The Role of GPs in Increasing Compliance to Colorectal Cancer ...

Cancer Causes and Control (2006) 17:45–52 DOI 10.1007/s10552-005-0380-9

ORIGINAL PAPER

The role of GPs in increasing compliance to colorectal cancer screening: a randomised controlled trial (Italy) Antonio Federici Æ Paolo Giorgi Rossi Æ Francesco Bartolozzi Æ Sara Farchi Æ Piero Borgia Æ Gabriella Guastcchi

Received: 10 March 2005 / Accepted: 22 June 2005 Springer-Verlag 2006

Abstract Aims To assess the effect of the provider (GPs versus hospital) on the compliance in returning the faecal occult blood test. To analyse the characteristics of the GP associated with high compliance among his beneficiaries. Methods A questionnaire about screening attitudes was mailed to the 1192 GPs working in 13 districts of the Lazio region. We asked the GPs to participate in a randomised trial, we sampled 130 GPs and about 1/10 of the GPs’ 50– 75 year old beneficiaries (n = 3657) were invited to be screened at the GP office and 1/10 (3675) at the nearest gastroenterology centre. Results 58.5% of the GPs completed the questionnaire and 22.7% agreed to participate in the trial. The compliance in the GP arm was 50%, in the hospital arm 16% (RR 3.4; 95% CI: 3.13–3.70). There was a high variability in the compliance obtained by the GPs. GPs with more than 25 patients visited/day and those incorrectly recommended screening of colorectal cancer obtained a lower compliance (OR 0.74, 95% CI: 0.57–0.95 and OR 0.76, 95% CI: 0.59– 0.97, respectively). Conclusions The involvement of GPs in colorectal cancer screening can be very effective to enhance the compliance, but the effectiveness is dependent on their willingness to be involved.

A. Federici Æ P. G. Rossi (&) Æ S. Farchi Æ Piero Borgia Æ G. Guastcchi Agency for Public Health, Lazio Region, via di S. Costanza 53, 00198, Rome, Italy e-mail: [email protected] Tel.: +39-068-3060438 Fax: +39-068-3060463 Francesco Bartolozzi Campus Biomedico, University Hospital, Rome, Italy

Keywords Colorectal cancer Æ Compliance Æ General practitioners Æ Oncological screening Æ Randomised controlled trial Introduction Colorectal cancer screening is an effective measure in reducing cancer mortality. The European Community recommends annual screening for people over 50 years old with the Faecal Occult Blood Test (FOBT) [1]. Organised programs of population screening are more effective than opportunistic screening to guarantee high participation, high standard of quality and monitoring interval cases and other adverse effects of screening [2]. Despite the evidence of efficacy [3] and the large consensus on screening strategies [4], in Italy to date few Colorectal Cancer Screening (CRCS) programs have been fully implemented. The involvement of general practitioners (GP) or family practitioners has been recommended by several guidelines about screening program organisation [4–6]. Even though GPs are considered very important in any preventive practice because of their natural proximity to healthy beneficiaries, several studies have shown that GPs are not always well informed about CRCS practice, a consistent percentage of them do not trust FOBTs as an effective screening tests and finally there is a large variability in the recommendations given to their beneficiaries about CRCS [7–14]. Few randomised trials have been conducted to evaluate the effectiveness of intervention in increase compliance to CRCS with FOBT [15–22], and only two involved a GP reminder as intervention [22, 23]. The Lazio region conducted a set of pilot studies to obtain the information needed to plan a CRCS program with an evidence-based organisation [14, 24, 25].

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This experimental phase consisted of a large survey of GP’s screening knowledge and practice. Within the surveyed population we asked the GPs to participate in a randomised controlled trial to assess the effect on the compliance of the provider, in one arm the GP and in the other arm the hospital. Aims of this study are to assess the effect of the provider on the compliance of the 50–74-year-old population in returning the FOBT and to analyse the characteristics of the GP that are associated with high compliance among his beneficiaries. Population and methods The setting The Lazio region has 5.3 million inhabitants and it includes the city of Rome. The design of the study has been described in detail elsewhere [24]. Briefly we selected a convenient sample of 13 hospitals (of 20 due to participate in the screening programme) to represent all types of gastroenterology units (five university hospitals, three large research hospitals, five local hospitals) and all the geographic areas (seven in the metropolitan area of Rome, two in the outskirts of Rome, four in the small cities and rural areas of the province).

