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Journal of Bodywork & Movement Therapies (2015) xx, 1e5

Available online at www.sciencedirect.com

ScienceDirect journal homepage: www.elsevier.com/jbmt

PREVENTION & REHABILITATION: EDITORIAL

About eccentric exercise A long walking descent from a mountain on the Isle of Skye some years ago taught me the effects of significant unaccustomed eccentric exercise on my quadriceps; significant pain with attendant weakness, stiffness and a 2 week rehabilitation. Each day of that recovery period the difficulty I experienced walking let me reflect that my primary exercise, cycling 60 miles (nearly 100 km) a week as my commute to work, provided no positive training effect or protection against injury, apart from perhaps a little cardio-vascular stamina. The primary muscular action in cycling is concentric (Bijker et al., 2002) while the muscular work in gait during descent is primarily eccentric. If I had, in the weeks before my trip, performed a graded eccentric overload program, I could have harnessed the repeated bout effect (McHugh, 2003) which demonstrates protection from eccentric muscle injury with later, more intense doses of eccentric work. My sequential left then right concentric quadricep shortening during the alternate downstroke on my pedals, was matched by the concentric use of both the gluteals and hamstrings. The posterior muscles initially provide hip extension, then a hamstring led concentric knee flexion (with the assistance of the pedal pushing the leg in the upstroke to the top of the crank). The all concentric pedalling action means there was no eccentric dosing in my usual muscular activities and no protection from injury from the unaccustomed hillwalking. I had climbed up the mountain first but the bias of uphill gait had been gluteal and hamstring concentric work in mid ranges, which was already a familiar task, with perhaps some carry over from the cycling, but, despite the substantially greater metabolic cost during the concentric work of ascent, it was the lengthened quadriceps eccentric deceleration of greater than body weight loads, fast motor unit dominant activity, which had injured my knee extensors. Hoppeler (2015) identifies that ‘the bulk of skeletal muscle consists of contractile proteins which is usually seen as responsible for muscle shortening (i.e. concentric contraction). It is often overlooked that in natural locomotion, just as often muscles do not shorten during activation but rather resist lengthening (i.e. perform eccentric contractions).’ He states that the 2 main purposes of eccentric contraction are to ‘dissipate energy for deceleration’ e and he uses downhill walking as the key

description of that purpose e and to ‘convert kinetic and potential energy into elastic strain energy of tendons and aponeuroses which occurs in the early stance phase of locomotion’, as is delivered ‘during limb support to minimise muscle work’ thus conserving energy. In short, eccentric work decelerates and stores energy. The way the human body responds to the actions of concentric and eccentric muscle contractions can be different. Which suggests that focussing on certain aspects of the physiological rules that muscles obey while working can be harnessed by a therapist when trying to achieve rehabilitative goals. Muscle fibre recruitment follows Hennemann’s size principle (Henneman, 1957) which reduces the metabolic cost of muscular work activity by recruiting the slow twitch, fatigue resistant motor units first then the larger fast fatigue resistant motor units before finally recruiting the largest fast fatiguing motor units for high intensity tasks such as jumping. Hoppeler quotes Hodson-Tole and Wakeling (2009) whose paper suggests that this classic pattern doesn’t always happen and that preferential fast motor unit contraction can happen in (rapid shortening and) rapid lengthening situations e such as eccentric muscle work. This suggests utilising fast eccentric contractions in exercise can selectively develop strength in the fast motor units, perhaps reducing the time taken to hypertrophy fast muscle fibres. The difference in force production between concentric and eccentric contractions is also significantly different. An eccentric contraction produces a sharp rise of force production several fold larger than a concentric contraction of the same velocity (Hoppeler, 2015; Brooks and Faulkner, 1994). Again suggesting further efficiencies possible with eccentric training. Eccentric contractions appear to only require half the electromyography (EMG) activity of concentric contractions of similar torque (Hoppeler, 2015), suggesting a lower perception of effort may be felt by an individual undertaking an eccentric load. Hoppeler describes a 1952 experiment (Abbott et al., 1952) in which two bicycles were placed back to back with one on rollers, and the others back wheel was free. A single bicycle chain connected the two. The cyclist on the

