Received: 14 December 2018 Revised: 21 February 2019 Accepted: 25 February 2019 DOI: 10.1002/pon.5041 REVIEW Systematic review on women's values and preferences concerning breast cancer screening and diagnostic services Alexander G. Mathioudakis1,2 | Minna Salakari3 | Liisa Pylkkanen4,5 | Zuleika Saz‐Parkinson4 | Anke Bramesfeld4,6 | Silvia Deandrea4,7 | Donata Lerda4 | Luciana Neamtiu4 | Hector Pardo‐Hernandez1,8 | Ivan Solà1,8 | Pablo Alonso‐Coello1,8 1 Biomedical Research Institute (IIB Sant Pau), Iberoamerican Cochrane Centre, Barcelona, Abstract Spain Background: There is still lack of consensus on the benefit‐harm balance of breast 2 Division of Infection, Immunity and Respiratory Medicine, Faculty of Biology, cancer screening. In this scenario, women's values and preferences are crucial for Medicine and Health, University of developing health‐related recommendations. In the context of the European Commis- Manchester, Manchester, UK 3 sion Initiative on Breast Cancer, we conducted a systematic review to inform the Department of Public Health, Faculty of Medicine, University of Turku, Turku, Finland European Breast Guidelines. 4 Joint Research Centre, European Methods: We searched Medline and included primary studies assessing women's Commission, Ispra, Italy 5 values and preferences regarding breast cancer screening and diagnosis decision Clinico‐Pharmacological Unit, Finnish Medicines Agency Fimea, Turku, Finland making. We used a thematic approach to synthesise relevant data. The quality of 6 Institute for Epidemiology Social Medicine evidence was determined with GRADE, including GRADE CERQual for qualitative and Health System Research, Hanover Medical research. School, Hannover, Germany 7 Health Protection Agency, Metropolitan city Results: We included 22 individual studies. Women were willing to accept the of Milan, Italy psychological and physical burden of breast cancer screening and a significant risk 8 CIBER de Epidemiología y Salud Pública of overdiagnosis and false‐positive mammography findings, in return for the benefit (CIBERESP), Barcelona, Spain of earlier diagnosis. The anxiety engendered by the delay in getting results of Correspondence diagnostic tests was highlighted as a significant burden, emphasising the need for Zuleika Saz‐Parkinson, European Commission, Joint Research Centre, Via E. Fermi, 2749. rapid and efficient screening services, and clear and efficient communication. TP127, I‐21027 Ispra (VA), Italy. Email: zuleika.saz‐parkinson@ec.europa.eu The confidence in the findings was low to moderate for screening and moderate for diagnosis, predominantly because of methodological limitations, lack of adequate Funding information European Commission, Joint Research Centre; understanding of the outcomes by participants, and indirectness. Fellowship in Guidelines Methodology by Conclusions: Women value more the possibility of an earlier diagnosis over the European Respiratory Society, Grant/Award Number: MTF 2015–01 risks of a false‐positive result or overdiagnosis. Concerns remain that women may not understand the concept of overdiagnosis. Women highly value time efficient Alexander Mathioudakis and Minna Salakari are equally contributing first authors. -------------------------------------------------------------------------------------------------------------------------------- This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Psycho‐Oncology Published by John Wiley & Sons Ltd. Psycho‐Oncology. 2019;28:939–947. wileyonlinelibrary.com/journal/pon 939 940 MATHIOUDAKIS ET AL. screening processes and rapid result delivery and will accept some discomfort for the peace of mind screening may provide. K E Y W OR D S breast cancer, cancer, diagnostic services, oncology, patient‐centred care, patient preference, practice guideline, screening 1 | I N T RO D U CT I O N 2 | METHODS Breast cancer is the most common cancer in women and one of 2.1 | Design the leading causes of all cancer deaths both in Europe and worldwide.1 Breast cancer screening with mammography, the only A systematic literature review, following standard Cochrane Collabo- population‐based method for the early detection of breast cancer ration methodology,10 was performed to address the following currently used, has been shown to reduce breast cancer mortality in question: What are the values and preferences of women regarding women aged 50 to 74 years2 and is widely implemented in most decision making on breast cancer screening and diagnosis. The review European countries.3 However, mammography screening is also protocol is registered in PROSPERO (https://www.crd.york.ac.uk/ associated with potential important undesirable effects, including PROSPERO/display_record.php?RecordID=41487). overdiagnosis, and hence overtreatment, and false‐positive mammog- raphy results.4 False‐positive mammography findings may cause 2.2 | Search strategy and selection criteria psychological distress.5 The balance between benefits and harms of screening becomes less favourable after 74 years of age and at 90; Medline (assessed through Ovid) was searched using terms regarding harms are considered to outweigh benefits, largely as a consequence breast neoplasm/cancer; screening; diagnosis; different screening of overdiagnosis.6 There is still a lack of consensus on the and diagnosis outcomes; values, and preferences (complete search benefit‐harm balance of breast cancer screening thus underlining the strategy in Appendix 1). As a source for individual studies, systematic need for women to receive balanced and adequate