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Department of Clinical Therapies, University of Limerick, Ireland Correspondence to Kieran O’Sullivan, Department of Clinical Therapies, University of Limerick, Limerick, Ireland; [email protected] Received 4 December 2011 Accepted 8 March 2012 The effects of eccentric training on lower limb flexibility: a systematic review Kieran O’Sullivan, Sean McAuliffe, Neasa DeBurca ABSTRACT Background Reduced flexibility has been documented in athletes with lower limb injury, however, stretching has limited evidence of effectiveness in preventing injury or reducing the risk of recurrence. In contrast, it has been proposed that eccentric training can improve strength and reduce the risk of injury, and facilitate increased muscle flexibility via sarcomerogenesis. Objectives This systematic review was undertaken to examine the evidence that eccentric training has demon- strated effectiveness as a means of improving lower limb flexibility. Study appraisal and synthesis methods Six elec- tronic databases were systematically searched by two independent reviewers to identify randomised clinical trials comparing the effectiveness of eccentric training to either a different intervention, or a no-intervention control group. Studies evaluating flexibility using both joint range of motion (ROM) and muscle fascicle length (FL) were included. Six studies met the inclusion/exclu- sion criteria, and were appraised using the PEDro scale. Differences in the muscles studied, and the outcome measures used, did not allow for pooled analysis. Results There was consistent, strong evidence from all six trials in three different muscle groups that eccentric training can improve lower limb flexibility, as assessed using either joint ROM or muscle FL. Conclusion The results support the hypothesis that eccentric training is an effective method of increasing lower limb flexibility. Further research is required to com- pare the increased flexibility obtained after eccentric training to that obtained with static stretching and other exercise interventions. INTRODUCTION Lower limb injuries are very common among ath- letes, with significant consequences for both ath- letes and their teams. 1 2 It is important therefore to identify, and effectively manage, factors that could reduce injury risk and the time until return to sport. 3–5 Several factors have been proposed as contributing to the high incidence of lower limb injuries, including non-modifiable factors such as age, 1 6 gender 7 and previous injury. 1 8 Modifiable factors have also been implicated, including altered neuromuscular control, 9 reduced muscle strength, 10 11 altered muscle length-tension curve 12 13 and reduced flexibility. 14 There is some evidence that using an early stretching programme to increase flexibility may reduce the time until return to sport. 4 15 However, the main benefit of stretching seems to be an increase in flexibility, 16 with most studies sug- gesting stretching is ineffective at reducing injury risk, 3 17–24 postexercise muscle soreness, 25 or improving performance. 26 27 Increased flexibility after a single bout of stretching only lasts approx- imately 30 min. 28–31 This short-term increase is mainly due to temporary changes in viscoelastic behaviour. 32 A stretching programme performed regularly for several weeks results in meaningful improvements in range of motion (ROM), 33–35 however, such increases in flexibility do not seem to reduce injury risk. Considering the existing evidence of reduced flexibility in some lower limb injuries, 29 36 37 the limited evidence to support stretching appears contradictory. However, it is possible that deficits in flexibility which are observed clinically are sim- ply one manifestation of an alteration in muscle function. Athletes with less flexible hamstrings display an altered muscle length-tension curve, with changes in the angle of peak torque and the torque produced at longer muscle lengths. 38 Consequently, athletes with reduced flexibility may be exposing their muscles to potentially damaging lengthening forces. Eccentric training results in the addition of sarcomeres in series (sar- comerogenesis) in animal models. 39 This increases the joint angle at which peak torque is generated, 40 and increases muscle fascicle length (FL). 41 The use of such eccentric training to increase flexibil- ity would combine strengthening and ‘stretching’ of the muscle tissues, which may be important considering the advantages for lower limb tissues avoiding prolonged eccentric loading at length- ened joint angles. 42 Currently, in the absence of clear effectiveness of many exercise interventions, training and rehabil- itation of lower limb injuries commonly includes strengthening, stretching and other components including balance training. 43 However, research from animal models 39 41 44 suggests that eccentric training could increase flexibility via sarcomero- genesis without the need for additional stretch- ing exercises. This is significant considering the additional benefits of eccentric training in terms of power development and injury risk reduction. 11 45 46 Furthermore, technological developments have facilitated the imaging of intramuscular responses to exercise, such as ultrasound imaging of muscle FL. 47 However, it is not clear if there is sufficient data from human studies to support the hypoth- esis that eccentric training is an effective stimulus for increased flexibility. Therefore, the aim of this systematic review was to appraise the evidence Published Online First 20 April 2012 Review 838 Br J Sports Med 2012;46:838845. doi:10.1136/bjsports-2011-090835 group.bmj.com on February 26, 2013 - Published by bjsm.bmj.com Downloaded from

