Journal of Genetic Counseling https://doi.org/10.1007/s10897-018-0239-3
ORIGINAL RESEARCH
Parkinson’s Disease: Patients’ Knowledge, Attitudes, and Interest in Genetic Counseling Kristin A. Maloney 1,2 & Dina S. Alaeddin 3 & Rainer von Coelln 4 & Shannan Dixon 5 & Lisa M. Shulman 4 & Katrina Schrader 4 & Yue Guan 1,2 Received: 30 October 2017 / Accepted: 8 February 2018 # National Society of Genetic Counselors, Inc. 2018
Abstract The objective of this study was to assess the genetics knowledge of patients with Parkinson’s disease (PD), and to explore their attitudes on genetic testing and interest in genetic counseling. We surveyed 158 patients from the University of Maryland Parkinson’s Disease and Movement Disorders Center. Patients averaged a score of 63% on general genetics knowledge and 73% on PD genetics knowledge. Participants had an overall positive attitude toward genetic testing: 80% believed that the use of genetic tests among people should be promoted, and 83% would undertake genetic test for PD if it was available. Patients reported a high interest to discuss the benefits, risks, and impacts of genetic testing for PD (mean sum score = 26, range = 9–35), and 43% patients expressed interest in meeting with a genetic counselor. Multivariate regression analysis showed that patients who had more positive attitudes toward genetic testing for PD were more interested in meeting with a genetic counselor (β = 0.6, p < 0.001). This study is the first to demonstrate an interest in genetic counseling among patients with PD. Our findings demonstrate a new niche for genetic counselors to support patients in clarifying gaps or misconceptions in knowledge about PD genetics as well as the possible risks, benefits, and limitations of genetic testing. Keywords Parkinson’s disease . Genetic counseling . Genetic testing . Attitudes . Knowledge
Introduction Parkinson’s disease (PD) is the second most common neurodegenerative disorder in the elderly, with an estimated prevalence of 1% among individuals over age 60 and about 4% among people over age 85 (de Lau and Breteler 2006). As a movement disorder, PD is clinically characterized by the cardinal features of rest tremor, bradykinesia, rigidity, and loss of
* Yue Guan
[email protected] 1
Department of Medicine, University of Maryland School of Medicine, Baltimore, MD, USA
2
Program for Personalized & Genomic Medicine, Department of Medicine, University of Maryland School of Medicine, 685 W. Baltimore St., MSTF 357E, Baltimore, MD 21201, USA
3
Inova Translational Medicine Institute, Falls Church, VA, USA
4
Department of Neurology, University of Maryland School of Medicine, Baltimore, MD, USA
5
Department of Pediatrics, University of Maryland School of Medicine, Baltimore, MD, USA
postural reflexes (Lees et al. 2009). In addition, patients with PD experience other motor symptoms such as hypophonia, hypomimia, and dysphagia, as well as non-motor features including neuropsychiatric problems (depression, anxiety, hallucinations), dysautonomia (sialorrhea, orthostatic hypotension), and sleep disturbances (Jankovic 2008). Loss of dopaminergic neurons of the substantia nigra and aggregation of misfolded alpha-synuclein in Lewy bodies are well-established hallmarks of PD pathology; however, the underlying cause remains unknown. Both genetic and environmental factors have been implicated in the pathogenesis of PD, and it appears to be a multifactorial disease in the majority of patients (Kalia and Lang 2015). Having a positive family history for PD is one of the strongest risk factors for the disease, and 10–16% of individuals with PD report at least one relative affected by PD, highlighting the importance of genetic factors (Calsbeek et al. 2007; Noyce et al. 2012; Rybicki et al. 1999). The past two decades have seen substantial advances in our understanding of PD genetics (Gasser 2009). Several monogenetic forms of PD have been identified that follow classic Mendelian patterns of inheritance, including dominant (mutations in the SNCA, LRRK2, and VPS35 genes) and
Maloney et al.
