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Gut Online First, published on April 8, 2015 as 10.1136/gutjnl-2014-308081 Recent advances in clinical practice
Optimising colorectal cancer screening acceptance: a review Carlo Senore,1 John Inadomi,2 Nereo Segnan,1 Cristina Bellisario,1 Cesare Hassan3 ▸ Additional material is published online only. To view please visit the journal online (http://dx.doi.org/10.1136/ gutjnl-2014-308081). 1
Centro di Prevenzione Oncologica (CPO Piemonte), AOU Città della Salute e della Scienza, Turin, Italy 2 Digestive Disease Center, University of Washington, Seattle, Washington, USA 3 Unit of Gastroenterology, Ospedale Nuovo Regina Margherita, Rome, Italy Correspondence to Dr Carlo Senore, AOU Città della Salute e della Scienza, Centro di Prevenzione Oncologica, Via S Francesco da Paola 31, Turin 10123, Italy; [email protected] Received 27 November 2014 Revised 5 March 2015 Accepted 9 March 2015
ABSTRACT The study aims to review available evidence concerning effective interventions to increase colorectal cancer (CRC) screening acceptance. We performed a literature search of randomised trials designed to increase individuals’ use of CRC screening on PubMed, Embase, Cochrane Database of Systematic Reviews and Database of Abstracts of Reviews of Effects. Small (≤100 subjects per arm) studies and those reporting results of interventions implemented before publication of the large faecal occult blood test trials were excluded. Interventions were categorised following the Continuum of Cancer Care and the PRECEDE–PROCEED models and studies were grouped by screening model (opportunistic vs organised). Multifactor interventions targeting multiple levels of care and considering factors outside the individual clinician control, represent the most effective strategy to enhance CRC screening acceptance. Removing financial barriers, implementing methods allowing a systematic contact of the whole target population, using personal invitation letters, preferably signed by the reference care provider, and reminders mailed to all non-attendees are highly effective in enhancing CRC screening acceptance. Physician reminders may support the diffusion of screening, but they can be effective only for individuals who have access to and make use of healthcare services. Educational interventions for patients and providers are effective, but the implementation of organisational measures may be necessary to favour their impact. Available evidence indicates that organised programmes allow to achieve an extensive coverage and to enhance equity of access, while maximising the health impact of screening. They provide at the same time an infrastructure allowing to achieve a more favourable cost-effectiveness profile of potentially effective strategies, which would not be sustainable in opportunistic settings.
INTRODUCTION
To cite: Senore C, Inadomi J, Segnan N, et al. Gut Published Online First: [please include Day Month Year] doi:10.1136/gutjnl2014-308081
The uptake rate represents a critical determinant of the magnitude of the health impact of colorectal cancer (CRC) screening at the population level. Non-adherence to recommended protocols represents an important attributable factor of CRC mortality,1 particularly among deprived groups. However, in spite of the strong evidence2 3 supporting the screening effectiveness and of a general consensus of guidelines recommending screening of average-risk individuals over age 50,3 4 CRC screening rates remain low. Inequalities in screening use represent an important component of the wide variability observed within and across countries5–9 and may result in higher disease burden, lower
Key messages ▸ Substantial differences in colorectal cancer (CRC) screening use may result in higher disease burden, lower quality of life, health inequities and increased healthcare cost. Non-adherence to recommended protocols represents an important attributable factor in CRC mortality, particularly among lower socio-economic status populations. ▸ Available evidence indicates that multifactor interventions targeting multiple levels and considering factors outside the individual clinician control represent the most effective strategy to enhance CRC screening acceptance, supporting the WHO recommendation to implement population-based organised programmes. ▸ Removing financial barriers, offering all subjects in the target population the option to adhere to high-quality, screening interventions, using personal invitation letters, preferably signed by the reference primary care practitioner, and reminders mailed to all non-attendees, represent a priority for interventions aimed to enhance acceptance of CRC screening. ▸ Physician reminders may represent an additional support to the diffusion of screening in areas with low baseline uptake rates, but in any case they can be effective only for individuals who have access to and make use of healthcare services. ▸ Educational interventions for patients and providers are effective, but the implementation of organisational measures may be necessary to favour their impact. Integrating qualitative research results in the design of educational interventions represents a challenge for future research.
quality of life, increased healthcare costs and health inequities. Screening is a complex process of care consisting of several steps and interfaces between patients, providers and health organisations, which may be promoted, or impeded, at different levels by a range of factors. An extensive literature exists concerning predictors of uptake and the effect of strategies promoting attendance. However, the variability in the screening protocols and the mix of programmatic and non-programmatic delivery systems are limiting the comparability and the transferability of the results. The framework of the quality in the continuum of cancer care model10–12 provides a systematic
Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
1
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Recent advances in clinical practice approach for assessing factors that influence delivery, access and quality of screening. Recognising that cancer care delivery occurs in a multilevel environment (figure 1), this model highlights those levels of the healthcare system representing potential targets for intervention, including policy, practice, provider and patient level. It may therefore offer useful clues to identify potential targets of interventions, to assess their potential reach, as well as the determinants of their success or failure, and to identify directions for further research. Several factors interact in a synergistic manner at these different levels of care to affect provider delivery and patients’ use of screening. The PRECEDE–PROCEED model,13 explaining behavioural change as the result of the interplay of predisposing, enabling and reinforcing factors, represents a useful tool to assess the mechanisms through which these factors can affect screening behaviours. The success of a behavioural intervention requires the identification of the level that must be influenced to achieve an impact and of the optimal strategy to address the relevant factors, which can favour behavioural change. Underuse of CRC screening among uninsured groups can be influenced, for example, by availability of free-of-charge screening programmes funded by national or regional governments, while participation among insured subjects may be enabled by mailing of the faecal occult blood test (FOBT) kit, at the organisational level. These theoretical frameworks (box 1) will be used to examine existing evidence of effectiveness of interventions aimed to enhance use of CRC screening, identifying the level of care and the behavioural mechanisms targeted by each intervention. Taking into account the public health perspective, we also assessed evidence concerning cost-effectiveness of successful interventions (box 2).
