Imaging surveillance programs for women at high breast cancer risk in Europe: Are women from ethnic minority groups adequately included? (Review)

  • Authors:
    • Karen Belkić
    • Miri Cohen
    • Brigitte Wilczek
    • Sonia Andersson
    • Anne H. Berman
    • Marcela Márquez
    • Vladana Vukojević
    • Miriam Mints
  • View Affiliations

  • Published online on: June 26, 2015     https://doi.org/10.3892/ijo.2015.3063
  • Pages: 817-839
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Abstract

Women from ethnic minority groups, including immigrants and refugees are reported to have low breast cancer (BC) screening rates. Active, culturally-sensitive outreach is vital for increasing participation of these women in BC screening programs. Women at high BC risk and who belong to an ethnic minority group are of special concern. Such women could benefit from ongoing trials aimed at optimizing screening strategies for early BC detection among those at increased BC risk. Considering the marked disparities in BC survival in Europe and its enormous and dynamic ethnic diversity, these issues are extremely timely for Europe. We systematically reviewed the literature concerning European surveillance studies that had imaging in the protocol and that targeted women at high BC risk. The aim of the present review was thereby to assess the likelihood that women at high BC risk from minority ethnic groups were adequately included in these surveillance programs. Twenty-seven research groups in Europe reported on their imaging surveillance programs for women at increased BC risk. The benefit of strategies such as inclusion of magnetic resonance imaging and/or more intensive screening was clearly documented for the participating women at increased BC risk. However, none of the reports indicated that sufficient outreach was performed to ensure that women at increased BC risk from minority ethnic groups were adequately included in these surveillance programs. On the basis of this systematic review, we conclude that the specific screening needs of ethnic minority women at increased BC risk have not yet been met in Europe. Active, culturally-sensitive outreach is needed to identify minority women at increased BC risk and to facilitate their inclusion in on-going surveillance programs. It is anticipated that these efforts would be most effective if coordinated with the development of European-wide, population-based approaches to BC screening.

1. Breast cancer survival disparities, ethnicity and related issues for Europe

Breast cancer is the most commonly diagnosed malignancy and a leading cause of cancer deaths among women in Europe (1,2). Survival after diagnosis of breast cancer varies markedly across Europe; this is attributed to differences in stage at diagnosis (3). Early breast cancer detection can be achieved through screening which, when followed by appropriate assessment and management, has been demonstrated to significantly reduce mortality from breast cancer (4,5).

The importance of screening has been particularly emphasized for women with high breast cancer risk, for whom there is a greater likelihood of more aggressive tumors presenting at a younger age (68). Intensive screening using various imaging modalities is reportedly tolerated and preferred by women at high risk, compared to options such as prophylactic mastectomy (9,10). Many investigations have focused upon finding the best strategies for screening surveillance of women with high breast cancer risk (11,12). In the UK women at very high risk of familial breast cancer are being offered annual surveillance with magnetic resonance imaging from age 30 to 49 years and annual mammography from the age of 40–69 (13).

A critical challenge is to effectively identify women from the general population who are at high risk for breast cancer, so that they can benefit from these more intensive screening surveillance strategies. Breast cancer risk assessment models have been based upon family history, including age of disease onset. However, it has been reported that relying on family history can be tenuous, especially for identifying BRCA1/2 mutation carriers (1416).

Certain ethnic groups within Europe are recognized to have a high prevalence of BRCA1/2 mutations; these include Ashkenazi Jewish, Icelandic and Inuit groups, inter alia (5,17,18). Founder BRCA1/2 mutations (founders are fairly small groups of people who have been somewhat isolated over long periods of time, such that a mutation which would otherwise have been rare becomes relatively common within the population) have been identified for these groups, as well as for other European populations including, for example, Norwegians, Finns, Swedes, Dutch, Calabrians and Sardinians from Italy (19) as well as among Slavic people (20). In addition, founder BRCA1/2 mutations have been detected for several other ethnic groups whose members have immigrated to Europe. Among these groups are Pakistanis, Malaysians, Hispanics from Colombia, Japanese, Chinese and Sephardic Jews from several Arab countries (19,21). It has been suggested that testing for BRCA1/2 should be considered for much less significant family history among founder populations (13), and that population screening for BRCA mutations may be an appropriate alternative for such populations (22). On the other hand, among ethnic groups in Europe with overall low breast cancer risk, the relative percentage of aggressive cancers appearing among young patients may be very high, as is reported among North African populations living in France (23).

