Couppé 2015 - Eccentric or Concentric Exercises For The Treatment of Tendinopathies
Couppé 2015 - Eccentric or Concentric Exercises For The Treatment of Tendinopathies
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
Downloaded from www.jospt.org at UNIVERSIDADE FEDERAL DE SO CARLOS on November 5, 2015. For personal use only. No other uses without permission.
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
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: [email protected] t Copyright ©2015 Journal of Orthopaedic & Sports Physical Therapy®
journal of orthopaedic & sports physical therapy | volume 45 | number 11 | november 2015 | 853
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
culture stimulation vary greatly, and it is storing energy deposits. However, the an- 1.3
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- Length/Mean Length (mm)
ing at 55% MVC, which causes approxi- out recovery periods.4,67,89 Overall, there
mately 3% tendon strain.5 is a lack of studies specifically addressing FIGURE 2. Achilles tendon force versus Achilles
Speed and/or duration of loading dur- the effects of recovery and how it affects tendon length. Eccentric data are shown as open
circles, whereas concentric data are filled circles.
ing exercise also appear to be important tendon adaptation.
Reprinted with permission from Chaudhry S,
for tendon adaptation.6,41,51,56 At the cellu- The majority of the tendon is com- Morrissey D, Woledge RC, Bader DL, Screen HR.
lar level, most,30,41,97 but not all,21 studies posed of extracellular matrix (ECM), Eccentric and concentric loading of the triceps
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
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
journal of orthopaedic & sports physical therapy | volume 45 | number 11 | november 2015 | 855
TABLE 1
would suggest a potential for greater me- for Achilles Tendinopathy
chanical stimulation from eccentric than
from concentric exercise.18,37 According- Study/Group Load* Pain Improvement†
ly, it has been suggested that the tendon Alfredson et al4
may stretch more during eccentric load- Isolated ECC 1260 (100%)‡§ VAS, 94%
ing than concentric loading.1,90 However,
Croisier et al13
while there is a potential for greater ten-
Isolated ECC 135 (130%)‖ VAS, 73% (10 wk)
don load and, consequently, stretch with
eccentric exercise, this potential is rarely Alfredson and Lorentzon3
utilized because rehabilitation exercises Isolated ECC 1260 (100%)‡§ VAS, 75%
seldom approach concentric 1-repeti- Öhberg and Alfredson70
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®
856 | november 2015 | volume 45 | number 11 | journal of orthopaedic & sports physical therapy
TABLE 1
for Achilles Tendinopathy (continued) concentric exercises.
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-
journal of orthopaedic & sports physical therapy | volume 45 | number 11 | november 2015 | 857
TABLE 2
izontal to avoid compression of the distal for Patellar Tendinopathy
end of the tendon against the posterior
aspect of the calcaneus.40 Study/Group Load* Pain Improvement†
Several studies have compared Bahr et al8
isolated eccentric loading with body Isolated ECC 630 (100%)‡§ VISA-P, 73%
weight to other types of nonloading
Croisier et al13
therapy (eg, prolotherapy, cryotherapy,
Isolated ECC 135 (130%)‖ VAS, 71%
splints).16,76,83,102 Most of these studies
report significant clinical improvements Purdam et al78
with eccentric exercise,16,76,83,102 although Isolated ECC 630 (100%)‡§ VAS, 62%
the effect relative to the alternative treat- Stasinopoulos and Stasinopoulos91
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®
858 | november 2015 | volume 45 | number 11 | journal of orthopaedic & sports physical therapy
TABLE 2
for Patellar Tendinopathy (continued) and firm conclusion.
