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. 2020 Apr 21;15(4):e0230611. doi: 10.1371/journal.pone.0230611

RADPAC-PD: A tool to support healthcare professionals in timely identifying palliative care needs of people with Parkinson’s disease

Herma Lennaerts-Kats 1,2,*, Jenny T van der Steen 3,4, Zefanja Vijftigschild 2, Maxime Steppe 1, Marjan J Meinders 5, Marten Munneke 1, Bastiaan R Bloem 1, Kris C P Vissers 2, Marieke M Groot 2
Editor: César Leal-Costa6
PMCID: PMC7173770  PMID: 32315302

Abstract

Background

Parkinson’s disease (PD) is a progressive degenerative disease without curative treatment perspectives. Even when palliative care for people with PD seems to be beneficial, the need for palliative care is often not timely recognized.

Aim

Our aim was to develop a tool that can help healthcare professionals in timely identifying palliative care needs in people with PD.

Design

We used a mixed-methods design, including individual and focus group interviews and a three-round modified Delphi study with healthcare professionals from a multidisciplinary field.

Results

Data from the interviews suggested two distinct moments in the progressive PD trajectory: 1) an ultimate moment to initiate Advance Care Planning (ACP); and 2) the actual start of the palliative phase. During the Delphi process, six indicators for ACP were identified, such as presence of frequent falls and first unplanned hospital admission. The start of the palliative phase involved four indicators: 1) personal goals have started to focus on maximization of comfort; 2) care needs have changed; 3) PD drug treatment has become less effective or an increasingly complex regime of drug treatments is needed; and 4) specific PD-symptoms or complications have appeared, such as significant weight loss, recurrent infections, or progressive dysphagia. Indicators for both moments are included in the RADboud indicators for PAlliative Care Needs in Parkinson’s Disease (RADPAC-PD) tool.

Conclusion

The RADPAC-PD may support healthcare professionals in timely initiating palliative care for persons with PD. Identification of one or more indicators can mark the need for ACP or the palliative phase. We expect that applying the RADPAC-PD, for example on an annual basis throughout the PD trajectory, can facilitate identification of the palliative phase in PD patients in daily practice. However, further prospective research is needed on the implementation of the RADPAC-PD.

Introduction

Parkinson’s disease (PD) is a progressive neurological disease that affects physical, psychosocial and spiritual aspects of life [1–3]. Initially, people with PD may experience relatively stable periods, but debilitating symptoms develops over time progressively, many of which do not respond adequately to any medical treatment. PD is viewed as a life-limiting disease, hence a palliative care approach may meet the needs of patients and caregivers [4, 5].

The World Health Organization (WHO) defined palliative care as “an approach that improves the quality-of-life of patients and their families facing problems associated with life-threatening illness, through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment of pain and other problems, physical, psychosocial and spiritual” [6]. Palliative care was initially developed for patients with incurable diseases such as cancer. But palliative care can also be beneficial for patients with a chronic progressive disease trajectory, such as heart failure, dementia and COPD. Meanwhile, palliative care in PD is widely advocated [4, 5, 7, 8]. Early qualitative studies [9–11] have shown that patients with advanced PD have palliative care needs. Late-stage PD is associated with considerable disability that is comparable to that of end-stage cancer [12, 13].

Although the potential need for palliative care is increasingly acknowledged, still little is known about effective and useful components in PD patients [4, 5, 14]. There is no clear conceptualization of palliative care in PD and as a result, many healthcare professionals experience difficulties in providing palliative care [15–18]. A typical general misconception is that palliative care is associated with cancer, terminal phase care or dying. Furthermore, healthcare professionals find it difficult how and when to start with palliative care or when to refer to specialist palliative care services [15–18]. The difficulty of identifying palliative care needs is likely explained by the slowly progressive nature of PD, with often no clear defining moment for starting with palliative care (unlike e.g. cancer where progression is usually much faster and the timing to start palliative care is often clearer) [4, 5]. Earlier studies pointed out that patients with PD mentioned difficulties to access palliative services [4, 5]. Another problem in not recognizing palliatieve care needs is that physicians may hesitate to discuss progression of the disease in early disease stages–as they fear diminishing hope [4]. Also patients have indicated a conflict of needs: wishing to receive more information on disease progression and death, while fearing to receive the information (“wanting but not wanting,” “an information tension”) [9]. Richfield et al. [4] pointed out an integrated model of care characterized by close collaboration between neurologist and palliative care specialists, from the time of diagnosis onwards. Besides, the US patient and caregivers council and the European Parkinson’s Disease Association (EPDA) recommends palliative care to be available from the time PD is diagnosed [19, 20].

Not recognizing palliative care needs can lead to unnecessary treatments. In studies of non-cancer chronic diseases, patients received fewer drugs for palliation than patients with cancer [21, 22]. Furthermore, as many persons with PD have substantial cognitive impairment, the process of advance care planning (ACP), in which communication about preferred future health and healthcare is pivotal, might start too late. In palliative care, ACP is important for providing information and support tailored to a persons’ needs and wishes. In a small study of patients with PD, only a few had had end-of-life care discussions [23]. Furthermore, a majority of people with PD die in a care home or hospital according to a report by Public Health England [24]. However, many patients and their families indicate a preference for dying at home [25].

Generic tools are available to support healthcare professionals in identifying patients who might benefit from palliative care, such as the Supportive & Palliative Care Indicators Tool (SPICT), the Gold Standards Framework (GSF-PIG) and the RADboud indicators for PAlliative Care Needs (RADPAC) [26–28]. Also the use of a single ‘surprise question’ [29]: ‘Would I be surprised if this patient died in the next 12 months?’ can help professionals to identify palliative care needs. However, a systematic review on the use of the ‘Surprise Question’ showed that this tool performs poorly, and even worse in a population of non-cancer illness, as a predictive tool for death [30]. Furthermore, none of these generic tools are been used in patients with PD. Only, a few studies in PD suggest warning signs for unmet palliative care needs that might trigger healthcare professionals to refer a patient with PD to specialized palliative care [4]. These warnings signs include clinical features associated with causes of death, or features such as recurrent aspiration pneumonia, visual hallucinations, regular falls, dementia) [4, 31, 32]. In this study, we aimed to systematically develop a set of indicators using mixed methodology that can help professionals in proactively providing palliative care for persons with PD.

Methods

We performed a mixed-methods study including ten individual interviews and three focus group interviews with healthcare professionals (step 1), followed by a three-round modified Delphi study to reach consensus on PD-indicators (step 2). Data were collected from September 2016 till May 2018.

Ethics

Ethical approval was received from the ethics committee Arnhem-Nijmegen [number; 2016–2424]. Healthcare professionals received oral and written information about the study and written and/or oral consent was obtained. The participating healthcare professionals were not compensated for their contributions to this study. All personal data such as names and work location were anonymised. Informed consent was stored securely in a locked cupboard and electronic data (interview and focus group transcripts, quantitative data) was stored in password protected documents on a secure RadboudUMC server.

