Top

20-12-2016 | Colorectal cancer | Article

Surveillance after curative treatment for colorectal cancer

Authors: Eric P. van der Stok, Manon C. W. Spaander, Dirk J. Grünhagen, Cornelis Verhoef, Ernst J. Kuipers

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.

Nat Rev Clin Oncol 2017; 14: 297–315. doi:10.1038/nrclinonc.2016.199

Subject terms: Cancer imaging • Cancer screening • Colorectal cancer • Medical imaging • Metastasis

Colorectal cancer (CRC) is a major cause of cancer-related deaths¹: CRC is the third most commonly diagnosed cancer worldwide, with an estimated 614,000 women (9.2% of all new cancer cases) and 746,000 men (10% of all new cancer cases) affected, and an estimated 693,900 CRC-related deaths in 2012 (Ref. 2). Around 50% of patients with CRC present with localized disease (stage I–II), about 25% with locoregional advanced-stage disease (stage III), and the remainder with metastases in distant organs (stage IV)^3, 4, 5. National screening programmes for CRC have been introduced in more than 50 countries, and this number is increasing⁶. Of note, screening increases the proportion of patients with CRCs who are diagnosed at an early disease stage⁷, thereby increasing the potential for treatment with curative intent and improving patients outcomes. After treatment with curative intent, patients with CRC enter a surveillance programme that generally lasts for 5 years. Approximately 30% of patients with stage I–III disease develop recurrent disease after initial treatment^8, 9; among patients with stage IV CRC, up to 65% have relapsed disease after treatment with curative intent^{10, 11, 12, 13, 14, 15, 16}.

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

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

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 ISI PubMed Article

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 Article

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 Article

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

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 ISI PubMed Article

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 Article

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 Articlede

10. 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).ISI PubMed

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 Article

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 ISI PubMed Article

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 Article

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).ISI PubMed Article

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).ISI PubMed Article

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

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

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 Article

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).Article

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).Article

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

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).ISI PubMed Article

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

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 Article

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 Article

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 ISI PubMed Article

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 Article

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 ISI PubMed Article

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).ISI PubMed Article

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 Article

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 Article

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).

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 Article

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).Article

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).

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 Article

39. Chen, F. & Stuart, M. Colonoscopic follow-up of colorectal carcinoma. Dis. Colon Rectum37, 568–572 (1994).CAS PubMed Article

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

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).Article

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 Article

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 ISI PubMed Article

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 ISI PubMed Article

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).

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 Article

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 Article

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 Article

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).Article

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 Article

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).

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).Article

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

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

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).Article

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. Gut61, 1552–1559 (2012).PubMed Article

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 Article

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

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 Article

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

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).Article

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 Article

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).Article

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 Article

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 Article

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 Article

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

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).Article

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 ISI PubMed

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 Article

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 Article

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).Article

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

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).Article

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).Article

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

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 Article

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).Article

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 Article

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

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 Article

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 Article

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

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).Article

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).Article

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 Article

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 Article

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 Article

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).ISI PubMed Article

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 Article

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

93. Bosch, L. J. et al. Molecular tests for colorectal cancer screening. Clin. Colorectal Cancer10, 8–23 (2011).CAS PubMed Article

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 Article

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 ISI PubMed Article

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

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 ISI PubMed Article

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

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 Article

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

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 Article

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).CAS Article

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

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

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 ISI PubMed Article

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).

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).Article

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).Article

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).Article

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 Article

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).ISI PubMed Article

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

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 Open3, e002391 (2013).Article

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 Article

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).CAS ISI PubMed Article

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 ISI PubMed Article

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 Article

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 Article

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).ISI PubMed Article

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 Article

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 Article

122. Treasure, T. et al. The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer. BMJ Open4, e004385 (2014).PubMed Article

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 Article

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

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).

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

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).

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).ISI PubMed Article

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 ISI PubMed Article

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 Article

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

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

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 Article

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 ISI PubMed Article

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).ISI PubMed Article

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 Article

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).

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 Article

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

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).Article

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

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 ISI PubMed Article

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).ISI PubMed Article

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 Article

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).Article

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).ISI PubMed Article

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).ISI PubMed Article

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).ISI PubMed Article

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).ISI PubMed Article

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).ISI PubMed Article

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 Article

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).Article

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).Article

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 Article

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).ISI PubMed Article

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 Article

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 Article

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).ISI PubMed Article

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).ISI PubMed Article

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 Article

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 Article

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).Article

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 Article

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 Article

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).

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 Article

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 Article

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).

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).Article

170. US National Library of Medicine. ClinicalTrials.gov https://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).Article

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. Cancer59, 13–21 (2016).Article

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 ISI PubMed Article

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

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 Article

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).Article

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).ISI PubMed Article

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 Article

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).Article

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).Article

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 Article

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).Article

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).

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 Article

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 ISI PubMed Article

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).ISI PubMed Article

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).Article

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.gov https://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).Article

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

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).Article

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).Article

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 Article

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).Article

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

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 Article

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 Article

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

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 Article

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

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

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

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 Article

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 Article

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

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).Article

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

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).Article

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 Article

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.gov https://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 Article

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). Article

Medicine Matters Oncology

Abstract