Assessment of muscle function in severely burned children

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9

avai lable at www.sc iencedi rec t .com

journal homepage: www.e lsevier .com/ locate /burns

§

Shashi M. Alloju c, David N. Herndon a,b,c, Serina J. McEntire a,b, Oscar E. Suman a,b,c,*aShriners Hospitals for Children, 815 Market Street, Galveston, TX 77550, United StatesbDepartment of Surgery, The University of Texas Medical Branch, Galveston, TX 77555, United StatescSchool of Medicine, The University of Texas Medical Branch, Galveston, TX 77555, United States

a r t i c l e i n f o

Article history:

Accepted 19 October 2007

Keywords:

Burns

Peak torque

Total work

Lean mass

a b s t r a c t

Introduction: The posttraumatic response to a severe burn leads to marked and prolonged

skeletal muscle catabolism and weakness, which persist despite standard rehabilitation

programs of occupational and physical therapy. We investigated the degree to which the

prolonged skeletal muscle catabolism affects the muscle function of children 6 months after

severe burn.

Methods: Burned children, with >40% total body surface area burned, were assessed at 6

months after burn in respect to lean body mass and leg muscle strength at 1508/s. Lean body

mass was assessed using dual-energy X-ray absorptiometry. Leg muscle strength was

assessed using isokinetic dynamometry. Nonburned children were assessed similarly,

and served as controls.

Results: We found that severely burned children (n = 33), relative to nonburned children

(n = 46) had significantly lower lean body mass. Additionally they had significantly lower

peak torque as well total work performance using the extensors of the thigh.

Conclusions: Our results serve as an objective and a practical clinical approach for assessing

muscle function and also aid in establishing potential rehabilitation goals, and monitoring

progress towards these goals in burned children.

# 2007 Elsevier Ltd and ISBI. All rights reserved.

1. Introduction

Severe burns result in marked and prolonged skeletal muscle

catabolism and weakness [1], which persist despite ‘‘stan-

dard’’ rehabilitation programs of occupational and physical

therapy. This state of catabolism and weakness is made worse

by the period of physical inactivity following the burn incident

[2]. Despite the extensive amount of literature on the physical

effects of a severe burn, there is a lack of individual

quantitative data of pediatric burn patients’ muscle function.

Individual and quantitative assessment of muscle function

can be useful information in evaluating functional capability,

and the efficacy of rehabilitation strategies. Therefore, in this

§ The study was supported by the National Institute for DisabilitieInstitutes of Health grants P50-GM06338, K01-HL70451, RO1-HD04947

* Corresponding author at: The Children’s Wellness and Exercise Cente77550, United States. Tel.: +1 409 770 6557; fax: +1 409 770 6919.

E-mail address: [email protected] (O.E. Suman).

0305-4179/$34.00 # 2007 Elsevier Ltd and ISBI. All rights reserved.doi:10.1016/j.burns.2007.10.006

study, individual isokinetic leg muscle function data in burned

children and age matched controls is presented as well as a

potential clinical application to assess the rehabilitation in

burned patients, and perhaps construct an individually

tailored rehabilitative plan.

2. Methods

2.1. Subjects

Children, ages 6–17, were enrolled in this study. The groups

consisted of children with burn and children without burn to

s and Rehabilitation Research grant H133A020102, the National1 and Shriners Hospitals for Children grant 8760.r, Shriners Hospitals for Children, 815 Market Street, Galveston, TX

Fig. 1 – Image showing the Biodex Isokinetic

Dynamometer. Subjects are seated upright with seat

height, distance from ankle to knee and distance from

knee to back recorded.

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9 453

serve as age matched controls. Only subjects with �40% of

total body surface area (TBSA) burned, as assessed by the ‘‘rule

of nines’’ method [3] during excisional surgery in the acute

phase injury, were enrolled. Patients were excluded if they had

one or more of the following: leg amputation, anoxic brain

injury, psychological disorders, quadriplegia, or severe beha-

vior or cognitive disorders. Informed consent was obtained by

the parent or legal guardian. All of the burned subjects

received ‘‘standard’’ medical care and treatment from the

time of admission and acute care of the burn until time of

discharge. This standard medical care refers to the typical and

reasonable surgical and medical care during the acute phase,

as well as after discharge from the acute unit [3–8]. The

nonburned group was randomly selected; however the age

and exclusion/inclusion criteria were met to match the burned

group.