Design

Step 1: Individual and focus group interviews

Individual and focus group interviews were held to gain insight in palliative care for PD from the perspective of healthcare professionals. An interview guide was developed starting from the research gap and questionnaire results (unpublished data) [33]. The guide was discussed and amended if needed by HL, MS and MG. An expert panel, consisting of three healthcare professionals and two researchers with experience in either PD, palliative care or both, reviewed this version and adjusted it. The final version consisted of four topics, each comprising multiple open-ended questions (S1 Appendix). We developed one interview guide for both the individual interviews as well as the focus group discussion. We attempted to use the strengths of both methods as we used the individual interviews to solicit individual views and experiences and in contrast, the focus group discussions served to engage the professionals in further in-depth discussions. The discussion format in the focus groups encouraged interaction between group members and elicited discussion about issues that had not emerge in the individual interviews.

Two of the authors (HL or MS) held individual semi-structured interviews with 10 healthcare professionals. Each interview took between 60 and 90 minutes, and was held at the professional’s place of work or other preferred location. Thereafter, we conducted three focus group interviews at a central location in the Netherlands, which lasted between 80 and 100 minutes. The sessions were chaired by either MG or MM, assisted by either HL or MS. One served as a moderator who fostered an active and open discussion; the other took notes (S1 Table). There was no prior relationship between the interviewers and the participants; before the start of the interview, only the interviewers’ names and occupations were mentioned. The number of healthcare professionals in the focus groups ranged from 8 to 10. Step 1 was performed from September 2016 till March 2017.

Step 2: A modified three round Delphi study

A Delphi study was performed consisting of three rounds to achieve consensus on the statements that had emerged from step 1. For all three rounds, online questionnaires were sent using Castor EDC platform to the same panel members. Confidentiality of individual responses was ensured by the processing of coded data. To stimulate discussions about the ACP and palliative care statements, and to avoid a semantic discussion, the panellists had beforehand received a definition of ACP and a model of care goals developed for people with dementia [34, 35]. The ACP definition we used has recently been developed in an international setting and is supported by the European Association for Palliative Care (EAPC) [34].

Round 1 started off with 34 draft statements distributed over four domains: 1) general statements on Advanced Care Planning (ACP); 2) general statements on palliative care in PD; 3) indicators for the ultimate moment to initiatie ACP; 4) indicators for the start of the actual palliative phase. We used a five-point scale to evaluate the statements (1 = strongly disagree—5 = strongly agree; options 2–4 were not labelled).

In round 2, we included revised statements from round 1 as well as new indicators. In total 52 statements were provided to the panellists. New indicators were based on feedback from the panellists on open-ended items. General statements on ACP and palliative care were also evaluated on the five-point scale. Indicators for timing of ACP and of the palliative phase were all evaluated on a three-point scale: 1 = no signal, 2 = a supportive signal, 3 = an individual (isolated) signal (see Additional files 3 and 4: Statements for Advance Care Planning and Palliative care).

In the third and final round, the respondents rated two sets of indicators and nine additional statements on the same five-point scale as used in round 1. Six statements were newly added to round 3 based on feedback from round 2. Round 1 was open from 9 February to 6 March 2018 (25 days); round 2 from 20 March to 3 April 2018 (16 days); and the final round 3 from 12 April to 15 May 2018 (33 days). In each round, we sent out two reminders to non-responders.

Selection of participants

Step 1: Individual and focus group interviews

We recruited only healthcare professionals from the Dutch ParkinsonNet [36] who met the following inclusion criteria: registered professionals who over the last two years, treated and supported a person with PD who subsequently died [33]. ParkinsonNet is a Dutch professional healthcare network with nationwide coverage, consisting of 70 regional networks which encompass healthcare professionals specialized in PD (n = 3,171) [37–39]. The central idea is that persons with PD should be treated preferentially by a small group of selected professionals with a high degree of expertise in PD [40]. All ParkinsonNet healthcare professionals were sent an email in which they were asked if they would be willing to elaborate on the topic of palliative care in PD in a semi-structured interview or focus group interview. Purposive sampling was employed to ensure that the ultimate sample represented a diverse range of healthcare professionals and characteristics such as age, sex, experience and professional background. We invited healthcare professionals who had expressed willingness to participate for either an individual or focus group interview. Standard procedures were employed for obtaining informed consent from the professionals who eventually participated.

Step 2: A modified three round Delphi study

For step 2, we recruited healthcare professionals via ParkinsonNet as well as via the Dutch Palliative care networks. Inclusion criteria for participating in this Delphi study were: 1) being a registered healthcare professional; 2) having at least 5 years’ of experience in the field of PD or palliative care, and 3) currently active in clinical practice. We sought for three potential types of end-users of the tool: those with specific expertise regarding care for PD patients but not necessarily with palliative care, those with specific expertise on PD and palliative care, and those with expertise on palliative care but not specifically for PD patients. We also ensured that different disciplines relevant to palliative care in PD were represented. A total of 51 professionals agreed to participate, out of the 56 who had been invited.

Data collection and analysis

Step 1: Individual and focus group interviews

All semi-structured interviews and focus group interview were audio-taped and transcribed. We used an inductive analysis, involving the conceptualization of themes from the transcripts. Two researchers (HL & MS) read and reread the transcripts and, by means of using open coding, coded the first four transcripts of the individual interviews. To increase the coding reliability, all transcripts were initially coded by HL and MS separately. Open codes were compared and discussed until an initial codebook was established. Next, all interviews and focus group transcripts were analyzed based on the codebook independently. Codes were discussed, added, modified or merged if necessary. After coding three interviews and two focus group interviews with the codebook, no new codes emerged and data saturation was reached. Afterwards a process of sorting and classifying codes into subthemes and themes started. When differences in interpretation between researchers remained, a third senior researcher (MG) was consulted. The reliability of the findings was further enhanced by scrutiny from the research team, which included researchers and practicing clinicians. Once consensus was reached, a final set of themes and subthemes was decided upon [41–43]. The software package Atlas Ti-8 supported the qualitative data analysis. We further followed the reporting adhered to the consolidated criteria for reporting qualitative research (S1 File) [44].

Step 2: A modified three round Delphi study

The panellists’ responses were used to calculate the levels of agreement [45, 46]. Median ratings of each statement were calculated after each round. A percentage of 70 or higher of respondents rating 4 and 5 on the five-point scale was considered as an acceptable level of agreement. If necessary, and based on the feedback from panellists, statements were discussed by the workgroup (HL, JTvdS, MG, ZV) and revised, except for statements with a percentage below 30. In each round, the panellists were invited to give feedback on each statement. The feedback was used to improve readability and phrasing of questions. The research team summarized the feedback and scores from previous rounds and introduced this information before the second or third round started. The analyses were performed using SPSS (version 25.0).

