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ORIGINAL CONTRIBUTIONS nature publishing group188 C

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Screening in Italy: Predictors of Patients ’ Participation Carlo Senore , MD 1 , Paola Armaroli , MD 1 , Marco Silvani , PhD 1 , Bruno Andreoni , MD 2 , Luigi Bisanti , MD 3 , Luisa Marai , RN 3 , Guido Castiglione , MD 4 , Grazia Grazzini , MD 4 , Serena Taddei , RN 4 , Stefano Gasperoni , MD 5 , Orietta Giuliani , BSc 5 , Giuseppe Malfi tana , MD 6 , Anna Marutti , RN 7 , Giovanna Genta , RN 7 and Nereo Segnan , MD 1

OBJECTIVES: The objective of this study was to study predictors of patients ’ participation in colorectal cancer (CRC) screening.

METHODS: Men and women, aged 55 – 64 years, were randomized to the following: (i) biennial fecal occult blood test (FOBT) delivered by mail ( n = 2,266); (ii) FOBT delivered by a general practitioner (GP) / screening facility ( n = 5,893); (iii) “ once-only ” sigmoidoscopy (FS) ( n = 3,650); (iv) FS followed by FOBT for screenees with negative FS ( n = 10,867); and (v) patient ’ s choice between FS and FOBT ( n = 3,579). A stratifi ed (by screening arm) random sample of attenders and nonattenders was contacted by trained interviewers 4 months after the initial invitation. Subjects giving their consent were administered a questionnaire (available online) investigating perceptions of individual CRC risk, attitudes toward prevention, adoption of health protective behaviors, and reasons for attendance / nonattendance. Adjusted prevalence odds ratios (ORs) were computed by multivariable logistic regression.

RESULTS: The response rate was 71.9 % (701 of 975) among nonattenders and 88.9 % (773 of 870) among attenders. Adjusting for screening arm, center, gender, age, and education, participation was signifi cantly higher among people who consulted their GP before undergoing screening (OR: 4.24; 95 % confi dence interval (CI): 3.11 – 5.78), who mentioned one fi rst-degree relative with CRC (OR: 3.62; 95 % CI: 2.02 – 6.49), who reported regular physical activity (OR: 1.85; 95 % CI: 1.33 – 2.55), and who read the mailed information (letter only: OR: 1.85; 95 % CI: 1.23 – 2.78; letter + leafl et: OR: 3.18; 95 % CI: 2.12 – 4.76). People who considered screening to be ineffective (OR: 0.12; 95 % CI: 0.08 – 0.19), those who considered it to be effective but reported even moderate levels of anxiety (OR: 0.32; 95 % CI: 0.23 – 0.45), and those who mentioned previous knowledge of CRC screening tests were less likely to accept the invitation (OR: 0.49; 95 % CI: 0.34 – 0.70).

CONCLUSIONS: Adoption of health protective behaviors is associated with a higher attendance rate, whereas anxiety represents a strong barrier, even among people who deemed screening to be effective. Increasing the proportion of people who consult their GP when making a decision regarding screening might enhance participation.

SUPPLEMENTARY MATERIAL is linked to the online version of the paper at http://www.nature.com/ajg

Am J Gastroenterol 2010; 105:188–198; doi:10.1038/ajg.2009.583; published online 13 October 2009

1 Centro Prevenzione Oncologica Regione Piemonte and Azienda Ospedaliero-Universitaria S. Giovanni Battista di Torino , Turin , Italy ; 2 Surgery Unit II, Istituto Europeo di Oncologia , Milan , Italy ; 3 Epidemiology Unit, ASL “ Citta ’ di Milano, ” Milan , Italy ; 4 Gastroenterology Unit, CSPO , Florence , Italy ; 5 Infermi Hospital, AUSL Rimini , Rimini , Italy ; 6 Gastroenterology Unit, Infermi Hospital, ASL 12 , Biella , Italy ; 7 Fondo E Tempia , Biella , Italy . Correspondence: Carlo Senore, MD , Centro Prevenzione Oncologica Regione Piemonte and Azienda, Ospedaliero-Universitaria S. Giovanni Battista di Torino , V. San Francesco da Paola 31 , Turin 10123 , Italy . E-mail: carlo.senore@cpo.it Received 25 November 2008; accepted 5 September 2009

© 2010 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

189 Predictors of Participation in CRC Screening

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INTRODUCTION In spite of strong evidence (1 – 8) supporting the eff ectiveness

of available screening strategies for colorectal cancer (CRC)

and of a general consensus of published guidelines recom-

mending the screening of average-risk individuals over the

age of 50 years (9) , the rates of screening remain low (10 – 12) .

Th e compliance rates observed in trials evaluating the effi -

cacy of CRC screening strategies showed a wide variability,

even when the tests proposed and the target populations were

similar (13 – 17) . Th e fi ndings of studies analyzing predictors of

screening attendance support the proposed models of behav-

ioral change, suggesting that an individual ’ s decision regard-

ing whether to undergo screening is dependent on a complex

array of demographic, psychosocial, normative, and organiza-

tional factors. Higher participation rates were observed among

people with higher education and income, personal or family

history of CRC, and among those adopting health protective

behaviors (10,18 – 20) . Practical constraints, cost of the test, lack

of interest, absence of current health problems or CRC symp-

toms, and lack of a physician ’ s recommendation have been

indicated as major barriers to participation (18 – 21) . However,

given diff erent research designs and target populations and dif-

ferent health-care systems, it is diffi cult to interpret the rela-

tive weight of these determinants, as well as their potential role

in diff erent contexts. Furthermore, each available test requires

the adoption of specifi c procedures and shows a diff erent risk

profi le. Th ese factors may aff ect an individual ’ s decision proc-

ess, in relation to his values, beliefs, and attitudes, and may also

aff ect how the person perceives the testing process as an incon-

venience to everyday life. However, direct comparisons of the

predictors of participation with diff erent strategies in the same

target population are lacking, as available studies generally con-

sidered a single test in one setting. Similarly, obtaining more

information regarding the predictors of sustained compliance

with fecal occult blood test (FOBT) screening would be helpful,

as published data from FOBT trials (22,23) indicated that the

response rate tends to decrease over subsequent rounds.

