Maximal eccentric strength training Clinical aspects

2nd MuscleTech Network Workshop on Muscle and Tendon From Translational Research to Translational Medicine Barcelona - September 26 th -28 th 2010 Use of Resistance Training in the Prevention and Rehabilitation of Muscle-Tendon Injury: Biomechanical and Neural aspects Per Aagaard Institute of Sports Science & Clinical Biomechanics University of Southern Denmark Rehabilitation and prevention of tendinopathy problems by use of resistance training Biomechanical and Neuromuscular Aspects Maximal eccentric strength training Clinical aspects Effects of ECC strength training on muscletendon injury rehabilitation and prevention Promising results for... Achilles tendinopathy Alfredson et al, Am J Sports Med 26, 1998 Roos et al, Scand J Med Sci Sports 14, 2004 Jonsson, Alfredson et al, Br J Sports Med 42, 2008 Patella tendon pain, jumpers knee Jonsson & Alfredson, Br J Sports Med 39, 2005 Purdam et al, Br J Sports Med 38, 2004 Young et al, Br J Sports Med 39, 2005 Frohm et al, Br J Sports Med 41, 2007 Anterior patella-femoral pain Werner & Eriksson, Knee Surg Recurrent hamstring strain injury Sports Traumatol Arthrosc 1, 1993 Croisier et al, Am J Sports Med 30, 2002 Askling et al, Scand J Med Sci Sports 13, 2003 Arnason et al, Scand J Med Sci Sports 18, 2008 1

Microdialysis peritendon area PINP PICP = Carboxyterminal propeptide of type I procollagen...a marker of type I collagen synthesis in vivo Perfusate * * * Dialysate Henning Langberg, Bispebjerg Hospital ECC muscle-tendon training regime Elite soccer players with Achilles tendinopathy ECC muscle-tendon training regime collagen type I synthesis Achilles tendon Collagen synthesis [PICP (ug/l)] 20 10 Injured tendon pre and post ECC training for 12 wks * Healthy tendons contralateral untrained leg Elite soccer players with Achilles tendinopathy tendinosis No significant change in collagen I breakdown [ICTP-concentration] No change in collagen III synthesis Pre Post Pre Post * post > pre (p < 0.01) Langberg, Aagaard, Kjær et al, Scand J Med Sci Sports 2007 2

Beneficial effects of decline squat Anterior Patella pain / Jumpers knee Superior clinical and functional rehabilitation of patellar tendinopathy have been reported by use of eccentric decline squat training compared to horizontal eccentric squats Jonsson & Alfredson, Br. J. Sports Med 39(11), 2005; Purdam et al, Br. J. Sports Med 38(4), 2004; Young et al, Br. J. Sports Med 39(2), 2005 Biomechanical and neuromuscular characteristics of decline squat VS. Patella tendon strain (US) and muscle EMG amplitudes were obtained during loaded decline squats and horizontal squats Relaxed, 90 o knee angle Standard horizontal squat, 90 o knee angle Kongsgaard, Aagaard, Magnusson et al, Clin. Biomech. 2006 Decline squat, 90 o knee angle Biomechanical and neuromuscular characteristics of decline squat % of MVC 80 Knee extensor peak EMG amplitude Knee extensor peak EMG * ** ** Standard Horizontal squat Decline squat 12 10 Patella Patella Tendon Tendon Strainstrain * Standard Horizontal squat Decline squat Relative EMG (%) EMG (%) 60 40 Strain (%) (%) 8 6 4 20 2 0 vastus lat VL VM vastus RF med rectus fem 0 Horizontal squat Decline squat Kongsgaard, Aagaard, Magnusson et al, Clin. Biomech. 2006 3

Patellar tendon loading in different types of eccentric squats ECC decline board squat BromsMan Frohm, Thorstensson et al, Clin. Biomech. 2007 Patellar tendon loading in different types of eccentric squats Knee Extension Moment Patellar Tendon Force ROM Decline board squat Decline board squat: tendon force Frohm, Thorstensson et al, Clin. Biomech. 2007 Patellar tendon loading in different types of eccentric squats Kinetics at the knee joint 25 30% higher patellar tendon forces (peak and mean) during eccentric squats using a decline board compared to using horizontal eccentric squats (free weight condition). Range of motion: In addition, ROM (angular excursions) at the knee, hip and ankle joints were larger in decline board conditions Frohm, Thorstensson et al, Clin. Biomech. 2007 4

