Feelings of Women With Strong Family Histories Who Subsequent to Their Breast Cancer Diagnosis Tested BRCA Positive.

ORIGINAL STUDY

Feelings of Women With Strong Family Histories Who Subsequent to Their Breast Cancer Diagnosis Tested BRCA Positive Meera Joseph, MD(c), BESc, BSc,* Faiza Rab, MBBS, MHSc, MSc,* Karen Panabaker, MSc, CGC, CCGC,Þ and Jeff Nisker, MD, PhD, FRCSC, FCAHS*

Objective: Family physicians in Canada as reported in several studies do not recognize the importance of family history in relation to breast/ovarian cancer and thus Canadian women with strong family histories continue to develop early-onset breast cancer without the knowledge of or ability to make choices regarding increased surveillance or preventative strategies. This study explored the feelings of women who learned about their hereditary risk only after their diagnosis younger than 52 years and who eventually tested positive for a BRCA gene mutation. Methods: Thirty-four such women were mailed an invitation to participate in this research including a letter of information, consent form, and discussion prompts for their written narrative response. Rigorous mixed method analyses were performed using Charmaz-based qualitative analyses as well as quantitative analyses. Results: Thirteen women (38.2%) responded with narratives for qualitative analysis from which 4 themes were coconstructed as follows: I, types of emotions; II, emotional response; III, coping with emotions; and IV, advice to women at similar risk. Women felt they should have learned about their hereditary risk from their family physician and through public education before their diagnosis. Although not experienced at the time of diagnosis, anger, frustration, and regret were experienced after receiving their BRCA results. These emotions arose from our research participants’ lack of opportunity for prior genetic counseling and testing opportunity for genetic counseling and testing. Conclusions: With increased public and physician education, it is hoped that women with significant family histories of breast/ovarian cancer will be identified before diagnosis and given options regarding cancer surveillance and risk reduction strategies. Key Words: Premenopausal breast cancer, BRCA1/2 genes, Emotions, Feelings Received July 4, 2014, and in revised form December 29, 2014. Accepted for publication December 29, 2014. (Int J Gynecol Cancer 2015;25: 584Y592)

omen diagnosed with early-onset breast cancer (generally premenopausal) have a 33% chance of carrying a

BRCA1 or BRCA2 gene mutation.1,2 Hereditary breast cancer, involving either the BRCA1 or the BRCA2 gene, is inherited in

*Department of Obstetrics and Gynaecology, Schulich School of Medicine & Dentistry, The University of Western Ontario; and †Cancer Genetics Program, London Health Sciences Centre, London, Ontario, Canada. Copyright * 2015 by IGCS and ESGO ISSN: 1048-891X DOI: 10.1097/IGC.0000000000000403

Address correspondence and reprint requests to Jeff Nisker, MD, PhD, FRCSC, FCAHS, London Health Sciences Centre, Victoria Hospital, Room E2-620E, 800 Commissioners Rd East, London, ON N6A 5W9, Canada. E-mail: [email protected]. The authors declare no conflicts of interest. This study was funded by Genome Canada and the Ontario Genomics Institute.

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an autosomal dominant manner, which means that siblings and offspring of gene mutation carriers will have a 50% risk of inheriting the gene mutation. Women with a BRCA gene mutation have a 45% to 87% risk of developing breast cancer at some point during their lifetime, with the age of onset usually at a significantly younger age than woman at average risk.3,4 Being identified as a BRCA gene mutation carrier qualifies women in Ontario to have breast magnetic resonance imaging (MRI) surveillance, starting as young as age 29 years, which has the ability to detect breast cancer in stage I significantly more often.5 Despite the availability of genetic counseling and genetic testing, as well as breast MRI surveillance and strategies for prevention including medical options, bilateral mastectomy,6Y9 bilateral salpingo-oophorectomy,10,11 and risk-reducing medication,12Y14 women who are at increased risk of hereditary breast cancer are not made aware of their risk or their options due to problems in the primary care setting.2,15Y22 These problems include family physicians not having enough time to take or update detailed family histories18Y20 and not having sufficient training regarding genetic and hereditary diseases in medical school20 or in accessing continuing education programs or Web sites.16,17,21,22 The purpose of this study was to explore the feelings of women in Southwestern Ontario, who had significant family histories of breast/ovarian cancer yet were not informed about their eligibility to have genetic counseling and genetic testing until after their breast cancer diagnosis and who subsequently tested positive for a BRCA gene mutation.