2.2. Strength measurements

Strength testing using a Biodex Isokinetic Dynamometer

(Shirley, NY) was done at approximately 6 months after the

date of burn [9]. The isokinetic test was performed on the

dominant leg extensors and tested at an angular velocity of

150 8/s. The children were seated and their position stabilized

with a restrained strap over the mid-thigh, pelvis, and trunk in

accordance to the Biodex Advantage Operating Manual. All

children were familiarized with the Biodex test in a similar

manner (Fig. 1). First, the procedure was demonstrated by the

administrator of the test. Second, the test procedure was

explained to the children, and third, the children were allowed

to warm-up and practice the actual movement by performing

three repetitions without a load. More repetitions were not

allowed to prevent the potential onset of fatigue. The

anatomical axis of the knee joint was aligned with the

mechanical axis of the dynamometer before the test. After the

three sub maximal warm-up repetitions, 10 maximal volun-

tary muscle contractions (full extension and flexion) were

performed. The maximal repetitions were performed con-

secutively without rest in between. Three minutes of rest was

given to minimize the effects of fatigue and the test was

repeated.

Values of peak torque and total work were calculated by the

Biodex software system (see Table 1 for definitions of peak

torque and total work). The highest peak torque (expressed as

Newton-meters (N m)) and total work (expressed as Joules (J))

between the two trials were selected. Peak torque was

corrected for gravitational moments of the lower leg and

the lever arm. Corrections for differences in leg lean mass

(LLM) were made by dividing peak torque and total work by

LLM.

Table 1 – Definitions of muscle function

Peak torque: Highest muscular force output at any moment during a

repetition. Indicative of a muscle’s strength capabilities

(reported in Newton-meters; N m)

Total work: Total muscular force output for the repetition with

greatest amount of work. Work is indicative of a muscle’s

capability to produce force throughout the range of motion

(reported in Joules; J)

2.3. Lean body mass measurements

Total lean body mass (TLBM) and LLM measurements were

made for both groups using the dual-energy X-ray absorptio-

metry (DEXA) using the QDR 4500A software (Hologic,

Waltham, MA). Scans were taken with the patient lying

supine on the scanning table. The protocol for obtaining a

whole body scan was done according to the manufacturer’s

instructions and has been described by our group. DEXA with

pediatric software can measure the attenuation of two X-ray

beams, one which is high energy and other which is low

energy. These measurements are then compared with

standard models of thickness used for bone and soft tissue.

Subsequently, the calculated soft tissue is separated into

TLBM, and fat mass. Lean mass whether it is TLBM or LLM is

reported in kilograms.

2.4. Data analysis

Differences in LLM and TLBM between burn and unburned

were assessed using Student’s t-test. Effects of burn on peak

torque and total work corrected for LLM were evaluated using

a two-way ANOVA followed by Tukey’s test when appropriate.

Relationships between variables such as LLM and peak torque

were evaluated using Pearson’s correlation coefficient and

linear regressions. Results are presented as mean � S.E.M.

Statistical significance was accepted at the p < 0.05 level.

Table 2 – Demographic characteristics of patients

Burned (n = 33) Nonburned (n = 46)

Gender 25 male/8 female 24 male/22 female

TBSA 56.0% � 15.0% N/A

Age (years) 11.8 � 3.4 12.1 � 2.6

Height (cm) 145.0 � 20.2 154.0 � 15.6

Weight (kg) 63.0 � 39.3 59.1 � 22.0

Values are means � S.E.M; n, no. of subjects; TBSA, total body

surface area. Burned and nonburned groups were similar in age,

height, and weight.

Fig. 3 – Mean values of lean body mass of the leg between

burned and nonburned children. Similar to total LBM, right

leg lean body mass was significantly lower in severely

burned children relative to nonburned children. Symbol *

denotes a significant difference between groups ( p < 0.01).

Values are means W S.E.M.

