Disclosing the Risk Associated with Isolated REM Behavior Disorder: The Sleep Experts’ Perspective

Abstract

Background

Isolated rapid‐eye‐movement sleep behavior disorder (iRBD) is associated with a high risk for phenoconversion to a neurodegenerative disorder, but the optimal approach for disclosure of this risk to patients is still debated.

Objectives

The aim of this study was to explore views and experiences of iRBD experts regarding risk disclosure.

Methods

In this qualitative study, semi‐structured interviews with sleep experts caring for patients with iRBD were analyzed through a conventional content analysis approach.

Results

We interviewed 22 iRBD experts (eight female, average age of 51.8 years) from 18 Italian sleep centers; 21/22 regularly disclosed the risks associated with iRBD, usually after the video‐polysomnography, and 8/22 regularly mentioned phenoconversion rates. Content analysis allowed us to identify three main themes. First, sleep experts reported several points in favor of risk disclosure, especially related to the principle of beneficence, but some highlighted the need for specific learning on the topic. Second, experts favored a patient‐tailored disclosure that should not upset the patient unnecessarily, since phenoconversion is uncertain. Third, risk disclosure was seen by participants as a relational task that should be carried out in person in the context of a trusting patient‐physician relationship, while they had contrasting views regarding patients’ previous knowledge.

Conclusions

Sleep experts generally preferred a tailored and reassuring approach to risk disclosure within a framework of relational autonomy. The results of this study indicate the need for specific education, training, and recommendations concerning risk disclosure that should also include patients’ and families’ preferences.

Rapid‐eye‐movement (REM) sleep behavior disorder (RBD) is a parasomnia, mostly arising in adulthood, characterized by the loss of physiological REM sleep atonia, resulting in dream‐enactment behaviors, possibly violent or aggressive, that may cause physical injuries to the patient and his/her bedpartner. ¹ , ² , ³ Episodes are to a certain degree responsive to pharmacological treatment. ³ , ⁴ Video‐polysomnography documenting REM sleep without atonia is mandatory for the diagnosis of RBD. ¹ , ⁵ The disorder is classified as idiopathic or isolated (iRBD) when there is not an apparent or demonstrable cause, including inciting substance or medication or a clear underlying disorder. ¹ , ⁴

At the present time, iRBD carries the highest positive predictive value for impending neurodegeneration. ⁶ , ⁷ Indeed, patients with iRBD have a high risk of phenoconversion to a clinically defined neurodegenerative disease (NDD), mainly an α‐synucleinopathy such as Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. This risk increases over time from ~15–28% over 2–5 years to 67.5–90.9% at 10–25 years after diagnosis, ⁸ , ⁹ , ¹⁰ but a substantial interindividual variability has been reported. ¹¹

Since providing an individualized prognosis for phenoconversion remains challenging, ¹¹ and there are currently no treatments available to prevent or reverse it, there is ongoing debate regarding the optimal approach for disclosure of the iRBD‐related risk to patients. An ethical tension between the principles of respecting patient autonomy and non‐maleficence (avoiding harm) has often been emphasized, although some scholars have also underlined the role of the principle of beneficence. ¹¹ , ¹² , ¹³ , ¹⁴ , ¹⁵ , ¹⁶ , ¹⁷ , ¹⁸ , ¹⁹ , ²⁰ , ²¹ , ²² , ²³ Balancing these ethical principles, and with the objective of preserving the patient‐physician relationship, there is an agreement that the patient should at least be informed of the association between iRBD and NDDs, and that the patient's preferences regarding further information should be investigated. ¹³ , ¹⁵ , ¹⁶ , ¹⁸ , ²⁰ , ²¹ , ²² , ²³ , ²⁴ , ²⁵

Recent surveys found that most patients with iRBD want to receive information concerning their risk of developing an NDD. ²⁵ , ²⁶ However, a third of patients did not recall having received this information at the time of diagnosis. ²⁵ This finding supports the observation that, in clinical practice, sleep experts’ approach remains heterogeneous. ²⁵ For example, while 93% of experts reported providing routine prognostic counseling for patients with iRBD, only 15% reported mentioning the specific risk to the patients, and prognostic counseling was documented in just 55% of patient records. ¹⁶ , ¹⁹ Similarly, among iRBD experts responding to an international survey, 41% stated they would inform patients of their risk of developing Parkinson's disease in all cases, while 41% would only disclose the risk upon patients’ request. ²² Unfortunately, the use of questionnaires or analysis of medical records did not provide explanations as to the physicians’ underlying reasoning, which is crucial for developing recommendations in clinical and research settings. ²⁴

The aim of this study was to address this gap by exploring the views and experiences of iRBD experts regarding risk disclosure, using a qualitative approach.

