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How to enhance physician and public acceptance and utilisation of colon cancer screening recommendations
Best Practice & Research Clinical Gastroenterology 24 (2010) 509–520
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Best Practice & Research Clinical Gastroenterology
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How to enhance physician and public acceptance and utilisation of colon cancer screening recommendations Carlo Senore a, *, Nea Malila b,1, Silvia Minozzi c, 2, Paola Armaroli a, 3 a Epidemiologist, AOU S Giovanni Battista – CPO Piemonte, SCDO Epidemiologia dei Tumori 2, Via S Francesco da Paola 31, 10123 Torino, Italy b Finnish Cancer Registry, Director of Mass Screening Registry and Tampere School of Public Health, Tampere, Finland c Epidemiologist, Italian Cochrane Centre, Istituto di ricerche farmacologiche Mario Negri, Milano, Italy
Keywords: Mass screening Colorectal cancer Screening uptake Health promotion
Colorectal Cancer (CRC) screening delivery is a multidisciplinary undertaking, aiming at reducing mortality from and incidence of CRC without adversely affecting the health status of participants. The adoption of a public health perspective involves commitment to ensure equity of access and sustainability of the program over time. We reviewed available evidence concerning predictors of CRC screening uptake and the impact of interventions to improve adoption of screening using conceptual frameworks defining the role of determinants of preventive behaviours and the reach and target of interventions. The results of this review indicate that policy measures aimed at supporting screening delivery, as well as organisational changes, influencing the operational features of preventive services, need to be implemented, in order to allow individual’s motivation to be eventually realised. To ensure coverage and equity of access and to maximise the impact of the intervention, policies aimed at implementing organised programs should be adopted, ensuring that participation in screening and any follow-up assessment should not be limited by financial barriers. Participants and providers beliefs may determine the response to different screening modalities. To achieve the desired health impact, an active follow-up of people with screening abnormalities should be implemented, supported by the
* Corresponding author. Tel.: 39 0116333890; fax: 39 0116333861. E-mail addresses: [email protected] (C. Senore), neamalila@cancer.fi (N. Malila), [email protected] (S. Minozzi), paola. [email protected] (P. Armaroli). 1 Roobertinkatu 9, 00130 Helsinki, Finland. 2 Via Pellicione 5, 54035 Fosdinovo (MS), Italy. Tel./fax: 39 0187693066. 3 Tel.: 39 0116333879; fax: 39 0116333861. 1521-6918/$ – see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.bpg.2010.06.002
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introduction of infrastructural changes and multidisciplinary team work, which can ensure sustainability over time of effective interventions. Continuous monitoring as well as the adoption of plans to evaluate for program effectiveness represent crucial steps in the implementation of a successful program. Ó 2010 Elsevier Ltd. All rights reserved.
Introduction The uptake rate represents a critical determinant of the magnitude of screening impact on colorectal cancer (CRC) incidence and mortality at the population level. In spite of the strong evidence [1–3] supporting the effectiveness of screening for CRC and of a general consensus of guidelines recommending screening of average-risk individuals over age 50,[4] CRC screening rates remain low, although a wide variability of the uptake rates exists within and across countries.[5–7] The observed variability is likely related to differences in the social and cultural background, including individuals’ representation of illness, their knowledge, beliefs and values concerning the role of preventive interventions, their awareness of CRC risk, and the organisation of the health care system. Similarly, the socio-cultural background likely represents a component of the observed effect of the organisational options adopted in different countries. International comparisons may therefore offer a limited contribution to disentangle the relative weight of these determinants and to identify potential targets for interventions. Comparative data from studies conducted in different countries, aimed at assessing the effectiveness of specific interventions in improving uptake beyond the local background rate, may be more informative. An extensive literature exists concerning predictors of uptake and the effect of strategies promoting attendance. Screening utilisation has been associated with factors related to individual’s characteristics, to the knowledge, attitudes and practise of the providers, to the setting and the organisation of the intervention and to the health care delivery system. However, the findings concerning the relative weight of these factors were not always consistent across the studies, making it difficult to interpret their influence in different contexts, or to identify determinants of success or failure of specific interventions. Understanding the reasons for non-participation may give clues about factors that might be the target of specific measures to gain the expected impact. The review will be focused on the identification of the determinants associated with the uptake of CRC and of strategies aimed at enhancing provider and patient utilisation of CRC screening. Concerns have been raised recently about the potential conflict between promoting high uptake rates and the spirit of enabling informed uptake, i.e. enabling people to make an informed choice about whether or not they want to be screened. The purpose of screening should be to benefit the whole community, respecting at the same time individual’s autonomy. Indeed, people may have different risks of contracting the disease based on factors such as age, social class and life style, while some of the harms related to screening are equitably distributed among the screenees.[8] Therefore, making an informed choice about entering screening and adherence to consumer’s chosen option is regarded as a desirable goal.[9] Equity of access to screening should be as important a challenge as is high compliance in screening campaigns. The assessment of the impact of effective interventions to enhance screening rates will therefore take into account both the public health perspective, considering their effect on participation inequalities, and the commitment to enable patient’s informed practise of screening tests. Conceptual framework Given the heterogeneity in the design, socio-cultural context, methodology and target of the interventions, the adoption of a conceptual framework in reviewing available evidence may offer useful clues to interpret findings concerning factors influencing screening practise, the potential reach of the
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interventions and the needs for further research. We will review available evidence concerning predictors of uptake within the framework of the PRECEDE model. The interventions which have been shown to influence uptake will be categorised according to the targeted level of the health care system. Among several models proposed to explain the adoption of health-related behaviours, the PRECEDE framework [10] represents a useful tool, as it takes into account the combined role of cultural, behavioural, economic and organisational factors in influencing screening utilisation. Behavioural change is explained as the result of the interplay of factors providing the rationale or the motivation for the behaviour (predisposing factors, such as knowledge, beliefs, values, attitudes, confidence, capacity), of factors enabling actual realisation of the decision (availability and/or accessibility of health resources, community/government laws, priority, and commitment to health, health-related skills), and of factors sustaining individuals in maintaining the adopted behaviour over time (reinforcing factors such as family, peers, teachers, employers, health providers, community leaders, decision makers). The success of a behavioural intervention is related to the implementation of practise enabling strategies and reinforcing methods, in addition to efforts aimed at modifying predisposing factors. This framework defines therefore a diagnostic approach to health education planning, as the analysis of the role of the determinants of behaviours is related to the design of interventions aimed at promoting change. More recently conceptual frameworks, specifically aimed at characterising the key components and the targets of screening improvement interventions, have been proposed.