information in reviews with no time restrictions were searched. For primary studies, order to make informed decisions concerning their participation in publications from 2006 until the end of June 2018 were included. screening programmes. Only studies in English were included. The European Commission Initiative on Breast Cancer (ECIBC) Only studies examining women's preferences for breast cancer (http://ecibc.jrc.ec.europa.eu/) uses the GRADE approach when screening versus no screening or about the potentially available breast formulating recommendations for breast cancer screening and cancer diagnostic alternatives, studies evaluating how women value diagnosis. This includes the use of Evidence to Decision (EtD) breast cancer screening and diagnosis outcomes, and those examining frameworks when moving from evidence to recommendations.7 The the choices women facing a breast cancer screening or diagnostic EtD frameworks provide an explicit and transparent system for decision make, when informed about the expected desirable and decision making that can help ensure all important criteria, informed undesirable outcomes, were included. We excluded studies restricted by the best available research evidence, needed to make a decision to women's knowledge, views, behaviours, perceptions, attitudes, are considered. One of these criteria is how those affected by a and expectations regarding breast cancer screening and diagnosis. recommendation value the main desirable and undesirable outcomes We also excluded those conducted in countries outside the of the interventions considered. In the case of recommendations on Organisation for Economic Co‐operation and Development (OECD) breast cancer screening, this means considering women's values and or those focusing exclusively on minorities from geographic regions preferences regarding potential consequences of participating in outside Europe. screening. Women's values and preferences refer to the relative weight those affected by a recommendation place on the different outcomes, such 2.3 | Screening and data collection as the potential benefits, harms, costs, limitations, and inconveniences of the available interventions or management options.8 Inclusion of One reviewer screened the search results based on title and abstract. women's values in the screening decision making process has been Two reviewers independently confirmed eligibility of relevant articles proposed for decades now,9 but its implementation is still suboptimal. based on the full text, and disagreement between researchers GRADE's EtD frameworks provide guidance on how to incorporate was solved by the third reviewer. One reviewer extracted the main women's values and preferences while drafting clinical recommenda- characteristics and main findings of the included studies in a tions. This systematic review was thus conducted to inform ECIBC's tabular format. Another reviewer checked the extracted data for clinical recommendations' development process. accuracy. The synthesis of the results is described narratively and MATHIOUDAKIS ET AL. 941 is based on the identification and grouping of themes reported in the is presented in Table 1. Evidence profiles including main findings included studies. and certainty of evidence, for both screening and diagnosis, are Risk of bias assessment was carried out using the domains included in Appendix 2. 11 suggested in the GRADE approach for quantitative studies and the Critical Appraisal Skills Programme (CASP) checklist12 for qualitative studies. The confidence (quality or certainty) of the evidence was 3.1 | Screening rated from high to very low considering the standard GRADE domains for quantitative data.10 For qualitative studies, the CERQual We identified the following main themes that contribute to how (Confidence in the Evidence from Reviews of Qualitative Research) women value the main outcomes of screening: risk of overdiagnosis approach was used. 13 The results of the systematic review were and false‐positive screening results, burden of breast cancer screening, reported according to the PRISMA (preferred reporting items for and challenges elderly women face when making a decision to partic- systematic reviews and meta‐analyses) statement. 14 ipate in screening programmes. 3.1.1 | Overdiagnosis 3 | RESULTS Five studies, four conducted in Europe15-18 and one in Australia,19 The search yielded 5063 unique references, of which 96 were evaluated women's knowledge and acceptability of the risk of overdi- deemed potentially eligible for inclusion, based on initial screening of agnosis. Results revealed limited awareness of the risk of overdiagno- titles and abstracts. After full text appraisal, 22 individual studies sis among women. Only 29% and 53% of participants in two (15 on screening and seven on diagnosis) involving 12 174 women population‐based surveys, conducted in the United Kingdom, were were included. The PRISMA flowchart is presented in Figure 1. A aware of the concept of overdiagnosis.16,18 In a study from Spain, only tabular summary of the findings and rating of certainty of evidence 10% of women had adequate knowledge about the implications of being overdiagnosed.15 Four studies15,17-19 assessed the impact exposure to information concerning overdiagnosis has on women of screening age. Information about overdiagnosis and its implications triggered different immediate reactions among participants. These included surprise and concern regarding the undesirable psychological and physical consequences, as well as defensive reactions and