Changes in body composition and safety of exercise for individuals with severe cerebral palsy: single-group pre-post observational study

Abstract

[Purpose] This study was a pilot investigation. The purpose is to examine short-term longitudinal changes in limb skeletal muscle mass and water content in participants with severe cerebral palsy and examine the safety of an exercise intervention in participants, as a single-group pre-post observational study. [Participants and Methods] The participants were 11 individuals. The survey period was set to 6 months. Body composition was assessed using the skeletal muscle mass index and extracellular water/total body water ratio. The first 3 months served as a non-intervention period, followed by a 3-month intervention period involving passive stretching and postural changes. [Results] extracellular water/total body water levels in the trunk and the right lower limb significantly increased at 3 and 6 months compared with the values at the start (p<0.05) (ηp²=0.58 and 0.49, respectively). The skeletal muscle mass index did not show any significant changes and remained very low. Within the 6-month observation period, edema progression was detectable, but measurable declines in muscle mass were not, suggesting that longer follow-up periods are likely needed to capture longitudinal changes in skeletal muscle in severe cerebral palsy. [Conclusion] The exercise did not show any significant impacts. Physical therapists should continue exploring effective way to improve the status of their body composition.

INTRODUCTION

Individuals with cerebral palsy (CP) have a group of disorders that affect the development of movement and posture, causing limitations to their activity that are attributed to nonprogressive disturbances in the developing fetal or infant brain¹⁾. Many children, adolescents, and adults with CP have reduced cardiorespiratory endurance, muscle strength, and habitual participation in physical activity (PA). Reduced cardiorespiratory endurance and muscular weakness each pose a significant risk for negative health outcomes and early, cardiovascular and all-cause mortality²⁾. PA, its promotion, and the avoidance of sedentary behavior, play important roles in health improvement and the prevention of lifestyle-related diseases^{2, 3)}.

Although it has been reported there are benefits to participation in PA for individuals with CP, the benefits of various approaches for initiating and administering a progressive activity program for individuals with CP, classified at the Gross Motor Function Classification System (GMFCS)⁴⁾ level IV or V, have not been systematically evaluated²⁾. Passive movement in individuals at GMFCS level V must be approached cautiously because these individuals are at increased risk for hip displacement, fragility fractures, pain, and respiratory compromise during handling^5,6,7). Therefore, evaluating the safety of therapist-led passive exercise is clinically important.

Individuals with severe CP typically demonstrate low muscle mass due to lifelong neuromuscular impairments. These include reduced voluntary muscle activation, altered muscle architecture, chronic non-weight-bearing, spasticity-related muscle changes, and decreased opportunities for functional movement. Prior literature shows that muscle underdevelopment in CP begins early in life and persists across the lifespan, independent of aging mechanisms⁸⁾. Therefore, the low muscle mass observed in individuals classified at GMFCS level V primarily reflects these CP-specific factors rather than age-related decline. It may be useful to measure body composition, such as muscle quality, to help develop an activity program suitable for people with CP of GMFCS level V because these measures may reflect chronic inactivity, altered muscle composition, and potential vulnerability to secondary health complications. Recently, the segmental extracellular water (ECW)/intracellular water (ICW) ratio, which is measured using bioelectrical impedance spectroscopy (BIS), has attracted attention as a measure of muscle quality⁹⁾. From the above, it can be hypothesized that individuals with severe cerebral palsy tend to experience progressive muscle loss and worsening fluid imbalance.

This study was a pilot investigation examining the short-term longitudinal changes in limb skeletal muscle mass and water content in participants with severe CP and examined the safety of an exercise intervention in participants

PARTICIPANTS AND METHODS

This is a single-group pre-post observational study of the factors related to changes in body composition and the safety of exercise intervention.

Those who registered with the Suita City Disability Support Center and were receiving rehabilitation support as of December 1, 2018 were 22. All of them were the participants. They had been diagnosed with cerebral palsy. They presented with severe motor and intellectual disabilities and displayed impaired communication abilities. Of the 22 eligible individuals, 11 were included in the analysis. The remaining 11 individuals were excluded because they were unable to complete the measurements due to absence on the measurement day or inability to perform the measurements appropriately (Fig. 1). Since all cases were included, missing data were not in the analysis. The characteristics of the 11 participants are presented in Table 1. An opt-out method of obtaining consent was used in this study. The participants’ family was informed that they were free to opt-out of participation in the study by completing an opt-out form. As this study involved human participants, it was performed under an approved protocol following the Ethics Review Committee of Kochi Professional University of Rehabilitation (R2-3), the 1964 Helsinki Declaration, and later amendments or comparable ethical standards.

Fig. 1.

