Barriers and facilitators of communication about off periods in Parkinson’s disease: Qualitative analysis of patient, carepartner, and physician Interviews

Background Successful patient-physician communication is critical for improving health outcomes, but research regarding optimal communication practices in Parkinson’s disease is limited. The objective of the current study was to investigate barriers and facilitators of communication between persons with Parkinson’s disease, carepartners, and physicians, specifically in the setting of off periods, with the goal of identifying ways to improve patient-carepartner-physician communication. Method We interviewed persons with Parkinson’s, carepartners, and physicians (specialists and non-specialists) using a semi-structured questionnaire to identify and describe experiences, barriers, and facilitators relating to communication about off periods in Parkinson’s disease. We used a qualitative descriptive approach to analyze interview transcripts and compare themes between participating groups. Results Twenty persons with Parkinson’s and their carepartners and 20 physicians (10 specialists, 10 non-specialists) participated in interviews. Identified communication barriers included patient-level (e.g. cognitive impairment, reluctance to discuss symptoms), caregiver-level (e.g. caregiver absence), and physician-level (e.g. distraction by technology, lack of appreciation of the burden of off periods) factors. Other barriers included the challenging nature of off periods themselves. Positive physician characteristics such as empathy, respect, and taking time to listen were major facilitators of communication regarding off periods. Persons with Parkinson’s, carepartners, and physicians described using various tools (e.g. home diaries, questionnaires, mobile phone videos) to aid communication regarding off periods but participants identified a need for more formal educational materials. Conclusions Physicians caring for persons with Parkinson’s can improve communication through more patient-centered practice but there is a need for improved educational tools regarding off periods. Further research is needed to identify optimal strategies for communication about off periods and preferred approaches for off period education.


Introduction
draft of the manuscript but had no role in study design, data collection, analysis, or decision to publish.
Competing interests: MJA receives compensation from the American Academy of Neurology for work as an evidence-based medicine methodology consultant and serves on the level of evidence editorial board for Neurology and related publications (uncompensated). She receives research support from ARHQ (K08HS24159), a 1Florida ADRC (AG047266) pilot grant, and as the local PI of a Lewy Body Dementia Association Research Center of Excellence. In the 5 years prior to submission, she also was a local investigator for studies sponsored by the Parkinson Study Group, the Huntington Study Group, the CHDI Foundation, Abbvie, Biotie, and Insightec and she received funding as a sub-investigator or local investigator on the NIH grants U01 AR057967-01, U01NS080818-01A1 and U01NS080840-01A1 (until 2015). She was a consultant on a TBI endpoints development (TED) seed grant 2016-2017. She receives royalties from the publication of the book Parkinson's Disease: Improving Patient Care and she has received honoraria for presenting at the Movement Disorders Society congress (2013,2014) and the AAN annual meeting (2014-2017) and participating in Medscape CME. TR and ARG have declared that no competing interests exist. CM has served as a consultant for Acorda Therapeutics. She receives honoraria for serving on the steering committee for the Michael J. Fox Foundation and for teaching from EMD Serono. She receives research support from the Michael J. Fox Foundation, Canadian Institutes of Health Research, Parkinson Foundation (U.S.), NIH, and International Parkinson and Movement Disorders Society. This does not alter our adherence to PLOS ONE policies on sharing data and materials. physician communication. Off periods are times when PD symptoms that respond to medication reappear or worsen-usually at the end of a treatment dose-resulting in functional disability. Re-emergent symptoms can include both motor (e.g. stiffness, slowness, tremor) and nonmotor (e.g. cognitive, mood) features [16]. Off periods were selected as the framing context for the study given the complexity of the phenomenon, its frequency (~40% of patients 4-6 years after starting treatment) [17], poorer associated health-related quality of life [18,19], and association with treatment decisions [20].

Design
An exploratory research design involving qualitative interviews with PwP, carepartners, and physicians (specialists and non-specialists) was chosen to thoroughly identify and describe communication experiences, barriers, and facilitators [21]. This was part of a larger study investigating off period experiences. A qualitative descriptive approach [22] was used to conduct and analyze interviews. This approach aims to explicitly report experiences without intending to use or generate theory. The University Health Network Research Ethics Board provided approval for this study (file number 16-5880). All participants provided written informed consent prior to interview. Consolidated criteria for reporting qualitative research [23] guided the reporting of study findings (S1 Checklist).

