Follow-up colonoscopy after colorectal cancer resection

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Background

Given that the objectives of surveillance are early detection of metachronous cancer and timely polypectomy for metachronous adenomas, recommendations about the timing of colonoscopy after resection of colorectal cancer (CRCColorectal cancer) should be largely based upon the natural history of metachronous colonic neoplasia. Intraluminal recurrences are infrequent and a secondary consideration.

The natural history of metachronous cancer and polyps is best estimated by studies of the yields of colonoscopy at various time points after surgery, when pre or perioperative colonoscopy has excluded synchronous cancer and cleared synchronous polyps.

Evidence

What should be the follow-up colonoscopy for patients after CRCColorectal cancer resection? (FUC1)

Systematic review evidence

A systematic review of studies published since 2010 was undertaken to update the evidence on which the 2011 version of these guidelines was based.[1]

No new studies were found (see Technical report).

The systematic review undertaken in 2010 is still relevant and summarises the available evidence for this clinical question.

In the literature prior to 2005, Barillari[2] and Neugut[3] found that more than one-half of metachronous adenomas and cancers were detected within the first 24 months after surgery. In a 2000 study, Togashi et al[4] detected 22 metachronous CRCs in 19 out of 341 patients after CRCColorectal cancer surgery, 14 (64 %) of them within 5 years of surgery. Most were small (≤10mm) and many had a flat endoscopic appearance. In a study of 174 patients reported by Juhl et al in 1990,[5] three-quarters of the colonoscopically detected neoplasms (adenomatous polyps and cancers) occurred within the first 24 months. In the period 12–30 months after surgery, 4metachronous cancers and 37 advanced adenomas were detected. A retrospective review by Khoury et al[6] concluded that annual follow-up colonoscopy for 2 years after CRCColorectal cancer surgery was beneficial and that the interval between subsequent examinations be increased depending on the result of the most recent examination.[6]

However, not all of these earlier studies advocated colonoscopy within 1 to 2 years of surgery. Among 175 patients who underwent a curative resection for CRCColorectal cancer between 1986 and 1992, colonoscopies performed 1 year after surgery and then at 2-year intervals revealed no metachronous cancers or advanced adenomas. The authors suggested that only patients who had had synchronous adenomas at pre-operative colonoscopy should undergo follow-up colonoscopy at 3 years.[7] Similarly, Stigliano et al[8] conducted a retrospective study of 322 patients and found no metachronous cancers within the first 2 years after surgery. In their 2002 review, Berman et al[9] suggested that there were insufficient data to support the routine use of annual or more frequent colonoscopy to identify metachronous or recurrent CRCColorectal cancer and they suggested post-operative colonoscopy be limited to every 3 to 5 years. A large retrospective audit of patients after CRCColorectal cancer resection by McFall et al, concluded that most patients are at very low risk of developing significant colonic pathology in the 5 years after resection, but the value of this study was limited by the fact that less than one-third of the patients underwent postoperative colonoscopy[10] and the mean interval between surgery and colonoscopy was more than 4 years. Similar reservations about the need for follow-up colonoscopy earlier than 2 to 3 years were expressed by Mathew et al,[11] even though 10 out of 14 patients with neoplastic findings at surveillance colonoscopy were detected 2 years postoperatively.

A Western Australian study by Yusoff et al audited all patients who underwent surgical resection of CRCColorectal cancer from 1989 to 2001[12] and found that no metachronous cancers (and only 1 of 11 recurrent anastomotic cancers) were found by surveillance of asymptomatic patients. The three metachronous cancers were all detected in symptomatic patients, at 4, 8 and 9 years after surgery. In a subset of their patients, the yields for adenoma were 10% at one 1 year post-operatively, 28% at 2 years and none at 3 years.