Effects of resistance training? Tendon CSA Tendon stiffness Tendon strain HEALTHY TENDONS Tendon hypertrophy reduced tendon stress ( N/m 2 ) for given level of force loading may reduce the risk of tendon overuse injury Before training force F CSA After training force F F/CSA Kongsgaard, Aagaard, Magnusson et al, Acta Physiol Scand 2007 Scand J Med Sci Sports 19, 2009 Comparing the effect of - peritendinous corticosteroid injections (CORT) - eccentric decline squats (ECC) - slow heavy-resistance strength training (HSR) on patellar tendinopathy 5

6000 4000 2000 0 0 2 4 6 Deformation (mm) Randomized, controlled & single-blinded design 12 weeks of CORT n = 12 2 peritendinous corticosteroid injections 4 weeks between each injection US-guided ECC n = 12 Training 2 times each day. 3 x 15 unilateral eccentric squats on 25 deg. decline board. Load progressively increased HSR n = 13 Training 3 times per week Leg-press, squat and hacksquat 3 x 6-15RM SLOW movements (6 sec.) Needle Kongsgaard, Aagaard, Magnusson et al, Scand J Med Sci Sports 2009 Assessment Methods Pain (VAS) Symptoms & function (VISA) Treatment satisfaction Tendon swelling Tendon neo-vascularization Tendon mechanical properties Tendon cross-link properties Tednon force (N) ½-Year follow-up Kongsgaard, Aagaard, Magnusson et al, Scand J Med Sci Sports 2009 Function (VISA-p) and Pain (VAS scoring) VISA-p 100 90 80 70 60 VISA-p ** VAS 70 60 50 40 30 20 VAS ** 50 10 40 0 0 wks 12 wks Follow-up 0 wks 12 wks Follow-up 6 months 6 months CORT VISA CORT ECC VISA ECC HSR VISA HSR ** post different from pre (p<0.01), Sign different from 12 wks Kongsgaard, Aagaard, Magnusson et al, Scand J Med Sci Sports 2009 6

Tendon size and Tendon Vascularization 9 8 ** Tendon Thickness ** Neovascularization/Colour Area ** 18000 16000 ** 14000 mm 7 6 # Pixels 12000 10000 8000 5 0 CORT ECC HSR 6000 4000 CORT ECC HSR pre post pre post ** post different from pre (p<0.01) Kongsgaard, Aagaard, Magnusson et al, Scand J Med Sci Sports 2009 Treatment satisfaction CORT - 12 WKS ECC - 12 WKS HSR - 12 WKS 42% 75% 70% Satisfied Not Satisfied CORT - FOLLOW-UP ECC - FOLLOW-UP HSR - FOLLOW-UP 36% Satisfied Not Satisfied 22% 73% * Kongsgaard, Aagaard, Magnusson et al, Scand J Med Sci Sports 2009 Study Conclusions CORT had excellent short-term but poor long-term clinical effect HSR showed superior short and long-term effects accompanied by reduced collagen cross-links and and tendency for increased collagen synthesis Tendon mechanical properties remained unaffected by tendinopathy and did not change with any treatment type Before treatment: VAS=76 After HSR: VAS=13 Kongsgaard, Aagaard, Magnusson et al, SJMSS 2009 7

Tendinopathy Tendon - Pre HSR Post HSR (heavy-resistance slow training) Tendinopathic patellar tendons display low collagen fibril density and a large mean fibril area HSR altered collagen fibril morphology: increased fibril density, reduced mean fibril area, increased number of small-sized collagen fibrils Healthy Tendon (patellar tendons) HSR Tendon CSA (prox,dist) Kongsgaard et al 2007 Tendon stiffness, Youngs Modulus Kongsgaard 2007 Tendon strain Kongsgaard et al 2007 Tendinopathy Tendon (patellar tendons) HSR tendon CSA (mid-portion) Kongsgaard et al 2009, 2010 / tendon stiffness, / Youngs Modulus 2007 & 10 Tendon strain Kongsgaard et al 2009 & 2010 Pentosidine cross-links, HP / LP ratio Kongsgaard 2009 Collagen content (tendency) Kongsgaard et al 2009 Mean collagen fibril diameter, fibril density do 2010 Collagen fibril volume fraction Kongsgaard et al 2010 8

