ORIGINAL ARTICLE
Understanding patients ’ and caregivers ’ perspectives
and educational needs in Parkinson ’ s disease: a multi-ethnic Asian study
Xing Yan Choo1&Shen-Yang Lim1&Karuthan Chinna2&Yan Jing Tan1&Voon Wei Yong1&Jia Lun Lim1&Kar Foo Lau1&
Jing Yi Chung1&Jun Min Em1&Hui Ting Tan1&Jia Hwa Lim1&Seng Beng Tan3&Chong Tin Tan1&Ai Huey Tan1,4
Received: 29 January 2020 / Accepted: 3 April 2020
#Fondazione Società Italiana di Neurologia 2020 Abstract
IntroductionLittle is known regarding the educational needs and perspectives of people living with Parkinson’s disease (PD), particularly in Asia.
ObjectiveTo assess knowledge and perceptions regarding PD in a large multiethnic urban Asian cohort of patients and caregivers.
Methods We conducted a survey at a university hospital neurology clinic, using a novel Knowledge and Perception of Parkinson’s Disease Questionnaire (KPPDQ).
ResultsThe KPPDQ had satisfactory psychometric properties among patients and caregivers. Five hundred subjects were recruited with a 97% response rate (211 patients, 273 caregivers). Non-motor symptoms such as urinary problems, visual hallucinations and pain were relatively poorly recognized. Many (≈50–80%) respondents incorrectly believed that all PD patients experience tremor, that PD is usually familial, and that there is a cure for PD. About one-half perceived PD to be caused by something the patient had done in the past, and that PD medications were likely to cause internal organ damage. Issues of stigma/shame were relevant to one-third of patients, and 70% of patients perceived themselves to be a burden to others. Two- thirds of participants felt that PD imposed a heavy financial toll. Participants were about equally divided as to whether they would consider treatment with deep brain stimulation, tube feeding or invasive ventilation. Over three-quarters of patients expressed a preference to die at home.
ConclusionsImportant knowledge gaps, misperceptions and perspectives on PD were identified, highlighting the need for further efforts to raise awareness and provide accurate information regarding PD, and to address patient’s and caregivers’needs and preferences.
Keywords Parkinson’s disease . Knowledge . Perception . Perspectives . Patient-centred care . Caregivers . Asia
Introduction
Parkinson’s disease (PD) is the second most common neuro- degenerative disease worldwide after Alzheimer’s disease and is estimated to affect around 1% of people over the age of 60 [1]. PD is characterized clinically by resting tremor, bradyki- nesia, rigidity and postural instability [2]. Apart from these core motor features, patients also experience a wide array of non-motor symptoms (NMS) in the neuropsychiatric, sleep, autonomic and sensory/pain domains [3–6]. Recognition of these motor and non-motor symptoms is crucial for proper diagnosis and management of PD [3–6].
Electronic supplementary materialThe online version of this article (https://doi.org/10.1007/s10072-020-04396-4) contains supplementary material, which is available to authorized users.
* Ai Huey Tan [email protected]
1 Division of Neurology and the Mah Pooi Soo & Tan Chin Nam Centre for Parkinson’s & Related Disorders, Department of Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
2 School of Medicine, Faculty of Health and Medical Sciences, Taylor’s University, Kuala Lumpur, Malaysia
3 Division of Palliative Care, Department of Medicine, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
4 Neurology Laboratory, University of Malaya Medical Centre, 6th Floor, South Tower, 50603 Kuala Lumpur, Malaysia
https://doi.org/10.1007/s10072-020-04396-4
/ Published online: 20 April 2020
Improvements in socio-economic conditions in Asian- Oceanian countries have increased life expectancy, resulting in a shift in the global burden of PD from indus- trialized western nations to the east [1,7,8]. Thus, there is a growing need to ensure that people living with PD in this region possess adequate health literacy, which is fun- damental to their engagement in the healthcare process and has an important impact on health outcomes [5, 9, 10]. This is especially important in PD since prompt rec- ognition and management of symptoms improve function- al status and quality of life [11,12].
In medicine, there has also been a growing emphasis on delivery of patient-centred care [5,13] (i.e.“providing care that is respectful of, and responsive to, individual patients’needs and preferences”), as well as inclusion of patient and caregiver perspectives in research and regula- tory decisions [14]. Indeed, PD clinicians have recently advocated the concept of “person-centred care”, which also takes into account the welfare of others involved in the care of PD patients. This includes informal caregivers, whose lives are significantly affected by the disease, and who make major personal and societal contributions to the support of patients with PD [5, 15, 16]. Caregivers can sometimes also provide a more accurate appraisal of symptoms and treatment effects than patients who may have altered capacity to evaluate themselves [17]. An em- pathetic [5, 18] partnership approach to enhancing en- gagement, satisfaction with (and adherence to) treatment, and quality of life, is based on understanding (and valu- ing) patients’ and caregivers’ concerns and priorities [5, 14,17–20].