Other studies have compared load-
Study/Group Load* Pain Improvement† ing regimes without matching the load
Kongsgaard et al 49 (TABLE 2). Isolated eccentric squats on a
decline board have been compared to
Isolated ECC 630 (100%)‡ VISA-P, 42%
mixed concentric/eccentric squats on
Heavy slow resistance (ECC + CON) 288 (130%) ‡
VISA-P, 39%
a flat surface in elite volleyball players:
Kongsgaard et al50 both groups performed exercises on only
No ECC ... ... the affected extremity for 12 weeks be-
Heavy slow resistance (ECC + CON) 288 (130%)‡ VISA-P, 27% fore starting the competitive season.103
Frohm et al26 Both protocols resulted in reduced pain
and increased function, without a differ-
Isolated ECC 315 (100%)‡§ VISA-P, 108%
ence between the groups. Twelve weeks
Isolated ECC overload 32 (170%) ‡‖
VISA-P, 76%
of isolated heavy eccentric training using
Cannell et al10 few repetitions of high load (100% MVC,
ECC drop squats 300 (60%)‡§ VAS, 55% approximately 170% body weight) has
Mixed ECC + CON, focused on CON 150 (CON, 125%)§‖ VAS, 31% been compared with isolated eccentric
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
journal of orthopaedic & sports physical therapy | volume 45 | number 11 | november 2015 | 859
by modulation of the applied cyclic strain mag- tendinopathy: a randomised controlled trial.
moted the paradigm of eccentric loading
nitude. J Exp Biol. 2007;210:2743-2753. http:// Br J Sports Med. 2007;41:e5. http://dx.doi.
for tendinopathy. However, as outlined dx.doi.org/10.1242/jeb.003814 org/10.1136/bjsm.2006.032532
in this review, there is little evidence for 6. Arampatzis A, Peper A, Bierbaum S, Al- 17. Dideriksen K. Muscle and tendon connective tis-
isolating the eccentric component of a bracht K. Plasticity of human Achilles tendon sue adaptation to unloading, exercise and NSAID.
mechanical and morphological properties Connect Tissue Res. 2014;55:61-70. http://dx.doi.
loading-based regime. The basic mecha-
in response to cyclic strain. J Biomech. org/10.3109/03008207.2013.862527
nisms that are likely to influence tendon 2010;43:3073-3079. http://dx.doi.org/10.1016/j. 18. Enoka RM. Eccentric contractions require
adaptations appear to be related mainly jbiomech.2010.08.014 unique activation strategies by the nervous sys-
to tendon load/strain magnitude and du- 7. Arnoczky SP, Lavagnino M, Egerbacher M. tem. J Appl Physiol (1985). 1996;81:2339-2346.
The mechanobiological aetiopathogenesis 19. Fahlström M, Jonsson P, Lorentzon R, Alfredson
ration, and there is no theoretical basis
of tendinopathy: is it the over-stimulation or H. Chronic Achilles tendon pain treated with
Journal of Orthopaedic & Sports Physical Therapy®
for greater tendon loads in eccentric ex- the under-stimulation of tendon cells? Int J eccentric calf-muscle training. Knee Surg Sports
ercises at a given force (body weight or Exp Pathol. 2007;88:217-226. http://dx.doi. Traumatol Arthrosc. 2003;11:327-333. http://
external load). org/10.1111/j.1365-2613.2007.00548.x dx.doi.org/10.1007/s00167-003-0418-z
8. Bahr R, Fossan B, Løken S, Engebretsen L. Sur- 20. Farup J, Rahbek SK, Vendelbo MH, et al. Whey
There is a paucity of clinical trials
gical treatment compared with eccentric train- protein hydrolysate augments tendon and mus-
directly comparing different exercise ing for patellar tendinopathy (jumper’s knee). cle hypertrophy independent of resistance exer-
regimes and different exercise dosages, A randomized, controlled trial. J Bone Joint cise contraction mode. Scand J Med Sci Sports.
but the available evidence provides little Surg Am. 2006;88:1689-1698. http://dx.doi. 2014;24:788-798. http://dx.doi.org/10.1111/
org/10.2106/JBJS.E.01181 sms.12083
support for the superiority of isolated
9. Beyer R, Kongsgaard M, Hougs Kjaer B, 21. Feng Z, Tateishi Y, Nomura Y, Kitajima T, Na-
eccentrics. It is worth noting that stud- Øhlenschlæger T, Kjaer M, Magnusson SP. kamura T. Construction of fibroblast–collagen
ies rarely use comparable load magni- Heavy slow resistance versus eccentric train- gels with orientated fibrils induced by static or
tude when comparing eccentric to other ing as treatment for Achilles tendinopathy: dynamic stress: toward the fabrication of small
a randomized controlled trial. Am J Sports tendon grafts. J Artif Organs. 2006;9:220-225.
