Eccentric training

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Eccentric training is a type of strength training [1] that involves using the target muscles to control weight as it moves in a downward motion. This type of training can help build muscle, improve athletic performance, and reduce the risk of injury. An eccentric contraction is the motion of an active muscle while it is lengthening under load. Eccentric training is repetitively doing eccentric muscle contractions. For example, in a biceps curl the action of lowering the dumbbell back down from the lift is the eccentric phase of that exercise – as long as the dumbbell is lowered slowly rather than letting it drop (i.e., the biceps are in a state of contraction to control the rate of descent of the dumbbell).

Contents

An eccentric contraction is one of the distinct phases in the movement of muscles and tendons; they include isometric contraction (no movement), isotonic contraction, and concentric contraction (shortening).

Eccentric training focuses on slowing down the process of muscle elongation to challenge the muscles, which can lead to stronger muscles, faster muscle repair and increasing metabolic rate. [2]

Eccentric movement provides a braking mechanism for muscle and tendon groups that are experiencing concentric movement to protect joints from damage as the contraction is released. [2]

Eccentric training is particularly good for casual and high-performance athletes or the elderly and patients looking to rehabilitate certain muscles and tendons. [3]

Negative movement

This movement has also been described as negative training. This "negative" movement is necessary to reverse the muscle from its initial trajectory. [2]

When the load exceeds the force that can be developed by the muscle at a constant length, as in an eccentric muscle action, the exercise is referred to as involving negative work, because the muscle is absorbing energy. [2]

Eccentric contractions use less metabolic energy, even though they can create more force than concentric actions. [2]

History

Adolf Eugen Fick discovered in 1882 that "contracting muscle under stretch could produce greater force than a shortening muscle contraction" like in concentric movements. Fifty years later, A.V. Hill found that "the body had lower energy demand during an eccentric muscle contraction than during a concentric muscle action". [4]

Erling Asmussen introduced eccentric training in 1953, with "ex" meaning "away from" and "centric" meaning "center". Hence, the term was coined to mean a muscle contraction that moves away from the center of the muscle. [4]

The first revelation of the functional significance of these properties occurred in a clever demonstration devised by Bud Abbott, Brenda Bigland, and Murdoch Ritchie. They connected two stationary cycle ergometers back-to-back with a single chain, such that one cyclist pedaled forward and the other resisted this forward motion by braking the backward-moving pedals. Because the internal resistance of the device was low, the same force was being applied by both individuals, yet the task was much easier for the individual braking. This demonstration cleverly revealed that a tiny female resisting the movement of the pedals could easily exert more force than, and hence control the power output of, a large burly male pedaling forward. [4]

Energy

During the eccentric phase of the movement, the muscle absorbs energy. This work is done "by stretching the muscle and in this process, the muscle absorbs mechanical energy". [4]

This mechanical energy is dissipated or converted into one or a combination of two energies.

Elastic recoil

The energy that is absorbed by the muscle can be converted into elastic recoil energy, and can be recovered and reused by the body. This creates more efficiency because the body is able to use the energy for the next movement, decreasing the initial impact or shock of the movement. [4]

For example, kinetic energy is absorbed in running every time one's foot strikes the ground and continues as one's mass overtakes the foot. At this moment, elastic recoil energy is at its maximum and a large amount of this energy is absorbed and is added to the next stride. [4]

This movement is similar to the action of springs, where the muscle is continually shortened and stretched resulting in enhanced effectiveness and force. It can lead to the perception of "less effort" even though dealing with higher force. [5]

But time matters in elastic recoil. If this energy is not used quickly it is dissipated as heat. The role of eccentric training is to use these principles of energy conversion to strengthen muscle and tendon groups. [4]

Heat

The energy that is absorbed by the muscle will be dissipated as heat if the muscle is being used as a "damper or shock absorber". This leads to an increase in body temperature. [4]

Physiological mechanisms

The muscle has "tension producing tissue comprising small contractile units referred to as sarcomeres" that each contains a "thick (myosin) and thin (actin) myofilament (muscle filaments or proteins) that overlaps to format a cross-bridge bond (attachment)". [2]

When in a concentric exercise, shortening of a muscle occurs as the myosin and actin cross-bridges repeatedly attach and detach to draw the actin across the myosin – creating force. Each cross-bridge attachment and detachment cycle is powered by the splitting of one molecule of adenosine triphosphate (ATP). Examples of such exercises include kicking a ball or lifting a weight. [2]

