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Benefits of intensive resistance training in patients with chronic polymyositis or dermatomyositis

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Benefits of intensive resistance training in patients with chronic polymyositis or dermatomyositis
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  Benefits of Intensive Resistance Training inPatients With Chronic Polymyositis orDermatomyositis HELENE ALEXANDERSON, 1 MARYAM DASTMALCHI, 2 MONA ESBJO ¨ RNSSON-LILJEDAHL, 3 CHRISTINA H. OPAVA, 1 AND  INGRID E. LUNDBERG 2 Objective.  To investigate the benefits and safety of an intensive muscular training program in patients with chronicpolymyositis (PM) and dermatomyositis (DM).  Methods.  Nine patients with chronic PM or DM (median age 53 years, range 44–61) were included. Assessments of impairment (10–15 voluntary repetition maximum [VRM], the Functional Index 2 [FI-2], the Grippit, and pain rated onthe Borg CR-10 scale), activity limitation (Myositis Activities Profile), and participation restriction (patients’ diseaseimpact on well-being) were performed 4 weeks prior to baseline, at baseline, and after 7 weeks of exercise. A 6-item coreset of disease activity measures was administered and muscle biopsy samples of vastus lateralis were obtained at baselineand after 7 weeks of exercise. Response criteria at an individual level were set for disability and disease activity. Thepatients exercised 3 days per week for 7 weeks on loads allowing 10 VRM.  Results.  On a group level there were no significant differences between assessments at 4 weeks before baseline comparedwith baseline. The group improved significantly regarding 10–15 VRM and FI-2 at 7 weeks compared with baseline (  P  < 0.05). All patients were responders with respect to impairment and 2 were activity limitation responders whereasparticipation restriction remained unchanged in all. Two patients were responders with reduced disease activity and nopatient had signs of increased muscle inflammation in the muscle biopsy sample after 7 weeks of exercise. Conclusion.  Patients with chronic, stable PM and DM can perform this intensive resistive exercise program with beneficial effects on impairment and activity limitation without increased muscle inflammation.KEY WORDS.  Polymyositis; Dermatomyositis; Exercise; Impairment; Activity limitation. INTRODUCTION Polymyositis (PM) and dermatomyositis (DM) are chronic,idiopathic inflammatory myopathies that are characterized by impairment (reduced muscle strength and endurance aswell as fatigue and myalgia) (1,2). Despite the initial favor-able effects of aggressive immunosuppressive treatment inmost patients with PM or DM, a majority develop sus-tained disability (3). The mechanisms for this effect are notfully understood and may vary during different phases of the disease. The inflammation is likely to cause muscleimpairment in the early phase. Secondary metabolic dis-turbances including reduced ATP levels in muscle tissuecould contribute to impairment (4–6). In the late chronicphase, other factors, such as muscle atrophy, steroid my-opathy, and disuse of muscle due to physical inactivity,could also play a role (7).Physical exercise could be one way to counteract severalof the mechanisms that are believed to have a negativeeffect on muscle function in patients with PM or DM.However, this group of patients has been previously dis-couraged from active exercise due to fear of exacerbationof disease activity. This cautious attitude is based on pre-vious studies revealing increased creatine phosphokinaselevels (CPK) and signs of inflammation in muscle tissueafter excessive exercise in healthy individuals (8,9). Sev- Supported by the Vårdal Foundation, Swedish Rheuma-tism Association, Swedish Research Council 2002-74X14045-02A, King Gustaf V’s 80-Year Foundation, ProfessorNanna Svartz Foundation, Magnus Bergvalls stiftelse, Stif-telsen Clas Groschinskys Minnesfond, and the KarolinskaInstitutet Foundation. 