Available at: http://www.nsca-cc.org/ceus/quizzes.html Eccentric Exercise Interventions for Daniel Lorenz, PT, DPT, ATC, CSCS, USAW Providence Medical Center, Kansas City, Kansas

SUMMARY resulted in 30% of all running-related programs to accommodate the athletes injuries, and elbow injuries can who have these conditions throughout TENDON INJURIES OR TENDINO- be as high as 40% in tennis players (26). the training cycle and during the com- PATHIES ARE A CHALLENGING People of all ages and skill levels, as petitive season. Being able to recognize AND PERPLEXING CONDITION FOR well as nonathletes can be afflicted by an ‘‘itis’’ or an ‘‘osis’’ is a crucial step STRENGTH AND CONDITIONING these conditions. Tendon pathologies because the management of the ath- PROFESSIONALS. TENDON can not only lead to lost time in sports lete’s training is vastly different. An INJURIES CAN BE DEBILITATING but also can result in long-term damage inflamed ‘‘itis’’ often has sharp localized AND RESULT IN LOST TIME FROM to that can even affect daily with activity and in the morning SPORTS PARTICIPATION. IF LEFT function and let alone sports perfor- or after periods of long rest. Pain may UNTREATED, TENDON INJURIES mance. There is discrepancy in the actually decrease during activity but CAN PROGRESS TO AFFECT DAILY literature about how to manage these worsens at rest. On the contrary, FUNCTION. FURTHERMORE, injuries as well as the proper terminol- a chronic ‘‘osis’’ has fairly constant TENDON INJURIES AFFLICT ALL ogy to use when referring to them. pain that is more of a dull ache and AGES AND SKILL LEVELS. IN THE The term ‘‘tendonitis’’ is often used poorly localized. Usually, a chronic PAST 10 YEARS, ECCENTRIC as a catchall term for tendon injuries. degenerative tendon gets worse with EXERCISE HAS GAINED SUPPORT Histological studies have shown that activity. A comprehensive review by IN THE LITERATURE AS AN EFFEC- oftentimes, no inflammation exists Nirschl (22) about stages of tendon TIVE NONSURGICAL NONPHAR- (20,21). The suffix ‘‘itis’’ indicates that injury has been published previously in the Table. MACOLOGICAL INTERVENTION TO an inflammatory process is present. TREAT THESE INJURIES. THE Leadbetter (19) has previously defined Within the past few years, eccentric PURPOSE OF THIS REVIEW IS TO tendonitis as a symptomatic degener- exercise has shown promise in multiple DISCUSS THE RELEVANT TERMI- ation of a tendon with vascular disrup- studies as a potential nonoperative and NOLOGY AS WELL AS THE tion and inflammatory repair. More effective training modality for tendino- ANATOMY AND PHYSIOLOGY OF recently, the term ‘‘’’ has pathies. The purpose of this review is TENDONS AND TENDON INJURY. been used as an all-encompassing term 3-fold. First, a brief discussion about ADDITIONALLY, THE CONCEPT OF for tendon injuries, whereas the term tendon anatomy and physiology will ECCENTRIC EXERCISE IN TREAT- ‘‘tendinosis’’ has been used to describe set the foundation for discussing why ING TENDINOPATHIES WILL BE chronic tendon issues. Leadbetter (19) eccentric exercise is of physiologic DISCUSSED, AND EXERCISE has also defined tendinosis to be a focal benefit to tendons. Second, a review INTERVENTIONS WILL BE area of noninflammatory degeneration of the causes of tendinopathies will be briefly discussed. Finally, exercise PROVIDED FOR COMMON that may be asymptomatic. The suffix interventions will be provided for TENDINOPATHIES. ‘‘osis’’ implies that a degenerative pro- cess is present. Complicating this mat- common tendinopathies as well as a framework for how to implement ter further is that there are significant them effectively. INTRODUCTION differences in the physiological healing endon injuries account for responses of acutely and chronically diseased tendons (15). KEY WORDS: 30–50% of injuries in sports (16). tendon; tendonitis; tendinopathy; Strength and conditioning professionals T Specifically, chronic problems tendinosis; eccentric exercise caused by overuse of tendons have often have to develop training

