In Australia, colorectal cancer screening rates are sub-optimal and considerably lower than those of other countries. The purpose of the current review was to identify in relation to colorectal cancer screening: (i) the number of Australian and international community-based intervention studies published between 2002-2011, (ii) the proportion of intervention studies that had adopted a community-based approach and met the Cochrane Effective Practice and Organisation of Care study design criteria; and (iii) the effectiveness of community-based interventions with at least a moderate level of methodological rigour at increasing colorectal cancer screening rates. Electronic database searches identified 86 intervention studies, of which 21 used a community-based approach and 15 met Cochrane Effective Practice and Organisation of Care study design criteria. Overall, the methodological rigour of community-based intervention studies using Cochrane Effective Practice and Organisation of Care -accepted study designs was moderate. Only one methodologically robust Australian community-based study was identified. Based on findings from studies with moderate methodological rigour, a number of potential options which the National Bowel Cancer Screening Program might consider to increase screening rates are discussed. The current review highlights the urgent need for further methodologically rigourous, community-based colorectal cancer screening intervention research in the Australian setting.
Worldwide, colorectal cancer (CRC) accounts for 9.4% of all cancer diagnoses and ranks as the fourth leading cause of cancer-related deaths.1 Australia has one of the highest age-standardised rates for CRC in the world, with the crude incidence set to increase as a consequence of an ageing population.2 In Australia, as in other countries, fewer than 40% of cases are diagnosed at an early localised stage.3-5 CRC screening has demonstrated effectiveness in reducing the incidence of CRC through the identification and removal of precancerous adenomatous polyps, 6,7 and increasing the rate of detection of early-stage disease.8,9
In Australia, the National Bowel Cancer Screening Program (NBCSP) takes a community-based approach by offering a mailed one-off Faecal Occult Blood Test (FOBT) to people turning 50, 55 and 65 years of age.10 Participation rates in Australia’s NBCSP have remained at a consistent rate of approximately 40 per cent.10-13 These rates, however, are only reflective of participation among the selected age brackets incorporated in the program. Australian community- and population-based assessments of people aged over 50 have consistently demonstrated low levels of CRC screening participation.14-18 Two population-based studies among at-risk persons (aged 50 and over) prior to the NBCSP indicated that less than 20% of the at-risk population undertook FOBT screening in the previous five years.15 18 A recent evaluation following the inception of NBCSP found that 20% of people aged above 55 years of age had undertaken FOBT screening within the guideline-recommended two-year period.19 The Australian CRC screening rate compares poorly with that of other countries. For example, FOBT screening rates in the UK and Finnish screening programs are currently 52% and 71% respectively.20 21
It is too early to identify the likely impact of the NBCSP program on mortality and incidence reduction in Australia. Nonetheless, the most recent data on a small number of histologically confirmed NBCSP cases suggests a high rate of early-staged CRC detection (58.3%).10 Further, an earlier review of CRC detection methods (ie. NBCSP-screened versus symptomatic presentation) across 19 Australian hospitals highlighted a significant downgrading in staging of disease among NBCSP-detected CRCs.22 While these results show promise, there is a need for expansion of this program (ie. extending the offer of FOBT screening to all people aged between 50 and 75 years biennially) if the high rate of mortality reduction (15-33%) reported in screening randomised control trials (RCT) is to be achieved.6 923 24
The most comprehensive review of intervention studies aimed at increasing CRC screening was confined to studies conducted in the United States during 1998-2009.25 In Australia, relatively little is known about the effectiveness of methodologically robust community-based interventions, although the NBCSP has adopted a community-based approach. It is crucial to identify robust evidence of effective strategies for increasing screening rates at a community level in order to maximise the effectiveness of the program. The Cochrane Effective Practice and Organisation of Care Group (EPOC) checklist, which provides valuable criteria against which to judge the methodological rigour of intervention studies, has been used in this review.26 The purpose of this review was to identify, in relation to increasing CRC screening uptake: (i) the number of Australian and international community-based intervention studies published between 2002-2011; (ii) the proportion of intervention studies that had adopted a community-based approach and met EPOC study design criteria; and (iii) the effectiveness of community-based interventions with at least a moderate level of methodological rigour.
Intervention studies published in English aimed at increasing rates of CRC screening (eg. by FOBT, colonoscopy or sigmoidoscopy) were included in this review. Studies that examined solely knowledge or intention to screen, or compared compliance rates across CRC testing modalities were excluded. Studies that evaluated CRC testing solely among the following population groups were excluded: CRC patients; people with advanced adenoma or bowel-related disease; and those at high risk due to familial predisposition to CRC.
