Recommendations from the European Breast Cancer Guidelines

Should an organised mammography screening programme vs. an opportunistic or non-organised mammography screening programme be used to diagnose early breast cancer in asymptomatic women?

Recommendation

The ECIBC's Guidelines Development Group recommends using an organised mammography screening programme for early detection of breast cancer in asymptomatic women (strong recommendation, moderate certainty in the evidence).

Recommendation strength

  •   Strong recommendation against the intervention
  •   Conditional recommendation against the intervention
  •   Conditional recommendation for either the intervention or the comparison
  •   Conditional recommendation for the intervention
  • Strong recommendation for the intervention

A recommendation can be strong or conditional.

When a recommendation is strong, most women will want to follow it. When a recommendation is conditional, the majority of women want to follow it but may need more discussion with their healthcare professional first.

Subgroup

None identified.

Justification

Overall justification

The GDG recommends by consensus that organised screening programmes should be used over opportunistic or non-organised mammography screening programmes on both the research evidence presented and the additional considerations noted above by the GDG.

Detailed justification

Desirable Effects:
The GDG judged that the desirable effects including increased breast cancer detection were large.

Undesirable Effects:
The GDG judged that the undesirable effects of an organised screening programme would be trivial.

Certainty of the evidence of test accuracy:
The GDG judged that the overall certainty of the test accuracy was moderate.

Balance of effects:
The GDG judged that the balance of effects favours organised screening.

Equity:
The GDG judged that organised screening would increase health equity.

Considerations

Implementation

1. Information from local contexts and grey literature may provide additional evidence on the cost-effectiveness of this intervention in different settings.
 
2. This recommendation only applies to the age-groups where the GDG has recommended screening.
 
3. The GDG notes that there may be barriers to implementation based on the resistance to organised screening programmes of some professionals.
 
4. The GDG agreed there was room for improvement in developing information material that is more acceptable to women invited to screening.

Monitoring and Evaluation

Appropriateness and adherence to protocols for organised screening programme.

Research Priorities

Additional research on the cost-effectiveness of organised screening in different settings is suggested.

Evidence

Download the evidence profile

Assessment

Background

Although mammography screening is recommended for women between the ages of 45 and 74 (and strongly recommended for women between the ages of 50 and 69), there is variation in practice with respect to offering them organised or non-organised screening. In 2003 the Council of the EU recommended the implementation of organised screening programmes. Currently, in most European countries that have screening, an organised screening programme is used (Giordano L et al., 2012). However, the two systems co-exist (see definitions of both below) and as there are some uncertainties regarding their effectiveness the Guidelines Development Group issued this healthcare question. The rationale for the recommendation of organised screening can be based on a greater ability to cover the target population and therefore greater effectiveness at the population level of organised programmes compared to non-organised screening, as shown by several observational studies, as well as a more equitable access. Several systematic reviews of large observational studies have focussed on specific aspects such as the effect of test uptake, equity in uptake (Palència L, 2010, Ferroni E, 2012), appropriate use of resources, false positives, interval cancers (Smith-Bindman R, 2003, Hofvind S, 2008, Domingo L, 2016) and costs (de Gelder R, 2009).
Definitions considered by the GDG for this healthcare question:

Organised screening is a screening programme that sets up a systematic call/recall system and quality assurance at all appropriate levels, together with an effective and appropriate diagnostic and treatment and after-care service following evidence-based guidelines. There are seven characteristics of an organised screening programme: a policy specifying target population, screening method and interval; a defined target population; an active invitation of the entire target population; a team responsible for overseeing screening centres; a decision structure and responsibility for healthcare management; a quality assurance system utilising relevant data; and monitoring of cancer occurrence in the target population(Madlensky L, 2003, Ponti A, 2017). Opportunistic or non-organised screening refers to all other screening programmes based on the initiative of women themselves to go for a mammogram (Madlensky L, 2003, Eichholzer M, 2016).

