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A pivotal role for the general practitioner in a mixed mammographic screening model
Revue d’Épidémiologie et de Santé Publique 60 (2012) 150–156
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ORIGINAL ARTICLE
A pivotal role for the general practitioner in a mixed mammographic screening model Un rôle crucial pour le médecin généraliste dans un modèle mixte de dépistage du cancer du sein G. François, S. Van Roosbroeck, S. Hoeck, E. Markovskaia, G. Van Hal * Department of Epidemiology and Social Medicine – Medical Sociology and Health Policy, Campus Drie Eiken, University of Antwerp, 1, 2610 Antwerp, Belgium Received 27 February 2009; accepted 7 September 2011
Abstract Background. – A mixed mammographic screening model presents a country or region with a complex problem. Promoting a significant shift within the target population from opportunistic breast cancer screening to participation in an organised screening programme offers many advantages. The objective was to explore the role of GPs as potential mediators by assessing their specific knowledge, attitudes, and experience on breast cancer and mammographic screening. Methods. – A detailed questionnaire was mailed in 2007 to 1500 GPs randomly sampled from the GP population in the province of Antwerp, Belgium. Levels of knowledge on epidemiology and screening, opinions and attitudes on systematic mammographic screening, and experience with breast cancer and mammography were evaluated. Results. – We received 317 completed questionnaires, 21.1% of the contacted GPs. General knowledge on basic concepts of mammographic screening was average, while the response to an open question on the differences between screening and opportunistic mammography was very limited. More than half of the participants had a positive or realistic attitude towards many aspects of systematic screening, and had satisfactory experience with breast cancer patients in their daily practice (about 82% saw one to four new cases a year). Many (72%) were favourably disposed towards systematic screening organised by the government. Conclusion. – The answers of the GPs suggest a promising potential with regard to the official breast cancer screening programme. Many participants presented qualifications, which could contribute to a change from the mixed model in favour of the official screening system. A number of gaps, however, need to be filled and there is a continuing need to educate physicians on principles and risks and benefits of systematic screening of the target group. ß 2012 Elsevier Masson SAS. All rights reserved. Résumé Position du problème. – Un modèle mixte de dépistage du cancer du sein place un pays ou une région devant un problème complexe. Promouvoir un changement important au sein de la population-cible du dépistage du cancer du sein opportuniste vers la participation à un programme de dépistage organisé offre de nombreux avantages. L’objectif était d’explorer le rôle des médecins généralistes comme des médiateurs en évaluant leurs connaissances, leurs attitudes et leur expérience sur le cancer du sein et la mammographie. Méthodes. – Un questionnaire détaillé a été envoyé en 2007 à 1500 médecins généralistes échantillonnés au hasard à partir de la population généraliste dans la province d’Anvers en Belgique. Le niveau des connaissances sur l’épidémiologie et le dépistage du cancer du sein, les opinions et les attitudes sur le dépistage systématique, et l’expérience avec le cancer du sein et la mammographie ont été évalués.
* Corresponding author. E-mail address: [email protected] (G. Van Hal). 0398-7620/$ see front matter ß 2012 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.respe.2011.09.008
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Résultats. – Nous avons reçu 317 questionnaires renseignés, soit un taux de réponse de 21,1 % du total des médecins généralistes contactés. Les connaissances générales sur les concepts de base du dépistage par mammographie sont moyennes, tandis que la réponse à une question ouverte sur les différences entre le dépistage opportuniste et le dépistage systématique était très limitée. Plus de la moitié des participants ont une attitude positive ou réaliste à l’égard de beaucoup d’aspects du dépistage systématique et ont une expérience satisfaisante avec le cancer du sein dans leur pratique quotidienne (environ 82 % voient un à quatre nouveaux cas par an). Beaucoup d’entre eux (72 %) sont favorables à un dépistage systématique organisé par le gouvernement. Conclusion. – Les réponses des médecins généralistes révèlent un potentiel prometteur en ce qui concerne le programme de dépistage du cancer du sein officiel. Beaucoup de participants semblent être compétents à modifier l’équilibre du modèle mixte en faveur du système officiel. Un certain nombre de lacunes, cependant, doivent être comblées et il faut continuer à éduquer les médecins sur les principes et les risques et avantages d’un dépistage systématique de la population-cible. ß 2012 Elsevier Masson SAS. Tous droits réservés. Keywords: Breast cancer; Organised screening; Opportunistic screening; Participation; General practitioner; Knowledge; Attitude; Practice Mots clés : Cancer du sein ; Dépistage organisé ; Dépistage opportuniste ; Médecin généraliste ; Connaissance ; Attitude ; Pratique
1. INTRODUCTION Breast cancer is, worldwide, the most common tumour affecting women and exerts a huge annual toll. The most affluent societies run the greatest risk, with incidence rates over 80 per 100,000 and globally nearly 580,000 new annual cases [1]. In Flanders, 5374 women were diagnosed with breast cancer in 2004, representing 34.2% of the total of invasive tumours in women. In 2000–2001, age-standardised incidence rates for invasive breast cancer in Flanders ranked among the highest in Europe [2,3]. Cancer screening implies pursuing early diagnosis in asymptomatic persons and is justified in terms of the presumed utility of early relative to late diagnosis. Mammographic screening, e.g., contributes to preventing progression of breast cancer and its complications by early intervention [4,5]. Breast cancer meets all ten criteria as proposed by the WHO to make it suitable for screening [6,7]. Breast cancer screening takes place in all Belgian Regions. The complex national healthcare system proved to be an important obstacle for full implementation of the European Guidelines [8] and therefore, some deviations were allowed. In Flanders, the official screening programme was introduced on June 15, 2001. Before that date, Flemish women could undergo a mammography, but this was only possible on an ‘‘individual’’ or ‘‘opportunistic’’ basis. From June 15, 2001 on, ‘‘individual’’/ ‘‘opportunistic’’ mammography and the official screening programme kept on coexisting. This complicated situation is the essence of the current mixed mammographic screening model. In the official programme, women aged 50–69 are twoyearly invited for a screening mammography. Invitation occurs through their GP (this is called Track 1) or by one of the official screening centres (this is called Track 2). Flanders has five screening centres (Antwerp, Bruges, Brussels, Ghent, Leuven). In addition to this official programme, as mentioned above, each woman is free to turn to a radiologist on a private basis for an ‘‘individual’’ or ‘‘opportunistic’’ mammography. The latter procedure takes place beyond the scope of the official
screening programme. In this case the involved woman usually annually undergoes a mammography and also an ultrasonographic breast examination. The official breast cancer screening programme has numerous advantages in comparison with the opportunistic way. These comprise: guaranteed, monitored high-quality mammography; continual quality control of programme, technical equipment, and performance of radiologists; registration of participation and follow-up; automatic re-invitation; lessons learned in terms of future campaigns; a free mammography; and a saving in public expenditures. Because of these reasons it is desirable that as many women as possible making part of the target population make the change-over from non-official opportunistic screening to participation in the official screening programme. Participation in the official breast cancer screening programme in Flanders amounts to on average ca 48% of the target group. One health target of the Flemish Government is to increase this figure to at least 75% by 2012 [9]. This gap can potentially and at least partially be filled if women now undergoing opportunistic screening (about 20% of the target population) can be convinced to switch to the official programme. GPs are in a favourable position to transmit the advantages of this step. To explore knowledge, attitudes, and experience of those functioning in a mammographic model wherein individual and organised screening coexist, we mailed a questionnaire to regional GPs, to sound out both their personal views and criticism on breast cancer screening. 2. METHODS 2.1. Sampling From the total population of GPs in the Province of Antwerp (Flemish Region), i.e. 2600 persons, 1500 (58%) were randomly selected and included as potential participants in the study. Stratification based on the degree of urbanisation was not considered, because the population density is very high
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(568 km 2) and clear-cut differences between urban, semirural, and rural communities do not apply.
