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  • Review Article
  • Published:

Surveillance after curative treatment for colorectal cancer

Key Points

  • Pooled analyses of prospective trials have demonstrated an overall survival benefit of intensive postoperative surveillance in patients with stage I–III colorectal cancer (CRC); however, individual studies used highly heterogeneous surveillance schemes

  • The overall survival benefit of intensive surveillance is only partly due to improved cancer-specific survival; other contributing factors include the treatment of comorbidities owing to frequent contact with medical professionals

  • For patients with stage I–III CRC, no optimal diagnostic tool or frequency of patient visits has been established; regular follow-up assessment by a clinician seem to be the most-important factor

  • Colonoscopies are generally performed at 6, 30 and 60 months after curative treatment of patients with stage I–III CRC; performing additional colonoscopies does not improve overall survival

  • Limited evidence is available regarding surveillance after endoscopic resection of early neoplasia, and after organ-sparing treatment for rectal cancer; prospective randomized trials are needed

  • Similarly, a lack of evidence exists on the effectiveness of surveillance after treatment of patients with stage IV CRC with curative intent, and thus randomized trials are also needed to address this issue

Abstract

Treatments for colorectal cancer (CRC) of all stages have evolved considerably over the past two decades, resulting in improved long-term outcomes. After curative treatment, however, 30% of patients with stage I–III and up to 65% of patients with stage IV CRC develop recurrent disease. Thus, patients are routinely offered surveillance in order to detect disease recurrence at an early, asymptomatic stage, with the intention of improving survival. Nevertheless, controversy continues to surround the optimal surveillance protocols. For patients with stage I–III CRC, more-intensive surveillance improves overall survival compared with less-intensive or no surveillance, probably owing to improved outcomes after cancer recurrence, as well as proactive treatment of other conditions detected opportunistically. The benefit of surveillance after curative treatment of stage IV CRC is more controversial, but might be justified because repeat resection can improve overall survival and 20% of these patients are eligible for such treatment with curative intent. No trials have assessed the optimal follow-up approach after curative resection of metastatic CRC, and similarly to surveillance of patients with stage I–III disease, most programmes are more intensive during the first 3 years than at later time points. Herein, we provide a comprehensive overview of surveillance strategies for patients with CRC, and discuss the future development of patient-centred programmes.

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Figure 1: CT imaging surveillance for the diagnosis of colorectal liver metastases.
Figure 2: PET–CT imaging surveillance for the diagnosis of pulmonary metastases.
Figure 3: Resection of colorectal liver metastases.

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References

  1. Kuipers, E. J. et al. Colorectal cancer. Nat. Rev. Dis. Primers 1, 15065 (2015).

    PubMed  PubMed Central  Google Scholar 

  2. Torre, L. A. et al. Global cancer statistics, 2012. CA Cancer J. Clin. 65, 87–108 (2015).

    Article  PubMed  Google Scholar 

  3. Elferink, M. A. et al. Marked improvements in survival of patients with rectal cancer in the Netherlands following changes in therapy, 1989–2006. Eur. J. Cancer 46, 1421–1429 (2010).

    CAS  PubMed  Google Scholar 

  4. van der Pool, A. E. et al. Trends in incidence, treatment and survival of patients with stage IV colorectal cancer: a population-based series. Colorectal Dis. 14, 56–61 (2012).

    CAS  PubMed  Google Scholar 

  5. van Steenbergen, L. N. et al. Improved survival of colon cancer due to improved treatment and detection: a nationwide population-based study in the Netherlands 1989–2006. Ann. Oncol. 21, 2206–2212 (2010).

    CAS  PubMed  Google Scholar 

  6. Schreuders, E. H. et al. Colorectal cancer screening: a global overview of existing programmes. Gut 64, 1637–1649 (2015).

    PubMed  Google Scholar 

  7. Kuipers, E. J., Rosch, T. & Bretthauer, M. Colorectal cancer screening — optimizing current strategies and new directions. Nat. Rev. Clin. Oncol. 10, 130–142 (2013).

    CAS  PubMed  Google Scholar 

  8. Pita-Fernández, S. et al. Intensive follow-up strategies improve outcomes in nonmetastatic colorectal cancer patients after curative surgery: a systematic review and meta-analysis. Ann. Oncol. 26, 644–656 (2015).

    PubMed  Google Scholar 

  9. Rose, J., Augestad, K. M. & Cooper, G. S. Colorectal cancer surveillance: what's new and what's next. World J. Gastroenterol. 20, 1887–1897 (2014).

    PubMed  PubMed Central  Google Scholar 

  10. de Jong, M. C. et al. Rates and patterns of recurrence following curative intent surgery for colorectal liver metastasis: an international multi-institutional analysis of 1669 patients. Ann. Surg. 250, 440–448 (2009).

    PubMed  Google Scholar 

  11. Elias, D. et al. Peritoneal colorectal carcinomatosis treated with surgery and perioperative intraperitoneal chemotherapy: retrospective analysis of 523 patients from a multicentric French study. J. Clin. Oncol. 28, 63–68 (2010).

    PubMed  Google Scholar 

  12. Glehen, O. et al. Cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for the management of peritoneal carcinomatosis from colorectal cancer: a multi-institutional study. J. Clin. Oncol. 22, 3284–3292 (2004).

    CAS  PubMed  Google Scholar 

  13. Jones, R. P. et al. Systematic review and meta-analysis of follow-up after hepatectomy for colorectal liver metastases. Br. J. Surg. 99, 477–486 (2012).

    CAS  PubMed  Google Scholar 

  14. Pfannschmidt, J., Dienemann, H. & Hoffmann, H. Surgical resection of pulmonary metastases from colorectal cancer: a systematic review of published series. Ann. Thorac. Surg. 84, 324–338 (2007).

    PubMed  Google Scholar 

  15. Verwaal, V. J. et al. Randomized trial of cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy and palliative surgery in patients with peritoneal carcinomatosis of colorectal cancer. J. Clin. Oncol. 21, 3737–3743 (2003).

    PubMed  Google Scholar 

  16. Warwick, R. & Page, R. Resection of pulmonary metastases from colorectal carcinoma. Eur. J. Surg. Oncol. 33 (Suppl. 2), S59–S63 (2007).

    PubMed  Google Scholar 

  17. Winawer, S. J. et al. Prevention of colorectal cancer by colonoscopic polypectomy. N. Engl. J. Med. 329, 1977–1981 (1993).

