Introduction

In the USA, breast cancer is the leading cause of cancer-related incidence and the second leading cause of cancer-related death in women. Although population related incidence rates are lower for Black women compared to White women, mortality is approximately 40% higher for Black women [1]. Reasons for these disparities are complex and have been attributed to advanced stage at diagnosis, higher likelihood of being diagnosed with a more aggressive phenotype such as triple-negative breast disease and earlier age at diagnosis [1]. There are also systemic and individual barriers that may contribute to the disparity seen such as poor access to quality healthcare systems and breast cancer screening as well as factors associated with social determinants of health [2, 3].

It is well-known that early detection of breast cancer can be accomplished through routine screening mammography. Despite this, studies have shown the use of mammography screening is lower in uninsured women and those with lower socioeconomic status [4,5,6]. In addition, breast cancer screening perceptions and anxieties may contribute to lower uptake of screening in minority populations.

In March of 2020, the SARS virus that causes the disease COVID-19 devastated the world. In the USA, northeastern metropolitan cities were the first to experience this devastation first-hand. During this time, local and federal agencies advised that non-elective procedures such as mammography screenings be postponed or canceled due to inadequate resources such as PPE and staffing [7]. Furthermore, guidelines from the American College of Radiology (ACR) recommended the breast cancer screenings be discontinued temporarily [8]. This led to unprecedented drops in breast cancer screenings [9]. While screening recommendations have since resumed across the USA, there is concern that resumption of screening for minority women will not immediately recover and that socioeconomic disadvantages should be considered [10].

Research shows that regardless of race and ethnicity, the lack of insurance and living in poverty are major barriers to breast cancer screening utilization [11,12,13]. Camden, New Jersey, is one of the poorest cities in the nation, with 36.4% of residents living in poverty in 2019 [14]. The 2016 Camden needs assessment noted that Camden County had lower mammography screening rates and women were diagnosed at a later stage and with a higher mortality than women in surrounding areas [15]. Brooklyn, New York, has the highest mortality due to breast cancer of all five boroughs of New York City [16].

The purpose of this study was to evaluate current day challenges to breast cancer screening for Black women in two diverse northeast communities in the midst of the COVID-19 pandemic. We explored women’s thoughts, feelings, experiences, and opinions towards mammography screening in the COVID-19 era. While hesitancy to get mammograms for Black women existed prior to the COVID-19 pandemic, we hypothesize that additional anxieties and barriers now exist. Understanding which factors may contribute to barriers and lack of adherence to screening for Black women in the COVID-19 era will be important for developing future community interventions to reach Black women. Additionally, understanding best practices for getting the word out to minority populations about the importance of mammography screening will better position community outreach leaders in narrowing the breast cancer disparities gap.

Methods

This study used focus group methodology as the first phase of a mixed method study across two locations, Camden, New Jersey, and Brooklyn, New York. Focus groups were chosen to not only develop an understanding of women’s thoughts, feelings, experiences, and opinions related to breast cancer screening in the COVID-19 era but to allow the researchers to compare women’s experiences at the two research sites. Two focus group meetings were planned for each location and the final focus group included participants from both locations.

Sampling

This study used a convenience sample and additional snowball recruitment to identify participants. Eligible women 40 years of age and older (in accordance with the American College of Radiology and the American Society of Breast Surgeons recommendations that average risk women begin screening at the age of 40 [17, 18]) were recruited to participate in these focus groups. Women who were English speaking and who identified as African American/Black, Afro-Caribbean, or Afro-Latina were recruited. Focus group-specific ads were placed in local newspapers and advertisements were placed on social media platforms. Advertisements directed interested women to a QR code-linked Qualtrics survey to assess eligibility, demographics, and contact information [19]. Additionally, a contact number was provided for interested participants who did not have digital access. Research team members than followed up with a call to eligible participants to further assess eligibility, interest, and availability. To expand diversity and representation within the sample, research team members partnered with local churches and other neighborhood organizations and used snowball recruiting methods. Knowledge and ability to use the Zoom virtual platform was assessed and a tutorial was provided when needed [20]. Online informed consent was obtained from the participants prior to participation. The women received $25 gift cards for their participation.