90 VOLUME 32 | NUMBER 2 | APRIL 2010 Copyright Ó National Strength and Conditioning Association Table Nirschl’s stages of tendinopathy

Stage Diagnosis Macroscopic pathology Histologic findings Clinical signs 0 Healthy No inflammation Organized collagen, Firm tendon, not painful, absent absent blood cells swelling, normal temperature I Acute tendinitis Symptomatic tendon Degenerative changes Acute swelling, pain, local degeneration, increased with microtears, tenderness, warmth, cellularity, vascular disruption, inflammatory cells in dysfunction inflammation of paratenon paratenon, focal collagen disorientation II Chronic tendinitis Increased tendon degeneration Greater evidence of Chronic pain with tenderness, and vascularity microtears, increased increased dysfunction, person levels of collagen voluntarily unloads structure disorientation in tissue hypercellularity III Tendinosis Intratendinous degeneration Increased cellularity, Palpable tendon enlargement, because of microtrauma, neovascularization, swelling of tissues, increased cellular/tissue aging, vascular focal necrosis, collagen dysfunction with or without compromise disorganization pain, tendon sheath may be and disorientation swollen IV Rupture Tendon failure Complete disruption of Weak and painful muscle testing, fibers inability to move affected , positive clinical tests for tendon disruption

ANATOMY ‘‘insertional’’ tendinopathy. Regardless the tendon will be in a perpetual state Tendons transmit force generated by of location, management is very similar of breakdown and attempted but failed muscle to bone and act as a buffer and eccentric exercise can be used. healing. The end result is pain, dys- by absorbing external forces to limit Tendons are prone to injury because of function, and, for the athlete, lost time muscle damage (27). Tendons them- a ‘‘tendon paradox’’ that exists. from sport. selves are relatively avascular but get consumption is 7.5 3 lower in tendons their innervations and vascular supply and ligaments than CAUSES OF TENDON INJURIES from the paratenon, the sheath around (33). To minimize the risk of ischemia, Tendons respond to repetitive overload the tendon proper. Tendons are com- which is a decrease in blood supply, beyond the physiological threshold by posed of 30% type I collagen, gly- a low metabolic rate and anaerobic inflammation of their sheath, degener- cosaminoglycans, elastin, and 68% generating capacity in tendons are ation of their body, or a combination of water (23). Collagen’s role is to resist needed to carry loads and maintain both (27). There are a host of reasons tensile forces, whereas elastin functions tension for long periods. In the case of that tendon injuries occur, but the to increase the flexibility of tendons. tendons, risk of inadequate or deficient etiology remains unclear, and many The structure of tendons reveals that blood supply is reduced because of the causes have been theorized (27). Typ- they have a wavelike appearance at lower metabolic rate. The lower met- ically, there are 2 main types of injury rest, indicating that it is susceptible to abolic rate indicates that there is less mechanisms that have several potential and allow stretch. need for oxygen for tendons during sources in each category (5). Intrinsic Tendon injuries can happen essentially functional tasks. However, the low causes are factors contributed to an at 2 locations. Tendon injury can be metabolic rate in tendons results in athlete’s makeup. Intrinsic risk factors midsubstance or in the body of the slow healing after injuries. Thus, this include, but are not limited to such tendon proper. There is also potential may explain why tendon injuries things as anatomical abnormalities or for injury at the enthesis, which is the persist or develop chronic issues (32). malalignments (i.e., genu valgum, or attachment of a tendon, ligament, or If an athlete does not rest from the ‘‘knock kneed’’, and leg length discrep- joint capsule to the bone (28). Injury at aggravating stimulus or provide the ancies), age, gender, flexibility, joint the enthesis is commonly referred to correct environment for regeneration, laxity, muscle weakness, biomechanics/

