Potential risk factors leading to tendinopathy

Abstract

Tendinopathy has a multifactorial etiology that is not well understood. Risk factors are often separated into extrinsic (those acting on the body) and intrinsic groups (those acting from within the body). In this narrative review, we will separate potential risk factors into 1) load-related (extrinsic); 2) biomechanical factors (intrinsic); and 3) other individual factors such as systemic factors (intrinsic). Too much load is clearly linked to tendinopathy, but there appears to be large variation in how much load individuals can endure before developing tendinopathy. Less active people also suffer tendinopathy, suggesting that the effect of load is likely to be moderated by intrinsic factors. These individual intrinsic factors are likely to reduce tolerance or capacity to withstand load. This narrative review will provide a brief overview of key potential risk factors and mechanisms, as well as limitations in the current literature.

Full text

Apunts Med Esport. 2017;52(194):71---77
www.apunts/org
REVIEW
Potential risk factors leading to tendinopathy
Peter Malliarasa,∗, Seth O’Neillb
aMonash University, Department of Physiotherapy, Melbourne, Australia
bUniversity of Leicester, Department of Medical and Social Care Education, Leicester, UK
Received 19 June 2017; accepted 22 June 2017
Available online 10 July 2017
KEYWORDS
Tendinopathy;
Etiology;
Risk factors;
Load;
Biomechanics;
Prevention
Abstract Tendinopathy has a multifactorial etiology that is not well understood. Risk factors
are often separated into extrinsic (those acting on the body) and intrinsic groups (those acting
from within the body). In this narrative review, we will separate potential risk factors into 1)
load-related (extrinsic); 2) biomechanical factors (intrinsic); and 3) other individual factors such
as systemic factors (intrinsic). Too much load is clearly linked to tendinopathy, but there appears
to be large variation in how much load individuals can endure before developing tendinopathy.
Less active people also suffer tendinopathy, suggesting that the effect of load is likely to be
moderated by intrinsic factors. These individual intrinsic factors are likely to reduce tolerance
or capacity to withstand load. This narrative review will provide a brief overview of key potential
risk factors and mechanisms, as well as limitations in the current literature.
© 2017 Published by Elsevier Espa˜
na, S.L.U. on behalf of Consell Catal`
a de l’Esport. Generalitat
de Catalunya.
PALABRAS CLAVE
Tendinopatía;
Etiología;
Factores de riesgo;
Carga;
Biomecánica;
Prevención
Factores potenciales de riesgo que conducen a la tendinopatía
Resumen La tendinopatía tiene una etiología multifactorial que no es bien conocida. Los
factores de riesgo a menudo se dividen en extrínsecos (los que actúan sobre el cuerpo) e
intrínsecos (los que actúan desde dentro del cuerpo). En esta revisión descriptiva clasificamos
los factores de riesgo potenciales en: 1) factores relacionados con la carga (extrínsecos); 2) fac-
tores biomecánicos (intrínsecos), y 3) otros factores individuales, como los factores sistémicos
(intrínsecos). Una carga excesiva está claramente relacionada con la tendinopatía, pero parece
que existe una gran diferencia en la cantidad de carga que los individuos pueden soportar antes
de desarrollar una tendinopatía. Las personas menos activas también sufren tendinopatía, lo
que sugiere que es probable que el efecto de la carga esté mediado por factores intrínsecos. Es
∗Corresponding author.
E-mail address: peter.malliaras@monash.edu ( P. Malliaras).
http://dx.doi.org/10.1016/j.apunts.2017.06.001
1886-6581/© 2017 Published by Elsevier Espa˜
na, S.L.U. on behalf of Consell Catal`
a de l’Esport. Generalitat de Catalunya.
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72 P. Malliaras, S. O’Neill
probable que estos factores intrínsecos individuales reduzcan la tolerancia o la capacidad de
soportar la carga. Esta revisión descriptiva ofrece un breve resumen de los principales factores
de riesgo y mecanismos, así como las limitaciones en la literatura actual.
© 2017 Publicado por Elsevier Espa˜
na, S.L.U. en nombre de Consell Catal`
a de l’Esport. Gener-
alitat de Catalunya.
