Exploring caregivers' attitudes and beliefs about nutrition and weight management for young people with Duchenne muscular dystrophy

Obesity disproportionately affects children and adolescents with Duchenne muscular dystrophy (DMD) and with adverse consequences for disease progression. This study aims to: explore barriers, enablers, attitudes, and beliefs about nutrition and weight management; and to obtain caregiver preferences for the design of a weight management program for DMD.


| INTRODUCTION
Obesity affects up to 50% of children with DMD. 1,2There is an increasing body of evidence that a higher body weight can worsen health and disease outcomes in individuals with DMD.[9] There are significant challenges in achieving and maintaining optimal weight status in the context of DMD. 10 Amongst all populations, the etiology of obesity is multifactorial relating to environment, genetic predisposition, biological, economic, and psychosocial factors. 11These factors are accentuated in individuals with DMD by the degree of physical disability and limitations on physical activity and reduced total energy expenditure, 12 and potentially further reduced resting energy expenditure due to relative reduction in lean mass with disease progression. 9Weight gain is compounded by long-term glucocorticosteroids ("steroids"), current gold-standard medical management, which are known to increase appetite and body weight. 13,14In two prior investigations of dietary intake of individuals with DMD, higher total energy intakes compared to estimated requirements and displacement of core food groups with discretionary (non-core) foods were observed. 15,16Qualitative research has identified challenges associated with weight management such as competing health care priorities, the complexities of the high level of care needs that comes with DMD, and balancing dietary restriction and the enjoyment associated with food. 17,18This study aimed to extend existing knowledge by exploring specific barriers and enablers that influence nutritionand weight-related behaviors as well as attitudes and beliefs about nutrition and weight management in the home environment.In tandem, this study aimed to collate caregivers' preferences for the design of a weight management program for young people with DMD.In doing so, we aimed to further knowledge about what dietary strategies may be useful in the rehabilitative management of young people with DMD with a high body weight living at home with their caregivers.nience sample of caregivers was recruited if they had at least one child diagnosed with DMD who attended one of the four neuromuscular clinic sites, were primarily responsible for the provision of food in their household, could read and understand English and, were willing to provide informed consent.There were no age limits for the young person with DMD, however as participants were recruited through a pediatric neuromuscular clinic, they were likely 18 years or younger.Participants were excluded if they did not complete the survey in full, as it was assumed they were opting to withdraw from the study.
The RCH Research Ethics and Governance Office approved all study procedures (HREC/51070/RCHM-2019).Site-specific governance authorization was obtained from each site.

| Survey development
The survey consisted of two parts which addressed each of the study aims (see Table S1 and Supplementary Methods A for the full survey).
The first part explored caregivers' perspectives on barriers and enablers to, and attitudes and beliefs about nutrition and weight management in young people with DMD.The second part asked caregivers' preferences on the design of a weight management program for DMD.
The survey was developed by a multidisciplinary team of neuromuscular and nutrition researchers and clinicians including: dietitians, occupational therapists, physiotherapists, specialist nurses, and neurologists.
Demographic and clinical characteristics were first collected including steroid treatment, self-reported height and weight and distance able to walk or use of wheelchair.Self-reported height and weight data were converted to body mass index (BMI) and BMI z-score using Centers for Disease Control and Prevention growth reference data. 19 identify factors influencing dietary intake and weight, survey questions were informed by the Theoretical Domains Framework (TDF, Table S1). 20The TDF combines 33 theories of behavior and behavior change into 14 domains and aims to identify the cognitive, affective, social, and environmental influences on behavior. 21Some questions regarding the home food environment were used or adapted, with the author's permission, from a survey previously published. 22regivers were then asked to imagine their family was going to take part in a healthy lifestyle program and were asked to provide their preferences on various aspects of its design.Caregivers were provided an opportunity to leave comments at the end of the first and second part of the survey and record their email address to receive more information about the program in the future.
Both sections of the survey were piloted amongst a multidisciplinary research team and with a convenience sample of caregivers who did not have a son with DMD recruited from personal and professional networks.This was to avoid unnecessary burden on families who have a son with DMD and to optimize eligible participants for the final survey.The purpose of pilot testing was to ensure face validity, survey flow, readability, comprehension of questions and identify the time taken to complete the survey.Content validity was tested by ensuring questions and responses aligned with potential nutritionand weight-related factors that are relevant to DMD.

| Survey procedures
The survey was distributed using Qualtrics survey platform (Qualtrics, Provo, UT, USA.Available from: https://www.qualtrics.com).A paper version of the survey was also available at participants' request which were entered manually into Qualtrics.Participants were identified from clinic lists at each site and their caregivers were approached to complete the survey during routine clinic visits, via email invitation, and through advertisement in clinic newsletters.Caregivers were able to complete the survey in their own time on their own device.After viewing the information statement and consenting, caregivers proceeded to two screening questions and the survey.

