colorectal screening in europe

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REVIEW Colorectal cancer screening in Europe: differences in approach; similar barriers to overcome Nicholas J. West & Christian Boustière & Wolfgang Fischbach & Fabrizio Parente & Roger. J. Leicester Accepted: 26 February 2009 / Published online: 19 March 2009 # Springer-Verlag 2009 Abstract Worldwide diagnoses of bowel cancer approxi- mate 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. Keywords Colorectal cancer . Bowel cancer . Screening . Bowel 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 [1]. For women, colorectal cancer (CRC) is the second most common cancer diagnosis to breast cancer, comprising 195,400 cases, and in men, the third with 217,400 cases, behind prostate and lung cancer. In 2006, of the 1.7 million cancer deaths in Europe, 207,400 were caused by CRC (almost equally distributed between sexes), an estimated increase of 1.8% from 2004 [2]. The age-standardised incidence rates for CRC within Europe are given in Table 1. In the UK, about 55% of all patients diagnosed with CRC have lymph node or distant metastases (stage III or IV disease) at the time of diagnosis [3]. The 5-year relative age-standardised survival rate for CRC in the UK is 51.8%, with rates across central Europe at 61.5% (Spain), 61.2% (Germany), 59.9% (France), 59.4% (Italy) and 58.5% (The Netherlands) [4]. A summary of the age-adjusted 5-year mortality rates for CRC in Europe is given in Table 2. 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 [2], there is likely to be a Int J Colorectal Dis (2009) 24:731740 DOI 10.1007/s00384-009-0690-6 Competing interests NJ West has no competing interests. C Boustière, W Fischbach, F Parente and RJ Leicester have served on advisory panels for Norgine. Disclaimer This article was sponsored by Norgine. The company has had the opportunity to comment on the medical content and accuracy of the article; however, final editorial control resides with the authors/ journal. No payment was received for the authorship of this article N. J. West (*) Endoscopy Department, St Georges Hospital, London, UK e-mail: [email protected] C. Boustière Gastrointestinal, Endoscopic Unit, St Joseph Hospital, Marseilles, France W. Fischbach Internal Medicine, Academic Teaching Hospital, University of Würzburg, Würzburg, Germany F. Parente Gastroenterology, A. Manzoni Hospital, Lecco, Italy R. J. Leicester Endoscopy Department, St Georges Hospital, Blackshaw Road, London SW17 OQT, UK

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Page 1: Colorectal screening in Europe

REVIEW

Colorectal cancer screening in Europe: differencesin approach; similar barriers to overcome

Nicholas J. West & Christian Boustière &

Wolfgang Fischbach & Fabrizio Parente &

Roger. J. Leicester

Accepted: 26 February 2009 /Published online: 19 March 2009# Springer-Verlag 2009

Abstract Worldwide diagnoses of bowel cancer approxi-mate an estimated one million new cases per year,comprising 9% of all cancer cases, and this has continuedto increase over the last 25 years. With the associationbetween cancer risk and increasing age, together with thesuggestion that by 2015 there will be a 22% increase in theproportion 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 theworld. This article discusses the current state of bowelcancer screening within Europe.

Keywords Colorectal cancer . Bowel cancer . Screening .

Bowel preparation

Epidemiology of colorectal cancer

Worldwide diagnoses of bowel cancer approximate anestimated one million new cases per year, comprising 9%of all cancer cases, and this has continued to increase overthe last 25 years [1].

For women, colorectal cancer (CRC) is the second mostcommon cancer diagnosis to breast cancer, comprising195,400 cases, and in men, the third with 217,400 cases,behind prostate and lung cancer. In 2006, of the 1.7 millioncancer deaths in Europe, 207,400 were caused by CRC(almost equally distributed between sexes), an estimatedincrease of 1.8% from 2004 [2]. The age-standardisedincidence rates for CRC within Europe are given in Table 1.