recessive (parkin, PINK1, and DJ-1) forms (Lesage and Brice 2012). However, only 10% of familial cases of PD and less than 5% of the sporadic cases are caused by mutations in one of these genes (Al-Mubarak et al. 2015; Tan and Jankovic 2006). Heterozygous carriers of mutations in the glucocerebrosidase gene (GBA), that cause Gaucher disease in the homozygous state, have a five-fold increased risk for PD, making it the strongest genetic risk factor identified to date (Sidransky et al. 2009). Furthermore, more than 20 genetic risk alleles for Bidiopathic^ PD have been identified in genome-wide association studies (Kalinderi et al. 2016; Nalls et al. 2014). The European Federation of Neurological Societies (EFNS) and the Movement Disorders Society–European Section (MDS-ES) have developed guidelines for genetic testing in PD in a clinical setting (Berardelli et al. 2013). These guidelines recommend that genetic testing in PD should be limited to the following scenarios: (1) Testing for mutations in SNCA and LRRK2 in patients with typical PD and a clear dominant family history; (2) Testing for mutations in the parkin, PINK1, and DJ-1 genes in patients with typical PD and either a family history compatible with recessive inheritance AND an age of onset below 50, or sporadic patients with typical PD AND an age of onset below 40; (3) Testing for variants with reduced penetrance and those considered to impose significant risk, such as the LRRK2 p.G2019S-mutation and GBA-variants, respectively, should be limited to patients from the appropriate founder populations; and (4) Testing for the many very rare genes causing atypical forms of Parkinsonism can be offered on a case-by-case basis or in a research setting. Only a small percentage of patients with PD are likely to fit into one of the above categories, yet prior studies have demonstrated a high interest in genetic testing among individuals who are affected. Fifty-nine percent of participants in a study by Falcone and colleagues stated they were interested in genetic testing for PD (Falcone et al. 2011), close to 75% of individuals with PD of Ashkenazi Jewish descent either definitely (32.6%) or probably (41.1%) wanted genetic testing in a 2015 study (Gupte et al. 2015), and 90% of participants in a 2014 study of Australian patients with PD stated they would undergo genetic testing for PD (Scuffham et al. 2014). Given the increasing availability of clinical genetic testing for PD, patients are more likely to be offered genetic testing by their health care providers. Genetic counselors are in a prime position to help patients with PD and their families understand the possible benefits and limitations of genetic testing for PD and facilitating the genetic testing process. It is important for genetic counselors to understand patients’ level of knowledge of genetics and their attitudes toward genetic testing, as these factors have been shown to influence patients’ uptake of new genomic technology and how individuals respond to genetic test results (Bosompra et al. 2000; Bunn et al. 2002;
Hann et al. 2017). In the context of PD, previous surveys revealed a low level of genetic knowledge among patients with PD, despite their positive attitudes toward PD genetic testing (Falcone et al. 2011; Sakanaka et al. 2014; Scuffham et al. 2014). Further qualitative studies among patients with PD and their relatives showed the most common motivators to undergo genetic testing are for medical decision-making and to understand implications for a family member (Gupte et al. 2015; Sakanaka et al. 2014). These findings show the importance of genetic counseling to review benefits and risks of genetic testing, while dispelling misperceptions. However, there have been few studies that investigate patients’ interest in genetic counseling for PD and whether individual patient characteristics influence patient interest. To address these gaps in the literature, this cross-sectional survey study aimed to describe patients’ knowledge and attitudes in genetics, genetic testing, and genetic counseling for PD, as well as to examine factors associated with patient interest in genetic counseling for PD.
Materials and Methods Participants and Data Collection Participants in the University of Maryland Parkinson’s Disease and Movement Disorders Center (UMPDMC) Longitudinal Quality of Life and Function (QoLF) Study with a clinical diagnosis of PD were recruited during office visits or by mail (to patients in the Center’s research database who previously consented to be contacted for future studies). Patients with a score of < 20 on the Montreal Cognitive Assessment (MOCA) test were excluded. Interested participants received a letter explaining the purpose of the study and a paper copy of the survey to complete and return during their office visit or by mail. Nearly 500 patients were contacted either by mail (450) or in person (46) between September and December 2016. All study activities were approved by the University of Maryland, Baltimore Institutional Review Board.
Measures The survey contained questions about knowledge of general genetics and PD genetics, attitudes toward genetic testing in general and for PD, and interest in genetic counseling. General genetics knowledge was assessed by a validated survey developed by Jallinoja and Aro (Jallinoja and Aro 1999) that included 11 questions with the options of Btrue,^ Bfalse,^ and BI do not know^. The question BIt has been estimated that a person has about 70,000 genes^ was changed to reflect current knowledge of the total number of genes (22,000). In addition, although one may argue that the
Parkinson’s Disease: Patients’ Knowledge, Attitudes, and Interest in Genetic Counseling
statement in the survey item BThe genotype is not susceptible to human intervention^ may no longer be 100% true, we coded the correct answer as Btrue,^ in order to be consistent with the coding in the validated survey (Jallinoja and Aro 1999). Knowledge of PD genetics was assessed by a set of five items with the options of Btrue,^ Bfalse,^ and BI do not know.^ These questions were adapted from previous studies on PD knowledge (Falcone et al. 2011; Gupte et al. 2015; Haga et al. 2013; Tan et al. 2007). Patients’ attitudes toward genetic testing in general and genetic testing for PD were assessed using a five-point Likert scale of five and eight statements, respectively, that were utilized in previous studies that analyzed views on genetic testing (Haga et al. 2013; Henneman et al. 2013; Scuffham et al. 2014). In addition, the impacts of PD genetic testing on participants’ future plans were assessed by a single multiple choice survey item BIn what ways do you think a genetic test could influence how a person with PD plans for the future?^ with possible responses of financial planning, decisions on health insurance, career planning, decisions on life insurance, family planning, it will not affect planning for the future, and other. Participants’ interest in genetic counseling was assessed using a Likert scale of Bstrongly disagree = 1^ to Bstrongly agree = 5^ of seven items that described common roles of genetic counselors (Uhlmann et al. 2011), including Bto discuss benefits and risks of genetic testing,^ Bto discuss the impact of genetic testing on my family,^ and Bto help me adapt to a diagnosis of PD.^ A sum score was generated, such that the maximum possible score was 35, indicating the greatest interest in meeting with a genetic counselor. Demographic questions included race, ethnicity, highest level of education, age at PD diagnosis, number of children, plans for more children, and family history of PD. For the purposes of this study, a family history of PD was defined as the self-reported number of relatives diagnosed with PD. Existing data from the research database utilized in the current study included gender and severity of PD, measured by Hoehn and Yahr (HY) stages I–V, with higher stages indicating more severe clinical symptoms (Hoehn and Yahr 1967).