Results

A detailed description of characteristics of healthcare professionals in the individual interviews, focus group interviews and Delphi study is presented in S2 Table. Three main themes and seven subthemes were identified based on data analysis of the individual interviews and focus group interviews.

Unclear concept of palliative care in PD

Although healthcare professionals identified palliative care as an important aspect of their practice, perceptions of palliative care varied. Some healthcare professionals found that palliative care equated to terminal care, while others had a broader perception of palliative care. A misinterpretation of palliative care rendered healthcare professionals reluctant to discuss palliative care with people with PD or other healthcare professionals. Many of them were not familiar with the WHO definition of palliative care [6] Once the WHO definition had been introduced during the course of the interview, it appeared that many healthcare professionals had the general feeling that this was not fitting the care for people with PD from diagnosis onward. Only a few healthcare professionals noted that palliative care starts at the time of diagnosis. However, the majority of healthcare professionals argued that starting palliative care right after a PD diagnosis was not appropriate (Table 1, Q1).

Table 1. Themes and subthemes from the individual interviews and focus group interviews.

Main theme Subthemes Quote number Quote
Unclear concept of palliative care in PD Perceptions of palliative care Q1 In principle, I don’t think a patient with PD right after diagnosis is per se a “palliative patient”. People can still live a very long time with the disease. (individual interview, physiotherapist)
Lack of defining palliative care I think it is a difficult question, to talk about palliative care from diagnosis. I don’t see it that way. People can live with PD for more than 30 years. On the other hand, PD care and palliative care overlap. The focus in palliative care is on quality of life. But, considering PD, from diagnosis you can only suppress symptoms. PD care is about, how can I live the best possible life with the disease. (individual interview, occupational therapist)
Discussions about needs and wishes for future care Timely speaking about future care Q2 Especially in PD, you need to speak timely about what a person’s needs are. I often notice that it is too late, that a patient with PD develops severe cognitive problems, so that he cannot speak for himself anymore. In fact, you need to prevent that (focus group interviews)
Stigma Q3 It is just the terminology, because I relate palliative care to dying. If a person is just diagnosed with PD, I do not think of the term death. However, I think that the goals of care are much identical (individual interview, nurse practitioner)
Family dynamics The question is whether the term palliative is too complicated for people. You should consider the best way to bring the message. Treatment of the disease is not meaningful, comfort and giving meaning to it, that’s what is should be about. I don’t care about which term you use as a professional. It can be palliative, but I have a different association with this term, more like end-of-life care (focus group interviews, neurologist)
Initiating palliative care Two marking moments Q4 This is such a clear and obvious moment: a neurologist says I have not many medical options anymore. Honestly, I think it is fine, but say it. Most patient do know, because they do not see the advantage of going to a neurologist anymore. Patients say “I’ll go for a talk but there is little value”. In a way, everyone feels that this moment is coming and that there are many PD medical options left. However, doctors don’t speak it out loud. I’m convinced that you should speak about this moment and hand over the care of a patient to a GP. (individual interview, elderly care physician)
Need for knowledge on ACP and role and responsibilities
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Discussions about needs and wishes for future care

Many healthcare professionals reported that a realistic conversation about disease stage, prognosis, possible therapeutic options and disadvantages of proposed treatments is important, but often not performed. Furthermore, discussions about future care (and care goals) should be initiated timely, definitely before cognitive impairment or communication problems arise (Table 1, Q2). However, as e.g. cognitive impairment declines gradually, it often seems unpredictable when a person with PD still can or can no more communicate coherently about his or her wishes for future care. Several professionals had experienced that addressing these important conversations with people with PD came too late.

Another important issue raised during individual interviews and focus group discussions was that healthcare professionals often did not talk about palliative care because of the stigma attached to it (Table 1, Q3). Healthcare professionals argued that speaking about future care too early might lead to depressive feelings in persons with PD. Besides, healthcare professionals further mentioned challenges in communicating with people with PD and their families. They felt that there was a need for an open communication style between the person with PD, their families and healthcare professionals. Family dynamics were not always seen in positive terms, while often communication with the person with PD was not possible due to communication problems and cognitive impairment.

Initiating palliative care

Healthcare professionals mentioned the implementation of palliative care interventions throughout the course of the disease to relieve symptoms. They argued that two specific marking moments in a PD trajectory should be discerned: 1) for initiating ACP discussions; and 2) for starting the actual palliative phase. It was emphasized that the process of ACP should be separated from ‘a palliative phase’ in order to avoid postponing speaking about ACP to a moment when the patient him- or herself can no longer be involved. Healthcare professionals defined ‘the palliative phase’ as a period when they should actively identify palliative care needs or when care goals focuses more on comfort. A number of indicators for both moments were proposed during the individual interviews and the focus group discussions (Table 1, Q4). However, none of them was felt to be a key indicator on its own. Furthermore, health care professionals suggested that not only the knowledge about ACP should be improved, but that it also should be made clearer by whom ACP must be initiated.

Delphi process

Statements which did reach consensus on ACP and palliative care are presented in S3 Table. Furthermore, results from rounds 1, 2 and 3 are presented in S2 Appendix. Fig 1 shows the final RADPAC-PD tool.

Fig 1. RADPAC-PD.

Fig 1

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Statements on palliative care

Our panel suggests that patients with PD are eligible for palliative care and that the support of patients with PD should include palliative care. The statement that PD is an illness you could die from was supported by only half of the panellists (S2 Appendix Table, round 1: statements 15) It was argued that patients do not directly die from PD, but are more likely to die from complications or co-morbidities. Therefore, this statement was rephrased and split into three separate statements (S2 Appendix Table, round 2: statements 13, 14, 15). Furthermore, it was stated that palliative care is multidimensional and pays attention to an individual’s wellbeing in the physical, psychological, social and spiritual domains. It was suggested that professionals should take a patient’s need as the leading principle in the decision-making process, even if this is contrary to wishes of the family. With regard to the roles of different professionals, there should be a shared responsibility for identifying the onset of the palliative phase according to our panellists. Timely identification was seen as important, as well as the provision of palliative care in accordance with the patient’s needs and wishes for future care.

The participants agreed on indicators for the start of the palliative phase, with two general indicators and two disease-specific indicators. The first referred to the moment when the preferred goal of care moves towards maximization of comfort. Other important indicators related to transitions in care, such as recurrent unplanned hospital admissions, nursing home admission or an increase in ADL-support. Furthermore, an important disease-specific indicator was the moment when PD drug treatment becomes less effective or increasingly complex. Complications such as significant weight loss, recurrent infections, progressive dysphagia, neuropsychiatric problems and multiple falls were identified as PD-specific indicators. There was no agreement on the value of the surprise question as an additional indicator for marking the onset of the palliative phase, nor on the minimum number of indicators for the RADPAC-PD that should be present to identify onset of a patient’s palliative phase.