Load
Stretch shorten cycle loads
In the lower limb, repetitive stretch-shortening cycles
(SSC) of the muscle-tendon unit (e.g. walking and run-
ning for Achilles tendinopathy or jumping for patellar
tendinopathy)1,2 is associated with tendinopathy. During SSC
there is energy storage through elastic lengthening of the
tendon and subsequent release of some of the stored energy
to reduce the energy cost of locomotion.3,4 In the Achilles-
calf there is energy storage in terminal midstance and
subsequently this energy contributes to positive work in toe
off of walking and running.2
The magnitude of tendon load can be quite high during
SSC activities. For example, Achilles tendon load is reported
to be 6 --- 8 times bodyweight in running5,6 and as high as
8---10 times bodyweight in submaximal hopping.7The mag-
nitude of tendon load is often lower with slow and heavy
contractions that are commonly used in rehabilitation (e.g.
heavy slow resistance training or eccentric training). Even
during a maximal isometric planterflexion contraction load
is about of a third to half (3.5 times bodyweight) of that
during hopping.8Although it seems that higher load is not
always a distinguishing feature between SSC and slow and
heavy loads. Patellar tendon load during loaded squatting
(4.78 bodyweights) is similar to load during a stop jump such
as a spike jump take off (5.17 bodyweights).9,10 However, the
tendon strain rate is much lower during the squatting task
(1---2 bodyweights/second) than during the stop jump task
(almost 40 bodyweights per second). The tendon strain rate
may explain why tendinopathy is associated with repetitive
SSC rather than slow and heavy loads.11
Compression
Compression has been suggested to play a part in most
insertional tendinopathies, or enthesopathies.12 Benjamin
et al.13 described a specialized tendon---bone junction, ‘the
enthesis organ’, that functions to reduce load concentra-
tion at the enthesis. A bony prominence, and at some sites
bursa adjacent to the enthesis, have a role in absorbing
and dispersing enthesis loads thereby limiting stress concen-
tration at the tendon---bone junction. Tendons adapt to the
increased compressive loads at the enthesis with increased
fibrocartilage, larger water-binding proteoglycans and type
II collagen.14 Ground substance accumulation is a feature
of insertional tendinopathy which has been suggested to be
a response to compressive load.12 The pathology has been
localized to the side of the tendon adjacent to the bone,
which also suggests compressive loads may be implicated.14
Soslowsky et al.15 investigated the effect of compressive
and tensile loads in isolation or combination (downhill run-
ning) on rat suprasinatus tendons. Their conclusions were
that a compressive load alone did not lead to reduced
mechanical properties, but a combination of compressive
and tensile load was more damaging than tensile load alone.
For insertional tendinopathies reducing enthesis compres-
sion is suggested to be an important aspect of prevention
and management.12 For example, in the case of the Achilles
this can be achieved by using a heel wedge/lift.
Intratendinous loading patterns
Tensile stress may not be uniform throughout a tendon.
Studies investigating cadavers,16 optic fibers in vivo17 and
mathematical modeling18 have found greater tensile strain
in the posterior compared with the anterior side of the
patellar tendon. This contrasts to Almekinders et al.19 who
found reduced strain in the posterior tendon in a cadaver
study. Despite inconsistencies, these studies demonstrate
different strain gradients or ‘stress shielding’ of part of
the tendon may have a role in the development of patel-
lar tendinopathy.20 Similarly, in the Achilles tendon, there is
emerging evidence from imaging studies using speckle track-
ing that the tendon does not strain uniformly under load.21
The implications for the development of tendinopathy and
rehabilitation (e.g. specific loading for certain parts of the
tendon) are so far unknown.
Change in load
The most common cause for tendinopathy is described as
‘‘training errors’’. This is an ambiguous term, but is nor-
mally considered to encompass any alterations in physical
load on the tendon.22 Primarily, this involves fluctuations
in intensity, frequency or duration of exercise, although it
may be components of all three. Returning to training after
a short break, e.g. after a holiday, is an example of a training
error involving sudden change in load. The break in exercise
is thought to lead to deconditioning, resulting in tendinopa-
thy on a return to normal load. This is often evidenced in
patients who misguidedly go through periods of rest to settle
the tendon and then return to normal loading immediately,
inevitably re-triggering symptoms.
