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Selection criteria
INTRODUCTION Selection criteria were developed prior to searching to
Hamstring strain injuries (HSIs) are the most common maintain objectivity when identifying studies for inclu-
non-contact injuries in Australian rules football,15 sion. To address the aims, included papers had to:
soccer,610 rugby union,1114 track and eld1517 and Assess at least one parameter of hamstring
American football.18 HSIs result in time away from strength (maximum strength, associated strength
competition,9 nancial burden9 19 and impaired per- ratios and angle of peak torque) or exibility in
formance on return to competition.20 humans with a prior HSI within 24 months
Further to this, recurrent HSI often leads to a from the time of testing;
greater severity of injury than the initial insult.10 14 Have control data for comparison (whether it
The most commonly cited risk factor for future HSI was a contralateral uninjured leg or an uninjured
To cite: Maniar N, is a previous HSI.2124 The high recurrence rates of group);
Shield AJ, Williams MD, HSI10 14 are proposed to result from incomplete Have the full-text journal article in English
et al. Br J Sports Med recovery and/or inadequate rehabilitation25 26 available (excluding reviews, conference
2016;50:909920. because of pressure for early return to play at the abstracts, case studies/series);
Maniar N, et al. Br J Sports Med 2016;50:909920. doi:10.1136/bjsports-2015-095311 1 of 14
Review
Strong: two or more studies of a high quality and generally con- RESULTS
sistent ndings (75% of studies showing consistent results); Search results
Moderate: one high-quality study and/or two or more low- The search strategy consisted of six steps (gure 1). The initial
quality studies and generally consistent ndings (75% of search yielded 7805 items (Cochrane Library=131;
studies showing consistent results); PubMed=2407, CINAHL=604; SPORTDiscus=640; Web of
Limited: one low-quality study; Science=1049; EMBASE=2974) from all databases. After
Conicting: inconsistent ndings (<75% of studies showing duplicates were removed, 4306 items remained. Title and
consistent results); abstract screening resulted in 92 remaining articles, reference list
None: no supportive ndings in the literature. hand searching and citation tracking resulted in the addition of
A high-quality study was dened as a risk-of-bias assessment six articles. Independent application of the selection criteria
score of 70%, whereas a low-quality study had a risk of bias yielded 28 articles to be included in the review, 22 of which
assessment score of <70%.57 were included in meta-analysis.
Table 2 Itemised scoring of study quality using a modified (see online supplementary table S1) Downs and Black checklist (50)
First author, year 1 2 3 5 6 7 10 11 12 16 18 20 21 25 27 28 29 Total Per cent Quality
Table 3 Best evidence synthesis data for all major categories of outcome variables assessed in individuals with a prior hamstring strain injury
not included in the meta-analysis.
Consistency (%)
Figure 2 Forest plot of concentric strength measured at (A) 60/s, (B) 180/s and (C) 300/s.
Best evidence synthesis. Of the dynamic strength variables strength in the previously injured hamstrings. Concentric strength
which were not included in the meta-analysis, one (seated isokin- at 270/s in a seated position42 had limited evidence and concentric
etic at 240/s)36 37 67 had moderate evidence for a decrease in strength at 60/s in a prone position49 had no supporting evidence.
Maniar N, et al. Br J Sports Med 2016;50:909920. doi:10.1136/bjsports-2015-095311 5 of 14
Review
Eccentric strength signicant effect for time since injury for isometric strength
Data for all studies which examined eccentric strength can be (intercept 0.92, p=0.002; coefcient 0.003, p=0.292).
found in online supplementary table S3. Best evidence synthesis. One study68 assessed isometric strength
Meta-analysis. Eccentric strength measured during the Nordic in a short muscle length (hip 0, knee 90). This study did not stat-
hamstring exercise34 41 64 and isokinetically at 6029 48 62 63 70 istically test for differences between muscles, but based on effect
and 180/s29 70 were included in the meta-analysis. Signicant size and CIs, isometric strength was reduced at the initial evalu-
decits in previously injured legs were found for eccentric ation (effect size 0.74; 95% CI 1.07 to 0.41) and at the
strength measured via the Nordic hamstring exercise (effect size 7-day follow-up (effect size 0.39; 95% CI 0.71 to 0.07),
0.39; 95% CI 0.77 to 0.00; I2 0%), but not for any other but not at the 26-week follow-up (effect size 0.12; 95% CI
method (gure 3). 0.45 to 0.20).
