Neurobiological and Psychosocial Correlates of Communication Between Huntington’s Disease Patients and Their Offspring
Publication: The Journal of Neuropsychiatry and Clinical Neurosciences
Abstract
Objective:
Huntington’s disease (HD) is an autosomal dominant neurodegenerative disease that presents significant challenges to family communication. The investigators examined observations of communication between parents with HD and their offspring talking about the challenges of HD and explored potential correlates of their communication.
Methods:
The sample included parents with HD and their adolescent and young-adult offspring (N=64). Parent communication and chorea were independently coded from video recordings. Parents and offspring completed working memory assessments and self-reports of neuropsychiatric symptoms, stress, and coping.
Results:
Evidence was found for the association of observed parent-offspring communication with disease markers, psychosocial characteristics, and neurocognitive function. For parents, disease markers and working memory were correlates of communication, whereas offspring’s psychiatric symptoms, stress, and coping were associated with their communication.
Conclusions:
These findings have potential implications for clinical interventions to enhance communication and quality of life for HD families.
Family relationships play a central role in health and illness. Close familial relationships are associated with better physical and mental health across the lifespan, whereas family conflict and strained relationships are associated with increased morbidity and mortality (1). Communication within the family may be especially important in the context of chronic illness, as family members often assist in disease management and provide instrumental and emotional support to one another. Families facing chronic illness experience persistent demands related to treatment, lifestyle and role adjustments, financial hardship, and serious medical events that can lead to poorer family cohesion and the breakdown of effective communication (2, 3).
Challenges to communication may be paramount in families faced with Huntington’s disease (HD), an autosomal dominant neurodegenerative disease caused by an expanded cytosine-adenine-guanine (CAG) repeat on the huntingtin gene and characterized by progressive cognitive, behavioral, emotional, and motor impairments. HD places a particular burden on the parent-offspring relationship because symptom onset is often in middle adulthood, a period that includes the primary years for parenting, and its heritability places offspring at a 50% risk for inheriting the mutation of the huntingtin gene (4). Families experience high levels of stress, and skillful communication within the parent-offspring relationship is important for managing and coping with the disease (5). However, the symptoms of HD likely present significant communication challenges, as cognitive impairments can adversely affect language skills, motor impairments can affect speech quality, and psychiatric symptoms can affect behavioral and emotional aspects of communication (6).
Qualitative research has highlighted significant disruptions in the communication skills of individuals with HD (7–10). More limited research has reported communication difficulties in HD using quantitative methods. For example, Jona et al. (11) found that individuals with HD and their partners reported significant deficits in communication and reduced affective engagement on a questionnaire. Two studies obtained questionnaire reports from offspring and found significant family challenges, including poor family cohesion, conflict, and verbal expressiveness (12), as well as increasing parent-child conflict with greater severity of parents’ HD symptoms (13).
An important direction for research is the use of observational methods to capture the quality of communication between parents with HD and their offspring. This method provides objective samples of emotions and behaviors that are less subject to problems of bias and retrospective recall that is a limitation of qualitative and self-reported measures. Furthermore, direct observations provide a more nuanced understanding of behavioral and affective aspects of dyadic communication that can inform family interventions to enhance communication skills (14, 15). In addition, although previous research suggests that communication may be impaired in families affected by HD, studies have not yet explored factors that may be related to disruptions in this population. Therefore, in the present study, we examined several correlates of emotional and behavioral aspects of parent-offspring communication during a conversation about the challenges of HD.
First, several psychosocial factors may be related to communication. Many families experience significant HD-related stress that may interfere with communicating about the disease, as high stress levels may lead to irritability and conflict (16). The high levels of stress further point to the importance of how individuals cope with HD-related stress, which may in turn be related to the ways they communicate about their experiences. Coping involves cognitive and behavioral efforts directed either toward or away from the source of stress (17). Primary control coping includes efforts to change the stressor or one’s emotions (e.g., problem solving); secondary control coping includes efforts to adapt to the stressor (e.g., acceptance); and disengagement coping involves efforts to evade the stressor or one’s emotions (e.g., avoidance). Parents and offspring who cope with HD-related stress using fewer primary and secondary control strategies and greater disengagement strategies may in turn communicate less effectively about HD, including talking less openly, listening less attentively, and displaying more negative emotions. Furthermore, HD is often characterized by depression and anxiety (18) and research suggests offspring may be at increased risk for psychiatric problems due to family stress (13, 19). Previous research has shown depression and anxiety symptoms predict less positive communication (20); therefore, psychiatric symptoms associated with HD may interfere with effective parent-offspring communication.
