Introduction

Women with strong family histories of breast cancer, genetic variants that predispose them to it, or substantial risk factors in their own medical histories can face between 20% and 80% lifetime risk of developing the disease [1]. Genetic testing provides personalized risk information that can inform risk-reduction choices, and enhanced surveillance routines (including breast MRIs, earlier initiation of mammograms, and more frequent screening mammograms) substantially increase the chances of diagnosing breast cancer in its earlier and more treatable phases [2]. Women can also reduce their elevated risk substantially—by 50% to 95%—using a variety of methods, including risk-reducing surgeries to remove one’s breasts (prophylactic mastectomy) and/or ovaries (prophylactic oophorectomy) as well as chemoprevention approaches that involve a daily dose regimen of anti-estrogen medication. Women’s decisions about whether and how to engage with these risk-management options can be complicated and often entail difficult tradeoffs, but decision making about breast cancer prevention has received relatively little scholarly attention [2].

There is much we do not know about prevention-related decision making among high-risk women. Increasing evidence shows that women’s choices and actions are shaped over time by a range of affective, emotional, cognitive, informational, interpersonal, and structural influences. These influences may include perceived risk of cancer and personal conceptualizations of what risk means for oneself and one’s family; family history of cancer and personal exposure to the cancers of others; general anxiety and specific cancer-related worries, medical and personal uncertainties, timing considerations, social networks and social support, and varied effects of socioeconomic status [2–6]. In addition, complex information transfer and information processing efforts rely on communication with healthcare providers who may vary in their ability to talk to their patients about risk and prevention [2, 5].

Although racial differences in the dynamics of prevention decision making have rarely been studied, there is ample evidence of broader racial disparities related to breast cancer. In the United States today, Black women are diagnosed with breast cancer at the same rate as white women, although at younger ages and later stages of disease, and with higher breast cancer mortality rates [7–9]. Well-established racial disparities that disadvantage Black women also exist in breast cancer screening, genetic testing among diagnosed women, and guideline-concordant use of non-invasive treatments for early-stage breast cancer [10–13]. Mammograms constitute a partial exception: Black women may be more likely to have appropriately-timed mammograms [14], but are less likely to have access to the highest-quality mammogram technologies and follow-up services [12]. Among high-risk women, Black women are relatively less likely to be knowledgeable about personal cancer risk or prevention approaches, and less frequently use either genetic testing or enhanced surveillance routines to help manage risk [15–17]. In addition, the relative use of prophylactic mastectomy, prophylactic oophorectomy, and chemoprevention by different groups of high-risk women suggests that Black women may also be less likely to utilize these methods of breast cancer prevention. Given this substantial range of racial disparities in screening rates and outcomes related to breast cancer, it seems likely that there may also be racial differences in the underlying dynamics through which high-risk women make decisions about their options for reducing breast cancer risk [18, 19]. Little is known about the origins of these racial disparities in screening, use of cancer prevention measures, and cancer outcomes, but they are likely to be quite complex, and may be driven by intertwined influences at personal, cultural, interactional, and structural levels.

This article draws on interviews with women at high risk of breast cancer, including both Black and white women, to address important gaps in our understanding of risk-management decision making. Specifically, the work aims to address two key questions: (a) are there notable differences between the experiences of Black and white high-risk women navigating the dynamics involved in managing breast cancer risk? and if so, (b) what are the consequences of these racial differences on women’s ability to effectively manage elevated breast cancer risk? Using grounded theory methodology and an inductive analysis of semi-structured in-depth interviews, this study documents the existence and consequences of racial differences in cancer prevention decision making. Identifying the range of racial differences in risk-related experiences and decisions is a novel outcome in itself, and it also sets the stage for future research diving deeper into the origins and effects of racial differences in risk-reduction decision making. Insights from the narratives of women at high-risk of breast cancer also form a basis for designing future interventions to better empower diverse women making decisions about breast cancer prevention.

Materials and methods

Data come from fifty semi-structured interviews conducted by the first author between May 2015 and March 2016. Recruitment, data collection, coding, and analysis are described here, and additional details are available in S1 Appendix.

