Design

We conducted a qualitative study with semi-structured interviews to explore oncology professionals’ views and expectations regarding cardiac surveillance in BC patients with a high cardiovascular risk. The consolidated criteria for reporting qualitative studies (COREQ) checklist was used to ensure complete reporting of methodology. A waiver was provided by the Medical Research Ethics Committee of Arnhem-Nijmegen because the study did not need an ethical review. The study was conducted in accordance with the principles of ICH Good Clinical Practice, applicable privacy requirements, and principles of the Declaration of Helsinki.

Participants and recruitment

A purposive sample with maximum variation in gender, work experience, and hospital type was selected with the aim to reflect the true variation in characteristics observed in clinical practice. Twelve oncology professionals specialized in BC care participated in this study: oncologists (N = 6), a cancer epidemiologist (N = 1), and oncology nurse practitioners (N = 5). In this paper, oncology professionals are referred to as professionals, unless otherwise specified. The professionals worked at the medical oncology department in either a university or general hospital. They were selected after consulting the head of the respective oncology departments. Eligibility was based on their experience in BC care: a minimum of 1 year in their current function. The coordinating investigator contacted eligible professionals (N = 16) from seven different hospitals via phone and invited them to participate in this qualitative study. Twelve professionals (75%) agreed to participate. Four professionals were unwilling to participate: one did not have any experience with cardiovascular diseases in BC patients, whereas the other three declined owing to logistic reasons.

Data collection

A semi-structured interview guide was developed, theoretically based on the seven domains of the Tailored Implementation for Chronic Diseases (TICD) checklist (Table 1), which is a synthesis of 12 existing checklists for identifying determinants of practice and factors that prevent or enable improvements in healthcare professional practice [14].

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Table 1. Interview topics.

https://doi.org/10.1371/journal.pone.0249067.t001

The interview guide was repeatedly reviewed by all investigators to ensure the feasibility and completeness of the topics; it consisted of open questions regarding clinical protocols, awareness, multi-disciplinary collaboration, organizational structure, and resources (S1 File). All interviews started with the same opening question about clinical protocols for cardiac surveillance in BC patients. All seven TICD domains were discussed. During the interviews, summaries, probes and prompts were used to ensure correct interpretation of professionals’ perceptions and encourage outspokenness [15].

Individual face-to-face interviews were conducted in a private room at the hospital where the participant was employed. Baseline characteristics were collected after informed consent was obtained and before the interview began. The interviews were conducted by a 35-year-old, independent, female health sciences student (MSc) with 2 years of work experience in the field of oncology (author LD). The interviewer was unknown to the professionals, which allowed them to express their experiences and perceptions without inhibitions. All interviews were conducted in Dutch, all quotes were translated to English with the forward backward procedure for translation reliability.

The interview duration ranged from 21 to 64 min (median: 36 min). The interviews were audio-recorded, transcribed verbatim, and checked for transcription errors. Field notes were made immediately after the interviews to record observations, capture initial ideas on the topics, and reflect on the methodology (e.g., interview guide refinement). Interview techniques were practiced with a simulation interview to enhance the interview skills and obtain feedback from more experienced researchers.

Data analysis

Thematic analysis as outlined by Braun and Clarke was used, an inductive, semantic and realist approach was applied. Thematic analysis consists of six steps: familiarizing with the data, generating initial codes, searching for themes, reviewing themes, defining and naming themes, and writing (Table 2; [16]). The supplementary 15-point checklist ensured the correct use of the thematic analysis method.

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Table 2. Six steps of thematic analysis.

https://doi.org/10.1371/journal.pone.0249067.t002

The first four interviews were coded by three researchers independently of each other and subsequently checked for inconsistencies and similarities; the remaining interviews were coded by two independent researchers. Inconsistencies were discussed in analysis meetings with the research team. After the first three interviews, the analysis step “searching for themes” was performed. After the remaining interviews, each theme was further considered and refined; illustrative quotes were also selected. Data saturation was defined as the point where additional interviews did not lead to any codes that introduced a new topic, which was reached after ten interviews. Two more interviews confirmed saturation and ensured maximum variation in the sample.

After transcribing the interviews, 740 codes were generated and grouped in 32 clusters, such as multidisciplinary collaboration, continuity of care, burden, need for knowledge, urgency, logistics, awareness, personalized care, research, visibility of late cardiac effects, and cost effectiveness. The recurring themes within these clusters were discussed to identify the final themes to answer the research question.

Regular data collection and analysis meetings were scheduled with the interviewer and experienced researchers, which resulted in researcher triangulation and peer review in all phases of the study; this enhanced the methodological quality, reliability, data dependability, and accuracy [15, 17, 18]. Additionally, an audit trail improved the confirmability of the study [15]. Data management was supported by ATLAS.ti software (version 8; Scientific Software Development GmbH, Berlin, Germany).

