The Impact of Paediatric Neuromuscular Disorders on Parents' Health-Related Quality of Life and Family Functioning
Aims: This study aimed to evaluate the impact of hereditary neuromuscular disorders on parent's health-related quality of life and family functioning, and to study the correlation of parental stress on family impact. Methods: This retrospective cross-sectional study analysed responses from 80 parents of 80 children with different neuromuscular disorders on two self-reported questionnaires: the Chinese version of PedsQLFamily Impact Module and the Parental Stress Scale. Results: We found the Parental Stress Score exhibited a moderate negative correlation with the PedsQLFamily Impact Module total score (Pearson correlation coefficient: -0.55). Among different neuromuscular disorders, spinal muscular atrophy had the worst negative family impact. Additionally, a non-walking status had moderate negative effects on family impact (T-test effect size: 0.71). Conclusion: Neuromuscular disorders cause a significant negative family impact. Evaluation of parental stress, parental health-related quality of life and family functioning should be part of the standard of care for affected families.
Keyword : Neuromuscular disorders; Quality of life research
Hereditary neuromuscular disorders (NMDs) are a heterogeneous group of conditions cause by underlying genetic mutation(s) leading to diseases arising from different parts of the lower motor neuron units. These diseases differ regarding age of onset, disease progression and life expectancy and commonly cause orthopaedic, respiratory, cardiovascular, nutritional and gastrointestinal complications. A child with an NMD presents a complex challenge to the whole family. Parents of chronically ill children frequently report physical, emotional and cognitive problems.1 Conversely, the family's wellbeing affects the care received by the ill child.2 Therefore, the importance of assessing the impact of chronic illness on parents or families has become evident. Parents with children having chronic illnesses often have significant stress affecting multiple aspects of their life.3
The family impact of an NMD can be evaluated by considering the effects of the disease on individual members (e.g., the parental HRQOL) and the overall family (e.g., family functioning). The parental HRQOL is a multi-dimensional construct used to evaluate parents' perceptions of the effects of their children's disease on the different life domains related to physical, mental and social wellbeing.4 Family functioning refers to a family's ability to accomplish tasks important to wellbeing, adapt to changing circumstances or balance the needs of individuals with those of the entire family.5 Up to date, very few reports have documented the family impacts of NMDs, or compared the family impacts of different paediatric NMDs.
The Family Impact Module (FIM) of the Paediatric Quality of Life Inventory (PedsQL4.0) (PedsQL©1998 JW Varni, Ph.D. All rights reserved) is a validated parent-report questionnaire developed by Varni et al6 and cross-culturally adapted into Chinese by Chen et al.7 The Chinese version comprises nine domains-Physical functioning, Emotional functioning, Social functioning, Cognitive functioning, Communication, Worry, Daily activities, Family relationships and Finance. The first 4 subscales measures parent self-reported HRQOL functioning, and the Daily activities and Family relationships subscales measure parent-reported family functioning and is commonly used to assess family impact. By contrast, other available instruments are generally brief and one-dimensional.8
The Chinese version of the Parental Stress Scale (PSS), a validated self-report scale developed by Cheung,9 was adapted from the Parental Stress Scale developed by Berry and Jones.10 This scale measures the level of stress experienced by parents and considers both positive (e.g., emotional benefits, self-enrichment, personal development) and negative components of parenthood (e.g., demands on resources, opportunity costs, restrictions). This one-page questionnaire is half the length of the PedsQLFIM and is commonly used in Hong Kong to screen and identify parents experiencing stress and to facilitate early referrals to clinical psychology services. However, it remains uncertain whether the PSS score correlates with a poor parental HRQOL or poor family functioning. Therefore, this study aimed to systemically evaluate the parental HRQOL and family functioning in the families of paediatric patients with NMD and to examine the correlations of these measures with parental stress.
At our hospital, all families of children with hereditary NMDs attend paediatric neuromuscular disorder clinics and complete the Chinese versions of the PSS and PedsQLFIM upon diagnostic confirmation. This retrospective study evaluated the parents' responses to both questionnaires during follow-up visits at our neuromuscular disorder clinics during the period of 4th July 2016 to 15th March 2018. Data on the age, sex, diagnosis, comorbidities, ambulation status (walker/non-walker), ventilation support (does/does not require) and feeding status (requires/does not require assistance) of each paediatric NMD patient were systematically collected from the electronic patient health record system at the same time as the questionnaire completion.
