“Is it cancer or not?” A qualitative exploration of survivor concerns surrounding the diagnosis and treatment of ductal carcinoma in situ (DCIS)

Abstract

Background:

Of the nearly 50,000 women in the United States who undergo treatment for ductal carcinoma in situ (DCIS) annually, many may not benefit from treatment. To better understand the impact of a DCIS diagnosis, we engaged patients self-identified as having had DCIS regarding their experience.

Methods:

In July 2014, we administered a web-based survey through the Susan Love Army of Women breast cancer listserv. The survey included open-ended questions designed to assess patients’ perspectives about DCIS diagnosis and treatment. We applied deductive and inductive codes to the responses; common themes were summarized.

Results:

Among 1,832 women included in the analytic sample, median age at diagnosis was 60. Four primary themes were identified: 1) uncertainty surrounding a DCIS diagnosis; 2) uncertainty about DCIS treatment; 3) concern about treatment side effects; and 4) concern about recurrence and/or developing invasive breast cancer. When diagnosed, participants were often uncertain about whether they had cancer or not, and whether they should be considered a “survivor.” Uncertainty about treatment manifested as questioning the appropriateness of the amount of treatment received. Participants expressed concern about the “cancer spreading” or becoming invasive, and that they were not necessarily “doing enough” to prevent recurrence.

Conclusion:

In a large, national sample, participants with a history of DCIS report confusion and concern about the diagnosis and treatment, causing worry and significant uncertainty. Developing strategies to improve patient and provider communications regarding the nature of DCIS as well as acknowledging gaps in current knowledge of management options should be a priority.

Precis

DCIS survivors often report feelings of uncertainty and concern about their diagnosis and treatment. Developing strategies to improve communication regarding the nature of DCIS as well as the potential benefits and harms of different DCIS management options should be a priority.

Introduction

Each year in the United States, nearly 50,000 women are diagnosed with ductal carcinoma in situ (DCIS), a non-invasive breast condition that has little potential to spread beyond the breast.¹ Despite the excellent prognosis associated with a DCIS diagnosis, the current standard of care for DCIS treatment is comparable to that of lower risk invasive breast cancer which usually includes some combination of surgery, radiation, and/or endocrine therapy. The majority of patients with DCIS remain free of invasive disease following treatment: in one study that enrolled women low-risk DCIS who received surgery without radiation,12-year ipsilateral invasive breast cancer rates were 7.5% and 13.4%, among those with low-intermediate and high-grade disease, respectively.² While there is substantial heterogeneity among DCIS lesions,³ epidemiology and natural history studies have estimated that only about 20–30% of DCIS diagnoses will advance to invasive cancer over a lifetime.^{4, 5} Thus many women are likely overtreated for their DCIS, underscoring the importance of patients fully understanding their disease and associated risks, in an effort to make informed decisions when choosing among treatment options.

The good prognosis associated with DCIS in combination with data that suggests that a significant proportion of DCIS will not progress to invasive breast cancer highlights the potential for non-surgical approaches to manage DCIS, particularly for patients with lower-risk disease.⁶ Research suggests that greater than 40% of women who are presented with the potential risks and benefits of different DCIS treatment options would think about active monitoring as a potential management option,⁷ indicating that a non-surgical approach would be appropriate for and acceptable to many women. Prospective trials currently evaluating surgical treatment for DCIS vs. active monitoring will provide critical information regarding disease outcomes, as well as quality of life and psychosocial health, from serial patient-report outcomes (PROs) that are being collected.^8–10

Understanding both the clinical and psychosocial impact of a DCIS diagnosis from the patient’s perspective can identify knowledge gaps, opportunities for improved communication, and unmet supportive care needs. To both inform and complement the PROs collected as part of the Comparing an Operation to Monitoring, with or without Endocrine Therapy (COMET), for low-risk DCIS Trial,⁸ we engaged a broad sample of women self-identified with DCIS regarding their experience of DCIS, from diagnosis, treatment, and survivorship care, in an effort to better understand their primary concerns at diagnosis through long-term follow-up.

Methods

In July 2014, we administered a one-time web-based survey (Appendix) to patients who were invited by email using the listserv of Dr. Susan Love Research Foundation’s Army of Women, a registry that facilitates recruitment of participants to breast cancer-focused research studies. The survey included open-ended questions designed to assess patients’ perspectives of their experiences with the diagnosis and treatment of their DCIS; close-ended questions captured socio-demographic characteristics and treatment details (surgery, radiation) as well as time from diagnosis. A single question assessed perceived income insecurity (How would you describe your household’s financial situation?) with response options including: enough money for special things; enough for bills but little extra; money for bills but need to cut back; difficulty paying bills.^{11, 12} This study was deemed exempt from full review by the Duke University Medical Center Institutional Review Board.