Current practice

Most oncology professionals (N = 10; 83%) stated that cardiac surveillance for BC patients is not structurally performed in their hospital. The majority of professionals (N = 10 [83%]; from 5 out of 7 [71%] hospitals) disclosed that cardiac monitoring focused on the performance of a multigated acquisition (MUGA) scan for the assessment of the LVEF prior to and during trastuzumab treatment for HER2⁺ BC patients. Patients receiving other (high-risk) cardiotoxic treatments did not receive any form of cardiac surveillance unless it was clinically indicated owing to the development of cardiac symptoms or patients already received it owing to pre-existing cardiovascular comorbidities. Only two professionals from two different hospitals mentioned the recent implementation of a cardio-oncology referral department for cancer patients receiving high-risk cardiotoxic treatment. At these dedicated cardio-oncology outpatient clinics, cardiovascular risk stratification and cardiotoxicity monitoring during cancer treatment are performed. Notably, all professionals indicated that strict clinical protocols (based on guidelines) for the detection of cardiotoxicity during and after cancer treatment are lacking.

Sense of urgency

All professionals were aware of the cardiotoxic effects of anthracycline- and trastuzumab-based regimens. They all clarified that their delivery of cardiac surveillance was mainly driven by their sense of (or lack of) urgency; they did not perform any form of cardiac surveillance mostly because they did not recognize the advantages.

The assumed low incidence of cardiac events in their patient population was the main cause and played a key role in the professionals’ clinical decision making. Oncologists indicated that they rarely treated BC patients with CTRCD; therefore, they perceived the occurrence of (adverse) cardiac events during cancer treatment as rare. Additionally, a reduction in LVEF was considered as reversible and therefore not important to detect using cardiac imaging.

“I can’t remember anyone from recent years who I referred to a cardiologist, no one who expressed complaints that could be of a cardiac nature and then came back with heart failure. And that could mean two things: either those patients weren’t there, or we haven’t searched properly.” (P6)

Most professionals did not feel the need to change current practice regarding cardiac surveillance despite the increasing awareness on cardiotoxicity among specialists.

“I remember a patient–she really had heart failure. The question is, if we had done things differently and screened the patient before cancer treatment, we probably couldn’t have prevented it anyway. So, in that case, I believe we’re still doing everything as we should, and we don’t have to change anything, but yes, that one patient–if I may say–was very unlucky. It did have a large impact; yes.” (P12)

Most professionals were not convinced that increased cardiac monitoring can prevent CTRCD or improve quality of life. Those in favor of cardiac monitoring mentioned their colleagues’ lack of knowledge on the topic as a barrier. Similarly, the perception of oncologists that cardiology waiting lists are usually long prevented them from referring their patients for cardiac screening because they feared this would significantly delay cancer treatment. Some oncologists disclosed that cardiac monitoring in cancer patients was not a priority for cardiologists because of anticipated poor cancer prognosis.

“When we say, ‘cancer patient’, the patient’s prognosis is not always correctly interpreted by cardiologists. It quickly sounds like, ‘It’s cancer. We don’t have to proceed with monitoring quickly because the prognosis is already limited.’ But that’s exactly the question. Obviously, this is true sometimes, but there are also situations in which we expect patients to have many more years to go; I feel [that] it sometimes influences a cardiologist’s advice too much.” (P10)

All professionals agreed that increased knowledge of CTRCD, improved awareness of all involved disciplines and practitioners, and more proactive and preventive behavior are important. Knowledge, experience, or patient stories may result in an increased sense of urgency of professionals regarding cardiac surveillance.

“And then, I had a patient with severe cardiac damage, and she told me, ‘It was completely not recognized at all, my cardiac complaints.’ She was in tears. Now, I recognize how important it is to properly inquire about potential [cardiac] complaints.” (P4)

Multidisciplinary collaboration

Multidisciplinary collaboration between oncologists and dedicated cardiologists highly influenced the manner in which cardiac surveillance was organized. Two oncologists involved in multidisciplinary cardio-oncology collaboration acknowledged that this facilitated communication and resulted in more structured cardiac surveillance in BC patients.

“For us, the logistics are now very easy; we have one contact person, someone who evaluates the risks of a patient […]. Sometimes we felt MUGA results were not sensitive enough. Now [with echo], we know more and are able to make well-thought-out decisions […]. Follow-up is every three months unless it is indicated to schedule it earlier.” (P11)

Multidisciplinary collaborations were often initiated after combined research projects and were implemented by dedicated professionals, both in oncology and cardiology, who have intrinsic motivation and a mutual interest in improving (cardiovascular) clinical outcomes of cancer patients.

“I see that most things are only achieved when a few people start collaborating. That is the way it works. It often starts with research collaborations.” (P8)

All professionals perceived multidisciplinary cardio-oncology collaboration as an important asset in delivering holistic care that takes into account patients’ mental, physical, and social well-being.

“I am always very medically involved, and the nurse, in my opinion, sees the patients and their [social] system. And I think that the nurse can offer a whole package, more than I can.” (P11)

Professionals without an established cardio-oncology department (N = 10; 83%) revealed that they refer their BC patients to a cardiologist only when the patients have a history of cardiac events. Many of these professionals perceived occasional consultation with a cardiologist as sufficient, given that they considered CTRCD as a rare complication. As such, they believed that multidisciplinary collaboration is not necessary nor recommended in the literature.