| Data analysis
All data were analyzed using SPSS statistical software version 26.0 (IBM, Armonk, NY).Data were presented graphically using either SPSS or Excel (Microsoft, Redmond, WA).All data were analyzed descriptively.Nominal data are reported as frequencies and continuous data as median with interquartile range (IQR) or mean and standard deviation (SD) depending on the normality of the distribution.For survey questions where caregivers were asked to rank their preferred option, proportions of participants who selected the response as either their first, second, or third preference are reported.All rating scales were ranging from 0 (not easy/not difficult/not a problem/not a priority) to 5 (extremely easy/extremely difficult/big problem/highest priority).
Raw text comments were organized thematically and classified according to TDF domains or physiological factors related to nutrition and weight.Comments were categorized independently by two researchers and consensus was reached by discussion.

| Survey participant characteristics
The eligible number of families across the four neuromuscular clinics when the survey was distributed was approximately 220.There were 79 survey respondents who commenced the survey.Of these, two were deemed ineligible based on screening questions and 24 did not complete the survey in full, were assumed to be opting to withdraw and were consequently excluded.Data were analyzed for the remaining 53 caregivers of 59 young people with DMD.The demographics of the households and young people with DMD are described in Table 1.Most participants were from Victoria.Most young people with DMD were treated with steroids and autism spectrum disorder was the most common neurodevelopmental comorbidity.Across families, 37 (70%) accessed a dietitian through a neuromuscular clinic, 14 (26%) did not access a dietitian and 2 (4%) accessed a dietitian externally to the neuromuscular clinic.

| Physiological factors related to nutrition and weight
Most participants were reported to be above a healthy weight; from both self-reported BMI z-score and caregivers' perception of their son's BMI status (Table 2).Of those who perceived their son to be above a healthy weight, 27 (96%) caregivers reported the weight gain was related to taking steroids.Whilst 40% of both caregivers and boys with DMD intended to lose weight, half of respondents reported managing weight was not easy.
Of young people with DMD, 20 (34%) were reported to be fussy/ picky eaters.Most caregivers reported that their son(s) avoid/choose certain foods due to the texture, smell, or taste at least some (n = 29, 49%) or most or all (n = 7, 12%) of the time.

| Knowledge
From a list of foods, 38 (72%) caregivers were able to identify which belonged to the five core food groups (fruit, vegetables, dairy, meat/ alternatives, breads, and cereals) according to the Australian Guide to Healthy Eating. 23From a second list of foods, 24 (45%) were able to correctly identify discretionary (non-core) foods.

| Skills and beliefs about capabilities
Caregivers reported high confidence in skills in both choosing and preparing/cooking healthy meals (Table 3).Yet, most caregivers wanted to improve skills such as preparing healthy snacks and buying and cooking healthy foods on a budget.The most common barriers to improving these skills were time, cost, and stress.

| Beliefs about consequences
Almost all (96%) caregivers thought healthy eating was highly beneficial (ratings of 4 or 5) to their son with DMD.Weight gain was the most frequently selected consequence for not following a healthy eating pattern (Figure 1).Self-consciousness and worry were the most frequently reported impacts of being above a healthy weight for children with DMD and their caregivers, respectively (Table 2).

| Reinforcement and goals
Healthy eating was a high priority amongst caregivers (median rating, IQR 4.1, 3.4-5.0).Most caregivers reported they considered the healthiness of food either most or all the time for their son(s) with DMD (87%) and family (81%).Eating a variety from food groups and reducing processed foods were the most common nutrition goals (Table S2).Avoiding weight gain was the most common reason healthiness was considered (91%).Besides healthiness, taste, family food preferences, the enjoyment their son gets from food, and food variety were most considered by caregivers.

| Environmental context and resources
Using an open-ended response, caregivers reported the biggest barriers to providing healthy foods to their family were: time constraints and fussiness or food preferences of either their son(s) with DMD or other family members related to taste, textures, or smells (Table S3).
T A B L E 1 Family and demographic characteristics.Regarding the mealtime environment in their household, eating family meals at a table or bench were common but screens were frequently used during meals (Table 4).

| Social influences
Most caregivers (n = 34, 58%) reported their son eats more "sometimes" No respondents reported more sometimes foods were eaten when alone.

| Emotion and behavioral regulation
When asked to rate certain situations related to eating, emotions, and appetite, caregivers rated an increased appetite because of medication as the most problematic (Figure 2) .
Using an open-ended response, caregivers were asked to record emotions (if any) that made their son want to eat.Eight (14%) caregivers recorded emotions such as sadness, depression, anger, boredom, and enjoyment (Table S4).