Data Collection

The focus groups were conducted by a team of moderators whose role was to facilitate the discussion and encourage all members to participate. The discussion guide consisted of open-ended questions relating to breast cancer screening with a specific focus on the experiences and perceptions of Black women. As this study was conducted during the COVID-19 pandemic, questions on access to health care and health education programs during the pandemic were included. The focus group interviews began by asking if participants had ever had a mammogram and proceeded to discuss the women’s perceptions of breast cancer screening and the breast cancer experience. See Fig. 1 for the list of interview questions.

Fig. 1
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Focus group questions

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Five 60–90-min focus groups were conducted via the zoom virtual platform on December 2020 and January 2021 [20]. Online informed consent was obtained from the participants prior to participation, and participants completed a short demographic survey. The women received $25 gift cards for their participation. This study was reviewed and received institutional review board exemption.

Analysis

Demographic data were analyzed with Stata version 16. All interviews were audiotaped with permission and transcribed verbatim. The focus group transcripts were analyzed using a qualitative descriptive design. This design provides a less abstract, more closely held description of the data [21]. Considered the least theoretical method of qualitative research, the qualitative descriptive design provides a narrative in everyday terms of a participant’s experiences and perceptions. In this design, codes are not pre-conceived but are generated from the data [22]. The first step in the analysis of these transcripts was to identify important sections of text and attach labels to index these sections into coherent higher order codes [21]. BJD and ERR read the transcripts individually, identified codes, and then compared their choices and discussed their differences. After multiple reviews, the researchers agreed on a specific number of codes, which were then compiled into themes. While a number of relatively distinct themes were identified, they largely fit within a higher-level binary framework of decision-making on screening: I do get screened or I do not get screened. The COVID-19-related questions resulted in a theme which was consistent with the idea of getting the word out to the community about the need for breast cancer screening.

Results

Thirty-three women participated in this study; sixteen women were recruited at the New Jersey location and seventeen at the New York location. The average age was 58.4, with a range of 46 to 73 years of age. Twenty-eight of the women identified as African American or Black; four identified as Afro-Caribbean, and one woman identified as Afro-Latina. Twenty-five of the women were born in the USA; two were born in Jamaica, two in Guyana, and one each from Trinidad and St. Vincent, with two women declining to answer. The women who were born in other countries resided in the USA for an average of 38 years. At least 16 (45%) of women reported an income of less than US $49,000 which is below the poverty line. Two of the women reported being uninsured, eight women were Medicaid recipients, seven received Medicare, and two reported being insured via the military or Veterans Affairs. Fourteen women reported having private insurance, and the remainder declined to answer. Ninety percent of the women (n = 30) reported having ever had a mammogram and 65.6% (n = 21) reported having had a mammogram within the past 2 years. See Table 1 for demographics.

Table 1 Characteristics of participants (n = 33)
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Themes

The major themes noted could be defined by the binary: I get screened, or I do not get screened. Subthemes were categorized as patient related or system related. Caplan defined delays related to breast cancer diagnosis or treatment as patient-related (a delay in accessing medical care after a need is perceived or failure to keep appointments) and/or system-related (delays in getting an appointment, receiving diagnostic testing after an abnormal screening, or a delay in the initiation of treatment) [23]. In this study, we defined patient-related themes as those that influenced a participant’s decision-making about screening and system-related themes as a difficulty in a participant’s navigation or interaction with the health care system. The final theme was specifically related to communicating with Black women about the need for breast cancer screening and the pros and cons of virtual methods of communication. See Table 2 for the major themes, subthemes, and supporting quotes.

Table 2 Participant quotes related to the themes
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I Do Get Screened

Patient-related subthemes discussed by women who do adhere to mammogram guidelines included having “the knowledge to take care of myself,” “my spirituality gives me strength,” and “I get screened because I have a family history.” Most of the participants reported having had at least one mammogram and this was consistent with the large number of participants demonstrating an understanding of the need for breast cancer screening. Many expressed the knowledge that an early diagnosis can improve outcome. One of the participants described her feelings this way, “If I do what I can, and I cope… I know I have to do it. So I do it. And that's all I can do is try to prevent it and get tested early.”

