International Journal of Sports Physiology and Performance, 2015, 10, 325-331 http://dx.doi.org/10.1123/ijspp.2014-0088 © 2015 Human Kinetics, Inc.
www.IJSPP-Journal.com ORIGINAL INVESTIGATION
Angle-Specific Eccentric Hamstring Fatigue After Simulated Soccer Daniel D. Cohen, Bingnan Zhao, Brian Okwera, Martyn J. Matthews, and Anne Delextrat Purpose: To evaluate the effect of simulated soccer on the hamstrings eccentric torque-angle profile and angle of peak torque (APTeccH), and on the hamstrings:quadriceps torque ratio at specific joint angles (ASHecc:Qcon). Methods: The authors assessed dominant-limb isokinetic concentric and eccentric knee flexion and concentric knee extension at 120°/s in 9 semiprofessional male soccer players immediately before and after they completed the Loughborough Intermittent Shuttle Test (LIST). Results: The LIST resulted in significant decreases in eccentric hamstrings torque at 60°, 50°, and 10° and a significant (21.8%) decrease in ASHecc:Qcon at 10° (P < .05). APTeccH increased from 7.1° ± 1.0° to 18.8° ± 4.2° (P < .05). Eccentric hamstrings peak torque significantly declined from 185.1 ± 70.4 N·m pre-LIST to 150.9 ± 58.5 N·m post-LIST (P = .002), but there were no significant changes in hamstrings or quadriceps concentric peak torque (P = .312, .169, respectively). Conclusions: Simulated soccer results in a selective loss of eccentric hamstrings torque and hamstrings-to-quadriceps muscle balance at an extended joint position and a shift in the eccentric hamstrings APT to a shorter length, changes that could increase vulnerability to hamstrings injury. These findings suggest that injury-risk screening could be improved by evaluating the eccentric hamstrings torque-angle profile and hamstrings strength-endurance and that the development of hamstrings fatigue resistance and long-length eccentric strength may reduce injury incidence. Keywords: injury-risk screening, strength imbalance, eccentric strength, muscle fatigue, isokinetic testing Hamstrings strains (HSSs) are the most common injury in professional soccer1 and other multiple-sprint sports.2 There is therefore considerable interest in addressing and where possible managing the multiple etiological factors that interact to determine risk.2,3 As risk factors that are potentially modifiable with training, muscle strength, fatigue, and the interaction between the 2 have received considerable attention in the sports-medicine literature.4–6 Inadequate hamstrings strength, in particular in the eccentric mode, or a low ratio of hamstrings to quadriceps strength is associated with increased HSS risk,7,8 and there is evidence that eccentric-emphasis strength training can reduce HSS incidence in soccer players. Accordingly, isokinetic assessment of the “conventional” peak-torque Hconcentric:Qconcentric ratio or of the “functional” peak-torque Heccentric:Qconcentric ratio is used in preseason injury-risk screening and in secondary HSS-prevention programs in professional soccer. Muscle fatigue is thought to explain epidemiological findings such as higher injury incidence in competitive match play compared with training,1 higher incidence in the latter part of the first and second halves of competitive soccer compared with the earlier parts of the game,1 and higher incidence in Australian rules footballers who were rotated less frequently than those who accumulated more rest within a game.10 Furthermore, hamstrings Cohen is with the Masira Institute, Faculty of Life Sciences, University of Santander (UDES), Bucaramanga, Colombia. Zhao and Okwera are with the Faculty of Life Sciences, London Metropolitan University, London, UK. Matthews is with the School of Health Sciences, Salford University, Salford, UK. Delextrat is with the Faculty of Sport and Health Sciences, Oxford Brookes University, Oxford, UK. Address author correspondence to Daniel Cohen at [email protected].
fatigue is associated with poorer mechanical knee stability, which may increase the risk of anterior cruciate ligament (ACL) injury.11 To better understand interactions between fatigue, strength, and vulnerability to injury during match play, studies have evaluated changes in muscle strength after protocols designed to simulate the metabolic demands of competition. The most consistent finding of these studies is a greater decline in eccentric hamstrings than concentric quadriceps peak torque, resulting in decreases of 16% to 26% in the Hecc:Qcon ratio.5,6,12 HSSs most commonly occur during high-speed running,1 with the hamstrings particularly vulnerable to damage and injury during the late swing phase, when the leg is extended and they are required to eccentrically contract to counteract the large torque generated by concentric quadriceps contraction.13 On this basis, it is argued that there should be specific emphasis on the evaluation and/or conditioning of hamstrings strength at longer muscle lengths, rather than on peak hamstrings strength per se.14–16 Accordingly, characterizing angle-specific strength changes after multiple-sprint activity may also help elucidate strength-fatigue-injury interactions and inform screening and prevention protocols. The main aims of the current study were to investigate the effects of simulated soccer activity on the eccentric hamstrings torque-angle profile and angle of peak torque (APT) and on the angle-specific ratios of eccentric hamstrings to concentric quadriceps (ASHecc:Qcon).
Methods Subjects Nine male soccer players (age 25.3 ± 0.8 y, height 178.8 ± 2.9 cm, body mass 77.0 ± 3.7 kg) were recruited as volunteers from
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semiprofessional soccer clubs in London, England. Players participated in 2 × 2-hour training sessions and two 90-minute matches per week. Those with any knee or thigh-muscle injuries in the past year were excluded. Participants were questioned about their general health history and informed of all the testing procedures in detail, and they gave written consent before data collection. Ethical approval for the project was given by the London Metropolitan University research ethics committee.