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2 roller could cycle concentrically, the other cyclist would resist the load and be cycling eccentrically. The experiment was to estimate the energy requirements of the ‘negative’ work (i.e. eccentric work). It was found that the physiological cost of the negative work was 3.5 times less than that of the positive (concentric) work, and, furthermore, at higher loads the negative work was at an even greater ratio e 6 times less than the corresponding positive work. This indicates that active muscle fibres use intrinsically less oxygen when being stretched than when being shortened. Hoppeler agrees that eccentric contraction can induce muscle injury ‘which is symptomatically associated with delayed onset muscle soreness (DOMS).’ DOMS typically presents 24 h post exercise though with significant eccentric contraction induced muscle injury immediate loss of muscle force can occur along with muscle swelling. This can be up to 50% of pre-exercise values. Recovery can be slow, taking several days, though more significant injury takes longer. Concentric contraction muscle injuries force loss is typically moderate with a 10e30% loss, but it typically recovers within hours (Hoppeler, 2015). As eccentric loads can be greater than concentric loads during training, Hoppeler suggests that eccentric loads can be up to 30% more than the concentric phase of the movement. He identifies that in a free weight gym a training partner can be used to apply more load in the eccentric phase, though specialist equipment has been developed to apply greater eccentric loads. One such ‘eccentric resistance strength trainer’ e the Eccentron has a marketing benefits list that succinctly summarises the assets of eccentric training, this is quoted verbatim (web source 1).  ‘Muscles resist force rather than produce it, requiring 80% less oxygen compared to of eccentric exercise concentric work  Low perceived exertion, so clients comfortably produce higher force output than in traditional concentric exercise  Body can resist 30e40% more weight eccentrically than it can push concentrically  Eccentric training helps enhance concentric abilities  Eccentric training promotes muscle growth and strength  High load eccentrics deliver proven benefits, including faster responses and greater workloads  Specificity of exercise, from ADLs to sports performance, offers a means to training for functional activities, including descending stairs, lowering loads, jumping, deceleration,etc  Eccentric training builds up type II (fast twitch) muscle fibers, for:  Enhanced overall athletic performance e power, “spring quality,” reaction, agility  Improved stability in stair descent and standing balance  Increased functional control and performance in activities of daily living’

Eccentric exercise in rehabilitation The best known application of eccentric exercise within the rehabilitative sphere has been in the treatment of

Prevention & rehabilitation: Editorial tendinopathies, though treatment protocols have been developed to cover muscle injury such as: hamstring strains (Askling et al., 2003; Heiderscheit et al., 2010) see Fig. 1 (Lorenz, and Reiman, 2011), post operative rehabilitation of anterior cruciate ligament repair (Gerber et al., 2009; Saka, 2014), post operative rehabilitation of both total knee replacements (Bade et al., 2012) and total hip replacements (Di Monaco et al., 2009), Rotator cuff injuries (Robb et al., 2009), and Sub acromial impingement syndrome (Holmgren et al., 2012). Hoppeler bemoans the lack of high quality multi-centre studies with a high number of subjects, comparing this field of research unfavourably with drug trials and predicting that there will be little change in the future.

Tendinopathy and eccentric exercise Tendonitis describes an inflammatory reaction of a tendon, which, on investigation proved not to be the key reason patients presented with pain, stiffness and a loss of function related to mechanical loading overuse related tendon problems. Khan et al. (1999) suggested that these problems should be described as Tendinopathies. Khan further suggested that the ‘effective treatment of athletes with tendinopathies must target the most common underlying histopathology, tendinosis, a non-inflammatory condition.’ Khan ascribes the first use of the term tendinosis to German workers in the 1940’s but the modern use stems from the work of Puddu et al. (1976). Khan described tendinosis as ‘tendon degeneration without clinical or histological signs of an inflammatory response, often associated with ageing, micro-trauma and vascular compromise’. Maffulli et al. (2003) characterise tendinosis as a failed healing response. Histologically the type 1 collagen fibres separate and lose their parallel orientation and a greater number of reparative type 3 collagen fibres are found. Joseph and Denegar (2015) identify intrinsic and extrinsic factors that lead to the development of tendinopathy or rupture. Advancing age and gender, namely men, genetics, and limb mechanics are the intrinsic factors and extrinsic factors include activity level, footwear, training technique, and surface type for both Achilles and patella tendinopathy. They identify loading history but point out that the threshold of overload is still currently poorly understood and that, ‘the quantification of appropriate load (volume, intensity, and frequency) for optimal tendon function remains elusive.’ Importantly Joseph and Denegar point out the fact that appropriate load on tendons is anabolic e constructive at the cellular level, and overloading is catabolic e destructive e to tendon tissue. They highlight the seemingly contradictory benefit seen with eccentric exercise. Adding load to a tendinosis which is a degenerative tendon is ‘counterintuitive,’ but the tenocyte (the tendon constructing cell) may well be stimulated anabolically by eccentric exercise and create its positive response, though, they point out, not in all cases. A certain percentage of those undergoing eccentric training for tendinosis fail e and this group may end up with a surgical repair. Tendonosis does not have to be painful which is why sometimes an Achilles tendon can rupture with no warning.

