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The Impact of Delays in Low-Income Women’s Breast Cancer Experiences

Jerome-D’Emilia, Bonnie PhD, MPH, CBCN, RN; Suplee, Patricia D. PhD, RNC-OB; Robles-Rodriguez, Evelyn DNP, APN, AOCN; D’Emilia, Wyatt MA

Author Information
doi: 10.1097/NCC.0000000000000878
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Abstract

The breast cancer mortality rate has declined in recent years because of improved treatment and increased screening adherence; however, certain subsets of women continue to be diagnosed at later stages with worse prognoses.1,2 Low-income, underinsured and uninsured women are less likely to be diagnosed via a screening mammogram and so are more often diagnosed at later stages with a resultant negative impact on breast cancer survival,3 even when free or low-cost screening and diagnostic services are relatively accessible.4

The National Breast and Cervical Cancer Early Detection Program (NBCCEDP) was established in 1990 to improve access to cancer screening services for low-income (income at or below 250% of the federal poverty level), underinsured and uninsured women in the United States.5 The NBCCEDP provides screening services in all 50 states, the District of Columbia, 6 US territories, and in concert with 13 Native American tribes or tribal organizations across the United States.5 The New Jersey Cancer Education and Early Detection Program (NJCEED) is the New Jersey state arm of the program. From 2007 to 2016, NJCEED funded 22 clinical sites, provided 132 765 mammograms, and diagnosed 1073 cases of breast cancer.6

A recent evaluation of the NJCEED program (cases from 2004 to 2014) found that women diagnosed with breast cancer through the program (enrollees) were significantly more likely to be diagnosed at a late stage (stage III or IV) when compared with nonenrollees.7 In a study by Wu and colleagues8 of the national program, a similar result was found, as was the case in state evaluations in Idaho, Florida, and California.8–11

There is no codified medical definition of the ideal time from diagnosis to treatment,12 but studies have varying outcomes due to length of time from diagnosis to surgery, or from the first notice of a possible symptom to treatment.12–14 Bleicher and colleagues14 found that delays from diagnosis to surgery (initiation of definitive treatment) of longer than 60 days had a negative impact on disease-specific survival. Stuver and colleagues15 examined time to diagnosis, from the first acknowledgement of a symptom to receipt of definitive diagnosis. Those researchers found that an interval of more than 90 days to surgery (as the first definitive treatment) could negatively impact disease-specific survival. When delays are greater than 90 days, which occurs in less than 2% of patients in the United States, overall survival has been found to decline by 3.1% to 4.6%.12

Delays related to breast cancer diagnosis or treatment have been defined as patient-related (defined as a delay in accessing medical care after self-discovering a symptom or failure to keep appointments) and/or system-related (a delay in getting an appointment, receiving diagnostic testing after an abnormal screening, receiving a definitive diagnosis, or a delay in the initiation of treatment).13 Efforts to improve cancer screening program effectiveness, by necessity, would have to specify the types of delays that are most commonly found in that patient population.

While quantitative studies of secondary data may be able to identify delays in diagnosis and/or from diagnosis to treatment, these studies cannot identify the specific factors that resulted in these delays or determine if the delays were patient- or system-related. Factors related to socioeconomics may play a role in both patient- and system-related delays.12,16,17 Indeed, a recent large-scale study found that almost half of observed racial/ethnic disparities in stage at diagnosis were mediated by insurance status.18 However, when free or low-cost services are accessible, it is reasonable to question the influence of other factors as well. To fully understand the factors that resulted in delays in diagnosis and treatment for women who are enrolled in the NJCEED program, qualitative research is warranted. Sandelowski19 described qualitative-descriptive research as a method in which researchers stay close to the data and the surface of events, to provide a truthful version of experiences and the meanings participants give to those experiences. Although much has been written about women’s experiences following a breast cancer diagnosis, few studies have focused on such a hard-to-reach and often marginalized population, women diagnosed through a state program that focuses on the low-income and uninsured. The purpose of this study was to determine if there were delays in diagnosis and treatment of women enrolled in the NJCEED program and, if so, what the causes were of delays in program enrollees.