Best evidence synthesis. Eccentric isokinetic strength measured
at 3036 37 42 61 and 120/s36 37 had moderate evidence, indicat-
ing lower strength in previously injured hamstrings, whereas H:Q torque ratio
measures at 23042 and 300/s39 had limited evidence. The Data for all studies which examined H:Q ratios can be found in
measurement of eccentric strength at 60/s in a prone position49 online supplementary tables S5 and S6.
had no supporting evidence. Meta-analysis. The conventional H:Q ratio, whereby peak
torque of each muscle group is assessed during concentric iso-
Isometric strength kinetic contraction, was assessed at 60:60,36 37 40 43 48 61 70 71
Data for all studies which examined isometric strength can be 180:180,40 61 70 71 240:24036 37 and 300:300/s39 40 71 (gure 6).
found in online supplementary table S4. A statistically signicant small effect for a lower conventional H:
Meta-analysis. Isometric strength measured at long muscle Q ratio was found in previously injured legs compared with the
lengths (hip 0; knee 015) was included in the uninjured contralateral legs at 60:60 (effect size 0.32; 95% CI
meta-analysis.28 34 68 Measures were taken at multiple time 0.54 to 0.11; I2=0%) and 240:240/s (effect size 0.43;
points (<7, 714, 21, 42 and >180 days) postinjury; thus, sub- 95% CI 0.83 to 0.03; I2 0%), but not at 180:180 and
groups were analysed (gure 4) and meta-regression was per- 300:300/s. Meta-analysis of the functional H:Q (fH:Q),
formed. A large effect for lower long-length isometric strength whereby the hamstring group is assessed eccentrically, but the
was statistically signicant in previously injured legs compared quadricep group is assessed concentrically, included isokinetic
with the uninjured contralateral legs <7 days postinjury (effect velocities 30:24036 37 67 and 60:60/s43 48 63 70 (gure 7). A
size 1.72; 95% CI 3.43 to 0.00; I2 91%), but not at any large effect size for a lower fH:Q ratio was found in previously
other time point. Meta-regression analysis (gure 5) revealed no injured legs at 30:240/s (effect size 0.88; 95% CI 1.27 to
Figure 3 Forest plot of eccentric strength measured at (A) 60/s, (B) 180/s and (C) during the Nordic hamstring exercise. Note that one study70
had two subgroups: Doherty 2012a, Division I athletes; Doherty 2012b, Division III athletes.
Figure 4 Forest plot of isometric strength assessed at (A) <7 days postinjury, (B) 714 days postinjury, (C) 21 days postinjury, (D) 42 days
postinjury and (E) >180 days postinjury. Note that one study28 had two subgroups: Askling 2006a, Sprinters; Askling 2006b, Dancers.
0.48; I2 0%), but there were no signicant differences between Angle of peak torque
injured and uninjured legs at 60:60/s. Data for all studies which examined optimal angle of peak
Best evidence synthesis. One study which examined H:Q torque can be found in online supplementary table S7.
(60:60/s)49 was not included in the meta-analysis owing to the Meta-analysis. The optimal angle of peak torque (concentric
prone and supine position in which knee exor and quadricep 60/s) had sufcient data61 66 67 for meta-analysis. No signicant dif-
strength, respectively, were assessed. This study found no signi- ferences between injured and uninjured legs were found (gure 8).
cant difference between injured and uninjured legs. No support- Best evidence synthesis. Limited evidence was found for the
ing evidence was found for the fH:Q strength ratio at eccentric angle of peak torque to occur at signicantly shorter
180:180,70 30:60 and 30:180/s,61 and limited evidence was muscle lengths in the injured legs compared with the uninjured
found for 300:300/s.39 The eccentric H:Q, whereby both knee contralateral legs at 30/s.61 No differences were found for angle of
exor and quadricep strength are assessed via eccentric contrac- peak torque between legs/groups at 24067 and 300/s39 concentric-
tions, was assessed isokinetically in prone/supine49 position. ally or 300/s39 eccentrically measured angle of peak torque.
This study found no differences between previously injured and
uninjured legs. Limited evidence was found for eccentric knee Flexibility
exor torque to concentric hip exor torque ratio decits in Passive straight leg raise
previously injured legs (effect size 0.9) compared with unin- Data for all studies which examined the passive straight leg raise
jured contralateral legs.39 can be found in online supplementary table S8.
