Colorectal cancer screening in Europe: differences in approach; similar barriers to overcome
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- Cite this article as:
- West, N.J., Boustière, C., Fischbach, W. et al. Int J Colorectal Dis (2009) 24: 731. doi:10.1007/s00384-009-0690-6
Worldwide diagnoses of bowel cancer approximate an estimated one million new cases per year, comprising 9% of all cancer cases, and this has continued to increase over the last 25 years. With the association between cancer risk and increasing age, together with the suggestion that by 2015 there will be a 22% increase in the proportion of the population aged over 65 years and a 50% increase in the proportion of people aged over 80 years, there is likely to be a significant increase in the demand on cancer services throughout Europe and the rest of the world. This article discusses the current state of bowel cancer screening within Europe.
KeywordsColorectal cancerBowel cancerScreeningBowel preparation
Epidemiology of colorectal cancer
Worldwide diagnoses of bowel cancer approximate an estimated one million new cases per year, comprising 9% of all cancer cases, and this has continued to increase over the last 25 years .
Estimated age-standardised incidence rates (European standard) per 100,000 by site, sex and country, 2006
Colon and rectum (C18–21)
European Union (EU25)
EEA and Switzerland
Republic of Moldova
Serbia and Montenegro
Estimated age-standardised mortality rates (European standard) per 100,000 by site, sex and country, 2006
Colon and rectum (C18–21)
European Union (EU25)
EEA and Switzerland
Republic of Moldova
Serbia and Montenegro
With the association between cancer risk and increasing age, together with the suggestion that by 2015 there will be a 22% increase in the proportion of the population aged over 65 years and a 50% increase in the proportion of people aged over 80 years , there is likely to be a significant increase in the demand on cancer services throughout Europe and the rest of the world.
CRC develops via the adenoma–carcinoma sequence [5–7], although it can take up to 10 years for malignancy to develop in this way , which provides an opportunity for screening with the interception of the adenoma via polypectomy at the time of colonoscopy with early detection resulting in improved outcomes with acceptable morbidity.
Summary of the FOBT trials
Randomised to screening or control groups only after agreeing to enter trial
Randomly selected from GP and population registers (Funen subjects only invited to further rounds of screening if completed first round)
Type of FOBT used
HemOccult II (unrehydrated)
HemOccult II (rehydrated)
Screening interval (years)
1 or 2 (2 groups)
Sigmoidoscopy and DCBE
No. of screening rounds
Annual group, 11; biennial group, 6
Last reported follow-up (years)
Compliance with FOBT for first (%)
Reduction in mortality (%)
Ann, 33; bi, 21
Case–control studies, which assume complete compliance, have shown that combining FOBT and flexible sigmoidoscopy (FS), CRC mortality rates can be reduced by approximately 35% [16, 17]. However, it has been suggested that utilising this strategy may miss up to 24% of advanced neoplasia (defined by the authors as a polyp with villous features or the presence of high-grade dysplasia or invasive cancer) .
Enthusiasts for colonoscopic screening  suggest that FS examination, as a screening modality, is second best because of the miss rate for neoplasia out of reach of the flexible sigmoidoscope and this has raised an argument for colonoscopy to be considered as the sole screening investigation [18, 20, 21]. Additionally, preliminary results from the Italian CRC screening programme reveal that 39% of screen-detected cancers are located proximal to the splenic flexure , and this supports the observation of a continued rightward-shift in colonic cancer distribution which has previously been demonstrated both in United States  and European populations  during the past three decades, lending further support to this argument.
In the future, newer technologies that expose the subject to less risk may be championed as the favoured screening tool: interest is growing in the use of computed tomographic colonography (CTC) and a recent study of more than 3,000 patients reported findings that support the use of CTC as a primary screening test prior to the use of optical colonoscopy .
Colorectal cancer screening in Europe
Thousands of deaths could be prevented within Europe with the use of bowel cancer screening programmes but few countries have these in place and those that do acknowledge lower than ideal compliance rates.
