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Keywords:

  • Juvenile dermatomyositis;
  • Physiotherapy;
  • Exercise;
  • Magnetic resonance imaging;
  • Myometry

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES

Objective

To investigate the short-term effects of exercise on muscle inflammation in children with juvenile dermatomyositis (juvenile DM). Magnetic resonance imaging (MRI), muscle strength, and blood parameters were used as outcome measures.

Methods

Children with active juvenile DM, inactive juvenile DM, and healthy children were assessed for muscle strength (using myometry) and function, and MRI T2-weighted relaxation time measurement; blood was obtained from patients with juvenile DM. A standardized physiotherapy-led exercise program was completed, and the MRI was performed immediately afterwards. All children were reassessed with myometry and MRI at 30 minutes and 60 minutes, and repeat blood tests were performed at 60 minutes for the patients with juvenile DM.

Results

Ten children with active juvenile DM, 10 with inactive juvenile DM, and 20 healthy controls completed the study. Muscle inflammation assessed by MRI, myometry, and blood parameters did not change significantly in response to exercise either immediately after or up to 60 minutes after the exercise program in any group.

Conclusion

In the short term, a single bout of exercise does not change the degree of inflammation within the muscles of children with active or inactive juvenile DM or in healthy children. The data suggest that, at least in this time period, there is no evidence that exercise increases the inflammation within the muscles. We propose therefore that a moderate exercise program is safe for children with juvenile DM.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES

Juvenile dermatomyositis (juvenile DM) is a well recognized but rare pediatric vasculopathy. It is characterized clinically by progressive muscle weakness, initially in the proximal muscles but expanding into the distal muscle groups, and a distinctive rash over the face and extensor surfaces of the limbs (1). The disease may also be systemic, affecting many organs and causing severe morbidity and disability. Severe features of the disease include the development of calcinosis, characterized by the deposition of calcium within tissues, which may cause severe limitations in muscle function and joint mobility as well as severe pain. Calcinosis is believed to be a complication of uncontrolled, active juvenile DM and is related to severe disease (2, 3). At the present time, juvenile DM is diagnosed using the criteria of Bohan and Peter (4), and although these criteria are internationally recognized they are partially outdated because clinical practice has changed and new diagnostic tools, such as magnetic resonance imaging (MRI), have become available. The monitoring of disease activity in juvenile DM remains difficult. Muscle enzyme levels such as creatine kinase (CK) and lactate dehydrogenase (LDH) may be elevated with muscle inflammation, but do not always correlate with disease activity. Changes in muscle strength and function are useful tools to assess disease activity. We have recently shown that inflammation characteristic of active juvenile DM is visible as a high signal intensity on fat suppressed T2-weighted spin echo and STIR MR images (5, 6).

Historically, exercises and muscle strengthening have often been avoided in active juvenile DM. It was believed that exercise may cause muscle fiber damage and inflammation in juvenile DM. Some research does describe the onset of muscle inflammation after exercise, but only after strenuous exercise such as marathon running (7). The degree of inflammation in normal muscle is dependent upon the type, severity, and the duration of the exercise (8).

There has also been concern about the formation of calcinosis in areas of stress within the muscle, which may be related to the amount of exercise. Evidence to support this concept is scarce, and it is now widely believed that calcinosis is a complication of uncontrolled and severe active juvenile DM (3). There are several reports of studies of adults with dermatomyositis and polymyositis that have shown exercise to be beneficial rather than detrimental to these patients, and there is no evidence to support the theory that exercise increases the incidence of calcinosis (9–11).

Very little research has been conducted on children with juvenile DM and their response to exercise, and the few studies that have examined the changes in MRI have not explored the changes in healthy children as a comparison (12). In practical terms, children are very active, and as soon as they are physically able, they start moving and playing after the onset of their juvenile DM, thereby exercising their muscles spontaneously. To our knowledge no treatment center restricts active play for children with juvenile DM. This highlights the inconsistencies of approaches to exercise in this patient population (13).

In considering the safety of an exercise program, the comparison of concentric and eccentric muscle work is important. Concentric muscle work tends to cause less inflammation than eccentric work and it also requires less force in controlling joint movement. Much of the evidence about muscle damage after exercise is based on extreme levels of eccentric exercise, such as marathon running, and is not representative of a prescribed physiotherapy program (8, 14–16).