    CAS  PubMed  Google Scholar 

  18. Bhangu, A. et al. Meta-analysis of survival based on resection margin status following surgery for recurrent rectal cancer. Colorectal Dis. 14, 1457–1466 (2012).

    CAS  PubMed  Google Scholar 

  19. Chua, T. C. et al. Hepatectomy and resection of concomitant extrahepatic disease for colorectal liver metastases — a systematic review. Eur. J. Cancer 48, 1757–1765 (2012).

    PubMed  Google Scholar 

  20. Dresen, R. C. et al. Radical resection after IORT-containing multimodality treatment is the most important determinant for outcome in patients treated for locally recurrent rectal cancer. Ann. Surg. Oncol. 15, 1937–1947 (2008).

    PubMed  PubMed Central  Google Scholar 

  21. Kanas, G. P. et al. Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors. Clin. Epidemiol. 4, 283–301 (2012).

    PubMed  PubMed Central  Google Scholar 

  22. Rees, M. et al. Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann. Surg. 247, 125–135 (2008).

    PubMed  Google Scholar 

  23. Cali, R. L. et al. Cumulative incidence of metachronous colorectal cancer. Dis. Colon Rectum 36, 388–393 (1993).

    CAS  PubMed  Google Scholar 

  24. Green, R. J. et al. Surveillance for second primary colorectal cancer after adjuvant chemotherapy: an analysis of Intergroup 0089. Ann. Intern. Med. 136, 261–269 (2002).

    CAS  PubMed  Google Scholar 

  25. Hohenberger, W. et al. Standardized surgery for colonic cancer: complete mesocolic excision and central ligation — technical notes and outcome. Colorectal Dis. 11, 354–364 (2009).

    CAS  PubMed  Google Scholar 

  26. Kapiteijn, E. et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N. Engl. J. Med. 345, 638–646 (2001).

    CAS  PubMed  Google Scholar 

  27. Mulder, S. A. et al. The incidence and risk factors of metachronous colorectal cancer: an indication for follow-up. Dis. Colon Rectum 55, 522–531 (2012).

    PubMed  Google Scholar 

  28. Obrand, D. I. & Gordon, P. H. Incidence and patterns of recurrence following curative resection for colorectal carcinoma. Dis. Colon Rectum 40, 15–24 (1997).

    CAS  PubMed  Google Scholar 

  29. Peeters, K. C. et al. The TME trial after a median follow-up of 6 years: increased local control but no survival benefit in irradiated patients with resectable rectal carcinoma. Ann. Surg. 246, 693–701 (2007).

    PubMed  Google Scholar 

  30. Ringland, C. L. et al. Second primary colorectal cancers (SPCRCs): experiences from a large Australian Cancer Registry. Ann. Oncol. 21, 92–97 (2010).

    CAS  PubMed  Google Scholar 

  31. Pickhardt, P. J. et al. Colorectal cancer: CT colonography and colonoscopy for detection — systematic review and meta-analysis. Radiology 259, 393–405 (2011).

    PubMed  PubMed Central  Google Scholar 

  32. Labianca, R. et al. Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 24 (Suppl. 6), vi64–vi72 (2013).

    PubMed  Google Scholar 

  33. Meyerhardt, J. A. et al. Follow-up care, surveillance protocol, and secondary prevention measures for survivors of colorectal cancer: American Society of Clinical Oncology clinical practice guideline endorsement. J. Clin. Oncol. 31, 4465–4470 (2013).

    PubMed  Google Scholar 

  34. National Comprehensive Cancer Network. Guidelines for treatment of colorectal cancer. NCCN https://www.nccn.org/professionals/physician_gls/f_guidelines.asp#site (2016).

  35. National Institute for Health and Care Excellence. Colorectal cancer: diagnosis and management. NICE http://www.nice.org.uk/Guidance/CG131 (updated 2014).

  36. Steele, S. R. et al. Practice guideline for the surveillance of patients after curative treatment of colon and rectal cancer. Dis. Colon Rectum 58, 713–725 (2015).

    PubMed  Google Scholar 

  37. Van Cutsem, E. et al. Metastatic colorectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 25 (Suppl. 3), iii1–iii9 (2014).

    PubMed  Google Scholar 

  38. Barillari, P. 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 39, 388–393 (1996).

    CAS  PubMed  Google Scholar 

  39. Chen, F. & Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis. Colon Rectum 37, 568–572 (1994).

    CAS  PubMed  Google Scholar 

  40. Granqvist, S. & Karlsson, T. Postoperative follow-up of patients with colorectal carcinoma by colonoscopy. Eur. J. Surg. 158, 307–312 (1992).

    CAS  PubMed  Google Scholar 

  41. Grobbee, E. J. et al. Second-look colonoscopies and the impact on capacity in FIT-based colorectal cancer screening. Am. J. Gastroenterol. 110, 1072–1077 (2015).

    PubMed  Google Scholar 

  42. Juhl, G. et al. Six-year results of annual colonoscopy after resection of colorectal cancer. World J. Surg. 14, 255–260 (1990).

    CAS  PubMed  Google Scholar 

  43. Kjeldsen, B. J. et al. A prospective randomized study of follow-up after radical surgery for colorectal cancer. Br. J. Surg. 84, 666–669 (1997).

    CAS  PubMed  Google Scholar 

  44. Schoemaker, D. et al. Yearly colonoscopy, liver CT, and chest radiography do not influence 5-year survival of colorectal cancer patients. Gastroenterology 114, 7–14 (1998).

    CAS  PubMed  Google Scholar 

  45. Togashi, K. et al. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis. Colon Rectum 43 (10 Suppl.), S47–S53 (2000).

    CAS  PubMed  Google Scholar 

  46. Wang, T. et al. The role of postoperative colonoscopic surveillance after radical surgery for colorectal cancer: a prospective, randomized clinical study. Gastrointest. Endosc. 69, 609–615 (2009).

    PubMed  Google Scholar 

  47. Robertson, D. J., Kaminski, M. F. & Bretthauer, M. Effectiveness, training and quality assurance of colonoscopy screening for colorectal cancer. Gut 64, 982–990 (2015).

    PubMed  Google Scholar 

  48. Kim, H. J. et al. CT colonography for combined colonic and extracolonic surveillance after curative resection of colorectal cancer. Radiology 257, 697–704 (2010).

