Alteracion de La Fuerza en La Tendinopatia de Aquiles

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Journal of Athletic Training 2019;54(8):889–900

doi: 10.4085/1062-6050-43-18
Ó by the National Athletic Trainers’ Association, Inc Ankle
www.natajournals.org

Altered Strength Profile in Achilles Tendinopathy: A


Systematic Review and Meta-Analysis
Seán McAuliffe, PhD, BSc*; Ariane Tabuena, BSc†; Karen McCreesh, PhD, BSc†;
Mary O’Keeffe, PhD, BSc†; John Hurley, BSc†; Tom Comyns, PhD, BSc‡;
Helen Purtill, PhD, BSc§; Seth O’Neill, PhD, BSc||; Kieran O’Sullivan, PhD, BSc*†
*Aspetar Orthopaedic and Sports Medicine Hospital, Doha, Qatar; †School of Allied Health, ‡Department of Physical
Education and Sports Science, §Department of Mathematics & Statistics, University of Limerick, Ireland; ||Department
of Medical & Social Care Education, University of Leicester, United Kingdom

Background: Persistent strength deficits secondary to Data Synthesis: A total of 19 studies were eligible. Pooled
Achilles tendinopathy (AT) have been postulated to account meta-analyses for isokinetic dynamometry demonstrated reduc-
for difficulty engaging in tendon-loading movements, such as tions in maximal strength (concentric PF peak torque [PT] slow
running and jumping, and may contribute to the increased risk of [Hedges g ¼ 0.52, 44% deficit], concentric PF PT fast [Hedges g
recurrence. To date, little consensus exists on the presence of ¼ 0.61, 38% deficit], and eccentric PF PT slow [Hedges g ¼ 0.26,
strength deficits in AT. Consequently, researchers are uncertain 18% deficit]). Reactive strength, particularly during hopping, was
about the appropriate methods of assessment that may inform also reduced (Hedges g range ¼ 0.32–2.61, 16%–35% deficit).
rehabilitation in clinical practice. For explosive strength, reductions in the rate of force develop-
Objective: To evaluate and synthesize the literature inves- ment (Hedges g range ¼ 0.31–1.73, 10%–21% deficit) were
tigating plantar-flexion (PF) strength in individuals with AT. observed, whereas the findings for ground reaction force varied
Study Selection: Two independent reviewers searched 9 but were not consistently altered.
electronic databases using an agreed-upon set of key words. Conclusions: Individuals with AT demonstrated strength
Data Extraction: Data were extracted from studies com- deficits compared with the uninjured side or with asymptomatic
paring strength measures (maximal, reactive, and explosive control participants. Deficits were reported across the strength
strength) between individuals with AT and healthy control spectrum for maximal, reactive, and explosive strength. Clini-
participants or between the injured and uninjured sides of cians and researchers may need to adapt their assessment of
people with AT. The Critical Appraisal Skills Programme Case- Achilles tendon function, which may ultimately help to optimize
Control Study Checklist was used to assess the risk of bias for rehabilitation outcomes.
the included studies. Key Words: tendon, strength spectrum, assessment

Key Points
 Traditional methods of strength assessment in patients with tendinopathy have focused on the heel-raise test.
 The heel-raise endurance test may not adequately quantify deficits across the entire strength spectrum.
 Individuals with Achilles tendinopathy displayed deficits in maximal, reactive, and explosive strength compared with
the uninjured side or asymptomatic controls.
 The current focus on maximal strength during assessments and rehabilitation, with little emphasis on explosive or
reactive strength, may not optimally match the entire strength spectrum and could explain why strengthening
exercises are only moderately effective for reducing pain and disability in patients with Achilles tendinopathy.

T
he Achilles tendon is the largest and strongest Individuals with AT often report impairments or an
tendon in the body.1,2 Despite the relative strength inability to engage in functional activities.3 One possible
of the Achilles musculotendinous unit, Achilles explanation may relate to an altered strength profile or
tendinopathy (AT) is a common musculoskeletal concern in persistent weakness due to AT.10–12 The mechanism behind
both athletes and nonathletes.3 In athletes, AT occurs most strength deficits due to AT remains unclear; however,
commonly among individuals participating in stretch- researchers have postulated that physiological alterations in
shortening–cycle (SSC) activities, such as running and the tendon, such as altered tendon mechanical properties,13
jumping.4–6 During such athletic endeavors, the Achilles pain inhibition, altered motor output,14,15 or muscle disuse
tendon is subjected to loads as high as 6 to 12 times body and atrophy,16 may result in an inability to generate or
weight (BW).7,8 The high loads placed on the Achilles tolerate the required loads.
tendon require a considerable degree of strength and power In clinical environments, the most common method of
from the plantar-flexor muscles to repeatedly generate quantifying tendon function in individuals with AT has
appropriate force and enable the tendon to store and release been the calf-raise or heel-raise test. The calf-raise test
energy for athletic movements.9 involves repetitive concentric-eccentric action of the