Second, previous studies have established links between executive functioning and communication in populations with neurodevelopmental disorders (21) and individuals with aphasia (22). Working memory is an executive functioning skill that involves the ability to process, hold, and manipulate information in one’s immediate memory (23). Working memory is likely an important foundational skill for the complex process of communication, including being able to comprehend a situation, formulate thoughts, and consider multiple perspectives. Given that working memory is impaired in HD (24), weaknesses in neurocognitive functioning may contribute to less effective communication. For offspring, research has established links between working memory and coping skills (25); however, studies have not examined the possible link between working memory and communication.
Finally, markers of disease severity for parents with HD may be associated with observed communication, given previous findings that communication skills decline as the disease progresses (7). Two variables that reflect disease severity are the CAG age-product (CAP) score and chorea. The CAP score provides an approximate measure of the length and severity of the patient’s exposure to the effects of mutant huntingtin, with higher scores indicating worse functioning (26). The hallmark symptom of HD is chorea: abnormal, involuntary movements that are brief, abrupt, irregular, and nonstereotyped and affect various body parts. Therefore, it is expected that higher CAP scores and greater chorea will both be associated with observations of less effective communication.
Here, we aimed to obtain direct observations of parents with HD and their offspring, discussing the challenges of being part of a family affected by HD, and to examine potential psychosocial, neurocognitive, and disease marker correlates of communication.
Methods
Participants
Participants were drawn from a sample of 37 family units that included 37 parents with HD and 44 adolescent and young-adult offspring who were enrolled in a study of stress, coping, and communication in families with HD whose demographic characteristics modeled that of persons with HD in the United States (26). Three families did not complete the observation task due to discomfort, and two families did not complete the task due to time constraints. There were no significant differences between families who completed the observation and those who did not on parent or offspring psychiatric symptoms, stress, coping, neurocognitive functioning, or parental disease characteristics. One offspring per family was randomly selected for analysis using a virtual coin toss method to insure the independence of observations.
Procedure
Families were recruited through a Huntington’s Disease Society of America Level 1 Center of Excellence (COE) in the southeastern United States. Families were eligible if the parent had a diagnosis of HD, had verbal ability sufficient to participate in a conversation about HD, had at least one biological offspring between 10 and 39 years old, was receiving care at the HD COE Clinic at the research site, and was fluent in English. Parents and offspring completed online surveys, neurocognitive testing, and two 10-minute video-recorded conversations. In the first conversation, parents and offspring discussed a positive experience they shared. In the second conversation, which is the focus of the present analyses, parents and offspring discussed the stresses and challenges of HD. Parents and offspring were given a task card with questions to facilitate conversation (e.g., “What has been the hardest part for each of us about HD?”). Informed consent and assent were obtained prior to study participation. Families were compensated after the study visit. The institutional review board at Vanderbilt University approved the study protocol and consent procedures.
Measures
Demographic characteristics.
Parents and offspring provided their age, sex, and race.
Disease characteristics.
Parent CAP scores were computed by the following equation: (CAG repeat length−33.66)×age (27). The CAG repeat lengths were extracted from medical records. Parent observed chorea was rated by a board-certified neurologist (D.C.) from observations of the parent-offspring conversation. The Unified Huntington’s Disease Rating Scale total maximal chorea score in seven body parts was calculated based on established criteria (28). This score ranges from 0 to 28, with a higher score indicating greater chorea.
Observed communication.
The parent-offspring conversation about HD was coded using the Iowa Family Interaction Rating Scales (IFIRS) (29), a macro-level coding system designed to assess verbal (e.g., content) and nonverbal emotional (e.g., eye contact) and behavioral aspects of communication. Codes are assigned values from 1 (not at all characteristic) to 9 (mainly characteristic) that take into consideration the frequency, intensity, and affective tone of the behavior. IFIRS has been validated in families faced with acute and chronic illnesses (30, 31). Parents and offspring were rated on four codes to assess emotional and behavioral aspects of communication. Sadness and hostility reflect affective components of communication, while listener responsiveness and communication reflect skills in the attentive listening, verbal expression, solicitation of information, and perspective taking.
All coding was completed by team members with a master’s degree or higher. Coders first passed a written exam, achieving a score ≥80%. Each video was independently rated by two trained coders who met to compare their ratings during a consensus meeting. Per the manual (29), if scores differed by one point, the higher score was given. Any code that differed by two or more points was discussed and assigned a consensus rating. Codes that were given the same rating or differed by one point were considered reliably coded. The percentage of agreement between coders was calculated to determine interrater reliability and ranged from 78% to 91% for the parent and offspring codes.