In the UK, about 55% of all patients diagnosed withCRC have lymph node or distant metastases (stage III or IVdisease) at the time of diagnosis [3]. The 5-year relativeage-standardised survival rate for CRC in the UK is 51.8%,with rates across central Europe at 61.5% (Spain), 61.2%(Germany), 59.9% (France), 59.4% (Italy) and 58.5% (TheNetherlands) [4]. A summary of the age-adjusted 5-yearmortality rates for CRC in Europe is given in Table 2.

With the association between cancer risk and increasingage, together with the suggestion that by 2015 there will bea 22% increase in the proportion of the population agedover 65 years and a 50% increase in the proportion ofpeople aged over 80 years [2], there is likely to be a

Int J Colorectal Dis (2009) 24:731–740DOI 10.1007/s00384-009-0690-6

Competing interests NJ West has no competing interests. CBoustière, W Fischbach, F Parente and RJ Leicester have served onadvisory panels for Norgine.

Disclaimer This article was sponsored by Norgine. The company hashad the opportunity to comment on the medical content and accuracyof the article; however, final editorial control resides with the authors/journal. No payment was received for the authorship of this article

N. J. West (*)Endoscopy Department, St George’s Hospital,London, UKe-mail: [email protected]

C. BoustièreGastrointestinal, Endoscopic Unit, St Joseph Hospital,Marseilles, France

W. FischbachInternal Medicine, Academic Teaching Hospital,University of Würzburg,Würzburg, Germany

F. ParenteGastroenterology, A. Manzoni Hospital,Lecco, Italy

R. J. LeicesterEndoscopy Department, St George’s Hospital,Blackshaw Road,London SW17 OQT, UK

Page 2: Colorectal screening in Europe

Table 1 Estimated age-standardised incidence rates (European stan-dard) per 100,000 by site, sex and country, 2006

Country Colon and rectum (C18–21)

M F

Austria 57.6 30.9

Belgium 53.3 34.3

Cyprus 41.2 29.0

Czech Republic 94.4 46.0

Denmark 61.0 48.0

Estonia 50.0 33.9

Finland 39.2 29.4

France 59.8 36.8

Germany 70.2 45.1

Greece 31.0 21.3

Hungary 106.0 50.6

Ireland 65.2 36.9

Italy 52.0 30.3

Latvia 47.0 28.7

Lithuania 53.1 32.5

Luxembourg 61.9 36.1

Malta 51.5 36.2

The Netherlands 61.2 43.9

Poland 43.1 27.7

Portugal 58.9 30.9

Slovakia 87.1 42.6

Slovenia 69.0 36.3

Spain 54.4 25.4

Sweden 49.2 37.4

United Kingdom 54.9 34.8

European Union (EU25) 59.0 35.6

Iceland 50.2 36.8

Norway 66.4 51.2

Switzerland 79.1 55.6

EEA and Switzerland 59.4 36.1

Bulgaria 49.6 31.3

Romania 40.7 25.1

Albania 13.6 21.4

Belarus 42.8 29.0

Bosnia Herzegovina 34.6 27.3

Croatia 57.0 36.9

Macedonia 49.4 30.0

Republic of Moldova 38.7 26.7

Russian Federation 46.5 33.9

Serbia and Montenegro 41.0 30.4

Ukraine 41.7 27.0

Europe 55.4 34.6

Adapted from Ferlay et al. [2]

Table 2 Estimated age-standardised mortality rates (European stan-dard) per 100,000 by site, sex and country, 2006

Country Colon and rectum (C18–21)