It is also important to take into account small family size, ‘limited family structure' (24) when assessing breast cancer risk, especially when there are few middle-aged or older female family members. Since the BRCA breast and ovarian cancer syndrome has an autosomal dominant inheritance, ~50% of the mutation carriers will be male. Especially insofar as the number of female 1st and 2nd degree relatives above age 45 is small, with a limited family structure, the likelihood of accurately predicting BRCA mutation carrier status in single cases of early-onset breast cancer may be substantially diminished (2527).

Lower breast cancer screening rates and consequent late stage diagnosis have been frequently associated with ethnic minority groups. This is particularly the case for women who are economically deprived and/or immigrants or refugees (2836). Women from ethnic minority groups who are at high breast cancer risk are thus of particular concern. A critical question is whether these women are adequately included in ongoing screening programs aimed at women with high breast cancer risk. Given Europe's enormous ethnic diversity and the influx of residents from the entire world, in addition to the marked disparities in breast cancer survival, these issues are extremely timely.

In our earlier review performed through 2008 (34), we identified breast cancer surveillance studies of high-risk women from fifteen European centers that had imaging in their protocols. Our focus therein was on the Jewish population as a high-risk group. Our conclusion at that time was that the imaging surveillance was beneficial, but that Jewish women and other ethnic minority groups at potentially high risk were unlikely to have been adequately included in these programs.

The aim of the present study is to systematically review the published literature from Europe, through the more recent period (end of 2014), on breast cancer surveillance studies that had imaging in the protocol and that targeted women at high-risk for breast cancer. Our research focus is broadened in the present study to assess the likelihood that women from diverse minority ethnic groups were adequately included in these surveillance programs. The overall purpose of this review is to identify ways of diminishing the disparities in breast cancer survival in Europe.

2. Search strategy for identifying European imaging surveillance studies targeting women at high breast cancer risk

We sought empirical studies based in Europe, which targeted women at high risk for breast cancer, and which had imaging as part of the surveillance protocol. The latter included more frequent mammography screening intervals, younger age of onset for mammography, use of magnetic resonance imaging (MRI) and/or ultrasound. Studies were excluded if only persons already diagnosed with breast cancer were examined or if imaging was only used for evaluating previously detected lesions.

We began with Ovid Medline using the search terms as key words plus the ‘explode' option. This was performed as follows: [(breast cancer) AND (high risk) AND {(ultrasound) or (mammography) or (magnetic resonance imaging)}]. Altogether, 1024 possibly eligible studies were identified. A PubMed search was then done, using the following strategy: [{(surveillance) or (early detection)} and (high risk) and (breast cancer)]. This yielded another 260 potentially eligible studies. We also searched PubMed through the strategy: [{(breast cancer)} AND (high risk) AND {(Europe) or (Scandinavia) or any of (42 European country names)}], finding another 90 potentially eligible studies. These searches were performed through December 2014. The abstracts and/or full-text studies were then reviewed. Relevant cited studies were accessed for needed background information.

Altogether we identified 27 different European study centers that fulfilled the above-described criteria. One or more studies were found that reported empirical data about these surveillance programs. There was a total of 62 such studies (3746,5067,7074,7682,8487,9193, 9596,99102,106,107,110112,120,121,123,126). In addition, information about the Study Centers (4749,68,69,75,83,8890,94,97,98, 103105,108,109,113119,122,124,125).