[11,12] These models conceptualise those levels of the health care system representing potential targets for intervention, including policy (organisational context within which health care is provided), practise (structural and operational features in the specific settings in which screening is recommended and provided), provider and patient level. Specific intervention components may act at several levels, while factors associated with screening uptake are often correlated and interdependent within all four levels. Literature search We searched relevant reviews in the Effective Practice and Organisation of Care (EPOC) Review Group Database-Cochrane library (2000 to December 2009), in MEDLINE and EMBASE (2000 to December 2009). Search strategies were tailored to the relevant databases, and as appropriate used mainly keywords and subject headings (MESH, MEDLINE) or the equivalent translated text words (EMBASE). ‘Explode’ functions were used on all subject headings. We subsequently searched MEDLINE and EMBASE for primary studies, published afterwards the search update of each relevant review, reporting comparative evaluations of different interventions or reports of screening activities in different countries. The search strategy was the following: for MEDLINE: (‘Health Promotion’[Mesh]) AND (‘Mass Screening’[Mesh]) AND (‘Colorectal Neoplasms’[Mesh]); for Embase: exp Colon Tumour/AND exp Cancer Screening/AND exp Health Promotion. Relevant studies published before the time limit of this search were also included. Results Determinants and barriers to participation The organisation of screening delivery within health services, which defines the structural and operational features enabling people to get access to screening services, has been indicated as the main determinant of participation in most countries.[13,14] Lack of funding (e.g. insurance coverage) and cost of the test have been consistently shown to reduce rates of use of preventive services and to influence preferences for specific screening tests.[15] Also, lack of resources likely explains the negative association of lower socio-economic status (SES -measured either by low educational level, indexes of socio-economic deprivation, income or unemployment) with completion of CRC screening tests. Other factors related to service organisation, fairly consistently related to poor screening attendance, are the amount of time required to perform screening and distance from the test provider.[13,14,16] Perceived benefits of screening, as well as perceived risk of CRC were associated with a higher participation in most studies, while lack of confidence in screening effectiveness was associated
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with decreased participation. Anxiety represents a strong negative predictor of engaging in screening, even among those who think screening is effective.[17] Previous participation in CRC screening is significantly associated with the uptake of FOBT,[13] but not of FS screening.[17] Health motivation, measured either by practise of health promoting behaviours (such as having a mammogram, cholesterol check, visits to GP or dentist) or by avoidance of unhealthy life habits (smoking or alcohol consumption) has been identified as a factor associated with a higher likelihood to engage in CRC screening. Being worried about pain, discomfort, or embarrassment associated with the test, or fear about test results were consistently associated with a lower attendance. Conflicting results have been reported concerning the role of family history of CRC.[13,17] Factors related to individual’s culture and beliefs may be responsible of the persisting gradient in the uptake across different geographical areas and socio-economic and ethnic groups still observed also in the context of organised programs with free access to the test.[18–21] The SES gradient may be partially explained by differences in beliefs and expectations [22]: lower social groups may evaluate screening more frightening and less beneficial, even if publicised identically and provided free of charge at a convenient location and time to all social groups. The positive association of marriage with screening uptake is likely explained by the support from a partner in maintaining health oriented behaviours.[23] Support from health care provider plays a strong role. Peoples’ compliance was shown to be closely linked to their practitioner’s motivation.[16,18] Persons’ characteristics, such as poor compliance and lack of knowledge, or low SES, have been shown to be associated with decreased odds of primary care provider (PCP) reported recommendation [24] or of receiving GP advice for CRC screening.[25–28] This would suggest that the SES gradient in uptake may be due to inadequate provider counselling rather than to poor screening acceptance by people. Interventions to promote participation Policy level Two main policy options can be identified to define the context within which screening is currently provided. Screening tests may be recommended by PCPs during routine medical consultations for unrelated conditions, or on the basis of a possible increased risk of developing CRC (family history or other known risk factors), or as result of a patient’s request. This approach is usually defined as opportunistic screening or case finding, as opposed to organised screening, where all eligible subjects are actively invited, following an explicit and pre-specified protocol, defining testing and assessment procedures. According to the International Agency for Research on Cancer (IARC) an organised screening program is characterised by the following features: (1) an explicit policy with specified age categories, method and interval for screening; (2) a defined target population; (3) a management team responsible for implementation; (4) a health-care team for decisions and care; (5) a quality assurance structure; and (6) a method for identifying cancer occurrence and death in the population.[29] Screening tests and the related assessments are usually free of charge for the target population in this context. These key features of organised population based screening programs, have also been identified as the main determinants of the effectiveness of interventions aimed at increasing screening uptake. Available evidence [11] suggests that implementing organisational changes that make delivery of these services a routine part of care, reducing, or eliminating, costs for the participant and establishing a system of patients reminders represent the most effective measures to improve preventive services utilisation. The organisational changes emerging as effective components of successful interventions included establishing separate clinics devoted to screening, use of planned care visits for prevention, involving nursing or clerical staff in the delivery of services, adoption of monitoring and quality improvement approaches. Reduced financial barriers are effective in increasing uptake,[40] particularly among disadvantaged groups.[13,39] Financial incentives to subjects invited for screening were not found to have an impact on participation.[13]
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The adoption of organised programs to enhance screening utilisation is also supported by findings from comparative studies showing that organised screening is more effective and likely more cost-effective than opportunistic screening. Organised programs can ensure a better coverage of the target population, including hard-to-reach and disadvantaged groups, with reduced inequalities in the access to preventive services.[30–33] Compared with opportunistic screening, organised screening resulted in a larger reduction of invasive cervical cancer incidence [34–36] or breast cancer mortality;[37] it also offers much greater attention on the quality of the screening process, including follow-up of participants,[12,38] thus ensuring greater protection against over-screening, poor quality and complications. Organisation – practise level Invitation. There is strong evidence documenting the positive impact of sending a letter signed by the GP on screening uptake, compared to letters from different authority sources,[13,41,42] although individuals may be encouraged to participate by having support by other health care professionals in whom they trust.[23] An advance notification letter may increase participation in FOBT screening.[43] The positive impact on participation of the offer of a pre-fixed appointment, reported by several studies of breast and cervical cancer screening [13,29] was confirmed also among people invited for FS screening.[44] Offering a pre-fixed appointment for FOBT kit delivering has been adopted in some programs, but comparative data on the impact of this strategy are lacking. Available evidence [45] indicates that several kinds of reminders, including letters, postcards, telephone, autodialer or provider delivered face-to-face reminder, are effective, with telephone reminders being most effective, but also most costly. Test delivery. In the context of FOBT screening, mailing of the test kit with instructions, the invitation letter and the information leaflet, has been adopted in several programs to maximise accessibility. Such strategy is effective in increasing participation rates,[46–48] although it may not always represent a cost-effective option, if baseline participation rate and the expected increase in uptake are low.