Muscle injuries have a high incidence in sports that involve high-speed movements1 such as track and field,2 rugby,3 basketball,4 soccer,5 and American football,6 as well as in ballet dancers.7 Muscle injuries are responsible for 10% to 55% of all injuries in sport,5,8–10 and they are common at the high school,11 college,12,13 and professional levels.5 About 92% of all lower limb muscle injuries affect hamstrings, adductors, quadriceps, or calf (gastrocnemius and/or soleus), and the hamstring muscles are the most commonly injuried.14 Most of hamstring strain injuries (HSI) are considered of moderate severity (54%), with the athlete losing 17 days of practice on average.15 However, 15% of HSI are severe, which usually requires a longer rehabilitation period (>28-d layoff).15 Furthermore, the reinjury rate of HSI is relatively high, especially when it affects the biceps femoris (18.4%).16 Consequently, HSI impairs athletes’ performance,17 and it has negative financial consequences for the club involved.18,19
With the aim of avoiding all the deleterious effects of an HSI, many studies20–26 have concentrated their efforts in identifying risk factors for HSI in an attempt to contribute to the development of prevention programs. The risk factors can be divided in nonmodifiable (eg, previous injuries, age, and genetics) and modifiable (eg, flexibility, fatigue, eccentric strength, and fascicle length).27,28 Knee flexors eccentric strength29–31 and biceps femoris fascicle length29,32,33 have received great attention in the last decade. For instance, a prospective cohort study29 evidenced that elite soccer players with knee flexors eccentric weakness (<337 N assessed with the NordBord System34) and short biceps femoris long head fascicle length (<10.56 cm) were 4.4 and 4.1 times more likely to sustain an HSI, respectively. Therefore, strategies capable of increasing both eccentric strength and fascicle length seem to be crucial to decrease risk of HSI.
Resistance training is conventionally performed with the same external load during the concentric and eccentric phases, but studies with different populations have demonstrated higher increments in muscle strength through eccentric overload training.35–38 Eccentric training also seems to generate greater strength gains than concentric training.39 Whereas concentric training presents small or nonsignificant impact on either muscle eccentric strength39 or fascicle length,40 training programs with eccentric overload seem to increase both eccentric strength and fascicle length.41,42 In fact, eccentric exercise has been suggested as an effective strategy to prevent HSI,20,24 and the Nordic hamstring exercise (NHE) is increasingly popular among athletes and coaching/medical staffs.43,44
Studies have shown that NHE-based training has the potential to reduce HSI rate in athletes of baseball,25 rugby,3 and soccer,20,22,24,45 and this preventive effect of NHE is further supported by a recent meta-analysis,46 which identified that NHE is capable of decreasing in 50% the incidence of HSI. In face of the promising results of NHE as a preventive strategy against the HSI in athletes, clarifying the mechanisms responsible for the preventive effect of this resistance exercise with eccentric emphasis is pertinent. Hence, this systematic review and meta-analysis aims to analyze the effects of NHE on knee flexors eccentric strength and fascicle length.
Evidence Acquisition
The current study utilized PRISMA (Preferred Reporting Items for Systematic Review and Meta-analyses) guidelines for systematic reviews and meta-analysis.47 Prior to search, a review protocol was completed and registered at PROSPERO (CRD42018092699).
Data Sources and Searches
We searched the following electronic databases (from inception to April 2020): MEDLINE (accessed by PubMed), Physiotherapy Evidence Database (PEDro), and The Cochrane Central Register of Controlled Trials (Cochrane CENTRAL). In addition, we searched the references of published studies. Retrieved references were imported into EndNote X7 (Thomson Reuters, New York City, NY), where duplicates were subsequently deleted. The search comprised the following terms: “Hamstring Muscle,” “Semitendinosus,” “Semimembranosus,” “Biceps Femoris,” “Posterior thigh,” “Muscle architecture,” “Fascicle length,” “Pennation angle,” “Muscle thickness,” “Nordic hamstring exercise,” “Nordic curl,” “Nordic curl exercise,” and “Hamstring injury prevention,” combined with a high-sensitivity combination of words used in the search for randomized clinical trials.48 We included only publications in English. For the combination of the keywords, we utilized the Boolean terms “AND” and “OR.”
Eligibility Criteria
We included randomized clinical trials and controlled clinical trials that evaluated the effects of NHE on eccentric strength and/or fascicle length. In order to improve the clarity of the information provided, the term “strength” will be used to refer the muscle ability to produce force. The following exclusion criteria were used: (1) samples comprised of people with any disease/dysfunction, (2) nonapplication of NHE, (3) nonevaluation of hamstring eccentric strength or fascicle length, (4) application of NHE in association with other exercises, (5) noninclusion of a control group (CG), (6) samples with mean age under 18 years old, and (7) studies with training protocol shorter than 4 weeks or 8 sessions. It should be mentioned that we chose to include participants of both genders because our analyses considered the difference between preintervention and postintervention whether than the peak values. Even though women might present lower peak torque when compared with men,49 the adaptations observed after training tend to be similar. As for fascicle length, a recent investigation has shown that fascicle length does not differ between sexes.50 Thus, the inclusion of both male and female participants is unlikely to affect our results.
Studies Selection and Data Extraction
Two investigators independently evaluated titles and abstracts of all articles identified by the search strategy. All abstracts that did not provide sufficient information regarding the inclusion and exclusion criteria were selected for full-text evaluation. In the second phase, the same reviewers independently evaluated the full-text articles and made their selection in accordance with the eligibility criteria. Disagreements between reviewers were solved by consensus. Using standardized forms, the same 2 reviewers independently conducted data extraction with regard to the methodological characteristics of the studies, number of participants, age, NHE training protocol, outcomes assessments, and results. Disagreements were also solved by consensus. The outcomes extracted were knee flexors eccentric strength (peak force or peak torque) and muscular fascicle length. It is important to highlight that the eccentric peak torque was evaluated by isokinetic dynamometry, while eccentric peak force was assessed during an NHE execution through specific devices with load cells.
Quality Assessment
The methodological quality of each study was independently assessed by 2 investigators, and any discrepancies were resolved by consensus. The quality and risk of bias were evaluated according to the Cochrane risk of bias tool,51 where 4 main domains of bias are assessed: selection bias, detection bias, attrition bias, and reporting bias. Studies without a clear description of these characteristics were considered unclear.