load regimes. To delineate the effects of
Med. 2015;43:1704-1711. http://dx.doi. http://dx.doi.org/10.1007/s10047-006-0354-z
mode and load magnitude, future work org/10.1177/0363546515584760 22. Ferretti A. Epidemiology of jumper’s knee.
should compare isolated eccentric and 10. Cannell LJ, Taunton JE, Clement DB, Smith C, Sports Med. 1986;3:289-295.
concentric action under equal load at Khan KM. A randomised clinical trial of the effi- 23. Finni T, Komi PV, Lepola V. In vivo human triceps
cacy of drop squats or leg extension/leg curl exer- surae and quadriceps femoris muscle function
various exercise dosages in individuals
cises to treat clinically diagnosed jumper’s knee in in a squat jump and counter movement jump.
with tendinopathy. The focus on eccen- athletes: pilot study. Br J Sports Med. 2001;35:60- Eur J Appl Physiol. 2000;83:416-426. http://
tric exercise has overshadowed other as- 64. http://dx.doi.org/10.1136/bjsm.35.1.60 dx.doi.org/10.1007/s004210000289
pects of tendinopathy rehabilitation, and 11. Chaudhry S, Morrissey D, Woledge RC, Bader 24. Folkhard W, Geercken W, Knörzer E, et al.
DL, Screen HR. Eccentric and concentric loading Structural dynamic of native tendon collagen.
acknowledgement of the limited evidence
of the triceps surae: an in vivo study of dynamic J Mol Biol. 1987;193:405-407. http://dx.doi.
may prompt a broader approach, includ- muscle and tendon biomechanical parameters. org/10.1016/0022-2836(87)90228-2
ing the use of heavy load and low speed, J Appl Biomech. 2015;31:69-78. 25. Fredberg U, Stengaard-Pedersen K.
which has some support from both basic 12. Couppé C, Kongsgaard M, Aagaard P, et al. Chronic tendinopathy tissue pathology,
science and clinical trials. t Habitual loading results in tendon hyper- pain mechanisms, and etiology with a spe-
860 | november 2015 | volume 45 | number 11 | journal of orthopaedic & sports physical therapy
of isometric, lengthening, or shortening mode org/10.1002/jor.20626 J, Kjaer M. Type I collagen synthesis and deg-
resistance exercise. J Appl Physiol (1985). 42. Kalson NS, Holmes DF, Herchenhan A, Lu Y, radation in peritendinous tissue after exercise
2007;102:135-143. http://dx.doi.org/10.1152/ Starborg T, Kadler KE. Slow stretching that mim- determined by microdialysis in humans.
japplphysiol.00776.2006 ics embryonic growth rate stimulates structural J Physiol. 1999;521 pt 1:299-306. http://dx.doi.
30. Gauvin R, Parenteau-Bareil R, Larouche D, et and mechanical development of tendon-like org/10.1111/j.1469-7793.1999.00299.x
al. Dynamic mechanical stimulations induce tissue in vitro. Dev Dyn. 2011;240:2520-2528. 56. Lavagnino M, Arnoczky SP, Tian T, Vaupel Z. Ef-
anisotropy and improve the tensile properties of http://dx.doi.org/10.1002/dvdy.22760 fect of amplitude and frequency of cyclic tensile
engineered tissues produced without exogenous 43. Ker RF, Wang XT, Pike AV. Fatigue qual- strain on the inhibition of MMP-1 mRNA expres-
scaffolding. Acta Biomater. 2011;7:3294-3301. ity of mammalian tendons. J Exp Biol. sion in tendon cells: an in vitro study. Connect
http://dx.doi.org/10.1016/j.actbio.2011.05.034 2000;203:1317-1327. Tissue Res. 2003;44:181-187.