Load management has recently been extensively investi-
gated by Gabbett and colleagues.23 They have demonstrated
a relationship between chronic workload rates (exercise lev-
els over the proceeding 4 week period) and the acute rates
(that week, although, to date, this ratio has not been exten-
sively investigated in relation to tendinopathy).24 Clinically,
it is important to ask about change in energy storage type
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Potential risk factors leading to tendinopathy 73
loads that may contribute to tendinopathy and reduce these
in the short term (load management) if pain is significant and
worsening for more than 24 h after performing these types
of activities.11
Load parameters
Training hours per week is associated with patellar tendon
pain (e.g. 25, 26) and greater running volume with Achilles
tendinopathy,27 suggesting excessive duration or volume is
associated with tendon injury. McCrory et al.28 found that a
higher training pace (intensity) was associated with Achilles
tendinopathy in endurance runners. Repeating loading too
often (frequency) may also be important. Four or more vol-
leyball sessions per week was associated with a doubling of
the prevalence of patellar tendon pain.29,30 This fits with
evidence that intense loading (e.g. 3 h run, 1 h of repet-
itive kicking) results in net collagen degradation for up
to 36 h.31 Repeated intense loading (i.e. repeated stretch
shorten cycle) without sufficient recovery time (i.e. at least
a rest day between sessions) may be a risk factor for tendon
pathology. It should be made clear, however, that factors
such as training hours per week and sessions per week are
not consistently associated with tendinopathy in the lit-
erature. This may be explained by confounders, including
change in load.
How does load lead to pathology?
How energy storage and compressive loads may lead to
tendon pathology is largely unknown. The current body
of evidence suggests the pathogenesis of tendinopathy
involves a change in tissue homeostasis. Homeostasis is nor-
mally maintained by the tendon cells (tenocytes), which
control tendon protein synthesis through various chemi-
cal messengers. Tendon matrix is directly influenced by
the activity of tenocytes. In a normal Achilles tendon we
expect to find a change in the collagen structure to fibro-
cartilage at zones that undergo high compressive loads,
this is an example of the capacity of tenocytes to respond
to different loads.32 Tendinopathy is likely to involve a
loss of homeostasis within the tendon due to excessive
loading (e.g. intensity, frequency, duration) and insuffi-
cient recovery/repair of the tendon.31 Changes in signaling
of cytokines, inflammatory factors, matrix regulator and
the stress-activated factors (e.g. TGFb-1, IGF, VEGF, sub-
stance P, TNFa, MMP’s, nitric oxide) may be involved in
loss of tendon homestasis.33,34 Various systemic factors may
influence repair rates whilst extrinsic factors and biome-
chanical factors are likely to influence the stress on the
tissue.
Biomechanics
Individual biomechanics, including movement kinetics and
kinematics, foot posture, flexibility, neuromuscular capac-
ity and structural anatomy may influence tendinopathy risk.
Horizontal or ‘stop’ jump landing is associated with greater
patellar tendon force than vertical landing.35 Further, par-
ticipants with asymptomatic patellar tendon pathology
landed in greater knee flexion and had a stiffer knee strat-
egy in stop jump landing than their counterparts with normal
patellar tendons.36 Asymptomatic pathology is considered a
useful model to investigate movement patterns that may
increase risk of pain. Given patellar tendon forces were
similar between the groups, the authors suggest that the
landing strategy of the pathology group may involve greater
patellar tendon shear forces. Azevedo et al.37 demonstrated
a stiffer knee strategy (reduced knee flexion from initial
contact to heel strike) among runners with Achilles tendon
pain. It is possible that this kinematic pattern is a protective
compensation to reduce Achilles tendon load. This exam-
ple highlights the limitations of cross sectional research
design where associated factors may develop secondary to
pain.
Foot posture and function (dynamic pronation) has been
proposed as a risk factor for lower limb tendinopathy,27
although there is conflicting literature.38 Patellar tendinopa-
thy has been associated with both a higher39 and lower26
static arch height. There is also limited or conflicting evi-
dence linking plantar heel pain with static and dynamic
foot posture.40 A recent systematic review identified limited
evidence for a change in plantar pressures in Achilles ten-
don pain during running gait, indicating a more lateral foot
roll over following heel strike.41,42 A lateral foot roll over
may indicate compromised windlass function but may also
be a secondary adaptation to reduce Achilles load. Murley
et al.43 found that a pronated foot posture was associated
reduced Achilles tendon cross sectional area among partici-
pants without pain, indicating that foot posture may impact
on tissue loading and development throughout life, poten-
tially increasing injury risk.