M F

Austria 29.3 15.6

Belgium 25.2 15.4

Cyprus 19.3 14.5

Czech Republic 51.0 24.1

Denmark 30.3 24.1

Estonia 26.6 16.6

Finland 17.8 11.3

France 23.2 13.2

Germany 26.7 16.5

Greece 15.5 10.8

Hungary 54.4 26.7

Ireland 29.4 15.6

Italy 23.5 13.9

Latvia 27.7 16.8

Lithuania 28.8 15.7

Luxembourg 26.1 14.6

Malta 23.4 18.4

The Netherlands 26.3 17.4

Poland 31.5 17.4

Portugal 30.2 17.5

Slovakia 43.3 24.4

Slovenia 39.6 17.3

Spain 28.2 14.6

Sweden 20.7 15.4

United Kingdom 22.8 13.9

European Union (EU25) 26.5 15.6

Iceland 27.5 14.2

Norway 28.7 21.4

Switzerland 19.1 11.6

EEA and Switzerland 26.4 15.6

Bulgaria 26.5 15.0

Romania 23.5 14.5

Albania 7.3 9.9

Belarus 26.9 15.2

Bosnia Herzegovina 19.5 12.9

Croatia 40.7 18.1

Macedonia 26.6 14.1

Republic of Moldova 25.1 15.5

Russian Federation 30.8 19.7

Serbia and Montenegro 24.9 14.9

Ukraine 27.6 15.8

Europe 27.3 16.6

Adapted from Ferlay et al. [2]

732 Int J Colorectal Dis (2009) 24:731–740

Page 3: Colorectal screening in Europe

significant increase in the demand on cancer servicesthroughout 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 todevelop in this way [8], which provides an opportunity forscreening with the interception of the adenoma viapolypectomy at the time of colonoscopy with earlydetection resulting in improved outcomes with acceptablemorbidity.

Screening modalities

The use of mass screening with faecal occult blood testing(FOBT) has repeatedly been shown to cause a modestreduction in mortality from CRC [9–11] with longer-termfollow-up data [12–15], giving an overall reduction inmortality from CRC as 16% (fixed and random effectsmodels; RR, 0.84; CI, 0.78–0.90) with a shift in detectionto early stage Dukes' A cancers in the screened group,compared to the control group [15]. A summary of theFOBT trials is given in Table 3.

Case–control studies, which assume complete compli-ance, have shown that combining FOBT and flexiblesigmoidoscopy (FS), CRC mortality rates can be reducedby approximately 35% [16, 17]. However, it has beensuggested that utilising this strategy may miss up to 24% ofadvanced neoplasia (defined by the authors as a polyp withvillous features or the presence of high-grade dysplasia orinvasive cancer) [18].

Enthusiasts for colonoscopic screening [19] suggest thatFS examination, as a screening modality, is second bestbecause of the miss rate for neoplasia out of reach of theflexible sigmoidoscope and this has raised an argument forcolonoscopy to be considered as the sole screeninginvestigation [18, 20, 21]. Additionally, preliminary resultsfrom the Italian CRC screening programme reveal that 39%of screen-detected cancers are located proximal to thesplenic flexure [22], and this supports the observation of acontinued rightward-shift in colonic cancer distributionwhich has previously been demonstrated both in UnitedStates [23] and European populations [24] during the pastthree decades, lending further support to this argument.

In the future, newer technologies that expose the subjectto less risk may be championed as the favoured screeningtool: interest is growing in the use of computed tomo-graphic colonography (CTC) and a recent study of morethan 3,000 patients reported findings that support the use ofCTC as a primary screening test prior to the use of opticalcolonoscopy [25].

Colorectal cancer screening in Europe

Thousands of deaths could be prevented within Europewith the use of bowel cancer screening programmes but fewcountries have these in place and those that do acknowl-edge lower than ideal compliance rates.

