- Email: [email protected]
Assessment of muscle function in severely burned children
burns 34 (2008) 452–459
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/burns
Assessment of muscle function in severely burned children§ Shashi M. Alloju c, David N. Herndon a,b,c, Serina J. McEntire a,b, Oscar E. Suman a,b,c,* a
Shriners Hospitals for Children, 815 Market Street, Galveston, TX 77550, United States Department of Surgery, The University of Texas Medical Branch, Galveston, TX 77555, United States c School of Medicine, The University of Texas Medical Branch, Galveston, TX 77555, United States b
article info
abstract
Article history:
Introduction: The posttraumatic response to a severe burn leads to marked and prolonged
Accepted 19 October 2007
skeletal muscle catabolism and weakness, which persist despite standard rehabilitation programs of occupational and physical therapy. We investigated the degree to which the
Keywords:
prolonged skeletal muscle catabolism affects the muscle function of children 6 months after
Burns
severe burn.
Peak torque
Methods: Burned children, with >40% total body surface area burned, were assessed at 6
Total work
months after burn in respect to lean body mass and leg muscle strength at 1508/s. Lean body
Lean mass
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 ‘‘standard’’ 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
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
§ The study was supported by the National Institute for Disabilities and Rehabilitation Research grant H133A020102, the National Institutes of Health grants P50-GM06338, K01-HL70451, RO1-HD049471 and Shriners Hospitals for Children grant 8760. * Corresponding author at: The Children’s Wellness and Exercise Center, Shriners Hospitals for Children, 815 Market Street, Galveston, TX 77550, 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
burns 34 (2008) 452–459
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 behavior 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 voluntary muscle contractions (full extension and flexion) were performed. The maximal repetitions were performed consecutively 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.
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.
2.3.
Total lean body mass (TLBM) and LLM measurements were made for both groups using the dual-energy X-ray absorptiometry (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. 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)
Lean body mass measurements
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.
454
burns 34 (2008) 452–459
Table 2 – Demographic characteristics of patients Burned (n = 33) Gender TBSA Age (years) Height (cm) Weight (kg)
25 male/8 female 56.0% 15.0% 11.8 3.4 145.0 20.2 63.0 39.3
Nonburned (n = 46) 24 male/22 female N/A 12.1 2.6 154.0 15.6 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.
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.
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.
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. 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.
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.
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
burns 34 (2008) 452–459
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.
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. Additionally, 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
455
burned patients. Static grip strength was measured and comparisons were made between test strengths and published 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 (unpublished 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 function 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 significantly 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
456
burns 34 (2008) 452–459
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.
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 established 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 application. 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
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.
and determine whether those are met (Cases 1 and 2). Functional assessment can be done regardless of the treatment 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 participated 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
burns 34 (2008) 452–459
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 followup 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.
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
457
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.
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 supplemented with physical and occupational therapy. The evaluation 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
458
burns 34 (2008) 452–459
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.
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 nonburned individuals (Figs. 7–12). More research in the quantitative 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.
references
[1] Hart DW, Wolf SE, Mlcak R, Chinkes DL, Ramzy PI, Obeng MK, et al. Persistence of muscle catabolism after severe burn. Surgery 2000;128(2):312–9. [2] Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 1996;270(4 Pt 1):E627– 33. [3] Herndon DN, Rutan RL, Alison WE, Cox CS. Management of burn injuries. In: Eichelberger MR, editor. Pediatric Trauma: Prevention, Acute Care and Rehabilitation. St. Louis: Mosby Year Book; 1993. p. 568–90. [4] Herndon DN, Curreri PW, Abston S, Rutan TC, Barrow RE. Treatment of burns. Curr Probl Surg 1987;24(6):341–97. [5] Herndon DN, Spies M. Modern burn care. Semin Pediatr Surg 2001;10(1):28–31. [6] Herndon DN, Thompson PB, Desai MH, Van Osten TJ. Treatment of burns in children. Pediatr Clin North Am 1985;32(5):1311–32. [7] Herndon DN. Burn Care 2007. [8] Celis MM, Suman OE, Huang TT, Yen P, Herndon DN. Effect of a supervised exercise and physiotherapy program on surgical interventions in children with thermal injury. J Burn Care Rehabil 2003;24(1):57–61. discussion 56. [9] Biodex Advantage Software Operations Manual [Isokinetic Dynamometer]. Version 3.2. Shirley, NY. 2001.
