Imaging surveillance programs for women at high breast cancer risk in Europe: Are women from ethnic minority groups adequately included? (Review)
- Authors:
- Published online on: June 26, 2015 https://doi.org/10.3892/ijo.2015.3063
- Pages: 817-839
Abstract
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 (6–8). 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 (14–16).
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 (25–27).
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 (28–36). 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 (37–46,50–67,70–74,76–82,84–87,91–93, 95–96,99–102,106,107,110–112,120,121,123,126). In addition, information about the Study Centers (47–49,68,69,75,83,88–90,94,97,98, 103–105,108,109,113–119,122,124,125).
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.
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 (37–46). 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 (52–76) 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) (52–67) 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) (78–85) CBE, CE-MRI, mammography and often ultrasound were also performed. The German Multicenter Study (#11) (78) and the Bonn Center (#12) (79–82) followed 413 and 629 women for up to 6 and up to 10 years, respectively.
The Italian Centers (##14–16) (86–95) 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) (91–93) included 1325 women who were followed for up to 11 years.
There were two Polish Study Centers (##17 and 18) (96–99). The Center from Szczecin (#17) (96–98) 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) (100–106) 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) (110–112) 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) (79–82) 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) (37–46) 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) (110–112) 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 (52–67) and psychological impact of mammography screening in women with family history of breast cancer (PIMMS) (73,74), the Stockholm Study Center (#23) (110–112), 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) (91–93), 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 (134–136). 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 (33,34,134,137–141). 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 (33,34,142–146). Culturally-tailored interventions have been very effective in increasing adherence to breast cancer screening guidelines among under-screened ethnic groups (147–150). As mentioned, women with a foreign birthplace and, especially, recent immigrants appear to be vulnerable for non-attendance in these screening programs (28–35). 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 (155–161).
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 (162–167). 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) |
References
|
Parkin DM, Bray F, Ferlay J and Pisani P: Global cancer statistics, 2002. CA Cancer J Clin. 55:74–108. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Perry N, Broeders M, de Wolf C, Törnberg S, Holland R and von Karsa L: European guidelines for quality assurance in breast cancer screening and diagnosis Fourth edition - summary document. Ann Oncol. 19:614–622. 2008. View Article : Google Scholar | |
|
Sant M, Allemani C, Capocaccia R, Hakulinen T, Aareleid T, Coebergh JW, Coleman MP, Grosclaude P, Martinez C, Bell J, et al; EUROCARE Working Group. Stage at diagnosis is a key explanation of differences in breast cancer survival across Europe. Int J Cancer. 106:416–422. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Armstrong K, Moye E, Williams S, Berlin JA and Reynolds EE: Screening mammography in women 40 to 49 years of age: A systematic review for the American College of Physicians. Ann Intern Med. 146:516–526. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Saslow D, Boetes C, Burke W, Harms S, Leach MO, Lehman CD, Morris E, Pisano E, Schnall M, Sener S, et al; American Cancer Society Breast Cancer Advisory Group. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 57:75–89. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sabatino SA, Burns RB, Davis RB, Phillips RS, Chen YH and McCarthy EP: Breast carcinoma screening and risk perception among women at increased risk for breast carcinoma: Results from a national survey. Cancer. 100:2338–2346. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Evans JP, Skrzynia C, Susswein L and Harlan M: Genetics and the young woman with breast cancer. Breast Dis. 23:17–29. 2006.PubMed/NCBI | |
|
Klauber-DeMore N: Tumor biology of breast cancer in young women. Breast Dis. 23:9–15. 2006.PubMed/NCBI | |
|
Kurian AW, Hartman AR, Mills MA, Ford JM, Daniel BL and Plevritis SK: Opinions of women with high inherited breast cancer risk about prophylactic mastectomy: An initial evaluation from a screening trial including magnetic resonance imaging and ductal lavage. Health Expect. 8:221–233. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Clements A, Henderson BJ, Tyndel S, Evans G, Brain K, Austoker J and Watson E; PIMMS Study Management Group. Diagnosed with breast cancer while on a family history screening programme: An exploratory qualitative study. Eur J Cancer Care (Engl). 17:245–252. 2008. View Article : Google Scholar | |
|
Bermejo-Pérez MJ, Márquez-Calderón S and Llanos-Méndez A: Cancer surveillance based on imaging techniques in carriers of BRCA1/2 gene mutations: A systematic review. Br J Radiol. 81:172–179. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Willey SC and Cocilovo C: Screening and follow-up of the patient at high risk for breast cancer. Obstet Gynecol. 110:1404–1416. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Armstrong AC and Evans GD: Management of women at high risk of breast cancer. BMJ. 348:g27562014. View Article : Google Scholar : PubMed/NCBI | |
|
Anderson E, Berg J, Black R, Bradshaw N, Campbell J, Cetnarskyj R, Drummond S, Davidson R, Dunlop J, Fordyce A, et al: Predicting breast cancer risk: Implications of a ‘weak' family history. Fam Cancer. 7:361–366. 2008. View Article : Google Scholar | |