Another Australian study by Platell et al published in 2005 specifically evaluated the clinical utility of performing a colonoscopy 12 months after curative resection for CRCColorectal cancer.[13] In 253 patients who had undergone complete colonoscopy prior to resection, 90% received their first post-operative colonoscopy at a mean of 1.1 years. Although no recurrent or metachronous cancers were found, 149 polyps were detected in 30% of patients, 42% of which were adenomas. Additionally, of the total number of polyps, 13% were villous or tubulovillous adenomas. Having observed such a high prevalence of advanced adenomas at 12 months (7.9% of patients), the authors raised the possibility that, instead of performing post-operative colonoscopy at 3 to 5 years, as recommended in then-current 2005 clinical practice guidelines for the prevention, early detection and management of CRCColorectal cancer,[14] a variably intense colonoscopy surveillance schedule might be justifiable. Similarly, a large study from Taipei[15] concluded that a lifelong schedule of postoperative colonoscopic surveillance was necessary.

According to Hassan et al,[16] who used a decision analysis model, early surveillance colonoscopy performed 1 year following CRCColorectal cancer resection was clinically efficient and cost-effective in terms of cancer detection and prevention of cancer-specific death.[16] Compared with 'no early colonoscopy' following surgery, the number of 1-year colonoscopies required to find one CRCColorectal cancer was 143 and the number needed to prevent one CRCColorectal cancer-related death was 926. In a 2007 analysis of 1002 operated CRCColorectal cancer patients, Rulyak et al[17] concluded that surveillance colonoscopy within one year of surgery was warranted because (i) 9 of the 20 metachronous cancers detected during the study period were found within 18 months of surgery and (ii) the rate of metachronous advanced neoplasia was significantly lower if colonoscopy was performed within 18 months of surgery (6.9 %) than if colonoscopy was delayed for 3 years or more (15.5 %).

In a 2009 study from China, Wang et al compared 'intensive colonoscopic surveillance' (3-monthly colonoscopy for the first year after surgery, then 6-monthly for the following 2 years and annually thereafter) with 'routine colonoscopic surveillance' (at 6, 30 and 60 months after surgery).[18] In the intensive surveillance group, one metachronous cancer was detected in the second year of surveillance, one in the fourth year and the third more than 5 years after initial surgery. In the routine surveillance group, no metachronous cancers were found at 6 months, four were found at 30 months, one was found at 5 years and one was found thereafter. The authors concluded that the routine schedule of surveillance was acceptable, with follow-up colonoscopy at one and two years after surgery and then 3 to 5 years thereafter.

Thus, while not all of the published evidence is in agreement, most studies demonstrate a significant incidence of metachronous cancers, advanced adenomas and other types of polyps after curative resection for CRCColorectal cancer. In many studies, a high proportion of the metachronous neoplasia was detected within the first 2 years after surgery.

Careful, high-quality colonoscopy at 12 months after surgery would be expected to detect the vast majority of metachronous neoplasia. In turn, this should improve survival in patients operated on for CRCColorectal cancer, by finding second cancers at a stage early enough to be cured by re-operation, and by removing metachronous adenomas while still benign. As a result, the weight of evidence from the literature would seem to support performing the initial postoperative surveillance colonoscopy at an interval of 1 year. If this examination does not reveal a metachronous cancer, the intervals between subsequent colonoscopies should probably be 3 and then 5 years, depending on the number, size and histologic type of polyps (if any) removed (see Colonoscopic surveillance after polypectomy).

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Overview of additional evidence (non-systematic review relevant literature)

The US guidelines for colonoscopy surveillance after cancer resection referenced in the last clinical practice guidelines[19] have since been updated to include additional data from 2005 to 2015.[20] The literature was summarised with regard to metachronous cancer development. Reporting pooled data from over 15,000 patients, 253 (1.6%) metachronous cancers were detected, 30% of these within 2 years of the index malignancy. While it could be argued that second cancers found so soon after surgery were in many instances missed synchronous (rather than metachronous) lesions, the importance of detecting them remains undiminished. Thus, the US Guidelines’ re-iterated previous recommendations to perform post-operative colonoscopy at an interval of 1 year (with subsequent colonoscopies after an interval of 3 years and then 5 years, if all surveillance examinations were normal).