In controlled release reversals of such concentric motions, the eccentric movement stretches the muscle with opposing force that is stronger than the muscle force. When myofilaments of the muscle fiber are stretched in such eccentric contractions there can be reduced numbers of detachments of cross bridge myosin and actin links. With more cross bridges remaining attached there is greater force production in the muscle. Examples of activities involving eccentric muscle contraction include walking down a hill or resisting the force of gravity while lowering a heavy object. [2]

Eccentric actions place a stretch on the sarcomeres to the point where the myofilaments may experience strain, otherwise known as exercise-induced delayed onset muscle soreness (DOMS). One area of research that has much promise in relation to DOMS and eccentric exercise is the repeated-bout effect (RBE). To help prevent or lessen DOMS from eccentric exercise, or to facilitate recovery from it, the exerciser would eccentrically stimulate the muscle, then repeat at weekly intervals to build up strength and allow the strain (in response to a given force level) to reduce over time. [2]

Muscle injury

Eccentric contractions are a frequent cause of muscle injury when engaging in unaccustomed exercise. But a single bout of such eccentric exercise leads to adaptation which will make the muscle less vulnerable to injury on subsequent performance of the eccentric exercise. [6]

Findings

Several key findings have been researched regarding the benefits of eccentric training:

Eccentric exercise

Eccentric exercise or resistance training is currently being used as a form of rehabilitation for sports injuries, but also as an alternative form of exercise for the elderly and those affected by neurological disorders, COPD, cardiopulmonary disorders, and cancer. [7] Muscle loss is a big problem faced by people afflicted with the above disorders and many cannot participate in rigorous exercise protocols. Eccentric muscle contractions produce high forces with low-energy costs. According to Hortobágyi due to these properties, eccentric exercise has the greatest potential for muscle strengthening. [8] To strengthen muscle the external force must exceed the muscle while it lengthens. [9] The definition of eccentric contraction is almost the exact definition of muscle strengthening.

Perceived muscle damage: There is a stipulation regarding eccentric contractions in that they actually cause muscle damage and injury. Eccentric contraction may result in delayed onset muscle soreness however; the contraction itself does not cause muscle damage or injury. [10]

Proof of muscle strengthening without damage: One recurring problem in ACL rehabilitation is improving muscle strength of the quadriceps without re-injury. Early, high-force eccentric training can be used to increase muscle strength and volume without damage to the ACL graft, surrounding soft tissue, and the articular cartilage. [9] In an experiment performed on rat muscles after twenty sessions of treadmill low-intensity eccentric training the wet weight of the muscles and the fiber cross-section was significantly larger than the control and level groups. [11] These results led to the conclusion that low-intensity eccentric contractions have the ability to "produce enough mechanical stress to induce muscle hypertrophy without over-stressing which could produce muscle fiber damage. Other articles have found that muscle damage is not required to reach hypertrophy. Greater mechanical stress brought on by eccentric contractions is what leads to hypertrophy in individuals undergoing eccentric training. [12] Studies done on the elderly show that low-intensity eccentric conditioning can actually minimize muscle damage [13] According to Gault the low cost of energy and low oxygen demand make low-intensity eccentric exercise ideal for the elderly. [14]

Eccentric contraction and oxygen consumption: Oxygen consumption is needed for muscles to work properly. Eccentric muscle contractions are considered to be negative work as the muscle is working with resistance. Negative work is the mechanical energy absorbed by the work conducted on a muscle when the force on the muscle is greater than the force produced. [10] An experiment was conducted on bicycle riding. The amount of oxygen consumption was measured during the motion of pedaling forward as positive work and pedaling with resistance as negative work. [15] Less oxygen was consumed during negative work than of positive work with the oxygen consumption ratio being 3:7. [15] Due to the low oxygen consumption of eccentric exercise studies have been conducted on patients with severe COPD. An eccentric cycling exercise workout was created for these patients and the results found there to be no side effects, minimal muscle soreness that had no effect on power, and high compliance. [16] Furthermore, other cycling studies concluded that eccentric cycling was a safe alternative for COPD patients as they can perform high-intensity work with lower cost. [17]

Eccentric contractions and cardiac output: With the lower cost of oxygen, how would eccentric exercise affect the heart? A study was performed to test how eccentric and concentric contractions affect cardiac autonomic modulation after exercise. Men (aged 18–30) were divided into four groups: concentric control, eccentric control, concentric training, and eccentric training. Results concluded that resistance training (eccentric contractions) promoted strength gain. An increase in cardiac vagal modulation during recovery was also concluded. [18]

A lot of studies have been conducted regarding eccentric exercise over the last decade. It can be said there is substantial evidence that eccentric exercise truly exceeds concentric exercise for rehabilitation and training aspects in force, energy cost, oxygen consumption, and muscular strengthening.

