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PRACTICE
Colorectal cancer is the fourth most common cause of cancer possibly due to an increased use of diagnostic endoscopy and
related mortality globally, with 1.4 million new cases and 700 polypectomy.24 25
000 deaths annually.1
What is colorectal cancer? What are the risk factors for colorectal
Colorectal cancer refers to tumours of the rectum or large bowel cancer?
(including the appendix) that arise from the colorectal mucosa Most colorectal cancer cannot be attributed to any single risk
(fig 1⇓). Adenocarcinoma is the most common form of factor, although increasing age and male sex have consistently
colorectal cancer (>95%). Rarer subtypes include carcinoid shown strong associations with disease incidence in
tumour, sarcoma, and lymphoma; these present differently from epidemiological studies.23 The evidence for the other major risk
adenocarcinoma1 and will not be discussed in this review. factors for colorectal cancer is summarised in box 1.
The key genetic syndromes associated with colorectal cancer
How does colorectal adenocarcinoma are summarised in table 1⇓; and the current UK
develop? recommendations for screening and surveillance of
asymptomatic patients in moderate-risk family groups are
Colorectal cancer typically develops from adenomatous polyps summarised in table 2⇓.26
that undergo dysplastic changes to become cancerous (fig 2⇓).2
Tumours can occur sporadically, but there are some inherited
colorectal cancer syndromes (see table 1⇓). Several risk factors
How do patients present, and who should
are also recognised (see box 1). be referred?
The commonest presenting features of colorectal cancer are
Who gets colorectal cancer? abdominal pain, change in bowel habit, rectal bleeding, and
The incidence of colorectal cancer strongly increases after 50 microcytic anaemia, although these commonly feature in other
years of age (fig 3⇓), and median age at diagnosis is about 70 gastrointestinal diseases. Left sided colorectal tumours typically
years in developed regions.23 In 2012, age standardised incidence present with altered bowel habit (such as loose stools, increased
rates were highest across Oceania (41.0 and 29.2 per 100 000 frequency, and intestinal obstruction secondary to progressive
in men and women respectively), North America, and Europe, luminal narrowing), rectal bleeding or mucus, or tenesmus.
and lowest across western Africa (4.5 and 3.8 per 100 000) and Right sided lesions may present more insidiously with weight
south-central Asia (fig 4⇓).8 Previously low risk regions (such loss, abdominal pain or mass, or iron deficiency anaemia.27
as Spain and several countries in Eastern Europe and East Asia) Urgently investigate and refer men and non-menstruating women
have seen rapid rises in incidence of colorectal cancer. This has with iron deficiency anaemia, as 10% of such patients will have
been attributed to the adoption of high fat diets heavy in red colorectal cancer.28 29
and processed meats, physical inactivity, excessive alcohol A UK population based case-control study of 2093 patients
consumption, and smoking. The US and other high income aimed to quantify the pre-diagnostic features of colorectal cancer
countries have seen a plateau or drop in disease incidence, (see table 3⇓ for details).30 The 2015 NICE guidelines for the
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BMJ 2016;353:i3590 doi: 10.1136/bmj.i3590 (Published 14 July 2016) Page 2 of 12
PRACTICE
Lifestyle factors
• Red meat and processed meat consumption
– A meta-analysis of 24 prospective studies found the relative risk of colorectal cancer for the highest versus the lowest intake of red or processed
meat in the pooled cohort was 1.22 (95% CI 1.11 to 1.34)9
– Relative risk for every 100 g/day increase in intake was 1.14 (1.04 to 1.24)
– Cancer risk increased linearly with increasing meat intake up to 140 g/day
• Obesity
– 13% of bowel cancers in the UK have been linked to obesity10
– A meta-analysis of 43 studies including nearly 9 000 000 individuals worldwide found a relative risk of 1.33 (1.25 to 1.42) in obese individuals (body
mass index >30) compared with those with normal BMI11
– Association with BMI is stronger in men than women,12 and in women it may vary with menopausal status and use of hormone replacement therapy13
• Alcohol
– 11% of bowel cancers in the UK have been linked to excessive alcohol consumption10
– A meta-analysis of 61 cohort and case-control studies found that, compared with infrequent or non-drinkers, those who consumed 1.6-6.2 British