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2.2. Survey A questionnaire (36 items) on knowledge, attitudes, own practice, and views on breast cancer and screening was sent in 2007 to the GPs by surface mail, accompanied with a cover letter and a stamped addressed envelope. Participants were asked to send their response within four weeks after receipt. Knowledge and attitude questions were mainly inspired by the literature, recommendations on prevention, newsletters for GPs, and private discussions with GPs. Attitudes towards screening mammography were evaluated by considering that answering ‘‘I agree’’ to this category of questions implied a positive, realistic, or negative attitude, depending on the case. Respondents’ practical experiences were considered in the context of numbers of cases in their practice, numbers of ‘‘longstanding’’ breast cancer patients, and false-positive and negative screening results. A number of questions were open, but most of them were multiple-choice questions. There was room for additional remarks, considerations, and suggestions. Participants were given the opportunity to express their personal views and criticism on breast cancer screening, together with their wishes and considerations. A limited number of personal details (gender, age category, year of graduation, type of practice, work pressure) were asked as well. The questionnaire was pre-tested before actual use. 2.3. Statistical analysis Descriptive statistics were used to summarize the main characteristics of the data set, particularly the specific knowledge, attitudes, and experiences on breast cancer and mammographic screening of the participants. Pearson Chi2 tests were performed (SPSS version 18.0) to test the association between participation/non-participation and gender, graduation year, and proportion of solo practices. Answers to open questions were repeatedly read in order to maintain a holistic view on the comments on the screening system. A highlighting approach was applied to gain insight in the essential themes and patterns, which were subsequently isolated from the responses and then clustered into core themes. This
procedure was independently performed by two investigators, to validate the analysis. 3. RESULTS 3.1. Participants We received 317 completed questionnaires, implying a response rate of 21.1%; 13 were not considered because they concerned physicians no longer active as GPs. Among the remaining 304, about one third was women. All age categories (25–65) were covered and all types of practice (individual, shared, or group practice) were represented. Participants’ pressure of work, expressed as number of visits per week, was as follows: 11.2% saw 20–50 patients, 42.4% saw 51–100 patients, 29.6% saw 101–150 patients, and 15.8% saw over 150 patients a week. Year of graduation was similar among participants and non-participants (1970 or earlier: 8.6 vs. 11.5%; 1971–1980: 25.3 vs. 27.1%; 1981–1990: 34.9 vs. 31.4%; 1991–2000: 24.0 vs. 23.4%; 2001 or later: 5.6 vs. 6.8%; p = 0.455). On the other hand, gender distribution (males: 62.2 vs. 69.7%; p = 0.011) and the proportion of solo practices were not alike in both populations (57.6 vs. 82.8%; p < 0.001).
3.2. Knowledge General questions on preventive medicine and breast cancer screening were answered as summarized in Table 1. Almost all (94.1%) knew that screening mammography does not yield a certainty diagnosis and 82.9% knew that hormone replacement therapy (HRT) increases the prevalence of breast cancer. All other questions were answered correctly by 48–69% of participants. The response to the open question ‘‘Please describe the differences between screening and opportunistic mammography’’ was limited. About one third (31.3%) of all participants did not answer the question or were not able to describe any differences. The majority of those that did respond delivered only fragmentary answers, meaning that only few of them were able to give an overview of all differences. Participants were then asked to indicate those types of cancer that meet the Wilson and Jungner criteria [6] and the European Guidelines [8] for mass screening. They could choose from a list of eight types
Table 1 General level of knowledge of participants on definitions and basic concepts of mammographic screening. Subject of the question
Correct answer n (%)
Incorrect answer n (%)
No answer n (%)
Definition of sensitivity Definition of specificity Dependency of sensitivity and specificity on age Definition of certainty diagnosis Which type of prevention is screening mammography? Effect of HRT on breast cancer prevalence Effect of breast cancer prevalence on predictive value of mammography
210 145 176 286 208 252 179
75 134 106 13 84 39 95
19 25 21 5 12 13 30
HRT: hormone replacement therapy.
(69.1) (47.7) (58.1) (94.1) (68.4) (82.9) (58.9)
(24.7) (44.1) (35.0) (4.3) (27.6) (12.8) (31.3)
(6.3) (8.2) (6.9) (1.6) (3.9) (4.3) (9.9)
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Thesis
Agree n (%)
Disagree n (%)
No opinion n (%)
Screening mammography is physically and/or mentally traumatising for womena Mammography is useful as a relatively simple and rapid tool for mass screeningb Screening mammography yields too many false-positive resultsa,c False-positive results often lead to unwanted reactions such as fear, uncertainty, and depressionc False-positive results frequently lead to breast amputationa False-negative results unfavourably affect the process of treatment and counsellingc Screening mammography was introduced in Belgium mainly for economic reasonsa Screening for breast cancer will lead to a decrease in cause-specific mortality in the long runb The cause-specific mortality is equal in screened and non-screened populationsa A screening mammography uptake of 75% is currently attainable in Flanders, Belgiumb I feel involved in the breast cancer screening programme in Flanders, Belgiumb
30 257 63 210 6 195 38 250 17 143 211
237 15 157 45 281 51 166 14 214 76 22
37 32 84 46 17 57 99 40 68 84 61
a b c
(9.9) (84.5) (20.7) (69.7) (2.0) (64.4) (12.5) (82.2) (5.7) (47.2) (71.8)
(78.0) (4.9) (51.6) (15.0) (92.4) (16.8) (54.8) (4.6) (71.6) (25.1) (7.5)
(12.2) (10.5) (27.6) (15.3) (5.6) (18.8) (32.7) (13.2) (22.7) (27.7) (20.7)
Answering ‘‘I agree’’ to this question was considered a negative attitude. Answering ‘‘I agree’’ to this question was considered a positive attitude. Answering ‘‘I agree’’ to this question was considered a realistic attitude.
