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Open Access 18-06-2023 | Fatigue | Original Article

Effects of muscle fatigue on exercise-induced hamstring muscle damage: a three-armed randomized controlled trial

Authors: Carsten Schwiete, Christian Roth, Christoph Skutschik, Sebastian Möck, Lukas Rettenmaier, Kevin Happ, Holger Broich, Michael Behringer

Published in: European Journal of Applied Physiology | Issue 11/2023

Abstract

Purpose

Hamstring injuries in soccer reportedly increase towards the end of the matches’ halves as well as with increased match frequency in combination with short rest periods, possibly due to acute or residual fatigue. Therefore, this study aimed to investigate the effects of acute and residual muscle fatigue on exercise-induced hamstring muscle damage.

Methods

A three-armed randomized-controlled trial, including 24 resistance-trained males, was performed allocating subjects to either a training group with acute muscle fatigue + eccentric exercise (AF/ECC); residual muscle fatigue + eccentric exercise (RF/ECC) or a control group with only eccentric exercise (ECC). Muscle stiffness, thickness, contractility, peak torque, range of motion, pain perception, and creatine kinase were assessed as muscle damage markers pre, post, 1 h post, and on the consecutive three days.

Results

Significant group × time interactions were revealed for muscle thickness (p = 0.02) and muscle contractility parameters radial displacement (D_m) and contraction velocity (V_c) (both p = 0.01), with larger changes in the ECC group (partial η² = 0.4). Peak torque dropped by an average of 22% in all groups; stiffness only changed in the RF/ECC group (p = 0.04). Muscle work during the damage protocol was lower for AF/ECC than for ECC and RF/ECC (p = 0.005).

Conclusion

Hamstring muscle damage was comparable between the three groups. However, the AF/ECC group resulted in the same amount of muscle damage while accumulating significantly less muscle work during the protocol of the damage exercise.

Trial registration

This study was preregistered in the international trial registration platform (WHO; registration number: DRKS00025243).

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Abdel-aziem AA, Soliman ES, Abdelraouf OR (2018) Isokinetic peak torque and flexibility changes of the hamstring muscles after eccentric training: trained versus untrained subjects. Acta Orthop Traumatol Turc 52(4):308–314. https://doi.org/10.1016/j.aott.2018.05.003 CrossRefPubMedCentralPubMed

Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88(1):287–332. https://doi.org/10.1152/physrev.00015.2007 CrossRefPubMed

Andonian P, Viallon M, Le Goff C, de Bourguignon C, Tourel C, Morel J, Giardini G, Gergelé L, Millet GP, Croisille P (2016) Shear-wave elastography assessments of quadriceps stiffness changes prior to, during and after prolonged exercise: a longitudinal study during an extreme mountain ultra-marathon. PLoS One 11(8):e0161855. https://doi.org/10.1371/journal.pone.0161855 CrossRefPubMedCentralPubMed

Askling CM, Tengvar M, Saartok T, Thorstensson A (2007) Acute first-time hamstring strains during high-speed running: a longitudinal study including clinical and magnetic resonance imaging findings. Am J Sports Med 35(2):197–206. https://doi.org/10.1177/0363546506294679 CrossRefPubMed

Avrillon S, Lacourpaille L, Hug F, Le Sant G, Frey A, Nordez A, Guilhem G (2020) Hamstring muscle elasticity differs in specialized high-performance athletes. Scand J Med Sci Sports 30(1):83–91. https://doi.org/10.1111/sms.13564

Behringer M, Montag J, Franz A, McCourt ML, Mester J, Nosaka K (2014) Exhaustive exercise—a near death experience for skeletal muscle cells? Med Hypotheses 83(6):758–765. https://doi.org/10.1016/j.mehy.2014.10.005 CrossRefPubMed

Bengtsson H, Ekstrand J, Hägglund M (2013) Muscle injury rates in professional football increase with fixture congestion: an 11-year follow-up of the UEFA Champions League injury study. Br J Sports Med 47(12):743–747. https://doi.org/10.1136/bjsports-2013-092383 CrossRefPubMed

