Addressing challenges in information-provision: a qualitative study among oncologists and women with advanced breast cancer

Background There is a need for more insight into how to address challenges of information-provision for women with advanced breast cancer. We aimed to explore oncologists’ and patients’ views on (i) the challenges of information-provision, and (ii) possible strategies to address these challenges, meanwhile (iii) exploring the possible facilitating role of positive expectations and empathy. Methods Semi-structured interviews were held with oncologists (n = 10) and women with advanced breast cancer (n = 14). Principles of Thematic Analysis were followed, with two researchers analyzing transcribed data, supported by Atlas.ti software. Results Taken together the data from oncologists and patients, we found that when communicating with patients with advanced cancer, oncologists face challenges, including handling patients’ unrealistic disease (status) beliefs, and choosing approaches for discussing available treatment options and their side effects. Possible strategies to address these challenges include balancing information with acceptance of denial, and using medical expertise to guide treatment discussions. A sensitive issue is whether to discuss the option of no anti-cancer treatment. Meanwhile, approaches and preferences for discussions of side effects vary. Positive expectations and empathy can facilitate information-provision by creating space and helping patients to open up more. Conclusions Integrating oncologists’ and patients’ views, oncologists can provide realistic information while also, temporarily, accepting denial, and can use their medical expertise to address challenges around unrealistic beliefs and discussion of treatment options. Finding ways to tailor discussions of no anti-cancer treatment and side-effect information are needed. Positive expectations and empathy might facilitate – tailored – information-provision, leading ultimately to patient-centered care lying at the heart of medicine. Supplementary Information The online version contains supplementary material available at 10.1186/s12904-021-00836-w.


Introduction
Good information-provision is fundamental to patientcentered decisions and care, especially when being faced with an advanced cancer diagnosis [1]. When patients feel better informed, they experience more person-centered care [1], i.e. care that is respectful of individual (NKI-AVL), which exempted the study from formal ethical approval (P18LVW). In addition, the Ethical Committee of Leiden University, Psychology Department, approved the conduct of the study. The participating hospital (St Antonius) approved recruitment in their hospital (Z18.031).

Sample Patients
Female patients (> 18 years) with incurable breast cancer; sufficient command of Dutch language; cognitively able to provide consent and be interviewed.

Oncologists
Providing care for women with advanced breast cancer in a Dutch hospital.

Recruitment and procedures Patients
We followed principles of purposeful sampling, aiming a variety in participants' age, disease characteristics, geographical location, education, cultural background.
Participants were recruited -June-Sept 2019 -through the Dutch breast cancer patient advocacy organization and a patient organization for migrant women, involved patient-representatives, snowballing procedures. Via personal contacts and oncologists within the participating hospital we purposefully recruited patients with a non-Western migrant background and/or low educational levels. Patients contacted the research team, who provided more information via telephone and checked inclusion criteria. An information letter/consent form and questionnaire were sent, and interviews were scheduled at patients' homes or at Leiden University. Written consent was obtained pre-interview and the questionnaire collected/completed. Patients were informed they could always stop the interview.

Oncologists
Recruitment occurred via personalized emails, or -for one hospital -via a medical psychologist. Oncologists interested in participating contacted the research team (LV), who provided more information (via email). The information letter/consent form, and questionnaire were sent and the interview was scheduled at the oncologist's hospital or by telephone. Written consent was obtained pre-interview and the questionnaire collected/completed (or sent by post).
Participants were reimbursed only for travel. Transcriptions were offered for comment/corrections.

Topic list
A topic list was created (Additional file 1), in collaboration with patient-representatives. The topic guide focused on i) the challenges of informing patients about treatment options, aims and side-effects; ii) strategies how these challenges can be overcome; iii) the possible facilitating role of empathy and positive expectations in reducing these challenges.

Outcomes Patients
Sociodemographic/ disease characteristics were assessed.

