12
8/20/2019 45-11 Couppe 2 http://slidepdf.com/reader/full/45-11-couppe-2 1/12 See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/282911158 Eccentric or Concentric Exercises for the Treatment of Tendinopathies?  ARTICLE · OCTOBER 2015 DOI: 10.2519/jospt.2015.5910 READS 128 5 AUTHORS, INCLUDING: Christian Couppé University of Copenhagen 28 PUBLICATIONS  739 CITATIONS SEE PROFILE Rene B Svensson University of Copenhagen 16 PUBLICATIONS  203 CITATIONS SEE PROFILE Karin Grävare Silbernagel University of Delaware 53 PUBLICATIONS  1,059 CITATIONS SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, letting you access and read them immediately. Available from: Christian Couppé Retrieved on: 09 November 2015

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See discussions stats and author profiles for this publication at httpwwwresearchgatenetpublication282911158

Eccentric or Concentric Exercises for theTreatment of Tendinopathies

ARTICLE middot OCTOBER 2015

DOI 102519jospt20155910

READS

128

5 AUTHORS INCLUDING

Christian Couppeacute

University of Copenhagen28 PUBLICATIONS 739 CITATIONS

SEE PROFILE

Rene B Svensson

University of Copenhagen16 PUBLICATIONS 203 CITATIONS

SEE PROFILE

Karin Graumlvare Silbernagel

University of Delaware

53 PUBLICATIONS 1059 CITATIONS

SEE PROFILE

All in-text references underlined in blue are linked to publications on ResearchGate

letting you access and read them immediately

Available from Christian Couppeacute

Retrieved on 09 November 2015

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 853

[ CLINICAL COMMENTARY ]

1Institute o Sports Medicine Copenhagen Bispebjerg Hospital Copenhagen Denmark 2Department o Orthopaedic Surgery Bispebjerg Hospital Copenhagen Denmark 3Centeror Healthy Aging Faculty o Health and Medical Sciences University o Copenhagen Copenhagen Denmark 4Musculoskeletal Rehabilitation Research Unit Department oPhysical Therapy Bispebjerg Hospital Copenhagen Denmark 5Department o Physical Therapy University o Delaware Newark DE 6CopenRehab Department o Public HealthUniversity o Copenhagen Copenhagen Denmark The authors certiy that they have no affiliations with or financial involvement in any organization or entity with a direct financialinterest in the subject matter or materials discussed in the article Address correspondence to Dr S Peter Magnusson Institute o Sports Medicine Copenhagen BispebjergHospital Bispebjerg Bakke 23 2400 Copenhagen NV Denmark E-mail pmagnussonsundkudk 983156 Copyright copy2015 Journal of Orthopaedic amp Sports Physical Therapyreg

983156SYNOPSIS Tendinopathy is a very commondisorder in both recreational and elite athletesMany individuals have recurrent symptoms thatlead to chronic conditions and termination osports activity Exercise has become a popularand somewhat efficacious treatment regime andisolated eccentric exercise has been particularlypromoted In this clinical commentary we reviewthe relevant evidence or different exercise regimesin tendinopathy rehabilitation with particular ocus

on the applied loads that are experienced by thetendon and how the exercise regime may affectthese applied loads There is no convincing clinicalevidence to demonstrate that isolated eccentricloading exercise improves clinical outcomes morethan other loading therapies However the great

variation and sometimes insufficient reporting o

the details o treatment protocols may hamper theinterpretation o what may be the optimal exerciseregime with respect to parameters such as load

magnitude speed o movement and recoveryperiod between exercise sessions Future studiesshould control or these loading parameters

evaluate various exercise dosages and thinkbeyond isolated eccentric exercises to arrive at

firm recommendations regarding rehabilitation o

individuals with tendinopathies J Orthop Sports

Phys Ther 201545(11)853-863 Epub 14 Oct 2015

doi102519jospt20155910

983156KEY WORDS Achilles forces load patellar

recovery tendon

Tendon tissue plays an essential role in transmitting muscle

contractile forces to produce movement and is therefore

uniquely designed to withstand considerable loads Duringlocomotion the Achilles and patellar tendons may see forces

up to approximately 8 times body weight233162 Repetitive loading of

a tendon often results in overuse injuries including tendinopathy which is a clinical condition characterized by pain in the area of the

Tendinopathy is the commonly ac-

cepted term for the clinical condition in

and around overloaded tendons46 These

injuries were previously considered to be

the result of a prolonged inflammatory

condition (chronic tendinitis)90

How-ever more recently the extent to which

inflammation plays a role in chronic ten-

dinopathy has been debated256380 The

slow insidious onset of tendinopathy

makes it difficult to identify the start of

the condition in humans and efforts to

develop animal models to study the early

events of the condition have been incon-

sistent3235 Therefore the definitive role

of inflammation in the early stages of the

condition remains difficult to investigate

Notwithstanding these limitations it has been shown that tendon tissue from in-

dividuals with Achilles tendinopathy

does not display an elevated expression

of inflammatory markers after 1 hour of

running77 Rather than inflamed tendon

tissue obtained from individuals with ten-

dinopathy is typically more cellular than

healthy tissue and displays both signs of

general tissue degeneration including

collagen degeneration and necrosis as

well as signs of regeneration including

neovascularization irregular fiber struc-ture and increased ground substance

(see Fredberg and Stengaard-Pedersen25)

Tendinopathy is a substantial clinical

challenge because it can severely limit

sports participation for months and po-

CHRISTIAN COUPPEacute PT PhD1-4 bull RENEacute B SVENSSON PhD1-3 bull KARIN GRAumlVARE SILBERNAGEL PT ATC PhD5

HENNING LANGBERG PT PhD DSc6 bull S PETER MAGNUSSON PT DSc1-4

Eccentric or Concentric Exercisesfor the Treatment of Tendinopathies

tendon during activity localized tender-

ness on palpation local swelling of the

tendon and impaired performance4560

Tendinopathy is a sizable problem in both

elite and recreational athletes222793 Spe-

cifically the incidence of tendon injuries

has been estimated to be as high as 30

to 50 of all sports injuries and 50 of

injuries to elite endurance runners and6 of sedentary people will at some point

experience a tendon injury5258 Moreover

the symptoms and reduction in perfor-

mance may last for an extended period

potentially years4457 The exact injury

mechanism remains elusive but an un-

derstanding of how tendon tissue adapts

to mechanical loading could be the key

to understanding the pathogenesis of

tendinopathy and thus provide the basisfor prevention of overuse injuries

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854 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

tentially years444 The list of currently

available interventions for this clinical

condition is extensive and may include

surgery nonsteroidal anti-inflammatory

drugs corticosteroids sclerosing injec-

tion shockwave therapy platelet-rich

plasma injection intratendinous hyper-

osmolar dextrose (prolotherapy) injec-

tion high-volume injections of 10 mL05 bupivacaine and 40 mL normal

saline into the paratenon Kinesio Tape

and therapeutic ultrasound just to men-

tion a few8192 Although these and other

treatment options are described in the

literature various loading interventions

have predominated in the treatment of

tendinopathies64 It seems that loading

paradigms yield positive clinical26188

structural50 and biochemical outcomes49

Much of the attention on loading pro-

grams as a treatment paradigm for thesechallenging injuries originated from an

article published by Stanish et al90 in

1986 In this article the loading regime

was described as a stretch-shortening

exercise that is an eccentric component

rapidly followed by a concentric com-

ponent For example in the case of the

patellar tendon ldquoThe patient from a

standing position flexes the knees and

drops to a squatting position abruptly

then recoils to the standing positionrdquo90

The progression of the exercise protocol

with abating symptoms was described

as increasing the speed of the movement

and thereafter an external load was add-

ed for additional progression90

Approximately a decade later it was

suggested that isolated eccentric contrac-

tion alone without the accompanying

concentric component of a stretch-short-ening cycle provided good clinical results

for patients with tendinopathy4 This

isolated eccentric loading paradigm has

since gained considerable popularity and

is now widely regarded as the treatment

of choice although there is a lack of con-

vincing evidence that it is the most effec-

tive exercise regime64 More recently new

loading-based exercise regimes such as

isolated concentric training61 heavy slow

resistance training949 and concentric

eccentric progressing to eccentric train-ing8889 have emerged This article focus-

es on the underlying rationale of these

various loading paradigms

Response of Healthy Tendon to LoadIt is well established that exercise in gen-

eral can affect both skeletal muscle38 and

tendon48 In tendon there is an acute

increase in blood flow and collagen syn-

thesis5455 and long-term effects lead to

tissue hypertrophy and altered material

properties128598 The magnitude and type

of adaptation likely depend on the ex-

ercise regime including the magnitude

of the load range of motion performed

contraction mode (eccentric lengthening

concentric shortening) movement speed

number of repetitions and rest periods

between the exercise sessions By varying

these components a wide range of exer-cise programs can be constructed from

endurance (low load high speed many

repetitions) to strength (high load low

speed few repetitions) programs with

myriad combinations in between The

response of tendon to the various exer-

cise parameters will be discussed in the

following sections though knowledge on

several matters remains limited

It is well known that the tendon cells

(fibroblasts) respond to mechanical stim-

uli in the form of strain426696

and thatdepriving them of strain (relative tissue

deformation) leads to degeneration and

apoptosis (cell death)71799 However the

dose response to strain magnitude is still

not well established Cell-culture experi-

ments suggest that there is an increased

response (increased collagen expression

reduced matrix metalloproteinase ex-

pression and increased matrix stiffness)

with increased strain56101 but there may

be an optimal strain beyond which the

No Load

A B

24

15

22

16

20

16

22

16

24

15

C D E

Body Weight

Concentric

Body Weight Body Weight

Eccentric

No Load

FIGURE 1 Schematic illustration o concentric and eccentric muscle contraction about the ankle joint Numbers illustrate lengths (not to scale) (A) During concentric heelrise the tendon and muscle are initially relaxed (B) As muscle shortens orce is generated causing the tendon to lengthen until sufficient orce has been reached and the heelbegins to rise (C) While muscle shortens ur ther the heel continues to rise under approximately constant orce and due to the constant load the length o tendon also remains

constant (D) In the eccentric phase the heel drops as muscle lengthens still at approximately constant orce and consequently tendon retains its length (E) Finally themuscle lengthens as it is relaxed and tendon shortens because load is removed Note that across the schematics tendon length is determined by the amount o load carriedindependent o muscle length

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 855

stretching becomes detrimental4168 The

absolute values of strain used in cell-

culture stimulation vary greatly and it is

uncertain how much of a given strain the

cells will experience in vivo because thesurrounding matrix may provide shield-

ing In vivo in healthy human Achilles

tendons it has been reported that with

equal exercise volume working at 90 of

maximum voluntary contraction (MVC)

which causes approximately 5 tendon

strain yields increased stiffness and

cross-sectional area compared to work-

ing at 55 MVC which causes approxi-

mately 3 tendon strain5

Speed andor duration of loading dur-

ing exercise also appear to be importantfor tendon adaptation6415156 At the cellu-

lar level most304197 but not all21 studies

have found that the adaptive response of

fibroblasts to dynamic load is superior to

that of static load (zero speed) Though

the response to different dynamic load re-

gimes is complex due to the interaction

of the parameters overall the evidence

suggests that increased time under load

increased number of load cycles and

increased loading rate result in a posi-

tive adaptive response (increased ma-trix strength and stiffness and decreased

matrix metalloproteinase expression) in

cultured fibroblasts4156100 The response

appears to be a bit different in vivo where

it has been reported that the stiffness

and size (cross-sectional area) of human

Achilles tendon were more responsive to

a low number of loads of long duration

(6-second cycle) than to a high number of

faster loads (2-second cycle) when the to-

tal exercise volume was kept constant56

This finding is corroborated somewhat by another study showing that isometric

contractions of long duration (20 sec-

onds) yielded greater patellar tendon ad-

aptation (increased stiffness) than rapid

(1-second) contractions at equal exer-

cise volume51 In the latter study muscle

strength and volume adaptation were un-

affected by contraction duration

It is unknown whether tendon cells

experience some form of fatigue as a re-

sult of repeated load cycles Tendon cells

have a low metabolic rate and probably

do not require rest for the purpose of re-

storing energy deposits However the an-

abolic response to loading is sustained in

tendon for up to several days following anexercise bout5565 which could indicate the

need for a postexercise recovery period63

But conversely studies on cell culture

have performed continuous stimulation

of fibroblasts for up to 24 hours per day

without detrimental effects4159 and most

exercise protocols for tendinopathy man-

agement are performed every day with-

out recovery periods46789 Overall there

is a lack of studies specifically addressing

the effects of recovery and how it affects

tendon adaptationThe majority of the tendon is com-

posed of extracellular matrix (ECM)

which is a passive structure and un-

like the cells does not actively respond

to load though it may still be differen-

tially affected by exercise parameters It

has been suggested that accumulation

of microdamage may be involved in the

etiology of tendinopathy 87 and because

the turnover in tendons is slow34 ECM

damage could accumulate Microdamage

is difficult to measure and its clinical rel-evance is therefore unclear However if it

does play a role it would be an argument

in favor of recovery periods Mechanical

studies have shown that both overload-

ing and mechanical fatigue can cause

damage to tendon ECM4372 which could

play a role in tendinopathy The tendon

ECM is also a viscoelastic material which

means that slower loading regimes can

yield greater strains than faster loading

regimes as the tendon has more time to

creep74

Creep also appears to be associ-ated with greater relative fibril slippage24

which may generate local shear strains

sensed by the cells Slow loading may

therefore produce particularly strong cell

stimuli that can be beneficial to the ten-

don if the strain is sufficient but could be

detrimental if strain is excessive This vis-

coelastic behavior depends on the amount

of time the tendon is under load and is

therefore unaffected by the mode of mus-

cle contraction (eccentric or concentric)

In summary tendon is responsive to

loading and will respond more strongly

to greater loads although there is likely

an optimum beyond which load becomes

detrimental Slower loading regimes may

be superior to rapid loading while theimportance of recovery between loading

sessions is unclear

Tendon Under Eccentric andConcentric Muscle Contractions

Although isolated eccentric loading re-

gimes for tendinopathy have been widely

accepted as the treatment of choice92 the

potential mechanisms behind this inter-

vention remain unclear In the following

section we discuss some of the proposed

mechanisms and their potential applica-tions in light of existing evidence

Strictly speaking the descriptions

ldquoconcentricrdquo and ldquoeccentricrdquo only apply to

muscle which actively contracts Tendon

is a mechanically passive structure that

lengthens when load increases and short-

ens when load is reduced (FIGURE 1) It is

therefore questionable whether the mode

of muscle contraction for a given load and

range of motion would have a differen-

tial effect on tendon tissue The fact that

07

095 10 105

08

09

10

11

12

13

14

F o r c e M e a n F o r c e

LengthMean Length (mm)

FIGURE 2 Achilles tendon orce versus Achillestendon length Eccentric data are shown as opencircles whereas concentric data are filled circles

Reprinted with permission rom Chaudhry SMorrissey D Woledge RC Bader DL Screen HREccentric and concentric loading o the tricepssurae an in vivo study o dynamic muscle andtendon biomechanical parameters J Appl Biomech

20153169-78 copyHuman Kinetics Inc

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856 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

muscles can produce greater maximal

force eccentrically than concentrically

would suggest a potential for greater me-

chanical stimulation from eccentric than

from concentric exercise1837

According-ly it has been suggested that the tendon

may stretch more during eccentric load-

ing than concentric loading190 However

while there is a potential for greater ten-

don load and consequently stretch with

eccentric exercise this potential is rarely

utilized because rehabilitation exercises

seldom approach concentric 1-repeti-

tion maximum It has been shown that

Achilles tendon load and stretch are

identical during the concentric and ec-

centric components of a heel risedropagainst body weight (FIGURE 2) a typi-

cal load used in rehabilitation1179 The 2

most commonly used eccentric exercises

for tendinopathy are squats for the patel-

lar tendon and standing heel lowering for

the Achilles tendon and both movements

are typically performed to a 15-repetition

maximum4103

TABLES 1 and 2 list the number of week-

ly repetitions and estimated loads used in

several eccentric exercise regimes pub-

lished in the literature It should be notedthat several studies have used an individ-

ualized load progression but they seldom

report the actual amount achieved only

the starting load It is also worth noting

that most studies do not include a control

group which is likely due to ethical con-

cerns therefore it is uncertain whether

the provided treatment was in fact supe-

rior to a ldquowait and seerdquo approach Howev-

er most of these studies included patients

with chronic symptoms suggesting that

time alone would not have improvedtheir condition

A few theoretical mechanisms have

been suggested to explain how eccentric

loading may differentially influence ten-

don For example during heel-lowering

raising tasks the ground reaction force

may fluctuate at a higher frequency (ap-

proximately 10 Hz) during the eccentric

phase367984 While tendon cells could

potentially register this modulation the

magnitude of the modulation is quite

small compared to the total load (ap-

proximately 10) It has also been pro-

posed that motor unit activation differs between concentric and eccentric exer-

cises18 which may produce a difference

in load distribution and shear within the

tendon although such a mechanism is

unlikely to be a factor for the patellar ten-

don in which load is distributed via the

patella Finally secreted signaling mol-

ecules from the muscle (myokines) such

as interleukin 6 (IL-6)75 could potentially

affect the nearby tendon and myokine

expression may differ between concen-

tric and eccentric exercise although the

effects are currently unclear7394

In contrast to these hypothetical con-siderations there is evidence to suggest

that eccentric and concentric muscle

contractions do not yield a differential re-

sponse of the tendon In animal models

it has been shown that concentric or ec-

centric contraction to the same force level

does not influence the expression of col-

lagen at the cellular level29 In fact even if

the eccentric muscular contraction force

were greater than concentric contraction

force both contraction modes would yield

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy

StudyGroup Load Pain Improvementdagger

Alredson et al4

Isolated ECC 1260 (100)Daggersect VAS 94

Croisier et al13

Isolated ECC 135 (130) VAS 73 (10 wk)

Alredson and Lorentzon3

Isolated ECC 1260 (100)Daggersect VAS 75

Oumlhberg and Alredson70

Isolated ECC 1260 (100)Daggersect Pain during activity reduced 88

Roos et al83

Isolated ECC 1260 (100)Daggersect Foot and Ankle Outcome Score 36

Shalabi et al86

Isolated ECC 1260 (100)Daggersect 6-point pain scale 40

de Vos et al16

Isolated ECC 1260 (100)Daggersect VISA-A 78

Langberg et al53

Isolated ECC 1260 (120)Daggersect VAS 71

Petersen et al76

Isolated ECC 1890 (100)Daggersect VAS 60

Yelland et al102

Isolated ECC 1260 (100)Daggersect VISA-A 38

Silbernagel et al88

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

VISA-A 60

Rompe et al82

Isolated ECC 1260 (100)Daggersect VISA-A 49 (16 wk)para

Wait and see 0 (0) VISA-A 14 (16 wk)