alcohol units daily had a 21% higher risk (95% CI 1.13 to 1.28) of bowel cancer, and those who drank over 6.2 units daily had a 52% higher risk
(95% CI 1.27 to 1.81)14
– Overall, bowel cancer risk increased by 7% per unit of alcohol consumed daily
• Tobacco smoking
– 8% of bowel cancers in the UK have been linked to tobacco smoking10
– A meta-analysis of 28 prospective studies and 1 463 796 subjects suggests current cigarette smokers have a 20% higher risk of disease (95% CI
1.10 to 1.30) than people who have never smoked15
– A meta-analysis of 106 observational studies suggests that former smokers have a 18% higher risk of bowel cancer (95% CI 1.11 to 1.25) than never
smokers; and that bowel cancer risk rises by 7-11% per 10 cigarettes smoked daily16
Medical factors
Family history
• 20% of bowel cancers are associated with hereditary factors other than familial adenomatous polyposis (FAP) and hereditary non-polyposis colorectal
cancer (HNPCC)6
• A meta-analysis of 59 studies suggested that bowel cancer risk was 80% higher in people with an affected first degree relative.17 A population lifetime
risk of 1.8% for a 50 year old increased to 3.4% (95% CI 2.8 to 4.0%) with at least one affected relative or 6.9% (4.5 to 10.4%) with two or more relatives
• A meta-analysis of 27 studies suggested a relative risk of 3.87 (2.40 to 6.22) for patients with an affected relative who was diagnosed before the age
of 45 years18
Colorectal adenomas or polyps
• A pooled analysis of 8 prospective studies comprising 9167 patients revealed that 1% of patients with colorectal adenomas >20 mm diameter or with
high grade dysplasia develop cancer within 4 years of adenoma removal19
• A meta-analysis of 7 studies comprising 11 387 patients revealed that patients with low risk polyps detected at first colonoscopy had a 80% higher risk
of advanced cancer than those with no polyps detected20
Inflammatory bowel disease (IBD)
• A meta-analysis of population based cohort studies found that patients with IBD (ulcerative colitis or Crohn's colitis) have a 70% higher risk (95% CI
1.2 to 2.2) of developing colorectal cancer than the general population21
• This risk increases with the duration and extent of disease: those with IBD for >20 years have a 5% risk of developing bowel cancer21
Diabetes
• A meta-analysis of 15 studies including 2 593 935 patients found that diabetes was associated with a 30% higher risk of colorectal cancer (relative
risk 1.30 (1.20 to 1.40))22
• Diabetic patients also suffered greater mortality from bowel cancer (relative risk 1.26 (1.05 to 1.50)), but there was evidence for heterogeneity between
studies (P=0.04)
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PRACTICE
How to investigate suspected colorectal As with colonoscopy, patients must be given comprehensive
information about stopping certain medications and adopting a
cancer low residue diet in the days before the test. Special instructions
Advise patients that more than one investigation may be are provided for diabetic patients. Depending on hospital policy,
necessary to confirm or exclude a diagnosis of colorectal patients will be requested to take oral Gastrografin (with or
cancer.32 without an accompanying bowel cleansing agent) at set times
Colonoscopy is the recommended first line imaging for for one or two days before the procedure. The procedure lasts
suspected colon cancer in patients without major comorbidity.32 about 30 minutes, during which a muscle relaxant (such as
Bowel preparation with oral laxatives improves the diagnostic buscopan) may be administered with intravenous contrast, while
yield of pan-colonic imaging. Biopsies are taken from any the colon is gently insufflated with carbon dioxide gas via the
suspicious lesions unless contraindicated (for example, in rectum, and scans obtained in various patient positions.
coagulopathy) to confirm the diagnosis and degree of tumour
differentiation (well, moderately, or poorly differentiated) to Double contrast barium enema
guide treatment. Patients who have undergone incomplete Double contrast barium enema is well tolerated and safe with
colonoscopy (due to intra-procedural discomfort or poor bowel excellent completion rates, but its relative impracticality and
preparation) may be offered repeat colonoscopy, computed lower diagnostic yields compared with the above investigations
tomographic (CT) colonography, or barium enema. Patients have resulted in its declining use across most UK centres.