Th e aim of this study was to characterize factors infl uenc-

ing participation in CRC screening among average-risk people

enrolled in a multicenter randomized trial in Italy (14) com-

paring diff erent strategies. As people who were enrolled in the

FOBT arms were regularly invited every 2 years, we could also

study factors predicting regular attendance to screening.

METHODS Th e aim of our population-based, multicenter, randomized,

controlled trial involving fi ve Italian centers (14) was to com-

pare acceptability, participation, detection rate, and costs of

fi ve protocols based on biennial FOBT and sigmoidoscopy (FS)

among average-risk people aged 55 – 64 years. A random sample

of men and women drawn from rosters of general practition-

ers (GPs) or from population registers were randomly assigned

to the following: (i) FOBT delivered by mail ( n = 2,266);

(ii) FOBT delivered by GP or screening facility ( n = 5,893);

(iii) “ once-only ” FS ( n = 3,650); (iv) FS followed by FOBT for

screenees with negative FS ( n = 10,867); and (v) individual ’ s

choice between FS or FOBT ( n = 3,579). Th e randomization

and study protocol have been described in detail elsewhere (14) .

Briefl y, GPs were asked to exclude noneligible subjects and to sign

the invitation letters and mail reminders. Eligible subjects were

mailed a personal letter signed by their GP (or by the local study

coordinator, if the GP refused to collaborate), which included a

leafl et that briefl y described the screening procedure and its pos-

sible side eff ects. Subjects allocated to the FS arms were off ered a

prefi xed test date and were asked to call the screening center to

confi rm, modify, or cancel their appointment. Th ose who agreed

to undergo FS were advised to visit their GP, or the screening

center, to obtain enema for bowel preparation. Subjects allocated

to FOBT arms received a letter that included a paper slide for

stool smearing and instructions for performing the test, or that

invited the patient to contact his GP or the screening center to get

an FOBT kit and instructions for performing the test. We used

an immunochemical test performed on a single sample without

dietary restrictions. A reminder letter was mailed to all subjects

who did not respond to the initial invitation within 45 days.

To assess the determinants of participation in screening, a

random, stratifi ed (by screening arm) sample of attenders and

nonattenders was taken in each center by the local coordinat-

ing unit, ~ 4 months aft er the initial invitation. Subjects were

considered attenders if they underwent the proposed test aft er

either the initial invitation or the mail reminder, whereas those

who did not respond to these two letters were classifi ed as non-

attenders. Subjects who phoned to decline the invitation men-

tioning some condition that was included among the exclusion

criteria, but not those who called to refuse screening, were

excluded from sampling.

All subjects included in the sample were contacted by trained

interviewers who knew the subject ’ s randomization group,

attendance status, and date of invitation (and the date and

test result for attenders). Subjects who did not respond to fi ve

telephone calls made during diff erent times of the day (at least

one call between 7 and 8 PM ) and on diff erent days during the

week were considered untraceable. When the interview could

not be conducted because the subject was temporarily unavail-

able, the interviewer fi xed a date for a second call. Aft er three

missed dates, the subject was considered as a refuser.

Subjects giving their consent to a telephone interview were

administered a questionnaire investigating factors infl uencing

attendance. We classifi ed predictors according to the model

proposed by Green (24) which described behavioral change

as the result of the interplay of PREDISPOSING (provide the

rationale or motivation for the behavior), ENABLING (allow a

motivation or environmental policy to be realized), and REIN-

FORCING factors (provide the continuing reward or incen-

tive for the persistence or repetition of the behavior). Beliefs

regarding the benefi ts of screening, attitude to having regular

medical controls (completely reassured, moderately reassured,

moderately worried, severely worried), perception of CRC

risk, adoption of health protective behaviors (physical activity,

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smoking habits), self-reported health status (good, fair, poor,

very poor), together with sociodemographic factors (gender,

age, education, occupation), were the predisposing factors that

were assessed in this study. Enabling factors included utilization

of media (newspapers, TV, internet) and information conveyed

with the invitation (letter and information leafl et). Reinforc-

ing factors included medical advice, knowing a close relative

or friend with CRC, and practice of previous examinations for

early detection of CRC or engaging in other preventive prac-

tices (mammography / Pap test for women, prostate-specifi c

antigen (PSA) testing for men).

Both attenders and nonattenders were asked to indicate the

main reason for accepting or refusing screening. Th ey were

then asked directly whether a number of factors identifi ed from

previous studies had infl uenced their decision making. Attend-

ers were also asked to rate their level of anxiety before and aft er

screening, and their impressions regarding the test. Nonattend-

ers were asked to indicate factors that might possibly induce

them to undergo screening in the future and to answer ques-

tions investigating their knowledge of aspects of the screening

process presented in the leafl et (duration of FS, probability of

FOBT positive result, and expected pain at FS).

