Endoscopic surveillance after surgical or endoscopic resection for colorectal cancer: European Society of Gastrointestinal Endoscopy (ESGE) and European Society of Digestive Oncology (ESDO) Guideline

Cesare Hassan; Piotr Tomasz Wysocki; Lorenzo Fuccio; Thomas Seufferlein; Mário Dinis-Ribeiro; Catarina Brandão; Jaroslaw Regula; Leonardo Frazzoni; Maria Pellise; Sergio Alfieri; Evelien Dekker; Rodrigo Jover; Gerardo Rosati; Carlo Senore; Cristiano Spada; Ian Gralnek; Jean-Marc Dumonceau; Jeanin E. van Hooft; Eric van Cutsem; Thierry Ponchon

doi:10.1055/a-0831-2522

Endoscopy, Table of Contents

Endoscopy 2019; 51(03): 266-277
DOI: 10.1055/a-0831-2522

Guideline

Endoscopic surveillance after surgical or endoscopic resection for colorectal cancer: European Society of Gastrointestinal Endoscopy (ESGE) and European Society of Digestive Oncology (ESDO) Guideline

Cesare Hassan

¹Gastroenterology Unit, Nuovo Regina Margherita Hospital, Rome, Italy

,

Piotr Tomasz Wysocki

²Maria Sklodowska-Curie Memorial Cancer Centre and Institute of Oncology, Warsaw, Poland

,

Lorenzo Fuccio

³Department of Medical and Surgical Sciences, S. Orsola-Malpighi Hospital, University of Bologna, Bologna, Italy

,

Thomas Seufferlein

⁴Department of Internal Medicine I, Ulm University Hospital, Ulm, Germany

,

Mário Dinis-Ribeiro

⁵CIDES/CINTESIS, Faculty of Medicine, University of Porto, Porto, Portugal

,

Catarina Brandão

⁵CIDES/CINTESIS, Faculty of Medicine, University of Porto, Porto, Portugal

,

Jaroslaw Regula

⁶Medical Centre for Postgraduate Education, Maria Sklodowska-Curie Memorial Cancer Centre and Institute of Oncology, Warsaw, Poland

,

Leonardo Frazzoni

³Department of Medical and Surgical Sciences, S. Orsola-Malpighi Hospital, University of Bologna, Bologna, Italy

,

Maria Pellise

⁷Gastroenterology Department, Endoscopy Unit, ICMDiM, Hospital Clinic, CIBEREHD, IDIBAPS, University of Barcelona, Catalonia, Spain

,

Sergio Alfieri

⁸Fondazione Policlinico A. Gemelli, IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy

,

Evelien Dekker

⁹Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands;

,

Rodrigo Jover

¹⁰Service of Digestive Medicine, Alicante Institute for Health and Biomedical Research (ISABIAL-FISABIO Foundation), Alicante, Spain

,

Gerardo Rosati

¹¹Medical Oncology Unit, S. Carlo Hospital, Potenza, Italy

,

Carlo Senore

¹²Azienda Ospedaliero Universitaria Cittá della Salute e della Scienza Centro per l'Epidemiologia e la Prevenzione Oncologica in Piemonte, Turin, Italy

,

Cristiano Spada

¹³Digestive Endoscopy Unit, Fondazione Poliambulanza, Brescia, Italy

,

Ian Gralnek

¹⁴Institute of Gastroenterology, Hepatology and Nutrition, Emek Medical Center, Afula, Israel

,

Jean-Marc Dumonceau

¹⁵Gedyt Endoscopy Center, Buenos Aires, Argentina

,

Jeanin E. van Hooft

⁹Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands;

,

Eric van Cutsem

¹⁶University Hospitals Gasthuisberg, Leuven, Belgium

,

Thierry Ponchon

¹⁷Gastroenterology and Endoscopy, Edouard Herriot Hospital, Lyon, France

› Author Affiliations

Abstract

Main Recommendations

1 We recommend post-surgery endoscopic surveillance for CRC patients after intent-to-cure surgery and appropriate oncological treatment for both local and distant disease.
Strong recommendation, low quality evidence.

2 We recommend a high quality perioperative colonoscopy before surgery for CRC or within 6 months following surgery.
Strong recommendation, low quality evidence.

