Maximal eccentric strength training Clinical aspects

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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

2nd MuscleTech Network Workshop on Muscle and Tendon

From Translational Research to Translational Medicine Barcelona - September 26th_-28th₂₀₁₀

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 muscle-tendon injury rehabilitation and prevention Promising results for...

O 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

O 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

O Anterior patella-femoral pain Werner & Eriksson, Knee Surg Sports Traumatol Arthrosc 1, 1993

O Recurrent hamstring strain injury 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

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Microdialysis

peritendon area

Perfusate Dialysate

* *

*

Henning Langberg, Bispebjerg Hospital PICP PINP = terminal propeptide of type I procollagen ...a marker of type I collagen synthesis in vivo

Elite soccer players with Achilles tendinopathy

ECC muscle-tendon training regime

No significant change in collagen I breakdown [ICTP-concentration] No change in collagen III synthesis

Co llag e n sy nt h es is [ P IC P (u g/ l)] 20 10 Injured tendon pre and post ECC training for 12 wks

Healthy tendons

Pre Post Pre Post

Elite soccer players with Achilles tendinosis

contralateral untrained leg *

Elite soccer players with Achilles tendinopathy

ECC muscle-tendon training regime

⇒

↑

collagen type I synthesis

Achilles tendon

*post > pre (p < 0.01) Langberg, Aagaard, Kjær et al,

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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, 90o knee angle Standard horizontal squat, 90o knee angle Decline squat, 90o knee angle Kongsgaard,

Aagaard, Magnusson et al, Clin. Biomech. 2006

St ra in ( % ) 0 2 4 6 8 10 12 Standard squat Decline squat * Patella Tendon Strain Knee extensor peak EMG

Relativ e EM G ( % ) 0 20 40 60

80 Standard squatDecline squat

VL VM RF

**

* **

Knee extensor

peak EMG amplitude Patella Tendon strain

% of MVC Stra in (%) Rela tive EMG ( % ) Horizontal squat Horizontal Decline Horizontal Decline Decline squat vastus lat vastus med rectus fem

Kongsgaard, Aagaard, Magnusson et al, Clin. Biomech. 2006

Biomechanical and neuromuscular

characteristics of decline squat

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Patellar tendon loading in different types of eccentric squats

ECC decline board squat BromsMan

Frohm, Thorstensson et al, Clin. Biomech. 2007

Knee Extension Moment

Frohm, Thorstensson et al, Clin. Biomech. 2007

Patellar Tendon Force

Decline board squat:

↑ tendon force Decline board squat

↑ ROM

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

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E

ffects of resistance training?

Tendon CSA Tendon stiffness Tendon strain force F After training ↑ CSA

↓

F/CSA

HEALTHY TENDONS

Tendon hypertrophy ⇒ reduced tendon stress (↓N/m2₎

for given level of force loading Æ may reduce the risk of tendon overuse injury

force F Before

training

Kongsgaard, Aagaard, Magnusson et al, Acta Physiol Scand 2007

Comparing the effect of

- peritendinous corticosteroid injections (CORT) - eccentric decline squats (ECC)

- slow heavy-resistance strength training (HSR) … on patellar tendinopathy

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Randomized, controlled & single-blinded design

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 hack-squat 3 x 6-15RM SLOW movements (6 sec.) 12 weeks of 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 • ½-Year follow-up Deformation (mm) 0 2 4 6 Tedn on f orc e (N) 0 2000 4000 6000

VISA-p VI S A -p 40 50 60 70 80 90 100 VISA CORT VISA ECC VISA HSR 0 wks 12 wks Follow-up ** § VAS VA S 0 10 20 30 40 50 60 70 CORT ECC HSR 0 wks 12 wks Follow-up ** §

** post different from pre (p<0.01), § Sign different from 12 wks

6 months 6 months

Function

(VISA-p) and

Pain

(VAS scoring)

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Tendon Thickness CORT mm 0 5 6 7 8 9 pre post HSR ECC ** ** Neovascularization/Colour Area CORT # P ix el s 4000 6000 8000 10000 12000 14000 16000 18000 pre post HSR ECC ** **

** post different from pre (p<0.01)

Tendon size

and

Tendon Vascularization

CORT - 12 WKS Satisfied Not Satisfied ECC - 12 WKS HSR - 12 WKS 42% 75% 70%

ECC - FOLLOW-UP HSR - FOLLOW-UP

73% 22% CORT - FOLLOW-UP 36%

*

Treatment satisfaction

Satisfied Not Satisfied

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

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Tendinopathy Tendon - Pre HSR Post HSR (heavy-resistance slow training)