Cancer Causes and Control (2006) 17:45–52

computer in the office; and willingness to provide the list of the practice population to the centre coordinating the study. The randomised controlled trial was planned with a four-armed factorial design: • •

Two test providers, the GP and the hospital Two types of test, Guaiac (Hemo-fec, Roche Diagnostic, Mannheim Germany) and immunochemical (OC-hemodia, Eiken, Tokio, Japan).

The trial outcome was the percentage of compliance: the number of people who responded over the total number of invited people. For each of the 13 districts we sampled 10 eligible GPs. The sampled GPs were randomised, for each district, five to the immunochemical test and five to the Guaiac test. We randomly sampled two-tenths of the target practice population of each GP; about one-tenth of the population were randomised to the GP arm and one-tenth to the hospital arm (Figure 1). We decided to invite one-tenth of the target population in one month in order to simulate a routine work load for yearly screening, considering 10 months of work per year; Figure 2 shows the schedule for the trial conduction. We analysed the lists of randomised beneficiaries in order to avoid assigning cohabitants to different arms: if the second member of a pair with the same telephone number was assigned to a different arm, he or she was rejected and substituted.

The survey

Description of the intervention

We included in the survey all the GPs with offices in the 13 districts (out of 50 existing in Lazio) where the selected hospitals are placed. In June 2002 we mailed a questionnaire with the letter of consent for the trial. After one month we offered the non-respondents the opportunity to complete the questionnaire during a telephone interview, this re-collecting lasted from July to October 2002; a second re-collecting phase was performed in the spring of 2003 [14].

The coordinating centre organised a one-day course about CRCS counselling and the objectives of the study for the participating GPs. The coordinating centre mailed different letters to the two randomised populations: the first to the GP arm group, signed by the GP, invited the patient to pick up and return the FOBT at the GP’s office; the second to the hospital arm group, also signed by the GP, invited the patient to pick up and return the FOBT at the gastroenterology centre of the hospital. The GPs were free to make phone reminders if the invited patients did not respond. Each individual GP decided how to schedule the appointments for their patients, which were then communicated in the invitation letter. An economic incentive of about e1000 was provided to the GPs who participated in the trial, plus e10 for each compliant beneficiary. The incentive was agreed to by the two major physicians’ unions and was comparable to the fee for other preventive actions. Patients received all instructions when they picked up the test. All tests were analysed at the gastroenterology centre of the district. The providers had to communicate the result of the test to the patients and, in case of positive test, the providers immediately scheduled an appointment for the colonoscopy at the

The questionnaire The questionnaire was translated and re-contextualised from the English version, which had been validated by the National Cancer Institute [7]. It was designed to be selfadministered by the physician in 15 min. It included: demographic characteristics, knowledge about oncological screenings, level of agreement with international CRCS guidelines, and recommendation of CRCS tests (FOBT, sigmoidoscopy, colonscopy) to the practice population. The trial The conditions for GP eligibility were: more than 100 in the target practice population (age 50–74); a personal

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Eligible GPs 1194

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Questionnaire on screening attitudes

Participation to trial

No 902

292 699 Sampling

130 Sampling of target population 2/10 =3604

65

GP Randomization Guaiaco vs.Immuno.

64

Sampling of target population 2/10 =3716

1 withdrawal Individual randomiz. GP vs.hospital Guaiaco hospital 1797

Individual randomiz. GP vs.hospital Guaiaco GP 1807

Immuno hospital 1858

Immuno GP 1858

Fig. 1 Study design. The flow chart describes the GPs population surveyed and the two-step randomisation, producing four arms of the factorial trial.