An electronic database search of Medline was conducted to identify relevant intervention studies published between 1 January 2002 and 11 October, 2011. This time period was considered appropriate, given that the National Health and Medical Research Council CRC screening guidelines were established in 1999 and that the wider adoption of supporting programs and interventions would take time to evolve. The Medline search included three search themes (colorectal cancer, screening and interventions) combined using the Boolean operator, “AND”. For a complete list of MeSH headings and search terms see table 1. The cochrane clinical trial database was also searched for relevant intervention studies using the following search terms, “colorectal neoplasms AND mass screening”.
All abstracts were reviewed by authors RJC and CLP to determine whether studies met the eligibility criteria. All relevant intervention studies were categorised based on the setting for recruitment or sampling: (i) primary care; (ii) community; or (iii) other. Intervention studies conducted in the primary care setting or recruiting persons directly from general practice registers were coded as “primary care”. Intervention studies sampling participants from an electoral roll/population register, using a broad sampling technique eg. state Driver’s licence databases, or directly recruiting participants from a community-setting, eg. seniors’ centres, were coded as “community”. Each intervention study coded as “community” was assessed against basic EPOC study design criteria: randomised control trial (RCT); controlled clinical trial (CCT); controlled before and after study (CBA); and interrupted time series (ITS). Intervention studies not meeting the above study designs were excluded.
Intervention studies coded as “community” and meeting EPOC-specified study design criteria (ie. RCT, CCT, CBA or ITS) were evaluated for methodological strength using the following EPOC criteria.27 For each criterion, a score of “yes” was assigned if the study met the criterion, “no” if it did not and “unclear” if there was insufficient information in the paper. For RCT, CCT, and CBA, these criteria included the following: 1) whether the allocation sequence was adequately generated (ie. the random component in the sequence generation process was described); 2) whether there was concealment of allocation (eg. unit of allocation by institution or team, a centralised randomisation scheme, an on-site computer system or sealed opaque envelopes); 3) whether baseline outcome measurements were similar in intervention and control groups (ie. the study reported whether baseline measurement was similar and, if not, whether appropriate adjusted analysis was performed); 4) whether baseline characteristics of study participants were reported and did not differ between experimental groups; 5) whether incomplete outcome data were adequately addressed (ie. missing data was unlikely to bias the results and the proportion of missing data was less than the effect size); 6) whether there was blinded allocation of intervention and control groups (ie. the primary outcome assessed blindly or by using an objective outcome); 7) whether the study was adequately protected against contamination (ie. it randomised by practice or institution, or it was unlikely for the control group to receive the intervention); 8) whether the study was free from selective reporting (ie. all relevant outcomes were reported); 9) whether the study was free from other risks of bias (ie. no evidence of other risk of bias). As a quality assurance measure, independent coding of intervention studies was conducted by two reviewers (RJC and SY). All differences were resolved by mutual discussion between coders and with a third-party (CLP), where necessary.
The Medline search found 1436 separate articles. Of these, 1350 articles were excluded as they were either descriptive studies or not relevant to increasing CRC screening. Of the remaining articles, 86 were intervention studies aimed at increasing CRC screening rates. A search of the Cochrane Clinical Trial database (n = 195) between 2002 and October 20, 2011 found no further intervention studies. The majority of intervention studies were conducted in the US (79%, 68/86). Few studies (9%, 8/86) had been undertaken in Australia, with the remainder of interventions (12%, 10/86) from the UK, Canada, Europe or Asia. Most studies (70%, 60/86) had sampled participants from either general practice registers or directly through primary care sites. Of the remaining interventions, participants were either recruited using a community or population-based sampling technique (24%, 21/86) or “other” sampling method (6%, 5/86). Of the eight studies conducted in Australia, only four had adopted a community- or population-based sampling approach.
Of the 21 community-based intervention studies,28-48 only 15 (71%) met EPOC criteria relating to research design; all of these studies were RCT.29,31-35,37,39-42,44, 45,47,48 The remaining six articles did not use an accepted EPOC study design.28,30,36,38,43,46 Overall, 10 out of 15 (66%) RCT scored at least five points or higher on methodological rigour (see Table 2). These studies were deemed to be of at least moderate methodological rigour and were evaluated for effectiveness at increasing CRC screening.