[48] Compared to mailing a second FOBT kit to all non-responders, mailing a recall letter with a test order coupon resulted in a substantial decrease in the program costs, but also in participation.[49] The authors suggested, however, that the spared costs might be allocated more efficiently to communication interventions which might have a higher impact on compliance. When the subject is required to reach health or community facilities to get the kit, easy access to the test provider should be ensured. The involvement of community volunteers, receiving some general training by the program staff, in the kit distribution in the context of ongoing organised programs,[50] were consistently associated with high participation rates As no randomised comparison is available, it is difficult to disentangle their specific effect from other characteristics of the communities involved. Compared to mailing of kit, FOBT uptake was raised when a trained non-health professional, delivered the kit and collected the sample from participant’s home.[51] Sustainability over time represents an important issue to be taken into account when planning the utilisation of support from volunteers. In the context of endoscopy screening, the aim of enhancing accessibility needs to be carefully balanced with the need to maintain high quality performance levels, which can be more likely achieved by centres with high activity volume. Screening modality. Better compliance can be achieved using immunochemical FOBT, compared to guaiac based test.[42,52,53] These results are explained by the lack of dietary and drug restrictions and easier and less unpleasant sampling methods.[54] Four RCTs compared offering FS and FOBT with FOBT alone: three reported a significantly lower uptake among people offered the two tests,[55–57] while no significant difference was observed in the
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other trial.[58] The uptake rate of FS was significantly lower compared to FOBT screening in two comparative trials;[59,60] no difference could be observed in another large population based RCT,[48] while a study conducted in a single UK general practise, where the GP was performing endoscopies, reported a higher uptake with FS than with FOBT screening.[61] The uptake of colonoscopy was significantly lower compared with FS and FIT screening in a comparative trial targeting an average-risk population.[62] The utilisation of different screening tests may be influenced by individuals’ characteristics. Participation was higher among women with FOBT [48,62–64] and among men with endoscopy screening.[48,62] An increased concern about personal risk of developing CRC was found to be associated with a higher likelihood to attend FS invitation, but it showed no influence on FOBT screening uptake.[17] Offering people the option to choose the preferred strategy between FS and FOBT did not increase the overall screening utilisation,[48] although pain-averse patients might prefer to undergo FOBT, while those who value improved accuracy may opt for FS.[17] PCP’s beliefs regarding the characteristics of health care delivery system (inadequate reimbursement, lack of time, absence of skilled clinicians), and the perceived performance of the screening test (too many false positive or false negative), may show a differential impact on the utilisation of screening options: organisational barriers limited FS utilisation, while test performance represented a barrier for FOBT use.[24]
Provider level The primary health care providers (PCP) should be involved in the process of conveying information to people invited for screening. They can be an effective media for improving awareness of the risk of CRC and of the benefits of screening and for increasing confidence in the screening method. Both the GP and other trusted health care professionals [23,64] may support individuals in their decision making process about screening. The involvement of GPs can be very effective in improving compliance, both in the context of organised and opportunistic screening, according to the findings of several studies from different countries.[65–68] GP’s involvement in the decision to undergo screening emerged as the strongest predictor of participation, in particular, for less educated people who were less likely to read the information leaflet.[17] Prompting subjects invited for screening to seek GP’s counselling might facilitate GP’s recommendation.[69] GPs can also advise non-compliers, which is important for older people, or for those with lower socio-economic status, and they can counsel patients with positive tests. To facilitate this task, GPs should receive the results of screening and assessment tests performed by their patients. PCPs referring their patients to other providers instead of performing the procedure themselves were less likely to recommend FS,[24] while higher FS uptake was observed when the GP was performing the exams.[61] Knowledge of GP attitudes and preferences is therefore crucial in enhancing participation. According to the findings of a UK survey [70] GPs need adequate information prior to the commencement of a screening program, focused specifically on the effectiveness of the screening program, the proportion of false negatives, the proportion of false positives, in order to effectively promote screening. The implementation of organisational measures may be necessary to achieve an impact of educational efforts [11]: educational seminars offered to physicians did not show an effect on rates of CRC screening,[71] while a reminder note to the physician to direct his patients to perform a FOBT was more effective than a mail reminder and as affective as a phone reminder for the patients. Some provider associated barriers (i.e. failure to recall patients and assignment of high priority to screening) may be addressed by relatively inexpensive interventions at the level of the organisation of the provider’s office. Reminder systems have been shown to increase the use of preventive services,[11,13,14] while a team approach, involving shifting of some responsibilities from the physician to other health professionals, may enhance screening rates by directly addressing the physician’s lack of time for preventive care.[72]
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Patient level Provision of information is necessary to enable subjects to make an informed choice. Most programs provide written information in the form of leaflets to people invited for screening. Leaflets have been shown to represent an additional valuable tool to the invitation letter, but the content and format of the information material may influence subject’s decision to undertake screening. The potential limitations of this communication tool have been highlighted by a review documenting that leaflets improve knowledge of screening, but may show a lower impact on individual’s attitudes and beliefs.[73] Written communication may also represent a barrier for subjects with low education, who may find it difficult to understand probabilistic estimates of benefits and risks and may have little confidence in relying on written information alone to make health-related decisions.[74] Findings from a recent study suggest that better educated subjects base their decision mainly on the information conveyed in the leaflet, which showed a positive influence on beliefs and attitudes about screening, while those with lower education, who were less likely to report having read the leaflet, tended to rely on GP’s advice.[17] Interventions using visual instruments to enhance appeal and clarity are more effective.[75] Culturally and linguistically appropriate approaches promoting FOBT can enhance screening practise in groups of low-income and less acculturated minority patients.[76] Personalised risk communication may have a small effect on increasing uptake of screening tests.[77] There is however limited evidence that educational interventions can promote informed decision making by the screenees.[13,77] Also, organisational changes, aimed at reducing logistical or economic barriers, may be required to ensure a positive impact of educational interventions. Screening rates showed a significant increase when the GP was delivering a FOBT request form, together with an information pamphlet, while no effect of the leaflet was observed when people interested in screening were requested to actively seek a referral to screening from their providers.[78,79] Offering a free FOBT together with an educational intervention was superior to the educational intervention alone in promoting completion of screening.[40] Available data indicate that promotional campaigns using the media could have a positive impact on health service utilisation, but firm conclusions can not be drawn on CRC screening. However, implementing mass media campaigns, also in the context of organised programs, should also be considered, as they may influence factors, such as individuals’ knowledge, attitudes and beliefs, affecting subjects’ motivation to engage with the proposed screening test.