Table continues on page 857

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 857

similar expressions of collagen33 These

animal findings imply that given a suf-

ficiently high force (and resulting strain

on the fibroblast) the contraction modeis inconsequential for the tendon cellu-

lar response A recent study examined

the effect of contraction mode on tendon

(and muscle) hypertrophy in healthy hu-

man subjects20 The 12-week resistance

training consisted of isolated concentric

knee extensions on one side and eccentric

knee extensions on the contralateral side

The sets repetitions and time of load-

ing were similar between sides but the

loading for the eccentric side was 120

that of the concentric side The results

showed that resistance training with ei-

ther concentric or eccentric contraction

produced a similar magnitude of tendonhypertrophy20 These findings reinforce

the notion that the cellular and tissue re-

sponse in healthy tendon is independent

of contraction mode

In summary there are a number of

mechanisms that could theoretically

differentiate the effect of eccentric from

concentric exercise on tendon but there

is no evidence that these mechanisms

actually play a role or are beneficial In

contrast there is evidence from animal

and human studies that suggests a lack

of differential effect of eccentric versus

concentric exercises

The Effects of Muscle ContractionRegimes on TendinopathyBoth elite and recreational athletes are

frequently afflicted by Achilles andor

patellar tendinopathy5257 The clinical lit-

erature has mainly focused on use of ec-

centric loading exercise in the treatment

of these tendinopathies and therefore the

following sections on Achilles and patellar

tendinopathy will first cover the clinical

studies that have investigated the effects

of eccentric loading followed by studies

that have investigated the effects of othertypes of loading exercises TABLES 1 and 2

cover the clinical studies on Achilles and

patellar tendinopathy with load reported

as weekly repetitions and estimated load

as a percentage of body weight

The Effect of Eccentric Muscle Contrac-

tion on Achilles Tendon It has been

shown that eccentric-loading regimens

for Achilles tendinopathy can provide

clinical improvements including reduc-

tion in pain and improved function15478892

Several studies313

have employed the iso-lated eccentric-loading paradigm initially

introduced by Alfredson et al4 When this

exercise model is performed as unilateral

heel drop the force placed on the ten-

don is a function of body weight and the

force can be modulated with additional

weight placed in a backpack worn by the

patient In addition to improvements in

pain and function it appears that struc-

tural features observed with ultrasound

and magnetic resonance imaging are al-

tered following isolated eccentric loadingin some28707186 but not all studies14697682

It has also been shown that in addition to

decreasing pain isolated eccentric load-

ing can result in increased synthesis of

type I collagen53 Thus isolated eccentric

loading appears to influence biochemical

and biomechanical parameters and im-

prove clinical outcomes The beneficial

effects of isolated eccentric loading with

body weight appear to be reduced if the

pain is located toward the tendon inser-

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric KOOS Knee injury Osteoarthritis Outcome Score

VAS visual analog scale VISA-A Victorian Institute of Sport Assessment-Achilles Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Noslashrregaard et al69

Isolated ECC 1260 (100)Daggersect Modified KOOS-score improved 25

Stretching Stretching Modified KOOS-score improved 25

Beyer et al9

Isolated ECC 1260 (100)Daggersect VISA-A 24VAS 59

Heavy slow resistance (ECC + CON) 144 (130)Dagger VISA-A 41VAS 69

Mafi et al61

Isolated ECC 1260 (100)Daggersect Satisfied 82para

VAS o satisfied 83

Isolated CON plus jump plus rope skipping 1260 (100)Dagger Satisfied 32VAS o satisfied 86

Niesen-Vertommen et al67

Isolated ECC 300 (55)sect VAS 78para

Mixed ECC + CON 300 (25)sect VAS 46

Silbernagel et al89

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

Pain during activity reduced 57

Mixed ECC + CON 1260 (50) or 315 (100)sect Pain during activity reduced 80

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858 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

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13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

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Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

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93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

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a randomized clinical trial Clin J Sport Med200515227-234

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mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

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66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 853

[ CLINICAL COMMENTARY ]

1Institute o Sports Medicine Copenhagen Bispebjerg Hospital Copenhagen Denmark 2Department o Orthopaedic Surgery Bispebjerg Hospital Copenhagen Denmark 3Centeror Healthy Aging Faculty o Health and Medical Sciences University o Copenhagen Copenhagen Denmark 4Musculoskeletal Rehabilitation Research Unit Department oPhysical Therapy Bispebjerg Hospital Copenhagen Denmark 5Department o Physical Therapy University o Delaware Newark DE 6CopenRehab Department o Public HealthUniversity o Copenhagen Copenhagen Denmark The authors certiy that they have no affiliations with or financial involvement in any organization or entity with a direct financialinterest in the subject matter or materials discussed in the article Address correspondence to Dr S Peter Magnusson Institute o Sports Medicine Copenhagen BispebjergHospital Bispebjerg Bakke 23 2400 Copenhagen NV Denmark E-mail pmagnussonsundkudk 983156 Copyright copy2015 Journal of Orthopaedic amp Sports Physical Therapyreg

983156SYNOPSIS Tendinopathy is a very commondisorder in both recreational and elite athletesMany individuals have recurrent symptoms thatlead to chronic conditions and termination osports activity Exercise has become a popularand somewhat efficacious treatment regime andisolated eccentric exercise has been particularlypromoted In this clinical commentary we reviewthe relevant evidence or different exercise regimesin tendinopathy rehabilitation with particular ocus

on the applied loads that are experienced by thetendon and how the exercise regime may affectthese applied loads There is no convincing clinicalevidence to demonstrate that isolated eccentricloading exercise improves clinical outcomes morethan other loading therapies However the great

variation and sometimes insufficient reporting o

the details o treatment protocols may hamper theinterpretation o what may be the optimal exerciseregime with respect to parameters such as load

magnitude speed o movement and recoveryperiod between exercise sessions Future studiesshould control or these loading parameters

evaluate various exercise dosages and thinkbeyond isolated eccentric exercises to arrive at

firm recommendations regarding rehabilitation o

individuals with tendinopathies J Orthop Sports

Phys Ther 201545(11)853-863 Epub 14 Oct 2015

doi102519jospt20155910

983156KEY WORDS Achilles forces load patellar

recovery tendon

Tendon tissue plays an essential role in transmitting muscle

contractile forces to produce movement and is therefore

uniquely designed to withstand considerable loads Duringlocomotion the Achilles and patellar tendons may see forces

up to approximately 8 times body weight233162 Repetitive loading of

a tendon often results in overuse injuries including tendinopathy which is a clinical condition characterized by pain in the area of the

Tendinopathy is the commonly ac-

cepted term for the clinical condition in

and around overloaded tendons46 These

injuries were previously considered to be

the result of a prolonged inflammatory

condition (chronic tendinitis)90

How-ever more recently the extent to which

inflammation plays a role in chronic ten-

dinopathy has been debated256380 The

slow insidious onset of tendinopathy

makes it difficult to identify the start of

the condition in humans and efforts to

develop animal models to study the early

events of the condition have been incon-

sistent3235 Therefore the definitive role

of inflammation in the early stages of the

condition remains difficult to investigate

Notwithstanding these limitations it has been shown that tendon tissue from in-

dividuals with Achilles tendinopathy

does not display an elevated expression

of inflammatory markers after 1 hour of

running77 Rather than inflamed tendon

tissue obtained from individuals with ten-

dinopathy is typically more cellular than

healthy tissue and displays both signs of

general tissue degeneration including

collagen degeneration and necrosis as

well as signs of regeneration including

neovascularization irregular fiber struc-ture and increased ground substance

(see Fredberg and Stengaard-Pedersen25)

Tendinopathy is a substantial clinical

challenge because it can severely limit

sports participation for months and po-

CHRISTIAN COUPPEacute PT PhD1-4 bull RENEacute B SVENSSON PhD1-3 bull KARIN GRAumlVARE SILBERNAGEL PT ATC PhD5

HENNING LANGBERG PT PhD DSc6 bull S PETER MAGNUSSON PT DSc1-4

Eccentric or Concentric Exercisesfor the Treatment of Tendinopathies

tendon during activity localized tender-

ness on palpation local swelling of the

tendon and impaired performance4560

Tendinopathy is a sizable problem in both

elite and recreational athletes222793 Spe-

cifically the incidence of tendon injuries

has been estimated to be as high as 30

to 50 of all sports injuries and 50 of

injuries to elite endurance runners and6 of sedentary people will at some point

experience a tendon injury5258 Moreover

the symptoms and reduction in perfor-

mance may last for an extended period

potentially years4457 The exact injury

mechanism remains elusive but an un-

derstanding of how tendon tissue adapts

to mechanical loading could be the key

to understanding the pathogenesis of

tendinopathy and thus provide the basisfor prevention of overuse injuries

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[ CLINICAL COMMENTARY ]

tentially years444 The list of currently

available interventions for this clinical

condition is extensive and may include

surgery nonsteroidal anti-inflammatory

drugs corticosteroids sclerosing injec-

tion shockwave therapy platelet-rich

plasma injection intratendinous hyper-

osmolar dextrose (prolotherapy) injec-

tion high-volume injections of 10 mL05 bupivacaine and 40 mL normal

saline into the paratenon Kinesio Tape

and therapeutic ultrasound just to men-

tion a few8192 Although these and other

treatment options are described in the

literature various loading interventions

have predominated in the treatment of

tendinopathies64 It seems that loading

paradigms yield positive clinical26188

structural50 and biochemical outcomes49

Much of the attention on loading pro-

grams as a treatment paradigm for thesechallenging injuries originated from an

article published by Stanish et al90 in

1986 In this article the loading regime

was described as a stretch-shortening

exercise that is an eccentric component

rapidly followed by a concentric com-

ponent For example in the case of the

patellar tendon ldquoThe patient from a

standing position flexes the knees and

drops to a squatting position abruptly

then recoils to the standing positionrdquo90

The progression of the exercise protocol

with abating symptoms was described

as increasing the speed of the movement

and thereafter an external load was add-

ed for additional progression90

Approximately a decade later it was

suggested that isolated eccentric contrac-

tion alone without the accompanying

concentric component of a stretch-short-ening cycle provided good clinical results

for patients with tendinopathy4 This

isolated eccentric loading paradigm has

since gained considerable popularity and

is now widely regarded as the treatment

of choice although there is a lack of con-

vincing evidence that it is the most effec-

tive exercise regime64 More recently new

loading-based exercise regimes such as

isolated concentric training61 heavy slow

resistance training949 and concentric

eccentric progressing to eccentric train-ing8889 have emerged This article focus-

es on the underlying rationale of these

various loading paradigms

Response of Healthy Tendon to LoadIt is well established that exercise in gen-

eral can affect both skeletal muscle38 and

tendon48 In tendon there is an acute

increase in blood flow and collagen syn-

thesis5455 and long-term effects lead to

tissue hypertrophy and altered material

properties128598 The magnitude and type

of adaptation likely depend on the ex-

ercise regime including the magnitude

of the load range of motion performed

contraction mode (eccentric lengthening

concentric shortening) movement speed

number of repetitions and rest periods

between the exercise sessions By varying

these components a wide range of exer-cise programs can be constructed from

endurance (low load high speed many

repetitions) to strength (high load low

speed few repetitions) programs with

myriad combinations in between The

response of tendon to the various exer-

cise parameters will be discussed in the

following sections though knowledge on

several matters remains limited

It is well known that the tendon cells

(fibroblasts) respond to mechanical stim-

uli in the form of strain426696

and thatdepriving them of strain (relative tissue

deformation) leads to degeneration and

apoptosis (cell death)71799 However the

dose response to strain magnitude is still

not well established Cell-culture experi-

ments suggest that there is an increased

response (increased collagen expression

reduced matrix metalloproteinase ex-

pression and increased matrix stiffness)

with increased strain56101 but there may

be an optimal strain beyond which the

No Load

A B

24

15

22

16

20

16

22

16

24

15

C D E

Body Weight

Concentric

Body Weight Body Weight

Eccentric

No Load

FIGURE 1 Schematic illustration o concentric and eccentric muscle contraction about the ankle joint Numbers illustrate lengths (not to scale) (A) During concentric heelrise the tendon and muscle are initially relaxed (B) As muscle shortens orce is generated causing the tendon to lengthen until sufficient orce has been reached and the heelbegins to rise (C) While muscle shortens ur ther the heel continues to rise under approximately constant orce and due to the constant load the length o tendon also remains

constant (D) In the eccentric phase the heel drops as muscle lengthens still at approximately constant orce and consequently tendon retains its length (E) Finally themuscle lengthens as it is relaxed and tendon shortens because load is removed Note that across the schematics tendon length is determined by the amount o load carriedindependent o muscle length

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 855

stretching becomes detrimental4168 The

absolute values of strain used in cell-

culture stimulation vary greatly and it is

uncertain how much of a given strain the

cells will experience in vivo because thesurrounding matrix may provide shield-

ing In vivo in healthy human Achilles

tendons it has been reported that with

equal exercise volume working at 90 of

maximum voluntary contraction (MVC)

which causes approximately 5 tendon

strain yields increased stiffness and

cross-sectional area compared to work-

ing at 55 MVC which causes approxi-

mately 3 tendon strain5

Speed andor duration of loading dur-

ing exercise also appear to be importantfor tendon adaptation6415156 At the cellu-

lar level most304197 but not all21 studies

have found that the adaptive response of

fibroblasts to dynamic load is superior to

that of static load (zero speed) Though

the response to different dynamic load re-

gimes is complex due to the interaction

of the parameters overall the evidence

suggests that increased time under load

increased number of load cycles and

increased loading rate result in a posi-

tive adaptive response (increased ma-trix strength and stiffness and decreased

matrix metalloproteinase expression) in

cultured fibroblasts4156100 The response

appears to be a bit different in vivo where

it has been reported that the stiffness

and size (cross-sectional area) of human

Achilles tendon were more responsive to

a low number of loads of long duration

(6-second cycle) than to a high number of

faster loads (2-second cycle) when the to-

tal exercise volume was kept constant56

This finding is corroborated somewhat by another study showing that isometric

contractions of long duration (20 sec-

onds) yielded greater patellar tendon ad-

aptation (increased stiffness) than rapid

(1-second) contractions at equal exer-

cise volume51 In the latter study muscle

strength and volume adaptation were un-

affected by contraction duration

It is unknown whether tendon cells

experience some form of fatigue as a re-

sult of repeated load cycles Tendon cells

have a low metabolic rate and probably

do not require rest for the purpose of re-

storing energy deposits However the an-

abolic response to loading is sustained in

tendon for up to several days following anexercise bout5565 which could indicate the

need for a postexercise recovery period63

But conversely studies on cell culture

have performed continuous stimulation

of fibroblasts for up to 24 hours per day

without detrimental effects4159 and most

exercise protocols for tendinopathy man-

agement are performed every day with-

out recovery periods46789 Overall there

is a lack of studies specifically addressing

the effects of recovery and how it affects

tendon adaptationThe majority of the tendon is com-

posed of extracellular matrix (ECM)

which is a passive structure and un-

like the cells does not actively respond

to load though it may still be differen-

tially affected by exercise parameters It

has been suggested that accumulation

of microdamage may be involved in the

etiology of tendinopathy 87 and because

the turnover in tendons is slow34 ECM

damage could accumulate Microdamage

is difficult to measure and its clinical rel-evance is therefore unclear However if it

does play a role it would be an argument

in favor of recovery periods Mechanical

studies have shown that both overload-

ing and mechanical fatigue can cause

damage to tendon ECM4372 which could

play a role in tendinopathy The tendon

ECM is also a viscoelastic material which

means that slower loading regimes can

yield greater strains than faster loading

regimes as the tendon has more time to

creep74

Creep also appears to be associ-ated with greater relative fibril slippage24

which may generate local shear strains

sensed by the cells Slow loading may

therefore produce particularly strong cell

stimuli that can be beneficial to the ten-

don if the strain is sufficient but could be

detrimental if strain is excessive This vis-

coelastic behavior depends on the amount

of time the tendon is under load and is

therefore unaffected by the mode of mus-

cle contraction (eccentric or concentric)

In summary tendon is responsive to

loading and will respond more strongly

to greater loads although there is likely

an optimum beyond which load becomes

detrimental Slower loading regimes may

be superior to rapid loading while theimportance of recovery between loading

sessions is unclear

Tendon Under Eccentric andConcentric Muscle Contractions

Although isolated eccentric loading re-

gimes for tendinopathy have been widely

accepted as the treatment of choice92 the

potential mechanisms behind this inter-

vention remain unclear In the following

section we discuss some of the proposed

mechanisms and their potential applica-tions in light of existing evidence

Strictly speaking the descriptions

ldquoconcentricrdquo and ldquoeccentricrdquo only apply to

muscle which actively contracts Tendon

is a mechanically passive structure that

lengthens when load increases and short-

ens when load is reduced (FIGURE 1) It is

therefore questionable whether the mode

of muscle contraction for a given load and

range of motion would have a differen-

tial effect on tendon tissue The fact that

07

095 10 105

08

09

10

11

12

13

14

F o r c e M e a n F o r c e

LengthMean Length (mm)

FIGURE 2 Achilles tendon orce versus Achillestendon length Eccentric data are shown as opencircles whereas concentric data are filled circles

Reprinted with permission rom Chaudhry SMorrissey D Woledge RC Bader DL Screen HREccentric and concentric loading o the tricepssurae an in vivo study o dynamic muscle andtendon biomechanical parameters J Appl Biomech

20153169-78 copyHuman Kinetics Inc

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856 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

muscles can produce greater maximal

force eccentrically than concentrically

would suggest a potential for greater me-

chanical stimulation from eccentric than

from concentric exercise1837

According-ly it has been suggested that the tendon

may stretch more during eccentric load-

ing than concentric loading190 However

while there is a potential for greater ten-

don load and consequently stretch with

eccentric exercise this potential is rarely

utilized because rehabilitation exercises

seldom approach concentric 1-repeti-

tion maximum It has been shown that

Achilles tendon load and stretch are

identical during the concentric and ec-

centric components of a heel risedropagainst body weight (FIGURE 2) a typi-

cal load used in rehabilitation1179 The 2

most commonly used eccentric exercises

for tendinopathy are squats for the patel-

lar tendon and standing heel lowering for

the Achilles tendon and both movements

are typically performed to a 15-repetition

maximum4103

TABLES 1 and 2 list the number of week-

ly repetitions and estimated loads used in

several eccentric exercise regimes pub-

lished in the literature It should be notedthat several studies have used an individ-

ualized load progression but they seldom

report the actual amount achieved only

the starting load It is also worth noting

that most studies do not include a control

group which is likely due to ethical con-

cerns therefore it is uncertain whether

the provided treatment was in fact supe-

rior to a ldquowait and seerdquo approach Howev-

er most of these studies included patients

with chronic symptoms suggesting that

time alone would not have improvedtheir condition

A few theoretical mechanisms have

been suggested to explain how eccentric

loading may differentially influence ten-

don For example during heel-lowering

raising tasks the ground reaction force

may fluctuate at a higher frequency (ap-

proximately 10 Hz) during the eccentric

phase367984 While tendon cells could

potentially register this modulation the

magnitude of the modulation is quite

small compared to the total load (ap-

proximately 10) It has also been pro-

posed that motor unit activation differs between concentric and eccentric exer-

cises18 which may produce a difference

in load distribution and shear within the

tendon although such a mechanism is

unlikely to be a factor for the patellar ten-

don in which load is distributed via the

patella Finally secreted signaling mol-

ecules from the muscle (myokines) such

as interleukin 6 (IL-6)75 could potentially

affect the nearby tendon and myokine

expression may differ between concen-

tric and eccentric exercise although the

effects are currently unclear7394

In contrast to these hypothetical con-siderations there is evidence to suggest

that eccentric and concentric muscle

contractions do not yield a differential re-

sponse of the tendon In animal models

it has been shown that concentric or ec-

centric contraction to the same force level

does not influence the expression of col-

lagen at the cellular level29 In fact even if

the eccentric muscular contraction force

were greater than concentric contraction

force both contraction modes would yield

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy

StudyGroup Load Pain Improvementdagger

Alredson et al4

Isolated ECC 1260 (100)Daggersect VAS 94

Croisier et al13

Isolated ECC 135 (130) VAS 73 (10 wk)