Oncologists
Sociodemographic and professional characteristics, and self-perceived confidence in discussing disease status (treatment aims), options and benefits/side effects in advanced cancer were assessed (self-created 1-4 scale).

Data collection
Interviews were held by one -trained/experienced female -researcher (LV -communication/palliative care/psychology background, or MM -communication/ psychology background), for many interviews both were present.
The audio-recorded interviews were transcribed verbatim, and personal identifiers removed. Data-analysis was part of a cyclical process of data collection and analysis. Data collection was stopped when data saturation was achieved.

Analysis process
Analysis was performed using Thematic Analysis [20]. Firstly, two researchers (LV, MM) (re)read the transcripts to familiarize themselves with the interview data and independently wrote a memo of the most striking findings of each interview (step 1). These memos were subsequently compared and discussed, and initial codes were given to relevant interview fragments (step 2). Using further discussion of memos and initial codes, the two researchers generated themes, which were displayed in a draft figure (step 3). At several points, themes and interim analyses were reviewed and discussed with co-authors (backgrounds in psychology/ medicine/nursing/communication) (step 4). Gradually, themes were further defined and named, and again discussed with co-authors (step 5). Lastly, the results section was written and the research question answered (step 6). Input was received from co-authors, and the final figure, displaying the main themes identified, was drawn. Steps 2-5 were supported by software program Atlas.ti. COREQ guidelines for qualitative research were followed for reporting. Table 1 shows the background characteristics of the 14 patients and 10 oncologists included; Fig. 1 shows the recruitment process.

Themes
From the analysis of oncologists' and patients' data, three main themes were identified, concerning challenges in the discussion of disease status, treatment options, and side effects. Patients often started by mentioning little challenges, mainly focusing on their preferences. Oncologists identified challenges, but considered informing patients a core task. Figure 2 displays themes and possible relations between them.

Challenge 1: How to handle unrealistic disease (status) beliefs
Oncologists mentioned the challenge of handling patients' unrealistic disease beliefs. This focused on patients not expecting or accepting the disease's incurability, and having overly optimistic/pessimistic expectations.

Strategy chosen by oncologists: informing & accepting
To address this challenge, oncologists try to provide information -especially concerning the disease's incurability -and to keep an open dialogue, actively exploring patients' perceptions. Simultaneously, they seem to accept -temporary -denial of the incurability of the disease. If necessary, e.g. with disease progression or if decision-making is hampered, this may be re-discussed.
What we often see in clinical practice is that as a coping mechanism people say "I hear you [that the disease is incurable, red], but I don't want to accept it yet (…). So I'll say (…) you need to know this to make well-informed decisions, but we don't need to keep discussing that you're dying. (4005).

Patients' preferences: informing
Patients stressed the importance of being clearly informed about their disease status; the incurable status is devastating but essential to know.

Challenge 2: How to approach discussing available treatment options
A second challenge involves discussing treatments options, specifically whether to discuss all options or a selection, and whether to include the option of no anticancer therapy.

Strategy 1 chosen by oncologists: medical expertise and selection is duty
Oncologists, though acknowledging patients' right to know all options, seemed to agree that medical expertise and selection is needed. They often select the most effective options (in terms of e.g. efficacy, limited side effects); some select options that differ (e.g. in terms of side effects or hospital visits needed); some actively enquire about patients' priorities/expectations. I generally make a selection. I think most people benefit from your advice; that's why they're there. I generally discuss the most effective treatment (…). If there are two equal options, then you discuss the pros and cons of the different options. (ID 4028).

Patients' preferences: medical expertise and selection is trusted
Patients often expressed faith in oncologists' medical expertise and appreciated them selecting treatment options. Most did not want to carry sole responsibility a Women can receive several treatments, so this does not add up to 100% Still, some women were keen to make their own decisions and/or wanted an oncologist to respect their decisions.