An overview of the intervention studies scoring five or more on the EPOC criteria for methodological rigour were grouped by intervention type: mail, non-mail (e.g. telephone, audiovisual, computer); and multiple component strategies. Findings are presented in tables 3, 4, and 5, respectively. As shown in table 3, mail-based strategies with FOBT invitation can achieve participation rates of 51 to 59%,34,47,48 with increased participation evident in two studies that had adopted pre-notification prior to the screening invitation.47,48 Tailoring of the screening invitations appeared to have a modest effect on screening participation.34 As described in table 4, non-mail-based strategies, including the use of an interactive electronic tool or video education, appeared to increase the rate of CRC screening significantly, compared to the usual care or standard condition.39,40 Studies of telephone-based outreach had mixed findings with samples drawn from private healthcare funds.35 Multiple-component interventions (see table 5) that involved education or self-empowerment of cultural groups showed modest improvements in CRC screening.31,32 An Australian study among lower socio-economically disadvantaged persons, contrary to expectation, indicated that the adoption of a decision making aid (ie. booklet and DVD) significantly decreased FOBT completion, compared to controls who received a standard NBCSP information package.45 Study findings from Powe et al.’s intervention should be considered with caution, given substantial limitations related to sample size and an under-representation of males. Further, the authors report the primary outcome (return of FOBT) as significant across group membership, despite not meeting the widely accepted statistically significant cut-point of p <.05.
The review indicated that most CRC screening intervention studies occurred in the US. Given the Australian setting differs from the US in terms of health system and population sub-groups, US findings may not generalise to the Australian setting. Only eight intervention studies were conducted in Australia, four of which adopted a community-based approach.28,30,37,45 Of these studies, only two used an EPOC-accepted study design.37,45 The lack of robust research with relevance to the community-based approach taken by the NBCSP is surprising.
The degree to which study findings are indicative of a high level of evidence is dependent on methodological rigour.49,50 Of the 21 intervention studies in this review adopting a community-based approach, 15 had used EPOC-accepted study designs, and 10 had at least moderate methodological rigour. However, only one methodologically robust community-based study was undertaken in Australia,45 providing scant evidence to base decisions on how to approach the crucial issue of maximising screening rates for CRC in Australia.
The NBCSP adopts a pre-notification strategy shown to be effective at increasing FOBT participation rates.37,47,48 Based on the studies with at least moderate experimental rigour, it would appear that there are a number of additional potential options which the NBCSP might consider to increase screening rates for the age groups included in the program. First, the relative value of co-ordinated advocacy from other respected organisations, including Cancer Council and other public health organisations, should be further examined.46 In addition, it should be noted that Australian studies, although not using an EPOC-accepted study design, have indicated that FOBT participation is improved one-off and over time if a letter of invitation includes general practitioner endorsement.28,46 Further, in the UK, for non-responders to CRC screening invitations, a final letter is sent to non-responders’ general practitioners.51 Given that direct linkage of the patient to his or her general practitioner is not easily attainable in Australia for community-based recruitment approaches, it is important to consider how the active endorsement of the NBCSP by general practitioners may be co-ordinated with NBCSP initiatives. In addition, the timing of reminder letters following non-response in the Australian screening program is at eight weeks, much longer than that adopted in the UK screening program, which is achieving higher rates of participation.20 Therefore, it is worthwhile to explore whether a shorter follow-up interval may increase participation rates.
It is important to consider the unexpected study findings found among an Australian cohort of lower socio-economic people aged between 55-64 years of age sent FOBT kits, where a particularly high rate of FOBT test return was identified among the control group (75% of those receiving standard NBCSP booklets), a rate higher than that in the intervention group (59% of those receiving a decision aid and accompanying DVD).45 It is noteworthy that two weeks following mail-out, participants received a follow-up telephone interview assessing other primary outcomes, ie. knowledge, attitudes and informed choice. It is possible that this follow-up call lifted participation rates across both groups. The incorporation of a telephone-based reminder system may be worth consideration in the NBCSP. Additionally, for the control group the FOBT return rate of 75% among a wide age-bracket (55-64 years) was achieved, much higher than the consistent return rate of approximately 40% achieved in the NBCSP. Overall, in addition to the above opportunities for increasing screening rates among those invited into the NBCSP, it should also be noted that a dominant rate-limiting factor for population-based screening uptake in Australia appears to be the limited age-brackets invited to screen in the NBCSP. The greatest opportunity for future increases in FOBT screening participation largely relies on opening the program to the entire at-risk population (all those aged between 50-74 years) for repeated screening.