3 We recommend performing surveillance colonoscopy 1 year after CRC surgery.
Strong recommendation, moderate quality evidence.

4 We do not recommend an intensive endoscopic surveillance strategy, e. g. annual colonoscopy, because of a lack of proven benefit.
Strong recommendation, moderate quality evidence.

5 After the first surveillance colonoscopy following CRC surgery, we suggest the second colonoscopy should be performed 3 years later, and the third 5 years after the second. If additional high risk neoplastic lesions are detected, subsequent surveillance examinations at shorter intervals may be considered.
Weak recommendation, low quality evidence.

6 After the initial surveillance colonoscopy, we suggest halting post-surgery endoscopic surveillance at the age of 80 years, or earlier if life-expectancy is thought to be limited by comorbidities.
Weak recommendation, low quality evidence.

7 In patients with a low risk pT1 CRC treated by endoscopy with an R0 resection, we suggest the same endoscopic surveillance schedule as for any CRC.
Weak recommendation, low quality evidence.

Full Text

References

References
1 Torre LA, Bray F, Siegel RL. et al. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65: 87-108
2 van der Stok EP, Spaander MCW, Grünhagen DJ. et al. Surveillance after curative treatment for colorectal cancer. Nat Rev Clin Oncol 2016; 14: 297
3 Levin TR, Corley DA, Jensen CD. et al. Effects of organized colorectal cancer screening on cancer incidence and mortality in a large, community-based population. Gastroenterology 2018; 155: 1383-1391.e5
4 Logan RF, Patnick J, Nickerson C. et al. Outcomes of the bowel cancer screening programme (BCSP) in England after the first 1 million tests. Gut 2012; 61: 1439-1446
5 Williams JG, Pullan RD, Hill J. et al. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013; 15 (Suppl. 02) 1-38
6 Richardson WS, Wilson MC, Nishikawa J. et al. The well-built clinical question: A key to evidence-based decisions. ACP J Club 1995; 123: A12-A13
7 Atkins D, Best D, Briss PA. et al. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 1490
8 Spada C, Stoker J, Alarcon O. et al. Clinical indications for computed tomographic colonography: European Society of Gastrointestinal Endoscopy (ESGE) and European Society of Gastrointestinal and Abdominal Radiology (ESGAR) Guideline. Endoscopy 2014; 46: 897-915
9 Kaminski MF, Thomas-Gibson S, Bugajski M. et al. Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) quality improvement initiative. United European Gastroenterol J 2017; 5: 309-334
10 Dumonceau JM, Hassan C, Riphaus A. et al. European Society of Gastrointestinal Endoscopy (ESGE) Guideline Development Policy. Endoscopy 2012; 44: 626-629
11 Rosati G, Ambrosini G, Barni S. et al. A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2-C colorectal carcinoma. Ann Oncol 2016; 27: 274-280
12 Rodriguez-Moranta F, Salo J, Arcusa A. et al. Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial. J Clin Oncol 2006; 24: 386-393
13 Schoemaker D, Black R, Giles L. et al. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology 1998; 114: 7-14
14 Makela JT, Laitinen SO, Kairaluoma MI. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch Surg 1995; 130: 1062-1067
15 Secco GB, Fardelli R, Gianquinto D. et al. Efficacy and cost of risk-adapted follow-up in patients after colorectal cancer surgery: a prospective, randomized and controlled trial. Eur J Surg Oncol 2002; 28: 418-423
16 Wattchow DA, Weller DP, Esterman A. et al. General practice vs surgical-based follow-up for patients with colon cancer: randomised controlled trial. Br J Cancer 2006; 94: 1116-1121
17 Grossmann EM, Johnson FE, Virgo KS. et al. Follow-up of colorectal cancer patients after resection with curative intent-the GILDA trial. Surg Oncol 2004; 13: 119-124