Data Analyses We summarized patient demographics, genetic knowledge, attitudes toward genetic testing, and interests in genetic counseling, using descriptive statistics. To examine factors associated with patients’ interest in genetic counseling for PD, multivariate linear regression was performed. The regression model was adjusted for age, gender, race (Caucasian vs. non-Caucasian), family history of PD, HY stage, PD knowledge, and attitudes toward genetic testing for PD. In all analyses, two-tailed tests and p values < 0.05 were used to draw conclusions regarding statistical significance. Data were analyzed using SPSS V.24
(IBM Corp. Released 2016. IBM SPSS Statistics for Macintosh, Version 24.0. Armonk, NY: IBM Corp.).
Results Sample Characteristics We received a total of 158 responses (response rate 32%), the majority of which (71%, N = 112) were by mail. The demographics and clinical characteristics of the 158 participants are summarized in Table 1. The majority of the participants were Caucasian (86%), male (67%), and had either graduated from college or had a post-graduate degree (77%). The mean age of participants was 68 years (SD = 9), with an average age at diagnosis of 58 years (SD = 12). About one-third of participants (N = 47, 32%) reported having one or more family members with PD; 21% (N = 15) had a first-degree relative affected, 25% (N = 18) had a second-degree relative affected, and 54% (N = 39) had a third-degree relative or further affected. The majority of participants fell in the Hoehn and Yahr stages II (N = 79, 58%) and III (N = 41, 30%), meaning they were mildly to moderately affected.
General Genetics and PD Genetics Knowledge Participants averaged a score of 63% on general genetic knowledge questions (7 out of 11 questions, SD = 1.9) and 73% on PD genetics knowledge (4 out of 5 questions, SD = 1.5) (Figs. 1 and 2). Most participants understood that if an individual has PD, not all other family members will develop PD (N = 147, 93%), and that having a mutation in a gene for PD does not mean that an individual will definitely develop PD (N = 110, 70%).
Attitudes Toward General Genetic Testing and Genetic Testing for PD Overall, participants had a positive attitude toward general genetic testing (Fig. 3). Most participants (N = 126, 80%) believed that the use of genetic tests among people should be promoted, and 97 participants (62%) would want genetic testing for a disease, even if there was no treatment. Similarly, participants had an overall positive attitude toward genetic testing for PD (mean = 30.8 out of 40, SD = 3.8) (Fig. 4). The majority of participants believed that genetic testing for PD should be offered to all patients with symptoms (91%) and 83% stated they would undergo testing themselves if available. Even for asymptomatic family members, more than half participants (54%) agreed that they should have the option of genetic testing. Most participants believed that, if they were found to be carriers
Maloney et al. Table 1 Patient demographics and clinical characteristics
Patient characteristics
All (N = 158)
Age (years), mean (SD, range)
68 (9, 38–90) Gender (N = 147)
Male Female
97 (67%) 48 (33%) Race (N = 160)
Caucasian
136 (86%)
Non-Caucasian
22 (14%) Education level (N = 148)
High school/GED Some college
16 (11%) 17 (12%)
College graduate
50 (34%)
Post-graduate Age at diagnosis (years), mean (SD, range)
63 (43%) 58 (12, 20–85)
Hoehn and Yhar stage (N = 136) I
8 (7%)
II III IV Family history of PD (≥ 1 affected family member) (n = 149)
of a PD mutation, this information could guide their therapeutic plan (91%) and they would share the information with their relatives (89%). Participants’ attitudes toward reproductive planning showed that about 43% participants would still want to have kids if they knew they carried a PD mutation, and 56% would want to know the carrier status of the fetus.