METHODS A mixed methods research approach used qualitative and quantitative analyses. Research ethics approval was obtained through the Western University’s Health Science Research Ethics Board (REB #7000) and the Lawson Clinical Research Impact Committee. Women in Southwestern Ontario diagnosed with breast cancer younger than 52 years (approximate age of menopause), who were not informed about their eligibility to have genetic counseling and genetic testing before their diagnosis, were referred subsequent to their diagnosis and were identified as having a BRCA gene mutation through the Cancer Genetics Clinic at the London Health Sciences Centre between 1997 and 2008. Thirty-four women were sent a letter of information, consent form, and discussion prompts by their primary genetics provider (K.P.) within the circle of care. The 4 discussion prompts were followed by space for open-ended responses as well as 4 Likert scale questions and 2 yes or no questions with additional space for comments. The survey questions are presented in Appendix 1. The written comments submitted by the research participants were transcribed into an electronic format that could be supported by NVivo 9 software.23 A grounded theory approach24 was used to analyze the data and develop a middle range theory. The narratives were first analyzed by independent reviewers (M.J., F.R.). During the analysis, the data were broken into small salient codes, using a line-by-line coding strategy. Initial coding was followed by a phase of focus coding where the data were recoded using the salient or

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significant codes from the previous phase coding. The data were continuously compared for similarities in content. The initial concepts were then categorized into preliminary subthemes and themes. The other researchers (K.P. and J.N.) participated in further organizing and developing the themes in relation to the narratives of the research participants. The quantitative data analysis was performed (by F.R.) using Excel spread sheet and STATA 11.25 Univariate and bivariate analyses were performed in STATA 11 determining the frequency of responses to different categories of answers. Frequencies and percentages were used to analyze previous knowledge about BRCA gene mutationYrelated breast cancer and opinions regarding preferred ways of learning about BRCA gene mutationYrelated breast cancer. One analyst (F.R.) did both qualitative and quantitative analyses, whereas others (M.J. and J.N.) only had access to qualitative analyses before the data were merged after the results of qualitative analyses were compiled.

RESULTS Of the 34 women invited to participate, 13 (38%) responded. Of the remaining 21, 1 was deceased, 2 actively declined to participate, 2 surveys returned as the patient had moved with no forwarding address, and the remaining 16 did not respond. One participant was excluded from the analysis as she lived outside of Canada before diagnosis. Descriptive analysis of the data indicated that despite having a significant family history of breast/ovarian cancer, 50% (6/12) of women had not had a discussion about their family history of breast/ovarian cancer with their family physician before their diagnosis, and none of the participants’ family physicians discussed their eligibility for genetic counseling and genetic testing. Almost 60% (7/12) women thought about developing breast cancer before their diagnosis. Most participants (10/12, 83%) wanted to have learned about their risk of developing hereditary cancer from their family physicians. Two thirds of our research participants also wanted to learn about their risk through public education. The participants shared personal stories and experiences. Their comments were a reflection of their emotions felt after being identified as having a BRCA gene mutation subsequent to their diagnosis of breast cancer. These comments are organized under 4 themes as follows: (I) types of emotions, (II) emotional response, (III) coping with emotions, and (IV) advice to women at similar risk. Subthemes emerged from participant responses to more than 1 prompt (Fig. 1). Table 1 shows themes I and II, along with their subthemes and their respective quotes. After individually completing both themes, it was realized that themes I and II were generated using identical quotes but presented the data from 2 different perspectives. To show and highlight this interaction between the themes, themes I and II are presented in the same table with theme I and its subthemes presented along the horizontal axis, and theme II and its subthemes are presented along the vertical axis, and shared quotes are placed in the middle. Through their narratives, women shared coping mechanisms such as networking, being physically active, and staying positive. Women also coped by informing family members about being a BRCA gene mutation carrier and educating them

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FIGURE 1. Outline of qualitative analysis. about opportunities for genetic counseling. The coping with emotions related to breast cancer diagnosis and being a BRCA gene mutation carrier was our third theme and is presented in Table 2. Being proactive, seeking genetic counseling, and appropriate cancer surveillance were some of the advice given to other women in a similar situation. Participants’ advices to women at similar risk are presented in Table 3. A timeline of emotions that research participants commented upon in relation to receiving the results of their BRCA genetic testing is illustrated in Figure 2. Specific emotions of anger, frustration, and regret were experienced by participants after receiving their BRCA genetic test results, yet not at the time of their breast cancer diagnosis. This depicts the way in which BRCA genetic testing subsequent to their cancer diagnosis acted as an emotional trigger, significantly modifying their experience with breast cancer.

