First surveillance intervals following removal of high-risk conventional adenomas only
Individuals at high risk are those who have had one or more conventional (tubular, tubulovillous or villous) adenomas removed at the baseline colonoscopy with one or more of the following four features:
- size ≥10mm*
- high-grade dysplasia (HGD)
- 3–4 adenomas.
*Adenomas ≥20mm are more likely to be excised piecemeal. For surveillance intervals for patients following removal of adenomas ≥20mm, see First surveillance intervals following removal of large sessile or laterally spreading adenomas.
For surveillance intervals for patients following removal of ≥5 conventional adenomas, see First surveillance intervals following removal of ≥5 conventional adenomas only (SAD5).
For surveillance intervals for clinically significant serrated polyps with or without synchronous conventional adenomas, see First surveillance intervals following removal of serrated polyps (± conventional adenomas).
The 2011 edition of this guideline recommended surveillance at 3 years for individuals following removal at baseline colonoscopy of adenomas with any of the following characteristics: size ≥10mm, HGD, villosity, 3–4 adenomas. The 2018 recommendations are based on systematic review, non-systematic review of relevant literature, international recommendations and expert opinion.
What should be the first surveillance interval following removal of high-risk conventional adenomas only (size ≥10mm, HGD, villosity and/or 3-4 adenomas)? [SAD2]
Systematic review evidence[edit source]
The systematic review included studies published since 2010 of colonoscopic procedures performed from 2002.
Four level II prospective and ten level III-2 retrospective cohort studies were included. Nine studies had a high risk of bias and five studies had a moderate risk of bias. Outcomes reported included incidence and risk of metachronous colorectal cancer (CRC), metachronous adenoma (MA) and metachronous advanced adenoma (MAA). Surveillance intervals ranged from less than 3 years to 3–5 years. None of the included studies reported follow up at 10 years or CRC mortality. Most studies consistently reported the risk of metachronous colorectal cancer and MA. The reporting of MAA was more variable. The evidence was probably generalisable to the Australian population and applicable to the Australian healthcare system with some caveats.
At variable surveillance intervals less than 3 years and between 3–5 years:
- Incidence of metachronous CRC ranged from 0–1.52%
- Incidence of MAA varied within the range of 2.40–24.24%
The evidence base is limited for outcomes in individuals after removal of high-risk adenomas, particularly high-quality studies with long-term outcomes using modern endoscopy techniques.
Overview of additional evidence (non-systematic literature review)[edit source]
Long-term outcomes[edit source]
Five level III-2 studies reported long-term CRC incidence and mortality following adenoma removal in high-risk groups (Table 5) but were not included in the systematic review as they did not fit the criteria, particularly as they included colonoscopies performed prior to 2002.
Three level III-2 studies reported long-term CRC incidence:
- Cottet et al reported on a French retrospective cohort (n=5779). Participants had incident high-risk adenomas removed between 1990 and 1999 and were followed up using registry data until 31/12/2003, for a median of 7.7 years (interquartile range [IQR] 5.2–10.5). The overall standardised incidence ratio (SIR) of CRC was 2.23 (1.67–2.92): 1.10 (0.62–1.82) with surveillance colonoscopy and 4.26 (2.89–6.04) without. The 10-year cumulative incidence of CRC was 2.05% (1.14–3.64) with and 6.22% (4.26–9.02) without surveillance colonoscopy.
- Brenner et al performed a large case-control study in Germany, identifying cases of CRC (n=2582) and controls (n=1798) from the population registry matched for age, sex and location. Patients who had had a colonoscopy with removal of a polyp with high-risk features had a reduced adjusted odds ratio (OR) of CRC at any site, proportional to time since polypectomy: 0.3 (0.3–0.7) for <3 years, 0.5 (0.3–0.8) for 3–5 years and 1.1 (0.5–2.6) for 6–10 years, compared to no colonoscopy (OR 1.0).
- Atkin et al looked at long-term incidence of CRC in those with 3–4 small adenomas and 1–2 adenomas at least one of which was ≥10mm (n=11,944) and compared it to age- and sex-standardised incidence from the general population. Years of entry were 1990–2010, with censoring in 2014 and median follow-up of 7.9 years (IQR 5.6–11.1). After adjustment for baseline risk factors, CRC incidence in the whole cohort was not significantly different from that of the general population (SIR 1.09, 95% confidence interval [CI] 0.91–1.30). Compared with no surveillance (hazard ratio [HR] 1), one surveillance visit at median 2.9 years (IQR 1.3–3.4) was associated with a significant reduction in colorectal cancer incidence (HR 0.57, 95% CI 0.40–0.80), two visits HR 0.51 (0.31–0.84) and three or more visits HR 0.54 (0.29–0.99); p=0.0029 for any surveillance visit, compared with no surveillance.
