1.2 Screening age range and intervals
1.3 Benefits and risks of bowel cancer screening
1.3.2 Potential adverse effects
1.4 Other potential screening tools
1.4.3 Plasma and faecal DNA testing
3. Screening people at increased risk
Finding bowel cancer or precancerous conditions early is a key to reducing bowel cancer mortality and morbidity. Bowel cancer is one of only three cancers for which population-based screening is recommended; the others are breast cancer and cervical cancer. (For generic information about cancer screening, see the Principles of screening chapter.)
Approximately 15-20% of bowel cancers arise from the serrated pathway, however, most bowel cancers develop from adenomatous polyps (adenomas); a small adenoma may grow into advanced cancer over an estimated 20-25 years on average. While common in middle aged and older people, 40% of advanced adenomas progress to cancer.
Adenomas are described as 'advanced' if they have certain features such as larger size (10 mm or more in diameter), contains villous growth pattern, or high-grade dysplasia. These features indicate a greater likelihood of progression to localised cancer and the risk of developing cancer elsewhere in the large bowel. Once cancer has developed, growth may occur gradually over 12 to 24 months or even longer. Most people with advanced adenomas and many with early-stage bowel cancer experience no obvious symptoms.
Bowel cancer survival is highly dependent on the pathological stage of tumour development at the time of diagnosis, as well as the treatments that follow. Earlier diagnosis is strongly associated with better prognosis. Patients with bowel cancer detected via participation in NBCSP were diagnosed at an earlier stage than patients with symptomatic cancers. In a global report, the 5-year survival data for Australian adults diagnosed with colon or rectum was 70.7% and 71%, respectively.
Australian five-year survival rates for bowel cancer, based on South Australian and Western Australian data, are:
- 88–92% for stage A/I, when the cancer is contained within the bowel wall;
- 70–83% for stage B/II, when the cancer has extended through the bowel wall, but with no lymph nodes affected;
- 43–53% for stage C/III, when the cancer is present in the lymph nodes;
- 7–19% for stage D/IV, when the cancer cannot be removed by surgery or has spread to other areas of the body.
There is evidence of an upward trend in survival figures over time in Australia, due to a number of factors including improvements in surgical technique and more widespread use of adjuvant chemotherapy and radiotherapy.
Bowel cancer screening
The two objectives of bowel cancer screening are:
- to prevent cancer by identifying and removing precancerous, advanced adenomas; and
- to diagnose and treat early-stage, curable cancers.
Population-based bowel cancer screening with the immunochemical faecal occult blood test (iFOBT) in Australia is managed through the National Bowel Cancer Screening Program (NBCSP). iFOBT is the recommended screening tool due to its high sensitivity and specificity, acceptability among the public and cost-effectiveness. For information on NBCSP, see the Policy context section.
Faecal occult blood test
Cancers in the large bowel tend to produce low-grade bleeding, so detecting blood in small (often invisible) concentrations in faeces is the basis for using FOBT to screen for bowel cancer. FOBT detects blood in faeces by identifying the chemical or immunochemical properties of haem and haemoglobin (substances found in blood).
There are two types of FOBT: the guaiac test (gFOBT) detects chemical activity in haem; the immunochemical test (iFOBT) uses globin antibodies to detect blood. The gFOBT relies on the user avoiding red meat and vitamin C supplements for several days before use; the iFOBT requires no change in diet or medication from the user.
In 2016, of those who had a follow-up colonoscopy after a positive screening result, 16% had some type of neoplastic lesion (3.8% had bowel cancer, 6% have an advanced adenoma, 6% have a precancerous growth called a non-advanced adenoma).
The sensitivity of iFOBT for advanced adenoma ranges from 16-64%. Furthermore, the sensitivity of iFOBT ranges from 53-100% and specificity is around 93% for detecting colorectal cancer.
Acceptability of iFOBT as a screening tool is high. A survey of WA residents in the target age group for the NBCSP found that, among those not yet invited to participate in screening, 83% stated they were ‘very/quite’ likely to participate if invited to do so and 94% were ‘very/quite’ likely to undergo the follow-up colonoscopy if their iFOBT result was positive.
The Clinical Practice Guidelines for the Prevention, Early Detection and Management of Colorectal Cancer, endorsed by the National Health and Medical Research Council (NHMRC), recommends organised population screening where iFOBT is performed every two years for the Australian population aged between 50 and 74 years. A cost-effectiveness analysis further supports the use of iFOBT in a population screening program as biennial iFOBT screening was found to be highly cost-effective in Australia. It was also the most cost-effective approach when compared with other screening technologies (including colonoscopy, computed tomographic colonography, DNA tests and flexible sigmoidoscopy) under all screening scenarios considered.
As early detection is the primary objective of screening, GPs are urged to recommend iFOBT as a screening tool for asymptomatic patients with no family history of bowel cancer. See role of GPs in screening for more information.
Screening age range and intervals
The clinical recommendations assessed different age range scenarios and found that the 50-74 age range was most cost-effective and had a balanced ratio of benefits to harms. Reducing the starting age to 45 years would present with a less favourable benefits-to-harms balance and require more colonoscopies for each extra cancer death prevented. Screening after 74 years was not cost-effective and not recommended. Therefore, bowel cancer screening is recommended for people aged 50-74 years.