METHODS Literature search We searched in first instance recent systematic reviews (SR) and meta-analyses addressing the same topics of our study on PubMed, Embase, Cochrane Database of Systematic Reviews and Database of Abstracts of Reviews of Effects. The search was based on the strategy used in the SR by Jepson et al15 with
appropriate changes according to our inclusion criteria and databases. Relevant original articles published before August 2012 (search update of the most recent review16) were retrieved through already published reviews. We subsequently searched PubMed, Embase and CENTRAL for randomised controlled trials (RCTs), reporting comparative evaluations of interventions, published until 15 October 2014. See online supplementary appendix 1 for the details of the search strategies. We excluded small-size trials (≤100 subjects per arm) and those reports preceding the publication of the European population-based trials17 18 documenting the effectiveness of guaiac FOBT (gFOBT) screening. The findings concerning the impact of interventions conducted when evidence of screening effectiveness was still lacking might not be comparable to those reported from more recent trials, implemented following endorsement of CRC screening by professional societies and governmental institutions. Observational studies were considered when assessing policy options, not easily amenable to testing by RCTs. The outcome of interest in the context of organised programmes was the participation in the first-level screening test, defined as the proportion of invited subjects who underwent the test. In opportunistic settings, the outcome considered was test coverage, defined as the proportion of the target population who had a test within the recommended interval. Interventions have been categorised according to the targeted level of the healthcare system, taking into account the specific behavioural mechanism involved and the screening model (opportunistic vs organised).
RESULTS The SR and meta-analyses literature search yielded 112 papers. These were screened for relevance based on titles and abstracts and 21 of them were judged potentially relevant. Full text could not be acquired for one review19 and 17 of the remaining 20 were included: 716 20–24 considered interventions addressing several levels of care, 610 25–29 were focused on provider, or organisation level, 330–32 on screening modality and 133 on community level.
Figure 1 Levels of intervention related to cancer screening interventions in health service settings.
2
Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
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Recent advances in clinical practice Box 1 Conceptual framework The PRECEDE–PROCEED model13 explains behavioural change as the result of the interplay of predisposing factors, providing the rationale, or the motivation, for the behaviour, of factors enabling actual realisation of the decision, and of factors reinforcing individuals’ decision to adopt the desired behaviour and supporting its maintenance over time. Interventions that focus on patient predisposing factors attempt to increase awareness and knowledge of colorectal cancer (CRC) and CRC screening, identify and address health beliefs, or values and fears that impede cancer screening. Interventions focused on patient enabling factors address costs of screening, diagnostic testing and cancer treatment, access to CRC screening and barriers impacting the acceptability of CRC screening. Patient reinforcement interventions may include reminders to complete screening or provide encouragement through peer or professional counselling. Interventions that focus on provider predisposing factors increase knowledge and enhance agreement with clinical practice guidelines for CRC screening, or dispel assumptions about subjects’ health beliefs and likelihood of screening completion. Provider interventions addressing enabling factors include the provision of sufficient time to determine CRC screening eligibility and needs, computer or manual reminders to recommend screening, or sufficient support staff and technology. Interventions of provider reinforcing factors may include the institution of payor requirements, leadership expectations, collegial norms and performance reports.
medical consultations for unrelated conditions, or on the basis of a possible increased CRC risk (family history or other risk factors, including symptoms), or as result of a patient’s request. This approach is defined as opportunistic screening, as opposed to organised screening, where all eligible subjects are actively invited, following an explicit and prespecified protocol stipulating testing and assessment procedures, offered free of charge, within an established organisational context ensuring systematic monitoring of the quality of the whole process.34 CRC screening rates in opportunistic settings differ by type of insurance and are influenced by the amount of patient copayment.35 Individuals without access to primary care are excluded from participation in those settings where most CRC screening relies on office-based interventions delivered by PCP36 and insurance status represents the most important determinant of screening coverage in the USA.37 Policy measures characterising the delivery of screening within organised programmes, including the reduction, or elimination, of costs for the participant and the implementation of a system of patients’ reminders, were identified as the most effective interventions aimed to enhance preventive services use in a comparative analysis of the relative impact of different strategies.38 Higher screening rates, with reduced inequalities across social groups, have been reported in France and Italy, in areas where organised CRC screening programmes had been introduced, as compared to areas where only opportunistic screening was available.39 40 Recent observational studies showed that the introduction of organised screening is associated with a substantial reduction in CRC mortality among populations served by the programmes, as compared with people not routinely invited.41–43
Practice organisation The RCTs literature search yielded 170 papers. These were screened for relevance based on titles and abstracts: 67 were obtained in full text and 44 were included. Reasons for exclusion are reported in online supplementary appendix 1. PRISMA flow charts are reported in online supplementary appendix 1.
Levels targeted by interventions Policy Two main policy options define the context within which screening is currently provided. Screening tests may be recommended by primary care practitioners (PCPs) during routine
Box 2 Directions for future research As long as maintaining subjects’ engagement over several screening rounds following initial attendance is required to ensure screening effectiveness, additional research is needed to identify interventions that can enhance sustained attendance. Qualitative research can offer insights on barriers to screening acceptance, which can be used to tailor educational messages. Integrating findings from qualitative studies into the design of interventions that can be sustainable in the context of large-scale population programmes represents an important aim to be addressed in future studies. Developing valid measures to evaluate the impact of specific interventions on the adoption of decisions consistent with individuals’ values and preferences represents a challenge to be addressed in future studies. Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