Journal of Athletic Training 889


plantar-flexor muscles in unipedal stance and is typically Table 1. Key Words for Search Strategy
quantified by the total number of raises performed. This achill* OR calf* OR plantarflex* OR tendocalcan* OR heel* OR soleus
method reflects the ability to perform repeated submaximal OR gastroc* (Abstract)
contractions (ie, fatigue or endurance).17 Consequently, the AND
heel-raise test is frequently used in clinical practice to assist tendon* OR tendin* (Abstract)
with diagnosis and to objectively assess the effects of AND
strength* OR weak* OR strong* OR power* OR force* OR isokinetic*
exercise interventions on AT. Its use is based on the
OR muscle* OR concentric* OR eccentric* OR isometric* OR
assumption that being able to perform pain-free heel raises torque* OR jump* OR hop* OR muscular OR neuromuscular OR
using repetitions comparable with the uninjured side neuro-muscular OR function* OR land* OR drop* OR raise OR
indicates functional restoration of strength. Despite the endurance OR fatigue* OR stiff* OR Hysteresis OR Rate of force
popularity of the heel-raise test in clinical practice, development OR RFD OR Ground reaction force OR GRF OR
physiological or clinical evidence to support its use is stress OR Strain OR Kinetic* OR fluctuation* OR oscillation* OR
limited.18,19 The preference for using the number of raises vibration* (Abstract)
as a primary outcome measure may be attributed to its AND
practical and ‘‘user-friendly’’ clinical application. Yet such non-injured OR noninjured OR asymptomatic OR contralat* OR
measures may not provide sufficient assessment of an opposite OR pain-free OR painfree OR control* OR healthy
(Abstract)
athlete’s entire strength profile. Consequently, the quanti-
fication of an individual’s functional capabilities may be
suboptimal, which may lead to persistent strength deficits12 confirmed by one of the authors (K.O.) to ensure that the
and inadequate rehabilitation programs, ultimately contrib- studies met the inclusion criteria and did not meet the
uting to the high recurrence rates seen with AT.20 exclusion criteria.
The lack of consensus on what exactly constitutes Inclusion Criteria. Studies were included if
strength may be adding to the predominance of unidimen-
sional measures for quantifying Achilles tendon function.  the researchers compared plantar-flexion (PF) muscle
To clarify this uncertainty, subcategories of strength have strength between individuals with AT and asymptomatic
been proposed, including maximal strength, which involves control participants or between injured and uninjured
maximal force development through high-load, low-veloc- sides within an AT population,
ity movements; explosive strength, which is the ability to  data were cross-sectional or baseline data from prospec-
rapidly produce muscle force through medium- to high- tive or intervention studies,
load, high-velocity movements (eg, rate of force develop-  articles were written in English and published in the 20
ment [RFD]); and reactive strength, which is the ability of
the calf-muscle complex to store and release energy years before our review, and
through sufficient function of the SSC through low-load,
 participants of any age were recruited.
high-velocity exercises (eg, hopping, jumping).21 Exclusion Criteria. We excluded studies if
Little consensus exists on the presence of strength deficits
in AT, so researchers are uncertain about the appropriate  the researchers investigated only kinematic variables,
methods of assessment that may inform rehabilitation in  the researchers investigated PF muscle strength in
clinical practice. Therefore, the purpose of our review was asymptomatic populations only,
to evaluate and summarize the evidence regarding the  participants with Achilles tendon rupture were explicitly
plantar-flexor strength profile in individuals with AT. included, or
 the researchers reported PF muscle strength only
METHODS postoperatively or after a strengthening intervention.
Search Strategy and Study Selection
The review was registered on the PROSPERO database Risk of Bias Assessment
(CRD42015025386) and has been reported in accordance The Critical Appraisal Skills Programme Case-Control
with the PRISMA statement for systematic reviews.22 The Study Checklist was used to assess the risk of bias in the
following databases were searched between February and
included studies.23 This checklist contains 12 questions;
April 2016 by 2 authors (S.M., J.H.) independently using an
questions 7 and 12 are guidance questions and were not
agreed-upon set of key words: Academic Search Complete,
AMED, Biomedical Reference Collection, MEDLINE, rated. Therefore, the included studies were appraised using
CINAHL, SPORTDiscus, Web of Science, Embase, and 10 questions. A list of criteria for each question and the
Scopus. The search strings are shown in Table 1. The 2 justification for providing the indicated score are outlined in
reviewers conducted the database searches independently Supplemental Tables 1 and 2 (available online at http://dx.
using prespecified inclusion and exclusion criteria. They doi.org/10.4085/1062-6050-43-18.S1). Two authors (S.M.,
independently compiled ‘‘short lists’’ of suitable abstracts M.O.) scored the studies independently using the criteria
and compared their respective short lists before reaching outlined, with any disagreements in scoring mediated by a
agreement on potentially relevant abstracts. A third third reviewer (K.O.). Given that the Critical Appraisal
reviewer (K.O.) reviewed the short-listed abstracts, and Skills Programme checklist was originally designed as an
any disagreement was discussed among the 3 reviewers. educational tool in a workshop setting, no overall quality
The primary author (S.M.) screened the agreed-upon score was awarded to the included studies. Instead, the
abstract list and obtained full texts of the studies that met strengths and weaknesses of each study were noted based
the inclusion criteria to create a final list. The final list was on these specific criteria.

890 Volume 54  Number 8  August 2019


Data Extraction RESULTS
The following data were extracted from each study by 2 Identification of Studies
reviewers (S.M., J.H.): characteristics of the participants
The electronic search yielded a total of 7133 potentially
(sample size, sex, and age) and details of the comparative
relevant studies. After the title and abstract of each study
assessment (groups compared, strength variable investigat-
were screened, 29 full-text studies were identified as
ed, and summary of the results). Study results were potentially relevant (Figure 1). A total of 11 studies were
extracted according to the subcategories for strength as removed after screening of the full texts.3,29–38 Searching
outlined previously. This included data on (1) maximal the reference lists of these full-text studies led to the
strength (peak torque [PT], maximal voluntary isometric addition of 1 study.39 The final number of studies reviewed
contraction, or peak force [in newtons]), (2) reactive was 19.
strength (distance and height during hopping or jumping
movements), and (3) explosive strength (RFD and ground
reaction force [GRF]). Data relating to the mechanical Participants
properties of the tendon (eg, tendon stiffness, leg stiffness, A detailed description of the selected studies, listed
tendon strain) or data on endurance (electromyography alphabetically, is provided in Supplemental Table 3. The
studies) or related concepts were not extracted. mean ages of the participants (range ¼ 24–59 years) were
similar among studies. A total of 13 studies11,19,40–50
Statistical Analysis included both male and female participants, whereas 6
studies13,39,51–54 included men only. The authors of 8
For all studies, where possible we computed the Hedges g studies13,39,42,43,48–51 compared strength measures between
effect size as a summary measure that is comparable across symptomatic and asymptomatic participants, the authors of
independent- and matched-groups study designs.24 If the 8 studies11,40,41,44–47,52 compared strength values between
standard deviation of the differences was not reported in injured and uninjured sides of the same participants, and the
studies examining differences between the injured and authors of 4 studies48,53–55 compared strength variables
uninjured limbs, it was estimated using the following between the injured and uninjured sides of the same
formula25: participant and between the injured side and asymptomatic
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi participants. Strength values between the ‘‘most’’ and
SDdiff ¼ SD21 þ SD22  2 3 r 3 SD1 3 SD2 ; ‘‘least’’ symptomatic sides were compared in 1 study.19 In
relation to the characteristics of the included studies
where r ¼ 0.7 was used as a conservative estimate of the comparing the injured limb with the asymptomatic controls,
within-participants correlation as recommended by Rosen- the control groups were generally similar with regard to sex
thal.26 Hedges g and associated 95% confidence intervals and age; only Firth et al43 reported variability in sex
(CIs) were computed manually using the formulae provided between groups. The average duration of symptoms among
by Borenstein et al.24 A positive effect size indicated the participants (range ¼ 5 weeks–37 months) was reported in
investigated strength measure was greater for the uninjured 15 of 19 studies.
limb or asymptomatic group. The magnitude of Hedges g
effect sizes was interpreted using the Cohen25 convention Outcome Measures
as small (0.2), medium (0.5), or large (0.8).
Studies were pooled for the meta-analysis according to Maximal-strength values using isokinetic dynamometry
similarities in study characteristics and methods. Given were reported in 8 studies.11,39–41,46,47,49,54 Large variations
the range of variables used in isokinetic dynamometry, the were present in the speed and mode of contraction.
results were further pooled according to the mode of Researchers investigated PF PT at slow speeds (1208/s)
contraction (eccentric or concentric) and speed of in 7 studies11,39–41,47,49,54 and at fast speeds (.1208/s) in 7
contraction (fast [.1208/s] or slow [1208/s]). Hedges g studies.11,39–41,46,47,54 Maximal isometric-strength measures
effect sizes were pooled using random-effects models. We were reported in 3 studies13,45,48 using various force
selected random-effects models a priori to account for apparatuses. Silbernagel et al19 used a variety of heel-raise
expected differences in study characteristics. Heterogene- tests to quantify both concentric and eccentric PF strength
ity between studies was assessed using the I2 statistic, and heel-raise–test outcomes using a customized spring-
which summarizes the percentage of total variation across loaded linear encoder. Authors investigated explosive-
strength variables in 7 studies,42,45,49–53 reported values
studies due to differences between studies rather than
for RFD in 2 studies,45,52 and addressed GRF in 5
chance. An I2 value of 30% or less indicates low
studies.42,49–51,53 For reactive-strength variables, various
heterogeneity, with cutoffs of I2 greater than 30% and I2
single-legged hop or jumping variables were compared in 4
greater than 50% indicative of moderate and substantial
studies.19,43,44,52
heterogeneity, respectively.27 For some outcomes of
interest, the data could not be pooled because of
heterogeneity in the measures, the methods used, or Risk of Bias
because only 1 study examined an outcome of interest (eg, The risk of bias of the included studies using the Critical
eccentric PF PT as a percentage of BW [BW%]) at 1808/ Appraisal Skills Programme checklist is shown in Table 2.
s). In these situations, such results are reported using One of the main weaknesses involved the reporting of
weighted means. All meta-analyses were carried out using statistical findings. Whereas most authors provided actual
the Excel (version 2010; Microsoft Corp, Redmond, WA) values with accompanying P values, few provided 95% CI
spreadsheets of Neyeloff et al.28 statistics. A further limitation was the considerable