There are wide discrepancies throughout Europe in survival for CRC patients due to poor patient education, late presentation of disease, lack of screening and insufficient funding for health care. Despite the cost of treatment of advanced stage cancer being approximately five times greater than for surgical treatment of an early screen-detected cancer , organised bowel cancer screening programmes are not common in Europe. The current strategies for some European countries are set out below:
The UK National Health Service Bowel Cancer Screening Programme
In 2004, the Secretary of State for Health announced the launch of the National Health Service Bowel Cancer Screening Programme (NHS BCSP) for 2006. This was in acknowledgement of the government's commitment to reduce cancer deaths in those under the age of 75 by at least 20% by 2010  and in response to the NHS Cancer Plan affirming the commitment to a national screening programme, subject to effective evidence of the pilot . The programme is expected to be rolled out nationally by 2009, with 14 centres operational by March 2007 utilising a central budget of £10 million for 2006/2007 and £25 million for 2007/2008.
The NHS BCSP uses biennial FOBT of 60- to 69-year-olds with the offer of colonoscopy for those who test positively. The programme is arranged via five programme hubs around the country with up to 20 local screening centres assigned to each. A single hub will cover a population of about ten million people. It will be the responsibility of each hub to send the screenees the FOBT, to send the results to the patient and their general practitioner (GP) and to arrange a follow-up visit for those with a positive test.
Each screening centre will serve a population of between 500,000 and 2,000,000 people. Assuming an uptake of 60% and a positivity rate of 2%, based on the pilot study , this may result in an estimated 300 extra colonoscopies per year, equating to one or two extra endoscopy lists per week. Outcomes and complications are being closely audited.
582,742 invitations were sent out nationally
537,770 returned, i.e. 52% compliance
9,946 self-referrals (70 years plus)
5,077 positive FOBT (1.8%)
4,344 attendees to a specialist nurse clinic
1,523 (44%) polyps
382 (11%) cancers detected
The agreed UK bowel screening programme is a pragmatic solution applied to the current financial and service restraints of the NHS that is expected to result in a reduction in mortality of patients from CRC within the UK. Following a promising initial analysis of the activity of the NHS BCSP across the country, the government has recently agreed to increase the age of inclusion into the programme to 74 years by 2010.
The Italian bowel cancer screening programme
A national campaign for CRC screening was officially launched in late 2005. The Ministry of Health has asked each regional health authority to organise the programme for their region providing specific extra funds for this purpose. Each region is able to make specific choices concerning the screening modalities used (e.g. FS or FOBT).
To date, CRC screening programmes have been launched in 11 out of the 21 Italian regions predominantly located in the north of the country. Except for Piedmont, where FS is being used as the primary screening modality, all other regions are using an immunochemical FOBT followed by total colonoscopy in FOBT-positive subjects. The Lecco province is the pilot province where the first round of CRC screening has been completed.
The Lecco colorectal cancer screening programme
The programme has been organised in this pilot area (one of the 11 provinces of Lombardy) according to the schedule of conditions defined by regional health authorities. It commenced in February 2006 using FOBT every 2 years in the target population followed by total colonoscopy in FOBT-positive individuals.
The target population for screening comprises 80,915 men and women aged between 50 and 69 years resident in the province. Criteria for exclusion are: history of colorectal adenoma or cancer, known inflammatory colonic disease and recent (within 3 years), well-documented complete colonoscopy.
78, 083 invitations were sent out regionally
36,693 returned, i.e. 49.6% compliance
2,392 positive FOBT (6.5%)
1,523 (44%) polyps
382 (11%) cancers detected
The screenee receives a letter of invitation by the community health care centre and the FOBT is distributed by pharmacists and GPs. In urban areas, subjects are invited to bring back the FOBT to local pharmacies; however, rurally, Red Cross volunteers collect the test from the subject. Once tested, individuals with a positive result are contacted by a nurse specialist in order to discuss arrangements for follow-up colonoscopy.
Specific colonoscopy lists are integrated within the existing endoscopy service and screening colonoscopies are usually scheduled within a maximum of 20 working days from the notification of FOBT positivity. Any further investigations or treatment needed are performed locally and a quality assurance infrastructure has been specifically set up to monitor colonoscopy performance.
The French bowel cancer screening programme
A national screening campaign was started in 2003 based upon biennial FOBT for screening subjects aged between 50 and 74 years using colonoscopy as the investigation of choice for those testing positive. Although currently, a guaiac-based FOBT test is used, a discussion is running within the National Cancer Institute to switch to an immunological-based test in the near future.