with major comorbidity and frail or elderly patients with poor
mobility and poor tolerance to bowel preparation may be offered Other tests
alternative imaging such as CT colonography or flexible
Testing for faecal occult blood (FOB) and serum tumour markers
sigmoidoscopy in the first instance, followed by biopsy of
(such as carcinoembryonic antigen) are not useful in the
suspicious lesions.32
investigation of suspected colorectal cancer. While FOB testing
is effective for population screening in asymptomatic cohorts,
Colonoscopy it is too insensitive to guide the investigation of patients with
Colonoscopy is operator dependent and requires full bowel colorectal symptoms. Similarly, tumour markers lack sensitivity
preparation. Completion rates (that is, passage of colonoscope and specificity but are useful in the follow-up of treated patients.
to caecum) vary widely because of technical challenges, and A negative FOB test or normal serum tumour markers should
experienced endoscopists typically achieve completion rates of not delay the referral of symptomatic patients.
98%. A 90% rate is considered acceptable.33 Histological
confirmation of malignancy requires multiple biopsies. Overtly What can be done to prevent colorectal
malignant lesions may be injected with dye contrast to mark
the area and facilitate subsequent surgical resection. Procedural cancer?
risks are mainly related to sedation and bowel perforation (table Primary prevention
5⇓).34 35 Prospective comparative studies have suggested that
patients are as comfortable with conventional colonoscopy as Diet
CT colonography. Both of these investigations are preferred A meta-analysis of 25 prospective studies revealed a 10% risk
over barium enema.36 37 Poor bowel preparation and incomplete reduction in developing colorectal cancer for an extra 10 g of
colonoscopy are the two main variables contributing to false total dietary fibre ingested daily. In particular, cereal fibre and
negative tumour detection.33 whole grains were associated with a reduction in colorectal
Box 2 lists advice for people referred for colonoscopy. If there cancer risk.39
is a clear contraindication or more than one relative A meta-analysis of 19 cohort studies suggested that, for every
contraindication to bowel preparation, offer admission on the 400 g of dairy products consumed daily, the risk of developing
day before colonoscopy for inpatient preparation. colorectal cancer was significantly reduced (relative risk 0.83
(95% CI 0.78 to 0.88). Similarly, the daily consumption of 200
CT colonography g of milk or 50 g of cheese was associated with a lower risk of
developing colorectal cancer.40
CT colonography (“virtual colonoscopy”) may be indicated
after failed colonoscopy, in light of patient preference, or when Another meta-analysis of 15 studies including 12 305 patients
a patient is deemed unsuitable for colonoscopy. Unlike revealed that every 300 mg of daily calcium intake (up to 1900
conventional colonoscopy, CT colonography allows intraluminal mg/day) reduced the risk of developing colorectal cancer.41
visualisation of the colourectum without the need for sedation,
while it offers a similar sensitivity for cancer detection but a Physical activity
lower specificity for polyp and tumour detection (table 5⇓).38 It is estimated that 5% of colon cancers (but not rectal cancers)
CT colonography may detect extraluminal pathology in patients in the UK are linked to inadequate physical activity.42 43
referred for weight loss or abdominal pain. Intravenous contrast Meta-analyses of cohort studies have revealed a 17-24% risk
and oral faecal tagging agents (such as Gastrografin, which also reduction in colon cancer from the most to the least physically
has a laxative effect) are used to differentiate stools and mass active people.43-45
lesions (polyps and cancers). CT colonography is not suitable
for pregnant patients. It is contraindicated in patients with iodine Pharmacological
allergies and may not be possible for those with impaired
swallowing or high aspiration risk. Tissue biopsy and polyp Two large trials in the 1980s, designed to evaluate the prevention
removal are not possible with CT colonography, so any lesions of vascular events by aspirin, revealed a 37% risk reduction of
detected will require endoscopic evaluation to confirm a colorectal cancer in patients with a daily intake of 300 mg
histological diagnosis. aspirin for at least five years.46 Various observational studies
support the use of long term aspirin in the chemoprevention of
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PRACTICE
colorectal cancer,47 and data from a large randomised controlled family history of colorectal cancer (a single first degree relative
trial revealed that taking 600 mg aspirin daily for two years led with colorectal cancer or advanced adenoma diagnosed at <60
to a risk reduction (hazard ratio 0.41) in colorectal cancer years old, or two first degree relatives with colorectal cancer or
incidence among patients with HNPCC.48 Non-steroidal advanced adenomas)26 56; inflammatory bowel disease (ulcerative
anti-inflammatory drugs (NSAIDs) have also been shown to or Crohn's colitis)56; and acromegaly.58 59
reduce colorectal cancer risk in various cohort studies and
case-control studies,49 and randomised controlled trials have Contributors: SGT, SSDT, and CEG conceived the review, extracted
shown that COX-2 inhibitors reduce adenoma incidence (relative evidence, and drafted the manuscript. All authors helped write the article
risk 0.72 (0.68 to 0.77)), potentially reducing subsequent cancer (including article direction, interpreting the literature, and editing the
risk.49 A large, randomised, double-blind trial revealed that daily manuscript). AH is guarantor and has approved the final article.