Methods

Women who experience social and economic vulnerabilities can be considered marginalized20 and are often not included in qualitative research. A literature search did not yield any qualitative studies that included women enrolled in the NBCCEDP. This is regrettable as those women likely have unique stories to tell. To allow these women’s voices to be heard, a qualitative descriptive design was utilized. This design provides for a less abstract, more closely held description of the data.19 Or as Lambert and Lambert21 explain, the qualitative descriptive design, considered by some to be the least theoretical method of qualitative research, allows for a comprehensive narrative in everyday terms of specific events as they have been experienced and perceived. We sought to identify participants who would provide rich, compelling narratives that would explicate the factors influencing care in this population and saturate the data.21

Sampling

To optimize our ability to recruit this hard-to-reach population, the researchers partnered with an NJCEED office in a low-income urban community in New Jersey. Following institutional review board approval, this program office provided the researchers with a list of all the women (n = 75) diagnosed with invasive breast cancer from 2010 through 2017. Using an opt-out mechanism, the researchers sent a letter describing the study to all of the women on the list who fit the eligibility criteria (age >18 years, English or Spanish speaking, diagnosed with invasive breast cancer through the NJCEED program in the years specified). While opt-out methods of recruitment are not widely used, studies that have examined recruitment in diverse and minority populations suggest that opt-out techniques significantly improve recruitment when compared with opt-in techniques.22,23 The letter, which included a stamped postcard addressed to the NJCEED program office, explained that if the woman did not want to receive further contact from the researchers she could return the postcard or call or email the program director to be removed from the list. The letter informed the women that if they were interested in participating in the study, they were to call or email the principal investigator (PI) or the director of the NJCEED program office, or they could wait to receive a call from the PI. Two women chose to opt out by returning the postcard, and 4 letters were returned to the PI for incorrect addresses. The researchers attempted to contact the remaining 69 women by telephone. A small number were excluded as they spoke a language other than English or Spanish. There were at least 40 or more for whom the phone number was no longer correct, or no one answered in multiple attempts; a small number were deceased; and 1 woman scheduled an interview but never showed up. Those who spoke to the PI but refused to participate did not provide reasons for declining the study. Twenty women who were willing to be interviewed were identified.

Data Collection

A semistructured interview guide was created for the identification and elaboration of information not previously anticipated by the researchers. An interview allows researchers to gain an understanding of how participants think and feel about a subject24 and provides an opportunity for participants to voice concerns and provide answers to questions that may be unanswerable through quantitative research.

B.J.-D. and P.D.S. interviewed 18 women either individually or together, and E.R.-R. assisted B.J.-D. in the remaining 2 interviews that were conducted in Spanish and then translated by E.R.-R. into English. All but one of the participants were interviewed face-to-face either in their home or the NJCEED office. The women completed an informed consent and a 12-item demographic questionnaire prior to the interview. Interviews lasted from 30 to 60 minutes. The one woman who was now residing some distance away was interviewed via telephone. She was mailed and returned the informed consent and the demographic questionnaire to the PI prior to the interview. Participants received a $50 gift card following their interview.

Interviews began with a broad open-ended question “Tell me (us) about your breast cancer journey,” to allow participants to freely describe their experiences and to provide the researchers with an overview prior to probing by the researcher for more information or clarity. Additional questions focused on diagnosis and treatment choices, probing for information related to decision making, and whether the participant felt comfortable with and/or wanted to actively participate in shared decision-making about treatment choices. See the Figure for the list of primary interview questions.

Figure
Figure:
Interview guide.

Analysis

Demographic data were analyzed with Stata version 14 (StataCorp. 2015. Stata Statistical Software: Release 14. College Station, TX: StataCorp LP). All interviews were audiotaped with permission and transcribed verbatim. Qualitative content analysis was used to analyze the data. In that method, codes are not preconceived; rather, they are generated from the data, as the study progresses.19 Miles et al25 describe coding as a method of discovery. They suggest that the researcher determines the code for a chunk of data by careful reading and reflection, and this provides for intimate familiarity with the data.25 P.D.S. and B.J.-D. debriefed after each interview when applicable, listened to the audio recordings, and read the transcripts individually in an initial process of coding the data. Each researcher identified codes individually and then compared their choices and discussed their differences. After multiple reviews of the transcripts, the researchers agreed to a specific number of codes. Although all 4 authors were involved in the data collection, transcription, and manuscript preparation, the coding was the job of the 2 researchers with experience in qualitative methodology. Once these researchers reached agreement on the coding, these codes were compiled into a secondary level of analysis resulting in themes. While this method of qualitative analysis suggested a number of relatively distinct themes with which to understand the women’s breast cancer experience, this study focused on 3 themes that were most relevant to the objective of this study—the consideration of delays in diagnosis and treatment.