Recommendations were made to keep screening frequency unchanged. Testing with iFOBT and other screening tools (including colonoscopy, computed tomographic colonography, DNA tests and flexible sigmoidoscopy) at various alternative intervals (including annual) were compared to biennial testing with iFOBT. The latter was found to be the most cost-effective approach for bowel cancer screening in Australia.
Benefits and risks of bowel cancer screening
Screening is effective at detecting bowel cancers early, when they are easier to treat. The AIHW found that NBCSP participants with screen-detected bowel cancer were more likely to be diagnosed at a less advanced stage than those who did not participate in 2006-2010 (44% vs 24%). Furthermore, NBCSP participants with screen-detected bowel cancer had a lower risk of bowel cancer mortality compared to those who were diagnosed outside of the program (9.6% vs 23.8%). Independent studies have shown similar outcomes which is consistent with highest-level international evidence showing that bowel cancer screening on a population basis significantly reduces mortality and morbidity. The most obvious benefit of screening for bowel cancer for people aged 50-74 years is the potential for reducing bowel cancer mortality by 36% with a current participation rate of 40% and 59% for participation rates of 70%. An independent analysis published in 2017 estimated that 2300-3200 bowel cancer deaths would be prevented each year from 2015-2040 through the NBCSP.
A number of studies have shown that bowel cancer screening using FOBT is cost-effective. See the Policy context section of this chapter for more information.
Potential adverse effects
The most significant potential adverse effect associated with screening asymptomatic people for bowel cancer is the risk of physical harm incurred through colonoscopy. Colonoscopy is performed as a day case procedure and usually requires sedation; it can produce severe complications such as perforation, haemorrhage or death and carries a remote risk of transmitting infections. In a review of six prospective studies of colonoscopy, about one in 1000 patients suffered perforation, three in 1000 suffered major haemorrhage, and between one and three in 10,000 died as a result of the procedure. In two more recent studies, the findings were similar, overall morbidity being 0.4%. A review of a large Australian hospital experience supported the conclusions of these other studies and reported a mortality rate of 0.004% in outpatients having the procedure.
Bowel cancer screening may also result in adverse psychological and physical effects due to false positive tests (i.e. a preliminary indication that cancer may be present, which is not confirmed through investigation). People who present with bowel lesions that are ultimately found to be benign may experience significant initial distress and anxiety. Studies have shown, however, that anxiety usually abates when individuals learn they do not have bowel cancer, with no evidence of long-term harm after screening.
Thus, timely follow-up is critical for people with a positive FOBT result. This is particularly important as a high number of people with positive FOBT results are not diagnosed with cancer. A recent NBCSP monitoring report has shown that only one in every 26 people who underwent a colonoscopy to follow up a positive iFOBT result are diagnosed with a confirmed or suspected cancer, and one in 9 found to have advanced adenomas.
The potential for these harms must be weighed against the significant benefits of population-based screening. On balance, this is the case for screening with iFOBT.
Other potential screening tools
Sigmoidoscopy involves tube examination of the rectum and the lower part of the colon (i.e. the section of large bowel closest to the anus). The sigmoidoscope may be rigid (best suited for examining the rectum) or flexible (reaching into the lower part, but unable to examine the upper part of the colon). Flexible sigmoidoscopy allows examination of the area where 55% to 60% of bowel cancers and advanced adenomas occur. When abnormalities are detected, a tissue sample (biopsy) can be collected for pathological examination.
Major randomised controlled trials using flexible sigmoidoscopy conducted in the US, UK, Italy and Norway were conducted following evidence from case-control studies showing a substantial reduction in bowel cancer mortality. Three of these trials showed that this tool was feasible, safe and well accepted. These studies showed a decrease in bowel cancer incidence of 18-26% and mortality of 22-30%. The population-based study conducted in Norway showed a similar reduction in incidence and mortality of bowel cancer.
While a meta-analysis of randomised controlled trials published in 2012 provided Level I evidence for efficacy of flexible sigmoidoscopy as a screening tool for bowel cancer, evidence based on population screening is limited.
A cost-effectiveness analysis showed that a once-off sigmoidoscopy at 60 years was the least effective strategy with the lowest reductions in colorectal cancer incidence and mortality compared to other strategies included in the evaluation.
High cost, low acceptability and concerns about impact on colonoscopy services are significant issues for the use of sigmoidoscopy on a population level in Australia.
A colonoscope is similar to a flexible sigmoidoscope, but is much longer and able to examine the entire length of the large bowel; studies have shown that colonoscopy has around 95% sensitivity for detection of cancer. Colonoscopy also allows biopsies to be taken from suspected abnormalities as well as enabling most adenomas and some polypoid cancers to be removed during examination.