1 Helene Alexanderson, RPT, PhD, Christina H. Opava,RPT, PhD: Karolinska Institutet and Karolinska UniversityHospital, Stockholm, Sweden;  2 Maryam Dastmalchi, MD,Ingrid E. Lundberg, MD, PhD: Karolinska Institutet, Stock-holm, Sweden;  3 Mona Esbjo¨rnsson-Liljedahl, PhD: Hud-dinge University Hospital, Stockholm, Sweden.Address correspondence to Helene Alexanderson, RPT,PhD, Department of Physical Therapy, Rheumatology UnitD2:07, Karolinska Hospital, SE-171 76 Stockholm, Sweden.E-mail: helene.alexanderson@karolinska.se.Submitted for publication June 14, 2006; accepted in re-vised form November 30, 2006. Arthritis & Rheumatism (Arthritis Care & Research)Vol. 57, No. 5, June 15, 2007, pp 768–777DOI 10.1002/art.22780© 2007, American College of Rheumatology ORIGINAL ARTICLE 768  eral studies demonstrating the safety of easy-to-moderateexercise programs and efficacy in reducing disability inpatients with PM and DM have been published during thelast decade (10–18), and resistive exercise is now recom-mended in the rehabilitation of these patients (19,20).In healthy individuals, improved muscle function dur-ing strengthening exercise is due to improved neuromus-cular adaptation (21), increased cross-sectional muscle fi- ber area (22,23), changes in fiber type composition (24),and metabolic changes (25–27). Healthy sedentary indi-viduals usually respond to any type of exercise (28,29) andcan attain a 40% increased muscle strength in 4 weeks,whereas longer periods of exercise are necessary to ob-tain the same effects in more trained individuals (23). Anexercise intensity of 40–50% of 1 repetition maximum(1 RM) is sufficient to obtain increased strength in un-trained individuals, whereas 80% of 1 RM is needed formore trained persons (30,31). According to the literature,it appears that untrained individuals benefit from bothsingle- and multiple-set exercise (32) and that it is neces-sary to exercise 2–3 times per week to increase musclestrength (33). In healthy muscle, overlap effects of strengthexercise to improve muscular endurance to some extenthave been described. The resting period between setsshould be 1–2 minutes for isolated muscle groups and 2–3minutes when exercising several joints (23).It has not yet been determined how different types of training affect muscle strength and muscle endurance inpatients with PM or DM. Moreover, it is not knownwhether these patients tolerate and benefit from more in-tensive muscular resistance exercise. The goal of thisstudy was to evaluate the potential benefit of an intensiveresistive muscular training program in patients withchronic PM and DM regarding different aspects of disabil-ity and to ensure the safety of the program with regards toeffect on disease activity. PATIENTS AND METHODS Patients.  All patients meeting the inclusion criteria forPM or DM with regular followup at the rheumatologyclinic at Karolinska University Hospital (Stockholm, Swe-den) were invited to participate (n  29). Inclusion criteriawere as follows: diagnosis of definite or probable PM orDM according to the Bohan and Peter criteria (34), diseaseduration  12 months, and unchanged disease activity andmedication for 3 months. Exclusion criteria were diagnosisof inclusion body myositis, comorbidities preventing vig-orous exercise, severe osteoporosis defined as multiplevertebral fractures, current malignant disease, and exercis-ing more than once per week. Exercise was defined as aphysical activity with the goal to improve fitness (35).Eleven patients accepted the invitation and gave in-formed consent. In the weeks before study entry, 2 patientswere excluded due to flares of their disease. Therefore, 9patients (5 women and 4 men) were included in the study.Five of the patients had a DM diagnosis and 4 had PM. Oneof the patients with PM had also been diagnosed withSjo¨gren’s syndrome. The median age was 53 years (range44–61 years), the median disease duration since diagnosiswas 4.5 years (range 2.7–29 years), and the median pred-nisone dosage was 2.5 mg/day (range 0–7.5). In addition, 6patients were treated with azathioprine, 1 in combinationwith cyclosporin A, and 1 patient was treated with meth-otrexate. Three patients were working full time, 4 wereworking part time, and 2 were retired or on sick leave.Three patients exercised once per week, either aerobics oraquatic exercise. The other 6 patients did not perform anyphysical activity other than activities of daily living andordinary walks. Assessments of impairment.  