Introduction

People with a progressive form of Multiple Sclerosis (MS) may live for many years while experiencing a wide range of symptoms, impairments (including cognitive deficits), and comorbidities [1]. For these reasons, they may benefit from Advance Care Planning (ACP), not only because it can lead to the creation of a legally binding document, but also because it represents an ongoing communicative process focused on identifying personal values and meanings to support informed and conscious health decisions.

The emphasis on patients’ values, preferences, and wishes is a core feature of ACP, as well as of shared decision making (SDM). SDM is a collaborative approach by which, in partnership with their HP, patients are encouraged to think about the available care options and the likely benefits and harms of each, to communicate their preferences, and help select the best course of action that fits these [2]. SDM mostly focuses on short-to-mid-term goals of care, while ACP on long-term goals of care, in the event of an impairment of decisional capacity. From MS diagnosis many key decisions are to be made by persons with MS. Most of such decisions are preference-sensitive, which makes SDM particularly important. Some MS clinical guidelines recommend incorporating patient preferences into disease-modifying treatment decisions [3]. However, evidence of implementation of SDM in routine MS care is limited [4–6].

SDM has been recently proposed as a ‘method of care’ for HPs and patients in any disease phase or care setting, including conversations to elicit patient-centered goals for end-of-life care in the acute setting [7,8].

Concerning ACP, discussing life goals and preferences, quality of life, dying, and self-determination can enhance satisfaction with communication between HPs, patients, and their families [9,10]. According to Pedrosa Carrasco et al. (2021) [10], ACP can improve patients’ awareness of their priorities and preferences, as well as their sense of engagement in the illness journey. Moreover, ACP can strengthen family relationships and foster trust and understanding between patients and HPs [11]. Also, emotions play a central role in the ACP process. There are few studies analyzing the impact of ACP on the care of people with MS, and even fewer that highlight the emotions that arise during ACP conversations between patients and their HPs. Among these studies, Tay et al. (2021) observed that during ACP conversations emotional expression with positive and negative valence emerged [12]. These emotions arose because conversations focused on positive and negative decisional, relational, and existential topics. Moreover, according to the literature the patients’ perception of ACP involvement seems to be associated with positive emotional functioning [13].

This manuscript reports the analysis of the first ACP conversation between people with progressive MS (PwPMS) and their neurologists in the ConCure-SM pilot trial (ISRCTN48527663) [14]. Briefly, ConCure-SM was a single-arm pilot and feasibility study on a structured ACP intervention, consisting of: I) a training program on ACP for neurologists and other MS HPs (S1 Appendix); II) a booklet to be used during the ACP conversation, which was co-produced with PwPMS and MS HPs [15]. The intervention supported neurologists in guiding PwPMS in their ACP. However, we found a worsening of PwPMS anxiety at both one and six-month follow-ups [14]. For this reason, we decided to add the analysis of the emotional contents of the conversations to the planned analysis of information exchange.

Materials and methods

We analyzed the first ACP conversation between PwPMS and their (trained) neurologist. Another HP could participate in the conversation, as well as a PwPMS significant other (SO). Each conversation was audio-recorded and transcribed verbatim. After the conversation, PwPMS completed the Quality of Communication Questionnaire (QOC) [16], SOs completed the SO version (QOC-SO), and neurologists the physician version (QOC-DOC; last two items of the QOC).

Results

Mean duration of the ACP conversations was 62.7 minutes (SD 18.3). Five conversations had two participants (the PwPMS and the neurologist), eight involved an additional participant (four the PwPMS SO, and four another HP), and five conversations involved two additional participants (the PwPMS SO and another HP). The general and clinical characteristics of the PwPMS and their SOs are reported in Table 1. PwPMS mean age was 61.8 years (range 50–77); 7 (39%) were women. Eleven (61%) had secondary progressive MS; median Expanded Disability Status Scale (EDSS) score was 8.0 (IQR 6.5–8.0). SOs were 57.1 (range 34–74) years old; 4/9 (44%) were women; six were the spouse, one the son, and two the brother of the PwPMS. The neurologists (5/7 women, 71%) were 30–62-year old and had 5–30 years of experience in MS care.