METHODS

Participants

The study was supported by the Italian Association of Sleep Medicine (AIMS) that selected 25 experts in RBD diagnosis and management who were invited to answer a semi‐structured telephone interview. A maximum variation sampling approach was used to include a wide range of ages, professional experience, sleep center size, and geographical areas. The invitation, sent by e‐mail, explained the study aims and methods, including a list of further data that, with the consent of participants, would be collected (ie, sex, age, geographical area, specialization, length of experience in sleep medicine, and number of iRBD diagnoses/year). Participants were informed that:

1. Participation was voluntarily, and they had the right to stop the interview at any time;

2. Their potential participation would be kept confidential;

3. With their consent, the interview would be recorded and transcribed anonymously (ie, not linked in any way to their names), and de‐identified quotations from the interview would be included in future publications.

All experts participated on a voluntary basis and provided oral consent at the beginning of the interview.

Interviews

The interview guide, including questions and prompts, was developed on the basis of a literature review and was adjusted between the first few interviews. The interview was divided into two parts. The first part investigated the experts’ experiences (whether, when, how, and which details they generally provide information about the risk for phenoconversion, whether they encountered difficulties or discomfort, whether the patient and family were already knowledgeable about the risk and how they usually reacted to the disclosure) and opinions concerning risk disclosure in the case of an iRBD diagnosis (the main pros and cons of a detailed risk disclosure, and patients’ and families’ preferences for disclosure). The second part sought experts’ indications for the improvement of the physician communication approach and suggestions as to what the AIMS could do in this regard.

The interviews were conducted between January and February 2019 by an ad hoc trained interviewer who did not know any of the possible participants; the interviews were audiotaped and transcribed verbatim.

Data Analysis

Since the primary goal of the study was to gain a richer understanding of the experts’ views and experiences, a qualitative conventional content analysis was used. ²⁷ The codebook was developed by two authors after they independently and repeatedly read the first five interviews, highlighting key participants’ thoughts or concepts that were labeled with codes in order to develop an initial coding scheme. The scheme was discussed and then used to code the remaining interviews. Code saturation (ie, when no new codes were identified) was reached upon analysis of interview 20. Through an iterative and consensus‐based approach involving a third author, differences in interpretation were resolved, and codes were organized into subthemes, and these into main themes. Analysis was supported by the NVivo software (QSR International). Standards for reporting qualitative research ²⁸ guided the present report.

Data Sharing

Because participants did not provide written informed consent to share the content of interviews, the Authors will not make the data available. The interview guide will be available upon request to the corresponding Author.

RESULTS

Of the 25 sleep experts invited, 22 from 18 sleep centers across the country accepted the invitation to participate. One expert was not contactable by telephone, while two experts declined the invitation after the first telephone contact, due to a lack of interest in the project.

Characteristics of participants were reported in Table 1. The mean age of participants was 51.8 years. Eight out of the 22 participants (36%) were female, and 18 (82%) were specialized in neurology while 4 (18%) were neurophysiopathologists. The mean length of experience in sleep medicine was 22.3 years, and the mean number of iRBD diagnoses during the past year was 13.1. The frequency of follow‐up visits for patients with iRBD ranged from once to three times a year.

TABLE 1.

