Recommendations to improve patient‐centred care for ductal carcinoma in situ: Qualitative focus groups with women

Abstract Background Patient‐centred care (PCC) improves health‐care experiences and outcomes. Women with ductal carcinoma in situ (DCIS) and clinicians have reported communication difficulties. Little prior research has studied how to improve communication and PCC for DCIS. Objective This study explored how to achieve PCC for DCIS. Design Canadian women treated for DCIS from five provinces participated in semi‐structured focus groups based on a 6‐domain cancer‐specific PCC framework to discuss communication about DCIS. Data were analysed using constant comparative technique. Setting and Participants Thirty‐five women aged 30 to 86 participated in five focus groups at five hospitals. Results Women said their clinicians used multiple approaches for fostering a healing relationship; however, most described an absence of desired information or behaviour to exchange information, respond to emotions, manage uncertainty, make decisions and enable self‐management. Most women were confused by terminology, offered little information about the risks of progression/recurrence, uninformed about treatment benefits and risks, frustrated with lack of engagement in decision making, given little information about follow‐up plans or self‐care advice, and received no acknowledgement or offer of emotional support. Discussion and Conclusions By comparing the accounts of women with DCIS to a PCC framework, we identified limitations and inconsistencies in women's lived experience of communication about DCIS, and approaches by which clinicians can more consistently achieve PCC for DCIS. Future research should develop and evaluate informational tools to support PCC for DCIS.


| BACKG ROU N D
Ductal carcinoma in situ (DCIS) is a non-invasive breast condition characterized by abnormal cells confined to the breast ducts that represents up to 25% of all screen-detected breast cancer. [1][2][3][4] itself is not life threatening, but is a risk factor for progression to invasive breast cancer. 5 Currently, there is no reliable way to determine which cases will progress. Thus, standard treatment for DCIS is similar to treatment for invasive breast cancer: lumpectomy-alone, lumpectomy and adjuvant radiation and/or hormone therapy, or mastectomy, options that may result in treatment-associated adverse clinical and psychological outcomes. [5][6][7] When DCIS is treated, the 20-year breast cancer-specific mortality rate is 3.3% (95% CI, 3.0% to 3.6%). 8 The management of DCIS is complex for several reasons.
Research shows that most women have not heard of DCIS prior to their own diagnosis, and since DCIS may not present with physical symptoms, the diagnosis is often shocking to women and their families. 9 Women are further confused when told they have a noninvasive condition with an excellent prognosis, yet surgical treatment is recommended. 10 Research shows that women with DCIS desire more comprehensive information to better understand their condition and treatment options. 11 Women with DCIS often have inaccurate perceptions of the risk of developing and dying from breast cancer, [12][13][14] and experience similar levels of anxiety to women with invasive breast cancer. 15 Given poor health-care experiences and outcomes, women with DCIS may benefit from a patient-centred approach.
Patient-centred care (PCC) is defined as care that considers a patient's clinical needs, life circumstances, and personal values and preferences. 16 PCC informs, educates and engages patients, so their perspectives are incorporated in care planning and treatment, and in on-going medical, psychosocial and self-management support. 17 PCC has improved patient knowledge, communication with providers, satisfaction, treatment adherence and health outcomes; and reduced patient anxiety, missed work, readmission rates and mortality. [16][17][18] Considerable research has conceptualized PCC and offers guidance on how to achieve it. [19][20][21] Specific to cancer, a series of studies gathered input from patients and providers to generate a framework comprised of 6 domains that, when met, optimize PCC: fostering healing relationships, exchanging information, responding to emotions, managing uncertainty, making decisions and enabling self-management. 22,23 Despite evidence of suboptimal care amongst women with DCIS, [9][10][11][12][13][14][15]

