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Systematic review

No sign of weakness: a systematic review and meta-­

Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
analysis of hip and calf muscle strength after anterior
cruciate ligament injury
Michael Girdwood ‍ ‍,1 Adam G Culvenor ‍ ‍,1 Brooke Patterson ‍ ‍,2
Melissa Haberfield ‍ ‍,3 Ebonie Kendra Rio,3,4,5 Michael Hedger,6 Kay M Crossley ‍ ‍6

► Additional supplemental ABSTRACT


material is published online Objective We aimed to determine hip and lower-­leg WHAT IS ALREADY KNOWN ON THIS TOPIC
only. To view, please visit the ⇒ Thigh muscle strength deficits are common
journal online (https://​doi.​ muscle strength in people after ACL injury compared with
org/1​ 0.​1136/​bjsports-​2023-​ an uninjured control group (between people) and the after ACL injury, with up to 20% deficits in
107536). uninjured contralateral limb (between limbs). quadriceps and 10% deficits in hamstring
Design Systematic review with meta-­analysis. strength reported at 12 months postsurgery.
1
La Trobe Sport and Exercise ⇒ Hip and calf muscle strength training is often
Data sources MEDLINE, EMBASE, CINAHL, Scopus,
Medicine Research Centre,
School of Allied Health, Human Cochrane CENTRAL and SportDiscus to 28 February added to rehabilitation after ACL reconstruction.
Services and Sport, La Trobe 2023. WHAT THIS STUDY ADDS
University, Bundoora, Victoria, Eligibility criteria Primary ACL injury with mean age
Australia 18–40 years at time of injury. Studies had to measure ⇒ Significant hip or lower-­leg muscle weakness
2
Sport and Exercise Medicine was not found in most planes compared with
Research Centre, La Trobe hip and/or lower-­leg muscle strength quantitatively
(eg, dynamometer) and report muscle strength for the uninjured controls or the uninjured limb in the
University, Melbourne, Victoria,
Australia ACL-­injured limb compared with: (i) an uninjured control first 12 months after ACL reconstruction.
3
La Trobe Sport and Exercise group and/or (ii) the uninjured contralateral limb. Risk of ⇒ Hip abduction strength had the most evidence
Medicine Research Centre, La
bias was assessed according to Cochrane Collaboration (very low certainty), and was not different
Trobe University, Bundoora, between people or between limbs after ACL
Victoria, Australia domains.
4
The Victorian Institute of Sport, Results Twenty-­eight studies were included reconstruction.
Melbourne, Victoria, Australia (n=23 measured strength ≤12 months post-­ACL ⇒ More between-­person comparisons, especially
5
The Australian Ballet, reconstruction). Most examined hip abduction (16 for hip internal rotation, ankle plantarflexion
Melbourne, Victoria, Australia and ankle dorsiflexion are needed to inform
6
La Trobe University, Melbourne, studies), hip extension (12 studies) and hip external
rotation (7 studies) strength. We found no meaningful clinical decision-­making.
Victoria, Australia
difference in muscle strength between people or
Correspondence to between limbs for hip abduction, extension, internal
weakness can persist for up to 20 years post-­ACL
Professor Kay M Crossley, La rotation, flexion or ankle plantarflexion, dorsiflexion
Trobe University, Melbourne, injury3 and may increase the risk of re-­injury and
(estimates ranged from −9% to +9% of comparator).
Victoria, Australia; post-­traumatic osteoarthritis (OA).4 5 The strength
​k.​crossley@​latrobe.​edu.a​ u The only non-­zero differences identified were in hip
of other lower-­limb muscles following ACL injury
adduction (24% stronger on ACL limb (95% CI 8% to
is less clear, despite hip and lower-­leg (calf) muscles
Accepted 28 February 2024 42%)) and hip external rotation strength (12% deficit
playing a critical role when executing most weight-­
on ACL limb (95% CI 6% to 18%)) compared with
bearing daily activities and more complex sporting
uninjured controls at follow-­ups >12 months, however
and athletic tasks.
both results stemmed from only two studies. Certainty of
The hip and calf muscles are integral to knee
evidence was very low for all outcomes and comparisons,
movements, with potential impacts on risk of knee
and drawn primarily from the first year post-­ACL
joint disease. Hip muscle strength is commonly
reconstruction.
impaired in many knee conditions,6 such as
Conclusion Our results do not show widespread or
patellofemoral pain,7 patellar tendinopathy8 and
substantial muscle weakness of the hip and lower-­
non-­traumatic knee OA,9 but consistent causal links
leg muscles after ACL injury, contrasting deficits of
to the development or worsening of knee condi-
10%–20% commonly reported for knee extensors and
tions are not seen.7 Through its direct link to the
flexors. As it is unclear if deficits in hip and lower-­leg
knee via the kinetic chain, the hip complex contrib-
muscle strength resolve with appropriate rehabilitation
utes frontal plane knee stability/control (eg, poten-
or no postinjury or postoperative weakness occurs,
© Author(s) (or their tially reducing dynamic knee valgus)10 11—which
employer(s)) 2024. No
individualised assessment should guide training of hip
if impaired may lead to worsening symptomatic
commercial re-­use. See rights and lower-­leg strength following ACL injury.
and structural outcomes at the knee.12 Adequate
and permissions. Published PROSPERO registration number CRD42020216793.
by BMJ. hip muscle strength may be vital after ACL injury,
where the risk of post-­traumatic OA is significantly
To cite: Girdwood M, higher. Lower hip external rotation strength at 1
Culvenor AG,
Patterson B, et al.
INTRODUCTION year was associated with greater odds of worsening
Br J Sports Med Epub ahead Knee muscle (quadriceps and hamstring) strength knee structural outcomes 5 years after ACL recon-
of print: [please include Day deficits are well-­established after ACL injury and struction (ACLR).13 Better hip muscle strength may
Month Year]. doi:10.1136/ reconstruction surgery and are a key focus of reha- also be linked to better functional performance14—
bjsports-2023-107536 bilitation guidelines.1 2 Quadriceps and hamstring an important benchmark for return to sport and

Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536    1


Systematic review
activity. Similarly, lower-­leg muscles (such as of the calf) may file 2). We searched MEDLINE, EMBASE, CINAHL, Scopus,

Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
impact knee function due to the gastrocnemius’ anatomical Cochrane CENTRAL and SportDiscus from inception to 28
origin being proximal to the knee. Indeed, the calf is emerging February 2023, limiting to humans where possible but with no
as a key contributor to knee joint stability and compression restrictions on language. In addition, we searched OpenGrey, as
forces,11 15 16 with potential implications for future re-­injury and well as checking reference lists of included articles and ahead of
structural outcomes following ACL injury. print sections of key physical therapy, rehabilitation and sports
Several authors have suggested hip muscle weakness might be medicine journals.
a problem requiring treatment after ACL injury,17–20 and reha-
bilitation trials often include hip and calf muscle strengthening Study selection
components.21–24 Yet hip and/or lower-­leg muscle strength are Two authors (MG and either MH or BP) independently screened
not clearly summarised after ACL injury. To inform the planning titles and abstracts against eligibility criteria, before screening full
and design of future rehabilitation programmes, the aim of this texts of relevant studies for final inclusion. Disagreements were
systematic review was to determine hip and lower-­leg muscle discussed until a consensus was reached, and a third reviewer
strength in ACL-­ injured limbs compared with (i) uninjured consulted for any disagreements as reported previously.25
controls and (ii) the uninjured contralateral limb.
Data extraction
METHODS Data were extracted using a prepiloted customised extraction
This systematic review adheres to Preferred Reporting Items form, by one author (MG) and checked by another (MH). Infor-
for Systematic Reviews and Meta-­Analyses guidelines. It was mation extracted included study design, country of study, demo-
prospectively registered (PROSPERO: CRD42020216793) graphics for each group (eg, age, sample size, number of women,
as part of a group of systematic reviews investigating changes body mass index, Tegner activity level, graft type), outcome
in strength and functional performance after ACL injury. This measure details, timepoint of data collection and outcome data
review focuses only on hip and lower-­leg strength, others will (reported as injured limb, non-­injured limb, control limb or limb
focus on quadriceps and hamstring strength as well as functional symmetry index (LSI)). For studies with multiple timepoints (eg,
test performance. There were three protocol deviations. The cohort studies or randomised controlled trials), we extracted
effect size in our analysis was changed from standardised mean data at all available timepoints. Where data were presented
differences to the ratio of means (RoM), to enable inclusion of only graphically, we extracted data using Plot Digitizer (V.2.6.8,
studies reporting only limb symmetry indices (see ‘Data anal- http://plotdigitizer.sourceforge.net/). Authors were contacted to
ysis’ section). This measure is also likely to be more clinically request any data unable to be extracted from the manuscript. If
interpretable. Second, meta-­analyses were conducted if two or no response was received after two attempts and the study had
more studies were available for analysis (instead of three), given no other data available for extraction, the study was excluded.
the lack of data for some measures. Lastly, we did not present Non-­English studies were translated using DeepL (http://www.​
comparisons between the uninjured leg of ACL-­injured groups deepl.com).26
and uninjured controls, as it was beyond the scope of this paper
given the breadth of this review. All deviations were made prior
Risk of bias assessment
to data analysis commencing.
We assessed risk of bias according to domains outlined by
Cochrane Collaboration guidelines (online supplemental file 3)
Eligibility criteria random sequence generation, allocation concealment, blinding
We included studies of primary ACL injury (managed with of therapist and patient, blinding of assessor, outcome measure-
surgical reconstruction or rehabilitation) with a mean partici- ment, bias in selection of participants, attrition and statistical
pant age of 18–40 years at the time of ACL injury. We did not analysis.27 Several different study designs were included, meaning
restrict inclusion on any other injury (eg, concomitant injuries), some risk of bias domains were not assessed in many studies
rehabilitation (eg, type, duration) or surgical (eg, graft type) (eg, bias related to randomisation or group allocation in cross-­
characteristics. Studies that reported a quantitative measure of sectional studies). Two reviewers (MG, MH) assessed risk of bias
hip or lower-­leg muscle strength measured by an isokinetic or independently with any disagreements resolved by discussion,
hand-­held dynamometer were included. Muscle strength had and a third reviewer (AGC) consulted as required. Certainty
to be reported for the ACL-­injured limb and (i) an uninjured of evidence was defined using the Grading of Recommenda-
control group (between-­person comparison) and/or (ii) the unin- tions, Assessment, Development and Evaluations,28 assessed by
jured contralateral limb (between-­ limb comparison). Studies two reviewers (MG, AGC). We assessed the certainty for each
that reported unilateral strength without comparison, or did strength outcome and comparison (between-­person and within-­
not specify the injured limb (eg, reported dominant and non-­ person). As most studies were observational, baseline grading
dominant side) were excluded. We did not restrict based on was ‘low’, with criteria used for downgrading evidence detailed
timing of strength assessment since surgery/injury. We also did in online supplemental table 11.3.
not limit based on study design, except for excluding studies of
fewer than 10 participants. Data analysis
Effect sizes for meta-­analyses were calculated as ratio of means
Search strategy (RoM).29 This method expresses the effect as the mean of
A search strategy was piloted based on key articles identified one group divided by the mean of the comparison. A detailed
in the literature and encompassed two elements: population description on the calculation of variance is published else-
(ACL injury) and outcome (strength or physical performance). where.29 30 For between-­limb comparisons (ie, within person),
We used the same search for all papers as part of this group these data are paired/correlated and so the RoM effect calcu-
of reviews. Free text and Medical Subject Headings terms were lation is modified slightly to account for this, by providing a
combined and tailored to each database (online supplemental correlation between limbs. As the between-­ limb correlation