Another participant expressed the understanding of the benefit of an early diagnosis, “because even you can have breast cancer and be treated and continue to live a happy and healthy life. So, because you are diagnosed with cancer, that doesn't mean that you're going to automatically die just like any other medical condition that you may have. Yeah, you can die from diabetes, you could die from a heart attack, but still you're going to treat the condition. So, whatever you're diagnosed with, you're going to treat … this you're unable to treat any longer.”

Spirituality was described as a source of strength to encourage women to get screened. As one woman stated, “it's a combination, both like God created medicine. You know, man-made medicine. So you have to take, you know, the treatment also, but also have faith that with that treatment, you're going to be healed in God's word. Amen.”

A number of participants discussed having a family history of breast cancer and that this made them more inclined to be screened. One participant stated, “I have, I have had several mammograms, I think basically started when I was in my either 40s or 50s. And I continue to have them on a yearly basis. And I think it's very important that we do this, especially if you have cancer run in your family on both sides of the family.”

Although many of the participants understood that an annual screening is recommended, there were frequent comments about the pain of the procedure. A few participants talked about breast size as a factor in determining how painful the procedure would be, “the, the old style one where they smash you down, and a lot of us don't really want to have to go through that. Because it is painful. And some of us don't have big breasts. I'm not a big breasted woman. So it's even more difficult for me. So those are the things I've definitely heard that the pain of it.” Another participant, while understanding that the procedure is painful, still encourages her friends to get screened, “I'm big breasted also. And you have to hug the machine and lift your breasts up on top of the machine and they tell you don't move, they squeeze it, squeeze it, you got to hold it in. It deters people, but I tried to encourage people to go you know, especially women of color, and the ones over 40.”

A system-related subtheme that was a positive influence on women getting screened was the ability to find access to compassionate care. One woman described a positive experience thusly, “They even have warm hands because some of them have cold hands. You know, so they warm their hands up. Thank goodness.”

I Do Not Get Screened

There were many patient-related subthemes that lead women to avoid screening. They included socioeconomic factors, fear, fatalism, medical mistrust, and mammogram skepticism. Some of the patient-related factors such as “I don’t have a family history, so I don’t need to be screened” reflect a lack of knowledge about the need for cancer screening.

Each of the focus groups had at least one participant who was skeptical of mammograms or who shared beliefs which were not consistent with fact. One participant expressed her concern that mammograms can be harmful to your health, “personally, I don’t want to do it every year, because I don’t think that the mammogram itself, I believe the mammogram itself is what you call is dangerous, personally, and and and it puts you at risk of getting breast cancer, which is crazy.” Several participants shared stories about relatives who refused to acknowledge that they were not feeling well or had symptoms of breast cancer, until it was too late. One participant told the story of her mother’s death, “I recently lost my mother. And she had a stroke. But when … I got her to the hospital. They told me it’s not the stroke. That was the issue. They said she had breast cancer. And she did not share that with the family. She kept it in secret. Oh my goodness. And we found out on a I guess on a Tuesday. She passed away on a Thursday. She kept it a secret. She didn’t tell any anybody. Yes, she didn’t want to say the word either… she had six siblings, except for one all were cancer patients. So it’s something that runs in our family. And now I’m fearful. I’ve canceled two appointments already. But, you know, my mother was looking at her sibling because her sibling also was a person who did not get mammograms and she got breast cancer, and she said to her, I’m going to, I’m going to die. So my mom took the same type of attitude. She just she kept this secret. You know, it wasn’t anything that we could do. There was no time left to fix it. But it was all because of fear. Her parents, they also had cancer. So she was in fear. To go to the doctor and to get checked and that’s why she kept it a secret because she knew that we would try to intervene and take her to a doctor. And now we can’t fix it.” Even after describing this experience the participant explained that she herself had not been screened; had canceled two appointments. She acknowledged the need for a mammogram and also expressed the fear of being given a cancer diagnosis.

Some of the fears described by participants as reasons to not get screened included fear of being diagnosed, fear of dying, and fear of having to tell your family that you have cancer. Indeed, family was cited as both a reason to get screened (“it runs in my family, “my family depends on me”) and a reason not to get screened (“No one in my family has had breast cancer, so I don’t need to get screened, I don’t want to burden my family because of my health, or I’m too busy taking care of my family to take care of myself”).