| Approach
Given the paucity of prior research on PCC for DCIS, we employed a qualitative design to thoroughly explore women's experiences and suggestions related to PCC for DCIS. 27 More specifically, a basic qualitative descriptive approach was used. 28 Unlike other qualitative approaches that employ or generate theory, this technique elicits straightforward descriptions of lived experiences. 29 We conducted in-person focus groups rather than individual interviews because interaction amongst participants encourages rich, synergistic discussion about common and differing views. 30 This study was approved by research ethics boards at the University Health Network and five Canadian hospitals at which focus groups were held. We complied with the 32-item Consolidated Criteria for Reporting Qualitative Research (Appendix S1). 31 Rigour was further ensured through purposive sampling, independent coding and review of data by the research team, reporting data with anonymous identifiers to demonstrate views from multiple participants and assessment of discrepant experiences and suggestions. 32 There was no relationship with participants, who provided consent prior to focus groups.

| Sampling and recruitment
We used purposive sampling by province and age to recruit Englishspeaking adult women (18+ years) treated for DCIS within the previous 2 years to minimize recall bias. Women were excluded if they had been subsequently diagnosed with invasive breast cancer.
Eligible women were identified and recruited through participating hospitals in five Canadian provinces where physician research team members were based. Recruitment strategies varied by hospital site dependent on local research ethics board requirements; most often, physicians linked us with their clinic nurse or research assistant, who identified eligible women from their practice and introduced the study to them either in-person or by telephone.
Thus, physicians on our research team were unaware of who from amongst their practice took part in focus groups. There was no prior relationship between focus group participants and those conducting focus groups. Women provided written informed consent in advance or at the outset of focus groups. From each of 5 provinces, we aimed to recruit 6 to 8 women, a common size for focus groups. 30 Recruitment proceeded to thematic saturation, which was established through review and discussion of emerging themes amongst the research team concurrent with data collection and analysis.

| Data Collection
Between April and August 2017, two-hour focus groups were held in a meeting room at hospitals where participants were treated to provide a familiar, accessible environment. The semi-structured focus group guide (Appendix S2) was informed by the McCormack et al PCC framework, 23 chosen because it is the most comprehensive, specific to cancer and reflects ideal information and behaviour considered essential by cancer patients and clinicians for achieving PCC. A cancer-specific PCC framework was chosen because prior research shows that women with DCIS are often told or believe they have invasive breast cancer [12][13][14] and experience similar levels of anxiety to women with invasive breast cancer. 15 A semi-structured approach was employed because we wanted to understand whether women experienced PCC according to its multidimensional components, which domains were met or not met, and their suggestions for addressing distinct domains in order to optimize PCC.
Women were asked to explain whether and how they experienced each of six PCC domains (fostering healing relationships, exchanging information, responding to emotions, managing uncertainty, making decisions and enabling self-management). They were asked to focus on communication between themselves and the clinicians involved in their treatment. The first focus group was facilitated by ARG (PhD, female Scientist, training and experience in qualitative research) and observed by BN (MSc, female, Research Associate, training in qualitative research), the second focus group was co-facilitated by BN and RU (PhD, female, Scientist, training and experience in qualitative research), and the following three focus groups were facilitated by BN. At each focus group, the facilitator reviewed the purpose of the study and focus group process. For each question, individual women were asked to speak, followed by group discussion. Focus groups were audio-recorded and transcribed verbatim by a professional transcriptionist.

| Data analysis
Unique themes were derived inductively from the data using constant comparison and Excel. 33 Transcripts were analysed to identify and code all themes, and create a codebook of themes and exemplar quotes (level one); then, coded data were examined to expand or merge thematic codes, and refine the codebook (level two). Following the first focus group, BN, BJ (a research assistant) and ARG independently analysed the transcript, then compared and discussed findings to establish the codebook. It was shared with the research team, which included 7 breast cancer surgeons, whose feedback refined the codebook, and wording and flow of questions for remaining focus groups. Subsequent transcripts were analysed by BN and BJ with periodic review from ARG. The research team reviewed themes and exemplar quotes on two occasions, which led to further refinement and interpretation of themes. Quotes were tabulated by PCC domain and theme. For each domain, descriptions of information or behaviour that was present or lacking were summarized as recommendations for PCC for DCIS.