Two level III-2 studies reported CRC-specific mortality:
- Zauber et al compared CRC-specific mortality in participants (n=2602) who had adenomatous polyps removed in the US National Polyp Study between 1980 and 1990 with standardised incidence-based CRC-specific mortality in the general population using Surveillance Epidemiology and End Results (SEER) data. Patients with low- and high-risk adenomas were included, with 57.3% advanced adenomas and 19.3% ≥3 adenomas. Median follow-up was 15.8 years, with maximum of 23 years. Overall, standardised mortality ratio (SMR) was 0.47 (0.26–0.80). The risk of CRC mortality of those with adenomas removed was the same as those with non-adenomatous polyps at 10 years. Cumulative CRC-specific mortality at 20 years was 0.8% for the National Polyp Study patients versus 1.5% in the general population. Mortality reduction was similar for the first 10 years of follow-up at 0.44 (0.14–1.06, p=0.09) compared with 10 or more years at 0.49 (0.23–0.93, p=0.04).
- Løberg et al followed n=40,826 individuals after adenoma removal during 1993–2007 and compared CRC-specific mortality with the general population up to 2011, with a median follow-up of 7.7 years (maximum 19 years). As per Norwegian Guidelines, a surveillance of 10 years is recommended for those with high-risk adenomas. The CRC-specific SMR was 1.16 (1.02–1.31).
Influence of high-risk features (size ≥10mm, HGD, villosity, 3-4 adenomas)[edit source]
Size distinguishes low risk (<10mm) and high risk (≥10mm) for metachronous adenoma (MA), with further division more recently into adenomas of 6–9mm (small) and 1–5mm (diminutive). Size correlates with advanced histology (villosity and/or HGD).
A recent review highlights the variability in the literature but summarises findings as “adenoma size ≥10mm appears to be associated with future advanced neoplasia and the magnitude of risk increases for larger adenomas ≥20mm in size.” A meta-analysis reported an OR for metachronous neoplasia (MN) of 2.24 (1.4–3.59) comparing various smaller adenomas with those ≥10mm, generally at median follow-up intervals between 17 months and 16 years. On multivariate analysis, Atkin et al found that adenoma size 10–19mm (HR 1.97; 1.01–3.81) and ≥20mm (HR 2.28; 1.16–4.50) was associated with increased incidence of CRC when compared with <10mm, at median follow-up of 7.9 years. Potential difficulty in interpreting the literature may arise from inconsistency in the measurement of adenoma size, which has been shown to be inconsistent among endoscopists.
High-grade dysplasia[edit source]
The question of whether HGD is associated with MN has been challenged by histologic consistency of reporting, separating the influence of size and villosity and population heterogeneity. Accordingly, the British guidelines do not incorporate HGD when considering surveillance intervals. Despite some variability, recent literature indicates an independent association between HGD and MN. A meta-analysis reported a multivariate relative risk (RR) of 2.04 (1.10–3.78) for HGD in the index adenoma predicting MN at median follow-up between 17 months and 16 years. Facciorusso et al reported a multivariate OR of 4.25 (2.11–7.5) for MAA at 3 years, whereas van Heijningen et al reported a RR for metachronous advanced neoplasia (MAN) of 1.9 (1.3–2.7) on univariate but 1.3 (0.9–1.9) on multivariate analysis at median follow up of 35 months. Taniguchi reported an OR 2.4 (1.51–3.83) for HGD versus low-grade dysplasia (LGD) in the largest adenoma for MA at follow up within 2 years on multivariate analysis. Another systematic review reported a small and variable association of HGD with risk of metachronous advanced neoplasia in a systematic review. Most recently, Atkin et al found a HR of 1.69 (1.21–2.36) for HGD versus LGD for incident CRC following removal of intermediate risk adenomas at median follow-up of 7.9 years. High-grade dysplasia is less common in diminutive polyps, with an incidence of around 0.1–0.3%, and 0.3–0.8% in small adenomas. The metachronous neoplasia risk is unclear, but is likely to be low.
The association of villosity with MN has been complicated by factors that make it difficult to compare outcomes between studies. These include variability in histologic diagnosis (the change in the World Health Organization definition in 2010 of 'villosity' from 20% to 25% villous component being particularly relevant), and different outcome definitions (sometimes tubulovillous and villous, at other times one or the other). Differing length of follow-up may also partially explain variation. Such is the uncertainty about the significance of villosity, that the British guidelines do not incorporate villosity when considering surveillance intervals.