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sport technique, fatigue, and psycho- in one location leads to changes in concentric/positive work, there is a logical factors. Intrinsic causes may or distant cells, even though the distal cell concurrent increase in cellular metab- may not be adjusted or changed and did not receive the mechanical stimulus olism. Thus, more waste products may be something that the athlete directly. Mechanotransduction closes will be generated, leading to chemical must learn to live with or possibly with the effector cell response. Here, irritation of nerves and eventually pain. make modifications in training or the mechanical stimulus on the outside Abbott and Bigland (1) did a study equipment. The other causes are due of the cell promotes intracellular pro- measuring oxygen uptake in subjects to extrinsic factors. Unlike intrinsic cesses, leading to matrix remodeling using a bicycle ergometer. Positive factors, extrinsic factors can usually through alterations in biochemical work (concentrics) always resulted in be easily changed and modified to help pathways and gene expression. In the more oxygen consumption than nega- the athlete. The 2 main extrinsic causes case of tendons, load-induced responses tive work. Abbott et al. (2) did a follow- of injury to tendons are overuse and via mechanotransduction have shown up study examining the relationship training errors (3–6,9,20). Considera- an upregulation of insulin-like growth between oxygen consumption and tions under the umbrella of extrinsic factor (IGF-I), which has been asso- work. Results of the study showed that causes include, but are not limited to, ciated with cellular proliferation and oxygen consumption is many times faulty equipment, playing surfaces, and matrix remodeling (17). larger at great force and low speed than shoe wear. Training errors can include In shortening of a muscle, the faster it at small force and high speed. Lastly, a number of factors that the strength contracts, the smaller the tension it can Bigland-Ritchie and Woods (7) found and conditioning professional can exert (10). Tension is considerably that less muscle activity is required to significantly contribute to either posi- greater in muscle fibers when length- maintain the same force during nega- tively or negatively. Doing ‘‘too much ened than when shortened (19–21). tive work, fewer muscle fibers are re- too soon’’ or having intensity/volume/ During negative work (eccentrics), the quired to exert a given force, and there load too high; progressions too fast; oxygen consumption rarely rises to is a substantial reduction in oxygen improper rest and recovery; and repe- more than twice the resting value uptake when fibers are stretched. The titive, asymmetric, specialized training (1,2,12,31,32). Studies have shown pre- above studies show that eccentric exer- are all things that put an athlete at viously that when a muscle is stretched, cise results in less oxygen consump- risk. A properly designed program with the energy requirement falls sub- tion, more force production, and less progressive overload helps minimize stantially because ATP breakdown energy requirement than concentric risk from these factors. and heat production are both slowed exercise. Put simply, ‘‘you get much (8,31,32). Clearly, the decreased energy more bang for your physiological THE CASE FOR ECCENTRIC and oxygen requirements needed are buck’’ with eccentric exercise, both EXERCISE of benefit to tendon metabolism based for the muscle and for the tendon. As stated previously, the current par- on the above discussion regarding Many studies in the past 10 years have adigm is shifting in favor of eccentric the ‘‘tendon paradox.’’ Furthermore, substantiated eccentric exercise as a exercise in the treatment of tendino- with increased heat generation during treatment for tendinopathies. In 1998, pathies. Khan and Scott (17) have discussed the role of mechanotrans- duction as a mechanism for healing in eccentric exercise. Mechanotransduction is the process by which the body converts mechanical loading into cellular responses (17). These cellular responses lead to cell signaling, an informational network of proteins, lipids, and ion channels that are part of a physiologic cascade. Mechano- transduction is broken down into 3 steps (17). Mechanocoupling is when a physical load (i.e., tension or shear) causes a physical perturbation of cells that make up a tissue. These forces elicit a deformation of the cell that triggers a series of events depending on the type, load, duration, and magnitude of loading. The second step is cell-cell communication. In this step, stimulus Figure 1. Leaning calf raise.