The patients' diagnoses were classified into one of four groups. Group 1 comprised patients with deteriorating muscle diseases, mainly Duchenne muscular dystrophy and congenital muscular dystrophy. Group 2 comprised patients with types 1 to type 3 5q spinal muscular atrophy (SMA), representing deteriorating motor neuron diseases. Group 3 comprised patients with stable neuromuscular diseases including congenital myopathy and congenital myasthenic syndrome. All patients with congenital myasthenic syndrome received oral medical therapy that resulted in clinical motor improvement. Group 4 comprised patients with hereditary stable peripheral nerve diseases with minimal or mainly distal weakness.
The parent who served as the main caregiver was invited to complete the questionnaires. If the questionnaires were completed during multiple visits, only the results from the first set were collected and documented. The total score, parental HRQOL summary score, family functioning summary score and each dimensional score in the PedsQLFamily Impact Module were computed according to the guideline provided by the developer. The total PSS score was also computed.
The primary study outcomes were the parental HRQOL and level of family functioning, measured by the PedsQLFIM. The secondary outcome was the correlation between PedsQLFIM and PSS.
The PedsQLFIM comprised 37 items across 9 domains. The Finance domain was not included in the analysis since this domain was only introduced in the Chinese version of the questionnaire and was not part of the validated original questionnaire developed by Varni et al. The parental HRQOL summary score was calculated as the average of the physical, emotional, social and cognitive functioning scores. The family functioning summary score was calculated as the average of the daily activities and family relationships scores.8 All scores ranged from 0 to 100, with higher scores indicative of better functioning. The total PedsQLFIM scores were compared with those of children with other neurological conditions. These were obtained from published studies that used the PedsQLFIM to assess paediatric neurological diseases in comparable sample sizes. The selected data for comparison were extracted from a study of acquired brain injury by de Kloet et al.11
The PSS comprised 17 items scored on a 6-point scale; higher scores indicate greater stress. Previous data indicated that a cut-off point of 52/53 could be used to demarcate parent groups exhibiting satisfactory adjustment vs maladjustment. This scale had demonstrated satisfactory levels of internal reliability and test-retest reliability.9,10
Descriptive statistics were calculated for the demographic features. Means and standard deviations (SD) of the PedsQLFIM and PSS scores were calculated for the total study sample and subgroups stratified by diagnosis and ambulation status. A t-test was used to compare data sets.
To compare the PedsQLFIM scale and total scores of patients with different diagnoses, the data was log10 transformed before analysis since the distribution of the data was not normal. A one-way analysis of variance (ANOVA) and post-hoc Tukey Kramer analysis were conducted.
A Pearson product-moment correlation analysis was used to determine the linear correlation between the PSS score and PedsQLFIM scale and summary scores. All statistical analyses were conducted using SPSS Statistics 20 (IBM, Armonk, NY, USA). Statistical significance was defined as p-value of <0.05.
This study was approved by the relevant Institutional Review Board.
Eighty parent reported PedsQLFIM and PSS questionnaires were collected from 21 fathers and 59 mothers. Most of the affected NMD children were medically stable and ambulatory (81% walkers, 94% not requiring ventilation support, 99% on full oral feeding).
The distribution of the patient demographics and age ranges of patients in the four disease groups are shown in Table 1.
The means and standard deviations of the PedsQLFIM scores of the four NMD groups are presented in Table 2. Among the eight inventory domains, the domain on 'Worry' received the worst scale score. The Cronbach's alpha coefficients for the total and all scale scores ranged from 0.86 to 0.98. No floor or ceiling effect was observed (floor/ceiling percentages: 0.0-18.7%). Furthermore, when the PedsQLFIM scores were compared among the 4 different groups of NMDs, parents in Group 2 (deteriorating motor neuron diseases) reported the lowest total and scale scores across all items. Parents in Group 4 (hereditary peripheral neuropathies) yielded the highest total and scale scores. A one-way ANOVA revealed significant differences among the mean PedsQLFIM total, parental HRQOL and family functioning scores of different disease groups (all p<0.01). A post-hoc analysis revealed that Group 2 accounted for the greatest differences in the mean scores when compared with the other groups. The results of the ANOVA and post-hoc analysis are shown in Table 3. Additionally, the PedsQLFIM scores were compared according to ambulation status. A non-walking status was found to have moderate negative effects on the overall family impact, parent HRQOL and family functioning scores (T-test effect size: 0.71-0.83) (Table 4). Moreover, the PedsQLFIM total score in our NMD cohort was worse than that of the patients with acquired brain injuries,11 as demonstrated in Table 5.