Statements on ACP

Advance care planning was seen as an important part of optimal palliative care. All respondents agreed with statements that ACP discussions can reduce anxiety and uncertainty. However, only the panellists with expertise in palliative care agreed that information about the prognosis can help patients to prepare better for future decision making. The panellists did not agree about the moment of initiating ACP. Some commented that ACP should be provided shortly after diagnosis. No consensus was reached on the statements about starting ACP at a certain period after diagnosis. Indicators for the initiation of ACP were found to be more helpful. Again, we found general and disease-specific indicators. A person’s individual’s readiness stage was suggested as an important indicator for panellists to start with ACP. The panellist agreed that all professionals can play a role in facilitating ACP, although a leading role herein was envisaged for the primary treating practitioner. It was mentioned that currently, physicians and nurses lack the required competencies and skills to discuss ACP.

Discussion

An important new finding from this study is that healthcare professionals suggest two important marking moments in a PD disease trajectory: 1) the ultimate moment to initiate ACP; and 2) the start of the actual palliative phase. Differentiating these two moments might help professionals to discuss needs and wishes of palliative care with a person with PD before he or she looses decisional capacity. Recognizing a palliative phase can contribute to evaluate appropriate care goals that are in line with the actual (medical) situation of a person with PD. Participants emphasized that the process of ACP should start earlier, even before the palliative phase. But this might also be due to the fact that ACP was not seen as part of palliative care by healthcare professionals. Many healthcare professionals emphasized the need for ACP as cognitive problems may already be present even at an earlier stage of PD trajectory [47]. Many of patients with PD will eventually develop dementia [4, 48, 49]. Therefore, professionals emphasized that the process of ACP should be separated from the palliative phase in order to avoid that a person with PD can no longer be involved due to a lack of decision-making capacity and communication problems. The suggested indicators that could contribute to specify both marking moments included dysphagia, dementia, weight loss, and falls, among other things. The indicators were either PD-specific symptoms or general indicators such as recurrent hospital admissions and more support needed for activities of daily living. Some of these indicators have also been described in earlier studies as triggers to initiate palliative care in PD [4, 31, 32].

This study also supports earlier findings that healthcare professionals experience difficulties in the conceptualization of palliative care for people with PD. Only fifty percent of our panellist in the Delphi study agreed on the statement that PD is a disease one can die from. Therefore, we doubt whether healthcare professionals regard PD as a terminal illness. As is known from studies in the field of dementia, healthcare professionals who do recognize a disease as terminal are more likely to initiate palliative care [35, 50]. In this study, many healthcare professionals report different views on palliative care and often equated palliative care with terminal care. Results from the individual and focus group interviews shows that professionals working in PD were not familiar with the WHO definition and more recent insights on palliative care, which was also found in earlier qualitative studies [16–18, 51]. Discussions about what essential elements are in palliative care for people with PD resulted in several specifications, such as ‘discussions about future care’ and ‘care goals focusing on comfort’.

Recognizing a palliative phase can contribute to evaluate appropriate care goals that are in line with the actual (medical) situation of a person with PD. However, different opinions about the time of the palliative phase were identified in the individual and focus group interviews. Participants emphasized that the process of ACP should start earlier, even before the palliative phase. But this might also be due to the fact that ACP was not seen as part of palliative care by healthcare professionals. Many healthcare professionals emphasized the need for ACP as mild cognitive impairment may already be present even at the moment of diagnosis [47]. Averaged across all stages, about a quarter of patients with PD develop dementia [48, 49], but ultimately, most will develop at least some form of dementia [4, 48, 49]. Therefore, professionals emphasized that the process of ACP should be separated from the palliative phase in order to avoid that a person with PD can no longer be involved due to a lack of decision-making capacity and communication problems. The suggested indicators that could contribute to specify both marking moments included dysphagia, dementia, weight loss, and falls, among other things. The indicators were either PD-specific symptoms or general indicators such as recurrent hospital admissions and more support needed for activities of daily living. Some of these indicators have also been described in earlier studies as triggers to initiate palliative care in PD [4, 31, 32].

Our Delphi study aimed to develop a tool that exists of a set of indicators for both marking moments. Finally, we had consensus on six indicators for the ultimate moment to initiate ACP and four indicators that might presume the start of a palliative phase. Furthermore, consensus was reached on eight statements on elements of ACP and seven statements for elements for palliative care.

We found no agreement about timing ACP after diagnosis (in months till years after diagnosis) in our Delphi study. This is in line with findings from a study by Rietjens et al [34] that found that ACP can be initiated at any stage of a person’s life, but that it should be more targeted when the health condition worsens. Other studies also show that ACP should be introduced when the individual person is ready [34, 52–54]. Both elements are presented in our set of indicators for initiating ACP. We further developed elements that could be helpful in implementing ACP in practice. As earlier studies [5, 14, 15, 55] describe difficulties in role and responsibility on this topic in PD, we found consensus on statements that give direction on how, what and by whom ACP could be performed. Our findings suggest that healthcare professionals of all disciplines do have a role or are entitled to introduce ACP. But final responsibility on the implementation of ACP rests on the primary treating practitioner. In line with this Rietjens et al [34] described consensus on the fact that a trained non-physician facilitator can support an individual in the ACP process. Van der Steen et al. [35] underlined a multidisciplinary approach to communication and shared decision making in people with dementia. Our results suggest in more detail a responsibility for the primary treating practitioner.

We identified four indicators in the disease trajectory of a person with PD that healthcare professionals considered signals to start the actual palliative phase. We found that all professionals have a role in identifying onset of the palliative phase. We did not found consensus on how many indicators should be present in order to identify the onset of a patients’ palliative phase. However, our panellist did agree on the fact that for initiating ACP at least two indicators should be present. We recommend that for the ultimate moment to initiate ACP at least two of six indicators are present. For the start of the actual palliative phase initiating at least one indicator should be present. Applying the RADPAC-PD, for example on an annual basis throughout the PD trajectory, can facilitate identification of PD patients’ palliative phase in daily practice. Our study found no consensus on adding the ‘surprise question’ to the RADPAC-PD. However, earlier research has found that the surprise question combined with an additional screening instrument seems to have a higher validity to identify patients likely in need of palliative care in specific conditions [26, 28, 56]. Further prospective research is needed on the implementation of the RADPAC-PD.

In this study, healthcare professionals report difficulties in recognizing palliative care needs because of the individual patient`s variability in clinical presentations and their rate of disease progression. We therefore suggested to develop a specific PD identification tool which includes some clinical indicators that are equated with the prognostic indicator guide of the Gold Standards Framework (GSF-PIG) and SPICT [26, 28]. Compared to the RADPAC-PD (which includes 5 PD-specific indicators out of 10), the GSF and SPICT include more different indicators relevant to the patient’s general health for COPD, heart failure or cancer. An important difference is that these general instruments only provide an indication of the start of the actual palliative phase, while the introduction of the RADPAC-PD suggests two marking moments in a PD disease trajectory of each individual patient.

This study describes the systematic development of the RADPAC-PD based on qualitative research and a Delphi study. We do not yet have evidence about the applicability of this instrument. We acknowledge that further research is needed on the implementation of the RADPAC-PD.