Recent literature generally indicates that villosity is an independent predictor for MN. A meta-analysis reported a multivariate-adjusted OR 1.77 (1.16–2.71) for MN at median follow-up of between 17 months and 16 years, whilst another concluded that villous histology within an adenoma may have a small association with future advanced neoplasia but this was not seen uniformly across all studies. In individual studies:
- Facciorusso et al reported an OR for MAA of 1.49 (0.47–5.18) on univariate analysis and 1.73 (0.68–4.45) on multivariate analysis at 3 years.
- Taniguchi reported an OR of 2.07 (1.59–2.70) on univariate analysis but 1.56 (0.98–2.52) on multivariate analysis at follow-up within 2 years.
- van Heijningen found villous histology significant on univariate and multivariate analysis at follow-up intervals of between less than 4 years and more than 6 years, with an OR of 2.3 (1.4–3.6).
- Atkin et al did not find villosity to be associated with metachronous CRC, with a HR of 1.16 (0.71–1.91) on multivariate analysis at median 7.9 years follow-up.
Increasing number of adenomas at baseline is associated with MN. A recent meta-analysis reported a RR of 2.32 (95% CI 1.81, 2.98) when comparing 1 to ≥2 baseline adenomas. An often-quoted large study of pooled trial data from 2009 described a relatively high risk of MAA within 3–5 years at 8.6%, 12.7%, 15.2%, 19.6% and 24.1% for one, two, three, four and five adenomas, respectively. Of note, the included trials recruited from the 1980s and 1990s in the era of lower quality colonoscopy.
More recent studies have shown much lower rates of MAA. In one study the incidence of MAA was 5.8% following removal of 3–4 non-advanced adenomas at baseline colonoscopy (n=291) at 4.0±1.3 years. Another showed the incidence of MAA to be 3.5% after removal of 1–2 diminutive adenomas, compared with 6.3% after 3–9 diminutive adenomas; and 9.8% following removal of both 1–2 and 3–9 small (6-9mm) adenomas at a median of 32 months (IQR 13–48). In another study, the risk of MAA was 11.9% in patients with 3–10 adenomas after follow-up of 4.0 years.
Although the relationship between number at baseline colonoscopy and MN is consistent across most literature, Atkin et al demonstrated a non-significant (p=0.12) multivariate HR of 0.58 (95% CI 0.31–1.11) for 3 or 4 adenomas compared to 1, perhaps suggesting an effect of higher quality colonoscopy with the detection of more adenomas.
3–4 small adenomas or 1–2 adenomas with one ≥10mm without advanced histologic features[edit source]
Several recent papers have investigated at whether, following removal of high-risk adenomas, a sub-group of patients may be at lesser risk. In the first study, institutional data from 2002–2012 were analysed, finding a 1.8% risk of MAA following removal of 3–4 adenomas all less than 10mm; compared with a risk of 8.6% at a mean of 3.28±1.75 years, when the size of at least one adenoma was ≥10mm.
In the second study, Atkin et al assessed long-term outcomes of standardised CRC incidence against a population reference in patients following removal of 3–4 small adenomas or 1–2 adenomas, one of which was ≥10mm (these included advanced histologic features as per British guidelines). Colorectal cancer incidence in these patients, regardless of follow-up, was not significantly different from that of the general population (SIR 1.09, 95% CI 0.91–1.30).
A retrospective, multicentre cohort study included patients recruited between 2007 and 2008 with ≥3 adenomas or one or more adenomas ≥10mm, stratified according to the British Guidelines. In the group with 3–4 non-advanced adenomas (n=291), at 4.0±1.3 years the incidence of MAA was 5.8% and CRC 0.3%.
Cumulative risk in patients with multiple high-risk factors detected[edit source]
Several groups have recently looked at the impact of multiple high-risk findings. A group from Korea retrospectively (2005–2009) analysed data for 862 individuals, with high-risk factors: size ≥10mm, HGD, villosity and ≥3 adenomas. The cumulative incidence of MAN was associated with the number of high-risk findings. At 5 years, MAN rates were 8.5% with no high-risk findings, 18.7% with one, 26.3% with two, and 37.2% with three or four high-risk findings, with the number needed to treat to find a single MAA at 3 years being 8.4, 6.5 and 4.1 for one, two and three to four factors, respectively. At 1 and 2 years for those with three to four factors, needed to treat was 12.5 and 6.6, respectively.