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Design Participants were tested on 2 separate occasions 1 week apart, for preliminary and main testing sessions, respectively. In the preliminary session, participants had an isokinetic familiarization session and performed the Multistage Fitness Test.17 After a standardized warm-up, subjects performed an isokinetic assessment of hamstrings and quadriceps peak torques with the dominant leg (defined as the leg used to kick a ball). This was immediately followed by a 90-minute simulated soccer activity: the Loughborough Intermittent Shuttle Test (LIST).18 After the LIST, participants repeated the isokinetic tests. The time between the completion of the LIST and the start of the post-LIST measurement was approximately 3 minutes. Players were asked to refrain from consuming any caffeine or alcohol for 2 hours before each session.
Methodology Participants performed the Multistage Fitness Test, which consists of running between 2 cones placed 20 m apart at a progressively increasing speed controlled by audio bleeps. The test has good reliability (r = .975) and validity (r = .87–.92) for the estimation of maximal aerobic capacity (VO2max).17 To ensure that players performed with maximal effort, a minimum of 2 players performed the test at the same time. The final level reached during the test was used to estimate VO2max and the running speed corresponding to 55% and 95% of maximal aerobic speed, required for the LIST protocol. The LIST18 consists of periods of walking, jogging, running, and sprinting based on the activity profile of football in terms of time, running patterns, and physiological and metabolic responses during soccer games and has good test–retest reliability; it is described in detail elsewhere.6,18 Before the pre-LIST test, participants performed a supervised 10-minute warm-up on a cycle ergometer (Monark 864, Varberg, Sweden) at 70 W, followed by 2 sets of 30-second static stretches for the hamstrings and quadriceps. They were then seated on the isokinetic dynamometer (HUMAC NORM, Computer Sports Medicine International, Stoughton, MA, USA), and adjustable segments of the dynamometer were set according to the participant’s body dimensions. Players performed 2 tests of 5 maximal repetitions at 120°/s with a 2-minute recovery period between and were encouraged to provide maximal effort for all repetitions of the maximal tests. Just before the maximal test, players performed 3 submaximal trials. Only the 5 maximal contractions in each mode were recorded, and the repetition with the highest peak torque was selected for further analysis. Concentric/eccentric extension and flexion were assessed in random order pre-LIST, with that order then repeated in the test that immediately followed the LIST. Gravity correction was selected for all tests. Isokinetic testing is characterized by a good test–retest reliability (intraclass correlation coefficient >.80) for the measurement of
hamstrings-to-quadriceps strength ratios and has been widely used to assess the strength of soccer players19; the angular velocity was 120°/s, used in a number of similar studies.4,6,12 The following isokinetic parameters were determined pre- and post-LIST. Peak values: • Peak torque (PT) of the concentric hamstrings (PT-Hcon), eccentric hamstrings (PT-Hecc), and concentric quadriceps (PT-Qcon). • The functional ratio (Hecc:Qcon), calculated as eccentric hamstrings PT:concentric quadriceps PT. • Angle of PT for hamstrings concentric (APTconH) and eccentric (APTeccH) and quadriceps concentric (APTconQ). Angle-specific values: • Eccentric hamstrings and concentric quadriceps torque at 10°, 20°, 30°, 40°, 50°, 60°, 70°, 80°, and 90°. • Angle-specific hamstrings:quadriceps torque ratios (ASHeccQcon), for angles 10° to 90°, calculated as Hecc torque/Qcon torque at each angle.
Statistical Analysis Statistical analysis was performed using SPSS statistical software (version 19.0). Mean ± SD were calculated for each dependent variable. The parametric nature of the data was checked by the Shapiro-Wilk test. A Student t-test for paired samples was applied to compare peak values. In addition, an analysis of variance (ANOVA) with repeated measures was used to test the effect of angle (0–90°) and fatigue (pre vs post) on angle-specific torques and ASHecc:Qcon. Post hoc t-tests were performed to determine where differences lay. Effect sizes were calculated using Cohen d and partial eta squared (ηP2) and interpreted as small (>0.1), medium (>0.3), and large (>0.5).20 Significance was set at P < .05.
Results Subjects’ estimated VO2max was 49.4 ± 4.2 mL · kg–1 · min–1, and their maximal aerobic speed averaged 12.7 ± 0.6 km/h. Figure 1 shows pre- and post-LIST eccentric hamstrings torques at 9 knee-flexion angles. The statistical analysis revealed significant main effects of angle (P = .001, ηP2 = .638) and fatigue (P = .039, ηP2 = .432) and an interaction between these factors (P = .010, ηP2 = .261). Torques tended to be lower after the LIST, and significant effects were observed in Hecc at 90° (P = .022, d = 2.3), 60° (P = .019, d = 1.57), 50° (P = .035, d = 1.37), and 10° of knee flexion (P = .006, d = 2.18). There were no significant decreases in Qcon or Hcon at any angle (Figures 2 and 3, respectively). Figure 4 shows pre- and post-LIST values for ASHecc:Qcon at 9 knee-flexion angles (ASHecc:Qcon). The ANOVA showed significant effects of angle (P = .001, ηP2 = .854) and fatigue (P = .030, ηP2 = .465 and an interaction between these factors (P = .003, ηP2 = .297). Subsequent analyses revealed a significant decrease in preversus post-LIST at 10° of knee flexion (P = .036) but not at any other angle tested. Pre-LIST ASHecc:Qcon at 10° of knee flexion was significantly higher than at the other 8 angles (P < .05, d = 2.06). Figure 5 shows angle-of-peak-torque (APT) values pre- and post-LIST. There was a significant (P = .025, d = 1.28) change in APTeccH from 7.1° ± 1.0° pre-LIST to 18.8° ± 4.2° post-LIST. Changes in the APTconH from 27.9° ± 2.8° pre-LIST to 27.8° ± 3.0°
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Figure 1 — Eccentric hamstrings torque at specific angles before and after the Loughborough Intermittent Shuttle Test (LIST). *Significantly different post-LIST (P < .05). **Significantly different post-LIST (P < .01).