Sports and rehabilitation

Kim St-Pierre healed from hip surgery with eccentric exercise Kim St-Pierre 33.jpg
Kim St-Pierre healed from hip surgery with eccentric exercise

With eccentric training, muscles are able to create more for less work, which has special meaning in the realms of high-performance sports – both for injury prevention and optimal-performance training. For athletes and sports enthusiasts, this eccentric model can help with explosive force [ citation needed ] training to prevent injuries or recurring injuries, and trains the body to use the kinetic force driven by eccentric training more efficiently. [19] Canadian Olympian Kim St-Pierre uses eccentric training as part of her regime. The Esmonde Technique takes eccentric training and makes it available to the masses through Classical Stretch and Essentrics. After having hip surgery in the summer of 2007, St-Pierre began to practice the Esmonde Technique with experts Miranda Esmonde-White from PBS's Classical Stretch and Sahra Esmonde-White host of the Essentrics workout to heal her hip. [20]

According to tests, increases in both strength and muscle fiber are higher in eccentric training than in traditional concentric training. [21]

The rehabilitative nature, low energy costs, high magnitudes of force, and low uptake of oxygen all align eccentric exercise for both the elderly and rehabilitative functions. [3]

In old age, loss of strength and muscle mass is commonplace. Add to these factors disease and cardiac and respiratory illness. Eccentric training enables the elderly, and those with the same problems, the ability to train muscle groups and increase strength and resiliency with low-energy exercise. [3]

Eccentric training has been found to be beneficial to those with a variety of physical ailments. [19]

According to one systematic review and meta-analysis on shoulder impingement syndrome, eccentric training didn't improve pain or function more than other types of training. [22]

Anterior cruciate ligament damage

Tearing an anterior cruciate ligament (ACL) in the knee causes serious damage that can last several years and often requires surgery. The ACL is one of the four main stabilizing ligaments of the knee. During the post-operative rehabilitation of patients, eccentric training can be used as a cornerstone of developing muscle size and strength. According to tests conducted by J. Parry Gerber in 2007, structural changes in the muscles greatly exceeded those achieved with standard concentric rehabilitation. The success of the involvement of gradual progressive exposure to negative work ultimately led to the production of high muscle force. [23]

Sarcopenia

Sarcopenia is the progressive loss of muscle mass due to aging. Muscle mass begins to deteriorate as early as the age of 25, and consistently deteriorates into old age. By the age of 80 "one-half of the skeletal muscle has been lost" (Lastayo, Woolf, Lewek, Snyder-Mackler, Reich & Lindstedt, 2003). With this great decrease in mass, strength is also decreased. Eccentric training has the ability to counteract sarcopenia through sustained training. The unique trait of greater overloads to the muscle with less strenuous impact on the body, as well as cardiac and respiratory systems, offers a unique case for the elderly. The high-force and low-cost set of attributes in eccentric exercise makes it ideal for the actively impaired. [24]

Muscle tendon injuries

The entire muscle-tendon system works cohesively to slow down limb movement. The close relationship between the muscle and tendons help to dissipate heat or temporarily store kinetic energy. If the forces needed to slow down a limb exceed the capacity of the muscle-tendon system, injury is likely to occur.

Athletes with recurring hamstring and abductor muscle injuries have greater impairment of eccentric strength, suggesting that improvements in eccentric training may minimize the risks of injury by strengthening the muscle-tendon groupings in high-stress areas of the body.

