Safety and efficacy of submaximal eccentric strength training for a subject with polymyositis

Authors

  • Michael O. Harris-Love

    Corresponding author
    1. Mark O. Hatfield Clinical Research Center, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland
    • Physical Therapy Section, Rehabilitation Medicine Department, Mark O. Hatfield Clinical Research Center, National Institutes of Health, Department of Health and Human Services, 10 Center Drive, Building 10, Room 1-1469, Bethesda, MD 20892-1604
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  • The opinions and information contained in this article are those of the author and do not necessarily reflect those of the National Institutes of Health or the Department of Health and Human Services.

Introduction

Polymyositis (PM) is a subset of idiopathic inflammatory myopathy (IIM), often associated with proximal muscle weakness and various autoimmune and connective tissue disorders. Histopathologic findings in PM include endomysial infiltration of CD8+ lymphocytes affecting muscle fibers with major histocompatibility complex class I (MHC1) expression (1). The resulting muscle weakness is typically addressed with pharmacologic and rehabilitation interventions (2). Therapeutic exercise serves as a useful adjunct in the treatment of PM (3), but optimal modes of exercise have not been established (4).

Some investigators caution against the use of eccentric exercise as a mode of intervention for individuals with IIM because of concerns about exercise-induced injury associated with maximal eccentric contractions (5). However, it has been demonstrated that eccentric exercise can be safely utilized by various patient populations, and may have greater efficacy than concentric exercise (6). No study to date has reported the efficacy or effectiveness of a submaximal eccentric exercise in subjects with IIM.

This case report describes a 12-week submaximal eccentric training program for an adult with PM. Measures of the patient's peak torque, subjective pain level, joint passive range of motion (ROM), sit-to-stand performance, and serum muscle enzymes were used to monitor his response to the submaximal eccentric exercise program. The method used to progress eccentric exercise intensity, and the patient's response to submaximal eccentric exercise are presented.

Case report

The patient, a 64-year-old man diagnosed with PM one year before his referral for physical therapy, presented with the primary symptoms of lower extremity weakness and repeated falls (1/week). He was initially diagnosed with inclusion body myositis, based on his age at disease onset (59 years old) and the asymmetry of his knee extensor strength impairment. However, his rheumatologist confirmed the diagnosis of PM after finding evidence of primary inflammation (CD8+/MHC1 complex) upon review of a followup muscle biopsy.

The patient's medication schedule one year prior to his physical therapy referral included oral prednisone (60 mg/day) for 3 weeks, followed by a taper resulting in a 4-month course of corticosteroid therapy. His trial of prednisone did not improve his muscle strength and he declined the use of methotrexate and other immunosuppressive agents. He took no prescription medications during the physical therapy intervention period.

The patient's manual muscle test (MMT; Kendall 10-point scale) scores for his knee extensors were 7 of 10 on the right side and 10 of 10 on the left side prior to any exercise intervention. Mild, bilateral strength impairment was also noted in his hip extensors and ankle dorsiflexors (MMT was 8 of 10). The patient's joint ROM was within normal limits with the exception of his ankle, which was limited to 5° of dorsiflexion bilaterally. Light touch sensation was intact in the patient's distal lower extremity, the sharpened Rhomberg maneuver did not elicit any loss of balance, and there were no vision or hearing deficits noted. The patient was independent in all transfers, activities of daily living, and ambulation.

The patient's initial program of physical therapy included 6 weeks of supervised, isotonic strengthening (2–3 sets for 12 repetitions) for his hip extensors, knee extensors, and ankle dorsiflexors 2–3 times per week. He transitioned to a home-based program and continued this exercise regimen over the next 4.5 months. A followup MMT was administered prior to the patient's discharge at month 6. The patient's MMT scores for hip extensors, ankle dorsiflexors, and right knee extensors increased to 9 of 10.

However, the patient reported that his lower extremity strength gains reached a plateau 6 months following discharge from physical therapy. He stated that this nominal response to exercise continued, despite his adherence to the home-based program. Consequently, his rheumatologist issued a second referral for physical therapy, and a trial of submaximal eccentric exercise was initiated due to the patient's decreased training response to the isotonic training program.