18 Pietra N, Sarli L, Costi R. et al. Role of follow-up in management of local recurrences of colorectal cancer: a prospective, randomized study. Dis Colon Rectum 1998; 41: 1127-1133
19 Mokhles S, Macbeth F, Farewell V. et al. Meta-analysis of colorectal cancer follow-up after potentially curative resection. Br J Surg 2016; 103: 1259-1268
20 Jeffery M, Hickey BE, Hider PN. et al. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst Rev 2016; 11: Cd002200
21 Pita-Fernandez S, Alhayek-Ai M, Gonzalez-Martin C. et al. Intensive follow-up strategies improve outcomes in nonmetastatic colorectal cancer patients after curative surgery: a systematic review and meta-analysis. Ann Oncol 2015; 26: 644-656
22 Tjandra JJ, Chan MK. Follow-up after curative resection of colorectal cancer: a meta-analysis. Dis Colon Rectum 2007; 50: 1783-1799
23 Wang T, Cui Y, Huang WS. et al. The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study. Gastrointest Endosc 2009; 69: 609-615
24 Choe EK, Park KJ, Chung SJ. et al. Colonoscopic surveillance after colorectal cancer resection: who needs more intensive follow-up?. Digestion 2015; 91: 142-149
25 Platell C, Salama P, Barwood N. et al. Performing a colonoscopy 12 months after surgery for colorectal neoplasia. ANZ J Surg 2005; 75: 282-285
26 Barrier A, Houry S, Huguier M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J Colorectal Dis 1998; 13: 93-98
27 Barillari P, Ramacciato G, Manetti G. et al. Surveillance of colorectal cancer: effectiveness of early detection of intraluminal recurrences on prognosis and survival of patients treated for cure. Dis Colon Rectum 1996; 39: 388-393
28 Lautenbach E, Forde KA, Neugut AI. Benefits of colonoscopic surveillance after curative resection of colorectal cancer. Ann Surg 1994; 220: 206-211
29 Moon CM, Cheon JH, Choi EH. et al. Advanced synchronous adenoma but not simple adenoma predicts the future development of metachronous neoplasia in patients with resected colorectal cancer. J Clin Gastroenterol 2010; 44: 495-501
30 Gresham G, Renouf DJ, Chan M. et al. Association between palliative resection of the primary tumor and overall survival in a population-based cohort of metastatic colorectal cancer patients. Ann Surg Oncol 2014; 21: 3917-3923
31 ʼt Lam-Boer J, Van der Geest LG, Verhoef C. et al. Palliative resection of the primary tumor is associated with improved overall survival in incurable stage IV colorectal cancer: A nationwide population-based propensity-score adjusted study in the Netherlands. Int J Cancer 2016; 139: 2082-2094
32 Mulder SA, Kranse R, Damhuis RA. et al. The incidence and risk factors of metachronous colorectal cancer: an indication for follow-up. Dis Colon Rectum 2012; 55: 522-531
33 Green RJ, Metlay JP, Propert K. et al. Surveillance for second primary colorectal cancer after adjuvant chemotherapy: an analysis of Intergroup 0089. Ann Intern Med 2002; 136: 261-269
34 le Clercq CM, Winkens B, Bakker CM. et al. Metachronous colorectal cancers result from missed lesions and non-compliance with surveillance. Gastrointest Endosc 2015; 82: 325-333.e322
35 Liu L, Lemmens VE, De Hingh IH. et al. Second primary cancers in subsites of colon and rectum in patients with previous colorectal cancer. Dis Colon Rectum 2013; 56: 158-168
36 Chen TA, Horng JT, Lin WC. Metachronous colorectal cancer in Taiwan: analyzing 20 years of data from Taiwan Cancer Registry. Int J Clin Oncol 2013; 18: 267-272
37 Couch DG, Bullen N, Ward-Booth SE. et al. What interval between colorectal cancer resection and first surveillance colonoscopy? An audit of practice and yield. Colorectal Dis 2013; 15: 317-322
38 Chung YW, Han DS, Park KH. et al. Patient factors predictive of inadequate bowel preparation using polyethylene glycol: a prospective study in Korea. J Clin Gastroenterol 2009; 43: 448-452
39 Hassan C, Fuccio L, Bruno M. et al. A predictive model identifies patients most likely to have inadequate bowel preparation for colonoscopy. Clin Gastroenterol Hepatol 2012; 10: 501-506