Results

Twenty women participated in this study; the average age was 56.6 years, with a range of 29 to 70 years. Seven of the 20 were African American, 5 were Latina (including one who identified as Mestiza), one was Asian, and the remaining 9 identified as White. Eighteen of the 20 women were uninsured at diagnosis; 2 were considered underinsured and had previously consulted physicians outside of the NJCEED program but did not receive a definitive diagnosis until enrolling in the NJCEED program. Nineteen of the women were provided with Medicaid through NJCEED, which is the standard procedure for eligible women when diagnosed with cancer through this federal program (see Table 1 for demographics). One of the women was not a citizen and so not eligible for Medicaid; her treatment was paid for by charity care. Ten of the women reported major comorbid conditions, and one of the women had recurrent breast cancer (Table 2).

Table 1 - Characteristics of Participants (n = 20)
Variable n %
Age, y
 <40 1 5
 40–50 1 5
 51–60 10 50
 61–70 8 40
Age at diagnosis, y
 <40 1 5
 40–50 6 30
 51–60 11 55
 61–70 2 10
Race
 White 9 45
 African American 7 35
 Asian 1 5
 Other 3a 15
Latina
 Yes 5 25
 No 15 75
Marital status
 Single 6 30
 Married 7 35
 Widowed 2 10
Separated/divorced 4 20
Domestic partner 1 5
No. of children
 0 1 5
 1–3 14 70
 >3 5 25
Education
 Less than high school 3 15
 High school graduate 6 30
 Some college 9 45
 College graduate 2 10
Employed outside the home
 Yes 7 35
 No 13 65
Insurance status
 Private 1 5
 Medicaid 11 55
 Medicare 6 30
 Uninsured 2 10
Income
  >$10 000 2 10
 $10 000–24 999 8 40
 $25 000–49 000 7 35
 $50 000–74 999 2 10
 $75 000–99 999 1 5
aMestiza.

Table 2 - Participant-Identified Comorbidities
Participant No. Comorbidities
1 Diabetes
Hypertension
2 Obesity
Diabetes
Hypertension
3 Diabetes
4 Hypertension
6 Asthma
7 Diabetes
9 Ovarian cancer—stage IV
13 Alcoholism
Brain aneurysm
17 Colitis
Hypertension
Arterial disease
18 Rheumatoid arthritis
Colon cancer

Thirteen (65%) of the women explained that they found a lump or noticed an unusual feeling in their breast, and that led them to access services. The women described their symptoms in various ways such as “swelling and fullness, a little bit of firmness” (participant 14), “my right breast was deformed, I had a lump like it was kind of dented in” (participant 20), and “I had a mass, and I would touch it, and it felt like an electric shock” (participant 19). One woman had abnormalities found by a physician on clinical breast examination, and the remaining 6 women reported that their cancer was diagnosed via mammogram (although only 3 specified that they were having regular mammograms).

Of the 20 women, 45% were diagnosed at later stages, 6 reported being told they had stage III cancer at diagnosis, and 3 reported that they had stage IV disease. Three women reported being told they were BRCA positive; this included 2 of the women who had stage IV disease and 1 woman who was 21 years of age at diagnosis (although NJCEED breast cancer services are routinely provided to women aged ≥40 years, younger women can be diagnosed and receive treatment at the discretion of the program director). Six of the women received bilateral mastectomies, including the woman who had recurrent breast cancer 15 years after a lumpectomy. Two additional women requested bilateral mastectomies but were advised to wait to remove the unaffected breast; both went on to remove the unaffected breast in a subsequent surgery. Two additional women expressed regret that they had not chosen to remove both breasts. The remaining women were treated with lumpectomy or mastectomy based on their tumor size and location.

Themes

Poor Access to Healthcare: “I Cannot Go to the Doctor”

Eighteen (90%) of the women interviewed appeared to have experienced a delay, either from screening to diagnosis, from diagnosis to treatment, or due to a lack of regular screening, all of which could have impacted their prognoses. Being uninsured was mentioned by 18 (90%) of the women during their interviews as a critical factor in these delays, although other factors such as fear, not wanting to have to pay for care, or being too busy with family responsibilities were also mentioned. The women reported going to a doctor only when very sick (Table 3).