Maniar N, et al. Br J Sports Med 2016;50:909920. doi:10.1136/bjsports-2015-095311 7 of 14
Review
Figure 5 Meta-regression plot (with 95% CI) for isometric strength. Passive knee extension
Intercept 0.92, p=0.002; coefcient 0.003, p=0.292. Data for all studies which examined the passive knee extension
can be found in online supplementary table S9.
Meta-analysis. No signicant differences were found for the
Meta-analysis. Quantitative analysis of the passive straight leg passive knee extension measure at either time point subgroup
raise26 28 62 68 revealed signicantly reduced range of motion in analysed (<10 and 2030 days postinjury; gure 11A,B).
previously injured legs compared with the uninjured contralat- Best evidence synthesis. A subset of the passive knee extension
eral leg. A large effect was found within 10 days (effect size (insufcient data for subgroup meta-analysis, unable to be
Figure 6 Forest plot of conventional H:Q ratio assessed at (A) 60:60/s, (B) 180:180/s, (C) 240:240/s and (D) 300:300/s. Note that one study70
had two subgroups: Doherty 2012a, Division I athletes; Doherty 2012b, Division III athletes. H:Q, hamstring to quadricep.
8 of 14 Maniar N, et al. Br J Sports Med 2016;50:909920. doi:10.1136/bjsports-2015-095311
Review
Figure 7 Forest plot of the fH:Q ratio assessed at (A) 30:240/s and (B) 60:60/s. Note that one study70 had two subgroups: Doherty 2012a,
Division I athletes; Doherty 2012b, Division III athletes. fH:Q, functional hamstring to quadricep.
pooled with acute data) showed conicting evidence across the DISCUSSION
three studies46 47 49 that conducted this assessment post return Our systematic review revealed that after HSI, isometric strength
to play. and passive straight leg raise decits normalised within 20
50 days. Decits at or after return to play, if they did exist, mani-
fested during dynamic strength measures (eccentric and concen-
Active knee extension
tric strength and their associated H:Q strength ratios).
Data for all studies which examined the active knee extension
We only included research articles that contained data from
can be found in online supplementary table S9.
participants who had previously sustained a HSI (between 2 and
Meta-analysis. No signicant differences were found for the
690 days prior). As a result, we cannot determine whether the
active knee extension measure at either time point subgroup ana-
reported decits were the cause of injury or the result of injury.
lysed (<10, 1030 and >100 days postinjury; gure 11CE).
Given the increased risk of future HSI in those with an injury
history,2124 the characteristics that exist in these legs should be
Active straight leg raise given consideration by the clinicians responsible for rehabilita-
Data for all studies which examined the active straight leg raise tion and clearance to return to play.
can be found in online supplementary table S8.
Best evidence synthesis. Conicting evidence was found for
Strength and exibility decits after hamstring injury
decits in the active straight leg raise.45 65 Of note, the one
Conventional rehabilitation practice traditionally focuses on
study65 which did nd decits in previously injured legs per-
restoring isometric strength and range of motion.72 The
formed the active straight leg raise in a rapid manner (Askling-H
meta-analysis revealed that decits in long length (hip 0; knee
test), and as such this study could not be appropriately pooled
015) isometric strength and the passive straight leg raise are
with the other data for meta-analysis purposes.
resolved 2050 days postinjury. This provides support for the
use of the passive straight leg raise and isometric strength mea-
Sit and reach sures during rehabilitation.72 Furthermore, decits in isometric
Best evidence synthesis. No evidence for differences in the sit strength and range of motion (as measured by the active knee
and reach was found between healthy and previously injured extension test) just after return to play are independent predic-
participants.48 63 tors of reinjury,73 suggesting that these variables likely also have
Figure 8 Forest plot for angle of peak torque assessed during 60/s concentric contraction.
Figure 9 Forest plot of the passive straight leg raise at (A) <10 days postinjury, (B) 1020 days postinjury, (C) 2030 days postinjury and (D) >40 days
postinjury. Note that two studies26 28 had two subgroups: Askling 2006a, Sprinters; Askling 2006b, Dancers; Silder 2013a, progressive agility and trunk
stabilisation (PATS) rehabilitation protocol; Silder 2013b, progressive running and eccentric strengthening (PRES) rehabilitation protocol.