mistrust of the investigators' motives. On the one hand, women considered that it would be appro- priate and fair to provide adequate information regarding overdiagno- sis to women invited for screening but, on the other, they were concerned this information may cause confusion and deter women from participating. Two studies evaluated the impact information concerning overdi- agnosis had on women's intention to participate in screening.17,18 Ninety percent of participants answered that they would probably or definitely attend screening in the future. Only 7%, especially women below the recommended screening age, actually showed a decrease in screening intention.18 Two studies evaluated the rate of overdiagnosis that women were willing to accept.16,19 On the one hand, a survey showed that they were willing to accept 15% and 31% overdiagnosis for an expected benefit of 10% and 50% reduction in cancer specific mortality, respec- tively.16 On the other hand, a focus group study, showed that a rate of 1% to 10% of overdiagnosis was perceived as completely acceptable; 30% was perceived as still acceptable by most women, but 50% was considered to be extremely high.19 The willingness to accept overdiagnosis was related to socio‐ demographic factors: those with a higher educational status accepted significantly higher levels of overdiagnosis than those with FIGURE 1 Preferred reporting items for systematic reviews and a lower educational status. Furthermore, women over 50 accepted meta‐analyses flowchart for inclusion and exclusion of the studies significantly less overdiagnosis than younger women.16 However, in 942 MATHIOUDAKIS ET AL. TABLE 1 Tabulated summary of findings and rating of the confidence in the evidence about screening Confidence in Studies Contributing Review Finding the Evidence Explanation to the Review Finding False positives Moderate There are significant concerns regarding Bolejko,20 Bolejko,21 Ganott,23 Women significantly confidence women's lack of understanding about Brodersen,22 Thompson,24 place a low value on the breast cancer screening, especially the Tosteson,25 Vass26 psychosocial and physical undesirable effects. In addition, the effects of false‐positive results. adequacy of the information provided However, women consider false‐ to the breast cancer participants, which positive results an acceptable would help them take an informed consequence of mammographic decision, seems to be inadequate. breast cancer screening. Overdiagnosis Low There are significant concerns regarding Baena‐Cañada,15 Hersch,19 Women significantly place a low confidence women's lack of understanding about Van den Bruel16 Waller,17 value on the psychosocial and breast cancer screening, especially the Waller18 physical effects of overdiagnosis. undesirable effects. For instance, Van However, women generally seem den Bruel et al reported that 10% to to consider these undesirable 14% of the participants accepted effects acceptable given their overdetection in the overall population, knowledge about the potential implying that they did not comprehend desirable consequences of breast the aims of screening and the concept cancer screening. of overdiagnosis. In addition, the information provided to breast cancer participants, which would help them take an informed decision, seems to be inadequate. Also, indirectness is a limitation of some of the included studies, which assessed adult women of any age, rather than women of screening age. another study, younger participants interpreted overdiagnosis as a In fact, over 60% of participants were prepared to accept a 20% distinctly negative factor, discouraging them from participating in false‐positive rate for a 3% probability of detecting cancer. screening.19 Two longitudinal European studies21,22 included a pooled popula- The confidence in the evidence regarding overdiagnosis was con- tion of 671 patients with false‐positive screening results, 174 sidered low. There were significant concerns regarding some studies patients diagnosed with breast cancer and 1363 matched women about whether women were adequately informed in order to fully with negative results. Here, a false‐positive mammography screening understand the extent of the risks and benefits associated with breast result was associated with consistently greater negative psychosocial cancer screening, and specifically the implications of overdiagnosis. consequences compared with a negative result, even 3 years after This can be seen, for example, in a cross‐sectional study evaluating final diagnosis. However, a study conducted in the United States25 510 British females, 15% of the participants declared that they found only a transient increase in personal anxiety after false‐ were prepared to accept overdiagnosis in the complete population, positive results, which did not persist at one year after final negative strongly suggesting that they may have not comprehended the diagnosis was made. 16 aims of screening and the concept of overdiagnosis. Indirectness Four studies assessed women's attitudes and beliefs on the effects was an additional limitation in some of the studies, as some of false‐positive mammograms towards future screening behaviour. studies included adult women of any age, rather than women at Ganott and colleagues23 reported that, prior to mammography exami- screening age. nation, 97% of women believed a false‐positive result would not deter them from screening. Tosteson et al25 reported that among women 3.1.2 | False‐positive screening results with a previous false‐positive mammography