Data Synthesis and Analysis
Intervention effects for strength and fascicle length were calculated using standardized mean differences (SMDs) with 95% confidence intervals (CIs), as all data were continuous. The mean change scores and SDs of the change scores from the intervention and CGs were used to calculate the SMD. If the SDs of the change scores were not reported, these were calculated using the formula,52 where correlation coefficients were conservatively set at .5.53 A positive SMD represents an effect in favor of intervention group and a negative SMD an effect in favor of CG. Statistical heterogeneity of the treatment effects among studies was assessed using Cochran Q test and the inconsistency I2 test, in which values above 25% and 50% were considered indicative of moderate and high heterogeneity, respectively.54 A random effects model was selected for the analysis. All analyses were conducted using Review Manager (version 5.3; London, United Kingdom). For the studies that reported only standard error, we estimated the SD by multiplying the standard error by the square root of the sample size (n). For the studies that presented the values of torque in Newton meter per kilogram,55,56 we multiplied the values by the mean weight of the subjects in order to normalize the results and perform a more complete analysis. Furthermore, it is important to point out that for the study that presented its data only through graphs,57 the values were extracted using the Plot Digitizer.58 We explored heterogeneity between studies by rerunning the meta-analyses removing one paper at a time to check whether some individual study explained heterogeneity.
Evidence Synthesis
Description of Studies
The search strategy yielded 1932 articles, after the exclusion of the duplicates (560 studies) identified by the software Endnote; 1377 titles were analyzed, of which 29 studies were considered as potentially relevant and retrieved for detailed analysis. In the full-text analysis, 17 studies were excluded. Hence, 12 studies met the eligibility criteria and were included in the systematic review (n = 299), and 9 studies presented suitable data for meta-analysis (n = 205). Figure 1 shows the flow diagram of the studies included in this review, and Table 1 summarizes the studies’ characteristics and their main results.
—Flowchart of the included studies. NHE indicates Nordic hamstring exercise.
Citation: Journal of Sport Rehabilitation 30, 3; 10.1123/jsr.2019-0388
Characteristics of the Included Studies
| Study | Groups | Mean age (SD) | NHE training program | Outcomes | Results for hamstring eccentric strength | Results for BFlh fascicle length |
|---|---|---|---|---|---|---|
| Bourne et al57 | 30 active males HE: 10 NHE: 10 CG:10 | HE: 23.1 (4.1) NHE: 21.6 (3.2) CG: 21.3 (3.7) | 2–5 × 6–10 repetitions 2 times per week 10 wk | ECC strength (during NHE) BFsh and ST architecture: FL, ACSA, and VOL | NHE: +26.3% CG: no change | NHE: +20.5% CG: no change |
| Delahunt et al59 | 29 active males NHE: 15 CG: 14 | 22 (1.38) | 2–3 × 5–12 repetitions 1–3 times per week 6 wk | ECC MVC (120 deg/s) EMG activity | NHE: +15.2% CG: no change | NA |
| Delextrat et al60 | 30 female hockey players NHE: 10 HC: 10 CG: 10 | NHE: 19.7 (1.4) HC: 19.5 (1.0) CG: 19.6 (1.4) | 2–3 × 6–10 repetitions 3 times per week 6 wk | ECC PT (120 deg/s) | NHE: 12.4% HC: 7.1% CG: −4.5% | NA |
| Iga et al61 | 18 male soccer players NHE: 10 CG: 8 | NHE: 23.4 (3.3) CG: 22.3 (3.9) | 2–3 × 5–8 repetitions 1–3 times per week 4 wk | ECC PT (60, 120, and 240 deg/s) EMG activity | NHE: +15% CG: no change | NA |
| Ishøi et al62 | 35 male soccer players NHE: 18 CG: 17 | NHE: 19.1 (1.8) CG: 19.4 (2.1) | 1–3 × 5–12 repetitions 1–3 times per week 10 wk | ECC strength (during NHE) RSA 10-m sprint | NHE: +19.2% CG: no change | NA |
| Lovell et al63 | 42 male amateur soccer players CG: 12 NHE before: 14 NHE after: 16 | 23.6 (4.7) | 2–4 × 5–12 repetitions 1–2 times per week 12 wk | ECC PT BFlh architecture: FL, MT, and PA EMG activity | NHE: +11.9% CG: no change | NHE: +12.9% CG: no change |
| Mendiguchia et al64 | 32 soccer players | Not informed | 2–3 × 5–12 repetitions 1–3 times per week 6 wk | BFlh architecture: FL, MT, and PA Sprint performance | NA | NHE: 7,4% CG: −0,2% |
| Mjølsnes et al65 | 21 well-trained male soccer players NHE: 11 HC: 10 | Not informed | 2–3 × 5–12 repetitions 1–3 times per week 10 wk | ECC (60 deg/s) and ISO PT H:Q ratio Flexibility | NHE: +11% CG: no change | NA |
| Ribeiro-Alvares et al66 | 14 active females and 6 active males | NHE: 23.7 (3.3) CG: 26.0 (2.7) | 3 × 6–10 repetitions 2 times per week 4 wk | CON and ECC PT (60 deg/s) H:Q ratio BFlh architecture: FL, MT, and PA Flexibility | NHE: +14.5% CG: no change | NHE: +22% CG: no change |
| Salci et al55 | 25 recreational female athletes NHE: 13 CG: 12 | NHE: 20.5 (1.2) CON: 21.0 (1.6) | 2–3 × 5–12 repetitions 1–3 times per week 10 wk | ECC and CON PT (60 deg/s) | NHE: +10% CG: no change | NA |
| Seymore et al56 | 20 adults: 6 males and 14 females NHE: 10 CG: 10 | NHE: 18.3 (0.5) CON: 19.9 (1.2) | 2–3 × 5–12 repetitions 1–3 times per week 6 wk | ECC PT (60 deg/s) ECC PT (deg) BFlh architecture: FL, PA, VOL, and PCSA Stiffness Passive PT | NHE: +12% CG: no change | NHE: +11.9% CG: no change |
| Suarez-Arrones et al67 | 50 male professional soccer players NHE1: 16 NHE2: 17 CG: 17 | 18.8 (0.8) | 2–3 × 5–10 repetitions 1–2 times per week 17 wk | ECC strength Spring performance | NHE: 15.7% CG: 2.8% | NA |
Abbreviations: ACSA, anatomical cross-sectional area; BFlh, biceps femoris long head; BFsh, biceps femoris short head; CG, control group; CON, concentric; ECC, eccentric; EMG, electromyography; FL, fascicle length; HE, hip extension; H:Q, hamstring:quadriceps; HC, hamstring curl; ISO, isometric; MT, muscle thickness; MVC, maximal voluntary contraction; NA, nonapplicable; NHE, Nordic hamstring exercise; PA, pennation angle; PCSA, physiological cross-sectional area; PT, peak torque; RSA, repeated sprint ability; SJ, squat jump; ST, semitendinosus; VOL, volume.