A few participants were convinced that breast cancer was a death sentence. Comparing breast cancer screening to taking a COVID-19 test one participant explained, “that again, it all boils down to a lot of people don’t want to look into COVID test, because there’s no cure for it? Well, you know, you got it, you know, you’re gonna die. Like who wants to know, they’re going to die in X amount of time. That’s the bottom line. Knowing in just a matter of time that you have something, there’s no cure for, and it’s a matter of time. So why would you want to do that?”

Some participants mentioned the fact that in their social groups they only discuss negative aspects of mammography, such as the pain of the procedure, and not the positive factors, such as early diagnosis, that would empower more women to get screened and adhere to a regular screening schedule. A small number of participants expressed the belief that if you do not have symptoms you do not need to be screened. One participant explained, “but I also know some of them just don’t have the reason to go see you know what’s going on because there’s no pain, no discharge, no lumps, no discoloration, no reason.”

Distrust of physicians and being treated by biased or inconsiderate providers or technicians was a complaint expressed by a small number of participants. One participant expressed her distrust this way, “And after they and I thought they were finished, they came back and kept taking pictures. And then they were taking pictures again, it was like, Hey, this is a human being, you know, what are you seeing that’s different that you didn’t see the first time. And that was a real turnoff for me. And I have not gone back to that place since then. And, you know, and and so, um, you know, I think in a sense, some people want you to, to leave the office with breast cancer. That’s kind of you know, and yeah, I think to some extent, some, some of the medical professionals, they believe that they I that they, you know, they can give everybody a diagnosis.” Another participant explained, “You know, but I think that people get what they expect. I think you get whatever you settle for.”

Getting the Word Out

While many of the focus group participants appeared to be knowledgeable about the need for breast cancer screening, they did have concerns about members of the community who may choose not to get screened. One participant expressed her concerns this way, “And … for me the piece is also that women not feel that they have been that they are responsible for their own lack of or, or, you know that they are made to feel as if they are the criminals, right. And just as has been discovered with COVID, which we all knew everyone that’s Black and knew this, they’re just discovering it with COVID, that Blacks are dying twice as much twice the rates of white, we always knew that Black people in terms of their health, (are) behind the eight ball.”

Participants talked about the need to empower Black women and educate them about breast cancer, but they were realistic in assessing that for Black women their own health is often not a priority. One participant stated, “So there is a system that has existed that has created circumstances around women’s health. So what we have to do is all of these pieces that we are naming, whether you agree with the heart of it or not all of them, it’s going to take all the pieces to help women be empowered to see themselves as priority and their health as priority.”

A number of participants talked about using church as a means to reach out to women in the community, while acknowledging the fact that now many churches are not meeting in person and so any educational program would have to be provided via the internet. The participants were asked if they thought that virtual educational programs would be effective, but some brought up the fact that many women in their communities, likely the women most in need of education and encouragement, do not have access to the internet or may only be able to use their telephones to participate in educational programs. One participant explained, “A lot of the individuals that I work with in my community, they pretty much don’t have that technology to do online …to listen and listen, a lot of them may be able to listen during phone calls, but not far as, you know, online.”

While one or two participants explained that they do discuss their health with their friends or relatives, a larger number expressed the concern that women were not sharing their experiences with breast cancer. One participant compared breast cancer with COVID-19 by saying, “understand that there’s a whole segment of women that just like the COVID wasn’t real for people, this is just not real to them. They don’t know anybody who’s had cancer, breast cancer, they don’t know anybody that had a mammogram, they don’t know anybody. And if you know us as a people, and we don’t know somebody that went through something, and we’re not touching it, like we don’t know, somebody that will take this vaccine, we’re not taking it. And you and they keep pushing it out there with all the people saying, Go take it, go take it, but you know, if we don’t know…we’re not gonna go take it.” Another participant stated, “but those are the detriments to women having mammograms and fear because there’s no there’s no information about it. And it’s not something that in our community we talk about. Conversation is going to be one of the most difficult because they don’t know anybody. So it’s not real to them. It’s like, stuff being on TV. It’s not real.”