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Evidence summary and recommendations

Evidence summary Level References
Follow-up colonoscopy reduces the mortality rate of patients after colorectal cancer (CRCColorectal cancer) resection. Most studies demonstrate a significant incidence of metachronous cancers, advanced adenomas and other types of polyps after curative resection for CRCColorectal cancer. II, III-2, III-3 [15], [17], [2], [4], [21], [22], [23], [24], [25], [3], [13], [16], [18]
In many studies, a high proportion of the metachronous neoplasia occurred within the first 2 years after surgery. III-3 [26]
Evidence-based recommendationA recommendation formulated after a systematic review of the evidence, indicating supporting references.Question mark transparent.png Grade
ColonoscopyAn examination of the large bowel using a camera on a flexible tube, which is passed through the anus. should be performed 1 year after the resection of a sporadic cancer, unless a complete postoperative colonoscopy has been performed sooner.

Recommendation unchanged from 2011 edition of clinical practice guidelines for surveillance colonoscopy.

C
Evidence-based recommendationA recommendation formulated after a systematic review of the evidence, indicating supporting references.Question mark transparent.png Grade
If the perioperative colonoscopy or the colonoscopy performed at 1 year reveals advanced adenoma, then the interval before the next colonoscopy should be guided by recommended surveillance intervals according to polyp features.

Recommendation unchanged from 2011 edition of clinical practice guidelines for surveillance colonoscopy.

C
Evidence-based recommendationA recommendation formulated after a systematic review of the evidence, indicating supporting references.Question mark transparent.png Grade
If the colonoscopy performed at 1 year is normal or identifies no advanced adenomas, then the interval before the next colonoscopy should be five 5 years (i.e. colonoscopies at 1, 6, and 11 years after resection).

Recommendation unchanged from 2011 edition of clinical practice guidelines for surveillance colonoscopy.

C
Consensus-based recommendationA recommendation formulated in the absence of quality evidence, after a systematic review of the evidence was conducted and failed to identify admissible evidence on the clinical question.Question mark transparent.png

If surveillance colonoscopy reveals adenoma, then the interval before the next colonoscopy should be guided by polyp features (evidence-based recommendation, Grade C). However, if subsequent colonoscopy is normal, then surveillance should revert back to the intervals recommended for initial cancer surveillance (colonoscopy at 6 and 11 years post resection).

Recommendation unchanged from 2011 edition of clinical practice guidelines for surveillance colonoscopy.

Consensus-based recommendationA recommendation formulated in the absence of quality evidence, after a systematic review of the evidence was conducted and failed to identify admissible evidence on the clinical question.Question mark transparent.png

If all colonoscopies performed at 1, 6 and 11 years post resection are normal, follow-up can be with either of the following options:

  • faecal occult blood test every 2 years
  • colonoscopy at 10 years (i.e. 21 years post resection)

Recommendation unchanged from 2011 edition of clinical practice guidelines for surveillance colonoscopy.

Practice pointA recommendation on a subject that is outside the scope of the search strategy for the systematic review, based on expert opinion and formulated by a consensus process.Question mark transparent.png

Patients undergoing either local excision (including transanal endoscopic microsurgery) of rectal cancer or advanced adenomas or ultra-low anterior resection for rectal cancer should be considered for periodic examination of the rectum at 6-monthly intervals for 2 or 3 years using either digital rectal examination, rigid proctoscopy, flexible proctoscopy, and/or rectal endoscopic ultrasound. These examinations are considered to be independent of the colonoscopic examination schedule described above

Practice pointA recommendation on a subject that is outside the scope of the search strategy for the systematic review, based on expert opinion and formulated by a consensus process.Question mark transparent.png

Patients with incomplete colonoscopy pre-operatively (e.g. impassable distal lesion) should have a semi-urgent elective post-operative colonoscopy when feasible, independent of surveillance intervals.

