Holtebekk, M. Elizabeth PT, MHSc; Berntsen, Sveinung MCEP, PhD; Rasmussen, Magnhild MD, PhD; Jahnsen, Reidun B. PT, PhD
The term “neuromuscular disorders” (NMDs) applies to a number of different diseases that are described as localized to the ventral horn cells in the spinal cord, peripheral nerves, and neuromuscular junction or muscle fibers.1,2 Most NMDs in children are genetic disorders. Debut age, motor function, and progression vary widely, often within each diagnosis. A common feature of many NMDs is the effect on walking ability. Limb-girdle and Becker muscular dystrophy and many congenital myopathies present with proximal weakness and thus reduced hip stability. Polyneuropathy/Charcot Marie Tooth disease presents in general with distal weakness, which imparts a tendency for dropfoot.1 All of these diagnoses are well-known entities in pediatric neuromuscular clinics. Limb girdle muscular dystrophies, congenital myopathies, and polyneuropathies are heterogeneous conditions. Prevalence numbers are not well known but are thought to be in the range of 1 per 2500 to 120 000. Among the Limb Girdle muscular dystrophies, type 2I is the most common form in Norway. Becker muscular dystrophy is a milder and less-frequent variant of Duchenne muscular dystrophy.2 The main symptom in subjects with NMD is reduction of strength because of reduced effective muscle mass and is due to both degeneration of muscles and inactivity.3
The importance of physical activity (PA) for children and adolescents has been emphasized during the last several years.4 McDonald3 described PA as an important factor in the prevention of health problems in adults with NMD and have stated that PA levels in childhood influence adult activity levels. Previous advice to people with NMD has been to avoid physical strain.5 Recent research has underlined that PA is beneficial for people with NMD with a potential of delaying the deterioration of physical function.5 There is a lack of evidence-based knowledge about functional level and PA level in children and adolescents with NMD. To provide recommendations on PA, the first step is to gain knowledge about the PA level of children and adolescents with NMD. The aim of this study was to determine the level of physical function and the PA level in daily life in a group of children and adolescents with NMD.
This study was conducted using a cross-sectional design that included clinical examination and activity monitoring and an activity questionnaire. Recruitment was conducted during 2008 and 2009.
Participants were recruited from the Section for Child Neurology and Section for Neurohabilitation at Oslo University Hospital and Ålesund Hospital. Oslo University Hospital is a regional hospital that recruits patients from multiple regions. The inclusion criteria were as follows: individuals with NMD aged 10 to 18 years, who were ambulant and understood how to complete a questionnaire. Ten years is considered to be the lowest age for a child to be able to give reliable answers.6 Twenty-eight children and adolescents, followed with check-ups at the hospitals, fulfilled the inclusion criteria. Seventeen (61%) agreed to participate and returned a signed consent. Four participants had polyneuropathy/Charcot Marie Tooth disease; 2 had congenital myopathy; 8 had limb-girdle 2I; 1 had Becker muscular dystrophy; and 2 had unspecified muscular disease. None of the participants used any medication. The participants varied in age and geographic location.