| Caregiver consultation on a healthy lifestyle program
Regarding the design of a weight management program for DMD, there was a clear preference for the program to be individualized, Preparing and cooking healthy meals 16 (39)   Reading food labels 8 (20)   Preparing and cooking vegetables 4 (10)   Finding healthy foods in the supermarket/shops 2 (5)   Learning which foods are healthy 1 Barriers to improving skills (n = 41) Finding time to learn them 21 (51) The cost of healthy foods 16 (39)   Being stressed about other things in my life 13 (32)   Not knowing where or how to learn them 6 (15)   Selective food preferences of son with DMD or other children (recorded as other)

(5)
T A B L E 2 Information about BMI status, impact and intentions.Ease of achieving and maintaining a healthy weight (scale ranged from 0 not easy at all to 5 very easy, n = 59), median (IQR) 2.0 (0.9, 3.1) with a whole-lifestyle focus and for a duration of 6 weeks (Table 5).
Most families selected face-to-face as one of the top three preferred modes of delivery, and approximately half of participants also selected remote delivery modes including phone, video call, or social media.Whilst weekly sessions were most frequently preferred by respondents, there was also similar support for both fortnightly and monthly sessions; and middle of the day and evening appeared to be the preferred time of day.Caregivers identified that they would like email and online support from a dietitian during the program.

| Additional comments regarding nutrition and weight management
Thirteen caregivers recorded additional comments at the end of the survey (Table S5).Five caregivers commented on physiological factors such as increased appetite that contribute to weight gain and the difficulty in managing weight: Our family eats meals at a table/bench 5 ( Our son eats meals in the car 50 ( Our son eats something different from other family members 40 Our son eats meals sitting in front of a screen (e.g., a TV, phone or tablet) 30 (57) 18 Someone in our household cooks the main meal 2 (4) 5 ( 9) 46 (87 The TV is on in the background during the main meal 22 Meals occur later than expected or just before bed time 44 (83) 9 (17) 0 My son has a big appetite and is continually telling us that he is hungry despite adequate amounts of nutritious/very healthy food provided 5 meals a day.He has not yet started steroid therapy.We find it very difficult/ stressful/tiring to continuously have to regulate/monitor his intake however we do as when we have previously relaxed a bit on food intake quantities (despite the food still being very healthy, low GI/carb), he has gained too much weight with little height growth.
Seven comments were recorded related to nutrition knowledge.
Caregivers identified a need for specific nutrition information and further input from health professionals regarding nutrition and weight management advice: Not enough information is provided in clinic to keep your child in a healthy weight range.How many calories he should be eating per day or even suggestions of foods that will keep him feeling full for longer.We need to research and work it out ourselves.