of cancer (breast, prostate, cervical, colorectal, ovarian, and lung carcinoma, melanoma, and non-Hodgkin lymphoma). Of all respondents, 72.7% were able to answer this question correctly. 3.3. Attitude The position of participants vis-à-vis some fundamental theses on screening mammography is displayed in Table 2. Most answers reflected a positive or realistic attitude. The first type is exemplified by responding to, e.g., ‘‘Mammography is useful as a relatively simple and rapid tool for mass screening’’ or ‘‘A screening mammography uptake of 75% is currently attainable in Flanders, Belgium’’ with ‘‘I agree’’. Commenting to, e.g., ‘‘False-negative results unfavourably affect the process of treatment and counselling’’ with ‘‘I agree’’ was considered as the result of a realistic attitude. In all considered cases, these two types of attitudes appeared to be more widespread among the respondents than a negative or unrealistic attitude, or having no opinion. Both pros and cons of participation are discussed with the involved women by 178 (59.5%) of the GPs; 108 (36.1%) inform them mainly on the advantages and only 13 (4.3%) mainly on the disadvantages. This resulted in 286 GPs (95.6%) discussing at least the advantages. The main arguments respondents found their advice on to women to participate are: to increase effectiveness of treatment (257; 84.5%); to diminish extent of possible surgery (231; 76.0%); to improve quality of life (223; 73.4%); to prolong lifespan of patients (218; 71.7%). They appeared to be less interested in the effects on mortality at population level (138; 45.4%). When asked which measures were the most important in combating breast cancer, among five given possibilities (early diagnosis through a screening programme; detection and follow-up of women with fibroadenoma or fibrocystic breast condition; detection and follow-up of families with hereditary breast cancer; scientific research on the mechanisms of carcinogenesis; and application of alternative cancer therapies
besides regular treatment), 245 (80.6%) included screening mammography. 3.4. Practical experience A majority (81.9%) of the responding GPs sees one to four new cases of breast carcinoma in the age category 50–69 in their practice a year (1–2: 58.9%; 3–4: 23.0%). In total, 95.1% see at least one new case a year. At any moment, about two thirds (68%) of the GPs have on average 2–20 ‘‘long-standing’’ breast cancer patients in their practice. Ten per cent of the practices even constantly harbour over 20 breast cancer patients. A significant number of participants (221, or 72.7%) had been confronted with false-positive mammography results obtained from the official screening programme during the last two years. This is in contrast with the number confronted with false-negative results (41, or 13.5%). 3.5. Wishes and considerations Among many different comments and suggestions, a lot of them illustrated a constructive attitude. They concerned dissemination of information to involved parties, the position of GPs within preventive medicine, their viewpoints on financial and logistic support, communication strategies, the approach of underprivileged subgroups, coordination between different medical disciplines, and reading of mammograms. The main messages are summarized in Table 3. 4. DISCUSSION In this observational survey we explored knowledge, attitudes, practical experience, and personal views on breast cancer and mammographic screening among GPs in the province of Antwerp. The Flemish system promotes participation of the target group in the official screening programme with encouraging results, although a background of opportunistic screening continues to exist.
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Table 2 Attitudes of respondents towards screening mammography.
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Table 3 Main comments on the breast cancer screening system as expressed by the participants. Distribute more detailed information – both to the target population and the GPs – on the increasing participation in the official breast cancer screening programme Most GPs realise their unique role in preventive medicine, but would like to see this discipline strengthened and promoted GPs ask for more financial and logistic support, e.g., in terms of stimuli to attain a target percentage of uptake among their female patient population aged 50–69 The five Flemish coordinating screening centres should transmit information on invited and (non)-screened women to their GPs Women who did not consider their invitation letter could be better motivated by their GP provided the latter is sufficiently informed on this matter Some GPs propose to organise regular meetings with local quality groups to assure more accurate communication, e.g., about participation coverage, between involved parties The underprivileged (e.g., those with low socioeconomic status, allochthonous or illegal population groups, asylum seekers) should be approached in a tailored way GPs seek a better cooperation with gynaecologists and wish to be informed when a woman is referred for opportunistic screening; some propose to create a database of mammograms, accessible to GPs, gynaecologists, and radiologists GPs expect more openness and consultation from the side of the radiologists The time between the first and the second reading of the mammograms should be shortened
The knowledge of participating GPs on definitions and basic concepts of mammographic screening obviously needs a brushup. Only the questions regarding certainty diagnosis and the effects of HRT scored points if, e.g., a threshold of 80% correct answers were adopted. The remaining listed questions yielded, roughly spoken, 50–70% correct answers. The low proportion of participants able to select the correct definition of test specificity is rather worrying. The same applies for their view on the dependency of sensitivity and specificity on age. This is striking, for the consideration that both sensitivity and specificity are sufficiently high to screen was one of the main arguments to introduce the programme. There is also a problem concerning some GPs’ understanding of the correlation between the predictive value of mammographic screening and breast cancer prevalence. Incidence and prevalence of breast cancer in Flanders belong to the highest in Europe and as a consequence, Flemish women derive benefit from a systematic screening programme. Knowledge of mammographic screening in the context of prevention strategies and the Wilson and Jungner criteria [6] was more or less satisfactory. Answering the question on differences between systematic and opportunistic screening was problematic for most. Giving no answer and knowing no differences represented 31.3% of all GPs. Most remaining responses were incomplete. If this reflects a lack of knowledge, it is of importance. The fact is that the differences yield a range of arguments in favour of systematic screening. The attitude of at least 50% of the sounded GPs is predominantly positive and/or realistic towards the proposed
theses in almost all cases. One crucial proposition, on the attainability of a 75% systematic screening mammography uptake in the Flemish Region, yielded less than 50% positive answers. Also two other propositions, on the frequency of false-positive results and the reasons for introducing screening mammography in Belgium, respectively, yielded not much more than 50% ‘‘positive’’ answers. At the other end of the spectrum, three theses were judged positively in over 80% of the cases: the expectation that screening will in the long run lead to a decrease in cause-specific mortality, the view that mammography is a useful and rapid tool for mass screening, and the ‘‘fact’’ that false-positive mammography results frequently lead to breast amputation. The proportions of respondents positively/realistically judging the remaining hypotheses all were between 60 and 80%. The combination of this moderately positive/realistic attitude with the preparedness of the majority of GPs to discuss at least the advantages of systematic screening is encouraging. The validity of their arguments to urge on their patients belonging to the target group to participate strengthens their position as professional mediators. However, also this can be improved because, crucial though the individual level is, also the population level deserves attention in terms of reduction of