Abstract
Purpose
Additional surgical resection (ASR) after endoscopic resection (ER) in patients with colorectal cancer (CRC) allows a complete staging and may decrease the recurrence rate, but no meta-analysis is available. This study aimed to compare the effectiveness of ER vs. ER + ASR as a treatment for patients with T1 (stage 1) CRC.
Methods
We performed a systematic search from databases (PubMed, Embase, and Cochrane library) for cohort studies published up to November 2019. The outcomes were overall survival (OS), local recurrence, recurrence, disease-specific survival, recurrence-free survival, and metastasis.
Results
Seven studies were included. There were 1205 patients in the ASR group and 993 patients in the ER group. Compared with ER, ASR was associated with better OS (OR = 0.31, 95% CI: 0.18–0.53, P < 0.001) and a borderline significant difference in lower local recurrence rates (OR = 0.29, 95% CI: 0.08–1.01, P = 0.052), but no differences were observed in recurrences, disease-specific survival, recurrence-free survival, and distant metastasis. A sensitivity analysis was performed; excluding each study sequentially from the pooled analysis did not affect the overall conclusion of the study.
Conclusion
Compared with ER, ASR after ER could improve the overall survival for patients with T1 CRC.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Kuipers EJ, Grady WM, Lieberman D, Seufferlein T, Sung JJ, Boelens PG, van de Velde CJ, Watanabe T (2015) Colorectal cancer. Nat Rev Dis Primers 1:15065. https://doi.org/10.1038/nrdp.2015.65
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424. https://doi.org/10.3322/caac.21492
Glynne-Jones R, Wyrwicz L, Tiret E, Brown G, Rodel C, Cervantes A, Arnold D, Committee EG (2017) Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 28(suppl_4):iv22–iv40. https://doi.org/10.1093/annonc/mdx224
Brenner H, Hoffmeister M, Arndt V, Stegmaier C, Altenhofen L, Haug U (2010) Protection from right- and left-sided colorectal neoplasms after colonoscopy: population-based study. J Natl Cancer Inst 102(2):89–95. https://doi.org/10.1093/jnci/djp436
NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines). Colon cancer. Version 4.2019 (2019). National Comprehensive Cancer Network, Fort Washington
Dumoulin FL, Hildenbrand R (2019) Endoscopic resection techniques for colorectal neoplasia: current developments. World J Gastroenterol 25(3):300–307. https://doi.org/10.3748/wjg.v25.i3.300
Emmanuel A, Gulati S, Burt M, Hayee B, Haji A (2017) Colorectal endoscopic submucosal dissection: patient selection and special considerations. Clin Exp Gastroenterol 10:121–131. https://doi.org/10.2147/CEG.S120395
Ebigbo A, Probst A, Messmann H (2018) Endoscopic treatment of early colorectal cancer-just a competition with surgery? Innov Surg Sci 3(1):39–46. https://doi.org/10.1515/iss-2017-0037
Tanaka S, Terasaki M, Kanao H, Oka S, Chayama K (2012) Current status and future perspectives of endoscopic submucosal dissection for colorectal tumors. Dig Endosc 24(Suppl 1):73–79. https://doi.org/10.1111/j.1443-1661.2012.01252.x
Muto T, Oya M (2003) Recent advances in diagnosis and treatment of colorectal T1 carcinoma. Dis Colon Rectum 46(10 Suppl):S89–S93. https://doi.org/10.1097/01.DCR.0000083525.97708.B5
Tanaka S, Haruma K, Oh EH, Nagata S, Hirota Y, Furudoi A, Amioka T, Kitadai Y, Yoshihara M, Shimamoto F (2000) Conditions of curability after endoscopic resection for colorectal carcinoma with submucosally massive invasion. Oncol Rep 7(4):783–788. https://doi.org/10.3892/or.7.4.783
Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR (2002) Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum 45(2):200–206. https://doi.org/10.1007/s10350-004-6147-7
