SYSTEMATIC REVIEW article

Front. Physiol., 25 April 2022

Sec. Exercise Physiology

Volume 13 - 2022 | https://doi.org/10.3389/fphys.2022.873370

The Effects of Eccentric Strength Training on Flexibility and Strength in Healthy Samples and Laboratory Settings: A Systematic Review

  • 1. Department of Biomechanics in Sports, Faculty of Sports Science, Leipzig University, Leipzig, Germany

  • 2. Department of Biomechanics, Institute for Applied Training Science, Leipzig, Germany

Abstract

Background: The risk of future injury appears to be influenced by agonist fascicle length (FL), joint range of motion (ROM) and eccentric strength. Biomechanical observations of the torque-angle-relationship further reveal a strong dependence on these factors. In practice, a longer FL improves sprinting performance and lowers injury risk. Classical stretching is a popular and evidenced-based training for enhancing ROM but does not have any effects on FL and injury risk. However, recent studies show that eccentric-only training (ECC) improves both flexibility and strength, and effectively lowers risk of injury.

Objectives: To review the evidence on benefits of ECC for flexibility and strength.

Methods: COCHRANE, PUBMED, SCOPUS, SPOLIT, and SPONET were searched for laboratory trials that compare ECC to at least one comparison group. Studies were eligible if they examined both strength and flexibility metrics in a healthy sample (<65 years) and met criteria for controlled or randomized clinical trials (CCT, RCT). 18 studies have been included and successfully rated using the PEDro scale.

Results: 16 of 18 studies show strong evidence of strength and flexibility enhancements for the lower limb. While improvements between ECC and concentric training (CONC) were similar for eccentric (+19 ± 10% vs. +19 ± 11%) and isometric strength (+16 ± 10% vs. +13 ± 6%), CONC showed larger improvements for concentric strength (+9 ± 6% vs. +16 ± 7%). While for ROM ECC showed improvements (+9 ± 7%), no results could be found for CONC. The overall effectiveness of ECC seems to be higher than of CONC.

Conclusion: There is clear evidence that ECC is an effective method for changes in muscle architecture, leading to both flexibility and strength improvements for the lower limb. Due to limited data no shoulder study could be included. Further research is needed for the upper body joints with a focus on functional and structural adaptions.

Systematic Review Registration:https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42021283248, identifier CRD42021283248

1 Introduction

High performance sports set high demands on physical abilities due to repeated high loads and limited recovery time. To be able to compete on a high level, a professional athlete needs to train several hours a day to reach a higher performance level. This amount of chronic stress leads to degenerations, lesions and injuries which have been confirmed for lower (; ) and upper body joint structures (; ). While strength training is commonly associated with performance improvements, flexibility training usually serves for recovery purposes and often is cut short in an athlete’s schedule. Therefore, it is important that athletic training aims for simultaneous and multiple effects on flexibility and strength to save time, reduce risk of injury and interruptions of training or so-called time-loss injury ().

Irrespective of any specific joint, it has been shown that flexibility and strength are highly modifiable (; ; ). Considering the fact that the muscle-tendon-unit contributes 51%, and therefore the greatest portion, to a joint’s flexibility (), muscle training has great potential for ensuring both high performance and injury prevention. Especially for muscle controlled joints, like the shoulder, multi-effective intervention strategies () are required to avoid prominent injuries like the “throwing-shoulder” () in overhead sports.

Common prevention and rehabilitation strategies are stretching, as conventional flexibility training, and concentric training (CONC). A combination of both prevention strategies requires a lot of training time but lacks effectiveness (). Examined for the lower limb, neither stretching (; ) nor concentric training () show evidence of fascicle lengthening. If reduced fascicle length (FL) is associated with increased injury risk () stretching seems to be inappropriate for injury prevention (). In contrast, eccentric training (ECC) for the lower limb additionally aims for flexibility-modification and leads to an increased FL () as well as isokinetic torque gains (). ECC also has a higher impact on concentric torque than CONC does on eccentric torque (). Due to its strong impact on muscular excursion range and eccentric torque, ECC might have two major effects: 1) enhanced motor performance due to an improvement of the acceleration way and torque production which might also lead to a lowered risk of injury for any joint; 2) enhanced muscular energy absorption in the decelerating limb after highly demanding concentric actions with a buffering effect on surrounding structures. The first assumption is based on research showing that ECC lowers the risk of injury by up to 70% (; ) and has benefits on motor performance (). The second assumption is based on higher flexibility benefits in muscles compared to various tissues (; ).

The existing systematic reviews and meta-analyses (; ; ) have not included concurrent multivariate effects on flexibility and strength and are solely focusing on the lower limb. Furthermore, most of the reviewed studies have incomparable study designs because of different definitions of eccentric training and insufficiently detailed descriptions of the eccentric training stimulus (e.g. ; ). Also, many studies of flexibility strength training have low methodological ratings and provide confusing data (; Toigo and Boutellier, 2006).