    PubMed  Google Scholar 

  49. Amitai, M. M. et al. Contrast-enhanced CT colonography with 64-slice MDCT compared to endoscopic colonoscopy in the follow-up of patients after colorectal cancer resection. Clin. Imaging 33, 433–438 (2009).

    PubMed  Google Scholar 

  50. Fletcher, J. G. et al. Contrast-enhanced CT colonography in recurrent colorectal carcinoma: feasibility of simultaneous evaluation for metastatic disease, local recurrence, and metachronous neoplasia in colorectal carcinoma. AJR Am. J. Roentgenol. 178, 283–290 (2002).

    CAS  PubMed  Google Scholar 

  51. Laghi, A. et al. Contrast-enhanced computed tomographic colonography in the follow-up of colorectal cancer patients: a feasibility study. Eur. Radiol. 13, 883–889 (2003).

    PubMed  Google Scholar 

  52. Lee, J. H. et al. CT colonography in patients who have undergone sigmoid colostomy: a feasibility study. AJR Am. J. Roentgenol. 197, W653–W657 (2011).

    PubMed  Google Scholar 

  53. Leonardou, P. et al. Screening of patients after colectomy: virtual colonography. Abdom. Imaging 31, 521–528 (2006).

    CAS  PubMed  Google Scholar 

  54. Neri, E. et al. Post-surgical follow-up of colorectal cancer: role of contrast-enhanced CT colonography. Abdom. Imaging 35, 669–675 (2010).

    PubMed  Google Scholar 

  55. You, Y. T. et al. Evaluation of contrast-enhanced computed tomographic colonography in detection of local recurrent colorectal cancer. World J. Gastroenterol. 12, 123–126 (2006).

    PubMed  PubMed Central  Google Scholar 

  56. de Wijkerslooth, T. R. et al. Burden of colonoscopy compared to non-cathartic CT-colonography in a colorectal cancer screening programme: randomised controlled trial. Gut 61, 1552–1559 (2012).

    PubMed  Google Scholar 

  57. Dighe, S. et al. Diagnostic precision of CT in local staging of colon cancers: a meta-analysis. Clin. Radiol. 65, 708–719 (2010).

    CAS  PubMed  Google Scholar 

  58. Kievit, J. Follow-up of patients with colorectal cancer: numbers needed to test and treat. Eur. J. Cancer 38, 986–999 (2002).

    CAS  PubMed  Google Scholar 

  59. Blomqvist, L. et al. MR imaging, CT and CEA scintigraphy in the diagnosis of local recurrence of rectal carcinoma. Acta Radiol. 37, 779–784 (1996).

    CAS  PubMed  Google Scholar 

  60. Pema, P. J. et al. CT versus MRI diagnosis recurrent rectosigmoid carcinoma. J. Comput. Assist. Tomogr. 18, 256–261 (1994).

    CAS  PubMed  Google Scholar 

  61. Group, M. S. Diagnostic accuracy of preoperative magnetic resonance imaging in predicting curative resection of rectal cancer: prospective observational study. BMJ 333, 779 (2006).

    Google Scholar 

  62. Bipat, S. et al. Rectal cancer: local staging and assessment of lymph node involvement with endoluminal US, CT, and MR imaging — a meta-analysis. Radiology 232, 773–783 (2004).

    PubMed  Google Scholar 

  63. Titu, L. V. et al. Routine follow-up by magnetic resonance imaging does not improve detection of resectable local recurrences from colorectal cancer. Ann. Surg. 243, 348–352 (2006).

    PubMed  PubMed Central  Google Scholar 

  64. Glynne-Jones, R. & Hughes, R. Critical appraisal of the 'wait and see' approach in rectal cancer for clinical complete responders after chemoradiation. Br. J. Surg. 99, 897–909 (2012).

    CAS  PubMed  Google Scholar 

  65. Glynne-Jones, R. & Hughes, R. Complete response after chemoradiotherapy in rectal cancer (watch-and-wait): have we cracked the code? Clin. Oncol. (R. Coll. Radiol.) 28, 152–160 (2016).

    CAS  Google Scholar 

  66. Furukawa, H. et al. Positron emission tomography scanning is not superior to whole body multidetector helical computed tomography in the preoperative staging of colorectal cancer. Gut 55, 1007–1011 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Shin, S. S. et al. Preoperative staging of colorectal cancer: CT versus integrated FDG PET/CT. Abdom. Imaging 33, 270–277 (2008).

    PubMed  Google Scholar 

  68. Tsunoda, Y. et al. Preoperative diagnosis of lymph node metastases of colorectal cancer by FDG-PET/CT. Jpn J. Clin. Oncol. 38, 347–353 (2008).

    PubMed  Google Scholar 

  69. Huebner, R. H. et al. A meta-analysis of the literature for whole-body FDG PET detection of recurrent colorectal cancer. J. Nucl. Med. 41, 1177–1189 (2000).

    CAS  PubMed  Google Scholar 

  70. Even-Sapir, E. et al. Detection of recurrence in patients with rectal cancer: PET/CT after abdominoperineal or anterior resection. Radiology 232, 815–822 (2004).

    PubMed  Google Scholar 

  71. Sobhani, I. et al. Early detection of recurrence by 18FDG-PET in the follow-up of patients with colorectal cancer. Br. J. Cancer 98, 875–880 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Khan, K. et al. Survival outcomes in asymptomatic patients with normal conventional imaging but raised carcinoembryonic antigen levels in colorectal cancer following positron emission tomography-computed tomography imaging. Oncologist http://dx.doi.org/10.1634/theoncologist.2016-0222 (2016).

  73. Fukunaga, H. et al. Fusion image of positron emission tomography and computed tomography for the diagnosis of local recurrence of rectal cancer. Ann. Surg. Oncol. 12, 561–569 (2005).

    PubMed  Google Scholar 

  74. Engenhart, R. et al. Therapy monitoring of presacral recurrences after high-dose irradiation: value of PET, CT, CEA and pain score. Strahlenther. Onkol. 168, 203–212 (1992).

    CAS  PubMed  Google Scholar 

  75. Moore, H. G. et al. A case-controlled study of 18-fluorodeoxyglucose positron emission tomography in the detection of pelvic recurrence in previously irradiated rectal cancer patients. J. Am. Coll. Surg. 197, 22–28 (2003).