Eccentric training is of huge benefit to those that wish to avert injuries by improving the muscle's abilities to absorb more energy before deteriorating. According to one article, "Increased stiffness in tendons, greater force at failure, and an improved ability to absorb energy at the musculotendonous junction result following eccentric exercise training". [24]

Osteopenia

Usually viewed as a precursor to osteoporosis, osteopenia is when bone density is lower than normal levels. Bone mass is affected by muscle forces and their loads on the bone structure. The strength and density of the bone are directly influenced by local strain. Due to the high strain on muscles during eccentric training, coupled with low energy output, eccentric training becomes a cornerstone of the rehabilitative process. [24]

Tendinoses

Intense repetitive activities tend to create chronic tendon disorders, where the tendons become injured, inflamed, or ruptured. While typically these disorders are directly related to eccentric muscle movements, the ability of a muscle to strengthen and prevent injury through eccentric training is great. Controlled rehabilitative regimes will actually strengthen and repair tendons. Ample evidence supports the notion that the tendon, like the muscle, can adapt favorably to physical stress and eccentric loads. [24]

It has been deduced that high muscle-tendon forces delivered in a controlled environment are needed for optimal tendon adaptation. While eccentric stress is related to the injury, high-force eccentric exercises are needed to maximize recovery. [24]

Chronic patellar tendonitis

A condition that arises when the tendon and the tissues that surround it, become inflamed and irritated. This is usually due to overuse, especially from jumping activities. This is the reason chronic patellar tendonitis is often called "jumper’s knee." A study was done by Roald Bahr and colleagues looked at which method of tendon rehabilitation exercise – the "eccentric squat" exercise or the universal gym "leg extension/leg curl" — produced more recovery results in terms of recovery in the treatment of chronic patellar tendonitis. On the twelve-week exercise program, participants were tested for thigh circumference and quadriceps, and hamstring moment of force. There was no significant difference between the groups in either quadriceps or hamstring moment of force and hamstring moment of force significantly increased in both groups, but the eccentric squat saw significantly lower pain ratings and produced twice as many pain-free subjects at the end of the program than the other group. [25]

Cardiovascular changes

Several recent studies have indicated that eccentric exercise as walking down hill has greater beneficial effects on insulin sensitivity, lipid profiles, and physical fitness than walking up hill. One study used stairs and elevators [26] and the other a mountain and a cable car. [27] In both cases the cardiovascular improvements were greater for being lifted up and walking down than for walking up and being lowered down.

See also

Related Research Articles

Spasticity is a feature of altered skeletal muscle performance with a combination of paralysis, increased tendon reflex activity, and hypertonia. It is also colloquially referred to as an unusual "tightness", stiffness, or "pull" of muscles.

<span class="mw-page-title-main">Rotator cuff</span> Group of muscles

The rotator cuff is a group of muscles and their tendons that act to stabilize the human shoulder and allow for its extensive range of motion. Of the seven scapulohumeral muscles, four make up the rotator cuff. The four muscles are:

<span class="mw-page-title-main">Skeletal muscle</span> One of three major skeletal system types that connect to bones

Skeletal muscles are organs of the vertebrate muscular system and typically are attached by tendons to bones of a skeleton. The muscle cells of skeletal muscles are much longer than in the other types of muscle tissue, and are often known as muscle fibers. The muscle tissue of a skeletal muscle is striated – having a striped appearance due to the arrangement of the sarcomeres.

Weakness is a symptom of many different medical conditions. The causes are many and can be divided into conditions that have true or perceived muscle weakness. True muscle weakness is a primary symptom of a variety of skeletal muscle diseases, including muscular dystrophy and inflammatory myopathy. It occurs in neuromuscular junction disorders, such as myasthenia gravis.

Delayed onset muscle soreness (DOMS) is the pain and stiffness felt in muscles after unaccustomed or strenuous exercise. The soreness is felt most strongly 24 to 72 hours after the exercise. It is thought to be caused by eccentric (lengthening) exercise, which causes small-scale damage (microtrauma) to the muscle fibers. After such exercise, the muscle adapts rapidly to prevent muscle damage, and thereby soreness, if the exercise is repeated.

Muscle fatigue is when muscles that were initially generating a normal amount of force, then experience a declining ability to generate force. It can be a result of vigorous exercise, but abnormal fatigue may be caused by barriers to or interference with the different stages of muscle contraction. There are two main causes of muscle fatigue: the limitations of a nerve’s ability to generate a sustained signal ; and the reduced ability of the muscle fiber to contract.