supplementation with 1200 mg calcium reduced colorectal Competing interests: We have read and understood the BMJ Group
adenoma recurrence (adjusted risk ratio 0.85 (0.74 to 0.98), policy on declaration of interests and have no relevant interests to
P=0.03).50 declare.
Despite insufficient evidence to recommend routine use of most Provenance and peer review: Not commissioned; externally peer
of the above agents for prevention of colorectal cancer, the US reviewed.
Preventive Services Task Force recently recommended use of
low dose aspirin for the primary prevention of cardiovascular 1 Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and
disease and colorectal cancer in adults aged 50-59 years who 2
Mortality Worldwide: IARC CancerBase No 11. 2013. http://globocan.iarc.fr.
Arnold CN, Goel A, Blum HE, Boland CR. Molecular pathogenesis of colorectal cancer:
have a ≥10% 10-year risk of cardiovascular disease, are not at implications for molecular diagnosis. Cancer 2005;104:2035-47. doi:10.1002/cncr.
increased risk for bleeding, have a life expectancy of ≥10 years, 21462 pmid:16206296.
3 Gala M, Chung DC. Hereditary colon cancer syndromes. Semin Oncol 2011;38:490-9.
and are willing to take low dose aspirin daily for ≥10 years.51 doi:10.1053/j.seminoncol.2011.05.003 pmid:21810508.
No similar recommendations exist in current British or European 4 Dunlop MG, Farrington SM, Carothers AD, et al. Cancer risk associated with germline
DNA mismatch repair gene mutations. Hum Mol Genet 1997;6:105-10. doi:10.1093/hmg/
guidelines. 6.1.105 pmid:9002677.
5 Galiatsatos P, Foulkes WD. Familial adenomatous polyposis. Am J Gastroenterol
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19 Martínez ME, Baron JA, Lieberman DA, et al. A pooled analysis of advanced colorectal 41 Keum N, Aune D, Greenwood DC, Ju W, Giovannucci EL. Calcium intake and colorectal
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20 Hassan C, Gimeno-García A, Kalager M, et al. Systematic review with meta-analysis: the 42 Parkin DM. 9. Cancers attributable to inadequate physical exercise in the UK in 2010. Br
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24593121. physical activity, and colorectal cancer by anatomical subsites: a systematic review and
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of population-based cohort studies. Inflamm Bowel Dis 2013;19:789-99. doi:10.1097/MIB. 44 Wolin KY, Yan Y, Colditz GA, Lee IM. Physical activity and colon cancer prevention: a
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22 Larsson SC, Orsini N, Wolk A. Diabetes mellitus and risk of colorectal cancer: a 45 Boyle T, Keegel T, Bull F, Heyworth J, Fritschi L. Physical activity and risks of proximal
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S0140-6736(13)61649-9 pmid:24225001. 46 Flossmann E, Rothwell PM. British Doctors Aspirin Trial and the UK-TIA Aspirin Trial.