3. Protocol for reviewing the identified surveillance studies

For each of the 27 surveillance programs, an independent review was performed by two investigators. Basic information was summarized, including the imaging modalities used, number of cases detected and benefit of the trial. The studies were scrutinized to ascertain how participants were recruited, as well as criteria for entry into the study. Next, the studies were examined to determine whether a) there was any note of ethnic minority groups at high risk for breast cancer, and if so, b) whether these groups were taken into account in the actual risk assessment and recruitment. Each reviewer also assessed whether the studies considered: c) the possibility of limited family structure and d) family members living outside the country.

On the basis of points a) through d) together with consideration of the entry criteria and recruitment procedure, each of the 27 study centers was given an overall assessment rating concerning the likelihood of adequately including minority ethnic women at high breast cancer risk in the study catchment area.

This overall assessment was scored as follows: 3, Active surveillance with a very high participation rate of the entire at-risk minority population in the catchment area; adequate account taken of eventual limited family structure and family living outside the country. 2, Systematic efforts were made to include at-risk minority populations, but the study center unlikely to have achieved sufficiently high coverage to do so. 1, Although not taken into account for recruitment, high-risk ethnicity and/or limited family structure and/or family members living outside the country were factors considered in the study design. 0, No attention whatsoever to high-risk ethnicity nor to limited family structure nor to family members living outside the country. Recruitment procedure and entry criteria render it very unlikely that women at high breast cancer risk who are from ethnic minority groups were included in the program.

The scores were additive, such that each study was credited for all actions that could have increased the likelihood of adequately detecting and including women from minority ethnic groups at high breast cancer risk within the catchment area. Fractional scores to the 0.25 level were permitted. Insofar as the two reviewers could not arrive at consensus, a third served as arbiter. Arbitration was needed for two of the 27 study groups.

4. General description of the 27 identified European study centers

Table I summarizes the pertinent considerations about each of 27 study centers. The centers are sorted by country, and each was assigned an identification number for the purpose of our assessment.

Table I

Breast cancer surveillance studies of women at increased risk in Europe.

Table I

Breast cancer surveillance studies of women at increased risk in Europe.

[i] Coding for Overall Assessment: 3, Active surveillance with a very high participation rate of the entire at-risk minority population in the catchment area; adequate account taken of eventual limited family structure and family living outside the country. 2, Systematic efforts were made to include at-risk minority populations, but unlikely to have achieved sufficiently high coverage to do so. 1, Although not taken into account for recruitment, high risk ethnicity and/or limited family structure and/or family members living outside the country was considered in the study design. 0, No attention whatsoever to high risk ethnicity nor to limited family structure nor to family members living outside the country. Recruitment procedure and entry criteria render it very unlikely that women at high breast cancer risk who are from ethnic minority groups were included in the program. ATDH, atypical ductal hyperplasia; BC, breast cancer; CBE, clinical breast examination; CE, contrast enhanced; D, day(s); DCIS, ductal carcinoma in situ; FHx, family history; GCHBOC, German Consortium for Hereditary Breast & Ovarian Cancer; GP, general practitioner; Hx, history; LCIS, lobular in situ carcinoma; LFS, limited family structure; M, month(s); MARIBS, magnetic resonance imaging for breast cancer screening; MM, mammography; MMCI, Masaryk Memorial Cancer Institute; MRI, magnetic resonance imaging; MRISC, Multicenter Dutch MRI Screening Study; OC, ovarian cancer; PIMMS, psychological impact of mammography screening in women with family history of breast cancer; PPV, positive predictive value; RRSO, risk-reducing salpinghooophorectomy; RT, radiation therapy; SES, socioeconomic status; sig, statistically significant; STIC IRM, Magnetic Resonance Imaging Study Group France; UMC, university medical center; y, year(s).

We begin with the Netherlands where one of the largest prospective investigations was performed among 2157 women. This was the Dutch Multicenter MRI Screening Study (MRISC), denoted as Study Center #1 (3746). In the MRISC, biannual clinical breast exam (CBE), annual contrast enhanced (CE) MRI and mammography were performed in most cases. The other two Study Centers from the Netherlands (50,51) also applied CBE, CE-MRI and mammography, and in Study Center #2 (50) ultrasound was used in some cases.