Muscle flexibility (e.g. hamstring) and joint range of
motion (e.g. ankle dorsiflexion) has received much inter-
est, probably more so than any other factors. Unfortunately,
the results are often conflicting, which leaves the clini-
cian with a dilemma in attempting to manage and prevent
injury. For example, both increased44 and decreased ankle
dorsiflexion45,46 range of motion have been associated with
the development of Achilles tendinopathy in prospective
studies. Patellar tendinopathy has been associated with both
increased26 and decreased47 hamstring flexibility. Clinically,
it may be important to consider addressing extremes of
range of motions of these joints/muscles where this is pos-
sible.
Although suggested to be a common risk factor, few
studies have investigated the link between neuromuscular
capacity and tendinopathy.48---50 Both cross-sectional47,51 and
prospective work has found that greater jump height is asso-
ciated with patellar tendinopathy and this is thought to
relate to greater thigh strength.52 Seemingly in contrast,
Crossley et al.26 found that patellar tendinopathy was asso-
ciated with reduced thigh strength, which may be explained
by change in neuromuscular function secondary to pain (long
or short term). Plantarflexor muscle weakness has been
associated with Achilles tendinopathy in cross-sectional
studies28,53 this has often been thought to be a direct
consequence of the pain. However, more recently Mahieu
et al.44 found that plantarflexor torque was 85% sensitive at
predicting those who went on to develop Achilles tendinopa-
thy, suggesting muscle weakness may be a causative
factor.
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74 P. Malliaras, S. O’Neill
Other individual factors
Multiple systemic factors have been linked with tendinopa-
thy including: age, lipid levels, adiposity and genetics. These
have been extensively reviewed elsewhere.34 Systemic risk
factors are thought to reduce the capacity of the tissue to
tolerate load, gradually altering tendon capacity so that an
extra walk, a quick dash across the road, or a day spent
gardening may be sufficient to overload the tendon trigger-
ing symptoms. Therefore, these factors may be particularly
relevant among patients who are not performing regular
high intensity SSC loads. They may also explain, along with
biomechanical factors, why not all athletes exposed to the
same loads develop tendinopathy. Systemic factors need to
be considered in clinical practice, as this population may be
more difficult to manage, respond less favorable to load-
based interventions and benefit from additional adjunct
interventions (e.g. aerobic exercise).
The exact mechanism by which systemic factors influ-
ence tendinopathy risk is largely unknown. For example,
increased age may be associated with change in tendon
cellular activity, mechanical properties (through glycation)
as well as muscle function,54 all of which may influence
tendinopathy risk. Adiposity is thought to increase the
level of pro-inflammatory cytokines in circulation and these
chemical messengers are thought to influence the tendon
matrix through various effects on tenocytes.55 An alter-
nate mechanism is that adiposity is associated with greater
bodyweight (which has also been linked to tendinopathy)
and increased tendon load. Malliaras et al.56 found that
waist girth was a stronger predictor of patellar tendinopa-
thy than body mass in a multivariate model. This highlights
that the link between anthropometry and tendinopathy is
more complex than purely increased tendon load and the
importance of multivariate models delineating confounding
factors.
We know that previous injury appears to be an impor-
tant predictor of tendinopathy. The reason for this has not
been established, but is thought to link to changes in tis-
sue resilience and/or the neuromuscular system22 reducing
the ability to withstand the demands of physical activity.48,57
These adaptations reduce the coping ability of the mus-
cle tendon unit. In such cases, continued loading can take
the tissue past the point of homeostasis, leading to tis-
sue breakdown and symptom onset.58 Obviously, we cannot
alter the fact that the patient has sustained a previous
injury or tendinopathy, but we can reduce the likelihood of
such issues in the first place. A recent meta-analysis pooled
data from 26,610 participants and showed that strength
training reduced overuse injuries by 50% and acute injuries
such as sprains and tears by 33%.59 This suggests that our
best approach is to ensure that all subjects at high risk of
tendinopathy include strength training regularly in order to
reduce risk. For example, in Achilles tendinopathy, target-
ing those with poor plantarflexor strength is likely to reduce
the risk of tendinopathy.