Table 3 - Participant Quotes Related to the Themes
Theme: Poor Access to Healthcare: “I Cannot Go to the Doctor”
Participant 16: “Only unless it was like dying with bronchitis was the only time and then I had to foot the bill for those times myself.”
Participant 20: “Just if I got sick. I had a primary just if I got sick. I had a primary, and I had to pay cash for the visits.” When asked why she had not gone for mammograms: “No, it wasn’t fear. It was just that I never had insurance. And I was like how my going to do that if I do not have the money to pay for it, how my going to get it done? I thought about what if something goes wrong and I have no insurance? Like how is this going to work? You know, we do not have insurance, and how are we going to pay these bills?”
Participant 8: “…um she say you have to do physical. I said oh Lord, I do not have any insurance. I do not even have a job.”
Participant 9: “I got Medicaid after I went through $100 000. I went through all my retirement and everything. And then right after I had my hysterectomy, I had no more money” (this women was diagnosed with stage IV ovarian cancer in addition to stage IV breast cancer).
Participant 1: “My job got closed down completely and my health insurance ran out. So I was like, what is this place? She told me about the place where she was going to get free medical examinations and so forth. And I winded up going there. And she (the nurse) said never ignore it. But at that time, a couple months went by after that. I kept getting this UPS mail, I mean certified mail. I was like, who keeps sending me the certified mail because I did see something from _____ hospital, but it was really saying that you know this is your problem. You’ve got cancer. So I did pick up the certified mail. It was from _____ hospital saying they need to see me. It’s been months in between. Yeah they give me 3 attempts. So imagine when the post office gives you 3 attempts, so it might have been 2 or 3 (months) in between, yeah, for you to pick up this letter.”
Participant 3: “October to December for diagnosis. Chemo started in January. I think I had a mammogram when I was 45 or 46; it was like my first one so I actually had insurance. And then that’s the only reason they brought me back because it was like a 2- to 3-year gap when they looked at the first one to the second one, and they could see just enough growth in it to warrant bringing me in. If I had not had that one, and they had only seen the one spot; they probably would’ve never brought me in the first place. They would’ve just said, ‘oh, we’ll watch it’; it’s a wait-and-see, see what happens next year when you get your mammogram. At that point, it could’ve been too late.”
Participant 4: “So anyway I, I noticed it was a lump underneath there. It was like a boil. The boil went away. So about maybe in August, uh-uh, maybe in November, I felt this little tiny, just little tiny, wasn’t no boil ‘cause the boil had busted. It wasn’t big as my fingernail. So I put my husband’s hand on it. I was like, ‘A., you ever felt that?’ He said no. So now I’m getting worried. Something tells me to go to doctors, but I’m scared. I do not know what they are gonna tell me. So that December, I called my girlfriend. She work for the, uh, cancer screening unit. So anyway I called her and I, and I, so she said, “Well V. you need to go see about it…. I just, I blocked the cancer out. I thought about it. I’m not gonna lie. But I just did not even want to go for them to tell me that. So I went when I knew that it wasn’t going away.”
Participant 17: So it was Friday night into Saturday night; I was lying in bed, and I was kind of rubbing myself because I was sore, and that’s when I found a lump. And then the next day, I had a girlfriend; I said, ‘feel this.’ I did not even know that our breasts are just cells, and I thought it was a muscle I pulled in here. I did not know, and she knew somebody; she felt it, she knew somebody who had breast cancer, and she said you better get that checked ASAP. So the following Tuesday, that quick, I went to—medicine on 45, had the mammogram, and then it all started. Everything, all broke loose. So it was almost stage III, I think 2.9. Yes, that was my first mammogram (she was 54). And they told me at the center that, by the size of it in the centimeters and all, I probably had had it 2½ years.
Participant 20: “To be honest with you, I did notice it for a while. But at the time my daughter and my granddaughter were going to be 16. So we had sweet 16’s plan for them. You know the whole, so my daughter’s was in September and my granddaughter’s was in December. So I was like I had to get through this because I could not, I knew if I went and got checked, I knew it was going to be an issue. So I figured let me just keep fighting it, and I just will not say anything. No one knew because I kept it very quiet, from my husband, everyone. I did not say a word. And I got through September and December, and then finally February, I had another event to go to, and I was like, you know what, this is it, I’m not going to go any farther. And then March, it was March when I finally called.”
Underinsured:
Participant 9: “I kind of expected it. I had been feeling crappy for years, and I have been going to the doctor, and it is the same 3 things. Pre, post, whatever stage of menopause and overweight… This went on for almost 10 years with me and that doctor. So finally when I looked at the tape and did this, and they told me it was ovarian cancer, and I said I know I have breast cancer. I have been getting shooting pains in my breasts for years. I forget what he said, oh that’s because I lift too much. Because I had a very physical job, and I did go to the gym. So I said that I need you to send me for a mammogram because I have breast cancer. I just knew I did. I just knew. My mother had it.” This woman, diagnosed with stage IV ovarian cancer and stage IV breast cancer, was found to be BRCA-positive.
Participant 14: “I told the doctor something did not feel right. It was at my annual exam. I had just had a mammogram that he was looking at that said I was fine, and they did not see anything. And I said that I thought that that breast was larger and had swelling and that I had swelling under the armpit. He made me think that that was normal because he was just so dismissive of it, and maybe a little annoyed that I pushed even after he checked me twice, I still pushed and kind of questioned, and he was kind of annoyed. So then I thought who am I to know; maybe they are different… So then over the course of those next 10 months, it was still there, the swelling is still there that I noticed. And then all of a sudden, I start to notice the nipple going in. And then at that time I had different insurance, and I was having a hard time getting an appointment. I had an insurance from the school (where she was employed) where they would reimburse me, but I had to pay upfront. And I went back to the same gynecologist office… And they were like ‘oh with that insurance, we have to clear you first.’ And I had to do this paperwork. So it was delayed at least a month… So I had to pay for it upfront and then get reimbursed. Then meanwhile I had the nipple pulling in… But then I went on the NJCEED (New Jersey Cancer Education and Early Detection Program) program because they basically said, ‘look, we have to treat you like you were under insured because even though this program that you are in will reimburse you, none of the doctors in New Jersey are going to see you upfront without you paying.’ So that’s how I ended up in that program.”
Theme: Lack of Knowledge: “I Do Not Know the Details”
Participant 4: “And mine is called HERS-2. I know that it’s very deadly and aggressive.”
Participant 15: “She said to me we could’ve done a mammogram on you. And because it was so large we may not have seen it. I said what do you mean you might not have seen it? Because the larger they are, the more they have coverage to hide behind breast tissue. So she said we could of did a mammogram on you. I said well, my next question, how long do you think it was there because it was so large? I should back up, it was so large. And she said well, she goes, we’ll say 3 or 4 months, could’ve been less, could’ve been longer.”
Participant 18: “And she told me that my cancer was the one that she would always want to find, that it was a pretty benign cancer and that there was no problem, I should feel well. And that she was going to operate on me.”
Participant 19: “No, I do not recall anyone telling me that” (When asked if she knew what type of breast cancer she had).
Theme: Sense of Spirituality: “Thank God”
Participant 4: “Yeah I think of myself as a survivor. I feel like of myself as a child of God, and I feel oh so blessed. All 3 of those things. Oh yes I do. Yeah I know. That stuff is devastating. You know sometimes I still well up about certain things. That’s the thing, you know, that God let me live. You know, to me, this is a renewal of the spirit and a second chance at life for me to live better. That’s what this is. Yeah I believe that God give people second chances, you know.”
Participant 5: “So we went there, and they had little prayer cards at the door, and if you wanted them to say a special prayer for you, you just fill a little card in. Then I filled my card in. They called my name and everything and had me come to her prayer, and, um, and I testified and everything like that, and, um, all of a sudden like a force came on, a force came on me… When I was going through that traumatic experience at church, somebody was going through my body like peristalsis wave; it was like something was going through my body. And, and I felt like everything was healed. You know and I said well I talked to the doctor about it. He understood. He said, “Well, do you still want to have surgery?” I said yeah, I’ll just go through the motions in case. I said that’s what the Lord put you here for to do this, so I might as well go ahead and get it done. You know, in case.”
Participant 6: “You learn to do with your faith. No one in this world is going to take your faith away from you except for yourself. Yes, I do believe there is the Lord, there is a God, there is a Jesus, there is somebody up there protecting us and giving us all the strength. Because if He brought us into this life, He is the only one that’s going to take us out. Doctors are there as tools from God. And I’m not in religious care. But yes, I do have my faith.”
Participant 7: “I just wanted to cry, why me, why me. I killed myself taking care of Pop and Mom, what else do you want me to do Lord? But you threw it out there to me, so there must be a way that I could go around it. But your mind cannot. The thing is you are all alone at night.”
Participant 10: “But I have a lot of faith. And immediately I said I’m not going to succumb to it, and I just believe that, due to, if I can be transparent, due to lifestyle decisions, that it was a test, it was a storm, and that God was going to bring me through it. And I did just that. I did just that.”