Brancaccio P, Maffulli N, Buonauro R, Limongelli FM (2008) Serum enzyme monitoring in sports medicine. Clin Sports Med 27(1):1–18. https://doi.org/10.1016/j.csm.2007.09.005 CrossRefPubMed

Brusco CM, Blazevich AJ, Radaelli R, Botton CE, Cadore EL, Baroni BM, Trajano GS, Pinto RS (2018) The effects of flexibility training on exercise-induced muscle damage in young men with limited hamstrings flexibility. Scand J Med Sci Sports 28(6):1671–1680. https://doi.org/10.1111/sms.13068 CrossRefPubMed

Cè E, Longo S, Limonta E, Coratella G, Rampichini S, Esposito F (2020) Peripheral fatigue: new mechanistic insights from recent technologies. Eur J Appl Physiol 120(1):17–39. https://doi.org/10.1007/s00421-019-04264-w CrossRefPubMed

Chapman D, Newton M, Sacco P, Nosaka K (2006) Greater muscle damage induced by fast versus slow velocity eccentric exercise. Int J Sports Med 27(8):591–598. https://doi.org/10.1055/s-2005-865920 CrossRefPubMed

Chapman D, Newton M, Zainuddin Z, Sacco P, Nosaka K (2008) Work and peak torque during eccentric exercise do not predict changes in markers of muscle damage. Br J Sports Med 42(7):585–591. https://doi.org/10.1136/bjsm.2007.037929 CrossRefPubMed

Chebbi S, Chamari K, Van Dyk N, Gabbett T, Tabben M (2020) Hamstring injury prevention for elite soccer players: a real-world prevention program showing the effect of players’ compliance on the outcome. J Strength Cond Res 36(5):1383–1388. https://doi.org/10.1519/JSC.0000000000003505 CrossRefPubMed

Cheung K, Hume PA, Maxwell L (2003) Delayed onset muscle soreness: treatment strategies and performance factors. Sports Med 33(2):145–164. https://doi.org/10.2165/00007256-200333020-00005 CrossRefPubMed

Clarkson PM, Hubal MJ (2002) Exercise-induced muscle damage in humans. Am J Phys Med Rehabil 81:52–69. https://doi.org/10.1097/00002060-200211001-00007 CrossRef

Cohen DD, Zhao B, Okwera B, Matthews MJ, Delextrat A (2015) Angle-specific eccentric hamstring fatigue after simulated soccer. Int J Sports Physiol Perform 10(3):325–331. https://doi.org/10.1123/ijspp.2014-0088 CrossRefPubMed

Coratella G, Bellin G, Beato M, Schena F (2015) Fatigue affects peak joint torque angle in hamstrings but not in quadriceps. J Sports Sci 33(12):1276–1282. https://doi.org/10.1080/02640414.2014.986185 CrossRefPubMed

Costa PB, Ruas CV, Smith CM (2018) Effects of stretching and fatigue on peak torque, muscle imbalance, and stability. J Sports Med Phys Fit 58(7):957–965. https://doi.org/10.23736/S0022-4707.17.07072-4 CrossRef

De Lima LC, Bueno Junior CR, de Oliveira Assumpção C, de Menezes Bassan N, Barreto RV, Cardozo AC, Greco CC, Denadai BS (2021) The impact of ACTN3 gene polymorphisms on susceptibility to exercise-induced muscle damage and changes in running economy following downhill running. Front Physiol 12:769971. https://doi.org/10.3389/fphys.2021.769971 CrossRefPubMedCentralPubMed

Dirnberger J, Wiesinger HP, Kösters A, Müller E (2012) Reproducibility for isometric and isokinetic maximum knee flexion and extension measurements using the IsoMed 2000-dynamometer. Isokinet Exerc Sci 20(3):149–153. https://doi.org/10.3233/IES-2012-0451 CrossRef

Ekstrand J, Hagglund M, Walden M (2009) Injury incidence and injury patterns in professional football: the UEFA injury study. Br J Sports Med 45(7):553–558. https://doi.org/10.1136/bjsm.2009.060582 CrossRefPubMed