Risk of Bias
Of the studies included in this systematic review, 50% presented an adequate sequence generation, 25% reported allocation concealment; 58% had blinded assessment of outcomes, 58% described losses to follow-up and exclusions, and none of the included studies had incomplete outcome data or selectively reported the outcomes (Table 2).
Risk of Bias of the Included Studies
| Study | Adequate sequence generation | Allocation concealment | Blinding of outcome assessors | Description of losses and exclusions | Incomplete outcome data | Selective outcome reporting |
|---|---|---|---|---|---|---|
| Bourne et al57 | Low risk | Unclear | Low risk | Unclear | Low risk | Low risk |
| Delahunt et al59 | Low risk | Low risk | Low risk | Unclear | Low risk | Low risk |
| Delextrat et al60 | Low risk | Unclear | Low risk | Low risk | Low risk | Low risk |
| Iga et al61 | Unclear | Unclear | Low risk | Unclear | Low risk | Low risk |
| Ishøi et al62 | Low risk | Low risk | Low risk | Low risk | Low risk | Low risk |
| Lovell et al63 | Unclear | Unclear | Unclear | Low risk | Low risk | Low risk |
| Mendiguchia et al64 | Unclear | Unclear | Low risk | Low risk | Low risk | Low risk |
| Mjølsnes et al65 | Low risk | Unclear | Low risk | Low risk | Low risk | High risk |
| Ribeiro-Alvares et al66 | Low risk | Unclear | High risk | Unclear | Low risk | Low risk |
| Salci et al55 | Unclear | Low risk | Unclear | Low risk | Low risk | Low risk |
| Seymore et al56 | Unclear | Unclear | Unclear | Unclear | Low risk | Low risk |
| Suarez-Arrones et al67 | High risk | High risk | Unclear | Low risk | Low risk | Low risk |
Effects of NHE on Eccentric Strength
Eleven studies evaluated the effects of NHE on eccentric strength (peak torque or force).56,57,59–63,65–68 Eight studies presented suitable data for meta-analysis. Analysis of studies that evaluated eccentric peak torque55,56,59,61,66 showed a significant difference between NHE and CG (0.68; 95% CI, 0.29 to 1.06; I2: 0%; Figure 2). Analysis of studies that assessed eccentric peak force57,62,67 also showed a significant difference between NHE and CG (01.11; 95% CI, 0.62 to 1.61: I2: 55%; Figure 3). The high heterogeneity in the latter analysis can be explained by the study from Bourne et al57 that worked with a different population when compared with the studies from Ishøi et al62 and Suarez-Arrones et al.67 It is reasonable to assume that the participants’ physical conditioning differences (active male vs soccer players) may have played a role in the difference in the adaptations found. When the study from Bourne et al57 was excluded from the meta-analysis, the heterogeneity was 0% (0.88; 95% CI, 0.33 to 1.42: I2: 0%).
—Analysis of eccentric strength during isokinetic dynamometry. CG indicates control group; CI, confidence interval; NHE, Nordic hamstring exercise.
Citation: Journal of Sport Rehabilitation 30, 3; 10.1123/jsr.2019-0388
—Analysis of eccentric strength during Nordic hamstring exercise test. CG indicates control group; CI, confidence interval; NHE, Nordic hamstring exercise.
Citation: Journal of Sport Rehabilitation 30, 3; 10.1123/jsr.2019-0388
Effects of NHE on Fascicle Length
Five studies56,57,63,64,66 evaluated the effects of NHE on biceps femoris long head fascicle length. All of them compared NHE with a CG (no intervention or alternative exercise). Four studies56,57,64,66 provided suitable data for meta-analysis. The analysis showed that NHE is effective in increasing fascicle length when compared with a CG (0.97; 95% CI, 0.46 to 1.48: I2: 71%; Figure 4). The high heterogeneity in the analysis of fascicle length can once again be explained by the study from Bourne et al.57 The authors performed a longer NHE training (10 wk) when compared with the other studies (466 and 6 wk56,64). It is possible that the longer training period might have contributed to the higher increase in fascicle length observed by Bourne et al.57 When this study was excluded from the meta-analysis, the heterogeneity was 0% (0.65; 95% CI, 0.09 to 1.20: I2: 0%).
—Analysis of fascicle length. CG indicates control group; CI, confidence interval; NHE, Nordic hamstring exercise.
Citation: Journal of Sport Rehabilitation 30, 3; 10.1123/jsr.2019-0388
Discussion
Summary of Evidence
The evidence presented in the current review showed that NHE-based training has the potential to enhance both HSI risk factors assessed in this review: knee flexors eccentric strength and biceps femoris long head fascicle length.
Effects of NHE on Strength
Hamstring muscles have a fundamental role on sprinting, especially during the terminal swing phase, when there is an intense active lengthening muscle action to decelerate both the hip flexion and the knee extension.69,70 Therefore, it seems plausible that increasing eccentric strength might decrease the risk of sustaining an HSI. However, the literature is not definitive regarding the role of poor hamstring strength as a risk factor for HSI. For instance, Van Dyk et al71 concluded that poor hamstring strength is a weak risk factor for HSI after assessing 614 professional soccer players through isokinetic dynamometry at preseason and following them along the season. On the other hand, Timmins et al29 and Lee et al30 prospectively assessed the hamstring eccentric strength of professional soccer players during the NHE execution and isokinetic dynamometry, respectively; those studies found that injured players throughout the subsequent season were approximately 13% to 19% weaker than the uninjured players. Despite these conflicting findings, it seems reasonable to assume that muscle weakness can never be considered as normal, and should always be addressed properly, especially in athletic populations.