Practice pointA recommendation on a subject that is outside the scope of the search strategy for the systematic review, based on expert opinion and formulated by a consensus process.Question mark transparent.png

Surveillance colonoscopy in those age ≥75 years should be based on age and comorbidity as assessed by the reproducible and validated Charlson score. Charlson score is useful to assess life expectancy and could be implemented to stratify benefits of surveillance colonoscopy in the elderly (see Table 18. Charlson score for colonoscopy benefit).

Table 18. Charlson score for colonoscopy benefit
Age Medical conditions
75–79 years

(3 points for age)

May have one of these conditions only (1 point each):

Mild liver disease

Diabetes without end-organ damage

Cerebrovascular disease

Ulcer disease

Connective tissue disease

Chronic pulmonary disease

Dementia

Peripheral vascular disease

Congestive heart failure

Myocardial infarction

May not have any of these medical conditions

(≥1 point each):

Moderate/severe liver disease

Diabetes with end-organ damage

Hemiplegia

Moderate or severe renal disease

AIDS

MetastaticCancer that has spread from the primary site of origin (where it started) into different area(s) of the body. or non-metastatic solid organ or haematopoietic malignancy

80 years

(4 points for age)

May not have any of the above medical conditions
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Health system implications

Clinical practice

No significant effects on clinical practice are anticipated, because the evidence-based recommendations and consensus-based recommendations have not changed.

Resourcing

No significant effects on resource requirements are anticipated, because the evidence-based recommendations and consensus-based recommendations have not changed.

Barriers to implementation

No significant barriers to the implementation of these recommendations have been identified.

