Abstract
Background:
Regular mammography accounts for half of the recent declines in breast cancer mortality. Mammography use declined significantly in 2008. Given the success of regular breast cancer screening, understanding why mammography use decreased is important. We undertook a focus group study to explore reasons women who were previously adherent with regular mammography no longer were screened.
Methods:
We conducted 20 focus groups with white non-Hispanic, black non-Hispanic, Hispanic, Japanese American, and American Indian/Alaska Native women, and segmented the groups by age, race/ethnicity, and health insurance status. A conceptual framework, based on existing research, informed the development of the focus group guide. Discussion topics included previous mammography experiences, perceptions of personal breast cancer risk, barriers to mammography, and risks and benefits associated with undergoing mammography. Atlas.ti was used to facilitate data analysis.
Results:
All focus groups (n=128 women) were completed in 2009 in five cities across the United States. Half of the groups were held with white non-Hispanic women and the remainder with other racial/ethnic groups. Major barriers to routine mammography included (1) concerns about test efficacy, (2) personal concerns about the procedure, (3) access to screening services, (4) psychosocial issues, and (5) cultural factors. For uninsured women, lack of health insurance was the primary barrier to mammography.
Conclusions:
Multilevel interventions at the health-care provider and system levels are needed to address barriers women experience to undergoing regular mammography screening. Ultimately, breast cancer screening with mammography is an individual behavior; therefore, individual behavioral change strategies will continue to be needed.
Introduction
Between 1987
Mammography is an effective tool for the early detection of breast cancer—the most commonly diagnosed cancer among women and the second leading cause of cancer-related death among women in the United States. 3 Routine use of mammography has been credited with reducing mortality from breast cancer through a combination of early detection and effective therapy following diagnosis. 4,5 At the time of the study, the U.S. Preventive Services Task Force (USPSTF) recommended routine mammography for women over 40 every 1–2 years. 6
Numerous studies have consistently demonstrated that factors such as confusion regarding the efficacy of mammography and screening guidelines, fear of receiving a cancer diagnosis, lack of social support, relatively low levels of income and education, and lack of insurance and access to readily available mammography screening services all decrease the likelihood that a woman will adhere to mammography screening guidelines. 7 –12 Distrust of the medical system is another barrier to mammography, particularly among black non-Hispanic women. 13 However, little is known about women who have previously adhered to mammography screening recommendations in the recent past but are no longer being screened. 14 The purpose of our exploratory study was to better understand why racially and ethnically diverse women who had participated in routine mammography screening in the past ceased getting screened at recommended intervals.
Methods
This study was conducted by researchers at the Centers for Disease Control and Prevention (CDC) and CDC Foundation with collaboration from ICF Macro. The ICF Macro institutional review board approved the study protocol. Each participant signed an informed consent form.
Given the exploratory nature of the study, focus group methodology was used. 15 From March to June 2009, we conducted 20 in-person focus groups with 128 women across the United States, segmented by race, ethnicity, and insurance status. Independent professional moderators facilitated all groups. One focus group with American Indian/Alaska Native participants had only two participants.
Literature review and expert interviews
A literature review and expert interviews were conducted to inform the study design including the development of research questions, racial/ethnic groups to recruit, information to collect, and identification of known barriers and facilitators to screening. We searched the Cochrane, Embase, ERIC, Medline, and PsycInfo databases for English language, peer-reviewed studies conducted in the United States and published from January 2000 to 2008 along with unpublished literature identified through general internet searches and CDC reports. Key words included breast cancer screening, guideline adherence, intervention research, focus group research, mammography, mammography utilization, mammography adherence, patient compliance, and mammography interventions.
Telephone interviews were conducted with 12 subject matter experts including health-care providers, researchers, and practitioners from three different U.S. regions (Northeast, Mid-Atlantic, and Midwest) with expertise across diverse racial/ethnic groups in breast cancer screening. These experts provided suggestions for our study design, including areas of questioning related to mammography adherence in racial and ethnic minority women and focus group recruitment strategies.