Therefore, the aim of this review is to investigate whether ECC is capable of improving both strength and flexibility within highly standardized settings and therefore extend existing knowledge on the effects of ECC (; ). For this purpose, the authors reviewed longitudinal studies that compared ECC to a comparison group in healthy adults. All reviewed studies meet RCT or CCT criteria. Parameters such as torque, force or load for strength and range of motion (ROM) for flexibility were compared between the different interventions. Due to this approach, we intend to highlight the multidirectional effect of ECC and, thus, its significance for injury prevention and performance enhancement.

2 Methods

This systematic review is reported in accordance with the PRISMA-statement () and is registered (CRD42021283248) in PROSPERO database.

2.1 Eligibility Criteria

This systematic review includes peer-reviewed RCT and CCT from 1999 to 2021. According to the PICOS eligibility criteria (

) studies have to show the following factors to be eligible for analysis:

  • • Population: healthy male or female adults (18–65 years of age), free of injury or neuronal disease, and recreationally active or used to strength training.

  • • Intervention: eccentric-only training (very low to no load in the concentric phase) within a laboratory setting with a training volume of at least two sessions per week

  • • Control: CONC, stretching or non-intervention control group

  • • Outcomes: flexibility (ROM and/or FL) and strength (torque, force, or load, and/or pennation angle [PA]).

  • • Study design: longitudinally studies (at least 4 weeks), measuring long-term effects on RCT or CCT.

Articles that did not meet the inclusion criteria were excluded from this systematic review.

2.2 Search Strategy and Selection Process

COCHRANE, PUBMED, SCOPUS, SPOLIT, and SPONET were searched by one author (SV). The search syntax included three search groups: eccentric (in abstract/title), flexib* (in abstract/title) and strength (in full text). As described in Table 1, the search groups were linked with the operator “AND”. Within each group “OR” was used to widen the search by using further synonyms. With the final syntax of step 29 (Table 1), the search was implemented in all databases. All searches were filtered for RCT, CCT, and publication date (2011–2021). Since the review of already included a systematic literature search from 1999–2010 with the same aim of research, we included its selected studies after the screening phase (described in Figure 1) and selected those studies who met the eligibility criteria of our systematic review.

TABLE 1

StepSearch terms (June 2020)N in PubMed
Filtered: RCT, CCT, 10 years
1Eccentrica (T/A)556
2Ecca (T/A)165
3Exzentrischa (T/A)0
4(1) OR (2) OR (3)671
5Flexiba (T/A)2,231
6“Range of motion” (T/A)1865
7“Range of movement” (T/A)142
8“Joint range” (T/A)71
9“Joint angle” (T/A)37
10“Fascicle length” (T/A)45
11“Fascicle angle” (T/A)4
12Rom (T/A)776
13FL (T/A)229
14Lengthening (T/A)129
15Elongation (T/A)107
16Stretcha (T/A)1,028
17Expana (T/A)2,381
18(5) OR … (17)7,784
19Strength8,754
20Training43,646
21Loading3,143
22Workout116
23Intervention194,619
24Exercise25,005
25Session17,425
26Krafttraininga4
27Übunga2
28(19) OR … (27)201,812
29(4) AND (18) AND (28)122

Example for the development of search syntax.

a

search for all kinds of word-endings; (T/A), search in title and abstract; (1), includes results of step 1; AND, operator AND combines all search groups; CCT, controlled clinical trial; N, number of records; OR, operator OR combines search terms of specific search step; RCT, randomized controlled trial.

FIGURE 1

Study selection included three major steps (Figure 1). After identification of studies, first and fast selection was based on title. If a title clearly showed a different topic or focus, other languages than English or German, the study was excluded. The second step was based on title and abstract. Studies were excluded if they conducted experiments on animals, focused on post-surgery training, training of injured athletes or did not focus on flexibility and strength. Full-text screening included a check for defined eligibility criteria. Therefore, studies were excluded if they showed insufficient ECC or testing protocols for flexibility and strength metrics, no laboratory settings, no comparison group, and if the full text could not be obtained from database or authors.

2.3 Data Extraction

Two authors (SV, HPK) independently extracted and cross-checked the following data:

  • a) Studies’ characteristics: authors and year, specifics of study, participants, activity level and health status, outcome variables,

  • b) Training protocol: training groups, exercises, number of training weeks and sessions, within training the number of sets and repetitions, intensity of training, range of motion and duration of each movement,

  • c) Methodological quality: description of exclusion criteria, randomization, concealment, baseline values, blinded subjects, blinded therapist, blinded assessor, follow-up/post-test, intention to treat, between group analysis, point measures and variability,

  • d) Results: FL, ROM, PA, eccentric, concentric and isometric strength.

2.4 Assessment of Methodological Quality

As a reliable () and valid tool () for rating methodological quality of studies, the PEDro scale was used independently by two authors (SV, HPK). The third author (AS) cross-checked the results and all three authors reached consensus. The classification of study quality can reach from “poor” (<4/11) over fair (4–5/11) to high (>6/11). A publication bias exists because articles were only searched in online databases. Performance criteria for flexibility and strength measurements were appraised and lead to a pre-selection of studies due to strict eligibility criteria.