With the exception of age and gender, there were relatively little data in this review about responses to interventions among population groups known to experience lower rates of CRC screening participation eg. Indigenous people, people from non-English speaking backgrounds and those from lower socio-economic backgrounds. Some studies indicated that younger people in the at-risk group had a considerably lower rate of screening participation compared to older age groups.35,40 A few studies used targeted approaches for certain cultural groups, eg. African Americans.31 However, findings for socio-cultural groups in the US may not generalise to the Australian context. In Australia, relatively little robust research has been directed towards population sub-groups less likely to participate in CRC screening, although the NBCSP has focused efforts towards reaching these groups, particularly through state-based initiatives. The present review identified only one Australian intervention that targeted CRC screening among lower socio-economic groups.45 It is important that future interventions pay close attention to population groups experiencing lower rates of CRC screening, to maximise broad participation and avoid increasing screening inequality.
Searching grey literature and non-English language studies was beyond the scope of the current review. Therefore, it is possible that some studies were missed. The ability to generalise international study findings to the Australian-setting should be considered with caution, given differing health care systems and CRC screening provisions across countries. The NBCSP currently offers one-off FOBT screening to just three selected age groups. This is in contrast to the evidence base for the benefits and cost-effectiveness of CRC screening, based on biennial screening from 50-74 years.52 In addition, it is important to monitor CRC screening rates across the entire at-risk population, as NBCSP monitoring reports are only reflective of participation among the selected age brackets. Unfortunately, given the low number of Australian community-based intervention studies identified in this review, few data are available to indicate the most effective approach for improving population-level CRC screening participation rates to an optimal level. The current review highlights the urgent need for more methodologically rigorous community-based CRC screening intervention research in the Australian-setting.
Recognition and thanks to Australian Rotary Health Research Fund and the Rotary District 9650 Bowelscan Committee for their funding of PhD scholar – Ryan J Courtney.
1. Boyle P, Levin B. International Agency for Research on Cancer. World Cancer Report 2008.
2. GLOBOCAN 2008 International Agency for Research on Cancer. [Internet]. Colorectal cancer incidence and mortality worldwide 2008. [cited 2011 Oct 1]. Available from: http://globocan.iarc.fr/factsheets/cancers/colorectal.asp
3. National Cancer Institute [Internet]. Surveillance Epidemiology and End Results. SEER Stat fact sheets: Colon and rectum, 2010. [cited 2011 Oct 2]. Available from: http://seer.cancer.gov/statfacts/html/colorect.html
4. Australian Health Technology Advisory Committee. Colorectal cancer screening. Canberra: Commonwealth Department of Health and Family Services.1997.
5. National Cancer Intelligence Network [Internet]. Colorectal cancer survival by stage – NCIN data briefing, 2009. [cited 2011 Oct 4]. Available from: http://www.ncin.org.uk/publications/data_briefings/colorectal_cancer_survival_by_stage.aspx
6. Mandel JS, Church TR, Bond JH, Ederer F, Geisser MS, Mongin SJ, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med. 2000;343(22):1603-7.
7. Winawer SJ, Zauber AG, Ho MN, O’Brien MJ, Gottlieb LS, Sternberg SS, et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med. 1993;329(27):1977-81.
8. 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;191(7):378-81.
9. Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, Amar SS, Balfour TW, et al. Randomised controlled trial of fecal occult blood screening for colorectal cancer. Lancet. 1996;348(9040):1472-77.
10. Australian Institute of Health and Welfare and Australian Government Department of Health Ageing. National Bowel Cancer Program: annual monitoring report 2009 data and data supplement 2010. Cancer Series no.57. Cat. No. CAN 53. Canberra: AIHW, 2010.
11. Australian Institute of Health and Welfare and Australian Government Department of Health Ageing. National Bowel Cancer Screening Program monitoring report 2008. Cancer series 44. Cat. no. 40. Canberra: AIHW, 2008.
12. Australian Institute of Health and Welfare and Australian Government Department of Health Ageing. National Bowel Cancer Screening Program: annual monitoring report 2009. Cancer series no. 49. Cat. no. CAN 45.Canberra :AIHW, 2009.
13. Australian Institute of Health and Welfare and Australian Government Department of Health Ageing. National Bowel Cancer Screening Program monitoring report 2007. Cancer series no. 40. Cat. no. CAN 35. Canberra: AIHW, 2008.