“There is no standard collaboration; [it occurs] only in acute situations. It’s just not a frequent complication. But then again, with that last patient [with cardiac damage], well, sometimes not all specialists completely understand or know what kind of treatment we use. I think it’s too easy to assume that cardiac damage during treatment is related to that treatment. It’s sometimes not clear […]. There is not enough evidence to initiate something or to structurally collaborate. At least we haven’t done that so far, and it’s also not in the guidelines.” (P7)

Patient burden

Professionals considered the occurrence of CTRCD as rare and therefore choose to limit informing patients regarding cardiotoxicity risk in an effort to “unburden” them. They stated that they want to avoid overwhelming their patients with extensive information on possible cardiac side effects before the start of essential or even life-saving cancer treatment. Moreover, they felt conflicted in disclosing complications they perceived as rare. Professionals also believed that patients are not very concerned about their cardiovascular health when first diagnosed with BC and also not during or after cancer treatment because staying alive is assumed to be considered of higher importance after a cancer diagnosis.

“It was just never a reason to give a different treatment. You just explain it. Patients are not very concerned with it [potential cardiac damage]. They are more like, ‘Do I need to go to a cardiologist? Ok then’ but never concerned about their cardiac function. But, of course, we don’t know what they’re thinking when they’re at home.” (P11)

Nonetheless, all professionals emphasized that quality of life after cancer treatment is an important topic to discuss with patients. They explained that long-term effects should be considered more often during patient counselling.

“Actually, I think we all want the same thing, which is keeping patients alive. But especially with a good quality of life. We don’t do that if we cure patients of cancer but then they die because of heart failure. If that’s the case, we did something drastically wrong or, at least, not as we’d wish. In that case, we should learn from this and do something about it.” (P6)

Continuity of care, both during BC treatment and during follow-up, was considered essential to unburden patients. Patients being assessed by different cardiologists during consecutive consultations was perceived by professionals as a negative aspect of cardiac care. Most professionals did not feel the need for patients to regularly visit different healthcare specialists involved in the care process (e.g., surgeon, radiotherapist, and cardiologist). Specifically, nurse practitioners underlined the importance of a familiar face for patients, and they recommended healthcare coordination via one professional to improve healthcare quality and accelerate decision making.

“Patients were seen by so many specialists, and then they returned to me. And I was like, ‘What was the additional value of all these separate visits?’ […] It’s good to get to know patients, coordinate their trajectory, monitor [them] more easily, and notice when something is going wrong […]. It’s good for the continuity we offer if I’m the main contact, then you’re more like ‘When was the last echocardiography? We need to request a new evaluation.’” (P5)

Nurse practitioners stated that continuity of care for BC patients has added value and perceived their involvement in the care process, from start to finish, as a strength. Continuity supports nurse practitioners in delivering personalized care. Health changes can be more easily detected, and health education can be tailored to patients’ needs.

“That is the advantage of knowing people, that you don’t just check things off your list. But you’re more like, ‘Who do I have in front of me and to what extent does each aspect [of complaints and health] need attention?’” (P5)

Practical tools for cardiac surveillance

All professionals acknowledged the need for practical tools in delivering cardiac surveillance for BC patients. They also underlined the need for clinical protocols and guidelines for cardiac surveillance, with a focus on risk stratification, to distinguish between high- and low-cardiovascular-risk patients and tailor cardiac surveillance accordingly. Oncologists stated that it is difficult to recognize CTRCD without proper knowledge.

“It would be great if we knew, for breast cancer, if we could identify when someone has a reduction in LVEF during treatment or shows certain specific cardiac complaints or has a risk profile. That you would know that this is a high-risk patient I need to follow up for the next four to five years.” (P11)

Most professionals expressed the need for evidence-based guidelines for cardiac surveillance and their structured implementation in current clinical practice.

“I really think you need to make a guideline for this [cardiac surveillance]. Not everyone should just start doing things. We need to prevent an abundance of initiatives without proper support from a guideline.” (P8)

Oncologists disclosed a knowledge gap regarding the necessity for cardiac surveillance, which is mainly due to a lack of data on long-term benefits and cost effectiveness.

“There is always a number-needed-to-harm and a consideration on how many patients are burdened by failed medical activities versus the benefits. That is an important question.” (P3)

All professionals shared the opinion that changes in healthcare practice should be evidence based and require an initiative from professionals themselves.

Implications for practice

• Knowledge of cardiotoxic effects and possibility of early detection is essential to reduce long-term cardiac damage.
• Oncology professionals express a need for structured clinical protocols to provide cardiac surveillance based on recommendations for all high-risk BC patients.
• Multidisciplinary collaboration between the cardiology and oncology departments is important to structure and coordinate cardiac surveillance for BC patients, and collaborative research projects can catalyze this process.