2 Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536


Systematic review
was not reported by any study, we estimated this based on our to investigate the effects of sex and gender on findings,

Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
strength data as r=0.85.13 31 The RoM allows for simplified clin- however we were not powered for this.
ical interpretation (eg, a RoM of 0.8=ACL limb is 0.8× strength
of the comparator, or 20% deficit), compared with traditional RESULTS
metrics such as the standardised mean difference.29 The RoM is The initial search yielded 11 177 unique studies (Preferred
widely used in ecological research, and allowed for incorpora- Reporting Items for Systematic Reviews and Meta-­ Analyses
tion of studies that present data only as LSI. For studies that only flow chart, see online supplemental figure 1.1). We included 28
reported LSI, we approximated these to the RoM using formulae studies from 12 different countries for analysis. Data from 1103
(online supplemental file 4). Findings that were not presented (423 women, 38%) ACL-­injured and 1145 (933 women, 81%)
as mean (SD) format (eg, SE, 95% CI) were transformed with uninjured controls were included, with mean age ranging from
appropriate formulae.32 Data presented as median and IQRs 19 to 38 years in the ACL group (table 1). All except one study40
were transformed to mean and SD according to published included participants managed with surgery (all ACLR except
methods.33 one study of ACL repair). Most studies measured strength in the
Data were pooled based on the strength outcome (eg, hip first 12 months postsurgery, with only three studies measuring at
abduction) and the type of comparison: (i) between person >36 months postsurgery (table 1).41–43 Only six studies reported
(compared with uninjured control group) or (ii) between limbs Tegner activity levels, with mean/median scores ranging from 5
(compared with uninjured contralateral limb). We selected the to 7.13 44 14 40 45 46 Five studies recruited specifically athletes,47–49
dominant limb of the control group for comparison where with two at elite levels,41 50 while four others specified recre-
possible. To ensure data from each study were only included ationally active populations.20 42 43 51
once per outcome, per comparison in each meta-­analysis,34 Isometric testing with a hand-­ held dynamometer was the
the following decisions were used: (i) where studies reported most common method of strength assessment (16 studies).
multiple different measures for the same outcome (eg, isoki- The remaining 12 studies measured slow speed concen-
netic testing at 60°/s and 120°/s), the measure that was most tric strength using computerised isokinetic dynamometers
similar to other studies was selected for pooling; (ii) where a (≤120°/s),13 14 40 43–47 51–57 with 2 also measuring eccentric
study reported outcomes across multiple timepoints, the time- strength.46 54 Hip external and internal rotation strength were
point closest to 12 months post-­injury or reconstruction was only measured with hand-­ held dynamometers. All studies
selected. Data from <1 month postinjury/reconstruction, or measuring plantarflexion and dorsiflexion strength except one58
from ACL deficient groups were not included in meta-­analysis, used an isokinetic dynamometer. Method of strength assessment
and were summarised narratively. Random effects meta-­ for each study is listed on each forest plot and detailed in online
analysis with a restricted maximum likelihood estimator was supplemental table 5.1.
used when more than two studies were available for pooling
for each outcome and comparison. Where possible (more than Risk of bias
two studies), we stratified our analyses based on time since All except three studies suffered from high risk of bias of assessor
ACLR as: (i) short-­term (≤12 months) or (ii) long-­term (>12 blinding (ie, the assessor was aware of the injury status of the test
months). Analysis was conducted using the ‘metafor’35 and limb, online supplemental file 7).55 59 60 Outcome measurement
‘meta’36 packages in RStudio.37 We calculated tau2 to assess was reliably reported with detailed methodology and low risk
between-­study variance, I2 to assess total variability explained of bias for all except four studies.50 52 53 58 Ten studies suffered
by between-­study heterogeneity, and presented 95% predic- from unclear selection bias.40 42–44 46 47 51 56 57 61 Of the inter-
tion intervals for all analyses (estimate of interval where future vention trials included, three out of six had high risk of bias
observations could fall).38 We performed a leave-­ one-­out/ in randomisation methods (sequence generation and conceal-
influence analysis to check the robustness of results for each ment), and blinding methods, respectively.40 52 53 A funnel plot
meta-­analysis of more than two studies39 (online supplemental was only assessed for studies measuring hip abduction strength
file 9), by examining the impact of removing a study on overall comparing between limbs (n=12 studies, online supplemental
estimates and heterogeneity statistics (‘influence’ command figure 6.1). On inspection, there appears some slight asymmetry
from metafor and ‘metainf ’ from meta package). Any data (lack of small sample studies showing hip abduction weakness
that could not be summarised quantitatively were synthesised on the affected limb), although the Egger’s test was not statisti-
narratively. Scripts and all data used are publicly available: cally significant (intercept estimate 0.24, 95% CI −3.37 to 2.89,
https://github.com/mgirdwood7/hipcalf_acl_sr p=0.87).
The certainty of evidence was rated as very low for all muscle
strength outcomes for between-­ person (online supplemental
Equity, diversity and inclusion statement table 11.1) and within-­person comparisons (online supplemental
Our authorship team is gender balanced (four women and table 11.2). Evidence was primarily downgraded due to risk of
three men) with early, mid and late career researchers, bias and inconsistency, and also imprecision for some between-­
although all from one country. We have made every attempt person comparisons.
to be inclusive of data in this review, including translating
four studies from other languages (Japanese and German), META-ANALYSES
and requesting data from authors where possible. We have We were able to complete meta-­analyses for all main hip and
included data from 12 different countries from Europe, lower-­leg muscle groups (summary plots—figure 1). Detailed
North and South America, Asia, Oceania and the Middle plots and statistics for all meta-­analyses and sensitivity analyses
East, although no studies from Africa. Participants included are shown in online supplemental files 8 and 9, along with raw
in this review were a mixture of men and women, although data from each study per outcome (online supplemental tables
some studies reported exclusively on men. We had hoped 12.1-­12.8).

Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536 3


4
Table 1 Study characteristics
ACL group Control group Mean (SD) Measurement
Graft/Surgical Time post-­ACLR sample size sample (n BMI, mean Tegner device, unit of Muscle strength
Study Design Country intervention (months) (n women) women) Age, mean (SD) (SD) activity level measurement outcome
Balki, Göktas59 RCT Turkey Mixed 0.1 26 (0) – 27.4 (5.9) Not reported Not reported HHD, kg Hip abduction,
hip adduction, hip
extension, hip flexion
Systematic review

Bando, et al 201761 Case-­control— Japan Not reported 8 9 (9) 22 (22) 29.7 (13.9) Not reported Not reported HHD, kgf/kg Hip external rotation,
healthy hip internal rotation
Barnett, et al Secondary analysis USA ACL repair 6 65 (37) – 19.4 (5.1) 24.7 (3.8) Not reported HHD, LSI Hip abduction
202060 of RCT cohort
Bell, et al 201662 Case-­control— USA Mixed 30.9 55 (48) 73 (60) 19.0 (1.7) Not reported Not reported HHD, kg/kg Hip abduction, hip
healthy external rotation,
hip extension, hip
internal rotation
Dalton, et al Case-­control— USA Mixed 36.4 17 (11) 17 (11) 24.5 (4.1) Not reported Not reported HHD, N/kg Hip abduction, hip
201142 healthy external rotation, hip
extension
Fukuyama, et al Case-­control— Japan Not reported 1.51 (postinjury) 20 (12) 20 (8) 24.7 (6.9) 23.3 (4.1) Not reported HHD, kgf Hip abduction,
202248 healthy hip adduction,
hip flexion, hip
extension, hip
internal rotation, hip
external rotation
Geoghegan, et al Non-­RCT UK BPTB, HS 3 22 (4) – 33.2 Not reported Not reported Isokinetic, LSI Hip extension
200752
Girdwood, et al Longitudinal cohort Australia HS-­ST 12 111 (43) – 27 25.6 Median 6 (IQR HHD, Nm/kg Hip external rotation,
202313 4–7) hip internal rotation
Hadi, et al 201953 Non-­RCT Iran Mixed 3 and 6 58 (5) – 26.7 Not reported Not reported Isokinetic, N/m/s Hip extension
Hall 2015 Cross-­sectional USA Mixed 5.7 33 (14) – 28.5 25.3 Not reported HHD, kg/kg Hip abduction
Harput, et al Cross-­sectional Turkey HS 6 72 (0) – 28 (7.6) 24.2 (4.2) 7.3 (1.4) Isokinetic, Nm/kg Hip abduction
201846
Hoch 2018 Cross-­sectional USA Not reported 84 18 (12) – 24.6 (4.6) Not reported Not reported Isokinetic, Nm/kg Plantarflexion
(knee extended),
dorsiflexion
Karanikas, et al Cross-­sectional Germany Mixed 4.5, 9 and 18 69 (not – 30.2 (7.6) Not reported 5.6 (2.8) Isokinetic, Nm Ankle plantarflexion
200444 reported) (knee extended),
dorsiflexion, hip
extension, hip flexion
Karanikas, et al Non-­RCT Germany Mixed 12 33 (not – 31.7 (10.1) Not reported 6.6 (3.0) Isokinetic, Nm Ankle plantarflexion
200540 reported) (knee extended),
dorsiflexion, hip
extension, hip flexion
Kline, et al 201814 Case-­control— USA Mixed 8.3 20 (11) 45 (22) 22.8 Not reported Median 5.5 HHD, N/kg Hip abduction, hip
healthy (range 3–9) external rotation, hip
extension
Continued

Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536


Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
Table 1 Continued
ACL group Control group Mean (SD) Measurement
Graft/Surgical Time post-­ACLR sample size sample (n BMI, mean Tegner device, unit of Muscle strength
Study Design Country intervention (months) (n women) women) Age, mean (SD) (SD) activity level measurement outcome
Lima, et al 201547 Case-­control— Brazil Not reported 9.6 27 (0) 27 (0) 25.6 (5.8) 25.6 (4.4) Not reported Isokinetic, Nm/kg Hip abduction, hip
healthy adduction
Mouzopoulos, et al Case-­control— Greece Mixed 12 68 (0) 64 (0) 26.3 (4.6) Not reported Not reported Isokinetic, Nm/kg Hip flexion
201554 healthy
Myklebust, et al Prospective cohort Norway Not reported 42 80 (80) 778 (778) 23.3 (4.1) 23.4 (0.5) Not reported HHD, kg/kg Hip abduction
201741
Nicholas, et al RCT USA PT Pre-­op and 0.7 48 (19) – 32.5 (8.0) Not reported Not reported Isokinetic, LSI Ankle plantarflexion
200155 (knee extended),
ankle dorsiflexion
Noehren, et al Case-­control— USA Mixed 7.3 20 (20) 20 (20) 21.1 (5.9) Not reported 6.5 (1.6) HHD, Nm/kg Hip abduction, hip
201445 healthy external rotation
Rahova, et al Case-­control— Turkey Not reported 6 20 (0) 20 (0) 24.5 (5.3) 23.5 (1.2) Not reported HHD Hip abduction,
202250 healthy hip adduction,
hip extension, hip
flexion, hip external
rotation, hip internal

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rotation
Rhatomy, et al Case series Indonesia Peroneus longus 6 31 (9) – 27.6 (8.7) Not reported Not reported HHD Ankle eversion,
201958 hallux plantarflexion
Rhim, et al 202056 Case-­control— South Korea HS Pre-­op and 12 32 (20) 32 (17) 30 (7) 22 (2) Not reported Isokinetic, Nm/kg Ankle plantarflexion
healthy (knee extended),
ankle plantarflexion
(knee flexed)
Sullivan 2022 Case-­control USA Not reported 10.4 18 (8) – 20.8 (6.3) Not reported Not reported HHD, % body mass Hip abduction
Tate, et al 201720 Case-­control— USA Mixed 32 12 (7) 12 (7) 20.8 (2.1) Not reported Not reported HHD, N/height×BM Hip abduction, hip
healthy extension
Thomas, et al Case-­control— USA BPTB Pre-­op and 7.0 15 (7) 15 (8) 20.3 (5.4) Not reported Not reported Isokinetic, Nm/kg Ankle plantarflexion
201357 healthy (knee extended),
ankle dorsiflexion,
hip abduction, hip
adduction, hip
extension, hip flexion
Tyler 2004 RCT USA BPTB 2.8 60 (27) – 36.6 (1.5) Not reported Not reported HHD, LSI Hip abduction,
hip adduction, hip
flexion
Urabe, et al 200251 Case series Japan HS-­ST Pre-­op, 3, 6, 9, 12 44 (20) – 32.7 (range 16–47) Not reported Not reported Isokinetic, Hip adduction
Nm/kg
ACLR, ACL reconstruction; BM, body mass; BMI, body mass index; BPTB, bone-­patellar tendon-­bone; HHD, hand-­held dynamometer; HS, hamstring; kgf, kg force; LSI, limb symmetry index; mixed, multiple different graft types; Nm, Newton metres;
Pre-­op, pre-­operatively; RCT, randomised controlled trial.
Systematic review

5
Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
Systematic review

Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
Figure 1 Summary forest plot of overall meta-­analysis estimates for each outcome, for comparison with uninjured control group (left) and with
uninjured limb (right). Black diamonds are summary estimates (95% CI) from meta-­analyses with orange bands representing the prediction intervals.
Grey shaded region indicates ±10% difference in strength. ACLR, ACL reconstruction.