Figure 2 — Concentric quadriceps torque at specific angles before and after the Loughborough Intermittent Shuttle Test.
and in the APTconQ from 63.1° ± 2.1° pre-LIST to 65.9° ± 2.2° postLIST were not significant (P = .954, 0.211, respectively). Pre-LIST, the APTeccH was significantly different from the APTconQ (P < .001, d = 4.60) and from APTconH (P = .004, d = 0.82). Figure 6 shows peak-torque values pre- and post-LIST. PT-Hecc significantly declined from 185.1 ± 70.4 N·m pre-LIST to 150.9 ± 58.5 N·m post-LIST (P = .002, d = 0.53). While PT-Qcon, declined from 166.6 ± 45.1 N·m pre-LIST to 155.0 ± 42.6 N·m post-LIST and PT-Hcon declined from 119.6 ± 24.2 N·m to 110.7 ± 27.9 N·m, these changes were not significant (P = .312, 0.169, respectively).
The Hecc:Qcon ratio significantly decreased from 1.11 pre-LIST to 0.98 post-LIST (P = .026, d = 0.60).
Discussion We evaluated angle-specific changes in hamstrings and quadriceps torque and torque ratios after the LIST simulated football protocol in semiprofessional male footballers. The novel findings of the study were that the LIST resulted in significant declines in hamstrings torque at 60°, 50°, and 10° and a significant 21.8%
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Figure 3 — Concentric hamstrings torque at specific angles before and after the Loughborough Intermittent Shuttle Test.
Figure 4 — Angle-specific eccentric hamstrings–to–concentric quadriceps ratios (ASHecc:Qcon) before and after the Loughborough Intermittent Shuttle Test (LIST) at specific angles. ٭Significantly different post-LIST (P < .05).
decrease in eccentric hamstrings to concentric quadriceps torque ratio (ASHecc:Qcon) at 10° of knee flexion, but not at any other angle. These changes were associated with large effect sizes. Confirming previous studies, we also found a significant decrease in the functional Hecc:Qcon ratio4–6 and a significant shift in APTeccH.12 Due to differences in isokinetic testing speeds, it is not possible to make direct comparisons with all of the relevant studies in the area. However, the 18.5% declines in Hecc at 120°/s concur with
the 16.8% to 17.5% previously reported at that speed after various protocols including a treadmill test reflecting the intensities of match play,4 the LIST,6 and a multidirectional soccer-specific aerobic field test (SAFT90).12 Similarly, the 12% decrease in Hecc:Qcon ratio compares with the 13% to 15% declines reported in these studies. The 11.7° shift in APTeccH partly confirms the work of Small et al,12 who observed a shift of 10.0° in the same direction in semipro players, but unlike the current study they also noted significant changes in
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Figure 5 — Angle of peak torque of eccentric hamstrings (eccH), concentric quadriceps (conQ), and concentric hamstrings (conH), before and after the Loughborough Intermittent Shuttle Test (LIST). ٭Significantly different post-LIST (P < .05).
Figure 6 — Peak torque of eccentric hamstrings (eccH), concentric quadriceps (conQ), and concentric hamstrings (conH) before and after the Loughborough Intermittent Shuttle Test (LIST). ٭Significantly difference from pre-LIST value (P < .01).
APTconH and APTconQ. The major difference in methodology was their use of the SAFT90; the greater mechanical demands associated with the more varied and frequent changes of direction of this protocol might therefore explain these differing outcomes. The lack of significant fatigue in Hcon and Qcon in the current study concurs with other studies in semiprofessional12 and professional soccer players.5 Our results show a selective deterioration of the force reduction and deceleration capabilities of the hamstrings in relation to the force-production capabilities of the quadriceps at a joint angle around which the hamstrings are highly vulnerable to strain injury.14 Moreover, the shift in APTeccH away from the more extended 7.1° to 18.8° is also predicted to increase susceptibility to damage and injury at longer lengths due to the greater likelihood of the muscle operating on the descending limb of the length–tension curve.21 Overall, the hamstrings could be characterized as more vulnerable to HSS related to eccentric overload. In addition, acute hamstrings fatigue leads to increased anterior tibial translation, indicative of reduced knee stability and increased vulnerability to ACL injury.11
Peak-torque ratios are derived from the highest torques produced within the range of motion for their respective contraction modes, yet peak torque occurs at substantially different angles; in the current study APTeccH and APTconQ occurred at 7° and 63.1°, respectively. Ayala et al14 argued that the functional interaction between the hamstrings and quadriceps in relation to HSS and ACL risk would be better represented by the assessment of HeccQcon torque ratios at specific joint angles (ASHecc:Qcon) and in particular near to full extension, a position where the hamstrings are highly vulnerable to strain13 and where ACL rupture is most likely to occur.14 This may explain why although there is evidence that a lower Hecc:Qcon ratio predicts HSSs,7,8 this is not an entirely consistent finding; a recent meta-analysis2 concluded that there was sparse evidence to support H:Q ratios as an HSS risk factor. Additional consideration of angle-specific ratios may improve the predictive value of screening14 by revealing interlimb imbalances in the torque-angle profile22 and in APT23 that are relevant to hamstring injury or reinjury. Brockett et al23 observed a significantly shorter APTconH (12.7°) in the previously injured limb of athletes compared with the healthy limb, but no significant difference in peak torque. Similarly, Sole et al22 found no significant interlimb difference in hamstring peak torque in athletes with previous HSS but did observe long-length interlimb torque deficits. While the 1 study that examined APT as a potential HSS risk factor, in sprinters, found no association,8 further research is warranted to determine the value of angle-specific torque ratios and/or interlimb deficits in APT in HSS-risk screening in soccer and other multiple-sprint sports. Theoretically, having higher longer-length strength reduces the likelihood that activity-induced fatigue will result in a decline in the force-absorption capabilities of the hamstrings to a point at which vulnerability