Fig. 1 General genetic knowledge
79 (58%) 41 (30%) 6 (5%) 47 (32%)
When participants were asked how they thought a genetic test would influence their future, the majority responded that it would affect their decisions on health insurance (84%, N = 135) and financial planning (83%, N = 132). Additionally, some participants stated that it would affect their career planning (61%, N = 96), family planning (67%, N = 107), and their decisions on life insurance (70%, N = 110). Eleven (7%) did
Wrong Correct
It has been estimated that a person has about 22,000 genes (T) The genotype is not susceptible to human intervention (T) Genes are bigger than chromosomes (F) Different body parts include different genes (F) A gene is part of a chromosome (T) A gene is a cell (F) A gene is a piece of DNA (T) Genes are inside cells (T) A gene is a molecule that controls hereditary characteristics (T) A gene is a disease (F) One can see a gene with a naked eye (F)
0
20
40
60
Percent
80
100
Parkinson’s Disease: Patients’ Knowledge, Attitudes, and Interest in Genetic Counseling Fig. 2 General PD knowledge
Wrong Correct Environmental factors can increase the risk of PD (T)
If a genetic test for PD is negative, that individual will not get PD (F)
Even if you have a mutation (change) in a gene for PD, you may not develop PD (T)
Scientists have identified genes associated with higher risk of developing PD (T)
If an individual has PD, all other family members will develop PD someday (F)
0
20
40
60
80
100
Percent
not believe genetic testing would affect planning for the future.
PD Genetic Testing and Counseling Experiences When asked if they had previously undergone genetic testing for PD, 17 out of 157 (11%) participants responded in the affirmative; three patients reported to have tested positive, two were negative, three received a variant of unknown significance (VUS), and nine did not know the test result.
Regardless of genetic test results, patients who had testing demonstrated significantly greater knowledge of PD (mean = 4.4) compared to those who did not do genetic testing (mean = 3.5, p = 0.03). The majority of people who answered the question about whether they had ever been offered genetic testing from their doctor either said that they had not (127/152, 83%) or did not remember (23/152, 15%). Of the two respondents who had been offered testing from their doctor, one did not remember the result and the other declined
Fig. 3 Attitude toward genetic testing
Strongly Disagree Disagree Neutral Agree Strongly Agree
I would do a genetic test that informs me how rapidly a disease will progress
I do not want a genetic test to tell me I'm at risk for a disease
I would want genetic testing for a disease, even if there is no treatment
Genetic tests should be available to those who want to use them
The use of genetic tests among people should be promoted
0
20
40
60
Percent
80
100
Maloney et al. Fig. 4 Attitude toward genetic testing for PD
Strongly Disagree Disagree Neutral Agree Strongly Agree
It would be too upsetting to learn I have a gene for PD, so I am happier not knowing Knowing that I carry a PD mutation (change) will make me more likely to find out about treatments for PD I would tell my family, if I had a positive genetic test for PD I would still want to have kids,if I was certain that I carried a PD mutation (change) If blood tests are available, I would want to get genetic testing for PD If blood tests are available to show whether a person inherited a PD gene, this test should be offered to people with symptoms If my partner and I are pregnant, I would want to know if my unborn child received a PD mutation (change) from me A family member that does not have any symptoms of PD should not get genetic testing
0
20
40
60
80
100
Percent
testing because Bthere might be a chance of other people finding out my test results.^
Participants’ Interest in Genetic Counseling Out of 156 participants, 60% (N = 94) had heard of genetic counseling prior to this survey; however, only 10% (N = 16) recalled actually meeting with a genetic counselor. One individual specified that the purpose of the meeting was to determine if his/her PD was hereditary. Other reasons for prior
meetings with a genetic counselor included breast cancer genetic testing, pregnancy-related indications (e.g., advanced maternal age, carrier status) and evaluation of children with known/suspected genetic disorders. When asked whether or not they would be interested in meeting with a genetic counselor (N = 150), 43% of participants responded yes, 33% responded no, and 24% were unsure. Overall, participants showed a high interest in the roles played by a genetic counselor during a counseling session. As shown in Fig. 5, the majority of participants agreed or strongly
Fig. 5 Interest in genetic counseling for PD
Strongly Disagree Disagree Neutral Agree Strongly Agree
To help me adapt to a diagnosis of PD
To discuss resources and research
To discuss the impact of genetic testing on my family To discuss impact of genetic testing on treatment and prevention To discuss benefits and risks of genetic testing
To discuss genetic testing for PD
To discuss genetic testing in general
0
20
40
60
Percent
80
100
Parkinson’s Disease: Patients’ Knowledge, Attitudes, and Interest in Genetic Counseling
agreed that they were interested in meeting with a genetic counselor to discuss genetic testing in general (55%), genetic testing for PD (67%), benefits and risks of genetic testing (66%), the impact of genetic testing on treatment and prevention (74%), family implications (68%), resources and research (66%), and adaptation to a diagnosis of PD (55%). The mean summary score was 25.7 out of 35 (range = 9–35, SD = 5.4).
Factors Associated with Interest in Genetic Counseling Table 2 illustrates the regression coefficients from the linear regression models (both adjusted and unadjusted for covariates) to identify factors associated with interest in meeting with a genetic counselor. In all unadjusted models, patients’ attitudes toward PD genetic testing were positively correlated with patients’ interest in genetic counseling for PD (β = 0.6, p < 0.001), while patients’ age (β = − 0.1, p = 0.01) and PD severity (HY stage) is negatively associated with an interest in genetic counseling (β = − 1.7, p = 0.04). To adjust for potential confounders, a multivariate linear regression model was created to include patient age, gender, race, family history of PD, PD knowledge, and attitudes toward PD genetic testing. The final adjusted model confirmed the finding from the unadjusted model that patients who had more positive attitudes toward genetic testing for PD were more interested in meeting with a genetic counselor (β = 0.6, p < 0.001).