finding, the future screening intention was significantly increased compared with those The burden and acceptability of false‐positive mammography screening with a negative mammogram. These findings were confirmed by two 20-26 results was evaluated in seven studies. A European cross‐sectional qualitative studies including women with false‐positive mammography study involving 1018 women from the general population used an results.20,24 A significant proportion of women would accept the online discrete choice experiment survey to elicit patients' preferences inconvenience and anxiety associated with a higher recall rate if this regarding false‐positive results.26 Respondents highly valued the implied the possibility to detect breast cancer earlier.23 possibility of early diagnosis and were prepared to accept unnecessary The confidence in the evidence from the cross‐sectional studies follow‐up appointments as a result of a false‐positive screening result. regarding false‐positive findings was moderate because of MATHIOUDAKIS ET AL. 943 methodological limitations (significant concerns regarding inadequacy receiving the test results over the phone to be acceptable if that of information provided to participants that led to poor understanding accelerated the process.30 A cross‐sectional study including women of benefits and risks of breast cancer screening). The confidence in the who had previously undergone sentinel node biopsy with intraopera- evidence from qualitative studies was low, as there were similar tive diagnosis found similar results; 95% of participants would choose methodological limitations, but also these studies mostly evaluated to undergo the procedure again in the future, in order to have the preferences of women who had already received a false‐positive results earlier.31 Another cross‐sectional study showed that better result and their preferences may not be representative of the general communication with the radiologist performing the biopsies was population of women at screening age. Based on all available associated with lower post‐biopsy anxiety.32 evidence, the confidence in the evidence was moderate. A systematic review showed that the needs for supportive care concerning diagnosis touch upon many domains, which cluster around 3.1.3 | Burden psychological and information needs. These needs are influenced by individual clinical, demographic, emotional, psychological, or psycho- A metasynthesis27 including 21 qualitative studies, assessed barriers social characteristics of subjects.35 Finally, one study, including only for breast cancer screening from the women's perspective. The women aged 60 and over, provided information on the benefits of a authors reported several aspects of breast cancer screening that may decision aid.33 The authors did not find any significant differences in be burdensome for women including: logistical implications, such as decisional support needs based on age at diagnosis, education level, investing time and money to reach the screening site, psychological ethnicity, or presence of comorbidities. Approximately 90% of distress associated with the screening process itself, derived from fear women indicated they had received a high level of support during their of a positive result, embarrassment, and from not receiving services in cancer diagnosis. However, the desire for additional educational line with their cultural and religious beliefs. The confidence in the resources such as worksheets, consultation summaries, or workbooks evidence was moderate being limited by the insufficiency of data to assist treatment decisions was highlighted. The overall confidence and methodological limitations. in these findings concerning anxiety is moderate because of inade- quacy of data. 3.1.4 | Screening decisions among elderly women 3.2.2 | Inconvenience Two studies in the United States assessed factors that influence the decision of elderly women (aged 80 and over) to participate in As part of a trial in Australia, a cross‐sectional study with 49 women 28,29 screening programmes. A qualitative study highlighted a more assessed their experience with contrast‐enhanced spectral mammog- pronounced variability in elderly women's preferences.28 Factors raphy (CESM) compared with contrast‐enhanced magnetic resonance influencing more their decision to be screened included women's imaging (MRI) (CEMRI) during preoperative breast cancer staging.36 perceived individual risk of breast cancer, physician's advice, previous Significantly higher overall preference towards CESM was shown, screening habits and experiences with mammography, as well as social with faster procedure time, greater comfort, and lower noise level and family influences. The most important reasons for declining cited as the commonest reasons. Participants also reported signifi- screening were the decision not to undergo a possible operation cantly lower rates of anxiety during CESM compared with CEMRI. given their age, and the discomfort associated with an additional The overall confidence in these findings is moderate because of inad- 28 clinical visit. In a cross‐sectional study, women aged 80 and equacy of data. older who decided not to undergo breast cancer screening, ranked their age and doctor's counselling as the factors mostly influencing their decision.29 4 | DISCUSSION AND CONCLUSIONS 3.2 | Diagnosis 4.1 | Main findings 3.2.1 | Anxiety Our review shows that women place a low value on the psychosocial and physical effects of overdiagnosis and false‐positive mammography One of the main themes concerning diagnostic procedures in breast screening results, as well on the inconvenience and burden associated cancer is the avoidable anxiety, mostly because of inadequacy of the with it. Women generally consider these undesirable effects accept- information regarding procedures and the delay in receiving test able, recognising the potential benefits of breast cancer screening. 