92 VOLUME 32 | NUMBER 2 | APRIL 2010 Alfredson performed, to the author’s knowledge, the first study investigating eccentric exercise on diseased tendons, and the protocol used in that study has been used in most studies on eccentric training (4). In a prospective study of 15 athletes with chronic Achilles tendinosis, subjects performed 3 sets of 15 repetitions of bent knee and straight knee calf raises, twice a day, 7 days per week over 12 weeks. Subjects were told to work through pain, only ceasing exercise if pain became dis- abling. Load was increased in 5 kg increments with use of a backpack that carried the weight once body weight was pain free. Researchers found that all 15 patients returned to preinjury levels of activity. Additionally, they had a significant decrease in pain with a significant increase in strength. Shalabi et al. (25) evaluated 25 patients with chronic Achilles tendinopathy measured before and after an eccentric program using the protocol of Alfred- son et al. via magnetic resonance imaging for tendon volume and intra- tendinous signal. Eccentric training resulted in decreased tendon volume and decreased intratendinous signal, which correlated to improved clinical outcomes. Reduction in fluid content within the tendon may suggest in- creased collagen deposition. The in- Figure 2. (a) Beginning of supine calf raise. (b) Eccentric portion of supine calf raise. crease in collagen is a possible effect because Langberg et al. (18) found that type I collagen synthesis increased after eccentric training in a group of 12 soccer players with unilateral Achilles tendinosis. Ohberg et al. (24) also found that in a group of subjects with chronic Achilles tendinosis training with the eccentric calf protocol of Alfredson et al. resulted in a decrease in tendon thickness and normalized tendon structure in most patients, both correlated with less pain. Jonsson and Alfredson (11) did a pro- spective study of athletes with jumper’s knee randomized into either an eccen- tric or a concentric group for 12 weeks. In the eccentric group, 9 of 10 subjects were pleased with treatment, whereas 10 of 10 in the concentric group were not. At mean follow-up of 32 months, Figure 3. Anterior step down.

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the eccentric group was still satisfied and sports active, but all in the con- centric group had surgery or sclerosing injections. In another study including athletes with patellar tendinopathy, Young et al. (34) used 2 different eccentric programs in elite volleyball players using the protocol of Alfredson et al. but with different exercises. One group did decline squats, whereas the other did a single-leg step down. Results of the study showed that both groups improved from baseline at 12 weeks and 12 months. Systematic reviews of literature by Wasielewski and Kotsko (30) and Kingma et al. (14) examined the effects of eccentrics in reducing pain and improving strength in those with lower extremity tendinosis and chronic Achilles tendinopathy, respectively. The systematic reviews revealed that eccentric exercise may reduce pain and improve strength in lower extremity tendinopathies, but whether it is better than other forms of rehabilitation has yet to be determined and the magni- tude of the effects are equivocal.

IMPLEMENTATION OF ECCENTRICS Kibler et al. (13) has previously stated that the goal of rehabilitation in tendinopathies is relief of the symp- Figure 4. (a) Concentric portion of leg press; (b) Eccentric portion of leg press. toms from the ‘‘itis’’ to the restoration of function that is lost with the ‘‘osis.’’ The previous studies have shown great potential in using eccentrics to restore function. From an exercise standpoint, regardless of body part, load and volume should be progressed gradually and should be dictated by the amount of pain the athlete experiences. Be- cause the athlete is recovering from injury, it is advised that load used not be determined by a 1 repetition maximum (RM). Furthermore, some of the exercises are for targeted muscle groups (elbow extensors for elbow injury), and determining a 1 RM is not practical or advised. The protocol of Alfredson et al. has been used in previous studies and appears to be a safe and effective method to imple- ment the eccentric training program. Figure 5. Decline squat.