Statistical analysis We planned to interview ~ 1,400 people with a 1:1 ratio of

attenders and nonattenders in each group. Assuming a propor-

tion of nonrespondents (or not traceable) equal to 20 % among

participants and 30 % among nonparticipants, we had to sam-

ple ~ 875 attenders (245 in Turin and 158 in each of the remain-

ing centers) and 1,000 nonattenders (270 in Turin and 182 in

each of the remaining centers). Given the observed response

rate, the choice of maintaining a 1:1 ratio between attenders

and nonattenders was more effi cient compared with the adop-

tion of proportional sampling, which would have resulted in

a 1:2 ratio. On the basis of the expected (14,18,19,25) distribu-

tion of the determinants of interest, ranging from 9 % (positive

family history) to 45 % (proportion of people reading the leafl et),

and assuming a 5 % (two-tailed) level of statistical signifi cance,

the planned size would give 80 % power to detect absolute diff er-

ences ranging between 5 and 8 % in their observed distribution

between attenders and nonattenders. On the basis of the esti-

mated proportion of regular attenders to FOBT screening, the

size of our sample of attenders would give 80 % power to detect

absolute diff erences of about 10 – 12 % in the distribution of the

same potential predictors between regular and irregular attend-

ers, assuming a proportion of people attending three consecutive

invitations (regular attenders) equal to 65 % .

Adjusted prevalence odds ratios (ORs) were computed by mul-

tivariable logistic regression. Separate models were also fi tted for

gender and for each screening arm: FOBT (groups 1 – 2), choice

(group 5), and FS (groups 3 – 4). All statistical tests were two-

sided and were considered statistically signifi cant at P < 0.05. We

calculated the fraction attributable to the strongest predictors in

the multivariable model using the method proposed by Green-

land and Drescher (26) . Th ese estimates can be interpreted as

the proportion of nonattenders who failed or of attenders who

agreed to attend screening because of that specifi c predictor.

RESULTS Th e response rate to the questionnaire ( Table 1 ) was 71.9 %

(701 out of 975) among nonattenders and 88.9 % (773 out of

870) among attenders. Th ese rates were similar across screen-

ing arms; the proportion of nonresponders was higher among

men than among women (OR: 1.53; 95 % confi dence interval

(95 % CI): 1.21 – 1.93).

Although the association between higher educational level

or knowledge of personal risk of CRC and propensity for par-

ticipation was no longer signifi cant in the multivariable model,

the role of the remaining predictors identifi ed in the univari-

ate analysis was maintained aft er adjusting for the eff ect of

the other determinants included in the model ( Table 2 ).

Adjusting for screening center and arm, participation was sig-

nifi cantly increased among patients who consulted their GP

before undergoing the test (OR: 4.24; 95 % CI: 3.11 – 5.78), who

mentioned one fi rst-degree relative with CRC (OR: 3.62; 95 %

CI: 2.02 – 6.49), or who reported regular (at least once a month)

physical activity (OR: 1.85; 95 % CI: 1.33 – 2.55). People who con-

sidered screening to be ineff ective (OR: 0.12; 95 % CI: 0.08 – 0.19),

or those who considered it to be eff ective but reported even

moderate levels of anxiety associated with repetition at regular

intervals of tests for early diagnosis of cancer (OR: 0.32; 95 %

CI: 0.23 – 0.45) showed a marked decrease in attendance, com-

pared with those who considered screening to be eff ective and

reported no anxiety. Lower attendance was also observed among

smokers (OR: 0.68; 95 % CI: 0.47 – 0.98) and among people rating

their health as either fair or poor (OR: 0.71; 95 % CI: 0.52 – 0.96).

Employed subjects were less likely to complete screening com-

pared with housewives or retired subjects (OR: 0.78; 95 % CI:

0.66 – 0.93). Compared with people who had read neither the

invitation letter nor the leafl et, the odds of attending screening

were about twice as high (OR: 1.85; 95 % CI: 1.23 – 2.78) among

people who reported having read the letter and more than three

times higher (OR: 3.18; 95 % CI: 2.12 – 4.76) among those who

mentioned having read both the letter and the leafl et. People

who reported any previous experience or knowledge of CRC

screening tests were less likely to accept the current invitation

(OR: 0.49; 95 % CI: 0.34 – 0.70).

Th e estimated fraction that can be attributed to the choice

to seek GP ’ s advice accounts for 36 % of the overall attendance,

whereas the fraction that can be attributed to family history is

8 % ; similarly, anxiety with regard to early-detection tests and

belief that screening is ineff ective account for 20 and 19 % of

nonresponders, respectively.

Predictors of participation by gender or screening strategy Although screening-related anxiety, belief that screening is

not eff ective, previous CRC screening experience, perceived

health, working status, and physician ’ s advice maintained their

role across gender and screening strategies, the infl uence of

© 2010 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

191 Predictors of Participation in CRC Screening

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attitudes toward prevention and awareness of CRC risk showed

wide variations.

Among women, who were also more likely to attend if they had

a fi rst-degree relative with CRC (OR: 4.61; 95 % CI: 2.09 – 10.13),

participation was associated with regular screening using a

Pap test (OR: 2.32; 95 % CI: 0.97 – 5.60) or mammography (OR:

3.73; 95 % CI: 1.15 – 12.12), but not with the adoption of other

health protective behaviors (smoking habit or regular physical

activity). Among men, a health-oriented lifestyle was instead

more infl uential, with a strong positive eff ect of regular physi-

cal activity (OR: 2.33; 95 % CI: 1.32 – 4.13) and a negative eff ect

of smoking (OR: 0.58; 95 % CI: 0.32 – 1.05), whereas practice of

PSA screening did not show any eff ect.