A Japanese group combined metabolic factors (age ≥65 years, BMI>25, fasting blood glucose >126 mg/dL) and adenoma predictors (HGD, villosity, right sided location, largest adenoma diameter ≥10mm, number removed ≥3) into a risk score from 0–10 points. The risk of adenoma recurrence increased as the risk score increased, with an OR of 7.07 for those with a score of 0–2 compared with those with a score of 3–10 (95% CI 5.30–9.43).
van Heijningen et al developed a simple risk score from 0 to 5 which was predictive of MAN and incorporated into the Dutch Surveillance Guidelines. The score consists of characteristics contributing 1 point (size ≥10mm, villous histology, proximal location, having 2–4 adenomas) or 2 points (having ≥5 adenomas). Although not yet externally validated, the score has been modelled with a c-statistic of 0.71, which is better than that of the British Society of Gastroenterology (BSG) (2010) guidelines (0.674; 0.634–0.713) and American Gastroenterological Association (AGA) (2012) guidelines (0.664; 0.625–0.703).
The risk for diminutive adenomas with advanced histologic features is poorly defined but seems low. Such adenomas are very rare.
Expert opinion and clinical practice guidelines from other countries[edit source]
The definition of ‘high risk’ varies amongst clinical practice guidelines from other countries, with previous Australian guidelines having both moderate- and high-risk categories. Similarly, in the BSG, European and New Zealand guidelines, 3–4 adenomas are split from ≥5 adenomas, with the BSG and NZ guidelines including 3–4 adenomas with at least one ≥10mm in the highest risk category.
A comparison of the AGA versus BSG guidelines using pooled trial data showed a risk of MAN at 1 year of 18.7% (14.8–22.5%) in this highest risk group. By contrast, Lee reports the 12-month follow-up of the high-risk group from the UK National Health Service Bowel Cancer Screening Programme, where the risk of MAN was lower, at 6.6%. The European guidelines incorporate ≥5 adenomas and size ≥20mm in the highest risk group, giving no special consideration to the ≥10 adenomas group. More than 10 adenomas are recognised in the AGA guidelines and Canadian Association of Gastroenterology guidelines as requiring surveillance at 1-year recommendation.
The Norwegian guidelines recommend surveillance at 10 years for patients with 1–2 adenomas, despite the presence of HGD or villous features or size ≥10mm.
A recent study based on long-term data from the Norwegian registry reported SMR for 40826 patients who had had adenomas removed. For, the high-risk group, CRC-specific SMR was 1.16 (1.02-1.31) implying a surveillance interval of 10 years was adequate to reduce the SMR to just above average population risk, but inadequate to reduce it to or below average population risk.
In the Dutch surveillance programme, based on the personalised risk score developed by van Heijningen et al a surveillance interval of 3 years is recommended for those with a score of 3–5, while a surveillance interval of 5 years is recommended for those with a risk score of 1–2.
Evidence summary and recommendations[edit source]
|The nine cohort studies of high-risk patients in whom surveillance was performed at 3–5 years reported an incidence of metachronous CRC of 0.00% to 1.52%.||II, III-2||, , , , , , , , |
|Surveillance time primarily ranged between 3 and 5 years amongst the seven cohort studies that reported incidence of any adenoma in patients with high-risk adenomas. Adenoma incidence ranged from 36.63% to 69.71% across the seven studies.||II, III-2||, , , , , , |
|Incidence of metachronous advanced adenoma was not consistent among the 10 cohort studies and ranged from 2.40% to 24.24%. Surveillance time varied across these studies, with five studies reporting surveillance within 3 years, and seven studies reporting surveillance within 3–5 years.||II, III-2||, , , , , , , , , |
Surveillance intervals should be determined after the colon has been cleared of all significant neoplasia, once histology is known, and in the context of individualised assessment of benefit to the patient.
Consistently high-quality colonoscopy is imperative for optimal cost effectiveness and for implementation of uniform surveillance guidelines.
Polyps removed at colonoscopy should be sent separately for histology to guide surveillance recommendations.
Clinicians should accurately include features relevant to surveillance intervals in their procedure reports so that individualised surveillance recommendations can be made.
Notes on the recommendations[edit source]
The systematic review supported surveillance within 5 years following removal of high-risk conventional adenomas but did not offer guidance on intervals within this broad timeframe. General review of the literature assessed high-risk features and suggested that combinations of these features might guide further stratification relevant to clinical practice.
The recommendations are based on the expectation that endoscopists in Australia are performing high-quality colonoscopy with complete adenoma excision and are supported by accurate pathology reporting.
The consensus-based recommendations are supported by the following key findings in the literature:
- Following removal of high-risk conventional adenomas, individuals require surveillance to reduce CRC incidence and CRC-specific mortality to levels at or just above population level.