Participants' characteristics (N = 22)

	N (%) or mean (SD)
Age, y	51.8 (10.9)
Female sex	8 (36)
Geographical area
North	12 (54)
Center	5 (23)
South	5 (23)
Specialization in neurology	18 (82)
Experience in sleep medicine, y	22.3 (11.2)
iRBD diagnosis/past year	13.1 (6.8)
Regularly disclosed neurodegenerative risk
At the first examination	3 (14)
After video‐polysomnography	18 (82)
No	1 (4)
Regularly provided phenoconversion rates	8 (36)
Regularly provided supplementary sources of information
Patients’ association website	3 (14)
Scientific articles	2 (9)
No	17 (77)

All experts but one (96%) reported that they habitually disclose the neurodegenerative risk, mainly (18 out of 22, 82%) after iRBD has been confirmed by video‐polysomnography, and 8 experts (36%) reported that it was common practice for them to mention phenoconversion rates. With regard to supplementary sources of information, 3 (14%) experts reported regularly recommending the patients’ association website, and 2 (9%) provided patients with scientific articles.

Compared to neurologists, neurophysiopathologists were younger (53.4 ± 10.8 vs. 40 ± 5.9 years), had a shorter length of experience in sleep medicine (24.6 ± 10.9 vs. 13.3 ± 5.4 years) and reported a lower mean number of iRBD diagnoses during the past year (16.3 ± 13.5 vs. 12 ± 5.9); none of the neurophysiopathologists reported habitually disclosing the neurodegenerative risk before having video‐polysomnography results (vs. three neurologists who reported that they informed patients of the risk when there was a suspected diagnosis) or provided supplementary sources of information (vs. four neurologists), while one out of four neurophysiopathologists versus seven out of 18 neurologists reported mentioning phenoconversion rates.

The mean length of interviews was 21.6 min (range 11–31).

The qualitative content analysis allowed us to identify three main themes, and several subthemes (Table 2), that are reported herein with representative quotes.

TABLE 2.

Main themes and subthemes

Theme 1: Experts reported several reasons for risk disclosure, especially related to beneficence, but some highlighted the need for specific learning Subthemes: 1.1 Experts reported several points in favor of risk disclosure, especially related to the principle of beneficence 1.2 Some experts highlighted the need for specific education and training on risk disclosure

Theme 2: Since phenoconversion is uncertain, experts favored a tailored disclosure that should not upset the patient unnecessarily Subthemes: 2.1 Experts favored a reassuring and cautious approach, since phenoconversion is uncertain 2.2 Experts underlined the importance of patient‐tailored communication

Theme 3: Risk disclosure was seen by participants as a relational task Subthemes: 3.1 Risk disclosure should occur within a trusting patient‐physician relationship 3.2 Leaflets and websites may help, but oral communication remains crucial 3.3 Physicians had contrasting views about patients’ previous knowledge

Theme 1: Experts Reported Several Reasons for Risk Disclosure, Especially Related to Beneficence, but Some Highlighted the Need for Specific Learning

Experts Reported Several Points in Favor of Risk Disclosure, Especially Related to the Principle of Beneficence

Table 3 shows the pros and cons of risk disclosure reported by the experts, and the related ethical principles or rules according to Beauchamp and Childress Principles of Biomedical Ethics. ²⁹

TABLE 3.

Pros and cons of risk disclosure and related ethical principles/rules

	Ethical principle/rule
Pros
Increasing the patient's compliance with follow‐up visits	Beneficence
Timely detection and treatment of signs of possible phenoconversion
Early access to future clinical trials
Protecting patients and family from inappropriate information, especially on internet
Helping patients to accept the disease in case of phenoconversion
Family members may better help the patient
Knowing is a patient's right	Autonomy
Patients prefer to know
Allowing the patient to plan
Disclosing information is a physician's professional and ethical duty	Veracity
Fostering and maintaining trust	Trust
Cons
Psychological consequences (eg, anxiety, depression)	Non maleficence
Social consequences (eg, divorce, early work retirement)

Most of the reasons in favor of disclosure were related to the principle of beneficence, including improving patients’ outcomes through a timely diagnosis and treatment in the case of phenoconversion, early access to future clinical trials, and protecting patients and family from receiving inappropriate information regarding the neurodegenerative risk. Other reasons concerned patient autonomy and the professional ethical obligation of veracity, and the objective of fostering and maintaining trust.

When asked about the cons of risk disclosure, some experts reported that risk disclosure may have psychological (anxiety or depression) or social (eg, divorce, early work retirement) consequences for the patient, but in their experience few patients or family members reacted with anxiety or fear to the disclosure regarding the association between iRBD and NDDs. On the other hand, a few experts reported patients’ apparent lack of interest in the diagnosis, wondering whether this may be an early sign of conversion, and the apparent underestimation of iRBD severity on the part of some older patients. One expert said: “On average, they don't consider it such a major disorder, especially those who are older”.