|
Eerola H, Blomqvist C, Pukkala E, Pyrhönen S and Nevanlinna H: Familial breast cancer in southern Finland: How prevalent are breast cancer families and can we trust the family history reported by patients? Eur J Cancer. 36:1143–1148. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Møller P, Hagen AI, Apold J, Maehle L, Clark N, Fiane B, Løvslett K, Hovig E and Vabø A: Genetic epidemiology of BRCA mutations - family history detects less than 50% of the mutation carriers. Eur J Cancer. 43:1713–1717. 2007. View Article : Google Scholar | |
|
Fackenthal JD and Olopade OI: Breast cancer risk associated with BRCA1 and BRCA2 in diverse populations. Nat Rev Cancer. 7:937–948. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Harboe TL, Eiberg H, Kern P, Ejlertsen B, Nedergaard L, Timmermans-Wielenga V, Nielsen IM and Bisgaard ML: A high frequent BRCA1 founder mutation identified in the Greenlandic population. Fam Cancer. 8:413–419. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ferla R, Calò V, Cascio S, Rinaldi G, Badalamenti G, Carreca I, Surmacz E, Colucci G, Bazan V and Russo A: Founder mutations in BRCA1 and BRCA2 genes. Ann Oncol. 18(Suppl 6): vi93–vi98. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Iyevleva AG, Suspitsin EN, Kroeze K, Gorodnova TV, Sokolenko AP, Buslov KG, Voskresenskiy DA, Togo AV, Kovalenko SP, Stoep N, et al: Non-founder BRCA1 mutations in Russian breast cancer patients. Cancer Lett. 298:258–263. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Sagi M, Eilat A, Ben Avi L, Goldberg Y, Bercovich D, Hamburger T, Peretz T and Lerer I: Two BRCA1/2 founder mutations in Jews of Sephardic origin. Fam Cancer. 10:59–63. 2011. View Article : Google Scholar | |
|
Manchanda R, Legood R, Burnell M, McGuire A, Raikou M, Loggenberg K, Wardle J, Sanderson S, Gessler S, Side L, et al: Cost-effectiveness of population screening for BRCA mutations in Ashkenazi jewish women compared with family history-based testing. J Natl Cancer Inst. 107:3802015. View Article : Google Scholar | |
|
Corbex M, Bouzbid S and Boffetta P: Features of breast cancer in developing countries, examples from North-Africa. Eur J Cancer. 50:1808–1818. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Weitzel JN, Lagos VI, Cullinane CA, Gambol PJ, Culver JO, Blazer KR, Palomares MR, Lowstuter KJ and MacDonald DJ: Limited family structure and BRCA gene mutation status in single cases of breast cancer. JAMA. 297:2587–2595. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Leu M, Czene K and Reilly M: The impact of truncation and missing family links in population-based registers on familial risk estimates. Am J Epidemiol. 166:1461–1467. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Leu M, Czene K and Reilly M: Bias correction of estimates of familial risk from population-based cohort studies. Int J Epidemiol. 39:80–88. 2010. View Article : Google Scholar | |
|
Weitzel JN: Limited Family structure and breast cancer risk. JAMA. 298:Letter. 2007, http://dx.doi.org/10.1001/jama.298.17.2007-b. View Article : Google Scholar | |
|
Cohen M and Azaiza F: Early breast cancer detection practices, health beliefs, and cancer worries in Jewish and Arab women. Prev Med. 41:852–858. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Goel MS, Wee CC, McCarthy EP, Davis RB, Ngo-Metzger Q and Phillips RS: Racial and ethnic disparities in cancer screening: The importance of foreign birth as a barrier to care. J Gen Intern Med. 18:1028–1035. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Li CI, Malone KE and Daling JR: Differences in breast cancer stage, treatment, and survival by race and ethnicity. Arch Intern Med. 163:49–56. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Lagerlund M, Maxwell AE, Bastani R, Thurfjell E, Ekbom A and Lambe M: Sociodemographic predictors of non-attendance at invitational mammography screening - a population-based register study (Sweden). Cancer Causes Control. 13:73–82. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Sassi F, Luft HS and Guadagnoli E: Reducing racial/ethnic disparities in female breast cancer: Screening rates and stage at diagnosis. Am J Public Health. 96:2165–2172. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Terán L, Baezconde-Garbanati L, Márquez M, Castellanos E and Belkić K: On-time mammography screening with a focus on Latinas with low income: A proposed cultural model. Anticancer Res. 27(6C): 4325–4338. 2007. | |
|
Belkić K, Cohen M, Márquez M, Mints M, Wilczek B, Berman AH, Castellanos E and Castellanos M: Screening of high-risk groups for breast and ovarian cancer in Europe: A focus on the Jewish population. Oncol Rev. 4:233–267. 2010. View Article : Google Scholar | |
|
Sándor J, Havasi V, Kiss I, Szücs M, Brázay L, Sebestyén A and Ember I: Small area inequalities in breast cancer mortality and screening. Magy Onkol. 46:139–145. 2002.(In Hungarian). | |
|
Copson E, Maishman T, Gerty S, Eccles B, Stanton L, Cutress RI, Altman DG, Durcan L, Simmonds P, Jones L, et al; POSH study steering group. Ethnicity and outcome of young breast cancer patients in the United Kingdom: The POSH study. Br J Cancer. 110:230–241. 2014. View Article : Google Scholar : | |
|
den Heijer M, Seynaeve C, Vanheusden K, Timman R, Duivenvoorden HJ, Tilanus-Linthorst M, Menke-Pluijmers MB and Tibben A: Long-term psychological distress in women at risk for hereditary breast cancer adhering to regular surveillance: A risk profile. Psychooncology. 22:598–604. 2013. View Article : Google Scholar | |
|
Essink-Bot ML, Rijnsburger AJ, van Dooren S, de Koning HJ and Seynaeve C: Women's acceptance of MRI in breast cancer surveillance because of a familial or genetic predisposition. Breast. 15:673–676. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Kriege M, Brekelmans CT, Boetes C, Rutgers EJ, Oosterwijk JC, Tollenaar RA, Manoliu RA, Holland R, de Koning HJ and Klijn JG: MRI screening for breast cancer in women with familial or genetic predisposition: Design of the Dutch National Study (MRISC). Fam Cancer. 1:163–168. 2001. View Article : Google Scholar | |