Alredson and Lorentzon3

Isolated ECC 1260 (100)Daggersect VAS 75

Oumlhberg and Alredson70

Isolated ECC 1260 (100)Daggersect Pain during activity reduced 88

Roos et al83

Isolated ECC 1260 (100)Daggersect Foot and Ankle Outcome Score 36

Shalabi et al86

Isolated ECC 1260 (100)Daggersect 6-point pain scale 40

de Vos et al16

Isolated ECC 1260 (100)Daggersect VISA-A 78

Langberg et al53

Isolated ECC 1260 (120)Daggersect VAS 71

Petersen et al76

Isolated ECC 1890 (100)Daggersect VAS 60

Yelland et al102

Isolated ECC 1260 (100)Daggersect VISA-A 38

Silbernagel et al88

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

VISA-A 60

Rompe et al82

Isolated ECC 1260 (100)Daggersect VISA-A 49 (16 wk)para

Wait and see 0 (0) VISA-A 14 (16 wk)

Table continues on page 857

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 857

similar expressions of collagen33 These

animal findings imply that given a suf-

ficiently high force (and resulting strain

on the fibroblast) the contraction modeis inconsequential for the tendon cellu-

lar response A recent study examined

the effect of contraction mode on tendon

(and muscle) hypertrophy in healthy hu-

man subjects20 The 12-week resistance

training consisted of isolated concentric

knee extensions on one side and eccentric

knee extensions on the contralateral side

The sets repetitions and time of load-

ing were similar between sides but the

loading for the eccentric side was 120

that of the concentric side The results

showed that resistance training with ei-

ther concentric or eccentric contraction

produced a similar magnitude of tendonhypertrophy20 These findings reinforce

the notion that the cellular and tissue re-

sponse in healthy tendon is independent

of contraction mode

In summary there are a number of

mechanisms that could theoretically

differentiate the effect of eccentric from

concentric exercise on tendon but there

is no evidence that these mechanisms

actually play a role or are beneficial In

contrast there is evidence from animal

and human studies that suggests a lack

of differential effect of eccentric versus

concentric exercises

The Effects of Muscle ContractionRegimes on TendinopathyBoth elite and recreational athletes are

frequently afflicted by Achilles andor

patellar tendinopathy5257 The clinical lit-

erature has mainly focused on use of ec-

centric loading exercise in the treatment

of these tendinopathies and therefore the

following sections on Achilles and patellar

tendinopathy will first cover the clinical

studies that have investigated the effects

of eccentric loading followed by studies

that have investigated the effects of othertypes of loading exercises TABLES 1 and 2

cover the clinical studies on Achilles and

patellar tendinopathy with load reported

as weekly repetitions and estimated load

as a percentage of body weight

The Effect of Eccentric Muscle Contrac-

tion on Achilles Tendon It has been

shown that eccentric-loading regimens

for Achilles tendinopathy can provide

clinical improvements including reduc-

tion in pain and improved function15478892

Several studies313

have employed the iso-lated eccentric-loading paradigm initially

introduced by Alfredson et al4 When this

exercise model is performed as unilateral

heel drop the force placed on the ten-

don is a function of body weight and the

force can be modulated with additional

weight placed in a backpack worn by the

patient In addition to improvements in

pain and function it appears that struc-

tural features observed with ultrasound

and magnetic resonance imaging are al-

tered following isolated eccentric loadingin some28707186 but not all studies14697682

It has also been shown that in addition to

decreasing pain isolated eccentric load-

ing can result in increased synthesis of

type I collagen53 Thus isolated eccentric

loading appears to influence biochemical

and biomechanical parameters and im-

prove clinical outcomes The beneficial

effects of isolated eccentric loading with

body weight appear to be reduced if the

pain is located toward the tendon inser-

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric KOOS Knee injury Osteoarthritis Outcome Score

VAS visual analog scale VISA-A Victorian Institute of Sport Assessment-Achilles Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Noslashrregaard et al69

Isolated ECC 1260 (100)Daggersect Modified KOOS-score improved 25

Stretching Stretching Modified KOOS-score improved 25

Beyer et al9

Isolated ECC 1260 (100)Daggersect VISA-A 24VAS 59

Heavy slow resistance (ECC + CON) 144 (130)Dagger VISA-A 41VAS 69

Mafi et al61

Isolated ECC 1260 (100)Daggersect Satisfied 82para

VAS o satisfied 83

Isolated CON plus jump plus rope skipping 1260 (100)Dagger Satisfied 32VAS o satisfied 86

Niesen-Vertommen et al67

Isolated ECC 300 (55)sect VAS 78para

Mixed ECC + CON 300 (25)sect VAS 46

Silbernagel et al89

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

Pain during activity reduced 57

Mixed ECC + CON 1260 (50) or 315 (100)sect Pain during activity reduced 80

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858 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

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13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

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different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

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Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

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Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

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93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

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a randomized clinical trial Clin J Sport Med200515227-234

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mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

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64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

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2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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854 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

tentially years444 The list of currently

available interventions for this clinical

condition is extensive and may include

surgery nonsteroidal anti-inflammatory

drugs corticosteroids sclerosing injec-

tion shockwave therapy platelet-rich

plasma injection intratendinous hyper-

osmolar dextrose (prolotherapy) injec-

tion high-volume injections of 10 mL05 bupivacaine and 40 mL normal

saline into the paratenon Kinesio Tape

and therapeutic ultrasound just to men-

tion a few8192 Although these and other

treatment options are described in the

literature various loading interventions

have predominated in the treatment of

tendinopathies64 It seems that loading

paradigms yield positive clinical26188

structural50 and biochemical outcomes49

Much of the attention on loading pro-

grams as a treatment paradigm for thesechallenging injuries originated from an

article published by Stanish et al90 in

1986 In this article the loading regime

was described as a stretch-shortening

exercise that is an eccentric component

rapidly followed by a concentric com-

ponent For example in the case of the

patellar tendon ldquoThe patient from a

standing position flexes the knees and

drops to a squatting position abruptly

then recoils to the standing positionrdquo90

The progression of the exercise protocol

with abating symptoms was described

as increasing the speed of the movement

and thereafter an external load was add-

ed for additional progression90

Approximately a decade later it was

suggested that isolated eccentric contrac-

tion alone without the accompanying

concentric component of a stretch-short-ening cycle provided good clinical results

for patients with tendinopathy4 This

isolated eccentric loading paradigm has

since gained considerable popularity and

is now widely regarded as the treatment

of choice although there is a lack of con-

vincing evidence that it is the most effec-

tive exercise regime64 More recently new

loading-based exercise regimes such as

isolated concentric training61 heavy slow

resistance training949 and concentric

eccentric progressing to eccentric train-ing8889 have emerged This article focus-

es on the underlying rationale of these

various loading paradigms

Response of Healthy Tendon to LoadIt is well established that exercise in gen-

eral can affect both skeletal muscle38 and

tendon48 In tendon there is an acute

increase in blood flow and collagen syn-

thesis5455 and long-term effects lead to

tissue hypertrophy and altered material

properties128598 The magnitude and type

of adaptation likely depend on the ex-

ercise regime including the magnitude

of the load range of motion performed

contraction mode (eccentric lengthening

concentric shortening) movement speed

number of repetitions and rest periods

between the exercise sessions By varying

these components a wide range of exer-cise programs can be constructed from

endurance (low load high speed many

repetitions) to strength (high load low

speed few repetitions) programs with

myriad combinations in between The

response of tendon to the various exer-

cise parameters will be discussed in the

following sections though knowledge on

several matters remains limited

It is well known that the tendon cells

(fibroblasts) respond to mechanical stim-

uli in the form of strain426696

and thatdepriving them of strain (relative tissue

deformation) leads to degeneration and

apoptosis (cell death)71799 However the

dose response to strain magnitude is still

not well established Cell-culture experi-

ments suggest that there is an increased

response (increased collagen expression

reduced matrix metalloproteinase ex-

pression and increased matrix stiffness)

with increased strain56101 but there may

be an optimal strain beyond which the

No Load

A B

24

15

22

16

20

16

22

16

24

15

C D E

Body Weight

Concentric

Body Weight Body Weight

Eccentric

No Load

FIGURE 1 Schematic illustration o concentric and eccentric muscle contraction about the ankle joint Numbers illustrate lengths (not to scale) (A) During concentric heelrise the tendon and muscle are initially relaxed (B) As muscle shortens orce is generated causing the tendon to lengthen until sufficient orce has been reached and the heelbegins to rise (C) While muscle shortens ur ther the heel continues to rise under approximately constant orce and due to the constant load the length o tendon also remains

constant (D) In the eccentric phase the heel drops as muscle lengthens still at approximately constant orce and consequently tendon retains its length (E) Finally themuscle lengthens as it is relaxed and tendon shortens because load is removed Note that across the schematics tendon length is determined by the amount o load carriedindependent o muscle length

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 855

stretching becomes detrimental4168 The

absolute values of strain used in cell-

culture stimulation vary greatly and it is

uncertain how much of a given strain the

cells will experience in vivo because thesurrounding matrix may provide shield-

ing In vivo in healthy human Achilles

tendons it has been reported that with

equal exercise volume working at 90 of

maximum voluntary contraction (MVC)

which causes approximately 5 tendon

strain yields increased stiffness and

cross-sectional area compared to work-

ing at 55 MVC which causes approxi-

mately 3 tendon strain5

Speed andor duration of loading dur-

ing exercise also appear to be importantfor tendon adaptation6415156 At the cellu-

lar level most304197 but not all21 studies

have found that the adaptive response of

fibroblasts to dynamic load is superior to

that of static load (zero speed) Though

the response to different dynamic load re-

gimes is complex due to the interaction

of the parameters overall the evidence

suggests that increased time under load

increased number of load cycles and

increased loading rate result in a posi-

tive adaptive response (increased ma-trix strength and stiffness and decreased

matrix metalloproteinase expression) in

cultured fibroblasts4156100 The response

appears to be a bit different in vivo where

it has been reported that the stiffness

and size (cross-sectional area) of human

Achilles tendon were more responsive to

a low number of loads of long duration

(6-second cycle) than to a high number of

faster loads (2-second cycle) when the to-

tal exercise volume was kept constant56

This finding is corroborated somewhat by another study showing that isometric

contractions of long duration (20 sec-

onds) yielded greater patellar tendon ad-

aptation (increased stiffness) than rapid

(1-second) contractions at equal exer-

cise volume51 In the latter study muscle

strength and volume adaptation were un-

affected by contraction duration

It is unknown whether tendon cells

experience some form of fatigue as a re-

sult of repeated load cycles Tendon cells

have a low metabolic rate and probably

do not require rest for the purpose of re-

storing energy deposits However the an-

abolic response to loading is sustained in

tendon for up to several days following anexercise bout5565 which could indicate the

need for a postexercise recovery period63

But conversely studies on cell culture

have performed continuous stimulation

of fibroblasts for up to 24 hours per day

without detrimental effects4159 and most

exercise protocols for tendinopathy man-

agement are performed every day with-

out recovery periods46789 Overall there

is a lack of studies specifically addressing

the effects of recovery and how it affects

tendon adaptationThe majority of the tendon is com-

posed of extracellular matrix (ECM)

which is a passive structure and un-

like the cells does not actively respond

to load though it may still be differen-

tially affected by exercise parameters It

has been suggested that accumulation

of microdamage may be involved in the

etiology of tendinopathy 87 and because

the turnover in tendons is slow34 ECM

damage could accumulate Microdamage

is difficult to measure and its clinical rel-evance is therefore unclear However if it

does play a role it would be an argument

in favor of recovery periods Mechanical

studies have shown that both overload-

ing and mechanical fatigue can cause

damage to tendon ECM4372 which could

play a role in tendinopathy The tendon

ECM is also a viscoelastic material which

means that slower loading regimes can

yield greater strains than faster loading

regimes as the tendon has more time to

creep74

Creep also appears to be associ-ated with greater relative fibril slippage24

which may generate local shear strains

sensed by the cells Slow loading may

therefore produce particularly strong cell

stimuli that can be beneficial to the ten-

don if the strain is sufficient but could be

detrimental if strain is excessive This vis-

coelastic behavior depends on the amount

of time the tendon is under load and is

therefore unaffected by the mode of mus-

cle contraction (eccentric or concentric)

In summary tendon is responsive to

loading and will respond more strongly

to greater loads although there is likely

an optimum beyond which load becomes

detrimental Slower loading regimes may

be superior to rapid loading while theimportance of recovery between loading

sessions is unclear

Tendon Under Eccentric andConcentric Muscle Contractions

Although isolated eccentric loading re-

gimes for tendinopathy have been widely

accepted as the treatment of choice92 the

potential mechanisms behind this inter-

vention remain unclear In the following

section we discuss some of the proposed

mechanisms and their potential applica-tions in light of existing evidence

Strictly speaking the descriptions

ldquoconcentricrdquo and ldquoeccentricrdquo only apply to

muscle which actively contracts Tendon

is a mechanically passive structure that

lengthens when load increases and short-

ens when load is reduced (FIGURE 1) It is

therefore questionable whether the mode

of muscle contraction for a given load and

range of motion would have a differen-

tial effect on tendon tissue The fact that

07

095 10 105

08

09

10

11

12

13

14

F o r c e M e a n F o r c e

LengthMean Length (mm)

FIGURE 2 Achilles tendon orce versus Achillestendon length Eccentric data are shown as opencircles whereas concentric data are filled circles

Reprinted with permission rom Chaudhry SMorrissey D Woledge RC Bader DL Screen HREccentric and concentric loading o the tricepssurae an in vivo study o dynamic muscle andtendon biomechanical parameters J Appl Biomech

20153169-78 copyHuman Kinetics Inc

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856 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

muscles can produce greater maximal

force eccentrically than concentrically

would suggest a potential for greater me-

chanical stimulation from eccentric than

from concentric exercise1837

According-ly it has been suggested that the tendon

may stretch more during eccentric load-

ing than concentric loading190 However

while there is a potential for greater ten-

don load and consequently stretch with

eccentric exercise this potential is rarely

utilized because rehabilitation exercises

seldom approach concentric 1-repeti-

tion maximum It has been shown that

Achilles tendon load and stretch are

identical during the concentric and ec-

centric components of a heel risedropagainst body weight (FIGURE 2) a typi-

cal load used in rehabilitation1179 The 2

most commonly used eccentric exercises

for tendinopathy are squats for the patel-

lar tendon and standing heel lowering for

the Achilles tendon and both movements

are typically performed to a 15-repetition

maximum4103

TABLES 1 and 2 list the number of week-

ly repetitions and estimated loads used in

several eccentric exercise regimes pub-

lished in the literature It should be notedthat several studies have used an individ-

ualized load progression but they seldom

report the actual amount achieved only

the starting load It is also worth noting

that most studies do not include a control

group which is likely due to ethical con-

cerns therefore it is uncertain whether

the provided treatment was in fact supe-

rior to a ldquowait and seerdquo approach Howev-

er most of these studies included patients

with chronic symptoms suggesting that

time alone would not have improvedtheir condition

A few theoretical mechanisms have

been suggested to explain how eccentric

loading may differentially influence ten-

don For example during heel-lowering

raising tasks the ground reaction force

may fluctuate at a higher frequency (ap-

proximately 10 Hz) during the eccentric

phase367984 While tendon cells could

potentially register this modulation the

magnitude of the modulation is quite

small compared to the total load (ap-

proximately 10) It has also been pro-

posed that motor unit activation differs between concentric and eccentric exer-

cises18 which may produce a difference

in load distribution and shear within the

tendon although such a mechanism is

unlikely to be a factor for the patellar ten-

don in which load is distributed via the

patella Finally secreted signaling mol-

ecules from the muscle (myokines) such

as interleukin 6 (IL-6)75 could potentially

affect the nearby tendon and myokine

expression may differ between concen-

tric and eccentric exercise although the

effects are currently unclear7394

In contrast to these hypothetical con-siderations there is evidence to suggest

that eccentric and concentric muscle

contractions do not yield a differential re-

sponse of the tendon In animal models

it has been shown that concentric or ec-

centric contraction to the same force level

does not influence the expression of col-

lagen at the cellular level29 In fact even if

the eccentric muscular contraction force

were greater than concentric contraction

force both contraction modes would yield

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy

StudyGroup Load Pain Improvementdagger

Alredson et al4

Isolated ECC 1260 (100)Daggersect VAS 94

Croisier et al13

Isolated ECC 135 (130) VAS 73 (10 wk)

Alredson and Lorentzon3

Isolated ECC 1260 (100)Daggersect VAS 75

Oumlhberg and Alredson70

Isolated ECC 1260 (100)Daggersect Pain during activity reduced 88

Roos et al83

Isolated ECC 1260 (100)Daggersect Foot and Ankle Outcome Score 36

Shalabi et al86

Isolated ECC 1260 (100)Daggersect 6-point pain scale 40

de Vos et al16

Isolated ECC 1260 (100)Daggersect VISA-A 78

Langberg et al53

Isolated ECC 1260 (120)Daggersect VAS 71

Petersen et al76

Isolated ECC 1890 (100)Daggersect VAS 60

Yelland et al102

Isolated ECC 1260 (100)Daggersect VISA-A 38

Silbernagel et al88

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

VISA-A 60

Rompe et al82

Isolated ECC 1260 (100)Daggersect VISA-A 49 (16 wk)para

Wait and see 0 (0) VISA-A 14 (16 wk)