There are very few studies regarding patient/caregiver knowledge of PD in the Asian-Oceanian region [10,21, 22], and even less research has been done on patient/
caregiver perceptions [21]. Furthermore, questionnaires used in previous studies were limited by ambiguous word- ing and the inclusion of content that is contentious even among PD experts [10,23–25]. A recent consensus panel of movement disorder experts from Asia (with additional input from European and North American experts) found a
“clear disconnect between clinicians’versus patients’per- ceptions about PD”[19], and proposed a number of mea- sures to address this problem, including urgent attempts to try and understand and improve patient knowledge of PD [19]. This has come amid calls from multiple stakeholders highlighting increased research to characterize patient and caregiver preferences as a significant unmet need in PD and related disorders [14,26,27]. Hence, we aimed to assess the knowledge and perceptions of patients and caregivers in a large multi-ethnic urban Asian cohort, using an expanded version of a previously published questionnaire [10]. We have also conducted several tests to verify the psychometric properties of this instrument.
Methods
Sample and recruitment
In this cross-sectional study, consecutive patients and their caregivers were recruited from the neurology outpatient clinic from July 2018 to March 2019. Diagnosis of PD was assigned by movement disorder specialists according to the Queen Square Brain Bank Criteria [28]. Exclusion criteria were age
≤18 years and comorbidities preventing reliable completion of the questionnaire. The study received approval from the Medical Research Ethics Committee, UMMC. Written con- sent was obtained from all respondents.
Development of the Knowledge and Perception of Parkinson’s Disease Questionnaire (KPPDQ) A previously published Knowledge of Parkinson’s Disease Questionnaire (KPDQ) [10] was revised and expanded to pro- duce a Knowledge and Perception of Parkinson’s Disease Questionnaire (KPPDQ). This questionnaire consists of two components: knowledge (part 1) and perceptions (part 2) (see Appendix for the KPPDQ form). For knowledge, recognition of PD symptoms (5 motor and 11 non-motor) was tested using a“Yes/No/Do not know”format (Part 1A), and general PD knowledge was tested with 12 statements using a“True/False/
Do not know”format (Part 1B). For perceptions, nine do- mains with a total of 22 items (encompassing aspects of:
Burden of PD; Access to information and community sup- ports; Misperceptions regarding PD causation and treatment effects; Satisfaction with treatment and care; Complementary and alternative treatments; Stigma of PD; Assistance for dis- ability; Treatments for advancing disease; and Autonomy) were assessed using a Likert scale (“Strongly agree/Agree/
Disagree/Strongly Disagree”).
Each item of the questionnaire was appraised by five Malaysian neurologists with expertise in PD for content va- lidity, based on relevance, clarity and conciseness. A Mandarin version of the questionnaire was translated and back-translated by medical doctors and neurologists fluent in both languages. For each version, cognitive debriefing and readability assessment were conducted in ten patients and ten caregivers. During each step, items that were unclear were revised accordingly.
Evaluation of psychometric properties
The KPPDQ was assessed for internal consistency (Cronbach’s alpha) and test-retest reliability. A subgroup of patients and caregivers from the pilot was recruited for retest after 2–4 weeks of initial completion of the KPPDQ. Test- retest reliability was measured using unweighted kappa (for part 1) and kappa with quadratic weighting (for part 2). A
kappa statistic value of≥0.4 was set as an acceptable test- retest reliability [29]. Factor analysis was used to test for di- mensionality of the items.
Statistical analysis
IBM SPSS version 23 was used for most statistical analyses.
For weighted kappa, an online calculator was used [30].
Descriptive results were reported as frequencies and percent- ages. Between-group differences were analysed using inde- pendent samplesttests and chi-square analyses. Factors asso- ciated with knowledge were tested using multiple regression analysis. For all tests, statistical significance was set as < 0.05.
Results
DemographicsOut of the 500 participants recruited for this study, 211 pa- tients and 273 caregivers completed the KPPDQ (96.8% re- sponse rate). Demographic characteristics of the respondents are shown in Table1. The PD group was significantly older than caregivers and had a higher proportion of males. Most (≈
90%) of the respondents had received at least secondary edu- cation. Patients were represented across a broad range of dis- ease severity, from those with no self-reported functional im- pairment to those requiring complete assistance (mean disease duration 7.9 ± 6.4 years; range < 1–30 years). In general, care- givers perceived functional impairments of the patients to be worse than the patients themselves.