Hip abduction 2 studies), but not in the short-­term (−1% (95% CI −22% to
We found no evidence for a difference in hip abduction strength +25%), ACL n=49, control n=77, 3 studies, figure 3). When
between ACL-­ injured limbs and uninjured controls (ACL pooling across all timepoints, we found no difference between
n=266, control n=926, 9 studies), or between limbs for ACL-­ ACL groups and uninjured control groups for hip external rota-
injured individuals (n=473, 12 studies), for both short-­term and tion strength (ACL n=121, control n=177, 5 studies, figure 3).
long-­term follow-­ups (figure 2). Results were robust to omis- This result was fragile to omission of two studies,45 61 suggesting
sion of any study (online supplemental figure 9.1). One study caution in this finding (online supplemental 9.3). When
also measured hip abduction strength eccentrically (estimate comparing between limbs in ACL-­injured groups, we found no
not included in meta-­analysis), finding no difference between difference in hip external rotation strength (n=186, 3 studies),
limbs.46 with significant heterogeneity of effects, and overall estimate
fragile to omission of one study.62
Hip adduction
We found 24% (95% CI 8% to 42%) stronger hip adductors on Hip internal rotation
the ACL-­injured limb compared with uninjured controls (ACL There was no difference in hip internal rotation strength in ACL-­
n=62, control n=62, 3 studies, online supplemental figure 8.1), injured people compared with uninjured controls (ACL n=64,
although this result was fragile to omission of two studies (online control n=95, 2 studies, online supplemental figure 8.2). There
supplemental figure 9.2).47 57 There was no difference between was no evidence for a difference in strength between limbs in
limbs in ACL groups (n=166, 5 studies, online supplemental ACL-­ injured populations (n=166, 2 studies, online supple-
figure 8.1). Omission of three studies lowered I2 values, but did mental figure 8.2). Both comparisons were limited by significant
not significantly alter overall estimates (online supplemental file variability of findings.
9.2).50 51 57
Hip extension
Hip external rotation Hip extension strength was not different between ACL-­injured
Hip external rotation strength was lower (−12% (95% CI −6% people and uninjured controls (ACL n=139, control n=182,
to −18%)) in ACL-­injured people compared with uninjured 6 studies, figure 4), or between limbs in ACL-­injured groups
controls at long-­term follow-­ups (ACL n=72, control n=100, (n=304, 9 studies). Both comparisons showed considerable

Figure 2 Forest plots from hip abduction meta-­analyses for comparison with uninjured control group (left) and with uninjured limb (right). ACL
reconstruction; Con, concentric; HHD, hand-­held dynamometer; ISK, isokinetic dynamometer; RoM, ratio of means.

6 Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536


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Figure 3 Forest plots from hip external rotation meta-­analyses for comparison with uninjured control group (left) and with uninjured limb (right).
HHD, hand-­held dynamometer; ISK, isokinetic dynamometer; Con, concentric; ACL reconstruction; RoM, ratio of means.

variability in effects, especially when comparing with uninjured Dorsiflexion strength


controls (I2=72%, prediction interval=0.61 to 1.67). Results Four studies measured dorsiflexion strength, with no differences
were consistent for short-­term and long-­term follow-­ups, and shown when compared with an uninjured control group (ACL
overall effect estimates were consistent with omission of any n=35, control n=35, 2 studies, (online supplemental figure 8.5)
study, although omission of three studies lowered I2 values or to the contralateral limb (n=143, 5 studies).
(online supplemental figure 9.3).20 44 53
Other outcomes
Two studies measured strength in the first month after ACLR and
Hip flexion were not included in any meta-­analyses. One study measured
There was no difference in hip flexion strength in ACL groups hip flexor, hip extensor, hip abductor and hip adductor strength
compared with uninjured controls (ACL n=103, control n=99, on the fourth day after surgery, finding deficits ranging from
3 studies, online supplemental figure 8.3). Comparison between 50% to 80% on the ACLR limb compared with the contralat-
limbs in ACL-­injured people showed no difference in hip flexion eral limb.59 Another study investigating the impact of tourniquet
strength (n=265, 6 studies, online supplemental figure 8.3). use 3 weeks postsurgery, showed ~15%–20% lower dorsi-
This finding was affected by significant variability of effects flexion strength, and ~10% lower plantarflexion strength (knee
(I2=97%, prediction interval=0.12 to 7.94). Omission of one flexed at 30°).55 Findings were not affected by tourniquet use.
study54 lowered I2, but did not alter the overall estimate (online One study measured ankle eversion and first ray plantarflexion
supplemental figure 9.5). strength (after use of peroneus longus autograft), and found no
differences between limbs.58 Five studies measured strength pre-­
operatively,48 51 55–57 with findings summarised in online supple-
Plantarflexion strength mental 10.
Plantarflexion strength was measured by six studies. No differ-
ence was found between ACL and uninjured control groups ACL deficient populations
(ACL n=67, control n=67, 3 studies, online supplemental figure One study measured non-­surgically managed ACL injuries 12
8.4), or between limbs in ACL-­injured groups (n=175, 6 studies, months postinjury (n=12) and found no differences between
online supplemental figure 8.4). Only one study measured plan- limbs for hip extension, hip flexion, plantarflexion or dorsi-
tarflexion strength in a knee flexed position (in addition to flexion strength.40
knee extended position included in meta-­analysis),56 finding no
difference comparing with uninjured controls, but significantly DISCUSSION
greater strength (10%) on the ACL limb compared with the Results from our meta-­analyses do not support the notion that
contralateral limb. widespread hip or lower-­leg muscle weakness exists after ACL