DISCUSSION This study reveals the emotional experiences of a previously unstudied population of young breast cancer patients

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who were not aware of the importance of their family history until after their diagnosis and were not referred for genetic counseling and consideration of BRCA genetic testing until after they were diagnosed. Although a response rate of 38% could have been higher, it is conceivable that some of the eligible women may have passed away without the genetics providers’ knowledge or the invitation to participate alone may have caused them to be too emotional to respond. This response rate speaks to how much the participants wanted to share their stories despite how difficult it may have been to do so. This is expressed by research participant (RP)7 who shared, ‘‘Ithis has been one of the hardest surveysI’’ Four unique and specific emotions were elicited in response to testing positive for a BRCA gene mutation subsequent to their diagnosis of breast cancer: anger, frustration, grief, and regret. Although the emotions are distributed among comments directed toward events occurring both before and subsequent to testing, the emotional response was triggered at the time of testing positive for a BRCA gene mutation (Fig. 2), in response to appreciating that they should * 2015 IGCS and ESGO


IID: Family history of breast cancer

IIC: Lack of information

‘‘Ithe idea of breast cancer af- ‘‘Saddened that I did not have this ‘‘I do wish that I would have fecting me was so minimal as I info earlier.’’ RP5 known about my genetic was told as there was no one on mutation years ago.’’ RP7 my mom’s side who had it, so ‘‘If I knew I had the gene to the gene wasn’t there.’’ RP7 develop cancer, I would haveI requested more aggressive treatment after my initial surgery.’’ RP8 ‘‘I was always aware that I may have ‘‘I feel sad now, as there are ‘‘I would have liked to have carried the gene. It was confusing departments out there to help. My known either as I would for me how to go about getting family doctor at the time said I have considered oophotested so I never did until after my probably would not get cancer rectomy and prophylactic diagnosis.’’ RP3 because my grandparents died mastectomies.’’ RP4 ‘‘It [the diagnosis] was 12 years when my mother was 12 and are ago. Times have changed, and I just guessing it was cancer.’’ RP2 didn’t even know genetic testing had occurred at the time.’’ RP4 ‘‘I was always aware that I may have ‘‘I had a lot of cancer in extended carried the geneI I was anxious family but never considered my whole life wondering when I there was a genetic link or even was going to get it.’’ RP3 availability of being tested.’’ RP5 ‘‘I was told as there was no one on my mom’s side who had it, so the gene wasn’t there. I am frustrated with the medical system.’’ RP7

IE: Regret

‘‘It’s awful to join the cancer club.’’ RP4 ‘‘I feel now that with help, maybe we would have got ‘‘I think I reacted in the grieving type it early before surgery, process. At first, I was angry then chemo and radiation had progressed to acceptance then to happen.’’ RP2 gathering information to my options.’’ RP13

ID: Sadness/Grief

IIB: BRCA+

IC: Frustration/Anger

‘‘I still fear it (cancer) will come back.’’ RP5 ‘‘I am scared that every time I have a pain etc, I think it is cancer.’’ RP11 ‘‘My experience is that it is an ongoing event. I had it 12 years ago, 2 years ago, and now it is always at the back of my mind when it will come back again.’’ RP2

IA: Worry/Fear

Theme I: Types of Emotions

IIA: Breast cancer diagnosis

Theme II: Emotional Response to

TABLE 1. Emotional response of women who tested positive for a BRCA gene mutation subsequent to their breast cancer diagnosis


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‘‘Ifor my 2 girls and sonI I fear that they may have to make decisions that could affect their early adult year.’’ RP5 ‘‘It does make me more fearful for my daughters.’’ RP10 ‘‘I worry about my daughter and my niece.’’ RP11 ‘‘The reason that I went through the genetic testing was for my sister and brothers’ children. I felt that if this could help them or at least bring their doctor’s attention to their risk factors, then I had to do it.’’ RP6 ‘‘Ifeltitwasnecessaryto inform myfamily members, close relatives, and cousins that I carry the hereditary geneI’’ RP7