Strategy 2 chosen by oncologists: option of no anti-cancer treatment is a sensitive issue & is used to influence patients
The discussion of 'no anti-cancer treatment' was a sensitive issue. Some oncologists always mention it, as it is a realistic option. Others acknowledged that it was not always a logical option to discuss, especially for young patients with hormone-sensitive tumors. The option of no anti-cancer treatment was explicitly discussed where the burdens of anti-cancer treatment might outweigh the gains (e.g., with older patients, limited prognosis, sole option of chemotherapy). Introducing the option (or not introducing it) was used to influence patients' decision-making.

Patients' preferences: option of no-anti-cancer treatment is a sensitive issue
Patients' -sometimes strongly expressed -views varied on whether this option should be discussed. For some it was a realistic option that should always be mentioned; for others it equaled the end of available treatments. For most, this option was not relevant at that time. They knew, however, that it was an option, which should be discussed in detail later in their disease trajectory (e.g. when fewer options are available, or quality of life becomes impaired).  Challenge: How to approach discussing side effects A last challenge is how to discuss possible side effects.

Strategy chosen by oncologists: different routes to complete information
Oncologists described several approaches, but ultimately favored full side-effect insight. Most oncologists mentioned common and alarming side effects (more would be overwhelming); a few mentioned all possible side effects (to inform the patient fully and protect against later complaints); some always mentioned specific side effects (e.g. nausea). Oncologists considered it important for patients ultimately to be fully informed -possibly through specialized nurses/written information -to make well-informed decisions. The impact of treatments on patients' daily functioning was also sometimes mentioned, but patients' priorities were seldom explored.
We try to mention the most important things. In the case of chemotherapy, they also talk to a nurse who informs them about almost all possible side effects, and often provides the information on paper as well. .

The facilitating role of expectancy
When introducing the topic of positive expectations, patients and oncologists stressed the importance of realism. Still, positive expectations can facilitate addressing the challenges encountered, by influencing decision-making, easing patients' disease burden, and creating space.

Influencing decisions: oncologists
Oncologists spoke about how they use positivity to influence treatment decision-making by highlighting benefits, (dis)advantages, and side effects. For example, potential positive outcomes are stressed early in the disease trajectory, while disadvantages are highlighted when oncologists think it might be better to stop intensive treatments.

Creating space: oncologists
Oncologists seldom explicitly mention that positive expectations can create space, but focus on balancing between discussing potential positive and negative outcomes/side effects.
So I talk about side effects, but immediately add that almost nobody has all side effects, and it varies -from people with almost none to people who do van

Creating space: Patients
Patients focused on how positive expectations can create space. They often mentioned the importance of receiving information about possible positive treatment outcomes and limited side effects. For some this needed to be balanced against potential negative outcomes (more realistic); others preferred a focus on positivity (something to aim for); some acknowledged they realized themselves things might not go well.

The facilitating role of empathy
Oncologists see empathy (see Table 2 for the faces of empathy) as the basis for their communication, while acknowledging that it depends on the patient, situation, and doctor-patient relationship.
It is easier to feel empathy with someone you find likable than someone who actually evokes irritation. (4018).

Oncologists
Oncologists did not always find it easy to cite concrete examples of how they demonstrate empathy. Still, they did sometimes mention examples of empathic behavior. Firstly, they could think things through with the patient, but from a medical perspective (e.g., suggesting that a daughter get married earlier so her mother could still attend). Secondly, they could reassure the patient that they would not be abandoned (e.g., telling patients that the medical team would do their utmost). Thirdly, they could state how sorry they feel for patients

Patients
Patients spoke in detail about the different forms of empathy oncologists could express, based on realistic foundations. Firstly, they highly appreciated the oncologist thinking things through with them from a medical and a practical perspective: for example, enquiring about the patient's home situation and whether they need practical help, or trying to think about the best treatments in line with the patient's preferences

