Professional Documents
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CHRISTIAN COUPPÉ, PT, PhD1-4 • RENÉ B. SVENSSON, PhD1-3 • KARIN GRÄVARE SILBERNAGEL, PT, ATC, PhD5
HENNING LANGBERG, PT, PhD, DSc6 • S. PETER MAGNUSSON, PT, DSc1-4
T
endon tissue plays an essential role in transmitting muscle Tendinopathy is the commonly ac-
contractile forces to produce movement and is therefore cepted term for the clinical condition in
Downloaded from www.jospt.org at on December 16, 2019. For personal use only. No other uses without permission.
uniquely designed to withstand considerable loads. During and around overloaded tendons.46 These
injuries were previously considered to be
locomotion, the Achilles and patellar tendons may see forces
the result of a prolonged inflammatory
up to approximately 8 times body weight.23,31,62 Repetitive loading of condition (chronic tendinitis).90 How-
a tendon often results in overuse injuries, including tendinopathy, ever, more recently, the extent to which
which is a clinical condition characterized by pain in the area of the inflammation plays a role in chronic ten-
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
injuries to elite endurance runners, and tendinopathy and thus provide the basis Notwithstanding these limitations, it has
6% of sedentary people will at some point for prevention of overuse injuries. been shown that tendon tissue from in-
dividuals with Achilles tendinopathy
TTSYNOPSIS: Tendinopathy is a very common
does not display an elevated expression
variation and sometimes insufficient reporting of
disorder in both recreational and elite athletes. the details of treatment protocols may hamper the of inflammatory markers after 1 hour of
Many individuals have recurrent symptoms that interpretation of what may be the optimal exercise running.77 Rather than inflamed, tendon
lead to chronic conditions and termination of regime with respect to parameters such as load tissue obtained from individuals with ten-
sports activity. Exercise has become a popular magnitude, speed of movement, and recovery dinopathy is typically more cellular than
and somewhat efficacious treatment regime, and period between exercise sessions. Future studies healthy tissue and displays both signs of
isolated eccentric exercise has been particularly should control for these loading parameters, general tissue degeneration, including
promoted. In this clinical commentary, we review evaluate various exercise dosages, and think
the relevant evidence for different exercise regimes collagen degeneration and necrosis, as
beyond isolated eccentric exercises to arrive at
in tendinopathy rehabilitation, with particular focus well as signs of regeneration, including
firm recommendations regarding rehabilitation of
on the applied loads that are experienced by the neovascularization, irregular fiber struc-
individuals with tendinopathies. J Orthop Sports
tendon and how the exercise regime may affect ture, and increased ground substance
Phys Ther 2015;45(11):853-863. Epub 14 Oct 2015.
these applied loads. There is no convincing clinical (see Fredberg and Stengaard-Pedersen25).
doi:10.2519/jospt.2015.5910
evidence to demonstrate that isolated eccentric
TTKEY WORDS: Achilles, forces, load, patellar,
Tendinopathy is a substantial clinical
loading exercise improves clinical outcomes more
than other loading therapies. However, the great recovery, tendon challenge because it can severely limit
sports participation for months and po-
1
Institute of Sports Medicine Copenhagen, Bispebjerg Hospital, Copenhagen, Denmark. 2Department of Orthopaedic Surgery, Bispebjerg Hospital, Copenhagen, Denmark. 3Center
for Healthy Aging, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark. 4Musculoskeletal Rehabilitation Research Unit, Department of
Physical Therapy, Bispebjerg Hospital, Copenhagen, Denmark. 5Department of Physical Therapy, University of Delaware, Newark, DE. 6CopenRehab, Department of Public Health,
University of Copenhagen, Copenhagen, Denmark. The authors certify that they have no affiliations with or financial involvement in any organization or entity with a direct financial
interest in the subject matter or materials discussed in the article. Address correspondence to Dr S. Peter Magnusson, Institute of Sports Medicine Copenhagen, Bispebjerg
Hospital, Bispebjerg Bakke 23, 2400 Copenhagen NV, Denmark. E-mail: p.magnusson@sund.ku.dk t Copyright ©2015 Journal of Orthopaedic & Sports Physical Therapy®
FIGURE 1. Schematic illustration of concentric and eccentric muscle contraction about the ankle joint. Numbers illustrate lengths (not to scale). (A) During concentric heel
rise, the tendon and muscle are initially relaxed. (B) As muscle shortens, force is generated, causing the tendon to lengthen until sufficient force has been reached and the heel
begins to rise. (C) While muscle shortens further, the heel continues to rise under approximately constant force and, due to the constant load, the length of tendon also remains
constant. (D) In the eccentric phase, the heel drops as muscle lengthens, still at approximately constant force, and consequently tendon retains its length. (E) Finally, the
muscle lengthens as it is relaxed and tendon shortens because load is removed. Note that across the schematics, tendon length is determined by the amount of load carried
independent of muscle length.