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9454

3. Results

3.1. Demographics

Seventy-nine children were enrolled in the study (49 boys, 30

girls). Thirty-three children with burn injury were tested 6

months after burn and compared to 46 children without burn,

who served as controls. The range in age for the burned

children’s group and the control group was 6–17 years. There

were no differences at 6 months after burn between the groups

in terms of age, vertical height, and standing weight (Table 2).

3.2. Lean mass

Measurement of total and leg lean mass obtained by DEXA

revealed significant differences between the two groups. For

nonburned children, absolute values in TLBM were 39.4 kg and

6.2 kg for LLM. In contrast, TLBM and LLM in the burned group

were 32.7 kg and 5.1 kg, respectively. This reflected a 20.3%

and 22.2% difference between the groups in mean TLBM and

LLM, respectively (Figs. 2 and 3).

Fig. 2 – Mean values of total lean body mass (TLBM)

between burned and nonburned children. As expected,

burned children have significantly lower total lean body

mass compared to nonburned children. Symbol * denotes

a significant difference between groups ( p < 0.01). Values

are means W S.E.M.

Fig. 4 – Individual values of peak torque (PKT) during leg

extension (speed of 1508/s) versus lean body mass (LBM) of

leg. Each point represents the highest muscular force at

any moment during a repetition. This is indicative of a

muscles strength capabilities. There is a strong and

significant relationship between PKT and leg LBM in both

burned and nonburned children.

3.3. Muscle function

Peak torque values for nonburned children were 91.5 N m. In

burned children, peak torque was 49.0 N m. There was a

significant difference in the amount of peak torque that could

be generated between the burn and nonburned groups. The

nonburned group had a 68.1% greater normalized peak torque

(Fig. 4).

Total work values for nonburned children were 84.4 J. In

burned children, total work was 46.9 J. A significant difference

was found in the amount of total work generated between the

Fig. 5 – Individual values of total work during leg extension

(speed of 1508/s) versus lean body mass (LBM) of leg. Total

work is indicative of muscle’s capability to produce force

throughout the range of motion. There was a significant

relationship between total work and right leg LBM in both

burned and nonburned children.

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9 455

burn and nonburned groups. The nonburned group had a

64.2% greater total work (Fig. 5).

4. Discussion

Our results indicate a significant difference in the total and leg

lean body mass between burned and nonburned children and

a difference in peak torque and total work across ages in

children 6 months after burn when compared to age matched

nonburned children. The loss of skeletal muscle results in a

decrease in muscle function. This decrease in muscle function

was quantitatively represented by our data and shows that

peak torque and total work produced by muscle are reduced at

6 months after burn, and that this muscle weakness persists

across ages. In contrast, there were no significant differences

in the functional range of motion between burned and

nonburned controls.

Our data on lean mass corroborates findings from our

group in which mean values of LBM were reported [10,11].

However, in these studies only mean values for LBM for

burned and nonburned children were reported with no

information on individual values of LBM. Therefore, in the

present study, we provide individual LBM and muscle strength

data, which may be useful to therapists and medical personnel

involved in the physical rehabilitation of burned children.

Muscle function has not been well documented in the burn

literature. Most of the studies give mean values, but the

studies are limited by fewer than 15 patients [10–15] and are

often not directly compared to a nonburned group. Addition-

ally, since individual LBM values were not reported, it is

difficult to use reported mean values to evaluate an individual

patient or a patient’s progress.

The type of testing used to evaluate muscle function has

also been a limitation. Roberts et al. [13], provided limited,

prospectively gathered information on hand strength of seven

burned patients. Static grip strength was measured and

comparisons were made between test strengths and pub-

lished norms, for age and gender, with analysis of variance.

They found that at discharge, isometric strength was

significantly less than normal for age and gender. However,

grip strength was improved by 6 weeks, and all measurements

were improved at 6 months after discharge, although grip

strength remained significantly less than norms. In spite of

significantly lower than normal grip and lateral strength

measurements at 6 months, it cannot be determined whether

this hinders performance of daily living skills, as most

physical activities are more dynamic and rhythmic in nature.