IA: Worry/Fear

IC: Frustration/Anger

ID: Sadness/Grief

Theme I: Types of Emotions

IIID: Informing family members

‘‘Network with other high-risk women (or those who have the diagnosis)’’ RP13 ‘‘I I have done my best to be proactive (cycling)I I am very active and know that my daily physical activity helps me to ‘cope’ with times of fear when I think of my cancer possibly returningI’’ RP7 ‘‘I.I was able to deal with it with a positive attitude (which I believe was the most important part of my healing). I met some wonderful people who will be lifelong friends, and it gave me a better appreciation for life. I never felt sorry for myself, only fortunate that I am still here to enjoy my family.’’ RP3 ‘‘I felt it was necessary to inform my family members, close relatives, and cousins that I carry the hereditary gene. The genetic counselors sent me out the template, and I sent it to all that I wanted to know and to really pass on this information.’’ RP7 ‘‘The reason that I went through genetic testing was for my sister and brothers’ children. I felt that if this could happen to them or at least bring their doctor’s attention to their risk factors, then I had to do it.’’ RP6

Comments

IE: Regret


IIIC: Positive attitude

IIIA: Networking IIIB: Physical activity

THEME III: Coping With Emotions

TABLE 2. Coping with emotions related to breast cancer diagnosis and testing positive for a BRCA gene mutation

IIF: Family members at high risk

IIE: Concerns for future generations

Theme II: Emotional Response to

TABLE 1. (Continued)

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TABLE 3. Advice to women at similar risk THEME IV: Advice to Women at Similar Risk IVA: Seek out and use information IVB: Pursue genetic counseling

IVC: Pursue better surveillance (MRI)

IVD: Peer support and networking

IVE: Self-advocacy

IVF: Be proactive

IVG: Know options for prevention

IVH: Health promotion

Comments ‘‘I tell them to do everything they can to search it out.’’ RP2 ‘‘Take advantage of all the information available. (However, I don’t agree with reading too much.) Do annual mammograms. Get to know your breasts and ensure your partner is informed.’’ RP3 ‘‘I guess my advice would be that knowledge is everything, and early detection is the key to take advantage of this that the genetic testing will bring.’’ RP6 ‘‘Igo talk to genetic counseling. I wished I had the opportunity a lot sooner.’’ RP7 ‘‘Do the genetic testing.’’ RP3 ‘‘I cannot think of a better place to spend health care dollars than prevention. The advances in genetic mapping are excitingI and will prevent much stress and suffering.’’ RP5 ‘‘Just keep getting checked because early detection is the key.’’ RP11 ‘‘Iearly detection is the key to take advantage of this that the genetic testing will bring.’’ RP6 ‘‘Screen Screen ScreenVmam and MRIsI’’ RP5 ‘‘Don’t settle for mammogram, ask for ultrasounds also. They never found mine on a mammogram. I had them as often as suggested. But it was very obvious on an ultrasound.’’ RP12 ‘‘Better screening strategies (ultrasound etc) and capable technicians to read reports.’’ RP7 ‘‘I am a peer support volunteer for cancer, and I always stress to the peers that I talk to, to at least talk about the hereditary part and go talk to genetic counseling. I wished I had the opportunity a lot sooner.’’ RP7 ‘‘II met some wonderful people who will be lifelong friends, and it gave me a better appreciation for life. I never felt sorry for myself only fortunate that I am still here to enjoy my family.’’ RP3 ‘‘If I wasn’t for myself of doing regular lump checks and finding cancer both times, I may not be here todayI’’ RP9 ‘‘I was misdiagnosed and my cancer spread. If I wasn’t proactive in insisting of another scan, I probably wouldn’t be here today.’’ RP7 ‘‘Be your own advocate, there is so much breast cancer. I think now a lot of symptoms may be ignored by patient and physician.’’ RP9 ‘‘Be persistent. If your doctor doesn’t listen, see someone else. I would be dead today if my daughter hadn’t made me change doctors.’’ RP12 ‘‘The only thing I find that makes me still angry was that my family doctor pooh-poohed my finding a lump. [My] mom was his patient as well. If I hadn’t pushed for a biopsy, I would not be alive today as my cancer was very aggressiveIAdvocate, advocate, and advocate for yourself. Don’t let your doctor stop you from having biopsies if you find something. I am alive today because I wouldn’t take no for an answer.’’ RP4 ‘‘Be proactive and be informed, and gather all the necessary information to make informed decision. Talk to the professionals who are so well educated to direct and guide in the right direction of what to do, how to go about doing it.’’ RP7 ‘‘Get all the information and make informed decision. Then be at peace with yourself no matter what happens down the road.’’ RP4 ‘‘Iif looking to have prophylactic mastectomies and oophorectomy, talk to people who have gone through itI Talk to specialists, eg, endocrinologist, about having to deal with long-term effects, eg, menopause, bone health.’’ RP4 ‘‘Some may think of prophylactic measure like mastectomy/reconstruction before.’’ RP5 ‘‘Get surgery as soon as you are able. Done having babies, and don’t delay thinking you might not get it.’’ RP8 ‘‘Whatever you decide, be confident in your decision. Try not to second guess yourself, but that seems to be human nature.’’ RP13 ‘‘Knowing [that you have hereditary breast cancer] can be scary, but it gives you control over where to lead your life choices. Not wanted to know can shorten your life, because when you find out, it may be too late, and now your life is out of your hands.’’ RP4