Please cite this article in press as: McNeill, W., About eccentric exercise, Journal of Bodywork & Movement Therapies (2015), http:// dx.doi.org/10.1016/j.jbmt.2015.05.002

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Prevention & rehabilitation: Editorial

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Fig. 1 The nordic hamstring lower is described as a partner exercise, biasing the eccentric lowering of body weight with (A.) the partner anhoring the feet, while the subject (B.) controls a lean forward till (C.) the point that the subject either experiences the beginning of their pain or they cannot control the load, when they are instructed to allow (D.) their fall to the floor catching with their upper limbs. There is a concentric element to this exercise in the return for the repeat but it is reduced by using the upper limbs to push off the floor back to the start position. Askling et al (2003) protocol for eccentric exercise looking at hamstring injury prevention in soccer player involved eccentric training in addition to typical soccer training, this occurred 1 to 2 times a week for 10 weeks. The eccentric training group had significantly fewer hamstring injuries (3 out of 15) compared to the control group (10 out of 15) as well as showing significant improvements in strength and speed.

So a seemingly healthy tendon ruptures and the surgeon repairing it finds the tendon markedly degenerative. Cook and Purdum (2009) have suggested a Continuum model with 3, probably overlapping, stages. These are: reactive tendinopathy, tendon disrepair (failed healing) and degenerative tendinopathy. ‘Reactive tendinopathy is proposed to occur in response to acute overload and is described as a noninflammatory proliferative response. Tendon disrepair resembles the initial stage of reactivity but with greater matrix disorganisation, neovascularity and neuronal ingrowth and represent an aspect of attempted but failed repair’, say Joseph and Denegar, and suggest that ‘evidence exists that the tendon can recover in form and function from this stage with appropriate treatment inclusive of load modulation and eccentric exercise stimulus. Degenerative Tendinopathy e tendinosis e is thought to be largely irreversible.’ In the clinic Joseph and Denegar divide this 3 part continuum into 2 e an ‘acute reactive’ and ‘late degenerative’ phase and suggest that the 2 phases may require different approaches in treatment. With the acute reactive phase requiring decreased tendon stress (decreased intensity of

exercise, relative rest and increased rest periods) and perhaps non steroidal anti-inflammatory drugs (NSAID’s), not to control inflammation, but for their ability to control the over proliferation of prostaglandins and ground substance. Steroids might convey short term pain relief but increase risk of rupture. So their use needs careful consideration, they suggest. The late degenerative phase focus of treatment could include eccentric exercise and extracorporeal shockwave therapy (ESWT). The Eccentric protocol for the Achilles Tendon can be read as a blueprint for how eccentric loading can be applied to other, especially lower limb, tendons. Achilles tendon injury diagnosis is reported by Cook et al. (2002) as being one of the ‘simpler clinical diagnosis to make’ as the change in activity levels that often precede the start of the pain is often remembered. The Achilles tendon needs, from the first step out of bed in the morning, to work in almost full range e which means that morning pain is a hallmark of the condition. The Victorian Institute of Sport Assessment (VISA-A) has been developed and is a reliable and valid outcome measurement tool (Robinson et al., 2001). The Eccentric exercise protocols for

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4 both the Achilles (and patella tendon) are based on the work of Alfredson (1998, 2005), see Fig. 2. They consist of heel drops off a step. The protocols involve no concentric action on the affected limb but a transfer of weight to the non-affected side to raise the heel and a transfer back to the injured side for the eccentric drop. Three sets are advocated by Alfredson (2005) of a 15RM (Repetitive maximum) exercise involving both a knee straight gastrocnemius biased eccentric exercise and a knee bent soleus biased one. As this is a big commitment for some patients a modification of the set numbers has been advocated by Stevens and Tan (2014) with still good results. Raising the load level can be achieved by providing a weighted back pack. Modifications to the protocol such as using the reformer, or an under slung sprung push through bar in a pilates equipped studio/clinic and altering the spring loading tension to gain the correct 15RM load, appears reasonable. Speed of lengthening is another factor that can