In a physiotherapy treatment program there are many reasons for performing exercises, including increasing strength and stamina or endurance, as well as increasing neuromuscular coordination and proprioception. Evidence has shown that a combination of eccentric and concentric exercise is the most effective training program for all ages (8, 14, 15, 17–21). This study program was designed to exercise different muscle groups within the thigh, because these are the muscles also being assessed by the MRI and myometer.

This study examines the effects of a specific single bout of moderate exercise on the changes in muscle inflammation of the thigh muscle as measured by MRI T2-weighted relaxation time, muscle strength (measured by myometry), and muscle enzymes (CK and LDH) in children with juvenile DM and healthy children.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES

Patients

Patients in the study were diagnosed with definite or probable juvenile DM by a consultant pediatric rheumatologist based on the Bohan and Peter criteria (4). These patients were seen at Great Ormond Street Hospital, London. Healthy children were recruited from the siblings of the children with juvenile DM and families of staff members. Ethical approval was provided by the Local Research Ethics Committee of the Institute of Child Health and Great Ormond Street Hospital National Health Service Trust.

Measures.

Physicians Global Assessment.

The Physicians Global Assessment (PGA) is a measurement of the overall impression of a patient's clinical wellbeing that takes into account other clinical features that aid in establishing the severity of disease activity. In this study the PGA was completed by a specialized physiotherapist (22). The PGA is scored on a visual analog scale. A score of 0 indicates no disease activity and a score of 10 represents the most active disease possible. From this score the children with juvenile DM were divided into active (PGA 2.1–10.0) or inactive (PGA 0.0–2.0) juvenile DM categories. This division allowed for some minor disease activity to be evident in assessment, such as mild skin rash, which would produce a score but indicates that there is minimal functional impairment.

Muscle strength

The assessment of muscle strength was performed using myometry (assessment using a CITEC hand-held dynamometer [CIT Technics, Groningen, The Netherlands] for quantitatively measuring the specific strength of a muscle group) (23). Myometry is a validated tool for measuring very small changes in muscle strength (24). The technique chosen for this study was “break test,” which is most accurate when maximum strength is allowed to build up over 2–5 seconds before the “break” and is completed by a single assessor (25–30).

The muscle groups assessed in the study were a representation of upper limb and lower limb proximal and semidistal muscle groups and included neck flexors, shoulder abductors, hip abductors, quadriceps, and hamstrings. These muscles were all tested in the midrange position against gravity. However, for the myometer to be effective each muscle group had to be able to achieve at least antigravity strength; therefore children with strength below antigravity strength were excluded. The only exception to this was neck flexors because this muscle group would not affect the thigh MRI changes or the ability to complete the exercise program and is an important measure of disease activity.

Magnetic resonance image T2 relaxation time

The magnet used in this project was a 1.5 Tesla Symphony (Siemens, Erlangen, Germany) and the coil used for the imaging of both thighs of each child was the inbuilt body coil. The T2-weighted relaxation mapping sequence or Carr-Purcell-Meiboom-Gill sequence (31) provided the data that allowed the objective assessment of signal abnormality to be achieved. Eight image slices were acquired during each scan at positions through the thigh from the base of the greater trochanters to the level of the superior aspect of the femoral condyles. The other 6 slices were automatically positioned equally between these 2 anatomic locations. Transverse imaging also enabled specific regions of interest to be included on individual muscle groups during the post processing image analysis stage, and this represents the average T2-weighted relaxation time of the tissue within this region of interest. Two consecutive slices were examined to make sure that there were not any significant changes between the 2; the average of these 2 scores were then used in the analysis. The regions of interest identified within each of the 4 T2 map sequences (1 pre- and 3 postexercise) resulted in a total of 8 slices to be analyzed for each subject. The T2 relaxation time was also assessed in different specific muscle groups (anterior, posterior, and medial muscle groups). The muscles included in the posterior muscle group were semimembranus, semitendinus, and biceps femoris; the muscles in the anterior muscle group were vastus lateralis, rectus femoris, and sartorius; and the muscles in the medial muscle group were adductor longus, adductor magnus, and gracilis. The regions of interest were determined and positioned by the radiographer who was blinded to the clinical findings and grouping of the children.

Blood serum muscle enzyme levels

During the initial assessment, the patients were cannulated and a blood sample was obtained for laboratory testing of CK and LDH. These tests of CK and LDH were repeated at the end of the assessments (60 minutes postexercise) to assess any change brought about by the exercise. No blood samples were obtained from control subjects. Normal ranges in our unit for CK are 0–120 units/liter and LDH are 120–750 units/liter.