In the FS arms, the role of factors related to preventive health

orientation (i.e., engaging in regular physical activity) or per-

ceived health status was no longer signifi cant. Perceived risk

seemed particularly infl uential, as subjects who were able to

indicate a fi gure for their estimated individual risk of CRC

over the next 10 years were more likely to attend (1 – 9 % OR:

2.42; 95 % CI: 1.06 – 5.55; ≥ 10 % OR: 2.64; 95 % CI: 1.13 – 6.16).

People who accepted the invitation to choose between FS and

FOBT were more likely to report regular physical activity (OR:

3.24; 95 % CI: 1.31 – 7.98), were less likely to smoke (smokers

OR: 0.37; 95 % CI: 0.13 – 1.05), and were better educated (high

school / university degree — OR: 3.86; 95 % CI: 1.28 – 11.65). Th e

involvement of GP seemed particularly infl uential in this group

(OR: 13.07; 95 % CI: 5.27 – 32.42).

Participants Th e decision to undergo screening seemed mainly driven by

positive beliefs (it is useful to undergo preventive tests) and

attitudes (feeling reassured by engaging in preventive con-

trols to reduce CRC risk) with regard to prevention ( Table 3 ),

endorsed, respectively, by 48.9 and 11.1 % of screenees as the

main reasons for attendance. Among people invited for FS, the

off er of a prefi xed appointment was mentioned by 8.6 % as the

main reason for attendance. Furthermore, convenience of the

screening facility and the fact that screening did not entail any

cost were mentioned as additional reasons for attendance by

14.0 and 19.3 % of screenees.

Th e proportion of participants who reported moderate or

severe anxiety before the test was higher among subjects attend-

ing FS (22.7 % ) than among those undergoing FOBT (15.4 % ;

OR: 1.62; 95 % CI: 1.05 – 2.49), but overall, ~ 90 % of those report-

ing high pretesting anxiety (FS: 88.2 % ; FOBT: 89.6 % ) reported

feeling reassured aft er completion of the test. Similarly, although

the proportion of people who stated they would have preferred

to undergo a diff erent test was 2.6 % among attenders to FOBT

and 10.5 % among those who underwent FS, 93.7 % of FOBT

and 93.3 % of FS attenders would advice a friend or relative to

undergo the same test, if invited.

Among people who were off ered a choice between the two

tests, the preference for FOBT was justifi ed on the basis of the

fact that the test was simple (23.5 % ) and noninvasive (44.7 % ),

whereas FS was preferred by those who valued the accuracy of

the test (48.6 % ) or by those were advised by their GP (22.2 % ).

Nonparticipants Not having any current health problem or symptoms of CRC, as

well as anxiety with regard to the possibility of being diagnosed

with CRC aft er the examination, together represented the most

important determinants of the decision to decline the invita-

tion ( Table 4 ). Being worried about pain, discomfort, or injury

associated with the examination was mentioned as the most

infl uential determinant of their decision by 23.3 % of those who

refused an invitation for FS, compared with 7.6 % of those who

refused FOBT (OR: 3.68; 95 % CI: 2.13 – 6.43). Organizational

barriers such as lack of time due to family or work constraints,

or being too busy or out of town, were mentioned as the main

reasons for declining the invitation by 18.0 % (126 out of 701) of

nonattenders. However, inconvenience of time or of the loca-

tion of the screening facility and the amount of time required

to complete the screening procedures were mentioned only by

1.0 % of refusers as the main reason for nonparticipation and

by 5.9 and 9.1 % , respectively, as additional reasons. Being ill

at the time of invitation was mentioned as the justifi cation for

declining screening by 18.9 % of nonparticipants who rated

their health as fair or poor and by 8.3 % of those reporting a

good health status (OR: 2.58; 95 % CI: 1.56 – 4.27).

Compared with noncompliers to FS who did not read

the leafl et mailed together with the invitation, those who

reported having read it were more likely to indicate the cor-

rect duration of an FS (OR: 1.86; 95 % CI: 1.06 – 3.26), whereas

no diff erence could be observed in the beliefs regarding the

association of pain with FS. Onset of CRC-related symptoms

ranked fi rst (62.9 % , 441 out of 701) among factors that might

Table 1 . Response rate stratifi ed for gender and age

Women Men

55 – 59 60 – 64 55 – 59 60 – 64

Attenders

( % ) Nonattenders

( % ) Attenders

( % ) Nonattenders

( % ) Attenders

( % ) Nonattenders

( % ) Attenders

( % ) Nonattenders

( % )

Responders 190 (92.23) 160 (74.77) 238 (90.15) 219 (76.31) 138 (85.19) 146 (65.47) 207 (86.97) 176 (70.12)

Nonresponders 16 (7.77) 54 (25.23) 26 (9.85) 68 (23.69) 24 (14.81) 77 (34.53) 31 (13.03) 75 (29.88)

Total 206 214 264 287 162 223 238 251

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Table 2 . Factors associated with participation in CRC screening

Factor associated with participation in CRC screening n Univariate Multivariable

OR 95 % CI OR 95 % CI

Gender

Women 807 1 1

Men 667 0.95 0.77 – 1.17 0.95 0.70 – 1.28

Age (years)