31. Giddings VL, Beaupré GS, Whalen RT, Carter DR. 44. Kettunen JA, Kvist M, Alanen E, Kujala UM. 57. Lian ØB, Engebretsen L, Bahr R. Prevalence
Calcaneal loading during walking and running. Long-term prognosis for jumper’s knee in male of jumper’s knee among elite athletes from
Journal of Orthopaedic & Sports Physical Therapy®
Med Sci Sports Exerc. 2000;32:627-634. athletes. A prospective follow-up study. Am J different sports: a cross-sectional study. Am
32. Glazebrook MA, Wright JR, Jr., Langman M, Sports Med. 2002;30:689-692. J Sports Med. 2005;33:561-567. http://dx.doi.
Stanish WD, Lee JM. Histological analysis of 45. Khan K, Cook J. The painful nonruptured org/10.1177/0363546504270454
Achilles tendons in an overuse rat model. J tendon: clinical aspects. Clin Sports Med. 58. Lopes AD, Hespanhol Junior LC, Yeung SS,
Orthop Res. 2008;26:840-846. http://dx.doi. 2003;22:711-725. Costa LO. What are the main running-related
org/10.1002/jor.20546 46. Khan KM, Cook JL, Kannus P, Maffulli N, Bonar musculoskeletal injuries? A systematic review.
33. Heinemeier KM, Olesen JL, Haddad F, et al. SF. Time to abandon the “tendinitis” myth. BMJ. Sports Med. 2012;42:891-905. http://dx.doi.
Expression of collagen and related growth 2002;324:626-627. http://dx.doi.org/10.1136/ org/10.1007/BF03262301
factors in rat tendon and skeletal muscle in re- bmj.324.7338.626 59. Maeda E, Shelton JC, Bader DL, Lee DA. Time
sponse to specific contraction types. J Physiol. 47. Kingma JJ, de Knikker R, Wittink HM, Takken dependence of cyclic tensile strain on collagen
2007;582:1303-1316. http://dx.doi.org/10.1113/ T. Eccentric overload training in patients with production in tendon fascicles. Biochem Bio-
jphysiol.2007.127639 chronic Achilles tendinopathy: a systematic re- phys Res Commun. 2007;362:399-404. http://
34. Heinemeier KM, Schjerling P, Heinemeier J, view. Br J Sports Med. 2007;41:e3. http://dx.doi. dx.doi.org/10.1016/j.bbrc.2007.08.029
Magnusson SP, Kjaer M. Lack of tissue renewal org/10.1136/bjsm.2006.030916 60. Maffulli N, Khan KM, Puddu G. Overuse tendon
in human adult Achilles tendon is revealed by 48. Kjaer M. Role of extracellular matrix in adapta- conditions: time to change a confusing termi-
nuclear bomb 13C. FASEB J. 2013;27:2074-2079. tion of tendon and skeletal muscle to mechani- nology. Arthroscopy. 1998;14:840-843. http://
http://dx.doi.org/10.1096/fj.12-225599 cal loading. Physiol Rev. 2004;84:649-698. dx.doi.org/10.1016/S0749-8063(98)70021-0
35. Heinemeier KM, Skovgaard D, Bayer ML, et al. http://dx.doi.org/10.1152/physrev.00031.2003 61. Mafi N, Lorentzon R, Alfredson H. Superior
Uphill running improves rat Achilles tendon tis- 49. Kongsgaard M, Kovanen V, Aagaard P, et al. short-term results with eccentric calf muscle
sue mechanical properties and alters gene ex- Corticosteroid injections, eccentric decline training compared to concentric training in a
pression without inducing pathological changes. squat training and heavy slow resistance randomized prospective multicenter study on
J Appl Physiol (1985). 2012;113:827-836. http:// training in patellar tendinopathy. Scand J Med patients with chronic Achilles tendinosis. Knee
dx.doi.org/10.1152/japplphysiol.00401.2012 Sci Sports. 2009;19:790-802. http://dx.doi. Surg Sports Traumatol Arthrosc. 2001;9:42-47.