Colonoscopy sensitivity for detection of adenomas varies according to their size within the large bowel. As with sigmoidoscopy, sensitivity for detection of lesions depends on the proficiency of the examiner, again highlighting the need for comprehensive training and the auditing of outcomes. In 2009, the Australian Department of Health and Ageing released detailed recommendations on key performance indicators for colonoscopy. The National Bowel Cancer Screening Program Quality Working Group recommends standards, objectives and performance indicators for colonoscopy use in Australia.
Colonoscopy is the recommended follow-up test for those with positive findings at iFOBT or screening sigmoidoscopy. It is also recommended as the primary tool for cancer surveillance in people with an increased risk of bowel cancer. When it is not possible to examine the total length of the bowel by colonoscopy, CT colonography should be performed.
There is no high-level evidence to support use of colonoscopy in population screening currently available. However, two randomised controlled trials are underway. Initial findings from the Spanish study reported people were more likely to participate in screening with FOBT than with colonoscopy. The number of bowel cancers detected were similar in the two groups, but more adenomas were identified in the colonoscopy group.
Screening with 10-yearly colonoscopy was not found to be cost-effective when compared with biennial iFOBT screening and other screening strategies considered in the study.
The acceptability of colonoscopy as a screening tool is limited by the procedure’s invasive nature and the need for vigorous bowel preparation and sedation.
Colonoscopy has been considered as a potential screening tool, rather than diagnostic tool, due to its high sensitivity for detecting bowel cancers and advanced adenomas. However, the overall appropriateness of colonoscopy as the primary tool in population screening remains unclear. Moreover, the feasibility of providing colonoscopy for the circa 8 million Australians recommended for screening is also doubtful, given the high cost of the procedure, potential adverse effects, workforce limitations and other logistical issues.
Plasma and faecal DNA testing
DNA biomarker testing, using plasma (blood) or faecal DNA samples, is an emerging technology for the detection of bowel cancer. A number of DNA modifications associated with bowel cancer and its precursors have been identified. These are both genetic (usually mutational changes to the genes) and epigenetic (changes to gene expression, usually by promoter methylation).
DNA biomarker tests for bowel cancer using plasma and faecal stool samples are available, however to date, the performance of such tests have not been evaluated for population screening.
Faecal DNA testing sensitivity is 41-57% for detecting advanced adenomas and 93-100% for bowel cancer (stage I to III). These studies have observed a specificity of 87-91%. In 2016, the U.S. Preventive Services Task Force noted the lower specificity of faecal DNA testing in comparison with iFOB testing may result in higher numbers of false-positive results, higher likelihood of follow-up colonoscopies and experiencing an associated adverse event per screening test.
In a preliminary evaluation of plasma DNA testing, sensitivity was 7% for advanced adenoma, 29% for stage I cancer and 68% for stage II cancer; specificity was 94%. Similar sensitivity and specificity rates at 51% and 92% were reported for colorectal cancer from another assessment. The poor sensitivity of plasma DNA testing for advanced adenoma and for stage I cancer makes the test inappropriate for population screening.
Five-yearly faecal DNA testing and 2-yearly plasma DNA testing have not been shown to be cost-effective when compared with biennial iFOBT testing and were also found to be less effective in preventing bowel cancer deaths. In comparison, the good sensitivity and specificity, cost-effectiveness and availability of iFOBT make it the most effective screening tool currently available.
Role of GPs in screening
GPs are urged to encourage Australians who receive an iFOBT kit mailed to their homes to participate in the NBCSP given the evidence for mortality benefit. All Australians aged 50 to 74 will be eligible for screening every two years by 2019. See the Policy context section of this chapter for more information on the NBCSP.
GPs have an important role at critical points in the screening process. These include:
- determining the appropriateness of screening for individual patients (e.g. excluding those with significant co-morbidities, or those who have recently undergone screening or colonoscopy outside the national program);
- assessing high-risk individuals and managing them according to NHMRC guidelines;
- receiving iFOBT results where the participant has nominated a GP;
- managing participants with a positive iFOBT result, such as organising colonoscopy through the usual care pathway; and
- notifying the central registry of outcomes.
GPs may also assess individuals with symptoms that could be related to cancer and for whom diagnostic investigations (rather than screening) are required. Symptoms include:
- bleeding from the back passage or any sign of blood in a bowel motion;
- an unexplained and persistent change in bowel actions;
- unexplained tiredness;
- iron deficiency anaemia (identified through a blood test) – which could be linked to unexplained tiredness (as above) and can be symptomatic of bowel cancer;
- lower abdominal pain; and
- a persistent feeling of fullness.
Recommendation from a GP has been shown to be the most significant factor in encouraging people to screen for bowel cancer with iFOBT. One survey showed more than 90% of respondents would be “likely” or “very likely” to have an iFOBT every two years if advised by a doctor. Pilot program invitees who did not participate reported a greater likelihood of doing so if it was recommended by a GP.
GP involvement is therefore critical to optimal participation in bowel cancer screening programs. While there is evidence that GPs support bowel cancer screening, they have articulated a need for further education on the issue..
Screening people at increased risk
The Australian Health Technology Advisory Committee’s report on bowel cancer screening recommended that a national approach to screening be complemented by policy for groups at increased risk of bowel cancer: e.g. individuals with a family history of bowel cancer, or a personal history of bowel adenoma, bowel cancer or inflammatory bowel disease.