| DISCUSSION
In this survey of caregivers, factors influencing nutrition and weight in young people with DMD included fussy eating, avoidance of foods due to their taste, texture, or smell, time constraints to prepare meals, and an increased appetite because of steroids.Preventing too much weight gain was the main factor that influenced food choices for families and healthy eating was a high priority.A deficit in caregivers' general nutrition knowledge was identified and a lack of nutrition information provided in clinical settings emerged as an issue.
This survey identified that weight is an important issue and can have an impact on the psychosocial wellbeing of young people with DMD and their caregivers.Considering the topic of weight may be emotive for families, 17 discussions about weight management need to be delivered by appropriately trained clinicians, sensitively, and without stigma.Weight stigma may take the form of language and bias but also access to appropriate health care resources such as equipment (e.g., appropriately sized wheelchairs), furniture (e.g., bariatric chairs), and services. 24dietitians' role should include addressing the gap in general nutrition knowledge as well as specialized nutrition principals for DMD including: foods and nutrients that promote satiety, reducing energy density, strategies to recognize internal hunger and satiety cues and nutrition supplements.We identified that restrictive eating in DMD is a major barrier to healthy eating, which may be contributed to by neurodevelopmental disabilities or related traits that are common in DMD. 25 Ideally, weight management would be multidisciplinary, but health professionals have reported a lack of confidence in addressing weight in DMD. 26 There may also be a lack of access to appropriate and sustainable clinical resources and clinicians with a suitable level of competency and understanding of DMD (e.g., psychologists 27 ) in addition to weight management.There are also many issues to discuss during routine neuromuscular clinic appointments, and some health care professionals feel apprehensive discussing the topic of weight. 18Health services may need to consider whether it is more appropriate to offer weight management care for DMD within or external to multidisciplinary neuromuscular clinics to discuss such sensitive topics.
This study and prior research have observed that caregivers' food provision may be influenced by their son's DMD diagnosis.In our study, caregivers reported moderate difficulty in denying their son's requests for food because of his DMD.Prior qualitative research has identified that parents feel guilty for restricting their son's food intake and may prioritize their son's perceived happiness over weight management strategies. 18Parents' food provision may be responsive to their son's level of functioning and some parents do not want to deny Problems and difficulties related to food, emotions, and appetite.
enjoyable food experiences in the light of their son's life-limiting condition. 17Competing health priorities has also been recognized as a key challenge in managing weight in DMD. 18Mutual goal setting between clinicians and families is important to balance parental guilt, the enjoyment food brings, competing priorities, and weight management strategies.
Environmental factors that influence healthy eating and weight management were identified in this study.Family meals are associated with a higher consumption of nutrient-rich foods, lower intake of soft drink, reduced likelihood of the child being overweight and improved psychosocial wellbeing. 28Positively, in our sample, most families ate meals together at a table or bench.However, caregivers reported frequent screen use during mealtimes which can be associated with a higher consumption of energy-dense nutrient-poor foods and makes it difficult for young people to recognize satiety signals.Tailored weight management programs for DMD and children with physical disabilities are scant. 30Caregivers indicated a preference for a holistic lifestyle-focused, short (6 week), face-to-face, and individualized weight management program.This predominantly aligns with the consensus that weight management interventions should be multi-component, family-focussed and include regular follow-up [31][32][33][34][35][36][37][38][39][40][41] ; however, longer interventions of at least 6 months are preferred. 35lehealth or phone sessions and online and digital resources were ranked as lower preferences by participants; however, as this survey was delivered prior to the COVID-19 pandemic, and thus prior to an increase in virtual services, it would be important to re-consult on this preference.Online platforms may be useful to achieve greater reach and sustainability for nutrition and weight management care.There was a gap in knowledge about discretionary foods, and consequently caregiver attitudes and preferences to this being included the program were low (17%).While program content needs to include consumer preferences, addressing knowledge gaps is also important.Quality of life and weight were preferred outcome measures.The impact of weight and weight management strategies on quality of life has been identified as a key issue for caregivers and individuals with DMD. 18,42mitations of the study included availability only in English and failure to obtain young peoples' perspectives directly.Also, the sample size did not allow for stratification according to age, BMI or ambulatory status, which may influence dietary intake and weight.Future research should consider exploring the perspectives of young people with DMD, to gain further insight into factors such as appetite, emotions, and food preferences and the influence of mobility.There is also a potential of response bias in this study; for example, caregivers may have reported nutrition to be a high priority due to an unconscious influence from researchers.Caregivers who completed the survey may also had an interested in nutrition that influenced their responses.

| CONCLUSION
This study explored the barriers and enablers to and attitudes and beliefs about nutrition and weight management as reported by caregivers of young people with DMD.Weight management appears to be a pertinent issue for families but with considerable perceived bar-

2 | METHODS 2 . 1 |
Study design, setting, and participants This was a cross-sectional mixed methods study utilizing a survey of caregivers of young people with DMD.Participants were recruited from the four major Australian pediatric neuromuscular clinics: Royal Children's Hospital (RCH), Melbourne, Victoria; Children's Hospital at Westmead and Sydney Children's Hospital Randwick, New South Wales; and Queensland Children's Hospital, Queensland.The survey was administered between June 2019 and March 2021.A conve- discretionary or non-core) foods depending on what social situation they are in.The most common social situations were family celebrations (n = 25, 42%), parties (n = 19, 32%), and when eating out (n = 17, 29%).
BMI status calculated from reported height and weight (n = 59),

T A B L E 4
Mealtime environment (n = 53).Rarely or never (1 time or less per week) n (N%) Some of the time (2-4 days per week) n (N%) Most or all of the time (5-7 days per week) n (N%) How often do the following situations occur during meal times in your household?
riers including food avoidance due to sensory preferences, time pressures felt by families, and a lack of practical nutrition knowledge delivered by health professionals.Enablers include nutrition being a high priority for families, caregivers having high confidence in their skills to prepare healthy foods and a sound understanding of the consequences (positive or negative) of healthy eating.Caregivers preferred an individualized weight management program delivered over 6 weeks including topics such as healthy lunchboxes, managing appetite, and mindfulness.This has informed the design of a feasibility and acceptability study for a lifestyle weight management program in DMD: Supporting Nutrition and Optimizing Wellbeing Program (SNOW-P) for DMD.
Caregivers' skills and beliefs about capabilities.

Table 6
summarizes caregivers' preferences for program topics, resources and outcomes.The three most frequently selected nutrition topics were preparing and cooking healthy meals and snacks, managing appetite, and healthy lunchboxes.Caregivers selected other topics