55 – 59 634 1 1

60 – 64 840 1.05 0.85 – 1.30 1.07 0.81 – 1.42

Education

Primary school 638 1 1

Secondary school 386 1.54 1.19 – 1.98 1.11 0.78 – 1.60

≥ High school 413 1.30 1.01 – 1.67 1.10 0.55 – 1.63

Knowledge of personal risk

Risk not known 1093 1 1

Risk 1 – 9 % 142 1.46 1.02 – 2.08 1.35 0.84 – 2.16

Risk >9 % 173 1.84 1.32 – 2.57 1.49 0.94 – 2.36

Family history

No history of CRC 881 1 1

First-degree relative with CRC

117 2.69 1.76 – 4.12 3.62 2.02 – 6.49

Friend with CRC 441 1.39 1.10 – 1.74 1.24 0.92 – 1.68

Physical activity

No physical activity 412 1 1

At least once a month 1029 1.88 1.48 – 2.38 1.85 1.33 – 2.55

Smoking habits

Never 691 1 1

Current smoker 312 0.56 0.43 – 0.73 0.68 0.47 – 0.98

Former smoker 426 0.91 0.72 – 1.17 0.75 0.53 – 1.05

Screening attitude

Believes screening is effective – – no anxiety

931 1 1

Believes screening is effective — anxiety

321 0.30 0.23 – 0.40 0.32 0.23 – 0.45

Believes screening is ineffective

196 0.10 0.07 – 0.15 0.12 0.08 – 0.19

GP’s advice

Did not seek GP counseling

922 1 1

Sought GP counseling

473 4.49 3.47 – 5.82 4.24 3.11 – 5.78

Health

Good health status 1039 1 1

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193 Predictors of Participation in CRC Screening

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convince noncompliers to undergo the proposed test in the

future, followed by physician ’ s advice (36.1 % ).

Factors associated with persistent compliance Th e proportion of regular attenders (in three consecutive screen-

ing rounds) in the FOBT arms was 63.7 % . Out of 303 attend-

ers allocated to the FOBT arms who were interviewed aft er the

fi rst invitation, 170 (56.1 % ) also attended the second and third

rounds. Knowing someone with CRC (fi rst-degree relative — OR:

2.59; 95 % CI: 1.09 – 6.15; friend — OR: 1.79; 95 % CI: 1.02 – 3.12)

and previous screening experience (OR: 1.92; 95 % CI: 1.05 – 3.53)

emerged as predictors of regular screening attendance, whereas

people aged 60 – 64 years at the time of fi rst screening (OR: 0.55;

95 % CI: 0.32 – 0.94) as well as those who were employed (OR: 0.69;

95 % CI: 0.49 – 0.98) were less likely to regularly repeat FOBT.

The infl uence of communication tools on attitudes toward screening People who read the letter (OR: 1.58; 95 % CI: 1.07 – 2.33) or the

letter and the leafl et (OR: 2.52; 95 % CI: 1.72 – 3.67) were more

likely to report having sought GP ’ s advice, which was instead

sought less frequently by smokers (OR: 0.70; 95 % CI: 0.50 –

0.97), by people with a high-school degree (OR: 0.71; 95 % CI:

0.51 – 0.98), and by those who considered screening ineff ective

(OR: 0.49; 95 % CI: 0.33 – 0.75). Compared with people who

attended primary school only, those with a higher educational

level were more likely to report having read the leafl et (inter-

mediate degree: OR: 2.23; 95 % CI: 1.56 – 3.18; ≥ high-school

degree: OR: 2.13; 95 % CI: 1.46 – 3.13).

Adjusting by gender, arm, and screening center ( Table 5 ),

people who read the leafl et (OR: 0.42; 95 % CI: 0.26 – 0.70) or

consulted their GP (OR: 0.51; 95 % CI: 0.33 – 0.77) were less likely

to consider screening ineff ective, whereas the opposite trend

could be observed for those who did not usually read newspa-

pers (OR: 1.81; 95 % CI: 1.20 – 2.72). Similarly, anxiety regarding

screening was more frequent among subjects who did not read

newspapers regularly (OR: 1.77; 95 % CI: 1.27 – 2.47), whereas it

was reduced among those who read the leafl et (OR: 0.50; 95 %

CI: 0.34 – 0.75); consulting the GP; however, did not show any

eff ect on anxiety levels.

DISCUSSION We studied the determinants of participation in an average-

risk population, targeted for enrolment in a trial compar-

ing diff erent CRC screening protocols, designed as the pilot

phase of an organized mass screening program. Such a context

off ered the opportunity to assess the role of factors associ-

ated with the decision to undergo specifi c screening protocols

among subjects with the same sociodemographic and cultural

background. Screening was off ered free of charge to all eligible

people, enrolled through a personal invitation letter.

Table 2 . Continued

Factor associated with participation in CRC screening n Univariate Multivariable

OR 95 % CI OR 95 % CI

Fair / poor health status

408 0.81 0.64 – 1.02 0.71 0.52 – 0.96

Employment status

Housewife / retired 1105 1 1

Employed 369 0.61 0.48 – 0.68 0.78 0.66 – 0.93

Source of information

Regularly reads daily newspaper

1021 1 1

Does not read newspaper

421 0.61 0.48 – 0.77 0.75 0.54 – 1.04

Reading information material

Did not read the letter or the leafl et

306 1 1

Did read the letter 476 2.45 1.81 – 3.32 1.85 1.23 – 2.78

Did read the letter and the leafl et

647 4.12 3.08 – 5 – 51 3.18 2.12 – 4.76

Knowledge of CRC preventive test

Does not know the test 296 1 1

Does know the test 1174 0.82 0.63 – 1.07 0.49 0.34 – 0.70

CI, confi dence interval; CRC, colorectal cancer; GP, general practitioner; OR, odds ratio.

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involvement in health protective behaviors, was positively asso-

ciated with adherence. Th e response rate was higher among

people who engaged in regular physical activity and tended

to be lower among smokers, consistent with previous reports

(29,32) . Women who reported regular practice of breast or

cervical cancer screening were also more likely to accept an

invitation for CRC screening. Th e lack of an eff ect of previous

practice of PSA testing among men might be explained by the

diff erent degree of an individual ’ s involvement in the choice to

be examined. Indeed, the decision to undergo this test is usually

prompted by direct physician ’ s advice as opposed to women ’ s

choice to respond to a program invitation.