Neurocognitive function.
Parent and offspring working memory was assessed using the List Sorting Working Memory Test (LSWMT) from the National Institutes of Health (NIH) Toolbox Cognition Battery administered by trained research assistants on an iPad (32, 33). The LSWMT requires the immediate recall and sequencing of various orally and visually presented stimuli. Scores were converted to age-adjusted standardized scores (mean=100 [SD=15]) using a nationally representative normative sample. This task has been shown to be developmentally appropriate for ages 7 to 85 years old (33, 34).
Stress and coping.
Parent and offspring HD-related stress and coping were measured using the Responses to Stress Questionnaire–Huntington’s Disease Version (25, 35). Participants were presented with 10 representative stressors related to HD (e.g., fear about my future, feeling isolated from friends or family) and asked to indicate whether they experienced each stressor in the previous 6 months. A sum of the stressor items endorsed was calculated for each participant. Participants then responded to 57 items that reflect coping and automatic responses to stressors. The three coping factors calculated include primary control (e.g., problem solving, emotional expression), secondary control (e.g., acceptance, cognitive reappraisal), and disengagement (e.g., wishful thinking, avoidance). To control for response bias in item endorsement, proportion scores were calculated by dividing the total score for each coping factor by the total score on the RSQ (36). Internal consistency for the coping factors ranged from α=0.70 to 0.85.
Psychiatric symptoms.
Parent depressive symptoms were assessed using the Patient Health Questionnaire–9 (PHQ-9) (37), a self-report measure of the nine symptoms of major depressive disorder based on DSM-IV criteria. Parents rated each item on a scale of 0 to 3 on the basis of how much a symptom bothered them in the past 2 weeks. Cut-offs for the PHQ-9 are minimal (1–4), mild (5–9), moderate (10–14), moderately severe (15–19), and severe (20–27) depression.
Offspring affective problems were assessed using the anxious/depressed subscales of the Youth Self-Report (YSR) (38) and the Adult Self-Report (ASR) (39). Offspring younger than 18 years old completed the YSR; offspring 18 years and older completed the ASR. These instruments are empirically based, developmentally appropriate tools to assess emotional and behavioral problems across the lifespan (40, 41). They have also shown excellent internal consistency, test-retest reliability, and construct validity. Internal consistency for the anxious/depressed subscales in the present sample was α=0.91 (YSR) and α=0.88 (ASR).
Statistical Analyses
Descriptive statistics were calculated for all measures and IFIRS codes. Independent sample t tests were used to compare mean scores between mothers and fathers on the parent variables. Within-subject mean scores for the IFIRS codes were compared for parents and offspring using paired sample t tests. Associations of observed communication with disease variables, neurocognitive function, and psychosocial factors were tested using bivariate correlations. Two-tailed tests were used to determine statistical significance in all analyses. Pairwise deletion (available case analysis) was used for all analyses. All statistical analyses were computed using SPSS (Version 27).
Results
Descriptive Statistics
The final sample (N=64) included 32 parents with HD and their offspring (10–37 years old; N=32). Forty-seven percent of parents were mothers. Parents had a mean age of 47.66 years (SD=9.14) and a mean CAP score of 477.52 (SD=96.21). As is representative of the HD population in the United States, 94% of parents identified as White (26). Offspring had a mean age of 21.41 years (SD=7.96), predominantly identified as White (88%) and female (59%). Twenty-six (81.3%) of the offspring had not undergone genetic testing and therefore did not know their genetic status at the study visit.
The means and standard deviations for all study variables are shown in Table 1. Mothers reported greater use of primary control coping compared with fathers (t=2.18, df=27, p<0.05), and mothers were also rated as having higher scores in communication (t=3.10, df=30, p<0.01). With regard to IFIRS, for parents, the mean score for sadness was significantly higher than the mean score for hostility (t=10.61, df=31, p<0.001). The same pattern was observed for offspring, as the sadness mean score was significantly higher than the hostility mean score (t=5.98, df=31, p<0.001). Both comparisons are large effect sizes (all Cohen’s d values >1.00). For behavioral aspects of communication, the difference between parents’ communication skills and responsive listening approached significance (t=-1.88, df=31, p=0.07). For offspring, the mean for communication skills was significantly higher than the mean for responsive listening (t=2.47, df=31, p=0.02). Both comparisons are small effects (all Cohen’s d values <0.50).
