Abstract
INTRODUCTION
In the advanced stage of Parkinson’s disease, neurologists and patients with Parkinson’s disease (PD) face a complex decision when choosing an advanced treatment. In moderate to advanced stages of PD, almost all patients develop motor and non-motor complications [1], which consist of unpredictable fluctuations between akinetic periods (off phase) and mobile periods (on phase), the latter often being complicated by dyskinesias. These complications negatively affect the quality of life [2]. It eventually becomes very difficult for many patients and their neurologists to manage the motor complications by adjusting oral medication. Deep brain stimulation (DBS), Levodopa-Carbidopa intestinal gel (LCIG), and continuous subcutaneous apomorphine infusion (CSAI) are the cornerstones of therapeutic management for such patients.
To reach an evidence-based treatment choice for this decision, shared decision-making (SDM) plays a vital, but too often neglected role. Evidence-based medicine was first defined as the conscientious and judicious use of current best evidence from clinical care research in the management of individual patients [3]. The authors further explain that it means one has to take into account not only the best research evidence available and the professional’s expertise, but also the patient’s preferences. In SDM, the provider and patient discuss the decision to be made and share the treatment options, available evidence, and the patient’s preferences regarding these options. Together, the provider and the patient reach a shared decision [4, 5]. The level of patient and professional involvement can differ depending on the patient’s preferences and circumstances [6].
Currently, there are several problems that hamper evidence-based practice for advanced PD treatments. First, no randomized controlled trials that compare these advanced treatments directly are available to guide the treatment decision [7]. Second, it appears that many patients are considered too late as potential candidates for DBS, LCIG, or CSAI, while some are never considered for these treatments. This leads to general under treatment of advanced PD [8]. Third, PD patients are involved in decision-making processes in all stages of the disease, but do not always have the opportunity to choose their therapy [9]. Focus group discussions indicate that PD patients, in general, prefer to become more involved, but they feel ill-equipped and unsupported by the medical specialist to do so [10].
In this study, we analyze if there is indeed a need for improvement of current evidence based practice in this decision for advanced therapies. We map current decision-making for advanced treatment options, analyze the characteristic factors of decision-making in this specific clinical situation, and explore the barriers and facilitators for evidence based decision-making among patients, their caregivers, and professionals.
MATERIAL AND METHODS
Study design
We have chosen a qualitative design as no previous studies have been published on current decision-making in advanced PD [11]. We used qualitative methods since they are particularly useful for describing and articulating stakeholder perspectives and they enabled us to obtain insight in the complex process of decision-making and to gain a deeper understanding of the behavior of everyone involved [11]. We conducted focus groups and interviews with patients and caregivers and conducted individual interviews with neurologists and PD nurse specialists in an iterative process. We chose focus groups to stimulate self-disclosure and to maximize exploration on different stakeholder perspectives in an interactive group setting reducing the influence of the interviewer to lead the discussion topic. The interview guides concentrated on current practice and the level of SDM in the decision-making process [12, 13]. The focus group and interview guides were designed using several decision-making frameworks, e.g., the Cabana model [14] and the Ottawa Decision Support Framework [15], and discussed with the research team before implementation. We followed the recommendations outlined in the COREQ criteria [16] to ensure trustworthiness throughout the qualitative study.
Selection of participants
Three focus group discussions with advanced PD patients with DBS or LCIG (N = 17) and three focus groups with their caregivers (N = 13) were conducted. Patients and their caregivers were recruited by neurologists at 11 Dutch hospitals and through an online request posted on the website of the Dutch Parkinson’s Disease Patients Association. We used purposive sampling [17] to select patients who had advanced PD and had undergone either LCIG, DBS, or both in the previous three years, and were willing to share their experiences of the decision-making process. Caregivers were asked to participate in separate focus groups to give them the opportunity to express and discuss experiences in the decision-making process that may conflict with their partner/next of kin. This was complemented by three individual semi-structured interviews with advanced PD patients with CSAI and their caregivers recruited by two different neurologists. These additional interviews were prompted by CSAI emerging as a third relevant treatment option in interviews with professionals and informal discussions with experts in the field. Conducting a focus group with CSAI patients was not feasible due to the small number of patients in the Netherlands who underwent this treatment. Individual interviews were used to evaluate whether patients with CSAI had different experiences than patients with DBS or LCIG.
Furthermore, we approached seven neurologists and three PD nurse specialists for interviews; all agreed to participate. We used purposive sampling to ensure diversity of professionals (i.e., from different types of hospitals with different treatment availability and with different levels of expertise). Participant details are given in Tables 1 and 2.