Psychometric properties of the KPPDQ
Overall, the KPPDQ showed good internal consistency with Cronbach’s alpha of 0.796 for part 1 and 0.562 for part 2. Test- retest reliability (tested in a subgroup of 56 patients and 56 caregivers) results are summarized in Supplementary Tables 1 and 2; the results were satisfactory. Items with borderline kap- pa statistics (i.e. part 2 item 16 for patients and part 2 items 4 and 12 for caregivers) were reviewed by a panel of neurolo- gists and retained for their relevance in assessing perception.
Factor analysis for items in part 2 showed Keiser-Meyer- Olkin (KMO) values of 0.5–0.7 and average variance extract- ed (AVE) values of 48.4–78.0%, demonstrating that each of the nine factors was clinically interpretable (Supplementary Tables 3 and 4).
Patients’and caregivers’knowledge regarding Parkinson’s disease
Results for part 1A are depicted in Fig.1. Motor symptoms of PD were better recognized by both patients and caregivers
(82.0–96.2%), compared to NMS (26.0–78.4%). Among mo- tor symptoms, slowness of movement was the most well rec- ognized, by≈95% of patients and caregivers, followed close- ly by tremor (≈93%) and walking problems (≈92–92%). The most well-recognized NMS were speech difficulty, constipa- tion and low mood/depression (all > 70%). Urinary problems and reduced sense of smell were recognized by only a minor- ity of patients/caregivers. Only a minority of patients were able to recognize visual hallucinations. Only about one-half of respondents were able to recognize pain. Overall, there were no significant differences between patients and care- givers in the total number of correctly identified motor symp- toms (4.5 ± 0.9 vs. 4.7 ± 0.8, out of five motor symptoms,P= 0.085) or NMS (6.5 ± 3.0 vs. 6.5 ± 2.8, out of 11 NMS,P= 0.813).
Results for general knowledge regarding PD are shown in Table2. The most common misconceptions among both pa- tients and caregivers (with > 50% answering incorrectly) pertained to statements 4 (all patients with PD experience tremor), 8 (PD is usually familial), 9 (PD is diagnosed using MRI) and 11 (there are new treatments that can cure PD).
Overall, patients and caregivers obtained similar scores (7.4
± 2.3 vs. 7.0 ± 2.3 correct, out of 12 statements,P= 0.067).
Regression analysis was used to test factors associated with knowledge (total score for part 1) among patients and care- givers (Supplementary Table 5). For patients, the associated factors were education (those with tertiary education were more knowledgeable) and PD duration. For caregivers, female gender, healthcare-related work experience, previous atten- dance at Parkinson’s events, and longer duration of caring for a patient with PD were associated with higher levels of knowledge.
Patients’and caregivers’perceptions towards Parkinson’s disease and its treatment
Results from the analysis of patients’and caregivers’percep- tions towards PD and its treatment are shown in Table 3.
Around two-thirds of patients and caregivers felt that PD posed a heavy financial burden. Significantly more patients perceived that they were a burden to others because of the disease, compared to caregivers (70.0% vs. 43.9%, P< 0.001). Almost one-half of patients and caregivers thought that PD was caused by the patient’s previous actions such as working in a stressful job. About one-third of patients felt ashamed of having PD and that people were uncomfortable being around them because of PD.
Almost 80% of patients and caregivers felt that they had good access to reliable information about PD, but only about one-half reported good access to community supports. Most respondents (> 90%) felt that they were receiving good care from their healthcare providers and that medications had helped significantly to control PD symptoms; however, about
one-half of them perceived that PD medications were likely to cause damage to the internal organs. About one-third of the respondents would consider taking traditional remedies (e.g.
herbal medicines, acupuncture), while≈60% would consider taking vitamin or other health supplements to treat PD symp- toms. A significant proportion (40.8–60.0%) would consider stem cell injection therapies.
Regarding treatments for advancing disease, a significantly higher proportion of patients considered having deep brain stimulation (DBS) surgery compared to caregivers (62.0%
vs. 45.9%,P= 0.022). A significant minority of participants would not consider using a walking aid (≈15–20%) or wheel- chair (≈30%) in spite of having falls. More patients would consider living in nursing homes compared to caregivers (56.8% vs. 23.3%;P< 0.001). In the event of swallowing difficulty and medical complications, only about one-half of
the patients would consider tube feeding or invasive medical treatment such as mechanical ventilation. Patients and care- givers were equally split regarding responsibility for medical decision-making. Almost three-quarters of participants expressed a preference to die at home rather than in a hospital.
Discussion
In this study, we first developed and tested the psychometric properties of a questionnaire on patient/caregiver knowledge and perceptions regarding PD. The reliability, validity, and dimensionality of the KPPDQ were in the acceptable-to- good range [31].