| Parents | Offspring | |||
|---|---|---|---|---|
| Characteristic | Mean | SD | Mean | SD |
| IFIRS | ||||
| Sadness | 5.13 | 1.86 | 4.91 | 1.73 |
| Hostility | 1.56 | 0.76 | 2.38 | 1.50 |
| Listener responsiveness | 5.66 | 1.29 | 5.38 | 1.24 |
| Communication | 5.28 | 1.65 | 5.91 | 1.42 |
| NIH Toolbox LSWMT | 81.94 | 17.65 | 99.28 | 16.79 |
| RSQ | ||||
| Primary control coping | 0.18 | 0.05 | 0.23 | 0.17 |
| Secondary control coping | 0.25 | 0.06 | 0.26 | 0.06 |
| Disengagement coping | 0.14 | 0.04 | 0.15 | 0.03 |
| CAP score | 477.52 | 96.21 | N/A | — |
| Chorea | 6.16 | 4.07 | N/A | — |
| PHQ-9 score | 9.55 | 6.02 | N/A | — |
| YSR and ASR (anxious and depressed subscales) scores | NA | — | 58.69 | 10.31 |
a
ASR=Adult Self-Report; CAP=CAG-age product; IFIRS=Iowa Family Interaction Rating Scales; LSWMT=List Sorting Working Memory Task; NA=not applicable; PHQ-9=Patient Health Questionnaire–9; RSQ=Responses to Stress Questionnaire; YSR=Youth Self-Report.
Performance on the NIH Toolbox LSWMT was significantly below the population mean of 100 for parents, but in the average range for offspring. The mean for parents’ PHQ-9 was at the upper end of the mild depression range, and 55% of parents scored in the moderate to moderately severe range. The mean score for offspring on the anxious/depressed subscales was approximately three-quarters of a standard deviation above the normative mean. In addition, 24% scored above the borderline cut-off (T≥65).
Neurobiological and Psychosocial Correlates of Parent Communication
Parent sadness was significantly and positively associated with self-reports of stress (r=0.48, df=27, p=0.01) and depressive symptoms (r=0.46, df=27, p=0.01). Listener responsiveness was significantly and positively associated with working memory skills (r=0.64, df=29, p<0.001) and negatively associated with CAP scores (r=−0.48, df=28, p=0.01) and observed chorea (r=−0.35, df=30, p=0.052). Communication skills were significantly and negatively associated with CAP scores (r=−0.57, df=28, p=0.001) and observed chorea (r=−0.57, df=30, p=0.001) and positively associated with working memory skills (r=0.63, df=29, p<0.001). All of the significant correlations reflect medium to large effect sizes. Parents’ observed emotional and behavioral communication was unrelated to coping with HD-related stress.
Neurobiological and Psychosocial Correlates of Offspring Communication
Offspring hostility was significantly and negatively associated with self-reports of secondary control coping (r=−0.40, df=27, p=0.03), and positive associations approached significance with disengagement coping (r=0.34, df=27, p=0.07) and HD-related stress (r=0.33, df=27, p=0.08). Offspring listener responsiveness was significantly and negatively associated with disengagement coping (r=−0.57, df=27, p=0.001) and positively associated with secondary control coping (r=0.38, df=27, p=0.04); it approached significance with primary control coping skills (r=0.32, df=27, p=0.10). Offspring’s communication skills were significantly and positively associated with primary control coping (r=0.50, df=27, p=0.01) and negatively associated with disengagement coping (r=−0.55, df=27, p=0.002); it approached significance with anxious/depressed symptoms (r=−0.36, df=27, p=0.06). All of the significant correlations reflect medium to large effect sizes. Offspring’s observed emotional and behavioral communication was not significantly related to offspring age or working memory, with one exception for working memory and communication skills (r=0.31, df=30, p=0.09).
Discussion
The primary aim of this study was to obtain observations of parents with HD and their offspring communicating about the challenges of HD and to examine potential psychosocial, neurocognitive, and disease marker correlates of emotional and behavioral aspects of communication. Communication between parents and offspring plays a central role in family adaptation to disease. Although previous research suggests communication is disrupted in HD families, to our knowledge relatively few studies have directly observed communication in HD (42, 43).
Mean levels of observed sadness and hostility, along with communication and responsive listening, in our study suggest that there is considerable, meaningful variability in the emotional and behavioral aspects of communication while talking about experiences with HD. Although previous research has noted greater levels of irritability and hostility in HD patients (44) and heightened levels of conflict in HD families (12), it is noteworthy that in our sample, observed levels of hostility were significantly lower than levels of sadness for both parents and offspring, and overall hostility was relatively infrequent and displayed at only low levels of intensity during the conversation about HD.