mortality. The engaged GPs’ practical experience on breast carcinoma and mammography can be considered satisfactory. A wide majority sees at least one new breast cancer patient in the target age category a year and almost 70% have 2–20 breast cancer patients in their practice at any time. They have experience with false-positive and -negative mammography results, albeit in a very different degree. Crucial in this context are the personal opinions regarding official breast cancer screening. It is obvious that many participants are favourably disposed towards systematic screening organised by the government. This is illustrated by their ‘‘wishes and considerations’’, which can be subdivided in five categories and concern measures to: increase participation in the official screening programme (motivate the target population based on response to invitation; approach the underprivileged in a tailored way); promote dissemination of information and communication between all those involved (inform GPs and target population on participation rates; stimulate communication between screening centres, GPs, local quality groups, gynaecologists, and radiologists); provide support to GPs dedicated to the programme (supply logistic and financial stimuli depending on the realised uptake); facilitate operational aspects (shorten time between first and second reading); enrich the curriculum of GPs (strengthen and promote the GP’s role in preventive medicine and screening). Our survey has its limitations as well, especially in terms of a low response rate. This, however, has to be put into perspective. Although the 317 completed questionnaires represent only about 21% of the selected GPs, they still stand for 12% of the total Antwerp GP population. Next, the concept ‘‘low response’’ to postal surveys among GPs in itself is to be relativised, since other
examples show that response rates can vary between, e.g., 15 and 80% [10–14]. The highest rates were usually obtained after telephonic or written precontact with potential participants [14], by urging them to participate through the use of up to three reminders or by offering monetary or non-monetary incentives. And finally, physicians’ response rates proved to be sensitive to relatively small differences in questionnaire length, as was shown in an American study [12]. These considerations, however, do not quite suffice to make up for questions regarding representativity, since for example gender distribution and proportion of solo practices were not alike among participants and non-participants. Mammographic screening leads to early detection of malignancies in the breast, possible early intervention, and prevention of progressive disease. Many countries therefore introduced mass screening for breast cancer. The complex nature of the Belgian political structure however, the concomitant fragmentation of political competences between Federal Government and Regions, the high-standard but complicated healthcare system, historical factors, and a certain inclination of professionals to defend acquired rights, resulted in a participation uptake that leaves room for improvement. The Flemish Region, responsible for cancer screening in Flanders, made it its purpose to raise the estimated uptake of 37% in 2004–2005 to 75% in 2012. One of the main reasons for the current rather low participation rate is that in 2004–2005 an estimated additional 21% of the target population participated outside the official programme, and underwent opportunistic screening [15]. If the Flemish health target on mammographic screening is to be reached soon, serious efforts will have to be made to convince this group and those who do not participate at all of the advantages of participation in the official screening programme. A key role in achieving this is reserved for the GP. It is also interesting to consider the Flemish/Belgian situation in an international context. Despite the numerous particularities of the Belgian mammographic screening model, there are similarities with several other countries. The results of the EDIFICE study (2005) reveal that among the French women aged 50-74 who declared to have ever undergone a mammography (92.5% of the target population), 44.6% (49% in 2006) had done so in the framework of the systematic screening plan [16,17]. These proportions are roughly in the order of the current uptake figures in Flanders (37% in 2004–2005; 46% in 2007) [9,15]. Also Switzerland faces substantial background rates of opportunistic screening [18]. A comparative study carried out in 2004 showed that the extent of organised breast cancer screening systems vs. opportunistic screening defers greatly, depending on the country. In the United Kingdom (UK), e.g., opportunistic screening activity was minimal, while in the United States (USA) cancer screening in general was predominantly opportunistic [19]. It is equally clear that local participation rates in official programmes can considerably differ from national averages; Parisian women aged 50-74 years, e.g., participated much less than the French average in 2006 (27% vs. 49%, resp) [16,20]. The generally positive disposition of the GPs corresponds with the results of the French EDIFICE study [17]. There is,
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however, also a continuing need to educate physicians on principles, benefits, and risks of systematic screening the target group, as was also observed in other countries with a mixed mammographic screening model [21]. This need is perhaps best illustrated by the fact that few participants were able to describe the differences between systematic and opportunistic screening. Also the effects of mammographic screening at population level deserve further attention. In the context of our mixed screening model, GPs seem to be in an excellent position to help shifting the balance in favour of the official screening system and bringing us closer to the Flemish health targets 2012. This position, however, is open to improvement and additional action is needed. DISCLOSURE OF INTEREST The authors declare that they have no conflicts of interest concerning this article. Acknowledgements The authors are grateful to Hilde Bastiaens, Marjoke van der Burg, Jos Droste, Manana Sariachvili, and Joost Weyler for their constructive advice during the realisation of this work. REFERENCES [1] International Agency for Research on Cancer (IARC).. World Cancer Report. In: Stewart BW, Kleihues P, editors. 5. Human cancers by organ site – Breast cancer. Lyon: IARC; 2003. p. 188–93. [Accessed 6 July 2011]www.iarc.fr. [2] Belgian Cancer Registry. www.kankerregister.be [Accessed 6 July 2011]. [3] Van Eycken E. Cancer Incidence and Survival in Flanders, 2000–2001. In: De Wever N, Rottiers L, Van de Walle G, Verstreken M, editors. Flemish Cancer Registry Network. Brussels: Flemish League against Cancer (Vlaamse Liga tegen Kanker, VLK); 2006. p. 11–76. [4] Miettinen OS, Yankelevitz DF, Henschke CI. Evaluation of screening for a cancer: annotated catechism of the Gold Standard creed. J Eval Clin Pract 2003;9:145–50. [5] Weyler J. Types of prevention: basic concepts. In: Schrijvers D, Senn HJ, Mellstedt H, Zakotnik B, editors. ESMO handbook of cancer prevention. London: Informa; 2008. p. 11–8. [6] Wilson JM, Jungner G. Principles and practice of screening for disease. In: Public Health Papers no. 34. Geneva: World Health Organization; 1968. p. 26–7. [7] Andermann A, Blancquaert I, Beauchamp S, Déry V. Revisiting Wilson and Jungner in the genomic age: a review of screening criteria over the past 40 years. Bull World Health Organ 2008;86:317–9. [8] Perry N, Broeders M, De Wolf C, Törnberg S, Holland R, von Karsa L, editors for the European Breast Cancer Network (EBCN). European guidelines for quality assurance in breast cancer screening and diagnosis. Fourth ed. Lyon: International Agency for Research on Cancer; 2004. [9] Flemish Agency for Care and Health. Gezondheidsdoelstellingen – Borstkankeropsporing [Health targets – Breast cancer]. www.zorg-engezondheid.be [Accessed 6 July 2011]. [10] Templeton L, Deehan A, Taylor C, Drummond C, Strang J. Surveying general practitioners: does a low response rate matter? Br J Gen Pract 1997;47:91–4. [11] Thomson CE, Paterson-Brown S, Russell D, McCaldin D, Russell IT. Short report: encouraging GPs to complete postal questionnaires – one big prize or many small prizes? A randomized controlled trial. Fam Pract 2004;21:697–8.