The current review evidenced that NHE-based training was associated with increase in knee flexors eccentric strength. It is important to highlight that NHE training generated significant increases on eccentric strength in all studies assessed by our review, regardless the type of evaluation performed. When tests were performed on the isokinetic dynamometer, strength gains ranged between 10% and 15%, while studies comprising tests on the NHE device found increases from 16% to 26%. The greater percentage strength gains reported on the NHE device is probably related to training specificity.72 As the NHE device mimics the exact movement performed during the training program, it is reasonable to assume that the gains would be higher when compared with the isokinetic dynamometry, which involves a totally different testing setting.
Studies included in this review assessed participants with different conditioning levels (from physically active university students66 to professional soccer players62). It is a factor that significantly influences the responses to any type of strength training, including the NHE. In addition, the training protocols varied among the studies regarding training period, weekly frequency, and total training volume. NHE training volume has been an issue of current interest as it remains a challenge for coaches and conditioning trainers to fit NHE training in an already busy schedule.73 There seems to be a concern that the NHE added to the athletes’ training routine will promote an overload of muscular work. Thus, the dose of NHE training that is sufficient to generate muscle adaptations without promoting excessive levels of fatigue remains uncertain.
Severo-Silveira et al74 compared the effects of 2 NHE training programs (progressive workload, 236 repetitions along 8 wk; and constant workload, 138 repetitions along 8 wk) in Rugby players, and found that only the group trained with the greater training volume increased knee flexors eccentric strength. Nevertheless, performing NHE progressively during the season might not be suitable for the athletes’ training routines. A possible solution for this issue could be performing high-volume training followed by a low-volume training. Presland et al75 reported that 2 weeks of high-volume NHE training followed by 4 weeks of low-volume training (128 repetitions along 6 wk) generate similar adaptations when compared with 6 weeks of high-volume training (440 repetitions along 6 wk). Therefore, performing a high-volume training during the preseason and maintaining the gains with a low-volume training during the season might be more suitable for the teams’ training routines. However, it is important to mention that there is no consensus in current literature regarding the minimal NHE training volume required to promote significant increase in strength. For instance, all studies included in this review reported increase in hamstring eccentric strength, regardless of the periodization employed. This highlights the need for further studies regarding muscular adaptations promoted by the NHE training, especially to establish the optimal training volume for athletic populations.
Effects of NHE on Fascicle Length
In the last decades, the study of muscle architecture has been enabled by the introduction of 2D image ultrasound in this field.76 This cost- and time-effective noninvasive and easily accessible tools have helped to expand the assessment of muscle thickness, pennation angle, and fascicle length of a range of muscles. Biceps femoris long head fascicle length is the most remarkable muscle architecture outcome related to HSI. Evidence suggests that previously injured biceps femoris long head muscles present significantly shorter fascicles than muscles without history of injury,77 which might be one of the reasons why previously injured muscles have an increased chance of sustaining a new injury.3 Even more impressive are prospective findings that biceps femoris long head fascicles shorter than 10.56 cm at preseason increase more than 4 times the risk to HSI along the season in professional soccer players.29 Therefore, biceps femoris long head fascicle length is considered the newest and a very promising risk factor for HSI in sports.
Fascicle length increase changes the force–velocity and force–length relationships, which directly impacts muscle function.78 In theory, a muscle with longer fascicles contains a higher amount of in-series aligned sarcomeres, which would increase muscle contraction velocity79 and also prevent the muscle from damage due to over-lengthening.32 On the other hand, a muscle with reduced fascicle length presents an increased muscle susceptibility to eccentrically induced microscopic muscle damage, which could facilitate a macroscopic damage.80 Hence, exercises capable of increasing fascicle length might contribute to prevent HSI.
Our results support NHE training as an effective strategy to increase the biceps femoris long head fascicle length, as previously evidenced through isokinetic eccentric training of the hamstrings40 and other muscle groups.42,81 All studies included in the current review that addressed fascicle length found that NHE training promoted significant increases in that outcome, independently of the training periodization or participants conditioning status. It is worth pointing out in this context that the only 2 studies74,75 to this date that have compared low and high volume of NHE training found that fascicle length is increased even with low-volume training programs. This information is relevant for clubs that have difficulties implementing high volumes of NHE training due to their tight schedule.
Interestingly, fascicle length enhancement seems to occur since the first month of NHE training.66 Short-term responses might be useful for athletes who have short periods of preseason such as soccer players,43,44 given that they could start the competitive season with longer fascicles and less susceptibility to HSI. However, the quick fascicle length adaptation in response to NHE training has been evidenced only in a nonathletic population.66 In well-trained athletes, a longer training period (8-wk NHE training program) seems to be necessary to increase the hamstring fascicle length.74 Nonetheless, further investigations are needed to verify the short-term responses of fascicle length in this population.
According to the logistic regression performed by Timmins et al,29 an increase in only 11% in biceps femoris long head fascicle length enables a decrease of approximately 21% in the probability of HSI. On the other hand, the same study demonstrated that increments of at least 50% in hamstring eccentric strength are required to achieve a similar decrease in the probability of injury,29 which is a muscle strengthening hardly achieved in well-trained athletes. In the present review, the studies found increases in fascicle length from 12% to 22%, while the increases in eccentric strength ranged between 10% and 26%. Therefore, it seems reasonable to hypothesize that fascicle length changes might have a key role for the preventive effect of NHE. However, it is important to point out that fascicle length and eccentric strength only contribute to preventing HSI to some point. There are several other determinants suggested by prospective studies (eg, lumbopelvic stability, posterior chain flexibility, workload) that play a role in HSI and will be not modified through NHE training.