|
Kriege M, Brekelmans CTM, Boetes C, Besnard PE, Zonderland HM, Obdeijn IM, Manoliu RA, Kok T, Peterse H, Tilanus-Linthorst MM, et al; Magnetic Resonance Imaging Screening Study Group. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. N Engl J Med. 351:427–437. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Kriege M, Brekelmans CT, Boetes C, Muller SH, Zonderland HM, Obdeijn IM, Manoliu RA, Kok T, Rutgers EJ, de Koning HJ, et al; Dutch MRI Screening (MRISC) Study Group. Differences between first and subsequent rounds of the MRISC breast cancer screening program for women with a familial or genetic predisposition. Cancer. 106:2318–2326. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Kriege M, Brekelmans CT, Peterse H, Obdeijn IM, Boetes C, Zonderland HM, Muller SH, Kok T, Manoliu RA, Besnard AP, et al: Tumor characteristics and detection method in the MRISC screening program for the early detection of hereditary breast cancer. Breast Cancer Res Treat. 102:357–363. 2007. View Article : Google Scholar | |
|
Obdeijn IM, Loo CE, Rijnsburger AJ, Wasser MN, Bergers E, Kok T, Klijn JG and Boetes C: Assessment of false-negative cases of breast MR imaging in women with a familial or genetic predisposition. Breast Cancer Res Treat. 119:399–407. 2010. View Article : Google Scholar | |
|
Pieterse K, van Dooren S, Seynaeve C, Bartels CC, Rijnsburger AJ, de Koning HJ, Klijn JG, van Elderen T, Tibben A and Duivenvoorden HJ: Passive coping and psychological distress in women adhering to regular breast cancer surveillance. Psychooncology. 16:851–858. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Rijnsburger AJ, Obdeijn I-M, Kaas R, Tilanus-Linthorst MMA, Boetes C, Loo CE, Wasser MN, Bergers E, Kok T, Muller SH, et al: BRCA1-associated breast cancers present differently from BRCA2-associated and familial cases: Long-term follow-up of the Dutch MRISC Screening Study. J Clin Oncol. 28:5265–5273. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Tilanus-Linthorst MM, Kriege M, Boetes C, Hop WC, Obdeijn IM, Oosterwijk JC, Peterse HL, Zonderland HM, Meijer S, Eggermont AM, et al: Hereditary breast cancer growth rates and its impact on screening policy. Eur J Cancer. 41:1610–1617. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Albada A, Werrett J, Van Dulmen S, Bensing JM, Chapman C, Ausems MG and Metcalfe A: Breast cancer genetic counselling referrals: How comparable are the findings between the UK and the Netherlands? J Community Genet. 2:233–247. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Boetes C: Update on screening breast MRI in high-risk women. Obstet Gynecol Clin North Am. 38:149–158. viii–ix. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Lammens CR, Bleiker EM, Aaronson NK, Wagner A, Sijmons RH, Ausems MG, Vriends AH, Ruijs MW, van Os TA, Spruijt L, et al: Regular surveillance for Li-Fraumeni Syndrome: Advice, adherence and perceived benefits. Fam Cancer. 9:647–654. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Fakkert IE, Jansen L, Meijer K, Kok T, Oosterwijk JC, Mourits MJ and de Bock GH: Breast cancer screening in BRCA1 and BRCA2 mutation carriers after risk reducing salpingo-oophorectomy. Breast Cancer Res Treat. 129:157–164. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Tilanus-Linthorst MM, Obdeijn IM, Bartels KC, de Koning HJ and Oudkerk M: First experiences in screening women at high risk for breast cancer with MR imaging. Breast Cancer Res Treat. 63:53–60. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Brown J, Coulthard A, Dixon AK, Dixon JM, Easton DF, Eeles RA, Evans DG, Gilbert FG, Hayes C, Jenkins JP, et al; UK MRI Breast Screening Study Advisory Group. Protocol for a national multi-centre study of magnetic resonance imaging screening in women at genetic risk of breast cancer. Breast. 9:78–82. 2000. View Article : Google Scholar | |
|
Brown J, Coulthard A, Dixon AK, Dixon JM, Easton DF, Eeles RA, Evans DG, Gilbert FG, Hayes C, Jenkins JP, et al; UK MRI Breast Screening Study Advisory Group. Rationale for a national multi-centre study of magnetic resonance imaging screening in women at genetic risk of breast cancer. Breast. 9:72–77. 2000. View Article : Google Scholar | |
|
Brown J, Buckley D, Coulthard A, Dixon AK, Dixon JM, Easton DF, Eeles RA, Evans DG, Gilbert FG, Graves M, et al; UK MRI Breast Screening Study Advisory Group. Magnetic resonance imaging screening in women at genetic risk of breast cancer: Imaging and analysis protocol for the UK multicentre study. Magn Reson Imaging. 18:765–776. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Evans DG, Lennard F, Pointon LJ, Ramus SJ, Gayther SA, Sodha N, Kwan-Lim GE, Leach MO, Warren R, Thompson D, et al; UK Study of MRI Screening for Breast Cancer in Women at High Risk (MARIBS). Eligibility for magnetic resonance imaging screening in the United Kingdom: Effect of strict selection criteria and anonymous DNA testing on breast cancer incidence in the MARIBS Study. Cancer Epidemiol Biomarkers Prev. 18:2123–2131. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Evans DG, Brentnall AR, Harvie M, Dawe S, Sergeant JC, Stavrinos P, Astley S, Wilson M, Ainsworth J, Cuzick J, et al: Breast cancer risk in young women in the national breast screening programme: Implications for applying NICE guidelines for additional screening and chemoprevention. Cancer Prev Res (Phila). 7:993–1001. 2014. View Article : Google Scholar | |
|