Study Centers ##4-10 (5276) from the UK used various combinations and schedules of mammography, CE-MRI and ultrasound and CBE. The UK Multicentre Study (MARIBS) and the subsequent Nightingale Study (Study Center #4) (5267) followed altogether 959 women at high risk for up to 7 years with annual CE-MRI and mammography. Study Center #10 (77) from the UK examined women age 35–39 with elevated breast cancer risk who underwent surveillance via annual mammography.

From the German Study Centers (##11–13) (7885) CBE, CE-MRI, mammography and often ultrasound were also performed. The German Multicenter Study (#11) (78) and the Bonn Center (#12) (7982) followed 413 and 629 women for up to 6 and up to 10 years, respectively.

The Italian Centers (##14–16) (8695) also used CBE, CE-MRI, mammography and ultrasound in various combinations. The Italian Multicenter Study (#14) (86,87) included 501 women enrolled between 2000 and 2007 and performed 1592 screening rounds. The Modena Study (#15) (9193) included 1325 women who were followed for up to 11 years.

There were two Polish Study Centers (##17 and 18) (9699). The Center from Szczecin (#17) (9698) provided the majority of 212 women at high breast cancer risk with mammography and in a few cases with MRI, and reported 18 months of follow-up. All 379 women included in the Krakow Center (#18) (99) received MRI, after undergoing mammography and ultrasound that had shown no abnormalities.

The French Study Centers (##19–21) (100106) used combinations of MRI, mammography and ultrasound. The French Multicenter Study (STIC IRM) (100,101) included 1561 women with a few months of reported follow-up. The Vienna Study Center (#22) (107) included 327 women with up to 7 years of follow-up, using mammography, MRI and ultrasound.

The Stockholm Center (#23) (110112) reported on 160 families receiving annual mammography and CBE. The two Norwegian Multicenter Studies (##24 and 25) (120,121) followed 754 and 491 women at high breast cancer risk for 5 and 3 years, respectively. In Study Center #24 (120) CBE, mammography and in some cases ultrasound were used, and in #25 (121) mammography, MRI and in some cases ultrasound.

In the Czech (Brno) Study Center (#26) (123) MRI, mammography and ultrasound were provided to 284 women at high risk, with follow-up reported for 3 years. The Irish (Dublin) Study Center (#27) (126) reported the results of 3-year follow-up of 1145 women at medium and high breast cancer risk with the option offered of imaging surveillance using CBE and mammography.

5. Benefits of imaging surveillance for women at high breast cancer risk as assessed in the 27 study centers

In all the centers where it was applied, MRI was recommended for screening women at increased risk, since it showed the highest sensitivity and thereby provided early breast cancer detection, frequently while still carcinoma in situ. However, MRI also yielded many false positive results, often more than mammography. This low positive predictive value of MRI was of concern and other modalities (mammography and/or ultrasound) were also usually recommended. On the other hand, the Bonn Center (#12) (7982) found that MRI alone was sufficient among women with BRCA1 mutations. These authors reported that mammography did not provide additional information for early breast cancer detection in this group. Considering the heightened vulnerability to ionizing radiation among BRCA1 mutation carriers, these authors recommended that mammography be discontinued for this group. Similarly, in the Dutch Multicenter Study (#1) (3746) MRI appeared to be effective for BRCA mutation carriers and was generally more sensitive than mammography. However, it was also noted that mammography detected some early cancers missed by MRI. Overall, the use of MRI and more intensive screening starting at a younger age provided earlier detection, such that there was a clear benefit for women with increased breast cancer risk.

From the Stockholm Study Center (#23) (110112) which focused on high-risk families, the decreasing age of cancer onset with successive generations was viewed as important for choosing surveillance modalities (110,114). The investigators from the Dusseldorf Center (#13) (84,85) stated that intensified early cancer detection programs for women at risk provide a less invasive option than chemoprevention or prophylactic surgery. Notwithstanding the high frequency of surveillance, these authors found it feasible to motivate at-risk women to participate. Despite the problems surrounding false positive findings, MRI was found to be acceptable by these women (84,85). This latter conclusion was shared by authors from the Dutch Multicenter study (#1) (38).