Perceived susceptibility to CRC was positively associated

with adherence, although participants tended to overestimate

their individual risk: ~ 80 % of those who were able to quantify

their risk over the next 10 years rated it higher than the actual

3 % cumulative CRC incidence fi gure derived from cancer reg-

istries. Perceived risk apparently has a more important role in

orienting the decision of people invited for a more invasive

test such as FS, as already reported (30,33) . Our data suggest

that, contrary to previous reports (29) , such a trend refl ects

According to the fi ndings of a recent systematic review (27) ,

the implementation of specifi c organizational changes (including

fi nancial coverage, active invitation, and reminders for patients)

represents the most eff ective intervention to promote adherence.

A positive association of the introduction of an organized pro-

gram with a reduction in disparities in screening adherence by

socioeconomic status (measured either by education, income,

or occupation), as well as in the context of CRC screening pro-

grams, was clearly documented (11,28) . Th erefore, the adoption

of such a model in our setting likely explains the lack of eff ect of

age and educational level on the likelihood of participation in our

population, contrary to previous fi ndings (29 – 31) .

Furthermore, the method of recruitment likely explains the

minor role of logistical barriers, which were cited as the primary

reason for declining the invitation by < 5 % of nonattenders. How-

ever, organizational barriers may still have a role, as employed

subjects showed a lower compliance at the initial invitation com-

pared with retired people and housewives, and the proportion of

regular attenders is signifi cantly lower in this group, thus indicat-

ing the persistent diffi culties faced by people with job constraints

in coping with screening-related procedures.

Predisposing factors related to attitudes and beliefs toward

screening emerged in our setting as the most important pre-

dictors of participation. Health motivation, indicated by active

Table 3 . Main reason for attending screening (attenders only)

Main reason for attending screening

Attenders

FOBT ( n =314) n ( % )

FS ( n =302) n ( % )

Patient’s choice

( n =157) n ( % )

Useful to un-dergo preven-tive tests

159 (50.6) 145 (48.0) 74 (41.1)

Feel reassured by engaging in preventive con-trols to reduce cancer risk

40 (12.7) 33 (10.9) 13 (8.3)

Feel at risk for CRC

19 (6.1) 20 (6.6) 7 (4.5)

Presence of symptoms possibly related to CRC

20 (6.4) 21 (7.0) 12 (7.6)

Advice from friends, partner, or GP

27 (8.6) 34 (11.3) 18 (11.5)

Know friends or relatives with CRC

25 (8.0) 22 (7.3) 11 (7.0)

Pre-existing appointment

12 (3.8) 26 (8.6) 10 (6.4)

CRC, colorectal cancer; GP, general practitioner; FS, sigmoidoscopy; FOBT, fecal occult blood test.

Table 4 . Main reason for refusing screening (nonattenders only)

Main reason for refusing screening

Non attenders

FOBT ( n =275) n ( % )

FS ( n =287) n ( % )

Patient’s choice ( n =139) n ( % )

Worried about pain, discom-fort, injury associated with the test

21 (7.6) 67 (23.3) 23 (16.6)

Have no current health problems or symptoms

32 (11.6) 49 (17.1) 26 (18.7)

Anxiety about the possibil-ity of being diagnosed with CRC

35 (12.7) 22 (7.7) 13 (9.4)

Believe the test could be ineffective

15 (5.5) 17 (5.9) 2 (1.4)

Work / family constraints

51 (18.6) 47 (16.4) 28 (20.1)

Already had the test done

29 (10.6) 18 (6.3) 16 (11.5)

Current illness 35 (12.7) 34 (11.9) 9 (6.5)

Lack of interest in screening

33 (12.0) 13 (4.5) 6 (4.3)

Do not remem-ber receiving the letter

32 (11.6) 20 (7.0) 16 (11.5)

CRC, colorectal cancer; FS, sigmoidoscopy; FOBT, fecal occult blood test.

© 2010 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

195 Predictors of Participation in CRC Screening

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increased participation and greater perception of personal

absolute CRC risk. Th is hypothesis is supported by the fi nd-

ings of the inquiry among subjects who were requested to

an increased concern regarding the personal risk of develop-

ing CRC. Indeed, among people allocated to the FS arms, but

not to other groups, we found a positive relationship between

Table 5 . Factors associated with anxiety or lack of confi dence in screening a

Factor associated with anxiety or lack of confi dence in screening

Anxiety about screening Believes that screening is ineffective

n OR 95 % CI OR 95 % CI

Age (years)

55 – 59 634 1 1

60 – 64 840 1.00 0.75 – 1.34 1.50 1.02 – 2.19

Education

Primary school 638 1 1

Secondary school 386 1.12 0.67 – 1.63 0.93 0.56 – 1.48

High school 413 1.22 0.81 – 1.84 0.63 0.37 – 1.07

Physical activity

No physical activity 412 1 1

At least once a month 1029 0.71 0.51 – 0.99 0.73 0.48 – 1.11

Smoking habits

Never 691 1 1

Current smoker 312 1.70 1.18 – 1.46 1.30 0.84 – 2.04

Former smoker 426 0.93 0.64 195 – 1.34 0.52 0.31 – 0.87

Employment status

Housewife / retired 1105 1 1

Employed 369 0.94 0.79 – 1.13 1.26 1.01 – 1.56

Source of information

Regularly reads daily newspaper

1021 1 1

Does not read news-paper

421 1.77 1.27 – 2.47 1.81 1.20 – 2.72

Reading information material

Did not read the letter nor the leafl et

306 1 1

Did read the letter 476 0.79 0.53 – 1.19 0.81 0.50 – 1.81

Did read the letter and the leafl et

647 0.50 0.34 – 0.75 0.42 0.26 – 0.70

GP’s advice

Did not seek GP’s counseling

922 1 1

Sought GP’s counseling 473 0.81 0.60 – 1.10 0.51 0.33 – 0.77

Knowledge of CRC preventive test

Does not know the test

296 1 1

Does know the test 1174 0.89 0.61 – 1.28 0.70 0.46 – 1.08

CI, confi dence interval; CRC, colorectal cancer; GP, general practitioner; OR, odds ratio. Reference: people considering screening effective and reporting low anxiety about regular practice of preventive tests. a Multinomial logistic regression model adjusted by gender, arm, and screening center.