Evans DG, Kesavan N, Lim Y, Gadde S, Hurley E, Massat NJ, Maxwell AJ, Ingham S, Eeles R, Leach MO, et al; MARIBS Group. MRI breast screening in high-risk women: Cancer detection and survival analysis. Breast Cancer Res Treat. 145:663–672. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Gilbert FJ, Warren RM, Kwan-Lim G, Thompson DJ, Eeles RA, Evans DG and Leach MO; United Kingdom Magnetic Resonance Imaging in Breast Screening (MARIBS) Study Group. Cancers in BRCA1 and BRCA2 carriers and in women at high risk for breast cancer: MR imaging and mammographic features. Radiology. 252:358–368. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Griebsch I, Brown J, Boggis C, Dixon A, Dixon M, Easton D, Eeles R, Evans DG, Gilbert FJ, Hawnaur J, et al; UK Magnetic Resonance Imaging in Breast Screening (MARIBS) Study Group. Cost-effectiveness of screening with contrast enhanced magnetic resonance imaging vs X-ray mammography of women at a high familial risk of breast cancer. Br J Cancer. 95:801–810. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Gui GP, Hogben RK, Walsh G, A'Hern R and Eeles R: The incidence of breast cancer from screening women according to predicted family history risk: Does annual clinical examination add to mammography? Eur J Cancer. 37:1668–1673. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Gui GP, Kadayaprath G, Darhouse N, Self J, Ward A, A'Hern R and Eeles R: Clinical outcome and service implications of screening women at increased breast cancer risk from a family history. Eur J Surg Oncol. 32:719–724. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Hutton J, Walker LG, Gilbert FJ, Evans DG, Eeles R, Kwan-Lim GE, Thompson D, Pointon LJ, Sharp DM and Leach MO; UK Study Group for MRI Screening in Women at High Risk Study. Psychological impact and acceptability of magnetic resonance imaging and X-ray mammography: The MARIBS Study. Br J Cancer. 104:578–586. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Leach MO, Eeles RA, Turnbull LW, Dixon AK, Brown J, Hoff RJ, Coulthard A, Dixon JM, Easton DF, Evans DG, et al; Magnetic Resonance Imaging as a Method of Screening for Breast Cancer Advisory Group. The UK national study of magnetic resonance imaging as a method of screening for breast cancer (MARIBS). J Exp Clin Cancer Res. 21(Suppl 3): 107–114. 2002. | |
|
Leach MO, Boggis CR, Dixon AK, Easton DF, Eeles RA, Evans DG, Gilbert FJ, Griebsch I, Hoff RJ, Kessar P, et al; MARIBS study group. Screening with magnetic resonance imaging and mammography of a UK population at high familial risk of breast cancer: A prospective multicentre cohort study (MARIBS). Lancet. 365:1769–1778. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Thompson DJ, Leach MO, Kwan-Lim G, Gayther SA, Ramus SJ, Warsi I, Lennard F, Khazen M, Bryant E, Reed S, et al; UK study of MRI screening for breast cancer in women at high risk (MARIBS). Assessing the usefulness of a novel MRI-based breast density estimation algorithm in a cohort of women at high genetic risk of breast cancer: The UK MARIBS study. Breast Cancer Res. 11:R802009. View Article : Google Scholar : PubMed/NCBI | |
|
Tilanus-Linthorst MM, Obdeijn IM and Bartels KC: MARIBS study. Lancet. 366:291–292. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Warren RM, Thompson D, Pointon LJ, Hoff R, Gilbert FJ, Padhani AR, Easton DF, Lakhani SR and Leach MO; Collaborators in the United Kingdom Medical Research Council Magnetic Resonance Imaging in Breast Screening (MARIBS) Study. Evaluation of a prospective scoring system designed for a multicenter breast MR imaging screening study. Radiology. 239:677–685. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Gilbert FJ: Breast cancer screening in high risk women. Cancer Imaging. 8(Spec No A): S6–S9. 2008.http://dx.doi.org/10.1102/1470-7330.2008.9002. View Article : Google Scholar : PubMed/NCBI | |
|
Leach MO: Breast cancer screening in women at high risk using MRI. NMR Biomed. 22:17–27. 2009. View Article : Google Scholar | |
|
Murday V, Pears R, Ball J, Eeles R and Hodgson S: An audit of screening for familial breast cancer before 50 years in the South Thames Region - have we got it right? Fam Cancer. 3:29–34. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Kollias J, Sibbering DM, Blamey RW, Holland PA, Obuszko Z, Wilson AR, Evans AJ, Ellis IO and Elston CW: Screening women aged less than 50 years with a family history of breast cancer. Eur J Cancer. 34:878–883. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Reis MM, Tavakoli M, Dewar J, Goudie D, Cook A, McLeish L, Young D, Kenyon J and Steel M: Evaluation of a surveillance programme for women with a family history of breast cancer. J Med Genet. 46:319–323. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Brain K, Henderson BJ, Tyndel S, Bankhead C, Watson E, Clements A and Austoker J; PIMMS Study Management Group. Predictors of breast cancer-related distress following mammography screening in younger women on a family history breast screening programme. Psychooncology. 17:1180–1188. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Tyndel S, Clements A, Bankhead C, Henderson BJ, Brain K, Watson E and Austoker J; PIMMS Study Management Group. Mammographic screening for young women with a family history of breast cancer: Knowledge and views of those at risk. Br J Cancer. 99:1007–1012. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Evans DG, Harvie M, Bundred N and Howell A: Uptake of breast cancer prevention and screening trials. J Med Genet. 47:853–855. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Howell SJ, Searle C, Goode V, Gardener T, Linton K, Cowan RA, Harris MA, Hopwood P, Swindell R, Norman A, et al: The UK national breast cancer screening programme for survivors of Hodgkin lymphoma detects breast cancer at an early stage. Br J Cancer. 101:582–588. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Evans DG, Thomas S, Caunt J, Roberts L, Howell A, Wilson M, Fox R, Sibbering DM, Moss S, Wallis MG, et al; FH02 study group. Mammographic surveillance in women aged 35–39 at enhanced familial risk of breast cancer (FH02). Fam Cancer. 13:13–21. 2014. View Article : Google Scholar | |
|
Schmutzler RK, Rhiem K, Breuer P, Wardelmann E, Lehnert M, Coburger S and Wappenschmidt B: Outcome of a structured surveillance programme in women with a familial predisposition for breast cancer. Eur J Cancer Prev. 15:483–489. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Kuhl CK: High-risk screening: Multi-modality surveillance of women at high risk for breast cancer (proven or suspected carriers of a breast cancer susceptibility gene). J Exp Clin Cancer Res. 21(Suppl 3): 103–106. 2002. | |