Strengths and Limitations
The current review is not without limitations. The main limitation of the present review is that we were not able to gather the totality of the studies in the quantitative analysis. Another limitation is the low to moderate methodological quality of the included studies. However, a strategy for a sensitive and comprehensive search to assure the location of all most recent studies in this field was held, further highlighting the need for additional investigations in that field. To the best of our knowledge, the current study is the first meta-analysis to exclusively analyze the role of NHE on specific hamstring injury risk factors (eccentric strength and fascicle length). Previous reviews82,83 have focused on HSI incidence, and even though we agree that this is the main variable in any injury prevention protocol, it is important to elucidate the mechanisms that underpin any positive results.
Conclusions
The present review evidenced that NHE is a valid strategy to enhance both knee flexors eccentric strength and fascicle length, 2 evidence-based risk factors for HSI. Our findings elucidated 2 of the main mechanisms that explain, at least in part, the preventive effect of NHE against HSI, and reinforce the adoption of this exercise during both training and rehabilitation programs. Nevertheless, further research is needed to verify the best NHE training protocol to modify eccentric strength and fascicle length without impairing athletes’ performance and increasing risk of HSI.
Acknowledgments
D.M.M. thanks CAPES-Brazil for the scholarship. B.M.B. thanks CNPq-Brazil for the research productivity fellowship. This work was not funded by any external source.
References
- 1.↑
Brukner P. Hamstring injuries: prevention and treatment—an update. Br J Sports Med. 2015;49(19):1241–1244. doi:10.1136/bjsports-2014-094427
- 2.↑
Malliaropoulos N, Isinkaye T, Tsitas K, Maffulli N. Reinjury after acute posterior thigh muscle injuries in elite track and field athletes. Am J Sports Med. 2011;39(2):304–310. PubMed ID: 21051422 doi:10.1177/0363546510382857
- 3.↑
Brooks JHM, Fuller CW, Kemp SPT, Reddin DB. Incidence, risk, and prevention of hamstring muscle injuries in professional rugby union. Am J Sport Med. 2006;34(8):1297–1306. doi:10.1177/0363546505286022
- 4.↑
Borowski LA, Yard EE, Fields SK, Comstock RD. The Epidemiology of US High School Basketball Injuries, 2005–2007. Am J Sports Med. 2008;36(12):2328–2335. PubMed ID: 18765675 doi:10.1177/0363546508322893
- 5.↑
Ekstrand J, Hägglund M, Waldén M. Epidemiology of muscle injuries in professional football (soccer). Am J Sports Med. 2011;39(6):1226–1232. PubMed ID: 21335353 doi:10.1177/0363546510395879
- 6.↑
Feeley BT, Kennelly S, Barnes RP, et al. Epidemiology of National Football League Training Camp Injuries from 1998 to 2007. Am J Sports Med. 2008;36(8):1597–1603. PubMed ID: 18443276 doi:10.1177/0363546508316021
- 7.↑
Askling CM, Tengvar M, Saartok T, Thorstensson A. Proximal hamstring strains of stretching type in different sports: injury situations, clinical and magnetic resonance imaging characteristics, and return to sport. Am J Sports Med. 2008;36(9):1799–1804. PubMed ID: 18448581 doi:10.1177/0363546508315892
- 8.↑
Garrett WE. Muscle strain injuries. Am J Sports Med. 1996;24(6):S2–S8. doi:10.1177/036354659602406S02
- 9.
Huard J, Li Y, Fu FH. Muscle injuries and repair: current trends in research. J Bone Joint Surg Am. 2002;84(5):822–832. doi:10.2106/00004623-200205000-00022
- 10.↑
Järvinen TAH, Järvinen TLN, Kääriäinen M, Kalimo H, Järvinen M. Muscle injuries: biology and treatment. Am J Sports Med. 2005;33(5):745–764. PubMed ID: 15851777 doi:10.1177/0363546505274714
- 11.↑
Shankar PR, Fields SK, Collins CL, Dick RW, Comstock RD. Epidemiology of High School and Collegiate Football Injuries in the United States, 2005-2006. Am J Sports Med. 2007;35(8):1295–1303. PubMed ID: 17369559 doi:10.1177/0363546507299745
- 12.↑
Price RJ, Hawkins RD, Hulse MA, Hodson A. The Football Association medical research programme: an audit of injuries in academy youth football. Br J Sports Med. 2004;38(4):466–471. PubMed ID: 15273188 doi:10.1136/bjsm.2003.005165
- 13.↑
Marshall SW, Hamstra-Wright KL, Dick R, Grove KA, Agel J. Descriptive epidemiology of collegiate women’s softball injuries: National Collegiate Athletic Association injury surveillance system, 1988–1989 through 2003–2004. J Athl Train. 2007;42(2):286–294. doi:10.1016/S0276-1092(08)79204-6
- 14.↑
Ekstrand J, Hägglund M, Waldén M. Injury incidence and injury patterns in professional football: the UEFA injury study. Br J Sports Med. 2011;45(7):553–558. doi:10.1136/bjsm.2009.060582
- 15.↑
Ekstrand J, Waldén M, Hägglund M. Hamstring injuries have increased by 4% annually in men’s professional football, since 2001: a 13-year longitudinal analysis of the UEFA Elite Club injury study. Br J Sports Med. 2016;50(12):731–737. PubMed ID: 26746908 doi:10.1136/bjsports-2015-095359
- 16.↑
Hallén A, Ekstrand J. Return to play following muscle injuries in professional footballers. J Sports Sci. 2014;32(13):1229–1236. PubMed ID: 24784885 doi:10.1080/02640414.2014.905695
- 17.↑
Tol JL, Hamilton B, Eirale C, Muxart P, Jacobsen P, Whiteley R. At return to play following hamstring injury the majority of professional football players have residual isokinetic deficits. Br J Sports Med. 2014;48(18):1364–1369. PubMed ID: 24493666 doi:10.1136/bjsports-2013-093016
- 18.↑
Woods C. The football association medical research programme: an audit of injuries in professional football—analysis of hamstring injuries. Br J Sports Med. 2004;38(1):36–41. PubMed ID: 14751943 doi:10.1136/bjsm.2002.002352
- 19.↑
Hägglund M, Waldén M, Magnusson H, Kristenson K, Bengtsson H, Ekstrand J. Injuries affect team performance negatively in professional football: an 11-year follow-up of the UEFA Champions League injury study. Br J Sports Med. 2013;47(12):738–742. PubMed ID: 23645832 doi:10.1136/bjsports-2013-092215
- 20.↑
Petersen J, Thorborg K, Nielsen MB, Budtz-Jørgensen E, Hölmich P. Preventive effect of eccentric training on acute hamstring injuries in men’s soccer: a cluster-randomized controlled trial. Am J Sports Med. 2011;39(11):2296–2303. PubMed ID: 21825112 doi:10.1177/0363546511419277
- 21.