Patients performed 10–15voluntary repetition maximum (10–15 VRM) for 5 musclegroups: deltoids and quadriceps muscles separately for theright and left sides, biceps/latissimus dorsi and the gas-trocnemius muscles bilaterally, and the abdominal mus-cles. To perform 10–15 VRM, an individual weight loadwas selected that allowed the performance of 10–15 cor-rect repetitions, but not more. This load was   70% of 1VRM.The Functional Index 2 (FI-2) measures muscle endur-ance and comprises 7 functional tasks: shoulder flexionand shoulder abduction separately on the right and leftsides, head lifts in supine position, hip flexion and steptest separately on the right and left sides, and bilateral heellifts and toe lifts. Each task is scored individually as thenumber of correctly performed repetitions. The maximumnumber of repetitions is 60 for all except the 2 latter tasks,for which the maximum number of repetitions is 120 (36).The Borg CR-10 scale, a category scale with ratio prop-erties in which numbers are anchored to verbal expres-sions, was used to assess pain. The Borg CR-10 scaleranges from 0 (no pain) to 10 (very severe pain) (37). Gripstrength was evaluated using the Grippit, which is anelectronic force instrument measuring both maximumforce and mean force in newtons over a 10-second period(38). Activity limitation assessments.  The Myositis Activi-ties Profile (MAP) is a disease-specific questionnaire as-sessing activity limitation in patients with PM or DM. TheMAP is divided into 4 subscales (movement activities,activities of moving around, self-care activities, and do-mestic activities) and 4 single items (social activities,avoiding overexertion, work/school work, and leisure ac-tivities). Each item is scored on a 7-grade scale from 1 (noproblem to do) to 7 (impossible to do). Each subscale isscored as the median of all items included and the singleitems are scored as the actual item score (39). Participation restriction assessment.  Patients’ globalassessment of the overall impact of disease on well-beingwas rated on a 0–10 visual analog scale (VAS), where 0indicates no impact of disease and 10 indicates very severeimpact of disease. Assessments of impairment and activitylimitation/participation restriction were performed by anindependent observer on 3 occasions: 4 weeks prior to baseline, at baseline, and after 7 weeks of exercise. Theseassessments were always performed in the same order andat the same time of day. Intensive Resistance Training in PM and DM   769  Disease activity assessments.  The 6-item core set of dis-ease activity measures developed by the International My-ositis Assessment and Clinical Studies Group (IMACS)includes physician’s and patient’s global assessment of disease activity rated on a 0–10 VAS, the Manual MuscleTest (MMT), the Health Assessment Questionnaire (HAQ),serum levels of CPK (normal values   2.5 and   3.0   cat/liter for women and men, respectively), and extraskeletalmuscle activity (Myositis Intention to Treat Activity Index[MITAX]) (40). The MMT includes assessment of isometricstrength in 8 muscle groups: neck flexors, gluteus mediusand maximus, deltoids, biceps brachii, wrist extensors,quadriceps, and dorsiflexors of the ankle. Each musclegroup is scored from 0 to 10, with a total score varyingfrom 0 to 80 (where 80    full strength). The HAQ com-prises 20 questions divided into 8 categories: dressing andgrooming, arising, eating, walking, hygiene, reach, grip,and other activity. The HAQ is scored from 0 to 3 (where3    unable to do) (41). The MITAX includes 7 organsystems: constitutional, cutaneous, skeletal, gastrointesti-nal, pulmonary, cardiovascular, and muscle. The totalscore is the sum of all organ systems varying from 0 to 63(where 0  no disease activity).Muscle biopsy samples from the vastus lateralis wereobtained using a conchotome under local anesthesia(42,43). The repeated biopsy sample was obtained from thecontralateral side to that obtained before training. The biopsy samples were analyzed by a neuropathologist andthe grade of inflammation was registered as the degree of mononuclear inflammatory cell infiltrates according to a4-grade scale from 0 (no inflammatory cells) to 3   (pro-nounced cellular infiltration). All disease activity mea-sures were performed 1 week prior to baseline and 1 weekafter completing the exercise period. The exercise program.  