Service delivery: According to the results of a recent review,38 establishing separate clinics devoted to screening, involving nursing or clerical staff in the delivery of services and adopting monitoring and quality improvement approaches can have a strong positive impact on screening use. These intervention components characterise the infrastructure of screening delivery within organised programmes. A positive impact of these measures was observed also in opportunistic settings. Staff delivered interventions, designed to identify subjects eligible for screening and to offer counselling about FOBT testing,44 or assistance to fix a TC appointment,45 were associated with an increase in the rates of FOBT and TC screening, in primary care clinics. A survey of family medicine practices reported that those using nurses, or health educators, to provide behavioural counselling were also more likely to show higher screening rates than those not involving staff in counselling activity.46 The introduction of a monitored institutional directive was associated with a significant increase in the screening rates in a managed care setting.47 Invitation: The offer of a pre-fixed appointment in the invitation letter represents an effective strategy to enhance uptake,15 currently adopted in sigmoidoscopy (FS)-based programmes,48 although tested in RCTs only among women invited for breast and cervical cancer screening. Compliance with FS screening was improved by timing invitations in proximity to annual milestones, or invitees’ birthday,49 while having a nurse calling invitees to schedule an appointment was not more effective than offering an open appointment.50 Test delivery (table 1): organised programmes: Mailing of the test kit with instructions, together with the invitation letter, has been adopted in several organised programmes to maximise accessibility. Subjects receiving an invitation including an 3
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Recent advances in clinical practice immunochemical FOBT (faecal immunochemical test (FIT)) kit showed a twofold increase in the likelihood to participate, as compared to subjects receiving an invitation letter with the indication to pick up the kit by their general practitioner (GP), in a population-based programme in Belgium,52 and a more modest, though statistically significant, increase in attendance (30% vs 28%), compared to those receiving the indication to pick up the kit at a pharmacy in an Italian pilot screening study.53 Mailing of FIT kit, compared with the invitation to pick up the kit at a pre-fixed date at a primary clinic, was associated with a statistically significant increase in the screening rates among attendees in previous screening rounds of two Italian population programmes (overall response: 63.0% vs 56.8%).55 Mailing of the gFOBT test kit, as opposed to a simple mail reminder, was associated with an increase from 9.6% to 20.1% in the screening rates among previous non-responders, in a population-based study in Canada,51 while a similar increase was observed only in one centre in the Italian FIT-based programmes.55 Delivery of the kit by the GP, or by non-medical staff, who may provide counselling, enhances acceptance. Completion of FIT and gFOBT was higher among subjects required to pick up the kit at the GP’s office than among those referred to the local hospital.54 Screening activity reports indicated that involvement of trained community volunteers,62 or of pharmacies,63 in the kit distribution is associated with high participation rates, although these options were not tested in comparative trials. Opportunistic setting: Mailing of gFOBT kit, resulting in a modest (4%), but statistically significant, absolute increase in participation of primary care patients, compared with mailing of a kit request card.61 Mailing of the kit emerged as the most effective component of interventions using reminders to enhance screening rates among subjects overdue for screening:57–59 compared with mailing of the kit alone, no additional effect could be observed when adding an educational brochure,58 61 a brochure followed by a follow-up phone call,59 or a web-based educational tool.57 A larger effect on FIT uptake has been observed in studies where mailing of kit was associated with multifaceted outreach interventions, providing multilingual, or low-literacy, educational brochures and using reminder phone calls, both automated and performed by screening navigators.45 56 The potential positive effect of face-to-face interactions is supported by the results of an RCT among primary clinic attendees, showing a higher FIT uptake when a trained non-health professional delivered the kit and collected the sample from participants’ home, as opposed to direct mailing of the kit.60 Screening modality (table 2): Multiple tests70 81 82 have been validated for CRC screening, showing a different effectiveness, acceptability, safety and cost profile. The findings of a recent survey among women who had never participated in CRC, cervical or breast cancer screening programmes83 suggest that although more global barriers, such as cancer fatalism, may explain non-participation in more than one programme, the uptake of CRC screening might be influenced by specific characteristics of recommended options as dislike of the test appears to be a stronger barrier to CRC screening. Differently from clinical practice, where decision-making process mostly depends on test accuracy, acceptance represents a critical factor to orient the choice in screening programmes and in the past 20 years several studies compared the relative uptake of competitive strategies.30 31 Organised programmes with FOBTs have been implemented in several countries,84 with a trend in most recent years favouring the adoption of FIT, as opposed to gFOBT. Despite the choice between the two tests depending on several 4
organisational and economic factors, uptake and effectiveness represent key elements in the decision-making process. The uptake was substantially higher among people invited for FIT than among those offered gFOBT, in two large population-based RCTs in the Netherlands71 85 and in a previous pilot population-based intervention in Italy.67 A large study conducted in the context of an established population programme has confirmed the findings of these pilot RCTs, showing that the adoption of FIT is associated with an increased uptake over gFOBT and that it may also result in a reduction in the participation gap for age, gender and deprivation.79 Screening rates were increased when using FIT as compared to gFOBT also in a US study in a clinic setting,77 but not in an RCT in primary care setting in Israel.78 However, in this latter study, three stool samples—rather than one, as in all previous studies—were required. A recent RCT in a managed care setting showed a lower adherence among people invited to perform a two-sample FIT, or a three-sample gFOBT, as compared to those allocated to a single-sample FIT regimen80 and indeed, the higher compliance achieved when using FIT instead of gFOBT has been explained by the lack of dietary restrictions, the easier and less unpleasant sampling methods and the lower number of samples.54 Inconsistent findings have been reported when comparing FS and faecal tests. Two large Italian population-based RCTs55 86 reported a similar uptake with FIT as with FS, while the attendance rate was substantially higher both with FIT and with gFOBT than with FS in a Dutch population RCT. Compliance was also significantly lower with screening FS than with gFOBT in two average risk population cohorts, in Italy and Sweden,65 68 while another study, conducted in a single UK practice, where the GP was performing FS, reported a higher uptake with FS than with gFOBT.76 FS would appear to be particularly penalised in settings with a high FIT, or gFOBT, adherence, while a low CRC screening uptake would marginalise such difference. Different combinations of FS and faecal tests have been tested to improve screening efficacy or uptake (table 3). The addition of FS to gFOBT was associated with a substantial decrease in the uptake, as compared to gFOBT alone, in three population-based RCTs.65 66 76 A similar trend was observed when adding FS to FIT in a small Australian population RCT69 and in a recent population-based RCT in Norway.73 Offering people the option to choose between FS and FIT did not improve uptake as compared to an invitation for one of the two tests.55 69 Offering FIT to those who refuse FS screening represents an effective alternative approach: the sequential offer of FIT retrieved 19% of those declining FS invitation in an Italian population-based programme and similar findings have been reported in a Dutch pilot screening study.72 The use of colonoscopy (TC) as a primary screening tool has also been advocated, despite the lack of experimental evidence of efficacy. The uptake was lower with TC than with FIT in two large population-based RCTs, in Italy86 and Spain,74 and in a small Australian population study.69 The uptake was higher when offering screening with CT colonography (CTC) than with TC in a Dutch population-based RCT.75 Two studies are ongoing to compare the uptake of CTC and of FS or FIT.98 99