Recruitment & data collection

Informants were recruited in three ways: (1) in-person recruitment of patients at the High-Risk Breast Program and Cancer Genetics clinics of the Ohio State University (OSU) Comprehensive Cancer Center; (2) recruitment of ResearchMatch volunteers (a national online database of research volunteers) through email and phone, and listing on StudySearch (a database of OSU research studies open for enrollment); and (3) snowball sampling from interviewed informants. Eligibility criteria included being at least 18 years of age, with no prior diagnosis of cancer and above average risk of breast cancer, and self-identifying as “white” or “Black or African American”. “Black or African” participants are referred to in this manuscript by the broader category: “Black”. Purposeful over-recruitment Black women for comparative purposes resulted in a final sample of 30 non-Hispanic white and 20 Black women; participants self-identified race and ethnicity. Six of the white women were diagnosed BRCA mutation carriers and therefore categorized as “severe” risk. Of the remaining 44 women, 41 (22 white and 19 Black) were “high” risk, and the last 3 women were “moderate” risk [20]. Table 1 presents demographic characteristics of the sample.

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Table 1. Sample demographics.

https://doi.org/10.1371/journal.pone.0278742.t001

Semi-structured interviews focused on eliciting women’s risk- and prevention-related stories in their own words, with follow-up questions to fill in gaps. Initial questions such as “When and how did you discover that you were at particular risk for breast cancer?” and “What kinds of actions have you considered to prevent breast cancer in your future?” aimed to elicit women’s stories in as much detail as possible; this informant-driven conversation comprised the majority of each interview. Non-guiding probes such as “what happened next?” and “how did you feel about that?” encouraged informants to delve deeper into their stories and share more detail. The interview protocol also included a range of follow-up questions on topics including “sources and content of risk information” and “decision-making process”, which were designed to elicit thorough coverage of women’s thoughts, feelings, and reflections on all topics related to the original research questions (see abbreviated interview protocol in S1 Table). Interviews were conducted at times and locations chosen by informants and averaged 57 minutes in length (range: 22–120 minutes). The study was conducted with approval of the OSU Cancer Institutional Review Board (IRB). Written informed consent was obtained from all participants interviewed in person. For participants interviewed by phone, oral consent was obtained and recorded after oral review of the informed consent document by the interviewer; this method was approved by the IRB.

Results

The core decision-making dynamics we identified are summarized in Table 2, with bolded items corresponding to dynamics where the experiences described by Black and white women differed most substantially. As this table illustrates, many of the core decision-making dynamics that high-risk women navigate differ substantially by race. In this section, we demonstrate that the experiences of these groups are distinct in terms of (a) how women make sense of their own breast cancer risk, and how they prioritize risk within the contexts of their broader lives (“contextualizing risk”); (b) how women learn about and conceptualize their options for preventing cancer and/or ensuring that cancer gets diagnosed early (“conceptualizing risk management”); and (c) the constraints women face throughout their decision-making and risk-management processes (“constraints on decision making and risk management”). Together, these patterns of racial difference suggest that Black women face more constraints on their risk-management decision making, have less access to the detailed information that would allow them to choose risk-management options, and are less well equipped to focus on coping with their specific breast cancer risks.

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Table 2. Core decision-making dynamics^a.

https://doi.org/10.1371/journal.pone.0278742.t002

Discussion

The contexts within which white and Black women make prevention decisions differ in important ways. These contexts are complex, involving past experiences, current health challenges, emotional states, access to and interactions with healthcare providers, and resource availability and constraints. But the broad patterns revealed by this study suggest that Black women may be less equipped to focus on breast cancer risk as an issue to be addressed proactively, may less frequently possess the information that would facilitate risk-management decision making, and may be more constrained in their ability to make and carry out those health-protective decisions. These patterns likely originate from a range of causes, which may include differential access to financial and other resources (i.e., comprehensive health insurance, household income and wealth, adequate time away from work and family responsibilities to seek out healthcare), cultural differences in orientation toward healthcare providers and options, differences in personal exposure to cancer and cancer treatment in loved ones, differential access to specialists or risk-informed PCPs, and distinct experiences of respect or discrimination in healthcare settings.

Women’s exposure to the cancers of loved ones forms the backdrop that shapes their own thinking about breast cancer risk and prevention. Due to their life experiences with many different types of cancer, the Black women we interviewed were less likely than the white women to think of themselves as at high risk specifically for breast and ovarian cancer. Although Black women may indeed be at higher-than-average risk for other cancers as well, underestimating specific biological risks for breast and ovarian cancers that run in their families may substantially affect how women cope with those risks [22]. Women with lower perceived personal cancer risk are less likely to engage in screening, exercise less, and eat fewer fruits and vegetables [23]. Conversely, women who have a higher perceived risk of breast cancer in particular, as well as women who have a family history of breast cancer rather than other cancers, are more likely to undergo first or repeat mammograms [24, 25] and more able to consider preventive surgery or chemoprevention options.