Discussion Research into the genetics of neurodegenerative diseases has identified genes that contribute to the development of PD, and the interest in PD genetic testing is increasing. As the availability of genetic tests for PD increases and the cost decreases, it is important to institute programs to guide and educate patients and facilitate informed decision-making. This study investigated genetic testing attitudes, general genetics knowledge, and PD-specific genetic knowledge in people with PD. This is the first study of knowledge and attitudes about genetic counseling in a sample of patients with PD. Table 2 Multivariate linear regression model: factors associated with interest in meeting with a genetic counselor
Overall, participants showed moderate levels of general genetics knowledge. When compared to other studies that used the same validated survey, our study population averaged a higher score than both the original study (Jallinoja and Aro 1999) and an older study (Calsbeek et al. 2007). Our population had less knowledge than the population studied by Haga and colleagues, which answered an average of 84% of questions correctly (range 50–100%) (Haga et al. 2013). Other studies have reported similar or lower scores on genetic knowledge questions: Sakanaka et al. 2014 reported a 65% average of correct answers in patients with PD (Sakanaka et al. 2014) and Scuffham et al. 2014 reported an average of 43% on overall knowledge (Scuffham et al. 2014). Knowledge levels may be reflective of the socioeconomic and academic status of the population at hand, as these were reported to be high in the Haga et al. study, while the Scuffman study sampled a cross-section from a major metropolitan city in Australia. Participants generally had a positive attitude toward general genetic testing, and the majority (91%) expressed interest in genetic testing for PD, consistent with results in previous studies (Falcone et al. 2011; Gupte et al. 2015; Sakanaka et al. 2014). Participants recognized the potential for genetic test results to influence decisions related to health insurance and financial planning. The majority of participants described the potential identification of at-risk family members as an advantage of genetic testing; however, they expressed less interest in prenatal genetic testing, with only 56% (N = 88) expressing interest in knowing if their unborn child inherited a PD mutation. Nevertheless, very few patients are likely to meet the clinical criteria for genetic testing proposed by the European Federation of Neurological Societies (EFNS) and the Movement Disorders Society –European Section (MDS-ES). Two-thirds of participants were interested in meeting with a genetic counselor to discuss the risks and benefits of genetic testing for PD. A majority of participants wanted to discuss the impact of testing on treatment and prevention and the impact of genetic testing on other family members. Still, only
Patient characteristics
Unadjusted coefficient (SE)
p value
Adjusted coefficient (SE)*
p value
Age Race Gender Family history of PD Hoehn and Yahr stage PD knowledge PD genetic testing attitude
− 0.13 (0.05) − 0.85 (1.49) − 0.52 (1.02) 1.36 (1.02) − 1.70 (0.81) 0.02 (0.32) 0.58 (0.11)
0.01 0.57 0.61 0.18 0.04 0.95 < 0.001
− 0.05 (0.05) 0.14 (1.93) − 0.81 (1.04) 1.82 (1.04) − 1.55 (0.82) 0.04 (0.34) 0.61 (0.12)
0.36 0.94 0.44 0.08 0.06 0.91 < 0.001
*The multivariate regression model was adjusted for age, gender, race, family history of PD, Hoehn and Yahr Stage, PD knowledge, and attitudes toward genetic testing for PD
Maloney et al.
43% percent expressed interest in meeting with a genetic counselor, which was a smaller proportion than the 56% previously reported (Falcone et al. 2011). One possible explanation for this difference is that Falcone and colleagues provided a definition of genetic counseling prior to asking participants about their interest (Falcone et al. 2011). In contrast, our study asked participants to describe their level of interest in topics frequently discussed during genetic counseling sessions; however, we did not provide a definition of genetic counseling. Another possible explanation is that participants would rather talk to the physician treating their PD symptoms about genetic testing, instead of having a separate appointment with a genetic counselor. Our study did not assess whether topics discussed during a genetic counseling session are also addressed by their current provider, but it is notable that for only two of the 17 people who reported having previously undergone genetic testing for PD had testing offered by their physician; it is possible that the other individuals either had testing performed through a direct-to-consumer genetic testing company or through a research protocol. Approximately two-thirds of participants understood that the statement BIf a genetic test for PD is negative, that individual will not get PD^ is incorrect. This result suggests that our population may benefit from pre-test genetic counseling to help patients understand the potential for true negative vs. uninformative negative results. The percentage of individuals with a college degree is higher