Data collection and analysis
Focus groups varied in size from three to eight participants [12]. Each focus group had a moderator who facilitated the group discussion and an observer who completed field notes and added question prompts as needed. Each focus group lasted two hours. The first author conducted the semi-structured interviews with CSAI patients, neurologists, and PD nurse specialists. The interviews lasted between 25 and 100 minutes. All focus groups and interviews were audio taped and transcribed verbatim. Transcript summaries were sent to all participants allowing them to reflect and comment on the data’s accuracy and validity (member validation) [17]. Two independent researchers (FN, JH) analyzed the data using thematic analysis [18] in an iterative process, which was supported by ATLAS.ti software (ATLAS.ti Scientific Software Development, Germany). The thematic analysis consists of several analysis steps which will be described further. The first step for the analyst was to get familiar with the data and start generating initial codes. A code is an interesting feature mentioned by the participants or an interesting observation from the interaction between the participants, which relates to the main research question. These initial codes were then clustered into categories. Categories represent a combination of codes that describe or relate to the same phenomena in a study. After this initial coding and clustering of codes, we started developing themes. Developing themes is the process of connecting codes and categories. These themes represent the interaction of codes and categories, and show patterns in the data. In an iterative process, each time new data emerged, we critically looked at the codes and reclassified the codes and categories and developed the themes further. When new topics were discovered in the analysis, these were included in the interview guides for the next focus group or interview until no new subjects emerged in the analysis [17, 19]. The analysis process and developed themes were discussed with the whole research team to ensure the themes and codes were representative for the data. Differences in interpretation were resolved in discussion, and consensus was reached on the codes, families, and main themes [18, 19]. The study protocol was approved by the Medical Ethics Committee of the Radboud university medical center and registered as 2011/085. All patients and caregivers gave written consent prior to the focus groups and interviews.
RESULTS
Our analysis led to four major themes of the decision-making process for an advanced PD treatment. Each theme consists of the patients’ and caregivers’ view and the professionals’ view and is clarified by illustrative citations.
Theme 1: Information and information needs
Patients and caregivers
Patients used many different information sources including the internet, pharmaceutical companies, professionals, the Dutch Parkinson’s Disease Patients Association, and experienced patients. Most patients felt they had to search for the scattered information themselves. Besides the standard information, patients were mainly interested in patient-tailored information that resulted in a large variety of different and very detailed information needs. Patients were satisfied with the information they had received, but realized that they had not received equivalent information about all treatment options. Patients felt professionals lacked knowledge about all treatment options, and patients and caregivers experienced that professionals emphasized their own treatment preferences. Some patients even discovered other treatment options for the first time during the focus group meeting. Missing information included CSAI as an option, psychological effects after DBS, the treatment’s long-term effects, the time to reach a treatment’s optimal settings, the role and effects of changing one’s current treatment, and the possibility and effects of discontinuing a new treatment.
Focus group 2 (Caregivers) interactive discussion
Participant 3: “We never heard much about Apomorphine or we have heard in the beginning something like you can let that option go, I do not remember anymore. It was not included as an option.”
Participant 1: “We also did not have that as an option. It was rejected here just like doctor X rejected DBS. My husband was first treated in Hospital X, but they rejected it. He was referred to Hospital Y because of the retirement of neurologist X who treated patients with Duodopa. But we have not received any information on Apomorphine and we could hardly find any information on the internet. I could just not imagine what the treatment would be like.”
Participant 2: “So, something must have been wrong with it right? What, I do not know.”
Participant 1: “I also do not know.”
Focus group 4 (Caregivers)
Participant 2: “There are people who consider the operation (DBS) so easy. It is just like removing a pimple. But it is so different for everyone. That was a disappointment for us, how serious the operation was, and we never thought of that beforehand.”
Professionals
Although no protocols existed, neurologists often gave general information, and PD nurse specialists gave practical details. Neurologists stated that the focus of information was often on one treatment, and when professionals reported that all three treatments were discussed, the type of information offered was not always equivalent. For instance, some centers had produced their own DBS information packages but used pharmaceutical folders for the other treatments. Furthermore, when patients were referred for information to other patients who had one of the treatments, they were directed to patients with the preferred treatment only, and not the alternatives. Professionals often gave more detailed information about the treatments available in their own center, although some referred patients to a center of expertise (on one or more of the treatments) for extra treatment information.