Strengths & limitations

The high response rate from panellists suggests that palliative care is perceived as relevant to clinical practice. Nevertheless, selection bias cannot be ruled out, with preferential inclusion of professionals who are already interested in providing palliative care. We did not perform member checking with the study participants for the individual and focus group interviews. However, the research team members regularly discussed data, coding and themes throughout analyses. Results from the interviews and focus group discussions were used as input for the Delphi study in which we searched for agreement. We acknowledged bias, maintained neutral, and objectively presented the methods and procedures for enhancing the rigor of research findings in the research process. Furthermore, whether the RADPAC-PD can support professionals in practice in offering palliative care is unknown. In a follow-up study, we will evaluate the usefulness of the RADPAC-PD. Additionally, as more evidence becomes available about its usefulness, we may find new arguments to further adjust the RADPAC-PD. Furthermore, the RADPAC-PD tool was developed in the Dutch medical landscape. International and cultural differences in providing care for patients with PD may affect the usefulness in other countries or other healthcare settings. We do expect that this tool can help healthcare professionals to identify two specific moments in a PD trajectory. The RADPAC-PD tool is a first instrument that separates those two important moments and can be a valuable contribution to the care for people with PD.

Supporting information

S1 Table. Researchers’ characteristics.

(DOC)

Click here for additional data file. (62KB, doc)
S2 Table. Characteristics of participants.

(DOC)

Click here for additional data file. (69KB, doc)
S3 Table. Statements and ratings for palliative care and ACP.

(DOC)

Click here for additional data file. (88KB, doc)
S1 Appendix. Interview guide for individual interviews and focus group interviews.

(DOC)

Click here for additional data file. (59KB, doc)
S2 Appendix. Statements and ratings for palliative care and ACP from round 1, 2, 3.

(DOCX)

Click here for additional data file. (38.8KB, docx)
S1 File. COREQ checklist.

(PDF)

Click here for additional data file. (490.3KB, pdf)
S2 File

(XLSX)

Click here for additional data file. (20.4KB, xlsx)

Acknowledgments

We thank healthcare professionals who participated in the study for their support of this study.

Abbreviations

PD

Parkinson’s Disease

SPC

Specialist Palliative Care

WHO

World Health Organization

COREQ

Consolidated criteria for reporting qualitative research

GP

General Practitioner

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

This study is funded by The Netherlands Organization for Health Research and Development (ZonMw). (Grant reference number 80-84400-98-086). www.zonmw.nl Prof. Bastiaan R. Bloem was supported by a research grant of the Parkinson’s Foundation. The funding party had no role in the design of the study, or in data collection, analysis or in writing the manuscript.

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Decision Letter 0

César Leal-Costa

6 Dec 2019

PONE-D-19-24988

RADPAC-PD: a tool to support healthcare professionals in timely identifying palliative care needs of people with Parkinson’s disease

PLOS ONE

Dear drs Lennaerts,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

While both reviewers saw merit in the manuscript, a number of issues were raised. I understand that the authors use a Delphi process, but it does not appear to have been used in practice. I consider whether, in its current form the manuscript will contribute to the base of academic knowledge, which is a requirement for publication. The remaining queries from the reviewers are clearly expressed.

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Additional Editor Comments (if provided):

I understand that the authors use a Delphi process, but it does not appear to have been used in practice. I consider whether, in its current form the manuscript will contribute to the base of academic knowledge, which is a requirement for publication.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

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Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Dear Authors,

I think your paper entitled “RADPAC-PD: a tool to support healthcare professionals in timely identifying palliative care needs of people with Parkinson’s disease” is quite interesting and useful for the whole society. In particular, I think your paper is very useful to improve the activity of health care providers and the welfare of patients and their families.

Parkinson Disease is, like Alzheimer Disease or other neurodegenerative illnesses, one of the critical issues that should be strongly addressed in this century. Both, patients and their families as well as care providers integrate a complex system conditioning the evolution of the disease. Your paper is useful in this process because it can be used to relieve suffering in all the actors involved. Although I think your work deserves to be published, I also think there are some points in the manuscript needing some improvement. As a result, I provide some suggestions here below. I hope my comments and suggestions help you to develop an even better version of your manuscript.

In my view, the mean weakness of the paper is in the theoretical background. I think the introduction is too short. For example, one of the main problems of the introduction is that there is no clear definition of “palliative care”. I think you should provide a theoretical contextualization of the term and related key words (like, for example, “Advanced Care Planning”. Otherwise, misconceptions might arise. Regarding to this, note that in your paper you complain about misconceptions when the transcription from the expert panel is presented (see Table 1, Q1 and Q2). The first sentence in discussion section stresses that idea and, therefore, I think a richer background at introduction will be positive for readers. If you do so, your readers will contextualise better your proposal.

I also find it difficult to assess the usefulness and the impact of the tool you have designed without clearer interpretation rules. For example, the last paragraph in section “Statements of palliative care” addresses that issue but your explanations are not clear for me. When is a practitioner supposed to consider seriously the study of an Advance Care Planning or the beginning of a palliative phase? Is it when one single item has been satisfied? Or, for example, is the number of satisfied items a measure of the urgency for Advance Care Planning or the beginning of a palliative phase? I think these issues deserve a few comments.

I think it would be great if you said whether you compensated the experts for participating in the study (step 1: individual and focus groups interviews). I also think it would be positive if you could provide indices of agreement between experts (for example, percentage of agreement or Cohen’s Kappa coefficients).

There are also some minor issues I would like to give advice about. Firstly, I recommend citing the scientific literature before ending the sentence and not otherwise. For example, in the first sentence the citation is introduced after the dot and I think it should appear before (it appears like: “…. aspects of life.[1-3]”, and I think it is better way: “…. aspects of life [1-3].”).

Secondly, I suggest not using the word “confirmed” in the first sentence of the section “Statements on palliative care”. In my opinion, the sentence with this verb gives the sensation of a strong result or conclusion. In scientific terms things are not so clear sometimes, especially in health and social sciences. Please, consider using another verb like, for example, “agree”.

Finally, I recommend not using abbreviations in Figure 2. I think it will be clearer for readers.

That is all from me, I hope you find my comments and suggestions useful and constructive.

Yours faithfully,

dr46

Reviewer #2: The aim of this study was to develop a tool that can help healthcare professionals in timely identifying palliative care needs in people with PD. Even though the aim can be of interest and it is well written, the manuscript has important problems.

ABSTRACT

- In Methods the authors only present the design. Please include more information about the sample and the analysis methods

INTRODUCTION

It is not clear, in the last paragraph, the need to develop a new specific instrument when instruments already exist, which although generic, include specific sections for the assessment of palliative needs in PD. Which are the problems of these generic tools for their use in PD?.

METHODS

In terms of samples, it is necessary to clarify what the inclusion and exclusion criteria were used for the interviews, focus group and subsequently for the Delphi study.