Right at the start our oncologist asked why we didn't have home help. (…) So the fact that a doctor comes back to it like that, and says 'think about it -you're entitled to it' (…) -that' s really great. But that' s what empathy is -thinking with the other person and imagining what you would feel yourself. (3018)
Secondly, they appreciated it if the doctor showed an interest in the patient and took them seriously, for example sincerely enquiring how patients and their loved ones were doing, asking about specific events such as holidays, considering patients' thoughts, preferences, or symptoms seriously We went to see him, and just after the diagnosis my husband got a tattoo, and he noticed. One time he was in the middle of a conversation, then he looks at my husband, and says "hey", "you didn't have that tattoo last time", he says. And those are the kinds of things I think -oh, he sees. And  Lastly, they did not seem to expect oncologists to provide specific psychological assistance, which they sought from other sources, such as specialized nurses, psychologists, or fellow patients van Vliet et al. BMC Palliat Care (2021) 20:142 Patients see expressions of empathy as important, but with a firm medical basis: the oncologists' medical expertise is paramount. A lack of empathy was perceived as hurtful.
Let's say [the medical part, ed.] 75%, and the personal part 25%; asking how I'm doing, how things are at home (…). And it's not strictly necessary, because basically I'm there for my disease and not to make friends. (3034).
However, although this is not mentioned as explicitly as for expectancy, oncologists' expressions of empathy may facilitate the process of addressing the challenges encountered, by helping patients to open up (e.g. about their thoughts, feelings, priorities, personal situation), thus allowing information and care to be tailored to their needs.

Helping patients to open up and tailoring information and care: oncologists
Some oncologists mentioned that expressions of empathy can lead patients to open up and confide their priorities. This in turn may facilitate the provision of person-centered information and -treatment -care.