Table continues on page 857

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 857

similar expressions of collagen33 These

animal findings imply that given a suf-

ficiently high force (and resulting strain

on the fibroblast) the contraction modeis inconsequential for the tendon cellu-

lar response A recent study examined

the effect of contraction mode on tendon

(and muscle) hypertrophy in healthy hu-

man subjects20 The 12-week resistance

training consisted of isolated concentric

knee extensions on one side and eccentric

knee extensions on the contralateral side

The sets repetitions and time of load-

ing were similar between sides but the

loading for the eccentric side was 120

that of the concentric side The results

showed that resistance training with ei-

ther concentric or eccentric contraction

produced a similar magnitude of tendonhypertrophy20 These findings reinforce

the notion that the cellular and tissue re-

sponse in healthy tendon is independent

of contraction mode

In summary there are a number of

mechanisms that could theoretically

differentiate the effect of eccentric from

concentric exercise on tendon but there

is no evidence that these mechanisms

actually play a role or are beneficial In

contrast there is evidence from animal

and human studies that suggests a lack

of differential effect of eccentric versus

concentric exercises

The Effects of Muscle ContractionRegimes on TendinopathyBoth elite and recreational athletes are

frequently afflicted by Achilles andor

patellar tendinopathy5257 The clinical lit-

erature has mainly focused on use of ec-

centric loading exercise in the treatment

of these tendinopathies and therefore the

following sections on Achilles and patellar

tendinopathy will first cover the clinical

studies that have investigated the effects

of eccentric loading followed by studies

that have investigated the effects of othertypes of loading exercises TABLES 1 and 2

cover the clinical studies on Achilles and

patellar tendinopathy with load reported

as weekly repetitions and estimated load

as a percentage of body weight

The Effect of Eccentric Muscle Contrac-

tion on Achilles Tendon It has been

shown that eccentric-loading regimens

for Achilles tendinopathy can provide

clinical improvements including reduc-

tion in pain and improved function15478892

Several studies313

have employed the iso-lated eccentric-loading paradigm initially

introduced by Alfredson et al4 When this

exercise model is performed as unilateral

heel drop the force placed on the ten-

don is a function of body weight and the

force can be modulated with additional

weight placed in a backpack worn by the

patient In addition to improvements in

pain and function it appears that struc-

tural features observed with ultrasound

and magnetic resonance imaging are al-

tered following isolated eccentric loadingin some28707186 but not all studies14697682

It has also been shown that in addition to

decreasing pain isolated eccentric load-

ing can result in increased synthesis of

type I collagen53 Thus isolated eccentric

loading appears to influence biochemical

and biomechanical parameters and im-

prove clinical outcomes The beneficial

effects of isolated eccentric loading with

body weight appear to be reduced if the

pain is located toward the tendon inser-

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric KOOS Knee injury Osteoarthritis Outcome Score

VAS visual analog scale VISA-A Victorian Institute of Sport Assessment-Achilles Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Noslashrregaard et al69

Isolated ECC 1260 (100)Daggersect Modified KOOS-score improved 25

Stretching Stretching Modified KOOS-score improved 25

Beyer et al9

Isolated ECC 1260 (100)Daggersect VISA-A 24VAS 59

Heavy slow resistance (ECC + CON) 144 (130)Dagger VISA-A 41VAS 69

Mafi et al61

Isolated ECC 1260 (100)Daggersect Satisfied 82para

VAS o satisfied 83

Isolated CON plus jump plus rope skipping 1260 (100)Dagger Satisfied 32VAS o satisfied 86

Niesen-Vertommen et al67

Isolated ECC 300 (55)sect VAS 78para

Mixed ECC + CON 300 (25)sect VAS 46

Silbernagel et al89

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

Pain during activity reduced 57

Mixed ECC + CON 1260 (50) or 315 (100)sect Pain during activity reduced 80

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858 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

trophy and increased stiffness o the hu-man patellar tendon J Appl Physiol (1985)2008105805-810 httpdxdoiorg101152japplphysiol903612008

13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

15 de Vos RJ Weir A van Schie HT et al Platelet-rich plasma injection or chronic Achilles tendi-nopathy a randomized controlled trial JAMA2010303144-149 httpdxdoiorg101001jama20091986

16 de Vos RJ Weir A Visser RJ de Winter T TolJL The additional value o a night splint to ec-centric exercises in chronic midportion Achillestendinopathy a randomised controlled trialBr J Sports Med 200741e5 httpdxdoiorg101136bjsm2006032532

17 Dideriksen K Muscle and tendon connective tis-sue adaptation to unloading exercise and NSAIDConnect Tissue Res 20145561-70 httpdxdoiorg103109030082072013862527

18 Enoka RM Eccentric contractions requireunique activation strategies by the nervous sys-tem J Appl Physiol (1985) 1996812339-2346

19 Fahlstroumlm M Jonsson P Lorentzon R AlredsonH Chronic Achilles tendon pain treated with

eccentric cal-muscle training Knee Surg SportsTraumatol Arthrosc 200311327-333 httpdxdoiorg101007s00167-003-0418-z

20 Farup J Rahbek SK Vendelbo MH et al Wheyprotein hydrolysate augments tendon and mus-cle hypertrophy independent o resistance exer-cise contraction mode Scand J Med Sci Sports201424788-798 httpdxdoiorg101111sms12083

21 Feng Z Tateishi Y Nomura Y Kitajima T Na-kamura T Construction o fibroblastndashcollagengels with orientated fibrils induced by static ordynamic stress toward the abrication o smalltendon grats J Artif Organs 20069220-225httpdxdoiorg101007s10047-006-0354-z

22 Ferretti A Epidemiology o jumperrsquos kneeSports Med 19863289-295

23 Finni T Komi PV Lepola V In vivo human tricepssurae and quadriceps emoris muscle unctionin a squat jump and counter movement jumpEur J Appl Physiol 200083416-426 httpdxdoiorg101007s004210000289

24 Folkhard W Geercken W Knoumlrzer E et alStructural dynamic o native tendon collagenJ Mol Biol 1987193405-407 httpdxdoiorg1010160022-2836(87)90228-2

25 Fredberg U Stengaard-Pedersen KChronic tendinopathy tissue pathologypain mechanisms and etiology with a spe-

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 861

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Sci Sports 2008183-15 httpdxdoiorg101111j1600-0838200700746x

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Med 200741e7 httpdxdoiorg101136bjsm2006032599

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Med 20024111-18 httpdxdoiorg101002ajim10019

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29 Garma T Kobayashi C Haddad F AdamsGR Bodell PW Baldwin KM Similar acutemolecular responses to equivalent volumeso isometric lengthening or shortening moderesistance exercise J Appl Physiol (1985)2007102135-143 httpdxdoiorg101152japplphysiol007762006

30 Gauvin R Parenteau-Bareil R Larouche D etal Dynamic mechanical stimulations induceanisotropy and improve the tensile properties oengineered tissues produced without exogenousscaffolding Acta Biomater 201173294-3301httpdxdoiorg101016jactbio201105034

31 Giddings VL Beaupreacute GS Whalen RT Carter DRCalcaneal loading during walking and running

Med Sci Sports Exerc 200032627-634 32 Glazebrook MA Wright JR Jr Langman M

Stanish WD Lee JM Histological analysis oAchilles tendons in an overuse rat model J

Orthop Res 200826840-846 httpdxdoiorg101002jor20546

33 Heinemeier KM Olesen JL Haddad F et alExpression o collagen and related growthactors in rat tendon and skeletal muscle in re-sponse to specific contraction types J Physiol20075821303-1316 httpdxdoiorg101113jphysiol2007127639

34 Heinemeier KM Schjerling P Heinemeier JMagnusson SP Kjaer M Lack o tissue renewalin human adult Achilles tendon is revealed by

nuclear bomb 13C FASEB J 2013272074-2079httpdxdoiorg101096f12-225599

35 Heinemeier KM Skovgaard D Bayer ML et alUphill running improves rat Achilles tendon tis-sue mechanical properties and alters gene ex-pression without inducing pathological changesJ Appl Physiol (1985) 2012113827-836 httpdxdoiorg101152japplphysiol004012012

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37 Hill AV The heat o shortening and the dynamic

constants o muscle Proc R Soc Lond B Biol Sci1938126136-195 httpdxdoiorg101098rspb19380050

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bolic consequences J Appl Physiol Respir Envi-ron Exerc Physiol 198456831-838

39 Jonsson P Alredson H Superior results witheccentric compared to concentric quadricepstraining in patients with jumperrsquos knee a pro-spective randomised study Br J Sports Med200539847-850 httpdxdoiorg101136bjsm2005018630

40 Jonsson P Alredson H Sunding K Fahlstroumlm MCook J New regimen or eccentric cal-muscletraining in patients with chronic insertionalAchilles tendinopathy results o a pilot studyBr J Sports Med 200842746-749 httpdxdoiorg101136bjsm2007039545

41 Joshi SD Webb K Variation o cyclic strain

parameters regulates development o elasticmodulus in fibroblastsubstrate constructsJ Orthop Res 2008261105-1113 httpdxdoiorg101002jor20626

42 Kalson NS Holmes DF Herchenhan A Lu YStarborg T Kadler KE Slow stretching that mim-ics embryonic growth rate stimulates structuraland mechanical development o tendon-liketissue in vitro Dev Dyn 20112402520-2528httpdxdoiorg101002dvdy22760

43 Ker RF Wang XT Pike AV Fatigue qual-ity o mammalian tendons J Exp Biol20002031317-1327

44 Kettunen JA Kvist M Alanen E Kujala UMLong-term prognosis or jumperrsquos knee in male

athletes A prospective ollow-up study Am JSports Med 200230689-692

45 Khan K Cook J The painul nonrupturedtendon clinical aspects Clin Sports Med200322711-725

46 Khan KM Cook JL Kannus P Maffulli N BonarSF Time to abandon the ldquotendinitisrdquo myth BMJ2002324626-627 httpdxdoiorg101136bmj3247338626

47 Kingma JJ de Knikker R Wittink HM TakkenT Eccentric overload training in patients withchronic Achilles tendinopathy a systematic re-view Br J Sports Med 200741e3 httpdxdoiorg101136bjsm2006030916

48 Kjaer M Role o extracellular matrix in adapta-

tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

49 Kongsgaard M Kovanen V Aagaard P et alCorticosteroid injections eccentric declinesquat training and heavy slow resistancetraining in patellar tendinopathy Scand J Med

Sci Sports 200919790-802 httpdxdoiorg101111j1600-0838200900949x

50 Kongsgaard M Qvortrup K Larsen J et alFibril morphology and tendon mechanicalproperties in patellar tendinopathy effectso heavy slow resistance training Am J

Sports Med 201038749-756 httpdxdoi

org1011770363546509350915 51 Kubo K Kanehisa H Fukunaga T Effects o

different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

org101111j1469-779320010649cxd 52 Kujala UM Sarna S Kaprio J Cumulative

incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

J Sport Med 200515133-135 httpdxdoiorg10109701jsm00001653475563823

53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

Med Sci Sports 20071761-66 httpdxdoiorg101111j1600-0838200600522x

54 Langberg H Olesen J Skovgaard D Kjaer M Agerelated blood flow around the Achilles tendonduring exercise in humans Eur J Appl Physiol

200184246-248 httpdxdoiorg101007s004210170013

55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

59 Maeda E Shelton JC Bader DL Lee DA Timedependence o cyclic tensile strain on collagenproduction in tendon ascicles Biochem Bio-

phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 855

stretching becomes detrimental4168 The

absolute values of strain used in cell-

culture stimulation vary greatly and it is

uncertain how much of a given strain the

cells will experience in vivo because thesurrounding matrix may provide shield-

ing In vivo in healthy human Achilles

tendons it has been reported that with

equal exercise volume working at 90 of

maximum voluntary contraction (MVC)

which causes approximately 5 tendon

strain yields increased stiffness and

cross-sectional area compared to work-

ing at 55 MVC which causes approxi-

mately 3 tendon strain5

Speed andor duration of loading dur-

ing exercise also appear to be importantfor tendon adaptation6415156 At the cellu-

lar level most304197 but not all21 studies

have found that the adaptive response of

fibroblasts to dynamic load is superior to

that of static load (zero speed) Though

the response to different dynamic load re-

gimes is complex due to the interaction

of the parameters overall the evidence

suggests that increased time under load

increased number of load cycles and

increased loading rate result in a posi-

tive adaptive response (increased ma-trix strength and stiffness and decreased

matrix metalloproteinase expression) in

cultured fibroblasts4156100 The response

appears to be a bit different in vivo where

it has been reported that the stiffness

and size (cross-sectional area) of human

Achilles tendon were more responsive to

a low number of loads of long duration

(6-second cycle) than to a high number of

faster loads (2-second cycle) when the to-

tal exercise volume was kept constant56

This finding is corroborated somewhat by another study showing that isometric

contractions of long duration (20 sec-

onds) yielded greater patellar tendon ad-

aptation (increased stiffness) than rapid

(1-second) contractions at equal exer-

cise volume51 In the latter study muscle

strength and volume adaptation were un-

affected by contraction duration

It is unknown whether tendon cells

experience some form of fatigue as a re-

sult of repeated load cycles Tendon cells

have a low metabolic rate and probably

do not require rest for the purpose of re-

storing energy deposits However the an-

abolic response to loading is sustained in

tendon for up to several days following anexercise bout5565 which could indicate the

need for a postexercise recovery period63

But conversely studies on cell culture

have performed continuous stimulation

of fibroblasts for up to 24 hours per day

without detrimental effects4159 and most

exercise protocols for tendinopathy man-

agement are performed every day with-

out recovery periods46789 Overall there

is a lack of studies specifically addressing

the effects of recovery and how it affects

tendon adaptationThe majority of the tendon is com-

posed of extracellular matrix (ECM)

which is a passive structure and un-

like the cells does not actively respond

to load though it may still be differen-

tially affected by exercise parameters It

has been suggested that accumulation

of microdamage may be involved in the

etiology of tendinopathy 87 and because

the turnover in tendons is slow34 ECM

damage could accumulate Microdamage

is difficult to measure and its clinical rel-evance is therefore unclear However if it

does play a role it would be an argument

in favor of recovery periods Mechanical

studies have shown that both overload-

ing and mechanical fatigue can cause

damage to tendon ECM4372 which could

play a role in tendinopathy The tendon

ECM is also a viscoelastic material which

means that slower loading regimes can

yield greater strains than faster loading

regimes as the tendon has more time to

creep74

Creep also appears to be associ-ated with greater relative fibril slippage24

which may generate local shear strains

sensed by the cells Slow loading may

therefore produce particularly strong cell

stimuli that can be beneficial to the ten-

don if the strain is sufficient but could be

detrimental if strain is excessive This vis-

coelastic behavior depends on the amount

of time the tendon is under load and is

therefore unaffected by the mode of mus-

cle contraction (eccentric or concentric)

In summary tendon is responsive to

loading and will respond more strongly

to greater loads although there is likely

an optimum beyond which load becomes

detrimental Slower loading regimes may

be superior to rapid loading while theimportance of recovery between loading

sessions is unclear

Tendon Under Eccentric andConcentric Muscle Contractions

Although isolated eccentric loading re-

gimes for tendinopathy have been widely

accepted as the treatment of choice92 the

potential mechanisms behind this inter-

vention remain unclear In the following

section we discuss some of the proposed

mechanisms and their potential applica-tions in light of existing evidence

Strictly speaking the descriptions

ldquoconcentricrdquo and ldquoeccentricrdquo only apply to

muscle which actively contracts Tendon

is a mechanically passive structure that

lengthens when load increases and short-

ens when load is reduced (FIGURE 1) It is

therefore questionable whether the mode

of muscle contraction for a given load and

range of motion would have a differen-

tial effect on tendon tissue The fact that

07

095 10 105

08

09

10

11

12

13

14

F o r c e M e a n F o r c e

LengthMean Length (mm)

FIGURE 2 Achilles tendon orce versus Achillestendon length Eccentric data are shown as opencircles whereas concentric data are filled circles

Reprinted with permission rom Chaudhry SMorrissey D Woledge RC Bader DL Screen HREccentric and concentric loading o the tricepssurae an in vivo study o dynamic muscle andtendon biomechanical parameters J Appl Biomech

20153169-78 copyHuman Kinetics Inc

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856 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

muscles can produce greater maximal

force eccentrically than concentrically

would suggest a potential for greater me-

chanical stimulation from eccentric than

from concentric exercise1837

According-ly it has been suggested that the tendon

may stretch more during eccentric load-

ing than concentric loading190 However

while there is a potential for greater ten-

don load and consequently stretch with

eccentric exercise this potential is rarely

utilized because rehabilitation exercises

seldom approach concentric 1-repeti-

tion maximum It has been shown that

Achilles tendon load and stretch are

identical during the concentric and ec-

centric components of a heel risedropagainst body weight (FIGURE 2) a typi-

cal load used in rehabilitation1179 The 2

most commonly used eccentric exercises

for tendinopathy are squats for the patel-

lar tendon and standing heel lowering for

the Achilles tendon and both movements

are typically performed to a 15-repetition

maximum4103

TABLES 1 and 2 list the number of week-

ly repetitions and estimated loads used in

several eccentric exercise regimes pub-

lished in the literature It should be notedthat several studies have used an individ-

ualized load progression but they seldom

report the actual amount achieved only

the starting load It is also worth noting

that most studies do not include a control

group which is likely due to ethical con-

cerns therefore it is uncertain whether

the provided treatment was in fact supe-

rior to a ldquowait and seerdquo approach Howev-

er most of these studies included patients

with chronic symptoms suggesting that

time alone would not have improvedtheir condition

A few theoretical mechanisms have

been suggested to explain how eccentric

loading may differentially influence ten-

don For example during heel-lowering

raising tasks the ground reaction force

may fluctuate at a higher frequency (ap-

proximately 10 Hz) during the eccentric

phase367984 While tendon cells could

potentially register this modulation the

magnitude of the modulation is quite

small compared to the total load (ap-

proximately 10) It has also been pro-

posed that motor unit activation differs between concentric and eccentric exer-

cises18 which may produce a difference

in load distribution and shear within the

tendon although such a mechanism is

unlikely to be a factor for the patellar ten-

don in which load is distributed via the

patella Finally secreted signaling mol-

ecules from the muscle (myokines) such

as interleukin 6 (IL-6)75 could potentially

affect the nearby tendon and myokine

expression may differ between concen-

tric and eccentric exercise although the

effects are currently unclear7394

In contrast to these hypothetical con-siderations there is evidence to suggest

that eccentric and concentric muscle

contractions do not yield a differential re-

sponse of the tendon In animal models

it has been shown that concentric or ec-

centric contraction to the same force level

does not influence the expression of col-

lagen at the cellular level29 In fact even if

the eccentric muscular contraction force

were greater than concentric contraction

force both contraction modes would yield

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy

StudyGroup Load Pain Improvementdagger

Alredson et al4

Isolated ECC 1260 (100)Daggersect VAS 94

Croisier et al13

Isolated ECC 135 (130) VAS 73 (10 wk)

Alredson and Lorentzon3

Isolated ECC 1260 (100)Daggersect VAS 75

Oumlhberg and Alredson70

Isolated ECC 1260 (100)Daggersect Pain during activity reduced 88

Roos et al83

Isolated ECC 1260 (100)Daggersect Foot and Ankle Outcome Score 36

Shalabi et al86

Isolated ECC 1260 (100)Daggersect 6-point pain scale 40

de Vos et al16

Isolated ECC 1260 (100)Daggersect VISA-A 78

Langberg et al53

Isolated ECC 1260 (120)Daggersect VAS 71

Petersen et al76

Isolated ECC 1890 (100)Daggersect VAS 60

Yelland et al102

Isolated ECC 1260 (100)Daggersect VISA-A 38

Silbernagel et al88

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

VISA-A 60

Rompe et al82

Isolated ECC 1260 (100)Daggersect VISA-A 49 (16 wk)para

Wait and see 0 (0) VISA-A 14 (16 wk)