6. Recruitment of women into the programs and considerations of ethnicity and high risk, including testing for relevant gene mutations

Most of the study participants were recruited from specialized clinics for women at high risk. It was noted that self-referral or referral from primary care physicians was possible for some of these programs. The latter include: UK Study Centers (#4 and #8) MARIBS (5267) and psychological impact of mammography screening in women with family history of breast cancer (PIMMS) (73,74), the Stockholm Study Center (#23) (110112), one of the Norwegian Multicenter Studies (#24) (120), the Dublin Study Center (#27) (126) and possibly the Czech (Brno) Study Center (#26) (123). The explicit possibility of self-referral or referral from primary care physicians might improve the coverage of the catchment area and thereby might have increased the chances of including a broader sampling of women at high breast cancer risk.

Ethnicity, including ethnic minority groups at increased breast cancer risk was mentioned in some of the studies as part of their introduction or general discussion. In a study (47) which provided relevant background for the Dutch Multicenter MRI Screening Study, MRISC (#1), a substantial percentage of women from minority ethnic backgrounds, including those with parents born elsewhere, were noted to have been referred to genetic counseling centers in the Netherlands. On the other hand, in the MRISC-B Study, requiring Dutch language proficiency (37) may have excluded a substantial percentage of ethnic minority women. Women from non-white minority ethnic backgrounds appear to have been under-represented in the UK MARIBS Study (#4) comprising only 2.3% of the sample according to the reported data (62). The statement in Brozek et al (98): ‘(The) Polish population is not ethnically mixed because of the loss of a considerable number of ethnic groups from Poland's territory' (p. 329) could be interpreted to imply that for the Polish Szczecin Study (#17) no special attention was given to minority groups that may be at high risk. In contrast, explicit appreciation of the country's ethnic diversity was indicated in a background article by the first author of the Czech Brno Study (#26) (124).

For a few centers [Szczecin #17 (96), Stockholm #23 (110) and Brno #26 (123)] relevant gene mutations were tested for some ethnic groups at high risk. It might be inferred from some studies (79,83,107) that the Bonn and Vienna Centers (##12 and 22) also tested for these gene mutations. In the Nightingale and PIMMS Studies from the UK (##4 and 8) (73,74) ande in the Dublin Study (#27) (126) high risk ethnicity (Ashkenazi Jewish) was considered as a subsidiary factor under stringent conditions, i.e. that two relatives with breast or ovarian cancer had already been identified.

7. Family history assessment, including reliance on national data registries

Several of the study centers allowed a woman to be included in their program if she had a single family member with breast cancer or ovarian cancer diagnosed at a young age. This might partially have taken limited family structure into account. However, limited family structure per se (24) was not examined in any of the studies.

Family members outside the country were not explicitly taken into account in any of the studies. Some of the Centers, for example, the German Multicenter Study (#11) (78), the Italian Modena Study (#15) (9193), the UK Study (#10) (77) of young women with increased risk and the Polish Krakow Study (#18) (99) described a very detailed procedure for taking a family history, and this may have facilitated inclusion of family who lived abroad. An adjudicating panel assessed the family history in the UK MARIBS study (#4) and it might be assumed that this would ensure completeness of the family history data. On the other hand, the adjudicating panel could have introduced greater stringency, as assessed in the sub-study by Evans et al (55). In one of the most recent studies from the MARIBS and subsequent Nightingale Studies (#4), it was explicitly recognized that there is a need for ‘systematic assessment of family history in primary care or through population-based screening [to] identify appreciable numbers of women in their forties, eligible for additional surveillance' (56) (p. 993).

The Stockholm Center (#23) (110,114) and possibly the Multicenter Norwegian Study (#24) (121,122) relied on National Data Registries for identifying high risk families. Whereas this procedure would facilitate inclusion of at-risk family members living within the country, the likelihood is greater of missing family members outside the country. Moreover, first generation immigrants were defined a priori as ‘without parents' in the Swedish database (117), rendering it even more difficult for first generation immigrant women to be included in the high risk programs.