GPs are well-placed to determine bowel cancer risk on the basis of family history and to instigate appropriate management according to the guidelines(see role of GPs in screening for more information).
The Clinical Practice Guidelines for the Prevention, Early Detection and Management of Colorectal Cancer defines three categories of people in relation to risk for bowel cancer based on their family history of the disease:
- the first category (near average risk; people with no relative diagnosed with bowel cancer and people with one first-degree and/or second-degree relative diagnosed with bowel cancer at age 55 or older) are advised to screen with biennial iFOBTs from age 50 to 74, which is the same screening as those at average risk and is the screening provided by the National Bowel Cancer Screening Program;
- the second category (moderately increased risk; people with one first-degree relative diagnosed with bowel cancer under age 55, or two first-degree relatives diagnosed with bowel cancer at any age, or a combination of the two) are advised to screen with biennial iFOBTs from age 40 to 49 and colonoscopy every five years from age 50 to 74; and
- the third category (potentially high risk; people with at least three first-degree or second-degree relatives diagnosed with bowel cancer where at least one was diagnosed under age 55, or at least three first-degree relatives diagnosed with bowel cancer at any age are advised to screen with biennial iFOBTs from age 35 to 44 and colonoscopy every five years from age 45 to 74. Patients with suspected Lynch syndrome should be managed as recommended in the High-risk familial syndromes chapter of Guidelines.
Detailed recommendations for surveillance by colonoscopy in those with past bowel cancer or adenoma are set out in the Practice Guidelines for Surveillance Colonoscopy.
- Gao Q, Tsoi KK, Hirai HW, Wong MC, Chan FK, Wu JC, et al. Serrated polyps and the risk of synchronous colorectal advanced neoplasia: a systematic review and meta-analysis. Am J Gastroenterol 2015 Apr;110(4):501-9; quiz 510 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25756237.
- Kuntz KM, Lansdorp-Vogelaar I, Rutter CM, Knudsen AB, van Ballegooijen M, Savarino JE, et al. A systematic comparison of microsimulation models of colorectal cancer: the role of assumptions about adenoma progression. Med Decis Making 2011 Jul;31(4):530-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21673186.
- Rutter CM, Knudsen AB, Marsh TL, Doria-Rose VP, Johnson E, Pabiniak C, et al. Validation of Models Used to Inform Colorectal Cancer Screening Guidelines: Accuracy and Implications. Med Decis Making 2016 Jul;36(5):604-14 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26746432.
- Bonnington SN, Rutter MD. Surveillance of colonic polyps: Are we getting it right? World J Gastroenterol 2016 Feb 14;22(6):1925-34 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26877600.
- Ananda SS, McLaughlin SJ, Chen F, Hayes IP, Hunter AA, Skinner IJ, et al. Initial impact of Australia's National Bowel Cancer Screening Program. Med J Aust 2009 Oct 5;191(7):378-81 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19807627.
- Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018 Mar 17;391(10125):1023-1075 Available from: http://www.ncbi.nlm.nih.gov/pubmed/29395269.
- South Australian Cancer Registry. Epidemiology of cancer in South Australia. Incidence, mortality and survival 1977 to 1996. Adelaide: Openbook Publishers; 1997.
- Morris M, Iacopetta B, Platell C. Comparing survival outcomes for patients with colorectal cancer treated in public and private hospitals. Med J Aust 2007 Mar 19;186(6):296-300 Available from: http://www.ncbi.nlm.nih.gov/pubmed/17371210.
- Cancer Council Australia Colorectal Cancer Working Party. Clinical practice guidelines for the prevention, early detection and management of colorectal cancer. [homepage on the internet] Sydney: Cancer Council Australia; 2017 Oct Available from: https://wiki.cancer.org.au/australia/Guidelines:Colorectal_cancer.
- Macrae FA, St John DJ. Relationship between patterns of bleeding and Hemoccult sensitivity in patients with colorectal cancers or adenomas. Gastroenterology 1982 May;82(5 Pt 1):891-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/7060910.
- St John DJ, Young GP, McHutchison JG, Deacon MC, Alexeyeff MA. Comparison of the specificity and sensitivity of Hemoccult and HemoQuant in screening for colorectal neoplasia. Ann Intern Med 1992 Sep 1;117(5):376-82 Available from: http://www.ncbi.nlm.nih.gov/pubmed/1503328.
- Young GP, Macrae FA & St John DJB. Clinical methods of early detection: basis, use and evaluation. In: Young GP, Rozen P & Levin B. Prevention and early detection of colorectal cancer. London: W.B. Saunders; 1996. p. 241-270.
- WHO (World Health Organization) and OMED (World Organization for Digestive Endoscopy), Young GP, St John DJ, Winawer SJ, Rozen P. Choice of fecal occult blood tests for colorectal cancer screening: recommendations based on performance characteristics in population studies: a WHO (World Health Organization) and OMED (World Organization for Digestive Endoscopy) report. Am J Gastroenterol 2002 Oct;97(10):2499-507 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12385430.