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
tentially years.4,44 The list of currently The progression of the exercise protocol, properties.12,85,98 The magnitude and type
available interventions for this clinical with abating symptoms, was described of adaptation likely depend on the ex-
condition is extensive and may include as increasing the speed of the movement, ercise regime, including the magnitude
surgery, nonsteroidal anti-inflammatory and thereafter an external load was add- of the load, range of motion performed,
drugs, corticosteroids, sclerosing injec- ed for additional progression.90 contraction mode (eccentric lengthening/
tion, shockwave therapy, platelet-rich Approximately a decade later, it was concentric shortening), movement speed,
plasma injection, intratendinous hyper- suggested that isolated eccentric contrac- number of repetitions, and rest periods
osmolar dextrose (prolotherapy) injec- tion alone, without the accompanying between the exercise sessions. By varying
Journal of Orthopaedic & Sports Physical Therapy®
tion, high-volume injections of 10 mL concentric component of a stretch-short- these components, a wide range of exer-
0.5% bupivacaine and 40 mL normal ening cycle, provided good clinical results cise programs can be constructed, from
saline into the paratenon, Kinesio Tape, for patients with tendinopathy.4 This endurance (low load, high speed, many
and therapeutic ultrasound, just to men- isolated eccentric loading paradigm has repetitions) to strength (high load, low
tion a few.81,92 Although these and other since gained considerable popularity and speed, few repetitions) programs, with
treatment options are described in the is now widely regarded as the treatment myriad combinations in between. The
literature, various loading interventions of choice, although there is a lack of con- response of tendon to the various exer-
have predominated in the treatment of vincing evidence that it is the most effec- cise parameters will be discussed in the
tendinopathies.64 It seems that loading tive exercise regime.64 More recently, new following sections, though knowledge on
paradigms yield positive clinical,2,61,88 loading-based exercise regimes, such as several matters remains limited.
structural,50 and biochemical outcomes.49 isolated concentric training,61 heavy slow It is well known that the tendon cells
Much of the attention on loading pro- resistance training,9,49 and concentric/ (fibroblasts) respond to mechanical stim-
grams as a treatment paradigm for these eccentric progressing to eccentric train- uli in the form of strain,42,66,96 and that
challenging injuries originated from an ing,88,89 have emerged. This article focus- depriving them of strain (relative tissue
article published by Stanish et al90 in es on the underlying rationale of these deformation) leads to degeneration and
1986. In this article, the loading regime various loading paradigms. apoptosis (cell death).7,17,99 However, the
was described as a stretch-shortening dose response to strain magnitude is still
exercise, that is, an eccentric component Response of Healthy Tendon to Load not well established. Cell-culture experi-
rapidly followed by a concentric com- It is well established that exercise in gen- ments suggest that there is an increased
ponent. For example, in the case of the eral can affect both skeletal muscle38 and response (increased collagen expression,
patellar tendon, “The patient, from a tendon.48 In tendon, there is an acute reduced matrix metalloproteinase ex-
standing position, flexes the knees and increase in blood flow and collagen syn- pression, and increased matrix stiffness)
drops to a squatting position abruptly, thesis,54,55 and long-term effects lead to with increased strain,56,101 but there may
then recoils to the standing position.”90 tissue hypertrophy and altered material be an optimal strain, beyond which the
854 | november 2015 | volume 45 | number 11 | journal of orthopaedic & sports physical therapy
uncertain how much of a given strain the abolic response to loading is sustained in
1.2
cells will experience in vivo, because the tendon for up to several days following an
Force/Mean Force
surrounding matrix may provide shield- exercise bout,55,65 which could indicate the 1.1
ing. In vivo, in healthy human Achilles need for a postexercise recovery period.63 1.0
tendons, it has been reported that with But, conversely, studies on cell culture
equal exercise volume, working at 90% of have performed continuous stimulation 0.9
maximum voluntary contraction (MVC), of fibroblasts for up to 24 hours per day 0.8
which causes approximately 5% tendon without detrimental effects,41,59 and most
strain, yields increased stiffness and exercise protocols for tendinopathy man- 0.7
0.95 1.0 1.05
cross-sectional area compared to work- agement are performed every day with-
Downloaded from www.jospt.org at on December 16, 2019. For personal use only. No other uses without permission.