Population and recruitment
Patients and carepartners. Convenience sampling was used. U.S.-based PwP and care partners were recruited via emails to the Parkinson Disease Foundation Care Partner 2016 Summit mailing list and posting of study information on Fox Trial Finder (2/13/17-10/16/17), a matching tool connecting PwP to research studies. Interested individuals responded by email, telephone, or through the Fox Trial Finder message system. Inclusion criteria for PwP were a PD diagnosis, presence of off periods, U.S. residence, and having a carepartner also willing to be interviewed. Consent forms were emailed to volunteers and returned to the study team prior to the interview. Potential participants had the opportunity to discuss questions by telephone with an investigator. Investigators and participants had no pre-existing relationships.
Physicians. Convenience sampling was used to recruit general neurologists and PD specialists working in the U.S. Invitations and consent forms were sent to U.S.-based movement disorder neurologists using the Movement Disorders Society mailing list. Interested participants contacted a study coordinator by telephone or email for further information. General neurologists were invited to participate through the American Academy of Neurology (AAN) members' online community forum Synapse as well as through a presentation at the general neurology section meeting at the annual AAN conference. Because these strategies were unsuccessful for meeting recruitment targets, most general neurologists were recruited by a recruitment agency (Sermo) using an email introduction sent by the recruitment agency. The agency shared the consent form with interested physicians. Sermo provided signed consent forms to the study team to schedule interviews. General neurologists needed to evaluate at least 10 PwP monthly to meet inclusion criteria.

Data collection
Investigators performed a preparatory systematic review which showed that (1) off periods are among the most troublesome symptoms to PwP, with a broad-ranging impact on patient and carepartner activities, (2) PwP and caregiver understanding of off periods is suboptimal, and (3) communication regarding off periods is largely unstudied [14]. Based on these results, investigators drafted semi-structured interview guides for PwP, carepartner, and physician interviews covering topics relating to experiences, barriers, and facilitators of communication to address literature gaps (S1 Interview guide). The guides were iteratively revised by authors with movement disorders (MJA, TR, CM) and qualitative research (AG, MJA) experience. Pilot testing occurred with at least one individual representing each of the target groups prior to finalization. Interviews were conducted by phone by a single investigator (TR), a neurologist obtaining movement disorders subspecialty expertise, who was trained and mentored by a PhD with qualitative methodological expertise (ARG). Investigators interviewed PwP and carepartners separately. Target interview length was 30-60 minutes for PwP and carepartners and 20-30 minutes for physicians. Interviews were audio-recorded with participant knowledge and professionally transcribed. Each participant received a $100 prepaid cash card by mail after interview completion except for physicians recruited through Sermo who received $140 based on their standard practices.

Analysis
Data were organized and analyzed using Microsoft Word and a qualitative descriptive approach [22]. One investigator (TR) independently analyzed transcripts to create a log of codes reflecting emerging themes and sample quotes (open coding). These were reviewed, revised, and discussed with the three other investigators to achieve consensus on emerging themes and expand or merge thematic codes (axial coding). Saturation was determined by discussion and consensus following completion of 20 interviews with each of the three groups. Themes, subthemes, and exemplar quotes were tabulated and summarized. MJA further categorized barriers and facilitators as patient-based, carepartner-based, physician-based, and "other" by referencing categories described in a prior systematic review [24]. Participant checking was not performed.

Results
Sixty subjects participated ( Table 1). All eligible patient and carepartner volunteers were included. Invitations were sent to 999 U.S.-based movement disorders specialists, 20 of whom expressed interest. Thirteen specialists agreed to participate and the first 10 were interviewed. All eligible general neurology volunteers were included. Interviews occurred between March and November 2017. Participating carepartners were mostly spouses (17, 85%; other: son, brother-in-law, close friend). Nine (45%) of participating PwP received care from a general neurologist; the remainder received specialty care. Mean interview duration was 39 minutes for PwP, 33 minutes for carepartners, and 21 minutes for physicians. Themes and select quotes are discussed here; additional quotes are summarized in S1 Appendix.