Table continues on page 857

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 857

similar expressions of collagen33 These

animal findings imply that given a suf-

ficiently high force (and resulting strain

on the fibroblast) the contraction modeis inconsequential for the tendon cellu-

lar response A recent study examined

the effect of contraction mode on tendon

(and muscle) hypertrophy in healthy hu-

man subjects20 The 12-week resistance

training consisted of isolated concentric

knee extensions on one side and eccentric

knee extensions on the contralateral side

The sets repetitions and time of load-

ing were similar between sides but the

loading for the eccentric side was 120

that of the concentric side The results

showed that resistance training with ei-

ther concentric or eccentric contraction

produced a similar magnitude of tendonhypertrophy20 These findings reinforce

the notion that the cellular and tissue re-

sponse in healthy tendon is independent

of contraction mode

In summary there are a number of

mechanisms that could theoretically

differentiate the effect of eccentric from

concentric exercise on tendon but there

is no evidence that these mechanisms

actually play a role or are beneficial In

contrast there is evidence from animal

and human studies that suggests a lack

of differential effect of eccentric versus

concentric exercises

The Effects of Muscle ContractionRegimes on TendinopathyBoth elite and recreational athletes are

frequently afflicted by Achilles andor

patellar tendinopathy5257 The clinical lit-

erature has mainly focused on use of ec-

centric loading exercise in the treatment

of these tendinopathies and therefore the

following sections on Achilles and patellar

tendinopathy will first cover the clinical

studies that have investigated the effects

of eccentric loading followed by studies

that have investigated the effects of othertypes of loading exercises TABLES 1 and 2

cover the clinical studies on Achilles and

patellar tendinopathy with load reported

as weekly repetitions and estimated load

as a percentage of body weight

The Effect of Eccentric Muscle Contrac-

tion on Achilles Tendon It has been

shown that eccentric-loading regimens

for Achilles tendinopathy can provide

clinical improvements including reduc-

tion in pain and improved function15478892

Several studies313

have employed the iso-lated eccentric-loading paradigm initially

introduced by Alfredson et al4 When this

exercise model is performed as unilateral

heel drop the force placed on the ten-

don is a function of body weight and the

force can be modulated with additional

weight placed in a backpack worn by the

patient In addition to improvements in

pain and function it appears that struc-

tural features observed with ultrasound

and magnetic resonance imaging are al-

tered following isolated eccentric loadingin some28707186 but not all studies14697682

It has also been shown that in addition to

decreasing pain isolated eccentric load-

ing can result in increased synthesis of

type I collagen53 Thus isolated eccentric

loading appears to influence biochemical

and biomechanical parameters and im-

prove clinical outcomes The beneficial

effects of isolated eccentric loading with

body weight appear to be reduced if the

pain is located toward the tendon inser-

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric KOOS Knee injury Osteoarthritis Outcome Score

VAS visual analog scale VISA-A Victorian Institute of Sport Assessment-Achilles Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Noslashrregaard et al69

Isolated ECC 1260 (100)Daggersect Modified KOOS-score improved 25

Stretching Stretching Modified KOOS-score improved 25

Beyer et al9

Isolated ECC 1260 (100)Daggersect VISA-A 24VAS 59

Heavy slow resistance (ECC + CON) 144 (130)Dagger VISA-A 41VAS 69

Mafi et al61

Isolated ECC 1260 (100)Daggersect Satisfied 82para

VAS o satisfied 83

Isolated CON plus jump plus rope skipping 1260 (100)Dagger Satisfied 32VAS o satisfied 86

Niesen-Vertommen et al67

Isolated ECC 300 (55)sect VAS 78para

Mixed ECC + CON 300 (25)sect VAS 46

Silbernagel et al89

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

Pain during activity reduced 57

Mixed ECC + CON 1260 (50) or 315 (100)sect Pain during activity reduced 80

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858 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

trophy and increased stiffness o the hu-man patellar tendon J Appl Physiol (1985)2008105805-810 httpdxdoiorg101152japplphysiol903612008

13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

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16 de Vos RJ Weir A Visser RJ de Winter T TolJL The additional value o a night splint to ec-centric exercises in chronic midportion Achillestendinopathy a randomised controlled trialBr J Sports Med 200741e5 httpdxdoiorg101136bjsm2006032532

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19 Fahlstroumlm M Jonsson P Lorentzon R AlredsonH Chronic Achilles tendon pain treated with

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21 Feng Z Tateishi Y Nomura Y Kitajima T Na-kamura T Construction o fibroblastndashcollagengels with orientated fibrils induced by static ordynamic stress toward the abrication o smalltendon grats J Artif Organs 20069220-225httpdxdoiorg101007s10047-006-0354-z

22 Ferretti A Epidemiology o jumperrsquos kneeSports Med 19863289-295

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25 Fredberg U Stengaard-Pedersen KChronic tendinopathy tissue pathologypain mechanisms and etiology with a spe-

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28 Gaumlrdin A Bruno J Movin T Kristoffersen-WibergM Shalabi A Magnetic resonance signal ratherthan tendon volume correlates to pain andunctional impairment in chronic Achilles tendi-nopathy Acta Radiol 200647718-724 httpdxdoiorg10108002841850600774035

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nuclear bomb 13C FASEB J 2013272074-2079httpdxdoiorg101096f12-225599

35 Heinemeier KM Skovgaard D Bayer ML et alUphill running improves rat Achilles tendon tis-sue mechanical properties and alters gene ex-pression without inducing pathological changesJ Appl Physiol (1985) 2012113827-836 httpdxdoiorg101152japplphysiol004012012

36 Henriksen M Aaboe J Bliddal H LangbergH Biomechanical characteristics o the ec-centric Achilles tendon exercise J Biomech2009422702-2707 httpdxdoiorg101016jjbiomech200908009

37 Hill AV The heat o shortening and the dynamic

constants o muscle Proc R Soc Lond B Biol Sci1938126136-195 httpdxdoiorg101098rspb19380050

38 Holloszy JO Coyle EF Adaptations o skeletalmuscle to endurance exercise and their meta-

bolic consequences J Appl Physiol Respir Envi-ron Exerc Physiol 198456831-838

39 Jonsson P Alredson H Superior results witheccentric compared to concentric quadricepstraining in patients with jumperrsquos knee a pro-spective randomised study Br J Sports Med200539847-850 httpdxdoiorg101136bjsm2005018630

40 Jonsson P Alredson H Sunding K Fahlstroumlm MCook J New regimen or eccentric cal-muscletraining in patients with chronic insertionalAchilles tendinopathy results o a pilot studyBr J Sports Med 200842746-749 httpdxdoiorg101136bjsm2007039545

41 Joshi SD Webb K Variation o cyclic strain

parameters regulates development o elasticmodulus in fibroblastsubstrate constructsJ Orthop Res 2008261105-1113 httpdxdoiorg101002jor20626

42 Kalson NS Holmes DF Herchenhan A Lu YStarborg T Kadler KE Slow stretching that mim-ics embryonic growth rate stimulates structuraland mechanical development o tendon-liketissue in vitro Dev Dyn 20112402520-2528httpdxdoiorg101002dvdy22760

43 Ker RF Wang XT Pike AV Fatigue qual-ity o mammalian tendons J Exp Biol20002031317-1327

44 Kettunen JA Kvist M Alanen E Kujala UMLong-term prognosis or jumperrsquos knee in male

athletes A prospective ollow-up study Am JSports Med 200230689-692

45 Khan K Cook J The painul nonrupturedtendon clinical aspects Clin Sports Med200322711-725

46 Khan KM Cook JL Kannus P Maffulli N BonarSF Time to abandon the ldquotendinitisrdquo myth BMJ2002324626-627 httpdxdoiorg101136bmj3247338626

47 Kingma JJ de Knikker R Wittink HM TakkenT Eccentric overload training in patients withchronic Achilles tendinopathy a systematic re-view Br J Sports Med 200741e3 httpdxdoiorg101136bjsm2006030916

48 Kjaer M Role o extracellular matrix in adapta-

tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

49 Kongsgaard M Kovanen V Aagaard P et alCorticosteroid injections eccentric declinesquat training and heavy slow resistancetraining in patellar tendinopathy Scand J Med

Sci Sports 200919790-802 httpdxdoiorg101111j1600-0838200900949x

50 Kongsgaard M Qvortrup K Larsen J et alFibril morphology and tendon mechanicalproperties in patellar tendinopathy effectso heavy slow resistance training Am J

Sports Med 201038749-756 httpdxdoi

org1011770363546509350915 51 Kubo K Kanehisa H Fukunaga T Effects o

different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

org101111j1469-779320010649cxd 52 Kujala UM Sarna S Kaprio J Cumulative

incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

J Sport Med 200515133-135 httpdxdoiorg10109701jsm00001653475563823

53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

Med Sci Sports 20071761-66 httpdxdoiorg101111j1600-0838200600522x

54 Langberg H Olesen J Skovgaard D Kjaer M Agerelated blood flow around the Achilles tendonduring exercise in humans Eur J Appl Physiol

200184246-248 httpdxdoiorg101007s004210170013

55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

59 Maeda E Shelton JC Bader DL Lee DA Timedependence o cyclic tensile strain on collagenproduction in tendon ascicles Biochem Bio-

phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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856 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

muscles can produce greater maximal

force eccentrically than concentrically

would suggest a potential for greater me-

chanical stimulation from eccentric than

from concentric exercise1837

According-ly it has been suggested that the tendon

may stretch more during eccentric load-

ing than concentric loading190 However

while there is a potential for greater ten-

don load and consequently stretch with

eccentric exercise this potential is rarely

utilized because rehabilitation exercises

seldom approach concentric 1-repeti-

tion maximum It has been shown that

Achilles tendon load and stretch are

identical during the concentric and ec-

centric components of a heel risedropagainst body weight (FIGURE 2) a typi-

cal load used in rehabilitation1179 The 2

most commonly used eccentric exercises

for tendinopathy are squats for the patel-

lar tendon and standing heel lowering for

the Achilles tendon and both movements

are typically performed to a 15-repetition

maximum4103

TABLES 1 and 2 list the number of week-

ly repetitions and estimated loads used in

several eccentric exercise regimes pub-

lished in the literature It should be notedthat several studies have used an individ-

ualized load progression but they seldom

report the actual amount achieved only

the starting load It is also worth noting

that most studies do not include a control

group which is likely due to ethical con-

cerns therefore it is uncertain whether

the provided treatment was in fact supe-

rior to a ldquowait and seerdquo approach Howev-

er most of these studies included patients

with chronic symptoms suggesting that

time alone would not have improvedtheir condition

A few theoretical mechanisms have

been suggested to explain how eccentric

loading may differentially influence ten-

don For example during heel-lowering

raising tasks the ground reaction force

may fluctuate at a higher frequency (ap-

proximately 10 Hz) during the eccentric

phase367984 While tendon cells could

potentially register this modulation the

magnitude of the modulation is quite

small compared to the total load (ap-

proximately 10) It has also been pro-

posed that motor unit activation differs between concentric and eccentric exer-

cises18 which may produce a difference

in load distribution and shear within the

tendon although such a mechanism is

unlikely to be a factor for the patellar ten-

don in which load is distributed via the

patella Finally secreted signaling mol-

ecules from the muscle (myokines) such

as interleukin 6 (IL-6)75 could potentially

affect the nearby tendon and myokine

expression may differ between concen-

tric and eccentric exercise although the

effects are currently unclear7394

In contrast to these hypothetical con-siderations there is evidence to suggest

that eccentric and concentric muscle

contractions do not yield a differential re-

sponse of the tendon In animal models

it has been shown that concentric or ec-

centric contraction to the same force level

does not influence the expression of col-

lagen at the cellular level29 In fact even if

the eccentric muscular contraction force

were greater than concentric contraction

force both contraction modes would yield

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy

StudyGroup Load Pain Improvementdagger

Alredson et al4

Isolated ECC 1260 (100)Daggersect VAS 94

Croisier et al13

Isolated ECC 135 (130) VAS 73 (10 wk)

Alredson and Lorentzon3

Isolated ECC 1260 (100)Daggersect VAS 75

Oumlhberg and Alredson70

Isolated ECC 1260 (100)Daggersect Pain during activity reduced 88

Roos et al83

Isolated ECC 1260 (100)Daggersect Foot and Ankle Outcome Score 36

Shalabi et al86

Isolated ECC 1260 (100)Daggersect 6-point pain scale 40

de Vos et al16

Isolated ECC 1260 (100)Daggersect VISA-A 78

Langberg et al53

Isolated ECC 1260 (120)Daggersect VAS 71

Petersen et al76

Isolated ECC 1890 (100)Daggersect VAS 60

Yelland et al102

Isolated ECC 1260 (100)Daggersect VISA-A 38

Silbernagel et al88

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

VISA-A 60

Rompe et al82

Isolated ECC 1260 (100)Daggersect VISA-A 49 (16 wk)para

Wait and see 0 (0) VISA-A 14 (16 wk)

Table continues on page 857

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 857

similar expressions of collagen33 These

animal findings imply that given a suf-

ficiently high force (and resulting strain

on the fibroblast) the contraction modeis inconsequential for the tendon cellu-

lar response A recent study examined

the effect of contraction mode on tendon

(and muscle) hypertrophy in healthy hu-

man subjects20 The 12-week resistance

training consisted of isolated concentric

knee extensions on one side and eccentric

knee extensions on the contralateral side

The sets repetitions and time of load-

ing were similar between sides but the

loading for the eccentric side was 120

that of the concentric side The results

showed that resistance training with ei-

ther concentric or eccentric contraction

produced a similar magnitude of tendonhypertrophy20 These findings reinforce

the notion that the cellular and tissue re-

sponse in healthy tendon is independent

of contraction mode

In summary there are a number of

mechanisms that could theoretically

differentiate the effect of eccentric from

concentric exercise on tendon but there

is no evidence that these mechanisms

actually play a role or are beneficial In

contrast there is evidence from animal

and human studies that suggests a lack

of differential effect of eccentric versus

concentric exercises

The Effects of Muscle ContractionRegimes on TendinopathyBoth elite and recreational athletes are

frequently afflicted by Achilles andor

patellar tendinopathy5257 The clinical lit-

erature has mainly focused on use of ec-

centric loading exercise in the treatment

of these tendinopathies and therefore the

following sections on Achilles and patellar

tendinopathy will first cover the clinical

studies that have investigated the effects

of eccentric loading followed by studies

that have investigated the effects of othertypes of loading exercises TABLES 1 and 2

cover the clinical studies on Achilles and

patellar tendinopathy with load reported

as weekly repetitions and estimated load

as a percentage of body weight

The Effect of Eccentric Muscle Contrac-

tion on Achilles Tendon It has been

shown that eccentric-loading regimens

for Achilles tendinopathy can provide

clinical improvements including reduc-

tion in pain and improved function15478892

Several studies313

have employed the iso-lated eccentric-loading paradigm initially

introduced by Alfredson et al4 When this

exercise model is performed as unilateral

heel drop the force placed on the ten-

don is a function of body weight and the

force can be modulated with additional

weight placed in a backpack worn by the

patient In addition to improvements in

pain and function it appears that struc-

tural features observed with ultrasound

and magnetic resonance imaging are al-

tered following isolated eccentric loadingin some28707186 but not all studies14697682

It has also been shown that in addition to

decreasing pain isolated eccentric load-

ing can result in increased synthesis of

type I collagen53 Thus isolated eccentric

loading appears to influence biochemical

and biomechanical parameters and im-

prove clinical outcomes The beneficial

effects of isolated eccentric loading with

body weight appear to be reduced if the

pain is located toward the tendon inser-

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric KOOS Knee injury Osteoarthritis Outcome Score

VAS visual analog scale VISA-A Victorian Institute of Sport Assessment-Achilles Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Noslashrregaard et al69

Isolated ECC 1260 (100)Daggersect Modified KOOS-score improved 25

Stretching Stretching Modified KOOS-score improved 25

Beyer et al9

Isolated ECC 1260 (100)Daggersect VISA-A 24VAS 59

Heavy slow resistance (ECC + CON) 144 (130)Dagger VISA-A 41VAS 69

Mafi et al61

Isolated ECC 1260 (100)Daggersect Satisfied 82para

VAS o satisfied 83

Isolated CON plus jump plus rope skipping 1260 (100)Dagger Satisfied 32VAS o satisfied 86

Niesen-Vertommen et al67

Isolated ECC 300 (55)sect VAS 78para

Mixed ECC + CON 300 (25)sect VAS 46

Silbernagel et al89

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

Pain during activity reduced 57

Mixed ECC + CON 1260 (50) or 315 (100)sect Pain during activity reduced 80

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858 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

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13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

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Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

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93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

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a randomized clinical trial Clin J Sport Med200515227-234

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mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

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66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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similar expressions of collagen33 These

animal findings imply that given a suf-

ficiently high force (and resulting strain

on the fibroblast) the contraction modeis inconsequential for the tendon cellu-

lar response A recent study examined

the effect of contraction mode on tendon

(and muscle) hypertrophy in healthy hu-

man subjects20 The 12-week resistance

training consisted of isolated concentric

knee extensions on one side and eccentric

knee extensions on the contralateral side

The sets repetitions and time of load-

ing were similar between sides but the

loading for the eccentric side was 120

that of the concentric side The results

showed that resistance training with ei-

ther concentric or eccentric contraction

produced a similar magnitude of tendonhypertrophy20 These findings reinforce

the notion that the cellular and tissue re-

sponse in healthy tendon is independent

of contraction mode

In summary there are a number of

mechanisms that could theoretically

differentiate the effect of eccentric from

concentric exercise on tendon but there

is no evidence that these mechanisms

actually play a role or are beneficial In

contrast there is evidence from animal

and human studies that suggests a lack

of differential effect of eccentric versus

concentric exercises

The Effects of Muscle ContractionRegimes on TendinopathyBoth elite and recreational athletes are

frequently afflicted by Achilles andor

patellar tendinopathy5257 The clinical lit-

erature has mainly focused on use of ec-

centric loading exercise in the treatment

of these tendinopathies and therefore the

following sections on Achilles and patellar

tendinopathy will first cover the clinical

studies that have investigated the effects

of eccentric loading followed by studies

that have investigated the effects of othertypes of loading exercises TABLES 1 and 2

cover the clinical studies on Achilles and

patellar tendinopathy with load reported

as weekly repetitions and estimated load

as a percentage of body weight

The Effect of Eccentric Muscle Contrac-

tion on Achilles Tendon It has been

shown that eccentric-loading regimens

for Achilles tendinopathy can provide

clinical improvements including reduc-

tion in pain and improved function15478892

Several studies313

have employed the iso-lated eccentric-loading paradigm initially

introduced by Alfredson et al4 When this

exercise model is performed as unilateral

heel drop the force placed on the ten-

don is a function of body weight and the

force can be modulated with additional

weight placed in a backpack worn by the

patient In addition to improvements in

pain and function it appears that struc-

tural features observed with ultrasound

and magnetic resonance imaging are al-

tered following isolated eccentric loadingin some28707186 but not all studies14697682

