Incorporating eccentric muscle activity into therapeutic exercise programs.

Isotonic and isometric muscle activities inherently occur during functional movements. Functional, isotonic activities consist of concentric and eccentric phases of muscle activation. Concentric contractions are synonymous with muscle shortening as the muscle performs “positive work,” whereas eccentric actions happen while the muscle elongates under tension and are often referred to as “negatives” because work occurs in the opposite direction. Eccentric actions are associated with delayed-onset muscle soreness and potentially play an etiological role with repetitive injuries. Therefore, many clinicians perhaps do not emphasize them when prescribing therapeutic exercises. The purpose of this article is to present the attributes of eccentric muscle activity and review current evidence supporting their incorporation into therapeutic exercise programs.

Activation and Force-Production Differences

Electromyographic activity (EMG) is different between eccentric and concentric muscle actions.^1,2 Eccentric actions typically result in less EMG amplitude than concentric contractions for the same relative level of force production. A current theory is that motor-neuron-firing rates decrease during eccentric actions, as opposed to a reduction of recruited motor units, and this results in less EMG amplitude.³ Mean electrical frequencies increase during eccentric actions, however, which suggests preferential recruitment of fast-twitch motor units.¹

Maximal eccentric activation of a muscle or muscle group produces significantly more force than concentric contractions due to several reasons. Some of these include the possibility of selective activation of fast-twitch muscle fibers during eccentric activation,¹ energy absorption by series and parallel elastic components, and altered motor-neuron-firing rates.³ Furthermore, resistance training that includes eccentric activity improves strength and hypertrophy relative to concentric-only training.⁴

Eccentric actions are less vulnerable to fatigue and are relatively more economical than concentric contractions.² Torque degradation within a set of multiple, maximal voluntary contractions is greater during the concentric phase of movement.² Also, the metabolic costs associated with concentric contractions are substantially more than eccentric actions during exercise of the same relative intensity.⁵

Eccentric Activity and Muscle Adaptation

Eccentric activity induces microtrauma within muscle tissue. The resulting microtrauma, if severe enough, causes “z-line streaming,” which is an irregular appearance of the sarcomere under micrographic examination. Microtrauma associated with eccentric muscle activity most often occurs in individuals unaccustomed to eccentrics and is associated with delayed-onset muscle soreness. There are several manifestations of the microtrauma accompanying eccentric actions that include decreased range of motion and muscle strength; and increased levels of pain, serum muscle proteins, and visible abnormalities on ultrasound or magnetic resonance imaging.⁶ These signs and symptoms of microtrauma initiate the inflammation process to repair the affected muscle tissue.

The degree of microtrauma incurred depends upon the muscle length during the eccentric bout and the specific muscle group exercised. Longer muscle lengths are associated with greater amounts of muscle damage, because increased intramuscular tension affects the susceptibility to microtrauma.⁶ Various muscle groups may be more predisposed to incurring microtrauma, as elbow flexors appear to be more susceptible than knee extensors.6 This appears to be related to the functional requirements of the various muscle groups. For example, the lower extremities are relatively accustomed to eccentric activity, because repetitious daily activities such as walking, descending stairs, and sitting down into a chair all require eccentric activation.

Consistent training with eccentric actions, however, induces muscle-tissue adaptation that increases resiliency against subsequent microtrauma. This is known as the “repeated bout effect,” and it may offer protection with as little as one exercise session.⁷ Relative protection occurs in the form of enhanced recovery and reduced damage from subsequent eccentric exercise. This window may last 8 weeks, although some aspects of protection persist at 12 weeks following the initial bout.8 Improvements in muscle soreness, range of motion, and strength; and reduced serum muscle proteins are among the benefits of the repeated bout effect.

Mechanisms of protection by the repeated bout effect are still not clear. However, there is evidence to support several beneficial responses that include cellular, mechanical, and neural adaptations. Muscle-tissue modification plays an important role in ameliorating subsequent damage, as stress-susceptible muscle cells may be remodeled or regenerated in the days following eccentric activity. The addition of sarcomeres in series or longitudinally within a myofibril and increased muscle-protein anabolism partially account for the remodeling that occurs from eccentric training.9 

Training specificity also influences adaptive responses associated with the repeated bout effect. Training eccentrically at both long and short muscle lengths provides relative protection against subsequent microtrauma encountered during exercise at long muscle lengths.⁶ Shorter muscle lengths offer effective protection. However, there is only about 50% to 70% attenuation of symptoms, compared to training at longer muscle lengths.6 Nonetheless, since the degree of microtrauma depends upon muscle length, eccentric exercise at shorter lengths induces less damage and yet provides some protection against subsequent damage incurred during exercise at longer lengths. This has important implications for inoculating untrained individuals against severe muscle damage in subsequent exercise bouts.