    PubMed  Google Scholar 

  76. Elferink, M. A. et al. Metachronous metastases from colorectal cancer: a population-based study in North-East Netherlands. Int. J. Colorectal Dis. 30, 205–212 (2015).

    PubMed  Google Scholar 

  77. Tan, E. et al. Diagnostic precision of carcinoembryonic antigen in the detection of recurrence of colorectal cancer. Surg. Oncol. 18, 15–24 (2009).

    PubMed  Google Scholar 

  78. Staab, H. J. et al. Slope analysis of the postoperative CEA time course and its possible application as an aid in diagnosis of disease progression in gastrointestinal cancer. Am. J. Surg. 136, 322–327 (1978).

    CAS  PubMed  Google Scholar 

  79. Verberne, C. J. et al. Detection of recurrences during follow-up after liver surgery for colorectal metastases: both carcinoembryonic antigen (CEA) and imaging are important. Ann. Surg. Oncol. 20, 457–463 (2013).

    PubMed  Google Scholar 

  80. Verberne, C. J. et al. Intensified follow-up in colorectal cancer patients using frequent carcino-embryonic antigen (CEA) measurements and CEA-triggered imaging: results of the randomized “CEAwatch” trial. Eur. J. Surg. Oncol. 41, 1188–1196 (2015).

    CAS  PubMed  Google Scholar 

  81. Bipat, S. et al. Colorectal liver metastases: CT, MR imaging, and PET for diagnosis — meta-analysis. Radiology 237, 123–131 (2005).

    PubMed  Google Scholar 

  82. Kinkel, K. et al. Detection of hepatic metastases from cancers of the gastrointestinal tract by using noninvasive imaging methods (US, CT, MR imaging, PET): a meta-analysis. Radiology 224, 748–756 (2002).

    PubMed  Google Scholar 

  83. Westwood, M. et al. Contrast-enhanced ultrasound using SonoVue® (sulphur hexafluoride microbubbles) compared with contrast-enhanced computed tomography and contrast-enhanced magnetic resonance imaging for the characterisation of focal liver lesions and detection of liver metastases: a systematic review and cost-effectiveness analysis. Health Technol. Assess. 17, 1–243 (2013).

    PubMed  PubMed Central  Google Scholar 

  84. Mainenti, P. P. et al. Non-invasive diagnostic imaging of colorectal liver metastases. World J. Radiol. 7, 157–169 (2015).

    PubMed  PubMed Central  Google Scholar 

  85. Niekel, M. C., Bipat, S. & Stoker, J. Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology 257, 674–684 (2010).

    PubMed  Google Scholar 

  86. Patel, S. et al. Positron emission tomography/computed tomographic scans compared to computed tomographic scans for detecting colorectal liver metastases: a systematic review. Ann. Surg. 253, 666–671 (2011).

    PubMed  Google Scholar 

  87. Kronawitter, U. et al. Evaluation of chest computed tomography in the staging of patients with potentially resectable liver metastases from colorectal carcinoma. Cancer 86, 229–235 (1999).

    CAS  PubMed  Google Scholar 

  88. Povoski, S. P. et al. Role of chest CT in patients with negative chest X-rays referred for hepatic colorectal metastases. Ann. Surg. Oncol. 5, 9–15 (1998).

    CAS  PubMed  Google Scholar 

  89. Duffy, M. J. et al. Use of faecal markers in screening for colorectal neoplasia: a European group on tumor markers position paper. Int. J. Cancer 128, 3–11 (2011).

    CAS  PubMed  Google Scholar 

  90. Whitlock, E. P. et al. Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann. Intern. Med. 149, 638–658 (2008).

    PubMed  Google Scholar 

  91. Jahn, H. et al. Can Hemoccult-II replace colonoscopy in surveillance after radical surgery for colorectal cancer and after polypectomy? Dis. Colon Rectum 35, 253–256 (1992).

    CAS  PubMed  Google Scholar 

  92. Imperiale, T. F. et al. Multitarget stool DNA testing for colorectal-cancer screening. N. Engl. J. Med. 370, 1287–1297 (2014).

    CAS  PubMed  Google Scholar 

  93. Bosch, L. J. et al. Molecular tests for colorectal cancer screening. Clin. Colorectal Cancer 10, 8–23 (2011).

    CAS  PubMed  Google Scholar 

  94. Lee, B. B. et al. Aberrant methylation of APC, MGMT, RASSF2A, and Wif-1 genes in plasma as a biomarker for early detection of colorectal cancer. Clin. Cancer Res. 15, 6185–6191 (2009).

    CAS  PubMed  Google Scholar 

  95. Leung, W. K. et al. Quantitative detection of promoter hypermethylation in multiple genes in the serum of patients with colorectal cancer. Am. J. Gastroenterol. 100, 2274–2279 (2005).

    CAS  PubMed  Google Scholar 

  96. Lalmahomed, Z. S. et al. Circulating tumor cells and sample size: the more, the better. J. Clin. Oncol. 28, e288–e289 (2010).

    PubMed  Google Scholar 

  97. Mostert, B. et al. KRAS and BRAF mutation status in circulating colorectal tumor cells and their correlation with primary and metastatic tumor tissue. Int. J. Cancer 133, 130–141 (2013).

    CAS  PubMed  Google Scholar 

  98. Mostert, B. et al. mRNA expression profiles in circulating tumor cells of metastatic colorectal cancer patients. Mol. Oncol. 9, 920–932 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Best, M. G. et al. RNA-Seq of tumor-educated platelets enables blood-based pan-cancer, multiclass, and molecular pathway cancer diagnostics. Cancer Cell 28, 666–676 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Nilsson, R. J. et al. Blood platelets contain tumor-derived RNA biomarkers. Blood 118, 3680–3683 (2011).

    PubMed  PubMed Central  Google Scholar 

  101. Metzger, J. et al. Urine proteomic analysis differentiates cholangiocarcinoma from primary sclerosing cholangitis and other benign biliary disorders. Gut 62, 122–130 (2013).

    CAS  PubMed  Google Scholar 

  102. Broker, M. E. et al. Collagen peptides in urine: a new promising biomarker for the detection of colorectal liver metastases. PLoS ONE 8, e70918 (2013).

    PubMed  PubMed Central  Google Scholar 

  103. Deslauriers, J. & Gregoire, J. Clinical and surgical staging of non-small cell lung cancer. Chest 117 (4 Suppl. 1), 96S–103S (2000).