Analysis

Responses to the open-ended questions ranged from shorter phrases to sentences as well as many longer paragraphs, thus necessitating a more in-depth qualitative analysis to explore the experiences and perspectives presented by participants. We conducted thematic analysis through an iterative multi-staged process that incorporated both inductive and deductive coding.^13–15 We applied deductive codes from the main topics of survey questions and then, through an iterative process, two coders (SMR and JMG) reviewed the responses of approximately 100 respondents and expanded the codes to include inductive codes emerging from the data. Following these initial steps, new codes were added to the codebook as they emerged to create a comprehensive coding schema that was applied to all survey responses. The full coding was conducted by several trained members of the research team, with a primary coder (SMR) reviewing the coded data and finalizing a coded, analytic data set. Each code was then examined in-depth, across all respondents, to identify key contexts, conditions, patterns and themes, as well as divergent cases, and to provide insight into the breadth of experiences across all respondents. To fully explore the complex and nuanced perspectives, each response was considered individually, and coding was conducted at the level of individual response i.e., if a participant discussed an issue in more than one response, each of these responses were considered and coded individually. A cross-code review identified four primary themes that highlighted the most critical aspects of the participants’ DCIS experiences. The code development process was started in Microsoft Excel (Microsoft Corporation, Redmond, WA) and then uploaded into NVivo (QSR International, Burlington, MA) where the comprehensive codebook was applied to all responses. Results were summarized, reviewed, and debriefed by two members of the research team (SMR and AR) to allow for interpretive scope and consistency.

Results

Study population

In total, 2,432 respondents self-identified as having been diagnosed with DCIS completed the survey. After accounting for duplicate responses and excluding participants who reported an invasive breast cancer, a second primary or recurrent tumor, or other benign breast lesions without DCIS, 1,832 (75.3%) participants remained in the analytic sample. Table 1 summarizes participant’s self-reported socio-demographic characteristics. The median age at diagnosis (n=1,781) was 60 years (range: 29–95 years). Median time from diagnosis (n=1,820) was 6 years (range: 0.1–61 years). Most participants (90.4%) identified as white, 2.4% as African American or Black, and 2.8% were Hispanic.

Table 1.

Study population characteristics (n=1,832)

	N (%)
Median age at time of survey (range)a	60 (29–95)
Race
African American/Black	44 (2.4)
White	1649 (90.0)
Asian	25 (1.4)
Native American	6 (0.3)
More than one race/Other	69 (3.7)
Not reported	39 (2.1)
Hispanic	52 (2.8)
Perceived financial situation
Enough money for special things	1229 (67.1)
Enough for bills but little extra	405 (22.1)
Money for bills but need to cut back	91 (5.0)
Difficulty paying bills	46 (2.5)
Not reported	61 (3.3)
Median time (years) from diagnosis (range)b	6 (0.1–61)
Surgeryc
Lumpectomy	1043 (56.9)
Unilateral mastectomy	426 (23.3)
Bilateral mastectomy	326 (17.8)
No surgery reported	37 (2.0)
Radiation
Yes	945 (51.6)
No	875 (47.8)
Not reported	12 (<1)

^an=1,781

^bn=1,820

^cMost definitive surgery if women reported more than one procedure (e.g., lumpectomy and bilateral mastectomy reported as “bilateral mastectomy”

Primary themes

We identified four primary themes in the data set: 1) uncertainty surrounding a DCIS diagnosis; 2) uncertainty about DCIS treatment; 3) concern about treatment side effects; and 4) concern about recurrence and/or invasive breast cancer. Table 2 includes illustrative quotes corresponding to each theme.

Table 2.

Themes and representative quotes

Uncertainty surrounding a DCIS diagnosis:

“It’s hard having a diagnosis that’s not really cancer, and yet you might still lose your breast. It’s been psychologically challenging, because you have cancer but not-cancer.”

“After everything was finished, the attitude was don’t worry it’s not really cancer. Very mixed message.”

“Doctors saying it’s only “pre-cancer” yet at the same time emphasizing that I needed a mastectomy because at some point it would likely become invasive.”

“… I feel like I don’t deserve the title of “survivor” since it was a lot of nothing given what other women with breast cancer have to go through.”