Interview 6 (Professionals) PD nurse specialist
“We have a patient information map for DBS, which we have made ourselves and we have videos of the pharmaceutical company. For LCIG there also some folders and a DVD. For Apomorphine a CD-ROM at least.”
Interview 10 (Professionals) neurologist
“Yes, I do give information. I always hand out the Duodopa folder. For DBS I have once designed a folder when I was still working in X, but it is too technical to give that to patients in the first stage (of decision-making). That (information) is only interesting when people have already thought about it and indeed I do not have alternatives for it.”
Interview 1 (professionals) neurologist
“I always offer patients the option to visit other patients, who already have experience with such a treatment. That applies to DBS, it applies to, in a lesser extent, apomorphine because we have fewer patients, and most patients get that treatment in another hospital. But for Duodopa and DBS I have patients that can be contacted.”
Theme 2: Factors influencing treatment choice and individual decision strategies
Patients and caregivers
An important observation was that several patients felt there was no choice; a change was inevitable because their quality of life was no longer acceptable. The treatment choice consisted of two components: the reasons for considering a new treatment and factors influencing the choice of a specific treatment (Table 3). The reasons for considering a new treatment were the current treatment’s side effects, unsatisfactory effect with the current treatment, a desire to reduce oral medication, and an unacceptable quality of life. The factors for choosing a specific treatment were very diverse and individually determined (Table 3). During the focus groups, patients were confronted with other participants who had different experiences, which revealed some relevant misconceptions such as the misconception that changing therapies is impossible (Table 3). The individual decision strategies ranged from deciding intuitively to balancing all pros and cons carefully. Some patients focused immediately on their first choice, not searching for information about alternatives. One patient added that he made a decision, although he felt he did not have enough information yet. Two patients said they would have chosen a different therapy if they had to choose again. Eight patients stated they would still choose the same therapy, although two would have more decisional conflict now that they have gained experience with the treatment. Patients highly valued another patient’s treatment experience for their own decision, although they also acknowledged the risk of developing unrealistic expectations toward the treatment if only one experience was taken into consideration. Caregivers, although they were closely involved, thought their own views were less important, and a few were afraid to discuss their worries and information needs in the patient’s presence.
Focus group 3 (patients)
Participant 3: “There is no choice. You are so far along in the disease that you have suffered so much and your quality of life is under such pressure. There is just no choice.”
Professionals
Provided that all treatments were viable options, five neurologists preferred DBS, and two neurologists preferred LCIG. All neurologists considered CSAI to be an eligible option. Importantly, neurologists emphasized the need to evaluate whether oral medication could still be optimized and suggested that continuing current treatment was a viable option. The PD nurse specialists based their preferences on each individual patient, but they also acknowledged that neurologists had a preference that they took into account. Personal treatment experience and treatment availability in their hospitals were important factors in treatment choice for the professionals. Neurologists acknowledged the clinical guideline but interpreted it differently, concluding that it did not give clear guidance. The extensive evidence for DBS was considered important, as were indications and contraindications for the treatments. Patient factors taken into account were the patient’s social background, ability to deal with the treatment’s daily care requirements, expectations, preference, and the burden on the patient (Table 4).
Interview 3 (professionals) Parkinson nurse specialist
“(I ask) What do you think of injecting yourself? What are your own expectations of the three therapies, and what is your preference? What do you think you will not be able to do anymore with these treatments? So (I try to create) a completely own view.”
Interview 9 (professionals) neurologist
“I think if patients are still eligible, DBS is the best option. That is the opinion internationally, right? First consider DBS if there are no contraindications, otherwise the other options.”
Interview 2 (professionals) neurologist
“Well in principle, if they are eligible, I most often give DBS.”
Interview 10 (professionals) Neurologist
“Well, I am very cautious with DBS, LCIG is easier accessible for many patients and we do not have experience with apomorphine yet in our practice.”
Theme 3: Roles in decision-making
Patients and caregivers
The patients described many different roles in decision-making (Supplement 1). Some patients took an active role and came with treatment suggestions to their neurologists. Others followed the neurologist’s advice on starting an advanced treatment. One caregiver decided for the patient, while all other caregivers played a supportive role. Although nobody felt that the neurologist made the decision (Supplement 1), some patients perceived that the professional had a large influence in directing the choice. This influence was both judged positive and negative. For instance some patients pointed out that the role of the neurologist was often as an advisor while others said the neurologist was biased with a preference or lacked knowledge and experience to give information on alternatives.