Dealing with non-compliance to work-up of screening positives The potential reduction of mortality through screening can only be achieved if subjects with abnormal findings receive timely and appropriate follow-up. Treatment and after-care service following evidence based guidelines should be offered to all patients detected with cancer or preinvasive lesions following assessment of abnormal findings. According to a recent US survey less than 15% of health plans monitor receipt of appropriate follow-up care by patents with abnormal results.[15] This lack of organised tracking systems likely explains the low proportion of people with abnormal screening findings who receive adequate follow-up.[80,81] Interventions found to be successful in increasing the proportion of screen positive individuals receiving timely follow-up include [12]: reducing financial barriers for further investigations, mail or telephone reminders and providing written information material or telephone counselling addressing fears related to abnormal findings. Few interventions have been assessed at the practise and provider level. The offer of same-day follow-up for abnormal FS, with on-site colonoscopy,[82] has lead to improved patient’s compliance. Conclusions CRC screening delivery is a multidisciplinary undertaking. The objective is to reduce mortality from and possibly incidence of CRC without adversely affecting the health status of participants. The
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adoption of a public health perspective involves a commitment to ensure equity of access and sustainability of the program over time. An effective program necessitates that screening is free of charge, that the provider offers and the participants accept the test, and that the provider has a system for tracking the results of screening.[83] The provision of screening has to take into account values and preferences of individuals. To achieve this goal educational interventions are necessary to convey relevant and appropriate information to support individual’s informed choice. Moreover, communication efforts targeting individuals invited for screening may contribute to reduce inequalities related to differences of expectations and beliefs across social groups. However, although provision of information is necessary, it may not sufficient to enhance participation. The results of this review indicate that policy measures, as well as organisational changes, need to be implemented, in order to allow the individual’s motivation to be eventually realised. Changes at the policy level may have a wide effect, as they form the context within which screening is delivered. Interventions targeting the practise and provider levels have as well the potential to affect care of many people over a long period of time, as they influence the operational features of the health care settings where preventive services are provided. The introduction of organised programs represents therefore the preferred option to enhance coverage, as they form a context where people’s participation in screening and related assessments is not limited by financial and other barriers. They ensure equity of access, while maximising the health impact of screening. In such context, personal invitation letters, preferably signed by the reference PCP, and reminders mailed to all non-attenders represent effective organisational options. Participants’ and providers’ attitudes and beliefs may determine the response to different screening modalities. Interventions aimed to enhance physician and public acceptance and adoption of CRC screening recommendations require a local assessment of needs and of factors influencing uptake. Continuous monitoring and the adoption of plans to evaluate program effectiveness represent crucial steps in the implementation of a successful program. There should be a national and governmental context for planning of CRC screening, but the GPs and primary care staff commitment and acceptance are crucial to success. Therefore GPs or reference PCPs should be involved both in the implementation of the programs, and in the process of conveying information to people invited for screening. Reducing organisational barriers to PCPs’ advice has been identified as an intervention priority to enhance the impact of their involvement. Screening entails also to ensure that all individuals have timely access to the proper diagnostic and treatment options. Therefore, to achieve the desired health impact, an active follow-up of people with screening abnormalities should be implemented, supported by the introduction of infrastructural changes (computerised systems for tracking and monitoring of screening abnormalities) and multidisciplinary team work, which can ensure sustainability over time of effective interventions.
Directions for future research Available evidence suggests that the proportion of regular attenders in FOBT screening tends to decline over time.[67] Since the effectiveness of FOBT-based programs is dependent on participant’s willingness to repeat testing at regular intervals, additional research is needed to identify predictors of sustained attendance and effective interventions to maintain subject’s engagement over several screening rounds following initial attendance. Intervention studies were mainly focused on evaluating uptake. Information on the impact of specific interventions on informed decision making and on the adoption of decisions consistent with individual’s values and preferences is still sparse. Developing valid measures to evaluate such outcomes and designing studies incorporating these dimensions represents a challenge to be addressed in future studies.
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Practice points The implementation of organised programs represents the preferred option to enhance coverage, while ensuring equity of access and maximising the health impact of screening. The primary health care providers should be involved in the process of conveying information to people invited for screening. Provider related barriers may be effectively addressed by relatively inexpensive interventions (i.e. reminders systems) at the level of the office organisation. Educational interventions targeting people invited for screening are necessary to support individual’s informed choice; they may contribute to reduce inequalities related to differences of expectations and beliefs across social groups. In order to ensure timely access of people with screening abnormalities to the proper diagnostic and treatment options, an active follow-up should be implemented, supported by the introduction of infrastructural changes and multidisciplinary team work.
Research agenda Further research is needed: to identify predictors of sustained attendance and effective interventions to maintain subject’s engagement over several screening rounds; to develop valid methods to assess and to favour informed decision making of people invited for screening.
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[38] Miles A, Cockburn J, Smith RA & Wardle J. A perspective from countries using organized screening programs. Cancer 2004; 101: 1201–1213. [39] Miller MF & Wong JG. Reducing financial barriers enhances the return rate of stool Hemoccult packets. Am J Med Sci 1993; 306: 98–100. [40] Plaskon PP & Fadden MJ. Cancer screening utilization: is there a role for social work in cancer prevention? Soc Work Health Care 1995;21: 59–70. [41] Cole SR, Young GP, Byrne D, Guy JR & Morcom J. Participation in screening for colorectal cancer based on a faecal occult blood test is improved by endorsement by the primary care practitioner. J Med Screen 2002;9: 147–152. [42] Federici A, Giorgi Rossi P, Bartolozzi F, Farchi S, Borgia P & Guasticchi G. Survey on colorectal cancer screening knowledge, attitudes, and practices of general practice physicians in Lazio, Italy. Prev Med 2005;41: 30–35.