Ekstrand J, Hägglund M, Waldén M (2011) Epidemiology of muscle injuries in professional football (Soccer). Am J Sports Med 39(6):1226–1232. https://doi.org/10.1177/0363546510395879 CrossRefPubMed

Ekstrand J, Spreco A, Bengtsson H, Bahr R (2021) Injury rates decreased in men’s professional football: an 18-year prospective cohort study of almost 12 000 injuries sustained during 1.8 million hours of play. Br J Sports Med 55(19):1084–1092. https://doi.org/10.1136/bjsports-2020-103159 CrossRefPubMed

Ekstrand J, Ueblacker P, Van Zoest W, Verheijen R, Vanhecke B, van Wijk M, Bengtsson H (2023) Risk factors for hamstring muscle injury in male elite football: medical expert experience and conclusions from 15 European Champions League clubs. BMJ Open Sport Exerc Med 9(1):e001461. https://doi.org/10.1136/bmjsem-2022-001461

Gleeson N, Eston R, Marginson V, McHugh M (2003) Effects of prior concentric training on eccentric exercise induced muscle damage. Br J Sports Med 37:119–125. https://doi.org/10.1136/bjsm.37.2.119 CrossRefPubMedCentralPubMed

Hader K, Rumpf MC, Hertzog M, Kilduff LP, Girard O, Silva JR (2019) Monitoring the athlete match response: can external load variables predict post-match acute and residual fatigue in soccer? A systematic review with meta-analysis. Sports Med Open 5(1):48. https://doi.org/10.1186/s40798-019-0219-7 CrossRefPubMedCentralPubMed

Hägglund M, Waldén M, Ekstrand J (2013) Risk factors for lower extremity muscle injury in professional soccer: the UEFA injury study. Am J Sports Med 41(2):327–335. https://doi.org/10.1177/0363546512470634 CrossRefPubMed

Harmsen JF, Franz A, Mayer C, Zilkens C, Buhren BA, Schrumpf H, Krauspe R, Behringer M (2018) Tensiomyography parameters and serum biomarkers after eccentric exercise of the elbow flexors. Eur J Appl Physiol 119(2):455–464. https://doi.org/10.1007/s00421-018-4043-4 CrossRefPubMed

Heller GZ, Manuguerra M, Chow R (2016) How to analyze the visual analogue scale: myths, truths and clinical relevance. Scand J Pain 13(1):67–75. https://doi.org/10.1016/j.sjpain.2016.06.012 CrossRefPubMed

Kakavas G, Malliaropoulos N, Kaliakmanis A, Georgios B, Maffulli N (2020) A ninety-minute football match increases hamstring flexibility in professional players. J Biol Regul Homeost Agents 34(5):87–92. https://doi.org/10.13140/RG.2.2.12949.24807 CrossRefPubMed

Kawama R, Yanase K, Hojo T, Wakahara T (2022) Acute changes in passive stiffness of the individual hamstring muscles induced by resistance exercise: effects of contraction mode and range of motion. Eur J Appl Physiol 122(9):2071–2083. https://doi.org/10.1007/s00421-022-04976-6

Kisilewicz A, Madeleine P, Ignasiak Z, Ciszek B, Kawczynski A, Larsen RG (2020) Eccentric exercise reduces upper trapezius muscle stiffness assessed by shear wave elastography and myotonometry. Front Bioeng Biotechnol 8:928. https://doi.org/10.3389/fbioe.2020.00928 CrossRefPubMedCentralPubMed

Koch AJ, Pereira R, Machado M (2014) The creatine kinase response to resistance exercise. J Musculoskelet Neuronal Interact 14(1):68–77 PubMed

Kozinc Ž, Šarabon N (2020) Shear-wave elastography for assessment of trapezius muscle stiffness: reliability and association with low-level muscle activity. PLoS One 15(6):e0234359. https://doi.org/10.1371/journal.pone.0234359 CrossRefPubMedCentralPubMed