Uncertainty about DCIS treatment:

“I was offered a mastectomy…at the time…seemed like over-kill when I could just have a lumpectomy.”

“I am…one of few who have chosen not to have surgery…I did a lot of research, and decided if I could find a doctor who would prescribe Tamoxifen (with no other treatment), that would be my choice of treatment… knowing I may not be doing enough (or maybe doing too much).”

“Did I really need treatment? Is DCIS like certain grades of prostate cancer that can be followed with no treatment? Who knows?”

“Doubt is always there - was mastectomy enough? should they have gone ahead and recommended chemo or radiation. Are we sure we got it all?”

Concern about treatment side effects

“I was only 33 and single. I was concerned about being rejected for my body.”

I just don’t like taking Tamoxifen. It is scary to take it and scary not to take it.”

“Occasionally, I wonder what after effects I could realize due to radiation - is my heart or lungs affected?”

Concern about recurrence and invasive breast cancer

“There is always the fear that if you had it in one breast, you will eventually get it in the other breast.”

“Will it return? Does this history affect my daughter? Am I more prone to a different cancer in another area?”

“Not knowing if it’s the aggressive kind and will continue on to invasive, or not.”

“Will it happen in the other breast? Is this something that can move to bone or lung, as some breast cancers do? I’ve been assured that it wasn’t that type--but one does think about it on occasion.”

Theme 1: Uncertainty surrounding a DCIS diagnosis.

When discussing uncertainty around DCIS diagnosis, most responses (n=1423) reflected uncertainty about whether DCIS was cancer or not, for example, describing the diagnosis as a “grey zone.” Associated with the diagnostic uncertainty was the common characterization of DCIS as a less severe diagnosis, (“it’s only DCIS”), however, this still promoted problematic dynamics. Some participants described an internal struggle about how to identify, if at all, as a cancer survivor, whilst others expressed a lack of understanding and support for patients with a DCIS diagnosis. This gap was felt most often through external relationships, including perceptions that their doctor minimized their diagnosis or failed to recognize its impact. There was, however, a minority of responses (n=43) where participants noted they were grateful they “only” had DCIS versus a more aggressive cancer diagnosis.

In addition to the lack of clarity about whether DCIS constituted a cancer diagnosis, there was inconsistency around what DCIS might become, namely whether it was a precursor to more advanced cancer. The severity of this concern, however, varied between participants with some simply acknowledging the issue as an unknown, while for others, questions regarding DCIS as a precursor to “full blown cancer” was a significant concern.

Theme 2: Uncertainty about DCIS treatment.

Over 2000 responses reflected feelings of uncertainty around the diagnosis. These responses were often related to the uncertainty around and difficulty in choosing a treatment for DCIS, with participants questioning if their level of treatment was appropriate, and some responses highlighting decisional regret even long after acute treatment phase. Responses varied between participants who wondered if they were over-treated for their DCIS and others who questioned whether they were “doing enough.” Regarding overtreatment, there were participants who were certain in their belief that their treatment was unnecessary or too aggressive, while others questioned or expressed uncertainty around the need for treatment. Concerns about undertreatment were sometimes expressed by participants, e.g., whether the treatment they chose would be sufficient to prevent recurrence or development of a future cancer. A small subset of responses (n=45) reflected more comfort or certainty with treatment decisions. These participants recognized the potential for overtreatment; however, they were unwilling to risk less aggressive treatment and saw their choice of treatment as based on their understanding at the time of their diagnosis.

Participants also expressed uncertainty and difficulty when considering surgery (lumpectomy vs. mastectomy), radiation, endocrine therapy, some combination of the three, or none at all. Others also mentioned struggles with their decision around breast reconstruction, including whether to choose it and, if opting for reconstruction, which type to have.

Perspectives regarding “watchful waiting” as a strategy were mixed. There were doubts and confusion about whether or not watchful waiting was adequate. Some participants said they had wanted it but were discouraged by their providers, and others were aware of it as an option but decided against it. A small number of responses (n=79) indicated that participants did in fact decline standard DCIS treatment; however, other responses (n=73) reflected upon whether participants would elect for watchful waiting if they were choosing treatment now, underscoring the persistent decisional regret some participants felt after the acute treatment phase for their DCIS diagnosis.

Theme 3: Concern about treatment side effects.