- Australian Institute of Health and Welfare. National Bowel Cancer Screening Program: monitoring report 2018. Canberra: AIHW; 2018 May. Report No.: Cat. no. CAN 112. Available from: https://www.aihw.gov.au/getmedia/df120b1a-1bda-49c1-8611-17a7256e61d0/aihw-can-12.pdf.aspx?inline=true.
- Chiu HM, Lee YC, Tu CH, Chen CC, Tseng PH, Liang JT, et al. Association between early stage colon neoplasms and false-negative results from the fecal immunochemical test. Clin Gastroenterol Hepatol 2013 Jul;11(7):832-8.e1-2 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23376002.
- Parra-Blanco A, Gimeno-García AZ, Quintero E, Nicolás D, Moreno SG, Jiménez A, et al. Diagnostic accuracy of immunochemical versus guaiac faecal occult blood tests for colorectal cancer screening. J Gastroenterol 2010 Jul;45(7):703-12 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20157748.
- de Wijkerslooth TR, Stoop EM, Bossuyt PM, Meijer GA, van Ballegooijen M, van Roon AH, et al. Immunochemical fecal occult blood testing is equally sensitive for proximal and distal advanced neoplasia. Am J Gastroenterol 2012 Oct;107(10):1570-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22850431.
- Khalid-de Bakker CA, Jonkers DM, Sanduleanu S, de Bruïne AP, Meijer GA, Janssen JB, et al. Test performance of immunologic fecal occult blood testing and sigmoidoscopy compared with primary colonoscopy screening for colorectal advanced adenomas. Cancer Prev Res (Phila) 2011 Oct;4(10):1563-71 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21750209.
- Terhaar sive Droste JS, Oort FA, van der Hulst RW, van Heukelem HA, Loffeld RJ, van Turenhout ST, et al. Higher fecal immunochemical test cutoff levels: lower positivity rates but still acceptable detection rates for early-stage colorectal cancers. Cancer Epidemiol Biomarkers Prev 2011 Feb;20(2):272-80 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21135261.
- Redwood DG, Asay ED, Blake ID, Sacco PE, Christensen CM, Sacco FD, et al. Stool DNA Testing for Screening Detection of Colorectal Neoplasia in Alaska Native People. Mayo Clin Proc 2016 Jan;91(1):61-70 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26520415.
- Park DI, Ryu S, Kim YH, Lee SH, Lee CK, Eun CS, et al. Comparison of guaiac-based and quantitative immunochemical fecal occult blood testing in a population at average risk undergoing colorectal cancer screening. Am J Gastroenterol 2010 Sep;105(9):2017-25 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20502450.
- Viana Freitas BR, Kibune Nagasako C, Pavan CR, Silva Lorena SL, Guerrazzi F, Saddy Rodrigues Coy C, et al. Immunochemical fecal occult blood test for detection of advanced colonic adenomas and colorectal cancer: comparison with colonoscopy results. Gastroenterol Res Pract 2013;2013:384561 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24319453.
- Imperiale TF, Ransohoff DF, Itzkowitz SH, Levin TR, Lavin P, Lidgard GP, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med 2014 Apr 3;370(14):1287-97 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24645800.
- Hundt S, Haug U, Brenner H. Comparative evaluation of immunochemical fecal occult blood tests for colorectal adenoma detection. Ann Intern Med 2009 Feb 3;150(3):162-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19189905.
- Graser A, Stieber P, Nagel D, Schäfer C, Horst D, Becker CR, et al. Comparison of CT colonography, colonoscopy, sigmoidoscopy and faecal occult blood tests for the detection of advanced adenoma in an average risk population. Gut 2009 Feb;58(2):241-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/18852257.
- Morikawa T, Kato J, Yamaji Y, Wada R, Mitsushima T, Shiratori Y. A comparison of the immunochemical fecal occult blood test and total colonoscopy in the asymptomatic population. Gastroenterology 2005 Aug;129(2):422-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16083699.
- Nakazako M., Yamano H., Matsushita H., et al. Immunologic Fecal Occult Blood test for Colorectal cancer Screening. Japan Med Assoc J 2006 Jun;49:203-7 Available from: http://www.med.or.jp/english/pdf/2006_05+/203_207.pdf.
- Chen Y-Y, Chen T-H, Su M-Y, Ning H-C, Kuo C-J, Lin W-P, et al.. Accuracy of immunochemical fecal occult blood test for detecting colorectal neoplasms in individuals undergoing health check-ups. Advances in Digestive Medicine 2014 Sep;Volume 1, Issue 3, Pages 74–79 Available from: http://www.aidm-online.com/article/S2351-9797(14)00045-0/abstract.
- Castro I, Cubiella J, Rivera C, González-Mao C, Vega P, Soto S, et al. Fecal immunochemical test accuracy in familial risk colorectal cancer screening. Int J Cancer 2014 Jan 15;134(2):367-75 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23818169.
- Lee YC, Chiu HM, Chiang TH, Yen AM, Chiu SY, Chen SL, et al. Accuracy of faecal occult blood test and Helicobacter pylori stool antigen test for detection of upper gastrointestinal lesions. BMJ Open 2013 Oct 30;3(10):e003989 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24176798.