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Department of Clinical Therapies, University of Limerick, Ireland

Correspondence to Kieran O’Sullivan, Department of Clinical Therapies, University of Limerick, Limerick, Ireland; [email protected]

Received 4 December 2011Accepted 8 March 2012

The effects of eccentric training on lower limb fl exibility: a systematic reviewKieran O’Sullivan, Sean McAuliffe, Neasa DeBurca

ABSTRACTBackground Reduced fl exibility has been documented

in athletes with lower limb injury, however, stretching

has limited evidence of effectiveness in preventing

injury or reducing the risk of recurrence. In contrast, it

has been proposed that eccentric training can improve

strength and reduce the risk of injury, and facilitate

increased muscle fl exibility via sarcomerogenesis.

Objectives This systematic review was undertaken to

examine the evidence that eccentric training has demon-

strated effectiveness as a means of improving lower

limb fl exibility.

Study appraisal and synthesis methods Six elec-

tronic databases were systematically searched by two

independent reviewers to identify randomised clinical

trials comparing the effectiveness of eccentric training

to either a different intervention, or a no-intervention

control group. Studies evaluating fl exibility using both

joint range of motion (ROM) and muscle fascicle length

(FL) were included. Six studies met the inclusion/exclu-

sion criteria, and were appraised using the PEDro scale.

Differences in the muscles studied, and the outcome

measures used, did not allow for pooled analysis.

Results There was consistent, strong evidence from all

six trials in three different muscle groups that eccentric

training can improve lower limb fl exibility, as assessed

using either joint ROM or muscle FL.

Conclusion The results support the hypothesis that

eccentric training is an effective method of increasing

lower limb fl exibility. Further research is required to com-

pare the increased fl exibility obtained after eccentric

training to that obtained with static stretching and other

exercise interventions.

INTRODUCTIONLower limb injuries are very common among ath-letes, with signifi cant consequences for both ath-letes and their teams.1 2 It is important therefore to identify, and effectively manage, factors that could reduce injury risk and the time until return to sport.3–5 Several factors have been proposed as contributing to the high incidence of lower limb injuries, including non-modifi able factors such as age,1 6 gender7 and previous injury.1 8 Modifi able factors have also been implicated, including altered neuromuscular control,9 reduced muscle strength,10 11 altered muscle length-tension curve12

13 and reduced fl exibility.14

There is some evidence that using an early stretching programme to increase fl exibility may reduce the time until return to sport.4 15 However, the main benefi t of stretching seems to be an

increase in fl exibility,16 with most studies sug-gesting stretching is ineffective at reducing injury risk,3 17–24 postexercise muscle soreness,25 or improving performance.26 27 Increased fl exibility after a single bout of stretching only lasts approx-imately 30 min.28–31 This short-term increase is mainly due to temporary changes in viscoelastic behaviour.32 A stretching programme performed regularly for several weeks results in meaningful improvements in range of motion (ROM),33–35 however, such increases in fl exibility do not seem to reduce injury risk.

Considering the existing evidence of reduced fl exibility in some lower limb injuries,29 36 37 the limited evidence to support stretching appears contradictory. However, it is possible that defi cits in fl exibility which are observed clinically are sim-ply one manifestation of an alteration in muscle function. Athletes with less fl exible hamstrings display an altered muscle length-tension curve, with changes in the angle of peak torque and the torque produced at longer muscle lengths.38 Consequently, athletes with reduced fl exibility may be exposing their muscles to potentially damaging lengthening forces. Eccentric training results in the addition of sarcomeres in series (sar-comerogenesis) in animal models.39 This increases the joint angle at which peak torque is generated,40 and increases muscle fascicle length (FL).41 The use of such eccentric training to increase fl exibil-ity would combine strengthening and ‘stretching’ of the muscle tissues, which may be important considering the advantages for lower limb tissues avoiding prolonged eccentric loading at length-ened joint angles.42