Based on the literature review and expert interviews, a behavioral determinant intervention (BDI) logic model was developed to represent potential causal pathways for mammography adherence (Fig. 1). 16 The pathways included mammography adherence (the health goal), a woman's individual behavior and other determinants that influence her decision to undergo mammography, and proposed intervention or activities to help women resume mammography screening. Together, the literature review, expert interviews, and BDI logic model informed our strategy for focus group segmentation as well as the questions included in the moderator's guide.

Behavioral determinant intervention logic model of mammography adherence.
Focus group participants
Participants included women ages 43–75 years, who had received two or more screening mammograms in the past 5 years but had not been screened within the past 18 months. We initially started with a screening interval of 2 years because this would exclude women who were adherent with the most generous time interval allowed. We did not anticipate difficulty in finding women who had not been screened in the past 2 years given findings in the literature that 20%–25% of women over 40 years had not been screened in the previous 2 years. 1,2 We began recruiting at age 43 because women would have had the opportunity to undergo two mammograms by that age. Women were excluded if they had received a mammogram before the age of 40 years; a mammogram requiring follow-up by a physician, which served as a proxy for a previous abnormal mammogram; or a previous diagnosis of breast cancer or any cancer other than basal or squamous cell carcinomas.
Focus group participants were segmented by age group (i.e., 43–49, 50–64, and 65–75 years), insurance status (insured or uninsured), and selected racial/ethnic groups: self-identified white non-Hispanic (WNH), black non-Hispanic (BNH), Hispanic, Japanese American (JA), and American Indian/Alaska Native (AI/AN) (Table 1). Focus groups were conducted in five U.S. cities: Atlanta, Georgia; Phoenix, Arizona; Pittsburgh, Pennsylvania; Los Angeles, California; and Seattle, Washington. All recruitment, with the exception of the AI/AN and JA groups, was conducted by a professional focus group vendor in each of the five cities. Given recruitment challenges for AI/AN and JA groups, community-based strategies were also used.
JA, Japanese American; WNH, white non-Hispanic; BNH, black non-Hispanic; AI/AN, American Indian/Alaska Native.
Recruitment screeners tailored to each racial/ethnic group were used to identify women who met the eligibility requirements. Participants received a $75 incentive for participating in the 2-hour focus group discussion. Additionally, participants were eligible for a $25 early bird raffle if they arrived 15 minutes before the start of the focus groups. All participants, with the exception of those recruited for the AI/AN focus groups, were rescreened prior to the start of the focus groups by staff with ICF Macro to confirm their eligibility; AI/AN groups were rescreened by an urban Indian health organization.
Data collection
Professional, racially and ethnically concordant female moderators conducted each focus group. The facilitator used a structured moderator's guide to explore the following topics: perceived benefits and consequences of mammography, factors affecting screening nonadherence, factors facilitating previous mammography adherence or as acting as barriers to routine screening, and factors that would encourage women to undergo routine screening once again.
With the exception of the AI/AN groups, all focus groups were conducted in professional facilities equipped with one-way mirrors, an observer viewing room, client waiting area, and audiotape equipment. The one-way mirrors allowed CDC Foundation, CDC, and ICF Macro staff to observe the discussions. The AI/AN groups were held at an urban Indian health organization facility to facilitate a higher attendance rate. Observers were present in the same room with participants. For all groups, ICF Macro and CDC staff members took notes and each group was audio-recorded and professionally transcribed.
All participants, with the exception of the AI/AN groups, completed a prediscussion information sheet to capture participant information. All focus groups were conducted in English with the exception of one JA group, which was conducted in Japanese and translated in real time by an interpreter who sat in the observer room.
Data analysis
Atlas.ti (Atlas.ti Scientific Software Development GmbH), a software program for qualitative data, was used to facilitate data analysis. ICF Macro developed a detailed codebook using both inductive and deductive techniques—individual codes were derived deductively from the research questions and moderator guide and inductively from the transcribed data. The final codebook was reviewed and approved by the CDC-ICF Macro project team. Staff from the urban Indian health organization provided input on the codes used for the AI/AN group. Four members of the CDC-ICF Macro project team were trained as coders. The coding team met regularly to discuss the coding process, ensure accurate code use, and make necessary modifications to the codebook. Once the group achieved 85% interrater reliability using a sample of transcripts, the 20 transcripts were divided among group members for coding.
