794; 95% CI 1.686–8.541) as independent predictive factors of RFS, and identified CCI (HR 10.266; 95% CI 2.856–36.899) as an independent predictive factor of OS.
Conclusion
The long-term outcomes of ER are comparable to those of surgery in T1 CRC patients with DSI when other high-risk factors are negative. Resection margin, tumor budding, sex, and CCI may be the most important long-term prognostic factors for T1 CRC patients.
Graphical abstract
Similar content being viewed by others
References
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249
Hashiguchi Y, Muro K, Saito Y, Ito Y, Ajioka Y, Hamaguchi T, Hasegawa K, Hotta K, Ishida H, Ishiguro M, Ishihara S, Kanemitsu Y, Kinugasa Y, Murofushi K, Nakajima TE, Oka S, Tanaka T, Taniguchi H, Tsuji A, Uehara K, Ueno H, Yamanaka T, Yamazaki K, Yoshida M, Yoshino T, Itabashi M, Sakamaki K, Sano K, Shimada Y, Tanaka S, Uetake H, Yamaguchi S, Yamaguchi N, Kobayashi H, Matsuda K, Kotake K, Sugihara K (2020) Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2019 for the treatment of colorectal cancer. Int J Clin Oncol 25:1–42
Pimentel-Nunes P, Dinis-Ribeiro M, Ponchon T, Repici A, Vieth M, De Ceglie A, Amato A, Berr F, Bhandari P, Bialek A, Conio M, Haringsma J, Langner C, Meisner S, Messmann H, Morino M, Neuhaus H, Piessevaux H, Rugge M, Saunders BP, Robaszkiewicz M, Seewald S, Kashin S, Dumonceau JM, Hassan C, Deprez PH (2015) Endoscopic submucosal dissection: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy 47:829–854
Shaukat A, Kaltenbach T, Dominitz JA, Robertson DJ, Anderson JC, Cruise M, Burke CA, Gupta S, Lieberman D, Syngal S, Rex DK (2020) Endoscopic recognition and management strategies for malignant colorectal polyps: recommendations of the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 115:1751–1767
Arthursson V, Medic S, Syk I, Rönnow CF, Thorlacius H (2022) Risk of recurrence after endoscopic resection of nonpedunculated T1 colorectal cancer. Endoscopy 54:1071–1077
Yeh JH, Tseng CH, Huang RY, Lin CW, Lee CT, Hsiao PJ, Wu TC, Kuo LT, Wang WL (2020) Long-term outcomes of primary endoscopic resection vs surgery for T1 colorectal cancer: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 18:2813–2823.e5
Ha RK, Park B, Han KS, Sohn DK, Hong CW, Chang Kim B, Kim B, Chan Park S, Chang HJ, Oh JH (2022) Subpopulation analysis of survival in high-risk T1 colorectal cancer: surgery versus endoscopic resection only. Gastrointest Endosc 96:1036–1046.e1
Dang H, Dekkers N, le Cessie S, van Hooft JE, van Leerdam ME, Oldenburg PP, Flothuis L, Schoones JW, Langers AMJ, Hardwick JCH, van der Kraan J, Boonstra JJ (2022) Risk and time pattern of recurrences after local endoscopic resection of T1 colorectal cancer: a meta-analysis. Clin Gastroenterol Hepatol 20:e298–e314
Shin J, Kim ER, Jang HJ, Baek DH, Yang DH, Lee BI, Cho KB, Cho JW, Jung SA, Hong SJ, Ko BM (2022) Long-term prognosis of curative endoscopic submucosal dissection for early colorectal cancer according to submucosal invasion: a multicenter cohort study. BMC Gastroenterol 22:417
Rönnow CF, Arthursson V, Toth E, Krarup PM, Syk I, Thorlacius H (2022) Lymphovascular infiltration, not depth of invasion, is the critical risk factor of metastases in early colorectal cancer: retrospective population-based cohort study on prospectively collected data, including validation. Ann Surg 275:e148–e154