Analysis of the interview data in this study also suggest that Black women at elevated risk may generally be less worried about cancer than their white counterparts. Several other dynamics observed in the interviews may account for this apparent difference: (1) Black informants more commonly have a generalized perception of cancer risk that may be too diffuse to focus a specific sense of worry; (2) they are more often worried about serious current health or economic concerns that likely take precedence over worry about possible future cancers; and (3) they have less specific information than white women about breast cancer risk and prevention options. Given that cancer worry usually motivates information-seeking, screening, and prevention-oriented behaviors, it is possible that low levels of worry among Black women may undermine their engagement with risk-management activities [25–28]. However, excessive cancer worry may itself constitute a mental health problem and may result in avoidance behaviors under some circumstances, so future interventions will need to motivate risk-management behaviors in ways that match objective risks and support emotional needs [26].

Our finding that the Black women in our study more often connect their faith to thoughts and worries about cancer suggests a possible foundation for helping some women cope proactively with cancer risk. Across research on cancer survivorship and other health issues, spirituality is usually found to be an effective coping mechanism, and to provide helpful avenues for social and emotional support. In rarer situations, reliance on spirituality has also been shown to undermine positive health behaviors [18, 19]. Programs that aim to empower Black women to employ breast cancer risk-management methods may at least need to integrate the understanding that some women are oriented toward coping by relying on God. Further research on the relationships between spirituality and health behavior may also help illuminate ways to build on the positive impacts of faith to increase patients’ engagement with risk-management behavior.

The existence of non-cancer-related health problems or risks in a woman’s life may reduce her investment in understanding or addressing breast cancer risk. This situation was more common among the Black women in our sample, likely reflecting population-based racial disparities in rates of chronic and acute disease [29, 30]. A smaller qualitative study conducted among low-income women of color also suggested that women prioritize current health conditions over addressing breast cancer risk [31]. Prioritizing present-day health threats over potential future problems could be a realistic, rational response of both women and their doctors to finite energy and resources. For women with high cancer risk, though, engaging in preventive and screening behavior may stave off life-threatening cancers and improve future health. For Black women who seem to have less risk-related information and poorer access to specialists, the challenge of cancer prevention among those with other health problems may be even further compounded.

Other important patterns in our data were the relatively low rates of cancer, breast, and genetics specialist use among Black women (although we do not know whether they have ever been referred for such care) and the correspondingly greater reliance of Black women on PCPs for information regarding breast cancer risk and prevention. Prior research has documented that management of high-risk women by PCPs is generally poor, as these providers have rarely received specific training about familial predisposition for cancer, and therefore lack sufficient knowledge about genetic screening, counseling, and risk-management methods recommended for high-risk women. It has also been found that PCPs rarely refer patients to relevant specialists unless the patient initiates the conversation [5, 32]. Specialist care is the most likely source for women to obtain reliable information about the specifics of cancer risk and learn about appropriate prevention options for their own situation [33, 34]. Indeed, our data suggest that Black women may less frequently be aware of the existence of relevant prevention options. This is likely a result of patterns other than women’s preferences; prior research has found, for instance, that women of all racial-ethnic groups prefer thorough information about risk and benefits of screening procedures [35]. Our finding that a higher proportion of whites had undergone genetic testing makes sense given that Black patients are more likely to see only PCPs, less likely to be asked for their family medical history, and generally receive care at poorer quality facilities where referrals for testing are less common [36, 37]. The sample size and design of this study do not allow us to confirm whether the patterns of specialist use and information access we observed are present across the broader population of high-risk women. It is important that future research investigate this question, however, because if these racial differences are statistically significant then a systematic lack of timely access to specialists could be limiting Black women’s access to information and risk-management options, and thereby contributing to breast cancer disparities among high-risk women.

Financial constraints also affected Black women in our study more profoundly than white women. This is consistent with the positive association between income and BRCA testing among Black women with breast cancer [38]. The U.S. Affordable Care Act (which requires insurers to pay for genetic counseling and testing of women meeting certain risk criteria) may continue to mitigate financial constraints on genetic testing, but higher uninsured rates persist for non-white groups, and many insured individuals remain unaware that genetic testing may now be covered [39]. In this study, Black women generally had lower SES than white participants and reported more financial constraints on their health behavior, reflecting broader U.S. trends that are associated with poorer access to care, quality of care, quality of physician-patient communication, and fewer health-protective behaviors [40, 41]. One can easily envision a range of other mechanisms–such as the affordability of specialist care, or the challenge of managing multiple health problems under financial constraint–through which limited economic resources could produce racial differences in breast cancer prevention decisions [42, 43].