Some Experts Highlighted the Need for Specific Education and Training on Risk Disclosure

Although experts supported risk disclosure, some of them reported a lack of specific education and training, acknowledging that such communication requires specialized knowledge and skills. One expert said: “We rely very much on our sensitivity and what we have acquired in our clinical practice, but […] we have not been prepared to do such specific things”. Some experts mentioned in particular the lack of guidance regarding the “right time” for risk disclosure (“We are not trained […] especially in terms of timing, that is, at which stages we should relay the various pieces of information”) and highlighted the need for studies that explore the patient perspective. One expert said: “It would be really, really important… to understand whether, for example, getting the information all in one shot, rather than a little at a time, in what way, during the course of their diagnosis or during the therapeutic monitoring, would be the best thing for a patient…”.

For a few experts, risk disclosure may be emotionally uncomfortable, especially because they cannot provide patients with preventive treatments. One expert said: “Unfortunately, we cannot […] offer possibilities for prevention, and therefore I always feel bad when proposing a hypothesis against which I can do nothing at the moment”.

For many experts, AIMS recommendations would help to improve and standardize risk disclosure. One expert said: “Guidelines are definitely welcome, because if we all have a very similar way of communicating… sure, there will still be subjectivity and individual sensitivity and experience, but of course there will be a consistent approach, which will be a great help”.

Theme 2: Since Phenoconversion is Uncertain, Experts Favored a Tailored Disclosure that Should Not Upset the Patient Unnecessarily

Experts Favored a Reassuring and Cautious Approach, Since Phenoconversion is Uncertain

Given the lack of elements for an individualized prognosis, the majority of experts underlined the need for a reassuring and cautious approach when breaking such news, trying to avoid upsetting patients unnecessarily or causing anxiety or resignation. One expert said: “It's not genetic counseling, it's something that has more variables and therefore you need to be as delicate as possible”. For this reason, most experts said they did not provide patients with phenoconversion rates. One expert said: “… Not having any way of telling [the patient] whether he'll be in that 10% or in the 80%… I don't think it's fair to instill that fear that can, in any case, influence a person in his everyday life”.

Participants underlined that when informing patients, the “right words and manners” (kindness, tact, empathy, use of simple terms and metaphors, and “avoiding presenting the risk as a sentence”) are needed and that patients should be reassured that they will be closely monitored and never abandoned: should Parkinson's disease develop, symptomatic treatments are available.

Experts Underlined the Importance of Patient‐Tailored Communication

Almost all experts underlined the importance of tailoring risk disclosure to the individual, mentioning several aspects that should be considered. Many experts mentioned the importance of considering patients’ educational background, the presence of family members and their supportiveness, and the patient's age and working status. Experts also underlined the need to consider psychological aspects, including mood disorders and emotional frailty. Finally, pre‐existing conditions, functional status and autonomy, and possible early signs of phenoconversion were mentioned.

For some experts, a stepped disclosure during follow‐up would allow the physician to provide a more tailored disclosure; with this regard, one expert said “… precisely because in this way we may take into account the patient's educational level, but also the patient's level of anxiety, and therefore perhaps the patient is told in a way that is slightly more custom‐built”.

Theme 3: Risk Disclosure was Seen by Participants as a Relational Task

Risk Disclosure Should Occur within a Trusting Patient‐Physician Relationship

Several experts outlined the concept that risk disclosure should occur within a long‐lasting physician‐patient relationship. One expert said: “You take care of the patient… in the context of a relationship with the patient that carries on in time… I think this might be the ingredient that stops this type of communication from being, let's say, a harbinger of panic or basically something bad”. This relationship requires a wide availability on the part of physicians (eg, patients and family may feel free to contact them via email or telephone) and some experts added that family members may play an important role.

Leaflets and Websites May Help, but Oral Communication Remains Crucial

When asked about the possible usefulness of written information, many experts answered that it would be useful to provide patients with good material, but some of them commented that written information should not replace patient‐doctor communication. One expert said: “Informative material… can be something that comes afterwards, but I need to speak to the patient”.