2.5 Data Synthesis

All joints and muscle groups were analyzed together to show consistent evidence of ECC on any joint’s flexibility and strength. Due to the amount of data, simple pooled analyses were conducted to summarize results for a quick overview. Complex pooled analyses were not part of this systematic review.

3 Results

3.1 Study Selection

As outlined in Figure 1, a total of 3,295 studies were identified via databases and registers as potentially relevant papers. After manually removing duplicates 777 records remained. The manual screening for title excluded 631 records. 146 records were screened for title and abstract. 54 reports were eligible for full-text analyses.

Additionally, the hand-search of references revealed 17 records, of which 6 were included in the systematic search of and of which 11 originated from different articles. The screening for title and abstract revealed 11 studies eligible for full-text analyses. 54 + 11 records met criteria for full-text analysis of which 47 were removed including 3 articles of . In the end a total of 18 studies met all inclusion criteria (; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; Uysal et al., 2021) and were included in this systematic review.

3.2 Description of Included Studies

Presented in Table 2, the number of participants ranged from n = 12 () to n = 60 subjects (). Samples’ mean age ranged from 19 () to 28 years (; ). 11 of the 18 studies included males only (; ; ; ; ; ; ; ; ; ; Uysal et al., 2021). 15 studies examined FL changes by ultrasound (; ; ; ; ; ; ; ; ; ; ; ; ; ; ). 6 studies measured ROM either with isokinetic dynamometer (; ), sit-and-reach-test (; Uysal et al., 2021), a 3D-video recording (), or a goniometer (). 3 studies measured FL and ROM concurrently (; ; ).

TABLE 2

StudySpecifics of studyParticipants (mean age)Activity level/Health statusOutcome flexibilityOutcome strength
Trained vs. untrainedm (n = 60); 21 yearActive; > 1 year without injury/complicationsROMMVC
CONC vs. ECC; region specific changesm (n = 16); 23 yearActive (>1 h/day; at least 3 days/week); no injuriesFLMVC, iMVC, PA
CONC vs. ECC; follow-upw/m (n = 33); 23 yearActive; no history of lower limb injury; no co-existing medical conditionFLMVC, PA
NHE vs. hip extensions; allocation by FLm (n = 30); 22 yearActive; no injury/strain for structures next to core, hips or kneeFLload (kg)
IK vs. ILm (n = 49); 20year>6 months no strength training; no knee injury/complicationFLMVC, iMVC, load (kg) PA
Four field exercisesm (n = 27); 23 yearActive; Sports with running actions; No injury of lower limb or history of knee surgeryROMMVC
Examining active and passive stiffnessm (n = 18); 23 yearActive; students without neurological injury/diseaseFLiMVC, PA
CONC vs. ECC; allocation by FLm (n = 30); 23 yearActive; no history of hamstrings/knee injuryFLiMVC, load, PA
CONC vs. ECC; allocation by strengthm (n = 12); 25 yearUntrained; health status not reportedFLiMVC, PA
IK vs. ILm (n = 31); 20 yearUntrained; healthy; no history of knee injuryFLMVC, iMVC,PA
Examining tendon stiffness and energy storage; allocation by sexw/m (n = 26); 28 yearActive; no history of lower limb injuryROM, FLMVC, iMVC, PA
NHE-modified for more stretching; sample has to be able to control at least 50% of ROM of NHEw/m (n = 34); 24 yearActive (>3 h of physical activity/wk); >12 months free from neural, muscular, skeletal, or connective tissue injuriesFLMVC, iMVC, PA
Age 20–50 yearsw/m (n = 22); 28 yearNo musculoskeletal injury; no co-existing medical conditionsROM, FLload (kg), PA
NHEw/m (n = 20); 25 yearActive; >1 year no lower limb injury; no history of hamstrings strainROM, FLMVC, iMVC, PA
NHEw/m (n = 20); 19 yearActive; no history of hamstrings injuries; No BMI >30 kg/m2FLMVC
Studying dose-response-relationshipw/m (n = 31); 27 yearFLiMVC
CONC vs. ECC; follow-up; allocation by FLm (n = 28); 22 yearActive; > 1 year no injury of lower limbFLMVC, PA
Uysal et al. (2021)NHE vs. CONC vs. NMES; relation between visco-elastic properties and flexibility/strength changesm (n = 40); 22 yearActive (<2x/week); no musculoskeletal or neurological problems, chronic pain, restrictions to execute exerciseROMiMVC

Studies’ characteristics.

—, not reported; <, less than; >, more than, CONC, concentric training group; d, days; ECC, eccentric training group; m, men; n, sample size; FL, fascicle length; iMVC, isometric MVC; IK, isokinetic training; IL, isoload training; mo, months; MVC, maximum voluntary contraction; NHE, nordic hamstrings exercise; NMES, electronical stimulation of muscle; PA, pennation angle; ROM, range of motion; w, women; wk, weeks; vs., versus; y, age in years.