36. Henriksen M, Aaboe J, Bliddal H, Langberg org/10.1111/j.1600-0838.2009.00949.x http://dx.doi.org/10.1007/s001670000148
H. Biomechanical characteristics of the ec- 50. Kongsgaard M, Qvortrup K, Larsen J, et al. 62. Magnusson SP, Aagaard P, Dyhre-Poulsen P,
centric Achilles tendon exercise. J Biomech. Fibril morphology and tendon mechanical Kjaer M. Load-displacement properties of
2009;42:2702-2707. http://dx.doi.org/10.1016/j. properties in patellar tendinopathy: effects the human triceps surae aponeurosis in vivo.
jbiomech.2009.08.009 of heavy slow resistance training. Am J J Physiol. 2001;531:277-288. http://dx.doi.
37. Hill AV. The heat of shortening and the dynamic Sports Med. 2010;38:749-756. http://dx.doi. org/10.1111/j.1469-7793.2001.0277j.x
journal of orthopaedic & sports physical therapy | volume 45 | number 11 | november 2015 | 861
to loading. Nat Rev Rheumatol. 2010;6:262-268. 75. Pedersen BK, Steensberg A, Fischer C, et al. volume and intratendinous signal as evaluated
http://dx.doi.org/10.1038/nrrheum.2010.43 Searching for the exercise factor: is IL-6 a candi- by MRI. Am J Sports Med. 2004;32:1286-1296.
64. Malliaras P, Barton CJ, Reeves ND, Langberg date? J Muscle Res Cell Motil. 2003;24:113-119. http://dx.doi.org/10.1177/0363546504263148
H. Achilles and patellar tendinopathy loading 76. Petersen W, Welp R, Rosenbaum D. Chronic 87. Shepherd JH, Screen HR. Fatigue loading of ten-
programmes: a systematic review comparing Achilles tendinopathy: a prospective ran- don. Int J Exp Pathol. 2013;94:260-270. http://
clinical outcomes and identifying potential domized study comparing the therapeutic dx.doi.org/10.1111/iep.12037
mechanisms for effectiveness. Sports Med. effect of eccentric training, the AirHeel brace, 88. Silbernagel KG, Thomeé R, Eriksson BI,
2013;43:267-286. http://dx.doi.org/10.1007/ and a combination of both. Am J Sports Karlsson J. Continued sports activity, using
s40279-013-0019-z Med. 2007;35:1659-1667. http://dx.doi. a pain-monitoring model, during rehabilita-
65. Miller BF, Olesen JL, Hansen M, et al. Coordi- org/10.1177/0363546507303558 tion in patients with Achilles tendinopathy:
nated collagen and muscle protein synthesis in 77. Pingel J, Fredberg U, Mikkelsen LR, et al. No in- a randomized controlled study. Am J Sports
human patella tendon and quadriceps muscle flammatory gene-expression response to acute Med. 2007;35:897-906. http://dx.doi.
after exercise. J Physiol. 2005;567:1021-1033. exercise in human Achilles tendinopathy. Eur J org/10.1177/0363546506298279
http://dx.doi.org/10.1113/jphysiol.2005.093690 Appl Physiol. 2013;113:2101-2109. http://dx.doi. 89. Silbernagel KG, Thomeé R, Thomeé P, Karls-
66. Moerch L, Pingel J, Boesen M, Kjaer M, Lang- org/10.1007/s00421-013-2638-3 son J. Eccentric overload training for patients
berg H. The effect of acute exercise on collagen 78. Purdam CR, Jonsson P, Alfredson H, Lorentzon with chronic Achilles tendon pain – a ran-
turnover in human tendons: influence of prior R, Cook JL, Khan KM. A pilot study of the eccen- domised controlled study with reliability test-
immobilization period. Eur J Appl Physiol. tric decline squat in the management of painful ing of the evaluation methods. Scand J Med
2013;113:449-455. http://dx.doi.org/10.1007/ chronic patellar tendinopathy. Br J Sports Med. Sci Sports. 2001;11:197-206. http://dx.doi.
s00421-012-2450-5 2004;38:395-397. http://dx.doi.org/10.1136/ org/10.1034/j.1600-0838.2001.110402.x
67. Niesen-Vertommen SL, Taunton JE, Clem- bjsm.2003.000053 90. Stanish WD, Rubinovich RM, Curwin S. Eccentric
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
ent DB, Mosher RE. The effect of ec- 79. Rees JD, Lichtwark GA, Wolman RL, Wilson AM. exercise in chronic tendinitis. Clin Orthop Relat
centric versus concentric exercise in the The mechanism for efficacy of eccentric loading in Res. 1986:65-68.