Patients exercised 3 days perweek for 7 weeks at the physical therapy department atKarolinska University Hospital. A physical therapist su-pervised all patients individually on all exercise occa-sions. The patients warmed up on either an ergometercycle or a treadmill for 10 minutes at 50% of their indi-vidual estimated maximal heart rate. After warming up,patients performed a 45-minute exercise program with aload of their individual 10 VRM in 5 muscle groups: del-toid muscles by shoulder flexion/abduction with freeweights, the quadriceps by knee extension in sitting posi-tion with weight cuffs around the ankles, the latissimusdorsi/biceps muscles and the gastrocnemius in a trainingapparatus, and the trunk muscles by performing situpswith/without weight cuffs placed on the chest. These ex-ercises were performed in 3 sets separated by 90-secondrests. The program ended with 5 minutes of stretching.During the first week all patients exercised at 50% of their10 VRM performing 15 repetitions of each exercise in 3sets. During the following 2 weeks, the resistance was Table 1. Impairment measures at 4 weeks prior to baseline, at baseline, and after 7 weeks of exercise in 8 patients*Variables4 weeks prior (n  8)Baseline(n  8)7 weeks(n  8)  P   value baselinevs. 7 weeks 10–15 VRM, muscle strengthDeltoid, right, kg 4.5  3.1 4.7  3.1 6.9  4.0   0.01Deltoid, left, kg 4.5  3.1 4.6  2.9 6.3  3.7   0.05Quadriceps, right, kg 14.4  3.6 13.1  2.9 18.9  5.7   0.05Quadriceps, left, kg 14.1  3.8 13.1  2.9 19.0  5.7   0.01Latissimus dorsi/biceps, kg 51.3  15.3 53.1  16.0 57.5  30.6 NSGastrocnemius, kg 101.3  20.3 103.8  19.8 138.7  26.7   0.01Abdominal muscles, kg 0.6  1.7 1.2  1.6 6.5  7.1   0.05FI-2, muscle enduranceShoulder flexion, right (0–60 reps) 31.6  20.6 33.8  18.3 43.6  23.0   0.05Shoulder flexion, left (0–60 reps) 28.3  18.3 29.3  15.8 43.6  22.0   0.05Shoulder abduction, right (0–60 reps) 31.1  20.5 37.9  21.1 38.1  21.8 NSShoulder abduction, left (0–60 reps) 30.0  19.1 34.4  20.0 45.6  22.4 NSHead lift (0–60 reps) 14.4  13.8 12.8  11.1 15.5  13.4 NSHip flexion, right (0–60 reps) 23.8  20.4 27.0  15.7 30.2  19.0 NSHip flexion, left (0–60 reps) 22.1  18.1 26.4  16.1 28.4  20.6 NSStep test, right (0–60 reps) 37.1  23.3 47.4  18.9 43.4  23.4 NSStep test, left (0–60 reps) 38.9  22.9 46.9  18.9 49.3  19.9 NSHeel lift (0–120 reps) 74.6  46.5 71.6  44.9 76.1  40.4 NSToe lift (0–120 reps) 49.3  41.1 50.3  44.7 69.1  42.6 NSGrippit, grip strengthMax, right, newtons 284.0  121.9 263.5  108.7 283.5  103.6 NSMax, left, newtons 273.0  101.0 268.5  105.0 261.1  87.6 NSMean, right, newtons 245.3  101.9 240.3  99.0 254.0  85.5 NSMean, right, newtons 237.1  85.0 238.5  93.4 232.6  74.1 NSMuscular painBorg CR-10 scale, median (range) (0–10) 2.5 (0.0–3.0) 1.3 (0.0–3.0) 1.3 (0.0–3.0) NS * Valuesarethemean  SDunlessotherwiseindicated.VRM  voluntaryrepetitionmaximum;NS  nonsignificant;FI-2  FunctionalIndex2;reps  repetitions. 770  Alexanderson et al   gradually increased to represent 100% of their individual10 VRM performed in 10 repetitions per set. After 3 and 5weeks of exercise, respectively, new 10 VRM tests for eachmuscle group were performed and the exercise loads wereadjusted. Ethical scrutiny.  The local ethical committee at theKarolinska Hospital, Stockholm, approved this study andall patients gave their informed consent to participate. Statistical analysis.  For analysis on a group level, re-peated-measures analysis of variance (ANOVA) was usedto compare ratio data for the 3 evaluation occasions andthe Friedman ANOVA was used for ordinal data. The levelof significance was set to  P   less than 0.05.All results were also analyzed individually for eachpatient, and improvement criteria according to Paulus et al(44) for measures of muscle impairment, activity limita-tion, and participation restriction were applied. Thus,changes of at least 20% in  1 test/task of the 10 VRM, theFI-2, and the Grippit, respectively, were considered asclinically relevant. For variables producing ordinal data,changes of 2 scale points were considered clinically im-portant for the MAP (  1 subscale/item) and the BorgCR-10 scale, and a change of 20 mm was considered clin-ically important for the VAS. Patients were consideredresponders if they improved in 2 of 4 impairment mea-sures (10–15 VRM, FI-2, Grippit, Borg CR-10), in 1 activitylimitation measure (MAP), or in 1 participation restrictionmeasure (patients’ overall assessment). Regarding diseaseactivity, improvement criteria developed by the IMACS forpatients with myositis were used (45), in which a re- Figure 1.  