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FIGURE 2. Timeline of emotions. have become aware of this fact before they developed their breast cancer, at a time when they could have considered options for increased surveillance for earlier diagnosis or prevention strategies. As depicted in the timeline (Fig. 2), participants received a diagnosis of breast cancer before receiving information about their BRCA gene mutation. Participants’ comments on their emotions regarding their diagnosis of breast cancer have been previously reported for women in other breast cancer populations, such as fear of return,26 worry,27 sadness,27 and grief.27 However, our participants added regret over not having had the knowledge about their gene mutation status to perhaps facilitate a diagnosis of cancer at an earlier stage (Table 1; themes IE/IIA). Although risk reduction strategies would have been discussed with participants had their BRCA gene mutation status been identified earlier, studies suggest that choosing those options (ie, prophylactic mastectomy or oophorectomy) is dependent upon influences such as psychosocial factors and past experiences,28Y30 and overall the uptake is low.31Y33 As (RP2) suggested (Table 1; themes IE/IIA), for those who are not comfortable with preventative strategies, there are other options such as breast MRI surveillance for earlier cancer detection, which could potentially increase cancer survival rates in women. Women commented on feelings of concern for future generations and family members at high risk (Table 1; themes 1/IIE and I/IIF), which has also been reported for other women who learn that they carry a BRCA gene mutation. Women from high-risk families in Ontario may have low levels of knowledge about hereditary breast cancer,34 in part through their belief that their paternal family history is irrelevant30,35 and that sharing physical attributes with a family member makes them more likely to share other genetic attributes as well.36,37 The core emotions reemerge in comments of women in our study from this lack of information and education they received regarding the significance of their family history (Table 1; themes I/IIC and I/IID) from their family physician. Women at high hereditary risk may not be made aware of the potential significance of their family history or the opportunity to have genetic counseling because their family physician may not have received sufficient cancer genetics training in medical school or through continuing education programs or Web sites.2,15,17,20,21,38 Often family physicians do not have time to take or update family histories.18Y20 Ultimately, it is likely that a lack of physician education and/or absent understanding through public education may have contributed to the avoidable circumstance that the participants found themselves in. This recognition elicited emotions of anger and frustration directed at the