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Th e information conveyed with the invitation showed a posi-

tive infl uence on an individual ’ s decision, as participants were

more likely to report having read the letter and / or the informa-

tion leafl et, and people having read the leafl et reported lower

levels of anxiety with regard to screening. Conversely, ~ 74 % of

the people enrolled had not read the leafl et and, even if knowl-

edge of the screening process was increased among refusers

who reported having read the leafl et, they shared the same

expectations with regard to the pain associated with FS as those

who had not read it.

Th e potential limitations of this communication tool have

been highlighted already by a recent review documenting that

leafl ets improve knowledge of screening, but may show a lower

impact on individual ’ s attitudes and beliefs (40) . Written com-

munication may still represent a barrier for subjects with low

education, who may fi nd it diffi cult to understand probabilistic

estimates of benefi ts and risks and may have little confi dence

in relying on written information alone to make health-related

decisions (41 – 43) . Indeed, educational level still showed an

eff ect on decision-making among subjects allocated to the

group that was off ered the choice between FS and FOBT on the

basis of the evaluation of the risk benefi t balance presented in

the leafl et. Moreover, subjects with lower education were less

likely to report having read the leafl et and they tended instead

to rely on their GP ’ s advice to orient their decision.

Th ese fi ndings confi rm the role of personal encounters in

transferring information, particularly among the less edu-

cated. Personal counseling might be important when consider-

ing that nonparticipants feel more oft en worried and nervous

about being examined; they expect screening to be painful and

they perceive diffi culties in fi nding time to participate. How-

ever, educational eff orts aimed at promoting the impact of

the messages conveyed by health-care providers may be nec-

essary (20) . Indeed, physician ’ s counseling showed a positive

infl uence on beliefs, but not on attitudes regarding screening,

as those who consulted their GP were less likely to consider

screening ineff ective, although reporting similar anxiety lev-

els with regard to undergoing screening tests as those who

decided on their own.

Th e observed absence of a signifi cant gradient in the likeli-

hood to comply with the screening invitation across educational

levels, aft er adjusting for beliefs and expectations regarding

screening and for the sources of health information, is con-

sistent with a previous report (44) , suggesting that cognitive

variables are mainly responsible for the observed association of

Socio-Economic Status with interest in screening.

Given the cross-sectional design of this analysis, we cannot

exclude the possibility that the association of leafl et reading with

a reduction in anxiety and an increased confi dence in screening

eff ectiveness may simply refl ect a self-selection of people who

read the information material. However, the eff ect was main-

tained aft er adjusting for other predisposing factors associated

with anxiety related to screening, and it was specifi c for the leaf-

let, as reading the invitation letter only did not show an eff ect.

Moreover, it seems highly unlikely that the possible selection

choose between FS and FOBT: pain-averse patients preferred

to undergo FOBT, whereas those who valued improved accu-

racy opted for FS.

Th e positive association of test completion with knowing a

close relative with cancer is likely explained by an increase in an

individual ’ s awareness of risk, reinforcing his decision to accept

screening. Such a direct experience of the disease emerges as

one of the most important determinants of sustained compli-

ance as well. However, given the low proportion of people with

a positive family history, the fraction of attendance attributable

to this determinant is low. Interventions aimed at promoting

screening by enhancing the awareness of family risk may there-

fore have a limited impact.

Th e individual ’ s choice to involve the GP in his decision-mak-

ing process with regard to screening emerged as the strongest

determinant of screening completion, and such an eff ect was

particularly infl uential among people who were off ered the

option to choose the preferred test. Several surveys showed that

the majority of unscreened respondents had not been coun-

selled (28) , and that both patients and their health-care provid-

ers showed a lack of knowledge or concern with regard to CRC

(34) , highlighting the fact that lack of physician ’ s involvement

represents an important missed opportunity for patient educa-

tion. Indeed, a visit to a physician ’ s offi ce recently has been asso-

ciated with having undergone a CRC test (35,36) in population

surveys, whereas receiving an invitation letter signed by the

GP was found to be associated with increased participation in

organized programs (37,38) . Physicians should be encouraged

to actively engage in promoting screening to the appropriate

target population. Eff orts aimed at increasing the proportion

of people who consult their GP regarding preventive behaviors

might favor the involvement of physicians in preventive coun-

seling (39) . Such interventions might have a major impact on

participation when considering the 36 % estimated fraction of

participants who can be attributed to the involvement of GPs

in decision making, even if only ~ 23 % of our patients sought

advice from their GP before undergoing the test.

A negative opinion regarding screening eff ectiveness rep-

resented the most infl uential barrier for compliance with

the invitation, and it accounted for ~ 20 % of cases of nonat-

tendance. Th e infl uence of beliefs with regard to prevention

is supported by the fact that more than 50 % of responders

mentioned usefulness of early diagnosis and a feeling of being

reassured by regular controls as the main reasons for com-

pleting the proposed test. However, awareness of cancer risk,

preventive health orientation, and positive beliefs regarding

screening may not be suffi cient for an individual to decide to

undergo screening. Anxiety with regard to regularly undergo-

ing preventive tests represents a strong negative predictor of

participation, even among patients who consider screening to

be eff ective.