94 VOLUME 32 | NUMBER 2 | APRIL 2010 Curwin (9) has previously proposed a method to determine training load in eccentric training for tendon injuries that is based on repetitions completed and the amount of pain experienced. One significant difference between Curwin’s program and Alfredson’s program is that the athlete performs both the concentric and eccentric portions of the exercise, with the eccentric portion being performed at a faster rate. In their protocol, they suggest that the athlete should experi- ence pain and fatigue between 20 and 30 repetitions at a given load, perform- ing 3 sets of 10 repetitions. Pain felt before that range is generally accom- panied by worsening of symptoms and Figure 6. Lateral step down. either load or speed is decreased. If there is no pain after 30 repetitions, the stimulus is inadequate. Either load is increased or the speed of exercise performance is increased but not both. Pain experienced during the exercise protocol should be similar to the pain experienced during the athlete’s func- tional activity with an acceptable moderate increase from that point. If it is the athlete’s first session, load is increased until symptoms appear. After a general warm-up (bike, upper-body ergometer), the athlete performs two 30-second stretches of the involved muscle group. The athlete then com- pletes the above exercise protocol. The author of this article suggests that once the athlete can complete 15 repetitions over all 4 sets, resistance should be increased to perform sets of 8 repetitions with the eighth repetition being close to failure. The athlete uses that load and builds up to 15 repeti- tions before increasing load again. Anecdotally, the author has found this method to be progressive yet safe, with less overall volume to help enhance recovery. Additionally, 3–4 sessions per week is advocated instead of everyday. The author proposes that ‘‘heavy load’’ is a misnomer in the study of Alfredson et al. because the volume of exercise is rather high and the load is low given the amount of exercise that is tolerated by the athlete. Ultimately, however, Figure 7. (a) Eccentric wrist curl, stretching wrist extensors. (b) Passive return to start dosing will be based on tendon position.

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reactivity. Load should be reduced at least 10% if the athlete has increased pain or worsening of symptoms, par- ticularly with activities of daily living. Depending on their symptoms, intro- ducing concentric exercise should be based on whether or not they have pain with nonsporting activities. Concentrics can be attempted once nonsport activities, like walking and stair climbing, are pain free. As with eccentrics, the concentric portion of exercise should involve a gradual pro- gression. Once concentrics are pain free, then the athlete can begin jogging or more sport-specific activities. A progression from individual drills to Figure 8. Eccentric radial deviation. team activities is a methodical way to reintroduce the athlete to sport. If the athlete has pain, they should regress to the previous regimen until pain free. In the author’s experience, a cooldown activity (i.e., recumbent bike) followed by stretching of involved muscles should follow the program. Although Thacker et al. (29) found that there is insufficient evidence to support pre- or postexercise stretching, lack of flexibil- ity is a common finding in chronic tendinopathies (9) and should be a part of the program. Ice to the affected area is advised to limit postexercise pain and potential inflammation. Athletes should be warned that eccentric exer- cise may make them sore initially, and this is to be expected. As a general rule, athletes are instructed to perform eccentrics by actively doing the eccen- tric portion of the muscle/joint in question while returning to the start position passively or with assistance of the other limb, instead of actively doing the concentric portion. ACHILLES TENDINOPATHIES The athlete could begin with calf raises on flat ground, plantar flexing with both legs, and going down with the involved muscles only. Once these are pain free, the athlete can be progressed to leaning calf raises with the use of a physioball (Figure 1). In the leaning position, there is more ankle dorsiflex- ion, which induces a greater stretch to the Achilles and thus more force is Figure 9. (a) Eccentric supination. (b) Passive return to start position. needed to plantar flex. Next, the athlete

96 VOLUME 32 | NUMBER 2 | APRIL 2010 CONCLUSION Eccentric exercise is showing promise as an effective means to treat tendon injuries. It is so promising because the basis for it is centered on muscle and tendon physiology, not a theory. It should be a part of a comprehensive program that involves collaboration of the health care team and the athlete’s coaches to ensure that all intrinsic and extrinsic risk factors have been ad- dressed as well as other complimentary pain alleviating modalities. It is hoped that more research will surface further, advocating the use of eccentric exercise.