Related to step 1, it is necessary to clearly separate the methodology by which the interviews were conducted and the methodology by which the focus groups were conducted. For example: the same interview guide was used in the interviews and focus groups, is it not clear?

Related to the analysis of step 1, were transcripts returned to participants? If not, it would be included in limitation section.

There are discrepancies, in the description of step 2 and figure 1, in the number of new indicators which the authors introduce in rounds 2 and 3, they need to be revised. Where do these new indicators come from?, this information is not clear in any section of the article.

Figure 1 is difficult to understand quickly, so it does not do its job well. As far as possible, it should be simplified.

RESULTS

In S4 “Table 2 Characteristics of participants” should include frequency and percentage of participants in each cells.

The analysis in step 1 have important limitations. The authors present the main themes, but they do not describe subthemes neither codes, which are included. As presented, the results do not know which topics were more frequent or were mentioned more in the interviews/focus groups. It would be necessary to include a table with this information. Quotations should be identified by codes, at least if they were identified in interviews or focus groups and placed in quotation marks. In addition, the results do not appear to have been contrasted with participants, which is an important limitation. These questions cast doubt on the credibility of the results.

The presentation of step 2 results appears to be a mere list of statements in no order and confuses the reader. Moreover, as in methods it is not clear how the authors arrive at the set of indicators, the results are very dubious and confusing.

On the other hand, information included S6 Appendix is not mentioned text.

All tables should include the number of participants (n)

DISCUSSION

The authors try to discuss the results, but it is not clear how useful the indicators are, at least those linked to the patient's prognosis, since there are generic instruments for this. However, it seems of greater relevance to have indicators to identify when to start an ACP.

The lack of basic data on applicability and psychometric properties makes it difficult to conclude that these indicators are useful for clinical practice with patients with PD.

REFERENCES

There are errors in the formats of many bibliographic references (e.g., reference 1, 3, 6, 8, etc.). All of them should be reviewed.

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2020 Apr 21;15(4):e0230611. doi: 10.1371/journal.pone.0230611.r002

Author response to Decision Letter 0

19 Feb 2020

To the Editors of PlosOne

date your letter dated phone fax

February 2020 +3124-3614701

subject your reference e-mail enclosures

submission of MS herma.lennaerts@radboudumc.nl

Dear sir Heber,

Thank you for giving us the opportunity to resubmit our manuscript for possible publication in PlosOne. We hereby submit an improved and rewritten version of our manuscript entitled “RADPAC-PD: a tool to support healthcare professionals in timely identifying palliative care needs of people with Parkinson’s disease.” [PONE-D-19-24988].

We appreciate the time and effort of the editor and reviewers in a new evaluation of this manuscript. We have revised the manuscript based on the earlier comments. Below, we provide point-by-point responses to these comments and textual proposals for the manuscript. We have uploaded a marked-up copy of the manuscript as well as an unmarked version of the revised paper.

We hope that our revised manuscript can be accepted for publication.

Thank you for your consideration.

Sincerely,

Also on behalf of the co-authors,

Herma Lennaerts, MSc

Radboud university medical center

Department of Anesthesiology, Pain and Palliative Care

Geert Grooteplein Noord 21 (route 549)

P.O. Box 9101

6500 HB Nijmegen

The Netherlands

Response to the editor

We are very grateful for the helpful and constructive comments on our manuscript. Below we provide our point-by-point responses.

Editor’s comments

1. While both reviewers saw merit in the manuscript, a number of issues were raised. I understand that the authors use a Delphi process, but it does not appear to have been used in practice. I consider whether, in its current form the manuscript will contribute to the base of academic knowledge, which is a requirement for publication. The remaining queries from the reviewers are clearly expressed.

This study describes how we systematically developed a tool for healthcare professionals which can help to timely provide palliative care. We therefore used a mixed-method design, comprising qualitative research followed by a Delphi study. The qualitative research concerned a thematic analysis to search for patterns and meanings on palliative care for PD. We performed an online Delphi study during the period from February 2018 till May 2018 according to a method described by Linstone et al.[1] We understand that this was insufficiently clear in our original submission, and this is now clarified better in the revision.

Our results contribute new academic knowledge to the field because there is no evidence or tool yet that can help professionals in identifying palliative care needs. Besides results from the Delphi study, further clarify important topics in palliative care (who, when and what) in which no research in PD is available. Furthermore, the tool we developed suggests two specific marking moments in PD rather than a single moment, which is of added value to other generic tools for identifying palliative care needs. The RADPAC-PD in its current form can be used in daily clinical practice, because it is underpinned by both evidence and consensus. Future research can focus on the actual implementation in daily clinical practice. Results of the guidance on ACP and palliative care strategies through the Delphi study can already help in developing palliative care and contribute to academic knowledge.

Reviewer 1 comments

1) In my view, the mean weakness of the paper is in the theoretical background. I think the introduction is too short. For example, one of the main problems of the introduction is that there is no clear definition of “palliative care”. I think you should provide a theoretical contextualization of the term and related key words (like, for example, “Advanced Care Planning”. Otherwise, misconceptions might arise.

We understand your comment, and have now expanded our introduction with a more in-depth theoretical background and definitions of palliative care and ACP. This can be found on page 3, lines 62-113

2) Regarding to this, note that in your paper you complain about misconceptions when the transcription from the expert panel is presented (see Table 1, Q1 and Q2).

The WHO definition does describe palliative care as “an approach that improves the quality-of-life of patients and their families facing problems associated with life-threatening illness, through the prevention and relief of suffering by means of early identification and impeccable assessment and treatment of pain and other problems, physical, psychosocial and spiritual” [2]. Nevertheless, despite the fact that we provided this definition, there is confusion and divergent interpretation of the definition which can induce misconceptions. Our results confirm this notion and are consistent with findings in the field of PD and palliative care [3, 4]. This is now clarified better in the revised version of the paper.

3) The first sentence in discussion section stresses that idea and, therefore, I think a richer background at introduction will be positive for readers. If you do so, your readers will contextualize better your proposal.

We trust that by having added richer background information on palliative care and related terms, better contextualization is possible. We described explicitly which misconceptions we found, as these are the basis of the RADPAC-PD and general statements on palliative care and ACP. We rewrote both the introduction section and the discussion section to better explain the context and background for developing the RADPAC-PD.

4) I also find it difficult to assess the usefulness and the impact of the tool you have designed without clearer interpretation rules. For example, the last paragraph in section “Statements of palliative care” addresses that issue but your explanations are not clear for me. When is a practitioner supposed to consider seriously the study of an Advance Care Planning or the beginning of a palliative phase? Is it when one single item has been satisfied? Or, for example, is the number of satisfied items a measure of the urgency for Advance Care Planning or the beginning of a palliative phase? I think these issues deserve a few comments.