24 Stock C, Pulte D, Haug U, Brenner H. Subsite-specific colorectal cancer risk in the Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from
colorectal endoscopy era. Gastrointest Endosc 2012;75:621-30. doi:10.1016/j.gie.2011. randomised and observational studies. Lancet 2007;369:1603-13. doi:10.1016/S0140-
10.025 pmid:22341107. 6736(07)60747-8 pmid:17499602.
25 Center MM, Jemal A, Smith RA, Ward E. Worldwide variations in colorectal cancer. CA 47 Chan AT, Arber N, Burn J, et al. Aspirin in the chemoprevention of colorectal neoplasia:
Cancer J Clin 2009;59:366-78. doi:10.3322/caac.20038 pmid:19897840. an overview. Cancer Prev Res (Phila) 2012;5:164-78. doi:10.1158/1940-6207.CAPR-11-
26 Cairns SR, Scholefield JH, Steele RJ, et al. British Society of Gastroenterology Association 0391 pmid:22084361.
of Coloproctology for Great Britain and Ireland. Guidelines for colorectal cancer screening 48 Burn J, Gerdes AM, Macrae F, et al. CAPP2 Investigators. Long-term effect of aspirin on
and surveillance in moderate and high risk groups (update from 2002). Gut 2010;59:666-89. cancer risk in carriers of hereditary colorectal cancer: an analysis from the CAPP2
doi:10.1136/gut.2009.179804 pmid:20427401. randomised controlled trial. Lancet 2011;378:2081-7. doi:10.1016/S0140-6736(11)61049-
27 Kanellos D, Kitsios G, Kanellos I, et al. Anaemia as a symptom of right colon cancer. 0 pmid:22036019.
Tech Coloproctol 2004;8(Suppl 1):s62-4. doi:10.1007/s10151-004-0114-0 pmid:15655646. 49 Rostom A, Dubé C, Lewin G, et al. US Preventive Services Task Force. Nonsteroidal
28 Rockey DC, Cello JP. Evaluation of the gastrointestinal tract in patients with iron-deficiency anti-inflammatory drugs and cyclooxygenase-2 inhibitors for primary prevention of colorectal
anemia. N Engl J Med 1993;329:1691-5. doi:10.1056/NEJM199312023292303 pmid: cancer: a systematic review prepared for the US Preventive Services Task Force. Ann
8179652. Intern Med 2007;146:376-89. doi:10.7326/0003-4819-146-5-200703060-00010 pmid:
29 Goddard AF, James MW, McIntyre AS, Scott BB. British Society of Gastroenterology. 17339623.
Guidelines for the management of iron deficiency anaemia. Gut 2011;60:1309-16. doi: 50 Baron JA, Beach M, Mandel JS, et al. Calcium Polyp Prevention Study Group. Calcium
10.1136/gut.2010.228874 pmid:21561874. supplements for the prevention of colorectal adenomas. N Engl J Med 1999;340:101-7.
30 Hamilton W, Round A, Sharp D, Peters TJ. Clinical features of colorectal cancer before doi:10.1056/NEJM199901143400204 pmid:9887161.
diagnosis: a population-based case-control study. Br J Cancer 2005;93:399-405. doi:10. 51 Bibbins-Domingo K. U.S. Preventive Services Task Force. Aspirin use for the primary
1038/sj.bjc.6602714 pmid:16106247. prevention of cardiovascular disease and colorectal cancer: US Preventive Services Task
31 National Institute for Health and Care Excellence. Suspected cancer: recognition and Force Recommendation Statement. Ann Intern Med 2016;164:836-45. doi:10.7326/M16-
referral (NICE guideline NG12). 2015. www.nice.org.uk/guidance/ng12. 0577 pmid:27064677.
32 Poston GJ, Tait D, O’Connell S, Bennett A, Berendse S. Guideline Development Group. 52 Malila N, Oivanen T, Malminiemi O, Hakama M. Test, episode, and programme sensitivities
Diagnosis and management of colorectal cancer: summary of NICE guidance. BMJ of screening for colorectal cancer as a public health policy in Finland: experimental design.