Over 1100 responses reflected participants’ concerns about treatment. These focused on both short and long-term side effects of surgery, radiation, and endocrine therapy, including concerns about physical and emotional sequelae. Most concerns were associated with specific sequelae of surgery and/or radiation including loss of a breast/nipples, uneven breasts, scarring, and disfigurement. Emotions ranged from severe depression and suicidal thoughts to lower levels of distress, fears, doubts, anxiety, embarrassment, feeling overwhelmed, and a general acknowledgment of an overall emotional burden. For some, this burden was intertwined with, and sometimes exacerbated by, the uncertainty and confusion surrounding the diagnosis and treatment of DCIS.

Concerns were also associated with specific treatment modalities. For example, participants noted that they wanted to avoid radiation or that choosing radiation was a difficult decision; a small number of participants reported choosing mastectomy in order to avoid radiation. Responses also highlighted long-term concerns about the effects of radiation on the heart and lungs. Additional concerns and side effects experienced included skin changes and complications (e.g., burns, scarring, sensitivity, texture changes), exhaustion/fatigue, pain, and impact of radiation on breast size and reconstruction. Additionally, responses noted difficulty with the length, frequency, and scheduling of radiation treatment.

Regarding surgery, pain and numbness along with the impact of surgery on appearance were common sequelae reported. Additional concerns and side effects experienced included impact on physical function (e.g., inability to breastfeed, loss of range of motion, back problems and mobility issues), and infection. The loss of a breast, recovery time, and reconstruction were reported as concerns for those who had considered mastectomy. Some participants emphasized the difficulty in having to have several surgeries, including re-excisions following a lumpectomy or having a mastectomy after failed lumpectomies.

Participants reported many of the side effects commonly experienced by survivors taking oral endocrine therapy. These included hot flashes, weight gain, muscle/joint pain/cramping, memory/cognition issues, depression, a decreased sex-drive, irregular periods and menopause, osteoporosis, fatigue, heartburn, hair loss, and vision problems. Some participants made general reference to endocrine therapy being challenging, upsetting, or not tolerated well, with a small subset of participants stating that they had stopped taking endocrine therapy because of side effects.

Theme 4: Concern about recurrence and/or invasive breast cancer.

Greater than 1100 responses reflected concerns about recurrence and/or invasive breast cancer. Participants expressed a variety of concerns about the likelihood of cancer coming back. Reponses often focused on participants’ concern around developing a cancer in the contralateral breast. Also mentioned were expressions about fear of developing “full blown cancer” or something “more aggressive” or “more harmful.” Spreading of the cancer to other parts of the body was also a concern for some participants.

Worry about recurrence or concern about the development of invasive breast cancer was sometimes tied into uncertainty and concerns about treatment. This included questions or doubts about whether their treatment decisions were sufficient. A few participants wondered what treatment options they would have or what that experience would be like if they recurred while others presented questions and concerns about how to monitor for recurrence or reduce their risk of recurrence. Additionally, a few participants noted that their concern shifted over time, resulting in decreased worry with the passing of time.

Responses also highlighted concerns or fears about DCIS being a precursor to other cancers, developing a different cancer, or being predisposed to or at increased risk of other types of cancer. A few participants described other cancer diagnoses that they perceived as connected to their DCIS diagnosis and treatment. Some pointed to their family history as playing a role in their risk perception for recurrence and other cancers. Other concerns included what a DCIS diagnosis meant in terms of risk to family members (e.g., daughters or sisters).

Discussion

A DCIS diagnosis can be confusing and distressing, with treatment decisions often made in the setting of a limited or incomplete understanding of the disease, its risks, and the pros and cons of different treatment options. We found that participants commonly expressed confusion about whether DCIS was cancer or not, as well as around the severity of DCIS. This confusion frequently factored into the uncertainty expressed with regard to DCIS treatment. Additionally, concerns around recurrence or developing a more aggressive cancer were fueled by the status of DCIS as a precursor lesion to invasive cancer and to the standard treatment of DCIS including surgery and potentially radiation. These themes are largely consistent with prior quantitative and qualitative studies that have explored the experiences and perspectives of DCIS survivors.^16–20 Our study builds on prior work as the largest analysis to date to address these issues in a national sample, adding granularity regarding the experiences of individuals with a history of DCIS with the open ended nature of many of the questions.