8. Overall assessment of the likelihood of including women at high breast cancer risk and who belong to minority ethnic groups into the 27 study centers

Based on the above considerations, the overall assessment scores were low vis-à-vis the likelihood of adequately including women at high breast cancer risk, who belong to minority ethnic groups and who were residing in the study catchment area. Namely, the mean score was 0.72 [standard deviation = 0.31 (range 0.25–1.5)] from a possible range of 0–3. All but four of the study centers (UK Multicentre #4, Stockholm #23, Brno #26 and Dublin #27) had an overall assessment score <1 and, as indicated, none of the centers had a score >1.5.

9. Broader considerations for Europe based on the present analysis

The present analysis, based on a larger number of European centers and extended for several more years, confirms our previous findings (34) that for women at high risk of breast cancer, intensive screening programs, starting at a younger age and including magnetic resonance imaging were beneficial. The present review on the basis of this extended analysis also confirms our previous conclusion (34) that none of the European study centers made systematic efforts to include women from ethnic minority groups and who were at high breast cancer risk. High-risk ethnicity was not taken into account in recruitment of participants in most of the examined high-risk surveillance studies in Europe. The three exceptions (Nightingale Study #4) (57), (PIMMS, Study #8) (73,74) and (Dublin, Study #27) (126), as noted, considered high-risk ethnicity (Ashkenazi Jewish) as a subsidiary factor under stringent conditions, i.e. that two relatives with breast or ovarian cancer had already been identified. While a few of the examined study centers (96,110,123) did test for the relevant gene mutations of ethnic minority groups at high risk, none of the studies reported active outreach efforts to ensure that these women participated in their programs.

Limited family structure (24) was not adequately considered in any of the reviewed study centers. It has been suggested that the probability models of breast cancer risk need to be revised so that limited family structure is taken into sufficient account. Limited family structure becomes especially problematic when there is a single case of breast cancer in the family. It is here, most notably that these models fail to identify high risk (25). When the family risk for disease is exceedingly high, these missing family links can become critical (16). For ethnic minority groups living in Europe, who have been exposed to war during which many family members have perished, these considerations regarding limited family structure warrant particular attention. For example, cases have been reported for which limited family history due to the Holocaust rendered timely detection of high risk for breast cancer very difficult (127).

Besides the possibility of limited family history, immigrants, refugees and ethnic minority groups, in general, are often geographically dispersed. Information about cancer occurrence may, therefore, be more difficult to obtain and confirm if the medical records are outside the country. We noted this to be particularly problematic for the study centers requiring documentation of all family cases and for those relying on the National Data Registries. None of the study centers explicitly indicated that efforts had been made to ascertain whether there was cancer incidence among family members outside the country.

In the attempt to obtain accurate information about family cancer history, the cultural as well as historical context should also be considered. Grief, fear and denial can hinder reporting the entire extent of family risk (128,129). Insofar as the family has endured trauma, these considerations may become even more salient and protracted. For example, it has been noted that the offspring of Holocaust survivors (second generation) are very susceptible to psychological distress, such that when confronted with breast cancer, they react with extremely high levels of distress (130). This effect appears to be synergistic, such that women with breast cancer and whose parents were Holocaust survivors (Holocaust survivors were defined as those who had been in a concentration camp, forced labor camp or extermination camp in Europe during World War II) had much higher psychological distress than expected, based on the distress levels found for each of these factors alone (131,132). Direct exposure to the Holocaust is also associated with increased risk of breast cancer and other malignancies (133). Other traumatic situations, especially those related to war and upheavals that are still occurring in various parts of the world may well have a similar effect on persons from the affected immigrant and refugee groups (130).