Lacourpaille L, Nordez A, Hug F, Doguet V, Andrade R, Guilhem G (2017) Early detection of exercise-induced muscle damage using elastography. Eur J Appl Physiol 117(10):2047–2056. https://doi.org/10.1007/s00421-017-3695-9 CrossRefPubMed

Leung WK, Chu K, Lai C (2017) Sonographic evaluation of the immediate effects of eccentric heel drop exercise on Achilles tendon and gastrocnemius muscle stiffness using shear wave elastography. PeerJ 5:e3592. https://doi.org/10.7717/peerj.3592 CrossRefPubMedCentralPubMed

Maeo S, Saito A, Otsuka S, Shan X, Kanehisa H, Kawakami Y (2018) Localization of muscle damage within the quadriceps femoris induced by different types of eccentric exercises. Scand J Med Sci Sports 28(1):95–106. https://doi.org/10.1111/sms.12880 CrossRefPubMed

Mair SD, Seaber AV, Glisson RR, Garrett WE (1996) The role of fatigue in susceptibility to acute muscle strain injury. Am J Sports Med 24(2):137–143. https://doi.org/10.1177/036354659602400203 CrossRefPubMed

Markus I, Constantini K, Hoffman JR, Bartolomei S, Gepner Y (2021) Exercise-induced muscle damage: mechanism, assessment and nutritional factors to accelerate recovery. Eur J Appl Physiol 121(4):969–992. https://doi.org/10.1007/s00421-020-04566-4 CrossRefPubMed

Mueller-Wohlfahrt HW, Haensel L, Mithoefer K, Ekstrand J, English B, McNally S, Orchard J, van Dijk CN, Kerkhoffs GM, Schamasch P, Blottner D, Swaerd L, Goedhart E, Ueblacker P (2013) Terminology and classification of muscle injuries in sport: the Munich consensus statement. Br J Sports Med 47(6):342–350. https://doi.org/10.1136/bjsports-2012-091448 CrossRefPubMed

Nakamura M, Hasegawa S, Umegaki H, Nishishita S, Kobayashi T, Fujita K, Tanaka H, Ibuki S, Ichihashi N (2016) The difference in passive tension applied to the muscles composing the hamstrings—comparison among muscles using ultrasound shear wave elastography. Manual Ther 24:1–6. https://doi.org/10.1016/j.math.2016.03.012

Nosaka K, Clarkson PM (1997) Influence of previous concentric exercise on eccentric exercise-induced muscle damage. J Sports Sci 15(5):477–483. https://doi.org/10.1080/026404197367119 CrossRefPubMed

Piqueras-Sanchiz F, Martín-Rodríguez S, Pareja-Blanco F, Baraja-Vegas L, Blázquez-Fernández J, Bautista IJ, García-García Ó (2020) Mechanomyographic measures of muscle contractile properties are influenced by electrode size and stimulation pulse duration. Sci Rep 10(1):8192. https://doi.org/10.1038/s41598-020-65111-z CrossRefPubMedCentralPubMed

Roth C, Rettenmaier L, Behringer M (2021) High-protein energy-restriction: effects on body composition, contractile properties, mood, and sleep in active young college students. Front Sports Active Living 3:683327. https://doi.org/10.3389/fspor.2021.683327 CrossRef

Ryu J, Jeong WK (2017) Current status of musculoskeletal application of shear wave elastography. Ultrasonography 36(3):185–197. https://doi.org/10.14366/usg.16053 CrossRefPubMedCentralPubMed

Saenz A, Avellanet M, Hijos E, Chaler J, Garreta R, Pujol E, Sandoval B, Buen C, Farrensy A (2010) Knee isokinetic test-retest: a multicentre knee isokinetic test-retest study of a fatigue protocol. Eur J Phys Rehabil Med 46(1):81–88 PubMed

Sanz A, Pablos C, Ballester R, Sánchez-Alarcos JV, Huertas F (2020) Range of motion and injury occurrence in elite Spanish soccer academies. Not only a hamstring shortening—related problem. J Strength Cond Res 34(7):1924–1932. https://doi.org/10.1519/JSC.0000000000003302 CrossRefPubMed