- Whilst combinations of high-risk features are associated with an increased risk of metachronous neoplasia, subgroups of high-risk individuals seem to be at lesser risk. These lesser risk sub-groups include:
(i) those in whom 3–4 small tubular adenomas without HGD have been removed, and
(ii) those in whom 1–2 tubular adenomas without HGD have been removed, one of which is ≥10mm.
The recommendation for a 5-year surveillance interval following the removal of 3–4 low-risk adenomas without HGD is consistent with this recognition and attempts to counteract the 'paradoxical' impact that high quality colonoscopy (with detection of multiple small adenomas) would otherwise have on the number of and intervals between surveillance procedures. It represents a reduction in frequency, compared with the 2011 Australian clinical practice guidelines for surveillance colonoscopy.
Expert opinion and guidelines from other countries vary in their definitions of the high-risk group, with a trend towards separating off an intermediate risk group from those at highest risk (Table 4 Summary of international surveillance guidelines). Associated with this, there is variability in the corresponding surveillance interval recommendations. For the highest-risk group (albeit variably defined), a shorter surveillance interval of 1 year is recommended. Otherwise, a 3-year interval is recommended.
The British guidelines differ in that they make surveillance recommendations based on size and number alone.
Table 3. Summary of recommendations for first surveillance intervals following removal of conventional adenomas only
Health system implications[edit source]
Clinical practice[edit source]
These surveillance guidelines will result in substantial change to which health care providers will need to adjust. The aim of Table 3 and colour-coding in this section is to facilitate transition from the old to new guidelines. An educational program and simple decision aids, such as wall charts and online decision tools, would help healthcare provider become familiar with the recommendations for surveillance intervals. These could be developed, promoted and distributed in conjunction with the relevant professional bodies and healthcare providers in the public and private domains.
The management of surveillance following removal of adenomas is critical in terms of health outcomes, demand for colonoscopy and cost. Recently, the Cancer Research Division, Cancer Council NSW used the Australian developed and validated model Policy1-Bowel to compare the new and previous surveillance guidelines specifically related to the National Bowel Cancer Screening Program. Preliminary results demonstrate comparable health outcomes, reduced number of surveillance colonoscopies and similar program-related costs (see the preliminary results report on Modelled comparison of proposed surveillance recommendations for the NBCSP)
There is likely to be an increased cost for pathologic assessment if a substantial proportion of health care providers do not currently submit all polyps removed for pathologic assessment or do not separate specimens.
Barriers to implementation[edit source]
The main barrier for implementation of these recommendations will be dissemination across Australia and familiarisation for healthcare providers. This will be facilitated by a coordinated implementation and evaluation programme.
Colorectal cancer incidence and mortality after adenoma removal[edit source]
Table 5. Colorectal cancer incidence and mortality after adenoma removal
|Up to 10 years||Adjusted OR for CRC incidence at follow-up after polypectomy:
<3 years: 0.2 (0.2–0.3), 3–5 years: 0.4 (0.3–0.6)
6–10 years: 0.9 (0.5–1.5) for low- and high-risk adenomas
cohort and registry
SIR 0.68 (0.44-0.99) regardless of follow-up;
SIR 0.60 (0.30-1.07) with a single follow-up colonoscopy
10-year cumulative probability of CRC was 0.76% (0.39–1.48) with and 1.37% (0.70–2.65) without surveillance colonoscopy.
SIR 2.23 (1.67–2.92): 1.10 (0.62–1.82) with follow-up 4.26 (2.89–6.04) without;
10-year cumulative probability 2.05% (1.14–3.64) with 6.22% (4.26–9.02) without surveillance colonoscopy
Retrospective cohort study
|Incident adenomas 1990–2010
Follow-up through 2014
|3–4 small adenomas or 1–2 adenomas, at least one of which is ≥10mm
After adjustment for baseline risk factors, CRC incidence in the whole cohort was not significantly different from that of the general population (SIR 1.09, 95% CI 0.91–1.30); compared with no surveillance, one surveillance visit at median 2.9 years (IQR 1.3–3.4), was associated with a significant reduction in CRC incidence rate (HR 0.57, 95% CI 0.40–0.80).
|Low-risk group (no surveillance colonoscopy)
SMR 0.75 (0.63–0.88)
|High-risk group (surveillance colonoscopy every 10 years)
SMR 1.16 (1.02–1.31)
|Removal of the first adenoma
1993–1999: SMR 1.17 (1.03–1.33) vs. 2000–2007: 0.76 (0.65–0.89)
|SMR 0.47 (0.26–0.80) cumulative mortality at 20 years 0.8 vs. 1.5% in general population. The risk of CRC mortality of those with adenomas removed was the same as those without adenomas at 10 years.|
|Abbreviations: CI: Confidence interval; CRC: colorectal cancer; HR: hazard ratio; IQR: interquartile range; OR: odds ratio; SIR: standardised incidence ratio; SMR: standardised mortality ratio; UK: United Kingdom; USA: United States of America|
- ↑ 1.0 1.1 1.2 Cancer Council Australia Colonoscopy 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.