Flowchart of the study.

Table 1. Basic information of participants.

Variable	Values
Sex (female/male)a	7/4
Age (years)b	39.7 ± 11.3
Height (cm)b	138.8 ± 14.0
Weight (kg)b	32.2 ± 5.2
Body mass index (kg/m2)b	16.9 ± 2.5
Cerebral palsy (diagnosis) a	11
GMFCS (Level) a	V
Type of CP (n) a
Spastic quadriplegia	9
Dyskinetic	2

^a: Number, ^b: Mean ± standard deviation. GMFCS: gross motor function classification system; CP: cerebral palsy.

The survey period was set to 6 months. The first 3 months comprised the non-intervention period, and the latter 3 months comprised the exercise intervention period.

The item of primary outcome was body composition. And the items of secondary outcomes were percutaneous arterial oxygen saturation (SpO₂), muscle tone, pulse rate, and adverse events.

For body composition, the skeletal muscle mass index (SMI) and ECW/total body water (ECW/TBW) ratio were measured using a body composition analyzer, the InBody S10 (InBody Co., Ltd., Tokyo, Japan). To identify changes in body characteristics, SMI and ECW/TBW were measured three times: at the start of the survey, 3 months from the start, and 6 months.

Muscle tone was evaluated, using the modified Ashworth scale¹⁰⁾, for the left and right elbow flexors, palmer flexor muscles, knee flexor muscles, and ankle flexor muscles. These were measured before the start of exercise on the first day of the intervention and before exercise at the end of the intervention. The sum of the first day of intervention and the end of intervention were compared.

The intensity of exercise performed during the intervention period was measured using the Karvonen formula [(maximal HR − resting HR) × training% + resting HR].

The therapist-led exercise intervention took place during the latter 3 months of the 6-month study period. The exercise parameters (20-minute passive sessions, low frequency, and content consisting of stretching and positional changes) reflected routine clinical practice at our facility for individuals at GMFCS level V. These individuals are unable to perform voluntary exercise, and passive movement routines of similar intensity and duration are commonly used to maintain joint mobility, prevent contractures, and facilitate caregiving. No established guidelines exist for exercise prescription in this population; therefore, the parameters used in this study were based on current clinical norms rather than evidence-based dose-response models.

The safety of the therapist-led passive exercise was assessed by pulse rate, SpO₂, muscle tone, and adverse events. Pulse rate and SpO₂ were measured before and after exercise on the first day of exercise and before and after exercise at the end of the intervention.

Adverse events included fractures that occurred during the exercise intervention, joint trauma, and falls from the bed.

For the statistical analysis, analysis of variance by repeated measurements was used for the SMI and ECW/TBW. Wilcoxon signed-rank test was used for pulse rate, SpO₂, and muscle tone. Statistical analyses were performed using SPSS version 22.0 (IBM, Tokyo, Japan). The level of significance was set at p<0.05. The effect sizes of this study were measured using partial eta-squared (η_p²). An η_p² value between 0.02 and 0.12 is considered small, between 0.13 and 0.25 is medium, and greater than 0.26 is large¹¹⁾.

RESULTS

Table 2 shows the changes in body composition and the statistical results of ECW/TBW and the SMI. During the 6-month survey, ECW/TBW levels in the trunk and the right lower limb significantly increased at 3 and 6 months compared with the values at the start (p<0.05). Although the SMI did not show any significant changes throughout the study period, it was found to remain very low. There was no significant difference in pulse rate and SpO₂ before and after exercise on the first day of exercise and before and after exercise at the end of the intervention.

Table 2. Statistical results of ECW/TBW and SMI.

Item	Start	3 months	6 months	Effect sizes
ECW/TBW_RA	0.386 ± 0.007	0.387 ± 0.008	0.388 ± 0.010	1.00
ECW/TBW_LA	0.384 ± 0.009	0.387 ± 0.008	0.383 ± 0.010	0.09
ECW/TBW_TR	0.406 ± 0.009	0.413 ± 0.013*a	0.411 ± 0.009*b	0.58
ECW/TBW_RL	0.412 ± 0.010	0.417 ± 0.009*a	0.419 ± 0.009*b	0.49
ECW/TBW_LL	0.406 ± 0.011	0.409 ± 0.011	0.409 ± 0.011	0.19
SMI (kg/m2)	2.976 ± 1.236	2.751 ± 0.998	2.8499 ± 1.073	0.20

Mean ± standard deviation. *p<0.05. a: Start vs. 3 months. b: Start vs. 6 months.

ECW: extracellular water; TBW: total body water; RA: right arm (upper limb); LA: left arm (upper limb); TR: trunk; RL: right lower limb; LL: left lower limb; SMI: skeletal muscle mass index.