Is the problem a priority?
Yes *
* Possible answers: ( No , Probably no , Probably yes , Yes , Varies , Don't know )
Research Evidence
Breast cancer is the second most common cancer in the world and, by far, the most frequent cancer among women with an estimated 1.67 million new cancer cases diagnosed in 2012—accounting for 25% of all cancers (Ferlay et al., 2013). Breast cancer ranks as the fifth leading cause of cancer death worldwide and the second leading cause of cancer-related death in developed regions (Ferlay et al., 2013). In the European Union, 367 090 women were diagnosed with breast cancer and 92 000 women died from the disease in 2012 (Ferlay et al., 2013). Breast cancer ranks fourth among the top five cancers with the highest disease burden (Tsilidis et al., 2016). Annual incidence of breast cancer in the EU among women aged 50 to 69 is 2.7 per 1 000 and mortality is 0.5 per 1 000 (Ferlay et al., 2013)
Additional Considerations

This question was prioritised by the GDG

How accurate is the test?
Accurate *
* Possible answers: ( Very inaccurate , Inaccurate , Accurate , Very accurate , Varies , Don't know )
Research Evidence
The GDG only included under this research evidence column those studies considered most direct comparisons between organised and non-organised screening programmes which were those studies carried out within the same country (Bihrmann K, 2008, Bulliard JL, 2009, Vanier A, 2013), as they assumed the definitions and techniques used as well as country breast cancer incidence within the populations would be more similar.

Test accuracy

Organised mammography screening programme: Sensitivity: 0.69 (95% CI: 0.64 to 0.74) Specificity: 0.99 (95% CI: 0.98 to 0.99)
Opportunistic or non-organised mammography screening programme: Sensitivity: 0.39 (95% CI: 0.30 to 0.50) Specificity: 0.98 (95% CI: 0.98 to 0.99)
Additional Considerations

In this column, the GDG decided to include one relevant study that compared screening programmes in different countries.

Domingo et al (Domingo L, 2016)reported a cross-national comparison of screening mammography accuracy measures in U.S. (opportunistic programme), Norway, and Spain (both population-based organised programmes) from women aged 50–69 years who underwent mammographic screening 1996–2009.

Organised mammography screening programme (Norway, Spain) Sensitivity: Norway 0.75 (95% CI 0.75-0.76), Spain 0.79 (95% CI 0.78-0.80) Specificity: Norway 0.97 (95% CI 0.97−0.97), Spain 0.96 95% CI (0.96−0.96)
Opportunistic or non-organised mammography screening programme (US) Sensitivity: 0.83 (95% CI 0.82-0.84); Specificity: 0.91 (95% CI 0.91.−0.91)

Although the 83% sensitivity might be overestimated in opportunistic screening from Domingo study due to a shorter screening interval, the sensitivity with opportunistic screening from Bihrmann study(Bihrmann K, 2008) is much lower (39%), probably due to retrospective interpretation of mammography results from the medical records without direct assessment of the images. The GDG notes that this question assesses two test strategies using the same screening test, mammography. The GDG clarified that the reference test for the calculation of the sensitivity and specificity is usual diagnostic work-up and clinical follow-up.

The GDG agreed by consensus that the tests are accurate.

The GDG notes that the mammography screening programmes conducted in the U.S. from the Domingo study(Domingo L, 2016) represent screening efforts that have some characteristics of organised screening programmes and are, therefore, not purely opportunistic. They do not invite, but they have a system for reminders, recall and follow-up. In this sense it is similar to organised screening. Also, we compare women 50-69, but in the US women have likely been screened up to 10 times previously before reaching the age of 50, and so the comparison is not similar.

How substantial are the desirable anticipated effects?
Large *
* Possible answers: ( Trivial , Small , Moderate , Large , Varies , Don't know )
Research Evidence
Test resultNumber of results per 1000 patients tested (95% CI)№ of participants
(studies)
Certainty of the evidence
(GRADE)
Prevalence 0%
organised mammography screening programme opportunistic or non-organised mammography screening programme
True positives
patients with (suspected lesions of) breast cancer
6 (6 to 7)3 (3 to 4)39927
(1)

MODERATE
a,b
3 more TP in organised mammography screening programme
False negatives
patients incorrectly classified as not having (suspected lesions of) breast cancer
3 (2 to 3)6 (5 to 6)
3 fewer FN in organised mammography screening programme
True negatives
patients without (suspected lesions of) breast cancer
977 (976 to 978)974 (969 to 979)39927
(1)

MODERATE
a,b
3 more TN in organised mammography screening programme
False positives
patients incorrectly classified as having (suspected lesions of) breast cancer
14 (13 to 15)17 (12 to 22)
3 fewer FP in organised mammography screening programme
  1. Single study
  2. Organised and opportunistic programmes were not performed in the same population. We cannot exclude some impact due to differences between study populations.
1. Bihrmann K, Jensen A,Olsen AH,Njor S,Schwartz W,Vejborg I,Lynge E. Performance of systematic and non-systematic ('opportunistic') screening mammography: a comparative study from Denmark. J Med Screen. 2008;15(1):23-6

Additional Considerations

The GDG notes that three more true positives and three more true negatives per 1,000 women screened are desirable effects. On an absolute scale the GDG notes that the doubling of true positive detections in organised screening programmes is a large desirable effect. The GDG notes that there are not likely many more breast cancers that could be detected.