40 Lim SW, Seo YW, Sinn DH. et al. Impact of previous gastric or colonic resection on polyethylene glycol bowel preparation for colonoscopy. Surg Endosc 2012; 26: 1554-1559
41 Pontone S, Leonetti G, Lamazza A. et al. A retrospective case-control study evaluating the bowel preparation quality during surveillance colonoscopy after colonic resection. ISRN Gastroenterol 2014; 2014: 681978
42 Pinol V, Andreu M, Castells A. et al. Synchronous colorectal neoplasms in patients with colorectal cancer: predisposing individual and familial factors. Dis Colon Rectum 2004; 47: 1192-1200
43 Mulder SA, Kranse R, Damhuis RA. et al. Prevalence and prognosis of synchronous colorectal cancer: a Dutch population-based study. Cancer Epidemiol 2011; 35: 442-447
44 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. NEJM 2010; 362: 1795-1803
45 Rex DK, Bond JH, Winawer S. et al. Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 2002; 97: 1296-1308
46 Rex DK, Petrini JL, Baron TH. et al. Quality indicators for colonoscopy. Am J Gastroenterol 2006; 101: 873-885
47 Barclay RL, Vicari JJ, Doughty AS. et al. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. NEJM 2006; 355: 2533-2541
48 Rex DK. Colonoscopic withdrawal technique is associated with adenoma miss rates. Gastrointest Endosc 2000; 51: 33-36
49 Cooper GS, Xu F, Barnholtz Sloan JS. et al. Prevalence and predictors of interval colorectal cancers in medicare beneficiaries. Cancer 2012; 118: 3044-3052
50 Kaminski MF, Wieszczy P, Rupinski M. et al. Increased rate of adenoma detection associates with reduced risk of colorectal cancer and death. Gastroenterology 2017; 153: 98-105
51 Lee RH, Tang RS, Muthusamy VR. et al. Quality of colonoscopy withdrawal technique and variability in adenoma detection rates (with videos). Gastrointest Endosc 2011; 74: 128-134
52 Shaukat A, Rector TS, Church TR. et al. Longer withdrawal time is associated with a reduced incidence of interval cancer after screening colonoscopy. Gastroenterology 2015; 149: 952-957
53 Atkin W, Wooldrage K, Brenner A. et al. Adenoma surveillance and colorectal cancer incidence: a retrospective, multicentre, cohort study. Lancet Oncol 2017; 18: 823-834
54 Rutter MD, Senore C, Bisschops R. et al. The European Society of Gastrointestinal Endoscopy Quality Improvement Initiative: developing performance measures. United European Gastroenterol J 2016; 4: 30-41
55 Mussetto A, Frazzoni L, Paggi S. et al. Split dosing with a low-volume preparation is not inferior to split dosing with a high-volume preparation for bowel cleansing in patients with a history of colorectal resection: a randomized trial. Endoscopy 2015; 47: 917-924
56 Carballal S, Maisterra S, Lopez-Serrano A. et al. Real-life chromoendoscopy for neoplasia detection and characterisation in long-standing IBD. Gut 2018; 67: 70-77
57 Rahmi G, Lecomte T, Malka D. et al. Impact of chromoscopy on adenoma detection in patients with Lynch syndrome: a prospective, multicenter, blinded, tandem colonoscopy study. Am J Gastroenterol 2015; 110: 288-298
58 Bouvier AM, Latournerie M, Jooste V. et al. The lifelong risk of metachronous colorectal cancer justifies long-term colonoscopic follow-up. Eur J Cancer 2008; 44: 522-527
59 Loberg M, Kalager M, Holme O. et al. Long-term colorectal-cancer mortality after adenoma removal. NEJM 2014; 371: 799-807
60 Lee SY, Kim BC, Han KS. et al. Incidence and risk factors of metachronous colorectal neoplasm after curative resection of colorectal cancer in Korean patients. J Dig Dis 2014; 15: 367-376
61 Patel A, Williams N, Parsons N. et al. Risk factors for metachronous adenoma in the residual colon of patients undergoing curative surgery for colorectal cancer. Int J Colorectal Dis 2017; 32: 1609-1616