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33 Bressler B, Paszat LF, Chen Z, Rothwell DM, Vinden C, Rabeneck L. Rates of new or 53 Hewitson P, Glasziou P, Watson E, Towler B, Irwig L. Cochrane systematic review of
missed colorectal cancers after colonoscopy and their risk factors: a population-based colorectal cancer screening using the fecal occult blood test (hemoccult): an update. Am
analysis. Gastroenterology 2007;132:96-102. doi:10.1053/j.gastro.2006.10.027 pmid: J Gastroenterol 2008;103:1541-9. doi:10.1111/j.1572-0241.2008.01875.x pmid:18479499.
17241863. 54 Hol L, van Leerdam ME, van Ballegooijen M, et al. Screening for colorectal cancer:
34 Lieberman DA, Weiss DG, Bond JH, Ahnen DJ, Garewal H, Chejfec G. Use of colonoscopy randomised trial comparing guaiac-based and immunochemical faecal occult blood testing
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37 Bosworth HB, Rockey DC, Paulson EK, et al. Prospective comparison of patient experience 57 Giardiello FM, Brensinger JD, Petersen GM. AGA technical review on hereditary colorectal
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38 Atkin W, Dadswell E, Wooldrage K, et al. SIGGAR investigators. Computed tomographic 58 Renehan AG, Odwyer ST, Shalet SM. Screening colonoscopy for acromegaly in
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39 Aune D, Chan DS, Lau R, et al. Dietary fibre, whole grains, and risk of colorectal cancer: Coloproctology for Great Britain and Ireland. Screening guidelines for colorectal cancer
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40 Aune D, Lau R, Chan DS, et al. Dairy products and colorectal cancer risk: a systematic
Published by the BMJ Publishing Group Limited. For permission to use (where not already
review and meta-analysis of cohort studies. Ann Oncol 2012;23:37-45. doi:10.1093/annonc/
mdr269 pmid:21617020. granted under a licence) please go to http://group.bmj.com/group/rights-licensing/
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Tables
6
It is estimated that another 20% of bowel cancer is linked to hereditary factors not associated with FAP and HNPCC.
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Table 2| Summary of recommendations for colorectal cancer (CRC) screening and surveillance in moderate risk family groups (adapted
from Cairns et al26)
Screening recommended
Lifetime risk of colorectal
Family history of colorectal cancer cancer death without Age at initial screen
(CRC) surveillance Procedure (years) Screening interval
In 3 relatives in first degree kinship*, none ~1 in 6-10 Colonoscopy 50 Every 5 years to age 75 years
<50 years old
In 2 relatives in first degree kinship*, ~1 in 6-10 Colonoscopy 50 Every 5 years to age 75 years
mean age <60 years
In 2 first degree relatives ≥60 years old ~1 in 12 Colonoscopy 55 No follow-up if initial screen normal
In 1 first degree relative <50 years old ~1 in 12 Colonoscopy 55 No follow-up if initial screen normal
Other family history of CRC <1 in 12 None NA NA
*Relatives who are first degree relatives of each other and at least one is a first degree relative of the consultand. No affected relative <50 years old (otherwise
26
high risk criteria apply).
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Table 4| Urgent referral criteria for suspected colorectal cancer for an appointment within two weeks (from National Institute for Health
and Care Excellence31)
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*Highly operator dependent. Many endoscopists have lower rates than quoted in published series.
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Figures
Fig 1 Distribution of bowel cancer by anatomical site, UK (2007-09) (adapted from Cancer Research UK, bowel cancer
incidence statistics,
www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/bowel-cancer/incidence)
Fig 2 Progression from colorectal polyp to cancer (adapted from Johns Hopkins Colon Cancer Center. Polyps 101.
www.hopkinscoloncancercenter.org/CMS/CMS_Page.aspx?CurrentUDV=59&CMS_Page_ID=744568E4-291E-4276-97C4-FA7A4EE02235)
Fig 3 Age specific incidence rates of colorectal cancer per 100 000 population, UK (2009-11) (adapted from Cancer Research
UK, bowel cancer incidence statistics,
www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/bowel-cancer/incidence)
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BMJ 2016;353:i3590 doi: 10.1136/bmj.i3590 (Published 14 July 2016) Page 12 of 12
PRACTICE
Fig 4 Estimated worldwide age standardised (per 100 000) incidence of colorectal cancer in men in 2012 (adapted from
GLOBOCAN 20121)
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