Given that the diagnosis of PD still rests primarily on a constellation of motor features [2], it was not surprising that Table 1 Demographic data of
participants Clinical characteristics PD patients (n= 211) Caregivers (n= 273) Pvalue
Age (years) 65.80 ± 10.390 51.97 ± 15.313 < 0.001*
Gender (%male) 58.8 40.7 < 0.001*
Race
% Chinese 73.5 71.8 0.605
% Malay 10.0 10.6
% Indian 15.2 14.3
% Others 1.4 3.3
Education level
% Tertiary 36.7 52.7 0.001*
% Secondary 51.4 42.5
% Primary 10.5 4.4
% None 1.4 0.4
Healthcare-related work (%yes) 8.5 14.3 0.071
Primary sources of healthcare information
% Internet 33.1 66.9 < 0.001*
% Television 40.8 59.2 0.707
% Newspapers/magazines 37.4 62.6 0.048*
% Doctors/health professionals 44.7 55.3 0.455
% Patient support group 48.5 51.5 0.675
Attendance at educational events (%yes) 31.8 28.2 0.455
Self-reported functional impairment
% Group 1 (normal) 5.7 2.2 < 0.001*
% Group 2 (minimally slow/clumsy) 29.4 17.6
% Group 3 (slow/clumsy but no limitations) 17.1 11.7
% Group 4 (limitation for demanding activities) 28.4 21.6
% Group 5 (limitation for basic ADLs) 12.8 26.7
% Group 6 (great limitation) 6.2 16.1
% Group 7 (complete assistance needed) 0.5 4.0
*Denotes significant between-group differences, analysed byttest and chi square test
Together with *, numbers in bold print highlight statistically significant results, making them easier for the reader to see
motor symptoms were better recognized by patients and care- givers compared to NMS. In an international survey, up to 62% of NMS in PD were undeclared to healthcare profes- sionals due to patients’lack of awareness that the symptoms were linked to PD, often leading to inadequate treatment of the symptoms [4]. Notably, several poorly recognized NMS found in the present study (pain, reduced sense of smell, uri- nary problems and visual hallucinations) were previously re- ported by patients to be among the most bothersome symp- toms in both early and advanced-stage PD [32,33], and were also a source of significant burden to caregivers [17]. Efforts to increase awareness of NMS among patients, caregivers and healthcare professionals, and use of patient/caregiver- completed questionnaires such as the NMSQuest [34], may facilitate the detection and management of these problems in routine clinical practice.
Misconceptions about PD among patients and caregivers can result in unwarranted fear, stigma and a mismatch in ex- pectations. More than half of the respondents in this study believed that PD is usually familial, which might add to the psychological burden in both caregivers and patients regard- ing the possibility of seeing themselves or their loved ones
developing the disease in the future [35]. While there is no scientific evidence to suggest that PD is caused by “un- healthy”behaviours [36–38], nearly half of the respondents believed that the disease developed because of something the patient had done in the past. This misperception regarding the root cause of PD could be a source for ongoing guilt or blame, and possibly internalized stigma; to our knowledge, there is no published literature on this issue [39]. Around 30% of patients felt ashamed of having PD (a perception endorsed by 45% of caregivers). Perceived public stigma (“I feel that people are uncomfortable around me because of my Parkinson’s”) was evident in≈40% of patients. Visible abnormalities of move- ment (tremor, dyskinesias, gait freezing, facial masking), drooling and communication and mental difficulties caused by PD likely contribute to this perceived public stigma [39, 40]. Although the functional impact of resting tremor in PD is often downplayed by clinicians [41], it is believed that the wide usage of anticholinergics in the Asian-Oceanian region—potentially problematic, due to the risk of cognitive decline [42]—may stem in part from stigma related to tremor [8,19,39]. By contrast with disorders such as epilepsy, re- search on stigma (a key determinant of health-related quality
26.0 43.6
54.9 51.3
64.1 61.5
64.5 63.0
71.4 70.3
78.4 89.4
91.2 92.7
94.1 95.6
47.1 47.4 47.9 53.6 54.0 58.8
60.7 61.6
70.1 74.4
78.2 82.0
87.2 90.5
92.9 96.2
0.0 20.0 40.0 60.0 80.0 100.0 120.0
Reduced sense of smell Urinary problems Visual hallucinations Pain Swallowing difficulty Memory problems Acting out dreams during sleep Difficulty sleeping/Insomnia Low mood/Depression Constipation Speech difficulty Rigidity (muscle stiffness) Imbalance/Tendency to fall Walking problems Tremors Slowness of movement
Percentage of Correct Responses (%)
Motor Symptoms
Patients Caregivers
Non-Motor Symptoms
*
*
* Fig. 1 Recognition of motor and
non-motor symptoms of Parkinson’s disease by patients and caregivers (part 1A).
*Denotes significant between- group differences, analysed using chi-square test
of life) in PD remains scarce [39,40,43] and further studies are required to understand the magnitude of this problem, in both the personal and public sphere.