- ↑ 2.0 2.1 2.2 Bjerrum A, Milter MC, Andersen O, Fischer A, Lynge E. Risk stratification and detection of new colorectal neoplasms after colorectal cancer screening with faecal occult blood test: experiences from a Danish screening cohort. Eur J Gastroenterol Hepatol 2015 Dec;27(12):1433-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26352132.
- ↑ 3.0 3.1 3.2 3.3 Chung SJ, Kim YS, Yang SY, Song JH, Kim D, Park MJ, et al. Five-year risk for advanced colorectal neoplasia after initial colonoscopy according to the baseline risk stratification: a prospective study in 2452 asymptomatic Koreans. Gut 2011 Nov;60(11):1537-43 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21427200.
- ↑ 4.0 4.1 4.2 4.3 Chiu HM, Lee YC, Tu CH, Chang LC, Hsu WF, Chou CK, et al. Effects of metabolic syndrome and findings from baseline colonoscopies on occurrence of colorectal neoplasms. Clin Gastroenterol Hepatol 2015 Jun;13(6):1134-42.e8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25445768.
- ↑ 5.0 5.1 5.2 5.3 Huang Y, Li X, Wang Z, Su B. Five-year risk of colorectal neoplasia after normal baseline colonoscopy in asymptomatic Chinese Mongolian over 50 years of age. Int J Colorectal Dis 2012 Dec;27(12):1651-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22763754.
- ↑ Kim NH, Park JH, Park DI, Sohn CI, Choi K, Jung YS. Metabolic syndrome is a risk factor for adenoma occurrence at surveillance colonoscopy: A single-center experience in Korea. Medicine (Baltimore) 2016 Aug;95(32):e4454 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27512862.
- ↑ 7.0 7.1 7.2 7.3 Lee JL, Cha JM, Lee HM, Jeon JW, Kwak MS, Yoon JY, et al. Determining the optimal surveillance interval after a colonoscopic polypectomy for the Korean population? Intest Res 2017 Jan;15(1):109-117 Available from: http://www.ncbi.nlm.nih.gov/pubmed/28239321.
- ↑ 8.0 8.1 Lee SM, Kim JH, Sung IK, Hong SN. The risk of metachronous advanced colorectal neoplasia rises in parallel with an increasing number of high-risk findings at baseline. Gut and Liver 2015;9(6):741-9.
- ↑ 9.0 9.1 9.2 9.3 Melson J, Ma K, Arshad S, Greenspan M, Kaminsky T, Melvani V, et al. Presence of small sessile serrated polyps increases rate of advanced neoplasia upon surveillance compared with isolated low-risk tubular adenomas. Gastrointest Endosc 2016 Aug;84(2):307-14 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26855297.
- ↑ 10.0 10.1 10.2 10.3 Tae CH, Moon CM, Kim SE, Jung SA, Eun CS, Park JJ, et al. Risk factors of nonadherence to colonoscopy surveillance after polypectomy and its impact on clinical outcomes: a KASID multicenter study. J Gastroenterol 2016 Nov 9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27830330.
- ↑ 11.0 11.1 11.2 11.3 11.4 Vemulapalli KC, Rex DK. Risk of advanced lesions at first follow-up colonoscopy in high-risk groups as defined by the United Kingdom post-polypectomy surveillance guideline: data from a single U.S. center. Gastrointest Endosc 2014 Aug;80(2):299-306 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24796960.
- ↑ 12.0 12.1 Jang HW, Park SJ, Hong SP, Cheon JH, Kim WH, Kim TI. Risk Factors for Recurrent High-Risk Polyps after the Removal of High-Risk Polyps at Initial Colonoscopy. Yonsei Med J 2015 Nov;56(6):1559-65 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26446637.
- ↑ Lee JY, Park HW, Kim MJ, Lee JS, Lee HS, Chang HS, et al. Prediction of the Risk of a Metachronous Advanced Colorectal Neoplasm Using a Novel Scoring System. Dig Dis Sci 2016 Oct;61(10):3016-3025 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27358228.
- ↑ 14.0 14.1 Lee TJ, Nickerson C, Goddard AF, Rees CJ, McNally RJ, Rutter MD. Outcome of 12-month surveillance colonoscopy in high-risk patients in the National Health Service Bowel Cancer Screening Programme. Colorectal Dis 2013 Aug;15(8):e435-42 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23663559.