    CAS  PubMed  Google Scholar 

  104. Staples, C. A. et al. Mediastinal nodes in bronchogenic carcinoma: comparison between CT and mediastinoscopy. Radiology 167, 367–372 (1988).

    CAS  PubMed  Google Scholar 

  105. Antoch, G. et al. Whole-body dual-modality PET/CT and whole-body MRI for tumor staging in oncology. JAMA 290, 3199–3206 (2003).

    CAS  PubMed  Google Scholar 

  106. Antoch, G. & Bockisch, A. Combined PET/MRI: a new dimension in whole-body oncology imaging? Eur. J. Nucl. Med. Mol. Imaging 36 (Suppl. 1), S113–S120 (2009).

    PubMed  Google Scholar 

  107. Pfannenberg, C. et al. Prospective comparison of 18F-fluorodeoxyglucose positron emission tomography/computed tomography and whole-body magnetic resonance imaging in staging of advanced malignant melanoma. Eur. J. Cancer 43, 557–564 (2007).

    PubMed  Google Scholar 

  108. Schmidt, G. P. et al. Comprehensive imaging of tumor recurrence in breast cancer patients using whole-body MRI at 1.5 and 3 T compared to FDG-PET-CT. Eur. J. Radiol. 65, 47–58 (2008).

    PubMed  Google Scholar 

  109. Squillaci, E. et al. Staging of colon cancer: whole-body MRI versus whole-body PET-CT — initial clinical experience. Abdom. Imaging 33, 676–688 (2008).

    PubMed  Google Scholar 

  110. Sargent, D. J. et al. End points for colon cancer adjuvant trials: observations and recommendations based on individual patient data from 20,898 patients enrolled onto 18 randomized trials from the ACCENT Group. J. Clin. Oncol. 25, 4569–4574 (2007).

    PubMed  Google Scholar 

  111. Tomlinson, J. S. et al. Actual 10-year survival after resection of colorectal liver metastases defines cure. J. Clin. Oncol. 25, 4575–4580 (2007).

    PubMed  Google Scholar 

  112. Walter, C. J. et al. Fifth-year surveillance computed tomography scanning after potentially curative resections for colorectal cancer. Surgeon 11, 25–29 (2013).

    PubMed  Google Scholar 

  113. Augestad, K. M. et al. Cost-effectiveness and quality of life in surgeon versus general practitioner-organised colon cancer surveillance: a randomised controlled trial. BMJ Open 3, e002391 (2013).

    PubMed  PubMed Central  Google Scholar 

  114. Grossmann, E. M. et al. Follow-up of colorectal cancer patients after resection with curative intent-the GILDA trial. Surg. Oncol. 13, 119–124 (2004).

    PubMed  Google Scholar 

  115. Mäkelä, J. T., Laitinen, S. O. & Kairaluoma, M. I. Five-year follow-up after radical surgery for colorectal cancer. Results of a prospective randomized trial. Arch. Surg. 130, 1062–1067 (1995).

    PubMed  Google Scholar 

  116. Ohlsson, B. et al. Follow-up after curative surgery for colorectal carcinoma. Randomized comparison with no follow-up. Dis. Colon Rectum 38, 619–626 (1995).

    CAS  PubMed  Google Scholar 

  117. Pietra, N. et al. Role of follow-up in management of local recurrences of colorectal cancer: a prospective, randomized study. Dis. Colon Rectum 41, 1127–1133 (1998).

    CAS  PubMed  Google Scholar 

  118. Primrose, J. N. et al. Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial. JAMA 311, 263–270 (2014).

    CAS  PubMed  Google Scholar 

  119. Rodriguez-Moranta, F. et al. Postoperative surveillance in patients with colorectal cancer who have undergone curative resection: a prospective, multicenter, randomized, controlled trial. J. Clin. Oncol. 24, 386–393 (2006).

    PubMed  Google Scholar 

  120. Rosati, G. et al. A randomized trial of intensive versus minimal surveillance patients with resected Dukes B2-C colorectal carcinoma. Ann. Oncol. 27, 274–280 (2016).

    CAS  PubMed  Google Scholar 

  121. Secco, G. B. 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. 28, 418–423 (2002).

    PubMed  Google Scholar 

  122. Treasure, T. et al. The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer. BMJ Open 4, e004385 (2014).

    PubMed  PubMed Central  Google Scholar 

  123. Wattchow, D. A. et al. General practice versus surgical-based follow-up for patients with colon cancer: randomised controlled trial. Br. J. Cancer 94, 1116–1121 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Wille-Jorgensen, P. et al. An interim analysis of recruitment to the COLOFOL trial. Colorectal Dis. 11, 756–758 (2009).

    CAS  PubMed  Google Scholar 

  125. Pugh, S. A. M. et al. Scheduled use of CEA and CT follow-up to detect recurrence of colorectal cancer: 6–12 year results from the FACS randomised controlled trial [abstract]. Ann. Oncol. 27 (Suppl. 6), 453O (2016).

    Google Scholar 

  126. Figueredo, A. et al. Follow-up of patients with curatively resected colorectal cancer: a practice guideline. BMC Cancer 3, 26 (2003).

    PubMed  PubMed Central  Google Scholar 

  127. Jeffery, M., Hickey, B. E. & Hider, P. N. Follow-up strategies for patients treated for non-metastatic colorectal cancer. Cochrane Database Syst. Rev. 1, CD002200 (2007).

    Google Scholar 

  128. Renehan, A. G. et al. Impact on survival of intensive follow up after curative resection for colorectal cancer: systematic review and meta-analysis of randomised trials. BMJ 324, 813 (2002).

    PubMed  PubMed Central  Google Scholar 

  129. Renehan, A. G. et al. Mechanisms of improved survival from intensive followup in colorectal cancer: a hypothesis. Br. J. Cancer 92, 430–433 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Tjandra, J. J. & Chan, M. K. Follow-up after curative resection of colorectal cancer: a meta-analysis. Dis. Colon Rectum 50, 1783–1799 (2007).

    PubMed  Google Scholar 

  131. Mokhles, S. et al. Meta-analysis of colorectal cancer follow-up after potentially curative resection. Br. J. Surg. 103, 1259–1268 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Kuchler, T. et al. Impact of psychotherapeutic support on gastrointestinal cancer patients undergoing surgery: survival results of a trial. Hepatogastroenterology 46, 322–335 (1999).