Journal of Athletic Training 891


Figure 1. Literature search flowchart.

variation in the measurement techniques used by some symptomatic group. Finally, several investigators41,46,53 did
researchers. Among the 4 studies42,49,51,53 in which GRF not provide detailed inclusion criteria.
was investigated, a large amount of variability was present
in the methods used to measure GRF. For example, some Maximal-Strength Profile
authors used an instrumented treadmill to measure GRF,
and others used force plates integrated in running tracks Isokinetic Dynamometry. The meta-analyses revealed
across a variety of capture distances. Furthermore, a large moderate effect sizes for concentric PF PT fast (pooled
number of variables were reported for GRF across studies, Hedges g ¼ 0.61; 95% CI ¼ 0.43, 0.79; Figure 2) and
such as horizontal braking force, vertical impact force, concentric PF PT slow (pooled Hedges g ¼ 0.43; 95% CI ¼
vertical loading rate, and vertical impulse. This variation in 0.25, 0.62; Figure 3). However, effect sizes for eccentric PF
reported variables may have accounted for the variation in PT slow were small (pooled Hedges g ¼ 0.25; 95% CI ¼
findings, leading to difficulty drawing conclusions from this 0.09, 0.40; Figure 4). These differences reflected deficits of
outcome. Another limitation was the wide range of approximately 38%, 44%, and 18%, respectively, between
symptom durations. The variations in symptom duration the symptomatic and asymptomatic sides or between the
suggested that considerable variation within the populations symptomatic side and asymptomatic controls.
studied may have been present; however, this may also As outlined, the data are reported using weighted means
have had the advantage of increasing the generalizability of when pooling was inappropriate because of heterogeneity
the findings. Whereas most researchers who compared in the measures, the methods used, or because only 1 study
strength between the injured limb and asymptomatic examined an outcome of interest.
controls ensured matched control groups, Firth et al43 Isokinetic Strength. Large effect sizes were observed for
included a control group that had more men than in the eccentric PF PT fast (Hedges g ¼ 1.26; 95% CI ¼ 0.34,

892 Volume 54  Number 8  August 2019


With Other
Results Fit
2.18),39 moderate effect sizes were observed for eccentric

Evidence?
PF PT BW% at 1808/s (Hedges g ¼ 0.36; 95% CI ¼ 0.07,

Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes

Yes

Yes
Yes
Yes
No

No
No
No

No

No
0.79),49 and small effect sizes were observed for eccentric
PF PT BW% at 608/s (Hedges g ¼ 0.24; 95% CI ¼ 0.19,
0.6749; Figure 5).
Generalizability

Isometric Strength. Small to moderate effect sizes were


of Results?

reported in 2 studies,45,48 indicating reduced isometric PF


Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes

Yes

Yes
Yes
Yes
Yes
Yes
strength in those with AT (Hedges g ¼ 0.46–0.78). These

No

No
No
No
effect sizes equated to a reduction of 5% to 12% between
the symptomatic and asymptomatic sides or between the
symptomatic side and asymptomatic controls. In contrast,
Child et al13 reported greater isometric strength in those
Reported?
Statistics

with AT than controls (9% stronger; Hedges g ¼ 0.30;


Clearly

Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes
Yes
Yes
Yes

Yes
Yes
Yes
Yes
No

No
95% CI ¼ 1.01, 0.41; Figure 5).
Isoinertial Strength. Silbernagel et al19 investigated PF
strength using a weighted eccentric-concentric calf-raise
test and a concentric calf-raise test. The PF strength was
of Results?
Precision

reduced in the most symptomatic side compared with the


Yes
Yes

Yes

Yes
Yes
least symptomatic side (Hedges g ¼ 0.30–0.60; Figure 5).
No
No
No
No
No
No

No
No

No
No
No

No
No
No
The results equated to a difference ranging from 16% to
28% (mean difference ¼ 39–83 W) between the most
symptomatic and least symptomatic sides. The remaining
Confounding

calf-raise test, which was a traditional calf-raise test with


Control of

Factors?

the addition of 10% BW, indicated no difference (P ¼ .08)


Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

in the number of repetitions performed between the least (n


¼ 24) and most (n ¼ 22) symptomatic sides.

Explosive-Strength Profile
Measured?
Accurately
Exposure

Ground Reaction Force. Five studies42,49,50,52,53 reported


Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes

Yes

Yes
Yes

Yes
No

No

No
No
No

No

inconsistent results of both increased and decreased GRF in


those with AT (Hedges g ¼ 0.73–0.66; Figure 6).
Rate of Force Development. Small to large effect sizes
indicated reduced RFD in those with AT across a variety of
of Controls?
Recruitment
Appropriate

time intervals measured (Hedges g ¼ 0.42–1.73; Figure


Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes

Yes
Yes
Yes

Yes

Yes
Yes
No

No

No

No

No

6).45,52 These effect sizes equated to a reduction of 10% to


21% between the symptomatic and asymptomatic sides.