The Cronbach's alpha coefficient for the PSS was 0.89, indicating high internal consistency. The PSS score exhibited a moderate negative correlation with the PedsQLFIM total score (Figure 1) (Pearson correlation coefficient: -0.55). Specifically, parents with a higher level of stress reported a significantly lower HRQOL and poorer family functioning. When a cut-off of 52/53 was used to categorise parents into low- and high-stress groups, 36.63% of parents were in the high stress group. The corresponding mean PedsQLFIM total scores were 75.92 (SD = 12.83) and 62.16 (SD = 15.38), respectively. This difference was significant and had a large effect size of 0.98.
This study conducted a multi-dimensional investigation of the family impact of NMDs. In this cohort, the affected NMD patients were mostly medically stable and ambulatory. The parents reported a poor parental HRQOL and a low level of family functioning significantly worse than those reported in acquired brain injury. Our findings suggested that rare hereditary NMD diseases with complex medical needs, have significant negative family impacts and the family needs should not be neglected.
This study found that out of the eight domains of the PedsQLFIM, parents reported the worst scores in the 'Worry' domain, which included worries about others' reactions to their child's condition. Previous studies revealed that some parents of children with disabilities avoided their relatives and friends since their child's and family's needs were often not understood by others.14 As NMDs are rare diseases, they are often poorly understood by the general public. Therefore, parents might be particularly worried about others' reactions to their affected child. The Worry domain also addressed worries on the efficacy and safety of the child's treatment, as well as the child's future. The current findings may correlate with the fact that treatments for some NMDs remain under research and there are still lack of cures or disease-modifying treatments for many NMDs at the current stage. Furthermore, NMDs have variable prognoses, and the uncertain treatment outcomes might increase parents' concerns about their child's future.
The lack of the availability of effective treatment that resulted in a negative family impact at the time of this study, was especially evident in the deteriorating motor neuron disease group 2 comprised of patients with 5q SMA. SMAs are mainly treated via supportive interventions during the study period from July 2016 to March 2018. The first US Food and Drug Administration (FDA)-approved drug treatment for SMA, named nusinersen, was available in the United States since December 2016. During the study period, Spinraza was not available to the patients with SMAs in Hong Kong. Parents were anxious about the deteriorating course of the disease without accessibility to the available treatment, and these concerns may have contributed to the poorer parental HRQOL and level of family functioning in this group. On the other hand, the PedsQLFIM scores from the deteriorating muscles diseases (the group with muscular dystrophies) and the stable neuromuscular diseases groups (the group with congenital myopathy and congenital myasthenic syndrome) were comparable. The PedsQLFIM scores of the peripheral neuropathy group were highest. This suggests the inaccessibility of available treatment might have a significant negative family impact in addition to the rate of disease progression. For DMD, the currently available with the fact that treatments for some NMDs remain under research and there are still lack of cures or disease-modifying treatments for many NMDs at the current stage. Furthermore, NMDs have variable prognoses, and the uncertain treatment outcomes might increase parents' concerns about their child's future.
The lack of the availability of effective treatment that resulted in a negative family impact at the time of this study, was especially evident in the deteriorating motor neuron disease group 2 comprised of patients with 5q SMA. SMAs are mainly treated via supportive interventions during the study period from July 2016 to March 2018. The first US Food and Drug Administration (FDA)-approved drug treatment for SMA, named nusinersen, was available in the United States since December 2016. During the study period, Spinraza was not available to the patients with SMAs in Hong Kong. Parents were anxious about the deteriorating course of the disease without accessibility to the available treatment, and these concerns may have contributed to the poorer parental HRQOL and level of family functioning in this group. On the other hand, the PedsQLFIM scores from the deteriorating muscles diseases (the group with muscular dystrophies) and the stable neuromuscular diseases groups (the group with congenital myopathy and congenital myasthenic syndrome) were comparable. The PedsQLFIM scores of the peripheral neuropathy group were highest. This suggests the inaccessibility of available treatment might have a significant negative family impact in addition to the rate of disease progression. For DMD, the currently available health status, could not be assessed. Furthermore, families between NMD groups were not matched by demographic variables, as inter-group differences may not be solely explained by the difference in diagnosis. Future studies with larger number of NMD patients with data stratification by different demographic variables, could be helpful to identify underlying risk and protective factors for parental stress and family functioning. Finally, this study included only patients attending the outpatient NMD clinics with a stable general health and not those with frequent inpatient admissions with more severe disease complications. Therefore, the results may not be able to reflect the family impact of NMDs of the whole spectrum of severity but only those more stable with higher functional performance.