have found that the adaptive response of which is a passive structure and, un- surae: an in vivo study of dynamic muscle and
fibroblasts to dynamic load is superior to like the cells, does not actively respond tendon biomechanical parameters. J Appl Biomech.
2015;31:69-78. ©Human Kinetics, Inc.
that of static load (zero speed). Though to load, though it may still be differen-
the response to different dynamic load re- tially affected by exercise parameters. It
gimes is complex due to the interaction has been suggested that accumulation In summary, tendon is responsive to
of the parameters, overall, the evidence of microdamage may be involved in the loading and will respond more strongly
suggests that increased time under load, etiology of tendinopathy87 and, because to greater loads, although there is likely
increased number of load cycles, and the turnover in tendons is slow,34 ECM an optimum beyond which load becomes
increased loading rate result in a posi- damage could accumulate. Microdamage detrimental. Slower loading regimes may
Journal of Orthopaedic & Sports Physical Therapy®
tive adaptive response (increased ma- is difficult to measure, and its clinical rel- be superior to rapid loading, while the
trix strength and stiffness and decreased evance is therefore unclear. However, if it importance of recovery between loading
matrix metalloproteinase expression) in does play a role, it would be an argument sessions is unclear.
cultured fibroblasts.41,56,100 The response in favor of recovery periods. Mechanical
appears to be a bit different in vivo, where studies have shown that both overload- Tendon Under Eccentric and
it has been reported that the stiffness ing and mechanical fatigue can cause Concentric Muscle Contractions
and size (cross-sectional area) of human damage to tendon ECM,43,72 which could Although isolated eccentric loading re-
Achilles tendon were more responsive to play a role in tendinopathy. The tendon gimes for tendinopathy have been widely
a low number of loads of long duration ECM is also a viscoelastic material, which accepted as the treatment of choice,92 the
(6-second cycle) than to a high number of means that slower loading regimes can potential mechanisms behind this inter-
faster loads (2-second cycle) when the to- yield greater strains than faster loading vention remain unclear. In the following
tal exercise volume was kept constant.5,6 regimes, as the tendon has more time to section, we discuss some of the proposed
This finding is corroborated somewhat creep.74 Creep also appears to be associ- mechanisms and their potential applica-
by another study showing that isometric ated with greater relative fibril slippage,24 tions in light of existing evidence.