burns 34 (2008) 452–459
[10] Suman OE, Spies RJ, Celis MM, Mlcak RP, Herndon DN. Effects of a 12-wk resistance exercise program on skeletal muscle strength in children with burn injuries. J Appl Physiol 2001;91(3):1168–75. [11] Suman OE, Thomas SJ, Wilkins JP, Mlcak RP, Herndon DN. Effect of exogenous growth hormone and exercise on lean mass and muscle function in children with burns. J Appl Physiol 2003;94(6):2273–81. [12] Przkora R, Herndon DN, Suman OE. The effects of oxandrolone and exercise on muscle mass and function in children with severe burns. Pediatrics 2007;119(1):e109–16. [13] Roberts L, Alvarada MI, McElroy K, Rutan RL, Desai MH, Herndon DN, et al. Longitudinal hand grip and pinch strength recovery in the child with burns. J Burn Care Rehabil 1993;14(1):99–101. [14] Cucuzzo NA, Ferrando A, Herndon DN. The effects of exercise programming vs traditional outpatient therapy in the rehabilitation of severely burned children. J Burn Care Rehabil 2001;22(3):214–20. [15] Cronan T, Hammond J, Ward CG. The value of isokinetic exercise and testing in burn rehabilitation and
[16] [17]
[18]
[19]
[20]
[21]
459
determination of back-to-work status. J Burn Care Rehabil 1990;11(3):224–7. Almekinders LC, Oman J. Isokinetic muscle testing: is it clinically useful? J Am Acad Orthop Surg 1994;2(4):221–5. Osternig LR. Optimal isokinetic loads and velocities producing muscular power in human subjects. Arch Phys Med Rehabil 1975;56(4):152–5. Osternig LR. Isokinetic dynamometry: implications for muscle testing and rehabilitation. Exerc Sport Sci Rev 1986;14:45–80. Osternig LR, Bates BT, James ST. Isokinetic and isometric torque force relationships. Arch Phys Med Rehabil 1977;58(6):254–7. Osternig LR, Hamill J, Corcos DM, Lander J. Electromyographic patterns accompanying isokinetic exercise under varying speed and sequencing conditions. Am J Phys Med 1984;63(6):289–97. Wiggin M, Wilkinson K, Habetz S, Chorley J, Watson M. Percentile values of isokinetic peak torque in children six through thirteen years old. Pediatr Phys Ther 2006;18(1):3–18.
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/burns
Assessment of muscle function in severely burned children§ Shashi M. Alloju c, David N. Herndon a,b,c, Serina J. McEntire a,b, Oscar E. Suman a,b,c,* a
Shriners Hospitals for Children, 815 Market Street, Galveston, TX 77550, United States Department of Surgery, The University of Texas Medical Branch, Galveston, TX 77555, United States c School of Medicine, The University of Texas Medical Branch, Galveston, TX 77555, United States b
article info
abstract
Article history:
Introduction: The posttraumatic response to a severe burn leads to marked and prolonged
Accepted 19 October 2007
skeletal muscle catabolism and weakness, which persist despite standard rehabilitation programs of occupational and physical therapy. We investigated the degree to which the
Keywords:
prolonged skeletal muscle catabolism affects the muscle function of children 6 months after
Burns
severe burn.
Peak torque
Methods: Burned children, with >40% total body surface area burned, were assessed at 6
Total work
months after burn in respect to lean body mass and leg muscle strength at 1508/s. Lean body
Lean mass
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 ‘‘standard’’ 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
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
§ The study was supported by the National Institute for Disabilities and Rehabilitation Research grant H133A020102, the National Institutes of Health grants P50-GM06338, K01-HL70451, RO1-HD049471 and Shriners Hospitals for Children grant 8760. * Corresponding author at: The Children’s Wellness and Exercise Center, Shriners Hospitals for Children, 815 Market Street, Galveston, TX 77550, 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
burns 34 (2008) 452–459
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 behavior 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 voluntary muscle contractions (full extension and flexion) were performed. The maximal repetitions were performed consecutively 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.
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.
2.3.
Total lean body mass (TLBM) and LLM measurements were made for both groups using the dual-energy X-ray absorptiometry (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. 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)
Lean body mass measurements
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.
454
burns 34 (2008) 452–459
Table 2 – Demographic characteristics of patients Burned (n = 33) Gender TBSA Age (years) Height (cm) Weight (kg)
25 male/8 female 56.0% 15.0% 11.8 3.4 145.0 20.2 63.0 39.3
Nonburned (n = 46) 24 male/22 female N/A 12.1 2.6 154.0 15.6 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.
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.
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.
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. 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.
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.
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
burns 34 (2008) 452–459
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.