All studies examined strength changes from pre to post intervention. 11 studies tested for isometric strength (; ; ; ; ; ; ; ; ; ; Uysal et al., 2021). 10 studies tested isokinetic strength (; ; ; ; ; ; ; ; ; ). 2 studies used field exercises for training and testing (; ). 1 study () tested for a 1RM with a hamstrings curls machine. Injured or previously injured samples were not part of any selected study. Eligibility criteria were similar between studies.

3.3 Characteristics of Eccentric Training

Training protocols were very heterogeneous between studies. 13 studies compared effects of a training group versus a non-training control group (; ; ; ; ; ; ; ; ; ; ; ; ). showed a non-training control limb. 11 studies showed more than one training group, thereof 6 studies had a CONC comparison-group (; ; ; ; ; Uysal et al., 2021), and 4 studies compared different ECC protocols (; ; ; ; ). 7 of 18 studies trained participants with an isokinetic dynamometer (; ; ; ; ; ; ), 8 with other machines (; ; ; ; ; ; ; Uysal et al., 2021), and 7 studies used different eccentric field exercises (; ; ; ; ; ; Uysal et al., 2021).

The average duration of intervention was 7.1 ± 2 weeks, ranging from 4 () to 10 weeks (; ; ; ). An average of 2.7 ± 0.8 sessions per week was documented, ranging from 1 (; ; Uysal et al., 2021) to 5 sessions (). Only 3 studies showed interventions lasting less than 6 weeks (; ; ). The average number of sets was 4.5 ± 1.2 sets with a minimum of 2 sets (; ; ; ; ; Uysal et al., 2021) and a maximum of 6 sets (; ; ; ; ). Repetitions per set show an average of 9.1 ± 2.8 repetitions, ranging from 5 (; ; ; Uysal et al., 2021) to 16 repetitions (). Duration of a repetition ranged from less than 1 s () to 5 s (; ). Training intensity ranged from 40% () to at least 100% of the concentric 1RM (; ; ; ; ; ; ; ; Uysal et al., 2021). 4 studies did not report training intensities (; ; ; ). ROM during training varied between 40° () and 85° or full ROM (; ; ; ; ; ; ; ). Table 3 presents further details on training characteristics.

TABLE 3

StudyExercisesWeeks x sessions/PauseSets x reps/PauseIntensity (%1RM)ROM & duration
Pulley system; horizontal; p.f. hips (90°), p.m. knee6 × 5/-6 × 5/-40%
IsoDyn:5 × 2/>48 h4 × 8/60 sAll-out—; 30°/s
IsoDyn; seated; p.f. hips; p.m. knee10 × 3/>24 h4>6 × 6/60 s90%ecc/conc85°; 3 s
ECC NHE: p.f. hips, p.m. knee; ECC HE: Hip extension machine (45°): p.f. knee, p.m. hips10 × 2/>48 h2>6 × 6>10/120 s60–80%90°; —
ECC IK: isoDyn; ECC IL: knee extension machine6x2/>48 h5 × 8/120 s120%conc85°; —
NHE; three other exercises: p.f. knee, p.m. hips6x2-3/>48 h2>3 × 6>10/120 sAll-out
Calf machine or leg press, full support for weight return; p.f. knee, p.m. foot7x2-3/-6 × 6/180 s120%conc50–60°; ∼3 s
NHE5 × 2<1/>48 h2>5 × 6/--80–90°; -
Leg press, full support for weight return; p.f. knee, p.m. foot10 × 3/-4x8-10/60 s80%—; 2–3 s
IsoDyn; horizontal; p.f. hips, p.m. knee9 × 2/—3>5 × 8/—Controlled by total work100%conc/all-out60°; —
IsoDyn; seated; p.f. hips, p.m. knee6 × 2/>48 h5 × 12/60 s>80%90°; 3 s
NHE-modified: p.f. hips 75°, p.m. knee; Askling’s-glider: p.f. knee, p.m. hips6 × 2/—2>3 × 5>8/—>50%ROM; 3–5s
Hamstrings-curls; p.f. hips, p.m. knee8 × 3/—3 × 8/—100%eccMaximum; 5 s
NHE4 × 2/—3x6-10/60 s—, @4 s
NHE6 × 1>3/—2>3 × 5>12/—
1–4) ECC low load, high load, low ROM, fast: isoDyn; p.f. hip, p.m. knee; subject 1: protocol 1 & 2, subject 2: 3 & 410 × 3/—1) 5 × 10 2) 5 × 6 3) 5 × 12 4) 5 × 16 Controlled by total work1) 65%ecc 2–4) 100%1–4) 75°; ∼1 s 1) 40°; <0,5 s
IsoDyn; seated; p.f. hips (85°), p.m. knee6 × 2>3/>48 h4>6 × 6>8/30 sAll-out90°; <1.5 s
Uysal et al. (2021)ECC NHE; CONC: hamstrings leg curl machine, lying, p.f. hips, p.m. knee8 × 1>3/>24 h2>3 × 5>12/120 sAll-out until full ROM reached

Eccentric training protocols.