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A randomized study. Scand J Gastroenterol 1999;34: 73–78. [57] Berry DP, Clarke P, Hardcastle JD & Vellacott KD. Randomized trial of the addition of flexible sigmoidoscopy to faecal occult blood testing for colorectal neoplasia population screening. Br J Surg 1997;84: 1274–1276. [58] Hoff G, Grotmol T, Skovlund E & Bretthauer M. Risk of colorectal cancer seven years after flexible sigmoidoscopy screening: randomised controlled trial. BMJ 2009;338: b1846. [59] Federici A, Giorgi Rossi P, Borgia P, Bartolozzi F, Farchi S & Gausticchi G. The immunochemical faecal occult blood test leads to higher compliance than the guaiac for colorectal cancer screening programmes: a cluster randomized controlled trial. J Med Screen 2005;12: 83–88. [60] Hol L, van Leerdam ME, van Ballegooijen M, van Vuuren AJ, van Dekken H, Reijerink JCY et al. Screening for colorectal cancer: randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy. Gut 2010;59: 62–68. [61] Verne JE, Aubrey R, Love SB, Talbot IC & Northover JM. Population based randomized study of uptake and yield of screening by flexible sigmoidoscopy compared with screening by faecal occult blood testing. BMJ 1998;317: 182–185. [62] Segnan N, Senore C, Andreoni B, Azzoni A, Bisanti L, Cardelli A et al. Comparing attendance and detection rate of colonoscopy with sigmoidoscopy and FIT for colorectal cancer screening. Gastroenterology 2007;132: 2304–2312. [63] Weller D, Coleman D, Robertson R et al. The UK colorectal cancer screening pilot: results of the second round of screening in England. Br J Cancer 2007;97: 1601–1605. [64] Malila N, Hakama M & Pukkala E. A 25-year follow-up of a population screened with faecal occult blood test in Finland. Acta Oncol 2007;46: 1103–1106. [65] Grazzini G, Castiglione G, Isu A, Mantellini P, Rubeca T, Sani C et al. Colorectal cancer screening by fecal occult blood testing: results of a population-based experience. Tumori 2000;86: 384–388. [66] Seifert B, Zavoral M, Fric P & Bencko V. The role of primary care in colorectal cancer screening: experience from Czech Republic. Neoplasma 2008;55: 74–80. [67] Tazi MA, Faivre J, Dassonville F, Lamour J, Milan C & Durand G. Participation in faecal occult blood screening for colorectal cancer in a well defined French population: results of five screening rounds from 1988 to 1996. J Med Screen 1997;4: 147–151. [68] Sewitch MJ, Fournier C, Dawes M, Yalle M, Snell L, Roper M et al. Do physician recommendations for colorectal cancer screening differ by patient age? Can J Gastroenterol 2007;21: 435–438. [69] Guerra CE, Schwartz JS, Armstrong K, Brown JS, Halbert CH & Shea JA. Barriers of and facilitators to physician recommendation of colorectal cancer screening. J Gen Intern Med 2007;22: 1681–1688. [70] Woodrow C, Rozmovits L, Hewitson P, Rose P, Austoker J & Watson E. Bowel cancer screening in England: a qualitative study of GPs’ attitudes and information needs. BMC Fam Pract 2006;7: 53. [71] Walsh JM, Salazar R, Terdiman JP, Gildengorin G & Perez-Stable EJ. Promoting use of colorectal cancer screening tests. Can we change physician behavior? J Gen Intern Med 2005;20: 1097–1101. [72] Klabunde CN, Lanier D, Breslau ES, Zapka JG, Fletcher RH, Ransohoff DF et al. Improving colorectal cancer screening in primary care practice: invvovative strategies and future directions. JGIM 2007;22: 1195–1205. [73] Fox R. Informed choice in screening programmes: do leaflets help? a critical literature review. J Public Health 2006;28(4): 309–317. [74] Smith AJ. Information leaflets. J Med Screen 1995;2: 3–4. [75] Brotherstone H, Miles A, Robb KA, Atkin W & Wardle J. The impact of illustrations on public understanding of the aim of cancer screening. Patient Educ Couns 2006;63: 328–335. [76] Tu SP, Taylor V, Yasui Y, Chun A, Yip MP, Acorda E et al. 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Contents lists available at ScienceDirect
Best Practice & Research Clinical Gastroenterology
11
How to enhance physician and public acceptance and utilisation of colon cancer screening recommendations Carlo Senore a, *, Nea Malila b,1, Silvia Minozzi c, 2, Paola Armaroli a, 3 a Epidemiologist, AOU S Giovanni Battista – CPO Piemonte, SCDO Epidemiologia dei Tumori 2, Via S Francesco da Paola 31, 10123 Torino, Italy b Finnish Cancer Registry, Director of Mass Screening Registry and Tampere School of Public Health, Tampere, Finland c Epidemiologist, Italian Cochrane Centre, Istituto di ricerche farmacologiche Mario Negri, Milano, Italy
Keywords: Mass screening Colorectal cancer Screening uptake Health promotion
Colorectal Cancer (CRC) screening delivery is a multidisciplinary undertaking, aiming at reducing mortality from and incidence of CRC without adversely affecting the health status of participants. The adoption of a public health perspective involves commitment to ensure equity of access and sustainability of the program over time. We reviewed available evidence concerning predictors of CRC screening uptake and the impact of interventions to improve adoption of screening using conceptual frameworks defining the role of determinants of preventive behaviours and the reach and target of interventions. The results of this review indicate that policy measures aimed at supporting screening delivery, as well as organisational changes, influencing the operational features of preventive services, need to be implemented, in order to allow individual’s motivation to be eventually realised. To ensure coverage and equity of access and to maximise the impact of the intervention, policies aimed at implementing organised programs should be adopted, ensuring that participation in screening and any follow-up assessment should not be limited by financial barriers. Participants and providers beliefs may determine the response to different screening modalities. To achieve the desired health impact, an active follow-up of people with screening abnormalities should be implemented, supported by the
* Corresponding author. Tel.: 39 0116333890; fax: 39 0116333861. E-mail addresses: [email protected] (C. Senore), neamalila@cancer.fi (N. Malila), [email protected] (S. Minozzi), paola. [email protected] (P. Armaroli). 1 Roobertinkatu 9, 00130 Helsinki, Finland. 2 Via Pellicione 5, 54035 Fosdinovo (MS), Italy. Tel./fax: 39 0187693066. 3 Tel.: 39 0116333879; fax: 39 0116333861. 1521-6918/$ – see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.bpg.2010.06.002
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introduction of infrastructural changes and multidisciplinary team work, which can ensure sustainability over time of effective interventions. Continuous monitoring as well as the adoption of plans to evaluate for program effectiveness represent crucial steps in the implementation of a successful program. Ó 2010 Elsevier Ltd. All rights reserved.