Changes in 10 voluntary repetition maximum (VRM) after 7 weeks of exercise compared with 4 weeks before baseline and baseline for  A,  musculus deltoids, right side,  B,  musculus deltoids, left side,  C,  musculus quadriceps, right side,  D,  musculus quadriceps,left side,  E,  musculus latissimus dorsi/biceps (patient H not assessed),  F,  musculus gastrocnemius, and  G,  trunk muscles. *   20%improvement at 7 weeks compared with baseline. **  40% improvement at 7 weeks compared with baseline. Intensive Resistance Training in PM and DM   771  sponder should improve by   20% in at least 3 of the 6parameters in the core set with no more than 2 parametersworsened by   25% (which cannot include the MMT as-sessed muscle strength). RESULTS After 3 weeks, 1 patient with PM reported influenza-likesymptoms and was excluded from the exercise program.The results are therefore based on the 8 remaining pa-tients. The program was well tolerated. Of the possible 21exercise occasions, the patients exercised on a median of 19 occasions (range 14–21). One patient went on a 1-weekholiday during the study, and therefore only exercised for6 weeks. Medication remained unchanged in all patientsand no patient changed any lifestyle factors such as phys-ical activity, smoking, or food intake.All patients experienced mild delayed-onset musclesoreness for 1 or 2 days after some exercise occasions. Onepatient experienced increased joint swelling and tender-ness of the metacarpophalangeal joints and was thereforeunable to perform the latissimus dorsi/biceps exercise dur-ing the last 2 weeks. This patient also reported pain in asternocostal joint and was not able to perform the situptests of the 10–15 VRM and FI-2 at 7 weeks. Anotherpatient experienced diffuse tendinitis pain of the shoul-ders and performed the deltoid exercises at   80% of the10 VRM during the entire exercise period. Impairment changes.  No significant differences oc-curred in the group during the 4 weeks prior to baseline.The group improved significantly at 7 weeks comparedwith baseline ( P   0.05) regarding the 10–15 VRM for allmuscle groups except for the latissimus dorsi/biceps mus-cles and in muscle endurance of shoulder flexion bilater-ally as assessed by the FI-2 ( P   0.05) (Table 1).All 8 patients were responders according to our criteriafor impairment reduction. All patients improved by  20%of the 10–15 VRM compared with baseline (Figures 1 and2) with improvements for all muscle groups ranging from20% to 900% (Figure 2). No patient had deterioration inany of the muscle groups.All patients responded at the   20% level set for theFI-2; however, 5 patients worsened in a few tasks (Table 2).Only 1 patient responded according to the criteria set formaximum and mean score of the Grippit on the right side,with 34% and 45% improvements, respectively. No pa-tient improved by  2 scale points in pain assessed by theBorg CR-10. No patient experienced   20% deteriorationin grip strength or pain. Changes in activity limitation and participation restric-tion.  The group did not improve significantly in activitylimitation or participation restriction (Table 3). Two pa-tients were responders according to our criteria for re-duced activity limitation in the MAP subscales movementand activities of moving around and the single item socialactivities. One patient had a decrease of   2 scale points inthe MAP single item leisure activities. No changes of   20mm on the VAS for overall disease impact occurred in anypatient. Disease activity.  On a group level, there was a statisti-cally significant improved MITAX score at 7 weeks com-pared with baseline ( P     0.05), whereas all other diseaseactivity measures remained unchanged. Two patients wereconsidered as responders fulfilling the IMACS improve-ment criteria for disease activity (Table 4). One patient Figure 2.  Number of responders at  20%, 40%, 60%, and 100%level of 10–15 VRM of deltoids and quadriceps on the right side,latissimus (lat.) dorsi/biceps, gastrocnemius, and trunk musclesafter 7 weeks of exercise compared with baseline. Table 2. Number of tasks improving or worsening according to the Functional Index 2*Patient,sex DiagnosisTasks improving > 20%, no. Tasks worsening > 20%, no. (task) A, male DM 2 1 (heel lift)B, female DM 3 4 (shoulder flexion, right; hip flexion, right;step test, right; heel lift)C, female PM 10 0D, male DM 2 0E, female DM 1 0F, male DM 5 4 (hip flexion, right and left; step test, rightand left)G, male PM 7 1 (shoulder abduction, right; step test, right)H, female PM 5 2 (shoulder abduction, right; hip flexion, right) * DM  dermatomyositis; PM  polymyositis. 772  Alexanderson et al 
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