One woman described the unique experience of accessing healthcare as an immigrant to the United States:

I did not do (get a mammogram) until 5 years after I got here because I had no idea where to go. Because one of the things with Latinos in this country is that nobody helps you or tells you what places you need to go… I had 3 jobs. I would leave the warehouse and go cooking, go cleaning, cleaning the offices because that is also where I like to go because it was less time and more pay and I learned how to drive. So then I had no time to get screening, and I would keep saying I would go tomorrow, and I would go the next day. And then before I knew it the time had passed. (Participant 18)

Other women who were symptomatic described waiting to go to a physician because of lack of insurance:

But I felt a lump that was probably like a bubble gum ball. It was very hard, and it was on my left breast. And that was during the summer. And by October, it had turned into almost a tennis ball. And it got to the point where it was overtaking my chest… So anyway I did not have insurance at the time, and I worked full-time, and because of my income, I could not get health insurance…, so at that point I just elected to not work…, so I had to quit my job, you know, get out of my job and have health, state insurance. And that’s how I did it… I collected welfare. It was $320 a month. (Participant 12)

She was a single mother of 2 young children who had been earning $75 000 a year; she lost her home during this period of unemployment as she could not pay her mortgage.

Two of the women were underinsured (defined by NJCEED as policies that do not cover screening examinations) prior to diagnosis. While not prevented from going to a physician, these women described a poor quality of care, and although they consulted with various providers, neither received a definitive diagnosis. Each of these women had significant delays from first noticing a symptom to diagnosis and then treatment, and these women were ultimately diagnosed as having stage IV disease. These women, both of whom were White and who had higher incomes than the other participants (although still at or below 250% of the federal poverty level), were also the only women who discussed wanting a second opinion and not trusting their initial doctors’ determinations (Table 3).

Lack of Knowledge: “I Do Not Know the Details”

Few of the women were able to provide accurate details about the kind of breast cancer they had. The researchers had been provided with a list of patients’ names and stages from the NJCEED program office, but some of the women provided information during the interview that contrasted with what was provided by NJCEED. The lack of knowledge of type of cancer, stage at diagnosis (other than the women diagnosed at stage III or IV), and the inconsistency in reporting may be related to a lack of understanding of the disease process, which could impede the pursuit of care (Table 3).

Yeah. I did not know these words and whatever. They may say to you and pronounce things, and I’m educated, but at that time, it just did not; everything was like you are throwing too much at me at one time. Because I have cancer. All I know is, oh you got this and this, and this and that. I could not understand that at that time, you know. And I had to go back. I had to have somebody sit me down, and they did do that. (Participant 1)

Sense of Spirituality: “Thank God”

Most of the women (90%) interviewed mentioned the word “God” during the interview. Many spoke of their religion/spirituality as a source of support during their treatment. The phrase “thank God” was used often in response to questions about treatments and being told they were “cancer-free.” Women spoke of prayer and praying with others, having faith and trust, and that God was going to “bring me through.” Some of the women discussed God as a powerful force who brings disease, but who can also cure disease. One woman described a spiritual experience that left her feeling healed of her breast cancer, but she had the recommended surgery, “to just go through the motions in case…” as she thought the Lord put the surgeon in place to do His work (participant 5) (Table 3).

Discussion

This study examined delays in diagnosis and treatment of breast cancer and the factors that may have led to those delays by focusing on underinsured or uninsured women diagnosed with invasive breast cancer. Of the 20 women who participated in this study, 6 of the women self-reported being diagnosed with stage III disease, and 3 women reported being diagnosed with stage IV disease. This finding, of such a large percentage of women diagnosed at a late stage, is consistent with that of Hsu and colleagues,3 which found that women with Medicaid or without insurance were more likely to be diagnosed with later-stage breast cancer. This population has also been found to have worse survival, which is consistent with diagnosis at a later stage.

While studies have found that non-White race is often associated with diagnosis at a later stage and with worse prognosis than White women,3,26 socioeconomic factors have consistently been found to be associated with later stage at diagnosis as well. Whereas Millon-Underwood and Kelber27 found that mammogram screening is lower among women who are uninsured and living in low-income communities that may lack screening facilities, other studies have found that social determinants of health (low income, low education or literacy, lack of transportation) and individual-level factors (poor understanding of the disease or mammography, previous unpleasant screening experiences, and social isolation) may all negatively impact screening utilization.26,28 While most of these women resided in a low-income urban community, there was a free cancer screening program located within that local community. However, a recent study of that cancer screening program found that women who were screened there tended to be symptomatic at diagnosis and diagnosed at a later stage when compared with insured women diagnosed at the same academic medical center.29 Despite the many educational efforts related to breast cancer screening and the availability of free screening services for uninsured women, many women still do not regularly utilize mammography services, and these factors must be understood to improve breast cancer outcomes for low-income women.