It has been suggested that use of the word “carcinoma” (despite DCIS being a non-invasive condition) may contribute to these concerns as well as to anxiety experienced following a DCIS diagnosis.²¹ In a series of interviews conducted with women without breast cancer, using the word “carcinoma” (vs. other descriptors such as ductal intraepithelial neoplasia or “abnormal cells”) evoked concern and apprehension.²² In another study that asked women without breast cancer about their treatment preferences in response to hypothetical instances where DCIS was referred to as either “non-invasive breast cancer”, a “breast lesion”, or “abnormal cells”, women were less likely to choose surgery when DCIS was described without the word “cancer”, suggesting that the language we use when examining DCIS to patients may impact treatment preferences.⁷ There has generally been a lack of consistency with regard to how clinicians describe DCIS to patients; “breast cancer”, “non-invasive cancer”, “pre-cancer”, and “abnormality/abnormal cells/cell changes”, are all commonly used in discussions with patients.^23–25 Concerns around how DCIS is perceived due to its description as a “carcinoma” and its potential influence on overtreatment has led to calls for the name to be changed,^26–28 including a 2009 National Institutes of Health (NIH) State of the Science Conference on DCIS Consensus Panel Statement which suggested that “strong consideration should be given to remove the anxiety-producing term ‘carcinoma’ from the description of DCIS.”^{21, 29} Though it has been alternatively argued that as long as the treatments remain the same as invasive disease with regard to surgery, radiation and endocrine therapy, a name change is not likely to substantially alter confusion and distress.²¹

Prior studies have documented that many women with DCIS have inaccurate risk perceptions related to DCIS and suboptimal knowledge about the condition. One study found that 43% of women were uncertain regarding the risk of DCIS spreading to other sites in their body and 27% were unsure about the risk of DCIS spreading and resulting in death without treatment.¹⁸ In another study, 61% and 33% of women with DCIS perceived their risk of a recurrence or of DCIS spreading to other parts of the body, respectively, as moderate likely, likely, or very likely within the next 5 years.³⁰ Risk of developing a recurrence of DCIS or invasive breast cancer, or cancer spreading to other parts of the body were similarly overestimated in a longitudinal study that enrolled over 400 women with DCIS.³¹ Importantly, studies of women with breast cancer suggest that anxiety is associated with overestimation of recurrence risks.^31–33 Thus, addressing confusion about the diagnosis and misconceptions about DCIS risk and prognosis can potentially improve underlying anxiety and DCIS-related concerns about treatment and outcomes as well as help foster quality decision-making around treament.²¹ There is also evidence that communication with a provider is positively related to the likelihood of breast cancer patients correctly estimating their risk of recurrence.³⁴ However, communicating cancer-related risk is complex, and improved methods to effectively communicate information around DCIS and its associated risks to those affected should be a priority.^{20, 35} While multiple online educational resources do exist for patients diagnosed with DCIS, few have focused on enhancing communication between patients and providers to support optimal decision-making around DCIS treatment.^{36, 37} Decision support tools, which can help patients weigh the risks and benefits of different treatment options whilst accounting for individual preferences, represent a promising approach. An interactive decision support tool (www.dcisoptions.org/dst) was recently developed for this purpose and is available to women diagnosed with DCIS who are considering their treatment options.³⁸

We acknowledge our analysis has some limitations. We relied entirely on self-report of a DCIS diagnosis and though we excluded participants who specifically referred to an invasive breast cancer diagnosis (with or without DCIS) in any response, we were unable to systematically confirm diagnoses. Army of Women participants have actively chosen to participate in a research registry and our respondents were overwhelmingly white and self-described as having a high level of financial comfort. Additionally, this was a convenience sample of DCIS survivors. Thus, our analysis sample may not be representative of others with DCIS. In particular, our predominantly white, non-Hispanic study sample may not reflect the experiences of patients of diverse racial and ethnic backgrounds. In one prior study, Spanish-speaking Latina women with DCIS were less satisfied with treatment decision-making and had more decisional regret relative to white women.³⁹ Latina women have also demonstrated lower levels of knowledge regarding DCIS treatment and outcomes, as well as increased levels of distress as a reaction to DCIS, compared to White women.^{40, 41} In a study of Chinese women with DCIS, Wong et al. reported suboptimal comprehension around issues related to a DCIS diagnosis, likely attributable to a scarcity of Chinese language informational resources.⁴² Collectively, these findings underscore the importance of cultural considerations when counseling patients regarding DCIS treatment options. Notwithstanding these limitations, our results suggest substantial heterogeneity around the experiences of DCIS survivors even among this selected group.

Our study further highlights the value of incorporating patient-reported experiences and endpoints to help inform preference-based decisions when patients are offered different treatment options. For women with DCIS, clinical trials like the COMET,⁸ LORIS,⁹ and LORD¹⁰ studies, which incorporate robust PROs, will provide additional evidence for patients, survivors, and their family members, health care providers and other stakeholders regarding the medical and psychosocial benefits and harms of different DCIS management options, including active monitoring.