Internet is often considered an untrustworthy source of information and some experts underlined that online information regarding the risk of developing an NDD may be scary or brutal for the patient. On the other hand, some experts pointed out that providing good quality information through the AIMS website would be very useful. One expert said: “If the AIMS produces something that is also made available to users… there is an interchange, therefore the patient goes home, searches, checks, finds information that is correct… then he comes back to us to ask for further explanations”.

Finally, some experts mentioned RBD patient associations’ websites (already existing in Italy, www.associazionerbd.it) and forums as a useful place where patients and family may share information and find emotional support.

Physicians Had Contrasting Views about Patients’ Previous Knowledge

Regarding previous knowledge about the risk of developing an NDD, some experts underlined the possibility that patients may misinterpret self‐retrieved information or “take away only the worst scenarios”, and it may be more difficult to properly inform and reassure them. One expert said: “One should not only inform, but also carry out a mission of counter‐information”. One expert reported that patients with previous knowledge make him feel uncomfortable because of the uncertainty of conversion: “They come and ask you whether or not they will get Parkinson's, they want to be told, and you can't say to them, ‘you will or you won't get Parkinson's’”.

For other experts, a patient's previous knowledge about the neurodegenerative risk eases the physician's job, because patients are more willing and ready for disclosure and it is easier to address the topic for the doctor. One expert said: “A patient who is already informed, is more willing to listen and is already emotionally a little ready for that type of perspective, so it's simpler…”.

DISCUSSION

Due to the increasing availability of new biomarkers for the detection of neurodegenerative disorders in their prodromal phase, the topic of risk disclosure is an emerging ethical question, with substantial implications in both clinical and research settings. ²² , ²⁴ , ³⁰ , ³¹ , ³² , ³³ , ³⁴ With regard to iRBD, we may expect that the issues will become even more complex with the availability of tests for a‐synuclein. ³⁵ , ³⁶

This qualitative study aimed to explore sleep experts’ perspectives regarding the disclosure to patients of the risk for phenoconversion associated with iRBD. We found that almost all sleep experts supported risk disclosure when the diagnosis of iRBD is confirmed by video‐polysomnography, ¹ within a strong commitment to taking care of patients and closely monitoring them, according to the principle of non‐abandonment. ¹³ Participants acknowledged the importance of an individualized approach that considers medical, psychological, and social factors, in line with a bio‐psycho‐social approach to iRBD.

Academic assumptions usually indicate the respect for patients’ autonomy as a pre‐eminent reason for risk disclosure. The qualitative approach adopted in our study allowed us to identify several other reasons in favor of risk disclosure. Interestingly, these reasons were, for the most part, related to the principle of beneficence, the goal being to improve patients’ outcomes and to protect them from inappropriate or overwhelming information on iRBD‐related risk. Also, professional ethical obligation of veracity and fostering and maintaining trust were reported as substantial reasons for disclosure. The need to understand the patient's perspective and the emphasis on the relational aspect of risk disclosure, in which family members may play an important role, suggests that the ethical framework was, for most participants, that of relational autonomy. ³⁷

These findings may help to understand inconsistent findings from previous studies and have practical implications. Indeed, if the main concern of physicians is acting for the benefit of the patient instead of promoting patient's autonomy, physicians may tend toward providing patients with information needed to improve their clinical outcomes rather than that required to assist in their decision‐making. This may explain why most experts worldwide, including the participants in our study, reported that they provide prognostic counseling, but only a minority mentioned the specific risk for phenoconversion or asked about patient preferences for prognostic counseling. ¹⁹ , ²⁵ , ²⁶ On the other hand, the few studies that have explored the patients’ perspective indicated that they prefer “more rather than less” information, ²⁵ , ²⁶ since “important decisions hinge on risk disclosure”. ³⁸