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Table 1. Characteristics of the people with progressive multiple sclerosis (PwPMS) and their significant others.

https://doi.org/10.1371/journal.pone.0336183.t001

Shared decision making

Inter-rater reliability for the OPTION total score was good (ICC 0.80, 95% CI 0.54–0.92). Disagreement exceeded 3 points in four instances. At the item level, disagreement exceeded one point in three instances: one for “offering opportunities to ask questions” (item 9) and two for “eliciting preferred involvement in decision-making” (item 10). After discussing discordant items, the resulting mean OPTION total score was 48.4 (SD 7.5; median 46.9, IQR 43.8–54.2), corresponding to a moderate degree of patient involvement. The most frequently observed behaviors were: “drawing attention to an identified problem requiring a decision” (item 1) and “exploring the patient’s concerns” (item 7). By contrast, in no case did neurologists elicit the patient’s preferred approach to receiving information (item 3); this behavior was not observed as the ACP interview was in fact structured, with the use of the booklet (Table 2). A key step in the ACP dialogue is the (continuous) clarification and understanding of the patient’s values, to help the delivery of care that aligns with those goals and values [29–31]. As this behavior is not assessed in the OPTION scale, we have added the item “exploring patient’s values”, which was rated using the same five-point scale, and obtained a median score of 50 (IQR 50–75).

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Table 2. Distribution of the Observing Patient Involvement in Shared Decision Making (OPTION) item and total scores.

https://doi.org/10.1371/journal.pone.0336183.t002

Emotional communication

According to the VR-CoDES analysis, PwPMS expressed 179 cues and 63 concerns, while neurologists provided space for 59% of cues and 73% of concerns (Table 3). Most cues were of B (37%) and D (14%) type (S1 Table). Expressions indicating hope, confidence, and positive wishes were coded as positive emotional statements (PESs), which accounted for 12% of the instances.

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Table 3. Distribution of concerns and cues (cue types detailed in S1 Table) according to whether spontaneous or neurologist-elicited and according to the neurologist’s immediate response (reduce vs. provide space).

https://doi.org/10.1371/journal.pone.0336183.t003

A quarter of cues/concerns (61/242) contained figurative expressions: most of them were in type B cues, but they were also found in type A, D, E, and G cues, in concerns, and PES (Table 3). 34/61 (55.7%) of neurologists’ responses were coded as explicit; 41/61 (67.2%) provided space for the PwPMS to stay on the emotional topic or delve deeper into the cue/concern. The most frequently coded types of responses were: “acknowledges content” (e.g., PwPMS: “I’m the type of person who wants to know who I have to fight-with”. Neurologist: “Clearly, it’s not a process that started yesterday […], living with the disease is something that is well established in your life…”), “ignores” (PwPMS: “Since I cannot go out, sometimes my daughter has to take over […]. Because I was very active …”. Neurologist: “Yes. However, other issues, for example, that may concern others?”), “acknowledges affective aspect” (e.g., PwPMS: “the disease really cut my legs off”. Neurologist: “This vision of life is comprehensible, there’s no doubt about it”), and “brief facilitation, encouragement (e.g., Neurologist: “Yes”; “Hmm”).

Thematic analysis

We identified four major themes that emerged from the emotional communication codes: the impact of the illness on PwPMS and SOs’ lives, the possible loss of personal autonomy, the caring approach of the physician, and feelings related to discussing EOL. Selected quotes supporting the four themes are reported in Table 4.

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Table 4. Selected quotes supporting the four themes.

https://doi.org/10.1371/journal.pone.0336183.t004

PwPMS expressed emotions related to the current impact of MS on their lives in terms of the need to adapt to and try to overcome the barriers imposed by the disease: they expressed both negative emotions, namely frustration about feeling overwhelmed by their MS, and positive emotions about developing new awareness on their personal resources. PwPMS also expressed the fear of being a burden to others or of a negative impact of their MS on relationships and friendships. The ACP conversation produced a sense of relief and self-confidence as it meant making decisions for themselves, without leaving beloved ones the burden of making choices.

The ACP conversation provided an opportunity to discuss the possible evolution of their disease and the related fear of losing autonomy. The concept of personal autonomy was manifested in two ways: the fear of becoming physically dependent on others in any daily activities, and concerns about losing mental capacity.