—, not reported; °, degrees of angle; >, more than; CONC, concentric training; conc, concentric strength; CG, control group; ECC, eccentric training; ecc, eccentric strength; h, hours; HE, hip extensions exercise; IK, isokinetic mode; IL, isoload mode; isoDyn, isokinetic dynamometry; NHE, Nordic hamstrings exercise; p.f., punctum fixum; p.m., punctum mobile; RM, repetition maximum; ROM, range of motion; s, seconds; x, times

3.4 Methodological Quality

Quality results are presented in Table 4. Based on the PEDro scale, every study received “high quality” rating ranging from 6 to 9 points. All studies were conducted under a concealed condition. Except , all studies reported clearly their exclusion criteria for the investigated groups. Apart from who divided the sample in advance according to the factor “training level”, the rest of the included studies showed clear characteristics of a randomized controlled trial (RCT). 5 studies reported specific allocation methods to equalize groups for strength (; ) or FL (; ; ). 3 studies reported baseline differences between groups (; ; ). This might affect adaptability of each group and could also explain different outcomes (see discussion). Blinding did not take part in any trial with exception of blinding the assessor in 3 studies (; ; ). All trials reported follow-up tests with at least 85% of participants as well as “between group analysis” (BGA) and “point measurements and variability” (PMV). 2 studies did not fulfill the intention-to-treat criteria (; ).

TABLE 4

StudyExclusion criteriaRandomConcealBaselineBlind subjectBlind therapistBlind assessorFollow-upITTABGAPMVScore
101100011117
111100011118
111100011118
111100111119
111100011118
111100111119
111100011118
111000011117
111000011117
111100111119
111100010117
111100011118
111000011117
111100011118
111100011118
011100010116
111100011118
Uysal et al. (2021)111100011118

Rating of methodological quality.

0, does not meet criteria; 1, meets criteria; BGA, between-group-analysis; ITTA, intention to-treat analysis; PMV, point measure and variability.

Bold values: total score for each study.

3.5 Description of Results

Table 5 shows the results of the 18 included studies. Since different muscle groups are involved, percentage changes in each parameter were extracted from all studies. If not provided by the authors, pre-post values were used for calculation of percentage change (underlined letters, Table 5). Based on these values, simple pooled analyses were conducted for ECC, CONC and control group (CG).

TABLE 5

StudyGroups∆ Eccentric strength∆ Concentric strength∆ Isometric strength∆ ROM∆ PA∆ FL
1) ECC trained7.6% IK 60°/s0.6%−11.4%
2) ECC untrained15%1,5%−19.6%
3) CG0.6%1.3%2.8%
1) ECC12.61%12.31%11.42% @ 70°4.09%*7.23%*
2) CONC13.41%11.09%10.71%1.36% distal-end0%
1) ECC38.9 ± 14.2% : IK 30°/s16.4 ± 5.1%21.4 ± 6.9% VL3.1 ± 1.6%
2) CONC35.9 ± 12.7%24.1 ± 4.2%*13.3 ± 3.0%6.3 ± 3.0%
3) CG3.0 ± 3.2%0.5 ± 1.8%0.4 ± 3.6% VL−0.3 ± 0.9%
1) ECC NHE97.38 N/26 kg NHE/HE2.22cm
2) ECC HE110.47 N/41kg1.33 cm
3) CG8.91 N/3.50 kg
1) ECC IK32.4%* IK 60°/s7.7%14.4%11.6%15.1%
2) ECC IL12.9%5.2%5.9%4.6%14%
3) CG−3.8%−4.7%−2.2%4.9%1.3%
1) ECC7.1% IK 30°/s7.2%: IK 60°/s12.7%
2) CG−3.3%−2%N.s
1) ECC13.3%7.6%6.8%
2) CGn.sn.s
1) ECC24% NHE−5%13%
2) CONC13%12%*6%
1) ECC11 ± 8%5 ± 1%12 ± 2%*
2) CONC9 ± 6%30 ± 0.5%*5 ± 1%
1) ECC IL+15 ± 4% IK 180°/s18 ± 3%16 ± 3%11 ± 6%*−3%
2) ECC IKn.s8 ± 3%14 ± 3%n.s3.4%
3) CGn.sn.sn.sn.sn.s
1) ECC29.5 ± 15.8% IK 30°/s17.4 ± 7.9%3.5%9.0 ± 2.8%−0.7 ± 0.9%
2) CG5.0 ± 2.8%−6.3 ± 4.8%−0.5%0.8%−0.9 ± 2.2%
1) ECC16.76% IK 60°/s18.05%16.67%11.43%7.49%
2) CG0%0.55%−1.99%0.77%−0.5%
1) ECC34.2% 1RM curling5%−2.9%33.5%
2) CG3.5%1.2%6.5%16.6%
1) ECC14.4% IK 60°/s12.3%9.6%0.4%−16,86%21.77%
2) CG1.2%3.1%2%4.1%1%2%
1) ECC11.6% IK 60°/s9.6%1.2%
2) CG4.6%(12.4°)0.1%
1) ECC low loadsignificant changes between 30–70°n.s
2) ECC high loadsignificant changes between 25–65°n.s
3) ECC low ROMsignificant changes between 30–60°n.s
4) ECC fastsignificant changes at 45°14%*
5) CGn.sn.s
1) ECC16.6% IK 60°/s16.5%−7.5%16.4%
2) CONC14.4%13.1%20.1%−11.8%
3) CG (second limb)
Uysal et al. (2021)1) ECCup to 44%*3.64 cm sit and reach
2) CONC20.4%2.58 cm sit and reach
3) NMES11.9%0.21 cm sit and reach
Total1) ECC+19 ± 10%+9 ± 6%+16 ± 10%+9 ± 7%+5 ± 7%+10 ± 9%
2) CONC+19 ± 11%+16 ± 7%+13 ± 6%+15 ± 11%−1 ± 8%
3) CG−1 ± 3%−1 ± 3%−3 ± 2%−2 ± 2%2 ± 3%+3 ± 6%