Currently, in the absence of clear effectiveness of many exercise interventions, training and rehabil-itation of lower limb injuries commonly includes strengthening, stretching and other components including balance training.43 However, research from animal models39 41 44 suggests that eccentric training could increase fl exibility via sarcomero-genesis without the need for additional stretch-ing exercises. This is signifi cant considering the additional benefi ts of eccentric training in terms of power development and injury risk reduction.11 45 46 Furthermore, technological developments have facilitated the imaging of intramuscular responses to exercise, such as ultrasound imaging of muscle FL.47 However, it is not clear if there is suffi cient data from human studies to support the hypoth-esis that eccentric training is an effective stimulus for increased fl exibility. Therefore, the aim of this systematic review was to appraise the evidence

Published Online First20 April 2012

Review

838 Br J Sports Med 2012;46:838–845. doi:10.1136/bjsports-2011-090835

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from randomised clinical trials on whether eccentric training results in meaningful increases in lower limb fl exibility when compared with another, or no, intervention.

METHODSOverviewThe Cochrane and MEDLINE databases were initially searched, revealing no systematic reviews regarding the effectiveness of eccentric training on lower limb fl exibility. Randomised clini-cal trials which compared the effect of eccentric training on lower limb fl exibility to either no intervention, or a differ-ent intervention, were included in this review. Studies using a method of measuring actual muscle length (eg, ultrasound imaging of FL) or joint ROM (eg, goniometry) were included. Studies involving adults aged >18 years, with or without a history of injury, were eligible. Studies focusing solely on the effects of eccentric training on other factors such as peak torque or injury incidence were excluded. Studies involving eccentric training of <4 weeks duration, such as those examin-ing muscle damage postexercise, were excluded. Only peer-re-viewed articles were considered. Conference proceedings were excluded because they are not consistently peer reviewed, and often lack suffi cient information to adequately assess method-ological quality. The review was registered (CRD42011001659) on the PROSPERO database,48 and has been reported in accor-dance with the PRISMA statement.49

Search strategy and inclusion criteriaThe following databases were searched; Academic Search Complete, AMED, Biomedical Reference Collection, CINAHL, MEDLINE and SPORTDiscus. Two authors (KOS, NDB) inde-pendently searched these databases using the following agreed range of keywords; eccentric (Abstract) AND fl exib* OR range of motion OR fascicle (Abstract) AND strength OR training (full-text) (fi gure 1). Studies were limited to those involv-ing humans, published in English, after 1999. The titles and abstracts of these selected articles were then screened. When no abstract was available, or when it was not clear if the study should be included, full-text articles were retrieved. Studies were excluded if they did not involve the lower limb, did not examine fl exibility or if eccentric training was only one of sev-eral interventions. The reference lists of the selected articles were also manually searched for any further relevant articles.

Data extractionFor each article the following information was extracted by two authors (SMA, KOS), and cross-checked for accuracy;

(1) sample size (2) participant gender, (3) participant age, (4) muscle group studied, (5) type of outcome measure used and (6) inclusion/exclusion criteria (table 1).

Assessment of methodological qualityTwo authors (NDB, SMA) independently rated the method-ological quality of the included studies using the PEDro scale, which has established reliability50 and validity.51 Neither author was specifi cally trained in the use of the PEDro scale, but clarifying information on several aspects of the scale was sought from the designers of the scale in advance. Authors of the original studies were emailed for clarifi cation if necessary. Thereafter, a consensus decision was reached with a third author (KOS). Study quality was classifi ed as ‘high’ (>6/10), ‘fair’ (4/10–5/10) or ‘poor’ (<4/10) according to PEDro scores.52 As this review only includes studies published in databases, there is an overall risk of publication bias. Furthermore, the reliability and validity of the methods used to analyse fl ex-ibility were appraised.

Data SynthesisDifferences in the muscles studied, and the outcome measures used, did not allow for pooled analysis. Instead, the data for each muscle group were analysed together to identify consis-tent effects of eccentric training on lower limb fl exibility.