Design of the study

The children were initially assessed using myometry and the MRI T2-weighted relaxation time gained using the MRI STIR image. Children with juvenile DM also had blood samples obtained to test CK and LDH levels. All children then completed a physiotherapy-designed exercise program (see below). Immediately after completion of the exercises, the children underwent a repeat MRI scan. After the scan the children rested, and at 30 minutes and 60 minutes the children received further MRI scans and myometry assessments of muscle strength. Children with juvenile DM underwent a repeat blood test to measure CK and LDH levels at the completion of all the assessments.

Exercise program

The exercise program was designed by a physiotherapist specialist in pediatric rheumatology and was representative of a program that would be used for children with juvenile DM. The exercises were open-chained exercises including concentric and eccentric muscle work of specific muscle groups, predominantly in the lower limbs. The muscle groups included were anterior muscle groups (knee extensors, quadriceps [vastus medialis, intermedialis, lateralis, and rectus femoris]), medial and lateral muscle groups (hip adductors and abductors), and posterior muscle groups (hip extensors and knee flexors; gluteus maximus and hamstrings). The children completed these exercises against gravity with no other resistance and repeated each exercise 20 times on each leg. The exercise program included straight leg raises in supine position, midrange quads in sitting position, hip abductors and adductors in side lying position, hip extension and knee flexion in prone position, and back extensor lifts and sit ups and heel raises in standing position.

Statistical analysis

Statistical analysis was completed using SPSS version 10.1 for Windows (SPSS, Chicago, IL). Analysis of the populations was completed using frequency and descriptive statistics. To compare the effect of the exercise on the muscles, the subjects were divided into 3 groups: those with active juvenile DM (PGA score >2.1), those with inactive juvenile DM (PGA score ≤2.0), and healthy controls.

It was recognized that the groups were independent of each other and that the mean changes within the groups should be compared. Therefore a 1-way analysis of variance was chosen. Because the specific groups had been planned in advance, an a priori approach was used. This approach assumes that the data is normally distributed and that the samples are drawn from a population of equal variance. Analysis was completed between the groups of active juvenile DM, inactive juvenile DM, and healthy controls. Bonferroni calculation was also performed to allow for the large number of comparisons. To test for statistical significance between the change in CK and LDH levels between the active and inactive juvenile DM groups, nonparametric Mann-Whitney test was used because the total number of subjects was smaller (only children with juvenile DM were tested).

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES

Patient characteristics

A total of 40 children were recruited for the study (20 children with juvenile DM and 20 healthy children). Of the children who completed the study, 10 had active juvenile DM (PGA score >2.1), 10 had inactive juvenile DM (PGA <2.0), and 20 were healthy controls. The demographic data of age, disease duration, mean PGA score, mean CK and LDH levels, and the mean score for the myometry of the neck flexors at the initial assessment are shown in Table 1.

Table 1. Baseline characteristics of the subject groups*
 Active JDM (n = 10)Inactive JDM (n = 10)Control (n = 20)Total (n = 40)
  • *

    Values are the mean (range). Active JDM = active juvenile dermatomyositis; NA = not applicable; PGA = Physician's Global Assessment; CK = creatine kinase; LDH = lactate dehydrogenase.

  • PGA score >2.1 = active disease; <2.0 = inactive disease.

  • Juvenile DM patients only.

Age at disease onset, years6.6 (3.8–11.8)6.9 (2.7–13.3)NA6.6 (2.8–13.3)
Disease duration, years2.2 (0.3–6.7)3.3 (1.3–8.0)NA5.8 (0.3–13.9)
PGA score, 0–104.52 (2.4–6.9)1.1 (0.2–2.0)NA2.81 (0.2–6.9)
Baseline neck myometry, Newtons10.1 (0–32)28.9 (3–55)36.7 (20–82)27.4 (0–82)
Baseline CK, units/liter196 (51–582)261 (31–1,147)NA230 (31–1,147)
Baseline LDH, units/liter1,137 (764–2,085)845 (661–1,224)NA987 (577–1,786)

Effects of exercise.

Blood serum muscle enzyme levels.