In addition, their study also contained a very small number of

patients. The idea of a simple test such as grip strength to

assess muscle function is attractive. We evaluated (unpub-

lished data) grip strength and isokinetic function in 11 burned

children and the correlation is extremely low (r2 = 0.11),

reflecting that static, isometric strength and isokinetic func-

tion are most probably not reflective of one another. Another

type of muscle function test is the ability to produce an

isotonic contraction. Cucuzzo et al. conducted a study where

they evaluated isotonic muscle strength in burned children.

However, in that study, mean values of load lifted were given,

and not corrected by body size (weight) or the amount of lean

mass [14]. In addition, it is often believed that isotonic testing

does not adequately test strength, power, and endurance [15].

In our present study, we used isokinetic testing to assess

muscle function. Isokinetic testing has been reported to

improve assessment of muscle function [15]. Isokinetic testing

also allows measurement of dynamic muscular parameters

under a predetermined rate. The rate chosen for this

experiment was 1508/s which closely approximates the

motion of walking of burn children. For practicality, we chose

this due to the fact that rehabilitation programs heavily focus

on helping the patient return to normalcy where they can

resume activities such as walking and playing, which are

largely dynamic muscular functions.

Almekinders and Oman stated in a review of isokinetic

dynamometry, that this form of testing produced reliable data

when testing simple uniaxial joints, such as the knee [16]. In

addition, they reported that the strength of isokinetic testing

was not in the diagnosis of orthopedic abnormalities, but

instead in the monitoring of a patient’s progress as they

recover or participate in a rehabilitation program. We agree

with these statements, and offer in our paper examples of how

monitoring patient’s progress could be accomplished using

our quantitative, individual data (see Cases 1 and 2 further

down in the Section 4). However, isokinetic testing does have

periods of accelerations and decelerations, even though a

constant force throughout the functional range of motion is

being exerted. Nonetheless, the final results in peak torque

and total work can be reproduced consistently with each

subject despite the accelerations and decelerations [17–20].

Our data shows that normalized peak torque is signifi-

cantly decreased when compared to age matched nonburned

controls. As postulated previously, we believe that the

catabolic state induced by the onset of the severe burn event

causes the decrease in muscle mass, as indicated by the

decrease in lean body mass and therefore muscle function.

Not only are the burn patients unable to generate equal

Fig. 6 – Individual values for functional ‘‘dynamic’’ range of

motion (ROM) measured in degrees. Functional ‘‘dynamic’’

ROM was assessed during the performance of leg

extension. Values of ROM between burned and nonburned

children were not significantly different ( p = 0.93). Values

are means W S.E.M.

Fig. 7 – Individual values of peak torque (N m/kg of lean

mass of leg during leg extension at a speed of 1508/s)

versus age for Case 1. N1E is a 12-year-old male with 53%

TBSA and 53% third degree burns. Upon discharge from

the hospital, a muscle function test was performed

yielding a peak torque of 9.0 N m/kg of lean mass of leg

(point DC). At that point, the patient started a 12-week

program of exercise conditioning supplemented with

physical and occupational therapy. At 6 months after burn

during a follow-up visit, peak torque had increased to

10.9 N m/kg of lean mass of leg (point 6m), reflecting an

increase of 21.5%. From time of discharge to 12 weeks after

discharge (approximately 12 weeks apart) the patient

participated in a 12-week exercise conditioning program,

which proved to be beneficial for physical function.

A 1-year follow-up assessment revealed that peak torque

again had increased to 14.1 N m/kg of lean mass of leg

(point 12m) indicating that strength levels and present

physical activity levels were appropriate.

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9456

muscular force during a repetition, they are not able to

generate as much equal muscular force through a single

repetition, which is indicated by total work.

Recently, Wiggin et al. provided individual values of peak

torque in nonburned children [21]. In their study, a total of

3587 children were tested for isokinetic knee strength.

Children ranged in age from 6 to 13 years of age, and percentile

charts of isokinetic peak torque for quadriceps were estab-

lished for gender and age. However, values of isokinetic peak

torque were not indexed for body weight or lean mass; two

factors that have an effect on strength and total work.

Nonetheless, their study is the first to report peak torque

values for quadriceps and hamstrings in nonburned children.