Eccentric Activity and Tendinopathy

Tendinopathy, especially in a chronic state, is associated with tissue degradation. It seems counterintuitive that eccentric actions associated with tissue microtrauma would benefit tendon degeneration. However, Stanish et al suggested the necessary inclusion of eccentric activity for tendon injuries in 1986, and the amount of clinical evidence to support this notion is increasing.¹⁰ It appears that eccentric actions promote optimal remodeling and increased tissue resilience in tendons affected by tendinopathy, and these physiological adaptations result in diminished neovascularization, reduced pain, improved strength, and earlier return to functional activities.^11-16

Tendinopathies may theoretically develop in any tendon, but there is evidence to suggest that degradation most often develops in regions of tenuous blood supply.¹⁷ Neovascularization is the growth of “new” vasculature into regions that normally have poor blood supply, and its role with tendinopathy pathogenesis is not well understood. It is possible that various chemical mediators signal tissue damage and the body attempts to bring more blood, via angiogenesis, to the affected area to expedite the healing process. The problem, however, is that neural structures concomitantly appear with neovascularization, and this partially accounts for increased pain perception.¹⁸ Eccentric training, however, appears to reverse neovascularization by an unknown mechanism.14 It is possible that tendon remodeling and subsequent healing associated with eccentric training diminishes cellular mediators that promote neovascularization, and thus, the stimulus for angiogenesis is diminished.

Eccentric exercise may benefit tendinopathies in various regions of the body. Substantial evidence now exists for the Achilles tendon, and emerging findings support the inclusion of eccentric exercise for the supraspinatus and patellar tendons.

Achilles tendinopathy affects both physically active and sedentary individuals, but both groups appear to respond favorably to eccentric training.^11,15 Controlled studies vary in duration. However, 6 weeks of eccentric training appear to be sufficient to decrease pain and improve function, and the effects last for at least 1 year.¹⁵ In addition to decreasing symptoms of pain, 12 weeks of eccentric training decreases neovascularization and promotes normal structure of the midportion of the Achilles tendon.14 Eccentric training exercises for Achilles tendinopathy are commonly performed in weight-bearing with the ball of the foot on a step so that the foot may move from concentric plantar-flexion into full dorsiflexion during the eccentric movement.

The exercise is performed by the following sequence: 1) The patient performs plantar-flexion “heel raises” using both extremities or only the unaffected leg during the concentric phase; and 2) At the top of the raise (full plantar-flexion), the patient lifts the unaffected lower extremity to allow full weight-bearing on the affected leg, which then controls the eccentric descent into full dorsiflexion (Figures 1 and 2, page 23). The patient performs the above exercise in full knee extension and also with partial knee flexion.11,15 

It is not uncommon for patients with Achilles tendinopathy to experience significant soreness from the eccentric exercise bout.¹¹ However, Roos et al recommend a gradual progression into the exercise regimen for patients with Achilles tendinosis to minimize the soreness that accompanies eccentric training.¹⁵ The authors recommend using one set of 15 repetitions for the first 2 days, increasing to two sets of 15 repetitions for days 3 and 4, and then three sets of 15 repetitions for days 5 through 7.15 Additionally, the patient performs the activities with only the extended knee during the first week and then adds knee flexion for subsequent weeks. Note that the patient performs these at least once per day, although study designs typically include a frequency of twice per day for a duration of 12 weeks.^11,15

Patellar tendinosis, or jumper’s knee, may be associated with tensile strain from excessive loading or impingement from the inferior pole of the patella against the patellar tendon during knee flexion.¹⁹ Preliminary studies indicate that eccentric training of 12 weeks’ duration improved pain scores on a visual analog scale, allowed the athletes to return to jumping activities, and the benefits persisted at 12 months follow-up.¹⁶ The authors recommend using a decline board angled at 25º from which patients perform unilateral squats.16 A patient performs this exercise by having the affected extremity eccentrically control movement into hip and knee flexion during the descent phase, whereas the unaffected extremity produces the concentric movement during knee and hip extension. One drawback to this study was the lack of a randomized control. However, the preliminary results are promising for including eccentric actions for the treatment of patellar tendinopathy.

The supraspinatus tendon is particularly vulnerable to degeneration, and its tissue degradation appears to increase linearly with age. Partial explanation for the susceptibility of the supraspinatus to degeneration may stem from the lack of vascularity close to its insertion on the humeral head, but this theory has been criticized.¹⁹ Eccentric activity may offer some benefit to patients with supraspinatus tendinopathy, although the results are not as strong compared to the Achilles-treatment regimen.¹³ Preliminary results from a pilot study of nine patients revealed that five of them improved enough by the end of 12 weeks’ training to avoid having corrective shoulder surgery.¹³

Isolated eccentric activities for the supraspinatus and deltoid muscles are more difficult to perform, and the authors incorporated the use of a pulley system with an arm sling to support the affected arm. This exercise is performed by the following sequence: 1) The unaffected upper extremity pulls the affected extremity into elevation within the scapular plane with full glenohumeral internal rotation (this movement replicates the traditional empty can exercise); then 2) The affected upper extremity eccentrically lowers the arm to the starting position. Patients performed this activity, despite the presence of pain, for three sets of 15 repetitions, twice per day, 7 days per week, for 12 weeks.¹³ As strength improves and pain subsides, resistance is progressed to reach a new level of discomfort. It is interesting to note that all five patients reporting improvement also had satisfactory results at 12-month follow-up.13 Furthermore, some of these patients had significant pathologies, some of which include a type III (hooked) acromion, bone spurs, and a partial rupture of the supraspinatus.