In Europe, disclosure of ethnicity per se may be problematic. Subsequent to World War II, a number of European countries avoided ethnic identification of individuals. It is also plausible that individuals can be reluctant to admit that their origin is other than that of the European country in which they are currently residing. This reluctance, while fully understandable, introduces yet more complexity regarding this topic within Europe. As counter-examples, in countries such as the Canada, USA and Australia, comprised of diverse immigrant populations since their establishment, asking about ethnicity in the relevant medical setting is not only acceptable, but is considered indispensable for providing adequate clinical care. In these countries, ethnic disclosure has been essential for ensuring appropriate attention to under-represented groups for clinical trials within oncology and elsewhere in medicine (134136). Moreover, it is well-appreciated that special, often labor-intensive outreach efforts to underserved ethnic minority groups are needed, with attention to structural and attitudinal barriers to cancer screening (33,34,134,137141). With specific regard to high breast cancer risk, it has been emphasized that ‘identification of the ethnic group of families undergoing genetic counseling enables the geneticist and oncologist to make more specific choices…to simplify the clinical approach to genetic testing carried out on members of high-risk families' (p. vi93) (19).

Successful outreach to underserved ethnic minorities requires cultural competence, which includes both knowledge as well as sensitivity (33,34,142146). Culturally-tailored interventions have been very effective in increasing adherence to breast cancer screening guidelines among under-screened ethnic groups (147150). As mentioned, women with a foreign birthplace and, especially, recent immigrants appear to be vulnerable for non-attendance in these screening programs (2835). A poignant example is provided in a study (151) about Russian immigrants to Israel, whose preoccupation was with immediate survival needs, such that attitudes towards breast cancer screening were expressed as: ‘I have no time for potential troubles' (p. 153).

This statement reflects another important concern regarding imaging surveillance of women with elevated risk of breast cancer, namely, the substantial possibility of obtaining false positive results from existing screening methods, including MRI. Indeed, in a multi-center study from the USA, Canada and Argentina, among women with increased breast cancer risk and who were eligible to undergo breast MRI, just over half agreed to do so (152). Claustrophobia was the most commonly noted reason for refusal, which may be related to general anxiety about the procedure and its possible results. Concern about additional biopsies or testing was explicitly cited by many women who declined to undergo MRI. It is plausible that this high refusal rate reflects a lack of confidence in the diagnostic accuracy of MRI. Although MRI is reported to be particularly sensitive for women with high breast cancer risk (153), the large number of false positive findings may have a deleterious effect upon quality of life (154). Thus, in the French Multicenter Study #17, although women at high breast cancer risk who underwent MRI had less anxiety at baseline than women at lower risk who were not offered MRI, abnormal surveillance study results were associated with significantly increased anxiety (100). The possibilities for improving the specificity of MRI through e.g. magnetic resonance spectroscopy and diffusion-weighted imaging warrant attention in this context (155161).

10. Limitations and challenges of this review

Together with our previous study (34), these are the first reviews, to the best of our knowledge, in which the special screening needs of ethnic minority women in Europe at high risk for breast cancer have been examined. Our search strategies were carefully conceived aiming for completeness. The scoring system was heuristic, because of the uncharted nature of this area of investigation. Nevertheless, we consider this scoring system to have good face validity. For some of the centers, inference was needed since the provided information was limited about recruitment of participants. We strove to avoid subjectivity in these ratings via two or more independent assessments.

Admittedly, the formal concept of limited family structure (24) is relatively new. Therefore, it might not be reasonable to expect this consideration to be fully incorporated into the study methodology of the examined centers. Nevertheless, the importance of family truncation as well as dispersion of family members outside the host country should certainly be a routine consideration to achieve adequate risk assessment. Simply stated, a complete family history should be taken ‘without borders'.

Another limitation of the present review is that the percentage of ethnic minority women varies greatly across the various European countries, and this was not taken into account in our assessment. Different regions, even within the same country, may have very different proportions of persons who are not of the primary nationality of the country (i.e. immigrants, refugees as well as ethnic minorities having lived in the region for a long period of time). Nevertheless, the needs of such persons, whatever their prevalence in the population, still warrant attention.

A number of questions are raised by the present review. Firstly, in Europe we do not know the preferences of women with an ethnic minority background and who are at high breast cancer risk with regard to approaches to screening. Attitudes regarding disclosure of ethnic identity are also not known. Within this context, issues regarding the safety and security of disclosing one's ethnicity must be clearly addressed and guaranteed. It is known that trauma survivors and their immediate descendants can become extremely distressed when faced with breast cancer. However, it is not known how the generational experience of the severe trauma affects screening behavior among women at high breast cancer risk who are from ethnic minorities. Hence, the most effective cultural-specific strategies to enhance adherence to screening guidelines among these groups in Europe remain to be identified.