There are wide discrepancies throughout Europe insurvival for CRC patients due to poor patient education,

Table 3 Summary of the FOBT trials

Minnesota, USA Funen, Denmark Gothenburg,Sweden

Nottingham, UK

Enrolment Randomised to screening orcontrol groups only afteragreeing to enter trial

Randomly selected from GP and population registers (Funensubjects only invited to further rounds of screening ifcompleted first round)

Numbers enrolled 46,551 61,993 1,393 150,251

Age (years) 50–80 45–75 60–64 45–74

Type of FOBT used HemOccult (rehydrated) HemOccult II(unrehydrated)

HemOccult II(rehydrated)

HemOccult(unrehydrated)

Screening interval (years) 1 or 2 (2 groups) 2 2 2

Follow-up interventions Colonoscopy Colonoscopy Sigmoidoscopyand DCBE

Colonoscopy

Dietary restrictions Yes Yes Yes No

No. of screening rounds Annual group, 11;biennial group, 6

9 1 6

Last reported follow-up (years) 18 17 15.5 18

Compliance with FOBT for first (%) 53.4 66.8 63 NR

Reduction in mortality (%) Ann, 33; bi, 21 18 16 15

DCBE double contrast barium enema, NR not reported

Int J Colorectal Dis (2009) 24:731–740 733

Page 4: Colorectal screening in Europe

late presentation of disease, lack of screening and insuffi-cient funding for health care. Despite the cost of treatmentof advanced stage cancer being approximately five timesgreater than for surgical treatment of an early screen-detected cancer [26], organised bowel cancer screeningprogrammes are not common in Europe. The currentstrategies for some European countries are set out below:

The UK National Health Service Bowel CancerScreening Programme

In 2004, the Secretary of State for Health announced thelaunch of the National Health Service Bowel CancerScreening Programme (NHS BCSP) for 2006. This was inacknowledgement of the government's commitment toreduce cancer deaths in those under the age of 75 by atleast 20% by 2010 [27] and in response to the NHS CancerPlan affirming the commitment to a national screeningprogramme, subject to effective evidence of the pilot [28].The programme is expected to be rolled out nationally by2009, with 14 centres operational by March 2007 utilising acentral budget of £10 million for 2006/2007 and £25million for 2007/2008.

The NHS BCSP uses biennial FOBTof 60- to 69-year-oldswith the offer of colonoscopy for those who test positively.The programme is arranged via five programme hubs aroundthe country with up to 20 local screening centres assigned toeach. A single hub will cover a population of about ten millionpeople. It will be the responsibility of each hub to send thescreenees the FOBT, to send the results to the patient and theirgeneral practitioner (GP) and to arrange a follow-up visit forthose with a positive test.

Each screening centre will serve a population of between500,000 and 2,000,000 people. Assuming an uptake of 60%and a positivity rate of 2%, based on the pilot study [29],this may result in an estimated 300 extra colonoscopies peryear, equating to one or two extra endoscopy lists per week.Outcomes and complications are being closely audited.

As of October 2007:

– 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– 3,349 colonoscopies– 1,523 (44%) polyps– 382 (11%) cancers detected

The agreed UK bowel screening programme is apragmatic solution applied to the current financial andservice restraints of the NHS that is expected to result in areduction in mortality of patients from CRC within the UK.

Following a promising initial analysis of the activity of theNHS BCSP across the country, the government has recentlyagreed to increase the age of inclusion into the programmeto 74 years by 2010.

The Italian bowel cancer screening programme

A national campaign for CRC screening was officiallylaunched in late 2005. The Ministry of Health has askedeach regional health authority to organise the programmefor their region providing specific extra funds for thispurpose. Each region is able to make specific choicesconcerning the screening modalities used (e.g. FS orFOBT).

To date, CRC screening programmes have beenlaunched in 11 out of the 21 Italian regions predominantlylocated 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 FOBTfollowed by total colonoscopy in FOBT-positive subjects.The Lecco province is the pilot province where the firstround of CRC screening has been completed.

The Lecco colorectal cancer screening programme

The programme has been organised in this pilot area (oneof the 11 provinces of Lombardy) according to the scheduleof conditions defined by regional health authorities. Itcommenced in February 2006 using FOBT every 2 years inthe target population followed by total colonoscopy inFOBT-positive individuals.

The target population for screening comprises 80,915men and women aged between 50 and 69 years resident inthe province. Criteria for exclusion are: history of colorectaladenoma or cancer, known inflammatory colonic diseaseand recent (within 3 years), well-documented completecolonoscopy.