Schache A. Eccentric hamstring muscle training can prevent hamstring injuries in soccer players. J Physiother. 2012;58(1):58. PubMed ID: 22341384 doi:10.1016/S1836-9553(12)70074-7
- 22.↑
van der Horst N, Smits D-W, Petersen J, Goedhart EA, Backx FJG. The preventive effect of the Nordic hamstring exercise on hamstring injuries in amateur soccer players. Am J Sports Med. 2015;43(6):1316–1323. doi:10.1177/0363546515574057
- 23.
Nichols AW. Does eccentric training of hamstring muscles reduce acute injuries in soccer? Clin J Sport Med. 2013;23(1):85–86. PubMed ID: 23269328 doi:10.1097/JSM.0b013e31827e9f40
- 24.↑
Arnason A, Andersen TE, Holme I, Engebretsen L, Bahr R. Prevention of hamstring strains in elite soccer: an intervention study. Scand J Med Sci Sport. 2008;18(1):40–48. doi:10.1111/j.1600-0838.2006.00634.x
- 25.↑
Seagrave RA, Perez L, McQueeney S, Toby EB, Key V, Nelson JD. Preventive effects of eccentric training on acute hamstring muscle injury in professional baseball. Orthop J Sport Med. 2014;2(6):232596711453535. doi:10.1177/2325967114535351
- 26.↑
Askling C, Karlsson J, Thorstensson A. Hamstring injury occurrence in elite soccer players after preseason strength training with eccentric overload. Scand J Med Sci Sport. 2003;13(4):244–250. doi:10.1034/j.1600-0838.2003.00312.x
- 27.↑
Opar DA, Williams MD, Shield AJ. Hamstring strain injuries: factors that lead to injury and re-injury. Sport Med. 2012;42(3):209–226. doi:10.2165/11594800-000000000-00000
- 28.↑
Larruskain J, Celorrio D, Barrio I, et al. Genetic variants and hamstring injury in soccer: an association and validation study. Med Sci Sports Exerc. 2018;50(2):361–368. PubMed ID: 28976491 doi:10.1249/MSS.0000000000001434
- 29.↑
Timmins RG, Bourne MN, Shield AJ, Williams MD, Lorenzen C, Opar DA. Short biceps femoris fascicles and eccentric knee flexor weakness increase the risk of hamstring injury in elite football (soccer): a prospective cohort study. Br J Sports Med. 2016;50(24):1524–1535. PubMed ID: 26675089 doi:10.1136/bjsports-2015-095362
- 30.↑
Lee JWY, Mok KM, Chan HCK, Yung PSH, Chan KM. Eccentric hamstring strength deficit and poor hamstring-to-quadriceps ratio are risk factors for hamstring strain injury in football: a prospective study of 146 professional players. J Sci Med Sport. 2018;21(8):789–793. PubMed ID: 29233665 doi:10.1016/j.jsams.2017.11.017
- 31.↑
Bourne MN, Opar DA, Williams MD, Shield AJ. Eccentric knee flexor strength and risk of hamstring injuries in rugby union. Am J Sports Med. 2015;43(11):2663–2670. PubMed ID: 26337245 doi:10.1177/0363546515599633
- 32.↑
Timmins RG, Shield AJ, Williams MD, Lorenzen C, Opar DA. Architectural adaptations of muscle to training and injury: a narrative review outlining the contributions by fascicle length, pennation angle and muscle thickness. Br J Sports Med. 2016;50(23):1467–1472. PubMed ID: 26817705 doi:10.1136/bjsports-2015-094881
- 33.↑
Timmins RG, Bourne MN, Hickey JT, et al. Effect of prior injury on changes to biceps femoris architecture across an Australian Football League season. Med Sci Sports Exerc. 2017;49(10):2102–2109. PubMed ID: 28548976 doi:10.1249/MSS.0000000000001333
- 34.↑
Opar DA, Piatkowski T, Williams MD, Shield AJ. A novel device using the Nordic hamstring exercise to assess eccentric knee flexor strength: a reliability and retrospective injury study. J Orthop Sports Phys Ther. 2013;43(9):636–640. PubMed ID: 23886674 doi:10.2519/jospt.2013.4837
- 35.↑
Onambélé GL, Maganaris CN, Mian OS, et al. Neuromuscular and balance responses to flywheel inertial versus weight training in older persons. J Biomech. 2008;42(7):956. doi:10.1016/j.jbiomech.2008.09.004
- 36.
Walker S, Blazevich AJ, Haff GG, Tufano JJ, Newton RU, Häkkinen K. Greater strength gains after training with accentuated eccentric than traditional isoinertial loads in already strength-trained men. Front Physiol. 2016;27(7):149. doi:10.3389/fphys.2016.00149
- 37.