The GDG agreed by consensus that the desirable anticipated effects of organised screening programmes were large.

As additional considerations to the results from the diagnostic accuracy studies, the other outcomes (breast cancer detection rates at different size and stage- table below the accuracy data results) of the included studies supported the accuracy results. The following statements synthesise the points taken into account by the GDG:

- The anticipated downstream clinical consequences from accuracy data were expected to be in favour of organised screening.

- This was confirmed with the other outcomes not related to test accuracy (shown in the table below) retrieved from the included studies. As can be seen, those studies reporting breast cancer detection rates at different size and stage also suggest a similar direction of effect to the diagnostic accuracy results.

- There was moderate certainty in the accuracy data, while the certainty was low to very low for the other outcomes (breast cancer detection rates, stage, etc.).

How substantial are the undesirable anticipated effects?
Trivial *
* Possible answers: ( Large , Moderate , Small , Trivial , Varies , Don't know )
Research Evidence
Test resultNumber of results per 1000 patients tested (95% CI)№ of participants
(studies)
Certainty of the evidence
(GRADE)
Prevalence 0%
organised mammography screening programme opportunistic or non-organised mammography screening programme
True positives
patients with (suspected lesions of) breast cancer
6 (6 to 7)3 (3 to 4)39927
(1)

MODERATE
a,b
3 more TP in organised mammography screening programme
False negatives
patients incorrectly classified as not having (suspected lesions of) breast cancer
3 (2 to 3)6 (5 to 6)
3 fewer FN in organised mammography screening programme
True negatives
patients without (suspected lesions of) breast cancer
977 (976 to 978)974 (969 to 979)39927
(1)

MODERATE
a,b
3 more TN in organised mammography screening programme
False positives
patients incorrectly classified as having (suspected lesions of) breast cancer
14 (13 to 15)17 (12 to 22)
3 fewer FP in organised mammography screening programme
  1. Single study
  2. Organised and opportunistic programmes were not performed in the same population. We cannot exclude some impact due to differences between study populations.
1. Bihrmann K, Jensen A,Olsen AH,Njor S,Schwartz W,Vejborg I,Lynge E. Performance of systematic and non-systematic ('opportunistic') screening mammography: a comparative study from Denmark. J Med Screen. 2008;15(1):23-6

Additional Considerations

The GDG notes that false positives would be undesirable effects. However, the evidence suggests that there are three fewer false positives with organised screening.

The GDG therefore agreed by consensus that these undesirable anticipated effects were trivial.

What is the overall certainty of the evidence of test accuracy?
Moderate *
* Possible answers: ( Very low , Low , Moderate , High , No included studies )
Additional Considerations

The GDG agreed based on the overall certainty of test accuracy data that it was moderate.

What is the overall certainty of the evidence for any critical or important direct benefits, adverse effects or burden of the test?
No included studies *
* Possible answers: ( Very low , Low , Moderate , High , No included studies )
Additional Considerations

The GDG noted that in organised screening there may be concerns with adverse effects such as stress due to the invitation process, as compared to opportunistic screening that may result from a conversation with their healthcare provider. In the context of a good invitation process, it is noted that this may not be a concern to women. The GDG noted that there may be benefits of invitation to screening, such as the feeling by women receiving invitations that the screening programme is looking out for their health.

No evidence on the impact of stress on women being invited in organised screening programmes was identified.

The GDG agreed by consensus that there were no included studies. However, the GDG had no concerns with regards to the effects of the test; they only had concerns regarding the effect of the invitation.

What is the overall certainty of the evidence of effects of the management that is guided by the test results?
No included studies *
* Possible answers: ( Very low , Low , Moderate , High , No included studies )
Additional Considerations

The GDG agreed that there were studies that addressed downstream outcomes that were directly measured, such as for example breast cancer stage that is a consequence of higher sensitivity, and also results on lymph node positivity (anticipating diagnosis and then having less lymph node positivity) that favour organised screening.

The GDG did not look for treatment studies, so there are no included studies, but the panel considered that the evidence that the treatment works better for women detected in earlier stages of breast cancer is probably at least moderate.

How certain is the link between test results and management decisions?
High *
* Possible answers: ( Very low , Low , Moderate , High , No included studies )
Additional Considerations

The GDG judged that the link between test results and management decisions was high. The GDG agreed that the link between test results and receiving treatment for breast cancer are quite strong.