Barriers to communication
Patient-level factors. One of the main barriers described by both PwP and physicians was PwP difficulty describing off period experiences: That general feeling of uneasiness is very difficult to explain to the doctor or anyone for that matter (PwP3). General neurologists and specialists described that patient recall of symptoms was an additional barrier ( Table 2). Disease-related symptoms such as cognitive impairment, trouble speaking, and anxiety hindered PwP communication regarding off periods: The biggest challenge is that sometimes just having Parkinson's, my brain don't want to work right and I forget stuff and, you know, I may forget to tell him about, maybe, certain symptoms (PwP13).
PwP admitted that pride, embarrassment, and an unwillingness to admit that something was happening limited what they raised with physicians. While carepartners did not identify many patient-level barriers, they reported that sometimes PwP were unlikely to report symptoms:

I tend to be more upfront and let [the doctor] know what's going on, where he's more wait and see, let's see if it gets worse, when we don't need to let it get worse, we need to just tell the doctor now (CP5).
The reluctance of PwP to report wearing off symptoms was unrecognized by physician participants.
Carepartner-level factors. PwP and carepartners reported that the lack of carepartners at clinical visits was the main carepartner-related barrier (Table 2). Physicians, on the other hand, reported challenges when carepartners had cognitive impairment themselves or when accounts from PwP and carepartners differed: You're running up against the difficulty of talking to someone and someone. . .and the patient saying one thing and the family member saying something else. And, there could be some disagreement and argument about it (GN6).
Physician-level factors. Physician-level barriers were described by PwP and carepartners but not by physicians themselves (Table 2). PwP described frustration that physicians do not appreciate the degree to which off periods impact daily life.
I guess maybe just drawing the line from the fact that I have these off periods to the fact that I think they're a major impediment to my life, and I think he thinks of them as just normal for Movement disorder specialists described the difficulty of distinguishing tremors during off periods from peak dose dyskinesias: A lot times patients misinterpret their dyskinesia as tremor and that can be confusing because when they're really on they think they're off and they're worried about that movement when it's really an on phenomenon (MDS10).
Specialists also reported challenges in identifying the presence of non-motor off symptoms: . . .So much of the time the off-periods are-so there are psychological symptoms, and if they're associated with obvious severe motor symptoms, then that's not hard to ferret out. But so many patients don't understand that the motor wearing off might be mild and the emotional symptoms might be much more severe (MDS7).
Related to these challenges is the lack of shared vocabulary about off periods, described by both PwP and physicians.
I also learned what an off period is, and that's what I'd been describing to my doctor as just the unevenness, I called it the unevenness before (PwP2).
Helping PwP understand what to expect, though, can be challenging: All symptoms vary quite substantially between individuals, so it's not sort of where I can say, here's a list of things, you know, more tremor or feeling slower or stiffer or things like that, because I think that people experience off differently (MDS2).
Clinical visit time was a barrier described by PwP, carepartners, and general neurologists, but not specialists. Lack of ancillary support (e.g. advance practice providers [APPs]) was a barrier for small general neurology practices.

Facilitators of communication
Identified patient-and carepartner-level facilitators were rare, though all groups agreed that having a carepartner present at visits was helpful (Table 3).
Physician-level factors. PwP valued physician traits such as empathy and respect.

Parkinson's is a very individual disease. And so you need somebody that's going to, you know, care about that and respect that and listen to you when. . . there's something really concerning you. I wouldn't bring this up if it wasn't important (PwP8).
Physician behaviors such as listening to PwP and carepartners, demonstrating interest and curiosity, and appreciating individual experiences were also identified facilitators:

You know, the doctors definitely are open to talking to both of us and, you know, I certainly get the feeling that he's as interested in what I observe as what my husband observes (CP12).
General neurologists described the importance of taking time to listen to PwP and carepartners:

I think trying to be cognizant of not being rushed when I'm actually in there. . . When I see a patient I actually don't-even though I have an electronic medical record-I actually don't type or work on EMR when I'm seeing a patient. So, trying to be present with them and having a conversation with them versus trying to do my data entry at the same time I'm talking to them (GN2).
Other clinical factors. General neurologists noted the value of longitudinal relationships over time, using the same questions each visit to facilitate patient understanding, and recognizing the importance of individual preferences (Table 3). PwP and carepartners described the value of in-person visits, though they also appreciated patient portals for communication between visits.
I still think the face to face conversations where I can ask him questions and he can give me answers or he can, you know, actually grab my arm and feel for rigidity or see how I walk across the room, I think those are the kinds of things that I benefit from the most (PwP3).
Tools to help symptom reporting. Interviewees described various tools as facilitators of communication regarding off periods. PwP and carepartners reported creating a list of concerns prior to clinic visits to guide discussion, sometimes using questionnaires to guide that preparation (Table 3). PwP also reported that using diaries and schedules was helpful if things weren't going well. One PwP described using a video to help his physician understand what was happening, but one carepartner felt that his loved one might feel "invaded" if he videotaped off periods.
General neurologists and specialists described using home videos and patient diaries to clarify patient symptoms, though several specialists described abandoning diary use given difficulty explaining instructions and overwhelming amounts of data. General neurologists also reported using questionnaires to streamline clinic interviews. Specialists described using levodopa challenges and wearable technology. Several specialists described the importance of intentionally developing a shared vocabulary: . . So then I write down, okay, your feet won't move, then I use their terminology and I write that down in the off column. And so then they take that piece of paper home and when they're filling out their diary, then they can look and say, now which one do I fit-the on or the off column-right now? So that's another tool (MDS7).

I give them kind of language because I think the most important thing is a shared language (MDS8).
Educational tools. Developing shared vocabulary was viewed as both a communication strategy and an educational tool. Other educational strategies included taking time to educate patients about off periods, often by sketching graphics (Table 3).

I'll draw a little, a little diagram for them, you know, where it's like being in the right window versus having too much and then having dyskinesias and then too little and feeling off (MDS5).
One specialist noted the particular importance of educating PwP about non-motor fluctuations. A general neurologist described using the teach-back method to ensure understanding. General neurologists reported using informal online videos to demonstrate symptoms and referring patients to online forums or local support groups. Numerous movement disorders specialists described the value of having allied health professionals and APPs to provide education informally or via scheduled training sessions.
Both general and specialist neurologists voiced interest in having video resources to teach people about off periods. Movement disorders specialists felt that having an educational page to send home with PwP would be helpful, whereas one general neurologist thought that a pamphlet would not be much use given the lack of associated visuals.