Exclusion of subjects for the test include a history of CRC or adenoma or other colonic disease requiring a colonoscopy, a first-degree relative affected with CRC before the age of 65 or two second-degree relatives affected or a total colonoscopy within the past 5 years.
The screening is organised via a local specific structure with precise financial and technical regulations. The screening process, from sending tests to collecting and reading the results, and procedures for the follow-up of positive cases are very well-defined and standardised. Contrasting with the UK, the GP is essential to the logistics of the programme and responsible for the implementation and follow-up of the test result for the screenees.
By the end of 2006, 23 out of 90 districts were participating, with an average 54% compliance of this population. The number of districts increased by more than 50% by the end of 2007, with 25 new districts starting the programme in December 2007, and a further 25 districts are expected to start before summer 2008. Local and regional meetings have and are being arranged around the country to educate and inform the population about the programme.
621,449 invitations sent (FOBT)
324,389 responders, i.e. 52.2% compliance
9,427 (2.9%) positive FOBT
7,947 (84.3%) colonoscopies
763 (9.6%) CRCs (>80% of cancers were detected as stage T1 or T2)
2,623 adenomas (33.0%)
In France, as with all countries who have or plan to have a screening programme, issues have been recognised which may give limitations to a successful programme such as the choice of FOBT to use (e.g. guaiac or immunological) and the best screening method (e.g. FOBT, colonoscopy, CT colonography, video capsule, etc.). The ultimate goal is to achieve screening for more than 65% of the eligible population with a 90% uptake of colonoscopies for those subjects with a positive test.
In Germany, there are 71,000 new cases of CRC per year and 27,000 deaths due to the disease. A National Cancer Prevention Programme incorporating screening colonoscopy and FOBT has been established since 2002. Every subject over the age of 55 years is offered colonoscopy with a second colonoscopy offered after 10 years if no neoplasms are found and the screenee is below the age of 65 at the first screening colonoscopy. Every subject over the age of 50 years is offered an annual FOBT, with a biennial test after the age of 55. This test is recommended for those patients who do not want to go undergo colonoscopy.
About 1.5 million colonoscopies were performed between January 2003 and December 2005 with an uptake of 8.8% for men and 10.2% for women. Including subjects undergoing colonoscopy via private insurance companies, the total compliance is about 12%. This figure is acknowledged as being lower than ideal but it is hoped that around 33% of the eligible population will accept colonoscopic screening within the next 10 years with the recruitment of family doctors educating patients about the benefits of the programme.
For 1,346,217 screening colonoscopies performed, adenomas were found in 18.9% of subjects and cancers in 0.8%. Of those 3,073 patients with a screened cancer, 46.8% had stage I disease, 22.6% stage II, 21.2% stage III and 9.4% stage IV. There has been a 10% reduction in mortality from CRC from approximately 30,000 in 2002 to 27,000 in 2005. There was a caecal intubation rate of 95% with a total complication rate of 0.3% (specifically 0.18% for bleeding and 0.02% for perforations).
Although in 2004, 4,545,000 FOBTs were performed in Germany, no data are available to correlate compliance of colonoscopy for those individuals who tested positively.
Currently, there is no CRC screening programme in The Netherlands. A study comparing guaiac-based FOBT (HemOccult) with an immunochemical test (OC-sensor mu) is currently being undertaken at the Universities of Amsterdam and Nijmegen (each centre with 10,000 subjects) encompassing 20,000 subjects aged between 50 and 74 years. Those with a positive test will be followed up with a colonoscopy.
Also, a comparative study is being undertaken at the University of Rotterdam between the efficacy of sigmoidoscopy and two different occult blood tests (iFOBT and GuiacFOBT), with a total of 15,000 subjects.
Additionally, sigmoidoscopy, colonoscopy and faecal DNA are being compared at the University of Maastricht, with 3,000 subjects in each arm of the study. The efficacy of using different faecal DNA tests is being conducted at the Free University of Amsterdam.
The Ministry of Health is awaiting the results of these ongoing trails before recommending which programme to follow.
