Effective communication in palliative care from the perspectives of patients and relatives: A systematic review

Objectives. In palliative care, effective communication is essential to adequately meet the needs and preferences of patients and their relatives. Effective communication includes exchanging information, facilitates shared decision-making, and promotes an empathic care relationship. We explored the perspectives of patients with an advanced illness and their relatives on effective communication with health-care professionals. Methods. A systematic review was conducted. We searched Embase, Medline, Web of Science, CINAHL


Introduction
Palliative care should be aligned to the needs, goals, and preferences of patients and their relatives. For many patients and relatives, it is important to retain (a certain degree of) control over care. Health-care professionals can only provide appropriate care at the appropriate moment if they are aware of the needs and preferences of those involved (Hoare et al. 2015;Shin et al. 2016; Steering Committee for Appropriate End-of-Life Care (RDMA) 2015; Stegmann et al. 2021). Patients and relatives should be confident that goals and preferences discussed with a health-care professional are known throughout the care process (Back 2020;den Herder-van der Eerden et al. 2017; Van Vliet and Epstein 2014). This requires continuous effective communication between health-care professionals and patients and their relatives, because needs, goals, and preferences can change during a disease trajectory (Bergqvist and Strang 2019;Hwang et al. 2015;Shin et al. 2016). Health-care professionals from all disciplines and professions providing palliative care, both generalists and specialists, should therefore have adequate communication skills.
In the Netherlands Quality Framework for Palliative Care (Boddaert et al. 2017), which is based on international literature and guidelines (Hospice New Zealand 2012; National Coalition for Hospice and Palliative Care 2013; National Institute for Health and Care Excellence (NICE) 2011; Palliative Care Australia 2005), effective communication is defined as "a structured process between patient and healthcare professional in which bilateral information exchange and equality -with respect for the dependent position of the patient -are the basis. "

Search strategy
The search strategy was based on PALETTE, the "Palliative cAre Literature rEview iTeraTive mEthod, " a method to develop search strategies in literature reviews on palliative care focused on complex concepts, such as effective communication (Zwakman et al. 2018b). We combined different information retrieval techniques, such as contacting experts, a focused initial search, pearl growing (Schlosser et al. 2006), and citation tracking (Papaioannou et al. 2010;Schlosser et al. 2006). An initial search and consultation of experts resulted in a set of 7 "golden bullet" articles. The search strategy was further developed in Embase in collaboration with an information specialist from Erasmus MC, University Medical Center Rotterdam, and optimized in an iterative validation process. Keywords were added until all 7 "golden bullets" were identified. The final search was carried out on March 4, 2021 using 5 databases: Embase, MEDLINE (Ovid), Web of Science, Cochrane, and CINAHL (EBSCOhost) (see Supplemental file 1 for search terms).

Inclusion and exclusion criteria
We included articles that met the following criteria: the article described an original empirical study on effective communication between patients and/or relatives with health-care professionals; the study assessed the experiences of patients diagnosed with advanced illness and/or their relatives; the article was published in English between January 1, 2015 and March 4, 2021. We chose the year 2015 as starting point, because from that time a growing patient-centered focus was found in studies on communication in palliative care (Bensing et al. 2013;De Boer et al. 2013). Studies on communication conducted in non-Western countries, in pediatric palliative care and review articles were excluded.
We started with screening titles and abstracts, and the next step was screening based on full-text articles. All steps were performed by 4 researchers using EndNote X9 (Bramer et al. 2017). Differences in the selection of potentially eligible articles were resolved by mutual agreement. When in doubt, an article was reviewed for its full text.

Data extraction and analysis
We developed a data-extraction form that included the aim of the study, the study setting, the study design, the study population, the method of data collection, and the results of the study. Data extraction was performed by 2 researchers (M.E. and M.K.).
Since the research question appeared to be addressed by studies with both qualitative, quantitative and mixed-methods research designs, we took a convergent integrated approach to synthesize and integrate the findings (Stern et al. 2021). First, a conceptual overview of the results relevant to the review question was made of each article. In this conceptual overview, we transformed quantitative findings from included studies into a qualitative description. Second, based on the overviews of articles published in 2020 and 2021 (n = 17), a first thematic structure to synthesize study results was developed. Third, remaining articles were then placed along this preliminary structure and if necessary or desirable, themes were added or existing themes were merged. This resulted in the final structure.