in our study population (77%) compared to the general population (33%) (US Census Bureau 2016), so it is possible that pre-test counseling may be beneficial to the general PD community as well. The importance of pre-test genetic counseling was highlighted in a recent study on patients with PD of Ashkenazi Jewish ancestry, in which one of the most important reasons participants gave in support of genetic testing was Bidentifying no mutation^ (Gupte et al. 2015). In this population, the p.G2019S mutation in LRRK2 has been identified in 26% of familial cases vs. 10.6% of sporadic cases (Orr-Urtreger et al. 2007). Therefore, the likelihood of a participant receiving an uninformative negative result is still quite high. This misconception among participants in that study solidifies the importance of genetic counseling in patients that are interested in genetic testing to explore the depth of their knowledge and their understanding of the limitations, risks, and benefits of genetic testing. The utility of genetic counseling for patients and families with PD can likely be extended beyond issues surrounding genetic testing, as has been demonstrated for other multifactorial, complex diseases such as schizophrenia, bipolar disorder, and diabetes. For psychiatric conditions, in which genetic testing cannot establish or exclude a diagnosis, genetic counseling has been shown to decrease anxiety, guilt, and stigma while increasing knowledge, empowerment, and self-efficacy in both patients and their families (Costain et al. 2014a, b; Hippman et al. 2016; Moldovan et al. 2017). Genetic counseling was also
shown to increase perceptions of disease controllability in patients with type 2 diabetes (Nishigaki et al. 2014). Indeed, 68 and 66% of participants expressed interest in meeting with a genetic counselor to discuss family implications and resources and research, respectively, and about half said they would like help adapting to the diagnosis of PD. The present study is not without limitations, including a small size sample that may not be representative of the PD community as a whole. The participants that returned the survey were mainly older well-educated Caucasians, and therefore the views may be specific to that population only. The age at diagnosis of PD in our population is 58 years. Previous large studies have described an age of onset between 55 and 68 years for the general population, consistent with our result (Searles Nielsen et al. 2013). However, only four participants were less than 50 years old, so we were limited in exploring the views of younger patients with PD. The EFNS criteria are quite restrictive, and may need to be reconciled with the strong interest patients affected by PD expressed in our study. Some participants were recruited from a research database, so our population may be enriched for people that are more likely to undergo genetic testing that can be viewed as exploratory in nature and may not lead to changes in clinical care. Additionally, we did not explore the role or impact of the physician-patient interaction regarding PD genetic testing, which may affect participants’ decision on undertaking genetic testing for PD and other patient outcomes. Finally, we cannot assess causal relationships because of our cross-sectional design.
Conclusions and Practice Implications This study confirms an interest in genetic testing among individuals with PD and shows that a positive attitude regarding genetic testing is associated with interest in meeting with a genetic counselor. Results also identified gaps and misconceptions that some individuals with PD have about genetics and genetic testing. Our findings demonstrate a possible new niche for genetic counselors to support patients in clarifying gaps of knowledge or misconceptions regarding PD genetics as well as the risks, benefits, and limitations of genetic testing. Future research should include follow-up of individuals who have received genetic testing with and without genetic counseling to explore differences in genetic testing perception, knowledge, attitudes, and communication with family members. Acknowledgements The authors thank the patients in the University of Maryland Parkinson’s Disease and Movement Disorders Center (UMPDMC) for their participation. We thank Christina Griffin of UMPDMC for her assistance with recruiting and IRB application. This study was performed as part of a thesis project to fulfill a degree requirement of the Master’s of Genetic Counseling Training Program at the University of Maryland School of Medicine.
Parkinson’s Disease: Patients’ Knowledge, Attitudes, and Interest in Genetic Counseling
Compliance with Ethical Standards Conflict of Interest Kristin Maloney, Dina Alaeddin, Rainer von Coelln, Shannan Dixon, Lisa M. Shulman, Katrina Schrader, and Yue Guan report that they have no conflict of interest. Human Studies and Informed Consent The current study was reviewed and approved by the University of Maryland School of Medicine Institutional Review Board. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study. Animal Studies This article does not contain any studies with animals performed by any of the authors.