There is currently no national screening programme in Spain. That there are 17 different health care regions with a mixture of public and private health care systems utilised by the population are seen as potential barriers to the realisation of effective screening. However, individual health care regions are addressing the issue although the main focus seems to be on “at-risk groups”.
Catalonia has completed a pilot screening programme with the aim of extending a screening programme to the whole of the region by 2010.
Valencia has a screening programme in progress with a population of 113,447 encompassing three health regions, and in April 2007, Castellón launched a programme for the early detection of CRC for 16,390 subjects between 50 and 70 years old.
Phase I: screening with FOBT in 3,000 asymptomatic people over the age of 50 years,
Phase II: screening extended to relatives of patients with CRC.
Summary of bowel cancer screening in Europe
Current national screening programme
Yes, since 2006
Yes, since 2002
Yes, since 2003
Yes, since 2005
Percentage of country
Aim for 100% by 2009
Aim for 100% by end 2008
Aim for 100% by end 2009
If no programme, when planned?
Planned after results of trials to investigate optimal screening test
Screening age range (years)
Likely 50 and above
Depends on region: FOBT-immuno (NB Piedmont using FS)
12 for colonoscopy (data unavailable for FOBT)
54 for FOBT
From Lecco province (pilot province), 49.6 for FOBT
Percentage of patients with pathology after colonoscopy, e.g. adenoma, carcinoma
CRC, 11; adenomas, 44
CRC, 0.8; adenomas, 18.9
CRC, 9.6; adenomas, 33
CRC, 4; adenomas, 48
Caecal intubation rate (%)
Perforation rate (%)
Bleeding complications (%)
Unavailable at time of publication
Unavailable at time of publication
One of the most important barriers to a widespread CRC prevention screening programme is the suitability of the test to the population it is being applied to. Thus, FOBT and colonoscopy need to be acceptable to this population, as compliance has been cited as the most important determinant of effectiveness for models of bowel cancer screening . It is also recognised that those individuals who perceive screening procedures to be embarrassing, uncomfortable or inconvenient are less likely to participate [31–33].
In a questionnaire study seeking to identify reasons for participant reluctance to undergo screening colonoscopy, comprising those respondents never screened (n = 126) and previously screened (n = 132), the most common reason given by both groups was unwillingness to take bowel preparation (66% and 57%, respectively) ; the second most preferred solution expressed by both groups of respondents was for small volume bowel preparation. Thus, bowel preparation has implications for compliance of screenees and, therefore, for the success of any screening programme.
The most common adverse symptoms from taking bowel preparation are nausea (and vomiting to a lesser degree), abdominal bloating and abdominal pain (more common with hyperosmolar solutions, e.g. sodium picosulphate) and a recent review  has highlighted the potential risks of taking bowel preparation, which include death in the most extreme cases. The majority of risk is primarily related to dehydration and electrolyte fluxes, especially in the elderly patients with co-morbidity (e.g. cardiac failure and renal failure) and those on medication that may influence fluid balance or electrolytes . To reduce the risk of complications and to increase patient compliance, the authors advocate tailoring the preparation to the patient, optimising patient education and promoting adequate hydration both before and after the examination as being of paramount importance.
In a meta-analysis comparing sodium phosphate and polyethylene glycol, the former gave improved bowel preparation and was better tolerated by patients ; this is in accordance with other studies  relating to the inverse relationship between volume of bowel preparation and patient preference/compliance, as polyethylene glycol is needed to be taken in larger volumes. However, a later study found that a polyethylene glycol preparation based on the GoLytely formulation (Klean-Prep) achieved better colonic visualisation than a sulphate-free polyethylene glycol preparation based on the NuLytely formulation (Endofalk) or a sodium phosphate preparation (Fleet) .
More recently, a new formulation of polyethylene glycol plus ascorbic acid has been shown to be as effective as standard polyethylene glycol, with the advantage that it can be taken in smaller volumes, 2 L compared with 4 L for standard polyethylene glycol preparation, which may improve patient acceptability and, therefore, compliance .
Poor bowel preparation is associated with increased miss rate for polyps [39, 40], greater procedural risk , increased cost , longer intubation times  and incomplete colonoscopy in up to 20% of examinations . If any of these factors contribute to an unfavourable experience for the screenee/patient, it will undoubtedly have a negative influence on the likelihood of the subject returning for subsequent examinations if required.