Reactive-Strength Profile (Hopping)


Recruitment
of Patients?
Appropriate

Small to large effect sizes were reported19,43,44,52 for


Yes
Yes
Yes

Yes
Yes

Yes
Yes

Yes
Yes

Yes
Yes
Yes
Yes
Yes
No
No

No

No

No

reduced hop performance in those with AT using a variety of


hop tests (Hedges g ¼ 0.32–2.61; Figure 7). This reflected a
difference of approximately 16% to 35% between the more
and less symptomatic sides. The mean difference in distance
Table 2. Risk of Bias Assessment of Included Studies

Methodology?
Appropriate

hopped was 33% (43 cm) for the single-legged hop and 35%
(151 cm) for the triple-legged hop. Average and maximal
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

hop height during a single-legged hop demonstrated deficits


of 18% (0.6 cm) and 16% (2.12 cm), respectively, on the
symptomatic side. In addition, the hopping quotient (flight
time/contact time) was reduced by 20% (0.1) on the
Focused
Issue?

symptomatic side during a single-legged hop.


Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes
Yes

Heterogeneity
Statistical analysis revealed the percentage of total
Silbernagel et al19 (2006)
Alfredson et al11 (1998)
Alfredson et al40 (1998)
Alfredson et al41 (1998)
Alfredson et al46 (1996)

variation across studies was low when comparing injured


Azevedo et al42 (2009)

McCrory et al49 (1999)


Masood et al48 (2014)
Haglund-Åkerlind and

Öhberg et al47 (2001)


Becker et al50 (2017)

Mayer et al54 (2007)

and uninjured sides versus injured sides and asymptomatic


Maquirriain44 (2012)

Wang et al52 (2012)


Wang et al45 (2011)
Eriksson39 (1993)
Grigg et al51 (2013)
Child et al13 (2010)
Baur et al53 (2004)

Firth et al43 (2010)

controls (Figures 2–4).

DISCUSSION
Study

The results of this systematic review and meta-analysis


demonstrated that individuals with AT displayed deficits in

Journal of Athletic Training 893


Figure 2. Meta-analysis of concentric plantar-flexion peak torque, fast. Abbreviation: CI, confidence interval.

Figure 3. Meta-analysis of concentric plantar-flexion peak torque, slow. Abbreviation: CI, confidence interval.

Figure 4. Meta-analysis of eccentric plantar flexion peak torque, slow. Abbreviation: CI, confidence interval.

894 Volume 54  Number 8  August 2019


Figure 5. Effect sizes for maximal strength variables. a Injured side versus asymptomatic control. b Injured versus uninjured side. c Most
versus least symptomatic side. Abbreviation: CI, confidence interval.

PF strength when the injured side was compared with the or jumping. Our results also indicated a consistent trend
uninjured side or with asymptomatic controls. Deficits in toward reduced explosive strength (10%–21% deficit) in
maximal-, reactive-, and explosive-strength outcomes were individuals with AT assessed by quantifying the RFD.
reported across the strength spectrum. Given that the RFD quantifies the ability to quickly produce
muscle force,58 identifying deficits may be important when
Assessing Musculotendinous Function in AT assessing individuals with AT to help guide rehabilitation.
In addition to explosive strength, many athletic move-
In clinical settings, the primary method used to assess PF ments, such as running and jumping, also require
function in individuals with AT has been the calf-raise or substantial amounts of reactive strength to store and release
heel-raise test. The validity of the heel-raise test as an energy and force. In AT, quantifying hopping ability (eg,
appropriate method for assessing PF strength in AT has hop distance, hop height) appears to be the most popular
been highlighted.17 However, relying on such unidimen- method of assessing reactive strength. Our results indicated
sional measures to quantify PF function may hinder the deficits of 16% to 35% in individuals with AT, suggesting
appropriate identification of functional deficits in AT, that these tests may be an appropriate way of assessing
which may lead to inadequate rehabilitation and persistent reactive-strength deficits in AT. Various hopping tasks have
symptoms. Our findings highlight the potential scope of the advantage of being inexpensive, quick, and reliable in
additional methods of quantifying PF strength in AT. research and clinical settings59; however, in isolation, they
Deficits in maximal strength ranging from 16% to 28% may not discriminate between people using very different
were reported using weighted concentric and eccentric calf- movement patterns to achieve hop distances, and hopping
raise tests, whereas deficits of 18% to 44% were observed does not isolate the PF muscle group. Similar magnitudes
when using eccentric and concentric isokinetic PT of deficits in reactive strength have also been reported after
assessments. Therefore, these assessment techniques may ankle60 and anterior cruciate ligament58,61 injury. However,
be more appropriate for identifying strength deficits than a reactive strength requires considerable effort and functional
BW maximal-repetition heel-raise test, in which deficits demands, so assessing reactive strength may not always be
appear to be much less obvious (deficits of only 8% appropriate, depending on an individual’s loading demands
between sides for the traditional BW heel-raise test). and current capacity. The gross nature and variability of
Unfortunately, research comparing these deficits in maxi- movement strategies possible during such tasks highlight
mal strength, particularly isokinetic variables, with other the need to combine these assessment techniques with other
pathologic tendon conditions is limited. We reported functional measures.62
deficits of 5% to 12% for maximal isometric strength, A further assessment technique that may complement the
which is broadly comparable with the isometric-strength aforementioned functional outcome measures is evaluation
deficits reported (9%–32%) for both patellar and gluteus of the tendon’s mechanical properties. Achilles tendinop-
medius tendinopathy.55–57 athy leads to alterations in the mechanical properties of the
Maximal-strength variables represent only 1 aspect of an tendon, typically reduced tendon stiffness and increased
individual’s overall strength profile and crucially may not strain.51,52,63 Researchers13,64,65 have postulated that such
sufficiently assess the explosive-strength capabilities that altered mechanical properties in AT may lead to increased
are fundamental during sport movements, such as running strain on the Achilles tendon, contributing to the ongoing

Journal of Athletic Training 895


Figure 6. Effect sizes for explosive-strength variables. A, Ground reaction force. B, Normalized rate of force development. a Injured side
versus asymptomatic controls. b Injured versus uninjured side versus asymptomatic controls. c Injured versus uninjured side.
Abbreviation: CI, confidence interval.

recurrence of symptoms due to an inability to dissipate ultrasound imaging combined with isokinetic dynamome-
forces during SSC loading activities. An emerging body of try. Although it is beyond the scope of this review,
literature55,56,64 has indicated that the tendon’s mechanical correlating the tendon’s mechanical properties using
response to load may be quantified in individuals with AT traditional functional measures may identify areas to be
using methods such as shear-wave elastography or addressed during rehabilitation.