Healthy tendons and Tendinopathy tendons may differ in adaptive training responses - proposed scheme Trained tendinopathy Tendon Trained healthy Tendon Duration of training Tendon Stiffness Tendon CSA Tendon collagen cross-links Tendon strain Rehabilitation and prevention of muscle strain disorders by use of (ECC) resistance training Biomechanical and Neuromuscular Aspects 9

Hamstring muscle strain Typical injury setting In situations of high eccentric muscle forces, typically at elongated muscle lengths Tension Length Total tension Passive tension Active tension Parallel-elastic forces >> active contractile forces High risk of sarcomere failure at the MTJ Muscle strain injury Aagaard 2008 Muscle strain injury Muscle strain injury scar tissue formation amount of type III collagen, irregular collagen fibril orientation, small collagen fibril size, reduced tensile strength of scar tissue Best et al, J Orthop Res 19, 2001 Croisier JL, Sports Med 34, 2004 Eccentric strength training is highly effective of rehabilitating and preventing recurrent Hamstring muscle strain injury Croisier et al, Am J Sports Med 30, 2002 Subjects Training group (n=18) soccer (n=14), track and field (n=7), martial arts (n=5) All sustaining unilateral hamstring strain injury Training 10 sessions x 2-5 pre and 12 months post Isokinetic eccentric hamstring training (slow: 30 o /s, fast: 180 o /s) 10

Eccentric strength training is highly effective of rehabilitating and preventing recurrent Hamstring muscle strain injury Croisier et al, Am J Sports Med 30, 2002 Training was repeated until subjects were above critical H/Q strength ratio levels: Hamstring strain reinjury 18/18 (1) H ecc /Q con > 0.98 pre: 0.73 ±.24, control leg: 0.90 (2) H con /Q con 0.57 (3) Bilateral deficit 5% Pre 0/17 Post Hamstring strain injury is reduced in elite soccer players after preseason ECC strength training Askling et al, Scand J Med Sci Sports 13, 2003 Training group (TG, n=15) Control group (CG, n=15) 16 sessions, pre-season 10 weeks (wks 1-10) maximal eccentric hamstring contractions (YoYo flywheel) maximum eccentric and concentric isokinetic hamstring strength (60 o /sec) Max 30-m run speed Hamstring strain injuries In-season injury registration over 35 wks (wks 11-46) Hamstring strain injury is reduced in elite soccer players after preseason ECC strength training Askling et al, Scand J Med Sci Sports 13, 2003 Maximal muscle strength Eccentric and concentric hamstring contraction strength increased in TG (19 and 15%, p<0.05) Maximal running speed 30-m maximal running speed improved in TG (2.4%, p<0.05), but not in the untrained players Hamstring injury rate In-season hamstring injury rate was substantially lower in trained players 3/15 TG 10/15 CG p < 0.05 11

Rehabilitation and prevention of muscle strain disorders by use of (ECC) resistance training Practical training regimes? YoYo flywheel Askling et al 2003 Isokinetic dynamometry Croiser et al 2002, Aagaard 2003-2010 Nordic Hamstring Arnason, Bahr et al 2008 What are the potential Adaptive Mechanisms evoked by ECC resistance exercise in tendon and muscle??? 12

MUSCLE-TENDON REHAB Eccentric muscle-tendon overloading seems to induce increased collagen turnover, with upregulated synthesis of beneficial collagen isoforms (type I collagen, type III collagen no change) Langberg, Aagaard et al, Scand J med Sci Sports 2007 MUSCLE-TENDON REHAB Eccentric muscle-tendon overloading seems to induce increased collagen turnover, with upregulated synthesis of beneficial collagen isoforms (type I collagen, type III collagen no change) Langberg, Aagaard et al, Scand J med Sci Sports 2007 Pre post ECC training Kongsgaard, Aagaard et al 2009 Decreased tendon vascularization (removed hyper vascularization) potential removal of epithel sensory pain receptor nerve endings Öhberg et al, Knee Surg Sports Traum Arthrosc 12, 2004 Boesen, Langberg et al, Scand J Med Sci Sports 16, 2006, Kongsgaard, Aagaard et al, Am J Sports Med 2009 MUSCLE-TENDON REHAB Maximal Eccentric muscle-tendon loading local IGF-1 expression in muscle fibers and/or fibroblasts after ECC contraction* [concentric contractions: no effect] Bamman et al. 2001, Yan et al. 1993 (*110% 1RM, 8 x 8 reps) * ECC : 110% 1RM, 8 sets x 8 reps CON : 85% 1RM, 8 sets x 8 reps 13