Bowel cancer screening programmes offer an excellent opportunity to beneficially alter the survival of patients with pre-cancerous polyps or early cancers, but a number of conditions need to be applied before this can be realised. The first and most important of these is that the population to which the programme is being applied need to be suitably receptive and compliant. Secondly, the bowel needs to be optimally clean and achieved by a preparation that is safe with a limited side effect profile. Thirdly, the colonoscopy should be performed by an experienced endoscopist trained to a standard to provide an examination which is safe, comfortable and can identify and safely treat any lesions encountered.
The compliance of the programmes currently in Europe report rates of between 40% and 54%. As a comparator, the UK National Breast Cancer Screening Programme achieved a compliance rate of 75.5% of the eligible screening population by the end of March 2006 and it is hoped that eventually similar levels will be achieved for bowel cancer screening.
The reasons given for patient non-compliance in bowel screening programmes are multiple and include: inconvenience; family or work conflicts; lack of interest; the absence of symptoms of bowel disease; embarrassment and worries about the test being unpleasant or painful . Clearly, the act of using a FOBT may be perceived by screenees to be embarrassing enough especially in the knowledge that a positive test will result in a colonoscopy, which again is potentially embarrassing and may be uncomfortable in some instances. Additionally, they will be required to take bowel preparation for the endoscopy. However, the benefit to that individual if an early neoplasia can be treated either endoscopically or with a “curative” operation would be considerable. Only by health care professionals understanding and overcoming these reasons for non-participation can compliance improve. Key to this is patient education via well-informed primary care physicians who are likely to be the first medical contact for the screenee, as endorsement by health care professionals has been shown to improve compliance [33, 44, 45]. Moreover, lack of a strong recommendation by a physician has been cited by patients as a reason for not undergoing screening , and because most people visit their doctor infrequently, the opportunity to discuss health prevention issues on these occasions has been recognised to be important . In mainland Europe, the GP will have an increasing responsibility to organise and enrol his/her patients into bowel cancer screening programmes.
Some patients would be positively influenced by information given by colon cancer survivors , including celebrities, which is a route of recruitment that might be explored in the future. Additionally, a recommendation from a relative, friend or colleague who has had a positive experience from bowel cancer screening will also serve to increase education and awareness and, therefore, hopefully compliance.
It is also important that screenees receive a personal invitation (“active individual invitation”) rather than a “general call-up”. And perhaps non-responders who fail to reply after being sent a postal reminder or second FOBT might receive a visit from a health care worker to enquire as to the reasons for that individuals reluctance to participate and at the same time address any worries, concerns or questions the potential screenee might have about the screening process. This strategy of course raises funding issues however.
For those screenees who do return a FOBT, it must be processed in a prompt manner including informing the subject of the result. For those who test positively, prompt contact from specifically trained health professionals within the screening team is needed to counsel the screenee about the practicalities of colonoscopy and the outcomes that may be encountered in terms of pathology and the likely increased chance of picking up early disease.
The importance of acceptable and safe bowel preparation has already been described, but to reduce intubation times, improve the pick-up rate of pathology and give effective cleaning, such that the need for a repeated examination is obviated, the choice of bowel preparation perhaps requires further consideration, tailored to the patient, using the minimal volume of preparation to achieve a “clean” colorectum. This again has implications for patient compliance.
Finally, continued training of endoscopists with closely audited performance and complication rates are paramount to provide accurate and comfortable colonoscopy especially if screenees are to return at the next round of screening.
Whichever screening methods are chosen across Europe and whether a common European approach to bowel cancer screening will emerge remains to be seen. However, the costs of such programmes will be balanced against the benefits of screening which include a reduction in the mortality from CRC, the detection of early cancers requiring less invasive surgery, lesser hospital in-patient admission days and the use of less adjuvant and palliative treatments.
Currently, the programmes for bowel cancer screening in Europe are different, where they exist, but the difficulties are similar: patient compliance is the core of screening and only when this has been maximised can bowel cancer screening realise its full potential: which could be the virtual elimination of sporadic CRC.