Focus group 6 (Caregivers)
Participant 5: “They (professionals) can direct you.“
Participant 2: “They have directed us as well; they directed us towards LCIG, though looking back we are happy with that.”
Professionals
Professionals often saw themselves as advising experts and valued the patient’s choice, although some acknowledged that they directed the patient with the information they provided. Professionals pointed out that their role depended a lot on the patient’s medical and personal characteristics (Supplement 1). They sometimes decided on behalf of the patient, assuming they knew the patient’s preference or judging the patient to be incapable of deciding, but patients could also get all freedom to decide themselves when the professional felt the patient was capable of that.
Interview 9 (professionals) neurologist
“I do discuss all three options (DBS, LCIG, and CSAI) and I describe that patients have very different preferences. So it (the treatment) has to suit you.”
Interview 7 (professionals) neurologist
“Well, you always decide together. But the question is how much we fool ourselves with that because it all depends on what information we give; we direct it a bit ourselves. Yes, that’s how it goes, and the patient can’t oversee all the options or can’t see all the consequences.”
Interview 2 (professionals) neurologist
“Apomorphine is discussed as well; I do not have such a good experience with apomorphine. I am a neurologist now for five years, and have worked here ten years as well as a resident and researcher. In the beginning we did some apomorphine and pumps (LCIG). It has changed a bit, but in essence we were not satisfied with that. I have to say I have patients who are not eligible for DBS or Duodopa, for example because they use anticoagulants. Yes, those are the patients that are very satisfied with apomorphine. But I do not discuss that during that conversation (on treatment options).”
Theme 4: Barriers and facilitators to shared decision-making
Patients and caregivers
Patients reported that a respectful relationship with the professional, good communication, and an involved partner facilitated the decision-making process. Personal decisional conflict, decision disagreement with the partner or neurologist, a lack of balanced information, a lack of support from the neurologist, the neurologist’s lack of knowledge about treatments, and the neurologist not involving the caregiver all formed barriers to reach a decision. The neurologist’s expertise was considered both a facilitator and a barrier in decision-making because it could increase information on options, but could also lead to the professional directing toward a decision.
Focus group 6 (caregivers) participant 3
“These people (professionals) will always talk about their own business (preach for their own church).”
Focus group 5 (patients)
Participant 8: “We were sent to another neurologist to get those pumps, but he did not have any experience yet. So when we asked, “Can you compare all options with the benefits and risks?” he said, “No, I just don’t have experience with those.””
Professionals
Important facilitators mentioned by the professionals were equality between professionals and patients, standardized and neutral information on all options, and creating more equal evidence on all treatments. Important barriers to SDM were the professionals’ lack of expertise with all treatment options, treatment availability in their own hospital, the professional leading the patient with the information he or she gives, the patient not having decision-making capacities, and SDM being too time-consuming.
Interview 10 (professionals) neurologist
“I discuss all three (options), but I do not discuss all three of them in that much detail. For patients it is already extremely new and unbelievable that you would do an operation, huh. So if you also announce that with a pump you can... (silent). I do believe to be honest that I discuss option one, so what is option one for me, that I already have made a decision for myself a bit.”
Interview 8 (professionals) neurologist
“DBS is not done often. That is because we feel so comfortable with LCIG, and it just feels nice to be able to offer it yourself and treat people yourself. And that creates the barrier for DBS for people because you have to [stops in the middle of the sentence]. Yes, I know that the indications make little difference, so maybe if you have a tremor-dominant patient, DBS might be slightly preferable, but it does not matter a lot for determining the indication. I do know that, but we still choose LCIG here.”
Interview 7 (professionals) neurologist
“Yes that’s right. But I do think that mainly one’s own experience with a certain treatment is decisive. If you have never treated a patient with apomorphine and you have not encountered it during your residency program, you will not be likely to start that treatment soon, and I hope you will not start that treatment soon.”
Interview 8 (professionals) neurologist
“If it (the decision process) will be shared, then I think you should take into account that the patient has the feeling, more than in current practice; he has an influence on the decision. Because if you look at it now, we (professionals) take the decision as we inform the patients in such a way that we say let us do that ... If it is more about shared decision-making, it should then be that the patient gets more objective information and independent of his doctor. I would not be able to do that, because I have a lot of experience with one (LCIG) and hardly any experience with the other (DBS) and with the last no experience at all (CSAI). You cannot expect me to give a balanced advice. I can’t, someone else should be doing that and our PD nurse specialist cannot either, so then we have a problem.”