Surprisingly, another misconception found in this study was regarding the availability of curative treatment for PD (≈50–60% of participants answering incorrectly), which was very similar to our previous result in a large public survey involving > 1000 participants [10] . This may be due, for example, to widespread advertising of“stem cell”procedures (which 60.0% of patients in this study reported they would consider using), facilitated by increased online access to health information and a lack of regulatory oversight [5,44].
One study of stem cell clinic websites found that PD was one of the top five conditions for which stem cell treatments were offered [45]; these clinics are proliferating in many parts of the world, particularly in Asia and South America [46,47]. The misconception regarding cures could also arise from a belief in complementary and alternative medicine treatments, which
are used by up to three-quarters of PD patients in the region [8, 48,49]. Although some of these treatment paradigms may offer hope, and a culturally relevant or holistic approach that many patients desire [8,48,49], these beliefs could potentially lead to inappropriate healthcare-seeking behaviours and pa- tients being exploited and squandering their financial re- sources on unproven treatments.
A corollary of a preference for“natural”treatments is a fear that synthetic chemicals (e.g. PD drugs) may have toxic ef- fects on the body. Indeed, although > 90% of study partici- pants felt that they were receiving good care from their healthcare providers (comparing favourably to a recent multi-national European survey [50]), and that PD medica- tions had helped significantly to control symptoms, ≈50%
of all participants perceived that PD medications were likely to cause internal organ (kidney, liver) damage. There is no evidence for a toxic effect of levodopa, which has been exten- sively prescribed as a“staple”medication for PD for half a Table 2 General knowledge
regarding Parkinson’s disease (part 1B)
No Statements Percentage with correct
responses (%)
P value Patients
(n= 211)
Caregivers (n= 273) 1 Parkinson’s disease and Alzheimer’s disease are different names for
the same disease (correct answer: x)
61.1 72.9 0.008*
2 Parkinson’s disease is a degenerative disease of the brain (associated
with loss of brain cells) (correct answer:✓) 83.9 76.6 0.061 3 In Parkinson’s disease, the level of a chemical (neurotransmitter) in
the brain called dopamine is reduced (correct answer:✓) 78.2 74.7 0.434 4 All patients with Parkinson’s disease experience tremor
(involuntary shaking movements) (correct answer: x)
22.3 21.2 0.872
5 Parkinson’s disease can initially affect one side of the body (correct answer:✓)
74.4 59.0 0.001*
6 Parkinson’s disease is more common in older persons (correct answer:✓)
70.6 57.1 0.003*
7 Parkinson’s disease can also affect young adults (correct answer:✓) 71.6 73.3 0.755 8 Parkinson’s disease usually affects multiple members of the same
family (correct answer: x)
47.4 40.3 0.141
9 Parkinson’s disease is diagnosed using a brain scan (MRI) (correct answer: x)
31.8 31.5 1.000
10 There are treatments that can improve the symptoms of Parkinson’s disease (correct answer:✓)
87.7 83.9 0.295
11 There are new treatments that can cure Parkinson’s disease (correct answer: x)
47.4 41.4 0.220
12 Patients with Parkinson’s disease usually become
wheelchair-dependent within 3 years of diagnosis (correct an- swer: x)
63.0 68.5 0.245
Numbers in bold print highlight statistically significant results, making them easier for the reader to see
*Denotes significant between-group differences, analysed using chi square
Table 3 Patients’and caregivers’perceptions towards Parkinson’s disease and treatment (part 2)
Responses (%) Pvalue
SA A D SD
Burden of Parkinson’s disease
I feel that having Parkinson’s poses a heavy financial burden to me and my family I feel that having Parkinson’s poses a heavy financial burden to the patient and his/her family
14.0 15.1
47.8 52.8
35.7 28.4
2.4 3.7
0.351 I feel that I am a burden to others because of my Parkinson’s
I feel that he/she is a burden to others because of his/her Parkinson’s
12.9 6.3
57.1 37.6
26.2 47.6
3.8 8.5
< 0.001*
Access to information and community supports
I feel that there is good access to reliable information about Parkinson’s I feel that there is good access to reliable information about Parkinson’s
13.9 9.6
65.6 67.6
19.1 20.6
1.4 2.2
0.475 I feel that there is good access to community supports/resources (e.g., local Parkinson’s Support Group)
I feel that there is good access to community supports/resources(e.g., local Parkinson’s Support Group)
6.4 7.8
51.0 45.9
39.2 41.5
3.4 4.8
0.657
Misperceptions regarding Parkinson’s disease causation and treatment effects
I think that my Parkinson’s was caused by something I have done in the past (e.g., worked in a stressful job) I think that his/her Parkinson’s was caused by something he/she has done in the past(e.g., worked in a stressful job)
12.4 7.0
35.4 39.7