RESULTSIdentifi cation of studiesThe electronic search resulted in a total of 530 potentially relevant papers, which was reduced to 285 after the removal of duplicates. After screening the title and abstract of each article, seven full-text articles were identifi ed by both reviewers independently. One study53 was excluded as it compared two mixed concentric/eccentric training pro-grammes of different intensities, rather than comparing eccen-tric training to a different exercise intervention. Searching the reference lists of these articles did not add any further articles. Consequently, the fi nal number of articles included in this review was six.54–59 The selection procedure is outlined in fi gure 2.

Description of included studiesA detailed description of the included studies, listed alpha-betically, is presented in table 1. The number of participants included ranged from 18 to 69. In fi ve54–58 of the six studies, the mean age of participants was 16 to 28 years, with one study59 including much older participants (mean age of 71 years). Four54 56 58 59 of the six studies included both male and female participants. ROM using goniometry,56–58 or FL using ultrasound,54 55 58 59 were used as outcome measures, with one study58 using both. Inclusion and exclusion criteria were very similar between studies. No study included participants with a current or previous lower limb injury. Only one study57 specifi cally included participants with muscle ‘tightness’.

Eccentric training characteristicsThe eccentric training completed in each study is described in table 2. There were signifi cant variations in terms of the type of eccentric training, the number of repetitions and sets per-formed, the intensity of the training, the duration for which the eccentric contraction was sustained, as well as the fre-quency and duration of the training.Figure 1 Boolean logic of search terms used.

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METHODOLOGICAL STUDY QUALITYAll six studies were rated as ‘high quality’ using the PEDro scale (table 3). All six studies randomly allocated participants and involved concealment of allocation. In three studies, par-ticipants were not different at baseline in the main outcome measure of interest to this review, either FL or ROM. However, in the other three studies,54 58 59 baseline differences were pres-ent, which could partly explain different responses between groups, and this concern is addressed in detail later. Two stud-ies did not state using an outcome assessor who was blinded to group allocation.57 59 None of the trials blinded the therapists or patients, which is almost unavoidable in studies of exercise interventions. All six studies reported follow-up measures for

at least 85% of participants, although in three studies,54 56 57 all participants were not followed up and there was no use of intention to-treat analysis, or detail on how dropouts were handled. All six studies performed between-group analysis, and provided information on both point measures and vari-ability. Regarding other methodological issues not covered in the PEDro scale, no study justifi ed the sample size used based on a power calculation, and there was a strong bias towards male participants in three studies.55 57 58

DESCRIPTION OF RESULTSAll six studies showed consistent evidence that eccentric train-ing increases ROM,56 57 or FL,54 55 59 or both,58 irrespective of the joint or muscle group studied. At the ankle, Mahieu et al56 reported a signifi cantly greater increase in dorsifl exion (mean change=+6°) compared with a no-exercise control group (mean change=+1°). Using ultrasound measurements of FL rather than ankle joint ROM, Duclay et al55 reported similar results. There was a signifi cant increase in FL (mean change=+3.36 mm) at rest after eccentric training, compared to a control group (mean change=+1.01 mm) which performed no exercise intervention.55

Consistent increases in fl exibility after eccentric training were also reported for the hamstrings. Nelson and Bandy57 ran-domised participants into one of three groups; static stretching, eccentric training and control (no exercise). Both the eccentric training (mean change=+12.79°) and static stretching (mean change=+12.05°) groups reported signifi cantly larger increases in ROM at follow-up compared with the control group (mean change=+1.67°). Potier et al58 also studied the hamstrings, and was the only study to include both FL and ROM as outcome measures. After the training period, there was a signifi cantly greater increase in ROM (mean change=+6.9°) in the eccen-tric training group, compared to the non-exercise control group (mean change=−1.8°). Furthermore, the increase in FL was signifi cantly larger for the eccentric training group (mean change=+34%), being twice as large as the increase reported in the control group (mean change=+17%).