There was no statistically significant difference in the levels of CK and LDH before and after the completion of the study protocol in the children with juvenile DM. There was no significant difference between the changes in CK and LDH levels between the children with active or inactive juvenile DM. The mean ± SEM difference in CK levels before and after exercise in active children with juvenile DM was −3.6 ± 5.56 units/liter, and the mean difference in inactive disease was 6.7 ± 8.8 units/liter. The mean difference in LDH levels before and after exercise in children with active disease was 23.1 ± 66 units/liter and the mean difference in inactive disease was −13.8 ± 29.6 units/liter.

Muscle strength changes

Figure 1 shows the mean changes in muscle strength over time in 2 of the different muscle groups measured (hip abductors and knee extensors). There were no statistically significant differences in the change of muscle strength after 60 minutes between the children with active juvenile DM compared with the children with inactive juvenile DM or the healthy children (range of 2-tailed significance test P = 0.067–0.836) in any of the muscle groups. There were no statistically significant changes in strength between the children with inactive juvenile DM and the healthy children after 60 minutes in either their neck flexors (P = 0.898), shoulder abductors (P = 0.061), quadriceps (P = 0.065), or hamstrings (P = 0.849). There was, however, a statistically significant difference in hip abductor strength between the children with inactive juvenile DM and the healthy children (P = 0.002), before and after the exercises, showing that the healthy children lost strength or fatigued after 60 minutes. The children with active disease also showed signs of fatigue, but this was not statistically significant.

thumbnail image

Figure 1. A, Changes in muscle strength after exercise of the hip abductors in children with active juvenile dermatomyositis, inactive juvenile dermatomyositis, and healthy children measured with a hand-held myometer. B, Changes in muscle strength after exercise of the knee extensors in all subjects. Error bars represent 2 SEMs.

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MRI T2-weighted relaxation time changes

The changes over time in the MRI T2-weighted relaxation times are presented in Figure 2. There were no statistically significant differences when comparing the values of the MRI T2-weighted relaxation times before exercise, immediately after, and 60 minutes after the exercises (P = 0.976–0.109) when children with active juvenile DM, those with inactive juvenile DM, and healthy controls were compared.

thumbnail image

Figure 2. A, Changes in mean values of magnetic resonance imaging (MRI) T2-weighted relaxation time over time in healthy children. B,Changes in mean values in children with active juvenile dermatomyositis. C, Changes in mean values of MRI T2-weighted relaxation time over time in children with inactive juvenile dermatomyositis.The mean values in msec of the MRI T2-weighted relaxation time are taken from 2 slices of a sequential set of scans of the thigh pre and post exercise in the children. Error bars represent 2 SEMs. Min = minutes; ant = anterior; post = posterior; med = medial.

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DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES

There have been many concerns about the safety of exercise in the management of juvenile DM, but very few published studies have addressed this issue. This study presents information on the immediate effects of exercise on muscle inflammation in children with juvenile DM compared with the effects in healthy children. It is recognized that the assessment of the degree of muscle inflammation is difficult, but this study uses currently accepted measures of blood serum muscle enzyme levels (CK and LDH), muscle strength, and MRI to assess any changes that may have occurred in response to muscle exercise. The results show that there was no statistically significant change in any of these measures in response to the exercise program in any of the 3 groups of children, except in the assessment of muscle strength of the hip abductors, which showed evidence of fatigue (after exercise) in the healthy children compared with the patients with juvenile DM. This indicates that this physiotherapy-designed exercise program does not immediately increase inflammation assessed at 60 minutes post exercise within the muscles in children with juvenile DM.

For the interpretation of these results, it should be noted that the children with the most severe juvenile DM could not be included in the study. The primary reason for this was that the children with very active disease generally had muscles that were below grade 3 in strength and therefore were unable to undergo myometry and were unable to complete the standardized antigravity exercise program. The exclusion of children with the most active disease does impact the issue of safety of exercise in the treatment of juvenile DM because many professionals are unsure about the treatment for the children with severe active disease. This issue is not directly answered by the study (13).

Open-chain exercises were chosen for the protocol because this type of exercise enables the child to isolate specific muscle groups and specific muscle actions and does not rely upon the weight-bearing capabilities of each child. Also, a previous study (12) used closed-chain exercises only, which are not realistic of a treatment program for children with juvenile DM when used without other types of muscle strengthening techniques.

Muscle inflammation in juvenile DM is patchy, both within the muscle itself and between muscle groups, with anterior muscles thought to be the most common muscle groups affected (32). In this study, it is apparent that the anterior muscle groups in children with juvenile DM as well as healthy children have a higher MRI T2-weighted relaxation time than the posterior and medial muscle groups (Figure 2). Because healthy children have not previously been studied, this difference in the anterior muscles may have been over-interpreted in studies of children with juvenile DM (12).