|
Kuhl CK, Schrading S, Leutner CC, Morakkabati-Spitz N, Wardelmann E, Fimmers R, Kuhn W and Schild HH: Mammography, breast ultrasound, and magnetic resonance imaging for surveillance of women at high familial risk for breast cancer. J Clin Oncol. 23:8469–8476. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Kuhl CK, Kuhn W and Schild H: Management of women at high risk for breast cancer: New imaging beyond mammography. Breast. 14:480–486. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Schrading S and Kuhl CK: Mammographic, US, and MR imaging phenotypes of familial breast cancer. Radiology. 246:58–70. 2008. View Article : Google Scholar | |
|
Meindl A; German Consortium for Hereditary Breast and Ovarian Cancer. Comprehensive analysis of 989 patients with breast or ovarian cancer provides BRCA1 and BRCA2 mutation profiles and frequencies for the German population. Int J Cancer. 97:472–480. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Lux MP, Ackermann S, Nestle-Krämling C, Goecke TO, Niederacher D, Bodden-Heidrich R, Bender HG, Beckmann MW and Fasching PA: Use of intensified early cancer detection in high-risk patients with familial breast and ovarian cancer. Eur J Cancer Prev. 14:399–411. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Lux MP, Ackermann S, Bani MR, Nestle-Krämling C, Goecke TO, Niederacher D, Bodden-Heidrich R, Bender HG, Beckmann MW and Fasching PA: Age of uptake of early cancer detection facilities by low-risk and high-risk patients with familial breast and ovarian cancer. Eur J Cancer Prev. 14:503–511. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Sardanelli F, Podo F, D'Agnolo G, Verdecchia A, Santaquilani M, Musumeci R, Trecate G, Manoukian S, Morassut S, de Giacomi C, et al; High Breast Cancer Risk Italian Trial. Multicenter comparative multimodality surveillance of women at genetic-familial high risk for breast cancer (HIBCRIT study): Interim results. Radiology. 242:698–715. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sardanelli F, Podo F, Santoro F, Manoukian S, Bergonzi S, Trecate G, Vergnaghi D, Federico M, Cortesi L, Corcione S, et al; High Breast Cancer Risk Italian 1 (HIBCRIT-1) Study. Multicenter surveillance of women at high genetic breast cancer risk using mammography, ultrasonography, and contrast-enhanced magnetic resonance imaging (the high breast cancer risk Italian 1 study): Final results. Invest Radiol. 46:94–105. 2011. View Article : Google Scholar | |
|
Sardanelli F, Giuseppetti GM, Canavese G, Cataliotti L, Corcione S, Cossu E, Federico M, Marotti L, Martincich L, Panizza P, et al: Indications for breast magnetic resonance imaging. Consensus document ‘Attualità in senologia', Florence 2007. Radiol Med (Torino). 113:1085–1095. 2008. View Article : Google Scholar | |
|
Manfrin E, Mariotto R, Remo A, Reghellin D, Falsirollo F, Dalfior D, Bricolo P, Piazzola E and Bonetti F: Benign breast lesions at risk of developing cancer--a challenging problem in breast cancer screening programs: Five years' experience of the Breast Cancer Screening Program in Verona (1999–2004). Cancer. 115:499–507. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Santoro F, Podo F and Sardanelli F: MRI screening of women with hereditary predisposition to breast cancer: Diagnostic performance and survival analysis. Breast Cancer Res Treat. 147:685–687. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cortesi L, Turchetti D, Marchi I, Fracca A, Canossi B, Rachele B, Silvia R, Rita PA, Pietro T and Massimo F: Breast cancer screening in women at increased risk according to different family histories: An update of the Modena Study Group experience. BMC Cancer. 6:2102006. View Article : Google Scholar : PubMed/NCBI | |
|
Cortesi L, Pecchi A, De Matteis E, Filieri E, Battista R, Canossi B, Torricelli P and Federico M: MRI in high risk women: Benefits and problems. Eur J Radiol. 81(Suppl 1): S19–S20. 2012. View Article : Google Scholar | |
|
Federico M, Maiorana A, Mangone L, Turchetti D, Canossi B, Cortesi L, Romagnoli R and Silingardi V: Identification of families with hereditary breast and ovarian cancer for clinical and mammographic surveillance: The Modena Study Group proposal. Breast Cancer Res Treat. 55:213–221. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Cortesi L, Masini C, Cirilli C, Medici V, Marchi I, Cavazzini G, Pasini G, Turchetti D and Federico M: Favourable ten-year overall survival in a Caucasian population with high probability of hereditary breast cancer. BMC Cancer. 10:902010. View Article : Google Scholar : PubMed/NCBI | |
|
Trecate G, Vergnaghi D, Manoukian S, Bergonzi S, Scaperrotta G, Marchesini M, Ferranti C, Peissel B, Spatti G, Bohm S, et al: MRI in the early detection of breast cancer in women with high genetic risk. Tumori. 92:517–523. 2006. | |
|
Gronwald J, Byrski T, Huzarski T, Cybulski C, Stawicka M, Szwiec M, Debniak T, Tulman A, Sun P, Oszurek O, et al: A survey of preventive measures among BRCA1 mutation carriers from Poland. Clin Genet. 71:153–157. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Górski B, Jakubowska A, Huzarski T, Byrski T, Gronwald J, Grzybowska E, Mackiewicz A, Stawicka M, Bebenek M, Sorokin D, et al: A high proportion of founder BRCA1 mutations in Polish breast cancer families. Int J Cancer. 110:683–686. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Brozek I, Cybulska C, Ratajska M, Piatkowska M, Kluska A, Balabas A, Dabrowska M, Nowakowska D, Niwinska A, Pamula-Pilat J, et al: Prevalence of the most frequent BRCA1 mutations in Polish population. J Appl Genet. 52:325–330. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Popiela TJ, Kibil W, Herman-Sucharska I and Urbanik A: The use of magnetic resonance mammography in women at increased risk for developing breast cancer. Wideochir Inne Tech Malo Inwazyjne. 8:55–62. 2013.PubMed/NCBI | |
|
Brédart A, Kop JL, Fall M, Pelissier S, Simondi C, Dolbeault S, Livartowski A and Tardivon A; Magnetic Resonance Imaging study group (STIC IRM 2005). Anxiety and specific distress in women at intermediate and high risk of breast cancer before and after surveillance by magnetic resonance imaging and mammography versus standard mammography. Psychooncology. 21:1185–1194. 2012. View Article : Google Scholar | |