Quality assessment
The quality assessment of included articles was performed independently by 2 researchers (M.E. and M.K.). Qualitative articles were assessed using the COnsolidated criteria for REporting Qualitative research (COREQ) checklist (Tong et al. 2007). Observational studies were assessed using an adapted version of the Cochrane risk-of-bias instrument, which was based on the Cochrane Bias Tool for intervention studies (Fahner et al. 2019;Higgins and Green 2011;Sondaal et al. 2016). Randomized controlled trials were assessed using the Cochrane tool for assessing risk of bias in randomized trials (Higgins et al. 2011). Given the exploratory nature of this systematic review, all articles were included in the analysis (Dixon-Woods et al. 2006).
An overview of the characteristics of the studies is presented in Table 1.
A classification of the included studies by study design, country, care setting, perspective studied, diagnosis, and method of data collection in addition to the characteristics in Table 1 is presented in Supplemental file 2.
In our quality assessment, for trials (n = 4) the median quality score was 4.5 out of 7 (range, 1-5). There was no blinding of the participants in any of the trials. For observational studies (n = 7) and the quantitative parts of mixed methods studies (n = 4), the median quality score was 3 (range, 0-7). For qualitative studies (n = 41) and for qualitative parts of mixed methods studies (n = 4), the median quality score was 18.0 out of 32 (range, 4.5-21.5). A detailed presentation of the quality assessments by the researchers is provided in Supplemental file 3.

Perspectives of patients and relatives
We identified 7 themes that from the perspectives of patients and relatives are important for effective communication in palliative care. A summary of our findings is presented in Table 2.

Open and honest information
Many patients wanted to be informed openly and honestly about their situation, including their diagnosis, disease, condition, treatment, side effects, disease course (metastases), and prognosis (Abdul-Razzak et al. 2016;Brom et al. 2017;Goebel and Mehdorn 2018;Masefield et al. 2019;Rohde et al. 2019;Seccareccia et al. 2015;Villalobos et al. 2018). In a few studies, patients stated that they also appreciated to be rapidly informed of results of diagnostic examinations (Goebel and Mehdorn 2018;Rohde et al. 2019;Seccareccia et al. 2015).
Several articles describe the impact of open communication. Some studies show that patients' satisfaction with communication improved when they could openly talk about the details of the disease, prognosis, or the dying process (Curtis et al. 2018;Houben et al. 2015). Open communication contributed to a stronger connection (rapport) between patient and health-care professional, which increased patients' trust (Abdul-Razzak et al. 2016;Fenton et al. 2018;Freytag et al. 2018;Paladino et al. 2020). In addition, some patients experienced more control and thus a stronger feeling of safety: being well informed about treatment options enabled them to make well-considered treatment or care decisions (Brom et al. 2017;Chen et al. 2021;Epstein et al. 2017;Paladino et al. 2020). The relationship between open communication and perceived safety was also demonstrated by the experiences of patients who (partially) missed open information. Several studies show that patients felt isolated when they had the impression that health-care professionals did not inform them adequately (Hilário 2020;Kitta et al. 2021;Rohde et al. 2019). Patients indicated that open and honest communication could help them to be better prepared to make informed decisions (Masefield et al. 2019).
When it came to feeling invited and safe to share their needs and concerns, the experiences and needs of relatives were broadly similar to patients (Ahmed et al. 2015;Caswell et al. 2015;Gilad et al. 2022;Ibañ ez-Masero et al. 2019;Kim et al. 2018;Masefield et al. 2019;Steinhauser et al. 2015). However, there were also differences between the needs and preferences of relatives and patients. Although relatives might also struggle with coping with open and honest information and might also need to hold on to hope (Applebaum et al. 2018), they generally indicated having a greater need for information than patients (Applebaum et al. 2018;Masefield et al. 2019). To provide optimal care and to be prepared for future care needs, relatives indicated that they needed timely, detailed prognostic information or information about the process of dying (Ahmed et al. 2015;Awdish et al. 2017;Bauman et al. 2018;Caswell et al. 2015;Cohen-Mansfield et al. 2017;Collins et al. 2018b;Im et al. 2019;Krawczyk and Gallagher 2016;McGinley and Waldrop 2020;Seccareccia et al. 2015;Steinhauser et al. 2015).