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ORIGINAL ARTICLE
A pivotal role for the general practitioner in a mixed mammographic screening model Un rôle crucial pour le médecin généraliste dans un modèle mixte de dépistage du cancer du sein G. François, S. Van Roosbroeck, S. Hoeck, E. Markovskaia, G. Van Hal * Department of Epidemiology and Social Medicine – Medical Sociology and Health Policy, Campus Drie Eiken, University of Antwerp, 1, 2610 Antwerp, Belgium Received 27 February 2009; accepted 7 September 2011
Abstract Background. – A mixed mammographic screening model presents a country or region with a complex problem. Promoting a significant shift within the target population from opportunistic breast cancer screening to participation in an organised screening programme offers many advantages. The objective was to explore the role of GPs as potential mediators by assessing their specific knowledge, attitudes, and experience on breast cancer and mammographic screening. Methods. – A detailed questionnaire was mailed in 2007 to 1500 GPs randomly sampled from the GP population in the province of Antwerp, Belgium. Levels of knowledge on epidemiology and screening, opinions and attitudes on systematic mammographic screening, and experience with breast cancer and mammography were evaluated. Results. – We received 317 completed questionnaires, 21.1% of the contacted GPs. General knowledge on basic concepts of mammographic screening was average, while the response to an open question on the differences between screening and opportunistic mammography was very limited. More than half of the participants had a positive or realistic attitude towards many aspects of systematic screening, and had satisfactory experience with breast cancer patients in their daily practice (about 82% saw one to four new cases a year). Many (72%) were favourably disposed towards systematic screening organised by the government. Conclusion. – The answers of the GPs suggest a promising potential with regard to the official breast cancer screening programme. Many participants presented qualifications, which could contribute to a change from the mixed model in favour of the official screening system. A number of gaps, however, need to be filled and there is a continuing need to educate physicians on principles and risks and benefits of systematic screening of the target group. ß 2012 Elsevier Masson SAS. All rights reserved. Résumé Position du problème. – Un modèle mixte de dépistage du cancer du sein place un pays ou une région devant un problème complexe. Promouvoir un changement important au sein de la population-cible du dépistage du cancer du sein opportuniste vers la participation à un programme de dépistage organisé offre de nombreux avantages. L’objectif était d’explorer le rôle des médecins généralistes comme des médiateurs en évaluant leurs connaissances, leurs attitudes et leur expérience sur le cancer du sein et la mammographie. Méthodes. – Un questionnaire détaillé a été envoyé en 2007 à 1500 médecins généralistes échantillonnés au hasard à partir de la population généraliste dans la province d’Anvers en Belgique. Le niveau des connaissances sur l’épidémiologie et le dépistage du cancer du sein, les opinions et les attitudes sur le dépistage systématique, et l’expérience avec le cancer du sein et la mammographie ont été évalués.
* Corresponding author. E-mail address: [email protected] (G. Van Hal). 0398-7620/$ see front matter ß 2012 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.respe.2011.09.008
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Résultats. – Nous avons reçu 317 questionnaires renseignés, soit un taux de réponse de 21,1 % du total des médecins généralistes contactés. Les connaissances générales sur les concepts de base du dépistage par mammographie sont moyennes, tandis que la réponse à une question ouverte sur les différences entre le dépistage opportuniste et le dépistage systématique était très limitée. Plus de la moitié des participants ont une attitude positive ou réaliste à l’égard de beaucoup d’aspects du dépistage systématique et ont une expérience satisfaisante avec le cancer du sein dans leur pratique quotidienne (environ 82 % voient un à quatre nouveaux cas par an). Beaucoup d’entre eux (72 %) sont favorables à un dépistage systématique organisé par le gouvernement. Conclusion. – Les réponses des médecins généralistes révèlent un potentiel prometteur en ce qui concerne le programme de dépistage du cancer du sein officiel. Beaucoup de participants semblent être compétents à modifier l’équilibre du modèle mixte en faveur du système officiel. Un certain nombre de lacunes, cependant, doivent être comblées et il faut continuer à éduquer les médecins sur les principes et les risques et avantages d’un dépistage systématique de la population-cible. ß 2012 Elsevier Masson SAS. Tous droits réservés. Keywords: Breast cancer; Organised screening; Opportunistic screening; Participation; General practitioner; Knowledge; Attitude; Practice Mots clés : Cancer du sein ; Dépistage organisé ; Dépistage opportuniste ; Médecin généraliste ; Connaissance ; Attitude ; Pratique
1. INTRODUCTION Breast cancer is, worldwide, the most common tumour affecting women and exerts a huge annual toll. The most affluent societies run the greatest risk, with incidence rates over 80 per 100,000 and globally nearly 580,000 new annual cases [1]. In Flanders, 5374 women were diagnosed with breast cancer in 2004, representing 34.2% of the total of invasive tumours in women. In 2000–2001, age-standardised incidence rates for invasive breast cancer in Flanders ranked among the highest in Europe [2,3]. Cancer screening implies pursuing early diagnosis in asymptomatic persons and is justified in terms of the presumed utility of early relative to late diagnosis. Mammographic screening, e.g., contributes to preventing progression of breast cancer and its complications by early intervention [4,5]. Breast cancer meets all ten criteria as proposed by the WHO to make it suitable for screening [6,7]. Breast cancer screening takes place in all Belgian Regions. The complex national healthcare system proved to be an important obstacle for full implementation of the European Guidelines [8] and therefore, some deviations were allowed. In Flanders, the official screening programme was introduced on June 15, 2001. Before that date, Flemish women could undergo a mammography, but this was only possible on an ‘‘individual’’ or ‘‘opportunistic’’ basis. From June 15, 2001 on, ‘‘individual’’/ ‘‘opportunistic’’ mammography and the official screening programme kept on coexisting. This complicated situation is the essence of the current mixed mammographic screening model. In the official programme, women aged 50–69 are twoyearly invited for a screening mammography. Invitation occurs through their GP (this is called Track 1) or by one of the official screening centres (this is called Track 2). Flanders has five screening centres (Antwerp, Bruges, Brussels, Ghent, Leuven). In addition to this official programme, as mentioned above, each woman is free to turn to a radiologist on a private basis for an ‘‘individual’’ or ‘‘opportunistic’’ mammography. The latter procedure takes place beyond the scope of the official
screening programme. In this case the involved woman usually annually undergoes a mammography and also an ultrasonographic breast examination. The official breast cancer screening programme has numerous advantages in comparison with the opportunistic way. These comprise: guaranteed, monitored high-quality mammography; continual quality control of programme, technical equipment, and performance of radiologists; registration of participation and follow-up; automatic re-invitation; lessons learned in terms of future campaigns; a free mammography; and a saving in public expenditures. Because of these reasons it is desirable that as many women as possible making part of the target population make the change-over from non-official opportunistic screening to participation in the official screening programme. Participation in the official breast cancer screening programme in Flanders amounts to on average ca 48% of the target group. One health target of the Flemish Government is to increase this figure to at least 75% by 2012 [9]. This gap can potentially and at least partially be filled if women now undergoing opportunistic screening (about 20% of the target population) can be convinced to switch to the official programme. GPs are in a favourable position to transmit the advantages of this step. To explore knowledge, attitudes, and experience of those functioning in a mammographic model wherein individual and organised screening coexist, we mailed a questionnaire to regional GPs, to sound out both their personal views and criticism on breast cancer screening. 2. METHODS 2.1. Sampling From the total population of GPs in the Province of Antwerp (Flemish Region), i.e. 2600 persons, 1500 (58%) were randomly selected and included as potential participants in the study. Stratification based on the degree of urbanisation was not considered, because the population density is very high
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(568 km 2) and clear-cut differences between urban, semirural, and rural communities do not apply.