896 Volume 54  Number 8  August 2019


Figure 7. Effect sizes for reactive-strength variables (hopping). a Injured side versus asymptomatic controls. b
Injured versus uninjured
side. c Most versus least symptomatic side. Abbreviation: CI, confidence interval.

Appropriate Comparative Groups in Assessing be the nonresolution of the strength deficits associated
Strength Variables with AT. The degree of improvement in PF strength
An area of debate in assessing strength outcomes among (maximal-, explosive-, and reactive-strength outcomes)
patients with tendinopathy centers on the suitability of the after loading interventions has been reported for only a
uninjured side as a comparison. In their systematic review, few strengthening interventions for AT. Yu et al79 and
Heales et al66 demonstrated motor deficits in the contralat- Alfredson et al41 noted improvements in concentric PF PT
eral uninjured limb of patients with unilateral tendinopathy of 10% to 15%, respectively, after the completion of a 12-
compared with asymptomatic controls, suggesting that the week strengthening intervention. However, such reported
uninjured side may not be as ‘‘healthy’’ and unaffected as a improvements were less than the deficits we observed in
pain-free matched control. In contrast, we did not find any isokinetic maximal-strength variables (up to 44%). Such
differences in effect sizes when comparing the injured and nonresolution of deficits after strength interventions was
uninjured sides or when comparing the injured side with reiterated by Silbernagel et al,12 who demonstrated that
asymptomatic matched controls. One potential explanation full symptomatic recovery did not ensure full recovery of
may relate to the characteristics of the studies included in muscle-tendon function in patients with AT. Comparisons
the review by Heales et al66; researchers in 18 of the 20 of outcomes at baseline and 1 year after a loading
studies investigated motor deficits in upper limb tendons, intervention revealed that only 4 (25%) of the 16 patients
which may limit the generalizability to the lower limb. A (67%) who had fully recovered had achieved an
further consideration is the influence of limb dominance in acceptable level of muscle function, which was defined
strength comparisons. In sport environments that require as having normal (90%) capability across the test
unilateral-dominant movements (eg, jumping in volleyball battery. These findings suggested that individuals with
or basketball), athletes may have a favored jumping limb, AT continued to display strength deficits despite reduced
which can complicate comparisons. Further research is pain and disability. The persistence of strength deficits
warranted to improve our understanding of appropriate could be speculated to result in the tendon’s inability to
comparative groups when assessing strength in patients withstand the desired load, potentially accounting for the
with tendinopathy. high recurrence rate associated with AT. In fact, the ‘‘one-
size-fits-all’’ method of assessing and rehabilitating
Current Rehabilitation Programs and Adequately Achilles tendon function may fail to adequately address
Addressing Deficits in Achilles Tendon Function deficits not only in maximal-strength variables but also
Exercise or strength interventions using repetitive throughout the entire strength spectrum.12,80 Alfredson
concentric-eccentric PF muscle exercises have become eccentric loading has become the mainstay of conservative
the cornerstone of conservative treatment for AT.67 The treatment for chronic AT.67 The preference for eccentric-
most popular exercise intervention has been the Alfredson only interventions reflects the suggestion that eccentric
heel-drop program, which is characterized by progressive, training is more specific and provides a greater load via
twice-daily, eccentric-only contractions over a 12-week the force-velocity curve than concentric loading.81 How-
period.11 The popularity of other strengthening programs, ever, evidence to support these claims appears tenuous.81
most notably progressive mixed concentric-eccentric load- Training only 1 aspect of an individual’s strength profile
ing and mixed-contraction, heavy, slow resistance training, may not optimally improve performance across the entire
has grown.12,38,55,68,69 Regardless of the mode of contrac- strength spectrum. Few researchers have attempted to
tion, strength interventions have been reasonably effective address the entire strength spectrum in an intervention
in improving pain and disability in those with midportion study. Notably, Silbernagel et al12 used a loading
AT; the average reduction in pain was approximately intervention aimed at improving functional outcomes
55%.34,68,70–78 across the entire strength spectrum by integrating
Despite the relative success of loading interventions for plyometric exercises for longer than the traditional 12
improving pain and disability, AT is associated with a weeks, which resulted in improvements in pain and
high recurrence rate (27%).20,35 One potential reason for disability at 1-year follow-up. This finding highlights the
the high recurrence rate and persistence of symptoms may need for further research in this area.