contractions of long duration (20 sec- which may generate local shear strains Strictly speaking, the descriptions
onds) yielded greater patellar tendon ad- sensed by the cells. Slow loading may “concentric” and “eccentric” only apply to
aptation (increased stiffness) than rapid therefore produce particularly strong cell muscle, which actively contracts. Tendon
(1-second) contractions at equal exer- stimuli that can be beneficial to the ten- is a mechanically passive structure that
cise volume.51 In the latter study, muscle don if the strain is sufficient, but could be lengthens when load increases and short-
strength and volume adaptation were un- detrimental if strain is excessive. This vis- ens when load is reduced (FIGURE 1). It is
affected by contraction duration. coelastic behavior depends on the amount therefore questionable whether the mode
It is unknown whether tendon cells of time the tendon is under load and is of muscle contraction for a given load and
experience some form of fatigue as a re- therefore unaffected by the mode of mus- range of motion would have a differen-
sult of repeated load cycles. Tendon cells cle contraction (eccentric or concentric). tial effect on tendon tissue. The fact that
tion maximum. It has been shown that Isolated ECC 1260 (100%)‡§ Pain during activity: reduced, 88%
Achilles tendon load and stretch are
Roos et al83
identical during the concentric and ec-
Isolated ECC 1260 (100%)‡§ Foot and Ankle Outcome Score, 36%
centric components of a heel rise/drop
against body weight (FIGURE 2), a typi- Shalabi et al86
cal load used in rehabilitation.11,79 The 2 Isolated ECC 1260 (100%)‡§ 6-point pain scale, 40%
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
TABLES 1 and 2 list the number of week- Isolated ECC 1890 (100%)‡§ VAS, 60%
ly repetitions and estimated loads used in Yelland et al 102
several eccentric exercise regimes pub- Isolated ECC 1260 (100%)‡§ VISA-A, 38%
Journal of Orthopaedic & Sports Physical Therapy®
VAS, 69%
tendinopathy will first cover the clinical
Mafi et al61 studies that have investigated the effects
Isolated ECC 1260 (100%)‡§ Satisfied, 82%¶ of eccentric loading, followed by studies
VAS of satisfied, 83% that have investigated the effects of other
Isolated CON plus jump plus rope skipping 1260 (100%)‡ Satisfied, 32% types of loading exercises. TABLES 1 and 2
VAS of satisfied, 86% cover the clinical studies on Achilles and
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
Abbreviations: CON, concentric; ECC, eccentric; KOOS, Knee injury Osteoarthritis Outcome Score;
VAS, visual analog scale; VISA-A, Victorian Institute of Sport Assessment-Achilles. Several studies3,13 have employed the iso-
*Load reported as weekly repetitions and estimated load as percentage of body weight (50% body lated eccentric-loading paradigm initially
weight is 2 legged and 100% is 1 legged). In general, peak load is listed, but for studies with load introduced by Alfredson et al.4 When this
progression that did not report the achieved progress, only the load before progression is listed.
No attempt was made to evaluate load in stretching exercises. exercise model is performed as unilateral
†
Unless otherwise stated, all studies had 12 weeks of intervention. heel drop, the force placed on the ten-
‡
Pain accepted. don is a function of body weight, and the
§
Study included unreported progression beyond what is listed.
‖
Estimated percent body weight from maximal voluntary contraction or other external load. force can be modulated with additional
¶
Improvement in ECC group significantly greater than in comparator. weight placed in a backpack worn by the
patient. In addition to improvements in
similar expressions of collagen.33 These that of the concentric side. The results pain and function, it appears that struc-
animal findings imply that given a suf- showed that resistance training with ei- tural features observed with ultrasound
ficiently high force (and resulting strain ther concentric or eccentric contraction and magnetic resonance imaging are al-
on the fibroblast), the contraction mode produced a similar magnitude of tendon tered following isolated eccentric loading
is inconsequential for the tendon cellu- hypertrophy.20 These findings reinforce in some,28,70,71,86 but not all, studies.14,69,76,82
lar response. A recent study examined the notion that the cellular and tissue re- It has also been shown that in addition to
the effect of contraction mode on tendon sponse in healthy tendon is independent decreasing pain, isolated eccentric load-
(and muscle) hypertrophy in healthy hu- of contraction mode. ing can result in increased synthesis of
man subjects.20 The 12-week resistance In summary, there are a number of type I collagen.53 Thus, isolated eccentric