44.5 43.4
7.7 9.9
0.168 I feel that Parkinson’s medication(s) are likely to damage my internal organs (e.g., kidneys and liver)
I feel that Parkinson’s medication(s)are likely to damage his/her internal organs(e.g., kidneys and liver)
7.6 6.2
44.1 41.0
42.3 49.6
3.5 3.1
0.960
Satisfaction with treatment and care
I feel that I am receiving good care from my Parkinson’s healthcare providers (doctors, therapists, etc.) I feel that he/she is receiving good care from his/her Parkinson’s healthcare providers(doctors, therapists, etc)
32.5 29.4
62.2 64.0
5.3 5.9
0.0 0.7
0.562 I feel that medications have helped significantly to control my Parkinson’s symptoms
I feel that medications have helped significantly to control his/her Parkinson’s symptoms
26.9 25.1
65.9 66.8
6.7 7.4
0.5 0.7
0.948
Complementary and alternative treatments
I would consider taking traditional remedies (e.g., herbal medicines, acupuncture) to treat my Parkinson’s symptoms I feel that he/she should consider taking traditional remedies(e.g., herbal medicines, acupuncture)to treat his/her
Parkinson’s symptoms
4.9 5.6
33.5 34.8
50.5 48.3
11.2 11.2
0.960
I would consider taking vitamin/mineral or other health supplements to treat my Parkinson’s symptoms
I feel that he/she should consider taking vitamin/mineral or other health supplements to treat his/her Parkinson’s symptoms 5.8 8.9
51.9 52.0
39.3 34.9
2.9 4.1
0.469 I would consider having current stem cell therapies (injections) to treat my Parkinson’s symptoms
I feel that he/she should consider having current stem cell therapies (injections) to treat his/her Parkinson’s symptoms 12.5 7.5
47.5 33.3
33.8 54.8
6.2 4.3
0.050
Stigma of Parkinson’s disease
I feel ashamed for having Parkinson’s I feel that he/she is ashamed of having Parkinson’s
3.3 7.7
27.3 37.9
56.5 47.1
12.9 7.4
0.003*
I feel that my family members are ashamed of me because I have Parkinson’s I feel that his/her family members are ashamed of him/her because he/she has Parkinson’s
1.0 2.2
16.3 6.2
61.5 61.5
21.2 30.0
0.001*
I feel that people are uncomfortable around me because of my Parkinson’s I feel that people are uncomfortable around him/her because of his/her Parkinson’s
5.3 2.6
35.4 18.4
47.8 61.0
11.5 18.0
< 0.001*
Assistance for disability
I would consider using a walking aid (walking stick or walking frame), if I am having falls I feel that he/she should use a walking aid (walking stick or walking frame), if he/she is having falls
18.5 21.2
64.0 65.2
13.7 10.6
3.8 2.9
0.634 I would consider using a wheelchair, if I am having falls
I feel that he/she should use a wheelchair, if he/she is having falls
12.4 17.3
56.9 52.4
25.8 26.2
4.8 4.1
0.483 I would not mind living in a nursing home, if I am unable to carry out activities independently
I would consider sending him/her to live in a nursing home, if he/she is unable to carry out activities independently
7.8 3.0
49.0 20.3
31.1 52.8
12.1 24.0
< 0.001*
Treatments for advancing disease
I would consider having deep brain stimulation (DBS) surgery to treat my Parkinson’s symptoms I feel that he/she should consider deep brain stimulation (DBS) surgery to treat his/her Parkinson’s symptoms
18.6 15.8
43.4 30.1
29.2 47.9
8.8 6.2
0.022*
I would consider having a feeding tube, if I become unable to swallow properly
I feel that he/she should consider having a feeding tube, if he/she becomes unable to swallow properly
4.4 5.2
51.5 55.2
38.3 32.1
5.8 7.5
0.521 If I have a medical complication due to advanced Parkinson’s (e.g., a severe chest infection due to impaired
swallowing), I would want to undergo invasive medical treatment, including ventilation (being connected to a breathing machine in the intensive care unit/ICU)
If he/she has a medical complication due to advanced Parkinson’s (e.g., a severe chest infection due to impaired swallowing), I would want him/her to undergo invasive medical treatment including ventilation (being connected to a breathing machine in the intensive care unit/ICU)
4.3 10.2
49.3 53.0
35.7 28.4
10.6 8.3
0.042*
century [51–53]. Ergot dopamine agonists which can poten- tially cause fibrotic complications [53] have been phased out worldwide many years ago and are almost never used in Malaysia. This misconception regarding organ damage prob- ably contributes to patient/caregiver reluctance to take PD medication and the generally lower dosages used in many Asian-Oceanian patients [8, 22]. Importantly, inadequate treatment of parkinsonian features could result in premature loss of function and employment [5,54], and currently there are relatively few legal safeguards protecting the rights of employees facing medical disability in many Asian- Oceanian countries. Another factor that likely contributes to under-utilization of treatments is the financial cost, as many study participants mentioned that PD posed a heavy financial burden to them. The financial burden of PD, already high in developed countries [55,56], is even more acute in develop- ing countries where medical insurance coverage is scarce [8].