14. Thomas RJ, Clarke VA. Colorectal cancer: a survey of community beliefs and behaviours in Victoria. Med J Aust. 1998;169(1):37-40.
15. Cockburn J, Paul CL, Tzelepis F, McElduff P, Byles J. Screening for bowel cancer among NSW adults with varying levels of risk: a community survey. A N Z J Public Health. 2002;26(3):236-41.
16. Weller DP, Owen N, Hiller JE, Willson K, Wilson D. Colorectal cancer and its prevention: prevalence of beliefs, attitudes, intentions and behaviour. Aust J Public Health.1995;19(1):19-23.
17. Carriere P, Baade P, Newman B, Aitken J, Janda M. Cancer screening in Queensland men. Med J Aust. 2007;186(8):404-07.
18. Weber MF, Banks E, Ward R, Sitas F. Population characteristics related to colorectal cancer testing in New South Wales, Australia: results from the 45 and Up study cohort. J Med Screen. 2008;15(3):137-42.
19. Courtney RJ, Paul C, Sanson-Fisher R, Macrae F, Carey M, Attia J, et al. Colorectal (bowel) cancer screening in Australia: a community-level perspective (in press). Med J Aust 2011.
20. Weller D, Coleman D, Robertson R, Butler P, Melia J, Campbell C, et al. The UK colorectal cancer screening pilot: results of the second round of screening in England. Br J Cancer. 2007;97(12):1601-05.
21. Malila N, Oivanen T, Malminiemi O, Hakama M. Test, episode, and programme sensitivities of screening for colorectal cancer as a public health policy in Finland: experimental design. BMJ. 2008;3371-75.
22. Ananda SS, McLaughlin SJ, Chen F, Hayes AP, Hunter AA, Skinner IJ, et al. Initial impact of Australia’s National Bowel Cancer Screening Program. Med J Aust. 2009;191(7):378-81.
23. Kronborg O, Fenger C, Olson J, Jorgensen OD, Sondergaard Ol. Randomised study of screening for colorectal cancer with faecal occult blood test. Lancet. 1996;348(9040)1467-71.
24. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM et al Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota colon cancer study. N Engl J Med. 1993;328(19):1365-71.
25. Holden D, Harris R, Porterfield D, Jonas D, Morgan L, Reuland D, et al. Enhancing the use and quality of colorectal cancer screening. Evidence Report/Technology Assessment No 190. 2010;AHRQ Publication No. 10-E-002. Rockville, MD: Agency for Healthcare Research and Quality.
26. Cochrane Effective Practice and Organisation of Care Review Group (EPOC) [Internet]. Data collection checklist. [cited 2011 Oct 10] Available from: http://epoc.cochrane.org/sites/epoc.cochrane.org/files/uploads/datacollectionchecklist.pdf
27. Cochrane Effective Practice and Organisation of Care Review Group (EPOC). 6.4.1 Risk of bias for studies with a separate control group (RCTs, CCTs, CBAs) [Internet]. [cited 2011 Oct 12]. Available from: http://epoc.cochrane.org/sites/epoc.cochrane.org/files/uploads/Risk%20of%20Bias%2005-01-2009.doc
28. 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.
29. Church TR, Yeazel MW, Jones RM, Kochevar LK, Watt GD, Mongin SJ, et al. A randomized trial of direct mailing of fecal occult blood tests to increase colorectal cancer screening. J Natl Cancer Inst. 2004;96(10):770-80.
30. Corbett M, Chambers SL, Shadbolt B, Hillman LC, Taupin D. Colonoscopy screening for colorectal cancer: the outcomes of two recruitment methods. Med J Aust. 2004;181(8):423-7.
31. Powe BD, Ntekop E, Barron M. An intervention study to increase colorectal cancer knowledge and screening among community elders. Public Health Nurs. 2004;21(5):435-42.
32. Braun KL, Fong M, Kaanoi ME, Kamaka ML, Gotay CC. Testing a culturally appropriate, theory-based intervention to improve colorectal cancer screening among Native Hawaiians. Prev Med. 2005;40(6):619-27.
33. Lipkus IM, Skinner CS, Dement J, Pompeii L, Moser B, Samsa GP, et al. Increasing colorectal cancer screening among individuals in the carpentry trade: test of risk communication interventions. Prev Med. 2005;40(5):489-501.