|
Brédart A, Kop JL, Fall M, Pelissier S, Simondi C, Dolbeault S, Livartowski A and Tardivon A; Magnetic Resonance Imaging study group (STIC IRM 2005). Perception of care and experience of examination in women at risk of breast cancer undergoing intensive surveillance by standard imaging with or without MRI. Patient Educ Couns. 86:405–413. 2012. View Article : Google Scholar | |
|
Daguet E, Malhaire C, Hardit C, Athanasiou A, El Khoury C, Thibault F, Ollivier L and Tardivon A; Groupe Femmes à Risque de l'Institut Curie. MR breast screening in patients with genetic mutation. J Radiol. 89:783–790. 2008.(In French). View Article : Google Scholar : PubMed/NCBI | |
|
Dorval M, Noguès C, Berthet P, Chiquette J, Gauthier-Villars M, Lasset C, Picard C, Plante M, Simard J and Julian-Reynier C; INHERIT BRCAs; GENEPSO Cohort. Breast and ovarian cancer screening of non-carriers from BRCA1/2 mutation-positive families: 2-year follow-up of cohorts from France and Quebec. Eur J Hum Genet. 19:494–499. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Eisinger F, Bressac B, Castaigne D, Cottu PH, Lansac J, Lefranc JP, Lesur A, Noguès C, Pierret J, Puy-Pernias S, et al: Identification and management of hereditary predisposition to cancer of the breast and the ovary (update 2004). Bull Cancer. 91:219–237. 2004.(In French). PubMed/NCBI | |
|
Eisinger F: Breast cancer screening for women with a strong familial risk. Bull Cancer. 92:874–884. 2005.(In French). PubMed/NCBI | |
|
Lapierre-Combes M, Rousset J, Combes E, Chinelatto S, Dupré PF and André V: Retrospective study conducted in northern Finistère about the role of breast MRI in normal breast screening, experience in 51 patients. Gynecol Obstet Fertil. 37:401–409. 2009.(In French). View Article : Google Scholar : PubMed/NCBI | |
|
Riedl CC, Ponhold L, Flöry D, Weber M, Kroiss R, Wagner T, Fuchsjäger M and Helbich TH: Magnetic resonance imaging of the breast improves detection of invasive cancer, preinvasive cancer, and premalignant lesions during surveillance of women at high risk for breast cancer. Clin Cancer Res. 13:6144–6152. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kroiss R, Winkler V, Bikas D, Fleischmann E, Mainau C, Frommlet F, Muhr D, Fuerhauser C, Tea M, Bittner B, et al; Austrian Hereditary Breast and Ovarian Cancer Group. Younger birth cohort correlates with higher breast and ovarian cancer risk in European BRCA1 mutation carriers. Hum Mutat. 26:583–589. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Kroiss R, Winkler V, Kalteis K, Bikas D, Rudas M, Tea M, Fuerhauser C, Muhr D, Cerny H, Glueck S, et al; Austrian Hereditary Breast and Ovarian Cancer Group. Prevalence of pre-malignant and malignant lesions in prophylactic mastectomy specimens of BRCA1 mutation carriers: Comparison with a control group. J Cancer Res Clin Oncol. 134:1113–1121. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Arver B, Borg A and Lindblom A: First BRCA1 and BRCA2 gene testing implemented in the health care system of Stockholm. Genet Test. 5:1–8. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Arver B, Haegermark A, Platten U, Lindblom A and Brandberg Y: Evaluation of psychosocial effects of pre-symptomatic testing for breast/ovarian and colon cancer pre-disposing genes: A 12-month follow-up. Fam Cancer. 3:109–116. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Zelada-Hedman M, Wasteson Arver B, Claro A, Chen J, Werelius B, Kok H, Sandelin K, Håkansson S, Andersen TI, Borg A, et al: A screening for BRCA1 mutations in breast and breast-ovarian cancer families from the Stockholm region. Cancer Res. 57:2474–2477. 1997.PubMed/NCBI | |
|
Arver B, Isaksson K, Atterhem H, Baan A, Bergkvist L, Brandberg Y, Ehrencrona H, Emanuelsson M, Hellborg H, Henriksson K, et al: Bilateral prophylactic mastectomy in Swedish women at high risk of breast cancer: A national survey. Ann Surg. 253:1147–1154. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Brandt A, Lorenzo Bermejo J, Sundquist J and Hemminki K: Breast cancer risk in women who fulfill high-risk criteria: At what age should surveillance start? Breast Cancer Res Treat. 121:133–141. 2010. View Article : Google Scholar | |
|
Czene K, Reilly M, Hall P and Hartman M: A constant risk for familial breast cancer? A population-based family study. Breast Cancer Res. 11:R302009. View Article : Google Scholar : PubMed/NCBI | |
|
Hemminki K, Ji J and Försti A: Risks for familial and contralateral breast cancer interact multiplicatively and cause a high risk. Cancer Res. 67:868–870. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Hemminki K, Mousavi SM, Sundquist J and Brandt A: Does the breast cancer age at diagnosis differ by ethnicity? A study on immigrants to Sweden. Oncologist. 16:146–154. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Margolin S, Werelius B, Fornander T and Lindblom A: BRCA1 mutations in a population-based study of breast cancer in Stockholm county. Genet Test. 8:127–132. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Von Wachenfeldt A, Brandberg Y, Johansson H and Fornander T: Socioeconomic status and quality of life of women with family history of breast cancer attending an oncogenetic counseling clinic: A comparison with general population. Acta Oncol. 48:86–92. 2009. View Article : Google Scholar | |
|
Dørum A, Heimdal K, Løvslett K, Kristensen G, Hansen LJ, Sandvei R, Schiefloe A, Hagen B, Himmelmann A, Jerve F, et al: Prospectively detected cancer in familial breast/ovarian cancer screening. Acta Obstet Gynecol Scand. 78:906–911. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Hagen AI, Kvistad KA, Maehle L, Holmen MM, Aase H, Styr B, Vabø A, Apold J, Skaane P and Møller P: Sensitivity of MRI versus conventional screening in the diagnosis of BRCA-associated breast cancer in a national prospective series. Breast. 16:367–374. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Albrektsen G, Heuch I and Thoresen SØ: Histological type and grade of breast cancer tumors by parity, age at birth, and time since birth: A register-based study in Norway. BMC Cancer. 10:2262010. View Article : Google Scholar : PubMed/NCBI | |