In Malaysia and elsewhere in the region, basic treatments such as levodopa can be obtained free-of-charge in public hospitals, but advanced therapies such as DBS are usually paid for out- of-pocket [8], which may partly explain why 38.0% of pa- tients and 54.1% of caregivers would not consider this established, evidence-based treatment. It should be noted that although motor symptoms usually improve substantially after DBS [53,57], caregiver burden may not change and some- times may even worsen, due to role changes associated with the sudden relief of physical disability, and possible worsen- ing or new development of neuropsychiatric issues such as cognitive impairment, impulsivity or apathy [16,57].
Our study provides some insights into patient and caregiver preferences in advancing disease phases. Interestingly, a sig- nificant minority (≈15–30%) would not consider using a walking aid or wheelchair despite having falls. There are a number of possible reasons for this, including a desire to re- main independent for as long as possible, but the stigma of being seen using assistive devices may also be a factor and is important to address when counselling patients about falls risk
[58–60]. Many patients worry about becoming a burden to their family [61], and a majority of patients indicated that they would not mind residing in a nursing home if no longer able to independently carry out daily living activities. Interestingly, only 23.3% of caregivers would consider this option, indicat- ing a desire to maintain patients in their home environment, which is in line with traditional Asian values of providing care for older family members at home [62]. However, this concept has been challenged by significant changes in population de- mographics (fewer children, outmigration of young adults, etc.), and the heavy burden to caregivers, who are often elder- ly spouses, due to the multifaceted nature of PD involving both physical and mental impairments [5, 17, 18, 26].
Previous studies have highlighted disease features that are particularly burdensome to caregivers (neuropsychiatric symptoms such as psychosis, anxiety and impulsive- compulsive behaviours; sleep disorders and falls) that may be amenable, at least in part, to treatment, and a need to pri- oritize adequate respite care and interventions that offer education/coaching and peer support by other caregivers [5, 16,26]. Researchers previously found poor nursing home staff knowledge regarding PD, resulting in a lack of empathy and undertreatment of motor and non-motor symptoms; recom- mendations to improve this situation have been made [18].
Regarding tube feeding and ICU treatment, overall respon- dents were roughly equally divided as to whether they would consider or desired these treatments, reflecting considerable variability in preferences that would need to be accounted for in caring for patients and families. One study from the USA reported much lower rates of patients opting for ventilation or tube feeding (16% and 20%, respectively) [63], but otherwise there is little previous published information on these aspects of care in PD. Indeed, there remains significant uncertainty among physicians treating PD regarding the appropriateness and timing of tube feeding [64,65]. Finally, the vast majority (≈70–75%) of participants wanted their home to be the place of death. This is consistent with studies from the West Table 3 (continued)
Responses (%) Pvalue
SA A D SD
Autonomy
I prefer to be responsible for actively deciding on my treatment (rather than the doctor, whose role should be to provide accurate medical information)
We prefer to be responsible for actively deciding on his/her treatment (rather than the doctor, whose role should be to provide accurate medical information)
8.7 10.7
44.0 45.2
43.0 38.5
4.3 5.6
0.692
When I pass away, I would prefer to be at home, instead of being in a hospital
When he/she passes away, I would prefer for him/her to be at home, instead of being in a hospital.
18.3 22.1
57.9 49.6
21.3 24.8
2.5 3.5
0.371
Numbers in bold print highlight statistically significant results, making them easier for the reader to see
SA: Strongly Agree; A: Agree; D: Disagree; SD: Strongly Disagree; statements and numbers in bold print were the version given and responses received from patients (n = 211), and those in italics were for caregivers (n= 273), respectively
*Denotes significant between-group differences (P< 0.05), analysed by chi square test
reporting that most people, including PD patients, prefer to die in familiar surroundings, rather than in hospital which may not be the optimal place for terminal care [66,67]. Despite this, many patients still end up dying in hospitals, which could be due to a current lack of community or hospice services for patients with neurodegenerative diseases and also a lack of advance care planning [66–68]. Having earlier conversations with patients and families about what might happen in the future with disease progression may help to mitigate uncer- tainty and crisis, although the unpredictability of PD progno- sis makes this a challenging task [68]. Previous research sug- gested that few PD patients considered the possibility of de- veloping cognitive impairment in the future and most did not make any provisions for this outcome [69].