The level of physical function was estimated using a modified version of the Six-minute Walk Test (6MWT) with a 10-m long walkway, and the Hammersmith Motor Ability Scale (HMAS). The 6MWT is a standardized test where the participants wear a heart rate monitor and walk a marked distance (the recommended minimum distance is 15.24 m between the turns), as many times as possible for 6 minutes.7 The distance walked during the 6MWT and the mean heart rate were registered according to The American Thoracic Society's procedure.7 The 6MWT has been used as an outcome measure in many intervention studies and is considered a satisfactory way to measure endurance, proven both valid and reliable (ICC 0.94),8 including for children with NMD.9
The HMAS includes 20 items measuring motor function (Table 1).10 The test is scored on a 3-point ordinal scale with a maximum score of 40, where 0 is unable to perform, 1 is performing with minimum assistance, and 2 is performing independently. Healthy children are assumed to master all the tasks from the age of 5 years.10 The HMAS has been found valid in NMD, showing that decline in muscle strength is highly correlated with motor function (r = 0.89).10
Physical activity level was measured with a SenseWear Armband activity monitor (SWA) version PRO3 (Body Media, Inc, Pittsburgh, Pennsylvania). SWA measures acceleration along 2 axes, heat flux, skin temperature, and galvanic skin response.11 The SWA is worn over the triceps muscle on the right arm. The program used to configure data was SenseWear Professional 6.1. The participant's weight, height, gender, handedness, and smoking habits were registered according to the user manual, before the activity monitoring. The monitor estimates energy expenditure (EE) and registers time in PA at different levels, steps and sedentary time, based on the registrations from the child. In this study, only time in PA with a cut point of 3 (moderate PA) and 6 (vigorous PA) metabolic equivalents (METs) and steps were considered. The SWA has been validated during daily activities in adults and children who are healthy, as well as in individuals with disabilities.11–13 The SWA has shown high agreement in adults with 9% underestimation of EE and 2.9% underestimation of moderate to vigorous PA.14 However, studies in children show diverse results, as bodyweight may influence the results, but the deviation between SWA and indirect room calorimetry was less for low- and moderate-intensity activities.11,15
The questionnaire used in this study was based on a questionnaire from the Personal and Environment Associations with Children's Health (PEACH) project at the University of Bristol and modified and translated to Norwegian.16,17 The questionnaire was originally used to calculate PA level in a study by Anderssen and Solberg.17 The questionnaire consists of 24 questions with multiple-choice answers about activities across 1 week, divided into PAs at school and physical and sedentary activities after school and during weekends. The participants registered the duration and level of exhaustion during different activities.
The study was approved by The Regional Committee for Research Ethics in Helse Soer. The 28 families were sent a written invitation explaining the aim of the study and describing the procedure to be conducted. The parents signed a consent form for participants younger than 16 years, and in addition, these children gave their oral consent. The participants who were 16 years and older signed their own consent forms.
The 1-hour long sessions were carried out in a room at the hospital approximately 10 m by 12 m, without any disturbances, conducted by the same person with 1 parent present. The participants wore light clothes and shoes or were barefoot at their own request. Weight was measured in kilograms using an electronic scale (Wilfa PS-1, China), and height was measured in centimeters without shoes using a wall-assembled stadiometer. Next, participants completed the questionnaire in approximately 15 minutes. Fourteen participants received help from parents to complete the questionnaire.
In this study, the course of the 6MWT was 10 m between the turning points. To make the distance covered as accurate as possible, the cones were placed ahead of the turning point, to have the participants turn as close to 10 m as possible. The tester observed the participant from a point beside the course. The participants were instructed to walk as fast as possible for 6 minutes and informed that the distance would be measured.7 They were given information during the test about the length of time used and received encouragement according to The American Thoracic Society's standard phrases.7
The participants were told to wear the SWA 4 days, from Sunday morning until Thursday morning during an ordinary, specified week.6 They were instructed to wear the monitor day and night and remove it only when showering or swimming. For inclusion of data from the SWA in this study, 11 waking hours per day and 2 days with complete data were required.18 For SWA data obtained Sunday, the term “weekend” is used in this study.
Because of the small number of participants and skewed distribution, results are presented as median values with interquartile range (IQR). Despite the small study group, data were examined by gender and weight status,19 because these personal characteristics influence PA levels. Data were analyzed using descriptive statistics and a Spearman rho correlation analysis. Body mass index percentiles were calculated using the Centers for Disease Control and Prevention's BMI Percentile Calculator for Child and Teen.20 Because of the small sample size and skewed distribution, z scores were not calculated. Data were analyzed using SPSS, version 18.0. An α value less than 0.05 was considered statistically significant.
Sample characteristics including age, gender, height, weight, and BMI percentile are presented in Table 2, showing a similar number of boys and girls, although the girls' mean age was lower than the boys' mean age. The participants presented a wide range of BMI percentiles. Two participants were classified as underweight. Three participants were classified as overweight and 3 as obese. Four of the overweight and obese participants were in the oldest group and 2 were in the youngest group.
The median HMAS scores are presented in Table 3. The range was wide with the median close to the maximum score. Six participants had maximum score on the HMAS.