Provider The involvement of GPs was shown to be highly effective in improving compliance, both in the context of organised100 101 and opportunistic screening settings;102 103 prompting subjects invited to seek advice might facilitate GPs’ counselling,104 Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
Baker et al56
Community health centresUSA
Pilot screening programme Italy
Segnan et al55
Opportunistic setting
Pilot screening programme Italy
Federici et al54
450 subjects who had prior negative FOBT, underserved, mostly (87%) Latinos
General population sample of 26 682 subjects listed in the National Health Service register
Subjects aged 50 to 69 listed in the rosters of 130 GPs:
First RCT 3196 individuals who had previously participated in CRC screening in the previous round Second RCT 4219 people aged 50–69 years who did not respond to the first invitation
Organised screening programmes in three regions of Central Italy Italy
Giorgi Rossi et al53
Subjects aged 50–74 who had not responded to an invitation in the Colon Cancer Check pilot project 19 542 people aged 50–74 years who had not performed a colonoscopy in the past 10 years
Province-wide CRC screening programme Canada
Participants
Van Roosbroeck et al52 Population-based screening programme for CRC Belgium
Tinmouth et al51
Setting
Interventions targeting organisation of practice
Organised programmes
Reference
Table 1
Participation following the initial or reminder invitation letter
Uptake of gFOBT within 6 months
Outcome
I: usual care plus 1. A mailed reminder letter+a free FIT with low-literacy instructions, and a postage-paid return envelope 2. An automated reminder telephone and text
Group 1: invitation letter+FIT kit with instructions+information leaflet Enabling factors Group 2: invitation letter with instruction to pick up the kit in a pharmacy +information leaflet Predisposing factors Group 3: invitation letter with the offer to choose between FS and FIT +information leaflet Predisposing factors Group 4: invitation letter with prefixed appointment for FS+ information leaflet Enabling factors Group 5: invitation letter with prefixed appointment for FS followed by FIT (negative FS only) +information leaflet Enabling factors Invitation letters signed by the GP Mail reminders for non–responders
GP provider arm: invitation letter signed by the GP, inviting the screenee to pick up and return the FOBT at the GP’s office Hospital arm: invitation letter signed by the GP, inviting the screenee to pick up and return the FOBT at a hospital gastroenterology unit Enabling factors
FIT completion rate
Screening FS or FIT or combination of the two tests
FIT and gFOBT compliance
First RCT Participation in screening Intervention: mailing of FIT kit+invitation letter within 90 days of the mailing Enabling factors Control: invitation letter with instruction to pick up the kit at a primary care clinic Second RCT Intervention: mailing of FIT kit+invitation letter Enabling factors Control: invitation letter with instruction to pick up the kit at a primary care clinic
Mail group: mailing of FIT kit+invitation letter Enabling factors GP group: invitation letter with instructions to pick up the kit by the GP
Intervention group: mailed gFOBT kit+reminder letter Enabling factors Control group: reminder letter
Intervention vs control
Intervention: 82.2% (185/225) usual care: 37.3%
Continued
Group 1: 30.1% (682/2266) Group 2: 28.1% (1654/5893) Group 3: 27.1% (970/3579) Group 4: 28.1% (1026/3650) Group 5: 28.1% (3049/10 867) OR, 95% CI Group 5: 1.00 (referent) Group 4: 1.00 (0.92 to 1.09) Group 3: 0.95 (0.88 to 1.04) Group 2: 1.00 (0.93 to 1.07) Group 1: 1.11 (1.00 to 1.22)
GP provider: 50.3% (N=3657) Hospital: 16.2% (N=3675) RR 3.4; 95% CI 3.13 to 3.70
First RCT Mailing 63.0% (N=1596) Control 56.8% (N=1600) RR=1.11 (95% CI 1.06 to 1.17) Second RCT Mailing 14.6% (N=2107) Control 10.7% (N=2112) RR=1.36 (95% CI 1.16 to 1.60)
Mail group (N=11 490) 52.3% (95% CI 51.3 to 53.2) GP group (N=8052) 27.7% (95% CI 26.7 to 28.6) OR=2.96, 95% CI 2.78 to 3.14
Intervention group: 20.1% (N=2008) Control group: 9.6% (N=1586) OR: 2.1; 95% CI 1.6 to 2.6
Participation
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Recent advances in clinical practice
5
6
Community-based and hospital-based primary care clinics and a tertiary care hospital USA
174 primary care physicians at 14 health centresUSA
Multispecialty group practice USA
General population sample USA
Primary healthcare centre Spain
Health Maintenance Organization Israel
Gupta et al45
Sequist et al57
Sequist et al58
Church et al59
Courtier et al60
Ore et al61
1940 men and women aged 50–74 years, residents of Haifa
2025 subjects aged 50–74 years attending a Primary Health Care centre
Residents aged 50 years or older selected from State Driver’s License and Identification Card database Total sample: N=1943 Estimated eligible participants. N=1394
21 860 subjects overdue for screening
Subjects overdue for screening aged 50–75 years
5970 participants—screening uninsured subjects overdue for CRC screening, age 54–64 years
Participants
Group 1: mailed FOBT kit and information leaflet about CRC risk and importance of early detection Group 2: FOBT kit request and information leaflet about CRC risks and importance of early detection Enabling factors
Group 1: mail invitation letter+2 containers for faecal sample collection Group 2: visit by a trained non-health professional who helped to collect the faecal sample Enabling–reinforcing factors
Group 1: mailing of FOBT kit+educational brochure Group 2: mailing of FOBT kit+educational brochure+phone call reminder Group 3: usual care+screening questionnaire Predisposing–enabling factors
Group 1: educational pamphlet+mailing of FOBT kit with a stamped return envelope+phone number to schedule TC or FS+mail reminder Group 2: usual care Predisposing–enabling factors
Group 1: electronic reminders, educational information, and link for additional information Group 2: usual care Predisposing–enabling factors
FIT outreach: mailed invitation plus FIT kit TC outreach : mailed invitation to schedule free colonoscopy+phone triage to assess TC risk; +bowel prep—mail or pick up+appointment reminders and review of prep 5–7 days prior to TC Both groups included: 1. Invitation letter in English and Spanish 2. Two pre-recorded automated telephone messages 3. Up to 2 ‘live’ telephone follow-up reminders 4. Aid with scheduling and understanding preparation Usual care: visit-based offer to complete screening with gFOBT, TC, barium enema or sigmoidoscopy at the discretion of primary care providers Predisposing–enabling–reinforcing factors
3. An automated telephone and text reminder 2 weeks later for those who did not return the FIT 4. Personal telephone outreach by a CRC screening navigator after 3 months Usual care: computerised reminders, clinic FIT, clinician feedback on CRC screening rates. Predisposing–enabling–reinforcing factors
Intervention vs control