Dan Lorenz is Figure 10. Shorter lever arm for exercise performance. a sports medicine specialist at Providence can progress to a staircase. A nice portion with both legs and the lower- Medical Center compliment to these exercises is using ing phase with just the involved and an adjunct a leg press machine as a ‘‘supine calf muscles. When using the decline board faculty member raise’’ fashion (Figure 2). Depending on or step, they should only get back on at Rockhurst how much pain the athlete is experi- the step using the uninvolved limb. University in encing, the supine position may be Kansas City, TENNIS ELBOW a more appropriate starting point Missouri. because the weight can be adjusted Tennis elbow, or lateral epicondylitis, is to be less than body weight. A very an irritation of the common extensor functional addition to the Achilles tendon from its attachment on the REFERENCES program would be an anterior step lateral epicondyle of the humerus. On 1. Abbott BC and Bigland B. The effects of down (Figure 3). The athlete leads with the extensor surface, the supinator force and speed changes on the rate of the uninvolved muscle, attempting to muscle is also implicated. Therefore, oxygen consumption during negative work. keep the involved heel on the step. As it should be included as part of a pro- J Physiol 120: 319–325, 1953. the reader can see, the ankle is in gram. The athlete can do ‘‘eccentric 2. Abbott BC, Bigland B, and Ritchie JM. The a dorsiflexed position, thereby placing wrist extension’’ (Figure 7). Here, the physiological cost of negative work. the Achilles on stretch because it weight is raised by the uninvolved limb J Physiol 117: 380–390, 1952. controls the motion. In this position, and then lowered by the involved 3. Alfredson H and Lorentzon R. Chronic the soleus muscle is targeted in its role muscles. A hammer or similar device Achilles tendinosis: Recommendations for as a decelerator of the tibia anteriorly with a long lever arm to do eccentric prevention and treatment. Sports Med 29: 135–146, 2000. during gait during the end of stance radial deviation (Figure 8) and eccen- phase to limit excessive dorsiflexion. tric supination (Figure 9) are additional 4. Alfredson H, Pietila T, Jonsson P, and To progress, the step can be increased exercises. Again, it must be reinforced Lorentzon R. Heavy-load eccentric calf muscle training for treatment of chronic that the athlete cannot raise the weight or the athlete can hold dumbbells. Achilles tendinosis. Am J Sports Med back to the starting position concen- 26: 360–366, 1998. trically. Although cumbersome to 5. Almekinders LC. Tendinitis and other PATELLAR TENDINOPATHIES reach across to the involved limb to chronic tendinopathies. J Am Acad Orthop It is suggested that an athlete begins raise it back to the starting position, it Surg 6: 157–164, 1998. using the leg press because the weight must be done initially to prevent 6. Almekinders LC and Temple JD. Etiology, can be adjusted to be less than body further flares. Athletes can be pro- diagnosis, and treatment of tendonitis: An weight if the athlete cannot tolerate gressed by increasing the lever arm or analysis of the literature. Med Sci Sports body weight due to pain (Figure 4). adding weight. Conversely, if they Exerc 30: 1183–1190, 1998. Other means include decline squats cannot tolerate a weight at a longer 7. Bigland-Ritchie B and Woods JJ. (Figure 5) or eccentric step downs lever arm position, it can be moved to Integrated electromyogram and oxygen (Figure 6). The athlete should be shorten the lever arm, which may uptake during positive and negative work. reminded to perform the concentric make the exercise tolerable (Figure 10). J Physiol 260: 267–277, 1976.

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