value in criterion-based rehabilitation progressions. However, likelihood that the demands of high-force musculotendinous
where evidence of decits were found beyond return to play, lengthening, such as during the terminal swing phase of running,
these were during measures of dynamic strength. exceed the mechanical limits of the tissue.74 It may be that lower
The evidence supporting decits in eccentric strength in those eccentric strength in previously injured hamstrings is at least partly
with prior HSI is mixed.29 34 36 37 39 4143 48 63 64 70 Lower responsible for the greater risk of recurrent hamstring strain.75
levels of eccentric hamstring strength are proposed to increase the Other measures of dynamic strength, including concentric
strength29 33 36 37 40 48 6163 66 67 71 and both
conventional33 36 37 39 40 43 48 61 66 70 71 and
functional36 37 39 43 48 61 63 67 70 H:Q strength ratios, also show
conicting ndings, with measures at some testing velocities
showing lower strength in previously injured legs, but others
showing no differences. The reasons for these discrepancies are
unclear, but it may be due to inherent differences in groups
studied and/or methodological issues. For example, studies which
included females tended to observe slightly higher strength in pre-
viously injured legs.70 71 Insufcient data were available to assess
this observation via regression analysis; thus, more research is
needed to investigate any potential gender-specic responses to
HSI. The particulars of the rehabilitation performed could also
Figure 10 Meta-regression plot (with 95% CI) for the passive straight explain the disparity, as differing rehabilitation strategies would
leg raise. Intercept 0.81, p<0.0001; coefcient 0.006, p=0.019. result in differing adaptations. Rehabilitation was rarely controlled
10 of 14 Maniar N, et al. Br J Sports Med 2016;50:909920. doi:10.1136/bjsports-2015-095311
Review
Figure 11 Forest plot for the knee extension assessments of range of motion at (A) passive, <10 days postinjury, (B) passive, 2030 days
postinjury, (C) active, <10 days postinjury, (D) active, 1030 days postinjury and (E) active, >100 days postinjury. Note that one study26 had two
subgroups: (A) progressive agility and trunk stabilisation (PATS) rehabilitation protocol; (B) progressive running and eccentric strengthening (PRES)
rehabilitation protocol.
in the included studies, suggesting that more studies should aim to not occur during concentric contractions;29 48 thus, further
control rehabilitation to limit this potential confounder. research is needed to understand why dynamic strength decits
tend to persist beyond return to play.
Mechanisms that may explain long-term dynamic muscle
strength decits Clinical implications
There is the possibility that chronic decit/s in dynamic strength The data presented in this review have implications for practi-
in previously hamstring strain injured legs is a downstream tioners who rehabilitate and return athletes to play following HSIs.
outcome of prolonged neuromuscular inhibition.35 Reduced The supplementary result tables provide practitioners a detailed
activation of previously injured hamstrings has been associated resource of data for almost all strength and exibility measures that
with maximal eccentric contractions,29 30 48 76 particularly at have been assessed in athletes with a prior HSI. These data can be
long muscle lengths.29 48 What remains to be seen, however, is used to compare individual athlete/patient data. It should also
whether or not these decits are associated with increased risk enable practitioners to select measures to monitor in their injured
of injury or reinjury, and what the most appropriate intervention athletes which are known to be in decit despite successful return
is to ameliorate these decits. However, activation decits do to play. The presented evidence justies the use of the passive
Maniar N, et al. Br J Sports Med 2016;50:909920. doi:10.1136/bjsports-2015-095311 11 of 14
Review
straight leg raise and isometric strength measures to monitor pro- acknowledge that the search strategy may not have captured all
gression through rehabilitation, while additional measures of relevant literature. However, reference list searching and cit-
dynamic strength may have more value at and after return to play. ation tracking were also performed to enhance article retrieval.
In addition, the present review would also question the use of
commonly recommended74 77 and employed markers for suc- CONCLUSION
cessful rehabilitation, such as knee exor angle of peak torque. In conclusion, the meta-analysis found that decits in isometric
The use of angle of peak knee exor torque, particularly during strength and exibility (as measured by the passive straight leg raise)
concentric contraction, in athletes with prior HSI has been resolve within 2050 days following HSI. Decits that were present
popularised following the seminal paper;66 however, the beyond return to play were found for dynamic measures of strength
ensuing evidence is generally conicting,33 39 61 67 suggesting (concentric and eccentric strength, and conventional and functional
that the value of this measure should be questioned. H:Q strength ratios). This evidence suggests that clinicians monitor
isometric strength and the passive straight leg raise throughout
Limitations rehabilitation, while dynamic measures of strength may hold more
The primary limitation of this review is that the retrospective value at/after return to play. Furthermore, it may behove clinicians
nature of the data makes it impossible to determine if decits are and patients to continue rehabilitation after return to play.