Finally, two studies54 59 examined the effect of eccentric training on quadriceps fl exibility. Unlike the other four studies, both of these studies used as the comparison another exercise intervention which could increase muscle strength, similar to eccentric training. Reeves et al59 observed a signifi cant increase in FL after eccentric training, which had not been evident dur-ing a 14-week pretraining monitoring period. Furthermore,

Table 1 Description of included studies

Study Sample size Gender Mean age Muscle group Outcome measure Inclusion/exclusion criteria

Blazevich et al54 33 16 M/17 F 23 Quadriceps FL Recreationally active; No lower limb injury; No weight training; No co-existing medical conditions; Not a manual occupation; Not exercising vigorously >4 times/week

Duclay et al55 18 All male 23 Calf FL Healthy students; Recreationally active; No neurological injury/disease; Not engaged in resistance training

Mahieu et al56 64 32 M/32 F 22 Calf ROM Recreationally active; No lower limb injury; Not elite athleteNelson and Bandy57 69 All male 16 Hamstring ROM Tight hamstrings; Not currently increasing their exercise

intensity; No lower limb injury; No low back painPotier et al58 22 16 M/6 F 28 Hamstring FL and ROM Not engaged in resistance training; No musculoskeletal injury;

No co-existing medical conditionsReeves et al59 19 8 M/10 F 71 Quadriceps FL Recreationally active; No musculoskeletal injury; No co-existing

medical conditions; Living independently

F, female; FL, fascicle length; M, male; ROM, range of motion.

Figure 2 Flow chart of study identifi cation procedure.

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while FL also increased from the baseline in a mixed concen-tric/eccentric training group (mean change=+6 mm, or +8%), the increase was signifi cantly greater in the eccentric train-ing group (mean change=+16 mm, or +22%). Blazevich et al54 included three groups in their study of the quadriceps; an eccentric group, a concentric group and a non-exercise control group. Both the eccentric (mean change=+3.1%) and concen-tric (mean change=+6.3%) training groups demonstrated sig-nifi cant increases in FL (mean change=+4.2%) after 10 weeks, unlike the control group (mean change=−0.3%). However, unlike Reeves et al,59 FL increased to a greater extent, albeit non signifi cantly, in the concentric training group.

DISCUSSIONMain fi ndingsConsistent evidence in six high-quality studies supported the hypothesis that eccentric training is effective at increasing lower limb fl exibility. This fi nding was consistent across dif-ferent muscle groups, and using different outcome measures. All four studies54 55 58 59 which examined muscle FL identifi ed signifi cant gains in FL following eccentric training, indicating structural adaptations within the muscle. Similarly, the fi nd-ings from all three studies56–58 examining ROM confi rm that increases in ROM occur after eccentric training, irrespective of the muscle group studied.

Defi ning and analysing fl exibilityReviewing the literature in this area is complicated by attempts to defi ne fl exibility. Flexibility has traditionally been examined

using indirect ROM measurements defi ned separately as ‘fl ex-ibility’ and ‘stretch tolerance’,60 while recent technological developments have allowed direct measurements of FL.58 In this review, we considered studies which have evaluated any of these measurements before and after eccentric training as a measure of ‘fl exibility’. The ROM measurements such as those used in this study are relatively reliable29 61 and clini-cally applicable. However, it must be acknowledged they may not accurately represent underlying muscle length, especially in biarticular muscles such as those included in these studies. Obviously other factors can increase ROM, such as a simple warm-up,29 and inconsistency across studies on the use of a warm-up could infl uence the magnitude of change in ROM observed, although this would not change the overall effec-tiveness reported across all muscle groups. Furthermore, in one study, the baseline differences in ROM between groups (7.9°) actually exceeded the increase reported after eccentric training (6.9°).

Analysing FL using ultrasound also involves a degree of error, especially in those studies involving vastus lateralis54

59 and the hamstrings,58 where their relatively long FLs47 55 required FL to be estimated using linear extrapolation. This may partly explain why there were baseline differences in FL in two studies.54 59 While the use of a repeated baseline with very little variation supports the measurement proto-col in one of these studies,59 a large change in FL among the control group in one study58 and after the intervention had ended in another study,54 further question the between-day reliability of FL measurement and the similarity of groups

Table 2 Eccentric training characteristics in each study

StudyComparison groups

Duration (weeks)

Total number of sessions Reps/Sets per session

Duration of each exercise (s) Intensity Intervention

Blazevich et al54 1) Eccentric2) Concentric3) Control

10 30 Progressed from 6/4 6/5 6/6 3 s* 1) 50%-100% E1RM

2) 50%–100% C1RM

1) Eccentric dynamometry

2) Concentric dynamometry

Duclay et al55 1) Eccentric2) Control

7 18 6/6 3 s (two exercises)