to HSS injury is increased. However, since force decline is more a function of a muscle’s fatigue resistance than its capacity for maximal force production,24 our findings support the suggestion that evaluation of hamstrings strength-endurance25 would be of value from a risk-screening perspective. Indeed, it was recently reported that poor performance in a test of hamstring strength-endurance25 was associated with increased risk of HSS in Australian rules footballers.26 Morgan and Proske21 demonstrated that eccentric hamstrings training leads to a shift in the APT to a longer length. This adaptation protects sarcomeres from overstretch, damage, and injury at longer lengths21,23 and may contribute to the reduced HSS incidence reported after eccentric-emphasis hamstrings training.9 In the current study, eccentric strength was highest at the joint angle closest to full extension; both pre- and post-LIST, eccentric hamstrings torque and ASHecc:Qcon were significantly higher at 10° than at all other angles tested, but fatigue was also greatest at this angle. These findings imply support both for an emphasis on long-length eccentric hamstrings strength15,16,23 and for the development of hamstrings strength-endurance1,25–28 in HSS-prevention programs. To our knowledge, the only prospective injury study of endurance/fatigue emphasizing hamstrings conditioning involved Australian rules footballers and did observe lower HSS incidence after a preseason intervention.27 HSS-prevention studies have otherwise evaluated programs designed to develop maximum eccentric hamstrings strength, typically comprising sets of 5 repetitions progressing to sets of 8 to 12 repetitions.9 In contrast, higher repetition ranges and short interset recovery are cited as key loading variables to optimally stimulate the physiological adaptations such as capillary number/density and buffer capacity that support local muscle endurance.29,30 We previously reported a good correlation between blood
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lactate and Hecc:Qcon decline in the LIST (r = .705),6 suggesting that the hamstrings may be more susceptible to disturbances in pH than the quadriceps. Consequently, promoting physiological adaptations that reduce pH disturbances could also attenuate the decline in hamstrings strength associated with high-intensity activity. While hamstrings muscle-endurance interventions are lacking, Small et al28 did report that semipro soccer players who underwent 8 weeks of eccentric strength training in a fatigued state (after a soccer training session) showed significant attenuation had significantly attenuated time-dependent declines in eccentric peak torque and Hecc:Qcon during the SAFT90. Players who performed the same intervention in a nonfatigued state significantly increased their eccentric peak torque and Hecc:Qcon but showed no reduction in the decline in these variables during the SAFT90. This study clearly demonstrates differential strength and strength-endurance adaptations and highlights the importance of understanding the appropriate loading variables to promote the optimal development of both aspects of muscle performance, particularly in light of a recent prospective injury study implicating lower hamstring strength-endurance as an HSS risk factor.26 Further research should investigate the potential for strength-endurance-emphasis hamstring conditioning to attenuate the deterioration of hamstrings strength during high-intensity activity. The evaluation of the impact on injury incidence of these programs and of those that emphasize long-length eccentric loading of the hamstrings is also warranted. The sample size and the protocol used represent 2 of the principal limitations of the current study. In evaluating only 9 players, we may not have had sufficient statistical power to detect significant changes in torque and torque ratios at angles other than 10°. Another limitation is the simulated soccer field test used to induce fatigue. Although the LIST protocol reflects the activity pattern of match play,19 it lacks activities such as kicking, jumping, and multidirectional movements that characterize match play and would be expected to influence the profile of neuromuscular fatigue. Despite these limitations, the pattern of changes we observed was very similar to that previously reported with larger sample sizes and using the more soccer-specific SAFT90.12 Evaluation of changes in torque-angle relationships may also be made more specific to the length–tension relationships in relevant phases of the sprint cycle by assessment of isokinetic strength in the prone rather than in the seated position.14
Practical Implications Simulated soccer activity produces a selective decrease in hamstrings eccentric strength and strength balance relative to the quadriceps close to a joint angle at which the hamstrings are highly vulnerable to injury due to eccentric overload. Injury-risk screening might therefore be enhanced by not only evaluating hamstringto-quadriceps peak-torque ratios but also assessing angle-specific hamstrings torque:torque ratios and hamstrings strength-endurance. These findings also suggest that HSS-prevention programs for soccer players and other multiple-sprint sport athletes should include both exercises that specifically strengthen the hamstrings eccentrically at long lengths15,16,23 to ensure adequate angle-specific eccentric hamstrings strength and conditioning to promote hamstrings strength-endurance1,25–28 to minimize high-intensity-activityinduced strength decline, particularly at long lengths. Given that hamstrings fatigue has been shown reduce mechanical stability at the knee and increase the vulnerability of ACL to rupture11 and this injury often occurs when the limb is close to full extension,14
these types of hamstring loading may also be beneficial in terms of ACL risk reduction.
Conclusions The current study shows selective decrements in hamstrings strength and hamstrings-quadriceps strength balance at an angle close to full extension after soccer-specific activity and a shift in the eccentric hamstrings angle of peak torque to a less extended position. These changes may mechanistically contribute to fatigue-related increases in HSS and ACL-injury incidence in multiple-sprint sports. Acknowledgments The authors would like to thank the players who participated in the study.