|
Foretova L, Petrakova K, Palacova M, Kalabova R, Svoboda M, Navratilova M, Schneiderova M, Bolcak K, Krejci E, Drazan L, et al: Genetic testing and prevention of hereditary cancer at the MMCI--over 10 years of experience. Klin Onkol. 23:388–400. 2010. | |
|
Foretova L, Machackova E, Navratilova M, Pavlu H, Hruba M, Lukesova M and Valik D: BRCA1 and BRCA2 mutations in women with familial or early-onset breast/ovarian cancer in the Czech Republic. Hum Mutat. 23:397–398. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Mateju M, Stribrna J, Zikan M, Kleibl Z, Janatova M, Kormunda S, Novotny J, Soucek P, Petruzelka L and Pohlreich P: Population-based study of BRCA1/2 mutations: Family history based criteria identify minority of mutation carriers. Neoplasma. 57:280–285. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Mulsow J, Lee J, Dempsey C, Rothwell J and Geraghty JG: Establishing a family risk assessment clinic for breast cancer. Breast J. 15(Suppl 1): S33–S38. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Brandt RT and Lynch HT: BRCA1 and BRCA2: To test or not to test. Breast Cancer Res Treat. 67:187–188. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Surbone A: Ethical implications of genetic testing for breast cancer susceptibility. Crit Rev Oncol Hematol. 40:149–157. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Márquez M, Belkić K, Nilsson S and Holmberg AR: Genetic testing in patients with hereditary cancer risk: Social, ethical and legal considerations. Instit Investig Jurid. 383:295–340. 2007. | |
|
Baider L, Peretz T, Hadani PE, Perry S, Avramov R and De-Nour AK: Transmission of response to trauma? Second-generation Holocaust survivors' reaction to cancer. Am J Psychiatry. 157:904–910. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Baider L, Goldzweig G, Ever-Hadani P and Peretz T: Psychological distress and coping in breast cancer patients and healthy women whose parents survived the Holocaust. Psychooncology. 15:635–646. 2006. View Article : Google Scholar | |
|
Baider L, Goldzweig G, Ever-Hadani P and Peretz T: Breast cancer and psychological distress: Mothers' and daughters' traumatic experiences. Support Care Cancer. 16:407–414. 2008. View Article : Google Scholar | |
|
Keinan-Boker L, Vin-Raviv N, Liphshitz I, Linn S and Barchana M: Cancer incidence in Israeli Jewish survivors of World War II. J Natl Cancer Inst. 101:1489–1500. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Brown DR, Fouad MN, Basen-Engquist K and Tortolero-Luna G: Recruitment and retention of minority women in cancer screening, prevention, and treatment trials. Ann Epidemiol. 10(Suppl 8): S13–S21. 2000. View Article : Google Scholar | |
|
Newman LA, Hurd T, Leitch M, Kuerer HM, Diehl K, Lucci A, Giuliano A, Hunt KK, Putnam W and Wells SA: A report on accrual rates for elderly and minority-ethnicity cancer patients to clinical trials of the American College of Surgeons Oncology Group. J Am Coll Surg. 199:644–651. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Guevara C, Cook C, Herback N, Pietrobon R, Jacobs DO and Vail TP: Gender, racial, and ethnic disclosure in NIH K-Award funded diabetes and obesity clinical trials. Account Res. 13:311–324. 2006. View Article : Google Scholar | |
|
Azaiza F, Cohen M, Awad M and Daoud F: Factors associated with low screening for breast cancer in the Palestinian Authority: Relations of availability, environmental barriers, and cancer-related fatalism. Cancer. 116:4646–4655. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Bobo JK, Shapiro JA and Brustrom J: Efforts to locate low-income women for a study on mammography rescreening: Implications for public health practice. J Community Health. 31:249–261. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Garbers S, Jessop DJ, Foti H, Uribelarrea M and Chiasson MA: Barriers to breast cancer screening for low-income Mexican and Dominican women in New York City. J Urban Health. 80:81–91. 2003.PubMed/NCBI | |
|
Otero-Sabogal R, Stewart S, Sabogal F, Brown BA and Pérez-Stable EJ: Access and attitudinal factors related to breast and cervical cancer rescreening: Why are Latinas still under-screened? Health Educ Behav. 30:337–359. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Otero-Sabogal R, Owens D, Canchola J, Golding JM, Tabnak F and Fox P: Mammography rescreening among women of diverse ethnicities: Patient, provider, and health care system factors. J Health Care Poor Underserved. 15:390–412. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Erwin DO, Johnson VA, Trevino M, Duke K, Feliciano L and Jandorf L: A comparison of African American and Latina social networks as indicators for culturally tailoring a breast and cervical cancer education intervention. Cancer. 109(Suppl 2): 368–377. 2007. View Article : Google Scholar | |
|
Glanz K, Croyle RT, Chollette VY and Pinn VW: Cancer-related health disparities in women. Am J Public Health. 93:292–298. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Meiser B, Eisenbruch M, Barlow-Stewart K, Tucker K, Steel Z and Goldstein D: Cultural aspects of cancer genetics: Setting a research agenda. J Med Genet. 38:425–429. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Remennick L: The challenge of early breast cancer detection among immigrant and minority women in multicultural societies. Breast J. 12(Suppl 1): S103–S110. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Valdez A, Banerjee K, Ackerson L and Fernandez M: A multi-media breast cancer education intervention for low-income Latinas. J Community Health. 27:33–51. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Borrayo EA: Where's Maria? A video to increase awareness about breast cancer and mammography screening among low-literacy Latinas. Prev Med. 39:99–110. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Cohen M and Azaiza F: Increasing breast examinations among arab women using a tailored culture-based intervention. Behav Med. 36:92–99. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Jibaja-Weiss ML, Volk RJ, Kingery P, Smith QW and Holcomb JD: Tailored messages for breast and cervical cancer screening of low-income and minority women using medical records data. Patient Educ Couns. 50:123–132. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Navarro AM, Senn KL, McNicholas LJ, Kaplan RM, Roppé B and Campo MC: Por La Vida model intervention enhances use of cancer screening tests among Latinas. Am J Prev Med. 15:32–41. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Remennick L: ‘I have no time for potential troubles': Russian immigrant women and breast cancer screening in Israel. J Immigr Health. 5:153–163. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Berg WA, Blume JD, Adams AM, Jong RA, Barr RG, Lehrer DE, Pisano ED, Evans WP III, Mahoney MC, Hovanessian Larsen L, et al: Reasons women at elevated risk of breast cancer refuse breast MR imaging screening: ACRIN 6666. Radiology. 254:79–87. 2010. View Article : Google Scholar : | |
|
Yu J, Park A, Morris E, Liberman L, Borgen PI and King TA: MRI screening in a clinic population with a family history of breast cancer. Ann Surg Oncol. 15:452–461. 2008. View Article : Google Scholar | |
|
Robson M: Breast cancer surveillance in women with hereditary risk due to BRCA1 or BRCA2 mutations. Clin Breast Cancer. 5:260–268; discussion 269–271. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Begley JK, Redpath TW, Bolan PJ and Gilbert FJ: In vivo proton magnetic resonance spectroscopy of breast cancer: A review of the literature. Breast Cancer Res. 14:2072012. View Article : Google Scholar : PubMed/NCBI | |
|
Belkić K and Belkić D: Possibilities for improved early breast cancer detection by Padé-optimized magnetic resonance spectroscopy. Isr Med Assoc J. 13:236–243. 2011. | |
|
Katz-Brull R, Lavin PT and Lenkinski RE: Clinical utility of proton magnetic resonance spectroscopy in characterizing breast lesions. J Natl Cancer Inst. 94:1197–1203. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Sardanelli F, Fausto A and Podo F: MR spectroscopy of the breast. Radiol Med (Torino). 113:56–64. 2008. View Article : Google Scholar | |
|
Tse GM, Yeung DK, King AD, Cheung HS and Yang WT: In vivo proton magnetic resonance spectroscopy of breast lesions: An update. Breast Cancer Res Treat. 104:249–255. 2007. View Article : Google Scholar | |
|
O'Flynn EA, Wilson RM, Allen SD, Locke I, Scurr E and deSouza NM: Diffusion-weighted imaging of the high-risk breast: Apparent diffusion coefficient values and their relationship to breast density. J Magn Reson Imaging. 39:805–811. 2014. View Article : Google Scholar | |
|
Eyal E, Shapiro-Feinberg M, Furman-Haran E, Grobgeld D, Golan T, Itzchak Y, Catane R, Papa M and Degani H: Parametric diffusion tensor imaging of the breast. Invest Radiol. 47:284–291. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Allgood PC, Warwick J, Warren RML, Day NE and Duffy SW: A case-control study of the impact of the East Anglian breast screening programme on breast cancer mortality. Br J Cancer. 98:206–209. 2008. View Article : Google Scholar | |
|
Anttila A, Koskela J and Hakama M: Programme sensitivity and effectiveness of mammography service screening in Helsinki, Finland. J Med Screen. 9:153–158. 2002. View Article : Google Scholar | |
|
Duffy SW, Tabár L, Chen HH, Holmqvist M, Yen MF, Abdsalah S, Epstein B, Frodis E, Ljungberg E, Hedborg-Melander C, et al: The impact of organized mammography service screening on breast carcinoma mortality in seven Swedish counties. Cancer. 95:458–469. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Gabe R, Tryggvadóttir L, Sigfússon BF, Olafsdóttir GH, Sigurđsson K and Duffy SW: A case-control study to estimate the impact of the Icelandic population-based mammography screening program on breast cancer death. Acta Radiol. 48:948–955. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Morimoto T, Nagao T, Okazaki K, Kira M, Nakagawa Y and Tangoku A: Current status of breast cancer screening in the world. Breast Cancer. 16:2–9. 2009. View Article : Google Scholar | |
|
Sarkeala T, Anttila A, Saarenmaa I and Hakama M: Validity of process indicators of screening for breast cancer to predict mortality reduction. J Med Screen. 12:33–37. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Vahabi M: Breast cancer and screening information needs and preferred communication medium among Iranian immigrant women in Toronto. Health Soc Care Community. 19:626–635. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Domingo L, Sala M, Servitja S, Corominas JM, Ferrer F, Martínez J, Macià F, Quintana MJ, Albanell J and Castells X: Phenotypic characterization and risk factors for interval breast cancers in a population-based breast cancer screening program in Barcelona, Spain. Cancer Causes Control. 21:1155–1164. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Vanags A, Štrumfa I, Gardovskis A, Borošenko V, Aboliš A, Teibe U, Trofimovičs G, Miklaševičs E and Gardovskis J: Population screening for hereditary and familial cancer syndromes in Valka district of Latvia. Hered Cancer Clin Pract. 8:82010. View Article : Google Scholar : PubMed/NCBI | |
|
Venturini E, Losio C, Panizza P, Rodighiero MG, Fedele I, Tacchini S, Schiani E, Ravelli S, Cristel G, Panzeri MM, et al: Tailored breast cancer screening program with microdose mammography, US, and MR Imaging: Short-term results of a pilot study in 40–49-year-old women. Radiology. 268:347–355. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Obralić N and Bešlija S: How to make the best use of limited resources in breast cancer treatment - experiences in Bosnia & Herzegovina. J BUON. 11:21–29. 2006. | |
|
Council of the European Union. Council conclusions on reducing the burden of cancer. In: Employment, Social Policy, Health and Consumer Affairs Council Meeting; Luxembourg. June 10, 2008; |