Figure 4 Forest plots from hip extension meta-­analyses for comparison with uninjured control group (left) and with uninjured limb (right). ACL,
anterior cruciate ligament; ACLR, ACL reconstruction; CI, CI interval; HHD, hand held dynamometer; ISK, isokinetic dynamometer; RoM, ratio of means.

Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536 7


Systematic review
injury. We found no consistent evidence for a difference between controlled trials. Although it is possible that non-­thigh muscles

Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
people (ie, compared with uninjured controls), or within people were not overly impaired pre-­injury or postsurgery, this seems
(ie, comparison with the uninjured contralateral limb), with the less likely, as hip muscle weakness is evident in some people pre-­
largest number of studies available for hip abduction and exten- injury,72 and two studies included in this review showed large
sion strength. The only non-­zero differences identified were 12% deficits in hip and lower-­leg strength in the first 2–3 weeks postre-
(95% CI 6% to 18%) weaker hip external rotators and 24% construction.55 59 Further longitudinal studies measuring muscle
(95% CI 8% to 42%) stronger hip adductors in the ACL-­injured strength across multiple timepoints may help to understand the
limb compared with uninjured controls, however both results trajectory and cause of any hip muscle strength changes.
were pooled from only two studies. Certainty of evidence was Thigh muscle weakness after injury may increase the demand
very low for all outcomes. Many between-­person estimates were on hip and lower-­leg muscles, and these non-­knee muscles may
affected by low numbers of included studies, as well as heteroge- need to be stronger than in uninjured people. Indeed, our results
neity of effects with wide prediction intervals, suggesting caution showed stronger adductors in the ACL-­injured limb compared
in interpreting these findings. Individualised assessment should with uninjured controls. Other studies have found greater
guide prescription of hip and lower-­leg muscle strengthening. hip extension strength in those with weaker quadriceps after
Our review provides the first comprehensive summary of hip ACLR,62 and change to a more ‘hip-­dominant’ strategy shown
and lower-­leg muscle strength after ACL injury. Contrary to our across movements such as hopping.73 Before we can recom-
expectations, there was no consistent evidence for widespread mend training a more hip dominant strategy to compensate for
lower-­ limb muscle weakness (ie, across different movement quadriceps weakness, we need to determine whether a clinically
directions), nor weakness with large effect sizes. SE of measure- meaningful link exists between greater hip strength and better
ment for hip and lower-­ leg strength assessment is generally structural and self-­reported outcomes, and whether this can be
between 5% and 10%.63–65 Acknowledging the limitations of targeted with tailored strength training.
sample sizes and variability of study effects, almost all of our For clinicians, restoring hip muscle strength may still be a
point estimates and summary findings (except for hip adduction priority—individualised assessment of the impairments and
strength) showed muscle strength outcomes within 5%–10% of goals of each person should be considered.22 24 However, our
the comparator (most data from 6 to 12 months post-­ACLR), results might indicate that routine isolated hip muscle strength
suggesting even with these limitations, major weakness such training may not be necessary in all people after ACL injury,
as is commonly reported for the quadriceps and hamstrings is acknowledging that wide prediction intervals for some results
unlikely to be present in the hip and lower-­leg muscles after ACL (eg, hip extension) could suggest significant variability from our
injury. estimates in some people. Many of our results are from data
Quadriceps and hamstring weakness is near universal after between 6 and 12 months post-­ACLR, although deficits might
ACL injury and a major clinical impairment that continues to still be present earlier post-­operatively. Maintenance of strength,
be a challenge, despite extensive rehabilitation efforts.23 Based particularly in the early postoperative phase, may be another
on our findings, persistent weakness may be contained to the justification for adding hip and calf training to rehabilitation.
thigh muscles. Pain, effusion and immobilisation caused by ACL Incorporating multijoint movements, functional tasks and closed
injury and reconstruction undoubtably affect the knee the most, kinetic chain exercises will also target the broader kinetic chain,
however it is surprising that other lower-­limb muscles such as including the hip and lower-­leg muscles. Targeting the hip and
the hip and calf appear unaffected, given their critical contribu- calf muscles may also benefit athletic performance. Guidelines
tions to knee movement and control. Unlike the thigh, the hip and consensus exercises recommend a key focus on regaining
and lower-­leg muscles could be less affected by central nervous quadriceps strength after injury,70 74 and this should remain a
system changes postinjury/surgery,66 that contribute to persistent top priority.2 For participants with hip and lower-­leg muscle
thigh muscle weakness. The hip and calf are also unlikely to be impairments identified during rehabilitation, targeted strength
affected by significant arthrogenic muscle inhibition or changes training may be appropriate. Monitoring hip muscle strength is
to activation commonly seen in the quadriceps and hamstrings feasible and reliable in the clinic with a hand-­held dynamometer,
as a result of pain and effusion at the knee joint.67 68 Certainty and can be used to guide training goals.64 75 Hip and lower-­leg
of evidence was very low for all outcomes, and most studies muscle strength within 5%–10% of either normative data, or the
reported strength between 6 and 12 months post-­ACLR). As contralateral leg may be an indicative standard for people to aim
further evidence emerges, it is possible our results could change. for after ACL injury.
Hip abduction strength had the most evidence, with narrow This review has several limitations. Many comparisons were
prediction intervals, where new papers are unlikely to alter our affected by small number of studies and included participants.
estimates, although certainty of evidence was still very low. Where possible (more than two studies), we conducted a leave-­
Current rehabilitation approaches for the hip and lower-­leg one-­out sensitivity analysis to assess the robustness of findings,39
muscles may adequately restore comparable muscle strength to and overall effect estimates for most outcomes were unaffected
the levels of uninjured controls. Training non-­thigh muscles is by removal of a study. Almost all included studies failed to
frequently recommended for knee injury rehabilitation (including blind the outcome assessor (ie, strength tester), which is rele-
ACL injury).24 69 No ACL clinical guidelines specifically recom- vant given assessor encouragement can impact the voluntary
mend hip or calf muscle strengthening,70 nor do major inter- effort needed to achieve an accurate measure of peak strength.
vention studies measure the impact of training these muscles. It may also be important for hand-­held dynamometry where
Unfortunately, rehabilitation was often insufficiently described the assessor must match or break the force. Many case-­control
in the included studies, leaving us to speculate. Rehabilitation studies were also affected by unclear selection bias, a common
completion and adherence was likely variable for participants in problem for this research design,76 likely adding to uncertainty
these studies, as previous studies have reported <50% of people of prediction intervals. Comparison with an uninjured control
engaged with a therapist for rehabilitation beyond 3 months group is important for outcomes such as muscle strength, as
post-­ACLR.71 On the other hand, some participants may have comparing with the uninjured contralateral leg may be affected
had structured training as part of study protocols in randomised by confounding factors including weakness pre-­injury, reduced