- Hernandez V, Cubiella J, Gonzalez-Mao MC, Iglesias F, Rivera C, Iglesias MB, et al. Fecal immunochemical test accuracy in average-risk colorectal cancer screening. World J Gastroenterol 2014 Jan 28;20(4):1038-47 Available from: http://www.ncbi.nlm.nih.gov/pubmed/24574776.
- Omata F, Shintani A, Isozaki M, Masuda K, Fujita Y, Fukui T. Diagnostic performance of quantitative fecal immunochemical test and multivariate prediction model for colorectal neoplasms in asymptomatic individuals. Eur J Gastroenterol Hepatol 2011 Nov;23(11):1036-41 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21897207.
- Brenner H, Tao S. Superior diagnostic performance of faecal immunochemical tests for haemoglobin in a head-to-head comparison with guaiac based faecal occult blood test among 2235 participants of screening colonoscopy. Eur J Cancer 2013 Sep;49(14):3049-54 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23706981.
- Elsafi SH, Alqahtani NI, Zakary NY, Al Zahrani EM. The sensitivity, specificity, predictive values, and likelihood ratios of fecal occult blood test for the detection of colorectal cancer in hospital settings. Clin Exp Gastroenterol 2015;8:279-84 Available from: http://www.ncbi.nlm.nih.gov/pubmed/26392783.
- Ng SC, Ching JY, Chan V, Wong MC, Suen BY, Hirai HW, et al. Diagnostic accuracy of faecal immunochemical test for screening individuals with a family history of colorectal cancer. Aliment Pharmacol Ther 2013 Oct;38(7):835-41 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23957462.
- Kato J, Morikawa T, Kuriyama M, Yamaji Y, Wada R, Mitsushima T, et al. Combination of sigmoidoscopy and a fecal immunochemical test to detect proximal colon neoplasia. Clin Gastroenterol Hepatol 2009 Dec;7(12):1341-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/19426835.
- Lee YH, Hur M, Kim H, Jeon KN, Yun CH, Lee CH, et al. Optimal cut-off concentration for a faecal immunochemical test for haemoglobin by Hemo Techt NS-Plus C15 system for the colorectal cancer screening. Clin Chem Lab Med 2015 Feb;53(3):e69-71 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25153599.
- Jalleh G, Donovan RJ, Lin C, Slevin T, Clayforth C, Pratt IS, et al. Beliefs about bowel cancer among the target group for the National Bowel Cancer Screening Program in Australia. Aust N Z J Public Health 2010 Apr;34(2):187-92 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23331364.
- 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.
- Lew JB, St John DJB, Macrae FA, Emery JD, Ee HC, Jenkins MA, et al. Evaluation of the benefits, harms and cost-effectiveness of potential alternatives to iFOBT testing for colorectal cancer screening in Australia. Int J Cancer 2018 Jul 15;143(2):269-282 Available from: http://www.ncbi.nlm.nih.gov/pubmed/29441568.
- Lew JB, St John DJB, Macrae FA, Emery JD, Ee HC, Jenkins MA, et al. Benefits, harms and cost-effectiveness of potential age-extensions to the National Bowel Cancer Screening Program in Australia. Cancer Epidemiol Biomarkers Prev 2018 Sep 6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/30190276.
- Australian Institute of Health and Welfare. Analysis of bowel cancer outcomes for the National Bowel Cancer Screening Program 2018. Canberra: AIHW; 2018 May. Report No.: Cat. no. CAN 113. Available from: https://www.aihw.gov.au/getmedia/7878d65f-d1dc-4be0-9b1c-4f897873f56c/aihw-can-113.pdf.aspx?inline=true.
- Cole SR, Tucker GR, Osborne JM, Byrne SE, Bampton PA, Fraser RJ, et al. Shift to earlier stage at diagnosis as a consequence of the National Bowel Cancer Screening Program. Med J Aust 2013 Apr 1;198(6):327-30 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23545032.
- Australian Health Technology Advisory Committee. Colorectal cancer screening. Canberra: Commonwealth Department of Health and Family Services; 1997.
- Winawer SJ, Fletcher RH, Miller L, Godlee F, Stolar MH, Mulrow CD, et al. Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology 1997 Feb;112(2):594-642 Available from: http://www.ncbi.nlm.nih.gov/pubmed/9024315.
- Dafnis G, Ekbom A, Pahlman L, Blomqvist P. Complications of diagnostic and therapeutic colonoscopy within a defined population in Sweden. Gastrointest Endosc 2001 Sep;54(3):302-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11522969.
- Gatto NM, Frucht H, Sundararajan V, Jacobson JS, Grann VR, Neugut AI. Risk of perforation after colonoscopy and sigmoidoscopy: a population-based study. J Natl Cancer Inst 2003 Feb 5;95(3):230-6 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12569145.
- Viiala CH, Zimmerman M, Cullen DJ, Hoffman NE. Complication rates of colonoscopy in an Australian teaching hospital environment. Intern Med J 2003 Aug;33(8):355-9 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12895166.