62 Fuccio L, Rex D, Ponchon T. et al. New and recurrent colorectal cancers after resection: a systematic review and meta-analysis of endoscopic surveillance studies. Gastroenterology 2018;
63 Hyman N, Moore J, Cataldo P. et al. The high yield of 1-year colonoscopy after resection: is it the handoff?. Surg Endosc 2010; 24: 648-652
64 Rulyak SJ, Lieberman DA, Wagner EH. et al. Outcome of follow-up colon examination among a population-based cohort of colorectal cancer patients. Clin Gastroenterol Hepatol 2007; 5: 470-476 ; quiz 407
65 Lan YT, Lin JK, Li AF. et al. Metachronous colorectal cancer: necessity of post-operative colonoscopic surveillance. Int J Colorectal Dis 2005; 20: 121-125
66 Battersby NJ, Coupland A, Bouliotis G. et al. Metachronous colorectal cancer: a competing risks analysis with consideration for a stratified approach to surveillance colonoscopy. J Surg Oncol 2014; 109: 445-450
67 Cone MM, Beck DE, Hicks TE. et al. Timing of colonoscopy after resection for colorectal cancer: are we looking too soon?. Dis Colon Rectum 2013; 56: 1233-1236
68 Fuccio L, Spada C, Frazzoni L. et al. Higher adenoma recurrence rate after left- versus right-sided colectomy for colon cancer. Gastrointest Endosc 2015; 82: 337-343
69 McFall MR, Woods WG, Miles WF. Colonoscopic surveillance after curative colorectal resection: results of an empirical surveillance programme. Colorectal Dis 2003; 5: 233-240
70 Rajaratnam SG, Dennett ER. Development of metachronous neoplasms after colorectal cancer resection: absence of synchronous neoplasms predicts a lower risk. N Z Med J 2009; 122: 61-66
71 Sakamoto T, Matsuda T, Nakajima T. et al. How often should we perform surveillance colonoscopy after surgery for colorectal cancer?. Int J Colorectal Dis 2013; 28: 835-840
72 Jayasekara H, Reece JC, Buchanan DD. et al. Risk factors for metachronous colorectal cancer following a primary colorectal cancer: A prospective cohort study. Int J Cancer 2016; 139: 1081-1090
73 Gervaz P, Bucher P, Neyroud-Caspar I. et al. Proximal location of colon cancer is a risk factor for development of metachronous colorectal cancer: a population-based study. Dis Colon Rectum 2005; 48: 227-232
74 Marques-Antunes J, Libanio D, Goncalves P. et al. Incidence and predictors of adenoma after surgery for colorectal cancer. Eur J Gastroenterol Hepatol 2017; 29: 932-938
75 Borda A, Martinez-Penuela JM, Borda F. et al. Drawing up an individual risk index for development of metachronous neoplastic lesions in resected colorectal cancer. Rev Esp Enferm Dig 2012; 104: 291-297
76 Hollington P, Tiong L, Young G. Timing and detection of metachronous colorectal cancer. ANZ J Surg 2011; 81: 272-274
77 Kjeldsen B, Kronborg O, Fenger C. et al. A prospective randomized study of follow‐up after radical surgery for colorectal cancer. Br J Surg 1997; 84: 666-669
78 Park IJ, Yu CS, Kim HC. et al. Metachronous colorectal cancer. Colorectal Dis 2006; 8: 323-327
79 Chen HS, Sheen-Chen SM. Synchronous and “early” metachronous colorectal adenocarcinoma: analysis of prognosis and current trends. Dis Colon Rectum 2000; 43: 1093-1099
80 Chen F, Stuart M. Colonoscopic follow-up of colorectal carcinoma. Dis Colon Rectum 1994; 37: 568-572
81 Granqvist S, Karlsson T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur J Surg 1992; 158: 307-312
82 Juhl G, Larson GM, Mullins R. et al. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg 1990; 14: 255-260 ; discussion 260 – 251
83 Togashi K, Konishi F, Ozawa A. et al. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis Colon Rectum 2000; 43: S47-S53
84 Kahi CJ, Boland CR, Dominitz JA. et al. Colonoscopy surveillance after colorectal cancer resection: recommendations of the US Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 2016; 111: 337-346 ; quiz 347
85 Fajobi O, Yiu CY, Sen-Gupta SB. et al. Metachronous colorectal cancers. Br J Surg 1998; 85: 897-901