The primary system-related subtheme discouraging mammography was experiences with biased or inconsiderate staff at screening sites. One woman expressed her negative experience this way, “And the fact that when women No, I think when Black women go to the doctor they’re not given the kind of attention that our white counterparts see.”

There were few differences noted in the transcripts based on a participant’s area of residence. Two of the participants did complain of an inability to find acceptable care near their homes in New York, whereas this did not appear to be a concern in the New Jersey participants. No other observations or concerns were expressed that would differentiate a participant based on her residence.

Discussion

The aim of this study was to better understand the factors that influence breast cancer screening among Black women in two locations: Camden, NJ, a low income primarily African American/Black and Latinx city in southern New Jersey, and Brooklyn, NY, a demographically heterogeneous borough of New York City. The initial goal of this study was to recruit low-income women who were uninsured or Medicaid recipients for the focus groups; however, due to the COVID-19 lockdown, difficulties in recruiting this essentially hard to reach population were found. The resultant focus groups were a combination of low income, uninsured women, and Medicaid recipients and women with higher socioeconomic status. Fourteen of the thirty-three women reported having private insurance, either through their employment or purchased on the Affordable Care Act Marketplace, and more than half of the women reported being college graduates. While women did discuss inability to access screening services related to lack of insurance or financial insecurity, the women with insurance in this sample did not describe being insured as a facilitating factor for mammography. No differences were noted by location in the themes identified through the focus group discussions; however, one participant in the Brooklyn sample did discuss her perception of inconsiderate care received from health care workers in Brooklyn. This participant would rather go outside of Brooklyn to receive services due to the disrespect she reported.

Just over 90% of the women reported having ever had a mammogram, while a much lower 65.6% of the women stated that they had received a mammogram within the last 2 years. This rate is lower than the 84.5% reported by the 2018 Behavioral Risk Factor Surveillance System (BRFSS) Data [24]. While socioeconomic status did not appear to reflect a difference in mammogram utilization in this study, in general, socioeconomic, structural, and cultural factors have been found to be barriers towards mammogram utilization in Black women [25] and any effort to increase screening utilization should be cognizant of these barriers. Additionally, the impact of COVID-19 on access cannot be understated.

The primary facilitators encouraging screening in this population included understanding the importance of screening, positive family history, spirituality, and having faith in the tools God has given them (medicine). Brandzel and colleagues found that Latinas and Black women who had faith in the benefits of the screening were more likely to get screened [2]. In this study, several women who reported having mammograms discussed the importance of early detection and understanding that outcomes improve when breast cancer is diagnosed early. As well, some noted the importance of empowering Black women about breast cancer through education.

Conversely, confusion about screening intervals and not having a clear understanding of the benefits serves as deterrents to screening [24, 25]. In this study, several participants expressed the understanding that if they had no signs or symptoms of breast cancer, then they did not need to be screened. Orji and colleagues, in an integrative review of 23 studies consisting almost entirely of African American/Black women, found that the lack of a perceived need for mammography, based on the belief that their breasts were healthy, was a major disincentive for women to undergo mammography [25].

Both family history and religiosity led to follow-through on mammography screening in our focus group members. Some group members discussed seeing family members diagnosed with cancer leading them to get screened while others pointed out that faith gave them strength to move on with their screening and trust man-made treatments. Similarly, the literature notes that a family history can positively influence mammography screening, especially when there is strong belief [25,26,27,28] and that women who attend religious services are more likely to have had a mammogram or other screenings [29]. Although our group did not equate faith with screening evasion, other studies have shown that having religious beliefs and faith in God can be a barrier to screening [30].

Despite the factors that can encourage women to perceive the need for screening, barriers were more frequently noted, and these were primarily patient related and included fears, fatalistic thoughts, and distrust. Fear included fear of dying, fear of the diagnosis, and fear of sharing the news with family. There were also fatalistic thoughts and negative social talk regarding mammography. These types of barriers have been previously identified in the literature and are often related to social determinants of care [3].

Some studies of Black women specifically have found additional barriers. Jones et al.’s review of the literature noted that fear of an abnormal finding and cancer treatments led to delays in care among Black women [31]. As well, for Black women, fear of the results/diagnosis led to decreased interest in obtaining mammography [28, 32]. Furthermore, Passmore et al. found that for uninsured Black women, family responsibilities led to secrecy and prevented them from sharing their diagnosis with family [28]. These fears are widely acknowledged in the literature and by the focus group participants as common reasons for avoiding screenings.