    CAS  PubMed  Google Scholar 

  133. Newell, S. A., Sanson-Fisher, R. W. & Savolainen, N. J. Systematic review of psychological therapies for cancer patients: overview and recommendations for future research. J. Natl Cancer Inst. 94, 558–584 (2002).

    PubMed  Google Scholar 

  134. Braunholtz, D. A., Edwards, S. J. & Lilford, R. J. Are randomized clinical trials good for us (in the short term)? Evidence for a “trial effect”. J. Clin. Epidemiol. 54, 217–224 (2001).

    CAS  PubMed  Google Scholar 

  135. Calle, E. E. et al. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348, 1625–1638 (2003).

    PubMed  Google Scholar 

  136. Kjeldsen, B. J. et al. Influence of follow-up on health-related quality of life after radical surgery for colorectal cancer. Scand. J. Gastroenterol. 34, 509–515 (1999).

    CAS  PubMed  Google Scholar 

  137. Bhangu, A. et al. Survival outcome of local excision versus radical resection of colon or rectal carcinoma: a Surveillance, Epidemiology, and End Results (SEER) population-based study. Ann. Surg. 258, 563–569 (2013).

    PubMed  Google Scholar 

  138. Verseveld, M. et al. Chemoradiation therapy for rectal cancer in the distal rectum followed by organ-sparing transanal endoscopic microsurgery (CARTS study). Br. J. Surg. 102, 853–860 (2015).

    CAS  PubMed  Google Scholar 

  139. Schlemper, R. J. et al. The Vienna classification of gastrointestinal epithelial neoplasia. Gut 47, 251–255 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Meining, A. et al. Risk factors for unfavorable outcomes after endoscopic removal of submucosal invasive colorectal tumors. Clin. Gastroenterol. Hepatol. 9, 590–594 (2011).

    PubMed  Google Scholar 

  141. Morson, B. C. et al. Histopathology and prognosis of malignant colorectal polyps treated by endoscopic polypectomy. Gut 25, 437–444 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Muller, S. et al. Significance of venous and lymphatic invasion in malignant polyps of the colon and rectum. Gut 30, 1385–1391 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Nascimbeni, R. et al. Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis. Colon Rectum 45, 200–206 (2002).

    PubMed  Google Scholar 

  144. Bach, S. P. et al. A predictive model for local recurrence after transanal endoscopic microsurgery for rectal cancer. Br. J. Surg. 96, 280–290 (2009).

    CAS  PubMed  Google Scholar 

  145. Davila, R. E. et al. ASGE guideline: the role of endoscopy in the diagnosis, staging, and management of colorectal cancer. Gastrointest. Endosc. 61, 1–7 (2005).

    PubMed  Google Scholar 

  146. Hassan, C. et al. Histologic risk factors and clinical outcome in colorectal malignant polyp: a pooled-data analysis. Dis. Colon Rectum 48, 1588–1596 (2005).

    PubMed  Google Scholar 

  147. Buchner, A. M., Guarner-Argente, C. & Ginsberg, G. G. Outcomes of EMR of defiant colorectal lesions directed to an endoscopy referral center. Gastrointest. Endosc. 76, 255–263 (2012).

    PubMed  Google Scholar 

  148. Khashab, M. et al. Incidence and predictors of “late” recurrences after endoscopic piecemeal resection of large sessile adenomas. Gastrointest. Endosc. 70, 344–349 (2009).

    PubMed  Google Scholar 

  149. Lieberman, D. A. et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 143, 844–857 (2012).

    PubMed  Google Scholar 

  150. Winawer, S. J. et al. Guidelines for colonoscopy surveillance after polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society. Gastroenterology 130, 1872–1885 (2006).

    PubMed  Google Scholar 

  151. Zlatanic, J. et al. Large sessile colonic adenomas: use of argon plasma coagulator to supplement piecemeal snare polypectomy. Gastrointest. Endosc. 49, 731–735 (1999).

    CAS  PubMed  Google Scholar 

  152. Di Gregorio, C. et al. Clinical outcome of low- and high-risk malignant colorectal polyps: results of a population-based study and meta-analysis of the available literature. Intern. Emerg. Med. 9, 151–160 (2014).

    PubMed  Google Scholar 

  153. Kim, M. N. et al. Clinical features and prognosis of early colorectal cancer treated by endoscopic mucosal resection. J. Gastroenterol. Hepatol. 26, 1619–1625 (2011).

    PubMed  Google Scholar 

  154. Ackland, S. P. et al. A meta-analysis of two randomised trials of early chemotherapy in asymptomatic metastatic colorectal cancer. Br. J. Cancer 93, 1236–1243 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Cairns, S. R. et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 59, 666–689 (2010).

    PubMed  Google Scholar 

  156. Hartley, A. et al. Pathological complete response following pre-operative chemoradiotherapy in rectal cancer: analysis of phase II/III trials. Br. J. Radiol. 78, 934–938 (2005).

    CAS  PubMed  Google Scholar 

  157. Habr-Gama, A. et al. Watch and wait approach following extended neoadjuvant chemoradiation for distal rectal cancer: are we getting closer to anal cancer management? Dis. Colon Rectum 56, 1109–1117 (2013).

    PubMed  Google Scholar 

  158. Maas, M. et al. Long-term outcome in patients with a pathological complete response after chemoradiation for rectal cancer: a pooled analysis of individual patient data. Lancet Oncol. 11, 835–844 (2010).

    PubMed  Google Scholar 

  159. Hiotis, S. P. et al. Assessing the predictive value of clinical complete response to neoadjuvant therapy for rectal cancer: an analysis of 488 patients. J. Am. Coll. Surg. 194, 131–135 (2002).

    PubMed  Google Scholar 

  160. Zmora, O. et al. Does rectal wall tumor eradication with preoperative chemoradiation permit a change in the operative strategy? Dis. Colon Rectum 47, 1607–1612 (2004).

    PubMed  Google Scholar 

  161. Pucciarelli, S. et al. Relationship between pathologic T-stage and nodal metastasis after preoperative chemoradiotherapy for locally advanced rectal cancer. Ann. Surg. Oncol. 12, 111–116 (2005).

    PubMed  Google Scholar 

  162. Maas, M. et al. Assessment of clinical complete response after chemoradiation for rectal cancer with digital rectal examination, endoscopy, and MRI: selection for organ-saving treatment. Ann. Surg. Oncol. 22, 3873–3880 (2015).