Study results.

Bold letters, significant change from pre-to-post or vs. CG; underlined letters, calculated based on pre-post-values; values within brackets, possibly wrong reported; -, not reported; °, degrees of angle; ±, standard deviation; *, significant improved vs. other training-group; CG, control group; CONC, concentric training; ECC, eccentric training; FL, fascicle length; IK, isokinetic mode; n.v., no pre-post values reported; HE, hyperextension exercise; IL, isoload mode; Nm, Newton meter; NHE, Nordic hamstrings exercise; NMES, neuromuscular electro stimulation; n.s., not significant without pre-post-values reported; italic letters, no pre-post values reported; PA, pennation angle; RM, repetition maximum; ROM, range of motion; TAR, measurement of torque angle relationship each 5°; VL, m. vastus lateralis; vs.; versus.

Among the 18 studies of this systematic review, a total of 25 ECC subgroups were identified and considered for the description of results. All included studies reported at least one result for functional strength changes (either eccentric, concentric or isometric) and flexibility changes (either range of motion, sit-and-reach or fascicular lengthening). Since a change in PA is understood as a change in strength by cross-sectional hypertrophy (), this parameter is also listed in Table 5 as a morphological surrogate for strength.

3.6 Functional and Morphological Strength Changes

3.6.1 Eccentric Strength

18 ECC subgroups were tested for eccentric strength, 3 groups without significant changes (; ). Results ranged from +7.1% () to +38.9% () enhancement in eccentric strength.

Simple pooled analysis of 15 ECC subgroups (; ; ; ; ; ; ; ; ; ; ; ; ) showed an average improvement of +19 ± 10% of eccentric strength. 4 subgroups with CONC revealed +19 ± 11% improvement (; ; ; ; ; ; ; ; ; ). 10 inactive CGs showed no significant change (−1 ± 3%) in eccentric strength (; ; ; ; ; ; ; ; ; ).

3.6.2 Concentric Strength

Concentric strength values were reported for 12 ECC subgroups, 6 of which showed no significant changes (; ; ; ). Results ranged from a non-significant gain of +0.6% (; ) to +18% () enhancement in concentric strength.

11 ECC subgroups were used for simple pooled analysis (; ; ; ; ; ; ; ; ). After ECC, concentric strength improved by +9 ± 6%. 3 CONC groups showed an mean improvement of +16 ± 7% (; ; ). CGs reported no change (−1 ± 3%) in concentric strength (; ; ; ; ; ).

3.6.3 Isometric Strength

All of 15 ECC groups revealed isometric strength gains. Results varied between +5.9% () and a significant gain of +44% (Uysal et al., 2021) after ECC. In contrast, the maximum improvement in isometric strength after CONC was +20.4% (Uysal et al., 2021).

For the simple pooled analysis, 11 ECC subgroups were included (; ; ; ; ; ; ; ; ). ECC improved by +16 ± 10%. 3 CONC subgroups showed mean isometric strength changes of +13 ± 6% (; ; Uysal et al., 2021). No significant changes (−3 ± 2%) were seen in CGs (; ; ).

3.6.4 Pennation Angle

PA values were reported for 15 ECC subgroups, 7 of which showed no significant changes (; ; ; ; ; ). Results ranged from −16.9% () to +21.4% ().

14 ECC subgroups were used for simple pooled analysis (; ; ; ; ; ; ; ; ; ; ; ; ). After ECC the average angular change in PA was +5 ± 7%. In comparison, 5 CONC subgroups showed an average PA change of +15 ± 11% (; ; ; ; ). 6 CGs showed no significant values with an average PA change of 2 ± 3% (; ; ; ; ; ).

3.7 Functional and Morphological Changes of Flexibility

3.7.1 Passive Range of Motion

7 subgroups were tested for ROM, 1 of which showed no significant changes (). Results ranged from −19.6% () up to +12.7% improvement ().

Simple pooled analysis of 6 ECC subgroups showed an average ROM improvement of +9 ± 7% (; ; ; ; ). 4 CGs revealed a mean decrease of −2 ± 2% (; ; ; ). None of the studies including CONC interventions did report ROM values.