Table 3 shows a result of totaling and comparing the muscle tone on the left upper and lower limbs and the right upper and lower limbs on the first day of the intervention and at the end of the intervention. No significant difference was observed between the two.

Table 3. Statistical results of muscle tone.

Part of body (Grades)	Initial day	Final day
Right elbow flexor muscles (1/2/3/4/5)	3/4/3/1/0	2/2/2/5/0
Left elbow flexor muscles (1/2/3/4/5)	3/0/4/3/1	5/0/1/4/1
Right palm flexor muscles (1/2/3/4/5)	2/7/2/0/0	6/1/2/2/0
Left palm flexor muscles (1/2/3/4/5)	5/3/2/1/0	6/1/1/3/0
Right knee extensor muscles (1/2/3/4/5)	7/2/2/0/0	9/1/0/1/0
Left knee extensor muscles (1/2/3/4/5)	6/4/1/0/0	8/1/2/0/0
Right plantar flexor muscles (1/2/3/4/5)	5/1/1/1/3	6/1/1/3/0
Left plantar flexor muscles (1/2/3/4/5)	4/3/1/1/2	2/5/2/2/0

Number.

No significant difference was observed comparing pulse rate and SpO₂ before and after exercise on the first day of exercise and before and after exercise at the end of the intervention.

No adverse events were observed during the intervention.

DISCUSSION

In this study, we investigated the natural changes in limb skeletal muscle mass and water content in participants with severe CP and examined the safety of an exercise intervention in participants. Although we hypothesized progressive muscle loss over the 6-month period, the SMI did not show a statistically significant decline. Conversely, ECW/TBW increased in the trunk and right lower limb, suggesting changes in fluid balance rather than measurable muscle loss.

It has been reported that skeletal muscle mass decreases due to aging and inactivity^12,13,14). Unloaded inactivity induces atrophy and functional deconditioning of skeletal muscle, especially in the lower extremities. In terms of aging upper and lower limb muscle mass, previous studies have also shown that lower limb muscle mass decreases more rapidly than that in the upper limbs^{12, 14)}. In the present study, the effect sizes for ECW/TBW other than the right upper limb were medium to large, characteristically ECW/TBW increased in the trunk and the lower limb at 3 and 6 months compared with at the start. A body composition analyzer is often used to evaluate muscle mass. As the amount of water is considered to be muscle mass when taking measurements with a body composition analyzer, it is said that an increase in water content correlates with an increase in SMI¹⁵⁾. In the participants of the present study, the decrease in muscle mass due to aging and inactivity progressed in the trunk and the lower limb, but the increase in water content, that is, the worsening of edema, might be related to the fact that there was no significant change in the SMI. These findings indicate that, within a relatively short observation window, edema progression may be more detectable than changes in skeletal muscle mass. Therefore, the longitudinal changes we observed were primarily related to fluid shifts, whereas muscle loss, if present, may require longer observation to detect.

A recent study showed that transitioning from a seated to a standing position contributes to the accumulation of light activity and reduces sedentary behavior. This activity might be a feasible option for children with CP who are classified in GMFCS levels IV or V¹⁶⁾. As the exercise content was passive in the present study, the exercise load was not sufficient to fluctuate the pulse rate and SpO₂, and it was not an exercise that affected muscle tone. The absence of adverse events applies only to the low-intensity, low-frequency passive exercise used in this study; the findings should not be generalized to more intensive or higher-frequency programs, so it is necessary to examine the type of feasible exercise for individuals at GMFCS level V.

This study had certain limitations. First, no control group was set up, so the intervention group could not be compared with a control group. Second, The small sample size, single-center design, and heterogeneity inherent to severe CP limit generalizability. Third, a small number of interventions was used; the results may have differed if the intervention frequency was increased. Fourth, the 6-month observation period may have been too short to detect meaningful natural declines in skeletal muscle mass, which often occur over years rather than months. This likely contributed to the absence of measurable SMI changes. Fifth, due to the small number of cases, we were unable to verify confounding factors such as age.

In conclusion, within the 6-month observation period, edema progression was detectable, but measurable declines in muscle mass were not, suggesting that longer follow-up periods are likely needed to capture natural changes in skeletal muscle in severe CP. Although the passive exercises did not lead to any adverse incidents for such cases, they did not demonstrate measurable effects on edema or muscle mass. Further research such as longer follow-up periods (≥12–24 months) to clarify natural muscle changes, and higher-frequency or alternative exercise modalities like tilt-table standing will be required in the future.

Conflict of interest

All authors have declared that no financial support was received from any organization for the submitted work. All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work.