30-33 results. This theme was reported in four cross‐sectional studies. However, the confidence in the evidence supporting these findings one qualitative study,34 and one systematic review35. is low to moderate because of methodological limitations. Regarding Women highly valued receiving diagnostic results in a timely diagnosis, women highly appreciate avoiding anxiety caused by delays manner. Twelve percent of women, who underwent image‐guided in the receipt of results or suboptimal communication with health care breast biopsies in the United States, were not even satisfied with a professionals. They also appear to value faster procedures over the 1‐day waiting time for their results. However, 90% of them found inconvenience associated with them. 944 MATHIOUDAKIS ET AL. 4.2 | Our results in the context of previous results have substantial other impacts on women's health behaviour and well‐being. Women with false‐positive findings have been shown to 4.2.1 | Overdiagnosis make a greater use of health care services and have reported lower quality of life than those without false‐positive findings.40 The level of overdiagnosis that women were willing to accept was Healthy women at screening age were prepared to accept a high relatively high, up to 30%.16,19 The most commonly reported risk of false‐positive screening results in order to detect breast cancer estimates of overdiagnosis from screening programmes are around early. Irrespective of false‐positive findings, the screening intention 10% and vary widely.4 Thus, the level of overdiagnosis women were remained high and was even higher among those with a false‐positive willing to accept was on the high end of the estimated average figures. result compared with those with a negative result. Despite significant The high rates of overdiagnosis women were willing to accept could psychosocial burden caused by false‐positive screening results, put into question whether the concept was really understood by study women acknowledge the value of mammography screening. Our participants. According to our review, women's knowledge and results are consistent with another recent systematic review and understanding concerning overdiagnosis were variable, and in general meta‐synthesis by the Health Care Ontario, assessing the burden of limited, with only about 30% to 50% of women being aware of the false‐positive and false‐negative results and their impact on women's concept and only 10% having adequate knowledge about its implica- screening intentions.41 tions. Results from a recently published study from the United Kingdom revealed that almost one‐third of participants reported 4.3 | Screening decision among elderly women having previously encountered the term overdiagnosis, but responses often indicated they had very limited knowledge about its Elderly women's preferences regarding breast cancer screening were implications.37 more heterogeneous. This is consistent with the decreased benefit Women appear to overestimate the benefits of mammography to risk ratio that these women face.42 For these reasons, screening screening. Up to 70% of women overestimated the possibility of of elderly women is not recommended by the majority of available having breast cancer detected during screening.23 The fear of getting guidelines.42 breast cancer may also lead women to be willing to accept a higher level of overdiagnosis. Population‐based studies have consistently 4.3.1 | Diagnostic procedures shown that between a quarter to a half of the general population worry to some extent about getting some type of cancer, and 5% to The importance of the quick receipt of diagnostic results has been 10% experience extreme worry.38 Altogether, these findings may previously emphasised in several studies.43,44 A very high number of partially explain the high levels of overdiagnosis women were willing women would choose to undergo the diagnostic procedure again in to accept and also underline the importance of providing women with the future in order to have the results earlier.31 A substantial propor- balanced information concerning the benefits and harms of breast tion of women are also willing to accept the inconvenience and cancer screening. anxiety associated with a higher recall rate if it results in earlier breast cancer detection.23 Altogether, these findings show that women 4.2.2 | False‐positive findings appear to value more the possibility of an earlier and accurate detec- tion of cancer over the inconvenience and anxiety associated with European studies show that false‐positive screening results were asso- the diagnostic process itself. ciated with long‐term negative psychosocial consequences,20-22 Our results are in agreement with Pahade and coworkers,45 who 25 whereas a US study showed only a transient increase in anxiety. have shown that most patients showed decreased anxiety after These conflicting results may be related to the different instruments receiving the examination results from the radiologist. Although it is used to measure anxiety. European studies used a screening‐specific generally assumed in clinical practice that the best way for patients validated questionnaire “Consequences of Breast Cancer Screening” to receive diagnostic results is to personally discuss them with a qual- specifically developed to assess the long term psychosocial conse- ified professional, Brandon and colleagues reported that most women quences of false‐positive mammography screening, while the US study (90%) found it acceptable to receive the results even over the used the 6 question short‐form (STAI‐6) of the Spielberger State‐Trait phone.29 This finding can also partially explain the higher value women Anxiety Inventory (STAI) instrument focusing on measurement of place on fast delivery of test results over the method chosen to com- general anxiety. Previous studies have shown inconsistent results municate them. concerning psychosocial consequences of false‐positive results, with some women showing persistent and others only transient anxiety.39 4.4 | Study limitations A systematic review focusing on the UK population reported that receiving a false‐positive screening mammogram caused breast Our review has several strengths. To the best of our knowledge, this is cancer‐specific psychological distress that may endure up to 3 years, the first systematic review focusing specifically on women's values and the degree of distress appears to be related to the level of inva- and preferences about breast cancer screening and diagnostic ser- siveness of the assessment procedure.34 False‐positive results may vices. In our evaluation, we applied rigorous methods including the MATHIOUDAKIS ET AL. 945 GRADE approach and CERQual methodology for evidence synthesis Neither patient consent nor ethical committee approval was and quality evaluation of qualitative results. necessary as, because of the type of work presented (a systematic The main limitation of our findings relates to the methodological review of the literature), this is not needed. limitations of the included studies. More specifically, we are not confident that the participants of several of the included studies received balanced information in order to understand complex CONFLIC T OF INT E RE ST S concepts, such as overdiagnosis. Our study is also limited by the AM, HPH, IS, and PAC were working at the time when this work was relatively small number of studies and small sample size in some of carried out for Iberoamerican Cochrane Collaboration, which received them. Another limitation is that we only included studies published payments from the European Commission to develop the systematic in English. However, the included studies evaluated a wide variety reviews informing the ECIBC recommendations. LP, ZSP, AB, SD, of populations and countries, so we do not believe this limits the DL, and LN were working, or are working, for the European Commis- generalisation of our findings. The restriction of the search to the last sion, JRC. No other interests are declared. 10 years for primary studies may have also limited our findings, but we are confident that the most important outcomes, such as overdiagnosis, have been mostly studied within this period. The FUNDING INFORMATION inclusion of previous systematic reviews also limits these concerns. The systematic review was carried out by Iberoamerican Cochrane In addition, more recent studies are likely to be more relevant Collaboration under Framework contract 443094 for procurement of because diagnostic and therapeutic options and outcomes of breast services between European Commission Joint Research Centre and cancer have significantly changed over the last decade. Asociación Colaboración Cochrane Iberoamericana. Administrative Arrangement SANCO/2012/C – 17.030600/12//SI2.635313 4.5 | Clinical implications between the European Commission Directorate‐General Health and Food Safety and the Directorate‐General Joint Research Centre. The low‐to‐moderate quality of the evidence for breast cancer AGM was funded by a Fellowship in Guidelines Methodology by the screening and moderate quality evidence for breast cancer diagnosis European Respiratory Society (MTF 2015‐01). underlines the need to carry out more well‐designed studies on women's values and preferences, including also minorities, women AUTHORS C ONTRIBU TIONS with disabilities, with different cultural, religious, educational, and Alexander Mathioudakis, Ivan Solà, and Pablo Alonso‐Coello were economic backgrounds. Such studies would provide valuable data responsible for conducting the systematic review, including the inter- to panels developing clinical or public health recommendations, pretation of the results and the drafting of the full report of the system- as well as to policy‐makers when making coverage or public health atic review (available upon request). Alexander Mathioudakis and decisions. Hector Pardo‐Hernandez conducted the search and data extraction. Health care community should focus on providing clear, adequate, Liisa Pylkkanen, Silvia Deandrea, and Donata Lerda contributed to the and balanced information on the benefits and risks of breast cancer definition of the research protocol and provided comments to the pre- screening to ensure informed participation. In this context, the use liminary results. Alexander Mathioudakis, Pablo Alonso‐Coello, Minna of decision aids could be helpful.46 A particular emphasis should be Salakari, and Liisa Pylkkänen drafted the first version of the article. All made on the communication of overdiagnosis, which was poorly authors contributed to the interpretation and reporting of the results understood based on our findings. Clinicians should also be and provided comments on