Friedmann-Bette B, Bauer T, Kinscherf R, et al. Effects of strength training with eccentric overload on muscle adaptation in male athletes. Eur J Appl Physiol. 2010;108(4):821–836. doi:10.1007/s00421-009-1292-2
- 38.↑
Gerber JP, Marcus RL, Dibble LE, Greis PE, Burks RT, LaStayo PC. Effects of early progressive eccentric exercise on muscle size and function after anterior cruciate ligament reconstruction: a 1-year follow-up study of a randomized clinical trial. Phys Ther. 2009;89(1):51–59. PubMed ID: 18988664 doi:10.2522/ptj.20070189
- 39.↑
Roig M, O’Brien K, Kirk G, et al. The effects of eccentric versus concentric resistance training on muscle strength and mass in healthy adults: a systematic review with meta-analysis. Br J Sports Med. 2009;43(8):556–568. PubMed ID: 18981046 doi:10.1136/bjsm.2008.051417
- 40.↑
Timmins RG, Ruddy JD, Presland J, et al. Architectural changes of the biceps femoris long head after concentric or eccentric training. Med Sci Sports Exerc. 2016;48(3):499–508. PubMed ID: 26460634 doi:10.1249/MSS.0000000000000795
- 41.↑
Geremia JM, Baroni BM, Bobbert MF, Bini RR, Lanferdini FJ, Vaz MA. Effects of high loading by eccentric triceps surae training on Achilles tendon properties in humans. Eur J Appl Physiol. 2018;118(8):1725–1736. PubMed ID: 29858689 doi:10.1007/s00421-018-3904-1
- 42.↑
Baroni BM, Rodrigues R, Franke RA, Geremia JM, Rassier DE, Vaz MA. Time course of neuromuscular adaptations to knee extensor eccentric training. Int J Sports Med. 2013;34(10):904–911. PubMed ID: 23526592 doi:10.1055/s-0032-1333263
- 43.↑
McCall A, Carling C, Nedelec M, et al. Risk factors, testing and preventative strategies for non-contact injuries in professional football: current perceptions and practices of 44 teams from various premier leagues. Br J Sports Med. 2014;48(18):1352–1357. PubMed ID: 24837243 doi:10.1136/bjsports-2014-093439
- 44.↑
Meurer MC, Silva MF, Baroni BM. Strategies for injury prevention in Brazilian football: perceptions of physiotherapists and practices of premier league teams. Phys Ther Sport. 2017;28:1–8. PubMed ID: 28886473 doi:10.1016/j.ptsp.2017.07.004
- 45.↑
Gabbe BJ, Branson R, Bennell KL. A pilot randomised controlled trial of eccentric exercise to prevent hamstring injuries in community-level Australian Football. J Sci Med Sport. 2006;9(1–2):103–109. PubMed ID: 16574482 doi:10.1016/j.jsams.2006.02.001
- 46.↑
van Dyk N, Behan FP, Whiteley R. Including the Nordic hamstring exercise in injury prevention programmes halves the rate of hamstring injuries: a systematic review and meta-analysis of 8459 athletes. Br J Sport Med. 2019;53(21):1362–1370. doi:10.1136/bjsports-2018-100045
- 47.↑
Shamseer L, Moher D, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ. 2015;349:g7647. doi:10.1136/bmj.g7647
- 48.↑
Robinson KA, Dickersin K. Development of a highly sensitive search strategy for the retrieval of reports of controlled trials using PubMed. Int J Epidemiol. 2002;31(1):150–153. PubMed ID: 11914311 doi:10.1093/ije/31.1.150
- 49.↑
Hewett TE, Myer GD, Zazulak BT. Hamstrings to quadriceps peak torque ratios diverge between sexes with increasing isokinetic angular velocity. J Sci Med Sport. 2008;11(5):452–459. PubMed ID: 17875402 doi:10.1016/j.jsams.2007.04.009
- 50.↑
Behan FP, Moody R, Patel TS, Lattimore E, Maden-Wilkinson TM, Balshaw TG. Biceps femoris long head muscle fascicle length does not differ between sexes. J Sports Sci. 2019;37(21):2452–2458. PubMed ID: 31303128 doi:10.1080/02640414.2019.1641016
- 51.↑
Higgins JPT, Altman DG. Higgins 2011. In: Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions. Version 5.1.0 [Updated March 2011]. Chichester, United Kingdom: The Cochrane Collaboration; 2011. doi:10.1002/9780470712184.ch8
- 52.↑
Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. Chichester, United Kingdom: The Cochrane Collaboration; 2008. doi:10.1002/9780470712184
- 53.↑
Follmann D, Elliott P, Suh I, Cutler J. Variance imputation for overviews of clinical trials with continuous response. J Clin Epidemiol. 1992;45(7):769–773. PubMed ID: 1619456 doi:10.1016/0895-4356(92)90054-Q
- 54.↑
Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ Br Med J. 2003;327(7414):557–560. doi:10.1136/bmj.327.7414.557
- 55.↑
Salci Y, Yildirim A, Celik O, Ak E, Kocak S, Korkusuz F. The effects of eccentric hamstring training on lower extremity strength and landing kinetics in recreational female athletes. Isokinet Exerc Sci. 2013;21(1):11–18. doi:10.3233/IES-2012-0466
- 56.↑
Seymore KD, Domire ZJ, DeVita P, Rider PM, Kulas AS. The effect of Nordic hamstring strength training on muscle architecture, stiffness, and strength. Eur J Appl Physiol. 2017;117(5):943–953. PubMed ID: 28280975 doi:10.1007/s00421-017-3583-3
- 57.↑
Bourne MN, Duhig SJ, Timmins RG, et al. Impact of the Nordic hamstring and hip extension exercises on hamstring architecture and morphology: implications for injury prevention. Br J Sports Med. 2017;51(5):469–477. PubMed ID: 27660368 doi:10.1136/bjsports-2016-096130
- 58.↑
Jelicic Kadic A, Vucic K, Dosenovic S, Sapunar D, Puljak L. Extracting data from figures with software was faster, with higher interrater reliability than manual extraction. J Clin Epidemiol. 2016;74:119–123. doi:10.1016/j.jclinepi.2016.01.002
- 59.↑
Delahunt E, McGroarty M, De Vito G, Ditroilo M. Nordic hamstring exercise training alters knee joint kinematics and hamstring activation patterns in young men. Eur J Appl Physiol. 2016;116(4):663–672. PubMed ID: 26754149 doi:10.1007/s00421-015-3325-3
- 60.↑