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physicians who failed to recognize the importance of their family history (Table 2; themes IC/IIB). In addition, participants felt sadness and regret over not having the information about how to pursue genetic testing as well as more rigorous screening or preventative options (Table 2; themes IC/IIC). Angelina Jolie, who recently publicized her decision to access genetic counseling, BRCA genetic testing, and preventative surgery to significantly reduce her risk of developing a breast and/or ovarian cancer,39 has done a great service in public and physician education, a service that could have been better provided much earlier in Canada by government and professional organizations.40 The impact has already been seen in the tripling of referrals to the Cancer Genetics Clinic at the London Health Sciences Centre within 2 months after Jolie’s story was published, as well as a significant increase in phone inquiries regarding referrals, many of which are from family physicians who have not previously referred patients for this reason. Similarly, the British Columbia Cancer Agency’s hereditary cancer program has seen a 60% increase in referrals since May 2013. If Angelina Jolie had gone public with her story 20 years ago, our participants’ stories may have been different. Women with a family history of breast/ovarian cancer who do not hear about Angelina Jolie’s story, as well as family physicians, residents, and medical students, must be educated to the importance of taking and updating family histories related to breast/ovarian cancer and the opportunities for improved cancer surveillance through breast MRI, as well as the availability of genetic counseling and genetic testing services. Furthermore, women must be empowered with public education strategies so that they may take charge of their own health promotion. As Angelina Jolie expressed in the conclusion of her piece, ‘‘Life comes with many challenges. The ones that should not scare us are the ones we can take on and take control of.’’ Her sentiments were echoed by RP4 who shared, ‘‘Knowing [that you have hereditary breast cancer] can be scary, but it gives you control over where to lead your life choices.’’

CONCLUSIONS Receiving a diagnosis of breast cancer can be an emotional experience for any woman; however, learning that her cancer might have been detected earlier or possibly prevented had an appropriate family cancer history assessment been done before that diagnosis elicits specific emotions of anger, frustration, and regret related to being denied the opportunity to take control over one’s personal health and explore options for increased surveillance and risk reduction strategies. With increased public and physician education, it is hoped that women with significant family histories of breast/ovarian cancer will be more readily identified before a putative diagnosis and presented with a more accurate risk assessment and associated options.

ACKNOWLEDGMENTS The authors wish to thank Dr Meredith Vanstone, Dr Peter Ainsworth, Dr Winsion Chow, Dr Muriel Brackstone, and Laura Lester.

REFERENCES 1. Claus EB, Schildkraut JM, Thompson WD, et al. The genetic attributable risk of breast and ovarian cancer. Cancer. 1996;77:2318Y2324. * 2015 IGCS and ESGO




2. Vig HS, Armstrong J, Egleston BL, et al. Cancer genetic risk assessment and referral patterns in primary care. Genet Test Mol Biomarkers. 2009;13:735Y741. 3. Antoniou A, Pharoah PD, Narod S, et al. Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history: a combined analysis of 22 studies. Am J Hum Genet. 2003;72:1117Y1130. 4. Ford D, Easton DF, Stratton M, et al. Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. The Breast Cancer Linkage Consortium. Am J Hum Genet. 1998;62:676Y689. 5. Warner E, Hill K, Causer P, et al. Prospective study of breast cancer incidence in women with a BRCA1 or BRCA2 mutation under surveillance with and without magnetic resonance imaging. J Clin Oncol. 2011;29:1664Y1669. 6. Meijers-Heijboer H, van Geel B, van Putten WL, et al. Breast cancer after prophylactic bilateral mastectomy in women with a BRCA1 or BRCA2 mutation. N Engl J Med. 2001;345:159Y164. 7. Hartmann LC, Schaid DJ, Woods JE, et al. Efficacy of bilateral prophylactic mastectomy in women with a family history of breast cancer. N Engl J Med. 1999;340:77Y84. 8. Rebbeck TR, Friebel T, Lynch HT, et al. Bilateral prophylactic mastectomy reduces breast cancer risk in BRCA1 and BRCA2 mutation carriers: the PROSE Study Group. J Clin Oncol. 2004;22:1055Y1062. 9. Hartmann LC, Sellers TA, Schaid DJ, et al. Efficacy of bilateral prophylactic mastectomy in BRCA1 and BRCA2 gene mutation carriers. J Natl Cancer Inst. 2001;93:1633Y1637. 10. Finch A, Beiner M, Lubinski J, et al. Salpingooophorectomy and the risk of ovarian, fallopian tube, and peritoneal cancers in women with a BRCA1 or BRCA2 mutation. JAMA. 2006;296:185Y192. 11. Eisen A, Lubinski J, Klijn J, et al. Breast cancer risk following bilateral oophorectomy in BRCA1 and BRCA2 mutation carriers: an international case-control study. J Clin Oncol. 2005;23:7491Y7496. 12. Cuzick J, Forbes J, Edwards R, et al. First results from the International Breast Cancer Intervention Study (IBIS-I): a randomized prevention trial. Lancet. 2002;360:817Y824. 13. Gronwald J, Tung N, Foulkes WD, et al. Tamoxifen and contralateral breast cancer in BRCA1 and BRCA2 carriers: an update. Int J Cancer. 2006;118:2281Y2284. 14. Narod SA, Brunet J, Ghadirian P, et al. Tamoxifen and risk of contralateral breast cancer in BRCA1 and BRCA2 mutation carriers: a case-control study. Lancet. 2000;356:1876Y1881. 15. Vanstone M, Chow W, Lester L, et al. Recognizing BRCA gene mutation risk subsequent to breast cancer diagnosis in southwestern Ontario. Can Fam Physician. 2012;58:e258Ye266. 16. Ontario Health Insurance Program. Bulletin 4352: Provincial Predictive Genetic Testing Service for Hereditary Breast, Ovarian and Colon Cancers. Ministry of Health and Long-term Care 2000 May [Cited 2013 Mar 21]. Available at: http://www.health.gov.on.ca/en/pro/programs/ohip/bulletins/ 4352/bul4352.aspx. Accessed March 25, 2013. 17. Carroll JC, Rideout AL, Wilson BJ, et al. Genetic education for primary care providers: improving attitudes, knowledge, and confidence. Can Fam Physician. 2009;55:e92Ye99. 18. Emery J, Watson E, Rose P, et al. A systematic review of the literature exploring the role of primary care in genetic services. Fam Pract. 1999;16:426Y445.