120% C1RM Eccentric dynamometry

Mahieu et al56 1) Eccentric2) Control

6 42 15/3 6 s N/R Eccentric heel drops

Nelson and Bandy57 1) Eccentric2) Stretching3) Control

6 18 6/1 5 s N/R 1) Eccentric hip fl exion with knee extended

2) Static hamstring stretching

Potier et al58 1) Eccentric2) Control

8 24 8/3 5 s 100% E1RM Weights machine

Reeves et al59 1) Eccentric2) Mixed conc/ecc

14 42 10/2 1) 3 s2) 2/3 s (two exercises)

1) 80% E5RM2) 80% C5RM

Weights machine for both

C1RM, concentric one repetition maximum; E1RM, eccentric one repetition maximum; N/R, not reported.*Approximation based on detail provided in the study.

Table 3 Methodological quality of included trials assessed using PEDro scale

Study Random Conceal BaselineBlind assessor

Blind subject

Blind therapist Follow-up ITTA BGA PMV Score

Blazevich et al54 X X X X 6 (High)Duclay et al55 X X 8 (High)Mahieu et al56 X X X 7 (High)Nelson and Bandy57 X X X X 6 (High)Potier et al58 X X X 7 (High)Reeves et al59 X X X X 6 (High)

BGA, between-groups analysis; , meets criteria; X, does not meet criteria; ITTA, intention to-treat analysis; PMV, point measure and variability.

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at baseline. This highlights the need for estimates of reli-ability or repeated baseline measurements when using this approach.55 59 Furthermore, studying a portion of a muscle group such as vastus lateralis may not necessarily refl ect accurately the rest of that muscle group.47 Interestingly, the recent availability of extended fi eld-of-view ultrasound (EFOV-US), has confi rmed that the estimation methods used in three of the four included studies which examined FL are likely to have underestimated FL, and the error involved is not consistent across muscle lengths.62 The availability of EFOV-US appears to be much more reliable and may address these concerns.62 Notwithstanding these legitimate method-ological concerns, the fi ndings are remarkably consistent in all studies.

Mechanism of increasing fl exibilitySarcomerogenesis remains the most likely mechanism by which fl exibility increases after eccentric training, as has clearly been demonstrated after eccentric training in animal studies.39 A prolonged shift in the muscle length-tension curve consistently occurs after repeated bouts of eccentric training,40 suggesting that muscles adapt to mildly damaging eccentric training by sarcomerogenesis. This optimises gen-eration of torque at more extended joint positions, to limit the potential for muscle damage.44 63 The fi ndings of this review further support this hypothesis, with increases in ROM,56 57 FL,54 55 59 or both58 evident after eccentric training. The fact that changes in both ROM60 and FL54 appear to be closely related to changes in the muscle length-tension curve further support this hypothesis.

Clinical implicationsThe magnitude of increase in fl exibility after eccentric training appears to be clinically relevant, and in line with the increases observed after static stretching. For example, a recent review64 demonstrated mean changes of between +6°and +13° in passive knee extension (PKE) ROM following static hamstring stretch-ing, in line with the gains in PKE ROM reported after eccen-tric hamstring training in this review.57 58 Considering ROM defi cits after hamstring injury are typically less than this,29 36 these increases appear to be clinically relevant, notwithstand-ing the fact that all studies in this review involved painfree participants. Similarly, the increase in dorsifl exion ROM (mean change =+6°) reported by Mahieu et al56 is relatively large, and at least matches the increases reported after static stretching.65 It is harder to interpret the clinical relevance of the increases in FL seen after eccentric training, other than to note that FL was signifi cantly increased in each muscle group studied to varying degrees. While it is likely that both measures of fl exibility (ROM and FL) correlate strongly, this has not yet been clearly established, and the pennation angle of mus-cle fi bres may infl uence the relationship. Nevertheless, the one study which examined both ROM and FL58 demonstrated clear improvements in both FL and ROM after eccentric training.