training consisted of isolated concentric mechanisms that could theoretically loading appears to influence biochemical
knee extensions on one side and eccentric differentiate the effect of eccentric from and biomechanical parameters and im-
knee extensions on the contralateral side. concentric exercise on tendon, but there prove clinical outcomes. The beneficial
The sets, repetitions, and time of load- is no evidence that these mechanisms effects of isolated eccentric loading with
ing were similar between sides, but the actually play a role or are beneficial. In body weight appear to be reduced if the
loading for the eccentric side was 120% contrast, there is evidence from animal pain is located toward the tendon inser-
ment varies (eg, eccentric loading regimes Isolated ECC 135 (100%)‡§ 5-point scale, 80% (4 wk)
have greater effect than cryotherapy, but
Visnes et al95
similar effect compared to shockwave
Isolated ECC + competitive volleyball 630 (100%)‡§ No improvement
therapy and heel brace).92
Collectively, these studies demonstrate Competitive volleyball (control) 0 (0%) No improvement
positive clinical benefits from eccentric Young et al 103
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
loading, but because none of these studies Isolated ECC on 25° decline board 630 (100%)‡§ VISA-P, 25%
has a comparison group using an alterna- VAS, 51%
tive muscle contraction mode (concentric Isolated ECC on horizontal step 630 (100%) VISA-P, 18%
or isometric), they are unable to show VAS, 53%
whether the actual muscle contraction Jonsson and Alfredson39
mode plays a role in the outcome. Isolated ECC 630 (100%)‡§ VISA-P, 102%¶
The Effect of Eccentric Muscle Contrac- VAS, 69%¶
tion Compared to Other Contraction Isolated CON (n = 4) 630 (100%)‡§ VISA-P, –9%
Regimes for Achilles Tendinopathy A VAS, 8%
Journal of Orthopaedic & Sports Physical Therapy®
¶
Improvement in ECC group significantly greater than in comparator.
repetitions per session), with the aim of
creating a high concentric load compo-
in clinical improvement when patients thy following eccentric exercise, but has nent (75%-80% MVC).10 Both groups
were instructed to refrain from sports ac- not demonstrated significant effects.49 trained with progressive loads 5 times
tivity during the intervention period.39,91 Collectively, the above studies show that weekly and had reduced tendon pain
However, in elite volleyball players with eccentric loading may provide clinical after 12 weeks, but outcomes were no
patellar tendinopathy, adding 8 weeks of benefits in patellar tendinopathy treat- different between groups. Only 1 study
isolated eccentric loading to the already ment, but, again, whether the actual di- has investigated biochemical outcomes:
existing activity during the season did rection of muscle contraction plays a role the efficacy of isolated eccentric squats
not confer any pain relief.95 In contrast, in in the outcome or clinical benefits are in- compared to mixed concentric/eccentric
Achilles tendinopathy, it has been shown stead related to the absolute magnitude heavy slow resistance training.49 Both ex-
that moderate physical activity during of loading is unclear, as none of these ercise regimes resulted in reduced pain
the treatment period was not detrimen- studies had a similar comparison group. and improved function, but biochemical
tal to the benefits of eccentric exercise.88 The Effect of Eccentric Muscle Contraction changes (increased collagen content and
The apparent difference between activ- Compared to Other Contraction Regimes reduced glycation) were only evident with
ity at an elite level and more moderate for Patellar Tendinopathy For patellar heavy slow resistance training. In addi-
activity may be related to insufficient tendinopathy, only 1 study has compared tion, heavy slow resistance training was
recovery time or possibly the total load isolated eccentric loading with an identi- associated with structural changes.50
volume of sports activity and the added cal concentric-loading regime at equal Therefore, collectively, there is no firm
eccentric-loading exercises,63 although load magnitude, volume, and speed.39 The evidence to support the notion that ec-
this requires further investigation. Ultra- authors39 concluded that eccentric loading centric loading is more efficient than
sonography has been used to investigate was more effective in reducing pain than concentric or other loading regimes for
structural changes (tendon thickness and concentric loading; however, due to a high patellar tendinopathy. Most studies have
Doppler activity) in patellar tendinopa- number of dropouts, only 4 of 7 partici- not matched for other parameters, such
by modulation of the applied cyclic strain mag- tendinopathy: a randomised controlled trial.
moted the paradigm of eccentric loading
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