There was considerable support for significant associations of parent disease characteristics, cognitive functioning, and some psychosocial factors with observed parent emotions and communication patterns. Specifically, there was evidence that at more advanced stages of disease, parents displayed less effective communication (e.g., perspective taking, providing explanations and reasoning) and less attentive listening with their offspring. With regard to cognitive functioning, previous research has established that HD is marked by working memory deficits (24). Our findings not only replicate those findings but also showed parents’ lower working memory skills were associated with less effective communication patterns and less responsive listening in conversations with their children. These findings provide evidence for the association between neurocognitive functioning and communication in this population and suggest one consequence of declining working memory may be poorer communication and listening skills. There was also evidence for the construct validity of the IFIRS codes, as observed parental sadness was significantly related to parent self-report of depressive symptoms and HD-related stress. However, parents’ coping strategies in response to HD-related stress were unrelated to their observed emotions and behaviors.
There was evidence that for offspring, HD-related stress, coping, and psychiatric symptoms but not age or neurocognitive function were significantly associated with their observed emotions and communication patterns. Offspring who reported experiencing greater HD-related stress were observed to be more hostile toward the parent with HD and displayed higher levels of sadness. Additionally, offspring who used greater primary control coping strategies in response to HD-related stress, such as problem solving and skillfully expressing their emotions, were observed to be more effective communicators, and offspring who used more secondary control coping strategies (e.g., acceptance, cognitive reappraisal) were less hostile toward their parents and were more sensitive listeners. In contrast, offspring who relied on greater disengagement strategies to deal with HD-related stress (e.g., avoidance, denial) were observed to be more hostile, less effective communicators, and less attentive listeners to their parents during a conversation about HD. In addition, offspring’s self-reports of greater anxiety and depressive symptoms were associated with observations of less skilled communication. These findings provide evidence that HD-related stress, coping, and psychiatric symptoms are related to how offspring communicate with their parents about their experiences with HD, and may have important implications for family-focused interventions to improve both individual and family functioning.
These important findings notwithstanding, our study has several limitations. First, the sample size limited statistical power to observe significant effects. However, despite the sample size, a number of significant effects were detected. Second, although a majority of families participated in the video-recorded conversations, three families declined, and therefore the sample may not be fully representative of parents with HD and their offspring. For example, it is possible that families in severe conflict may not have volunteered to participate. Third, the study was cross-sectional and so the direction of effects cannot be determined. And fourth, total maximal chorea was rated with the Unified Huntington’s Disease Rating Scale, which does not address certain aspects key to communication in HD (e.g., perseverations). These limitations were offset in part by a number of notable strengths, including a multimethod design using observations of family communication in HD and identifying correlates of communication for parents and offspring.
These findings have several implications for directions for future research and clinical applications. Future studies are needed to extend this observation method to other family members (e.g., spouses). Additionally, it will be important to use a longitudinal method to examine the role of parent communication on offspring’s psychiatric and cognitive functioning in HD families. These findings also have potential implications for interventions and suggest there are at least three avenues to intervene to improve family communication. First, in addition to speech therapy (43) and communication aids (42) that can support communication for patients with HD, these findings suggest that programs to directly teach specific skills to parents and offspring (e.g., attentive listening) may also be important for improving family communication (14). Second, the findings suggest that in order to improve communication skills in parents with HD, it may be important to also address declining executive functioning skills. Previous research has shown promise for improving executive functioning through cognitive training programs in HD populations (45). For offspring, the findings suggest it may be important to reduce neuropsychiatric symptoms as well as teach coping skills to reduce avoidance and improve skills including acceptance, problem solving, emotional expression, and cognitive reappraisal. Previous studies have shown it is possible to improve communication and coping skills and reduce neuropsychiatric symptoms through family interventions (14).
Conclusions
In summary, these findings provide preliminary evidence that family communication in HD can be captured in real time using observational methods. The emotional and behavioral aspects of parent and offspring communication were associated with individual characteristics, including psychosocial factors, neurocognitive functioning, and markers of disease severity. The findings highlight the potential importance of interventions aimed at simultaneously addressing cognitive functioning and coping skills in HD families to improve family communication.
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Information & Authors
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Published In
History
Received: 23 December 2020
Revision received: 22 March 2021
Accepted: 6 May 2021
Published online: 19 July 2021
Published in print: Fall 2021
Keywords
Authors
Competing Interests
Supported by funds from the Griffin Family Foundation and by NIMH (grant T32-MH018921).
Funding Information
The authors report no financial relationships with commercial interests.
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