Group 1: 44.0% (N=10 930) Group 2: 38.1% (N=10 930) p
Gut Online First, published on April 8, 2015 as 10.1136/gutjnl-2014-308081 Recent advances in clinical practice
Optimising colorectal cancer screening acceptance: a review Carlo Senore,1 John Inadomi,2 Nereo Segnan,1 Cristina Bellisario,1 Cesare Hassan3 ▸ Additional material is published online only. To view please visit the journal online (http://dx.doi.org/10.1136/ gutjnl-2014-308081). 1
Centro di Prevenzione Oncologica (CPO Piemonte), AOU Città della Salute e della Scienza, Turin, Italy 2 Digestive Disease Center, University of Washington, Seattle, Washington, USA 3 Unit of Gastroenterology, Ospedale Nuovo Regina Margherita, Rome, Italy Correspondence to Dr Carlo Senore, AOU Città della Salute e della Scienza, Centro di Prevenzione Oncologica, Via S Francesco da Paola 31, Turin 10123, Italy; [email protected] Received 27 November 2014 Revised 5 March 2015 Accepted 9 March 2015
ABSTRACT The study aims to review available evidence concerning effective interventions to increase colorectal cancer (CRC) screening acceptance. We performed a literature search of randomised trials designed to increase individuals’ use of CRC screening on PubMed, Embase, Cochrane Database of Systematic Reviews and Database of Abstracts of Reviews of Effects. Small (≤100 subjects per arm) studies and those reporting results of interventions implemented before publication of the large faecal occult blood test trials were excluded. Interventions were categorised following the Continuum of Cancer Care and the PRECEDE–PROCEED models and studies were grouped by screening model (opportunistic vs organised). Multifactor interventions targeting multiple levels of care and considering factors outside the individual clinician control, represent the most effective strategy to enhance CRC screening acceptance. Removing financial barriers, implementing methods allowing a systematic contact of the whole target population, using personal invitation letters, preferably signed by the reference care provider, and reminders mailed to all non-attendees are highly effective in enhancing CRC screening acceptance. Physician reminders may support the diffusion of screening, but they can be effective only for individuals who have access to and make use of healthcare services. Educational interventions for patients and providers are effective, but the implementation of organisational measures may be necessary to favour their impact. Available evidence indicates that organised programmes allow to achieve an extensive coverage and to enhance equity of access, while maximising the health impact of screening. They provide at the same time an infrastructure allowing to achieve a more favourable cost-effectiveness profile of potentially effective strategies, which would not be sustainable in opportunistic settings.
INTRODUCTION
To cite: Senore C, Inadomi J, Segnan N, et al. Gut Published Online First: [please include Day Month Year] doi:10.1136/gutjnl2014-308081
The uptake rate represents a critical determinant of the magnitude of the health impact of colorectal cancer (CRC) screening at the population level. Non-adherence to recommended protocols represents an important attributable factor of CRC mortality,1 particularly among deprived groups. However, in spite of the strong evidence2 3 supporting the screening effectiveness and of a general consensus of guidelines recommending screening of average-risk individuals over age 50,3 4 CRC screening rates remain low. Inequalities in screening use represent an important component of the wide variability observed within and across countries5–9 and may result in higher disease burden, lower
Key messages ▸ Substantial differences in colorectal cancer (CRC) screening use may result in higher disease burden, lower quality of life, health inequities and increased healthcare cost. Non-adherence to recommended protocols represents an important attributable factor in CRC mortality, particularly among lower socio-economic status populations. ▸ Available evidence indicates that multifactor interventions targeting multiple levels and considering factors outside the individual clinician control represent the most effective strategy to enhance CRC screening acceptance, supporting the WHO recommendation to implement population-based organised programmes. ▸ Removing financial barriers, offering all subjects in the target population the option to adhere to high-quality, screening interventions, using personal invitation letters, preferably signed by the reference primary care practitioner, and reminders mailed to all non-attendees, represent a priority for interventions aimed to enhance acceptance of CRC screening. ▸ Physician reminders may represent an additional support to the diffusion of screening in areas with low baseline uptake rates, but in any case they can be effective only for individuals who have access to and make use of healthcare services. ▸ Educational interventions for patients and providers are effective, but the implementation of organisational measures may be necessary to favour their impact. Integrating qualitative research results in the design of educational interventions represents a challenge for future research.
quality of life, increased healthcare costs and health inequities. Screening is a complex process of care consisting of several steps and interfaces between patients, providers and health organisations, which may be promoted, or impeded, at different levels by a range of factors. An extensive literature exists concerning predictors of uptake and the effect of strategies promoting attendance. However, the variability in the screening protocols and the mix of programmatic and non-programmatic delivery systems are limiting the comparability and the transferability of the results. The framework of the quality in the continuum of cancer care model10–12 provides a systematic
Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
1
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Recent advances in clinical practice approach for assessing factors that influence delivery, access and quality of screening. Recognising that cancer care delivery occurs in a multilevel environment (figure 1), this model highlights those levels of the healthcare system representing potential targets for intervention, including policy, practice, provider and patient level. It may therefore offer useful clues to identify potential targets of interventions, to assess their potential reach, as well as the determinants of their success or failure, and to identify directions for further research. Several factors interact in a synergistic manner at these different levels of care to affect provider delivery and patients’ use of screening. The PRECEDE–PROCEED model,13 explaining behavioural change as the result of the interplay of predisposing, enabling and reinforcing factors, represents a useful tool to assess the mechanisms through which these factors can affect screening behaviours. The success of a behavioural intervention requires the identification of the level that must be influenced to achieve an impact and of the optimal strategy to address the relevant factors, which can favour behavioural change. Underuse of CRC screening among uninsured groups can be influenced, for example, by availability of free-of-charge screening programmes funded by national or regional governments, while participation among insured subjects may be enabled by mailing of the faecal occult blood test (FOBT) kit, at the organisational level. These theoretical frameworks (box 1) will be used to examine existing evidence of effectiveness of interventions aimed to enhance use of CRC screening, identifying the level of care and the behavioural mechanisms targeted by each intervention. Taking into account the public health perspective, we also assessed evidence concerning cost-effectiveness of successful interventions (box 2).