The exact timeframe for improving fl exibility with eccen-tric training is unclear, although sarcomerogenesis is thought to occur within 10 days of starting eccentric training.63 In this review, eccentric training as short as 6 weeks resulted in signif-icant increases in fl exibility.56 57 It is unclear if these increases in fl exibility are maintained after ceasing eccentric training, although it is likely that some ongoing eccentric training would be needed, similar to gains in fl exibility achieved with static stretching.33 35 66

It is not possible to conclusively establish how the gains in fl exibility observed after eccentric training compare with those reported for static stretching. The only study in this review which compared eccentric training and a static stretch-ing programme observed no signifi cant difference between them, with both groups demonstrating large, clinically mean-ingful increases in ROM.57 Given the additional benefi ts of eccentric training in the development of power and injury prevention,67 68 this questions the benefi t of additional static stretching. However, the increases in ROM after eccentric training reported in the two studies of the hamstrings are quite different.57 58 When the actual exercise programmes are analysed, the eccentric training used by Nelson and Bandy57 was not related to maximal baseline strength, and appears to be of relatively low load. Despite this, they report a larger increase in ROM (12.79°) than reported by Potier et al58 (6.9°) after longer duration, higher load eccentric training. Since the eccentric training used by Nelson and Bandy57 incorporated a static hold at end range, their ‘eccentric’ training could be considered a mix of traditional eccentric training and static stretching. Therefore, the improvements in fl exibility after more typical eccentric training in the other fi ve studies may not be as large as those obtained by static stretching. No other study in this review analysed both ROM and FL. Nelson and Bandy57 did not analyse injury rate or changes in torque profi le, such that it is not possible to determine if their pro-gramme improved these other parameters as effectively as tra-ditional eccentric training. There is considerable evidence that eccentric training is associated with improvements in peak torque,67 performance,67 muscle length-tension curves63 and reduced pain and disability.69–72 As a result, even in the event that eccentric training is not as effective as static stretching in increasing fl exibility, these other advantages of eccentric train-ing over static stretching suggest an eccentric component to training is very important.

The two studies to compare eccentric training with other exercise interventions based on strengthening reported dif-ferent fi ndings, despite examining the same muscle (Vastus Lateralis) and using the same outcome measure (FL). Both studies reported that eccentric training increased FL. However, while Reeves et al59 reported a greater increase in FL after eccentric training, Blazevich et al54 observed no signifi cant difference between the two training groups, with a trend for greater increases in FL among the concentric training group. While the population in the Reeves et al study59 was much older, which may infl uence muscular responses to eccentric training,73 the results are very consistent with other studies in this review. The effectiveness of the eccentric training stimu-lus used by Blazevich et al54 is unclear. Typically, exercise gains are magnifi ed in the exercise mode which is trained, such that concentric training increases concentric strength more than eccentric training and vice-versa.59 74 In contrast, Blazevich et al54 reported that while the concentric training group dem-onstrated greater gains in concentric torque than the eccentric training group, there were no between-group differences in eccentric torque afterwards. This suggests that the eccentric training may have been suboptimal, despite being designed relative to one repetition maximum (1RM) ability. Another concern relates to the baseline between-group differences in FL,54 which may also explain why FL continued to increase towards the values of the control group during the detraining period. Furthermore, nearly all of the increase in FL occurred in the fi rst 5 weeks of the 10-week training programme, before a further slight increase in FL after training ceased. This data

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for FL contrasts with data for concentric and eccentric torque in the same subjects, which showed predictable, incremental increases over the 10-week programme, with some rever-sal after training ceased, in line with data from other stud-ies. Blazevich et al54 proposed that the lack of superiority for eccentric training suggests that the ROM through which the muscle is exercised may be more critical than the mode of exercise, which is consistent with the trend for greater fascicle strain observed among their concentric training group. The fact that muscle damage, and the subsequent adaptation, is strongly linked to the length of the muscle while being exer-cised supports this proposal.60 75 76 Furthermore, the changes in FL reported were strongly related to changes in the torque-angle relationship. However, considering the fi ndings outlined above in this study which are at odds with other studies, rep-lication in other studies is required to support the contention that concentric training is as effective a stimulus for increasing FL as eccentric training.