Journal of Athletic Training 897


Mechanistic Effects of Strength Training in ACKNOWLEDGMENTS
Tendinopathy This study was supported by PhD scholarships from the School
Numerous mechanistic theories have been proposed to of Allied Health, the University of Limerick (Dr McAuliffe) and
the Irish Research Council (Mr Hurley) and by a research grant
explain improvements in pain and disability associated
from the Private Physiotherapy Educational Foundation (Dr
with strengthening interventions in AT. The term mech- O’Neill).
anotherapy has been used to describe how the body
converts a mechanical stimulus into a cellular response,82
REFERENCES
which may influence structural alterations in the tendon
due to AT (eg, disorganized collagen architecture, thinner 1. O’Brien M. The anatomy of the Achilles tendon. Foot Ankle Clin.
collagen fibers, increased water content in the extracellu- 2005;10(2):225–238.
lar matrix). These structural alterations may alter a 2. Bjur D, Alfredson H, Forsgren S. The innervation pattern of the
tendon’s capacity to store and produce kinetic energy, human Achilles tendon: studies of the normal and tendinosis tendon
with markers for general and sensory innervation. Cell Tissue Res.
affecting strength and functional performance.13,83 Inves-
2005;320(1):201–206.
tigators84,85 have suggested that the loading forces applied
3. Paavola M, Kannus P, Paakkala T, Pasanen M, Jarvinen M. Long-
to the tendon will help stimulate the remodeling of the term prognosis of patients with Achilles tendinopathy: an observa-
abnormal tendon structure. However, alterations in tendon tional 8-year follow-up study. Am J Sports Med. 2000;28(5):634–642.
structure may not be associated with improved clinical 4. Kvist M. Achilles tendon injuries in athletes. Sports Med.
outcomes. In a systematic review, Drew et al86 concluded 1994;18(3):173–201.
that alterations in tendon structure did not adequately 5. Alfredson H, Lorentzon R. Chronic Achilles tendinosis: recom-
explain the response to loading interventions in tendinop- mendations for treatment and prevention. Sports Med.
athy, which is consistent with little turnover of collagen 2000;29(2):135–146.
after puberty.87 Nevertheless, tendon structure can be 6. Józsa LG, Kannus P. Human Tendons: Anatomy, Physiology, and
altered in young populations (,25 years) after loading Pathology. Champaign, IL: Human Kinetics; 1997.
interventions.88,89 Whereas the evidence for the effect of 7. Fukashiro S, Komi PV, Järvinen M, Miyashita M. In vivo Achilles
loading interventions in altering abnormal tendon struc- tendon loading during jumping in humans. Eur J Appl Physiol
ture is conflicting, loading interventions may effectively Occup Physiol. 1995;71(5):453–458.
improve the mechanical properties of the tendon, albeit in 8. Komi PV. Stretch-shortening cycle: a powerful model to study
normal and fatigued muscle. J Biomech. 2000;33(10):1197–1206.
asymptomatic populations.90
9. Cook JL, Rio E, Purdam CR, Docking SI. Revisiting the continuum
model of tendon pathology: what is its merit in clinical practice and
LIMITATIONS research? Br J Sports Med. 2016;50(19):1187–1191.
Our study had limitations. We pragmatically limited 10. Mahieu NN, Witvrouw E, Stevens V, Van Tiggelen D, Roget P.
inclusion to studies published in the 20 years before our Intrinsic risk factors for the development of Achilles tendon overuse
injury: a prospective study. Am J Sports Med. 2006;34(2):226–235.
review. Another potential limitation relates to the
11. Alfredson H, Pietilä T, Jonsson P, Lorentzon R. Heavy-load
exclusion of tendon mechanical properties. Originally, eccentric calf muscle training for the treatment of chronic Achilles
we planned to incorporate assessments of tendon mechan- tendinosis. Am J Sports Med. 1998;26(3):360–366.
ical properties (eg, stress, strain); however, the scope of 12. Silbernagel KG, Thomee R, Eriksson BI, Karlsson J. Full
the topic area became too broad, and these aspects were symptomatic recovery does not ensure full recovery of muscle-
removed. The cross-sectional nature of the included tendon function in patients with Achilles tendinopathy. Br J Sports
studies led to difficulty in determining a causal relation- Med. 2007;41(4):276–280.
ship between strength and the development of AT 13. Child S, Bryant AL, Clark RA, Crossley KM. Mechanical properties
symptoms, although the authors of 1 prospective study10 of the Achilles tendon aponeurosis are altered in athletes with
reported that reduced PF strength predicted the onset of Achilles tendinopathy. Am J Sports Med. 2010;38(9):1885–1893.
AT in military recruits. Finally, whereas pathologic 14. Ngomo S, Mercier C, Bouyer LJ, Savoie A, Roy JS. Alterations in
tendon changes on the uninjured side or in asymptomatic central motor representation increase over time in individuals with
controls can potentially influence strength variables, few rotator cuff tendinopathy. Clin Neurophysiol. 2015;126(2):365–371.
researchers provided information on the control side or a 15. Rio E, Kidgell D, Purdam C, et al. Isometric exercise induces
analgesia and reduces inhibition in patellar tendinopathy. Br J
comparative group, making it difficult to investigate this
Sports Med. 2015;49(19):1277–1283.
phenomenon. 16. Edgerton VR, Roy RR, Allen DL, Monti RJ. Adaptations in skeletal
muscle disuse or decreased-use atrophy. Am J Phys Med Rehabil.
CONCLUSIONS 2002;81(suppl 11):S127–S147.
Individuals with AT displayed deficits in maximal, 17. Hébert-Losier K, Newsham-West RJ, Schneiders AG, Sullivan SJ.
Raising the standards of the calf-raise test: a systematic review. J
reactive, and explosive strength compared with the
Sci Med Sport. 2009;12(6):594–602.
uninjured side or asymptomatic controls. Our focus on 18. Bruyère O, Beaudart C, Reginster JY, et al. Assessment of muscle
maximal strength during assessments and rehabilitation, mass, muscle strength and physical performance in clinical practice:
with little emphasis on explosive or reactive strength, an international survey. Eur Geriatr Med. 2016;7(3):243–246.
possibly did not optimally match the entire strength 19. Silbernagel KG, Gustavsson A, Thomee R, Karlsson J. Evaluation
spectrum. This could also explain why strengthening of lower leg function in patients with Achilles tendinopathy. Knee
exercises have had moderate effectiveness in reducing pain Surg Sports Traumatol Arthrosc. 2006;14(11):1207–1217.
and disability in AT, yet residual deficits and high 20. Gajhede-Knudsen M, Ekstrand J, Magnusson H, Maffulli N.
recurrence rates persisted even after strength training. Recurrence of Achilles tendon injuries in elite male football players