Thus, an important role for clinicians, armed with knowl- edge of some of the issues highlighted above, is to direct patients/families away from false or misleading medical infor- mation, and towards accurate and reliable sources, and to do so in a timely manner [5,19,44]. For example, it often takes months or even years for patients/families to get used to the idea of utilizing device-aided therapies [70], and lack of infor- mation from doctors and late referrals [8,71,72] could result in low uptake of such therapies which can substantially im- prove motor complications and health-related quality of life at a point in the disease course when further adjustments of con- ventional medications yield little benefit. In this study, doctors and other healthcare professionals were reported to be one of the primary sources of healthcare information, which was ex- pected and in line with previous research [73]. Interestingly, only slightly over half of the participants expressed a prefer- ence to be actively responsible for medical decision-making, indicating a relatively high reliance on doctors’recommenda- tions, in contrast to the findings in a recent Dutch study of advanced PD patients, where the vast majority (93%) indicat- ed a preference to be actively involved in the decision-making process [74]. The desire (and ability) to actively participate in medical decision-making varies with educational level, cogni- tive capacity, cultural background, age, quality of the patient- doctor relationship and decision type [50,73,74]. Therefore, clinicians should not force an active role for all patients and caregivers, which could cause unnecessary distress [74].
Many participants in this study, especially caregivers, used the Internet as a primary source of healthcare information, consistent with the findings of other studies [44,73]. This is both a challenge and an opportunity for professional bodies and support organizations such as the International Parkinson and Movement Disorder Society (MDS), the World Parkinson Coalition, and local-regional groups to provide information that is accessible, readable, accurate and up-to-date on their websites [44,73]. The MDS is continuing to develop patient information e-leaflets that are currently available in over 30 languages, including topics that may sometimes be difficult for clinicians to broach face-to-face e.g. end-of-life issues.
Support groups play a very important role for many people living with PD, and in one study caregivers cited these as their most useful resource [55,75]. However, only slightly more than half of the participants in our study reported good access to community supports, indicating an area for further im- provement. In Malaysia, there are only two active PD com- munity support groups, for a population of > 30 million.
The main limitation of this study was that sampling was done in a single university hospital clinic; thus, the findings may not be generalizable, although this could be mitigated by recruitment of a relatively large number of participants across a broad range of disease severity. To our knowledge, this is the largest survey ever conducted on PD patient/caregiver knowl- edge and perspectives in Asia. We did not formally test cog- nition in patients, and acknowledge that cognitive decline can be a challenge to effectively capture patient preferences [14].
Because of the sensitive nature of some of the items in the KPPDQ, the questionnaires were completed anonymously to protect participant privacy, and we were thus unable to corre- late disease features of patients with their questionnaire re- sponses. Finally, we acknowledge that statistical correction for multiple comparisons was not implemented in our study, as we believed that the approach of applying a standard alpha threshold for significance (< 0.05) was justified to decrease the risk of type II (false negative) errors, so that potentially relevant associations/differences could be identified and ex- plored further, rather than being discarded [76].
Conclusions
In conclusion, important knowledge gaps, misconceptions and perspectives regarding PD were identified, and these find- ings can help in fulfilling patients’, caregivers’and clinicians’
goals and expectations. We believe the study contributes sub- stantially to the very limited literature on this topic, in a region poised to account for the majority of PD patients worldwide, and is a step towards much-needed larger efforts to understand patients’and caregivers’perspectives and educational needs in this complex and heterogeneous disease. In the future, the KPPDQ could also be administered and validated in larger cohorts representing different cultural and socio-economic backgrounds to unravel new and important insights, with the aim of improving care in PD communities across different countries.
Acknowledgements We would like to thank Drs. Kwang Hwee Goh, Thien Thien Lim, Kenny Tan, Phaik Yee Ooi and Chiun Hian Chai for their helpful appraisal and suggestions to improve the KPPDQ.
Funding information This work was supported by the University of Malaya Parkinson’s Disease and Movement Disorder Research Program (PV035-2017), and a donation from the family and friends of the late Mr. Rodney Cooke. These funding sources had no role in the
study design; in the collection, analysis and interpretation of data; in the writing of the report and in the decision to submit the article for publication.
Compliance with ethical standards
Conflict of interest SYL reports lecturing honoraria from Lundbeck, Medtronic, Novartis, and UCB; and consultation fees from Lundbeck.
AHT reportslecturing honoraria from Novartis and Boehringer Ingelheim. The other authors have no conflicts of interest.
Ethical approval The study was approved by the Medical Research Ethics Committee, University of Malaya Medical Centre (ID number 2018723-6507) and conducted ethically in accordance with the World Medical Association Declaration of Helsinki. Written informed consent was obtained from all subjects.
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