METHODS Literature search We searched in first instance recent systematic reviews (SR) and meta-analyses addressing the same topics of our study on PubMed, Embase, Cochrane Database of Systematic Reviews and Database of Abstracts of Reviews of Effects. The search was based on the strategy used in the SR by Jepson et al15 with
appropriate changes according to our inclusion criteria and databases. Relevant original articles published before August 2012 (search update of the most recent review16) were retrieved through already published reviews. We subsequently searched PubMed, Embase and CENTRAL for randomised controlled trials (RCTs), reporting comparative evaluations of interventions, published until 15 October 2014. See online supplementary appendix 1 for the details of the search strategies. We excluded small-size trials (≤100 subjects per arm) and those reports preceding the publication of the European population-based trials17 18 documenting the effectiveness of guaiac FOBT (gFOBT) screening. The findings concerning the impact of interventions conducted when evidence of screening effectiveness was still lacking might not be comparable to those reported from more recent trials, implemented following endorsement of CRC screening by professional societies and governmental institutions. Observational studies were considered when assessing policy options, not easily amenable to testing by RCTs. The outcome of interest in the context of organised programmes was the participation in the first-level screening test, defined as the proportion of invited subjects who underwent the test. In opportunistic settings, the outcome considered was test coverage, defined as the proportion of the target population who had a test within the recommended interval. Interventions have been categorised according to the targeted level of the healthcare system, taking into account the specific behavioural mechanism involved and the screening model (opportunistic vs organised).
RESULTS The SR and meta-analyses literature search yielded 112 papers. These were screened for relevance based on titles and abstracts and 21 of them were judged potentially relevant. Full text could not be acquired for one review19 and 17 of the remaining 20 were included: 716 20–24 considered interventions addressing several levels of care, 610 25–29 were focused on provider, or organisation level, 330–32 on screening modality and 133 on community level.
Figure 1 Levels of intervention related to cancer screening interventions in health service settings.
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Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
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Recent advances in clinical practice Box 1 Conceptual framework The PRECEDE–PROCEED model13 explains behavioural change as the result of the interplay of predisposing factors, providing the rationale, or the motivation, for the behaviour, of factors enabling actual realisation of the decision, and of factors reinforcing individuals’ decision to adopt the desired behaviour and supporting its maintenance over time. Interventions that focus on patient predisposing factors attempt to increase awareness and knowledge of colorectal cancer (CRC) and CRC screening, identify and address health beliefs, or values and fears that impede cancer screening. Interventions focused on patient enabling factors address costs of screening, diagnostic testing and cancer treatment, access to CRC screening and barriers impacting the acceptability of CRC screening. Patient reinforcement interventions may include reminders to complete screening or provide encouragement through peer or professional counselling. Interventions that focus on provider predisposing factors increase knowledge and enhance agreement with clinical practice guidelines for CRC screening, or dispel assumptions about subjects’ health beliefs and likelihood of screening completion. Provider interventions addressing enabling factors include the provision of sufficient time to determine CRC screening eligibility and needs, computer or manual reminders to recommend screening, or sufficient support staff and technology. Interventions of provider reinforcing factors may include the institution of payor requirements, leadership expectations, collegial norms and performance reports.
medical consultations for unrelated conditions, or on the basis of a possible increased CRC risk (family history or other risk factors, including symptoms), or as result of a patient’s request. This approach is defined as opportunistic screening, as opposed to organised screening, where all eligible subjects are actively invited, following an explicit and prespecified protocol stipulating testing and assessment procedures, offered free of charge, within an established organisational context ensuring systematic monitoring of the quality of the whole process.34 CRC screening rates in opportunistic settings differ by type of insurance and are influenced by the amount of patient copayment.35 Individuals without access to primary care are excluded from participation in those settings where most CRC screening relies on office-based interventions delivered by PCP36 and insurance status represents the most important determinant of screening coverage in the USA.37 Policy measures characterising the delivery of screening within organised programmes, including the reduction, or elimination, of costs for the participant and the implementation of a system of patients’ reminders, were identified as the most effective interventions aimed to enhance preventive services use in a comparative analysis of the relative impact of different strategies.38 Higher screening rates, with reduced inequalities across social groups, have been reported in France and Italy, in areas where organised CRC screening programmes had been introduced, as compared to areas where only opportunistic screening was available.39 40 Recent observational studies showed that the introduction of organised screening is associated with a substantial reduction in CRC mortality among populations served by the programmes, as compared with people not routinely invited.41–43
Practice organisation The RCTs literature search yielded 170 papers. These were screened for relevance based on titles and abstracts: 67 were obtained in full text and 44 were included. Reasons for exclusion are reported in online supplementary appendix 1. PRISMA flow charts are reported in online supplementary appendix 1.
Levels targeted by interventions Policy Two main policy options define the context within which screening is currently provided. Screening tests may be recommended by primary care practitioners (PCPs) during routine
Box 2 Directions for future research As long as maintaining subjects’ engagement over several screening rounds following initial attendance is required to ensure screening effectiveness, additional research is needed to identify interventions that can enhance sustained attendance. Qualitative research can offer insights on barriers to screening acceptance, which can be used to tailor educational messages. Integrating findings from qualitative studies into the design of interventions that can be sustainable in the context of large-scale population programmes represents an important aim to be addressed in future studies. Developing valid measures to evaluate the impact of specific interventions on the adoption of decisions consistent with individuals’ values and preferences represents a challenge to be addressed in future studies. Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