subsequent versions of the article. All encouraged to improve their communication skills and health care authors read and approved the final manuscript prior submission. systems to provide adequate and timely information about test results. ORCID E TH I CAL BA CK G R OU N D Alexander G. Mathioudakis https://orcid.org/0000-0002-4675-9616 Liisa Pylkkanen https://orcid.org/0000-0002-8375-6035 The European Commission Initiative on Breast Cancer (ECIBC) (http:// Zuleika Saz‐Parkinson https://orcid.org/0000-0002-3518-5899 ecibc.jrc.ec.europa.eu/) uses the GRADE approach when formulating Silvia Deandrea https://orcid.org/0000-0003-1509-951X recommendations for breast cancer screening and diagnosis. This Hector Pardo‐Hernandez https://orcid.org/0000-0003-3714-0309 includes the use of Evidence to Decision (EtD) frameworks that Ivan Solà https://orcid.org/0000-0003-0078-3706 provide an explicit and transparent system for decision making to Pablo Alonso‐Coello https://orcid.org/0000-0002-8001-8504 ensure all important criteria needed to make a decision are considered. One of these criteria is how those affected by a recommendation RE FE RE NC ES value the main desirable and undesirable outcomes of the interven- 1. Ferlay J, Forman D, Mathers CD, Bray F. Breast and cervical cancer tions considered. This systematic review was thus conducted to in 187 countries between 1980 and 2010. Lancet. 2012;379 inform ECIBC's clinical recommendations' development process. (9824):1390‐1391. https://doi.org/10.1016/S0140‐6736(12)60595‐9 946 MATHIOUDAKIS ET AL. 2. IARC Handbook. Breast Cancer Screening. 15. IARC Handbooks f consequences of a false‐positive screening mammography. J Clin Nurs. Cancer Prevention Lyon, France: IARC; 2016. 2014;23(13‐14):2053‐2062. 3. Deandrea S, Molina‐Barceló A, Uluturk A, et al. Presence, characteris- 21. Bolejko A, Hagell P, Wann‐Hansson C, Zackrisson S. Prevalence, long‐ tics and equity of access to breast cancer screening programmes in term development, and predictors of psychosocial consequences of 27 European countries in 2010 and 2014. Results from an international false‐positive mammography among women attending population‐ survey. Prev Med. 2016;91:250‐263. based screening. Cancer Epidemiol Biomarkers Prev. 2015;24(9): 4. Marmot MG, Altman DG, Cameron DA, Dewar JA, Thompson SG, 1388‐1397. Wilcox M. The benefits and harms of breast cancer screening: an 22. Brodersen J, Siersma V. Long‐term psychosocial consequences of independent review. Br J Cancer. 2013;108(11):2205‐2240. false‐positive screening mammography—a cohort study with 3‐year 5. Salz T, Richman AR, Brewer NT. Meta‐analyses of the effect of false‐ follow‐up. Ann Fam Med. 2013;11(2):106‐115. positive mammograms on generic and specific psychosocial outcomes. 23. Ganott MA, Sumkin JH, King JL, et al. Screening mammography: do Psychooncology. 2010;19(10):1026‐1034. women prefer a higher recall rate given the possibility of earlier detec- 6. van Ravesteyn NT, Stout NK, Schechter CB, et al. Benefits and harms tion of cancer? Radiology. 2006;238(3):793‐800. of mammography screening after age 74 years: model estimates of 24. Thompson J, Coleman R, Colwell B, et al. Levels of distress in breast overdiagnosis. J Natl Cancer Inst. 2015;107(7):djv103‐djv103. cancer survivors approaching discharge from routine hospital follow‐ 7. Schünemann HJ, Mustafa R, Brozek J, et al. 2016. GRADE Guidelines: up. Psychooncology. 2013;22(8):1866‐1871. 16. GRADE evidence to decision frameworks for tests in clinical 25. Tosteson AN, Fryback DG, Hammond CS, et al. Consequences of false‐ practice and public health. J Clin Epidemiol. 2016;76:89‐98. positive screening mammograms. JAMA Intern Med. 2014;174(6): 8. Muhlbacher AC, Juhnke C. Patient preferences versus physicians' 954‐961. judgement: does it make a difference in healthcare decision making? 26. Vass CM, Rigby D, Payne K. Investigating the heterogeneity in Appl Health Econ Health Policy. 2013;11(3):163‐180. women's preferences for breast screening: does the communication 9. Pellissier JM, Venta ER. Introducing patient values into the decision of risk matter? Value Health. 2018 Feb;21(2):219‐228. making process for breast cancer screening. Women Health. 1996; 27. Azami‐Aghdash S, Ghojazadeh M, Sheyklo SG, et al. Breast Cancer 24(4):47‐67. Screening Barriers from the Womans Perspective: a Meta‐synthesis. 10. Higgins J, Green S. Cochrane Handbook for Systematic Reviews of Asian Pac j cancer prev: APJCP. 2015;16(8):3463‐3471. Interventions. West Sussex, England: John Wiley & Sons; 2011. 28. Schonberg MA, Ramanan RA, McCarthy EP, Marcantonio ER. Decision 11. Guyatt GH, Oxman AD, Schunemann HJ, Tugwell P, Knottnerus A. making and counseling around mammography screening for women GRADE guidelines: a new series of articles in the Journal of Clinical aged 80 or older. J Gen Intern Med. 2006;21(9):979‐985. Epidemiology. J Clin Epidemiol. 2011;64(4):380‐382. 29. Schonberg MA, McCarthy EP, York M, Davis RB, Marcantonio ER. 12. Critical Appraisal Skills Programme (CASP) 2015. http://www.casp‐uk. Factors influencing elderly women's mammography screening net/casp‐tools‐checklists decisions: implications for counseling. BMC Geriatr. 2007;7(1):26. 13. Lewin S, Glenton C, Munthe‐Kaas H, et al. Using qualitative evidence 30. Brandon CJ, Mullan PB. Patients' perception of care during image‐ in decision making for health and social interventions: an approach to guided breast biopsy in a rural community breast center: communica- assess confidence in findings from qualitative evidence syntheses tion matters. J cancer educ: the official journal of the American (GRADE‐CERQual). PLoS Med. 2015;12(10):e1001895. https://doi. Association for Cancer Education. 