What is the overall certainty of the evidence of effects of the test?
No included studies *
* Possible answers: ( Very low , Low , Moderate , High , No included studies )
Additional Considerations

Do not have direct evidence for mortality, but have evidence for surrogates, some prognostic factors.

Is there important uncertainty about or variability in how much people value the main outcomes?
Probably no important uncertainty or variability *
* Possible answers: ( Important uncertainty or variability , Possibly important uncertainty or variability , Probably no important uncertainty or variability , No important uncertainty or variability , No known undesirable outcomes )
Additional Considerations

The GDG did not reach consensus on how women value the main outcomes (such as diagnostic accuracy, breast cancer detection, interval cancer, recall rate, participation in screening, etc.) and therefore voting was conducted.

Among 20 GDG members without CoI: 8 members voted ‘possibly important uncertainty or variability’; 11 probably no important uncertainty or variability; 1 no important; 0 abstentions.

Does the balance between desirable and undesirable effects favor the intervention or the comparison?
Favors the intervention *
* Possible answers: ( Favors the comparison , Probably favors the comparison , Does not favor either the intervention or the comparison , Probably favors the intervention , Favors the intervention , Varies , Don't know )
Additional Considerations

The GDG agreed by consensus that the balance favours the intervention.

How large are the resource requirements (costs)?
Varies *
* Possible answers: ( Large costs , Moderate costs , Negligible costs and savings , Moderate savings , Large savings , Varies , Don't know )
Research Evidence
Organised vs. opportunistic screening






Additional Considerations

The GDG reviewed evidence incorporated from three research studies (Neeser K, 2007, de Gelder R, 2009, Schiller-Fruehwirth I, 2017), notes that the costs were lower for organised screening and higher in one study. The GDG discussed that the differences in the total costs of opportunistic vs organised screening may be related to differences in the year value of costs (one study uses 2004 cost value (Neeser K, 2007)and the other one uses 2007 cost value (de Gelder R, 2009)) or it may also be related to the model inputs or type of modelling used (Markov modelling vs microsimulation). For this reason the quality of the evidence was downgraded to low. There was uncertainty in the results because of indirectness, information from two studies come from the same canton in Switzerland (Voud) and may not be able to be extrapolated(Neeser K, 2007, de Gelder R, 2009).

The GDG noted that radiologist costs may be higher for opportunistic screening.

The GDG also notes that in organised screening there may be additional administration costs, however, the cost per examination may be lower and would vary by country.

The GDG notes that health related costs may be higher if additional tests beyond mammogram are ordered as a result of opportunistic screening.

The GDG also notes that the definition of organised screening may vary from country to country in Europe. The GDG agreed by consensus that the resources required would vary.

What is the certainty of the evidence of resource requirements (costs)?
Low *
* Possible answers: ( Very low , Low , Moderate , High , No included studies )
Research Evidence
The quality is low due to imprecision and indirectness. Two studies reported organised screening as a dominant strategy, that is more effective and less costly and the other one did not. The research was further downgraded for imprecision and indirectness.
Additional Considerations

The GDG suggests that local data may be available in their own languages, and not published, to inform cost-effectiveness evidence. The GDG also notes that grey literature may also inform cost-effectiveness decision-making locally.


Does the cost-effectiveness of the intervention favor the intervention or the comparison?
Probably favors the intervention *
* Possible answers: ( Favors the comparison , Probably favors the comparison , Does not favor either the intervention or the comparison , Probably favors the intervention , Favors the intervention , Varies , No included studies )
Research Evidence
Cost-effectiveness of organised vs. opportunistic screening


Additional Considerations

The GDG reviewed evidence incorporated from three research studies (Neeser K, 2007, de Gelder R, 2009, Schiller-Fruehwirth I, 2017). Two studies demonstrated that organised screening was dominant; in the Neeser (2007) study the ICER was 75,602 Euros per life year gained. As one may expect that health benefits are higher in organised screening, costs in relation to these benefits will porbably be favoured. Costs may differ, but even if they are higher or lower, in most cases, organised screening will be cost-effective.

The GDG agreed by consensus that the cost-effectiveness would probably favour the intervention in most settings.