For the period 2006–2008:

– 78, 083 invitations were sent out regionally– 36,693 returned, i.e. 49.6% compliance– 2,392 positive FOBT (6.5%)– 2,054 colonoscopies– 1,523 (44%) polyps– 382 (11%) cancers detected

The screenee receives a letter of invitation by thecommunity health care centre and the FOBT is distributedby pharmacists and GPs. In urban areas, subjects are invitedto bring back the FOBT to local pharmacies; however,rurally, Red Cross volunteers collect the test from thesubject. Once tested, individuals with a positive result are

734 Int J Colorectal Dis (2009) 24:731–740

Page 5: Colorectal screening in Europe

contacted by a nurse specialist in order to discuss arrange-ments for follow-up colonoscopy.

Specific colonoscopy lists are integrated within theexisting endoscopy service and screening colonoscopiesare usually scheduled within a maximum of 20 workingdays from the notification of FOBT positivity. Any furtherinvestigations or treatment needed are performed locallyand a quality assurance infrastructure has been specificallyset up to monitor colonoscopy performance.

The French bowel cancer screening programme

A national screening campaign was started in 2003 basedupon biennial FOBT for screening subjects aged between50 and 74 years using colonoscopy as the investigation ofchoice for those testing positive. Although currently, aguaiac-based FOBT test is used, a discussion is runningwithin the National Cancer Institute to switch to animmunological-based test in the near future.

Exclusion of subjects for the test include a history ofCRC or adenoma or other colonic disease requiring acolonoscopy, a first-degree relative affected with CRCbefore the age of 65 or two second-degree relatives affectedor a total colonoscopy within the past 5 years.

The screening is organised via a local specific structurewith precise financial and technical regulations. Thescreening process, from sending tests to collecting andreading the results, and procedures for the follow-up ofpositive cases are very well-defined and standardised.Contrasting with the UK, the GP is essential to the logisticsof the programme and responsible for the implementationand follow-up of the test result for the screenees.

By the end of 2006, 23 out of 90 districts wereparticipating, with an average 54% compliance of thispopulation. The number of districts increased by more than50% by the end of 2007, with 25 new districts starting theprogramme in December 2007, and a further 25 districts areexpected to start before summer 2008. Local and regionalmeetings have and are being arranged around the country toeducate and inform the population about the programme.

The results from four pilot districts (Côte-d'Or, Haut-Rhine, Ille-et-Vilaine and Saône-et-Loire) showed:

– 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 havea screening programme, issues have been recognised which

may give limitations to a successful programme such as thechoice of FOBT to use (e.g. guaiac or immunological) andthe best screening method (e.g. FOBT, colonoscopy, CTcolonography, video capsule, etc.). The ultimate goal is toachieve screening for more than 65% of the eligiblepopulation with a 90% uptake of colonoscopies for thosesubjects with a positive test.

Germany

In Germany, there are 71,000 new cases of CRC per yearand 27,000 deaths due to the disease. A National CancerPrevention Programme incorporating screening colono-scopy and FOBT has been established since 2002. Everysubject over the age of 55 years is offered colonoscopy witha second colonoscopy offered after 10 years if no neo-plasms are found and the screenee is below the age of 65 atthe first screening colonoscopy. Every subject over the ageof 50 years is offered an annual FOBT, with a biennial testafter the age of 55. This test is recommended for thosepatients who do not want to go undergo colonoscopy.

About 1.5 million colonoscopies were performed be-tween January 2003 and December 2005 with an uptake of8.8% for men and 10.2% for women. Including subjectsundergoing colonoscopy via private insurance companies,the total compliance is about 12%. This figure is acknowl-edged as being lower than ideal but it is hoped that around33% of the eligible population will accept colonoscopicscreening within the next 10 years with the recruitment offamily doctors educating patients about the benefits of theprogramme.