Communication between provider and patient, on the basis

of an explicit sharing of information regarding risks and ben-

efi ts, has been identifi ed as a critical factor aff ecting cancer-

screening rates (21) .

© 2010 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

197 Predictors of Participation in CRC Screening

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associated with the lower response rate to the questionnaire

among nonattenders compared with that of attenders might

have determined the observed results. However, given the fact

that, among nonattenders, people who could not be traced rep-

resent about half of the 28 % of nonresponders to the interview,

this might result in a slight underestimation of the role of logis-

tical barriers. When considering the determinants of sustained

compliance, it should be noted that the size of the compared

groups (irregular and regular attenders among compliers to

the fi rst invitation) was low and therefore we were able to show

only the most infl uential predictors.

Recent randomized trials (45,46) have shown that better

compliance can be achieved using an immunological FOBT,

as in our study, compared with guaiac tests. Th ese results are

explained by the lack of dietary and drug restrictions and easier

sampling methods, which suggest that the infl uence of prac-

tical barriers on participation rates might be increased when

considering programs using guaiac FOBT, as compared with

our setting. However, it seems unlikely that the role of beliefs,

attitudes, and expectations related to screening, as well as of

communication tools, might be infl uenced by those logistical

diff erences.

In conclusion, we found that, in the context of an organ-

ized population-based screening program, direct experience

of CRC among close relatives represents a strong predictor

of participation, reinforcing both the decision to undergo

the proposed test and to maintain such behavior over time.

Previous experience or knowledge of the proposed test rep-

resents a barrier to participation in the initial screening, but

the actual screening experience may reinforce the motivation

to maintain the adopted behavior. Subjects completing the

initial screening test tend to be more health oriented and to

show a better knowledge of CRC, although they may overes-

timate their individual risk. Anxiety represents a strong neg-

ative predictor of engaging in screening, even among patients

who consider screening to be eff ective. Lack of confi dence in

screening eff ectiveness was also an important determinant of

nonparticipation. Th e involvement of GPs in decision-making

represented the strongest predictor of participation. Even if

only 23 % of people actually shared their decision with a phy-

sician, this was helpful, in particular, for less-educated people

who were less likely to read the information leafl et. Interven-

tions aimed at prompting subjects invited for screening to

seek GP ’ s counseling might facilitate GP ’ s recommendation

(39) . Th e fi nding of a positive impact of GP ’ s counseling on

beliefs regarding screening, but not on anxiety related to the

testing process, suggests the need of educational interven-

tions to support the potential role of GPs. Th e leafl et mailed

together with the invitation represented an additional valu-

able tool for orienting screening behavior. Approximately

26 % of subjects, mainly better educated, based their deci-

sion only on the information conveyed in the leafl et, which

showed a positive infl uence on beliefs and attitudes regard-

ing screening. Even if the role of factors related to screening

organization seemed less infl uential, organizational changes

may be required to favor access to the screening of employed

subjects and to support maintenance of screening attendance

over time.

Questionnaire : Questionnaire depicting Predictors of Patients ’ Participation S.CO.RE. 2 Trial is available on the online version of the paper at http://www.nature.com/ajg.

CONFLICT OF INTEREST Guarantor of the article : Carlo Senore, MD.

Specifi c authors contributions : Study concept and design:

Carlo Senore, Paola Armaroli, Nereo Segnan, Luigi Bisanti,

Grazia Grazzini, and Bruno Andreoni; data acquisition: Marco

Silvani, Serena Taddei, Orietta Giuliani, Luisa Marai, Anna

Marutti, and Giovanna Genta; performance of endoscopic

exams: Guido Castiglione, Stefano Gasperoni, and Giuseppe

Malfi tana; data analysis and interpretation: Carlo Senore,

Paola Armaroli, and Nereo Segnan; draft ing of the paper:

Carlo Senore and Paola Armaroli; and critical revision of the

paper for important intellectual content: Nereo Segnan, Luigi

Bisanti, and Grazia Grazzini. All authors have revised and

approved this version of the paper.

Financial support : Support for the study was provided by a

grant from the Italian Association for Cancer Research (AIRC:

1998 – 2000). Th e Istituto Oncologico Romagnolo (IOR), the

Fondo “ E Tempia, ” the University of Milan, and the Piedmont

Regional Health Authority supported the implementation of

the study in Rimini, Biella, Milan, and Turin, respectively.

Potential competing interests : None.

Study Highlights

WHAT IS CURRENT KNOWLEDGE 3 Higher socioeconomic status, family history of colorec-

tal cancer (CRC), and health orientation may increase, whereas organizational constraints, cost of the test, absence of current health problems or CRC symptoms, and lack of a physician ’ s recommendation may reduce CRC screening rates.

3 Each available test requires specifi c procedures and shows a different risk profi le.

3 The relative weight of the predictors of participation is infl uenced by the screening setting and by the health-care organization.

WHAT IS NEW HERE 3 A greater perception of personal absolute CRC risk is as-

sociated with the choice of more invasive tests, such as sigmoidoscopy. Pain-averse patients prefer to undergo fecal occult blood test.

3 Better-educated people are more likely to use written information conveyed with the invitation, whereas those with a lower educational level are more likely to rely on a physician ’ s advice.

3 Anxiety regarding early-detection tests represents a strong negative predictor of engaging in screening, even among people who consider screening to be effective.

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