management of Achilles tendonitis. Clin J Achilles tendon injury; an in vivo study in humans. 91. Stasinopoulos D, Stasinopoulos I. Comparison
Sport Med. 1992;2:109-113. http://dx.doi. Rheumatology (Oxford). 2008;47:1493-1497. of effects of exercise programme, pulsed ultra-
org/10.1097/00042752-199204000-00006 http://dx.doi.org/10.1093/rheumatology/ken262 sound and transverse friction in the treatment
68. Nirmalanandhan VS, Shearn JT, Juncosa-Melvin 80. Rees JD, Stride M, Scott A. Tendons – time of chronic patellar tendinopathy. Clin Rehabil.
N, et al. Improving linear stiffness of the cell- to revisit inflammation. Br J Sports Med. 2004;18:347-352.
seeded collagen sponge constructs by varying 2014;48:1553-1557. http://dx.doi.org/10.1136/ 92. Sussmilch-Leitch SP, Collins NJ, Bialocerkowski
the components of the mechanical stimulus. bjsports-2012-091957 AE, Warden SJ, Crossley KM. Physical therapies
Tissue Eng Part A. 2008;14:1883-1891. http:// 81. Roche AJ, Calder JD. Achilles tendinopathy: a for Achilles tendinopathy: systematic review
dx.doi.org/10.1089/ten.tea.2007.0125 review of the current concepts of treatment. and meta-analysis. J Foot Ankle Res. 2012;5:15.
69. Nørregaard J, Larsen CC, Bieler T, Lang- Bone Joint J. 2013;95-B:1299-1307. http:// http://dx.doi.org/10.1186/1757-1146-5-15
Journal of Orthopaedic & Sports Physical Therapy®
berg H. Eccentric exercise in treatment of dx.doi.org/10.1302/0301-620X.95B10.31881 93. Tanaka S, Petersen M, Cameron L. Prevalence
Achilles tendinopathy. Scand J Med Sci 82. Rompe JD, Nafe B, Furia JP, Maffulli N. Eccentric and risk factors of tendinitis and related disor-
Sports. 2007;17:133-138. http://dx.doi. loading, shock-wave treatment, or a wait-and- ders of the distal upper extremity among U.S.
org/10.1111/j.1600-0838.2006.00545.x see policy for tendinopathy of the main body of workers: comparison to carpal tunnel syndrome.
70. Öhberg L, Alfredson H. Effects on neovasculari- tendo Achillis: a randomized controlled trial. Am Am J Ind Med. 2001;39:328-335. http://dx.doi.
sation behind the good results with eccentric J Sports Med. 2007;35:374-383. http://dx.doi. org/10.1002/1097-0274(200103)39:3<328::AID-
training in chronic mid-portion Achilles tendi- org/10.1177/0363546506295940 AJIM1021>3.0.CO;2-I
nosis? Knee Surg Sports Traumatol Arthrosc. 83. Roos EM, Engström M, Lagerquist A, Söder- 94. Toft AD, Jensen LB, Bruunsgaard H, et al. Cy-
2004;12:465-470. http://dx.doi.org/10.1007/ berg B. Clinical improvement after 6 weeks tokine response to eccentric exercise in young
s00167-004-0494-8 of eccentric exercise in patients with mid- and elderly humans. Am J Physiol Cell Physiol.
71. Öhberg L, Lorentzon R, Alfredson H. Eccen- portion Achilles tendinopathy – a random- 2002;283:C289-C295. http://dx.doi.org/10.1152/
tric training in patients with chronic Achilles ized trial with 1-year follow-up. Scand J Med ajpcell.00583.2001
tendinosis: normalised tendon structure and Sci Sports. 2004;14:286-295. http://dx.doi. 95. Visnes H, Hoksrud A, Cook J, Bahr R. No effect
decreased thickness at follow up. Br J Sports org/10.1111/j.1600-0838.2004.378.x of eccentric training on jumper’s knee in vol-
Med. 2004;38:8-11; discussion 11. http://dx.doi. 84. Semmler JG, Tucker KJ, Allen TJ, Proske U. leyball players during the competitive season:
org/10.1136/bjsm.2001.000284 Eccentric exercise increases EMG amplitude a randomized clinical trial. Clin J Sport Med.