In conclusion, this is the first multi-dimensional study on the family impact using PedsQLFIM on paediatric NMDs. We found that paediatric onset NMDs can cause significant negative family impact and affect the family functioning. Evaluation of parental stress, parental health-related quality of life and family functioning should be part of the standard of care for families with affected children with NMDs. The significantly lower family impact in the group of 5q-SMA may be attributed to both the rapid deteriorating disease course and the inaccessibility of treatment available overseas, at the time of the study. While PSS could be used in the clinic setting to screen for high risk families with affected paediatric NMD children, the use of PedsQLFIM self- reported questionnaires help to understand the affected parental HRQOL and the family impact better, so to guide the necessary support for the family.
The authors thank Mapi Research Trust for their approval to use PedsQL-2.0-FIM_AU2.0_cmn-CN_Academic-Translation version in our research. The authors also take this opportunity to thank all the participating families. Without their support and help, this study will not be possible.
Declaration of Interest
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
1. Haverman L, van Oers HA, Maurice-Stam H, Kuijpers TW, Grootenhuis MA, van Rossum MA. Health related quality of life and parental perceptions of child vulnerability among parents of a child with juvenile idiopathic arthritis: results from a web-based survey. Pediatr Rheumatol Online J 2014;7;12:34.
2. Panepinto JA, Hoffmann RG, Pajewski NM. A psychometric evaluation of the PedsQL Family Impact Module in parents of children with sickle cell disease. Health Qual Life Outcomes 2009;7:32.
3. Cousino MK, Hazen RA. Parenting stress among caregivers of children with chronic illness: A systematic review. J Pediatr Psychol 2013;38:809-28.
4. Defenderfer EK, Rybak TM, Davies WH, Berlin KS. Predicting parent health-related quality of life: evaluating conceptual models. Qual Life Res 2017;26:1405-15.
5. Epstein NB, Bishop DS, Baldwin LM. McMaster Model of Family Functioning: A view of the normal family. In: Walsh F, ed. Guilford family therapy series. Normal family processes. Guilford Press, New York, 1982;115-41.
6. Varni JW, Sherman SA, Burwinkle TM, Dickinson PE, Dixon P. The PedsQL Family Impact Module: preliminary reliability and validity. Health Qual Life Outcomes 2004;2:55.
7. Chen R, Hao Y, Feng L, Zhang Y, Huang Z. The Chinese version of the Pediatric Quality of Life InventoryPedsQLFamily Impact Module: cross-cultural adaptation and psychometric evaluation. Health Qual Life Outcomes 2011;9:16.
8. Jastrowski Mano KE, Khan KA, Ladwig RJ, Weisman SJ. The impact of pediatric chronic pain on parents' health-related quality of life and family functioning: reliability and validity of the PedsQL 4.0 Family Impact Module. J Pediatr Psychol 2011;36:517-27.
9. Cheung SK. Psychometric properties of the Chinese version of the Parental Stress Scale. Psychologia 2000;43:253-61.
10. Berry JO, Jones WH. The parental stress scale: Initial psycho-metric evidence. J Soc Pers Relat 1995;12:463-72.
11. de Kloet AJ, Lambregts SA, Berger MA, van Markus F, Wolterbeek R, Vliet Vlieland TP. Family impact of acquired brain injury in children and youth. J Dev Behav Pediatr 2015;36:342-51.
12. Bray P, Bundy AC, Ryan MM, North KN, Burns J. Health status of boys with Duchenne muscular dystrophy: a parent's perspective. J Paediatr Child Health 2011;47:557-62.
13. Liang R, Chan SHS, Ho FKW, et al. Health-related quality of life in Chinese boys with Duchenne muscular dystrophy and their families. J Child Health Care 2019;23:495-506.