In line with the principle of non‐maleficence, participants in our study favored a cautious approach when disclosing the risk for NDDs, since an individual prognosis is still not possible. On the other hand, for some participants avoiding making the patient upset seemed to be more related to their own discomfort when addressing the uncertainty of prognosis, which was a commonly perceived disadvantage in counseling, ¹⁹ rather than to a wish not to harm the patient. This finding could be related to scarce education and training specific to risk disclosure that was reported by some participants ³⁹ and supports the need to provide communication programs focused on risk disclosure. ²⁵ Moreover, recommendations from scientific societies may offer guidance to sleep experts and a common approach to disclosure that may improve communication with the patient and family when iRBD is diagnosed. Patient and family preferences for risk disclosure should be investigated and incorporated into both educational/training programs and recommendations. ⁴ , ²⁵ , ²⁶ , ⁴⁰ To this regard, it would be important to explore their preference for a one‐time information delivery as opposed to a stepwise approach that would allow the physician to provide a more patient‐tailored communication during follow‐up. ²³ , ²⁵ Moreover, since recent findings suggested that the iRBD diagnosis may be associated with psychological distress for approximately half of patients, ²⁶ it is important to explore their opinion regarding the need for psychological support during the disclosure process.

The third theme identified in our study revealed conflicting views concerning the “informed patient” ⁴¹ and the role of internet that have never been reported by previous studies involving sleep experts. Online information was viewed by many experts with suspicion, especially because it may be misleading or overwhelming for patients and family, but the quality of information makes the difference. ⁴² , ⁴³ , ⁴⁴ Sleep experts recognized the potential of trustworthy websites, such as those managed by scientific societies or patients’ associations, to provide accurate and reliable information. Considering the desire of patients for more information, sleep experts should be encouraged to recommend trusted websites, to be available to discuss the results of internet searches with patients and family members, ⁴⁵ and to contribute themselves, as individuals or as members of scientific societies, to fostering high‐level quality online information on iRBD.

The main limitations of this study are related to the fact that only one person conducted the interviews, and to the potential subjective interpretation of data that is inherent to the qualitative approach adopted. These results may not represent the attitudes of all Italian RBD experts and may not reflect those of experts from other countries. However, the analysis of the interviews provided insights into the experts’ attitudes concerning risk disclosure that are consistent with findings found by other studies. The main strengths of this study were the participation of experienced RBD experts from all over the country, and rich data obtained from participants that encompassed the ethical, professional, psychological, and even emotional domains. Finally, despite the percentage of neurologists in our study was in line with that of a previous study on prognostic counseling involving sleep experts from the International RBD Study Group, ¹⁹ their disclosure practice may be different from the comfort level or preferences of non‐neurology providers. Studies including a larger number of sleep experts from different backgrounds are needed to investigate the existence of different perspectives and practices concerning risk disclosure between sleep medicine providers with different training backgrounds.

In conclusion, we found that, in the case of iRBD diagnosis, sleep experts generally favored a tailored and reassuring disclosure approach in the context of a trusting physician‐patient relationship, mainly with the aim of improving patient outcomes. This approach is in line with a relational account of patient autonomy and with the model of shared decision making that has recently been proposed for iRBD prognostic counseling. ²³ On the other hand, the “danger that misunderstandings and misappropriations of ideas derived from relational accounts could encourage the kinds of inappropriate paternalism” ⁴⁶ exists. Therefore, studies investigating the patient and family perspectives are needed to understand whether this approach satisfies their needs and preferences, aspects that should be considered when developing educational programs and recommendations on risk disclosure.

Author Roles

(1) Research Project: A. Conception, B. Organization, C. Execution; (2) Qualitative Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript: A. Writing of the First Draft, B. Review and Critique.

F.I.: 1A, 1B, 2A, 2B, 2C, 3A

A.D.: 2A, 2B, 3A

A.R.: 2B, 2C, 3B

E.A.: 1A, 2A, 2C, 3B

G.P.: 1A, 2C, 3B

Disclosures

Ethical Compliance Statement: The authors confirm that the approval of the Ethics Committee was not required for this work. All experts participated on a voluntary basis, providing oral consent at the beginning of the interview. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this work is consistent with those guidelines.

Funding Sources and Conflicts of Interest: This research did not receive any financial support. The authors report no conflicts of interest.

Financial Disclosures for Previous 12 Months: Francesca Ingravallo reports no disclosure. Alessandra D'Alterio reports no disclosure. Andrea Rossetti reports no disclosure. Elena Antelmi has served on an advisory board for Polifarma. Giuseppe Plazzi reports grant and consultancy fees from Bioprojet, Idorsia, Takeda, Orexia, and Jazz Pharmaceuticals.