Introduction The uptake rate represents a critical determinant of the magnitude of screening impact on colorectal cancer (CRC) incidence and mortality at the population level. In spite of the strong evidence [1–3] supporting the effectiveness of screening for CRC and of a general consensus of guidelines recommending screening of average-risk individuals over age 50,[4] CRC screening rates remain low, although a wide variability of the uptake rates exists within and across countries.[5–7] The observed variability is likely related to differences in the social and cultural background, including individuals’ representation of illness, their knowledge, beliefs and values concerning the role of preventive interventions, their awareness of CRC risk, and the organisation of the health care system. Similarly, the socio-cultural background likely represents a component of the observed effect of the organisational options adopted in different countries. International comparisons may therefore offer a limited contribution to disentangle the relative weight of these determinants and to identify potential targets for interventions. Comparative data from studies conducted in different countries, aimed at assessing the effectiveness of specific interventions in improving uptake beyond the local background rate, may be more informative. An extensive literature exists concerning predictors of uptake and the effect of strategies promoting attendance. Screening utilisation has been associated with factors related to individual’s characteristics, to the knowledge, attitudes and practise of the providers, to the setting and the organisation of the intervention and to the health care delivery system. However, the findings concerning the relative weight of these factors were not always consistent across the studies, making it difficult to interpret their influence in different contexts, or to identify determinants of success or failure of specific interventions. Understanding the reasons for non-participation may give clues about factors that might be the target of specific measures to gain the expected impact. The review will be focused on the identification of the determinants associated with the uptake of CRC and of strategies aimed at enhancing provider and patient utilisation of CRC screening. Concerns have been raised recently about the potential conflict between promoting high uptake rates and the spirit of enabling informed uptake, i.e. enabling people to make an informed choice about whether or not they want to be screened. The purpose of screening should be to benefit the whole community, respecting at the same time individual’s autonomy. Indeed, people may have different risks of contracting the disease based on factors such as age, social class and life style, while some of the harms related to screening are equitably distributed among the screenees.[8] Therefore, making an informed choice about entering screening and adherence to consumer’s chosen option is regarded as a desirable goal.[9] Equity of access to screening should be as important a challenge as is high compliance in screening campaigns. The assessment of the impact of effective interventions to enhance screening rates will therefore take into account both the public health perspective, considering their effect on participation inequalities, and the commitment to enable patient’s informed practise of screening tests. Conceptual framework Given the heterogeneity in the design, socio-cultural context, methodology and target of the interventions, the adoption of a conceptual framework in reviewing available evidence may offer useful clues to interpret findings concerning factors influencing screening practise, the potential reach of the
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interventions and the needs for further research. We will review available evidence concerning predictors of uptake within the framework of the PRECEDE model. The interventions which have been shown to influence uptake will be categorised according to the targeted level of the health care system. Among several models proposed to explain the adoption of health-related behaviours, the PRECEDE framework [10] represents a useful tool, as it takes into account the combined role of cultural, behavioural, economic and organisational factors in influencing screening utilisation. Behavioural change is explained as the result of the interplay of factors providing the rationale or the motivation for the behaviour (predisposing factors, such as knowledge, beliefs, values, attitudes, confidence, capacity), of factors enabling actual realisation of the decision (availability and/or accessibility of health resources, community/government laws, priority, and commitment to health, health-related skills), and of factors sustaining individuals in maintaining the adopted behaviour over time (reinforcing factors such as family, peers, teachers, employers, health providers, community leaders, decision makers). The success of a behavioural intervention is related to the implementation of practise enabling strategies and reinforcing methods, in addition to efforts aimed at modifying predisposing factors. This framework defines therefore a diagnostic approach to health education planning, as the analysis of the role of the determinants of behaviours is related to the design of interventions aimed at promoting change. More recently conceptual frameworks, specifically aimed at characterising the key components and the targets of screening improvement interventions, have been proposed.[11,12] These models conceptualise those levels of the health care system representing potential targets for intervention, including policy (organisational context within which health care is provided), practise (structural and operational features in the specific settings in which screening is recommended and provided), provider and patient level. Specific intervention components may act at several levels, while factors associated with screening uptake are often correlated and interdependent within all four levels. Literature search We searched relevant reviews in the Effective Practice and Organisation of Care (EPOC) Review Group Database-Cochrane library (2000 to December 2009), in MEDLINE and EMBASE (2000 to December 2009). Search strategies were tailored to the relevant databases, and as appropriate used mainly keywords and subject headings (MESH, MEDLINE) or the equivalent translated text words (EMBASE). ‘Explode’ functions were used on all subject headings. We subsequently searched MEDLINE and EMBASE for primary studies, published afterwards the search update of each relevant review, reporting comparative evaluations of different interventions or reports of screening activities in different countries. The search strategy was the following: for MEDLINE: (‘Health Promotion’[Mesh]) AND (‘Mass Screening’[Mesh]) AND (‘Colorectal Neoplasms’[Mesh]); for Embase: exp Colon Tumour/AND exp Cancer Screening/AND exp Health Promotion. Relevant studies published before the time limit of this search were also included. Results Determinants and barriers to participation The organisation of screening delivery within health services, which defines the structural and operational features enabling people to get access to screening services, has been indicated as the main determinant of participation in most countries.[13,14] Lack of funding (e.g. insurance coverage) and cost of the test have been consistently shown to reduce rates of use of preventive services and to influence preferences for specific screening tests.[15] Also, lack of resources likely explains the negative association of lower socio-economic status (SES -measured either by low educational level, indexes of socio-economic deprivation, income or unemployment) with completion of CRC screening tests. Other factors related to service organisation, fairly consistently related to poor screening attendance, are the amount of time required to perform screening and distance from the test provider.[13,14,16] Perceived benefits of screening, as well as perceived risk of CRC were associated with a higher participation in most studies, while lack of confidence in screening effectiveness was associated
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with decreased participation. Anxiety represents a strong negative predictor of engaging in screening, even among those who think screening is effective.[17] Previous participation in CRC screening is significantly associated with the uptake of FOBT,[13] but not of FS screening.[17] Health motivation, measured either by practise of health promoting behaviours (such as having a mammogram, cholesterol check, visits to GP or dentist) or by avoidance of unhealthy life habits (smoking or alcohol consumption) has been identified as a factor associated with a higher likelihood to engage in CRC screening. Being worried about pain, discomfort, or embarrassment associated with the test, or fear about test results were consistently associated with a lower attendance. Conflicting results have been reported concerning the role of family history of CRC.[13,17] Factors related to individual’s culture and beliefs may be responsible of the persisting gradient in the uptake across different geographical areas and socio-economic and ethnic groups still observed also in the context of organised programs with free access to the test.[18–21] The SES gradient may be partially explained by differences in beliefs and expectations [22]: lower social groups may evaluate screening more frightening and less beneficial, even if publicised identically and provided free of charge at a convenient location and time to all social groups. The positive association of marriage with screening uptake is likely explained by the support from a partner in maintaining health oriented behaviours.[23] Support from health care provider plays a strong role. Peoples’ compliance was shown to be closely linked to their practitioner’s motivation.[16,18] Persons’ characteristics, such as poor compliance and lack of knowledge, or low SES, have been shown to be associated with decreased odds of primary care provider (PCP) reported recommendation [24] or of receiving GP advice for CRC screening.[25–28] This would suggest that the SES gradient in uptake may be due to inadequate provider counselling rather than to poor screening acceptance by people. Interventions to promote participation Policy level Two main policy options can be identified to define the context within which screening is currently provided. Screening tests may be recommended by PCPs during routine medical consultations for unrelated conditions, or on the basis of a possible increased risk of developing CRC (family history or other known risk factors), or as result of a patient’s request. This approach is usually defined as opportunistic screening or case finding, as opposed to organised screening, where all eligible subjects are actively invited, following an explicit and pre-specified protocol, defining testing and assessment procedures. According to the International Agency for Research on Cancer (IARC) an organised screening program is characterised by the following features: (1) an explicit policy with specified age categories, method and interval for screening; (2) a defined target population; (3) a management team responsible for implementation; (4) a health-care team for decisions and care; (5) a quality assurance structure; and (6) a method for identifying cancer occurrence and death in the population.[29] Screening tests and the related assessments are usually free of charge for the target population in this context. These key features of organised population based screening programs, have also been identified as the main determinants of the effectiveness of interventions aimed at increasing screening uptake. Available evidence [11] suggests that implementing organisational changes that make delivery of these services a routine part of care, reducing, or eliminating, costs for the participant and establishing a system of patients reminders represent the most effective measures to improve preventive services utilisation. The organisational changes emerging as effective components of successful interventions included establishing separate clinics devoted to screening, use of planned care visits for prevention, involving nursing or clerical staff in the delivery of services, adoption of monitoring and quality improvement approaches. Reduced financial barriers are effective in increasing uptake,[40] particularly among disadvantaged groups.[13,39] Financial incentives to subjects invited for screening were not found to have an impact on participation.[13]