Fatalism continues to be a barrier to care among Black women [28, 33, 34]. The belief that mammography and positive findings are equated to death may prevent a number of Black women from being screened [30, 35]. A few focus group members stated that breast cancer was incurable and a death sentence.

Pain was a concern for both the focus group participants who do or do not get screened. The pain could have been personally experienced during a previous mammography screening or shared by other persons around them. Though the “I do get screened” group dealt with it and still followed through with screening, the “I do not get screened” group saw it as a reason to avoid screening. Several previous studies have pointed out that pain is a barrier for screening among Black women and a reason to avoid mammography [36,37,38]. The conversations about negative experiences of mammography among Black women may be especially influential upon other women’s avoidance of screening, especially in those who are mammography-naive [34, 36, 37]. Developing future messaging related to this barrier to care may be helpful in educating Black women while debunking some of the widely held myths that lead to avoidance of screening.

Distrust of mammography and distrust of the healthcare team and system were of concern and may be related to the barriers identified as system related, specifically the contact with biased and disrespectful healthcare providers. Prather and colleagues found that discriminatory healthcare practices negatively influence the quality and types of healthcare provided to Black women [39]. Distrust of the health care system as well as concerns regarding discrimination has been found to be a barrier to screening [26, 40]. Discrimination is especially perceived by Black women compared to other ethnic groups, leading to increased screening barriers [41]. A few of the focus group participants voiced concerns about distrust and biases related to the physicians or technicians who cared for them. Kim et al. noted that Black women, women who do not have trust in the healthcare system, and those who live in poverty less often report or acknowledge barriers to mammography screening; thus, they may be less likely to receive support such as navigation [42]. This is quite important as several studies have shown that patient navigation is critical to increasing screening rates in minority communities [43,44,45,46]. As we continue to assess barriers to care for Black women, it is just as important to educate them about resources, such as navigation services, regardless of whether or not they have requested these services. Additionally, building systems that are trust-worthy is a critical first step in addressing this system-based barrier.

Finally, the COVID-19 pandemic has presented many unforeseen challenges. Using data from the Breast Cancer Surveillance Consortium, Sprague et al. looked at trends utilizing screening and diagnostic mammography during the COVID-19 pandemic and noted racial/ethnic differences in rebound mammography use [47]. Implementing community sensitive strategies to get the word out about the importance of breast screening in such circumstances would be important. The COVID-19 pandemic magnified the existence of the digital divide; not all technological advances are equally accessible to minority communities. Developing outreach that incorporates telephone engagement as well as advocating for access to broad band service and advanced technology will be an important first step in getting the word out.

Strengths and Limitations

As in all qualitative research, limitations in generalizability must be accepted. While the focus groups were united in their self-identification as Black, not all of these women reported low incomes, low education levels, or a lack of insurance. Given the fact that the researchers were recruiting and conducting this study during the COVID-19 pandemic, it is likely that the reliance on online communication had a negative impact on the broader representation of the two communities in the focus groups, thus requiring the researchers to include women who did not report low incomes or the lack of insurance. Despite this, the barriers discussed in the focus groups were similar to those found in studies of low-income and uninsured Black women. The strengths of this study, however, outweigh the limitations by explicating the lived experience of Black women residing in two urban communities in the Northeast. The focus group discussions from the two different sites resulted in similar findings, which lend credence to the assumption that the participants of this study were able to give voice to the barriers that prevent Black women from accessing preventive care and cancer screening.

Conclusion

Despite numerous studies on why Black women hesitate to obtain screening mammography, there are still research gaps surrounding this issue. One study suggested the importance of specifically focusing future research on women who are not getting screened in order to better understand this question [48], but this group is hard to reach and perhaps less likely to have access to research. Our findings on factors that affect breast cancer screening decisions point to both barriers and facilitators that are not solely related to poverty and insurance. Community outreach efforts should concentrate on building trust, providing equitable digital access, and skillfully addressing breast health perceptions while incorporating strategies to address fear and fatalism.