To provide further information on the usefulness and interpretation rules of the RADPAC -PD, we have now added on page 14-15, lines 378 - 387, the following paragraph:

We did not find consensus on how many indicators should be present to mark the onset of a patient’s palliative phase. However, the panellists did agree that for initiating ACP, at least two indicators should be present. We recommend to initiate ACP if at least two of six indicators are present. Furthermore, at least one indicator should be present to start the actual palliative phase initiating. Applying the RADPAC-PD, for example on an annual basis throughout the PD trajectory, can facilitate identification of PD patients’ palliative phase in daily practice. Further prospective research is needed on the implementation of the RADPAC-PD.

5) I think it would be great if you said whether you compensated the experts for participating in the study (step 1: individual and focus groups interviews).

We added on page 5, line 123, the following sentence:

The participating healthcare professionals were not compensated for their contributions to this study.

6) I also think it would be positive if you could provide indices of agreement between experts (for example, percentage of agreement or Cohen’s Kappa coefficients).

We now present percentages of agreement for all respondents. The supplement additionally provides agreement percentages for two groups, those with expertise in PD only and those with expertise in palliative care only. We did not calculate Cohens’ Kappa coefficients as our aim was not to calculate inter-rater reliability between single indicators.

7) There are also some minor issues I would like to give advice about. Firstly, I recommend citing the scientific literature before ending the sentence and not otherwise. For example, in the first sentence the citation is introduced after the dot and I think it should appear before (it appears like: “…. aspects of life.[1-3]”, and I think it is better way: “…. aspects of life [1-3].”).

Thank you; we verified all references and made further adjustments based on criteria of PLOS One.

8) Secondly, I suggest not using the word “confirmed” in the first sentence of the section “Statements on palliative care”. In my opinion, the sentence with this verb gives the sensation of a strong result or conclusion. In scientific terms things are not so clear sometimes, especially in health and social sciences. Please, consider using another verb like, for example, “agree”.

We agree and have now replaced ‘confirmed’ with the more appropriate scientific term “suggest”. This can be found on page 11, line 283

Our panel suggests that patients with PD are eligible for palliative care and that the management of patients with PD should include palliative care.

9) Finally, I recommend not using abbreviations in Figure 2. I think it will be clearer for readers.

On page 11, Figure 2, we have now described these terms in full.

Reviewer 2 comments

10) In Methods the authors only present the design. Please include more information about the sample and the analysis methods

We rewrote our method section and have added more information about the sample and analysis methods. We divided this section into three parts (headed: design, selection of participants, and data analysis) to further enhance comprehensibility. This can be found on page 5 – 8.

11) It is not clear, in the last paragraph, the need to develop a new specific instrument when instruments already exist, which although generic, include specific sections for the assessment of palliative needs in PD. Which are the problems of these generic tools for their use in PD?.

Thank you for raising this topic. On the basis of our qualitative research, we found a need for two specific marking moments, rather than just one. The healthcare professionals emphasized that the process of ACP for people with PD is different from the identification of ‘a palliative phase’. These two moments are important in order to avoid postponing speaking about ACP to a moment when the patient can no longer be involved. The need for two marking moments is specific for PD and is not addressed in the more generic instruments. We developed a new instrument because the participating healthcare professionals mentioned specific PD issues that might be different from, for instance, COPD or heart failure.

12) In terms of samples, it is necessary to clarify what the inclusion and exclusion criteria were used for the interviews, focus group and subsequently for the Delphi study.

We applied two inclusion criteria for the interviews and focus group discussion: 1) being an active member of ParkinsonNet; 2) being a registered healthcare professional who has treated and supported a person with PD in the past 2 years and who subsequently died. We rephrased the paragraph in which step 1 (page 7, line 178) is described to start with the description of the inclusion criteria.

We recruited only healthcare professionals from the Dutch ParkinsonNet [5] who met the following inclusion criteria: registered professionals who during the last two years, treated and supported a person with PD who subsequently died [6].

We also clarified the inclusion criteria for the Delphi study on page 7, line 192 by adding the following sentence:

Inclusion criteria for participating in this Delphi study were: 1) being a registered professional caregiver; 2) having at least 5 years of experience in the field of PD or palliative care and 3) currently active in daily practice.

13) Related to step 1, it is necessary to clearly separate the methodology by which the interviews were conducted and the methodology by which the focus groups were conducted. For example: the same interview guide was used in the interviews and focus groups, is it not clear?

We further clarified individual interviews and focus group interviews at page 5 lines 135 - 140. We added the following text:

We developed a single interview guide for both the individual interviews and the focus group interviews. The individual interviews served to solicit individual views and experiences. In contrast, the focus group discussions served to engage the professionals in further discussions. The discussion format encouraged interaction between group members and elicited discussion about issues that had not emerged from the individual interviews.

14) Related to the analysis of step 1, were transcripts returned to participants? If not, it would be included in limitation section.

No, the transcripts were not returned to individual interviewees and focus group participants. However, the research team members regularly discussed data, coding and themes throughout analyses. We added this limitation on page 15, line 403 – 408:

We did not perform member checking with the study participants for the individual and focus group interviews. However, the research team members regularly discussed data, coding and themes throughout analyses. Results from the interviews and focus group discussions were used as input for the Delphi study in which we searched for agreement. We acknowledged bias, maintained neutral, and objectively presented the methods and procedures for enhancing the rigor of research findings in the research process.

15) There are discrepancies, in the description of step 2 and figure 1, in the number of new indicators which the authors introduce in rounds 2 and 3, they need to be revised. Where do these new indicators come from?, this information is not clear in any section of the article.

We now further describe how new indicators emerged in rounds 2 and 3 in the following section, which is included in the manuscript on page 6, lines 164 – 174:

In round 2, we included revised statements from round 1 as well as new indicators. In total 52 statements were provided to the panellists. New indicators were based on feedback from the panellists on open-ended items. General statements on ACP and palliative care were also evaluated on the five-point scale. Indicators for timing of ACP and of the palliative phase were all evaluated on a three-point scale: 1 = no signal, 2 = a supportive signal, 3 = an individual (isolated) signal (see Additional files 3 and 4: Statements for Advance Care Planning and Palliative care).

In the third and final round, the respondents rated two sets of indicators and nine additional statements on the same five-point scale as used in round 1. Six statements were newly added to round 3 based on feedback from round 2. Round 1 was open from 9 February to 6 March 2018 (25 days); round 2 from 20 March to 3 April 2018 (16 days); and the final round 3 from 12 April to 15 May 2018 (33 days). In each round, we sent out two reminders to non-responders.

16) Figure 1 is difficult to understand quickly, so it does not do its job well. As far as possible, it should be simplified.

We have now provided the information from the table in the manuscript at page 6, lines 129 – 174, and deleted figure 1.

17) In S4 “Table 2 Characteristics of participants” should include frequency and percentage of participants in each cells.

We adjusted S4 “Table 2 Characteristics of participants” and included the above-mentioned values (marked in yellow).

18) The analysis in step 1 have important limitations. The authors present the main themes, but they do not describe subthemes neither codes, which are included. As presented, the results do not know which topics were more frequent or were mentioned more in the interviews/focus groups. It would be necessary to include a table with this information.