gastroenterology centre. We registered compliance only for the colonoscopies performed in the participating centres. We made a site visit to all gastroenterology centres to install the optical reading machines for the immunochemical test. All study participants were informed about the study aims and methods, and about the use of the tests. We provided hospitals and GPs with EpiData 2.1 software [26] with the personal data of the invited subjects, to which they added pick up and return dates, any phone contact and test outcome. After the 30 days recruitment period and 15 days test return period, all data was collected from the providers. Test results from the providers were compared with those sent from laboratories interpreting the tests at the gastroenterology centre.

ommending (FOBT to people under 50 or more than yearly); under-recommending (beginning after age 50, or with longer than 2-year periods); and non-recommending. We computed a screening knowledge score based on 13 items of the questionnaire, the possible range was from 0, all the worst answers, to 18, all the best answers [14]. Statistical methods

We classified the GPs as correctly recommending (that is FOBT every 1 or 2 years, in people over 50); over-rec-

We drew a factorial design to analyse the effects of provider and type of test. To determine the necessity of a stratified analysis, the interaction between provider and type of test was estimated with a log-likelihood ratio test between the logistic regression models with and without the interaction component (this analysis was performed not taking into account the effects of practice clustering in order to have inflated power). To quantify the effect of the provider, we used a random effect logistic regression using the GPs as clustering

Fig. 2 Time schedule for the trial conduction. with each GP was agreed a day 0 as the starting date. The test pick-up period lasted one month, while the returning was admitted for other 15 days. The

time schedule was the same for the two arms, GP and Hospital. Patients could participate in the screening after the deadlines, but were not considered as compliant for the trial outcome

Analysis

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Table 1 Comparing the characteristics of GPs that participated in the trial with those who did not

Consent to participate in the trial Yes

No

N % N % N % N %

90 53.25 202 46.98 28 48.28 2 25

79 46.75 228 53.02 30 51.72 6 75

169 100 430 100 58 100 8 100

N 268 % 50.66 Female N 78 % 45.88 Recommendation of FOBT for CRCS Incorrect N 127 % 57.73 Non-recommending N 63 % 25.4 Correct N 156 % 67.53 Patients visited per day £25 N 252 % 50.91 >25 N 92 % 46 Residence Rome N 251 % 53.52 Other N 99 % 44

261 49.34 92 54.12

529 100 170 100

93 42.27 185 74.6 75 32.47

220 100 248 100 231 100

243 49.09 108 54

495 100 200 100

218 46.48 126 56

469 100 225 100

Age £45 46–55 56–65 >65 Gender Male

variable; this model also quantifies the effect of each GP individually, estimated by rho. The association between compliance in the GP arm with the compliance in the hospital arm among GPs was tested performing an ANOVA regression. Box. Sample size and power of the study Survey: The power of our survey (699 GPs) is 80% to detect a relative risk of 1.5 for an exposure prevalence of 30% with 95% confidence. The power of the survey nested in the trial to detect a 1.5 relative risk for a factor with a prevalence in the population of 25%, (127 GPs, i.e. primary sample unit, with 55 individuals each, or 28 by arm, with an intra-cluster correlation of 0.1, alpha 0.05) is 88.8% for the total population, and 85% by arm. Trial: The study size was calculated, with the hypothesis of absence of interaction, to obtain a power of 90%, with alpha .05, to detect a relative risk of 1.44 for the type of test, with an expected response rate in the lowest group of 18% (data from an unpublished pilot), an intra cluster correlation of .1 and an average cluster size of 55 [29]. As a consequence the minimum detectable relative risk for provider was 1.17. The resulting study size was 130 cluster and 7150 subjects. The power, eventually reduced due to interaction and to the consequent stratified analysis, allows us to detect a relative risk of 1.5 for the type of test and of 1.25 for the provider.

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Pearson v2

Total

v2 (3) = 3.70, p = 0.296

v2 (1) = 1.18, p = 0.278

v2 (2) = 93.61, p = 0.000

v2 (1) = 1.37, p = 0.241

v2 (1) = 5.51, p = 0.019

The association between compliance and GPs’ characteristics was tested performing a logistic regression in which the GP was considered the primary sampling unit. All analyses were performed with Stata 7 [27] software. All odds ratios given by logistic regressions were converted to relative risks using the formula reported by Zhang and Yu [28]. The study was submitted and approved by the Committee for Ethics in Screening of the Regional Agency for Public Health, June 16 2002, approval no 1.