For 1,346,217 screening colonoscopies performed, ade-nomas were found in 18.9% of subjects and cancers in0.8%. Of those 3,073 patients with a screened cancer,46.8% had stage I disease, 22.6% stage II, 21.2% stage IIIand 9.4% stage IV. There has been a 10% reduction inmortality from CRC from approximately 30,000 in 2002 to27,000 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 inGermany, no data are available to correlate compliance ofcolonoscopy for those individuals who tested positively.

The Netherlands

Currently, there is no CRC screening programme in TheNetherlands. A study comparing guaiac-based FOBT(HemOccult) with an immunochemical test (OC-sensormu) is currently being undertaken at the Universities ofAmsterdam and Nijmegen (each centre with 10,000 sub-

Int J Colorectal Dis (2009) 24:731–740 735

Page 6: Colorectal screening in Europe

jects) encompassing 20,000 subjects aged between 50 and74 years. Those with a positive test will be followed upwith a colonoscopy.

Also, a comparative study is being undertaken at theUniversity of Rotterdam between the efficacy of sigmoid-oscopy and two different occult blood tests (iFOBT andGuiacFOBT), with a total of 15,000 subjects.

Additionally, sigmoidoscopy, colonoscopy and faecalDNA are being compared at the University of Maastricht,with 3,000 subjects in each arm of the study. The efficacyof using different faecal DNA tests is being conducted atthe Free University of Amsterdam.

The Ministry of Health is awaiting the results of theseongoing trails before recommending which programme tofollow.

Spain

There is currently no national screening programme inSpain. That there are 17 different health care regions with amixture of public and private health care systems utilisedby the population are seen as potential barriers to therealisation of effective screening. However, individualhealth care regions are addressing the issue although themain focus seems to be on “at-risk groups”.

Catalonia has completed a pilot screening programmewith the aim of extending a screening programme to thewhole of the region by 2010.

Valencia has a screening programme in progress with apopulation of 113,447 encompassing three health regions,and in April 2007, Castellón launched a programme for theearly detection of CRC for 16,390 subjects between 50 and70 years old.

In 2004, the Canary Islands created a medical unit forthe prevention of CRC (Hospital Universitario de Canarias)incorporating a screening programme for the region:

– Phase I: screening with FOBT in 3,000 asymptomaticpeople over the age of 50 years,

– Phase II: screening extended to relatives of patientswith CRC.

A summary of the programmes described above is givenin Table 4.

Bowel preparation

One of the most important barriers to a widespread CRCprevention screening programme is the suitability of the testto the population it is being applied to. Thus, FOBT andcolonoscopy need to be acceptable to this population, ascompliance has been cited as the most important determi-

nant of effectiveness for models of bowel cancer screening[30]. It is also recognised that those individuals whoperceive screening procedures to be embarrassing, uncom-fortable or inconvenient are less likely to participate [31–33].

In a questionnaire study seeking to identify reasons forparticipant reluctance to undergo screening colonoscopy,comprising those respondents never screened (n=126) andpreviously screened (n=132), the most common reasongiven by both groups was unwillingness to take bowelpreparation (66% and 57%, respectively) [34]; the secondmost preferred solution expressed by both groups ofrespondents was for small volume bowel preparation. Thus,bowel preparation has implications for compliance ofscreenees and, therefore, for the success of any screeningprogramme.

The most common adverse symptoms from taking bowelpreparation are nausea (and vomiting to a lesser degree),abdominal bloating and abdominal pain (more commonwith hyperosmolar solutions, e.g. sodium picosulphate) anda recent review [35] has highlighted the potential risks oftaking bowel preparation, which include death in the mostextreme cases. The majority of risk is primarily related todehydration and electrolyte fluxes, especially in the elderlypatients with co-morbidity (e.g. cardiac failure and renalfailure) and those on medication that may influence fluidbalance or electrolytes [35]. To reduce the risk ofcomplications and to increase patient compliance, theauthors advocate tailoring the preparation to the patient,optimising patient education and promoting adequatehydration both before and after the examination as beingof paramount importance.