We have changed Table 1 and have added main themes and subthemes. However, we did not present the frequencies in which themes, subthemes or codes were mentioned. Qualitative data analyzed with a content analysis method can include frequencies at which a topic is mentioned. However, this is not the same for a thematic analysis method in which it is unusual to rate how often a phenomenon is mentioned. A specific item mentioned by only one respondent can be very valuable in understanding the research topic.

19) Quotations should be identified by codes, at least if they were identified in interviews or focus groups and placed in quotation marks. In addition, the results do not appear to have been contrasted with participants, which is an important limitation. These questions cast doubt on the credibility of the results.

To clarify the origin of the quotes, we included after each quote whether it came from an individual interview or a focus group discussion. Three main themes and seven subthemes emerged after analyzing the qualitative material from part 1. We choose in our first draft not to present all subthemes for reasons of readability. However, we acknowledge that this might confuse readers. We therefore changed table 1.

The reviewer also mentioned the topic of a member check earlier. We have not discussed the results with participants. However, research team members regularly discussed data, coding and themes throughout analyses. We added this limitation on page 15, line 403 – 408.

20) The presentation of step 2 results appears to be a mere list of statements in no order and confuses the reader. Moreover, as in methods it is not clear how the authors arrive at the set of indicators, the results are very dubious and confusing.

We rewrote our result section in order to improve readability. In the first place, we described at point 15 how new indicators were developed for rounds 2 and 3. Secondly, we present in the manuscript only statements and the final set of indicators that achieve consensus after round 3. Further, in other to clarify how we arrive the set of indicators, we added in the appendix all results from rounds 1, 2 and 3.

21) On the other hand, information included S6 Appendix is not mentioned text.

Thank you for pointing this out. We added a sentence on page 11, line 279 to introduce S6 Appendix.

22) All tables should include the number of participants (n)

We added the number of participants to all tables in the manuscript.

23) The authors try to discuss the results, but it is not clear how useful the indicators are, at least those linked to the patient's prognosis, since there are generic instruments for this. However, it seems of greater relevance to have indicators identifying the moment when to start an ACP.

Based on both reviewers’ comments on the discussion, we rewrote this part and added information about the RADPAC-PD in relation to generic instruments and the need for two marking moments, usefulness of the RADPAC-PD and why it is needed. We rewrote the discussion part at page 15 added following text on the relation of the RADPAC-PD and generic tools (lines 387 – 395):

In this study, healthcare professionals report difficulties in recognizing palliative care needs because of the individual patient`s variability in clinical presentations and their rate of disease progression. We therefore developed a specific PD identification tool to support healthcare professionals. This tool includes clinical indicators that are equated with the prognostic indicator guide of the Gold Standards Framework (GSF-PIG) and SPICT.[7, 8] The GSF and SPICT include more different indicators relevant to the patient’s general health for COPD, heart failure or cancer, than does the RADPAC-PD (which includes 5 PD-disease specific indicators for PD out of 10). Furthermore, while these general instruments only provide an indication of the start of the actual palliative phase, the introduction of the RADPAC-PD suggests two marking moments in a PD disease trajectory of each individual patient.

24) The lack of basic data on applicability and psychometric properties makes it difficult to conclude that these indicators are useful for clinical practice with patients with PD.

Of course, the applicability and psychometric properties of the RADPAC-PD need further prospective investigation. In the current study, we describe the process of development of the RADPAC-PD, an important step in acceptance and use. We might have been too strong in our recommendations about the usefulness for clinical practice without scientific evidence about the applicability. We therefore added the following sentence at the end of the discussion, page 15 lines 396 - 398:

This study describes the systematic development of the RADPAC-PD based on qualitative research and a Delphi study. We do not yet have evidence about the applicability of this instrument. We acknowledge that further research is needed on the implementation of the RADPAC-PD.

25) There are errors in the formats of many bibliographic references (e.g., reference 1, 3, 6, 8, etc.). All of them should be reviewed.

We reviewed all bibliographic references based on PlosOne criteria policy.

REFERENCES

1. Linstone HA, Turoff M. The Delphi method: techniques and applications. Addison-Wesley, editor1975.

2. WHO definition of palliative care. 2015. http://www.who.int/cancer/palliative/definition/en/ Accessed on 14 May 2015.

3. Waldron M, Kernohan WG, Hasson F, Foster S, Cochrane B. What do social workers think about the palliative care needs of people with Parkinson’s disease? British Journal of Social Work. 2013;43. doi: 10.1093/bjsw/bcr157.

4. Fox S, Cashell A, Kernohan WG, Lynch M, McGlade C, O’Brien T, et al. Interviews with Irish healthcare workers from different disciplines about palliative care for people with Parkinson’s disease: a definite role but uncertainty around terminology and timing. BMC palliative care. 2016;15(1):1-9. doi: 10.1186/s12904-016-0087-6.

5. Bloem BR, Rompen L, Vries NMd, Klink A, Munneke M, Jeurissen P. ParkinsonNet: a low-cost health care innovation with a systems approach from the Netherlands. Health Affairs. 2017;36(11):1987-96.

6. Lennaerts H, Groot M, Steppe M, van der Steen JT, Van den Brand M, van Amelsvoort D, et al. Palliative care for patients with Parkinson's disease: study protocol for a mixed methods study. BMC palliative care. 2017;16(1):61. doi: 10.1186/s12904-017-0248-2. PubMed PMID: 29178865; PubMed Central PMCID: PMCPMC5702094.

7. National Gold Standards Framework Centre England. Gold Standards Framework. http://www.goldstandardsframework.org.uk/evidence (accessed 15 Nov 2018).

8. Highet G, Crawford D, Murray SA, Boyd K. Development and evaluation of the Supportive and Palliative Care Indicators Tool (SPICT): a mixed-methods study. BMJ supportive & palliative care. 2014;4(3):285-90. doi: 10.1136/bmjspcare-2013-000488. PubMed PMID: 24644193.

Decision Letter 1

César Leal-Costa

5 Mar 2020

RADPAC-PD: a tool to support healthcare professionals in timely identifying palliative care needs of people with Parkinson’s Disease

PONE-D-19-24988R1

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Acceptance letter

César Leal-Costa

12 Mar 2020

PONE-D-19-24988R1

RADPAC-PD: a tool to support healthcare professionals in timely identifying palliative care needs of people with Parkinson’s Disease

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Associated Data

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    Supplementary Materials

    S1 Table. Researchers’ characteristics.

    (DOC)

    Click here for additional data file. (62KB, doc)
    S2 Table. Characteristics of participants.

    (DOC)

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    S3 Table. Statements and ratings for palliative care and ACP.

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    S1 Appendix. Interview guide for individual interviews and focus group interviews.

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    S2 Appendix. Statements and ratings for palliative care and ACP from round 1, 2, 3.

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    S2 File

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