MUSCLE-TENDON REHAB Maximal Eccentric muscle-tendon loading local IGF-1 expression in muscle fibers and/or fibroblasts after ECC contraction* [concentric contractions: no effect] Bamman et al. 2001, Yan et al. 1993 (*110% 1RM, 8 x 8 reps) * ECC : 110% 1RM, 8 sets x 8 reps CON : 85% 1RM, 8 sets x 8 reps IGF-1 promotes de novo synthesis of muscle protein and collagen tissue, i.e. is of importance for muscle, tendon and ECM remodelling MUSCLE-TENDON REHAB Maximal ECC muscle-tendon loading Vinculin, Talin = integral cytoskeletal-ecm proteins transmitting mechanical force at myotendinous junction Frenette & Cote, Int J sports Med 2000 Focal Adhesion Complex: Integrins mechanically link the interior of the cell with the ECM Extracellular Matrix (ECM) Basal membrane Muscle cell membrane Interior of the muscle cell From Drawing Narici from & Maganaris, Narici & Maganaris, Exerc ESSR Sports 35, 2007 Sci Rew 35, 2007 14

MUSCLE-TENDON REHAB Animal experiments: ECC muscle loading may result in serial sarcomere addition, i.e. increased muscle fiber lengths Lynn & Morgan 1994, Lynn et al 1998, Butterfield et al 2005, Butterfield & Herzog 2006 MUSCLE-TENDON REHAB Animal experiments: ECC muscle loading may result in serial sarcomere addition, i.e. increased muscle fiber lengths Lynn & Morgan 1994, Lynn et al 1998, Butterfield et al 2005, Butterfield & Herzog 2006 Human experiments: ECC muscle loading led to longer muscle fascicle length [at rest], i.e. signs of increased muscle fiber length Duclay et al Muscle & Nerve 39, 2009 [gastrocnemius muscle] MUSCLE-TENDON REHAB Animal experiments: ECC muscle loading may result in serial sarcomere addition, i.e. increased muscle fiber lengths shift in the Force-Length relationship Lynn & Morgan 1994, Lynn et al 1998, Butterfield et al 2005, Butterfield & Herzog 2006 reduced sarcomere strain for a given Human experiments: ECC joint muscle Range loading of Motion (ROM) led to longer muscle fascicle length [at rest], i.e. signs of increased muscle fiber length Duclay et al Muscle & Nerve 39, 2009 [gastrocnemius muscle] 15

MUSCLE-TENDON REHAB Reduced passive muscle-tendon tension following prolonged ECC training? Mahieu et al, Med Sci Sports Exerc 40, 2008 35 non-injured subjects performed standard unilateral eccentric heel drop exercise (29 gender + age matched controls) ECC training daily, 6 weeks (Alfredson et al. 1998) MUSCLE-TENDON REHAB Reduced passive muscle-tendon tension following prolonged ECC training?...yes! Outcome: passive dorsiflexion ROM passive resistive peak torque* No change controls * ROM = 20 o plantarflexion to 10 o dorsiflexion Passive resistive torque (Nm) 20 18 16 14 12 10 8 6 4 2 0 PRE * POST training Mahieu et al, Med Sci Sports Exerc 40, 2008 16

SUMMARY Potential adaptive mechanisms evoked by ECCENTRIC muscle-tendon training SUMMARY Potential adaptive mechanisms evoked by ECCENTRIC muscle-tendon training (i) Tendon and ECM: type I collagen synthesis upregulated (ii) Increase in local production of IGF-I and other growth factors by muscle cells and/or ECM fibroblasts (iii) Increased amounts of membrane-ecm proteins involved in mechano-transduction at the MTJ (i.e. Vinculin, Talin) (iv) More sarcomeres in-series? longer muscle fibers: shift in the F-L curve, reduced sarcomere strain (v) More uniform and homogenous muscle activation pattern during maximal eccentric muscle contraction ECM-muscle fiber stress MTJ stress / strain concentrations Tendon and Muscle Fiber Strain rehabilitation Acknowledgements Coworkers at Institute of Sports Medicine Copenhagen, University of Copenhagen; Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark: Peter Magnusson Mads Kongsgaard Christian Couppe Bjarki Haraldsson Michael Kjær Henning Langberg Jens Bojsen-Møller Philip Hansen 17

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