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2.2. Survey A questionnaire (36 items) on knowledge, attitudes, own practice, and views on breast cancer and screening was sent in 2007 to the GPs by surface mail, accompanied with a cover letter and a stamped addressed envelope. Participants were asked to send their response within four weeks after receipt. Knowledge and attitude questions were mainly inspired by the literature, recommendations on prevention, newsletters for GPs, and private discussions with GPs. Attitudes towards screening mammography were evaluated by considering that answering ‘‘I agree’’ to this category of questions implied a positive, realistic, or negative attitude, depending on the case. Respondents’ practical experiences were considered in the context of numbers of cases in their practice, numbers of ‘‘longstanding’’ breast cancer patients, and false-positive and negative screening results. A number of questions were open, but most of them were multiple-choice questions. There was room for additional remarks, considerations, and suggestions. Participants were given the opportunity to express their personal views and criticism on breast cancer screening, together with their wishes and considerations. A limited number of personal details (gender, age category, year of graduation, type of practice, work pressure) were asked as well. The questionnaire was pre-tested before actual use. 2.3. Statistical analysis Descriptive statistics were used to summarize the main characteristics of the data set, particularly the specific knowledge, attitudes, and experiences on breast cancer and mammographic screening of the participants. Pearson Chi2 tests were performed (SPSS version 18.0) to test the association between participation/non-participation and gender, graduation year, and proportion of solo practices. Answers to open questions were repeatedly read in order to maintain a holistic view on the comments on the screening system. A highlighting approach was applied to gain insight in the essential themes and patterns, which were subsequently isolated from the responses and then clustered into core themes. This
procedure was independently performed by two investigators, to validate the analysis. 3. RESULTS 3.1. Participants We received 317 completed questionnaires, implying a response rate of 21.1%; 13 were not considered because they concerned physicians no longer active as GPs. Among the remaining 304, about one third was women. All age categories (25–65) were covered and all types of practice (individual, shared, or group practice) were represented. Participants’ pressure of work, expressed as number of visits per week, was as follows: 11.2% saw 20–50 patients, 42.4% saw 51–100 patients, 29.6% saw 101–150 patients, and 15.8% saw over 150 patients a week. Year of graduation was similar among participants and non-participants (1970 or earlier: 8.6 vs. 11.5%; 1971–1980: 25.3 vs. 27.1%; 1981–1990: 34.9 vs. 31.4%; 1991–2000: 24.0 vs. 23.4%; 2001 or later: 5.6 vs. 6.8%; p = 0.455). On the other hand, gender distribution (males: 62.2 vs. 69.7%; p = 0.011) and the proportion of solo practices were not alike in both populations (57.6 vs. 82.8%; p < 0.001).
3.2. Knowledge General questions on preventive medicine and breast cancer screening were answered as summarized in Table 1. Almost all (94.1%) knew that screening mammography does not yield a certainty diagnosis and 82.9% knew that hormone replacement therapy (HRT) increases the prevalence of breast cancer. All other questions were answered correctly by 48–69% of participants. The response to the open question ‘‘Please describe the differences between screening and opportunistic mammography’’ was limited. About one third (31.3%) of all participants did not answer the question or were not able to describe any differences. The majority of those that did respond delivered only fragmentary answers, meaning that only few of them were able to give an overview of all differences. Participants were then asked to indicate those types of cancer that meet the Wilson and Jungner criteria [6] and the European Guidelines [8] for mass screening. They could choose from a list of eight types
Table 1 General level of knowledge of participants on definitions and basic concepts of mammographic screening. Subject of the question
Correct answer n (%)
Incorrect answer n (%)
No answer n (%)
Definition of sensitivity Definition of specificity Dependency of sensitivity and specificity on age Definition of certainty diagnosis Which type of prevention is screening mammography? Effect of HRT on breast cancer prevalence Effect of breast cancer prevalence on predictive value of mammography
210 145 176 286 208 252 179
75 134 106 13 84 39 95
19 25 21 5 12 13 30
HRT: hormone replacement therapy.
(69.1) (47.7) (58.1) (94.1) (68.4) (82.9) (58.9)
(24.7) (44.1) (35.0) (4.3) (27.6) (12.8) (31.3)
(6.3) (8.2) (6.9) (1.6) (3.9) (4.3) (9.9)
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Thesis
Agree n (%)
Disagree n (%)
No opinion n (%)
Screening mammography is physically and/or mentally traumatising for womena Mammography is useful as a relatively simple and rapid tool for mass screeningb Screening mammography yields too many false-positive resultsa,c False-positive results often lead to unwanted reactions such as fear, uncertainty, and depressionc False-positive results frequently lead to breast amputationa False-negative results unfavourably affect the process of treatment and counsellingc Screening mammography was introduced in Belgium mainly for economic reasonsa Screening for breast cancer will lead to a decrease in cause-specific mortality in the long runb The cause-specific mortality is equal in screened and non-screened populationsa A screening mammography uptake of 75% is currently attainable in Flanders, Belgiumb I feel involved in the breast cancer screening programme in Flanders, Belgiumb
30 257 63 210 6 195 38 250 17 143 211
237 15 157 45 281 51 166 14 214 76 22
37 32 84 46 17 57 99 40 68 84 61
a b c
(9.9) (84.5) (20.7) (69.7) (2.0) (64.4) (12.5) (82.2) (5.7) (47.2) (71.8)
(78.0) (4.9) (51.6) (15.0) (92.4) (16.8) (54.8) (4.6) (71.6) (25.1) (7.5)
(12.2) (10.5) (27.6) (15.3) (5.6) (18.8) (32.7) (13.2) (22.7) (27.7) (20.7)
Answering ‘‘I agree’’ to this question was considered a negative attitude. Answering ‘‘I agree’’ to this question was considered a positive attitude. Answering ‘‘I agree’’ to this question was considered a realistic attitude.