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22. Sole G, Milosavljevic S, Nicholson HD, et al. Selective strength loss and decreased muscle activity in hamstring injury. J Orthop Sports Phys Ther. 2011;41(5):354–363. PubMed doi:10.2519/ jospt.2011.3268 23. Brockett CL, Morgan DL, Proske U. Predicting hamstring strain injury in elite athletes. Med Sci Sports Exerc. 2004;36(3):379–387. PubMed doi:10.1249/01.MSS.0000117165.75832.05 24. Jacobs C, Uhl TL, Seeley M, et al. Strength and fatigability of the dominant and nondominant hip abductors. J Athl Train. 2005;40(3):203– 206. PubMed 25. Sangnier S, Tourny-Chollet C. Comparison of the decrease in strength between hamstrings and quadriceps during isokinetic fatigue testing in semiprofessional soccer players. Int J Sports Med. 2007;28(11):952– 957. PubMed doi:10.1055/s-2007-964981 26. Freckleton G, Cook J, Pizzari T. The predictive validity of a single leg bridge test for hamstring injuries in Australian rules football players. Br J Sports Med. 2014;48(8):713–717. PubMed doi:10.1136/ bjsports-2013-092356 27. Verrall GM, Slavotinek JP, Barnes PG. The effect of sports specific training on reducing the incidence of hamstring injuries in professional Australian Rules football players. Br J Sports Med. 2005;39(6):363– 368. PubMed doi:10.1136/bjsm.2005.018697 28. 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 doi:10.1519/JSC.0b013e318194df5c 29. Campos GE, Luecke TJ, Wendeln HK, et al. Muscular adaptations in response to three different resistance-training regimens: specificity of repetition maximum training zones. Eur J Appl Physiol. 2002;88(12):50–60. PubMed doi:10.1007/s00421-002-0681-6 30. Kraemer WJ, Ratamess NAJ, Staron RS. Fundamentals of resistance training: progression and exercise prescription. Med Sci Sports Exerc. 2004;36(4):674–688. PubMed doi:10.1249/01. MSS.0000121945.36635.61
www.IJSPP-Journal.com ORIGINAL INVESTIGATION
Angle-Specific Eccentric Hamstring Fatigue After Simulated Soccer Daniel D. Cohen, Bingnan Zhao, Brian Okwera, Martyn J. Matthews, and Anne Delextrat Purpose: To evaluate the effect of simulated soccer on the hamstrings eccentric torque-angle profile and angle of peak torque (APTeccH), and on the hamstrings:quadriceps torque ratio at specific joint angles (ASHecc:Qcon). Methods: The authors assessed dominant-limb isokinetic concentric and eccentric knee flexion and concentric knee extension at 120°/s in 9 semiprofessional male soccer players immediately before and after they completed the Loughborough Intermittent Shuttle Test (LIST). Results: The LIST resulted in significant decreases in eccentric hamstrings torque at 60°, 50°, and 10° and a significant (21.8%) decrease in ASHecc:Qcon at 10° (P < .05). APTeccH increased from 7.1° ± 1.0° to 18.8° ± 4.2° (P < .05). Eccentric hamstrings peak torque significantly declined from 185.1 ± 70.4 N·m pre-LIST to 150.9 ± 58.5 N·m post-LIST (P = .002), but there were no significant changes in hamstrings or quadriceps concentric peak torque (P = .312, .169, respectively). Conclusions: Simulated soccer results in a selective loss of eccentric hamstrings torque and hamstrings-to-quadriceps muscle balance at an extended joint position and a shift in the eccentric hamstrings APT to a shorter length, changes that could increase vulnerability to hamstrings injury. These findings suggest that injury-risk screening could be improved by evaluating the eccentric hamstrings torque-angle profile and hamstrings strength-endurance and that the development of hamstrings fatigue resistance and long-length eccentric strength may reduce injury incidence. Keywords: injury-risk screening, strength imbalance, eccentric strength, muscle fatigue, isokinetic testing Hamstrings strains (HSSs) are the most common injury in professional soccer1 and other multiple-sprint sports.2 There is therefore considerable interest in addressing and where possible managing the multiple etiological factors that interact to determine risk.2,3 As risk factors that are potentially modifiable with training, muscle strength, fatigue, and the interaction between the 2 have received considerable attention in the sports-medicine literature.4–6 Inadequate hamstrings strength, in particular in the eccentric mode, or a low ratio of hamstrings to quadriceps strength is associated with increased HSS risk,7,8 and there is evidence that eccentric-emphasis strength training can reduce HSS incidence in soccer players. Accordingly, isokinetic assessment of the “conventional” peak-torque Hconcentric:Qconcentric ratio or of the “functional” peak-torque Heccentric:Qconcentric ratio is used in preseason injury-risk screening and in secondary HSS-prevention programs in professional soccer. Muscle fatigue is thought to explain epidemiological findings such as higher injury incidence in competitive match play compared with training,1 higher incidence in the latter part of the first and second halves of competitive soccer compared with the earlier parts of the game,1 and higher incidence in Australian rules footballers who were rotated less frequently than those who accumulated more rest within a game.10 Furthermore, hamstrings Cohen is with the Masira Institute, Faculty of Life Sciences, University of Santander (UDES), Bucaramanga, Colombia. Zhao and Okwera are with the Faculty of Life Sciences, London Metropolitan University, London, UK. Matthews is with the School of Health Sciences, Salford University, Salford, UK. Delextrat is with the Faculty of Sport and Health Sciences, Oxford Brookes University, Oxford, UK. Address author correspondence to Daniel Cohen at [email protected].
fatigue is associated with poorer mechanical knee stability, which may increase the risk of anterior cruciate ligament (ACL) injury.11 To better understand interactions between fatigue, strength, and vulnerability to injury during match play, studies have evaluated changes in muscle strength after protocols designed to simulate the metabolic demands of competition. The most consistent finding of these studies is a greater decline in eccentric hamstrings than concentric quadriceps peak torque, resulting in decreases of 16% to 26% in the Hecc:Qcon ratio.5,6,12 HSSs most commonly occur during high-speed running,1 with the hamstrings particularly vulnerable to damage and injury during the late swing phase, when the leg is extended and they are required to eccentrically contract to counteract the large torque generated by concentric quadriceps contraction.13 On this basis, it is argued that there should be specific emphasis on the evaluation and/or conditioning of hamstrings strength at longer muscle lengths, rather than on peak hamstrings strength per se.14–16 Accordingly, characterizing angle-specific strength changes after multiple-sprint activity may also help elucidate strength-fatigue-injury interactions and inform screening and prevention protocols. The main aims of the current study were to investigate the effects of simulated soccer activity on the eccentric hamstrings torque-angle profile and angle of peak torque (APT) and on the angle-specific ratios of eccentric hamstrings to concentric quadriceps (ASHecc:Qcon).