Results Adhesion to the study: comparison of participating and non-participating GPs Table 1 shows a comparison of the 292 GPs who agreed to participate in the trial and the 407 GPs who did not. Those who participated were more likely to reside in Rome and more likely to have correctly recommended the FOBT for CRCS.


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Fig. 3 The graph reports the compliance obtained in each of the 129 practices: the compliance of those assigned to the GP arm is reported on the x axis, and the compliance of those assigned to the hospital arm is reported on the y axis. The broken lines represent the mean compliance obtained in the arm, the relative risk is 3.4, 95% CI: 3.13–3.70

compliant subjects while the hospital had only 16.2% (597) (Figure 3), RR 3.40 (95% CI: 3.13–3.70). The difference was completely due to a higher probability of picking up the test, while the probability of not returning the test is almost the same: 8.7% in the GP arm and 8.3% in the hospital arm (RR 0.97, 95% CI: 0.69–1.37). Six phone contacts were reported in the hospital arm, and 1162 in the GP arm. The presence of phone contact was significantly associated with the probability of returning the FOBT (odds ratio 1.4; 95% CI: 1.2–1.7; adjusting by provider and test and taking into account the effect of individual GP on variance). Colonoscopies were recommended for all the 192 subjects with positive FOBTs, 145 (7.9%) in the GP arm and 47 (7.9%) in the hospital arm, the compliance to colonoscopy was similar in the two arms: 69.0% and 72.3% respectively (v2 (1) = 0.19; p = 0.66).

Sampling and randomisation (Figure 1)

Variability among GPs and among hospitals

Of the 1194 GPs with offices in the 13 health districts with gastroenterology centres, 699 (58.5%) answered the questionnaire: 263 (37.6%) by mail, 277 (39.6%) after the first telephone collection and 159 (22.7%) after the second. Two hundred and ninety-two (24.5%) GPs consented to the trial (range among the districts 12.3–39%), of whom 130 were sampled and randomised to the two type of test arms: a GP, randomised to the Guaiac, fell seriously ill after randomisation and it was impossible to contact him. There were 3611 individuals randomised to the Guaiac test, and 3721 to the immunochemical test. The populations randomised to the GP did not statistically differ from the hospital group for any of the characteristics that we analysed: gender (v2 = 0.29; p = 0.59), three age classes (v2 = 0.52; p = 0.77), and residence (v2 = 0.02; p = 0.89).

Figure 3 shows the strong variability among GPs in the compliance obtained within their practice population: the compliance in the group assigned to the GP is on the x axis and the compliance in the group assigned to the hospital is on the y axis. The range of the percentage of compliance among practices is 0–95% for the GP arm and 0–56% for the hospital; variability is higher than expected by random fluctuation in both the arms (the value of rho, i.e. the proportion of the total variance contributed by the practice, in the hospital group is 0.34, 95% CI: 0.25–0.44; the value of rho in the GP group is 0.41 95% CI: 0.34–0.49). There is a statistically significant association (r2 = 0.195; f(1;127) = 30.8; p = 2 · 10 7) between the compliance obtained by a GP in the population assigned to GP arm and the compliance observed for the population of the same practice assigned to the hospital arm. Also among the districts

60% 50% 40% 30%

hhospital mean= 16.2%

Compliance in the hospital arm

GP mean= 50.2% 50.

20% 10% 0% 0%

20% 0%

40%

60%

80%

100%

Compliance in the GP arm

Given the factorial design we had to check for interaction before choosing the strategy of analysis. The interaction we detected was very small: RR for testing through the provider (GP versus Hospital) 3.4 (95% CI: 3.0–3.8) in the Guaiac arm and 3.4 (95% CI: 3.0–3.8) in the immuno arm (test for the interaction between the factors (log likelihood ratio test: v2(1) = 1.63; p = 0.20). In the absence of interaction we proceeded analysing the two factors independently. The effect of the provider on compliance In our setting, the provider is a strong determinant of compliance to FOBT: GP providers had 50.3% (1840)