Maly and colleagues30 examined delays in diagnosis and treatment in a multiethnic, multiracial sample of 921 low-income women, including women who were diagnosed via screening or who detected their own breast cancer. In that study, the symptomatic (self-detected) women experienced much greater diagnostic and treatment delay than the screening detected women, and the African American women experienced the longest delays between symptom detection and diagnosis. Those researchers found that greater perceived self-efficacy in healthcare provider interactions was the only significant predictor of shorter delays in the symptomatic women.30

Women who self-detect breast cancer must first realize that what they are feeling may be serious and then must navigate the healthcare system to get the treatment needed. These women are perhaps more likely to experience patient-related delays. Some causes of these delays include a lack of knowledge, perception of competing priorities, and fear of breast cancer or cancer treatment.31 In this study, we saw that the majority of women were symptomatic on diagnosis and expressed concern with their inability to access healthcare. Other causes of delay were the lack of a usual source of care because of a lack of insurance, a limited understanding of their symptoms, a reliance on spirituality as a means of cure, a fear of cancer as a death sentence, and competing priorities (family, finances). The women did not express a fear of treatment for the most part, and once they began treatment, all of the women expressed satisfaction, particularly with the NJCEED staff, but also with the physicians and the hospital.

Women who are participating in systems by utilizing screening services on a regular basis have already made a connection that is likely to facilitate a timelier receipt of follow-up care, although they may experience system-related delays. These delays, which have been found more likely to impact low-income populations, were more difficult to tease out, especially when the women were unclear about the sequence or the length of treatments.

Studies have examined system-related delays in many low-income countries.32 In Thailand, referral to a surgeon after an initial visit with a primary care provider depends on disease severity and insurance33; in Malaysia, as in other low-income countries, mammogram use is low, but additionally, there is a high rate of false-negative mammograms that lead to delay in referral34; in multiple African countries, there are delays due to false initial diagnoses in primary care and the cost of and distance to secondary or tertiary care centers.35 Studies of system-related delays in the United States are few. Bleicher and colleagues36 found that preoperative delays were increasing in older women (based on Medicare data) related to imaging modalities, biopsy type, clinician visits, and extent of surgery (planning for immediate reconstruction was a frequent cause of delay). An integrative review of 317 studies (United States and many other countries included) found that comorbidity, communication between doctor and patient, preoperative components, and ethnicity were associated with system-related delays.37 Lobb and colleagues38 suggest that improved communication between patient and physician can reduce these system-related barriers to care. However, a recent article on medical mistrust cautions providers not to expect patients from marginalized groups to attempt to bridge the trust gap alone. In discussing medical mistrust, Sullivan39(p25) suggests “in the context of a history of oppression, the burden falls on members of the group with greater power to understand how to be trustworthy and how to signal their trustworthiness.” In this study, the researchers did not have access to specific dates of care such as timing of mammography to follow-up for diagnosis or date of treatment, however, the women spoke of weeks to months between stages of care.

Barriers to Care

Participants tended to focus on their lack of insurance as a major barrier toward accessing screening and treatment services and as a significant cause of the delays in treatment that they experienced. While services were available in the local community, the women tended not to search them out for preventive healthcare, but they were able to locate the program office for diagnostic services once symptoms were found. This lack of access to preventive care may reflect the lack of a usual source of care and reliance on the fragmented care available at local low cost clinics used by most of the women. A providers’ recommendation for screening has been found to be one of the most predictive factors in screening adherence; physicians or other primary care providers can play an integral role in recommending screening, providing referrals, and coordinating follow-up care.40

One notable exception was found with the 2 women who were underinsured, rather than uninsured prior to diagnosis. These women, both ultimately diagnosed with stage IV cancer, reported spending months or years arguing with their physicians to acknowledge their symptoms, with limited effectiveness, and then reaching out for second opinions. This is in stark contrast to the other women in this study who were diagnosed in the NJCEED program and who did not report seeking a second opinion even if their surgeon refused to perform a requested bilateral mastectomy. Indeed, 3 women told the same story that they could not get a bilateral mastectomy because often an infection will develop in the noncancerous breast, which will delay needed follow-up treatment, a rationale that lacks clinical evidence. In a similar study from 2015, in a sample of middle-class primarily White insured women diagnosed with breast cancer, the majority of the women sought a second opinion.41 A recent study found that of 70 women who sought a second opinion at a National Cancer Institute–designated cancer center after a breast cancer diagnosis, the diagnosis was changed for 43% of the patients who presented42; therefore, receipt of a second opinion may improve care or treatment outcome. Breast cancer treatment decision-making, including the pursuit of a second opinion, has been found to vary based on tumor characteristics, surgeon’s experience, and patient’s preference.42 Women with lower SES have reported experiencing poorer communication from their providers, less satisfaction with treatment decision making, and increased decision regret when compared with women with higher SES.43,44