86 Papadopoulos V, Michalopoulos A, Basdanis G. et al. Synchronous and metachronous colorectal carcinoma. Tech Coloproctol 2004; 8 (Suppl. 01) s97-s100
87 Hassan C, Pickhardt PJ, Zullo A. et al. Cost-effectiveness of early colonoscopy surveillance after cancer resection. Dig Liver Dis 2009; 41: 881-885
88 Hojo K. Anastomotic recurrence after sphincter-saving resection for rectal cancer. Length of distal clearance of the bowel. Dis Colon Rectum 1986; 29: 11-14
89 Jung WB, Yu CS, Lim SB. et al. Anastomotic Recurrence After Curative Resection for Colorectal Cancer. World J Surg 2017; 41: 285-294
90 Matsuda K, Hotta T, Takifuji K. et al. Clinicopathological features of anastomotic recurrence after an anterior resection for rectal cancer. Langenbecks Arch Surg 2010; 395: 235-239
91 Obrand DI, Gordon PH. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis Colon Rectum 1997; 40: 15-24
92 de Chaisemartin C, Penna C, Goere D. et al. Presentation and prognosis of local recurrence after total mesorectal excision. Colorectal Dis 2009; 11: 60-66
93 McDermott FT, Hughes ES, Pihl E. et al. Local recurrence after potentially curative resection for rectal cancer in a series of 1008 patients. Br J Surg 1985; 72: 34-37
94 Patel SA, Chen YH, Hornick JL. et al. Early-stage rectal cancer: clinical and pathologic prognostic markers of time to local recurrence and overall survival after resection. Dis Colon Rectum 2014; 57: 449-459
95 Kim Y-W, Kim N-K, Min B-S. et al. Factors associated with anastomotic recurrence after total mesorectal excision in rectal cancer patients. J Surg Oncol 2009; 99: 58-64
96 Kang DW, Kwak HD, Sung NS. et al. Oncologic outcomes in rectal cancer patients with a ≤ 1-cm distal resection margin. Int J Colorectal Dis 2017; 32: 325-332
97 Stulc JP, Petrelli NJ, Herrera L. et al. Anastomotic recurrence of adenocarcinoma of the colon. Arch Surg 1986; 121: 1077-1080
98 Pihl E, Hughes ES, McDermott FT. et al. Recurrence of carcinoma of the colon and rectum at the anastomotic suture line. Surg Gynecol Obstet 1981; 153: 495-496
99 Harris GJ, Church JM, Senagore AJ. et al. Factors affecting local recurrence of colonic adenocarcinoma. Dis Colon Rectum 2002; 45: 1029-1034
100 Bowne WB, Lee B, Wong WD. et al. Operative salvage for locoregional recurrent colon cancer after curative resection: an analysis of 100 cases. Dis Colon Rectum 2005; 48: 897-909
101 Nash GM, Weiss A, Dasgupta R. et al. Close distal margin and rectal cancer recurrence after sphincter-preserving rectal resection. Dis Colon Rectum 2010; 53: 1365-1373
102 Hogan J, Chang KH, Duff G. et al. Lymphovascular invasion: a comprehensive appraisal in colon and rectal adenocarcinoma. Dis Colon Rectum 2015; 58: 547-555
103 Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer?. J Clin Oncol 2008; 26: 303-312
104 Adam IJ, Mohamdee MO, Martin IG. et al. Role of circumferential margin involvement in the local recurrence of rectal cancer. Lancet 1994; 344: 707-711
105 Matsuda A, Kishi T, Musso G. et al. The effect of intraoperative rectal washout on local recurrence after rectal cancer surgery: a meta-analysis. Ann Surg Oncol 2013; 20: 856-863
106 Zhou C, Ren Y, Wang K. et al. Intra-operative rectal washout with saline solution can effectively prevent anastomotic recurrence: a meta-analysis. Asian Pac J Cancer Prev 2013; 14: 7155-7159
107 Terzi C, Unek T, Sagol O. et al. Is rectal washout necessary in anterior resection for rectal cancer? A prospective clinical study. World J Surg 2006; 30: 233-241
108 Docherty JG, McGregor JR, Akyol AM. et al. Comparison of manually constructed and stapled anastomoses in colorectal surgery. West of Scotland and Highland Anastomosis Study Group. Ann Surg 1995; 221: 176-184
109 van den Brink M, Stiggelbout AM, van den Hout WB. et al. Clinical nature and prognosis of locally recurrent rectal cancer after total mesorectal excision with or without preoperative radiotherapy. J Clin Oncol 2004; 22: 3958-3964