When coding was complete, all of the study team met to discuss relevant themes and categories. The constant comparative method was used throughout the analysis to identify similarities and differences in themes across the groups. 17 Team members developed detailed summaries of each focus group segment.
Results
Based on our analysis, we identified five barriers to routine mammography screening among previously adherent women: concerns about test efficacy, personal concerns about the procedure, access to screening services, psychosocial issues, and cultural factors. Each of these findings is discussed in following sections along with our suggested strategies to encourage women to seek routine mammography once again. Table 2 provides additional quotes supporting each of the identified barriers.
Concerns about test efficacy
Participants frequently expressed concerns about the efficacy of mammography. Some women described real-life instances of false-positive or false-negative results they or others they knew had received. In the case of false-negative results, women believed that mammograms can create a delusive sense of security, contributing to skepticism about the test's utility. Several participants shared stories of friends or family members who had received a negative mammography screening result only to be followed by a breast cancer diagnosis a short time later. One woman said, “My mother-in-law, she actually had a mammogram done here in Atlanta and was told she was cancer free. And then [she] went to Indiana, and she was diagnosed with breast cancer and actually had a mastectomy.” (Atlanta, WNH, insured, 43–49 years old)
Many women in the groups also believed that compared with mammography, cancer was more frequently detected by the woman herself when, for instance, she found a lump in her breast. Knowing others who had detected their own breast cancer seemed to undermine women's trust in the accuracy of mammography. A participant reported, “A lot of people don't have faith in the mammogram. Everyone that I know who has had breast cancer—it was never detected in a mammogram. It was detected either through something that they felt, but never through the mammogram. So they're just not as thorough as they're being projected.” (Atlanta, BNH, insured, 50–64 years old)
Personal concerns about the procedure
A second barrier to mammography screening is concern about the procedure itself. Women in the groups recounted painful mammography procedures and otherwise negative experiences such as insensitive technicians that deterred regular screening. Some were embarrassed about the procedure and having their breasts touched by others. One woman said, “I thought those women were very mechanical, stick it here, put it here. They were like you were in and out, and they were herding you in there and throwing you in the machine, and I didn't think they were very sensitive. I thought they would be more so.” (Pittsburgh, WNH, insured, 50–64 years old)
In addition, many women expressed concerns about potential side effects from the procedure. Some, for example, women raised concern that radiation exposures from annual mammography might accumulate and lead to breast cancer. One woman said, “You take a chance on something happening to you from just the x-ray, something getting in your system that wasn't in there before. And maybe in six months or three months later, something shows up and you wonder where it came from because you didn't have it.” (Pittsburgh, BNH, uninsured, 50–64 years old)
Access to mammography
Women in all groups experienced system-level barriers to accessing mammography, most of which were primarily structural, including cost, inconvenient facility location; concern about being denied insurance in the future if diagnosed with breast cancer, and lack of both child care and transportation. Women without insurance more often stated cost as a barrier than those with coverage. The most common barriers cited by participants were long wait times to schedule appointments, undergo a mammogram, and receive test results. “What I can't stand is the time you [take to] have the mammogram, and then the time they wait to tell you. I think it should be sooner, like a week or so before – you've got to worry all that time.” (Seattle, AI/AN, insured, 50–64 years old)
Psychosocial issues
Another important barrier to adherence involved psychosocial issues. Women used the term, “manifest destiny,” in two groups (AI/AN and non-Hispanic women) representing the belief that breast cancer can develop from talking, thinking, and worrying about it. “I'd be afraid that it would be manifest destiny, if you're too concerned about it, then you're going to end up with the problem. No news sometimes, for me, is good news because I'm struggling with it right now because they tried to get me to go back again now.” (Seattle, AI/AN, insured 50–64 years old)
Other barriers included low personal risk, fear of being diagnosed with breast cancer, procrastination, and embarrassment about the procedure. For example, “Well, it's embarrassing, period. Because the first time, it's just like childbirth, you're thinking, oh my God, I have to do this in front of several people. And this baby is coming out of an end of me. You're exposing your breasts to somebody other than, maybe anybody, maybe you're not even married.” (Seattle, WNH, uninsured, 50–64 years old)