    PubMed  PubMed Central  Google Scholar 

  163. Araujo, R. O. et al. Nonoperative management of rectal cancer after chemoradiation opposed to resection after complete clinical response. A comparative study. Eur. J. Surg. Oncol. 41, 1456–1463 (2015).

    CAS  PubMed  Google Scholar 

  164. Dalton, R. S. et al. A single-centre experience of chemoradiotherapy for rectal cancer: is there potential for nonoperative management? Colorectal Dis. 14, 567–571 (2012).

    CAS  PubMed  Google Scholar 

  165. Habr-Gama, A. Assessment and management of the complete clinical response of rectal cancer to chemoradiotherapy. Colorectal Dis. 8 (Suppl. 3), 21–24 (2006).

    PubMed  Google Scholar 

  166. Maas, M. et al. Wait-and-see policy for clinical complete responders after chemoradiation for rectal cancer. J. Clin. Oncol. 29, 4633–4640 (2011).

    PubMed  Google Scholar 

  167. Smith, J. D. et al. Nonoperative management of rectal cancer with complete clinical response after neoadjuvant therapy. Ann. Surg. 256, 965–972 (2012).

    PubMed  Google Scholar 

  168. Yeo, S. G., Kim, D. Y. & Oh, J. H. Long-term survival without surgery following a complete response to pre-operative chemoradiotherapy for rectal cancer: a case series. Oncol. Lett. 6, 1573–1576 (2013).

    PubMed  PubMed Central  Google Scholar 

  169. Yu, S. K. et al. Deferral of rectal surgery following a continued response to preoperative chemoradiotherapy (Watch and Wait) study: a phase II multicenter study in the United Kingdom [abstract]. J. Clin. Oncol. 29, 489 (2011).

    Google Scholar 

  170. US National Library of Medicine. ClinicalTrials.govhttps://clinicaltrials.gov/ct2/show/NCT00939666 (2011).

  171. Martens, M. H. et al. Long-term outcome of an organ preservation program after neoadjuvant treatment for rectal cancer. J. Natl Cancer Inst. 108, djw171 (2016).

    PubMed  Google Scholar 

  172. de Ridder, J. A. et al. Management of liver metastases in colorectal cancer patients: a retrospective case–control study of systemic therapy versus liver resection. Eur. J. Cancer 59, 13–21 (2016).

    PubMed  Google Scholar 

  173. Heinemann, V. et al. FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab as first-line treatment for patients with metastatic colorectal cancer (FIRE-3): a randomised, open-label, phase 3 trial. Lancet Oncol. 15, 1065–1075 (2014).

    CAS  PubMed  Google Scholar 

  174. Loupakis, F. et al. Initial therapy with FOLFOXIRI and bevacizumab for metastatic colorectal cancer. N. Engl. J. Med. 371, 1609–1618 (2014).

    PubMed  Google Scholar 

  175. van der Geest, L. G. et al. Nationwide trends in incidence, treatment and survival of colorectal cancer patients with synchronous metastases. Clin. Exp. Metastasis 32, 457–465 (2015).

    CAS  PubMed  Google Scholar 

  176. Ayez, N. et al. Long-term results of the “liver first” approach in patients with locally advanced rectal cancer and synchronous liver metastases. Dis. Colon Rectum 56, 281–287 (2013).

    PubMed  Google Scholar 

  177. House, M. G. et al. Survival after hepatic resection for metastatic colorectal cancer: trends in outcomes for 1,600 patients during two decades at a single institution. J. Am. Coll. Surg. 210, 744–752 (2010).

    PubMed  Google Scholar 

  178. van der Pool, A. E. et al. Optimizing the outcome of surgery in patients with rectal cancer and synchronous liver metastases. Br. J. Surg. 97, 383–390 (2010).

    CAS  PubMed  Google Scholar 

  179. Chua, T. C. et al. Predictors of cure after hepatic resection of colorectal liver metastases: an analysis of actual 5- and 10-year survivors. J. Surg. Oncol. 103, 796–800 (2011).

    PubMed  Google Scholar 

  180. Vigano, L. et al. Liver surgery for colorectal metastases: results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann. Surg. Oncol. 15, 2458–2464 (2008).

    PubMed  Google Scholar 

  181. Gonzalez, M. et al. Risk factors for survival after lung metastasectomy in colorectal cancer patients: a systematic review and meta-analysis. Ann. Surg. Oncol. 20, 572–579 (2013).

    PubMed  Google Scholar 

  182. Zampino, M. G. et al. Lung metastases from colorectal cancer: analysis of prognostic factors in a single institution study. Ann. Thorac. Surg. 98, 1238–1245 (2014).

    PubMed  Google Scholar 

  183. Migliore, M. et al. Finding the evidence for pulmonary metastasectomy in colorectal cancer: the PulMicc trial. Future Oncol. 11 (Suppl. 2), 15–18 (2015).

    CAS  PubMed  Google Scholar 

  184. Treasure, T. & Macbeth, F. The GILDA trial finds no survival benefit from intensified screening after primary resection of colorectal cancer: the PulMiCC trial tests the survival benefit of pulmonary metastasectomy for detected asymptomatic lung metastases. Ann. Oncol. 27, 745 (2016).

    CAS  PubMed  Google Scholar 

  185. de Cuba, E. M. et al. Cytoreductive surgery and HIPEC for peritoneal metastases combined with curative treatment of colorectal liver metastases: systematic review of all literature and meta-analysis of observational studies. Cancer Treat. Rev. 39, 321–327 (2013).

    CAS  PubMed  Google Scholar 

  186. Elias, D., Quenet, F. & Goere, D. Current status and future directions in the treatment of peritoneal dissemination from colorectal carcinoma. Surg. Oncol. Clin. N. Am. 21, 611–623 (2012).

    PubMed  Google Scholar 

  187. Esquivel, J. et al. The American Society of Peritoneal Surface Malignancies (ASPSM) multiinstitution evaluation of the Peritoneal Surface Disease Severity Score (PSDSS) in 1,013 patients with colorectal cancer with peritoneal carcinomatosis. Ann. Surg. Oncol. 21, 4195–4201 (2014).

    PubMed  Google Scholar 

  188. Leung, U. et al. Colorectal cancer liver metastases and concurrent extrahepatic disease treated with resection. Ann. Surg. http://dx.doi.org/10.1097/SLA.0000000000001624 (2016).