An interesting finding was the relatively high percentage of women who chose to undergo bilateral mastectomy after being diagnosed with unilateral breast cancer. Most studies have found that low-income, uninsured, and racial/ethnic minority women are less likely to make this choice, although the procedure has been steadily increasing in women with higher socioeconomic status.45 Baptiste and colleagues,46 in a study of women who underwent bilateral mastectomy at 4 Indiana University affiliated hospitals, found that reducing long-term risk was the strongest motivation for this more extensive procedure. Those authors found that lower-income women were more motivated to choose bilateral mastectomy, as compared with women with higher incomes, for both long-term risk reduction and the avoidance of treatment. In this study, a number of women expressed the notion “I’m not playing around” as a rationale for removing both breasts—as though they wanted to take control and eliminate as much as possible a recurrence of their breast cancer by making this surgical choice. It is not known whether the women were told that removing both breasts would prevent a return of the cancer. Baptiste and colleagues46 propose that financial insecurity and the desire to avoid the costs of another cancer diagnosis may be a reason for this decision making, but that was not a certainty in their study or in this study. Further research should follow women’s choice of bilateral mastectomy as a function of socioeconomics and as a measure of women’s self-efficacy and comfort with taking on a major decision-making role so as to better understand the factors that are driving bilateral mastectomy across race, ethnicity, and socioeconomics.

While 18 of the 20 women who participated in this study experienced delays, it appears that 11 of these women were experiencing patient-related delays as defined by Caplan13 as a delay in accessing medical care after self-discovering a symptom. Studies have found that women who are diagnosed in the NBCCEDP are more likely to be symptomatic on diagnosis as compared with nonenrollees.47,48 While the percentage of breast cancers found by mammography has increased over the years, recent studies still find that many breast cancers are diagnosed via self-detection or clinical breast examination, and low-income women are even less likely to be diagnosed via a screening mammogram.49–51 An important question that remains unanswered is what could encourage low-income, uninsured women to prioritize their own health by utilizing preventive services. Perhaps the many uncertainties of living in poverty are just too overwhelming, and to be effective, a reform would need to capture the upstream social determinants that keep these women from acknowledging their own health needs. Or perhaps, as a physician’s recommendation has been found to be one of the most effective facilitators in breast cancer screening,40 the lack of a usual source of care somewhat negates the benefits of an easily accessible cancer outreach program.

One woman in this study who detected her own tumor did not report any delays in the receipt of care. This woman was 21 years old at diagnosis, too young to be receiving breast cancer screening, and the first in her family to find that she was BRCA-positive. She was diagnosed with stage II breast cancer and received a bilateral mastectomy. Now that she is 8 years out from her cancer diagnosis, she no longer has the Medicaid coverage that she had received from NJCEED and has not received the appropriate follow-up care. She stated that she “would like to have an actual scan, so that can be worrisome sometimes, not having insurance.”

Limitations

In qualitative research, limitations in generalizability must be expected. All participants were diagnosed and treated at one academic medical center NJCEED program, which may lead to recruitment bias. Although the researchers were interested in women’s decision-making related to delays in treatment, for many women it was difficult to track the actual timeline. The participants in this study did not appear to recall or keep written records of their diagnoses and treatment. The majority of the women could not provide information on the type of cancer, and their recall of stage at diagnosis was inconsistent with the information provided to the researchers by the NJCEED program. The women diagnosed with stages III and IV cancer, however, were the most likely to recall specifics of their diagnosis and treatment.

Conclusion

There have been few if any articles that explicitly address the concerns of low-income, uninsured women diagnosed with breast cancer through the NBCCEDP. This qualitative study revealed that delays in diagnosis and treatment were quite common for these women. While the lack of insurance is a factor in these delays, it was not the only factor. Women expressed fear, the need to care for their families, and a tendency to not prioritize their own health concerns as reasons to not pursue diagnosis and treatment. While programs such as NJCEED are integral to the care of low-income, uninsured individuals throughout the United States, it is likely that access to a consistent primary care provider who oversees a woman’s use of preventive care can help her to navigate the healthcare system as a most effective means of improving breast cancer outcomes for financially insecure, resource-poor women in the United States.

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Keywords:

Breast cancer; Disparities; Treatment delays

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