The median 6MWT distance was less than 500 m with a nonsignificant increased range in the boys compared with the girls (Table 3). A nonsignificant difference in the 6MWT distance between the participants with overweight and obesity (N = 5; median, 485; IQR, 117) and the other participants (N = 10; median, 509; IQR, 235) was observed. The median heart rate during the 6MWT was 116 beats per minute (N = 16; min-max, 93–157). Thirteen participants had an average heart rate equal to or less than 132 beats per minute during 6MWT. Heart rate was not measured for 1 participant. The 6MWT distance was not associated with height (r = 0.11; P > .05), mean heart rate (r = 0.13; P > .05), or age (r = 0.11; P > .05). There was no difference in 6MWT distance between the genders. The HMAS score was positively correlated with the 6MWT distance (r = 0.69; P < .01).
Time in moderate-intensity PA (3–6 MET [MPA]) and steps per weekend/weekday measured by SWA are presented in Table 4. None of the participants registered time in vigorous-intensity PA (6–9 MET). Two participants did not have data for the weekend that fulfilled the requirements. One participant fulfilled the requirements for only 2 of 3 weekdays. Median hours the participants wore the SWA per weekend/weekday were 13.7/23.4 (N = 17; IQR 4.3/2.3). Total median hours they wore the SWA was 91 (N = 17; IQR 23.8), and the median number of days was 4 (N = 17; IQR 0). None of the participants smoked, and all the participants were right-handed. Correlation between the 6MWT and steps was moderate and significant (r = 0.67 P < .01), and correlation between the 6MWT and MPA was not significant (r = 0.34; P > .05).
Data from the questionnaire (Table 5) showed that 11 participants (64%) were driven to schools or used public transportation whereas 6 (35%) used a bicycle or walked. Five of the 6 participants who walked or bicycled to school had less than a 15-minute commute. Three participants (18%) were physically active during school breaks. In their leisure time, 9 participants exercised “regularly,” and 6 “sometimes.” The other 2 participants had considered exercising but had not yet started. Six participants did no exercise, playing, or sports during weekends.
In this study, most of the participants had a lower score on the HMAS in the items of getting up to stand, jumping on 1 leg, and standing on heels, confirming the study by Scott et al,10 which concluded that the HMAS is closely related to muscle strength. Decreased muscle strength in the lower limbs is also likely to influence walking, and thus the distance on the 6MWT as shown by a moderate correlation between the HMAS score and the 6MWT distance. Even those with high HMAS scores, as the HMAS showed a ceiling effect in 6 participants, had a wide range of 6MWT distance. The 6MWT is consequently more suitable for discriminating between the participants with less impairment. The HMAS measures standardized functional capacity,10 whereas the 6MWT is considered to measure endurance and exercise tolerance.8
The participants in this study walked significantly shorter 6MWT distances (29%) than a group of 369 children and adolescents who were white, healthy, and age matched.21 Because of lack of access to a quiet longer corridor, this study used a course of 10 m, which is shorter than in the original test7 and the test of Geiger et al.21 However, most of the participants performed the 6MWT at a pace where they could master the turns around the cones and still keep a steady pace. Even the participants with a higher speed did not appear to slow down at the turns. However, the short track may have influenced the significant difference between the distances covered by the 2 groups.
The participants in this study represent various diagnoses. Merging small diagnostic groups may influence the results, but it is justified when functional level is being studied and walking ability is an inclusion criterion.22 The results showed a variation in physical function within the different diagnoses rather than between them. One participant could barely finish the 6MWT, whereas others with the same diagnosis had no difficulties.
The 6MWT distance depends on the participants' motivation and physical capacity. Although there was a wide range, most of the participants showed a heart rate well below the average 140 beat heart rate of peers who are healthy.21 The moderate pace might be due to motivational factors but could be a result of muscle weakness due to the disease and also overweight.1,2 Progression of the disease leads to reduced muscle strength and thus a decline in motor function that also will influence exercise tolerance as measured by the 6MWT.8 Four participants in the oldest group were overweight, and muscle weakness combined with increased weight makes PA a greater challenge, and a possible explanation of the shorter median 6MWT distance in the oldest group (Table 3). Motivation is hard to evaluate and was not investigated in this study.