| Participants
In total, 35 women participated in five focus groups (mean seven per group). Participants varied by age, treatment received and self-reported family history of breast cancer (Table 1).

| Themes by PCC domain
Themes and exemplar quotes by PCC domain are included in Appendix S3, summarized in Table 2 and discussed here. Themes were similar across age groups, treatment received and province, suggesting that our findings reflect the experiences of women with DCIS across Canada.

| Fostering healing relationships
Most women reported having a good relationship with their clinician. Women described several clinician characteristics and behaviours they viewed as fundamental to having a good relationship.
Characteristics were identified by the themes of honesty, competence and patience, and behaviours were identified by the themes of non-domineering body language and personal inquiries.

Competence
Several women said that having trust in clinician's technical competence provided them with a sense of security during a state of vulnerability, and with reassurance that they would be taken care of.
One woman said that knowing her surgeon was 'the best' was more important than having a surgeon that was personable.

Patience
All women said that clinician patience during their discussion was imperative to a positive relationship. They described patience as having a calm demeanour, and providing information and answering questions in an unrushed manner. This made women feel listened to and cared for. Women who were rushed by the clinician during their appointment said they felt isolated and upset.

Non-domineering body language
Several women emphasized the role of body language in communication. Women said that their clinician expressed caring and commitment by sitting beside them and at the same eye level. Alternatively, one woman said that, by standing or sitting at a higher point than her and talking physically down to her during the entire discussion, the clinician made her feel insignificant.

Personal inquiries
Most women valued when clinicians spent time to inquire personally about them prior to discussing clinical details. By taking time to get to know them, women said this reduced anxiety and made them feel more at ease to discuss concerns and ask for support.

| Exchanging information
Most women were confused by unclear and conflicting terminology used by clinicians to describe DCIS, which also failed to distinguish DCIS from invasive breast cancer. Several women said their understanding improved when clinicians took time to explain and repeat information, and some women desired guidance on which questions to ask.

Variable language to describe DCIS
Women said their clinician used multiple terms to describe DCIS including 'early-stage breast cancer', 'pre-cancer' and 'abnormal cells', terms that led them to believe they had cancer rather than a pre-malignant condition. Several women said they were given conflicting information about their diagnosis by different clinicians, for example their surgeon and their radiation oncologist, throughout their care. Women felt that multiple terms and discrepancy in language between clinicians amplified confusion and misunderstanding of their condition.

Repeating and summarizing information
Several women said they appreciated that their clinician took time to repeat information and to summarize the information discussed at the end of their appointment. They said this helped them feel more comfortable with their clinician and helped to consolidate information.

Guidance with questions
Several women said they were unprepared to know what to ask, making it difficult to engage in discussion, and be an advocate for their needs and preferences. They suggested that information tools or education about what to ask would help them communicate with clinicians.

| Responding to emotions
Nearly all women felt emotional about their diagnosis but many withheld emotions from their physician. Those that did experience an emotional reaction said their physician did not enquire about, acknowledge or offer emotional support, and few were referred to supportive care.

Little response from physicians
Many women conveyed an emotional reaction to their physician.
Amongst those, most said their emotions were not acknowledged. A few said their physician addressed concerns by emphasizing the slow progression to invasive cancer and good overall prognosis, information that women said was important for reducing anxiety.

Women reluctant to express emotions
Several women said they did not convey an emotional reaction to their physician, but provided differing reasons: they did not know if it was appropriate or acceptable to discuss those feelings, they felt uncomfortable sharing those feelings, they were overwhelmed with a DCIS diagnosis, and the emotional reaction was delayed to after the appointment, and they felt guilty for feeling emotional given that clinicians and family said 'they were lucky to just have DCIS' and that 'DCIS was the best cancer to have'.