LIMITATIONS AND RECOMMENDATIONSDespite promising results, several limitations must be acknowledged. Since all included studies involved only uninjured participants, care must be taken when extrapolat-ing the fi ndings to people with lower limb injury. Eccentric training is associated with signifi cant postexercise sore-ness77 and poor compliance,77 and these issues may be even greater in injured participants if addition of eccentric load is not managed carefully. However, since injured athletes are more likely to display defi cits in fl exibility,29 there may be greater scope for improving fl exibility. As mentioned earlier, the term ‘fl exibility’ and what tissue properties this actually refl ects, is debatable. The authors who rated study quality were not specifi cally trained in the use of the PEDro scale, which could affect the reliability of the scoring.50 In contrast to the approach typically taken in PEDro rating, we con-tacted the study authors if further information was required, although the authors of one study57 failed to reply with the requested clarifying information.

Whether increases in fl exibility after eccentric training reduce the need for static stretching requires clarifi cation, as while the results of one study57 suggest this, their eccentric training protocol contained a static stretch-type component. Similarly, it is unclear if concentric training done at a suf-fi ciently high load, either through a large ROM or in a length-ened position, is as effective as eccentric training since the two studies54 59 comparing concentric and eccentric training report contrasting fi ndings. Therefore, further research is needed to extrapolate which exercise parameters, including mode, intensity and the ROM used, have the greatest infl u-ence on fl exibility. Ideally, these studies would also evaluate other parameters of muscle function including peak torque and the muscle length-tension curve. Furthermore, while eccentric training may be a useful component in the man-agement of several lower limb disorders,69–72 the precise eccentric training programme which is the most effective at increasing lower limb fl exibility, or indeed improving perfor-mance and/or reducing injury risk, is debatable. For example, despite considerable differences between the eccentric train-ing programmes, all appear to have signifi cantly increased lower limb fl exibility. Future studies will hopefully be able to address the main limitations identifi ed among the stud-ies included in this review. Specifi cally, this would include ensuring baseline comparability between groups, blinding of the outcome assessor, using more accurate EFOV-US or

similar to measure FL, and cross-checking the effectiveness of the training programmes used by also analysing related measures such as peak torque, torque-angle relationships and injury rate.

CONCLUSIONBased on six high-quality studies in different muscle groups, this systematic review demonstrated consistent evidence that eccentric training is an effective method of increasing lower limb fl exibility, measured using either joint ROM or muscle FL in uninjured participants. Combined with evidence that eccentric training is also associated with benefi ts including reductions in pain, disability and injury recurrence, as well as alterations in peak torque, muscle length-tension curves and athletic performance, eccentric training is an important part of lower limb rehabilitation. It remains unclear if the improve-ments in fl exibility with eccentric training reduce the need for static stretching to increase fl exibility, and whether the improvements in fl exibility are similar with other exercise interventions.

Contributors KOS and SMA were involved in conception and design. KOS and NDB independently reviewed the literature. KOS/SMA extracted the study data. SMA and NDB were involved in rating the literature, with KOS acting to mediate disagreements in ratings. All authors were involved in data analysis and interpretation, as well as preparing the manuscript for publication.

Acknowledgements The fi rst author (KOS) is currently on a research fellowship funded by the Health Research Board of Ireland.

Funding One author (KOS) is supported by a Health Research Board of Ireland research fellowship.

Competing interests None.

Provenance and peer review Not commissioned; externally peer reviewed.

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What is already known on this topic

▶ Flexibility is often reduced in athletes with lower limb injury.

▶ Static stretching increases fl exibility, but has little impact on injury risk or recurrence.

▶ Eccentric training has been shown in animal models to be capable of increasing muscle fascicle length, suggesting it may be an option for improving fl exibility.

What this study adds

▶ Eccentric training is an effective means of improving lower limb fl exibility, assessed by either joint range of motion or muscle fascicle length.

▶ This effect is seen in all lower limb muscle groups studied, suggesting the effects are not specifi c to any one muscle group.

▶ This review has highlighted the need to clarify the effects of eccentric training on fl exibility compared with static stretching and other exercise interventions.

Review

Br J Sports Med 2012;46:838–845. doi:10.1136/bjsports-2011-090835 843

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doi: 10.1136/bjsports-2011-0908352012

2012 46: 838-845 originally published online April 20,Br J Sports Med Kieran O'Sullivan, Sean McAuliffe and Neasa DeBurca limb flexibility: a systematic reviewThe effects of eccentric training on lower

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