the cause or result of injury. For example, eccentric strength de-
cits could be the result of uncorrected strength deciency that
may have caused injury, as higher levels of eccentric strength and What are the ndings?
eccentric training are associated with a reduction in new and
recurrent HSI.73 78 79 Furthermore, the majority of the included
studies did not control rehabilitation, and this introduces another
After HSI,
potential source of bias. For example, a study in which partici-
Isometric strength returns to the level of the contralateral
pants focused heavily on eccentric exercise as part of rehabilita-
uninjured leg within 20 days.
tion may show no evidence of signicant eccentric strength
Range of motion measured by the passive straight leg raise
decits post HSI. Consequently, the effect of these interventions
returns to the level of the contralateral uninjured leg within
on strength and exibility outcomes remains an area for future
50 days.
research. Ideally, researchers should control rehabilitation to min-
Lower dynamic strength (concentric, eccentric and associated
imise confounding, and where this is not possible, collect and
strength ratios) in previously injured legs compared with the
report details of rehabilitation protocols. Inconsistent time from
uninjured contralateral legs persists beyond return to play,
injury until testing between studies also introduces bias. We ana-
but this is inconsistent across measurement technique.
lysed data in time bands and performed meta-regression analysis
where possible to assess and adjust for this potential confounder,
but we also acknowledge that this approach was limited by
within-study variability, variability between studies within the How might it impact on clinical practice in the future?
time band subgroups and insufcient data for regression analysis.
Future research should investigate the effect of time since injury Isometric strength and the passive straight leg raise provide
on decits, particularly prior to return to play, as strength and a measure of progression during rehabilitation.
exibility appear to change rapidly during this period. Dynamic strength (concentric/eccentric hamstring strength
One of the difculties of this review was the numerous methods and associated hamstring to quadricep strength ratios) may
employed by different studies to assess a given parameter. For also be helpful in monitoring progress through rehabilitation
strength testing, it appeared that lower isokinetic velocities (<60/ and return-to-play decisions.
s) were the most sensitive to decits; however, there are insufcient This review adds weight to the argument that rehabilitation
data at higher velocities to draw denitive conclusions. Similarly, a should continue after return to play if the goal is to achieve
number of different measures of exibility (passive26 28 42 65 and symmetry in strength and range of motion.
active45 65 straight leg raise, passive26 46 47 49 and active knee
extension,26 48 sit and reach test48 63) have been assessed in previ-
ously injured athletes, with inconsistent ndings among studies.
Twitter Follow Nirav Maniar @niravmaniar91, Anthony Shield @das_shield,
Indeed, within each variable, the meta-analysis revealed signicant Morgan Williams @drmorgs, Ryan Timmins @ryan_timmins and David Opar
heterogeneity as determined by the I2 statistic in certain measures, @davidopar
particularly in the initial days following injury. Acknowledgements The primary authors position was supported through the
To address these issues as far as possible, we performed sensi- Australian Governments Collaborative Research Networks (CRN) program. The
tivity analysis (see online supplementary table S10) to examine authors would also like to sincerely thank Professor Geraldine Naughton for acting
the inuence of individual studies on effect estimates and hetero- as an independent assessor for the risk-of-bias assessment.
geneity where moderate (30%) heterogeneity57 may have been Contributors NM conducted the search, risk-of-bias and criteria assessments,
present. While high heterogeneity often impairs the validity of extracted the data, performed all analysis and drafted the manuscript. AJS and
MDW contributed to interpretation of results and the manuscript. RGT conducted
synthesised data, the low number of studies in many of these criteria assessments and contributed to the manuscript. DAO conducted risk-of-bias
subgroups precludes condence in the precision in these I2 esti- and criteria assessments and contributed to the interpretation of results and the
mates, suggesting that more studies are needed to properly manuscript.
interpret heterogeneity estimates. These studies should also Funding Australian Governments Collaborative Research Networks (CRN).
take care to accurately describe diagnostic procedures, injury Competing interests DAO and AJS are listed as coinventors on an international
severity and other lower limb injuries likely to confound patent application lled for the experimental device (PCT/AU2012/001041.2012)
results. The data reported in this review may also have limited used in three of the included studies in this review. The authors declare no other
application to female athletes, as majority of the data were competing interests.
obtained from male only or predominately male cohorts. We Provenance and peer review Not commissioned; externally peer reviewed.