of cancer (breast, prostate, cervical, colorectal, ovarian, and lung carcinoma, melanoma, and non-Hodgkin lymphoma). Of all respondents, 72.7% were able to answer this question correctly. 3.3. Attitude The position of participants vis-à-vis some fundamental theses on screening mammography is displayed in Table 2. Most answers reflected a positive or realistic attitude. The first type is exemplified by responding to, e.g., ‘‘Mammography is useful as a relatively simple and rapid tool for mass screening’’ or ‘‘A screening mammography uptake of 75% is currently attainable in Flanders, Belgium’’ with ‘‘I agree’’. Commenting to, e.g., ‘‘False-negative results unfavourably affect the process of treatment and counselling’’ with ‘‘I agree’’ was considered as the result of a realistic attitude. In all considered cases, these two types of attitudes appeared to be more widespread among the respondents than a negative or unrealistic attitude, or having no opinion. Both pros and cons of participation are discussed with the involved women by 178 (59.5%) of the GPs; 108 (36.1%) inform them mainly on the advantages and only 13 (4.3%) mainly on the disadvantages. This resulted in 286 GPs (95.6%) discussing at least the advantages. The main arguments respondents found their advice on to women to participate are: to increase effectiveness of treatment (257; 84.5%); to diminish extent of possible surgery (231; 76.0%); to improve quality of life (223; 73.4%); to prolong lifespan of patients (218; 71.7%). They appeared to be less interested in the effects on mortality at population level (138; 45.4%). When asked which measures were the most important in combating breast cancer, among five given possibilities (early diagnosis through a screening programme; detection and follow-up of women with fibroadenoma or fibrocystic breast condition; detection and follow-up of families with hereditary breast cancer; scientific research on the mechanisms of carcinogenesis; and application of alternative cancer therapies
besides regular treatment), 245 (80.6%) included screening mammography. 3.4. Practical experience A majority (81.9%) of the responding GPs sees one to four new cases of breast carcinoma in the age category 50–69 in their practice a year (1–2: 58.9%; 3–4: 23.0%). In total, 95.1% see at least one new case a year. At any moment, about two thirds (68%) of the GPs have on average 2–20 ‘‘long-standing’’ breast cancer patients in their practice. Ten per cent of the practices even constantly harbour over 20 breast cancer patients. A significant number of participants (221, or 72.7%) had been confronted with false-positive mammography results obtained from the official screening programme during the last two years. This is in contrast with the number confronted with false-negative results (41, or 13.5%). 3.5. Wishes and considerations Among many different comments and suggestions, a lot of them illustrated a constructive attitude. They concerned dissemination of information to involved parties, the position of GPs within preventive medicine, their viewpoints on financial and logistic support, communication strategies, the approach of underprivileged subgroups, coordination between different medical disciplines, and reading of mammograms. The main messages are summarized in Table 3. 4. DISCUSSION In this observational survey we explored knowledge, attitudes, practical experience, and personal views on breast cancer and mammographic screening among GPs in the province of Antwerp. The Flemish system promotes participation of the target group in the official screening programme with encouraging results, although a background of opportunistic screening continues to exist.
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Table 2 Attitudes of respondents towards screening mammography.
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Table 3 Main comments on the breast cancer screening system as expressed by the participants. Distribute more detailed information – both to the target population and the GPs – on the increasing participation in the official breast cancer screening programme Most GPs realise their unique role in preventive medicine, but would like to see this discipline strengthened and promoted GPs ask for more financial and logistic support, e.g., in terms of stimuli to attain a target percentage of uptake among their female patient population aged 50–69 The five Flemish coordinating screening centres should transmit information on invited and (non)-screened women to their GPs Women who did not consider their invitation letter could be better motivated by their GP provided the latter is sufficiently informed on this matter Some GPs propose to organise regular meetings with local quality groups to assure more accurate communication, e.g., about participation coverage, between involved parties The underprivileged (e.g., those with low socioeconomic status, allochthonous or illegal population groups, asylum seekers) should be approached in a tailored way GPs seek a better cooperation with gynaecologists and wish to be informed when a woman is referred for opportunistic screening; some propose to create a database of mammograms, accessible to GPs, gynaecologists, and radiologists GPs expect more openness and consultation from the side of the radiologists The time between the first and the second reading of the mammograms should be shortened
The knowledge of participating GPs on definitions and basic concepts of mammographic screening obviously needs a brushup. Only the questions regarding certainty diagnosis and the effects of HRT scored points if, e.g., a threshold of 80% correct answers were adopted. The remaining listed questions yielded, roughly spoken, 50–70% correct answers. The low proportion of participants able to select the correct definition of test specificity is rather worrying. The same applies for their view on the dependency of sensitivity and specificity on age. This is striking, for the consideration that both sensitivity and specificity are sufficiently high to screen was one of the main arguments to introduce the programme. There is also a problem concerning some GPs’ understanding of the correlation between the predictive value of mammographic screening and breast cancer prevalence. Incidence and prevalence of breast cancer in Flanders belong to the highest in Europe and as a consequence, Flemish women derive benefit from a systematic screening programme. Knowledge of mammographic screening in the context of prevention strategies and the Wilson and Jungner criteria [6] was more or less satisfactory. Answering the question on differences between systematic and opportunistic screening was problematic for most. Giving no answer and knowing no differences represented 31.3% of all GPs. Most remaining responses were incomplete. If this reflects a lack of knowledge, it is of importance. The fact is that the differences yield a range of arguments in favour of systematic screening. The attitude of at least 50% of the sounded GPs is predominantly positive and/or realistic towards the proposed
theses in almost all cases. One crucial proposition, on the attainability of a 75% systematic screening mammography uptake in the Flemish Region, yielded less than 50% positive answers. Also two other propositions, on the frequency of false-positive results and the reasons for introducing screening mammography in Belgium, respectively, yielded not much more than 50% ‘‘positive’’ answers. At the other end of the spectrum, three theses were judged positively in over 80% of the cases: the expectation that screening will in the long run lead to a decrease in cause-specific mortality, the view that mammography is a useful and rapid tool for mass screening, and the ‘‘fact’’ that false-positive mammography results frequently lead to breast amputation. The proportions of respondents positively/realistically judging the remaining hypotheses all were between 60 and 80%. The combination of this moderately positive/realistic attitude with the preparedness of the majority of GPs to discuss at least the advantages of systematic screening is encouraging. The validity of their arguments to urge on their patients belonging to the target group to participate strengthens their position as professional mediators. However, also this can be improved because, crucial though the individual level is, also the population level deserves attention in terms of reduction of mortality. The engaged GPs’ practical