It has also been shown that in addition to

decreasing pain isolated eccentric load-

ing can result in increased synthesis of

type I collagen53 Thus isolated eccentric

loading appears to influence biochemical

and biomechanical parameters and im-

prove clinical outcomes The beneficial

effects of isolated eccentric loading with

body weight appear to be reduced if the

pain is located toward the tendon inser-

TABLE 1Exercise Programs Used in Studies

for Achilles Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric KOOS Knee injury Osteoarthritis Outcome Score

VAS visual analog scale VISA-A Victorian Institute of Sport Assessment-Achilles Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Noslashrregaard et al69

Isolated ECC 1260 (100)Daggersect Modified KOOS-score improved 25

Stretching Stretching Modified KOOS-score improved 25

Beyer et al9

Isolated ECC 1260 (100)Daggersect VISA-A 24VAS 59

Heavy slow resistance (ECC + CON) 144 (130)Dagger VISA-A 41VAS 69

Mafi et al61

Isolated ECC 1260 (100)Daggersect Satisfied 82para

VAS o satisfied 83

Isolated CON plus jump plus rope skipping 1260 (100)Dagger Satisfied 32VAS o satisfied 86

Niesen-Vertommen et al67

Isolated ECC 300 (55)sect VAS 78para

Mixed ECC + CON 300 (25)sect VAS 46

Silbernagel et al89

Isolated ECC plus mixed ECC + CONplus other exercises

Mixed 840 (50)Dagger

Mixed 945 (100)Daggersect

ECC 630 (100)Daggersect

Pain during activity reduced 57

Mixed ECC + CON 1260 (50) or 315 (100)sect Pain during activity reduced 80

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[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

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13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

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16 de Vos RJ Weir A Visser RJ de Winter T TolJL The additional value o a night splint to ec-centric exercises in chronic midportion Achillestendinopathy a randomised controlled trialBr J Sports Med 200741e5 httpdxdoiorg101136bjsm2006032532

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18 Enoka RM Eccentric contractions requireunique activation strategies by the nervous sys-tem J Appl Physiol (1985) 1996812339-2346

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eccentric cal-muscle training Knee Surg SportsTraumatol Arthrosc 200311327-333 httpdxdoiorg101007s00167-003-0418-z

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25 Fredberg U Stengaard-Pedersen KChronic tendinopathy tissue pathologypain mechanisms and etiology with a spe-

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tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

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different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

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incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

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53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

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55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

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phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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858 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

stretching which places a low-magnitude

load on the tendon for an extended period

and the results showed that the interven-

tions yielded a similar clinical outcome69

It was recently demonstrated that heavy

slow resistance training 3 times per week

was equally effective in reducing symp-

toms compared to the traditional eccen-

tric regimen performed 7 days per week

in patients with Achilles tendinopathy9

These data indicate that different musclecontraction loading regimes can accom-

plish the same clinical improvement in

patients with Achilles tendinopathy Thus

it seems that loading confers some clinical

improvements to Achilles tendinopathy

but based on the available literature it is

not possible to delineate the role of con-

traction mode (eccentric or concentric)

from that of load magnitude number of

repetitions and sets contraction speed

and recovery time between sessions

The Effects of Eccentric Muscle Con-

traction on Patellar Tendon Similar to

Achilles tendinopathy it has been sug-

gested that eccentric-loading regimes

for patellar tendinopathy may provide

clinical improvements8133978 Patients

typically eccentrically load the affected

patellar tendon while performing a par-

tial squat on the affected limb and then

return to the starting position by concen-

trically loading the nonaffected tendonOne study compared isolated eccentric

loading with body weight to nonloading

therapy with ultrasound or transverse

friction massage91 The authors reported

that as few as 3 weekly sessions (each ses-

sion consisting of 3 sets of 15 repetitions)

of isolated eccentric squats for 4 weeks

yielded significant clinical improve-

ments which were far greater than with

nonloading therapy91 It has also been

shown that eccentric loading can result

tion19 however this might be remedied

by avoiding ankle dorsiflexion below hor-

izontal to avoid compression of the distal

end of the tendon against the posterior

aspect of the calcaneus40

Several studies have compared

isolated eccentric loading with body

weight to other types of nonloading

therapy (eg prolotherapy cryotherapy

splints)167683102 Most of these studies

report significant clinical improvements

with eccentric exercise167683102 although

the effect relative to the alternative treat-

ment varies (eg eccentric loading regimes

have greater effect than cryotherapy but

similar effect compared to shockwave

therapy and heel brace)92

Collectively these studies demonstrate

positive clinical benefits from eccentric

loading but because none of these studies

has a comparison group using an alterna-

tive muscle contraction mode (concentric

or isometric) they are unable to show

whether the actual muscle contraction

mode plays a role in the outcome

The Effect of Eccentric Muscle Contrac-

tion Compared to Other Contraction

Regimes for Achilles Tendinopathy A

limited number of studies have investi-gated the effect of isolated eccentric ex-

ercise relative to other loading regimes

for Achilles tendinopathy961676989 It has

been shown that fast heel-drop exercises

with a high eccentric load were more ef-

fective in reducing overall pain than iso-

tonic concentriceccentric exercises at

lower loads67 Others have compared iso-

lated eccentric and concentric loading and

demonstrated similar pain reduction with

both regimes with the load on the ten-

don being greater in the eccentric (body weight plus backpack) than in the con-

centric (less or equal body weight) group

(TABLE 1)61 A more extensive rehabilitation

program that included concentriceccen-

tric loading with body weight yielded bet-

ter self-reported outcomes (questionnaire

on function and pain) than a concentric

program of a lesser total loading volume

not at 6 weeks but at 1-year follow-up89

Isolated eccentric loading with body

weight has also been compared to static

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy

StudyGroup Load Pain Improvementdagger

Bahr et al8

Isolated ECC 630 (100)Daggersect VISA-P 73

Croisier et al13

Isolated ECC 135 (130) VAS 71

Purdam et al78

Isolated ECC 630 (100)Daggersect VAS 62

Stasinopoulos and Stasinopoulos91

Isolated ECC 135 (100)Daggersect 5-point scale 80 (4 wk)

Visnes et al95

Isolated ECC + competitive volleyball 630 (100)Daggersect No improvement

Competitive volleyball (control) 0 (0) No improvement

Young et al103

Isolated ECC on 25deg decline board 630 (100)Daggersect VISA-P 25VAS 51

Isolated ECC on horizontal step 630 (100) VISA-P 18VAS 53

Jonsson and Alredson39

Isolated ECC 630 (100)Daggersect VISA-P 102para

VAS 69para

Isolated CON (n = 4) 630 (100)Daggersect VISA-P ndash9VAS 8

Table continues on page 859

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

trophy and increased stiffness o the hu-man patellar tendon J Appl Physiol (1985)2008105805-810 httpdxdoiorg101152japplphysiol903612008

13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

15 de Vos RJ Weir A van Schie HT et al Platelet-rich plasma injection or chronic Achilles tendi-nopathy a randomized controlled trial JAMA2010303144-149 httpdxdoiorg101001jama20091986

16 de Vos RJ Weir A Visser RJ de Winter T TolJL The additional value o a night splint to ec-centric exercises in chronic midportion Achillestendinopathy a randomised controlled trialBr J Sports Med 200741e5 httpdxdoiorg101136bjsm2006032532

17 Dideriksen K Muscle and tendon connective tis-sue adaptation to unloading exercise and NSAIDConnect Tissue Res 20145561-70 httpdxdoiorg103109030082072013862527

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19 Fahlstroumlm M Jonsson P Lorentzon R AlredsonH Chronic Achilles tendon pain treated with

eccentric cal-muscle training Knee Surg SportsTraumatol Arthrosc 200311327-333 httpdxdoiorg101007s00167-003-0418-z

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22 Ferretti A Epidemiology o jumperrsquos kneeSports Med 19863289-295

23 Finni T Komi PV Lepola V In vivo human tricepssurae and quadriceps emoris muscle unctionin a squat jump and counter movement jumpEur J Appl Physiol 200083416-426 httpdxdoiorg101007s004210000289

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Sci Sports 2008183-15 httpdxdoiorg101111j1600-0838200700746x

26 Frohm A Saartok T Halvorsen K Renstroumlm PEccentric treatment or patellar tendinopathy a

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27 Frost P Bonde JP Mikkelsen S et al Risk oshoulder tendinitis in relation to shoulderloads in monotonous repetitive work Am J Ind

Med 20024111-18 httpdxdoiorg101002ajim10019

28 Gaumlrdin A Bruno J Movin T Kristoffersen-WibergM Shalabi A Magnetic resonance signal ratherthan tendon volume correlates to pain andunctional impairment in chronic Achilles tendi-nopathy Acta Radiol 200647718-724 httpdxdoiorg10108002841850600774035

29 Garma T Kobayashi C Haddad F AdamsGR Bodell PW Baldwin KM Similar acutemolecular responses to equivalent volumeso isometric lengthening or shortening moderesistance exercise J Appl Physiol (1985)2007102135-143 httpdxdoiorg101152japplphysiol007762006

30 Gauvin R Parenteau-Bareil R Larouche D etal Dynamic mechanical stimulations induceanisotropy and improve the tensile properties oengineered tissues produced without exogenousscaffolding Acta Biomater 201173294-3301httpdxdoiorg101016jactbio201105034

31 Giddings VL Beaupreacute GS Whalen RT Carter DRCalcaneal loading during walking and running

Med Sci Sports Exerc 200032627-634 32 Glazebrook MA Wright JR Jr Langman M

Stanish WD Lee JM Histological analysis oAchilles tendons in an overuse rat model J

Orthop Res 200826840-846 httpdxdoiorg101002jor20546

33 Heinemeier KM Olesen JL Haddad F et alExpression o collagen and related growthactors in rat tendon and skeletal muscle in re-sponse to specific contraction types J Physiol20075821303-1316 httpdxdoiorg101113jphysiol2007127639

34 Heinemeier KM Schjerling P Heinemeier JMagnusson SP Kjaer M Lack o tissue renewalin human adult Achilles tendon is revealed by

nuclear bomb 13C FASEB J 2013272074-2079httpdxdoiorg101096f12-225599

35 Heinemeier KM Skovgaard D Bayer ML et alUphill running improves rat Achilles tendon tis-sue mechanical properties and alters gene ex-pression without inducing pathological changesJ Appl Physiol (1985) 2012113827-836 httpdxdoiorg101152japplphysiol004012012

36 Henriksen M Aaboe J Bliddal H LangbergH Biomechanical characteristics o the ec-centric Achilles tendon exercise J Biomech2009422702-2707 httpdxdoiorg101016jjbiomech200908009

37 Hill AV The heat o shortening and the dynamic

constants o muscle Proc R Soc Lond B Biol Sci1938126136-195 httpdxdoiorg101098rspb19380050

38 Holloszy JO Coyle EF Adaptations o skeletalmuscle to endurance exercise and their meta-

bolic consequences J Appl Physiol Respir Envi-ron Exerc Physiol 198456831-838

39 Jonsson P Alredson H Superior results witheccentric compared to concentric quadricepstraining in patients with jumperrsquos knee a pro-spective randomised study Br J Sports Med200539847-850 httpdxdoiorg101136bjsm2005018630

40 Jonsson P Alredson H Sunding K Fahlstroumlm MCook J New regimen or eccentric cal-muscletraining in patients with chronic insertionalAchilles tendinopathy results o a pilot studyBr J Sports Med 200842746-749 httpdxdoiorg101136bjsm2007039545

41 Joshi SD Webb K Variation o cyclic strain

parameters regulates development o elasticmodulus in fibroblastsubstrate constructsJ Orthop Res 2008261105-1113 httpdxdoiorg101002jor20626

42 Kalson NS Holmes DF Herchenhan A Lu YStarborg T Kadler KE Slow stretching that mim-ics embryonic growth rate stimulates structuraland mechanical development o tendon-liketissue in vitro Dev Dyn 20112402520-2528httpdxdoiorg101002dvdy22760

43 Ker RF Wang XT Pike AV Fatigue qual-ity o mammalian tendons J Exp Biol20002031317-1327

44 Kettunen JA Kvist M Alanen E Kujala UMLong-term prognosis or jumperrsquos knee in male

athletes A prospective ollow-up study Am JSports Med 200230689-692

45 Khan K Cook J The painul nonrupturedtendon clinical aspects Clin Sports Med200322711-725

46 Khan KM Cook JL Kannus P Maffulli N BonarSF Time to abandon the ldquotendinitisrdquo myth BMJ2002324626-627 httpdxdoiorg101136bmj3247338626

47 Kingma JJ de Knikker R Wittink HM TakkenT Eccentric overload training in patients withchronic Achilles tendinopathy a systematic re-view Br J Sports Med 200741e3 httpdxdoiorg101136bjsm2006030916

48 Kjaer M Role o extracellular matrix in adapta-

tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

49 Kongsgaard M Kovanen V Aagaard P et alCorticosteroid injections eccentric declinesquat training and heavy slow resistancetraining in patellar tendinopathy Scand J Med

Sci Sports 200919790-802 httpdxdoiorg101111j1600-0838200900949x

50 Kongsgaard M Qvortrup K Larsen J et alFibril morphology and tendon mechanicalproperties in patellar tendinopathy effectso heavy slow resistance training Am J

Sports Med 201038749-756 httpdxdoi

org1011770363546509350915 51 Kubo K Kanehisa H Fukunaga T Effects o

different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

org101111j1469-779320010649cxd 52 Kujala UM Sarna S Kaprio J Cumulative

incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

J Sport Med 200515133-135 httpdxdoiorg10109701jsm00001653475563823

53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

Med Sci Sports 20071761-66 httpdxdoiorg101111j1600-0838200600522x

54 Langberg H Olesen J Skovgaard D Kjaer M Agerelated blood flow around the Achilles tendonduring exercise in humans Eur J Appl Physiol

200184246-248 httpdxdoiorg101007s004210170013

55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

59 Maeda E Shelton JC Bader DL Lee DA Timedependence o cyclic tensile strain on collagenproduction in tendon ascicles Biochem Bio-

phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

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journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 859

pants remained in the concentric group

hampering any meaningful comparison

and firm conclusion

Other studies have compared load-

ing regimes without matching the load(TABLE 2) Isolated eccentric squats on a

decline board have been compared to

mixed concentriceccentric squats on

a flat surface in elite volleyball players

both groups performed exercises on only

the affected extremity for 12 weeks be-

fore starting the competitive season103

Both protocols resulted in reduced pain

and increased function without a differ-

ence between the groups Twelve weeks

of isolated heavy eccentric training using

few repetitions of high load (100 MVCapproximately 170 body weight) has

been compared with isolated eccentric

squats on a decline board using a larg-

er number of repetitions at lower load

(100 body weight approximately 60

MVC)26 Both groups markedly improved

in pain and function but without a differ-

ence between the groups Another study

compared eccentric drop squats land-

ing on 2 feet (60 repetitions per session)

with knee flexionextension exercise (30

repetitions per session) with the aim ofcreating a high concentric load compo-

nent (75-80 MVC)10 Both groups

trained with progressive loads 5 times

weekly and had reduced tendon pain

after 12 weeks but outcomes were no

different between groups Only 1 study

has investigated biochemical outcomes

the efficacy of isolated eccentric squats

compared to mixed concentriceccentric

heavy slow resistance training49 Both ex-

ercise regimes resulted in reduced pain

and improved function but biochemicalchanges (increased collagen content and

reduced glycation) were only evident with

heavy slow resistance training In addi-

tion heavy slow resistance training was

associated with structural changes50

Therefore collectively there is no firm

evidence to support the notion that ec-

centric loading is more efficient than

concentric or other loading regimes for

patellar tendinopathy Most studies have

not matched for other parameters such

in clinical improvement when patients

were instructed to refrain from sports ac-

tivity during the intervention period3991

However in elite volleyball players with

patellar tendinopathy adding 8 weeks of

isolated eccentric loading to the already

existing activity during the season did

not confer any pain relief95 In contrast in

Achilles tendinopathy it has been shown

that moderate physical activity during

the treatment period was not detrimen-tal to the benefits of eccentric exercise88

The apparent difference between activ-

ity at an elite level and more moderate

activity may be related to insufficient

recovery time or possibly the total load

volume of sports activity and the added

eccentric-loading exercises63 although

this requires further investigation Ultra-

sonography has been used to investigate

structural changes (tendon thickness and

Doppler activity) in patellar tendinopa-

thy following eccentric exercise but has

not demonstrated significant effects49

Collectively the above studies show that

eccentric loading may provide clinical

benefits in patellar tendinopathy treat-

ment but again whether the actual di-

rection of muscle contraction plays a role

in the outcome or clinical benefits are in-

stead related to the absolute magnitude

of loading is unclear as none of these

studies had a similar comparison groupThe Effect of Eccentric Muscle Contraction

Compared to Other Contraction Regimes

for Patellar Tendinopathy For patellar

tendinopathy only 1 study has compared

isolated eccentric loading with an identi-

cal concentric-loading regime at equal

load magnitude volume and speed39 The

authors39 concluded that eccentric loading

was more effective in reducing pain than

concentric loading however due to a high

number of dropouts only 4 of 7 partici-

TABLE 2Exercise Programs Used in Studies

for Patellar Tendinopathy (continued)

Abbreviations CON concentric ECC eccentric VAS visual analog scale VISA-P Victorian Institute

of Sport Assessment-patella

Load reported as weekly repetitions and estimated load as percentage of body weight (50 body

weight is 2 legged and 100 is 1 legged) In general peak load is listed but for studies with load

progression that did not report the achieved progress only the load before progression is listed

No attempt was made to evaluate load in stretching exercisesdaggerUnless otherwise stated all studies had 12 weeks of interventionDagger Pain acceptedsect Study included unreported progression beyond what is listed Estimated percent body weight from maximal voluntary contraction or other external loadpara Improvement in ECC group significantly greater than in comparator

StudyGroup Load Pain Improvementdagger

Kongsgaard et al49

Isolated ECC 630 (100)Dagger VISA-P 42

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 39

Kongsgaard et al50

No ECC

Heavy slow resistance (ECC + CON) 288 (130)Dagger VISA-P 27

Frohm et al26

Isolated ECC 315 (100)Daggersect VISA-P 108

Isolated ECC overload 32 (170)Dagger VISA-P 76

Cannell et al10

ECC drop squats 300 (60)Daggersect VAS 55

Mixed ECC + CON ocused on CON 150 (CON 125)sect

(ECC 63)VAS 31

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

trophy and increased stiffness o the hu-man patellar tendon J Appl Physiol (1985)2008105805-810 httpdxdoiorg101152japplphysiol903612008

13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

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17 Dideriksen K Muscle and tendon connective tis-sue adaptation to unloading exercise and NSAIDConnect Tissue Res 20145561-70 httpdxdoiorg103109030082072013862527

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eccentric cal-muscle training Knee Surg SportsTraumatol Arthrosc 200311327-333 httpdxdoiorg101007s00167-003-0418-z