Prevention & rehabilitation: Editorial be altered by the therapist in charge the rehabilitation process. Pain during the eccentric loading, according to Joseph and Denegar, is ok, but persisting pain suggests an alteration to decrease the work rate or load is required. A Patella tendinosis regime utilises the same protocol but uses a decline squat exercise on an incline board. Eccentric exercise as a tool has its place in the rehabilitation of various sporting and age related musculoskeletal conditions. It is regarded as an effective tool particularly for tendinopathies, but it is the peculiar response of muscle to a loaded lengthening force, which is different to the response in a muscle to a concentric contraction that allows a therapist to achieve greater strengthening at less physiological cost. Eccentric exercise can apply load to the connective elements of the movement system to alter the histology with the view to effect positive change. Further reading of the 2015 Hoppeler text

Fig. 2 The Alfredson ‘painful’ heel drop protocol avoids concentric contraction on the injured side. Instructions to the patient are; (A.) Stand on a step on the uninjured side. (B.) lift heel. (C.) Transfer weight on to the left (in this example) planter flexed injured side. Keeping the knee straight to bias the gastrocnemius. (D.) Lower the heel. After the weight transfer, (E.) bias the soleus by bending the knee. (F.) Drop the heel keeping the knee bent. The protocol suggests 3 sets of 15 repetitions twice a day, every day for 12 weeks, in both the straight leg gastrocnemius variation and the bent knee soleus version. This is 180 repetitions a day. The Alfredson protocol allows for the patient to push into discomfort while performing the task but not for pain to persist. Once pain decreases, increase load by adding to the body weight, keeping to the 15 repetitions.

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Prevention & rehabilitation: Editorial will elucidate a reader wanting to find out significantly more about this subject.

In this P&R section This Prevention and Rehabilitation section of the Journal of Bodywork and Movement Therapies serves to highlight papers relevant to the day to day work of therapists. As Professor Shirley Sahrmann has repeated many times in her career, and I paraphrase, ‘It is in the ‘repeated movements’, and, ‘sustained postures’ of your clients that you find the causes of their musculoskeletal issues.’ A repeated movement is discussed in ‘Does anterior knee pain severity and function relate to the frontal plane projection angle and trunk and hip strength in women with patellofemoral pain?’ (Almeida et al.) and sustained (poor) postures are discussed in the second paper, ‘Common postural defects among music students’ (Blanco-Pin ˜eiro et al.). Our job is to recognise the causes and ‘sell’ the fix to our clients who may well prefer a more passive but less effective solution.

References Abbott, B.C., Bigland, B., Ritchie, J.M., 1952. The physiological cost of negative work. J. Physiol. 117, 380e390. Alfredson, H., 2005. The chronic painful Achilles and patellar tendon: research on basic biology and treatment. Scand. J. Med. Sci. Sports 15, 252e259. Alfredson, H., Pietila, T., Jonsson, P., Lorentzon, R., 1998. Heavyload eccentric calf muscle training for the treatment of chronic Achilles tendinosis. Am. J. Sports Med. 26, 360e366. Almeida et al. doi:10.1016/j.jbmt.2015.01.004. Askling, C., Karlsson, J., Thorstensson, A., 2003. Hamstring injury occurrence in elite soccer players after preseason strength training with eccentric overload. Scand. J. Med. Sci. Sports 13 (4), 244e250. Bade, M.J., Stevens- Lapsley, J.E., 2012. Restoration of physical function in patients following total knee arthroplasty: an update on rehabilitation practices. Curr. Opin. Rheumatol. 24, 208e214. Bijker, K.E., de Groot, G., Hollander, A.P., 2002 Oct. Differences in leg muscle activity during running and cycling in humans. Eur. J. Appl. Physiol. 87 (6), 556e561. Blanco-Pin ˜eiro et al. doi:10.1016/j.jbmt.2015.04.005. Brooks, S.V., Faulkner, J.A., 1994. Isometric, shortening, and lengthening contractions of muscle fiber segments from adult and old mice. Am. J. Physiol. 267, C507eC513. Cook, J.L., Purdam, C.R., 2009. Is tendon pathology a continuum? A pathology model to explain the clinical presentation of loadinduced tendinopathy. Br. J. Sports Med. 43, 409e416. Cook, J.L., Khan, K.M., Perdham, C., 2002. Masterclass: Achilles tendinopathy. Man. Ther. 7 (3), 121e130. Di Monaco, M., Vallero, F., Tappero, R., Cavanna, A., 2009. Rehabilitation after total hip arthroplasty: a systematic review of controlled trials on physical exercise programs. Eur. J. Phys. Rehabil. Med. 45, 303e317. Gerber, J.P., Marcus, R.L., Dibble, L.E., Greis, P.E., Burks, R.T., La Stayo, P.C., 2009 Jan. Effects of early progressive eccentric