In a meta-analysis comparing sodium phosphate andpolyethylene glycol, the former gave improved bowelpreparation and was better tolerated by patients [36]; thisis in accordance with other studies [34] relating to theinverse relationship between volume of bowel preparationand patient preference/compliance, as polyethylene glycolis needed to be taken in larger volumes. However, a laterstudy found that a polyethylene glycol preparation based onthe GoLytely formulation (Klean-Prep) achieved bettercolonic visualisation than a sulphate-free polyethyleneglycol preparation based on the NuLytely formulation(Endofalk) or a sodium phosphate preparation (Fleet) [37].

More recently, a new formulation of polyethylene glycolplus ascorbic acid has been shown to be as effective asstandard polyethylene glycol, with the advantage that it canbe taken in smaller volumes, 2 L compared with 4 L forstandard polyethylene glycol preparation, which mayimprove patient acceptability and, therefore, compliance[38].

Poor bowel preparation is associated with increased missrate for polyps [39, 40], greater procedural risk [41],

736 Int J Colorectal Dis (2009) 24:731–740

Page 7: Colorectal screening in Europe

Tab

le4

Sum

maryof

bowel

cancer

screeningin

Europ

e

UK

Germany

France

Spain

The

Netherlands

Italy

Current

natio

nalscreening

prog

ramme

Yes,since20

06Yes,since20

02Yes,since20

03No

No

Yes,since20

05

Percentageof

coun

try

Aim

for10

0%by

2009

All

Aim

for10

0%by

end20

08N/A

N/A

Aim

for10

0%by

end20

09

Ifno

prog

ramme,

when

planned?

N/A

N/A

N/A

Currently

unkn

own

Plann

edafterresults

oftrialsto

investigate

optim

alscreeningtest

N/A

Screening

agerang

e(years)

60–6

9Over55

50–7

4N/A

Likely50

andabov

e50

–69

Screening

frequency

2yearly

10yearly

2yearly

N/A

N/A

2yearly

Screening

mod

ality

FOBT-gu

aiac

Colon

oscopy

FOBT-gu

aiac

N/A

N/A

Depends

onregion

:FOBT-im

mun

o(N

BPiedm

ontusingFS)

Com

pliance(%

)52

forFOBT

12forcolono

scop

y(dataun

available

forFOBT)

54forFOBT

N/A

N/A

From

Lecco

prov

ince

(pilo

tprov

ince),49

.6forFOBT

Percentageof

patientswith

patholog

yaftercolono

scop

y,e.g.

adenom

a,carcinom

a

CRC,11;

adenom

as,44

CRC,0.8;

adenom

as,18

.9CRC,9.6;

adenom

as,33

N/A

N/A

CRC,4;

adenom

as,48

Caecalintubatio

nrate

(%)

9295

96N/A

N/A

97

Perforatio

nrate

(%)

0.5

0.02

0.05

N/A

N/A

0.05

Bleedingcomplications

(%)

Unavailableat

timeof

publication

0.18

Unavailable

attim

eof

publication

N/A

N/A

0.7

Int J Colorectal Dis (2009) 24:731–740 737

Page 8: Colorectal screening in Europe

increased cost [41], longer intubation times [42] andincomplete colonoscopy in up to 20% of examinations[43]. If any of these factors contribute to an unfavourableexperience for the screenee/patient, it will undoubtedlyhave a negative influence on the likelihood of the subjectreturning for subsequent examinations if required.

Discussion

Bowel cancer screening programmes offer an excellentopportunity to beneficially alter the survival of patients withpre-cancerous polyps or early cancers, but a number ofconditions need to be applied before this can be realised.The first and most important of these is that the populationto which the programme is being applied need to besuitably receptive and compliant. Secondly, the bowelneeds to be optimally clean and achieved by a preparationthat is safe with a limited side effect profile. Thirdly, thecolonoscopy should be performed by an experiencedendoscopist trained to a standard to provide an examinationwhich is safe, comfortable and can identify and safely treatany lesions encountered.