Similar to our study, they state that the use of a standardized

testing protocol and normative data, allows clinicians to

assess the degree of muscle weakness, as well as the

effectiveness of intervention strategies. We agree with this

statement and strongly believe that Wiggin’s study is

extremely valuable; however the question of how a single

burned child’s muscle function will compare to other burned

or nonburned children, is not answered by Wiggin’s study. Our

study utilizes the amount of lean mass as a correction factor

for observed values of peak torque and total work, and shows

indexed individual quantitative data of burned children,

which has not been previously done.

To our knowledge, individual values of functional, dynamic

range of motion in burned children relative to nonburned

children have not been published. Functional, dynamic range

of motion was found to be similar between the burned and

nonburned groups (Fig. 6). We attribute this result to the

excellent post burn surgical care to release skin and tissue

contractures to restore functional range of motion. However,

this needs to be studied further as it is presently speculative.

Our study has potential clinical significance and applica-

tion. For example, we applied our study to specific patient

cases to assess a patient’s progress. For example, one can plot

the status of a patient and assess the condition, set objectives

and determine whether those are met (Cases 1 and 2).

Functional assessment can be done regardless of the treat-

ment during the acute or outpatient phase, conditions such as

length of hospital stay, presence or absence of inhalation

injury since each person can be compared to himself or if

desired compared relative to others.

4.1. Case 1

N1E is a 12-year-old male with 53% TBSA and 53% third degree

burns. Peak torque—upon discharge from the hospital, a

muscle function test was performed yielding a peak torque

of 9.0 N m/kg of leg lean mass (Fig. 7, point DC). At 6 months

after burn, peak torque had increased to 10.9 N m/kg of leg

lean mass (Fig. 7, point 6m), reflecting an increase of 21.5%. It

must be noted that from time of discharge to 12 weeks after

discharge (approximately 12 weeks apart), the patient parti-

cipated in a 12-week exercise conditioning program, which

proved to be beneficial for physical function. At 1-year after

burn follow-up assessment revealed that peak torque again

had increased to 14.0 N m/kg of leg lean mass (Fig. 7, point

Fig. 8 – Individual values of total work (Joules/lean mass of

leg) during leg extension (speed of 1508/s) versus age for

Case 1. N1E is a 12-year-old male with 53% TBSA and 53%

third degree burns. Upon discharge from the hospital, a

muscle function test yielded a total work performed of

8.1 J/kg of lean mass of leg (point DC). At that point, the

patient started a 12-week program of exercise

conditioning supplemented with physical and

occupational therapy. At 6 months post burn during a

follow-up visit, total work performed had increased to

11.1 J/kg of lean mass of leg (point 6m), reflecting an

increase of 36.7%. It must be noted that from time of

discharge to 12 weeks after discharge (approximately 12

weeks apart) the patient participated in a 12-week

exercise conditioning program, which proved to be

beneficial for physical function. A 1-year post burn follow-

up assessment revealed that total work performed again

had increased to 13.2 J/kg of lean mass of leg (point 12m)

indicating that strength levels and present physical

activity levels were appropriate relative to nonburned

children.

Fig. 9 – Individual values of peak torque (N m/kg of lean

mass of leg during leg extension at a speed of 1508/s)

versus age for Case 2. J2M is a 9-year-old male with 40%

TBSA and 40% third degree burns. Upon discharge from

the hospital, a muscle function test was performed

yielding a peak torque value of 5.0 N m/kg of lean mass of

leg (point DC). At that point, the patient started a 12-week

program of exercise conditioning supplemented with

physical and occupational therapy. The evaluation after

the 12-week program yielded a peak torque of 10.0 N m/kg

of lean mass of leg (point 6m), also reflecting the efficacy of

the training program. However, at 1-year post burn, a

follow-up assessment showed that peak torque had

decreased (peak torque = 9.3 N m/kg of lean mass of leg)

and still under the level of nonburned children (point 12m),

suggesting the need for an increase in physical activity or

additional resistive exercises to increase strength.