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The adoption of organised programs to enhance screening utilisation is also supported by findings from comparative studies showing that organised screening is more effective and likely more cost-effective than opportunistic screening. Organised programs can ensure a better coverage of the target population, including hard-to-reach and disadvantaged groups, with reduced inequalities in the access to preventive services.[30–33] Compared with opportunistic screening, organised screening resulted in a larger reduction of invasive cervical cancer incidence [34–36] or breast cancer mortality;[37] it also offers much greater attention on the quality of the screening process, including follow-up of participants,[12,38] thus ensuring greater protection against over-screening, poor quality and complications. Organisation – practise level Invitation. There is strong evidence documenting the positive impact of sending a letter signed by the GP on screening uptake, compared to letters from different authority sources,[13,41,42] although individuals may be encouraged to participate by having support by other health care professionals in whom they trust.[23] An advance notification letter may increase participation in FOBT screening.[43] The positive impact on participation of the offer of a pre-fixed appointment, reported by several studies of breast and cervical cancer screening [13,29] was confirmed also among people invited for FS screening.[44] Offering a pre-fixed appointment for FOBT kit delivering has been adopted in some programs, but comparative data on the impact of this strategy are lacking. Available evidence [45] indicates that several kinds of reminders, including letters, postcards, telephone, autodialer or provider delivered face-to-face reminder, are effective, with telephone reminders being most effective, but also most costly. Test delivery. In the context of FOBT screening, mailing of the test kit with instructions, the invitation letter and the information leaflet, has been adopted in several programs to maximise accessibility. Such strategy is effective in increasing participation rates,[46–48] although it may not always represent a cost-effective option, if baseline participation rate and the expected increase in uptake are low.[48] Compared to mailing a second FOBT kit to all non-responders, mailing a recall letter with a test order coupon resulted in a substantial decrease in the program costs, but also in participation.[49] The authors suggested, however, that the spared costs might be allocated more efficiently to communication interventions which might have a higher impact on compliance. When the subject is required to reach health or community facilities to get the kit, easy access to the test provider should be ensured. The involvement of community volunteers, receiving some general training by the program staff, in the kit distribution in the context of ongoing organised programs,[50] were consistently associated with high participation rates As no randomised comparison is available, it is difficult to disentangle their specific effect from other characteristics of the communities involved. Compared to mailing of kit, FOBT uptake was raised when a trained non-health professional, delivered the kit and collected the sample from participant’s home.[51] Sustainability over time represents an important issue to be taken into account when planning the utilisation of support from volunteers. In the context of endoscopy screening, the aim of enhancing accessibility needs to be carefully balanced with the need to maintain high quality performance levels, which can be more likely achieved by centres with high activity volume. Screening modality. Better compliance can be achieved using immunochemical FOBT, compared to guaiac based test.[42,52,53] These results are explained by the lack of dietary and drug restrictions and easier and less unpleasant sampling methods.[54] Four RCTs compared offering FS and FOBT with FOBT alone: three reported a significantly lower uptake among people offered the two tests,[55–57] while no significant difference was observed in the
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other trial.[58] The uptake rate of FS was significantly lower compared to FOBT screening in two comparative trials;[59,60] no difference could be observed in another large population based RCT,[48] while a study conducted in a single UK general practise, where the GP was performing endoscopies, reported a higher uptake with FS than with FOBT screening.[61] The uptake of colonoscopy was significantly lower compared with FS and FIT screening in a comparative trial targeting an average-risk population.[62] The utilisation of different screening tests may be influenced by individuals’ characteristics. Participation was higher among women with FOBT [48,62–64] and among men with endoscopy screening.[48,62] An increased concern about personal risk of developing CRC was found to be associated with a higher likelihood to attend FS invitation, but it showed no influence on FOBT screening uptake.[17] Offering people the option to choose the preferred strategy between FS and FOBT did not increase the overall screening utilisation,[48] although pain-averse patients might prefer to undergo FOBT, while those who value improved accuracy may opt for FS.[17] PCP’s beliefs regarding the characteristics of health care delivery system (inadequate reimbursement, lack of time, absence of skilled clinicians), and the perceived performance of the screening test (too many false positive or false negative), may show a differential impact on the utilisation of screening options: organisational barriers limited FS utilisation, while test performance represented a barrier for FOBT use.[24]
Provider level The primary health care providers (PCP) should be involved in the process of conveying information to people invited for screening. They can be an effective media for improving awareness of the risk of CRC and of the benefits of screening and for increasing confidence in the screening method. Both the GP and other trusted health care professionals [23,64] may support individuals in their decision making process about screening. The involvement of GPs can be very effective in improving compliance, both in the context of organised and opportunistic screening, according to the findings of several studies from different countries.[65–68] GP’s involvement in the decision to undergo screening emerged as the strongest predictor of participation, in particular, for less educated people who were less likely to read the information leaflet.[17] Prompting subjects invited for screening to seek GP’s counselling might facilitate GP’s recommendation.[69] GPs can also advise non-compliers, which is important for older people, or for those with lower socio-economic status, and they can counsel patients with positive tests. To facilitate this task, GPs should receive the results of screening and assessment tests performed by their patients. PCPs referring their patients to other providers instead of performing the procedure themselves were less likely to recommend FS,[24] while higher FS uptake was observed when the GP was performing the exams.[61] Knowledge of GP attitudes and preferences is therefore crucial in enhancing participation. According to the findings of a UK survey [70] GPs need adequate information prior to the commencement of a screening program, focused specifically on the effectiveness of the screening program, the proportion of false negatives, the proportion of false positives, in order to effectively promote screening. The implementation of organisational measures may be necessary to achieve an impact of educational efforts [11]: educational seminars offered to physicians did not show an effect on rates of CRC screening,[71] while a reminder note to the physician to direct his patients to perform a FOBT was more effective than a mail reminder and as affective as a phone reminder for the patients. Some provider associated barriers (i.e. failure to recall patients and assignment of high priority to screening) may be addressed by relatively inexpensive interventions at the level of the organisation of the provider’s office. Reminder systems have been shown to increase the use of preventive services,[11,13,14] while a team approach, involving shifting of some responsibilities from the physician to other health professionals, may enhance screening rates by directly addressing the physician’s lack of time for preventive care.[72]
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Patient level Provision of information is necessary to enable subjects to make an informed choice. Most programs provide written information in the form of leaflets to people invited for screening. Leaflets have been shown to represent an additional valuable tool to the invitation letter, but the content and format of the information material may influence subject’s decision to undertake screening. The potential limitations of this communication tool have been highlighted by a review documenting that leaflets improve knowledge of screening, but may show a lower impact on individual’s attitudes and beliefs.[73] Written communication may also represent a barrier for subjects with low education, who may find it difficult to understand probabilistic estimates of benefits and risks and may have little confidence in relying on written information alone to make health-related decisions.[74] Findings from a recent study suggest that better educated subjects base their decision mainly on the information conveyed in the leaflet, which showed a positive influence on beliefs and attitudes about screening, while those with lower education, who were less likely to report having read the leaflet, tended to rely on GP’s advice.[17] Interventions using visual instruments to enhance appeal and clarity are more effective.[75] Culturally and linguistically appropriate approaches promoting FOBT can enhance screening practise in groups of low-income and less acculturated minority patients.[76] Personalised risk communication may have a small effect on increasing uptake of screening tests.[77] There is however limited evidence that educational interventions can promote informed decision making by the screenees.[13,77] Also, organisational changes, aimed at reducing logistical or economic barriers, may be required to ensure a positive impact of educational interventions. Screening rates showed a significant increase when the GP was delivering a FOBT request form, together with an information pamphlet, while no effect of the leaflet was observed when people interested in screening were requested to actively seek a referral to screening from their providers.[78,79] Offering a free FOBT together with an educational intervention was superior to the educational intervention alone in promoting completion of screening.[40] Available data indicate that promotional campaigns using the media could have a positive impact on health service utilisation, but firm conclusions can not be drawn on CRC screening. However, implementing mass media campaigns, also in the context of organised programs, should also be considered, as they may influence factors, such as individuals’ knowledge, attitudes and beliefs, affecting subjects’ motivation to engage with the proposed screening test.