Methods Subjects Nine male soccer players (age 25.3 ± 0.8 y, height 178.8 ± 2.9 cm, body mass 77.0 ± 3.7 kg) were recruited as volunteers from
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semiprofessional soccer clubs in London, England. Players participated in 2 × 2-hour training sessions and two 90-minute matches per week. Those with any knee or thigh-muscle injuries in the past year were excluded. Participants were questioned about their general health history and informed of all the testing procedures in detail, and they gave written consent before data collection. Ethical approval for the project was given by the London Metropolitan University research ethics committee.
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Design Participants were tested on 2 separate occasions 1 week apart, for preliminary and main testing sessions, respectively. In the preliminary session, participants had an isokinetic familiarization session and performed the Multistage Fitness Test.17 After a standardized warm-up, subjects performed an isokinetic assessment of hamstrings and quadriceps peak torques with the dominant leg (defined as the leg used to kick a ball). This was immediately followed by a 90-minute simulated soccer activity: the Loughborough Intermittent Shuttle Test (LIST).18 After the LIST, participants repeated the isokinetic tests. The time between the completion of the LIST and the start of the post-LIST measurement was approximately 3 minutes. Players were asked to refrain from consuming any caffeine or alcohol for 2 hours before each session.
Methodology Participants performed the Multistage Fitness Test, which consists of running between 2 cones placed 20 m apart at a progressively increasing speed controlled by audio bleeps. The test has good reliability (r = .975) and validity (r = .87–.92) for the estimation of maximal aerobic capacity (VO2max).17 To ensure that players performed with maximal effort, a minimum of 2 players performed the test at the same time. The final level reached during the test was used to estimate VO2max and the running speed corresponding to 55% and 95% of maximal aerobic speed, required for the LIST protocol. The LIST18 consists of periods of walking, jogging, running, and sprinting based on the activity profile of football in terms of time, running patterns, and physiological and metabolic responses during soccer games and has good test–retest reliability; it is described in detail elsewhere.6,18 Before the pre-LIST test, participants performed a supervised 10-minute warm-up on a cycle ergometer (Monark 864, Varberg, Sweden) at 70 W, followed by 2 sets of 30-second static stretches for the hamstrings and quadriceps. They were then seated on the isokinetic dynamometer (HUMAC NORM, Computer Sports Medicine International, Stoughton, MA, USA), and adjustable segments of the dynamometer were set according to the participant’s body dimensions. Players performed 2 tests of 5 maximal repetitions at 120°/s with a 2-minute recovery period between and were encouraged to provide maximal effort for all repetitions of the maximal tests. Just before the maximal test, players performed 3 submaximal trials. Only the 5 maximal contractions in each mode were recorded, and the repetition with the highest peak torque was selected for further analysis. Concentric/eccentric extension and flexion were assessed in random order pre-LIST, with that order then repeated in the test that immediately followed the LIST. Gravity correction was selected for all tests. Isokinetic testing is characterized by a good test–retest reliability (intraclass correlation coefficient >.80) for the measurement of
hamstrings-to-quadriceps strength ratios and has been widely used to assess the strength of soccer players19; the angular velocity was 120°/s, used in a number of similar studies.4,6,12 The following isokinetic parameters were determined pre- and post-LIST. Peak values: • Peak torque (PT) of the concentric hamstrings (PT-Hcon), eccentric hamstrings (PT-Hecc), and concentric quadriceps (PT-Qcon). • The functional ratio (Hecc:Qcon), calculated as eccentric hamstrings PT:concentric quadriceps PT. • Angle of PT for hamstrings concentric (APTconH) and eccentric (APTeccH) and quadriceps concentric (APTconQ). Angle-specific values: • Eccentric hamstrings and concentric quadriceps torque at 10°, 20°, 30°, 40°, 50°, 60°, 70°, 80°, and 90°. • Angle-specific hamstrings:quadriceps torque ratios (ASHeccQcon), for angles 10° to 90°, calculated as Hecc torque/Qcon torque at each angle.
Statistical Analysis Statistical analysis was performed using SPSS statistical software (version 19.0). Mean ± SD were calculated for each dependent variable. The parametric nature of the data was checked by the Shapiro-Wilk test. A Student t-test for paired samples was applied to compare peak values. In addition, an analysis of variance (ANOVA) with repeated measures was used to test the effect of angle (0–90°) and fatigue (pre vs post) on angle-specific torques and ASHecc:Qcon. Post hoc t-tests were performed to determine where differences lay. Effect sizes were calculated using Cohen d and partial eta squared (ηP2) and interpreted as small (>0.1), medium (>0.3), and large (>0.5).20 Significance was set at P < .05.
Results Subjects’ estimated VO2max was 49.4 ± 4.2 mL · kg–1 · min–1, and their maximal aerobic speed averaged 12.7 ± 0.6 km/h. Figure 1 shows pre- and post-LIST eccentric hamstrings torques at 9 knee-flexion angles. The statistical analysis revealed significant main effects of angle (P = .001, ηP2 = .638) and fatigue (P = .039, ηP2 = .432) and an interaction between these factors (P = .010, ηP2 = .261). Torques tended to be lower after the LIST, and significant effects were observed in Hecc at 90° (P = .022, d = 2.3), 60° (P = .019, d = 1.57), 50° (P = .035, d = 1.37), and 10° of knee flexion (P = .006, d = 2.18). There were no significant decreases in Qcon or Hcon at any angle (Figures 2 and 3, respectively). Figure 4 shows pre- and post-LIST values for ASHecc:Qcon at 9 knee-flexion angles (ASHecc:Qcon). The ANOVA showed significant effects of angle (P = .001, ηP2 = .854) and fatigue (P = .030, ηP2 = .465 and an interaction between these factors (P = .003, ηP2 = .297). Subsequent analyses revealed a significant decrease in preversus post-LIST at 10° of knee flexion (P = .036) but not at any other angle tested. Pre-LIST ASHecc:Qcon at 10° of knee flexion was significantly higher than at the other 8 angles (P < .05, d = 2.06). Figure 5 shows angle-of-peak-torque (APT) values pre- and post-LIST. There was a significant (P = .025, d = 1.28) change in APTeccH from 7.1° ± 1.0° pre-LIST to 18.8° ± 4.2° post-LIST. Changes in the APTconH from 27.9° ± 2.8° pre-LIST to 27.8° ± 3.0°
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Figure 1 — Eccentric hamstrings torque at specific angles before and after the Loughborough Intermittent Shuttle Test (LIST). *Significantly different post-LIST (P < .05). **Significantly different post-LIST (P < .01).