Yasue C, Chino A, Takamatsu M, Namikawa K, Ide D, Saito S, Igarashi M, Fujisaki J (2019) Pathological risk factors and predictive endoscopic factors for lymph node metastasis of T1 colorectal cancer: a single-center study of 846 lesions. J Gastroenterol 54:708–717
Arthursson V, Rosén R, Norlin JM, Gralén K, Toth E, Syk I, Thorlacius H, Rönnow CF (2021) Cost comparisons of endoscopic and surgical resection of stage T1 rectal cancer. Endosc Int Open 9:E1512–E1519
Nagtegaal ID, Odze RD, Klimstra D, Paradis V, Rugge M, Schirmacher P, Washington KM, Carneiro F, Cree IA (2020) The 2019 WHO classification of tumours of the digestive system. Histopathology 76:182–188
Participants in the Paris Workshop (2003) The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. Gastrointest Endosc 58(6 Suppl):S3–S43
Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y (1995) Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 38:1286–1295
Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD (1985) Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology 89:328–336
Lugli A, Kirsch R, Ajioka Y, Bosman F, Cathomas G, Dawson H, El Zimaity H, Fléjou JF, Hansen TP, Hartmann A, Kakar S, Langner C, Nagtegaal I, Puppa G, Riddell R, Ristimäki A, Sheahan K, Smyrk T, Sugihara K, Terris B, Ueno H, Vieth M, Zlobec I, Quirke P (2017) Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016. Mod Pathol 30:1299–1311
Belderbos TD, van Erning FN, de Hingh IH, van Oijen MG, Lemmens VE, Siersema PD (2017) Long-term recurrence-free survival after standard endoscopic resection versus surgical resection of submucosal invasive colorectal cancer: a population-based study. Clin Gastroenterol Hepatol 15:403–411.e1
Zwager LW, Bastiaansen BAJ, Montazeri NSM, Hompes R, Barresi V, Ichimasa K, Kawachi H, Machado I, Masaki T, Sheng W, Tanaka S, Togashi K, Yasue C, Fockens P, Moons LMG, Dekker E (2022) Deep submucosal invasion is not an independent risk factor for lymph node metastasis in T1 colorectal cancer: a meta-analysis. Gastroenterology 163:174–189
Bae HJ, Ju H, Lee HH, Kim J, Lee BI, Lee SH, Won DD, Lee YS, Lee IK, Cho YS (2023) Long-term outcomes after endoscopic versus surgical resection of T1 colorectal carcinoma. Surg Endosc 37:1231–1241
Nian J, Tao L, Zhou W (2022) Prior endoscopic resection does not affect the outcome of secondary surgery for T1 colorectal cancer, a systematic review and meta-analysis. Int J Colorectal Dis 37:273–281
Takamaru H, Saito Y, Sekiguchi M, Yamada M, Sakamoto T, Matsuda T, Sekine S, Ochiai H, Tsukamoto S, Shida D, Kanemitsu Y (2021) Endoscopic resection before surgery does not affect the recurrence rate in patients with high-risk T1 colorectal cancer. Clin Transl Gastroenterol 12:e00336
Shin JW, Han KS, Hyun JH, Lee SJ, Kim B, Hong CW, Kim BC, Sohn DK, Chang HJ, Kim MJ, Park SC, Oh JH (2018) Risk of recurrence after endoscopic resection of early colorectal cancer with positive margins. Endoscopy 50:241–247
Brooker JC, Saunders BP, Shah SG, Thapar CJ, Suzuki N, Williams CB (2002) Treatment with argon plasma coagulation reduces recurrence after piecemeal resection of large sessile colonic polyps: a randomized trial and recommendations. Gastrointest Endosc 55:371–375