Compliance in the hospital arm

35%

Test for interaction

Rome other

30% 25% 20% 15% 10% 5% 0% 30%

40%

50%

60%

70%

80%

Compliance in the GP Fig. 4 The graph reports the compliance obtained in each of the 13 districts: the compliance of those assigned to the GP arm is reported on the x axis, and the compliance of those assigned to the hospital arm is reported on the y axis. The squares represent the districts in Rome and the diamonds the districts in the rest of the region

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we observed a statistically significant difference in the compliance obtained (the value of rho is 0.41 95% CI: 0.34–0.49); no clear geographical trend is discernible, the city of Rome had the best and worst performers (range 5–29%), while in the rest of the region the hospitals had medium and high performances (range 11–25%) (Table 2, Figure 4). GP characteristics that influenced compliance Table 3 shows the multivariate logistic regression analysis performed on 127/129 GPs participating in the trial who completed the questionnaire. The analysis showed substantially the same results for both halves of the practice population. The following associations resulted statistically significant associated in the model with the whole population: GPs who visited more than 26 patients per day obtained lower compliance (OR 0.74, 95% CI: 0.57–0.95), GPs residing in Rome obtained lower compliance (OR 0.77, 95% CI: 0.62–0.95) as well as GPs who incorrectly recommended the FOBT for CRCS (OR 0.76, 95% CI: 0.59–0.97). The score of screening practice knowledge did not show a significant association with the compliance obtained. The intra-cluster correlation was higher in the GP arm than in the hospital arm.

Discussion The main objective of the study was to ascertain which provider could obtain more compliance, the GP or the hospital. The answer to this question in our setting is very Table 2 Multivariate analysis of the GP’s characteristics influencing compliance obtained during the trial, by provider arm

Total population model

Hospital arm population

GP arm population

OR

OR

OR

95% Conf. interval

95% Conf. interval

95% Conf. interval

Gender Male Female

1 1.26

0.94

1 1.67 1.30

0.87

1 1.94 1.31

0.90

1.91

Age 35 year Increase per year

1.00 1.02

1.00

1.00 1.04 1.03

1.00

1.00 1.06 1.02

0.99

1.05

Patients visited per day £25 1.00 >25 0.74

0.58

1.00 0.95 0.68

0.47

1.00 0.98 0.73

0.52

1.04

Recommendation of FOBT for CRCS Correct 1.00 Incorrect 0.76 0.59 Non recommending 0.94 0.69

1.00 0.97 0.77 1.28 0.86

0.54 0.58

1.00 1.09 0.71 1.27 0.97

0.52 0.64

0.99 1.47

Residence Other Rome

1.00 0.95 0.71

0.53

1.00 0.95 0.77

0.57

1.04

1.00 0.77

Intra-cluster correlation 0.080

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clear: the relative risk for returning the test to the GP is 3.4 (95% CI: 3.13–3.70) times higher than the hospital, independent of type of test and district. Our results support those of the existing studies: we found only two randomised controlled trials that considered the involvement of the GP [22, 23], and even though the contribution of GPs in these trials was limited to a mail-in reminder, the effect was positive. Other studies tested different interventions aimed at increasing compliance, but rarely was the observed effect so large [15–20, 30, 31]. Surprisingly the involvement of the GP did not increase colonoscopy compliance, a critical point in CRC screening [32], we do not know however if there are differences in the proportion of colonoscopies performed outside the participating gastroenterology centres. We observed very high variability among the 13 hospitals (Table 3). The city of Rome shows the most dramatic differences in performance; no other geographical pattern was discernible. We had little information about the accessibility and organizational efforts actually implemented by the hospitals in order to enhance compliance; furthermore, the design of the study did not allow us to analyze the effect of the hospitals’ characteristics. There is extreme variability in the compliance obtained by each GP, ranging from 0% to 95%, and was not explained by the small effect of phone contacts (odds ratio 1.4). A smaller variability (range 0–50%) not due to a random effect was also detectable in the hospital arm and there was a significant positive correlation between the percent of compliance in the GP arm and in the hospital arm in the same practice population. Consequently, the first question generated by the main