DISCUSSION
The aim of this study was to explore the current decision-making process in advanced PD. We identified four important themes; Information and information needs, factors influencing treatment choice and individual decision strategies, roles in decision-making, and barriers and facilitators to SDM.
To be able to make a decision, information is crucial. Information needs were diverse among patients, but the most important finding was that patients were often not informed about all treatment options. Our findings are in line with the study by Lökk that showed that just a quarter of advanced PD patients were informed by their neurologist about the various advanced treatment options [20]. An evidence based choice cannot be made unless all options are known. It is important to use strategies to create better informed patients and professionals to reach an evidence-based treatment choice.
The factors in treatment choice varied substantially between individuals, highlighting the importance of including a patient’s individual context and preferences in a treatment choice [3]. Though similarities in factors between patients and professionals dominated, important different perspectives also became clear. Where professionals focused more on evidence and own expertise, patients relied on advice of the professional, other patient’s experiences and had very personal factors for treatment choice. Important to notice was the fact that patients mentioned some very relevant misconceptions that may have negatively affected their decision-making. Addressing the PD patients’ perspective to improve patient care has been highlighted in different studies [21–24]. To improve evidence based decision-making, the preferences and reasoning of the individual patient has to be known in order to prevent a preference misdiagnosis (i.e., the silent misdiagnosis) [25].
The roles in decision-making varied on a continuum of different levels of decision-making [6]. Our results showed that patients felt actively involved in decision-making, but realized afterwards that they were directed by the options offered by their neurologist and lacked balanced information. The professionals acknowledged that they directed the patients’ decisions with the information they gave. In our observations, patients often chose the professionals’ preference, which was often based on local treatment availability and treatment expertise. Although the professional’s clinical expertise is important in evidence based medicine [3], the professional can influence information transfer in both beneficial and harmful ways [26, 27].
Both patients and professionals mentioned several barriers and facilitators for SDM specific for this decision. Both pointed out that a lack of professional expertise with all treatments is a barrier to SDM. The neurologists’ lack of knowledge of advanced treatment options was recently reported internationally, and guidance about advanced treatments was advised [28]. An important facilitator mentioned was creating more equal evidence on all treatments to be able to compare these treatments. Professionals mentioned patients’ limited decision-making capacities as a possible SDM barrier. As SDM can be a strategy to implement evidence based practice, it is important to acknowledge barriers to SDM. Our study showed that the decision for advanced treatment options, comes with unique barriers, on top of those described in the literature [29, 30]
Strengths and weaknesses
This is the first study evaluating the decision-making process in advanced PD patients. Because no earlier studies were known, we used an explorative qualitative approach. Although we only have a small sample, purposive sampling made it possible to portray a broad spectrum of views of patients, their caregivers, and health care providers. Furthermore using the iterative process we continued with interviews and focus groups till data saturation emerged. The limitation of this qualitative study is that we do not know how representative this is for all the decision-making processes in advanced PD. To increase validity and to evaluate if these findings are consistent in the advanced PD cohort, a quantitative study in a large sample is recommended. The PD patients and caregivers were relatively well educated, which could have introduced a bias in how they perceive the decision-making process as it is known that higher educated patients are more likely to be actively involved in the decision-making process [31]. Another bias could be that most patients were satisfied with their treatment results. However, despite the positive results, patients had numerous suggestions for improvement for the decision-making process.
CONCLUSIONS
In this study we found several factors explaining why in current practice, evidence-based decision-making for advanced PD treatments is not optimal. The lack of professional expertise on all options, and the fact that patients are not aware of all options are important contributors. This study also highlighted the importance of including the patient’s preferences as they are highly individual. Though this study emphasized the need to improve this decision-making, we will first confirm these findings in a larger cohort through a quantitative study. This study was explorative and helped identifying the characteristics of the current decision-making process. This study, together with the quantitative analysis to confirm if findings are representative on a larger scale, can help identify strategies to improve evidence based decision-making in advanced PD.
CONFLICTS OF INTEREST
Abbott, Apotheekzorg, and Medtronic funded this study but had no influence on study design, data interpretation, or reporting. The authors report no other conflicts of interest.
Footnotes
ACKNOWLEDGMENTS
We would like to acknowledge all those who participated in the focus groups and interviews and shared their experiences. We thank Martijn van der Eijk, Ella Fonteyn, and Simone van der Burg for their help in conducting the focus groups.