Delextrat A, Bateman J, Ross C, et al. Changes in torque-angle profiles of the hamstrings and hamstrings-to-quadriceps ratio after two hamstring strengthening exercise interventions in female hockey players. J Strength Cond Res. 2020;34(2):396–405. PubMed ID: 31425454 doi:10.1519/JSC.0000000000003309
- 61.↑
Iga J, Fruer CS, Deighan M, Croix MDS, James DVB. Nordic hamstrings exercise-engagement characteristics and training responses. Int J Sports Med. 2012;33(12):1000–1004. PubMed ID: 22895870 doi:10.1055/s-0032-1304591
- 62.↑
Ishøi L, Hölmich P, Aagaard P, Thorborg K, Bandholm T, Serner A. Effects of the Nordic hamstring exercise on sprint capacity in male football players: a randomized controlled trial. J Sports Sci. 2018;36(14):1663–1672. PubMed ID: 29192837 doi:10.1080/02640414.2017.1409609
- 63.↑
Lovell R, Knox M, Weston M, Siegler JC, Brennan S, Marshall PWM. Hamstring injury prevention in soccer: before or after training? Scand J Med Sci Sport. 2018;28(2):658–666. doi:10.1111/sms.12925
- 64.↑
Mendiguchia J, Conceição F, Edouard P, et al. Sprint versus isolated eccentric training: comparative effects on hamstring architecture and performance in soccer players. PLoS One. 2020;15(2):e0228283. PubMed ID: 32045411 doi:10.1371/journal.pone.0228283
- 65.↑
Mjølsnes R, Arnason A, Østhagen T, Raastad T, Bahr R. A 10-week randomized trial comparing eccentric vs concentric hamstring strength training in well-trained soccer players. Scand J Med Sci Sport. 2004;14(5):311–317. doi:10.1046/j.1600-0838.2003.00367.x
- 66.↑
Ribeiro-Alvares J, Marques VB, Vaz MA, Baroni BM. Four weeks of Nordic hamstring exercise reduce muscle injury risk factors in young adults. J Strength Cond Res. 2018;32(5):1254–1262. PubMed ID: 28459795 doi:10.1519/JSC.0000000000001975
- 67.↑
Suarez-Arrones L, Lara-Lopez P, Rodriguez-Sanchez P, et al. Dissociation between changes in sprinting performance and Nordic hamstring strength in professional male football players. PLoS One. 2019;14(3):e0213375. doi:10.1371/journal.pone.0213375
- 68.↑
Small K, Mcnaughton L, Greig M, Lovell R. Effect of timing of eccentric hamstring strengthening exercises during soccer training: implications for muscle fatigability. J Strength Cond Res. 2009;23(4):1077–1083. PubMed ID: 19528859 doi:10.1519/JSC.0b013e318194df5c
- 69.↑
Schache AG, Dorn TW, Blanch PD, Brown NAT, Pandy MG. Mechanics of the human hamstring muscles during sprinting. Med Sci Sports Exerc. 2012;44(4):647–658. PubMed ID: 21912301 doi:10.1249/MSS.0b013e318236a3d2
- 70.↑
Guex K, Millet GP. Conceptual framework for strengthening exercises to prevent hamstring strains. Sport Med. 2013;43(12):1207–1215. doi:10.1007/s40279-013-0097-y
- 71.↑
Van Dyk N, Bahr R, Whiteley R, et al. Hamstring and quadriceps isokinetic strength deficits are weak risk factors for hamstring strain injuries. Am J Sports Med. 2016;44(7):1789–1795. doi:10.1177/0363546516632526
- 72.↑
Reilly T, Morris T, Whyte G. The specificity of training prescription and physiological assessment: a review. J Sports Sci. 2009;27(6):575–589. PubMed ID: 19340630 doi:10.1080/02640410902729741
- 73.↑
Lovell R, Whalan M, Marshall PWM, Sampson JA, Siegler JC, Buchheit M. Scheduling of eccentric lower limb injury prevention exercises during the soccer micro-cycle: which day of the week? Scand J Med Sci Sport. 2018;28(10):2216–2225. doi:10.1111/sms.13226
- 74.↑
Severo-Silveira L, Dornelles MP, Lima-E-Silva FX, et al. Progressive workload periodization maximizes effects of Nordic hamstring exercise on muscle injury risk factors. J strength Cond Res. 2018;28(7):1775–1783. doi:10.1519/JSC.0000000000002849
- 75.↑
Presland JD, Timmins RG, Bourne MN, Williams MD, Opar DA. The effect of Nordic hamstring exercise training volume on biceps femoris long head architectural adaptation. Scand J Med Sci Sport. 2018;28(7):1775–1783. doi:10.1111/sms.13085
- 76.↑
Blazevich AJ, Gill ND, Zhou S. Intra- and intermuscular variation in human quadriceps femoris architecture assessed in vivo. J Anat. 2006;209(3):289–310. PubMed ID: 16928199 doi:10.1111/j.1469-7580.2006.00619.x
- 77.↑
Timmins RG, Shield AJ, Williams MD, Lorenzen C, Opar DA. Biceps femoris long head architecture: a reliability and retrospective injury study. Med Sci Sports Exerc. 2015;47(5):905–913. PubMed ID: 25207929 doi:10.1249/MSS.0000000000000507
- 78.↑
Lieber RL, Bodine-Fowler SC. Skeletal muscle mechanics: implications for rehabilitation. Phys Ther. 1993;73(12):844–856. PubMed ID: 8248293 doi:10.1093/ptj/73.12.844
- 79.↑
Lieber RL, Fridén J. Muscle damage is not a function of muscle force but active muscle strain. J Appl Physiol. 1993;74(2):520–526. PubMed ID: 8458765 doi:10.1152/jappl.1993.74.2.520
- 80.↑
Morgan DL. New insights into the behavior of muscle during active lengthening. Biophys J. 1990;57(2):209–221. PubMed ID: 2317547 doi:10.1016/S0006-3495(90)82524-8
- 81.↑
Geremia JM, Baroni BM, Lanferdini FJ, Bini RR, Sonda FC, Vaz MA. Time course of neuromechanical and morphological adaptations to triceps surae isokinetic eccentric training. Phys Ther Sport. 2018;34:84–91. PubMed ID: 30248491 doi:10.1016/j.ptsp.2018.09.003
- 82.↑
Al Attar WSA, Soomro N, Sinclair PJ, Pappas E, Sanders RH. Effect of injury prevention programs that include the Nordic hamstring exercise on hamstring injury rates in soccer players: a systematic review and meta-analysis. Sport Med. 2017;47(5):907–916. doi:10.1007/s40279-016-0638-2
- 83.↑
Goode AP, Reiman MP, Harris L, et al. Eccentric training for prevention of hamstring injuries may depend on intervention compliance: a systematic review and meta-analysis. Br J Sports Med. 2015;49(6):349–356. PubMed ID: 25227125 doi:10.1136/bjsports-2014-093466