Emotions related to the caring approach of the physician were reported as anger or feelings of abandonment by PwPMS who, during the illness pathway, had to make health decisions alone, while other PwPMS expressed gratitude to be cured by a physician with “a good soul” and able to have a deep communication with them.

Finally, some PwPMS were comforted and calm during the structured conversation dedicated to EOL issues. In contrast, others expressed negative emotions such as anxiety. Some PwPMS tried to avoid these thoughts and found the scenarios related to EOL choices too challenging.

Discussion

Findings of our pilot and feasibility trial on a training program on ACP for neurologists and other MS HPs have been recently published [14]. ACP training programs for HPs have been developed and tested in various disciplines, including oncology [32–34], and internal medicine [35] where recent evidence shows that clinician training had a positive effect on ACP uptake and documentation. Further, preliminary evidence in ALS [36] and Parkinson’s disease [37,38] suggests that integrating palliative care with ACP is feasible and valuable for patients and clinicians.

Here we report the communication competences of neurologists who participated in our pilot trial. Eighteen first ACP conversations of PwPMS with seven neurologists were transcribed and analysed. Physicians well varied in age and years of MS experience; none of them had any previous experience of ACP.

We assessed the perspectives of the diverse participants (PwPMS, SOs, and neurologists) using corresponding versions of the QOC scale [20]. Moreover, these competences were assessed by independent observers considering two pivotal elements of medical communication: information exchange/SDM (using the OPTION) and emotional communication (using the VR-CoDES).

Mean QOC scores of PwPMS and SOs were high (around 90) for both ‘general communication’ and ‘communication about EOL care’ subscales, while neurologists were more self-critical, with mean values below 70. Although PwPMS and SOs completed the QOC using a dedicated platform (or by an interviewer) to guarantee confidentiality it is possible that the high scores obtained were affected by acquiescence bias. Concerning the lower QOC-Doc scores, this can be explained by the fact that ACP was a new practice for all the participating centers, and neurologists were at their first ACP experience after the training, out of the comfort zone of a typical MS consultation.

The mean OPTION total score was 48.4, corresponding to a moderate degree of SDM competences of our neurologists. This value was higher compared to the two studies that, to our knowledge, have used the OPTION in the context of consultations at MS centers in Italy [22] and Germany [39], both with mean scores around 30. Recently, a large cluster randomized controlled trial involving 65 Belgian nursing home wards applied the OPTION to audio recordings of ACP conversations between residents, families and staff [40]. Wards assigned to SDM training showed an increase in mean OPTION score from 27 to 54 (p < 0.001) while time spent on the conversations did not increase. This improvement persisted six months after training (mean OPTION score 56; p < 0.001) [40].

The VR-CoDES revealed two main findings. First, PwPMS expressed a median of 8.5 cues and 3 concerns per conversation, and these expressions were higher compared to a study of first consultations at Italian MS centers (median 4 cues and 1 concern per consultation) [23]. This indicates that the ACP conversation can elicit a huge number of patient emotions, which is consistent with the increase in PwPMS anxiety symptoms as assessed using the Hospital Anxiety and Depression Scale (p = 0.02), and with the qualitative study nested in the trial, revealing the ‘emotional cost’ of ACP for both PwPMS and their SOs [14]. Second, neurologists provided space to 59% of cues and 73% of concerns. This differed from Del Piccolo et al. (2015) study, where corresponding figures were 42% for cues and 24% for concerns, and common neurologists’ reactions included changing the subject, taking no notice, and giving medical advice [23]. This suggests that the ConCure-SM training program helped neurologists to provide space to the many emotions that emerged and to show a meaningful engagement in the ACP conversation.

Emotions that emerged were not only related to the disease and treatment decisions, but also to broader aspects of patients’ lives, such as the loss of personal autonomy, the individual resources in managing the disease, and the overall impact of the disease on personal identity. This is particularly noteworthy, as it demonstrates that ACP is not merely a tool for obtaining consent for healthcare choices, but a process through which personal values and life perspectives are more deeply understood, articulated, made explicit and shared.