11. Suggested next steps

Population-based invitational breast cancer screening programs that already exist in many European countries would be an appropriate starting point for launching this initiative. These programs have a well-documented success in achieving high participation rates and lowering mortality from breast cancer (162167). Outreach, including the use of multi-lingual media, is increasingly appreciated as an effective strategy for enhancing participation in breast cancer screening programs among ethnic minority groups. Inclusion of trusted community leaders may be particularly helpful (150,168). This type of initiative is currently on-going, e.g. in Stockholm (169).

Several population-based invitational breast cancer screening programs operate in countries whose native populations are at increased risk of carrying deleterious breast cancer gene mutations. Analysis of cases of interval breast cancers from population-based screening programs underscores the importance of identifying women at high risk e.g. carriers of a more aggressive molecular phenotype such as BRCA1/2 mutations (170). Screening at the population level for hereditary and familial cancer syndromes has been demonstrated to be a potentially viable strategy within the European setting (171). Population-based screening programs that tailor to risk profiles also represent a promising possibility, based on a recent study from Italy (172). Especially within such settings, systematic outreach to women at high risk from various ethnic groups would certainly be feasible.

As noted, several European countries have population-based breast cancer screening programs. Unfortunately, however, even more European countries do not (35,173). We would contend that efforts could be particularly promising insofar as they were coordinated with improved and more systematic breast cancer screening programs across Europe.

12. Conclusions

Women from ethnic minority groups in Europe and who are at high breast cancer risk do not appear to have sufficiently benefitted from existing high-risk screening programs. Systematic outreach targeting these populations, in a culturally sensitive manner, is needed. These efforts are likely to be most effective on a European-wide basis. Given the ever-increasing mobility of the global working force and socio-economic migration across national borders, the question of providing adequate breast cancer risk assessment for women of different ethnic origin is becoming more and more relevant. Furthermore, these efforts are in line with the European Union Council's initiative aimed at ‘Reducing the Burden of Cancer in Europe' (174).

Acknowledgements

The present review was supported by Cancerfonden; Radiumhemmet Research Fund; the Müllerska Fund through the Royal Swedish Academy of Sciences; FoUU through Stockholm County Council and Karolinska Institutet Research Foundation to which the authors are grateful.

Abbreviations:

CBE

clinical breast examination

CE

contrast enhanced

MARIBS

magnetic resonance imaging for breast cancer screening study (UK)

MRI

magnetic resonance imaging

MRISC

multicenter MRI screening study (The Netherlands)

PIMMS

psychological impact of mammography screening in women with family history of breast cancer (UK)

STIC IRM

magnetic resonance imaging study group (France)

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APA
Belkić, K., Cohen, M., Wilczek, B., Andersson, S., Berman, A.H., Márquez, M. ... Mints, M. (2015). Imaging surveillance programs for women at high breast cancer risk in Europe: Are women from ethnic minority groups adequately included? (Review). International Journal of Oncology, 47, 817-839. https://doi.org/10.3892/ijo.2015.3063
MLA
Belkić, K., Cohen, M., Wilczek, B., Andersson, S., Berman, A. H., Márquez, M., Vukojević, V., Mints, M."Imaging surveillance programs for women at high breast cancer risk in Europe: Are women from ethnic minority groups adequately included? (Review)". International Journal of Oncology 47.3 (2015): 817-839.
Chicago
Belkić, K., Cohen, M., Wilczek, B., Andersson, S., Berman, A. H., Márquez, M., Vukojević, V., Mints, M."Imaging surveillance programs for women at high breast cancer risk in Europe: Are women from ethnic minority groups adequately included? (Review)". International Journal of Oncology 47, no. 3 (2015): 817-839. https://doi.org/10.3892/ijo.2015.3063