HSR ⇒ altered collagen fibril morphology:

increased fibril density, reduced mean fibril area, increased number of small-sized collagen fibrils Tendinopathic patellar tendons display low

collagen fibril density and a large mean fibril area

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

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Trained tendinopathy Tendon → Trained healthy Tendon Tendon Stiffness Tendon CSA Tendon collagen cross-links Tendon strain

Healthy tendons and Tendinopathy tendons may differ in adaptive training responses - proposed scheme

Duration of training

Rehabilitation and prevention of

muscle strain disorders

by

use of

(ECC)

resistance training

Biomechanical and Neuromuscular Aspects

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Hamstring muscle strain

Typical injury setting

In situations of high eccentric muscle forces, typically at elongated muscle lengths

Total tension Passive tension Active tension Length Te n si o

n >> active contractile forcesParallel-elastic 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

Training

• 10 sessions x 2-5 • pre and 12 months post Isokinetic eccentric

hamstring training (slow: 30o_{/s, fast: 180}o_/s)

Subjects

Training group (n=18) soccer (n=14), track and field (n=7), martial arts (n=5) All sustaining unilateral hamstring strain injury

Croisier et al, Am J Sports Med 30, 2002

Eccentric strength training is highly effective of rehabilitating and preventing recurrent Hamstring

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Post

0/17 18/18

Pre

Hamstring strain reinjury

Croisier et al, Am J Sports Med 30, 2002

Training was repeated until subjects were above critical H/Q strength ratio levels: (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%

Eccentric strength training is highly effective of rehabilitating and preventing recurrent Hamstring

muscle strain injury

• 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 (60o_/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

Hamstring injury rate In-season hamstring injury rate was substantially lower in trained players

p < 0.05

TG CG

10/15

3/15

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 strain injury is reduced in elite soccer players after preseason ECC strength training

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Rehabilitation and prevention of

muscle strain disorders by use of (ECC) resistance training

Practical training regimes?

Nordic Hamstring Arnason, Bahr et al 2008 YoYo flywheel Askling et al 2003 Isokinetic dynamometry Croiser et al 2002, Aagaard 2003-2010

What are the potential

Adaptive Mechanisms

evoked by ECC resistance exercise

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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 O

Potential physiological adaptation mechanisms

MUSCLE-TENDON REHAB Eccentric muscle-tendon exercise

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

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

O

Pre post ECC training Kongsgaard, Aagaard et al 2009

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)

O

* ECC : 110% 1RM, 8 sets x 8 reps CON : 85% 1RM, 8 sets x 8 reps

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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)

IGF-1 promotes de novo synthesis of muscle protein and collagen tissue, i.e. is of importance for muscle, tendon and ECM remodelling

O

* ECC : 110% 1RM, 8 sets x 8 reps CON : 85% 1RM, 8 sets x 8 reps

Maximal ECC muscle-tendon loading

⇒↑Vinculin, Talin = integral cytoskeletal-ECM proteins transmitting mechanical force at myotendinous junction

Frenette & Cote, Int J sports Med 2000 O

From Narici & Maganaris, Exerc Sports Sci Rew 35, 2007

Extracellular Matrix (ECM) Basal membrane

Muscle cell membrane

Interior of the muscle cell

Drawing from Narici & Maganaris, ESSR 35, 2007

Focal Adhesion Complex:

Integrins

mechanically link the interior of the cell with the ECM

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O

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] Potential physiological adaptation mechanisms

O

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] Potential physiological adaptation mechanisms

O

⇒ shift in the Force-Length relationship ⇒ reduced sarcomere strain for a given joint Range of Motion (ROM)

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Reduced passive muscle-tendon tension following prolonged ECC training?

Mahieu et al, Med Sci Sports Exerc 40, 2008 O

• 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)

Reduced passive muscle-tendon tension

following prolonged ECC training? ...YES!

O

Outcome:

↑passive dorsiflexion ROM

↓ passive resistive peak torque* No change controls * ROM = 20o plantarflexion to 10o dorsiflexion 0 2 4 6 8 10 12 14 16 18 20 *

PRE POST training

Passive resistive torque (Nm)

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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:

Michael Kjær Henning Langberg Jens Bojsen-Møller Philip Hansen Peter Magnusson Mads Kongsgaard Christian Couppe Bjarki Haraldsson

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