Discussion
This study aimed to explore oncologists' and patients' views on challenges of providing information to women with advanced breast cancer, and possible strategies to address these challenges, meanwhile exploring the possible facilitating role of positive expectations and empathy, with the ultimate aim to come to patient-centered care. Integrating oncologists' and patients' views, we observed that oncologists face challenges regarding handling unrealistic beliefs, and regarding choosing how to discuss treatment options (including no anticancer therapy) and possible side effects. Strategies to address these challenges include balancing informationprovision with acceptance of denial, and using medical expertise to guide treatment discussions (though discussing the option of no anti-cancer therapy remains a sensitive issue). A variety of approaches and preferences for discussing side effects exists. Positive expectations and empathy can facilitate information-provision byamongst others -creating space and helping patients to open up.
In general, oncologists reported more challenges in information-provision than patients. While patients are increasingly involved in agenda-setting [21], oncologists bear the responsibility for explaining complex medical information in a manner patients can understand [22]. This imbalance sheds light on the challenges and also strategies being formulated from the oncologists' viewpoints while they derived from both oncologists' and patients' data.
A first main challenge that arises in information-provision is handling patients' unrealistic disease beliefs, mainly about the diseases incurability. While patients stressed the importance of realism, oncologists also leaned towards accepting denial. Previous studies have found that patients place great importance on realism [23][24][25]. Simultaneously, denial of a life-threatening diagnosis occurs in 4-47% of patients, can be temporary [26], and can serve as an adaptive coping mechanism [27]. The strategy endorsed by clinicians in our study (and beyond [28]) -accepting temporary denial after providing realistic information -may be the best way to approach unrealistic beliefs.
A second core challenge is which treatment options to discuss: all or a selection. Patients and oncologists both mentioned that medical expertise is essential for selecting treatment options, while individuals held strong views on whether the option of no anti-cancer therapy should be mentioned. Previous research has found that oncologists want to discuss "best options" [29] -not always including no-treatment [7,30] -while patients have faith in oncologists' treatment recommendations [12,29,[31][32][33]. This seems to contradict legal requirements [34][35][36] and guidelines stressing the importance of mentioning all available treatment options [37], including solely optimal supportive care [22]. Perhaps such guidelines overlook patients' need for medical guidance, and the emotional impact of raising the option of no anti-cancer therapy. In an era of increased focus on patients' responsibility, we should not overlook the sensitivity of discussing no anticancer treatment, and the importance of medical expertise in guiding patients through difficult, uncertain times.
A last challenge, with no clear solution, seems to be how to discuss potential side effects. Patients and oncologists agreed that alarming attention-requiring side effects should be discussed; however, while patients varied in their preferences regarding additional information on side effects, oncologists favored complete informationprovision. Given the ethical and legal requirements for "informed consent" [35][36][37] to be based on full information and insight, oncologists' perspectives are understandable. Some previous studies have found patients wishing to receive more [1,38] and not too much [33] information on side effects. Our study suggests that above all information on serious side effects is appreciated. Whether mild/nonspecific side effects should also always be discussed remains unanswered. Moreover, the variety in patients' preferences regarding the discussion of side-effects (and treatment options), once again highlights the importance of adjusting information to each individual patients' needs and preferences, in order to come to patient-centered care. In order to tailor information, oncologists have been advised to ask patients about their information-preferences [39].
Next, we also explored the roles of positive expectations and empathy in facilitating information-provision. For patients, positive expectations might provide hope, as stressing potential positive outcomes and treatment options has previously been described as hopeful [12,24,25]. For oncologists, who seem regularly to mention possible positive treatment outcomes [40], stressing potential advantages or disadvantages can serve as a tool to influence decision-making, as also previously found [30]. In this earlier study, oncologists acknowledged to sometimes provide information regarding hams and benefits in line with their preferred (treatment) option. It remains to be determined whether, as suggested in our study, positive expectations can ease disease burden in advanced cancer; positive effects on non-cancer symptoms have been described [13,14] while it might also improve coping and thereby symptom burden [41].
Where empathy is concerned, some oncologists and patients agreed it can prompt patients to share personal preferences and information, which oncologists can use to tailor information and care plans. In this regard, we could speculate that the trust patients placed in oncologists' treatment plans may also have originated from empathy. Relationship-building and information-provision are often seen as distinct elements of the medical encounter [42,43], but our study seems to question this. This view is supported by previous findings demonstrating that empathy can facilitate information-processing and improve patients' recall [16][17][18]. Providing empathy need not be time-consuming [44,45], with studies demonstrating that effective empathy can be achieved in less than 40 s [16,44]. It is a powerful, and often under-used [45], tool oncologists can use to make patients feel better [46,47] and optimize information and care.
Our study has strengths and limitations. strengths mainly concern the often overlooked focus on challenges in information-provision and the dual focus on both patients' and oncologists' perspectives. Limitations mainly concern the generalizability of results beyond our study sample. Despite various attempts to include women with nonwestern migrant backgrounds and/or low educational level, mainly high-educated Caucasian women participated. Second, oncologists with a specific interest in communication might have participated, biasing our results.
Future studies might focus on how to tailor and match individual patients' preferences -specifically on discussing the option of no anti-cancer treatment -with oncologists' information-provision approaches. Assessing patients' information needs pre-consultation, as one oncologist suggested, might help. More insight is needed into how to inform patients about potential side effects in a way that is tailored to individuals' preferences while adhering to information-provision obligations, and without eliciting nocebo effects. In addition, we encourage future studies to be more culturally and health literate diverse, and to include males and other cancer types, as these variables might influence communication needs [48][49][50][51].

Conclusions
Integrating patients' and oncologists' views, oncologists can provide realistic information while also -temporarily -accepting denial, and can use their medical expertise when addressing challenges around unrealistic beliefs and the discussion of treatment options. Finding ways to tailor discussions of no anti-cancer treatment and sideeffect information are needed. Positive expectations and empathy might facilitate -tailored -information-provision, leading ultimately to patient-centered care at the heart of medicine.