A previous study reported a change in the MRI after exercise, but this has not been compared with the changes in healthy children before (12). MRI has been shown to measure inflammation in muscle and can provide an assessment of disease activity (5). In this study, there was no statistically significant change in the MRI T2-weighted relaxation time over time in any of the groups and between any of the groups. It is therefore assumed that the changes that did occur did not represent a significant change in inflammation. However, it is also recognized that in assessment of inflammatory response to exercise, a response can be seen up to 48 hours after strenuous exercise. It was not ethically possible to assess the children in this study over a 24-hour period and therefore we do not have data on longer-term changes.

The measurement of muscle force (taken as the myometry scores of muscle strength) is dependent upon many factors, including age and size of the child, cooperation, pain, fatigue, and assessment positioning (33). This effect was minimized by analyzing the change in values. This change in muscle strength represents a change in disease because it is assumed that as inflammation increases, muscle strength or force will decrease; this response can occur over a short period (34). However, a reduction in the myometer scores will also occur if the muscle becomes fatigued and is unable to exert as much force; our results showed that the children with juvenile DM did not fatigue significantly over the study period. This was surprising because inflamed muscles might be expected to fatigue faster than normal muscles. There was a trend in both healthy children and the children in the inactive juvenile DM group to demonstrate an increase in muscle strength over time in all muscle groups except hip abductors. This may be due to an increase in neuromuscular coordination and recruitment of muscle fibers. This effect was not observed to the same degree in the children with active disease. Hip abduction muscles showed evidence of fatiguing in the healthy children but not in the children with juvenile DM. One explanation might be that the children with inactive juvenile DM have a regular home exercise program that works on all muscle groups individually, both eccentrically and concentrically, and that hip abductors are very rarely specifically strengthened in general sports and physical exercise activities in healthy children. Further support for this theory is that unaccustomed eccentric exercise causes rapid-onset muscle weakness and fatigue, yet fatigue does not occur after repeated training has been completed (35). The changes in muscle force described in this study indicate that exercise does not increase muscle inflammation in the short term, and in fact may increase recruitment of muscle fibers and therefore improve muscle function, even in active disease.

The measure of CK and LDH levels is also believed to be a measure of inflammation or muscle damage; however, as other studies have shown, CK and LDH levels are often not an accurate measure of disease activity (2, 36, 37). The LDH and CK levels were not altered by the exercise program applied in this study. However, changes in these measures seen in another study were brought about by strenuous eccentric exercise and occurred between 24 and 48 hours after exercise (8). The exercises performed in our study were not believed to be strenuous or predominantly eccentric, and therefore a delayed response would not be expected. It was also ethically inappropriate in this study to prolong the assessment period of the CK and LDH.

This study begins to address the effect exercise may have on muscles in patients with juvenile DM by assessing the short-term impact that a moderate exercise program has upon the available measures of muscle inflammation. It is important to note that exercise is vital for the repair and growth of muscle, and that lack of exercise and muscle action causes muscle atrophy after a relatively short period of immobility (35). Several studies have also suggested that hypoxia of muscle fibers may have a role in the pathology of juvenile DM and therefore improving circulation to the muscles would be important. Circulation to the muscles is increased by exercise and therefore damage may be decreased if adequate blood and oxygen are supplied to the muscles (38).

Each exercise program should be designed for the individual child, and specific goals need to be identified. During active disease, the aim of treatment should be to maintain muscle length, maintain circulation, and minimize atrophy. Initially this can be achieved by correct positioning of the child and use of active/assisted exercises and by altering the effects of gravity on a muscle group to allow the extremely weak child independent movement and to allow the muscle to function. As disease control is gained by medication, the focus should change to increasing muscle strength and improving muscle endurance. The program should include a combination of concentric muscle work that is progressed by the addition of resistance and moderate eccentric muscle work (39–41). Therefore, we suggest that moderate and controlled combined concentric and eccentric exercise for children with juvenile DM does not increase muscle inflammation. Further research is needed to analyze the longer-term effects of exercise for these children.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES

We would like to thank Prof. R. Wiggins, Professor of Sociology, City University, London, for advice and statistical support during the completion of this project, the parents and children who participated in the study, and the staff at GOSH and ICH who supported the study.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
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