19. Rich EC, Burke W, Heaton CJ, et al. Reconsidering the family history in primary care. J Gen Intern Med. 2004;19:273Y280. 20. Watson EK, Shickle D, Qureshi N, et al. The ‘new genetics’ and primary care: GPs’ views on their role and their educational needs. Fam Pract. 1999;16:420Y425. 21. Greendale K, Pyeritz RE. Empowering primary care health professionals in medical genetics: how soon? How fast? How far? Am J Med Genet. 2001;106:223Y232. 22. Carroll JC, Cappelli M, Miller F, et al. Genetic services for hereditary breast/ovarian and colorectal cancersVphysicians’ awareness, use and satisfaction. Community Genet. 2008;11:43Y51. 23. NVivoi 9 Software [computer program]. Doncaster, Victoria, Australia: QSR International Pty Ltd.; 2010. Available at: http://www.qsrinternational.com/products_nvivo.aspx. 24. Charmaz K. Constructing Grounded Theory: A Practical Guide Through Qualitative Analysis. Thousand Oaks, CA: Sage; 2006. 25. Stata: Release 11. Statistical Software. College Station, TX: StataCorp LP [computer program]; 2009. Available at: http://www.stata.com/ 26. Nelson JP. Struggling‘ to gain meaning: living with the uncertainty of breast cancer. ANS Adv Nurs Sci. 1996;18:59Y76. 27. Madden J. The problem of distress in patients with cancer: more effective assessment. Clin J Oncol Nurs. 2006;10:615Y619. 28. Weil J. Psychosocial Genetic Counseling. New York, NY: Oxford University Press; 2000. 29. Schneider K. Counseling About Cancer: Strategies for Genetic Counseling. 2nd ed. New York, NY: Wiley-Liss; 2002. 30. Patenaude AF. Genetic Testing for Cancer: Psychological Approaches for Helping Patients and Families. 1st ed. Washington, DC: American Psychological Association; 2005. 31. Metcalfe KA, Birenbaum-Carmeli D, Lubinski J, et al. International variation in rates of uptake of preventive options in BRCA1 and BRCA2 mutation carriers. Int J Cancer. 2008;122:2017Y2022. 32. Singh K, Lester J, Karlan B, et al. Impact of family history on choosing risk-reducing surgery among BRCA mutation carriers. Am J Obstet Gynecol. 2013;208:329.e1Y329.e6. 33. Nisker J. From Calcedonies to Orchids: Plays Promoting Humanity in Health Policy. Toronto, Canada: Iguana Press; 2012. 34. Panabaker K, Azcona C, McCullum M, et al. A survey of women receiving an uninformative BRCA1/2 result: reactions, risk perceptions, and disclosure to family members. In: Dickerson CD, Wicklund CAL, eds. Abstracts From the Twenty-First Annual Education Conference of the National Society of Genetic Counselors (Phoenix, AZ, November 2002). New York, NY: Kluwer Academic/Plenum Publishers: 2002:445Y537. 35. Katapodi MC, Aouizerat BE. Do women in the community recognize hereditary and sporadic breast cancer risk factors? Oncol Nurs Forum. 2005;32:617Y623. 36. Klitzman RL. Misunderstandings concerning genetics among patients confronting genetic disease. J Genet Couns. 2010;19:430Y446. 37. Emslie C, Hunt K, Watt G. A chip off the old block? Lay understandings of inheritance among men and women in mid-life. Public Underst Sci. 2003;12:47Y65. 38. Carroll JC, Cremin C, Allanson J, et al. Hereditary breast and ovarian cancers. Can Fam Physician. 2008;54:1691Y1692.