Initial isometric strength assessment of his knee extensors revealed a 57.8% peak torque deficit on the right side in comparison with the left side values (16.2 foot-pounds [ft-lbs] and 38.4 ft-lbs, respectively). Therefore, the patient began a 12-week submaximal eccentric training regimen for his right knee extensors using an isokinetic dynamometer (Biodex Medical Systems, Shirley, NY). All training occurred with the patient in a seated position (in 90° of hip flexion) with knee extension and flexion ROM between 10° and 100°.

The submaximal exercise regimen was divided into 3 phases: familiarization, acclimatization, and progression. Week 1 of training was the familiarization phase of the exercise regimen. The purpose of this phase of training was to introduce the patient to the visual feedback provided by the dynamometer, which corresponds with the torque targets used to guide exercise intensity. Training loads were limited to 2 sets of exercise (45°/s, 0.79 rads/s) at 40–50% of the estimated eccentric one repetition maximum (1 RM). Eccentric muscle contractions are capable of producing torques approximately 40% higher than concentric muscle contractions (7). Therefore, the following equation was used to calculate the estimated eccentric 1 RM:

1 RMecc = (1 RMcon)(1.4)

where ecc = eccentric and con = concentric.

As a result, the 40–50% of the estimated eccentric 1 RM used in the familiarization phase is approximately 80–90% of the concentric 1 RM.

The acclimatization phase of the exercise regimen occurred during weeks 2 and 3. The purpose of this phase of training was to prepare the patient to eventually use training loads of sufficient intensity to induce a training response. Low volume eccentric training results in the “repeated bout effect” that describes the role of prior eccentric contraction history in protecting against subsequent eccentric exercise-induced muscle injury in untrained individuals (8). Training loads during this period were 2 to 3 sets of exercise (60°/s, 1.05 rads/s) at 50–60% of the estimated eccentric 1 RM. Weeks 4–12 comprised the progression phase of the exercise regimen. Initial training loads used during this phase (60°/s and 90°/s, 1.05 rads/s and 1.58 rads/s) were 70% of the estimated eccentric 1 RM and exercise intensity was progressed as shown in Figure 1.

Figure 1.

Exercise intensity algorithm for the progression phase of the eccentric exercise intervention. The progression phase (weeks 4 to 12) of the intervention proceeds the familiarization and acclimatization to submaximal eccentric exercise. The target torque at week 4 is 70% of the estimated eccentric 1 RM and is subsequently adjusted after each set of exercise based on the magnitude of fatigue derived from the torque-time curves. This algorithm allowed the therapist to gradually increase or decrease the exercise intensity based on the performance of the patient. *The patient was permitted to increase his target torque a maximum of 1 time per exercise session. ECC 1 RM = eccentric 1 repetition maximum; ft-lbs = foot-pounds of torque.

Measures of exercise-induced training damage include an acute loss of muscle torque, pain, decreased ROM, and elevated serum muscle enzyme levels (8). Therefore, outcome measures included peak torque of the knee extensors, estimates of delayed-onset muscle soreness (DOMS), passive ROM at the right knee joint, and lowest sit-to-stand height. Serum enzyme levels associated with IIM disease activity were obtained 6 weeks prior to training and 1 week following the cessation of the intervention period. These laboratory values were obtained as part of the patient's customary medical followup visits. A priori criteria to prematurely end the training program included a decrease in 1 RM torque (concentric or isometric) exceeding 15%, a decrease in target torque for 2 consecutive training sessions, pain of 5 or greater on a 0–10 visual analog pain scale (VAS), or a decrease of knee passive ROM (secondary to edema) >15%.

The patient averaged 2 exercise sessions per week during the 12-week period. The patient's weekly VAS rating of his DOMS was consistently 0 of 10, and he did not experience an exacerbation of his IIM based on serum muscle enzyme levels during his eccentric training regimen (Table 1). Furthermore, the weekly goniometric measures of right knee joint passive ROM remained unchanged during the training period (0°–125°).