- ↑ 15.0 15.1 15.2 15.3 Park SK, Kim NH, Jung YS, Kim WH, Eun CS, Ko BM, et al. Risk of developing advanced colorectal neoplasia after removing high-risk adenoma detected at index colonoscopy in young patients: A KASID study. J Gastroenterol Hepatol 2016 Jan;31(1):138-44 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26404417.
- ↑ 16.0 16.1 Cottet V, Jooste V, Fournel I, Bouvier AM, Faivre J, Bonithon-Kopp C. Long-term risk of colorectal cancer after adenoma removal: a population-based cohort study. Gut 2012 Aug;61(8):1180-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22110052.
- ↑ Brenner H, Chang-Claude J, Jansen L, Seiler CM, Hoffmeister M. Role of colonoscopy and polyp characteristics in colorectal cancer after colonoscopic polyp detection: a population-based case-control study. Ann Intern Med 2012 Aug 21;157(4):225-32 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22910933.
- ↑ 18.0 18.1 18.2 18.3 18.4 18.5 18.6 Atkin W, Wooldrage K, Brenner A, Martin J, Shah U, Perera S, et al. Adenoma surveillance and colorectal cancer incidence: a retrospective, multicentre, cohort study. Lancet Oncol 2017 Jun;18(6):823-834 Available from: http://www.ncbi.nlm.nih.gov/pubmed/28457708.
- ↑ 19.0 19.1 Zauber AG, Winawer SJ, O'Brien MJ, Lansdorp-Vogelaar I, van Ballegooijen M, Hankey BF, et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med 2012 Feb 23;366(8):687-96 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22356322.
- ↑ 20.0 20.1 20.2 Løberg M, Kalager M, Holme Ø, Hoff G, Adami HO, Bretthauer M. Long-term colorectal-cancer mortality after adenoma removal. N Engl J Med 2014 Aug 28;371(9):799-807 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25162886.
- ↑ 21.0 21.1 21.2 Calderwood AH, Lasser KE, Roy HK. Colon adenoma features and their impact on risk of future advanced adenomas and colorectal cancer. World J Gastrointest Oncol 2016 Dec 15;8(12):826-834 Available from: http://www.ncbi.nlm.nih.gov/pubmed/28035253.
- ↑ 22.0 22.1 22.2 Jayasekara H, Reece JC, Buchanan DD, Ahnen DJ, Parry S, Jenkins MA, et al. Risk factors for metachronous colorectal cancer or polyp: A systematic review and meta-analysis. J Gastroenterol Hepatol 2017 Feb;32(2):301-326 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27356122.
- ↑ Anderson BW, Smyrk TC, Anderson KS, Mahoney DW, Devens ME, Sweetser SR, et al. Endoscopic overestimation of colorectal polyp size. Gastrointest Endosc 2016 Jan;83(1):201-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26318830.
- ↑ 24.0 24.1 24.2 Cairns SR, Scholefield JH, Steele RJ, Dunlop MG, Thomas HJ, Evans GD, et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 2010 May;59(5):666-89 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20427401.
- ↑ Facciorusso A, Di Maso M, Serviddio G, Vendemiale G, Muscatiello N. Development and validation of a risk score for advanced colorectal adenoma recurrence after endoscopic resection. World J Gastroenterol 2016 Jul 14;22(26):6049-56 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27468196.
- ↑ 26.0 26.1 26.2 van Heijningen EM, Lansdorp-Vogelaar I, van Hees F, Kuipers EJ, Biermann K, de Koning HJ, et al. Developing a score chart to improve risk stratification of patients with colorectal adenoma. Endoscopy 2016 Jun;48(6):563-70 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27167762.
- ↑ 27.0 27.1 Taniguchi R, Takahashi H, Endo H, Nakajima A. Risk of colorectal cancer after detection and removal of adenomas at colonoscopy. Transl Gastroint Cancer 2013 Jan;2(1):4-5 Available from: http://www.amepc.org.
- ↑ Jeong YH, Kim KO, Park CS, Kim SB, Lee SH, Jang BI. Risk Factors of Advanced Adenoma in Small and Diminutive Colorectal Polyp. J Korean Med Sci 2016 Sep;31(9):1426-30 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27510386.
- ↑ Chiu HM, Chang LC, Shun CT, Wu MS, Wang HP. Current management of diminutive colorectal polyps in Taiwan. Dig Endosc 2014 Apr;26 Suppl 2:64-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24750151.
- ↑ Ponugoti PL, Cummings OW, Rex DK. Risk of cancer in small and diminutive colorectal polyps. Dig Liver Dis 2017 Jan;49(1):34-37 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27443490.