34. Marcus AC, Mason M, Wolfe P, Rimer BK, Lipkus I, Strecher V, et al. The efficacy of tailored print materials in promoting colorectal cancer screening: results from a randomized trial involving callers to the National Cancer Institute’s Cancer Information Service. J Health Commun. 2005;10 Suppl:183-104.
35. Basch CE, Wolf RL, Brouse CH, Shmukler C, Neugut A, DeCarlo LT, et al. Telephone outreach to increase colorectal cancer screening in an urban minority population. Am J Public Health. 2006;96(12):2246-53.
36. Sarfaty M, Feng S. Choice of screening modality in a colorectal cancer education and screening program for the uninsured. J Cancer Educ. 2006;21(1):43-9.
37. Cole SR, Smith A, Wilson C, Turnbull D, Esterman A, Young GP. An advance notification letter increases participation in colorectal cancer screening. J Med Screen. 2007;14(2):73-5.
38. Katz ML, Tatum C, Dickinson SL, Murray DM, Long-Foley K, Cooper MR, et al. Improving colorectal cancer screening by using community volunteers: results of the Carolinas cancer education and screening (CARES) project. Cancer. 2007;110(7):1602-10.
39. Ruffin MT, Fetters MD, Jimbo M. Preference-based electronic decision aid to promote colorectal cancer screening: results of a randomized controlled trial. Prev Med. 2007;45(4):267-73.
40. Gimeno-Garcia AZ, Quintero E, Nicolas-Perez D, Parra-Blanco A, Jimenez-Sosa A. Impact of an educational video-based strategy on the behavior process associated with colorectal cancer screening: a randomized controlled study. Cancer Epidemiol. 2009;33(3-4):216-22.
41. Maxwell AE, Bastani R, Danao LL, Antonio C, Garcia GM, Crespi CM. Results of a community-based randomized trial to increase colorectal cancer screening among Filipino Americans. Am J Public Health. 2010;100(11):2228-34.
42. Morgan PD, Fogel J, Tyler ID, Jones JR. Culturally targeted educational intervention to increase colorectal health awareness among African Americans. J Health Care Poor Underserved. 2010;21(3 Suppl):132-47.
43. Nguyen TT, Love MB, Liang C, Fung L-C, Nguyen T, Wong C, et al. A pilot study of lay health worker outreach and colorectal cancer screening among Chinese Americans. J Cancer Educ. 2010;25(3):405-12.
44. Simon SR, Zhang F, Soumerai SB, Ensroth A, Bernstein L, Fletcher RH, et al. Failure of automated telephone outreach with speech recognition to improve colorectal cancer screening: a randomized controlled trial. Arch Intern Med. 2010;170(3):264-70.
45. Smith SK, Trevena L, Simpson JM, Barratt A, Nutbeam D, McCaffery KJ. A decision aid to support informed choices about bowel cancer screening among adults with low education: randomised controlled trial. BMJ. 2010;341:c5370.
46. Zajac IT, Whibley AH, Cole SR, Byrne D, Guy J, Morcom J, et al. Endorsement by the primary care practitioner consistently improves participation in screening for colorectal cancer: a longitudinal analysis. J Med Screen. 2010;17(1):19-24.
47. Libby G, Bray J, Champion J, Brownlee LA, Birrell J, Gorman DR, et al. Pre-notification increases uptake of colorectal cancer screening in all demographic groups: a randomized controlled trial. J Med Screen. 2011;18(1):24-9.
48. van Roon AHC, Hol L, Wilschut JA, Reijerink JCIY, van Vuuren AJ, van Ballegooijen M, et al. Advance notification letters increase adherence in colorectal cancer screening: a population-based randomized trial. Prev Med. 2011;52(6):448-51.
49. Evans D. Hierarchy of evidence: a framework for ranking evidence evaluating healthcare interventions. J Clin Nurs. 2003;12(1):77-84.
50. Harbour R, Miller J. A new system for grading recommendations in evidence based guidelines. BMJ. 2001;323:334.1.
51. Weller D, Moss S, Butler P, Campbell C, Coleman D, Melia J, et al. English pilot of Bowel Cancer Screening: an evaluation of the second round. Edinburgh: The Institute of Cancer Research. 2006.
52. Pignone MP, Flitcroft KL, Howard K, Trevena L, Salkeld GP, St John J. Costs and cost-effectiveness of full implementation of a biennial faecal occult blood test screening program for bowel cancer in Australia. Med J Aust. 2011;19(4):180-85.