Schwiete C, Franz A, Roth C, Behringer M (2021) Effects of resting vs. continuous blood-flow restriction-training on strength, fatigue resistance, muscle thickness, and perceived discomfort. Front Physiol 12:663665. https://doi.org/10.3389/fphys.2021.663665 CrossRefPubMedCentralPubMed

Silva JR, Rumpf MC, Hertzog M, Castagna C, Farooq A, Girard O, Hader K (2018) Acute and residual soccer match-related fatigue: a systematic review and meta-analysis. Sports Med 48(3):539–583. https://doi.org/10.1007/s40279-017-0798-8 CrossRefPubMed

Spiering B, Mujika I, Sharp M, Foulis S (2021) Maintaining physical performance: the minimal dose of exercise needed to preserve endurance and strength over time. J Strength Cond Res 35(5):1449–1458. https://doi.org/10.1519/JSC.0000000000003964 CrossRefPubMed

Vincent B, Windelinckx A, Nielens H, Ramaekers M, Leemputte MV, Hespel P, Thomis MA (2010) Protective role of alpha-actinin-3 in the response to an acute eccentric exercise bout. J Appl Physiol 109:564–573. https://doi.org/10.1152/japplphysiol.01007.2009 CrossRefPubMed

Voglar M, Vatovec R, Kozinc Ž, Šarabon N (2022) The effects of eccentric exercise on passive hamstring muscle stiffness: comparison of shear-wave elastography and passive knee torque outcomes. Eur J Transl Myology 32(2). https://doi.org/10.4081/ejtm.2022.10567

Wilmes E, de Ruiter CJ, Bastiaansen BJ, Goedhart EA, Brink MS, van der Helm FC, Savelsbergh GJ (2021) Associations between hamstring fatigue and sprint kinematics during a simulated football (soccer) match. Med Sci Sports Exerc 53(12):2586–2595. https://doi.org/10.1249/MSS.0000000000002753 CrossRefPubMedCentralPubMed

Wilson HV, Jones A, Johnson MI, Francis P (2019) The effect of inter-electrode distance on radial muscle displacement and contraction time of the biceps femoris, gastrocnemius medialis and biceps brachii, using tensiomyography in healthy participants. Physiol Meas 40(7):075007. https://doi.org/10.1088/1361-6579/ab1cef CrossRefPubMed

Wollin M, Thorborg K, Pizzari T (2017) The acute effect of match play on hamstring strength and lower limb flexibility in elite youth football players. Scand J Med Sci Sports 27(3):282–288. https://doi.org/10.1111/sms.12655 CrossRefPubMed

Xu J, Fu SN, Zhou D, Huang C, Hug F (2019) Relationship between pre-exercise muscle stiffness and muscle damage induced by eccentric exercise. Eur J Sport Sci 19(4):508–516. https://doi.org/10.1080/17461391.2018.1535625 CrossRefPubMed

Zhang Q, Léam A, Fouré A, Wong DP, Hautier CA (2021) Relationship between explosive strength capacity of the knee muscles and deceleration performance in female professional soccer players. Front Physiol 12:723041. https://doi.org/10.3389/fphys.2021.723041 CrossRefPubMedCentralPubMed

Title: Effects of muscle fatigue on exercise-induced hamstring muscle damage: a three-armed randomized controlled trial
Authors: Carsten Schwiete
Christian Roth
Christoph Skutschik
Sebastian Möck
Lukas Rettenmaier
Kevin Happ
Holger Broich
Michael Behringer
Publication date: 18-06-2023
Publisher: Springer Berlin Heidelberg
Keyword: Fatigue
Published in: European Journal of Applied Physiology / Issue 11/2023
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-023-05234-z

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Effects of muscle fatigue on exercise-induced hamstring muscle damage: a three-armed randomized controlled trial

Abstract

Purpose

Methods

Results

Conclusion

Trial registration

Keynote Webinar | Spotlight on Diet and Diabetes

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Trial registration

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