Interestingly, positive PwPMS emotions also emerged, including expressions of hope, confidence, and positive expectations, suggesting a potentially beneficial role of ACP.

The emotional burden of the ACP process emerged through the figurative language used during the conversations. These expressions helped PwPMS to share how they perceive themselves within the context of the disease. Our results are consistent with studies performed in other settings, showing the occurrence of both positive and negative emotional expressions during ACP discussions and more generally during EOL conversations [12,41]. Two studies also reported an increased patient trust in the care team and a stronger sense of closeness with the clinician because of ACP conversation [42,43].

Our study has some limitations. First, our sample was small with 18 ACP conversations included in the analysis, which may limit the generalizability of our findings to a broader population of neurologists or PwPMS. Moreover, the study was conducted in Italian MS centers, which may not account for cultural or contextual differences in other countries or healthcare settings.

In conclusion, our multi-perspective analysis of the first ACP conversations document good communication competences of MS neurologists, exhibited in a highly emotive context. Our findings support the value of training programs to improve the confidence of neurologists in ACP practice. Further research should explore strategies to implement this practice out of the setting of a pilot trial, in the busy environment of an MS center.

Supporting information

Acknowledgments

We thank all the PwPMS and SOs who participated in the study.

ConCure-SM project investigators

Steering Committee: LuDP; SV; Michela Bruzzone, Italian Multiple Sclerosis Society, Genoa, Italy; AGa; MGG; Paola Kruger, The European Patients’ Academy (EUPATI), Rome, Italy; AL; SM; FP; Eugenio Pucci, UOC Neurologia, AST Fermo, Fermo, Italy; CS; AGi; AS (Principal Investigator; alessandra.solari25@gmail.com).

Data Safety and Monitoring Committee: David Oliver, The Tizard Centre, University of Kent, Canterbury, UK (Chair); Kevin Brazil, School of Nursing and Midwifery, Queen’s University of Belfast, Belfast, Northern Ireland, UK; Bobbie Farsides, Brighton & Sussex Medical School, Falmer, Brighton, United Kingdom; Luciano Orsi, The Italian Society of Palliative Care (SICP), Milan, Italy; Carlo Peruselli, SICP, Milan, Italy.

Data Management and Analysis Committee: AGi; MF.

Qualitative Analysis Panel: LuDP; SV; Marta Perin, Unit of Bioethics, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy; Luca Ghirotto, Qualitative Research Unit, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia, Italy; Katia Mattarozzi, Department of Medical and Surgical Sciences, Alma Mater Studiorum University of Bologna, Bologna, Italy; RMZ.

HP Training Panel: LuDP; SV; Marta Cascioli, Hospice La Torre sul Colle, Spoleto, Italy; Katia Mattarozzi, Department of Medical and Surgical Sciences, Alma Mater Studiorum University of Bologna, Bologna, Italy; Eugenio Pucci, UOC Neurologia, AST Fermo, Fermo, Italy; Michela Rimondini, Section of Clinical Psychology, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Policlinico G.B. Rossi, Verona, Italy; AS.

Linguistic Validation Panel: MF; Paola Kruger, The European Patients’ Academy (EUPATI), Rome, Italy; SV; AGi; AS.

Enrolling Centers and Investigators: Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona; Unit of Neurology, Borgo Roma Hospital, Azienda Ospedaliera Universitaria Integrata Verona, Verona: AGa, RO, Angelica Filosa. Department of Rehabilitation M. L. Novarese Hospital, Moncrivello, Vercelli: CS, Erica Grange. Multiple Sclerosis Center, Azienda USL-IRCCS di Reggio Emilia, Reggio Emilia: SM, Francesca Sireci. UOSI Riabilitazione Sclerosi Multipla, IRCCS Istituto delle Scienze Neurologiche di Bologna; Dipartimento di Scienze Biomediche e Neuromotorie, Università di Bologna, Bologna: AL, Federica Pinardi, Loredana Sabbatini, Cinzia Scandellari, Elisa Ferriani. Fondazione IRCCS Santa Lucia, Rome: MGG, GP, Luigi Iasevoli. University Hospital Policlinico Vittorio Emanuele, Catania: FP, ST, Clara Grazia Chisari.