Aligning to the process of uptake and coping with information
Although many patients expressed a desire for open and honest communication, many studies also show that patients often found it difficult to cope with information about their deteriorating health (Abdul-Razzak et al. 2016;Goebel and Mehdorn 2018;Ibañ ez-Masero et al. 2019;Im et al. 2019;Masefield et al. 2019;Rohde et al. 2019;Seccareccia et al. 2015;Shen et al. 2020;Weerasinghe and Maddalena 2016). There were many potentially defining moments in the palliative trajectory that could be threatening, such as being diagnosed with a severe illness, the failure of treatment, the transition from curative to palliative or comfort care, transfer to another care organization, etc. (Collins et al. 2018a;Goebel and Mehdorn 2018;Hilário 2020;Hjelmfors et al. 2018;Im et al. 2019;Kitta et al. 2021;Kvåle et al. 2020;Masefield et al. 2019;Melis et al. 2021;Netsey-Afedo et al. 2020;Pini et al. 2021;Schulman-Green et al. 2018;Schulz et al. 2017;Tavares et al. 2020;Villalobos et al. 2018). Although patients indicated that they preferred open and honest information about these topics, such information confronted patients with their deterioration, their "running out" of treatment options and thus with the threat of increasing dependence and the approaching end of life. This could result in fear, stress, and existential disruption, inducing feelings of insecurity and loss of control. For many patients who thought they were willing to face their end of life and the series of decisions that came with it, arriving at the moment where they had to do so turned out to be a heavy task Krug et al. 2021;Masefield et al. 2019;Netsey-Afedo et al. 2020;Pini et al. 2021;Rohde et al. 2019;Schulz et al. 2017). This tension between wanting to be openly informed and feeling safe, and how patients and relatives found their way in this, looked different for each patient and relative. Some patients were open for detailed information about end-of-life issues while others indicated that they preferred to stay away from the discussion about their prognosis or future care (Bergenholtz et al. 2020;Hjelmfors et al. 2018;Kirby et al. 2018;Krug et al. 2021;Schulman-Green et al. 2018;Seifart et al. 2020;Shen et al. 2020). This required customization and a person-centered approach. Patients preferred the physician to assess which and how much information they appreciated (Abdul-Razzak et al. 2016;Bergenholtz et al. 2020;Goebel and Mehdorn 2018;Lin et al. 2018). Patients and relatives stated that they sometimes found it difficult to ask for more information: they often did not know what to ask and liked to be explicitly invited to ask questions during or after a conversation with a health-care professional (Awdish et al. 2017;Collins et al. 2018a;Goebel and Mehdorn 2018;Kitta et al. 2021;O'Connor et al. 2020).
Patients indicated that they needed time to process the information provided (Abdul-Razzak et al. 2016) and wanted health-care   Voruganti et al. 2018). Continuity of health-care professionals prevented patients from having to tell the same story over and over again, but also facilitated a human connection, that could appeal to health-care professionals' sense of responsibility and commitment (Brom et al. 2017;Middleton-Green et al. 2019;Voruganti et al. 2018

Recognition of relatives in their role as caregiver
In several studies, relatives emphasized that patients often largely relied on their caregiving and that they considered themselves the backbone of the patient's support system. Many felt heavily burdened and believed that their role as caregiver deserved explicit attention and recognition from health-care professionals (Masefield et al. 2019;Washington et al. 2019). Patients and relatives indicated that health-care professionals should take time to "really" listen to their concerns and needs and where possible provide personalized support (Awdish et al. 2017;Caswell et al. 2015;Collins et al. 2018b;Masefield et al. 2019;Seccareccia et al. 2015;Steinhauser et al. 2015). Sometimes, the relative felt the need to protect the patient from threatening information, for example about the prognosis, so that the patient continued to have hope (Melis et al. 2021) and did not suffer too much from knowing the truth (Ibañ ez-Masero et al. 2019; Weerasinghe and Maddalena 2016). Although this could be the case especially in non-Western cultures, relatives indicated that they preferred to receive understandable information themselves to be able to care for their family member (Weerasinghe and Maddalena 2016). Applebaum et al. (2018) found that relatives did not ask their own questions out of respect for the patient, who might not want to know everything. On the other hand, some patients indicated that they preferred to keep relatives not informed, especially if the disease progressed and the burden or fear and worry of the relatives might increase Melis et al. 2021). Relatives indicated that the key to open communication lied with the health-care professional, she/he could set the example (Ibañ ez-Masero et al. 2019).