72. Parent G, Huppé N, Langelier E. Low stress and force fluctuations during submaximal 2005;15:227-234.
tendon fatigue is a relatively rapid process in contractions of elbow flexor muscles. J Appl 96. Wang JH. Mechanobiology of tendon. J Bio-
the context of overuse injuries. Ann Biomed Eng. Physiol (1985). 2007;103:979-989. http://dx.doi. mech. 2006;39:1563-1582. http://dx.doi.
2011;39:1535-1545. http://dx.doi.org/10.1007/ org/10.1152/japplphysiol.01310.2006 org/10.1016/j.jbiomech.2005.05.011
s10439-011-0254-0 85. Seynnes OR, Erskine RM, Maganaris CN, et 97. Webb K, Hitchcock RW, Smeal RM, Li W, Gray
73. Paulsen G, Mikkelsen UR, Raastad T, Peake al. Training-induced changes in structural SD, Tresco PA. Cyclic strain increases fibroblast
JM. Leucocytes, cytokines and satellite cells: and mechanical properties of the patellar proliferation, matrix accumulation, and elastic
what role do they play in muscle damage and tendon are related to muscle hypertrophy but modulus of fibroblast-seeded polyurethane con-
regeneration following eccentric exercise? Exerc not to strength gains. J Appl Physiol (1985). structs. J Biomech. 2006;39:1136-1144. http://
Immunol Rev. 2012;18:42-97. 2009;107:523-530. http://dx.doi.org/10.1152/ dx.doi.org/10.1016/j.jbiomech.2004.08.026
74. Pearson SJ, Burgess K, Onambele GN. Creep japplphysiol.00213.2009 98. Woo SL, Ritter MA, Amiel D, et al. The bio-
and the in vivo assessment of human patellar 86. Shalabi A, Kristoffersen-Wilberg M, Svensson mechanical and biochemical properties
tendon mechanical properties. Clin Biomech L, Aspelin P, Movin T. Eccentric training of the of swine tendons — long term effects of
862 | november 2015 | volume 45 | number 11 | journal of orthopaedic & sports physical therapy
Tissue Res. 1980;7:177-183. http://dx.doi. and collagen production of human patellar Alfredson H. Eccentric decline squat protocol
org/10.3109/03008208009152109 tendon fibroblasts in response to cyclic uniaxial offers superior results at 12 months compared
99. Yamamoto E, Hayashi K, Yamamoto N. Mechani- stretching in serum-free conditions. J Biomech. with traditional eccentric protocol for patel-
cal properties of collagen fascicles from stress- 2004;37:1543-1550. http://dx.doi.org/10.1016/j. lar tendinopathy in volleyball players. Br J
shielded patellar tendons in the rabbit. Clin jbiomech.2004.01.005 Sports Med. 2005;39:102-105. http://dx.doi.
Biomech (Bristol, Avon). 1999;14:418-425. 102. Yelland MJ, Sweeting KR, Lyftogt JA, Ng SK, org/10.1136/bjsm.2003.010587
100. Yamamoto E, Kogawa D, Tokura S, Hayashi K. Scuffham PA, Evans KA. Prolotherapy injections
Effects of the frequency and duration of cyclic and eccentric loading exercises for painful
@
stress on the mechanical properties of cultured Achilles tendinosis: a randomised trial. Br J
collagen fascicles from the rabbit patellar ten- Sports Med. 2011;45:421-428. http://dx.doi.
MORE INFORMATION
don. J Biomech Eng. 2005;127:1168-1175. org/10.1136/bjsm.2009.057968 WWW.JOSPT.ORG
Copyright © 2015 Journal of Orthopaedic & Sports Physical Therapy®. All rights reserved.
journal of orthopaedic & sports physical therapy | volume 45 | number 11 | november 2015 | 863