The compliance of the programmes currently in Europereport rates of between 40% and 54%. As a comparator, theUK National Breast Cancer Screening Programme achieved acompliance rate of 75.5% of the eligible screening populationby the end of March 2006 and it is hoped that eventuallysimilar levels will be achieved for bowel cancer screening.

The reasons given for patient non-compliance in bowelscreening programmes are multiple and include: inconve-nience; family or work conflicts; lack of interest; theabsence of symptoms of bowel disease; embarrassmentand worries about the test being unpleasant or painful [33].Clearly, the act of using a FOBT may be perceived byscreenees to be embarrassing enough especially in theknowledge that a positive test will result in a colonoscopy,which again is potentially embarrassing and may beuncomfortable in some instances. Additionally, they willbe required to take bowel preparation for the endoscopy.However, the benefit to that individual if an early neoplasiacan be treated either endoscopically or with a “curative”operation would be considerable. Only by health careprofessionals understanding and overcoming these reasonsfor non-participation can compliance improve. Key to thisis patient education via well-informed primary care physi-cians who are likely to be the first medical contact for thescreenee, as endorsement by health care professionals hasbeen shown to improve compliance [33, 44, 45]. Moreover,lack of a strong recommendation by a physician has beencited by patients as a reason for not undergoing screening[46], and because most people visit their doctor infrequent-ly, the opportunity to discuss health prevention issues on

these occasions has been recognised to be important [47].In mainland Europe, the GP will have an increasingresponsibility to organise and enrol his/her patients intobowel cancer screening programmes.

Some patients would be positively influenced byinformation given by colon cancer survivors [34], includingcelebrities, which is a route of recruitment that might beexplored in the future. Additionally, a recommendationfrom a relative, friend or colleague who has had a positiveexperience from bowel cancer screening will also serve toincrease education and awareness and, therefore, hopefullycompliance.

It is also important that screenees receive a personalinvitation (“active individual invitation”) rather than a“general call-up”. And perhaps non-responders who fail toreply after being sent a postal reminder or second FOBTmight receive a visit from a health care worker to enquire asto the reasons for that individuals reluctance to participateand at the same time address any worries, concerns orquestions the potential screenee might have about thescreening process. This strategy of course raises fundingissues however.

For those screenees who do return a FOBT, it must beprocessed in a prompt manner including informing thesubject of the result. For those who test positively, promptcontact from specifically trained health professionals withinthe screening team is needed to counsel the screenee aboutthe practicalities of colonoscopy and the outcomes that maybe encountered in terms of pathology and the likelyincreased chance of picking up early disease.

The importance of acceptable and safe bowel preparationhas already been described, but to reduce intubation times,improve the pick-up rate of pathology and give effectivecleaning, such that the need for a repeated examination isobviated, the choice of bowel preparation perhaps requiresfurther consideration, tailored to the patient, using the minimalvolume of preparation to achieve a “clean” colorectum. Thisagain has implications for patient compliance.

Finally, continued training of endoscopists with closelyaudited performance and complication rates are paramountto provide accurate and comfortable colonoscopy especiallyif screenees are to return at the next round of screening.

Whichever screening methods are chosen acrossEurope and whether a common European approach tobowel cancer screening will emerge remains to be seen.However, the costs of such programmes will bebalanced against the benefits of screening which includea reduction in the mortality from CRC, the detection ofearly cancers requiring less invasive surgery, lesserhospital in-patient admission days and the use of lessadjuvant and palliative treatments.

Currently, the programmes for bowel cancer screening inEurope are different, where they exist, but the difficulties

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are similar: patient compliance is the core of screening andonly when this has been maximised can bowel cancerscreening realise its full potential: which could be thevirtual elimination of sporadic CRC.

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