- Lindholm E, Berglund B, Kewenter J, Haglind E. Worry associated with screening for colorectal carcinomas. Scand J Gastroenterol 1997 Mar;32(3):238-45 Available from: http://www.ncbi.nlm.nih.gov/pubmed/9085461.
- Wardle J, Taylor T, Sutton S, Atkin W. Does publicity about cancer screening raise fear of cancer? Randomised trial of the psychological effect of information about cancer screening. BMJ 1999 Oct 16;319(7216):1037-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/10521195.
- Parker MA, Robinson MH, Scholefield JH, Hardcastle JD. Psychiatric morbidity and screening for colorectal cancer. J Med Screen 2002;9(1):7-10 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11943790.
- Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial Project Team, Gohagan JK, Prorok PC, Hayes RB, Kramer BS. The Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial of the National Cancer Institute: history, organization, and status. Control Clin Trials 2000 Dec;21(6 Suppl):251S-272S Available from: http://www.ncbi.nlm.nih.gov/pubmed/11189683.
- UK Flexible Sigmoidoscopy Screening Trial Investigators, Atkin WS, Cook CF, Cuzick J, Edwards R, Northover JM, et al. Single flexible sigmoidoscopy screening to prevent colorectal cancer: baseline findings of a UK multicentre randomised trial. Lancet 2002 Apr 13;359(9314):1291-300 Available from: http://www.ncbi.nlm.nih.gov/pubmed/11965274.
- SCORE Working Group--Italy, Segnan N, Senore C, Andreoni B, Aste H, Bonelli L, et al. Baseline findings of the Italian multicenter randomized controlled trial of 'once-only sigmoidoscopy'--SCORE. J Natl Cancer Inst 2002 Dec 4;94(23):1763-72 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12464648.
- Holme Ø, Løberg M, Kalager M, Bretthauer M, Hernán MA, Aas E, et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: a randomized clinical trial. JAMA 2014 Aug 13;312(6):606-15 Available from: http://www.ncbi.nlm.nih.gov/pubmed/25117129.
- Selby JV, Friedman GD, Quesenberry CP Jr, Weiss NS. A case-control study of screening sigmoidoscopy and mortality from colorectal cancer. N Engl J Med 1992 Mar 5;326(10):653-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/1736103.
- Newcomb PA, Norfleet RG, Storer BE, Surawicz TS, Marcus PM. Screening sigmoidoscopy and colorectal cancer mortality. J Natl Cancer Inst 1992 Oct 21;84(20):1572-5 Available from: http://www.ncbi.nlm.nih.gov/pubmed/1404450.
- PLCO Project Team, Weissfeld JL, Schoen RE, Pinsky PF, Bresalier RS, Church T, et al. Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial. J Natl Cancer Inst 2005 Jul 6;97(13):989-97 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15998952.
- Wardle J, Miles A, Atkin W. Gender differences in utilization of colorectal cancer screening. J Med Screen 2005;12(1):20-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15814015.
- UK Flexible Sigmoidoscopy Trial Investigators, Atkin WS, Edwards R, Kralj-Hans I, Wooldrage K, Hart AR, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet 2010 May 8;375(9726):1624-33 Available from: http://www.ncbi.nlm.nih.gov/pubmed/20430429.
- Segnan N, Armaroli P, Bonelli L, Risio M, Sciallero S, Zappa M, et al. Once-only sigmoidoscopy in colorectal cancer screening: follow-up findings of the Italian Randomized Controlled Trial--SCORE. J Natl Cancer Inst 2011 Sep 7;103(17):1310-22 Available from: http://www.ncbi.nlm.nih.gov/pubmed/21852264.
- Schoen RE, Pinsky PF, Weissfeld JL, Yokochi LA, Church T, Laiyemo AO, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med 2012 Jun 21;366(25):2345-57 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22612596.
- Atkin W, Wooldrage K, Parkin DM, Kralj-Hans I, MacRae E, Shah U, et al. Long term effects of once-only flexible sigmoidoscopy screening after 17 years of follow-up: the UK Flexible Sigmoidoscopy Screening randomised controlled trial. Lancet 2017 Apr 1;389(10076):1299-1311 Available from: http://www.ncbi.nlm.nih.gov/pubmed/28236467.
- Elmunzer BJ, Hayward RA, Schoenfeld PS, Saini SD, Deshpande A, Waljee AK. Effect of flexible sigmoidoscopy-based screening on incidence and mortality of colorectal cancer: a systematic review and meta-analysis of randomized controlled trials. PLoS Med 2012;9(12):e1001352 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23226108.
- Leaper M, Johnston MJ, Barclay M, Dobbs BR, Frizelle FA. Reasons for failure to diagnose colorectal carcinoma at colonoscopy. Endoscopy 2004 Jun;36(6):499-503 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15202045.
- Robertson DJ, Greenberg ER, Beach M, Sandler RS, Ahnen D, Haile RW, et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology 2005 Jul;129(1):34-41 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16012932.