Discussion
PwP, carepartners, general neurologists, and movement disorder specialists identified numerous patient-level, carepartner-level, and physician-level barriers and facilitators to communication regarding off periods. In a prior study of advanced PD, PwP, carepartners, and physicians also identified lack of information, poor neurologist support, patient cognitive impairment, lack of caregiver involvement, and PwP-caregiver disagreements as barriers to decision-making [11], consistent with current results. The barriers identified in this study are also consistent with those reported by patients across diseases: patient uniqueness/variability, cognitive/physical impairments, poor physician listening, insufficient information/education, use of medical terminology, lack of time, lack of decision support, and differing expectations between patients and physicians [24]. While many of these barriers are relevant outside PD, the challenging nature of off periods is a unique barrier affecting many aspects of PwP-carepartner-physician communication. PwP described difficulty putting their off symptoms into words. Physicians described challenges correlating symptoms with medication dosing and identifying if there is a treatable fluctuation. Both parties highlighted the lack of a shared vocabulary.
Facilitators of communication described in this study and in the literature include presence of a caregiver for decision support, continuity of care, adequate time, respect, physicians taking time to listen, good communication, provision of information about options, and written decision support [11,24]. Strategies to supplement physician teaching and in-person visits (e.g. use of APPs, patient portals) were also facilitators of communication regarding off periods (Table 3). Successful communication regarding off periods, though, necessarily includes facilitators specific to this phenomenon. Pre-visit preparation and questionnaires were identified as facilitators of communication in our study, consistent with prior findings that using wearing off questionnaires was helpful in identifying fluctuations (particularly motor) [25,26]. Diaries, home videos, levodopa challenges, and wearable technology have utility in select circumstances, but patient/carepartner comfort with selected approaches and physician resources for conducting and/or interpreting these assessments, including the time needed to evaluate large amounts of data, may limit these approaches. Additionally, while 87% of PwP described interest in recording information to monitor symptoms in a survey, only 49% were actually doing so [27].
Our results highlight that lack of patient/carepartner education regarding off periods, lack of shared understanding of the concept between PwP and physicians, and limited physician appreciation of the personal impact of off periods are important modifiable communication barriers. These results are consistent with prior PD research demonstrating lack of education and understanding as barriers to PD care [5][6][7][8][9][10]. Physicians described the value of educational programs, classes, and online forums, but used verbal education and hand-drawn graphics in clinical encounters. Physicians desired video educational tools and handouts regarding off periods to improve education and communication, consistent with a known need for better patient education in PD [28]. These findings suggest an opportunity for Parkinson societies, patient organizations, centers, and physicians to develop off period video and print educational tools for use within clinical encounters, in community settings, and for patient and carepartner self-education. Subsequent to the conduct of this study, the Parkinson's Foundation published "Managing PD Mid-Stride," a booklet with text and figure-based education regarding off periods that addresses some of the needs identified by study participants [29]. Educational tools can potentially improve health related quality of life in PD [30] and medication adherence [31].
While it is not surprising that physicians neglecting to probe the daily impact of off periods, failure to engage carepartners in clinical visits, and distraction by technology impeded communication, physicians in our study appeared largely unaware of the ways they impeded communication about off periods. Opportunities for physicians to improve communication include allowing more time, involving carepartners, active listening, showing interest, asking about the personal impact of wearing off, avoiding distractions from technology, and providing education about off periods and what to expect (Table 4). These are common-sense approaches for patient-centered medical care, but they are important to specifically identify for clinicians given the experiences reported by participants in this study and studies showing PwP dissatisfaction with communication and the information they receive [5][6][7][8][9][10][11]. Identifying these facilitators also has implications for hospital system and clinic planning: clinicians need adequate time to assess patients and query the daily impact of off periods, clinical rooms designed to facilitate interactions of patients, families, and clinicians and seamlessly integrate technology, ancillary staff to support assessments and education, and opportunities for  (Table 4). Patients and carepartners can also take steps to improve communication with their medical team (Table 4).

Limitations
This study likely enrolled highly engaged PwP and carepartners and thus may not represent barriers and facilitators for patients who are less active in seeking information about their PD. Recruitment through an online research matching tool will underrepresent the views of those who do not use the internet as a communication method, though it is notable that even these connected PwP describe numerous communication barriers. Patients had to recognize that they have off periods to meet inclusion criteria, so the study lacks the views of PwP who have off periods but don't recognize them. General neurologists had to see at least 10 PwP monthly to participate, so this study did not capture the views of general neurologists with limited PD experience. All participating subjects were U.S.-based and this limits generalizability to other medical contexts. Response to physician recruitment strategies was low, consistent with other survey-and interview-based studies but also affecting generalizability.

Conclusions
Identified barriers and facilitators to communication between PwP, carepartners, and physicians regarding off periods include components related to communication generally and challenges relating to off periods in particular. Physicians caring for PwP can improve communication through more patient-centered practice but there is also a need for improved educational tools regarding off periods. Successful tool development will require PwP and carepartner involvement. Opportunities also exist for PwP, carepartners, and clinics/hospital systems to contribute to improved communication. Further research is needed to identify optimal strategies for communication about off periods and preferred approaches for off period education.
Supporting information S1 Checklist. COREQ checklist. COREQ 32-item checklist outlining the page where each element of qualitative research is reported.
(DOCX) S1 Interview guide. Semi-structured interview guides for PwP, carepartners, and physicians. This file includes the three semi-structured interview guides used for the study.
(DOCX) S1 Appendix. Qualitative coding. Coding tables for barriers and facilitators to communication about off periods for PwP, carepartners, and physicians. (DOCX)