Service delivery: According to the results of a recent review,38 establishing separate clinics devoted to screening, involving nursing or clerical staff in the delivery of services and adopting monitoring and quality improvement approaches can have a strong positive impact on screening use. These intervention components characterise the infrastructure of screening delivery within organised programmes. A positive impact of these measures was observed also in opportunistic settings. Staff delivered interventions, designed to identify subjects eligible for screening and to offer counselling about FOBT testing,44 or assistance to fix a TC appointment,45 were associated with an increase in the rates of FOBT and TC screening, in primary care clinics. A survey of family medicine practices reported that those using nurses, or health educators, to provide behavioural counselling were also more likely to show higher screening rates than those not involving staff in counselling activity.46 The introduction of a monitored institutional directive was associated with a significant increase in the screening rates in a managed care setting.47 Invitation: The offer of a pre-fixed appointment in the invitation letter represents an effective strategy to enhance uptake,15 currently adopted in sigmoidoscopy (FS)-based programmes,48 although tested in RCTs only among women invited for breast and cervical cancer screening. Compliance with FS screening was improved by timing invitations in proximity to annual milestones, or invitees’ birthday,49 while having a nurse calling invitees to schedule an appointment was not more effective than offering an open appointment.50 Test delivery (table 1): organised programmes: Mailing of the test kit with instructions, together with the invitation letter, has been adopted in several organised programmes to maximise accessibility. Subjects receiving an invitation including an 3
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Recent advances in clinical practice immunochemical FOBT (faecal immunochemical test (FIT)) kit showed a twofold increase in the likelihood to participate, as compared to subjects receiving an invitation letter with the indication to pick up the kit by their general practitioner (GP), in a population-based programme in Belgium,52 and a more modest, though statistically significant, increase in attendance (30% vs 28%), compared to those receiving the indication to pick up the kit at a pharmacy in an Italian pilot screening study.53 Mailing of FIT kit, compared with the invitation to pick up the kit at a pre-fixed date at a primary clinic, was associated with a statistically significant increase in the screening rates among attendees in previous screening rounds of two Italian population programmes (overall response: 63.0% vs 56.8%).55 Mailing of the gFOBT test kit, as opposed to a simple mail reminder, was associated with an increase from 9.6% to 20.1% in the screening rates among previous non-responders, in a population-based study in Canada,51 while a similar increase was observed only in one centre in the Italian FIT-based programmes.55 Delivery of the kit by the GP, or by non-medical staff, who may provide counselling, enhances acceptance. Completion of FIT and gFOBT was higher among subjects required to pick up the kit at the GP’s office than among those referred to the local hospital.54 Screening activity reports indicated that involvement of trained community volunteers,62 or of pharmacies,63 in the kit distribution is associated with high participation rates, although these options were not tested in comparative trials. Opportunistic setting: Mailing of gFOBT kit, resulting in a modest (4%), but statistically significant, absolute increase in participation of primary care patients, compared with mailing of a kit request card.61 Mailing of the kit emerged as the most effective component of interventions using reminders to enhance screening rates among subjects overdue for screening:57–59 compared with mailing of the kit alone, no additional effect could be observed when adding an educational brochure,58 61 a brochure followed by a follow-up phone call,59 or a web-based educational tool.57 A larger effect on FIT uptake has been observed in studies where mailing of kit was associated with multifaceted outreach interventions, providing multilingual, or low-literacy, educational brochures and using reminder phone calls, both automated and performed by screening navigators.45 56 The potential positive effect of face-to-face interactions is supported by the results of an RCT among primary clinic attendees, showing a higher FIT uptake when a trained non-health professional delivered the kit and collected the sample from participants’ home, as opposed to direct mailing of the kit.60 Screening modality (table 2): Multiple tests70 81 82 have been validated for CRC screening, showing a different effectiveness, acceptability, safety and cost profile. The findings of a recent survey among women who had never participated in CRC, cervical or breast cancer screening programmes83 suggest that although more global barriers, such as cancer fatalism, may explain non-participation in more than one programme, the uptake of CRC screening might be influenced by specific characteristics of recommended options as dislike of the test appears to be a stronger barrier to CRC screening. Differently from clinical practice, where decision-making process mostly depends on test accuracy, acceptance represents a critical factor to orient the choice in screening programmes and in the past 20 years several studies compared the relative uptake of competitive strategies.30 31 Organised programmes with FOBTs have been implemented in several countries,84 with a trend in most recent years favouring the adoption of FIT, as opposed to gFOBT. Despite the choice between the two tests depending on several 4
organisational and economic factors, uptake and effectiveness represent key elements in the decision-making process. The uptake was substantially higher among people invited for FIT than among those offered gFOBT, in two large population-based RCTs in the Netherlands71 85 and in a previous pilot population-based intervention in Italy.67 A large study conducted in the context of an established population programme has confirmed the findings of these pilot RCTs, showing that the adoption of FIT is associated with an increased uptake over gFOBT and that it may also result in a reduction in the participation gap for age, gender and deprivation.79 Screening rates were increased when using FIT as compared to gFOBT also in a US study in a clinic setting,77 but not in an RCT in primary care setting in Israel.78 However, in this latter study, three stool samples—rather than one, as in all previous studies—were required. A recent RCT in a managed care setting showed a lower adherence among people invited to perform a two-sample FIT, or a three-sample gFOBT, as compared to those allocated to a single-sample FIT regimen80 and indeed, the higher compliance achieved when using FIT instead of gFOBT has been explained by the lack of dietary restrictions, the easier and less unpleasant sampling methods and the lower number of samples.54 Inconsistent findings have been reported when comparing FS and faecal tests. Two large Italian population-based RCTs55 86 reported a similar uptake with FIT as with FS, while the attendance rate was substantially higher both with FIT and with gFOBT than with FS in a Dutch population RCT. Compliance was also significantly lower with screening FS than with gFOBT in two average risk population cohorts, in Italy and Sweden,65 68 while another study, conducted in a single UK practice, where the GP was performing FS, reported a higher uptake with FS than with gFOBT.76 FS would appear to be particularly penalised in settings with a high FIT, or gFOBT, adherence, while a low CRC screening uptake would marginalise such difference. Different combinations of FS and faecal tests have been tested to improve screening efficacy or uptake (table 3). The addition of FS to gFOBT was associated with a substantial decrease in the uptake, as compared to gFOBT alone, in three population-based RCTs.65 66 76 A similar trend was observed when adding FS to FIT in a small Australian population RCT69 and in a recent population-based RCT in Norway.73 Offering people the option to choose between FS and FIT did not improve uptake as compared to an invitation for one of the two tests.55 69 Offering FIT to those who refuse FS screening represents an effective alternative approach: the sequential offer of FIT retrieved 19% of those declining FS invitation in an Italian population-based programme and similar findings have been reported in a Dutch pilot screening study.72 The use of colonoscopy (TC) as a primary screening tool has also been advocated, despite the lack of experimental evidence of efficacy. The uptake was lower with TC than with FIT in two large population-based RCTs, in Italy86 and Spain,74 and in a small Australian population study.69 The uptake was higher when offering screening with CT colonography (CTC) than with TC in a Dutch population-based RCT.75 Two studies are ongoing to compare the uptake of CTC and of FS or FIT.98 99