References Al-Mubarak, B. R., Bohlega, S. A., Alkhairallah, T. S., Magrashi, A. I., AlTurki, M. I., Khalil, D. S., et al. (2015). Parkinson’s disease in Saudi patients: a genetic study. PLoS One, 10(8), e0135950. https:// doi.org/10.1371/journal.pone.0135950. Berardelli, A., Wenning, G. K., Antonini, A., Berg, D., Bloem, B. R., Bonifati, V., et al. (2013). EFNS/MDS-ES/ENS [corrected] recommendations for the diagnosis of Parkinson’s disease. European Journal of Neurology, 20(1), 16–34. https://doi.org/10.1111/ene. 12022. Bosompra, K., Flynn, B. S., Ashikaga, T., Rairikar, C. J., Worden, J. K., & Solomon, L. J. (2000). Likelihood of undergoing genetic testing for cancer risk: A population-based study. Preventive Medicine, 30(2), 155–166. https://doi.org/10.1006/pmed.1999.0610. Bunn, J. Y., Bosompra, K., Ashikaga, T., Flynn, B. S., & Worden, J. K. (2002). Factors influencing intention to obtain a genetic test for colon cancer risk: a population-based study. Preventive Medicine, 34(6), 567–577. https://doi.org/10.1006/pmed.2002.1031. Calsbeek, H., Morren, M., Bensing, J., & Rijken, M. (2007). Knowledge and attitudes towards genetic testing: a two year follow-up study in patients with asthma, diabetes mellitus and cardiovascular disease. Journal of Genetic Counseling, 16(4), 493–504. https://doi.org/10. 1007/s10897-006-9085-9. Costain, G., Esplen, M. J., Toner, B., Hodgkinson, K. A., & Bassett, A. S. (2014a). Evaluating genetic counseling for family members of individuals with schizophrenia in the molecular age. Schizophrenia Bulletin, 40(1), 88–99. https://doi.org/10.1093/schbul/sbs124. Costain, G., Esplen, M. J., Toner, B., Scherer, S. W., Meschino, W. S., Hodgkinson, K. A., & Bassett, A. S. (2014b). Evaluating genetic counseling for individuals with schizophrenia in the molecular age. Schizophrenia Bulletin, 40(1), 78–87. https://doi.org/10.1093/ schbul/sbs138. de Lau, L. M., & Breteler, M. M. (2006). Epidemiology of Parkinson’s disease. Lancet Neurology, 5(6), 525–535. https://doi.org/10.1016/ S1474-4422(06)70471-9. Falcone, D. C., Wood, E. M., Xie, S. X., Siderowf, A., & Van Deerlin, V. M. (2011). Genetic testing and Parkinson disease: assessment of patient knowledge, attitudes, and interest. Journal of Genetic Counseling, 20(4), 384–395. https://doi.org/10.1007/s10897-0119362-0. Gasser, T. (2009). Mendelian forms of Parkinson’s disease. Biochimica et Biophysica Acta, 1792(7), 587–596. https://doi.org/10.1016/j. bbadis.2008.12.007.
Gupte, M., Alcalay, R. N., Mejia-Santana, H., Raymond, D., SaundersPullman, R., Roos, E., et al. (2015). Interest in genetic testing in Ashkenazi Jewish Parkinson’s disease patients and their unaffected relatives. Journal of Genetic Counseling, 24(2), 238–246. https:// doi.org/10.1007/s10897-014-9756-x. Haga, S. B., Barry, W. T., Mills, R., Ginsburg, G. S., Svetkey, L., Sullivan, J., & Willard, H. F. (2013). Public knowledge of and attitudes toward genetics and genetic testing. Genetic Testing and Molecular Biomarkers, 17(4), 327–335. https://doi.org/10.1089/ gtmb.2012.0350. Hann, K. E. J., Freeman, M., Fraser, L., Waller, J., Sanderson, S. C., Rahman, B., et al. (2017). Awareness, knowledge, perceptions, and attitudes towards genetic testing for cancer risk among ethnic minority groups: a systematic review. BMC Public Health, 17(1), 503. https://doi.org/10.1186/s12889-017-4375-8. Henneman, L., Vermeulen, E., van El, C. G., Claassen, L., Timmermans, D. R., & Cornel, M. C. (2013). Public attitudes towards genetic testing revisited: comparing opinions between 2002 and 2010. European Journal of Human Genetics, 21(8), 793–799. https://doi. org/10.1038/ejhg.2012.271. Hippman, C., Ringrose, A., Inglis, A., Cheek, J., Albert, A. Y., Remick, R., et al. (2016). A pilot randomized clinical trial evaluating the impact of genetic counseling for serious mental illnesses. The Journal of Clinical Psychiatry, 77(2), e190–e198. https://doi.org/ 10.4088/JCP.14m09710. Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: onset, progression and mortality. Neurology, 17(5), 427–442. Jallinoja, P., & Aro, A. R. (1999). Knowledge about genes and heredity among Finns. New Genetics and Society, 18(1), 101–110. Jankovic, J. (2008). Parkinson’s disease: clinical features and diagnosis. Journal of Neurology, Neurosurgery, and Psychiatry, 79(4), 368– 376. https://doi.org/10.1136/jnnp.2007.131045. Kalia, L. V., & Lang, A. E. (2015). Parkinson’s disease. Lancet, 386(9996), 896–912. https://doi.org/10.1016/S0140-6736(14) 61393-3. Kalinderi, K., Bostantjopoulou, S., & Fidani, L. (2016). The genetic background of Parkinson’s disease: current progress and future prospects. Acta Neurologica Scandinavica, 134(5), 314–326. https://doi. org/10.1111/ane.12563. Lees, A. J., Hardy, J., & Revesz, T. (2009). Parkinson’s disease. Lancet, 373(9680), 2055–2066. https://doi.org/10.1016/S0140-6736(09) 60492-X. Lesage, S., & Brice, A. (2012). Role of mendelian genes in Bsporadic^ Parkinson’s disease. Parkinsonism & Related Disorders, 18(Suppl 1), S66–S70. https://doi.org/10.1016/S1353-8020(11)70022-0. Moldovan, R., Pintea, S., & Austin, J. (2017). The efficacy of genetic counseling for psychiatric disorders: a meta-analysis. Journal of Genetic Counseling, 26(6), 1341–1347. https://doi.org/10.1007/ s10897-017-0113-8. Nalls, M. A., Pankratz, N., Lill, C. M., Do, C. B., Hernandez, D. G., Saad, M., et al. (2014). Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson’s disease. Nature Genetics, 46(9), 989–993. https://doi.org/10.1038/ng.3043. Nishigaki, M., Tokunaga-Nakawatase, Y., Nishida, J., & Kazuma, K. (2014). The effect of genetic counseling for adult offspring of patients with type 2 diabetes on attitudes toward diabetes and its heredity: a randomized controlled trial. Journal of Genetic Counseling, 23(5), 762–769. https://doi.org/10.1007/s10897-013-9680-5. Noyce, A. J., Bestwick, J. P., Silveira-Moriyama, L., Hawkes, C. H., Giovannoni, G., Lees, A. J., & Schrag, A. (2012). Meta-analysis of early nonmotor features and risk factors for Parkinson disease. Annals of Neurology, 72(6), 893–901. https://doi.org/10.1002/ana. 23687. Orr-Urtreger, A., Shifrin, C., Rozovski, U., Rosner, S., Bercovich, D., Gurevich, T., et al. (2007). The LRRK2 G2019S mutation in Ashkenazi Jews with Parkinson disease: is there a gender effect?