What would be the impact on health equity?
Increased *
* Possible answers: ( Reduced , Probably reduced , Probably no impact , Probably increased , Increased , Varies , Don't know )
Additional Considerations

Palencia et al. (Palència L, 2010) performed a cross-sectional study using individual-level data from the WHO World Health Survey (2002) and data regarding the implementation of cancer screening programmes. The study population consisted of women from 22 European countries who participated in cervical and breast cancer screening programmes. A total of 4784 women aged 50 to 69 years participated in breast cancer screening.

Socio-economic inequalities (comparing highest with lowest educational level) were found in countries with opportunistic screening, but not in those with national (organised) screening programmes.

In certain country settings, women would have to pay for opportunistic screening, whereas with organised screening they would not have to pay. In this context, organised screening would increase equity.

The GDG noted that the impact of organised screening on equity may vary based on the participation rate in organised screening. As agreement could not be reached, voting was conducted among members without CoI: 15 members voted in favour of ‘increased’, 5 members voted in favour of ‘probably increased’.

Is the intervention acceptable to key stakeholders?
Varies *
* Possible answers: ( No , Probably no , Probably yes , Yes , Varies , Don't know )
Additional Considerations

The GDG agreed that stakeholder acceptability of organized screening may vary, depending on the stakeholder and their setting.

Radiologists may not favour organised screening programmes in certain contexts, depending on funding considerations. Also accepatability depends on the healthcare system and the incentives given to the different types of screening.

Policy-makers may not find this intervention feasible if organised screening is not currently implemented due to the new administrative costs associated with it.
Kalecinski at al.
(Kalecinski J, 2015) reported the results from a qualitative interview in 48 women from a randomly selected sample of women who were invited to attend organised breast cancer screening in 13 French departments between 2010 and 2011.

Twenty-seven women chose the organised screening programme, which they considered to be trustworthy, as negative mammograms are double checked by a second radiologist. Twenty-one women preferred individual screening, which they considered to be more reliable, less anonymous and providing them with more liberty to take control of their own health.

Women that would want to participate in screening may find this intervention acceptable. Some women may not wish to receive invitations for organised screening programmes depending on their preferences.

Is the intervention feasible to implement?
Varies *
* Possible answers: ( No , Probably no , Probably yes , Yes , Varies , Don't know )
Additional Considerations

There may be some other barriers to implementation in addition to the economic ones that may be strong in certain settings for the feasibility of organised screening programmes. Barriers related to acceptability discussed above, such as that of radiologists, may impact the feasibility of implementing organised screening programmes.

Voting was conducted among members without CoI because agreement was not reached by consensus: 13 members voted in favour of ‘varies’, 5 members voted in favour of ‘probably yes’ and 2 members voted in favour of ‘yes’.