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39. Jolie A. My medical choice. The New York Times; May 14, 2013. http://www.nytimes.com/2013/05/14/opinion/ my-medical-choice.html/?_r=0. 40. Nisker J. Finally a public health education initiative to empower Canadian women with a family history of breast/ovarian cancer to be in charge of their health: why did it take the American Angelina Jolie? J Obstet Gynaecol Can. 2013;35:689Y691.

APPENDIX 1: SURVEY QUESTIONS 1. Before your breast cancer diagnosis, how often did you think about the possibility of developing breast cancer? 2. Before your breast cancer diagnosis, how often did you and/or your family talk about your risk of developing breast and/or ovarian cancer? 3. Before your breast cancer diagnosis, how often did your family doctor talk with you about your family history of breast and/or ovarian cancer? 4. Before your breast cancer diagnosis, how often did your family doctor talk with you about your eligibility to have genetic counseling?

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5. Before your breast cancer diagnosis, did any other health professional(s) talk with you about the option to have genetic counseling? 6. Before your breast cancer diagnosis, did you feel that you had adequate knowledge about your risk of developing breast cancer? Please describe below how you feel about not knowing your options for genetic counseling and potential strategies for earlier detection or risk reduction of breast cancer. How would you have liked to learn about your risk of developing breast cancer and the opportunity for genetic counseling? 7. Please describe below how you feel about having developed hereditary breast cancer? 8. What thoughts or advice would you like to share with other women at high risk of developing hereditary breast cancer? 9. Is there anything else you would like to tell us about your experience with learning that you had a hereditary form of breast cancer? Please use as much space as you need and attach extra sheets if necessary.



Marital and reproductive histories of women with cancer of the breast and their sisters.

The Effect of Reproductive Factors on Breast Cancer Presentation in Women Who Are BRCA Mutation Carrier.

Knowledge about hereditary cancer of women with family histories of breast, colorectal, or both types of cancer.

Who Improved in a Trauma Intervention for HIV-Positive Women with Child Sexual Abuse Histories?

Exome sequencing in a breast cancer family without BRCA mutation.

The impact of a breast cancer diagnosis in young women on their relationship with their mothers.

A high frequency of BRCA mutations in young black women with breast cancer residing in Florida.

Diagnosis of breast cancer in young women.

Comparison of nodal metastasis between BRCA mutation carriers and non-BRCA mutation carriers with breast cancer.

Adjuvant Oophorectomy in the Treatment of Early-Stage BRCA Mutation-Positive Breast Cancer.

Family Health Histories and Their Impact on Retirement Confidence.

The mammographic parenchymal patterns of nulliparous women and women with a family history of breast cancer.

Breast cancer diagnosis: biographical disruption, emotional experiences and strategic management in Thai women with breast cancer.

Impact of a False-Positive Screening Mammogram on Subsequent Screening Behavior and Stage at Breast Cancer Diagnosis.

Comparison of risk management strategies between women testing positive for a BRCA variant of unknown significance and women with known BRCA deleterious mutations.

Blunted natriuretic responses in normotensive men with positive family histories of hypertension.

Reduced venous compliance in normotensive men with positive family histories of hypertension.

Women who kill their children.

A review of "Family caregivers of women with breast cancer in Iran report high psychological impact six months after diagnosis".

A step towards a HER2-positive breast cancer super family.

Patterns and predictors of first and subsequent recurrence in women with early breast cancer.

Breast cancer, BRCA mutations, and attitudes regarding pregnancy and preimplantation genetic diagnosis.

Salivary gland cancer in BRCA-positive families: a retrospective review.

Family History of Cancer in Relation to Breast Cancer Subtypes in African American Women.