<span class="mw-page-title-main">Stretching</span> Form of physical exercise where a muscle is stretched to improve it

Stretching is a form of physical exercise in which a specific muscle or tendon is deliberately expanded and flexed in order to improve the muscle's felt elasticity and achieve comfortable muscle tone. The result is a feeling of increased muscle control, flexibility, and range of motion. Stretching is also used therapeutically to alleviate cramps and to improve function in daily activities by increasing range of motion.

<span class="mw-page-title-main">Muscle contraction</span> Activation of tension-generating sites in muscle

Muscle contraction is the activation of tension-generating sites within muscle cells. In physiology, muscle contraction does not necessarily mean muscle shortening because muscle tension can be produced without changes in muscle length, such as when holding something heavy in the same position. The termination of muscle contraction is followed by muscle relaxation, which is a return of the muscle fibers to their low tension-generating state.

<span class="mw-page-title-main">Strength training</span> Performance of physical exercises designed to improve strength

Strength training, also known as weight training or resistance training, involves the performance of physical exercises that are designed to improve strength and endurance. It is often associated with the lifting of weights. It can also incorporate a variety of training techniques such as bodyweight exercises, isometrics, and plyometrics.

<span class="mw-page-title-main">Plyometrics</span> Maximum-intensity explosive exercises

Plyometrics, also known as jump training or plyos, are exercises in which muscles exert maximum force in short intervals of time, with the goal of increasing power (speed-strength). This training focuses on learning to move from a muscle extension to a contraction in a rapid or "explosive" manner, such as in specialized repeated jumping. Plyometrics are primarily used by athletes, especially martial artists, sprinters and high jumpers, to improve performance, and are used in the fitness field to a much lesser degree.

<span class="mw-page-title-main">Achilles tendon rupture</span> Medical condition where the tendon at the back of the ankle breaks

Achilles tendon rupture is when the Achilles tendon, at the back of the ankle, breaks. Symptoms include the sudden onset of sharp pain in the heel. A snapping sound may be heard as the tendon breaks and walking becomes difficult.

Muscle weakness is a lack of muscle strength. Its causes are many and can be divided into conditions that have either true or perceived muscle weakness. True muscle weakness is a primary symptom of a variety of skeletal muscle diseases, including muscular dystrophy and inflammatory myopathy. It occurs in neuromuscular junction disorders, such as myasthenia gravis. Muscle weakness can also be caused by low levels of potassium and other electrolytes within muscle cells. It can be temporary or long-lasting. The term myasthenia is from my- from Greek μυο meaning "muscle" + -asthenia ἀσθένεια meaning "weakness".

Hypertonia is a term sometimes used synonymously with spasticity and rigidity in the literature surrounding damage to the central nervous system, namely upper motor neuron lesions. Impaired ability of damaged motor neurons to regulate descending pathways gives rise to disordered spinal reflexes, increased excitability of muscle spindles, and decreased synaptic inhibition. These consequences result in abnormally increased muscle tone of symptomatic muscles. Some authors suggest that the current definition for spasticity, the velocity-dependent over-activity of the stretch reflex, is not sufficient as it fails to take into account patients exhibiting increased muscle tone in the absence of stretch reflex over-activity. They instead suggest that "reversible hypertonia" is more appropriate and represents a treatable condition that is responsive to various therapy modalities like drug or physical therapy.

A negative repetition is the repetition of a technique in weight lifting in which the lifter performs the eccentric phase of a lift. Instead of pressing the weight up slowly, in proper form, a spotter generally aids in the concentric, or lifting, portion of the repetition while the lifter slowly performs the eccentric phase for 3–6 seconds.

A stretch-shortening cycle (SSC) is an active stretch of a muscle followed by an immediate shortening of that same muscle.

<span class="mw-page-title-main">Backward running</span>

Backward running, also known as backwards running, running backwards, reverse running, retro running, or retro locomotion is the act of running in reverse, so that one travels in the direction one's back is facing rather than one's front. It is classed as a retro movement, the reverse of a normal movement.

<span class="mw-page-title-main">Anterior cruciate ligament injury</span> Ligament injury near the knee

An anterior cruciate ligament injury occurs when the anterior cruciate ligament (ACL) is either stretched, partially torn, or completely torn. The most common injury is a complete tear. Symptoms include pain, an audible cracking sound during injury, instability of the knee, and joint swelling. Swelling generally appears within a couple of hours. In approximately 50% of cases, other structures of the knee such as surrounding ligaments, cartilage, or meniscus are damaged.