Limitations of this exploratory study include the small sample. However, the study design maximizes in-depth data that accurately reflects the phenomenological experience of women at elevated breast cancer risk, whose own stories and realities have often been omitted from research on risk management and cancer prevention. Our sample size was sufficiently large to achieve theoretical saturation with respect to all the emergent themes of the study, to capture previously unstudied dynamics of prevention decision making, and to enable important comparisons that can inform the design of future research and tailoring of clinical care to meet the needs of diverse women. The observational nature of the study and the convenience sample of women mainly from Ohio does not enable definitive claims about broader racial patterns or cause-and-effect relationships. These findings should be confirmed with larger and more representative samples; methods to quantify objective severity of risk should be used; and the experiences of other racial and ethnic groups should be explored. Larger samples would also enable further analysis of the heterogeneity of experience within groups of women who identify as Black.

Implications for research, practice, and policy

The study results offer an important roadmap of future research questions. Issues particularly deserving of attention include: (1) the ramifications of breast/ovarian cancer specific risk perception vs. general cancer risk perception on prevention behavior; (2) whether and how provision of risk and prevention information might motivate risk-reducing behavior without inducing avoidance behaviors and/or excess worry that might cause negative mental health; (3) methods for increasing the competence and confidence of PCPs both in providing specific information and/or resources about cancer risk and risk-management, and in referring appropriate patients to specialists; and (4) the impacts of financial constraints on women’s coping with breast cancer risk, and racial variations in the prevalence of such constraints.

This study also has important implications for the future of healthcare, suggesting clinical care and health system changes that could improve women’s ability to understand and cope with elevated breast cancer risk, and simultaneously ameliorate health disparities that render the management of elevated breast cancer risk particularly challenging for Black women. Methods should be developed to aid healthcare providers in exploring the psychosocial characteristics that shape their patients’ approaches to risk management: their prior experiences with cancer among loved ones, the degree to which they worry about cancer, and the role of faith and other social supports in how they cope with health issues. If confirmed through future research, these findings also point toward the need to make clinicians aware that many Black women have been exposed to less information and support related to breast cancer risk reduction options; such clinician education could facilitate specific efforts to reverse these trends. Conversations about cancer risk should acknowledge that this may be only one of several health challenges women are facing, and that plans for preventive action must take the demands of multiple comorbidities into account. The resulting insights may help clinicians understand how women perceive risk and respond to prevention options, leading to17 new routes for empowering preventive behavior among patients. As part of these conversations, decision aids may be used to help improve women’s understanding of their options and their ability to make choices consistent with their personal values and priorities [44].

At the level of the healthcare system, a variety of changes could be made to improve the access of Black women to risk-reduction information, options, and behavior. First, new continuing education programs and revisions to clinical guidelines could improve the ability and consistency of PCPs in collecting family history information, educating patients about cancer risk, and making appropriate specialist referrals. Both patients and clinicians should be made aware that health insurance generally covers genetic counseling and testing for women with sufficient family history. Changes in health insurance regulations to improve access to specialists could have significant impact on women’s understanding of their risk and empower them to take health-protective actions. The prevention of future cancers could render these changes cost-effective at the long-term system level. If future research confirms racial disparities in specialist access, genetic testing, and prevention information, particular effort should be made to rectify these disparities by bringing these innovations to clinicians and healthcare organizations that serve Black women.

Conclusion

To address important gaps in our knowledge of how women at high risk of breast cancer make difficult decisions about complex risk-management options, this study directly addressed the questions of racial difference in women’s decision-making dynamics, and the consequences of these differences. While both white and Black women contend with complicated personal, interpersonal, and structural landscapes as they navigate risk management, Black women seem to face some additional systematic disadvantages. Understanding that one is specifically at risk for breast cancer and being able to invest resources (time, energy, money) in coping with that risk are critical contexts for successful risk-management, and Black women often face barriers to both. Understanding the medical interventions that can prevent cancer or diagnose it earlier is a necessary precursor to using those options successfully; our data suggest that Black women may have less personalized information about their own genetic risk, less knowledge of about risk-management options, and less access to the specialists who usually explain them. In addition, our data suggest that Black women’s decisions may more often be constrained by financial and other limitations–which prevent risk-management behavior from aligning with women’s preferences and choices. These racial disparities will need to be studied further and addressed directly, if ongoing attempts to improve access to enhanced screening, preventive surgeries, and preventive medication are to be equally effective for all high-risk women.

Supporting information

Acknowledgments

The authors would like to acknowledge coding assistance from Melissa Angeli-Reyes, Kaela Lewis, Tiffany McCoy, and Theresa Tran, and editorial assistance from R. Kelly Garrett, Kelly Bragg, and Christina Bijou.