Iguchi K, Mushiake H, Aoyama T, Suwa H, Yukawa N, Ota M, Rino Y, Kunisaki C, Endo I, Masuda M (2019) Additional surgical resection after endoscopic resection for patients with high-risk T1 colorectal cancer. In Vivo 33(4):1243–1248. https://doi.org/10.21873/invivo.11596
Fujihara S, Mori H, Kobara H, Nishiyama N, Yoshitake A, Deguchi A, Masaki T (2017) Endoscopic treatment for high-risk T1 colorectal cancer: is it better to begin with endoscopic or surgical treatment? Transl Gastroenterol Hepatol 2:39. https://doi.org/10.21037/tgh.2017.04.04
Choi JY, Jung SA, Shim KN, Cho WY, Keum B, Byeon JS, Huh KC, Jang BI, Chang DK, Jung HY, Kong KA, Korean ESDSG (2015) Meta-analysis of predictive clinicopathologic factors for lymph node metastasis in patients with early colorectal carcinoma. J Korean Med Sci 30(4):398–406. https://doi.org/10.3346/jkms.2015.30.4.398
Bosch SL, Teerenstra S, de Wilt JH, Cunningham C, Nagtegaal ID (2013) Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 45(10):827–834. https://doi.org/10.1055/s-0033-1344238
Beaton C, Twine CP, Williams GL, Radcliffe AG (2013) Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer. Color Dis 15(7):788–797. https://doi.org/10.1111/codi.12129
Turner RM, Bird SM, Higgins JP (2013) The impact of study size on meta-analyses: examination of underpowered studies in Cochrane reviews. PLoS One 8(3):e59202. https://doi.org/10.1371/journal.pone.0059202
Deeks JJ, Dinnes J, D’Amico R, Sowden AJ, Sakarovitch C, Song F, Petticrew M, Altman DG, International Stroke Trial Collaborative G, European Carotid Surgery Trial Collaborative G (2003) Evaluating non-randomised intervention studies. Health Technol Assess 7(27):iii–x, 1-173. https://doi.org/10.3310/hta7270
Lau J, Ioannidis JP, Terrin N, Schmid CH, Olkin I (2006) The case of the misleading funnel plot. BMJ 333(7568):597–600. https://doi.org/10.1136/bmj.333.7568.597
Higgins J, Green S (2011) Recommendations on testing for funnel plot asymmetry. In: Higgins J, Green S (eds) Cochrane handbook for systematic review of interventions. Version 5.1.0. Cochrane Collaboration, London
Nishikawa Y, Horimatsu T, Nishizaki D, Kohno A, Yokoyama A, Yoshioka M, Hida K, Sakanaka K, Minamiguchi S, Seno H, Sakai Y, Nakayama T (2019) Qualitative and quantitative analysis of posttreatment strategy after endoscopic resection for patients with T1 colorectal cancer at high risk of lymph node metastasis. J Gastrointest Cancer 51:242–249. https://doi.org/10.1007/s12029-019-00247-4
Tamaru Y, Oka S, Tanaka S, Nagata S, Hiraga Y, Kuwai T, Furudoi A, Tamura T, Kunihiro M, Okanobu H, Nakadoi K, Kanao H, Higashiyama M, Arihiro K, Kuraoka K, Shimamoto F, Chayama K (2017) Long-term outcomes after treatment for T1 colorectal carcinoma: a multicenter retrospective cohort study of Hiroshima GI Endoscopy Research Group. J Gastroenterol 52(11):1169–1179. https://doi.org/10.1007/s00535-017-1318-1
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(3):403–411 e401. https://doi.org/10.1016/j.cgh.2016.08.041
Nozawa H, Ishihara S, Fujishiro M, Kodashima S, Ohtani K, Yasuda K, Nishikawa T, Tanaka T, Tanaka J, Kiyomatsu T, Kawai K, Hata K, Kazama S, Sunami E, Kitayama J, Watanabe T (2016) Outcome of salvage surgery for colorectal cancer initially treated by upfront endoscopic therapy. Surgery 159(3):713–720. https://doi.org/10.1016/j.surg.2015.09.008
Yoshii S, Nojima M, Nosho K, Omori S, Kusumi T, Okuda H, Tsukagoshi H, Fujita M, Yamamoto H, Hosokawa M (2014) Factors associated with risk for colorectal cancer recurrence after endoscopic resection of T1 tumors. Clin Gastroenterol Hepatol 12(2):292–302 e293. https://doi.org/10.1016/j.cgh.2013.08.008
Yoda Y, Ikematsu H, Matsuda T, Yamaguchi Y, Hotta K, Kobayashi N, Fujii T, Oono Y, Sakamoto T, Nakajima T, Takao M, Shinohara T, Fujimori T, Kaneko K, Saito Y (2013) A large-scale multicenter study of long-term outcomes after endoscopic resection for submucosal invasive colorectal cancer. Endoscopy 45(9):718–724. https://doi.org/10.1055/s-0033-1344234