110 Ohlsson B, Breland U, Ekberg H. et al. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis Colon Rectum 1995; 38: 619-626
111 Figueredo A, Rumble RB, Maroun J. et al. Follow-up of patients with curatively resected colorectal cancer: a practice guideline. BMC Cancer 2003; 3: 26
112 Renehan AG, Egger M, Saunders MP. et al. Mechanisms of improved survival from intensive followup in colorectal cancer: a hypothesis. Br J Cancer 2005; 92: 430-433
113 Snyder RA, Hu C, Cuddy A. et al. Association between intensity of posttreatment surveillance testing and detection of recurrence in patients with colorectal cancer. JAMA 2018; 319: 2104-2115
114 Wille-Jørgensen P, Syk I, Smedh K. et al. Effect of more vs less frequent follow-up testing on overall and colorectal cancer–specific mortality in patients with stage ii or iii colorectal cancer: The colofol randomized clinical trial. JAMA 2018; 319: 2095-2103
115 Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin 2018; 68: 7-30
116 Cubiella J, Gomez R, Sanchez E. et al. Endoscopic follow-up of patients after curative surgery for colorectal cancer: results of a medical assistance protocol. Rev Esp Enferm Dig 2003; 95: 273-281
117 Yun GY, Moon HS, Kwon IS. et al. Left-sided colectomy: one of the important risk factors of metachronous colorectal adenoma after colectomy for colon cancer. Dig Dis Sci 2018; 63: 1052-1061
118 Matsuda T, Fujii T, Sano Y. et al. Five-year incidence of advanced neoplasia after initial colonoscopy in Japan: a multicenter retrospective cohort study. Jpn J Clin Oncol 2009; 39: 435-442
119 Yoshida N, Naito Y, Siah KT. et al. High incidence of metachronous advanced adenoma and cancer after endoscopic resection of colon polyps >/=20 mm in size. Dig Endosc 2016; 28: 194-202
120 Kim NH, Jung YS, Park JH. et al. Risk of developing metachronous advanced colorectal neoplasia after colonoscopic polypectomy in patients aged 30 to 39 and 40 to 49 years. Gastrointest Endosc 2018; 88: 715-772
121 Hassan C, Quintero E, Dumonceau JM. et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2013; 45: 842-851
122 Yazdanyar A, Newman AB. The burden of cardiovascular disease in the elderly: morbidity, mortality, and costs. Clin Geriatr Med 2009; 25: 563-577
123 Labianca R, Nordlinger B, Beretta GD. et al. Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013; 24 (Suppl. 06) vi64-vi72
124 Watanabe T, Muro K, Ajioka Y. et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 2018; 23: 1-34
125 Benson 3rd AB, Venook AP, Al-Hawary MM. et al. Rectal cancer, Version 2.2018, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Cancer Netw 2018; 16: 874-901
126 Quirke P, Risio M, Lambert R. et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First Edition--Quality assurance in pathology in colorectal cancer screening and diagnosis. Endoscopy 2012; 44 (Suppl. 03) Se116-Se130
127 Poston GJ, Tait D, O’Connell S. et al. Diagnosis and management of colorectal cancer: summary of NICE guidance. BMJ 2011; 343: d6751
128 Ikematsu H, Yoda Y, Matsuda T. et al. Long-term outcomes after resection for submucosal invasive colorectal cancers. Gastroenterology 2013; 144: 551-559 ; quiz e514
129 Yoshii S, Nojima M, Nosho K. et al. Factors associated with risk for colorectal cancer recurrence after endoscopic resection of T1 tumors. Clin Gastroenterol Hepatol 2014; 12: 292-302.e293
130 Backes Y, de Vos Tot Nederveen Cappel WH, van Bergeijk J. et al. Risk for incomplete resection after macroscopic radical endoscopic resection of t1 colorectal cancer: a multicenter cohort study. Am J Gastroenterol 2017; 112: 785-796
131 Eckardt VF, Fuchs M, Kanzler G. et al. Follow-up of patients with colonic polyps containing severe atypia and invasive carcinoma. Compliance, recurrence, and survival. Cancer 1988; 61: 2552-2557

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Supplementary material