898 Volume 54  Number 8  August 2019


is more common after early return to play: an 11-year follow-up of 40. Alfredson H, Nordström P, Lorentzon R. Prolonged progressive
the UEFA Champions League injury study. Br J Sports Med. calcaneal bone loss despite early weightbearing rehabilitation in
2013;47(12):763–768. patients surgically treated for Achilles tendinosis. Calcif Tissue Int.
21. Beattie K, Kenny IC, Lyons M, Carson BP. The effect of strength 1998;62(2):166–171.
training on performance in endurance athletes. Sports Med. 41. Alfredson H, Pietilä T, Ohberg L, Lorentzon R. Achilles tendinosis
2014;44(6):845–865. and calf muscle strength: the effect of short-term immobilization
22. Moher D, Liberati A, Tetzlaff J, Altman DG; the PRISMA Group. after surgical treatment. Am J Sports Med. 1998;26(2):166–171.
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: 42. Azevedo LB, Lambert MI, Vaughan CL, O’Connor CM, Schwell-
the PRISMA statement. Ann Intern Med. 2009;151(4):264–269. nus MP. Biomechanical variables associated with Achilles tendin-
23. Critical Appraisal Skills Programme. CASP Case-Control Study opathy in runners. Br J Sports Med. 2009;43(4):288–292.
Checklist. https://casp-uk.net/wp-content/uploads/2018/01/CASP- 43. Firth BL, Dingley P, Davies ER, Lewis JS, Alexander CM. The
Case-Control-Study-Checklist-2018.pdf. Accessed November 14, effect of kinesiotape on function, pain, and motoneuronal
2018. excitability in healthy people and people with Achilles tendinop-
24. Borenstein M, Hedges LV, Higgins J, Rothstein HR. A basic athy. Clin J Sport Med. 2010;20(6):416–421.
introduction to fixed-effect and random-effects models for meta- 44. Maquirriain J. Leg stiffness changes in athletes with Achilles
analysis. Res Synth Meth. 2010;1(2):97–111. tendinopathy. Int J Sports Med. 2012;33(7):567–571.
25. Cohen J. Statistical Power Analysis for the Social Sciences. 45. Wang HK, Lin KH, Wu YK, Chi SC, Shih TTF, Huang YC. Evoked
Hillsdale, NJ: Lawrence Erlbaum Associates; 1988. spinal reflexes and force development in elite athletes with middle-
26. Rosenthal R. Meta-Analytic Procedures for Social Research. Vol 6. portion Achilles tendinopathy. J Orthop Sports Phys Ther.
Newbury Park, CA: Sage Publications; 1991. 2011;41(10):785–794.
27. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring 46. Alfredson H, Pietilä T, Lorentzon R. Chronic Achilles tendinitis and
inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560. calf muscle strength. Am J Sports Med. 1996;24(6):829–833.
28. Neyeloff JL, Fuchs SC, Moreira LB. Meta-analyses and forest plots 47. Öhberg L, Lorentzon R, Alfredson H. Good clinical results but
using a Microsoft Excel spreadsheet: step-by-step guide focusing on persisting side-to-side differences in calf muscle strength after
descriptive data analysis. BMC Res Notes. 2012;5:52. surgical treatment of chronic Achilles tendinosis: a 5-year follow-
29. Chimenti RL, Flemister AS, Tome J, et al. Altered tendon up. Scand J Med Sci Sports. 2001;11(4):207–212.
characteristics and mechanical properties associated with insertional
48. Masood T, Kalliokoski K, Bojsen-Mller J, Magnusson SP, Finni T.
Achilles tendinopathy. J Orthop Sports Phys Ther. 2014;44(9):680–
Plantarflexor muscle function in healthy and chronic Achilles
689.
tendon pain subjects evaluated by the use of EMG and PET
30. Nawoczenski DA, Barske H, Tome J, Dawson LK, Zlotnicki JP,
imaging. Clin Biomech (Bristol, Avon). 2014;29(5):564–570.
DiGiovanni BF. Isolated gastrocnemius recession for Achilles
49. McCrory JL, Martin DF, Lowery RB, et al. Etiologic factors
tendinopathy: strength and functional outcomes. J Bone Joint Surg
associated with Achilles tendinitis in runners. Med Sci Sports Exerc.
Am. 2015;97(2):99–105.
1999;31(10):1374–1381.
31. Croisier JL, Forthomme B, Foidart-Dessalle M, Godon B, Crielaard
50. Becker J, James S, Wayner R, Osternig L, Chou LS. Biomechanical
JM. Treatment of recurrent tendinitis by isokinetic eccentric
factors associated with Achilles tendinopathy and medial tibial
exercises. Isokinet Exerc Sci. 2001;9(2–3):133–141.
stress syndrome in runners. Am J Sports Med. 2017;45(11):2614–
32. Maffulli N, Walley G, Sayana MK, Longo UG, Denaro V. Eccentric
2621.
calf muscle training in athletic patients with Achilles tendinopathy.
51. Grigg NL, Wearing SC, O’Toole JM, Smeathers JE. Achilles
Disabil Rehabil. 2008;30(20–22):1677–1684.
tendinopathy modulates force frequency characteristics of eccentric
33. Ram R, Meeuwisse W, Patel C, Wiseman DA, Wiley JP. The limited
effectiveness of a home-based eccentric training for treatment of exercise. Med Sci Sports Exerc. 2013;45(3):520–526.
Achilles tendinopathy. Clin Invest Med. 2013;36(4):E197–E206. 52. Wang HK, Lin KH, Su SC, Shih TF, Huang YC. Effects of tendon
34. Rompe JD, Nafe B, Furia JP, Maffulli N. Eccentric loading, shock- viscoelasticity in Achilles tendinosis on explosive performance and
wave treatment, or a wait-and-see policy for tendinopathy of the clinical severity in athletes. Scand J Med Sci Sports. 2012;22(6):e147–
main body of tendo Achillis: a randomized controlled trial. Am J e155.
Sports Med. 2007;35(3):374–383. 53. Baur H, Divert C, Hirschmüller A, Müller S, Belli A, Mayer F.
35. Van der Plas A, de Jonge S, de Vos RJ, et al. A 5-year follow-up Analysis of gait differences in healthy runners and runners with
study of Alfredson’s heel-drop exercise programme in chronic chronic Achilles tendon complaints. Isokinet Exerc Sci.
midportion Achilles tendinopathy. Br J Sports Med. 2012;46(3):214– 2004;12(2):111–116.
218. 54. Mayer F, Hirschmüller A, Müller S, Schuberth M, Baur H. Effects
36. Habets B, van Cingel REH, Backx FJG, Huisstede BMA. Alfredson of short-term treatment strategies over 4 weeks in Achilles
versus Silbernagel exercise therapy in chronic midportion Achilles tendinopathy. Br J Sports Med. 2007;41(7):e6.
tendinopathy: study protocol for a randomized controlled trial. BMC 55. Kongsgaard M, Qvortrup K, Larsen J, et al. Fibril morphology and
Musculoskelet Disord. 2017;18(1):296. tendon mechanical properties in patellar tendinopathy: effects of
37. Baur H, Müller S, Hirschmüller A, Cassel M, Weber J, Mayer F. heavy slow resistance training. Am J Sports Med. 2010;38(4):749–
Comparison in lower leg neuromuscular activity between runners 756.
with unilateral mid-portion Achilles tendinopathy and healthy 56. Helland C, Bojsen-Mller J, Raastad T, et al. Mechanical properties
individuals. J Electromyogr Kinesiol. 2011;21(3):499–505. of the patellar tendon in elite volleyball players with and without
38. Silbernagel KG, Thomee R, Eriksson BI, Karlsson J. Continued patellar tendinopathy. Br J Sports Med. 2013;47(13):862–868.
sports activity, using a pain-monitoring model, during rehabilitation 57. Allison K, Vicenzino B, Wrigley TV, Grimaldi A, Hodges PW,
in patients with Achilles tendinopathy: a randomized controlled Bennell KL. Hip abductor muscle weakness in individuals with
study. Am J Sports Med. 2007;35(6):897–906. gluteal tendinopathy. Med Sci Sports Exerc. 2016;48(3):346–352.
39. Haglund-Åkerlind PY, Eriksson E. Range of motion, muscle torque 58. Angelozzi M, Madama M, Corsica C, et al. Rate of force
and training habits in runners with and without Achilles tendon development as an adjunctive outcome measure for return-to-sport
problems. Knee Surg Sports Traumatol Arthrosc. 1993;1(3–4):195– decisions after anterior cruciate ligament reconstruction. J Orthop
199. Sports Phys Ther. 2012;42(9):772–780.