Provider The involvement of GPs was shown to be highly effective in improving compliance, both in the context of organised100 101 and opportunistic screening settings;102 103 prompting subjects invited to seek advice might facilitate GPs’ counselling,104 Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
Senore C, et al. Gut 2015;0:1–20. doi:10.1136/gutjnl-2014-308081
Baker et al56
Community health centresUSA
Pilot screening programme Italy
Segnan et al55
Opportunistic setting
Pilot screening programme Italy
Federici et al54
450 subjects who had prior negative FOBT, underserved, mostly (87%) Latinos
General population sample of 26 682 subjects listed in the National Health Service register
Subjects aged 50 to 69 listed in the rosters of 130 GPs:
First RCT 3196 individuals who had previously participated in CRC screening in the previous round Second RCT 4219 people aged 50–69 years who did not respond to the first invitation
Organised screening programmes in three regions of Central Italy Italy
Giorgi Rossi et al53
Subjects aged 50–74 who had not responded to an invitation in the Colon Cancer Check pilot project 19 542 people aged 50–74 years who had not performed a colonoscopy in the past 10 years
Province-wide CRC screening programme Canada
Participants
Van Roosbroeck et al52 Population-based screening programme for CRC Belgium
Tinmouth et al51
Setting
Interventions targeting organisation of practice
Organised programmes
Reference
Table 1
Participation following the initial or reminder invitation letter
Uptake of gFOBT within 6 months
Outcome
I: usual care plus 1. A mailed reminder letter+a free FIT with low-literacy instructions, and a postage-paid return envelope 2. An automated reminder telephone and text
Group 1: invitation letter+FIT kit with instructions+information leaflet Enabling factors Group 2: invitation letter with instruction to pick up the kit in a pharmacy +information leaflet Predisposing factors Group 3: invitation letter with the offer to choose between FS and FIT +information leaflet Predisposing factors Group 4: invitation letter with prefixed appointment for FS+ information leaflet Enabling factors Group 5: invitation letter with prefixed appointment for FS followed by FIT (negative FS only) +information leaflet Enabling factors Invitation letters signed by the GP Mail reminders for non–responders
GP provider arm: invitation letter signed by the GP, inviting the screenee to pick up and return the FOBT at the GP’s office Hospital arm: invitation letter signed by the GP, inviting the screenee to pick up and return the FOBT at a hospital gastroenterology unit Enabling factors
FIT completion rate
Screening FS or FIT or combination of the two tests
FIT and gFOBT compliance
First RCT Participation in screening Intervention: mailing of FIT kit+invitation letter within 90 days of the mailing Enabling factors Control: invitation letter with instruction to pick up the kit at a primary care clinic Second RCT Intervention: mailing of FIT kit+invitation letter Enabling factors Control: invitation letter with instruction to pick up the kit at a primary care clinic
Mail group: mailing of FIT kit+invitation letter Enabling factors GP group: invitation letter with instructions to pick up the kit by the GP
Intervention group: mailed gFOBT kit+reminder letter Enabling factors Control group: reminder letter
Intervention vs control
Intervention: 82.2% (185/225) usual care: 37.3%
Continued
Group 1: 30.1% (682/2266) Group 2: 28.1% (1654/5893) Group 3: 27.1% (970/3579) Group 4: 28.1% (1026/3650) Group 5: 28.1% (3049/10 867) OR, 95% CI Group 5: 1.00 (referent) Group 4: 1.00 (0.92 to 1.09) Group 3: 0.95 (0.88 to 1.04) Group 2: 1.00 (0.93 to 1.07) Group 1: 1.11 (1.00 to 1.22)
GP provider: 50.3% (N=3657) Hospital: 16.2% (N=3675) RR 3.4; 95% CI 3.13 to 3.70
First RCT Mailing 63.0% (N=1596) Control 56.8% (N=1600) RR=1.11 (95% CI 1.06 to 1.17) Second RCT Mailing 14.6% (N=2107) Control 10.7% (N=2112) RR=1.36 (95% CI 1.16 to 1.60)
Mail group (N=11 490) 52.3% (95% CI 51.3 to 53.2) GP group (N=8052) 27.7% (95% CI 26.7 to 28.6) OR=2.96, 95% CI 2.78 to 3.14
Intervention group: 20.1% (N=2008) Control group: 9.6% (N=1586) OR: 2.1; 95% CI 1.6 to 2.6
Participation
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Recent advances in clinical practice
5
6
Community-based and hospital-based primary care clinics and a tertiary care hospital USA
174 primary care physicians at 14 health centresUSA
Multispecialty group practice USA
General population sample USA
Primary healthcare centre Spain
Health Maintenance Organization Israel
Gupta et al45
Sequist et al57
Sequist et al58
Church et al59
Courtier et al60
Ore et al61
1940 men and women aged 50–74 years, residents of Haifa
2025 subjects aged 50–74 years attending a Primary Health Care centre
Residents aged 50 years or older selected from State Driver’s License and Identification Card database Total sample: N=1943 Estimated eligible participants. N=1394
21 860 subjects overdue for screening
Subjects overdue for screening aged 50–75 years
5970 participants—screening uninsured subjects overdue for CRC screening, age 54–64 years
Participants
Group 1: mailed FOBT kit and information leaflet about CRC risk and importance of early detection Group 2: FOBT kit request and information leaflet about CRC risks and importance of early detection Enabling factors
Group 1: mail invitation letter+2 containers for faecal sample collection Group 2: visit by a trained non-health professional who helped to collect the faecal sample Enabling–reinforcing factors
Group 1: mailing of FOBT kit+educational brochure Group 2: mailing of FOBT kit+educational brochure+phone call reminder Group 3: usual care+screening questionnaire Predisposing–enabling factors
Group 1: educational pamphlet+mailing of FOBT kit with a stamped return envelope+phone number to schedule TC or FS+mail reminder Group 2: usual care Predisposing–enabling factors
Group 1: electronic reminders, educational information, and link for additional information Group 2: usual care Predisposing–enabling factors
FIT outreach: mailed invitation plus FIT kit TC outreach : mailed invitation to schedule free colonoscopy+phone triage to assess TC risk; +bowel prep—mail or pick up+appointment reminders and review of prep 5–7 days prior to TC Both groups included: 1. Invitation letter in English and Spanish 2. Two pre-recorded automated telephone messages 3. Up to 2 ‘live’ telephone follow-up reminders 4. Aid with scheduling and understanding preparation Usual care: visit-based offer to complete screening with gFOBT, TC, barium enema or sigmoidoscopy at the discretion of primary care providers Predisposing–enabling–reinforcing factors
3. An automated telephone and text reminder 2 weeks later for those who did not return the FIT 4. Personal telephone outreach by a CRC screening navigator after 3 months Usual care: computerised reminders, clinic FIT, clinician feedback on CRC screening rates. Predisposing–enabling–reinforcing factors
Intervention vs control
Group 1: 44.0% (N=10 930) Group 2: 38.1% (N=10 930) p