Sidhu M, Shahidi N, Gupta S, Desomer L, Vosko S, Arnout van Hattem W, Hourigan LF, Lee EYT, Moss A, Raftopoulos S, Heitman SJ, Williams SJ, Zanati S, Tate DJ, Burgess N, Bourke MJ (2021) Outcomes of thermal ablation of the mucosal defect margin after endoscopic mucosal resection: a prospective, international, multicenter trial of 1000 large nonpedunculated colorectal polyps. Gastroenterology 161:163–170.e3
Avalos DJ, Jia Y, Zuckerman MJ, Michael M, Gonzalez-Martinez J, Mendoza-Ladd A, Garcia CJ, Sunny J, Delgado VC, Hernandez B, Dwivedi AK, Mallawaarachchi IV, Dodoo C, Othman MO (2020) Segmental withdrawal during screening colonoscopy does not increase adenoma detection rate. South Med J 113:438–446
Markowski AR, Markowska AJ, Ustymowicz W, Pryczynicz A, Guzinska-Ustymowicz K (2022) Simultaneous analysis of tumor-infiltrating immune cells density, tumor budding status, and presence of lymphoid follicles in CRC tissue. Sci Rep 12:21732
Park EY, Baek DH, Lee MW, Kim GH, Park DY, Song GA (2020) Long-term outcomes of T1 colorectal cancer after endoscopic resection. J Clin Med 9:2451
Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383
Marco S, Michael JB, Roberta M, Marhieu P, Pradeep B, Jérémie J, Amyn H, Dennis Y, Eduardo A, Michal Filip K, Helmut M, de Alberto Herreros T, Sandro S, Boris P, Jerome R, Sophie G, Shraddha G, Peter D, Neal S, Ejaz H, Carola F, Edoardo V, Andrea I, Asma A, Cesare H, Alessandro R (2022) Clinical outcome of non-curative endoscopic submucosal dissection for early colorectal cancer. Gut 71:1998–2004
Ouchi A, Toriyama K, Kinoshita T, Tanaka T, Shimizu Y, Niwa Y, Tajika M, Komori K (2020) Variations in clinical features and oncologic behaviors of T1 colorectal cancer according to tumor location. Int J Clin Oncol 25:1130–1136
Ichimasa K, Kudo SE, Kouyama Y, Mochizuki K, Takashina Y, Misawa M, Mori Y, Hayashi T, Wakamura K, Miyachi H (2022) Tumor location as a prognostic factor in T1 colorectal cancer. J Anus Rectum Colon 6:9–15
Mochizuki K, Kudo SE, Ichimasa K, Kouyama Y, Matsudaira S, Takashina Y, Maeda Y, Ishigaki T, Nakamura H, Toyoshima N, Mori Y, Misawa M, Ogata N, Kudo T, Hayashi T, Wakamura K, Sawada N, Ishida F, Miyachi H (2020) Left-sided location is a risk factor for lymph node metastasis of T1 colorectal cancer: a single-center retrospective study. Int J Colorectal Dis 35:1911–1919
Acknowledgements
We are very grateful to all patients and families that agreed to participate in the study.
Funding
This research was supported by grants from (1) CAMS Innovation Fund for Medical Sciences (CIFMS) (Grant Nos. 2021-I2M-1-061, 2021-I2M-1-015, 2021-I2M-1-013, 2022-I2M-C&T-B-054, 2021-I2M-1-010); (2) Sanming Project of Medicine in Shenzhen (No. SZSM201911008); (3) Capital’s Funds for Health Improvement and Research (Grant No. CRF2020-2-4025); (4) Beijing Hope Run Special Fund of Cancer Foundation of China (Grant No. LC2021A03).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Disclosures
Shibo Song, Lizhou Dou, Yueming Zhang, Xudong Liu, Yong Liu, Shun He, and Guiqi Wang have no conflicts of interest or financial ties to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Song, S., Dou, L., Zhang, Y. et al. Long-term outcomes of endoscopic or surgical resection in T1 colorectal cancer patients: a retrospective cohort study. Surg Endosc 38, 1499–1511 (2024). https://doi.org/10.1007/s00464-023-10586-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-023-10586-w