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21 Feng Z Tateishi Y Nomura Y Kitajima T Na-kamura T Construction o fibroblastndashcollagengels with orientated fibrils induced by static ordynamic stress toward the abrication o smalltendon grats J Artif Organs 20069220-225httpdxdoiorg101007s10047-006-0354-z

22 Ferretti A Epidemiology o jumperrsquos kneeSports Med 19863289-295

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25 Fredberg U Stengaard-Pedersen KChronic tendinopathy tissue pathologypain mechanisms and etiology with a spe-

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12 Couppeacute C Kongsgaard M Aagaard P et alHabitual loading results in tendon hyper-

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1012

journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 861

cial ocus on inflammation Scand J Med

Sci Sports 2008183-15 httpdxdoiorg101111j1600-0838200700746x

26 Frohm A Saartok T Halvorsen K Renstroumlm PEccentric treatment or patellar tendinopathy a

prospective randomised short-term pilot studyo two rehabilitation protocols Br J Sports

Med 200741e7 httpdxdoiorg101136bjsm2006032599

27 Frost P Bonde JP Mikkelsen S et al Risk oshoulder tendinitis in relation to shoulderloads in monotonous repetitive work Am J Ind

Med 20024111-18 httpdxdoiorg101002ajim10019

28 Gaumlrdin A Bruno J Movin T Kristoffersen-WibergM Shalabi A Magnetic resonance signal ratherthan tendon volume correlates to pain andunctional impairment in chronic Achilles tendi-nopathy Acta Radiol 200647718-724 httpdxdoiorg10108002841850600774035

29 Garma T Kobayashi C Haddad F AdamsGR Bodell PW Baldwin KM Similar acutemolecular responses to equivalent volumeso isometric lengthening or shortening moderesistance exercise J Appl Physiol (1985)2007102135-143 httpdxdoiorg101152japplphysiol007762006

30 Gauvin R Parenteau-Bareil R Larouche D etal Dynamic mechanical stimulations induceanisotropy and improve the tensile properties oengineered tissues produced without exogenousscaffolding Acta Biomater 201173294-3301httpdxdoiorg101016jactbio201105034

31 Giddings VL Beaupreacute GS Whalen RT Carter DRCalcaneal loading during walking and running

Med Sci Sports Exerc 200032627-634 32 Glazebrook MA Wright JR Jr Langman M

Stanish WD Lee JM Histological analysis oAchilles tendons in an overuse rat model J

Orthop Res 200826840-846 httpdxdoiorg101002jor20546

33 Heinemeier KM Olesen JL Haddad F et alExpression o collagen and related growthactors in rat tendon and skeletal muscle in re-sponse to specific contraction types J Physiol20075821303-1316 httpdxdoiorg101113jphysiol2007127639

34 Heinemeier KM Schjerling P Heinemeier JMagnusson SP Kjaer M Lack o tissue renewalin human adult Achilles tendon is revealed by

nuclear bomb 13C FASEB J 2013272074-2079httpdxdoiorg101096f12-225599

35 Heinemeier KM Skovgaard D Bayer ML et alUphill running improves rat Achilles tendon tis-sue mechanical properties and alters gene ex-pression without inducing pathological changesJ Appl Physiol (1985) 2012113827-836 httpdxdoiorg101152japplphysiol004012012

36 Henriksen M Aaboe J Bliddal H LangbergH Biomechanical characteristics o the ec-centric Achilles tendon exercise J Biomech2009422702-2707 httpdxdoiorg101016jjbiomech200908009

37 Hill AV The heat o shortening and the dynamic

constants o muscle Proc R Soc Lond B Biol Sci1938126136-195 httpdxdoiorg101098rspb19380050

38 Holloszy JO Coyle EF Adaptations o skeletalmuscle to endurance exercise and their meta-

bolic consequences J Appl Physiol Respir Envi-ron Exerc Physiol 198456831-838

39 Jonsson P Alredson H Superior results witheccentric compared to concentric quadricepstraining in patients with jumperrsquos knee a pro-spective randomised study Br J Sports Med200539847-850 httpdxdoiorg101136bjsm2005018630

40 Jonsson P Alredson H Sunding K Fahlstroumlm MCook J New regimen or eccentric cal-muscletraining in patients with chronic insertionalAchilles tendinopathy results o a pilot studyBr J Sports Med 200842746-749 httpdxdoiorg101136bjsm2007039545

41 Joshi SD Webb K Variation o cyclic strain

parameters regulates development o elasticmodulus in fibroblastsubstrate constructsJ Orthop Res 2008261105-1113 httpdxdoiorg101002jor20626

42 Kalson NS Holmes DF Herchenhan A Lu YStarborg T Kadler KE Slow stretching that mim-ics embryonic growth rate stimulates structuraland mechanical development o tendon-liketissue in vitro Dev Dyn 20112402520-2528httpdxdoiorg101002dvdy22760

43 Ker RF Wang XT Pike AV Fatigue qual-ity o mammalian tendons J Exp Biol20002031317-1327

44 Kettunen JA Kvist M Alanen E Kujala UMLong-term prognosis or jumperrsquos knee in male

athletes A prospective ollow-up study Am JSports Med 200230689-692

45 Khan K Cook J The painul nonrupturedtendon clinical aspects Clin Sports Med200322711-725

46 Khan KM Cook JL Kannus P Maffulli N BonarSF Time to abandon the ldquotendinitisrdquo myth BMJ2002324626-627 httpdxdoiorg101136bmj3247338626

47 Kingma JJ de Knikker R Wittink HM TakkenT Eccentric overload training in patients withchronic Achilles tendinopathy a systematic re-view Br J Sports Med 200741e3 httpdxdoiorg101136bjsm2006030916

48 Kjaer M Role o extracellular matrix in adapta-

tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

49 Kongsgaard M Kovanen V Aagaard P et alCorticosteroid injections eccentric declinesquat training and heavy slow resistancetraining in patellar tendinopathy Scand J Med

Sci Sports 200919790-802 httpdxdoiorg101111j1600-0838200900949x

50 Kongsgaard M Qvortrup K Larsen J et alFibril morphology and tendon mechanicalproperties in patellar tendinopathy effectso heavy slow resistance training Am J

Sports Med 201038749-756 httpdxdoi

org1011770363546509350915 51 Kubo K Kanehisa H Fukunaga T Effects o

different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

org101111j1469-779320010649cxd 52 Kujala UM Sarna S Kaprio J Cumulative

incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

J Sport Med 200515133-135 httpdxdoiorg10109701jsm00001653475563823

53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

Med Sci Sports 20071761-66 httpdxdoiorg101111j1600-0838200600522x

54 Langberg H Olesen J Skovgaard D Kjaer M Agerelated blood flow around the Achilles tendonduring exercise in humans Eur J Appl Physiol

200184246-248 httpdxdoiorg101007s004210170013

55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

59 Maeda E Shelton JC Bader DL Lee DA Timedependence o cyclic tensile strain on collagenproduction in tendon ascicles Biochem Bio-

phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

Page 9: 45-11 Couppe 2

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860 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

as load speed frequency and rest peri-

ods102639 and it is therefore still unclear

what specific load magnitude frequency

or total load volume per session should be

used to provide meaningful clinical andstructural improvements in patients with

patellar tendinopathy

Clinical Implications andFuture DirectionsTendinopathies are a common ailment

among athletes and there is currently

an incomplete picture of the etiology

Although there are several suggested

treatment options loading regimes ap-

pear to have good clinical results Early

works have shown an exercise program with isolated eccentric contraction to

have good clinical outcomes which pro-

moted the paradigm of eccentric loading

for tendinopathy However as outlined

in this review there is little evidence for

isolating the eccentric component of a

loading-based regime The basic mecha-

nisms that are likely to influence tendon

adaptations appear to be related mainly

to tendon loadstrain magnitude and du-

ration and there is no theoretical basis

for greater tendon loads in eccentric ex-ercises at a given force (body weight or

external load)

There is a paucity of clinical trials

directly comparing different exercise

regimes and different exercise dosages

but the available evidence provides little

support for the superiority of isolated

eccentrics It is worth noting that stud-

ies rarely use comparable load magni-

tude when comparing eccentric to other

load regimes To delineate the effects of

mode and load magnitude future workshould compare isolated eccentric and

concentric action under equal load at

various exercise dosages in individuals

with tendinopathy The focus on eccen-

tric exercise has overshadowed other as-

pects of tendinopathy rehabilitation and

acknowledgement of the limited evidence

may prompt a broader approach includ-

ing the use of heavy load and low speed

which has some support from both basic

science and clinical trials 983156

trophy and increased stiffness o the hu-man patellar tendon J Appl Physiol (1985)2008105805-810 httpdxdoiorg101152japplphysiol903612008

13 Croisier JL Forthomme B Foidart-Dessalle M

Godon B Crielaard JM Treatment o recurrenttendinitis by isokinetic eccentric exercises Iso-

kinet Exerc Sci 20019133-141 14 de Jonge S de Vos RJ Van Schie HT Verhaar

JA Weir A Tol JL One-year ollow-up o arandomised controlled trial on added splint-ing to eccentric exercises in chronic midpor-tion Achilles tendinopathy Br J Sports Med201044673-677 httpdxdoiorg101136bjsm2008052142

15 de Vos RJ Weir A van Schie HT et al Platelet-rich plasma injection or chronic Achilles tendi-nopathy a randomized controlled trial JAMA2010303144-149 httpdxdoiorg101001jama20091986

16 de Vos RJ Weir A Visser RJ de Winter T TolJL The additional value o a night splint to ec-centric exercises in chronic midportion Achillestendinopathy a randomised controlled trialBr J Sports Med 200741e5 httpdxdoiorg101136bjsm2006032532

17 Dideriksen K Muscle and tendon connective tis-sue adaptation to unloading exercise and NSAIDConnect Tissue Res 20145561-70 httpdxdoiorg103109030082072013862527

18 Enoka RM Eccentric contractions requireunique activation strategies by the nervous sys-tem J Appl Physiol (1985) 1996812339-2346

19 Fahlstroumlm M Jonsson P Lorentzon R AlredsonH Chronic Achilles tendon pain treated with

eccentric cal-muscle training Knee Surg SportsTraumatol Arthrosc 200311327-333 httpdxdoiorg101007s00167-003-0418-z

20 Farup J Rahbek SK Vendelbo MH et al Wheyprotein hydrolysate augments tendon and mus-cle hypertrophy independent o resistance exer-cise contraction mode Scand J Med Sci Sports201424788-798 httpdxdoiorg101111sms12083

21 Feng Z Tateishi Y Nomura Y Kitajima T Na-kamura T Construction o fibroblastndashcollagengels with orientated fibrils induced by static ordynamic stress toward the abrication o smalltendon grats J Artif Organs 20069220-225httpdxdoiorg101007s10047-006-0354-z

22 Ferretti A Epidemiology o jumperrsquos kneeSports Med 19863289-295

23 Finni T Komi PV Lepola V In vivo human tricepssurae and quadriceps emoris muscle unctionin a squat jump and counter movement jumpEur J Appl Physiol 200083416-426 httpdxdoiorg101007s004210000289

24 Folkhard W Geercken W Knoumlrzer E et alStructural dynamic o native tendon collagenJ Mol Biol 1987193405-407 httpdxdoiorg1010160022-2836(87)90228-2

25 Fredberg U Stengaard-Pedersen KChronic tendinopathy tissue pathologypain mechanisms and etiology with a spe-

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matol Arthrosc 200311196-199 httpdxdoiorg101007s00167-003-0360-0

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6 Arampatzis A Peper A Bierbaum S Al-bracht K Plasticity o human Achilles tendonmechanical and morphological propertiesin response to cyclic strain J Biomech2010433073-3079 httpdxdoiorg101016jjbiomech201008014

7 Arnoczky SP Lavagnino M Egerbacher MThe mechanobiological aetiopathogenesiso tendinopathy is it the over-stimulation or

the under-stimulation o tendon cells Int JExp Pathol 200788217-226 httpdxdoiorg101111j1365-2613200700548x

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Surg Am 2006881689-1698 httpdxdoiorg102106JBJSE01181

9 Beyer R Kongsgaard M Hougs Kjaer BOslashhlenschlaeligger T Kjaer M Magnusson SPHeavy slow resistance versus eccentric train-ing as treatment or Achilles tendinopathya randomized controlled trial Am J Sports

Med 2015431704-1711 httpdxdoi

org1011770363546515584760 10 Cannell LJ Taunton JE Clement DB Smith C

Khan KM A randomised clinical trial o the effi-cacy o drop squats or leg extensionleg curl exer-cises to treat clinically diagnosed jumperrsquos knee inathletes pilot study Br J Sports Med 20013560-64 httpdxdoiorg101136bjsm35160

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12 Couppeacute C Kongsgaard M Aagaard P et alHabitual loading results in tendon hyper-

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1012

journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 861

cial ocus on inflammation Scand J Med

Sci Sports 2008183-15 httpdxdoiorg101111j1600-0838200700746x

26 Frohm A Saartok T Halvorsen K Renstroumlm PEccentric treatment or patellar tendinopathy a

prospective randomised short-term pilot studyo two rehabilitation protocols Br J Sports

Med 200741e7 httpdxdoiorg101136bjsm2006032599

27 Frost P Bonde JP Mikkelsen S et al Risk oshoulder tendinitis in relation to shoulderloads in monotonous repetitive work Am J Ind

Med 20024111-18 httpdxdoiorg101002ajim10019

28 Gaumlrdin A Bruno J Movin T Kristoffersen-WibergM Shalabi A Magnetic resonance signal ratherthan tendon volume correlates to pain andunctional impairment in chronic Achilles tendi-nopathy Acta Radiol 200647718-724 httpdxdoiorg10108002841850600774035

29 Garma T Kobayashi C Haddad F AdamsGR Bodell PW Baldwin KM Similar acutemolecular responses to equivalent volumeso isometric lengthening or shortening moderesistance exercise J Appl Physiol (1985)2007102135-143 httpdxdoiorg101152japplphysiol007762006

30 Gauvin R Parenteau-Bareil R Larouche D etal Dynamic mechanical stimulations induceanisotropy and improve the tensile properties oengineered tissues produced without exogenousscaffolding Acta Biomater 201173294-3301httpdxdoiorg101016jactbio201105034

31 Giddings VL Beaupreacute GS Whalen RT Carter DRCalcaneal loading during walking and running

Med Sci Sports Exerc 200032627-634 32 Glazebrook MA Wright JR Jr Langman M

Stanish WD Lee JM Histological analysis oAchilles tendons in an overuse rat model J

Orthop Res 200826840-846 httpdxdoiorg101002jor20546

33 Heinemeier KM Olesen JL Haddad F et alExpression o collagen and related growthactors in rat tendon and skeletal muscle in re-sponse to specific contraction types J Physiol20075821303-1316 httpdxdoiorg101113jphysiol2007127639

34 Heinemeier KM Schjerling P Heinemeier JMagnusson SP Kjaer M Lack o tissue renewalin human adult Achilles tendon is revealed by

nuclear bomb 13C FASEB J 2013272074-2079httpdxdoiorg101096f12-225599

35 Heinemeier KM Skovgaard D Bayer ML et alUphill running improves rat Achilles tendon tis-sue mechanical properties and alters gene ex-pression without inducing pathological changesJ Appl Physiol (1985) 2012113827-836 httpdxdoiorg101152japplphysiol004012012

36 Henriksen M Aaboe J Bliddal H LangbergH Biomechanical characteristics o the ec-centric Achilles tendon exercise J Biomech2009422702-2707 httpdxdoiorg101016jjbiomech200908009

37 Hill AV The heat o shortening and the dynamic

constants o muscle Proc R Soc Lond B Biol Sci1938126136-195 httpdxdoiorg101098rspb19380050

38 Holloszy JO Coyle EF Adaptations o skeletalmuscle to endurance exercise and their meta-

bolic consequences J Appl Physiol Respir Envi-ron Exerc Physiol 198456831-838

39 Jonsson P Alredson H Superior results witheccentric compared to concentric quadricepstraining in patients with jumperrsquos knee a pro-spective randomised study Br J Sports Med200539847-850 httpdxdoiorg101136bjsm2005018630

40 Jonsson P Alredson H Sunding K Fahlstroumlm MCook J New regimen or eccentric cal-muscletraining in patients with chronic insertionalAchilles tendinopathy results o a pilot studyBr J Sports Med 200842746-749 httpdxdoiorg101136bjsm2007039545

41 Joshi SD Webb K Variation o cyclic strain

parameters regulates development o elasticmodulus in fibroblastsubstrate constructsJ Orthop Res 2008261105-1113 httpdxdoiorg101002jor20626

42 Kalson NS Holmes DF Herchenhan A Lu YStarborg T Kadler KE Slow stretching that mim-ics embryonic growth rate stimulates structuraland mechanical development o tendon-liketissue in vitro Dev Dyn 20112402520-2528httpdxdoiorg101002dvdy22760

43 Ker RF Wang XT Pike AV Fatigue qual-ity o mammalian tendons J Exp Biol20002031317-1327

44 Kettunen JA Kvist M Alanen E Kujala UMLong-term prognosis or jumperrsquos knee in male

athletes A prospective ollow-up study Am JSports Med 200230689-692

45 Khan K Cook J The painul nonrupturedtendon clinical aspects Clin Sports Med200322711-725

46 Khan KM Cook JL Kannus P Maffulli N BonarSF Time to abandon the ldquotendinitisrdquo myth BMJ2002324626-627 httpdxdoiorg101136bmj3247338626

47 Kingma JJ de Knikker R Wittink HM TakkenT Eccentric overload training in patients withchronic Achilles tendinopathy a systematic re-view Br J Sports Med 200741e3 httpdxdoiorg101136bjsm2006030916

48 Kjaer M Role o extracellular matrix in adapta-

tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

49 Kongsgaard M Kovanen V Aagaard P et alCorticosteroid injections eccentric declinesquat training and heavy slow resistancetraining in patellar tendinopathy Scand J Med

Sci Sports 200919790-802 httpdxdoiorg101111j1600-0838200900949x

50 Kongsgaard M Qvortrup K Larsen J et alFibril morphology and tendon mechanicalproperties in patellar tendinopathy effectso heavy slow resistance training Am J

Sports Med 201038749-756 httpdxdoi

org1011770363546509350915 51 Kubo K Kanehisa H Fukunaga T Effects o

different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

org101111j1469-779320010649cxd 52 Kujala UM Sarna S Kaprio J Cumulative

incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

J Sport Med 200515133-135 httpdxdoiorg10109701jsm00001653475563823

53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

Med Sci Sports 20071761-66 httpdxdoiorg101111j1600-0838200600522x

54 Langberg H Olesen J Skovgaard D Kjaer M Agerelated blood flow around the Achilles tendonduring exercise in humans Eur J Appl Physiol