Maloney et al. Neurology, 69(16), 1595–1602. https://doi.org/10.1212/01.wnl. 0000277637.33328.d8. Rybicki, B. A., Johnson, C. C., Peterson, E. L., Kortsha, G. X., & Gorell, J. M. (1999). A family history of Parkinson’s disease and its effect on other PD risk factors. Neuroepidemiology, 18(5), 270–278. https://doi.org/10.1159/000026222. Sakanaka, K., Waters, C. H., Levy, O. A., Louis, E. D., Chung, W. K., Marder, K. S., & Alcalay, R. N. (2014). Knowledge of and interest in genetic results among Parkinson disease patients and caregivers. Journal of Genetic Counseling, 23(1), 114–120. https://doi.org/10. 1007/s10897-013-9618-y. Scuffham, T. M., McInerny-Leo, A., Ng, S. K., & Mellick, G. (2014). Knowledge and attitudes towards genetic testing in those affected with Parkinson’s disease. Journal of Community Genetics, 5(2), 167–177. https://doi.org/10.1007/s12687-013-0168-7. Searles Nielsen, S., Bammler, T. K., Gallagher, L. G., Farin, F. M., Longstreth Jr., W., Franklin, G. M., et al. (2013). Genotype and age at Parkinson disease diagnosis. International Journal of Molecular Epidemiology and Genetics, 4(1), 61–69. Sidransky, E., Nalls, M. A., Aasly, J. O., Aharon-Peretz, J., Annesi, G., Barbosa, E. R., Bar-Shira, A., Berg, D., Bras, J., Brice, A., Chen, C. M., Clark, L. N., Condroyer, C., de Marco, E. V., Dürr, A., Eblan, M. J., Fahn, S., Farrer, M. J., Fung, H. C., Gan-Or, Z., Gasser, T., Gershoni-Baruch, R., Giladi, N., Griffith, A., Gurevich, T.,
Januario, C., Kropp, P., Lang, A. E., Lee-Chen, G. J., Lesage, S., Marder, K., Mata, I. F., Mirelman, A., Mitsui, J., Mizuta, I., Nicoletti, G., Oliveira, C., Ottman, R., Orr-Urtreger, A., Pereira, L. V., Quattrone, A., Rogaeva, E., Rolfs, A., Rosenbaum, H., Rozenberg, R., Samii, A., Samaddar, T., Schulte, C., Sharma, M., Singleton, A., Spitz, M., Tan, E. K., Tayebi, N., Toda, T., Troiano, A. R., Tsuji, S., Wittstock, M., Wolfsberg, T. G., Wu, Y. R., Zabetian, C. P., Zhao, Y., & Ziegler, S. G. (2009). Multicenter analysis of glucocerebrosidase mutations in Parkinson’s disease. The New England Journal of Medicine, 361(17), 1651–1661. https://doi.org/ 10.1056/NEJMoa0901281. Tan, E. K., & Jankovic, J. (2006). Genetic testing in Parkinson disease: promises and pitfalls. Archives of Neurology, 63(9), 1232–1237. https://doi.org/10.1001/archneur.63.9.1232. Tan, E. K., Lee, J., Hunter, C., Shinawi, L., Fook-Chong, S., & Jankovic, J. (2007). Comparing knowledge and attitudes towards genetic testing in Parkinson’s disease in an American and Asian population. Journal of the Neurological Sciences, 252(2), 113–120. https://doi. org/10.1016/j.jns.2006.10.016. Uhlmann, W. R., Schuette, J. L., & Yashar, B. (2011). A guide to genetic counseling (pp. 7): John Wiley & sons. US Census Bureau. (2016). Educational attainment in the United States: 2016 Retrieved January 9, 2018, from https://www.census.gov/data/ tables/2016/demo/education-attainment/cps-detailed-tables.html.