3.7.2 Muscle Fascicle Length

FL values were reported for 21 subgroups, 7 of which showed no significant changes (; ; ; ). Results ranged from a non-significant result of −3% () to a significant improvement of FL by +33.5% ().

Simple pooled analysis revealed an average gain of FL by +10 ± 9% for 16 ECC subgroups (; ; ; ; ; ; ; ; ; ; ; ; ). 5 CONC showed an average change of −1 ± 8% (; ; ; ; ). 7 CGs reached an average FL change of +3 ± 6%, all of which were non-significant (; ; ; ; ; ; ). Only reported differences of FL change between ECC and CONC subgroups and found a significant higher gain in FL after ECC (+7%) than after CONC (0%).

4 Discussion

4.1 Main Findings

17 of 18 studies showed significant improvements in at least one strength parameter and 16 of 18 studies in at least one flexibility parameter after ECC. This can be seen as a very consistent result which could also be concluded from comparable review articles (; ; ; ; ). Further, results are independent of the included muscle groups. Simple pooled analysis of ECC revealed overall positive changes of +19% for eccentric, and +9% for concentric strength, +10% for FL and +9% for ROM. In contrast, CONC also shows improvements in eccentric (19%) and larger effects for concentric (16%) strength but could not improve FL (−1%) (Table 5). Therefore, there is clear evidence that ECC concurrently improves flexibility and strength parameters by combining the benefits of strengthening and stretching interventions in one exercise.

4.2 Interpretation of Results

The main findings of this review describe a large benefit of ECC compared to CONC. While observed strength improvements between ECC and CONC are comparable (e.g. ; ), the induced change in ROM is much larger in ECC compared to CONC which shows no changes in ROM. A comparison of studies on stretching show that the ROM improvements caused by ECC are comparable to specific stretching exercise like ballistic stretching (11%), but minor compared to static exercises (18–21%) (). However, since ECC shows effects for both stretching and strength, it has multiple effects and is therefore suitable for improving training efficiency. What is further unique to ECC is fascicle lengthening, which is neither induced by CONC () nor by stretching (; ).

The effects described for ECC may be explained by several mechanisms. The most important mechanism which can explain improvements of a torque-angle relationship is sarcomerogenesis (). It leads to a longitudinal hypertrophy of muscular fascicles. This happens after a repeated overstretch of muscular structures follow by a reconstruction and addition of sarcomeres in order to avoid further traumas of the muscle within the “new” ROM (Toigo and Boutellier, 2006). Therefore, most studies examine a change in FL to describe a possible addition of sarcomeres in series. If maximum degrees of ROM get barely used, an atrophic response can follow fast (Toigo, 2019). This reaction is characterized by a significant reduction of FL after detraining (). A positive change in FL is reported to be closely related to shifts in the torque-angle relationship after ECC for the vastus lateralis (). This is confirmed by a second study showing that sprinting performance is positively associated with a fascicles’ length (). Therefore, exercises combining stretching and strengthening, such as ECC, seem to be most effective in simultaneously increasing strength and flexibility. The result is a gain in motor performance () and a highly relevant reduction of injury risk by improving FL, strength and ROM as three of the most important risk factors (Wilk et al., 1993; ; ). Nevertheless one study calculated the correlation between a change of FL and ROM without a significant result ().

In contrast to the main findings and their accordance to literature, several studies showed opposite and unexpected results for ROM (), FL (; ; ; ), PA (; ), eccentric strength (; ), or concentric strength (; ; ; ). Whereas positive ROM, FL and eccentric strength changes are common after weeks of ECC (; ) and a longitudinal hypertrophy seems obvious, a positive change in PA or concentric strength can be interpreted as a sign of radial hypertrophy (; ). Whereas most of the studies show results in accordance with literature, 2 studies (; ) do not show any relevant change in flexibility or strength and are worth discussing.

revealed a non-significant eccentric strength change of +11.6% for ECC in contrast to −4.6% for CG. This percentage change lies in between the lowest significant result reported by with +7.1% and the overall average change of +19% across all included studies. To explain differences within the results, we compared the methods of training and testing which led to several possible reasons for this unusual result. At first, examined the impact of a field exercise (NHE) on flexibility and strength resulting in lower improvements compared to exercises on a very standardized training machine such as an isokinetic dynamometer (e.g. ; ; ). Second, show 6 weeks of intervention and within each session a load of 12 repetitions and 3 sets in total. The average training load across all included studies showed 7 weeks of training, more than 4 sets per training and more intense workouts on a weight machine (Table 3). Therefore, the chosen training load in the reported study of is not only below average, it also appears to be below the recommended load for stimulation of longitudinal and cross-sectional hypertrophy of the skeletal muscle (Toigo and Boutellier, 2006; ; ). Third, only tested for isokinetic eccentric strength, which was non-significant for another 2 subgroups (). In contrast to eccentric or concentric dynamic testing, isometric tests revealed significant improvements for all 15 subgroups (Table 5). It shows that an isometric test can reveal hidden information on multiple effects of ECC.