Figure 2 — Concentric quadriceps torque at specific angles before and after the Loughborough Intermittent Shuttle Test.
and in the APTconQ from 63.1° ± 2.1° pre-LIST to 65.9° ± 2.2° postLIST were not significant (P = .954, 0.211, respectively). Pre-LIST, the APTeccH was significantly different from the APTconQ (P < .001, d = 4.60) and from APTconH (P = .004, d = 0.82). Figure 6 shows peak-torque values pre- and post-LIST. PT-Hecc significantly declined from 185.1 ± 70.4 N·m pre-LIST to 150.9 ± 58.5 N·m post-LIST (P = .002, d = 0.53). While PT-Qcon, declined from 166.6 ± 45.1 N·m pre-LIST to 155.0 ± 42.6 N·m post-LIST and PT-Hcon declined from 119.6 ± 24.2 N·m to 110.7 ± 27.9 N·m, these changes were not significant (P = .312, 0.169, respectively).
The Hecc:Qcon ratio significantly decreased from 1.11 pre-LIST to 0.98 post-LIST (P = .026, d = 0.60).
Discussion We evaluated angle-specific changes in hamstrings and quadriceps torque and torque ratios after the LIST simulated football protocol in semiprofessional male footballers. The novel findings of the study were that the LIST resulted in significant declines in hamstrings torque at 60°, 50°, and 10° and a significant 21.8%
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Figure 3 — Concentric hamstrings torque at specific angles before and after the Loughborough Intermittent Shuttle Test.
Figure 4 — Angle-specific eccentric hamstrings–to–concentric quadriceps ratios (ASHecc:Qcon) before and after the Loughborough Intermittent Shuttle Test (LIST) at specific angles. ٭Significantly different post-LIST (P < .05).
decrease in eccentric hamstrings to concentric quadriceps torque ratio (ASHecc:Qcon) at 10° of knee flexion, but not at any other angle. These changes were associated with large effect sizes. Confirming previous studies, we also found a significant decrease in the functional Hecc:Qcon ratio4–6 and a significant shift in APTeccH.12 Due to differences in isokinetic testing speeds, it is not possible to make direct comparisons with all of the relevant studies in the area. However, the 18.5% declines in Hecc at 120°/s concur with
the 16.8% to 17.5% previously reported at that speed after various protocols including a treadmill test reflecting the intensities of match play,4 the LIST,6 and a multidirectional soccer-specific aerobic field test (SAFT90).12 Similarly, the 12% decrease in Hecc:Qcon ratio compares with the 13% to 15% declines reported in these studies. The 11.7° shift in APTeccH partly confirms the work of Small et al,12 who observed a shift of 10.0° in the same direction in semipro players, but unlike the current study they also noted significant changes in
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Figure 5 — Angle of peak torque of eccentric hamstrings (eccH), concentric quadriceps (conQ), and concentric hamstrings (conH), before and after the Loughborough Intermittent Shuttle Test (LIST). ٭Significantly different post-LIST (P < .05).
Figure 6 — Peak torque of eccentric hamstrings (eccH), concentric quadriceps (conQ), and concentric hamstrings (conH) before and after the Loughborough Intermittent Shuttle Test (LIST). ٭Significantly difference from pre-LIST value (P < .01).
APTconH and APTconQ. The major difference in methodology was their use of the SAFT90; the greater mechanical demands associated with the more varied and frequent changes of direction of this protocol might therefore explain these differing outcomes. The lack of significant fatigue in Hcon and Qcon in the current study concurs with other studies in semiprofessional12 and professional soccer players.5 Our results show a selective deterioration of the force reduction and deceleration capabilities of the hamstrings in relation to the force-production capabilities of the quadriceps at a joint angle around which the hamstrings are highly vulnerable to strain injury.14 Moreover, the shift in APTeccH away from the more extended 7.1° to 18.8° is also predicted to increase susceptibility to damage and injury at longer lengths due to the greater likelihood of the muscle operating on the descending limb of the length–tension curve.21 Overall, the hamstrings could be characterized as more vulnerable to HSS related to eccentric overload. In addition, acute hamstrings fatigue leads to increased anterior tibial translation, indicative of reduced knee stability and increased vulnerability to ACL injury.11
Peak-torque ratios are derived from the highest torques produced within the range of motion for their respective contraction modes, yet peak torque occurs at substantially different angles; in the current study APTeccH and APTconQ occurred at 7° and 63.1°, respectively. Ayala et al14 argued that the functional interaction between the hamstrings and quadriceps in relation to HSS and ACL risk would be better represented by the assessment of HeccQcon torque ratios at specific joint angles (ASHecc:Qcon) and in particular near to full extension, a position where the hamstrings are highly vulnerable to strain13 and where ACL rupture is most likely to occur.14 This may explain why although there is evidence that a lower Hecc:Qcon ratio predicts HSSs,7,8 this is not an entirely consistent finding; a recent meta-analysis2 concluded that there was sparse evidence to support H:Q ratios as an HSS risk factor. Additional consideration of angle-specific ratios may improve the predictive value of screening14 by revealing interlimb imbalances in the torque-angle profile22 and in APT23 that are relevant to hamstring injury or reinjury. Brockett et al23 observed a significantly shorter APTconH (12.7°) in the previously injured limb of athletes compared with the healthy limb, but no significant difference in peak torque. Similarly, Sole et al22 found no significant interlimb difference in hamstring peak torque in athletes with previous HSS but did observe long-length interlimb torque deficits. While the 1 study that examined APT as a potential HSS risk factor, in sprinters, found no association,8 further research is warranted to determine the value of angle-specific torque ratios and/or interlimb deficits in APT in HSS-risk screening in soccer and other multiple-sprint sports. Theoretically, having higher longer-length strength reduces the likelihood that activity-induced fatigue will result in a decline in the force-absorption capabilities of the hamstrings to a point at which vulnerability to HSS injury is