- ↑ Bosman FT, Carneiro F, Hruban R H, Theise N. WHO classification of tumours of the digestive system, fourth edition. France: IARC; 2010 [cited 2018 Jul 10] Available from: http://www.ncbi.nlm.nih.gov/nlmcatalog/101553728.
- ↑ Klein A, Jayasekeran V, Hourigan LF, Tate DJ, Singh R, Brown GL et. 812b A Multi-Center Randomized Control Trial of ThermalAablation of the Margin of the Post Endoscopic Mucosal Resection (EMR) Mucosal Defect in the Prevention of Adenoma Recurrence Following EMR: Preliminary Results from the “SCAR” Study. Gastroenterology 2016 Available from: http://www.gastrojournal.org/article/S0016-5085(16)34279-2/pdf.
- ↑ Facciorusso A, Di Maso M, Serviddio G, Vendemiale G, Spada C, Costamagna G, et al. Factors Associated With Recurrence of Advanced Colorectal Adenoma After Endoscopic Resection. Clin Gastroenterol Hepatol 2016 Aug;14(8):1148-1154.e4 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27005802.
- ↑ Martínez ME, Baron JA, Lieberman DA, Schatzkin A, Lanza E, Winawer SJ, et al. A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy. Gastroenterology 2009 Mar;136(3):832-41 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19171141.
- ↑ 35.0 35.1 35.2 Park SK, Song YS, Jung YS, Kim WH, Soo Eun C, Ko BM, et al. Do surveillance intervals in patients with more than five adenomas at index colonoscopy be shorter than those in patients with three to four adenomas? A Korean Association for the Study of Intestinal Disease study. J Gastroenterol Hepatol 2017 May;32(5):1026-1031 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27862272.
- ↑ 36.0 36.1 Sneh Arbib O, Zemser V, Leibovici Weissman Y, Gingold-Belfer R, Vilkin A, Eizenstein S, et al. Risk of advanced lesions at the first follow-up colonoscopy after polypectomy of diminutive versus small adenomatous polyps of low-grade dysplasia. Gastrointest Endosc 2017 Mar 8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/28284884.
- ↑ 37.0 37.1 Park SK, Hwang SW, Kim KO, Cha JM, Boo SJ, Shin JE, et al. Risk of advanced colorectal neoplasm in patients with more than 10 adenomas on index colonoscopy: A Korean Association for the Study of Intestinal Diseases (KASID) study. J Gastroenterol Hepatol 2017 Apr;32(4):803-808 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27785837.
- ↑ Taniguchi L, Higurashi T, Uchiyama T, Kondo Y, Uchida E, Uchiyama S, et al. Metabolic factors accelerate colorectal adenoma recurrence. BMC Gastroenterol 2014 Oct 23;14:187 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25341954.
- ↑ Martínez ME, Thompson P, Messer K, Ashbeck EL, Lieberman DA, Baron JA, et al. One-year risk for advanced colorectal neoplasia: U.S. versus U.K. risk-stratification guidelines. Ann Intern Med 2012 Dec 18;157(12):856-64 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23247939.
- ↑ Hassan C, Quintero E, Dumonceau JM, Regula J, Brandão C, Chaussade S, et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2013 Oct;45(10):842-51 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24030244.
- ↑ Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012 Sep;143(3):844-857 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22763141.
- ↑ Leddin D, Enns R, Hilsden R, Fallone CA, Rabeneck L, Sadowski DC, et al. Colorectal cancer surveillance after index colonoscopy: guidance from the Canadian Association of Gastroenterology. Can J Gastroenterol 2013 Apr;27(4):224-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23616961.
- ↑ Hoff G, Sauar J, Hofstad B, Vatn MH. The Norwegian guidelines for surveillance after polypectomy: 10-year intervals. Scand J Gastroenterol 1996 Sep;31(9):834-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/8888428.
- ↑ Lew JB, St John DJB, Xu XM, Greuter MJE, Caruana M, Cenin DR, et al. Long-term evaluation of benefits, harms, and cost-effectiveness of the National Bowel Cancer Screening Program in Australia: a modelling study. Lancet Public Health 2017 Jul;2(7):e331-e340 Available from: http://www.ncbi.nlm.nih.gov/pubmed/29253458.
- ↑ Brenner H, Chang-Claude J, Rickert A, Seiler CM, Hoffmeister M. Risk of colorectal cancer after detection and removal of adenomas at colonoscopy: population-based case-control study. J Clin Oncol 2012 Aug 20;30(24):2969-76 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22826281.
|PICO question SAD 1||Evidence statement form SAD2||Systematic review report SAD2|