Some women reasoned that by living a “healthy lifestyle,” or lacking a family history of breast cancer, reduced their risk of breast cancer making breast cancer screening unnecessary. These women often believed that positive thinking, eating well, exercise, and knowing their bodies were enough to prevent breast cancer. They were unaware that risk of developing breast cancer increases with age. One woman shared, “This is probably going to seem totally ridiculous. But I, personally, feel that I know my body. And I make decisions accordingly. …I don't say ‘Every November I need to do this, or every year.’ But I just feel that I'm in tune with my body, and I can pretty well tell if there's something that's going on.” (Phoenix, WNH, insured, 65–75 years old)
Another barrier to screening that women expressed was their fear of being diagnosed with breast cancer. One participant said, “Fear. I really think fear. There's so many people in my community that have gotten breast cancer. And I know a lady, her mother had breast cancer, and her best friend had it. And she will not go get a mammogram. And I know she's just afraid that they might find something. She said, I would rather not know.” (Atlanta, WNH, insured, 43–49 years old)
Finally, some women simply did not include their own health among their priorities. “I think women in general, I think we always kind of put ourselves on the bottom of the list. Everything else comes first, and we forget about ourselves, taking care of ourselves.” (Atlanta, WNH, insured, 43–49 years old)
Cultural factors
Cultural factors were also important barriers to mammography. Hispanic women spoke about the intimate nature of the mammography procedure and how exposure of their breasts to a stranger was viewed as a cultural taboo. They also shared how their short stature made it difficult to undergo the procedure. AI/AN women attributed their race to the poor treatment they received from white technicians. For example, “I think they need training in respect for the Native people. I felt like these are white women coming in, and I'm not putting them down, it's just I didn't feel like I got any respect that I deserved.” (Seattle, AI/AN, insured, 50–64 years old)
JA women spoke about having a low risk of developing breast cancer due to their ethnicity. One woman shared, “Being Japanese, and being [there is] no family factor in my family, my risk is much less, so I am kind of at the point maybe I quit the mammogram forever. I am at kind of that point, maybe I do it like every 10 years or something.” (Los Angeles, JA, insured, 50–64 years old)
Discussion
As far as we know, this is the first qualitative study to examine barriers to mammography screening among previously adherent women across the United States since the decline in mammography noted in 2005. 1,2 Several recent survey-based studies have examined barriers to mammography adherence. In a study of state employees, Gierisch et al. 18 reported that more than 50% of women did not maintain annual screening adherence over a 3-year period. Identified barriers to adherence included being age 40–49 years old, reporting fair or poor health, having more than one reported barrier to mammography, and feeling less confident about obtaining future mammograms. In another study, O'Donnell et al. 19 found a correlation between mammography nonadherence and psychological distress among women recruited from physician offices in Los Angeles.
Regardless of race/ethnicity, geographic location, health insurance status, and previous utilization of mammography screening, women in our study continue to experience barriers to mammography adherence including access, concerns about test efficacy and the procedure itself, mammography access, and psychosocial issues and cultural factors. Some of our results support previously reported barriers to screening among women generally (e.g., access to screening, fear of radiation exposure, absence of family history of breast cancer, harsh treatment by technician). 7,9,20 –23 Other barriers that have been reported in the literature, such as distrust of the medical system among black non-Hispanic women 13 and confusion about screening guidelines among the general population 11,12 were not as salient in this study. It is possible that, for women in these focus groups, other barriers took precedence over these issues.
Revised breast cancer screening guidelines introduced in 2009 by the USPSTF have renewed the discourse among scientists, advocates, and others over the efficacy of mammography screening as well as potential harms of screening due to unneeded diagnostic work-up and over-treatment. 5,24 –31 Even though organizations disagree about the age to initiate mammography (Susan G. Komen for the Cure, American Cancer Society, American College of Radiology), all agree that the maximum benefit is realized from repeated mammography use and that mammography is the best method for the early detection of breast cancer. 32 –34 Breast cancer advocacy groups, public health professionals, and health-care practitioners should develop uniform messages about the benefits and risks of mammography so that women can make informed decisions regarding mammography. Because of the timing of our study, we were not able to examine the impact of these new recommendations.