0.62

0.074

0.153


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Table 3 Characteristics of the 13 hospitals and districts that participated in the trial, and compliance obtained by trial arm Hospital

A B C D E F G H I J K L M

Type of hospital

University Hospital University Hospital University Hospital District Hospital Independent Hospital University Hospital Independent Hospital University Hospital District Hospital District Hospital District Hospital District Hospital Independent Hospital

Location

Rome Rome Rome Rome Rome Rome Rome Rome Out of Out of Out of Out of Out of

Rome Rome Rome Rome Rome

Type of district

City centre Metropolitan area Metropolitan area City centre Hinterland Metropolitan area Metropolitan area Metropolitan area Hinterland Town (50,000 inhabitants) Town (50,000 inhabitants) Rural Town (100,000 inhabitants)

result was which characteristics of the GPs determine compliance. We found a negative association with visiting more than 26 patients per day: we can interpret that the negative effect of having little time to commit to screening is not balanced by the advantage of having more contact with the patients. The differences between the geographical areas are important and significant: the metropolitan area of Rome has lower compliance, possibly due to the difficulties in mobility in the urban area. Finally, the GPs who incorrectly recommend FOBT had poor performance. Greater knowledge and acknowledgement of guideline recommendations about screening in our trial did not always indicate a stronger effort to obtain high compliance to the FOBT. These results were similar for both randomised populations, independent of provider: the characteristics of the GP determine the compliance and have the same magnitude of effect regardless of testing location. We think that the easier explanation is that the GPs’ characteristics we are analysing are underlying determinants both of the practice population and of the relations between beneficiaries and GP. These do not necessarily reflect the work or involvement in the trial by the GP, because there were probably few actual activities to increase compliance. On the other hand, the GP office is generally easier to get to than the hospital. The variability among GPs’ populations observed in the hospital arm may be related to characteristics of the practice population. Because the study’s focus was to define provider characteristics involved in screening compliance it is beyond the scope of this study to discuss the characteristics of the population that may have determined compliance, however, in this context it is relevant to report that in Italy beneficiaries choose their GP. Less than one fourth of the GPs in the study population agreed to participate in the trial, despite the economic

No. of colono scopies in 2003

No. of CRC patients treated in 2003

Compliance obtained in the trial (%) Hospital arm

Gp arm

700 1300 2400 1500 1900 3500 2300 1000 1000 2500 1300 800 1200

671 93 59 244 393 715 251 111 38 119 93 47 127

8.9 21.3 21.5 29.5 10.8 14.3 10.2 5.1 21.7 19.7 15.6 12.2 24.9

42.3 40.2 53.0 74.0 58.2 51.9 40.5 30.3 55.2 49.4 45.5 54.2 61.9

incentive. A relevant question in this situation is: Are the GPs who participated in the trial different than those who did not for the characteristics that we found to be relevant in obtaining high compliance? As expected, many characteristics of the two groups of GPs differ: the GPs who agreed to participate in the trial were younger and more frequently male, and these characteristics were not strongly associated with better performance in the trial; they were also more likely to correctly recommend FOBT for CRCS, and this characteristic is associated with the ability to obtain high compliance. So it is likely that the GPs who did not participate would have obtained low compliance. The poor participation was the first source of concern for the external validity of the trial. On the other hand, we made all efforts to operate in a setting that represented a real situation as close as possible: (1) the number of patients to be involved was proportional to the time given to conduct the screening; (2) we used two types of tests to see if there was any interaction; (3) hospitals were selected from different geographic areas, and (4) represented all levels of specialisation, from university to district hospitals. Nevertheless, the good performance of the randomisation guarantees the internal validity. Conclusions • •

•

The GPs showed scarce interest in participating in this trial. The compliance to the FOBT with GPs was 3.4 times higher than compliance with the hospital, independent from type of test and geographical area. There was high variability among GPs: GPs with heavy workloads and those who incorrectly recommended FOBT for CRCS obtained lower compliance.

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• •


The high compliance obtained in the GPs’ arm is not applicable to the whole population of GPs. The involvement of GPs in the FOBT for screening can be very effective in improving compliance, but the effectiveness is dependent on the willingness of the GP to be involved.

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