5 exercise on muscle size and function after anterior cruciate ligament reconstruction: a 1-year follow-up study of a randomized clinical trial. Phys. Ther. 89 (1), 51e59. Epub 2008 Nov 6. Heiderscheit, B.C., Sherry, M.A., Silder, A., Chumanov, E.S., Thelen, D.G., 2010. Hamstring strain injuries: recommendations for diagnosis, rehabilitation, and injury prevention. J. Orthop. Sports Phys. Ther. 40, 67e81. Henneman, E., 1957. Relation between size of neurons and their susceptibility to discharge. Science 126, 1345e1347. Hodson-Tole, E.F., Wakeling, J.M., 2009. Motor unit recruitment for dynamic tasks: current understanding and future directions. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 179, 57e66. Holmgren, T., Bjornsson Hallgren, H., Oberg, B., Adolfsson, L., Johansson, K., 2012. Effect of specific exercise strategy on need for surgery in patients with subacromial impingement syndrome: randomised controlled study. Br. Med. J. 344, e787. Hoppeler, Hans, 2015. Eccentric Exercise: Physiology and Application in Sport and Rehabilitation. Routlegde. Joseph, M.F., Denegar, C.R., 2015. Treating tendinopathy perspective on anti-inflammatory intervention and therapeutic exercise. Clin. Sports Med. 34, 363e374. Khan, K.M., Cook, J.L., Bonar, F., Harcourt, P., Astrom, M., 1999. Histopathology of common tendinopathies. Update and implications for clinical management. Sports Med. 27 (6), 393e408. June. Lorenz, D., Reiman, M., 2011. The role and implementation of eccentric training in athletic rehabilitation: tendinopathy, hamstring strains, and ACL reconstruction. Int. J. Sports Phys. Ther. 6, 27e44. Maffulli, N., Wong, J., Almekinders, L.C., 2003. Types and epidemiology of tendinopathy. Clin. Sports Med. 22, 675e692. McHugh, M.P., 2003. 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 13, 88e97. Puddu, G., Ippolito, E., Postacchini, F., 1976. A classification of Achilles tendon disease. Am. J. Sports Med. 4, 145e150. Robb, G., Arroll, B., Reid, D., Goodyear-Smith, F., 2009. Summary of an evidence-based guideline on soft tissue shoulder injuries and related disorders e part 2: management. J. Prim. Health Care 1, 42e49. Robinson, J.M., Cook, J.L., Purdam, C., Visentini, P.J., Ross, J., MaVulli, N., Taunton, J.E., Khan, K.M., 2001. The VISA-A questionnaire: a valid and reliable index of the clinical severity of Achilles tendinopathy. Br. J. Sports Med. 35, 335e341. Saka, T., 2014. Principles of postoperative anterior cruciate ligament rehabilitation. World J. Orthop. 5 (4), 450e459. Stevens, M., Tan, C.W., 2014. Effectiveness of the Alfredson protocol compared with a lower repetition-volume protocol for midportion Achilles tendinopathy: a randomized controlled trial. J. Orthop. Sports Phys. Ther. 44, 59e67. Web source 1. http://www.btetech.com/lit/collateral/BTEEccentron-Why-Eccentrics.pdf.

Warrick McNeill, Dip. Phyty. (NZ) MCSP * Physioworks, 53 Wimpole Street, London W1G 8YH, UK *Tel.: þ44 7973 122996. E-mail address: [email protected]

Please cite this article in press as: McNeill, W., About eccentric exercise, Journal of Bodywork & Movement Therapies (2015), http:// dx.doi.org/10.1016/j.jbmt.2015.05.002

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