increased. However, since force decline is more a function of a muscle’s fatigue resistance than its capacity for maximal force production,24 our findings support the suggestion that evaluation of hamstrings strength-endurance25 would be of value from a risk-screening perspective. Indeed, it was recently reported that poor performance in a test of hamstring strength-endurance25 was associated with increased risk of HSS in Australian rules footballers.26 Morgan and Proske21 demonstrated that eccentric hamstrings training leads to a shift in the APT to a longer length. This adaptation protects sarcomeres from overstretch, damage, and injury at longer lengths21,23 and may contribute to the reduced HSS incidence reported after eccentric-emphasis hamstrings training.9 In the current study, eccentric strength was highest at the joint angle closest to full extension; both pre- and post-LIST, eccentric hamstrings torque and ASHecc:Qcon were significantly higher at 10° than at all other angles tested, but fatigue was also greatest at this angle. These findings imply support both for an emphasis on long-length eccentric hamstrings strength15,16,23 and for the development of hamstrings strength-endurance1,25–28 in HSS-prevention programs. To our knowledge, the only prospective injury study of endurance/fatigue emphasizing hamstrings conditioning involved Australian rules footballers and did observe lower HSS incidence after a preseason intervention.27 HSS-prevention studies have otherwise evaluated programs designed to develop maximum eccentric hamstrings strength, typically comprising sets of 5 repetitions progressing to sets of 8 to 12 repetitions.9 In contrast, higher repetition ranges and short interset recovery are cited as key loading variables to optimally stimulate the physiological adaptations such as capillary number/density and buffer capacity that support local muscle endurance.29,30 We previously reported a good correlation between blood
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lactate and Hecc:Qcon decline in the LIST (r = .705),6 suggesting that the hamstrings may be more susceptible to disturbances in pH than the quadriceps. Consequently, promoting physiological adaptations that reduce pH disturbances could also attenuate the decline in hamstrings strength associated with high-intensity activity. While hamstrings muscle-endurance interventions are lacking, Small et al28 did report that semipro soccer players who underwent 8 weeks of eccentric strength training in a fatigued state (after a soccer training session) showed significant attenuation had significantly attenuated time-dependent declines in eccentric peak torque and Hecc:Qcon during the SAFT90. Players who performed the same intervention in a nonfatigued state significantly increased their eccentric peak torque and Hecc:Qcon but showed no reduction in the decline in these variables during the SAFT90. This study clearly demonstrates differential strength and strength-endurance adaptations and highlights the importance of understanding the appropriate loading variables to promote the optimal development of both aspects of muscle performance, particularly in light of a recent prospective injury study implicating lower hamstring strength-endurance as an HSS risk factor.26 Further research should investigate the potential for strength-endurance-emphasis hamstring conditioning to attenuate the deterioration of hamstrings strength during high-intensity activity. The evaluation of the impact on injury incidence of these programs and of those that emphasize long-length eccentric loading of the hamstrings is also warranted. The sample size and the protocol used represent 2 of the principal limitations of the current study. In evaluating only 9 players, we may not have had sufficient statistical power to detect significant changes in torque and torque ratios at angles other than 10°. Another limitation is the simulated soccer field test used to induce fatigue. Although the LIST protocol reflects the activity pattern of match play,19 it lacks activities such as kicking, jumping, and multidirectional movements that characterize match play and would be expected to influence the profile of neuromuscular fatigue. Despite these limitations, the pattern of changes we observed was very similar to that previously reported with larger sample sizes and using the more soccer-specific SAFT90.12 Evaluation of changes in torque-angle relationships may also be made more specific to the length–tension relationships in relevant phases of the sprint cycle by assessment of isokinetic strength in the prone rather than in the seated position.14
Practical Implications Simulated soccer activity produces a selective decrease in hamstrings eccentric strength and strength balance relative to the quadriceps close to a joint angle at which the hamstrings are highly vulnerable to injury due to eccentric overload. Injury-risk screening might therefore be enhanced by not only evaluating hamstringto-quadriceps peak-torque ratios but also assessing angle-specific hamstrings torque:torque ratios and hamstrings strength-endurance. These findings also suggest that HSS-prevention programs for soccer players and other multiple-sprint sport athletes should include both exercises that specifically strengthen the hamstrings eccentrically at long lengths15,16,23 to ensure adequate angle-specific eccentric hamstrings strength and conditioning to promote hamstrings strength-endurance1,25–28 to minimize high-intensity-activityinduced strength decline, particularly at long lengths. Given that hamstrings fatigue has been shown reduce mechanical stability at the knee and increase the vulnerability of ACL to rupture11 and this injury often occurs when the limb is close to full extension,14
these types of hamstring loading may also be beneficial in terms of ACL risk reduction.
Conclusions The current study shows selective decrements in hamstrings strength and hamstrings-quadriceps strength balance at an angle close to full extension after soccer-specific activity and a shift in the eccentric hamstrings angle of peak torque to a less extended position. These changes may mechanistically contribute to fatigue-related increases in HSS and ACL-injury incidence in multiple-sprint sports. Acknowledgments The authors would like to thank the players who participated in the study.
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