8 Girdwood M, et al. Br J Sports Med 2024;0:1–11. doi:10.1136/bjsports-2023-107536


Systematic review
activity post-­injury and central nervous system changes.77 78 We Provenance and peer review Not commissioned; externally peer reviewed.

Br J Sports Med: first published as 10.1136/bjsports-2023-107536 on 27 March 2024. Downloaded from http://bjsm.bmj.com/ on April 12, 2024 by guest. Protected by copyright.
identified two additional studies unable to be included,79 80 with Data availability statement Data are available in a public, open access
hip strength outcomes reported without specifying the injured repository.
limb, or reported only as a strength ratio (eg, abduction:ad- Supplemental material This content has been supplied by the author(s). It
duction ratio). We are also aware of five studies measuring hip has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have
muscle strength in adolescent/paediatric populations which did been peer-­reviewed. Any opinions or recommendations discussed are solely those
of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and
not fit our criteria.81–85
responsibility arising from any reliance placed on the content. Where the content
Another limitation was the pooling of different contraction includes any translated material, BMJ does not warrant the accuracy and reliability
types and strength testing methods (eg, concentric and isometric of the translations (including but not limited to local regulations, clinical guidelines,
tests), which may have diluted any potential deficits. Isometric terminology, drug names and drug dosages), and is not responsible for any error
contractions may be more sensitive to showing asymmetries, as and/or omissions arising from translation and adaptation or otherwise.
muscles can exert higher force during isometric contractions, ORCID iDs
compared with concentrically.86 87 Similarly, the hip muscles are Michael Girdwood http://orcid.org/0000-0001-6477-7263
often tested in different positions (eg, in hip neutral vs 90° hip Adam G Culvenor http://orcid.org/0000-0001-9491-0264
flexion for hip rotation strength), influencing length-­ tension Brooke Patterson http://orcid.org/0000-0002-6570-5429
Melissa Haberfield http://orcid.org/0000-0002-6366-0896
relationships which could explain some of the variability seen
Kay M Crossley http://orcid.org/0000-0001-5892-129X
in our estimates.
Results from our review are most generalisable to young (age
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