Three insights can be gleaned from our study. First, we found that some women felt that a healthy lifestyle protected them from developing breast cancer and, therefore, they did not feel they needed to undergo routine screenings. One approach to help women make informed decisions about mammography is for health-care providers to personalize health information and highlight each woman's potential benefit gained from routine, repeated mammography screening. Positive patient and provider interactions have been shown to improve mammography adherence. 35 Barrett et al. 25 recommends that health-care providers use a less complicated probability method such as natural frequency to explain breast cancer risk with their patients. For example, health-care providers could explain the risk of dying of breast cancer by measuring risk based on mammography adherence versus lack of adherence. Additionally, clear, accurate, and consistent public health messages should educate women about breast cancer risk in general and their personal risk for breast cancer.
Second, contrary to previous research identifying fear of a breast cancer diagnosis as a barrier among BNH and AI/AN women, 36,37 we found that all groups of women reported fear as a reason they had not returned for their mammogram. In most groups, women also reported fear of a false-negative result. Confusion surrounding benefits and limitations of mammography, a finding of our study and others, 7,8,22 may also contribute to their fear. One solution would be to use patient navigators who could provide information, education, and peer support to women while navigating the complex health-care system. 38
Finally, women's concern about the efficacy of mammography screening suggests that public health practitioners and health-care providers must provide clear and simple information about the limitations of mammography screening. While mammography is currently the best early detection breast cancer screening tool available, 39,40 accounting for approximately 50% of the reduction in breast cancer mortality, 4 it also fails to detect up to 20% of breast cancers. 41 Promoting a screening test, while at the same time acknowledging its limitations, is difficult, but necessary.
The women in our study report experiencing a combination of barriers to mammography adherence. While the proposed improvements in patient–provider communication and education about the benefits and consequences of mammography are important, collaboration between public health professionals, health-care providers, and policy-makers is needed to minimize the structural barriers women face in undergoing screening during appropriate intervals. The Affordable Care Act, passed March 23, 2010, is one policy that should help to eliminate cost as a barrier 42 to mammography screening. While this is a step in the right direction, many important barriers that remain, such as convenient facility locations and improved wait time for the test and test results, need attention, as evidenced by our study.
This research identified challenges a sample of women report adhering to mammography screening; however, further research is needed to better understand if these identified challenges are shared more broadly. In addition, further research is needed to explore barriers rural women and other ethnic minority women face in adhering to mammography. Larger population-based studies with greater generalizability could help to further enhance our understanding of mammography adherence barriers and contribute to the development of effective mammography adherence interventions as found by Gierisch et al. 18
Limitations
Our study of previously adherent women sheds light on an overlooked population and illuminates the complexity of barriers faced by this group of women. Like all focus group studies, the results may not be generalized beyond the women studied. However, the nature of focus groups allowed for in-depth discussion about mammography adherence.
Conclusion
Although mammography use has improved slightly since we began our study in 2008, screening prevalence has not returned to levels reported before 2000. 43 Controversy surrounding breast cancer screening guidelines and efficacy of mammography remains. Public health practitioners and health-care providers are faced with the challenge of presenting the pros and cons to routine breast cancer screening with mammography in a balanced manner. Breast cancer risk increases with age, 44 and women need resources to make informed decisions about their health care.
Multilevel interventions aimed at reducing structural barriers and improving access to mammography, are needed to help women maintain routine screening behavior. Public health and breast cancer advocacy groups should include previously adherent women in their messaging to remind them of their individual risk factors, the purpose of undergoing routine screening, and prevent them from dying of breast cancer.
Footnotes
Acknowledgments
This study is supported by a grant to the CDC Foundation from Susan G. Komen for the Cure. We thank Susan G. Komen for the Cure for funding the study, CDC Foundation for providing technical assistance, Komen affiliates for contributing to the recruitment effort, and all the participants for sharing their experiences and thoughts. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
Author Disclosure Statement
The authors have no conflicts of interest to report.