Limitations of the literature
A major limitation of the literature is that most studies use
a cross-sectional design which does not allow a temporal
sequence between exposure to the risk factor and develop-
ment of tendinopathy to be established. Thereby, no causal
inferences can be made. It is likely that changes in kine-
matics and neuromuscular function may be secondary to
pain.60 In managing tendinopathy, it may still be necessary
to address these changes that may be secondary to pain in
order to restore optimal function and tendon loading.
Another consideration is that most studies investigate the
relationship between potential risk factors and the onset
or presence of pain (e.g. 26, 45). Pathology is thought
to precede pain and a recent systemic review concluded
that pathology is a risk factor for the onset of tendon
pain in Achilles and patellar tendinopathy.61 Many factors
such as load may influence the risk of both pathology
and pain. Some factors may increase the risk of develop-
ing pain among people with asymptomatic tendinopathy.
These may include cognitive and emotional factors such as
anxiety and maladaptive beliefs about pain that lead to fear-
avoidance behaviors.62 Understanding factors that influence
pain is important in order to prevent and manage painful
tendinopathy.
Some authors have suggested that unilateral and bilat-
eral tendinopathy have a different etiology.63 For example,
Crossley et al.26 found that hamstring flexibility was
increased in unilateral but not bilateral patellar tendinopa-
thy. What is becoming increasingly clear is that bilateral
tendinopathy is common. There may be several explanations
for this, including biomechanical load affecting both sides of
the body, systemic factors that are described above, or even
bilateral nervous system involvement.64---66 More evidence is
needed to understand the potentially different etiology of
unilateral and bilateral tendinopathy.
Implications for prevention
There are four stages to injury prevention outlined by van
Mechelen et al.67 These include 1) establishing the extent of
the injury problem; 2) establishing the etiology and mecha-
nisms of injury; 3) introducing preventative measures; and
4) assessing the effectiveness of these measures by re-
assessing the extent of the problem. There are several
studies that investigate potential risk factors for tendinopa-
thy (stage 2) as outlined in this review, but very few
that evaluate preventative interventions (stage 3). In any
case, targeting preventive interventions toward individuals
deemed to be at greater risk of injury based on screening
to identify risk factors has been challenged.68 Most risk fac-
tors are not strongly associated with injury so do not clearly
delineate individuals who will develop injury from those who
do not. Therefore, preventative interventions may be more
effective if applied across an entire cohort rather than solely
among individuals deemed to be at greater risk of injury. In
summary, risk factor knowledge is important and may inform
injury prevention interventions (e.g. calf weakness may be
a risk factor for Achilles pain suggesting calf loading may
be an effective preventative intervention). However, it is
important to progress to stage three of the injury prevention
model and evaluate whether changing risk factors influences
injury risk.
Only two randomized trials have evaluated preventative
exercise interventions for tendinopathy. Kraemer et al.69
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Potential risk factors leading to tendinopathy 75
found that a neuromuscular conditioning program reduced
the risk of Achilles and patellar tendinopathy development
among female soccer players. However, Fredberg et al.53
investigated whether eccentric training for the Achilles and
patellar tendons performed during the season reduced injury
risk among soccer players. There was no change in Achilles
tendinopathy risk but an increase in patellar tendon pain
among those with asymptomatic patellar tendon pathol-
ogy at baseline. This suggests the addition of rehabilitation
loads to sporting load for people with existing asymptomatic
patellar tendon pathology may increase the risk of pain. We
need to know more about effective rehabilitation strategies
to prevent tendinopathy and in the meantime load monitor-
ing (e.g. acute to chronic workload) is critical.
Conclusion
Understanding risk factors and mechanisms is critical for
prevention and management of tendinopathy. Change in
SSC loads seem to be related to the onset of tendinopa-
thy, particularly in the lower limb and monitoring change
in these loads is important for tendinopathy prevention.
Multiple biomechanical and neuromuscular factors have
been identified but the literature is limited and many
neuromuscular changes from cross-sectional studies may
have arisen after the onset of pain. The current chal-
lenge to researchers is to identify prospective risk factors
and then investigate whether modifying these factors
reduces injury risk in cohorts of individuals at risk of
tendinopathy.67
Conflicts of interest
Authors declare that they don’t have any conflict of inter-
ests.
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