Interestingly, do not show any of these differences in testing and training. Nevertheless, both studies (; ) also reported no change in any flexibility parameter. A possible explanation for was a lack of overloaded stretch resulting in a low stimulus for sarcomergenesis. Since showed that ROM and movement velocity need to be higher than usual to enhance FL, we can share the interpretation of . At the very end of a movement when Titin has to compensate for a muscles’ continued extension, the rising stress on the muscle-tendon-unit also raises the probability for sarcomerogenesis (). Interestingly, the unexpected and positive change of PA within both studies (; ) may have led primarily to a radial and not to a longitudinal hypertrophy (associated with a positive change in FL) of the muscle (; ). This may confirm the hypothesis that both training protocols included significantly fewer stimulus of flexibility training and more stimulus typical for strength training.

Another explanation for an unexpected lack of FL improvement may be the employed test method. It is a fact that ultrasound is very economic compared to other methods of measurements such as magnet resonance imaging (MRI, ) or even biopsy (). The downside is its lowered reliability () compared to MRI () or an extended field of view ultrasound (EFOV, ). Especially a different handling and positioning of ultrasound can change results () which may explain why found a +47% fascicular lenghening in pre-study observations compared to a non-significant result after ECC isokinetic training in the main study. Since a classical ultrasound may also lead to an underestimation of FL by up to +20.3% (; ), it can be seen as another possible reason for low changes of FL observed in both studies (; ). The fact that sarcomer length and elongation are not uniform across the muscle () and that a classical ultrasound allows a limited view of bigger muscles (), emphasizes the need for MRI, EFOV, or 3D ultrasound (Uysal et al., 2021) applications.

5 Limitations and Recommendations

Several limits of this systematic review have been observed. Due to the reviews’ exclusive focus on healthy samples, laboratory settings and long-term interventions with RCT characteristics, some interesting trials could not be included. Especially interventional studies examining the shoulder joint (; ; ; Uhl et al., 2017) did not meet the inclusion criteria. Therefore, we were not able to interpret the effects of ECC for the shoulder as planned. Exclusion of injured samples and studies with a focus on easy-to-implement interventions further limit this review. We are not able to fully understand the effectiveness of ECC implemented in frequent athletic training. In addition, we do not know the effects of ECC compared to conventional athletic training. Most studies used an isokinetic dynamometer to maximize intensity and validity of training. Based on trials of and , it seems to be clear which ECC training stimulus is needed for improvements in FL, ROM and strength. Also, studies by and helped to unterstand the different responses after ECC or CONC and the time course of adaption.

Since Zandt et al. (2010) realized that there exist few ECC studies on the shoulder joint, future studies and review articles need to focus on the upper body joints. This is also relevant because of the anatomical and physiological differences between a shoulder and a knee joint which will lead to different reactions after ECC (Zandt et al., 2010). It also seems to be important to review studies comparing ECC to conventional athletic training with a focus on its consequences on sport-related performance metrics.

6 Conclusion

The results of 18 laboratory and multivariate studies show that ECC is a multi-effective intervention strategy for the lower limb. Not only the magnitude of change but also the amount of significant changes for several flexibility and strength metrics reveal benefits compared to classical strength training. ECC combines both stretching and strengthening in one exercise. In conclusion, especially risk factors like low eccentric strength, FL, and ROM can be improved best with ECC. It remains unclear whether this can be achieved similarly for other regions than the legs and other samples.

Statements

Data availability statement

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

Author contributions

We confirm that all authors mentioned were involved in this systematic review and in the preparation of the manuscript. SV, HPK, AS and MW developed the conception and study design. SV conducted the systematic literature search. SV extracted the data of the selected studies. SV and HPK independently rated the methodological quality of studies, mediated by AS. SV and HPK analyzed the data. SV prepared and developed the manuscript in accordance with all co-authors. All authors were involved in data interpretation, in revision and finalization for publication. SV is the first author. HPK and MW share the last authorship.

Acknowledgments

The authors acknowledge support from the German Research Foundation (DFG) and Leipzig University within the program of Open Access Publishing. We would also like to acknowledge the financial support of Sebastian Vetter within the Pre-Doc Award of Leipzig University.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

References

Summary

Keywords

fascicle lengthening, flexibility training, athletic training, muscle adaptation, resistance training, injury prevention

Citation

Vetter S, Schleichardt A, Köhler H-P and Witt M (2022) The Effects of Eccentric Strength Training on Flexibility and Strength in Healthy Samples and Laboratory Settings: A Systematic Review. Front. Physiol. 13:873370. doi: 10.3389/fphys.2022.873370

Received

10 February 2022

Accepted

31 March 2022

Published

25 April 2022

Volume

13 - 2022

Edited by

Eisuke Ochi, Hosei University, Japan

Reviewed by

Trevor Chung-Ching Chen, National Taiwan Normal University, Taiwan

Xin Ye, University of Hartford, United States

Updates

Copyright

*Correspondence: Hans-Peter Köhler,

This article was submitted to Exercise Physiology, a section of the journal Frontiers in Physiology

Disclaimer

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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