experience on breast carcinoma and mammography can be considered satisfactory. A wide majority sees at least one new breast cancer patient in the target age category a year and almost 70% have 2–20 breast cancer patients in their practice at any time. They have experience with false-positive and -negative mammography results, albeit in a very different degree. Crucial in this context are the personal opinions regarding official breast cancer screening. It is obvious that many participants are favourably disposed towards systematic screening organised by the government. This is illustrated by their ‘‘wishes and considerations’’, which can be subdivided in five categories and concern measures to: increase participation in the official screening programme (motivate the target population based on response to invitation; approach the underprivileged in a tailored way); promote dissemination of information and communication between all those involved (inform GPs and target population on participation rates; stimulate communication between screening centres, GPs, local quality groups, gynaecologists, and radiologists); provide support to GPs dedicated to the programme (supply logistic and financial stimuli depending on the realised uptake); facilitate operational aspects (shorten time between first and second reading); enrich the curriculum of GPs (strengthen and promote the GP’s role in preventive medicine and screening). Our survey has its limitations as well, especially in terms of a low response rate. This, however, has to be put into perspective. Although the 317 completed questionnaires represent only about 21% of the selected GPs, they still stand for 12% of the total Antwerp GP population. Next, the concept ‘‘low response’’ to postal surveys among GPs in itself is to be relativised, since other
examples show that response rates can vary between, e.g., 15 and 80% [10–14]. The highest rates were usually obtained after telephonic or written precontact with potential participants [14], by urging them to participate through the use of up to three reminders or by offering monetary or non-monetary incentives. And finally, physicians’ response rates proved to be sensitive to relatively small differences in questionnaire length, as was shown in an American study [12]. These considerations, however, do not quite suffice to make up for questions regarding representativity, since for example gender distribution and proportion of solo practices were not alike among participants and non-participants. Mammographic screening leads to early detection of malignancies in the breast, possible early intervention, and prevention of progressive disease. Many countries therefore introduced mass screening for breast cancer. The complex nature of the Belgian political structure however, the concomitant fragmentation of political competences between Federal Government and Regions, the high-standard but complicated healthcare system, historical factors, and a certain inclination of professionals to defend acquired rights, resulted in a participation uptake that leaves room for improvement. The Flemish Region, responsible for cancer screening in Flanders, made it its purpose to raise the estimated uptake of 37% in 2004–2005 to 75% in 2012. One of the main reasons for the current rather low participation rate is that in 2004–2005 an estimated additional 21% of the target population participated outside the official programme, and underwent opportunistic screening [15]. If the Flemish health target on mammographic screening is to be reached soon, serious efforts will have to be made to convince this group and those who do not participate at all of the advantages of participation in the official screening programme. A key role in achieving this is reserved for the GP. It is also interesting to consider the Flemish/Belgian situation in an international context. Despite the numerous particularities of the Belgian mammographic screening model, there are similarities with several other countries. The results of the EDIFICE study (2005) reveal that among the French women aged 50-74 who declared to have ever undergone a mammography (92.5% of the target population), 44.6% (49% in 2006) had done so in the framework of the systematic screening plan [16,17]. These proportions are roughly in the order of the current uptake figures in Flanders (37% in 2004–2005; 46% in 2007) [9,15]. Also Switzerland faces substantial background rates of opportunistic screening [18]. A comparative study carried out in 2004 showed that the extent of organised breast cancer screening systems vs. opportunistic screening defers greatly, depending on the country. In the United Kingdom (UK), e.g., opportunistic screening activity was minimal, while in the United States (USA) cancer screening in general was predominantly opportunistic [19]. It is equally clear that local participation rates in official programmes can considerably differ from national averages; Parisian women aged 50-74 years, e.g., participated much less than the French average in 2006 (27% vs. 49%, resp) [16,20]. The generally positive disposition of the GPs corresponds with the results of the French EDIFICE study [17]. There is,
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however, also a continuing need to educate physicians on principles, benefits, and risks of systematic screening the target group, as was also observed in other countries with a mixed mammographic screening model [21]. This need is perhaps best illustrated by the fact that few participants were able to describe the differences between systematic and opportunistic screening. Also the effects of mammographic screening at population level deserve further attention. In the context of our mixed screening model, GPs seem to be in an excellent position to help shifting the balance in favour of the official screening system and bringing us closer to the Flemish health targets 2012. This position, however, is open to improvement and additional action is needed. DISCLOSURE OF INTEREST The authors declare that they have no conflicts of interest concerning this article. Acknowledgements The authors are grateful to Hilde Bastiaens, Marjoke van der Burg, Jos Droste, Manana Sariachvili, and Joost Weyler for their constructive advice during the realisation of this work. REFERENCES [1] International Agency for Research on Cancer (IARC).. World Cancer Report. In: Stewart BW, Kleihues P, editors. 5. Human cancers by organ site – Breast cancer. Lyon: IARC; 2003. p. 188–93. [Accessed 6 July 2011]www.iarc.fr. [2] Belgian Cancer Registry. www.kankerregister.be [Accessed 6 July 2011]. [3] Van Eycken E. Cancer Incidence and Survival in Flanders, 2000–2001. In: De Wever N, Rottiers L, Van de Walle G, Verstreken M, editors. Flemish Cancer Registry Network. Brussels: Flemish League against Cancer (Vlaamse Liga tegen Kanker, VLK); 2006. p. 11–76. [4] Miettinen OS, Yankelevitz DF, Henschke CI. Evaluation of screening for a cancer: annotated catechism of the Gold Standard creed. J Eval Clin Pract 2003;9:145–50. [5] Weyler J. Types of prevention: basic concepts. In: Schrijvers D, Senn HJ, Mellstedt H, Zakotnik B, editors. ESMO handbook of cancer prevention. London: Informa; 2008. p. 11–8. [6] Wilson JM, Jungner G. Principles and practice of screening for disease. In: Public Health Papers no. 34. Geneva: World Health Organization; 1968. p. 26–7. [7] Andermann A, Blancquaert I, Beauchamp S, Déry V. Revisiting Wilson and Jungner in the genomic age: a review of screening criteria over the past 40 years. Bull World Health Organ 2008;86:317–9. [8] Perry N, Broeders M, De Wolf C, Törnberg S, Holland R, von Karsa L, editors for the European Breast Cancer Network (EBCN). European guidelines for quality assurance in breast cancer screening and diagnosis. Fourth ed. Lyon: International Agency for Research on Cancer; 2004. [9] Flemish Agency for Care and Health. Gezondheidsdoelstellingen – Borstkankeropsporing [Health targets – Breast cancer]. www.zorg-engezondheid.be [Accessed 6 July 2011]. [10] Templeton L, Deehan A, Taylor C, Drummond C, Strang J. Surveying general practitioners: does a low response rate matter? Br J Gen Pract 1997;47:91–4. [11] Thomson CE, Paterson-Brown S, Russell D, McCaldin D, Russell IT. Short report: encouraging GPs to complete postal questionnaires – one big prize or many small prizes? A randomized controlled trial. Fam Pract 2004;21:697–8.
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