Table 1. Changes in serum muscle enzymes in an adult patient with myositis before and after a 12-week eccentric training regimen
 Preexercise values units/literPostexercise values units/liter
Aldolase118
Creatine phosphokinase (total)619483
Serum glutamic pyruvic transaminase4241
Serum glutamic oxaloacetic transaminase4438
Lactate dehydrogenase209195

Peak knee extensor torque was measured at 0°/s (0 rads/s; 3 isometric contractions) and 180°/s (3.15 rads/s; 5 isokinetic concentric contractions) every 3 weeks during the intervention period. The posttraining isometric and isokinetic peak torque values increased by 48.8% and 52.6%, respectively, when compared with pretraining values (Figure 2). The patient's ability to independently rise from a low surface (9) improved from 55 cm at week 1 to 44 cm at week 12; however, the self-reported rate of falls remained unchanged.

Figure 2.

Peak right knee extensor torque values obtained at 3-week intervals throughout the submaximal eccentric exercise intervention period. ft-lbs = foot-pounds; deg = degrees; s = second.

Discussion

The patient had increased right knee extensor strength without any signs of muscle injury following a submaximal eccentric training regimen. However, he may have achieved similar strength gains with a progressive concentric exercise program supervised by a physical therapist. The patient's diminished response to isotonic exercise may have been related to inadequate exercise intensity or an exacerbation of his disease activity. Additionally, this case was an atypical clinical presentation of PM, therefore the patient may have had another form of IIM.

Despite the role of eccentric contractions in common functional activities such as walking, or descending a flight of stairs (10), use of this contraction mode for strength training does not have widespread clinical acceptance (5). This is perhaps a reflection of the research literature describing increased exercise-induced injury associated with maximal eccentric contractions. Maximal eccentric contractions have been linked to increased cellular permeability secondary to sarcolemmal injury, degradation of the structural proteins titin and nebulin, elevated serum levels of creatine kinase, and impairment of excitation-contraction coupling because of disrupted t-tubules (8, 11–13).

Nevertheless, eccentric exercise continues to hold promise for rehabilitation and sport training regimens because of its potential benefits. Compared with concentric muscle contractions, eccentric muscle contractions generate approximately 40% higher torque, produce greater strength gains, and require a lower rate of oxygen consumption (7, 10). The strength gains derived from eccentric training are most apparent during eccentric contractions, but significant training effects also transfer to concentric (8) and isometric (7, 14) contractions. Additionally, the studies by Paddon-Jones et al (8) and LaStayo et al (10) suggest that adaptive strengthening to eccentric exercise can occur without muscle injury. The apparent protective effect of initial submaximal resistance exercise, coupled with the efficacy of low-volume eccentric contractions (8), comprise important elements of a safe eccentric training regimen.

The relative benefit of eccentric training for individuals with muscle disease remains an open question, as it has been the subject of only one research study. Kilmer et al (15) investigated the effect of a single bout of high-intensity eccentric elbow flexion in 14 subjects with progressive muscular dystrophy and 18 healthy control subjects. Post-exercise measures of concentric peak torque, serum creatine kinase, elbow ROM, arm circumference (to assess acute edema), and DOMS depicted a similar injury response between both groups. However, the magnitude of the injury response was greater for the control group at 3 and 7 days post-exercise. The researchers speculated that this finding might reflect the positive relationship between maximal eccentric torque levels and indices of muscle damage (15). Their investigation utilized maximal eccentric contractions for one bout of exercise. Therefore, the effects of submaximal eccentric exercise over longer periods of time in subjects with muscle disease cannot be inferred from the study results.

This was the first report to describe the training response of a patient with PM following a submaximal eccentric training regimen. The patient exhibited improved strength and sit-to-stand performance without experiencing an exacerbation of his PM. The clinical observations from this account suggest that this intervention method merits additional study. Future investigations may determine the utility of the exercise progression algorithm described in this case report, and compare the efficacy of isotonic and eccentric training regimens for people with IIM.

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