In an isotonic contraction, tension remains the same, whilst the muscle's length changes. Isotonic contractions differ from isokinetic contractions in that in isokinetic contractions the muscle speed remains constant. While superficially identical, as the muscle's force changes via the length-tension relationship during a contraction, an isotonic contraction will keep force constant while velocity changes, but an isokinetic contraction will keep velocity constant while force changes. A near isotonic contraction is known as Auxotonic contraction.

<span class="mw-page-title-main">Pulled hamstring</span> Medical condition

Straining of the hamstring, also known as a pulled hamstring, is defined as an excessive stretch or tear of muscle fibers and related tissues. Hamstring injuries are common in athletes participating in many sports. Track and field athletes are particularly at risk, as hamstring injuries have been estimated to make up 29% of all injuries in sprinters. Hamstring injuries can also come with a hip injury from sprinting. Symptoms for a hip injury are pain, aching and discomfort while running or any physical exercise.

<span class="mw-page-title-main">Architectural gear ratio</span> Ratio between muscle-shortening velocity and fiber-shortening velocity

Architectural gear ratio, also called anatomical gear ratio (AGR) is a feature of pennate muscle defined by the ratio between the longitudinal strain of the muscle and muscle fiber strain. It is sometimes also defined as the ratio between muscle-shortening velocity and fiber-shortening velocity.

References

  1. ↑ Imran, Ali (26 May 2022). "#ccentric Training: 5 Reasons to Include It in Your Training". fitness mantras. Retrieved 28 February 2023.
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  20. ↑ "Goalie St.Pierre Takes A Page From The Ballet World". TSN. 17 April 2009.
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  22. ↑ Larsson, Robin; Bernhardsson, Susanne; Nordeman, Lena (2019). "Effects of eccentric exercise in patients with subacromial impingement syndrome: a systematic review and meta-analysis". BMC Musculoskeletal Disorders. 20 (1): 446. doi: 10.1186/s12891-019-2796-5 . ISSN   1471-2474. PMC   6792214 . PMID   31610787.
  23. ↑ Gerber, Marcus; Parry, J.; Robin, L.; Dibble, Leland E.; Greis, Patrick E.; Burks, Robert T.; LaStayo, Paul C.; March (2007). "After Anterior Cruciate Ligament Reconstruction Effects of Early Progressive Eccentric Exercise on Muscle Structure". The Journal of Bone and Joint Surgery. 89 (3): 559–57. doi:10.2106/jbjs.f.00385. PMID   17332105.
  24. 1 2 3 4 5 LaStayo, Paul C. PhD; Woolf, John M.; Lewek, Michael D.; Snyder-Mackler, Lynn; Trude-Reich, Lindstedt; Stan, L. PhD; October (2003). "Eccentric Muscle Contractions: Their Contribution to Injury, Prevention, Rehabilitation, and Sport". Journal of Orthopaedic & Sports Physical Therapy. 33 (10): 557–71. doi: 10.2519/jospt.2003.33.10.557 . PMID   14620785.
  25. ↑ Bahr, Roald; Fossan, Bjorn; Loken, Sverre; Engebretsen, Lars; August (2006). "Surgical Treatment Compared with Eccentric Training for Patellar Tendinopathy (Jumpers Knee) A Randomized Controlled Trial". The Journal of Bone and Joint Surgery. 88A (8): 1689–1698. doi:10.2106/JBJS.E.01181. PMID   16882889. S2CID   10659933.
  26. ↑ Chen, Trevor; Hsieh, Chung-Chan; Tseng, Kuo-Wei; Ho, Chih-Chiao; Nosaka, Kazunori (2017). "Effects of Descending Stair Walking on Health and Fitness of Elderly Obese Women". Medicine & Science in Sports & Exercise. 49 (8): 1614–1622. doi:10.1249/MSS.0000000000001267. PMID   28291022. S2CID   46849524.
  27. ↑ M, Zepetzauer; Drexel, H; Vonbank, A; Rein, P; Aczel, S; Saely, CH (2013). "Eccentric endurance exercise economically improves metabolic and inflammatory risk factors". Eur J Prev Cardiol. 20 (4)): 577–84. doi: 10.1177/2047487312444236 . PMID   22505055. S2CID   39990249.

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