Dealing with non-compliance to work-up of screening positives The potential reduction of mortality through screening can only be achieved if subjects with abnormal findings receive timely and appropriate follow-up. Treatment and after-care service following evidence based guidelines should be offered to all patients detected with cancer or preinvasive lesions following assessment of abnormal findings. According to a recent US survey less than 15% of health plans monitor receipt of appropriate follow-up care by patents with abnormal results.[15] This lack of organised tracking systems likely explains the low proportion of people with abnormal screening findings who receive adequate follow-up.[80,81] Interventions found to be successful in increasing the proportion of screen positive individuals receiving timely follow-up include [12]: reducing financial barriers for further investigations, mail or telephone reminders and providing written information material or telephone counselling addressing fears related to abnormal findings. Few interventions have been assessed at the practise and provider level. The offer of same-day follow-up for abnormal FS, with on-site colonoscopy,[82] has lead to improved patient’s compliance. Conclusions CRC screening delivery is a multidisciplinary undertaking. The objective is to reduce mortality from and possibly incidence of CRC without adversely affecting the health status of participants. The
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adoption of a public health perspective involves a commitment to ensure equity of access and sustainability of the program over time. An effective program necessitates that screening is free of charge, that the provider offers and the participants accept the test, and that the provider has a system for tracking the results of screening.[83] The provision of screening has to take into account values and preferences of individuals. To achieve this goal educational interventions are necessary to convey relevant and appropriate information to support individual’s informed choice. Moreover, communication efforts targeting individuals invited for screening may contribute to reduce inequalities related to differences of expectations and beliefs across social groups. However, although provision of information is necessary, it may not sufficient to enhance participation. The results of this review indicate that policy measures, as well as organisational changes, need to be implemented, in order to allow the individual’s motivation to be eventually realised. Changes at the policy level may have a wide effect, as they form the context within which screening is delivered. Interventions targeting the practise and provider levels have as well the potential to affect care of many people over a long period of time, as they influence the operational features of the health care settings where preventive services are provided. The introduction of organised programs represents therefore the preferred option to enhance coverage, as they form a context where people’s participation in screening and related assessments is not limited by financial and other barriers. They ensure equity of access, while maximising the health impact of screening. In such context, personal invitation letters, preferably signed by the reference PCP, and reminders mailed to all non-attenders represent effective organisational options. Participants’ and providers’ attitudes and beliefs may determine the response to different screening modalities. Interventions aimed to enhance physician and public acceptance and adoption of CRC screening recommendations require a local assessment of needs and of factors influencing uptake. Continuous monitoring and the adoption of plans to evaluate program effectiveness represent crucial steps in the implementation of a successful program. There should be a national and governmental context for planning of CRC screening, but the GPs and primary care staff commitment and acceptance are crucial to success. Therefore GPs or reference PCPs should be involved both in the implementation of the programs, and in the process of conveying information to people invited for screening. Reducing organisational barriers to PCPs’ advice has been identified as an intervention priority to enhance the impact of their involvement. Screening entails also to ensure that all individuals have timely access to the proper diagnostic and treatment options. Therefore, to achieve the desired health impact, an active follow-up of people with screening abnormalities should be implemented, supported by the introduction of infrastructural changes (computerised systems for tracking and monitoring of screening abnormalities) and multidisciplinary team work, which can ensure sustainability over time of effective interventions.
Directions for future research Available evidence suggests that the proportion of regular attenders in FOBT screening tends to decline over time.[67] Since the effectiveness of FOBT-based programs is dependent on participant’s willingness to repeat testing at regular intervals, additional research is needed to identify predictors of sustained attendance and effective interventions to maintain subject’s engagement over several screening rounds following initial attendance. Intervention studies were mainly focused on evaluating uptake. Information on the impact of specific interventions on informed decision making and on the adoption of decisions consistent with individual’s values and preferences is still sparse. Developing valid measures to evaluate such outcomes and designing studies incorporating these dimensions represents a challenge to be addressed in future studies.
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Practice points The implementation of organised programs represents the preferred option to enhance coverage, while ensuring equity of access and maximising the health impact of screening. The primary health care providers should be involved in the process of conveying information to people invited for screening. Provider related barriers may be effectively addressed by relatively inexpensive interventions (i.e. reminders systems) at the level of the office organisation. Educational interventions targeting people invited for screening are necessary to support individual’s informed choice; they may contribute to reduce inequalities related to differences of expectations and beliefs across social groups. In order to ensure timely access of people with screening abnormalities to the proper diagnostic and treatment options, an active follow-up should be implemented, supported by the introduction of infrastructural changes and multidisciplinary team work.
Research agenda Further research is needed: to identify predictors of sustained attendance and effective interventions to maintain subject’s engagement over several screening rounds; to develop valid methods to assess and to favour informed decision making of people invited for screening.
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