Little supportive care
Following physician consultation, few women were directed to meet with or were given contact information for a nurse or patient navigator to discuss their concerns. During and following treatment, several women desired psychological support. These women said that during treatment they focused on survival and next steps, while after treatment, when they had time to process what happened, they felt emotional and experienced psychological distress. Women in need of psychological support following treatment reported that physicians did not ask them about emotions during follow-up appointments, and they were unaware of how to access DCIS-specific resources such as a support group or psychological counselling on their own.

Little information about prognosis
Nearly all women had misconceptions about the progression of DCIS to invasive breast cancer, in part because DCIS was described using cancer-related terms (ie pre-cancer) and because they were given little to no information about the likelihood of progression. As a result, women thought they already had cancer or that progression was inevitable, contributing to confusion and anxiety. Two women given brief information about the risk of DCIS progressing to invasive disease said this helped them understand the purpose and high chance of successful treatment.

| Making decisions
Few women reported being engaged by their physician in treatment decision making. They felt obliged to comply with physician recommendations, uninformed about treatment benefits and risks, and frustrated with the lack of information or education to help them to participate in their care.

Little involvement in discussions or decisions
Few women were asked about lifestyle and preferences for recovery, or involved in discussing or choosing treatment. Instead, most women said their physician told them what treatment they would receive, or described treatment options but strongly recommended one option with little rationale or discussion about how that option matched women's preferences.

Uninformed and frustrated
Given no option to participate in discussions or decisions about treatment options, women said they felt obliged to comply with physician decisions or recommendations even if it was not their personal preference. Women felt uninformed about the possible benefits and risks of treatment, which left them frustrated. They emphasized the need for DCIS information and education that would better prepare them for involvement in decisions.

| Enabling self-management
Little information about follow-up or self-care.
Many women described an abrupt termination from interaction or communication with clinicians following treatment, which led to feeling isolated and unsupported. Most women said they were not given information about a follow-up plan, self-care advice or who to contact if they experienced side-effects or other concerns, so they felt unprepared to manage their health and confused about on-going care. A few women were given contact information of a patient navigator or nurse, which they found helpful in addressing concerns following treatment.   57 As noted earlier, due to research ethics board requirements that limited access to demographic information, we lacked certain information such as ethnicity, and the characteristics of 4 participants were unable to be matched to responses. As is typical of focus groups, exemplar quotes are identified only by the focus group location and not by characteristics of individuals; while this may limit readers' ability to distinguish between statements, key findings were consistent amongst women. Here we did not consider clinician experiences; we concurrently interviewed clinicians about PCC for DCIS and will report those findings elsewhere.

| D ISCUSS I ON
Despite these limitations, we transformed findings into tangible recommendations that could be validated and then widely applied elsewhere to improve PCC for DCIS.

| CON CLUS ION
Although previous DCIS research identified persistent patient-clinician communication challenges, this study was the first to compare the experiences of women with DCIS to an established ideal of PCC.
This identified information or behaviour that was present and appreciated, or absent and desired. These experiences were transformed into recommendations, offering clinicians numerous approaches to more consistently engage women and achieve PCC for DCIS by fostering a healing relationship, exchanging information, responding to emotions, managing uncertainty, making decisions and enabling self-management. Future research is needed to continue improving patient-clinician communication by considering a name change for DCIS, and by developing and evaluating information tools that can support PCC.

ACK N OWLED G EM ENTS
Thanks to Bismah Jameel for assistance in analysing interview transcripts.

CO N FLI C T O F I NTE R E S T
None to declare.

DATA AVA I L A B I L I T Y S TAT E M E N T
All data are included in the manuscript and accompanying supplemental files.

I N FO R M E D CO N S E NT A N D PATI E NT D E TA I L S
I confirm all patient/personal identifiers have been removed or disguised so the patient/person(s) described are not identifiable and cannot be identified through the details of the story.