2011;26(1):156‐160. org/10.1371/journal.pmed.1001895 31. Chicken DW, Sivanadarajah N, Keshtgar MRS. Patients' view on intra- 14. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for operative diagnosis of sentinel nodes in breast cancer: is it an reporting systematic reviews and meta‐analyses of studies that evalu- automatic choice? Int j surg (London, England). 2007;5(2):76‐80. ate healthcare interventions: explanation and elaboration. BMJ. 32. Miller LS, Shelby RA, Balmadrid MH, et al. Patient anxiety before and 2009;339(jul21 1):b2700. immediately after imaging‐guided breast biopsy procedures: impact 15. Baena‐Cañada JM, Rosado‐Varela P, Expósito‐Álvarez I, González‐ of radiologist‐patient communication. J Amer Coll Radiol: JACR. Guerrero M, Nieto‐Vera J, Benítez‐Rodríguez E. Women's perceptions 2013;10(6):423‐431. of breast cancer screening. Spanish screening programme survey. 33. Presutti R, D'Alimonte L, McGuffin M, et al. Decisional support Breast. 2014;23(6):883‐888. https://doi.org/10.1016/j.breast.2014. throughout the cancer journey for older women diagnosed with early 09.010 stage breast cancer: a single institutional study. J cancer educ: the offi- 16. Van den Bruel A, Jones C, Yang Y, Oke J, Hewitson P. People's willing- cial journal of the American Association for Cancer Education. ness to accept overdetection in cancer screening: population survey. 2014;29(1):129‐135. BMJ. 2015;350:h980. https://doi.org/10.1136/bmj.h980 34. Bond M, Pavey T, Welch K, et al. Psychological consequences of 17. Waller J, Douglas E, Whitaker KL, Wardle J. Women's responses to false‐positive screening mammograms in the UK. Evid Based Med. information about overdiagnosis in the UK breast cancer screening 2013;18(2):54‐61. https://doi.org/10.1136/eb‐2012‐100608 programme: a qualitative study. BMJ Open. 2013;3(4). pii: e002703 35. Fiszer C, Dolbeault S, Sultan S, Brédart A. Prevalence, intensity, and pre- 18. Waller J, Whitaker KL, Winstanley K, Power E, Wardle J. A survey dictors of the supportive care needs of women diagnosed with breast study of women's responses to information about overdiagnosis cancer: a systematic review. Psychooncology. 2014;23(4):361‐374. in breast cancer screening in Britain. Br J Cancer. 2014;111(9): 36. Hobbs MM, Taylor DB, Buzynski S, Peake RE. Contrast‐enhanced 1831‐1835. spectral mammography (CESM) and contrast enhanced MRI (CEMRI): 19. Hersch J, Jansen J, Barratt A, et al. Women's views on overdiagnosis in Patient preferences and tolerance. J Med Imaging Radiat Oncol. breast cancer screening: a qualitative study. BMJ. 2013;346:f158. 2015;59(3):300‐305. https://doi.org/10.1136/bmj.f158 37. Ghanouni A, Meisel SF, Renzi C, Wardle J, Waller J. Survey of public 20. Bolejko A, Zackrisson S, Hagell P, Wann‐Hansson C. A roller coaster of definitions of the term ‘overdiagnosis’ in the UK. BMJ Open. emotions and sense‐‐coping with the perceived psychosocial 2016;6(4):e010723. https://doi.org/10.1136/bmjopen‐2015‐010723 MATHIOUDAKIS ET AL. 947 38. Wrinten C, McGregor LM, Heinrich M, et al. What do people fear 45. Pahade J, Couto C, Davis RB, Patel P, Siewert B. Rosen MP.2012. about cancer? A systematic review and meta‐synthesis of cancer fears Reviewing imaging examination results with a radiologist immediately in the general population. Psychooncology. 2017;26(8):1070‐1079. after study completion: patient preferences and assessment of feasibil- https://doi.org/10.1002/pon.4287 ity in an academic department. Am J Roentgenol. 2012;199(4):844‐851. 39. Nelson HD, Cantor A, Humphrey L, Fu R, Pappas M, Daeges M, Griffin 46. Martínez‐Alonso M, Carles‐Lavila M, Pérez‐Lacasta MJ, Pons‐ J. Screening for breast cancer: a systematic review to update the Rodríguez A, García M, Rué M. Assessment of the effects of decision 2009 U.S. preventive services task force recommendation. evidence aids about breast cancer screening: a systematic review and meta‐ syntheses, No.124. Rockville (MD): Agency for Healthcare Research analysis. BMJ Open. 2017;7(10):e016894. https://doi.org/10.1136/ and Quality (US); 2016. Report No.: 14‐05201‐EF‐1. bmjopen‐2017‐016894 40. van der Steeg A, Keyzer‐Dekker C, De Vries J, Roukema JA. Effect of abnormal screening mammogram on quality of life. Br J Surg. 2011; 98(4):537‐542. https://doi.org/10.1002/bjs.7371 SUPPORTING INFORMATION 41. Health Quality Ontario. Women's experiences of inaccurate breast cancer Additional supporting information may be found online in the screening results: a systematic review and qualitative meta‐synthesis. Supporting Information section at the end of the article. Ont Health Technol Assess Ser. 2016;16(16):1‐22. eCollection 2016 42. Jørgensen KJ, Kalager M, Barratt A, et al. Overview of guidelines on breast screening: why recommendations differ and what to do about it. Breast. 2017;31:261‐269. How to cite this article: Mathioudakis AG, Salakari M, 43. Hislop T, Harris S, Jackson J, et al. Satisfaction and anxiety for women Pylkkanen L, et al. Systematic review on women's values and during investigation of an abnormal screening mammogram. Breast preferences concerning breast cancer screening and Cancer Res Treat. 2002;76(3):245‐254. diagnostic services. Psycho‐Oncology. 2019;28:939–947. 44. Molina‐Barceló A, Salas Trejo D, Miranda García J. Women's satisfac- tion with waiting times for further investigation in breast cancer https://doi.org/10.1002/pon.5041 screening. Gac Sanit. 2011;25(5):357‐262.