Discussion
The aim of this systematic review was to synthesize existing knowledge about the perspectives of patients with advanced illness and their relatives on effective communication in palliative care. We found that many patients and relatives wanted to be informed openly and honestly about their situation and that this brought a feeling of security. However, patients and relatives also wanted health-care professionals to align to their process of uptake and coping with information, because honest information also could induce fear, stress and existential disruption. For effective communication, patients and relatives further indicated that they preferred the following elements: empathy, clear and understandable language, leaving room for positive coping strategies, committed health-care professionals taking responsibility, and recognition of relatives in their role as caregiver.
Our study brings to light that the dynamics of patients and relatives in communication with health-care professionals have their own process, and that health-care professionals must align with this process. Guidance of patients and relatives in their process over time is important, while research on communication by health-care professionals is often done once after, for example, a communication training program in a following conversation with a real or simulated patient (Selman et al. 2017). Our finding that for patients and relatives the informative side was inextricably linked to the empathic side of communication underlines the findings of a recent systematic review of Van der Velden et al. (2020). Their systematic review on the effect of prognostic communication on patient outcomes in palliative cancer care showed the benefit for most patients of explicit information in combination with empathic communication strategies by health-care professionals, although literature studying longer-term outcomes of prognostic communication was limited (Van der Velden et al. 2020). Westendorp et al. (2022) found that patients considered a lack of empathy in the communication by the oncologist as potentially harmful whereas they considered the exploring of patient's needs and preferences by the oncologist as helpful communication. Our review emphasizes that patient-centered communication is essential for high-quality palliative care. Such awareness should be expressed by physicians as well as nurses in planned or goal-directed communication, but also in unplanned communication.
We also found that patients and relatives preferred a proactive attitude from health-care professionals. However, numerous studies show that physicians often feel hampered in discussing prognosis and palliative care issues with patients with advanced illness and therefore do not communicate about needs, goals, and preferences regarding treatment and care in an adequate and timely manner with patients and relatives (Horlait et al. 2016;Stegmann et al. 2020;Udo et al. 2018). Physicians often act reactively rather than proactively (Udo et al. 2018). Over the last decade, several communication skills training programs for health-care professionals on communication with palliative care patients have been developed and evaluated (Fujimori et al. 2014;Paladino et al. 2019;Slort et al. 2014); however, there is little consensus on their effectiveness and how to evaluate their added value (Back 2020;Bos-van den Hoek et al. 2019). In evaluation studies of such communication skills training programs in palliative care, gradually more attention is paid to their effectiveness on the broader experiences of patients and relatives in quantitative studies (Curtis et al. 2018;Doorenbos et al. 2016) as well as in qualitative studies (Kim et al. 2018;Krug et al. 2021), although comparing studies can be difficult because of the wide diversity of outcomes in included studies (Van der Velden et al. 2020). The most promising communication skills training interventions for high-quality palliative care point to the training of professionals' communication skills in teams (Back 2020).
In addition to shared preferences of a patient and her/his relative for communication in palliative care, health-care professionals should be aware of possible differences in their preferences in conversations. Sometimes, relatives want more prognostic information. While it may be complicated, for legal privacy reasons, to have an additional conversation with the relative, for example in case the patient has no limited capacity for communication, healthcare professionals should be sensitive to the needs of relatives and support relatives to discuss their concerns.
Most studies in this review focused on communication with physicians in a hospital setting, although many studies also emphasize the important role of general practitioners, nursing home physicians, and nurses in different care settings in palliative care (Gilissen et al. 2017;Sekse et al. 2017;Van der Plas et al. 2018). Therefore, more attention should be paid to the experiences of patients and relatives with communication with nurses in all care settings and physicians in nonhospital care settings. From the studies in this review, it is unclear whether there is a difference in effective communication as perceived by patients and/or relatives between generalists and in palliative care specialized professionals.

Limitations of the study
Some limitations of this systematic review should be taken into account. First, most studies included no information about the level of expertise in palliative care of the health-care professionals involved. This limits the opportunity to explore the potential added value of in palliative care specialized professionals. Second, most studies concerned planned conversations with physicians, whereas also other health-care professionals communicate with patient and relatives in planned as well as unplanned conversations. Third, only 3 studies have been found in which diversity of patients and relatives is given attention. Besides those about patients or relatives from a non-Western culture, we did not find any studies that paid attention to other diversity in Western countries, for example, in religion, socio-economic background, sexual orientation, or health skills.

Conclusion
Our systematic review demonstrates that, for effective communication, patients and their relatives, besides open and honest information, want health-care professionals to pay attention not only to the patient's disease and symptoms but also to who the patient is beyond the illness and to the role of the relative. Such attention can give patients and relatives a sense of safety within the uncertainty of experiencing a trajectory of advanced illness. Tailored information, empathy, and clear language are the basic elements of effective communication. Our review also shows that additional research is needed on effective communication by nurses, in nonhospital settings and on the added value of in palliative care specialized professionals. More research is also needed in the natural setting of clinical practice (e.g., ethnographic research) and on diversity of patients and relatives.
Supplementary material. The supplementary material for this article can be found at https://doi.org/10.1017/S1478951523001165.