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. Additionally, 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
455
burned patients. Static grip strength was measured and comparisons were made between test strengths and published 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 (unpublished 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 function 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 significantly 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
456
burns 34 (2008) 452–459
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.
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 established 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 application. 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
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.
and determine whether those are met (Cases 1 and 2). Functional assessment can be done regardless of the treatment 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 participated 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
burns 34 (2008) 452–459
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 followup 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.
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
457
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.
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 supplemented with physical and occupational therapy. The evaluation 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
458
burns 34 (2008) 452–459
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.
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 nonburned individuals (Figs. 7–12). More research in the quantitative 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.
references
[1] Hart DW, Wolf SE, Mlcak R, Chinkes DL, Ramzy PI, Obeng MK, et al. Persistence of muscle catabolism after severe burn. Surgery 2000;128(2):312–9. [2] Ferrando AA, Lane HW, Stuart CA, Davis-Street J, Wolfe RR. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 1996;270(4 Pt 1):E627– 33. [3] Herndon DN, Rutan RL, Alison WE, Cox CS. Management of burn injuries. In: Eichelberger MR, editor. Pediatric Trauma: Prevention, Acute Care and Rehabilitation. St. Louis: Mosby Year Book; 1993. p. 568–90. [4] Herndon DN, Curreri PW, Abston S, Rutan TC, Barrow RE. Treatment of burns. Curr Probl Surg 1987;24(6):341–97. [5] Herndon DN, Spies M. Modern burn care. Semin Pediatr Surg 2001;10(1):28–31. [6] Herndon DN, Thompson PB, Desai MH, Van Osten TJ. Treatment of burns in children. Pediatr Clin North Am 1985;32(5):1311–32. [7] Herndon DN. Burn Care 2007. [8] Celis MM, Suman OE, Huang TT, Yen P, Herndon DN. Effect of a supervised exercise and physiotherapy program on surgical interventions in children with thermal injury. J Burn Care Rehabil 2003;24(1):57–61. discussion 56. [9] Biodex Advantage Software Operations Manual [Isokinetic Dynamometer]. Version 3.2. Shirley, NY. 2001.
burns 34 (2008) 452–459
[10] Suman OE, Spies RJ, Celis MM, Mlcak RP, Herndon DN. Effects of a 12-wk resistance exercise program on skeletal muscle strength in children with burn injuries. J Appl Physiol 2001;91(3):1168–75. [11] Suman OE, Thomas SJ, Wilkins JP, Mlcak RP, Herndon DN. Effect of exogenous growth hormone and exercise on lean mass and muscle function in children with burns. J Appl Physiol 2003;94(6):2273–81. [12] Przkora R, Herndon DN, Suman OE. The effects of oxandrolone and exercise on muscle mass and function in children with severe burns. Pediatrics 2007;119(1):e109–16. [13] Roberts L, Alvarada MI, McElroy K, Rutan RL, Desai MH, Herndon DN, et al. Longitudinal hand grip and pinch strength recovery in the child with burns. J Burn Care Rehabil 1993;14(1):99–101. [14] Cucuzzo NA, Ferrando A, Herndon DN. The effects of exercise programming vs traditional outpatient therapy in the rehabilitation of severely burned children. J Burn Care Rehabil 2001;22(3):214–20. [15] Cronan T, Hammond J, Ward CG. The value of isokinetic exercise and testing in burn rehabilitation and
[16] [17]
[18]
[19]
[20]
[21]
459
determination of back-to-work status. J Burn Care Rehabil 1990;11(3):224–7. Almekinders LC, Oman J. Isokinetic muscle testing: is it clinically useful? J Am Acad Orthop Surg 1994;2(4):221–5. Osternig LR. Optimal isokinetic loads and velocities producing muscular power in human subjects. Arch Phys Med Rehabil 1975;56(4):152–5. Osternig LR. Isokinetic dynamometry: implications for muscle testing and rehabilitation. Exerc Sport Sci Rev 1986;14:45–80. Osternig LR, Bates BT, James ST. Isokinetic and isometric torque force relationships. Arch Phys Med Rehabil 1977;58(6):254–7. Osternig LR, Hamill J, Corcos DM, Lander J. Electromyographic patterns accompanying isokinetic exercise under varying speed and sequencing conditions. Am J Phys Med 1984;63(6):289–97. Wiggin M, Wilkinson K, Habetz S, Chorley J, Watson M. Percentile values of isokinetic peak torque in children six through thirteen years old. Pediatr Phys Ther 2006;18(1):3–18.