- Singh H, Turner D, Xue L, Targownik LE, Bernstein CN. Risk of developing colorectal cancer following a negative colonoscopy examination: evidence for a 10-year interval between colonoscopies. JAMA 2006 May 24;295(20):2366-73 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16720822.
- van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol 2006 Feb;101(2):343-50 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16454841.
- The National Bowel Cancer Screening Program Quality Working Group. Improving colonoscopy services in Australia. Canberra: Australian Government Department of Health and Ageing; 2009 Available from: http://www.cancerscreening.gov.au/internet/screening/publishing.nsf/Content/3FD09B61D2B4E286CA25770B007D1537/$File/Improving%20col%20serv0709.pdf.
- Cancer Council Australia Colonoscopy Surveillance Working Party. Clinical Practice Guidelines for Surveillance Colonoscopy. Sydney: Cancer Council Australia; 2018 [cited 2018] Available from: https://wiki.cancer.org.au/australia/Guidelines:Colorectal_cancer/Colonoscopy_surveillance.
- Kaminski MF, Bretthauer M, Zauber AG, Kuipers EJ, Adami HO, van Ballegooijen M, et al. The NordICC Study: rationale and design of a randomized trial on colonoscopy screening for colorectal cancer. Endoscopy 2012 Jul;44(7):695-702 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22723185.
- Quintero E, Castells A, Bujanda L, Cubiella J, Salas D, Lanas Á, et al. Colonoscopy versus fecal immunochemical testing in colorectal-cancer screening. N Engl J Med 2012 Feb 23;366(8):697-706 Available from: http://www.ncbi.nlm.nih.gov/pubmed/22356323.
- Lidgard GP, Domanico MJ, Bruinsma JJ, Light J, Gagrat ZD, Oldham-Haltom RL, et al. Clinical performance of an automated stool DNA assay for detection of colorectal neoplasia. Clin Gastroenterol Hepatol 2013 Oct;11(10):1313-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23639600.
- Bibbins-Domingo K, Grossman DC, Curry SJ, Davidson KW, Epling JW Jr, García FAR, et al. Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. JAMA 2016 Jun 21;315(23):2564-2575 Available from: http://www.ncbi.nlm.nih.gov/pubmed/27304597.
- Young GP, Pedersen SK, Dekker E, Cole SR, Osborne JM, Symonds El et al. Evaluation of a 2-gene (IKZF1 and BCAT1) DNA blood test for detection of colorectal cancer. In: AASLD, AGA, ASGE, SSAT. Digestive Disease Week. 2014 May 3-6; Chicago.; 2014.
- Church TR, Wandell M, Lofton-Day C, Mongin SJ, Burger M, Payne SR, et al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut 2014 Feb;63(2):317-25 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23408352.
- Department of Health and Ageing. National bowel cancer screening program. Information for general practitioners. Canberra: DoHA; 2006.
- McMurrick P, Dorien S, Shapiro J. Bowel cancer - guide for the GP. Aust Fam Physician 2006 Apr;35(4):192-7 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16642233.
- Cole SR, Young GP, Byrne D, Guy JR, Morcom J. Participation in screening for colorectal cancer based on a faecal occult blood test is improved by endorsement by the primary care practitioner. J Med Screen 2002;9(4):147-52 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12518003.
- Salkeld GP, Solomon MJ, Short L, Ward J. Measuring the importance of attributes that influence consumer attitudes to colorectal cancer screening. ANZ J Surg 2003 Mar;73(3):128-32 Available from: http://www.ncbi.nlm.nih.gov/pubmed/12608975.
- Epidemiology Services Unit, Health Information Branch, Queensland Health. Bowel cancer knowledge, perceptions and screening behaviours: knowledge, attitudes & practices pre- and post-intervention surveys (2002 & 2004). Final report. Canberra: Bowel Cancer Screening Pilot Monitoring and Evaluation Steering Committee; 2004 Available from: http://www.cancerscreening.gov.au/internet/screening/publishing.nsf/Content/C4E3336BCE08842DCA2574EB007F73DB/$File/know-att.pdf.
- Millard FB. Bowel cancer screening in Australia. Aust Fam Physician 2006 Apr;35(4):188-91 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16642232.
- Turner GB, Chin MW, Foster NM, Emery J, Forbes GM. Attitudes of Western Australian general practitioners to colorectal cancer screening. Med J Aust 2006 Aug 21;185(4):237 Available from: http://www.ncbi.nlm.nih.gov/pubmed/16922675.
- Tong S, Hughes K, Oldenburg B, Del Mar C. Would general practitioners support a population-based colorectal cancer screening programme of faecal-occult blood testing? Intern Med J 2004 Sep;34(9-10):532-8 Available from: http://www.ncbi.nlm.nih.gov/pubmed/15482265.
- Harris M, Bennett J, Del Mar C, Fasher M, Foreman L, Furler J, et al. Guidelines for preventive activities in general practice. 7th ed. South Melbourne: Royal Australian College of General Practitioners; 2009 Available from: http://healthprofessionals.flyingdoctor.org.au/IgnitionSuite/uploads/docs/RACGP%20Guidelines%20for%20Preventive%20Activities%20in%20General%20Practice.pdf.