References summary

  • Ferroni E, Camilloni L Jimenez B Furnari G Borgia P Guasticchi G Giorgi Rossi P, [Methods to increase participation Working Group. How to increase uptake in oncologic screening: a systematic review of studies comparin population-based screening programs and spontaneous access] Prev Med; 2012
  • Hofvind S, Geller B Skaane P, [Mammographic features and histopathological findings of interval breast cancers] Acta Radiol; 2008
  • Palència L, Espelt A Rodríguez-Sanz M Puigpinós R Pons-Vigués M Pasarín MI Spadea T Kunst AE Borrell C, [Socio-economic inequalities in breast and cervical cancer screening practices in Europe: influence of the type of screening program] Int J Epidemiol; 2010
  • Vanier A, Leux C Allioux C Billon-Delacour S Lombrail P Molinié F., [Are prognostic factors more favorable for breast cancer detected by organized screening than by opportunistic screening or clinical diagnosis? A study in Loire-Atlantique (France).] Cancer Epidemiol. ; 2013
  • Bulliard JL, Ducros C Jemelin C Arzel B Fioretta G Levi F., [Effectiveness of organised versus opportunistic mammography screening] Ann Oncol; 2009
  • Domingo L, Hofvind S Hubbard RA Román M Benkeser D Sala M Castells X, [Cross-national comparison of screening mammography accuracy measures in U.S., Norway, and Spain.] Eur Radiol.; 2016
  • Tsilidis, K. K., Papadimitriou, N., Capothanassi, D., Bamia, C., Benetou, V., Jenab, M., Freisling, H., Kee, F., Nelen, A., O'Doherty, M. G., Scott, A., Soerjomataram, I., Tjonneland, A., May, A. M., Ramon Quiros, J., Pettersson-Kymmer, U., Brenner, H., Schottker, B., Ordonez-Mena, J. M., Karina Dieffenbach, A., Eriksson, S., Bogeberg Mathiesen, E., Njolstad, I., Siganos, G., Wilsgaard, T., Boffetta, P., Trichopoulos, D., Trichopoulou, A., [Burden of Cancer in a Large Consortium of Prospective Cohorts in Europe] J Natl Cancer Inst; 2016
  • Bihrmann K, Jensen A Olsen AH Njor S Schwartz W Vejborg I Lynge E., [Performance of systematic and non-systematic ('opportunistic') screening mammography: a comparative study from Denmark] J Med Screen; 2008
  • Eichholzer M, Richard A Rohrmann S Schmid SM Leo C Huang DJ Güth U, [Breast cancer screening attendance in two Swiss regions dominated by opportunistic or organized screening] BMC Health Serv Res; 2016
  • Neeser K, et al., [Cost-effectiveness analysis of a quality-controlled mammography screening program from the Swiss statutory health-care perspective: quantitative assessment of the most influential factors] Value Health; 2007
  • Giordano L, von Karsa L Tomatis M Majek O Wolf CD Lancucki L Hofvind S Nystrom L Segnan N Ponti A, Group, the EUNICE Working, [Mammographic screening programmes in Europe: Organization, coverage and participation] J Med Screen; 2012
  • Smith-Bindman R, Chu PW Miglioretti DL Sickles EA Blanks R Ballard-Barbash R Bobo JK Lee NC Wallis MG Patnick J Kerlikowske K, [Comparison of screening mammography in the United States and the United kingdom] JAMA; 2003
  • Kalecinski J, Régnier-Denois V Ouédraogo S Dabakuyo-Yonli TS Dumas A Arveux P Chauvin F., [[Organized or individual breast cancer screening: what motivates women?]] Sante Publique; 2015
  • Schiller-Fruehwirth I, et al., [The Long-Term Effectiveness and Cost Effectiveness of Organised versus Opportunistic Screening for Breast Cancer in Austria] Value Health; 2017
  • Ferlay, J, Soerjomataram, I , Ervik, M, Dikshit, R , Eser, S , Mathers, C, Rebelo, M, Parkin, DM, Forman, D, Bray, F, [GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide] ; 2013
  • Madlensky L, Goel V Polzer J Ashbury FD, [Assessing the evidence for organised cancer screening programmes] Eur J Cancer; 2003
  • de Gelder R, Bulliard JL de Wolf C Fracheboud J Draisma G Schopper D de Koning HJ, [Cost-effectiveness of opportunistic versus organised mammography screening in Switzerland] Eur J Cancer; 2009
  • Ponti A, Anttila A Ronco G Senore C Basu P Segnan N et al. (IARC), [Cancer screening in the European Union. Report on the implementation of the Council Recommendation on cancer screening (second report)] Brussels: European Commission; 2017

Bibliography

Evidence of effects
  • Bihrmann K, Jensen A,Olsen AH,Njor S,Schwartz W,Vejborg I,Lynge E.. Performance of systematic and non-systematic ('opportunistic') screening mammography: a comparative study from Denmark. J Med Screen; 2008.
  • Bulliard JL, Ducros C, Jemelin C, Arzel B, Fioretta G, Levi F. Effectiveness of organised versus opportunistic mammography screening. Ann Oncol. 2009; 20 (7):1199-202. doi: 10.1093/annonc/mdn770. Epub 2009 Mar 12.
  • Vanier A, Leux C, Allioux C, Billon-Delacour S, Lombrail P, Molinié F. Are prognostic factors more favorable for breast cancer detected by organised screening than by opportunistic screening or clinical diagnosis? A study in Loire-Atlantique (France). Cancer Epidemiol. 2013; 37 (5): 683-7.
Acceptability
  • Kalecinski J, Régnier-Denois V,Ouédraogo S,Dabakuyo-Yonli TS,Dumas A,Arveux P,Chauvin F.. [Organized or individual breast cancer screening: what motivates women?]. Sante Publique; 2015.
Economic evidence
  • de Gelder R, Bulliard JL,de Wolf C,Fracheboud J,Draisma G,Schopper D,de Koning HJ. Cost-effectiveness of opportunistic versus organised mammography screening in Switzerland. Eur J Cancer; 2009.    
  • Neeser K, et al.. Cost-effectiveness analysis of a quality-controlled mammography screening program from the Swiss statutory health-care perspective: quantitative assessment of the most influential factors. Value Health; 2007.
  • Schiller-Fruehwirth I, et al.. The Long-Term Effectiveness and Cost Effectiveness of Organised versus Opportunistic Screening for Breast Cancer in Austria. Value Health; 2017.