200184246-248 httpdxdoiorg101007s004210170013

55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

59 Maeda E Shelton JC Bader DL Lee DA Timedependence o cyclic tensile strain on collagenproduction in tendon ascicles Biochem Bio-

phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1112

862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1212

amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

Page 10: 45-11 Couppe 2

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1012

journal of orthopaedic amp sports physical therapy | volume 45 | number 11 | november 2015 | 861

cial ocus on inflammation Scand J Med

Sci Sports 2008183-15 httpdxdoiorg101111j1600-0838200700746x

26 Frohm A Saartok T Halvorsen K Renstroumlm PEccentric treatment or patellar tendinopathy a

prospective randomised short-term pilot studyo two rehabilitation protocols Br J Sports

Med 200741e7 httpdxdoiorg101136bjsm2006032599

27 Frost P Bonde JP Mikkelsen S et al Risk oshoulder tendinitis in relation to shoulderloads in monotonous repetitive work Am J Ind

Med 20024111-18 httpdxdoiorg101002ajim10019

28 Gaumlrdin A Bruno J Movin T Kristoffersen-WibergM Shalabi A Magnetic resonance signal ratherthan tendon volume correlates to pain andunctional impairment in chronic Achilles tendi-nopathy Acta Radiol 200647718-724 httpdxdoiorg10108002841850600774035

29 Garma T Kobayashi C Haddad F AdamsGR Bodell PW Baldwin KM Similar acutemolecular responses to equivalent volumeso isometric lengthening or shortening moderesistance exercise J Appl Physiol (1985)2007102135-143 httpdxdoiorg101152japplphysiol007762006

30 Gauvin R Parenteau-Bareil R Larouche D etal Dynamic mechanical stimulations induceanisotropy and improve the tensile properties oengineered tissues produced without exogenousscaffolding Acta Biomater 201173294-3301httpdxdoiorg101016jactbio201105034

31 Giddings VL Beaupreacute GS Whalen RT Carter DRCalcaneal loading during walking and running

Med Sci Sports Exerc 200032627-634 32 Glazebrook MA Wright JR Jr Langman M

Stanish WD Lee JM Histological analysis oAchilles tendons in an overuse rat model J

Orthop Res 200826840-846 httpdxdoiorg101002jor20546

33 Heinemeier KM Olesen JL Haddad F et alExpression o collagen and related growthactors in rat tendon and skeletal muscle in re-sponse to specific contraction types J Physiol20075821303-1316 httpdxdoiorg101113jphysiol2007127639

34 Heinemeier KM Schjerling P Heinemeier JMagnusson SP Kjaer M Lack o tissue renewalin human adult Achilles tendon is revealed by

nuclear bomb 13C FASEB J 2013272074-2079httpdxdoiorg101096f12-225599

35 Heinemeier KM Skovgaard D Bayer ML et alUphill running improves rat Achilles tendon tis-sue mechanical properties and alters gene ex-pression without inducing pathological changesJ Appl Physiol (1985) 2012113827-836 httpdxdoiorg101152japplphysiol004012012

36 Henriksen M Aaboe J Bliddal H LangbergH Biomechanical characteristics o the ec-centric Achilles tendon exercise J Biomech2009422702-2707 httpdxdoiorg101016jjbiomech200908009

37 Hill AV The heat o shortening and the dynamic

constants o muscle Proc R Soc Lond B Biol Sci1938126136-195 httpdxdoiorg101098rspb19380050

38 Holloszy JO Coyle EF Adaptations o skeletalmuscle to endurance exercise and their meta-

bolic consequences J Appl Physiol Respir Envi-ron Exerc Physiol 198456831-838

39 Jonsson P Alredson H Superior results witheccentric compared to concentric quadricepstraining in patients with jumperrsquos knee a pro-spective randomised study Br J Sports Med200539847-850 httpdxdoiorg101136bjsm2005018630

40 Jonsson P Alredson H Sunding K Fahlstroumlm MCook J New regimen or eccentric cal-muscletraining in patients with chronic insertionalAchilles tendinopathy results o a pilot studyBr J Sports Med 200842746-749 httpdxdoiorg101136bjsm2007039545

41 Joshi SD Webb K Variation o cyclic strain

parameters regulates development o elasticmodulus in fibroblastsubstrate constructsJ Orthop Res 2008261105-1113 httpdxdoiorg101002jor20626

42 Kalson NS Holmes DF Herchenhan A Lu YStarborg T Kadler KE Slow stretching that mim-ics embryonic growth rate stimulates structuraland mechanical development o tendon-liketissue in vitro Dev Dyn 20112402520-2528httpdxdoiorg101002dvdy22760

43 Ker RF Wang XT Pike AV Fatigue qual-ity o mammalian tendons J Exp Biol20002031317-1327

44 Kettunen JA Kvist M Alanen E Kujala UMLong-term prognosis or jumperrsquos knee in male

athletes A prospective ollow-up study Am JSports Med 200230689-692

45 Khan K Cook J The painul nonrupturedtendon clinical aspects Clin Sports Med200322711-725

46 Khan KM Cook JL Kannus P Maffulli N BonarSF Time to abandon the ldquotendinitisrdquo myth BMJ2002324626-627 httpdxdoiorg101136bmj3247338626

47 Kingma JJ de Knikker R Wittink HM TakkenT Eccentric overload training in patients withchronic Achilles tendinopathy a systematic re-view Br J Sports Med 200741e3 httpdxdoiorg101136bjsm2006030916

48 Kjaer M Role o extracellular matrix in adapta-

tion o tendon and skeletal muscle to mechani-cal loading Physiol Rev 200484649-698httpdxdoiorg101152physrev000312003

49 Kongsgaard M Kovanen V Aagaard P et alCorticosteroid injections eccentric declinesquat training and heavy slow resistancetraining in patellar tendinopathy Scand J Med

Sci Sports 200919790-802 httpdxdoiorg101111j1600-0838200900949x

50 Kongsgaard M Qvortrup K Larsen J et alFibril morphology and tendon mechanicalproperties in patellar tendinopathy effectso heavy slow resistance training Am J

Sports Med 201038749-756 httpdxdoi

org1011770363546509350915 51 Kubo K Kanehisa H Fukunaga T Effects o

different duration isometric contractions ontendon elasticity in human quadriceps musclesJ Physiol 2001536649-655 httpdxdoi

org101111j1469-779320010649cxd 52 Kujala UM Sarna S Kaprio J Cumulative

incidence o Achilles tendon rupture and ten-dinopathy in male ormer elite athletes Clin

J Sport Med 200515133-135 httpdxdoiorg10109701jsm00001653475563823

53 Langberg H Ellingsgaard H Madsen T et alEccentric rehabilitation exercise increasesperitendinous type I collagen synthesis inhumans with Achilles tendinosis Scand J

Med Sci Sports 20071761-66 httpdxdoiorg101111j1600-0838200600522x

54 Langberg H Olesen J Skovgaard D Kjaer M Agerelated blood flow around the Achilles tendonduring exercise in humans Eur J Appl Physiol

200184246-248 httpdxdoiorg101007s004210170013

55 Langberg H Skovgaard D Petersen LJ BuumllowJ Kjaer M Type I collagen synthesis and deg-radation in peritendinous tissue ater exercisedetermined by microdialysis in humansJ Physiol 1999521 pt 1299-306 httpdxdoiorg101111j1469-7793199900299x

56 Lavagnino M Arnoczky SP Tian T Vaupel Z E-ect o amplitude and requency o cyclic tensilestrain on the inhibition o MMP-1 mRNA expres-sion in tendon cells an in vitro study Connect

Tissue Res 200344181-187 57 Lian OslashB Engebretsen L Bahr R Prevalence

o jumperrsquos knee among elite athletes rom

different sports a cross-sectional study AmJ Sports Med 200533561-567 httpdxdoiorg1011770363546504270454

58 Lopes AD Hespanhol Junior LC Yeung SSCosta LO What are the main running-relatedmusculoskeletal injuries A systematic reviewSports Med 201242891-905 httpdxdoiorg101007BF03262301

59 Maeda E Shelton JC Bader DL Lee DA Timedependence o cyclic tensile strain on collagenproduction in tendon ascicles Biochem Bio-

phys Res Commun 2007362399-404 httpdxdoiorg101016jbbrc200708029

60 Maffulli N Khan KM Puddu G Overuse tendonconditions time to change a conusing termi-

nology Arthroscopy 199814840-843 httpdxdoiorg101016S0749-8063(98)70021-0

61 Mafi N Lorentzon R Alredson H Superiorshort-term results with eccentric cal muscletraining compared to concentric training in arandomized prospective multicenter study onpatients with chronic Achilles tendinosis Knee

Surg Sports Traumatol Arthrosc 2001942-47httpdxdoiorg101007s001670000148

62 Magnusson SP Aagaard P Dyhre-Poulsen PKjaer M Load-displacement properties othe human triceps surae aponeurosis in vivoJ Physiol 2001531277-288 httpdxdoiorg101111j1469-779320010277jx

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1112

862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

8202019 45-11 Couppe 2

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amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

Page 11: 45-11 Couppe 2

8202019 45-11 Couppe 2

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862 | november 2015 | volume 45 | number 11 | journal of orthopaedic amp sports physical therapy

[ CLINICAL COMMENTARY ]

gastrocnemius-soleus complex in chronic Achil-les tendinopathy results in decreased tendonvolume and intratendinous signal as evaluatedby MRI Am J Sports Med 2004321286-1296httpdxdoiorg1011770363546504263148

87 Shepherd JH Screen HR Fatigue loading o ten-don Int J Exp Pathol 201394260-270 httpdxdoiorg101111iep12037

88 Silbernagel KG Thomeeacute R Eriksson BIKarlsson J Continued sports activity usinga pain-monitoring model during rehabilita-tion in patients with Achilles tendinopathya randomized controlled study Am J Sports

Med 200735897-906 httpdxdoiorg1011770363546506298279

89 Silbernagel KG Thomeeacute R Thomeeacute P Karls-son J Eccentric overload training or patientswith chronic Achilles tendon pain ndash a ran-domised controlled study with reliability test-ing o the evaluation methods Scand J Med

Sci Sports 200111197-206 httpdxdoiorg101034j1600-08382001110402x

90 Stanish WD Rubinovich RM Curwin S Eccentricexercise in chronic tendinitis Clin Orthop Relat

Res 198665-68 91 Stasinopoulos D Stasinopoulos I Comparison

o effects o exercise programme pulsed ultra-sound and transverse riction in the treatmento chronic patellar tendinopathy Clin Rehabil200418347-352

92 Sussmilch-Leitch SP Collins NJ BialocerkowskiAE Warden SJ Crossley KM Physical therapiesor Achilles tendinopathy systematic reviewand meta-analysis J Foot Ankle Res 2012515httpdxdoiorg1011861757-1146-5-15

93 Tanaka S Petersen M Cameron L Prevalenceand risk actors o tendinitis and related disor-ders o the distal upper extremity among USworkers comparison to carpal tunnel syndrome Am J Ind Med 200139328-335 httpdxdoiorg1010021097-0274(200103)393lt328AID-AJIM1021gt30CO2-I

94 Tot AD Jensen LB Bruunsgaard H et al Cy-tokine response to eccentric exercise in youngand elderly humans Am J Physiol Cell Physiol2002283C289-C295 httpdxdoiorg101152ajpcell005832001

95 Visnes H Hoksrud A Cook J Bahr R No effecto eccentric training on jumperrsquos knee in vol-leyball players during the competitive season

a randomized clinical trial Clin J Sport Med200515227-234

96 Wang JH Mechanobiology o tendon J Bio-

mech 2006391563-1582 httpdxdoiorg101016jjbiomech200505011

97 Webb K Hitchcock RW Smeal RM Li W GraySD Tresco PA Cyclic strain increases fibroblastprolieration matrix accumulation and elasticmodulus o fibroblast-seeded polyurethane con-structs J Biomech 2006391136-1144 httpdxdoiorg101016jjbiomech200408026

98 Woo SL Ritter MA Amiel D et al The bio-mechanical and biochemical propertieso swine tendons mdash long term effects o

63 Magnusson SP Langberg H Kjaer M The patho-genesis o tendinopathy balancing the responseto loading Nat Rev Rheumatol 20106262-268httpdxdoiorg101038nrrheum201043

64 Malliaras P Barton CJ Reeves ND Langberg

H Achilles and patellar tendinopathy loadingprogrammes a systematic review comparingclinical outcomes and identiying potentialmechanisms or effectiveness Sports Med201343267-286 httpdxdoiorg101007s40279-013-0019-z

65 Miller BF Olesen JL Hansen M et al Coordi-nated collagen and muscle protein synthesis inhuman patella tendon and quadriceps muscleater exercise J Physiol 20055671021-1033httpdxdoiorg101113jphysiol2005093690

66 Moerch L Pingel J Boesen M Kjaer M Lang-berg H The effect o acute exercise on collagenturnover in human tendons influence o priorimmobilization period Eur J Appl Physiol

2013113449-455 httpdxdoiorg101007s00421-012-2450-5

67 Niesen-Vertommen SL Taunton JE Clem-ent DB Mosher RE The effect o ec-centric versus concentric exercise in themanagement o Achilles tendonitis Clin J

Sport Med 19922109-113 httpdxdoiorg10109700042752-199204000-00006

68 Nirmalanandhan VS Shearn JT Juncosa-MelvinN et al Improving linear stiffness o the cell-seeded collagen sponge constructs by varyingthe components o the mechanical stimulusTissue Eng Part A 2008141883-1891 httpdxdoiorg101089tentea20070125

69 Noslashrregaard J Larsen CC Bieler T Lang-

berg H Eccentric exercise in treatment oAchilles tendinopathy Scand J Med Sci

Sports 200717133-138 httpdxdoiorg101111j1600-0838200600545x

70 Oumlhberg L Alredson H Effects on neovasculari-sation behind the good results with eccentrictraining in chronic mid-portion Achilles tendi-nosis Knee Surg Sports Traumatol Arthrosc200412465-470 httpdxdoiorg101007s00167-004-0494-8

71 Oumlhberg L Lorentzon R Alredson H Eccen-tric training in patients with chronic Achillestendinosis normalised tendon structure anddecreased thickness at ollow up Br J Sports

Med 2004388-11 discussion 11 httpdxdoi

org101136bjsm2001000284 72 Parent G Huppeacute N Langelier E Low stress

tendon atigue is a relatively rapid process inthe context o overuse injuries Ann Biomed Eng 2011391535-1545 httpdxdoiorg101007s10439-011-0254-0

73 Paulsen G Mikkelsen UR Raastad T PeakeJM Leucocytes cytokines and satellite cellswhat role do they play in muscle damage andregeneration ollowing eccentric exercise Exerc

Immunol Rev 20121842-97 74 Pearson SJ Burgess K Onambele GN Creep

and the in vivo assessment o human patellartendon mechanical properties Clin Biomech

(Bristol Avon) 200722712-717 httpdxdoiorg101016jclinbiomech200702006

75 Pedersen BK Steensberg A Fischer C et alSearching or the exercise actor is IL-6 a candi-date J Muscle Res Cell Motil 200324113-119

76 Petersen W Welp R Rosenbaum D ChronicAchilles tendinopathy a prospective ran-domized study comparing the therapeuticeffect o eccentric training the AirHeel braceand a combination o both Am J Sports

Med 2007351659-1667 httpdxdoiorg1011770363546507303558

77 Pingel J Fredberg U Mikkelsen LR et al No in-flammatory gene-expression response to acuteexercise in human Achilles tendinopathy Eur J

Appl Physiol 20131132101-2109 httpdxdoiorg101007s00421-013-2638-3

78 Purdam CR Jonsson P Alredson H LorentzonR Cook JL Khan KM A pilot study o the eccen-tric decline squat in the management o painul

chronic patellar tendinopathy Br J Sports Med200438395-397 httpdxdoiorg101136bjsm2003000053

79 Rees JD Lichtwark GA Wolman RL Wilson AMThe mechanism or efficacy o eccentric loading inAchilles tendon injury an in vivo study in humansRheumatology (Oxford) 2008471493-1497httpdxdoiorg101093rheumatologyken262

80 Rees JD Stride M Scott A Tendons ndash timeto revisit inflammation Br J Sports Med2014481553-1557 httpdxdoiorg101136bjsports-2012-091957

81 Roche AJ Calder JD Achilles tendinopathy areview o the current concepts o treatmentBone Joint J 201395-B1299-1307 http

dxdoiorg1013020301-620X95B1031881 82 Rompe JD Nae B Furia JP Maffulli N Eccentr ic

loading shock-wave treatment or a wait-and-see policy or tendinopathy o the main body otendo Achillis a randomized controlled trial Am

J Sports Med 200735374-383 httpdxdoiorg1011770363546506295940

83 Roos EM Engstroumlm M Lagerquist A Soumlder-berg B Clinical improvement ater 6 weekso eccentric exercise in patients with mid-portion Achilles tendinopathy ndash a random-ized trial with 1-year ollow-up Scand J Med

Sci Sports 200414286-295 httpdxdoiorg101111j1600-08382004378x

84 Semmler JG Tucker KJ Allen TJ Proske U

Eccentric exercise increases EMG amplitudeand orce fluctuations during submaximalcontractions o elbow flexor muscles J Appl

Physiol (1985) 2007103979-989 httpdxdoiorg101152japplphysiol013102006

85 Seynnes OR Erskine RM Maganaris CN etal Training-induced changes in structuraland mechanical properties o the patellartendon are related to muscle hypertrophy butnot to strength gains J Appl Physiol (1985)2009107523-530 httpdxdoiorg101152japplphysiol002132009

86 Shalabi A Kristoffersen-Wilberg M SvenssonL Aspelin P Movin T Eccentric training o the

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1212

amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587

Page 12: 45-11 Couppe 2

8202019 45-11 Couppe 2

httpslidepdfcomreaderfull45-11-couppe-2 1212

amp | | | | 863

MORE INFORMATION

WWWJOSPTORG

exercise on the digital extensors Connect

Tissue Res 19807177-183 httpdxdoi

org10310903008208009152109

99 Yamamoto E Hayashi K Yamamoto N Mechani-

cal properties o collagen ascicles rom stress-

shielded patellar tendons in the rabbit Clin

Biomech (Bristol Avon) 199914418-425

100 Yamamoto E Kogawa D Tokura S Hayashi K

Effects o the requency and duration o cyclic

stress on the mechanical properties o cultured

collagen ascicles rom the rabbit patellar ten-

don J Biomech Eng 20051271168-1175

101 Yang G Craword RC Wang JH Prolieration

and collagen production o human patellar

tendon fibroblasts in response to cyclic uniaxial

stretching in serum-ree conditions J Biomech

2004371543-1550 httpdxdoiorg101016j

jbiomech200401005 102 Yelland MJ Sweeting KR Lytogt JA Ng SK

Scuffham PA Evans KA Prolotherapy injections

and eccentric loading exercises or painul

Achilles tendinosis a randomised trial Br J

Sports Med 201145421-428 httpdxdoi

org101136bjsm2009057968

103 Young MA Cook JL Purdam CR Kiss ZS

Alredson H Eccentric decline squat protocol

offers superior results at 12 months compared

with traditional eccentric protocol or patel-

lar tendinopathy in volleyball players Br J

Sports Med 200539102-105 httpdxdoi

org101136bjsm2003010587