An important caveat about eccentric training is the necessary motivation required to perform the exercises despite the pain and discomfort associated with treatment. Although some authors advocate modifying eccentric protocols to minimize delayed-onset muscle soreness, most suggest that the exercises should be painful to perform.^11-13,15,16 Furthermore, performing the exercises twice per day for three sets of 15 repetitions requires discipline, and many patients may not comply with this regimen.

In conclusion, eccentric muscle actions induce various adaptations to skeletal muscle and tendon structure. These adaptations are beneficial for strength gains, hypertrophy, and resiliency against subsequent damage from eccentric exercises. Additionally, evidence is emerging that advocates the inclusion of eccentric exercise in tendinopathy-treatment regimens. More research is needed in the form of randomized controlled trials to determine the specific benefits of eccentric training for different tendinopathies.

R. Barry Dale, PT, PhD, SCS, ATC, CSCS, is an assistant professor in the Department of Physical Therapy at the University of South Alabama, Mobile. His primary teaching and research areas are related to exercise physiology and sports medicine. He may be reached at bdale@usouthal.edu.

References

1. McHugh MP, Tyler TF, Greenberg SC, et al. Differences in activation patterns between eccentric and concentric quadriceps contractions. J Sports Sci. 2002;20:83–91.

2. Tesch PA, Dudley GA, Duvoisin MR, et al. Force and EMG signal patterns during repeated bouts of concentric or eccentric muscle actions. Acta Physiol Scand. 1990;138:263–271.

3. Coburn JW, Housh TJ, Malek MH, et al. Mechanomyographic and electromyographic responses to eccentric muscle contractions. Muscle Nerve [epub ahead of print]. January 24, 2006.

4. Hather BM, Tesch PA, Buchanan P, et al. Influence of eccentric actions on skeletal muscle adaptations to resistance training. Acta Physiol Scand. 1991;143:177–185.

5. Perrey S, Betik A, Candau R, et al. Comparison of oxygen uptake kinetics during concentric and eccentric cycle exercise. J Appl Physiol. 2001;91:2135–2142.

6. Nosaka K, Newton M, Sacco P, et al. Partial protection against muscle damage by eccentric actions at short muscle lengths. Med Sci Sports Exerc. 2005;37:746–753.

7. McHugh MP. Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports. 2003;13: 88–97.

8. Nosaka K, Newton MJ, Sacco P. Attenuation of protective effect against eccentric exercise-induced muscle damage. Can J Appl Physiol. 2005;30:529–542.

9. Ingalls CP, Wenke JC, Nofal T, et al. Adaptation to lengthening contraction-induced injury in mouse muscle. J Appl Physiol. 2004;97:1067–1076.

10. Stanish WD, Rubinovich RM, Curwin S. Eccentric exercise in chronic tendinitis. Clin Orthop Relat Res. 1986(208): 65–68.

11. Alfredson H, Pietila T, Jonsson P, et al. Heavy-load eccentric calf muscle training for the treatment of chronic Achilles tendinosis. Am J Sports Med. 1998;26:360–366.

12. Jonsson P, Alfredson H. Superior results with eccentric compared to concentric quadriceps training in patients with jumper’s knee: a prospective randomised study. Br J Sports Med. 2005;39:847–850.

13. Jonsson P, Wahlstrom P, Ohberg L, et al. Eccentric training in chronic painful impingement syndrome of the shoulder: results of a pilot study. Knee Surg Sports Traumatol Arthrosc. 2006;14:76–81.

14. Ohberg L, Alfredson H. Effects on neovascularisation behind the good results with eccentric training in chronic mid-portion Achilles tendinosis? Knee Surg Sports Traumatol Arthrosc. 2004;12:465–470.

15. Roos EM, Engstrom M, Lagerquist A, et al. Clinical improvement after 6 weeks of eccentric exercise in patients with mid-portion Achilles tendinopathy—a randomized trial with 1-year follow-up. Scand J Med Sci Sports. 2004;14:286–295.

16. Young MA, Cook JL, Purdam CR, et al. Eccentric decline squat protocol offers superior results at 12 months compared with traditional eccentric protocol for patellar tendinopathy in volleyball players. Br J Sports Med. 2005;39:102–105.

17. Pufe T, Petersen WJ, Mentlein R, et al. The role of vasculature and angiogenesis for the pathogenesis of degenerative tendons disease. Scand J Med Sci Sports. 2005;15:211–222.

18. Alfredson H, Forsgren S, Thorsen K, et al. Glutamate NMDAR1 receptors localised to nerves in human Achilles tendons. Implications for treatment? Knee Surg Sports Traumatol Arthrosc. 2001;9: 123–126.

19. Rees JD, Wilson AM, Wolman RL. Current concepts in the management of tendon disorders. Rheumatology (Oxford) [epub ahead of print]. February 20, 2006.