Median time in MPA for the participants measured with SWA activity monitor was more than the recommended 60 minutes per day for children and adolescents,4 but none of the participants had any PA at a vigorous level, which is essential to preserve or increase fitness in healthy individuals.23 The participants' physical capacity, and thus their distance on 6MWT, may be influenced by earlier advice telling them to avoid participation in physical activities with increased intensity.5 Strong et al4 reported that a level of 5 to 8 METs is necessary to derive health benefits in children and adolescents who are healthy. Children and adolescents with NMD also probably can benefit from spending more time in PA, but this study does not tell to what extent they can benefit from increasing the intensity of their activities.
The comparison between the current participants and the results of Berntsen et al13 of 79 adolescents who were healthy using the same activity monitor indicated that the group with NMD had 69% less activity time on a weekend and 48% less activity time on the weekdays (Table 4). In addition, the data of Berntsen et al included both moderate and vigorous activities.
Results of studies of children and adolescents who are healthy show lower levels of PA on weekends compared with weekdays,13,19 but the difference between weekend and weekdays was greater for the participants in this study than for children and adolescents who are healthy.13 Six of the participants (35%) registered no training, play, or activity during weekends in the questionnaire, and 1 participant gave the answer “very seldom” to the same question.4 One explanation, concerning the low level of activity during weekends, may be that some of the participants use a lot of energy to get through all the activities at school during the week, and thus use the weekends for recovery after a week at school. The need for rest is consistent with the shorter distance of 6MWT, showing less exercise tolerance for the participants than for the peers who are healthy.8,21 A moderate and significant correlation was found between the 6MWT and steps, but not a significant correlation between the 6MWT and MPA. This may reflect that the participants walk a lot at a slow pace. If optimal training could increase their physical function, they might be able to keep up a generally higher level of activity in daily life.
The health authorities in Canada recommend 12 000 steps per day for children and adolescents. The number of steps during the weekend of the participants in this study was far below this recommendation. This is consistent with the shorter time in MPA compared with the time in moderate to vigorous PA of the adolescents in Berntsen et al's13 study who were healthy.
Two validation studies on the SWA activity monitor in children produced different results.11,15 Energy expenditure and resting metabolic rate in children and adolescents differ from adult values and therefore MET values have limitations.4 Energy expenditure and time in PA measured by activity monitors can also vary between monitors.13 In the present study, we only compared time in activity between the participants and peers who were healthy and used the same monitor.13 This is likely to have reduced the difference in estimation between the 2 groups. Even when considering the uncertainty of the SWA data, the difference in time in PA between the study participants and the peers who are healthy cannot be eliminated.
Activity monitors are considered more reliable than questionnaires when measuring activity, due to recall bias, especially in children.6 The data from the questionnaire were, therefore, used only as background information and a supplement to the data measured with the SWA. The SWA is easy to use and does not inhibit the child from being active, which is important when measuring activity in children and adolescents.6 The acceleration along 2 axes and different physiological parameters are also considered strengths when measuring PA.
A limitation of the study is the small sample, and that only 61% of those fulfilling the inclusion criteria volunteered. However, the participants represented a diversity of age and functional levels and came from throughout the country. Still, the results cannot be generalized to a larger group.
CONCLUSION AND FUTURE PERSPECTIVES
The aim of the study was to gain knowledge about PA level and level of function in a group of children and adolescents with NMD. The results of this study show that the group with NMD had substantially lower level of physical function than peers who are healthy, as measured by the 6MWT and HMAS, and PA level of the participants indicated a lower level of activity compared with healthy children and public recommendations on the number of steps per day for children. Since neuromuscular diseases are rare and thus the number of children and adolescents with NMD is low, multicenter studies are recommended to provide sufficient statistical power.
The lower level of PA indicates that it is necessary to increase PA in children and adolescents with NMD. The great variations in severity and functional level of people with NMD make it a future challenge to organize PA in an individually tailored and motivational way for children and adolescents with NMD who are inactive to promote health and function for this group of patients. This calls for studies on the effect of training for different diagnoses and functional levels and exploration of the optimal level of training intensity for each of them.
The authors thank the Norwegian Resource Centre for Inborn Muscular Diseases for providing the project with activity monitors and a special thanks to Inger Lund Petersen, who gave us the inspiration to start the project. We also thank Sara Glent for help with grammar and spelling. Finally we thank the children and adolescents and their families who took part in the project.
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adolescent; ambulation; child; neuromuscular disorders; physical activity; severity of illness index
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