Nakadoi K, Tanaka S, Kanao H, Terasaki M, Takata S, Oka S, Yoshida S, Arihiro K, Chayama K (2012) Management of T1 colorectal carcinoma with special reference to criteria for curative endoscopic resection. J Gastroenterol Hepatol 27(6):1057–1062. https://doi.org/10.1111/j.1440-1746.2011.07041.x
Rickert A, Aliyev R, Belle S, Post S, Kienle P, Kahler G (2014) Oncologic colorectal resection after endoscopic treatment of malignant polyps: does endoscopy have an adverse effect on oncologic and surgical outcomes? Gastrointest Endosc 79(6):951–960. https://doi.org/10.1016/j.gie.2013.11.014
Kobayashi H, Higuchi T, Uetake H, Iida S, Ishikawa T, Ishiguro M, Sugihara K (2012) Resection with en bloc removal of regional lymph node after endoscopic resection for T1 colorectal cancer. Ann Surg Oncol 19(13):4161–4167. https://doi.org/10.1245/s10434-012-2471-7
Takatsu Y, Fukunaga Y, Hamasaki S, Ogura A, Nagata J, Nagasaki T, Akiyoshi T, Konishi T, Fujimoto Y, Nagayama S, Ueno M (2016) Recurrent colorectal cancer after endoscopic resection when additional surgery was recommended. World J Gastroenterol 22(7):2336–2341. https://doi.org/10.3748/wjg.v22.i7.2336
Kobayashi H, Mochizuki H, Morita T, Kotake K, Teramoto T, Kameoka S, Saito Y, Takahashi K, Hase K, Oya M, Maeda K, Hirai T, Kameyama M, Shirouzu K, Sugihara K (2011) Characteristics of recurrence after curative resection for T1 colorectal cancer: Japanese multicenter study. J Gastroenterol 46(2):203–211. https://doi.org/10.1007/s00535-010-0341-2
Kouyama Y, Kudo SE, Miyachi H, Ichimasa K, Matsudaira S, Misawa M, Mori Y, Kudo T, Hayashi T, Wakamura K, Ishida F, Hamatani S (2018) Risk factors of recurrence in T1 colorectal cancers treated by endoscopic resection alone or surgical resection with lymph node dissection. Int J Color Dis 33(8):1029–1038. https://doi.org/10.1007/s00384-018-3081-z
Watanabe D, Toyonaga T, Ooi M, Yoshizaki T, Ohara Y, Tanaka S, Kawara F, Ishida T, Morita Y, Umegaki E, Matsuda T, Sumi Y, Nishio M, Yokozaki H, Azuma T (2018) Clinical outcomes of deep invasive submucosal colorectal cancer after ESD. Surg Endosc 32(4):2123–2130. https://doi.org/10.1007/s00464-017-5910-5
Japanese Society for Cancer of the Colon and Rectum (1994) General rules for clinical and pathological studies on cancer of the colon, rectum and anus. Revision 5th ed. Kanehara & Co., Ltd., Tokyo
Japanese Society for Cancer of the Colon and Rectum (1998) General rules for clinical and pathological studies on cancer of the colon, rectum and anus. 6th ed. Kanehara & Co., Ltd., Tokyo
Awadie H, Bourke MJ (2018) When colonoscopy fails... refer, repeat, and succeed. GE Port J Gastroenterol 25(6):279–281. https://doi.org/10.1159/000486804
Kaltenbach T, Anderson JC, Burke CA, Dominitz JA, Gupta S, Lieberman D, Robertson DJ, Shaukat A, Syngal S, Rex DK (2020) Endoscopic removal of colorectal lesions-recommendations by the US Multi-Society Task Force on Colorectal Cancer. Gastrointest Endosc 91(3):486–519. https://doi.org/10.1016/j.gie.2020.01.029
Rex DK, Petrini JL, Baron TH, Chak A, Cohen J, Deal SE, Hoffman B, Jacobson BC, Mergener K, Petersen BT, Safdi MA, Faigel DO, Pike IM (2006) Quality indicators for colonoscopy. Gastrointest Endosc 63(4 Suppl):S16–S28. https://doi.org/10.1016/j.gie.2006.02.021
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Tian, Y., Rong, L. & Ma, Y. Surgical resection after endoscopic resection in patients with T1 colorectal cancer: a meta-analysis. Int J Colorectal Dis 36, 457–466 (2021). https://doi.org/10.1007/s00384-020-03752-2
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DOI: https://doi.org/10.1007/s00384-020-03752-2