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References

  1. Cancer Council Australia ColonoscopyAn examination of the large bowel using a camera on a flexible tube, which is passed through the anus. Surveillance Working Party. Clinical Practice Guidelines for Surveillance Colonoscopy – in adenoma follow-up; following curative resection of colorectal cancer; and for cancer surveillance in inflammatory bowel disease. Sydney: Cancer Council Australia; 2011 Dec.
  2. 2.02.1 Barillari P, Ramacciato G, Manetti G, Bovino A, Sammartino P, Stipa V. Surveillance of colorectal cancer: effectiveness of early detection of intraluminal recurrences on prognosis and survival of patients treated for cure. Dis ColonThe main part of the large bowel, which absorbs water and electrolytes from undigested food (solid waste). Its four parts are the ascending colon, transverse colon, descending colon and sigmoid colon. RectumThe final section of the large bowel, ending at the anus. 1996 Apr;39(4):388-93 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/8878497.
  3. 3.03.1 Neugut AI, Lautenbach E, Abi-Rached B, Forde KA. Incidence of adenomas after curative resection for colorectal cancer. Am J Gastroenterol 1996 Oct;91(10):2096-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/8855728.
  4. 4.04.1 Togashi K, Konishi F, Ozawa A, Sato T, Shito K, Kashiwagi H, et al. Predictive factors for detecting colorectal carcinomas in surveillance colonoscopy after colorectal cancer surgery. Dis ColonThe main part of the large bowel, which absorbs water and electrolytes from undigested food (solid waste). Its four parts are the ascending colon, transverse colon, descending colon and sigmoid colon. RectumThe final section of the large bowel, ending at the anus. 2000 Oct;43(10 Suppl):S47-53 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/11052478.
  5. Juhl G, Larson GM, Mullins R, Bond S, Polk HC Jr. Six-year results of annual colonoscopy after resection of colorectal cancer. World J Surg ;14(2):255-60; discussion 260-1 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/2327099.
  6. 6.06.1 Khoury DA, Opelka FG, Beck DE, Hicks TC, Timmcke AE, Gathright JB Jr. Colon surveillance after colorectal cancer surgery. Dis ColonThe main part of the large bowel, which absorbs water and electrolytes from undigested food (solid waste). Its four parts are the ascending colon, transverse colon, descending colon and sigmoid colon. RectumThe final section of the large bowel, ending at the anus. 1996 Mar;39(3):252-6 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/8603543.
  7. Barrier A, Houry S, Huguier M. The appropriate use of colonoscopy in the curative management of colorectal cancer. Int J ColorectalReferring to the large bowel, comprising the colon and rectum. Dis 1998;13(2):93-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/9638495.
  8. Stigliano V, Fracasso P, Grassi A, Lapenta R, Citarda F, Tomaselli G, et al. Endoscopic follow-up in resected colorectal cancer patients. J Exp Clin Cancer Res 2000 Jun;19(2):145-8 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/10965809.
  9. Berman JM, Cheung RJ, Weinberg DS. Surveillance after colorectal cancer resection. Lancet 2000 Jan 29;355(9201):395-9 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/10665570.
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  11. Mathew J, Saklani AK, Borghol M. Surveillance colonoscopy in patients with colorectal cancer: how often should we be doing it? Surgeon 2006 Feb;4(1):3-5, 62 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/16459492.
  12. Yusoff IF, Hoffman NE, Ee HC. Colonoscopic surveillance after surgery for colorectal cancer. ANZ J Surg ;73(1-2):3-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/12534728.
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  14. Australian Cancer Network ColorectalReferring to the large bowel, comprising the colon and rectum. Cancer Guidelines Revision Committee. Clinical practice guidelines for the prevention, early detection and management of colorectal cancer. The Cancer Council Australia and Australian Cancer Network 2005.
  15. 15.015.1 Lan YT, Lin JK, Li AF, Lin TC, Chen WS, Jiang JK, et al. Metachronous colorectal cancer: necessity of post-operative colonoscopic surveillance. Int J ColorectalReferring to the large bowel, comprising the colon and rectum. Dis 2005 Mar;20(2):121-5 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/15349739.
  16. 16.016.116.2 Hassan C, Pickhardt PJ, Di Giulio E, Kim DH, Zullo A, Morini S. Cost-effectiveness of early one-year colonoscopy surveillance after polypectomy. Dis ColonThe main part of the large bowel, which absorbs water and electrolytes from undigested food (solid waste). Its four parts are the ascending colon, transverse colon, descending colon and sigmoid colon. RectumThe final section of the large bowel, ending at the anus. 2009 May;52(5):964-71; discussion 971 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/19502863.
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  20. Kahi CJ, Boland CR, Dominitz JA, Giardiello FM, Johnson DA, Kaltenbach T, et al. Colonoscopy surveillance after colorectal cancer resection: recommendations of the US multi-society task force on colorectal cancer. Gastrointest Endosc 2016 Mar;83(3):489-98.e10 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/26802191.
  21. Hassan C, Gaglia P, Zullo A, Scaccianoce G, Piglionica D, Rossini FP, et al. Endoscopic follow-up after colorectal cancer resection: an Italian multicentre study. Dig Liver Dis 2006 Jan;38(1):45-50 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/16216566.
  22. Fisher DA, Jeffreys A, Grambow SC, Provenzale D. Mortality and follow-up colonoscopy after colorectal cancer. Am J Gastroenterol 2003 Apr;98(4):901-6 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/12738475.
  23. Lieberman DA, Weiss DG, Harford WV, Ahnen DJ, Provenzale D, Sontag SJ, et al. Five-year colon surveillance after screening colonoscopy. Gastroenterology 2007 Oct;133(4):1077-85 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/17698067.
  24. Unger SW, Wanebo HJ. Colonoscopy: an essential monitoring technique after resection of colorectal cancer. Am J Surg 1983 Jan;145(1):71-6 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/6849497.
  25. Eckardt VF, Stamm H, Kanzler G, Bernhard G. Improved survival after colorectal cancer in patients complying with a postoperative endoscopic surveillance program. Endoscopy 1994 Aug;26(6):523-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/7828564.
  26. Bouvier AM, Latournerie M, Jooste V, Lepage C, Cottet V, Faivre J. The lifelong risk of metachronous colorectal cancer justifies long-term colonoscopic follow-up. Eur J Cancer 2008 Mar;44(4):522-7 Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/18255278.

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Appendices

Jutta's magnifying glass icon.pngPICO question FUC1 View Systematic review report FUC1Systematic review report FUC1
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