Journal of Athletic Training 899


59. Swearingen J, Lawrence E, Stevens J, Jackson C, Waggy C, Davis 75. Yelland MJ, Sweeting KR, Lyftogt JA, Ng SK, Scuffham PA, Evans
DS. Correlation of single leg vertical jump, single leg hop for KA. Prolotherapy injections and eccentric loading exercises for
distance, and single leg hop for time. Phys Ther Sport. painful Achilles tendinosis: a randomised trial. Br J Sports Med.
2011;12(4):194–198. 2011;45(5):421–428.
60. Caffrey E, Docherty CL, Schrader J, Klossnner J. The ability of 4 76. Langberg H, Ellingsgaard H, Madsen T, et al. Eccentric rehabil-
single-limb hopping tests to detect functional performance deficits itation exercise increases peritendinous type I collagen synthesis in
in individuals with functional ankle instability. J Orthop Sports humans with Achilles tendinosis. Scand J Med Sci Sports.
Phys Ther. 2009;39(11):799–806. 2007;17(1):61–66.
61. Augustsson J, Thomeé R, Karlsson J. Ability of a new hop test to 77. Mafi N, Lorentzon R, Alfredson H. Superior short-term results with
determine functional deficits after anterior cruciate ligament recon- eccentric calf muscle training compared to concentric training in a
struction. Knee Surg Sports Traumatol Arthrosc. 2004;12(5):350–356. randomized prospective multicenter study on patients with chronic
62. Ortiz A, Olson S, Trudelle-Jackson E, Rosario M, Venegas HL. Achilles tendinosis. Knee Surg Sports Traumatol Arthrosc.
Landing mechanics during side hopping and crossover hopping 2001;9(1):42–47.
maneuvers in noninjured women and women with anterior cruciate 78. Murphy M, Travers M, Gibson W, et al. Rate of improvement of
ligament reconstruction. PM R. 2011;3(1):13–20. pain and function in mid-portion Achilles tendinopathy with loading
63. Lee MH, Cha JG, Jin W, et al. Utility of sonographic measurement protocols: a systematic review and longitudinal meta-analysis.
of the common tensor tendon in patients with lateral epicondylitis. Sports Med. 2018;48(8):1875–1891.
AJR Am J Roentgenol. 2011;196(6):1363–1367. 79. Yu J, Park D, Lee G. Effect of eccentric strengthening on pain,
64. Arya S, Kulig K. Tendinopathy alters mechanical and material muscle strength, endurance, and functional fitness factors in male
properties of the Achilles tendon. J Appl Physiol (1985). patients with Achilles tendinopathy. Am J Phys Med Rehabil.
2010;108(3):670–675. 2013;92(1):68–76.
65. Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H. Elastic 80. Silbernagel KG. Does one size fit all when it comes to exercise
properties of human Achilles tendon are correlated to muscle treatment for Achilles tendinopathy? J Orthop Sports Phys Ther.
strength. J Appl Physiol (1985). 2005;99(2):665–669.
2014;44(2):42–44.
66. Heales LJ, Lim EC, Hodges PW, Vicenzino B. Sensory and motor
81. Allison GT, Purdam C. Eccentric loading for Achilles tendinopathy:
deficits exist on the non-injured side of patients with unilateral
strengthening or stretching? Br J Sports Med. 2009;43(4):276–279.
tendon pain and disability: implications for central nervous system
82. Khan KM, Scott A. Mechanotherapy: how physical therapists’
involvement. A systematic review with meta-analysis. Br J Sports
prescription of exercise promotes tissue repair. Br J Sports Med.
Med. 2014;48(19):1400–1406.
2009;43(4):247–252.
67. Malliaras P, Barton CJ, Reeves ND, Langberg H. Achilles and
83. Wang JH. Mechanobiology of tendon. J Biomech. 2006;39(9):1563–
patellar tendinopathy loading programmes: a systematic review
1582.
comparing clinical outcomes and identifying potential mechanisms
84. Wearing SC, Grigg NL, Hooper SL, Appleton EE, Smeathers JE.
for effectiveness. Sports Med. 2013;43(4):267–286.
The acute response of tendon to loading: implications for
68. Beyer R, Kongsgaard M, Hougs Kjær B, Øhlenschlæger T, Kjær M,
Magnusson SP. Heavy slow resistance versus eccentric training as rehabilitation. J Foot Ankle Res. 2011;4(suppl 1):I13.
treatment for Achilles tendinopathy: a randomized controlled trial. 85. Ohberg L, Lorentzon R, Alfredson H. Eccentric training in patients
Am J Sports Med. 2015;43(7):1704–1711. with chronic Achilles tendinosis: normalised tendon structure and
69. Kongsgaard M, Kovanen V, Aagaard P, et al. Corticosteroid injections, decreased thickness at follow up. Br J Sports Med. 2004;38(1):8–11.
eccentric decline squat training and heavy slow resistance training in 86. Drew BT, Smith TO, Littlewood C, Sturrock B. Do structural
patellar tendinopathy. Scand J Med Sci Sports. 2009;19(6):790–802. changes (eg, collagen/matrix) explain the response to therapeutic
70. Kingma JJ, de Knikker R, Wittink H, Takken T. Eccentric overload exercises in tendinopathy: a systematic review. Br J Sports Med.
training in patients with chronic Achilles tendinopathy: a systematic 2014;48(12):966–972.
review. Br J Sports Med. 2007;41(6):e3. 87. Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer
71. Magnussen RA, Dunn WR, Thomson AB. Nonoperative treatment M. Lack of tissue renewal in human adult Achilles tendon is
of midportion Achilles tendinopathy: a systematic review. Clin J revealed by nuclear bomb 14C. FASEB J. 2013;27(5):2074–2079.
Sport Med. 2009;19(1):54–64. 88. Kongsgaard M, Reitelseder S, Pedersen TG, et al. Region specific
72. Rowe V, Hemmings S, Barton C, Malliaras P, Maffulli N, patellar tendon hypertrophy in humans following resistance training.
Morrissey D. Conservative management of midportion Achilles Acta Physiol (Oxf). 2007;191(2):111–121.
tendinopathy: a mixed methods study integrating systematic review 89. Seynnes OR, Erskine RM, Maganaris CN, et al. Training-induced
and clinical reasoning. Sports Med. 2012;42(11):941–967. changes in structural and mechanical properties of the patellar
73. Sussmilch-Leitch SP, Collins NJ, Bialocerkowski AE, Warden SJ, tendon are related to muscle hypertrophy but not to strength gains. J
Crossley KM. Physical therapies for Achilles tendinopathy: systematic Appl Physiol (1985). 2009;107(2):523–530.
review and meta-analysis. J Foot Ankle Res. 2012;5(1):15. 90. Bohm S, Mersmann F, Arampatzis A. Human tendon adaptation in
74. Habets B, van Cingel RE. Eccentric exercise training in chronic response to mechanical loading: a systematic review and meta-
mid-portion Achilles tendinopathy: a systematic review on different analysis of exercise intervention studies on healthy adults. Sports
protocols. Scand J Med Sci Sports. 2015;25(1):3–15. Med. 2015;1(1):7.

Address correspondence to Seán McAuliffe, PhD, BSc, Aspetar Orthopaedic and Sports Medicine Hospital, Aspire Zone, Doha, Qatar,
29222. Address e-mail to [email protected].

900 Volume 54  Number 8  August 2019

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