  189. US National Library of Medicine. ClinicalTrials.govhttps://clinicaltrials.gov/ct2/show/NCT01792934 (2015).

  190. Sotiropoulos, G. C. & Lang, H. Clinical scoring systems for predicting outcome after surgery for colorectal liver metastases: towards a better multidisciplinary approach. Liver Int. 29, 6–9 (2009).

    PubMed  Google Scholar 

  191. Adam, R. et al. Repeat hepatectomy for colorectal liver metastases. Ann. Surg. 225, 51–60 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  192. Butte, J. M. et al. Recurrence after partial hepatectomy for metastatic colorectal cancer: potentially curative role of salvage repeat resection. Ann. Surg. Oncol. 22, 2761–2771 (2015).

    PubMed  PubMed Central  Google Scholar 

  193. de Jong, M. C. et al. Repeat curative intent liver surgery is safe and effective for recurrent colorectal liver metastasis: results from an international multi-institutional analysis. J. Gastrointest. Surg. 13, 2141–2151 (2009).

    PubMed  Google Scholar 

  194. Lam, V. W. et al. A systematic review of repeat hepatectomy for recurrent colorectal liver metastases. J. Gastrointest. Surg. 17, 1312–1321 (2013).

    PubMed  Google Scholar 

  195. van der Pool, A. E. et al. Local treatment for recurrent colorectal hepatic metastases after partial hepatectomy. J. Gastrointest. Surg. 13, 890–895 (2009).

    PubMed  Google Scholar 

  196. Chen, F. et al. Repeat resection of pulmonary metastasis is beneficial for patients with colorectal carcinoma. World J. Surg. 34, 2373–2378 (2010).

    PubMed  Google Scholar 

  197. Bhattacharjya, S., Aggarwal, R. & Davidson, B. R. Intensive follow-up after liver resection for colorectal liver metastases: results of combined serial tumour marker estimations and computed tomography of the chest and abdomen — a prospective study. Br. J. Cancer 95, 21–26 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  198. Connor, S. et al. Follow-up and outcomes for resection of colorectal liver metastases in Edinburgh. Eur. J. Surg. Oncol. 33, 55–60 (2007).

    CAS  PubMed  Google Scholar 

  199. Gomez, D. et al. Outcomes of intensive surveillance after resection of hepatic colorectal metastases. Br. J. Surg. 97, 1552–1560 (2010).

    CAS  PubMed  Google Scholar 

  200. Langenhoff, B. S., Krabbe, P. F. & Ruers, T. J. Efficacy of follow-up after surgical treatment of colorectal liver metastases. Eur. J. Surg. Oncol. 35, 180–186 (2009).

    CAS  PubMed  Google Scholar 

  201. Metcalfe, M. et al. Detecting curable disease following hepatectomy for colorectal metastases. ANZ J. Surg. 75, 524–527 (2005).

    PubMed  Google Scholar 

  202. Metcalfe, M. S., Mullin, E. J. & Maddern, G. J. Choice of surveillance after hepatectomy for colorectal metastases. Arch. Surg. 139, 749–754 (2004).

    PubMed  Google Scholar 

  203. Wilhelmsen, M. et al. Determinants of recurrence after intended curative resection for colorectal cancer. Scand. J. Gastroenterol. 49, 1399–1408 (2014).

    PubMed  Google Scholar 

  204. Belt, E. J. et al. Peri-operative bowel perforation in early stage colon cancer is associated with an adverse oncological outcome. J. Gastrointest. Surg. 16, 2260–2266 (2012).

    CAS  PubMed  Google Scholar 

  205. Honore, C. et al. Definition of patients presenting a high risk of developing peritoneal carcinomatosis after curative surgery for colorectal cancer: a systematic review. Ann. Surg. Oncol. 20, 183–192 (2013).

    PubMed  Google Scholar 

  206. Cortet, M. et al. Patterns of recurrence of obstructing colon cancers after surgery for cure: a population-based study. Colorectal Dis. 15, 1100–1106 (2013).

    CAS  PubMed  Google Scholar 

  207. Krarup, P. M. et al. Anastomotic leak increases distant recurrence and long-term mortality after curative resection for colonic cancer: a nationwide cohort study. Ann. Surg. 259, 930–938 (2014).

    PubMed  Google Scholar 

  208. Busch, O. R. et al. Blood transfusions and prognosis in colorectal cancer. N. Engl. J. Med. 328, 1372–1376 (1993).

    CAS  PubMed  Google Scholar 

  209. Elias, D. et al. Results of systematic second-look surgery in patients at high risk of developing colorectal peritoneal carcinomatosis. Ann. Surg. 247, 445–450 (2008).

    PubMed  Google Scholar 

  210. Elias, D. et al. Results of systematic second-look surgery plus HIPEC in asymptomatic patients presenting a high risk of developing colorectal peritoneal carcinomatosis. Ann. Surg. 254, 289–293 (2011).

    CAS  PubMed  Google Scholar 

  211. Ripley, R. T. et al. Prospective randomized trial evaluating mandatory second look surgery with HIPEC and CRS versus standard of care in patients at high risk of developing colorectal peritoneal metastases. 11, 62 (2010).

  212. US National Library of Medicine. ClinicalTrials.govhttps://clinicaltrials.gov/ct2/show/NCT00005944 (2011).

  213. de Wijkerslooth, T. R. et al. Immunochemical fecal occult blood testing is equally sensitive for proximal and distal advanced neoplasia. Am. J. Gastroenterol. 107, 1570–1578 (2012).

    CAS  PubMed  Google Scholar 

  214. Edelman, B. R. & Weiser, M. R. Endorectal ultrasound: its role in the diagnosis and treatment of rectal cancer. Clin. Colon Rectal Surg. 21, 167–177 (2008).

    PubMed  PubMed Central  Google Scholar 

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E.P.v.d.S., C.V. and E.J.K. researched the data for article. All authors contributed substantially to discussions of content. E.P.v.d.S., C.V. and E.J.K. wrote the manuscript. M.C.W.S., D.J.G., C.V., and E.J.K. reviewed/edited the manuscript before submission.

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Correspondence to Ernst J. Kuipers.

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van der Stok, E., Spaander, M., Grünhagen, D. et al. Surveillance after curative treatment for colorectal cancer. Nat Rev Clin Oncol 14, 297–315 (2017). https://doi.org/10.1038/nrclinonc.2016.199

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