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9 457

12m) indicating that strength levels and present physical

activity levels were appropriate. Total work—upon discharge

from the hospital, the patient results were 8.1 J/kg of leg lean

mass (Fig. 8, point DC). At 6 months after burn the amount of

total work increased to 11.1 J/kg of knee lean mass (an increase

of 36.7%). At one year follow-up assessment the total work

done was 13.2 J/kg of leg lean mass, supporting the similar

findings of improved and appropriate muscle strength (Fig. 8,

point 12m). Comparatively this patient started at the expected

level for a burn patient but made progress during the course of

a year to perform at the level of a nonburned child.

4.2. Case 2

J2M is a 9-year-old male with 40% TBSA and 40% third degree

burns. Peak torque—upon discharge from the hospital, a

muscle function test was performed yielding a peak torque

value of 15.6 N m/kg of leg lean mass (Fig. 9, point DC). At that

point, he started a 12-week program of exercise conditioning

supplemented with physical and occupational therapy. The

evaluation after the 12-week program yielded a peak torque of

33.7 N m/kg of leg lean mass (Fig. 9, point 6m), also reflecting

the efficacy of the training program. However, at 1-year after

burn, a follow-up assessment showed that peak torque had

remained relatively unchanged (peak torque = 37.7 N m/kg of

leg lean mass) and still under the level of nonburned children

(Fig. 9, point 12m), suggesting the need for an increase in

physical activity or even additional resistive exercises to

increase strength. Total work—upon discharge from the

hospital, muscle function test results for total work was

4.2 J/kg of leg lean mass (Fig. 10, point DC). At that point, he

started a 12-week program of exercise conditioning supple-

mented with physical and occupational therapy. The evalua-

tion after the 12-week program yielded a total work of 6.9 J/kg

of leg lean mass (Fig. 10, point 6m), also reflecting the efficacy

of the training program. However, at 1-year, a follow-up

assessment showed that total work had remained relatively

unchanged (total work = 6.8 J/kg of leg lean mass) and still

under the level of nonburned children (Fig. 10, point 12m),

suggesting the need for an increase in physical activity or even

additional resistive exercises to increase strength and work

performed.

We believe that the strength of this study lies in the

individual, indexed, quantitative analyses performed on

Fig. 10 – Individual values of total work (Joules/lean mass of

leg) during leg extension (speed of 1508/s) versus age for

Case 1. J2M is a 9-year-old male with 40% TBSA and 40%

third degree burns. Upon discharge from the hospital, a

muscle function test yielded a total work performed of

4.2 J/kg of lean mass of leg (point DC). At that point, the

patient started a 12-week program of exercise

conditioning supplemented with physical and

occupational therapy. At 6 months post burn during a

follow-up visit, total work performed had increased to

6.9 J/kg of lean mass of leg (point 6m), reflecting an

increase of 64.2%. It must be noted that from time of

discharge to 12 weeks after discharge (approximately 12

weeks apart) the patient participated in a 12-week

exercise conditioning program, which proved to be

beneficial for physical function. A 1-year follow-up

assessment revealed that total work performed had

decreased slightly to 6.8 J/kg of lean mass of leg (point

12m) suggesting the need for an increase in physical

activity or additional resistive exercises to increase

strength.

Fig. 11 – Individual values of peak torque (PKT)/lean mass

of leg during leg extension (speed of 1508/s) versus age.

Age did not seem to influence normalized peak torque

(r2 = 0.11). However, there was a significant difference

( p < 0.001) in normalized PKT between burned and

nonburned children across age.

Fig. 12 – Individual values of total work/lean mass of leg

during leg extension (speed of 1508/s) versus age. Age did

not seem to influence normalized total work. However, a

significant difference ( p < 0.001) in normalized total work

occurred between burned and nonburned children across

ages.

b u r n s 3 4 ( 2 0 0 8 ) 4 5 2 – 4 5 9458

muscle function in burned children. This is information that is

lacking in the burn literature. Our study fills this void. In

addition, our study has potential clinical importance in that

therapists or exercise specialists may be able to use this

information to evaluate and compare the muscle function of

their individual burned patient to other burned and non-

burned individuals (Figs. 7–12). More research in the quanti-

tative assessment of muscle function and the progress or lack

of progress of an individual burned child is needed. This paper

may serve as a tool to fulfill this need.

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